Skip to main content

Full text of "System of ophthalmology"

See other formats 


!.?;':'iiiK,M '  ''■:;iH(Kiii»iMs;'.' 


lilllll 


SYSTEM  OF  OPHTHALMOLOGY 


The  scheme  for  the  "System  of  Ophthalmology"  is  as  follows,  but  its 
division  into  different  volumes  is  liable  to  alteration. 

Vol.         I.     THE  EYE  IN  EVOLUTION 

Vol.       II.     THE  ANATOMY  OF  THE  VISUAL  SYSTEM 

Vol.     III.     NORMAL  AND  ABNORMAL  DEVELOPMENT 
Pt.    I.  Embryology 
Pt.  II.  Congenital  Deformities 

Vol.      IV.     THE  PHYSIOLOGY  OF  THE  EYE  AND  OF  VISION 

Vol.        V.     OPHTHALMIC  OPTICS  AND  REFRACTION 

Vol.      VI.     OCULAR  MOTILITY  AND  STRABISMUS 

Vol.    VII.     THE  FOUNDATIONS  OF  OPHTHALMOLOGY 

Heredity,  Pathology,  Methods  of  Diagnosis, 
General  Therapeutics 

Vol.  VIII.     DISEASES  OF  THE  OUTER  EYE 
Pt.    I.  Conjunctiva 
Pt.  II.  Cornea  and  Sclera 

Vol.      IX.     DISEASES  OF  THE  UVEAL  TRACT 

Vol.       X.     DISEASES  OF  THE  RETINA 

Vol.      XL     DISEASES  OF  THE  LENS  AND  VITREOUS; 
GLAUCOMA  AND  HYPOTONY 

Vol.    XII.     NEURO-OPHTHALMOLOGY 

Vol.  XIII.     THE  OCULAR  ADNEXAn 

Lids,    Lacrimal    Apparatus,    Orbit    and    Para- 
orbital  Structures 

Vol.  XIV.     INJURIES 

Vol.     XV.     INDEX  OF  GENERAL  AND  SYSTEMIC 
OPHTHALMOLOGY 


SYSTEM  OF  OPHTHALMOLOGY 

EDITED  BY 

SIR    STEWART   DUKE-ELDER 

G.C.V.O.,  M.A.,  LL.D.,  Ph.D.,  D.Sc,  M.D.,  D.M.,  F.R.C.S.,  F.R.C.S.E.,  F.A.C.S.,  F.R.A.C.S. 


VOL.  I 


THE  EYE  IN  EVOLUTION 

BY 

SIR  STEWART   DUKE-ELDER 


WITH  902  ILLUSTRATIONS,  15  COLOURED  PLATES 
AXD  3.')0  MARGINAL  ILLUSTRATIONS 


ST.  LOUIS 

THE  C.  V.  MOSBY  COMPANY 

1958 


@1958  by  Henry  Kimpton  Publishers, 

7  Leighton  Place, 

Leighton  Road, 

London  NWH 

All  rights  reserved.  No  part  of  this  publication  may 
be  reproduced,  stored  in  a  retrieval  system,  or  trans- 
mitted, in  any  form  or  by  any  means,  electronic, 
mechanical,  photocopying,  recording  or  otherwise, 
without  the  prior  permission  of  the  publishers. 


Reprinted  1970,  1976 


ISBN  0  85313  213  a 


MADE  AND  PRINTED  IN  GREAT  BRITAIN 


PREFACE 

The  reception  accorded  to  my  Textbook  of  Ophthalmology  has  per- 
suaded me  that  there  is  a  need  for  its  continuation  in  a  second  edition.  The 
seven  volumes  of  the  Textbook  took  almost  a  quarter  of  a  century  to  write, 
a  period  unfortunately  longer  than  it  might  have  been  owing  to  the  exigencies 
of  war.  The  first  four  volumes  have  long  been  out  of  print — and  inten- 
tionally so  because  they  have  long  been  out  of  date.  It  is  to  be  remembered 
that  the  second  volume  was  written  before  the  suljjhonamides  were  intro- 
duced ;  the  third  before  the  antibiotics  revolutionized  the  therapeutics  of 
infective  diseases  ;  both  of  them  before  the  role  of  viruses  in  ocular  disease 
was  adequately  appreciated  ;  the  physiology  of  the  eye  of  yesterday  is 
unrecognizable  when  compared  with  that  of  today  ;  even  the  anatomy  has 
been  transformed  by  more  elaborate  optical  and  chemical  methods  of 
investigation  and  the  advent  of  the  electron  microscope.  The  re-writing  of 
the  whole  work  if  its  com^^rehensive  nature  were  to  be  retained  would  be  an 
immense  task  occupying  more  time  than  I  could  reasonably  expect  to  have 
at  my  disposal.  Moreover,  tomorrow  ^^•ill  be  different  from  today,  and  if 
a  work  such  as  this  is  to  be  of  any  lasting  value  it  would  seem  to  me  desirable 
that  a  new  edition  be  published  at  least  every  fifteen  or  twenty  years  ; 
fortunately,  ophthalmology  is  no  static  science. 

It  therefore  seemed  to  me  wise  to  sliare  the  task  of  re-writing  the 
original  Textbook  with  my  colleagues  at  the  Institute  of  Ophthalmology  in 
London.  I  am  grateful  that  they  have  accepted  this  burden.  For  this 
reason  I  have  changed  the  name  of  the  book  to  a  ''System  of  Ophthalmology  " 
since  it  will  necessarih^  be  less  personal. 

This  first  volume  in  the  new  series  is  an  extension  of  the  first  twenty 
pages  of  Volume  I  of  the  old  Textbook  ;  this  I  have  %^Titten  myself,  largely 
because  it  is  a  subject  in  which  I  am  particularly  interested — and  I  wished 
to  write  it.  The  subject-matter  has  never  been  gathered  together  in  a  single 
book  before  and  it  is  my  hope  that  it  will  interest  ophthalmologists  in  so 
far  as  it  forms  the  basis  of  the  science  of  vision  ;  and  it  may  be  that  it  will  be 
of  value  also  to  those  whose  interest  is  biological  rather  than  clinical. ; 

The  numerous  marginal  sketches  are  not  usual  in  a  book  of  this  type. 
To  the  student  of  natural  history  they  may  seem  superfluous,  but  to  the 
ophthalmologist  some  of  the  animals  may  be  unfamiliar  and  the  drawings 
may  perchance  add  meaning  to  the  zoological  nomenclature  and  thus  give 
the  text  more  life  and  interest.  It  is  to  be  noted,  however,  that  they  are 
drawn  not  to  scale,  but  approximately  to  a  standard  size  to  fit  into  a  1-inch 
margin, 

Stewart  Duke-Elder. 

Institute  of  Ophthalmology, 

London, 

1957. 


ACKNOWLEDGEMENTS 

In  the  preparation  of  this  book  I  have  incurred  a  considerable  amount  of 
indebtedness  which  is  a  pleasure  to  record. 

Many  of  the  illustrations  are  borrowed,  and  in  each  the  source  is  acknowledged. 
There  are,  however,  five  sovirces  from  which  I  have  liberally  drawn,  and  these  merit 
special  thanks  :  Dr.  Gordon  Walls,  for  a  number  of  his  original  drawings  ;  Masson  et 
Cie  of  Paris,  who  have  allowed  me  to  use  some  illustrations  from  Rochon-Duvigneaud's 
classical  work,  Les  Yeux  et  la  Vision  des  Vertebris  ;  Dr.  Maurice  Burton  and  his 
publishers,  the  Elsevier  Publishing  Co.  of  Holland,  for  some  illustrations  from  The 
Story  of  Animal  Life  ;  the  Royal  Society  for  permission  to  iise  a  large  number  of 
Lindsay  Johnson's  illustrations  published  in  their  Proceedings  ;  and  Macmillan  &  Co. 
for  giving  free  permission  to  copy  a  large  number  of  the  illustrations  of  animals  in  the 
Cambridge  Natural  History  in  the  form  of  inarginal  sketches. 

In  preparing  the  illustrations  I  have  had  the  willing  co-operation  of  Dr.  Peter 
Hansen  and  the  Department  of  Medical  Illustration  of  the  Institute  of  Ophthalmology, 
the  assistance  of  which,  particularly  that  of  Mr.  T.  R.  Tarrant,  the  Medical  Artist,  has 
been  invaluable.  The  Zoological  Society  of  London  has  lent  me  a  number  of  photo- 
graphs, as  also  has  the  Natural  History  Museum  of  London,  together  with  specimens 
of  various  invertebrates.  Professor  Ida  Mann  has  allowed  me  to  use  a  large  number 
of  her  illustrations  of  the  eyes  of  animals,  and  Dr.  Kevin  O'Day  of  Melbourne  has 
allowed  me  to  use  photographs  and  slides  of  the  eyes  of  Monotremes  and  Marsupials 
which  are  unobtainable  outside  Australia  ;  while  in  this  Institute  Professor  Norman 
Ashton  and  Dr.  Katharine  Tansley  have  provided  me  with  sections  and  photographs 
of  the  eyes  of  a  number  of  animals. 

In  several  instances  my  knowledge  of  zoology  has  been  brought  up  to  date 
by  the  great  kindness  of  Dr.  Mary  Whitear  of  the  Zoology  Department  of  University 
College,  London,  who  has  read  the  proofs  of  those  sections  dealing  with  zoological 
classification  ;  while  Dr.  Katharine  Tansley  and  Dr.  Robert  Weale  of  this  Institute 
have  given  me  most  helpful  criticism  in  some  aspects  of  the  visual  problems  discussed. 
Miss  M.  H.  T.  Yuille,  Mr.  A.  J.  B.  Goldsmith  and  my  wife  have  shared  with  me  the 
onerous  task  of  proof-reading. 

It  is  difficult  for  me  to  express  my  indebtedness  to  my  secretary.  Miss  Rosamund 
Soley,  who  has  borne  much  of  the  burden  of  the  technical  aspects  of  the  production  of 
this  Volume.  She  has  typed  and  iDrejDared  the  manuscript,  corrected  the  proofs,  and 
undertaken  the  immense  and  somewhat  thankless  task  of  verifying  the  bibliographies, 
prepared  the  Zoological  Glossary  and  the  Index,  and  drawn  the  350  marginal  sketches. 

Finally,  my  indebtedness  to  my  publishei's,  Henry  Kimpton,  continues  to  be 
immense.  They  have  assisted  me  in  every  possible  way.  Why  Mr.  G.  E.  Deed  con- 
tinues to  put  up  with  my  inoods  and  vagaries  after  thirty  years  is  to  me  quite 
incomprehensible. 

Stewart  Duke -Elder. 


CONTENTS 

VOLUME  I 

THE  EYE  IN  EVOLUTION 

Part  I.    The  Effect  of  Light  on  Living  Organisms 


Chapter  I 
Introduction 


The  Scope  of  the  Subject 

The  Responses  of  Organisms  to  Light 


Photosynthesis 


Chapter  II 

The  Effect  of  Light  on  Metabolism  :  Photoperiodism 

MetaboHc  Effects  of  Light    . 
Photoperiodism  in  Plants 
Photoperiodism  in  Animals  . 

(a)  Metabolic  Activities  . 

(b)  Sexual  Cycle  of  Animals 

(c)  Pigment  Migration     . 

(d)  Bioluminescence 

(e)  Time -memory  of  Insects  and  Birds 


7 
9 
13 
13 
16 
19 
21 
22 


Chapter  III 
The  Effect  of  Light  on  Movement 


Historical  Development 
Types  of  Motorial  Responses 

(a)  Photokinesis 

(i)   Orthokinesis 
(ii)  Klinokinesis 

(b)  Phototropism    . 

(c)  Phototaxis 


(i) 
(ii) 
(iii) 
(iv) 

(V) 


(vi) 


Klinotaxis 

Tropotaxis 

Telotaxis 

Scototaxis 

Menotaxis 

Light-compass  Reaction,  61  ;  Navigational  Sense  in  Birds, 
63  ;  Orientation  to  Polarized  Light,  66  ;  Orientation  of 
Insects  Out-of-doors,  67  ;  Orientation  to  a  Visual  Pat- 
tern, 73  ;    Dorsal  (Ventral)  Light  Reaction,  74 

Mnemotaxis     ......... 


27 
31 
33 
34 
34 
38 
42 
47 
52 
55 
60 
60 


78 


CONTENTS 


Chapter  IV 

The  Effect  of  Light  on  Pigmentation 

The  Types  of  Colour  Change 
Mechanism  of  Colour  Changes 

Chromatophores   . 

Types  of  Pigment 

Types  of  Response 

Primary,  89  ;    Secondary,  91  ;   Indirect,  92 
Central  Organization  of  Pigmentary  Changes,  Nervous  and  Hormonal 

Chapter  V 
The  Emergence  of  Vision 
Light -sensitiveness,  the  Light  Sense  and  Vision       .... 


PAGE 

82 
85 
85 
87 
89 

92 


102 


Part  II.    The  Evolution  o!  the  Visual  Apparatus 

Chapter  VI 
The  Morphology  of  Invertebrate  Eyes 


I.  The  Genesis  of  the  Eye  .... 

Dermal  Photosensitivity. 
Specific  Light-sensitive  Cells    . 

Pigments  ..... 

Melanin,  118  ;  Visual  Pigments,  118 


Ommochromes,  122 


II.  The  Structure  of  Invertebrate  Eyes 

1.  Eye-spots  :   Stigmata 

2.  Light-sensitive  Cells    . 

3.  The  Simple  Eye 

(a)  The  Unicellular  Eye    . 
(6)  The  Multicellular  Simple  Eye 
(i)  The  Subepithelial  Eye 
(ii)  The  Epithelial  Invaginated  Eye 

The  Flat  Eye,    136;    the  Cupulate  Eye,    137;  the 
Vesicular  Eye,  141 
(iii)  The  Inverted  Retina 

(c)  Aggregate  Eyes  ..... 

(d)  Composite  Ocelli        ..... 

4.  The  Compound  Eye   ...... 

(a)  The  Development  of  Ocelli  and  Compound  Eyes 
(6)  The  Structure  of  the  Compound  Eye    . 

The  Simple  Ommatidial  Eye,  159  ;    the  Composite  Com 

pound  Eye,  160 
(i)  The  Compound  Eyes  of  Arachnids 
(ii)  The  Compound  Eyes  of  Crustaceans 
(iii)  The  Compound  Eyes  of  Insects 
(c)   The  Optical  System  of  the  Compound  Eye 

The   Appositional   Eye,    173  ;     the    Superpositional   Eye, 
174  ;   the  Analysis  of  Polarized  Light,  174 


113 
114 
115 
117 

126 
125 
127 
129 
130 
132 
132 
135 


146 
151 
152 
154 
156 
157 


160 
163 
166 
170 


CONTENTS 


XI 


Chapteb  VII 
The  Systematic  Anatomy  of  Invertebrate  Eyes 
The  Structural  Variability  of  Invertebrate  Eyes 
I.  Protozoa      .... 
II.  Parazoa  (Porifera  :   Sponges) 
III.  Invertebrate  Metazoa    . 

1.  Coelenterata 

(a)  Cnidaria   . 

Hydrozoa  ;   Scyphozoa  ;  Anthozoa 

(b)  Acnidaria  :  Ctenophora 

2.  Echinodermata  ..... 

Holothuroidea,  184  ;  Echinoidea,  185  ;  Asteroidea,  185 

3.  Worms       .... 

(a)  Unsegmented  Worms 

(i)  Platyhelminthes 

Turbellaria,  188  ;  Trematoda,  189  ;  Cestoda,  189 
(ii)  Nemertea 
(iii)  Nematoda 
(6)  Segmented  Worms  :  Annelida 
(i)  Oligochpeta     . 
(ii)  Polycheeta 
(iii)  Archiannelida 
(iv)  Hirudinea  :   Leeches 

4.  Chgetognatha  :  Arrow-worms 
6.  Rotifera    . 

6.  Polyzoa  :  Bryozoa 

7.  Brachiopoda  :   Lamp  Shells 

8.  Mollusca    ... 

(a)  Placophora 

(b)  Solenogastres     . 

(c)  Seaphopoda 

(d)  Gastropoda 

(e)  Lamellibranchiata 
(/)  Cephalopoda 

9.  Arthropoda 

(a)  Onychophora     . 
Crustacea . 
Myriapoda 
Arachnida 

Scorpionidea,    211  ;     Xiphosura,    212  ;     Araneida,    213 
Pseudoscorpionidea,  214  ;    Pedipalpi,  214  ;    Phalangida 
215  ;    Solifugae,  216  ;    Acarina,  216  ;    Pycnogonida,  21' 
Insecta      ....... 

(i)  The  Stemmata  of  Larval  or  Pupal  Forms 
(ii)  The  Dorsal  Ocelli  of  Adults      . 
(iii)  The  Compound  Eyes  of  Adults 


(b) 
(c) 
(d) 


{e) 


PAGE 

178 
180 
181 
181 
181 
182 
182 
182 
183 

186 
187 

188 

189 
190 
190 
190 
191 
193 
193 
194 
194 
194 
195 
195 
196 
197 
197 
197 
200 
201 
204 
204 
206 
210 
211 


217 
222 
224 

224 


Chapter  VIII 
The  Eyes  of  Proto-chordates 

1.  Hemichordata  ....... 

2.  Tunicata  :  Urochordata  ...... 

3.  Cephalochordata  :  Lancelots   ..... 


227 
228 
228 


Xll 


CONTENTS 


Chapter  IX 
The  Evolution  of  the  Vertebrate  Eye 

The  Vertebrate  Phylum        ..... 

1 .  The  Phylogeny  of  the  Vertebrate  Eye 

2.  The  Ontogeny  of  the  Vertebrate  Eye 

3.  The  Emergence  of  the  Vertebrate  Eye 

4.  The  General  Structm-e  of  the  Vertebrate  Eye 


PAGE 

233 
237 

239 
242 

248 


Chapter  X 
The  Eyes  of  Cyclostomes 


The  Class  of  Cyclostomes 

1.  The  Ammoccete  Eye 

Light-sensitive  Cells 

2.  The  Lamprey  Eye  . 


259 
261 
263 
263 


Chapter  XI 
The  Eyes  of  Fishes 


General  Configviration  of  the  Eye . 
The  Class  of  Fishes 

L  The  Selachian  Eye    . 

2.  The  Holocephalian  Eye 

3.  The  Teleostean  Eye 

4.  The  Dipnoan  Eye 

5.  The  Coelacanth  Eye 

6.  The  Chondrostean  Eye 

7.  The  Holostean  Eye 
Anomalies  in  the  Eyes  of  Fishes 

(a)  The  Tubular  (Telescopic)  Eye 
(6)  The  Amphibious  Eye 

(c)  Stalked  Eyes   . 

(d)  The  Migratory  Eye  . 


273 
278 
279 
290 
291 
312 
314 
315 
321 
322 
322 
324 
326 
328 


Chapter  XII 

The  Eyes  of  Amphibians 


The  Class  of  Amphibians 
General  Configuration  of  the  Eye. 

1.  The  Anuran  Eye 

2.  The  Urodelan  Eye     . 


333 
334 
334 
346 


Chapter  XIII 
The  Eyes  of  Reptiles 


The  Class  of  Reptiles  . 

General  Configuration  of  the  Eye 

1.  The  Lacertilian  Eye 

2.  The  Chelonian  Eye   . 

3.  The  Crocodilian  Eye 

4.  The  Rhynchocephalian  Eye 

5.  The  Ophidian  V.ye     . 


353 
353 
355 
368 
375 
379 
383 


CONTENTS 


Xlll 


Chapter  XIV 
The  Eyes  of  Birds 


The  Class  of  Birds 
General  Configuration  of  the  Eye. 
The  Avian  Eye 


397 
401 
401 


Chapter  XV 
The  Eyes  of  ]\Iam>iaxs 


The  Class  of  Mammals 

1.  The  Monotreme  Eye 

2.  The  Marsupial  Eye    . 
The  Sub-class  of  Placentals 

3.  The  Placental  Eye     . 

Aquatic  Adaptations 


429 
431 
437 
441 
446 
501 


Chapter  XVI 
The  Central  Organization  of  Vision 


General  Principles 


II. 


The  Nervous  Control 

1.  The  Nerve -net 

2.  Trunk-pathways 

3.  The  Ganglionic  Nervous  System 

(a)  The  Nervous  System  of  Worms 

(6)  The  Nervous  System  of  Arthropods . 

(c)   The  Nervous  System  of  Molluscs 

4.  The  Central  Nervous  System  of  Vertebrates 

Hind-brain,  533  ;   Mid-brain,  534  ;    Diencephalon,  537 

mus,  538  ;    Telencephalon,  542 
Evolution  of  the  Visual  Pathways  and  Centres 
The  Hormonal  Control   ...... 

Hormones  and  Neuro -secretory  Cells 

(a)  The  Neuro-endocrme  System  of  Crustaceans 

(b)  The  Neuro -endocrine  System  of  Insects 

(c)  The  Neuro -endocrine  System  of  Vertebrates 


Optic  Thala- 


509 
511 
614 
616 
617 
518 
521 
527 
530 


543 
647 
550 
552 
555 
556 


Part  III.    The  Function  of  the  Eyes  of  Animals 

Chapter  XVII 

The  Vision  of  Invertebrates 

Methods  of  Investigation      ..... 
1.  The  Reactions  of  the  Lower  Invertebrates  to  Light 

(a)  Protozoa        ..... 

(b)  Coelenterata  ..... 

(c)  Echinodermata       .... 


567 
670 
570 
571 
571 


XIV 


CONTENTS 


2.  The  Vision  of  Worms       .... 

(a)  Unsegmented  Worms 
(6)  Segmented  Worms 

3.  The  Vision  of  Molluscs     .... 

(a)  Gastropods  and  Lamellibranchs 
(6)  Cephalopods 

4.  The  Vision  of  Arthropods 

(a)  Onychophora 
(6)  Myriapods 

(c)  Crustaceans 

(d)  Arachnids 

5.  The  Vision  of  Insects 

(a)  The  Larvse  of  Insects      .... 

(b)  The  Dorsal  Ocelli  of  Adults      . 

(c)  The  Compound  Eyes  of  Insects 

(i)  Behavioural  Experiments 
(ii)  Electro-physiological  Characteristics 
(iii)  Spectral  Sensitivity 
(iv)  Discrimination  of  Luminosity-differences 
(v)  Perception  of  Colour  . 
(vi)  Perception  of  Form     . 
(vii)  Perception  of  Distance 
(viii)  Spatial  Appreciation  and  Localization 
Accommodation  in  Invertebrates 


PAGE 

572 

572 
572 
574 
574 
575 
677 
578 
578 
578 
579 
681 
582 
582 
683 
583 
584 
584 
585 
586 
588 
589 
589 
590 


Chapter  XVIII 


The  Vision  of  Vertebrates 


The  Role  of  Vision  in  Vertebrate  Life 

(a)  Cyclostomes 

(b)  Fishes 

(c)  Amphibians 
{d)  Reptiles 
(e)  Birds 
(/)  Mammals 

I.  The  Perception  of  Light 

1.  The  Nocturnal  Eye 

(a)  The  Optical  System 

The  Tapetum  Lucidum 

(b)  The  Organization  of  the  Retina 

2.  The  Diurnal  Eye     .... 

3.  The  Arhythmic  Eye 

(a)  Contractile  Pupils 
(6)  Occlusible  Tapeta  . 

(c)  Photo -mechanical  Changes  in  the  Retina 
(rf)  The  Static  Organization  of  the  Retina 

4.  Absolute  Sensitivity  to  Light  . 

6.  Discriminati       of  Variations  in  Intensity  . 


597 
598 
698 
599 
599 
600 
600 

602 
605 
605 
606 
609 
611 
612 
612 
612 
614 
616 
616 
617 


CONTENTS 


XV 


PAGE 

II.  The  Perception  of  Colour        .........  619 

Objective  Methods  of  Investigation          ......  621 

Subjective  Methods  of  Investigation        ......  623 

1.  The  Colour  Vision  of  Cyclostomes     .......  624 

2.  The  Colour  Vision  of  Fishes 624 

3.  The  Colour  Vision  of  Amphibians      .......  627 

4.  The  Colour  Vision  of  Reptiles             .......  628 

6,  The  Colour  Vision  of  Birds 629 

6.  The  Colour  Vision  of  Mammals          .......  632 

III.  The  Perception  of  Form          .........  637 

1.  Optical  Factors 638 

(a)  The  Refraction  of  Vertebrates           ......  638 

(6)  Accommodation  in  Vertebrates          ......  640 

(i)  Static  Devices       ........  640 

Stenopoeic    Pupil,    641  ;     Duplicated    Optical    System, 
641  ;    Interposition  of  Nictitating  Membrane,    643  ; 
Duplicated  Retina,    643  ;     Ramp-retina,    643  ;     Cor- 
rugated Retina,  643  ;    Length  of  Receptor  Elements, 
643 

(ii)  DjTiamic  Devices           .......  644 

(a)  Movement  of  Lens  as  a  ^^^^ole        ....  644 

Backward  Movement,  644  ;    Forward  Movement, 
647 

(^)  Deformation  of  Lens     ......  649 

By  Direct  Ciliary  Pressure,   649  ;     by    Capsular 
Elasticity,  652 

(iii)  Accommodation  in  Amphibious  Vertebrates     .           .           .  654 

(c)   Other  Optical  Factors  determining  Visual  Acuity        .           .           .  655 

2.  The  Structure  of  the  Retina 656 

(a)  The  Area  Centralis           ........  657 

(b)  The  Fovea 658 

(c)  The  Degree  of  Summation        .......  659 

3.  The  Visual  Acuity  of  Vertebrates      .......  660 

(a)  The  Visual  Acuity  of  Fishes 660 

(b)  The  Visual  Acuity  of  Amphibians     .  .  .  .  .  .661 

(c)  The  Visual  Acuity  of  Reptiles .          ......  661 

(d)  The  Visual  Acuity  of  Birds 662 

(e)  The  Visual  Acuity  of  Mammals         ......  663 


rV.  The  Perception  of  Space 

1.  The  Visual  Fields  of  Vertebrates 

(a)  The  Uniocular  Field 
(6)  The  Binocular  Field 

Cyclostomes,  678  ;    Fishes,  678 
682  ;    Birds,  684  ;    Mammals, 

2.  The  Ocular  Movements    . 

(a)  Involuntary  Ocular  Movements 
(6)  Voluntary  Ocular  Movements 

Fishes,  693  ;    Amphibians,  694 
Mammals,  696 


Amphibians,  682 
687 


Reptiles, 


666 
669 
669 
672 


689 
690 
692 


Reptiles,  694  ;    Birds,  695 


XVI 


CONTENTS 


The  Perception  of  Space — contd.  page 

3.  Uniocular  and  Binocular  Vision         .......      697 

Spatial  Judgments        .  .  .  .  .  .  .  .  .700 

Fishes,    701  ;    Amphibians    and    Reptiles,    702  ;    Birds,    702  ; 
Manmials,  704 
V.  The  Perception  of  Movement         .  .  .  .  .  .  .  .705 

Part  IV.    Evolutionary  By-ways 

Chapter  XIX 
Median  Eyes 

1.  Pineal  and  Parietal  Organs        .  .  .  .  .  .  .  ..  711 

Cyclostomes,  713  ;  Fishes,  713  ;  Amphibians,  714  ;  Reptiles,  715 

(a)  The  Median  Eye  of  the  Lamprey  .  .  .  .  .  .716 

(6)  The  Median  Eyes  of  Lizards  and /S^/ienorfon     .  .  .  .  .716 

2.  The  Function  of  the  Pineal  and  Parietal  Organs  .  .  .  .  .718 

Chapter  XX 

Rudimentary  Eyes 

Habit  and  Regression  .  .  .  .  .  .  .  .  .  .721 

1.  The  Sedentary  Habit 722 

Molluscs,  722  ;    Crustaceans,  722 

2.  The  Abyssal  Habit 722 

Molluscs,  723  ;   Crustaceans,  723  ;  Fishes,  723 

3.  The  Cavernicolous  or  Limicoline  Habit         .  .  .  .  .  .724 

Invertebrates,  724  ;    Cave-fishes,  725  ;    Amphibians,  726 

4.  The  Fossorial  or  Burrowing  Habit       .  .  .  .  .  .  .728 

Invertebrates,  728  ;  Amphibians,  730  ;  Reptiles,  731  ;  Mammals,  733 

5.  The  Parasitic  Habit 733 

Invertebrates,  733  ;  Cyclostomes,  734  ;  Fishes,  734 


Chapter  XXI 
Luminous  Organs 
Bioluminescence  ..... 

1.  The  Occurrence  of  Bioluminescence  . 

The  Biological  Purpose  of  Bioluminescence 

2.  The  Biological  Mechanism  of  Bioluminescence 

Extracellular  Bioluminescence 
Intracellular  Production  of  Bioluminescence 

3.  The  Chemical  Mechanism  of  Bioluminescence 


736 
737 
741 

744 
745 
746 

747 


Chapter  XXII 
Electric  Organs 
The  Electric  Organs  of  Fishes  :  Astroscopus 

EPILOGUE 

APPENDIX.  Pala^ontological  Table  . 
Zoological  Glossary  .... 
Index  ...... 


751 

753 

754 
756 
779 


PART  I 
THE  EFFECT  OF  LIGHT  ON  LIVING  ORGANISMS 

Introduction 

The  Effect  of  Light  on  Metabolism 
The  Effect  of  Light  on  Movement 
The  Effect  of  Light  on  Pigmentation 
The  Emergence  of  Vision 


S.O.— VOL.  I. 


Fig.   1.— Charles  Darwin  (1809-1882). 
(From  a  portrait  by  John  Collier  in  the  Linnean  Society.) 


CHAPTER   I 
INTRODUCTION 

We  begin  with  a  drop  of  viscid  protoplasm  the  reactions  of  which 
we  do  not  understand,  and  we  end  lost  in  the  delicacy  of  the  structure 
of  the  eye  and  the  intricacies  of  the  ten  thousand  million  cells  of  the 
human  brain.  We  begin  with  photosjnithesis  in  a  unicellular  plant,  or 
with  a  change  in  the  viscosity  produced  by  light  in  the  outer  layers  of 
the  amoeba,  and  we  end  with  the  mystery  of  human  perception.  We 
begin  some  one  or  two  thousand  million  years  ago  in  the  warm  waters  of 
the  Archeozoic  era  and  we  end  with  the  speculations  of  tomorrow.  And 
as  we  travel  together  tracing  the  responses  of  living  things  to  light  from 
the  energy  liberated  by  a  simple  photochemical  reaction  to  the  faculty 
of  appreciating  and  interpreting  complex  perceptual  patterns,  neither 
in  fact  nor  in  fiction  does  a  story  more  fascinating  unfold.  It  is  a  story 
which  traces  a  development  from  a  vague  sentiency  to  apperception, 
from  vegetative  existence  to  the  acquisition  of  the  power  to  mould  the 
environment,  from  passive  reactivity  to  the  ability  to  create  history. 
Nor  is  there  a  story  more  important.  Even  at  the  physiological  level 
some  38%  of  our  sensory  input  is  derived  from  the  retinae,^  impulses 
from  which,  even  in  the  complete  absence  of  visual  stimuli,  are  largely 
responsible  for  maintaining  a  tonic  influence  upon  the  level  of 
spontaneous  activity  in  the  brain. ^  From  the  psychological  point  of 
view  the  importance  of  vision  is  still  greater.  If,  indeed,  the  proper 
study  of  mankind  is  Man,  and  if  (as  we  must  agree)  his  behaviour  and 
his  contact  with  the  outside  world  are  mediated  through  his  senses, 
what  can  be  more  fundamental  than  the  study  of  the  sense  which,  more 
than  any  other,  determines  his  intelligence  and  regulates  his  conduct,  of 
the  faculty  which  eventually  played  the  preponderant  role  in  assuring 
his  dominance  and  determining  his  physical  dexterity  and  intellectual 
supremacy  ?     We  are  indeed  highly  visual  creatures. 

It  would  seem  appropriate  to  introduce  a  book  devoted  to  the  evolution  of 
vision  with  a  portrait  of  charles  darwin  (1809-1882)  (Fig.  1),  the  great  English 
naturalist  who,  like  Newton  in  the  world  of  physics,  was  one  of  the  very  few  men 
who  revolutionized  world  thought  in  the  subject  on  which  he  worked— and 
beyond.  But  Darwin  has  a  special  claim  to  introduce  this  chapter,  for  at  a  time 
when  the  conduct  of  animals  was  generally  ascribed  to  the  existence  of  vital 
forces  or  psychic  activities,  and  when  the  orientation  of  plants  was  thought  to 
be  due  to  the  direct  influence  of  physical  stimuli  such  as  light  and  heat  upon  the 

^  According  to  the  calculations  of  Bruesch  and  Arey  (J.  cx>mp.  Neurol.,  77,  631, 
1942). 

2  See  Claes  [Arch,  intern.  Physiol.,  48,  181,  1939)  and  many  others,  admirably 
summarized  in  Grauit  {Receptors  and  Sensory  Perception,  New  Haven,  1955). 

3 


THE   EYE   IN   EVOLUTION 

plant  as  a  whole,  he  transformed  biology  to  a  more  factvial  plane  based  on 
observation  and  experiment,  and  was  the  first  to  show  that  in  the  higher  plants 
receptor  tissues  existed  separately  from  motor  tissues,  and  that  the  orientation 
of  plants  to  light  was  due  to  the  transference  over  some  distance  of  stimuli 
appreciated  by  the  former  to  be  made  effective  by  the  latter.  These  observations 
which  appeared  in  the  last  of  the  classical  books  derived  from  his  pen  ^  form  a 
typical  example  of  the  revolutionary  nature  of  Darwin's  philosophy — the  result 
of  a  unique  combination  of  experimental  genius  with  penetrative  powers  of 
interpretation  which  have  rarely  been  equalled — and  from  these  observations 
have  directly  followed  our  understanding  of  the  development  of  the  sensory 
organs  and  their  effect  on  the  evolution  of  the  higher  species  in  the  animal  scale. 
The  son  of  a  doctor  in  the  English  country  town  of  Shrewsbury,  he  went  to 
the  University  of  Edinburgh  to  study  medicine  ;  this,  however,  he  forsook  and 
went  to  Cambridge  with  the  intention  of  entering  the  Church  ;  but  here  Sedgwick 
and  Henslow,  the  professors  of  geology  and  botany,  inspired  him  again  with  a 
love  of  natural  history  which  eventually  was  to  become  a  passion.  Darwin's 
assessment  of  the  qualities  responsible  for  his  own  success  is  worth  remembering  : 
"  the  love  of  science,  unbounded  patience  in  long  reflecting  over  any  subject, 
industry  in  observing  and  collecting  facts  and  a  fair  share  of  invention  as  well 
as  of  common  sense  ".  And  again  :  "I  have  steadily  endeavoured  to  keep  my 
mind  free  so  as  to  give  vip  any  hypothesis,  however  much  beloved  (and  I  cannot 
resist  foi-ming  one  on  every  subject),  as  soon  as  facts  are  shown  to  be  opposed 
to  it  ".- 

THE  RESPONSES  OF  ORGANISMS  TO  LIGHT 

LIGHT — the  visible  radiant  energy  derived  from  the  sun — is  respon- 
sible for  the  whole  existence  of  living  things  on  the  earth,  and  without 
question  photosynthesis  in  plants — the  reaction  whereby  the  carbon 
dioxide  and  water  which  permeate  the  atmosphere  and  the  earth's 
crust  are  converted  into  the  organic  substances  which  constitute  the 
basis  of  all  living  things — is  the  most  fundamental  and  important 
chemical  process  on  our  planet.  Not  only  was  photosynthesis  respon- 
sible for  the  origin  of  'life  but  it  maintains  the  perpetual  cycle  of  the 
activities  of  living  things.  By  oxidation,  living  structures  are  con- 
tinuously broken  down  to  their  initial  constituents  (carbon  dioxide 
and  water),  the  process  being  accompanied  by  the  liberation  of  the 
energy  required  by  organisms  to  perform  their  varied  activities  ;  by 
photosynthesis  the  carbon  dioxide  and  water  produced  by  the  oxidation 
of  living  matter  are  perpetually  reunited  by  an  opposite  process  of 
reduction  with  the  return  of  oxygen  to  the  atmosphere,  the  high  energy 
requirements  necessary  being  supplied  by  the  capacity  of  the  chloro- 
phyll group  of  pigments  in  green  plants  to  absorb  sunlight.  This 
reaction  whereby  the  chlorophyll  system  stores  and  then  liberates 
light-energy  is  thus  not  only  the  source  of  the  activities  of  all  living 
things  but  supplies  much  of  the  energy  at  the  disposal  of  the  civilized 
world  in  the  stores  of  coal  and  petroleum  formed  throughout  the  ages. 

^  Pouer  of  Movements  in  Plants,  London,  1880. 

^  Life  and  Letters  of  Darwin,  by  Francis  Darwin,  1887. 


RESPONSES   OF   ORGANISMS   TO   LIGHT 

It  would  be  out  of  place  to  enter  fully  into  the  mechanism  of  photosynthesis 
by  chlorophyll  here  ;  for  a  recent  summary  the  reader  is  referred  to  the  mono- 
graph by  Hill  and  Whittingham.i  The  chlorophyll  group  of  pigments  are  tetra- 
pyrrolic  compounds  in  which  magnesium  is  present  in  non-ionic  form  ;  they  are 
related  to  hgemin  which,  however,  contains  a  central  iron  atom.  The  completed 
process  whereby  carbohydrates  are  synthesized  has  long  been  known  and  may 
be  represented  by  the  equation  : 

.rCOj  +  .rHaO  +  radiant  energy  -^  Ca;H2j;0a;  +  .rOj  +  stored  energy. 
The  intimate  mechanism,  however,  has  only  recently  begun  to  be  analysed,  an 
advance  largely  due  to  the  use  of  radio-active  carbon  (i*C)  as  a  "  tracer  ". 
Although  many  of  the  details  are  still  obscure,  particularly  the  way  in  which 
chlorophyll  absorbs  radiant  energy  and  directs  it  into  chemical  processes,  the 
basic  reactions  are  known  and  can  indeed  be  carried  out  in  the  test-tube.  The 
essential  process  is  the  photolysis  of  water.  Chlorophyll  induces  the  energy 
derived  from  light  to  break  the  hydrogen-oxygen  bonds  in  the  molecule  of  water  ; 
the  hydrogen  therefrom  is  used  to  convert  the  single  carbon  atoms  of  CO 2  into 
long-chained  carbohydrates  through  the  medium  of  phosphoglyceric  acid  and 
the  oxygen  is  liberated  as  a  free  gas  ;  meantime  a  store  of  chemical  energy  is 
provided  by  the  photosynthesis  of  energy-rich  compounds  such  as  adenosine 
triphosphate,  the  break-down  of  which  by  simple  hydrolysis  releases  large 
amounts  of  energy  to  drive  the  process.  It  is  probable  that  these  and  the  many 
other  compounds  fovind  in  jjlants  are  formed  by  enzyme-reactions  from  one  or 
more  of  the  constituents  of  the  photosynthetic  cycle  at  either  the  C3  or  Cg  level. ^ 

Apart  from  this  basic  activity  which  characterizes  the  vegetable 
world,  light  produces  photochemical  reactions  of  great  variety  in 
living  organisms.  The  energy  thus  liberated  produces  in  the  most 
primitive  creatures  the  only  response  available — a  change  of  general 
activity,  frequently  of  motion,  just  as  do  other  stimuli,  mechanical, 
gravitational,  thermal,  chemical  or  electrical  ;  in  the  higher  forms  a 
multitude  of  activities  may  be  initiated  or  influenced. 

These  responses  we  will  review  under  four  main  headings.  In  the 
first  place,  the  response  may  take  the  form  of  a  change  in  general 
metabolic  activity,  usually,  but  not  invariably,  an  increase  of  activity 
under  the  influence  of  light.  As  a  natural  extension  of  this,  the  diurnal 
cycle  of  light  and  darkness  has  in  the  course  of  evolution  so  impressed 
itself  upon  a  number  of  the  fundamental  activities  of  many  organisms 
(including  man)  that  these  show  a  corresponding  rhythm  which  has 
eventually  become  innate  and  endogenous  (photoperiodism).  In  the 
second  place,  the  response  may  be  expressed  as  a  variation  in  movement. 
In  its  simplest  form  this  is  also  merely  a  change  in  general  activity 
wherein  movements  are  random  in  nature  and  undirected  (photo - 
kinesis)  ;  as  an  evolutionary  extension  of  this  the  movements  initiated 
by  light  come  under  the  directional  control  of  the  stimulus  so  that  the 
organism  is  orientated  by  light  in  a  definite  way  ;     such  movements 

1  Photosynt}(e.sis.  London,  1955.  See  also  Proc.  roy.  Soc.  B,  157,  291  (1963). 

2  For  reviews,  see  Arnon  (An?i.  Rev.  plant  Physiol..  7,  325,  1956,  Nature  (Lond.), 
184,  10,  1959),  Rosenberg  (Ibid.,  8,  1957). 


THE   EYE   IN  EVOLUTION 

may  affect  the  component  parts  of  sessile  organisms  (phototropism) 
or  may  be  expressed  in  translatory  movements  by  motile  organisms 
(phototaxes).  In  the  third  place,  light  acting  directly  or  indirectly  is 
the  most  potent  stimulus  for  altering  the  pigmentary  distribution  in 
both  plants  and  animals — an  understandable  reaction  since  pigment 
has  been  evolved  specifically  for  the  absorption  of  light,  either  to 
utiHze  its  energy  or  as  a  protection  against  its  excess. 

All  these  activities  have  become  more  complex  as  evolution  has 
proceeded.  The  most  primitive  required  no  specific  organization  ; 
the  more  complex  called  for  the  acquisition  of  one  or  more  receptor 
organs,  which  in  their  most  elementary  stages  need  appreciate  only 
changes  in  the  intensity  of  the  light,  but  in  their  more  advanced  forms 
must  analyse  the  direction  of  its  incidence  and  its  spatial  distribution. 
Initially,  in  some  unicellular  organisms  a  diffuse  reactivity  sufficed  ; 
but  as  multicellular  organisms  developed,  the  stimulus  must  needs  be 
transported  to  the  effector  organs,  either  chemically  by  hormones  or 
by  nervous  activity.  In  this  way  the  effects  of  light  upon  metabolism, 
orientation  and  pigmentation  became  correlated  through  primitive 
nerve-nets  and  then  became  integrated  in  the  ganglia  of  the  central 
nervous  system  ;  and  eventually,  when  the  nervous  pathways  from  the 
eyes  were  projected  into  a  head-ganglion  and  ultimately  into  the  fore- 
brain,  the  highly  complex  faculties  of  vision  and  apperception  evolved. 


CHAPTER   II 
THE  EFFECT  OF  LIGHT  ON  METABOLISM 

It  is  well  known  and  iniiversally  recognized  that  the  general 
behaviour  of  many  organisms  is  regulated  by  light  ;  the  contrast 
between  the  activities  of  nature  by  day  and  its  stillness  by  night  needs 
no  stress.  This  is  a  widespread  characteristic  of  vegetable  life  which 
exists  so  much  more  closely  to  the  sun  and  the  earth  than  do  animals, 
but  even  among  the  latter  dramatic  changes  are  frequently  evident, 
particularly  in  the  lower  forms.  Thus  among  Protozoa,  some  Rhizopods 
change  their  form,  contracting  under  the  influence  of  light  (Engelmann, 
1882  ;  Verworn,  1889)  (Figs.  2  and  3),  many  species  are  activated  by 
light  (such  as  flat-worms,  Loeb,  1893-94),  while  other  creatures  become 
inactive  under  its  influence  (maggots,  Herms,  1911  ;  and  many  insects, 
such  as  cockroaches,  Gumi,  1940).  Among  the  higher  forms  of  life,  in 
addition  to  a  number  of  basic  metabolic  functions,  the  reproductive 


Fig.  2.  Fig.  3. 

Figs.  2  and  3. — Pelomyxa  pahistris  at  rest  (Fig.  2),  and  contracted 
under  the  influence  of  light  (Fig.  3). 

cycle  and  secondary  features  such  as  colour  changes  and  behavioural 
habits  are  similarly  regulated  by  light  although  in  many  cases  other 
factors  such  as  temperature,  humidity  and  nutrition  exert  sometimes 
contributory,  sometimes  more  potent  effects.  In  this  way  the  alterna- 
tion of  day  and  night  has  imposed  a  rhythmic  diurnal  cycle  upon  a 
number  of  the  activities  of  living  organisms  (photoperiodism)  ;  and 
it  is  to  be  remembered  that  in  many  of  the  phenomena  thus  involved 
darkness  seems  to  be  as  important  a  stimulus  as  light.  Indeed,  in 
many  cases  the  rhythm  has  become  so  fundamental  that  if  the  organism 
is  placed  in  experimental  circumstances  wherein  the  natural  alternation 
of  light  and  darkness  is  changed  to  become  out-of-phase,  or  if  it  is 
exposed  to  continuous  light  or  darkness,  many  of  these  cyclic  changes 
continue  as  if  the  normal  24-hour  rhythm  still  persisted  ;  the  rhythm 
originally  imposed  by  external  circumstances  has  eventually  become 
autochthonous. 


THE   EYE   IN   EVOLUTION 


Fig.  4.— Carl  Linn.t^us  (1707-1778). 

Carl  Linnsous,  son  of  a  Lutheran  Swedish  pastor  and  Professor  of  Botany 
at  Uppsala,  is  universally  acknowledged  as  the  Father  of  Scientific  Botany. 
His  main  work  was  his  System  of  Nature  which  passed  through  1 2  editions  in 
his  lifetime  following  its  initial  publication  in  1741.  He  had  a  passion  for 
classification.  Not  only  did  he  classify  in  a  system  based  on  their  reproductive 
organs  the  18,000  species  of  plants  known  to  him,  which  he  and  his  pupils 
travelled  far  and  wide  to  collect  (one  of  them,  for  example,  accompanied 
Captain  Cook  on  his  first  voyage,  1768-71)  ;  but  he  also  classified  animals, 
diseases  and  minerals — even  past  and  jiresent  scientists  in  a  system  of  military 
rank  with  himself  as  general.  He  introduced  the  now  universally  adopted 
nomenclature  of  plants  and  animals,  first  the  generic  name  indicating  the 
genus,  and  second  the  specific  name  indicating  the  species.  His  garden  is 
still  tended  in  Uppsala.  The  Linnean  Society  of  London  which  jDOSsesses  his 
library  and  collections  was  founded  in  1788. 

This  portrait  of  "  Carl  v.  Linne  astat.  67",  lent  me  by  the  Linnean  Society, 
is  from  the  original  by  Krafft,  the  Swedish  artist,  who  painted  it  in  1774  for 
the  College  of  Physicians  at  Stockholm  of  which  Linnaeus  was  one  of  the 
founders. 


LIGHT  AND  METABOLISM 

The  origin  of  such  rhythms  is  speculative,  but  it  is  interesting  to  recall  the 
environment  of  living  creatures  when  first  they  experienced  the  drama  of  a  day- 
night  cycle  on  the  earth.  For  millions  of  years  living  organisms  never  experienced 
conditions  more  varied  than  those  of  the  warm  but  placid  sea,  but  as  the  sea- 
weeds of  the  swamps  spread  onto  the  land,  plants  became  exposed  alternately 
to  the  stimulating  conditions  of  a  humid  hot-house  during  the  day  and  the 
depression  of  the  comjDarative  chill  of  night.  Similarly,  as  Amphibians  emerged 
to  creep  upon  the  land  in  the  heat  of  the  Palfeozoic,  and  as  thej'  and  the  Reptiles 
matured  in  the  torrid  Jurassic  and  Cretaceous  ages,  it  is  difficult  to  realize  the 
violence  of  the  contrast  between  the  extreme  metabolic  and  nervous  activity 
which  must  have  occurred  in  the  blaze  of  noon,  and  the  sluggishness  of  sleep  and 
the  reduction  of  nervous  energy  which  must  have  prevailed  in  the  cold  of  night  ; 
for  chemical  activity  and  the  speed  of  nervous  impulses  are  both  dependent  on 
temperature.  It  is  probable,  indeed,  that  the  development  of  thermostasis  and 
its  ultimate  evolution  into  homeostasis  were  the  determining  events  which  made 
possible  the  evolution  and  ultimate  supremacy  of  Birds  and  Mammals  on  a 
cooling  globe,  and  that  the  lack  of  the  control  of  temperature  was  the  main  cause 
of  the  extinction  of  the  Dinosaurs  and  the  retreat  of  the  Amphibians  to  a  few 
degenerate  types.  But  it  is  to  be  remembered  that  the  period  during  which  the 
primitive  creatures  which  first  inhabited  the  still-warm  earth  experienced  this 
alternating  climax  of  delirious  activity  each  noon  and  fatigued  torpidity  each 
night,  occupied  some  hundred  million  years  ;  and  even  although  their  descendants 
have  long  acquired  the  peace  of  thermostas's,  it  is  not  surprising  that  traces  of 
the  early  turmoil  still  remain. 

PHOTOPEEIODISM    IN    PLANTS 

Over  200  years  ago,  carl  linn.^us  (1707-1778)  (Fig.  4),  who  laid 
the  groundwork  of  scientific  botany  at  Uppsala,  noted  that  many 

Figs.  5  and  6. — Sleep  ^Movements  in  Flowers  and  Leaves. 


Fig.  5. — Oxalis  rosea  awake. 


Fig.  6. — Oxalis  rosea  asleep. 


10  THE   EYE   IN   EVOLUTION 

flowers  have  a  time  of  opening  and  closing  so  regular  that  he  constructed 
a  flower-clock  from  which  the  time  of  day  could  be  read — the  poppy 
opened  at  6  a.m.,  the  speedwell  at  mid-morning,  the  white  campion  in 
the  evening  (to  be  pollinated  by  night  moths),  and  so  on  (Figs.  5  and  6). 
At  a  much  later  date,  the  "  sleep  movements  "  of  leaves  were  similarly 
studied  by  Darwin  (1880)  :  those  of  the  runner  bean,  for  example,  raise 
themselves  during  the  morning,  become  horizontal  by  noon,  fall  in  the 
afternoon  and  fold  up  at  night.  The  significance  of  these  daily 
rhythms,  however,  was  largely  neglected  until  they  were  intensively 
investigated  by  the  German  botanist,  E.  Blinning  (1931-56),  who 
showed  that  they  were  not  simply  an  immediate  response  to  the 
passing  stimuli  of  day  and  night,  but  were  part  of  a  rhythmic  change 
which  has  become  characteristic  and  endogenous  to  the  plant  itself — a 
24-hour  rhythm  in  the  intensity  of  endosmosis  throughout  its  structure, 
in  the  rate  of  growth,  the  rate  of  respiration,  the  activity  of  enzymes  and 
the  entire  metabolism,  a  rhythm  to  which  the  plant  has  become 
habituated  so  that  the  periodicity  persists  for  some  time  even  if  it  is 
placed  in  continuous  darkness,  and  is  only  slowly  readjusted  if  an 
artificial  rhythm  is  imposed  upon  it.^.  Other  factors  may  supervene, 
the  most  important  of  which  are  temperature  and  nourishment,  but 
the  most  profound  influence  on  basic  activities  is  that  of  the  sun,  from 
the  energy  of  which  all  life  is  ultimately  derived. 

The  pattern  of  the  flowering  of  many  plants  is  a  good  example  of 
this  general  tendency^ — and  an  important  one,  for  floral  initiation  is  a 
fundamental  factor  marking  the  change  from  vegetative  life  to  reproduc- 
tive activity.  Although  experimental  work  of  considerable  merit  had 
been  done  on  the  effects  of  artificially  varying  the  periods  of  illumina- 
tion on  the  growth  and  maturation  of  plants,  particularly  by  Schiibeler 
(1880)  in  England,  Tournois  (1912)  in  France,  and  Klebs  (1918)  in 
Germany,^  it  was  left  to  two  American  botanists.  Garner  and  Allard 
(1920),  to  establish  finally  the  important  fact  that  in  many  species 
flowering  did  not  depend  primarily  on  temperature  or  the  intensity  of 
illumination  but  on  the  daily  lengths  of  the  periods  of  light  and  darkness  ; 
they  therefore  introduced  the  term  photoperiodism.  In  many  plants 
the  determining  factor  is  the  length  of  the  day,  and,  as  was  first  proved 
by  the  Russian  botanist,  Cailahian  (1936),  the  primary  receptor  organ 
is  the  leaf  ;  even  although  the  rest  of  the  plant  is  covered,  the  exposure 
of  one  leaf,  or  even  part  of  a  leaf,  to  the  rhythm  of  light  and  darkness 
determines  the  cycle,  and  if  the  leaves  are  removed  and  the  plant 
rendered  naked  to  live  on  its  stored  food  it  immediately  becomes 

1  See  Grossenbacher  (1939),  Engel  and  Heimann  (1949),  Flligel  (1949),  Hagan 
(1949),  Heimann  (1950-52),  Enderle  (1951),  Vegis  (1955),  Biinning  (1956),  Wareing 
(1956),  and  others. 

"  For  review,  see  Smith,  1933. 


LIGHT   AND  METABOLISM 

indifferent  to  the  alternating  change  between  darkness  and  light. 
Moreover,  if  a  plant  of  one  tyjDe  is  denuded  of  leaves  and  the  leaf  of  a 
plant  with  a  different  cyclic  character  is  grafted  onto  it,  the  host-plant 
assumes  the  periodicity  of  the  grafted  leaf.^ 

Two  different  responses  are  well  recognized.     In  summer-flowering  plants 
{long-day  plants)  which  bloom  when  the  spring  days  lengthen,  the  formation  of 


11 


Fig.   7. — The  Effect  on  Flowerixg  of  Ixtermittent  Light  during  the 

Night. 

On  the  /eft  are  two  gladioli  (long-day  plants)  grown  in  a  control  green- 
house with  a  normal  solar  day-and-night  rhythm  ;  on  the  right,  two  similar 
plants  growai  with  intermittent  light  during  the  night  (Boyce  Thompson 
Institute  for  Plant  Research). 


flowers  is  inhibited  in  darkness  while  during  the  periods  of  light  some  substance 
is  presumably  formed  in  the  leaves  which  counteracts  this  inhibition  ;  in  short- 
day  plants  which  come  to  flower  when  the  autumn  days  shorten,  both  dark  and 
light  periods  are  necessary  for  the  develoiament  of  the  stimulus,  each  with  opposite 
effects,  one  depending  on  light-energy  and  the  other  being  inhibited  by  light.  In 
summer-flowering  jolants  artificial  light  during  the  night  promotes  flowering 
(Fig.  7)  ;  in  autumn-flowering  plants  flowering  in  short  days,  light  during  the 
day  promotes  flowering  but  short  joeriods  of  light  during  the  night  prevent  it. 

1  Melchers  (1936-37),  Cailahian  (1936-47),  Loehwing  (1938),  Borthwick  and  Parker 
(1938-40),  Hamner  and  Naylor  (1939),  Harder  and  v.  Witsch  (1940),  Withrow  et  al. 
(1943),  and  others. 


12  THE   EYE   IN  EVOLUTION 

The  mechanism  of  these  photoperiodic  responses  is  unknown  but 
several  facts  are  now  estabhshed.  It  is  significant  that  a  brief  exposure 
(1  sec.  in  some  species)  to  fight  of  a  very  low  intensity  (of  the  order  of 
1  ft.  candle,  that  is,  of  the  intensity  of  moonlight)  is  sufficient  to 
determine  the  periodicity.  The  wave-length  of  the  fight  is  of  import- 
ance, for  the  action-spectrum  shows  a  specificity  with  maxima  in  the 
red  and  blue — a  fact  which  suggests  the  presence  of  one  or  more 
absorbing  pigments  ;  moreover,  there  are  indications  of  an  antagonism 
between  the  action  of  different  spectral  regions,  while  near  infra-red 
radiation  takes  an  active  part  in  the  effect  (see  Wassink  and  his 
co-workers,  1950-56).  Such  a  pigment  (or  pigment -mixture)  has  not 
been  isolated,  but  Borthwick  and  his  colleagues  (1948-54)  speculated 
that  it  is  an  open-chain  tetrapyrrol  pigment,  a  distant  relative  of 
chlorophyll.  With  its  aid  a  photosynthetic  reaction  takes  place,  the 
nature  of  which  is  unknown  ^  with  the  probable  result  that  one  or 
more  plant  hormones,^  perhaps  both  activating  and  inhibiting  in  their 
action,  travel  down  the  leaf-stalk  and  up  the  shoot  to  influence 
flowering  ;  the  substance  can  travel  through  living  cells  and  across 
grafts  but  not  across  an  inanimate  obstacle  (Cailahian,  1940). 

The  fact  that  such  a  substance  (or  substances)  has  eluded  chemical 
detection,  has  stimulated  several  alternative  hypotheses.^  However 
that  may  be,  and  whatever  the  intimate  mechanism,  the  fact  remains 
that  the  order  of  the  procession  of  flowers  through  the  seasons  is  largely 
determined  by  the  diurnal  periodicity  of  light  and  darkness. 

Bonner.     Botan.  Gaz.,  110,  625  (1949).  Darwin.       The.    Power    of    Movement    in 
Bonner  and  Thurlow.     Botan.  Gaz.,  110,  Plants,  London  (1880). 

613(1949).  Enderle.    PZan/a  (Berl.),  39,  570,  (1951). 

Borthwick,  Hendricks  and  Parker.    Botan.  Engel  and  Heimann.     Planta  (Berl.),  37, 

Gaz.,  110,  103  (1948).  437  (1949). 

Borthwick,  Hendricks,  Toole,  E.  H.,  and  Engelmann.     Pfliigers  Arch.  ges.  Physiol., 

V.  K.     Botan.  Gaz.,  115,  205  (1954).  29,  387  (1882). 

Borthwick  and  Parker.     Botan  Gaz.,  100,  Fliigel.     Planta  (Berl.),  37,  337  (1949). 

374  (1938)  ;    101,  806  (1940).  Garner  and  Allard.    J .  agric.  Res.,  18,  553 
Borthwick,  Parker  and  Hendricks.    Amer.  (1920). 

Naturalist,  84,  117  (1950).  Grossenbacher.     Amer.  J.  Botan.,  26,  107 
Biinning.    J6.  wrss  Bo/an.,  75,  439  (1931).  (1939). 

Ber.  dfsch.  botan.  Ges.,  54,  590  (1937).  Gunn.    J.  e.rp.  Biol.,  17,  267  (1940). 

Biol.  Zbl.,  64,  161  (1944).  Hagan.     Plant  Physiol.,  24,  441  (1949). 

P/ora,  38,  93  (1944).  Hamner  and  Naylor.     Botan.   Gaz.,  \{iQ, 
Naturwissenschaften,  33,  271  (1946).  853  (1939). 

A^oYwr/orsc/).,  3b,  457  (1948).  Harder     and     van     Senden.      Naturwiss- 
Plania  (Berl.),  38,  521  (1950).  enschaften,  36,  348  (1949). 

Ann.  Rev.  Plant  Physiol.,  7,  71  (1956).  Harder  and  von  Witsch.     Gartenhauwiss., 
Cailahian.    C.  R.  Acad.  Sci.  U.R.S.S.,  12,  15,  226  (1940). 

443  (1936)  ;   27,  160,  253,  370  (1940)  ;  Heimann.     Planta  (Berl.),  38,  157  (1950)  ; 

31,  949  (1941)  ;    47,  220  (1945)  ;    54,  40,  377  (1952). 

735,  837  (1946)  ;   55,  69  (1947).  Herms.    J.  e.r;x  Zoo/.,  10,  167  (1911). 

1   Review,  see  Lang,  1952.  ^  p.  39. 

3  See  Buiming  (1937-50),  Bonner  and  Thurlow  (1949),  Bonner  (1949),  Harder  and 
van  Senden  (1949),  van  Senden  (1951).  Recent  research  indicates  that  the  gibberillins  are 
of  fundamental  importance  in  the  photoperiodism  of  plants. 


LIGHT  AND  METABOLISM                                      13 

Klebs.     i'^ora,  11-12,  128  (1918).  Tournois.     C.  R.  Acad.  Sci.  (Faris),  155, 

Lang.     Ann.  Rev.  Plant  Physiol,  3,  265  297  (1912). 

(1952).  Vegis.     Sijmbolae  Botan.,  Upsalienses,  14, 

Loeb.     Pfliigers  Arch.  ges.  Physiol. ,  54,  81  1  (1955). 

(1893)  ;    56,  247  (1894).  Verworn.     Psychophysiologische  Protisten- 

Loehwing.     Proc.  Soc.  exp.  Biol.  Med.,  37,  studien,  Jena  (1889). 

631  (1938).  Wareing.      Ann.    Rev.    Plant   Physiol.,   7, 

Melchers.  Biol.   Zhl.,  56,   567  (1936);   57,  191  (1956). 

568  (1937).  Wassink,SluysmansandStolwijk.Xonin^-/. 

Parker,  Hendricks  and  Borthvvick.    Botan.  tied.  Akad.    Wetens.    Proc,  53,    1466 

Gaz.,  Ill,  242  (1950).  (1950). 

Schubeler.    A'«?(/re  (Lond.).  21,  31 1  (1880).  Wassink  and  Stolwijk.     Ann.  Rev.  Plant 

van  Senden.    Biol.  Zbl.,  70,  537  (1951).  Physiol.,  7,  373  (1956). 

Smith,  F.     Meld.  Norg.  LandbrHoisk.,  12,  Withrow,    Withrow    and    Biebel.      Plant 

1  (1933).  Physiol.,  18,  294  (1943). 


PHOTOPERIODISM    IN    ANIMALS 

DIURNAL  METABOLIC  RHYTHMS  are  equally  remarkable  among 
animals,  for  the  cycle  of  day  and  night  with  its  rhythm  of  changes  in 
illumination,  temperature  and  other  environmental  factors  has  so 
impressed  itself  upon  living  creatures  in  the  course  of  their  palaeonto- 
logical  development  that  many  of  their  metabolic  processes  vary  with 
a  corresponding  periodicity,  synchronized  as  it  were  by  an  internal 
physiological  clock. 

These  physiological  rhythms  have  received  much  study  and  have  accumu- 
lated a  considerable  literature. ^  Among  Mammals,  including  Man,  the  periodicity 
of  sleep  and  activity  is  the  most  obvious, ^  possibly  a  survival  of  the  nocturnal 
reduction  of  nervous  activity  in  primaeval  Amphibians.  Most  animals  are 
diurnally  active  ;  but  in  nocturnal  animals  the  cycle  of  activity  is  reversed.^ 
A  similar  cyclic  variation  is  seen  in  bodily  temperature. ^^  In  Man  the  temperature 
through  the  day  is  higher  than  at  night,  but  considerable  variations  occur  in 
the  characteristics  of  the  curve  ;  in  some  individuals  the  peak  is  in  the  morning, 
in  others  in  the  afternoon  and  in  others  at  an  intermediate  .time.  The  blood 
constituents  show  a  variation  affecting  the  haemoglobin,  haematocrit  readings  and 
plasma  proteins,^  while  the  variation  in  the  eosinophil  count  is  dramatic  ;  in 
Man,  in  the  morning  there  is  an  eosinopenia*  ;  in  nocturnal  animals  such  as 
mice  the  count  is  high  in  the  morning  and  low  in  the  early  hours  of  the  night.' 
A  similar  rhythm  acting  independently  of  the  intake  of  fluid  affects  the  urinary 
output,  involving  not  only  the  excretion  of  water  but  also  that  of  electrolytes 
(Na,  K  and  chlorides,  etc.)  and  urea  which  persists  even  if  the  24-hour  day  is 
disrupted  for  periods  up  to  6  weeks. ^  Even  more  fundamental  cellular  processes 
are  involved  such  as  mitotic  activity  which  is  maximal  in  the  rest-period  at 

»  See  Kleitman  (1949),  Menzel  (1952),  Halberg  (1953).  Marker  (1958). 

2  See  Kleitman  (1939). 

3  Rat— Richter  (1922),  Browman  (1937)  ;  wood  rat— Colton  (1933)  ;  vole— Davis 
(1932)  ;  hedgehog— Herter(  1934)  ;  mice— Achelis  and  Nothdurft  (1939),  Aschoff(  1952), 
Kowalski  (1955)  ;    wikl  mice — Johnson  (1926). 

«  See  Kleitman  et  al.  (1937-38),  Kleitman  (1949),  Halberg  et  al.  (1953). 
«  Renbourn  (1947). 
*  von  Domarus  (1931). 
'  Halberg  and  Visscher  (1950-52). 

«  Gerritzen  (1936-40),  Mills  (1951),  Mills  and  Stanbury  (1952),  Mills  et  al.  (1954), 
Lewis  et  al.  (1956),  Lewis  and  Lobban  (1956). 


14  THE   EYE   IN  EVOLUTION 

midnight  and  minimal  at  noon,  a  rhythmic  variation  first  noted  in  plants  ^  and 
discovered  in  mammalian  tissues  (including  the  corneal  epithelium)  by  van 
Leijden  (1917),  confirmed  in  the  human  epidermis  by  Cooper  (1939)  and  noted 
in  the  cornea  of  tadjDoles  by  Meyer  (1954).^  It  is  interesting  that  it  is  a  physio- 
logical process  not  seen  in  cancer  cells.  As  will  be  fully  discussed  in  a  subsequent 
volume,  a  diurnal  variation  of  soine  3-5  inin.  Hg  occurs  in  the  ocular  tension.^ 

Established  by  constant  repetition,  these  rhythms  persist  for  some 
time  in  the  absence  of  environmental  reinforcement  when  the  external 
rhythm  has  been  artificially  altered  or  has  ceased.  The  mechanism  of 
these  changes  is  unknown  ;  most  of  them  are  probably  maintained  by 
rhythmic  changes  of  activity  in  the  neuro -vegetative  centres  of  the 
diencephalon,  while  the  endocrine  system,  particularly  the  pituitary 


70 

1^50 

=^     30 

^ 

^   eo 

'H;^^^;^^:.^^^ 

10 

0 

8         '°  ^M» 

Fig.  8. — The  Normal  Diurnal  Variation  in  the  Intra-ocular 
Pressure. 

The  abscissae  are  times  of  the  day  ;    the  vertical  line  denotes  when  the 
patient  was  asleep. 

complex,  probably  has  some  effect.  Apart  from  the  long-known 
centres  controlling  thermo-regulation  and  urinary  output,  functions 
such  as  the  variation  in  circulating  eosinophils  are  governed  by  the 
diencephalo-hypophyseal  system  through  the  secretion  of  cortico- 
steroids by  the  adrenal  cortex  (Hume,  1949  ;  Porter,  1953),  and  the 
evidence  is  rapidly  accumulating  that  a  region  in  the  same  neighbour- 
hood exerts  control  over  the  intra-ocular  pressure  (v.  Sallman  and 
Lowenstein,  1955  ;  Gloster  and  Greaves,  1957).  However  they  are 
controlled,  these  rhythms  are  real  and  autochthonous.  Thus  in  man 
the  normal  variation  in  temperature  persists  for  a  considerable  period 
after  the  commencement  of  habitual  night  work,  and  the  diurnal 
rhythm  of  urinary  flow  survives  a  uniform  intake  of  fluid  throughout 


Kellicott  (1904). 

See  Blumenfeld  (1939),  Halberg  (1953). 

Mailenikow  (1904)  ;    see  Duke-Elder  (1952). 


See  also  p.  560. 


LIGHT   AND  METABOLISM  15 

the  24  hours  and  the  reversal  of  the  sleep  habit.  Similarly,  the  normal 
phasic  swing  of  the  ocular  tension  is  independent  of  the  blood  pressure, 
osmotic  changes  in  the  blood,  illumination,  the  time  of  meals,  feasting 
or  fasting,  or  bodily  activity  ;  the  rhythm  can  only  be  altered  by  a 
complete  reversal  of  the  sleep  habit  established  over  some  time 
(Raeder,  1925)  (Fig.  8).  The  fact  that  such  rhythms  as  the  diurnal 
variation  in  temperature  in  the  new-born  infant,  or  the  24-hour 
periodicity  of  activity  of  the  newly  hatched  chick  kept  under  constant 
laboratory  conditions  (Aschoff  and  Meyer-Lohmann,  1954),  are 
apparent  from  birth  indicates  that  at  any  rate  some  of  these  fluctuations 
are  fundamental  and  innate — an  environmental  influence  of  biological 
value  which  has  with  time  so  impressed  itself  upon  organisms  that  it 
has  become  hereditarily  transmitted. 

Some  of  these  diurnal  variations,  however,  seem  to  depend  on  environ- 
mental stimulation.  Thus  the  cyclic  variation  in  the  eosinophil  count  of  mice 
was  found  by  Halberg  and  his  associates  (1954)  to  be  abolished  by  the  enucleation 
of  both  eyes,  although  it  partially  returned  some  5  months  after  blinding.  The 
rhythm  of  diurnal  activity  of  the  minnow,  Phoxinus,  is  said  to  be  reversed  on 
blinding  (Jones,  1956).  In  man  the  variation  in  eosinophilia  depends  to  some 
extent  on  activity  (Halberg  et  al.,  1953),  and  illumination  has  a  subsidiary 
influence  (Appel  and  Hansen,  1952  ;   Landau  and  Feldman,  1954). 

The  same  rhythms  in  general  activity  are  seen  in  Invertebrates, 
among  which  Insects  provide  some  of  the  most  dramatic  examples  (see 
Welsh,  1938  ;  Wigglesworth,  1953).  The  habit  of  nocturnal  activity 
and  diurnal  catalepsy  show^l  by  the  stick-insect,  Dixippus,  for  example, 
persists  unchanged  for  some  days  in  permanent  darkness  or  in  reversed 
illumination  (Steiniger,  1933),  a  daily  rhythm  which  applies  to  such 
activities  as  defsecation  and  ovij^osition  (Kalmus,  1938).  The  same 
general  tendency  is  seen  in  many  other  species.^  The  rhythm  may, 
indeed,  be  acquired  in  the  larval  stage  in  response  to  diurnal  changes 
of  light,  persist  through  the  pupal  stage  and  determine  the  activity  in 
the  adult. 2  A  metabolic  rhythm  in  which  the  CO2  is  higher  (some- 
times by  30%)  during  the  night  even  although  the  animal  is  kept  in 
constant  darkness  is  seen  in  Crustaceans.^  A  similar  diurnal  rhythm 
of  the  opening  and  closing  of  the  valves  of  the  clam,  Venus  mercenaria, 
persists  under  laboratory  conditions  of  constant  illumination  ;  it  is 
interesting  that  in  this  case  there  is  also  a  persistent  tidal  rhythm  and 
the  interaction  of  the  two  produces  a  lunar  cycle  (Bennett,  1954).  A 
similar  phenomenon  whereby  an  endogenous  tidal  rhythm  displaces 

^  It  is  seen  in  some  forest  insects  (Lutz,  1932  ;  Park  and  Keller,  1932),  mayflies 
(Harker,  1953),  cockroaches  (Gunn,  1940  ;  Mellanby,  1940  ;  Marker,  1954),  millipedes 
(Park,  1935),  and  other  species. 

2  In  Leptinoiarsa — Grison  (1943). 

^  The  crab,  Carcinus — Menkes  (1952)  ;  the  woodlouse,  Oniscus — Cloudesley- 
Thompson  (1952). 


16  THE   EYE   IN  EVOLUTION 

the  endogenous  diurnal  rhythm,  is  seen  in  the  fiddler-crab,  Uca 
(Brown  et  al.,  1952-54)  and  also  in  marine  forms  of  the  protozoon, 
Euglena  (Pohl,  1948).  A  lunar  as  well  as  a  diurnal  rhythm  of  activity 
and  oxygen  consumption  is  seen  in  the  earthworm,  Lumbriciis  (Ralph, 
1957),  and  in  crayfish  such  as  Cambarus  virilis  (Guyselman,  1957). 
The  timing  of  these  rhythms  with  respect  to  the  solar  day  when  the 
animals  are  kept  in  darkness  has  been  altered  by  lowering  the  tem- 
perature (the  fiddler-crab,  Uca,  Stephens,  1957). ^ 

THE  SEXUAL  CYCLE  OF  ANIMALS,  as  with  flowering  in  plants,  is  also 
frequently  determined  by  the  influence  of  light  as  expressed  by  the 
gradual  change  in  the  length  of  day  in  the  annual  solar  cycle  ;  in  this 
way  the  onset  of  the  breeding  season  becomes  rhythmic  as  though 
there  has  been  implanted  on  the  central  nervous  and  hormonal 
systems  a  pattern  of  behaviour  automatic  and  innate  so  that  it  can 
only  be  altered  experimentally  by  a  prolonged  disturbance  of  the 
natural  phases.  In  some  species,  it  is  true,  particularly  in  Invertebrates 
and  the  lower  Vertebrates,  other  factors  such  as  temperature  and 
humidity  also  enter  into  the  question,  but  controlled  experiments  have 
shown  that  these  and  other  extraneous  circumstances,  such  as  physical 
activity  and  feeding,  are  often  secondary  and  in  many  cases  can  be 
excluded  and  that  the  most  important  factor  is  the  duration  of  the 
period  of  light — not  its  intensity  or  wave-length.  These  phenomena 
have  been  particularly  studied  in  animals  inhabiting  the  northern 
hemisphere.  Spring  in  these  regions  with  its  increasing  days  is  the 
appropriate  season  for  reproduction  if  survival  is  to  be  maintained, 
and  in  those  species  with  a  long  gestation  period,  the  shortening  days 
of  autumn  are  most  suitable  for  mating.  In  general,  when  species  with 
a  breeding  periodicity  of  this  type  are  experimentally  subjected  to 
artificially  lengthening  days  in  late  autunrn  or  winter,  they  can  be 
brought  from  their  sexually  quiescent  condition  into  the  ripeness 
typical  of  spring,  while  conversely,  if  the  lengthening  days  of  spring 
are  artificially  curtailed,  sexual  regression  occurs  ;  indeed,  it  is  possible 
by  these  means  to  bring  some  types  (birds,  for  example)  into  breeding 
condition  several  times  in  the  year — a  change  which  applies  not  only 
to  anatomical  considerations  such  as  the  development  of  the  gonads, 
but  also  to  those  habits  and  modes  of  conduct  which  are  'essentially 
sexual  in  origin  such  as  (in  birds)  singing  and  migration. 

Such  phenomena  have  been  investigated  in  many  species  of  Inverte- 
brates, Fishes,  Amphibians,  Reptiles,  Birds  and  Mammals. 

In  the  INVERTEBRATES,  even  among  Protozoa,  Ehret  (1951)  found  that 
the  diurnal  rhythm  of  the  mating  reaction  of  Paramceciuni  bursaris  persists  for 
several  days  in  complete  darkness  and  can  be  altered  by  varying  the  illumination 

^  Compare  p.  22. 


LIGHT   AND   METABOLISM  17 

at  different  periods  of  the  daily  cycle.  In  snails,  a  prolongation  of  the  diurnal 
period  of  light  beyond  13  hours  stimulates  egg-laying,  while  periods  of  11  hours 
or  less  inhibit  it  (Jenner,  1951)  ;  it  is  interesting  that  short  intervals  of  illumina- 
tion during  the  dark  periods  of  a  short-day  cycle  stimulate  egg-laying,  showing 
that,  as  with  short -day  plants,  the  length  of  the  dark  period  is  an  essential 
feature  in  the  stimulus.  Similarly  the  strawberry -root  louse.  Aphis  forbesi,  can 
be  made  to  breed  in  midsummer  instead  of  February  by  artificially  curtailing 
the  summer  days  (Marcovitch,  1923).  A  more  dramatic  influence  is  seen  in  the 
plant-louse,  Psylla  :  individuals  hatched  in  autumn  differ  from  those  hatched 
in  spring  but  the  winter-type  can  be  produced  in  spring  by  subjecting  the  larv£e 
to  an  artificial  diurnal  rhythm  in  which  the  period  of  light  is  shortened  (Bonne- 
maison  and  Missonnier,  1955). 

Among  FISHES,  temperature  has  been  shown  to  be  a  potent  factor,  but  it 
has  been  demonstrated  that  the  reproductive  cycle  of  the  trout  can  be  photo- 
periodically  determined  (Hoover  and  Hubbard,  1937)  ;  similarly  the  activity 
of  the  gonads  of  certain  amphibians  such  as  the  clawed  toad,  Xenopus  Icevis, 
(Shapiro  and  Shapiro,  1934)  and  reptiles  such  as  the  lizard,  Anolis  carolinensis 
(Clausen  and  Poris,  1937),  has  been  altered  by  means  of  artificial  illumination. 

BIRDS  show  more  dramatic  changes  than  most  species,  and  these  have 
received  much  attention  probably  because  of  their  obvious  habits  of  migration 
and  singing,  the  sexual  connection  of  which  has  been  recognized  since  the  time 
of  ArLstotle.  For  long  the  annual  rhythm  of  the  avian  gonad  was  held  to  be 
determined  bj^  temperature.  It  is  true  that  in  the  old  custom  of  "  muit  "  long 
prevalent  in  Holland,  birds  were  brought  into  song  in  autumn  by  confining  them 
in  the  dark  in  the  middle  of  June  and  exposing  them  to  light  in  September,  and 
that  by  the  similar  ancient  practice  of  "yogai",  Japanese  pet  birds  were  brought 
into  singing  condition  in  January  by  providing  them  with  extra  hours  of 
illumination  in  the  autumn  (Miyazaki,  1934).  In  this  respect,  however,  zoologists 
waited  on  botanists  ;  for  although  Schafer  (1907)  had  suggested  that  migration, 
because  of  its  accurate  periodicity,  must  depend  on  the  mathematically  regular 
changes  in  length  of  day  rather  than  on  the  notoriously  irregular  variations  in 
climate,  it  was  not  until  the  work  of  C4arner  and  AUard  on  the  influence  of  photo- 
periodism  on  the  flowering  of  plants  had  been  published  in  1920  ^  that  Eifrig 
(1924)  propounded  a  similar  hypothesis  to  explain  the  habits  of  birds,  a  con- 
ception eventually  proved  by  the  experimental  work  of  Rowan  (1925-38). 

Rowan's  classical  work  was  on  the  junco  finch,  which  migrates  from  wintering 
grounds  in  the  middle  United  States  to  Alberta  ;  he  found  that  even  if  the  birds 
were  retained  in  an  aviary  in  Alberta,  provided  they  were  subjected  to  the 
artificial  increase  of  daily  illumination  (2-3  mins.)  that  they  would  have 
experienced  in  the  early  spring  in  the  States,  their  gonads  matured  and  they 
bvirst  into  song  in  December  despite  the  temperature  of  the  Canadian  winter 
(minimum,  —  50^F).  These  results  were  confirmed  by  Bissonnette  (1930-32) 
in  Connecticut  experimenting  on  starlings  ;  and  it  is  now  amply  established 
that  among  many  birds  of  the  temperate  zones  of  the  northern  hemisphere,  the 
testes  of  which  normally  reach  a  peak  of  activity  as  the  days  lengthen  in  late  . 
spring,  an  artificial  increase  of  the  period  of  illumination  over  some  time  brings 
on  a  precociovis  activity,  while  a  curtailment  or  denial  of  light  brings  on  the 
reverse  changes.-    On  the  other  hand,  confinement  of  male  parrots  in  continuous 

1  p.  10. 

2  See  among  others  :  junco,  Junco  hyemalis — Rowan  (1929),  Jenner  and  Engels 
(1952)  ;  starling,  Slurnus  vulgaris — Bissonnette  (1930-32)  ;  pheasant — Martin  (1935), 
B.  C.  Clark  et  al.  (1936-37)  ;  house  span-ow.  Passer  domesticus — Riley  (1936),  Kirsch- 
baum    and    Ringoen    (1936)  ;     white-throated    sparrow — Jenner    and   Engels    (1952)  ; 

S.O. — VOL.  I.  2 


THE   EYE   IN   EVOLUTION 

darkness  for  a  month  results  in  testicular  activity,  while  continuous  illumination 
produces  a  resting  state  (Vaugien,  1952).  The  same  result  follows  a  "  natural  " 
change  in  the  day-night  cycle,  for  if  the  birds  in  the  northern  hemisphere  are 
transported  to  the  southern,  their  breeding  season  is  reversed  (Rowan,  1926)  ; 
while  in  regular  migrants  across  the  equator  the  stimulus  for  the  recrudescence 
of  sexual  activity  and  enlargement  of  the  gonads  is  the  shortening  of  the  days 
in  March  in  southern  lands  (Rowan,  1938),  an  inherent  habit  which  can  only  be 
broken  if  such  species  are  retained  for  several  years  in  the  southern  hemisphere 
and  prevented  from  migrating  (Marshall,  1937  ;  Baker  and  Ranson,  1938).  It 
would  therefore  seem  established  that  the  sexual  cycle  and  the  migration  of 
birds,  rhythins  which  have  become  innate,  are  determined  essentially  by  photo- 
period,  although  it  is  to  be  remembered  that  periods  of  darkness  may  have  an 
influence  equal  to  or  even  more  potent  than  light  (Hammond,  1953  ;  Kirk- 
patrick  and  Leopold,  1953),  while  temperature  also  has  an  adjuvant  effect 
(Bissonnette,  1937  ;   Farner  and  Mewaldt,  1952-53  ;   Wilson  et  al.,  1956). 

Similarly  among  mammals,  male  ferrets,^  mice  ^  and  ewes  ^  can  be  brought 
into  oestrus  in  winter  when  normally  they  are  in  anoestrus  by  subjecting  them  to 
rhythmic  periods  of  increased  illumination  for  2  months  or  more,  while  the 
gonads  of  the  field-mouse  have  been  shown  to  diminish  by  exposing  the  animals 
to  increased  periods  of  darkness  (Baker  and  Ranson,  1932).*  As  would  be 
expected,  these  changes  do  not  apply  to  non-seasonable  animals  ^  or  those  that 
reach  sexual  maturity  dviring  hibernation  ®  or  aestivation.^  Among  those  animals 
in  which  it  is  operative,  however,  and  particularly  among  those  with  migratory 
habits,  the  periodic  behaviour  thus  induced  sometimes  assumes  legendary 
exactitude,  a  fact  commented  on  since  the  days  of  Pliny  ;  the  cuckoo  arrives 
in  England  on  "Cuckoo  Day",  the  early  stream  of  swifts  is  expected  to  arrive 
on  the  last  three  days  of  April  and  the  big  arrival  on  May  24th,  while  in  the  late 
autumn  each  year  the  male  markhor  is  said  to  descend  from  the  high  Hindu 
Kush  into  the  valleys  to  meet  the  females  on  December  14th  precisely,  and  the 
rut  begins  (Burton,  1951).* 

The  mechanism  of  the  action  of  hght  in  these  photoperiodic 
activities  varies,  but  in  general  is  mediated  through  hormones  the 
activity  of  which  is  largely  determined  by  stimulation  through  the 
eyes.  This  complex  matter  will  be  discussed  subsequently,^  but  at  this 
stage  it  is  convenient  to  note  that  in  Crustaceans,  several  hormones  are 

white-crowned  sparrow — Farner  et  al.  (1953) ;  dove,  Zenaidura  macroura — Cole  (1933) ; 
Japanese  white-eye,  Zosterops — Miyazaki  (1934)  ;  duck — Benoit  (1934-35),  Radnot 
(1953-55)  ;  quail— B.  C.  Clark  et  al.  (1936-37),  Hammond  (1953)  ;  fowl— Radnot 
(1955),  Radnot  and  Orban  (1956). 

1  Bissonnette  (1932),  Marshall  and  Bowden  (1934-36),  Hart  (1951),  Thomson 
(1954). 

2  Whitaker  (1936). 
»  Hafez  (1951). 

*  For  further  details  of  the  mechanism  involved,  see  p.  559. 

5  Guinea-pigs — Dempsey  et  al.  (1933-34)  ;   rabbit — Smelser  et  al.  (1934). 
«  Squirrel— Wells  (1934-35),  Johnson  and  Gann  (1933). 
'  Alexander  and  Bellerby  (1935-38),  Bellerby  (1938). 

*  In  a  similar  manner  the  palolo  (Polych^te)  worms  of  the  South  Pacific  shed  their 
eggs  or  sperms  in  countless  millions,  sufficient  to  give  the  sea  the  appearance  of 
vermicelli  soup,  at  a  specific  time.  These  are  eminently  edible,  and  the  natives  of 
Samoa  have  learned  to  expect  a  great  feast  precisely  at  dawn  one  week  after  the 
November  full  moon. 

*  p.  547. 


LIGHT   AND  METABOLISM  19 

secreted  in  the  eye -stalks  and  central  nervous  system  and  stored  in  the 
sinus  glands  and  these  regulate  ovarian  maturation  and  testicular 
development.  In  Vertebrates  the  pituitary  gland  exerts  an  analogous 
gonadotropic  influence  under  the  control  of  its  associated  centres  in 
the  diencephalon  which  in  turn  receive  their  stimulation  from  the 
retinae. 1 

PHOTOPERiODiSM  IN  PIGMENT  MIGRATION.  Pigment,  the  fuuction 
of  which  is  so  closely  related  to  light,  would  be  expected  to  be  peculiarly 
susceptible  to  its  influence  ;  in  its  migration  to  cause  colour  changes,^ 
rhjrthmic  diurnal  variations  of  a  primitive  type  frequently  survive. 
That  a  persistent  rh}i:hm  of  this  kind  occurs  in  the  migration  of  the 
retinal  pigment  ^  in  the  eyes  of  a  noctuid  moth,  Phisia  garmna,  was  first 
reported  by  Kiesel  (1894),  an  observation  which  has  been  repeated  in 
several  Arthropods  with  compound  eyes  and  shown  to  persist  even 
although  the  animals  are  kept  for  a  considerable  time  in  conditions  of 
constant  illumination  and  temperature  or  are  reared  from  the  larval 
stage  in  the  laboratory  in  constant  darkness.*  The  effect  is  well  seen 
in  the  crayfish  in  the  eye  of  which  there  is  a  tapetal  reflecting  pigment  ^ 
obscured  during  the  day  but  unprotected  at  night  so  that  the  eye 
then  assumes  an  orange  glow  ;  even  if  the  animal  is  kept  in  conditions 
of  constant  darkness  and  temj^erature,  the  diurnal  rhythm  of  orange 
"  eye-shine  "  at  night  will  continue  automatically  for  months  (Welsh, 
1941).  Similar  rh}i;hms  affecting  the  retinal  and  tapetal  pigments  are 
seen  in  many  species  of  Crustaceans  (Henkes,  1952),  and  it  would 
appear  that  these  pigmentary  movements  are  under  hormonal  control, 
a  subject  which  will  be  discussed  in  a  later  chapter.^ 

Closely  associated  with  the  movements  of  the  retinal  pigment  are  the 
corresponding  movements  of  the  rods  ayid  cones  of  some  of  the  lower  Vertebrates. 
As  with  the  retinal  pigment,  these  movements  are  usually  a  direct  response  to 
light,  but  evidence  was  produced  by  Welsh  and  Osborn  (1937)  that  these  elements 
in  the  eye  of  the  catfish  underwent  a  diui-nal  rhythmic  change  of  position  even 
although  the  fish  were  kept  in  constant  darkness  ;  the  mechanism  of  this 
rhythmic  activity  is  unknown. 

The  integumentary  cliromatopliore  sy stein  frequently  shows  similar 
cyclic  activities.  The  responses  of  this  pigmentary  system  to  light  are 
complex  and  will  be  studied  in  a  laier  section  ^  ;  it  is  sufficient  to  note 
here  that  many  animals  show  a  rhji;hmic  day-night  change  of  colour 
wherein  they  pale  by  night  and  darken  by  day,  a  rhythm  which  may 
persist  for  a  considerable  time  if  they  are  kept  in  conditions  of  constant 

1  p.  556.  2  p_  go.  3  p_  170. 

*  In  the  beetle,  Bolitotherus  cornutus — Park  and  Keller  (1932)  ;  and  a  number 
of  Crustaceans  such  as  fresh-water  shrimps,  Macrohrachium  and  others — Welsh  (1930)  ; 
crayfish,  Cam6a rws—Bennitt  (1932),  Welsh  (1939-41)  ;  crab,  C7ca— Smith  (1948); 
Brown  et  al.  (1951-54),  Kleinholz  (1937)  ;    and  so  on. 

6  p.  165.  «  p.  547.  '  p.  82. 


20 


THE   EYE   IN   EVOLUTION 


illumination  or  darkness.^  Gamble  and  Keeble  (1900)  first  reported 
such  a  cyclic  diurnal  colour  change  which  persisted  under  constant 
illumination  in  the  prawn,  Hippolyte  varians,  but  although  subsequent 
work  has  not  confirmed  this  particular  observation  (Kleinholz  and 
Welsh,  1937),  the  phenomenon  has  been  demonstrated  in  a  number  of 
species  of  both  Invertebrates  and  the  lower  Vertebrates.-  In  some 
cases  these  diurnal  changes  are  largely  masked  by  other  factors  such 
as  pigmentary  changes  adopted  to  mimic  the  background,^  but  the 

Figs.  9  and   10. — Diurnal  Rhythms  in  the  Pigment  of  the  Crab,   Uca. 

The  black  and  white  segments  at  the  top  of  the  graphs  and  in  the  corre- 
sponding position  immediately  below  the  graphs  represent  the  normal  rhythm 
of  daylight  and  darkness.  The  second  tier  of  markings  below  indicate  the 
experimental  variations  introduced.  Ordinates  :  the  degree  of  pigmentation 
expressed  in  Hogben  and  Slome's  scale,  1  representing  complete  concentration 
of  pigment,  i.e.,  the  light  phase,  and  5  its  complete  dispersal,  i.e.,  the  dark 
phase  (Brown  and  Webb,  1949). 


!   ^  '^^^  ^u\^^^  Aj\     , 

U-t--^  -  -  -V--  -V  '^- 

l^ri 

]                                             V   V 

'  J  U  U  U  U  U  U  LLLLL^Ms, 

Fig.  9. — The  normal  diurnal  rhythm  of 
pigmentation  (dark  through  the  day 
and  light  at  night)  is  seen  to  continue 
uninterruptedly  after  the  animal  has 
been  9  days  in  darkness. 


Fig.  10. — At  the  beginning  of  the  experiment  Uca 
was  exposed  to  continuous  illumination  (80  foot 
candles)  from  A  to  B.  There  is  a  decrease  in 
amplitude  and  then  a  gradual  inhibition  of  the 
rhythm  until  eventually  the  chromatophores 
change  irregularly.  At  B  the  animals  were  trans- 
ferred to  continuous  darkness,  whereupon  the 
chromatophores  becaine  almost  completely  con- 
centrated and  thereafter  a  normal  24-hour  rhythm 
in  phase  with  solar  day-night  was  observed. 


effect  of  the  underlying  rhythm  is  seen  in  the  increased  rapidity  of 
these  secondary  responses  when  they  are  in  phase  with  the  primary 
diurnal  cycle  and  their  sluggishness  when  they  antagonize  it.  In  other 
animals  the  fundamental  rhythm  is  preponderant  so  that  secondary 

1  8  to  9  weeks  in  the  beach-louse,  Idotea — Menke,  (1911)  ;  18  days  in  the  lizard, 
Anolis — Rahn  and  Rosendale  (1941)  ;   and  so  on. 

^  Several  Invertebrates  such  as  the  black  sea-urchin,  Diadema  antillarum — Millott 
(1950)  ;  many  Crustaceans  in  addition  to  Idotea  :  the  prawn,  Paloemon — Keeble 
and  Gamble  (1904),  the  fiddler  crab,  Uca — Abramowitz  (1937),  the  Isopod,  Ligia — 
H.  Smith  (1938)  ;  a  few  Insects  such  as  the  stick-insect,  Dixippus — Schleip  (1910). 
Compare,  for  example,  Figs.  64-68. 

A  number  of  Vertebrates,  particularly  in  their  youth  (Cf.  Figs.  70  and  73)  ;  Cyclo- 
stomea  such  as  the  lampern,  Lampetra — Young  (1935),  Jones  (1955)  ;  Amphibians 
such  as  salamander  larva*  and  frogs — Hooker  (1914),  Welsh  (1938)  ;  and  Reptiles  such 
as  the  American  horned  "toad",  Phrynosortui — Redfield  (1918),  the  lizard,  Anolis — 
Rahn  and  Ro  i»ndale  (1941),  and  the  chameleon — Zoond  and  Eyre  (1934). 

3  p.  82. 


LIGHT   AND   METABOLISM  21 

environmental  factors  have  but  a  slightly  modifying  effect  upon  it.  A 
good  example  of  this  is  the  crab,  Uca,  the  responses  of  which  have  been 
extensively  studied  i  ;  the  diurnal  rhythm  of  its  colour  change  is 
remarkably  constant,  and  within  wide  limits  is  independent  of  influences 
such  as  humidity  and  temperature,  but  the  influence  of  metabolism  on 
the  phenomenon  is  exemplified  in  its  retardation  with  a  lengthening  of 
the  cycle  on  exposure  to  cold  below  6°  C  (Figs.  9  and  10). 

This  rhythmic  mechanism  operating  to  disperse  pigment  in  the 
day  phase  and  concentrate  it  in  the  night  phase  of  the  cycle  would 
seem  to  be  adaptive  in  function,  partly  protective  against  deleteriously 
bright  illumination,  partly  thermo-regulatory.  In  all  species  in  which 
these  colour  changes  occur  the  controlling  factors  are  hormones 
differing  in  nature  from  the  retinal  pigment  hormones  but,  like  them, 
elaborated  in  Invertebrates  by  the  neuro -secretory  system  and  in 
Vertebrates  by  the  neurohypophysis  both  of  which  show  an  endo- 
genous rhythm.  This  question  will  be  discussed  in  a  subsequent 
chajDter.^ 

The  seasonal  changes  in  colour  of  the  coats  of  many  Birds  and 
Mammals  are  analogous  phenomena  which  are  also  to  some  extent 
determined  by  photoperiod.  It  is  well  known  that  the  majority  of 
common  birds  undergo  a  post-nuptial  moult  immediately  after  the 
breeding  season  and  a  second  pre-nuptial  moult  in  spring  when  they 
assume  their  wedding  robes.  The  times  at  which  birds  assume  their 
nuptial  and  winter  plumages  are  governed  by  a  number  of  factors,  the 
most  potent  of  which  is  a  pituitary  hormone  with  an  inherent  cyclic 
activity  depending  in  part  on  the  length  of  the  daily  light  periods 
(Witschi,  1935  ;  Bro\\Ti  and  Rollo,  1940  ;  Lesher  and  Kendeigh,  1941  ; 
Kobayashi  and  Okubo,  1955).  A  similar  control  operates  the  seasonal 
moulting  of  many  northern  Birds  and  Mammals  the  colours  of  which 
change  from  a  sinnmer  brown  to  a  winter  white. 

Among  Birds,  the  ptarmigan  of  the  northern  tundra  or  the  high  mountains 
(Host,  1942),  and  among  Mammals  the  varying  hare  (Lyman,  1943)  and  the 
ermine  (Bissonnette  and  Bailey,  1944)  are  good  examples  of  this  ;  these 
phenomena  of  moulting  and  change  of  colour  can  be  induced  out  of  season  by 
artificially  varying  the  diurnal  periods  of  ilkimination.  It  is  interesting  that  in 
the  hare  the  eyes  seem  to  be  the  normal  receptors  of  this  stimulus  since  if  these 
are  masked  the  changes  do  not  occur.  The  pituitary  seems  to  be  the  only 
endocrine  gland  involved  since  castration  and  thyroidectomy  in  the  hare  are 
without  effect  (Lyman,  1943),  while  hypophysectomy  abolishes  the  cyclic 
moulting  of  ferrets  (Bissonnette,  1935-38). 

PHOTOPERiODiciTY  IN  BiOLUMiNESCENCE.  The  ability  to  produce  light 
occurs  widely  but  sporadically  among  bacteria,  fungi,  and  most  types  of  animals 

1  Abramowitz  (1937-38),  Browii  and  Webb  (1947-49),  Brown  and  Sandeen  (1948), 
Webb  (1950). 

2  p.  547. 


22  THE   EYE   IN   EVOLUTION 

from  the  Protozoa  to  the  chordate  Fishes  ;  it  is  a  phenomenon  which  will  be 
discussed  in  greater  detail  later. ^  It  is  well  known  that  in  most  animal  species 
the  reaction  appears  intermittently  in  response  to  various  stimuli,  light  having 
a  general  inhibitory  effect,  sometimes  directly  by  destruction  of  the  photogenic 
material  in  the  light-producing  cells,  sometimes  indirectly,  acting  through  a 
central  regulatory  mechanism,  hormonal  or  nervous  (Harvey,  1925  ;  Heymans 
and  Moore,  1925  ;  Moore,  1926).  In  the  present  connection  it  is  interesting  to 
remark  that  in  a  number  of  species  there  is  a  daily  rhythm  in  the  capacity  to 
luminesce,  a  phenomenon  seen  even  in  unicellular  Dinofiagellates  (Harvey, 
1952);  and  in  some  types  of  Insects  ^  and  perhaps  in  some  jellyfish^  and  a 
balanoglossid  *  the  rhythm  may  persist  for  several  days  so  that  the  animal 
will  light  up  at  the  normal  time  of  the  day  even  if  kept  in  constant 
darkness. 

A  final  expression  of  diurnal,  khythmicity  is  seen  in  the  time -memory 
OF  SOME  AUTHROPODS  AND  BIRDS.  This  curious  and  interesting  phenomenon 
was  first  demonstrated  in  bees  by  von  Stein-Beling  (1929-35)  who  showed  that 
within  a  cycle  of  24  hours  bees  could  be  trained  to  visit  an  artificial  feeding 
station  at  regular  occasions  throughovit  the  day,  a  habit  which  could  not  be 
maintained  if  an  attempt  were  made  to  operate  within  a  cycle  greater  or  less 
(e.g.,  19  hours)  than  the  normal  solar  diurnal  rhythm.  This  ability  has  since 
been  verified  by  a  number  of  observers  ^  and  it  has  been  confirmed  in  wasps  ® 
and  ants  ^  as  well  as  in  the  Amphipod  Talitrus.^  So  far  as  honey -gathering 
insects  are  concerned  it  is  probably  connected  with  the  hours  at  which  flowers 
periodically  offer  their  nectar,  but  other  activities  are  also  involved.  Thus 
Kalmus  (1935)  found  that  if  larvae  and  pupse  of  Drospohila — an  insect  which 
normally  emerges  from  its  pupa  before  dawn — were  kept  in  darkness  during  the 
daytime  and  artificially  illuminated  for  3  consecutive  nights,  the  flies  emerged 
in  the  evenings,  remembering  the  time  of  the  artificial  dawn  even  although  kept 
in  perpetual  darkness.  Such  time-keeping  mechanisms  or  "  internal  clocks  " 
are  of  wide  occurrence,  keeping  time  automatically  with  considerable  precision, 
but  regularly  set  and  kept  in  pace  by  light  stimuli.  It  would  seem  that  the 
rhythm  is  influenced  metabolically  since  it  can  be  retarded  by  low  temperatures 
(under  5°  C,  Kalmus,  1934)  or  by  drugs  ;  thus  Grabensberger  (1934)  found  that 
by  feeding  quinine  to  trained  bees,  arrival  at  the  sources  of  food  was  retarded, 
while  it  was  accelerated  by  iodothyroglobin. 

A  similar  apparently  innate  time-sense  can  be  deinonstrated  in  some  Birds, 
which  we  will  see  ^  assvunes  considerable  importance  in  their  extraordinary 
ability  to  navigate  over  long  distances.  Thus  Stein  (1951)  found  that  passerine 
birds  could  be  trained  to  coqie  to  feed  at  a  particular  hour  each  day  provided 
only  that  a  24-hour  cycle  were  maintained,  an  acquirement  retained  for  some 
considerable  time  although  the  birds  were  kept  in  constant  illumination  or  had 
irregular  feeding  times  ;  experimental  exposure  to  irregular  periods  of  light  and 
darkness,  however,  tends  to  disorientate  this  sense  when  it  is  used  as  an  aid  to 
navigation  (Matthews,  1953-55). 

1  p.  736. 

2  Such  as  the  firefly,  Photinus—Bxic'k  (1937). 
^  Pelagia — Heymans  and  Moore  (1924-25). 

*  Ptychodera—CrozieT  (1920). 

5  Wahl  (1933),  Kalmus  (1934-54),  Kleber  (1935),  v.  Frisch  (1937),  and  others. 

6  Verlaine  (1929). 

'  Grabensberger  (1934). 

8  Pardi  and  Papi  (1952-53), 

«  p.  63. 


LIGHT   AND   METABOLISM 


23 


Abramowitz.     Biol.  Bull.,  72,  344  (1937). 

J.  exp.  Zool.,  76,  407  (1938). 
Abramowitz  and  Abramowitz.    Biol.  Bull 

74,  278  (1938). 
Acholis   and   Nothdurft.      Pflilgers   Arch. 

ges.  Physiol.,  241,  651  (1939). 
Alexander  and  Bellerby.    J.  exp.  Biol.,  12 

306  (1935)  ;    15,  74  (1938). 
Appel   and   Hansen.      Dtsch.   Arch.   klin. 

Med.,  199,  530  (1952). 
Aschoff.     Pflilgers  Arch.  ges.  Physiol.,  255, 

189,  197  (1952). 
Aschoff   and    Meyer-Lohmann.      Pfliigers 

Arch.  ges.  Physiol.,  260,  170  (1954). 
Baker  and   Ranson.      Proc.   roy.  Soc.   B, 

110,  313  ;    112,  39  (1932)  ;    113,  486 
(1933). 

Proc.  zool.  Soc.  Lond.,  108A,  101  (1938). 
Bellerby.    J.  exp.  Biol.,  15,  82  (1938). 
Bennett.     Biol.  Bull.,  107,  174  (1954). 
Bennitt.     Physiol.  Zool.,  5,  65  (1932). 
Benoit.    C.  R.  Acad.Sci.  (Paris),  199,  1671 
(1934)  ;   201,  359  (1935). 
C.  R.  Soc.  Biol.  (Paris),  118,  664,  669, 
672;    120,136,905,1326(1935). 
Bissonnette.    .4wer.  J.  ^4?k;/.,  45,  289  ;  46, 
477  (1930). 
J.  exp.  Zool.,  58,  281  (1931). 
Physiol.    Zool.,   4,    542    (1931)  ;     5,    92 

(1932). 
Proc.  roy.  Soc.  B.,  110,  322  (1932). 
Anat.  Rec,  63,  159  (1935). 
Wilson  Bull.,  49,  241  (1937). 
Endocrinology,  22,  92  (1938). 
Bissonnette  and  Bailey.    Anti.  N.Y.  Acad. 

Sci.,^5,  221  (1944). 
Blumenfeld.    Science,  90,  446  (1939). 
Bonnemaison  and  Missonnier.  C.  R.  Acad. 

Sci.  (Paris),  240,  1277  (1955). 
Browman.    J.  exp.  Zool.,  75,  375  (1937). 
Brown,  Fingerman  and  Hines.    Biol.  Bull., 

106,  308  (1954). 
Brown,  Fingerman,  Sandeen  and  Webb. 

J.  exp.  Zool.,  123,  29  (1952). 
Brown  and  Rollo.    T/ie.4!<A-,57,485  (1940). 
Brown  and  Sandeen.     Physiol.  Zool.,  21, 

361  (1948). 
Brown,  Sandeen  and  Webb.     Anat.  Rec, 

111,  569  (1951). 

Brown  and  Webb.     Anat.   Rec,  99,   674 

(1947)  ;    101,  733  (1948). 
Physiol.  Zool.,  21,  371  (1948)  ;    22,  136 

(1949). 
Buck.     Physiol.  Zool.,  10,  412  (1937). 
Burton.      Illust.    Lond.    News,    223,    996 

(1951). 
Clark,  B.  C.,  Leonard  and  Bump.    Science, 

83,  268  (1936)  ;   85,  339  (1937). 
Clausen   and   Poris.     Anat.   Rec,   69,    39 

(1937). 
Cloudesley-Thompson.     J.  exp.  Biol.,  29, 

295  (1952). 
Cole.     T/ieylw/l-,  50,  284  (1933). 
Colton.    J.  MammoL,  14,  309  (1933). 
Cooper.    J.  invest.  Derm.,  2,  289  (1939). 
Crozier.     Anat.  Rec,  20,  186  (1920). 


Davis.    J.  ani7n.  EcoL,  2,  232  (1932). 
Dempsey,   Young,    Myers   and  Jennison. 

Anat.  Rec,  57,  Suppl.,  29  (1933)  ;  58 

Suppl.,  59  (1934). 
Arner.  J.  Physiol.,  109,  307  (1934). 
von  Domarus.     Dtsch.  Arch.  klin.  Med., 

171,  333  (1931). 
Duke-Elder.      Amer.   J.    Ophthal.,    35,    1 

(1952). 
Ehret.    Anat.  Rec,  111,  528  (1951). 
Eifrig.     The  Auk,  41,  439  (1924). 
Earner   and   Mewaldt.     Anat.   Rec,   113 

612,  (1952). 
Experientia,  9,  219  (1953). 
Earner,  Mewaldt  and  Irving.    Science,  118, 

351  (1953). 
von  Frisch.     Z.  Tierpsychol.,  1,  9  (1937). 
Gamble  and  Keeble.    Quart.  J.  micr.  Sci., 

43,  589  (1900). 
Gerritzen.      Acta    med.    scand.,    89,    101 

(1936)  ;    Suppl.,  108,  121  (1940). 
Gloster  and  Greaves.     Brit.  J.   Ophthal., 

41,  513  (1957). 
Grabensberger.     Z.  vergl.  Physiol.,  20,  1, 

338  (1934). 
Grison.    C.  R.  Acad.  Sci.  (Paris),  217,  621 

(1943). 
Gunn.    J.  exp.  Biol.,  17,  267  (1940). 
Guyselman.     Physiol.  Zool.,  30,  70  (1957). 
Hafez.    Experientia,  6,  423  (1951). 
Halberg.    J.  Lancet,  73,  20  (1953). 
Halberg,  Engel,  Treloar  and  Gully.    Arch. 

Neurol.  Psychiat..  69,  462  (1953). 
Halberg,  Levy  and  Visscher.     Fed.  Proc, 

12,  59  (1953). 
Halberg   and   Visscher.      Proc.  Soc.   exp. 

Biol.  Med.,  75,  846  (1950). 
A77ier.  J.  Physiol.,  171,  732  (1952). 
Halberg,  Visscher  and  Bittner.    A^yier.  J. 

Physiol.,  179,  229  (1954). 
Hammond.    Science,  117,  389  (1953). 
Harker.    J.  exp.  Biol.,  30,  525  (1953). 
Nature  (Lond.),   173,   689   (1954). 
Biol.  Rev..  33,  1  (1958). 
Hart.    J.  exp.  Biol.,  28,  1  (1951). 
Harvey.  J.   gen.  Physiol.,  7,  679  (1925). 

Bioluminescence,  N.Y.  (1952). 
Henkes.    J.  exp.  Biol.,  29,  178  (1952). 
Herter.     Z.  vergl.  Physiol.,  20,  511  (1934). 
Heymans  and  Moore.    J.  gen.  Physiol.,  6, 

273  (1924)  ;    7,  345  (1925). 
Hill  and  Parkes.     Proc  roy.  Soc.  B,  115, 

14  (1934). 
Hooker.    Amer.  J.  Anat.,  16,  237  (1914). 
Hoover  and  Hubbard.    Copeia,  206  (1937). 
Host.     The  Auk,  59,  388  (1942). 
Hume.    J.  din.  Invest.,  28,  790  (1949). 
Jenner.    ^«a<.  i?ec.,  Ill,  512  (1951). 
Jenner  and  Engels.     Anat.  Rec,  113,  548 

(1952). 
Johnson.    J.  MammoL,  7,  245  (1926). 
Johnson    and    Garm.      Anat.    Rec,    57, 

Suppl.,  28  (1933). 
Jones.      J.    exp.    Biol,    32,    492    (1955)  ; 

33,  271  (1956). 


24 


THE   EYE   IN   EVOLUTION 


Kalmus.    Z.  vergl.  Physiol.,  20,  405  (1934); 

25,  494,  798  (1938). 
Biol,  generalis,  11,  93  (1935). 
Nature  (Lond.),  173,  657  (1954). 
Keeble  and  Gamble.      Philos.  Trans.  B, 

196,  295  (1904). 
Kellicott.     Bull.  Torreij  Bot.  Club,  31,  529 

(1904). 
Kiesel.    S.  B.  Akad.  Wiss.  Wien,  103,  97 

(1894). 
Kirkpatrick  and  Leopold.     Science,  117, 

390  (1953). 
Kirschbaum  and  Ringoen.    Anat.  Rec,  64, 

453  (1936). 
Kleber.     Z.  vergl.  Physiol. ,  22,  221  (1935). 
Kleinholz.     Biol.  Bull.,  72,  24  (1937). 
Kleinholz    and    Welsh.      Nature     (Lend), 

140,  851  (1937). 
Kleitman.    Sleep  and  IFoAe/M/ness,  Chicago 

(1939). 
Physiol.  Rev.,  29,  1  (1949). 
Kleitman,  Titelbaum  and  Feiveson.  Amer. 

J.  Physiol.,  121,  495  (1938). 
Kleitman,  Titelbaum  and  Hoffman.  Amer. 

J.  Physiol.,  119,  48  (1937). 
Kobayashi  and  Okubo.    Science,  121,  338 

(1955). 
Kowalski.      Folia    biol.   (Warsaw),    3,   55 

(1955). 
Landau  and  Feldman.  Actaendocr.  (Kbh.), 

15,53(1954). 
van    Leijden.     Proc.   Sec.   Sci.    kon.    ned. 

Akad.     Wet.     (Amsterdam),    19,     38 

(1917). 
Lesher  and  Kendeigh.     Wilson  Bull.,  53, 

169  (1941). 
Lewis  and  Lobban.    J.  Physiol.,  133,  670 

(1956). 
Lewis,   Lobban  and   Shaw.     J.   Physiol., 

133,  659  (1956). 
Lutz.    Amer.  Mus.  Nov.,  550,  1  (1932). 
Lyman.     Bull.  Mus.  comp.  Zool.  Harvard, 

93,  391  (1943). 
Marcovitch.    Science,  58,  537  (1923). 
Marshall.    Nature  (Lond.),  129,  344  (1932). 
Philos.  Trans.  B,  226,  423  (1936). 
Proc.  roy.  Soc.  B,  122,  413  (1937). 
Marshall  and  Bowden.     J.  e.vp.  Biol.,  11, 

409  (1934)  ;    13,  383  (1936). 
Martin.    Oame  Breeder  and  Sportsman,  39, 

95  (1935). 
Maslenikow.     Vestn.  OJtal.,  21,  237  (1904). 
Matthews.    J.  exp.  Biol.,  30,  243  (1953)  ; 

32,  59  (1955). 
Mellanby.    J.  exp.  Biol.,  17,  278  (1940). 
Menke.     Pflugers  Arch.  ges.  Physiol.,  140, 

37  (1911). 
Menzel.      Z.    Altersforschung,   6,    26,    104 

(1952). 
Meyer.    Z.  Zellforsch.,  40,  228  (1954). 
Millott.    Biol.  Bull.,  99,  329  (1950). 
Mills.    J.  Phi/siol.,  113,  528  (1951). 
Mills  and  Stanbury.    J.  Physiol.,  117,  22 

(1952). 
Mills,   Thomas   and  Yates.     J.    Physiol., 

125,  466  (1954). 


Miyazaki.     Sci.  Rep.  Tohoku  Univ.,  Biol. 

Ser.,  9,  183,  427  (1934). 
Moore.    Amer.  J.  Physiol.,  76,  112  (1926). 
Pardi  and  Papi.     Naturwissenschaften,  39, 

262  (1952). 
Z.  vergl.  Physiol.,  35,  459  (1953). 
Park.    Ecology,  16,  152  (1935). 
Park  and  Keller.    Ecology,  13,  335  (1932). 
Pohl.    Naturforsch.,  3b,  367  (1948). 
Porter.    Amer.  J.  Physiol.,  172,  515  (1953). 
Radnot.    Orv.  Hetil.,  94,  262  (1953). 
Ophthalmologica,  127,  422  (1954). 
Acta  morphol.  hung.,  5,  369  (1955). 
Radnot  and  Orban.    Acta  med.  Budapest, 

8,  369  (1956). 
Raeder.     Klin.  Mhl.  Augenheilk.,  74,  424 

(1925). 
Rahn    and    Rosendale.      Proc.   Soc.    exp. 

Biol.  Med.,  48,  100  (1941). 
Ralph.     Physiol.  Zool.,  30,  41  (1957). 
Redfield.    J.  e.vp.  Zool.,  26,  275  (1918). 
Renbourn.    J.  Hyg.,  45,  455  (1947). 
Rifhter.     Comjj.   Psychol.   Monogr.,   1,    1 

(1922). 
Riley.     Proc.  Soc.  exp.  Biol.  Med.,  34,  331 

(1936). 
Anat.  Rec,  67,  327  (1937). 
Rowan.    Nature  (Lond.),  115,  494  (1925)  ; 

119,  351  (1927)  ;    122,  11  (1928). 
Proc.    Boston  Soc.   nat.   Hist.,   38,    147 

(1926)  ;    39,  151  (1929). 
Proc.  nat.  Acad.  Sci.  (Wash.),  16,  520 

(1930)  ;   18,  639  (1932). 
Kongressbericht  d.  W eltgefliigelkongresses, 

1,  vi,  142  (1936). 
Biol.  Rev.,  13,  374  (1938). 
Proc.  zool.  Soc.  Lond.,  108A,  51  (1938). 
von  Sallmann  and  Lowenstein.     Arner.  J. 

Ophthal.,  39  (2),  11  (1955). 
Schafer.    Nature  (Lond.),  77,  159  (1907). 
Schleip.    Zool.  Jb.,  Abt.  Zool.  Physiol.,  30, 

45  (1910). 
Shapiro  and  Shapiro.    J.  exp.  Biol.,  11,  73 

(1934). 
Smelser,  Walton  and  Whetham.     J .  exp. 

Biol.;  11,  352  (1934). 
Smith,   H.      Proc.  roy.  Soc.   B,   125,    250 

(1938). 
Smith,  R.  I.    Biol.  Bull.,  95,  169  (1948). 
Stein.     Z.  vergl.  Physiol.,  33,  387  (1951). 
von  Stein-Beling.      Z.  vergl.   Physiol.,   9, 

259  (1929). 
Biol.  Rev.,  10,  18  (1935). 
Steiniger.      Z.   Morph.    Oekol.    Tiere,   26, 

591  ;   28,  1  (1933). 
Stephens.     Physiol.  Zool,  30,  55  (1957). 
Thomson.      Proc.    roy.    Soc.   B,   142,    146 

(1954). 
Vaugien.     C.  R.  Acad.  Sci.   (Paris),  234, 

1489  (1952). 
Verlaine.     Bidl.  Ann.  Soc.  Ent.  Belg.,  69, 

115  (1929). 
Wahl.     Z.  vergl.  Physiol.,  18,  709  (1933). 
Webb.  Physiol.  Zool.,  23,  316  (1950). 
Wells.    Anat.  Rec,  60,  Suppl.,  53  (1934)  ; 

62,  409  (1935). 


LIGHT   AND   METABOLISM 


25 


Welsh.     Proc.  nat.  Acad.  Sci.  (Wash.),  16, 
386  (1930). 
Quart.  Rev.  Biol.,  13,  123  (1938). 
Biol.  Bull.,  77,  119  (1939). 
J.  e.rp.  ZooL,  86,  35  (1941). 
Welsh  and  Osborn.     J.  com}).  Neurol.,  66, 

349  (1937). 
Whitaker.     Proc.  Soc.  e.vp.  Biol.  Med.,  34, 
329  (1936). 


Wigglesworth.  Principles  of  Insect  Physio- 
logy, London,  5th  Ed.  (1953). 

Wilson,  Woodard  and  Abplanalp.  Biol. 
Bull.,  Ill,  415  (1956). 

Witschi.     Wilson  Bull.,  47,  177  (1935). 

Young.    J.  exp.  Biol.,  12,  254  (1935). 

Zoond  and  Eyre.  Philos.  Trans.  B,  223, 
27  (1934). 


26 


THE   EYE   IN   EVOLUTION 


Fig.  11.— Jacques  Loeb  (1859-1924). 

JACQUES  LOEB  was  assistant  in 
physiology  at  the  University  of 
Wiirzburg  where  he  was  much 
influenced  by  his  botanical  col- 
league, Sachs  ;  he  then  went  to 
Strasbourg,  and  thereafter,  going 
to  America,  became  professor  of 
physiology  at  the  Universities  of 
Chicago  and  California,  and 
finally  head  of  the  Division  of 
General  Physiology  at  the 
Rockefeller  Institute  for  Medical 
Research  in  New  York.  I  am 
indebted  to  that  institution  for 
his  photograph.  samuel  o. 
MAST,  Professor  of  Zoology  in 
Johns  Hopkins  University,  was 
one  of  the  band  of  men  who  have 
made  Baltimore  outstanding 
among  the  centres  of  learning  in 
the  world. 


It  is  good  to  have  Jaccjues 
Loeb  and  Samuel  Mast  on  the 
same  page — the  two  great  pro- 
tagonists of  the  mechanistic  and 
the  vital  interpretations  of  ani- 
mal behaviour,  both  of  whom 
propagated  their  views  with  un- 
usual vigour — the  first  an  intel- 
lectual descendant  of  Descartes, 
the  second  of  Leibnitz  and 
Goethe. 


Fig.  12.— Samuel  O.  Mast  (1871-1947). 


CHAPTER   III 
THE  EFFECT  OF  LIGHT  ON  MOVEMENT 

The  control  of  the  movements  of  living  organisms,  both  plants 
and  animals,  by  light  is  a  fundamental  function  of  great  phylogenetic 
age,  preceding  the  acquirement  of  vision  and,  indeed,  leading  directly 
to  its  development  ^  ;  it  will  be  remembered  that  the  association  of 
the  functions  of  equilibration  and  orientation  with  the  visual  system 
of  the  higher  animals  is  in  every  sense  basic.  This  primitive  control  of 
movement  by  light  is  undoubtedly  an  adaptive  process,  directing  the 
organism  to  regions  in  the  environment  which  are  favourable  to  it, 
and  has  originated  and  evolved  in  the  same  way  as  other  biologically 
useful  reactions. 

Historical  development 

It  was  originally  held  that  the  orientation  of  primitive  organisms 
in  space  depended  on  the  exercise  of  those  "vital  forces  "  the  presence 
of  which  were  considered  to  differentiate  living  creatures  from  the 
inanimate  world  ;  and  it  was  not  until  the  time  of  the  Cambridge 
clergyman-journalist,  John  Ray  (1693),  that  a  mechanistic  explanation 
was  offered  to  account  for  this  aspect  of  the  behaviour  of  plants.  This 
English  botanist  suggested  that  plants  placed  before  a  window  turned 
towards  the  light  because  the  side  towards  the  window  was  cooler  than 
that  towards  the  room  and  consequently  grew  more  slowly  so  that  the 
plant  became  bent  by  the  relatively  greater  growth  on  the  warmer  side. 
The  Huguenot  botanist,  August  de  Candolle  (1832),  on  the  other  hand, 
introduced  the  conception  that  light  rather  than  heat  was  the  respon- 
sible agent,  a  concept  elaborated  and  rationalized  by  Sachs  (1882), 
the  botanist  of  Wiirzburg  ;  he  maintained  that  orientation  was 
determined  by  the  directional  incidence  of  the  light  and  so  formulated 
the  interpretation  of  these  phenomena  generally  current  today. 

Meantime,  similar  reactions  in  the  animal  world  were  considered 
to  be  dominated  by  a  vital  force  usually  conceived  as  acting  automatic- 
ally and  thoughtlessly,  a  view  ej^itomized  by  the  great  French 
philosopher,  Rene  Descartes  (1650).  The  publication  of  Darwin's 
Origin  of  Sjiecies  in  1859,  however,  caused  a  revolution  in  biological 
thinking  so  that  contemporaneous  writers  spent  much  ingenuity  in 
interpreting  the  behaviour  of  the  lower  animals  in  an  anthropomorphic  ^ 
way,  attributing  their  reactions  to  primitive  psychic  activities  which 

»  p.  105. 

*  avOpwTTos,  man  ;   ^lop^-q,  form. 
27 


28  THE   EYE   IN   EVOLUTION 

were  held  to  be  pre-human  in  the  sense  that  they  were  the  evolutionary 
forerunners  of  the  mental  attributes  of  man.^  Emotions  were  thus 
attributed  to  the  lowest  animals  so  that  their  conduct  could  be  equated 
to  that  of  man  who  was  their  descendant.  The  rationalization  of 
zoology  thus  lagged  behind  that  of  botany,  the  progress  of  which  seems 
to  have  been  unnoticed  by  those  engaged  in  the  study  of  animal  life, 
possibly  because  the  temptation  to  endow  plants  with  anthropomorphic 
attributes  was  less  compelling. 

In  extenuation  of  the  general  acceptance  of  what  would  be  considered  a 
shallow  philosophy  today,  it  must  be  remembered  that  the  doctrine  of  "  animal 
spirits  "  was  of  extreme  antiquity  ^;  as  a  basis  of  his  philosophy  man  required 
the  concept  of  an  incorporeal  essence  to  give  meaning  even  to  corporeal  objects, 
a  need  still  felt  by  such  philosophers  as  Descartes  (1650-64)  and  such  scientists 
as  Willis  (1670)  and  Boerhaave  (1708)  ;  and  it  was  not  until  almost  the  middle 
of  the  19th  century  that  the  physical  discoveries  of  Galvani  (1791),  the  anatomist 
of  Bologna,  and  Volta  (1796-1800),  the  physicist  of  Pavia,  were  applied  to  the 
reactions  of  living  creatures  by  the  two  great  founders  of  modern  physiology, 
Johannes  Miiller  (1834)  and  du  Bois-Reymond  (1843-49),  who  laboriously  began 
to  build  ujD  a  physiological  doctrine  on  a  physical  basis.  Almost  half  a  century 
was  to  pass,  however,  before  these  new  concepts,  already  accepted  by  botanists 
and  for  long  part  of  physiological  teaching,  were  applied  to  the  problems  of  the 
orientation  of  animals  by  light  and  other  stimuli.  The  early  experimenters  in 
this  field  from  Paul  Bert  (1869)  to  Graber  (1883-84)  interpreted  these  reactions 
in  anthropomorphic  terms  :  animals  sought  or  avoided  light  because  it  was 
"  agreeable  "  or  "  disagreeable  "  ;  indeed,  the  experimental  studies  of  Engel- 
mann  (1879-82)  and  Verworn  (1889)  were  the  first  in  which  attempts  were 
made  to  place  a  physiological  interpretation  upon  these  responses,  attempts 
which  rapidly  fructified  so  that  the  doctrine  soon  became  generally  accepted  by 
zoologists  and  physiologists.^ 

At  the  beginning  of  this  period  of  activity  and  reorientation,  a 
prophet  arose  in  the  person  of  the  German  biologist,  jacques  loeb 
(1859-1924)  (Fig.  11).  Loeb's  life-work  was  a  study  of  the  differentia- 
tion between  the  animate  and  the  inanimate  and  his  thesis  the  identity 
of  the  two,  for  to  him  all  living  things  were  chemical  and  mechanical 

1  Darwin  (1872),  Lubbock  (1881-89)  in  England  ;  Paul  Bert  (1869),  Plateau  (1886), 
Binet  (1894)  in  France  ;  Graber  (1883-84)  in  Germany  ;  Romanes  (1883)  in  America  ; 
and  others. 

^  This  belief  permeated  the  whole  of  ancient  thought  and  mythology.  Even 
although  the  philosophy  of  the  Ionian  Greeks  became  more  impersonal  than  the  bronze- 
age  cosmologies,  Thales  of  Miletus,  c  625-545  B.C.,  the  first  of  the  .Greek  natural 
philosophers,  ascribed  a  soul  to  the  lodestone  because  it  could  move  a  piece  of  iron,  a 
view  generalized  by  Anaxagoras,  c  488-428  B.C.,  who  ascribed  all  motions  of  material 
or  living  things  to  the  operation  of  a  mind  or  a  soul.  Erasistratus  of  Chios, ^.  c  300-260 
B.C.,  believed  that  the  inspired  air  was  transferred  into  vital  spirit  in  the  heart,  to  be 
relayed  as  such  all  over  the  body  by  the  arteries  ;  the  small  amount  reaching  the  brain 
was  again  transformed  into  animal  spirit  {animus,  a  soul)  which  was  distributed  by 
the  nerves  ami  was  responsible  for  sensitivity  and  movement.  The  same  philosophy 
was  further  elaboiated  by  Galen,  a.d.  c  130-200,  and  for  centuries  was  an  accepted  doc- 
trine. 

3  Loeb    (^  1913),    Jennings    (1904^-6),   Mast    (1906-38),   Bohn    (1909),    Patten 

(1919),  and  oti 


LIGHT  AND  MOVEMENT  29 

machines  the  activities  of  which  were  expHcable  by  the  same  physical 
laws.i  As  a  young  colleague  of  the  botanist,  Sachs,  at  Wiirzburg,  he 
appreciated  the  immense  strides  his  friend  had  made  in  the  interpreta- 
tion of  the  responses  of  plants  and  unicellular  organisms  to  light,  and 
applied  the  same  techniques  to  the  animal  world.  All  voluntary  and 
instinctive  reactions  of  animals  he  considered  to  be  determined  by 
internal  and  external  forces,  the  majority  of  their  responses  thereto 
depending  upon  their  bilaterally  symmetrical  structure.  Thus,  in  the 
simple  reaction  of  an  animal  going  towards  or  away  from  a  light,  if  the 
velocity  of  the  chemical  reactions  in  one  eye  is  increased,  the  equality 
of  "  tonus  "  in  symmetrical  muscles  on  the  two  sides  of  the  body  is 
altered  so  that  the  animal  is  compelled  to  change  its  direction  of 
locomotion  ;  as  soon  as  the  plane  of  symmetry  becomes  directed 
through  the  source  of  light,  muscular  tone  becomes  equalized  and  the 
animal  progresses  straight  ahead  until  some  other  asymmetrical 
disturbance  changes  its  direction  of  motion.  Any  other  form  of 
energy,  he  claimed,  acted  in  the  same  way  as  light,  so  that  the  animal, 
which  may  appear  superficially  to  move  purposively  and  of  its  own 
will,  is  in  reality  forced  to  go  where  it  is  carried  by  its  legs  or  wings. 
Animal  conduct  was  thus  interpreted  as  consisting  of  forced  move- 
ments, a  conception  very  different  indeed  from  the  anthropomorphic 
and  teleological  views  prevailing  throughout  the  nineteenth  century. 

Loeb  pursued  his  theories  with  immense  activity  and  application, 
and  defended  them  with  unusual  vigour  and  stubbornness.  It  soon 
became  obvious,  however,  despite  his  warm  advocacy,  that  the 
intricacies  of  animal  behaviour  could  not  be  contained  within  a  theory 
so  simple.  Moreover,  its  all-embracing  character  and  its  rigidity 
readily  opened  it  to  attack  as  observations  on  the  complexity  of  the 
conduct  of  animals  multiplied.  Jennings  (1904-6)  first  showed  that 
the  reactions  even  of  Protozoa  could  not  be  explained  in  this  decep- 
tively simple  way,  and  the  automaticity  of  the  reactions  of  animals  was 
challenged  and  disproved  by  many  workers, ^  but  by  none  more 
conclusively  and  consistently  than  by  samuel  o.  mast  (1871-1947) 
who  proved  to  be  Loeb's  most  violent  and  successful  opponent  (Fig.  12). 
Undoubtedly  Loeb  had  swung  the  pendulum  too  far.  A  considerable 
reconciliation  between  the  two  opposing  views  was  put  forward  by 
Kiihn  (1919),  but  general  accord  has  by  no  means  yet  been  reached. 

It  is  probably  true  that  the  mechanical  evidences  of  organic 
activities  ultimately  conform  to  the  rules  of  chemistry  and  physics  ; 
but  these  rules  have  yet  to  be  formulated  ;  nor — most  fortunately — is  it 
necessary  to  await  a  complete  explanation  in  fundamental  terms  before 

1  See  especially  his  Mechanistic  Conception  of  Life  (1912). 

2  V.  Buddenbrock  (1915),  Bierens  de  Haan  (1921),  Alverdes  (1932),  Russell  (1938), 
and  others. 


30 


THE   EYE   IN  EVOLUTION 


we  attempt  to  analyse  the  behaviour  of  living  things.  Loeb's  great 
contribution  was  the  application  of  the  experimental  method  to  the 
reactions  of  animals,  thus  retrieving  their  interpretation  from  the 
vagueness  and  sterility  of  conjectural  anthropomorphism  and  subjecting 
them  to  objective  analysis.  It  must  be  admitted  at  once  that  any 
attempt  to  explain  animal  behaviour  in  terms  of  our  present  knowledge 
by  one  single  embracing  theory  is  premature  ;  and  while  more  can  be 
learned  by  studying  reactions  to  stimuli  and  classifying  the  responses 
of  animals  on  a  mechanistic  rather  than  on  a  teleological  basis/  and 
although  higher  functions  can  never  wisely  be  called  upon  to  explain 
an  action  if  lower  functions  can  provide  a  rational  and  consistent 
interpretation,  there  are  many  aspects  of  the  behaviour  of  animals 
wherein  a  mechanomorphic  scheme  based  solely  on  forced  and  stereo- 
typed responses  fails  to  meet  the  case  and  wherein  the  conceptions  of 
motivation,  incentive  and  learning  can  be  more  usefully  and  economic- 
ally invoked.  2 


Alverdes.     The  Psychology  of  Animals  in 

relation  to  Human  Psychology,  London 

(1932). 
Bert.     Arch.  Physiol,  norm,  path.,  Paris, 

2,  547  (1869). 
Bierens    de    Haan.      Biol.    Zbl.,    41,    395 

(1921). 
Binet.        The     Psychic     Life     of    Micro- 
organisms, Chicago  (1894). 
Boerhaave.     Institutiones  medicce  (1708). 
Bohn.     Rap.   VI  Cong,  internat.  Psychol., 

Geneva  (1909). 
du  Bois-Reymond.    An.  Phys.  Chem.,  134, 

1  (1843). 
Untersuch.   ii.   thierische   Elektricitdt,    1 

(1848)  ;   2  (1849). 
von    Buddenbrock.      Biol.    Zbl.,    35,    481 

(1915). 
de   Candolle.      Physiologic   vegetale,   Paris 

(1832). 
Darwin.     Expression   of  the   Emotions   in 

Man  and  Animals  (1872). 
Descartes.     Les  passions  de  I'dme  (1650). 

De  homine  (1664). 
Engelmann.     Pflilgers  Arch.  ges.  Physiol., 

19,  1  (1879)  ;    29,  387  (1882). 
Galvani.     De  viribus  electricitatis  in  motu 

musculari,  Acad.  Sci.  Inst.  Bologna,  7, 

363  (1791). 
Graber.    S.  B.  Akad.  Wiss.  Wien,  87,  201 

(1883). 
Grundlinien  z.  Erforschung  d.  Helligkcits 

und    Forbensinnes   d.    Tiere,    Leipzig 

(1884). 


Jennings.      Publ.   Carnegie   Inst.,   Wash., 
No.  16,  256  (1904). 
Behavior    of    Lower    Organisms,    N.Y. 
(1906). 
Kiihn.      Die    Orientierung    der    Tiere    im 

Raum,  Jena  (1919). 
Loeb.     Pfliigers  Arch.  ges.  Physiol.,  64,  81 
(1893)  ;     56.    247    (1894)  ;     115,    564 
(1906). 
The  Dynamics  of  Living  Matter,   N.Y. 

(1906). 
The    Mechanistic    Conception    of    Life, 

Chicago  (1912). 
Hb.  vergl.  Physiol.,  4,  451  (1913). 
Forced  Movements,  Tropisms  and  Animal 
Conduct,  Phila.  (1918). 
Lubbock.     J.  Liym.  Soc.  (Zool.),  16,   121 
(1881)  ;    17,  205  (1883). 
The  Senses,  Instinct  and  Intelligence  of 
Animals,  London  (1889). 
Mast.    J.  exp.  Zool.,  3,  359  (1906). 

Light  and  Behavior  of  Organisms,  N.Y. 

(1911). 
J.  anim.  Behav.,  2,  256  (1912). 
Biol.  Zbl.,  33,  581  (1913)  ;  34,  641  (1914). 
Arch.  EntwMech.  Org.,  41,  251  (1915). 
Motor    Responses   to    Light   in   the    In- 
vertebrate Animals,  N.Y.  (1936). 
Biol.  Rev.,  13,  186  (1938). 
Miiller,  J.     Hb.  d.  Physiol,  d.  Menschen, 

3,  Sect,  1  and  2  (1834). 
Patten.    J.  gen.  Physiol.,  1,  435  (1919). 
Plateau.    J.  Anat.  (Paris),  22,  431  (U 
Ray.    Historia  Plantarum,  2,  985  (1693). 


^  The  value  of  the  objective  approach  in  comparison  with  the  teleological  as  a 
stimulus  to  i^i-o^ress  is  seen  in  comparing  two  textbooks  published  about  the  same 
time — War:-  ,  "^onkins  and  Wtirner's  Introduction  to  Comparative  Psychology  (N.Y., 
1934)  and  t,.  uithropomorphic  The  Animal  Mind:  a  Textbook  of  Comparative 
Psychology  b;         >shburn  (N.Y.,  1936). 

*  See  fur         p.  107. 


LIGHT   AND   MOVEMENT  31 

Romanes.        Animal     Intelligence,      X.Y.       Verworn.     Psychophysiologische  Protisten- 
(1883).  studien,  Jena  (U 


Russell.     The  Behaviour  of  Animals,  2nd.  Volta.      Galvanismus    u.    Entdeckung    d. 

Ed.,  London  (1938).  Sdulenapparates  (1796-1800). 

Sachs.      Vorlesungen  iiber  Pflanzen physio-  Willis.       De     motu     animalium,     London 

Zo^/c,  Leipzig  (1882).  (1670). 

The  Types  of  Motorial  Responses 

The  behavioural  responses  of  organisms  to  hght  are  diverse  and  for 
three-quarters  of  a  century  workers  in  this  field  have  made  numerous 
attempts  to  rationalize  them  into  a  single  system  of  classification. 
While  terminology  itself  cannot  claim  to  be  an  end  of  science — and, 
indeed,  its  apparent  definiteness  is  often  misleading — the  labelling 
and  classification  of  phenomena  are  of  great  value  in  the  economy  and 
clarification  of  thinking.  Adequate  classification,  however,  entails 
fundamental  knowledge  and  it  is  not  surprising  in  a  subject  which  is 
still  highly  controversial  and  inadequately  understood  that  agreement 
has  not  yet  been  reached. 

In  this  connection  several  terms  have  been  introduced  into  the  literature. 
Strasburger  (1878)  in  his  revolutionary  work  on  botany,  wherein  he  made  a 
fundamental  study  of  the  movements  of  plants,  used  the  term  phototropism 
((f)U)s,  (fxjoTos,  hght  ;  TpoTirj,  a  turning)  to  describe  the  mov^ements  of  sedentary 
plants  in  contradistinction  to  phototaxis  (rants',  a  precise  arrangement)  to 
describe  the  locomotor  reactions  of  freely  moving  organisms  to  light.  Shortly 
thereafter,  Engelmann  (1883)  introduced  the  term  kinesis  (/ctvi^at?,  a  movement) 
to  indicate  reactions  wherein  the  \-elocity  of  movement  depended  on  the  strength 
of  the  stimulus.  The  next  contribution  to  terminology  was  due  to  Pfeffer 
(1904)  who  introduced  the  useful  differentiation  of  phobotaxis  (^o'jSo?.  fear)  to 
describe  random,  trial-and-error  avoiding  naovements,  and  topotaxis  (totto?,  a 
place)  to  indicate  directional  attraction  movements,  while  Kiihn  (1919-32) 
subdivided  the  latter  into  four  categories  of  increasing  complexity  in  responso, 
which  we  shall  adopt — tropotaxis,  telotaxis,  menotaxis,  and  mnemotaxis.^ 
To  these,  Gunn  and  his  colleagues  (1937)  added  the  term  kxinokinesis  and 
klinotaxis  {kX'lv oj,  bend)  to  express  changes  in  orientation  determined  by 
turning  movements.  The  term  scototaxis  {aKoro?,  dark)  suggested  by  Alverdes 
(1930)  and  Dietrich  (1931)  is  probably  unnecessary  since  those  movements 
which  may  be  interpreted  as  the  result  of  an  attraction  to  darkness  are  probably 
best  looked  upon  as  a  negative  phototaxis. 

It  is  true  that  against  this  urge  for  classification  some  have  rebelled  (Mast, 
1938),  but  although  the  dangers  of  a  system  of  classification  in  concealing 
ignorance  are  obvious,  its  advantages  are  so  considerable  that  as  a  tentative 
measure  we  will  base  oiu"  terminology  on  the  classical  scheme  of  Kiihn,  introduc- 
ing some  modifications  advanced  by  Fraenkel  and  Gvmn  (1940).  It  is  to  be 
remembered,  however,  that  the  tj^^es  of  response  are  by  no  means  mutually 
exclusive  and  that  in  their  activities  many  animals  show  a  combination  of 
reactions. 

A  somewhat  revolutionary  view  has  recently  been  advanced  by 
Viaud  (1948).  He  divided  the  reactions  of  animals  to  light  into  two 
types  : 

1  p.  43. 


32  THE   EYE   IN   EVOLUTION 

(a)  "  Dermatoptic  sensitivity'',  a  "primary"  reaction  of  proto- 
plasm to  light  evident  throughout  the  cell  in  Protozoa  and  particularly 
in  the  surface  layer  in  Metazoa  ;  and  (6)  "visual  sensitivity",  a 
characteristic  of  specific  photoreceptor  organs. 

The  first  tyjDe  of  reaction  is  concerned  with  simple  attraction 
towards  (or  repulsion  from)  light  ;  the  second  is  concerned  with  orienta- 
tion. The  first  has  two  distinct  and  reciprocal  phases  :  the  essential 
reaction  is  attraction  towards  the  light  (phototropism),  purposeful  in 
nature,  elicited  most  readily  by  short-waved  light,  the  response  varying 
as  the  logarithm  of  the  intensity  of  the  stimulus  (the  Weber-Fechner 
law).  Repulsion  from  light  (photoi^hobism),  on  the  other  hand,  is  a 
negative  reaction,  a  phase  of  adaptation  and  recuperation  in  which 
the  animal  flees  from  light  at  its  own  particular  speed.  Visual  sen- 
sitivity, on  the  other  hand,  is  confined  to  the  eyes  and,  concerning 
itself  solely  with  visual  orientation,  responds  most  readily  to  stimula- 
tion by  the  mid-region  of  the  spectrum.  The  first  type  of  reaction  is 
prepotent  in  lowly  forms  (such  as  Hydra)  but  becomes  masked  in 
higher  forms  by  the  second,  although  it  again  determines  the  animal's 
conduct  when  it  is  blinded  (Crustaceans  such  as  Dajylmia,  Rotifers 
such  as  Asplanchna)  ;  it  cannot  be  elicited  in  forms  higher  than 
Amphibians.  The  second  type  of  reaction  does  not  appear  in  the 
lowest  forms  and  in  the  higher  adds  visual  apperception  to  its  original 
function  of  spatial  orientation.  This  is  an  interesting  although  some- 
what speculative  philosophy,  and  although  all  the  complex  story  of 
orientation  to  light  cannot  be  fitted  into  it  as  it  stands,  it  may  perhaps 
contain  much  truth. 

In  the  scheme  to  be  adopted  here,  the  motorial  responses  of 
organisms  to  light  will  be  divided  into  two  main  classes  : 

(a)  PHOTOKINESES,  non-cUrectional  changes  in  random  movements. 
This  implies  merely  a  change  of  activity  depending  on  the  intensity  of 
the  stimulation,  not  on  its  direction  ;  for  its  initiation  a  mechanism 
is  required  sensitive  only  to  changes  in  intensity  ;  there  is  no  true 
orientation  and  the  direction  of  the  response  is  merely  a  matter  of 
weighted  chance. 

(6)  DIRECTIONAL  ORIENTATIONS  towards  (positive)  or  away  from 
{negative)  the  stimulating  light.  The  term  phototropism  will  be 
retained  to  indicate  the  directional  orientation  of  parts  of  sessile  plants 
and  animals  ;  while  the  translatory  movements  of  motile  organisms 
will  be  described  as  phototaxes.  It  is  obvious  that  these  directional 
responses  are  more  efficient  and  purposive  than  the  more  primitive 
changes  ir-,  --ndom  activity,  since  they  allow  the  organism  to  adapt 
itself  mo:  rapidly  to  the  most  favourable  location  in  its 
environmcii  . 


LIGHT   AND   MOVEMENT  33 

To  retain  a  sense  of  proportion  it  is  well  to  remember  that  forms  of  stimula- 
tion other  than  light  are  operative  on  living  organisms,  although  none  shows  the 
same  interest  and  complexities  in  the  responses  elicited.  The  scientific  conception 
of  GEOTROPISM  in  plants  to  describe  the  effects  of  gravitational  influences  was 
introduced  by  Knight  (1806)  at  a  very  early  date,  even  before  de  Candolle  (1832) 
formulated  his  theory  of  phototropism.  Towards  the  end  of  the  19th  century 
however,  the  study  of  the  responses  of  organisms  to  various  stimuli  rapidly 
widened.  In  ec^ually  fundamental  researches  on  the  action  of  chemicals  on  the 
sperm  of  ferns  and  mosses,  Pfeffer  (1883-88)  introduced  the  term  chemotaxis, 
Stahl  (1884)  described  hydrotropism  in  fungi,  Wortmann  (1883)  discovered 
THERMOTROPISM,  and  Verwom  (1889)  thigmotropism  (contact  stimulation  ; 
diyixoL,  touch)  and  galvanotropism.  These,  however,  are  not  our  present 
concern,  and  we  shall  proceed  to  exemplify  shortly  the  various  types  of  response 
to  light. 

It  is  also  to  be  remembered  that  these  various  responses  may  be  mutually 
additive  ;  thus  some  flat  worms  are  photo -negative  and  at  the  same  time  swim 
towards  a  cathode.  When  the  two  stimvili  are  presented  together  the  response 
depends  upon  the  direction  and  strength  of  each.  Thus  when  the  light  and  the 
cathode  are  at  right  angles  the  worm  will  swim  at  an  angle  bisecting  the  direction 
of  the  stimvili  when  the  density  of  the  current  is  proportional  to  the  logarithm 
of  the  intensity  of  the  illumination. 

Alverdes.     Z.  wiss.  Zoo/.,  137,  403  (1930).  Claus,   Grobben  and   Kiihn's   Lhb.   der 

Cailahian.    C.  R.  Acad.  ScL,  U.R.S.S.,  27,  Zoologie,  Berlin,  246  (1932). 

160,  253,  374  (1940).  Mast.     Biol.  Bev.,  13,  186  (1938). 

de   Candolle.      Phusioloqie   vegetale,   Paris  Pfeffer.      Ber.   dtsch.   botan.   Oes.,   1,    524 

(1832).  (1883). 

Dietrich.    Z.  mss.  ZooZ.,  138,  187  (1931).  Untersuch.  botan.  Inst.  Tubingen,  1,  362 

^""'iTZn^H^r''  ^"'-  '''■  '''"""''  P^a'''l^S^r776  (1904). 

tfU,  yo  U»m;.           ^,     ^   .     ,  ,.          ,  Sfahl.    Bo/««.  Z.,  42,  145,  160,  187  (1884). 

Fraenkel  and  Gunn.      TAe  Onentatwn  of  gtrasburger.     Jena.   Z.  Naturw.,  12,  551 

Animals,  Oxon.  (1940).  (1878) 

Gunn,     Kennedy     and     Pielou.       Nature  Verworn.    ' Psydiophysiologische  Protisten- 

(Lond.),  140,  1064  (1937).  studien,  Jena  (1889). 

Knight.    P/n7os.  Tra/is.  B,  96,  99  (1806).  Viaud,    Le    photoiropisme    animal,    Paris 

Kiihn.     Orientierung  der  Tiere  im  Raum,  (1948). 

Jena  (1919).  Went.      Rec.    Trav.   botan.   Neerl.,   25,    1 

Bethes  Hb.  norm.  path.  Physiol.,  12  (1),  (1928). 

17  (1929).  Wortmann.    Botan.  Z.,  41,  457  (1883). 

PHOTOKINESIS 

KINESES  [Kivrjois,  movement)  are  the  most  simple  responses  of 
motile  organisms  to  light — they  are  merely  the  alteration,  either  a 
quickening  or  a  slowmg,  of  normal  random  movements  witJiout  specific 
directional  orientation  ;  all  that  is  required  for  their  initiation  is  a 
mechanism  of  the  simplest  type  which  possesses  the  ability  to  react 
photochemically  to  variations  in  the  intensity  of  illumination  ;  specific 
photoreceptors  (eyes)  are  in  no  sense  necessary.  The  phenomenon  is 
essentially  the  same  in  character  as  the  alterations  in  metabolic  activity 
produced  by  light  which  we  have  lately  considered.  It  must  be 
remembered,  however,  that  a  motorial  response  of  this  type  but 
frequently  more  dramatic  in  nature  may  result  from  other  stimuli 
such  as  variations  in  temperature  or  moisture. 

1.0.— VOL.   /.  3 


34 


THE   EYE   IN   EVOLUTION 


King-crab 


Whip-tail  scorpion 


Lamprey 


Cockroach 


The  response  may  involve  a  change  of  velocity  (orthokestesis) 
{opdos,  straight)  or  a  change  in  direction  (kllnoklnesis)  {kXlvco,  turn). 

ORTHOKESTESIS,  wherein  random  movements  are  accelerated  or 
decelerated  according  to  changes  in  the  intensity  of  the  illumination,  is 
seldom  the  sole  mode  of  response  of  any  organism  to  light  but  usually 
reinforces  reactions  of  another  type.  In  its  most  dramatic  form  the 
organisms  move  while  the  stimulus  acts,  that  is,  so  long  as  an  intensity 
gradient  exists  ;  when  the  intensity  becomes  constant  they  come  to 
rest.  Viewed  superficially  this  elementary  response  gives  a  false 
impression  of  orientation.  Thus  if  the  locomotor  activity  of  an 
organism  is  increased  by  light  and  diminished  in  darkness,  it  aggregates 
preferentially  in  the  shadowed  region  even  if  its  movements  continue 
to  be  random,  just  as  the  density  of  vehicular  traffic  increases  as  it  is 
slowed  in  towns  and  decreases  when  speed  is  regained  on  the  trunk 
roads  ;  an  organism  with  this  reaction  of  a  high  kinesis  in  the  light 
thus  appears  to  show  a  negative  phototaxis  but  can  be  said  to  be 
negatively  phototactic  with  as  much  logic  as  the  average  motorist  may 
be  assumed  to  delight  in  traffic-jams. 

This  response  of  activity  in  a  light -gradient  and  rest  in  the  shade 
giving  rise  to  an  apparently  photophobic  tendency  to  aggregation  in 
the  dark  is  relatively  common  ;  it  is  seen  typically  in  the  Bacterium 
photometricum  which,  as  its  name  implies,  becomes  active  only  under 
the  influence  of  light,  in  many  flat-worms,^  in  the  maggot  larvae  of 
various  flies, ^  in  certain  Arthropods  such  as  the  king-crab  ^  or  the 
whip-tail  scorpion,*  in  primitive  Vertebrates  such  as  the  lamprey  ^ 
and  in  the  larvae  of  certain  fish  such  as  the  herring,  Clupea,  and  plank- 
tonic  animals  as  a  means  of  depth-control.^  The  converse  reaction  is 
less  common  but  is  well  exemplified  by  the  inactivity  of  the  cockroach 
in  daylight  and  its  activity  in  darkness.'^ 

In  higher  forms  these  simple  kinetic  responses  are  less  evident  but  stimula- 
tion of  the  eyes  by  light  frequently  has  a  dramatic  effect  on  general  activity. 
This  is  especially  seen  in  Insects  :  thus  in  the  cockroach,  Periplaneta,  exposure 
to  light  considerably  reduces  the  threshold  of  response  to  other  stimuli  (Brecher, 
1929),  and  as  the  intensity  of  light  is  increased  the  beetle,  Popillia,  walks  more 
quickly  (Moore  and  Cole,  1921). 

KLiNOKESTESis  is  of  much  wider  application  and  interest  ;  in  it  a 
change  of  direction  is  involved,  so  that  turning  tnovements,  normally 

^  Planaria—Pe&T]  (1903),  Walter  (1907)  ;  Leptoplana—Kovey  (1929)  ;  Plagio- 
s/omwm— Welsh  (1933). 

«  Mast  (1911),  Herms  (1911). 
=  Limulus— Cole  (1923). 

*  Mastigoproctus  giganteus — Patten  (1917). 
'      :i!,^petra — Young  (1935). 

*  Vvoodhead  and  Woodhead  (1955). 

'  ^iuma  orientalis — Szymanski  (1914),  Wills  (1920). 


LIGHT   AND  MOVEMENT 

haphazard,  are  influenced  by  the  intensity  of  light  so  that  avoiding 
reactions  occur  by  trial -and -error  with  the  result  that  a  devious  path 
is  taken  in  a  general  direction  away  from  the  light  ;  in  a  favourable 
environment  the  animal  pursues  a  straight  course,  but  entering  an 
unfavourable  environment  it  turns  away.  This  may  be  accomplished 
by  creeping  or  oscillatory  movements  as  in  Alg*  such  as  diatoms  and 
desmids  (Pfeffer,  1904),  by  amoeboid  movements  as  in  slime-fungi 
(Stahl,  1884)  or  the  amoiba  (Mast,  1911),  or  by  free-swimming  move- 
ments by  cilia  as  in  the  swarm  spores  of  Algse  and  some  Ciliates 
(Oltmanns,  1922).  In  some  Cihates,  for  example,  the  direction  of 
movement  in  a  uniform  environment  changes  periodically  for  no 
apparent  reason  so  that  the  animal  does  not  travel  long  in  a  straight 
line  ;    when  exposed  to  illumination  the  rate  of  change  of  direction  is 


35 


■cipf 


ca 


Fig.   13. — Negative  Ki.inokinesis  in  Am<kha. 

The  organism  is  moving  onto  an  illuminated  cover-glass  and  eventually 
its  movement  is  reversed  (after  Mast). 


Diatom 


Desmid 


increased  although  the  speed  remains  constant,  so  that  they  apjDcar  to 
avoid  the  light  and  tend  to  aggregate  in  shadow  (Ullyott,  1936).  In 
comparison  with  orthokinesis  whereby  aggregation  is  reached  entirely 
by  chance,  klinokinesis,  although  still  haphazard,  is  obviously  a  more 
effective  mechanism  of  orientation  to  attain  an  optimum  environment 
either  towards  or  away  from  the  area  of  the  highest  concentration  of 
the  stimulus. 

The  simplest  and  most  primitive  response  of  this  tj^e  is  seen  in 
the  photo-negative  kinesis  of  Amoeba  i^roteus,  the  reactions  of  which 
have  received  much  study. ^  The  reaction  is  extremely  elementary. 
In  a  uniform  environment  this  Rhizopod  periodically  throws  out 
pseudopodia  in  an  indiscriminate  way  and  thereby  effects  movement. 
If,  however,  it  is  placed  on  a  microscope  slide  with  an  illuminated 

1  Engelmann  (1879).  Davenport  (1897),  Mast  (1910-32),  Mast  and  Pusch  (1924), 
Folger  (1925-27),  Luce  (1926),  Bovie  (1926),  Mast  and  Hulpieu  (1930),  and  others. 


36 


THE   EYE   IN   EVOLUTION 


Amoeba 


Paramcecium 


Dendroccelum 

(ciliated  on 

ventral  surface) 


square,  a  pseudopod  on  entering  the  square  will  stop  for  a  moment, 
then  protoplasmic  flow  will  commence  in  the  reverse  direction,  the 
pseudopod  being  finally  withdrawn  from  the  area.  After  repeated 
experiences  of  trial-and -error,  pseudopodia  appear  on  the  opposite  side 
of  the  animal  and  its  whole  movement  is  reversed  (Fig.  13). 

Before  the  response  occurs  there  is  a  latent  period  which  varies 
with  the  intensity  of  the  light  ^  ;  and  if  the  stimulus  be  intensified  by 
the  use  of  ultra-violet  light,  a  single  stimulus  may  be  sufficient  to 
reverse  the  direction  of  locomotion  at  once.  It  is  also  interesting  that 
modifications  in  behaviour  due  to  experience  occur  even  in  organisms 
so  lowly  as  the  amoeba,  for  the  time-reactions  of  the  response  are 
accelerated  as  the  number  of  consecutive  tests  is  increased,  so  that  the 
animal  becomes  habituated  to  the  stimulus  (Mast  and  Pusch,  1924  ; 
Grindley,  1937). 

As  would  be  expected  in  this  lowly  organism,  the  receptor  mechanism  is 
undifferentiated  and  the  response  is  primitive  ;  measurements  of  the  elasticity 
of  the  plasmagel  indicate  that  the  change  of  movement  is  due  to  the  gelating 
effect  of  radiation  on  the  relatively  flviid  protoplasm  ^  so  that  flow  and  the 
formation  of  pseudopodia  are  inhibited  on  the  more  highly  illuminated  parts  but 
can  occur  readily  in  those  parts  of  the  organism  on  which  the  illumination  is 
dim  (Mast,  1932).  The  intimate  natvire  of  the  mechanism  whereby  these  changes 
are  brought  about  is  not  known.  It  is  noteworthy,  however,  that  similar  changes 
follow  mechanical  stimulation,  and  Folger  (1926-27)  concluded  that  since  light 
and  mechanical  agitation  produce  the  same  changes  and  since  the  two  are 
additive  in  the  sense  that  the  one  stimulus  can  reinforce  the  other  when  both 
are  subliminal,  the  response  to  the  former  is  perhaps  not  specifically  photo- 
chemical but  of  an  even  more  primitive  nature.  It  is  also  to  be  remembered 
that  in  some  cases  minute  thermal  increments  are  more  effective  than  illumination, 
so  that  resjjonses  superficially  accepted  as  photokinetic  may  in  fact  result  from 
differential  heating  (differences  as  small  as  0-0005°  C  are  effective  in  the  slime- 
mould,  Dictyosteliurn  discoideum,  Bonner  et  al.,  1950). 

More  mobile  Protozoa  appear  to  react  with  greater  effect.  Thus 
ciliated  species  such  as  Paramoecium  swim  about  haphazardly  but  if 
they  approach  a  noxious  stimulus  (light,  heat,  acids,  etc.)  they  back 
and  turn  and  start  off  in  a  different  direction,  a  process  which  is  repeated 
until,  leaving  the  stimulus  behind,  they  can  swim  freely  forward.^  A 
reaction  which  appears  more  complex  is  exemplified  by  the  turbellarian 
flat-worm,  Dendrocoelujn  (Ullyott,  1936)  (Fig.  14).  This  ciliated 
flat -worm  never  travels  far  in  a  straight  line  even  if  its  environment  is 
uniform,  but  if  the  intensity  of  light  is  increased,  although  its  velocity 
remains  unaltered,  the  changes  in  direction  occur  more  frequently,  a 

'  Pelomyxa — Wilber  and  Franklin  (1947). 

^  That  the  amoeboid  movements  of  pseudopodia  were  due  essentially  to  a  gel-sol 
transformation  in  which  the  propulsive  force  is  derived  from  the  contractility  of  the 
elastic  plasmagel  was  suggested  by  Wallich  in  1863  and  the  theory  was  confirmed  by 
Hymaii  (1917),  Pantin  (1924-26)  and  Mast  (1926-31). 

3  Ehrenberg  (1838),  Jennings  (1906),  Mast  (1911),  Rose  (1929),  and  others. 


LIGHT   AND   MOVEMENT 

response  which  decays  with  time  as  the  organism  becomes  adapted.  It 
follows  that  if  travel  in  a  certain  direction  exposes  it  to  an  increase  in 
the  intensity  of  light,  the  direction  is  changed  by  an  increase  in  the 
rate   of  automatic   turning   and   the   worm  eventually   arrives   in   a 


37 


Fig.   14. — Klinokinesis  in  a  Motilk  Organism. 

Track  of  Dendrocalum.  At  the  upper  part  of  the  figure  illumination  was 
turned  on  ;  turning  movements  are  rapid.  As  their  frequency  decreases  the 
path  of  the  organism  tends  to  straighten  out  so  that  it  moves  to  an  area  of 
shadow.  The  velocity  remains  constant  all  the  time  ;  the  cross-lines  mark  half- 
ininute  intervals  (after  Ullyott,  1936). 


haphazard  way  at  the  darker  end  of  a  gradient  where  a  crowd  tends  to 
aggregate  ;  moreover,  if  it  crosses  from  a  dark  region  into  an  area  of 
bright  illumination,  an  immediate  increase  in  the  rapidity  of  turning 
renders  it  very  probable  that  its  re-entry  into  the  dark  is  speedy.  It  is 
interesting  and  significant  that  the  reactions  of  this  organism  seem  to 
have  a  sensitivity  to  light  resembling  that  of  the  human  eye  (Pirenne 
and  Marriott,  1955). 


Bonner,  Clarke,  Neely  and  Slifkin.    J.  cell. 

comp.  Physiol.,  36,  149  (1950). 
Bovie.       Biol.     Aspects     of    Colloid     and 

Physiol.  Chem.,  London  (1926). 
Brecher.    Z.  vergl.  Physiol.,  10,  497  (1929). 
Cole.    J.  gen.  Physiol.,  5,  417  (1923). 


Davenport.       E.rperimental     Morphology, 

N.Y.,  1,  (1897). 
Ehrenberg.       Die    Infusionsthierchen    als 

volk.  Organismen,  Leipzig  (1838). 
Engelmann.     Pfliigers  Arch.  ges.  Physiol., 

19,  1  (1879). 
Folger.    J.  exp.  Zool.,  41,  261  (1925). 


38 


THE   EYE   IN   EVOLUTION 


Folger.     J.  Morph.,  42,  359  (1926). 

Biol.  Bull.,  53,  405  (1927). 
Grindley.      The   Intelligence   of  Animals, 

London  (1937). 
Herms.    J.  e.Tp.  Zool.,  10,  167  (1911). 
Hovey.     Physiol.  Zool.,  2,  322  (1929). 
Hyman.    J.  exp.  Zool.,  24,  55  (1917). 
Jennings.     Behavior  of  Loiver  Organisms, 

N.Y.  (1906). 
Luce.    Anat.  Bee,  32,  Suppl.,  55  (1926). 
Mast.    J.  exp.  Zool.,  9,  265  (1910)  ;   51,  97 
(1928). 
Light  and  the  Behavior  of  Animals,  N.Y. 

(1911). 
J.  Morph.,  41,  347  (1926). 
Protoplasma,   8,    344    (1929)  ;     14,    321 

(1931). 
Physiol.  Zool.,  5,  1  (1932). 
Mast  and  Hulpieu.     Protoplasma,  11,  412 

(1930). 
Mast  and  Pusch.    Biol.  Bull.  46,  55  (1924). 
Moore  and  Cole.    J.  gen.  Physiol.,  3,  331 

(1921). 
Oltmanns.      Morph.    u.    Biol.    d.    Algen, 
Jena  (1922). 


Pantin.     J.  marine  Biol.  Ass.,  U.K.,  13, 
24  (1924). 
Brit.  J.  exp.  Biol.,  1,  519  (1924)  ;  3,  275, 
297  (1926). 
Patten.    J.  exp.  Zool.,  23,  251  (1917). 
Pearl.    Quart.  J.  micr.  Sci.,  46,  509  (1903). 
Pfeffer.    Pflanzenphysiologie,  2,  776  (1904). 
Pirenne   and   Marriott.      Nature   (Lond.), 

175,  642  (1955). 

Rose.      La   question   des   tropismes,   Paris 

(1929). 
Stahl.    Botan.  Z.,  42,  146,  162,  187  (1884). 
Szymanski.     Pfliigers  Arch.  ges.  Physiol., 

158,  343  (1914). 
Ullyott.    J.  exp.  Biol.,  13,  253  (1936). 
Walter.    J.  e.rjo.  Zoo?.,  5,  35  (1907). 
Welsh.     Biol.  Bull.,  65,  168  (1933). 
Wilber  and  Franklin.    Atiat.  Rec,  99,  680 

(1947). 
Wille.       Biologie    und    Bekdmpfung    der 

deutschen  Schabe,  Berlin  (1920). 
Woodheadand  Woodhead.  Nature  (Lond.), 

176,  349  (1955). 

Young.    J.  exp.  Biol.,  12,  229  (1935). 


PHOTOTROPISM 

Used  in  Strasbiirger's  (1878)  original  sense,  the  term  photo- 
TROPISM  connotes  the  orientation  of  sessile  organisrns  towards  or  away 
from  light.  The  phenomenon  is  a  widespread  and  well-known  charac- 
teristic of  plant  life  and  as  a  rule  the  stimulus  is  the  sun  (heliotropism  ; 

TJXios,  the  sun).  Among  the  higher  plants 
which  are  fixed  in  their  habitat,  heliotropic 
movements  are  limited  to  the  component 
parts  ;  the  aerial  vegetative  axes  usually 
turn  towards  the  light,  thus  exhibiting  a 
POSITIVE  HELIOTROPISM,  the  Icaf-bladcs 
take  up  a  position  at  right -angles  to  the 
rays  of  light  in  order  to  receive  as  much 
illumination  as  possible  (transverse  or 
DiA -heliotropism),  while  tendrils  and  roots 
grow  from  the  light  (negative  helio- 
tropism) (Fig.  15).  Occasionally  these 
movements  are  remarkably  delicate  and 
rapid  ;  thus  the  Bengal  plant,  Hedysarum 
girans,  nods  to  a  passing  cloud.  Some- 
times, however,  the  axes  of  the  plant  are 
photo -negative  ;  thus  several  grasses,  corn 
and  rice  grow  erect  in  darkness  and  tend  to 
lie  prostrate  in  bright  iUumination,  becom- 
ing positively  phototropic  when  shaded 
(Langham,  1941). 


Fig.   15. — Heliotropism. 


Seedling  of  Sinapsis  alba  in 
water  supported  on  a  cork 
plate.  It  has  been  illuminated 
initially  from  all  sides  and 
then  from  one  side  only:  the 
stem  turns  towards  the  light, 
the  root  away  from  it,  and  the 
leaf-blades  at  right  angles  to  it 
(after  Strasbvirgt-r). 


LIGHT   AND  MOVEMENT 


39 


It  is  interesting  that  comparable  non-translatory  movements  of  the  organs 
of  animals  may  occur  ;  thus  the  hydroid,  Eudendrium,  and  the  marine  polychsete 
worm,  Spirographis  spallanzani,  show  heliotropic  bending  movements  (Loeb, 
1890),  some  shell-fish  open  and  others  close  their  valves,  clams  retract  their 
siphons  (Hecht,  1919-20  ;  Light,  1930),  snails  their  tentacles  (Grindley,  1937  ; 
and  others)  and  sea-urchins,  such  as  Diadema  antillarum,  move  their  spines  if  a 
light  is  flashed  on  them  (P.  and  F.  Sarasin,  1887  ;  v.  Uexkiill,  1897  ;  Millott, 
1950),  while  many  sedentary  tubicolous  polychsete  worms,  such  as  Branchiomma, 
withdraw  into  their  tubes  on  a  decrease  in  light  intensity  (Nicol,  1950). 

An  interesting  variant  of  this  reaction  is  seen  in  certain  sea-urchins  such  as 
the  European  Strongijlocentrotus  (Dubois,  1913)  and  the  Caribbean  Lytechinus 
(Millott,  1957),  which  normally  withdraw  their  podia  when  illuminated.  When 
lying  in  sunlit  waters  these  echinoids  gather  small  stones,  the  shells  of  bivalve 
molluscs,  pieces  of  seaweed  or  whatever  debris  may  be  within  reach  of  their 
tube-feet,  and  heap  them  upon  themselves,  using  them  as  a  parasol  to  protect 
themselves  from  light. 

The  mechanism  of  the  phototropic  responses  of  plants  is  now 
relatively  clear.  They  are  due  to  the  production  of  growth-regulating 
phytohormones  ^  called  auxins,  a  generic  term  applied  to  a  number 
of  related  chemical  substances  of  wide  distribution  formed  by  specialized 
parts  of  the  plant — the  tip  of  the  coleoptile  in  seedlings  and  the  leaves, 
particularly  the  young  leaves,  of  mature  plants.  There  these  hormones 
are  formed  from  precursors  on  stimulation  by  light  and  thence  they  are 
transported  throughout  the  tissues  of  the  plant  at  a  rate  more  rapid 
than  can  be  accounted  for  by  simple  diffusion  (about  10  mm.  per  hour)  ; 
as  it  travels  through  the  tissues  the  freely-moving  auxin  regulates  the 
varying  rates  of  growth  that  account  for  such  phenomena  as  photo- 
and  geotropism,  while  some  of  it  becomes  bound  in  the  tissues,  there 
to  regulate  normal  growth.  In  phototropic  curvature  the  freely  avail- 
able hormone  becomes  unequally  distributed  in  its  passage  along  the 
two  sides  of  a  laterally  illuminated  plant,  an  increase  of  concentration 
on  the  shaded  side  of  the  stem  leading  to  a  bending  of  the  organ.  Its 
precise  mode  of  action  is  unknown,  but  it  would  seem  probable  that, 
in  addition  to  other  activities  such  as  the  regulation  of  osmosis,  it 
acts  essentially  as  a  co-enzyme  in  the  respiratory  activity  of  the  cells, 
causing  them  to  elongate  and  sometimes  stimulating  them  to  divide. 

In  these  processes  determining  the  phototropic  movements  of 
plants — and  also  of  animals — carotenoid  pigments  act  as  sensitizers. 
These  pigments  are  quite  different  in  chemical  structure  and  absorjDtive 
properties  from  the  chlorophyll  group  of  pigments  which  are  primarily 
responsible  for  the  photosynthesis  concerned  with  metabolism  in  the 
vegetable  kingdom  ^  ;  they  will  be  more  fully  described  at  a  later 
stage  ^. 

We  have  already  seen  that  de  Candolle  (1832)  first,  and  Sachs  (1882-87)  at 
a  later  date  showed  that  light  was  responsible  for  the  directional  growth  of 

1  p.  547.  2  p.  5.  3  p.  118. 


Branchiomma 


40 


THE   EYE   IN   EVOLUTION 


plants,  and  since  most  plants  bend  towards  the  light,  it  was  generally  assumed 
that  it  had  a  retarding  influence  upon  growth,  a  view  elaborated  in  great  detail 
by  Blaauw  (1909-18).  That  an  explanation  so  simple  could  not  account  for  the 
facts,  however,  had  already  been  shown  in  the  classical  researches  of  Darwin 
(1880)  on  the  behaviour  of  seedlings  of  grass  {Phalaris  canariensis)  and  the  oat 
{Avena  sativa) — observations  from  which  all  modern  views  on  the  mechanism 
of  phototropism  have  directly  descended.  Darwin  showed  that  the  seedlings 
only  curved  towards  the  light  when  the  tijD  of  the  coleoptile  was  unilaterally 


Figs.   16-20. — Phototropism  in  Seedlings. 


(a)  (A)  (c) 

Fig.   16. 


(a)  (b)  (c) 

Fig.   17. 


[~3 


^  n 


(a)      (b)      (c) 

Fig.   18. 


Fig.  20. 


Fig.  16. — Darwin,  1880.  The  grass  coleoptile  exposed  to  lateral  illumina- 
tion (a)  bends  towards  the  light  (6).  When  the  tip  is  removed  (c)  the 
phototropic  response  does  not  occur. 

Fig.  17. — Boysen-Jensen,  1910-11.  When  a  coleoptile  tip  is  excised  and 
replaced  with  gelatin  inserted  between  it  and  the  stump  (a),  phototropic 
curvature  results  normally  ;  a  diffusible  substance  therefore  jjasses  across 
the  plate  of  gelatin.  If,  however,  a  plate  of  mica  is  inserted  on  the  shaded 
side  (6),  no  response  occurs.  If  the  mica  is  inserted  on  the  illuminated 
side,  the  response  is  normal  (c).  It  follows  that  the  diffusible  substance 
passes  down  the  shaded  side. 

Figs.   18-20.     Went,  1928. 

Fig.  18.  When  the  tip  of  the  coleoptile  is  removed,  growth  in  length  ceases  (a). 
An  agar  block  placed  on  the  stump  has  no  effect  (6).  An  agar  block  con- 
taining juice  extracted  from  the  excised  tip  promotes  normal  growth  (c). 

Fig.  19.  The  coleoptile  tip  is  placed  upon  an  agar  block  (a),  and  a  piece  of  the 
block  transferred  unilaterally  to  a  decapitated  coleoptile  (6).  Unilateral 
growth  resembling  phototropic  curvature  results  due  to  the  diffusion  of  the 
hormone  from  the  agar  derived  from  the  tip. 

Fig.  20. — When  unilateral  light  falls  on  an  excised  tip  in  contact  with  two  agar 
blocks  separated  by  a  razor  blade,  the  greater  part  (65%)  of  the  growth- 
hormone  is  recovered  from  the  agar  on  the  shaded  side. 


illuminated  and  never  when  it  was  shaded  by  tinfoil  even  while  the  rest  of  the 
plant  was  exposed,  and  that  no  curvature  ever  occurred  in  the  stem  or  the  root 
if  the  growing  tip  were  removed  (Fig.  16).  This  localization  of  sensitivity  to 
the  growing  tip  of  the  seedling  was  confirmed  by  subsequent  workers.  Rothert 
(1892-96)  incised  the  vascular  bundles  in  various  places  and  proved  that  the 
phototropic  stimulus  travelled  from  the  sensitive  tip  throughout  the  plant  in 
the  parenchyma,  while  Fitting  (1905-7)  observed  that  the  curvature  was  caused 
by  a  difference  in  the  rate  of  growth  of  the  two  sides,  in  positive  phototropism 
the  darkened  side  growing  more  rapidly  than  the  illuminated  side.     The   next 


LIGHT   AND   MOVEMENT  41 

fundamental  step  was  due  to  Boysen-Jensen  (1910-13)  who  showed  that  the 
stimulus  could  trav^erse  a  layer  of  gelatine  but  was  arrested  by  a  plate  of  mica,  thus 
demonstrating  that  the  curvature  was  due  to  the  diffusion  down  the  shaded 
side  of  the  plaiit  of  a  chemical  substance  stimulating  growth  (Fig.  17).  These 
observations  were  confirmed  by  Paal  (1914^18)  who  showed,  moreover,  that  if 
an  unstimulated  tip  were  excised  and  replaced  towards  one  side  of  the  stvunp, 
growth  was  accelerated  on  that  side,  thus  demonstrating  that  the  stimulatory 
substance  was  continuously  formed  in  the  sensitive  region.  The  final  proof 
was  effected  by  Stark  (1921),  Stark  and  Drechsel  (1922),  Cholodny  (1927-35) 
and  especially  by  the  Dutch  botanist,  Went  (1926-45),  who  trapped  the  diffusible 
growth-hormone  descending  from  the  coleoptile  tip  in  a  piece  of  gelatine  or 
agar  inserted  into  the  plant  and,  transferring  the  jelly  from  the  plant  and  placing 
it  on  the  cut  end  of  a  non-illuminated  plant  from  which  the  tip  had  been  removed, 
demonstrated  the  occurrence  of  a  typical  jahototropic  response  in  the  second 
even  although  light  had  been  entirely  excluded  (Figs.  18-20).  All  that  remained 
was  to  identify  the  chemical  nature  of  the  active  agent. 

A  growth-hormone  of  this  type  was  first  extracted  from  fungi  by  Nielsen 
(1930)  and  Boysen-Jensen  (1931),  and  shortly  thereafter  was  chemically 
identified  by  Kogl  (1932)  and  Kogl  and  Kostermans  (1934)  as  3,indole-acetic 
acid.  Subsequent  intensive  research,  particularly  by  Kogl  and  his  colleagues 
(1931-35)  in  Germany,  Zimmerman  and  Hitchcock  and  their  colleagues  (1935-48) 
in  the  Boyce  Thompson  Institute  for  Plant  Research  in  New  York,  has  shown 
that  there  are  many  such  physiologically  active  substances  {auxins)  of  wide 
distribution  ;  indeed,  over  50  compounds,  natural  and  synthetic,  having  this 
growth-producing  property  had  been  isolated  by  1935.  The  most  interesting 
historically  are  auxin  a  (a  monocyclic  trihj^droxy-carboxylic  acid,  Cj^8H3205), 
auxiyi  h  (a  monocyclic  hydroxy-keto-carboxylic  acid,  CjgHgoO),  and  heterauxin 
(3,indole-acetic  acid,  C^oHgOaN)  (Kogl,  1935).  Whether  the  first  two  or  other 
allied  substances  are  present  in  the  living  j^lant  •  is  not  clear  ;  but  the  most 
popular  hypothesis  at  present  is  that  heterauxin  is  present  in  the  tip  of  the  stem 
initially  as  a  precursor  ;  here  it  is  activated  into  freely  moving  auxin  by  enzymic 
action  ;  and  it  would  appear  that  its  activity  may  be  masked  or  reduced  by 
anti-auxins.  However  that  may  be,  it  is  clear  that  svich  substances  applied  to 
the  intact  plant  or  inserted  into  incisions  or  fed  to  the  plant  through  the  soil  not 
only  induce  tropic  curvatures  but  can  modify  the  plant  in  size,  shape,  pattern 
and  texture,  can  inhibit  the  formation  of  buds  and  perhaps  of  flowers, ^  and  in 
supra-physiological  concentrations  can  induce  tumour-like  growths. ^  It  is 
puzzling  why  the  same  substances  are  found  in  human  saliva  (Seubert,  1925) 
and  urine  (Kogl  and  Smit,  1931). 

It  is  interesting  that  an  artificial  end-organ  to  stimulate  phototropic 
activity  can  be  synthesized  (Brauner,  1952).  If  capillary  tubes  filled  with  photo- 
sensitized indolylacetic  acid  are  svibstituted  for  the  cotyledons  in  Helianthus 
seedlings,  illumination  of  one  produces  a  marked  curvature  of  the  other  hypocotyl. 

This  description  may  give  the  impression  of  over-simplification.  It  must 
not  be  thought  that  the  whole  story  of  the  growth  of  plants  is  explained  in 
terms  of  a  single  auxin.  Research  in  progress  as  this  book  is  being  written  is 
showing  that  the  regulation  of  growth  is  based  on  a  complex  system  of  several 
auxins,  kinetin-like  hormones  and  gibberellin-like  hormones,  and  possibly 
other  related  substances. 

1  p.  12. 

^  For  general  reviews,  see  Boysen-Jensen  (1936),^Went  (1939),  Zimmerman  (1948). 
van  Overbeek  n956),  Bentley  (1957). 


42 


THE   EYE   IN  EVOLUTION 


Bentley.      Ann.    Rev.    Plant    Physiol.,    8 

(1957). 
Blaauw.     Rec.  Trav.  botan.  Nierl.,  5,  209 
(1909). 
Z.  Botan.,  6,  641  (1914)  ;   7,  465  (1915). 
Meded.       Landbouivhoogeschool    Wagen- 
ingen,  15,  89  (1918). 
Boysen-Jensen.      Ber.   dtsch.   botan.   Ges., 
28,  118  (1910)  ;  31,  559  (1913). 
Biochem.  Z.,  236,  205  ;  239,  243  (1931). 
Growth  Hormones  in  Plants, 'HJ.Y.  (1936). 
Braxiner.    Experientia,  8,  102  (1952). 
de   Candolle.      Physiologie  vegetale,   Paris 

(1832). 
Cholodny.    Biol.  Zbl.,  47,  604  (1927). 
Planta  (Berl.),  6,   118  (1928)  ;    7,  461, 
702  (1929)  ;    13,  665  ;    14,  207  ;    15, 
414  (1931)  ;    17,  794  (1932)  ;    20,  594 
(1933)  ;   23,  289  (1935). 
Herbage  Rev.,  3,  210  (1935). 
Darwin.       The    Power    of    Movement    in 

Plants,  London  (1880). 
Dubois.        IX     Internal.     Congr.      Zool., 

Monaco,  1,  148  (1913). 
Fitting.     Ergeb.  Physiol.,  4,  684  ;    5,  155 
(1905). 
Jb.  wiss.  Botan.,  44,  177  (1907). 
Grindley.      The   Intelligence   of  Animals, 

London  (1937). 
Hecht.      J.    gen.    Physiol.,    1,    545,    657 

(1919)  ;    2,  337  (1920). 
Hitchcock.       Conirib.     Boyce     Thompson 

Inst.,  7,  87  (1935). 
Hitchcock     and     Zimmerman.       Contrib. 
Boyce  Thompson  Inst.,  7,  447  (1935)  ; 
8,  63  (1936)  ;    9,  463  (1938)  ;    10,  461 
(1939). 
Kogl.    Chem.  Weekbl.,  29,  317  (1932). 
Naturwissenschaften,  21,  17  (1933)  ;   23, 

839  (1935). 
Z.  angew.  Chem.,  46,  166,  469  (1933). 
Hoppe-Seyl.  Z.  physiol.  Chem.,  228,  90 
(1934). 
Kdgl    and    Erxleben.       Hoppe-Seyl.     Z. 

physiol.  Chetn.,  235,  181  (1935). 
Kogl  and  Kostermans.      Hoppe-Seyl.   Z. 

physiol.  Chem.,  228,  113  (1934). 
Kogl  and   Smit.      Proc.   Icon.   ned.   Akad. 

Wet.,Z\,  1411  (1931). 
Kogl,  Smit  and  Erxleben.    Hoppe-Seyl.  Z. 
physiol.  Chem..,  214,   241  ;    216,   31  ; 
220,  137  (1933) ;   225,  215  ;   227,  51  ; 
228,  90,  104  (1934). 


Kogl,  Smit  and  Tonnis.     Hoppe-Seyl.   Z. 

physiol.  Chem.,  220,  162  (1933). 
Langham.    Science,  93,  576  (1941). 
Light.    J.  Morph.  Physiol.,  49,  1  (1930). 
Loeb.      Der    Heliotropismus    der    Thiere, 

Wurzburg  (1890). 
Millott.    Biol.  Bull,  99,  329  (1950). 

Endeavour,  16,  19  (1957). 
Nicol.    J.  marine  Biol.  Ass.,  U.K.,  29,  303 

(1950). 
Nielsen.    Jb.  wiss  Botan.,  73,  125  (1930). 
van  Overbeek.    Ann.  Rev.  Plant  Physiol., 

7,  355  (1956). 
Paal.      Ber.    dtsch.    botan.    Ges.,    32,    499 
(1914). 
Jb.  wiss.  Botan.,  58,  406  (1918). 
Rothert.     Ber.  dtsch.  botan.  Ges.,  10,  374 
(1892). 
Beit.  Biol.  Pflanzen,  7,  1  (1896). 
Sachs.    Textbook  of  Botany,  Oxford  (1882). 
Vorlesungen    i'lber    Pflanzenphysiologie, 
Leipzig  (1887). 
Sarasin,  P.  and  F.    Ergebn.  Natur.  Forsch. 

Ceylon,  1,  1  (1887). 
Seubert.     Z.  Botan.,  17,  49  (1925). 
Stark.    Jb.  wiss.  Botan.,  60,  67  (1921). 
Stark  and  Drechsel.    Jb.  wiss.  Botan.,  61, 

339  (1922). 
Strasburger.     Jena.   Z.  Naturw.,  12,   551 

(1878). 
V.  Uexkiill.     Z.  Biol.,  34,  315  (1897). 
Went.     Proc.    kon.  ned.  Akad.   Wet.,  29, 
185  (1926) ;    30,    10  (1927) ;    32,   35 
(1929)  ;   37,  445,  547  (1934)  ;   38,  752 
(1935)  ;   42,  581,  731  (1939). 
Rec.   Trav.  botan.  Neerl.,  25,   1  ;    25A, 

483  (1928). 
Botan.    Rev.,    1,    162    (1935)  ;    11,    487 

(1945). 
Plant  Physiol,  13,  55  (1938)  ;    14,  365 

(1939)  ;   17,  236  (1942). 
Ann.  Rev.  Biochem.,  8,  521  (1939). 
Botan.  Gaz.,  103,  386  (1941). 
Amer.  Sci.,  SI,  189  (1943). 
Zimmerman.  Plant  Hormones,  in  Crocker's 
Growth  of  Plants,  N.Y.,  p.  204  (1948). 
Zimmerman     and     Hitchcock.       Contrib. 
Boyce  Thompson  Inst.,  8,  311  (1936)  ; 
12,  1,  491  (1941). 
Zimmerman     and     Wilcoxon.         Contrib. 
Boyce  Thompson  fnst.,  7,  209  (1935). 


PHOTOTAXIS 

A  DIRECTED  RESPONSE  TO  LIGHT  is  obviously  a  much  more  efficient 
orientating  mechanism  than  the  simple  change  in  activity  we  have 
already  discussed  as  photokinesis  wherein  a  difference  of  intensity 
serves  as  the  stimulus  and  aggregation  is  determined,  as  it  were,  merely 
by  accident.  The  phototactic  reaction  is  purposive  ;  for  example,  by 
suitable  manipulation  of  the  lighting  system  it  is  possible  to  make 


LIGHT   AND  MOVEMENT  43 

certain  photo -positive  animals  travel  towards  a  light  even  although 
this  movement  brings  them  into  a  region  of  lower  intensity  of  illumina- 
tion,^ or  certain  photo -negative  animals  to  seek  a  dark  shelter  even 
although  this  entails  moving  towards  a  light. ^  It  is  a  response, 
however,  which  requires  one  or  more  receptor  organs  specially  designed 
to  appreciate  the  direction  of  the  incident  light  rather  than  merely 
changes  in  its  intensity,  and  as  the  response  becomes  more  and  more 
efficient  and  therefore  more  and  more  complex,  the  receptor  organs 
become  progressively  specialized  until  they  eventually  achieve  the 
structural  differentiation  necessary  to  mediate  the  faculty  of  vision. 
The  directional  phototropic  movements  of  sessile  plants  are  slow  and 
leisurely,  essentially  kinetic  in  nature,  quantitative  in  type  and 
chemical  in  execution  ;  but  motile  organisms  require  a  more  efficient 
mechanism  capable  of  qualitative  responses — a  shock-reaction  eventu- 
ally mediated  by  nervous  activity.  The  difference  between  the  two 
types  of  response  is  well  exemplified  in  the  mutilation  experiments  of 
Viaud  and  Medioni  (1949)  on  the  flat -worm.  Planar  ia  luguhris,  an 
animal  in  which  both  reactions  are  present  ;  they  found  that  its 
positive  photokinesis  was  entirely  due  to  the  action  of  light  on  the  skin 
while  positional  orientation  by  phototaxis  depended  on  the  eyes. 

As  they  evolved,  these  phototactic  responses  increased  in  com- 
plexity and  efficiency  ;  the  various  stages  may  be  classified  as  follows 
(Kiihn,  1919-32  ;   Gunn  et  al,  1937). 

(i)  KLEsroTAXis  (kXlvo),  tum  ;  rafts-,  a  precise  arrangement), 
wherein  turning  movements,  normally  alternating  regularly,  are 
directed  towards  or  away  from  the  light.  One  receptor  organ  only  is 
necessary  which  responds  by  comparing  the  intensities  of  successive 
stimuli  as  the  organism  turns,  and  the  directional  path  is  consequently 
irregular  and  wavy. 

(ii)  TEOPOTAXis  (rpoTT-q,  a  tum),  wherein  orientation  is  effected 
by  the  sirrmlianeous  comparison  of  the  intensities  of  the  stimulation  of 
two  symmetrical  receptors  and  the  maintenance  of  a  bilateral  balance. 
The  path  is  thus  continuously  corrected  so  that  it  is  practically  straight 
towards  or  away  from  the  light,  and  it  is  obvious  that  greater  accuracy 
and  precision  are  obtained  by  a  simultaneous  comparison  than  by 
comparing  present  experiences  with  past. 

(iii)  TELOTAXis  (TeAo?,  a  goal),  a  direct  orientation  towards  or 
away  from  the  light  without  the  necessity  of  bilateral  balance.  A 
single  receptor  organ  which  can  fixate  the  source  of  light  is  sufficient 
for  its  initiation,  but  it  must  possess  a  number  of  elements  spatially 
distributed  so  that  the  stimulus  can  be  localized  on  the  sensory  surface 
and  the  head  and  body  can  be  orientated  directly  in  line  with  the  light. 

1  See  the  experiments  of  Richard  (1948)  on  termite  larvae  {Calotermes  flavicollis). 
*  See  Gousrard  (1948-50)  experimenting  on  the  cockroach,  Blatella  ;    Bolwig  (1954) 
experimenting  on  the  stomatopod,  Gonodactylus. 


44 


THE   EYE   IN  EVOLUTION 


Drosoph  ila 


(iv)  MENOTAXis  {fiiveiv,  to  remain).  Orientation  is  not  directly 
towards  or  away  from  the  light  but  at  an  angle  to  it  ;  the  animal 
appreciates  a  definite  distribution  of  the  stimulus  over  its  retina  where 
it  retains  the  impression,  and  having  evolved  beyond  the  ability  to 
travel  only  in  a  straight  line,  it  can  orientate  itself  and  accomplish 
separate  reactions  with  reference  to  different  parts  of  its  field  of  vision. 
This  activity  is  exemplified  in  the  light-compass  reactions  of  insects, 
or  the  dorsal  (or  ventral)  light  reaction  of  fishes. 

(v)  Kiihn's  final  category,  mnemotaxis  (/xvtj/mt^,  memory), 
wherein  immediate  orientation  is  aided  by  memory-images  of  past 
experience,  is  associated  with  other  methods  as  an  adjuvant  mechanism 
of  a  higher  type. 

In  these  responses  to  light  three  stages  emerge  in  the  evolutionary 
process.  In  the  simplest  and  most  primitive  response,  the  stimulus  is 
appreciated  in  an  indeterminate  manner  and  orientating  movements 
are  corrective.  In  the  next  stage  a  more  complicated  but  obviously 
more  efficient  reflex  mechanism  ensures  a  directed  and  purposeful 
orientation.  The  third  and  highest  development  involves  the  ability 
to  retain  the  impression  made  upon  the  receptor  organ,  to  adjust  the 
response  and  utilize  various  means  to  gain  the  desired  end  should  the 
most  obvious  fail  ;  it  is  a  purposive  rather  than  a  reflex  response.  This 
more  advanced  development  is  exemplified  in  its  simplest  terms  in  the 
continued  ability  of  some  worms  to  orientate  themselves  to  light  when 
one  eye  has  been  removed,  or  in  the  compensatory  modifications  in  the 
responses  of  certain  insects  when  some  of  the  legs  on  one  side  have  been 
removed  ;  the  same  adaptability  is  seen  in  the  complicated  manoeuvres 
of  ants,  backwards,  sideways  or  forwards,  to  reach  the  desired  goal, 
and  reaches  its  highest  forms  in  the  reactions  of  Vertebrates  among 
which  its  culmination  is  seen  in  the  navigational  ability  of  birds. 

All  these  reactions,  however,  whether  simple  or  complex,  have 
certain  features  in  common.  In  the  first  place,  they  are  all  innate  and 
show  no  evidence  of  being  acquired  ;  thus  Payne  (1910-11)  bred  the 
fruit -fly,  Drosojjhila,  in  the  dark  and  found  that  individuals  of  the 
69th  generation  were  normally  photo -positive  at  the  first  trial  ;  while 
the  young  bird  may  set  out  on  its  first  migration  to  a  new  land  2,000 
miles  away  and  follow  by  a  light-compass  reaction  approximately  the 
same  route  as  its  parents.  It  is  true  that  the  standard  responses  may 
become  altered  by  use,  being  either  accentuated  by  habituation  (as  we 
have  seen  even  in  Amoeba,  Mast  and  Pusch,  1924),^  or  diminished  by 
adaptation  (as  we  shall  see  in  some  insects,  Clark,  1928-33)  ;  but  these 
are  physical  processes.  It  is  also  true  that  their  efficiency  may  be 
increased  with  training,  as  is  seen  in  the  migration  or  homing  of  birds 
(Rupp(  ''  and  Schein,  1941  ;  Matthews,  1953),  or  can  be  altered  and  even 

1  p.  36. 


LIGHT   AND   MOVEMENT 


45 


inhibited  by  associations  established  by  conditioned  reflexes  ;  thus  the 
photo -negativity  of  the  cockroach,  BlateUa,  can  be  inhibited  by  training 
if  a  hght  is  placed  over  its  dark  shelter  (Goustard,  1948-50).  It  is  also 
to  be  remembered  that  the  removal  of  necessary  effector  organs  may 
inhibit  or  invert  a  normal  phototactic  response  even  although  these 
have  no  apparent  connection  with  photoreceptors  (the  antennae  of  the 
cockroach  or  the  wings  of  the  fruit -fly,  Drosoj^hila ,  Goustard,  1949). 

In  the  second  place,  these  resjjonses  are  all  of  biological  value  and 
to  attain  this  end  they  may  vary  with  the  strength  of  the  stimulus  or 
change  their  character  if  associated  with  a  second  stimulus  of  another 
nature  ;  moreover,  they  may  alter  in  type  and  even  reverse  their 
nature  during  the  life  of  the  animal  to  meet  the  needs  of  a  change  in 
environment. 

Thus  the  usual  photo-negative  response  (the  shadow-reflex)  seen 
in  so  many  worms  and  molluscs  is  essentially  an  escape  movement 
from  the  presence  of  predators,  while  the  opposite  response  of  the 
tentacle  of  the  snail  is  the  expression  of  the  fact  that  a  shadow  usually 
signifies  food.  Some  of  these  responses  are  very  sensitive  :  thus  the 
acorn-shell,  Balanus,  responds  to  a  darkening  of  5%  (v.  Buddenbrock, 
1930).  The  simplest  example  of  a  variation  in  the  response  with  the 
strength  of  stimulus  is  seen  in  the  protozoon,  Euglena,  which  is  photo- 
positive  in  weak  and  negative  in  strong  light  so  that  it  orientates  itself 
to  favourable  mid-intensities  (Mast,  1938),  or  in  the  fruit-fly,  Droso- 
-phila,  which  is  positively  phototactic  in  illuminations  below  9  lux 
and  negatively  over  79  lux  (Medioni,  1954).  A  similar  variation  may 
occur  with  the  nature  of  the  light  ;  thus  the  flat -worm,  Planaria 
lugubris,  is  said  to  be  positively  phototactic  to  red  and  negatively  to 
blue  light  (Viaud,  1949).  Again,  other  environmental  circumstances 
may  alter  the  response.  Paramcecium  is  geo-positive  in  the  light  and 
negative  in  the  dark  (Fox,  1925)  ;  the  normal  negative  phototaxis  of 
the  goldfish,  Carassius  auratus,  disappears  if  the  temperature  is  in- 
creased by  10°  C  (Andrews,  1952)  ;  the  normal  positive  phototaxis  of 
the  tsetse-fly,  Glossina,  becomes  negative  if  the  temperature  is  raised 
above  40°  C  even  if  the  temperature  in  the  dark  is  so  high  that  it  drops 
down  dead  (Jack  and  Wilhams,  1937)  ;  exposure  to  dry  air  alters  the 
phototactic  reaction  of  the  woodlouse,  Armadillidium,  from  negative 
to  positive  (Henke,  1930)  ;  while  the  negative  response  of  the  ohgo- 
chsete,  Perichmta,  when  it  is  extended  can  be  changed  to  a  positive 
response  when  the  worm  is  contracted  (Harper,  1905). 

An  excellent  example  of  a  change  in  response  with  different  combinations 
of  stimuli  is  seen  in  the  behaviour  of  Littorina  neritoides,  a  tiny  mollusc  which 
inhabits  the  rocky  shores  of  Etu-opean  seas.  Fraenkel  (1927)  showed  experi- 
mentally that  it  was  always  geo -negative,  photo -negative  always  when  out  of 
the  water  and  when  normally  orientated  in  the  water,  but  photo -positive  when 


Balanus 


0^ 

Carassius 


■'^=-^ 


Glossina 


Littorina 


46 


THE   EYE   IN   EVOLUTION 


Forficula 


Two  members  of 
Polyzoan  colony 


Caterpillar 


Any  u  ilia 


in  water  and  upside-down,  one  stimulus  (the  presence  of  water)  thus  modifying 
the  influence  of  another  (light).  Its  geo -negativity  drives  it  to  the  surface  of 
the  sea  and  if  it  surfaces  in  bright  light  it  returns  to  the  water  because  of  its 
photo  negativity  ;  if  it  surfaces  beneath  a  submerged  rock  its  positive  photo- 
taxis  makes  it  crawl  beneath  it  in  the  upside-down  position  until,  reaching  the 
air,  its  negative  phototaxis  keeps  it  in  a  shaded  cleft.  Again,  when  the  gardener 
traps  an  earwig  in  a  flower-pot  containing  dry  straw  inverted  on  a  cane,  he  is 
utilizing  the  fact  that  Forficula  deinonstrates  photokinesis,  thigniotaxis,  hydro- 
kinesis  and  negative  geotaxis. 

A  change  in  response  during  the  development  of  the  animal  is  well 
exemplified  in  the  case  of  some  marine  worms  ;  these  are  usually 
photo-positive  when  they  leave  the  egg  so  that  they  come  to  the 
surface  and  swim  ;  at  a  later  stage  they  become  photo-negative  with 
the  result  that  they  burrow  in  the  mud  and  crawl  (Mast,  1911).  The 
larva?  of  the  polyzoan  sea-mat,  Bugula,  similarly  disperse  under  a 
positive  phototaxis,  but  after  a  few  hours  turn  photo -negative  so  that 
they  attach  themselves  to  the  bottom  and  undergo  metamorphosis 
(Grave,  1930  ;   Ljoich,  1949). 

These  changes  may  be  associated  with  stages  in  the  development  of  the 
visual  cells.  Thus  the  larvte  of  the  cat-flsh,  Ameiurus,  are  initially  imresponsive 
to  light  at  a  stage  when  the  visual  elements  are  not  fully  differentiated  ;  later 
they  become  photo -negative,  a  phase  during  which  the  rods  and  cones  are 
contracted  and  show  no  retinomotor  reactions  ;  finally  the  larvae  become 
photo -positive,  a  phase  characterized  by  the  commencement  of  retinomotor 
reactions  (Armstrong,  1949). 

A  change  in  response  may  also  accompany  a  change  of  habit. 
Thus  young  caterpillars  of  Porthesia  are  strongly  photo-positive  when 
they  are  hungry,  a  response  which  normally  leads  them  upwards  to  the 
leaves  of  their  food  plant,  but  the  response  is  lost  after  feeding  ;  while 
male  and  female  ants  become  temporarily  photo-positive  at  the  time 
of  their  nuptial  flight,  a  reaction  lost  when  they  shed  their  wings 
(Loeb,  1918). 

Another  interesting  example  of  this  type  of  change  to  suit  a  marked  change 
in  habit  is  the  common  eel,  Anguilla.  At  the  stage  of  sexual  maturity  in  the 
autumn  when  it  lea\es  fresh  water  to  migrate  downstream^  on  its  journey  to 
its  mating  grounds  in  the  Sargasso  Sea,  there  is  a  great  increase  in  the  size  of 
the  eyes  and  the  fish  becomes  photo-negative.  This  season  coincides  with  the 
safety  afforded  by  floods  and  moonless  nights  and  the  fish  avoids  the  light  to 
such  purpose  that  its  nuptial  journey  can  be  checked  and  the  eels  diverted  into 
traps  in  large  numbers  by  means  of  underwater  lights  shining  upstream 
(Lowe,  1952). 

A  phototactic  response  of  this  type  may  be  so  prepotent  that,  although 
generally  biologically  useful,  it  may  driv^e  the  animal  to  destruction.  Thus  the 
stimulus  which  leads  the  moth  to  fly  towards  the  sun  will  drive  it  into  the 
candle-flame  ;  the  same  response  in  the  newly  hatched  larva  of  Euproctis  which 
normally  loads  it  upwards  towards  the  leaves  of  its  food  plant  will  force  it  to 


LIGHT   AND  MOVEMENT  47 

migrate  downwards  to  starvation  if  illuminated  from  below  (Loeb,  1918  ; 
Lammert,  1925  ;  v.  Buddenbrock,  1930)  ;  while,  provided  the  stimulating  light 
is  sufficiently  bright,  the  negative  phototaxis  of  the  larva  of  the  bluebottle, 
Calliphora,  will  induce  it  to  approach  a  source  of  ammonia  of  lethal  concentra- 
tion (Hurst,  1953). 

Andrews.     Physiol.  ZooL,  25,  240  (1952).  Claus,   Grobben   and   Kiihn'a    Lhb.   der 

Armstrong.    Anat.  Rec,  105,  515  (1949).  ZooL,  Berlin  (1932). 

Bolwig.      Brit.  J.   anim.    Behav.,   2,    144  Lammert.       Z.    vergl.     Physiol.,    3,    225 

(1954).  (1925). 

V.  Buddenbrock.     Z.  vergl.   Physiol.,  13,  Loeb.     Forced  Moveinents,   Tropisma  and 

164  (1930).  Animal  Conduct,  Phila.  (1918). 

Clark.    J.  exp.  ZooL,  51,  37  (1928)  ;   58,  31  Lowe.    J.  Anim.  EcoL,  21,  275  (1952). 

(1931)  ;   66,  311  (1933).  Lynch.    JSioZ.  JSmZZ.,  97,  302  (1949). 

Fox.     Proc.  Carnb.  philos.  Soc.  biol.  Sci.,  Mast.    Light  and  the  Behavior  of  Organisms, 

1,219(1925).  N.Y.  (1911). 

Fraenkel.    Z.  vergl.  Physiol.,  5,  585  (1927).  Biol.  Rev.,  13,  186  (1938). 

Goustard.     C.  R.  Acad.  Sci.  (Paris),  227,  Mast   and    Pusch.        Biol.    Bull.,    46,    55 

785  (1948)  ;   228,  864  (1949).  (1924). 

C.  R.  Soc.  Biol.  (Paris),  144,  485  (1950).  Matthews.    J.  exp.  BioL,  30,  268  (1953). 

Grave.    J.  Morph.  Physiol.,  4i9,  355  {1930).  Medioni.     C.   R.  Soc.   Biol.   (Paris),   148, 

Gunn,     Kennedy     and     Pielou.       Nature  2071  (1954). 

(Lond.),  140,  1064  (1937).  Payne.     Biol.  Bull.,  18,  188  (1910)  ;    21, 

Harper.     Biol.  Bull,  10,  17  (1905).  297  (1911). 

Henke.     Z.  vergl.  Physiol.,  IZ,  53'^  (\930).  Richard.     C.   R.  Acad.  Sci.   (Paris),  226, 

Hurst.     AWwre  (Lond.),  171,  1120  (1953).  356(1948). 

Jack  and  Williams.     Bull.  ent.  Res.,  28,  Ruppell   and    Schein.      Vogelzug.,   12,    49 

499  (1937).  (1941). 

Kiihn.      Die    Orieyitierung    der    Tiere    im  Viaud.     C.  R.  Soc.  Biol.  (Paris),  143,  534 

iJaum,  Jena  (1919).  (1949). 

Bethea  Hb.  norm.  path.  Physiol.,  12  (I),  Viaud    and    Medioni.      C.    R.   Soc.    Biol. 

17  (1929).  (Paris),  143,  1221  (1949). 

The  Types  of  Phototactic  Response 

We  shall  now  proceed  to  exemplify  the  various  types  of  phototactic 
responses  ;  but,  as  we  have  just  seen,  it  is  to  be  remembered  that 
animals  usually  orientate  themselves  in  more  than  one  way  depending 
on  the  circumstances  prevailing.  It  is  less  correct  to  say,  for  example, 
that  an  animal  is  telotactic  than  that  it  may  exhibit  a  telotactic 
reaction.  Thus,  as  we  shall  see,  some  ciliated  Protozoa  or  worms  show 
an  undifferentiated  photokinetic  response  with  one  stimulus  and  a 
klinotactic  or  tropotactic  response  with  another,  while  in  its  complex 
but  very  efficient  mechanism  of  orientation,  the  honey-bee  combines 
tropotaxis,  telotaxis  and  menotaxis  with  mnemotaxis. 

KLINOTAXIS 

The  most  primitive  directed  orientation  to  light  is  by  klestotaxis 
whereby  turning  movements,  normally  alternating  regularly,  are  specific- 
ally orientated  with  respect  to  the  light.  This  is  well  exemplified  in  the 
behaviour  of  flagellated  or  ciliated  Protozoa  or  the  maggot  larvae  of 
certain  common  flies.  Each  of  these  shows  a  different  type  of  response. 
The  Protozoa  orientate  themselves  as  a  result  of  successive  stimuli 
falling  on  a  photosensitive  organ  periodically  exposed  as  they  rotate 


48 


THE   EYE   IN   EVOLUTION 


Euglena 


longitudinally  by  means  of  cilia,  maggots  by  muscular  contraction  as 
they  crawl. 

The  Flagellates,  protozoans  which  swim  by  means  of  a  flagellum 
much  after  the  manner  of  a  gondolier,  in  reverse,  with  his  single  oar, 
are  frequently  photosensitive.  Some  of  them  retain  a  primitive  photo- 
kinetic  response  whereby  they  become  inactive  in  low  illumination  and 
resume  activity  if  the  light  is  increased.  This  simple  kinetic  response 
determining  general  activity  is,  however,  supplemented  by  a  shock- 
reaction  which  determines  orientation  ;  for  this  purpose  they  have 
evolved  a  sensitized  area  specially  modified  for  the  reception  of  the 
stimulus.  In  a  homogeneous  environment  they  take  a  direct  course 
undergoing  continuous  rotation  on  a  longitudinal  axis  as  they  are 
propelled  by  the  flagellum  ;  to  variations  of  the  intensity  of  light  they 
respond  by  abrupt  changes  in  the  rate  and  direction  of  movement 
either  towards  or  away  from  the  light.  Once  orientated  they  are  not 
held  on  a  direct  course  by  the  continuing  action  of  light,  but  if  they 
diverge,  the  orientating  stimulus  changes  and  immediately  recalls  them 
automatically.  The  automaticity  of  the  response  is  seen  if  the  field 
contains  two  beams  of  light  crossing  at  an  angle,  in  which  case  these 
organisms  orientate  themselves  and  proceed  in  a  direction  between  the 
two  beams  determined  by  their  relative  intensities  and  angles  of 
incidence  (Buder,  1917  ;  Mast  and  Johnson,  1932).  Their  photic 
responses  have  been  studied  most  fully  in  the  typical  species,  Euglena, 
a  transparent  green  Protozoon  photo -positive  in  weak,  photo -negative 
in  strong  light. ^ 

Euglena  viridis,  the  flagellate  infusorian  which  commonly  forms  the  green 
scvim  on  stagnant  fresh  water,  has  a  photosensitive  "  eye-spot  "  or  "  stigma  "  ^ 
situated  in  the  concavity  of  a  pigmented  shield  ^  in  close  association  with  the 
root  of  the  flagellum  ;  the  arrangement  is  such  that  when  the  surface  of  the  eye- 
spot  is  illuminated  the  photosensitive  substance  at  the  base  of  the  flagellum  is 
thrown  into  the  shadow  (Fig.  80).  It  follows  that  rotation  of  the  transparent 
organism  on  its  longitudinal  axis  produces  an  alternate  shading  and  exposure 
of  this  substance  unless  it  is  orientated  so  as  to  proceed  directly  towards  or 
away  from  a  light  (Fig.  21).  If  the  direction  of  the  rays  is  changed  through 
90°  to  illuminate  the  organism  laterally,  no  reaction  occurs  until  the  rotation 
brings  the  eye -spot  to  face  the  light  thus  throwing  the  photosensitive  area  into 
the  shade  ;  thereupon  the  organism  suddenly  bends  away  from  the  light,  and, 
continviing  rotation  thus,  gradually  straightens,  a  response  which  is  repeated  on 
each  rotation  so  that  it  is  soon  proceeding  again  directly  away  from  the  new 
direction  of  the  light.  Subsequent  rotation  in  this  position  no  longer  produces 
changes  in  the  intensity  falling  upon  the  two  surfaces  and  the  organism  therefore 
proceeds  uninterruptedly  in  this  direction. 


1  Verworn  (1889),  Jennings  (1904),  Mast  (1911-3P,),  Bconcroft  (1913),  Buder  (1917), 
Mast  and  Gover  (1922),  Mast  and  Johnson  (1932),  and  others. 
^  p.  126. 
'  The  pigment  is  astaxanthin,  p.  120. 


LIGHT   AND   MOVEMENT 


49 


} 


Fig.  21. — Klinotaxis  in  a  Swimming  Organism. 

The  orientation  of  £'M5'Ze?ia  I'iVfrZ/s.  The  orientation  of  the  organism  as  it 
swims  away  from  the  hght  (coming  from  below)  rotating  in  a  wavy  path  ( 1  to  6). 
At  6  the  du'ection  of  the  light  is  reversed  to  come  from  above  ;  each  time  the 
receptor  area  is  shielded  by  the  pignient  the  organism  swerves  to  the  dorsal  side. 
After  an  initial  wavy  course  (7  to  8)  it  bends  laterally  across  the  path  of  the 
beam,  and  from  13  to  18  it  again  swims  as  before  away  from  the  light  (after 
Jennings,  1906). 


The  Ciliates,  which  orientate  themselves  by  means  of  ciha  much 
as  a  rowing  boat  without  a  rudder,  react  phototactically  in  a  similar 
manner  (Fig.  22).  Thus  Stentor  cceruleus,  a  trumpet -shaped  ^  Protozoon, 
the  bell  of  which  is  surrounded  by  cilia  within  which  is  an  eccentrically 
placed  mouth,  exhibits  the  same  reaction  by  virtue  of  the  fact  that  the 
oral  surface  is  more  photosensitive  than  the  aboral  (Jennings,  1904  ; 
Mast,  1906-11). 

A  similar  arrangement  multiplied  many-fold  is  seen  in  colonial  forms,  such 
as  Volvox  globator,  a  green  organism  found  in  fresh-water  pools,  formed  of  a 
hollow  spherical  colony  of  some  10,000  individual  zooids  each  of  which  is 
equipped  with  two  fiagella  and  a  stigma  protected  on  one  side  by  a  pigmentary 
shield  ;  stimulation  of  the  sensitive  area  results  in  the  translation  of  the  diagonal 

1  The  name  is  from  Stentor,  the  herald  of  the  Iliad  who  had  a  loud  trumpet-like 
voice. 

S.O.— VOL.  I.  4 


Stentor 


Volvox 


50 


THE   EYE   IN   EVOLUTION 


6 


5      V 


^^-. 


N 


111 


M 

Fig.  22. — Klinotaxis  in  Stentor  cceruleus. 

In  1  and  2  the  organism  is  seen  swimming  away  from  the  hght  shining 
from  behind  it  (indicated  by  the  lower  arrows,  M).  As  it  swims  it  rotates  so 
that  the  oral  side  (o)  and  the  aboral  side  (a)  are  equallj^  stimulated.  At  3  the 
original  light  is  turned  off  and  a  lateral  light  (indicated  by  the  side  arrows,  N) 
is  turned  on.  As  soon  as  the  oral  side  faces  the  light  the  organism  turns  rapidly 
away  to  position  4  and  continues  in  this  sense  until,  at  6,  the  oral  side  is 
approximately  equally  exposed  to  light  in  all  positions  on  the  spiral  course 
(after  Mast,  1911). 


^^^axnuP 


Maggot   of  Musca 


Maggot     of     Calli- 
phora 


stroke  of  the  flagella  into  a  backward  sweep,  the  whole  number  beating  in  unison 
and  thus  orientating  the  colony  in  the  required  direction  (Mast,  1906-27  ;  Mast 
and  Johnson,  1932). 

Crawling  organisms  such  as  the  maggots  of  flies  (the  house-fly, 
Musca  domestica,  the  bhiebottle,  Callij^Jiora  erythrocephala,  etc.)  were 
among  the  first  organisms  to  be  investigated  in  this  way.^  Their 
phototactic  response  is  somewhat  different  from  that  of  swimming 
Flagellates  or  Ciliates.  Although  the  photosensitive  structures  are  ex- 
ceedingly primitive,  the  anterior  end  of  the  larva  is  negatively  respon- 
sive to  light.  When  crawling  it  raises  its  head  in  the  air  and  alternately 
deviates  to  either  side  as  if  in  exploratory  movements  ;  on  lateral 
illumination,  the  head  is  swung  violently  away  from  the  light,  a  reaction 
which  is  repeated,  turning  the  animal  round  until  the  head  is  equally 
illuminated  at  two  successive  deviations,  whereupon  it  crawls  directly 

1  Pouchet  (1872),  Holmes  (1905),  Loeb  (1905-18),  Mast  (1911),  Herms  (1911), 
Patten  (1914-16),  Ellsworth  (1933),  Welsh  (1937). 


LIGHT   AND  MOVEMENT 


51 


II 


Fig.  23. — Klinotaxis  in  a  Crawling  Organism. 

The  maggot  is  photo-negative  and  crawls  away  from  the  hght  (below). 
From  the  initial  position,  1,  it  contracts  into  2,  elongates  into  3  and  contracts 
again  into  4,  each  time  swinging  its  head  across  to  one  or  other  side.  So  long  as 
the  sides  of  the  head  are  equally  illuminated  its  path  is  straight.  At  3,  the 
lower  light  is  switched  off  and  the  side  light  switched  on  ;  the  organism 
immediately  swings  violently  into  position  .5.  Thereafter  it  contracts  to  6,  and, 
having  swaing  in  the  opposite  direction  to  7,  again  receives  preferential  illu- 
mination on  the  side.  It  therefore  swings  again  violently  to  8  and,  having 
contracted  to  9,  proceeds  again,  as  before,  directly  away  from  the  light  (10) 
(after  Mast,  1911). 


away  from  the  light  (Fig.  23).  If  a  hght  is  persistently  flashed  on  the 
same  side  on  each  deviation  of  the  head,  a  circus  movement  is  produced, 
and  if  two  directed  lights  are  simultaneously  employed  the  animal 
crawls  away  at  a  direction  half-way  between  the  two  beams  if  they  are 
equal,  or  proportionately  more  nearly  in  line  with  the  brighter  beam  if 
they  are  unequal  (Patten,  1914). 


Bancroft.    J.  exp.  ZooL,  15,  383  (1913). 
Buder.    Jb.  wiss.  Bot.,  58,  105  (1917). 
Ellsworth.     Ann.  entom.  Soc.  Amer.,  26, 

203  (1933). 
Herms.    J.  exp.  ZooL,  10,  167  (1911). 
Holmes.     J.   comp.   Neurol.,   15,   98,   305 

(1905). 
Jennings.      Publ.   Carnegie   Inst.,   Wash., 

No.  16,  256  (1904). 
Loeb.      Studies    in    General    Physiology, 

Chicago  (1905). 
The  Dynamics  of  Living  Matter,  N.Y. 

(1906). 
Forces,  Movement  s,Tropis7ns  and  Animal 

Conduct,  Phila.  (1918). 
Mast.    J.  exp.  Zool.,  3,  359  (1906). 


Light   and  the   Behavior  of  Organisms, 

N.Y.  (1911). 
Biol.  Zbl.,  34,  641  (1914). 
Z.  vergl.  Physiol.,  5,  730  (1927). 
Biol.  Rev.,  13,  186  (1938). 
Mast    and    Cover.      Biol.    Bull.,   43,    203 

(1922). 
Mast  and  Johnson.     Z.  vergl.  PliysioL,  16, 

252  (1932). 
Patten.    J.  exp.  ZooL,  17,  213  (1914)  ;   20, 

585  (1916). 
Pouchet.     Rev.  mag.  ZooL,  23,   HO,   129, 

183,  225,  261,  312  (1872). 
Verwom.     Psychophysiologische  Protisten- 

studien,  Jena  (1889). 
Welsh.    Science,  85,  430  (1937). 


52 


THE   EYE   IN   EVOLUTION 


TROPOTAXIS 


In  tropotaxis  at  least  two  symmetrical  receptor  organs  are  neces- 
sary, and  instead  of  relying  on  successive  exposures  of  a  single  receptor 

1  1  1  J 


Fig.  24. — The  Tropic  Response  of  Larva  of  Aresicola. 

A.  The  head  of  the  larva  with  two  symmetrical  eyes. 

B.  The  path  of  movement  of  the  larva  :    in   1   to  4  the  light  remains 
stationary  ;    in  5  to  8  it  is  placed  at  right  angles  (after  Mast). 

by  trial  movements,  the  animal  orientates  itself  by  the    simultaneous 
comparison  of  the  intensity  of  stimulation  on  the  tivo  sides.    In  the  simple 


r         /5 
\3 

Fig.  25. — Negative 
Tropotaxis. 

The  path  of  the  flour- 
moth  larva,  Ephestia, 
starting  from  the  small 
circle  with  a  light  shown 
as  indicated  by  the  arrow, 
1.  Each  successive  num- 
ber indicates  the  position 
of  a  new  light  turned  on 
when  the  animal  reached 
the  corresponding  point 
on  its  track  ;  its  direction 
changed  in  a  straight  line 
directly  from  the  light 
(after  I3randt). 


forms  inequality  of  stimulation  leads  to  orienta- 
tion in  the  required  direction  by  a  reciprocal 
coordination  of  the  muscles  of  either  side  of  the 
animal  controlled  by  the  nervous  system  :  if 
there  is  an  excess  of  stimulation  on  one  side,  a 
turning  movement  occurs  ;  if  equality,  the 
stimuli  cancel  each  other  out  and  the  animal 
progresses  straight  forwards  ;  and  if  it  subse- 
quently strays  from  its  path  a  renewed  in- 
equaUty  corrects  the  deviation.  It  follows  that 
if  two  sources  of  light  appear  simultaneously 
the  animal  orientates  itself  directly  between 
them  in  proportion  to  their  relative  intensities. 

The  larvae  of  some  marine  worms  provide  the 
most  simple  type  of  this  reaction  ;  they  swim  by  the 
activity  of  cilia  but  orientation  is  the  result  of 
muscular  contraction.  Of  these,  the  larvae  of  the 
polychsete  worm,  Arenicola,  have  been  most  inten- 
sively studied  (Mast,  1911  ;  Garrey,  1918).  These  are 
minute  creatures  with  two  eyes  anteriorly  and  a  band 
of  cilia  at  either  end  ;   as  they  swim  they  rotate  longi- 


LIGHT   AND   MOVEMENT  53 

tudinally  so  that  on  lateral  illumination  each  eye  is  alternately  illuminated  and 
shaded.  As  each  eye  becomes  exposed  to  the  light,  the  muscles  of  the  illumi- 
nated side  contract  violently  turning  the  head  towards  the  light  (Fig.  24).  Since 
this  occurs  twice  during  each  rotation,  the  larva  is  rapidly  orientated  towards 
the  light  until  the  two  eyes  are  equally  illuminated  all  the  time,  whereupon 
further  muscvilar  contraction  and  orientation  cease. 

A  very  similar  and  typical  reaction  is  seen  in  the  rotifer,  Branchionus 
(Viaud,  1948),  and  in  the  photo-negative  larvae  of  the  flour-moth,  Ephestia, 
which  are  provided  on  either  side  of  the  head  with  an  aggregate  eye  composed  of 
six  ocelU  (Brandt,  1934)  (Fig.  25). 

A  further  evolutionary  step  is  seen  in  earthworms.  As  is  the 
general  rule,  impulses  originating  in  the  photoreceptors  on  one  side  of 
the  body  determine  orientation  by  inducing  a  simple  reflex  contraction 
of  the  muscles  on  the  opjDOsite  side,  but  it  is  obvious  that  if  these 
impulses  can  be  modified  and  integrated  in  the  central  nervous  system, 
a  more  effective  response  is  obtained. 

Such  responses  have  been  fully  studied  in  the  earthworm,  Lumbricus 
terrestris,  and  Eisenia  foetida.^  In  these  animals  the  existence  of  photoreceptor 
organs  associated  with  a  subepidermal  nerve-net  was  demonstrated  by  Richard 
Hesse  (1896)  and  confirmed  by  W.  N.  Hess  (1925)^  ;  they  are  most  numerous 
and  receptive  near  the  anterior  extremity  of  the  animal.  The  response  to  light 
is  somewhat  complicated  and  has  given  rise  to  some  difference  of  opinion  ;  but 
it  would  seem  most  likely  that  if  the  worm  is  sluggish  and  is  exposed  to  dim 
light,  it  slowly  extends,  turns  its  anterior  end  away  from  the  light,  and  continues 
to  move  thus.  If,  however,  the  worm  is  active  when  it  is  illuminated  from  the 
side,  the  anterior  end  is  quickly  raised  and  turned  in  the  direction  opposite  to 
that  in  which  it  happens  to  be,  whether  it  is  directed  to  the  light  or  not,  and 
thereafter  swung  from  side  to  side,  a  position  and  direction  being  eventually 
adopted  in  which  the  anterior  end  is  least  exposed  to  the  light. 

If  now  the  cerebral  ganglion  is  removed  or  destroyed  or  if  it  is  inhibited  by 
a  reduction  of  temperature  or  the  injection  of  depressant  drugs  such  as  cocaine 
or  alcohol,  the  opposite  reaction  of  a  positive  phototaxis  results  ;  in  these 
circumstances  lateral  illumination  of  the  more  posterior  photoreceptors  produces 
a  contraction  of  the  muscles  of  the  same  side  which  causes  the  worm  to  turn 
towards  the  light,  a  reaction  due  to  reflexes  mediated  through  the  ventral  cord 
(Hess,  1924  ;  Prosser,  1934).  It  would  seem  that  normally  this  weak  positive 
ipsilateral  response  mediated  through  the  cord  is  overshadowed  by  the  stronger 
negative  contralateral  response  derived  from  the  receptors  in  the  highly  sensitive 
anterior  end  and  mediated  by  the  cerebral  ganglion,  and  that  the  final  response 
of  the  animal  is  the  resultant  of  the  two  antagonistic  tendencies  after  integration 
and  coordination  in  the  central  nervous  system. 

It  is  obvious  that  the  bilateral  balance  of  the  tropotactic  response 
will  be  upset  if  one  eye  is  blinded,  either  by  painting  it  over  or  by  its 
removal,  so  that  with  lateral  illumination  the  animal  will  tend  con- 

1  Loeb  (1894),  R.  Hesse  (1896),  Parker  and  Arkin  (1901),  Smith  (1902),  Adams 
(1903),  Hoknes  (1905),  Harper  (1905),  Mast  (1911),  W.  N.  Hess  (1924),  Nomura  (1926- 
27),  Prosser  (1934),  and  others. 

2  pp.  131,  518. 


54 


THE   EYE   IN  EVOLUTION 


Fig.  26. — Positive 
Tropotaxis. 

The  tracks  taken  by  the 
woodlouse,  Armadilli- 

dium,  blinded  on  the 
right  side,  a,  b,  c,  d.  The 
tracks  of  the  louse  in 
darkness.  e,  /.  Circvis 
movements  with  the  light 
overhead  (after  Henke). 


1      i         i      i     i 


Fig.  27.— Circus  Movements  in  a 
Unilaterally  Blinded  Noioxecta. 

The  animal  directs  itself  towards  the  light 
above,  indicated  by  arrows.  The  illustra- 
tion shows  the  path  taken  in  repeated  trials. 
From  left  to  right,  the  tracks  are  the  1st,  3rd, 
35th,  39th,  41st  and  43rd  attempts.  It  is 
seen  that  the  initial  attempts  are  circus 
movements  which  gradually  straighten  out 
until  eventually,  after  some  trials,  the  track 
is  almost  straight  (after  Clark,  1928). 


Armadillidium 


stantly  to  deviate  towards  one  side,  or  in  an  overhead  light  to  perform 
circus  movements.  This  deviation  towards  the  seeing  side  after 
unilateral  blinding  is  well  seen  in  the  case  of  the  woodlouse,  Armadilli- 
dium, a  Crustacean  which  lives  under  stones  or  decaying  wood 
(Henke,  1930)  (Fig.  26).  In  some  instances  these  abnormal  deviations 
occur  for  an  indefinite  time,^  but  in  others  a  process  of  adaptation  sets 
in  so  that  the  circus  movements  gradually  cease  and  the  path  eventually 
straightens  out  ^  (Fig.  27).  An  exception  to  this  type  of  behaviour  is 
seen  in  the  evolutionary  development  of  the  tropotactic  response 
whereby  each  eye  becomes  regionally  differentiated  so  that  each  can 
act  as  a  symmetrical  pair  of  organs.  Thus  the  eyes  of  some  worms  and 
insects  possess  two  functionally  different  regions  one  of  which  initiates 

1  The  snail.  Helix — von  Buddenbrock  (1919)  ;  the  millipede,  Julus — Muller  (1924)  ; 
the  silver  T'sh,  Lepisma — Meyer  (1932)  ;  the  larva  of  the  flour -moth,  Ephestia — Brandt 
(1934). 

2  Thf^  water-boatman,  Notonecta — Hobnes  (1905),  Clark  (1928),  Liidtke  (1935-42)  ; 
the  robber-fly,  Proctacanthus — Garrey  (1918);  the  whirligig  beetle,  Dineutus  assimilis — 
Clark  (1931-33),  Raymont  (1939). 


LIGHT   AND   MOVEMENT 


55 


turning  towards  one  side  and  the  other  in  the  opposite  direction  ; 
although  the  responses  are  typically  tropotactic  in  nature,  the  telotactic 
response  is  simulated  since  each  eye  exerts  a  symmetrical  control. 

Among  worms,  these  reactions  have  been  most  closely  studied  in  Planaria 
maculata,  one  of  the  turbellarian  worms. ^  The  normal  individual  orientates 
photo -negatively,  illumination  of  one  side  producing  a  muscular  contraction  of 
the  opposite  side  so  that  the  worm  proceeds  directly  away  from  the  light.  If, 
however,  one  eye  is  dissected  out  and  the  light  is  accurately  directed  or  if  different 
parts  of  the  remaining  eye  are  removed,  it  can  be  shown  that  stimulation  of  the 
elements  of  the  anterior  end  of  the  eye  makes  the  animal  turn  from  the  illuminated 
side,  while  stimulation  of  the  posterior  or  ventral  parts  of  the  eye  induces  a 
turning  towards  the  illuminated  side.  The  boundary  between  these  two  con- 
stitutes the  "  line  of  fixation  "  (a  functional  fovea)  stimulation  of  which  evokes 
no  turning  movements  (Liidtke,  1942).  A  somewhat  similar  reaction  is  seen  in 
the  drone-fly,  Eristalis,  and  related  insects  (Mast,  1923). 


Adams.    Amer.  J.  Physiol.,  9,  26  (1903). 
Boring.    J.  anim.  Behav.,  2,  229  (1912). 
Brandt.         Z.    vergl.    Physiol.,    20,     646 

(1934). 
von  Buddenbrock.     Zool.  Jb.,  Abt.  Zool. 

Physiol,  37,  315  (1919). 
Clark.    J.  exp.  Zool.,  51,  37  (1928)  ;  58,  31 

(1931)  ;    66,  311  (1933). 
Garrey.    J.  gen.  Physiol.,  1,  101  (1918). 
Harper.     Biol.  Bull.,  10,  17  (1905). 
Henke.     Z.  vergl.  Physiol.,  13,  534  (1930). 
Hess,  W.  N.    J.  Morph.,  39,  515  (1924)  ; 

41,  63  (1925). 
Hesse,  R.    Z.  wiss.  Zool.,  61,  393  (1896). 
Holmes.     J.   comp.   Neurol.,   15,   98,   305 

(1905). 
Loeb.    Pfliigers  Arch.  ges.  Physiol.,  56,  247 

(1894). 
Liidtke.    Z.  vergl.  Physiol.,  22,  67  (1935)  ; 

26,  162  (1938). 
Biol.  Zbl.,  62,  220  (1942). 


Mast.      Yearbook   Carnegie   Inst.,    9,    131 

(1910). 
Light  and   the   Behavior  of  Organists, 

X.Y.  (1911). 
J.  exp.  Zool.,Zi,  109  (1923). 
Meyer.     Z.  wiss.  Zool.,  142,  254  (1932). 
MuUer.     Zool.  Jb.,  Abt.  Zool.  Physiol.,  40, 

399  (1924). 
Nomura.     Tohoku  Imp.   Univ.  Sci.  Rep., 

Ser.  iv,  1,  294  (1926)  ;    2,  1  (1927). 
Parker  and  Arkin.     Amer.  J.  Physiol.,  5, 

151  (1901). 
Pearl.    Quart.  J.  micr.  Sci.,  46,  509  (1903). 
Prosser.     J.  Neurol.   Psychopath.,  59,  61 

(1934). 
Raymont.    Biol.  Bull.,  77,  354  (1939). 
Smith.    A7ner.  J.  Physiol.,  6,  459  (1902). 
Steinmann    and    Bresslau.      Die  Strudel- 

wiirmer,  Leipzig  (1913). 
Taliaferro.    J.  exp.  Zool.,  31,  59  (1920). 
Viaud.     Le   phototropisme    animal,    Paris 

(1948). 


\l 


Turbellarian 
worm 


TELOTAXIS 

In  TELOTAXIS  orientation  is  directly  towards  {or  away  from)  the 
source  of  light  ;  there  is  no  question  of  bilateral  balance,  nor,  indeed, 
are  two  eyes  necessary  ;  but  it  is  essential  to  have  an  eye  with  several 
receptor  elements  which  are  able  to  ajDpreciate  the  direction  of  a  single 
light  or  each  of  several  sources  simultaneously,  and  a  central  nervous 
organization  which  can  inhibit  all  stimuli  except  one.  It  is  this  factor 
of  inhibition  which  forms  the  essential  evolutionary  advance,  for  it 
provides  a  mechanism  much  more  efficient  than  is  available  to  the 
previous  types  which  respond  to  the  summation  of  all  stimuli  (Figs. 
28  to  31)."^ 

1  Pearl  (1903),  Mast  (1910-11),  Boring  (1912),  Steinmann  and  Bresslau  (1913),  and 
particularly  Taliaferro  (1920). 


56 


THE   EYE   IN   EVOLUTION 


This  type  of  response  is  characteristic  of  a  large  number  of 
Arthropods,  particularly  Insects,  in  laboratory  conditions;  most  of 
them  react  in  a  similar  manner.^  Whether  flying  or  walking  deprived 
of  their  wings,  they  proceed  directly  towards  a  light  ;  if  two  lights  are 


Figs.  28-29. — Telotaxis  in  the  Bee. 


Fig.  28. 


Fig.  29. 


Fio.  28. — The  tracks  of  two  bees  in  a  relatively  straight  line  towards  a  light 

(indicated  by  the  circle). 
Fig.  29. — The  path  taken  by  a  bee  in  a  directive  light  (indicated  by  the  arrow), 

when  the  left  eye  is  blackened.     There  are  some  circus  movements  to  the 

right  initially,  whereafter  the  insect  eventually  walks  directly  towards  the 

light  (Minnich,  1919). 


Figs.   30-31. — Telotaxis  in  a  Two-light  Experiment. 


Lz 


Fig.  31. 

Fig.  30. — The  tracks  of  5  hermit  crabs  in  their  taxes  towards  two  lights,  L^  and 
Lz-  Each  part  of  the  track  is  directed  towards  one  light  only.  1,  4  and  3 
travel  directly  to  L2.  2  does  so  mitially  and  after  a  short  time  directs 
itself  towards  L^  but  rapidly  resumes  the  path  straight  to  L2'  5,  after 
an  initial  start  towards  L2,  travels  straight  towards  L^  (after  von  Budden- 
brock,  1922). 

Fig.  31. — The  track  of  an  isopod,  Aega.  For  a  time  it  follows  a  zigzag  course 
alternating  between  ij  and  L^  until  it  finally  makes  up  its  mind  to  travel 
straight  towards  L^  (after  Fraenkel,  1931). 

^  The  blow-fly,  CalUphora  vomitoria — Radl  (1903)  ;  the  aquatic  nepid,  Ranatra 
— Holmes  (1905)  ;  the  fruit-fly,  Drosophila — Carpenter  (1908)  ;  the  butterfly, 
Vanessa — Dollej-  (1916)  ;  the  robber-fly,  Erax  rufibarbis — Garrey  (1918)  ;  the  honey- 
bee, Apis — Minnich  (1919),  Clark  (1928),  Urban  (1932)  ;  the  drone-fly,  Eristalis—M&at 
(1923),  Dolley  and  Wierda  (1929)  ;  the  flesh-fly,  Sarcophaga—W eWington  (1953)  ;  the 
locust,  Locusta  nngraforia,  in  the  hopper  stage — Chapman  (1954)  ;   and  others. 


V 


LIGHT   AND   MOVEMENT 

exposed  they  may  take  a  zig-zig  path  initially,  as  if  hesitating  between 
the  two,  but  soon  the  insect  goes  towards  one,  usually  the  stronger, 
neglecting  the  other  (Figs.  30  and  31)  ;  and  if  it  is  unilaterally  blinded, 
after  some  initial  circus  movements  it  again  jjroceeds  straight  towards 
the  light  (Fig.  29).  Experimenting  with  termite  larvae  (Calotermes), 
Richard  (1948)  found  that  the  direction  of  motion  was  determined 
by  the  direction  of  the  rays  rather  than' by  the  intensit}'  gradient, 
but  that  the  latter  determined  the  straightness  of  the  path.     The 


57 


Fig.  32. — The  Relative  Role  of  the  Ocelli  and  Compound  Eyes 
IN  Telotaxis. 

A,  B,  C,  D,  the  track  of  the  flesh-fly,  Sarcophaga,  in  a  darkened  room 
towards  a  Hght  indoors  (6-watt  lamp,  marked  by  the  circle). 

A,  a  fly  with  all  its  eyes  uncovered  ;  B,  only  the  compound  eyes  un- 
covered ;  C,  only  the  ocelli  uncovered  ;  D,  all  the  eyes  covered.  It  is  seen  that 
in  C  and  D  the  insect  is  completely  at  a  loss. 

A',  B',  C" ,  D' .  Movements  of  the  same  individuals  over  the  ground  out- 
doors towards  the  sun.  It  is  seen  that  the  fly  with  only  its  ocelli  uncovered 
orientates  itself  well.  The  irregularities  of  the  tracks  were  produced  by 
responses  to  patches  of  cirrus  cloud  passing  overhead  and  do  not  occur  when 
the  sky  is  clear. 

E.  The  track  of  the  larva  of  the  sawfly,  Neodiprion,  indoors,  and  E'  out- 
doors. It  is  seen  that,  in  contradistinction  to  Sarcophaga,  the  track  outdoors 
is  straighter  than  that  indoors. 

The  time-marks  in  all  tracks  show  lO-second  intervals  (W.  G.  Wellington, 
Nature). 


stemmata  of  larvae  generally  mediate  this  activity,  but  in  the  adult  as 
a  rule  the  effective  organ  is  the  compound  eye,  the  action  of  which  is 
frequently  supplemented  by  the  ocelli  which,  however,  may  be  quite 
ineffective  by  themselves. 

Fig.  32,  for  example,  taken  from  Wellington's  (1953)  work,  shows  the 
phototactic  response  of  the  common  dipterous  parasite,  the  fiesh-fiy,  Sarcophaga, 
crawling  with  clipped  wings  towards  an  ordinary  (non-polarized)  light  in  the 


58 


THE   EYE   IN   EVOLUTION 


Sarcophaga 


Honey-bee 


Mysid 


Eupaguriis 


Photinus 


laboratory  ;  its  path  towards  the  light  with  all  its  eyes  uncovered  is  straight  ; 
with  only  its  compound  eyes  uncovered,  relatively  straight  ;  and  with  only 
its  ocelli  uncovered,  quite  indeterminate. 

The  compound  eye  of  the  average  adult  insect  is  well  equipped  to 
respond  accurately  to  a  telotactic  stimulus  of  this  type,  and  may  be 
specifically  differentiated  for  the  purpose.  In  the  honey-bee,  for 
example,  the  rapidity  and  accuracy  of  the  response  are  due  to  the 
functional  arrangement  of  this  organ  wherein  tropotactic  as  well  as 
telotactic  elements  are  found  ;  the  anterior  median  units  of  the  eye 
(ommatidia)  initiate  reflex  turning 
movements  to  the  contralateral  side, 
the  lateral  ommatidia  to  the  ipsilateral 
side,  while  the  central  ommatidia,  which 
alone  are  used  for  fixation,  initiate  none 
(Fig.  33).  The  animal  is  thus  provided 
with  a  very  efficient  mechanism  of 
orientation,  the  peripheral  parts  of 
which  can  initiate  turning  in  either 
direction  so  that  the  stimulus  is  rapidly 
directed  to  the  important  central  area, 
a  reflex  mechanism  which  is  analogous 
to  the  fixation  reflexes  in  man. 

A  more  plastic  mechanism  is  seen 
in  some  aquatic  Crustaceans  such  as 
the  tiny  mysids  of  aquarium  tanks 
{Hemimysis — Franz,  1911  ;  Fraenkel, 
1931)  or  the  hermit  crab,  Eupagurus 
(von  Buddenbrock,  1922  ;  Alverdes, 
1930).  The  latter  animal  goes  towards 
a  single  light,  and  even  although  it  con- 
tinually changes  its  method  of  progression,  now  walking  forwards,  now 
sideways  or  at  an  angle,  it  invariably  walks  straight  towards  one  light  in 
the  environment,  a  directness  of  path  unaffected  by  the  removal  of  one 
eye.  It  would  seem  that,  unlike  the  bee,  any  part  of  the  crab's  retina 
can  act  as  a  fixation  area,  and  that  it  must  be  endowed  with  a  more 
plastic  degree  of  visual  coordination. 

The  orientation  of  the  fire-fly,  Photinus  pyralis,  is  even  more  interesting 
(Mast,  1912  ;  Buck,  1937).  If  a  male  glows  ^  in  the  neighbourhood  of  a  female, 
she  raises  and  twists  her  abdomen  so  that  its  ventral  surface  is  directed  straight 
towards  him  no  matter  in  which  direction  he  may  be,  and  produces  a  momentary 
glow  ;  he  thereupon,  no  matter  in  which  direction  he  is  going,  turns  through 
any  required  angle  between  0°  and  180"'  towards  the  spot  whence  the  glow  came 
and  pr  ceeds  in  total  darkness  straight  towards  her.     These  responses,  which 


Fig.  33. — The  Telotactic  Turn- 
ing Response  in  the   Compound 
Eye. 

When  /  is  the  line  of  fixation  the 
arrows  show  the  direction  of  turning 
induced  by  iUumination  of  different 
regions  of  the  eye  (after  Kiihn). 


p.  742, 


LIGHT   AND   MOVEMENT 


59 


frequently  occur  when  one  eye  only  is  illuminated,  are  directionally  very  exact 
and  do  not  depend  on  the  persistence  of  the  stimulus— a  primitive  kind  of 
menotaxis. 

The  execution  of  these  movements  of  orientation  in  insects  is  the 
result  of  a  complex  series  of  coordinated  reflexes  in  the  wings  or  legs  of 
both  sides,  each  of  which  is  specifically  correlated  to  the  location  of  the 

Figs.   34-36. — The  Orientation  of  the  Robber-fly,   Proctaca.\thvs,  on  a 
White  Background  in  a  Horizontal  Beam  of  Light. 


Fig.  34. — The  upper  portion  of  the  left  eye  and  the  lower  portion  of  the  right 
eye  are  covered.  The  insect  is  leaning  to  the  left  and  turning  to  the 
right  towards  the  light. 


Fig.  35. — One  leg  has  been  removed  on 
the  right  side  while  the  light  conies 
from  the  left.  The  insect  is  seen  turn- 
ing to  the  left  towards  the  light  guided 
largely  by  its  left  front  leg. 


Fig.  36. — When  the  light  comes  from  the 
right,  in  order  to  orientate  itself  in  this 
direction,  the  left  front  leg  is  thrown 
over  to  the  right  side  and  is  used  to 
pull  the  animal  in  this  direction  (after 
Mast,  1924). 


stimulus  in  the  eyes.  The  excitation  of  a  particular  retinal  area  induces 
a  reaction  w^hich  orientates  the  insect  in  a  direction  such  that  the 
continuous  turning  allows  successive  retinal  points  to  be  stimulated 
until  the  fixation  ommatidia  are  reached  ;  once  this  orientation  has 
been  attained,  the  reflexes  become  inoperative,  and  if  any  subsequent 
deviation  occurs  further  reflex  re-orientation  immediately  corrects  it. 
These  reflexes  are  somewhat  analogous  to  the  segmental  scratch- 
reflexes  in  higher  mammals,  and  their  effects  have  been  explored 
experimentally  (as  by  rotatory  experiments  on  a  turn-table)  in  a  large 


60 


THE   EYE   IN   EVOLUTION 


Silver-fish 


Mosquito 


Gonodactylus 


number  of  species  by  numerous  observers.^  If  the  insect  is  illuminated 
from  in  front,  it  steps  forwards  using  all  its  legs  ;  if  from  the  side,  the 
front  legs  on  both  sides  step  towards  that  side  even  if  one  eye  only  or 
parts  of  the  eye  are  functional  (Fig.  34)  ;  and  if  the  front  leg  on  one 
side  is  removed,  on  lateral  illumination  the  front  leg  of  the  other  side 
is  extended  towards  the  light,  pulling  the  animal  round  towards  the 
normal  or,  if  necessary,  the  mutilated  side  so  that  it  can  orientate 
nearly  as  precisely  as  a  normal  insect  (Mast,  1923-24)  (Figs.  35  and  36). 

scoTOTAXis  (oKOTos,  darkness)  is  a  term  sometimes  employed  to  describe 
the  habit  of  some  organisms,  particularly  insects,  to  travel  towards  a  dark 
object  :  thus  insects  such  as  the  silver-fish,  the  caterpillar,  the  ant,  the  mosquito 
and  the  louse  ^  will  travel  towards  a  dark  screen  ;  if  such  a  screen  and  a  light 
are  exposed,  some  will  go  directly  away  from  the  light  (negative  phototaxis) 
and  some  towards  the  dark  screen  (scototaxis).^  The  stomatopod,  Oonodactylus, 
which  becomes  more  active  in  darkness,  will  always  seek  a  dark  shelter  rather 
than  a  bright  object  even  althovigh  it  has  to  swim  towards  the  light  to  get  there 
(Bolwig,  1954).  It  is  jorobable,  however,  that  in  most  cases  such  behaviour  can 
be  included  within  the  concept  of  negative  telotaxis,  althovigh  occasionally  the 
form  of  a  dark  object  may  be  important  in  the  orientation. 


Alverdes.  Z.  wiss.  ZooL,  137,  403  (1930). 
Bauers.  Z.  vergl.  Physiol.,  34,  589  (1953). 
Bolwig.      Brit.   J.   anim.    Behav.,   2,    144 

(1954). 
Buck.     Physiol.  ZooL,  10,  412  (1937). 
v.  Buddenbrock.    Wiss.  Meeresuntersuch. 

N.  F.  Abt.  Helgoland,  15,  1  (1922). 
v.    Buddenbrock   and    Schulz.      Zool.   Jb. 

Abt.  Zool.  Physiol.,  52,  513  (1933). 
Carpenter.      J.    co7np.    Neurol.,    18,    483 

(1908). 
Chapman.     Brit.  J.  anim.  Behav.,  2,  146 

(1954). 
Clark.    J.  exp.  Zool.,  51,  37  (1928). 
Dolley.    J.  exp.  Zool.,  20,  357  (1916). 
Dolley  and  Wierda.  J.  e.rp.  Zool.,  53,  129 

(1929). 
Fraenkel.    Z.  vergl.  Physiol.,  6,  385  (1927). 

Biol.  Rev.,  6,  36  (1931). 
Franz.      Internat.    Rev.   Hydrobiol.    {Biol. 

Suppl.),  3,  1  (1911). 
Garrey.    J.  gen.  Physiol.,  1,  101  (1918). 
Gotz.    Z.  vergl.  Physiol.,  23,  429  (1936). 
Holmes.    J.  cojnp.  Neurol.,  15,  305  (1905). 


Kennedy.     Proc.  Zool.  Soc.  Lond.,  109A, 

221  (1939). 
Klein.     Z.  wiss.  Zool,  145,  1  (1934). 
Mast.    J.  anim.  Behav.,  2,  256  (1912). 
J.  exp.  Zool.,  38,  109  (1923). 
Amer.  J.  Physiol.,  68,  262  (1924). 
Meyer.     Z.  wiss.  Zool.,  142,  254  (1932). 
Minnich.    J.  exp.  Zool.,  29,  343  (1919). 
Radl.      Utitersuchungen   iiber   den    Photo- 

tropismus  der  Tiere,  Leipzig  (1903). 
Rao.    J.  exp.  Biol.,  24,  64  (1947). 
Richard.     C.   R.  Acad.  Sci.   (Paris),  226, 

356  (1948). 
Santschi.    Rev.  suisse  Zool.,  19,  117  (1911). 
Schulz.     Z.  vergl.  Physiol.,  14,  392  (1931). 
Urban.     Z.  wiss  Zool.,  140,  299  (1932). 
Wellington.      Nature    (Lond.),    172,    1177 

(1953). 
Weyrauch. 

(1936). 

Zool.  Am.,  113,  115  (1936). 
Wigglesworth.    Parasitology,  33,  67  (1941). 
Wolf.     Z.  vergl.   Physiol.,  3,  615  (1926)  ; 

6,  221  (1927)  ;   14,  746  (1931). 


Rev.    Suisse    Zool.,    43,    455 


MENOTAXIS 

So  far  we  have  considered  orientations  either  directly,  or  relatively 
directly,  towards  or  away  from  a  source  of  light  ;  it  is  obviously  of 
greater  biological  importance  if,  in  addition,  an  animal  can  travel  at  an 

1  P.adl  (1903),  Santschi  (1911),  Wolf  (1927-31),  Fraenkel  (1927),  Schulz  (1931), 
v.  Buddi'nbrock  and  Schulz  (1933),  and  others. 

2  ir./v-ma— Meyer  (1932)  ;  Vanessa— Gotz  (1936)  ;  Los  ms— Weyrauch  (1936)  ; 
Aedes — T,  imedy  (1939)  ;  Culex,  Ano2}heles — Rao  (1947)  ;  Pediculus — Wigglesworth 
(1941). 

3  For      iZa— Klein  (1934). 


LIGHT   AND   MOVEMENT 


61 


angle  to  the  light,  thereby  putting  itself  in  the  position  of  the  pilot  of  a 
ship  who  can  steer  otherwise  than  directly  in  line  with  the  sun  or  the 
pole-star.  In  the  simpler  types  of  orientation,  light  acts  as  a  stimulus 
attracting  or  repelling  the  animal  into  a  more  favourable  environment  ; 
in  menotaxis  light  is  merely  used  as  a  means  to  an  end,  guiding  the 
animal  to  a  place  where  it  wishes  to  go  whether  favourable  or  not. 

Four  types  of  response  which  can  be  considered  as  menotactic  (the 
term  being  used  in  its  widest  sense)  require  particular  note — the  light- 
compass  reaction,  orientation  to  polarized  light,  orientation  to  a  visual 
pattern,  and  the  dorsal  (or  ventral)  light  reaction. 


Fig.  37.— 
Menotaxis. 


The  orientation  MENOTAXIS  wherein  the  receptor  organ  is  sufficiently 
Eiysia        viridis,  evolved  to  appreciate  the  direction  of  a  light  and  is  able 
with    respect    to  ^o  inhibit  other  stimuli  so  that  it  can  orientate  itself 
onentation  ^"angle  with  reference  to  it  alone, 
which   the   longi-  There  is  no  doubt  that  in  laboratory  conditions 

tudinal  axis  of  the  ,        .,,  ,iit         ,•[^•^  ri-ij. 

Mollusc       makes  and  With   controlled  artihcial  sources  ot  light  many 
with  the  direction  Arthropods  show  a  remarkably  high  degree  of  accuracy 


of 
(Fraenkel) 


'^      in  maintaining  an  orientation  angle  by  this  means  ; 


1  p.  68. 

2  V.  Buddenbrock  (1937). 

^  The  common  snail,  i^eZf.r — v.  Buddenbrock  (1919)  ;  the  Mediterranean  Gastropod, 
Eiysia— Fv&er\ke\  (1927). 

«  Pardi  and  Papi  (1953). 

=  Bartels  and  Bahzer  (1928),  Bartels  (1929),  v.  Buddenbrock  (1937). 

6  V.  Buddenbrock  (1931-37),  v.  Buddenbrock  and  Schulz  (1933). 

'  Ruppell  and  Sehein  (1941),  Lack  (1943),  Wilkinson  (1949),  Matthews  (1951-.53). 

8  The  caterpillars  of  the  gipsy  moth,  Lymantria  dispar — Ludwig  (1934)  ;  the  dung 
beetle,  Oeotrupes  sylvaticus — Honjo  (1937). 


The  LIGHT-COMPASS  REACTION,  whereby  the  animal  travels  at  a 
fixed  angle  to  a  light  (the  orientation  angle)  either  in  a  straight  or  a 
circular  direction,  was  first  described  by  Santschi  (1911)  in  his  observa- 
tions on  ants,^  and  was  so  named  by  von  Buddenbrock 
flight        (1917)  (Lichtkompassbewegung)  (Fig.  37).     It  is  a  res- 
ponse of  considerable  complexity  and  of  wide  distri- 
bution, occurring  in  some  polychfete  worms, ^  in  some 
molluscs,^    in    the    Amphipod,    Talitrus    saltator,'^    in  Web  spider 

spiders  returning  from  a  kill  in  the  centre  of  their  web,^ 
in  a  large  number  of  insects  returning  to  their  nests, ^ 
and  in  some  birds  as  a  means  of  navigation.'  In  general, 
light -compass  reactions  may  be  divided  into  two  types. 
In  the  first  (tropo-menotaxis,  Ludwig,  1934),  the 
reaction  is  essentially  simple  and  tropic  in  type,  being 
governed  primarily  by  the  intensity  of  the  light,  and 
if  two  lights  appear,  their  effects  are  summated  and  the 
animal  orientates  itself  balanced  at  an  angle  between 
them  ^  ;    but  the  more  common  reaction  is  one  of  telo- 


Oeotrupe 


62  THE   EYE   IN   EVOLUTION 

the  Amphipod,  Talitrus  saltator,  for  example,  reacts  in  this  way  to 
the  moon  (Pardi  and  Papi,  1953).  Until  recently  most  writers  agreed 
that  this  reaction  was  the  essential  factor  in  the  orientation  of  insects 
out-of-doors.  This  is  probably  the  case  when  fog  or  cirrostratus  turns 
the  sun  into  a  small  light  source,  but  the  lack  of  consistency  in  the 
behaviour  of  insects  in  natural  conditions  when  the  sun  is  bright  does 
not  substantiate  that  this  is  the  main  or  even  an  effective  mechanism, 
and  the  experiments  of  Wellington  (1955)  would  seem  to  indicate  that 
solar  heat  and  the  response  to  the  plane  of  polarization  of  light^  are  the 
essential  factors  in  determming  their  conduct  in  these  circumstances. 

The  accuracy  of  the  response  of  the  light -compass  reaction  in 
insects  is  made  possible  by  the  structure  of  the  compound  eyes,  for 


Fig.  38. — Menotaxis. 

The  insect  moves  so  that  its  course  makes  a  constant  angle  (a)  with  rays 
of  Hght  issuing  from  a  source  ;  it  therefore  approaches  the  source  along  a 
logarithmic  spiral  (after  von  Buddenbrock). 

they  orientate  themselves  in  such  a  way  that  the  sun's  rays  stimulate 
one  or  at  most  a  few  ommatidia  all  the  time.^  The  high  degree  of 
accuracy  thus  obtained  may  be  gathered  from  the  fact  that  insects 
sometimes  correct  their  angle  of  orientation  if  the  light  merely  passes 
from  one  ommatidium  to  its  neighbour  (von  Buddenbrock  and  Schulz, 
1933).  When  the  guiding  light  is  sufficiently  far  away  this  type  of 
response  is  effective  in  orientating  the  insect  in  a  straight  line,  but  if 
the  stimulus  is  close  an  entirely  different  result  is  seen.  If  the  insect 
were  to  pursue  a  straight  path,  the  incidence  of  such  a  light  on  the 
retina  would  constantly  change  ;  and  if  the  angle  of  incidence  is  to  be 
kept  constant,  the  insect  must  perforce  turn  along  a  logarithmic  spiral 
which  ends  in  the  light  itself  (Fig.  38)  (von  Buddenbrock,  1937).  Cater- 
pillars crav  ]  to  a  light  in  this  type  of  sj^iral  path  (Ludwig,  1933-34) 
and  it  is  for    liis  reason  that  the  moth,  applying  a  mechanism  adapted 

1  p.  73.  *  p.  174. 


LIGHT   AND   MOVEMENT 


63 


for  reference  to  a  distant  source  of  light,  flies  to  its  death  in  the  nearby- 
flame. 

This  behaviour  is  not  constant  in  moths.  If  a  number  of  these  insects  is 
introduced  into  a  room  where  a  candle  is  situated  on  a  table  they  will  take  up 
positions  on  the  table  around  the  light  with  their  heads  turned  towards  it. 
As  a  rule,  one  by  one  they  take  wing  ;  the  first  may  fly  arovmd  the  flame  in 
diminishing  circles  until  it  passes  through  it  to  fall  in  flames  into  the  molten 
mass  of  wax  beneath  ;  the  next  will  similarly  follow  to  commit  deliberate  suicide  ; 
and  so  on  the  procession  goes,  some  perishing  in  the  flame  itself,  others  escaping 
with  singed  wings  to  fall  on  the  table  when,  with  wings  too  charred  to  use,  they 
may  crawl  with  difficulty  up  the  candle  and  walk  straight  into  the  base  of  the 
flame  to  die.  While  most  fly  around  the  flame  in  decreasing  circles,  some  may 
fly  straight  into  it  ;  others  remain  upon  the  table  apparently  worshipping  from 
afar,  while  others  again  wander  aimlessly  about  the  room  paying  no  attention 
to  the  light.  The  cause  of  this  variation  in  conduct  is  quite  unknowTi  ;  it  seems 
to  indicate  that  the  phototactic  response  is  not  entirely  determmed  on  a  mechanis- 
tic level. 


The  navigational  sense  in  birds  is  an  astonishing  example  of  the 
accuracy  of  a  modification  of  the  light -compass  reaction.  It  has  long 
been  knowai  that  young  birds  will  undertake  their  initial  migration  from 
one  continent  to  another  unaccompanied  by  their  parents  and  arrive 
in  the  correct  habitat  with  extreme  precision,  and  that  homing  birds 
such  as  the  pigeon  or  the  gull,  released  in  an  unkno\m  area  in  random 
directions,  will  rapidly  head  straight  for  home  in  a  dh-ect  line  of  flight 
(Matthews,  1951-55  ;  Kramer  and  St.  Paul,  1952  ;  Kramer,  1953). 
The  Manx  shearwater,  Puffinns,  for  example,  transported  to  America, 
has  homed  3,050  miles  across  the  Atlantic  wastes  to  arrive  after  \2\ 
days  in  its  own  particular  burrow  on  an  island  off  the  west  coast  of 
England  (Matthews,  1953).  It  is  obvious  that  in  navigational  feats  of 
this  type  visual  orientation  is  quite  inadequate  and  a  bi-coordinate 
orientating  mechanism  of  great  accuracy  must  exist.  It  is  true  that 
many  birds  show  a  relatively  simple  positive  phototactic  response, 
flying  towards  an  illuminated  patch  or  the  lighted  end  of  a  long  dark 
tunnel — a  primitive  reaction  still  carried  out  after  ablation  of  the 
cerebral  hemispheres  (j^igeons,  Viaud  and  Marx,  1948)  ;  but  it  is 
equally  true  that  they  are  capable  of  executing  the  most  complex  type 
of  orientation. 

For  years  this  navigational  ability  of  some  birds  has  excited  the 
curiosity  of  naturalists.  Several  explanations  have  been  explored  such 
as  an  acceleration-displacement  recording  mechanism  or  an  ability  to 
exploit  the  earth's  magnetic  field,  but  they  have  all  been  discredited 
by  experiment  ^  ;  nor  do  the  structural  arrangements  apparently  exist 
in  the  eyes  of  birds  as  in  the  compound  eyes  of  insects  to  appreciate  the 

1  Gordon  (1948),  Matthews  (1951-55),  Yeagley  (1951),  van  Riper  and  Kalmbach 
(1952). 


Puffinus 


64 


THE   EYE   IN   EVOLUTION 


Homing  pigeon 


polarization  pattern  of  the  sky  (Montgomery  and  Heinemann,  1952). 
The  evidence  would  seem  incontrovertible  that  these  birds  can 
orientate  themselves  by  an  innate  ability  to  estimate  the  sun's  arc  by 
observation  of  its  movement  over  a  small  distance  and,  by  extrapola- 
tion, to  navigate  automatically  over  great  distances  with  extreme 
accuracy  even  when  flying  is  continued  during  the  night.  Flight 
throughout  the  journey  is  governed  by  a  number  of  factors  developed 
by  individual  experience  in  respect  of  which  considerable  variations 
exist,  but  the  fundamental  basis  of  the  method  of  orientation  is  an 
innate  form  of  sun-navigation  depending  on  an  appreciation  and 
memory  of  the  angle  of  incident  light  and  an  ability  to  make  appropriate 
corrections  according  to  the  24-hour  rhythm  of  a  reference  system  (an 
internal  clock)  operating  in  the  brain  (Ruppell  and  Schein,  1941  ; 
Lack,  1943  ;  Saint  Paul,  1953  ;  Matthews,  1953-55  ;  Kalmus,  1954  ; 
Pratt  and  Thouless,  1955). 

This  theory  had  its  origin  in  the  observations  of  Ising  (1945),  Varian  (1948), 
Davis  (1948)  and  Wilkinson  (1949),  but  the  most  satisfying  evidence  came 
from  the  experiments  of  Matthews  (1951-55)  on  homing  pigeons,  gulls  and 
Manx  shearwaters.  He  found  (as  have  others)  that  birds  released  in  a  strange 
or  clueless  environment  (such  as  over  the  sea)  rapidly  orientated  themselves  in 
the  correct  direction  for  home  as  they  soared  to  jfly,  and  maintained  their  direction 
over  long,  direct  flights  over  unknown  country  ;  but  they  were  able  to  find  the 
correct  direction  only  when  the  sun  was  up  and  their  initial  accuracy  in  flight 
depended  on  a  clear  sky  ;    in  cloudy  or  overcast  weather  they  were  helpless 

Figs.  39-40. — Navigation  by  Birds. 
To    illustrate    the    initial    orientation    of   the    Manx    shearwater    when 
released  in  a  strange  environment.    The  home  direction  is  vertically  upwards. 
The  length  and  breadth  of  the  rays  is  proportional  to  the  number  of  birds 
that  orientated  in  the  direction  indicated. 


Fig.  39. 


Fig.  40. 


Fig.  39. — Orientation  under  a  cloudless  sky.  It  is  seen  that  the  great 
majority  of  the  birds  orientated  themselves  initially  in  approximately  the 
right  direction. 

o"ra.  40. — Orientation  under  heavily  clouded  skies.  The  ability  to 
orieniate  correctly  has  been  lost  (G.  V.  T.  Matthews). 


LIGHT   AND   MOVEMENT 


65 


(Figs.  39  and  40).  By  keeping  the  birds  in  conditions  wherein  tlie  sun  and 
sky  were  excluded  for  a  number  of  days  before  release,  consistent  errors  were 
made  which  could  only  be  explained  on  the  supposition  that  the  birds  were 
failing  to  correct  for  the  seasonal  variation  in  the  sun's  altitude  from  which  they 
derived  their  measurement  of  latitude.  By  de-synchronizing  the  day-night 
rhythm  before  release  by  arranging  an  artificial  day  beginning  and  ending  a  few 
hours  earlier  or  later  than  normal,  errors  in  longitude  were  made  which  could 
be  explained  on  the  basis  of  a  disturbance  of  an  inherent  time-sense  based  on 


Home 
-noon  L, 

\ry- ^c^i^"®"^*  posicion 

'  ^-        2t  local  noon 


o^;:o-^^ 


•Decrease  in 
azimuths  time 


Fig.  41. — Diagram  Illustrating  the  Hypothesis  of  Sun  Navigation. 
Released  to  north  and  west  of  home.     See  text.     (Tlie  diagram  is  not  to 
scale.)     (After  G.  V.  T.  Matthews.) 


regular  light-dark  sequences  ;  they  flew  in  a  false  direction — too  far  east  after 
an  advanced  day,  too  far  west  after  a  retarded  day.  That'  the  direction  is 
determined  by  the  incident  light  was  strikingly  shown  in  Kramer's  (1952) 
experiments  with  migrating  starlings  :  when  the  light  was  deflected  by  90^  by 
mirrors,  the  birds'  flight  was  equally  deflected  and  in  the  same  direction, 

Wilkinson's  hypothesis  is  illustrated  in  Fig.  41.  Briefly,  the  sun's  arc 
is  observed  over  a  small  excursion  and  from  this  its  position  at  local  noon  and 
the  geographical  south  are  extrapolated  ;  the  latitude  is  determined  by  the 
difference  between  the  observed  noon  altitude  and  the  remembered  noon 
altitude  at  home.  The  difference  in  longitude  is  derived  joartly  by  comparison 
with  the  home  position  in  azimuth  at  local  noon  combined  with  an  estimation 
of  time  in  the  diurnal  night-day  cycle.  This,  although  it  is  not  yet  experimentally 

S.O. — VOL.  I. 


66  THE   EYE   IN   EVOLUTION 

proven,  appears  at  present  to  be  the  most  probable  explanation  of  the  observed 
facts  ;  it  may  well  seem  so  complicated  an  automatic  calculation  by  a  creature 
with  a  proverbially  small  brain  as  to  appear  fantastic  ;  but  the  ability  of  a  bird 
released  in  America  to  orientate  itself  immediately  for  its  flight  to  a  particular 
and  very  precise  locality  in  Europe  is  fantastic — it  occurs  within  40  seconds  of 
viewing  the  sun.  It  would  seem  that  on  the  basis  of  its  structural  potentialities, 
the  avian  retina  should  be  capable  of  such  a  feat.^  It  has  also  been  suggested 
(again  without  proof)  that  the  pecten  ^  may  play  some  part  in  the  analysis  by 
acting  as  a  fixed  point  when  taking  observations  (Mermer,  1938  ;  see  also 
Crozier  and  Wolf,  1943  ;    Griifin,  1952). 

ORIENTATION  TO  POLARIZED  LIGHT.  Arthropods  as  widely  different 
as  the  king-crab,  the  sand-hopper,  the  ant  and  the  honey-bee  possess 
the  abihty  to  respond  to  the  plane  of  polarization  of  light,  and  by  this 
means  may  orientate  themselves  in  skylight  out-of-doors.  This  faculty 
can  be  investigated  experimentally  by  observing  the  response  to  the 
rotation  of  the  axis  of  a  sheet  of  "  Polaroid  "  glass.  Sensitivity  of 
this  type  was  first  demonstrated  in  bees  by  von  Frisch  (1949)  and  has 
since  been  confirmed  in  behavioural  experiments  involving  a  number 
of  Arthropods,  both  larvae  and  adults,^  and  has  also  been  proved  by 
electroretinographic  responses.* 

Light  from  the  blue  sky  (not  directly  from  the  sun)  has  been  scattered  from 
particles  in  the  atmosphere  which  also  partly  polarize  it,  that  is,  more  of  the 
light-waves  vibrate  in  one  transverse  direction  than  in  others.  The  plane  of 
maximum  polarization  is  different  for  each  patch  of  blue  sky,  and  the  proportion 
of  light  polarized  also  varies,  being  greatest  at  90°  from  the  sun.  Thus  each 
patch  of  blue  sky  has  its  own  plane  and  intensity  of  polarization,  differing  from 
every  other  patch.  A  "  Polaroid  "  glass  is  a  submicroscopic  crystalline  grid  trans- 
mitting chiefly  light  vibrating  in  one  particular  direction  ;  it  can  be  used  to 
analyse  the  plane  and  intensity  of  polarization  of  light  since,  on  rotation,  light 
polarized  in  other  planes  is  cut  off. 

We  shall  see  presently  ^  that  insect  larvae  have  simple  eyes 
(stemmata)  while  adults,  in  addition  to  simple  eyes  (ocelli)  are  usually 
equipped  also  with  two  large  compound  eyes.  The  stemmata  of  the 
larvae  respond  both  to  direct  light  and  alterations  in  the  plane  of 
polarization,  while  in  adults  the  ocelli  sometimes  show  little  or  no 
phototactic  response  to  non-polarized  light,  but  aid  the  compound 
eyes  in  their  response  to  polarized  light.  In  these  cases  the  former  are 
thus  supplementary  in  function  so  that  the  intact  animal  reacts  more 
quickly  and  accurately  than  one  deprived  of  its  ocelli. 

1  p.  417.  2  p.  416. 

*  Larvtp  of  the  sawfly,  Neodiprion — Wellington  et  al.  (1951)  ;  mosquito  larva? — 
Baylor  and  Smith  (1953)  ;  adult  insects — Vowles  (1950-54),  Menzer  and  Stockhammer 
(1951),  Cartiiv  (1951),  Stephens  et  al.  (1952-53),  Wellington  (1953),  de  Vries  et  al. 
(1953)  ;  oth;  Arthropods— Waterman  (1950),  Kerz  (1950),  Pardi  and  Papi  (1952), 
Baylor  and  vSi     ,li  (1953),  and  others. 

«  Autrun.      id  Stumpf  (1950).  Waterman  (1950-51). 

s  p.  222. 


LIGHT  AND  MOVEMENT 


67 


The  interesting  experiments  of  Wellington  (1953)  will  make  the  matter 
clear.  Fig.  42  shows  the  abrupt  changes  of  direction  associated  with  rotation 
of  the  axis  of  a  sheet  of  "  Polaroid  "  held  over  larvie  crawling  over  the  ground  ; 
the  intact  animal  responds  most  markedly,  but  an  adequate  response  is  obtained 
if  either  the  ocelli  or  the  comijound  eyes  are  functioning  alone. 


SUN 


Fig.   42. — The  Effects  of  Alterations  in  the  Plane  of  Polarizai'ion 
ON  THE  Orientation  of  Insects. 

The  plane  of  polarization  was  changed  by  rotation  of  the  axis  of  a  sheet 
of  "  Polaroid  '"  held  between  the  insect  and  the  sun  as  it  crawled  over  the 
ground.  The  circles  show  the  point  at  which  tlie  sheet  of  Polaroid  was  placed 
over  the  moving  insect  or  rotated  or  withdrawn.  The  bar  inside  the  circles 
shows  the  orientation  of  the  axis  with  respect  to  the  sun,  and  the  shading  of 
the  circle  indicates  wliether  or  not  the  sky  was  appreciably  darkened  when 
viewed  through  the  "Polaroid"  with  the  axis  set  as  shown. 

A,  B,  C.  The  path  of  a  fly  :  A,  with  all  its  eyes  functioning  ;  B,  with  only 
its  compound  eyes  uncovered  ;    C,  with  only  its  ocelli  uncovered. 

D.  A  fourth-instar  larva  of  Neodiprion  (drawn  on  a  different  scale). 

The  marked  convolutions  in  the  path  of  B  show  the  response  to  alterations 
in  the  polarization  of  the  skylight  when  a  patch  of  cinus  cloud  passed  over- 
head (W.  G.  Wellington,  Nature). 


The  Orientation  of  Insects  out-of-doors 

It  would  thus  apjDear  that  the  orientation  of  insects  in  natural 
conditions  in  daylight  is  a  very  complicated  matter.  Wlien  these 
questions  first  received  attention  in  the  classical  observations  of 
Santschi  (1911)  and  Brim  (1914)  on  the  behaviour  of  the  ant.^  its 
conduct  was  interpreted  as  being  regulated  by  a  light -compass  reaction 
alone.  At  a  later  date  the  experiments  initiated  by  von  Frisch 
(1949-51)  introduced  the  complicating  factor  of  a  response  to  the  j^lane 
of  polarization  of  light.  Finally,  the  experiments  of  Wellington  and 
his  co-workers  (19.^)3-55)  have  stressed  the  importance  of  a  thermal 
response.      There    is    complete    agreement    that    the    light-compass 

1   p.  6S. 

5—2 


68 


THE   EYE   IN  EVOLUTION 


Ant 


reaction  is  the  essential  determinant  of  behaviour  in  laboratory  condi- 
tions with  artificial  light,  in  natvu^al  surroundings  at  night  and  in  cir- 
cumstances during  the  day  when  the  sun  is  largely  obscured,  but  these 
latter  workers  believe  that  on  a  clear  day  the  sun  acts  primarily  as  a 
source  of  heat.  Wellington  (1955)  concluded  that  in  full  sunlight,  insects 
in  open  places  orientate  themselves  primarily  by  solar  heat  when  it  is 
available  and  maintain  their  orientation  to  the  sun  or  their  straight -line 
travel  in  its  absence  by  polarized  light  from  the  overhead  sky  ;  if 
as  may  happen  when  smoke  or  cirrus  cloud  of  varying  densities 
passes  overhead,  the  plane  of  polarization  changes  rapidly,  the  response 
may  completely  break  down  and  the  insect  remains  stationary  even 
although  the  sun  remains  exposed  (see  Fig.  32).  This  sometimes  makes 
its  behaviour  appear  irregular  and  difficult  to  interjDret,  particularly 
in  the  neighbourhood  of  industrial  centres  where  haze  and  smoke  are 
plentiful.  Wellington  considered  that  during  overcast  weather  travel  is 
probably  also  aided  by  light  gradients  (tropo-menotaxis).  In  general, 
when  an  insect  is  cool  it  is  thermo-positive  and  travels  towards  the  sun  ; 
when  it  is  warm  it  is  thermo-negative  and  orientates  itself  away  from 
the  sun,  and  if  it  becomes  overheated  and  the  plane  of  polariza- 
tion changes  rapidly  the  insect  becomes  disorientated  and  is  incapable 
of  travelling  so  that  it  often  circles  aimlessly  until  it  succumbs  to  heat- 
stroke (W^ellington  et  al.,  1951-54  ;  Sullivan  and  Wellington,  1953  ; 
Wellington,  1955).  The  same  complex  interaction  between  thermal  and 
visual  stimuli  is  seen  in  the  locust  which  postures  at  right  angles  or 
parallel  to  the  sun's  rays  depending  on  the  temperature  (Volkonsky, 
1939).  Occasionally,  as  in  the  ant,  the  evidence  suggests  that  other 
stimuli  such  as  gravity  are  also  effective  in  orientation  in  such  a  way 
that  the  geotropic  and  phototactic  elements  are  correlated  in  a  single 
central  mechanism  of  taxis  (Vowles,  1954). 

From  the  historical  point  of  view,  the  homing  of  the  ant  provided 
the  classical  example  of  this  type  of  activity.  The  purposive  behaviour 
of  these  insects,  particularly  when  returning  to  the  nest  laden  with 


>N 


Menotaxis. 


The  ant  was  returning  to  its  nest,  N,  with  the  sun  on  its  left  side.  On 
four  consecutive  places,  1,  2,  3  and  4,  it  was  shaded  from  the  direct  light  of 
the  sun  and  the  image  from  the  sun  was  projected  from  the  animal's  right 
by  iii^ans  of  a  mirror.  On  each  occasion  the  animal  preserved  its  initial  orienta- 
tion n-lative  to  the  sun  or  its  image  by  turning  round  (Santschi). 


LIGHT   AND   MOVEMENT 

food,  in  spite  of  an  immense  load  between  their  mandibles  and  in  face 
of  all  obstacles,  has  excited  admiration  and  conjecture  for  centuries. 
Nevertheless,  although  considerable  intelligence  is  suggested,  the 
response  is  largely  automatic.  Cornetz  (1911)  observed  that  if  such  an 
insect  were  lifted  up  and  set  down  in  another  place,  it  set  off  in  the  same 
direction  as  before  whether  or  not  this  led  to  the  nest.  That  the 
directing  influence  was  the  sun  was  shown  by  Santschi  (1911)  who 
shaded  the  ant  from  the  sun  and  deflected  its  rays  by  a  mirror  so  that 
they  reached  the  insect  from  the  opposite  side  ;  each  time  this  was 
done  the  ant  immediately  changed  its  path  so  that  it  maintained  the 
same  direction  with  regard  to  the  reflected  rays  as  it  had  previously  to 


69 


5^9'pnn 


2^  39'pnn. 

Fig.   44. — Menotaxis. 


The  orientation  of  the  ant,  Lasius  niger.  The  dark  Une  indicates  the 
route  taken  by  the  ant  towards  its  nest,  N.  The  initial  part  of  its  journey 
was  orientated  at  an  angle  of  about  90^  to  the  sun.  At  X,  the  ant  was 
imprisoned  in  a  box  for  2.V  hours,  from  2.39  p.m.  to  5.9  p.m.  During  this 
time  the  sun  had  traversed  an  angle  of  37-5°.  On  its  release,  the  ant  resumed 
its  path  again  at  right  angles  to  the  late  afternoon  sun,  deviating  from  its 
former  path  by  an  angle  of  37°  (after  Brun). 


the  direct  rays  (Fig.  43).  The  same  reaction  was  demonstrated  in 
locusts  by  Kennedy  (1945-51),  who  found  that  the  direction  of  the 
marching  desert  hoppers  could  readily  be  changed  and  that  of  flying 
adults  momentarily  changed  by  reflecting  sunlight  onto  them  with  a 
mirror.  At  first  this  response  was  assumed  to  be  a  typical  examjDle  of 
the  light-compass  reaction,  but  Wellington  (1955)  broitght  forward 
evidence  that  it  was  more  probable  that  radiant  heat  associated  with 
the  reflected  light  was  the  more  effective  stimulus. 

A  still  more  elaborate  response  was  demonstrated  in  the  classical 
experiment  of  Brun  (1914)  who  confined  an  ant  in  a  box  for  some  hours 
in  the  middle  of  its  homeward  journey  to  its  nest  ;  on  releasing  the 
insect  it  set  out  on  a  new  track,  not  now  towards  its  nest  but  deviating 
from  its  original  route  by  an  angle  corresponding  to  that  through 
which  the  sun  had  moved  in  the  interval  so  that  its  rays  were  still 
received  at  the  same  angle  as  before  (Fig.  44).    Again,  this  was  initially 


70 


THE   EYE   IN   EVOLUTION 


taken  to  be  an  example  of  the  light-compass  reaction,  but  the  response 
could  be  equally  explained  by  orientation  by  the  j^attern  of  polarization 
which  also  shifts  with  the  sun  (Griffin,  1953  ;  Wellington,  1955).  The 
homing  of  the  honey-bee  when  dejirived  of  other  optical  clues  such  as 
conspicuous  landmarks^  is  determined  by  the  same  mechanism  (Wolf, 
1927  ;  von  Frisch,  1931).  Behavioural  experiments  have  demonstrated 
that  certain  insects  are  not  only  able  to  analyse  the  polarization  of 
light  but  can  retain  its  pattern  in  their  memory  to  take  account  of  the 
alteration  in  the  position  of  the  sun  with  the  time  of  day  (von  Frisch, 
1950  ;  Vowles,  1950  ;  Griffin,  1950  ;  Stephens  et  al.,  1952)  ;  by  this 
type  of  mnemotaxis  it  is  probable  that  homing  remains  accurate  for 
long  journeys  despite  the  changing  position  of  the  sun. 

It  is  not  to  be  thought,  however,  that  the  homing  of  the  ant  need  be  an 
entirely  visual  process.  Bonnet  (1779-83)  first  showed  that  odour  trails  may 
be  an  effective  aid  (Carthy,  1950  ;  Vowles,  1955),  and  the  ability  of  this  insect 
to  improve  its  path-finding  and  avoid  detours  is  exemplified  in  its  extraordinary 
capacity  to  learn  quite  complex  mazes  (Turner,  1907  ;   Schneirla,  1929-33  ;  etc.). 

It  is  interesting  that  the  "  danciyig  "  of  bees,  the  ballet  by  which 
they  communicate  to  other  foraging  bees  the  direction,  the  distance  and 
the  richness  of  a  discovery  of  nectar,  is  also  largely  determined  by  the 


J      I      '      I 


j^ 


I     1 
/      ; 


Fig.  45. — The  Dance-figures  of  Bees. 

(a)   The    round    dance    for    short    distances    performed    by    German    and 

Austrian   bees,      (b)   The   "  sickle  dance  "   for  short  distances  performed  by 

Dutch  and  Swiss  bees,     (c)  The  figure-of-eight  dance  for  long  distances,  with 

the  "  wagi.:'. '-run  "  forming  the  central  component  of  the  figure  (von  Frisch). 

1  p.  78. 


LIGHT   AND   MOVEMENT  71 

polarization  pattern  reflected  from  the  sky.  The  coordinated  dance 
which  a  returned  forager  performs  on  the  surface  of  the  comb  within 
the  hive  was  described  by  Aristotle, ^  and  in  recent  times  has  been  most 
closely  studied  by  von  rrisch,^  the  Austrian  naturalist  (1949-54), 
using  slow-motion  cinematography  and  specially  marked  bees  attracted 
to  rich  diets  placed  at  different  distances  in  different  directions  from 
the  hive.  For  distances  closer  than  10  metres  the  returned  bee  com- 
municated its  news  to  the  rest  of  the  hive  by  performing  a  simple 
circular  dance  ;  for  distances  greater  than  this  the  direction  of  the 
food  is  indicated  by  using  the  vertical  direction  on  the  surface  of  the 


"           11 

.1 

f/..    A_ 

u 

„ 

"C-:'A-    , 

, 

"  " 

v.:        A_ 

/■k 

" 

fe^  L 

/c9^^30°ny.H( . 

ii 

-    „    'St  ,, 

•1 

. 

:::a:.   ^    K 

.1 

••    -   ■■ 

;■■  A.  A. , 

a 

1 

Qrub  Z3.6.5Z 

•A--           /I 

■/^ 


'4 


VI     / 


15  ■.     "       "        .,    ^^1 


-^ 


^- 


^O^ny.W. 

V/  "  " 
/       " 


Dachau  30.6.52 


Fig.   46. — 1  he  "  Displacemp:nt  Test  "  in  the  Orientation  of  the  Bee. 

This  test  indicates  the  abihty  of  the  honey-bee  to  allow  for  a  change  in 
the  position  of  the  sun.  In  («),  marked  bees  from  a  hive,  St.,  were  allowed  to 
feed  on  the  afternoon  of  June  29th,  1952,  from  a  feeding  place,  F,  180  m. 
away  in  the  direction  30°  north  of  west.  The  following  morning  the  hive  was 
transported  to  another  entirely  unknown  landscape  of  a  completely  different 
type.  Tlie  vast  majority  of  the  bees  (15  out  of  19),  without  any  help  from 
familiar  landmarks,  went  to  one  of  4  alternative  feeding  places  180  m.  away 
from  the  hive  and  30^  north  of  west,  ignoring  other  symmetrically  placed 
feeding  places.  On  the  first  afternoon  the  sun  had  been  in  the  west  ;  on  the 
second  morning  the  sun  stood  '\\\  the  east  ;  so  that  in  order  to  retain  the  same 
orientation  the  Ijees  must  have  been  able  to  calculate  and  allow  for  the  solar 
moveinents  (von  Frisch). 

comb  (the  direction  of  gravity)  to  represent  the  direction  of  the  sun's 
rays  outside  the  hive,  the  distance  of  the  soinxe  of  food  by  the  speed  of 
the  dance,  and  the  richness  of  the  find  by  its  vigour.  The  dance  takes 
the  form  of  a  squat  figure-of-eight,  the  straight  transverse  run  of  which 
is  marked  by  the  liee  actively  waggling  its  body  with  an  enthusiasm 
depending  on  the  richness  of  the  nectar  (Fig.  45)  ;  the  direction  of  this 
run  bears  the  same  relation  to  the  vertical  as  does  the  position  of  the 

1  Hist.  An'nunL,  18,  624b.  8.     See  Haldane,  Behaviour,  6,  256  (1954). 

2  See  Fig.  728. 


72  THE   EYE   IN   EVOLUTION 

source  of  food  to  the  position  of  the  sun  at  the  time,  while  the  speed 
of  the  dance  varies  inversely  as  the  distance  (about  10  revolutions  in 
15  sees,  to  indicate  a  distance  of  100  metres,  2-5  revolutions  to  indicate 
3,000  metres).  The  indications  of  direction  attain  an  accuracy  of  3° 
in  good  conditions,  of  distance  of  up  to  100  metres.  Moreover,  unlike 
the  ant,  bees  possess  an  innate  time-keeping  mechanism  whereby  they 
can  make  compensation  for  the  movements  of  the  sun  or  changes  in  the 
pattern  of  polarization  in  the  sky  as  the  day  progresses,  making  the 
appropriate  correction  in  their  direction  (Fig.  46). 

It  is  interesting  that  there  is  no  component  in  the  dance  for  a  vertical 
distance,  presumably  because  svich  is  rarely  required  in  natural  surroundings  ; 
and  when  von  Frisch  et  al.  (1953)  fed  bees  on  a  feeding-table  perched  on  a  radio 
beacon  directly  above  the  hive,  new  foragers  were  unable  to  find  it.  As  performed 
in  the  hive  the  waggle-rvin  serves  to  indicate  the  direction  of  the  food  as  related 
to  the  sun  by  reference  to  the  vertical  as  determined  by  gravity  ;  occasionally 
the  dance  is  performed  on  the  horizontal  alighting  board  in  front  of  the  hive 
and  in  this  case  the  waggle-run  points  to  the  actual  direction  of  the  feeding  place 
without  reference  to  the  sun.  Moreover,  in  different  localities  different  "  dialects  " 
are  used.  Thus,  while  von  Frisch  (1950)  found  that  Avistrian  and  German  bees 
dance  in  a  circle  to  indicate  food  near  at  hand  without  giving  any  indication 
of  its  direction,  Tschumi  (1950)  and  Baltzer  (1952)  found  that  Swiss  bees,  and 
Hein  (1950)  that  Dutch  bees  perform  a  "sickle  dance",  dancing  in  a  semi-circle 
the  axis  of  which  denotes  the  appropriate  direction  to  be  followed  exactly  in  the 
same  way  as  the  straight  part  of  the  figure-of-eight  dance  indicates  this  for  far 
distances  (Fig.  45b). 

This  extremely  complex  and  highly  ritualized  pattern  of  behaviour 
is  an  astonishing  performance,  particularly  when  it  is  recalled  that  the 
brain  of  the  bee  is  about  one-tenth  of  an  inch  in  diameter  ;  it  is 
apparently  inborn  and  instinctive,  but  its  precise  implications  have  to 
be  learnt  through  experience  by  the  young  workers  (Lindauer,  1952). 
The  response  is  disorientated  in  shadow,  resumes  its  rhythm  as  soon 
as  a  patch  of  blue  sky  becomes  visible,  and  can  be  artificially  changed 
-  by  the  interposition  of  a  polarizing  film  between  the  insects  and  the 
sun.  Moreover,  when  trained  bees  are  transported  from  the  northern 
to  the  southern  hemisphere  where  the  direction  of  the  sun's  movement 
to  an  observer  is  anti-clockwise  instead  of  clockwise,  their  foraging 
movements  tend  to  be  reversed  (Kalmus,  1956).  A  somewhat  similar 
or  even  more  complicated  "  language  "  is  used  by  scout  bees  to  indicate 
the  position  or  direction  for  a  suitable  new  home  or  swarm. 

It  is  clear,  therefore,  that  the  orientation  of  insects  out-of-doors,  although 
determined  by  automatic  responses,  is  an  extremely  complex  affair  influenced 
by  many  stimuli  acting  sometimes  singly,  sometimes  in  combination  ;  and  it 
is  equally  clear  that  much  work  will  require  to  be  done  before  their  behaviour  is 
fully  elucidated, 

Aqnafir  ■  rfhrojwds  also  make  use  of  polarized  light  to  orientate 
themselves  \^    ile  swimming,  in  some  cases  reacting  to  the  polarized 


LIGHT   AND   MOVEMENT 


73 


light  of  the  sky,  as  do  Amphipods  when  seeking  their  return  to  the  sea 
(Pardi  and  Papi,  1952-53),  or  making  use  of  the  polarization  patterns 
which  exist  between  the  air-water  interface  (Waterman,  1954).  Such 
reactions  have  been  demonstrated  in  12  species  of  Cladocera,  water- 
mites  and  caddis-fly  larvae,  which  tend  to  swim  so  that  their  direction 
of  movement  is  at  right  angles  to  the  plane  of  polarization  (Baylor  and 
Smith,  1953).  The  crab,  Ewpagurus,  shows  a  definite  response  to  a 
change  in  the  direction  of  polarization  (Kerz,  1950)  as  also  do  mosquito 
larvae. 

The  navigation  of  the  small  crustacean,  Talitrus  saltator,  as  recorded  by 
Pardi  and  Papi  (1952-53)  is  a  fascinating  story.  These  Amphipods  normally 
live  in  the  intertidal  zone.  Transferred  inland,  they  move  towards  the  coastline 
whence  they  came,  taking  their  direction  from  the  angle  of  the  sun  ;  as  with 
insects  and  birds  their  course  can  be  deflected  by  changing  the  direction  of  the 
incident  light  by  a  mirror.  If  direct  sunlight  is  not  available  they  can  orientate 
themselves  by  polarized  light  from  patches  of  blue  sky  and  can  be  similarly 
deflected  by  the  interposition  of  a  polarizing  sheet  ;  under  a  completely  overcast 
sky  they  are  disorientated.  As  with  bees  there  is  also  an  innate  mechanism  which 
allows  them  to  compensate  for  movements  of  the  sun  throughout  the  day,  but, 
unlike  the  reactions  of  the  bee,  it  would  seem  that  the  whole  mechanism  is 
established  by  heredity  or  acquired  in  early  youth  and  is  set  in  each  individual 
for  ever  and  cannot  be  changed.  Thus  specimens  on  the  west  coast  of  Italy  move 
westwards  towards  the  sea,  and  even  when  brought  to  the  seaside  of  the  east 
coast  will  automatically  attempt  to  travel  westward  right  across  country  away 
from  the  nearby  water.  The  most  extraordinary  thing  about  these  creatures  is 
that  travelling  through  the  night  they  appear  to  be  able  to  navigate  with 
reference  to  the  moon.  This  is  the  only  instance  where  this  has  been  established 
and  in  view  of  the  complication  and  rapid  change  of  the  lunar  path  across  the 
sky,  it  would  seem  to  be  an  extraordinary  feat. 

ORIENTATION  TO  A  VISUAL  PATTERN  SO  that  its  reception  on  the 
retina  remains  constant  corresponds  closely  in  its  mechanism  to 
orientation  with  respect  to  a  source  of  light.  Thus  insects  placed  on  a 
turn-table  facing  a  window  will  move  round  when  the  table  rotates 
(Radl.  1902)  and  if  a  striped  drum  is  rotated  in  front  of  them  they  will 
endeavour  to  keejD  in  line  with  a  given  stripe  (an  "  optomotor  response'") 
(Schlieper,  1927  ;  Schulz.  1931  ;  Zeiser.  1934)i.  Gregariousness  in 
locusts  depends  on  the  same  reaction  ;  moving  so  that  it  nullifies  the 
movement  of  images  across  its  retina,  each  swarming  insect  travels 
precisely  with  its  neighbour  ("  gregarian  inertia  "),  the  whole  host 
being  guided  by  a  light-compass  reaction  to  the  incidence  of  the  sun's 
rays  (Kennedy,  1939-45).  Orientation  when  swimming  against  a 
current  of  water  ("  rheotaxis  ")  is  in  fact  a  visual  response  of  the  same 
type  :  the  water-boatman,  Notonecta,  for  example,  turns  upstream  and 
swims  with  sufficient  strength  to  maintain  a  constant  impression  of 
the  nearby  bank  ;  if  the  landmarks  on  the  bank  are  moved,  the  water- 

1  This  reaction  has  been  used  to  measure  the  visual  acuity  of  insects,  see  p.  588. 


Eupagurus 


Talitrus  saltator 


Locust 


Xotonecta 


74 


THE   EYE    IN   EVOLUTION 


Gyrinid  beetle 


Daphnia 


boatman  moves  with  them,  and  if  they  are  obliterated  as  when  swim- 
ming in  the  dark  or  between  plain  white  boards,  the  insect  allows  itself 
to  be  carried  j^assively  downstream  (Schulz,  1931).  Gyrinid  beetles  are 
similarly  disorientated  when  swimming  in  the  dark  or  if  a  sndden 
change  is  made  in  the  landmarks  on  the  banks  (Brown  and  Hatch, 
1929). 

THE  DORSAL  (ventral)  LIGHT  REACTION.  The  Orientation  of 
animals  which  progress  on  the  earth's  surface  can  be  treated  as  if 
movement  on  one  plane  only  need  be  considered  ;  but  those  that  swim 
or  fly  have  three  available  planes  of  movement — they  can  turn  as  do 
land  animals  on  a  vertical  axis,  but  they  can  also  roll  on  a  longitudinal 
axis  or  they  can  pitch,  turning  somersaults  about  a  transverse  axis 
(Fig.  48).  They  must  therefore  possess  a  complex  means  of  orientation 
to  maintain  the  body  in  a  desired  position  as  it  travels  towards  a  goal. 
Because  of  its  relatively  greater  specific  gravity  the  stability  of  an 
animal  body  in  air  is  greater  than  in  water,  and  since  the  attachments  of 
wings  are  comparatively  high  making  the  centre  of  gravity  relatively 
low,  the  equilibrium  of  balance  in  birds  raises  no  serious  difficulties. 
This  does  not  apply  with  the  same  force  to  insects  although  some,  such 
as  the  dragon-fly,  Anax,  demonstrate  a  dorsal  light  response  during 
flight,  the  effective  organ  being  mainly  the  compound  eye  (Mittelstaedt, 
1950)  ;  but  aquatic  animals  require  to  perform  constant  and  active 
balancing  movements  to  maintain  their  normal  orientation.  Many 
fishes  maintain  their  position  optically  by  keeping  one  surface  (usually 
the  dorsal)  perpendicular  to  the  light,  using  their  eyes  as  receptor 
organs  ;  others  have  evolved  a  specific  statocyst  organ  to  maintain 
equilibrium,  but  although  this  development  has  assumed  the  greater 
importance  eventually,  the  eyes  still  participate  in  the  orientating 
reflexes,  a  collaboration  between  the  senses  which  survives  in  the 
elaborate  reflex  connections  which  continue  to  yoke  the  visual  with  the 
vestibular  system  in  Man. 

The  dorsal  light  reaction  was  initially  recognized  in  the  crustacean, 
Da])hnia,  by  Radl  (1901),  and  its  wide  distribution  was  first  appreciated 
by  von  Buddenbrock  (1914-37)  ;  it  has  since  been  observed  in  many 
groups  of  aquatic  animals  of  a  wide  variety.^  In  its  essentials  the 
DORSAL  LIGHT  REACTION  eusures  that  when  the  light  is  above,  the 
animal  swims  with  the  dorsal  surface  upwards,  maintaining  itself 
symmetrically  to  it  and  moving  (if  it  does  move)  in  a  plane  at  right 


1  In  Medusaj — Fraenkel  (1931)  ;  polychaete  worms — Fraenkel  (1931),  v.  Budden- 
brock (1937)  ;  in  a  large  number  of  Crustaceans — v.  Buddenbrock  (1914),  Alverdes 
(1926-30).  Schulz  (1928),  Seifert  (1930-32)  ;  among  Insects  in  nymphs  and  larvje— 
V.  Buddf  Ml)rock  (1915),  Wojtusiak  (1929)  ;  in  the  dragon-fly,  Anax,  during  flight — ■ 
Mittelsta.  t  (1949)  ;  perhaps  in  the  desert  locust,  Schistocerca  gregaria — Rainey  and 
Ashall  (1!     '.)  ;   and  particularly  in  Fishes — v.  Hoist  (1935). 


LIGHT   AND   MOVEMENT 

angles  to  it  ;  if  the  light  is  placed  horizontally  the  animal  rotates 
correspondingly,  and  if  the  light  is  placed  below,  it  either  rolls  or 
somersaults  over  to  swim  belly-upwards  (Fig.  47).  In  the  ventral 
LIGHT  REACTION  an  animal  which  normally  swims  belly-upwards 
behaves  analogously  (Fig.  48).  Occasionally,  however,  if  the  normal 
direction  of  the  incidence  of  the  light  is  changed,  the  animal  does  not 


Fig.  47. — The  Dorsal  Lkjht  Reaction. 


On  the  left  half  of  the  aquarium  the  Crustacean,  Apiis,  is  illuminated 
from  its  right  side;  on  the  right  half  of  the  aquarium,  from  its  left  side.  As 
it  swims  between  the  two,  it  orientates  itself  by  rolling  on  its  longitudinal 
axis  (after  Seifert). 


® 


^"■"^^.^^^J 


Fig.  48. — The  Ventral  Li(;ht  Keaction. 
The  change  of  orientation  in  the  Crustacean,  Artemia  salitia,  when  the 
light   is  changed  from  abo\p  to  below.     Fig.   48«,  by  a  rolling  movement  ; 
Fig.  4S6,  by  a  back  somersault   or  pitching  movement    (in   a   photo-positive 
individual)  (after  Seifert). 

act  reflexly  but  becomes  completely  disorientated  and  swims  aimlessly, 
a  reaction  seen,  for  example,  in  the  nemertine  worm,  Linens  ruber,  which 
in  normal  circumstances  is  negatively  phototactic  (GoutcharofF,  1952). 
The  visual  mechanism  involved  varies  in  different  species.  In 
some  larvae  the  response  is  mediated  by  the  dermal  light  sense  and 
persists  after  total  blinding  (Schone,  1951)  but  as  a  rule  the  eyes  are 


Linens  ruber 


76 


THE   EYE   IN   EVOLUTION 


A  pus 


implicated.  The  water-flea,  Daphnia,  orientates  itself  in  the  typical 
manner  by  means  of  a  single  dorsal  median  eye  ;  while  the  fresh-water 
crustacean,  Apus,  has  two  compound  eyes  and  a  median  eye  on  the 
dorsal  surface.  Other  crustaceans  have  two  eyes  ;  when  one  is 
removed  or  painted  over,  rolling  and  circling  movements  occur  towards 
the  seeing  side,  and  if  both  are  thrown  out  of  action  the  light  reaction 
disappears  (the  brine-shrimp,  Artemia,  Seifert,  1930-32). 

The  relation  between  the  statocyst  and  the  eyes  in  those  animals 
which  possess  the  dual  mechanism  was  prettily  shown  by  von  Hoist 


(a) 


(h) 


\       \ 


\        t 


t       t 


Fig.  49. — The  Dor.sal  Light  Reaction. 

In  the  fish,  Crenilahrus  rostratus. 

Upper  two  fish.  The  Hght  comes  from  above  ;  (a)  in  the  intact  animal, 
(b)  in  the  labyrinthectomized  animal.     Orientation  is  normal. 

Lower  two  fish.  The  light  comes  from  below  ;  (a)  the  norinal  posture 
is  retained  owing  to  the  influence  of  the  labyrinth  ;  (b)  the  labyrinthec- 
tomized animal  swims  in  an  upside-down  posture  (after  von  Hoist). 

(1935)  in  the  fish,  Crenilahrus  rostratus.  Normally  the  balance  is 
maintained  essentially  by  the  static  reactions  of  the  labyrinth  which 
are  supplemented  by  the  light  reaction.  If,  however,  a  light  is  placed 
horizontally,  a  compromise  orientation  is  assumed  with  the  body 
slightly  tilted  towards  the  light,  the  inclination  varying  directly  with 
the  strength  of  the  illumination  ;  when  the  light  is  placed  underneath, 
the  static  reactions  control  the  animal  and  the  light  is  without  effect 
(Fig.  49).  When,  however,  the  labyrinths  are  put  out  of  action,  the 
optical  reaction  functions  in  the  pure  form,  the  movements  of  the 
trunk,  the  fins  and  the  tail,  hitherto  controlled  by  the  labyrinth,  now 
being  entirely  coordinated  by  the  eyes  so  that  with  a  transverse  light 
the  fish  swims  on  its  side ;  with  a  light  below,  upside-down ;  finally, 
when  one  eye  is  put  out  of  action,  the  fish  rolls  towards  the  seeing  side 
for  a  time  until  an  adaptive  reaction  asserts  itself. 

This  reaction,  of  course,  is  often  combined  with  other  types  of  phototaxLs. 
Thus  the  water-flea,  Daphnia,  is  usually  positively  tropotactic  and  also  exhibits 
a  compa'is  reaction  (von  Frisch  and  Kupelwieser,  1913  ;  Eckert,  1938),  the 
brine-shrimp,  Artemia,  may  be  positively  or  negatively  phototactic,  and  so  on. 


LIGHT   AND   MOVEMENT 


77 


Alverdes.    Z.  vergl.  Physiol.,  4,  699  (1926). 
Z.  iciss.  ZooL,  132,  135  (1928)  ;   137  403 

(1930). 
Antrum  and  Stiimpf.     Z.  Naturforccli.,  5b, 

116  (1950). 
Baltzer.     Arch.  Julius  Klaus-Stift.    Verer- 

bungsforsch.,  27,  197  (1952). 
Bartels.     Z.  vergl.  Physiol.,  10,  527  (1929). 
Bartels  and  Baltzer.     Rev.  Suisse  ZooL,  35, 

247  (1928). 
Baylor  and   Smith.      Ainer.   Nat.,   87,   97 

(1953). 
Bonnet.        Observations     sur     des     pet  its 

fourmis.     Oeuvres  Hist.   nat.   Philos., 

Neuchatel.  1  (1779-83). 
Brown  and  Hatch.     J.  cotirp.  Psychol.,  9, 

159  (1929). 
Brun.   Die  liauniorientierang  d.  Anuneisen, 

Jena  (1914). 
von   Buddenbrock.      Zool.  Jb.,   Abt.   allg. 

Zool.    Physiol.,  34,   479    (1914)  ;     37, 

313  (1919). 
S.  B.  Heidelberg.  Akad.  wiss.  Math.-Xat. 

KL.  6B,  1  (1915)  ;   8B,  1  (1917). 
Z.  vergl.  Physiol.,  15,  597  (1931). 
Grundriss   der   vergl.   Phi/sinl.,  Berlin,  1 

(1937). 
von  Buddenbrock  and  Scliulz.     Zool.  Jb., 

Abt.     allg.     Zool.     Physiol.,    52,     513 

(1933). 
Carthy.     Nature  (Lond.),  166,  154  (1950). 

Behaviour,  3,  275  (1951). 
Cornetz.    Rev.  Suisse  Zool.,  19,  153  (1911). 
Crozier  and  Wolf.     J.  gen.   Physiol.,  27, 

287,  315  (1943). 
Davis.    J.  appl.  Pht/sioL,  19,  307  (1948). 
Eckert.     Z.  vergl.  Physiol.,  25,  655  (1938). 
Fraenkel.       Z.     vergl.     Physiol.,    6,     385 

(1927). 
Biol.  Rev.,  6,  36  (1931). 
von  Friseh.     Aus  deni  Leben   der  Bienen, 

Berlin,  2nd  ed.  (1931). 
Experientia,    5,     142     (1949)  ;      6,     210 

(1950). 
Bees,  their  ]'ision.  Chemical  Senses  and 

Language,  Ithaca  (1950). 
Naturwissenschaften,  38,  105  (1951). 
von    Friscli,    Heran    and    Lindauer.       Z. 

vergl.  Physiol.,  35,  219  (1953). 
von  Friseh  and  Kvipelwieser.     Biol.  Zbl., 

33,  517  (1913). 
von  Friseh  and  Lindauer.     Naturwissen- 
schaften, M,  245  (1954). 
Gordon.    Science,  108,  710  (1948). 
(Joutcharoff.    C.  R.  Acad.  Sci.  (Paris),  235, 

1690  (1952). 
Griffin.     Biol.  Bull.,  99,  326  (1950). 
Biol.  Rev.,  27,  359  (1952). 
Amer.  Sci.,  41,  209  (1953). 
Hein.     Experientia,  6,  142  (1950). 
von  Hoist.     Biol.  Rcc.  10,  234  (1935). 

Pubbl.  Staz.  zool.  Xapoli,  15,  143  (1935). 
Honjo.    Zool.  Jb.,  Abt.  allg.  Zool.  Physiol., 

57,  375  (1937). 
Ising.     Ark-,  mat.  uslr.  Fys.,  32,  1  (1945). 


Kalmus.    Nature  (Lond.),  173,  657  (1954). 

J.  exp.  Biol.,  33,  554  (1956). 
Kennedy.         Trans,      roi/.      entcm.     Sac, 
Lone/.,  89,  385(1939)  ;  95,247  (1945). 
Philos.  Trans.  B,  235,  163  (1951). 
Kerz.     Experientia,  6,  427  (1950). 
Kramer.     The  Ibis,  94,  265  (1952). 

J.  Ornith.,  Leipzig,  94,  194,  201  (1953). 
Kramer  and  St.  Paul.     Z.  Tierpsychol.,  7, 
620  (1951). 
Verh.  dtsch.  zool.  Ges.,  1951  (1952). 
Lack.     Brit.  Birds,  37,  122,  143  (1943). 
Lindauer.       Z.    vergl.     Physiol.,    34,    299 

(1952). 
Ludwig.     Z.  wiss.  Zool.,  144,  469  (1933)  ; 

146,  193  (1934). 
Mattliews.      J.    Inst.    Navigation,    4,    260 
(1951). 
J.  exp.  Biol..  28,  508  (1951)  ;    30,  243, 

268,  370  (1953)  ;    32,  39  (1955). 
r/(e/6i:s,  94,  243(1952)  ;  96,432(1954). 
Behaviour,  4,  202  (1952). 
Trans.  ophthcd.Soc.  U.K..  74,  67  (1954). 
Bird  Navigation,  Camb.  (1955). 
Menner.    Zool.  Jb.,  Abt.  allg.  Zool.  Physiol., 

58,  481  (1938). 
Menzer  and  Stockhammer.    Naturwissen- 
schaften, 38,  190  (1951). 
Mittelstaedt.    Naturwissenschaften,  36,  90 
(1949). 
Z.  vergl.  Physiol.,  32,  422  (1950). 
Montgomery    and    Heinemann.      Science, 

116,  454  (1952). 
Pardi  and  Papi.    Naturwisse)ischaften,  39, 
262  (1952). 
Z.  vergl.  Physiol.,  35,  459,  490  (1953). 
Pratt  and  Thouless.    J.  exp.  Biol..  32,  140 

(1955). 
Radl.     Biol.  Zbl.,  21,  75  (1901)  ;    22,  728 

(1902). 
Rainey  and  Ashall.     Brit.  J.  anim.  Behav., 

1,  136  (1953). 
van  Riper  and  Kalmbach.     Science,  115, 

577  (1952). 
Ruppell    and    Schein.       Vogelzug,    12,    49 

(1941). 
St.  Paul.     Behaviour,  6,  1  (1953). 
Sant.schi.    Rev.  Suisse  Zool.,  19,  117  (1911). 
Schiieper.       Z.    vergl.     Physiol.,    6,    453, 

(1927). 
Schneirla.      C'omp.    Psychol.    Monogr.,    6, 
No.  30  (1929). 
J.  comp.  Psychol.,  15,  243,  367  (1933). 
Z.  vergl.  Physiol.,  19,  439  (1933). 
Schone,     Z.  vergl.  Physiol.,  33,  63  (1951). 
Schulz.     Z.  vergl.  Physiol.,  7,  488  (1928)  ; 

14,  392  (1931). 
Seifert.     Z.  vergl.  Physiol.,  11,  386  (1930)  ; 

16,  111  (1932). 
Stephens,  Fingerman  and  Brown.     Anat. 
Rec,  113,  559  (1952). 
Ann.  entom.  Soc.  Amer.,  46,  757  (1953). 
Sullivan  and  Wellington.     Canad.  Entom., 

85,  297  (1953). 
Tsclmmi.      Scliweiz.    Bienoi-Zeitung,    129 
(1950). 


78                                       THE   EYE    IN  EVOLUTION 

Turner.    J.  comp.  Neurol.  Psychol. ,11,  Ml  Wellington.      Nature    (Lond.),    172,    1177 

(1907).  (1953). 

Biol.  Bull.,  13,  333  (1907).  Ann.  entom.  Soc.  Amer.,  48,  67  (1955). 

Varian.    J.  apjd.  Physiol.,  19,  306  (1948).  Wellington,  Sullivan  and  Green.     Canad. 

Viaud  and  Marx.    C.  R.  Soc.  Biol.  (Paris),  j.  ZooL,  29,  339  (1951). 

142,249,251,254(1948).  Wellington,  Sullivan  and  Henson.   Canad. 

Volkonsky.      Arch.    Inst.    Pasteur   Alger.,  Entom.    86    529(1954). 

^T      }^'  ^\i  [^^^^\-  Wilkinson.  '  Proc.  Linn.  Soc.  Lond.,  160, 

Vowles.     Nature  (Lond.),  165,  282  (19o0).  q.  MQ^Q^ 

J.  ea;«.  BioZ.,  31,  341,  356  (1954).  ...   •/       ,          d   „      •,       ,     ^     ^ 

Brit.  J.  anim.  Behav.,  3,  1  (1955).  ^^  °JVI''%''-o    f,"^^  o^    -ui^^L  ^  "''''"' 

de  Vries,  Spoor  and  Jielof.     Physica,  19,  ,,,  J^"^^'  ^''{-^'Jr^^^^^JT^l'.n.n. 

419(1953).  ^^°lf-     -Z.  I'er^^-  -P/'y«'o^-,  6,  221  (1927). 

Waterman,    ^c/ence,  111,  252  (1950)  ;  120,  Yeagley.    J.  a^pyjL  P/;ys;oZ.,  22,  746  (1951). 

927  (1954).  Zeiser.    Zool.  Jb.,  Abt.  allg.  Zool.  Physiol., 

Trans.  N.Y.  Acad.  Sci.,  14,  11  (1951).  53,  501  (1934). 


MNEMOTAXIS 

MNEMOTAXis  is  the  most  complicated  method  of  orientation  and 
allows  the  animal  to  deal  ivith  all  the  elements  of  a  coynplex  situation  in 
the  light  of  experience  gained  in  the  past  (Kiihn,  1919-39).  In  the 
previous  reactions  we  have  studied,  the  response  is  made  to  one 
stimuhis  only  or  the  synthesis  of  several,  and  it  may  be  either  direct 
as  in  tropotaxis  or  indirect  as  in  menotaxis,  a  simple  mechanism  which 
becomes  effective  by  the  inhibition  of  all  stimuli  but  the  dominant  one. 
These  more  primitive  taxes  determine  the  reactions  of  lower  species, 
and  although  they  enter  into  the  total  response  of  the  higher  animals 
and  can  be  studied  separately  in  experimental  conditions,  the  normal 
activities  of  the  latter  are  rarely  based  on  so  simple  a  pattern  of 
behaviour.  It  is  true  that  the  homing  honey-bee  can  orientate  itself 
with  regard  to  the  sun  and  that  this  is  the  only  mechanism  available  to 
the  soaring  bird  as  it  rises  in  strange  surroundings,  but  both  also  make 
use  of  other  clues  in  ordinary  life  as  soon  as  they  can  appreciate  objects 
in  a  known  environment.  In  this  more  elaborate  type  of  orientation 
two  new  capacities  are  added  to  one  or  other  of  the  simpler  methods — 
(1)  the  ability  to  integrate  a  number  of  stimuli  simultaneously  instead 
of  inhibiting  all  but  one,  and  (2)  the  modification  of  a  direct  automatic 
response  by  the  factor  of  memory  through  a  process  of  conditioning. 
By  a  synthesis  of  these  factors  the  animal  is  thus  able  to  deal  with  a 
complex  situation  as  a  whole  (Adlerz,  1903-9  ;  v.  Buttel-Reepen, 
1907  ;  Turner,  1908  ;  Rabaud,  1924-26  ;  Wolf,  1926-27  ;  Hertz, 
1929-31  ;  Friedlander,  1931  ;  Tinbergen,  1932-51  ;  Tinbergen  and 
Kruyt,  1938  ;   Baerends,  1941  ;   and  others). 

In  its  simplest  form  this  is  illustrated  by  the  experimients  of  van  Beusekom 
(1948)  with  the  homing  digger  wasp,  Philanthus  (Fig.  50).  The  initial  training 
situation  to  which  the  wasp  was  conditioned  was  a  square  block  set  at  right 
angles  close  to  the  nest  and  a  model  of  a  tree  1  metre  from  the  nest.  In  the 
test  experiment  the  block  was  turned  through  45"  and  the  tree  displaced  first 
to  one  side  and  tlien  the  other  ;   the  wasp  approached  the  corner  opposite  to  that 


LIGHT   AND   MOVEMENT 


79 


in  which  the  tree  was  located  as  if  up  to  the  last  moment  she  used  both  the 
tree  and  the  block  as  landmarks. 

The  prettj^  experiment  of  Tinbergen  and  Kruyt  (1938)  shows  the  astonishing 
rapidity  and  precision  with  which  the  wasp  learns  to  relate  its  nest  to  neighbouring 
landmarks  and  to  appreciate  a  situation  as  a  whole.  A  ring  of  20  pine-cones 
was  placed  around  the  nest  while  she  was  inside  ;  on  leaving  she  made  a  study 
of  the  locality  for  6  seconds  only  (Fig.  51)  ;  the  pine-cones  were  then  arranged 
similarly  one  foot  away  from  the  nest  ;  returning  after  90  minutes  with  a 
captured  bee,  she  alighted  in  the  middle  of  the  ring  of  cones,  a  choice  repeated 


T 

6 


--a- 


Fig.  50. — The  Path  of  the  Digger  Wasp,  PHiLAyrHcs  TRiAyocLcn. 

On  the  left,  the  training  situation.  The  path  of  tlie  wasp  ^starting  from 
the  circle)  is  directly  to  its  nest  at  the  angle  of  the  block  past  the  tree. 

On  the  right,  the  test  situation.  The  block  is  rotated  througli  4.5^  and 
tlie  tree  moved  tirst  to  A  and  then  to  B.  The  wasp  alights  alternately  at 
a  and  b  (simplified  from  van  Beusekom). 


13  times,  and  only  found  the  nest  after  the  original  situation  had  been  restored 
(Fig.  52).  A  still  more  extraordinary  ability  is  seen  in  the  wasp,  Ammophila, 
which  hunts  caterpillars  too  heavy  to  be  brought  back  on  the  wing  ;  as  it 
laboriously  drags  its  prey  to  the  nest  it  is  apparently  able,  apart  from  occasional 
exploratory  flights,  to  utilize  the  memories  of  aerial  observation,  probably 
aided  by  light-compass  orientation  (Thorpe,  1943-56). 

Behaviour  of  this  type  is  obviously  determined  by  the  iitiHzation 
of  a  number  of  stimuH  and  experiment  has  sho^\^l  that  in  making  its 
decision  the  insect  does  not  condition  itself  to  every  available  landmark 
but  exercises  some  degree  of  choice  on  principles  which  would  differ 
from  that  of  a  human  being.  Moreover,  the  stimuli  need  not  be 
simultaneous  for  visual  memories  may  be  retained  for  some  considerable 
time  ;  thus  the  bumble-bee,  Bombus,  will  fly  regularly  round  a  number 
of  fixed  landmarks  in  the  same  sequence  for  weeks  on  end  (Frank, 
19-11).  Such  studies  are  of  unusual  interest  but  our  knowledge  of  the 
problems  they  raise  is  yet  very  imperfect  ;  indeed,  experiment  has  just 


Bombus 


80 


THE   EYE   IN   EVOLUTION 

Figs.  51  and  52. — The  Reactions  of  the  Digger  Wasp. 


Fig.  51. — The  wasp,  Philanthus  triangulum,  on  leaving  the  nest  in  the  centre 
of  the  ring  of  pine  cones,  makes  a  locaUty-study  lasting  6  seconds  and 
then  leaves. 


Nest ' 


■^^     ^     k. 


Fig.  52. — The  ring  of  pine  cones  is  then  displaced  from  the  nest  and  on  her 
return  the  wasp  alights  in  the  centre  of  the  ring  and  will  only  find  the 
nest  after  the  original  situation  has  been  restored  (Tinbergen,  Study  of 
Instinct;  Clarendon  Press). 

begun  to  elucidate  the  more  complex  aspects  of  animal  psychology  in 
which  the  basic  instinctive  reactions  are  modified  by  experience  of 
the  past. 


Adlerz.    K.Sveriska  Vetensk.  Akad.  Handl., 
37,   No.    5,    1    (1903)  ;    42,   No.    1,    1 
(1906). 
Entom.  TidsJ-r.,ZO,  163  (1909). 

Baerends.       T.    Entom.    (Amst.),    84,    68 
(1941). 

van  Beusekom.     Behaviour,  1,  195  (1948). 


von   Buttel-Reepen.     Naturwiss.    Wschr., 

22,  465  (1907). 
Frank.     Z.  vergl.  Physiol.,  28,  467  (1941). 
Friedlander.      Z.  vergl.   Physiol.,  15,   193 

(1931). 
Hertz.     Z.  vergl.  Physiol.,  8,  693  (1929)  ; 

11,  107  (1930)  ;   14,  629  (1931). 


LIGHT   AND  MOVEMENT  81 

Kiihn.       Die    Orientierung    der    Tiere    in  Tinbergen.      Z.    vergl.    Physiol.,    16,    305 
i?aum,  Jena  (1919).  (1932). 

Grundriss  d.  allg.  Zool.,  Leipzig  (1939).  The  Study  of  Instinct,  Oxon  (1951). 

Rabaud.     Feuill.  Nat.,  1,  1  (I92i).  Tinbergen  and  Kruvt.     Z.  vergl.  Physiol., 

Bull.  Biol.  Fr.  Belg.,  60,  319  (1926).  25,  292  (1938). 

Thorpe.     Brit.  J.  Psychol.,  ii,  220  ;    34,  Turner.     Biol.  Bull.,  15,  2-il  {1908). 

20,  66  (1943-44).  Wolf.     Z.  vergl.   Physiol.,  3,  615  (1926)  ; 
Learning     and     Instinct     in     Animals,  6,  221  (1927). 

London  (1956).  J.  soc.  Psychol.,  1,  300  (1930). 


so.— VOL.  I 


CHAPTER   IV 
THE  EFFECT  OF  LIGHT  ON  PIGMENTATION 

The  dramatic  effects  of  light  on  the  pigments  of  plants  and 
animals  have  long  been  recognized.  The  yellowish-white  pallor 
assumed  by  plants  containing  chlorophyll  confined  in  darkness  is  well 
known,  while  the  diatoms  of  the  Lakes  of  Anvergne,  equipped  with 
green  chlorophyll  and  brown  diatomin,  change  colour  according  to  the 
depth  of  the  water  in  which  they  find  themselves  (Heribaud,  1894)  ; 
but  the  most  dramatic  effects  are  evident  in  the  integumentary 
pigments  of  2^oikilochromic  ^  animals.  The  spectacular  and  rapid 
changes  in  colour  between  black  and  green  seen  in  the  chameleon  were 
noted  in  the  fourth  century  B.C.  by  Aristotle,  while  Pliny  described 
somewhat  similar  changes  in  the  dying  mullet.  Since  classical  times  a 
considerable  amount  of  observation  and  research  has  been  devoted  to 
the  subject  and  a  surprisingly  wide  range  of  colour  changes  has  been 
recorded  in  a  large  variety  of  animals — a  euglenoid  Protozoon, 
polycheete  worms,  leeches,  Echinoderms,  Cephalopods,  Crustaceans, 
Insects,  and  among  Vertebrates,  numerous  Fishes,  Amphibians  and 
Reptiles. 2 

Biologically  these  changes  may  be  assumed  to  serve  two  purposes, 
one  the  antithesis  of  the  other — cryptic  or  protective  and  'phayieric  or 
demonstrative.  The  protective  function  is  the  more  fundamental  and 
the  more  common,  the  demonstrative  is  a  later  and  more  rare 
acquisition.^ 

The  PROTECTIVE  FUNCTION  is  designed  in  general  to  allow  the 
animal  to  adapt  itself  to  its  environment  and  shows  three  main 
modifications.  In  its  most  primitive  form  such  a  variation  in  jsigment 
probably  developed  as  a  light -absorptive  function  to  provide  protection 
against  deleterious  light  and  heat  ;  occasionally  pigmentary  variations 
are  apparently  thermo-regulatory — an  early  attempt  at  thermostasis — 
as  is  seen  strikingly  in  some  desert  lizards  in  which  colour  changes 
may  be  induced  experimentally  by  changes  in  temperature  alone 
(Parker,  1906-38  ;  Bauer,  1914  ;  Kriiger  and  Kern,  1924  ;  -and  others). 
The  most  common  and  dramatic  colour  variations,  however,  have 
evolved  as  an  adaptive  phenome7ion  allowing  the  animal  to  become  as 

1  TToiKi'Aof,  varied  ;    xpuiyi'^,  colour. 

2  For  extensive  reviews  see  van  Rynberk  (1906),  Fuehs  (1914),  Hogben  (1924), 
Parker  (1930-5r.)  and  Brown  (1950). 

^  These  are  r  xamples  of  a  large  group  of  phenomena  termed  allcesihetic  by  Huxley 
(1938)  which  exer!  their  biological  effect  through  the  agency  of  the  distance  receptors 
of  another  individual — sight,  hearing  or  smell. 

82 


LIGHT  AND   PIGMENTATION 


83 


inconspicuous  as  possible  and  obliterate  itself  in  its  environment  ; 
and,  as  we  shall  see,  this  faculty  of  mimicey  or  homochromatism  is 
sometimes  carried  to  almost  unbelievable  lengths,  particularly  among 
teleostean  fishes,  the  animal  not  only  changing  its  general  appearance 
in  light  and  shade  but  assuming  the  pattern  of  colour — blue,  red, 
yellow,  green,  black — of  its  surroundings  (Fig.  53). 


Fig 


-The  Eukopkan  Plaice 


LEV ROy  EVTES    PLA  2'Et<SA  . 


Lying  in  shallow  water  on  the  hed  of  the  sea,  to  harmonize  with  wliieh 
it  is  able  to  change  its  colovir  within  wide  limits.  The  camouflage  in  tlie 
figure  is  obvious  (photograph  by  Douglas  P.  Wilson). 


Occasionally  the  opposite  type  of  beliaviour  is  apparent  and  instead  of 
changing  its  coat  to  suit  its  environment,  the  animal  alters  its  surroundings  to 
sviit  its  own  coloration  :  tlius  the  sihery  young  of  the  Malayan  sj^ider,  Cyclosa 
insulana,  normally  rests  on  a  silvery  silk  platform,  but  as  the  animal  becomes 
older  and  brown  in  coloiu',  it  covers  the  platform  with  brown  debris  (Bristowe, 
1941).  In  other  cases  a  suitable  environment  is  deliberately  chosen  ;  thus  the 
desert  lark.  Aynmomanea,  will  settle  with  great  reluctance  on  a  terrain  not  of  its 
own  colouring  such  as  black  lava,  red  earth,  or  light  sand  (Meinertzhagen,  1940), 
just  as  bark-like  moths  will  adopt  postures  that  make  their  disrupted  wing-design 
conform  with  the  configuration  of  the  background  (Cott.  1940).  In  still  other 
cases  an  artificial  camouflage  is  assumed,  such  as  the  beetles  or  dressing-crabs 
which  drape  themselves  throughout  life  with  a  clothing  of  leaf -fragments,  sticks 
or  weeds  suitable  to  each  successi^^e  en\'ironment,  or  the  geometrid  lar\-a  of 
Borneo  which  similarly  adorns  itself  with  flower-buds  (Shelford,  1902). 

DEMONSTRATIVE  COLOTR  CHANGES,  although  less  conuuon,  may 
also  be  striking  plienomena.     These  changes  in  colour  whereby  the 


84 


THE   EYE   IN   EVOLUTION 


Latrodectus 


Betta 


Ch  laniydosa  ur'us 


Boinbinaior 

in  warning 

attitude 


animal  strives  to  make  itself  as  conspicuous  as  possible,  may  be 
directed  towards  several  ends.  In  the  first  place  they  may  serve  the 
essential  biological  purpose  of  reproduction  whereby,  simulating  the 
sexual  riot  of  the  flowers,  colour  displays,  sometimes  of  extraordinary 
vividness,  are  associated  with  courtship  and  mating  behaviour,  a 
phenomenon  seen  in  marked  degree  in  certain  cephalopods  and  fishes 
(Hadley,  1929  ;  Parker  and  Brower,  1935)  ;  it  is  a  function  analogous 
to  the  conspicuousness  of  many  male  birds  adopted  possibly  for  display 
and  distraction  in  contrast  to  the  cryptic  inconspicuousness  of  the 
brooding  female.  It  is  interesting  that  such  sexual  dimorphism  is 
rarely  seen  in  birds  which  feel  secure,  either  because  of  their  fighting 
ability  or  in  their  colonial  habits,  the  latter  finding  safety  in  a  flock 
(Mottram,  1915).  In  the  second  place  they  may  be  designed  for 
aggression,  wherein,  as  if  in  defiance  of  all  creation,  the  animal  when 
sufficiently  moved  to  excitement  assumes  the  most  blatant  hues 
possible  (as  in  squids,  cuttle-fish,  teleostean  fishes,  spiders  and  lizards  : 
Kleinholz,  1938  ;  and  others).  Less  commonly  they  may  have  a  more 
social  purpose,  serving  as  signals  of  warning  or  recognition  between 
members  of  the  same  species  or  as  feeding-releasers  between  parent 
and  offspring  (see  Marshall,  1936  ;  Huxley,  1914-38  ;  Cott,  1940-54  ; 
Armstrong,  1947  ;   and  others). 


Thus  when  facing  an  enemy  the  venomous  Australasian  spider,  Latrodectus, 
turns  a  fiery  red,  and  the  cornered  green  chameleon  an  inky  black,  opening 
widely  at  the  same  time  its  brightly  coloured  movith.  Nowhere,  however,  in 
the  whole  animal  kingdom  are  displays  so  lavish  and  theatrical  provided  as 
among  teleostean  fishes  in  their  wild  ecstasies  of  love  or  fighting  ;  none  so 
exquisite  as  the  elaborately  graceful  love-dance  of  the  male  European  stickleback, 
Gasterosteus  aculeatus,  when  his  incandescent  blue-green  back  and  transparent 
red  sides  glow  like  neon  lighting  ;  none  so  awesome  as  the  life-and  death  war- 
dance  of  the  ordinarily  brownish-grey  male  Siamese  fighting-fish,  Betta  pugnax, 
as  his  widespread  fins  light  up  in  a  luminous  multi-coloured  glory  of  burning 
passion  which  for  centuries  has  whetted  the  gambling  instincts  of  the  Siamese  as 
did  cock-fights  the  English.  In  these  cases  the  stimulus  is  purely  visual  for  the 
stickleback  will  fight  its  own  image  in  a  mirror  with  the  utmost  savagery 
(Tinbergen,  1951). 

In  other  cases  a  colour-demonstration  is  made  which,  strictly  speaking, 
does  not  involve  a  true  colour  change.  The  Australian  frilled  lizard,  Chlamydo- 
saurus,  for  example,  carries  arovind  its  neck  a  large  frill -like  fold  supported  by 
cartilaginous  rods  which  can  be  opened  like  a  huge  circular  umbrella  around 
the  head.  When  scared  the  frill  is  closed  and  the  lizard  dashes  for  safety  ;  when 
it  turns  to  face  its  enemy  the  great  greenish -yellow  frill  splashed  with  red  forms 
a  striking  and  terrifying  picture  in  contrast  to  the  saffron  yellow  of  its  open  mouth, 
before  which  the  eneiuy  visually  retires  discomfited.  Again,  the  small  European 
fire-bellied  toad,  Bombinator  igneus,  has  its  dark  under-surface  spotted  vividly 
with  yellow  or  red,  associated  with  a  poisonous  exudate  from  the  skin  ;  when 
danger  tljreatens  the  animal  throws  itself  on  its  back  or  arches  its  body  to  pro- 
claim its  unsuitability  as  food. 


LIGHT   AND   PIGMENTATION 


85 


The  mechanism  oj  the  colour  change  varies  in  diilerent  sjDecies.  In 
the  simplest  unicellular  form,  Euglena,  a  red  hsematochrome  pigment 
migrates  from  a  deeper  position  beneath  the  green  chloroj)lasts  to 
disperse  itself  superficially  under  the  influence  of  light  (Johnson. 
1939)  ;  but  the  most  common  mechanism  is  through  the  activity  of 
special  integumentary  cells  ^  called  chromatophores  (xptD/Lia.  colour  ; 
(f)6pog,  a  carrier).  Occa.sionally  the  phenomenon  is  morphoJogicaJ 
involving  a  change  in  the  number  of  functioning  chromatophores  or  an 
alteration  in  the  quantity  of  pigment  in  each.  This,  a  relatively  slow 
mechanism,  is  well  exemplified  in  the  pigmentation  that  can  be 
induced  in  the  white  belly  of  flounders  if  normal  fish  are  kept  in  a  black 
tank  or  are  blinded  and  are  illuminated  from  below  (Osborn,  1940). 
Sometimes,  as  in  certain  insect  larvae  and  spiders,  this  is  the  sole 
mechanism  of  colour-change  available  (Gabritschevsky,  1927)  ;  it  is 
usually  less  obvious  and  impressive  than  the  more  common  method 
which  is  responsible  for  the  dramatically  vivid  colour  changes  in 
poikilochromic  Crustaceans,  Fishes,  Reptiles  and  Amphibians. ^  This — 
a  functional  or  j^hysiological  change — involves  merely  a  redistribution 
of  pigment.  The  change  may  be  effected  by  a  single  pigment  which  at 
one  time  is  concentrated  into  tiny  spots  lost  in  a  pallid  background  of 
skin  so  that  it  contributes  little  to  the  colour  of  the  animal,  at  another, 
dispersed  so  that  the  animal  becomes  apj^ropriately  tinted.  Alterna- 
tively a  pigment  of  one  colour  may  stream  in  front  of  or  retire  behind 
pigments  of  other  colours  so  that  surprising  changes  of  hue  may  raj)idly 
occur.  The  two  methods,  morphological  or  ph3'siological,  are  not 
mutually  exclusive,  for  if  the  conditions  determining  the  second  are 
maintained  for  a  sufticiently  long  time,  permanent  morphological 
changes  tend  to  occur,  a  generalization  sometimes  known  as  Babak's 
law  (1913). 

Warm-blooded  animals,  on  the  other  hand,  can  only  change  their  colour 
by  the  slow  and  laborious  process  of  renewing  their  inert  feathers  or  hairs  ;  to 
this  there  are  a  few  exceptions  wherein  specific  stratagems  are  adopted,  .such  as 
the  antelope-jackrabbit  which  turns  white  in  its  flight  by  rolling  up  the  skin  of 
its  belly  on  the  side  towards  its  pursuer. 

Two  major  tyj^es  of  chromatophores  occur.  In  Molluscs  (cuttle- 
fish and  their  allies,  squid,  octojDus),  the  chromatophores  are  in  highly 
organized  groups  of  cells  in  which  the  pigment  is  redistributed  by 
neuromuscular  activity.  Each  organ  consists  of  a  central  cell  filled 
with  pigment  (red.  brown  or  yellow)  around  which  radiate  a  number  of 
muscle-fibres   which,  on  their  simultaneous  contraction,  pull  out  the 


r 


^  In  certain  transparent  Fishes  part  or  al)  of  the  colour  pattern  is  found  in  interna] 
organs  such  as  the  peritoneum  and  meninges. 

^  Crustaceans,  Keeble  and  Gamble  (1903-5)  ;  various  Vertebrates,  Babak  (1913), 
Brown  (1934)  ;   Fishes,  Odiorne  (1933)  ;   Amphibians,  Sumner  (1935). 


86 


THE   EYE   IN   EVOLUTION 


small  pigmented  cell-body  into  a  great  disc  some  twenty  times  the 
diameter  of  the  original  sphere  ;  a  nerve -fibre  supplies  each  muscular 
cell  and  the  resulting  changes  are  rapid  (Figs.  54  and  55). ^  In  all 
other  animals  the  chromatophores  are  single  cells  ;  usually  they  are 
specialized  cells  provided  with  arborizing  processes,  arranged  singly  or 
in  a  syncytium,  and  by  a  process  of  cytoplasmic  streaming  the  pigment 
may  be  concentrated  into  inconspicuous  punctate  masses  in  the  centre 
of  the  cell  or  dispersed  throughout  the  branching  structure  to  give  a 
diffuse  colour  to  the  animal  (Figs.  56  to  59).'^  In  Insects,  however,  the 
ordinary  epidermal  cells  fulfil  this  function  ;  normally  a  dark  brown- 
black  pigment  lies  beneath  an  evenly  disposed  yellow-green  pigmented 


Figs.  54  and  ."jo. — A  Chromatophore  of  the  Cephalopod. 


Fig.  54. 

Fig.  54. — The  appearance  of  the 
chromatophore  with  the  radiating 
muscular  cells  and  the  small  con- 
centrated clump  of  central  pigment. 


Fig.  55. 

Fig.  55. — The  extended  mass  of  pig- 
ment pulled  out  by  contraction  of 
the  muscle  cells  (after  Bozler). 


Hyla  arborea 


layer,  and  on  stimulation  the  former  migrates  to  the  surface  and 
disperses  itself  over  the  lighter  layer  thus  darkening  the  animal 
(Figs.  60  and  (U)  (Giersberg,  1928-30). 

The  coloration  resulting  from  the  migration  of  pigment  is  often 
assisted  by  its  new  relationship  to  static  pigment.  Under  the  chromato- 
phores of  Cephalopods  and  Crustaceans,  for  example,  there  is  an 
immobile  layer  of  light -reflecting  pigment  so  that  considerable  varia- 
tions in  colour  are  possible  depending  on  the  amount  of  light  permitted 
to  pass  to  the  deeper  tissues  (Webb  et  al.,  1952).  In  Insects,  as  we  have 
seen,  the  variegation  is  enhanced  by  the  migratory  brown  or  red 
pigment  covering  over  or  retreating  behind  the  static  green  and  yellow 
pigments.  In  Amphibians  such  as  the  tree-frog,  Hyla  arborea,  a  colour 
change  from  green  through  lemon-yellow  to  grey  is  attained  by  varia- 
tions in  the  dispersion  of  melanin  underneath  layers  of  yellow  and  white 

1  Sre  especially— Phisalix  (1894),  Hertel  (1907),  Hofmaim  (1907-10),  Frohlich 
(1910),  iiozler  (1928). 

2  Set^  especially— Spaeth  (1913),  Perkins  (1928),  Matthews  (1931),  Perkins  and 
Snook  (1932),  Brown  (1935),  and  others. 


LIGHT   AND   PIGMENTATION 


87 


Fig.    ,j(). — Three    Stages    in    the    Dispersion  of  Pigment  in  a  Mei.anophore 
OF  the   Lizard,    Taremola    (Hogbeii). 


Fic 


TO  59. 


-Pigment  Spots  in  Web  of  a  Frog  in  Different 
Conditions  (Hogljen). 


Fig.   57. — Dark  animal. 


1-^ 


^  ♦  j 


t 


A 


Fig 


5S. — Intermediate 
condition. 


Fig.   5<). — Pale  an 


cells  and  its  streaming  towards  the  surface  between  them  (Schmidt, 
1920).  A  compara))le  arrangement  may  be  seen  in  RejDtiles  ;  thns  in 
the  lizard,  Anolis,  the  animal  is  darkened  by  the  streaming  of  melanin 
in  the  processes  of  chromatophores  to  become  superficial  to  an  inert 
whitish  layer  (v.  Geldern,  1921  ;  Kleinholz,  1938)  (Figs.  62^3),  while 
the  proverbial  chameleon  changes  from  a  dark  l)rown  to  a  light  green 
depending  on  the  degree  of  dispersion  of  the  melanin  which  lies  in  front 
of  a  sheet  of  four  different  kinds  of  colour-cells. 

The  types  of  'pi<jment  also  vary,  but  the  intimate  chemical  nature 
of  many  is  unknown.  The  most  primitive  and  universal  pigment  is 
melanin  ^  of  a  dark  brown  colour  ;  the  cells  containing  it  are  usually 
monochromatic  and  are  termed  meJanophores.  A  second  type  of 
pigment — more  A'ivid  and  varied  than  the  dull  l^rown  of  melanin — is 

^   F'or  a  di-sfussion  of  the  chemical  nature  of  melanin,  see  p.  118. 


Anolis 


Chameleon 


88 


THE   EYE   IN   EVOLUTION 


Figs.    60    and    61. — The    Pigmentary    Changes     in    the     Stick-Insect, 

Dl  XI  FPUS. 

There  are  3  types  of  pigmentation  :  (A)  the  cross-hatching  indicates  a 
static  layer  of  yellow-green  pigment  underneath  the  cuticle,  (B)  the  fine  dots 
indicate  red  pigment  which  may  be  either  aggregated  into  clumps  or  dis- 
persed, and  (C)  coarse  dots  indicating  brown-black  pigment  which  migrates 
from  a  deep  site  underneath  the  nuclei  to  a  superficial  position  underneath  the 
cuticle  (after  Giersberg). 


'yn, 


^^ul>^--\^:-.i<-^^^^tmuj^ 


■' — B 


Fig.  60. — The  epidermis  in  the  light- 
adapted  stage. 


Fig.  61. — The  epidermis  in  the  dark- 
adapted  stage. 


Salmo  triitta 


comprised  of  various  fat-soluble  carotenoids  ^  contained  in  lipophores. 
In  Invertebrates  (Crustaceans,  Insects)  the  chromatophores  are 
frequently  polychromatic  since  each  may  contain  a  variety  of  these 
pigments — blue-green,  orange,  yellow  and  red — sometimes  each  with 
a  separate  distribution  within  the  cells.-  In  Vertebrates  the  chromato- 
phores are  usually  monochromatic — red  (within  erythroxthores),  yellow 
(within  xantho2)hores)  or  green  ^ — one  animal  often  having  several  types 
of  pigment  in  different  integumentary  cells  (purple  astacene  and  yellow 
lutein  in  the  brown  trout,  Salmo  trntta,  Steven,  1948).  A  third  pigmen- 
tary factor  is  found  extensively  both  in  Invertebrates  and  Vertebrates 


Figs.   62  and  63. — Colour  Changes  in  the  Lizard. 


Fig.  62. — The  deposition  of  the  melano- 
phores  in  the  brown  state  when  the 
branches  of  these  cells  extend  into 
the  stratum  germinativum. 


Fig.  63. — The  lizard  in  the  green  con- 
dition when  the  pigment  is  con- 
centrated beneath  the  static  pig- 
ment in  the  superficial  layers. 


The  stratum  corneum  has  been  displaced  from  the  section  (Kleinholz). 

1  The  carotenoid  pigments  are  of  wide  distribution  and  great  biological  interest, 
playing  a  part  as  sensitizers  to  the  phototropic  movements  of  plants,  the  phototactic 
movements  of  animals,  and  also  participating  in  visual  processes.  Their  nature  will  be 
discussed  at  a  later  stage  (p.  118). 

2  In  Crustaceans — Kiihn  and  Lederer  (1933),  Fabre  and  Lederer  (1934)  ;  in 
Insects — Schleip  (1910-15),  Giersberg  (1928). 

3  See  Fox  (1947). 


LIGHT   AND   PIGMENTATION 


89 


— guanine.  This  may  form  a  white  highly  reflecting  layer,  as  in 
Crustaceans,  or,  as  in  many  Vertebrates,  may  be  contained  in  white 
gtianophores  or  variegated  iridocytes,  the  iridescent  colour  changes  of 
which  are  due  to  the  arrangement,  form  and  movements  of  plate-like 
crystals  of  guanine — a  form  of  coloration  akin  to  that  due  to  the  diffrac- 
tion of  light  by  the  scales  offish  and  reptiles  or  the  feathers  of  birds.  The 
colour  changes  in  these  cells  are  sometimes  quite  remarkable  ;  thus  in 
the  killifish,  Fundulus,  a  single  iridocyte  may  exhibit  blue-green, 
orange,  yellow  and  red  phases  in  successive  moments. 

The  factors  causing  colour  changes  in  animals  include  extremes  of 
temperature,  humidity,  contact  stimulation,  and  psychic  stimuli, 
particularly  excitement  and  fear  ;  but  the  most  general  and  much  the 
most  important  is  light. 

Light  acts  upon  chromatophores  in  one  of  three  ways — by  a  direct, 
primary  effect  on  the  cells  themselves,  by  a  secondary  reaction  through 
the  eye,  or  by  indirect  reactions  through  receptor  mechanisms  other 
than  the  eyes  (the  central  nervous  system  and  the  pineal  body). 

A  further  response — the  endogenous  diurnal  variation  in  coloration,  largely 
controlled  by  hormones  and  nervous  centres  situated  in  the  mid-brain — we  have 
already  discussed.^ 

{a)  When  light  acts  directly  upon  the  chromatophores  themselves 
the  reaction  may  be  called  a  peimary  response.  This  is  the  most 
primitive  mechanism  and  the  only  one  available  to  unicellular  plants 
(diatoms)  or  animals  {Euglena),  but  it  is  frec|uently  retained  in  higher 
forms,  usually  as  a  generalized  darkening  in  the  shade  and  lightening 
with  illumination,  a  change,  however,  normally  obscured  by  the  more 
dominant  secondary  responses  through  the  eyes.  The  primary 
response,  however,  can  be  observed  in  young  specimens  the  chromato- 
phores of  which  have  not  yet  come  under  the  control  of  the  secondary 
mechanism,  in  blinded  animals  (Osborn,  1940),  in  denervated  regions 
after  nerve  section  and  degeneration,  and  in  isolated  fragments  of  the 
skin  when  exposed  to  illumination,  a  reaction  demonstrated  in 
crustaceans  (Keeble  and  Gamble,  1905)  and  in  some  sea-urchins 
(Kleinholz,  1938  ;   Millott,  1954-57)  (Figs.  64  to  67). 

The  direct  motor  resjionse  of  individual  ectodennal  cells  to  the  stimulus 
of  light  survives  among  the  higher  animals  in  the  movements  of  the  retinal 
rods  and  cones  -  and  in  the  contraction  of  the  pupillary  mviscles,  both  of  which 
are  ectodermal  in  origin.  In  the  iris  of  Cephalopods,  Fishes  and  Amphibia  a 
direct  contraction  to  light  commonly  occurs,^  and  although  the  primitive  response 
in  the  higher  ^Mammals  and  man  has  been  replaced  by  a  reflex  nevu'o-mechanism, 

1  p.  19.  "  p.  "31. 

3  Brown-Sequard  (1847-.59),  Budge  (1855),  Miiller  (1860),  Schur  (1868),  Steinach 
(1890-92),  Magnus  (1899),  Guth  (1901),  Marenghi  (1902),  Hertel  (1907),  Young  (1933), 
Weale  (1956),  and  others. 


Fundulus 


Diatom 


90 


THE   EYE   IN   EVOLUTION 


Figs.  64  to  67. — Pigmentary  Changes  with  Light  Intensity 
IN  A  Sea-urchin. 


Fig.  65. 


X 

■  i 

"mk 

X  / 


Fig.   66. 


Fig.   67. 


To  show  the  variation  of  pigmentation  in  a  young  specimen  of  Diadema 
antiUarum.  In  the  hght-adapted  phase  the  animal  appears  uniformly  black 
owing  to  the  dispersion  of  melanin  pigment  (Fig.  64).  In  the  dark-adapted 
phase  the  melanin  recedes  from  the  aboral  surface  leaving  beautifully  defined 
patterns  of  white  lines  and  a  ring,  an  effect  due  to  the  concentration  of 
pigment  (Fig.  65). 

In  older  specimens,  the  changes  are  less  marked  (Figs.  66  and  67) 
(N.  Millott). 


LIGHT  AND   PIGMENTATION 


91 


it   may  still   be  elicited   with  the  more  effective  stimulus  of  ultra-violet  light 
after  all  connections  with  the  central  nervous  system  have  been  severed. 

(6)  The  most  dramatic  reactions  follow  stimulation  of  the  eyes 
(SECONDARY  RESPONSES).  Hogben  and  Slome  (1931),  for  example, 
found  that  in  the  case  of  the  clawed  toad,  Xenopus.  when  the  field  of 
vision  was  occupied  by  a  light-scattering  surface  the  animal  became  pale, 
when  set  in  the  dark  background  of  a  light-absorbing  surface  the 
animal  suffered  generalized  darkening  of  the  skin,  a  response  abolished 
on  removal  of  the  eyes.  While  the  primary  responses  react  in  general 
to  the  total  intensity  of  light,  the  secondary  resjDonse  is  usually 
based  on  the  ratio  of  the  amount  of  incident  light  entering  the  eye 
directly  from  above  to  the  amount  of  reflected  light  from  the  back- 
ground, so  that  on  a  dark  background,  when  the  ratio  is  large,  the 
animal  becomes  dark  and  on  a  light  background,  when  the  ratio  is 
small,  it  becomes  pale  ;  it  is  to  be  noted  that  these  changes  occur 
without  regard  to  the  intensity  of  the  total  illumination  (Sumner, 
1911-40  ;  Sumner  and  Keys,  1929  ;  Brown,  1936  ;  Sumner  and 
Doudoroff.  1937).  This  influence  of  the  reflectance  or  albedo  of  the 
background  (to  borrow  an  astronomical  term)  has  been  fully  established 
by  experiment  ;  thus  the  effect  of  a  dark  background  can  be  faithfully 
reproduced  by  makmg  the  lower  half  of  the  cornea  opaque  ^  ;  reversal 
of  the  fish  or  of  the  illumination  or  the  background  produces  the 
expected  effect  ;  and  Butcher  (1938),  on  rotating  the  eye  of  the 
killifish,  Fu7idulus.  through  180°,  found  that  it  gave  its  tawny  response 
to  a  yellow  backgroimd  only  when  the  latter  was  above  the  animal. 

In  his  work  on  teleostean  fishes  Sumner  (1940)  established  that  the  reflect- 
ance of  the  substrate  had  an  important  effect  on  morphological  colour  changes 
also,  for  he  found  that  the  melanophore  count  and  the  total  quantity  of  melanin 
varied  inversely  as  the  logarithm  of  the  reflected  light.  The  mathematical  nature 
of  the  relationship  is  interesting  and  unexpected  ;  it  recalls  Fechner's  modifica- 
tion of  Weber's  Law  defining  the  relationship  between  the  intensity  of  stimuli 
and  their  sensory  apjDreciation,  and  suggests  that  in  assuming  control  of  these 
colour  changes  the  eye  applies  the  same  quantitative  standards  as  govern  its 
sensory  activities. 

In  addition  to  this  general  quantitative  reaction,  a  differentiated 
response  to  the  siDectral  nature  of  the  light  reflected  from  the  back- 
ground is  relatively  common  so  that  the  animal  can  assume  the  colour 
of  its  environment,  sometimes  with  remarkable  rapidity  and  accuracy. 
This  apparently  extraordinary  reaction  was  first  scientifically  described 
in  the  chameleon  prawn,  Hippolyte,  by  Keeble  and  Gamble  (1899)  and 
many  instances  have  now  received  study.  The  prawn,  Paloemon,  for 
exaniiDle,  can  manipulate  its  red,  yellow  and  blue  pigments,  so  that  with- 

1  In  the  insert.  Di.rippus — Atzler  (1930)  ;  Priebatsch  (1933)  ;  in  shrimps — 
Hanstrom  (1937-38)  ;    in  fishes — Sumner  (1940). 


Hippolyte 


92 


THE   EYE   IN   EVOLUTION 


Epinephelus 


Triturus  cristatus 


Phoxinus 


in  a  few  days  it  can  adapt  itself  to  its  habitat  by  becoming  red,  yellow 
blue,  green,  white  or  black  (Brown,  1935),  a  facility  possessed  in  some 
degree  by  several  crabs  ^  and  Cephalopods.^  Such  a  change  may  occur 
rapidly  ;  thus  the  larvse  of  butterflies  (Brecher,  1922)  and  salamanders 
(Kammerer,  1920)  when  placed  under  variously  coloured  glasses  readily 
change  their  hue  ;  and  not  only  the  tone  of  the  general  background  but 
its  colour-pattern  may  be  simulated  with  great  fidelity  by  certain 
teleostean  fishes.  The  most  remarkable  changes  of  this  type  are  seen 
in  the  groupers  (Epiriephelus)  that  swim  over  the  variegated  patterns 
of  the  coral  reefs  in  tropical  waters  and  within  a  few  minutes  may 
change  a  livery  of  bright  blues  and  browns  into  an  equally  brilliant 
costume  of  yellow  and  black  ;  a  similar  virtuosity  is  seen  in  flat-fishes 
such  as  the  fiounder,  Paralichthys  albiguttus  (Kuntz,  1916  ;  Mast, 
1916).  It  is  interesting  that  adaptation  during  the  early  stages  of 
development  may  play  an  important  part  in  determining  the  final 
pattern  of  colour  in  the  adult  ;  thus  if  the  larvae  of  the  crested  newt, 
Triturus  cristatus,  develop  on  a  dark  background  the  yellow  markings 
of  the  adult  become  suppressed,  if  on  a  light  background,  the  dark 
markings  suffer  a  similar  fate  (Lautz,  1953).  It  is  to  be  noted  that 
all  these  reactions  are  completely  dependent  on  the  eyes  and  have 
invariably  been  shown  to  be  lost  if  the  animal  is  blinded  or  even  if  it 
is  dazzled  by  a  blinding  light  which  abolishes  the  contrast  between 
the  dorsal  and  ventral  portions  of  the  retina  (octopus.  Prince,  1949). 
(c)  Occasionally  indirect  responses  may  follow  stimulation  of 
receptor  mechanisms  other  than  the  eyes — the  mid-brain  as  in  some 
fishes  {Phoxinus — Scharrer,  1928)  or  the  pineal  body  as  in  lampern 
larvae  (Young,  1935)  or  teleostean  fishes  (Breder  and  Rasquin,  1950). 


AmmoccEte  larva 
of  lamprey 


The  central  organization  of  these  pigmentary  changes  is  as  varied 
and  complex  as  the  variations  in  the  colours  themselves,  and  in  view 
of  the  multiplicity  of  the  types  of  chromatophores  and  their  reactions 
it  is  not  surprising  that  our  knowledge  of  their  control  is  by  no  means 
complete  in  spite  of  much  research.  Apart  from  local  primary 
reactions,  two  methods  of  coordination  are  found,  hormonal  and 
nervous,  the  first  the  more  primitive  and  slower  in  its  development, 
the  second  the  more  elaborate  and  efficient.  Sometimes  the  one  is 
present  alone,  as  is  seen,  on  the  one  hand,  in  the  simple  hormonal 
control  found  in  Crustaceans,  the  more  primitive  Fishes,  frogs  and 
lizards,  or,  on  the  other  hand,  in  the  simple  nervous  control  found  in 
the  leech  or  the  chameleon.  More  often  the  two  are  combined  in  a  dual 
mechanism  of  coordination,  the  hormonal  control  being  sometimes  the 
preponderatiiig  influence  as  in  Insects  or  the  eel,  but  usually  being 

1   Portunus — Abramowitz  (lOST))  ;    Planes — Hitchcock  (1941). 
■  Sepia— Kiihri  and  Heberdey  (lSt29),  Kuhn  (1950). 


LIGHT   AND   PIGMENTATION 


93 


dominated  by  the  nervous  mechanism  as  in  Gephalopods  such  as  the 
octopus  or  the  more  highly  developed  Teleosteans  such  as  the  cat- 
fish. The  hormones  {chroniatophorotropins),  of  which  there  may  be 
more  than  one  with  mutually  antagonistic  reactions,  are  elaborated  in 
Crustaceans  in  the  neuro -secretory  cells  formed  in  the  eye-stalks  and 
elsewhere  in  the  central  nervous  system  ^  ;  in  Vertebrates  the  pituitary- 
hypothalamic  complex  ^  is  the  primary  source  although  the  adrenals 
may  provide  an  antagonistic  element.  The  nerve  supply  may  be 
simple  with  one  tj^^je  of  fibre  which  is  pigment -concentrating  as  in  the 
dogfish  or  the  chameleon,  or  it  may  be  dual  comprised  of  two  opposing 
types  of  fibre,  one  resembling  adrenalin  with  a  pigment-concentrating 
(symjDathetic)  action  being  antagonized  by  a  second  resembling  acetyl- 
choline with  a  pigment-dispersing  (parasympathetic)  effect. 

Among  ANNELIDS,  such  as  some  polychsete  worms  (Hempelmann, 
1939)  and  leeches  (Wells,  1932  ;  Janzen,  1932  ;  Smith,  1942),  most  of 
which  become  pale  in  darkness  and  dark  when  illuminated,  the  evidence 
suggests  that  the  control  is  primarily  nervous,  correlated  most  effec- 
tively through  the  ocelli  at  the  anterior  end  but  operated  less  efficiently 
by  widely  distributed  photoreceptors  through  segmental  reflexes. 
Thus  if  a  leech  is  decapitated  or  stimulated  faradically,  a  pale  animal 
kept  in  darkness  will  become  pigmented,  but  if  the  nerve-cord  is 
truncated  the  change  passes  only  to  the  level  of  trans- section ;  while 
decapitated  animals  show  the  same  responses  as  normal  animals  but 
respond  more  sluggishly  (Smith,  1942).  Among  these  animals  there 
is  no  evidence  of  a  response  to  the  background. 

In  CEPHALOPODS  there  is  a  slowly  acting  hormonal  control, 
probably  mediated  by  substances  of  the  nature  of  tyramine  and 
betaine  ;  the  former  has  an  adrenalin -like  action  increasing  the  tonus 
of  motor  centres  and  producing  a  dark  coloration,  while  the  latter,  like 
acetylcholine,  decreases  the  tone  of  the  chromatophores  and  lightens  the 
animal.  The  injection  of  these  substances  produces  the  same  colour 
changes  as  also  does  the  transference  of  blood  from  a  dark  to  a  light 
animal  (Sereni,  1928-30).  This  simple  and  fundamental  chemical 
action,  however,  is  dominated  by  nervous  activity  ;  the  stimulus  is 
received  primarily  through  the  eyes,  control  being  maintained  through 
centres  in  the  cerebral  and  suboesophageal  ganglia,  the  isolation  of 
which  by  nerve  section  stops  all  colour  change  in  the  area  affected,  and 
the  response  is  effected  probably  by  a  double  innervation,  both 
excitatory  and  inhibitory,  to  the  muscles  of  the  chromatophores 
(Phisahxi  1892-94  ;    Sereni,  1927-28  ;    Bozler,  1928-29). 

Among  INSECTS  the  control  is  both  hormonal  and  nervous  and  the 
part  played  by  the  eyes  varies.  In  this  respect  the  stick-insect, 
Dixippus,  has  been  investigated  most  extensively  (Giersberg,   1928). 

'   p.  .').52.  -  p.  556. 


Leech 


]!ephalopod 
(Octopus) 


94 


THE   EYE   IN   EVOLUTION 


In  it,  the  eyes  are  the  sole  photoreceiDtors  and  their  occhision  or  section 
of  the  optic  tracts  inhibits  all  normal  responses  (Atzler,  1930)  ;  but 
the  fundamental  role  of  hormonal  control  is  seen  in  the  fact  that 
transplanted  portions  of  integument  react  normally  long  before  nervous 
connection  can  be  established  (Janda,  1936).  On  the  other  hand,  in 
the  grasshopper,  Acrida  turrita,  some  colour  changes  (adaptation  to  red, 
orange,  yellow  and  violet)  are  said  to  occur  after  the  eyes  are  totally 
varnished,  while  a  green  colour  can  be  developed  only  if  the  eyes  are 
functioning  (Ergene,  1952). 

Among  CRUSTACEANS  the  vividly  dramatic   colour  changes   are 


'•:2?* 


I'  *r'  / 


4 


-Colour  Changes  in  Crustaceans. 

The  three  shrimps  (Crago)  were  initially  coloured  alike,  as  the  specimen 
on  the  left.  This  was  used  as  a  conti'ol  and  showed  no  change  after  an  injection 
of  sea-water.  That  in  the  centre  was  injected  with  an  alcohol-insoluble  fraction 
of  the  commissures  ;  that  on  the  right  by  a  total  water-soluble  fraction  of  the 
commissures  (Brown  and  Klotz). 


Prawn 


entirely  mediated  by  hormones  elaborated  in  the  cephalic  neuro- 
secretory system. 1  That  a  blood-borne  agent  was  the  responsible 
factor  was  first  demonstrated  by  Roller  (1925-30)  who  found  that  the 
colour  of  a  lightly  coloured  shrimp,  Crago  vulgaris,  could  be  altered  by 
blood  transfusion  from  a  darkened  specimen.  Perkins  (1928-32) 
thereafter  discovered  in  the  prawn,  Pakemonefes,  that  denervation  of  a 
region  had  no  effect  on  colour  responses  while  occlusion  of  the  blood 
supply  inhibited  them  ;  he  also  demonstrated  that  injection  of  an 
extract  of  the  sinus  gland  induced  blanching  in  a  blinded  animal  while 
removal  of  the  eye-stalks  resulted  in  the  assumption  of  a  permanently 
darkened  appearance.  These  early  results  have  been  amply  confirmed 
and  it  would  appear  that  the  intricate  control  of  the  chromatophores  of 
Crustaceans  is  effected  by  at  least  two  and  sometimes  three  or  four 


^  See  further  p.  554. 


LIGHT   AND   PIGMENTATION 


95 


chromatophorotropiiis  antagonizing  and  supplementing  each  other, 
neither  species-  nor  genus -specific,  secreted  in  various  jjarts  of  the 
neuro-secretory  system  ^  (Fig.  08).  In  some  cases  the  process  is  more 
complex  and  adaptation  to  the  background  is  achieved  by  the  produc- 
tion of  different  hormones  when  the  dorsal  or  the  ventral  aspect  of  the 
retina  is  stimulated  (the  Isopod,  Ligia  oceana — Smith,  1938). 

In  CYCLOSTOMES  and  the  more  primitive  fishes  such  as  the 
SELACHIANS  -  liomiones  derived  from  the  pituitary  seem  to  be  the 
only  active  agents  in  the  control  of  the  chromatophores,  a  pigment- 


Ligia 


Sun  ^^ 


Background 


Fig.    69. — The    Controlling    Mechanism    of    the    JMelanophores    of    a 
Fish  (the  Eel,  Asouilla). 

The  direct  light  from  the  suti  strikes  the  ventral  portion  of  the  retina,  VR, 
while  the  light  reflected  from  the  background  strikes  the  dorsal  portion,  DR. 
From  the  retina  nerve  paths  lead  to  the  central  nervous  system,  CNS,  and 
thence  directly  to  the  chromatophores  by  adrenergic  nerve  fibres,  AN,  and 
cholinergic  nerve  fibres,  CN.  A  second  relay  is  made  to  the  pituitary  body. 
Pit,  from  which  hormones  are  flistributed  through  the  lilood  vessels,  BV. 
CM  is  a  chromatophore  with  its  melanin  concentrated  ;  DM  with  its  melanin 
dispersed  (after  Parker). 


dispersing  agent  (intermedin)  causing  darkening  and  a  pigment- 
concentrating  factor  causing  blanching  ;  the  colour  of  the  fish  is 
determined  by  the  ratio  of  these  two  antagonistic  substances  in  the 
blood,  this  ratio  being  in  turn  controlled  by  visual  stimuli  through  the 
differential  effects  of  dorsal  and  central  stimulation  of  the  retina 
(Zondek   and   Krohn,    1932  ;     Lundstrom   and   Bard,    1932  ;     Young, 

1  The  shrimps,  Crago  and  Pala'inon,  the  fiddler  crab  of  the  Pacific  coast  of  N. 
America,  Uca,  the  lobster,  Homarus,  etc.  (Hanstrom,  1933-35  ;  Brown  and  his  colleagues, 
1933-52  ;    Webb  et  ah.  1951). 

^  Cyclostomes,  such  as  the  lamprey,  Lampeira — Young  (1935)  ;  Selachians,  such 
as  the  skate,  liaja — Parker  (1937),  and  the  dog-fish,  Scyllium — Young  (1933). 


96 


THE   EYE   IN   EVOLUTION 


Anguilla 


1935  ;  Hogben,  1936).  In  teleostean  fishes,  however,  which  show 
more  elaborate  colour  changes  than  any  other  species,  a  dual  mechanism 
emerges  for  a  more  efficient  nervous  control  has  developed,  depending 
on  the  excitability  of  specialized  retinal  areas  above  and  below  the  level 
of  the  optic  nerve  (Hogben  and  Landgrebe,  1940)  (Fig.  69).  In  some 
types,  it  is  true,  the  hormonal  influence  remains  preponderant  ;  this  is 
seen  in  the  eel,  Anguilla  (Neill,  1940  ;  Waring,  1940),  or  in  the  minnow. 


Fig.   70. — Colour  Changes  in  the   Female  Clppy,   Ljmisr^s  kejiculatus 

On  the  left  the  noi'mal  aninial  ;  on  the  right  a  fish  after  25  /Lig.  per  ml.  of 
LSD  (D-lysergic  diethvlamide)  had  been  added  to  the  water  of  the  aquarium 
(Sancloz  J.  Med.  Sci.,  1956). 


Figs.  71  and  72. — The  Melanophores  of  the  Guppy,  Lubistux  itmicnLATL 
{SandozJ.  Med.  Sci.,  1956). 


J^^"^^*- 


.*? 


*'>".<*f«.?j 


Fig.   71. — After  adaptation  to  a  light 
environment. 


Fig.  72.— After  LSD  (25  /xg.  per  ml.) 
had  been  added  to  the  water  of  the 
aquarium. 


Mustelus 


Phoxinus  Icevis,  in  which  even  section  of  the  sjDuial  cord  fails  to  alter 
the  response  to  the  background  (Healey,  1951-54  ;  Gray,  1956).  In 
most  Teleosteans,  however,  colour  changes  are  dominated  by  a  nervous 
control  which  persists  in  hypophysectomized  animals.  That  the 
changes  in  the  chromatophores  were  determined  by  chemical  mediators 
liberated  at  the  nerve  terminals  has  been  shown  in  a  striking  series  of 
experiments  by  Parker  (1940-55),  who  studied  the  effects  of  sectioning 
the  radial  nerves  of  the  tail-fin.  The  chromatophores  of  Selachians 
possess  a  single  innervation  mediated  by  an  adrenalin-like  substance, 
selachine,  which  is  pigment -concentrating  (the  dogfishes,  Mustelus  and 


LIGHT   AND   PIGMENTATION 


97 


Squalus — Parker,  1935-36)  ;    Teleosteans  possess  a  double  innervation 

with,   in  addition,  pigment -dispersing  fibres   the  action  of  which  is 

mediated   by   acetylchoHne    (the   kilhfish,    Fundulus — Parker,    1934  ; 

the    catfish,    Ameitirus — Mills,    1932,    Parker,    1940-41  ;     and    other  Squalus 

species).      These  two  types  of  nerve  correspond  to  the  sympathetic  and 

parasympathetic   systems  of  warm-blooded  animals  since  adrenalin 

blanches  and  acetylcholine  darkens  the  eserinized  animal  (Giersberg, 

1930  ;    Smith,    1931).     Similarly,   darkening   of  certain  Teleosts  (the 

giippy,  Lebistes  reticulatus)  can  be  brought  about  by  adding  D-lysergic  Ameiurus 

acid  diethylamide  to  the  water  of  the  aciuarium  (Cerletti  and  Berde, 

1955)  (Figs.  70  to  72).       At  the  same  time,  however,  even  in  these 


Fig.   73. — The  Effect  of  the  Injection  of  Pituitrin  on  a  Frog. 
The   right   animal   injected  six   hours  previously   witli   pituitary   extract 
from  a  fietal  ox  ;    left,  control  (Hogben). 


fishes  some  hormonal  influence  remains  since  pituitary  extracts  are 
slowly  efi:ective  in  denervated  areas  (Matthews,  1933  ;  Kleinholz. 
1935  ;    Abramowitz.  1937). 

AMPHIBIANS  were  the  first  class  of  animals  in  which  a  humoral 
control  of  colour  was  demonstrated,  when  P.  E.  Smith  (1916)  showed 
that  hypophysectomized  tadpoles  remain  indefinitely  pale.  Although 
there  is  some  evidence  of  a  mmor  nervous  influence  in  some  species 
such  as  the  darkening  of  the  leg  of  the  toad,  Bufo  arenarwn,  on  section 
of  the  sciatic  nerve  and  its  blanching  on  peripheral  stimulation  of  the 
cut  nerve  (Stoppani,  1942).  it  may  be  said  in  general  that  amphibian 
chromatophores  are  essentially  under  humoral  control.  This  is  main- 
tained by  two  antagonistic  hormones  elaborated  in  the  pituitary- 
hypothalamic  system — a  melanin-concentrating   W-snbstance  causing 


Bufo 


S.O. — VOL.  I. 


98 


THE   EYE   IN  EVOLUTION 


Rana 


Xenopus 


Anal  is 


Phrynosoma 


blanching,  mediated  by  the  pars  tuberahs,  and  a  melanin-dispersing 
B-stibstance  (intermedin)  mediated  by  the  posterior  or  intermediate 
lobe  ;  their  relative  concentration  in  the  blood  is  determined  by 
environmental  stimuli  operating  through  the  eyes  and  their  activity  is 
usually  abolished  when  these  or  the  optic  nerves  are  destroyed,  although 
some  residual  responses  remain  after  removal  of  both  eyes  which  may 
be  due  to  the  direct  action  of  light  on  the  hypothalamic  region 
(Rowlands,  1952-54).  These  conclusions  have  been  confirmed  by  the 
effects  of  excision  of  the  whole  or  parts  of  the  pituitary  and  by  the 
induction  of  colour  changes  by  the  injection  of  extracts  of  the  gland 
both  in  the  frog,  Raiia}  and  in  the  African  clawed  toad,  Xenopus 
Icevis  -  (Fig.  73).  It  is  also  interesting  that  injection  of  pineal  extract 
produces  a  contraction  of  the  melanophores  of  Xenopus  (Bors  and 
Ralston,  1951)  while  pigmentary  changes  are  constantly  produced  in 
tadpoles  by  feeding  on  pineal  tissue  (McCord  and  Allen,  1917). 

REPTILES,  like  Aniijhibians,  show  less  elaborate  responses  to  light 
than  teleostean  Fishes  ;  the  only  conspicuous  changes  occur  among 
lizards  and  the  only  active  cells  are  the  melanophores  which  send  up 
pigment  into  their  branches  entwined  among  the  variegated  chromato- 
phores,  thus  varying  the  colour  scheme  ;  the  gaiety  of  their  various 
costumes  is  due  to  individual  variation  in  these  static  cells.  The  only 
phdtic  response  is  to  light  entering  the  eye,  and  the  colour  of  the 
background  is  without  primary  significance.  Within  these  limitations, 
however,  the  large  family  of  lizards  shows  every  possible  variation 
in  control.  On  the  one  hand,  the  iguanid,  Anolis  (the  "  Florida 
chameleon  "),  shows  little  evidence  of  nervous  intervention  ;  it 
becomes  dark  brown  in  bright  illumination,  pale  green  in  darkness  ;  a 
hypophysectomized  or  a  blinded  animal  becomes  light  green  and 
thereafter  loses  all  colour  responses  except  a  peculiar  mottling  on 
electrical  stimulation  or  on  the  injection  of  adrenalin  ;  while  denervated 
areas  of  the  skin  respond  as  do  normal  areas  (Kleinholz,  1938)  (Figs.  62 
and  63).  An  intermediate  position  is  occupied  by  such  iguanids  as  the 
American  horned  "toad,"  Phrynosoma.  The  chromatophores  of  this 
animal  are  under  the  influence  of  pigment-concentrating  nerve  fibres 
and  react  to  adrenalin  ;  stimulation  or  section  of  these  fibres  results 
respectively  in  blanching  or  abolition  of  responses.  At  the  same  time 
the  injection  of  pituitrin  or  of  the  blood  of  a  darkened  specimen  induces 
darkening,  while  hypophysectomy  or  the  injection  of  adrenalin, 
adrenal  extract  or  of  blood  from  a  pale  animal  induces  blanching 
(Redfield,  1918  ;  Parker,  1938).  It  would  seem  that  the  two  antago- 
nistic hormones  act  directly  on  the  chromatophores  since  they  are 


1  Hogben  and  Winton   (1922-23),   Steggerda  and   Soderwall    (1939),   Parker  and 
Scatterty'(1937). 

2  Hogben  and  Slome  (1931-36),  Atwell  and  Holley  (1936). 


LIGHT   AND   PIGMENTATION 


99 


equally  effective  in  areas  denervated  by  nerve  section.  On  the  other 
hand,  in  the  chameleon  the  chromatophores  show  no  evidence  of 
hormonal  control  and  appear,  apart  from  the  primary  response 
characteristic  of  this  animal,  to  be  influenced  solely  by  one  set  of 
pigment-concentrating  nerves  ;  denervation  results  in  darkening, 
possibly  due  to  the  absence  of  tonic  impulses,  whereafter  there  is  a 
complete  absence  of  further  responses  (Hogben  and  Mirvish,  1928  ; 
Zoond  and  Eyre,  1934  ;   Sand,  1935). 

Abramowitz.      Proc.    nat.   Acad.  Sci.,   21, 

677  (1935). 
Biol.  Bull.,  73,  134  (1937). 
Armstrong.     Bird  Display  and  Behaviour, 

London  (1947). 
At  well  and  Hollev.     J.  c.vp.  ZooL,  73,  :^3 

(1936). 
Atzler.     Z.  vergl.  Physiol.,  13,  oU5  (1930). 
Babak.     Pflitgers  Arch.  ges.  Physiol.,  149, 

462  (1913). 
Bauer.     Z.  allg.  Physiol.,  16,  191  (1914). 
Bors  and  Ralston.     Proc.  Sac.  exp.  Biol. 

Med.,  77,  807  (1951). 
Bozler.     Z.  vergl.  Physiol.,  7,  379  (1928)  ; 

8,  371  (1929). 
Brecher.     Arch.  EntuMech.  Org.,  50,   41 

(1922). 
BrederandRasquin.6'fience,lll,  10(1950). 
Bristowe.     The  Comity  of  Spiders,  London 

(1941). 
Brown.      Proc.    nat.    Acad.   i>ci.,    19,    32/ 

( 1933). 
Biol.  Bull.,  67,  365  (1934)  ;  70,  8  (1936). 
J.  Morph.,  57,  317  (1935). 
Physiol.  ZooL,  13,  343  (1940). 
Comparative  A  n  imal  Physiology,  Loiidon, 

677  (1950). 
The  Action  of  Hormones  in  Plants  and 

Invertebrates,  l^i.Y.,  171  (1952). 
Brown,  Ederstrom  and  Seudaniore.    Anat. 

Rec,  75,  Suppl.,  129  (1939). 
Brown  and  Klotz.     Proc.  Soc.  e.vp.   Biol. 

J/ecZ.,  64,  310  (1947). 
Brown  and  Sandeen.     Physiol.  ZooL,  21, 

361  (1948). 
Brown,  Sandeen  and  Webb.     Anat.  Rec, 

111,  569  (1951). 
Brown    and    Scudamore.      J.    cell,    coinp. 

Physiol.,  15,  103  (1940). 
Brown  and  Wulff.    J.  cell.  comp.  Physiol.. 

18,  339  (1941). 
Brown-Sequard.    C.  R.  Acad.  Sci.  (Paris), 

25,  482,  508  (1847). 
J.  Physiol.  (Paris),  2,  281,  451  (1859). 
Budge.     Bewegungen  d.  Iris  (1855). 
Butcher.    J.  exp.  ZooL,  79,  275  (1938). 
Cerletti  and  Berde.    Experientia,  11,  312 

(1955). 
Cott.      Adaptive    Coloration    in    Animals, 

London  (1940). 
Alkesthetic    Selection    and    Evolutionary 

Aspects,  in  Huxley,  Hardy  and  Ford's 

Evolution  as  a  Process,  London  (1954). 


Ergene.      Z.     vergl.      Physiol.,     34,      159 

(1952). 
Fabre  and  Lederer.     Bull.  Soc.  Chim.  biol. 

(Paris),  16,  105  (1934). 
Fox.     Ann.  Rev.  Biochem.,  16,  443  (1947). 
Frohlich.     Z.  allg.  Physiol.,  11,  269,  316, 

351  (1910). 
Fuchs.    Winterstein's  Handb.  vergl.  Phy- 

sicl.,Jena,  3  (1),  1189  (1914). 
Gabritschevsky.     J.   exp.    Zocl.,   47,    251 

(1927). 
von  Geldern.     Proc.  Calif.  Acad.  Sci.,  10, 

77  (1921). 
Giersberg.       Z.     vergl.     Physiol.,     7,     657 

(1928) ;      9,     523     (1929) ;      13,     258 

(1930). 
Gray.     Xature  (Lond.),  177,  91  (1956). 
Gross.     Pfiugers  Arch.  ges.  Physiol.,  112, 

302  (1906). 
Guth.     Pflilgers  Arch.  ges.  Physiol.,  85,  119 

(1901). 
Hadley.     Bull.  Mus.  comp.  ZooL  Harvard, 

69,  108  (1929). 
HanstrOm.    ZooL  Jb.,  Abt.  Anat.,  56,  387 

(1933). 
Proc.  nat.  Acad.  Sci.,  21,  584  (1935). 
Kungl.  Svenska   Vetensk.  Akad.  HandL, 

16,  1  (1937). 
Kungl.    Fysiogr.   Sdllsk.    HandL,   49,    3 

(1938). 
Healey.    J.  exp.  Biol.,  28,  298  (1951)  ;   31, 

473  (1954). 
Hempelmann.      Z.   iviss.    ZooL,   152,    353 

(1939). 
Heribaud.     C.  R.  Acad.  Sci.  (Paris),  118, 

82  (1894). 
Hertel.    v.  Graefes  Arch.  OphthaL,  65,  106 

(1907). 
Z.  allg.  Physiol.,  6,  44  (1907). 
Hitchcock.     Biol.  Bull.,  80,  26  (1941). 
Hofmann.    Arch.    mikr.    Anat.,    70,    361 

(1907).     . 
Pflitgers  Arch.   ges.   Physiol.,   118,    375 

(1^7)  ;    132,  43  (1910). 
Hogferen.     The  Pigmentary  Effector  System, 

Edin.  (1924). 
Proc.  roy.  Soc.  B,  120,  142  (1936). 
Hogben  and  Landgrebe.     Proc.  roy.  Soc. 

B,  128,  317  (1940). 
Hogben  and  Mirvish.     Brit.  J.  exp.  Biol., 

5,  295  (1928). 
Hogben   and   Slome.      Proc.    roy.  Soc.    B, 

108,  10  (1931)  ;    120,  158  (1936). 


100 


THE   EYE   IN   EVOLUTION 


Hogben  and  Winton.      Proc.  roy.  Soc.  B, 

93,    318  ;     94,    151    (1922)  ;     95,    15 

(1923). 
Huxley.      Proc.   zool.  Soc.    Lond.,  2,   491 

(1914). 
J.  Linn.  Soc.  (Zool.),  35,  253  (1922). 
Proc.    VIII  Int.   Ornith.  Cong.,  Oxon., 

430-55,  1934  (1938). 
Janda.     Zool.  Anz.,  115,  177  (1936). 
Janzen.     Z.  Morph.  Oekol.  Tiere,  24,  327 

(1932). 
Zool.  Anz.,  101,  35  (1932). 
Johnson.     Trans.  Amer.  micr.  Soc,  58,  42 

(1939). 
Kammerer.      Nafurivissenschaften,    8,    28 

(1920). 
Keeble  and  Gamble.     Proc.  roy.  Soc.  B, 

65,  461  (1899)  ;    71,  69  (1902). 
Philos.  Trans.  B,  196,  295  (1904);   198, 

1  (1905). 
Kleinholz.     Biol.  Bull.,  69,  379  (1935). 
J.  exp.  Biol.,  15,  474,  492  (1938). 
Pubbl.Siaz.  zool.  Napoli,  17,  53  (1938). 
Keller.      Verh.   dtsch.   zool.   Ges.,   30,    128 

(1925). 
Z.  vergl.  Physiol.,  5,  191  (1927)  ;    8,  601 

(1928)  ;   12,  632  (1930). 
Kriiger    and    Kern.      Pfliigers   Arch.    ges. 

Physiol.,  202,  119  (1924). 
Kuhn,  A.  Z.  vergl.  Physiol.,  32,  573  (1950). 
Kiihn,    A.,    and    Heberdey.     Zool.    Anz., 

Suppl.  4,  231  (1929). 
Kiihn,  R.,  and  Lederer.    Ber.  dtsch.  chem. 

Ges.,  66,  488  (1933). 
Kuntz.      Bull.    U.S.    Bur.    Fish.,    35,    1 

(1916). 
Lautz.    J.  Genet.,  51,  502  (1953). 
Lundstrom  and  Bard.     Biol.  Bull.,  62,  1 

(1932). 
McCord  and  Allen.    J.  e.rp.  Zool.,  23,  207 

(1917). 
Magnus.     Z.  Biol,  38,  567  (1899). 
Marenghi.    Arch.  itcd.  Biol.,  37,  274  (1902). 
Marshall.     Philos.     Trans.    B,    226,    423 

(1936). 
Ma.st.      Bull.    U.S.    Bur.    Fish.,    34,    173 

(1916). 
Matthews.    J.  exp.  Zool.,  58,  471  (1931). 

Biol.  Bull.,  64,  315  (1933). 
Meinertzhagen.      The    Ibis,    4,    106,    187 

(1940). 
Millott.  Philos.   Tra«s.  ii,  238,  187  (1954). 

E7ideavour,  16,  19  (1957). 
Mills.    J.  exp.  Zool.,  64,  231  (1932). 
Mottram.     Proc.   zool.  Soc.    London,    663 

(1915). 
Miiller.      Verh.  jihys.-med.  Ges.   Wurzburg, 

10,  p.  L  (1860). 
Neill.    J.  exp.  Biol.,  17,  74  (1940). 
Odiorne.      Proc.   nat.  Acad.  Sci.,  19,  329 

(1933). 
Osborn.      Pruc.   nat.   Acad.  Sci.,   26,    155 

(1940). 
Parker.    J.  exjK  Zool.,  3,  401  (1906)  ;    89, 

451  (1942), 
Biol.  Rev.,  5,  59  (1930). 


Proc.   nat.  Acad.  Sci.,  17,    594    (1931), 

20,  306  (1934). 
Biol.  Bull.,  68,  1  (1935)  ;   71,  255  (1936). 
Proc.  Amer.  philos.  Soc,  77,  223  (1937)  ; 

83,  379  (1940)  ;    85,  18  (1941). 
J.  exp.  Biol.,  15,  48  (1938). 
Quart.   Rev.   Biol.,  18,  205   (1943)  ;   30, 

105  (1955). 
Animal  Colour  Changes  and  their  Neuro- 

humors,  Cambridge  (1948). 
Parker   and    Brower.      Biol.    Bull.,   68,    4 

(1935). 
Parker    and    Scatterty.      J.    cell.    co?np. 

Physiol.,  9,  297  (1937). 
Perkins.    J.  e.rp.  Zool.,  50,  71  (1928). 
Perkins  and  Snook.    J.  exp.  Zool.,  61,  115 

(1932). 
Phisalix.       Arch.     Physiol,     norm.    path. 

(Paris),    4,    209,    445    (1892)  ;     6,   92 

(1894). 
Priebatsch.      Z.    vergl.    Physiol.,    19,    453 

(1933). 
Prince.      Visual    Development,    Edin.,    1, 

(1949). 
Redfield.    J.  exp.  Zool.,  26,  275  (1918). 
Rowlands.    J.  exp.  Biol.,  29,  127  (1952)  ; 

31,  151  (1954). 
van   Rynberk.      Ergebn.    Physiol.,   2,    347 

(1906). 
Sand.     Biol.  Rev.,  10,  361  (1935). 
Scharrer.     Z.  vergl.  Physiol.,  7,  1  (1928). 
Schleip.    Zool.Jb.,  Abt.  allg.  Zool.  Physiol., 

30,  45  (1910)  ;    35,  225  (1915). 
Schmidt.       Arch.    mikr.    Anat.,    93,    414 

(1920). 
Schur.     Z.  roi.  Med.,  31,  373  (1868). 
Sereni.     Boll.  Soc.  ital.  Biol,  sper.,  2,  377 

(1927)  ;   3,  707  (1928)  ;   4,  749  (1929). 
Z.  vergl.  Physiol.,  8,  488  (1928)  ;  12,  329 

(1930). 
Biol.  Bull.,  59,  247  (1930). 
Shelford.     Proc.  zool.  Soc   Lond.,  2,  230 

(1902). 
Smith,  D.  C.    J.  exp.  Zool.,  58,  423  (1931). 
Smith,  H.  G.     Proc.  roy.  Soc.  B,  125,  250 

(1938). 
Smith,  P.  E.    Anat.  Rec,  11,  57  (1916). 
Smith,    R.    I.      Physiol.    Zool.,    15,    410 

(1942). 
Spaeth.    Ajiat.  Anz.,  44,  520  (1913). 
Steggerda  and  Soderwall.     J.  cell.  comp. 

Physiol.,  13,  31  (1939). 
Steinach.     Pfliigers  Arch.  ges.  Physiol.,  47, 

289  (1890)  ;    52,  495  (1892). 
Steven.    J.  exp.  Biol.,  25,  369  (1948). 
Stoppani.     Endocririology,  30,  782  (1942). 
Sunmer.  J.  e.rp.  Zool.,  10,  409  (1911). 
^mer.Aro^,69,245(1935);  73,219(1936). 
Biol.  Rev.,  15,  351  (1940). 
Sumner  and  Doudoroff.     Proc.  nat.  Acad. 

Sci.,ZZ,  211  (1937). 
Sumner  and  Keys.     Physiol.  Zool.,  2,  495 

(1929). 
Tuibergen.     Wilson  Bull.,  60,  6  (1948). 
The  Study  of  Instinct,  Oxon.  (1951). 


LIGHT    AND   PIGMENTATION 


101 


Tschirkowski.  Xeurol.  Vestri.,  11  (4)  (1904).      Wells.    Nature  (LoncL).  129,  686  (1932). 


Arch.  Augenheilk.,  55,  119  (1906) 
Waring.       Proc.    roy.    Soc.    B,    128,    343 

(1940). 
Weale.    J.  Physiol.,  132,  257  (1956). 
Webb,    Brown.     Fingerman    and    Hines. 

Anat.  Rec,  111,  569  (1951). 
Webb,  Brown  and  Graves.      Biol.   Bull., 

103,  310  (1952). 


Young.    Proc.  roy.  Soc.  B,  112,  228  (1933). 
Quart.  J.  micr.  Sci.,  75,  571  (1933). 
J.  e.vp.  Biol.,  12,  254  (1935). 
Zondek  and  Krohn.    Klin.  W.ichr.,  11,  405 

(1932). 
Zoond  and  Eyre.     Philo.s.  Trans.  B,  223, 
27  (1934). 


CHAPTER   V 
THE  EMERGENCE  OF  VISION 

In  the  varying  reactions  of  living  organisms  to  light  that  we  have 
now  studied,  in  some  cases  vision  does  not — or  need  not — co-exist,  in 
others  an  associated  sensory  impression  is  conjectural  and  unimportant 
while  in  others  it  seems  to  be  a  necessary  accompaniment  ;  indeed,  it 
is  no  easy  matter  to  decide  where  its  origin  lay  or  when  the  sense  of 
vision  first  became  a  factor  in  conscious  behaviour.  There  are  many 
creatures  which  have  no  eyes  (as  we  understand  the  term)  and  yet 
"  see  "  (using  the  word  in  its  widest  sense)  ;  and  equally  reasonably  it 
may  be  said  that  there  are  many  which  have  what  we  may  well  call 
"  eyes  "  and  yet  see  not. 

To  a  considerable  extent  the  matter  is  one  of  definition  ;  on  the 
one  hand,  few  would  acquiesce  with  Max  Schultze  (1868)  who  spoke  of 
the  transformation  of  luminous  into  nervous  energy  as  vision  ;  more 
would  agree  with  Hesse  (1908)  who  contended  that  the  light-sensitiveness 
of  primitive  creatures  did  not  imply  the  possession  of  a  light  sense.  On 
the  other  hand,  there  are  those  w^ho  would  ascribe  to  all  animals  which 
react  to  light  a  sentiency,  no  matter  how  vague  (McDougall,  1933). 
To  many  this  may  seem  gratuitously  anthropocentric  ;  for  if  such  an 
awareness,  tinged  with  affective  tone,  is  ascribed  to  the  amoeba  as  it 
flees  from  a  bright  light  and  expands  in  mid-intensities  of  illumination, 
is  it  to  be  ascribed  also  to  the  speedwell  which  opens  its  petals  to  the 
mid-morning  sun?  The  question  is  disputable  ;  but  whichever  attitude 
we  adopt  the  most  illegitimate  premise  from  which  we  can  reason  is  the 
assumption  that  an  organism  has  the  same  appreciation  of  light  and 
patterns  of  shade  or  hue  as  ourselves,  whether  it  reacts  diffusely  without 
specific  end-organs  or  whether  it  is  possessed  of  eyes  more  highly 
differentiated  for  the  resolution  of  visual  images  than  the  relatively 
simple  eyes  of  man.^ 

It  must  be  remembered,  however,  that  vision  is  one  of  the  latest 
senses  to  be  evolved  and  that  in  its  phylogenetic  development  it 
lingered  long  behind  those  depending  on  mechano -receptors  and 
chemo-receptors.  Even  when  a  considerable  stage  of  complexity  had 
been  reached  there  was  little  attempt  at  discrimination  ;  for  this 
purpose  reliance  was  placed  upon  those  senses  which  are  more  fully 
developed  in  primitive  life — the  tactile  sense,  the  chemical  sense,  and 
the  olfactory  sense.     The  great   majority  of  animals  are  non-visual 

'   The  few  sicjn-stimuli  to  which   the  vision  even   of  birds  is  limited  are  striking 
examples  (p.  664 , 


THE    EMERGENCE   OF   VISION 


103 


creatures    depending    essentially    in    their    behaviour    on    non-visual 
stimuli. 

For  example,  the  scallop  has  numerous  visual  cells  around  the  edge  of  its 
mantle,  and  if  these  are  stimulated  by  the  "  sight  "  of  its  enemy,  the  starfish, 
no  response  except  the  awareness  of  the  presence  of  something  is  elicited,  and 
no  attempt  at  flight  is  made  ;  but  whenever  some  extract  of  starfish  is  added 
to  the  water  in  which  the  animal  lies,  the  scallop  immediately  runs  away  (Dakin, 
1909  ;  von  Uexkiill,  1921).  ]\Ioreover,  in  Pecten,  no  response  is  called  forth 
until  the  object  moves,  and  any  movement  of  any  object  excites  the  same 
response,   a  protrusion  of  the  tentacles  ;    these  are  endowed  with  organs  of 


Fig.   74. — The  Sensory  Reactions  of  the  Water  Beetle. 

A  watery  meat  extract  is  contained  in  tiie  bag.  The  feeding  responses  of 
Dytiscus  marginalis  show  its  dependence  on  chemical  stimuli  rather  than  vi.sual 
(Tinbergen,  Study  of  Instinct  ;   Clarendon  Press). 


chemical  and  tactile  sensitivity  which  exjilore  the  object  "  intelligently",  and 
on  the  results  of  their  findings  the  animal  either  eats  or  flees  (Dakin,  1910). 
The  purpose  of  this  response  is  obviously  to  secure  further  information  in  a  form 
in  which  it  is  analysable.  Even  in  man  the  olfactory  sense  organs  are  relatively 
more  fully  developed  than  the  visual  at  birth  ;  a  fish  with  its  olfactory  nerves 
severed  ceases  to  feed  spontaneously  (Steiner,  1888)  ;  and  the  lately-born  rabbit 
will  die  of  starvation  if  deprived  of  the  sense  of  smell  because  it  cannot  find  the 
teats  of  its  mother,  even  although  it  has  been  allowed  to  make  use  of  its  eyes 
before  it  has  suffired  the  loss  of  the  more  fundamental  sense. 


104  THE   EYE   IN   EVOLUTION 

It  must  also  be  remembered  that  even  although  vision  is  well  developed  it 
may  not  be  used  in  many  innate  reactions  for  the  efficient  execution  of  which 
it  would  appear  to  us  to  be  of  value.  The  feeding  response  of  the  carnivorous 
water-beetle,  Dytiscus  marginalis,  is  a  good  example  of  this  (Tinbergen,  1936) 
(Fig.  74).  This  beetle  has  elaborately  developed  compound  eyes  and  can  be 
trained  to  respond  to  visual  stimuli.  Its  feeding  response,  however,  is  released 
only  by  chemical  and  tactile  stimuli,  and  visual  impressions,  even  those  of  a 
moving  prey,  never  release  this  reaction.  Thus  in  the  presence  of  a  watery  meat 
extract  it  neglects  the  source  but,  going  to  the  region  of  highest  concentration, 
it  attacks  any  solid  object  it  touches. 

Of  the  three  fundamental  effects  of  hght  on  Hving  organisms — the 
stimulation  (or  occasionally  the  depression)  of  metabolic  activity,  the 
orientation  of  movement,  and  the  control  of  pigment  and  colour — it 
would  he  reasonable  to  assume  that  the  first,  equally  shared  between 
plants  and  animals,  does  not  necessarily  involve  vision  as  a  conscious 
experience,  occurring  as  it  does  in  Protozoa  and  eyeless  types. ^  In  its 
more  primitive  form  this  activity  may  conjecturally  be  accompanied 
by  a  vague  sentiency,  but  this  can  be  little  more  than  an  awareness  of 
light,  and  even  in  its  most  advanced  forms  it  is  essentially  a  chemical 
or  hormonal  function  for  the  implementation  of  which  eyes  are  effective 
but  not  unique  receptors.  The  last — the  control  of  colour — is  a  late 
evolutionary  development,  and  although  j^oikilochromic  reactions 
would  appear  to  occur  without  conscious  accompaniment,  in  their 
higher  developments  they  would  seem  to  imply  the  existence  of  a  visual 
sense  in  the  organism  for  whose  benefit  (or  confusion)  they  are  intended. 
The  economy  would  seem  unnatural  and  contrary  to  all  biological 
trends  that  at  one  time  urged  all  plants  except  the  modest  Cryptogams, 
in  their  struggle  for  existence  in  a  cooling  world,  to  luxuriate  so  shame- 
lessly in  the  blatant  sexual  exhibitionism  of  flowering  if  the  pollinating 
insects  could  not  both  see  and  appreciate  their  charms  ;  their  appre- 
ciation, however,  has  probably  no  resemblance  to  the  interpretation 
of  the  same  imagery  by  the  human  brain.  Equally  uneconomic  would 
be  the  scandalously  attractive  dress  put  on  by  many  fishes  and  birds 
for  tlieir  love-making.  Clearly,  if  they  are  endowed  with  biological 
usefulness  and  survival-values,  allsesthetic  characters — and  without 
these  endowments  they  would  not  jiersist — must  be  appreciated  by 
other  organisms. 

Although  the  eyes  serve  as  the  receptors  for  many  adaptive  colour 
changes,  this  function  need  not  imj^ly  that  the  animal  it'self  has  any 
conscious  appreciation  excited  by  shifting  visual  patterns.  Even  when 
the  responses  are  mediated  nervously  and  are  rapid  and  complex,  as  in 
teleostean  fishes,  they  show  no  parallelism  with  what  is  known  of  the 
visual  functions  of  the  animals  concerned,  for  reflex  alterations  of  the 
chromatophores  may  occur  to  suit  differences  in  shade  of  the  back- 

'  Such,  for  example,  as  the  white  cave  crayfish,  Cambarus  ayersii  (Wells,  1952). 


THE    EMERGENCE   OF   VISION  105 

ground  too  small  to  excite  visual  discrimination  in  training  experiments. 
Many  of  the  reactions,  as  we  have  seen,  are  hormonal  ;  some  may 
occur  in  eyeless  animals  ;  and  indeed,  in  species  wherein  these  organs 
are  necessary  for  their  occurrence  the  chromatophores  may  still  respond 
if  the  eyes  are  transplanted  to  a  new  location  in  the  body  (as  was 
demonstrated  in  the  adult  fish,  Fitzroya  lineafa,  by  Szepsenwol,  1938). 
Temperature  and  humidity,  as  seen  in  Amj)hibians  and  Reptiles,  may 
be  equallj^  or  more  effective  stimulants  in  comparison  with  light,  and 
although  heat  and  light  usually  coincide  in  natural  surroundings,  the 
paling  of  the  desert  lizard  in  the  heat  of  noon  so  that  it  blends  with  the 
sand  is  fortuitous  so  far  as  its  own  vision  is  concerned.  Tactile  organs 
are  sometimes  adequate  receptors  as  is  seen  in  the  control  of  chromato- 
phores by  the  suckers  of  Cephalopods  (Steinach,  1901)  ;  while  the 
adoption  of  a  brown  colour  by  the  European  tree-frog,  Hyla  arborea, 
when  it  steps  on  a  rough  surface  and  of  a  green  colour  on  a  smooth 
surface  brings  about  an  environmental  adaptation  to  a  background  of 
tree-bark  or  leaves  respectively  as  adequate  as  any  photic  response. 
Indeed,  many  of  these  colour  reactions  are  fortuitous  so  far  as  adapta- 
tion to  a  background  is  concerned  ;  thus  the  iguanid  lizard,  Anolis, 
turns  green  in  the  shade  and  brown  when  exposed  to  light,  and  it  is 
merely  coincidental  that  in  its  natural  haiuits  it  usually  becomes 
invisible  on  a  background  of  shady  foliage  in  the  first  event  or  of  soil 
in  the  second,  since,  if  it  is  removed  from  the  shade  upon  a  green  leaf 
and  placed  in  the  sun  still  sitting  on  the  leaf,  it  promptly  changes  its 
colour  into  a  vividly  contrasting  brown  (Wilson,  1939). 

It  is  essentially  from  the  primitive  motor  response  to  light  that 
vision  almost  certainly  developed.  In  natural  circumstances  these 
tropisms  and  taxes  are  invariably  of  biological  utility,  and  it  would 
appear  that  the  essential  and  'primary  function  of  vision  was  the  control 
of  movement  iyi  order  to  attain  an  optimum  environment  as  efficiently  as 
jiossible,  a  function  which  is  eventually  employed  for  the  avoidance 
of  obstacles,  the  pursuit  of  prey  and  flight  from  enemies,  and  survives 
in  man  in  the  close  relationship  between  the  eyes  and  the  vestibular 
apparatus  and  in  their  importance  in  the  control  of  posture.  It  follows 
that  visual  organs  are  found  almost  solely  in  actively  moving  animals, 
while  in  such  as  assume  a  sedentary  phase  they  tend  to  degenerate 
and  disappear.^ 

The  stage  at  which  these  motorial  responses  to  light  evolved 
beyond  purely  reflex  acts  below  the  level  of  consciousness  and  became 
endowecl  with  awareness  is  impossible  to  conjecture.  This  question 
has  given  rise  to  a  controversy  which  is  still  luisettled. 

In  the  simple  philosophy  of  Aristotle  -  and  for  2,000  years  thereafter  no 
argument  arose  ;   plants  had  a  vegetative  soul  responsible  for  growth  and  repro- 

1  o.  721.  -  p.  28. 


106  THE   EYE   IN   EVOLUTION 

duction,  to  animals  was  added  a  sensitive  soul  governing  movement  and  sensation, 
and  to  man  a  rational  soul.  But  doubts  occupied  men's  minds  particularly  in 
the  seventeenth  and  eighteenth  centuries  in  the  long  disputation  between  the 
materialistic  French  Cartesians  who  followed  Descartes  (1596-1650)  and  the 
English  Newtonians  who  were  inspired  by  Newton  (1642-1727)  on  the  one  hand, 
and  the  mystic  German  Nature-philosophers  on  the  other,  the  disciples  of 
Paracelsus  in  the  classical  tradition,  who  found  philosophical  expression  in 
Leibnitz  (1646-1716)  and  Goethe  (1749-1832).  To  the  first  the  universe  was  essenti- 
ally mechanical ;  to  the  second  not  only  living  creatures  but  minerals  and  chemical 
compounds  were  permeated  by  a  directive  vital  force.  A  middle  view  was 
represented  by  Lamarck  (1744-1829)  who  claimed  that  the  lowest  organisms 
were  insensitive  and  that  their  conduct  was  completely  governed  by  external 
factors,  driving  forces  derived  from  the  environment  ;  but  as  the  evolutionary 
scale  was  ascended  and  a  centralized  nervous  system  was  acquired,  organisms 
generated  their  own  "  sentient  interieur  "  to  a  progressivly  greater  degree,  thus 
attaining  an  ever-increasing  measure  of  self-determination  until  Vertebrates 
were  reached,  at  which  stage  intelligence  became  possible  and  ultimately  found 
its  fullest  expression  in  Man.  Each  of  these  views  has  been  maintained  in  recent 
times — the  simple  reflexology  represented  by  Loeb  (1918)  and  the  Russian  school 
(Sechenov,  1863  ;  Bekhterev,  1913  ;  Pavlov,  1926-27)  on  the  one  hand,  and 
the  purposive  or  "directive"  psychology  represented  by  Whitehead  (1929), 
McDovigall  (1933)  and  Russell  (1934-45)  on  the  other,  wherein  vital  force  has 
been  replaced  by  the  "  general  drive  "  of  modern  biologists,  a  state  of  tension 
or  action-energy  which  activates  living  organisms.  Each  view  would  find  its 
advocates  today. 

The  mechanistic  view  would  place  the  emergence  of  visual  reflexes 
into  the  plane  of  consciousness  as  a  late  development.  This  attitude 
found  its  apostle  in  Jacques  Loeb  (1906-18)  ^  who  considered  that  all 
the  orientating  and  instinctive  reactions  of  the  lower  animals  to  light 
or  other  stimuli  were  mechanically  determined  ;  although  in  many- 
cases  it  seems  to  respond  voluntarily  and  often  purposively,  the  move- 
ments of  the  phototactic  animal  are  those  of  a  robot  ;  it  is  forced  to  go 
where  it  is  taken  by  its  reflexly-driven  cilia,  legs  or  wings,  an  activity 
in  which  consciousness  or  vision  has  no  place.  Even  an  ant  with  all  its 
proverbial  intelligence  orientates  its  journey  to  light  unthinkingly  as 
does  a  sleep-walker  or  an  automaton  ^  and  in  this  respect  is  as  unteach- 
able  as  a  machine,  completely  totalitarian  and  incapable  of  individual 
adjustment. 

It  must  be  remembered  that  the  new  science  of  cybernetics  has  demonstrated 
that  similar  reactions,  sometimes  of  astonishing  complexity,  can  be  carried  out 
by  non -vital  mechanisms,  those  curious  electro -mechanical  first  cousins  of 
computing  machines,  which  by  a  combination  of  photo-cells,  amplifiers,  motors  and 
automatic  governing  devices,  can  simulate  many  of  the  reactions  of  living  things, 
not  in  appearance  bvit  in  behaviour,  as  they  navigate  themselves  around  the 
play-room  of  the  electronic  engineer  (see  Ashby,  1952  ;  Walter,  1953  ;  and 
others).  Such  mock-biological  robots,  goal-seeking  and  self-regulatory,  capable 
of  the  storage  of  information  and  possessed  of  a  rudimentary  type  of  memory 

1  p.  28.  2  p   (38_ 


THE   EMERGENCE   OF   VISION  107 

maintained  by  electrical  oscillations,  have  been  constructed  so  that  they  can 
explore  their  environment  with  an  apparent  purpose.  A  photo-cell  can  serve 
as  a  receptor  and  amplifiers  and  motors  can  be  interconnected  in  such  a  way 
that  a  positive  taxis  (for  example)  to  a  moderate  light  and  a  negative  taxis  to 
bright  light  (or  to  material  obstacles,  gradients,  etc.)  can  endow  it  with  the  faculty 
to  discriminate  between  effective  and  ineffective  behaviour,  to  seek  actively  an 
environment  with  moderate  and  optimal  conditions,  to  acquire  conditioned 
reflexes,  and  even  to  perpetuate  its  activity  and  "  feed  "  itself  with  electricity 
by  being  optically  attracted  to  a  charging  circuit  when  its  batteries  begin  to  fail. 

On  the  other  hand,  there  are  those  who  consider  that  such  auto- 
mata have  httle  resemblance  to  even  the  simplest  living  things  ;  their 
behaviour  has  only  a  superficial  appearance  of  being  dominated  by- 
taxes  and  kineses,  by  memory,  habituation  or  trial-and-error  learning. 
The  school  of  biological  philosophy  formalized  by  Whitehead  (1929), 
amplified  by  McDougall  (1933)  and  pursued  by  such  recent  writers  as 
Agar  (1943)  and  Thorpe  (1956)  argues  that  every  vital  event  is  an  act 
of  percejition.  a  mental  as  opposed  to  a  material  process  ;  a  living 
organism  is  essentially  something  which  perceives  ;  its  behaviour 
is  not  an  automatic  response  to  sensory  impressions  but  includes  an 
element  of  purpose  building  up  primary  perceptions  into  unitary 
systems  in  which  the  whole  is  different  from  and  greater  than  the 
sum  of  its  constituent  parts.  Such  a  view,  as  we  have  already  hinted, 
tends  to  pan-psychism,  or  even  to  pan-theism  ;  according  to  it  a 
purely  objective  biology  is  sterile  ;  like  the  warp  and  woof,  mechanism 
must  be  interwoven  with  teleology.^  While  mechanisms  may  even- 
tually become  explicable  in  physico-mathematical  terms,  there  is  no 
suggestion  yet  that  the  subjective  concepts  of  conscious  purpose  ever 
will  be  (Sommerhoff,  1950).  But.  even  although  this  is  agreed,  it  is  to 
be  remembered  that  there  are  no  grounds  for  supposing  that  any 
well-defined  mental  content  is  associated  with  the  reactions  of  the 
lower  animals  comparable  to  the  perceptual  experiences  of  the 
higher  animals. 

On  tlie  whole  it  would  seem  that  the  matter  is  not  so  simple  as  the 
more  materialistic  outlook  might  suggest.  It  is  true  that  many  of  these 
primitive  tropic  activities  of  the  animal  world  can  be  interpreted  as 
reflexes  without  motivation,  incentive  or  appreciation  ;  but  because 
there  are  no  discernible  conscious  acconipaniments  to  many  purely 
reflex  acts  in  man  whose  apperceptive  powers  have  been  translated 
from  the  level  of  ganglia  to  the  cerebral  cortex,  it  by  no  means  follows 
that  there  are  none  in  those  lowlier  organisms  the  nervous  system  of 
which  consists  only  of  ganglia  and  nerve -fibres — or  even  of  an  un- 
centralized  nerve-net  or  nothing  at  all.  It  must  be  remembered  that  the 
transference  of  sensory  appreciation  to  the  neopallium  occurred  late  in 
evolutionary  history,^  and  that  although  the  lower  centres  in  man  have 

1   See  D'Arcy  Thompson  (1942).  =  p.  542. 


108  THE   EYE    IN   EVOLUTION 

become  merely  relay-stations  in  this  respect,  they  used  to  subserve 
much  more  important  functions.  Indeed,  in  the  higher  animals — and 
to  some  extent  also  in  man — much  of  mental  and  most  of  visual 
activity,  especially  those  aspects  associated  with  primitive  responses 
and  endowed  with  emotional  tone,  remain  closely  associated  with  the 
vegetative  activities  which  are  integrated  in  the  thalamus.  Even  in 
Fishes  and  Amphibians,  vision  is  entirely  unrepresented  in  the  cortex. 

Thus  although  ablation  of  his  occipital  lobes  deprives  man  permanently 
and  completely  of  all  sensations  of  light,  the  higher  mammals  are  by  no  means 
so  incapacitated. 1  Most  decerebrate  Vertebrates  will  react  and  exhibit  emotions 
to  visual  stimuli  and  even  perform  complex  instinctive  reactions  without 
difficulty.  So  will  the  headless  bee  sting  with  accuracy  on  irritation  (Bethe, 
1897)  and  the  clover-fly  clean  its  wings  with  its  legs  after  decapitation 
(Sherrington,  1920).  A  brain,  or  even  a  head -ganglion,  is  thus  not  a  necessary 
residence  for  apparently  "  intelligent  "  reactions. 

Phototactic  reactions  are  "  instincts",  that  is,  adapted  reactions 
of  a  purposive  nature  handed  down  from  the  previous  experience  of 
ancestors  ;  and,  as  with  all  instincts,  the  component  afferent  impulses 
have  become  associated  in  consciousness  and  synthesized  into  a 
meaningful  pattern,  a  process  which  necessarily  connotes  some  degree 
of  perception. 2  As  instincts,  their  usual  stereotyped  uniformity  can  be 
modified  by  experience  provided  the  modification  tends  to  the  well- 
being  of  the  individual — or  the  race.  The  reactions  of  even  the  lowly 
earthworm  are  amenable  to  training  ^  ;  many  molluscs  are  readily 
trainable  ;  many  insects  eminently  so.  Thus  the  photo -negative 
cockroach,  BlateUa  gennanica,  can  be  conditioned  to  advance  towards 
a  light  provided  it  has  been  taught  that  a  dark  and  comfortable  shelter 
is  placed  beneath  it  (Goustard,  1948).  Similarly,  as  we  have  seen,* 
after  interference  with  its  receptors  or  effectors  either  by  partial 
blinding  or  by  removing  some  of  its  legs,  the  mutilated  insect  will 
rapidly  modify  its  reactions  and  after  several  trials  will  learn  to 
orientate  itself  to  light  with  almost  the  same  accuracy  as  before.  It  is 
thus  impossible  to  say  where  in  the  animal  scale  reactions  to  light  were 
first  associated  with  conscious  awareness  ;  nor  can  we  guess  the  form 
such  consciousness  may  take,  for  like  a  solid  to  an  inhabitant  of 
Flatland,  it  exists  in  a  form  which  cannot  be  assessed  by  the  measuring 
instruments  at  our  disposal  ;  we  can  only  reason  by  inference  from  an 
analysis  of  our  own  peculiar  form  of  consciousness  of  which  alone  we 
have  immediate  knowledge.  From  a  study  of  the  sensory  capacities  of 
animals  few  things  emerge  more  certainly  than  that  each  species  has 
its  own  perceptual  world  (the  MerhveU  of  v.  Uexkiill,  1921),  and  that 

1  p.  545. 

2  See  Lloyd  Morgan  (1896-1912),  Jennings  (1906),  Sherrington  (1920),  Parsons 
(1927),  and  manv  others. 

»  p.  573.      "  «  p.  59. 


THE   EMERGENCE   OF   VISION  109 

each  of  this  midtitiide  of  worlds  bears  Httle  resemblance  to  the  environ- 
ment of  the  animal  as  we  see  it  or  interpret  it  in  terms  of  our  own 
Merkwelt. 

It  seems  reasonable  to  assume  that  the  development  of  vision  as  a 
facet  of  consciousness  evolved  in  three  stages.  We  may  surmise  that 
the  first  conscious  appreciation  was  a  mere  sentiency,  crudely  vague 
and  undifferentiated,  characterized  perhaps  by  a  minimum  of  cognition 
endowed  with  a  rudimentary  affective  tone  ;  it  was  limited  perhaps  to 
an  awareness  of  the  existence  of  light  as  a  change  in  the  environment, 
tinged  perhaps  with  sufficient  affective  tone  to  allow  it  to  be  appreciated 
as  pleasant  or  mipleasant,  and  endowed  witli  meaning  in  so  far  as  the 
organism  responded  apjDropriately  by  motor  activity  in  which  initially 
there  was  offered  the  choice  only  of  two  alternatives,  towards  or  away 
from  the  source  of  stimulation.  We  may  even  surmise^  as  indeed  exjjeri- 
mental  evidence  on  the  amoeba  would  suggest,^  that  the  most  primitive 
sensation  was  a  co-sesthesis  without  constituent  modalities  in  which  the 
several  senses  as  we  know  them  were  merged  into  a  vague  and  indis- 
criminate unity,  and  the  stimuli  (photic,  chemical,  tactile,  etc.)  which 
to  us  are  distinct  and  unrelated  were  co-equal  and  additive.  Some  such 
concept  as  the  emergence  of  a  consciousness  of  a  lowly  type  at  an  early 
but  unknown  stage,  on  the  reflex  plane  or  even  below,  would  seem 
a  possible  hypothesis,  a  consciousness  at  first  indefinable  and  vague 
but  at  the  same  time  sufficiently  plastic  to  contain  the  germ  of  the 
elaborate  emotional  behaviour  of  the  higher  animals — so  long  as  we 
remember  that  the  latter  with  all  its  undoubted  richness  and  com- 
plexity bears  little  resemblance  to  the  consciousness  of  man. 

For  such  a  surmise,  however,  there  is  no  direct  evidence;  at  this 
level  the  motor  response  to  stimulation  is  all  we  can  directly  assess. 
From  morphological  and  behavioural  observations,  however,  we  can 
be  more  certain  that  a  primitive  perception  of  light  emerged  with  the 
development  of  a  centralized  nervous  system  in  worms  - ;  at  this  stage 
in  evolution  it  would  seem  reasonable  to  suppose  that  a  mechanism 
became  available  for  the  creation  of  perceptual  symbolism;  and  at 
this  stage  vision  undoubtedly  became  a  perceptual  process  forming  part 
of  the  conscious  life  of  the  animal  and  capable,  at  first  in  a  minor 
degree,  of  determining  its  conduct.  As  we  ascend  the  animal  scale  the 
primitive  light-sense  evolved  into  a  sense  of  appreciation  of  the 
directional  incidence  of  light,  of  movement,  of  form,  and  eventually 
of  colour,  until  in  the  Primates  the  capacity  to  analyse  complex 
visual  patterns  ])ecame  the  chief  determinant  of  conduct.  In  its  final 
development,  the  first  elements  of  which  have  been  detected  in  the 
chimpanzee,'*  the  sense  of  vision  j^assed  beyond  the  stage  of  passively 

1   p.   3G.     Compari'  also  the  integration  of  jjliototaxi.s  and  galvaiiotroi^ism  seen  in 
certain  worms  (p.  33).  ^  p.  572.  ^  p.  602. 


110 


THE   EYE    IN   EVOLUTION 


recording  objective  appearances  in  the  outside  world  and  emerged  as 
an  imaginative  and  creative  sense.  This  aesthetic  quahty  was  certainly 
a  late  acquisition  acquiring  maturity  only  in  man.^ 

The  extent  to  which  in  the  animal  scale  an  appreciation  of  these 
three  progressive  stages  became  a  factor  in  the  customary  activities 
of  the  life  of  living  organisms  is  a  question  which  must  await  the 
acquisition  of  a  much  more  profound  knowledge  of  their  natural 
history  than  we  at  present  possess.  And — whatever  the  future  may 
bring  forth — the  manner  of  its  becoming  so  is  inexj^licable  by  any 
physico-mathematical  techniques  we  have  at  our  disposal  today  or  will 
have  tomorrow. 


Agar.     The  Theory  of  the  Living  Orgaytism, 

Melbourne  (1943). 
Ashby.       Design   for    a    Brain,     London 

(1952). 
Bekhterev.        La     Psychologie     obiective, 

Paris  (1913). 
Bethe.     Arch,  viikr.  Anat.,  50,  589,   629 

(1897). 
Dakin.     Pecten,  London  (1909). 

Quart.  J.  micr.  Sci.,  55,  49  (1910). 
Goustard.     C.  R.  Acad.  Sci.  (Paris),  227, 

785  (1948). 
Hesse,   R.      Das  Sehen  d.  niederen   Tiere 

(1908). 
Handb.  norm.  path.  Physiol.,  12  (1),  61 

(1929). 
Jennings.     The  Behavior  of  Lower  Organ- 
isms, N.Y.  (1906). 
Lloyd     Morgan.        Habit     and     Instinct, 

London  (1896). 
Instinct  and  Experience,  London  (1912). 
Loeb.      The  Dynamics  of  Living  Matter, 

N.Y.  (1906). 
The    Mechanistic    Conception    of    Life, 

Chicago  (1912). 
Forced  Movements,  Tropisms  and  Animal 

Conduct,  Phila.  (1918). 
McDougall.      An    Outline    of   Psycliology, 

6th  Ed.  (1933). 
Parsons.    Intro,  to  the  Theory  of  Perception, 

Cantab.  (1927). 
Pavlov.     Die  hochste  Nerventdtigkeit   (das 

Verhalten)      von      Tier  en,      Miinohen 

(1926). 
Conditioned  Reflexes,  Oxon.  (1927). 


Russell.        The     Behaviour     of    Animals, 

London  (1934). 
The  Directiveness  of  Organic  Activities, 

Cantab.  (1945). 
Schultze.     Untersuch.  il.  das  Zusam.  Auge 

der  Krebse  u.  Insekten,  Bonn  (1868). 
Sechenov^       The    Reflexes    of    the    Brain 

(1863)  :     Trans,    in    Selected    Works, 

Moscow  (1935). 
Sherrington.     Tlie  Integrative  Action  of  the 

Nervous  System,  Yale  (1920). 
Sommerhoff.     Ancdytical    Biology,    Oxon. 

(1950). 
Steinach.     Pfliigers  Arch.  ges.  Physiol.,  81, 

1  (1901). 
Steiner.        Die    Functionen    des    Central- 

nervensystem,  2  (1888). 
Szepsenwol.    C.  R.  Soc.  Biol.  (Paris),  129, 

1265  (1938). 
Thompson,  D'Arcy.    On  Growth  and  Form, 

Cantab.  (1942). 
Thorpe.    Learning  and  Instinct  in  Animals, 

London  (1956). 
Tinbergen.     De  Levende  Natuur,  41,  225 

(1936). 
von   Uexktill.      Umwelt  u.   Innenwelt  der 

Tiere,  Berlin  (1921). 
Walter.        The     Living     Brain,     London 

(1953). 
Wells.    Anat.  Rec,  113,  613  (1952). 
Whitehead.   Process  and  Reality,  Cantab. 

(1929). 
Wilson.    Amer.  Nat..  73.  190  (1939). 


p.  753. 


PART  II 
THE  EVOLUTION  OF  THE  VISUAL  APPARATUS 

The  Morphology  of  Invertebrate  Eyes 

The  Systematic  Anatomy  of  Invertebrate  Eyes 

The  Eyes  of  Protochordates 

The  Evolution  of  the  Vertebrate  Eye 

The  Eyes  of  Cyclostomes 

The  Eyes  of  Fishes 

The  Eyes  of  Amphibians 

The  Eyes  of  Reptiles 

The  Eyes  of  Birds 

The  Eyes  of  Mammals 

The  Central  Organization  of  Vision 


Fig.  75.— Richard  Hesse  (1868-1944). 


CHAPTER    VI 
THE  MORPHOLOGY  OF  INVERTEBRATE  EYES 

RICHARD  HESSE  (1868-1944)  (Fig.  75),  one  of  the  greatest  of  German 
zoologists,  probably  contributed  more  towards  the  study  of  the  sense  organs, 
particularly  the  visual  organs,  of  the  lower  animals  than  any  other  single  indivi- 
dual. The  greater  part  of  his  life  was  devoted  to  this  subject.  Professor  of 
Zoology  at  Tiibingen  in  1901,  he  became  Professor  at  the  Agricultural  School 
in  Berlin  in  1909,  occupied  the  Chair  of  Zoology  at  Bonn  in  1914,  and  was 
Professor  of  Zoology  and  Director  of  the  Zoological  Institute  at  the  University 
of  Berlin  from  1926  to  1935.  His  systematic  study  of  the  light-sensitive  organs 
of  Invertebrates  was  lai-gely  conducted  between  1896  and  1908  and  included 
an  immense  range  of  types  varying  from  the  relatively  simple  eyes  of  worms 
to  the  highly  developed  visual  organs  of  Molluscs  and  Arthropods,  an  interest 
which  he  maintained  throughout  his  long  and'  fruitful  life.  As  will  be  seen  in 
the  following  pages,  his  studies  form  the  basis  of  our  understanding  of  the 
astonishing  variation  in  the  morjDhology  of  the  eyes  of  the  Invertebrates.  It  is 
surprising  how  little  systematic  work  has  been  done  on  this  fascinating  subject 
since  his  day. 

THE  GENESIS  OF  THE  EYE 

It  is  evident  from  the  subject-matter  of  the  previous  chapters  that 
the  eye  has  evolved  from  remote  and  lowly  origins,  far  removed  in  form 
and  in  function  from  the  highly  specialized  mechanism  we  find  in  Man. 
In  the  most  primitive  miicellular  organism,  as  we  have  already  seen  in 
the  case  of  the  amoeba,^  there  is  a  diffuse  reaction  to  light  whereby  the 
entire  cell,  and  particularly  its  superficial  layers,  in  the  absence  of  any 
apparent  specialization  of  structure  responds  by  a  simple  alteration  of 
the  sol-gel  reversibility  of  the  relatively  fluid  protoplasm.  In  its 
earliest  form  this  would  seem  to  be  an  imdifferentiated  response 
common  to  all  stimuli  (photic,  tactile,  thermal,  chemical)  (Pantin, 
1924-26  ;  Folger,  1926-27  ;  Mast,  1926-32).  A  reaction  of  this  simple 
nature  to  light  is  t\^3ical  of  the  Rhizopods,  such  as  the  amoeba, 
but  among  multicellular  organisms  we  would  expect  it  to  be  localized 
preferentially  in  the  cells  on  the  surface  which  are  exposed  to  the 
stimuli  of  the  external  world  ;  it  thus  evolves  into  a  general  dermal 
jihotosensitivity.  This  may  occur  sometimes  in  the  absence  of  known 
photoreceptors,  sometimes  in  association  with  them,  and  it  is  interesting 
that  even  when  these  are  present,  the  more  primitive  and  less  specialized 
mechanism  may  dominate  the  behaviour  of  the  animal  in  its  reactions 
to  light  more  effectively  than  the  conspicuous  receptor  organs. 

1  p.  3.-,. 


114 


THE   EYE   IN   EVOLUTION 


Dytiscus 


Myxine 


A  nodonta 


The  mechanism  of  this  dermal  sensitivity  is  conjectural.  The 
reaction  may  be  initiated  by  photosensitive  pigments  and,  although  in 
most  cases  such  have  not  been  identified,  they  could  be  present  in  very 
small  amounts  (von  Uexkiill,  1897).  On  the  other  hand,  it  is  conceiv- 
able that  nerve  elements  lying  subdermally  may  be  directly  stimulated, 
a  view  for  which  Millott  (1954-57)  produced  firm  evidence  in  the  case 
of  the  sea-urchin,  Diadema.  Such  a  reaction  would  correspond 
to  the  activity  of  the  organelle  of  the  apolar  hght-sensitive  cells  of 
worms,  the  sixth  abdominal  ganglion  of  crayfish  and  lobsters,^  and  the 
nerve  elements  in  the  diencephalon  of  lampreys,  minnows  and  ducks. ^ 
Again,  Bohn  (1940)  and  Viaud  (1948)  looked  upon  the  reaction  as  a 
common  property  of  protoplasm  depending  on  "  electrochemical 
polarization",  a  property  readily  evident  in  lower  forms  but  often 
neutralized  or  masked  by  more  potent  reactions  in  higher  forms. 

Such  a  dermal  light-sensitivity  (the  dermatopsia  of  Graber,  1884)  is  of 
wide  distribution  occurring  in  members  of  almost  all  phyla. ^  While  it  is  usually 
diffuse  it  may  be  particularly  well  developed  in  certain  situations  wherein  its 
biological  utility  is  greatest,  often  the  fore-pai't  of  the  animal  or  in  such  situations 
as  the  region  of  the  spiracles  of  the  abdomen  of  the  larv.'B  of  the  water-beetles, 
Acilius  and  Dytiscus  (Schone,  1951).  Such  a  sensitivity  is  particularly  marked 
and  widesj^read  among  Echinoderms  (Cuenot,  1891)  ;  it  occurs  in  some  Molluscs, 
Turbellarians  and  Annelids,  as  well  as  in  some  Insects,  in  Cyclostomes  [Myxine 
glutinosa,  Newth  and  Ross,  1955),  in  eyeless  cave-fish  (Thines  and  Kahling,  1957) 
and  in  blinded  cat-fish.  The  response  to  dermal  sensitivity  is,  of  course,  a  photo- 
kinesis  which  may  be  either  jjositive  or  negative.  Thus  the  eyeless  mussel, 
Anodonta,  reacts  to  a  passing  shadow  (Knoop,  1954  ;  Braun  and  Faust,  1954), 
blind  cavernicolous  beetles  (Anophthalmns)  respond  to  the  light  of  a  candle 
(Marchal,  1910),  and  after  complete  blinding  some  insects,  such  as  cockroaches, 
will  settle  preferentially  in  the  dark,^  a  reaction  which  may  persist  even  after 
decapitation,^  while  others  are  attracted  to  light.* 

It  is  to  be  noted  that  the  dermal  response  to  light  need  not  be  of  the 
same  type  as  the  ocular  response  ;  the  two  may,  indeed,  be  mutually  exclusive. 
Thus  it  will  be  remembered  '  that  the  flat-worm,  Planaria  lugubris,  is  positively 
photokinetic  so  far  as  the  dermal  response  is  concerned  while  it  orientates  itself 
by  a  negative  phototaxis  through  the  eyes  (Viaud  and  Medioni,  1949).  Again, 
the  receptors  in  the  skin  and  the  eyes  may  show  different  sensitivities.  Thus 
Viaud  (1948)  found  that  in  some  organisms  the  maximum  response  of  the  dermal 
mechanism  was  elicited  by  wave-lengths  at  the  short  end  of  the  visible  spectrum 
(the  water-flea,  Daphnia  ;  the  rotifer,  Branchionus)  while  the  eyes  responded 
preferentially  to  wave-lengths  about  the  middle  of  the  spectrum.  A  com- 
bination of  the  two  mechanisms  in  the  same  organism  may  thvis  involve  two 
maxima  in  the  response  (as  in  the  fruit-fly,  Drosophila). 


Daphnia 


^  p.  115.  2  p_  537 

3  For  reviews,   see   Willem   (1891),   Dubois   (1892),   Nagel   (1896). 
Viaud  (  1948)  whose  views  have  already  been  discussed  on  p.  31. 

4  i.'A/^eito— Graber  (1883)  ;    PeW;j7aneta— Brecher  ( 1929). 

^  The  larvsG  of  the  meal-worm,  Tenebrio — Tucoleseo  (1933). 

M      erpillars— Lammert    (1925),    Suffert    (1932),  Oehmig  (1939). 

'    p.    HtJ, 


See   especially 


THE   GENESIS   OF   THE   EYE 


115 


Specialization,  however,  occurred  at  a  very  early  stage,  for  some 
degree  of  a  localization  of  the  sensitivity  to  light  is  seen  even  among 
Protozoa.  The  most  elementary  expression  of  this  advance  is  the 
accentuation  of  photosensitivity  in  one  part  of  the  cell,  and  since  the 
early  response  to  the  stimulation  of  light  was  motorial,  this  occurred 
particularly  in  the  anterior  part  of  the  organism  or  in  close  association 
with  the  organs  of  locomotion,  as  is  seen  in  the  eye-spots  of  Flagellates 
and  Ciliates  ;  an  appreciation  of  directional  activity  was  thereby 
gained.  When  unicellular  organisms  developed  into  multicellular, 
however,  the  subdivision  into  cells  gave  the  opportunity  for  more 
intense  specialization,  and  out  of  the  generalized  dermal  sensitivity, 
specific  integumentary  liglitsensitive  cells  were  evolved  ;  these  again 
tended  to  accumulate  in  localities  where  the  recejition  of  stimuli  was 
of  most  biological  value — towards  the  head-end  of  the  animal,  as  in 
annelid  worms,  or  in  association  with  the  motile  organs  such  as  the 
tentacles  of  Coslenterates,  or  the  siphon  or  mantle  of  Molluscs. 

Such  a  single  cell,  however,  although  able  to  appreciate  the 
presence  of  light,  is  unable  to  form  images  ;  for  this  purpose  a  number 
of  photosensitive  cells  must  be  aggregated  together  to  form  an  "  organ". 
The  most  primitive  organ  of  this  type  is  composed  of  a  simple  colony 
of  independent  cells  without  functional  relationship — the  simple  eye  or 
ocellus — and  eventually  such  a  grouj^ing  of  cells  became  structurally 
and  functionally  related  in  the  compound  eye  ;  in  either  case  the 
receptor  cells  were  usually  provided  with  a  focusing  arrangement  to 
concentrate  the  light  and  a  j^igment  mantle  to  absorb  any  excess.  In 
this  way  eyes  are  found  in  some  polychsete  worms  and  higher  Inverte- 
brates which  from  the  anatomical  point  of  view  can  form  the  basis  of 
vision  of  varying  degrees  of  sensitivity  and  resolution. 

Throughout  Invertebrates  there  is  therefore  a  wide  range  of 
photoreceptor  mechanisms  ;  they  have,  however,  one  thing  in  common 
— that  in  contradistinction  to  the  "  cerebral  eye  "  of  Vertebrates,  which 
is  essentially  of  one  general  type  and  is  developed  from  the  neural 
ectoderm,  with  few  exceptions  (e.g.,  Rotifera)  they  are  all  derived  from 
the  surface  epithelium.  It  is  to  be  remembered,  however,  that  in  some 
Invertebrates,  in  addition  to  the  integument  and  its  derivatives, 
portions  of  the  central  nervous  system  appear  to  be  light-sensitive. 
This  api^lies,  for  examj)le,  to  the  sixth  abdominal  ganglion  of  the 
crayfish  (Prosser,  1934)  ;  in  the  eyeless  white  cave  crayfish,  Cambarus 
ayersii.  Wells  (1952)  found  that  stimulation  of  the  cerebral  ganglion  by 
light  results  in  an  increased  kinesis  without  the  suggestion  of  a  visual 
sense.  This  is  analogous  to  the  light -sensitivity  of  portions  of  the 
central  nervous  system,  particularly  of  the  ependymal  cells,  of  some 
Vertebrates,^  and  the  gonadotrophic  action  of  light  on  the  hypothalamus 
of  some  birds  such  as  the  duck  ^  (Benoit  et  al.,  1952). 


Drosoph  ila 


Rotifer 


p.  537. 


p.  559. 


116  THE    EYE   IN    EVOLUTION 

It  is  interesting  that  to  a  certain  extent  "  photoreceptors  "  may  be  seen  in 
the  vegetable  world  with  an  appropriate  structural  differentiation.  Some  plant 
cells,  for  example,  may  be  raised  up  and  rendered  more  convex  with  a  lens-like 
thickening  of  the  cuticle  so  that  they  may  collect  and  concentrate  the  light 
more  easily  on  the  chloroplasts  underneath  (Haberlandt,  1901)  (Fig.  76). 
This  forms  a  receptor  organ  comparable  to  that  seen  in  many  animals — a  veritable 
eye. 

The  range  of  photoreceptive  mechanisms  seen  in  Invertebrates  is 
wide,  and  far  exceeds  in  its  complexity  the  degree  of  vision  which  has 
hitherto  been  functionally  demonstrated  in  many  species,  but  at  the 
same  time  it  is  probably  legitimate  to  correlate  function  with  structure 
to  some  extent.    In  the  Protozoa  we  presumably  have  merely  a  common 

irritability,  from  which  we  may 
deduce  a  sentiency  without  specific 
characteristics.^  With  the  appearance 
of  multicellular  animals  specialization 
became  possible  so  that  some  of  the 
cells  in  the  outer  layer  could  acquire 
a  specific  response  to  various  types  of 
stimuli.   When  the  receptors  thus  be- 

FiG.   76.— Protonema  of  Schlstosteua  ,         ,         n         i-rv.  j  ■    i     ^      -i 

otiMusDACEA.  camc   structurally   dirierentiated,  it 

The  feeble  light  available  in   the     may  be  assumed  that  a  correspond- 

habitat  of  the  plant  is  concentrated  by     j^g   differentiation   in   function   be- 

the  lens-shaped  cells  upon  the  chloro-  "  -i  i  -n 

plasts  underneath.  came  possible.     Four  mam  groups  or 

modalities  appeared  —  mechano-, 
chemo-,  thermo-  and  radio -receptors  ;  of  these  the  first  was  probably 
the  most  fundamental,  but  the  last,  although  originally  the  least  im- 
portant, in  subsequent  evolution  has  far  transcended  the  others  by 
virtue  of  its  greater  potentialities  in  being  able  to  project  itself,  as  it 
were,  into  the  distance.  The  development  of  "  distance  "  receptors  and 
of  the  projicient  senses  is  late. 

Indeed,  it  has  been  suggested  that  radio -receptors  only  acquired  their 
attributes  as  distance-receptors  secondarily  and  that  appreciation  of  light  and 
darkness  originated  in  a  ^ahotoreceptor  sensitive  to  a  photochemical  change  in 
a  substance  with  which  it  was  in  contact.  The  sea  anemone  appears  to  possess 
I)hotoreceptors  of  this  simple  kind  (von  Uexkiill,  1909),  and  a  similar  faculty  is 
present  in  the  skin  of  the  ammocoete  larva  of  the  lamprey  (Parker,  1903-5)  and 
in  numerous  Amphibians  (Nagel,  1896). 

This  tendency,  of  course,  is  not  confined  to  vision,  l^he  touch-spots  of  the 
skin  have  been  projected  in  certain  Carnivora  to  the  tips  of  vibrissae  so  that 
exploration  of  the  immediate  environment  is  rendered  more  easy,^  while  the 
glorified  mechano -receptoi's  of  the  organs  of  Corti  respond  to  vibrations  from  a 
wide  ;: ;  ea  in  space  of  an  amplitude  considerably  less  than  the  diaineter  of  the 
hydrog    >  atom  (von  Bekesy  and  Rosenblith,   1951).     Similarly,  the  heat-spots 

1  p.  36. 

-   For  a  general  study,  see  Fitzgerald  (1940). 


Ammocoete  larva 
of  lamprey 


THE   GENESIS   OF   THE   EYE 


117 


of  the  skin  become  prtijected  in  the  temperature  receptors  seen  in  vipers  in  which 
a  facial  pit -like  "  eye  "  has  developed  for  the  reception  of  infra-red  radiation 
(Bullock  et  al.,  1952-56).^  The  eye,  of  course,  has  transcended  all  other  organs 
in  this  respect,  projecting  itself  to  astronomical  distances  and  responding  to  a 
few  qvianta  of  luminous  energy. 

Originally  it  is  probable  that  within  the  main  groups,  or  modalities, 
appreciation  was  relatively  undifferentiated  ^  ;  for  example,  a  usual 
accompaniment  of  the  radio -receptors  is  an  absorbing  pigment,  and  it 
is  possible  that  the  early  pigmented  cell  responded  to  thermal  energy  as 
well  as  to  luminous  radiation.  Subsequent  evolution,  both  in  the  receptors 
and  in  their  cerebral  connections,  determined  not  only  an  increase  in 
the  number  of  modalities  (touch,  temperature,  smell,  sight,  hearing) 
but  eventually  led  to  the  differentiation  of  various  individual  receptors 
within  the  same  modality,  thus  allowing  the  emergence  of  qualities 
within  a  modality,  such  as  colour  within  the  modality  of  sight. 


PIGMENTS 

PIGMENT  is  a  common  feature  of  photoreceptors  of  all  tyjDcs  ; 
indeed,  Bernard  (1S97)  suggested  that  light-sensitive  cells  first  arose  as 
modifications  of  the  epidermis  induced  by  crowding  of  pigment  granules 
in  situations  which  were  most  frequently  and  brilliantly  illuminated. 
The  physical  energy  of  light  can  be  converted  into  physiological 
activity  only  in  so  far  as  it  is  absorbed,  and  the  primary  function  of 
the  deposition  of  pigment  in  the  neighbourhood  of  light-sensitive 
areas  is  to  serve  as  an  absorbing  agent  ;  a  further  development  is 
the  initiation  of  a  specific  photochemical  reaction. 

In  its  simplest  form,  pigment  may  aid  the  general  dermal  sensitivity 
to  light,  a  function  well  illustrated  in  Echinoderms.  Thus  the  entire 
surface  of  the  sea-cucumber,  Holothuria,  is  photosensitive  and  is 
coloured  by  two  greenish-yellow  pigments  ;  the  reaction  of  the  animal 
varies  with  the  amount  of  pigment  present,  for  young  and  lightly 
pigmented  individuals  are  poorly  light-sensitive  while  heavily  pig- 
mented adults  are  markedly  so  (Crozier,  1914-15).  Again,  the  sea- 
urchin,  Centrostephanus  Joricjisinnus.  shows  a  high  light-sensitivity  in 
the  violet  spicules  around  the  anal  orifice  whence  a  purple  pigment  can 
be  extracted  (von  Uexkiill.  1900) — an  early  example,  incidentally,  of  the 
frequent  aggregation  of  sensory  organs  around  the  body  orifices. 
When,  however,  specific  light-sensitive  organs  are  developed,  pigment 
is  concentrated  in  tlieir  vicinity — melanin  as  an  absorbent  and 
visual  pigments  as  sensitizers.  All  these  pigments  are  synthesized 
by  special  cells  called  ciiromatoblasts  {xpojyt-y..  colour  ;  ^Xxaros,  a 
sprout). 

1  See  further,  p.  600  «  p.  109. 


Holothuria 


Cetitrostephanus    ^- 


118  THE   EYE   IN   EVOLUTION 

MELANIN 

MELANIN  (jLte'Aas-,  black)  is  the  common  dark  brown  pigment  ;  it 
is  elaborated  locally  by  the  organism  from  a  colourless  precursor  found 
in  the  nucleus  of  special  cells  (melanoblasts).  Very  inert  chemically, 
it  acts  merely  as  an  absorbing  agent. 

Melanin  is  a  close  relative  of  adrenalin  and  was  originally  thought  to  be 
derived  from  the  blood  (Scherl,  1893  ;  Ehrmann,  1896  ;  Augstein,  1912),  but  at 
an  early  date  it  was  shown  to  have  nothing  in  common  with  the  derivatives  of 
haemoglobin.  A  cellular  origin  therefore  being  necessitated,  Kromayer  (1893)  and 
Hertwig  (1904)  suggested  that  it  was  derived  from  the  nucleus,  and  Meirowsky 
(1906)  narrowed  this  down  to  the  nucleolus  owing  to  the  demonstration  of  large 
quantities  of  pyronin  (a  nuclear  constituent)  in  melanotic  cells,  a  view  which 
appeared  to  be  substantiated  by  the  finding  of  this  material  in  melanotic  tumours 
by  Rossle  (1904).  A  further  advance  was  made  by  von  Szily  (1911)  who  showed 
that  the  pigment  was  formed  from  a  colourless  precursor  by  the  action  of  a 
ferment.  Masson  (1913)  established  that  the  action  was  oxidative  in  nature,  and 
Bloch  (1917)  cleared  up  the  matter  by  demonstrating  that  the  cells  of  pigmented 
regions  contain  a  specific  intracellular  oxidase.  Bloch  then  isolated  from  the 
embryo  of  the  broad  bean  3-4-dihydroxyphenylalanine,  a  substance  which  he 
conveniently  called  "dopa",  and  showed  that  it  was  readily  changed 
by  this  oxidase  to  melanin.  When  this  svibstance  is  added  to  the  epidermal 
cells  of  skin  in  frozen  forn^alin-fixed  sections,  granules  of  melanin  are  formed 
(the  "  dopa  reaction  ").  A  large  nvunber  of  the  groupings  in  the  protein  molecule 
form  coloured  products  on  oxidation  (tyrosine,  jDhenylalanine,  tryptophane, 
etc.),  and  it  seems  obvious  that  melanin,  like  adrenalin,  is  formed  as  an  end- 
product  from  one  of  these  chromatogen  groups.  Bloch  concluded  that  the 
colourless  "  mother  substance  "  (or  melanogen)  is  almost  certainly  either 
identical  with  or  related  to  "  dopa  "  ;  this  colourless  substance  is  brovight  by 
the  blood-stream  to  the  cell  ;  here  it  meets  the  "  dopa-oxidase  "  and  thus  is 
turned  into  the  coloured  pigment  melanin. 

THE    VISUAL   PIGMENTS 

Photochemical  and  sensitizing  reactions  in  both  plants  and  animals, 
both  phototactic  and  visual,  depend  almost  universally  upon  one 
distinctive  and  compact  group  of  substances,  the  carotenoids — a 
striking  indication  of  the  close  evolutionary  relationship  between 
phototropism  and  vision.  These  form  a  number  of  pigments  varying 
in  colour  from  red  to  yellow,  fat-soluble  and  highly  unsaturated, 
occurring  alone  or  as  the  prosthetic  groups  of  proteins  ;  all  of  them 
seem  to  be  related  to  the  chromophore  moiety  of  visual  purple  and 
are  identifiable  by  their  absorption  spectra,  the  maxima  of  which  usually 
lie  somewhere  towards  the  blue  side  of  the  mid-region  of  the  visible 
band.  As  we  have  seen  in  a  previous  chapter  ^  they  also  have  a  wide 
integumentary  distribution  among  many  species  where  they  may 
play  a  dnr  atic  part  in  the  coloration  of  the  animal.  Their  high 
concentrati;  1  in  the  sex-glands  (the  interstitial  cells  of  the  gonads,  the 

1  p.  87. 


PHOTOPIGMENTS 


119 


adrenal  and  renal  cortex)  is  a  further  point  of  association  between 
the  action  of  hght  and  sexual  activities  ^  (Goodwin,  1950). 

In  the  vegetable  kingdom  the  predominant  carotenoids  are 
j3-CAR0TENE,  C40H56,  and  XANTHOPHYLL,  C4oH54(OH)2 — jellow  pig- 
ments absorbing  preferentially  blue  light  with  absorption  spectra  quite 
diflferent  from  that  of  chlorophyll.  The  latter  and  its  relatives  are  active 
in  the  photosynthesis  of  plant  metabolism  and  have  no  effect  upon 
phototropic  responses  ;  the  former  and  its  derivatives  are  concerned  in 
photoreception  in  systems  mediating  orientation  to  light,  they  are 
pecuharly  susceptible  to  the  blue  end  of  the  spectrum,  and  are  found 
only  in  the  photosensitive  parts  of  plants,  such  as  the  oat  coleoptile 


10 

z 
0 

0  8 

06 

2 

\~- 

04- 

X 

LU 

02 

0 

—t Y — 

A 

^»s 


400 


500 


Way/zlenqt'h  ~mu. 


100 

80 

60 

40 

20 

0 


c 


Fig.  77. — Spectral  Sensitivity  of  the  Phototropic  Bending  of  Plants, 
AND  THE  Absorption  Spectra  of  the  Associated  Carotenoids. 

Absorption  spectrum  (extinction)  of  the  total  carotenoids  of  the  etiolated 
oat  coleoptile,  Avena  ;  continuous  line  (after  Wald).  Relative  spectral  sensi- 
tivity of  the  oat  shoot  ;   broken  line  (after  Johnston). 


(Voerkel,  1933  ;  Castle,  1935  ;  Biinning,  1937  ;  Wald,  1943).  Wald 
(1945-46)  brought  out  this  relationship  dramatically  by  a  study  of  the 
absorption  characteristics  of  the  phototropic  response  ;  he  found  that 
the  active  spectrum  of  the  phototropic  bending  of  the  seedling  of  the 
oat,  Avena,  was  maximal  in  a  blue  light  of  440  m/x  and  corresponded 
very  closely  with  the  absorption  spectrum  of  the  carotenoids  extracted 
from  the  coleoptile  (Fig.  77). 

The  phototactic  movements  of  animals,  so  far  as  they  have  been 
investigated,  are  also  determined  by  carotenoids  but  in  these  the  single 
maxima  of  absorption  are  disjDlaced  to  wave-lengths  considerably  longer 
than  those  associated  with  the  phototropic  bending  of  plants  (473  to 
534  niju)  (Mast,  1917  ;  Laurens  and  Hooker,  1920  ;  Luntz,  1931).  The 
pigment  responsi])le  for  phototactic  activity  in  a  number  of  the  green 

1  p.  16, 


120 


THE   EYE   IN   EVOLUTION 


Flagellates  {Eucjlena,  etc.)  has  been  identified  as  astaxanthin  (di- 
hydroxy  di-keto  /3-carotene,  C40H52O4)  (Tischer,  1936-38;  Kiihn  et  al., 
1939)  ;  this  pigment  is  found  only  in  animal  tissues,  is  produced  by 
the  modification  of  ingested  plant  carotenoids,  and,  depending  on  its 
chemical  nature,  may  range  in  colour  from  blue  to  red  with  varying 
characteristics  of  absorption.  The  pigments  associated  with  the 
photoreceptors  of  the  lower  Invertebrates  have  not  been  fully  investi- 
gated, but  the  available  evidence  indicates  that  the  phototropic 
responses  of  the  polyps  of  Coelenterates  ^  and  the  siphons  of  clams, ^  as 
well  as  the  phototactic  activity  of  worms, ^  are  also  mediated  by 
pigments  of  the  astaxanthin  type  (Fig.  78). 

On  the   other   hand,    when  image -forming  eyes   are   reached   in 


Z 

o 
^ 

X 

UJ 


10 
08 
0  6 
04- 
0-2 
0 


■^^^'si^ — 


100 

80 
60 
40 
20 
0 


400 


500 


600 


Wave/enohh  -mu 


Fig.    78. — Spectral   Sensitivity   for  Photo-orientation   of  the   Green 

Flagellate. 

Absorption  spectrum  (extinction)  for  astaxanthin  dissolved  in  hexane  ; 
continuous  line  (after  Wald).  Relative  spectral  sensitivity  of  Euglena  viridis  ; 
broken  line  (after  Mast). 


Molluscs  and  Arthropods,  the  power  has  been  gained  to  degrade 
vegetable  carotenoids  into  the  vitamin  A  system.  Thus  among 
Molluscs,  the  retina  of  the  squid,  Lolicjo  pealii,  has  been  found  to  have 
considerable  quantities  of  retinene^  and  vitamin  A^  which,  combined 
with  a  specific  protein,  produces  a  pigment  with  absorptive  charac- 
teristics resembling  those  of  rhodopsin  (Wald,  1941  ;  Bliss,  1943-48  ; 
St.  George  and  Wald,  1949  ;  Hubbard  and  St.  George,  1956).  It 
would  appear  that  in  the  squid  this  reddish  photopigment  is  a  non- 
photosensitive  type  of  rhodopsin,  for  which  reason  it  was  distinguished 
as  cephdiopsin  b}^  its  discoverer  (Bliss,  1948). 

^  Hydioids  of  Sertularia  and  Eudendriuw ,  maximum  absorption  474  m/u,  Loeb 
and  Wasteiii  -s  (1915). 

^  Mya.  iximum  absorption  490  ni/it,  PJiolas,  maximum  absorption  555  m/x, 
Hecht  (191; 

*  The  eji  i  irm,  Lumhricus  lerrestris,  and  the  larva?  of  the  marine  worm,  Arenicola, 

maximum  abs.        ion  483  m/i.  Mast  (1917). 


PHOTOPIGMENTS 


121 


Vitamin  A^  has  also  been  isolated  in  quantity  from  the  eyes  of  a 
number  of  marine  Crustaceans,^  and  the  occurrence  of  this  photo- 
chemical system  in  the  eyes  of  the  king-crab,  Limidus,  and  of  Insects 
has  been  corroborated  by  studies  of  their  spectral  sensitivity  (Graham 
and  Hartline,  1935  ;  Jahn,  1946  ;  Granit,  1947  ;  Jahn  and  Wulff, 
1948  ;  and  others)  and  also  by  behavioural  experiments  (Weiss,  1943). 
It  is  evident  that  more  than  one  ty^e  of  pigment  exists  belonging  to 
the  vitamin  A^  family  ;  thus  among  the  shrimp-like  euphausiid 
Crustaceans,  Kampa  (1955)  isolated  a  pigment  [Euj^hausiojisin)  ^  with 
a  maximum  absorption  of  462  m/x,  and  in  the  deep-sea  pra-wn,  Pandalus, 
an  isomer  was  detected  by  Lambertsen  and  Braekkan  (1955),  It  is 
true  that  in  some  of  these  organisms  astaxanthin  may  also  be  found  ^ 


MO 
Wavelength -ny^ 


Fig.  79. — Spectra  of  the  Rhodopsin  and  Porphyropsin'  Systems 
Direct  spectra  of  crude  preparations  from  the  retinae  of  the  marine  scup 
(broken  hnes)  and  the  freshwater  cahco  bass  (continuous  lines).  Rhodopsin 
and  porphyropsin  are  dissolved  in  1  per  cent,  aqueous  digitonin  solution,  the 
retinenes  and  vitamins  A  in  chloroform.  All  maxima  have  been  brought  to 
the  same  height  to  facilitate  comparison  (Wald). 


but  this  pigment  appears  to  take  no  part  in  the  visual  process  and  is 
also  distributed  throughout  the  integument  (Wald,  1941-46). 

Among  Vertebrates  the  primitive  Cyclostomes  still  retain  the 
vitamin  A^  system  (visual  jDurple)  (Steven,  1955)  associated  with  their 
retinal  rods,  as  also  does  the  majority  of  marine  fishes  ^  so  far  examined  ; 
on  the  other  hand,  most  fresh-water  fishes  ^  possess  a  different 
svstem  based  on  vitamin  Ao  and  retinenco.    In  Amphibians  and  hioher 

1  Crabs,  lobsters  and  others,  Wald  (194.5-46),  Fisher  et  al.  (1952-5.5). 

^  Possibly  related  to  or  identical  with  the  pigment  absorbing  maximally  at  467  m/x 
described  by  Dartnall  (1952)  in  the  tench. 

^  As  in  the  fresh-water  crayfi.sh,  Caniharus  virilis  ;  the  shrimp,  Aristeomorpha, 
Grangaud  and  INIassonet  (1950). 

^  Exceptions  are  found,  for  example,  among  the  wrasse  fishes  {Labrus  bergylta  and 
Tautoga  onitis),  the  eves  of  which  have  a  pigment  based  on  the  vitamin  Aj  svstem 
(Bayliss  et  al.,  1936  ;    Dartnall,  1955). 

*  An  exception  is  the  fresh-water  bleak,  Alburr^us  lucidiis,  which  has,  in  addition 
to  two  pigments  based  on  vitamin  A,,  another  probably  ba.sed  on  Aj  (Dartnall,  1955). 
It  is  to  be  remembered,  however,  that  only  a  few  species  have  hitherto  been  examined 
so  that  further  iii\estigation  may  weaken  this  generalization. 


122  THE   EYE   IN   EVOLUTION 

forms  in  the  vertebrate  phylum  the  vitamin  A^  system  is  again 
encountered.  Wald  (1939-56)  considered  that  two  specific  pigments 
were  concerned — rhodopsin  (visual  purple)  with  the  vitamin  A^ 
system  and  porphyropsin  (visual  violet)  with  the  vitamin  A 2  system 
(Fig.  79).  Evidence  is  rapidly  accumulating,  however,  that  the  matter 
is  not  so  simple,  for  it  would  appear  that  each  of  these  does  not  repre- 
sent a  single  specific  pigment  ;  both  vitamins  Aj  and  A 2  can  exist  as  a 
number  of  isomers  some  of  which  combine  with  suitable  proteins  to  yield 
photosensitive  pigments  of  distinctive  absorptive  properties,  several  of 
which  have  already  been  discovered.  Rhodopsin  should  therefore  be 
interpreted  as  a  generic  name  for  all  visual  pigments  associated  with  the 
rods  based  on  vitamin  A^,  while  porphyropsin  is  best  similarly 
interpreted  as  embracing  several  rod -pigments  based  on  vitamin  A  2 
(see  Dartnall,  1957). 

The  photosensitive  pigments  so  far  claimed — although  with  little 
substantial  evidence — to  be  present  in  vertebrate  cones — iodopsin 
associated  with  the  vitamin  Aj  system  and  cyanopsin  associated 
with  vitamin  A 2 — are  also  related  carotenoid-proteins  (Wald,  1937-55  ; 
Bliss,  1946)  ^  ;  on  the  other  hand,  accessory  needs  in  the  visual 
system  such  as  the  yellow  pigment  of  the  human  macula  are  said  to 
be  met  by  xanthophyll — the  intact  carotenoid  which  mediates  photo- 
reception  in  plants. 

The  multiplicity  of  pigments  of  these  two  general  types  associated  with  the 
visual  system  is  becoming  increasingly  apparent,  and  odd  varieties  have  been 
discovered  in  special  circumstances,  differing  considerably  from  the  main  groups. 
As  we  have  seen,  fresh -water  fish  usually  have  a  pigment  of  the  porphyropsin 
family,  salt-water  fish  of  the  rhodopsin  family  ;  euryhaline  and  migratory 
fishes  which  adapt  themselves  to  both  fresh  and  salt  water  therefore  present  an 
interesting  problem.  Since  their  spectral  absorption  curve  is  intermediate 
between  that  of  rhodopsin  and  porphyropsin,  Wald  (1941)  concluded  that 
their  retinae  contained  a  mixture  of  both  ;  but  it  has  been  shown  by  Munz 
(1956)  that  in  one  at  least  of  these  fishes  (the  mud-sucker,  Qillichthys  mirahilis) 
the  retina  contains  a  single  homogeneous  pigment  characteristic  of  the  retinene^ 
type  with  an  absorption  maximum  intermediate  between  the  two  main  groups 
(512m!JL).  Again,  the  gecko  (Gekko  gekko)  has  an  unusual  spectral  sensitivity 
curve,  similar  to  the  human  scotopic  curve  but  with  its  maximum  displaced 
20  to  SOmji,  towards  the  red  end  of  the  spectrum  (Denton,  1956).  Retinal 
extracts  from  the  Australian  gecko,  Phyllurus  milii,  have  shown  the  presence 
of  an  unusual  pigment  with  an  absorption  maximum  at  524m(ji,  typical  of  the 
retinene^  system  but  intermediate  between  the  rhodopsin  of  the  rods  and  the 
iodopsin  of  the  cones  (Crescitelli,  1956).  This  is  interesting  in  view  of  the  theory 
that  the  rods  of  this  nocturnal  animal  may  be  transmutations  from  the  cones 
of  ancestr  i  cUurnal  lizards.^ 

Pigments  of  unknown  composition  and  tinknown  function  which  appear, 

^  In  tilt  -es  of  primates  three  pigments  have  been  detected:  chlorolabe  (a  green- 
absorbing  ]i  nt),  erythrolabe  (red-absorbing),  and  cyanolabe  (blue-absorbing).  See 
Vol.  IV,  p.  4 

2  p.  252. 


PHOTOPIGMENTS  123 

however,  to  differ  from  the  preceding,  have  been  found  in  the  eyes  and  also  in  the 
integument  of  Arthropods  among  which  they  appear  to  have  a  wide  distribution. 
They  have  been  most  fully  studied  in  the  eyes  and  integument  of  Insects  and  were 
first  cursorily  examined  by  Chauvin  (1938-41).  Becker  (1939-41),  studying  these 
pigments  in  the  ommatidia  of  a  number  of  insect  sjaecies,  gave  them  the  generic 
term  ommochromes  and  subdivided  them  into  ommins  and  ommatins.  In 
certain  insects,  such  as  the  fruit-fly,  Drosophila,  for  example,  he  described  a 
purplish-red  pigment  (erythrommatin)  and  a  yellowish-brown  (phgeommatin). 
During  pupal  development  the  brown  pigment  appears  first  and  the  red  later, 
their  appearance  being  determined  by  hormones,  and  one  or  other  or  both  of 
the  pigments  may  be  absent  in  certain  stocks,  the  eyes  appearing  respectively 
brown,  red  or  white, ^  At  a  later  date,  however,  Goodwin  and  Srisukh  (1950) 
and  Goodwin  (1950),  working  on  locusts  (the  desert  locust,  Schistocerca  gregaria, 
and  the  African  migratory  locust,  Locusta  migratoria),  concluded  that  these 
pigments  represented  a  redox  complex,  yellow  when  oxidized  and  wine-red  when 
reduced.  For  this  variable  pigment,  or  group  of  very  closely  related  pigments 
which  are  at  the  moment  indistinguishable,  they  suggested  the  name  insecto- 
BUBIN,  in  view  of  its  widespread  distribution  among  insects.  Whatever  its 
chemical  nature,  it  is  very  resistant  to  chemical  attack,  bat  has  been  isolated 
as  a  reddish-brown  powder  which  quickly  changes  into  a  stable  dark  brown 
powder  reminiscent  of  melanin,  and  shows  characteristic  absorption  spectra 
differing  according  to  the  method  of  extraction,  whether  measured  in  the  fresh 
extract  or  in  tlie  reduced  or  oxidized  forni. 

Related  pigments  with  similar  absorption  curves  have  been  described  in 
crustaceans  (the  shrimps,  Leander  and  Crangon — Polonovski  et  al.,  1948  ;  the 
fresh-water  Amphipod,  Oammarus  pulex — Michel  and  Anders,  1954). 

Such  is  the  general  evolutionary  story  of  the  photopigments  ;  it  is  a  large 
subject  which  will  be  discussed  more  fully  when  we  deal  with  the  physiology  of 
vision  in  a  subsequent  volume.  In  passing,  however,  it  is  interesting  to  note 
that  many  years  ago  Patten  (1886)  put  forward  the  theory  that  photoreceptors 
were  originally  evolved,  not  as  sentient  organs,  but  as  receptors  of  light-energy 
for  metabolic  purposes  as  occurs  in  plants.  He  called  them  heliophags.  The 
theory,  however,  in  its  time  raised  a  storm  of  criticism  and  never  received 
credence  ;  the  most  cogent  evidence  against  it  is  the  completely  different 
chemical  nature  of  chlorophyll  and  the  carotenoids  and  the  contrast  in  their 
functions — metabolism  on  the  one  hand,  and  photoreception  or  integumentary 
coloration  on  the  other. 

Augstein.     Klin.  Mbl.  Augeuhcilk.,  50  (1),  Bernard.      Quart.   J.    micr.   Sci.,    39,    343 

1  (1912).  (1897). 

Bayliss,  Lythgoe  and  Tansley.    Proc.  roy.  Bliss.    J.  gen.  Fhysiol.,26,^Ql  (l9iS)  ;   29, 

Soc.  B,  120,  95  (1936).  277  (1946). 

Beadle.     Gene^/cs,  22,  587  (1937).  J.    biol.    Chcm.,    172,    165;     176,    563 

Beadle   and   Ephrussi.      Genetics,  21,    225  (1948). 

(1936).  Bloch.     Hoppe  Seyl.  Z.  physiol.  Chem.,  9S, 

Becker.     Biol.  Zbl.,  59,  597  (1939).  226  (1916-17). 

Naturwissenschaften,  29,  237  (1941).  Bohn.      Actions  directrices  de  la  lumiere, 

v.     Bekesy    and    Kosenblith.       Hb.     e.vp.  Paris  (1940). 

Psychol.  (Stevens),  1075  (1951).  Braim   and   Faust.      E.vperientia,   10,   504 

Benoit,  Assenmacher  and  Manuel.     C.  R.  (1954). 

Acad.  Sci.  (Paris),  235,  1695  (1952).  Brecher.    Z.  vergl.  Physiol.,  10,  497  (1929). 

1  See  Beadle  and  Ephrussi  (1936),  Beadle  (1937),  Ephrussi  and  Beadle  (1937), 
Mainx  (1938),  Ephrussi  (1942),  Ephrussi  and  Herold  (1944),  Wald  and  Allen  (1946), 
Villee  (1947),  Maas  (1948),  Okay  (1948),  Nolte  (1954). 


124 


THE   EYE   IX   EVOLUTION 


Bullock   and   Cowles.     Science,   115,    541 

(1952). 
Bullock  and  Diecke.    J.  Physiol.,  134,  47 

(1956). 
Bullock  and  Faulstick.    Fed.  Proc.  12,  22 

(1953). 
Biinning.    Plaixta  (Bed.),  26,  148,  583,  719 

(1937). 
Castle.      Cold   Spr.    Harb.    Symp.    quant. 

Biol.,Z,  224  (1935). 
Chauvin.     C.  R.  Acad.  Sci.  (Paris),  207, 
1018  (1938). 
Ann. Soc.etUom.  France.  110,  133(1941). 
Bui  .  Soc.  zool.  France.  69,  154  (1944). 
Crescitelli.      J.    gen.     Physiol.,    40,     217 

(1956). 
Crozier.    Amer.  J.  Physiol.,  36,  8  (1914). 
Zool.  Jb.,  Abt.   Zool.   Physiol.,  35,  233 
(1915). 
Cuenot.    Arch.  Biol.  Paris.  11,  313  (1891). 
Dartnall.     J.   Physiol.,  116,   257   (1952)  ; 
128,  131  (1955). 
The  Visual  Pigments,  London  (1957). 
Denton.    J.  gen.  Physiol.,  40,  201  (1956). 
Dubois.    Ayin.  Unir.  Lyon,  2,  1  (1892). 
Ehrmann.     Bibl.  Med.,  2    (6)  (1896). 
Ephrussi.     Cold.  Spr.  Harb.  Sytnp.  quant. 

Biol.,  10,  40  (1942). 
Ephrussi   and   Beadle.      Genetics,   22,    65 

(1937). 
Ephrussi  and  Herold.     Genetics,  29,   148 

(1944). 
Fisher,  Kon  and  Thompson.     J.   marine 
Biol.  Ass.  Soc,  31,  229  (1952)  ;    33, 
589  (1954)  ;   34,  81  (1955). 
Fitzgerald.    J.  Physiol..  98,  163  (1940). 
Folger.    J.  Morphol.,  42,  359  (1926). 

Biol.  Bull.,  53,  405  (1927). 
Goodwin.     Biochem.  J.,  47,  554  (1950). 

Biol.  Rev.,  2b,  391  (1950). 
Goodwin  and  Srisukh.     Biochem.  J.,  45, 

263  (1949)  ;   47,  549  (1950). 
Graber.    S.  B.  Akad.  Wiss.  Wien..  Abt.  1, 
87,  201  (1883). 
Grundlinien  zur  Erforschung  des  Hellig- 
keits-    und    Farbensinnes    der    Tiere, 
Leipzig  (1884). 
Graham  and  Hartline.    J.  gen.  Physiol.,  18, 

917  (1935). 
Grangaud  and  Massonet.    C.  R.  Acad.  Sci. 

(Paris),  230,  1319  (1950). 
Granit.       Sensory     Mechanisms     of     the 

Retina,  Oxford  (1947). 
Haberlandt.     Ber.  dtsch.  botan.  Ges.,  569 

(1901). 
Hecht.    J.  gen.  Physiol.,  1,  545,  657,  667 
(1919)  ;  2,  229,  337  (1920)  ;  3,  1,  285, 
375  (1921)  ;   6,  731   (1924)  ;    11,  657 
(1928) 
Physiol.  Rev.,  17,  239  (1937). 
Hertwig.     Fe.stschr.  f.  Haeckel  ( 1 904). 
Hubbard  aii!  St.  George.    Fed.  Proc,  15, 

277  (HC 
Jahn.    J.  y.  •;     ^«/ow.  .Soc,  54,  1  (1946). 
Jahn  and  \\  .J.  X.Y.  entom.  Soc,  56, 

109  (194- 


Kampa.    Nature  (Lond.).  175.  996  (1955). 
Knoop.     Z.  Beitr.,  1,  219  (1954). 
Kromaver.      Arch.    mikr.    Anat.,    42,     1 

(1893). 
Kuhn.   Stene  and  Sorensen.      Ber.  dtsch. 

chem.  Ges.,  72,  1688  (1939). 
Lambert  sen     and     Braekkan.  Nature 

(Lond.),  176,  553  (1955). 
Lammert.    Z.vergl.  Physiol. ,2,  225  (1925). 
Laurens  and  Hooker.  J.  exp.  Zool..  30,  345 

(1920). 
Loeb  and  Wastenevs.    J .  exp.  Zool.,  19,  23 

(1915). 
Luntz.     Z.  vergl.  Physiol.,  14,  68  (1931). 
Maas.     Genetics,  33,  177  (1948). 
Mainx.    Z.    indukt.    Abstamm.  u.    Vererb- 

Ze/ire,  75,  256  (1938). 
Marchal.  Richet's  Dictionnaire  de  Physiol., 

9,  273  (1910). 
Masson.     C.  R.  Soc.  Biol.  (Paris),  75,  210 

(1913). 
Mast.    J.  exp.  Zool.  22,  471  (1917). 
J.  Morphol.,  41,  347  (1926). 
Protoplasma,   8,    344    (1929)  ;     14,    321 

(1931). 
Physiol.  Zool.,  5,  1  (1932). 
^leirowskv.    Mschr.  prakt.  Derm.,  42,  541  ; 

43,  155  (1906). 
IMichel  and  Anders.    Xaturwissenschafteri, 

41,  72  (1954). 
Millott.    Philos.  Tra72s.  B,  238,  187  (1954). 

Endeavour,  16,  19  (1957). 
Munz.     J.  gen.   Physiol.,  40,   233   (1956). 
Nagel.      Der   Lichtsinn   augenloser    Tiere, 

Jena  (1896). 
Newth   and   Ross.     J.   exp.    Biol.,   32,    4 

( 1955). 
Nolte.    J.  Genet.,  52,  111,  127  (1954). 
Oehmig.    Z.  vergl.  Physiol.,  27,  492  (1939). 
Okay.    Comm.  Fac.  Sci.,  Univ.  Ankara,  1, 

178  (1948). 
Pantin.    J.  marine  Biol.  Ass.  U.K.,  13,  24 

(1924). 
Brit.  J.  exp.  Biol,  1,  519  (1924)  ;  3,  275, 

297  (1926). 
Parker.    Amer.  J.  Physiol.,  10,  28  (1903)  ; 

14,  413  (1905). 
Patten.    Mitt.  zool.  Stat.  Xeapel,  6  (1886). 
Polonovski,  Busnel  and  Grundland.   C.  R. 

Acad.  Sci.  (Paris),  226,  2182  (1948). 
Prosser.     J.  cell.   comp.   Physiol.,  4,   363 

(1934). 
J.  comp.  Neurol.,  59,  61  (1934). 
Rossle.     Z.  Krebforsch.,  2,  291  (1904). 
St.   George,   Goldstone  and  Wald.      Fed. 

Proc,  11,  153  (1952).     ' 
St.  George  and  Wald.    Biol.  Bull.,  97,  248 

(1949). 
Scherl.     v.  Graefes  Arch.  Ophthal.,  39  (2), 

130  (1893). 
Schone.     Z.  vergl.  Physiol.,  33,  63  (1951). 
Steven.    .J.  exp.  Biol.,  32,  22  (1955). 
V.  Studnitz.    Pfliigers  Arch.  ges.  Physiol., 

243,  181  (1940). 
Siiffert.    Z.  Morphol.  Oekol.  Tiere,  26,  147 

(1932). 


INVERTEBRATE   EYES  125 

V.  Szily.    .-Irc/i. /mX-r.  .4nar,  77,  87  (1911).  J.   gen.    Physiol.,  22,   391,   775   (1939); 

Thines  and  Kahling.     Z.  Biol.,  109,   150  25,    235,    331     (1941-42)  ;     38,    623 

(1957).  (1955). 

Tischer.     Hoppe  Seyl.   Z.  physiol.  Chein.,  Ainer.  J.  Phy.siol.,  133,  419  {IMl). 

239,  257  (1936)  ;    252,  225  (1938).  Viia7nins  and  Hormones,  1,  195  (1943). 

Tucolesco.     Bull.  Biol.  Fr.  Belg.,  67,  480  Harvey  Lecture  Series,  i^l,  117(1945-46). 

(1933).  i^ed.  Proc,  12,  606  (1953). 

V.  Uexkiill.     Z.  BtoZ.,  34,  315  (1897)  ;   40,  .4/i/i.  i?er.  B^oc^em.,  22,  497  (1953). 

447  (1900).  Modern  Problems  in  Ophthalmology,    1 

Umwelt  u.  Innenwelt  der   Tiere,  Berlin  (Suppl.     Ophthalmologica,     47),     173 

(1909).  (1956). 

Viaud.     Experientia,  4,  81  (1948).  Wald  and  Allen.     J.  gen.  Physiol.,  30,  41 

Le  phototropisme  animal,  Paris  (1948).  (1946). 

Viaud    and    Medioni.      C.    R.    Soc.    Biol.  Weiss.      Entom.    News    (Phila.),    54,    152 

(Paris),  143,  1221  (1949).  (1943). 

Villee.    Genetics.32,  211  (1941).  Wells.    .4«a^  i?ec..  113,  613  (1952). 

Voerkel.     Planta  (Bed.),  21,   156  (1933).  WUlem.      Bull.   Sci.    Fr.    Belg.,    23,    329 

Wald.     Nature  (Lond.),   140,   545   (1937).  (1891). 

THE  STRUCTURE  OF  INVERTEBRATE  EYES 

We  are  now  in  a  position  to  study  the  various  types  of  photo- 
receptors found  among  Invertebrates.  In  unicelhdar  organisms  the 
diffuse  sensitivity  to  hght  evolves  into  the  locahzed  sensitivity  of  an 
"  eye-spot  "  ;  in  multiceHular  organisms  the  diffuse  dermal  sensitivity 
evolves  into  the  specialization  of  certain  epithelial  cells  as  specific 
photoreceptors. 

EYE-SPOTS  :     STIGMATA 

The  earliest  stage  in  the  evolution  of  an  eye  is  seen  in  unicellular 
organisms  in  which  a  small  area  of  the  protoplasm  is  differentiated  to 
become  specially  sensitive  to  light  ;  this  development  is  seen  in  actively 
motile  ciliate  and  flagellate  Protozoa,  and  since  in  these  organisms  light 
serves  not  as  a  visual  but  as  an  orientating  stimulus,  the  specialized 
area  is  always  in  close  association  ^viih  the  cilia  or  flagella.  Among 
Ciliates  such  specialization  is  primitive  ;  thus  without  observable 
structural  differentiation,  the  oral  surface  of  Stentor  coendeus  is  more 
photosensitive  than  the  aboral  so  that,  as  the  organism  rotates  while 
swimming,  successive  exjjosures  of  these  two  areas  determine  a  negative 
klinotaxis.  orientating  it  away  from  the  light  (Jennings,  1904  ;  Mast, 
1 906-1 1).^  In  Flagellates,  however,  a  degree  of  structural  differentia- 
tion appears  which  is  sufficient  to  dignify  the  organelle  thus  formed 
with  the  name  of  an  eye-spot  or  stigma  {ariyiJix,  a  spot)  ;  there  is  a 
light-sensitive  area,  a  mass  of  pigment  which  serves  to  make  the 
organelle  a  directional  detector  useful  in  phototaxis.  and  occasionally 
a  refractile  structure  wliich  serves  to  concentrate  the  light,  thus  acting 
as  a  lens.- 

The  stigma  of  tlie  common  green  protozoon  of  ponds,  Eugle?ia 

»  p.  49. 

-  As  occurs  in  the  Alg;p,  Cladophora  and  Gonium  (Mast,  1916). 


Stentor 


126 


THE   EYE   IN  EVOLUTION 


viridis,  is  of  the  simplest  variety  (Fig.  80)  ;  the  entire  structure  is 
about  5/x  in  diameter  (Franz,  1893).  The  base  of  the  single  flagellum 
shows  a  thickening  just  anterior  to  its  bifid  root  in  the  cavity  of  the 
reservoir  ;   it  would  seem  that  this  is  the  photoreceptive  area  and  it  is 


BLIND  SlD£ 


S£EIN0    SiD^ 


Fig.   80. — The  Eye-spot  of  Euglesa    viridis. 
A  side  view  of  the  anterior  end  of  the  flagellate.    /.  The  flagellum  with 
an  enlargement,  e/,  which  constitutes  the  photoreceptive  area.    The  two  roots 
of  the  flagellum  are  anchored  in  the  large  contractile  vacuole  {cv.).     Opposite 
the  sensitive  area  is  a  shield  of  pigment  (e)  (after  Wager,  1900). 

flanked  on  one  side  by  a  shield  of  the  red  carotenoid  pigment,  astaxan- 
thin  (Engelmann,  1882  ;  Wager,  1900  ;  Mast,  1911-38  ;  Buder,  1917  ; 
Tischer,  1936-38  ;  Kuhn  et  al.,  1939).  It  is  interesting  that  Ehrenberg 
(1838),  who  first  described  this  flagellate,  assumed  that  the  pigmented 
area  was  light-sensitive  and  considered  that  it  constituted  the  most 
primitive  eye  in  nature  and  called  it  the  eye-spot 
("  Augenfleck").  It  seems  more  probable,  however, 
that  it  serves  as  an  absorbing  agent,  shielding  the 
flagellar  swelling  from  incident  light  on  one  side  and 
allowing  it  to  be  exposed  on  the  other,  so  that  as 
the  organism  rotates  in  swimming,  the  alternating 
stimulation  and  shading  of  the  stigma  affect  the 
beat  of  the  flagellum  and  directional  phototaxis  is 
attained.^ 

The  instability  of  such  an  eye-spot  is  intei'esting.  The 
Pringsheims  (1952)  found  that  if  Euglena  gracilis  were 
grown  at  temperatures  below  the  optimuni  the  pig- 
ment was  lost  and  an  apoplastidic  race  was  produced  in 
which  the  stigma  disappeared  if  the  organism  were  kept 
in  the  dark  ;    once  lost,  the  eye-spot  did  not  reappear. 

In  certain  Dinoflagellates,  organisms  which  form  an 
important  part  of  the  plankton  of  lakes  and  the  sea,  the 
1  p.  48. 


Fig.  81.— The  Eye- 
spot  OF  PoUCHETIA. 
Showing  1  hf  large 
pigmented  /-  ■•,  P, 
and  the  lens,  '■■  ifter 
Schiitt). 


INVERTEBRATE    EYES  127 

stigma  may  be  more  complex.  In  Pouchetia,  for  example,  the  pignient  is  arranged 
in  the  form  of  a  cup-shaped  mass  the  opening  of  which  is  covered  by  a  refractile 
structure,  while  within  the  cup,  between  the  primitive  lens  thus  formed  and  the 
pigment,  lies  the  light-sensitive  protoplasm  (Fig.  81)  (Schiitt,  1896)  ;  occasionally 
in  the  marine  forms  this  structure  is  of  such  a  size  that  it  has  been  called  an 
ocellus,  but  it  is  acellular.  In  all  these  cases  the  organelle  combines  photo- 
sensitivity with  directional  detection  in  order  to  perform  its  phototactic  function. 

Buder.  Jb.  wiss.  Botan.,  58,  105  (1917).  Biol.  Zbl.,  34,  641  (1914). 

Ehrenberg.       Die    Infusionsthierchen     als  Z.  vergl.  Physiol.,  5,  730  (1927). 

volk-.  Organi.smen,  Leipzig  (1838).  Biol.  Rev.,  13,  186  (1938). 

Engelmann.     Pfliigers  Arch.  ges.  Physiol.,  .^     <.        i  t  i  /^  ?    m      •  ;     io 

2Q    387  (188'^r  Mast  and  Johnson.     Z.  vergl.  Physiol.,  IQ, 

Franz.  Z.  wiss.  Zool,  56,  138  (1893).  "^^  (1932). 

Jennings.    Pub.  Carnegie  Inst.  Washington,  Pringsheim,   E.    G.   and   O.      New   Phyto- 

No.  16,  256  (1904).  logist,  51,  65  (1952). 

Kuhn,    Stene   and    Sorensen.      Ber.   dtsch.  Schutt.     Ergebn.  Plank,  e.vped.  (1896). 

c/^em.Ge^.,  72,  1688(1939).  J          ^     i     v       j         i    r, 

Mast.     J.  exp.   Zool.,  3,   359   (1906)  ;    20,  Tiseher.     Hoppe  beyl.   Z.  physiol.  Chem., 

6(1916)                                          ^  '    ''".  239,  257  (1936)  ;   252,  225  (1938). 

Light   and   the    Behavior   of  Organisms,  Wager.     J.   Linn.  Soc.   (Zool.)  Lond.,  27, 

N.Y.  (1911).  463(1900). 

LIGHT-SENSITIVE    CELLS 

Once  multicellular  organisms  evolved,  the  obvious  specialization 
occurred  whereby  certain  cells  acquired  a  special  sensitivity  to  light  ; 
as  would  be  expected,  they  were  ectodermal  cells  initially  developed  in 
the  surface  epithelium  although  on  occasion  they  migrated  below  the 
surface  layer.  Such  cells  may  be  found  alone  or  may  occur  in  associa- 
tion with  others  to  form  an  eye  ;  and  in  either  case  they  may  assume 
several  forms  usually  with  well-defined  characteristics,  including  a 
specially  sensitive  receptor  as  well  as  an  arrangement  to  conduct  away 
the  excitation.  Frequently  the  cell  is  associated  with  pigment  which 
serves  as  an  absorbing  agent,  a  fimction  which  becomes  all  the  more 
important  when  the  sentient  cells  sink  below  the  surface,  in  which  case 
the  receptive  pole  is  frequently  surrounded  by  a  pigment  mantle 
(Fig.  82).  While  thus  aiding  the  receptor  mechanism,  an  absorbing 
pigment  mantle  is  not  essential  and,  indeed,  is  frequently  absent. 

The  light-sensitive  cell  usually  assumes  a  specialized  form  which 
may  be  differentiated  into  two  main  types.  In  the  first  and  more 
common  type  two  poles  are  distinguished — a  distal  to  receive  the 
stimulus  of  light  and  a  jjroximal  to  conduct  away  the  excitation.  In 
the  fully  developed  bipolar  cell,  therefore,  three  regions  are  apparent  : 
a  receptor  or  end-organ,  a  cell  body  with  the  nucleus,  and  a  proximal 
prolongation  into  a  conducting  fibre. 

The  recejitive  end-organ  of  the  cell  is  often  found  to  assume  a 
complicated  form  ;  sometimes  it  is  provided  with  digitations,  presum- 
ably in  an  attempt  to  increase  the  receptor  surface  (Fig.  87)  ;  more 
frequently  it  undergoes  specific  modifications  which  can  be  classed  as 
belonging  to  two  main  types,  cilia  and  rods,  the  second  presumably  a 


128 


THE    EYE    IN   EVOLUTION 


Figs.  82  to  85. — Types  of  Bipolar  Visual  Cell. 


Fig.  82. 


Fig.  83. 


J. 


Fig.   84. 


Fig.   85. 


Fig.  82. — The  visual  cell  of  the  edible  snail,  Helix  pomatia,  showing 
cilia  (after  Hesse). 

Fig.  83. — The  visual  cell  of  the  grey  slug,  Llnuix  maximus,  showing 
elongated  end  with  cilia  (after  Hesse). 

Fig.  84. — The  visual  cell  of  the  marine  worm,  Phniaria  forva,  showing 
brush-like  border  (after  Hesse). 

Fig.  85. — Rod-like  visual  cell  of  the  Tabanid  fly,  Cliry.b-ops  marmoratus 
(after  Ciaccio). 


specialized  derivative 
in  many  ectodermal 
several  types  of  sensor 


Fig.  86. — Apolar  Visual 
Cell. 

A  light-sensitive  cell  in 
the  earthworm,  LiDtibvi- 
cus  terre.stris,  stained  with 
silver  nitrate.  N,  nu- 
cleus ;  OX,  optic  nerve 
which  breaks  up  into  a 
network  of  neurofibrils, 
CN,  throu;^:  out  the  cyto- 
plasm ;  ()(i,  optic  orga- 
nelle coverev  a,  denser 
network  of  urofibrils 
to  form  ti  ■.'tinella 
(after  W.  N.  li       ). 


of  the  first. 1  cilia  (Figs.  82  and  83)  are  found 
cells  and  form  an  important  differentiation  of 
y  cells,  and  it  may  be,  as  Hesse  (1902)  surmised, 
that  they  represent  the  distal  terminations  of 
bmidles  of  the  "  neuro-fibrillse  "  which  form  the 
primitive  conducting  mechanism  ^  ;  a  similar 
configuration  is  seen  in  cells  with  a  striated  or 
brush-like  border  (Fig.  84).  rods  (or  rhabdites) 
appeared  originally  as  simple  but  stouter 
cylindrical  prolongations  of  protoplasm,  clear 
and  refractile  in  nature,  which  in  subsequent 
evolution  have  undergone  innumerable  speciali- 
zations (Fig.  85)  ;  they  are  found  in  worms, 
Arthropods,  and  Molluscs,  and  they  attain 
their  highest  differentiation  in  the  rods  and 
cones  which  form  the  imique  receptor  apparatus 
in  the  eyes  of  Vertebrates. 

The  second  type  of  recejDtor  is  seen  among 
worms  and  Molluscs  ;  in  it  the  cell  is  apolar  in 
its  general  arrangement  but  contains  a  light- 
sensitive  mechanism  within  the  cell  body  (Fig. 
80).      This    typically    takes    the    form    of    a 

1  p.  243. 

2  See  VVorley  (1933-41). 


INVERTEBRATE   EYES  129 

peculiarly  shaped  ellipsoidal  mass — the  optic  organelle  (the  "  Binnen- 
korper  "  of  Hesse  ;  the  "  Glaskorper  "  of  Apathy,  1897) — distinctly 
marked  off  from  the  rest  of  the  cytoj)lasm  by  its  deeper  staining, 
occupying  the  centre  of  the  cell  and  crowding  the  nucleus  to  one  side  ; 
it  is  made  up  of  a  clear  hyaline-like  structure  (a  "  lens  ")  surrounded 
by  a  dense  neurofibrillar  network  (the  retinella).  Hess  (1925) 
found  experimentally  that  no  matter  from  which  direction  light  was 
directed  onto  the  cell,  the  "  lens  "  brought  it  to  a  focus  on  the  sur- 
rounding network  of  the  retinella,  a  circumstance  which  suggests  that 
the  hyaline  mass  focuses  the  light  which  induces  a  direct  stimulation 
of  the  nerve-fibres,  possibly  by  a  photo-electrical  rather  than  a 
photochemical  effect. 

Depending  on  the  arrangement  of  these  cells  singly  or  in  com- 
munities to  form  an  organ,  invertebrate  eyes  may  be  classified  morpho- 
logically as  follows. 

I.  The  SIMPLE  EYE  or  ocellus. 

1.  The  unicellular  eye. 

(a)  epithelial, 
(6)  subepithelial. 

2.  The  multicellular  eye. 

(a)  the  subepithelial  eye, 
(6)  the  epithelial  invaginated  eye. 
(i)  the  flat  eye, 

(ii)  the  cupulate  eye, 

(iii)  the  vesicular  eye. 

II.  Intermediate  forms. 

(a)  The  aggregate  eye. 

(6)  The  composite  ocellus. 

(c)  The  simple  ommatidial  eye. 

III.  The  compound  eye. 

The  Simple  Eye 

A  simple  light-sensitive  cell,  an  ectodermal  cell  differentiated  from 
its  neighbours  in  order  to  receive  incident  light  and  transmit  a  physio- 
logical imjjulse,  ranks  as  a  very  primitive  type  of  eye.  With  single 
cells,  each  of  which  is  responsive  merely  to  the  presence  of  light,  a 
light-sense  may  exist,  but  no  definite  image  such  as  is  necessary  for  the 
development  of  the  visual  sense  can  be  formed.  If,  however,  these 
cells  multiply  and  group  together  in  clumps  l^o  form  an  "  organ  ",  some 
conception  of  an  object  may  be  realized  and  a  primitive  directional 
analysis  may  be  made  of  visual  space.    Each  single  constituent  cell,  it 


S.O.— VOL.  I. 


130 


THE   EYE   IN   EVOLUTION 


is  true,  merely  records  the  sensation  of  light,  but  the  summation  of 
all  their  individual  sensations  will  give  an  elementary  mosaic  or  pattern 
of  light  and  shade  with  a  consequent  impression  of  the  external  world. 
So  long  as  the  component  cells  of  the  group  retain  their  individuality 
and  act  independently  of  each  other,  they  may  be  considered  to  form 
a  "  simple  "  eye.  The  simple  eye  or  ocellus  (dim.  of  oculus,  eye) 
may  therefore  be  defined  as  a  single  light-sensitive  cell  or  group  of  such 
cells  acting  ivithout  functional  association. 


Leucosolenia 


THE    UNICELLULAR    EYE 

Single  cells  which  are  responsive  to  light  ("  cellules  visuelles  "  of 
Apathy,  1897  ;  "  Photores  "  of  Beer,  1901)  were  first  adequatel}^ 
described  by  Richard  Hesse  (1896)  as  occurring  in  the  epidermal  layer 
of  worms  ;  he  called  them  "  Sehzellen  ",  but  since  in  many  cases  they 
appreciate  the  presence  of  light  for  the  purposes  of  jDliototactic  reactions 
and  are  probably  not  associated  with  a  visual  sense  as  the  term  is 
generally  understood,  we  shall  call  them  light-sensitive  cells. 
Shortly  thereafter  they  were  found  in  a  large  number  of  animals, 
sometimes  scattered  about  indiscriminately  but  usually  aggregated  in 
those  regions  where  they  are  of  most  importance  to  the  organism.  Thus 
in  clams  they  are  confined  to  the  siphon,  in  some  shell-fish  are  arranged 
like  a  coronet  around  the  edge  of  the  mantle,  and  in  annelid  worms  they 
are  concentrated  at  the  two  extremities,  particularly  the  anterior.^ 

Unicellular  eyes  may  assume  either  of  the  two  forms  of  light- 
sensitive  cell  we  have  already  discussed — the  bipolar  form   with    a 
specialized    sensory    termination    or    the    apolar 
form  characterized  by  an  intracellular  organelle. 

SINGLE    BIPOLAR    LIGHT-SENSITIVE    CELLS    are 

usually  provided  with  a  ciliate  or  brush-like  border 
and  are  associated  with  pigment,  usually  placed  as 
a  cap  around  the  light-sensitive  end  of  the  cell. 
They  are  seen  in  the  unicellular  photoreceptors  of 
the  larvse  of  certain  sponges  {Leucosolenia, 
Minchin,  1896)  and  in  Rotifers,  but  occur  most 
typically  among  worms.  Examples  of  this  are 
the  light-sensitive  cells  of  Tristomum  papillosum, 
a  Trematode  parasitic  on  marine  fishes  (Fig.  87),  or 
in  Polyophthalmus  pictus,  a  sedentary  Polychsete 
which  abounds  in  the  Bay  of  Naples  (Hesse,  1899- 
1908). 


eye 


is  interesting  that  the  most  primitive  "cerebral  " 
ordates,  seen  in  the  neural  tube  of  Amphioxus^ 


190. 


p.  230. 


Fig.  87. — Unicellu- 
lar Eye  of  the 
Trematode  Worm, 
Tristomum  papil- 
losum. 

The  cell  is  provi- 
ded with  a  crenated 
border  and  piginent 
mantle  (after  Hesse). 


THE   SIMPLE   EYE 


131 


is  similarly  a  single  photosensitive  neural  cell  associated  with  a  pigment  mantle 
(Fig.  238). 

SINGLE  APOLAR  VISUAL  CELLS  are  typified  in  the  light-sensitive 
organs  of  the  earthworm,  Limibricus  terrestris  ;  these  have  received 
closer  study  than  those  of  any  other  species  (R.  Hesse,  1894—97  ;  Beer, 
1901  ;  Kowalski,  1909  ;  W.  N.  Hess,  1924-25)  (Figs.  86  and  88). 
They  are  found  in  two  sites — ^in  the  epithelium  and  in  association  with 
the  nerves  immediately  underneath  ; 
it  is  probable,  as  has  been  shown  in 
the  medicinal  leech  (Whitman,  1893), 
that  the  latter  originated  in  and 
migrated  from  the  epidermal  layer. 
In  appearance  they  are  distinctive. 
The  superficial  cells  are  small  and 
rounded,  lying  at  the  base  of  the 
epithelium  and  into  each  the  sub- 
epithelial nerve-net  sends  a  nerve- 
fibre  which  breaks  up  into  a  network 
of  neurofibrils  surrounding  the  ellip- 
soidal optic  organelle  ^  ;  the  sub- 
epithelial cells  clumped  around 
enlargements  of  the  nerve  plexus  are 
similar  in  type  and  presumably  in 
function.  It  is  interesting  that  a 
dense  layer  of  pigment  lies  under  the 
epithelium  apparently  unassociated 
with  the  light-sensitive  cells  ;  but  as 
they  traverse  this  layer  and  run  into 
the  epithelium,  the  nerves  make  pin- 
point openings  in  the  dense  pigmen- 
tary blanket  so  disposed  that  incident 
light  will  enter,  dorso -anteriorly  at 
the  anterior  end  of  the  worm  and 
dorso -posteriorly  at  the  posterior  end, 
and  will  thus  strike  the  subepithelial  cells  directly  as  either  extremity 
emerges  from  the  burrow. 

The  light-sensitive  cells  of  leeches  are  also  of  a  very  similar  type,  each 
containing  an  identical  optic  organelle  supplied  with  a  nerve  fibre  from  the 
dorsal  ganglion  (R.  Hesse,  1897).  They  may  occur  as  isolated  cells  just  below 
the  epithelium  or  may  lie  in  association  with  other  sensory  cells. ^  Light- 
sensitive  cells  identical  with  those  of  the  earthworm  are  also  found  in  lamelli- 
branch  molluscs  ;  thus  in  the  clam,  Mya  arenaria,  they  are  seen,  plentifully 
supplied  with  nerves,  lying  jvist  beneath  the  epithelial  layer  on  the  inner  surface 

1  p.  128.  2  p.  1.3.3. 


Fig.      88. — Single      Light-sensitive 
Cells    in    the    Earthworm,   Lim- 

BRICVS   TERllKSTRIS. 

The  photoreceptor  cells,  L,  lying  in 
tlie  basal  region  of  the  epidermis,  E, 
and  also  in  enlargements  of  the  nerve 
in  close  relation  to  the  eijidermis.  The 
nerve  is  seen  to  spread  out  beneath 
the  epithelium  as  a  subepidermal 
nerve  plexus,  the  fibres  of  which  go  to 
the  photoreceptor  cells.  C,  cuticle 
(after  W.  N.  Hess). 


4fipii^i4uiuiS$&^^l^ 


Lumbricus 


Mya  arenaria 


132  THE   EYE   IN  EVOLUTION 

of  the  siphon  ;  again,  each  contains  an  optic  organelle  with  a  surrounding 
nerve-plexus  (Light,  1930).  It  is  interesting  that  somewhat  similar  cells, 
presumably  sensitive  to  light,  have  been  described  in  the  epidermis  of  the  tail 
of  the  ammocoete  larva  of  the  lamprey  (Steven,  1951).^ 

Apathy.     Mitt.  zool.  Stat.  Neapel,  12,  495  Kowalski.     La  Cellule,  25,  291  (1909). 

(1897).  Light.    J.  Morph.  Physiol.,  49,  1  (1930). 

Beer.      Wien.  klin.   Wschr.,  \^,  255,  29,5,  Minchin.    Proc.  roj/.  5'oc.  J5,  60,  42  (1896). 

314(1901).  Steven.      Quart.    J.    micr.    Sci.,    92,    233 

Hess,  W.  N.     Biol.  Bull.,  38,  291  (1919).  (1951). 

J.  Mor/j/i.,  39,  515(1924)  ;  41,63(1925).  Whitman.     Zool.  Jb.,  Abt.  Anat.,  6,  616 

Hesse,  R.     Z.  m«s.  Zoo/.,  58,  394  (1894)  ;  (1893). 

81,  393  (1896)  ;    62,  671  (1897)  ;    63,  Worley.      Proc.   nat.   Acad.  Sci.,   19,   323 

361(1898);    65,446(1899);    72,565  (1933). 

(1902).  J.  exp.  Zool.,  69,  105  (1934). 

Die    Sehen    der    niederen    Tiere,    Jena  J .  cell.  comp.  Physiol.,  b,5Z  {l^^'i)  ;   18, 

(1908).  187  (1941). 

THE    MULTICELLULAR    SIMPLE    EYE 

While  the  most  primitive  example  of  the  simple  eye  is  represented 
by  a  single  light-sensitive  cell,  the  next  obvious  development  is  the 
association  of  a  group  of  epithelial  cells  each  reinforcing  the  effective- 
ness of  the  others.  For  this  purpose  several  evolutionary  lines  have 
been  followed  so  that  eventually  the  end-organ  appears  to  reach  a 
degree  of  complexity  greater  than  the  analysing  capacity  of  the  nervous 
organization.  Efficiency  is  enhanced  not  only  by  the  progressive 
development  of  the  capacity  to  form  detailed  images  as  the  number  of 
sensory  cells  increases,  but  also  of  the  ability  thereby  obtained  to 
localize  the  stimulus  in  space  and  analyse  the  visual  field  (a  directional 
eye).  The  association  of  pigment  forming  an  absorbent  screen  within 
or  around  the  sensory  cells  is  a  constant  feature,  while  the  efficiency  of 
the  organ  is  further  increased  by  the  development  of  a  focusing 
apparatus.  To  this  end  a  wide  variety  of  optical  mechanisms  is 
exploited  varying  from  a  pin-hole  to  a  lens-system  of  progressive 
elaboration  until,  in  Cephalopods.  a  dioptric  mechanism  comparable  to 
that  of  Vertebrates  is  reached.  The  inner  ends  of  the  sensory  cells  are 
prolonged  to  form  elongated  processes  or  nerve  fibres  which  leave  the 
deep  surface  of  the  ocellus  to  join  a  subepithelial  plexus  or  a  ganglion. 

The  sensory  cells  usually  remain  in  association  with  the  surface 
layer  but  occasionally  migrate  inwards  to  the  subepithelial  tissues  ; 
and  since  the  latter  type  of  ocellus  undergoes  less  evolutionary  develop- 
ment than  the  former,  we  will  discuss  it  first. 

The  Subepithelial  Eye 
The  fnigration  of  a  number  of  light-sensitive  cells  from  the  surface 
with  th(  ■    aggregation  in   the  subepithelial  tissues  to  form  a  sub- 
epithelial       >  always  results  in  an  organ  of  a  very  elementary  type. 

1  p.  263. 


THE   SIMPLE   EYE 


133 


These  cells  may  belong  to  either  of  the  two  main  types  we  have  just 
discussed.  In  the  first  place,  we  have  already  seen  in  the  case  of  the 
earthworm  that  an  aggregation  of  apolar  cells  with  a  central  organelle 
in  the  cell-body  may  migrate  from  the  surface  epithelium  to  form  a 
subepithelial  mass  in  association  with  the  nerve  fibres  (Fig.  88). 
Subepithelial  eyes  formed  by  the  clumping  together  of  a  multitude  of 
visual  cells  of  this  tjrpe  within  a  dense  pigmentary  mantle  are  found  in 
certain  leeches. 


Figs.    89    and 


90. — The    Sensory    Organs    of    the    Medicinal    Leech, 
HlRCDO   Medici.\alis. 


Fig.  89. — The  sensory  organ  of  the  inter- 
mediate'segments  consists  of  a  collection 
of  undifferentiated  sensory  cells,  S, 
among  which  are  seen  the  large  light- 
sensitive  cells,  V  (4  in  the  figure), 
with  the  kidney-shaped  hyaline  optic 
organelle  (after  Biitschli). 


jg^trasOTiamjxr 


FiG.  90. — Each  "  eye  "'  situated 
in  the  anterior  segments  con- 
sists of  a  cluster  of  apolar 
cells  provided  with  optic 
organelles,  the  whole  being 
enclosed  in  a  pigment  mantle 
through  which  the  nerve  fibres 
travel,  and  Ij'ing  beneath  the 
surface  epithelium  (schematic 
after  Hesse). 


The  ocelli  of  the  medicinal  leech,  Hirudo  medi'^inalis,  are  of  unusual  interest 
since  they  show  all  stages  of  evolution  from  a  unicellular  to  a  multicellular  eye. 
As  we  have  noted, ^  typical  apolar  light-sensitive  cells  may  occur  lying  singly, 
deep  in  the  epithelium.  On  the  dor.sal  surface  of  the  intermediate  segments  of 
the  animal  there  are  paired  clusters  of  undifferentiated  sensory  cells  derived 
from  the  epithelium,  each  cluster  forming  a  segmental  sensory  organ  the  function 
of  which  seems  to  be  essentially  tactile  ;  among  these  cells  there  are  several 
typical  light-sensitive  cells  so  that  the  colony  presumably  has  a  dual  function 
(Fig.  89).  On  the  anterior  five  segments  these  clusters  of  cells  are  purely  visual 
and  are  clumped  together  in  a  cylindrical  mass  at  right  angles  to  the  surface 
enclosed   in  a  dense  pigmentary  mantle,   forming  subepithelial   eyes  (Fig.   90) 

1  p.  131. 


Hirudo 


134 


THE   EYE   IN   EVOLUTION 


HoBmadipsa 


(Whitman,  1889-93  ;  Maier,  1892  ;  Hesse,  1897-1902  ;  Biitschli,  1921).  In  the 
land-leech,  Hoemadipsa,  the  ordinary  segmented  papillfe  more  closely  resemble 
eyes  since  the  visual  cells  are  associated  with  j^igment  (Bhatia,  1956). 

In  the  second  place,  bipolar  cells  with  a  cihate  or  brush-like 
receptor  and  a  proximal  nerve  fibre  may  similarly  migrate  into  the 
subepithelial  tissues,  aggregating  into  a  cluster  in  association  with  a 
mantle  of  pigment  cells.  These  are  seen  typically  in  the  leaf-like 
turbellarian  and  the  ribbon-like  nemertine  worms  (Figs.  91  to  93).  In 
these,  the  eye  consists  merely  of  one  or  a  number  of  elongated  visual 
cells  with  a  distal  ciliated  border,  the  fibrillar  terminations  of  which 
run  proximally  to  form  an  optic  nerve  ;    the  organ  lies  under  the 


Figs.  91  to  93. — Subepithelial  Eyes  (after  Hesse). 


Fig.  91. — The  eye  of  the  turbellarian  worm,  Planaria  torva,  consisting  of  two 
light  cells  with  cilia  (c),  nucleus  (71)  and  pigment  mantle  (p),  the  whole 
Ij'ing  underneath  the  epithelium  (e). 


r]~o] *  I  o|V|^"je|fr  e 


HZ 


™aaa, 


Fig.    '.2. — The  eye  of  the  turbellarian 
'>)rm,  Planaria  gonocephala. 


Fig.    93. — The    eye   of  the   nemertine 
worm,  Drepanophorus. 


THE   SIJVIPLE   EYE 


135 


epithelium  and  the  elongated  visual  cells  curve  away  from  the  surface 
to  crowd  into  a  cellular  cup  of  densely  pigmented  cells.  Such  an  organ 
in  addition  to  being  light-sensitive  can  appreciate  the  direction  of 
incident  light,  and  forms  a  primitive  type  of  directional  eye.  A  still 
more  complicated  organ  of  this  type  is  seen  in  the  paired  eyes  of 
Chaetognaths,  such  as  the  marine  arrow-worm,  Spadella  (Hesse,  1902), 
and  in  the  median  eyes  of  certain  Crustaceans.^ 

It  is  of  interest  that  in  this  subepithehal  type  of  eye  the  sensory  pole  of  the 
cell  is  usually  directed  away  from  the  incident  light  which  has  to  traverse  the 
cell -body  in  order  to  reach  it  ;  technically,  therefore,  these  are  examples  of  an 
inverted  retina.^ 


Chsetognath 


The  Epithelial  Invaginated  Eye 

A  much  more  common  arrangement,  however,  is  an  association  of 
a  number  of  contiguous  cells  in  the  epithelial  layer,  which  as  evolution 
progresses  eventually  invaginate  into  the  underlying  tissues.  In  such  a 
development  the  first  stage  is  the  specialization  of  a  number  of  con- 


mii^ 


b 


Fig.   94. — Scheme   of  Development  of  the   Simple   Epithelial  Eye   of 

Invertebrates. 

(a)  Single  epithelial  light-cell. 

(6)  A  group  of  light-cells  forming  a  flat  eye  (Fig.  95). 

(c)  The  cupulate  eye  (Fig.  97). 

(d)  The  formation  of  a  dark  chamber  (Fig.  100). 

(e)  The  vesicular  eye  (Fig.  110). 

(/)  The  eye  of  Cephalopods  (Fig.  113). 


tiguous  surface  cells  to  form  a  plaque  on  the  surface — the  flat  eye 
(Fig.  946)  ;  the  second  stage  is  evident  when  the  epithelium  becomes 
invaginated  so  that  the  sentient  cells  line  a  simple  depression  on  the 
surface^ — the  cupulate  eye  ;  thus,  while  to  some  degree  protected, 
their  functional  utility  is  increased  by  the  crowding  together  of  more 
units  into  the  same  space,  and  by  an  arrangement  whereby  they  can 
orientate  more  accurately  the  incident  light.     A  further  improvement 

1  p.  152.  -  p.  146. 


136 


THE   EYE   IN   EVOLUTION 


is  gained  when  the  opening  of  the  depression  is  narrowed  so  that  a  dark 
chamber  with  a  pin-hole  opening  is  formed.  The  last  step  in  the 
differentiation  of  the  simple  eye  is  marked  by  the  closure  of  the  opening 
leading  into  the  depression  by  a  circular  in-folding  of  the  surrounding 
epithelium  ;  thus  is  formed  the  vesicular  eye,  the  highest  differentia- 
tion of  which  is  reached  in  the  eye  of  Cephalopods  wherein  the  vesicle 
is  associated  with  a  secondary  invagination  of  the  ectodermal  layer 
which,  in  addition  to  providing  a  protective  covering,  helps  to  constitute 
a  dioptric  mechanism.  The  scheme  of  the  development  of  the  simple 
eye  from  its  primitive  beginning  as  a  single  cell  to  this  highly  complex 
structure  is  seen  in  Fig.  94. 

The  simiDlicity  of  these  eyes  is  seen  in  their  capacity  for  regeneration,  a 
potentiality  first  demonstrated  by  Bonnet  (1781).  If  the  tentacle  with  the  eye 
is  removed  from  the  edible  snail  or  the  grey  slug,  another  regenerates,  occasion- 
ally equipped  with  two  eyes,  a  process  which  has  been  known  to  occur  twenty 
times  in  succession  (Galati-Mosella,  1915-17).  ExiDerimenting  similarly  on  the 
gastropod,  Murex,  Carriere  (1889)  found  that  the  regenerating  eye  initially  took 
the  form  of  a  simple  depression,  which  gradually  closed  leaving  only  a  pore-like 
opening  and  eventually  developed  into  a  closed  vesicle. 


THE    FLAT    EYE 


This  is  the  most  primitive  association  of  light-sensitive  cells  and 
usually  consists  of  5  or  6  epithelial  cells  lying  upon  the  surface, 
differentiated  by  being  a  little  larger  than  their  unspecialized  neigh- 
bours.    Such  an  ocellus  is  seen  in  the  aquatic  worm,  Stylaria  lacustris 


Figs.  9.5  and  96 — Flat  Eyes. 


Dendrocarhcm 


Fig.  95. — The  ocellus  of  the  aquatic 
amielid  worm,  Stylaria  lacustris  (after 
Hesse). 


Fig.  96. — The  ocellus  of  the  hydro- 
medusan,  Lizzia,  the  epithelial  sen- 
sory cells  being  capped  by  a  lens-like 
thickening  of  the  cuticle  (Hertwig 
and  Jourdan). 


(Fig.  95)  (Hesse,  1908),  in  certain  unsegmented  planarian  worms  such 
as  Dendrocoslum  and  some  leeches,  while  in  the  larvae  of  some  insects 
the  eyes  consist  merely  of  a  pair  of  visual  cells  and  two  overlying 
pigTi^ent  cells  (Hesse,  1908  ;  Imms,  1935).  Occasionally  a  simple 
cuti.  ;lar  refringent  apparatus  is  added  to  collect  the  light  as  well  as 
pignic '  t  to  absorb  it  ;  thus  in  the  hydromedusan,  Lizzia,  the  eye, 
situa        at  the  base  of  the  tentacle,  is  composed  of  a  number  of  sensory 


THE   SIMPLE   EYE 


137 


cells  associated  with  j)igmented  cells  capped  by  a  "  lens  "  formed  by  a 
localized  thickening  of  the  cuticle  (Fig.  96)  (Hertwig,  1878  ;  Jourdan. 
1889). 

THE    CUPULATE  EYE 

The  crpuLATE  or  cup-shaped  eye  {cupula,  a  cup)  forms  a  distinct 
functional  advance,  for  the  invagination  of  the  light-sensitive  epithelium 
allows  the  development  of  a  primitive  directional  sense  (Patten,  1886). 
Its  development  may  be  seen  in  three  stages.     The  first  is  a  simple 

Figs.  97-100. — Typical  Cupulate  Eyes  of  the  Simplest  Type. 


Fig.    97. — The   ocellus   of  the   limpet, 
Patella. 

Ep,  epithelium  ;  S,  secretory  sub- 
stance covering  visual  cells  ;  N,  nerve 
(after  Hesse). 


Fig.  98. — The  ocelkis  of  the  ear-shell, 
Haliotis. 

The  cup-shaped  depression  is  deep 
with  a  narrow  neck  and  is  filled  with 
secretion  formed  by  the  epithelial  cells 
(after  Hesse). 


Fig.  99. — The  visual  organ  of  the  larva 
of  the  house-fly,  Musca. 

There  is  a  small  cavity  in  the 
cephalo-phar\Tigeal  skeleton  wherein 
lie  light-sensitive  cells,  C,  from  which 
issues  the  optic  nerve,  N  (after 
Bolwig). 


Fig.  100. — The  ocellus  of  the  mollusc. 
Nautilus,  with  its  pin-hole  opening 
(after  Hesse). 


138 


THE    EYE    IN   EVOLUTION 


ViGS.    101-3. — Representative  Cupulate  Eyes  of  a  Moke  Complex 

Type. 


Fig.   101. — The  ocellus  of  the  polychspte  worm, 
Nereis. 

C,  cuticle  ;  Ep,  epithelmm  ;  N,  nerve  fibres  ; 
P,  pigment  between  the  sensory  cells  ;  R, 
nucleated  sensory  cells  provided  with  cilia  ; 
y,  vitreous  (after  Hesse). 


Fig.  102.— The  ocellus  of  the  Cubo- 
medusan,  C'harybdea. 

L,  cellular  lens  ;  V,  "  vitreous 
body  "  of  the  clear  rhabdites  of 
retinal  cells  ;  P,  pigmented  zone 
of  retinal  cells  ;  R,  retinal  cells  ; 
N,  nerve  tissue  with  ganglion  cells, 
G  (after  Berger). 


ON 


CG 


Fig.    103. — The  eye  of  Peripalns. 

Diagrammatic  sagittal  section  of  t}ie  e\e  ;  partly  depigmented  to 
demons;  i  ate  details  of  the  visual  cells. 

C  lea  ;    CG,  cerebral  ganglion  ;    Ep,  hypodermis  ;    L,  lens  ;   OG,  optic 

ganglio;         ')N,  optic  nerve  ;    R,  rods  ;    V,  visual  cells  (after  Dakin). 


THE   SIMPLE   EYE 


139 


depression  or  dimple  in  the  epithelium,  such  as  is  seen  typically  among 
Molluscs  ;  some  30  such  cup-shaped  depressions,  for  example,  each 
^  mm.  in  diameter,  skirt  the  border  of  the  mantle  of  the  bivalve,  Lima, 
while  similar  structures  are  seen  at  the  base  of  the  tentacles  of  the 
common  limpet.  Patella  (Fig.  97).  The  simple  eyes  of  the  larva  of  the 
house-fly,  Musca,  are  of  a  similar  type  (Bolwig,  1946)  (Fig.  99).^  In  such 
cases  the  sensory  epithelium  may  be  composed  of  light-sensitive  pig- 
mented cells  interspersed  with  unpigmented  secretory  cells  which  secrete 
a  protective  material  covering  the  epithelium.  The  second  stage  is 
marked  by  an  overlapping  of  the  surface  epithelium  so  that  the  shallow 
pit  becomes  converted  into  a  cavity  with  a  tiny  opening.  Such  a  cup 
may  be  oval  and  deep  and  filled  with  secretion,  as  in  the  ear-shell, 
Haliotis  (Fig.  98),  but  the  tendency  is  seen  in  its  most  marked  form  in 
the  rare  pearly  mollusc.  Xaufilus.  which  lives  in  a  beautiful  spiral  shell 
in  the  seas  of  the  Far  East  (Fig.  100).  In  this  cephalopod,  situated 
just  behind  the  tentacles,  a  pin-hole  opening  2  mm.  in  diameter 
leads  into  a  large  ocular  cavity  lined  by  light-sensitive  cells  bathed  by 
sea-water,  the  eye  thus  constituting  a  veritable  dark  chamber  (Merton, 
1905).  In  a  third  and  final  development  the  cavity  is  closed  by  the 
growth  of  the  cuticle  associated  with  hypodermal  cells  over  the  opening. 
Although  a  closed  vesicle  is  thus  formed,  it  is  made  up  of  the  non- 
cellular  cuticle  which  extends  uninterruptedly  over  the  cupula  of  the 
invaginated  layer  of  cells,  while  the  secretory  mass  elaborated  by  the 
sensory  cells  becomes  enclosed  to  form  a  vitreous  body  (the  marine 
polychgete  worm.  Nereis— Hesse,  1897-1908)  (Fig.  101). 

Once  this  stage  has  been  reached,  further  advances  can  be  made  in 
the  optical  arrangements  of  such  an  eye.  The  simplest  is  the  more  or 
less  elaborate  thickening  of  the  cuticular  layer  of  the  epithelium  to 
form  a  refringent  apparatus.  In  its  most  primitive  form  such  an  eye 
consists  merely  of  a  group  of  visual  cells  arranged  in  a  hollow  beneath 
a  lens  formed  from  the  cuticle  as  is  seen,  for  example,  in  the  medusoid, 
Sarsia,  or  the  louse,  Pediculus,  or  other  insects  (Fig.  106).  A  somewhat 
similar  morphology  is  seen  in  the  eye  of  the  Onychophore.  Perijmtus,^ 
but  in  it  the  large  lens  is  formed  from  the  hypodermal  cells  and 
takes  the  place  of  the  vitreous  (Fig.  103)  (Cuenot,  1949).  Usually, 
however.  h\^odermal  cells  continuous,  on  the  one  hand,  with  the 
surface  ectoderm  and,  on  the  other,  with  the  sensory  cells  of  the 
cupula,  edge  their  way  underneath  the  cuticle  where  they  may  form  a 
clear,  refractile  mass  underneath  the  cuticular  lens  constituting  a 
primitive  lens  or  vitreous  (as  in  the  ocelli  of  many  insects  and  in  some 
spiders.  Figs.  104  and  105)  (Biitschli,  1921;  Wigglesworth,  1941;  and 
others).  Alternatively,  as  in  the  C'ubomedusan,  Charybdea,  the  distal 
ends  of  the  retinal  cells  (rhabdites)  develop  greatly  to  form  a  clear 

1  p.  224.  2  p.  204. 


^^^^a^miD 


Larva  of  Musca 


Nautilus 


Nereis 


Sarsia 


Pediculus 


Peripatus 


Figs.   104—9. — Cupulate  Eyes  of  Arthropods. 


Fig.  104. — The  frontal  stemma  of  the 
imago  of  the  blow-fly,  Calliphora 
(after  Lowne). 


Fig.  10.5. — Sagittal  section  of  the 
median  anterior  ocellus  of  the 
jumping  spider,  Salticus  (after  Biit- 
schli). 


DIS 


Fig.    106.— The  frontal  oceUus  of  the 
hover-fly,  Helophilus. 

DIS,  cells  with  long  sensory  ends 
lying  distant  from  the  lens  ;  Pr,  cells 
with  short  sensory  ends  lying  proxi- 
mally  to  the  lens  (after  Hesse). 


Fig.  107. — The  anterior  median  ocellus 
of  the  house  spider,  Tegenaria  domes- 
tica. 

It  is  to  be  noted  that  the  optic  nerve 
fibres,  ON,  issue  from  the  lateral  aspect 
of  the  visual  cells,  R  (compare  p.  159). 


Fig.    108.— The  dorsal  ocellus  of  the 
insect,   Aphrophora  spumaria   (after 


Fig.    109. — The  lateral  ocellus  of  the 
scorpion       (after      Lankester      and 
Link).  Bourne). 

In  Figs.  !  ()H-9  the  eye  is  in  every  sense  simple  although  there  is  some  association  of 
the  visual  >  .•  lis  around  rhabdon>«s. 


Cut,  cuticle  ;  Ep,  hypodermal  epithelium  ;  L,  cuticular  lens  ;  N,  ON,  optic  nerve 
fibres  ;  P,  p  nent  cells  ;  PS,  preretinal  space  ;  R,  retinal  (visual)  cells  ;  Rd,  rods  or 
rhabdites  ;   i        rhabdomes  ;   V,  hypodermal  cells  forming  vitreous. 


THE   SIMPLE   EYE 


141 


"vitreous"  mass  (Fig.  102)  (Berger,  1898;  Berger  and  Conant, 
1898-99).  The  lens  may  thus  be  aceUular  and  cuticular,  or  cellular  ; 
the  vitreous  cellular  or  gelatinous,  formed  either  a3  a  secretion  of  the 
retinal  cells  or  by  their  degeneration  and  coalescence. 

An  interesting  modification  is  seen  in  the  stemmata  or  simple  eyes 
of  the  larval  and  pupal  forms  of  some  insects  such  as  sawflies  (Ten- 
thredinidse)  and  many  beetles  (Coleoptera)  as  well  as  in  the  ocelli  of 
most  adult  insects,  in  the  lateral  eyes  of  the  scorpion  (Figs.  108-9),  and 
the  median  eyes  of  the  king-crab,  Limulus  (Fig.  142)  ;  in  these  the 
visual  cells  are  arranged  in  loose  groups  of  two  or  three  around  a  rod- 
like structure  secreted  by  the  visual  cells — the  rhabdome  (/ia^Sajyiia, 
a  rod).  Such  an  arrangement  does  not  alter  the  essential  simplicity 
of  the  eye. 

It  has  been  suggested  that  some  accommodative  adjustment  of  a 
static  type  may  be  provided  in  these  eyes  by  the  existence  of  differences 
in  the  distance  between  the  sensory  cells  and  the  lens  (some  flies,  as 
Helojjhilus)  (Fig.  106)  (Hesse,  1908). 

THE    VESICULAR    ETE 

The  final  stage  in  the  evolution  of  the  simple  eye  is  the  closure  of 
the  invaginated  epithelium  to  form  an  enclosed  vesicle  divorced  entirely 
from  the  surface  ectoderm  and  usually  separated  from  it  by  mesen- 
chyme. In  its  simplest  form  such  an  eye  is  merely  a  spherical  vesicle 
lined  with  ectodermal  cells  ;    the  cells  of  the  proximal  (deep)  part  of 


Helophilus 


Fig.   110. — The  Vesicular  Eye. 

The  ocellus  of  the  edible  snail. 

Ep,    epithelium  ;     vs,    visual    cell  ;     pc,    pigment    cell  ;     n,   nerve    (after 
Hesse). 


142 


THE   EYE   IN   EVOLUTION 


Buccinum 


Helix 


the  vesicle  are  partly  light-sensitive,  partly  secretory,  the  former  being 
frequently  associated  with  pigment  and  connected  by  nerve  fibres  with 
the  oi^tic  or  cerebral  ganglion  ;  the  distal  (superficial)  elements  are  rela- 
tively undifferentiated,  and  a  refractile  mass  of  secreted  material, 
homologous  M'itli  the  vitreous  of  higher  types,  fills  the  cavity.  Such  a 
simple  ocellus,  lying  in  the  subepithelial  tissues  over  which  the 
epithelium  passes  without  interruption,  is  seen  most  particularly  in 
Gastropods  such  as  Murex  which  furnished  the  Tyrian  purple,^  the 
common  whelk,  Buccinum,  or  the  edible  snail,  Helix  pomatia  (Fig. 
110). 

Its  most  elaborate  form  is  seen  in  tlie  spider-  or  scorpion-shell,  Pterocera 
lamhls,  a  gastropod  found  on  tropical  reefs,  wherein  the  vesicle,  filled  with  a 
vitreous-like  material,  has  a  clear  tlistal  wall  (a  cornea),  while  the  proximal  part 


a 


i'iu.    111. — TiiK  Ketina  of  Ptehoceua  lambis. 

The  retina  contains  four  layers  :  (a)  a  layer  of  rods  ;  (b)  a  layer  of  pigment 
cells  containing  some  rod  nuclei  ;  (c)  a  cellular  layer  in  which  are  distin- 
guishable most  of  the  rod  nuclei,  bipolar  cells,  a  few  horizontal  cells,  ganglion 
cells  and  supporting  cells  with  a  reticulum  resembling  Midler's  fibres  in  tlie 
vertebrate  retina  ;    (d)  a  layer  of  optic  ner\e  fibres  (J.  H.  Prince). 


of  the  vesicle  is  occupied  by  a  retina  consisting,  according  to  Prince  (1955),  of 
4  layers — (a)  most  distally,  a  layer  of  rod -like  visvial  cells,  (6)  a  layer  of  pigment 
cells,  (c)  a  cellular  layer  containing  the  nuclei  of  the  rods,  synaptic  "bipolar", 
"  horizontal  "  and  ganglion  cells,  and  {d)  a  layer  of  ojjtic  nerve  fibres,  the  axons 
of  the  ganglion  cells  which  leave  the  eye  in  nvimerous  optic  nerve  bundles 
(Figs.  Ill  and  189).  With  a  receptor  population  ajaproaching  10,000  per  scj.  mm., 
the  sensitivity  of  the  eye  is  j^robably  considerable  although,  in  the  absence  of  an 
efficient  optical  system,  image -format  ion  must  be  verj^  deficient. 

In  a  further  stage  of  complexity  a  lens  is  added  to  the  vesicular 
eye  so  as  to  form  a  camera-like  eye  resembling  that  of  vertebrates  ; 
an  accommodative  mechanism  and  an  extra-ocular  musculature  are 
provided.  This  is  typically  seen  in  two  very  different  phyla  :  among 
the  Polychsetes  in  the  family  of  Alciopidae,  and  among  the  Cephalopods 
whic>    have  the  most  elaborate  eyes  in  the  invertebrate  kingdom. 

^  Set?  Singer,  The  Earliest  Chemical  Industry,  London,  pp.  12-14  (1948). 


THE    STIMPLE   EYE 


143 


The  remarkable  eyes  of  the  Alciopidse,  a  family  of  pelagic  polychsetes 
{Alciopa,  Vanadis,  etc.),  have  received  considerable  study  ^  (Fig.  112).  In  these 
worms  the  proximal  part  of  the  vesicle  is  occupied  by  a  retina  with  direct 
receptors  ;  the  main  body  of  the  vesicle  contains  a  vitreous-like  mass  of  two 
consistencies,  separating  the  retina  from  the  anteriorly  situated  lens.  The 
posterior  portion  of  the  vitreous  is  jelly-like  and  is  secreted  by  the  intercalary 
cells  of  the  retina  ;  the  distal  portion  is  derived  from  a  glandular  cell  situated 
ventrally.  There  is  an  effective  accommodative  mechanism  -  and  the  eyes  are 
moved  by  3  extrinsic  muscles.  Nothing  is  known  about  the  function  of  these 
elaborate  eves. 


Fig.   112. — ^The  Eye  of  the  Polych.ete  Worm,   Va.\adi^. 

BV,  blood  vessels  ;  CT,  connective  tissue  ;  DV,  distal  vitreous  ;  G, 
ganglion  cells  ;  GC,  glandular  cell  secreting  the  distal  vitreous  ;  L,  lens  ; 
ON,  optic  nerve  ;  NF,  optic  nerve  fibres  ;  PR,  proxiinal  retina  ;  PV,  proximal 
vitreous  ;  R,  main  retina  showing  the  rods  separated  from  the  visual  cell-bodies 
by  a  dense  line  of  pigment  (after  Hesse). 


The  eyes  of  the  dibranchiate  cephalopods  (cuttlefish,  squids,  octojxis,  etc.) 
have  received  a  considerable  amount  of  study  (Figs.  113,  114).^  The  two  eyes 
are  set  on  pedicles  on  either  side  of  the  head,  and  are  partly  enclosed  in  a  dense 
supporting  envelope  reinforced  with  cartilage.  The  vesicle  is  filled  with  a 
vitreous  secretion  ;  the  cells  lining  its  proximal  portion  form  the  retina  ;  the 
distal  portion  fuses  with  an  invagination  of  the  surface  epithelium  to  form  a 
composite  spheroidal  lens,  the  inner  half  of  which  is  thus  made  up  of  vesicular 
epitheliuiB,  the  superficial  half  of  surface  epithelium.  On  either  side  of  the  lens 
the  fusion  of  these  two  layers  forms  a  doiible  epithelial  layer — a  "  ciliary  body  " 
— and  then  the  surface  epithelium  turns  upon  itself  to  form  an  "  iris  "  before 

1  Greef,  187.5-77  ;    Demoll,  1909  ;    v.  Hess,  1918  ;    Pflugfelder,  1932. 

«  p.  591. 

3  See  Scarpa  (1789),  Cuvier  (1817),  Soemmerring  (1818),  Krohn  (1835-42),  Hensen 
(1865),  Schultze  (1869),  Patten  (1886),  Carriere  (1889),  Grenacher  (1895),  Hesse  (1900-2), 
Merton  (1905),  Butschli  (1921),  Alexandrowicz  (1927),  Heidermanns  (1928),  and  others. 


144 


THE   EYE   IN  EVOLUTION 


Figs.   113  and   114. — The  Eye  of  a  Typical  Cephalopod. 

e 


Fig.   113. 

Invaginated  epithelium  forms  the  optic  vesicle  (a)  lined  by  the  retina  (b), 
the  posterior  layer  of  the  "  ciliary  body  "  (c),  and  the  posterior  part  of  the 
lens  (d).  The  surface  epithehum  i'orms  the  cornea  (e),  the  anterior  part  of  the 
ciliary  body  (/  ),  the  iris  (t),  and  the  anterior  part  of  the  lens  (g),  a  hole  (h) 
being  left  at  the  point  of  invagination.  The  eye  is  surrounded  by  a  carti- 
laginous orbit,  formed  by  an  anterior  cartilage  (k),  an  equatorial  cartilage  (I), 
and  an  orbital  cartilage  {m).     n  is  the  optic  nerve. 


Fig. 


— The  eye  of  Octopus  vulgaris  (specimen  from  J.  Z.  Young). 


THE   .Si:\irLE   EYE 


145 


invaginating  to  line  a  volummous  cul-de-sac  extending  far  posteriorly.  Over  this 
the  transparent  surface  epithelium  forms  a  "  cornea",  sometimes,  in  Myopsidse, 
forming  a  continiiovis  layer  in  which  case  the  cul-de-sac  (the  "  anterior  chamber  ") 
is  filled  with  an  "  aqueous  humour  "  (cuttlefish.  Sepia  ;  squid,  Loligo),  some- 
times, in  CEgopsidae,  perforated  by  a  hole  so  that  the  cavity  is  flushed  by  seawater 
(Octopus).  The  iris  is  supported  by  a  plate  of  cartilage  and  both  it  and  the 
ciliary  body  are  provided  with  contractile  muscular  tissue.  The  pupil  is  rect- 
angular in  shape  and  actively  contractile  and  there  is  an  efficient  accommodative 
mechanism  ^  (v.  Hess,  1909)  ;   while  covering  the  iris  and  extending  some  distance 


Sepia 


is 


Fig.   115. — The  Retina  of  the  Octopus. 

The  retina  is  composed  primarily  of  a  single  layer  of  visual  cells  with 
rod-like  terminations,  r,  and  nuclei,  n.  Between  the  rods  and  the  cell-bodies 
there  is  a  dark  line  of  pigment,  p,  and  at  the  proximal  extremities  of  the  rods 
a  layer  of  protective  pigment,  pp.  Most  externally  there  is  a  layer  of  nerve 
fibres,  /,  with  ganglion  cells.  The  white  line  underneath  the  pigment  is  an 
artefact  at  the  site  of  a  supporting  membrane  (  X  150)  (froin  a  specimen  of 
J.  Z.  Young). 

posteriorly,  is  a  silvery  membrane  of  pavement  epithelium  which  glitters  and 
shines  like  mother-of-pearl  (Figs.  116-17  ;   Fig.  192). 

The  retina  itself  is  coiTiprised  in  the  main  of  visual  cells  sujDported  by  two 
limiting  membranes — an  internal  membrane  lining  the  cavity  of  the  vesicle  and 
an  external  membrane  dividing  the  retina  transversely  into  two  (Fig.  115).  The 
visual  cells  are  made  up  of  two  elements,  a  rod -like  termination  and  a  cell -body. 
The  rods  lie  between  the  two  membranes  in  palisade  arrangement  ;  they  are 
constricted  as  they  pierce  the  external  membrane,  proximal  to  which  lie  the 
cell-bodies  with  their  nuclei,  the  visual  pathway  being  continued  by  nerve 
fibres  running  in  an  optic  nerve  to  an  optic  ganglion.-  Prince  (1956)  described 


■)90. 


p.  52 


Loligo         -^^    - 


Octopus 


S.O. — VOL.  I. 


146 


THE   EYE   IN   EVOLUTION 


Eledone 


bipolar  cells  and  ganglion  cells  in  the  nuclear  layer  proximal  to  the  pigmented 
layer.  A  considerable  amount  of  pigment  is  found  in  association  with  the 
visual  cells  which  is  most  abundant  near  the  narrow  neck  of  the  cell  between  the 
rod  and  the  cell-body,  and  in  some  species  at  any  rate,  it  is  claimed,  migrates 
towards  the  extremities  of  the  rods  in  bright  light  {Eledone — Rawitz,  1891). 

Such  an  eye  is  thus  a  highly  complex  organ  capable  of  image-formation  and 
structurally  equipped  to  mediate  pattern-vision,  able  to  accommodate  over  a 
considerable  range  and  possessed  of  some  power  of  adaptation.  Indeed,  in  one 
species,  Bafkyteiifhis,  the  elements  of  a  central  retinal  area  become  apparent  since 


Figs. 


116   AND    117. — The   Pupils   of   Cephai.opods    in    Various    Stages 
OF  Contraction. 


Fig.   116. — The  pupil  of  the  octopus. 


Cj 


Fig.   117. — The  pupil  of  the  cuttlefish,  Sepia. 

the  rods  are  greatly  elongated  as  if  to  form  a  primitive  area  centralis,  a  differen- 
tiation suggesting  the  existence  of  a  fixation  mechanism  endowed  with  con- 
siderable visual  sensitivity  (Chun,  1903). 


The  Inverted  Retina 

A  peculiar  form  of  simple  eye  is  associated  with  an  inverted  (or 
inverse)  retina,  that  is,  a  retina  wherein  the  visual  cells  are  orientated' 
so  that  their  sensory  ends  are  directed  away  fro7n  the  incident  light.  As  a 
rule,  inversion  of  the  retina  is  associated  with  a  secondary  invagination 
of  the  optic  vesicle.  In  the  usual  form  of  verted  (or  converse) 
retina,  as  we  have  seen,  the  cells  lining  the  proximal  (deep)  portion  of 
the  vesicle  form  the  visual  cells  and  their  orientation  is  quite  straight- 
forward ;  their  receptive  elements  face  the  surface  and  the  optic  nerve 
fibres  lead  directly  away  from  their  proximal  ends  (Figs.  118,  120).  In 
some  cases,  however,  the  cells  lining  the  distal  (superficial)  portion  of  the 
vesicle  form  the  visual  cells  ;  since  the  receptive  elements  face  the 
inter,  of  the  vesicle,  the  light  must  traverse  the  cell-bodies  before  it 
reac.'i      the  end-organ,  and  the  nerve  fibres,  issuing  superficially,  must 


THE   SIMPLE   EYE 


147 


double  backwards  to  reach  the  o])tic  panghon  (Figs.  119-121).  In  such 
cases  the  proximal  cells  of  the  vesicle  usually  contain  an  absorbing  pig- 
ment, and  the  recejitive  ends  of  the  visual  cells  approximate  closely  to 
them,  thus  reducing  the  vesicle  to  a  slit-like  potential  cavity.  An 
arrangement  which  might  at  first  sight  seem  anomalous  thus  acquires  a 
distinct  biological  value.  Moreover,  in  many  species  a  reflecting  crys- 
talline layer,  or  tapetum,  is  found  next  to  the  receptive  ends  of  the  visual 


il'l-l-l-l-M-hi' 


Fig. 


118. — The   Verted    Retina   of 
THE  Vesicular  Eye. 


Fir.. 


119. — The  Inverted  Retina  of 
the  Vesicular  Eye. 


Fig.  120. — The  Arrangement  of  the 
Visual  Cells  in  the  Verted 
Retina. 


Fio.  121. — The  Simplest  Arrange- 
ment OF  THE  Visual  Cells  in  the 
Inverted  Retina. 


In   each   case   light    falls    upon    the    visual   cells   from   above    (modified   from 

Buxton,  li)12). 


cells  which  reflects  the  incident  light  backwards  so  that  it  traverses  the 
sensory  cells  a  second  time  thus  doubling  the  intensity  for  stimulation 
and  incidentally  giving  the  eye  a  metallic  sheen.  This  arrangement  is 
therefore  characteristic  of  animals  to  which  vision  in  dim  illuminations 
is  important . 

An  inverted  retina  of  this  type  is  typical  of  Vertebrates  but  is  rare 
among  Invertebrates,  being  seen  in  a  few  Molluscs  and  Arachnids. 

Among  MOLLUSCS  it  is  found  in  four  species — in  its  simplest  form  in 
the  pulmonate,  Onchidmm.  and  in  the  cockle,  Cardium.  and  in  its  most 
elaborate  form  in  two  bivalves,  the  scallop,  Pecten,  and  Spondylus. 
In  the  jDulmonate  mollusc,  Onchidium,  the  visual  cells  of  a  simple  vesi- 
cular eye  are  inverted  and  the  optic  flbres,  issuing  from  their  distal  ends, 
pierce  the  posterior  pole  of  the  vesicle  in  a  bundle  exactly  as  does  the 
optic  nerve  of  Vertebrates  (Fig.  122)  (Semper,  1883).  This  peculiar  eye 
is  also  unique  in  that  the  "  vitreous  "'  filling  the  optic  cavity  is  made  up 
of  a  small  number  of  enormous  cells.  In  Cardium  the  arrangement  of 
the  visual  cells  is  somewhat  similar  but  that  of  the  optic  nerve  fibres 


Cardium 


148 


THE   EYE   IN   EVOLUTION 


Pecten 


completely  different.  The  receptive  ends  of  the  visual  cells  lie  upon 
an  ectodermal  layer  of  pigment  cells  crowned  by  a  reflecting  tapetum, 
while  their  distal  ends  are  prolonged  as  nerve  fibres  which  run  over 
the  retina  towards  the  periphery  and  then  bend  backwards  circum- 
ferential ly  to  form  the  optic  nerve  which  issues  posteriorly. 

The  eye  of  Pecten  is  of  umisual  interest  (Fig.  123)  ^  ;  that  of  Spondylus  is 
similar.^  A  single  layer  of  epithelial  cells  forms  the  cornea,  underneath  this  is  a 
clear  cellular  lens,  and  posteriorly,  separated  from  the  lens  by  a  transverse 

Figs.   122  and   123. — Inverted  Retina  in  Molluscs. 


Fig.   122. — The  dorsal  eye  of  Onchidium. 
Showing  an  inverted  retina  pierced  by 
the  fibres  of  the  optic  nerve,  resembling 
the  arrangement  in  Vertebrates. 

CC,  connective  tissue  forming  the  cor- 
nea ;  Ep,  epithelium  ;  F,  fibrous  tissue 
capsule  ;  ON,  optic  nerve  ;  ONF,  optic 
nerve  fibres  ;  P,  pigment  layer  of  the 
retina  ;  R,  visual  cells  of  the  retina  ; 
V,  two  large  vitreous  cells  (after  Glad- 
stone). 


O.N. 

Fig.    123.— The  eye  of  Pecten. 

C,  cornea  ;  Ep,  surface  epithelium  ; 
G,  ganglion  cell  layer  of  the  retina  ; 
L,  cellular  lens  ;  ON,  optic  nerve  ; 
P,  layer  of  pigmented  cells  and  above  it, 
the  tapetum  ;  R,  layer  of  rods  ;  V, 
cavity  of  the  vesicle  ;  VS,  vascular 
sinus  (after  Hesse). 


Spondylus 


septum,  lies  the  flattened  optic  vesicle,  the  cavity  of  which  has  become  virtual. 
The  retina  itself  is  complicated.  The  proximal  (deep)  portion  of  the  vesicle 
consists  of  a  single  layer  of  cubical  pigmented  cells  covered  by  a  tapetum  ;  the 
more  superficial  portion  of  the  vesicle  consists  of  two  well-defined  layers — a 
proximal  layer  of  rod-like  visual  elements,  the  receptive  ends  of  which  point 
posteriorly  into  the  cavity  of  the  vesicle,  and  a  distal  layer  of  cells  (the  ganglion 
cell  layer  of  Patten,  1886)  through  which  pass  nerve  fibres  from  the  visual  cells 
as  they  run  towards  the  periphery  at  the  equatorial  region  whence  (as  in  Cardium) 
they  encircle  the  posterior  part  of  the  globe  to  form  the  optic  nerve  (Kiipfer, 

'   ^ee  Keferstein  (1862),  Patten  (1886).  Kalide  (1888),  Carriere  (1889),  Schreiner 
(1896).  .;psse  (1900-2). 
2  ■■       Hickson  (1882). 


THE   SIMPLE   EYE 


149 


1915).  It  is  interesting  that  in  studying  the  electrical  responses  in  the  eye  of 
Pecten,  Hartline  (1938)  found  that  the  distal  layer  of  the  retina  mediated  a 
strong  off-response  while  the  proximal  layer  discharged  impulses  whenever 
illuminated. 

In  AEACHNiDS,  ail  inverse  retina  is  seen  in  the  lateral  and  median 
posterior  eyes  of  spiders  (Araneida),  in  all  the  ocelli  of  pseudo -scorpions 
(Pseiidoscorpionidea).  in  the  lateral  eyes  of  whip-tailed  scorpions 
(Pedipalpi)  and  in  sea-spiders  (Pycnogonida).     Each  one  of  these  has  a 


Pseudo-scorpion 


Figs.   124  to   127. — Inverted  and  Semi-inverted  Retin.e  in  Arachnids. 


Fig.   124. — The  lateral  eye  of  a  whip- 
tailed  scorpion. 

C,  cuticular  lens  ;  X,  optic  nerve 
fibres  ;  T,  tapetum  (after  Versluys 
and  DenioU). 


Fig.  125. — -The  eye  of  a  sea-spider. 
C,  cuticle  ;  Ep,  the  hypodermal  cells,  the 
central  ones  of  which  become  extremely 
elongated  and  surround  the  retinal  cells,  V. 
In  the  distal  part  of  the  eye  they  give  rise  to 
the  cells  of  the  lens,  L,  and  in  the  proximal 
part,  to  the  tapetum,  T.  The  retinal  cells 
themselves  are  elongated  with  a  nucleus  in 
the  distal  part,  while  the  proximal  granular 
part  is  the  sensory  receptor.  Into  these  cells 
the  optic  nerve  fibrils,  OX,  ramify.  The 
whole  eye  is  surrounded  in  a  pigment  cap- 
sule, P  (after  Schlottke). 


Fig.  126. — The  lateral  eye  of  a  spider. 
C,   cuticular   lens  ;     X,    optic   nerve 
fibres  ;     T,    tapetum    (after    Versluys 
and  Demoll). 


Fig.  127. — The  median  eye  of  a  whip- 
tailed  scorpion. 

C,   cuticular   lens  ;     X,   optic   nerve 
fibres  (after  Versluys  and  Demoll). 


150 


THE   EYE   IN   EVOLUTION 


Sea-spider 


Web  spider 


Scorpion 


different  arrangement.  In  a  further  variation,  seen  in  the  median  eyes 
of  scorpions  (Scorpionidea)  and  in  the  median  eyes  of  whip-tailed 
scorpions,  the  visual  cells  are  doubled  upon  themselves  so  that  the 
base  of  the  cell  is  verted  and  the  sensory  end  inverted. 

The  simplest  arrangement  of  an  inverted  retina  in  Arachnids 
is  seen  in  the  lateral  eyes  of  whip-tailed  scorpions  (Fig.  124)  ; 
the  sensory  ends  of  the  inverted  visual  cells  rest  on  the  tapetum, 
directed  away  from  the  incident  light,  and  from  the  mid-point  of  the 
cell-bodies  the  nerve  fibres  emerge  to  run  to  the  periphery  whence  the 
optic  nerve  emerges  on  the  side  of  the  eye  (Versluys  and  Demoll, 
1923). 

A  different  arrangement  again  is  found  in  the  sea-spiders 
(Pycnogonids)  (Fig.  125).  In  these,  the  hypodermal  cells  secrete  a 
cuticular  lens  in  the  anterior  part  of  the  eye  and  a  reflecting  tapetum 
in  the  posterior  part.  The  visual  cells  are  unusually  interesting.  They 
are  large  and  triangular  in  shape,  the  apex  of  the  triangle  lying  on  the 
tapetum  ;  the  nuclei  are  placed  distally  at  the  base  of  the  triangle  and 
the  narrow  proximal  ends  filled  with  granular  material  form  the  receptive 
portion  of  the  cell.  The  arrangement  of  the  optic  nerve  fibres  is  unique 
for  they  interA^  eave  in  the  substance  of  the  large  retinal  cells,  reaching 
distally  towards  the  nuclei.^ 

An  ingenious  arrangement  which  probably  has  optical  advantages  is 
seen  in  the  lateral  and  posterior  median  eyes  of  web-spiders  :  the 
(anterior)  median  eyes  of  these  animals  have  direct,  verted  retinae  (Wid- 
mann,  1908).  In  the  former  the  sensory  portions  of  the  elongated  visual 
cells  point  proximally  to  lie  on  the  tapetum,  while  the  cell-bodies  are  bent 
on  themselves  at  an  angle  of  90°,  to  run  towards  the  periphery  of  the 
retina  where  the  nuclei  lie  (Fig.  126)  ;  this  portion  of  the  cell  does  not 
therefore  interpose  itself  in  the  path  of  incident  light  (Versluys  and 
Demoll,  1923). 

A  semi-inimied  retina  is  found  in  the  median  eyes  both  of 
scorpions  and  of  whip -scorpions.  Here  the  visual  cells,  grouped 
in  retinules  around  rhabdomes,  are  bent  upon  themselves  at  180°,  their 
nuclei  lying  proximally  next  to  the  tapetum  and  the  receptor  ends  of  the 
cells  being  bent  round  so  that  their  extremities  lie  alongside  the  nuclei  : 
here  again  there  is  the  optical  advantage  that  the  incident  light  does 
not  travel  through  the  bases  of  the  visual  cells  (Fig.  127)  (Scheuring, 
1913  ;   Versluys  and  Demoll,  1923). 

It  will  be  remembered  that  the  subepithelial  eyes  seen  most  typically  in 
platiarian  and  nemertine  worms  ^   wherein  the  visual  cells  dip  downwards  from 


'   ;  [organ   (1891),   Korsehelt   and    Heidei-    (1893),   Bouvier    (1913) 
Schlottke  (1933). 
"  P    134. 


Wiren    (1918), 


THE    SIMPLE    EYE 


151 


the  surface  into  a  cup  of  pigmented  cells,  and  the  conducting  prolongations  of 
the  cells  are  turned  towards  the  direction  of  the  incident  light,  have  the  con- 
figuration of  an  "  inverted  "'  retina.  In  a  sense,  also,  the  composite  simple  eyes 
of  Chsetognaths  and  some  of  the  smaller  Crustaceans  to  be  discussed  immediately 
are  also  of  this  type. 


AGGREGATE  EYES 

The  AGGREGATE  EYE  is  a  Suitable  name  to  designate  an  accumu- 
lation of  ocelli  so  closely  packed  that  they  bear  a  superficial  resemblance 
to  a  compound  eye  although  each  is  anatomically  separate.  Such  an 
arrangement  is  seen  in  its  most  simple  form  in  starfishes  (Plate  I),  in 
such  insects  as  the  male  Stylops  ^  or  in  Myriapods  (Fig.  210),^  in  which 
it  appears  as  a  cluster  of  ocelli. 


Stylops 


Figs.    128  and    129.     The  Aggregate  Eye  of   Braxchiomma   yEsicctoscM. 


Fig. 


128. — Cross-section  through  a  branchial  fila 
ment  of  the  worm. 


BV,  blood  vessel  ;  C,  cuticle 
F,  fibril  ;  L,  lens  ;  X,  nucleus  ; 
visual  cell  (after  Hesse). 


Fig.    129. — Axial    section 
through  two  ocelli. 

Car,  cartilage  ;   Cil,  cilia  ;   Ep,  epidermis  ; 
ON,  optic  nerve  ;    P,  pigment   cells  ;    R, 


An  entirely  difTerent  type  of  aggregate  eye  is  seen  in  the  branchial 
filaments  of  some  sedentary  polychsete  worms  and  in  certain  lamelli- 
branch  molluscs  wherein  the  organ  has  a  superficial  structural  resem- 
blance to  a  compound  eye  but  each  element  contains  only  one  sensory 
cell  (Figs.  175-6).  In  the  first  case,  the  eye  of  the  polychsete, 
Branchiomma  vesiculosum,  is  made  ujd  of  a  spherical  group  of  elements 
resembling  ommatidia,  but  since  each  contains  only  a  single  cell  it 
should  be  considered  an  ocellus  and  the  eye  is  technically  a  simple 
organ  of  the  aggregate  type  (Brunotte.  1888  ;  Hesse,  1896-99) 
(Figs.  128  and  129).  It  is  to  be  remembered,  however,  that  in  such 
tube-worms  these  structures  do  not  seem  to  be  essential  for  the  animal's 
characteristic  response  to  changes  in  light  intensity  (Millott,  1957). 
A  similar  arrangement  is  seen  in  the  eyes  of  the  lamellibranch  molluscs. 
Area  and  Pechmcidus  (Carriere,  1885  ;   Patten,  1886  ;   Hesse,  1900). 


Branchiomma 


221, 


'  P- 


110. 


152 


THE   EYE   IN   EVOLUTION 


COMPOSITE    OCELLI 

COMPOSITE  OCELLI  (SIMPLE  EYEs)  are  formed  by  the  fusion  of  two 
or  more  ocelli  each  with  its  own  retina  and  pigment  cnp,  a  process 
which   seems   to   have   arisen   independently   in   several   phyla  ;     in 


Figs.   130  to   132. — The  Composite  Ocellus. 


Cypris 


Fig.   130. — The  ocellus  of  Cypris. 


Fig.    131. — The  ocellus  of  Daphnia. 


The  unpaired  median  eye  represents  the  fusion  of  3  ocelli  (see  Fig.  228).  DL, 
dorso-lateral  ocelli;  VE,  ventral  ocellus;  P,  pigment  mantle;  V,  visual  cells; 
T,  tapetum  (after  Claus,  1891). 


EDIAL 


VENTRAL 

Fig.   132. — The  ocellus  of  the  chsetognath,  Spadella  exaptera. 
Showing  3  of  the  5  simple  eyes,  one  to  the  left  and  2  to  the  right,  arranged 
round  the  central  pigment,  P.     Ep,  epithelium  ;    V,  visual  cells  ;    R,  rods  ; 
N,  nerve  fibres  (after  Hesse). 

general,  the  fusion  is  associated  with  degeneracy  and  lack  of  use.  It  is 
interesting  that  the  same  cyclopic  tendency  is  seen  in  the  median 
(pineal)  eye  of  Vertebrates,  which  initially  was  a  paired  organ. ^  Among 
certain  smaller  Crustaceans,  lowly  types  which  have  undergone  much 
reduction  of  the  head  and  have  largely  lost  their  segmentation,  a 
median  unpaired  eye  is  a  characteristic  feature,  and  is  frequently 
composed  of  the  fusion  of  a  number  of  ocelli  arranged  in  a  somewhat 
similar  way  (the  Cladoceran,  Daphnia  ;  the  Ostracods,  Cypris  and 
Cypridina  ;  the  Copepod,  Cyclops)  (Figs.  130  and  131). ^  Among  the 
marine  arrow-worms  (Chsetognatha),  Spadella  has  two  composite  ocelli 
near  the  anterior  extremity  of  its  body,  each  organ  made  up  of  the 
fusioi!   >f  5  simple  eyes  of  the  cupulate  type  arranged  around  a  central 


Cyclops 


1  p.  711. 


p.  163,  Fig.  145. 


THE    SIMPLE    EYE 


153 


mass  of  pigment  which  sends  out  partitions  between  each  (Fig.  132) 
(Hesse,  1908).  In  such  eyes  the  receptor  ends  of  the  sensory  cells  are 
directed  inwards  towards  the  cup  of  pigment,  and  the  nerve  fibre  is 
peripheral  so  that  the  eye  may  be  considered  as  of  the  inverted  type 
(Vaissiere,  1955). 


Alexandrowicz.    Arch.  Zool.  exp.  gen.,  66, 

76  (1927). 
Berger.    J.  comp.  Xeurol.  Psychol.,  8,  -23 

(1898). 
Berger  and  Conant.     Johns  Hopk.   Univ. 

Circ,  Baltimore,  18,  9  (1898-99). 
Bhatia.     Nature  (Lond.),  178,  420  (1956). 
Bolwig.      Vidensk.  Medd.   Dansk.   naturh. 

Foren.,  109,  81  (1946). 
Bonnet.    Oewi'res,  Neiichatel  (1781). 
Bouvier.       Deu.xihne     exped.     antarctiqite 

frang.,  Paris,  1  (1913). 
Brunotte.     C.R.   Acad.  Sci.   (Paris),  106, 

301  (1888). 
Biitschli.      Vorlesungen   iiber  vergl.  Anat., 

Berlin,  817,  826,  872  (1921). 
Buxton.    Arch,    vergl.    Ophthal.,    2,    405 

(1912). 
Carriere.    Die  Sehorgane  der   Tiere,  Miin- 

chen  (1885). 
Arch.  mikr.  Anat.,  33,  378  (1889). 
Chun.      Verhdl.  dtsch.   Zool.   Ges.,   13,   67 

(1903). 
Cuenot.    Grasse's  Traite  de  Zool.,  Paris,  6, 

13  (1949). 
Cuvier.        Alew.    pour    servir    a    Vhistoire 

et  a  Vanntomie  des  mollusques,  Paris 

(1817). 
Demoll.      Zool.  Jb.,   Abt.   Anat.,  27,   651 

(1909). 
Galati-Mosella.     Monit.  Zool.  Hal.,  26,  75 

(1915);  27,  161  (1916);  28,  129  (1917). 
Greeff.     Sitz.   Ges.   Beforderung  Gesammt. 

Naturw.  Marburg,  115  (1875). 
Nova  Acta  Leopoldina,  39,  33  (1877). 
Grenadier.     Zool.  Anz.,  18,  280  (1895). 
Hartline.     J.  cell.  comp.  Physiol.,  11,  465 

(1938). 
Heidermanns.      Zool.      Jb.,      Abt.      Zool. 

Physiol.,  45,  609  (1928). 
Hensen.     Z.  wiss.  Zool.,  15,  155  (1865). 
Hertwig.     Das  Nervensysteni  ii.  die  Sinnes- 

organe  der  Medusen,  Leipzig  (1878). 
Die  Zelle  und  die  Gewebe.  Jena  (1893). 
V.  Hess.     Arch.  Augenheilk..  64,  Erg.,  125 

(1909). 
Pflilgers   Arch.    ges.    Physiol.,   122,  449 

(1918). 
Hesse.      Z.   uiss.    Zool.,   61,    393   (1896)  ; 

62,     671     (1897) ;      63,     361     (1898) ; 

65,    446    (1899) ;     68,    379    (1900) ; 

72,  565  (1902). 
Das    Sehen    der    )iiederen     Tiere,    Jena 

(1908). 


Hickson.      Quart.   J.    micr.   Sci.,    22,    362 

(1882). 
Imms.      Textbook  of  Entomology,  London 

(1935). 
Jourdan.       Les    sens    chez     les     animaux 

infer ieurs,  Paris  (1889). 
Kalide.    Zool.  Anz.,  11,  679,  698  (1888). 
Keferstein.    Z.  wiss.  Zool.,  12,  133  (1862). 
Korschelt  and  Heider.    Vergl.  Entwicklung. 

d.  Wirbellosen  Tiere,  Jena,  664  (1893). 
Krohn.    Nova  Acta  Acad.  Leop. -Carol.,  17, 

337  (1835)  ;    19,  41  (1842). 
Kiipfer.      Viertlj.  naturf.  Ges.  Zurich,  60, 

568  (1915). 
Maier.      Zool.  Jb.,   Abt.   Anat..   5,    8,    552 

(1892). 
Merton.     Z.  u-iss.  Zool..  97,  341  (1905). 
Millott.     Endeavour,   16,    19    (1957). 
Morgan.     Biol.  Stud.  Johns  Hopk.   Univ., 

5,  49  (1891). 
Patten.     Mitt.  zool.  Stat.  Neapel,  6,  568 

(1886). 
Pfliigfelder.     Z.     wiss.     Zool.,     142,     540 

(1932). 
Prince.      Texas  Rep.  Biol.  Med.,  13,  323 

(1955). 
Comparative      Anatomy      of     the      Eye, 

Springfield,  111.  (1956). 
Rawitz.      Arch.   Anat.    Physiol.    {Physiol. 

Abt.),  367  (1891). 
Scarpa.      Anatomical  disquisitiones,  Ticini 

(1789). 
Scheunng.     Zool.  Jb..  Abt.  Anat.,  33,  553 

(1913). 
Schlottke.    Z.  mikr.  Anat.  For.sch..  32,  633 

(1933). 
Schreiner.     Die  Augen  bei  Pecten  u.  Lima, 

Bergons  Museum  Aarbog  (1896). 
Schultze.     Arch.  mikr.  Anat.,  5,  1  (1869). 
Semper.    Int.  Sci.  Ser..  31,  371  (1883). 
Soemmerring,  D.  W.     De  oculorum  hominis 

aniynaliumque     etc.,    Goettingen,     76 

(1818). 
Vaissiere.     C.  R.  Acad.  Sci.  (Paris),  240, 

345  (1955). 
Versluys    and    Demoll.      Ergebn.    Fortsch. 

Zool.,  5,  66  (1923). 
Whitman.    J.  Mor;j/io/.,  2,  586  (1889). 

Zool.  Jb.,  Abt.  Anat.,  6,  616  (1893). 
Widmann.     Z.  wiss.  Zool.,  90,  258  (1908). 
Wigglesworth.    Parasitology,  33,  67  (1941). 
Wiren.       Zool.     Bidrag     Uppsala,    6,     41 

(1918). 


154 


THE   EYE   IN   EVOLUTION 


Fig.   133.— Johannes  Muller  (1801-18.18). 


The  Compound  Eye 

Nothing  could  be  more  suitable  to  introduce  this  section  on  the  anatomy 
and  physiology  of  the  compound  eye  than  the  portrait  of  Johannes  mxjllee 
(1801-1  :-^s  (Fig.  133),  Professor  of  Physiology  first  at  Bonn  and  then  at  Berlin, 
a  studeii  friend  and  collaborator  of  von  Helmholtz.  In  association  with 
Malpighi  ,  Haller,  he  may  be  considered  the  fovmder  of  the  great  German 
School  of   .        -iology   of  the    19th   century.      Throughout   his  relatively   short 


THE   COMPOUND   EYE 

career  he  contributed  lavishly  to  many  branches  of  biology  but  perhaps  the 
conception  for  which  he  is  best  remembered  is  the  law  of  specific  yierve  energies 
which  lays  down  that  each  organ,  however  stimulated,  gives  rise  to  its  own 
characteristic  sensation. ^^  His  enunciation  of  the  Mosaic  Theory  to  explain  the 
optical  properties  of  the  compound  eye  has  stood  the  test  of  time,  and  was  the 
first  scientific  explanation  advanced  on  this  subject  ;  Fig.  156  is  a  characteristic 
illustration  from  his  book.  His  classical  textbook  on  human  physiology  - 
crystallized  the  knowledge  of  his  day  in  a  vast  compendium  which  stimulated 
work  in  every  field  for  more  than  one  generation. 

The  compound  eye,  an  organ  peculiar  to  Arthropods,  has  evolved 
along  different  lines  from  the  ocellus.  In  the  former,  instead  of  being 
independent  of  each  other,  the  sensory  elements  are  structurally  and 
fnnctionaUy  associated  in  groups.  For  this  purpose  complexity  has 
been  attained  by  the  division  of  the  indi^•idual  sensory  cells  of  a  simple 


155 


Fig.   134. — The  Compound  Eye. 

Diagram  of  a  compound  eye  of  an  insect  with  a  sector  excised. 
a,  corneal  facet  ;    h,  crj'stalline  cone  ;    c,  surface  epithelium  ;    d,  matrix 
cells  of  cornea  ;    e,  iris  pigment  cell  ;   /,  cell  of  retinule  ;    g,  retinal  pigment 
cell  ;     h,   rhabdome  ;     ;',   fenestrated   basement   membrane  ;    _;,   nerves   from 
retinular  cells  ;    k,  lamina  ganglionaris  ;    /,  outer  chiasma. 


eye  to  form  a  coordinated  colony,  a  process  first  shown  to  occur  in  the 
development  of  the  stalkefl  eyes  of  the  shrimp,  Crangon,  by  Kingsley 
(1886)  and  confirmed  by  others  in  many  different  species.  Moreover, 
optical  imagery  has  been  attained  not  by  the  single  large  lens  charac- 
teristic of  the  ocellus  (or  of  the  vertebrate  eye)  which  by  attaining  an 
adjusting  mechanism  reached  its  highest  development  in  Cephalopods, 
but  by  ensheathing  each  individual  group  with  pigment,  thus  convert- 
ing the  eye  into  a  series  of  blackened  tubes  so  that  the  multiplicity  of 
images  increases  the  acuity  of  vision  by  a  mosaic  effect.  In  this 
arrangement  each  separate  element  is  called  an  ommatidium  {ofifnx, 

'    Zur  veryleicheiulen  Physiologie  <hr  GesiclitNtilnnes,  Leipzig,  1826. 
*  Handbuch  der   Physiologic  der  Menschen,    18.34-40,   translated   into   English   in 
Baly's  Elenieitts  of  Physiology,  London,  1838-42. 


156  THE   EYE   IN   EVOLUTION 

eye  ;    dim.  ofxixxTlSiov)  ;    the  typical  formation  of  the  whole  eye  is 
seen  in  Figs.  134  and  150. 

The  developnietit  of  ocelli  and  cotnpound  eyes  indicates  their  essential  kinship 
despite  their  outward  disjDarity  of  form.  The  oceUus,  as  we  have  seen,  originates 
as  a  hypodermal  pit,  the  superficial  cells  of  which,  infolding  under  the  cuticle, 
become  differentiated  into  a  refringent  apparatus,  the  deeper  cells  into  the 
retinal  elements.  Each  ommatidium  of  the  compound  eye  originates  some- 
what similarly  as  a  consolidated  pillar  of  hypodermal  cells  and  between  the 
pillars  lie  undifferentiated  cells  (Fig.  135)  ;  the  superficial  cells  of  these  pillars 
form  the  basis  of  the  corneal  facets,  the  crystalline  cones  and  primary  pigmented 
cells,  the  deeper  cells  develojD  into  the  retinviles,  while  those  between  the  pillars 
form  the  secondary  pigmented  cells.  In  both  cases  the  baseinent  membrane  is 
continuous  with  that  of  the  integument  (Patten,  1888-1912  ;    Johansen,  1893  ; 


A 


Fig.   135. — The  Development  of  the  Compound  Eye. 

An  early  stage  in  the  development  of  the  eye  of  the  pupa  of  the  moth, 
Saturnia  pernyi,  showing  the  ommatidial  pillars  (after  Bugnion  and  Popoff ). 

Bugnion  and  Popoff,  1914).  It  wovild  thus  seem  that  ontogenetically  as  well  as 
phylogenetically  the  two  types  of  eye  are  parallel  developments  from  some 
(unknown)  common  primitive  origin. 

While  ocelh  and  compound  eyes  show  this  kinship  in  development,  the  studies 
of  Watase  (1890)  and  Hanstrom  (1926)  would  indicate  that  they  have  a  different 
origin  ;  all  true  compound  eyes  arise  from  the  lateral  ectodermal  mass  in  the 
embryo,  while  ocelli  take  origin  from  either  the  dorsal  or  the  ventral  ectodermal 
mass.  Although  the  lateral  ocelli  of  modern  arachnids  and  all  the  eyes  of 
diplopods  and  chilopods  arise  from  the  lateral  mass,  Hanstrom  considers  them 
to  represent  degenerate  forms  of  the  ommatidia  of  compound  eyes. 

It  woiild  thus  seem  reasonable  to  assume  that  the  compound  eye  has  evolved 
from  the  simple  eye  at  an  early  period,  but  it  is  clear  that  the  first  is  not  an 
adaptive  modification  of  the  second  after  it  has  reached  an  elaborate  stage  of 
development.  It  is  true  that  intermediate  stages  are  extant — the  association 
of  the  sensory  cells  into  a  group  under  a  single  common  lens,  seen  in  the  simple 
ommatidial  e  of  some  larval  and  adult  insects  and  Copepods  (Fig.  138),  or  the 
multitubui.  rangement  of  the  aggregate  eye  wherein  each  element  contains  a 
single  senses        -U,  seen  in  some  polychsete  worms  (Fig.  128).     It  is  significant. 


THE   COMPOUND   EYE 


157 


however,  that  among  the  eai'Hest  fossils  known  to  man — the  Trilobites,  Arthro- 
pods which  crept  over  the  ooze  of  the  sea-bed,  and  the  Eurypterids,  enormous 
marine  spider-Hke  creatvires  sometimes  over  6  feet  in  length,  which  flourished 
in  the  Palaeozoic  era  more  than  300  million  years  ago  and  are  long  since  extinct — 
both  median  ocelli  and  lateral  compound  eyes  are  present  which  have  reached  a 
high  stage  of  complexity  (Figs.  136  and  137)  (Brink,  1951).  It  would  seem, 
therefore,  that  both  types  of  eye  were  derived  from  a  simple  ancestral  stock 


Fig.    136. — Reconstruction   of   the 
Fossil   Tbilobite,    ^^aiixA    prisca. 

On  the  glabella  {gl)  there  are  impres- 
sions of  a  median,  m,  and  paired  lateral 
ocelli,  /.  The  compound  eyes,  CE, 
are  very  large  (after  Barrande). 


Fig.    137. — Reconstbuction    of   the 
Fossil      Eubypterid,     PiERraoTUS 

AyCLlCU.'i. 

An  ancient  extinct  Arachnid  found 
in  the  Old  Red  Sandstone  rocks  in 
Scotland.  It  is  possessed  of  elaborate 
compound  eyes,  E,  as  well  as  two 
dorsal  ocelli,  Oc. 


before  the  beginning  of  known  geological  time,  that  each  has  evolved  in  its  diffe- 
rent way  along  diverging  lines,  and  that  their  general  form  as  seen  today  has  been 
essentially  the  same  since  the  early  Pakeozoic  period.^ 


The  Structvre  of  the  Co7npou7id  Eye 

The  essential  structure  of  each  ommatidiuin  is  relatively  simple. 
Most  superficially  the  cuticle  forms  a  corneal  facet  (Fig.  134) 
underneath  lies  the  crystalline  cone,  usually  with  two  convex 
surfaces,  the  two  together  acting  as  a  light-collecting  system.  The 
remainder  of  the  organ  is  occupied  by  the  sentient  elements  arranged 
in  tubular  form  ;  this  associated  grouj)  of  cells  is  called  the  retinule 
the  cells  of  which  rest  upon  a  fenestrated  basement  membrane  and  are 
arranged  so  that  their  differentiated  inner  borders  together  form  a 

1  Compare  p.  754. 


158  THE    EYE    TN    EVOLUTION 

central  refractile  rod,  the  rhabdome.  The  rhabdome  is  a  product  of 
the  collective  secretion  of  the  cells  of  the  retinule  and  has  a  light - 
conducting  function  ;  presumably  in  its  substance  photochemical 
changes  occur,  the  products  of  which  stimulate  the  neighbouring 
retinular  cells,  but  the  nature  of  the  absorbing  pigments  has  not  yet 
been  elucidated.  The  entire  group  of  ommatidia,  each  individual  of 
which  is  separated  in  some  degree  from  its  neighbour  by  a  mantle  of 
pigment  cells,  constitutes  the  compound  eye,  the  surface  being  made 
up  of  the  corneal  facets  fitting  into  each  other  to  form  a  mosaic  (hence 
the  common  name  "  faceted  "'  eye),  and  the  retinules  together  forming 
the  retina.  The  structure  would  therefore  suggest  that  Hght  striking  a 
retinule  stimulates  it  as  a  whole  and  produces  a  single  sensation,  and 
consequently  the  great  advance  in  the  development  of  the  compound 
eye  is  the  coordination  of  individual  elements  in  a  unity  of  function. 
The  mosaic  of  vision  is  made  up  of  the  images  from  the  individual 
ommatidia  of  which  there  may  be  few  or  many,  each  of  which  acts  in 
the  same  way  as  a  single  retinal  cell  of  the  simple  eye.  As  in  the 
ocellus,  the  entire  structure  is  derived  from  the  surface  ectoderm. 

The  sensory  mechanism  of  the  compound  eye  is  not  at  all  clear  for  on  this 
subject  much  research  yet  remains  to  be  done.  Most  authorities  accept  that 
the  retinular  cells  are  the  photosensitive  elements  ^;  these  form  a  characteristic 
complex  for  any  given  species  and  are  precisely  arranged,  usually  7  or  8  in  number 
but  varying  from  4  to  20  in  different  species  of  Arthropods.  It  used  to  be 
generally  accepted  that  each  retinular  cell  was  a  primary  neurone,  and  certainly 
each  extends  proximally  as  an  axon  which  terminates  synaptically  in  optic 
ganglia  or  nuclei  ;  but  the  interesting  thing  is  that  on  the  few  occasions  in  which 
the  matter  has  been  experimentally  explored,  no  conducted  action  potentials 
have  ever  been  demonstrated  in  these  cells  or  their  axons  (Bernhard,  1942  ; 
Antrum  and  Gallwitz,  1951).  In  the  king-crab,  Limulus,  it  has  long  been  known 
that  only  one  active  fibre  can  be  detected  in  the  whole  bundle  of  axons  emerging 
proximally  from  the  retinule  (Hartline  and  Graham,  1932  ;  Hartline  et  al., 
1952-53),  and  Waterman  and  Wiersma  (1954)  have  brought  forward  significant 
evidence  that  this  activity  is  associated  with  a  characteristic  eccentric  cell  one 
of  which  is  found  in  each  ommatidivnn.  In  Crustaceans  little  work  has  been 
done  germane  to  this  problem,  but  it  would  seem  that  the  electronic  spread  of 
retinal  potential  travels  towards  the  first  optic  ganglion  without  giving  rise  to 
any  spikes  (Hanaoka,  1950).  In  these  and  in  Insects  the  conducting  neurones 
may  be  located  in  the  first  optic  ganglion  (the  lamina  ganglionaris)  ^  which  lies 
immediately  under  the  basement  membrane  of  the  retina.  In  Insects  there  are 
also  units  comparable  to  the  eccentric  cells  of  Limulus,  the  axons  of  which  do 
not  terminate  with  those  from  the  retinular  cells  in  the  first  optic  ganglion  but 
in  the  next  more  proximal  ganglion  (Cajal  and  Sanchez,  1915  ;  Hanstrom,  1927). 
The  evidence  available  to-day  would,  indeed,  suggest  the  somewhat  surprising 
deduction  that  although  the  photosensitive  region  is  near  the  rhabdomes  of  the 

•  Aci'  ling  to  Berger  and  Courrier  (1952)  the  photoreceptors  in  the  eyes  of  Insects 

are  situate  t  the  bases  of  the  rhabdomes  and  are  not  represented  by  the  longitudinal 

cells  usuaL  signated  as  "  sensory  ". 

"  p.  5l 


THE   COMPOUND   EYE 


159 


retinular  cells,  the  axons  of  these  cells  do  not  conduct  impulses  even  although 
they  form  the  majority  of  the  fibres  of  the  optic  nerve,  while  this  function  is 
taken  over  by  other  structures  analogous  to  the  bipolar  cells  of  the  vertebrate 
retina,  the  electronic  potentials  induced  by  the  primary  i-eceptor  process 
giving  rise  to  propagated  impulses  in  closely  contiguous  conducting  neurones. 
It  is  obvious  that  many  fascinating  problems  still  remain  to  be  elucidated. 

As  in  other  evolutionary  processes  it  cannot  be  said  that  a  ciit- 
and-dried  differentiation  exists  between  the  simple  and  the  compound 
eye.  Intermediate  forms  between  the  two  may 
be  seen  in  some  worms.  On  the  one  hand,  as  we 
have  already  seen,i  some  sedentary  poly  chaste 
worms  and  lamellibranch  molluscs  are  provided 
M  ith  structures  superficially  resembling  a  com- 
pound eye,  but  since  each  element  contains  a 
single  visual  cell  they  are  more  correctly  termed 
AGGREGATE  EYES.  On  the  other  hand,  the 
stemmata  of  the  larvse  of  most  holometabolous 
insects  and  the  lateral  ocelli  of  many  adult 
types  such  as  butterflies  and  moths  (Lepidop- 
tera)  and  all  the  ocelli  of  springtails  (Collem- 
bola)  have  structures  somewhat  resembling  the 
single  ommatidium  of  a  compoimd  eye,  consist- 
ing of  a  cornea,  a  crystalline  lens  and  seven 
retinular  cells  arranged  around  a  central 
rhabdome  (Dethier,  1942-43  ;  and  others)  ; 
such  an  arrangement  may  be  called  a  simple 
OMMATiDiAL  EYE  (Fig.  138).  The  ventral  eye 
of  Copepods  forms  a  similar  intermediate  step 
between  an  ocellus  and  an  ommatidium. 
Thus  the  female  Ponfellojjsis  regalis,  for  ex- 
ample, has  an  eye  composed  of  a  single  retinule  of  6  cells  arranged 
in  two  groups  of  3  (Vaissiere,  1954),  while  Copilia  and  its  relatives  have 
a  single  group  of  3  cells  arranged  around  a  rhabdome  (Grenacher, 
1879-80  ;  Exner,  1891). 

These  tiny  crustaceans  have  unique  eyes  (Fig.  139)  ;  each  is  almost  half 
as  long  as  the  body  and  is  pulled  about  in  all  directions  with  great  rapidity 
by  muscles,  a  device  presumably  designed  to  increase  its  visual  field.  Moreover, 
the  optic  nerve  issues,  not  from  the  proximal  end  of  the  ommatidium,  but  from 
its  side.  A  similar  point  of  exit  for  the  optic  nerve  from  the  middle  of  the  lateral 
wall  of  the  visual  cells  is  seen  in  the  anterior  median  ocelli  of  the  common  house 
spider,  Tegenaria  domestica  (Biitschli,  1921)  (Fig.  107). 

True  compound  eyes,  however,  are  seen  only  among  the  Arthro- 
pods.     They   occur  in  several  fossil  forms   (Trilobites,   Eurypterids, 


Fig.  138.— The  Simple 
Ommatidial  Eye  of 
THE  Larva  of  the 
Moth,  Gaxtropacha 

RUBI. 

A  lens  and  retinule  are 
arranged  after  the  man- 
ner of  a  single  omma- 
tidium (after  Demoll). 

C,  corneal  lens  ;  Ep, 
epithelial  cell  ;  L,  lens  ; 
M,  mantle  cell  ;  R,  R, 
visual  cells  ;  Rh,  rhab- 
dome ;    V,  vitrellfe. 


Copilia 


Tegenaria 


p.  151. 


160 


THE   EYE   IN   EVOLUTION 


Scutigera 


Phronirna 


Dineutus 


Stylocheiron 


Cut 


Chilopods  and  Diplopods),  in  the  centipede,  Saifigem,  and  its  close 
allies  ;  in  Arachnids  an  atypical  form  occurs  in  the  lateral  eyes  of  the 
king-crab,  but  their  full  development  is  characteristic  of  Crustaceans 
and  Insects,  in  which  they  are  found  in  the  most  varied  forms.  Of 
these,  the  most  elaborate  is  the  composite  compound  eye  wherein 
the  organ  is  formed  by  the  apparent  fusion  of  two  compound  eyes, 
usually  a  frontal  and  a  lateral. 
Among  Crustaceans  this  is  seen  in 
pelagic  Schizopods  (Hesse,  1908),  or 
in  some  Amphipods  such  as  Phronirna 
sedentaria  (Claus,  1879).  Among 
Insects  a  frontal  and  lateral  combina- 
tion is  seen  in  some  flies  (Diptera) 
and  mayflies  (Ephemeroptera),  a 
dorsal  and  ventral  in  wasps 
(Vespoidea)  and  longhorn  beetles 
(Cerambycidse)  (Fig.  140).  Such  an 
arrangement  undoubtedly  increases 
the  visual  field  and  may  also  serve  as 
an  accommodative  device  providing 
two  focusing  mechanisms,  one  anato- 
mically adjusted  for  distant  and  the 
other  for  near  vision  (Dietrich,  1909  ; 
Weber,  1934).  A  further  example  is 
the  dorsal  and  ventral  eyes  of  the 
whirligig  beetle,  Dineutus,  the  former 
for  aerial  vision  and  the  latter  for 
vision  under  water  (Fig.  231). 

A  final  complication  is  seen  in  some 
abyssal  Crustaceans  wherein  a  frontal 
portion  of  the  compound  eye  contains  few 
ommatidia  provided  with  little  pigment, 
obviously  adapted  for  dim  light,  a  lateral 
portion  has  many  small  ommatidia  each  of 
which  is  ensheathed  in  pigment  so  as  to  be 
effective  in  brighter  light,  while  immediately 
below  this  a  third  part  is  adapted  as  a 
luminous  organ  ^  {Stylocheiron  mastigo- 
phorum— Chun,  1896)  (Fig.  141). 


Fig.  139. — The  Eye  of  the 
CoPEPOD,  CopiLiA  (foreshort- 
ened). 

Cut,  cuticle  ;  L,  lens  ;  N,  nerve 
fibre  to  epidermis  ;  C,  crystalline 
cone  ;  O,  optic  nerve  ;  R,  rhab- 
dome  with  surrounding  sensory 
cells,  encased  in  a  pigment  mantle  ; 
M,  muscle  ;  A,  antennae  (after 
Grenacher). 


THE  COMPOUND  EYES  OF  ARACHNIDS 

In  general  Arachnids  are  provided  with  ocelli,  but  in  a  few  cases — 
the  scorpion,  the  median  eyes  of  the  whip-scorpion  and  of  the  king-crab — 
the  eye  is  of  the  type  wherein  the  visual  cells  are  arranged  in  groups, 

1  p.  736. 


THE   COMPOUND   EYE 


161 


Figs.   140  and   141. — The  Composite  Compound  Eye, 


Fig.   140. — Frontal  section  of  the  eye  Fig.    141. — The    faceted    eye     of   the 

of  the  male  April  fly,  Bibio  marci.  Schizopod,       Stylocheiroyi       mastigo- 

F,  frontal  eye  ;    L,  lateral  eye  (after  phorum. 

Hesse).  F,    frontal    eye  ;     L,    lateral    eye  ; 

c,  corneal  lens  ;  k,  crystalline  cone  ; 
r,  rhabdomes.  The  luminous  organ  is 
not  shown  (after  Hesse). 

each  around  a  rhabdome,  the  whole  collection  lying  underneath  a 
common  lens  (Fig.  142).  The  large  lateral  eyes  of  the  king-crab, 
however,  are  unique  and  merit  a  special  description. 

The  compound  (lateral)  eyes  of  the  king-crab,  Limulus,  are  of  a 
relatively  simple  but  unique  structure,  but  are  of  unusual  interest  since 
they  have  been  widely  used  by  Hartline  and  his  collaborators  as  a 
means  of  studying  the  electrical  activity  of  photoreceptor  cells  ;  their 
choice  was  determined  by  the  fact  that  one  fibre  only  of  the  optic 
nerve  apparently  acts  as  a  conductor  on  stimulation  of  an  ommatidium. 
A  considerable  amoimt  of  work  has  been  done  on  the  minute  structure 
of  this  eye,  but  some  points  in  the  anatomy,  particularly  of  its  nervous 
connections,  still  remain  obscure  ^  (Fig.  143). 

Although  the  ej'e  show  s  wide  differences  in  size  and  complexity  of  structure 
with  growth  and  between  species  (Waterman,  1954),  as  a  rule  it  consists  of  some 
600  ominatidia,  the  whole  being  covered  with  a  continuous  corneal  stratum  of 
transparent  chitin  ;  on  its  inner  surface  this  presents  a  series  of  papilliform 
downgrowths  which  act  as  corneal  lenses  to  the  barrel-shaped  retinules  which 

1  See  Lankester  and  Bourne  (1883),  Watase  (1890),  Miller  (1952),  Waterman  and 
Wiersma  (1954). 

S.O.— VOL.  I.  11 


Limulus 


162 


THE   EYE   IN    EVOLUTION 


Figs.  142  to  144. — The  Eyes  of  the  King-crab,  Limulvs  polyphemus. 


Fig.   142. — The  median  eye. 


ONF 
Fia.   143. — The  lateral  eye. 


Ch,  chitinous  carapace,  with  the  iDajoilla-like  thickening  forming  a  lens,  L  ; 
Ep,  hypodermal  epithelial  cells  ;  ONF,  optic  nerve  fibres  ;  R,  retinal  cells  ; 
V,  continuation  of  the  hypodermal  cells  to  form  a  vitreous  lamina  (after 
Lankester  and  Bourne). 


Fig.  144. — Section  of  the  lateral  eye. 
Tangential  section  through  the  retina.  The  top  ommatidium  is  cut  perpen- 
dicular to  the  longitudinal  optic  axis.  Each  retinule  consists  of  a  cluster  of 
cells  (10  to  15  in  number)  arranged  round  the  darkly  staining,  star-shaped 
rhabdome.  The  left-central  ommatidium  was  sliced  obliquely  and  more 
proximally  and  shows  the  body  of  the  eccentric  cell  running  into  the  axial 
canal  of  the  central  rhabdome  towards  1  o'clock  (Waterman  and  Wiersma, 
J.  exp.  ZooL). 


THE   COMPOUND   EYE 


163 


lie  directly  beneath  them.  The  retinule  contains  two  types  of  cell.  The  main 
mass  is  made  up  of  about  a  dozen  elongated  sensory  cells  grouped  round  central 
rhabdomes,  their  prolongations  giving  rise  to  fibres  which  mingle  in  a  plexus 
before  they  emerge  to  run  proximally  in  the  optic  nerve  (Fig.  144).  In  each 
retinule  there  is  also  one  eccentric  cell  the  axon  of  which  travels  down  the  central 
rhabdome  and  along  the  nerve  ;  it  would  seem  probable  that  this  forms  the 
conducting  element  for  nerve  imiDulses  set  up  by  stimulation  of  the  retinular 
cells  (Hartline  et  al.,  1953  ;  Waterman  and  Wiersma,  1954). ^  A  white  pigmented 
strvicture,  the  rudimentary  eye,  lies  behind  the  posterior  margin  of  the  compound 
eye  and  sends  a  third  type  of  large  nerve  fibre  into  the  optic  nerve  (Waterman, 
1950  ;   Waterman  and  Enami,  1953). 

THE    COMPOUND    EYES    OF    CRUSTACEANS 

Crustaceans  show  two  types  of  compound  eyes — a  relatively 
primitive  type  associated  with  the  smaller  siDecies  and  a  well  formed 
type  associated  with  the  larger  (crayfish,  lobster,  crab,  etc.). 


Fig.    145. — The  Head  of  the  Water-flea,   Daphma 


The  compound  eye  is  seen  above  with  several  of  its  22  omniatidia  appear- 
ing as  rounded  facets  in  a  bed  of  pigment.  Two  of  the  4  ocular  muscles  are 
also  seen  encircling  the  eye. 

Underneath,  the  pigmented  spot  is  the  composite  ocellus  -^'hich  lies  in 
the  mid-line;  it  is  made  up  of  the  fusion  of  3  ocelli  (E.  F.  Fincham) 
(see  Fig.  131). 

The  compound  eyes  of  the  tiny  Branchiopods  and  some  Ostracods  are 
relatively  primitive  organs  with  poorly  formed  ommatidia.  The  compound 
eye  of  the  water-flea,  Daphnia,  may  be  taken  as  representative  (Fig.  145).  It 
is  composed  of  22  rudiinentary  ommatidia  arranged  in  a  sphere  of  pignient 
and  represents  the  fusion  of  two  lateral  eyes.  The  eyes  of  other  Branchiopods 
are  often  more  elaborate,  Leptodora,  for  example,  having  300  facets  and  Poly- 
phemus 160.  In  those  Ostracods  which  possess  compound  eyes,  the  organs  are 
sometimes  separate  (paired)  if  the  median  composite  ocellus  is  present,  but 
fused  if  the  latter  is  lacking.  On  the  average  they  possess  between  4  and  50 
ommatidia  (Cypridinse,  etc.). 

The  compound  eyes  of  Malacostraca  consist  of  ommatidia  built 
upon  the  standard  plan  of  a  cuticular  cornea,  a  crystalline  cone,  and  a 

1  p.  158. 


Leptodora 


Polyphemus 


164 


THE   EYE   IN   EVOLUTION 


Astacus 


retinule,  the  whole  being  more  or  less  encased  by  pigmentary  cells. 
As  a  general  rule  the  ommatidia  are  fewer  than  in  the  eyes  of  Insects, 
but  many  variations  in  detail  exist  ^  ;  a  typical  example  is  seen  in 
Fig.  146  which  illustrates  the  eye  of  the  crayfish,  Astacus.  The 
cuticular  cornea  is  not  invariably  faceted  as  is  usually  the  case  in 
Insects,  but,  for  example,  in  Amphipods  appears  as  a  flat  extension 
of  the  cuticle  of  the  integument.  Underneath  the  cuticle  is  invaginated 
a  layer  of  hypodermal  cells  (Fig.  148).  The  crystalline  cone,  in 
contradistinction  to  its  variability  in  the  eyes  of  Insects,  is  never 
lacking  and  is  often  composite  and  divided  into  three  segments,  a 


Fig.   146. — The  Eye  of  a  Crayfish. 
Showing  the  faceted  appearance  of  the  compound  eye  (Norman  Ashton). 


Fig.    147. — Hemisection    of    the    Eye    of    the    Lobster    (see    Fig.    69.3) 

(Norman  Ashton). 


-    (1916), 
Heber'loy  and  Kupka  (1942) 


THE   COMPOUND   EYE 


165 


short  outer,  a  main  intermediate,  and  a  hollow  inner  segment.  The 
retinule  consists  of  relatively  few  cells  (4  in  crabs)  grouped  around  the 
central  rhabdome,  the  proximal  extremity  of  which  rests  on  a  fenes- 
trated membrane.  There  is  evidence  that  the  retinular  cells  are  not  all 
of  the  same  kind  ;  thus  3  different  types  have  been  described  in  the 
Isopod.  Ligia  (Ruck  and  Jahn,  1954).  In  some  species  (the  crayfish. 
Astacus,  and  the  shrimp,  Crago)  the  nuclei  of  the  retinular  cells  are 
arranged  in  three  zones,  a  configuration  somewhat  reminiscent  of  the 
multi-layered  retina  of  Vertebrates  ;  it  is  to  be  remembered,  however, 
that  all  are  derived  from  the  hypodermal  cells 
of  the  integument. 

The  pigmentation  is  complicated,  for  each 
ommatidium  possesses  at  least  two  functionally 
different  pigments.  Pigmentary  cells  (ikis 
cells)  containing  melanin  surround  the  distal 
part  of  each  ommatidium  ;  the  proximal  part  is 
similarly  ensheathed  or  the  retinular  cells  them- 
selves also  contain  melanin  ;  while  at  the  level 
of  the  retinule  is  a  clear  reflecting  pigment  ^ 
contained  in  separate  cells  ;  this  by  reflection 
prevents  the  entry  of  oblique  rays.  Although 
the  pigmentary  cells  do  not  move,  the  melanin 
pigment  within  them  shows  marked  migratory 
changes  (Welsh,  1930-41  ;  Parker,  1932  ; 
Bennitt,  1932)  (Fig.  148).  In  bright  light  the 
black  pigment  in  the  iris  cells  meets  that  in  the 
retinular  cells  so  that  the  entire  ommatidium 
is  encased  in  a  sleeve  of  pigment  ;  in  dim  light 
the  pigment  in  the  iris  cells  migrates  distally  to 
lie  between  the  cones,  that  in  the  retinular  cells 
migrates  to  a  position  proximal  to  the  basement 
miembrane,  while  the  reflecting  particles  sur- 
rounding the  retinal  elements,  cleared  of  absorb- 
ing pigment,  act  as  a  functional  tapetum.  We 
have  already  seen  that  the  migration  of  these 
pigments  often  sho\\'s  an  autochthonous  diurnal 
rhythm  -  and  that,  in  addition  to  this  response 

to  the  direct  action  of  light,  they  are  under  a  complex  hormonal  and 
nervous  control  (Kleinholz,  1936-38  ;  Welsh.  1939-41  ;  Brown,  1944  ; 
and  others).^ 

1  The  chemical  nature  of  the  reflecting  pigment  varies.  In  the  crayfish,  Astacus, 
the  iris  tapetum  is  of  uric  acid,  in  the  lobster,  Homnrus,  uric  acid  is  supplemented  by 
at  least  3  other  substances,  none  of  which  is  guanine  (Kleinholz  and  Henvvood,  1953  ; 
Kleinholz,  1955). 

2  p.  19.  *  See  further  p.  554. 


Fig.  148. — The  Ommati- 
muM  OF  THE  Cray- 
fish, Astacus. 

On  the  left,  in  the  light- 
aflapted,  and  on  the  right, 
the  dark-adapted  state. 

a,  Cornea  ;  b,  hypo- 
dermal  corneal  cells  ;  c, 
body  of  crystalline  cone  ; 
d,  inner  segment  of  crys- 
talline cone  ;  e,  retinal 
pigment  cells  ;  f,  rhab- 
dome separating  retinular 
cells;  g,  tapetal  cells;  h, 
basement  membrane  (mo- 
dified from  Bernhards). 


Ligia 


166 


THE   EYE   IN  EVOLUTION 


Lobster 


We  shall  see  ^  that  the  stalked  eyes  of  such  Decapods  as  the  lobster,  the 
shrimp  and  the  prawn  are  remarkable  in  that  the  nervous  connections  run  to  the 
procephalic  lobes  of  the  cerebral  ganglion  up  the  long  stalks  containing  the  optic 
lobe  with  its  series  of  ganglia  and  intervening  plexiform  zones.  The  presence 
of  a  three-layered  compound  retina  and  a  ganglionated  optic  lobe  makes  these 
crustacean  eyes  the  most  complex  among  Invertebrates  (Figs.  147,  693). 

The  eyes  of  Crustaceans  living  at  ocean  depths  are  rarely  so  well  formed  as 
those  inhabiting  littoral  or  shallow  waters  ;  as  a  rule — to  which,  however,  there 
are  marked  exceptions,  particularly  in  the  more  active  forms — the  number  of 
ommatidia  in  bathypelagic  forms  is  decreased  and  the  pigment  is  scanty  or 
absent  so  that  the  organ  functions  as  a  superposition  eye  ^  adapted  for  dim 
illumination  (Edwards  and  Bouvier,  1892). 


THE    COMPOUND    EYES    OF    INSECTS 

The  compound  eye  of  Insects  has  excited  interest  and  admiration 
for  centuries  (Figs.  149  and  150)^;  indeed,  the  faceted  cornea  attracted 
the  attention  of  the  pioneer  Dutch  microscopist,  van  Leeuwenhoek, 


li  r 


Fig.   149. — The  Eyes  of  Insects.  Fig.    150. — The    Compound    Eye    of 

An  old  anatomical  drawing  from   Swammer-  ^ 

dam  (Byhel  der  Natuure,  Leyden,  1737).  Section  through  the  compound  eye. 

Although    inaccurate    in    details,   the    surface  showing  the  optic  lobe  consisting  of  3 

of  the  intact  compound  eye  is  seen  on  the  left,  optic  ganglia,  and  the  protocerebrum 

a  partially  dissected  eye  on  the  right,  as  well  as  (below)  (Norman  Ashton). 

the  3  central  ocelli  (reproduced  by  permission  of 
the  Cambridge  University  Library  ;  by  courtesy 
of  Dr.  Pirenne  and  the  Pilot  Press). 

'  p.  521.  2  p_  169^ 

'  For  the  descriptive  anatomy  of  the  compound  eyes  of  insects,  see  Miiller  (1826), 
Gram  ;iier  (1879),  Exner  (1891),  Hesse  (1901-8),  Seaton  (1903),  Dietrich  (1909),  Johnas 
(1911;,  Bedau  (1911),  Geyer  (1912),  Demoll  (1912-17),  Zimmermann  (1913),  Jorschke 
(1914),  "Bugnion  and  Popoff  (1914),  Priesner  (1916).  Ast  (1920),  Cajal  and  Sanchez 


THE   COMPOUND   EYE 


167 


at  the  end  of  the  seventeenth  century.  Each  individual  ommatidium 
has  a  relatively  simple  structure  similar  to  that  already  described  in 
Crustaceans.  Most  externally  is  the  focusing  apparatus,  made  up 
from  without  inwards  of  a  cuticular  lens-like  formation  (the  corneal 
lens  or  facet)  under  which  lies  the  crystalline  cone  surrounded  by 
nucleated  hypodermal  cells  which  do  not  form  a  complete  layer  as  in 
the  typical  crustacean  eye  (Fig.  151). 

Such  a  dioptric  apparatus  forms  the  typical  arrangement   (the 
EUCONE  eye)  ;    but  variations  occur  in  which  the  entire  refractive 


Colorado  beetle 
(Coleoptera) 


Figs.    151   and    152.^Schematic   Structure   of   the   Two   Types   of 
Ommatidia  of  Insects. 


1/ 


/- 


^\) 


I 


Fig.  151. — The  apposition  eye,  with 
(alongside  and  below)  a  section 
through  the  retinule. 


Fig.  152. — The  superposition  eye  in 
the  dark-adapted  condition  with  the 
pigment  in  the  iris  cells  almost 
entirely  withdrawn  into  their  upper 
extremities. 


a,  corneal  facet  ;  b,  corneal  cells  ;  c,  crystalline  cone  ;  d,  iris  piginent 
cells  ;  e,  rhabdome  ;  /,  sensory  cells  of  the  retinule  ;  g,  retinal  pigment  cells  ; 
h,  fenestrated  basement  membrane  ;  i,  eccentric  retinal  cell  ;  k,  filament 
connecting  crystalline  cone  with  rhabdome  ;  I,  nerve  fibre  (after  Weber  and 
Snodgrass). 


function  is  taken  over  by  the  cornea.  In  place  of  a  separate  crystalline 
cone  secreted  by  special  crystalline  cells  (vitrellce),  these  cells  may 
merely  secrete  an  accumulation  of  fluid  (the  pseudocone  eye),  as 
occurs  in  Muscids.  In  other  types,  such  as  beetles  (Coleoptera),  some 
bugs  (Hemiptera)  and  crane-flies  (Tipulids),  the  cones  remain  cellular 
and  non-refringent   (the  acone   eye).     Alternatively,   the  refractive 

(1921).  Cornell  (1924),  Kuhn  (1926),  Gotze  (1927),  Bott  (1928),  Friederichs  (1931), 
Nowikoff  (1931),  Werringloer  (1932),  Weber  (1934),  Llidtke  (1935-51),  Wundrig  (1936), 
Vidal  and  Courtis  (1937),  Zankert  (1939),  Verrier  (1940),  Lhoste  (1941),  Roonwal  (1947), 
Ehnbom  (1948),  Tuurala  (1954),  Fernandez-Moran  (1956). 


Crane-fly 
(Tipulidse) 


168 


THE   EYE   IN   EVOLUTION 


Dytiscus 


functions  of  the  crystalline  structure  may  be  replaced  by  the  cuticular 
cornea  which  itself  forms  a  cone-like  invagination,  as  occurs  in  fire-flies 
(Lampyrids)  or  the  water-beetle,  Dytiscus  (the  exocone  eye),  an 
arrangement  reminiscent  of  that  seen  in  the  king-crab  (Fig.  143). 

In  most  diurnal  insects  the  retinule  with  its  tubular  arrangement 
of  a  group  (usually  7  or  8)  of  elongated  sensory  cells  arranged  around 
the  central  rhabdome  lies  immediately  underneath  the  lens,  resting 
upon  a  fenestrated  basement  membrane  through  which  pass  nerve 
fibres  which  run  to  the  outermost  nucleus  of  the  optic  lobe.^  Around 
the  bases  of  the  retinular  cells  in  close  association  with  the  basement 
membrane  are  refractile  trachea  which  increase  the  optical  efficiency 


Fig.  153. — Image  Formation  in  the  Compound  Eye. 

A,  apposition  eye.  Only  the  rays  of  light  falling  normally  (or  practically  so) 
(a,  b,  c)  reach  the  rhabdomes  and  retinular  cells  so  that  each  ommatidium 
functions  as  a  unit.  The  ray  from  b  deviating  to  the  left  is  absorbed  by  the 
pigment  sheath,  P.      (Compare  Fig.  156.) 

B,  superposition  eye.  The  main  part  of  the  diagram  shows  the  pigment 
in  the  dark-adapted  position  drawn  up  between  the  cones  in  which  case  the 
superposition  optical  system  is  effective  ;  thus  the  rays  from  d  and  e  can 
traverse  many  ommatidia  to  become  focused  on  one  rhabdome,  Rh.  In  the 
two  ommatidia  on  the  right  the  pigment  is  in  the  light-adapted  position  so 
that  all  rays  except  those  entering  normally  (or  nearly  so)  on  the  facet  are 
intercepted  by  the  pigment,  P. 


of  the  eye  by  reflecting  the  light  back  through  the  rhabdome.  thus 
serving  the  function  of  a  ta/petum.  As  in  Crustaceans,  pigment  is 
usually  a  prominent  feature.  In  most  diurnal  insects  each  ommatidium 
is  entirely  ensheathed  by  pigmented  cells  arranged  in  two  sections,  the 
iris  2^igment  cells  or  primary  iris  cells  lying  distally  surrounding  the 
crystalline  cones,  and  the  retired  pigynent  cells  or  secondary  iris  cells 
lying  proximally  which  encircle  the  retinule  ;  the  ommatidium  thus 
act.s  optically  as  an  isolated  unit.  The  iris  cells  contain  not  only 
black  absorbing  pigment  but  also  pale  or  coloured  reflecting  granules 
witi)  i  tapetal  function. 

1  p.  521. 


THE   COMPOUND   EYE  169 

While  this  is  the  most  common  form  of  compound  eye  wherein  each 
ommatidium  is  designed  to  act  by  itself  with  the  result  that  the  optical 
image  resembles  a  finely  grained  mosaic  (the  apjposition  eye)}  many 
nocturnal  insects  show  a  dramatic  contrast  wherein  light  is  utilized 
more  effectively  by  an  arrangement  which  allows  incident  rays  from 
several  facets  to  reach  one  rhabdome  (the  sujierposition  eye).  The 
typical  structure  of  this  type  of  eye  is  seen  in  beetles  and  noctuid 
moths  (Fig.  152).  In  these  the  retinule  is  situated  far  back  and  the 
interval  between  it  and  the  crystalline  cone  is  traversed  by  a  non- 
refractile  translucent  filament  connecting  this  structure  with  the 
rhabdome.  while  the  pigmented  iris  cells  are  concentrated  distally 
between  the  crystalline  cones  leaving  the  retinules  without  an  insulating 
sheath. 

Figs.   154  ant>   1.5.5. — Superposition  Images  formed  by  the  Refractive 
System  of  LAMpyjtis. 


Fig.      154. — The     mosaic     of     images  Fig.    155. — The   superimjiosed   images 

formed  at  a  level  immediately  be-  at  the  level  of  the  rhabdome  (after 

neath  the  optical  system.  Exner). 

The  functional  contrast  between  the  two  types  is  seen  in  Fig.  153. 
In  Figs.  154  and  155  are  seen  the  illustrations  from  Exner's  (1891) 
classical  treatise  showing  the  image  of  a  candle  flame  formed  by  the 
corneal  facets  and  cones  of  the  fire-fly,  Lampyris.  When  the  microscope 
is  focused  just  below  the  dioptric  apparatus  a  multitude  of  luminous 
spots  is  seen  all  of  which  become  merged  into  one  at  the  level  of  the 
rhabdomes.  The  light  from  as  many  as  30  different  facets  may  thus  be 
concentrated  on  one  of  these  structures. 

Intermediate  forms  between  these  two  types  of  compound  eye 
exist  ;  nor  are  they  mutually  exclusive.  Thus  in  Mantids  the  two  are 
seen  combined  in  the  same  eye  ;  the  anterior  ommatidia  which  are 
used  for  binocular  vision  are  of  the  apposition  t^'pe  while  the  lateral 
parts  are  of  the  superposition  tyjDe  (Friza,  1928) — a  functionally 
efficient  arrangement.  Moreover,  as  in  Crustaceans,  the  change  from  a 
superjDosition  eye  of  the  nocturnal  tyjje  to  an  apposition  eye  of  the 
diurnal  type  with  its  high  degree  of  resolution  can  be  made  functionally 

1  p.  173. 


Fire-fly 


170 


THE   EYE   IN  EVOLUTION 


Butterfly 
( Vanessa) 


by  a  migration  of  pigment,  thus  effecting  an  adaptive  process  in  species 
which  are  active  both  by  day  and  by  night  :  in  dim  hght  the  pigment 
becomes  concentrated  anteriorly  so  that  the  eye  can  function  as  a  super- 
position eye  and  make  full  use  of  all  the  available  light  ;  while  in 
bright  illumination  it  disperses  and  migrates  posteriorly  surrounding 
each  retinule  with  an  opaque  mantle  intercepting  all  lateral  rays 
(Parker,  1932).  Thus  in  the  dark-adapted  state  examination  of  the 
eyes  of  certain  noctuid  moths  with  an  ophthalmoscopic  mirror  shows  a 
luminous  red  reflection  from  a  group  of  ommatidia  ;  in  the  light - 
adapted  state  there  is  a  minute  glow  from  one  central  ommatidium 
only  (Demoll,  1917  ;  Horstmann,  1935).  This  pigmentary  migration 
in  some  butterflies  and  moths  begins  from  half  to  one  hour  before 
sunrise  or  sunset  and  the  change  occupies  an  interval  varying  from  r. 
few  minutes  to  an  hour  (Merker,  1929-34  ;  Collins,  1934).  The 
excised  eye  always  adopts  the  light-adapted  distribution  of  pigment. 
The  migratory  response  is  abolished  by  narcosis  nor  does  it  occur  in 
butterflies  when  the  insect  is  at  rest  and  inactive  (Demoll,  1909-11  ; 
Day,  1941).  Its  mechanism  is  unknown  ;  a  purely  hormonal  control  is 
improbable  since  individual  ommatidia  may  respond  to  localized 
illumination  (Day,  1941)  ;  but  whether  the  migration  of  pigment  is 
dependent  upon  nervous  reflexes  from  the  retinule  or  is  initiated  by 
photochemical  reactions  within  the  pigmentary  cells  is  controversial. 


Notonecta 


Pigmentary  migration  of  a  less  dramatic  kind  occurs  in  certain  purely 
apposition  eyes  of  diurnal  species  as  a  response  to  rapid  changes  in  illumination. 
These  are  associated  chiefly  with  the  pigment  in  the  cells  around  the  basement 
meinbrane  (butterflies — Demoll,  1909  ;  the  water-boatman,  Notonecta — Bedau, 
1911).  In  the  latter  the  visual  cells  also  elongate  in  the  dark-adapted  state 
(Liidtke,  1951-53). 


The  Optical  System  of  the  Coni2)ound  Eye 

The  optical  system  of  the  compound  eye  has  always  excited 
considerable  interest  since  it  was  first  studied  by  Johannes  Miiller 
(1826)  ;  Fig.  156,  taken  from  his  classical  work  on^  this  subject, 
indicates  characteristically  his  conception  of  the  optical  mechanism 
whereby  a  point  source  of  light  excites  only  one  (or  two)  ommatidium. 
In  his  Mosaic  Theory  he  showed  that  an  image  of  considerable  definition 
would  be  formed  by  the  juxtaposition  of  the  many  small  luminous 
stimuli  received  by  the  ommatidia,  each  of  them  the  impression  of  the 
corresponding  projection  in  the  visual  field,  each  of  them  varying 
acocjrding  to  the  pattern  of  the  incident  light.  Such  an  image,  in 
CO])- r?)  distinction  to  that  formed  by  the  eye  of  Vertebrates,  is  erect,  and 
the  -f  can  be  easily  simulated  by  allowing  light  to  traverse  a  bundle 
of  Dj         tubes  and  fall  upon  a  plate  of  ground-glass,  an  arrangement 


THE   COMPOUND   EYE 


171 


which  clearly  shows  that  the  definition  of  the  image  depends  on  the 
number  of  tubes  per  unit  area  (Alverdes,  1924).  Using  the  excised 
anterior  segment  of  the  eye  of  the  fire-fly,  Lampyris,  as  a  lens,  Exner 
(1891)  succeeded  in  photographing  the  image  (Fig.  157)  ;  the  degree 
of  resolution  thus  obtained  has  been  estimated  by  Marchal  (1910)  to 


Fig.   156. — The  Compound  Eye  According  to  Johannes  Muller. 

When  light  emitted  by  different  points,  a,  b,  c,  d,  falls  on  the  ej^e,  that 
from  a  completely  illuminates  cone  e,  but  the  ommatidia  to  the  right  of  e 
are  not  illuminated  all  the  way  down.  Only  the  nerve  /,  issuing  from  cone  e, 
is  thus  stimulated  by  the  source  a,  while  light  from  the  same  source  entering 
other  onimatidia  is  unable  to  stimulate  the  fibres  since  it  is  absorbed  by 
the  pigment  sheaths.  Similarly,  light  from  b,  stimulates  two  ommatidia  at/  ; 
light  from  c,  two  ommatidia  at  g  ;  and  light  from  d,  one  ommatidium  at  h 
(from  Miiller,  1826  ;  by  permission  of  the  Cambridge  University  Library  ; 
by  courtesy  of  Dr.  Pirenne  and  the  Pilot  Press). 


correspond  approximately  to  an  acuity  of  1/60  in  the  human  eye. 
It  is  important  to  realize  that  owing  to  the  isolating  effect  of  the  pig- 
ment mantle,  no  formed  image  is  produced  at  the  level  of  the  receptor 
cells  ;  each  of  these  acts  only  as  a  photometer  and  from  the  mosaic 
thus  formed  by  the  individual  ommatidia  the  picture  of  the  outside 
world  is  synthesized  in  the  central  nervous  system  (van  der  Horst,  1933). 


172 


THE   EYE   IN   EVOLUTION 


Musca 


Dragonfly 


Necrophorus 


Apis 


In  the  compound  eye  of  the  winged  male  of  Lam2Jyris  there  are 
2,500  ommatidia  ;  but  the  number  of  elements  varies  considerably 
between  different  species  depending  largely  on  their  habits.  Thus,  in 
Solenopsis,  the  worker-ants  which  live  underground  have  6  or  9, 
while  the  winged  males  which  pursue  the  female  in  tlie  air  are  provided 
with  400  ;  in  genera  with  a  high 
visual  acuity  the  numbers  are  much 
higher — in  the  house-fly,  Musca, 
4,000  ;  in  the  water-beetle,  Dytiscus, 
9,000  ;  and  in  dragonflies  (Odonata) 
up  to  28,000  (Demoll,  1917  ;  Imms, 
1935),  or  the  burying  beetle,  Necro- 
phorus, 29,300  (Leinemann,  1904). 
The  size  of  the  individual  facets  re- 
mains fairly  constant  (15  to  40/x) ;  the 
size  of  the  eye  is  determined  essenti- 
ally by  their  number. 

From  the  functional  point  of 
view,  however,  the  most  important 
feature  is  the  ommatidial  angle. 
that  is,  the  angular  extent  of  the 
visual  field  covered  by  each  element. 
It  is  obvious  that  if  a  pattern  is  to  be 
resolved,  two  adjacent  ommatidia 
must  be  unequally  stimulated  so  that 
their  angular  separation  must  form 
the  anatomical  basis  of  the  visual 
acuity,  corresponding  in  man  to  the 
inter-cone  distance  and  determining 
the  fineness  of  the  "  grain  "  of  the 
resulting  picture  (del  Portillo,  1936). 
As  this  angle  becomes  smaller,  the 
resolving  power  increases,  but  less 
light  will  enter  each  facet.  Thus  the 
angle  in  the  bee.  Apis,  varies  from 

0-9°  to  1°  in  the  centre  of  the  eye,  and  in  the  earwig,  Forficula,  is  8°, 
so  that  the  latter  will  obtain  a  single  point  of  light  as  the  image  of  an 
object  which  the  eye  of  the  bee  will  resolve  into  64  (Baumgartner,  1928  ; 
V.  Buddenbrock,  1937).  In  the  locust,  Locusta,  the  ommatidial  angle 
is  about  21°  (Burtt  and  Catton,  1954).  In  the  periphery  of  the  eye  the 
ommatidial  angle  is  larger  than  in  the  centre  and  the  acuity  corres- 
pondingly less;  in  the  anterior  region  of  the  eye  it  is  often  smaller  than 
in  i  '  ventral,  an  arrangement  which  favours  visual  acuity  in  flight 
(Aut.  jiu,  1949)  (Fig.  158). 


Fig.  157. — Exner's  Classical  Photo- 
graph THROUGH  THE  OPTICAL  SYS- 
TEM OF  THE  Compound  Eye  of 
Lamp  mis  splesdidula. 

Showing  a  window  with  a  letter  R 
on  one  pane  and  a  church  beyond  (from 
Wigglesworth's  Principles  of  Insect 
Physiologu,  Methuen). 


THE   COMPOUND   EYE 


173 


Exner's  early  work  on  the  dioptrics  of  the  ommatidial  system  still  remains 
classical.  He  showed  that  the  essential  refractive  device  is  the  crystalline  cone, 
which,  of  course,  vmlike  the  lens  of  Cephalopods  and  Vertebrates,  has  a  fixed 
focus  incapable  of  adjustment.  The  crystalline  cone  itself  is  composed  of 
concentric  lamellae  the  refractive  index  of  which  increases  progressively  from 
the  perii^hery  to  the  central  axis  (Fig.  159)  ;  it  therefore  acts  as  a  "  lens-cylinder  " 
wherein  an  obliquely  incident  ray  is  progressively  refracted  until  it  is  gradually 


Forficiila 


Fig.   158. — The  Ommatidial  Angles  of  the  Eye  of  the  Honey-Bee. 

The  ommatidia  are  drawn  in  groups  of  3,  and  the  drawing  shows  the 
way  in  which  an  ommatidial  angle  varies  in  different  parts  of  the  eye  ;  the 
values  of  the  angles  are  given  in  degrees  (Pirenne,  after  Baumgartner). 


brought  back  to  the  axis.  It  is  probable  that  the  crystalline  cone  thus  brings 
the  image  formed  bj^  an  ommatidimn  to  a  small  point  although  different  wave- 
lengths will  be  brought  to  a  focus  at  different  places  (Goulliart,  1953).  To  some 
extent  therefore,  the  optics  of  the  comjaoand  eye  with  its  many  elements  is 
comparable  to  the  analysis  made  by  television. 

The  appositional  eye  wherein  the  retinule  abuts  against  the  crystalline 
cone  may  be  compared  oj)tically  to  such  a  system  wherein  rays  of  light  pass 
through  a  lens-cylinder  of  a  length  equal  to  its  focal  distance  (Fig.  160).  In  this 
event  a  beam  of  parallel  light  (mpn)  entering  perpendicularly  to  one  edge  of  the 
cylinder  (ab)  will  be  focused  as  an  inverted  image  at  y  on  the  other  edge  and  will 


Locust  a 


174 


THE   EYE   IN   EVOLUTION 


b 

Fig.  159. —  The 
Lens  Cone  of 
THE  Compound 
Eye. 

The  laminated 
optical  structure  of 
superimposed  la- 
mellae (after  Exner). 


emerge  as  a  diverging  beam  (m'  p'  n').  Oblique  rays  (g)  will 
emerge  at  an  angle  as  q' .  The  pigment  mantle  around  the 
cones,  however,  will  absorb  oblique  rays  and  virtually 
permit  the  light  to  emerge  only  at  y,  where  the  image  falls 
as  a  single  luminous  point  on  the  subjacent  retinule  ;  the 
apposition  of  all  such  points  will  form  the  complete  erect 
image  perceived  by  the  eye. 

In  the  superpositional  eye,  on  the  other  hand,  the 
optical  system  will  correspond  to  a  lens-cylinder  of  a  length 
equal  to  twice  its  focal  distance  (Fig.  161).  The  inverted 
image  of  a  distant  object  will  be  formed  in  the  middle  of  the 
cylinder  {xy)  ;  the  rays  traversing  the  remaining  half  of  the 
cylinder  will  pursue  a  symmetrical  course  and  emerge  at  an 
angle  (^)  equal  to  that  at  which  they  entered  (a)  but 
opposite  in  direction.  Not  only  will  normal  rays  thus  fall 
on  the  distant  rhabdome  but  also  oblique  rays  refracted 
from  the  cones  towards  the  same  side  from  which  they  have 
come,  so  that  a  number  of  separate  images  can  be  super- 
iinposed  on  one  visual  element.  The  resultant  image  thus 
gains  in  luminosity  at  the  sacrifice  of  resolution. 


The  ability  to  analyse  the  plane  of  polarized  light  is 
a  common  function  of  the  compomid  eyes  of  Arthropods  and  of  both  the 
simple  and  compound  eyes  of  Insects  ;  it  is  a  function  which  is  freely 
used  to  aid  orientation  out-of-doors.^  The  structure  which  serves  as 
an  analyser,  however,  has  given  rise  to  controversy.  The  suggestion  that 


Fig.    160. — The   Optical   System   of 
THE  Apposition  Eye. 

The  i;  u^  cylinder  is  equal  in  length 
to  its  foe-  distance  (after  Exner). 


Fig.    161. — The   Optical   System   of 
THE  Superposition  Eye. 

The  lens  cylinder  is  equal  in  length 
to  twice  its  focal  distance  (after  Exner). 


1  p.  66.  See  Kalmus.  Nature  (Lend.),  184,  228  (1959). 


THE   COMPOUND   EYE  176 

the  retinular  cells  act  as  differentially  orientated  detectors  ^  was  based 
on  differences  in  the  electrical  response  with  variations  of  the  direction 
of  polarization  of  the  incident  light.  Such  a  suggestion,  however,  is 
difficult  to  accept  if  it  is  agreed  that  the  individual  cells  are  not 
furnished  with  corresponding  axonal  transmission  ^  ;  the  theory  could 
not  be  made  to  adapt  itself  to  the  proven  single  impulse  transmitted 
from  each  entire  ommatidium  in  the  eye  of  Limulus  (Waterman,  1950; 
Waterman  and  Wiersma,  1954)  ;  moreover,  such  a  change  does  not 
seem  to  be  invariable.^  It  has  also  been  suggested  that  the  ultra- 
structure  of  the  rhabdome  with  its  composite  laminated  and  fenestrated 
bodies,  could  provide  a  physical  basis  for  this  faculty  (Fernandez- 
Moran,  1956).  An  alternative  hypothesis  is  that  the  responsible 
structure  is  the  corneal  facet  with  its  chitinous  covering  which  is 
birefringent,  rather  than  any  structure  within  the  ommatidium 
(Waterman,  1951  ;  Berger  and  Segal,  1952).  Wolsky  (1929)  and 
Stockhammer  (1956),  however,  were  unable  to  detect  any  optical 
mechanism  which  could  act  as  an  analyser  in  the  entire  dioptric 
apparatus  in  the  insects  which  they  studied,  and  concluded  that  this 
mechanism  resided  in  the  visual  cells.  It  is  obvious  that  further 
research  is  required  on  this  problem,  and  it  may  well  be  that  more  than 
one  mechanism  is  operative,  differing  in  different  species,  or  a  mecha- 
nism as  yet  unsuspected. 

Alverdes.  fii'o?.  Z6Z.,  43,  577  (1924).  Biitschli.  Vorlesungeniiber vergl.Anatomie, 
Ast.     Zool.  Jb.,  Abt.  Anat.,  41,  411  (1920).  Berlin,  872  (1921). 

Autrum.  Exjjerientia,  7,  271  (1949).  Cajal  and  Sanchez.  Trab.  Lab.  Invest. 
Autrum  and  Gallwitz.     Z.  vergl.  Physiol.,  biol.  Univ.  Madrid,  13,  1  (1915). 

33,  407  (1951).  Rev.  chil.  Hist,  nat.,  25  (1921). 

Autrum  and  Stumpf.    Z.  Xafurjorsch.,  5b,  Chun.     Bibl.  Zool.,  7,  193,  213  (1896). 

116  (1950).  Claus.    Manuale  de  Zool.,  Milano  (1879). 

Baumgartner.      Z.   vergl.    Physiol.,   7,   56  Collins.    J.  ex;;.  Zoo/.,  69,  165  ( 1934). 

T,  ,  ^  J"  •  rr  r  nr,  ,,-,,n,,^  Comeli.  Zool.  Jb.,  Abt.  Anat.,  46,  573 
Bedau.     Z.  wiss.  Zool,  97,  il~  (1911).  (19->4) 

Bennitt.    Physiol.  Zool.,  5,  49,  65  (1932).  j^  ^-J  ^^^^  gg^  075  (1941). 

Berger   and   Courrier.      C.    B.   Acad.  Sci.  t^         ,,      pfif.aers  irrh    aes    Physiol     12q 

(Pans),  234,  1208  (1952).  461  {\S)  ^nyswi.,  i^y, 

Berger    and    Segal.      C.    R.    Acad.    Sci.  „     ,     j,      " !',.      ,      ,     o-v    c-i    /ir^nr>\ 

(Pans),  234,  1308  (1952).  ^"i./^y    ^^p/""  "  3  ,^^^  //q^i^,^  = 

Bernhard.    J.  NeurophysioL,  5,  32  (1942).  i^^'-^^f^J.^r      '  ^°'  ^        ^  ' 

Bernhards.    Z.  it'fss.  Zoo/.,  116, 649  (1916).  ^'^■^' .'^^^  ^^"^^-'-      ,         ,     ,  ,        ., 

Bott.     Z.  Morphol.  Oekol.   Tiere,  10,  207  ^^^  Sinnesorgane    der   Arthropoden    ihr 


(1928). 


Bau     und     ihre     Funktion,     Braun- 


Brink.    S.  African  J.  Sci.,  47,  162  (1951).  schweig  (1917). 

Brown.    Quart.  Rev.  Biol.,  19,  32  (1944).  Dethier.     J.  cell.  comp.  Physiol.,  19,  301 

von   Buddenbrock.      Grundriss   der  vergl.  (1942)  ;   22,  115  (1943). 

Physiol,  Berlin  (1937).  Dietrich.     Z.  wiss.  Zool,  92,  465  (1909). 

Bugnion  and  Popoff.     Arch.  Anat.  micr.,  Doflein.     Wiss.  Ergebn.  Dtsch.  Tiefseeexp. 

16,  261  (1914).  Valdivia,  6,  141  (1914). 

Burtt  and  Catton.     J.  Physiol,  125,  566  Edwards   and   Bouvier.      Ann.  Sci.   Xat. 

(1954).  (Zool),  13,  185  (1892). 

*  Autruin  and  Stumpf  (1950),  Menzer  and  Stockhammer  (1951)  in  the  bee  ;    Stock- 
hammer  (1956)  in  Diptera  and  Hymenoptera. 
2  p.  158. 
^  de  Vries  et  al.  (1953),  in  the  blowfly,  Calliphora. 


176 


THE    EYE   IN   EVOLUTION 


Ehnbom.       Opuscula     Entomol.,     Suppl. 

VIII,  Lund  (1948). 
Exner.      Die    Physiologic   der  facetlierten 

Augen    von    Krebsen    und    Insekten, 

Leipzig  (1891). 
Fernandez-Moran.      Nature  (Lond.),  177, 

742  (19.56). 
Fricke.      Zool.    Jb.,    Abt.    Anat.,    53,    70 

(1931). 
Friederichs.    Z.  Morphol.  Oekol.  Tiere,  21, 

1  (1931). 
Friza.     Z.  vergl.  Physiol.,  8,  289  (1928). 
Geyer.     Zool.  Anz.,  39,  375  (1912). 
Gotze.     Zool.  Jb.,  Abt.  Zool.  Physiol.,  44, 

211  (1927). 
Goulliart.     C.R.   Acad.  Sci.   (Paris),  236, 

1508  (1953). 
Greeff.     Sitz.    Ges.   Bef order ung   gesammt. 

Naturw.  Marburg,  115  (1875). 
Nova  Acta  Leopoldina,  39,  33  (1877). 
Grenadier.      Untersuch.  iiber  das  Sehorgan 

der  Arthropoden,  Gottingen  (1879). 
Arch.  mikr.  Anat.,  18,  415  (1880). 
Hanaoka.    Seitai  No  Kagaku,  2,  8  (1950). 
Hanstrom.  K.  Svenska  Vetensk.  Handl.,  4, 

1  (1926). 
Z.  vergl.  Physiol.,  6,  566  (1927). 
Z.  Morphol.  Oekol.  Tiere,  23,  80  (1931). 
Zool.Jb.,Abt.Anat.,5e,387  (1933)  ;  58, 

101  (1934). 
Kungl.  Fysiogr.  Sdllsk.  Lund  Forhandl., 

5,  156  (1935). 
Hartline.    J.  cell.  comp.  Physiol.,  11,  465 

(1938). 
Fed.  Proc,  8,  69  (1949). 
Hartline    and    Graham.      J.    cell.    comp. 

Physiol.,  1,  277  (1932). 
Hartline,  Wagner  and  MacNichol.     Cold 

Spr.  Harb.  Symp.  quant.  Biol.,  17,  125 

(1952). 
Hartline,     Wagner    and    Tomita.       Proc. 

XIX  int.  physiol.  Cong.,  441  (1953). 
Heberdey  and  Kupka.     Z.  vergl.  Physiol., 

29,  541  (1942). 
Herter.     Zool.  Jb.,  Abt.  Zool.  Physiol.,  45, 

159  (1928). 
von  Hess,  C.    PJlilgers  Arch.  ges.  Physiol., 

122,  449  (1918). 
Hesse.     Z.  wiss.  Zool..  61,  393  (1896)  ;    65, 

446  (1899)  ;    68,  379  (1900)  ;    70,  347 

(1901). 
Das    Sehen    der    niederen    Tiere,    Jena 

(1908). 
van  der  Horst.   Acta  Zool.,  14,  101  (1933). 
Horstmann.     Biol.  Zbl.,  55,  93  (1935). 
Imms.      Textbook  of  Entomology,  London 

(1935). 
Jorschke.     Z.  wiss.  Zool.,  Ill,  153  (1914). 
Johansen.     Zool.  Jb.,  Abt.  Anat.,  6,  246 

(1893). 
Johnas.     Z.  wiss.  Zool.,  97,  218  (1911). 
Kingslev.     Zool.  Anz.,  9,  597  (1886). 
Kleinhol/        Biol.  Bidl.,  70,   159  (1936)  ; 

75,  '!■       510  (1938)  ;    96,  218  (1949)  ; 

109,  1955). 


Kleinholz    and    Henwood.       Anat.    Rec, 

117,  637  (1953). 
Kuhn.     Z.  Morphol.  Oekol.   Tiere,  5,  489 

(1926). 
Kiipfer.     Viertlj.  naturf.  Ges.  Zurich.,  60, 

568  (1915). 
Lankester  and  Bourne.     Quart.  J.   micr. 

Sci.,  23,  177  (1883). 
Leinemann.     Diss.,  Miinster  (1904). 
Lhoste.    Bull.  Soc.  zool.  Fr.,  66,  62  (1941). 
Ludtke.     Z.  vergl.  Physiol.,  22,  69  (1935)  ; 

35,  129  (1953). 
Naturwissenschaften,  38,  285  (1951). 
MacNichol,  Wagner  and  Hartline.     Proc. 

XIX  int.  physiol.  Cong.,  582  (1953). 
Marchal.      Richet's  Dictionnaire  de  Phy- 
siol., 9,  273  (1910). 
Menzer  and  Stockhammer.    Naturwissen- 
schaften, 38,  190  (1951). 
Merker.    Zool.  Jb.,  Abt.  Zool.  Physiol.,  46, 

297  ((1929). 
Biol.  Rev.,  9,  49  (1934). 
Miller.  Bull.  Johns  Hopkins  Hosp.,  91,  72 

(1952). 
Miiller.      Zur  vergl.   Physiol,   d.   Gesichts- 

sinnes,  Leipzig  (1826). 
NowikoiT.    Z.  wiss.  Zool.,  79,  432  (1905)  ; 

138,  1  (1931). 
Parker.      Mitt.    zool.  Stat.    Neapel,   12,    1 

(1897). 
Ergebn.  Biol.,  9,  239  (1932). 
Patten.     Mitt.  zool.  Stat.  Neapel,  6,  568 

(1886). 
J.  Morphol.,  2,  97  (1888). 
The  Evolution  of   Vertebrates  and  their 

Kin,  London  (1912). 
Pfiugfelder.        Z.    iviss.    Zool.,    142,    540 

(1932). 
del  Portillo.      Z.   vergl.   Physiol.,  23,    100 

(1936). 
Priesner.     Zool.  Jb.,  Abt.  Anat.,  39,  485 

(1916). 
Roonwal.      Proc.    roy.   Soc.    B,    134,    245 

(1947). 
Rosenstadt.     Arch.  mikr.  Atiat.,  47,   748 

(1896). 
Ruck  and  .Jahn.    J.  gen.  Physiol.,  37,  825 

(1954). 
Seat  on.    Amer.  Nat.,  37,  319  (1903). 
Stockhammer.     Z.  vergl.  Physiol.,  38,  30 

(1956). 
Strauss.     Wiss.  Ergebn.  dtsch.   Tiefseeexp. 

Valdivia,  20,  1  (1909).' 
Tuurala.     Ann.   Acad.  Sci.  fenn.  Ser.,   5 

(1954). 
Vaissiere.     C.  R.  Acad.  Sci.  (Paris),  238, 

942  (1954). 
Verrier.     Bull.  Biol.  France  Belg.,  74,  309 

(1940). 
Vidal  and  Courtis.     Acta  I  Cong,  argent. 

Oftal.,  1,  418  (1937). 
de  Vries,  Spoor  and  Jielof.     Physica,  19, 

419  (1953). 
Watase.  Biol.Studies  Johns  Hopkins  Univ., 

4,  287  (1890). 


THE   COMPOUND   EYE  177 

Waterman.    5'cie/ice,  111,  252  (1950).  J.  exp.  Zoo/.,  86,  35  (1941). 

Trans.  N.Y.  Acad.  Sci.,  1^,  11  (1951).  Wenke.     Z.  wiss.  ZooL,  91,  236  (1908). 

J.  Morja/ioZ.,  95,  125  (1954).  Werringloer.      Z.    wiss.    ZooL,    141,    432 

Waterman  and  Enaini.     Pubbl.  Staz.  zool  (lOS'') 

^'apoli,  Suppl     24,  81  (1953).  Wolsky.  ^ Zool.  Am.,  80,  56  (1929). 

Iz^'^'l'd^^mlr''^'''           '■'''■  Wundrig.     Zool.  Jb.,  Abt.  Anat.,  62,  45 

Weber.  'ZooZ..4n2'.,  108,  49(1934).  v-    /^f^^c-  »^            ,     .        ,      tt          ; 

Welsh.       Proc.    nat.   Acad.  ScL,    16,   386  Zankert.    S.B.  Ges.  naturforsch.  Freunde, 

(1930).  Berlin,  1-3,  82(1939). 

Biol.    Bull.,    72,    57    (1937);     77,    119  Zimmermann.    Zoo/.  J6.,  .46^  .4na^,  37,  1 

(1939).  (1913). 


S.O. — VOL.  I. 


CHAPTER  VII 

THE  SYSTEMATIC  ANATOMY 
OF  INVERTEBRATE  EYES 

From  the  morphological  point  of  view  we  have  seen  that  the 
visual  organs  of  Invertebrates  show  an  astonishing  range  in  structure, 
varying  in  complexity  from  the  simple  eye-spot  or  the  single  visual  cell 
to  the  elaborate  organs  characteristic  of  Cephalopods  or  Insects  ;  from 
the  functional  point  of  view  the  variation  is  equally  great,  evolving 
from  a  primitive  and  j^erhaps  undifferentiated  sentiency  which  may 
influence  metabolic  and  motorial  reactions,  to  the  capacity  to  form 
elaborate  images  whereby  intensity,  hue,  form  and  spatial  relationships 
can  be  differentiated  with  sufficient  exactitude  and  appreciation  to 
determine  behaviour.  The  curious  thing,  however,  is  that  in  their 
distribution  the  eyes  of  Invertebrates  form  no  series  of  contiguity  and 
succession.  Without  obvious  phylogenetic  sequence,  their  occurrence 
seems  haphazard  ;  analogous  photoreceptors  appear  in  unrelated 
species,  an  elaborate  organ  in  a  primitive  species  ^  or  an  elementary 
structure  high  in  the  evolutionary  scale, ^  and  the  same  animal  may  be 
provided  with  two  different  mechanisms  with  different  spectral 
sensitivities  subserving  different  types  of  behaviour. 

A  striking  example  of  this  is  seen  in  the  flat-worm,  Planaria  lugubris,  which 
has  both  positive  and  negative  photo -reactions  (Viaud  and  Medioni,  1949)  ;  if 
this  aniinal  is  bisected  the  photo -positive  reactions  appear  in  the  posterior 
segment  before  the  nerves  regenerate  suggesting  that  these  responses  are  due  to 
dermal  sensitivity,  while  it  has  been  shown  that  the  photo -negative  reactions 
are  due  to  the  eyes  ;  photokinesis  is  dependent  on  the  skin,  positional  orientation 
to  light  on  the  eyes.  In  the  earthworm,  Lurnbricus  terrestris,  on  the  other  hand, 
the  photo-negative  reactions  in  bright  light  are  controlled  by  the  head -ganglion, 
while  the  photo-jDOsitive  reactions  in  dim  light  are  nnediated  by ;  the  ventral 
cord  ;  the  two  activities  are  mutually  antagonistic  but  normally  the  cephalic 
mechanism  is  dominant  (Prosser,  1934).  Again,  the  possession  of  both  ocelli 
and  compound  eyes  by  many  insects,  the  first  sometimes  reacting  to  polarized 
light  and  orientative  in  function,  and  the  second  to  ordinary  light  as  well  and 
also  subserving  form  vision,  is  an  example  of  two  mechanisms  which  are 
supplementary  in  function  and  not  antagonistic  (Wellington,  1953). 

We  shall  now  discuss  the  occurrence  of  these  organs  in  the  inverte- 
brate phyla,  referring  back  to  the  previous  chapter  for  a  description  of 
their  ii:  nute  structure. 

^  Such  as  the  complex  eye  of  the  jelly-fish,  Charybdea  (p.  183). 
Such  as  the  simple  eyes  of  Insects  (p.  224). 


TYPICAL  PROTOZOA 

[Drawn  not  to  scale,  but  approximately  to  a  starulard  size.'] 


SARCODINA 


179 


A  mceba 


Foraminifei 


Radiolariaii  shell 


FLAGELT.ATA 


Euglena 


Trypanosoma 


Trichomonas 


Xoctiluca 
(see  Fig.  886) 


Gonyaulax 
(Dinoflagellate) 


Paramcpcium  Vorlicella 


SPOROZOA 


Suctorian 


Sporozoite 

of 
Plasmodium 


180  THE   EYE   IN   EVOLUTION 


Protozoa 

PROTOZOA  are  the  most  primitive  and  simplest  of  animals,  some  of 
which  might  with  equal  justification  be  considered  as  plants  ;  they  are 
essentially  single-celled  but  sometimes  form  loose  colonies  by  budding 
or  by  cell-division,  showing  some  degree  of  co-ordination  but  never 
forming  differentiated  tissues.  Of  all  animal  types  they  are  the  most 
numerous,  being  found  in  every  continent,  on  land,  in  fresh  water,  in 
the  seas  and  impartially  distributed  as  parasites  within  all  animals 
(including  some  of  their  own  kind),  among  which  not  the  least  fre- 
quented is  Man  ;  their  skeletons  contribute  largely  to  the  oozes  of  the 
seas  and  to  the  composition  of  the  rocks  of  which  the  land-masses  are 
made. 

Within  the  phylum  four  methods  of  activity  are  evident — 
amoeboid  movement,  flagellate  and  ciliary  progression,  and  encystment 
with  spore -formation,  characteristics  under  which  the  upwards  of 
15,000  species  may  be  conveniently  grouped  into  4  classes  (see  p.  179). 

SABCODiNA  (or  rhizopoda),  Organisms  which  progress  by  sending  out 
finger-Hke  pseudopodia  into  which  the  protoplasm  of  the  cell  pours  itself.  This 
class  comprises  such  types  as  the  fresh -water  Amoeba,  the  parasitic  Entamceha 
or  the  marine  Foraminifera  with  chalky  shells  and  Radiolaria  with  siliceous 
shells  which  after  death  enter  largely  into  the  formation  of  the  oozes  of  the  bed 
of  the  ocean. 

FLAGELLATA  (or  mastigophora),  Organisms  which  swim  by  the  lashing 
movements  of  one  or  a  few  whip-like  flagella.  The  class  comprises  such  types 
as  the  common  Euglena  and  colonial  forms  such  as  Volvox  almost  universal  in 
fresh-water  ponds,  the  parasitic,  disease-producing  Trypanosomes  and  Tricho- 
monads,  Dinoflagellates  including  Noctiluca  which  gives  luminescence  to  the  seas,^ 
and  Cystoflagellates,  important  constituents  of  the  plankton  of  lakes  and  the 
oceans. 

ciliophora,  organisms  which  progress  by  the  coordinated  movements  of 
many  hair-like  cilia.  The  class  comprises  the  Ciliates  (such  common  types  as 
the  slipper-shaped  Paramoscium,  the  bell-shaped  Vorticella  or  the  trumpet- 
shaped  Stentor)  and  the  Suctorians  which  lose  their  cilia  in  adult  life  and  in  their 
place  develop  tentacles  used  as  suckers  by  which  they  capture  and  suck  out  the 
bodies  of  their  protozoan  prey. 

sporozoa,  encysted  organisms  without  a  locomotive  mechanism  ;  they  are 
parasitic  on  almost  every  species  of  animal  and  are  spore-forming  in  habit 
(Coccidia,  Hsemosporidia,  Plasmodium,  etc.). 

In  view  of  the  fact  that  the  response  to  light  in  these  primitive 
forms  is  motorial,  it  is  not  surprising  that  receptors  are  not  found  in  the 
passive  parasitic  Sporozoa  ;  in  the  first  three  classes  responses  to  light 
are  found  among  the  freely-swimming  active  types,  but  as  would  be 
expected  in  imicellular  organisms,  the  receptor  mechanisms  are  of  the 
most  pr  i   itive  nature.     In  the  Sarcodina  (Amceba)  and  some  Ciliates 

1  p.  738. 


PARAZOA 


181 


{Paramoecmm)  sensitivity  to  light  is  diffuse  ;  in  other  Cihates  {Stentor) 
it  is  localized  to  a  part  of  the  organism  but  without  apparent  specific 
mechanism  ;  but  even  at  this  primitive  unicellular  stage  an  obvious 
localization  of  function  may  be  attained  by  the  development  of  an 
EYE-SPOT  and  the  efficiency  of  the  organelle  increased,  particularly  in 
the  acquirement  of  a  crude  directional  appreciation,  by  the  provision 
of  pigment  (as  in  Euglena)  ^  or  even  of  a  primitive  refractile  mechanism 
(as  in  some  Dinoflagellates).^ 

Parazoa 

The  SPONGES  (porifera),  sessile  marine  animals  which  form  living 
thickets  in  the  sea,  represent  a  cul-de-sac  in  evolution  between  Protozoa 
and  Metazoa  dating  back  almost  to  the  beginning  of  geological  records. 
They  are  the  simplest  multicellular  animals  and  show  the  beginnings 
of  the  development  of  a  ""  body  "  composed  of  tissues  ;  but  although 
there  is  cellular  differentiation  there  is  little  cellular  co-ordination. 
Being  vegetative  and  sedentary  in  habit  they  have  no  need  of  sense- 
organs  as  they  lie  moored  to  rocks  or  sea-weed.  They  possess  no  nerve 
cells  but  the  body  cells  retain  properties  of  an  irritability  of  a  low 
level  ;  and  in  the  active  larval  forms  of  certain  types  (the  simple 
sponge,  Leucosolenia)  apolar  light-sensitive  cells  of  the  most  elementary 
type  have  been  described  (Minchin,  1896). 

Invertebrate  Metazoa 

In  Metazoa — which  includes  all  animal  species  apart  from  the 
Protozoa  and  Parazoa — -the  development  of  specialized  cells  and  their 
eventual  co-ordination  into  distinct  organs  allow  the  evolution  of 
specific  sensory  activities  as  the  term  is  generally  understood.  These 
we  shall  now  study,  but  it  must  be  remembered  that  the  Invertebrates 
(or  Non-chordates)  do  not  form  a  homogeneous  sub-kingdom  but  rather 
represent  an  assemblage  of  unrelated  groups  of  animals  which  have 
little  in  common  except  the  negative  attribute  of  not  being  provided 
with  a  dorsal  nerve-cord  with  its  supporting  axis  or  with  gill-slits. 
From  our  restricted  point  of  view  there  is  the  dramatic  diff"erence  that 
(with  few  exceptions)  the  eye  when  present  is  developed  from  the  skin, 
while  in  Vertebrates  it  originates  as  an  outgrowth  of  the  brain. 

cgelexterata 

CCELENTERATES  are  simply  formed  animals  with  a  body-cavity 
(coelom)  and  digestive  cavity(enteron)  combined  so  that  the  body  is  formed 
as  a  sac  with  an  opening  at  one  end  only.  They  show  the  beginnings  of 
separate  organs  witli  a  consequent  division  of  labour,  and  among  them 


Leucosolenia 


Sycon 


126. 


-  p.  126. 


182 


THE   EYE   IN   EVOLUTION 


Hydra 


Obelia  medusoid 


Obelia  polyp 


Sea-anemone 


Comb  jelly 
(see  Figs.  887-8) 


visual  structures  of  some  complexity  first  make  their  appearance.  The 
phylum  may  be  divided  into  two  sub-phyla — the  cnidaria,  provided 
with  numerous  stinging  cells  (kvlSy),  a  nettle),  and  acnidaria,  wherein 
these  are  replaced  by  adhesive  cells.  The  first-sub-phylum  is  divided 
into  3  classes  : 

HYDROZOA,  comprising  solitary  polyps  such  as  tlie  fresh-water  Hydra,  the 
marine  Hydroids,  branching  colonial  polyps  of  vegetative  appearance  liberating 
freely-swimming  Hydromedusie  {Obelia,  Sarsia,  etc.)  and  some  j^elagic  colonial 
forms. 

SCYPHOZOA  ("  cup  animals  "),  marine  jellyfish,  free-swimming  medusae, 
typically  umbrella-shaped  with  the  important  organs  situated  on  the  margin  or 
under-surface. 

ANTHOZOA  ("  flower  animals  "),  sessile  marine  polyjas  with  no  medusa- 
forms,  such  as  sea-anemones,  sea-fans,  sea-pens  and  corals. 

ACNIDARIA,  comprising  the  Ctenophnra  (comb-jellies  or  sea-gooseberries), 
delicate  freely-swimming  globular  organisms,  pelagic  in  habit,  gelatinous  and 
transparent,  beautifully  iridescent  in  the  sunlight  and  often  luminescent  in  the 
dark,^  provided  with  comb-like  rows  of  cilia. 

The  degree  of  elaboration  of  the  visual  receptors  varies  with  the 
motility  of  the  organism,  and  many  Coelenterates  are  sessile,  plant-like 
zoophytes  ;  eyes  are  therefore  confined  to  the  mobile  medusae  and  these 
are  of  a  very  primitive  nature,^  while  the  sessile  polyps  of  this  phylum 
(hydroid  forms  and  all  Anthozoa)  have  no  sense  organs  or,  at  most, 
contact  photoreceptors  of  the  most  elementary  type.^ 

The  Ctenophora  are  provided  with  a  sense  organ  at  the  upper  pole  of  the 
organism  consisting  of  a  mass  of  limestone  particles  sup- 
ported on  cilia  associated  with  sensory  cells  communicating 
by  nerve  fibrils  with  the  swimming-combs;  this  is  considered 
to  act  as  a  statocyst  or  balancing  device  and  visual  organs 
are  absent. 


Among  the  Hydrozoa,  some  fresh-water  forms 
are  sensitive  to  light  but  possess  no  detectable  visual 
organs  ;  a  hydra,  for  example,  will  migrate  towards 
the  lighted  side  of  its  container  where,  incidentally, 
there  are  usually  more  food-organisms.  In  some 
freely-swimming  Hydromedusae,  however,  externally 
visible  light-sensitive  organs  provided  with  sensory 
cells  and  pigment  and  sometimes  a  refringent  appara- 
tus may  be  found  in  the  tentacular  bulbs  at  the  bases 
of  the  tentacles  (Fig.  162)  ;    these  take  the  form  of 

'  p.  739. 
^'ir  detailed  information,  see  O.   and  R.   Hertwig  (1877) 
Ber^  S98),  Linko  (1900),  v.  Uexkull  (1909),  Lehmann  (1923). 

il6. 


Fig.  162.—  The 
Medusoid  Form 
OF  BoviiAi.sriL- 
LEA  (Margel/.s). 
M,     manubrium; 

R,     radial     canal  ; 

S,       sense       organ 

(after  Allman). 


Schewiakoff  (1889), 


CCELENTERATA 


183 


a  primitive  fiat  eye,  as  in  Turris  or  Lizzia  (Fig.  96),  or  are  invaginated 
as  an  elementary  cupulate  eye,  as  in  Sarsia  (O.  and  R.  Hertwig,  1878  ; 
Jourdan,  1889).  These  organisms  are  light-sensitive  and  extirpation  of 
the  tentacular  bulbs  with  the  ocelli  completely  abolishes  the  response 
to  light. 

Among  the  jellyfish  (Scyphozoa)  more  elaborate  organs  are  seen. 
In  the  common  jellyfish.  Aurelia  aurita,  which  is  found  in  great  shoals 
around  the  British  coast,  eight  sense-organs  (tentaculocysts)  arise 
as  modifications  of  tentacles  ;  each,  lying  in  the  protection  of  a  marginal 


Figs.    163  and    1(54. — The  Common  Jellyj^sh,  Acrelia   aurita. 


Fig.  163. — Side  view  of  the  jellyfish,  showing  the 
numerous  marginal  tentacles  hanging  from  the 
border  of  the  convex  umbrella,  and  the  dependent 
oral  arms.  The  margin  of  the  umbrella  is  broken 
by  8  notches,  the  marginal  lappets  (L). 


Fig.  164. — A  marginal 
notch,  showing  a  ten- 
taculocyst  comprised  of 
two  olfactory  pits,  OP, 
a  calcareous  concre- 
tion, C,  and  an  ocellus, 
OC  (modified  from 
Lankester). 


niche,  has  three  types  of  sensory  cells — red  or  black  pigmented  cells 
responding  to  light,  "  olfactory  "  cells  with  a  chemical  appreciation, 
and  club -like  cells  containing  calcareous  concretions  with  a  balancing 
function  (Figs.  163-4). 

Exceptionally,  as  in  the  Cubomedusan,  Charybdea,  a  large  ocellus  has  been 
reported  with  a  cellular  lens,  a  vitreous  structure  and  a  complex  retina — an 
organ  structurally  capable  of  some  degree  of  visual  imagery  (Fig.  102)  (Schewia- 
koff,  1889  ;  Berger,  1898).  The  biological  value  of  this  elaboration  in  a  brainless 
organism  is  somewhat  speculative. 


ECHINODERMATA 


Among  ECHiNODERMS  ("  spiny  skinned  "),  a  phylum  characterized 
by  its  radial  symmetry,  visual  organs  are  rudimentary.    This  would 


184 


THE   EYE   IN   EVOLUTION 


Starfish 


Brittle-star 


be  anticipated  from  the  absence  of  centralization  in  the  nervous 
system,  associated  presumably  with  the  absence  of  a  head  region, 
and  from  the  characteristically  sluggish  and  sedentary  habits  of  its 
members.     The  phylum  is  divided  into  5  extant  classes  : 

ASTEROiDEA,  or  starfishes,  motile  but  sluggish  organisms. 

OPHiUKOiDEA  or  brittle-stars,  resembling  starfishes  but  with  the  arms 
sharply  marked  off  from  the  central  disc. 

ECHINOIDEA  or  sea-urchins,  living  off  rocky  coasts,  with  a  round  pin- 
cushion-like body  covered  with  plates  and  provided  with  long  sharp  spines. 

HOLOTHUEOiDEA  Or  sea-cucumbers,  worm-like  creatures  with  calcareous 
plates,  occurring  in  most  seas. 

CRiNOiDEA,  sea-lilies  or  feather-stars,  stalked  forms  anchored  on  rocks  or 


Free-swimming 
feather-star 


Fig.  165. — The  Iridophokes  ix  the  .Sea-urchin,  Djadema  aatjllarum. 

Section  through  a  cluster  of  iridophores,  I  ;  E,  epidermal  layer  ;  M, 
melanophores,  underneath  which  lies  the  superficial  nerve  layer  (fixed  Bouin  ; 
stained  Masson's  argentaffine  reaction  ;  counter-stained  Mallory's  triple 
stain.     (Approx.   X  500)  (N.  Millott). 

in  mud  usually  at  great  depths,  with  appendages  (cirri)  and  branching  arms 
growing  from  a  central  cujd  ;    feather-stars  become  free-swimming  in  adult  life. 

In  most  Echinoderms  the  skin  is  diffusely  sensitive  to  light, 
particularly  in  sea-cucumbers  (Crozier,  1914-15)  ;  in  brittle-stars  and 
feather-stars  there  are  no  special  sense  organs  ;  in  sea-cucumbers 
sense  organs  are  represented  by  statocysts  sometimes  present  at  the 
bases  of  the  tentacles,  and  tactile  processes  sometimes  present  on  the 
dorsal  surface  of  some  of  the  creeping  forms  ;  "  eyes  "  are  present  only 
in  starfishes. 

The  diffuse  dermatoptic  sense  shows  interesting  variations.  Thus  in  some 
starfishes  the  body-surface  is  said  to  be  sensitive  to  changes  in  intensity,  the 
podia  and  skin  gills  to  steady  light  ;  in  some  sea-cucumbers  {Synapta)  the  whole 
sn;  •■■  is  sensitive  to  both,  while  in  others  {Holothuria  surinamensis)  the  rim  of 
the  •■''  ica  is  particularly  sensitive,  the  posterior  end  and  tentacles  less  so  and 
the  )       ia  least.     In  the  sea-urchin,  Paracentrotus  lividus,  the  apical  poles  are 


ECHINODERMATA 


185 


Fig.   166. — Diagram  of  a  Very  Young  Asteroid 
At  the  base  of  the  5  terminal  tentacles  is  an  optic  cushion  with  a  bright  red 
ocellus,  Oc,  connected  by  an  epidermal  radial  nerve  which  runs  to  the  central 
nerve  pentagon  surrounding  the  mouth  (after  Lang).     Compare  Plate  I. 

said  to  show  the  most  rapid  reactions  (Scheer,  1956).  In  the  Echinoid,  Diadema, 
the  distribution  of  sensitivity  corresponds  to  the  distribution  of  the  nerve 
elements  and  it  may  be  that  these  are  directly  stimulated  bj-  light  as  we  have 
seen  to  occur  in  the  apolar  light-sensitive  cells  of  w- orms  (Millott,  1954).  On  the 
other  hand,  photosensitive  pigments  may  be  present  in  minute  quantities,  but 
there  is  yet  no  evidence  as  to  their  nature. 

Many  sea-urchins  have  the  same  primitive  sensitivity  associated  particu- 
larly with  their  pigmented  spicules  which  move  on  the  stimulus  of  light  (v. 
Uexkiill,  1900),  and  in  some  types  characteristic  iridescent  bodies  associated  with 
melanin  pigment  lie  near  the  spines  {Diadema  antillarutti)  (P.  and  F.  Sarasin, 
1887  ;  Dahlgren,  1916;  Millott,  1950-54).  These  represent  clusters  of  regularly 
arranged  plates  resembling  iridoi^hores  ^  in  their  arrangement,  which  presumably 
act  by  reflecting  the  light  onto  the  sensitive 
spines  (Millott,  1953)  (Fig.  165).  It  is  of  historical 
interest  that  the  Sarasins  (1887),  in  a  much 
quoted  paper,  described  similar  structures  in 
Diadema  setosum,  an  allied  species  inhabiting 
the  Indian  Ocean,  as  being  "eyes"  composed 
of  several  hundred  polygonal  corneal  facets,  a 
vitreous-like  jelly  and  a  ''  retina",  but  without 
nerve  fibres. 


Cuf 


In  STARFISHES  (Asteroids  such  as  the 
common  five-rayed  Asterias),  although  the 
skin  is  often  diffusely  light-sensitive,  on 
the  tip  of  each  of  the  five  arms  a  visual 

1  Compare   iridocytes,  p.  89. 


Fig.  167. — The  optic  cushion  of 
the  Asteroid 

Cut,  cuticle  ;  CT,  connective 
tissue  ;  Ep,  epithelium  ;  NN, 
nerve-net  ;    P,  pigment  cells. 


Sea-cucumber, 
Holothuria 


The  sea-urchin, 
Diadema 


186  THE   EYE   IN   EVOLUTION 

organ  is  formed  as  a  modified  tube-foot  lying  on  a  slight  elevation  (the 
"  optic  cushion  ")  on  the  dorsal  surface  of  the  terminal  ossicle  (Fig.  166). 
The  organ  is  bright  red  due  to  the  presence  of  ^-carotene  and  esterified 
astaxanthin  and  consists  of  an  aggregation  of  several  cupulate  ocelli  of 
the  simplest  type  covered  by  cuticle  and  lined  by  sensory  and  pig- 
mented cells  (Plate  I  ;  Fig.  167)  (PfefiFer,  1901)  ;  a  central  lenticular 
body  may  serve  to  concentrate  light  upon  the  receptive  elements  (van 
Weel,  1935  ;  Smith,  1937).  The  optical  function  of  this  organ  in 
Asterias  has  been  convincingly  demonstrated  by  Hartline  and  his  co- 
workers (1952)  who  recorded  the  electric  impulses  following  stimulation 
by  light.    The  terminal  tube-foot  appears  to  be  olfactory  in  function. 

Berger.    J.  comp.  Neurol.  Psychol.,  8,  223  Philos.  Trans.  B,  238,  187  (1954). 

(1898).  Minchin.  Proc.  roy.  Soc.  B,  60,  42  (1896). 

Crozier.    ^mer.  J.  P/i^sioZ.,  36,  8  (1914).  Pfeffer.      Zool.  Jb.,   Abt.   Anat.,   14,    523 

Zool.  Jb.,  Abt.   Zool.   Physiol.,  35,  233  (1901). 

(1915).  Prosser.     J.   cell.   comp.   Physiol.,  4,   363 

Dahlgren.      J.    Franklin   Inst.,    181,    377  (1934). 

(1916).  J.  comp.  iVewroZ.,  59,  61  (1934). 

Hartline,   Wagner  and  MacNichol.     Cold  Sarasin,    P.    and    F.      Ergebn.    naturwiss. 

Spr.  Harb.  Symp. Quant.  Biol.,  17,  125  Forsch.Ceylon,V^\esh&den,  1,  1  (1887). 

(1952).  Scheer.         Naturwissenschaften,     43,     501 

Hertwig,  O.  and  R.    Jena.  Z.  Naturwiss.,  (1956). 

11,  355  (1877).  Schewiakoff.    Morphol.  Jb.,  15,  21  (1889). 

Das  Nervensysteyn  u.   die  Sinnesorgane  Smith.  Philos.  Trans.  B.,  227,  HI  (1937). 

d.  Medusen,  Leipzig  (1878).  von  Uexkiill.  Z.  Biol.,  40,  447  (1900). 

Jourdan.       Les    sens    chez    les    animaux  Umwelt   u.   Innenwelt   d.    Tiere,   Berlin 

inferieurs,  Paris  (1889).  (1909). 

Lehmann.     Zool.  Jb.,  Abt.  Zool.  Physiol.,  Viaud    and    Medioni.      C.    R.    Soc.    Biol. 

39,  321  (1923).  (Paris),  143,  1221  (1949). 

Linko.     Acad.  Imp.    Sci.    St.   Petersburg,  van    Weel.     Arch,     neerl.     Zool.,     1,    347 

Mem.  Ser.  8,  10  (1900).  (1935). 

Millott.     Biol.  Bull.,  99, 'S29  (1950).  Wellington.      Nature    (Lond.),    172,    1177 

Nature  (Lond.),  170,  325  (1952)  ;    171,  (1953). 

973  (1953). 


WORMS 

The  large  group  of  "  worms  "  shows  a  variety  of  visual  organs  as 
pleomorphic  as  the  multitude  of  forms  which  constitute  this  loose 
grouping  of  animals,  showing  every  variation  from  a  unicellular  eye  to 
a  relatively  complex  organ.  In  some  cases  the  surface  of  the  whole  body 
seems  to  be  sensitive  to  light  and  it  has  not  been  possible  to  identify 
specific  sensory  cells  ;  in  most  cases,  however,  specialized  sensory 
structures  occur,  for  the  elucidation  of  which  we  are  largely  indebted 
to  the  classical  work  of  Richard  Hesse  (1899-1908).  Their  presence, 
their  number,  and  the  degree  of  their  differentiation  vary  with  the 
animal's  mode  of  life.  This  is  the  lowest  group  in  the  animal  kingdom 
to  show  l>ilateral  symmetry  and  the  sense  organs  share  in  this  general 
scheme  distribution  ;  moreover,  these  organs  are  usually  concen- 
trated 1  rds  the  head-end  of  the  animal  where  they  are  of  greatest 
biologic;        lue. 


PLATE  I 
The  Light-sensitive  Apparatus  of  the  Starfish 


^^imf>^ 


Fitt.  1. — Maiih<istcrliis  (/Idruilis,  showing  th(>  ]>nsiti()ii  of  the  eye-spot,  e.s. 
one  of  which  is  jjresent  at  the  tip  of  each  of  the  five  arms. 


Fig.  2. — The  excised  eye-spot  (optic  cushion)  showing  the 
o])tic  cups,  o.c.  They  have  a  striking  red  colom-  due  to 
L'-carotene  and  esterified  astaxanthin;  it  is  to  be  noted 
that  some  of  the  colour  of  the  body-wall,  which  is  also 
light-sensitive,  is  due  to  the  same  ])igments  (X.  ]\Iillott, 
Endeavour,  1957). 


S.O. — VOL.1 


[To  face  2>-  186. 


WORMS 


187 


These  photoreceptors  are  of  the  most  varied  types  and  many  species 
possess  eyes  of  more  than  one  variety.  The  neuro -sensory  cells  may  be 
either  apolar  in  type  provided  with  an  internal  optic  organelle,  or 
bipolar,  provided  with  a  ciliated  or  striated  border  ^  :  they  may  occur 
as  single  cells  or  in  groups  forming  an  eye  of  either  the  subepithelial  or 
epithelial  variety,  in  which  case  it  may  show  a  flat,  cupulate  or  vesicular 
arrangement.  Pigment  is  a  constant  association,  situated  within  the 
sensory  cells  or  in  special  supporting  cells.  If  a  refractive  medium  is 
present  it  may  be  formed  either  from  the  retinal  or  the  epidermal  cells, 
while  light-refracting  structures  are  usually  cuticular  in  origin.  As  a 
general  rule  their  function  can  only  be  the  primitive  ability  to  detect 
light,  but  the  visual  organs  of  some  types,  such  as  some  polychaete 
worms,  are  structurally  capable  of  some  degree  of  localization  and 
resolution  (a  directional  eye)  and  perhaps  even  of  visual  imagery. 

UNSEGMEXTED    WORMS 

The  unsegmented  worms  may  be  divided  into  three  phyla — flat- 
worms,  ribbon-worms,  and  thread-worms. 

1.  PLATYHELMINTHES  or  FLAT-WORMS  Constitute  a  gi(jup  of  very  simply 
organized  creatures  the  members  of  which  show  the  progressive  degeneration 
associated  with  parasitism.     It  is  divided  into  3  main  classes  : 

(a)  TURBELLARiANS,  freely -Swimming  leaf-shaped  aquatic  creatures  of 
carniv^orous  habit,  frequenting  brackish  or  salt  water  or  moist  places  on  land  ; 
the  name  is  derived  from  the  turbulence  caused  in  the  water  by  the  beating  of 
their  cilia  when  they  swim.  They  are  classified  accoi'ding  to  the  arrangement 
of  the  gut — the  minute  marine  Actf-la  (without  intestine),  the  small  salt  and 
fresh-water  Rhabdocojla  (rod-shaped  intestine),  the  (mainly)  marine  Alloeocoela 
(irregular  intestine),  the  small,  flat,  elongated  Tricladida  (3-branched  intestine) 
found  in  fresh  or  salt  water  or  on  land  (including  the  Planaria),  and  the  large, 
leaf-like,  marine  Polycladida  (many-branched  intestine). 

(6)  TREMATODES  or  FLUKES,  leaf-like  parasites,  external  or  internal,  found 
on  or  in  all  types  of  \'ertebrates,  clinging  to  their  hosts  with  suckers.  Examples 
are  the  liver-fluke,  Fasciola  hepatica,  which  infests  the  livers  of  sheep  and 
cattle,  or  the  Schistosoma  Juematobia  which  causes  bilharziasis. 

(c)  CESTODES  or  TAPE-WORMS,  endoparasites,  frequenting  the  alimentary 
canal  of  Vertebrates,  including  domestic  animals  and  man,  such  as  Taenia  eckino- 
coccus,  or  T.  solium. 

2.  NEMERTiNES  or  RIBBON-WORMS,  ribbon-  or  thread-like  in  shape,  often 
vividly  multi-coloured,  varying  in  size  from  under  an  inch  to  enormous  lengths 
(25  metres  in  Linens)  and  provided  with  cilia  and  a  remarkable  retractile  pro- 
boscis forming  a  tactile  organ  used  to  capture  prey.  Most  are  marine  in  habitat, 
creeping  in  the  mud  and  under  stones  ;  a  few  are  found  in  fresh-water  (Prostoma); 
some  are  terrestrial  (Geonemertes)  ;  and  a  few  live  commensally  with  bivalves 
or  ascidians. 

3.  NEMATODES,  ROUND-  Or  THREAD-WORMS,  Cylindrical  in  shape  and  often 
minute,  which  teem  in  the  soil  or  in  water  and  are  often  endojjarasitic  in  plants 
and  animals  (Ascaris,  Trichinella,  Ankylostoma,  Filaria,  etc.)  ;  but  free-living 
forms  occur  at  any  rate  in  part  of  the  life-cycle. 

1  p.  127. 


Polyclad, 
Leptoplana 


Schistosoma 


Teen  in 
echinococcus 


THE   EYE    IN   EVOLUTION 

The  PLATYHELMiNTHES  have  sense  organs  only  of  the  most 
rudimentary  type — if  any.  The  freely-hving  turbellarians  (Plana- 
rians,  etc.)  are  the  most  adequately  equipped  with  eyes  (Figs.  168  to 
170).  These  may  be  merely  two  or  four  in  number,  in  which  case  they 
lie  on  the  dorsal  aspect  of  the  head-end  associated  with  the  tentacles 
near  the  cerebral  ganglion,  as  in  the  fresh-water  Rhabdocoela  ;  but 
others  such  as  the  marine  Polycladida  may  possess  several  hundred. 
A  common  arrangement,  well  seen  in  the  Tricladida,  is  that  these 
multiple  ocelli  are  distributed  around  the  circumference  of  the  body 
concentrated  particularly  at  the  anterior  margin  (Figs.  168  and  170) 
(Busch.  1851  ;    Hyman,  1938-51).     The  eyes  are  always  very  elemen- 


FiGS.   168  TO   170. — The  Eyes  of  Turbellarian  Worms. 

\k  s-  „ 

M 


Fig.  168. — A  land  pla- 
narian,  Geoplana  mexi- 
cana. 

There  is  a  row  of  eyes 
along  the  entire  margin 
of  the  animal  (after 
Hyman). 


Fig.     169.— The    eyes    of 
the     pelagic     Rhabdo- 
coele,     Alaurina    proli- 
fera. 
S,      papillated      snout  ; 

M,  mouth  ;    E,  paired  eye 

(after  Busch). 


Fig.  170.— The  eyes  of 
the  fresh-water  pla- 
narian,  Polycelis  coro- 
nata.  They  are  concen- 
trated at  the  head-end 
(after  Hyman). 


Dendrocoelum 


tary,  and  lacking  a  dioptric  apparatus  are  capable  only  of  light 
perception  although  a  directional  appreciation  may  be  evident 
(Taliaferro,  1920).  The  number  of  visual  cells  is  said  to  vary  between 
1  and  200  (Hesse,  1896  ;  Schmidt,  1902).  Occasionally,  as  in 
Dendroccehim,  they  are  of  the  flat  epithelial  type  (Fig.  95).  Usually 
they  are  of  the  subepithelial  type,  appearing  as  minute  pigmented 
spots  about  0"1  mm.  in  diameter  and  consisting  of  a  pigmented  goblet 
enclosing  the  sensory  cells  (Figs.  91  and  92).  In  these  the  sensory 
ce-lr-  .T,re  of  the  bipolar  type  with  a  striated  margin  facing  away  from 
tlK  direction  of  light  to  form  an  inverted  retina.  When  the  eyes  are 
nea  ''hi^  cerebral  ganglion  the  sensory  fibres  enter  the  latter  directly  ; 
othc       -e  they  enter  the  peripheral  nerve-net. 


WORMS 


189 


In  some  Rhabdocoela  {Stenostonuni)  curious  hemispherical  bodies  consisting 
of  refringent  granules  lying  underneath  a  bowl -shaped  mass  have  been  credited 
with  a  photosensitive  function  ;  there  is  no  good  evidence,  however,  for  this 
assumption. 

Eyes  are  lacking  in  the  cave-dwelling  planarians  (Kenkiidae)  and  in  endo- 
parasitic  Rhabdocoela.^ 

TREMATODES  may  possess  simple  ocelli  in  the  larval  stage  (as  in 
the  liver-fluke.  Fasciola  hepatica),  but  the  adults,  leading  an  essentially 
parasitic  existence,  rarely  possess  sense  organs.  If  they  are  present 
they  are  of  the  simjDlest  type,  usually  consisting  of  a  single  cell  with  a 
striated  border  invested  by  a  cup  of  pigment  (Hesse,  1897  ;  Andre, 
1910  ;    Faust,  1918)  ;    a  typical  example  is  seen  in  the  luiicellular  eye 


Fasciola  hepatica 


Figs.   171  and   172. — The  Eyes  of  Xemertine  Worms. 
E 


Fig.  171. — Lineus  ruber. 
E.  eyes  (after  Hyman) 


Fig.    172. — The   head   of  Ampkiporus 
angulatus.    E,  eyes  (after  Hyman). 


of   Tristomum   impiUosum.    a   marine   Trematode   jiarasitic   on   fishes 

(Fig.  87). 

CESTODES,  in  keeping  with  their  endoparasitic  life,  are  without  sense 
organs. - 

Among  the  nemertines,  most  of  which  are  freely-living  and  marine 
in  habitat,  rudimentary  eyes  of  the  same  subepithelial  type  as  occur  in 
flat-worms  are  general  and  occasionally  are  very  numerous  (Figs.  17 1-72). 
They  are  always  limited  to  the  anterior  end  of  the  animal.  Some 
species  possess  two  eyes,  others  four  or  six  on  the  prostomium  ;  others 
up  to  250  eyes  [Amphiporus)  arranged  in  clusters  or  rows,  while  the 
number  may  vary  in  different  individuals  of  the  same  species.  The 
eyes  are  nearly  always  subepithelial  in  type  consisting  of  bipolar  cells 
terminating  in  a  brush  border  enclosed  within  a  pigment  cup  of 
epithehum  (Hilton,  1921)  (Fig.  93).    The  eyes  of  the  terrestrial  genus, 

1  pp.  724,  733.  "^  p.  734. 


Amphiporus 


190 


THE   EYE   IN  EVOLUTION 


Nematode, 
Ascaris 


Arenirola 


Hcemadipsa 


Luinbricus 


Geonemertes,  differ  from  the  usual  type.  In  these  the  pigmented 
epithehum  forms  a  complete  circle  within  which  is  a  mass  of  refractile 
material  ;  the  nuclei  of  the  sensory  cells  are  arranged  outside  the  circle 
of  pigment  and  their  distal  terminations  pass  through  it  into  the 
central  refractile  mass  (Schroder,  1918). 

In  the  NEMATODES,  the  majority  of  which  are  endoparasitic,  sense  organs 
are  Hmited  to  papillae  on  the  lips  ;  in  the  free-living  sexual  state,  however, 
rudimentary  eyes  may  exist,  consisting  of  a  lens-like  cuticular  body  resting  on  a 
cup  of  pigmented  cells  (Steiner,  1916  ;   Hilton,  1921  ;    Schulz,  1931). 

SEGMENTED  WOBMS  (ANNELIDS) 

The  segmented  worms  exhibit  much  diversity  in  habit  and 
structure  but  their  essential  characteristics  are  segmentation  of  the 
body  with  paired  appendages  on  each  segment  and  a  closed  vascular 
system.  Annelids  are  found  both  in  marine  and  fresh  water  and  on 
land,  and  in  the  entire  phylum  more  than  6,500  species  are  known. 
These  are  divided  into  4  classes,  the  first  two  of  which  are  provided  with 
chitinous  bristles  or  setae  for  locomotion. 

1.  OLiGOCH^TES  (with  few  setne),  hermaphroditic  creatures,  essentially 
terrestrial  in  habit,  typified  in  the  common  earthworm,  Lumhricus  terrestris,  or 
the  tiny  aquatic  mud-worms  living  in  brooks  or  between  tide-marks. 

2.  polycHjEtes  (with  many  setae),  essentially  marine  in  habit  ;  in  them 
the  sexes  are  separate.  Two  types  exist,  distinguished  by  their  habits.  The 
more  active  forms  (errantia)  are  typified  in  the  common  lob-worm,  Arenicola 
marina,  found  burrowing  in  sandy  beaches,  or  the  freely-swimming  types,  such 
as  the  rag-worm.  Nereis.  The  sedentary  forms  (sedentaria)  are  tubicolous  in 
habit  leading  a  sluggish  life  within  tubes,  limy,  sandy  or  gelatinous  ;  as  an 
adaptive  characteristic  the  tentacles,  gills  and  sensory  organs  are  aggregated  in 
the  anterior  part  of  the  woi-m  which  protrudes  from  the  tube. 

3.  ARCHiANNELiDS  Comprise  a  small  and  anomalous  class  of  simple  marine 
worms  with  juvenile  characteristics  and  without  seta?,  freely  swimming  or 
burrowing  in  sand  and  gravel. 

4.  HiRUDiNES  or  LEECHES  form  a  highly  specialized  and  much  modified 
class,  most  of  which  live  in  fresh  water  in  ponds  or  sluggish  streams  although 
a  few  are  marine  and  others  (the  wiry  land-leeches  of  the  Far  Eastern  jungles, 
Hcemadi])sa)  are  terrestrial,  living  in  inoist  places.  In  habit  they  are  greedily 
suctorial,  sucking  the  blood  of  fishes,  amphibians  or  other  victims. 

Eyes  are  usually  lacking  in  the  oligoch^tes  ;  of  those  possessing 
visual  organs,  the  most  typical  example  is  the  earthworm,  Lumhricus 
terrestris.  Its  unicellular  light-sensitive  organs  distributed  in  the 
epithelium  and  aggregated  around  subepithelial  nerves  have  already 
])een  fully  described  ^  (Figs.  86,  88).  These  visual  elements  are  situated 
\N  iiere  they  are  of  the  greatest  biological  value,  being  concentrated  at 
til;      vo  extremities,  particularly  the  anterior. 


131. 


WORMS 


191 


Thvis  W.  N.  Hess  (1925)  found  that  in  the  prostomium  there  were  some 
440  light-sensitive  cells  in  the  epidermis  and  700  sitviated  in  nearby  nerve 
enlargements,  while  in  subsequent  segments  they  were  much  fewer.  Their  rela- 
tive numbers  in  corresponding  sinall  areas  (200  x  SOOti.)  on  the  dorsal  surface  of 
the  animal  are  as  follows — in  the  prostomium,  18  ;  1st  seginent,  10  ;  2nd  segment, 
5  ;  3rd  segment,  3  ;  40th  segment,  0  ;  antepenultimate  segment,  1  ;  penultimate 
segment,  1  ;  last  segment,  4.  The  segiuental  photic  sensitivity  varies  directly 
with  the  number  of  receptors,  and  the  distribution  of  light-sensitive  elements 
conforms  with  the  habits  of  the  earthworm. ^ 

Among  POLYCH.ETE  woEMS.  the  burrowing  lob-worm,  Are^iicola 
marina,  is  not  provided  with  visual  organs  although  the  prostomial 


Fig.   173. — The  Head   of  Nereis,  Showing  the  Four  Eyes. 

e,  eyes  ;  j,  jaw  ;  p,  palp  ;  pe,  peristomium  (first  two  segments  fused)  ; 
ph,  pharynx  ;  pp,  first  ordinaiy  paraijodium  ;\  pr,  prostomium;  t,  accessory 
teeth  ;  tc,  tentacular  cirri ;  te,  tentacle.  (From  Borradaile's  Manual  of 
Elementary  Zoology  ;    Oxford  University  Press.) 


lobes  are  diffusely  sensory.  In  contrast  with  the  burrowing  type, 
however,  the  freely-swimming  marine  polychaetes  show  a  much  richer 
development  (Fig.  173).  Of  these,  Nereis  is  a  typical  example.  This 
worm  has  four  prominent  eyes  situated  on  the  prostomium,  each  of 
the  cupulate  type  with  a  cuticle  externally  and  a  retina  internally 
formed  of  well-developed  sensory  cells  with  rod-like  receptor  endings 
(Fig.  101).  Other  forms,  such  as  Polyoplithalmus,  have  in  addition  to 
the  prostomial  eyes  similar  pairs  of  subepithelial  organs  in  many 
segments  of  the  body  ;  such  eyes  ^  are  formed  sometimes  on  each 
segment  {Myxicola  (esfhetica  ;  Eunice),  and  occasionally  on  the  anal 
segment  {Fabricia). 

A  much  more  complex  type  of  e}e  of  the  vesicular  type  is  found 

1   p.  572. 

^  These  organs,  usually  considered  to  be  "  eyes  "  are  said  by  some  to  be  liglit- 
producing  (p.  736)  (Benham,  1896). 


Nereis 


192 


THE   EYE   IN   EVOLUTION 


Branchiomma 


in  certain  pelagic  polychsetes  such  as  Alciopa  and  Eupolyodonfes,  the 
intimate  structure  of  which  has  already  been  described. ^  These  worms 
have  two  eyes,  sometimes  facing  forwards  {Eupolyodontes),  sometimes 
diverging  widely  (Alciopa)  (Fig.   174).     Each  organ  is  provided  with 

an  elaborate  retina,  a  lens,  an  accom- 
modative mechanism  and  extra-ocular 
muscles  suggesting  the  potentiality  for 
binocular  vision,  an  equipment  which 
seems  capable  of  considerable  visual 
powers  approximating  those  of  the 
Cephalopods.2  Little,  however,  is  known 
of  the  habits  of  these  worms. 

In  the  sedentary  tubicolous  poly- 
chsetes  (Potamilla,  Branchiomma,  Dasy- 
chone,  etc.)  the  ocelli  are  frequently 
grouped  in  masses  on  the  branchial  fila- 
ments to  form  a  composite  simple  eye 
of  great  complexity  (Brunotte,  1888  ; 
Andrews,  1891  ;  Hesse,  1896)  (Figs.  175  and  176)  ;  Vermilia  infundi- 
bulum  has  at  least  220  ocelli  on  the  external  aspect  of  each  branchium, 
a  total  of  some  11,000  eyes  (Parker  and  Haswell,  1940).  These 
creatures  live  within  their  tubes  from  out  of  which  extend  the  branchial 
plumes  bearing  the  filaments  on  each  of  which  there  is  one  or  more 
such  eyes  (Figs.    128,    129).     The  curious  thing,  however,  is  that  in 

Figs.   175  and   176. — The  Complex  Eyes  of  Tubicolous  Polych^tes. 

e 


Fig.  174. — The  Anterior  End  of 
THE  Polych^te  Wokm,  Alciopa. 

Showing  the  two  large  eyes  (after 
Greeff). 


Fig.   175. 


Fig.   176. 


The  secondary  filaments  are  seen  issuing  horizontally  from  the  central 
axis  of  the  branchial  filament.  Fig.  175,  Branchiomma,  showing  the  single 
complex  eye,  e,  near  the  termination  of  the  central  axis.  Fig.  176,  Dasychone, 
showing  the  row  of  complex  eyes  (2  of  which  are  marked  e)  running  up  and 
';osvn  the  central  axis  (after  Benham,  Camh.  Nat.  Hist.). 


143. 


Fig.  112. 


WORMS 


193 


Branchiomma,  at  any  rate,  these  structures  do  not  seem  to  be  essential 
for  the  most  characteristic  responses  of  the  worm  to  changes  in  tlie 
intensity  of  hght  (Millott,  1957)  ;   the  position  is  therefore  somewhat 
anomalous. 

In  the  simple  marine  archiannelids,  eyes  of  a  similar 
type  are  found.  In  Dinophilus,  for  example,  a  minute  worm 
found  among  alga^,  two  kidney-shaped  pigmented  eyes  are 
found  on  the  prostomium  (Hilton,  1924)  (Fig.  177). 

LEECHES  (hirudinea)  may  be  provided  with 
visual  organs  of  a  simple  type  varying  in  number 
from  2  to  10  (Hesse,  1897  ;  Herter,  1932)  ;  they  are 
incajDable  of  optical  imagery  although  highly  light- 
sensitive,  but  in  some  species  may  be  absent.  They 
are  found  near  the  anterior  extremity  of  the  body 
and  vary  considerably  in  their  morphology,  but  the 
visual  cells  are  always  of  the  spherical  apolar  type 
with  a  central  optic  organelle  (Figs.  178-9). 


Fig.  177.— The 

rchiannelid, 

DlXOPUlLUS. 

Showing  the 

paired     ocelli,      Oc 
(after  Sheldon- 

Harmer). 


In  Branchellion  these  organs  are  unicellular;  in  Piscicola 
they  consist  of  12  cells  arranged  in  a  row  surrounded  by 
pigment.  In  Hcemopis  both  unicellular  and  multicellular 
ocelli  are  found  (Fig.  179).  In  the  common  medicinal  leech, 
Hirudo  medictnalis,  there  are  segmental  papilhe  with  a 
sensory  function  on  the  middle  ring  of  each  of  the  26  segments.  Although  all 
the  sense  organs  are  serially  homologous  the  pairs  on  the  dorsal  surface  of  the 
first  five  segments  are  purely  visual,  constituting  ten  "  eyes  "  (Fig.  90),  provided 
with  a  rich  nerve  supply  to  the  cerebral  ganglia.     At  the  other  extremity  the 


Branchellion 


Hirudo 


Figs.   178  and   179. — The  Eyes  of  Leeches. 


Fig.  178. — The  head  end  of  the  medicinal  leech, 
Hirudo  niedicinalis. 
The  dorsal  aspect.  The  body  is  divided  into 
segments,  each  of  which  contains  5  rings 
(annulae).  In  the  middle  ring  of  each  segment 
the  segmental  papillte  have  a  sensory  function. 
The  first  7  (and  the  last  3)  segments  have  less 
than  the  normal  number  of  rings,  and  the  first  5 
show  two  paired  eyes  as  larger  black  spots. 
El  to  Eg,  serially  homologous  with  the  sensory 
papillae  (see  Figs.  89-90)  (after  Parker  and 
Haswell). 

S.O.      VOL.  I. 


W^^ 

"<?linBK' 

Cy'*?w 

)'.^ 

■^X 

^^^^ 

^Jl^^KA 

'^ 

m), 

Fig.  179. — Solitary  and  aggre- 
gated eyes  of  the  horse-leech, 
Hcemopis  sanguisuga  (after 
Kappers). 


194 


THE   EYE   IN  EVOLUTION 


organs  are  probably  purely  tactile,  and  between  these  two  regions  the  sense  organs 
are  compound  since  they  contain  both  visual  and  tactile  cells  (Fig.  89).^ 


Chsetognath, 
Sagitta 


Subsidiary  Invertebrate  Phyla 

For  convenience,  four  small  and  subsidiary  phyla  of  the  Inverte- 
brates are  most  usefully  considered  here. 

CH^TOGNATHA  ("  bristle-jawed  ")  or  arrow-worms,  delicate,  translucent 
torpedo -shaped  creatures  comprising  some  30  species  which  swim  in  incredible 
numbers  in  great  shoals  among  the  plankton  of  all  seas,  have  well-developed 
eyes.  Spadella,  for  example,  or  Sagitta,  has  two  composite  simple  eyes  at  the 
anterior  extremity  of  its  body,  formed  by  the  union  of  5  ocelli,  the  structure  of 
which  has  already  been  described  (Fig.  132)  ;  although  presumably  tripartite, 
the  nerve  fibre  from  each  eye  is  gathered  into  a  single  optic  nerve  trunk. 

Figs.   180  and   181. — The  Eyes  of  Rotifera, 

L 


Fig.   180. — The  cerebral  eye. 

Section  through  the  cerebral  gan- 
glion of  Synchceta,  showing  two  cere- 
bral eyes,  E  (after  Peters). 


Fig.      181.— The     frontal 
eye. 

The  eye  of  Rhinoglena 
with  pigment  spot,  P,  and 
refractile  lens,  L  (after 
Stossberg). 


Rotifer 


Bryozoa 


BOTiFERA  ("  wheel-bearers  "),  the  beautiful  minute  wheel-animalcules, 
sometimes  of  fantastic  shape,  which  swim  so  abvindantly  with  the  aid  of  a  crown 
of  cilia  like  revolving  wheels  in  fresh  water,  damp  moss  or  the  sea  all  the 
world  over,  are  usually  highly  light-sensitive.  There  is  a  generalized  dermatoptic 
sense  which  evokes  a  positive  phototaxis,  but  exact  orientation  is  determined 
by  the  eyes  and  varies  with  their  morphological  development  (Viaud,  1938-43). 
Frequently  there  is  a  single  or  paired  cerebral  eye  embedded  in  the  dorsal 
nerve  ganglion  {Synchceta)  (Fig.  180).  In  other  species,  sometimes  in  addition 
to  the  cerebral  eyes,  there  is  one  or  two  frontal  or  lateral  eyes  (Fig.  181).  The 
cerebral  eye  consists  of  a  single  cell  resembling  a  brain  cell  ;  the  lateral  or 
frontal  eyes  are  epidermal  cells  inside  which  is  a  lens-like  body  associated  with 
a  mass  of  red  pigment  (Peters,  1931  ;  Stossberg,  1932).  Branchionus,  one  of 
the  commonest  members  of  this  class  which  inhabits  ponds  and  ditches  in 
abundance,  has  a  simple  unpaired  eye  surrounded  by  red  pigment  and  associated 
with  tufts  of  sensory  hairs,  situated  where  the  cerebral  ganglion  comes  into 
contact  with  the  body-wall  just  behind  the  wheel  of  cilia  at  the  anterior  end 
of  the  animal. 

POLYZOA  (bryozoa),  very  ancient  plant-like  organisms  which  include  fresh- 
W:ter  and  marine  forms  (sea-mats,  etc.)  are  sessile  colonial  corallines  or  "  moss 
ari        Is  "  which  grow  in  tufts  on  the  shores  or  in  pools  all  over  the  world  encrust- 

1  p.  133. 


MOLLUSCA 


195 


Fig.  182.— The 

Ocelli    (Oc)    of 
the     l.\rva     of 

THE  BrACHIO- 

POD,  ClSTELLA 

(afterGladstone). 


ing  seaweed,  rocks  and  piles  with  a  lace-like  coating,  and 
multiply  by  budding.  Some  1,800  species  have  been  des- 
cribed. The  larva?  of  some  species  during  their  short  freely- 
swimming  life  before  they  settle  on  the  rocks  or  mud,  are 
sometimes  provided  with  rudimentary  eyes.  Thus  the  larvae 
of  Bugula  turrila  which  have  4  or  5  slender  flagellae,  have  4 
brilliantly  red  spherical  eye-spots,  2  close  to  the  pyriform 
organ  and  2  larger  eye-spots  located  in  the  opposite  hemis- 
phere. The  larva  of  the  American  Bugula  flahellata  has  no 
light-sensitive  organs,  but  the  European  variety  has  10 
symmetrically  arranged  eye-spots  (Xit.sche,  1870  ;  Calvet, 
1900  ;    Grave,  1930  ;    Lynch,  1949). 


BRACHIOPODA  (lamp-shells),  marine  organisms  of 
great  anticiuitj^  which  have  existed  unchanged  since  the 
Palaeozoic  era  ^  and  are  found  in  the  seas  in  most  parts  of  the  world  covered  by 
their  shells  firmly  attached  to  rocks,  are  in  some  cases  devoid  of  sense  organs  ; 
in  the  freely-swimming  larvte  of  others,  patches  of  sensory  epithelium  form  paired 
eye-spots  immediately  over  the  cerebral  ganglion  which  disappear  when  the  larvie 
become  sessile  (Cistella)  (Fig.  182)  ;  but  rudimentary  eyes  are  exceptional 
{Megerlia). 


Andre.  Z.  wiss.  Zool.,  95,  203  (1910). 
Andrews.  J.  MorphoL,  5,  271  (1891). 
Benham.     Camb.  Nat.  Hist.,  London,  2, 

272  (1896). 
Brunette.     C.  R.  Acad.  Sci.  (Paris),  106, 

301  (1888). 
Busch.      Beobacht  i'l  Anat.  u  Entwicklung 

einiger  Wirbellosen  Seethiere  (18.51). 
Calvet.     Trav.  Inst.  Zool.,  Montpellier,  8, 

22  (1900). 
Faust.    Biol.  Bull,  35,  117  (1918). 
Grave.    J.  MorphoL,  49,  3.55  (1930). 
Herter.    Biol.  Tiere  Deutsclilands,  Lfg.  35, 

Teil  12b  (1932). 
Hess,  W.  N.    J.  Morplwl.,  41,  63  (192.5). 
Hesse,  R.     Z.  wiss.  Zool.,  61,  393  (1896)  ; 

62,  527,  671  (1897)  ;    63,  361  (1898)  ; 

65,  446  (1899)  ;    68,  379  (1900)  ;    70, 

347  (1901)  ;    72,  565.  656  (1902). 
Zool.  Anz.,  24,  30  (1901). 
Das    Sehen    der    niederen    Tiere,    Jena 

(1908). 


Hilton.  J.  entom.  Zool.,  13,  49,  55  (1921)  ; 

16,  89  (1924). 
Hj'man.      Ainer.   Mus.   Xovit.,   No.    1005 

(1938). 
The  Invertebrates,  London  2,  (1951). 
Lynch.     Biol.  Bull.,  97,  302  (1949). 
Nitsche.     Z.  wiss.  Zool.,  20,  1  (1870). 
Parker  and  Haswell.     Te.vtbook  of  Zoology, 

1  (1940). 
Peters.     Z.  wiss.  Zool.,  139,  1  (1931). 
Schmidt.     Z.  wiss.  Zool.,  72,  545  (1902). 
Schroder.     Abliandl.  Senckenberg.   Xatur- 

forsch.  Ges.,  35,  153  (1918). 
Schulz.      Zool.   Anz.,    95,    241  ;     96,    159 

(1931). 
Steiner.     Zool.  Jb.,  Abt.  System.  Biol.,  39, 

511  (1916). 
Stossberg.    Z.  wiss.  Zool..  142,  313  (1932). 
Taliaferro.    J.  e.vp.  Zool.,  31,  59  (1920). 
Viaud.    C.  R.  Soc.  Biol.  (Paris),  129,  1174, 

1178  (1938). 
Bidl.  biol.  France  Belg.,  74,  249  (1940)  ; 

77,  224  (1943). 


Brachiopod 


MOLLUSCA 

Among  MOLLUSCS  (''  soft  bodied  ")  the  most  elementary  types  of 
eyes  are  found  and  also  the  most  elaborate  forms  that  the  simple  eye 
assimies,  organs  capable  of  a  degree  of  resolution  that  the  animal 
cannot  probably  utilize  ;  between  the  two  extremes  almost  every 
imaginable  form  of  eye  is  encountered.  The  characteristics  of  this 
phylum  are  an  unsegmented  body  with  a  muscular  "  foot  "  protruding 

1  Lingula,  with  fossil  records  dating  some  500,000,000  years,  is  the  oldest  known 
animal  genus. 


196 


THE   EYE   IN  EVOLUTION 


Solenogastre 


Nudibranch 


Pulmonate, 

Limnoea 


Nautilus 


from  the  ventral  surface  serving  for  locomotion,  a  dorsal  or  lateral 
fold  of  the  body-wall  to  form  a  mantle  or  pallium  within  which  lie  the 
gills,  and  frequently  a  shell.  As  a  general  rule,  two  cephalic  eyes 
subserve  the  visual  function,  but  these  may  be  replaced  by  more 
rudimentary  organs  in  the  dorsal  region  or  around  the  margin  of  the 
mantle  or  at  the  end  of  the  tentacles  or  the  siphons.  Occasionally 
eyes  are  lacking,  in  which  case  the  skin  has  usually  some  sensitivity 
to  light. 

The  large  phylum  of  Molluscs  is  conveniently  divided  into  six  classes  ; 
three  are  relatively  unimportant,  sluggish  in  habit,  and  live  in  the  mud  or  sand 
of  the  sea-bottom — the  shelled  placophorans  and  scaphopods,  and  the  worm- 
like soLENOGASTRES.  The  remaining  three  classes  contain  an  enormous  number 
of  species  of  great  variety — Gastropods,  Lamellibranchs  (Bivalves)  and 
Cephalopods. 

The  GASTROPODS  ("  belly-footed  ")  constitute  a  very  varied  group  comprising 
some  40,000  species  and  include  three  main  classes  : 

(a)  OPiSTHOBRANCHS  :  sea-hares,  Pteropods  (transparent  marine  plankton 
forms),  and  the  brilliantly  coloured  Nudibranchs  or  sea-slugs  which  have  no 
shell  ; 

(h)  PROSOBRANCHS,  an  enormous  and  varied  grouj^  including  sea-snails, 
whelks,  limpets,  Heteropods,  etc.  ; 

(c)  PULMONATES.  The  abundant  and  universally  distributed  fresh-water 
and  terrestrial  snails  and  slugs. 

The  BIVALVES  :  shell -fish  such  as  cockles,  mvxssels,  clams,  scallops  and 
oysters  which  live  within  a  rigid  hinged  shell  often  at  the  bottom  of  the  sea. 
They  comprise  some  11,000  species. 

The  remaining  class,  the  cephalopods,  are  the 
most  interesting  ;  they  are  usually  active,  moving  by 
jet  propulsion  with  a  jet  of  water  expelled  from  the 
siphon.  Two  orders  are  recognized  :  the  Tetra- 
branchiates,  with  two  pairs  of  gills,  represented  by  a 
single  living  species,  the  Pearly  Nautilus  of  the  South 
Pacific,  and  the  Dibranchiates,  with  a  single  pair  of 
gills  and  remarkably  well-developed  eyes  (cuttlefish, 
sqviid,  octojxis). 

In  the  most  primitive  type  of  molluscs,  the 
PLACOPHORANS,  cycs  may  be  lacking  althovigh  some  of 
their  sensory  organs  may  be  sensitive  to  light  (Plate, 
1899;  Nowikoff,  1907).  Some  of  them  possess  a  multi- 
tude of  minute  ocelli  ;  Corephiutn,  for  example,  may 
have  as  many  as  8,500.  The  most  interesting  in  this 
class  are  the  Chitons  ("  coats -of-mail")  ;  these  possess 
cephalic  eyes  in  the  larval  stage  which,  however,  dis- 
appear as  the  advilt  becomes  clothed  by  its  eight- 
plated  dorsal  shell,  thus  rendering  them  useless.  In 
the- ■  place  numerous  innervated  papillis  appear  con- 
tai:  i.ij  sensory  organs  {aesthetes)  which  perforate  the 
shei.  :^)earing  in  rows  as  minute  black  dots  ("  shell- 
eyes  loseley,  1884)  (Fig.  183).    The  larger  of  these 


Fig. 


183. — The  Mollusc, 
Chitox. 

The  sense  organs,  aes- 
thetes, perforate  the  shell, 
appearing  as  minute  black 
dots  ;  the  larger  of  these 
contain  an  ocellus  (Thom- 
son's Zoology,  James 
Ritchie  ;  Oxford  Univer- 
sity Press). 


MOLLUSCA 


197 


are  light  -sensitive,  containing  an  ocellus  composed  of  a  deep  retinal  cup  surrounded 
by  pigment  lying  beneath  a  lens,  the  whole  organ  being  covered  by  a  cornea.  It 
is  to  be  remembered,  however,  that  Crozier  (1920)  could  find  merely  a  general 
photosensitivity  in  Chiton,  most  pronounced  where  ocelli  are  lacking.  Among 
SOLENOGASTKES,  these  organs  are  replaced  by  simple  epithelial  papillte.  In  the 
SCAPHOPODA  ("  tusk-shells  "),  a  small  class  of  molluscs  which  burrow  in  the  sand 
{Dentalium,  elephant's-tooth  shell,  etc.)  the  sensory  organs  are  represented  only 
by  statocysts. 

Most  members  of  the  large  class  of  gastropods,  the  eyes  of  which 
were  studied  at  an  early  date  by  J.  Miiller  (1831),  are  provided  with 
ocelh  of  a  relatively  primitive  kind  often  associated  with  the  tentacles. 
In  the  extremely  passive  limpet,  Patella ,  the  eyes  at  the  base  of  the 
tentacles  are  very  elementary,  being  merely  lepresented  by  simple 


Dentalium 


Fig.  185. — The  Common  Whelk  or  Buckie, 
buccisum  vsdatum. 
Note  the  two  simple  eyes  (e)  at  the  base  of 
the  tentacles,  s,  respiratory  siphon  ;  o,  oper- 
culum ;  /,  foot  (Thomson's  Zoology,  James 
Ritchie  ;    Oxford  University  Press). 


Fig.      184. — The       Limpet, 
Patella  vulgata 

Ventral  surface.  Note  the 
simple  eyes  (appearing  as 
black  dots)  at  the  base  of  tlie 
2  tentacles.  The  star-shaped 
median  structure  is  the 
mouth  (Thomson's  Zoology, 
James  Ritchie  ;  Oxford  Uni- 
versity Press). 


cupiilate  depressions  of  sensory  and  pigmented  cells  (Figs.  97  and  184). 
More  usually,  however,  the  eyes  are  vesicular  in  type.  These  are  typified 
in  the  two  simple  vesicular  eyes  of  the  grey  slug,  Limax,  or  the  snail, 
Helix  (Fig.  110),  perched  on  the  tips  of  the  two  longer  (and  jjosterior) 
tentacles  ("  horns  '")  and  innervated  from  the  cerebral  ganglion 
(Galati-Mosella,  1915)  ;  on  exjDosure  to  light  the  tentacle  is  capable  of 
retraction  like  the  finger  of  a  glove  so  that  the  eye  can  be  drawn  within 
it  (Figs.  186  to  188).  The  common  whelk,  Bticcinum,  has  eyes  of  a 
somewhat  similar  vesicular  type  situated  near  the  base  of  the  tentacles 
(Fig.  185),  as  also  has  Murex. 

The  most  elaborate  eye  of  this  type,  however,  is  seen  in  the  spider-shell, 
Pterocera  lambis,  a  gastropod  found  in  quantity  on  tropical  reefs.    According  to 


Shell  of  Murex 


198 


THE   EYE   IN  EVOLUTION 


Figs.   186  to  188. — The  Common  Garden  Snail,  Helix  aspebsa. 


Fig.  186. — The  two  eyes  arc  situated  on  the  tijD  of  each  of  the  long  posterior 

horns. 


Fig. 


187 — The  eye  at  the  tip  of  the  ex- 
panded horn. 


Shell  of  Pterocera 


Fig.  188.— The  eye  (E)  retracted  into 
the  horn.  The  horn  invaginates  like 
the  inturned  finger  of  a  glove  ;  the 
obliquity  of  this  section  gives  the 
appearance  of  a  double  cavity 
(Norman  Ashton). 


Prince  (1955),  the  two  vesicular  eyes,  which  have  an  elaborate  neural  structure, ^ 
are  mounted  on  the  tip  of  stalks  (ommatophores)  which  also  carry  an  olfactory 
tentacle  and  a  sensory  node  (Fig.  189).  These,  supplied  with  muscles  arranged 
round  a  central  sinus,  are  retractile  partly  by  muscular  activity  and  partly  by 
fluid  engorgement  by  heemolymph.  Retraction  can  be  slow  and  voluntary  or 
r;i!)id  and  reflex  in  response  to  stimuli  such  as  touch,  odour  or  the  cutting  off  of 
I':--"'  i  :  the  reaction  is  thus  the  opposite  of  that  seen  in  the  snail.  It  appears 
als     -hat  a  certain  amount  of  convergence  upon  an  object  is  possible. 

1  p.  142. 


MOLLUSCA 


199 


In  Onchidium,  a  naked  littoral  Pulmonate  which  creeps  on  rocks  near  the 
high-water  mark,  a  unique  type  of  vesicular  eye  with  an  inverted  retina  is  found 
arranged  on  papillae  scattered  over  the  skin  of  the  back  in  groups  of  six  or  up 
to  a  total  which  inay  reach  a  hundred  (Fig.  122).^ 

An  interesting  elaboration  is  seen  in  some  marine  heteropods  {Carinaria, 


tCMBORY  NOOC 


NAOIAL    MU«CL£ 


Carinaria 


RITIOULO-CHOOTHELIAL    SYCTIM. 


Fig.    189. — The  Stalked  Eye  of  the  Spider-shell,  Pterocera   lambis. 

Showing  the  sensory  tentacle,  sensory  node,  sinus,  and  muscular  systems 
(after  J.  H.  Prince). 


Pterotrachea)  which  ha\e  tubular  eyes  containing  a  large  spherical  lens;  the 
available  visual  field  is  increased  by  the  provision  of  lateral  "  windows  "  wherein 
pigment  is  lacking,  opposite  which  the  posterior  retina  is  prolonged  up  the  side 
of  the  eye.  Pterotracliea  coronata  which  swims  with  its  belly  in  the  air  has  an 
eye  at  the  extremity  of  each  of  its  two  tentacles  ;  images  in  front  are  focused 
on  the  posterior  retina  by  the  enormovis  lens,  while  movements  and  changes  in 

1  p.  148. 


200 


THE   EYE   IN   EVOLUTION 


Avicula 


Mi/tilus 


Pholas 


Cardium 


illumination  above  and  below  are  probably  appreciated  through  the  dorsal  and 
ventral  "  windows  "  (Hesse,  1908  ;  v.  Hess  and  Gerwerzhagen,  1914).  Such 
fenestrated  eyes  are  also  seen  in  abyssal  fishes.^ 

LAMELLiBRANCHS  or  BIVALVES  have  ail  Undeveloped  head-region, 
and  the  two  lobes  of  the  mantle  which  secrete  the  two  valves  of  the 
shell  are  frequently  united  posteriorly  to  form  exhalant  and  inhalant 
siphons.  Anterior  eyes  are  therefore  rare.  Such  cephalic  eyes  are 
sometimes  seen  in  larval  forms  but  in  the  adult  they  tend  to  become 
vestigial   remnants,    a    cupulate    depression   of  bipolar   sensory   and 


>..7.J-.i_ 


X--^'y^^^ 


Fig.  190. — The  Common  Scallop,  Pectes. 

The  pallial  ocelli,  Oc,  are  seen  in  a  single  row  i-ound  the  margin  of  the 
mantle.    For  section  of  the  eye,  see  Fig.  123  (after  Pelseneer). 

pigmented  cells  as  occurs  in  the  j^earl-oyster,  Avicula,  or  the  edible 
mussel,  Mytilus.  More  usually  they  are  replaced  by  ocelli  located  in 
situations  where  they  are  of  greater  biological  value  such  as  the 
siphons,  the  tentacles  or  the  mantle  (Fig.  190). 

Thus  the  ocelli  are  found  on  the  inner  surface  of  the  siphons  in  clams  which 
habitually  lie  buried  in  the  sand  or  mud  (Mya)  or  bore  into  soft  rocks  (Pholas) 
(Light,  1930)  ;  as  they  lie  buried  these  molluscs  extend  the  siphon  to  the  surface 
to  feed  and  at  daybreak  or  whenever  the  illumination  increases  the  siphon  is 
withdrawn  (Wenrich,  1916  ;  Hecht,  1919-20  ;  Pieron,  1925  ;  Folger,  1927  ; 
and  others).  It  will  be  remembered  that  these  visual  organs  are  of  the  most 
simple  type  resembling  those  of  the  earthworm,  being  merely  single  cells  of  the 
apolar  type  with  a  refractive  organelle  in  the  cell-body  richly  supplied  with 
nerves.-  In  the  cockle,  Cardium,,  small  ocelli  are  situated  at  the  tips  of  the 
tentacles,  about  100  in  number,  which  are  arranged  around  the  siphonal 
apertvires  ;  the  eye  is  of  a  simple  cupulate  form,  the  cuj^-shaped  retinal  cells 
resting  on  a  layer  of  double  pigmented  cells  underneath  a  large  ectodermal 
cell^iJar  lens  and  cornea  (Kishinouye,  1894).  As  in  the  pallial  eyes  of  Pecten, 
the  !ct ina  is  inverted. 


Pecten 


1  p.  323. 


p.  131. 


MOLLUSCA 


201 


Most  bivalves,  however,  have  numerovis  oceUi  arranged  Hke  a  coronet 
around  the  margin  of  the  mantle  (pallial  eyes)  ;  these  may  be  numbered  in 
hundreds  and  are  probably  to  be  looked  upon  as  modified  tentacles.  In  some 
foi-ms,  such  as  Lima,  they  are  very  primitive.  This  bivalve  is  provided  with 
30  simple  cup-shaped  depressions,  0-3  mm.  in  diameter,  lined  with  sensory  and 
pigmented  cells  forming  primitive  cu2:)ulate  eyes  ;  in  others  such  as  the  fresh- 
water mussel,  Anodonta,  eyes  are  completely  absent.  Most  of  these  types  are 
relatively  shiggish  and  quiescent,  but  in  actively  swimming  forms  the  eyes  may 
be  more  elaborate.  This  development  is  well  exemplified  in  svich  bivalves  as 
the  comnion  scallop,  Pecten,  and  Spondylus,  both  of  which  possess  eyes 
unique  among  IMolluscs.  The  pallial  eyes  are  arranged  in  a  single  row  around  the 
edge  of  the  mantle  ;  when  they  are  exposed  as  the 
shell  gapes  they  shine  as  brilliant  emerald  green  or 
purple  spots,  0-6  to  0-8  mm.  in  diameter  ;  28  to  46 
have  been  counted  in  the  upper  half  of  the  mantle, 
15  to  36  in  the  lower,  and  each  is  borne  on  a  con- 
tractile pedicle  (Fig.  190).  These  are  of  remarkable 
complexity  with  a  well-formed  inverted  retina 
which  appears  to  be  much  more  elaborate  than  the 
visual  demands  of  the  shell-fish  would  seem  to 
warrant  (Fig.  123).  Each  is  comiected  by  means  of 
its  optic  nerve  with  a  large  circumpallial  nerve  and 
so  with  the  branchial  ganglion.^  An  anomalous 
occurrence  in  certain  lamellibranch  molluscs  (the 
Noah's-ark  shell.  Area  ;  Pectunculus),  is  that  of 
unicellular  ocelli  grouped  together  in  a  spherical 
mass  constituting  an  aggiegate  eye  which 
bears  a  superficial  resemblance  to  a  compound  eye  - 
(Carriere,  1885  ;    Patten,  1886  :  Hesse,  1900). 


Pearly 

Nautilus 


Fig.    191.  —  The 
Nautilus, 
pompilius. 

The  animal  is  seen  in 
section.  Above  is  the  spiral 
shell.  E,  the  eye,  which 
opens  to  the  exterior  ;  Si, 
siphon  ;  T,  tentacles  (after 
Owen). 


The  CEPHALOPODS  (cuttlefish,  etc.) 
usually  exhibit  the  most  elaborate  visual 
organs  found  among  Molluscs,  a  characteristic 
understandable  in  view  of  their  active  be- 
haviour and  carnivorous  habits  ;  only  one  species  living  at  abyssal 
ocean  depths  is  knoAMi  to  lack  eyes,  Cirrofhauma  murrayi?  They  are 
the  most  specialized  of  the  molluscs  and  i:)resent  considerable  diversities 
of  type,  but  most  of  them  are  freely  SAvimming  and  they  all  have  a 
\vell-develoj)ed  head  furnished  with  numerous  "arms"  bearing  tentacles 
or  suckers  and  provided  with  eyes  and  other  sensory  structures. 

In  the  pearly  nautilus  of  the  seas  of  the  Far  East,  the  sole  survivor  of  the 
primitive  and  almost  extinct  tetrabranchiate  Cephaloi^ods  which  were  largely 
Palaeozoic  in  distribution,  the  eye  retains  its  ancestral  simplicity  and  consists 
merely  of  an  epithelial  depression  with  a  tiny  aperture  2  mm.  in  diameter 
(Figs.  100  and  191)  ;  it  is  situated  on  a  raised  flat  peduncle  which  is  also  provided 
witli  two  "  ocular  tentacles  "',  probably  olfactory  in  function. 

In  the  more  recent  and  voraciously  carnivorous  dibranchiate 
Cephalopods,    however,   such   as   the   common   cuttlefish,   Sepia,   the 


Ayiodonta 


Spondylus 


Sepia 


p.  1.51. 


J23. 


202 


THE   EYE   IN   EVOLUTION 


squid,  Loligo,  and  the  octopus,  the  two  eyes  are  large  and  prominent 
(Figs.  192-3).  They  are  situated  conspicuously  on  either  side  of  the 
head  behind  the  main  body  of  tentacles,  protected  in  part  by  the 
cartilage  surrounding  the  brain  and  in  part  by  cartilages  in  their  own 


Fig.   192. — Octopus   vulgaris  (J.  Z.  Young). 


walls,  and  provided  with  rudimentary  lids  and  a  set  of  4  extra-ocular 
muscles  which  confer  a  wide  range  of  movement  on  the  globe  (Hesse, 
1908  ;  Tompsett,  1939)  (Figs.  113  and  114).  The  complex  structure  of 
these  organs  has  already  been  described, ^  and  although  they  rival  the 
eyes  of  Vertebrates  in  their  morphology,  they 
are  simple  in  type,  derived  from  the  epithelium. 
The  close  resemblance  of  the  eyes  of  these 
molluscs  to  the  cerebral  "  camera  "  eyes  of 
Vertebrates  is  a  striking  examjDle  of  convergent 
evolution  whereby  Nature  achieves  comparable 
results  by  travelling  along  entirely  different 
routes.  The  nervous  connections  are  promi- 
nent ;  in  the  posterior  wall  of  each  eye  is  a 
large  optic  ganglion  from  which  the  thick  optic 
lobes  lead  directly  to  the  closely  associated 
cerebral  ganglion  ^  (Fig.  698).  There  is  a  well- 
developed  olfactory  sac  behind  each  eye  as  well 
as  two  statocysts  and  organs  of  general  sensa- 
tion, but  it  would  seem  that  vision  plays  a 
dominant  part  in  the  behaviour  of  the  animal.^ 


The   Common 
Loligo       vul- 


the  two  large 
f^yes,    one    on 
the    head 
in). 


143. 


575. 


2  p.  5: 


MOLLUSCA 


203 


Anomalous  types  of  eyes  are  seen  among  Cephalopods  found  at  great  ocean 
depths  (Chun,  1903).  Stalked  eyes  comparable  to  those  found  in  some  deep-sea 
fishes,  are  exemplified  in  Bathothauma  (Fig.  194)  and  Srindalops  (Fig.  195)  ;  both 
of  these  live  at  great  depths  in  the  South  Atlantic  and  the  eyes  of  the  latter  are 
unic£ue  in  that  they  point  obliquely  downwards,  a  curious  configvu'ation  said  to  be 
explained  by  the  fact  that  the   squid  swims  with   its  body  slanting  upwards. 

Figs.   19-1  to   196. — The  Eyes  of  Dkep-sea  Cephalopods. 


Fig.    19.5. 


Fig.   194. 


Fig.   196. 


Fig.  194. — The  deep-sea  squid,  Bathothauma.  There  are  luminous  organs 
beside  the  eyes  which  are  perched  on  the  end  of  stalks.  Found  at  a  depth 
of  3,000  m.  (from  the  Valdtvia  Reports). 

Fig.  19.5. — The  deep-sea  squid,  Sandalops  melancholicus.  The  stalked  eyes 
are  unique  in  that  they  point  obliquely  downwards,  possibly  because  the 
animal  swims  with   its  body  slanting  upward   (from  the    Vahlivia^  Reports). 

Fig.  196. — The  pelagic  octopus,  Amphitretus.  The  tubular  eyes  point 
upwards  and  the  whole  body,  including  the  eyes,  is  covered  with  a  delicate 
gelatinous  covering  (from  the  Valdivia  Reports). 

Another  curious  arrangement  is  seen  in  Amphitretus  (Fig.  196)  found  in  the  Indian 
and  Pacific  oceans.  The  eyes  of  this  octopod  resemble  the  tubular  organs  of 
some  deep-sea  fishes, i  pointing  directly  upM^ards  and  enclosed,  as  is  the  entire 
body  of  the  animal,  in  a  delicate  and  transparent  gelatinous  covering. 


Boulet.    C.  B.  Soc.  Biol.  (Paris),  148,  I486 

(1954). 
Carriere.     Die  Sehorgane  der  Ticre,  Miin- 

chen(1885). 
Arch,  niikr.  Anat.,  33,  378  (1889). 
Chun.       Verhdl.   dtsrh.    Zool.   Oes.,   13,    67 

(1903). 
Crozier.    J.  gen.  Physiol..  2,  627  (1920). 
Folger.     Anat.  Rec,  34,  1  b5  (1927). 
Galati-Mosella.     Motiit.  Zool.  ital.,  26,  75 

(1915). 
Hecht.      J.    gen.    Phi/xioL,    1,    545,    657 

(1919)  ;    2,  337  (1920). 
v.  Hess  and  Gerwerzliagen.     ^4rc/(.   vergl. 

Ophthal.,^,  300  (1914). 
He.sse,  R.     Z.  ^ris.<.■.  Zool..  68,  379  (1900)  ; 

70,  347  (1901)  ;    72,  565,  656  (1902). 
Das    Sehen     der    niederen     Tiere,    Jena 

(1908). 

'  p. 


Kishinouye.      J.    Coll.    Scl.    Imp.     Univ. 

Japan.  4,  55  (1891)  ;    6,  279  (1894). 
Light.    J.  Morphol.  Phi/siol..  49,  1  (1930). 
Moseley.     Ann.  Mag.  not.  Hist.,  14,   141 

(1884). 
Mtiller,  J.    Ann.  Sci.  nat.,  22,  5  (1831). 
Nowikoff.     Z.  wiss.  Zool.,  88,  153  (1907). 
Patten.     Mitt.  zool.  Stat.  Neapel,  6,  546, 

568,  605  (1886). 
Pieron.    C.  R.  Soc.  Biol.  (Paris),  93,  1235 

(1925). 
Plate.     Zool.  Jb.,  Suppl.  4,  1  (1899). 
Prince.      Te.ras   J.    Biol.    Med.,    13,    323 

(1955). 
Tompsett.    Liverpool    marine    biol.  Comm. 

Mem.,  32,  1  (1939). 
Wenrich.     J.  anim.  Behav.,  6,  297  (1916). 
Willem.     Arch.  Biol..  Gand.  12,  57  (1892). 
322. 


204 


THE   EYE   IN   EVOLUTION 


ARTHROPODA 

ARTHROPODS  embrace  more  than  three-quarters  of  the  known 
species  of  animals,  and  in  view  of  their  number  and  variety  and  the 
diversity  of  their  habits,  it  is  not  surprising  that  an  extraordinary 
variation  occurs  in  their  visual  organs,  while  the  intense  and  purposive 
activity  of  many  of  them  accounts  for  the  complexity  and  efficiency  of 
their  eyes.  Arthropods  are  characterized  by  their  bilateral  symmetry, 
their  cegmental  structure  with  jointed  appendages,  their  chitinous 
cuticle,  a  distinct  head  where  the  sense  organs  are  aggregated,  and  a 
nervous  system  consisting  of  a  dorsal  brain-ganglion  connected  by  a 
ring  round  the  gullet  with  a  double  chain  of  ventral  ganglia.  From 
the  ocular  point  of  view,  although  simple  eyes  often  of  quite  a  rudi- 
mentary type  are  frequent,  and  may  indeed  be  the  sole  visual  organs 
(as  in  Arachnids),  the  characteristic  feature  of  the  phylum  is  the 
presence  of  compound  eyes  of  elaborate  structure  and  frequently  with 
highly  developed  functional  abilities. 

The  Arthropods  may  conveniently  be  divided  into  five  sub-phyla  : 

(1)  the  primitive  worm-like  onychophora,  unique  in  having  a  soft,  velvety 

skin,  and  provided  with  a  separate  head,  one  pair  of  antennae 

and  20  legs  all  alike  ; 

(2)  the  CRUSTACEANS,  comprising  some  25,000  species, 
with  the  head  fused  with  the  thorax,  2  pairs  of  antennae  and 
at  least  5  dissimilar  pairs  of  legs  ; 

(3)  the  MYRiAPODS  (centipedes,  millipedes,  etc.),  of  some 
2,000  species,  with  a  distinct  head,  one  pair  of  antennae  and 
numerous  legs  all  alike  ; 

(4)  the  ARACHNIDS,  of  some  36,000  species,  having  2 
body -segments  with  a  fused  cephalothorax,  without  antennae 
or  wings,  and  4  pairs  of  legs  ; 

(5)  the  INSECTS,  of  which  more  than  577,000  species 
have  now  been  scientifically  described  and  probably  several 
times  as  many  await  investigation,  with  a  body  divided 
sharply  into  3  segments,  head,  thorax  and  abdomen,  bear- 
ing one  pair  of  antennae,  3  pairs  of  legs  and  (usually)  one  or 
two  pairs  of  wings  in  the  adult. ^ 


Fig.  197.  —  The 
Onychophore, 
Peripatus. 

Note  the  two 
simple  eyes  on  top 
of  the  head  at  the 
base  of  the  anten- 
nae (Thomson's 
Zoologij,  James 
Ritchie  ;  Oxford 
Univer.^ity  Press). 


ONYCHOPHORA 

The  most  primitive  class  of  Arthropods,  the 
ONYCHOPHORA  {Peripatus  and  its  allies),  inhabiting 
the  forests  of  the  Southern  Hemisphere,  represent  an 
archaic  type,  differing  widely  from  other  members  of 
the  phylum.    Seeking  out  damj)  places  under  leaves 


^  In  oue  acre  of  farm-land  in  England  it  has  been  estimated  that  there  are  from 
700,000,or^:;  to  800,000,000  Insects  and  as  many  Arachnids.  They  would  usurp 
Man's  do.  .11  it  ion  of  the  earth  were  their  numbers  not  kept  in  check  by  voracious 
predators        ^  parasites  of  their  own  kind. 


ARTHROPODA 


205 


and  in  rotting  wood,  they  are  shy  and  nocturnal  in  habit  with  a  marked 
dishke  of  hght.  They  are  beautiful,  velvety,  caterpillar-like  creatures 
with  paired  eyes  set  like  diamonds  (0-  2  to  0-  3  mm. )  on  the  side  of  the  head 
behind  the  two  sensitive  antenna?,  looking  upwards  and  outwards,  not 
forwards  (Fig.  197)  ;    the  eyes,  like  those  of  marine  Polychsetes,  are  of 


Figs. 


198  TO   200. — The   Eyes   of   the   Large   Crustaceans   (Decapods) 
(Specimens  from  Natural  History  Museum,  London). 


Fig.   199. 


Fig.   198. 


Fig.  200. 


Fig.  198. — The  common  shrimp,  Crangon  vulgaris.  The  short  eye-stalks 
bearing  the  compound  eyes  lie  in  sockets  in  the  carapace. 

Fig.  199. — The  fiddler  crab,  Gelasimus  arcuatus.  There  are  two  com- 
pound eyes,  C,  each  standing  out  prominently  on  a  muscular  eye-stalk  and 
protruding  on  either  side  of  the  median  rostrum.  The  left  claw  is  repi-esented 
by  a  small  stump  ;    the  huge  right  claw  gives  the  animal  its  name. 

Fig.  200. — The  racing  crab,  Ocyilpoda  ippens.  Two  j^rominent  elongated 
compound  ejes,  C,  are  set  on  eye-stalks,  in  sockets  on  the  carapace. 


206 


THE   EYE   IN  EVOLUTION 


the  simple  type,  cupulate  in  form  with  a  corneal  lens  formed  by  the 
cuticle  and  hypodermal  cells  (Fig.  103).  Eyes  so  simple  as  this  serve 
merely  as  a  means  of  orientation  away  from  light,  and  two  cave- 
dwelling  species  are  blind  ^  (Dakin,  1921). 

CRUSTACEA 

The  CRUSTACEANS  (lobsters,  crabs,  shrimps,  water-fleas,  barnacles, 
etc.)  with  few  exceptions  (land-crabs,  wood-lice,  sand-hoppers)  are 
aquatic  in  habit  and  in  most  the  eyes  are  prominent  ;  some  pelagic 
forms  are  transparent  except  for  the  eyes  which  are  highly  coloured  or 
phosphorescent.  Compound  eyes  are  usually  present,  occasionally 
supplemented  by  eyes  of  the  simple  type,  but  in  sessile  or  parasitic 
forms  the  visual  organs  may  be  vestigial  or  lacking.     Most  forms 


Q 


Fig.   201. — The  Woodlouse,  Sph.sroma  lanceolata. 

The  compound  eyes,  C,  are  sessile,  lying  on  the  extreme  lateral  aspects 
of  the   head   segment    (specimen   from   Natural   History  Museum,  London). 


Homams 


Phronima 


commence  life  as  a  nauplius  larva  with  an  oval  body,  three  pairs  of 
limbs  and  a  single  eye  in  the  middle  of  the  head. 

Of  the  larger  forms  (the  sub-class  malacostraca)  the  Decapods 
(lobsters,  shrimps,  prawns,  crabs)  have  the  most  elaborate  eyes  ;  of 
these  the  common  lobster,  Homarus  vulgaris,  may  be  taken  as  repre- 
sentative. It  possesses  two  typical  compound  eyes,  each  with  a  multi- 
tude of  ommatidia,  associated  with  the  procephalic  lobes  of  the  cerebral 
ganglion.  They  stand  out  prominently  on  muscular  eye-stalks  to 
protrude  on  either  side  of  the  median  rostrum  and  are  capable  of  some 
degree  of  movement  (Fig.  198).  In  crabs  a  similar  pair  of  compound 
eyes  with  relatively  few  but  large  ommatidia  are  set  on  eye-stalks  in 
sockets  in  the  carapace  (Figs.  199-200).  The  fact  that  the  eye-stalks 
L. ^Hi  in  the  crab  and  in  the  crayfish  exhibit  optomotor  reactions  as  when 
tJir-  animal  turns  or  is  confronted  by  a  black  and  white  striped  rotating 
dr^   ',    indicates    that    their    movements    are    optically    determined 

1  p.  724. 


ARTHROPODA 


207 


(v.  Buddenbrock  ei  ah.  1954  ;  Dijkgraaf,  1956).  One  group,  the 
Eryonidea,  confined  to  the  deep  seas,  are  blind,  the  eyes  being  reduced 
to  stalks  only.  In  other  species  the  eyes  are  sessile,  both  in  terrestrial 
Isopods  (such  as  woodlice,  Fig.  201)  and  in  pelagic  Amphipods  : 
among  the  latter  in  the  smaller  forms  the  eyes  may  be  minute 
{CapreUa,  Fig.  202),  while  in  the  larger  forms  they  may  assume 
enormous  dimensions  (the  "  wondrous-eyed  hopper,"  Thaumatojis 
magna.  Fig.  203).  Sedentary  types  such  as  Asellus,  an  Isopod  which 
lives  in  holes,  are  completely  blind. 


Fig.   202. — The   Amphipod,   Caprella 

LjyEJItl.s. 

Two   ocelli   are   seen   on   the   dorsal 
surface  of  the  head. 


Fig.  203. — The  "  Wondrous-eyed 
Hopper,"  Thaumatops  magxa. 
The  largest  known  hyperiid  Crusta- 
cean, found  at  a  depth  of  2,500  in., 
with  enormous  compound  eyes  (to 
the  right)  (f  natural  size)  (after 
Brehm). 


Euphausiid 
Crustacean 


Asellus 


The  smaller  Crustaceans  (branchiopods,  cojDepods,  ostracods, 
cirripedes)  include  a  vast  number  of  types  in  which  the  active  swimming 
forms  are  provided  with  eyes,  while  in  most  sessile  and  j)arasitic  forms 
the  organs  become  degenerate.  They  comprise  four  diverse  and  little 
related  orders  : 

(a)  BKANCHiOPODS — protected  by  a  shell  and  provided  with  4  pairs  of  leaf- 
like swimming  feet.  They  comprise  tw'O  groups  :  (1)  the  phvllopoda  such  as 
the  brine-shrimp,  Artemia,  which  can  survive  even  in  Salt  Lake,  and  the  large 
fresh-water  Apus,  of  world-wide  distribution,  and  (2)  the  laterally  compressed 
minute  water-fleas  (cladocera),  Daphnia,  Polyphemus  and  Leptodora,  so  abund- 
ant in  fresh  water. 

(6)  OSTRACODS — small  laterally  compressed  creatures  with  a  bivalve  shell 
and  indistinct  segmentation,  breeding  parthenogenetically.  Typical  examples 
are  the  fresh-water  Cypris  and  the  salt-water  Cypridina. 

(c)  COPEPODS — elongated  segmented  creatures  without  a  protective  shell. 
Typical  examples  are  the  beautiful  fresh-water  Cyclops  and  the  salt-water 
Calanus.     Copepods  occur  in  vast  numbers  in  the  seas  and  constitute  the  most 


Artemia 


Leptodora 


Calanus 


208 


THE   EYE   IN   EVOLUTION 


Nauplius  larva 


abundant  animal  constituent  of  the  plankton.     The  group  also  contains  some 
parasites,  as  the  common  fish-louse,  Caligus. 

{d)  ciKRiPEDE.i — with  an  indistinctly  segmented  body  and  usually  provided 
with  a  calcareous  shell.  They  have  a  complex  life-history.  They  are  born  as 
actively  swimming  nauplius  larvae,  develop  into  a  pupal  cypris-like  stage,  again 
swimming  freely  with  appendages,  but  in  the  adult  condition  lead  an  entirely 
sessile  or  parasitic  life.  Typical  examples  are  the  barnacle,  Lepas,  which  attaches 
itself  to  the  bottoms  of  ships  or  floating  logs,  the  acorn-shell,  Balanus,  which 

Figs.  204  to  206. — The  Eyes  of  Small  Crustaceans 
(Specimens  from  Natural  History  Museum,  London). 


c 


X^^ 


i^ 


Fig.   204. 

Fig.  204. — The  dorsal  surface  of  a  Branchiopod,  Triops  [Apus)  cancri- 
formis.  In  the  anterior  region  are  two  compound  eyes,  C,  and  behind  them  a 
median  eye  of  the  composite  simple  type,  S. 

Fig.  205. — An  Ostracod,  Cypria  ophthalmica.  The  single  deeply  jjigmented 
eye,  E,  is  seen  shining  through  the  semi-transparent  shell. 

Fig.  206. — The  water-flea,  Daphnia.  Prominently  in  the  head  region 
(at  the  junction  of  the  arrows)  is  the  compound  eye,  ajDijearing  as  a  mass 
of  pigment  with  little  facets  romid  it.  Behind  and  underneath  lies  the  minute 
composite  median  ej^e  (see  also  Fig.  145).  j 


encrusts  the  rocks  between  tidal  marks  in  enormous  numbers,  and  Sacculina, 
■.■!ie  of  the  most  degenerate  of  parasites  which  becomes  an  endoparasite  in  the 
i.-'    •' anen  of  crabs. 


of 


rhe  characteristic  ociilar  feature  of  the  whole  group  is  the  presence 
uedian  unpaired  eye  ;    it  is  sometimes  unique,  as  in  Cyclops^ 


ARTHROPODA 


209 


sometimes  associated  with  a  single  compound  eye,  as  in  Daphnia, 
sometimes  with  paired  lateral  eyes  which  may  be  either  simple,  as  in 
PonteUopsis,  or  comp>ound  in  type,  as  in  the  Phyllopod,  Apus  (Fig.  204). 
In  Apus  the  median  eye  is  really  a  paired  organ  but  the  two  are  so 
closely  situated  that  they  appear  on  examination  to  be  a  single  spot. 
The  median  e^-e  of  these  small  Crustaceans  is  situated  either  dorsal 
or  ventral  to  the  cervical  ganglion  and  is  of  the  composite  simple 
type  ^  ;  it  is  comjDosed  of  the  fusion  of  a  number  of  constituent 
ocelli  (usually  3).  Such  a  median  eye  is  present  in  most  of  the 
Branchiopods  and  Ostracods,  only  occasionally  degenerating  when 
the  compound  eyes  are  particularly  well  developed  {Polyphemus, 
Leptodora). 

The  ocular  arrangements  in  these  actively  swimming  small  Crustaceans  is 
therefore  very  varied.  The  eyes  of  the  water-flea,  Daphnia,  may  be  taken  as 
representative  of  the  Branchiopods  and  Ostracods.  There  is  a  single  compound 
eye  in  the  mid-line  composed  of  22  relatively  rudimentary  ommatidia  (Fig.  206). 
Behind  and  below  this,  buried  in  the  central  nervous  system,  is  the  small 
composite  ocellus  (Figs.  131  and  145).  It  is  interesting  that  the  compound 
eye  is  actively  motile,  being  kept  in  a  state  of  continual  vibration  by  4  muscles 
somewhat  resembling  in  their  arrangement  the  rectus  muscles  of  vertebrates 
(Rabl,  1901  ;  Hess,  1912).  It  would  seem  that  the  small  composite  ocellus  is 
of  little  functional  value.  The  phototactic  responses  exhibited  by  the  animal 
depend  entirely  upon  the  more  elaborate  compound  eye  ;  when  this  has  been 
removed  the  phototactic  responses  fail  although  the  more  primitive  generalized 
sensitivity  to  light  persists  (Schulz,  1928  ;    Harris  and  ^lason,  1956). 

The  eyes  of  some  of  the  actively  swimming  Copepods  take  on  another  form. 
In  the  female  PonteUopsis  regalis,  there  are  two  very  small  dorsal  ocelli  sym- 
metrically placed  and  a  large  unpaired  median  eye  situated  fronto -vent  rally 
underneath  the  rostrum  ;  it  has  a  large  cuticular  lens  and  6  retinal  cells  arranged 
in  an  inverted  position  in  two  groups  of  3,  forming  an  intermediate  step  between 
a  simple  eye  and  an  ommatidiura  (Vaissiere,  1954-55).  The  elongated,  actively 
motile  eyes  of  Copilia  are  of  the  same  general  structure  with  a  retinule  of  3 
sensory  cells  (Fig.  139)  (Grenacher,  1880-95  ;  Exner,  1891).  This  animal  has  two 
such  eyes  facing  forwards  and  widely  separated  ;  in  Sapphirina  they  are 
close  together  ;  and  in  Corycceus  so  close  that  the  lenses  ai-e  fused  in  the 
mid-line. 


Polyphemus 


Copilia 


Balanus 


In  sessile  forms  eyes  are  usually  present  in  the  actively  swimming 
nauplius  stage  ;  thus  in  the  acorn-shell,  Balanus.  there  is  initially  a 
median  unpaired  eye  but  after  several  moults  in  the  pupal  stage  two 
lateral  composite  eyes  are  acquired.  In  adult  life,  however,  these 
become  vestigial,  as  also  does  the  unpaired  eye  of  the  ship-barnacle, 
Lepas  (Fales,  1928).  In  some  parasitic  forms  such  as  the  fish-louse, 
Caligus,  both  median  (sim^^le)  and  lateral  (composite)  eyes  are  also 
present,  but  in  degenerate  types  such  as  SaccuJina  eyes  and  other 
sense  organs  are  lost. 


1  p.  152. 


Lepas 


S.O.  —VOL.  I. 


210 


THE   EYE   IN  EVOLUTION 


MYRIAPODA 

The  MYEiAPODS  (the  quick-moving,  carnivorous  solitary  centipedes 
or  Chilopoda^  some  with  more,  some  with  less  than  100  legs,  and  the 
slow-moving  vegetarian,  gregarious  millipedes  or  Diplopoda)  are 
characterized  by  the  possession  of  two  groups  of  ocelli  forming  aggregate 
eyes  on  either  side  of  the  head  so  closely  packed  together  as  to  suggest  a 
compound  eye  (Figs.  207  to  210);  so  close  are  they  in  the  Chilopod, 
Scutigera,  that  they  form  a  pair  of  true  compound  eyes  (Grenacher, 

Figs.  207  to  210. — The  Aggreg.a.te  Eyes  or  Myriapods 
(Specimens  from  Natural  History  Museum,  London). 


Fig.   208. 


Fig.   209. 


Fig.  210. 


Figs.  207  and  209. — The  centipede,  ScoJopendra  morsitans  from  India. 
The  jToup  of  4  ocelli,  E,  are  situated  on  either  side  of  the  head. 

■  ':s.  208  AND  210. — A  iSpirostreptid  millipede  from  the  Seychelles. 
Thi  .iip  of  ocelli  forming  an  aggregate  eye,  E,  is  seen  on  either  side  above 
the  a     ,  iinae.     Fig.  210  shows  the  close  resemblance  to  a  true  compound  eye. 


ARTHROPODA 


211 


1880;  Graber,  1880  ;  Caesar,  1913  ;  Const  ant  ineanu,  1930).  In  some 
types,  such  as  Pauropus,  which  live  in  moist  debris  in  the  woods  and 
forests,  eyes  are  lacking. 


ARACHNIDA 


The  ARACHNIDS  form  a  large  and  loosely  associated  group  which 
includes  scorpions,  king-crabs,  spiders,  pseudo-scorpions,  whip-tailed 
scorpions,  harvest-men,  jerrymanders,  mites  and  ticks.  With  the 
single  exception  of  the  king-crab  they  do  not  possess  conii^ound  eyes 


Fig.   211. — The  Kikg-crab,   Limvlus  polypbeml's. 
A  .simple  ej'e,  S,  is  seen  as  a  dark  spot  situated  on  either  side  of  the  median 
spine.     The  two  compound  eyes,  C,  are  situated  on  the  external  aspect  of 
each   of  the   first   lateral  spines   (specimen  from   Natural   Historj^  Museum, 
London). 

but  all  are  provided  with  ocelli  sometimes  of  considerable  size  and 
complexity. 

SCORPIONS  (scorpionidea),  venomous  animals  up  to  8  in.  in  length 
with  a  long  stinging  tail,  are  restricted  to  warm  countries  ;  in  habit 
they  are  essentially  solitary  and  nocturnal,  being  active  during  the 
night  and  spending  the  day  lurkmg  under  stones  or  in  crevices.  They 
are  provided  with  a  pair  of  large  median  eyes  situated  about  the  middle 
of  the  cephalothorax,  and  2  to  6  pairs  of  lateral  ocelli  placed  on  its 
antero-lateral  margins,  the  more  anterior  being  simpler  in  structure 
than  the  posterior.^     The  lateral  eyes  are  simple  ocelli  in  which  the 

1  p.  141. 


Scorpion 


212  THE   EYE   IN  EVOLUTION 

borders  of  the  visual  cells  unite  with  their  neighbours  to  form  rhabdomes 
(Fig.  109)  ;  the  median  eyes  are  also  of  the  simple  type  with  the 
sensory  cells  arranged  in  groups  each  centred  on  a  rhabdome.  These 
cells,  however,  are  peculiar  in  that  they  are  doubled  upon  themselves 
to  form  a  semi-inverted  retina  ^  (compare  Fig.  127). ^ 

The  KING-CRABS  (xiphosuea),  a  very  ancient  type  dating  to  the 
Silurian,  w^hich  live  in  shallow  water  on  the  sandy  shores  of  North 
America  {Limulus)  or  Asia,  have  two  large  lateral  compound  eyes  and 
two  median  ocelli  (Fig.  211).  The  compound  eye  is  of  a  unique  and 
elementary  type  ^  (Fig.  143)  ;  it  is  not  faceted  but  is  covered  by  a 
chitinous  thickening  of  the  cuticle  which  sends  projections  inwards  as 


Ki( 


'I'll  i:   .1  I  Mi'iN(.    Si'i  1  'i:i!,    /'/  /  A  //■ 


SIM'ATL'f!. 


From  the  Dutch  East  Indies.  The  2  large  and  6  small  simple  eyes  are 
seen  surrounding  the  anterior  and  lateral  aspects  of  the  carapace  (specimen 
from  Natural  History  Museum,  London). 


conical  papillse  over  each  ommatidium  to  form  a  corneal  lens.  The 
small  median  eyes  are  of  the  simple  type  wherein  the  sensory  cells  are 
associated  with  rhabdomes  (Fig.  142). 

In  addition,  a  third  pair  of  ventral  eyes  is  present  in  the  larva  on 
either  side  of  the  frontal  organ  of  the  hypostoma.  an  olfactory  organ  ; 
in  the  adult  these  eyes  become  degenerate  but  it  is  possible  that  they 
may  participate  in  the  olfactory  function  (Patten,  1893  ;  Hanstrom, 
1926). 

2  F  '  details,  see  J.  Miiller   (1826),  Lankester  and  Bourne  (1883),  Parker  (1887), 

Petrun!  -li   (1907),   Police   (1908),   Scheuring   (1913-14).   Biitschli   (1921),  Versluys 

and  Deu:  1923). 

"p. 


ARTHROPOD A 


213 


SPIDERS  (araneida)  are  of  widespread  distribution  and,  although 
comprising  some  14,000  species,  are  conveniently  divided  according  to 
their  habits  into  two  types,  the  relatively  sedentary  "  web-spinners  " 
and  the  more  active  "  wanderers  "  which  hunt  their  prey  ;  all,  how- 
ever, sjiin  silk,  either  as  a  web,  or  for  snaring  or  tying  up  their  victims, 
for  protection  of  their  cocoons  or  for  making  bridges  for  travelling.  In 
both  types  on  the  cephalothorax  there  are  G  or  more  usually  8  simple 
eyes  arranged  in  two  or  three  rows  (Fig.  212)  ;  these  have  received  a 
c«j:>''  ^'^rable  amount  of  study. ^  The  arrangement  of  these  ocelli  varies 
remarkably  (Figs.  213  to  216).  Among  the  web-spinners  the  ocelli  are 
rudimentary  and  their  effective  range  is  short.     The  common  house 

Figs.    213    to    216. — The    Arrangement    of    the    Ocelli    in    Different 
Species  of  Spiders. 


Fig.    213. — The  ocelli  of  tlu*  comtnon 
house  spider,  Te'jcu'irio  doinestica. 


Fic;.  214. — The  ocelli  of  the  common  garden 
spider,  Araueus  dldilcmatus. 


Y\Q.    21.5. — The    ocelli     of    the     wolf  FiG.  216. — The  ocelli  of  the  jumping  spider, 

spider,   Li/ro.sd  lujricoht.  Salticus  scenicu.s. 

1   For  details,  see  Hentschel  (1899),  Widmann  (1908),  Petrunkevitch  (1911),  Scheuring 
(1914),  Versluys  and  Demoll  (1923),  Savory  (1928),  Homanu  (1928-53),  Millot  (1949). 


214 


THE   EYE   IN  EVOLUTION 


Tegenaria 


Aratieus 


Salticus 


Whip-scorpiou 


spider,  Tegenaria  domestica,  has  two  rows  of  4  ocelli,  those  of  the 
anterior  row  being  slightly  smaller  than  those  of  the  posterior  (Fig.  213); 
the  common  garden  spider,  Araneus  diadematus,  has  4  median  and  4 
small  lateral  eyes  (Fig.  214).  The  more  active  hunting  species  which 
construct  no  web  have  larger  eyes  ;  thus  the  wolf-spider,  Lycosa, 
has  an  anterior  row  of  4  small  ocelli,  two  large  posterior  median 
and  two  smaller  posterior  lateral  ocelli  (Fig.  215)  ;  while  the  jumping- 
spider,  Salticus,  with  a  visual  capacity  more  fully  developed  than 
the  wolf-spider,  has  an  anterior  row  of  two  large  and  two  smaller 
ocelli  on  the  front  of  its  square-shaped  cephalothorax,  and  two  very 
small  posterior  median  and  two  posterior  lateral  ocelli  on  the  top 
(Fig.  216).  With  all  its  variations  the  general  plan  is  thus  consistent  ; 
the  anterior  median  eyes  (the  two  central  eyes  in  the  front  row)  have  a 
verted  retina,  the  remainder  are  inverted  provided  with  a  crystalline 
tapetum  ^  and  since  these  latter  glow  in  the  dark  the  former  are  some- 
times called  "  diurnal  eyes."  The  nerve-fibres  from  the  two  anterior 
median  eyes  travel — with  a  partial  decussation  at  a  chiasma — to  the 
ganglion  of  the  first  cephalic  segment,  from  the  remaining  eyes  to  that 
of  the  second  (Figs.  107,  126). 

It  is  interesting  that  the  anterior  median  eyes  of  spiders  are 
equipped  with  muscles  attached  to  their  posterior  aspect  rendering  them 
motile  so  that  they  can  increase  their  visual  field  ;  thus  web-spiders 
have  one  muscle,  Lycosids  two,  and  Salticids  six.  These  are  absent  in 
the  lateral  and  posterior  median  eyes. 

Curious  anomalies  to  this  general  arrangement  exist,  but  they  are  rare  ; 
thvis  in  the  female  of  a  spider  found  in  France,  Walckenaera  acuminata,  the  eyes 
are  arranged  on  a  dumpy  tubercle  on  the  cephalothorax,  while  in  the  inale  they 
are  perched  on  a  long  stalk-like  periscope,  4  on  the  tip  and  4  half-way  down 
(Millot,  1949).  It  is  interesting  that  among  spiders  the  lens,  which  is  part  of  the 
outside  covering  of  the  animal,  is  cast  at  the  time  of  moulting  and  thtis  it  would 
appear  that  the  spider  may  be  ren-dered  temporarily  blind. 

PSEUDO-SCORPIONS  (pseudoscorpionidea),  minute  animals  resem- 
bling miniature  scorpions  but  without  the  long  tail  and  sting,  found 
burrowing  in  books  or  under  stones,  the  bark  of  trees  and  the  wing- 
covers  of  insects,  are  provided  with  two  pairs  of  simple  eyes  (when 
they  exist)  on  either  side  of  the  cephalothorax  ;  the^e  are  typically 
equipped  with  an  inverted  retina  and  a  tapetum  (Scheuring,  1913) 
(Fig.  217). 

w^HiP-TAiLED  SCORPIONS  (PEDiPALPi).  The  eycs  of  this  order  are 
not  well  known  (Scheuring,  1913  ;  Versluys  and  Demoll,  1923  ;  Millot, 
H'49).  They  are  entirely  absent  in  some  species  ;  in  others  there  are 
two  median  eyes  only  ;  but  the  typical  arrangement  consists  of  two 
median  (principal)  eyes  and  two  groups  of  3  lateral  eyes. 

'  Except  Salticus,  the  eyes  of  which  lack  a  tapetum  and  are  therefore  "  diurnal  ". 
See  fr  '-■  p.  1.50. 


ARTHROPODA 


215 


The  median  eyes  are  of  the  cupulate  type  with  a  semi-inverted 
retina  the  cells  of  which  are  doubled  upon  themselves  ^  (Fig.  127).  The 
lateral  eyes  have  an  inverted  retina  with  a  tapetum  (Fig.  124). 


Fig.   217. — The  Pseudoscorpion,  Carffosius  ischsocbules. 

Showing  two  simple  eyes,  S,  on  either  side  (specimen  from  Natural  History 
IMuseum ) . 

HARVESTMEN  (PHALAXGIDA  ;  OPILIONES),  minute  spider-like 
Arachnids  with  extremely  long  legs,  which  avoid  the  glare  of  daylight, 
have  two  simple  ocelli  mounted  one  on  either  side  of  an  oculiferous 
tubercle  (ocularium)  (Fig.  218).  It  would  seem  that  with  its  laterally 
directed  eyes  the  animal  has  no  frontal  vision.    Each  ocellus  is  a  simple 


Harvestman 


As^.  *** 


Fig.  218. — The  Eye  of  the  Harvestman,  Megabusus  diadem  a. 
The  smiple  eye  is  seen  on  a  siDecial  oculiferous  tubercle  (specimen  from 
Natural  History  Museum). 

cupulate  eye  with  a  large  cuticular  lens  and  a  simple  row  of  visual  cells 
from  which  the  fibres  emerge  in  several  branches  to  form  the  optic 
nerve  (Purcell,  1894). 

^  p.  1.50. 


216 


THE   EYE   IN   EVOLUTION 


Jerrymander 


JEBRYMANDERS  (soLiFUG^) — active,  pugiiacious,  non-venomous, 
nocturnal  creatures  found  in  warm  countries — possess  a  pair  of  median 
(principal)  eyes  situated  on  a  small  tubercle  and  one  or  two  pairs  of 
lateral  eyes  usually  rudimentary,  difficult  to  see  and  probably  function- 
less.  Both  types  are  simple  cupulate  ocelli  with  direct  (verted)  retinse 
(Scheuring,  1913;  Demoll,  1917). 

MITES  and  TICKS  (acarina).  mites  are  minute  Arachnids  of  which 
over  20,000  species  are  known,  found  almost  universally  in  the  earth  or 
in  water,  salt  and  fresh,  often  of  parasitic  habit  on  or  within  animals 

(including  man)  and  plants  whether  alive 
or  decaying  after  death  :  well-known 
human  j^arasites  are  SarcojJtes  scabiei  (the 
itch-mite)  causing  scabies,  and  Dernodex 
foUiculorum  found  in  the  hair  follicles  ; 
the  harvest-mite  (chigger)  is  a  virulent 
pest  to  both  man  and  animals  (particularly 
rodents),  while  others  infest  insects  (Isle 
of  Wight  bee  disease)  and  others  plants 
(gall  mites,  red  spiders,  etc.).  Many,  such 
as  SarcojJtes  are  without  eyes  (Fig.  219)  ; 
others,  such  as  the  Prostigmata  and  the 
Hydracarina  (fresh-water  mites)  are  pro- 
vided with  2,  4  or  6  ocelli  on  the  front  and 
lateral  aspects  of  the  head  depending  on 
the  species,  the  individual  organs  being 
sometimes  fused  (Fig.  220  and  221)  (Lang, 
1905).  Each  possesses  a  convex  lens  often 
difficult  to  distinguish  from  the  surround- 
ing skin. 
TICKS  (ixoDiDEs)  are  larger  than  mites  and  are  frequently  of 
biological  importance  as  causing  disease  (tick-fevers)  in  man  ^  and 
animals. 2  Most  types  are  without  eyes,  but  such  species  may  have 
thin  transparent  areas  on  the  dorsal  surface  which  perhaps  respond  to 
differences  in  the  intensity  of  light.  When  visual  organs  are  present 
they  are  extremely  rudimentary,  being  minute  ocelli  mounted  curiously 
on  the  animal's  shoulder  (Fig.  222). 

Figs.  220  and  221. — The  Eyes  of  Fresh-water  Mites  (Hydracarina). 


Fig.  219. 


-The  Mite,  Sarcoptes 

SCABIEI. 


(Female)  (  X  125)  (Sutton  and 
Sutton,  Hh.  o/  Dis.  of  the  Skin, 
Mosby). 


Fig. 


220. — The    4    separate    ocelli    of 
Limnesia. 


Fig.  221. — Hijgrobates,  showing  fusion 
of  the  anterior  and  posterior  ocelli 
(after  P.  Lang). 

^  Texas  fever.  Rocky  Mountain  spotted  fever,  etc. 
2  Red -water  fever  in  cattle,  heart -water  in  sheep,  etc. 


ARTHROPODA 


217 


SEA-SPIDERS  (PYCNOGONiDA  ;  pantopoda).  marine  species  related  to  the 
Arachnids,  inhabit  the  shores  or  the  depths  of  the  seas,  Hving  on  seaweed, 
hydroids  and  sponges.  They  are  provided  with  4  primitive  oceUi  perched  in 
two  pairs  on  an  ocuHferovis  tubercle  on  the  cephalothorax  ;  as  we  have  already 
noted,  the  retinse  are  of  a  jieculiar  and  characteristic  inverted  type  ^  (Morgan, 
1891  ;   Korschelt  and  Heider,  1893  ;   Sokolow.  1911  ;   Schlottke.  1933)  (Fig.  125). 


Fig.   222. — The  Tick,  Amblfomma  pompo.^vm. 

The  two  simple  eyes,  S,  lie  well  posteriorly  on  the  shoulder  of  the  animal 
(specimen  from  Xatural  History  Museum). 


Pj'cnogonid 


IXSECTA 

INSECTS  form  the  largest  class  of  Arthropods  and  their  multitude 
of  types  is  subdivided  with  reference  to  their  possession  of  wings  ;  it  is 
interesting  that  the  complexity  of  their  eyes  varies  directly  with  this 
characteristic,  an  association  only  natural  in  view  of  the  demands  made 
upon  vision  by  a  high  degree  of  mobility. 

(1)  Sub-class  APTERYGOTA  (d,  privative  ;  -nrepv^  a  wing),  wingle.gs  forms, 
in  which  through  a  series  of  moults  the  adult  differs  little  from  the  newly  hatched 
insect  except  in  size.  They  are  the  most  primitive  of  insects,  some  species  being 
marine,  and  when  eyes  are  present  they  are  simple  in  type. 

THYSAXURA — bristle-tails,  of  wide  distribution  in  damp  soil,  son"ie  living 
between  tide-marks  or  under  stones  or  bark  ;  others  (silver-fish)  in 
bread-bins  or  books.    Closely  related  are  the  eye-less  diplura. 

PROTURA — ininute  creatures  (2  mm.)  living  in  moist  soils  vmder  stones 
and  bark,  without  wings,  antennae  or  eyes  of  anj^  kind. 

COLLEMBOLA — .sjiringtails,  living  under  stones  and  leaves  ;  one  species 
lives  between  tide-marks. 

(2)  Sub-class  pterygota,  provided  with  wings  which,  however,  may  be 
secondarily  lost  through  highly  evolved  specialization.     The  sub-class  is  divided 

1  p.  150. 


218 


THE   EYE   IN  EVOLUTION 
TYPICAL  INSECTS  :  I 

(Draivn  not  to  scale  but  approxitnately  to  a  standard  size.) 


THYSANURA 


APTERYGOTA 

PROTURA 


COLLEMBOLA 


Silver-fish 


Acerentonion 
EXOPTERYGOTA 


ORTHOPTERA 


Springtail 


DERMAPTERA 


Cockroach 


Grasshopper 


Stick-insect 


Earwig 


PLECOPTERA 


ISOPTERA 


PSOCOPTERA 


ANOPLURA 


Stone-fly 


Termite 


Book-louse 


Pediculus 


EPHEMEROPTERA 


THYSANOPTERA 


HEMIPTERA 


Thrip 


Bed-bug 


ARTHROPODA 


219 


TYPICAL  INSECTS  :  II 

(Drcuun  not  to  scale  but  approximately  to  a  standard  size.) 
EXDOPTERYGOTA 

NEUROPTEHA  TRICHOPTERA  LEPIDOPTERA 


Lacewing 


Caddis-fly 


Butterfly 


Moth 


COLEOPTERA 


^ky 


A. 


Colorado  beetle, 
Leptinotarsa 


Burying  beetle, 
Necrophorus 


Rose-chafer, 
Cetonia 


Fire-fly, 
Photinus 


HYMENOPTERA 


Bee,  Bombus 


Wasp,  Vesjm 


Ant 


APHANIPTERA 


Blue-bottle, 

CalUphora 


Gad-fly, 
Tabanus 


Bee-fly, 
Bombiiliiis 


Flea, 
Pulex  irritans 


220  THE   EYE   IN   EVOLUTION 

into  two,  depending  on  whether  their  wings  are  developed  externally  (Exoptery- 
gota)  or  internally  (Endopterygota)  ;  in  the  latter  the  wings  become  evident 
only  in  the  adult  (imago)  stage. 

(a)  EXOPTERYGOTA,  insects  which  undergo  a  series  of  moults  marked  by 
the  gradual  development  of  wings.     The  more  important  orders  are  : — • 

ORTHOPTERA — cockroaches,  locusts,  grasshoppers,  crickets,  stick- 
insects,  praying  mantis. 

DERMAPTERA — earwigs. 

PLECOPTERA — stone-flies,  a  small  and  little  known  order,  the  aquatic 
larvte  being  found  beneath  the  stones  of  mountain  streams,  and  the 
slow-flying  adults  having  a  very  short  life. 

ISOPTERA — termites  living  under  grovmd  without  eyes. 

EMBIOPTERA — a  few  species  of  insignificant  tropical  insects. 

ZORAPTERA — a  few  species  of  minute  insects  resembling  termites. 

psocoPTERA — small  plump,  book-lice  (winged  or  wingless). 

ANOPLURA — biting  or  sucking  lice,  wingless,  parasitic  on  man  and 
animals  and  frequently  disease-producing  {Pediculus,  Phthirus,  etc.). 

EPHEMEROPTERA — mayflies,  the  aquatic  larva3  living  up  to  3  years,  the 
delicate  adult  a  few  hours. 

ODONATA — brilliantly  colovired  dragonflies  and  demoiselle  flies  with 
aquatic  larvae,  the  former  unusually  active,  swift-flying  and 
voracious,  the  latter  more  delicate. 

THYSANOPTERA — the  minute  thrips,  vegetarian  in  habit,  living  on 
flowers,  leaves  and  decayed  vegetation. 

HEMiPTERA — bugs  with  a  specially  developed  proboscis  (rostrum) 
adapted  for  piercing  and  sucking,  many  of  them  beautiful  and  slender 
despite  their  name  :  land  bugs  including  the  bed-bug,  water  bugs 
varying  from  the  giant  flsh-killer  or  the  water-scorpion  to  the  water 
boatman  (Notonecta),  the  cicadas,  the  frog-hoppers,  tree-hoppers, 
leaf-hoppers,  the  aphids  (or  green-flies)  and  the  scale-insects. 

(b)  ENDOPTERYGOTA,  winged  insects  which  have  a  complete  metamorphosis 
(egg,  larva,  pupa,  adult)  with  a  resting  pupa  (or  chrysalis). 

NEUROPTERA — lace-wings,  alder-flies,  scorpion-flies. 

TRiCHOPTERA — caddis-flies,  with  aquatic  larvae  and  moth-like  adults 
with  hair-covered  bodies  and  wings. 

LEPIDOPTERA — butterflies  and  moths. 

COLEOPTERA — beetles,  including  over  200,000  known  species,  both 
terrestrial  and  water-beetles. 

STREPSiPTERA — Stylops,  miuvitc  insects,  parasitic  on  other  insects, 
particularly  wasps  and  bees. 

HYMENOPTERA — gall-flies,  saw-flies,  ichneumon-flies,  bees,  wasps,  ants. 

DIPTERA — two-winged  flies,  midges,  gnats,  mosquitoes  and  frviit-flies. 

APHANiPTERA — the  secondarily  wingless  fleas  (jiggers,  etc.),  blood- 
sucking in  habit  and  parasitic  on  birds  and  mammals. 

Ill  the  larval  form  all  insects  possess  simple  lateral  eyes  (stemmata; 
ardixixy.,  a  garland).  The  adult  also  frequently  possesses  simple  eyes 
(DOES.\f.  ocelli),  although  they  are  absent  or  vestigial  in  many  species, 
as  in  rt.ost  beetles  and  mosquitoes,  some  families  of  flies,  and  noctuid 
moths  nt  in  addition  it  is  provided  with  multifaceted  compound 
EYES.  his  generalization  there  are  some  exceptions  in  degenerative 


ARTHROPODA 


221 


forms  which  are  unprovided  with  compound  eyes — the  primitive 
wingless  Collembola  (Fig.  223),  hce  and  parasitic  fleas  which  possess 
only  ocelli  (Fig.  224),  while  species  which  live  in  darkness  may  be 
iniprovided  with  eyes,  such  as  the  Protura,  the  driver  ant  of  Africa, 
Dorylus  (with  the  exception  of  the  winged  male),  or  most  termites. 
The  winged  male  Stylops  has  aggregate  eyes  composed  of  a  multitude  of 
ocelli  so  closely  packed  together  as  to  resemble  a  compound  eye,  but 
the  parasitic  female  Mhich  passes  its  whole  life  within  its  host,  is 
unprovided  with  eyes.^ 


jVIale  driver  ant 


Figs.     22.3  and  224. — Insects    with    Ocelli    and    Xo    Compound    Eyes 
(Xatural  History  Museum,  London). 


Fig.  2l':;.  Tlic  springtail, 
Arrhi.stoiuti  brs-selsi  (Collem- 
bola). 

There  are  8  ocelli  on  each  side 
and  no  compound  eyes. 


Fig.   224. — The  bird-louse,   Trinoton  acidenlioii 
(Anoplura). 

There  are  2  simple  eyes  (S)  on  each  side  and  no 
compoimd  eyes. 


We  shall  see  ^  that  the  compound  eyes  are  the  dominant  organs  in  the 
adult  insect,  the  simple  eyes  essentially  accessory  ;  this  is  .seen  in  the  occasional 
disappearance  of  the  latter  as  the  former  develop.  Thus  the  larva  of  the 
water-beetle,  Dytiscus,  has  6  ocelli  on  each  side  of  the  head,  but  in  the  later 
stages  of  larval  development  the  compound  eye  appears  in  front  of  them,  first 
as  a  crescentic  area  on  each  side.  At  the  stage  of  moulting  the  cornea^  of  the 
ocelli  are  shed  with  the  cuticle  and  as  the  compound  eye  rapidly  develojDs  the 
bodies  of  the  ocelli  recede,  remaining,  however,  permanently  attached  in  vestigial 
form  to  the  optic  nerves, 

1  For  the  descriptive  anatomy  of  the  compound  eyes  of  Insects,  see  p.  166  ;  for 
that  of  the  ocelli,  see  Hesse  (1901),  Merton  (1905),  Link  (1908-9),  Strohm  (1910), 
Demoll  and  Scheurins  (1912).  Bugnion  and  Poiwff  ( 1914),  Melin  (1923).  Homann  (1924), 
Hamihon  (1925),  Zikan  (1929),  Wolsky  (1930-31),  Friederichs  (1931).  Verrier  (1940), 
Lhoste  (1941). 

^  p.  224. 


Female  driver  ant 


Stylops 


222 


THE   EYE   IN   EVOLUTION 


Figs.  225  to  227. — The  Compound  Eyes  of  Insects. 


Fig.   225. — The  head  of  the  dragon-fly,  jEschna  californica  (Odonata)  capped 
by  two  enormovis  crescent-like  comiDound  eyes  (James  Needham). 


Fig. 


l&.- 


-The    male    gadfly,    Ancnia   fasciata 
nilotica  (Diptera). 

The  immense  compound  eyes  occupy  the 
whole  of  the  surface  of  the  head  (Natural  History 
Museum,  London). 


Fig.    227. — The    cave-bug,    Leotichius 
glaucopis  (Hemiptera). 

From  Malaya.  Dorsal  surface.  The 
2  prominent  compound  eyes  (C)  are 
largely  spread  over  the  ventral  surface. 
There  are  2  median  ocelli  (S)  (Natural 
History  Museum,  London). 


THE  STEMMATA  (OR  LATERAL  OCELLi)  OF  LARVAL  OR  PUPAL  FORMS 

can  in  general  be  classified  into  two  main  types.  The  most  elaborate 
organs  are  seen  in  the  larvae  of  Lepidoptera  and  Trichoptera  ; 
these  are  arranged  in  a  group  of  variable  size  ^  on  either  side  of 
the  Jjcnd,  each  separate  individual  of  which  takes  the  form  of  the 
single       itnatidium  of  a  compound  eye  with  a  cuticular  corneal  lens, 

g.,  6  on  either  side  of  the  head  in  the  caterpillars  of  butterflies. 


ARTHROPODA 


223 


Figs.  228  and  229. — Stalked  Compound  Eyes. 


Fig.  228. — A  grouse  locust,  Ophiotettix  limosina  (Orthoptera). 

'        The  compound  eyes  (C)  are  placed  on  either  side  at  the  end  of  the  stalk- 
like head.     (One  antenna  is  missing.)     (Natural  History  Museum,  London.) 


Fig.   229. — The  stalk-eyed  fly,  Achias  rothschildi  (Diptera). 

The  lai'ge  compound  eyes  (C)  are  at  the  end  of  unusually  long  stalks 
(Natural  History  Museum,  London). 


a  crystalline  cone  and  a  retinule  of  7  sensory  cells  grouped  around  a 
rhabdome  (Fig.  138)  (Dethier,  1942-43).  A  more  simple  variety  is 
seen  in  the  larvae  of  Tenthredinidffi  (saw-flies)  and  Coleoptera.  These 
usually  have  two  lateral  eyes  of  cupulate  shape  with  a  retma  formed  as 
a  palisade  of  sensory  cells  under  a  lens -like  thickening  of  the  cuticle. 
The  retinular  cells  are  arranged  in  groups  of  two  or  three,  each 
group  around  an  elementary  rhabdome  which  is  not  constructed  for 
the  reception  of  images.     More  rudimentary  forms  occur  such  as  the 


Sawfly 


224 


THE   EYE   IN   EVOLUTION 


simple  pair  of  visual  cells  with  two  overlying  pigment  cells  which  form 
the  eye  of  the  larva  of  the  midge,  Ceratojjogon,  or  the  few  light-sensitive 
cells  lying  in  a  shaded  pocket  in  the  pharyngeal  skeleton  of  the  larva  of 
the  house-fly,  Musca  (Fig.  99)  (Welsh,  1937  ;    Debaisieux,  1939). 

THE  DORSAL  OCELLI  OF  ADULTS  were  described  and  figured  as  early 
as  1678  by  the  French  scientist,  de  la  Hire  (Figs.  149,  227,  230).  They 
are  usually  three  in  number  arranged  in  triangular  form,  one  median 
and  anterior  and  two  lateral  and  posterior  on  the  dorsal  aspect  of  the 


Figs.    230    and    23  L — Unusual    Compound    Eyes    in    Insects    (Natural 
History  Museum,  London). 


Fig.      230. — The     aphid,      Dnctynotus 
obscuras  (Homoptera). 

There  are  2  compound  eyes  (C)  one 
on  each  side  of  the  head,  and,  in 
winged  forms,  3  ocelh  on  tlie  vertex 
of  the  head,  the  median  one  of  which 
is  marked  S.  In  the  family  Aphididae 
there  is  in  addition  a  prominence,  the 
triommatidion  (T),  of  unknown  func- 
tion, bearing  3  facets  at  the  base  of 
each  compound  eye.  This  organ  is 
always  present,  even  in  those  forms  in 
which  a  comjjound  eye  is  lacking. 


Fig.       231.— The      Whirligig      beetle, 
Dineutus  grossus  (Coleoptera). 

There  are  2  compound  eyes  on  each 
side  of  the  head,  one  dorsal  (D)  for 
aerial  vision,  and  one  ventral  (V)  for 
vision  under  water. 


head  between  the  compound  eyes  ;  but  they  are  small  and  incon- 
spicuous, being  often  hidden  by  scales  as  in  moths  or  hairs  as  in  bees. 
In  some  species  of  ants  belonging  to  the  sub-family  Myrmicinae,  the 
anterior  ocelli  are  double  or  binary  in  type  (Weber,  1947).  In  others, 
such  as  Orthoptera,  the  ocelli  are  vestigial  ;  in  general,  their  degree  of 
development  shows  some  correlation  with  that  of  the  wings  (Kalmus, 
1945).  As  a  rule  they  resemble  in  structure  the  more  simple  type  of 
stemmata,  being  comjirised  merely  of  a  group  of  visual  cells  associated 
with  rb-'bdomes  lying  beneath  a  common  cuticular  lens  (Fig.  108). 

T        OMPOUND  EYES  OF  ADULTS  are  laterally  situated  on  the  head 
and  foi        be  essential  visual  organ  (Fig.   149).     They  are  large  and 


ARTHROPODA 


225 


prominent  and  vary  in  complexity  from  the  small  organ  of  the  worker 
of  the  ant,  Solenopsis.  which  lives  underground  and  is  provided  with 
6  or  8  facets,  to  the  elaborate  organ  of  dragon-flies  (Odonata)  with  up 
to  28,000  1  ommatidia  (Imms,  1935)  (Figs  225  to  227).  Occasionally 
the  compound  eyes  are  enormous,  literally  occupying  the  whole 
surface  of  the  head,  as  is  seen  in  the  gad-flies  (Tabanida?)  (Fig.  226)  ; 
usually  they  are  situated  on  the  surface  of  the  head,  sometimes  they 
stand  out  prominently  as  in  the  praying  mantis  (Fig.  734),  but  occasion- 
ally they  are  perched  on  long  stalks  (Figs.  228  and  229).  Exceptionally 
two  compound  eyes  are  differentiated  in  function,  such  as  in  the 
whirligig  beetle,  Dineutus,  which  has  a  dorsal  compound  eye  for  aerial 
vision  and  a  ventral  for  vision  under  water  (Fig.  231).-  A  unique  organ 
is  seen  in  the  Aphid  family  ("  green-fly  ")  in  which  an  additional  tri- 
faceted  organ,  the  triommatidion,  is  found  at  the  base  of  each 
compound  eye  (Fig.  230)  ;  the  function  of  this  organ  is  imknown  but 
it  is  present  even  in  those  forms  of  aphids  which  have  no  compound 
eyes. 


von      Buddenbrock,      Moller-Racke      and 

Schaller.    Experientia,  10,  333  (1954). 
Biitschli.       Vorlesungen     ii.     vergl.    Anrit., 

Berlin,  872  (192'l). 
Bugnion  and  Popoff.     Arch.  Anat.  inter., 

16,  261  (1914). 
Caesar.      Zool.   Jb.,   Abt.    Anat.,   35,    161 

(1913). 
Constantineanu.    Zool.  Jb.,  Abt.  Annt.,  52, 

253  (1930). 
Dakin.    Quart.J.»ilcr.Sci..6b,  163(1921). 
Debaisieux.    Ann.  Soc.  Sci.,  Bruxelles,  59, 

9  (1939). 
DenioU.   Die  Sinnesorgane  der  A  rthropoden, 

Braunschweig  (1917). 
Demoll   and   Scheuring.      Zool.  Jb.,   Abt. 

Zool.  Physiol.,  31,  519  (1912). 
Dethier.     J.  cell.  camp.  Pltysiol.,  19,  301 

(1942)  ;    22,  115  (1943).' 
Dijkgraaf.       Z.    vergl.    Phi/siol.,    38,    491 

(1956). 
Exner.       Die     Physiologic    d.    Jacetlicrten 

Augen     von     Krebsen      u.     Insekten, 

Leipzig  (1891). 
Fales.    Biol.  Bull.,  54,  534  (1928). 
Friederichs.    Z.  Murphol.  Oekol.  Tiere,  21, 

1  (1931). 
Graber.    Arch.  mikr.  Anat.,  17,  58  (1880). 
Grenacher.      .-^rch.    mikr.   Anat.,   18,   415 

(1880). 
Zool.  An: 
Hamilton. 

(1925). 
Hanstrom. 

(1926). 
Harris  and  Mason 

280  (1956). 


,  18,  280  (1895). 

Publ.    U.S.  nat.   Mus.,  65,    1 


Lunds     I 


Aarssr,     22 
Proc.  toy.  Soc.  B.,  145, 

1  p.  172. 


Hentsfhel.     Zool.  Jb.,  Abt.  Anat.,  12,  509 

(1899). 
von  Hess.  Vergl.  Physiol,  d.  Gesichtssinnes, 

Jena,  79  (1912). 
Hesse,  R.     Zool.  Anz.,  24,  30  (1901). 

Das    Sehen    der    niederen     Tiere,    Jena 

(1908). 
de  la  Hire.     Mem.  Acad.    roy.  Sci.  Paris 

(1666-1699),  10,  609  (1730). 
Homann.    Z.  vergl.  Physiol.,  1,  541  (1924)  ; 

7,  201  (1928)  ;    14,  40  (1931). 
Zool.  Jb..  Abt.  Anat.,  71,  56  (1950)  ;   72, 

345  (1952). 
Biol.  Zbl.,  72,  373  (1953). 
Imms.      Textbook  of  Entomology ,  London 

(1935). 
Kalmus.     Proc.  roy.  entom.  Soc.  Lond.,  A, 

20,84(1945). 
Kor.schelt  and  Heider.    Vergl.  Entwicklung. 

d.  Wirbellosen  Tiere,  Jena,  664  (1893). 
Lang.      Zool.    Jb.,    Abt.    Anat.,    21,    453 

(1905). 
Lankester  and  Bourne.     Quart.  J.  micr. 

Sci.,  23,  177  (1883). 
Lhoste.    Bull.  Soc.  zool.  Fr.,  66,  62  (1941). 
Link.     Zool.  Anz.,  33,  445  (1908). 

Zool.  Jb.,  Abt.  Anat. ,2,1, -m,  281  (1909). 
Melin.     Zool.  Bidrag  Uppsala,  8,  1  (1923). 
Merton.     Z.  iviss.  Zool.,  79,  325  (1905). 
Millot.     Grasse's  Traite  de  Zool.,  Paris,  6, 

295,  533,  589,  698  (1949). 
Morgan.     Biol.  Stud.  Johns  Hopk.  Univ., 

5,  49  (1891). 
Muller,  J.     Zur  vergl.  Pliysiol.  des  Gesichts- 
sinnes   des    Mensclien    it.    d.     Thiere, 

Leipzig  (1826). 


Dragon-fly 


Whirligig  beetle 


Aphid 


-  Compare  the  eye  of  Anableps,  p.  324. 


S.O. — VOL.  I. 


15 


226 


THE   EYE   IN   EVOLUTION 


Parker.     Bull.  Mus.  Comp.  Zool.,  13,  173 

(1887). 
Patten.     Quart.  J.  micr.  Set.,  35,  1  (1893). 
Petrunkevitch.       J.     exp.     Zool.,    5,     275 

(1907). 
Zool.  Jb.,Abt.Syst.  Biol.,  Zl,  355  {Idll). 
Police.    Zool.  Jb.,  Abt.  Anat.,  25,  1  (1908). 
Purcell.     Z.  wiss.  Zool.,  58,  1  (1894). 
Radl.      Pflugers  Arch.   ges.    Physiol.,   87, 

418  (1901). 
Savory.     The  Biology  of  Spiders,  London 

(1928). 
Scheuring.     Zool.  Jb.,  Abt.  Anat.,  33,  553 

(1913)  ;   37,  369  (1914). 
Schlottke.    Z.  mikr.  Anat.  Forsch.,  32,  633 

(1933). 
Sehulz.    Z.  vergl.  Physiol. ,1,  488  (1928). 


Sokolow.     Z.  wiss.  Zool.,  98,  339  (1911). 
Strohrn.     Zool.  Anz.,  36,  156  (1910). 
Tompsett.     Liverpool  marine  biol.  Comm. 

Mem.,  32,  1  (1939). 
Vaissiere.     C.  R.  Acad.  Sci.  (Paris),  238, 

942  (1954)  ;    240,  345  (1955). 
Verrier.     Bull.  Biol.  France  Belg.,  74,  309 

(1940). 
Versluys   and   Demoll.      Ergebn.    Fortsch. 

Zool.  Jena,  5,  67  (1923). 
Weber.     Biol.  Bull.,  93,  112  (1947). 
Welsh.    .Sczence,  85,  430  (1937). 
Widmann.     Z.  wiss.  Zool.,  90,  258  (1908). 
Wolsky.    Z.  vergl.  Physiol.,  12,  783  (1930) ; 

14,  385  (1931). 
Biol.  Bev.,  8,  370  (1933). 
Zikan.     Zoo/,  ylnz.,  82,  269  (1929). 


CHAPTER   VIII 
THE  EYES  OF  PROTO-CHORDATES 

The  Chordates  constitute  a  phylum  characterized  by  a  dorsal 
tubular  nerve-cord,  a  dorsal  supporting  axis  (a  notochord)  and  pharjTi- 
geal  gill-slits  ;  the  last  two,  however,  may  be  temporary  in  duration. 
The  Vertebrates  constitute  a  sub-phylum  within  the  Chordates  which 
possesses  as  distinctive  characters  a  head  and  skull,  a  brain  with  eyes,  a 
vertebral  column,   and  (generally)  paired  limbs.     Stumbling  on  the 


FiG.   232. — B.iLAyoGLOssvr. 

The   long   tongue-like   proboscis    (Pr)    resembles  an   acorn    (/3aAo(i'Of,    an 
acorn  ;    yXioaax,  a  tongue). 


border-line  between  Invertebrates  and  Vertebrates  are  three  classes  of 
animals  (Proto-chordates)  possessed  of  a  rudimentary  nerve-cord,  a 
notochord  and  gill-clefts — the  Hemichordates,  the  Tunicates,  and  the 
Lancelets.  Apart  from  the  pelagic  Tunicates,  these  lowly  creatures 
are  either  sessile  or  burro\\ing  in  habit. 

The  HEMiCHOEDATA  are  typified  in  Balanoglossus,   a  worm-like 
marine  creature  burrowing  in  the  sand  and  mud  of  most  seas  (Fig.  232). 


Fig.  233. — The  Eyes  in  the  Tornaria  Larva  of  Bala.\oolossvs. 
Antero-posterior  section  through  the  apical  plate  showing  the  anterior, 
EA,  and  posterior,  EP,  eyes  (after  Morgan). 


The  nervous  system  arises  as  a  longitudinal  groove  of  ectoderm  which 
becomes  tubular  but  gives  no  evidence  of  visual  out-pouchings.  In  the 
larv£e  (tornaria)  of  some  species  situated  on  the  apical  plate  there  are 
two  eye-spots  consisting  of  cup-shaped  depressions  of  clear  cells 
surrounded  by  pigment  (Fig.  233),  but  in  the  adult  there  are  no  special 
sense  organs  (Spengel,  1893  ;   Stiasny,  1914). 

227 


228 


THE   EYE   IN  EVOLUTION 


Fig.    234.— The    Sea- 
squirt,  ascidia. 

The  adult  covered  by 
its  tunic  (test),  the  lower 
end  attached  to  a  rock, 
the  upper  end  ending  in 
an  inhalant  siphon 
(mouth),  and  on  the  mor- 
phological dorsal  surface 
an  exhalant  sijshon 
(atrial  opening).  Around 
both  apertures  thei-e  are 
sometimes  jDigment  spots 
of  unknown  character. 
During  life,  the  animal 
draws  water  in  through 
the  first  and  expels  it 
from  the  second  ;  if 
irritated,  water  is  forci- 
bly expelled  from  both, 
hence  the  name  "  sea- 
squirt." 


The  TUNiCATA  (urochordata)  are  typified 
in  the  Ascidians  or  sea-squirts  (Fig.  234). 
Ascidia  in  its  free-swimming  larval  stage  is  a 
tadpole-like  creature,  about  1"0  mm.  in  length, 
possessing  the  chordate  characteristics  of  a 
brain  and  a  dorsal  tubular  nervous  system,  a 
notochord  and  gill-slits.  At  this  stage  it  is 
provided  with  a  single  cerebral  eye  associated 
with  a  statocyst,  but  as  the  hermaphroditic 
adult  settles  to  its  sedentary  plant-like  life 
within  its  thick  tunic  of  cellulose  and  attaches 
itself  to  rocks  or  weeds,  the  nervous  system  is 
reduced  to  a  single  ganglion  above  the  pharynx 
and  the  eye  disappears.  In  some  of  these  forms 
the  siphons  respond  to  light  by  retraction.  It 
is  true  that  pigmented  spots  are  found  around 
the  siphonal  openings,  which  used  to  be  con- 
sidered "  ocelli",  but  in  Ciona,  at  any  rate,  they 
are  in  fact  not  light-sensitive  (Millott,  1957). 


The  transient  eye  of  the  larval  Ascidian  is  of  un- 
usvialmterest  (Kowalevsky,  1871  ;  vonKvipffer,  1872  ; 
Froriep,  1906).  It  arises  as  an  out-pouching  of  the 
cerebral  vesicle  which  forms  a  single  sensory  organ 
consisting  of  a  sac  containing  a  statocyst  and  an 
extremely  elementary  eye  on  its  dorso -posterior  wall 
(Fig.  235).  The  retina  is  composed  of  a  few  sensory 
cells  derived  from  the  inner  wall  of  the  neural  tube  ; 
it  is  capped  with  pigment  and  above  it  lies  a  rudi- 
mentary cellular  lens.  It  is  interesting  that  the  visual  cells  are  morphologically 
inverted  inasmuch  as  they  face  towards  the  cavity  of  the  sensory  vesicle  while  the 
intrinsic  lens  faces  towards  the  brain  as  if  it  would  be 
effective  only  for  light  traversing  the  transparent  body 
of  the  animal. 

In  free -swimming  Tunicates  visual  organs  may 
persist  ;  thvis  in  the  asexual  form  of  Salpa  there  is  a 
single  median  horse-shoe-shaped  ocellus  and  some- 
times smaller  accessory  ocelli  on  the  dorsal  aspect  of 
the  animal  closely  associated  with  the  single  nerve 
ganglion. 


The      LANCELETS       (ACRANIA  ;         CEPHALO- 

chordata)  are  variously  regarded  as  a  pioneer 
off-shoot  from  the  chordate  stock  or  as  a 
degenerate  member  of  the  phylum.  They 
possess  a  dorsal  tubular  nerve-cord,  a  notochord 
and  giU  slits  but  lack  a  differentiated  brain  or 
eyes.  T"     -  are  typified  in  the  common  lancelet. 


Fig.    235. — The   Eye   of 

THE  ASCIDIAN  TaDPOLE 

Diagram  of  the  sensory 
vesicle  with  a  unicellular 
otolith  and  an  ocellus 
(above  right)  with  retinal 
cells,  pigment  and  3  lens 
cells  situated  towards  the 
cavity  of  the  vesicle  (Ber- 
rill,  The  Origin  of  Verte- 
brates, Oxon.,  1955). 


PROTO-CHORDATES 


229 


Branchiostoma  (Amphioxus)  lanceolatum,  a  small  translucent  fish-like 
marine  creature  about  2  in.  in  length  the  body  of  which  is  divided  into 
62  myotomes  (Fig.  236).  Although  possessing  no  definitive  eyes,  the 
animal  is  strongly  photo -negative  and  sensory  organs  occur,  some 
possibly  in  the  surface  ectoderm  and  others  deeply  placed  in  relation 
to  the  neural  tube  which  tend  to  enforce  upon  the  animal  its  burrowing 
habit. 


Fig.   236. — The  Lancelet,  Amphioxus. 
The  head  end  is  towards  the  right,  the  tail  end  to  the  left  (after  Haeckel). 

The  superficial  sensory  organs  are  the  large  isolated  cells  of  Joseph 
(1904-28),  associated  with  the  surface  eiaitheliuni  on  the  dorsal  aspect,  which 
were  claimed  by  this  investigator  to  be  light-sensitive  (Fig. 237)  ;  this  view, 
however,  is  by  no  means  substantiated. 

The  neural  photosensitive  organs  are  of  two  types  (Fig.  237).  Towards  the 
cephalic  end  of  the  animal  a  small  median  area  of  ependymal  cells  lining  the 
central  canal  of  the  nerve-cord  is  specially  differentiated  to  form  an  infundi- 
bular ORGAN  which  appears  to  be  light-sensitive  and  is  functionally  allied  to  a 


Fig.  237. — Sagittal  Section  of  the  Anterior  Portion  of  Amphioxus. 

CJ,  cells  of  Joseph  ;   Inf,  infundibulum  ;   NC,  neural  oanal  ;   PS,  anterior 
pigment  spot  (after  Boeke). 


dark  pigment -spot  situated  at  the  head  end  of  the  animal.  The  pigment-spot 
was  originally  described  as  an  "  eye-spot  "  by  Johannes  Miiller  in  1842,  and 
used  to  be  credited  with  light-sensitive  properties  and  specific  connections  with 
the  central  nervous  system  ^;  it  was  indeed  held  to  be  the  phylogenetic  precursor 
of  the  vertebrate  eye.  Its  specific  innervation,  however,  was  contested  initially 
by  Kohl  (1890)  and  conclusively  by  Fi-anz  (1923),  and  a  visual  function  excluded 

1  See  the  writings  of  W.  Miiller  (1874),  Langerhans  (1876),  Ayers  (1890),  Joseph 
(1904-28),  Edinger  (1906),  Boeke  (1908),  Pietschmann  (1929). 


230 


THE   EYE   IN   EVOLUTION 


by  the  experiments  of  Nagel  (1896)  and  Hesse  (1898) 
and  more  particularly  by  those  of  Parker  (1908)  and 
Crozier  (1917).  There  would  seem  little  doubt  that 
it  is  not  a  vestigial  eye  but  that  its  function  is  to 
endow  the  infundibular  organ  with  directional  ability 
by  casting  a  shadow  upon  it  when  the  animal  or  the 
light  source  moves,  a  primitive  role  we  have  already 
seen  in  the  eye -spot  of  the  Protozoon,  Euglena  ^ 
(Franz,  1912-34  ;   WoUenhaupt,  1934). 

A  second  jDhotosensitive  mechanism  is  seen  in  the 
ORGANS  OF  HESSE  (1898),  individual  cells  scattered  on 
the  ventral  and  lateral  aspects  of  the  nerve-cord  to- 
wards its  posterior  end  (Figs.  238  and  239).  These 
are  single  large  ganglion  cells  variously  orientated, 
each  provided  with  a  brush-like  ciliated  margin  and  an  issuing  nerve-fibre,  each 
capped  by  a  crescent-shaped  pigment  cell  to  give  it  directional  a.bility.  The 
distribution  and  structure  of  these  unique  cells  have  been  fully  studied  by  a 
number  of  observers  (Franz,  1923  ;  Joseph,  1928  ;  Kolmer,  1928  ;  WoUenhaupt, 
1934)  and  their  photosensory  function  established  by  Parker  (1908)  and  Crozier 
(1917). 


Fig.    238. — Visual   Cell 
of  auphioxvs. 

n,  nucleus  ;  c,  striated 
margin  ;  p,  jjigment 
mantle. 


Fig.  239. — The  Neural  Visual  Cells  of  Amphioxus. 

Section  through  the  sj^inal  cord  in  the  region  of  the  5th  segment,  showing 
the  central  canal,  C,  and  the  large  visual  cells  of  Hesse,  H,  with  their  associated 
pigment  cells  (after  Hesse). 


Ayers.    ZooZ.  ^Inz.,  13,  504  (1890). 
Boeke.    Anat.  Anz.,  32,  473  (1908). 
Crozier.    Anat.  Rec,  11,  520  (1917). 
Edingef.    Anat.  Anz.,  28,  417  (1906). 
Franz.     /?-o/.  Zbl.,  32,  375  (1912). 
Jena.  Z.  Natzirw.,  59,  401  (1923). 


Bolks  . 
Berl,. 


vergl.  Anat.  d.  Wirb'lliere, 
(ii),  989  (1934). 


Froriep.      Handbuch   d.   vergl.   und  exper. 
Entwicklungslehre  d.  WirbeUiere,  Jena, 
2  (1906). 
Anat.  Anz.  (suppl.),  29,  145  (1906). 
Hesse.  R.  Z.  wiss.  ZooL,  63,  456  (1898). 
Joseph.    Anat.  Anz.  (suppl.),  25,  16  (1904). 

Biol,  generalis,  4,  237  (1928). 
Kohl.     Zool.  Anz.,  13,  182  (1890). 


126. 


PROTO-CHORDATES 


231 


Kolmer.     Biol.  generaUs,  4,  256  (1928). 
Kowalevsky.     Arch.  wikr.  Anat.,  7     101 

(1871). 
von  Kupffer.     Arch,  tnikr.  Anat.,  8    358 

(1872). 
Langerhans.     Arch.  mikr.  Anal.,  12.  290 

(1876). 
Millott.     Endeavour,  16,  19  (1957). 
Miiller,  J.     Abh.  Kgl.  Akad.  Wiss.,  Perlin 

(1842). 
Muller,   W.      V.  d.  Stamme.sentivicklunq  d. 

Sehorgans     d.      Wirbelthiere,     Leipzig 

(1874).  ^     ^ 


Nagel.      Der  Lichtsinn  uugenloser   Tiere  : 

eine  biologi.<<che  Studie,  Jena  (1896). 
Parker.     Proc.  Amer.  Acad.  Arts  Sci..  43, 

415  (1908). 
A7ner.  Nat..  42,  601  (1908). 
Pietschmann.     Kiikenthal's  Handbnch  der 

Zoologie,  Berlin  (1929). 
Spengel.    Fau?ia  e  Flora  Golf.  Napoli,  18, 

1  (1893). 
Stiasny.     Z.  wis.':.  Zool.,  110.  36  (1914). 
Wollenhaupt.     Jena.  Z.  Naturw.,  69,   193 

(1934). 


Fig.  240.— Sir  Edwin  Ray  Lankester  (1847-1929). 
^From  a  portrait  by  John  Collier  in  the  Linnean  Society.) 


CHAPTER   IX 
THE  EVOLUTION  OF  THE  VERTEBRATE  EYE 

SIR  EDWIN  RAY  LANKESTER  (1847-1929)  (Fig.  240),  One  of  the  foremost 
British  naturalists  of  the  last  generation,  made  outstanding  contributions 
to  the  subject-matter  of  this  chapter.  The  origin  of  the  vertebrate  eye  has  long 
been  a  puzzle  and  indeed  still  is  ;  and  Lankester  was  one  of  the  first  to  introduce 
rationalism  into  the  problem  which  had  been  largely  speculative  up  to  his  tiine. 
He  sviggested  that  in  the  early  Proto-chordates,  transparent  marine  animals, 
an  eye  associated  with  the  central  nervovis  system  would  be  a  more  plastic 
organ  than  one  derived  from  the  integumentary  epithelium  and  as  effective 
optically  in  organisms  of  this  type  ;  as  the  bodies  of  Vertebrates  become  opaque, 
migration  of  the  eye  towards  the  svirface  became  an  obvious  evolutionary 
expedient.  He  was  an  example  of  that  erudite  type  of  scientist  who  was  yet  able 
to  popularize  his  philosophy,  a  type  in  which  Britain  has  always  been  rich.  His 
academic  career  was  full — Professor  of  Zoology  and  Comparative  Anatomy  at 
University  College  London  (1874-90),  Linacre  Professor  of  Comparative  Anatomy 
at  Oxford  (1891-98),  director  of  the  Xatural  History  Department  of  the  British 
Museum  (1898-1907),  and  much  of  that  time  FuUerian  Professor  of  Physiology 
and  Comparative  Anatomy  at  the  Royal  Institution,  London.  He  founded  the 
Marine  Biological  Association  in  1884,  was  its  President  in  1892,  and  received 
the  Royal  (1885)  and  Copley  (1913)  Medals  of  the  Royal  Society. 

The  VERTEBRATE  PHYLUM  is  of  cnormous  anticjuity  and  stems  from  the 
primitive  Agnatha,  jaw-less  pre-fishes,  the  fossil  remnants  of  which  are  400 
million  years  old  and  are  found  abundantly  in  ancient  Silurian  rocks.  Their 
ancestors  are  unknowTi  ^  but  their  descendants  have  become  the  lords  of  the 
earth.  It  is  interesting  that  as  a  general  rule  evolution  proceeds  through  primi- 
tive forms  which,  because  of  their  simplicity  and  plasticity,  have  the  jDOtentiality 
to  evolve  into  more  highly  differentiated  forms  ;  but  these  latter,  because  of 
their  high  differentiation  and  consequent  superior  equipment,  can  exterminate 
their  primitive  forebears  in  the  struggle  for  existence,  but  for  the  same  reason 
are  incapable  of  further  differentiation.  The  tendency  is  therefore  for  evolution 
to  proceed  from  primitive  forms  which  have  become  largely  extinct,  producing 
in  its  progress  a  series  of  evolutionary  dead-ends  each  showing  different  highly 
developed  tj-pes  of  adaptive  mechanisms  designed  to  meet  different  specialized 
circumstances. 

During  recent  years  the  views  of  zoologists  on  evolution  within  the  vertebrate 
phylum  have  changed  considerably  and  it  is  probable  that  they  have  not  yet 
finally  crystallized  (Romer,  1947  ;  Trewavas  et  al.,  1955)  (Fig.  241).  It  would 
seem  established,  however,  that  the  most  archaic  vertebrates  are  the  worm-like 
Agnatha,  pre-fishes  without  jaws  or  limbs,  which  survive  to-day  in  the  primitive 

^  At  one  time  or  another  the  ancestry  of  Vertebrates  has  been  sought  in  almost 
every  invertebrate  group,  particularly  annelid  worms,  Arthropods  (especially  Arachnids 
through  Eurypterids).  Perhaps  the  most  reasonable  theory,  however,  ascribes  a  com- 
mon origin  to  the  larvaj  of  the  simplest  Chordates  and  those  of  Echinoderms,  despite  the 
vast  and  obvious  discrepancy  between  the  adults  in  each  phylum.  Palaeontology, 
however,  provides  no  record  of  such  tiny,  soft -bodied  creatures  as  these  larvae  since  they 
are  incapable  of  preservation  as  fossils  (see  Romer,  1947). 

233 


234 


THE   EYE   IN   EVOLUTION 


PLACODERMS^ 
(all  extinct) 


Fig.  241.— The  Vertebrate  Phylum 


AGNATHA 


Primitive 
Fishes 


)-Lamprey~l  Extant 

Hag  JCyclo- 

J  stomes 

.CHONDRICHTHYES 
(Selachians  and 
Holocephalians) 


Poiypterini  -^ 
and  sturgeons 


Bow-fin  and 
gar-pike 


OSTEICHTHYES 

I 
Actinopterygii       |      Crossopterygii- 


Chondrostei 


Holostei 


I 

Teleostei 

(modern  bony 

fishes) 


Rhipidistia 


Primitive  - 
AMPHIBIA 


I 

Primrtive 

REPTILES 

(Cotylosauria) 


— >Dipnoi 


Coelacanths 
{Latimeria) 


f;"":;^   lExtant 
Urodela  >  .       ,  .,  . 
Apoda    J  Amphib.a 


-Chelonia\ 


Therapsida  |  Sauropsida->Sp/ienodon 
Lizards 
and 
snakes 


Extant 
Reptiles 


4 
MAMMALS 


Archosauria  ->  Croco- 
(Dinosaurs)       diles 

I 

BIRDS 


EXTINCT    VERTEBRATES 

(Drawn  not  to  scale  but  to  standard  size) 


Agnathous  Fishes 
Pteraspis  Cephnlaspis 


Placoderm 


Rhipidistian 


Prinutive 
Ampb  ■  '-n 


Primitive 
Reptile 


Dinosaur, 
Diplodocus 


THE   VERTEBRATE   EYE  235 

Cyclostomes,  the  lamprey  and  the  hag.  From  these  there  evolved  somewhere 
in  the  Upper  Silurian  period,  350  million  years  ago,^  the  true  (gnathous)  fishes, 
possessed  of  jaws  and  paired  fins.  From  these  primitive  fishes  three  classes 
radiated  :  (1)  the  Placoderms,  a  motley  class  mostly  with  bony  armour,  which 
flourished  in  Devonian  times  but  none  of  which  survived  the  Palaeozoic  era  ; 
(2)  the  Chondrichthyes,  a  class  of  cartilaginous  fishes  of  great  age  which  are  now 
represented  only  by  the  Selachians  (sharks  and  rays)  and  Holocephalians  (deep- 
sea  chimtpras)  ;  and  (3)  the  Osteichthyes,  the  much  larger  class  of  bony  fishes. 
While  the  Placoderms  have  disappeared,  and  the  cartilaginous  fishes,  prolific 
in  the  older  geological  periods,  have  steadily  decreased  in  importance  in  more 
recent  times,  the  bony  fishes  have  shown  themselves  remarkably  adaptive. 
By  the  end  of  the  Palceozoic  era  they  had  attained  almost  sole  possession  of 
fresh-water  streams  and  lakes  ;  at  that  time  they  had  invaded  the  sc^^s  also 
and  rapidly  constituted  the  vast  majority  of  marine  forms. 

These  bony  fishes  may  be  divided  into  two  main  sub-groups,  each  of  which 
has  numerous  survivors  :  the  Actinopterygii  and  the  Crossopterygii.  From  the 
former  a  series  of  forms  arose  in  linear  progression — the  Chondrostei,  still  with 
a  largely  cartilaginous  internal  skeleton,  degenerative  representatives  of  which 
still  survive  as  the  Polypterini  (two  species  of  which  are  extant)  and  the  sturgeons  ; 
the  Holostei,  provided  with  bony  skeletons,  represented  today  only  by  two 
American  fresh-water  fishes,  the  bow-fin  and  the  gar-pike  ;  and  eventually  the 
Teleostei,  the  most  specialized  of  all  fishes  which  include  practically  all  modern 
species. 

From  the  early  Crossopterygii  the  Dipnoi  (lung-fishes)  appeared  as  an 
aberrant  off-shoot  in  the  lower  Devonian  period  ;  of  these,  three  species  survive 
today,  swamp -dwelling,  mud-loving  and  eventually  air-breathing  fishes  in  which 
the  swim-bladder  has  been  retained  as  a  functioning  lung.  From  the  main 
group,  however,  a  direct  line  of  vertebrate  descent  continued  through  the 
Rhipidistia  (a  derivative  of  which  exists  today  as  the  Coelacanth,  Latimeria)  ; 
these  fish  could  already  breathe  air  so  that  they  only  had  to  turn  their  fins 
into  legs  and  modify  the  ear  to  become  Amphibia  and  survive  on  land.  Develop- 
ing as  tadpole-like  aquatic  creatures,  they  underwent  this  remarkable  meta- 
morphosis as  they  matured  into  their  adult  forms.  Initially  they  lived  side-by- 
side  with  their  cousins,  the  lung-fishes,  in  the  swamps  ;  but  when  the  great 
droughts  appeared  and  the  fresh-water  pools  dried  up  towards  the  end  of  the 
Devonian  period  some  300  million  years  ago,  the  lung-fishes  largely  perished, 
but  the  Amphibians,  capable  of  creeping  and  feeding  on  land,  survived.  Their 
first  representatives  have  long  become  extinct  and  the  class  survives  today 
only  in  three  relatively  unimportant  and  highly  specialized  groups — the  frogs 
and  toads  (Anura),  the  salamanders  and  newts  (Urodela)  and  the  worm-like 
Cfecilians  (Apoda).  From  the  highly  adaptable  primitive  types,  however, 
there  evolved  in  the  Upper  Carboniferous  period  the  first  fully  terrestrial  verte- 
brates, the  most  primitive  Reptiles,  born  on  land  and  capable  of  existing  away 
from  water  altogether.  This  spectacular  step  in  evolution  was  made  possible 
by  the  development  of  a  large  and  highly  nutrient  egg  protected  by  a  porous 
shell  so  that  the  young  reptile  could  emerge  fully  equipped  for  terrestiial  life. 

For  many  millions  of  years  these  primitive  reptiles  fiourished  exceedingly  ; 
emerging  on  to  the  hitherto  unexploited  land,  rich  in  vegetation  and  food,  they 
spread  and  gave  rise  to  a  multitude  of  new  types,  some  of  them  of  incredible 
form  and  giant  size.  They  still  retained,  however,  the  cold-blooded  characteristic 
of  their  fish  and  amphibian  ancestors,  and  thus,  presumably  owing  to  the  climatic 
changes  at  the  end  of  the  IMesozoic  era,  this  group  which  had  dominated  the 

1  See  p.  754. 


236  THE   EYE   IN  EVOLUTION 

earth  for  more  than  100  miUion  years  perished,  apart  from  a  few  unimportant 
exceptions — the  very  primitive  Chelonians  (tortoises  and  turtles),  the  almost 
extinct  Rhynchocephalian,  Sphenodon,  of  lineage  almost  as  remote  ;  and  the 
more  modern  groups,  lizards  and  snakes  and  crocodiles. 

The  handicap  of  cold-bloodedness  limited  these  surviving  Reptiles  to  the 
warmer  parts  of  the  earth.  In  the  even  temperature  of  the  sea  the  Teleosteans 
could  flourish  without  hindrance  ;  to  populate  the  cooling  earth  homeostasis 
had  to  be  achieved  ;  this  was  eventually  acquired  by  Birds  and  Mammals,  the 
former  assuming  an  insulating  coat  of  feathers,  the  latter  usually  of  hair  in 
place  of  the  scales  characteristic  of  Reptiles.  Of  the  two  the  Mammals 
claim  the  more  primitive  descent,  stemming  from  the  Therapsidans,  mammalian- 
like Reptiles  which  flourished  in  Permian  and  early  Triassic  times.  During  the 
latter  period  it  would  seem  that  Mammals  made  their  appearance  as  small 
mouse-sized  creatures,  but  throughovit  the  entire  Mesozoic  era  they  appear  to 
have  been  sparse,  leaving  few  fossil  remains  ;  it  was  not  until  the  end  of  the 
Cretaceous  period,  75  million  years  ago,  when  the  great  carnivorous  Reptiles 
finally  died  off  that  these  retiring,  inconspicuous  creatures,  probably  nocturnal 
or  arboreal  in  habit,  were  able  to  take  the  leading  place  in  evolvitionary  progress. 
This  they  have  done  to  such  good  purpose  that  they  have  adapted  themselves 
to  and  become  completely  predominant  in  almost  every  environment  on  land, 
some  of  them  even  returning  to  the  water  wherein  their  lately  acquired  superiority 
afforded  them  a  relatively  easy  existence  (whales,  seals,  Sirenians)  while  others 
(bats)  have  invaded  the  air. 

Parallel  with  the  Therapsida  stands  the  other  reptilian  group  of  Sauropsida, 
of  which  lizards  and  snakes  are  a  direct  off-shoot  ;  from  it  was  derived  the 
Archosauria,  a  group  characterized  by  a  limb-and-girdle  structure  enabling  them 
to  run  semi-erect  upon  their  hind  legs  with  a  bipedal  gait.  The  only  members 
of  this  stock  which  have  survived  are  the  crocodiles  and  their  relatives  the 
alligators  ;  but,  particularly  in  their  most  spectacular  forms,  the  Dinosaurs, 
some  of  them  as  heavy  as  40  or  50  tons,  they  constituted  the  dominant  terrestrial 
type  during  the  latter  half  of  the  Mesozoic  era.  From  these  are  descended 
modern  Birds  which  show  innumerable  reptilian  features. 

Curiously  it  was  from  the  most  primitive  type  of  placental  Mammal,  the 
Insectivores,  that  the  Primates  and  Man  evolved,  and  in  the  evolution  of  these 
the  great  advance  has  been  associated  with  the  brain.  This  was  achieved  in  a 
peculiar  way.  A  small  and  unimportant  group  became  adapted  to  arboreal  life, 
thus  developing  their  cortical  capacity  by  the  coordination  of  the  eye  and  hand  ; 
thereafter,  descending  from  the  trees  and  freeing  their  hands  by  becoming 
bipedal,  they  passed  the  critical  point  at  which  physical  dexterity  could 
combine  with  conceptual  thought  and  the  faculty  of  speech,  and  thus  a  new 
method  of  evolution  became  possible  based  on  the  transmission  of  cultural 
experience.  At  this  stage  the  potentialities  of  vision  are  measured  not  by 
the  optical  and  structural  excellence  of  the  receptive  end-organ,  but  by  the 
apperceptive  capacity  of  the  mind.  In  this  way,  just  as  the  Mammals  defeated 
the  lower  Vertebrates  on  land,  leaving  the  water  to  the  Teleosts  and  the  air  to 
the  Birds,  so  the  Placentals  eliminated  the  Monotremes  and  Marsupials  wherever 
they  came  in  contact  with  them,  the  Carnivora  dominated  the  lower  Placentals, 
the  monkeys  the  Prosimians,  and  finally  Man  triumjihed  over  all  the  others. 

From  the  anatomical  point  of  view — and  certainly  from  the  aspect  of  the 
structure  of  the  eye — these  six  classes  of  the  Vertebrates,  neglecting  the  Cyclo- 
stomes,  can  conveniently  be  reduced  to  three  great  groups  as  suggested  by 
Huxley  : 


THE   VERTEBRATE   EYE  237 

1.  The  ICHTHYOPSIDA — Fishes  and  Amphibians,  the  primary  habitat  of 
which  is  water — completely  so  in  the  case  of  the  first  and  developmentally  so  in 
the  second.  Although  the  eyes  of  adult  Amphibians  show  many  terrestrial 
adaptations,  the  larval  stage  is  spent  in  water  and  the  adjustments  for  aerial 
vision  are  added  to  the  general  plan  of  the  aquatic  eye. 

2.  The  SAUROPSIDA — Reptiles  and  Birds  which,  despite  the  difference  in 
their  external  appearance,  show  many  close  structural  affinities.  In  them  the 
eyes  have  become  completely  adapted  to  aerial  vision. 

3.  The  MAMMALIA,  in  which  the  eye,  starting  from  a  primitive  reptilian 
source,  has  developed  along  separate  lines  adapting  itself  to  almost  every 
environmental  habitat — including  a  return  to  aquatic  vision. 

THE  PHYLOGENY  OF  THE  VERTEBRATE  EYE 

We  have  already  seen  that  the  eyes  of  Invertebrates  are  developed 
from  the  surface  ectoderm  and  that  the  visual  cells  are  connected  to 
the  nervous  system  secondarily  ;  the  eyes  of  Vertebrates,  on  the  other 
hand,  arise  from  the  neural  ectoderm.  It  is  true  that  the  neural 
ectoderm  itself  is  ultimately  derived  as  an  infolding  from  the  surface 
layer,  but  the  cerebral  eye  of  Vertebrates  indicates  a  major  evolu- 
tionary step  affording  the  sentient  layer  of  cells  all  the  opportunities 
for  the  pluripotential  differentiation  characteristic  of  the  central 
nervous  system  of  which  in  every  sense  it  forms  an  integral  part.  An 
apparatus  capable  of  subserving  a  highly  developed  sense  of  vision 
depends  no  less  on  the  efficiency  of  its  central  nervous  representation 
which  interprets  its  images  than  on  the  peripheral  sensory  apparatus 
which  receives  and  resolves  them.  Moreover,  an  endoneural  receptor 
immune  because  of  its  position  to  other  stimuli,  mechanical  or 
chemical,  can  evolve  a  delicacy  of  response  without  danger  of  false 
alarms  that  could  not  be  attained  by  an  organ  exposed  on  the  surface. 
The  significance  of  the  origin  of  the  vertebrate  eye  is  thus  apparent  ; 
the  process  is  essentially  the  same  as  in  Invertebrates,  both  the  eye  and 
the  central  nervous  system  being  ectodermal,  but  in  the  latter  the  eye 
has  evolved  from  the  surface  ectoderm  primarily,  in  Vertebrates  it  is 
secondarily  derived.^ 

The  curious  thing,  however,  about  the  evolution  of  the  vertebrate 
eye  is  the  apparent  suddenness  of  its  appearance  and  the  elaboration  of 
its  structures  in  its  earliest  known  stages.  There  is  no  long  evolutionary 
story  as  we  have  seen  among  invertebrate  eyes  whereby  an  intracellular 
organelle  passes  into  a  unicellular  and  then  a  multicellular  eye,  attaining 
by  trial  and  error  along  different  routes  an  ever-increasing  degree  of 
complexity.  Within  the  vertebrate  phylum  the  eye  shows  no  progress 
of  increasing  differentiation  and  perfection  as  is  seen  in  the  brain,  the 

^  It  is  to  be  noted  that  the  sensory  cells  in  the  epidermis  of  the  tail  of  the  ammocoete 
larva  of  the  lamprey  are  probably  light-sensitive  (Steven,  1950-51)  ;  they  resemble 
the  apolar  light  cells  seen  in  some  worms  (Lumbricu.s)  and  molhiscs  (Mya)  (p.  l.*^!). 
This  is  the  only  instance  of  the  occurrence  among  Vertebrates  of  the  primitive  light 
cells  characteristic  of  Invertebrates,  and  is  analogous  (perhaps)  with  the  cells  of  Joseph 
seen  in  the  integument  of  Amphioxus  (p.  229). 


238  THE   EYE   IN  EVOLUTION 

ear,  the  heart  and  most  other  organs.  In  its  essentials  the  eye  of  a 
fish  is  as  complex  and  fully  developed  as  that  of  a  bird  or  man  ;  the 
differences  between  the  members  of  the  series  are  relatively  minor 
in  character,  adaptations  to  the  habits  of  the  animals  rather  than 
expressions  of  phylogenetic  evolution.  All  Vertebrates  have  a  three- 
layered  retina  and  a  pigmentary  epith&lium,  all  have  the  same  dioptric 
apparatus  of  a  cornea  and  an  epithelial  lens,  all  have  the  same  nutrient 
mechanism.  It  is  true  that  the  essential  visual  components  except  the 
three-layered  retina  are  found  in  many  invertebrate  eyes ;  but  at  the  same 
time  it  is  to  be  remembered  that  the  optic  ganglion  of  the  latter  group 
corresponds  essentially  to  the  nervous  layers  of  the  retina  of  Verte- 
brates. Despite  these  similarities,  however,  a  revolution  has  taken 
place. 

Throughout  the  whole  phylum  paired  lateral  eyes  are  present, 
although  occasionally,  as  in  specialized  predators  such  as  the  hagfish, 
Myxine,  or  in  cave-dwelling  or  abyssal  fishes,  subterranean  amphibians 
and  reptiles  and  the  mole,  they  may  degenerate.^  In  the  most  primi- 
tive vertebrates  known  to  man — the  long  extinct  agnathous  fishes 
{Pteraspis,  Cephalaspis,  etc.)  the  fossil  remnants  of  which  are  found  in 
the  rocks  of  the  Silurian  era  ^ — a  median  and  two  lateral  eyes  were 
present.  In  the  extant  representatives  of  this  primitive  stock,  the 
lampreys  (Petromyzon),  the  lateral  eyes  are  rudimentary  and  hidden  in 
the  arnmocoete  (larval)  stage  ;  but  in  the  adult  they  become  well- 
developed  and  reach  the  surface  (Figs.  276-7),  while  the  animal  is  also 
provided  with  median  pineal  and  parietal  "  eyes  ".^  Although 
primitive,  however,  and  lacking  the  diagnostic  characteristics  of  true 
fishes,  the  lateral  eyes  of  this  most  primitive  type  emerge  as  fully 
differentiated  organs  and  shed  little  light  on  the  origin  of  the  eyes  of 
the  higher  species.  It  would  seem,  therefore,  that  the  vertebrate  eye 
evolved  not  as  a  late  off-shoot  from  the  simple  eye  of  Invertebrates 
after  the  latter  had  reached  an  advanced  stage  ;  it  probably  emerged 
at  a  very  early  stage,  further  back  than  geological  evidence  can  take  us, 
and  developed  along  parallel  but  diverging  lines.  The  apposite  remark 
of  the  great  German  anatomist,  Froriep  (1906),  that  the  vertebrate  eye 
sprang  into  existence  fully-formed,  like  Athene  from  the  forehead  of 
Zeus,  expressed  the  frustration  of  the  scientists  of  half  a  century  ago 
to  account  for  its  appearance  ;   today  we  are  little  wiser. 

The  apparently  revolutionary  changes  in  morphology  which 
characterize  Vertebrates  are  not,  of  course,  confined  to  the  eyes.  The 
abruptness  of  the  separation  between  the  backboned  and  backboneless 
animals  -Aab  evident  to  Aristotle  and  was  firmly  drawn  by  Lamarck 
in  1801),  but  the  pedigree  of  the  former — presumably  from  the  latter — 
still  ren!  V  '^s  unknown  and  all  the  theories  which  have  been  advanced 
^  p.  72i.  2  320  to  350  million  years  ago,  p.  754.  *  p.  713. 


THE   VERTEBRATE   EYE  239 

are  suggestive  rather  than  convincing.  Moreover,  in  the  case  of  a  soft 
organ  any  help  from  fossil  types  is  lacking.  We  are  therefore  driven  to 
seek  what  evidence  we  can  from  ontogeny. 

Froriep.     Hb.  d.  vergl.  u.  exper.  Entwick-      Romer.     Vertebrate  Paleontology,  Chicago 
lungslehre     d.     Wirbeltiere,     Jena,     2  (1947). 


(1906). 


Steven.    J.  exp.  Biol.,  27,  350  (1950). 
Quart.  J.  micr.  Sci.,  92,  233  (1951). 


Anat.  Anz.  (buppL),  29,  145  (1906).  Trewavas,  White,  Marshall   and   Tucker. 

Lamarck.     Zoological  Philosophy  (1809).  Nature  (Lond.),  176,  126  (1955). 

THE  ONTOGENY  OF  THE  VERTEBEATE  EYE 

Ontogenetically,  the  central  nervous  system  first  appears  as  a 
superficial  groove  along  the  mid-dorsal  line  of  the  embryo  which 
eventually  invaginates,i  the  anterior  part  to  form  the  anlage  of  the 
brain,  the  remaining  and  greater  part  to  form  the  spinal  cord.  At  an 
early  stage  before  the  closing-in  process  occurs,  the  anterior  cephalic 
end  grows  more  rapidly  than  the  rest  and  forms  three  primary  vesicles,  ^ 
and  at  the  cephalic  end  of  the  rudiment  of  the  forebrain,  tucked  into  a 
recess  at  each  corner,  a  paired  lateral  depression  appears,  known  as  the 
optic  pits  {foveolce  opticce).  These  paired  pits,  lying  on  the  surface  of 
the  open  cephalic  plate,  have  been  seen  on  the  surface  of  many  types  of 
embryos  in  some  of  which  they  are  pigmented  (Froriep,  1906  ;  Lange, 
1908  ;  Franz,  1934  ;  and  others)  (Figs.  242  to  247).  As  the  neural 
groove  invaginates  to  become  the  neural  tube,  the  optic  pits  become 
invaginated  with  it  to  form  the  primary  optic  vesicles,  which,  reaching 
the  surface  as  lateral  out-pouchings  of  the  cerebral  vesicles,  again 
invaginate  to  form  the  secondary  optic  vesicles  (or  optic  cups). 

In  all  Vertebrates  the  retina  participates  in  the  high  degree  of 
differentiation  which  characterizes  the  central  nervous  system.  The 
proximal  wall  of  the  optic  cup  remains  as  a  unicellular  layer  and 
acquires  pigment  to  form  the  pigmentary  epithelium,  but  its  inherent 
plasticity  is  seen  in  the  capacity  of  the  amphibian  epithelium  to  regener- 
ate an  entirely  new  functional  retina  if  the  inner  layer  is  removed 
(Stone,  1950).  The  neuro-epithelium  which  forms  the  distal  layer 
of  the  cup,  like  that  which  determines  the  cerebral  and  cerebellar 
cortex,  differentiates  into  three  strata — a  marginal  zone  of  ganglion 
cells,  an  intermediate  mantle  zone  (bipolar,  amacrine,  horizontal  and 

^  The  fact  that  the  nerve-cord  in  Amphioxus  first  appears  as  a  solid  rod  which 
canalizes  at  a  later  stage  has  suggested  to  some  authorities  that  this  sequence 
represents  a  phylogenetic  step  in  the  evolution  of  the  central  nervous  system  of  Verte- 
brates ;  but  it  is  to  be  remembered  that  the  evidence  indicates  that  the  Lancelets  are 
an  off-shoot  of  the  main  vertebrate  stock  rather  than  a  primitive  type.  It  is  also  to 
be  noted  that  Graham  Kerr  (1919)  described  the  forebrain  of  Lepidosiren  and  other 
fishes  as  developing  in  the  form  of  a  solid  rod  from  which  the  optic  vesicles  grew  as 
solid  buds  to  become  canalized  later.  This,  however,  is  probably  merely  a  question 
of  the  timing  of  various  stages  of  development  ;  and  no  dogmatic  judgment  on  this 
question  can  vet  be  given. 

2  p.  532.' 


240 


THE   EYE   IN   EVOLUTION 


Figs.    242    to    247. — The    Ontogenetic    Development    of   the    Lateral 

EYE    of    VeBTEBRATES. 


Fig.  242. 


Fig.  243. 


Fig.   244. 


Fig.  245. 


Fig.  246. 


Fig.  242. — The  appearance  of  the  foveolae  opticse  ( / )  on  the  dorsal 
ectoderm  of  the  cephahc  (medullary)  plate  {m.p.). 

Fig.  243. — Invagmation  of  the  surface  ectoderm  with  the  optical  area 
to  form  the  primitive  neural  tube. 

Fig.  244. — Evagination  of  the  primary  optic  vesicle. 

Fig.  245. — The  commencement  of  secondary  invagination  of  the  neural 
epithelium  with  thickening  of  the  surface  epithelium. 

Fig.  246. — Invagination  of  the  surface  epithelium. 

Fig.  247. — Detachment  of  the  lens  from  the  surface  epithelium. 


Miiller's  cells)  and  an  outer  zone  of  sensory  cells,  perhaps  the  linear 
descendants  of  the  ependymal  cells  (rods  and  cones).  In  this  way  the 
strati  I-! cation  of  cells  with  their  accompanying  system  of  interconnecting 
neurones  allows  the  appearance  of  a  complex  conducting  and  associating 
appara   's.     With  very  few  exceptions  the  retina  of  Invertebrates  is 


THE   VERTEBRATE   EYE  241 

formed  by  a  single  ectodermal  layer  ;  but  into  the  retina  of  Vertebrates 
is  thus  aggregated  the  analogue  of  the  ojitic  ganglion  of  Invertebrates  ; 
it  becomes  an  island  of  the  central  nervous  system,  and  the  optic  nerve 
becomes  a  tract  of  this  system  connecting  the  outlying  part  with  the 
main  body. 

In  the  vast  majority  of  cases  we  have  seen  that  the  receptor  end 
of  the  sensory  cell  in  the  epithelial  eye  of  the  Invertebrate  lay  towards 
the  surface  of  the  body/  but  when  it  was  enfolded  in  the  neural  tube 
of  the  Vertebrate,  this  end  now  lay  deeply  and  the  pole  from  which  the 
nerve  fibre  issues  became  superficial  (Fig.  247).  It  follows  that  in  the 
cerebral  eye  of  the  Vertebrate,  light  must  traverse  the  whole  thickness 
of  the  retina  in  order  to  reach  the  sentient  layer  ;  such  an  arrangement 
we  have  already  called  an  inverted  retina  in  contradistinction  to  the 
more  primitive  verted  retina  wherein  light  first  strikes  the  visual 
cells  before  reaching  their  nervous  prolongations.^  The  inverted  retina 
may  seem  an  anomalous  arrangement  from  an  optical  point  of  view, 
but  it  carries  the  advantage  that  the  visual  receptors  can  be  brought 
into  contact  with  the  pigment  and  that  the  part  of  the  retina  in  which 
the  greatest  activity  occurs  lies  nearest  the  caj)illaries  of  the  choroid  ; 
both  of  these — pigment  and  a  dense  layer  of  blood-vessels^ — for  optical 
reasons  could  only  be  situated  deeply  to  the  visual  elements.  More- 
over, an  inverted  arrangement  allows  the  evolution  of  intracellular 
colour  filters  within  the  visual  cells  (Walls  and  Judd,  1933)  and  permits 
an  increase  of  the  resolving  power  of  the  central  region  by  the  formation 
of  a  fovea  (Walls,  1937). 

The  remainder  of  the  eye  is  derived  from  the  surrounding  ecto- 
dermal and  mesodermal  tissues.  The  surface  ectoderm  devotes  itself 
entirely  to  the  formation  of  the  dioptric  apjDaratus.  an  arrangement 
which  allows  greater  efficiency  than  was  the  case  in  Invertebrates  in 
which  a  refringent  mechanism  was  developed  from  the  same  layer  as  the 
sentient  cells  themselves.  Intercalary  cells  in  the  sentient  layer, 
however,  retain  this  function  to  some  extent  by  secreting  a  transparent 
medium  (the  vitreous).  Organs  of  protection  are  provided  from  the 
surrounding  mesodermal  tissues — a  fibrous  sclerotic  coat,  lids,  a 
lacrimal  apparatus,  and  a  bony  orbit  ;  and  from  the  same  source  a 
motor  apparatus  is  added,  and  a  vascular  system  provided. 

Franz.       Bolk's    Hb.    d.    vergl.    Anat.    d.  Lange.      Zbl.  prnkf.  Angeuheilk.,  32,    131 

Wirbeltiere,  Berlin,  2  (ii),  989  (1934).  (1908). 

Froriep.     Hb.  d.  vergl.  u.  e.rper.  Entwick-  Stone.     Anat.  Fee,  106,  89  (1950). 

lungslehre     d.     Wirbeltiere,     Jena,     2  Walls.     Arch.  Ophthal.  (Chicago),  18,  912 

(1906).  (1937). 

.4no?.  ^nz.  (Snppl.),  29,  145  (1906).  Walls  and  Judd.      Brit.  J.   Ophthal.,   17, 

Kerr,  Graham.      Te.rtbook  of  Embryology.  641,  705  (1933). 

London  (1919). 

1  p.  146,  2  p.  146. 

S.O.— VOL.  I.  IG 


242  THE   EYE   IN   EVOLUTION 

THE    EMERGENCE    OF    THE    VERTEBRATE    EYE 

Since  Wilhelm  Miiller  (1875)  first  put  forward  his  view  that  the 
pigment-spot  in  Amphioxus  represented  the  forerunner  of  the  vertebrate 
eye,  many  hypotheses  have  been  advanced  to  explain  its  sudden  and 
pecuhar  appearance,  but  even  today  no  theory  can  be  said  to  be 
completely  convincing  and  each  raises  difficulties  in  interpretation. 
These  theories  we  shall  now  briefly  discuss. 

Ray  Lankester  (1880-90)  was  among  the  first  to  appreciate  the 
importance  of  the  cerebral  origin  of  the  vertebrate  eye  and  reasoned 
that,  with  the  visual  cells  buried  in  the  central  nervous  system,  the 
original  pelagic  pre -vertebrate  must  have  been  transparent,  as  indeed 
are  Ascidians  and  Lancelets,  so  that  the  light  could  traverse  their 
bodies.  As  the  body  became  opaque  the  eye  was  then  forced  to  travel 
nearer  and  nearer  to  the  surface  until  eventually  it  became  separated 
from  it  only  by  a  layer  of  ectoderm  which  retained  its  primitive 
transparency.  In  this  view  the  light-sensitive  cells  originally  associated 
with  the  medullary  tube  migrated  to  the  surface  bringing  with  them 
their  associated  pigment  cells,  and  were  multiplied  and  differentiated 
to  form  the  retina  ;  meantime,  the  surface  epithelium  in  the  correspond- 
ing area  remained  transparent  and  ultimately  became  differentiated  to 
form  the  dioptric  apparatus  (cornea  and  lens). 

This  view  seemed  a  reasonable  explanation  of  the  phenomenon  and 
was  crystallized  by  Balfour  (1881)  who  pointed  out  that  although  the 
retina  appeared  to  derive  from  the  brain  it  did  not  originate  there  but, 
like  the  photoreceptors  of  Invertebrates,  was  really  of  integumentary 
origin,  appearing  initially  as  patches  of  photosensory  epithelium  on  the 
area  of  the  dorsal  ectoderm  which  happened  to  become  involuted  with 
the  neural  tube  (Figs.  248  to  254).  Such  a  theory  accounted  for  the 
inversion  of  the  retina  as  well  as  its  cerebral  origin — a  characteristic 
unique  among  vertebrate  sense  organs.  The  concept  that  the  vertebrate 
eye  ultimately  derives  from  the  skin  was  supported  by  a  number  of  in- 
vestigators,^ while  Schimkewitsch  (1921)  carried  the  theory  further  by 
suggesting  that  the  lateral  eyes  were  merely  a  pair  of  a  series  of  homo- 
logous pit-like  sense  organs,  the  more  anterior  of  which  Were  photo- 
sensory,  a  series  in  which  were  included  other  evaginations  of  the  roof  of 
the  diencephalon  such  as  the  pineal  and  parietal  eyes.  In  these  latter  eyes 
there  is  no  secondary  invagination  so  that  a  verted  retina  is  formed ;  and 
Sleggs  (1926)  and  Estable  (1927)  explained  the  secondary  invagination 
of  the  optic  vesicles  as  a  positive  evolutionary  step  taken  in  order  that 
abundant  nourishment  might  be  available  from  the  choroid  to  allow  a 
high  degree  of  differentiation  and  activity  in  the  sensory  mechanism. ^ 

1  von  Kennel  (1881),  Dohrn  (1885),  Keibel  (1906),  Froriep  (1906),  Lange  (1908), 
Franz  (!  ']  •-),  and  others. 


THE   VERTEBRATE   EYE 

The  origin  of  the  essential  sensory  cells,  the  rods  and  cones,  has 
long  remained  a  matter  of  dispute.  Ever  since  the  time  of  Scliwalbe 
(1874)  they  had  been  generally  considered  as  neuro-epithelium. 
Kraiise  (1875),  however,  originally  put  forward  the  suggestion  that  they 

Figs.  248  to  254. — Hypothetical  Scheme  fob  the  Phylogenetic 
Development  of  Vertebrate  Eyes. 


243 


Fig.  248. 


Fig.  252 


Fig.   249. 


Fig.   253. 


Fig.   250. 


Fig.  251. 


Fig.  254. 


Fig.   248. — Photosensitive  ciliated  ectoderm  on  the  dorsal  aspect. 

Figs.  249  and  250. — Invagination  of  the  surface  ectoderm  to  form  the 
neural  tube,  carrying  with  it  the  photosensitive  ectoderm. 

Fig.  251. — The  formation  of  the  neural  tube  enclosing  the  photosensitive 
epithelium  as  ependyma. 

Fig.   252. — Commencing  evagination  of  the  neural  tube. 

Fig.   253. — The  formation  of  one  median  and  two  lateral  optic  vesicles. 

Fig.  254. — Invagination  of  the  surface  ectoderm  with  secondary  in- 
vagination of  the  lateral  optic  vesicles  to  form  two  lateral  eyes  with  inverted 
retinse.  The  surface  epithelium  takes  no  part  in  the  development  of  the 
median  eye  which  forms  its  own  dioptric  apparatus  (lens)  in  the  distal  part 
of  the  vesicle  which  itself  does  not  undergo  secondary  invagination  and  thus 
forms  a  verted  retina. 


were  derived  from  the  ciliated  ependymal  cells  lining  the  neural  tube, 
the  cilia  eventually  forming  the  outer  segments  of  the  visual  cells — 
a  view,  however,  which  he  quickly  withdrew  (1876).  The  vast 
authority  of  these  two  pioneers  in  the  histology  of  the  visual  organs 
long  remained  unchallenged,  but  t  he  view  that  this  layer  of  cells  might 


244 


THE    EYE   IN  EVOLUTION 


be  ependymal  in  origin,  the  receptor  end  being  phylogenetically 
homologous  with  the  single  cilium  of  an  ependymal  cell,  was  revived  by 
Leboucq  (1909),  a  theory  which  was  elaborated  with  great  persuasive- 
ness by  Studnicka  (1912-18),  and  subsequently  supported  by  Walls 
(1939)  and  Willmer  (1953).  In  this  view  the  phylogenetic  homologue 
of  the  vertebrate  retina  may  be  assumed  to  be  the  infundibular  organ 
of  Amphioxus  ^  ;  but  it  must  be  remembered  that  any  convincing 
phylogenetic  sequence  connecting  the  two  is  lacking. 


Figs.  25.5  to  258. — Boveri's  Conception  of  the  Development  of  the 
Vertebrate  Eye  from  the  Organs  of  Hesse  of  an  Amphioxus- 
LiKE  Ancestor. 


Fig.  255. — Symmetrical  arrangement 
of  the  organs  of  Hesse  with  pigment 
cells  facing  the  central  canal. 


Fig.    256. — Evagination    of  the  canal 
carrying  with  it  the  organs  of  Hesse. 


Fig.    257. — Invagination    to    form    a 
sensory  and  pigmented  layer. 


Fig.  258. — Secondary  invagination  of 
the  lens  vesicle  (from  Walls,  after 
Boveri). 


Such  a  development  would  not  be  unique  since  modified  flagellated  cells  of 
this  type  are  also  seen  in  other  sensory  organs  such  as  the  olfactory  cells,  the 
hair  cells  of  the  labyrinth,  the  cells  of  the  taste-buds  and  lateral  line  organs  ;  and 
it  is  to  be  remembered  that  there  is  a  considerable  amount  of  evidence  that  the 
ependymal  cells  in  the  diencephalic  region  retain  some  photosensory  properties 
in  several  species  of  Vertebrates  -  (von  Frisch,  1911  ;  Scharrer,  1928  ;  Nowikoff, 
1934  ;  Young,  1935  ;   Benoit,  1937  ;   and  others). 

Agreement  on  the  ependymal  origin  of  the  visual  receptors  is, 
however,  by  no  means  universal  and  many  investigators,  following 
Schwalbe,  believe  that  they  are  endoneural.  Thus  Boveri  (1904)  traced 
their  origin  from  the  ganglion-like  cells  of  Hesse  in  an  Amphioxus-hke 
ancestors  In  this  view  he  was  supported  by  Parker  (1908-9), 
1  p.  229.  2  p.  537.  3  p^  230. 


THE   VERTEBRATE   EYE 


245 


Tretjakoff  (1913),  Hescheler  and  Boveri  (1923)  and  Nowikoff  (1932).  It 
was  assumed  that  these  cells  became  orientated  in  a  regular  manner 
with  their  associated  pigment  cells  towards  the  central  canal,  and  then 
were  carried  towards  the  skin  in  company  with  paired  lateral  diverticuli 
of  the  neural  tube  (Figs.  255  to  258).  It  is  to  be  noted  that  by  this 
hypothesis  the  inversion  of  the  retina  and  the  position  of  the  pigmentary 
epithelium  are  also  well  explained.  Although  objections  have  been 
raised  to  this  conception,  such  as  the  lack  of  ontogenetic  and  phylo- 
gent^l-  confirmation  of  any  intermediate  stages  of  the  migration,  the 


Figs.   259  to   262. 


-Froriep's  Derivation  of  the  Ascidian   (and  Verte- 
brate) Eye. 


Fig.   259. 


Fig.   260. 


Fig.  261. 


Fig.  259. — The  hypothetical  original  exi.stence  of  two  sensory  vesicles 
with  an  external  lens  and  verted  retina. 

Fig.  260. — Involution  of  the  neural  tube  showing  a  lens  facing  the  neural 
canal  and  a  verted  retina. 

Figs.  261  and  262. — Degeneration  of  one  eye  of  the  original  pair  and 
migration  of  the  lens  to  an  external  position.  For  siinijlicitj-  the  statocyst 
portion  of  the  sensory  vesicle  is  omitted. 


absence  of  Hesse's  cells  in  the  head-end  of  Amphioxus  and  the  danger 
of  phylogenetic  deduction  from  a  species  which  appears  to  be  an  off- 
shoot rather  than  a  primitive  t\^e,  the  theory  is  undoubtedly  ingenious. 
On  the  other  hand,  a  phylogenetic  analogy  with  the  vesicular  eye 
of  the  ascidian  tadpole  ^  was  suggested  by  Lankester  (1880)  and 
strongly  advocated  by  Jelgersma  (1906).  Such  an  ascidian  hypo- 
thesis had  to  meet  the  criticism  that  this  eye  is  unpaired  while  the 
presence  of  a  lens  situated  on  the  cerebral  aspect  of  the  retina  is 
obviously  an  anomaly  (Fig.  235).  Froriep  (1906),  however,  suggested 
that  the  first  difficulty  could  be  overcome  if  the  apparently  unpaired 
eye  in  reality  represented  one  of  a  pair  ;  in  support  of  his  hy|3othesis 
he  showed  that  it  was  situated  asymmetrically  towards  the  right  and 
was  balanced  by  a  degenerate  mass  on  the  left  which  he  interpreted  as  a 

1  p.  228. 


246  THE   EYE   IN   EVOLUTION 

vestigial  eye.  He  attempted  to  overcome  the  second  difficulty  by 
postulating  a  migration  of  the  lens  from  the  cerebral  to  the  superficial 
aspect  of  the  vesicle  ;  his  conception  of  the  evolution  of  the  organ  is 
seen  in  Figs.  259  to  262.  If  the  vertebrate  eye  stems  from  an  ascidian- 
like  ancestor  in  this  way,  the  formation  of  the  tubular  neural  structure 
precedes  sensory  differentiation,  and  any  superficial  sensory  organ  asso- 
ciated with  the  surface  ectoderm  must  be  assumed  to  disappear  and  be  re- 
placed by  the  establishment  of  a  neural  photosensory  organ.  Why  the  dor- 
sal and  lateral  areas  of  the  neural  tube  should  show  this  photosensitive 
differentiation  raises  a  difficult  problem  ;  as  occurs  in  many  Inverte- 
brates, the  tendency  may  be  associated  with  orientation  to  light  coming 
from  above,  the  paired  lateral  areas  being  evolved  primarily  in  relation 
to  orientation  in  the  horizontal  plane.  The  analogy,  however,  is  by  no 
means  proved  or  even  clear,  and  the  danger  of  phylogenetic  deductions 
in  such  a  case  is  obvious  ^  ;  in  Froriep's  (1906)  view  a  common  ancestry 
is  more  probable  than  a  sequential  derivation. 

A  further  hypothesis,  the  placode  theory,  usvially  credited  to  von  Kvipffer 
(1894),  was  suggested  by  Nuel  (1887)  and  supported  by  Beraneck  (1890), 
Burckhardt  (1902)  and  Lubosch  (1909).  It  postulated  the  development  of 
ectodermal  placodes  homologous  with  the  lateral  line  organs  from  the  anterior 
members  of  which  the  olfactory  organs,  the  membranous  labyrinth  of  the  ear  and 
the  Jens  of  the  lateral  eyes  were  developed.  The  lens  was  originally  vesicular 
and  was  considered  to  form  an  eye  with  a  verted  retina  ;  the  definitive  retina 
emerged  from  the  central  nervous  system  to  act  as  its  optic  ganglion,  homologous 
with  a  spinal  ganglion,  and  eventually  as  phylogenetic  evolution  proceeded, 
took  over  the  sensory  function  of  the  lens  which  degenerated  into  a  dioptric 
accessory.  This  theory,  however,  has  long  been  in  disrepute  since  no  evidence, 
ontogenetic  or  phylogenetic,  connects  a  non-sensory  retina  with  a  sensory  lens. 

The  origin  of  the  lens^ — the  other  major  factor  in  the  development 
of  the  vertebrate  eye — has  also  given  rise  to  speculation.  The 
homologous  position  of  the  olfactory  and  otic  anlages  suggested  first  to 
Sharp  (1885)  that  this  structure  arose  from  an  ectodermal  placode  and 
was  in  its  own  right  a  sensory  structure.  Without  attributing  photo- 
sensitive properties  to  its  cells  as  called  for  in  the  preceding  theory  of 
retinal  development,  several  investigators  have  been  attracted  to  the 
view  that  the  lens  is  an  independent  organ  derived  from  an  anterior 
placode  of  the  epibranchial  series  (Jelgersma,  1906  ;  Studnicka,  1918  ; 
Schimkewitsch,  1921).  The  evidence  of  experimental  embryology  is 
conflicting.  Many  experimenters  have  established  that  the  presence 
of  the  optic  vesicle  is  necessary  for  the  development  of  the  lens,  and 
some  liave  claimed  that  this  structure  alone  is  sufficient  for  its  deter- 
mination so  that  a  lens  will  form  from  undifferentiated  ectoderm  at  an 
abnormal  site  if  the  optic  cup  is  transplanted  thereto.     Others  have 

1  Seo  -vritings  of  Balfour  (1878-81),  Metcalf  (1906),  Keibel  (1906),  Buxton 

(1912),  Bti  ;  921),  and  others. 


THE   VERTEBRATE   EYE 


247 


found  that  a  lens  may  partially  or  completely  develop  if  the  retinal 
anlage  has  been  removed  from  the  optic  plate  at  an  early  stage  or  in 
anencephalic  monsters.^  It  may  well  be  that  there  is  some  tendency 
for  the  formation  of  a  lens  inherent  in  the  ectoderm  of  the  region  where 
it  is  normally  found  ;  but  on  the  whole,  in  the  present  stage  of  our 
knowledge,  the  evidence  would  seem  to  suggest  that  this  structure  is 
secondarily  formed,  called  into  existence  normally  by  two  mutually 
reinforcing  inductors — the  cells  of  the  optic  vesicle  and  the  mesoderm 
of  the  head — although  in  certain  experimental  conditions  no  further 
stimulus  beyond  that  provided  by  the  latter  may  be  necessary  (Twitty, 
1930-55  ;   Woerdeman,  1950  ;   Liedke,  1951). 

It  would  seem,  therefore,  that  despite  the  considerable  amount  of 
thought  expended  on  the  question,  the  emergence  of  the  vertebrate  eye 
with  its  inverted  retina  of  neural  origm  and  its  elaborate  dioptric 
mechanism  derived  from  the  surface  ectoderm,  is  a  problem  as  yet 
unsolved.  Indeed,  appearing  as  it  does  fully  formed  in  the  most 
primitive  species  extant  today,  and  in  the  absence  of  transition  forms 
with  which  it  can  be  associated  unless  by  speculative  hypotheses  with 
little  factual  foundation,  there  seems  little  likelihood  of  finding  a 
satisfying  and  pragmatic  solution  to  the  puzzle  presented  by  its 
evolutionary  development. 


Balfour.     J.  Anat.   Physiol.,  9,   128,  408 

(1878). 
A  Treatise  on  Comparative  Embryology, 

London  (1881). 
Beckwith.    J.  e.rp.  ZooL,  49,  217  (1927). 
Benoit.     Bull.  Biol.  France  Belgique,  71, 

393  (1937). 
Beraneck.     Arch.  Sci.  phys.  nat.,  Geneve, 

24,  361  (1890). 
Boveri.     Zool.  Jb.,  Suppl.  7,  409  (1904). 
Biitschli.       Vorlesiingen    it.    vergl.    Anat., 

Berlin  (1921). 
Burckhardt.        Verh.     int.     Zoologencotig. 

(1901),  621  (1902). 
Buxton.      Arch,    vergl.    Ophthal.,    2,    405 

(1912). 
Choi.     Folia  anat.  japon.,  10,  29  (1932). 
Dohrn.     Mitt.   zool.  Stat.  J^eajoel,   6,   432 

(1885). 
Estable.     Ayx.  Inst.  Neurol.,  Montevideo, 

1,  328  (1927). 
Franz.      Bolk's      Hb.    d.    vergl.    Anat.    d. 

Wirbeltiere,  Berlin,  2  (ii),  989  (1934). 
von  Frisch.     Pfli'igers  Arch.  ges.  Physiol., 

138,  319  (1911). 
Froriep.  Hertwig'a  Handbnch  d.  vergl.  und 

exper.    Entwicklungslehre    d.     Wirbel- 
tiere, Jena,  2  (1906). 
Anat.  Anz.  29,  145  (1906). 
Hagedoorn.    Arch.  Ophthal.  (Chicago),  16, 

783  (1936). 


Hescheler    and    Boveri.      Vjschr.    naturf. 

Ges.  Zurich,  68,  398  (1923). 
Jelgersma.    Morphol.  Jb.,  35,  377  (1906). 
Keibel.     Klin.  Mbl.  Augenheilk.,  44   (2), 

112  (1906). 
von  Kennel.    Diss.,  Dorpat  (1881). 
Krause,   W.     Arch.   mikr.  Anat.,   11,   216 

(1875)  ;    12,  742  (1876). 
von  Kupffer.     Studien  zur  vergl.  Entwick- 

lungsgeschichte  d.  Kopfes  d.  Kranioten : 

II.    Die    Entwicklung    d.    Kopfes    v. 

Ammocoetes  planeri,  Munich  (1894). 
Lange.     Zbl.  prakt.  Augenheilk.,  32,   131 

(1908). 
Lankester.       Darwinisyn     and     Partheno- 
genesis, London  (1880). 
Quart.  .J.  micr.  Sci.,  31,  445  (1890). 
Leboucq.       Arch.    Anat.     micr.,    10,    555 

(1909). 
Leplat.    C.  B.  Ass.  Anat.,  17,  194  (1922). 
Lewis.     At)ier.  J.  Anat.,  3,  505  (1904). 
Liedke.    J.  exp.  Zool.,  117,  573  (1951). 
Lubosch.    Morphol.  Jb.,  39,  146  (1909). 
Mangold.    Ergebn.  Biol.,  7,  193  (1931). 
Metcalf.    .4/ia^  .4h;.,  29,  526  (1906). 
Miiller,  W.     Beit,  zur  Anat.  unci  Physiol. 

{Festgabe    C.     Eudwig),     Leipzig,     2 

(1875). 
Nowikoff.    .4cac/.    Tcheque   d.   Sci.,    Bull. 

internat.  Clin.  d.  Sci.  math.,  nat.  med., 

33,  131  (1932). 


»  See  Lewis  (1904),  Keibel,  (1906),  Srockard  (1910),  Spemann  (1912),  Leplat  (1923), 
Beckwith  (1927),  Mangold  (1931),  Choi    1932),  Waddington  and  Cohen  (1936). 


248 


THE   EYE   IN   EVOLUTION 


Nowikoff.  Biol.  Zbl.,  52,  548  (1932). 

Z.  Morphol.  Oekol.  Tiere,  29,  374  (1934). 
Nuel.    Arch.  Biol.,  Gand,  7,  389  (1887). 
Parker.    Amer.  Nat.,  42,  601  (1908). 

Amer.  J.  Physiol.,  25,  77  (1909). 
Scharrer.     Z.  vergl.  Physiol.,  7,  1  (1928). 
Schimkewitsch.     Lehrbuch  d.  vergl.  Anat. 

d.  WirbeUiere,  Stuttgart  (1921). 
Schwalbe.     Graefe-Saemisch  Handbuch  d. 
ges.  Augenhk.,  Leipzig,  1,  398  (1874). 
Sharp.     Proc.  Acad.  Nat.  Sci.  (Phila.),  300 

(1885). 
Sleggs.    Amer.  Nat.,  60,  560  (1926). 
Spemann.     Zool.  Jb.,  Abt.  Zool.  Physiol., 


32,  1  (1912). 
Stockard.     Avier.  J. 
(1910). 


Anat.,  10,  369,  393 


Studnicka.     Anat.  Anz.,  41,  561   (1912); 

44,  273  (1913). 
Zool.  Jb.,  Abt.  Anat.,  40,  1  (1918). 
Tretjakoff.    Z.  wiss.  Zool.,  105,  537  (1913). 
Twitty.     J.    exp.     Zool.,    55,    43    (1930). 

In   Analysis   of  Development.   Phila., 

p.  404  (1955). 
Waddington  and  Cohen.    J .  exp.  Biol.,  13, 

219  (1936). 
Walls.     Arch.  Ophthal.  (Chicago),  22,  452 

(1939). 
Willmer.    Symposia  Soc.  exp.  Biol.,  7,  377 

(1953). 
Woerdeman.     Aim.  Biol.,  26,  699  (1950)- 
Young.    J.  exp.  Biol.,  12,  254  (1935). 


THE    GENERAL    STRUCTURE    OF    THE    VERTEBRATE    EYE 

We  have  seen  that  the  eyes  of  Vertebrates  are  very  true  to  type 
and  (apart  from  a  few  degenerate  forms  ^)  consist  essentially  of  a 
retina  derived  from  neural  ectoderm,  a  lens  derived  from  the  surface 
ectoderm,  a  uvea  wit/h  a  nutritive  function,  a  protective  tunic  the 
anterior  segment  of  which  is  transparent,  and  a  dark  chamber  filled 
with  the  vitreous  body,  the  entire  organ  being  encased  in  the  orbital 
cavity  and  moved  by  a  group  of  extra-ocular  muscles.  All  the  varia- 
tions in  structure — and  they  are  marked  and  of  great  interest — seen  in 
the  major  classes  within  the  phylum  are  incidental  in  nature  and  have 
evolved  essentially  as  adaptations  to  differences  in  habitat  or  function. 

Of  all  the  ocular  tissues  the  retina  is,  of  course,  the  most  important 
and  undoubtedly  the  most  interesting.  Apart  from  the  abundance 
and  motility  of  its  pigment,  its  occasional  assumption  of  a  tapetal 
function  and  the  rare  presence  of  oil-droplets,  the  pigmented  epithelium 
shows  little  fundamental  variation.  The  retina  proper  (the  pars  optica 
retinae)  regularly  comprises  three  layers  of  cells  arranged  in  the  following 
strata  (Fig.  263)  : 


NEURONE   I 

(percipient  elements) 

NEURONE    II 

(conductive  and  associa- 
tive elements) 

NEURONE    III 

(conductive  elements) 


'1.  Layer  of  rods  and  cones. 

2.  Outer  nuclear  layer. 
>3.  Outer  plexiform  layer. 

4.  Inner  nuclear  layer  (bipolar,  horizontal 

and  amacrine  cells). 
>5.  Inner  plexiform  layer. 

6.  Ganglion  cell  layer. 

7.  Nerve  fibre  layer. 


The  sustentacular  functions  of  the  glial  cells  of  the  central  nervous 
system  are  taken  over  by  large  fibres  of  Mtiller,  the  nuclei  of  which  lie 
in  the  inner  nuclear  layer,  while  their  extremities  combine  to  form  an 

1  p.  721. 


THE   VERTEBRATE   EYE 


249 


external  limiting  membrane  between  the  rods  and  cones  and  their 
nuclei  and  an  internal  limiting  membrane  on  the  inner  surface  of  the 
nerve-fibre  layer.  Throughout  the  vertebrate  phylum  the  structure  of 
the  retina  is  remarkably  constant,  the  layers  varying  only   in  the 

M>    «=^    «ai        •   ^*  Nomina  vitrea 

^   "4i»    (^  **niqmenf  epithelium 

V    I' 


Fig.   263.— The  Humax  Retina. 

At  the  left,  the  retina  in  the  nasal  fundus  as  it  appears  after  fixation  in 
Kolmer's  fluid,  nitro-cellulose  embedding,  ]\Iallory's  trij^le  stain  or  Heiden- 
hain's  haematoxylin  and  phloxine.  At  the  right,  the  neuronic  hook-up  of  the 
retina,  with  examples  of  its  principal  elements,  as  revealed  by  the  Golgi 
methods  (  X  .500)  (Gordon  Walls,  based  largely  on  the  work  of  Polyak,  1941). 

o,  amacrine  cell  (diffuse  type)  ;  h,  bipolar  cells  of  ordinarj^  "midget" 
type;  c,  cones;  ch,  "centrifugal"  bipolar  (believed  to  conduct  outward 
through  the  retina  rather  than  inward)  ;  dh,  diffuse  bipolar  cells,  connecting 
with  many  visual  cells,  chiefly  rods  ;  g,  ganglion  cells  of  ordinary  "  midget  " 
type  ;  /;,  horizontal  cell  with  dendrites  connecting  only  with  cones,  axon  with 
both  rods  and  cones  at  some  distance;  m,  Miiller's  fibre  (forms  limiting  mem- 
branes) ;  pg,  "  parasol"  ganglion  cell  (one  of  .several  giant  types,  connecting 
with  many  bipolars)  ;    r,  rods. 

regularity  of  their  architecture  and  in  the  density  and  relative  pre- 
ponderance of  their  cellular  elements  ;  even  in  Cyclostomes  the  typical 
layering  can  be  recognized  although  the  various  elements  tend  to  be 
intermingled,  particularly  the  ganglion  cells  \\-ith  the  inner  nuclear 
layer.  These  minor  variations  which  occur  will  be  noted  in  the 
subsequent  chapters. 


250 


THE   EYE   IN   EVOLUTION 


THE  VISUAL  CELLS  Constitute  the  most  important  and  interesting 
of  the  constituent  elements  of  the  retina. i  They  have  been  divided 
into  two  types — rods  and  cones  (Figs.  264-267).  Typically  the  rod 
consists  of  an  outer  and  inner  segment,  a  nucleus  and  a  foot -piece. 
The  outer  segment,  possibly  representing  the  cilium  of  the  ancestral 


Fig.  264. 


Fig.  266. 


Figs.  264  and  265. — Typical  Rods  and 

Cones    of     the    Fbog,    Baxa    pipiess 

(Gordon  Walls). 

Fig.  264. — (a)  A  common  rod  (dark- 
adapted)  ;    (6)  a  green  rod. 

Fig.  265. — A  typical  cone  (dark- 
adapted). 

d,  oil-droplet  ;  e,  ellipsoid  ;  /,  foot- 
piece  ;  I,  external  limiting  membrane  ; 
m,  myoid  ;   n,  nucleus  ;   o,  outer  segment. 


Fig.  267. 


Figs.  266  and  267. — Typical  Rods  and 
Cones  of  Man  (after  Greeff). 

Fig.   266. — A  typical  rod. 

Fig.  267. — (a)  A  peripheral  cone  near 
the  ora  ;  (6)  a  peripheral  cone  near  the 
equator  ;    (c)  a  macular  cone. 

o,  outer  segment  ;  6,  inner  segment  ; 
c,  cell  fibre  ;  d,  cell  nucleus  ;  e,  cell  foot  ; 
/,  ellipsoid  ;    g,  myoid. 


ependymal  cell,  is  the  photosensitive  tip  of  the  cell  ;  the  inner  segment, 
possibly  representing  the  columnar  body  of  the  ependymal  cell,  has  at 
its  outer  end  an  ellipsoid  containing  mitochondria,  presumably  the 
principal  site  of  metabolic  activity,  while  its  inner  end  is  termed  the 
myoid  ....hough  it  is  by  no  means  always  contractile.     The  cone  has 

^  For  structure  of  rods  and  cones,  see  C.  Miiller  (1926),  Wislocki  and  Sidman 
(1954),  Sidman  and  Wislocki  (1954)  (histochemistry)  ;  Sjostrand  (1949-53),  de  Robertis 
(1956)  (ele(  -n-microscopy)  ;  Saxen  (1955-6)  (development)  ;  Sidman  (1957)  (phase- 
contrast  ail        fractometry). 


THE   VERTEBRATE   EYE  261 

the  same  component  parts,  the  outer  segment  being  typically  (but  not 
invariably)  conical,  the  inner  segment  typically  fatter,  shorter  and 
more  squat  than  the  corresponding  part  of  the  rod,  often  with  an  oil- 
droplet  in  the  ellipsoid,  and  sometimes  with  a  paraboloid  composed 
of  glycogen  lying  more  proximally  ;  the  nucleus  is  relatively  larger 
and  the  foot-piece  more  widely  spread.  Variations  to  this  standard 
structure  are  common,  such  as  the  presence  or  absence  of  oil-droplets, 
the  occurrence  of  double,  triple  or  even  quadruple  elements,  and  so  on  ; 
these  will  be  discussed  in  the  sections  on  systematic  anatomy. 

While  these  are  the  typical  structural  features,  however,  the 
variations  in  the  morphology  of  the  rods  and  cones  are  so  marked  as  to 
have  led  to  much  confusion  and  some  controversy  ;  some  rods  resemble 
cones  more  closely  than  some  members  of  their  owii  family,  while  the 
cones  of  a  well-developed  fovea  often  resemble  elongated  rods  more 
closely  than  typical  cones  (Fig.  267c).  Indeed,  in  our  systematic 
survey  we  shall  on  more  than  one  occasion  run  up  against  difficulties 
in  describing  particular  visual  cells  either  as  a  rod  or  a  cone. 

Schultze  (1866),  who  first  clearly  differentiated  the  two  types  of  cell,  did  so 
primarily  on  anatomical  grounds,  his  three  criteria  being — (o)  the  cylindrical 
termination  of  the  rods  in  contrast  to  the  conical  tip  of  the  cones,  (b)  the  more 
external  position  of  the  cone-nuclei  close  to  the  limiting  membrane  owing  to 
the  shortness  of  the  inner  segment,  and  (c)  the  knob-like  ending  of  the  rods  in 
contrast  to  the  spread-out  foot-piece  of  the  cones.  Unfortunately,  all  these 
conditions  ai'e  violated,  sometimes  even  in  the  same  retina.  The  tip  of  the  cone 
may  be  slender,  elongated  and  cylindrical  (as  in  lizards  and  birds,  Verrier,  1935  ; 
Detwiler,  1943)  ;  the  nuclei  may  lie  in  a  single  layer  (amphibians,  Saxen,  1953), 
or  the  usual  arrangement  may  be  rev^ersed  (some  fishes  and  amphibians  :  Cajal, 
1893  ;  Franz,  1913  ;  Memier,  1929)  ;  while  the  foot-pieces  of  rods  may  be 
branched  (some  fishes,  amphibians  and  birds:  Greeff,  1900;  Putter,  1912; 
Detwiler,  1943). 

Differential  methods  of  staining  have  been  attempted  as  a  criterion  (Dogiel, 
1888  ;  Kolmer,  1936  ;  Wolff,  1949  ;  Wislocki  and  Sidman,  1952  ;  Saxen,  1953  ; 
and  others)  and  again  have  led  to  inconclusive  results.  A  further  point  of 
differentiation  is  a  study  of  the  connections  of  the  visual  cells  ;  several  rods  are 
typically  associated  with  one  bipolar  cell,  while  each  foveal  cone  is  ordinarily 
connected  with  one  bijoolar  cell  ;  but  again,  this  relationship  is  not  maintained 
by  the  peripheral  cones  nor  in  retinae  without  a  fovea.  It  is  possible  that,  when 
more  fully  developed,  the  study  of  the  ultra-microscopic  structure  may  provide 
further  evidence  whereon  a  distinction  between  the  two  types  of  cell  may  be  based. 

The  difficulty  in  anatomical  differentiation  has  naturally  stimulated 
attempts  at  a  functional  basis  for  classification,  for  it  is  generally 
conceded  that  the  cones  mediate  photopic  (and  colour)  vision  while 
the  rods  are  concerned  with  scotopic  vision.  Tlie  physiological  distinc- 
tion between  "  photocytes  "  and  "  scotocytes,""  however,  is  equally 
fraught  with  difficulties.  The  presence  of  rhodopsin  or  its  relatives 
would  theoretically  substantiate  ihe  presence  of  rods,  but  while  this  is 


252  THE   EYE   IN   EVOLUTION 

possible  in  a  uniform  retina  by  extraction  of  the  photopigments,  the 
method  is  inapphcable  in  a  duplex  retina  since  the  concentration  of 
pigment  is  not  sufficiently  great  to  allow  the  histological  demonstration 
of  vitamin  A  even  by  methods  so  delicate  as  fluorescence -microscopy 
(Stern,  1905  ;  Hopkins,  1927  ;  Walls,  1935  ;  Stenius,  1940  ;  Greenberg 
and  Popper,  1941  ;   see  Saxen,  1954  ;   and  others). 

There  is  no  doubt,  of  course,  that  fundamentally  the  two  elements 
are  alike  and  it  is  obvious  that  within  the  vertebrate  phylum  many 
transitional  forms  between  the  two  exist  ;  between  these,  wherein  the 
anatomical  difficulties  of  differentiation  occur,  a  sharp  distinction  may 
be  illegitimate.  Both  are  probably  derived  from  the  same  primitive 
ancestral  cells,  and  it  has  been  suggested  that  cones  are  transformed 
into  rods  during  development  (Steinlin,  1868  ;  Bernard,  1900-3  ; 
Cameron,  1911),  a  theory,  however,  which  later  evidence  has  questioned 
(Detwiler,  1943  ;  Birukow,  1949  ;  Saxen,  1954)  ;  similar  criticism  has 
been  directed  to  the  theory  of  Walls  (1934)  that  the  one  may  be 
transmuted  into  the  other  in  phylogeny. 

Walls's  theory — ingenious,  attractive,  fanciful  and  mvich  criticized — is  that 
the  primitive  visual  cell  of  Vertebrates  was  a  cone  and  that  therefrom  rods  were 
evolved  as  a  transmvitation-form  with  a  view  to  increasing  sensitivity  with  the 
development  of  rhodopsin — presumably  first  in  deep-sea  types.  The  brilliance 
of  illumination  on  land  allowed  many  reptiles  (diurnal  lizards)  to  retain  a  pure- 
cone  retina  ;  their  adoption  of  nocturnality  as  a  protective  measure  forced  some 
species  (Xavtusia)  to  develop  a  transitional  rod-like  element,  and  the  adoption 
of  complete  nocturnality  by  most  geckos  led  to  the  transmutation  into  rods. 
The  visual  elements  of  many  snakes  are  similarly  interpreted,  the  cones  of  some 
secretive  nocturnal  types  showing  a  structvnal  or  a  complete  transmutation 
into  rods,  in  the  first  case  withovit,  in  the  second  with  rhodopsin. 

It  is  interesting  that  recent  research  has  to  a  considerable  extent 
confirmed  this  somewhat  revolutionary  view.  That  such  a  trans- 
mutation had  in  fact  occurred  is  suggested  by  the  finding  of  Crozier  and 
Wolf  (1939^  that  the  rod-retina  of  the  gecko,  Sphcerodactylus,  has  a 
critical  fusion  frequency  similar  to  that  obtained  in  the  turtle  with 
its  predominantly  pure-cone  retina.  The  same  conclusions  could  be 
said  to  follow  the  finding  of  Underwood  (1951)  that  some  primitive 
Jamaican  geckos  had  oil-droplets  in  their  rod-like  receptors.  The 
peculiar  pigment  with  its  unusual  absorption  curve  for  a  substance 
based  on  vitamin  A^  (maximum  at  524  m^ti)  described  in  certain 
geckos  by  Denton  (1953)  {Gekko  gekko)  and  Crescitelli  (1956)  {Phyl- 
lurus)  again  could  perhaps  be  interpreted  as  an  attempt  to  transform 
ancestral  cones  into  rods,  as  if  they  were  unable  to  re-invent  rhodopsin 
for  lack  of  the  suitable  protein,  and  had  thus  been  forced  to  conjugate 
their  ret;;,enei  as  a  chromophore  and  produce  a  pigment  with  an 
absorpti       intermediate  in  spectral  position  between  those  generally 


THE   VERTEBRATE   EYE  253 

accepted  as  typical  of  rod-pigments  and  cone-pigments.  Finally,  the 
observations  of  Bellairs  and  Underwood  (1951)  support  the  view  that 
snakes  were  derived  from  burrowing  lizard-like  ancestors. 

In  the  present  state  of  our  knowledge  the  problem,  which  raises 
questions  as  difficult  as  they  are  interesting,  is  unsolved. 

Combinations  of  these  visual  elements  are  frequently  encountered 
in  several  classes  of  the  vertebrate  phylum.  Double  rods  are  rare 
(geckos  and  some  nocturnal  snakes).  A  second  rarity  is  the  twin 
cones — a  fusion  of  identical  elements — which  are  found  only  in  Teleo- 
steans  (Figs.  347-8).  Double  cones  are  more  common,  appearing  first 
in  Holosteans  and  occurring  in  every  other  class. ^  Typically  they 
represent  the  fusion  of  two  unlike  elements,  the  principal  resembling 
the  single  cones  in  the  same  retina  and  the  accessory,  generally  of  a 
simpler  type,  rarely  containing  an  oil-droplet  but  frequently  an 
unusually  large  paraboloid.  In  Amphibians,  Saxen  (1954-56)  has 
brought  forward  evidence  that  the  double  visual  elements  represent 
not  the  fusion  of  two  cones  as  has  generally  been  thought  but  the  fusion 
of  a  rod  with  a  cone.  Triple  "  cones  "  (perhaps  two  cone-like  com- 
ponents with  a  third  rod-like  component,  Saxen,  1953)  occur  in  some 
Teleosts  (trout)  and  Anurans,  while  quadruple  elements  have  also 
been  described  in  the  minnow,  Phoxinus  (Lyall,  1956).- 

The  origin  of  these  double  cells  has  given  rise  to  some  controversy.  The 
sceptical  view  that  they  were  histological  artefacts  was  put  forward  by  Koganei 
(1884)  and  has  been  maintained  by  such  writers  as  Cameron  (1911)  and  Roze- 
meyer  and  Stolte  (1930).  There  seems  no  doubt,  however,  that  they  do  exist. 
Dobrowolsky  (1871)  put  forward  the  hypothesis  that  they  resulted  from  the 
incomplete  division  of  single  cones,  a  view  upheld  by  Howard  (1908)  and  Franz 
(1913).  On  the  other  hand,  Detwiler  and  Laurens  (1921),  finding  that  double 
cones  appeared  during  development  at  a  stage  when  no  further  cell-divisions 
took  place,  suggested  that  they  were  produced  by  the  fusion  of  two  separate 
progenitors  ;  this  view  has  been  well  substantiated  in  Amphibians  by  Saxen 
(1954-56). 

The  physiological  significance  of  the  association  of  more  than  one  visual 
cell  is  not  understood.  The  fact  that  the  dendrites  of  the  two  components  sink 
to  different  depths  in  the  outer  plexiform  layer  suggests  some  difference  in  func- 
tion (Cajal,  1893  ;  Greeff,  1898),  while  the  observation  of  v.  Genderen-Stort 
(1887)  that  photomechanical  reactions  are  confined  to  the  principal  elements 
points  to  the  probability  that  the  accessory  element  has  a  subsidiary  function. 
Whether  this  is  visual  or  metabolic,  the  two  elements  living  in  symbiosis  (Howard, 
1908  ;   Franz,  1913),  is  conjectural. 

Apart  from  the  fundamental  structure  of  the  retina  the  other 
ocular  tissues,  although  in  general  conforming  to  the  vertebrate  plan 
seen  in  man  (Fig.  268),  show  considerable  variations  depending  upon 

^  Many  Teleosts,  Protopterus,  Amjjhibians,  Reptiles  except  some  snakes,  Birds,  the 
platypus,  and  Marsupials. 

2  See  also  footnote,  p,  364. 


254 


THE   EYE   IN  EVOLUTION 


an  unusually  wide  range  of  adaptive  demands,  for  vertebrates  have 
succeeded  in  making  themselves  at  home  in  every  environment  where 
life  is  possible.  These  differences  have  been  very  considerable  and  the 
adaptations  demanded  have  been  great.  The  vertebrate  eye  was 
initially  evolved  for  vision  in  shallow  water  ;  it  has  been  asked  to 
adapt  itself  for  vision  in  the  abyss,  in  the  rivers,  in  the  mud  of  the 
swamps,  on  land  and  in  the  air,  and  on  occasion  to  readapt  itself  for 


Fig.  268. — Diagram  of  the  Longitudinal  Section  of  the  Human  Eyeball. 


a,  angle  of  anterior  chamber.  ac, 
anterior  chamber.  aCV,  anterior  ciliary 
vessel.  C,  cornea.  CB,  ciliary  body. 
Ch,  choroid.  CO,  ocular  conjunctiva. 
CS,  canal  of  Schlemm.  DS,  dural 
sheath.  F,  fovea.  I,  iris.  L,  lens. 
ON,     optic     nerve.      OS,     ora     serrata. 


PC,  posterior  chamber.  PCV,  posterior 
ciliary  vessel.  PP,  pars  plana.  R, 
i-etina.  RM.  rectus  muscle.  S,  sclera. 
SCT,        subconjunctival         tissue.  V, 

vitreous.  VS,  vaginal  sheath.  VV,  vortex 
vein.  Z,  zonule. 


vision  in  the  seas  ;  it  has  been  asked  to  fit  itself  for  vision  at  night,  in 
twilight  or  in  dark  cavernicolous  surroundings  and  in  the  brightest  of 
dajdight  ;  it  has  been  asked  to  cater  for  panoramic  vision  where  the 
detection  of  movement  is  paramount,  or  to  accommodate  itself  to  the 
finest  stereoscopic  prowess,  to  meet  the  needs  of  a  sluggish  or  an  active 
habit  (ji  Jife,  to  be  content  with  a  vague  apperception  or  to  evolve  the 
capacit\  for  minute  resolution  in  form  vision  and  master  the  intricacies 
of  colou,  iiion.  All  this — and  more — it  has  done  ;  and  in  so  doing 
it  has  trit-i,  and  often  discarded,  now  this  expedient,  now  that. 


THE   VERTEBRATE   EYE  255 

The  requirements  of  aerial  vision  when  Amphibians  left  the  water 
for  the  dry  land  were  met  by  an  optical  reorientation  of  the  primitive 
aquatic  eye  to  suit  the  new  medium  and  the  provision  of  lids  equipped 
with  elaborate  glandular  structures  as  a  protection  against  drying  ;  a 
return  to  water  (as  in  the  whale  or  the  dolphin)  has  led  to  a  reversion 
of  this  process.  The  requirements  of  an  amphibious  life  have  resulted  in 
the  adoption  of  a  host  of  ingenious  devices  to  allow  an  easy  transition 
from  one  medium  to  the  other  and  to  maintain  adequate  vision  in  each. 
The  dangers  of  a  burrowing  habit  or  a  sandy  environment  have  led  to 
the  acquirement  of  protective  "  spectacles  "  (in  lizards  and  snakes). 
The  vagaries  of  nocturnal,  crepuscular  or  diurnal  vision  are  met  by 
several  expedients — variations  in  the  size  of  the  eye  and  the  lens,  in 
the  relative  proportions  of  the  percipient  elements  in  the  duplex  retina, 
in  the  size,  shape  and  motility  of  the  pupil,  and  the  provision  of  a 
tapetum  or  argentea,  choroidal  or  retinal  in  site,  fibrous,  cellular  or 
crystalline  in  nature,  which  augments  a  scanty  supply  of  light  by  its 
mirror-like  effect.  The  requirements  of  acuity  of  vision  are  met  by  the 
development  of  an  area  centralis  and  a  fovea,  the  receptor  elements  of 
which  are  provided  with  individual  nervous  connections  ;  stereopsis 
by  the  provision  of  more  than  one  fovea  or  by  a  swinging  forward  of 
the  visual  axes  ;  focusing  at  varying  distances  by  a  host  of  accommoda- 
tive devices — the  development  of  accessory  retinae  close  to  the  dioptric 
apparatus  (as  in  the  tubular  eyes  of  deep-sea  fishes),  variations  in  the 
position  of  the  visual  cells  relative  to  the  lens  (as  in  some  bats  or  in  the 
horse),  the  use  of  a  stenopoeic  pupil  (as  in  the  gecko  or  the  cat),  the 
deformation  of  the  eye  by  muscular  action  from  outside  (as  in  the 
lamprey),  the  pushing  or  pulling  of  the  lens  backwards  or  forwards  (as 
in  some  Fishes,  Amphibians  and  snakes),  or  a  change  in  its  shape  by 
squeezing  it  (as  in  Reptiles  and  Birds)  or  relaxing  it  (as  in  Mammals). 
These  serve  to  illustrate  the  multitude  of  expedients  adopted  by  an 
organ  of  unique  plasticity  to  meet  the  requirements  of  environments 
so  completely  different  as  the  abyss  of  the  ocean  and  the  upper  air,  or 
habits  so  diverse  as  the  sluggishness  of  a  parasite  and  the  activity  of 
a  bird-of-prey. 

The  general  scheme  of  phylogenetic  development  of  the  vertebrate 
eye  is  therefore  interesting  in  that  it  does  not  show  a  steady  and 
gradual  increase  in  efficiency,  but  illustrates  the  elaboration  of  more 
than  one  type  from  a  common  beginning  along  different  lines  to  reach 
more  than  one  culminating  point.  The  common  beginning  may  be 
found  in  Cyclostomes,  the  eyes  of  which  are  primitive  and  show  no 
specializations.  From  this  starting  point  three  peak-points  have 
evolved  in  types  which  in  their  habits  of  life  are  peculiarly  visually 
conscious — in  teleostean  Fishes,  Sauropsida  (lizards  and  Birds) 
reaching  its  highest  development  in  Avians,  and  among  Mammals  in 


256  THE   EYE   IN   EVOLUTION 

the  Primates.  In  these  three  groups  alone  is  a  fovea  found  making 
possible  a  good  acuity  of  vision  ;  in  these,  highly  developed  accommo- 
dative mechanisms  are  present  allowing  accuracy  of  form  vision  over  a 
wide  range  of  distances  ;  and  in  these  alone  good  colour  vision  has 
been  demonstrated.  In  each  of  these  the  optic  axes  may  be  swung 
forwards  so  that  the  visual  fields  are  made  to  overlap,  thus  rendering 
it  possible  for  binocular  to  replace  panoramic  vision  ;  in  the  last  group 
a  partial  decussation  of  the  optic  nerve  fibres  allows  an  anatomical 
basis  for  the  coordination  of  ocular  movements  ;  and  finally,  a  neo- 
pallium built  up  upon  the  sense  of  vision  replaces  the  original  archi- 
pallium  which  was  based  upon  the  sense  of  smell.  In  this  way  the 
dyscritic  mechanism  of  the  simple  eye  of  the  lower  Vertebrates,  which 
was  essentially  adapted  to  the  biologically  primitive  function  of  the 
appreciation  of  light  and  movement,  developed  the  capacity  for  the 
intelligent  appreciation  of  complex  visual  patterns  and  the  potentiality 
to  form  reasoned  visual  judgements. 

The  interesting  thing  is  that  the  eye  of  each  of  these  types  has 
developed  separately  and  independently  ;  between  them  there  is  no 
evolutionary  sequence,  for  all  have  attained  their  high  degree  of 
efficiency  by  different  expedients  which,  when  they  show  affinities,  owe 
their  relationship  to  the  fact  that  they  have  evolved  not  the  one  from 
the  other,  but  all  from  the  same  original  substrate  of  physiological 
potentialities.  It  is  also  interesting  that  of  these  types  the  sauropsidan 
eye  is  the  most  efficient  as  an  optical  mechanism  ;  of  all  the  three, 
Birds  have  relatively  the  largest  and  absolutely  the  most  specialized 
eyes,  tlie  most  efficient  focusing  apparatus,  a  pecten  structure  instead 
of  a  retinal  system  of  vessels,  the  most  complex  macular  arrangements, 
and  the  highest  visual  acuity.  The  eye  of  man  cannot  therefore  be 
considered  as  representing  the  acme  of  efficiency  as  an  optical  instru- 
ment ;  it  is  to  the  unique  and  transcendent  development  of  the 
associated  cerebral  centres  that  it  owes  its  functional  predominance. 

Bellairs  and  Underwood.     Biol.  Rev.,  26,       Dobrowolsky.     Arch.  Anat.  Physiol.,  208 
193  (1951).  (1871) 


Bernard.      Quart.    J.    micr.    Sci.,    43,    23  Dogiel.    Anat.  Anz.,  S,  133  {li 

(1900)  ;      44,    443    (1901)  ;      46,    25  Franz.      Oppel's    Lhb.   vergl.   mikr.   Anat. 
(1903).  Wirbeltiere,  Jena,  7,  1  (1913). 

^''■''n°,r^o.    ^-    '"'■^^-    ^''^■"'°^"    31'    ^'"  van    Genderen-Stort.      v.  Graefes    Arch. 


Ophthal.,  33  (3),  229  (1887). 


(1949). 

Cajal.     LaCe//!/7e,  9,  119  (1893).  r^       «•        ^      e>       ,    ,      r>,      •  ,      la      i«i 

Cameron.    J.  Anat.  Physiol. ^6,  45  {\9\l).  ^''^^f^oo.f-    ^'''^'^'°^-    ^'^i/*'°'-    16'    ^^^ 
Crescitelli.    J.  gen.  Physiol.,  ^0,217  {1956).  GraehSaemisch    Hb     aes     Auaenheilk 

Crozier   and  Wolf.     J.   gen.    Physiol.,   22,  fr^   V        !^  naf^'a^^         Augenheitk., 

555  (1939)  '     '  ^'^P-  '^  (iJUU). 

Denton.     XIX  Internal.   Cong.   Physiol.,  ^'^''^iT^  f?*?,^°PP'''"-    ^"^'^er.  J.  Physiol., 

Abstr.  Communications,  306  (1953).  ^34,  114  (1941). 

Detwiler.     Vertebrate  Photoreceptors,  N.Y.  Hopkins.    Z.  vergl.  Physiol.,  6,  345  (1927). 

(1943)  Howard.    J.  Morphol.,  19,  561  (190S). 

Detwiler  an  ;  Laurens.    J.  comp.  Neurol.,  Koganei.      Arch.    mikr.    Anat.,    23,    335 

33,  493  (1921).  (1884). 


THE   VERTEBPvATE   EYE 


257 


Kolmer.     Mollendorff's  Hh.  niikr.  Annt.  d. 

Menschen,  3  (2).  310  (1936). 
Lyall.    Nature  (Lond.),  177,  1086  (1956). 
Menner.     Z.  vergl.  Phy.sioL.  8,  761   (1929). 
MuUer,  C.    Z.  Anat.  Enlwick.  Ges.,  81,  220 

(1926). 
Putter.     Graefe-Saemisch  Hb.  ges.  Augen- 

heilk..  III.  1,  Kap.  10,  1  (1912). 
de  Robertis.     J.  biophys.  biochem.  Cytol., 

2,  319  ;    suppL,  209  (1956). 
Rozemeyer  and   Stolte.       Z.   niikr.   Anat. 

Forsch.,  23,  98  (1930). 
Saxen.     Ajin.  Med.  e.vp.  Biol.  Fenn..  31, 

254  (1953). 
Ann.  Acad.  Sci.fen.  A  IV,  23,  1  (1954). 
Acta  Anat.,  Basel,  25,  319  (1955). 
J.  Embryol.  exp.  Morphol.,  4,  57  (1956). 
Schultze.       Arch,     niikr.     Anat.,     2,     175 

(1866)  ;   3,  215  (1867). 
Sidman.      J.   biophys.   biochem.   Cytol..   3, 

15  (1957). 


Sidniau     and     Wislocki.       ./.     histo-chem. 

Cytochem.,  2,  413  (1954). 
Sjostrand.    J.  cell.  comp.  Physiol.,  33,  383 

(1949)  ;    42,  15,  45  (1953). 
Steinlin.     Arch.  mikr.  Anat.,  4,  10  (1868). 
Stenius.      Acta    Physiol.    Scand.,    1,    380 

(1940). 
Stern,     v.  Graefes  Arch.  Ophthal.,  61,  561 

(1905). 
Underwood.       Nature    (Land.),    167,    183 

(1951). 
Verrier.     Bull.  Biol.  France  Belg.,  Suppl. 

20,  1  (1935). 
Walls.     Anier.  J.  Ophthal.,  17,  892  (1934). 
Brit.  J.  Ophthal.,  19,  129  (1935). 
The  Vertebrate  Eye,  Michigan  (1942). 
Wislocki  and  Sidman.     Anat.   Bee,   113, 

540  (1952). 
J.  conip.  Neurol,  101,  53  (1954). 
Wolff.      The  Anatomy  of  the  Eye  and  the 

Orbit,  London  (1949). 


258 


THE   EYE   IN   EVOLUTION 


Fig.   269. — U.  W.  SoEMMP:RRiN(i   (1793-1871). 


CHAPTER  X 
THE   EYES   OF   CYCLOSTOMES 

Although  he  made  a  classical  description  of  the  eyes  of  all  classes  of 
Vertebrates  except  Cyclostomes,  I  am  introducing  this  chapter  which  is  the 
first  of  a  series  dealing  with  the  structure  of  the  eyes  of  Vertebrates  with  the 
portrait  of  detmar  wilhelm  soemmerring  (1793-1871)  (Fig.  269)  in  view  of 
the  fact  that  he  was  one  of  the  earliest  writers  to  make  a  systematic  study  of  this 
subject.  It  is  true  that  many  incidental  observations  had  been  made  on  the 
fijier  structure  of  the  eyes  of  different  Vertebrates  by  such  investigators  as  van 
Leeuwenhoek,^  Zinn  ^  and  Young,^  while  compendia  had  been  published  by  such 
authors  as  Bluraenbach,*  Albers,^  and  Cuvier  ®  ;  but  none  is  so  delightful  to 
read  as  is  the  thesis  written  in  Latin  which  brought  Soemmerring  his  doctorate 
in  Gottingen  in  1816,  and  was  published  in  1818  under  the  title  De  oculorum 
hominis  animaliumque  sectione  horizontali  commentatio  ;  the  illustrations  are  so 
beautiful  that  several  of  them  have  been  reproduced  in  the  following  chapters. 
D.  W.  Soemmerring,  the  son  of  an  equally  distinguished  German  ophtha,lmologist, 
S.  T.  von  Soemmerring  (who,  it  will  be  remembered,  first  described  the  macula 
lutea  as  a  hole  in  the  retina),  was  born  in  Frankfurt  where  in  later  life  he  practised 
for  many  years  and  where  his  jubilee  as  a  doctor  was  officially  celebrated  in 
1866.  He  is  also  remembered  ophthalmologically  for  two  particular  observations 
— a  description  of  the  organic  changes  in  the  eye  after  the  operation  for  cataract 
in  which  he  described  the  annular  remnant  of  the  lens  now  universally  known 
as  Soemmerring's  ring  (1828),  and  the  first  description  of  a  living  cysticercus  in 
the  human  eye  (1830). 

The  CYCLOSTOMES  (kJk/\o9.  round  ;  otoixx,  a  mouth),  so  called 
because  of  their  round,  jawless,  suctorial  mouths  which  differentiate 
them  from  all  other  Vertebrates,  are  the  only  surviving  representatives 
of  the  large  class  of  agnatha  (a,  privative  ;  yvddos,  jaw)  which  flourished 
in  great  variety  and  numbers  during  Palaeozoic  times  and  are  now 
with  this  exception  extinct.  They  are  freely-swimming  worm -like 
"  pre-fishes  "'  of  extreme  antiquity,  essentially  primitive  in  their 
structure  and  differing  in  many  ways  from  true  Fishes,  principally  in 
the  absence  of  jaws,  by  the  single  olfactory  organ  and  by  the  absence 
of  paired  fins.  Today  they  are  represented  by  two  existing  types  and 
a  few  others  like  them — the  hagfishes  (slime-eels)  and  the  lampreys. 
The  eyes  of  the  former,  buried  deeply  within  the  skm,  are  degenerate 
and  sightless  and  are  described  at  a  later  stage^  ;  those  of  the  latter, 
at  first  buried  and  later  coming  to  the  surface,  constitute  the  most 

'  Epistolce  physiologicce,  Delphis,  1719. 
-  Comment.  Soc.  Sci.,  Gottingen,  1754. 
3  Philos.  Trans.,  1793. 

*  Vergl.  Anat.,  1784. 

5  Beyt.  z.  Anat.  u.  Physiol,  d.  Thiere,  1802. 

*  Leg-ons  d'anat.  comparee,  Paris,  1805. 
'  p.  734. 

259 


260  THE   EYE   IN   EVOLUTION 

primitive   type   of  vertebrate   eye   showing   characteristics    differing 
markedly  from  those  of  Fishes. 

THE    LAMPREYS    (PETROMYZONIDiE) 

The  lampreys  are  large  eel -like  creatures  found  mainly  in  the  seas  and 
rivers  of  the  northern  hemisphere  ;  the  sea  lamprey  {Petromyzon  marinus), 
about  3  feet  in  length,  and  the  fresh-water  river  lampern  {Lanipetra  fluviatilis), 
about  2  feet  in  length,  eat  worms  and  small  crustaceans  and  are  also  ectoparasites 
on  living  fishes  to  which  they  attach  themselves  and  feed  by  rasping  off  the  flesh. 
From  the  latter  species  smaller  brook  lamperns  (sand-prides)  have  presumably 
been  derived  ;  these  do  all  their  feeding  as  larvae  and  after  metamorphosis  to 
the  advilt  form,  breed  and  then  die.  Related  genera  are  Mordacia  and  Oeotria 
from  the  coasts  of  Chile  and  Australasia,  and  Ichthyomyzon  from  the  western 
coasts  of  North  America  (Fig.  270). 

The  hfe-cycle  of  the  lamjDrey  is  interesting  and  complex.  The 
larva,  or  Ammocoetes  (sometimes  known  as  the  "  pride  "  when  it  was 


Fig.  270. — The  Sea  Lamprey,  Petromtzon  maris  us. 

There  are  two  unpaired  median  fins  and  a  relatively  large  eye  ;  behind 
the  eye  are  seven  point-like  gill-slits.  For  the  head  of  the  lamprey,  see 
Fig.  862. 

thought  to  be  a  different  species),  is  a  small  creature  without  a  sucking 
mouth  and  with  a  solid  spinal  cord  in  which  a  medullary  cavity 
subsequently  develops  ^  ;  the  eyes  are  extremely  rudimentary  and  lie 
beneath  the  skin.  Before  metamorphosis  the  larva  burrows  in  mud 
and  the  non-functional  eyes  are  covered  with  opaque  integument.  At 
metamorphosis  during  the  latter  half  of  July,  at  the  age  of  2  to  4  years, 
great  changes  occur  as  the  ammocoetes  leaves  the  mud  or  sand  and 
transforms  into  the  eel-like  adult,  changes  which  include  the  develop- 
ment and  emergence  of  the  eyes.  The  simple  and  relatively  undiffe- 
rentiated retina  of  the  larva  (retina  A)  rapidly  becomes  transformed 
into  the  functional  adult  tissue  (retina  B)  and  as  it  does  so  the  over- 
lying skin  atrophies  and  becomes  transparent.  The  adult  organ  is 
rapidly  formed,  neither  regressive,  atrophied  nor  degenerate  in  type, 
but  primitive  in  nature  and  embryonic  in  certain  characteristics, 
particularly  in  the  structure  of  the  optic  nerve. 

It        nteresting  that  the  animal  also  possesses  pineal  and  parietal  "  eyes," 
a  subjf  ich  will  be  fully  discussed  in  a  later  chapter. ^ 

'  Compare  p.  239,  footnote.  ^  p.  711. 


CYCLOSTOMES 


261 


THE    AMMOCCETE    EYE 

Since  the  original  description  by  W.  Miiller  (1875),  several  studies 
have  been  made  of  the  animocoete  eye.  The  youngest  specimen 
described  was  that  of  Ida  Mann  (1928)  who  figured  a  simple  optic 
vesicle  evaginated  from  the  anterior  cerebral  vesicle  lying  close 
underneath  the  surface  ectoderm  (Fig.  271).  At  this  early  stage 
there  was  neither  vitreous  nor  lens,  the  outer  layer  of  the  vesicle 


mM^m 


Fig.    271. — Section  Through  the  Eye  of  the  Ammoccetes   (the    Larva 

OF    PETROMYZOy    FLUVIATlLIs). 

There  is  neither  vitreous  nor  lens  ;  the  optic  cup  is  closely  folded  upon 
itself,  the  outer  layer  being  pigmented  and  the  inner  showing  a  considerable 
degree  of  differentiation. 

a,  surface  epithelium  of  the  head  ;  6,  pigmented  outer  layer  of  the  optic 
cup  ;  c,  nuclei  of  the  visual  cells  ;  d,  nuclei  of  bipolar  cells  ;  e,  ganglion  cells 
with  nerve  fibres  arising  from  them  ;  /,  visual  cells  ;  g,  muscle  mass  of  head  ; 
h,  optic  nerve  (Ida  Mann). 


being  pigmented  and  the  inner  showing  differentiation  into  the  three 
layers  of  cells  characteristic  of  the  vertebrate  visual  retina — visual 
cells  (indistinguishable  either  as  rods  or  cones),  bipolar  cells  and  gan- 
glion cells  the  axons  of  which  constitute  the  oj^tic  nerve.  In  somewhat 
older  larvae  (5-10  mm.),  von  Kupffer  (1894)  and  Studnicka  (1912)  des- 
cribed a  lens  vesicle  lying  underneath  the  single  layered  ectoderm 
and  completely  separate  from  the  ojjtic  vesicle  (Figs.  272  and  273), 
while  Carriere  (1885)  in  a  more  mature  larva  (30  mm.)  described 
a  lens,  at  this  stage  still  vesicular,  invagiTiated  within  the  optic 
vesicle.     Eventually  the  lens  becomes  solid,  tlie  anterior  and  vitreous 


262 


THE   EYE   IN   EVOLUTION 


Figs.   272  and   273. — The  Ammocoete  Eye  (after  Studnicka). 


Fig.  272. — The  eye  of  the  8  mm.  lar\a 
of  Pctromyzon,  showing  the  optic 
vesicle  and  the  smaller  lens  vesicle 
superficial  to  it. 


Fig.  273. — The  eye  of  the  18  nun. 
ammocoetes  showing  the  lens  vesicle 
incor^jorated  into  the  optic  vesicle. 
In  the  latter  the  outer  pigmented 
layer  and  the  highly  differentiated 
inner  layer  with  the  projecting  visual 
cells  are  evident. 


chambers  till  ^\'\i\\  fibrillar  material,  the  cornea  is  entirely  cellular, 
the  retina  becomes  relatively  differentiated  but  blood  vessels  and 
mesodermal  elements  do  not  invade  the  vesicular  eye  (Mawas  and 
Magitot,  1912;  Diicker,  1924)  (Figs.  274  and  275).  Meantime  the  eye 
sinks  beneath  the  skin  to  become  separated  from  it  by  a  considerable 
thickness  of  tissue. 

The  depth  at  which  the  vesicular  eye  lies  at  this  stage  beneath  the  skin 
suggested   to   Hagcdoorn    (1930)   that   the   lens   was   derived   from   the   retinal 


Fig.   274. — The  Eye  of  the  Ammoccetes. 

A\  a  late  stage.  On  top  is  the  surface  epithelium,  underneath  which  lies 
the  ii'i^sodernaal  skin.  Underneath  this  is  the  scleral  cornea.  The  lens  is 
fully  '  vnied,  as  also  are  the  anterior  and  vitreous  chambers  (a  drawing  from 
Mawas  i 


CYCLOSTOMES 


263 


vesicle  ;  the  suggestion  that  the  eye  of  the  lamprey  differed  from  all  other 
vertebrate  eyes  in  that  its  elements  were  all  autonomous  in  the  sense  that  the 
entire  oi'gan  arose  from  the  neural  ectoderm  is,  however,  by  no  means  proven 
by  the  evidence  submitted  by  this  author  and  should  be  discarded.  It  is  apposite 
that  in  the  still  more  primitive  eye  of  the  myxinoid,  Bdellost07na,  Stockard 
(1907)  found  that  the  lens  appeared  in  the  usual  vertebrate  way  as  a  vesicle 
from  the  surface  epithelium  inrlependently  of  the  optic  vesicle. 

LIGHT-SENSITIVE  CELLS.  In  the  ojiidermis  of  the  tail  of  the  animoccotes 
there  are  numerous  iiiteresting  cells  cojiiously  inncr\'ated  from  the  lateral  line. 
Morphologically  they  resemble  the  ajiolar  visual  cells  seen  in  tlie  earthworm  or 


¥ui 


s     THiMncH    THE    l'<isTEi:iui;    .Segment    (.if 
THE  Fully  Developed  Ammoccetes. 


THE    Eye   of 


'/,  ganglion  cells  ;  /,  internal  nuclear  layer  ;  c.  external  nucleai'  layer  ;  v, 
visual  cells  ;  7;,  pigmented  epithelium  ;  ch,  rlioroid  ;  s,  sclera  ;  m,  muscular 
tissue  (Azan,    X  250)  (Katharine  Tansloy). 

Mya  (Fig.  86)  and  are  said  to  be  associated  with  a  photosensitive  pigment  ;  they 
probably  act  as  primitive  ])liotoreceptors  determining  phototactic  activity 
(Young,  1935  ;  Steven,  1950  51).  It  will  be  remeinbered  that  light-sensitive 
cells  of  the  type  characteristic  of  Invertel)rates  are  also  found  ainong  Chordates 
in  Amphio.ru.s  as  the  cells  of  .loscphi  ;  anil  it  is  interesting  that  the  only  other 
Vertebrate  which  shows  evidence  (^f  a  similar  primiti\e  ])li()totaxis  is  the  cave- 
dwelling  salamander,  Proteus  a>i</ii/)i us  (Hawes.  194(i). 


THE    LAMPREY    EYE 

The  eye  of  the  lamprey  and  its  relatives  is  of  unusual  interest  in 
that  it  shows  a  ninnber  of  primitive  characteristics  differentiating  it 
clearly  from  the  eyes  of  Fishes  and  all  other  higher  Vertebrates  ; 
nevertheless,  it  conforms  closely  to  the  essential  structure  of  the  eyes 

1   p.  229. 


264 


THE   EYE   IN   EVOLUTION 


Figs.  276  and  277. — The  Eye  of  Lampetra  planeri. 

SC  DC  DE 

/ 

CM 
VS 


Fig.  276. 


DC     SC 


CM 


The  outline  of  the  large  circular  lens  is  seen  as  a  dark  circle  ;  it  has 
slipped  backwards  and  the  inner  part  of  the  lens  has  fallen  out  of  the  section 
(Mallory's  phospho-tungstic  acid  haematoxylin  (  X  34)  (Katharine  Tansley). 

Ch,  choroid  (black)  ;  CM,  cornealis  muscle  ;  DC,  dermal  cornea  ;  DE, 
dermal  epithelium  ;  ER,  external  rectus  ;  10,  inferior  oblique  ;  IR,  internal 
rectu::  ON,  optic  nerve  ;  RCT,  retrochoroidal  tissue  ;  Sc,  sclera  ;  SC, 
scleral      j  nea  ;   VS,  venous  sinuses. 


CYCLOSTOMES  265 

of  this  phylum.  Of  all  vertebrate  eyes  it  is  the  simplest  (Figs.  276  and 
277).    Its  characteristic  features  are  : 

an  avascular  retina  wherein  the  ganglion  cell  layer  7nerges  with  the 

inner  mcclear  layer  ; 
ike  embryonic  nature  of  the  optic  nerve,   ivithout  septa  but  ivith  an 

ependymal  axis,  and  provided  ivith  non-myelinated  nerve  fibres  ; 
the  thick  epichoroid  in  certain  species  ; 
the  large  primitive  lens  lacking  sutures  ; 
the  absence  of  intra-ocular  musculature  ; 
the  separation  of  the  cornea  from  the  surface  ectoderm  ; 
the  absence,   alone  among   Vertebrates,  of  a  cartilaginous  or  bony 

orbit ; 
the  blending  of  some  of  the  extra-ocular  muscles  ; 
and  the  presence  of  an  extra-ocular  muscle  of  accommodation  ivhich 

acts  by  deforming  the  eyeball  from  the  outside. 

The  structure  of  the  eyes  of  all  adult  lampreys  {Petromyzon 
marinus,  Lampetra  fluviatilis,  etc.)  conforms  to  the  same  general  plan 
(W.  Miiller,  1875  ;  Franz,  1932-34  ;  Walls,  1935-42  ;  Rochon- 
Duvigneaud,  1943  ;  Henckel.  1944 — Mordacia). 

THE  GLOBE,  as  in  most  Fishes,  is  flattened  antero-posteriorly, 
givmg  the  eye  an  ellipsoid  configuration,  the  most  prominent  feature 
being  the  large  anteriorly-situated  lens  which  makes  underwater 
focusing  possible.^  The  cornea-sclera  is  primitive  ;  the  latter  is  a  thin, 
purely  fibrous  structure,  the  former  a  tenuous  lamellated  stratum 
almost  reduced  to  Descemet's  membrane  together  with  its  endothelium, 
continuous  with  the  sclera.  Superficial  to  this  the  skm  is  transparent 
and  thm,  forming  a  layer  in  which  the  dermal  glands  and  vessels  are 
lost  and  merely  the  multi-stratified  epithelium  remains,  consistuig  of 
6  or  7  layers  of  regularly  arranged  cells.  The  space  between  the  two 
structures — the  dermal  cornea  and  scleral  cornea — is  occupied  by  a 
delicate  mucoid  tissue  derived  from  orbital  connective  tissue,  the  loose 
structure  of  which  allows  the  globe  to  rotate  /reely  underneath  the 
skin. 

The  composite  "  cornea  "  of  Cyclostomes  thus  represents  an  early  stage  in 
the  development  of  the  typical  vertebrate  cornea  wherein  the  superficial  layers 
derived  from  the  surface  ectoderm  have  not  yet  fused  with  the  deeper  layers 
of  mesodermal  origin.  The  eye  is  thus  entirely  a  subcutaneous  organ.  To  the 
specialized  area  of  transparent  skin  constituting  the  dermal  cornea,  German 
authors  have  given  the  name  of  primary  spectacle  ('-primare  Brilla"),  the  term 
denoiing  a  fixed  transparent  structure  separate  from  the  globe  underneath  irhich  the 
eye  is  free  to  rotate  (Fig.  278)  (Haller,  1768  ;  Treviranus,  1820  ;  and  others  ;  and 
Franz,  1934V  Such  an  arrangement  is  seen  in  tadpoles  and  adult  aquatic 
Amphibians  as  well  as  in  Cyclostomes.     A  secondary  splitting  of  the  cornea  into 

1  p.  276. 


266 


THE   EYE   IN   EVOLUTION 


two  layers  to  prodvice  a  similar  configuration  may  occur  in  some  fishes  as  an 
adaptation  to  protect  the  eye  when  the  animal  is  crawling  in  mud  or  sand 
(bottom-fishes,  lung-fishes,  cat-fishes)  or  to  prevent  desiccation  in  forms  which 
leave  the  water  for  air  (lung-fishes,  eels,  mud-skippers,  some  gobies,  etc.).  An 
entirely  different  configuration — the  secondary  spectacle — is  formed  by  the 
development  of  a  transjMrent  area  in  the  lids,  either  a  transparent  window  in  a 
moveable  lower  lid,  as  in  a  few  chelonians  and  some  lizards,  or  by  the  edge-to- 
edge  fusion  of  the  two  lids  which  have  become  transparent  to  form  a  fixed 
spectacle  as  is  seen  among  Fishes  in  anchovies  and  in  many  Reptiles 
(snakes  and  some  lizards)  ;  it  is  this  that  gives  the  characteristic  glassy 
stare  to  the  eyes  of  snakes  and  most  lizards.  In  this  case  the  cornea  is  comprised 
of  all  its  constituent  layers  and  between  it  and  the  fused  lids  there  is  a  true  cavity 


Figs.  278  and  279. 


Spectacles." 


Fig.  278. — The  primary  spectacle  of 
Cyclostomes  and  aquatic  Amphi- 
bians. 

E,  the  surface  epithelium  forming 
the  dermal  cornea  ;  C,  scleral  cornea  ; 
M,  mucoid  tissue  between  the  two. 


Fig.  279. — The  secondary  spectacle  as 
seen    jiarticularly    in    Reptiles. 

E,  the  "  spectacle  "  formed  by 
fusion  of  the  lids  which  are  transparent; 
C,  the  cornea  ;  S,  the  conjunctival  sac 
lined  throughout  by  epithelium,  proxi- 
mally   corneal   and   distally   palpebral. 


(the  conjunctival  space)  lined  by  epithelium,  the  distal  part  of  which  represents 
the  palpebral  conjunctiva,  the  proximal  the  corneal  epithelium  (Figs.  279  and 
470)  (Hein,  1913  ;    Franz.  1934  ;    Walls,  1942). 

The  uveal  tract  of  the  lamprey  is  also  primitive  in  its  characteristics. 
A  single  artery  penetrates  the  sclera  beneath  the  optic  nerve,  which 
divides  into  four  vessels,  one  for  each  quadrant  ;  these  break  up  into 
a  choriocapillaris  overlying  the  retina,  but  instead  of  the  efferent  blood 
being  drained  away  by  veins,  the  outer  half  of  the  choroid  is  composed 
of  a  continuous  lake  of  blood  (the  subscleral  sinus)  which  in  turn 
leads  hy  four  apertures  traversing  the  sclera  into  a  complex  system  of 
extra-ocular  venous  sinuses  surrounding  the  outer  aspect  of  the  sclera 
(Figs.  276-7).  In  the  posterior  half  of  the  globe  between  the  subscleral 
venous  =<inus  and  the  sclera  there  is  in  some  species  (Petromyzon 
marinus)  a  peculiar  epichoroidal  tissue  composed  of  large  pigmented 


CYCLOSTOMES  267 

cells  and  equally  large  vesicular  cells  forming  a  relatively  thick  cushion 
between  the  choroid  and  the  sclera.  There  is  no  ciliary  body,^  only  a 
flat  ciliary  zone,  and  the  immobile  non-mviscular  iris  consists  merely  of 
the  usual  two  layers  of  (retinal)  epithelium  covered  anteriorly  by  a 
tenuous  and  lightly  pigmented  stroma  binding  together  the  blood- 
vessels which  are  supplied  by  three  anterior  ciliary  arteries.  Contrary 
to  the  arrangement  in  higher  ^>rtebrates.  the  epithelial  layers  of  the 
iris  continue  forwards  the  state  of  pigmentation  of  the  corresponding 
retinal  layers  ;  the  anterior  layer  is  pigmented,  the  posterior  un- 
pigmented  almost  up  to  the  pupillary  border.  The  anterior  surface  of 
the  iris  has  a  light  metallic  sheen  due  to  a  fine  argentea  comprised 
of  a  layer  of  closely  packed  cells  containing  guanine  crystals,  a  configura- 
tion which  is  not  continued  into  the  choroid. 

The  angle  of  the  anterior  chamber  is  constructed  on  simple  lines. 
A  ring  of  large  endothelial  cells  encircles  the  periphery  of  the  cornea 
as  the  ANNULAR  LIGAMENT,  continues  anteriorly  with  the  corneal 
endothelium  and  sends  strands  posteriorly  to  the  choroid  suggestive 
of  the  tensor  choroidese  of  Teleosteans  ;  while  from  the  region  of  this 
ring,  fine  strands  span  the  angle  to  reach  the  anterior  surface  of  the 
iris,  reminiscent  of  a  pectinate  ligament.  The  large  and  almost 
circular  lens  is  wedged  in  the  immobile  pupil  and  approximates  the 
cornea,  separated  from  it  at  most  by  a  capillary  space  ;  it  is  held  in 
place  by  the  support  of  the  cornea  in  front  and  the  vitreous  behind. 
The  lens  is  primitive  in  formation  compared  with  the  structures  found 
in  other  Vertebrates,  showing  a  central  zone  of  polygonal  or  rounded 
fibres  and  a  somewhat  irregular  arrangement  in  the  periphery  without 

1  The  origin  of  the  aqueous  humour  of  Cyclostomes  and  Fishes  is  obscure,  but  it 
is  possible  that  the  ocular  fluids  are  maintained  directly  by  osmosis  through  the  cornea, 
the  pressure  being  ccjuilibrated  through  the  blood-stream.  In  fresh-water  fish  and  the 
lamprey  the  blood  is  hypertonic  to  the  mediimi  so  that  the  body  fluids  are  constantly 
replenished  by  the  absorption  of  water  through  the  skin  by  osmosis,  the  fish  excreting 
the  large  cjuantities  of  fluid  thus  absorbed  by  producing  immense  quantities  of  urine. 
In  marine  teleosts,  on  the  other  hand,  the  blood  is  hypotonic  to  the  sea-water  ;  dehydra- 
tion is  avoided  only  by  the  copious  drinking  of  the  latter.  This  is  actively  absorbed 
in  the  gut  against  tlie  osmotic  gradient  while  the  excess  of  salts  is  excreted  differentially 
in  the  gut,  kidneys  and  gills.  Selachian  fishes  maintain  a  high  level  of  urea  in  the 
blood  (some  2%)  thus  keeping  it  at  a  higher  osmotic  level  than  sea-water  ;  the  latter 
is  thus  absorbed  osmotically  while  the  excess  of  salts  is  excreted  through  the  gills. 
It  would  appear  that  Myxine  has  a  salt  concentration  in  the  blood  approaching  that  of 
sea-water  and  thus  higher  than  that  of  any  other  vertebrate  (Robertson,  1957).  It 
is  probable  that  the  fluid-exchange  and  the  pressure  ecjuilibrium  in  the  eye  is  main- 
tained in  much  the  same  manner.  There  would  seem  to  be  no  anatomical  basis  in 
any  cyclostome  or  fish  for  an  elaborate  secretorj'  mechanism  for  the  intra-ocular 
fluid  ;  the  only  types  which  possess  ciliary  processes  are  the  Selachians  and  these,  in 
Franz's  view  (1934),  probably  serve  merely  as  a  mechanism  for  supporting  the  lens. 
All  land  animals,  on  the  other  hand,  secrete  the  aqueous  humour.  It  should  not  be 
considered  strange  that  the  tissues  of  the  earliest  Vertebrates  (fresh-water  agnathous 
fishes)  were  hj'pertonic  to  the  medium  in  which  they  lived  ;  the  same  relationship  is 
seen  in  the  tissue-cells  of  inan  which  are  maintained  in  a  state  of  hypertonicity  in  com- 
parison with  the  surrounding  tissue-fluid  by  an  osmo- regulation  depending  on  respira- 
tory activity  (see  Bartley,  Davies  ami  Krebs,  Proc.  n-y.  Soc.  B.,  142,  187,  1954). 


268 


THE   EYE   IN   EVOLUTION 


sutures  (Capraro,  1 934-37 ).i  It  has  a  light  yellow  coloration  derived 
from  a  pigment  the  composition  of  which  is  unknown  (Plate,  1924  ; 
Franz,  1932  ;   Walls  and  Judd,  1933). 

The  retina,  even  at  this  early  stage  of  Vertebrate  evolution,  shows 
the  essential  architecture  of  the  vertebrate  eye  ;  but  is  entirely  avas- 
cular and  without  any  suggestion  of  an  area  centralis  (Fig.  280). 
Next  to  the  outer  layer  of  pigmentary  epithelium  lie  the  visual  elements, 


^^=' 


M»»^-.^ 


Fig.   280. — The  Retina  of  Lampetra   fluviatilis. 

g,  ganglion  cells  ;  i,  internal  nuclear  layer,  consisting  essentially  of 
horizontal  cells  above  and  bipolar  cells  below  ;  e,  external  nuclear  layer  ; 
?»,  visual  cells  ;  p,  pigmented  epithelium  (Feulgen,  X  370)  (Katharine  Tansley). 


thereafter  their  nuclei  form  an  outer  nuclear  layer  which  is  followed 
by  a  combined  layer  containing  bipolar  cells,  horizontal  cells,  amacrine 
cells  and  a  few  sparse  ganglion  cells. 

The  nature  of  the  visual  elernejifs  has  given  rise  to  some  controversy, 
but  most  authorities  are  now  agreed  that  even  in  this,  the  most  primitive 
of  Vertebrates,  two  types  of  cell  exist,  a  relatively  long  and  a  relatively 
short  cell,  the  former  with  a  voluminous  ellipsoid  and  short  external 
segment,  the  latter  with  a  smaller  ellipsoid  capped  by  a  longer  external 
segment.  The  differentiation  between  the  two  types  and  their  relative 
numbers  vary  in  different  families  (Walls,   1035).     In  the  primitive 

1  Compare  the  lens  of  lizards,  p.  361. 


CYCLOSTOMEvS 


269 


genus,  Ichthyomyzon,  the  two  differ  little  in  size  ;  in  Lmnpefra  fluviatilis 
the  difference  is  marked  and  in  Entosjjhenus  it  is  maximal.  In  shallow- 
water  forms  such  as  Lampetra  fluviatilis  and  the  brook  lampreys,  the 
two  types  are  found  in  apjaroximately  equal  numbers,  while  in  those 
which  live  in  deeper  waters  {Petromyzon  marinus,  etc.)  and  presumably 
demand  greater  sensitivity  to  light,  the  short  greatly  outnumber  the 
long  (Figs.  281  and  282). 

The  existence  of  a  duplex  mechanism  in  the  retina  has  not  always  been 
accepted  and  the  nature  of  the  cells  has  long  been  called  in  ciuestion.  Heinrich 
Miiller  (1857)  who  first  studied  the  subject  in  L.  fluviatilis,  differentiated  the 


Fig.  281. — The  Visual  Cells  of  the 
Atlantic     Lamprey,      PET/to.vrzoy 

MARIXVS. 

Showing  the  "  long  "'  and  the 
"  short  "  elements  (  X  1,000)  (Gordon 
Walls). 


Fig.  282. — The  Visual  Cells  of  the 
New  Zealand  Lamprey,  Geotria 
australia. 

There  are  three  types  of  cell  in 
apjDroximately  equal  numbers,  one 
plump  (to  the  left),  one  slender  (to  the 
right)  and  an  intermediate  type 
(middle)  with  a  eosinophobic  ellipsoid 
(  X  1,000)  (Gordon  Walls). 


two  types  of  cell,  and  while  initially  he  called  them  both  cones,  he  later  (1862) 
suggested  that  the  short  elements  were  rods.  Since  his  time  every  possible 
suggestion  has  been  made — that  both  cell-types  are  rods  (Schultze,  1866-71  ; 
Franz,  1932)  ;  that  both  are  cones  (Kohl,  1892)  ;  that  the  cells  are  neither  rods 
nor  cones  but  primitive  and  undifferentiated  in  type  (Plate,  1924  ;  Diicker, 
1924);  that  the  long  cells  are  cones  and  the  short  rods  (Walls,  1935);  or — the  view 
of  the  majority  of  workers — that  the  long  cell  is  a  rod  and  the  short  a  cone 
(W.  Krause,  1868-76  ;  Langerhans,  1873-76  ;  Greeff,  1900  ;  Tretjakoff,  1916  ; 
R.  Krause,  1923).  Most  of  the  evidence  brought  forward  in  support  of  these 
divergent  views  is  morphological  in  nature — a  somewhat  dangerous  basis  for 
the  differentiation  of  rods  and  cones. ^  The  demonstration  by  Kiihne  (1878) 
that  rhodopsin  is  present  in  the  retina  of  the  lamprey  proves  the  presence  of 
rods  ;  the  difference  in  the  two  types  of  cell  suggests  strongly  a  duplex  population; 

'  p.  251. 


270 


THE   EYE   IN   EVOLUTION 


but  the  presence  of  a  dendritic  foot-piece  in  the  long  cells  and  a  smooth  knob  in 
the  short  (Tretjakoff,  1916)  as  well  as  the  comjoarative  and  taxonomic  evidence 
collected  by  Walls  (1935),  provide  weighty  evidence  in  favour  of  Heinrich 
Midler's  original  suggestion  that,  desj^ite  their  length,  the  long  elements  are 
probably  cones  and  the  short,  rods.  At  the  present  time,  as  was  suggested  by 
W.  Miiller  (1875)  and  maintained  by  Franz  (1934),  it  may  be  safer,  while 
admitting  the  presence  of  two  morphologically  different  types  of  cell,  to 
refrain  from  dogmatic  differentiation  until  more  conclusive  evidence  derived 
from  their  histochemistry  or  neural  connections  is  available. 

The  oj)tic  nerve  is  primitive,  consisting  (unlike  that  of  Fishes)  of 
non-myehnated  fibres  (Briiesch  and  Arey,  1942)  ;  as  occurs  in  the 
human  embryo  there  is  no  septal  system  but  merely  an  axial  column 

Figs.  283  and  284. — The  Optic  Nerve  of  Cyclostomes. 


Fig.     28,3. — The    optic    nerve    of    the 
ammoeopte  larva  (after  Studnicka). 


Fig 


284. — The  optic  nerve  of  Lumpetra 
fluvintili.s  (after  Diicker). 


In  both  cases  there  is  no  sejital  system  but  merely  an  axial  column  of 
ependymal  cells  running  down  the  centre  of  the  nerve  sending  processes 
radiating  to  the  surface. 

d,  dural  sheath  ;  pa,  pia  arachnoid  sheath  ;  n,  nerve  fibres  ;  e,  epen- 
dymal cells  sending  out  radiating  processes  ;   oa,  ophthalmic  artery. 


of  cell-bodies,  probably  ependymal  in  nature,  running  down  the  nerve, 
each  sending  processes  radiating  to  the  sm-face  forming  a  primitive 
oligodendroglial  system  (Deyl,  1895  ;  StMnicka,  1912  ;  Keibel,  1928  ; 
Walls,  1942  ;  Prince,  1955)  (Figs.  283  and  284).  The  chiasma  remains 
within  the  brain  and  in  it  the  optic  nerves  cross  as  separate  individuals 
without  division  into  fascicles  or  bundles. 

THE  EXTRA-OCULAR  STRUCTURES  of  the  eye  of  the  lamprey  are 
simple.  Contrary  to  the  configuration  found  in  all  other  Vertebrates, 
there  is  no  skeletal  orbit,  but  the  organ  lies  in  a  simple  connective - 
tissue  ca     -de.    The  orbits  and  the  eyes  are  laterally  placed  so  that  no 


CYCLOSTO:\IES 


271 


binocular  field  is  possible.  The  rectus  muscles  are  largely  blended 
together  and  are  inserted  into  the  globe  as  a  ring  around  the  periphery 
of  the  cornea  ;  the  inferior  oblique  arises  in  common  with  the  internal 
rectus,  and  the  superior  oblique,  identifiable  only  by  its  nerve-supply, 
is  inserted  into  the  infero-tem}Doral  quadrant  of  the  globe.  The  nerve- 
supply  to  the  muscles  corresponds  to  the  scheme  common  to  all 
Vertebrates  (including  man)  except  that  the  sixth  cranial  nerve  appears 
to  supply  the  inferior  as  well  as  the  external  rectus  ;  it  may  be, 
however,  that  the  trunk  contains  fibres  derived  from  the  third  nucleus. 
The  most  interesting  feature,  however,  is  the  coknealis  muscle,  a 


Fig.  285. — The  Cornealis  Muscle  of  the  Lamprey. 

The  cornealis  muscle,  c,  running  horizontally  outside  the  orbit  on  the 
caudal  aspect  of  the  globe,  showing  its  insertion  into  the  cornea  (Mallory"s 
phospho-tungstic  acid  hsematoxylin)  (  ;     44)  (Katharine  Tansley)  (cf.  Fig.  276). 


massive  muscle  arising  outside  the  orbit  on  the  caudal  aspect  and 
inserting  into  the  transparent  dermal  cornea  (Tretjakoff,  191G)  (Fig. 
285)  ;  its  function  is  accommodative,  dra\\ing  this  element  of  the 
cornea  taut  and,  in  so  doing,  flattening  the  scleral  cornea,  pressing  the 
lens  backw  ards  towards  the  retina  and  thus  rendering  the  normally 
myopic  eye  {■ — 8  dioj^tres)  ennnetropic  or  even  hypermetropic.  Unlike 
man,  the  lamprey  thus  accommodates  for  distant  vision. ^  An  accom- 
modative mechanism  acting  by  deforming  the  globe  from  the  outside 
is  among  Vertebrates  unique  to  the  lamprey. 


Bruesch  and  Arey.     J.  com  p.  Xeui-ol..  77, 

631  (1942). 
Capraro.     Arch.  ital.  Anat.  Embriol..  32, 

491  (1934)  ;   38,  1  (1937). 
Monit.  Zool.  iluL,  45,  Suppl.  97  (1935). 
Carridre.     Die  Schorgane  der  Thieve,  vergl.- 

anat.  dargestellte,  Mlinchen  (1885). 
Deyl.       Bull,     intern.    Acad.    Sci.    Enip. 

Francois  Joseph  I,  Prague  (1895). 
Diicker.     Jena.   Z.  f.  Naturwiss.,  60,  471 

(1924). 
Franz.     Zool.  Jb.,  Alt.  Zool.  Physiol,  52, 

118  (1932). 
Bolk's  Hb.  d.  vergl.  Anal.  d.  Wirbelticn, 

Berlin,  2  (ii),  997  (1934). 
Greeff.     Graefe-Saeniiscli  Hb.  ges.  Aiigen- 

heilk.,  Leipzig,  II,  1  (2),  Kap.  5,  74 

(1900). 


Hageeloorn.      ArcJi.   AugenheilJ:.,   102,    33, 

393  (1930). 
Haller.    Opera  anatomici  mi)ujra,  3  (1768). 
Hawes.     Quart.  J.  micr.  Sci.,  86,  1  (1946). 
Hein.      T.    ned.    Dierk.    Vereen,    12,    238 

(1913). 
Henckel.        Bol.     Soc.     biol.     Concepcion, 

Chile,  19,  69  (1944). 
Keibel.      Z.   mikr.  Anat.   Forsch.,  12,  391 

(1928). 
Kohl.     Das  Auge  von  Peiromyzon  planeri 

iind    von    Myxine    glutinosa,    Leipzig 

(1892). 
Bibl.  zool,  4  (13)  (1892). 
Krause,   R.     Mikr.   Anat.   d.    Wirbelliere. 

IV,  Berlin  (1923). 
Krause,  W.    Nacltriclilen  Ges.  Wiss.  G.  A. 

Unir.  f.'ottingen.  23,  484  (1868). 

644. 


272 


THE   EYE   IN   EVOLUTION 


Krause,  W.     Arch.   7nikr.   Anat.,  12,   742 

(1876). 
Kuhne.     tlntersuch.  a.  d.  physiol.  Inst.  d. 

Univ.  Heidel,  1,  1,  15,  119,  341,  370 

(1877-78). 
von  Kupffer.     Studien  zur  vergl.  Entwick- 

lungsgeschichte  d.  Kopfesd.  Kranioten  : 

II  Die  Entwicklung  d.  Kopfes  v.  Am- 

vwcoetes  planeH,  Munich  (1894). 
Langerhans.      Vers,  dtsch.  Naturf.  Aerzte, 

Wiesbaden,  Sept.   Atiat.   Physiol.,   69 

(1873). 
Ber.   Verh.  naturj.  Ges.  Freiburg.,  6(3), 

1  (1876). 
Mann.      The   Development   of  the   Human 

Eye,  London,  274  (1928). 
Mawas  and  Magitot.     Arch.  Anat.  micr., 

Paris,  14,  41  (1912). 
Miiller,  H.     Z.  wiss.  Zool.,  8,  1  (1857). 

Wurzburg.  naturwiss.  Z.,  3,  10  (1862). 
Miiller,  W.     Beit,  zur  Anat.  und  Physiol. 

(Festgabe     C.     Ludwig),     Leipzig,     2 

(1875). 
Plate.    Allgemeitie  Zool.  u.  Abstammungs- 

lehre,  Jena,  2  (1924). 


Prince.    J.  comp.  Neurol.,  103,  541  (1955). 
Robertson.     Biol.  Rev.,  32,  156  (1957). 
Rochon-Duvigneaiid.       Les     yeux    et     la 

vision  des  vertebres,  Paris,  183  (1943). 
Schultze.       Arch.     mikr.     Anat.,    2,     175 

(1866)  ;    3,  215  (1867). 
Strieker's  Hb.  d.  Lehre  v.  d.  Geweben  d. 

Menschen    ii.    d.     Thieve,    Kap.     26, 

Leipzig  (1871). 
Steven.    J.  exp.  Biol,  27,  350  (1950). 
Quart.  J.  micr.  Sci.,  92,  233  (1951). 
Stockard.    A^ner.  J.  Anat.,  6,  511  (1907). 
Studnicka.    Anat.  Anz.,  41,  561  (1912). 
Tretjakoff.        Bull,     physico-math.     Dept. 

Imp.  Novoross.  Univ.,  Odessa  (1916). 
Treviranus.     Vertnischte  Schriften  anat.  u. 

physiol.  Inhalts,  Bremen,  3  (1820). 
Walls.     Brit.  J.  Ophthal.,  19,  129  (1935). 
The     Vertebrate     Eye,     Michigan,     555 

(1942). 
Walls  and  Judd.      Brit.  J.   Ophthal.,  17, 

641  (1933). 
Young.    J.  exp.  Biol.,  12,  229  (1935). 


CHAPTER  XI 
THE  EYES  OF  FISHES 

No  book  on  the  comparative  anatomy  and  physiology  of  the  eye  would  be 
complete  withovit  a  tribute  to  victor  julius  franz  (1883-1950)  (Fig.  286). 
The  son  of  a  famous  astronomer  in  Konigsberg,  he  worked  successively  in  Ziirich, 
Breslau,  Halle,  Frankfurt,  Leipzig  and  Jena  where  he  occupied  the  Chair  of 
Phylogeny  at  the  Ernst -Haeckel-Havis  until  after  the  World  War  when,  in  1946, 
he  was  relieved  of  his  post  owing  to  his  political  associations  with  the  Nazi 
party.  From  the  time  he  gained  his  doctorate  thesis  on  the  anatomy,  histology 
and  function  of  the  eyes  of  Selachians  in  1905,  his  scientifle  output  was  con- 
tinuous until  1944,  and  included  such  subjects  as  the  anatomy  of  the  eyes  of 
Invertebrates  and  Vertebrates,  particularly  Acrania  and  Fishes,  the  anatomy 
and  function  of  the  brain  of  Fishes,  the  structure  and  function  of  jDigment  cells, 
investigations  into  ocvilar  functions  such  as  phototaxis,  accommodation  and  the 
light  sense  of  a  vast  number  of  species,  and  a  wide  range  of  other  kindred  subjects. 
His  systematic  writings  were  also  prolific,  on  comparative  anatomy,  evolutionary 
processes  and,  above  all,  on  the  structure  and  function  of  the  organs  of  sight 
in  the  animal  world. 

Compared  with  Cyclostomes,  true  fishes  show  many  and  con- 
siderable advances  not  only  in  their  general  structure  as  in  the  presence, 
among  other  things,  of  jaws,  limbs  (fins)  and  an  exo-skeleton  of  scales 
from  which  teeth  are  derived,  but  also  in  their  eyes  which  are  more 
fully  differentiated. 

The  general  co7ifignration  of  the  eyes  of  Fishes  exhibits  structural 
characteristics  which  might  at  first  sight  appear  to  be  peculiarities  but 
most  of  them  depend  on  the  requirements  of  vision  in  water  :  it  is  to 
be  remembered  that  the  vertebrate  eye  initially  evolved  as  an  under- 
water visual  organ  (Figs.  287  to  291). 

In  general,  the  globe  is  large,  its  size  tending  to  vary  with  the 
depth  at  which  the  animal  lives  ;  as  a  rule  deep-sea  fishes  are  provided 
with  large  eyes  to  receive  as  much  light  as  possible  in  these  dim 
regions — until,  indeed,  the  absence  of  light  in  benthonic  depths  leads  to 
the  degeneration  of  the  entire  organ. ^  When  a  change  of  habitat 
occurs  during  development  the  size  of  the  globe  may  vary  accordingly  ; 
thus  the  sunfish,  Banzariia  truncata.  spends  its  larval  life  at  great 
depths  at  which  stage  the  eyes  occupy  one-quarter  of  the  area  of  the 
body,  but  when  the  adults  come  to  spend  their  lives  near  the  surface 
their  eyes  become  relatively  quite  small  in  maturity.  A  corresponding 
change  occurs  in  the  eye  of  the  eel,  Ang^iilla.  which  grows  to  a  relatively 
enormous  size  before  it  migrates  from  its  river  habitat  to  breed  and 
die  in  the  Atlantic  ocean. 

1  p.  722. 

S.O.— VOL.  I.  273  18 


274 


THE   EYE   IN   EVOLUTION 


Fig.  286.— Victor  Julius  Franz  (1883-1950). 


FISHES 

Figs.   287  to  291. — The  Eyes  of  Typical  Fishes. 


275 


Fig.     287. — The    sturgeon,    Acipenser 
sturio  {Chondrostean). 


..-^^r^ 


'% 


tA 


Fig.   288.- 

-The  pike, 

Eso.r 

lucius 

(Teleostean). 

^ 

>^!' 

J5>> 

Fig.   289. — The  cod.  Gndus  morrhna  (Teleostean). 


Fig.   290. — The  ray.  Raja  clavata 
(Selachian). 


Fig.    291.— The    dogfish,   Squaluf 
aranthias  (Selachian). 


(Reproductions  of  five  of  the  beautiful  engravings  of  D.  W.  Soenimerring, 
1818.  The  reproductions  are  life-size  and  each  represents  the  lower  half  of  a 
horizontal  section  of  the  left  eye.) 

Vision  under  water  requires  an  eye  relatively  hypermetropic  to 
vision  in  air  ;  moreover,  the  resistance  of  water  while  swimming  is 
considerable  and,  therefore,  as  an  optical  and  a  streamlining  device 
particularly  among  actively  swimming  fishes,  the  tendency  is  towards 
a  flattening  of  the  anterior  segment  of  the  globe.    The  typical  section 


276  THE   EYE   IN   EVOLUTION 

of  the  fish-eye  is  therefore  elhpsoidal  with  the  shortest  diameter  the 
visual  axis  (Figs.  292  and  365)  ;  only  in  sluggish  forms  such  as  the 
bow-fin,  Amia,  does  the  globe  become  spherical.  The  maintenance  of 
a  non-spherical  shape  in  the  face  of  changes  in  pressure  which  may  be 
considerable  necessitates  a  sturdy  outer  coat  ;  the  sclera  therefore 
tends  to  be  thick  and  is  typically  reinforced  with  a  supporting  layer 
of  cartilage  sometimes  supplemented  by  bone. 

The  flattening  of  the  anterior  segment  implies  a  flat  cornea  ;   but 
in  a  watery  medium  this  structure  is  in  any  case  useless  as  a  refracting 


Fig.  292. — The  Eye  of  the  Trout. 
Note  the  flat  shape  with  the  short  antero-iDosterior  axis. 

agent.  Perfection  in  its  optical  properties  is  thus  neglected  ;  it  is 
therefore  often  irregular  and  even  ridged,  and  in  the  interests  of  strength 
is  frequently  thin  centrally  and  thick  in  the  jDeriphery  giving  it  the 
construction  of  a  sturdy  arch.  It  follows  that  the  entire  responsibility 
for  refraction  falls  upon  the  lens.  The  lens  of  fishes  is  consequently 
enormously  large  and  almost  spherical  with  a  highly  refractive  nucleus 
and  higher  total  refractive  index  (1-649  to  1-653)  than  in  any  other 
Vertebrate,  making  a  maximal  difference  between  it  and  the  refractive 
indices  of  the  other  media.  With  the  elimination  of  the  cornea  from 
the  dioptric  system  and  the  dependence  on  the  lens  for  refraction,  it  is 
necessary  that  a  constant  proportion  should  exist  between  the  size  of 
the  leii  ■  and  its  distance  from  the  retina  ;  Matthiessen  (1886),  indeed, 
showed  Miat  this  is  so,  that  the  eyes  of  fishes,  no  matter  what  their 
size  ail  liape,  are  standardized  in  their  configuration,  the  distance 
from  th'.       ntre  of  the  lens  to  the  retina  being  constant  (radius  of  lens 


FISHES 


277 


X  2-55  =  Matthiessen's  ratio).  The  lens  has  not  only  a  light-refracting 
function,  but  in  the  absence  of  an  optically  effective  cornea,  it  must 
also  assume  the  onus  of  light -gathering.  It  is  therefore  typically 
situated  far  forward  in  the  globe,  bulging  through  the  pupil  and 
approximating  the  cornea.  This  large  anteriorly-situated  lens  being 
an  optical  necessity,  all  other  considerations  of  general  configuration 
give  place  to  it,  and  in  cases  wherein  the  globe  would  become  too 
large  to  accommodate  a  lens  of  the  required  dimensions,  as  in  some 
dec;  _?a  types  frequenting  an  almost  lightless  habitat,  the  shape  of 
the  eye  is  changed  from  the  ellipsoidal  to  a  tubular  form  so  that 
the  large  lens  can  remain  at  the  required  distance  from  the  retina 
(Fig.  380). 

The  large  spherical  lens  makes  accommodation  by  its  deformation 
impossible,  so  that  where  an  accommodative  mechanism  exists  the 
expedient  is  adopted  of  moving  the  lens  forwards  or  backwards — 
towards  the  cornea  in  the  hypermetropic  Selachians  so  that  they 
accommodate  for  near  vision,  towards  the  retina  in  myopic  Teleosts 
so  that  they  accommodate  for  distance.  The  ciliary  region  is  thus 
more  specialized  than  in  C!yclostomes  giving  rise  to  a  suspensory 
apparatus  for  the  lens  and  different  tj'jjes  of  muscular  structures  to 
effect  these  changes  in  its  position. 

The  necessity  of  making  as  much  use  of  the  relatively  small 
amount  of  light  available  in  most  watery  habitats  (apart  from  abyssal 
depths  where  no  light  is  available)  has 
led  to  the  jacketing  of  the  uvea  of  most 
pelagic  and  surface  fishes  with  a  mirror- 
like arrangement  of  guanine  crystals  to 
form  the  argentea,  while  the  choroid  of 
Selachians  is  provided  with  a  tapetum 
lucidum  ;  an  alternative  seen  in  certain 
Teleosteans,  is  a  similar  deposition  of 
guanine  crystals  in  the  jjigment  epithe- 
lium (the  retinal  tapetum). 

While  these  form  the  main  struc- 
tural characteristics  of  the  eyes  of 
Fishes,  other  advances  are  seen  in  com- 
parison with  those  of  Cyclostomes, 
particularly  the  presence  of  an  iris 
musculature  so  that  the  structure  be- 
comes mobile,  a  considerably  greater 
elaboration  of  the  visual  cells  and  the 
retinal  structure,  and  myelination  of 
the  optic  nerve  fibres  and  the  provision 
of  septa  within  the  optic  nerve  itself. 


Ant 


ON 


-apex 


SIR 


Fig.  293. — The  General  Scheme 
OF  Fish  Muscles  (seen  from  the 
DoRS.\L  Aspect). 

Ant,  anterior  part  of  orbit  ;  apex, 
apex  of  orbit  ;  LR,  lateral  rectus  ; 
MR,  medial  rectus  ;  O,  superior 
(and  inferior)  oblique  ;  ON,  optic 
nervp  ;  SIR,  superior  (and  inferior) 
rectus. 


278  THE   EYE    IN   EVOLUTION 

As  in  all  Vertebrates  below  Mammals  the  decussation  of  the  optic 
nerve  fibres  at  the  chiasma  is  total. ^  An  area  centralis,  exceptional  in 
Selachians,  is  commonly  seen  in  Teleosteans  and  in  a  number  of 
particularly  agile  littoral  types  of  this  class  a  fovea  is  present. 

The  ocular  movements  in  Fishes  are  in  general  restricted,  reflex 
and  primitive,  and  the  extra-ocular  muscles  are  essentially  designed 
to  subserve  rotations  of  the  eyes  compensatory  to  movements  of  the 
body  ;  with  few  exceptions  ^  fixation  is  attained,  not  by  movements 
of  the  eyes  but  of  the  body  in  swimming.  The  muscles  are  therefore 
designed  to  subserve  merely  the  simple  rotations  required  by  the 
postural  mechanism  ;  the  recti  form  a  cone  arising  from  the  apex  of 
the  orbit,  and  the  obliques,  subserving  simple  wheel-rotations,  arise 
anteriorly  and  remain  on  a  plane  anterior  to  the  recti  (Fig.  293). 

The  super-class  of  Fishes  includes  an  enormous  number  of  forms,  many  of 
them  long  since  extinct  ;  the  extant  types  may  be  divided  into  two  main  classes^  : 

(a)  CHONDRiCHTHYES  ()(6v8pos.  Cartilage  ;  l^dvs,  a  fish)  (or  elasmobranchs 
— eAaa/i,o9,  a  metal  plate  ;  branchia,  a  gill  ;  so  called  because  of  their  lamelliform 
gills)  with  a  cartilaginous  skeleton,  and 

{b)  OSTEICHTHYES  (dcTTeov,  bone ;  l^Ovs,  a  fish)  with  a  more  or  less  ossified 
skeleton. 

CHONDRICHTHYES  (or  cartilaginous  fishes)  are  represented  today  only  by 
two  sub-classes — the  selachii  (CTeAa;;^os',  a  cartilaginous  fish)  which  include  the 
families  of  sharks  and  skates  or  rays,  and  the  holocephali  (oAo?,  whole  ; 
K€<f)C/.Xrj,  a  head),  such  as  the  Chimcera. 

OSTEICHTHYES  *  (or  bony  fishes)  form  a  much  more  heterogeneous  class. 
With  the  exception  of  the  relatively  inodern  Teleosteans,  most  types  are  largely 
extinct  and  are  now  represented  by  few  species,  but  all  of  them  flourished  in 
large  numbers  in  ancient  times.    The  class  is  conveniently  divided  into  6  groups. 

The  DIPNOI  (  St?,  twice  ;  771^017,  breath)  (lung-  or  mud-fishes)  are  a  very 
ancient  form  abundantly  represented  by  fossils  in  the  Mesozoic  beds  throughout 
the  world  but  today  found  sporadically  as  three  genera  only  in  Eastern  Australia, 
in  the  marshes  of  Africa  and  the  swamps  of  the  Amazon  basin.  Their  skeleton 
is  largely  cartilaginous  and  their  name  is  derived  from  their  double  method  of 
breathing,  for  their  air-bladder  is  developed  to  form  a  breathing  lung. 

The  ccELACANTHiNi  are  represented  today  only  by  one  living  species — 
Latimeria,  a  fish  thought  to  have  disappeared  80,000,000  years  ago  but  recently 
discovered  in  the  coastal  seas  of  south-east  Africa.  The  Coelacanths  are 
characterized  by  a  skeleton,  part  bone,  part  cartilage,  basal  skeletal  supports 
formed  by  a  solid  projecting  lobe  on  which  the  fringe-like  pectoral  Und  pelvic 
fins  are  set. 

The  CHONDROSTEi  {-^ovhfjos,  cartilage  ;  oGrdov  bone) — fishes  with  a  cartila- 
ginous internal  skeleton — are  represented  today  only  by  a  few  species  of 
sturgeons  and  the  polypterini  (tvoAl'?,  many;  irrepov,  awing)  which  have  a  series 
of  finlets  instead  of  a  dorsal  fin.  The  latter  survive  as  two  types  found  in  African 
rivers  {Polypterus  or  bichir,  and  C alamo ichthys).  The  skeleton  is  very  bony, 
and  till  bilobed  air-bladder,  the  duct  of  which  opens  ventrally  into  the  pharynx, 

^  i".;o,  however,  some  Reptiles  which  form  an  exception  (p.  392). 
2  p.  «93.  »  p.  234. 

*  E;  'uding  Dipnoi  and  Teleostei  this  large  class  used  to  be  known  as  ganoids 
iyavos,  li.       ')  on  account  of  their  ganoin-coated  scales. 


FISHES  279 

functions  as  an  air-breathing  lung.  Although  the  C'hondrostei  ai'e  thus  largely 
extinct,  their  descendants  comprise  most  of  the  modern  fishes. 

The  HOLO.STEI  (oAo?,  whole  ;  oareov,  bone),  another  ancient  off-shoot  of 
the  primitive  Chondrosteans  dating  from  the  Permian  era,  are  represented  only 
by  two  extant  species  found  in  X.America,  the  gar-pike  {Lepidosteus)  and  the  bow- 
fin  {Amia);  they  are  characterized  by  the  completeness  of  their  bony  skeleton. 

The  TELEOSTEi  (reAeo?,  complete  ;  oareov,  bone)  or  modern  bony  fishes, 
probably  stand  in  a  continuous  genetic  line  with  the  Holosteans  and  include  the 
vast  majority  of  fishes  now  alive — some  20,000  si^ecies.  They  date  from  Jurassic 
times,  and  because  of  their  high  differentiation  probably  began  to  assume  their 
overwhelming  preponderance  as  inhabitants  of  the  seas  in  the  later  Cretaceous 
and  Tertiary  epochs.  As  would  be  imagined  they  exhibit  the  most  fully  developed 
and  specialized  eyes  of  all  fishes. 

We  shall  first  discuss  in  some  detail  the  characteristics  of  the  eyes  of  the 
species  at  each  end  of  the  scale — the  relatively  simple  eyes  of  Selachians  and 
the  highly  developed  eyes  of  Teleosteans,  and  thereafter  note  the  essential 
differences  in  the  intermediate  classes. 

Chondrichthyes  (Elasmobranchii) 

The  Selachian  Eye 

THE  SELACHIANS  are  divided  into  two  orders,  between  which,  however,  the 
eyes  differ  little — (i)  an  older  group  of  fusiform-shaped  fishes,  the  euselachii, 
comprising  the  sharks  and  their  relative,  the  dogfish  (Fig.  294),  and  (ii)  the 
BATOiDEi,  modified  forms  with  flattened  bodies  comprising  the  skate-ray- 
torpedo  group  (Figs.  295  and  296).  All  are  voracious  carnivorous  fishes  with 
cartilaginous  skeletons,  and  with  few  exceptions,  such  as  the  fresh-water  saw- 
fish, Pristis,  marine  in  habitat.  Most  of  them  are  of  benthonic  habits  and 
their  eyes  are  therefore  specifically  adapted  for  dim  illumination  ;  occasionally 
in  abyssal  forms  which  frequent  the  sea-bottom,  the  eyes  have  become  vestigial 
and  blind  as  in  the  deep-sea  rays,  Benthobatis,  Typhlonarke  and  Bengalichthys.^ 

The  general  configuration  of  the  eye  is  simple  with  the  tj^Dical 
ellipsoidal  shape  and  the  scleral  cartilage  found  generally  in  fishes 
(Figs.  297-9).    The  main  selachian  characteristics  are  : 

a  thick  ejyichoroid  on  the  outer  surface  of  the  choroid,  somewhat 
reminiscent  of  that  seen  in  the  lamprey,  and  icithin  the  choroid  an  u7iusuaUy 
elaborate  tapetum  lucidum,  a  structure  which  {unlike  the  tapetum  of  Teleo- 
steans) has  a  vi sued  function  in  dim  illuminations  ; 

a  ciliary  zone  provided  with  antero-posterior  folds  giving  rise  dorsally 
to  a  suspensory  ligament  of  the  lens  and  ventrally  to  a  cushion-like  papilla 
provided  ivith  an  ectodermal  protractor  lentis  mivscle  ; 

a  sluggishly  mobile  iris  provided  ivith  primitive  sphincter  and 
dilatator  muscles,  at  this  stage,  hoivever,  autonomously  contractile  and 
without  a  nerve  supply  ; 

a  shallow  anterior  chamber  icithout  an  annular  ligament  {as  in  the 
lamprey),  without  a  pectinate  ligayne^it  or  other  structures  in  the  free  angle, 
and  without  a  cajial  of  Schlemm  ; 

1  p.  724. 


Pristis 


280 


THE   EYE    IN   EVOLUTION 

Figs.   294  to  296. — Typical  Selachian  Fishes. 


Fig.   294. — -The  dogfish,  Scylliorhinus  canicula. 


Fig.   295. — The  thorziback  ra\',  Raja  clavata  (swimming) 


^^^  .^-      T    ,         .-.-1  ^        ».Af-^-v.  m 


^^  iF^  *  .*  ■•••»*  «  •  •  •  •    •*  *  .  -        ^^ 


■;;*;  •  i 


•  • 


•  #  * 


^,i^iPr""i^ 


Fig.  2!){). — The  sjDotted  ray,  Rajd  montagui  (resting  on  the  bottom)  (photo- 
graphs by  Douglas  P.  Wilson). 


FISHES 


281 


o  retina  without  blood-vessels  {in  the  ad^dt)  and,  icith  few  excejttions, 
•provided  only  with  rods  ; 

an  optic  nerve  jnovided  with  myelinated  nerve  fibres  and,  in  some 
species,  an  axial  core  of  ependymal  cells  resembling  the  arrangement  in 
lampreys  ; 

a  cartilaginous  orbit  within  ivhich  the  globe  is  supported  by  an  optic 
pedicle,  also  of  cartilage. 


THE  GLOBE  is  iisiially  large  in  the  sharks,  smaller  in  the  upward- 
looking  Batoidei,  and  varies  with  the  depth  of  the  habitat — in  general, 
the  deeper  the  habitat,  the  larger  the  eye.  as  is  exemplified  in  the 
enormous  eyes  of  some  deep-sea  sharks  {Etmopterus)  ;  the  dorsal  eyes 
of  rays  are  generally  small. ^  The  cornea  is  more  highly  curved  than  is 
seen  in  other  fishes,  and  is  usually  oval  in  shape  with  the  long  axis 
horizontal  ;  it  contains  all  the  layers  characteristic  of  the  mammalian 
cornea  with  a  thick  epithelium  derived  from  the  skin.  Bowman's  and 
Descemet's  membranes,  the  latter  with  an  endothelium,  and  a  neatly 
laminated  substantia  propria  which,  how^ever,  tends  to  become  con- 
siderably thinner  centrally  (Strampelli,  1934  ;  Loewenthal,  1938).  It 
is  pigmented  peripherally  in  some  species,  particularly  in  its  upper 
part,  probably  as  a  protection  against  light  (e.g.,  Torpedo),?i,nd  receives 
a  rich  nerve-supply  (Shearer,  1898).  The  sclera  varies  considerably  in 
thickness,  being  very  thick  in  the  largest  sharks;  the  fibrous  outer  half 
is  supported  by  a  firm  and  complete  cartilaginous  cup  on  the  inner 
aspect  extending  from  the  optic  nerve  behind  to  the  corneal  margin 
anteriorly  (Yatabe,  1932).  Sometimes  this  becomes  calcified,  and  in 
one  shark  {Lc^margus)  the  scleral  cartilage  sends  large  processes  into 
the  choroid. 

The  uveal  tract  presents  features  both  interesting  and  distinctive  ; 
it  is  the  only  vascularized  tissue  within  the  globe  of  the  adult  ( Virchow, 
1890).  The  vascular  part  of  the  choroid  is  typical  in  structure,  the 
choriocapillaris  being  supplied  by  an  artery  which  enters  on  the 
temporal  side  of  the  globe  and  drained  by  two  main  veins,  one  ventral 
and  one  dorsal.  On  its  outer  aspect  is  a  heavily  vascularized  epichoroid 
of  connective  tissue,  sometimes  cavernous  in  its  structure,  particularly 
marked  near  the  posterior  pole  so  that  the  optic  nerve  has  an  mtra- 
choroidal  course  of  several  millimetres.  Between  these  two  layers  the 
centre  of  the  choroid  is  occupied  by  the  tapetum  lucidum,  a  structure 
carried  forwards  in  a  much  less  marked  form  onto  the  anterior  surface 
of  the  iris. 

The  TAPETUM  LUCIDUM  of  Selachians  is  a  remarkable  structure 
and  is  found  in  all  forms  except  some  benthonic  sharks  (Lamargus) 


Torpedo 


Lcemargus 


1  The  dorso-lateial  eyes  of  the  eagle -ray,  Myliobutis,  are,  however,  quite  large. 


282 


THE   EYE   IN   EVOLUTION 


Figs.   297  to  299. — Selachian  Eye^ 


Fig.  297. — Diagram  of  a  Euselachiaii  Fig.  298.— Diagram  of  a  Batoid  eye. 

eye. 

CF,  ciliary  fold  ;  Ch,  choroid  ;  CP,  ciliary  papilla  ;  Ec,  epichoroid  ; 
ON,  optic  nerve  ;  P,  optic  pedicle  ;  S,  sclera  with  complete  cartilaginous  oiip  ; 
SL,  suspensory  ligament. 


Fig.   299. — The  eye  of  the  dogfi.sli. 

Tlie  retina  has  been  torn  at  the  ora  and  the  uvea  detached  in  the  ciliarj' 
zone.  In  the  section  the  iris  seems  to  adhere  to  the  back  of  the  cornea.  Note 
the  great  thickness  of  the  corneal  eiDithelium  and  the  well-fornied  eyelids  ;  the 
latter  f-ature  is  unique  to  Selachians  among  Fishes  (  X  20)  (Norman  Ashton). 


FISHES 


283 


and  rays  {Myliobatis)  and  the  basking  shark  {Selache  maxima).  It  was 
know  to  Soemmerring  (1818)  and  has  been  most  fully  studied  by  Franz 
(1905-34).  Structurally  it  is  made  up  of  two  elements,  highly  reflecting 
cells  packed  with  guanine  crystals,  and  heavily  pigmented  melanophores. 
In  some  species  such  as  the  porbeagle  shark.  Lamna  cornubica,  the 
guanophores  lie  in  parallel  layers,  the  interstices  between  them  being 
occupied  by  melanophores.  In  the  more  typical  arrangement,  however, 
the  flat  silvery  guanophores  are  arranged  as  a  series  of  plates  running 
in  a  slanting  direction  to  the  choriocapillaris,  and  over  them  the 
chromatophores  send  pigmented  processes.  The  arrangement  as 
depicted  by  Franz  is  seen  in  Fig.  300.     In  dim  illumination  the  pig- 


Fig.  300. — The  Tapetum  Lucidum  of  the  Dogfish,  Mr.<Ti:LLs. 

In  vertical  section,  from  the  dorsal  part  of  the  fundus. 

C,  choriocapillaris  ;  PE,  pigment  epithelium  ;  PC,  pigmented  layei-  of  the 
choroid  ;  V,  vessels  of  the  choroid  ;  P,  pigmented  cells,  the  processes  of 
which  (Pr)  migrate  over  the  tapetal  plates  (T)  (after  Franz,  1931). 


MyUohatid 


Selache 


mentary  processes  are  retracted  and  the  guanophores  appear  as  a 
silvery  row  of  plates  like  the  tiles  on  a  roof  from  which  the  incident 
light  is  reflected  back  to  the  retina  ;  in  bright  illumination  the  pig- 
mented cells  send  down  their  migratory  processes  which  cover  the 
guanophores  so  that  all  the  incident  light  reaching  the  choroid  is 
absorbed. 

The  ciliary  zone  of  Selachians  has  some  unique  features.  It 
is  thin  and  without  musculature,  occupying  a  broad  belt  between  the 
retina  and  the  iris,  consisting  from  without  inwards  of  three  layers — a 
mesodermal  layer,  the  forward  continuation  of  the  choroid,  a  pigmented 
ectodermal  layer,  the  forward  continuation  of  the  pigmented  retinal 
epithelium,    and    a    non-pigmented    ectoderm;!.  1    layer,    the    forward 


Lamna 


284 


THE   EYE   IN  EVOLUTION 


Figs.  301  and  302. — The   Ciliary  Papilla   of  the  Dogfish,  Sctlliorhinus. 

I 


Fig 


301. — The  lens,  /,  is  seen  resting  on  the  papilla,  and  the  filaments  of 
the  zonule,  z,  are  seen  running  from  it  towards  the  ciliary  region.  The 
papilla,  p,  is  much  larger  than  the  ordinary  ciliary  processes,  cp,  and  the 
small  white  area  at  its  ajsex  represents  the  remains  of  the  foetal  fissure,  /. 
r,  retina. 


Fig.  302. — Drawing  of  a  section  through  the  ciliary  papilla.     The  papilla,  p, 
is  Keen  approximating  the  lens,  I.     s,  sclera  ;    z,  zonular  fibres. 


Massoi 


■wings  from  Rochon-Duvigueaud,  Les  Ycux  et  la  Vision  des  Vertebres, 
'  Cie.) 


FISHES 


285 


continuation  of  the  retina.  Anteriorly  its  inner  surface  is  broken  by 
low  ciliary  folds  ^  which  run  in  an  irregularly  radial  direction  onto  the 
posterior  surface  of  the  iris,  a  formation  restricted  in  some  species  of 
rays  to  the  dorsal  and  ventral  quadrants.  A  gelatinous  disc-like  zonule 
runs  from  the  coronal  region  of  the  ciliary  body  to  the  lens  near  its 
equator,  augmented  in  the  mid-line  dorsally  by  a  firmer  suspensory 
ligament,  and  ventrally  (in  most  species)  by  a  cushion-like  ciliary 
papilla  upon  which  the  lens  rests.  The  zonule  and  the  suspensory 
ligament  are  essentially  condensations  of  the  anterior  part  of  the 
vitreous  (Teulieres  and  Beauvieux,  1931).  The  ciliary  papilla,  which 
develops  in  the  lips  of  the  foetal  fissure  of  the  invaginating  optic  vesicle, 
resembles  a  hypertrophied  ciliary  fold,  and  is  continued  for  some 
distance  onto  the  back  of  the  iris  (Figs.  301-2);  it  is  said  to  contain 
smooth  muscle  fibres,  presumably  of  ectodermal  origin,  derived  from 
the  retinal  layer  of  the  ciliary  body,  so  orientated  that  it  acts  as  a 
protractor  lentis  muscle,  which  on  contraction  would  pull  the  lens 
forwards  on  accommodation  (Franz,  1931).  It  would  appear,  however, 
that  such  fibres  are  scanty  and  their  presence  has  been  denied  (Verrier, 
1930  ;   Rochon-Duvigneaud,  1943). ^ 

The  iris  is  thin  but  usually  extensive,  being  bowed  forwards  over 
the  protruding  lens.  Both  ectodermal  layers  are  pigmented  near  the 
pupillary  margin,  but  towards  the  ciliary  body  the  posterior  layer 
usually  loses  its  melanin  content  ;  pigmentation  of  tliis  layer  is  there- 
fore more  extensive  than  in  the  case  of  Cyclostomes,  and  in  some 
species  the  whole  of  this  layer  is  pigmented  (some  sharks — Lamna 
cornuhica — and  rays — Trygon,  etc.)  as  is  the  case  in  Teleosteans  and 
higher  Vertebrates.  From  the  anterior  layer  are  developed  the 
SPHINCTER  and  dilatator  muscles  of  the  pupil  which  have  received 
considerable  study  (Franz,  1905  ;  Gr\Tifeltt  and  Demelle,  1908  ;  L. 
Carrere,  1923).  They  are  comprised  of  long,  spindle-shaped  ecto- 
dermal cells  which,  acting  autonomously  and  directly  tlu-ough  the 
stimulus  of  light,  undergo  sluggish  and  delayed  contractions  (Brown- 
Sequard,  1847-59  ;  Young,  1933)  ;  they  are  more  primitive  than  those 
of  higher  vertebrate  types  in  that  the  elongated  myo -ectodermal  cells 
never  leave  their  parent  epithelial  layer.  It  is  interesting  that  in  some 
sharks  and  dogfishes  prolonged  exposure  to  light  may  lead  to  a  state 
of  "  mydriatic  rigor  "  wherein  the  pupil  remains  permanently  fixed 
{Mustelus,  Squalus).  The  mesodermal  layer  of  the  iris  is  thin,  contain- 
ing vessels  and  chromatophores  in  its  deeper  aspects,  and  in  its  anterior 
parts,  guanine-laden  cells,  not,  however,  arranged  in  packed  parallel 
layers  as  is  the  argentea  of  Teleosts,  but  in  sufficient  numbers  to  give 
the    iris   a    distinctly  metalHc  sheen.   In  the   angle    of  the   anterior 


Trygon 


Mustelus 


Squalus 


^  See  footnote,  p. 
»  p.  647. 


267. 


286 


THE   EYE   IN   EVOLUTION 


chamber  there  are  ill -developed  sinuses  lined  by  endothelium  (Rochon- 
Duvigneaud,  1943)  ;  it  may  be  that  these  allow  the  escape  of  aqueous 
humour  when  the  lens  is  pulled  forward  towards  the  cornea  in 
accommodation. 

The  pufjiUary  wperture  varies  and  is  largely  determined  by  the 

Ftos.   303  TO  313.— The  Pitils  of  Selachians. 


® 

Fro.   303.— The 

angel  shark, 

Sqnntina. 


Fig.   304.— The 
.school  shark, 
Oaleorhinns. 


Fig.   305.— The 

guinmy  shark. 

Must  el  us  antarctic  us. 


Fig.   306.— The 

nurse  shark, 
Gin  glym  ostoma . 


Fig.   307.— The 

dogfish, 
Mustelus  canis. 


Fig.   308.— The 

carpet  shark, 

Orectolobus. 


Fig.   309.— The 

leopard  shark, 

Triakis. 


Fig.   310.— The 

white -tip  shark, 

Carcharodon. 


Fig.  311. — The  crested  Port  Jackson 
shark,  H  eterodontus ,  pupil  dilated 
and  contracted. 


Fig.    312. — The   fiddler  ray,    Trygono- 
rhina,  pupil  dilated  and  contracted. 


Fig.  313.- 


<::::> 


-The  pupil  of  the  dogfish,  Scylliorhinus. 
traction  (after  Franz). 


Showing  stages  of  con- 


Heterodontus 


arrangement  of  the  musculature  of  the  iris  ;  when  this  forms  a  con- 
tinuous sheet  a  round  or  oval  pupil  results  ;  where  this  is  lacking  in 
certain  areas  an  operculum  is  formed  (Grynfeltt  and  Demelle,  1908). 
Of  the  first  type,  some  deep-sea  species  (the  luminous  shark,  Etmopterus; 
C'enirojjhorus  calceus)  have  large,  round,  almost  immobile  pupils  with 
poorly  developed  muscles — a  configuration  to  be  expected  in  their  dimly 
lit  habitat.  Species  which  come  to  the  surface  and  bask  have  contrac- 
tile pupils,  usually  circular  in  dilatation  and  elliptical  on  contraction 
(characteristically  in  the  vertical  direction  but  sometimes  oblique  or 


FISHES 


287 


horizontal)^  (Figs.  303  to  312).  Amongst  fishes  this  shape  of  pupil  is 
characteristic  only  of  Selachians.  An  expansible  opeeculum,  a 
structure  described  by  Cuvier  (1805)  and  subsequently  by  Leuckart 
(1875),  is  a  feature  of  the  flattened  Batoidei  with  their  upward-looking 
eyes  ^  ;  it  is  a  structure  on  the  upper  part  of  the  pupillary  margin 
which  expands  downwards  in  bright  light  to  block  the  aperture  so  that 
the  eyes  appear  to  "  close."  The  mechanism  whereby  this  non-muscular 
structure  contracts  and  exjDands  is  unknow^l.  These  opercula  are  of 
varying  shapes  :  thus  the  contracted  pupil  of  the  electric  ray,  Torpedo, 
or  the  spotted  dogfish,  ScyJliorhinus,  is  a  horizontal  slit  divided  in  the 
middle  by  a  tiny  operculum  (Fig.  313)  ;  the 
operculum  may  be  provided  with  a  smooth  edge, 
as  in  the  sting-ray,  Trygon,  and  Torpedo,  or  the 
margin  may  be  serrated  as  in  other  members  of 
the  ray  family  {Raja  clavata,  R.  bat  is,  Trygono- 
rkina  and  others),  so  that  on  full  expansion  it 
reduces  the  pupil  to  a  crescent  of  stenopoeic 
apertures  (Fig.  312). 

The  voluminous  leyis  is  never  completely 
spherical  as  in  Teleosteans,  but  is  always  lenti- 
cular in  shape  with  the  transverse  diameter 
slightly  greater  than  the  antero-posterior.  Un- 
like the  cyclostome  lens  and  as  occurs  in  all  other 
Vertebrates  except  lizards,  a  system  of  sutures 

is  present  ;  it  is,  however,  very  simple  consisting  merely  of  a  single  line- 
suture  rumiing  vertically  in  the  anterior  part  and  horizontally  in  the 
posterior  3  (Rabl,  1898)  (Fig.  314).  The  epithelium  clothing  the 
anterior  surface  is  continued  beliind  the  equator,  whereafter,  as  m 
other  ^>rtebrates,  the  cells  are  prolonged  into  fibres,  the  nuclei  of 
which  lie  in  the  posterior  cortex.  The  vitreous  is  of  a  dense  consistency 
particularly  in  its  anterior  parts  where  it  forms  the  susjDensory  apparatus 
of  the  lens  ;  it  has  little  adherence  to  the  retina  posteriorly  whence  it 
is  readily  detached. 

The  retina  has  received  a  considerable  amount  of  study. "^  In  the 
embryo,  blood  vessels  lie  in  the  foetal  fissure  (de  Waele,  1900)  but  these 
disappear  and  in  the  adult  the  retina  is  quite  avascular  and  shows  no 
trace  of  the  foetal  fissure  except  a  tiny  wliite  area  on  the  summit  of  the 
ciliary  papilla  (Fig.  301).     The  retinal  epithelium  is  comprised,  as  is 

1  The  basking  shark,  Selache  ;    the  spiny  dogfish,  Squalus  ;    the  porbeagle  shark, 
Latnna  ;   and  so  on. 

2  Thus  it  is  absent  in  the  devil-fisli  rays,  Mobuhda?,  wliich  have  lateral  eyes  and 
also  in  the  dorso-lateral  eyes  of  Myliobatis. 

3  A  single  line-suture  is  found  also  in  the  lenses  of  most  Teleosts,  Anurans,  Reptiles, 
some  Birds  and  the  rabbit. 

*  Krause,  1886-89;  Xeumayer.  1897;  Schaper,  1899;  Greeff,  1899;  Addario, 
1903  ;   Retzius,  1905  ;   Schnaudigel,  1905  ;   Franz,  1905  ;   Verrier,  1930  ;   and  others. 


Fig.      314. — Lenticular 
Sutures  of  Selachians. 

Showing     the     vertical 
anterior     suture.  Pos- 

teriorly   there    is    a    short 
horizontal  suture. 


Sci/lliorhinus 


Raj.t 


288 


THE   EYE   IN   EVOLUTION 


usual,  of  a  single  layer  of  hexagonal  cells,  but  when  a  tapetum  is 
i^resent  these  are  unjiigmented  until  the  ora  is  reached  in  order  to 
allow  the  passage  of  light  to  tliis  structure  (Fig.  315).  The  architecture 
of  the  retina  itself  is  simple  with  the  usual  layering,  but  a  considerable 
scattering  of  cells  outside  the  confines  of  their  layers  may  occur.  The 
horizontal  cells  are  unusually  massive  (like  those  of  the  lamprey)  and 
ganglion  cells  are  sparse.    Characteristically  the  retina,  is  pure -rod,  the 


Fig.  315. — The  Selachian  Retina. 

The  retina  of  the  ray,  Raja  maculata.  1,  pigment  of 
choroid  ;  2,  (non-pigniented)  retinal  epitheUum  ;  3,  laj'er 
of  rods  ;  4,  external  limiting  meinbrane  ;  5,  outer 
nuclear  layer  ;  6,  inner  nuclear  layer ;  7,  nerve  fibre  layer 
(Mallory's  trijjle  stain)  (Katharine  Tansley). 


Fig.  316.  —  The 
Cone  and  Rod 
OF  THE  Dogfish, 

JVffsri.;7.f.s'(xlOOO) 
(Gordon  Walls). 


Squatina 


cells  being  thin  and  long  ;  the  ratio  of  visual  to  ganglion  cells  varies 
(152  :  1  in  Efmoptenis,  14  :  1  in  Myliohatis,  12  :  1  in  Raja  miraletus — 
Verrier,  1930).  There  is  no  area  centralis,  although  in  some  species, 
jiarticularly  the  dogfish,  Mustelus,  the  density  of  the  visual  elements 
is  increased  in  a  round  central  area  so  as  to  suggest  an  elementary 
precursor  of  this  characteristic  of  the  higher  Vertebrates  (Franz,  1905) 
(Fig.  317).  Only  in  a  few  particularly  active  species  are  cones  found — 
the  dogfish,  Mustelus,  the  eagle-ray,  Myliohatis,  and  the  angel-shark, 
Squatina  (Franz,  1905  ;  Verrier,  1930  ;  Rochon-Duvigneaud,  1943) 
(Fig.  316). 

The  optic  nerve  has  various  septal  patterns  and  in  some  species 
an  cpendymal  core,  as  in  lampreys  (Prince,  1955)  ;  like  the  retina  it  is 
avas     lar.    The  optic  disc  is  small  and  flat  and  a  lamina  cribrosa  is 


FISHES 

lacking.  Unlike  those  of  the  lamprey,  the  optic  nerve  fibres  have 
become  myelinated  (Bruesch  and  Arey,  1942).  At  the  chiasma  there 
is  a  complete  crossing  of  the  nerve  fibres,  frequently  in  the  form  of 
interlacing  bundles  (Figs.  318  and  319)  (Verrier,  1930). 

THE  EXTEA-ocTJLAR  STRUCTURES.     The  jDresencc  of  mobile  eyelids, 
both  upper  and  lower,  sometimes  with  an  additional  fold  constituting 


289 


Fig.    317. — The    Area    Centralis    {ac)    of    the    Dogfish,    Mustelvs. 

Xote  the  increase  in  length  and  concentration  of  the  visual  cells  and 
the  great  number  of  ganglion  cells  (after  Franz). 

a  third  or  nictitating  membrane  in  many  selachian  species  is  a  curious 
anomaly  in  the  eyes  of  a  fish  (Fig.  299).  These  structures  are  supplied 
with  an  elaborate  musculature  blended  with  the  muscles  of  the  spiracle; 
a  superficial  layer  comprises  a  retractor  palpebrse  superioris  and  a  con- 
strictor spiraculi,  and  a  deep  layer  consists  of  a  levator  palpebrse 
nictitantis,  a  depressor  palpebrae  superioris  and  a  dilator  spiraculi,  the 

Figs.   318  and   319. — The  Chiasma  of  Selachians  (Verrier,   1930). 


Fig.   318. — The  dogfish,  Squalus. 


Fig.  319.— The  skate,  Raja. 


different  elements  being  more  or  less  blended.  The  palpebral  muscles 
are  supplied  by  the  seventh  nerve,  the  muscles  of  the  nictitating  mem- 
brane by  the  maxillo-mandibular  division  of  the  trigeminal  (Ridewood, 
1898  ;  Harman,  1899-1903).  The  lids  are  well  developed  in  the  deep- 
sea  sharks  of  the  requin  family  {Galeorhinus)  wherein  the  outside  of  the 
nictitating  membrane  is  clothed  with  the  same  type  of  minute  placoid 
scales  as  is  the  outer  surface  of  the  lower  lid.  Occasionally  there  is 
merely  an  immobile  circular  lid-fold  in  which  case  a  nictitating  membrane 
alone  is  present  (the  bonnet  shark,  Sphyrna  tihuro).  The  purpose  of  these 
elaborate  lids  is  difficult  to  imagine  ;  Franz  (1905)  concluded  that  they 
were  not  used  to  escape  from  the  dazzling  of  bright  light. 


290 


THE   EYE   IN   EVOLUTION 


The  orbit  is  cartilaginous  and  usually  very  incomplete  ;  in  it  the 
eye  lies  in  a  bed  of  gelatinous  connective  tissue  rich  in  blood  sinuses. 
The  extra-ocular  muscles  are  simple — four  recti  form  a  cone  inserted 
into  the  globe  about  its  equator  wliile  the  two  obliques,  arising  close 
together,  sweep  round  the  anterior  part  of  the  globe  in  front  of  the 
recti  and  are  inserted  in  common  with  the  vertical  recti.  These  muscles 
may  be  enormously  developed  in  the  larger  sharks  ;  in  the  basking- 
shark,  Selache,  for  example,  they  are  as  thick  as  the  biceps  of  the 
average  man.  The  most  characteristic  structure  in  the  orbit,  however, 
is  the  peculiar  optic  pedicle,  a  prop-like  cartilaginous  structure  which 
runs  from  the  cranium  to  the  posterior  pole  of  the  eye  which  it  receives 

in  an  expanded  cupped  head,  thus 
forming  a  simple  ball-and-socket 
joint  (Figs.  290  and  298).  The 
globe  in  its  cartilaginous  sclera 
thus  receives  a  firm  support. 
Sometimes  the  pedicle  is  firm  and 
stiff  ;  in  some  sharks  and  rays  it 
is  slender,  bending  when  the  extra- 
ocular  muscles  contract, 
straightening  and  proptosing  the 
eye  when  these  relax.  Sometimes 
it  is  incomplete,  either  not  reach- 
ing the  eye  or  the  cranium  (in  the 
elongated  orbit  of  the  hammerhead 
shark,  Sphyrna  zyqcena)  (Fig.  387), 

Fig.  320.— The  head    of    the    rabbit-fish,  •     i       ,  i        i      i  •  /xi, 

Chimcera      monstrosa      (Bland-Sutton's       O^    mdeed,     may   be    lacking    (the 
Lectures  and  Essays,  Heinemann).  spotted  dogfish,  ScylUorMnus) . 


THE    HOLOCEPHALIAN    EYE 

THE  HOLOCEPHALiANS  are  represented  today  only  by  the  Chimseras 
(rabbit-fishes  or  ghost-sharks),  somewhat  shark-like  fish  of  wide  distri- 
bution and  very  primitive  in  type  (Fig.  320)  ;  they  are  all  deep-sea 
bottom  fishes,  and  their  eyes,  which  are  of  the  same  type  as  the 
selachian  eye,  are  remarkable  for  their  adaptation  to  the  dim  illumina- 
tion of  the  ocean  depth.  For  this  reason  the  pupils  are  large,  round 
and  almost  immobile,  a  tapetum  is  lacking,  and  the  retina  has  an 
unusually  dense  population  of  rods  summated  by  an  unusually  small 
number  of  ganglion  cells  (100,000  rods  per  sq.  mm.  and  600  ganglion 
cells,  Franz,  1905) — a  ratio  not  exceeded  amongst  Selachians  except 
in  the  abyssal  forms  such  as  the  luminous  shark,  Etmopterus.  The 
shape  (f  the  eye  is  the  typical  ellipsoid  of  the  selachian  eye  but, 
curious •      the  sclera  is  thin,  sometimes  apparently  discontinuous. 


FISHES 


291 


Osteichthyes 


THE    TELEOSTEAN    EYE 


TELEOSTEAXS  are  a  huge  and  diversified  class  which  comprises  the 
great  majority  of  modern  fishes.  Ocularly — and  in  many  other  respects 
— they  show  the  highest  differentiation  among  fishes,  exhibiting  many 
anatomical  and  physiological  characteristics  which  are  peculiar  to 
themselves. 


Figs.  ,321   and   322. — Typical  Teleostean  Fishes. 


Fig.   321. — The  cai'p,  Cyprinus  (photograph  by  Michael  Soley). 


Fig.    322. — The  mouth-ljreeder  cielihd,  CicJiIa  (Zool.  Soo.,  London). 

Although  there  are  great  variations  among  the  many  sjDecies.  tlie 
teleostean  eye  has  certain  essential  characteristics  (Figs.  323-4)  : 

an  mcoiuplefe  civp  of  hijaUne  scleral  cartilage,  and  a  tendevcy  to 
multi-layering  of  the  cornea  ; 

a  very  elaborately  developed  annidar  ligament  bridging  the  angle  of 


292 


THE   EYE   IN  EVOLUTION 


Caraasius 


the  anterior  chamber  between  the  cornea  and  the  iris,  and  a  tensor 
choroidece  muscle  ; 

the  presence  of  a  choroidal  gland  in  most  species  ; 

a  failure  in  closure  of  the  foetal  fissure  allowing  the  protrusion  of  the 
choroid  through  the  retina  as  the  falciform  process  [or  alternatively  the 
emergence  of  a  hyaloid  system  of  vessels)  to  nourish  the  inner  layers  of 
the  retina,  which  with  one  known  exception  {the  eel)  is  avascular  ; 

an  ectoderynal  retractor  lentis  muscle  at  the  distal  end  of  the  falciform 
process  ; 

the  frequent  presence  of  a  choroidal  tapetum  (argentea)  usually  of  the 
lucidum  type,  but  sometimes  cellular,  neither  type,  however,  having  a 
visual  function  since  they  are  masked  by  the  pigment  epithelium  of  the 
retina  ; 

a  pupil  usually  immobile  and  often  so  large  as  to  leave  an  aphakic 
aperture  ; 

a  highly  organized  retina  typically  containing  both  rods  and  cones  as 
well  as  double  cones,  and  sometimes  a  fovea. 

THE    GENERAL   SHAPE    OF   THE    TELEOSTEAN    EYE    USUally   COnformS 

to  the  standard  type  characteristic  of  Fishes  ;  in  most  species  it  is  an 
anteriorly  flattened  elHpsoid  with  the  antero -posterior  diameter  shorter 
than  the  transverse,  although  in  slow-swimming  and  small-eyed  types 
the  shape  tends  to  be  more  nearly  spherical. 

An  exception  to  this  occurs  in  certain  deep-sea  Teleosts.  In  these  dark 
regions  the  poverty  of  the  illumination  requires  an  immensely  large  lens,  to 
accommodate  which  the  globe  may  acquire  a  tubular  shape. ^  Other  benthonic 
Teleosts,  giving  up  the  struggle  to  make  use  of  light  in  their  dark  environment, 
have  vestigial  eyes,  often  covered  with  opaque  skin  ^ — one  deep-sea  Teleost  (the 
only  known  Vertebrate  in  such  a  case)has  no  eyes  {Ipnops);  as  an  accessory,  certain 
benthonic  fishes  have  developed  luminous  organs,  sometimes  in  association  with 
their  eyes,  with  which  they  make  contact  with  their  kind.^ 

The  sclera  is  a  fibrous  tunic  sometimes  tenuous  and  thin  (as  in  the 
goldfish,  Carassius  auratus),  sometimes  immensely  thick  (tjie  star-gazer, 


1^   Astroscopus),  reinforced  by  hyaline  cartilage  which  sometimes  becomes 


partly  ossified  (Yatabe,  1932  ;  Rochon-Duvigneaud,  L943  ;  Woelfflin, 
1955)  :  only  in  a  few  forms  is  cartilage  lacking  (some  eels,  Gymnotidae  ; 
the  pearl-fish,  Encheliophis) .  Instead  of  forming  a  complete  cup  as  in 
Selachians,  however,  the  cartilage  is  lacking  in  the  posterior  part  ;  the 
general  arrangement  is  therefore  the  opposite  to  that  which  occurs  in 
Birds  in  which  the  posterior  segment  of  the  sclera  is  reinforced  by 
cartilage  (Fig.  327).*  Its  extent  varies  considerably  ;  sometimes  it  is 
confined  to  a  relatively  narrow  ring  around  the  limbus  (the  salmon- 
trout  family,  Salmonidae)  or  the  equator  ;    sometimes  it  clothes  the 


1  p.  332. 
■  p.  722. 


3  p.  736. 

^  p.  403,  Fig.  496. 


FISHES 

Figs.  323  and  324. — The  Teleostean  Eye. 


293 


Fig.   323. — Diagram  of  a  Teleostean  eye. 

AC,  autochthonous  layer  of  cornea  ;  AL,  annular  ligament  ;  CE,  corneal 
epithelium  ;  CG,  choroidal  gland  ;  CH,  campanula  of  Haller  ;  FP,  falciform 
process  ;  LB,  lentiform  body  ;  OX,  optic  nerve  ;  S,  scleral  cartilage  ;  Sc, 
sclera  ;    SC,  scleral  cornea  ;    SL,  suspensory'  ligament  ;    TC,  tensor  choroidese. 


\  ■(, 


Fig.  324.- 


-The  eye  of  the  trout.  In  the  section  the  dermal  layer  of  the  cornea 
has  come  loose,  as  usuallj^  occurs  (Norman  Ashton). 


294 


Mormyrid 


THE   EYE   IN  EVOLUTION 

entire  eye  apart  from  a  small  fibrous  zone  around  the  oiDtic  nerve  (the 
soles,  Soleidpe)  ;  sometimes  it  forms  discontinuons  islands  (the  elephant- 
fish  family,  Mormyridse)  ;  sometimes  it  becomes  partially  calcified, 
and  exceptionally,  as  in  Tetragonopterus,  this  transformation  is  com- 
plete. Scleral  ossicles  formed  of  true  bone  are  also  usually  found, 
typically  as  thin  plates  embedded  in  the  fibrous  tissue  of  the  sclera, 
situated  temporally  and  nasally  anterior  and  external  to  the  cartilage  ; 
occasionally  in  active  types  with  large  eyes  these  combine  to  form  a 
complete  osseous  ring  of  considerable  strength  (the  sword-fish,  Xiphias  ; 
tunny,  Thuimiis).^ 


Fig.  325 — The  Cornea  of  the  Carp. 
iShowing  the  thick  epitheHuni  (Smelser  and  Chen). 


Xiphias 


Minnow 


The  cornea,  usually  elliptical  with  the  long  axis  horizontal, 
(Grynfeltt,  191  ()  :  Verrier,  1927).  is  frequently  irregular  and  grooved 
and  has  a  variable  constitution.  In  some  forms  it  shows  the  usual 
vertebrate  configuration,  the  substantia  propria  being  relatively 
homogeneous  (Salmonidce — salmon,  trout  ;  Cyprinidse — minnows  and 
carps  ;  Esocidae — pike)  (Fig.  325)  ;  but  in  others  it  is  uniquely  complex, 
4  layers  being  readily  distinguishable  : 

(1)  A  dermal  layer,  derived  from  and  continuous  with  the  skin, 
consisting  of  a  multi-layered,  usually  thick  ejiithelium.  Bowman's 
membrane  and  the  superficial  portion  of  the  substantia  propria. 

^  It  is  to  be  remembered  that  the  scleral  ossicles  of  Sauropsida  are  homologous 
not  with  the  scleral  ossicles  of  fishes,  but  with  the  circumorbital  bones.  The  ossicles 
of  tli(>  sturgeon  are  derived  not  from  the  sclera  but  from  the  skin  (H.  Miiller,  1872), 
p.  317. 


FISHES  295 

(2)  An  intermediate  layer  between  the  dermal  and  scleral  portions 
corresponding  topographically  to  the  episcleral  tissue.  It  consists  of 
very  loose  lamellar  tissue,  so  loose  that  it  readily  allows  the  superficial 
layer  to  be  peeled  from  the  deeper  and  occasionally  permits  some 
degree  of  movement  of  the  globe  under  the  dermal  cornea  (the  eel, 
AnguiUa)  (Hein,  1913).  It  is  interesting  that  on  luxation  of  the  eye 
the  scleral  cornea  readily  splits  from  the  dermal  so  that  the  latter  may 
remain  in  place  and  be  left  behind  (Rochon-Duvigneaud.  1916)  (cf. 
Fig.  324). 

(3)  A  scleral  layer  consisting  of  dense  lamella'  of  substantia 
propria  structurally  continuous  with  the  sclera  itself. 

(4)  Descemet's  membrane  and  its  endothelium  of  extreme 
delicacy.  In  some  species,  indeed,  the  endothelium  and  Descemet's 
membrane  appear  to  be  absent  in  the  central  area  of  the  cornea  (carp, 
Cyprinus — Smelser  and  Chen,  1954)  (Fig.  325). 

So  far  this  arrangement  somewhat  resembles  that  seen  in  lamprej's,^  and 
appears  to  be  more  primitive  than  the  typically  vertebrate  selachian  cornea. 
In  some  species,  however,  there  is  an  apparently  separate  layer  of  coarse  fibres 
on  the  inner  aspect  of  the  finely  lamellar  scleral  layer — the  autochthonous 
LAYEK  of  Leuckart  (1876).  It  thickens  greatly  towards  the  periphery  and  termin- 
ates abruptly  at  the  scleral  margin,  but  is  probably  merely  a  modified  portion 
of  the  scleral  cornea. 

An  interesting  phenomenon  is  the  occurrence  of  yellow  pigmentation  in  the 
corneae  of  many  Fishes  due  to  the  presence  of  xanthophores  in  the  ei^ithelium. 
In  the  bull-head.  Coitus,  for  example,  there  is  a  pigmented  process  running  over 
the  cornea  like  a  yellow  waterfall  (Walls  and  Judd,  1933),  while  the  entire 
cornea  of  the  carp,  Cyprinus,  and  the  jDike,  Esox  (Schiefferdecker,  1887)  is  yellow. 
It  is  interesting  that  Soemmerring  (1818)  in  describing  this  appearance  originally, 
attributed  it  to  a  yellow  aqueous  humour.  The  pigment  must  act  as  a  light - 
filter  as  does  yellow  pigmentation  in  the  lens.- 

A  regular  feature  of  the  teleost  cornea  is  an  accumulation  of  cells, 
apparently  continuous  with  the  endothelium,  which  fills  the  angle  of 
the  anterior  chamber  and  is  reflected  over  the  surface  of  the  iris  to 
form  a  massive  axnular  ligament  (Angelucci,  1881  ;  Lauber,  1901), 
the  "  vesiculo -hyaline  tissue  of  the  angle  "  of  Rochon-Duvigneaud 
(1943)  (Fig.  326)  ;  from  it  the  tensor  choroidete  muscle  is  probably 
derived.  The  annular  ligament,  somewhat  reminiscent  of  the  endothelial 
proliferation  seen  in  Cyclostomes  and  Chondrosteans,  is  elaborately 
developed  in  Teleosteans.  It  is  composed  of  large  polyhedral  epithelioid 
cells  (Giacomelli.  1935)  ;  it  may  be  vascularized  (the  mud-skipper, 
Periojihthalmus^)  or  contain  melanophores  (the  cod,  Gadus)  and  is 
sometimes  rich  in  lymphatic  sinuses  which,  however,  cannot  be 
considered  homologous   with  the   canal   of  Schlemm    (Franz,    1910  ; 

1  p.  265. 

^  Compare  the  yellow  pigmentation  in  the  cornea  of  the  bow-fin,  Ajyiia,  in  the 
lenses  of  the  lamprev  and  of  diurnal  snakes  and  squirrels,  or  yellow  oil-globules  in  some 
retinal  cones  (p.  656).  »  p.  326,  Fig.  386. 


296 


THE   EYE   IN   EVOLUTION 


Karsten,  1923).  Not  only  does  this  layer  cover  most  of  the  anterior 
surface  of  the  iris,  but  in  a  few  Teleosteans  it  appears  to  form  a  thick 
stratum,  in  part  fibrillar,  in  part  cellular,  on  the  inner  aspect  of  the 
scleral   cornea — the   supplementary  layer   of  Rochon-Duvigneaud 


Fig.   326. — The  Angle  of  the  Anterior  Chamber  of  the  Trout. 

Showing  the  immense  thickening  in  the  periphery  of  the  cornea  and  the 
annular  ligament  filling  up  the  angle  of  the  anterior  chamber  and  binding  the 
iris  to  the  cornea.  The  dermal  layer  of  the  cornea  (as  often  occurs)  has  been 
lost    (  X  84)  (Norman  Ashton). 


11 


(1943)  (goby-fishes,  Gobius  niger,  Periojjhthalmus  ;   the  soles,  Soleidse, 
etc.).     Various  views  have  been  put  forward  as  to  the  nature  of  this 
structure  which  may  add  another  layer  to  the  already  complex  cornea 
Qobius  and  appears  topographically  to  be  continuous  with  the  choroid  ;    a 

secretory  function  has  been  suggested,  but 
r  its    exact   significance    must   await   further 

study  (see  Ballowitz,  1913  ;  Kolmer,  1913  ; 
Remotti,  1929  ;  Schaffer,  1929  ;  Baecker, 
1931). 

The  uveal  tract  shows  several  distinctive 
characteristics  (Fig.  327).  The  choroid  has 
the  essential  vertebrate  structure  of  a  chorio- 
capillaris  and  a  heavily  pigmented  vascular 
layer,  but  is  noteworthy  for  three  features — 
the  argentea,  the  choroidal  gland  and  the 
falciform  process.  In  the  majority  of  pelagic 
forms  there  is  a  layer  of  guanine-laden  cells 
interspersed  with  chromatophores  —  the 
argentea — jacketing  the  outside  of  the 
choroid  with  a  silvery  coat  which  is  continued 
forwards  over  the  anterior  surface  of  the  iris 
giving  it  its  metallic  appearance.  In  view  of 
the  fact  that  it  is  obscured  from  the  retina  by 
pigment,  this  layer  can  have  no  visual  value  ; 


Fig.  327. — Section  through 
THE  Equatorial  Segment 
OF  THE  Eye  of  the 
Trout. 

Showing  the  thick  choroid, 
ch,  the  retina,  r,  and  the 
scleral  cartilage,  s  (Feulgen  ; 
X  6;     'Katharine  Tansley). 


FISHES 


297 


Figs.  3:28  and  329. — Thk  Chokoidal  Gland  of  the  Trout,  Salmo  trutta 
(Xorman  Ashton). 


Fig.  328. — The  "  gland  "  occupies  the  upper  part  of  the  figure  (  X  SO). 


Fig.   329.— Structure  of  the  -'gland"  (  X  320). 

it  is  possible  that  it  serves  a  protective  disguise  in  tloe  transparent  larva 
the  black  eyeball  of  which  would  otherwise  be  dangerously  conspicuous, 
blending  with  the  reflexes  of  the  water  m  the  same  way  as  do  the  silver 
reflections  from  the  sides  of  the  adult  fish.  In  a  few^  species  there  is, 
in  addition,  a  tapetum  fibrosum  on  the  inner  aspect  of  the  choroid 
separating  the  main  vascular  layer  from  the  choriocapillaris,  such  as  is 
typical  of  hoofed  Mammals  (Millot,  1923)  ^  :  it  is  composed  of  a  layer 
of  dense  fibrous  tissue  of  a  glistening  tendon-like  structure  wherein  the 

'  p.  457. 


298  THE   EYE   IN   EVOLUTION 

Figs.  330  and  331. — The  Falcifobm  Process,  in  an  Adult  Teleostean 

(Trout). 


""^ 

W ' 

^^      •    / 

^\yV    ^ 

\-^^          r^^y 

^""""•'Sii^^-L^^K^^^ 

u 

^<^^::ip>^ 

Fig.  330. — The  macroscoiDic  intra-ocular  ajDpearance  of  the  posterior  half  of 
the  globe  seen  from  the  front.  F,  falciform  process. 


Fig.  331. — Section  across  the  region  of  the  fcetal  fissure.  H,  vascular  mesoderm 
of  the  falciform  process  ;  E.  neuro-ectoderm  of  the  wall  of  the  oj^tic  cup 
(Mann,  after  von  Szily). 


other  choroidal  constituents  (pigment  cells  and  vessels)  have  been  cut 
down  to  a  minimum  (Walls,  1942). 

The  CHOROIDAL  C4LAND,  an  organ  so  called  by  Cuvier  (1805)  but 
with  no  structural  or  functional  affinities  to  a  gland,  is  a  peculiar 
vascular  formation  lying  in  the  posterior  part  of  the  globe  between 
the  choioid  and  the  sclera  (Figs.  328-9).  It  is  highly  vascularized, 
consistiim  essentially  of  a  mass  of  juxta-apposed  capillaries  sometimes 
forming  a  ring  around  the  optic  nerve,  more  frequently  horse-shoe-shaped 
in  whicii      se  the  open  end  of  the  horse-shoe,  ventral  to  the  nerve,  may 


FISHES 


299 


be  partially  filled  by  a  similar  accessory  body,  the  lentiform  body. 
It  occurs  in  the  majority  of  Teleosteans  (Erdl,  1839) — according  to 
J.  Miiller  (1840),  in  all  those  provided  with  the  hyoid  gill  (or  pseudo- 
branch)  from  which  it  is  directly  supj^lied  with  highly  oxygenated 
arterial  blood  ;  from  the  "gland"  the  blood  flows  into  the  choroidal 
circulation.  Both  the  pseudobranch  and  the  choroidal  gland  are 
absent  in  some  genera  with  small  eyes,  such  as  the  eels  [AngnUla)  and 
the  cat -fishes  (Siluroids). 

It  has  been  suggested  that  the  choroidal  gland  forms  a  special  mechanism 
whereby  the  circulation  is  maintained  despite  considerable  changes  in  pressure 
when  rapid  alterations  occur  in  the  dejith  of  swimming  (Allen,  1949)  ;  this, 
however,  seems  unlikely  in  view  of  its  constant  presence  whatever  the  habitat 
of  the  fish.  Nor  does  it  appear  to  act  as  an  erectile  organ  assisting  accommodation 
by  pushing  the  retina  forwards  (Barnett,  1951  ;  Yamasaki,  1954)  ;  it  is  probably 
pvirely  nutritive  in  function. 


Anguilla 


Cat-fish 


The  vascularisation  of  the  inner  eye  is  further  maintained  by  the 
falciform  process,  or  when  it  is  absent,  by  a  hyaloid  system  of  vessels. 
The  FALCIFORM  PROCESS  is  a  peculiarity  of  Teleosteans  and  consists  of 
a  prominent  sickle-shaped  ridge  of  pigmented  and  richly  vascularized 
choroidal  tissue  which  j^rotrudes  through  the  inferior  part  of  the  retina 
in  the  region  of  the  foetal  fissure  (which  has  never  closed),  running  from 
the  optic  disc  to  the  ciliary  region  (Figs.  330-1)  (Franz,  1910).  This 
structure  is  somewhat  analogous  to  the  cone  of  Reptiles  and  the  pecten 
of  Birds  although  these  structures  are  ectodermal  in  origin  and  are 
secondarily  vascularized.  In  some  species  the  fissure  has  closed 
posteriorly  so  that  only  the  anterior  portion  of  the  falciform  process 
remains  (the  cod.  Gadns  :  herring.  Clujiea  :  carp.  Cyprinus  :  etc.).  In 
those  species  in  which  the  process  is  small  or  absent,  as  in  certain  eels 
(conger.  H.  Virchow,  1882),  cyprinoids  such  as  the  carp  and  roach 
(O.Schultze.  1892),  and  goby  fishes  (Karsten.  1923),  the  nutriment  of  the 
inner  eye  is  taken  over  by  a  hyaloid  system  of  vessels  which,  like  the 
falciform  process,  issues  through  the  foetal  fissure  :  the  main  artery 
enters  the  eye  in  the  region  of  the  oj^tic  disc  and  instead  of  running 
through  the  choroid  to  constitute  the  basis  of  the  falciform  process, 
breaks  into  the  superficial  layers  of  the  vitreous  and  forms  a  dense 
vascular  plexus  running  anteriorly  lying  loosely  upon  the  inner  surface 
of  the  retina  (Chrustschoff,  1926)  (Figs.  332-3).  This  membrana 
VASCULOSA  retix.e  Constitutes  an  arrangement  of  widespread  dis- 
tribution among  Vertebrates  and  is  comparable  to  that  seen  in  certain 
Amphibians  and  Reptiles  (snakesj.  It  is  to  be  noted  that  these  vessels 
ramify  in  the  vitreous,  lying  superficially  on  the  retina  without 
entering  it.  The  veins  drain  anteriorly  into  an  annular  vein  which 
leaves  the  eye  through  the  ciliary  zone,  and  between  tlie  two  a  widely- 


Gadus 


Clupea  harenytxs 


300 


THE   EYE   IN   EVOLUTION 


meshed  net  is  spread  in  which  the  capillaries  are  associated  with  the 
AT^eins  leaving  a  zone  free  of  small  vessels  around  the  arteries. 

An  exception  of  more  than  usual  interest  is  seen  in  the  ee\,Anguilla. 
This  fish  is  unique  in  having  no  demonstrable  choroid,  for  the  large 
cells  of  the  retinal  pigment  epithelium  lie  directly  on  the  sclera,  and 
as  if  in  compensation  the  vessels  of  the  membrana  vasculosa  vascularize 
the  retina  directly  (Fig.  334)  (W.  Krause,  1876  ;  Virchow,  1882  ; 
Denissenko,  1882  ;    Michaelson,  1954).     The  vessels  of  this  membrane 


Figs.  332  and  333. — The  Membrana  Vasculosa  Retinae  of  Teleosteans. 


Fig.  332. — In  the  goby  fish,  Gobius 
poecilichthys.  The  vessels  emanate 
from  the  central  artery  of  the  retina 
and  run  over  this  tissue  within  the 
vitreous.  The  division  of  the  prin- 
cipal vessel  into  the  annular  vein  is 
seen  on  the  nasal  side,  at  V  (after 
Karsten). 


Fig.  333. — Sketch  of  injected  retina  of  the 
roach,  Eutihis,  .showing  the  concentra- 
tion of  capillaries  around  the  vein  (to  the 
left)  while  the  peri-arterial  zone  (to  the 
right)  is  relatively  free  from  capillaries 
(  X  23)  (I.  C.  Michaelson). 


derive  from  a  large  central  artery  entering  the  eye,  as  is  usual,  through 
the  optic  disc  and  its  branches  form  an  arterial  network  in  the  vitreous 
lying  on  the  surface  of  the  retina  and  extending  to  the  periphery  of 
the  fundus  where  they  form  capillary  loops.  From  this  arterial  network 
numerous  branches  pass  from  the  vitreous  through  the  internal 
limiting  membrane  into  the  retina  :  Virchow  (1882)  estimated  that 
there  were  9,600  of  them.  In  the  substance  of  the  retina  they  divide 
into  two  strata  of  capillaries,  one  in  the  inner  and  one  in  the  outer 
nuclear  layer,  and  from  these  retinal  capillary  nets  blood  is  drained 
by  large  veins  which  combine  to  form  four  main  vessels  and  eventually 
join  to  fdrni  a  central  vein  in  the  optic  nerve  head  (Figs.  334  and  335). 
The  abs;  iice  of  a  choroid  in  this  fish  is  unique  and  the  direct  vasculariza- 
tion oft       inner  retinal  layers  constitutes  the  only  known  exception 


FISHES 


301 


Fig.  334. — Section  of  the  Eye  of  the  Eel. 

The  superficial  vitreous  and  both  retinal  capillary  nets  can  be  seen 
filled  with  indian  ink  (»■).  The  cells  of  the  retinal  epithelium  form  a  broad 
layer.  There  is  no  choroid  present,  the  epithelial  layer  lying  directly  on  the 
cartilaginous  sclera  (s)  (  X  169)  (I.  C.  Michaelson). 


Fig.  33o. — The  Retina  of  the  Eel. 

Injected  with  indian  ink,  mounted  in  glycerme.     The  superficial  vitreous 
vessels  are  in  focus  :    these  are  arterial  (  y.  37)  (I.  C.  IMichaelson). 


to  the  general  avascularity  of  the  teleostean  retina  ;  indeed,  it  is  the 
only  known  case  in  which  the  vertebrate  retina  is  directly  vascularized 
except  in  the  colnbrid  snake  Tarbophis  and  in  Mammals. 

The  ciliary  zone  is  narrow  and,  without  folds  or  processes,  may  be 
said  not  to  exist  so  that  the  choroid  apjoears  to  i3ass  directly  into  the 
iris  (Fig.  336)1;  only  in  a  few  amphibious  types  such  as  Anahhps  do  a 
few  processes  exist.  This  region,  however,  provides  the  supporting 
and  accommodative  apparatus  of  the  lens.     Dorso-nasally  the  latter 

^  See  footnote  p.  267. 


302 


THE   EYE   IN   EVOLUTION 


is  suspended  pendulum-like  by  a  firm  suspensory  ligament,  a  con- 
densation of  the  anterior  vitreous  with  a  fibrillar  appearance  on 
microscoj)ic  examination  (Harms,  1928  ;  Teulieres  and  Beauvieux, 
1931  ;  Koch,  1952).  Ventrally,  at  the  ciliary  end  of  the  falciform 
process,  a  small  structure  of  great  variability  in  size  and  shape  makes 
contact  with  the  lens  by  ligamentous  condensations  of  the  vitreous — 
the  CAMPANULA  of  Hallcr  (1762).  It  contains  a  triangular  muscle  of 
smooth  fibres  of  ectodermal  origin  being  derived  from  the  retinal 
epithelium  of  the  ciliary  zone  at  the  open  lips  of  the  fcetal  fissure,  thus 
resembling  in  this  respect  the  muscles  of  the  iris  (Nussbaum,  1901  ; 
V.  Szily,   1922),  and  is  innervated  by  a  short  ciliary  nerve  from  the 


Fig.    336. — The    Anterior    Segment    of    the    Eye    of    the    Bull-head, 

CoTTVS  BCBALIS. 

i,  iris  ;  si,  suspensory  ligament  ;  s,  serous  spaces  behind  the  annular  liga- 
ment ;  ca,  scleral  cartilage  ;  co,  conjunctiva  ;  c,  cornea  ;  p,  posterior  layer 
of  the  cornea  ;  CH,  campanula  of  Haller  (after  a  drawing  by  Rochon- 
Duvigneaud). 


Scorpcena 


ciliary  ganglion  (TretjakofF,  1926  ;  Meader,  1936).  It  has  been 
generally  accepted  as  being  the  effector  muscle  in  the  accommodative 
mechanism,  acting  by  retracting  the  lens  towards  the  retina,  a  claim, 
however,  contested  by  Bourguignon  and  Verrier  (1930)  who  failed  to 
find  muscular  tissue  in  this  somewhat  peculiar  structure.  Whatever 
its  true  nature,  it  is  a  characteristic  of  Teleosteans,  being  absent  only 
in  a  few  species  such  as  the  eel. 

An  additional  muscle  is  found  in  this  region  in  practically  all 
species — the  tensor  CHOROiDEiE.  It  was  initially  described  as  being 
composed  of  fibrous  tissue  and  named  the  "  ciliary  ligament  "  (Leydig, 
1853  ;  Leuckart,  1876),  but  has  been  shown  to  contain  smooth 
muscle  fibres  (Grynfeltt,  1910  ;  Rochon-Duvigneaud,  1943).  It  is 
a  tenuous  muscle,  about  1-5  mm.  in  length,  lying  between  the  sclera 
and  the  uvea,  arising  from  the  annular  ligament  anteriorly,  thus 
clioring  itself  to  the  cornea,  and  inserting  itself  into  the  anterior 
i^  ri  of  the  choroid  just  behmd  the  ora  (Faravelh,  1890-91  ;  Grynfeltt, 
It;'')  ;     in   the   scorpion-fish,   ScoriKena,   there   is   an   additional   shp 


PLATE  II 

Thk  TiuDES  OF  Teleosts  (Ida  Mann) 


I 


Fig.    1. — The  kilJifish,  AiAodieiliditliys 
ruiirostKjmfi. 


Fig.  2. — The  salmon.  S<ilmo  sakir. 


Fig.  3.— The  tele.sc.. 


l;iiI(IHs1i,  C'linis-siiis. 


Fig.    4. — The    red-e_\'e(_l  fish,    Ik'lragonojtfcni.f 
rubropictiis. 

C,  ciliary  arteries. 


Fig.  .5.    -The  common  goldfish.  Carassias 
fixrutus. 

('.  ciliary  arteries. 


S.O  — VOL.  I 


[  To  face  p.  302. 


FISHES 


303 


running  between  the  cornea  and  the  sclera,  while  in  Beryx  the  entire 
muscle  seems  to  pass  from  the  cornea  to  the  sclera  without  a  choroidal 
attachment  (Rochon-Duvigneaud,  1943). 

The  tensor  choroidese  is  generally  accej^ted  as  the  precursor  of  the  ciliary 
muscle  (of  Briicke)  of  Sauropsida  and  Mammals,  but  in  Fishes  its  function  is 
not  clear  ;  it  has  been  said  to  brace  the  retina  and  choroid  when  the  lens  presses 
backwards  ujjon  the  vitreous  during  accommodation  (Beer,  1894),  while  the  main 
role  in  teleostean  accommodation  was  ascribed  to  it  by  Bourguignon  and 
Verrier  (1930). i 

The  iris  is  complex  in  structure  and  frequently  brilliantly  coloured. 
The  continuation  of  the  choroidal  argentea  over  its  anterior  surface 
gives  it  a  metallic  sheen  and  in  addition  bright  pigments  abound — 
gold,  scarlet,  yellow,  mauve  and  others,  sometimes  so  dense  that  the 
structure  of  the  tissue  or  the  arrangement  of  its  vessels  is  completely 
obscured  (Plate  II).  In  some  species  Beer  (1894)  foimd  that  a  slow 
change  in  colour  could  be  induced  by  electrical  stimulation,  presumably 
owing  to  contraction  of  the  clu-omatophores  ;  a  similar  change  has 
been  induced  in  the  carp,  Cyj^ririus,  by  the  injection  of  adrenalin  or 
ablation  of  the  hypoiDh3%sis  (Rochon-Duvigneaud.  1943).  The  two 
ectodermal  layers  conform  to  the  usual  pattern,  the  posterior  being 
non-pigmented  almost  half-way  towards  the  pujDil,  the  anterior  heavily 
pigmented  tlu'oughout  its  extent.  From  the  latter  are  developed  the 
myoepithelial  fibres  of  the  sphincter  muscle  ;  in  most  species  a  few 
radial  cells  represent  the  elements  of  a  dilatator  muscle  although  in 
some  these  may  be  marked  (the  sword-fish,  Xijihias — Barraquer- 
Cerero,  1952).  Anterior  to  the  ectodermal  layer  the  heavily  pigmented 
vascular  layer  forms  the  forward  continuation  of  the  choroid,  covered 
superficially  by  the  thick  argentea  ;  while  over  a  varying  j^ortion  of 
the  peripheral  area  of  the  anterior  siuface  of  the  iris  the  cellular 
annular  ligament  spreads  itself,  filling  up  the  angle  of  the  anterior 
chamber  in  contininty  with  its  corneal  extension.  The  iris  is  usuallj^ 
supplied  by  two  anterior  ciliary  arteries  which  enter  in  the  horizontal 
meridian  on  either  side  and  run  on  the  superficial  surface  straight 
towards  the  pupil  ;  here  they  divide  to  form  a  circular  arterial  anasto- 
mosis around  the  pupillary  margin  (Plate  II,  Fig.  5).  The  venous 
drainage  is  by  deeper  vessels  running  beneath  the  argentea,  and  there- 
fore hidden  from  view  ;  they  are  continuous  with  the  choroidal  veins 
(J.  Miiller,  1840  ;    Virchow,  1882  ;   Mann,  1929-31). 

The  pujril  is  round  or  horizontally  oval  or  pear-shaped,  but  in 
general,  even  in  the  rare  tyjjes  wherein  the  sphincter  forms  a  massive 
band,  the  pupils  of  Teleosts  are  essentially  immobile,  the  iris  being 
widely  fixed  to  the  posterior  surface  of  the  cornea  by  the  aimular 
ligament.    As  wath  selachian  irides.  the  pupils  contract  sluggishly  and 

1  p.  646. 


Beryx 


Xiphias 


304 


THE   EYE   IN   EVOLUTION 


autonomously  by  the  direct  action  of  light  (Brown-Sequard,  1847-59  ; 
Magnus,  1899)  (Figs.  337-9). 

Only  in  a  few  species,  such  as  the  flounders  with  upward-looking  eyes,  and 
the  eels,  does  much  pupillary  excursion  occur  ;  in  the  pearl -fish,  Encheliophis, 
also  with  upward-looking  eyes,  the  pupil  is  highly  contractile.  Some  cat-fishes 
have   an   opercvilum   which   reduces   the   pupillary   aperture   to   a   circular   slit 

Figs.  337  to  341. — The  Pupils  of  Teleosteans. 

® 

Fig.  338.— The 

sailfish, 

IstiopJwrus. 


Fig.  337.— The 

Moray  eel, 
Gymnothorax. 


Fig.  339.— The 

flounder, 

Pleuronectes. 


Fig.   340.— The 

serpent  eel, 

Leptognofhus. 


@ 

Fig.  341. — The    cat-fish,    Plecostomus,    showing    the    operculum    in    various 
stages  of  closure  of  the  pupil. 

{Plecostomus,  Fig.  341),  while  the  serpent-eel  of  New  Zealand  (Leptognathus) 
has  a  secondary  pupillary  aperture  in  its  lower  part  giving  it  a  double  effect 
(Fig.  340).^  An  interesting  feature  is  the  common  presence  of  an  aphakic  area 
in  the  pupillary  aperture  which  the  lens  rarely  entirely  fills  (Plate  II).  This 
is  sometimes  situated  below  but  is  visually  on  the  temporal  or  nasal  side  and 
becomes  particularly  niarked  when  the  lens  is  drawn  sideways  in  accommoda- 
tion (Beer,  1894). 

The  lens  of  Teleosteans  is  usually  spherical,  approximating  the 
cornea,  with  a  large  spherical  nucleus  and  a  well-marked  system  of 
sutures  usually  taking  the  form  of  a  single  Ime 
as  in  Selachians  but  sometimes  star-shaped 
(Figs.  314,  342)  (Rabl,  1898  ;  Koch,  1950-52)  ; 
Yamasaki,  1953).  The  peripheral  shell  has  a 
refractive  index  approximating  that  of  water  ; 
the  central  core,  on  the  other  hand,  has  the 
high  refractive  index  of  1-5  and  is  the  effective 
refractive  constituent  of  the  optical  system 
(Hogben  and  Landgrebe,  1940).  The  vitreous 
is  dense  and  filamentous  (Koch,  1952-53). 

The  teleostean  retina  is  an  advanced  and 
fully  differentiated  structure  with,  as  we  have 
already  seen,  an  open  foetal  fissure,  nourished 

1  p.  325. 


Fig.    342.  —  Lenticular 

SUTURES     OF    TeLEOSTS. 

The  usual  system  is 
that  of  Selachians  (Fig. 
314)  ;  ;\  star-shaped  sys- 
tem is  ■  !so  relatively 
common. 


FISHES 


305 


(with  the  exception  of  the  eel)  either  by  the  falciform  process  or  a 

hyaloid  system  of  vessels.     The  pigmentary  eijithelium  has  a  normal 

configuration  (Fig.  343),  but  in  some  species  (Cyprinidse,  Percidae)  has  an 

occlusible  retinal  tapetum  lucidum  of  varying  extent,  sometimes 

small,  sometimes  occupying  a  large  oval  area  or  almost  the  entire 

fundus.     In  the  region  thus  occupied  the  epithelial  cells  have  long 

processes  heavily  packed  with  crystals  of  guanine  or 

a  guanine-like  compound   containing   calcium  ;    in 

dim  light  the  fuscin  pigment   migrates   backwards 

into    the   cell-bodies  exposing    a   silvery    mirror   of 

guanine  ;   in  bright  light  the  dark  pigment  migrates 

through  the  guanine  layer  to  the  tips  of  the  processes, 

covering  up  the  tapetum  and  absorbing  the  excess  of 

incident   light    (SchiefFerdecker,    1887  ;     AbelsdorfF, 

1896;  Garten,  1907;  Wunder,  1925-30).  Occasionally 

in  abyssal  fishes  which  are  never  exposed  to  bright 

light  {Evermanella),   the  pigment  does  not  migrate 

and  is  confined  to  small  masses  at  the  ends  of  the  cell 

processes,   an   arrangement  also   seen    in   Chondro- 

steans. 

The  visual  retina  has  received  much  study  (Figs. 
344-(5).^  This  structure  in  Teleosteans  is  remarkable 
among  Fishes  for  the  regularity  of  its  layers  and  the 
absence  of  displaced  elements,  the  thickness  of  the 
nuclear  layers  and  the  number  of  ganglion  cells  ;  it 
is  the  most  highly  differentiated  retina  among  the 
Fishes  and  compares  in  this  respect  only  with  the 
highest  Vertebrates.  Typically  both  rods  and  cones 
are  found  :  only  rarely  as  in  deep-sea  species  {Batliy- 
troctes)  and  exceptionally  in  fresh- water  types 
(Hiodon)  are  the  cones  absent  (Moore,  1944).  In 
deep-sea  forms,  in  order  to  increase  the  sensitivity  to 
light,  the  rod  population  is  usually  dense  and  may 
indeed  be  the  liighest  among  all  Vertebrates  (5,000,000  sq.  mm.  in 
Lampayiyctus — Vilter,  1951)  (Wunder,  1925-30)  while  the  individual 
elements  may  be  elongated  ;  in  a  bathypelagic  species,  Bathylagus 
benedicti,  they  are  arranged  in  three  distinct  rows  (Vilter,  1953). 


C^C 


Fifj.  343.  —  The 
Pigment  Epi- 
thelium OF  THE 
Goldfish, 
C  A  /!  A  s  s  /  u  s 
A  U  It  A  T  u  .y. 

Ill  the  light- 
adapted  state. 
The  processes  con- 
tain migratory  pig- 
ment in  rod -like 
granules  concentra- 
ted mainly  in  their 
tips,  r  and  c  repre- 
sent spaces  occu- 
pied by  rods  and 
cones  (after  Walls). 


Presumably  as  an  adaptation  to  increase  the  visual  acuity  in  the  direction 
in  which  food  is  usually  obtained,  different  areas  of  the  retina  frequently  vary 
in  the  relative  density  of  the  population  of  rods  and  cones  ;  thvis  in  the  ininnow, 
Ericymba,  which  frecjuents  the  bottom,  the  ventral  area  of  the  retina  contains 

1  H.  Muller  (1857),  M.  Schultze  (1866),  Dobrowolskv  (1871),  W.  Muller  (187.5), 
Hannover  (1876),  Denissenko  (1881),  W.  Krau.se  (1886),  Cajal  (1893-1933),  Greeff  (1899), 
Hesse  (1904),  Wunder  (1925-30),  Arev  (1928),  Verrier  (1928-38),  Mayou  (1933), 
Rochon-Duvigneaud  (1943),  Vilter  (1947-54),  Sverdliek  (1954),  H.  Muller  (1954). 

S.O. — VOL.  I.  20 


306 


THE   EYE    IN   EVOLUTION 


Figs.  344  and  345. — The  Ophthalmoscopic  Appearance  of  the  Fundus 
or  Teleostean  Fishes. 


Fig.  344. — The  cod,  Gadus,  showing  the 
vessels  of  the  falciform  j^i'ocess  running 
over  the  elongated  optic  disc  and 
breaking  up  into  6  branches  of  the 
hyaloid  artery  (after  Beauregard). 


Fig.  345.— The  scorjjion  fish,  Scorpcena, 
showing  the  optic  nerve  entrance  in 
relation  to  the  falciform  process  and  the 
peculiar  mosaic  arrangement  of  the  back- 
ground of  the  fundus  (after  Franz). 


These  illustrations  may  seem  to  require  an  apology  but  the  fundus  of  a 
fish  is  very  difficult  to  see  ophthalmoscopically.  It  can  be  examined  out  of 
water  if  the  fish  be  kept  alive  by  a  current  of  water  supplied  to  the  mouth  and 
gills  ;  some  species  such  as  the  carp  can  survive  being  kept  out  of  water  for 
some  time.  The  difficulties  do  not  end  here.  Out  of  water  the  cornea  is 
irregular  ;  and  in  addition  to  the  great  liypermetropia  in  air  of  an  eye  optically 
designed  for  vision  under  water,  the  splierical  shape  of  the  crystalline  lens 
makes  the  dioptrics  such  that  only  a  minute  portion  of  the  fundus  can  be  seen 
at  one  time  and  no  overall  view  can  be  obtained. 


'tf"^^' 


.  1 

^  2 
3 

■5  n 


^m  7 

8 
9 


Fig.  346. — The  Retina  of  the  Trout,  Salmo  trutta. 
1,  optic  nerve  fibre  layer  ;  2,  ganglion  cell  layer  ;  3,  inner  plexiform 
layer  ;  4,  inner  nuclear  layer  with  a  prominent  layer  of  large  horizontal 
cells  (5)  ;  6,  outer  plexiform  layer  ;  7,  outer  nuclear  layer  ;  8,  external 
limiting  membrane  ;  9,  visual  cells  ;  10,  rods  ensheathed  in  pigment  (light- 
adaptc'l)  (Azan  ;     X  112)  (Katharine  Tansley). 


FISHES 


307 


40%  more  rods  than  the  doi.sal  area  (]M(jore  et  al.,  1950),  iu  tlie  pelagic  dragonet, 
Callionymus,  the  dorsal  half  is  almost  entirely  populated  by  cones,  the  ventral 
by  rods  (Vilter,  1947),  while  in  the  sardine,  Clupea  pUchardus,  which  feeds  on 
Crvistaceans  in  the  water  above  it,  this  relationship  is  reversed  (Vilter,  1950). 
This  adaptation  may  develop  with  the  growth  of  the  fish  and  a  change  in  its 
habitat ;  thus  in  the  elver  (and  cavernicolous  eels)  the  rods  are  more  numerous 
in  the  ventral  part  of  the  retina,  while  in  adult  eels  in  rivers  they  are  more 
numerous  in  the  dorsal  area,  (Vilter,  1951). 

The  rods  are  usually  small,  elongated  and  very  numerous,  although 
in  some  species  (the  cat-fish,  Ameiurus)  they  are  thick,  plump  and  few  in 
number  (18,400/sq.  mm.).    The  cones,  in  contradistinction  to  the  rods, 


Ameiurus 


Figs.  347  to  349. 


-The  Visual  Cells  of  Teleosts  (x  1,000) 
(Gordon  Walls). 


i 


4- 


! 


Fig.   341 


Fig.  348. 


Fig.   347. — The  cone  and  rod  of  the  goldfish,  Carassius. 

Fig.  348. — A  single  cone,  a  twin  cone  and  a  rod  of  the  pike-perch, 
Stizosiedion. 

Fig.  349. — The  twin  cone  of  the  sunfish,  Lepomis  (light-adapted)  and 
the  conjugate  element  of  Fundulus  (after  Butcher,  1938). 

c,  "clear  mass"  and  g,  "granular  mass"  in  the  conjugate  element; 
e,  ellipsoid  ;  /,  footpiece  ;  /,  external  limiting  membrane  ;  //(,  myoid  ; 
n,  nucleus  ;    o,  outer  .segment. 


308 


THE   EYE   IN  EVOLUTION 


Fundnlus 


are  relatively  bulky  (Fig.  347).  These  are  remarkable  for  the  presence 
of  twin  and  double  cones,  double  cones,  seen  also  in  Holosteans  and 
widely  distributed  among  most  Vertebrates,  occur  in  many  Teleosteans 
such  as  the  roach,  Rutilus  (Greeff,  1899),  the  goldfish  (Walls,  1942), 
some  of  the  Salmonidse  (Verrier,  1935  ;  McEwan,  1938),  the  kilhfish, 
Fundulus,  and  others.  They  were  first  described  by  Hannover  (1840), 
M.  Schultze  (1867)  and  Dobrowolsky  (1871)  and  consist  of  the  fusion 
of  two  dissimilar  cones  in  the  lower  myoid  region,  one,  a  large  cone, 
being  the  chief  element  and  the  only  one  which  participates  in  photo- 
mechanical movements,  the  other,  a  smaller  accessory  element  with  an 
unusually  large  paraboloid.  There  are  two  nuclei,  and  the  two  foot- 
pieces  may  connect  with  different  bipolar  cells,     twin  cones,  on  the 


I  ♦  %^    *         If 


A«> 


Fig.  3.50. — Triple  and  Quadruple  Cones  in  a  Teleostean  Fish. 
A  tangential  section  through  the  retina  of  the  minnow,  Phoxinus  Icpvis, 
to  show  double,  d,  triple,  t,  and  quadruple,  q,  cones  (  X  500)  (A.  H.  Lyall). 


Salmo  trutta 


other  hand,  are  found  only  in  the  teleostean  retina  in  which  their 
occurrence  is  widespread  (Fig.  348-9).  In  these  the  two  elements, 
fused  throughout  their  entire  inner  segments,  are  identical  and  both 
contract  and  elongate  in  photomechanical  movements.  Twin  cones 
are  more  numerous  in  the  central  retina  than  the  peripheral  and  in 
surface  fish  than  deep-sea  types  ;  in  some  particularly  active  species 
they  are  the  only  cone  elements  encountered  (flat-fishes  ;  some  species 
of  scorpion-fish,  Scorpcena  ;  cod,  Gadus  ;  etc.)  (Wunder,  1925-30). 
While  they  are  thus  associated  with  vision  in  bright  light,  they  do  not 
seem  to  subserve  accuracy  of  vision  since  they  are  absent  from  the 
fovea  when  this  is  present. 

MULTIPLE  CONES  (triple  and  quadruple)  have  been  described  by  Lyall 
(1956-57) — triple  cones  ^  in  the  retina  of  the  trout,  Salmo  trutta,  which  appear  to 
be  anomalous  double  cones  ;  and  triple  and  quadruple  cones  in  the  retina  of  the 
minnow,  Phoxinus,  where  they  occur  in  considerable  numbers  (Fig.  350).     In 


'  Triple  cones  have  also  been  described  in  the  frog,   Bana  temporaria    (p.    342) 
an<l    Me  gecko,  Aristelliger  (p.  364).     See,  however,  p.  253. 


FISHES 


309 


this  species  the  triple  cone  consists  of  a  large  central  cone  with  two  smaller  ones 
on  either  side  of  it  ;  the  quadruple  cones  are  formed  by  three  small  cones 
grouped  symmetrically  around  a  large  central  cone.  A  physiological  explanation 
of  the  significance  of  double,  twin  or  multii)le  cones  has  not  yet  been  advanced.^ 

In  most  Teleosteans  the  retina  shows  a  circumscribed  region 
where  it  is  thicker  and  more  liighly  j^acked  with  visual  elements  than 
is  the  remainder  of  the  fundus,  constituting  an  ill-defined  area  centralis  ; 

Figs.   .3.")1   to  3.')8. — The  Fovea  of  Teleosts. 


Fig.   3")1. — Section  through  the  fovea  of  the  blenny,  Blennius. 


Fig 


3o2.— The  fovea,  Fo,  of  the  sea- 
horse, Hippocampus. 


Fig.  3.53. — The  fovea,  Fo,  of  the  sea- 
bass,  Serranus  (Kahmann,  v.  Graefes 
Arch.  Ophthal). 


here  the  density  of  the  cones,  the  bipolar  cells  and  the  ganglion  cells 
is  increased.  In  the  guppy,  Lebistes,  and  the  killifish,  Fundulus,  the 
area  is  apparently  duplicated,  one  lying  axially,  another  ventrally 
(Vilter,  1948).  In  a  number  of  species,  particularly  the  agile  and  lively 
inhabitants  of  the  littoral  zone,  a  fovea  is  present  in  addition  in  the  hori- 
zontal meridian  of  the  temporal  retina  (Kahmann,  1934-36)  (Figs.  351-3). 
Among  Fishes  this  is  unique  to  Teleosteans.  It  usually  takes  the  form 
of  a  shallow  pit,  inferior  in  its  retinal  differentiation  to  the  correspond- 
ing area  in  lizards, Birds  and  Primates,  but  it  may  be  well  formed  (pipe- 
fish, Syngnathus — Krause,   1886  ;    the  labrid,  Jul  is,  and  the  blennj-, 

1  p.  253. 


Syngnathun 


310 


THE   EYE   IN   EVOLUTION 


Blennius 


Bathylagus 


Blennius — Verrier,  1933)  and  on  occasion  is  deep  and  highly  organized, 
as  in  the  sea-bream,  6VreZZa  (Verrier,  1935).i  With  few  exceptions  such  as 
the  sea-horse,  Hippocampus,  where  it  is  nearly  central  (J.  Carriere,  1885), 
it  is  typically  situated  temporally  in  the  region  of  the  retina  which  could 
be  used  for  binocular  vision.  In  this  region  rods  and  twin  cones  are 
excluded  and  the  single  cones  are  densely  packed,  long  and  rod-like, 
while  the  other  retinal  layers,  including  the  ganglion  cells,  become 
attenuated  but  do  not  disappear.  It  is  interesting  that  in  some  deep- 
sea  Teleosts  {Bathyfrocfes,  Bafhylagus)  with  a  pure-rod  retina,  the 
rare  occurrence  of  a  temporal  fovea  populated  with  rods  is  found 
(Brauer,  1908)-;  in  Bafhylagus  there  are  6  superimposed  rows  of  rods 
in  this  region  instead  of  the  usual  3  found  elsewhere  in  the  retina 


Fig.  354. — The  Optic  Xerve  of  Teleosts. 

Cross-section  of  the  optic  nerve  of  Serranus  cahrilla  showing  the  folded 
ribbon  structure  (after  tStudnicka). 


Hippocampus 


(Vilter,    1954),    an   arrangement   which   may   act   by   increasing   the 
sensitivity  to  light. 

The  optic  yierve,  even  in  Teleosteans,  is  relatively  primitive  (Ucke, 
1891  ;  Deyl,  1895  ;  Lumbroso,  1935).  In  many  species  the  disc  is 
narrow  and  oblong,  for  the  nerve  fibres  leave  the  retina  not  only  at  this 
point  but  for  some  distance  along  the  open  foetal  fissure.  The  nerve 
thus  emerges  from  the  eye  as  a  tape  rather  than  a  cord  assuming  a 
circular  cross -section  in  the  orbit,  and  on  section  the  nerve  fibres  appear 
as  a  broad  pleated  ribbon  folded  concertina-like  to  accommodate  itself 
into  its  tubular  sheath  (Fig.  354).  In  a  few  species  on  approaching  the 
globe  the  nerve  divides  into  as  many  as  a  dozen  strands  so  that  it  enters 
the  eye  in  multiple  rootlets  with  a  corresponding  number  of  optic  discs 
(the  bull-head  catfish,  Ameiurus,  the  loach,  Misgurnus,  and  the 
deep-sea  Polyipnus).^    A  septal  system  may  be  absent  or  represented 

1  Other  foveate  Teleosts  are  the  butter-fish,  Pholis,  the  puffer-fish,  Tetraodon,  the 
sea-bass,  Serranus,  the  trigger-fish,  Batistes,  and  the  weever,  Trachinus. 

-  See,  also,  pp.  365,  382,  486. 

^  This  peculiar  arrangement  is  also  seen  in  Pohjpterus,  some  salamanders  and  some 
meiiSfirs  of  the  deer  family. 


FISHES 


311 


by  a  few  large  sej^ta  (the  sword-fish,  Xipliias,  the  eel,  Anguilla),  but  as 
a  general  rule  the  simple  ependymal  core  of  the  Cyclostomes  has 
developed  into  a  more  mature  system  wherein  the  oligodendroglial 
cells  are  scattered  in  a  nerve  which  is  not  sharply  fasciculated  (Prince, 
1955).  At  the  chiasma  a  total  decussation  of  the  nerve  fibres  occurs, 
sometimes  as  a  simple  crossing  of  two  intact  nerves,  occasionally  (as 
in  the  herring)  one  nerve  button-holing  through  the  other,  or  crossing 
in  the  form  of  interlacing  bundles  (Hannover.  1852  ;  Parker,  1904  ; 
Mayhoff.  1912  ;    Verrier.  1930)  (Figs.  355  to  357). 

It  is  interesting  that  Kasquin  (1949)  reported  re-mj-elination  of  the  optic 
nerve  and  the  return  of  vision  4  weeks  after  section  of  the  optic  nerve  in  Astyanax 
mexicanus,  provided  the  cut  ends  of  the  optic  nerve  were  approximated. 


Figs.   .355  to  357. — The  Chiasma  of  Teleosts. 


Fig.  355. — The  usual  con- 
figuration :  the  simple 
crossing  of  intact 
nerves. 


Fig.  356. — The  herring  : 
the  button-holing  of 
one  nerve  bv  another. 


Fig.  357. — The  parrot- 
fish  :  the  interlacing  of 
bundles. 


THE  OCULAR  ADXEXA.  The  eyeball  is  marked  off  from  the  surface 
of  the  head  by  a  circumocular  sulcus,  a  shallow  depression  between 
the  corneal  epithelium  and  the  skin  running  circumferentially  around 
the  globe  ;  tliis  represents  the  conjunctival  sac  and  affords  the  globe 
the  small  liberty  of  movement  it  possesses.  The  outer  margin  of  this 
sulcus  constitutes  a  poorly  developed  lid-fold— the  only  representa- 
tive of  eyelids.  Such  a  rudimentary  arrangement  is  in  marked  contrast 
to  the  relatively  well-formed  lids  in  Selachians. ^  In  a  number 
of  swift -swimming  pelagic  types,  however,  particularly  the  herrings 
(Clupeidse)  and  the  mackerels  (Scombrida?),  the  eye  is  partially  covered 
by  adipose  lids,  thui  cutaneous  folds  often  enclosing  fatty  tissue 
arising  from  the  outer  lip  of  the  circumocular  sulcus.  They  are  usually 
vertically  disposed,  one  anteriorly  and  one  posteriorly  so  that  when 
these  fids  are  well  developed  the  aperture  is  a  narrow  vertical  elHpse, 
as  in  the  skip-jack,  Pomolohus  ;  occasionally  they  are  fused  so  that 
the  globe  is  covered  except  for  a  circular  opening  opposite  the  pupil, 
as  in  the  mullet,  Mugil  ;  rarely  the  skin-folds  fuse  completely  across 
the  eye  (as  in  the  anchovy,  Engraidis,  and  relatives  of  the  herring 
such  as  Chanos)  (Hein,   1913  ;    Walls,   1942).     In  this  last  event  the 


1  p.  289. 


312  THE   EYE    IN   EVOLUTION 

fused  lids  become  extremely  thin  and  transparent  forming  a  "  secondary 
spectacle  ",^  and  between  them  and  the  corneal  epithelium  there  is  a 
closed  "  conjunctival  sac  "  lined  by  epithelium  (Fig.  279). 

The  Salmonidae  (the  salmon-trout  family)  have  a  peculiar  arrangement  of 
lids.  The  posterior  lid  is  of  the  usual  type  but  the  anterior,  which  has  been 
called  a  false  nictitating  membrane,  is  not  derived  from  the  skin  of  the  circum- 
ocular  sulcus  but  is  represented  by  a  broad  triangular  fold  arising  deeply  from 
the  anterior  rim  of  the  membranous  orbit. 

The  orbit  is  bony  and  completely  enclosed  ;  its  roomy  cavity  is 
filled  with  loose  tissue  and  venous  sinuses  serving  as  a  cushion  for  the 
globe,  which  is  sometimes  anchored  by  a  tenacular  ligament.  The 
extra-ocular  muscles  correspond  with  those  of  Selachians  and  are 
carried  through  canals  in  the  orbital  bones  where  they  find  insertion, 
an  anterior  canal  serving  the  obliqiies,  a  posterior  the  recti  (Corning, 
1900  ;   Allis,  1922)  (Fig.  293). 

THE    DIPNOAN    EYE 

THE  DIPNOI  (lung-  OR  MUD-FISHES)  are  a  very  primitive  stock  with  three 
surviving  representatives — Protopterus,  the  African  lung-fish  which  bvirrows  in 
the  earth  in  the  dry  season,  the  eel-like  Lepidosiren  from  the  swamjDS  of  the 
Amazon,  and  the  6-foot  long  Neoceratodus  from  Queensland  (Figs.  358-360). 

Figs.  358  to  360. — Extant  Dipnoan  Fish. 


Fig.   358. — Protopterus. 


Fig.  359. — Lepidosiren. 


Fig.  360. — Neoceratodus. 


The  eyes  of  the  first  species  have  received  some  perfunctory  study 
which  has  shown  them  to  be  very  primitive  structures  indeed  (Hosch, 
1904  ;  Grynfeltt,  1911)  :  those  of  the  second  have  been  described 
by  Eochon-Duvigneaud  (1943)  (Fig.  361).  As  in  the  Cyclostomes, 
there  is  a  dermal  cornea  separate  from  the  scleral  cornea,  allowing  free 

1  p.  266. 


FISHES  313 

rotation  of  the  eye  under  the  transparent  skin.  The  thin  scleral 
cartilage  reaches  only  to  the  equator,  and  there  is  no  amiular  ligament 
or  nieshwork  in  the  angle  of  the  anterior  chamber,  no  ciliary  body, 
zonule  or  muscles,  and  apparently  no  accommodative  mechanism. 
The  choroid  is  extremely  thin  and  lightly  pigmented  without  an 
argentea,  and  there  is  a  well-developed  membrana  vasculosa  retinae 
which,  however,  can  be  separated  from  the  retina  only  with  difficulty. 
The  iris  shows  no  evidence  of  pupillary  musculature. 

The  retina  shows  several  peculiarities.    The  cells  of  the  pigmentary 


Fig.   361.  Fig.   362. 

Fig.  361. — Diagram  of  a  Dipnoau  eye. 

Ch,  choroid  ;  CE,  corneal  epithelium  ;  IC,  intermediate  corneal  tissue 
MV,  membrana  vasculosa  retina?  ;  OX,  optic  nerve  ;  S,  scleral  cartilage 
Sc,  sclera  ;    SC,  scleral  cornea. 

Fig.  362. — The  pupil  of  Xeoceratodus. 


epithelium  are  enormously  large  so  that  this  layer  is  thicker  than  the 
entire  choroid  and  they  are  provided  with  numerous  long  filamentary 
processes  (Fig.  363).  In  the  visual  retina  the  outer  nuclear  layer  con- 
sists of  2  rows  of  cells,  the  inner  nuclear  layer  of  4,  and  there  is  a  single 
row  of  ganglion  cells.  The  rods  are  unique — enormous  and  cone-like 
with  a  large  oil-droplet  (except  in  N eoceratodus)  and  a  paraboloid — 
probably  representing  a  very  primitive  type,  derived,  according  to 
Walls  (1942),  from  an  archaic  early  cone;  in  Protopterus  the  cones  are 
of  two  forms,  single  and  double,  also  provided  with  oil-droplets  confined 
to  one  member  of  the  double  cone  (Fig.  364)  ;  in  A^ eoceratodus  there 
are  single  cones  onl}-  ;  and  in  Lepidosiren  the  cones  are  absent  and  the 
retina  is  pure-rod  (with  oil-droplets)  (Kerr,  1902-19). 

In  Profopterns  the  optic  nerve,  as  is  seen  in  Cyclostomes.  is  a 
single  cord  with  an  ependymal  core  ;   in  Lepidosiren  and  N eoceratodus 


314 


THE    EYE   IN   EVOLUTION 


Figs.   363  and   364. — Thk  Retinal  Elements  of  Protopterus 
(Gordon  Walls). 


C      C 


Fig.  363. — A  Pigment  Cell. 
Showing  a  mass  of  filamentous  pro- 
cesses laden  with  pigment  sharply 
differentiated  froni  the  body  of  the 
cell,  r  and  c  represent  the  spaces 
occupied  by  the  rods  and  cones  respec- 
tively (  X  500). 


Fig.  364. — A  Single  Cone,  a  Double 
Cone  and  a  Rod. 

Members  of  the  double  cone  are 
unusually  loosely  associated.  There 
is  an  oil -droplet  in  the  single  cone  and 
one  member  of  the  double  cone.  The 
rods  are  large  and  have  an  oil -droplet 
as  well  as  a  paraboloid  (  X  1,000). 


the  nerve  divides  into  a  number  of  bundles  each  with  a  similar  core,  as 
if  the  primitive  optic  nerve  of  the  lamprey  had  reduplicated  itself 
several  times  and  all  the  nerve -cords  had  been  gathered  in  one  sheath  ^ 
(Prince,  1955). 


THE    CCELACANTH    EYE 

THERE  IS  ONLY  ONE  SPECIES  of  this  ancicnt  order  of  fishes  known 
to  be  extant —  Latimeria  (Fig.  365) — lately  and  surprisingly  discovered 
in  the  Indian  Ocean  off  the  coasts  of  South-East  Africa.  The  eye  of 
this  species  is  of  great  interest,  showing  characteristics  closely  resem- 
bling those  of  Selachians  on  the  one  hand  and  Chondrosteans  on  the 
other,  clearly  demonstrating  the  remarkable  unity  of  this  organ  through- 
out the  vertebrate  phylum. ^  In  general  its  structure  shows  adaptation 
for  vision  in  the  ocean  depths  where  little  light  is  available.  For  this 
reason  trie  eye  is  unusually  large  and  takes  the  general  form  of  a  flat- 


1   See  also  snakes,  p.  392. 


-  p.  234. 


FISHES  315 

tened  sphere  with  a  relatively  short  antero-posterior  diameter  (Millot 
and  Carasso,  1955)  (  Figs.  3()B-7). 

The  cornea  is  flat  and  the  sclera  lined  by  a  continuous  cartilage, 
thin  (0-5  mm.)  in  front  and  thick  (1-8  mm.)  posteriorly  where  it  encircles 
the  optic  nerve.  As  with  most  fossil  Crossopterygians  and  as  in 
C'hondrosteans.  there  is  a  pericorneal  ring  of  calcified  scleral  plaques, 
18  to  20  in  number.  The  choroid  is  thin,  the  choriocapillaris  being 
particularly  tenuous,  and  there  is  a  well-formed  cr3\stalline  tapetum 
which,  being  continued  over  the  anterior  surface  of  the  iris,  gives  the 
eye  a  brilliant  metallic  sheen.  The  ciliary  zone  is  particularly  rudimen- 
tary, showing  no  I'adial  folds  nor  any  structure  resembling  a  cam^^anula 


Fig.  365. — The  CVxlacanth,   Laiimeria   cuALCMy.E. 
(1,16  natural  size)  (after  Giinther  and  Deckert). 

or  other  focusing  apparatus.  The  lens,  which  approaches  the  cornea 
leaving  a  very  shallow  anterior  chamber,  is  almost  spherical  and  large. 
The  retina  is  completely  avascular  and  shows  no  area  centralis. 
As  would  be  expected  in  the  presence  of  the  tapetum.  the  epithelium 
is  devoid  of  pigment.  The  visual  cells  are  practically  entirely 
represented  by  long,  thin  rods  ;  cones  are  very  rare  and  contain  well- 
defined,  colourless  oil-droplets,  again  recalling  the  corresponding 
structures  in  the  chondrostean  eye.  The  general  architecture  of  the 
retina  is  poorly  differentiated  although  Mliller's  cells  are  particularly 
numerous.  Ganglion  cells  are  few  and  their  ratio  to  visual  elements  is 
remarkably  low.  The  eye  is  characterized  by  its  great  simplicity  and 
priniitiveness,  presumably  possessing  a  high  sensitivity  to  light  but 
a  rudimentary  visual  acuity. 

THE    CHOXDROSTEAX    EYE 

THE  CHONDROSTEAXS  are  represented  today  only  by  the  sturgeons  and  the 
Polypterini.  The  sturgeons  are  a  group  of  old-fashioned  marine  fi.shes  which 
ascend  rivers  to  shed  their  spawn  (caviare)  in  the  Xorthern  hemisphere,  and 
are  today  represented  by  Acipenser  (Fig.  368)  and  a  few  related  genera — Polyodon. 
the  spoonbill  sturgeon  of  the  Mississippi,  Psephurus,  an  enormous  fish  of  the 
Yangtze-Kiang   in   China,    and   Scaphirhynchus,    the   shovel-nosed   sturgeon   of  Polyodon 


316 


THE   EYE   IN   EVOLUTION 


Figs.    366    and    367. — The  Eye   of  the   Ccelacanth   (from  a  specimen  of 

J.   Millot,  Paris). 


Fig.  366.  The  general  configvn-ation  of  the  eye  showing  the  short  antero- 
posterior diameter,  the  large  cornea  through  which  the  lens  is  visible, 
and  the  peri-corneal  ring  of  calcified  scleral  plaques. 


Fig.    /-G7. — Section  of  the  eye  .showing  the  large  spherical  lens  lying  close  to 

the  cornea. 


FISHES  317 

North  America  and  Asia.  They  are  the  largest  fish  inhabiting  fresh  water  and 
are  the  most  primitive  of  the  bony  fishes,^  showing  many  selachian  charac- 
teristics. 

In  its  general  shape  the  globe  of  the  sturgeon  is  flattened  as  is  usual 
in  fishes  (Figs.  3(59-70).  The  cornea  has  the  standard  layering  and 
Descemefs  endothelium  is  piled  up  at  the  angle  of  the  anterior  chamber 
to  form  an  annular  ligament  which  fills  the  angle  with  loose  tissue 
refiected  onto  the  iris  (Baecker.  1931).  The  sclera  is  usually  tliick  and 
its  inner  half  is  occupied  by  an  immensely  thick  scleral  cartilage  which 
forms  a  feature  of  the  eye  ;  and  in  some  species  two  crescentic  bony 
plaques   lie.   one   superiorly  and   one    inferiorly,   athwart    the  hmbus 


Fig.  368. — The  Sterlet,  AciPEysER  rctbesvs  (Zool.  Soc,  London). 

external  to  the  scleral  cartilage,  extending  onto  the  cornea  where  they 
lie  under  the  epithelium  in  tlie  periphery  (Soemmerring,  1818  ;  the 
CONJUNCTIVAL  EOXE  of  H.  Muller,  1872;  Edinger,  1928). 

The  choroid  is  heavily  pigmented  and  richly  vascular,  being  lined 
externall}'  with  an  argentea  as  in  Teleosteans,  while  its  inner  2/5  just 
external  to  the  choriocajjillaris  is  occupied  by  a  tapetum  lucidum  ^ 
comj^rised  of  some  12  laj^ers  of  cells  packed  with  guanine  crystals 
intersj^ersed  with  occasional  pigment  cells,  the  dense  structure  being 
pierced  at  intervals  by  vessels  supj)lying  the  capillary  layer  for  the 
vascular  layer  of  the  choroid  (Fig.  371)  (Briicke,  1845  ;   Miirr,  1927). 

The  amuscular  ciliary  body  may  hardly  be  said  to  exist 
(Fig.  372)  ;  sui^eriorly  it  gives  rise  to  a  suspensory  ligament  of  the  lens 
resembling  that  of  Teleosts.  and  inferiorly  to  a  papilla  resembling  that 
of  Selachians  which  ajDj^arently  does  not  contain  muscle  fibres  (v.  Hess, 
1912).  The  iris  also  is  devoid  of  muscles  and  like  that  of  the  lamprey 
is  immobile,  while  the  stroma  contains  a  thick  argentea.  a  continuation 
of  the  corresjDonding  layer  in  the  choroid.  The  immobile  puj^il  is  of 
the  form  of  a  vertical  ellipse  {AcijJenser)  (Fig.  368)  or  a  square  with 
rounded  corners  {Scaphirhynchus). 

1  p.  234.  2  p.  609. 


318 


THE   EYE   IN   EVOLUTION 

Figs.  369  and  370. — The  Chondrostean  Eye. 

,ch 

s 


Fig.  369. — Diagram  of  a  Chondrostean  eye. 
S         Ch         R 


ON 


Fig.  370.^ — Drawing  of  the  eye  of  Acipenser  ruthenus  (Rochon-Duvigneaud, 
Les  Yeux  et  la  Vision  des  Vertebres  ;   Masson  et  Cie). 

AL,  annular  hgament  ;  G,  cornea  ;  Ch,  choroid  ;  CP,  cihary  papilla  ; 
CT,  connective  tissue  ;  /,  iris  ;  L,  lens  ;  ON,  optic  nerve  ;  R,  retina  ; 
S,  scleral  cartilage  ;  SL,  suspensory  ligament  ;  SO,  scleral  ossicles  ;  V,  vortex 
vein  ;    Z,  zonule. 


The  retina  is  primitive  in  its  structure  (Dogiel,  1883  ;  Scliieffer- 
decker.  1886).  The  pigmentary  epithehum,  resembling  that  of 
Selachiajis,  is  practically  devoid  of  pigment  throughout  the  sensory 
retina  in     -der  that  the  mirror  effect  of  the  tapetum  may  be  effective 


FISHES 


319 


-T    St'  ~      f'-'   £?«! 


Fig.  371. — The  Tapetum  of  CJhondrosteans. 

The  choroid  of  the  sturgeon,  Acipenser.  The  tapetum,  T,  lying  between 
the  choriocapillaris,  C,  and  the  vessel  layer  of  the  choroid,  V,  pierced  by 
a  large  vessel  from  the  latter  to  supply  the  former.  The  pigment  epithelium, 
P,  is  devoid  of  pigment  apart  from  small  accumulations  on  its  inner  surface 
(a  drawing  after  Miirr). 

(Fig.  371)  ;  in  the  ciliary  region  it  becomes  heavily  j^igniented.  The 
sensory  retina  is  characterized  b}'-  the  large  size  of  the  horizontal  cells, 
the  virtual  absence  of  a  distinct  inner  nuclear  layer,  and  the  small 
number  of  ganglion  cells  which  remain  isolated  without  forming  a 


Fig.   372. — The  Angle  of  the  Anterior  Chamber  of  AciPE.xsEJi. 

A,  argentea  of  iris  ;  AL,  annular  liganient  ;  C,  cornea  ;  Ch,  choroid  ; 
O,  osseous  placjues  ;  R,  retina  ;  S.  scleral  cartilage  ;  V,  vessel  behind  annular 
ligament  ;  Z,  zonule  (from  a  drawing  by  Rochon-Duvigneaud,  Les  Yeux  et  la 
Vision  des  Vertebres  ;    Masson  et  Cie). 


320 


THE   EYE   IN  EVOLUTION 


Polypterus 


definite  layer.  Both  rods  and  cones  are  present  ;  the  rods,  long  and 
thick,  the  cones  single  and  containing  colourless  oil -droplets — the  most 
primitive  Vertebrate  species  in  which  these  appear.  There  is  no  area 
centralis  (Fig.  373). 

In  general  it  would  appear  that  the  eye  of  the  sturgeon  represents  a 
transitional  phase  between  the  selachian  and  teleostean  eye  with  more 
affinities  for  the  former  than  the  latter.  The  scleral 
cartilage  is  of  the  selachian  type,  but  the  subcon- 
junctival bony  plaques  are  an  innovation.  The 
argentea,  present  in  Selachians  as  a  rucUmentary 
layer  in  the  iris,  is  continued  throughout  the  uveal 
tract.  The  foetal  fissure  persists  but  the  retractor 
lentis  muscle  of  Teleosts  has  not  yet  evolved.  The 
immobility  of  the  iris  is  more  primitive  even  than  in 
Selachians.  The  general  architecture  of  the  retina  is 
selachian  in  its  simplicity  rather  than  teleostean  in 
its  perfection  ;  but  the  appearance  of  oil-droplets  at 
an  early  stage  among  Vertebrates  in  the  cones  is  an 
interesting  phylogenetic  innovation. 

The  POLYPTERiNi  are  represented  only  by  two 
archaic  types  both  inhabiting  African  waters — 
Polypterus  and  Calamoichthys.  The  eyes  of  the 
former  were  studied  by  Ley  dig  (1854)  and  Rochon- 
Duvigneaud  (1943),  and  the  latter  also  by  Roclion- 
Duvigneaud  (1943).  In  Polypterus  the  eye  appears 
to  resemble  that  of  Amia^  and  is  of  the  teleostean 
type.  The  cornea  is  not  divided  and  Bowman's 
membrane  is  lacking  ;  there  is  a  continuous  scleral 
cartilage  without  bony  enforcement,  an  argentea 
lining  the  choroid  but  poorly  represented  in  the  iris,  and  a  spherical 
lens.  There  is  no  open  foetal  fissure,  no  choroidal  gland  but  an 
extensive  membrana  vasculosa  retinse,  no  pupillary  musculature,  no 
tensor  choroideae,  and  a  poorly  developed  annular  ligament.  The  rods 
are  large,  the  cones  are  single  and  contain  oil-droplets,  the  ganglion 
cells  are  scanty  and  do  not  form  a  definite  layer,  and  the  optic  nerve 
which  has  the  lamellar  structure  of  the  teleostean  type,  is  branched 
with  multiple  optic  discs  (Studnicka,  1898). 


Fig.     373.  —  The 
Visual  Ele- 

ments    OF     Aci- 

PESSER         FULVES- 

CEN.S. 

A  cone  (contain- 
ing a  colourless  oil- 
droplet)  and  a  long 
thick  rod  (  X  1,000) 
(Gordon  Walls). 


Calamoichthys 


The  eye  of  Calamoichthys  is  of  the  same  general  structure  but,  according  to 
Rochon-Duvigneaud  (1943),  the  retina  is  exceedingly  thin,  with  few  cellular 
elements  of  any  kind,  the  short  and  thick  visual  cells  being  of  one  type  only 
having  the  morphological  characteristics  of  cones  some  of  which  are  provided 
with  an  oil-droplet. 

»  p.  321. 


FISHES 


321 


THE    HOLOSTEAN    EYE 

TWO  EXTANT  REPRESENTATIVES  are  all  that  leniaiii  of  the  very 
ancient  group  of  Holosteans,  both  confined  to  North  American  waters 
— the  bow-fin,  Amia,  and  the  gar-pike,  Lepidosieus.  As  the  progenitors 
of  Teleosteans,  it  is  to  be  expected  that  their  eyes  resemble  the 
teleostean  type  (Ziegenhagen,  1895  ;    Franz.  1934). 


A  m  ia 


Figs.  374  and   375. — The  Visual  Elements  of  Am/a 


Lepidosieus 


Fig.   374. 


Fig.   375. 


Fig.  374. — Tlic  cones  of  Amia  ;    a  single  cone  and  a  double  cone. 
Fig.  375.— a  rod  of  Amia  (  X  1,000)  (Gordon  Walls). 


The  sclera  has  a  complete  cup  of  hyaline  cartilage  ;  the  cornea  is 
tinted  a  yellow  colour  (Walls  and  Judd,  1933)  and  the  laminated 
substantia  propria  is  homogeneous  ;  the  annular  ligament  at  the  angle 
of  the  anterior  chamber  is  marked.  The  choroid  has  typical  teleostean 
features  with  an  argentea,  a  large  choroidal  gland  (in  Amia  only),  a 
falciform  process  and  a  campanula  with  an  ectodermal  muscle  ;  there 
is  a  dorsal  suspensory  ligament  and  (as  in  some  Teleosts)  a  membrana 
vasculosa  retinae,  the  vessels  of  which,  however,  enter  at  the  mid- 
ventral  point  of  the  ora.    The  iris,  over  which  the  argentea  is  prolonged. 


S.O. — VOL.  I. 


322 


THE   EYE   IN   EVOLUTION 


is  devoid  of  muscles  and  the  pupil  is  slightly  oval  with  the  long  axis 
vertical,  moving  only  passively  when  the  lens  moves  in  accommodation. 
The  retina  is  typically  teleostean,  and  contains  double  cones  (Fig.  374)  ; 
there  are,  however,  no  twin  cones  nor  an  area  centralis.  The  optic 
nerve  is  of  the  teleostean  type,  with  a  broad  ribbon  of  nerve  fibres 
folded  over  itself  in  pleats  within  the  tubular  sheath. 

ANOMALIES    IN    THE    EYES    OF    FISHES 

In  a  group  so  heterogeneous  as  the  Fishes  it  is  not  surprising  that 
many  modifications  to  the  general  form  arise  ;  some  of  the  most 
important  of  these  deserve  a  passing  note. 

THE    TUBULAR    OR    TELESCOPIC    EYE 

We  have  already  seen  that  lack  of  illumination  in  the  abyssal 
depths  has  led  to  the  development  of  an  immensely  large  lens  to 

Figs.  376  to  379. — The  Tubular  Eyes  of  Deep-sea  Fish. 
Figs.  376  and   377. — The  Hatchet  Fish,  Argyropelecus. 


Fig.   376. — In  the  larva  the  eve  is  directed  forwards. 


Fig.  377. — In  the  adult  the  eyes  are  tubular  and  uijward-looking  ;  the  body 
is  covered  with  luminous  organs  giving  the  scales  a  silvery  gleam 
(compare  Fig.  892)  (after  Goode  and  Bean). 


Fig.  378. — Stylophorus  paradoxus.  An 
inhabitant  of  the  deep  Atlantic.  The 
eyes  are  directed  forwards  and 
sligVilly  upwards  (after  Goode  and 
Bean,  1896). 


Fig.  379.— The  giant-tailed  fish, 
Giganturus  chuni.  An  inhabitant  of 
the  deep  Atlantic.  The  eyes  are 
directed  straight  forwards  (from  the 
Valditia  Reports). 


FISHES 

collect  as  miicli  as  possible  of  the  small  amount  of  light  available,  and, 
indeed,  in  some  species  in  order  to  accommodate  this  structure  the 
eye  may  attain  a  size  more  than  half  the  length  of  the  head  {Bathylagus, 
Zenion,  etc.) — relatively  the  largest  eyes  of  all  Vertebrates.  A  much 
more  economic  arrangement  may  therefore  be  adopted  by  some  deep- 
sea  Teleosts  in  the  tubular  eye  (or  telescojjic  eye)  wherein  the 
unnecessary  volume  of  a  relatively  circular  organ  has  been  eliminated 
in  favour  of  a  cylindrical  shape,  the  axial  portions  only  of  the  globe 


323 


Fig.  380. — The  Tubular  Eye  of  a  Deep-sea  Fish. 

The  eye  of  Scopelarchus  analis,  an  inhabitant  of  the  deep  Atlantic  and 
Indian  oceans,  in  longitudinal  section,  showing  the  enormous  lens  and  the 
general  distortion  of  the  globe.  C,  the  lens  cushion  moved  by  a  muscle,  .1/, 
which  accommodates  for  distance  ;  T,  tapetum  ;  Ch,  choroid  ;  i?j,  accessory' 
retina  ;    R^,  princijjal  retina  ;    O,  optic  nerve  (after  Chun). 


being  retained  in  order  that  the  enormous  lens  might  be  accommodated 
in  an  organ  which  had  not  become  imj)ossibly  large  (Fig.  380).  In 
such  an  e3^e  the  lens  occupies  the  entire  anterior  portion  of  the  globe 
and  the  iris  is  eliminated.  In  order  to  increase  the  visual  field,  however, 
the  "principal  retina  "lying  at  the  bottom  of  the  tube  may  be  reinforced 
by  an  "  accessory  retina  "  continued  up  one  side  ojDposite  which  the 
sclera  remains  transparent  (Brauer,  1908).  In  these  species  the  eye  is 
initially  normal  in  form  and  becomes  tubular  as  growth  proceeds  (the 
hatchet  fish,  Argi/ropelecus,  etc.,  Contino,  1939)  (Figs.  376-7)  ;  in 
some  the  eyes  are  eventually  directed  forwards  ((r/f/f/M^j/rMs)  (Fig.  379)  or 


324 


THE   EYE   IN   EVOLUTION 


Opisthoproctiis 


forwards  and  uj^wards  {Stylophorus)  (Fig.  378)  ;  in  others,  upwards 
{Argyro'pelecus,  OpistJwiiroctus),  in  whicli  case  the  sclera  on  the 
dorsal  aspect  becomes  transparent  and  the  ventral  part  of  the  retina 
assumes  the  function  of  the  "  principal  retina",  so  that  the  optic  nerve 
emerges  from  its  edge  instead  of  from  its  centre  (Fig.  380). 

The  intimate  structure  of  such  an  eye  is  seen  in  Fig.  380.     The  principal 
retina   is  well  formed,   the   accessory   retina  atrophied,   while  the   optic  nerve 

emerges  laterally  between  the  two.  To  move 
the  immense  lens  there  is  a  lens  pad  con- 
trolled to  some  extent  by  muscles  which 
enable  the  eye  to  be  focused  on  a  distant 
object.  On  the  whole,  however,  such  eyes 
are  myopic  and  specifically  adapted  for  the 
perception  of  the  small  amount  of  light  avail- 
able, although  it  is  possible  that  a  sufficiently 
adequate  image  of  prey  may  be  appreciated 
to  allow  its  capture  when  it  approaches  so 
closely  that  it  can  be  snapped  at. 

Such  an  eye  is  found  in  several  species  in 
addition  to  Oiganturus,  Stylophorus  and 
Argyropelecus — some  relatives  of  the  deep- 
sea  salmonids,  Dolichopteryx  and  Winteria, 
and  some  of  the  deep-sea  lantern  fishes 
(Myctophidte),  such  as  some  species  of  Ever- 
manella  and  Scopelarchus. 

It  is  interesting  that  a  "  deformed  " 
tubular  eye  of  this  ty^ie  can  be  produced  by  artificial  selection  in  breeding,  as  is 
seen,  for  example,  in  the  "  telescope-eyed  "  goldfish  (Fig.  381). 


Fig.       381. — The       "  Telescope 

EYED  "    Goldfish     (Zool.     Soc. 
London). 


THE   AMPHIBIOUS    EYE 

Fishes  which  require  to  see  both  under  water  and  in  air  are 
presented  with  the  difficulty  of  combining  two  very  different  optical 
requirements.  In  many  cases  there  seems  to  be  little  structural 
adaptation  to  the  comparative  myopia  of  aerial  and  the  hypermetropia 
of  aquatic  vision  unless  the  accommodative  range  is  unusually  great. 
Very  interesting  modifications,  however,  occur  in  at  least  one 
species — AnabJei^s  teirophthalmus.  the  "  Cuatro  ojos  "  wliich  swims 
sedately  in  quiet  waters  of  South  and  Central  America  in  such  a  way 
that  the  water-line  cuts  across  the  middle  of  the  prominently  raised 
eyes  (Figs.  382  to  384).  This  extraordinarily  interesting  eye  has 
received  a  considerable  amount  of  study  from  the  time  of  Artedi  (1758) 
and  Soemmerring  (1818)  (Schneider  and  v.  Orelli,  1908  ;  Arruga,  1941). 
It  is  provided  with  two  distinct  optical  systems,  the  upper  for  aerial, 
the  lower  for  aquatic  vision.  The  cornea  is  divided  into  two  segments 
b}'-  a  densely  pigmented  horizontal  raphe,  and  the  iris  is  similarly 
divided  so  that  two  pupillary  apertures  are  j)resent  ;  the  lens  is  fusiform 
in  -nape,  its  short  axis  refracting  rays  onto  the  lower  part  of  the  retina 


FISHES 


325 


from  the  upper  (aerial)  pupil  and  its  long  axis  refracting  rays  from  the 
lower  (aquatic)  pupil  onto  the  upjjer  part  (Fig.  385).  It  would  seem 
therefore  that  both  aerial  and  aquatic  objects  are  focused  simul- 
taneously on  different  j^arts  of  the  retina,  the  dioptrics  in  either  case 

Figs.   382  to  3S-J-. — Axablfps  TETnoriiTHALiiv>!. 


Fir;, 


i'l' 


0  5i. 


Showing  the  horizontal  division  of  the  pupil,  the  upper  part  being  adapted 
for  vision  in  the  air,  the  lower  part  in  the  water.  A  Brazilian  specimen 
(N.  Ambache). 


being  catered  for  by  the  peculiar  shape  of  the  lens  (Fig.  766).  The 
four-eyed  blenny.  Dialoymnns  fuscus,  which  frequents  rocks  between 
the  tide-marks,  has  a  similar  division  of  its  otherwise  heavily  pigmented 
cornea  into  two  clear  areas,  but  the  pupillary  aperture  is  single  (Breder 
and  Gresser.  1939).  A  pupil  which  is  practically  double,  however,  is 
seen  in  the  large  serpent  eel  of  New  Zealand.  Leptognathus.  an  inhabitant 
of  the  deep  seas  which  burrows  in  the  mud  (Prince,  1949)  (Fig.  340). 


326 


THE   EYE   IN   EVOLUTION 


Fig.  385. — The  Eye  of  Asableps  in  Vertical  Section. 

The  immense  cornea  (to  the  left)  occupies  2/5ths  of  the  surface  of  the 
globe  and  is  bisected  horizontally  across  the  middle.  Internal  to  the  bisection 
is  seen  the  part  of  the  iris  which  spans  the  anterior  chamber  transversely  to 
create  the  two  j^upils,  the  upper  for  aerial,  the  lower  for  aquatic  vision.  In 
the  lower  part  of  the  choroid  is  seen  the  huge  choroidal  gland  lying  between 
the  detached  retina  and  the  sclera  (H.  Arruga). 


STALKED    EYES 

In  a  few  Teleosteans  the  eyes  are  set  prominently  on  stalks.  An 
example  of  this  is  the  mud-skipper,  Periophthalmus,  found  in  the 
tropical  swamps  of  Asia,  Africa  and  Poljmesia,  which  skips  upon  the 
mud  on  its  stiff  f)ectoral  fins  seeking  insects  (Fig.  386).  The  eyes  are 
retractile  and  can  be  withdrawn  for  protection  when  they  are  covered 
by  puckered  skin-folds  ;  they  are  raised  by  a  hammock  formed  by  a 
crossing  of  the  inferior  rectus  and  inferior  oblique  muscles.     When 


FiG.^3S6. — The  Mljd-skipper,  Fejuophihalmus. 

The  water-line  cuts  the  head  of  the  fish  just  beneath  the  eyes  ;  the 
cor:.  ,il  reflex  is  seen  reflected  immediately  underneath  on  the  surface  of  the 
wat        nhotograph  by  Michael  Soley). 


FI8HES 


327 


accommodating  maximally  the  eyes  are  focused  for  aerial  vision,  and 
to  adapt  the  vision  to  the  bright  sunlight  on  land,  the  inferior  part  of 
the  retina  is  populated  only  by  cones,  while  rods  become  increasingly 
more  numerous  in  its  upper  half. 

The  hammerhead  shark,  Sphyrna  zijgcena,  has  eyes  which  are 
located  far  laterally  at  the  ends  of  the  "  hammers",  and  show  a  peculiar 
adaptation  of  the  extra-ocular  muscles  (Fig.  388).  The  elongation  of 
the  orbits  in  the  lateral  direction  would  ordinarily  necessitate  muscles 

Figs.  387  and  388.— The  Hammerhead  Shark,  Sphyrsa  zycesa. 


Fig.  387.  Fig.  388. 

Fig.  387.— The  dissected  orbit. 

Fig.  388. — The  head,  showmg  the  extraordinarily  elongated  orbits  giving 
the  impression  of  the  heads  of  two  symmetrical  hammers  on  which  the  eyes 
are  perched  (Bland-Sutton's  Lectures  and  Essays  ;    Heinemann). 


of  quite  unusual  length  ;  these,  however,  are  no  longer  proportionately 
than  in  any  other  sjDecies  of  shark  and,  instead  of  being  inserted  at  the 
apex  of  the  orbit,  take  origin  from  a  common  tendon  running  parallel 
with  the  optic  nerve  throughout  the  inner  three-quarters  of  the  orbit 
(Bland-Sutton.  1920)  (Fig.  387).  The  bonnet-shark,  Sjjhyrna  tiburo, 
has  a  head  of  a  somewhat  similar  configuration,  taking  the  shape  of  a 
crescent  with  the  eyes  situated  on  the  widest  part. 

The  most  extraordinary  stalked  eye  among  Teleosts,  however,  is 
seen  in  the  Sti/lophthalmus  j^aradoxus,  the  larva  of  the  deep-sea  Idia- 
canthus  (Brauer,  1908  ;  Beebe,  1934).  The  eye  is  i^erched  on  an 
enormously  long,  freely  movable  stalk  wliich  contains  the  optic  nerve 
and   filamentous   muscles   and   is   supported   by  a   cartilaginous  rod 


Sphyrna  tiburo 


328 


THE   EYE   IN   EVOLUTION 


Fig.   389. — The   Stalked-eyed   Teleost,  Sj i-lopjjthaimus   pahadoxvs,    the 
Larva  of  Ib/acaxthus. 

Showing  the  eyes  at  the  termination  of  the  two  stalks  (after  Brauer). 

Figs.    3'JO    to    392. — Diagram    of    the    Development    of    the    Teleost, 
Idiacanthus  fjsciola  (after  Beebe). 


Fig.   39U. — Young  stalk-eyed  larva,  Sli/lopIitJialmns  paradoxus,   16  mm.  long. 


Fig.  391. — Larva  with  degenerating  eye,  40  mm.  long. 
Fig.  392. — Adult  male  Idiacanthus. 


Plaice 


Sole 


rooted  on  the  skull  (Figs.  389,  390).  In  the  adult  the  eyes  retract  into 
a  normal  position,  the  cartilaginous  rod  becoming  folded  upon  itself 
into  a  tangled  mass  in  the  orbit  (Figs.  391-2). 

THE    MIGRATORY    EYE 

This  is  a  curious  phenomenon  seen  in  the  many  types  of  flat-fishes. 
In  the  Selachians  which  are  compressed  dorso-ventrally,  the  two  eyes 
migrate  equally  towards  the  dorsal  mid-line  so  that  they  are  directed 
more  or  less  skywards.  The  flat  Teleosteans  (which  include  such  food- 
lishes  as  halibut,  plaice,  turbot  and  sole)  when  young  have  the  normal 
t<rrnedo -shaped  body  of  a  fish  and  they  swim  with  the  usual 
oj;     tation  with  laterally  directed  eyes  ;    but  at  a  later  stage  when 


FISHES 


329 


they  remain  constantly  at  the  bottom  of  the  sea,  they  he  upon  one 
side  so  that  the  eye  wliich  finds  itself  underneath  (the  left  eye  in  the 
sole,  the  right  in  the  turbot)  migrates  to  the  upper  side  and  eventually 
lies  alongside  the  other  in  a  hole  formed  in  the  frontal  bone.  The  two 
orbits,  like  the  rest  of  the  head,  are  consequently  very  asymmetrical. 
In  one  species  (Psetfodes)  the  migration  is  incomplete  so  that  the 
migratory  eye  does  not  reach  the  top  of 
the  head.  In  this  way  the  flat-fish  attams 
a  wide  binocular  field  above^,  and  in  many 
species  the  eyes  are  raised  on  ocular 
turrets  so  that  vision  is  still  possible  when 
most  of  the  body  of  the  fish  is  concealed 
under  sand.  In  order  to  avoid  dazzle  in 
the  uj) ward-looking  eyes  of  these  flat- 
fishes, as  well  as  in  some  other  bottom 
fishes,  an  expansile  pupillary  operculum  is 

developed  comparable  to  that  found  in  Batoidei.-  Tliis  structure  may 
be  small,  as  in  the  star-gazer,  Uranoscoi^us  (Fig.  3'.»3)  or  so  large  that 
it  practically  occludes  the  entire  juipil.  as  in  the  cat-fish,  Plecosfomus 
(Fig.  394).   ^ 


Fig.  393. 


Fig.  394. 


Fig.   393. — The  Pupil  of  the 

StAKGAZEB,     U  RAyOSCOPVS. 

Fig.   394. — The  Pupil  of  the 
Catfish,  Plecostomus. 


Abelsdorff.      Arch.    Anat.    PJn/sioI..    Abf. 

Physiol..  34.J  (189(>). 
Addario.    Monit.  ZnnJ.  itnl..  13,  16  (]n03). 
Allen.     Annt.  Ere,  103,  20.",  (1949). 
Allis.    J.  Anat.,  56,  1S9  (1922). 
Angehicci.      Arch,    milcr.    Anat.,    19,    1-j2 

(1881). 
Arey.    Cowdry's  Special  Ciitolocjii.  N.Y.,  2, 

889  (1928). 
Arruga.     O  Olho  do  Qunlr  Alios.  Barcelona 

(1941). 
Artedi.     Seba's  Rfrum  lutluraliiini  thesauri 

descriptions,  Amstel..  3  (17.58). 
Baecker.     Z.  mikr.  Anat.  Forsch.,  26,  412 

(1931). 
Ballowitz.    Anat.  Anz.,  45,  91  (1913). 
Barnett.    J.  Anat.,  85,  113  (1951). 
Barraquer-Cerero.    Arch.  Soc.  Oftal.  Jtisp.- 

amer.,  12,  507  (1952). 
Beebe.     Zoologica  (N.Y.),  16,  149  (1934). 
Beer.    Pfliigers  Arch.  ges.  Physiol.,  58,  523 

(1894). 
Bland-Sutton.         Selected     Lectures     and 

Essays,  4th  Ed.,  London,  76  (1920). 
Bourguignon    and    Verrier.       Bull.    Soc. 

ophtal.  Paris,  273  (1930). 
Brauer.     Wiss.  Ergeb.  dt.sch.  Tiefsee  Expcd. 

"  Valdivia'\\b,  266  (1908). 
Breder  and  Gresser.    Zoologica  (X.Y.),  24, 

239  (1939). 
BrowTi-Sequard.    C.  R.  Acad.  Sci.  (Paris), 

25,  482,  508  (1847). 
J.  Physiol.  Path,  gen.,  2,  281  (1859). 
Briicke.'   Arch.  Anat.  Physiol.,  387  (1845). 

1  p.  679. 


Bruesrh  and  Arev-     J-  comp.  XcuroL,  77, 

631  (1942). 
Cajal.     La  Cellule.  9,  119  (1893). 

Trav.  Lab.  biol.  Madrid.  28,  Appendix,  1 

(1933). 
Carrcre.       Les    muscles    de    Viris    chcz    les 

Selaciens,  Montpellier  (1923). 
Carriere,    J.       Die    Sehorgane    d.     Thiere, 

Vergl.-anat.         da7-f/cstelt,         Mlinchon 

(1885). 
Chrustschoff.      Z.  )nikr.  Anat.  Forsch.,  7, 

121  (1926). 
Contino.     v.  Graefes  Arch.  Ophtlnd..    140, 

390  (1939). 
Corning.     Morphol.  .Jh..  29,  94  (1900). 
Cuvier.      Leqcjns    d'anat.    coniparce,    Paris 

(1805). 
Uenissenko.      Arch.   mikr.   Anat.,   19,   395 

(1881)  :    21,  1  (1882). 
Detwiler.      Vertebrate  Photoreceptors,  N.Y, 

(1943). 
Devi.     Anat.  Anz.,  11,  8  (1895). 
Dobrowolsky.     Arch.  Anat.  Physiol.,  208 

(1871). 
Dogiel.    Arch.  mikr.  Anat.,  22,  419  (1883). 
Edinger.     Anat.  Anz.,  66,  172  (1928). 
Erdl.     DLsquisitiones  de  glandula  choroid- 

eali,  Monarchi  (1839). 
Faravelli.    Atti  ro>/.  Acad.  Sci.,  Torino,  26, 

268  (1890-91). 
Franz.       .Jcnu.     Z.     Xaturtriss.,     40,     697 

(1905)  ;    41,  429  (1906). 
Arch,  vergl.  Uphthal.,  1,  427  (1910). 

■-  p.  287. 


Psettodes 


330 


THE   EYE   IN   EVOLUTION 


Franz.  Zool.  Jb.,  Abt.  Zool.   Physiol.,  49, 
323   (1931). 
Bolk's  Hh.  d.  vercjl.  A^iat.  d.  Wirbeltiere, 
Berlin,  2  (ii),  1009  (1934). 
Garten.       Graefe-Saemisch     Hb.     d.     ges. 
Augenheilk.,  II,  3,  Kap.   12,  Anhang 
(1907). 
Winterstein's   Hb.   d.  vergl.  Physiol.,  3, 
105  (1910). 
Giacomelli.      Atti   Cong.   Soc.    Oflnl.    ital., 

533  (1935). 
Greeff.        Graefe-Saemisch     Hb.     d.     ges. 
Augenheilk.,   II,    1,    (2),   Kap.    5,    74 
(1899). 
Grynfeltt.     Arch.  Anat.  micr.,  Paris,   12, 
475  (1910). 
C.  R.  Acad.  Sci.  (Paris),  150,  420  (1910). 
Bull.  Mens,  Acad.  Sci.  Letlr.  de  Mont- 
pellier,  210  (1911). 
Grynfeltt  and  Demelle.     Bibl.  Anat.,  18, 

17  (1908). 
Haller.    Acad.  d.  Sci.,  76  (1762). 

Opera  anatomici  minora,  Lusanne  (1768). 
Hannover.      Arch.    Anat.    Physiol,    wiss. 
Med.,  320  (1840). 
Das  Auge,  Leipzig  (1852). 
La   retine   de   Vhotnme   et   des   vertebrcs, 
Copenhagen  (1876). 
Harman.    J.  Anat.  Physiol.,  34,  1   (1899). 
Trayis.    ophthal.    Soc.     U.K.,    23,     356 
(1903). 
Harms.     Z.  unss.  Zool.,  131,  157  (1928). 
Hein.      T.   Ned.   Dierk.    Vereen.,   12,    238 

(1913). 
V.     Hess.      Winterstein's     Hb.     d.     vergl. 

Physiol.,  Jena,  4,  1  (1912). 
Hesse.     Zool.  Jb.,  Abt.  Syst.,  Suppl.  7,  471 

(1904). 
Hogben  and  Landgrebe.      Proc.  roy.  Soc. 

B,  128,  317  (1940). 
Hosch.     Arch.  mikr.  Anat.,  64,  99  (1904). 
Kahmann.     Zool.  Anz.,  106,  49  (1934). 
V.    Graefes    Arch.    Ophthal.,     135,    265 
(1936). 
Karsten.     Jena.    Z.   Naturwiss.,   59,    115 

(1923). 
Kerr.    Quart.  J.  Med.  Sci.,  46,  417  (1902). 
Textbook    of    Embryology,    London,     2 
(1919). 
Koch.    Atti  Soc.  Oftal.  ital.,  12,  108  (1950). 
Ann.  Ottal.,  78,881  (1952). 
Atti  Soc.  Oftal.  Lombarda,  7,  197  (1952). 
Ophthalmologica,  126,  58  (1953). 
Kolmer.    Anat.  Anz.,  44,  183  (1913). 
Krause,   W.     Henle's   Hb.    syst.    Anat.  d. 
Menschen,  3  (1876). 
Internat.  Mschr.  Anat.  HistoL,  3,  8,  41 
(1886)  ;    6,  206,  250  (1889). 
Lauber.    Anat.  Hefte,  18,  369  (1901). 
Leuckart.       Graefe-Saemisch    Hb.    d.    ges. 

Augenheilk.,  I,  2  (2),  145  (1876). 
Leydig.    Anat.  Hist.  Untersuch.  ii.  Fische 
u.  Reptilien,  Berlin  (1853). 
Z.  ui    ■'  Zool.,  5,  40  (1854). 
Loeweii  Arch.  Anat.  (Paris),  25,  167 

(193: 


Lumbroso.      Ric.    Morfol.,    14,    163,    257 

(1935). 
Lyall.    Nature  (Lond.),  177,  1086  (1956). 

Quart.  J.  micros.  Sci.,  98,  189  (1957). 
McEwan.    Acta  Zool.,  19,  427  (1938). 
Magnus.     Z.  Biol.,  20,  567  (1899). 
Mann.     Trans,  ophthal.  Soc.  U.K.,  49,  353 

(1929). 
Proc.  zool.  Soc.  Lond.,  21,  355  (1931). 
Matthiessen.     Pflilgers  Arch.  ges.  Physiol., 

38,  521  (1886). 
Mayhoff.     Zool.  Anz.,  Z9,  18  (1912). 
Mayou.     Brit.  J.  Ophthal.,  17,  477  (1933). 
Meader.    J.  Morph.,  59,  163  (1936). 
Michaelson.     Retinal  Circulation  in  Man 

and  Animals,  111.  (1954). 
Millot.       Le    pigment    purique     chez     les 

vertebres  inferieurs,  Paris  (1923). 
Millot    and    Carasso.        C.R.    Acad.    Sci. 

(Paris),  241,  576  (1955). 
Moore.    J.  comp.  Neurol.,  80,  369  (1944). 
Moore,     Pollock    and    Lima.      J.    comp. 

Neurol.,  93,  289  (1950). 
Miiller,    Heinrich.      Z.    wiss.    Zool.,    8,    1 

(1857)  ;    9,  147  (1858). 
Gesamnielte  u.  hinterlassene  Schriften  z. 

Anat.   u.    Physiol,   d.   Auges,   Leipzig 

(1872). 
Miiller,  H.     Z.  vergl.  Physiol.,  37,  1  (1954). 
Miiller,    J.      Arch.    Anat.    Physiol.,     101 

(1840). 
Miiller,  W.     Beit.  Anat.  Physiol.  {Festgabe 

C.  Liidwig),  Leipzig,  2  (1875). 
Miirr.     Z.  Zellforsch.  mikr.  Anat.,  6,  315 

(1927). 
Nemnayer.      Arch.    mikr.    Anat.,    48,    83 

(1897). 
Nussbaum.      Arch.   mikr.   Anat.,   58,    199 

(1901). 
Parker.     Bull.  Mus.  comp.  Zool.,  40,  221 

(1904). 
Prince.    Visual  Development, 'E.iXin.  (1949). 

J.  comp.  Neurol.,  103,  541  (1955). 
Rabl.     Z.  iviss.  Zool.,  63,  496  (1898). 
Ueber  d.  Bau  ti.  d.  Entwicklung  d.  Linse, 

Leipzig  (1900). 
Rasquin.     Physiol.  Zool.,  22,  131  (1949). 
Remotti.     Ric.  Morfol.,  9,  89  (1929). 
Retzius.  Bioloqische     Unterstichungen, 

Stockholm,    1,    89    (1881)  ;     12,    55 

(1905). 
Ridewood.      J.    Anat.    Physio}.,    33,    228 

(1898). 
Rochon-Duvigneaud.  Ann.        Oculist. 

(Paris),  153,  185  (1916). 
Les  yeiLv  et  la  vision  des  vertebres,  Paris 

(1943). 
Schaffer.     Z.  mikr.  Anat.  Forsch.,  18,  37 

(1929). 
Schaper.       Festschr.    z.     70    Geburt.    von 

Kupffer,  1  (1899). 
Schiefferdecker.      Arch.    mikr.   Anat.,   28, 

305  (1886). 
Anat.  Anz.,  2,  381  (1887). 
Schnaudigel.       Ber.    dtsch.    ophthal.     Ges. 

Heidel.,  32,  329  (1905). 


FISHES 


331 


Schneider  and  v.  Orelli.     Mitt.  d.  naturf. 

Ges.  Berne,  87  (1908). 
Schultze,   M.      Arch.  mikr.   Anat.,  2,    175 

(1866)  ;   3,  215  (1867). 
Schultze,     O.       Zur    Entwicklungsges.    d. 

Gefdsssystems  in  Sdugetiere,  Wvirzberg 

(1892). 
Shearer.    J.  comp.  Neurol.,  8,  209  (1898). 
Smelser  and  Chen.     Acta  XVII  Intemnt. 

Cotig.  Ophthal.,  Montreal-X.Y.,  1,  490 

(1954). 
Soemmerring,  D.  W.    De  oculorum  hominis 

animaliumque  etc.,  Goettingen,  p.  68 

(1818). 
Strampelli.     Ric.  Morfol.,  13,  47  (1934). 
Studnicka.      Jena.    Z.    Naturwiss.,   31,    1 

(1898). 
Sverdlick.      Acta    XVII    Internat.    Cong. 

Ophthcd.,     Montreal-N.Y.,     3,      1959 

(19.54). 
V.  Szilv.    V.  Graefes  Arch.  Ophthal.,   109,  1 

(1922). 
Teulieres  and  Beauvieux.     Arch.  Ophtal. 

(Paris),  48,  465  (1931). 
Tretjakoff.     Morphol.  Jb..  56,  402  (1926). 
Z.  wiss.   ZooL,   127,   645   (1926)  ;     137, 

550  (1930). 
Ucke.     Diss..  Dorpat  (1891). 
Verrier.     Bull.  Mtis.  Paris,  33,  361  (1927). 
BuU.  Biol.  France  Belg.,  Suppl.  11,  137 

(1928). 


Ann.  Sci.  nat.  ZooL,  13,  5  (1930)  ;    18, 

205  (1935). 
Bull.  Soc.  zool.  Fratice,  58,  62  (1933). 
C.  R.  Soc.  Biol.  (Paris),  113,  134  (1933). 
Les  yeu.v  et  la  vision,  Paris  (1938). 
Vilter.     C.  R.  Soc.  Biol.  (Paris),  141,  344, 
346   (1947);     142,    292    (1948);     144, 
200  (19.50)  ;    145,  52,  54  (1951)  ;    147, 
1937  (1953)  ;   148,  59,  327,  466  (1954). 
Virchow.    Morphol.  Jb.,  7,  573  (1882). 
Arch.  Anat.  Physiol.,  Physiol.  Abt.,  169 
(1890). 
de    Waele.      Bull.    Mus.    Hist,    nat.,    378 

(1900). 
Walls.       The     Vertebrate    Eye,    Michigan 

(1942). 
Walls  and  Judd.      Brit.  J.   Ophthal,   17, 

641  (1933). 
Woelfflin.      Klin.   Mbl.   Augenheilk.,   126, 

348  (19.55). 
Wiinder.      Z.    vergl.    Physiol.,    3,    1,    595 
(1925)  ;   4,  22  (1926)  ;    11,  749  (1930). 
Z.  u-iss.  Biol.,  Abt.  C3,  1  (1926). 
Yamasaki.     Yokohama  Med.  Bull.,  4,  325 

(1953)  ;    5,  304  (19.54). 
Yatabe.     Keijo  J.  Med.,  3,  15  (1932). 
Young.    Proc.  ray.  Soc.  B,  112,  228  (1933). 
Ziegenhagen.    Beit.  z.  Anat.  d.  Fischaugen, 
Berlin  (1895). 


332 


THE    EYE   IN  EVOLUTION 


Fig.  395. — Andre-Jean-Feancois   Rochon-Duvigneaud   (1863-1952) 


CHAPTER  XII 
THE  EYES  OF  AMPHIBIANS 

One  of  the  most  interesting  figures  associated  with  the  study  of  the  eyes 
of  Vertebrates  was  ANDRE-jEAN-FRANgois  rochon-duvigneaud  (1863-1952) 
(Fig.  395).  Born  in  the  Dordogne,  he  studied  medicine  in  the  Faculte  de  Bordeaux 
and  in  1889  became  an  interne  des  Hopitaux  de  Paris  at  the  Hotel  Dieu  and  a 
Chef  de  Clinic  in  1895.  A  cUnician  and  operator  of  repute,  he  contributed  a 
number  of  excellent  papers  to  ophthalmic  literature,  but  he  was  always  interested 
in  anatomy.  His  doctorate  thesis  (1892)  was  on  the  anatomy  of  the  angle  of 
the  anterior  chamber  and  the  canal  of  Schlemm — a  historic  paper.  His  anatomical 
researches  on  the  human  eye  led  him  to  study  the  eyes  of  animals  and  from  1916 
onwards  numerous  papers  on  this  subject  full  of  painstaking  and  careful  observa- 
tions of  unusual  originality  and  exactitude  appeared  from  his  pen.  A  study  of 
these  papers  reveals  even  to  the  casual  reader  the  delight  it  must  have  given 
him  to  produce  them,  and  it  is  not  surjarising  that  he  retired  from  clinical  jaractice 
in  1926  and  devoted  all  his  time,  working  in  a  small  laboratory  at  his  home,  to 
the  study  of  the  eyes  of  x'arious  species  and  spending  much  energy  in  observing 
the  habitsof  animals  in  all  the  parts  of  France.  His  numerous  papers  on  compara- 
tive anatomy  were  collected  together  in  his  classical  textbook,  Les  Yeux  et  la 
Vision  des  Vertebres  (1943),  and  earned  him  a  well-deserved  international 
reputation.  Nor  was  he  withovit  honour  in  his  own  country,  having  been  elected 
to  the  Academie  de  Medecine  in  France  in  1940.  At  his  death  it  was  truly 
written  :  "  Homme  droit,  desinteresse,  serviable,  c'est  un  grand  savant  modeste 
qui  disparait." 

AMPHIBIA  {ayi(f)[^iov,  double  life)  mark  the  transition  from  aquatic  to 
terrestrial  life.  The  early  forms  found  in  upper  Devonian  strata  and 
probably,  as  we  have  seen,^  sprung  from  the  lobe-finned  Crossoptery- 
gians,  are  extinct.  In  Carboniferous  times-  these  reached  their  prime 
and  some  species  attained  a  gigantic  size  ;  today  relatively  few  types 
are  extant  and  these,  usually  small  in  size  and  sluggish  in  habit, 
generally  live  near  the  water's  edge.  The  main  features  wherein  they 
differ  from  fishes  are  determined  by  their  life  on  land — the  disappear- 
ance of  the  gills  in  adult  life,  the  development  of  lungs  (with  a  three- 
chambered  heart)  from  the  air-bladder,  the  transformation  of  the 
lobed  fins  into  chgital  limbs,  the  (usual)  loss  of  the  scaly  exoskeleton, 
the  adaptation  of  the  ear  to  aerial  vibrations  and  of  the  eye  to  aerial 
vision. 

The  surviving  members  of  this  once  populous  class  are  divided  into  three 
orders  : 

1.  APODA  (d,  without ;  ttov?,  ttoSos,  afoot)  (or  Gymnophiona,  yu^vo?,  naked; 

ocfiLoveos,  serpent-like),  a  peculiar  archaic  worm-like  type  without  limbs  and  of 

burrowing  habit,  are  found  in  the  mud-banks  of  tropical  countries.     They  are 

1  p.  235.  2  p   754 

333 


334 


THE   EYE   IN  EVOLUTION 


Caecilian 


represented  by  the  c^cilians  {ccecus,  blind)  and  a  number  of  related  species 
in  all  of  which  the  eyes  are  degenerate  ;  they  will  therefore  be  discussed 
subsequently.^ 

2.  URODELA  (ovpd,  tail  ;  StjAo?,  visible)  (or  caudata,  cauda,  a  tail),  tailed 
Amphibians,  typified  in  the  salamanders  and  the  newts,  are  generally  divided 
into  7  families.  Of  these  several  are  cavernicolous  in  habit,  having  little  use 
for  eyes  ;  these  are  therefore  often  degenerate  and  are  discussed  at  a  later  stage 
{Proteus,  etc.).^  Others,  such  as  the  newts  {Triturus),  Ambystoma,  and  the 
terrestrial  salamanders,  have  relatively  simple  but  well-formed  eyes. 

3.  ANURA  (d,  privative  ;  ovpd,  tail)  or  tail-less  Amphibians,  consisting  of 
nearly  1,000  different  types  including  the  common  frog  (Kana),  the  toad  (Bufo), 
the  tree-frog  (Hyla),  the  obstetric  toad  (Alytes),  the  Surinam  toad  (Pipa), 
the  African  clawed  toad  (Xenoptis)  and  some  other  species,  have  well-developed 
eyes. 

The  general  characteristics  of  the  amphibian  eye  as  seen  in  the 
last  two  orders  are  as  follows  : 

The  transition  from  water  to  air  and  the  consequent  lack  of  the 
necessity  for  streamlining  the  globe,  allow  it  to  assume  a  spherical  shape. 
Moreover,  the  difference  in  refractivity  between  the  air  and  the  cornea 
allows  this  structure  to  assume  a  7iew  role  in  the  dioptrics  of  the  eye  ;  it 
therefore  becomes  highly  arched  and  its  optical  properties  are  good.  The 
lens  can  therefore  fall  backwards  from  the  cornea  ;  it  still,  however, 
remains  large  and  is  moved  as  a  whole,  thus  retaining  an  accommodative 
mechanism  somewhat  resembling  although  7iot  analogous  with  that  seen  in 
fishes. 

The  visual  elements  are  complex  and  relatively  gross — two  types  of 
rods  and  single  arid  double  cones  rerniniscent  of  those  occurring  in 
Holosteans  and  Dipnoans. 

To  protect  and  moisten  the  cornea,  lids  are  provided,  together  with  a 
harderian  gland  and  a  naso-lacrimal  duct. 


THE    ANURAN    EYE 

THE  EYE  OF  THE  FROG  [Rana)  has  probably  received  more 
detailed  study  than  that  of  any  Vertebrate  other  than  man  (Figs. 
397-8).^  The  globe  is  almost  spherical,  the  cornea  and  the  sclera  main- 
taining the  same  curvature.  The  latter,  after  metamorphosis  from  the 
tadpole  stage,  develops  on  its  inner  aspect  a  cup  of  hyaline  cartilage, 
thickest  at  the  posterior  pole  and  extending  anteriorly  to  beyond  the 
insertions  of  the  rectus  nmscles  ;  it  is  pierced  by  the  foramen  for  the 
optic  nerve  as  well  as  by  small  canals  which  allow  the  passage  of  the 
ciliary  vessels  and  nerves  (Caso,  1931  ;  Yamasaki,  1952).  In  some 
tree-frogs  (Hylidse)  the  scleral  cartilage  is  discontinuous  or  lacking  ; 

1  p.  730.  2  p.  728. 

^  Dating  from  the  description  of  Petit  (1737)  and  Soemmerring  (1818).  See  Gaupp 
(19C  •),  Tretjakoff  (1906),  Walls  (1942),  Rochon-Duvigneaud  (1943).  For  development, 
see  r:  -riep  (1906),  Studnicka  (1913),  Jokl  (1918-20). 


AMPHIBIANS  335 

and  in  one  species  it  is  replaced  anteriorly  by  a  ring  of  bone  {Hypo- 
pachus  incrassatus).  The  cornea  in  the  larval  stage  has  the  duplex  form 
of  many  fishes,  with  the  dermal  ^^ortion  separate  from  the  scleral  ; 
fusion,  however,  takes  place  in  the  adult  so  that  the  fully  metamor- 
phosed structure  has  the  tyj)ical  vertebrate  characteristics  of  a  regu- 
larly-layered epithelium,  a  homogeneously  stratified  substantia  propria 
and  Descemet's  membrane  with  its  tenuous  endothelium. 

The  uvecd  tract  is  well  developed  (Fig.  399).  The  choroid  consists 
essentially  of  a  choriocapillaris  external  to  which  the  heavily  pigmented 
tissue  is  divided  into  two  strata  separated  by  a  layer  of  large  veins, 
traversed  by  broad  pigmented  bands  running  obliquely  (the  vascular 
layer  of  Gaupp,  1904)  ;    there  is  no  true  argentea  or  tapetum,  but  a 


Fig.  396.— The  Frog,  Ba.\a. 

The   disc-sliapcd   patch   behind   and   below   the   eye   marks   the   position 
of  the  ear. 

certain  degree  of  "  eye-shine  "  is  contributed  by  cells  containing  a 
carotenoid  yellow  pigment  and  others  with  crystals  of  guanine. 

The  ciliari/  body  is  well-formed  and  triangular  in  shape.  On  the 
internal  aspect  the  double  laj-er  of  epithelium  is  plicated  into  numerous 
meridional  ciliary  folds  rmmmg  anteriorly  to  the  back  of  the  iris  and 
from  these  the  fibres  of  the  zonule  take  origin  (Teulieres  and  Beauvieux, 
1931).  Dorsally  and  ventrally  these  folds  are  hyper tro jellied,  two  or 
three  neighbouring  folds  dorsally,  a  single  fold  ventrally,  and  in  most 
species  are  continued  to  the  pupillary  margin  where  they  thicken  to 
form  the  dorsal  and  ventral  pupillary  nodules  :  their  function  may  be 
to  keejD  the  iris  away  from  the  lens  and  thus  to  allow  the  aqueous 
humour  to  flow  backwards  when  the  lens  is  drawTi  forwards  in  accom- 
modation (v.  Hess,  1912).  The  mass  of  the  triangular  ciliary  body  is 
occupied  by  a  meshwork  of  vascularized  pigmented  tissue  ;  and  from 
the  scleral  aspect  of  the  triangle  in  the  dorsal  and  ventral  regions  a 
ciliary  muscle    (or  tensor  choroidese)   forms  two   crescentic   slips   of 


336 


THE   EYE   IN   EVOLUTION 


Fig.  397. — Diagram  of  an  Anuran  Ete. 

Ch,  choroid  ;  MV,  nieinbrana  vasculosa  retinae  ;  ON,  optic  nerve  ; 
PL,  protractor  lentis  muscle  ;  PN,  pupillary  nodule  ;  S,  scleral  cartilage  ; 
Sc,  sclera  ;  TC,  tensor  choroidese  ;  V,  hyaloid  vein  ;  VS,  ciliary  venous 
sinus  ;    Z,  zonule. 


Fig.    3'JS. — [Section    through   the    Head    of   the    Frog   to    show   Both 
Eyes   (  x  20)   (Norman  Ashton). 


meridional  smooth  fibres  running  backwards  to  be  inserted  into  the 
choroid.  This  muscle  is  discontinuous  and  is  absent  in  the  lateral 
segments  of  the  globe.  In  the  same  two  regions  a  ciliary  venous  sinus, 
reminiscent  of  a  canal  of  Schlemm,  forms  two  discontinuous  crescents, 
a  dorsal  and  a  ventral,  situated  between  the  sclera  and  the  ciliary 
body,  connecting  the  veins  of  the  iris  with  the  subconjunctival  veins 
(Tretjakoff,  f906).  Also  in  the  same  two  regions  there  are  two  pro- 
tractor lentis  muscles  (Tretjakoff,  1906)  of  mesodermal  origin 
supplied  by  a  branch  of  the  3rd  nerve.  Each,  the  dorsal  and  the 
ventral,  arises  from  the  corneal  margin,  enters  the  ciliary  triangle  and 
is  inserted  into  the  hypertroplued  ciliary  processes.  These  by  traction 
on  th  'lular  fibres  23ull  the  lens  forward  in  accommodation,  approxi- 
mating     is  structure  to  the  cornea  as  in  Selachians  (Figs.  400-1). 


AMPHIBIANS 


337 


The  iris  is  thin  and  dehcate  (Plate  III).  Both  retinal  layers  are 
i:)igmented  and  an  ectodermal  sphincter  and  dilatator  of  myo-epithelial 
cells  are  present  (Grynfeltt,  1906  ;  Tretjakoff,  1900).  The  stroma  is 
thickly  packed  with  melanophores  as  well  as  with  cells  containing  yel- 
low, brown  and  copper-coloured  carotenoid  pigments  often  associated 
with  a  metallic  sheen  due  to  the  presence  of  guanine  crystals.  As  a 
result  the  iris  is  usually  In'illiantl}'  coloured,  as  if  dusted  with  a  golden  or 
bronze  powder  so  that  it  simulates  the  lustrous  appearance  of  old  gold 
or  Chmese  lacquer  ^  (Millot,  1923  :  Mami,  1931).  It  is  often  coloured 
similarly  to  the  skin  of  ^^'hich  at  first  glance  it  appears  to  be  an  integral 
part.  An  almost  constant  feature  is  a  vertical  stripe  often  associated 
with  a  groove  running  do\\7iwards  from  the  lower  pupillary  margin  to 


•^v*^V*  p 


Fig.  399. — The  Ocular  Coats  of  Ra\a. 

Showing  the  rods  and  cones,  r  ;  the  pigmentary  epitheUum,  p  ;  the 
choroid,  c.  divided  into  two  strata  ;  the  scleral  cartilage,  s  ;  and  the  sclera,  sc 
(  X  200)  (Xorman  Ashton). 


the  periphery  of  the  iris  where  it  ends,  presumably  a  relic  of  the  ftetal 
cleft  (Johnson,  1927  ;  Mann.  1931  ).2  The  A^essels  of  the  iris  are 
arranged  in  the  same  general  ^Aan  as  those  of  Fishes  :  several  superficial 
arteries  run  irregularly  and  circumferentially  on  the  surface  taking  a 
tortuous  course  tow^ards  the  pupil  and  draining  into  vems  which  run 
in  a  radial  course  but  lie  at  a  deeper  level  and  are  thus  usually  hidden 
by  the  heavy  pigmentation  (Mann,  1929-31)  (Plate  III  ;  Fig.  402).  In 
the  primitive  clawed-toad,  Xenojnis,  all  the  vessels  are  obscured  by 
pigment. 

1  Some  of  the  colours  seen  are  brilliant  and  c^uite  beautiful — gold  and  brown  spots 
on  chocolate  in  the  ecHble  frog,  Rana  escidenta  ;  red  and  green  dots  in  the  American 
bull-frog.  R.  catesbiana  ;  a  chocolate  stri^De  across  a  gold  and  browni  backgroimd  in  the 
Malayan  bull-frog,  Kaloula  puJchra  ;  gold  speckled  in  russet  in  the  tree-frog.  Hyla,  as 
also  in  the  giant  toad.  Bufo  marinus  ;  gold  and  brown  in  the  common  toad,  Bufo  bufo  ; 
a  brilliant  metallic  green  in  the  gi-een  toad,  B.  viridis  ;  green  and  silver  with  a  horizontal 
stripe  of  brown  in  the  S.  American  toad,  B.  arenarum  ;    and  so  on. 

-  Such  a  pigmeiated  furrow  or  ridge,  sometimes  associated  with  a  pupillary  notch 
is  seen  in  certain  teleostean  Fishes  (herring,  trout,  minnow,  orfe.  cod,  carp.  etc.).  rarely 
in  Reptiles  (the  Bengal  monitor,  Varcmus  bengalensis,  and  Igucnin  titherrulald),  and 
never  in  Urodeles. 

S.O. — VOL.  I.  "- 


Xenopus 


338 


THE   EYE   IN  EVOLUTION 


Fig. 


400. — The   Ciliary   Region   of   the   Frog,  i?.i.v.^    ( X  126)    (Norman 
Ashton). 


Fig.  401. — The  Ciliary  Region  of  the  Frog,   Rasa. 

A  I'adial  section  through  the  inferior  part  of  the  eye.  c,  cornea  ;  cp,  ciliary 
process  ;  cz,  cihary  zone  ;  ha,  hyaloid  artery  penetrating  the  region  of  the 
foetal  iissure  ;  pi,  protractor  lentis  muscle  ;  tc,  tensor  choroidese  ;  vs,  ciliary 
venoi'  inus  ;  sc,  sclera  ;  z,  region  of  zonular  attachment  (Rochon-Duvigneaud, 
Les  J  •        et  la  Vision  des  Verfebres,  Masson  et  Cie,  Paris). 


AMPHIBIANS 


339 


».* 


Fig.  402. — The  Iris  of  the  Frog,   Ra.\a. 
Sliowing  a  large  superficial  artery  (  x  500)  (Xorman  Ashton). 

The  pKpil  is  nsuall}-  circular  in  dilatation  but  on  contraction  takes 
on  varied  shapes,  sometimes  round  {Pipa).  usually  horizontally  oval 
(Rana),  occasionally  forming  a  vertical  lozenge-shaped  slit  (the  spade- 
foot  toad.  Scapliiopus.  Plirynomeriis,  Ah/fes.  Hykt.  etc.)  (Boulenger, 
1890  ;  Johnson,  1927  ;  Mann,  1931  ;  and  others)  (Fig.  4U3).  Otlier 
irregular  shapes  occur,  such  as  the  lieart-shaped  jDupi^l  of  the  fire-bellied 
toad,  BoDibinatcr,  the  diamond-shaj^ed  j^ujiil  of  the  large -fingered  frog, 
Ra7ia  halecina,  the  semicircular  j^upil  witli  the  flat  side  uppermost  of 
the  bull-frog,  B.  caiesbiana .  or  the  pear-shaped  pupil  of  Pelobafes  (Figs. 
403  and  404).  The  jDupils  retain  some  of  the  autonomous  activity 
characteristic  of  Fishes,  contracting  on  the  direct  stimulation  of  light, 
and  for  tliis  purpose  the  sphincter  is  lieavily  pigmented  so  that  its 


Figs.  403  and  404. — Aniran  Pupils. 


00 


♦)(?)(? 


Fig.  403. — The  typical  pupils  of  various  Amphibians  in  the  contracted  state 
(right  eye)  ;  when  dilated  all  are  circular,  (a)  The  Javanese  flying  frog, 
Polypedates  reinwardti  ;  (b)  Trachycephalus  ;  (c)  the  obstetric  frog, 
Alytes  obsfetncans  ;  (d)  Hyla  vasta  ;  (e)  the  fire-bellied  toad,  Bombinator  ; 
(f)  Pelohntes  fuf!cus. 


Bomhinator 

in  warning 

attitude 


Fig.  404. 


-The  dilated   (a)  and  contracted  (b)  pupil  of  the  green  tree  frog, 
Hyla  ccpndra. 


340  THE    EYE    IN   EVOLUTION 

myo-epithelial  cells  will  absorb  a  considerable  amount  of  light-energy  ; 
indeed,  contraction  occurs  in  the  excised  eye  (Brown-Sequard,  1859  ; 
Steinach,  1890  ;  Magnus,  1899  ;  Guth,  1901),  the  effect  being  most 
marked  in  the  blue  region  of  the  spectrum  (Weale,  1956,  in  Rana 
temporaria  but  not  in  Xenopus).  Ordinarily,  however,  this  action  is 
masked  by  the  nervous  reflex  action  which  originates  from  retinal 
activity. 

Amphibians  are  the  first  among  Vertebrates  wherein  the  movements  of  the 
pupil  are  mediated  by  a  neural  mechanism,  but  although  their  pupils  are  more 
actively  motile  than  those  of  Fishes,  their  movements  remain  sluggish  for  the 
sphincter  muscle  is  still  comparatively  weak.  Thus  the  oval  pupil  of  the  common 
frog  requires  the  stimulus  of  an  increase  of  light -intensity  of  200  times  to  induce 
a  contraction  to  ^  of  its  size  from  full  dilatation. 

The  le7is  in  the  tadpole,  like  that  of  Fishes,  is  spherical  and 
approximates  the  cornea  ;  in  the  adult  frog  it  moves  posteriorly 
leaving  a  deep  anterior  chamber  and  becoming  somewhat,  flattened  in 
an  antero -posterior  direction  (axial  :  equatorial  diameter,  1:  1-3,  Rabl, 
1898)  (Fig.  398).  The  large  nucleus  is  dense  and  the  periphery  soft 
and  elastic,  the  internal  structure  and  the  epithelium  conforming  to 
the  usual  vertebrate  plan  with  a  vertical  suture  anteriorly  and  a  short 
horizontal  suture  in  the  posterior  part,  as  in  selachian  fishes  (Fig.  314). 

The  blood  supply  to  the  eye  has  several  points  of  interest  and  has 
been  studied  by  H.  Virchow  (1881),  Tretjakoflf  (1906),  Grynfeltt  (1907), 
and  Kutsukaka  (1952).  It  is  derived  from  the  ophthalmic  artery,  a 
branch  of  the  internal  carotid.  From  this  artery  two  posterior  ciliary 
branches  are  given  off  which  enter  the  eye  posteriorly  just  above  the 
disc  and  diverge  to  run  forwards  in  the  choroid  on  its  nasal  and  temporal 
sides  to  supply  the  choriocapillaris.  From  this  layer  blood  is  gathered 
into  the  central  venous  plexus  of  Gaupp,  the  flat  vessels  of  wliich  run 
in  a  general  vertical  direction  in  the  midst  of  the  choroid  ;  these 
converge  to  leave  the  globe — dorsally  as  two  veins  which  imite  to  form 
the  superior  bulbar  vein,  ventrally  as  a  single  vein  which  enters  the 
jugular  vein.  After  giving  off  the  ciliary  branches  the  main  trunk  of 
the  ophthalmic  artery  enters  the  globe  on  its  under  aspect  in  the  region 
of  the  foetal  fissure  and  runs  forward  to  the  ciliary  region  ;  here,  at 
the  mid-ventral  pomt,  it  sends  off  two  branches  which  rim  circum- 
ferentially  round  the  ciliary  body  as  an  arterial  circle.  From  this  the 
superficial  arteries  of  the  iris  emerge  ;  the  corresponding  veins  lie 
more  deeply  and  drain  partly  into  the  venous  plexus  of  the  ciliary 
body  and  thence  to  the  choroidal  veins,  partly  through  the  two 
crescentic  segments  of  the  ciliary  venous  sinus  into  the  subconjunctival 
veins.  After  it  has  given  off  the  ciliary  arterial  circle,  the  ophthalmic 
arter  lirns  backwards  on  itself  as  a  "  hyaloid  artery  "  and  almost 
immc:        ly  divides  into  two  branches,  a  nasal  and  temporal,  wliich 


AMPHIBIANS 


341 


form  an  incomplete  ring  romid  the  circumference  of  the  ora  ;  thence 
branches  run  posteriorly  to  form  a  membrana  vasculosa  retina 
lying  in  the  vitreous  on  the  surface  of  the  retina,  a  form  of  vasculariza- 
tion analogous  to  that  seen  in  many  Fishes  i  (Plate  III  ;  Figs.  405-6) 
(Hyrtl,  1801  :  Cuignet,  1860  :  Hirschberg,  1882).  The  capillaries  of 
this  system  form  a  close  net  at  the  posterior  jDole  but  are  few  in  the  peri- 
phery and  are  associated  Avith  the  veins  rather  than  the  arteries.  They 
are  collected  by  three  large  venous  trunks,  a  ventral,  a  nasal  and  a  tem- 
poral, and  combine  to  form  a  hyaloid  vein  which  eventually  leaves  the 
globe  alongside  the  entering  artery  and  drains  into  the  ophthalmic  vein. 
It  is  interesting  that  the  arteries  of  the  anterior  segment  are  plentifully 


Fig.  405. — Injected  Membrana  Vasculosa  Retinae  of  an  Adult  Frog. 
There  is  a  capillary-free  zone  around  the  artery  (A)  (  X  161)  (I.  C.  Michaelson). 


provided  with  pad-like  valves  (Grynfeltt,  1907)  while  in  the  hyaloid 
vessels  of  the  vascular  membrane  of  the  retina  contractile  cells  are 
unusually  prominent  (Rouget,  1873  ;  Mayer,  1902)  ;  it  is  possible, 
therefore,  that  there  may  be  a  switch-mechanism  from  one  circulation 
to  the  other  as  illumination  and  activity  vary. 

Ophthalmoscopically  the  retina  of  the  frog  appears  as  a  somewhat 
mottled  slatey-grey  background  over  which  the  semi-opacpie  nerve 
fibres  radiate  in  immense  numbers  uniformly  from  the  oj^tic  disc  to 
the  periphery  in  Rana,  for  a  relatively  short  distance  in  Bufo  and 
HyJa  ;  in  these  latter  the  remainder  of  the  fundus  is  covered  with 
orange  or  golden  sago-like  grains.  In  the  Pvanida?  and  Bufonidse  the 
optic  disc  is  long  and  narrow,  resembling  in  its  appearance  a  white 
caterpillar  lying  vertically  ;  in  the  Hylidse  it  is  circular  ;  sometimes  it 
is  covered  by  a  dark  grey  or  even  black  pigment  (the  giant  toad,  Bufo 

1  p.  -im. 


Bufo 


Hyla 


342  THE   EYE   IN   EVOLUTION 

marinus).  The  most  prominent  feature  in  the  fundus  is  the  vessels  of 
the  vascular  membrane.  These  stand  out  clearly,  and  in  the  main 
vessels  the  large  nucleated  erythrocytes  characteristic  of  Amphibians 
can  be  seen  clearly  as  brilliantly-lit  points  racing  along  after  each  other. 
The  arteries  are  thinner  than  the  veins  and  lie  over  them  ;  the  veins 
are  gathered  into  a  large  vena  media  which  stands  out  in  conspicuous 
relief  as  it  courses  vertically  downwards  over  or  near  the  optic  disc  to 
disappear  in  the  ventral  area  of  the  fundus  (Cuignet,  1866  ;  Hirschberg, 
1882  ;   Johnson,  1927)  (Plate  III). 

The  pigment  epithelium  of  the  retina  is  possessed  of  long  processes 
dipping  down  among  the  visual  elements. 

The  visual  retina  is  avascular  and  has  the  usual  vertebrate 
architecture,  the  layers  being  of  average  thickness  (Figs.  406-7).  The 
visual  cells,  however,  are  of  unusual  interest  and  have  received  much 
study  (Figs.  408-9).^  They  are  commonly  of  four  types,  all  of  them  large 
and  coarse  in  structure  :  violet  and  green  rods,  single  cones  and  double 
visual  elements,  while  triple  visual  elements  have  been  described.  The 
violet  (or  red)  rod,  which  contains  rhodopsin,  is  unusually  plump,  the 
outer  segment  unusually  large  and  the  nucleus  in  contact  with  the 
external  limiting  membrane,  a  level  generally  occupied  by  the  nuclei  of 
cones.  The  green  rod  (of  Schwalbe)  is  found  only  in  Amphibians  among 
which,  however,  it  is  widely  distributed  (Denton  and  Pirenne,  1952)  ; 
it  has  a  smaller  outer  segment  lacking  rhodopsin,  a  long  slim  stalk,  and 
its  nucleus  lies  at  a  deeper  level  in  the  inner  part  of  the  outer  nuclear 
layer  ;  in  structure  it  therefore  occupies  an  intermediate  position 
between  a  cone  and  an  ordinary  (red)  rod  (Walls,  1942).  The  single 
cones  resemble  those  of  the  Holosteans  and  Dipnoi,  and  in  diurnal 
types  {Rana)  they  possess  a  yellow  oil-droplet  in  the  upper  part  of  the 
ellipsoid,  a  structure  first  described  by  H.  Miiller  (1861)  and  Babuchin 
(1863-64).  Double  visual  elements  commonly  occur,  usually  said  to 
Rana  \)q  "  double  cones  "  but  perhaps  representing  the  fusion  of  a  rod  and 

cone  (Saxen,  1954-56)  ;  in  these  the  oil -droplets  are  confined  to  the 
main  member  of  the  pair.  Triple  cones,  only  two  members  of  which 
bear  oil-droplets,  have  been  described  by  Saxen  (1953)  in  the  retina 
of  Rana  temporaria,  a  formation  suggesting  that  these  and  the  double 
cones  result  from  a  fusion  of  elements  rather  than  from  a  process  of  cell- 
division.  There  is  a  vague  area  centralis  which  has  probably  more 
resolving  power  than  the  remainder  of  the  retina  (Krause,  1875)  ;    it 

1  H.  Miiller,  1857  ;  Hulke,  1864  ;  Schultze,  1866  ;  Steinlin,  1868  ;  Dobrowolsky, 
1871  ;  Landolt,  1871  ;  Schwalbe,  1874-87  ;  Krause,  1875-92  ;  Hoffmann,  1876-77  ; 
Boll,  1877  ;  Kuhne,  1878  ;  Dogiel,  1888  ;  Cajal,  1893  ;  Greeff,  1899  ;  Gaupp,  1904  ; 
Kolmer,  1904  ;  Hesse,  1904  ;  Garten,  1907  ;  Hess,  1910  ;  Arey,  1916  ;  Majima, 
1925  ;  Noble,  1931  ;  Rozemeyer  and  Stolte,  1930  ;  Police,  1932  ;  Detwiler,  1943  ; 
Khau-van-Kien,  1954  ;  and  many  others.  For  iiltramicroscopic  structure,  see  Sherman, 
1'  "1  :  for  localization  of  mitochondria,  see  Carasso,  1954  ;  for  histochemistry,  see 
V-     locki  and  Sidman,  1954  ;   for  development,  see  Saxen,  1954-56. 


PLATE  III 

The  Eyes  of  Axukans 


Fk;.  1. — The  fundus  ot  the  frog.  Barm  leinpornria. 


Fig.  2. — The  iris  of  the  giant  toad,  Biifo  Niarunis       Fig.    3. — The   iris   of  the   common   frog,    Bana 
(blood  flow  shoA\-n  by  arrows)  (Ida  Mann).  teniporariu  (Ida  Mami). 


Fig.    4. — The    ui.s    ot    ih       .\laiayan    tree-frog.       Fig.    5. — The    iris    ui     Whites    tree-frog,    Hyla 
Bhacophorus  leiicninijstax  (Ida  Mann).  coenilea  (Ida  Mann). 


S.O. — VOL.  I 


[To  face  p.  342. 


A^IPHIBIANS 

Figs.  406  and  407.— The  Anuran  Retina. 


343 


•  ^ 


-*♦ 


-»•      •• 


Fig.  406. — The  retina  of  Rana  temporaria. 

Note  the  vessels  of  the  membrana  vasculosa  retinae  lying  on  the  inner  surface 
of  the  retina  (above)  (  x  320)  (Norman  Ashton). 


-2-  --^^s*^  -  y^W^-'^T^' 


%. 


'"    4 


W^'' 


Fig.    407. — The   retina  of  Xenopiis  hevis   (  X  450)    (Katharine   Tansley). 

(1)  optic  nerve  fibre  layer  ;  (2)  ganglion  cells  ;  (3)  inner  plexiform  layer 
(4)  inner  nuclear  layer  ;  (5)  outer  plexiform  layer  ;  (6)  outer  nuclear  layer 
(7)  visual  cells  ;    (8)  pigmentary  epithelium  ;    (9)  choroid. 


344 


THE   EYE   IN   EVOLUTION 


assumes  varying  shajDes — a  crescent  above  the  optic  disc  in  Rana,  a 
circle  around  it  in  Hyla  and  Bufo,  a  linear  band  in  B.  esculenta,  and  so 
on  (Hulke,  1864  ;   Chievitz,  1891  ;    Slonaker,  1897  ;   von  Hess,  1910). 
The  02)fic  nerve  is  thin  and  cylindrical  with  connective  tissue  septa 


Figs.  408  and  409. — The  Visual  Cells  of  Anurans. 


Fig.  408. — The  dark-adapted  common 
rod  (on  the  left)  and  the  green 
(Schwalbe's)  rod  of  the  leopard  frog, 
Rana  pipiens  (on  the  right) 
(Gordon  Walls). 

e,  ellipsoid  ;  /,  foot-piece  ;  I,  ext. 
limiliiig  membrane  ;  m,  myoid  ;  n, 
nucleus  ;    o,  outer  segment. 


Fig.  401). — .Single,  double  and  triple 
cones  from  the  eye  of  the  tadpole  of 
Rana  temporaria  (aged  26  days). 

There  is  an  achromatic  oil-droplet  in 
the  single  cone,  in  the  chief  member  of 
the  double  cone,  and  not  in  the  acces- 
sory member  of  the  triple  cone.  In  the 
double  cones  the  accessory  member 
has  an  extensive  paraboloid  and  a 
rod-shaped  outer  segment.  In  the 
triple  cone  there  are  3  components, 
2  similar  in  all  respects  to  the  chief 
component  of  the  double  cone,  the 
third  similar  to  the  accessory  element 
of  the  double  cone  (L.  Saxen). 


(Studnicka,  1898),  while  the  chiasnia  shows  a  total  decussation 
frequently  in  the  form  of  large  fascicula?  interdigitating  with  one 
another  (J.  Miiller,  1826  ;  Leuckart,  1876  ;  Gross,  1903). 


The  OCULAR  ADNEXA  are  very  different  from  those  of  Fishes,  for 
in  the  f;;  ln.lt  a  complicated  protective  and  lubricating  system  is  necessary 
to  proi     '  an  eye  exposed  to  air  ;   lids  are  thus  absent  in  the  larvae  of 


AMPHIBIANS  345 

Amf)liibians,  all  of  which  are  aquatic,  and  in  those  adult  frogs  which 
do  not  leave  tlie  water.  In  the  majority,  however,  which  live  their  adult 
life  on  land,  a  short  njaper  and  lo\A'er  lid  develop  during  metamorphosis 
(Maggiore,  1912)  ;  the  upper  lid  is  immobile,  but  associated  with  the 
lower  an  elastic  translucent  fold  forms  n  false  nictitating  meinbrane,  the 
free  border  of  which  is  usually  spotted  with  a  brilliant  bronze  pigment 
(green  in  some  Hylidae,  as  Hyla  coerulea).  Normally  the  lid  lies  as  a 
Z-shaped  fold  in  the  loAver  fornix  and  its  thickened  upper  border  is 
continued  as  a  cord  which  runs  around  the  posterior  part  of  the  eyeball 
slinging  itself  around  the  retractor  bulbi  muscle  (Fig.  410)  :  when  this 
muscle  contracts  the  eye  is  pulled  into  the  orbit  and  the  tug  on  the 
cord  draws  the  membrane  upwards  over  the  cornea  completely  covering 
it.  The  membrane  is  thus  entirely  passive  in  its  action  and.  forming 
part  of  the  lower  lid  itself,  differs  funda- 
mentally from  the  pseudo-nictitating  mem- 
brane seen  in  some  Teleosteans  and  also  from 
the  true  nictitating  membrane  of  the  higher 
Vertebrates.  Lubrication  is  effected  by  a 
development  of  glands  in  the  margin  of  the 
upper  lid  ;  those  on  the  nasal  side  hyper- 
trophy to  form  the  massive  harderian  gland  ^ 

,  7    ,'  .  -Ill  -1  'tUi.    410. ]MrSCUL.\TUKE    OF 

which  occupies  a  considerable  sjjace  m  the        the    Nictitating    MEM- 
nasal  half  of  the  orbit,  while  those  on  the        ^^-^^e  of  the  Frog. 
temporal  side  become  the  precursor  of  the        R-'etmctor  bulbi  muscle  ; 

^  ^  \,      tendon      oi      nictitatuig 

lacrimal   gland  ;     two   puncta   aj^pear   on   the      membrane    on    the    temporal 

free  border  of  the  lo\\er  lid,  the  canaliculi     side  of  the  posterior  aspect 

OI  the  globe  (after  Pranz). 

uniting    into   a  subcutaneous    naso-laerimal 

duct  running  horizontally  into  the  middle  fossa  of  the  nose. 

Ocular  movements,  apart  from  retraction,  are  negligible.  The 
usual  0  extra-ocular  muscles,  however,  are  present  with,  in  adchtion.  a 
jDowerful  EETRACTOR  BULBI  MT7SCLE  innervated  by  the  Vltli  nerve  and 
probably  derived  from  the  external  rectus,  and  a  second  muscle  behind 
the  eye,  the  levator  bulbi,  derived  from  the  jaw-musculature  and 
supplied  by  the  Vth  nerve.  If  the  eye  is  touched,  retraction  of  the 
globe  is  effected  by  the  retractor  muscle  which  at  the  same  time  pulls 
the  nictitating  membrane  over  the  cornea  ;  thereafter  the  levator 
bulbi  pulls  the  globe  forAvard  again  and  the  membrane  of  the  lower  lid 
falls  back  into  its  normal  folded  j^osition.  This  movement  of  retraction, 
however,  is  possibly  as  useful  as  an  aid  to  swallowing  food  as  a  protec- 
tive device  :  the  partition  between  the  orbit  and  the  mouth  is  merely 
a  thin  membranous  sheet  and  when  the  eyeball  is  jiulled  into  the  head 

^  In  most  Vertebrates  the  lids  are  lubricated  by  a  row  of  compound  glands  which 
are  frequently  best  developed  temporally  and  nasally  ;  those  on  the  temporal  side 
develop  into  the  l.^crimal  glands  .secreting  tears,  tliose  on  the  nasal  side  into  the 
GLAND  OF  HARDER  {Actci  eruditorum  pub.,  Lij^siae,  1694)  with  a  sebaceous  oily  secretion. 


346 


THE   EYE   IN  EVOLUTION 


Amby  stoma 


it  bulges  downwards  into  the  roof  of  the  month,  thus  forcing  food  down 
the  throat. 

The  anuran  orbit  is  large  and  membranous  with  considerable  gaps 
in  its  walls  and  without  an  interorbital  septum  or  any  division  between 
the  two  cavities.  As  we  have  seen,  the  orbital  cavity  opens  directly 
into  the  pharynx. 

THE    URODELAN    EYE 

MANY  OF  THE  TAILED  AMPHIBIANS,  witli  their  cavcrnicolous  and 
secretive  habits,  have  reduced  or  degenerate  eyes  ^  ;  even  those  types 
which  are  visually  active,  such  as  the  salamanders  and  newts  {Sala- 
niandra,  Triturus)  and  Axolotl  (the  larva  of  the  salamander,  Amhy- 
stonia  tigrinum),  have  eyes  which  are  smaller  and  simpler  than  those  of 
Anurans  although  designed  on  the  general  amphibian  plan  (see  Okajima, 
1909  ;     Rochon-Duvigneaud,    1943).      The    main   differences    are   the 


Fig.  411. — The  Head  of  the  Newt,   Triturus. 


Fig.  412. — The  Axolotl,  larva  of  Ambystoma   tigrjxum  (Zool.  Soc, 

London). 

1  p.  726. 


PLATE  IV 

The  Eyes  of  Urodeles 


Fig.  1. — The  iris  of  the  Californian  newt,  Triturus  torosus  (Ida  Mann). 


Fiu.  '1. — Tlie  I'uiulus  oi  tinlamandra  maculosa 
(Lindsay  Johnson). 


To  fun-  p.  :J47 


S.O. — VOI,    I 


AMPHIBIANS 


347 


fibrous  sclera  without  cartilage  (except  for  anterior  cartilaginous  plaques 
in  Triton,  and  the  small  fragmented  cartilage  in  Hynohius — Stadtmiiller, 
1914-29  ;  Tsusaki,  1925  ;  Inagaki,  1930  ;  Yatabe,  1931),  the  com- 
paratively large  size  of  the  lens  as  would  be  expected  in  creatures 
favouring  dimly-lit  surroundings,  the  comparatively  shallow  anterior 
chamber,  the  thicker  and  less  highly  organized  choroid  separated  from 
the  sclera  by  large  serous  spaces,  the  lack  of  ciliary  folds  on  the  inner 
surface  of  the  ciliary  body  and  iris  with  the  exception  of  a  single  mid- 
ventral  ciliary  process,  the  lack  of  a  dorsal  protractor  lentis  muscle  in 
the  place  of  which  the  suspensory  ligament  is  strengthened  locally  as  in 
Fishes,  the  lack  of  pupillary  nodules,  of  the  primitive  and  discontinuous 
ciliary  venous  sinuses,  and  of  an  area  centralis  in  the  retina.  Accom- 
modation is  thus  effected  through  a  ventral  protractor  lentis  muscle  after 
the  manner  seen  in  selachian  fishes,  by  a  forward  pendular  movement 
of  the  lens  rather  than  its  forward  displacement  as  a  whole  (Beer,  1898). 

The  vascular  supply  to  the  anterior  segment  is  similar  in  its  general 
plan  to  that  of  the  Anurans,  but  curiously  the  vascular  arrangements 
in  the  iris  partake  of  a  more  definite  pattern  (Plate  IV)  ;  as  in  the  frog, 
the  arteries  are  superficial  but  instead  of  entering  at  various  apparently 
haphazard  positions  around  the  circumference  as  in  this  animal,  they 
are  represented  in  the  salamander  by  two  trunks,  an  inferior  and  a 
temporal  artery  of  the  iris,  an  arrangement  anticipating  that  seen 
typically  in  Reptiles  such  as  the  lizard  (Plate  V)  (Mann,  1929). 
Sometimes  the  inferior  artery  of  the  iris  is  a  branch  of  the  temporal 
and  does  not  enter  separately.  The  arteries  break  up  irregularly  round 
the  pupil  and  the  blood  is  drained  away  by  a  few  radial  veins  lying 
in  a  deeper  plane  so  that  they  are  often  obscured  by  pigment.  In 
newts  {Triturus,  Pleurodeles)  the  artery  breaks  up  into  some  6  branches 
which  encircle  the  pupil  and  drain  aA\'ay  on  the  nasal  side  (Mann,  1931). 

In  tailed  Amphibians  the  pupil  is  usuall}^  round  and  the  iris  may 
be  brilliantly  pigmented — dark  brown  with  faint  metallic  flecks  in  the 
spotted  salamander  {Salamandra  maculosa),  horizontal  green  and  brown 
banding  in  the  Californian  newt  {Triturus  torosus),  sage-green  with 
peripheral  horizontal  bands  of  metallic  gold  in  the  Japanese  newt 
{Trititriis  2)l/rrhogaster),  and  so  on  (Mami.  1931)  (Plate  IV,  Fig.  1). 

The  fundus  in  salamanders  is  uniformly  the  same  throughout,  of 
a  pinkish  hue  with  a  granular  texture  in  the  middle  of  which  the 
circular  grey  optic  disc  is  set  (Plate  IV,  Fig.  2).  The  retina  is 
avascular  and  there  is  no  membrana  vasculosa  retinae  as  in  Anurans 
(Virchow,  1881)  {Salamandra,  H\Ttl,  1861  ;    Triton,  Kessler,  1877). 

The  visual  elements  tend  to  be  sparser  and  larger  than  in  the  frog, 
but  are  generally  of  the  same  morphological  types  except  for  the 
absence  of  oil-droplets  in  the  cones  (Fig,  413-5),  and  the  occasional 
lack  of  green  rods  (in  Salamandra). 


Trit 


urus  cristatus 
(male) 


Trit 


urus  cristatus 
(female) 


348 


THE   EYE   IN   EVOLUTION 


^**^ieoM<i:^«3*5MM^ii^^ 


Fio.  413. — The  Retina  of  the  Newt,    Triturus. 
1,    optic    nerve    fibres  ;     2,    ganglion    cells  ;     3,    inner    plexiform    layer  ; 
4,   inner  nuclear   layer  ;     5,   outer   plexiform   layer  ;     6,   outer   nuclear   layer, 
consisting    of    large    elongated    nuclei  ;      7,    external    limiting    membrane  ; 
8,  visual  cells  ;    9,  pigment  (  X  253)  (Katharine  Tansley). 


Fig.  414. — A  Double  Cone  in 
THE  Xewt  (Azan  ;  X  792) 
(Katharine  Tansley). 


Fig.     41.'). — The     Visu.4.l     Cells     of     the 
AXOLOTL,  Ambystoma  tigbinvm. 

A  single  cone,  a  double  cone  (compare 
Fig.  414).  a  common  rod  and  a  green 
(Schwalbe's)  rod   (  x  1,000)   (Gordon  Walls). 


AMPHIBIANS 


349 


Movable  eyelids  are  found  only  in  tlie  Urodeles  which  have 
adopted  terrestrial  life  ;  in  aquatic  forms  the  lids  have  receded  to 
immovable  ridges  or  low  folds,  while  in  subterranean  species  the  eyes 
are  completely  covered  by  the  skin.^  It  is  interesting  that  in  terrestrial 
salamanders  the  lacrimal  glands  are  distributed  along  the  lower  lids 
(Piersol,  1887  ;   Maggiore,  1912  ;    Engelhardt,  1924). 

The  limicoline  types  f)f  the  Urodela  which  hve  in  mud,  such  as  tlie  North 
American  genera,  Cryptobranchus,  Amphluma,  Necturus  and  Siren,  have  relatively 


Mega  lohatrach  ?<.s 


Amphiuma 


■J      0. 


cv 


rl' 


u^' 


Fig.  416. — The  Eye  of  MEdALOBAiRAcuua  maximum. 

A  section  of  the  ill-formed  eye  of  this  Urodele.  C,  cornea  ;  Ch,  choroid  ; 
CO,  optic  canal  ;  H,  skin  ;  K,  the  enormously  lai'ge  scleral  cartilage  with 
its  dense  core,  P;  O,  o[iti('  nerve  ;  R,  retina  ;  S.  fihrous  tissue  of  sclera 
{after  Lauber). 


crude  and  ill-developed  eyes  which  seem  incapable  of  elaborate  optical  imagery. 
In  the  related  Japanese  giant  salamander,  ]\Iegalobatrachns  maximus,  found  also 
in  China  and  Tibet — incidentally  the  largest  extant  Ami:)hibian,  5  feet  in  length 
— the  monstrously  hypertrophied  scleral  cartilage  occupies  more  space  than  the 
remainder  of  the  eye  ;  indeed,  this  cartilage  is  the  most  massive  seen  among  the 
Vertebrates  and  occupies  two-thirds  of  the  section  of  the  globe  (Lauber,  1902  ; 
Reese.  1905  ;  Yano,  1926-28  ;  Aoyama,  1928  ;  Stadtmilller,  1929)  (Fig.  416). 
In  this  salamander  also,  as  in  some  other  Japanese  types,  the  cornea  is  vascu- 
larized (Tawara,   1933:  Kurose,   1956).  The  visual  elements  are  similarly  sparse 


Necturus 


1-2G. 


350 


THE   EYE   IN  EVOLUTION 


and  crude.  The  violet  rods  of  the  mvid-puppy,  Necturus,  for  example,  are  enor- 
mous, two  and  a  half  times  the  thickness  of  the  corresponding  structures  in  the 
frog  and  the  largest  known  in  the  vertebrate  phyhim.  The  optic  nerve  fibres  are 
relatively  few,  one  ganglion  cell  subserving  more  visual  elements  than  in  the  frog 
(Burkhardt,  1931).  Thus  there  are,  according  to  Palmer's  (1912)  heroic  counting, 
only  962  nerve  fibres  subserving  the  53,000  rods,  42,000  single  cones  and  15,000 
double  cones  in  the  retina. 


Angelucci.    Arch.  Anat.  Physiol.,  5-6,  363 

(1878). 
Aoyama.    Folia  Anat.  jap.,  Tokyo,  6,  829 

(1928). 
Arey.      J.    co7np.    Neurol.,    26,    121,    429 

(1916). 
Babixchin.     Wiirzburg.  naturwiss.  Z.,  4,  71 

(1863)  ;   5,  141  (1864). 
Beer.      Pflugers  Arch.    ges.    Physiol.,   73, 

501  (1898). 
Boll.     Arch.  Anat.  Physiol.,  4  (1877). 
Boulenger.      The    Tailless   Batrachians  of 

Europe,  London  (1896). 
Brown-Sequard.     J.   Physiol.   Path,   gen., 

2,    281  (1859). 
Burkhardt.      Z.   vergl.    Physiol.,    15,    637 

(1931). 
Cajal.     La  cellule,  9,  1  (1893). 
Carasso.    C.  R.  Acad.  Sci.  (Paris),  238,  617 

(1954). 
Caso.     Lettura  Oftal.,  8,  339  (1931). 
Chievitz.      Arch.    Anat.    Physiol.,    Anat. 

Abt.,  139,  332  (1889)  ;    311  (1891). 
Cuignet.      Ann.   Oculist.    (Paris),   55,    128 

(1866). 
Denton   and   Pirenne.     J.    Physiol.,   116, 

33P  (1952). 
Detwiler.     Vertebrate  Photoreceptors,  N.  Y. 

(1943). 
Dobrowolsky.    Arch.   Anat.   Physiol.,   320 

(1871). 
Dogiel.    Anat.  Anz..  3,  342  (1888). 
Engelhardt.    Jena.  Z.  Naturwiss.,  60,  241 

(1924). 
Englemann.     Pfliigers  Arch.  ges.  Physiol., 

35,  498  (1885). 
Froriep.    Hertwig's    Hb.    d.    vergl.    exper. 

Entwicklungslehre  d.  WirbeUiere,  Jena, 

2  (2)  (1906). 
Garten.        Graefe-Saemisch    Hb.     d.     ges. 

Augenheilk.,  II,  3,  Kap.   12,  Anhang 

(1907). 
Gaupp.  Eckers  and  Wiederscheimer's  Atiat. 

des  Frosches,Z  (1904). 
Greeff.         Oraefe-Saemisch     Hb.     d.     ges. 

Augenheilk.,    II,    1    (2),    Kap.    5,    74 

(1899). 
Gross.      Zool.   Jb.,    Abt.    Anat.,    17,    763 

(1903). 
GrynfeUt.    Bib.    Anat.    (Paris),    15,    177 

(1906). 
C.  R.  Assoc.  Anat.,  Lille  (1907). 
Guth.        ' 'Ggers  Arch.   ges.   Physiol.,   85, 

lu:       h). 

v.    Hess.  rch.   vergl.    Ophthal.,    1,    153 

(1910  . 


Vergl.    Physiol,   d.   Gesichlssinnes,   Jena 

(1912). 
Hesse.     Zool.  Jb.,  Abt.  Syst.,  Suppl.  7,  471 

(1904). 
Hirschberg.       Arch.    Anat.     Physiol.,    81 

(1882). 
Hoffmann.      Niederl.    Arch.    Zool.,    3,    45 

(1876-77). 
Hulke.     Roy.  Land,  ophthal.  Hosp.   Rep., 

4,  243  (1864). 
Hyrtl.    ;S'.  B.  Akad.  Wiss.  Wien.,  43  (1861). 
Inagaki.    Keijo  J.  Med.,  1,  49  (1930). 
Johnson.       Philos.    Trans.    B,    215,    315 

(1927). 
Jokl.    Anat.  Anz.,  51,  209  (1918). 

Anat.  Hefte,  59,  211  (1920). 
Kessler.       Entwicklung     des     Auges     der 

Wirbelthiere,  Leipzig  (1877). 
Khau-van-Kien.     C.  R.  Assoc.  Anat.,  82, 

907  (1954). 
Kolmer.    Anat.  Anz.,  25,  102  (1904). 
Krause,  W.    v.  Graefes  Arch.  Ophthal.,  21 

(1),  296  (1875). 
Internat.  Mschr.  Anat.,  9,  150  (1892). 
Kiihne.     Untersuch.  a.  d.  physiol.  Inst.  d. 

Univ.  Heidel.,  1,  15,  455  (1878). 
Kurose.     Acta  Soc.  ophthal.  jap.,  60,  621 

(1956). 
Kutsukaka.     Acta  Soc.  ophthal.  jap.,  56, 

988  (1952). 
Landolt.     Arch.  mikr.  Anat.,  7.  81  (1871). 
Lauber.     Anat.  Hefte,  20,  1  (1902). 
Leuckart.      Graefe-Saemisch    Hb.    d.    ges. 

Augenheilk.,  1,  2,  145  (1876). 
Maggiore.      Ricerche  morfol.   sulV apparato 

palpebrcde  degli  Anfibi,  Roma  (1912). 
Magnus.     Z.  Biol.,  20,  567  (1899). 
Majima.     v.  Graefes  Arch.    Ophthal.,  115, 

286  (1925). 
Mann.     Trans,  ophthal.  Soc.  U.K.,  49,  353 

(1929). 
Proc.  Zool.  Soc.  Lond.,  21,  355  (1931). 
Mayer.    ^na<.  ^nz.,  21,  442  (1902). 
Millot.       Le    pigment    purique     chez     les 

vertebres  inferieurs,  Paris  (1923). 
Miiller,  H.     Z.  wiss.  Zool.,  8,  1  (1857). 

Wurzburg.  naturwiss.  Z.,  2,  139  (1861). 
Miiller,    J.       Vergl.    Physiol,    d.    Gesichts- 

sinnes,  Leipzig  (1826). 
Noble.     The  Biology  of  the  Amphibia,  N.  Y. 

(1931). 
Okajima.     Z.  wiss.  Zool.,  94,  171  (1909). 
Palmer.    J.  comp.  Neurol.,  22,  405  (1912). 
Petit.      Mem.   Acad.   Sci.,   A,   Paris,    142 

(1737). 


AMPHIBIANS 


351 


Piersol.    Arch,  jnikr.  Ayuit..  29,  594  (1887). 
Police.    Arch.  Zool.  Ital.,  17,  449  (1932). 
Rabl.     Z.  wiss.  ZooL,  63,  496  (1898). 
Reese.     Biol.  Bull.,  9,  22  {1905). 
Roehon-Duvigneaud.       Les     yeux     et     la 

vision  des  vertebres,  Paris  (1943). 
Rouget.       Arch.     Phtjsiol.      (Paris),     603 

(1873). 
Rozemever  and   Stolte.      Z.   mikr.   Anctt. 

Forsch.,  23,  98  (1930). 
Saxen.    Acta  Anat.  (Basel),  19,  190  (19.53). 
Ajin.  Acad.  Sci.fenn.,  Series  A,  iv  (Biol.), 

23,  1  (19.54). 
J.  Embryol.  e.rp.  Morphol.,  4,  57  (1956). 
Schultze.       Arch.    mikr.     Anat.,    2,     175 

(1866)  ;    3,  215  (1867). 
Schwalbe.      Graefe-Saemi.?ch    Hb.    d.    ges. 

Augenheilk.,  I,  1,  354  (1874). 
Lehrb.  d.  Anat.  d.  Sinnesorgane,  Erlangen 

(1887). 
Sherman.    Anat.  Rec,  109,  383  (1951). 
Slonaker.    J.  Morphol.,  13,  445  (1897). 
Soemmerring,  D.  W.    De  oculorum  hominis 

animcdiumque  etc.,  Goettingen,  p.  57 

a818). 
Stadtmuller.     Anat.  Hefte,  51,  427  (1914). 
Morphol.  Jb.,  61,  221  (1929). 


Steinaoh.     Pfli'igers  Arch.  ges.  Physiol.,  47, 

289  (1890). 
Steinlin.     Arch.  mikr.  Anat.,  4,  10  (1868). 
Studnicka.. Jena. Z.Naturu-iss..^l,  1  (1898). 
Tavvara.      Nagasaki   Igak.    Zeis.,    11,    350 

(1933). 
Teulieres  and  Beauvieux.     Arch.   Ophtal. 

(Paris),  48,  465  (1931). 
Tretjakoff.     Z.  iviss.  Zool.,  80,  327  (1906). 

Anat.  Am.,  28,  25  (1906). 
Tsusaki.     Folia  Anat.  jap.,  Tokyo,  3,  345 

(1925). 
Virchow,  H.    Z.  wiss.  Zool.,  35,  247  (1881). 
Phifsiol.  Med.  Ges.,  Wurzburg,  16,  108 

(1881). 
Walls.        llie     Vertebrate    Eye,    Michigan 

(1942). 
Weale.    J.  Physiol.,  132,  257  (1956). 
Wislocki  and  Sidman.     J.  comp.  Neurol., 

101,  53  (1954). 
J.  Histochem.  Cytochem.,  2,  413  (1954). 
Yamasaki.     Yokohama  Med.  Bull.,  3,  266 

(1952). 
Yano.      Folia    Anat.  jap.,    Tokyo,    4.    57 

(1926)  ;   6,  103  (1928). 
Yatabe.     Keijo  J.  Med..  2,  1  (1931). 


352 


THE   EYE   IN   EVOLUTION 


Fig.  417.— Gordon  L.  Walls  (1905 ). 


CHAPTER  XIII 
THE  EYES  OF  REPTILES 

The  portrait  of  Gordon  l.  walls  (1905 )  (Fig.  417)  could  suitably  serve 

as  an  introduction  to  many  chaj^ters  in  this  book  for  he  has  done  much  to  corre- 
late and  rationalize  our  ideas  on  the  structvire  and  function  of  the  eyes  of 
Vertebrates.  Originally  trained  as  an  engineer,  he  branched  into  zoology  at 
Harvard  University  ;  here,  expecting  to  work  on  Rotifers,  he  was  arbitrarily 
assigned  a  problem  on  the  retina  for  investigation  and  for  many  years  devoted 
all  his  energies  to  the  study  of  the  finer  structure  and  function  of  this  tissue 
throughout  the  vertebrate  phylum.  His  most  striking  contribution  in  this  field 
was  his  enthusiastic  advocacy  of  the  theory  that  the  cones  were  more  primitive 
than  the  rods  and  that  in  the  evolutionary  process  the  cones  of  an  ancestral 
species  transmuted  into  rods  in  a  descendant  species.  It  was  in  the  eyes  of 
Reptiles,  particularly  snakes,  that  he  found  the  most  satisfying  evidence  for 
his  views,  and  his  observations  led  him  to  formulate  new  ideas  about  the  evolu- 
tionary history  of  groups  such  as  these.  His  work  in  this  field  was  summarized 
in  his  classical  book.  The  Vertebrate  Eye  and  its  Adaptive  Radiation,  published 
in  1942,  which  is  undoubtedly  the  most  comprehensive  and  readable  vokime 
on  this  subject  in  the  English  literature  ;  to  it  I  have  been  greatly  indebted  in 
the  writing  of  this  volume.  This  task  completed,  he  forsook  comparative 
ophthalmology  and,  as  Professor  of  Physiological  Optics  at  the  University  of 
California,  he  devoted  his  attention  to  the  still  more  complex  problems  of  colovu" 
vision  and  colour  blindness,  a  subject  wherein  his  contributions  will  be  noted 
in  a  subsequent  volume  of  this  series. 

Of  the  five  main  groups  of  extant  Reptiles,  the  chelonl\ns  (turtles, 
tortoises)  are  the  most  archaic  and  primitive  ;  the  rhynchocephalians  (the 
sole  extant  representative  of  which  is  Sphenodon)  have  relatively  simple  eyes 
largely  adapted  for  noctumality  ;  the  crocodilians  (crocodiles,  alligators) 
again  have  relatively  simple  eyes  largely  adapted  for  vision  under  water  ;  the 
LACERTLLiANS  (lizards),  active  and  (with  many  exceptions)  typically  diurnal 
creatures,  have  the  most  elaborately  formed  eyes  among  the  entire  class  and  the 
most  typically  reptilian  in  their  characteristics;  while  ophidians  (snakes)  have 
eyes  peculiar  to  themselves  and  in  most  of  their  essential  features  widely  different 
from  all  other  members  of  the  group,  bearing  little  resemblance  to  the  eyes  of 
their  immediate  ancestors,  the  lizards. 

We  shall  therefore  describe  the  eyes  of  lizards  in  some  detail  as  the  essential 
reptilian  type,  enumerate  shortly  the  main  simi^lifieations  seen  in  the  first  three 
groups,  and  finally  discuss  the  unique  eyes  of  snakes. 

THE  EYES  OF  BEPTILES  are  tlie  first  to  be  finally  and  completely 
adapted  to  terrestrial  life.  We  have  already  seen  that  those  of  the 
Ichthyopsida  have  many  features  in  common  and  that  although 
Amphibians,  leaving  the  water  after  the  larval  stage,  have  acquired 
many  adaptations  for  vision  on  dry  land,  their  eyes  still  exhibit  a 

S.O.— VOL.  I.  3.>3  -ii 


354  THE   EYE   IN   EVOLUTION 

general  plan  broadly  comparable  with  that  of  the  eyes  of  Fishes.  In 
the  eyes  of  Sauropsida,  however,  a  revolution  has  occurred.  Even 
among  the  most  primitive  Reptiles  adaptations  of  a  different  character 
and  a  much  higher  order  are  found,  most  of  them  having  little  apparent 
evolutionary  relationship  with  the  characteristics  of  the  visual  organs 
of  surviving  Amphibians,  and  these  become  perfected  in  their  descen- 
dants, the  Birds.  The  entire  sauropsidan  family  will  be  found  to  have 
much  in  common,  having  evolved  a  type  of  eye  very  different  from 
their  ancestors  and  as  different  from  the  mammalian  eye  which  has 
developed  on  entirely  separate  lines. 

Fig.  418. — The  Eyes  of  Reptiles. 


The  lizard, 
Lacerta  mo?iitor. 


The  tortoise, 
Testudo  tnydas. 


The  crocodile, 
Crocodilus  sclerops. 


Reproductions  of  Soemmerring's  engravings   (1818).     The  reproductions 
are  life  size  and  represent  the  lower  half  of  a  horizontal  section  of  the  left  eye. 


The  essential  features  of  the  typical  reptilian  eye  are  tlie  fol- 
lowing (Fig.  418)  : 

An  effective,  accommodative  mechanism  de^yending  on  deformation  of 
the  lens — not  its  to-and-fro  movement  as  m  Ichthyojisida.  This  is 
effected  by  a  striated  ciliary  ynuscle  arising  in  the  cornea  and  deriviyig 
firm  leverage  from  a  ring  of  scleral  ossicles — a  descendayit  of  the  tensor 
choroidece  of  Fishes.  To  this  is  added  a  ventral  transversalis  muscle 
emerging  from  the  regioji  of  the  {closed)  foetal  fissure,  the  function  of  ivhich 
is  to  swing  the  lens  yiasally  and  attain  the  convergence  necessary  for 
hinocidar  vision — homologous  7vith  the  j^rotractor  lentis  of  Apiphihians. 
The  lens  is  necessarily  soft  and  the  subcajjsular  epithelial  cells  in  the 
equatorial  region  have  elongated  enormously  in  a  radial  direction  to  form 
an  anmdar  2)ad  to  ivhich  are  fused  the  ciliary  jifocesses,  notv  tall  ayid 
well-formed  in  contrast  to  the  small  ciliary  folds  hitherto  found. 

A  striated  iris  musculature  giving  the  iris  considerable  mobility. 

An  avascular  retina  nourished  indirectly  by  the  choroid  and,  in 
addition,  through  the  conus  pajnllaris  {in  lizards),  or  through  a  inembrana 
vasculv'-a  retince  {in  snakes). 

A   ■■:'tern  of  iris  vascularization  co7isisting  of  deep  circumferential 


REPTILES 


355 


arteries  and  suj)erficiaJ  radial  veins  in  jylace  of  the  reverse  arrangement  in 
IcJithyojJsida. 

An  esseniiaUy  simjAe  retina  tvith  a  cone  2^opidation  in  diurnal 
species  and  a  rod  jioiJidation  in  those  with  nocturnal  habits  ;  each  type 
of  cell  may  be  single  or  donble  and  each  may  contain  an  oil-drop)let. 


THE    LACERTILIAN    EYE 

there    are    some    20    families    extant, i    essentially 


Of     LIZARDS 

inhabitants  of  the  warmer  regions  of  the  earth  ;  they  are  active,  agile 
animals,  with  an  exoskeleton  of  scales  often  beautifully  coloured, 
feeding  usually  on  insects,  worms  and  other  small  animals,  although 


Fig.     419. — The     Head     of     the     Lizard,     Lacerta     muralis     (X  3-5) 
(Katharine  Tanslev).  • 


Fig.   420. — The  Chameleon  (photograph  by  Michael  Soley) 


1  Including  the  true  lizards  of  the  Old  Vv'orld  deserts,  the  skinks,  the  geckos,  the 
monitors  (or  dragons),  iguanas,  agamid  lizards,  Gila  monsters,  glass  snakes,  limbless 
slow-worms  and  the  chameleon. 


356 


THE   EYE   IN   EVOLUTION 


Ch  la  m  yclosa  w  ru  s 


some  (Iguanids)  are  vegetarian  ;  they  are  mostly  terrestrial,  some 
arboreal,  a  few  amphibious  (the  iguanid,  A7nblyrhynchus  cristatus  of  the 
Galapagos  Islands).  Only  exceptionally  in  sluggish  limbless  types  are 
the  eyes  poorly  developed — the  Anguida^  (slow-worms)  and  the 
degenerate  Amphisbeenidse  of  subterranean  habits. 

The  EYEBALL  is  almost  spherical  although  the  an tero -posterior 
axis  is  the  shortest,  but  there  is  a  marked  concavity,  the  corneo-scleral 
sulcus,  in  the  region  of  the  junction  of  these  two  tissues  (Fig.  421).  The 
sclera  is  relatively  thin  and  is  supported  over  most  of  its  extent  by  a 
scleral  cartilage  which,  starting  from  the  posterior  pole,  usually  reaches 
to  the  equator  or  beyond  (Fig.  422)  ;  occasionally,  as  in  the  chameleon, 


Fig.  421. — Diagram  of  the  Eye  of  a  Lizard. 

A,  annular  pad  ;  C,  conus  ;  Ch,  choroid  ;  CM,  ciliary  muscle  ;  F,  fovea 
P,  pectinate  ligament  ;  S,  scleral  cartilage  ;  8c,  sclera  ;  SM,  sphincter  muscle 
SO,  sclei'al  ossicles  ;    VS,  ciliary  venous  sinus  ;    Z,  zonule. 


Gecko 


it  is  confined  to  a  small  disc  in  the  foveal  region.  Anteriorly,  and  lying 
superficial  to  the  cartilage  when  it  is  prolonged  forwards,  is  a  ring  of 
some  14  scleral  ossicles  distributed  around  the  deep  corneo-scleral 
sulcus  sometimes  imbricated  in  2  or  3  layers  ;  these,  noted  by  such 
early  writers  as  Zinn  (1754)  and  Soemmerring  (1818),  support  and 
maintain  the  convexity  of  the  globe  in  this  region  thus  approximating 
the  ciliary  body  to  the  lens.  The  cornea  is  circular  and  thin  and  has  the 
usual  layering  characteristic  of  Vertebrates  apart  from  the  absence  of 
Descemet's  membrane  and  its  endothelium  in  some  geckos  ;  its  inner 
third  merges  with  the  pectinate  ligament  and  gives  rise  to  the  ciliary 
muscle. 

The  uvea  in  general  is  thin.  The  choroid  forms  a  tenuous  layer 
without  distinctive  characteristics.  The  ciliary  body  varies  in  shape — 
narrow  and  angular  in  the  geckos,  broad  and  romided  in  the  chameleon 
— and  has  no  ciliary  processes  but  abuts  directly  on  the  annular  pad 


REPTILES 


357 


It, 


fi!i»VN[*»l'--»'?^^« 


of  the  lens  (Figs.  423-4).  The  musculature  is  complicated  and  is 
divided  into  3  sj^stems.  The  ciliary  muscle  (of  Briicke)  is  well  developed, 
the  fibres  running  meridionally  from  their  origin  from  the  inner  layers  of 
the  cornea,  not  to  the  choroid  as  does  the  tensor  choroidese  of  Fishes 
and  Ampliibians  (or  the  ciliary  muscle  of  Mammals),  but  to  the 
orbiculus  ciliaris.  where  its  anchorage  is  continued  by  a  tenacular 
LIGAMENT  running  from  the  orbiculus  into  the  sclera.  These  fibres  are 
particularly  marked  anteriorl}^  those 
arising  from  the  cornea  being  to  some 
extent  isolated  to  form  the  iniuscle 
OF  CRAiNiPTON,  a  muscular  bundle 
more  fully  developed  in  Birds. ^  The 
meridional  ciliary  fibres  are  some- 
times augmented  by  circumferential 
fibres  arising  dorsally  and  extend- 
ing round  in  the  temporal  half  of 
the  globe  ;  and  m  most  species  by 
an  inferior  transverse  muscle.  This 
muscle  arises  ventrally  from  the  con- 
nective tissue  between  the  ciliary 
body  and  the  sclera  and  passes 
tlu'ough  an  open  portion  of  the  foetal 
cleft  to  be  inserted  into  the  zonular 
fibres  and  thus  indirectly  to  the  lens. 
It  would  seem  analogous  to  the  pro- 
tractor lent  is  muscle  of  Ampliibians 
and  probably  moves  the  lens  nasally 
during  accommodation,  presumabh^ 
to  increase  convergence  {Seps, 
Lacerta — Leplat ,  1921). 

The  iris  is  relatively  thin  at  the 
periphery,  but  thick  toAvards  the 
pupillary  margm  w^here  it  forms  a  well-marked  ramp.  The  two 
posterior  ectodermal  layers  are  deeply  f)igmented  and  from  the  anterior 
are  derived  the  striated  fibres  of  the  jDupillary  musculature.  The 
circumferential  spMncter  fibres  are  well  developed.  The  dilatator 
fibres  form  a  thin  layer  next  the  ej)itheliuni,  their  ordinarily  radial 
direction  assummg  complex  configurations  in  those  species  wherein  the 
pupil  is  slit-shaj^ed.  The  mesodermal  portion  of  the  iris  is  usually 
highly  coloured  as  if  in  an  attempt  to  make  the  eye  consi^icuous,  some- 
times with  red,  yellow  and  melanin  jDigments,  sometimes,  as  in  the 
chameleon,  having  a  brilhant  metallic  sheen  owing  to  a  layer  of  guanine- 


Fig.  422. — The  Posterior  Segment  of 
THE  Eye  of  the  Lizaed. 

Showing  the  retma,  r,  with  its  pig- 
mentary epitheHum,  p,  choi'oid,  ch, 
scleral  cartilage,  s,  and  the  fibrous  sclera, 
sc  (  X  320)  (Norman  Ashton). 


1  p.  405. 


358 


THE   EYE   IN   EVOLUTION 

Figs.  423  and   424. — The  Ciliary  Region  of  the  Lacertilian  Eye. 


Fig.  423.— Tho  lizard,  Tupiiuimbis. 

G,  scleral  cartilage  ;    il/,  ciliaiy  muscle  ;    0,  scleral  ossicles  ;    P,  jDectinate 
ligament  ;    S,    ciliary    venous   sinus  ;     2',    tenacular   ligament    (after   Franz). 


Fig.   424.— The  skink. 

M ,  ciliary  muscle  ;    O,  scleral  ossicles  ;     T',  ciliary  ^'enous  sinus   (  X  60) 

(Norman  Ashton). 


Iguana  tuberculata 


containing  iridocytes  (Plate  V).i  The  vascular  arrangements  resemble 
those  of  the  salamander  ;  the  two  feeding  arteries  enter  peripherally 
below  and  to  the  temporal  side  and  run  circnmferentially  but,  in  con- 
tradistinction to  the  arrangement  in  amphibian  eyes,  the  veins  lie 
superficially  forming  a  plexus  of  radial  vessels  which  are  usually 
conspicuous  ;    the  cajiillary  zone  is  of  varying  width  but  is  often  con- 

^  The  irides  of  many  lizards  compare  in  their  remarkable  brilliance  with  those  of 

nrie  parrots.    In  the  green  lizard,  Lncertn  viridis,  they  are  of  brightly  speckled  gold  ;   in 

■■!n(A  tuberculata  they  show  an  exceedingly  delicate  festooned  pattern  of  gold  and 

b       ■;  fibres  ;    in  the  geckos,  a  striped  pattern  of  dark  brown  in  a  light  yellow-ochre, 

g!         -h  or  grey  background  ;    and  so  on. 


PLATE  V 

The  Irides  of  Lizakds 
(Ida  IVIann) 


Fig.  1.^ — Cochin-China  water-lizard, 
Physignathus  cochinchinensis  (right  eye). 


Fig.  2. — Agamid  lizartl,  Agama  agaiiit 


Fig.  3. — ^  iplia  iguaud.  Ojiln yo(  act  ,'>i(jj(  iLilioaa. 


Fig.  4. — African  plated  lizaid.  Gcrrhosaurut 

girniih'.s. 


:^\ur 


%;, 


Fig.     5. — Black-pointed     tejii,      Tuphtambi-s 
uigropunciutus. 

[To  f (toe  p.  358. 


REPTILES 


359 


fined  to  the  thickened  rim  of  the  pupillary  margin  (Mann,  1929).  This 
vascular  pattern  may  to  some  extent  be  obscured  by  the  pigment  of 
the  multicoloured  iris  {Agama)  but  stands  out  in  prominent  relief  in 
those  irides  provided  with  a  guanine  layer  on  which,  indeed,  the  vessels 
may  cast  shadows  ;  it  is  to  be  noted  that  the  general  arrangement  of 
deep  circumferential  arteries  and  superficial  radial  veins,  found 
commonly  among  Sauropsida.  is  completely  different  from  the  ichthyo- 
psidan  j^lan. 

The  angle  of  the  anterior  chamber  is  occujoied  by  a  loose  jDectinate 
ligament  bridging  over  the  space  between  the  cornea  and  the  anterior 


Agama 


Fig.  425. — The  Pupils  of  a  Xoctviinal  Gecko. 

The  Tokay  gecko,  so  called  from  its  chirping  cry  "  Tuk-kaa."  On  the 
left,  the  pupil  contracted  by  bright  light,  showing  its  reduction  to  a  slit  with 
three  stenopa?ic  openings.  On  the  right,  the  wide  hexagonal  pupil  in  dark- 
ness photographed  by  infra-red  light.  (New  York  Zoological  Society  ;  photo- 
graphs by  Sam  Dunton  ;    from  the  Illustrated  London  Xexcs.) 


chamber,  ■\\hile  a  ciliary  sinus, ^  venous  in  nature  but  usually  devoid 
of  blood,  runs  circumferentially  around  the  region  of  the  angle 
separated  from  the  sclera  by  fibres  of  the  ciliar}^  muscle  (Lauber,  1931) 
(Figs.  423-4). 

The  ^Ji<^Ji7  in  diurnal  lizards  is  usually  round  and  relatively 
immobile,  in  nocturnal  lizards  extremely  active  and  contracting  to  a 
slit-shape  (with  the  exception  of  the  Gila  monster,  Helodenna,  wliich 
has  circular  pupils,  Walls,  1934).  Of  the  latter  tjq)e,  a  typical  slit- 
shaped  pupil  is  seen  in  the  Mexican  night  lizard,  Xanfusia  (Kallmann, 
1932-33).  In  this  class,  however,  the  most  interesting  is  the  pupil  of 
the  nocturnal  geckos  (Fig.  425)  which  is  somewhat  reminiscent  of  that 
seen  in  the  dogfish,  ScijlUorhinus  (Fig.  313)  and  in  some  rays, 
(Fig.  312).  The  diurnal  geckos,  like  the  great  majority  of  lizards,  have 
a  round  pupil,  remaining  circular  on  contraction  and  little  if  at  all 
affected  by  sunlight  or  drugs,  but  in  the  nocturnal  types  in  diffuse 

1  Analogous  to  the  canal  of  Schlemm. 


Heloderma       ._ 


360 


THE   EYE   IN   EVOLUTION 

Figs.  426    to    428. — The  Lenses  of  Lizards. 


Fig.  426. — Section  through  the  annular  pad  of  the  skink.    The  iris  and  cornea 
above  and  to  the  right  (  x  70)  (Norman  Ashton). 


Fig.  427. — The  lens  of  Lacerta,  sin  ■wing  a  small  annular  pad  (after  Rabl). 


Fig.  428. — The  lens  of  the  chameleon. 
Showing  a  large  annular  jaad  (after  Rabl). 


REPTILES 


361 


light  the  pupil  assumes  the  form  of  a  vertical  slit  with  several  paired 
notches  on  its  margins  ;  on  contraction  in  bright  light  the  slit  com- 
pletely closes  leaving  only  a  row  of  stenopoeic  openings  down  its 
length,  which,  acting  together,  would  produce  an  image  of  considerable 
clarity  without  any  dioptric  mechanism  or  accommodative  adjustment 
(Fig.  425)  (Beer,  1898  ;  Lasker,  1034).  Such  an  arrangement  is  un- 
doubtedly of  considerable  visual  value,  and  Johnson  (1027)  after 
repeated  observation  concluded  that  to  some  extent  the  movements 
of  this  exceedingly  sensitive  pupil  were  under  voluntary  control.^ 

The  lens  is  typically  sauropsidan  (Beer,  1898  ;  Rabl,  1898).  In 
size  it  is  voluminous,  particularly  in  nocturnal  types  ;  in  shape  it  is 
flattened  antero -posteriorly  with  a  low  curvature  on  its  anterior  surface 
and  a  high  convexity  posteriorly  except  in  nocturnal  types,  particularly 
the  gecko,  wherein  it  is  almost  spherical  ;  in  consistency  it  is  soft  and 
readily  mouldable  with  a  tliin  capsule  ;  and,  as  in  Cyclostomes, 
sutures  are  usually  absent  for  the  fibres  terminate  in  one  circumscribed 
area  anteriorly  and  posteriorly.  The  most  characteristic  feature, 
however,  is  the  equatorial  annular  pad,^  formed  by  the  radial  growth 
of  the  subcapsular  epithelium  in  this  region  which  elongates  to  such 
an  extent  that  it  abuts  against  the  ciliary  body.  In  most  lizards  the 
pad  is  marked,  in  the  chameleon  enormous,  the  thickest  known  among 
Sauropsida  (Figs.  426-8).  The  zonular  fibres  arising  from  a  broad 
area  of  the  ciliary  body  are  attached  to  this  structure.  In  one  diurnal 
gecko  [Lygodaciylus)  the  lens  is  coloured  with  a  yellow  pigment. 

The  retina  of  lizards  shows  many  interesting  peculiarities.^  The 
pigment  epithelium  is  well  formed  with  numerous  long,  fine  processes 
dipping  dowTi  permanently  between  the  outer  segments  of  the  visual 
cells.  The  extent  of  the  migration  of  pigment  with  variations  of  light  is 
small  (3/x  in  SceJoporus)  ;  and  the  contraction  of  the  cones  on  exposure 
to  light  is  also  minimal  (Detwiler,  1016-23). 

As  seen  ophthalmoscopically,  the  fundus  of  lizards  varies  in  its 
appearance  in  the  different  genera,  but  it  sho\\s  the  same  general 
characteristics  (Plate  VI,  Figs.  1  to  5).  The  background  tends  to 
be  uniform — usually  slate-grey  (as  in  the  alligator  lizard.  Anolis 
alligator),  sometimes  dark  or  almost  black  (as  in  Lacerta  galloti).  brick- 
red  in  the  nocturnal  geckos  (grey  in  diurnal  types),  and  exceptionally 
green  (as  in  the  iguanid.  Conolojyhus  cristafus)  or  variegated  (as  grey  in 
the  upper  half  and  dark  red  below  in  the  iguanid,  Metopoceros  cornutus). 
Sometimes  it  is  heavily  besprinkled  with  white  spots  {Lacerta  galloti), 

^  Compare  the  pupils  of  seals  and  sea-lions,  p.  470. 

*  An  annular  pad  situated  laterally  is  marked  in  Chelonians,  Crocodilians 
and  lizards  (thin  in  geckos  and  snake-lizards).  It  is  vestigial  in  Monotremes  and 
some  Marsupials.    It  is  situated  anteriorly  in  Ophidians. 

3  Krause  (1863-93).  Schultze  (1866-67),  Ranvier  (1889),  Hess  (1912).  Franz  (1913), 
Rochon-Duvigneaud  (1917-43),  Verrier  (1930-32).  Kahmann  (1933),  Walls  (1934-42), 
Underwood  (1951). 


Anolis 


362 


THE   EYE   IN   EVOLUTION 


while  in  Conolophus  cristatus  there  are  yellow  spots  over  the  green 
background.  Usually  the  semi-opaque  nerve  fibres  radiate  uniformly 
outwards  from  the  disc,  sometimes,  as  in  the  American  "  glass-snake," 
O'phisatirus  ventralis,  coarse  in  texture,  sometimes  so  fine  as  to  be  barely 
visible  (the  leaf-footed  lizard,  Pygojnis  lejndopus,  Cham.celeo7i).  The 
disc  itself  is  circular  and  white  but  is  practically  entirely  obscured  by  the 
conus.    The  retina  is  invariably  entirely  avascular. 


Fig.  429. — The  Posterior  Pole  of  the  Eye  of  the  Lizard,  Lacerta  muralis. 

Showing  the  optic  nerve  and  the  conus  papillaris  approaching  the  lens  (  X  50) 
(Katharine  Tansley). 


Nutrition  is  conveyed  to  the  retina  by  a  peculiar  vascular  structure, 
the  CONUS  PAPILLARIS,  an  outgrowth  of  glial  tissue  from  the  optic  disc 
supplied  by  an  artery  and  vein  issuing  from  the  optic  nerve  and  derived 
from  the  hyaloid  (not  the  choroidal)  vascular  system  (Fig.  429). 
Originally  described  by  8oemmerring  (1818)  in  the  eye  of  lizards  {Lacerta 
monitor,  L.  vulgaris,  L.  iguana),  the  conus  has  attracted  a  great  deal  of 
study. ^  It  is  a  richly  vascular  structure  with  a  central  artery  and  vein 
surrounded  by  a  thick  layer  of  wide  capillaries  heavily  dusted  with 
pigment  granules,  the  A\'hole  lying  in  a  framework  of  neuroglial  tissue 

'    i  i-    (1853),    Hulke    (1864),    H.    Mliller    (1862),    Beauregard    (1876),    Kopsch 

(1892),   -         ow  (1901),  Jokl  (1923),  Johnson  (1927),  and  many  others. 


PLATE  VI 

The  Fundi  of  Lizabds 

(Lindsay  Johnson) 


Fig.  I.  -  ^VlJigator  lizard,  Anolis  alUyutor.  Fig.  -. — Tuilii.sli  gucku,  llemidactylus  turcious. 


Fig.  3. — GalDpagoan  iguanid,  Conoloplius  subcvistutus. 


• 


Fig.  1.     Dlaulv  1^, 
[To face  p.  363. 


-l/f  iojiUt  (  lif,   I  UCItUtUS. 


Fit..  :>.      (  haui.lt'cii,  L  lutiiiiLku,!  culgai-iis. 

S.O. — VOL.  I 


REPTILES 

(Franz,  1913  ;  JokL  1923).  Considerable  variations  occur  in  size  and 
shape.  As  a  rule  it  is  a  relatively  simj)le  structure  and  only  in  some 
Iguanids  (particular!}-  Conolopkus  and  Metopoceros,  Plate  VI)  does 
it  become  plicated  and  approach  the  complexity  and  beauty  of  the 
pecten  of  Birds.  It  may  be  circular  in  cross-section,  oval,  X-  or  Y- 
shaped  (as  in  the  monitor  lizard.  Varanus)  ;  it  may  be  short  and 
stumpy,  forming  a  small  cushion-like  paj^illa  on  the  disc,  as  in  nocturnal 


363 


"^^'i?»i.^>**-ii^' 


Fig.  430. — The  Retina  of  the  Lizaed. 

(1)  ganglion  cells  ;  (2)  inner  plexiform  layer  ;  (3)  inner  nuclear  layer  ; 
(4)  outer  plexiform  layer  ;  ('^)  outer  nuclear  layer  ;  (6)  visual  cells  ;  (7)  pig- 
mentary epithelium  ;    (8)  choroid  (  X  500)  (Xorman  Ashton). 


forms  (most  geckos;  the  leaf- footed  lizard,  Pygopus)  or  in  the  chameleon, 
or  long  and  slender  pointing  toAvards  the  centre  of  the  globe  (the  slow- 
worm,  A7iguis  fragilis),  sometimes  nearly  reaching  the  lens  (the  green 
lizard  of  Southern  Europe,  Lacerta  viridis)  ;  only  in  the  degenerate 
burrowing  types  (Ampliisbaenidae,  etc.)  is  the  conus  lacking.^ 

In  its  histological  structure  the  retina  itself  is  avascular,  thick  and 
richly  cellular  with  a  well-defined  lamination  (Fig.  430)  ;  the  inner 
nuclear  layer  with  9  or  10  rows  of  superimposed  nuclei  is  compact  and 
the  ganglion  cell  layer  with.  2  or  3  rows  of  cells  is  particularly  well- 
developed  and  conspicuous.    The  visual  cells  in  most  species  are  of  two 

1  p.  733. 


Anguis 


364 


THE   EYE   IN   EVOLUTION 


types,  showing  a  variation  in  configuration  from  typical  cones  to  rods 
(Walls,  1934)  (Figs.  431-3).  In  the  great  majority  of  lizards  of  diurnal 
habit  there  are  typical  single  and  double  cones  ;  the  single  cones  have 
a  yellow  oil-droplet  ;  of  the  double  cones,  one  element  has  an  oil- 
droplet  and  the  other  a  voluminous  paraboloid  (Krause,  1863).  In  some 
geckos.  Underwood  (1951)  described  another  type  of  double  visual  cell 
wherein  each  member  possessed  a  paraboloid  and  an  ellipsoid  while  the 

Figs.  431  to  433. — Visual  Cells  of  Lizards. 


Fig.  431.— The  cones  of 
a  diurnal  lizard,  Crota- 
jjhytus. 


Fig.  432.— The  cones  of 
a  nocturnal  lizard, 
Xantitsia. 


Fig.  433.— The  rods  of 
a  gecko,  Coleonyx  ( X 
1,000)   (Gordon  Walls). 


larger  member  had  an  oil-droplet.^  In  some  nocturnal  species  the  drop- 
lets are  discarded  (the  worm-lizard,  Aniella  ;  the  poisonous  Gila  mon- 
ster of  Mexico  and  Arizona,  Heloderma)  or  colourless  (the  night  lizard, 
Xantusia,  Heinemann,  1877),  but  the  outer  segments  of  the  visual 
cells,  both  single  and  double,  are  elongated  and  rod-like  although 
rhodopsin  is  lacking.  In  the  nocturnal  geckos,  however,  both  elements 
are  frankly  slim  and  rod -like  and  the  long  outer  segments  contain  an 
abundance  of  visual  purple  ;  these  should  therefore  be  considered  as 
rods  (Detwiler,  1923  ;  Walls,  1942).  There  is  little  convergence  in  the 
retina  ;  Vilter  (1949),  indeed,  found  that  the  ratio  between  visual  cells 
and  ga-  .  lion  cells  was  approximately  unity. 

Tn  Aristelliger  Underwood  noted  occasional  trijjle  visual  cells. 


REPTILES 


365 


The  eyes  of  diurnal  lizards  contain  a  central  area  at  the  posterior 
pole  wherein  the  cones  are  longer  and  thinner  than  in  the  peripheral 
retina  ;  in  addition,  in  diurnal  varieties  a  central  fovea  is  present 
wherein  the  cones  are  closely  packed,  long  and  filamentous  (Fig.  434). 
The  fovea  is  very  striking  in  such  forms  as  the  American  horned 
"  toad,"  Phrynosoma  (Detwiler  and  Laurens,  1920  ;  Ochoterena,  1949), 
but  is  seen  in  its  most  fully  developed  form  in  the  chameleon.     The 


PJirynosoma 


Fig.  43-1. — The  Remarkably  Well-formed  Fovea  of  the  Gippslaxd  Water- 

DRAGOX,    PHTSKJyATHCS    (O'Dav). 

ch,  the  thick  choroid  ;    ?•.  the  remarkably  well-formed  retina  ;    s,  scleral 
cartilage  ;    sc,  sclera  ;    v,  \isual  cell^;. 


remarkable  fovea  of  this  animal  wherein  the  cones  are  longer  (100^), 
their  concentration  higher  (756,000/sq.  mm.),  and  the  pit  deei3er  than 
in  the  fovea  of  man,  has  long  excited  admiration  (H.  ^Nliiller,  1861-72  ; 
Chievitz,  1889  ;  A  Vails,  1942  ;  Detwiler,  1943  ;  Rochon-Duvigneaud, 
1943  ;  and  others).  In  nocturnal  species,  on  the  other  hand,  only  a 
trace  of  a  foveal  pit  ma}'  be  observed  {Xanfusia)  or  it  may  be  entirely 
lacking  {Heloderma,  and  usually  in  the  geckos).  In  some  geckos  a  shal- 
low temporal  fovea  exists  {Gonatodes  ftiscus,  Sphoerodacfylus  argus,  S. 
parkeri,  Underwood,  1951)^;  while  in  certam  arboreally  active  species 
of  the  diurnal  lizard,  Anolis,  in  addition  to  the  deep  central  fovea,  a 

^  Gonatodes  has  a  pure-cone  retina,  SphcKrodnctijlus  argus  has  visual  elements 
intermediate  between  rods  and  cones,  .S.  parkeri  has  a  pure-rod  retina  and,  incidentally, 
a  pure-rod  fovea. 


366 


THE   EYE   IN   EVOLUTION 


Chameleon 


Skink 


shallow  temporal  one  may  also  be  present  containing  both  single  and 
double  cones  (Underwood,  1951)  ;  this  is  the  only  known  occurrence  of  a 
bifoveate  retina  apart  from  Birds.  It  is  to  be  noted  that  with  their 
lateral  eyes  and  small  binocular  field  (about  20°,  Kahmann,  1932) 
binocular  fixation  with  the  central  foveae  of  lizards  is  out  of  the  question; 
each  is  used  monocularly  and  independently  except,  perhaps,  for  the 
chameleon  with  its  quite  extraordinary  ocular  movements.^  The 
shallow  temporal  fovea  in  Anolis  can,  however,  be  used  for  binocular 
vision  to  assist  in  its  agile  arboreal  activities. 

The  0^)110  nerve  does  not  have  a  well-defined  and  orderly  fascicular 
system  and  throughout  it  the  oligodendroglial  cells  are  somewhat 
irregularly  scattered  (Prince,  1955). 

THE  OCULAR  ADNEXA.  Most  lizards  j30ssess  two  eyelids  outlining 
a  horizontal  palpebral  aperture  (Fig.  419),  and  with  the  exception  of  an 
iguanid,  Anolis  alligator,  a  species  of  American  "  chameleon  "  in  which 
the  two  lids  move  equally,  the  upper  lid  is  more  or  less  stationary,  the 
lower  mobile  as  is  usual  in  the  lower  Vertebrates  ;  the  latter  is  often 
supported  by  a  tarsal  plate  of  fibrous  tissue  and  moved  by  a  retractor 
muscle  attached  to  its  lower  border  and  arising  from  the  depths  of  the 
orbit  (Cords,  1922  ;  Anelli,  1936). ^  In  some  forms  (Chamceleon)  in 
which  the  globe  is  very  large,  the  palpebral  aperture  is  constricted  to 
the  size  of  the  pupil  and  the  lids  move  with  the  eyeball  (Figs.  420  and 
845).  In  this  lizard  the  lids  are  exceedingly  soft  and  thin  and  rarely 
close  ;  when  they  do  they  form  a  horizontal  slit  at  the  same  time 
pushing  the  eye  backwards  into  the  orbit. 

In  a  number  of  lizards  belonging  to  the  families  Lacertidse  (as  Eremias, 
Cahrita  and  Ophiops),  Tejidte  and  Scincida?,  and  in  some  species  as  Cordylosaurus, 
Lanthanotus  and  soine  West  Indian  members  of  the  iguanid  genus,  Anolis,  there 
is  a  transparent  window  in  the  lower  lid  where  the  scales  are  reduced  or  absent 
throvigh  which  vision  is  possible  when  the  lid  is  drawn  upwards  ;  alternatively, 
as  in  the  Iguanids,  two  or  three  black-bordered  scales  are  semi-transparent, 
forming,  as  it  were,  a  window  with  panes  of  glass  through  which  some  vision  is 
possible  (Figs.  435-441).  The  area  involved  is  small  and  when  the  eye  is  opened 
the  window  is  concealed  in  a  fold  in  the  lower  lid.  Most  of  these  lizards  live  in 
deserts  or  a  rocky  habitat  and  it  is  probable  that  such  a  window  may  serve  as  a 
protective  measure  against  abrasion  by  sand  or  grit  (Walls,  1934).  In  other  cases 
(as  the  West  Indian  Anolina?)  the  animals  inhabit  dark  caves  and  frequently  come 
out  to  the  sun  ;  it  may  be  that  the  black-bordered  scales  act  as  dark  glasses  as  a 
protection  against  the  sun  in  an  animal  with  a  relatively  immobile  pupil  (Plate, 
1924;  Mertens,  1954  ;  Williams  and  Hecht,  1955).  In  others  again,  particularly 
bin-rowing  lizards,  the  skink,  Ablepharus,  and  those  which  like  the  geckos  crawl 
in  gravel  and  stubble,  as  a  protective  measure  the  transparent  lower  lid  is  fused 
with  the  upper  to  constitute  a  "  secondary  spectacle  "  ^  fitting  over  the  globe 

1  p.  694. 

"  Only  in  some  Mammals  (the  leopard,  bat  and  hedgehog)  is  cartilage  found  in 
tlv-  '  :rsal  plate, 
p.  266. 


REPTILES 


367 


like  a  contact  glass  and  separated  from  it  by  a  closed  conjunctival  sac  as  is  seen 
in  snakes  (Schwarz-Karsten,  1933  ;  Walls,  1934  ;  Verrier,  1936  ;  Rochon- 
Duvigneavid,  1943).  In  such  cases  the  spectacle  may  be  surrounded  by  a  rim 
of  tiny  scales,  as  in  Ablepharns,  Ophiops,  or  the  geckos  (Fig.  435)  ;  alternatively, 
as  in  snakes,  such  a  rim-formation  is  lacking  and  the  spectacle  is  inserted 
into   the   ordinary   arrangement   of  the   scales   of  the   head    (Fig.    436).      It   is 

Figs.  435  to  441. — The  Eyelids  of  Lizards. 


Fig.  43.5. — Ablepharus. 


Fig.   ■iZQ.—  TyphlcEontias. 


There  is  a  secondary  spectacle  formed  by  the  fused  transparent  lids. 
In  Ablepharus  this  is  surrounded  by  a  ring  of  scales  ;  in  Typhlceontias  this 
is  absent. 


Fig.  437. — Zonosaurus. 


Fig.  438. — Eremius. 


Fig.  439. — Mabuija. 


The  lower  lid  is  mobile.  In  Zonosaurus  the  scaly  lower  lid  rises  to  meet 
the  upper  lid  ;  in  Eremias  the  central  scales  are  transparent  ;  in  Mabuya 
the  central  scales  are  lacking  (after  Angel). 


Fig.  440. — Anolis  lucius. 


Fig.  441. — Anolis  argenteolus. 


The  mobile  lower  lid  has  semi-transparent  scales   (3   in   .4.  lucius,   2    in 
A.  argenteolus)  with  a  black  bordered  edge  (Williams  and  Hecht). 


exceptional  for  eyelids  to  be  absent,  as  in  Pachydactylus  maculatus,  one  of 
the  geckos  wherein  they  are  represented  only  by  a  thickened  dermal  fringe 
around  the  periphery  of  the  eye. 

When  the  lower  Hd  i.s  mobile  and  opaque,  a  transparent  nictitating 
membrane  is  formed  from  a  vertical  fold  of  the  conjunctiva  at  the 
nasal  corner  of  the  palj^ebral  aperture  which  can  be  swept  across  the 
cornea  from  the  nasal  to  the  temporal  side.  Moisture  and  lubri- 
cation are  usually  attained  by  a  lacrimal  gland  with  several  con- 
tractile ducts  at  the  temporal  canthus  and  a  large  harderian  gland 


368 


THE   EYE   IN   EVOLUTION 


lying  naso-ventrally  provided  with  a  single  duct  (Loewenthal,  1935-36  ; 
Schwarz-Karsten,  1937  ;  Bellairs  and  Boyd,  1947-50).  The  lacrimal 
gland,  however,  is  absent  in  the  chameleon  and  many  geckos.  The 
naso-lacrimal  duct  enters  the  nose  within  the  accessory  olfactory 
vomero-nasal  organ  of  Jacobson.  The  nictitating  membrane  is  pulled 
across  by  a  tendon-like  cord  arising  from  its  free  edge  and  attached  to 
the  dorsal  wall  of  the  orbit,  its  movements  being  controlled  by  a 
special  arrangement  of  muscles  behind  the  eyeball  (Fig.  442). 

In  addition  to  the  rectus  muscles  and  a  well-formed  retractor 
bulbi,  two  extra  muscles  are  inserted  into  the  posterior  aspect  of  the 
globe,  both  supplied  by  the  Vlth  cranial  nerve  (Fig.  443).  The  first, 
the  BUiiSALis  (quadratus)  muscle,  is  inserted  into  the  sclera  near  the 


Fig.  HI. — The  Orbit  of  the  Monitor, 
Varan  us. 

With  the  eye  removed  showing  the 
nictitating  membrane  with  its  tendon 
looping  through  the  bursahs  muscle  (after 
Bland- Sutton). 


Fig.    443. — The    Posterior    Aspect    of 
the  Globe  of  Lacerta. 

B,  bursalis  muscle  ;  N,  the  tendon  of 
the  nictitans  ;  ON,  optic  nerve  ;  R, 
retractor  bulbi  muscle  ;  RB,  retractor 
bursalis  muscle  (after  Franz). 


optic  nerve  and  round  it  the  tendon  of  the  nictitating  membrane  loops 
so  that  the  latter  is  drawn  taut  when  the  muscle  contracts  ;  from  it  a 
muscular  slip  runs  upwards  to  be  inserted  more  dorsally  in  the  sclera, 
the  RETRACTOR  BURSALIS,  wliicli  acts  by  bracing  the  bursalis  so  that 
the  muscular  apparatus  and  the  looped  tendon  are  kept  away  from  the 
optic  nerve  when  contraction  occurs.  In  most  lizards  ocular  move- 
ments are  sluggish  or  occasionally  absent,  a  marked  and  extraordinary 
exception  being  the  insectivorous  chameleon  ^  :  in  it  the  extra-ocular 
muscles  are  very  fully  developed  (Leblanc,  1925). 

The  orbit  of  lizards  is  open  and  fenestrated,  a  peculiarity  being 
that  the  optic  nerves  pass  through  several  openings  in  the  endocranium  ; 
the  posterior  bony  wall  is  very  deficient  to  allow  room  for  a  wide 
gape  of  the  jaws. 

THE    CHELONIAN    EYE 

THE  TORTOISES  AND  TURTLES  are  the  most  ancient  of  surviving 
Reptili'^s  2 — sluggish  animals  encased  in  a  dorsal  and  ventral  bony  cara- 
pac(      '  f)  the  shelter  of  which  the  head  as  well  as  the  limbs  and  tail  can 

1  p.  604.  2  p.  234. 


HEPTlLEg 


S60 


be  withdrawn.  The  Chelonia  are  divided  into  two  sub-groups — of  the 
first,  wherein  the  vertebrae  and  ribs  are  free  from  the  carapace, 
Dermochelys  coriacea,  a  huge  marine  turtle  sometimes  6  feet  in  length, 
widely  but  sparsely  distributed  in  tropical  seas,  is  the  sole  representa- 
tive. The  second  group,  with  dorsal  vertebrae  and  ribs  fused  in  the 
carapace,  comprises  the  chelonidj]],  marine  and  amphibious  turtles 
with  paddle-like  flippers  living  on  or  near  the  shores  of  tropical  seas, 
and  the  testudixid.e,  land  tortoises  with  feet  provided  with  toes 
adaj^ted  for  walking,  found  widel}^  in  the  warmer  regions  of  the 
Eastern  and  Western  Hemispheres  (Fig.  444)  ;  among  these  the 
terrajDins  form  an  intermediate  group  with  webbed  toes. 


Turtle 


0t  a^w*-'  '-■"■  "  i». 

Fig.    444. — The    Head    of    the    Tortoise,    Testudo    (Katharine    Taiislej'). 


The  eyes  of  the  Chelonians,  described  and  beautifully  figured  by 
Albers  (1808)  and  Soemmerring  (1818),  and  intensively  studied  by 
Kopsch  (1892),  bear  a  close  resemblance  to  the  lacertilian  eye  just 
described,  but  in  general  are  more  simi^le  in  structure  ;  there  are, 
however,  some  major  difl^erences — the  i^resence,  of  ciliary  processes,  the 
participation  of  the  sphincter  pupillce  in  the  act  of  accommodation,  and 
the  absence  of  a  conus  (Figs.  445  and  446). 

The  GLOBE  is  comj)aratively  small  and  the  cornea,  instead  of 
projecting  forwards,  continues  the  curvature  of  the  sclera  so  that  the 
corneo -scleral  sulcus  is  insignificant.  The  epithelium  is  thick.  Bowman's 
membrane  absent  and  the  endothelium  markedly  developed  (Fig.  448). 
The  scleral  ossicles  are  imbricated  in  several  layers  so  that  the  edge 
of  one  lamella  is  inserted  ]:)etween  two  others.  Their  numbers  vary 
from  6  to  15,^  while  the  scleral  cartilage  is  very  thick  (1  cm.  in  the 

1  The  scleral  ossicles  number  6-9  in  the  Greek  tortoise,  Testudo  grceca  ;  10  in  the 
tortoise,  Emys  (Konig,  1934)  ;  15  in  the  Mauritius  tortoise  (Rochon-Duvigneaud, 
1943)  ;  and  so  on. 


S.O.— vol.  I. 


24 


370 


THE   EYE   IN   EVOLUTION 

Figs.  445  and  446. — The  Chelonian  Eye. 
so. 


Fig.   445. — Diagram  of  a  Chelonian  eye. 

A,  annular  pad  ;  Ch,  choroid  ;  CM,  ciliary  muscle  ;  ON,  optic  nerve  ; 
P,  pectinate  ligament  ;  S,  scleral  cartilage  ;  Sc,  sclera  ;  SM,  sphincter 
muscle  ;    SO,  scleral  ossicles  ;    VS,  ciliary  venous  sinus  ;    Z,  zonule. 


Fig.  446. — Section  through  the  eye  of  the  tortoise,  Testudo  (Norman  Ashton) 


leathery-skinned  turtle,  Dermochelys,  Rochon-Duvigneaiid,  1943) 
(Fig.  447).  In  aquatic  forms,  the  iris  has  the  same  bright  and  varie- 
gated colour  as  in  the  lizard — red,  yellow,  green  and  brown — and  in 
some  ■  y])es  is  strij^ed  in  such  a  way  that  the  pattern  on  the  skin  is 
cont  i  v-rl  over  the  iris  as  if  for  the  purposes  of  camouflage  (the  terrapin, 
Cle7n:;        Mann,  1931  ;  and  particularly  the  i3ainted  turtle,  CAr^/'^ew?/^, 


REPTILES 


371 


Walls,  1942)  (Plate  VII ).^  In  the  land  tortoises  the  colours  are  less 
bright,  brown  predominating.  The  common  box  tortoise,  Testudo 
Carolina,  is  peculiar  in  that  it  shows  a  remarkable  instance  of  sexual 
dimorphism,  the  iris  of  the  male  being  red,  of  the  female  brown. 


'».*»^^  •;t*i^    »  *^*  •««*»*•  •• 


Fig.  447. — The  Posterior  Segment  of  the  Eye  of  the  Tortoise. 

1,   tlie   retina  ;     2,   choroid  ;     3,   scleral   cartilage  ;     4.   fibrous  sclera   (X  112) 
(Katharine  Tansley). 


Fig.  448. — The  Ciliary  Region  of  the  Eye  of  the  Tortoise. 

Note  the  immensely  thick  corneal  epithelium,  the  scleral  ossicles,  O, 
arranged  in  layers,  the  trabecular  tissue  forming  a  pectinate  ligament  across 
the  angle  of  the  anterior  chamber,  and  the  highly  developed  sphincter  of 
the  pupil.  The  vessel  lying  internal  to  the  angle  of  the  anterior  chamber  is  the 
ciliary  venous  sinus,  homologue  of  the  canal  of  Schlemin  (  X  60)  (Norman 
Ashton). 


1  This  matching  of  the  colour  of  the  iris  to  form  an  "eye  mask"  in  a  uniform 
pattern  with  the  colours  of  the  head  is  also  well  seen  in  such  fish  as  (he  lidless 
lion-fish,  Pterois  ;  in  Amphibians,  such  as  the  frog,  Rnna  sjiJienocephala,  the  newt, 
Triturus  torosiis  :  in  Reptiles,  such  as  the  tree-snake,  Oxyheli.^  (See  Cott,  1940  •  O'Day 
1942).  '  '  ^' 


372 


THE   EYE   IN   EVOLUTION 


Tortoise 


The  pupil  is  circular  and  immobile  both  to  light  and  drugs  although 
its  sphincter  is  powerful  ;  this  muscle  is  essentially  accommodative 
in  function  (Fritzberg,  1912).  The  ciliary  body  separates  abruptly  from 
the  sclera  to  approach  the  lens  leaving  the  angle  of  the  anterior 
chamber  deep  and  cleft-like  ;  the  angle  is  traversed  by  the  loose 
pectinate  ligament  linking  the  iris  with  the  cornea,  while  deep  in  the 
cleft  lies  the  ciliary  venous  sinus.  The  ciliary  body  has  some  60  well- 
marked  ciliary  processes  which  abut  against  the  lens  in  accommodation. 
The  striated  musculature  resembles  that  of  the  lacertilian  eye  with 
the  ventral  transversalis  muscle  usually  well-developed  (Briicke,  1846  ; 
Mercanti,  1883  ;  Hess,  1912  ;  Fritzberg,  1912)  ;  the  latter  is  absent 
in  some  forms  {Testudo,  Konig,  1934).  The  vascular  arrangements  of 
the  uveal  tract  are  of  the  usual  reptilian  type  (Fritzberg,  1912). 

The  lens  is  extremely  soft  and  almost  fluid  in  consistency,  probably 
the  most  readily  moulded  in  the  vertebrate  phylum,  and  while  it  takes 
the  form  of  a  flat  ellipse  in  land  tortoises,  it  is  of  necessity  almost 
spherical  in  sea  turtles  ;   the  annular  pad  is  small. 

The  fundus  oculi  of  Chelonians  as  seen  ophthalmoscopically  is 
singularly  primitive  and  uniform  (Plate  VII,  Fig.  3).  The  background 
is  orange-red  and  from  the  circular  disc  readily  visible  nerve  fibres 
radiate  to  the  periphery,  sometimes,  as  in  the  snapping  turtle,  Chelydra 
serpentina,  almost  completely  obscuring  the  background.  The  disc  is 
without  a  conus  and  is  white,  apart  from  a  brownish  patch  of  pigment 
in  the  Murray  turtle,  Chelodina  longicollis,  in  which  the  nerve  fibres 
are  few  and  faintly  marked. 

The  fundus  of  the  Bvirgoma  soft-shelled  turtle,  Emyda  granosa,  is  unique 
(Plate  VII,  Fig.  4).  The  background  is  of  brownish  pink  with  red  dots,  and  the 
large  white  disc  is  surrounded  by  a  red  choroidal  ring  outside  which  the  nerve 
fibres  radiate  giving  the  ai3i:)earance  of  a  solar  corona  (Johnson,  1927). 

Histologically  the  retina  does  not  reach  the  high  degree  of  defini- 
tion in  its  architecture  found  in  the  lizard  ;  throughout  its  extent  the 
different  layers  are  by  no  means  exclusively  segregated  but  their 
elements  tend  to  be  intermingled  (Figs.  449-452). ^  In  the  early  stages 
of  development  an  avascular  glial  cone  may  appear-  on  the  optic  disc 
in  some  turtles  ^  but  this  always  disappears  in  the  adult  ;  the  retina  is 
thus  entirely  avascular  depending  only  on  the  choroid  for  its  nourish- 
ment. The  visual  cells  show  a  vast  predominance  of  cones,  either  single 
or  double,  the  former  and  one  element  of  the  latter  containing  an  oil- 
droplet,  orange,  yellow  or  ruby -red  in  colour.  Cells  with  a  cone -like 
structure  but  resembling  rods  in  the  heaviness  of  the  outer  segment 

1  See  Hulke  (1864),  Heinemann  (1877),  Chievitz  (1889),  W.  Krause  (1893),  Putter 
(1912). 

2  In  the  sea-turtle,  Chelonia,  the  snapping  turtle,  Chelydra,  the  painted  turtle, 

Ch^-;icmys,  etc. 


PLATE  VII 


The  Eyes  of  Chelonia^js 


•t-'* 


Fig.   1 . — The  iris  of  the  painted  turtle. 
Chrysemys  picta  (Ida  Mann). 


Fig.  2. — The  iris  of  the  European  pond-tortoise, 
Emys  orbicularis.  A,  thin  circiunpupillary 
zone ;  B,  capiUary  plexus ;  C,  zone  of  large 
vessels  hidden  by  pigment  (Ida  Mann). 


J'"lU.    3. The    fundus    of  (.'//V.C'.v    rrosn    il.iii(l-a\     .J  <  ihli>(  ill ). 


■a 


i^'ji;.  4.  — ■I]i«  iiiiidus  of  the  ijurgoma  river  turtle,  Einyda 
i/ranosa  (Lindsay  Johnson), 


S.O. VOL.   I 


[To  face  p.  372. 


REPTILES 

Figs.   449  to  451. — The  Chelonian  Retina. 


i 


373 


Fig.  449. — The  retina  of  the  tortoise  (  x  200)  (Xorman  Ashton) 


V«-   ^^Ff 


i^r^ 


"M\# 


Fig.  4.50. — The  visual  cells  of  the  tortoise"(  X  834)  (Xorman  Ashton). 


im" 


f 


<«  \ 


Fig.  451. — The  visual  cells  of  the  ^liuray  turtle,  Chelodina  (O'Day). 


374 


THE   EYE   IN   EVOLUTION 


Terrapin 


and  the  absence  of  an  oil-droplet  are  also  present  ;  these  anomalous 
cells  occur  particularly  in  those  species  which  habitually  avoid  the 
light  (the  snapping  turtle,  Chelydra)  or  are  frankly  nocturnal  (the 
terrapin,  Pseudemys)  (Detwiler,  1916-43  ;  Walls,  1934-42).  The 
cones  retract  slightly  on  exposure  to  light  (Detwiler,  1916)  and,  as  in 
lizards,  the  migration  of  the  retinal  pigment  is  restricted  (3-6/x  in  the 
tortoise,  Detwiler,  1916). 

An  area  centralis  on  the  visual  axis  is  present  in  the  retina  of 

most  species  where  the  cones  are  smaller 
and  more  densely  packed  than  else- 
where and  the  increased  number  of 
nuclei  determine  a  thickening  of  the 
nuclear  layers  ^  ;  a  fovea,  however,  is 
absent  except  as  a  rarity  when  a  shallow 
depression  is  found. ^  In  the  central 
area  the  ratio  of  receptor  cells  to 
ganglion  cells  is  1  :  1 ,  while  in  the  peri- 
phery it  is  3  :  1.^ 

THE  OCULAR  ADNEXA.      Of  the   twO 

lids  the  lower  is  the  larger  and  more 
mobile  and  the  palpebral  aperture, 
horizontal  in  the  lacertilian  eye,  is 
canted  so  that  it  runs  from  the  dorso- 
temporal  to  the  ventro -nasal  quadrants 
of  the  eye,  as  if  to  make  it  parallel  with 
the  surface  of  the  water  in  aquatic  types 
when  swimming  with  the  head  raised 
above  the  surface.  Only  rarely  is  there 
a  transparent  window  in  the  centre  of 
the  mobile  lower  lid  (the  Murray  turtle,  Chelodina  ;  the  turtle, 
Emyda).  The  movements  of  the  lower  lid  and  the  semi-opaque 
nictitating  membrane  are  controlled  by  two  long  tendons  which  arise 
from  a  fan-shaped  pyeamidalis  muscle  fixed  to  the  posterior  aspect 
of  the  globe  (Fig.  453)  ;  the  retractor  bulbi  muscle  is  powerful  and 
when  it  contracts  the  globe  is  drawn  inwards  and  twisted  far  round, 
the  lower  lid  and  nictitating  membrane  covering  the  eye  at  the  same 
time.  So  forceful  may  this  movement  be  in  some  turtles  that  when  the 
lower  lid  closes  against  the  upper  the  action  is  continued  so  that  the 
latter  is  pushed  back  into  the  orbit.  The  ocular  movements,  however, 
are  relatively  sluggish,  the  eyes  moving  independently  of  each  other. 


Fig.   4.52. — The  Visual  Cells   of 
THE   Snapping  Turtle,  Chelydra. 

A  single  cone,  a  double  cone  and 
a  rod  (  X  1,000)  (Gordon  Walls). 


'  The  painted  turtle,  Chrysemi/s,  Detwiler  (1943),  etc. 

2  The  soft-shelled  turtle,  Emyda,  Gillett  (1923). 

■   The  common  European  fresh-water  turtle,  Emys  obicularis,  Vilter  (1949). 


REPTILES 


375 


A  harderian  gland  with  a  single  duct  is 
always  present;  a  naso-lacrimal  duct  never.  The 
lacrimal  gland  varies  considerably.  Curiously  it 
is  large  in  marine  turtles,  and  may  be  confined 
to  the  temporal  aspect  of  the  orbit  or  scattered 
along  the  length  of  the  movable  lower  lid  with 
one  or  several  ducts. 

The  orbit  of  the  turtle  is  relatively  small 
and  enclosed  ;  some  of  the  bones  common  to 
the  ^'ertebrates  have  been  discarded,  the  nasal 
and  lacrimal  bones,  for  examj^le.  being  replaced 
by  the  frontal. 


Fig.  453. — The  Poster- 
ior Segment  of  the 
Globe  of  the  Turtle. 

L,  tendon  to  lower  lid  ; 
X,  tendon  to  nictitans  ; 
P,  pyramidalis  niu.scle  ; 
R,  retractor  bulbi  muscle 
(after  Franz). 


THE    CROCODILIAN    EYE 

THE  CEOCODiLiA  are  the  largest  extant  Reptiles,  decadent  survivors 
of  the  giant  Reptiles  wliich  dominated  the  earth  in  Mesozoic  times. 
Tliree  genera  are  extant — the  crocodiles,  widely  spread  over  tropical 
rivers  in  Africa.  Asia.  Central  America  and  Australia,  the  alligators 


ViG.   4.54.- 


-The  Head  of  a  young  American  Allig.ator  of  the  Genus 
Caimas  (R.  M.  Holmes). 


of  North  and  South  America  and  Cliina,  and  the  fish-eating  ga vials 
of  the  Ganges  River.  They  are  sluggish  creatures,  more  motile  on 
water  than  on  land  where  most  of  them  obtain  their  prey,  fond 
of  basking  in  the  sun  and  prone  to  hide  in  mud  in  the  hot  season 
(Fig.  454).  Their  eye?.,  primarily  nocturnal  in  their  characteristics,  are 
adapted  for  aerial  vision  for  in  their  predominantly  aquatic  activities 
these  reptiles  float  with  the  eyes  and  nostrils  above  the  surface  and  the 
rest  of  the  body  awash.  Their  essential  features  are  the  ahseyice  of  scleral 
ossicles,  the  reduced  accommodative  m.nscidature,  the  sUt-jmiiil,  the 
marked  ciliary  j^rocesses,  the  retinal  taj^etum.  the  rod-rich  retina,  and  the 
rudimentary  optic  nerve. 


Gavial 


376 


THE   EYE   IN   EVOLUTION 


The  EYEBALL  shows  the  main  characteristics  of  the  typical 
reptihan  eye  described  in  hzards.^  The  globe,  however,  is  almost 
spherical,  little  deformed  by  a  corneo -scleral  sulcus.  The  cornea  is 
thin  ;  the  scleral  cartilage  reaches  almost  to  the  ora  serrata  and  scleral 
ossicles  are  absent. 

The  ciliary  body  shows  more  than  100  tongue-shaped  ciliary 
processes^  which  contact  the  lens  at  its  equator  ;  the  ciliary  musculature 


Fig.  455. — The  Crocodilian  Eye. 

ap,  annular  pad  ;  c,  cornea  ;  cp,  attenuated  tongue-shaped  ciliary 
processes  ;  i,  iris  ;  I,  lens  ;  o,  ora  serrata  ;  on,  optic  nerve  ;  s,  scleral  carti- 
lage ;  V,  ciliary  venous  sinus  ;  z,  position  of  zonule  (from  a  drawing  by 
Rochon-Duvigneaud,  Les  Yeiix  et  la  Vision  des  Vertebres,  Masson  et  Cie). 


is  represented  by  meridional  elements  only,  the  transversalis  muscle 
being  absent  ;  while  the  angle  of  the  anterior  chamber  forms  a  wide 
cleft  spanned  by  an  unusually  large  pectinate  ligament.  In  this 
region  the  branched  ciliary  venous  sinus,  the  analogue  of  the  canal 
of  Schlemm,  is  wholly  embedded  in  the  sclera.  The  anterior  surface 
of  the  iris  is  covered  by  a  thick  layer  of  lipophores  and  guanine-bearing 
iridocytes  giving  this  structure  a  conspicuously  bright  lemon-yellow 
sheen  (Plate  VIII).  The  pupil,  contrary  to  its  behaviour  in  Lacertilians 
and  C'helonians,  is  briskly  I'eactive  both  to  light  and  drugs  (Johnson, 

1  p.  356. 

^   110   ciliary  proces.ses  :    Tiedemaiui,    Oppel    and   Liposchitz,  Xalurgeschichte    der 
A'ni'phibii ,:.  Part  1.     Heidelberg  (1817). 


REPTILES 


377 


1927)  ;  it  contracts  to  a  vertical  slit  which  becomes  narrowed  to  a 
stenopoeic  slit  when  the  animal  basks  in  the  sun.  The  contraction 
time  is  short,  the  dilatation  time  long  (Laurens,  1923).  The  lens  is 
ellipsoidal  in  shape  and  the  annular  pad  small  ;  accommodation  is 
slow  and  its  range  relatively  small. 

In  the  alligator  the  retinal  epithelium  is  modified  in  the  upper  half 
of  the  fundus  to  form  a  tapetum  which  shines  with  a  bright  pinkish- 
orange  glow  ;    in  a  dark-adapted  eye  the  red  shimmer  of  rhodopsin 


Fig.   456. — The  Visual  Cells  of  Crocodilians. 

The  visual  cells  of  the  American  alligator,  Alligator  mississippiensis. 
Reading  from  the  left,  the  elements  are  :  a  single  cone  and  a  double  cone  from 
the  ventral  fundus  ;  a  rod  ;  a  single  cone  and  a  double  cone  from  the  periphery 
of  the  fundus  opposite  the  centre  of  the  tapetum  lucidum  (  X  1,000)  (Gordon 
Walls). 


can  be  seen  ophthalmoscopically  against  the  bright  background  rapidly 
fading  on  exposure  to  light,  a  phenomenon  which  provided  the  first 
demonstration  of  visual  purjile  in  the  living  eye  (AbelsdorfiF,  1898). 
The  retinal  epithelium  in  the  tapetal  area  is  heavily  packed  with 
guanine  crystals  and  does  not  contain  sufficient  fuscin  in  the  cell- 
bodies  or  in  their  processes  to  occlude  the  mirror  effect  of  the  tapetum 
(Kopsch,  1892  ;   Laurens  and  Detwiler,  1921). 

The  visual  cells  resemble  those  of  the  Chelonians  except  that  oil- 
droplets  are  lacking  from  the  cones  (Fig.  456).  The  rods,  however, 
greatly  outnumber  the  cones  (12  to  1  in  the  periphery,  Verrier,  1933) 
and  in  the  tapetal  area  the  cones,  both  single  and  double,  tend  to 
assume  a  slender,  more  rod-like  shape,  forming,  in  Walls's  (1934)  view, 
a  transition  stage  ]iet\\een  the  two  visual  elements.  Near  the  ventral 
border  of  the  tapetum  there  is  a  horizontally  oval  area  centralis, 


378 


THE   EYE   IN   EVOLUTION 


Crocodile 


populated  mainly  by  rods,  in  which  all  the  visual  elements  are  slender 
and  more  closely  packed  than  elsewhere  ;   a  fovea  is  absent. 

The  fundus  seen  ophthalmoscopically  presents  a  uniform  yellow 
background  stippled  with  brownish  pigment  and  orange  dots  in  the 
centre  of  which  is  the  white  circular  optic  disc  with  its  patch  of  dark 
moss-like  pigment  (Plate  VIII).  The  retina  is  avascular  and  is  nour- 
ished from  the  choroid  ;  in  the  crocodile  a  small,  flat  pigmented  glial 
pad  with  one  or  two  capillaries  represents  a  rudimentary  and  function- 
less  conus  ;  in  the  alligator  the  disc  is  devoid  of  vessels  although 
there  are  a  few  capillaries  in  the  optic  nerve  (Mann,  1929).  The  optic 
nerve  is  slender  and  elementary  in  structure  with  no  septal  system. 


Figs.  457  and  458. 
P 


-The  Eye  of  the  Alligator. 


Fig.  457.— (After  Bland-Sutton.) 


Fig.  458.— (After  Franz.) 


A'^.  tendon  of  nictitans  ;  OiV,  optic  nerve  ;   P,  pyramidalis  muscle  ;   i?,  retractor 

bull>i  muscle. 


THE  OCULAR  ADNEXA.  The  lids  are  said  to  be  peculiar  in  that, 
alone  among  Reptiles,  the  upper  is  the  more  mobile,  an  observation, 
however,  which  has  been  questioned  (Prince,  1956).  This  lid  usually 
contains  a  tarsal  plate  of  fibrous  tissue  ;  it  is  fringed  by  a  tough  mem- 
brane split  at  the  margin  into  some  20  broad  pieces  giving  the  appear- 
ance of  a  row  of  exceptionally  thick  eyelashes  which  had  been  glued 
together  and  then  had  their  tips  cut  off.  In  addition  there  is  a  well- 
developed  nictitating  membrane  so  transparent  that 'all  the  details  of 
the  iris  can  be  seen  through  it  with  ease  ;  its  convex  free  border 
is  marked  by  three  or  four  bands  of  brown  pigment  and  the  mem- 
brane itself  is  stiffened  by  a  cartilage.  It  moves  obliquely  backwards 
and  slightly  upwards  controlled  directly  through  a  long  tendon  by  a 
pyramidalis  muscle  corresponding  to  that  in  Chelonians  (Figs.  457-8). 
The  membrane  is  often  moved  across  the  eye  without  the  eyelids  being 
closed  ;  and,  if  the  eyes  are  closed  the  nictitans  is  first  moved  across, 
not  simultaneously  with  the  lids,  as  occurs  in  most  other  Reptiles. 
Both  the  harderian  and  lacrimal  glands  are  well  developed  as  are  the 
conjunctival  glands,  the  latter  associated  with  the  movable  upper  lid  ; 


REPTILES 

just  inside  this  lid  there  is  a  row  of  3  to  8  piincta  leading  to  the  lacrimal 
duct.  In  Crocodihis  'porosiis,  however,  the  lower  lid  is  lined  with 
lacrimal  glands  and  there  is  only  one  punctnm.  In  all  the  Crocodilia 
these  glands  are  said  to  play  a  relatively  small  part  in  the  lubrication 
of  the  eye  ;  as  was  first  pointed  out  by  Rathke  (18G6)  the  secretion 
appears  to  pass  directly  dowai  the  lacrimal  duct  possibly  with  the 
object  of  lubricating  the  food  (Leydig.  1873). 

Xo  signs  of  external  lacrimation  can  be  elicited  even  on  stimulation  of  the 
eye  by  the  instillation  of  such  irritative  solutions  as  the  juice  of  an  onion  mixed 
with  common  salt  (Johnson,  1927).  It  would  appear  that  the  legend  of 
"  crocodile  tears  "  is  a  myth  :  it  will  be  remembered  that  Sir  John  Maunderville 
in  his  TraiJels  {ca.  1400)  accused  this  reptile  of  shedding  hypocritical  tears  in 
sorrow  before  it  devoured  its  victim. 

The  bony  orbit  is  enclosed  and  witliin  it  the  eye  projects  upwards 
so  that  it  remams  above  the  level  of  the  water  when  the  rest  of  the 
head  is  submerged. 

THE    IIHYXCHOCEPHALIAX    EYE 

S'phenodon  {Haiteria)  X)^^nctatns,  the  New  Zealand  "  lizard  "  or 
tuatara.  is  a  veritable  living  fossil  and  the  only  extant  representative 
of  the  Rhynchocephalia  ;  it  is  a  small  olive-green  animal  spotted  with 
yellow  above  and  white  below,  carnivorous  in  habit,  living  a  solitary 


379 


Fig.  459.- 


-Thi:  Tr^'r\R\,  Sput  \oj)o\   (fidtii  15urton\  N/ 
Else\  icr  Pub.  Co.). 


I  of  Animal  Life 


380  THE   EYE   IN   EVOLUTION 

.  nocturnal  life  in  holes  or  burrows  which  it  often  shares  with  a  petrel, 
and  is  found  only  in  some  small  islands  in  the  Bay  of  Plenty  off  the 
coast  of  the  North  Island  of  New  Zealand  where,  however,  it  is  tending 
to  become  extinct  (Fig.  459). 

The  eyeball  as  a  whole,  studied  originally  by  Osawa  (1898)  and 
later  by  Dendy  (1910),  Howes  and  Swinnerton  (1903)  and  Mann 
(1932-33),  resembles  closely  that  of  the  lizard  adapted  for  nocturn- 
ality  ;  its  essential  features  are  the  large  cornea  and  lens,  the  reduced 
accommodative  apparatus,  the  slit-pupil,  the  rod-rich  avascular  retina 
with  feiv  insignificant  cones,  and  the  presence  of  a  fovea. 


Fig.  460. — The  Ciliary  Region  of  Spbenodox. 

A  diagram  from  Walls  showing  cm,  ciliary  muscle  ;  co,  conjunctiva  ; 
cs,  ciliary  venous  sinus  (containing  a  nerve  shown  in  black)  ;  I,  lens  ;  ot,  ora 
serrata  ;   r,  annular  pad  ;   sc,  scleral  cartilage  ;   so,  scleral  ossicles  ;   z,  zonule. 

The  GLOBE  is  large  with  a  marked  sclero -corneal  sulcus  ;  the 
cornea  is  strongly  curved  with  a  thin  two-layered  epithelium  ;  and 
the  sclera  is  provided  with  an  extensive  cartilaginous  cup  and  a  ring 
of  16  to  17  ossicles. 

In  the  choroid  there  are  peculiar  spheroidal  cells,  heavily  pigmented 
and  with  central  nuclei,  which  form  a  dense  aggregation  opposite  the 
fovea.  The  ciliary  body,  like  that  of  the  lizard,  shows  no  ciliary  pro- 
cesses, and  the  circular  ciliary  venous  sinus,  lying  on  the  inner  aspect 
of  the  sclera  at  the  level  of  the  root  of  the  iris,  is  very  large  with  an 
annular  nerve  on  its  posterior  aspect  (Fig.  460).  The  ciliary  muscle 
is  feebly  developed.  The  iris  is  brightly  coloured  with  a  layer  of 
chocolate-coloured  chromatophores  through  the  apertures  of  which 
are   seen   coppery   lipophores   and   silvery   iridocytes  ;     the   vascular 


PLATE  VIII 

The  Eyks  of  Crocodilians  and  Sphkxohon 


'>-,«>', 


JvV^ 


FiQ_  1. — The  iris  of  the  broad-fronted  crocodile,        Fio.    2. — The    iris    of    the    spectacled    cayman, 
Oslmlrfmus  tetraspis  (Ida  Mann).  Caiman  crocdilus  (Ida  Mann). 


"•y^'s'"  ,'  „ 

*'•"•';  ;';,'^'' 

''^  -V. '  '  .'■., 

S"i' 

'\S'r  '' 

/  ,.jll».     \ 

X    -^.^ 

^  ■     ■    ■    .. 

''  ^1^   (  ' 

.'•  •/>'>*"■ 

^  " 

i  S^^^y^   ; 

' '  *  ■'!  . 

;.  ■'^^    ■ 

'  ■  .'  */  '^1 

',',.  ''"^. 

^ 

'■.;-  ;.V 

r'-*;--  ^"  ' 

,     V-'   *    J™  -  ..  •■ 

■  ,•.»,. 

"  *  ■' 

'   i  .     '-'     '^2 

V  -  "^-^    ' 

r.5^V:-'^  • 

Fig.  :;.      '\l)r  fun. his  ,.|   ,  I //;,/,/.'o,>  ,/,, 


I  l.ini  l-.iy  .Idhnsdii). 


Vic.  4. — The  fundus  <ii  Spheiwdoi 
(Lindsay  Johnsim). 


[To /,„■('  p.  381. 


S.O. — VOL.  I 


REPTILES 


381 


pattern  comprises  a  system  of  arcades  running  towards  the  pupillary- 
margin,  some  of  the  vascular  loops  of  which  leave  the  iris  and  float 
freely  in  the  anterior  chamber  (Mann,  1931)  (Figs.  461  and  462). 
The  round  jpwpil  contracts  into  a  vertical  slit,  and  both  circumferential 
sphincter  and  radial  dilatator  muscle  fibres  are  present. 

The  lens  is  large,  making  the  anterior  chamber  shallow  ;  it  is 
more  spherical  than  in  diurnal  lizards  and  the  annular  pad  is  well 
developed.     The  zonular  fibres  are  peculiar  in  that,  arising  from  the 

Figs.  461  and  462. — The  Iris  of  Sphexodox. 


Fig.  461. — Showing  the  vascular  arrangements  (Ida  Mann). 


Fig.  462. — Showing  the  pigmentary  epithehum,  ^4,  tlie  sphincter  mu-scle, 
C,  and  the  peciihar  vascular  arrangements.  Among  the.se,  B  is  an  afferent 
vessel  from  the  ciliary  region,  and  D  is  one  of  the  many  arteries  of  the  iris 
which  float  freely  in  the  anterior  chamber.   £' is  a  nerve  trunk  (Ida  Mann). 


ciliary  body,  they  are  inserted  into  the  posterior  surface  of  the  iris  as 
well  as  into  the  lens,  as  if  the  former  tissue  were  imjjressed  into  the  act 
of  accommodation  by  being  forced  against  the  periphery  of  the  lens 
to  make  the  axial  area  bulge  forward.^ 

The  retina  has  received  a  considerable  amount  of  study. ^  It  is 
completely  avascular  and  a  conus  is  absent  ;  only  a  few  capillaries  are 
evident  forming  a  network  on  the  pale  vertically  elongated  optic  disc, 
to  which  structure  they  are  rigidly  restricted  (Plate  VIII).    Ophthal- 

1  p.  651. 

2  Osawa  (1898-99),  Kallius  (1898),  Virchow  (1901),  Bage  (1912),  Mann  (1932-33), 
Walls  and  Judd  (1933),  Walls  (1934). 


382 


THE   EYE   IN   EVOLUTION 


n«w.i  •/■»'*'* 


c/( 


Fig.  463. — The  Retin.4  of  Sphesobos  in  the  Central  Area. 

Showing   the    shallow    fovea,      r,    retina  ;     ch,    choroid  ;     s,    scleral    cartil 
(  X  90)  (Gordon  Walls). 


moscoiDically  the  fundus  is  reddish-broAvn  witJi  a  stippling  of  golden 
sjiots  whereon  the  arrangement  of  the  white  and  relatively  coarse 
nerve  fibres  is  clearly  delineated  as  they  radiate  uniformly  outwards 
from  the  optic  disc.  Three  visual  elements  are  present,  the  majority 
of  which  were  interpreted  by  the  older  writers  as  cones  and  are  still 
held  to  be  such  by  observers  such  as  Vilter  (1951)  who  found  a  rela- 
tionship between  the  receptor  and 
ganglion  cells  of  1  :  1,  as  in  the  lizard. 
Walls  (1934).  on  the  other  hand, 
claimed  that  the  prej)onderant  visual 
cells  are  rods  with  enlarged  and  sturdy 
outer  segments,  homologous  with  the 
cones  of  Clielonians  and  Crocodilians  ; 
single  and  double  elements  are  present 
in  approximately  equal  numbers,  with 
colourless  oil-droplets  in  the  former  and 
in  one  component  of  the  latter  (Walls 
and  Judd,  1933).  The  third  type  of 
cell,  a  small  and  ill- formed  cone  without 
an  oil-droplet,  is  sparse  and  absent  from 
the  fovea  (Fig.  464).  The  central  fovea 
is  shallow  but  well-formed,  and,  if 
Walls's  interpretation  is  accepted,  shares 
with  that  of  a  gecko ,  ^  and  some  noctii  rnal 
primates,-  the  distinction  of  being  the 
1  p.  365.  -  p.  486. 


> 


Fig.   404.- 


-The  Visual  Cells   of 

SpHEyoDOX. 

A  sinalf  "rod",  a  double  "rod"  and 
a  cone   (       1,000)    (Gordon   Walls). 


REPTILES 


383 


only  rod-fovese  in  terrestrial  Vertebrates  (Fig. 
463). 1  The  optic  nerve,  like  that  of  Crocodilians, 
is  slender  and  simjole  in  architecture  without  a 
septal  system. 

THE  OCULAR  ADNEXA  resemble  closely 
those  of  the  lizard,  but  the  tendon  of  the  nicti- 
tating membrane  slips  round  a  sling  formed 
by  the  unusually  large  two-headed  retractor 
bulbi  nniscle,  to  find  insertion  into  the  orbital 
wall.  The  lacrimal  gland  is  lacking  but  a 
simple  harderian  gland  is  present.  In  contrast 
to  that  of  the  lizard,  the  orbit  is  enclosed  with 
sturdy  temporal  arches. 


Fig.  465. — The  Poster- 
ior Segment  of  the 
Globe    of    Sphesodox. 

B  and  R,  the  two  heads 
of  the  retractor  bulbi 
muscle  ;  A',  tendon  of 
nictitans  ;  ON,  optic 
nerve  (after  Franz). 


THE    OPHIDIAN    EYE 

THE  OPHiDiA  (snakes  or  SERPENTS),  Hmbless  reptiles  having  no 
pectoral  and  never  more  than  a  hint  of  a  pelvic  girdle,  are  of  widespread 
distribution  j)articularly  in  the  trojDics  ;  most  are  terrestrial,  a  few 
amphibious,  and  many  habitually  marine.  Although  many  genera 
exist,  the  eyes  of  all  snakes  are  very  alike — apart  from  the  Typhlopidae, 
degenerate  creatures  generally  smaller  than  earthworms  and  sub- 
terranean in  habit  which  have  vestigial  eyes.^ 

Curiously,  however,  the  ophidian  eye  is  extremely  unlike  that  of 
all  other  Reptiles  in  almost  every  particular.  There  is  no  scleral 
cartilage  or  ossicles  ;  the  iris  vasculature  forms  an  indiscriminate  iietivork 
and  its  striated  muscnlature,  ectodertnal  in  other  Reptiles,  is  replaced  by 
mesodermal  fibres  derived  from  the  ciliary  region  ;  the  ciliary  venous  sinus 
is  corneal  in  location  ;  the  lens  possesses  sutures  and  an  anterior  annular 
pad,  and  since  it  is  divorced  from  the  ciliary  body,  a  new  method  of 
accommodation  has  been  invented  depending  on  pressure  transmitted  to 
the  vitreous  ;  the  retina  has  no  conus  papillaris  but  a  membrana  vasculosa 
retince  ;  the  visual  elements  are  distinctive  and  varied  in  their  type  ;  and 
the  thick  optic  nerve  is  fascicular,  each  bundle  being  provided  with  an 
axial  core  of  ependymcd  cells. 

It  would  at  first  sight  seem  strange  that  the  eyes  of  snakes  should 
be  unique  and  so  profoundly  different  from  those  of  other  Reptiles, 
particularly  lizards  from  wliich  the  Ophidia  are  directly  derived.  It 
would  appear,  indeed,  as  was  suggested  by  Walls  (1942)  and  maintained 
by  Bellairs  and  Underwood  (1951),  that  the  first  snakes,  derived  from 
burrowing  lizards,   lived  a  nocturnal  existence  underground  during 

1  Compare  the  ill-formed  temporal  fovea^  of  the  deep-sea  Teleosts,  Bathyirocies 
and  Balhi/Iar/us  which  also  contain  rods,  p.  310. 

2  p.  731. 


384  THE   EYE   IN   EVOLUTION 

which  period  their  eyes  lost  most  of  the  speciaHzed  adaptations  found 
in  Lacertihans  and  became  degenerate  ;  on  emerging  again  above 
ground  it  became  necessary  for  them  to  be  reconstituted  anew  so  that 
devices  of  their  own  were  invented  to  compensate  for  those  lost  in  the 
dark  subterranean  phase  of  their  existence.     That  snakes  developed 


Fig.    4G6. — The      Head      of     the     Gtiass     Snaxk     Tropiboxotus    satkix 
KATRix  (Katharine  Tansley). 


Fig.  467. — The  Head  of  the   }'\  ihun',  Spiluteh   \-Aiiit.i,ATL  -. 
■    .' .  To  show  the  spectacle  (O'Day). 

eyes  quite  unlike  those  of  all  other  Reptiles  is  readily  understandable 
in  terms  of  this  hypothesis.  Indeed,  that  they  approach  so  nearly  the 
standard  vertebrate  pattern  after  the  tremendous  feat  of  reconstituting 
themselves  after  near-extinction  is  more  surprising  than  that  they 
differ  so  markedly  from  their  near  relations  ;  the  fact  that  they  did  so 
is  a  li'ibute  to  the  adaptability  of  the  vertebrate  eye  and  the 
biological  utility  of  its  general  organization. 


REPTILES 


385 


The  GLOBE  OF  THE  EYE  is  tj^icallv  sj^lierical  or — for  the  first  time 
among  Vertebrates — sliglitly  elongated  in  the  direction  of  the  visual 
axis.  The  sclera  is  composed  entirely  of  connective  tissue  without 
cartilaginous  or  osseous  supports,  varymg  considerably  in  thickness 
among  the  different  families  but  usually  tliinnest  about  the  ec-[uator 
where  it  is  most  deformed  during  accommodation.  Usually  its  outer 
surface  is  jjigmented  with  melanojjhores.  typically  forming  a  dotted 
pattern,  sometimes  a  continuous  layer,  and  occasionally  {Python)  the 

Figs.  468  and  469.— The  Ophidian  Eye. 


Fig.  468. 


Fig.  469. 


Fig.  468. — Diagram  of  an  ophidian  eye.  .4,  anterior  pad  ;  Ch,  choroid  ;  CR, 
ciliary  roll  ;  CV,  circular  vein  ;  MA,  muscle  of  accommodation  ;  MV, 
n:iembrana  vasculosa  retinae  ;  ON ,  optic  nerve  ;  PL,  pectinate  ligament  ; 
Sc,  sclera  ;   SM,  sphincter  muscle  ;    VS,  ciliary  venous  sinus  ;    Z,  zonule. 

Fig.  469. — The  eye  of  the  tiger  snake,  NotecJiis  (Norman  Ashton). 


whole  thickness  of  the  sclera  contains  pigment  cells.  The  cortiea,  with 
its  delicate  single-layered  epithelium  protected  by  the  "  spectacle  "  ^  and 
without  a  Bowman's  membrane,  continues  the  arc  of  the  sclera  and 
usually  shows  a  peculiar  thickening  at  the  corneo -scleral  margin 
(Fig.  470). 

The  choroid  is  unusually  thin,  the  tenuous  capillary  layer  in  most 
species  ajDj^earing  as  if  it  were  fused  with  the  sclera  (Fig.  471).  The 
ciliary  region  starts  with  a  narrow  orbicular  zone  comprised  of  the  two 
layers  of  the  tall  ciliary  ei^ithelium  (absent  in  the  boas :  the  common 
boa,  Constrictor,  the  rubber  boa,  Charina),  anterior  to  wliich  the  roll- 
like  ciliary  body  rises  abruptly  as  an  annular  fold  wherein  the  ciliary 


1  p.  266,  Fig.  279. 


S.O. — VOL.   I. 


386 


THE   EYE   IN   EVOLUTION 


epithelium  caps  a  ])ad  of  highly  vascular,  deejjly  pigmented  uveal 
tissue  (Fig.  470)  ;  from  this  ciliary  roll  strands  of  fibrous  tissue 
run  forwards  across  the  angle  of  the  anterior  chamber  to  find  insertion 
in  the  peripheral  corneal  thickening.  The  circumferential  ciliary 
venous  sinus  is  usually  corneal  in  location  separated  from  the  anterior 
chamber  by  connective  tissue  and  draining  backwards  into  the  uveal 
veins  of  the  ciliary  region  (Fig.  472).    Individual  variations,  however. 


Fig.  470. — The  Anterior  Se(3ment  of  the  Eye  of  the  Tiger  Snake. 

Externally  is  the  sjDectacIe,  s,  beneath  which  the  cornea,  c,  is  seen  with 
the  peculiar  thickening  at  its  limbal  margin.  Between  s  and  c  lies  the  closed 
conjunctival  sac.  I,  lens.  The  ciliary  roll,  cr,  is  a  marked  feature  and  above 
it  is  seen  the  ]ioctinate  ligament  traversing  the  angle  of  the  anterior  chamber 
immediately  above  which  is  the  large  ciliary  venous  sinus  within  the  corneal 
limbus  (  X  53)  (Norman  Ashton). 


C'ohra 


occur  particularly  among  the  Boidae  ;  in  Python,  for  example,  it  is 
situated  close  to  the  outer  surface  of  the  cornea  and  drains  into  the 
sulK-onjunctival  veins,  and  in  Constrictor-  and  the  sand-boa,  Eryx, 
it  is  absent. 

The  iris  is  a  thick  and  relatively  massive  tissue  heavily  pigmented 
vvith  melanophores,  lipojahores  and  iridocytes.  As  a  rule,  however,  the 
resultant  colour-scheme  is  relatively  dull  and  compared  with  many 
other  Rej)tiles  the  variations  are  small,  the  jDreponderant  colours  being 
browns  and  yellows  sometimes  with  a  metallic  sheen  ;  quite  often  the 
colour-pattern  of  the  skin  is  continued  in  the  eye  (Plate  IX). 

Thus  in  the  cobras  (Elapid;e)  the  iris  is  brownish-yellow  speckled  with  gold  ; 
ill  the  corn-snake,  Coluber  guttatus,  orange-red  ;   in  Python,  brown  with  a  metallic 


PLATE  IX 

The  Irides  of  Snakes 
(Ida  Mann) 


Fig.  1. — Royal  i)\-tli(in.  /'i/llion  rcijiiis 


Fig.  3. — Kmih    im-     nake,  Elaplie 
qaiUuuiii  tmiitd. 


Fig.    2. — Roticulated    python,    Pythoit, 

retic/ilatiis. 


Fjg.  4. — J31ack-and-g(jW  trL-L'--^nake.  Boii/u  dcii- 
drophiln.  The  edges  of  the  brown  and  yellow 
scales  below  the  eye  are  seen. 


Fig.  .5. — Emerald  tree-snake.  Passciita  pni-siiin. 
A.  right  eye;  aphakic  area  on  right.  The 
outline  of  the  lens  can  be  seen.  The  green 
scales  surrounding  the  eye  are  shown.  JJ,  the 
shape  of  the  pupil  when  contracted. 


Fig.  (). — Chieken-snake,  FJaplin  ijiHidr/r/llata. 
The  edges  nf  the  scales  bordo'inu  the  eye  are 
also  shown. 


[To /lire  p.  386. 


REPTILES 


387 


silver  sheen  (Plate  IX,  Figs.  1  and  2),  In  many  sjjecies  a  clear-cut  differentiation 
in  colour  occurs — brown  and  gold  in  the  king -snake,  Lampropeltis  getulus,  silver 
and  gold  in  the  black-and-go Id  tree-snake,  Boiga  dendrophila  (Fig.  4).  A  bright 
yellow  pattern  is  seen  in  the  four-line  snake,  Elaphe  quatnorUneata  (Fig.  3),  a 
silver  appearance  in  the  painted  tree -snake.  Ah  oetulla  picta,  and  in  the  chicken- 
snake,  Elaphe  quadrivittata  (Fig.  6). 

TJie  vascular  pattern  of  the  iris  is  j^ec^^iHar  and  unique  (Mann. 
1931).  The  most  j^rimitive  tj^Des  (Boidte)  show  a  fairly  well  defined 
arrangement  of  vessels  somewhat  resembling  that  seen  m  geckos.    This 


4: 


->^li*'^  j'i:€^'  flf,Tv^i^^^-f:l/*€[:*i»^'''^'^^ 


Fig.   471. — The   Posterior  ."Segment  of  the   globe   of  the   Copperhead 

Snake. 

r,  retina  ;  p,  j^igmentary  epithelium';  ch,  choroid  which  became  detached 
from  the  pigmentary  epithelium  ;  s,  fibrous  sclera  ;  v,  a  vessel  of  the  mem- 
brana  vasculosa  retinte  (  X  240)  (Xorman  Ashton). 


is  most  ajjparent  in  the  pj^thons  (Plate  IX,  Figs.  1  and  2)  ;  two  main 
arteries  enter,  one  on  either  side,,  and  run  to  the  pupillary  aperture 
round  which  they  supj^ly  a  narrow  circumpupillary  jjlexus  wliile  the 
rest  of  the  iris  is  occupied  by  an  intermediate  network  of  vessels.  In 
most  other  .snakes  the  walls  of  the  vessels  are  ojsaque  so  that  no  blood- 
flow  can  be  made  out  ;  moreover,  they  are  heavily  obscured  by  j^igment 
and  are  arranged  in  so  haphazard  a  marmer  that  the  interpretation  of 
the  vascular  arrangements  is  difficult. 

The  musculature  of  the  iris  is  mesodermal  and  derived  from  the 
ciliary  region.  Circular  fibres  predommate,  being  concentrated  into 
two  accumulations,  one  near  the  pupil  to  form  a  relatively  comjjact 
mass  acting  as  a  sphincter,  the  other  at  the  root  acting  as  a  muscle  of 


Cop]3crhead 
(crotalid  snake) 


388 


THE   EYE   IN  EVOLUTION 


accommodation  ;  the  dilatator  fibres  lie  beneath  these  and  rmi  radially 
towards  and  sometimes  into  the  ciliary  body.  The  pupils  are  usually 
very  active  since  they  assume  the  light-protective  function  in  the 
absence  of  movable  lids  ;  in  some  types,  however,  the  contraction  is 
slight  {Pytho7i)  or  even  absent  (the  European  grass-snake,  Trojndonotus 
natrix  ;  the  Madagascar  sharjj-nosed  snake,  Heterodon  madagas- 
cariensis).  Probably  because  of  the  imjDermeability  of  the  corneal 
spectacle,  the  instillation  of  miotic  or  mydriatic  drugs  is  without  effect 
(Johnson,  1927).    In  nocturnal  and  burrowing  snakes  (with  few  excep- 


FiG.    472. — The    Ciliary    Reuion    of   the    Grass    Snake,    T/toPinoyoTUs 

.\Arji/x  yATRix. 

Showing  cr,  ciliary  roll  ;    o,  ora  serrata  ;    va,  hyaloid  venous  arc  ;    vs,  ciliary 

venous  siiuis  {  X   108)  (Katharine  Tansley). 


tions  such  as  the  coral  snake,  Elups),  the  constricted  aperture  is  a 
vertical  slit  or  ellipse  ;  in  diurnal  types  it  is  circular  except  in  some 
Asian  and  African  tree-snakes  (Opisthoglyi^hs). 

In  these  (the  East  Indian  long-nosed  tree-snake,  Dryophis,  and  its  relative 
Dryophio])s,  the  African  bird-snake,  Thelotornis,  and  the  emerald  tree-snake, 
Passerita)  the  pupil  is  a  horizontal  slit  shajaed  like  a  key-hole  with  the  slot  of 
the  key-hole  extending  on  the  nasal  side  almost  to  the  limbus,  weW  beyond  the 
equator  of  the  lens.  As  occurs  in  many  teleostean  Fishes,^  the  pupil  thus  shows 
a  phakic  and  an  aphakic  area  (Fig.  808).  On  contraction  of  the  pvipil  the  central 
part  closes  completely  leaving  two  small  pvipillary  apertures,  a  larger  temporal 
(phakic)  and  a  smaller  nasal  (aphakic)  aperture.  It  is  significant  that  at  least 
in  some  of  these  snakes  a  temporal  fovea  occurs  and  their  vision  is  said  to  be 
veiy  acute  (Plate  IX,  Fig.  5). 

'i'be  lens  is  subspherical  (1- 1-1-25),  is  firmer  in  consistency  than 
in  ot:      Heptiles.  is  provided  with  sutures,  and  instead  of  an  equatorial 

1  p.  304. 


REPTILES 


389 


annular  pad.  there  is  a  region  on  the  anterior  surface  (except  in  BoicW) 
where  the  subcapsular  epithelial  cells  instead  of  being  cuboidal  are 
elongated  to  form  an  anterior  pad  (Fig.  468).  In  most  diurnal  types 
the  whole  structure  is  pigmented  yellow  (Rabl.  1898  ;  Hess,  1912  ; 
Walls,  1931).  The  zonule  consists  of  two  systems  of  fibres,  one  running 
from  the  anterior  surface  of  the  ciliary  roll  to  the  anterior  surface  of 
the  lens,  the  other  from  the  posterior  surface  of  the  ciliary  body  to  the 


"^-«.0m%^Sffi 


WftfftffHiiiiliffffff 


¥iG.    -t73. — The 


iioriiiijsoT  r 


Ketixa    of    the    Grass    Sxake.    T ik 

XAritix. 

The  pure-cone  retina  of  a  dinrnal  snake.      1.  optic  ner\-e  fibre  layer  ;    2, 

ganglion  cell  layer  ;    .3,  inner  plexiform  layer  ;    4,  inner  nuclear  layer  ;    .■>,  outer 

plexiform  la,\-er  ;    6,  outer  nuclear  layer  ;    7.  external  limiting  membrane  ;    8, 

cones  ;    9,  pigmentary  epithelium  (  ;■    330)  (Katharine  Tansley). 

posterior  surface  of  the  lens  ;  except  in  the  boa.  Emcrates,  there  are 
no  intermediate  fibres  attaching  to  the  equatorial  region  between  these 
two  systems.  Accommodation  is  effected  by  a  unique  mechanism  cpiite 
different  from  that  seen  in  other  Reptiles. ^ 

The  fundus  oculi  seen  ophthalmoscopically  presents  a  remarkably 
constant  picture  (Johnston,  1927)  (Plate  X.  Figs.  1  and  2).  The  back- 
ground is  grey  mottled  with  spots,  usually  white  (as  in  the  corn-snake. 
Coluber  guftatus)  or  red  (as  in  the  Boidse).  and  the  semi-opaque  nerve 
fibres  radiating  uniformly  from  the  optic  disc  are  consi)icuous.     Occa- 

1  p.  64S. 


390 


THE   EYE   IN  EVOLUTION 


L;a?je-T 


W; 


5^'--^.; 


sionally,  particularly  in  the  Indian  python,  Python  molurus,  choroidal 
vessels  somewhat  resembling  those  seen  in  the  human  eye  are  evident 
in  the  periphery  of  the  fundus.     The  optic  disc  is  always  round  and 

white,  although  it  varies  much  in 
size  ;  that  of  the  water-snake, 
Trojpidonotus  fasciatus,  is  enormous, 
exceeding  in  size  that  of  any 
Vertebrate  with  a  circular  disc,  even 
that  of  the  whales  in  which  the  eye 
may  reach  a  diameter  of  5|  inches. 
Usually  on  the  surface  of  the  disc 
there  is  some  melanin  pigment,  some- 
times in  small  quantity  (Boidse), 
sometimes  associated  with  a  cushion 
of  mesoderm,  resembling  the  ap- 
pearance seen  in  Crocodilians 
(Beauregard,  1876  ;  Kopsch,  1892  ; 
Leplat,  1922  ;  Jokl,  1923).  This,  re- 
presenting the  remains  of  mesoderm 
entering  with  the  hyaloid  vessels,  is 
functionless  and  is  not  homologous 
with  the  neuroglial  conus  of 
lizards  although  in  certain  species 
it  may  project  into  the  vitreous  to 
form  a  very  similar  structure  (pig- 
mented in  the  British  adder,  Vipera 
berus  ;  colourless  in  the  king-snake, 
Lamprojjeltis).  The  remains  of  the 
hyaloid  vasculature,  however,  form 
a  well-defined  system  of  vessels,  three 
and  sometimes  four  of  which  emerge 
through  the  disc  from  the  optic  nerve. 
In  some  species  these  are  small  and 
are  apparent  only  a  short  distance 
from  the  disc  (Boidae)  ;  more  usually 
arteries  of  considerable  size  run 
nasally  and  temporally,  drain  into  two 
venous  arcs  which  encircle  the  globe  in  the  region  of  the  orbiculus,  and 
combine  to  form  a  hyaloid  vein  which  runs  backwards  in  the  fundus  mid- 
ventrally  to  leave  the  eye  at  the  optic  disc.  Over  the  surface  of  the  retina 
lying  in  the  vitreous  there  is  a  membrana  vasculosa  of  very  fine  capil- 
laries (Fig.  471)  (Hyrtl.  1861  ;  Virchow,  1901  ;  Szent-Gyorgyi,  1914); 
onl\-  ■■  the  colubrid  snake,  TarbojjJiis,  are  these  known  to  penetrate 
the  1-       a  itself.^ 

'   Cf.  the  direct  \-asculai'ization  of  the  retina  of  the  eel,  p.  300. 


D 


■->  Vf  w 


v< 


Fig.  474.— The  Retina  or  Leptodeira 

A.W PLATA. 

The  mixed  retina  of  a  nocturnal 
snake.  1,  optic  nerve  layer  ;  2,  gan- 
glion cell  layer  ;  3,  inner  plexiforni 
layer  ;  4,  inner  nuclear  layer  ;  5,  outer 
plexiform  layer  ;  6,  outer  nuclear 
layer  ;  7,  external  limiting  membrane  ; 
8,  visual  cells  (above  are  rods,  and 
below  cones  ;  D,  double  cone  ;  S, 
single  cone)  (  X  500)  (Gordon  Walls). 


PLATE  X 

The  Fuxdi  of  Snakes 

(Lindsay  Johnson) 


l-'iG.  L — J  he  sharp-nosed  snake,  Hrtirodon  waiiaiinscd)  ientu^ 


Fig.  2. — The  Imhan  cobra.  y<ij(i  tn'pxdians. 


3.0. — VOL.  I. 


[  To  face  p.  ."OO. 


Figs.  475  to  480.— The  Visual  Cells  of  Snakes  (x  1,000)  (Gordon  Walls). 


Fig.  47.5.— The  3  cone-types  (A,  B,  C) 
constituting  the  fundamental  pattern  in 
diurnal  forms  (drawn  from  the  European 
grass  snake,   Tropidonotus  natrix). 


Fig.    477. — Visual  cell   types   of  scotopic 
colubrids. 


Fig.  479. — \isuai  cell  types  of  the  African 
puff-adder,  Bitis  arietans  (strongly 
nocturnal  in  habit).  The  Type  C  (rod) 
is  the  most  abundant  element. 


Fig.  476. — The  3  rod-types  in  the  spotted 
night  snake,  Hypsiglena. 


P'iG.  478. — Visual  cell  types  of  the  crota- 
lids.  Type  C  is  a  rod  containing 
rhodopsin. 


Fig.  480. — Visual  cell  types  of  the  Cape 
viper,  Causus  rhomheatus  (crepuscular 
in  habit).  There  are  two  variations  of 
TyjDe  C,  Type  C  (rod)  being  most 
abundant. 


392 


THE   EYE   IN   EVOLUTION 


Head  of 

Dasypeltis 


Head   of   the 
horned  viper 


Head  of  the 
puff  adder 


The  retina  has  the  usual  vertebrate  structure  (Figs.  473-4),i  but 
the  visual  elements  show  a  remarkable  variation  which  has  been  most 
thoroughly  studied  and  integrated  by  Walls  (1932-42)  (Figs.  475-80). 
In  the  primitive  Boidse  (boas,  pythons,  etc.)  two  elements  only  are 
present,  rhodopsin-bearing  rods  and  single  cones  without  oil-droplets 
or  paraboloids.  In  most  Colubridae,  on  the  other  hand,  the  retina  con- 
tains cones  only,  three  types  being  present — Type  A,  a  stumpy,  fat, 
single  cone  ;  Type  B,  a  double  cone  ;  and  Type  C  with  the  structure  of 
the  single  cones  of  the  boids.  In  diurnal  colubrids  and  elapids  (cobras), 
the  relatively  poor  C-cone  is  eliminated  ;  in  nocturnal  varieties  all 
three  elements  become  more  slender  and  in  some  the  C-cone  contains 
rhodopsin  and  becomes  a  rod  {Tarbophis,  the  egg-eating  snake, 
Dasypeltis,  etc.).  In  the  vipers  (Viperida^^)  the  same  change  has  occurred 
but  some  C-cones  remain,  while  others  appear  as  rods,  four  elements 
thus  being  present  ;  while  in  the  Crotahdse  (rattle -snakes,  moccasins) 
the  rods  greatly  outnumber  the  cones.  It  is  interesting  that  in  some 
forms  these  four  elements  are  all  distinctive  (the  puff-adder,  Bitis 
arietans)  while  in  others  (the  common  British  adder,  Vipera  berus)  the 
transmutation  from  the  Type  C  cone  to  its  rod-form  is  seen  in  all 
gradations. 

As  we  have  noted,  a  temi^oral  fovea  occurs  in  certain  tree-snakes  (Drtjnphis)  ^ 
and  in  the  African  bird-snake,  Thelotornis  kirtlandi  (comjiare  Fig.  807). 

The  optic  nerve  is  primitive  in  its  construction  unlike  that  of  all 
other  Reptiles  and  resembling  that  of  the  dipnoan,  Neoceratodus,^  the 
fibres  being  compactly  segregated  by  septa  into  fasciculi  each  with  a 
central  ependymal  core  (Prince,  1955).  Afferent  fibres  are  present,  and 
although  the  majority  of  fibres  cross  at  the  chiasma,  some  uncrossed 
fibres  are  present  which  terminate  in  the  lateral  geniculate  nucleus 
{Natrix  {Tropldonotus)  natrix,  Armstrong,  1951  ;    Prince,  1955). 

THE  OCULAR  ADNEXA.  Although  snakes  are  popularly  considered 
Hdless,  the  eyelids  are  present  but  have  fused  over  the  eye  to  form  a 
hard  and  horny  "  spectacle  "  *  fitting  over  the  globe  like  a  contact 
lens  and  separated  from  the  cornea  by  a  closed  conjunctival  sac.  This 
structure  has  excited  interest  from  early  times  (Blumenbach,  1788  ; 
Soemmerring,  1818)  and  has  been  fully  discussed  by  Schwarz-Karsten 
(1933)  and  Walls  (1934).  The  nictitans,  at  one  time  assumed  to  form 
the  spectacle,  is  absent.  Embryologically,  as  in  all  Vertebrates,  the 
hds  develop  as  a  lid-fold  without  commissures  surrounding  the  eye, 
but  in  snakes  this  fold  gradually  grows  over  the  cornea,  the  palpebral 
aperture  at  the  same  time  closing  and  moving  dorsally  as  it  does  so  ; 
ihe  lower  lid  thus  takes  the  greatest  share  in  the  process.     Closure  is 

■■  Leydig  (1853),  Hulke  (1864),  Schultze  (1866-67),  Hoffmann  (1876),  Heinemann 
(i  Franz  (1913),  Verrier  (1933).  Kahmann  (1933). 

■.  388.  3  p.  314.  *  p.  266. 


REPTILES  393 

usually  effected  before  birth,  but  in  the  uropeltid  snake,  Rhinophis,  a 
small  slit-like  palpebral  aperture  is  still  present  at  that  time.  The 
spectacle  is  quite  insensitive  so  that  in  time  it  gets  scratched  and  dull  ; 
Johnson  (1927)  found  that  it  could  be  touched  and  even  polished  with 
a  cloth  in  order  to  get  a  view  of  the  fundus  without  any  signs  of 
inconvenience  or  resistance  on  the  part  of  the  animal,  even  in  resentful 
species  like  the  cobra  or  python. 

When  the  snake  sheds  its  skin  the  milky  layer  which  forms  under  the  stratum 
corneum  throughout  the  body  is  very  obvious  through  the  transparent  spectacle  ; 
and  with  the  skin  the  spectacle  is  also  shed,  leaving  a  free  ragged  border  on  its 
inner  surface  where  it  was  attached  at  the  sclero- 
corneal  junction.     So  tough  is  this  thin  layer  of 
skin    (0-1    mm.    thick)   that    it   still   retains  its 
hemispherical  form  after  it  has  been  discarded  ; 

meantime,  the  snake  lies  sluggish  and  irritable       /^       J_^  ^..rJ^^*,^^^  /  •' 

and  seeks  no  food. 


Fig.    481.— The   Harderian 


It    is    curious    that    in    snakes    the 
lacrimal  gland  (associated  with  the  lids)  is 

absent,  but  the  harderian  gland  (usually  Duct  of" a" Snake! 

associated  with  the  nictitating  membrane)  E,  the  eye  ;  H,  harderian 
is  present.  The  latter  is  very  large  and  its  f^^^^  Be/a:irsf  """""^^""^  °'^^" 
oily  secretion  flows  into  the  closed  con- 
junctival sac  and  from  its  nasal  corner  drains  into  the  nose  through  a 
single  naso-lacrimal  duct  which  empties  (as  in  lizards)  inside  the 
vomero-nasal  organ  of  Jacobson  (Bellairs  and  Boyd.  1947-50)  ;  thence 
it  flows  into  the  mouth  where  it  acts  as  an  accessory  salivary  secretion, 
lubricating  the  unchewed  prey  as  an  aid  to  the  difiicult  act  of  swallow- 
ing the  enormous  mouthfuls  of  food  habitual  to  the  snake  (Fig.  481). 

Underneath  the  spectacle  the  eyes  of  snakes  are  freely  movable, 
but  spontaneous  movements  are  not  marked.  The  bursalis  and 
retractor  bulbi  are  absent  (Nishi,  1938).  The  movements  of  the  two 
eyes  are  independent  except  for  convergence,^  and  as  a  general  rule 
in  order  to  obtain  a  view  of  an  object  reliance  is  placed  on  the  pendulum- 
like movements  of  the  head  as  it  is  swmig  from  side  to  side  rather 
than  upon  movements  of  the  eyes. 

Apart  from  the  primitive  boas  and  pythons,  the  orbit  of  snakes  is 
open  and  fenestrated,  in  keeping  with  the  general  lightness  of  the 
architecture  of  the  skull  ;  in  contrast  to  Lacertilians  there  is,  however, 
a  well-formed  optic  foramen.  Temporal  arches  and  a  zygomatic  bone 
are  absent,  probably  to  facilitate  the  wide  gape  of  the  jaws. 

Abelsdorff.    Arch.  Anat.  Physiol,  Physiol.      AneHi.     i?/c.  Mor/o?.,  15,  233  (1936). 

Abt.,  155  (1898).  Armstrong.    J.  Anat.,  85,  275  (1951). 

Albers.      Denkschriften    K.    Akad.    Wiss.      Bage.      Quart.    J.    micr.    Sci.,    57,     305 

Miinchen,  81  (1808).  (1912). 

1  See  p.  695. 


394 


THE   EYE   IN   EVOLUTION 


Beauregard.    Ann.  Sci.  nat.  Paris  (Zool.), 

4,  70  (1876). 
Beer.    Pfliigers  Arch.  ges.  Physiol.,  69,  507 

(1898). 
Bellairs  and  Boyd.    Proc.  zool.  Soc.  Lond., 

117,  81  (1947)  ;    120,  269  (1950). 
Bellairs  and  Underwood.     Biol.  Rev.,  26, 

193  (1951). 
Blumenbach.    Voigt's  Mag.  fi'ir  d.  Neueste 

aus  d.    Physik  u.   Nafurgesch.,   5,    10 

(1788). 
Brucke.    Arch.  Anat.  Physiol.,  370  (1846). 
Chievitz.    Arch.  Anat.  Physiol.,  Abt.  Anat., 

Suppl.,  139  (1889). 
Cords.    Z.  Anat.  Entuick.,  65,  277  (1922). 
Cott.      Adaptive  Colouration    in   Animals, 

London  (1940). 
Dendy,     Philos.  Trans.  B,  201,  227  (1910). 
Detwiler.     J.  exp.  Zool.,  20,   165  (1916)  ; 

37,  89  (1923). 
J.  comp.  Neurol,  36,  125  (1923). 
Vertebrate  PhotorecejJtors,  N.Y.  (1943). 
Detwiler  and  Laurens.     J.  com}).  Neurol., 

32,  347  (1920). 
Evans  and  Minckler.    J .  comp.  Neurol.,  69, 

303  (1938). 
Franz,      v.    Oppel's  Lhb.    d.    vergl.    mikr. 

Anat.  d.  Wirbeltiere,  Jena,  7  (1913). 
Bolk's  Hb.  d.  vergl.  Anat.  d.  Wirbeltiere, 

Berlin,  2  (ii),  1093  (1934). 
Fritzberg.      Arch,   vergl.   Ophthal.,   3,    292 

(1912). 
Gillett.     Amer.  .J.  Ophthal.,  6,  955  (1923). 
Heinemann.     Arch.  mikr.  Anat.,  14,  409 

(1877). 
Hess.     Winterstein's  Hdb.  vergl.  Physiol., 

Jena,  4,  1  (1912). 
Hoffmann.      Niederl.    Arch.    Zool.,    3,    1 

(1876). 
Howes  and  Swinnerton.     Trans,  zool.  Soc. 

London,  16,  1  (1903). 
Hulke.     Roy.  Lond.  ophthal.  Hasp.  Rep., 

4,  243  (1864). 
Hyrtl.   S.  B.  Akad.  wiss.  Wien.,  43  (1861). 
Johnson.       Philos.    Trans.    B,    215,    315 

(1927). 
Jokl.     Z.  Anat.  Entwick.,  68,  523  (1923). 
Kahmann.       Zool.    Jb.,    Abt.    allg.    Zool. 

Physiol.,  52,  295  (1932). 
Zool.  Anz.,  102,  177  (1933). 
V.    Graefes     Arch.    Ophthal.,    135,    265 

(1936). 
Kallius.    Anat.  Anz.,  14,  623  (1898). 
Konig.      Jena.    Z.    Naturwiss.,    69,    223 

(1934). 
Kopsch.       Iris     u.     Corpus     ciliare     des 

Reptilienauges,  Berlin  ()892). 
Krause,  W.     Z.  rat.  Med.,  20,  1  (1863). 

Int.  Mschr.  Anat.  HistoL,  10,  12  (1893). 
Lasker.      Jena.     Z.    Naturwiss.,    69,     15 

(1934). 
Laubc;      (Traefe-Saemisch  Hb.  ges.  Augen- 

hf         Leipzig,  II,  1  (2),  Kap.  3  (1931). 
Lauren        Imer.  J.  Physiol.,  64,  97  (1923). 


Laurens  and  Detwiler.     J.  exp.  Zool.,  32, 

207  (1921). 
Leblanc.     C   R.  Acad.  Sci.    (Paris),  179, 

996  (1924). 
Btdl.   Soc.    Hist.    nat.    de    I'Afrique    du 

Nord,  16,  49  (1925). 
Leplat.     Bull.  Acad.  belg.  CI.  Sci.,  7,  748 

(1921). 
C.  R.  Ass.  Anat.,  17,  195  (1922). 
Leydig.    Anat. -hist.  Untersuch.  fiber  Fische 

u.  Reptilien,  Berlin  (1853). 
Arch.  mikr.  Anat.,  9,  598  (1873). 
Loewenthal.      Arch.    Anat.,    Paris,    20,    1 

(1935)  ;    21,  315  (1936). 
Mann.     Trans,  ophthal.  Soc.  U.K.,  49,  353 

(1929). 
Trans,  zool.  Soc.  London,  21,  355  (1931). 
Proc.  roy.  Soc.  Med.,  25,  834  (1932). 
Brit.  J.  Ophthal,  17,  1  (1933). 
Mercanti.     Arch.  ital.  Biol,  4,  195  (1883). 
Mertens.    Natur  u.  Volk,  84,  184  (1954). 
Miiller,   H.      Wurzburg.   naturwiss.   Z.,  2, 

139  (1861)  ;   3,  10  (1862). 
Gesammelte  u.  hinterlassene  Schriften  zur 

Anat.  und  Physiol  des  Auges,  Leipzig 

(1872). 
Nishi.     Hb.  d.  vergl.  Anat.  d.   Wirbeltiere, 

Berlin,  4  (1938). 
O'Day.     Victorian  Nat.,  59,  141  (1942). 
Osawa.     Arch.  mikr.  Anat.  Entwick.,  51, 

481  ;    52,  268  (1898). 
Anat.  Anz.,  15,  226  (1899). 
V.  Pfluck.      Bull.  Soc.  frang.   Ophtal,  25, 

155  (1908). 
Plate.     Allgemeine  Zool.  u.  Abstanmiungs- 

lehre,  Jena,  2,  675  (1924). 
Prince.    J.  comp.  Neurol,  103,  541  (1955). 
Comparative     Anatomy     of     the     Eye, 

Springtield,  111.  (1956). 
Putter.     Graefe-Saemisch  Hb.  ges.  Augen- 

heilk..  Ill,  1  (x)  (1912). 
Rabl.     Z.  wiss.  Zool,  65,  257  (1898). 
Ranvier.       Traite    technique    d'histologie, 

Paris  (1889). 
Rathke.    U ntersuchungen  iiber  die  Entwick. 

der  Krokodile  (1866). 
Rochon-Duvigneaud.  Ann.  Oculist.  (Paris), 

154,  633  (1917)  ;    170,  177  (1933). 
Les  yeu.v  et  la  vision  des  vertebres,  Paris 

(1943). 
Schultze.       Arch.     mikr.     Anat.,     2,     175 

(1866)  ;    3,  215  (1867). 
Schwarz-Karsten.     Morphol  Jb.,  72,  499 

(1933)  ;    80,  248  (1937). 
Soeminerring.  De     oculorum     hominis 

aniynaliumque,  etc.,  Goettingen(1818). 
Szent-Gyorgyi.      Arch.    mikr.    Anat.,    85, 

303  (1914). 
Underwood.      Nature    (Lond.),    167,    183 

(1951). 
Verrier.      C.    R.    Acad.   Sci.    (Paris),    190, 

517  (1930)  ;    196,  723  (1933). 
Arch.  Zool,  Paris,  74,  30.5  (1932). 
Bull,  biol  France  Belg.,  67,  350  (1933). 
Bull.  Soc.  zool  France,  60,  443  (1936). 


REPTILES  395 

Vilter.     C.  R.  Soc.  Biol.  (Paris),  143,  338,  Amer.     J.     Ophthal.,     17,     892,     1045 

781,    784    (1949)  ;     145,    20,    24,    26  (1934). 

(1951).  Biol.  Si/mposia,  7,  203  (1942). 

Virchow.      Anat.   Hefte,   Abt.    2,    10,    720  Walls  and  Judd.      Brit.  J.   Ophthal,   17 
(1901).  641,  705  (1933). 

Arch.  Anat.  Physiol.,  Physiol.  Abt.,  355  Williams  and   Hecht.     Science,   122,   691 
(1901).  (1955). 

Walls.    Copeia,p.  125(1931).  Zinn.     Comment.  Soc.  Sci.   Goettingen,  3, 
Bull.  Antiven.  Inst.  A^ner.,  5,  68  (1932).  191  (1754). 


396 


THE   EYE   IN   EVOLUTION 


Fig.  482.— Casey  Albert  Wood   (1856-1942) 


CHAPTER  XIV 
THE  EYES  OF  BIRDS 


A  chapter  on  the  anatomy  of  the  eyes  of  birds  at  once  suggests  the  name  of 
CASEY  ALBERT  WOOD  (1856-1942)  (Fig.  482).  Born  of  American  parents  in 
Canada,  he  graduated  in  medicine  in  Montreal  in  1877,  becoming  one  of  the 
clinical  clerks  of  the  great  physician.  Osier,  at  ^McGill.  After  practising  for  some 
time  in  Montreal,  he  continued  his  studies  in  England  and  Europe,  and  in  1890 
settled  in  Chicago  where  he  occupied  the  Chair  of  Ophthalmology  initially  at 
the  Northwestern  University  and  eventually  at  the  University  of  Illinois.  He  was 
successively  president  of  the  American  Academy  of  Medicine  and  the  American 
Academy  of  Ophthalmology,  and  a  founder  member  of  the  Ainerican  College 
of  Surgeons.  A  man  of  extraordinarily  wide  interests  and  more  than  usual 
erudition,  he  is  particularly  remembered  for  his  prolific  writings,  the  most 
impressive  of  which  is  his  editorship  of  the  American  Encyclopedia  and  Dictionary 
of  Ophthcdmology  of  18  volumes,  to  which  he  contributed  largely.  He  was  also 
editor-in-chief  of  the  Anncds  of  Ophtlialmology  (1894-1901),  the  Ophthcdmic 
Record  (1902-8)  and  the  American  Journal  of  Ophthalmology  (1908-14).  His 
knowledge  of  the  history  of  ophthalmology  was  most  extensive,  a  subject  on 
which  he  wrote  an  interesting  manvial  ;  he  also  made  scholarly  translations  of 
ancient  works,  studying  for  this  purj^ose  in  the  Vatican  Library  at  Rome,  and 
wrote  a  delightful  book  on  his  researches.  The  comparative  anatomy  of  the  eye 
interested  him  greatly,  and  within  this  sphere  his  ])assion  for  ornithology 
earned  for  him  a  world-wide  reputation  ;  in  its  pursuit  he  travelled  widely  to 
countries  as  far  apart  as  British  Guiana  and  the  Far  East  to  study  the  eyes  of 
rare  birds.  These  observations  were  collected  in  his  classical  book.  The  Fundus 
Oculi  of  Birds  (Chicago,  1917),  while  his  extraordinary  erudition  and  pains- 
taking thoroughness  in  literary  research  is  nowhere  better  illustrated  than  in 
his  elaborate  and  exhaustive  Introduction  to  the  Literature  of  Vertebrate  Zoology 
(Oxon.,  1931).  A  true  scholar  with  an  unusual  and  contagious  enthusiasm,  he 
was  also  one  of  the  inost  delightful  and  gracious  of  men. 


BIRDS,  descendants  of  primitiv-e  Reptiles  probably  through  the  Dinosaiu's,^ 
are  essentially  adapted  for  the  air  for  which  purpose  their  forelegs  are  modified 
as  wings.     The  extant  species  are  divided  into  two  main  classes  : 

(a)  PAL.^coGNATH.E  (or  eatit^e),  a  relatively  sinall  class  of  running  birds 
with  degenerate  wings  and  a  flat  breast -bone  (the  ostriches  in  Africa  [Struthio) 
and  America  {Rhea),  the  emu  {Dromoeus)  and  the  cassowaries  (Casuarius)  in 
Australia,  the  tinamous  of  Central  and  South  America  and  the  kiwi  {Apteryx) 
in  New  Zealand,  Fig.  484)  ; 

(b)  neogxath.^  (or  carixat.e),  flying  birds  with  well-developed  wings  and 
a  keeled  breast -bone,  comprising  the  vast  majority  of  birds  of  over  11,000  living 
species  (Figs.  483,  485).  The  penguins  (Impennes),  however,  have  taken  to  the 
water  and  do  not  flv  at  all  ;    thev  have  hair-like  feathers,  a  whale-like  blubber 


Emu 


1  p.  234. 


Tinainou 


398 


THE   EYE   IN   EVOLUTION 


Figs.  483  to  4SH. — Typical  I'^.x-ampii's  ok  TJikd 


Fig.  483. — The  Barbaiy  turtle  dove, 
Streptopelia  roseogrisea  (Zool.  Soc, 
London). 


Fig.  484. — The  kiwi,  AjAeryx  (Burton's  Story  of 
Anhnal  Lije,  Elsevier  Pub.  Co.). 


Fig.  485. 


liilean  eagle,  Geranoaetus  (photo- 
!)y  Michael  Soley). 


Fig.  486. — The  ringed  penguin   (Zool. 
Soc.,  London). 


BIRDS 


399 


for  lieat -insula! ion  and  their  eyes,  highly  myopic  on  land,  are  entirely  adapted 
for  aquatic  vision  (Fig.  486).^ 

Among  the  Vertebrates,  Birds  share  with  Mammals  the  distinction 
of  having  attained  the  liighest  degree  of  speeiaHzation,  being  inferior 
to  them  only  in  cerebral  organization.  With  their  intense  activity  and 
highly  developed  emotional  life,  it  would  be  expected  that  the 
visual  organs  of  the  former  would  be  very  efficient  ;  this  is  indeed 
the  case  and,  in  fact,  the  eyes  of  Birds   are   supreme   amongst   all 

Figs.  487  to  491. — The  Eyes  of  Typical  Birds. 


Fig.  487.-^The  falcon. 


Fig.  488.— The  ow 


Fig.  489.— The  parrot. 


Fig.  490. — The  ostrich. 


Fig.  491.^The  swan. 


Some    of   Soeininerriiig's    heautiful    eiigra\'ings.      Xatural    size,    showing    the 
inferior  half  of  a  horizontal  section  of  the  left  eye  in  eacli  case. 

1  Other  water-hirds  have  eyes  suited  for  aerial  vision  and  have  adopted  devices 
for  adaptation  to  acjuatic  vision,  such  as  an  exceptional  range  of  accommodation 
(cormorant),  a  highly  refractile  nictitating  membrane  (ducks)  or  the  use  of  a  temporal 
fovea  with  a  hypermetropic  refraction  (kingfishers)  ;  others  have  not  done  so  and  act 
blindly  under  water  (tern)  (compare  p.  6.14). 


400 


THE   EYE   IN   EVOLUTION 


Figs.  492  and  493.— The  Avian  Eye. 


Fig.  492. — Diagram  of  the  eye  of  a  bird. 

A,  annular  pad  ;  BM,  Briicke's  muscle  ;  CC,  ciliary  cleft  ;  Ch,  choroid 
MC,  muscle  of  Crampton  ;  ON,  optic  nerve  ;  P,  pecten  ;  8,  scleral  cartilage 
Sc,  sclera  ;    SO,  scleral  ossicles  ;   TL,  tenacular  ligament. 


Fig.  493. — The  eye  of  the  domestic  chicken  (Norman  Ashton). 


BIRDS  401 

living  creatures.  This  somewhat  sweeping  statement  apphes  to  all 
birds  with  remarkably  few  exceptions,  such  as  the  shy,  nocturnal 
kiwi,  Apteryx,  the  eye  of  w'hich,  a  small  myopic  organ,  is  the  poorest 
among  birds,  for  the  dominant  sense  is  smell  rather  than  vision — a 
unique  j)henomenon  in  this  class.  Interestingly,  its  nostrils  are  placed 
near  the  tip  instead  of  the  base  of  its  long,  exploring  beak  (Fig.  484). 

Built  on  the  same  general  plan  as  the  eyes  of  their  ancestors,  the 
Reptiles,  the  eyes  of  Birds  are  remarkably  standardized  throughout 
the  entire  class,  showing  few  variations  among  themselves.  The 
general  features  of  the  avian  eye  are  as  follow^s  : 

The  large  size  of  the  eye  ^  and  its  flattened,  globular  or  tubular  shajie 
with  a  nasal  eccentricity  of  the  cornea  and  lens  to  assist  binocular  vision. 

The  deep  concavity  in  the  ciliary  region  to  maintain  which  the  sclera 
is  supported  by  scleral  ossicles,  the  non-spherical  shajic  of  the  globe  being 
further  supported  by  a  posterior  cartilaginous  cup. 

The  presence  of  muscular  elements  in  the  choroid,  ectodermal  striated 
muscles  in  the  iris,  and  a  complex  and  tvell-developed  ciliary  musculature 
which  bulges  the  lens  forwards  in  accommodation. 

A  lens  ivith  a  well-defined  annular  pad. 

An  elaborate  vascularized  glial  j)ccten  supiilementing  the  choroid  in 
supp>lying  nourishment  to  the  retina. 

A  thick  ayid  remarkably  icell-formed  retina  with  precise  layering  and 
quite  unusually  dense  pachiyig  of  the  visual  elements,  duplex  in  type  with 
rods  and  single  and  double  cones  containing  oil-droplets,  and  p>rovided 
with  one  or  sometimes  two  fovece. 

THE  GLOBE  OF  THE  AViAX  EYE  with  few  exceptions  is  relatively 
and  absolutely  large  although,  being  entirely  covered  by  the  lids 
apart  from  the  relatively  small  cornea,  its  external  appearance 
gives  the  opposite  impression  (Fig.  494).  The  two  ej'es  of  a  bird, 
however,  often  out^^'eigh  the  brain,  and  some  hawks  or  owls,  despite 
their  comparatively  small  size,  have  eyes  larger  than  those  of  man.  The 
shape  is  peculiar  and  distinctive  :  the  cornea  is  small  and  globular, 
the  posterior  segment  almost  hemispherical  with  the  horizontal 
diameter  often  slightly  greater  than  the  vertical,  but  the  intermediate 
region  between  the  tw'o  varies  (Figs.  488  and  490).  This  is  the  region 
strengthened  by  the  ring  of  scleral  ossicles  and  its  conformation 
determines  the  shape  of  the  eye  (Figs.  487  to  491).  Most  commonly 
it  resembles  a  flat  disc  in  which  the  cornea  is  set  centrally  while  the 
peripheral  border  joins  with  the  hemispherical  posterior  segment  of  the 
globe  ;    the  result  is  a  flat  eye  with  a  short  ant ero -posterior  axis,  a 

^  The  general  rule  illaller's  ratio,  1768)  (p.  450)  that  the  size  of  the  eye  is  inversely 
proportional  to  the  .size  of  the  body  is  here  overshadowed  by  the  complementary 
generalization  (Leuckart's  ratio,  1876)  that  the  size  of  the  eye  varies  directly  with 
swiftness  of  movemeut. 

S.O.— VOL.  I.  26 


402 


THE   EYE   IN  EVOLUTION 


(i  rouse 


conformation  characteristic  of  diurnal  birds  with  narrow  heads,  such 
as  the  Columbid?e  (doves,  pigeons)  or  the  Galhformes  (pheasants, 
grouse,  fowls,  etc.).  Alternatively,  in  diurnal  birds  with  broader  heads, 
such  as  the  Passeriformes  (perching  birds  such  as  thrushes,  sparrows, 
swallows  and  the  Corvida? — crow,  raven,  magpie,  jay,  etc.)  and  diurnal 
birds  of  prey,  such   as  the  Falconiformes   (eagle,  hawk,  falcon),  the 


Fig.  494. — The  Head  of  the  Owl,  Stri.x  alvco. 

To  show  tlie  enormous  size  of  the  eye  in  the  orbit  when  the  hds  and 
skin  are  removed  (Barany  et  a1.,  Brit.  J.  Ophthal.). 


Thiais 


Raven 


intermediate  segment  is  cone-shaped,  sloping  backwards  at  a  varying 
angle  to  meet  the  posterior  segment,  giving  the  configuration  of  a 
globular  eye.  In  nocturnal  birds  of  prey,  on  the  other  hand,  the 
intermediate  segment  runs  directly  backwards  with  a  marked  waist - 
like  concavity  before  it  I'uns  outwards  to  meet  the  posterior  segment 
at  a  sharply  angulated  junction,  producing  a  tubular  eye  as  is  seen 
most  tyjDically  in  the  Strigidse  (owls)  ;  in  this  case,  of  course,  the 
retina  is  comparatively  much  smaller.  In  each  type  in  the  interests 
of  easy  binocular  vision  there  is  a  considerable  nasal  asymmetry 
whereby  the  lens  and  cornea  are  centred  towards  the  mid-line,  making 
-lie  intermediate  segment  shorter  on  the  nasal  than  the  temporal  side. 
The  maintenance  of  this  non-spherical  shape  demands  skeletal 
i-       )ort  (Figs.  495-98).  The  hemispherical  posterior  segment  is  therefore 


BIRDS 


403 


Fig.  49;"). — The  Ring  of  Scleral 
Ossicles  of  the  Right  Eye  of 
THE    Goshawk,   Astch  PALcvBARirs 

d,    dorsal  ;     r,    ventral  ;     /;.    nasal  ; 
t,  temporal  (after  Franz). 


Fig.  496. — The  Cartilaginous  Cup 
IN  THE  Posterior  Part  of  the 
Globe  of  the  Hawk. 


strengthened  by  a  firm  cartilaginous  cup  which  occupies  the  inner  half 
of  the  thick  fibrous  sclera,  while  the  waist-like  constriction  is  maintained 
by  a  ring  of  imbricating  scleral  ossicles  made  up  of  membranous  bones 
overlapping  the  anterior  edge  of  the  cartilaginous  cup  (Figs.  495  and 
497).  These  ossicles,  described  by  Malpighi  (1697)  in  the  eye  of  the 
eagle,  vary  in  number  from  10  to  18,  the  commonest  being  15  (Dabelow, 
1926-27),  and  while  they  are  formed  of  compact  bone  in  small  eyes,  in 
large  and  particularly  in  tubular  eyes  they  contain  air-spaces  as  do 
many  of  the  bones  of  the  bird's  skeleton  (Lemmrich,  1931)  ;  it  is  this 
ring  of  bone  w^hich  essentially  determines  and  maintains  the  configura- 
tion of  the  intermediate  segment  and  therefore  of  the  entire  eye. 

Incorporated  in  the  posterior  cartilaginous  cup  a  ring-  or  horse-shoe-shaped 
bone  may  be  found,  the  os  opticus  or  ossicle  of  GEiiMiNGEK  (1852)  surrounding 
the  optic  nerve-head  in  one  or  several  pieces  ;  like  the  anterior  scleral  ossicles 
it  is  highly  cancellous  in  texture.  Tiemeier  (1950)  found  it  present  in  219  out  of 


Magjjie 


Fig.   497. — The  Ciliary  Region  of  the  Chicken. 
Showing  the   imbricated  scleral  ossicles  beneath   (  X  84)    (Norman  Ashton). 


404 


THE   EYE   IN  EVOLUTION 


The  cormorant 
Phalucrocorar. 


532  species  without  any  apparent  logical  distribution  ;    no  satisfactory  theory 
for  its  2:)resence  has  been  put  forward. 

Tlie  cornea  is  usually  small,  tliin  and  liighly  arched  but  becomes 
large  and  prominently  globular  in  predators,  particularly  those  of 
nocturnal  habit  ;  in  diving  birds  it  is  relatively  flat  and  tliick.  In 
these  a  zone  around  the  limbus  becomes  thickened  and  opaque,  resem- 
bling the  sclera,  while  the  scleral  ossicles  are  particularly  heavy  to  stiffen 
the  globe  against  the  shock  of  immersion  (as  in  the  cormorant, 
Phalacrocorax).     In  structure  it  conforms  to  the  usual  vertebrate  plan. 

The  anterior  chamber  of  certain  owls  {Strix  (Syrnium)  aluco)  contains  a 
slimy,  highly  visc<ius,  mucinovis  substance  of  a  mucopolysaccharide  (hyaluronic 


mm^ 


^y^yy^/  fi!^Lmmiwi.^a»,i  ^mm  v^,T\p^<m^^^ 


Fig.  498. — The  Posteriok  Segment  of  the  Globe  of  the  Chicken. 
r,  retina  ;   cJi.  fhoroid  ;   s,  scleral  cartilage  ;   sc,  sclei'a  (  X  80)  (Norman  A.shton). 


acid)  nature  ;  it  is  most  concentrated  (or  more  highly  polymerized)  close  to 
the  cornea  ami  is  perhaps  secreted  by  the  corneal  endothelium  (Abelsdorff  and 
Wessely,  1909  ;  Barany  et  al.,  1957).  It  .should  be  noted  that  the  anterior 
chamber  of  the  owl's  eye  is  relatively  enorinous  and  it  may  be  that  this  material 
allows  the  fluid  in  the  anterior  joart  to  remain  almost  stagnant  to  decrease 
the  turnover  that  would  be  necessary  were  the  exceptionally  large  amount  of 
aqueous  to  be  renewed  at  the  average  rate. 

The  uveal  tract  has  several  peculiarities.  The  choroid  is  tliick, 
particularly  posteriorly,  often  especially  so  in  the  region  of  the  macular 
area  (Fig.  498).  The  lamina  fusca  lies  directly  on  the  scleral  cartilage. 
Immediately  external  to  the  choriocapillaris  there  lies  a  stratum  of 
feeding  arteries,  outside  which  is  a  thick  layer  of  venous  sinusoidal 
spaces  traversed  by  radial  cords  of  smooth  (the  heron,  Ardea)  or 
striated  (the  cross-bill,  Loxia)  muscle  fibres  and  connective  tissue  of 
ry  variable  distiibution.  These  muscular  cords,  originally  described 
Wittich    n855),    Pagenstecher    (I860)    and    H.  Midler    (1861). 


BIRDS 


405 


and  most  fully  studied  by  Kajikawa  (1923),  are  most  marked  near  the 
fovea.  It  may  be  that  they  regulate  the  amount  of  blood  in  the 
choroid  which  in  Birds  is  particularly  distensible,  swelling  remarkably, 
for  example,  and  becoming  intensely  engorged  if  the  intra-ocular 
pressure  is  suddenly  lowered  by  paracentesis  of  the  anterior  chamber 
(Abelsdorff  and  Wessely,  1909)  ;  others,  again,  consider  that  their 
contraction  adjusts  the  position  of  the  fovea  in  accommodation,  acting 
after  the  manner  of  a  fine  adjustment  of  a  microscope. 

In  the  Picidffi  (woodjoecker,  Colaptes)  the  sinusoidal  choroidal  layer  is 
filled  with  mucoid  tissue,  as  if  to  provide  a  cushion  against  the  repeated  mechanical 
trauma  of  wood-pecking  (Walls,  1942).  Birds  have  no  tapetum  ;  the  "  eye- 
shine  "  seen  in  some  species  has  been  attributed  to  a  reflex  from  Bruch's 
membrane  (ostrich,  Struthio). 

The  vascular  layer  of  the  choroid  is  continued  forwards  into  the 
ciliary  region  without  the  intervention  of  an  orbiculus,  the  whole  zone 
being  occupied  by  the  numerous  elongated  ciliary  processes  ;  ventrally, 
in  the  region  of  the  fa?tal  cleft,  it  is  claimed  that  a  particularly  marked 
CILIARY  CLEFT  between  the  processes  allows  communication  between 
the  anterior  and  posterior  chambers  (Niissbaum.  1901  ;  Hess,  1912  ; 
Ischreyt,  1914).  The  ciHary  processes  and  their  associated  uveal  tissue 
angle  sharply  inwards  to  approach  the  lens,  while  the  ciHary  muscles 
cling  closely  to  the  sclera,  thus  separating  the  two  components  of  the 
ciliary  body  and  leaving  a  deep  cleft-like  space  bet^^  een  the  two  layers 
traversed  by  the  strands  of  the  pectinate  ligament  (Fig.  499).  The 
ciliary  musculature,  which  is  made  up  of  striated  fibres,  reseml)les  that 
of  the  lizard  in  its  topography  ^  (Fig.  500)  ;  both  it  and  the  muscles  of 
the  iris  are  supplied  by  a  complicated  plexus  of  motor  and  sensory 
nerves  (Boeke,  1933).  The  meridional  muscular  bundle  apj^ears  to  be 
divided  into  two  ;  anteriorly  the  muscle  of  cramptox.  a  stout 
muscular  band,  arises  from  the  inner  sm^face  of  the  cornea  at  its 
margin  and  is  inserted  into  the  sclera  as  it  bitlges  axially  in  the  ciliary 
region  ;  more  posteriorly  brucke's  muscle,  arising  from  the  inner 
aspect  of  the  sheet  of  sclera  which  forms  the  anchorage  of  the  pectinate 
ligament,  is  inserted  into  the  posterior  portion  of  the  ciliary  body,  an 
insertion  A\hich  is  prolonged  to  the  sclera  by  the  texacular  ligament, 
thus  relieving  the  choroid  of  mechanical  strain.  Accommodation,  as 
in  lizards,  is  mainly  effected  by  the  contraction  of  the  meridional 
musculature  forcing  the  ciliary  body  against  the  lens  so  as  to  deform  it, 
tautening  the  fibres  of  the  pectinate  ligament  meanwhile  (Wychgram, 
1913-14).  Simultaneously  the  stout  Crampton's  muscle  running  from 
the  cornea  to  the  sclera  like  a  bow^-string,  deforms  the  cornea  and 
shortens  its  radius  of  curvature,  an  action  much  more  pronounced  in 
Birds  than  in  lizards. 

1  p.  3.57. 


The  ostrich 
Struthio 


406 


THE   EYE   IN  EVOLUTION 


Fig.    499. — The    Ciliary    Kegion    of    the    Goshawk,  Astur   palvmbariur. 

B,  Bi'ucke's  muscle  ;  C,  cornea  ;  CM,  Ci'ampton's  muscle  ;  CP,  ciliary 
processes;  M,  MuUer's  muscle  ;  O — O,  ring  of  ossicles  ;  P,  ciliary  process  abut- 
ting the  lens  capsule  ;  S,  fibrous  sclera  ;  ST,  subconjunctival  tissue  ;  T, 
tenacular  ligament  ;    V,  ciliary  venous  sinus  (after  H.  Miiller,  1857). 


The  cassowur;; 
Casuarius 


Fig.  500. — The  Striated  Fibres  of  Crampton's  Muscle  in  the  Chicken 
(  X  240)  (Norman  Ashton). 

/ 

These  muscles  are  of  considerable  interest  and  have  received  much  study. 

Crampton  (1813)  first  described  a  muscle  in  this  region  in  the  ostrich,  Struthio, 

and  the  anterior  segment  of  the  ciliary  musculature  has  been  called  eponymously 

after  him  ;    he  termed  it  the  depressor  cornece.    Thirty-three  years  later,  Briicke 

(1846)   described  a  more  posteriorly  situated  muscular  zone  in  the  eagle-owl. 

Bubo  orientalis,  and  the  cassowary,  Casuarms,  calling  it  the  tensor  choroidece. 

Sometimes  this  latter  muscle  is  divided  into  two — an  anterior  portion  {Muller''s 

uiuscle)  which  was  first  described  by  this  author  (1856)  in  the  hawk,  Accipiter, 

and  a  posterior,  Brikke^s  muscle.  There  is  probably  little  functional  difference 

between  these  slips  of  muscles  thus  separated  anatomically,  nor  is  it  easy  to 

'■'cide  which  is  their  fixed  and  which  their  mobile  attachment  ;    connected  as 

y  are  by  aponeurotic  membranes,  they  probably  form  a  single  functional 

-'em. 


PLATE  XI 

The  Irides  of  Birds 
(Ida  Mann) 


xwrniCy***^ 


Fig.  1. — Jackdaw  (albino),  Coloslus  monedula. 


Fig.  2. — Pigeon,  Columba. 


Fig.  3. — Duck.  Dendrocygna. 


m 


Fig.     4. — Uock-ho]j    -r     penguin,     Eudyptes  FiG.  5. — Scops  owl,  Otus  bakkanice.na. 

cr    :itliis. 

A,  zone  of  radial  veins  and  deep  circumferential  arteries:  B,  sphincteric  plexus; 
G,  avascular  circumpupillary  zone;  D,  diagrammatic  section  through  iris.  a,  artery; 
c,  plexus ;  v,  vein. 


t  To  face  p.  407. 


so. — VOL.  I 


BIRDS 


407 


There  are  only  incidental  differences  between  these  muscles  in  the  various 
species  of  Birds.  In  diurnal  predators  they  tend  to  amalgamate  on  the  shortened 
nasal  side  and  sejtarate  on  the  lengthened  temporal  side;  in  the  swift,  Micropiis, 
the  entire  ring  is  symmetrical.  In  nocturnal  predators  Crampton's  mviscle  is 
well -developed  and  Briicke's  muscle  is  small  and  may  be  almost  absent  (most 
owls,  Strigidfe).  Since  deformation  of  the  cornea  is  of  no  value  in  aquatic 
vision,  CramjDton's  muscle  is  small  in  water-birds  (as  in  diving  ducks)  or  absent 
(as  in  the  cormorant,  Phalacrocomx),  while  in  compensation  and  to  attain  the 
necessary  accommodative  range  to  change  from  aerial  to  aquatic  vision,  Briicke's 
meridional  muscle  is  massive  in  these  types  and  may  even  be  supplemented  by 
circular  fibres  as  in  the  mviscle  of  Miiller  in  the  human  eye  (cormorant  ;  gamiet, 
Sula  hassana)  (Ischreyt,  1914).  A  muscle  homologous  to  the  transversalis 
muscle  of  lizards  has  been  described  in  the  pigeon  (Zalmann,  1921). 

The  iris  is  remarkably  thin  at  its  cihary  attachment  where  it  is 
reduced  ahnost  to  the  two  ectodermal  layers,  tliickens  towards  its 
mid -point  and  tliins  again  at  the  pupillary  margin.  The  ectodermal 
layers  are  both  heavily  pigmented  and  give  rise  to  the  striated  sphincter 
and  dilatator  muscles.  These  are  extremely  active  and  unusually 
powerful,  particularly  the  former  which  is  richly  vascularized  ;  it 
braces  the  iris  against  the  periphery  of  the  lens  thus  assisting  the 
ciliary  musculature  in  the  moulding  of  this  tissue  in  the  act  of 
accommodation,  at  the  same  time  confining  the  deformation  to  the 
axial  region.  The  sphincter  is  particularly  well  developed  in  some 
amphibious  birds  (cormorant,  Phalacrocorax  ;  shearwater,  Puffinus  ; 
gannet,  Sula  ;  and  the  sea-gulls,  Laridse,  etc.)  ;  in  the  cormorant, 
for  example,  it  is  able  to  force  the  axial  portion  of  the  soft  lens  as  a 
conical  protrusion  through  the  pupillary  aperture.  The  dilatator 
fibres  form  a  complete  layer  behind  the  sphincter,  running  into  the 
ciliary  region,  their  unusually  great  development  being  perhaps  due 
to  the  probability  that  they  also  play  a  part  in  compressing  the  lens 
on  accommodation  and  provide  a  fixed  anchorage  for  the  sjjliincter 
(Grynfeht,  1905  ;  Hess,  1910  ;  Zietzschmann,  1910  ;  Wychgram, 
1914  ;  Zalmann.  1921  ;  Welmer,  1923  ;  Anelli,  1934).  In  colour  the 
iris  is  variegated.  Most  of  the  song-birds  have  a  brown  pigmentation 
resembling  the  mammalian  tyj)e  ;  but  in  other  species  brilliant 
lipochrome  pigments  are  common,  particularly  yellow,  bright  blue  and 
green,  often  giving  the  eye  a  bright  colour-contrast  with  the  rest  of 
the  body  (Balducci,  1905)  (Plate  XI,  Figs.  1  to  5). 

This  advertising  habit  is  carried  a  stage  further  in  the  I'eriivian  guano 
coi-morant,  PhalacrGCorax  hougainvillii,  the  eye  of  which,  with  its  dun-brown  iris, 
is  surrounded  by  a  ring  of  naked  skin  coloured  bright  green.  The  colour  of  the 
iris  is  yellow  in  most  owls,  the  jaigeon,  Columba,  and  the  starling,  Lamprocolius 
chalybeus  ;  bright  blue  in  the  nocturnal  oil-bird,  Steatornis  ;  sky-blue  and 
chocolate  in  the  yellow  hang-nest,  Cacicus  cela  ;  green  in  the  cormorant  and  the 
duck,  Dendrocygyui,  and  the  flamingo,  Phoenicopterns  ruber  ;  white  peripherally 
and  chocolate  with  white  concentric  lines  in  the  pupillary  part  in  the  budgerigar, 


The  swift 
Micropus 


The  gaiiiiet 
Sula 


The  shearwater 
Puffinus 


The  flamingo 
Phanicopterus 


408 


THE   EYE   IN   EVOLUTION 


The  pengiiin 

Eudyptes 


The   house-sparrow 
Passer  domesticus 


Melopsiffacus  undulatus  ;  white  in  the  jackdaw,  Corvus,  and  the  crane,  Grus  ; 
and  so  on.  In  the  rock-pigeon,  Columba  livia,  it  appears  to  be  scarlet  because  of 
the  richness  of  the  superficial  blood-vessels.  In  the  honey-buzzard,  Pernis 
apivorus,  a  layer  of  guanine-containing  cells  in  the  yellow  iris  makes  the  tissue 
opaque  to  transmitted  light  and  a  brilliant  white  to  reflected  light.  Sexual 
differences  occur  in  a  few  species  ;  thus  the  male  breeding  blackbird,  Euphagus 
cyanoce2)halus,  has  a  yellow,  the  female  a  brown  iris  ;  again,  in  the  rock-hopper 
pengviin,  Eudyptes  cristatus,  the  colour  of  both  the  iris  and  the  beak  varies  from 
red  to  yellow  with  the  seasons  (Mann,  1931  ;    Lienhart,  1936  ;    and  others). 

The  pupil  is  always  circular  in  Birds  and  very  motile  ;  it  responds 
relatively  poorly,  however,  to  changes  in  light-intensity,  but  actively 
to  accommodation  and,  particularly  in  captive  wild  birds,  so  dramatic- 
ally to  emotional  factors  such  as  excitement  or  fear  that  it  has  been 
claimed  to  be  under  voluntary  control.  In  domesticated  birds,  on  the 
other  hand,  less  alert  and  more  placid  on  close  examination,  the 
ordinary  response  to  light  becomes  relatively  more  conspicuous.  There 
is  sometimes  an  apparent  consensual  light  reflex,  slow  in  its  onset  and 
irregular  in  its  degree  ;  Levine  (1955)  suggested  that  the  reaction  was 
due  to  light  sliining  through  the  head  to  stimulate  the  retina  of  the 
other  eye  directly,  and  in  birds  such  as  the  owl  wherein  the  visual 
axes  are  parallel,  no  such  reaction  can  be  seen. 

The  vascular  pattern  of  the  iris  is  typical  of  the  Sauropsida  and 
conforms  to  the  general  plan  seen  in  lizards  (Mann,  1929-31)  (Plate  XI, 
Figs.  1  and  5).  Several  arteries  enter  at  the  periphery,  run  in  a  deep 
plane  for  some  distance  circumferentially  and  supply  the  rich  capillary 
plexus  associated  with  the  sphincter  muscle  ;  thence  radial  veins  run 
superficially  towards  the  periphery,  sometimes  raised  up  from  the  sur- 
face of  the  iris  in  high  relief,  sometimes  largely  obscured  by  j)igment  and 
sometimes  completely  so  (the  falcon,  Falco  subbuteo,  or  the  shearwater, 
Puffitius).  The  sphincteric  capillary  plexus  is  usually  prominent  but 
is  variable  in  extent  ;  it  may  be  so  broad  as  to  occupy  almost  the 
entire  surface  of  the  iris  (as  in  the  oriental  eagle-owl,  Biibo  orientalis, 
or  the  rock-hopjDer  penguin,  Ei(di/2^tes  crisfafvs,  or  the  pigeon,  Columba) 
or  may  be  reduced  to  a  minimum  so  that  the  surface  is  largely  occupied 
by  the  radial  veins  (as  in  the  duck,  Dendrocygna) . 

At  the  angle  of  the  anterior  chamber  the  circumferential  ciliary 
venous  sinus  forms  a  complex  system  lying  in  connective  tissue  close 
to  the  inner  surface  of  the  sclera,  sometimes  separated  from  it  by  the 
anterior  end  of  Crampton's  muscle.  Two  annular  vessels  encircle  the 
eye  associated  with  at  least  one  large  artery  and  sometimes  with  two 
(in  the  sparrow.  Passer  domesticus),  and  draining  into  the  subcon- 
iiMK'tival  veins.    Only  occasionally,  as  in  the  kestrel,  Falco  tinnunculus, 

^   the  bull-finch,  Pyrrhula,  is  the  circle  incomplete  (Lauber,  1931). 

The  lens  usually  has  a  relatively  flat  anterior  surface  in  diurnal 

ij       ,  almost  plane  in  some  species  such  as  parrots  (Psittaciformes), 


BIRDS 


409 


but  more  spherical,  although  never  completely  so,  in  nocturnal  and 
aquatic  types  (Figs.  501-3).  It  is  always  soft  and  readily  deformed  ; 
apart  from  its  capsule  it  has  no  consistency  (Rabl,  1898),  and  according 
to  Kajikawa  (1923),  the  soft  mouldability  is  retained  all  through  life 
into  old  age.  In  some  aquatic  species,  particularly  the  cormorant,  it 
comj)ares  in  softness  only  with  the  lens  of  turtles.  The  system  of 
sutures  is  simple,  comprising  a  single  line  in  some  species,  a  star-shape 

Figs.  501  to  503. — The  Lenses  of  Birds. 


Fig.  501.— The  pigeon.  Fig.  502.— The  owl.  Fig.  503.— The  bullfinch. 

Note  the  relatively  flat  anterior  surface  (to  the  right  in  each  ca.se). 

in  others.  The  annular  pad  is  usually  well  formed,  sometimes  enor- 
mous in  diurnal  predators  with  a  high  degree  of  accommodation,  as  in 
the  hawk,  wherein  it  occupies  half  the  area  of  a  cross-section  of  the 
lens  (Fig.  504),  smaller  in  nocturnal  species  (Fig.  505),  still  smaller  in 
aquatic  forms  wherein  the  sphincter  of  the  iris  rather  than  the  ciliary 
muscle  is  especially  active  in  accommodation  (as  in  the  Anseriformes 
such  as  ducks,  geese,  swans,  etc.  ;  the  Ciconiiformes,  such  as  herons, 
storks,  spoonbills;  and  the  cormorant),  and  very  small  indeed  or  even 
vestigial  in  running  birds  (Palaeognathae,  particularly  the  kiwi, 
Ajyteryx)  ;  in  the  Australian  goose,  Cereojisis,  a  terrestrial  bird  which 
hardly  ever  leaves  the  ground,  the  pad  is  practically  non-existent. 


Figs.  504  and  505. — The  Lenses  and  Annular  Pads  of  Birds. 


Fig.  504. — The  lens  of  a  diurnal  predator 
(a  hawk).  Showing  a  very  large  annular 
pad. 


Fig.   505. — The  lens  of  a  nocturnal  bird 
(an    owl).      Showing    a    small    annular 


410 


THE   EYE   IN  EVOLUTION 


The  goat-sucker 
Caprimulrjus 


The  bald  eagle 
Haliaetus 


The  pelican 
Pelecanus 


The  zonular  fibres  arise  over  a  wide  area  from  and  between  the  ciliary 
processes  (Teulieres  and  Beauvieux,  1931). 

Between  the  annvilar  pad  and  the  main  body  of  the  lens  a  small  vesicle 
filled  with  albuminovis  fluid  remains  as  a  remnant  of  the  embryonic  lens  vesicle 
- — the  CAVUM  LENTicuLi  of  Franz  (1934).  To  some  extent  this  may  be  an  artefact 
of  preparation,  but  it  probably  aids  the  process  of  deformation  when  the  lens 
is  squeezed  by  the  ciliary  processes. 

Ophthalmoscopically,  the  fundus  oculi  of  Birds  presents  a  remark- 
ably constant  picture  which  has  been  extensively  studied  and 
beautifully  illustrated  in  a  unique  volume  by  Casey  Wood  (1917).  The 
background  of  the  fundus  is  usually  fairly  uniform  and  almost  invari- 
ably besprinkled  with  pigmented  dots  of  yellow  or  brown.  Its  colour 
varies  from  grey  or  a  slate-colour  to  orange  and  red.  In  general,  the 
fundi  of  diurnal  birds  are  characterized  by  a  grey  or  light  brown 
background  (such  as  the  bluebird,  Sialia)  (Plate  XII,  Fig.  3)  ;  that  of 
nocturnal  birds  tends  to  be  yellow,  orange  or  reddish  (such  as  the  kiwi, 
Apteryx,  the  tawny  owl,  Strix  aluco,  the  European  night-jar  or  goat- 
sucker, Caprimulgus  europceus)  (Plate  XII,  Figs.  1,  2,  4)  ;  a  multi- 
coloured background  is  more  rare  (buff  and  dull  red  in  the  American 
ostrich,  Rhea;  dark  reddish-brown  and  grey  in  the  bald  eagle,  Haliaetus 
leucocephalus).  Frequently  choroidal  vessels  may  be  seen  shining 
through,  an  appearance  usually  confined  to  a  small  segment  of  the 
fundus  in  its  ventral  part,  as  in  the  Australian  pelican,  Pelecanus 
conspicillatus,  and  the  kestrel,  Falco  tinnunculus  (Plate  XII,  Fig.  5)  ; 
more  rarely  the  vessels  are  generalized,  as  occurs  in  the  tawny  owl,  Strix 
aluco  (Plate  XII.  Fig.  2)  ;  as  a  rule  these 
vessels  are  most  apparent  in  nocturnal 
birds.  Nerve  fibres  are  usually  not  seen 
ophthahnoscopically  ;  they  are  rarely 
visible  in  nocturnal  birds,  but  in  divn-nal 
types  they  often  radiate  outwards  from  the 
disc,  sometimes  inconspicuously  and  run- 
ning for  a  short  distance  only  (Plate  XII, 
Fig.  4)  but  occasionally  covering  a  wide 
area  (Plate  XII,  Fig.  3).  The  optic  disc  is 
invariably  white  and  elongated  into  a  long 
CAUDA  (except  in  the  kiwi,  Apertyx)  which 
runs  ventrally  along  the  line  of  the  foetal 
fissure  (v.Szily,  1922  ;  Mann,  1924 ;  Uyama, 
1936)  ;  it  is,  however,  almost  entirely  ob- 
scured by  the  pecten. 

The  PECTEN, 1  originall}^  described  by 

1  The  name  is  derived  from  the  French  peigne  (a  comb),  but  in  view  of  the  fact 
!   there  are  no  separate  teeth  in  the  structure,  a  more  happily  chosen  name  is  the 
•        nan  Fdcher  (a  fan).     An  early  narne  was  Marsupium  (see  Crampton,  1813). 


Fig.  .506. — Vertical  Section 
OF  THE  Right  Eye  of  a 
Goose. 

Showing  the  temporal  half 
of  the  globe.  The  jDecten 
arising  from  the  elongated  optic 
disc  is  seen  (Thomson). 


PLATE  XII 

The  Fl-n-di  of  Birds 


Fig,  L-    Tin-  kiwi,  ^ijdrryx  niatitdli. 


Fig.  .'j. — Tlie  lihu-hiid.  Sial/'n  sudis. 


Fig.  5. — The  Euiupcan  ke:~trcl,  Fulco 


Fig.  2. — The  tawnv  owl.  Stric  nluco. 


Fig.  4. — The  Eiircipcan  nightjar,  Capri niidgus 
curopceus. 


Fig.  0. — Tlie  alhatro.ss,  DioinaJcu. 

{Figs.  1-5.  Casey  \\nn,\  :  Fio;.  G,  0"Day). 

[To  face  p.  410. 


BIRDS 


411 


Perrault  (1676)  whose  observation  was  elaborated  by  Petit  (1735),  is 
a  structure  peculiar  to  Birds  and  forms  the  most  dramatic  feature  of 
the  fundus  when  viewed  oi3hthalmoscopically.  It  ajDpears  in  the  ven- 
tral part  of  the  fundus  as  a  black  velvety  mass  rising  from  the  elon- 
gated optic  disc,  heavily  pigmented  particularly  towards  its  apex. 
Beautifully  and  elaborately  convoluted,  it  projects  freely  into  the 
vitreous,  usually  moving  undulatingly  with  movements  of  the  gel  (Fig. 
506).    Morphologically  two  main  types  occur  : 


Figs.  507  and  508. — The  Vaned  Type  of  Pecten. 


Fig.   507. — Diagram  of  the  pecteii  of 
the  ostrich,  Struthio  (  X  5). 


Fig.  508. — Section  jmrallel  to  tlie  base 
showing  the  central  web  and  the 
lateral  vanes  (after  Franz). 


(1)  The  varied  type.  In  Pal^eognathfe  (except  the  cassowary  and 
the  kiwi)  the  organ  is  composed  of  a  central  vertical  panel  with  laterally 
disposed  vanes  (Figs.  507-8).  In  the  kiwi.  Apteryx,  it  has  a  form  resem- 
bling the  conus  of  lizards  (Fig.  512). 

(2)  The  pleated  type.  In  Neognathse  (and  the  cassowary)  the 
whole  organ  is  pleated  upon  itself  like  an  accordion,  the  convolutions 
being  held  in  place  by  a  band-shaped  apical  bridge  running  along  the 
top  (absent  in  the  owl-^)  ;  if  this  is  cut  away,  the  pleats  can  be 
freely  smoothed  out  (Fig.  509). 

Although  always  built  on  much  the  same  general  plan,  the 
pecten  varies  considerably  in  shape,  size  and  the  number  of  folds. 
To  a  certain  extent  its  size  and  complexity  vary  with  the  visual  acuity 
of  the  bird  and  its  activity  in  daylight  (Wagner,  1837  ;  Virchow, 
1901)  ;  active  diurnal  birds  therefore  tend  to  have  a  large  and  many- 
folded  organ,  nocturnal  varieties  a  small  and  simpler  structure. 

The  number  of  pleats  varies  between  5  and  30  (Wood,  1917  ;  Kajikawa, 
1923  ;    Franz,  1934)  (Figs.  510-11)  ;    14  to  27  in  the  average  ground -feeding  or 


% 


The  kiwi 
Apteryx 


412 


THE   EYP]   IN   EVOLUTION 


^wSi^ 


mm 


Fig.  509. — The  Pleated  Type  of  Pecten. 

(A)  vertical  longitudinal  section  ;    (B)  transverse  horizontal  section  ;    (C)  and 
(D)  transverse  vertical  sections  (Thomson). 

perching  (passerine)  birds,  30  in  the  jay,  Garrulus  ;  in  predators  the  folds  are 
thicker  but  fewer  (13  to  17).  Sea-birds  and  shore-birds  tend  to  have  fewer  pleats, 
usually  less  than  12  ;  Anseriformes  (ducks  and  geese)  average  between  10  and 
16  ;  while  the  terrestrial  Australian  goose,  Cereopsis,  has  only  6.  Nocturnal 
sea-birds  have  very  few  (7  in  the  stone -cvirlew,  (Edicnenms).  Other  nocturnal 
forms  have  a  similarly  simple  structure  ;  the  swift,  Micropus,  has  11  pleats,  the 
owl.  Bubo,  5  to  8,  and  its  relatives  the  European  night-jar,  Caprimulgus,  3  to  5, 
and  the  frog-mouth,  Podargus,  3  to  4  ;    none  of  these  three  members  of  the  owl 


Fig.  Ti! ';,— The  Simple  Pleated  Pec- 
ten .;  THE  Barn  Owl,  Stbix 
FLAM  (Casev  Wood). 


Fig.  511. — The  Elaborate  Pleated 
Pecten  of  the  Red -headed 
Woodpecker,  Melanerpes  ery- 
throcephalus. 


BIRDS 


413 


family  possesses  a  bridge.  The  number  of  folds  does  not  depend  so  much  on  the 
species  of  bird  as  on  its  habits.  Thus  among  the  Palacognathn?,  the  active  diurnal 
ostriches,  Struthio  and  Rhea,  have  25  to  30  folds,  the  shy  and  crepuscular 
cassowary,  Casuarius,  4  large  and  2  small  folds  (almost  a  cone),  and  the  nocturnal 
kiwi,  Apteryx,  none. 

In  its  general  form  the  pecten  assumes  a  number  of  variations 
which,  have  been  classified  into  4  types  by  Casey  Wood  (1917)  (Figs. 
512  to  520  ;   Plate  XII)  : 

(1)  a  stumpy  structiu-e  projecting  only  a  short  distance  into  the 
vitreous,  such  as  in  the  night  heron,  N^ yet icorax,  and  the  secretary  bird, 
Serpentarius  cristatus  (Figs.  513-4)  : 

(2)  a  curved  structure  sloping  away  from  the  visual  axis  ventrally, 

Figs.  512  to  520. — Types  of  Pecten  in  Birds 
(The  fovea  when  present  is  shown)  (after  Casey  Wood). 


The  night  heron 
Nycticorax 


The  secretary  bird 
Serpentarius 


Fig.  512.— Tlie  kiwi, 
Apteryx. 


Fig.    513. — Tlie    common 
kestrel,  Falco  tinnuncuhts. 


Fig.    514. — The   secretary 
Vjird,  Serpentarius. 


Fig.  515. — The  herring- 
gull,  Larus  argentatun. 


Fig.  516. — The  wood- 
pigeon,  Columba 
palutnbus. 


Fig.  517. — The  American 
ostrich,  Rhea. 


Fig.    518.— The    laughing 
kingfisher,  Dacelo  yiyK.s. 


Fig.    519. — The    cliimney 
swallow,  Hirumlo  rusticu. 


Fig.   520.— The  blue  jay, 
Cyanocitta. 


414 


THE   EYE   IN   EVOLUTION 


The  blue  jay 
CyunoclUa 


all  the  time,  however,  close  to  the  bulbar  wall  and  not  penetrating 
far  into  the  vitreous,  such  as  in  the  pigeon,  Coluniba,  and  the  herring 
gull,  Larus  argentatus  (Figs.  515-8)  ; 

(3)  a  slender  sickle-shaped  structure  proceeding  with  a  curved 
course  from  the  disc  towards  the  equator  of  the  lens,  such  as  in  the 
blue  jay,  Cyanocitta  cristata,  and  the  chimney  swallow,  Hirundo  rustica 
(Figs.  519-20),  sometimes  almost  touching  it,  as  in  the  Anseriform  birds 
(goose,  swan).  Between  these  last  two  forms  gradations  occur,  such  as 
is  seen  in  the  great  spotted  woodpecker,  Dendrocopus  major  ; 


The  swallow 
Hirundo 


The  woodpecker 

Dendrocopus 

major 


Fig.  ,521. — The  Microscopic  Structure  of  the  Pecten  of  the  Chicken 
{  X  84)  (Norman  Ashton). 

(4)  a  cone-shaped  structure  without  pleats,  uniquely  found  in  the 
kiwi,  Apteryx  (Plate  XII,  Fig.  1  ;   Fig.  512). 

The  histological  structure  of  the  pecten  has  received  much  atten- 
tion (Fig.  521).i  Essentially  it  is  made  up  of  a  dense  and  elaborate 
capillary  network  associated  with  a  comparatively  small  amount  of 
supporting  tissue  ;  this  was  originally  (Mihalkovics,  1873  ;  Leuckart, 
1876  ;  Kessler,  1877)  and  sometimes  has  subsequently  (Bacsich  and 
Gellert,  1935)  been  said  to  be  mesodermal  in  origin,  but  following  the 
work  of  Bernd  (1905)  and  Franz  (1908),  has  been  generally  accepted  to 
be  glial  in  nature.  The  glial  tissue  derived  from  the  optic  disc  is  more  of 
the  nature  of  a  syncytium  than  cellular.  The  rich  vascular  plexus, 
\-,  liich  is  composed  of  vessels  of  greater  than  capillary  size,  is  supplied 

1  Mihalkovics  ( 1 873),  Denissenko  (1881),  Bernd  (1905),  Franz  (1908-9),  Blochmann 
:  V.  Husen  (1911),  Lschreyt  (1914),  Kajikawa  (1923),  Mann  (1924),  Menner  (1935), 
ika  (1938). 


BIRDS 


415 


by  an  artery  derived  from  the  hyaloid  system  emerging  from  the  optic 
disc  entirely  separate  from  the  choroidal  circulation  ;  this  artery  runs 
along  the  base  of  the  pecten  and  gives  off  ascending  branches  to  each 
of  the  folds,  whence  the  blood  is  gathered  by  large  veins  which  combine 
to  pierce  the  sclera  and  the  cartilaginous  cup  at  about  the  level  of  the 
middle  of  the  pecten  (Fig.  522).  The  walls  of  the  capillaries  contain 
no  muscle  or  nerve  fibres  and  between 
them  lie  epithelial  pigment -containing 
cells  ;  the  consensus  of  opinion  is  that 
there  are  no  structures  resembling  sensory 
end -organs  as  was  suggested  by  Franz 
(1908). 

The  function  of  the  pecten  has  excited 
speculation  ever  since  it  was  discovered  ; 
this  has.  indeed,  been  one  of  the  great 
puzzles  in  comparative  ophthalmology 
and,  based  on  the  dramatic  differences  in 
its  size  and  complexity  in  various  species, 
more  than  thirty  separate  theories  as  to 
its  possible  use  have  been  advanced.  Un- 
fortunately few  of  them  are  based  on 
physiological  experiment.  It  is  to  be 
remembered  that  the  presence  of  the 
structures  described  by  Franz  (19U8) — 
cilium-like  hairs  along  the  free  edge  of  the 
bridge  associated  with  bulbous  cells  with 
nerve  fibrils  running  between  the  pecten 
and  the  nerve -fibre  layer  of  the  retina — 
has  never  been  substantiated  ;  there  is  no 
evidence  that  the  pecten  is  anythmg  more 
than  a  complex  capillary  network  or  that 
it  can  be  interpreted  in  any  respect  as  a 
sense  organ.  Whatever  accessory  func- 
tions (if  any)  it  may  have,  all  authorities 
are  agreed  that  its  main  role  is  to  assist  in  the  nutrition  of  the  retina 
and  the  inner  eye  generally  ;  it  is  thus  strictly  comparable  to  the  falci- 
form process  of  teleostean  fishes  or  the  conus  of  lizards.  The  metabolism 
of  birds  runs  at  a  high  rate  ;  their  normal  temperature,  for  example, 
may  be  2'  to  14^  F  above  that  of  Mammals.  The  metabolism  of  the 
cone-rich  retina  must  be  similarly  high  and,  as  we  have  seen,  the  size 
and  the  complexity  of  the  pecten  vary  closely  with  the  diurnal  activity 
of  the  species  concerned.  Its  nutritive  function  was  proved  by  Abels- 
dorff  and  Wessely  (1909)  who  showed  the  high  permeability  of  the  rich 
capillary  system  to  the  solutes  of  the  blood,  while  its  complex  shape 


ON 


Fig.  r)22. — The  Structure  of 
THE  Pecten. 

Sliowing  its  relations  to  the 
entrance  of  the  optic  nerve  and 
its  vasenhir  connections.  A,  The 
supplying  artery  which  sends  a 
branch  to  each  fold  ;  Ch, 
choroid  ;  ON,  optic  nerve  ; 
P,  pecten  ;  i?,  retina  ;  Ȥ,  sclera  ; 
T^  efferent  vein  which  receives  a 
branch  from  each  angle  of  the 
fold  (Wood  and  Slonaker  ;  the 
illustration  is  inverted). 


416  THE   EYE   IN   EVOLUTION 

may  be  most  simply  interpreted  partly  as  a  mechanical  expedient  for 
buttressing  the  organ  to  give  it  rigidity  but  mainly  as  a  means  of 
increasing  the  available  diffusing  surface.  From  the  optical  point  of 
view,  there  is  little  doubt  that  a  pecten,  occupying  the  space  already 
taken  up  by  the  blind  spot  corresponding  to  the  optic  disc,  is  a  more 
efficient  method  of  nourishing  the  retina  than  the  provision  of  a  diffuse 
vascular  system  whether  it  be  intra-retinal  or  supra-retinal.  Indeed, 
the  position  of  the  pecten  is  such  as  to  interfere  as  little  as  possible  with 
the  function  of  the  retina  (Petit,  1735),  a  point  to  be  remembered  when 
considering  any  possible  optical  function.  In  this  respect  the  eyes  of 
birds  are  optically  superior  to  those  of  man. 


The  most  popular  subsidiary  functions  which  have  been  ascribed  to  the 
pecten,  four  of  them  metabolic,  four  of  them  optical  in  purpose,  may  most 
conveniently  be  summarized  as  follows  : 

(1)  An  aid  in  the  mechanism  of  accommodation  (Beauregard,  1875  ;  Rabl, 
1900  ;  Franz,  1909  ;  Hess,  1910).  It  was  suggested  that  an  increase  or  decrease 
in  turgidity  makes  the  pecten  act  as  an  erectile  organ  capable  of  displacing  the 
lens  hydraulically.  It  is  true  that,  in  general,  the  size  and  complexity  of  the 
pecten  vary  with  the  accommodative  capacity,  but  the  accommodative  capacity 
itself  varies  with  the  visual  effectivity,  that  is,  with  the  metabolic  level  of  the 
retina.  Any  relationship  between  the  two  may  therefore  be  parallel  rather  than 
causal  and  there  is  no  evidence  that  the  organ  changes  in  volume  with  accom- 
modative adjustments. 

(2)  A  stabilizer  of  the  intra-ocular  pressure,  acting  as  a  large  capillary- 
venous  reservoir  or  as  an  organ  of  secretion  or  excretion  to  regularize  the  tension 
of  the  eye  particularly  during  changes  of  altitude  during  flight  (Franz,  1909). 

(3)  A  means  of  smoothing  out  the  considerable  excursion  in  the  ocular 
pulse -pressure. 

(4)  A  means  of  maintaining  a  high  temperature  in  the  eye  particularly  at 
high  altitudes  in  an  animal  with  a  metabolic  rate  as  rapid  as  the  bird  (Kajikawa, 
1923). 

(5)  To  screen  the  retina  from  the  sun's  rays  from  above  (Paul  Bert,  1875) 
or,  alternatively,  to  serve  as  a  dark  mirror,  relaying  images  onto  the  retina, 
particularly  from  objects  above.  Thus  it  has  been  said  to  tone  down  excessive 
brightness  from  an  image  in  the  sky  or,  alternatively,  to  allow  a  ground -feeding 
bird  to  see  a  predator  overhead  (Thomson,  1928). 

(6)  To  intercept  rays  reaching  the  eye  simultaneously  from  in  front  and 
above  (Beauregard,  1875).  It  is  thus  held  to  suppress  binocular  vision  during 
mojiocular  fixation  or,  alternatively,  to  suppress  monocular  diplopia  during 
binocular  vision. 

(7)  To  aid  the  visual  resolution  of  moving  objects  when  in  flight.  Menner 
(1938)  suggested  that  finger-like  shadows  were  thrown  upon  the  retina  when  the 
bird  looked  at  the  sun  ;  a  moving  object  would  thus  be  seen  intermittently 
and  therefore  more  clearly  as  are  the  spokes  of  a  rotating  wheel  when  viewed 
stroboscopically. 

(;j)  As  an  aid  to  navigation.  This  extraordinary  faculty  of  birds  has  already 
beei:     ■■  "ussed.^     We  have  seen  that   one   of  the  necessities   for  orientation, 

1  p.  63. 


BIRDS 


417 


in  Wilkinson's  (1949)  view,  is  the  observation  of  the  sun's  arc  with  great  accuracy 
over  a  small  excursion,  and  it  is  said  that  the  pecten  may  play  an  important 
part  in  the  visual  analysis  thus  involved  by  acting  as  a  fixed  point  when  taking 
observations  (Menner,  1938  ;   Crozier  and  Wolf,  1943  ;   Griffin,  1952). 

Areas  subserving  acute  vision  are  the  rule  in  birds  and  are  more 
elaborately  constituted  than  in  any  other  species.^  An  area  centralis 
is  almost  invariably  present,  one  fovea  is  the  rule  and  two  occur  in 
many  species.^  The  single  fovea  usually  takes  the  character  of  a 
remarkably  deej)  and  well-formed  pit,  the  depth  varying  with  the 
excellence  of  vision  ;  it  is  thus  deepest  in  swift -flying  diurnal  birds 
of  prey.  This  central  fovea  subserves  monocular  vision.  Only  rarely 
does  a  single  fovea  occur  in  the  temporal  part  of  the  fundus  (owls). 
In  bifoveate  birds,  usually  diurnal  birds  of  prey,  the  deep  central 
fovea  is  associated  with  a  temporal  fovea  which  is  shallow  and  less 
^^'ell  formed,  except  in  hawks  and  eagles,  where  it  is  deep  ;  the  temporal 
fovea  is  used  for  seeing  straight  ahead  and  sometimes  for  binocular 
vision.  The  kingfisher,  Alcedo,  is  unique  in  that  it  uses  its  central 
fovea  for  aerial  vision,  its  temporal  fovea  for  aquatic  vision.^  In 
addition  to  these  macular  areas  with  their  fovese,  a  ribbon-like  band 
of  specialized  retina  is  sometimes  associated  (the  infula),^  running  in 
the  horizontal  meridian  through  the  fovea,  particularly  in  birds  that 
seek  their  food  in  the  ground  {Strufhio,  Saxicola)  or  in  aquatic  birds 
( Anseriformes :  geese,  swans,  etc.).  It  would  seem  probable  that  tliis 
band  subserving  accurate  vision  may  be  designed  for  food-searching. 

From  the  point  of  view  of  these  areas  for  specialized  vision,  birds 
may  be  classified  as  follows,  a  classification  which  depends  less  on  the 
type  of  bird  than  on  its  habits  (Plate  XII)  : 

(1)  Afoveal.  {a)  Domesticated  birds  and  some  ground-feeders. 
There  is  a  suggestion  of  an  area  centralis  centrally  but  it  is  sometimes 
absent  and  at  best  is  poorly  defined,  and  a  fovea  is  absent.  Typical 
examples  are  the  domestic  fowl,  Gallus  domesticus,  and  the  Californian 
valley  quail,  Lophortyx  californicus  vaUicola.  In  the  turkey,  Mehagris 
gallopavo,  the  guinea-hen,  Numida  jyucJierayii,  and  the  pigeon,  Columba, 
there  is  an  attempt  at  a  shallow  fovea.  (6)  Some  sea-birds  have  a  well- 
formed  area  centralis  in  wluch  cones  only  are  fomid  but  a  fovea  is 
absent — the  shearwater,  Puffinus,  and  the  fulmar,  Fulmarus  glacialis 
(Lockie,  1952). 

(2)  Central  monofoveal.  Tliis  applies  to  the  majority  of  birds  in 
which  a  well-formed  fovea  situated  centrally  is  surrounded  by  a  large 
macular  area. 

1  Chievitz    (1891),    Slonaker    (1897),    Casey    Wood    (1917),    Rochon-Duvigneaud 
(1919-23),  Franz  (1934),  Walls  (1942),  Bruckner  (1949). 
^  Compare  the  lizard,  Anolis,  p.  365. 
3  p.  641. 
*  Lat.  infula,  a  band  (Casey  Wood,  1917). 

S.O.— VOL.  I.  27 


Hawk, 
Buteo 


Kingfisher^ 
Alcedo 


Californian  quail, 
Lophortyx 


418 


THE   EYE   IN   EVOLUTION 


Owl -parrot, 
Stringops 


(3)  Temporalmonofoveal.  Owls  (including  the  owl-parrot,  Strin- 
gops) have  a  round  macular  area  in  the  temporal  quadrant  with  a 
shallow  fovea  (occasionally  absent).  The  swift,  Micropus,  has  in 
addition  a  trace  of  a  central  macula. 

(4)  Infula-mo7iofoveal.  Some  ground-feeders  and  water-birds, 
including  swimmers,  divers  and  waders,  have  a  central  round  macular 
area  with  a  fovea  of  medium  dejDtli  tlu'ough  which  runs  a  horizontal 
band  of  acute  vision.  These  include  the  albatross,  Diomedea  cauta,  and 
the  giant  ]3etrel,  Macromectes  giganteus  (O'Day,  1940)  (Plate  XII, 
Fig.  6). 


At'. 


'•■•-t»i»  ••♦•» 


Albatross, 
Diomedea 


Fig.   523. — The  Retina  of  the  Albatross,  Diomedea. 

Section  through  the  region  of  the  central  streak.  1,  optic  nerve  fibre 
layer  ;  2,  ganglion  cells  ;  3,  inner  plexiform  laj'er  ;  4,  inner  nuclear  layer  ; 
.T,  outer  plexiform  layer  ;  6,  outer  nuclear  layer  ;  7,  external  limiting  mem- 
brane ;    8,  visual  cells  ;    9,  pigment  epithelium  (O'Day). 

(5)  Bifoveal.  Many  birds  which  seek  their  prey  on  the  wing 
(j)asserines,  kingfishers,  bitterns,  humming  birds,  Calypte,  and  so  on) 
are  commonly  jDrovided  with  a  deej^ly  excavated  principal  central 
fovea  and  a  subsidiary  shallower  temi^oral  fovea  surrounded  by  a 
smaller  macular  area  lying  about  the  same  distance  from  the  optic 
disc  as  the  central  fovea. 

((^)  Infnla-bifoveal.  Certain  predators  have  two  foveae  associated 
with  a  band  of  clear  vision,  (a)  The  more  common  arrangement  is 
two  circular  macule  connected  by  a  band,  as  occurs  in  hawks,  eagles 
'  '^  swallows  ;  each  macula  has  a  fovea,  the  central  being  deepest 
€'       ot  in  the  eagles  wherein  the  temporal  is  deepest,    {b)  Alternatively, 


BIRDS 


419 


the  central  fovea  may  be  situated  in  a  band  but  this  does  not  inckide 
the  temporal  fovea  wliich  is  situated  above  and  separate  from  the 
former  (the  tern,  Sterna  Mr  undo). 

(7)  Infular.  Some  water-birds  have  a  horizontal  band  only  with 
no  macular  area  and  in  it  may  be  a  linear  trough-like  fovea  :  gulls, 
flamingo. 

Histologically  the  retina  of  birds  is  the  most  beautiful  and 
elaborate  in  its  arcliitect  ure  in  the  animal  kingdom  ^  ;  layers  and  sub- 
layers are  clearly  defined  with  each  cell 
accurately  in  place  (Fig.  523).  As  with 
other  Sauropsida  the  pigmentary  epi- 
thelial cells  send  slender  processes  con- 
taining fuscin  granules  extending 
inwards  to  the  inner  segments  of  the 
visual  cells  ;  their  movements  with 
variations  of  light  and  shade  are  rapid 
and  Extensive,  possibly  making  up  for 
the  relative  inertia  of  the  pupil  to  light. 
In  the  visual  retina  the  ganglion  cells  lie 
in  2  or  3  rows.  The  inner  plexiform 
layer  is  unusually  thick  and  stratified 
at  the  levels  at  wliich  the  arborizations 
of  the  amacrine  cells  deploy.  The  inner 
nuclear  layer  is  expanded  to  have  three 
strata — innermost  the  (integrative) 
amacrine  cells  which  may  even  out- 
number the  bijDolars,  outermost  the 
(conductive)  bipolar  elements,  and  in 
the  middle  a  single  com23act  row  of 
Miiller's  fibres.  This  layer  as  a  whole  is 
thus  very  tliick,  and  mainly  because  of 
the  unusual  development  of  this  and 

the  inner  plexiform  layer,  the  retina  of  Birds  is  some  one-and-a-half 
times  to  twice  as  thick  as  that  of  the  majority  of  Vertebrates,  being 
approached  in  this  respect  only  by  a  few  Teleosteans. 

The  visual  cells  are  slender  and  closely  packed  (Fig.  524).  The 
retina  is  duplex  in  type,  containing  rods  and  single  and  double  cones. 
The  rods  are  slender  with  a  long  thin  paraboloid  and  contain 
rhodopsin  but  have  no  oil-droplets,  resembling  in  their  general  structure 
those  of  Chelonians  or  Crocodilians  ;  in  nocturnal  birds  they  pre- 
dominate while  in  diurnal  types  they  may  be  very  few  and  limited  to 

1  H.  Miiller  (1856-63),  Krause  (1863-94),  Merkel  (1870),  Dobrowolsky  (1871), 
Schultze  (1873),  Waelchli  (1881-83),  Dogiel  (1888-95),  Cajal  and  Greeff  (1894),  Fritsch 
(1911),  Rochon-Duvigneaud  (1919-43),  Kajikawa  (1923),  Kolmer  (1924-36),  Chard 
(1938),  van  Eck  (1939).  O'Day  (1940),  Walls  (1942),  Lockie  (1952),  Yamamoto  (1954). 


Fig.   524. — The   Visual  Cells   of 
Birds. 

From  the  left,  a  single  cone,  a 
double  cone,  both  from  the  peri- 
phery ;  a  peripheral  rod,  and  a 
central  rod  of  the  English  sparrow, 
Passer  domesticus.  p,  the  para- 
boloid  (X   1,000)   (Gordon  Walls). 


Tern, 
Sterna 


420 


THE   EYE   IN  EVOLUTION 


Kite,  Milvus 


Flicker,  Coluptes 


the  23eriphery.  The  cones,  which  in  diurnal  varieties  greatly  outnumber 
the  rods,  may  be  single  or  double.  As  in  Chelonians,  the  single  cones 
and  the  chief  element  in  the  double  cones  contain  an  oil-droplet,  a 
prominent  feature  of  the  avian  retina  known  to  the  early  anatomists 
such  as  Treviranus  (1837)  and  Hannover  (1840).  They  are  of  various 
colours — red,  orange,  yellow — and  colourless  ;  they  tend  to  be  brightly 
coloured  in  diurnal  types,  particularly  in  small  song-birds,  but  pallid 


Fig.   5:i5. — The  Fovea  of  the  Albatkuss,   Diomedea    (O'Day). 


and  almost  colourless  in  nocturnal  types, 
have  been  described  in  a  few  species.^ 


Green  droplets  are  rare  but 


stormy  petrel, 
■  Procellaria 


At  first  supposed  to  be  associated  with  colour  vision  (Krause,  1863),  these 
oil  droplets  are  now  more  generally  considered  to  have  a  pvirely  absorptive  func- 
tion, eliminating  light-rays  which  are  inconvenient  qualitatively  or  quantitively 
and  aiding  the  acuity  of  vision.- 

The  fovea  of  Birds,  particularly  the  central  fovea,  is  remarkably 
deep  with  liighly  convex  sides,  resembling  in  its  general  shape  the  deep 

1  The  domestic  cock,  Gallus  doynesticus  (Waelchli,  1883),  the  kite,  Milvus,  and  the 
Ti  parrot,  Chrysoiis  (Kiihne,   1882),  the  flicker,  Colaptes  auralus  (Walls  and  Judd, 
')  and  the  stormy  petrel,  Procellaria  pelagica  (Rochon-Duvigneaud,  1943). 
p.  631. 


BIRDS 


421 


m. 


f*"'-. 


^^^^-'^^^uijiiyijii^y^l^ 


Fig.  526.— The  Central  Fovea  of  the  Swallow,  Hirvsdo. 
(Rochon-Duvigneaud). 


2A^'3?*ip-;ix?«v;vs^yji^^^Ss^gr&, 


..,.f:?;'^^*^•.'A's>l^i:;y*?^.'*^♦.^^^^* 


i^ «» *.* 


,t.v«    »^,''''^f*^ 


,.1  **^* 


Fig.  .527.— The  Lateral  Fovea  op  the  Swallow,  HiRvyoo. 
(Rochon-Duvigneaud) . 


•-*^ 


YiQ,  528.— The  Band-shaped  Area  of  the  Gannet,  Sula 
(Rochon-Duvigneaud). 


422 


THE   EYE   IN   EVOLUTION 


pit-like  fovepe  of  lizards  ;  the  temporal  fovea  is  shallower  and  some- 
what reminiscent  of  the  human  fovea  (Figs.  525-7).  In  the  central  pit, 
single  cones  containing  yellow  oil-droplets  predominate  and  rods  are 
excluded.  In  the  deep  fovea  of  the  Lacertilians  and  the  shallow  fovea 
of  the  Primates,  the  cones  are  slim  and  elongated, 
the  nuclear  layers  are  pushed  away  from  the 
central  area  and  the  nerve  fibres  aggregated  to 
form  a  layer  of  Henle  ;  in  Birds,  on  the  other 
hand,  a  considerable  proportion  of  the  nuclei  is 
retained,  a  circumstance  which  would  seem  to 
sujjport  Walls's  (1937)  suggestion  that  the 
purpose  of  the  fovea  is  not  so  much  to  remove 
cellular  impediments  to  the  incident  light  as 
to  scatter  it  over  a  wider  area.^  In  the  band- 
shaped  areas  of  greater  acuity  the  retina  is  thicker  than  usual  so  that 
it  projects  into  the  vitreous  owing  to  an  enormous  increase  in  the 
number  of  nuclei  in  the  bipolar  layer,  a  considerable  increase  in  the 
outer  nuclei  and  a  lengthening  of  the  visual  cells  (Fig.  528)^  At  the  edge 
of  the  fovea  this  thickening  of  the  retinal  layers  is  further  increased  to 
form  a  definite  ridge  owing  to  the  lateral  displacement  of  cells  from 
the  foveal  pit  (O'Day,  1940). 

The  02:)tic  nerve  is  of  the  usual  vertebrate  type  with  a  variable 


Fig.    529. — The    Decus- 
sation AT  THE  ChTASMA 

OF  A  Bird. 


Fig.   530. — The  Milky  Eagle  Owl,   Bubo  lacteus. 

i  his  bird  is  unusual  ;    showing  the  greater  development  of  the  upper  lid 
■    moves  preferentially  (photograph  by  Michael  Soley). 

1  p.  658. 


BIRDS 


423 


Figs.  531   and   532. — The  Mechanism  of  the  Nictitating  Membrane  in 

Birds. 


Fig.  531. — The  anterior  aspect  of  the 
ej^e  of  the  turkey. 

Showing  the  insertion  of  the  pyra- 
midalis  tendon  into  the  nictitans 
(Bland-Sutton). 


Fi( 


532. — The  posterior  aspect  of  the 
eye  of  the  turkey. 

Showing     the     pyramidalis 
fontinued  as  a  tendon  (below 
through     the     sling     formed 
quadrat  us     muscle     (above) 
Sutton). 


muscle 
looping 
by  the 
(Bland- 


septal  system  ;  a  single  large  septum  ma}'  run  to  the  axis  where  it 
subdivides  ;  the  oligodendroglial  cells  are  widely  scattered  and 
numerous,  being  thickly  packed  between  the  fascicules  of  nerve  fibres 
(Prince,  1955).  The  decussation  of  fibres  at  the  chiasma  is  complete 
with  an  elaborate  interdigitation  of  fasciculi  (Beauregard,  1875  ; 
Gudden,  1879  ;  Gallerani.  1888  ;  Faravelh  and  Fasola.  1889)  (Fig.  529). 

THE  OCULAR  ADXEXA.  The  Hfls  almost  cover  the  globe  revealing 
only  the  small  cornea  through  their  (usually)  circular  aperture, 
deceptively  hiding  the  relatively  enormous  eye  (Fig.  530).       In  the 


y 


Fig.  533. — The  Orbits  of  the  Sparrowhawk,  A'cipiTEit. 


424  THE   EYE   IN   EVOLUTION 

movements  of  the  iids  there  is  a  more  equable  distribution  of  labour 
than  is  seen  in  Amphibians  and  other  Sauropsidans  (Bartels  and 
Demiler,  1921)  :  the  lower  is  usually  the  more  active  of  the  two,  but 
the  upjDer  lid  also  plays  a  considerable  part.  Except  in  parrots,  the 
more  active  lower  lid  is  provided  with  a  fibrous  tarsal  plate  composed 
of  fibro -elastic  tissue  without  cartilage  (Naglieri,  1932).  The  nictitating 
membrane  is  well  developed  with  a  feather-like  epithelium  (Kajikawa, 
1923  ,    Kolmer,   1923-30  ;    AnelH,   1935)  ;    it  sweeps  over  the  globe 


Fig.    534. — The  Orbits  and    Brain    of    the    English  Sparrow,   Passeb 

domestivus. 

c,  optic  chiasma  ;  e,  external  rectus  ;  g,  gasserian  ganglion  ;  /;,  liarderian 
gland  ;  in,  inferior  rectus  ;  io,  inferior  obliqvie  ;  ir,  internal  rectus  ;  /,  lacrimal 
gland  ;  m,  medulla  ;  o,  optic  nerve  ;  ol,  optic  lobe  (midbrain)  ;  p,  pituitary  ; 
3,  third  cranial  (oculomotor)  nerve,  supplying  the  superior,  internal,  and  inferior 
recti  and  the  inferior  oblique  ;  4,  fourth  cranial  (trochlear)  nerve,  supplying 
the  superior  oblic^ue  ;  5,  fifth  cranial  (trigeminal)  nerve,  several  of  the  branches 
of  which  carry  fibres  to  the  eye  and  adnexa  ;  6,  sixth  cranial  (abducens) 
nerve,  supplying  external  rectus  (Gordon  Walls  ;  drawni  from  Wood  and 
Slonaker). 

from  the  nasal  canthus  controlled  by  a  pyramidalis  muscle  attached  to 
the  posterior  surface  of  the  sclera,  the  optic  nerve  being  protected  by 
lacing  the  tendon  tlu'ough  the  well-developed  quadratus  (bursalis) 
muscle  (Figs.  531-2).  It  is  probable  that  these  two  muscles  are  homo- 
logous with  the  retractor  bulbi  of  Crocodilians  (Wedin,  1953).  The 
nictitans  is  very  transparent  and  has  no  fibrous  or  cartilaginous  basis  ; 
it  is  probable  that  it  can  cover  the  eye  without  affecting  vision  greatly, 
and  in  fact  many  believe  that  it  is  drawn  over  the  cornea  habitually 
as  a  p    '-^ctive  goggle  during  rapid  flight. 

In  •  in  diving  birds  (diving  ducks  ;    auks,  Alcidse  ;    and  the  loon,  Gavia) 

the  nict  i  membrane  has  a  central  clear  window  which,  being  highly  refractile, 


BIRDS  425 

adjusts  the  eye  to  under-water  vision  as  it  is  drawn  across  immediately  the  head 
is  immersed  (Ischreyt,  1913-14)  ;    it  thus  acts  as  the  lens  of  a  diver's  spectacle. ^ 

The  lacrimal  gland  with  its  single  duct  is  ventre -temporal  in 
location  being  associated,  as  is  usual,  with  the  more  active  lid  ;  although 
it  is  well  developed  in  most  water-birds,  it  is  absent  in  the  fully  water- 
adapted  penguins  (Impennes)  and  also  in  the  owl,  Bubo.  The  harderian 
gland  in  its  nasal  position  associated  with  the  nictitating  membrane, 
secretes  a  thick  oily  fluid  ;  in  the  cormorants  it  is  exceptionally 
large  and  the  secretion  abimdant,  acting  probably  as  a  protection 
against  sea-water.  Meibomian  glands  are  absent  (Anelli,  1936).  There 
are  two  slit-shaped  lacrimal  puncta,  a  larger  upper  and  a  smaller  lower 
at  the  nasal  canthus. 

The  orbits  are  very  large  to  accommodate  the  enormous  eyes  and 
occupy  a  considerable  proportion  of  the  entire  head  (Fig.  533)  ;  as  a 
rule  they  meet  in  the  median  plane,  being  separated  from  each  other 
only  by  a  thin  bony  interorbital  septum  (Bellairs,  1949). 

The  orbits  are  open  in  type  ^  resembling  in  their  general  form  those 
of  Reptiles,  particularly  the  tortoises  ;  it  is  to  be  remembered  that  the 
lack  of  protection  to  the  anterior  part  of  the  globe  that  results  from  this 
configuration  is  to  some  extent  compensated  by  the  firm  ring  of  im- 
bricated scleral  ossicles  which  encircles  the  sclera  immediately  behind 
the  limbus. 

Into  this  orbit  the  globe  usually  fits  so  snugly  that  the  extra- 
ocular muscles  must  perforce  be  small  (Fig.  534)  ;  a  retractor  bulbi  is 
absent  in  Birds  since  the  globe  cannot  be  further  retracted  into  a 
cavity  which  it  already  fills.  In  consequence,  ocular  movements  are 
negligible  or  absent.  As  we  shall  see  at  a  later  stage, ^  this  immobihty 
of  the  eyes  is  compensated  by  the  extreme  mobility  of  the  neck  and  the 
constant  movements  of  the  head.  Nevertheless,  although  the  muscles 
are  tenuous,  the  four  recti  and  the  two  obliques  are  normally  repre- 
sented, each  being  provided  with  the  standard  nerve  supply  charac- 
teristic of  the  vertebrate  phylum. 


Abelsdorff   and    Wessely.      Arch.    Augen-  Barany,  Berggren  and  Vrabec.     Brit.  J. 

heilk.,  64,  Erg.,  65  (1909).  Ophthal,  41,  25  (1957). 

Anelli.    Boll.  Oculist.,  13,  1461  (1934);  14,  Bartels  and  Dennler.     Zool.  Anz.,  52,  49 

499  (1935).  (1921). 

Ric.  Morjol..  15,  233  (1936).  Beauregard.     C.  R.  Soc.  Biol.  (Paris),  27, 
Bacsich   and   Gellert.       v.    Graejes   Arch.  132  (1875). 

Ophthal.,  133,  448  (1935).  Bellairs.     J.   Linn.  Soc.   London,  41,   482 
Balducci.       Monit.    zool.    Ital.,    16,     258  (1949). 

(1905).  Bernd.     Inaug.  Diss.,  Bonn  (1905). 

1  p.  643. 

^  To  this  generalization  there  are  exceptions,  such  as  the  Australian  cockatoo, 
Cacatua  roseocapella  (Prince,  1956). 
3  p.  696. 


426 


THE   EYE   IN   EVOLUTION 


Bert.    C.  R.  Soc.  Biol.  (Paris),  2,  65  (1875). 
Blochmann  and  vanHusen.  Biol.  Zbl.,  31, 

150  (1911). 
Boeke.      Z.  mikr.-Anat.   Forsch.,   33,   233 

(1933). 
Briicke.    Arch.  Anat.  Physiol.,  370  (1846). 
Bruckner.         Ophthalmologica,     118,     969 

(1949). 
Cajal  and  Greeff.     Die  Retina  d.   Wirbel- 

thiere,  Wiesbaden  (1894). 
Chard.    J.  comp.  Psychol,  25,  249  (1938). 
Chievitz.    Arch.  Anat.  Physiol.,  Aht.  Anat., 

311  (1891). 
Crampton.     Thompson's  Ann.   Philos.,  1, 

170  (1813). 
Crozier  and  Wolf.     J.  gen.   Physiol.,  27, 

287,  315  (1943). 
Dabelow.    Anat.  Anz.,  61,  Erg..  95  (1926). 

Z.  Morphol.  Anthrop.,  26,  305  (1927). 
Denissenko.     Arch.  mikr.  Anat.,  19,    395 

733  (1881). 
Dobrowolsky.     Arch.  Anat.  Physiol.,  208, 

221  (1871). 
Dogiel.    Anat.  Anz.,  3,  133,  342  (1888). 

Arch.  mikr.  Anat.,  44,  622  (1895). 
van  Eck.    Arch,  neerl.  Zool.,  3,  450  (1939). 
FaravelH  and  Fasola.     Ann.  Ottal.,  18,  20 

(1889). 
Franz.     Biol.  Zbl.,  28,  467  (1908). 

Zool.    Jb.,    Abt.    Anat.    Ontog.,    28,    73 

(1909). 
Bolk's  Hb.  d.  verql.  Anat.  d.  Wirbeltiere, 
Berlin,  2  (ii),  l'l27  (1934). 
Fritsch.    Arch.  mikr.  Anat.,  78,  245  (1911). 
Gallerani.       Fisiol.    d.    commessure    ence- 

faliche,  Padova  (1888). 
Gemminger.     Z.  tviss.  Zool.,  4,  215  (1852). 
Griffin.     Biol.  Rev.,  27,  359  (1952). 
Grynfeltt.  G.  R.  Ass.  Anat.,  Geneve  (1905). 
Gudden.    v.  Graefes  Arch.  Ophthal.,  25  (1), 

1  (1879). 
Haller.     Opera  minora,  3  (1768). 
Hannover.       Arch.    Anat.     Physiol.,    320 

(1840). 
Hess.     Arch.  Augenheilk.,  62,  345  (1909). 
Arch,  vergl.  Ophthal,  1,  153  (1910). 
Zool.  Jb.,  Abt.  Zool.  Physiol,  Suppl.  15 
(3),  155  (1912). 
Ischreyt.     Arch,  vergl.  Ophthal,  3,  39,  369 

(1913)  ;   4,  162  (1914). 
Jokl.     Z.  ges.  Anal,  63,  227  (1922)  ;    68, 

523  (1923). 
Kajikawa.     v.  Graefes  Arch.  Ophthal,  112, 

260  (1923). 
Kessler.      Zur   Entwicklung   d.    Auges   d. 

Wirbeltiere,  Leipzig  (1877). 
Kohner.    Anal  Anz.,  57,  122  (1923). 
Pfliigers  Arch.   ges.    Physiol,   204,    266 

(1924). 
Hb.  mikr.  Anat.  d.  Menschen,  Berlin,  3 

(2).  431  (1936). 
V.    C'raefes    Arch.    Ophthal.,     124,     652 
(lii:^0). 
Kraus;e.  Z.  rat.  Med.,  20,  1  (1863). 

Arch.       Lr.  Anal,  19,  309  (1881). 


Internal  Mschr.  Anat.  Physiol,   11,    1, 
69  (1894). 
Kiihne.     Untersuch.  a.  d.  physiol  Inst.  d. 

Univ.  Heidelberg,  2,  89  (1882). 
Lauber.     Graefe-Saemisch  Hb.  ges.  Augen- 
heilk., II,  1  (2),  Kap.  3  (1931). 
Lemmrich.     Jena.  Z.  Naturwiss.,  65,  513 

(1931). 
Leuckart.  Graefe-Saemisch.  Hb.  ges.  Augen- 
heilk., I,  2,  (2),  145  (1876). 
Levine.    Science,  122,  690  (1955). 
Lienhart.     C.   R.  Soc.   Biol.   (Paris),  121, 

1415,  1630  (1936). 
Lockie.    Quart.  J.  micr.  Sci.,  93,  347  (1952). 
Malpighi.  Opera  posthuma,  London  (1697). 
Mann.     Bril  J.  Ophthal,  8,  209  (1924). 
Trans,  ophthal.  Soc.  U.K.,  49,  353  (1929). 
Trans,  zool  Soc.  Lond.,  21,  355  (1931). 
Menner.     Zool  Anz.,  Suppl.  8,  244  (1935). 
Zool.  Jb.,  Abt.   Zool   Physiol,  58,  481 
(1938). 
Merkel.     Arch.  Anat.  Physiol,  642  (1870). 
Mihalkovics.      Arch.   mikr.   Anal,   9,   591 

(1873). 
Miiller,  H.    Anat.-physiol  Untersuchungen 
iiber    d.    Retina    d.    Menschen    u.    d. 
Wirbeltiere,  Leipzig  (1856). 
Wurzburg.  nctturwiss.  Z.,  2,  139  (1861). 
Klin.  Mbl  Augenheilk.,  1,  438  (1863). 
Naglieri.     Monit.  zool.  Ital,  43,  17  (1932). 
Niissbaum.      Arch.   mikr.   Anal,   57,    346 

(1901). 
O'Day.     Brit.  J.  Ophthal,  24,  201  (1940). 
Pagenstecher.       Verhdl    phys.-tned.    Ges. 

Wurzburg,  10,  173  (1860). 
Perrault.     Memoirs  pour  servir  d  Vhistoire 
naturelle     des     animaux,       2nd     Ed. 
(1676). 
Petit.    Mem.  Acad.  Sci.,  Paris,  123  (1735). 
Prince.    J.  comp.  Neurol,  103,  541  (1955). 
Comparative      Anatomy     of     the     Eye. 
Springfield,  Illinois  (1956). 
Rabl.     Z.  wiss.  Zool,  65,  257  (1898). 
Ueber  d.   Bau.   u.   die  Entwickelung  d. 
Linse,  Leipzig  (1900). 
Rochon-Duvigneaud.  Ann.  Oculist.  (Paris), 
156,    717    (1919);     157,    673    (1920); 
160,  769  (1923). 
Les  yeux  et  la  vision  des  vertebres,  Paris 
(1943). 
Schultze.      Strieker's  Manual  of  Human 
and  Comp.  Histol,  London,  3  (1873). 
Slonaker.    J.  Morphol,  13,  445  (1897). 
V.  Szily.      V.  Graefes  Arch.  Ophthal,  107, 

317  ;    109,  3  (1922). 
Tanaka.    Jap.  J.  med.  Sci.,  I  Anal,  7,  95, 

133  (1938). 
Teulieres  and  Beauvieux.       Arch.  Ophtal, 

48,  465  (1931). 
Thomson.     Trans,  ophthcd.  Soc.  U.K.,  48, 

293  (1928). 
Tiemeier.    J.  Morphol,  86,  25  (1950). 
Treviranus.     Ueber  d.  Theorie  d.  Sehens  u. 
il.  d.  innern.  Bau  d.  Netzhaut  d.  Auges, 
Bremen  (1837). 


BIRDS 


427 


Uyama.       v.   Graefes  Arch.  Ophthah,  135, 

240  (1936). 
Virchow.     Anat.   Hefte,  Abt.   II,   10,   720 

(1901). 
Waelchli.      v.  Graefes  Arch.  Ophthal.,  27, 

303  (1881)  ;   29,  205  (1883). 
Wagner.     Abh.  bayer.  Akad.  wiss.,  Math.- 

phijs.,  2,  270  (1837). 
Walls.     Arch.  Ophthal.  (Chicago).  18,  912 

(1937). 
The  Vertebrate  Eye,  Michigan  (1942). 
Walls  and  Judd.    Brit.  J.  Ophthal,  17,  641 , 

705  (1933). 
Wedin.    Acta  Anat.,  18,  30  (1953). 
Wehner.      Z.   Anat.   Entw.   Ges.,   69,   250 

(1923). 


Wilkinson.     Proc.  Linn.  Soc.  Lond.,  160, 

94  (1949). 
Wittich.     V.  Graefes  Arch.  Ophthal.,  2(1), 

124  (1855). 
Wood.       The     Fundus     Oculi     of    Birds, 

Chicago  (1917). 
Wychgram.      Arch,   vergl.   Ophthal.,  3,   22 

(1913)  ;    4,  282  (1914). 
Yamamoto.     Acta  Soc.  ophthal.  Jap.,  58, 

586  (1954), 
Zalmann.     Konigl.  Akad.   Wiss.,  Amster- 
dam, 30,  106  (1921). 
Zietzschmann.     Arch,  vergl.  Ophthcd.,  1,  9 

(1910). 


428 


THE   EYE   IN  EVOLUTION 


^-^r/,,^ 


^yfli^X? 


r^i^2^    .^^^^^-^-^ 


Fig.  535. — George  Lindsay  Johnson  (1853-1943). 


CHAPTER  XV 
THE  EYES  OF  MAMMALS 


The  portrait  of  geobge  lindsay  johnson  (1853-1943)  (Fig.  535)  seems 
to  be  a  suitable  introduction  to  this  chapter  on  the  mammaUan  eye.  He  was 
one  of  those  extraordinary  people  whose  life  was  full  of  interest  and  odd 
happenings.  Born  in  England,  in  Manchester,  he  received  much  of  his  early 
education  in  Germany  and  for  that  purpose  was  in  Strasbovu-g  when  it  was  taken 
by  the  Germans  in  1870.  Thereafter  he  completed  his  medical  studies  and 
ophthahnic  training  in  London,  leaving  in  1911  for  South  Africa  where  he  died 
at  the  age  of  90.  In  London  he  spent  most  of  his  spare  time  in  the  Zoological 
Gardens  where  he  stvidied  intensively  the  comparative  anatomy  of  the  eye, 
making  contributions  to  the  Royal  Society  on  the  eyes  of  Reptiles,  Amphibians 
and  Mammals.  This  interest  he  maintained  to  the  end.  So  enthusiastic,  indeed, 
was  he  that  at  an  advanced  age,  determined  to  observe  the  fundus  of  the  whale 
in  life,  he  joined  a  whaling  expedition,  had  a  special  crane  built  on  the  deck  of 
the  ship  and  had  himself  lowered  over  the  back  of  the  animal  so  that  he  could 
sketch  its  fundus.  His  Pocket  Atlas  of  the  Fundus  Oculi  is  well  knowTi  ;  and  his 
extraordinary  versatility  is  exemplified  in  the  many  optical  instruments  which 
he  devised  as  well  as  his  pioneer  work  in  colour  photographj%  a  subject  in  which 
he  maintained  an  interest  to  the  end  of  his  life. 


1VIAM1VIAI.IA,  the  highest  class  of  the  Vertebrates,  have  evolved  from  primitive 
Reptiles  on  diverging  lines  from  the  Birds^;  both  classes  show  high  adaptations, 
and  if  the  Birds  possess  the  air.  Mammals  possess  the  earth  although  a  few  have 
taken  to  the  air  and  more  to  the  trees,  while  others  have  become  amphibious  or 
aquatic.  The  Mammals,  however,  have  two  distinctive  peculiarities — the 
elaboration  of  the  brain  and  the  intimate  organic  connection  between  mother 
and  offspring.  They  possess  in  common  several  characteristic  features — a 
covering  of  hair,  a  diaphragm  and  a  foi.u'-chambered  heart,  three  auditory 
ossicles  and  a  three-chambered  ear,  a  single  jaw-bone,  and — a  circumstance 
peculiar  to  Mammals — the  young  are  nourished  by  milk  secreted  from  the  female 
mammary  gland.  The  eyes  are  not  so  fully  develoj^ed  as  those  of  Birds,  but 
their  comparative  anatomical  simplicity  is  more  than  compensated  functionally 
by  the  efficiency  of  the  central  nervous  organization  of  vision. 

From  the  ocular  point  of  view — and  from  practically  every  other  point 
of  view — the  extant  members  of  the  class  are  divided  into  three  subclasses,  which, 
it  should  be  remembered,  are  not  linearly  derived  the  one  from  the  other  : 

( 1 )  The  PEOTOTHERiA  or  MONOTREMES  which  are  oviparous,  the  yoi.mg  being 
hatched  from  eggs  outside  the  body. 

(2)  The  METATHERiA  or  MARSUPiAXS,  in  which  the  young  are  born  in  an 
immature  state  and  are  (generally  but  not  invariably)  nourished  and  protected 
for  some  time  in  an  external  pouch  (or  marsupium). 

(3)  The  EUTHERiA  or  placentaxs,  in  which  the  young  are  nourished  within 
the  uterus  through  the  placenta  until  development  is  far  advanced.  It  is  among 
the  Placentals  that  cerebral  advancement  begins  to  be  marked. 

1  p.  234. 

429 


430 


THE   EYE   IN   EVOLUTION 


Fig.  536. — The  Platypus,  Orsithorhtxchus  (tVoin  Burton's  Story  of  Animal 
Life,  Elsevier  Pub.  Co.). 


>'A1 . — The  Echidna,  TACHraLOssun  (from  Burton's  Slory  of  Aitmuil 
Life,  Elsevier  Pul).  f"o.). 


MAMMALS  431 

The  eyes  of  these  three  tyjjes  differ  considerably,  those  of  the 
first  two,  particularly  the  Monotremes,  exhibiting  many  features 
characteristic  of  their  reptilian  ancestors  adapted  for  nocturnality. 

THE    MONOTREME    EYE 

THE  MONOTREMES  are  the  most  primitive  of  Mammals  and  include  two  types 
(Figs.  536-7)  :  the  duck-mole  or  duck-billed  platypus  {Ormthorh yncltus) ,  found  in 
the  rivers  and  lakes  of  Australia  and  Tasmania,  a  shy  creature  with  an  enormous 
fiat  bill,  which  spends  most  of  its  time  grubbing  for  small  animals  in  the  muddy 
bottoms  ;  and  the  spiny  ant-eaters  (the  echidna,  Tachyglossus,  found  in  Australia, 
New  Zealand  and  New  Guinea,  and  its  near  relative,  Zaglossus,  found  only  in 
New  Guinea),  nocturnal  ant -eating  creatures  burrowing  in  rocky  regions. 
Neither  relies  primarily  on  vision  ;  the  platypus  relies  largely  on  hearing,  the 
eyes  being  closed  when  submerged,  but  the  vision  appears  to  be  acute  during 


Fig.  538. — Diagram  of  a  Monotreme  Eye. 

A,  small  annular  pad  ;   Ch,  choroid  ;   ON,  optic  nerve  ;   S,  scleral  cartilage; 
Sc,  sclera  ;    SM,  sjDhincter  muscle  ;    VS,  ciliary  venous  sinus. 


the  twilight  hours.    Vision  can  be  only  of  secondary  importance  to  the  nocturnal 
ant-eater  with  its  keratinized  cornea. 

The  monotreme  eye  has  many  affinities  with  the  eyes  of  Rejjtiles 
which  it  resembles  much  more  than  the  tyj)ical  eye  of  Mammals  ;  the 
eye,  indeed,  is  that  of  a  reptile  in  a  mammal.  There  are  only  two 
outstanding  differences  between  it  and  the  reptilian  eye.  The  first 
concerns  the  intra-  and  extra-ocular  musculature,  the  former  being 
confined  to  a  spliincter  of  smooth  fibres,  the  latter  including  a  superior 
oblique  muscle  arising  from  the  apex  of  the  orbit.  In  the  second  place, 
the  (otherwise  typically  rei)tilian)  retina  is  completely  avascular 
without  any  cone-like  structure  nor  any  participation  of  a  hyaloid 
system  in  its  nutriment.  There  has,  however,  been  comparatively  little 
work  devoted  to  the  subject — Marcus  Gunn  (1884)  (the  specimen  sent 
from  Australia  to  London  preserved  in  Scotch  whisky),  O'Day  (1938- 
52)  and  Newell  (1953)  on  Ornifhorhynchus,  and  Owen  (1868)  (macro- 


432 


THE   EYE   IN   EVOLUTION 


Fig.   539. — The   Eye   of  the   Platypus,   Ornithobhynchvs   (Xll)    (O'Day). 


540. — The  Eye  of  the  Echidna,   Tachtglossvs  ( X  7)  (O'Day). 


MAMMALS 


433 


Fig.    541. — The   Posterior   Segment   of   the    Globe   of   the   Platypus. 

ch,  choroid  ;    /,  orbital  fat  ;    r,  retina  ;    s,  scleral  cartilage  ;    sc,  fibrous 
sclera  (  X  126)  (O'Day). 


scopic  examination),  Kolmer  (1925-36),  Franz    (1934),    Gresser   and 
Noback  (1935)  and  O'Day  (1938-52)  on  the  echidna  (Figs.  538  to  540). 

THE  GLOBE  OF  THE  EYE  is  roughly  Spherical,  the  sclera,  as  in  most 
Reptiles,  having  a  well-formed  cartilaginous  cup  extending  forwards 
to  a  little  behind  iTachyglossus)  or  to  the  level  of  the  ora  (Zaglossus) 
or  to  the  level  of  the  ciliary  processes  {Ornithorhynchus)  ;  it  is  perforated 
to  allow  the  transmission  of  the  optic  nerve, 
and  the  intra-ocular  vessels  and  nerves  (Fig. 
541).  This  is  the  only  instance  of  a  scleral 
cartilage  among  the  Mammals.^  The  corneal 
epithelium  of  the  echidna  is  heavily  kera- 
tinized like  that  of  other  ant-eaters  (the 
armadillo,  Xnarthia,  and  the  aard-vark, 
Orycteropus),  possibly  as  a  protection  against 
the  formic  acid  with  which  ants  defend 
themselves.  As  in  aquatic  Vertebrates 
generally,  the  corneal  epithelium  of  the 
platypus  is  thick  and  Bowman's  membrane 
is  absent.  The  anterior  ends  of  the  ciliary 
processes  are  connected  by  a  shelf-like 
structure  running  circumferentially  around 
the  globe  (the  Sims  of  Virchow,  1886  ;    the 

^  With  the  exception  of  the  cartilaginous  nodules  in  Notoryctes,  p.  438. 

S.O.— VOL.  T.  28 


Fig.  542. — The  Ciliary  Pro- 
cesses of  Echidna 

C,  ciliary  body  ;  CS, 
ciliary  shelf ;  I,  iris  ;  S, 
sphincter  muscle  (after 
Franz,  1911). 


434 


THE   EYE   IN   EVOLUTION 


Figs.  543  and  544. — The  Ciliary  Body  of  Monotremes. 


Fig.   543. — The  ciliary  body  of  the  jjlatypus. 
Note  the  large  ciliary  venous  sinus  in  the  connective  tissue  filling  the 
angle  of  the  anterior  chamber.     The  small  annular  pad  in  the  lens  is  seen  to 
the  right  (O'Day). 


Fig.   544. — The  ciliary  body  of  tVie  echidna. 
The  ciliai'v  venous  sinus  is  much  smaller  (O'Day). 


MAMMALS 


435 


ciliary  iveb  of  Walls.  1942) — a  mammalian  characteristic  (Fig.  542).  As 
in  SaurojDsida  generally,  the  connective  tissue  of  the  ciliary  region  runs 
forwards  to  be  inserted  into  Descemets  membrane  and  embedded  in 
this  lies  the  ciliary  venous  sinus,  a  structure  more  pronounced  in 
Placentals  ^  (Fig.  543).    The  brown  iris  is  tenuous,  consisting  merely  of 


IJCxi  *•  I 


*^W         ,^.       ^ 


,     3 


^'msmwii!^*^^^ 


Fig.  545. — The  Retina  of  the  Platypus. 

1,  optic  nerve  fibre  layer  ;  2,  ganglion  cells  ;  3,  inner  plexiforni  laj-er  ; 
4,  inner  nuclear  laj'er  ;  5,  outer  plexiforni  layer  ;  6,  outer  nuclear  layer  ; 
7.  external  limiting  membrane  ;  8,  visual  cells  ;  9,  jaigmentarv  epithelium  ; 
10,  choroid  (O'Day). 


-■.*K^ 


,:'-   r 


■^^' 


«H 


:i.    . 


.4,1 


F-:*^* 


Fig.  546. — The  Retina  of  the  Echidna. 

1,  optic  nerve  fibre  layer  ;  2,  ganglion  cells  ;  3,  inner  j^Iexiforni  laj'er  ; 
4,  inner  nuclear  layer  ;  5,  outer  plexiforni  layer  ;  6,  outer  nuclear  layer  ; 
7,  external  limiting  membrane  ;    8,  visual  cells  (O'Day). 

1  p.  472. 


436 


THE   EYE   IN  EVOLUTION 


the  two  epithelial  layers  and  some  radial  blood  vessels  lying  in  loose 
connective  tissue.  The  sphincter  muscle,  comprised  of  the  unstriated 
fibres  characteristic  of  Mammals,  is  massive  ;  it  constitutes  the  only 
intra-ocular  muscle  for  a  dilatator  or  cihary  musculature  is  absent,  nor 
is  any  accommodative  mechanism  present. ^ 

Except  in  the  aquatic  platypus,  the  lens  is  relatively  small  and 
flat  and  the  zonular  fibres,  arising  from  the  coronal  zone  of  the  ciliary 
body,  are  inserted  into  its  equator.  In  this  region  the  subcapsular 
epithelium  is  tall,  twice  as  tall  as  at  the  anterior  pole,  to  form  a 
miniature  annular  pad,  a  characteristic  of  Reptiles  (Fig.  543). 

The  retina  is  entirely  avascular,  dependent  on  the  choroid  for 
nutriment.     Ophthalmoscopically  the  fundus  of  the  echidna  is  of  a 


Fig.     547. — The    Visual    Elements 
OF  THE  Platypus. 

Showing  double  and  single  cones 
(the  latter  in  the  centre)  and  the  long 
slender  rods  (O'Day). 


Fig.  548. — A  Visual  Element  from 
THE  Pure-rod  Retina  of  the 
Echidna  (O'Day). 


uniform  brownish  colour  with  a  chalky -white  oval  optic  disc  from  which 
nerve  fibres  radiate  ;  it  thus  closely  resembles  a  common  sa-uropsidan 
type  (Johnson,  1901)  (Plate  XIII,  Fig.  1).  The  visual  elements  are 
sauropsidan  in  character  :  the  platypus  has  a  duplex  retina,  the  rods 
and  cones  being  in  approximately  equal  numbers.  The  cones  are  both 
single  and  double  with  oil-droplets  in  the  former  and  in  the  chief 
member  of  the  latter,  but  with  no  paraboloids  ;  the  echidna  has  a 
pure-rod  retina  with  no  oil-droplets  (Figs.  545  to  548).  In  neither 
genus  is  there  evidence  of  an  area  centralis  or  a  fovea.  In  the  optic 
nerves  of  the  platypus  there  are  some  32,000  fibres  (Bruesch  and  Arey, 
1942). 

THE  OCULAR  ADNEXA  are  sauropsidan  apart  from  the  extra-ocular 
muscles.     The  lids  are  thick  and  well-formed  ;     the  echidna  has  a 

'  A  dilatator  is  also  absent  in  Crocodilians  and  Marsupials. 


PLATE  XIII 

The  Fundi  of  INIoxotremes  and  Marsupials 
(Lindsay  Johnson) 


Fio.   I.    -Tlir  Eeliidna. 


Fig.  '2. — 'i'he  rufous  rat -kangaroo, 

Hi/ji.si/iii/tninis  nifesceiis. 


Fig.  o. — The  squirrel-like  phalanger, 
Bdlihiis  scinnis. 


Fig.  4. —  The  Virumiau  ii|h,ssuiii, 
I)/(/t  l/ili//-^  virijiuiiniii . 


:.n. — VOL,  I 


Fig.    ;■). — The    Tasnianian    dcx-il.    SarcojiltiUi-'^ 
ur.'iiiiii.s. 

I  To  face.  p.  4:i(i. 


MAMMALS 


437 


tarsus  in  the  lower  lid  only  ;  the  platypus  in  neither  (Newell,  1953). 
Lacrimal  and  harderian  glands  are  said  to  be  present  in  both.  The 
platypus  has  a  well-formed  and  quite  opaque  nictitating  membrane  ; 
the  ant-eater  has  none.  The  eye  of  the  echidna,  however,  has  a 
habit  of  rolling  inwards  and  retracting  into  the  socket  rhythmically, 
an  action  aided  by  squeezing  the  lids  (Johnson,  1901)  ;  the  same  pro- 
tective phenomenon  is  seen  in  Edentates,  the  bandicoot  and  the 
porcupine.  Both  have  the  usual  six  extra-ocular  muscles  in  addition 
to  a  retractor  bulbi  muscle  ;  but  the  superior  oblique  muscle  is 
essentially  mammalian  in  type.  It  will  be  remembered  that  in  Verte- 
brates below  Mammals  the  recti  take  origin  from  the  apex  of  the  orbit, 
the  obliques  from  its  anterior  part^;  in  Monotremes  the  superior 
oblique  arises  close  to  the  origin  of  the  recti  and  is  threaded  through  a 
pulley  in  the  supero -medial  aspect  of  the  anterior  part  of  the  orbit  so 
that  it  runs  sharply  backwards  towards  the  temporal  aspect  of  the 
globe.  This  typically  mammalian  form  is  supplemented  in  the  echidna 
by  a  second  muscular  slip  running  to  the  globe  directly  from  the 
anterior  nasal  orbital  wall,  a  relic  of  the  sub-mammalian  arrangement. 
The  orbit  in  the  platypus  is  merely  a  shallow  depression  at  the 
cephalic  extremity  of  the  combined  temporo-orbital  fossa,  provided 
only  with  dorsal  and  median  walls  and  without  an  interorbital  septum 
— a  non-mammalian  configuration  (Watson,  1916  ;  Kesteven  and 
Furst,  1929  ;  de  Beer  and  Fell,  1936).  There  is  no  optic  foramen,  for 
the  optic  and  other  cranial  nerves  leave  the  skull  through  a  large 
pseudo-optic  foramen  (Watson,  1916  ;   Hines,  1929). 


THE   MARSUPIAL   EYE 

The  MAESUPiALS  (metatheria) — in  the  Eocene  period  a  large  and  wide- 
spread group — are  today  found  only  in  Australasia  with  the  exception  of  the 
American  opossums  (Didelphyidaj),^  arboreal,  rat-like  animals  found  in  Central 
and  South  America,  and  the  Selvas  (Ctenolestes),  a  primitive  family  until  recently 
believed  extinct,  found  in  South  America.  In  Australasia,  however,  where 
competition  from  the  higher  carnivorous  Mammals  has  not  occurred,  there  are 
many  forms — (a)  the  cat-like  dasyures  (Dasyuridte)  (including  the  squirrel-like 
banded  ant-eater,  Myrmecohius,  and  the  Tasmanian  devil,  Sarcophilus);  (b)  the 
burrowing,  mole-like  Notoryctidsc  ^  ;  (c)  the  burrowing,  rabbit-  or  rat-like 
bandicoots  (Peramelidte)  ;  (d)  the  squirrel-like  arboreal  Phalangeridse,  including 
the  flying  phalangers,  Petaurus  and  Acrobates  (Phalangerinse),  the  bear-like 
wombats  (Phascolomyinfe),  and  the  koala  (Phascolarctinje)  ;  and  (e)  the  unique 
kangaroos  and  wallabies  (Macropodidse). 

'  p.  277,  Fig.  293. 

^  Incidentally,  among  the  American  opossums,  the  pouch  is  generally  absent,  and 
the  young  are  carried  on  the  back  of  the  mother,  their  tails  coiled  round  hers. 

'  Notoryctes  typhlops,  the  marsupial  mole,  has  vestigial  eyes,  less  than  1  mm.  in 
diameter,  which  lack  lens,  vitreous  and  visual  cells,  p.  733. 


Banded  ant-eater, 
Myrmecohius 


Marsupial  mole, 
Notoryctes 


438 


THE   EYE   IN   EVOLUTION 


Spotted  cuscus, 
Phalanger 
mactdatus 


The  eyes  of  Marsupials  represent  a  transition  between  the  wholly 
rejDtilian-like  eyes  of  Monotremes  and  the  mammalian-like  eyes  of 
Placentals.  The  globe  is  spherical  and  the  sclera  fibrous  like  that  of 
snakes,  the  ciliary  musculature  shows  a  reptilian  ancestry  but  the 
structures  accessory  to  reptilian  accommodation  have  all  been  lost, 
the  retina  may  have  a  vascularization  either  of  the  reptilian  or  mammal- 
ian type,  a  retinal  tapetum  as  occurs  in  some  Reptiles  may  be  present, 
and  the  visual  elements,  closely  resembling  those  of  Monotremes,  are 
tyjjically  rej)tilian. 


Fig.  549. — The  Eye  of  the  Wallaby  (  x  5)   (O'Day). 


Dasyure, 
Dasyurus 


Tasmanian  devil, 
Sarcophilus 


THE  GLOBE  OF  THE  EYE  is  Spherical  or  almost  sj^herical,  with  a 
large  cornea  and  a  fibrous  sclera  without  cartilaginous  or  osseous 
suj)ports  ;  the  marsupial  mole,  Notoryctes,  has  cartilaginous  nodules 
in  the  sclera.  There  is  no  Bowman's  membrane  but  a  thick  Descemet's 
membrane.  The  choroid  is  of  the  mammalian  type  with,  in  a  few 
species,  a  tapetum  fibrosum  (the  flying  phalanger,  Petaurus,  and  some 
of  the  Dasyuridse — the  cat-like  Dasyurus,  the  Tasmanian  wolf, 
Thylacinus,  the  Tasmanian  devil,  Sarcojjhilus).  In  Dasyurus  this 
extends  over  the  entire  funchis  but  is  fimctional  only  in  the  upper  half 
where  the  retinal  epithelium  is  devoid  of  pigment.  The  ciliary  body 
is  well  formed  and  provided  with  j^rocesses,  and  a  ciliary  musculature 
is  always  present  despite  the  fact  that  no  accommodation  has  yet  been 
"nnstrated  in  any  member  of  the  group  (Figs.  550-1).  Sometimes 
3  disposed  as  in  Reptiles,  com2:)rised  of  a  meridional  muscle  (of 


MAMMALS 


439 


Fig.  550. — The  Ciliary  Region  of  the  Wallaby. 

Showing  tlie  well-formed  ciliary  processes,  the  meridional  muscle,  and 
the  well-formed  fibres  of  the  pectinate  ligament  traversing  the  deep  ciliary 

cleft  (  X  60)  (O'Day). 

Briicke)  arising  from  the  cornea  ;  more  often  circular  fibres  are 
added  anteriorly  {Dasijiirus  ;  the  opossums,  Marmosa,  Dideljihi/s,  etc.). 
The  iris  is  densely  j^igmented  and  richly  vascularized  with  many  vessels 
standing  out  from  the  anterior  sm'face  ;  the  pupil  is  round  (in  Dasynrus 
viverrinus  the  contracted  pupil  is  a  vertical  slit)  and  a  sjDhincter  of 
unstriated  muscle  surrounds  the  puijillary  margm  but  a  dilatator  is 
absent.  In  the  bandicoot,  Perameles,  nij>ple- 
like  cystic  protrusions  of  the  pigmented  retinal 
layers  form  flocculi  ^  around  the  pupillary 
margin.  The  angle  of  the  anterior  chamber  and 
the  circumferential  ciliary  venous  sinus  are  of 
the  mammalian  type  (Fig.  550). 

The  lens  is  comparatively  large,  flat  in 
diurnal,  round  and  almost  filling  the  interior  of 
the  globe  in  the  smaller  nocturnal  types  ;  there 
are  often  traces  of  the  amiular  j)ad  of  Reptiles, 
but  it  never  touches  the  ciliary  processes  as  is 
characteristic  of  Sauropsida. 

The  type  of  retinal  vascularization  varies. 
Usually  this  structure  is  avascular,  and,  as  if 
in  compensation,  the  choroidal  vessels  are  so 
large  as  to  be  easily  seen  ophthalmoscopically 
(except  in  some  jDhalangers)  ;   frequently  there 

1  p.  469. 


Opossum, 
Didelphys 


Fig.  551. — The  Ciliary 
Processes  of  the 
Kangaroo,  Macropus 
A(uus  (after  Franz, 
1911). 

I,     iris  ;       CS,     ciliarj' 
shelf. 


440 


THE   EYE   IN   EVOLUTION 


Wallaby, 
Petrogale 


are  fine  vessels  on  the  optic  disc,  sometimes  (as  in  the  kangaroo  and 
wallaby)  projecting  like  a  dome-shaped  cushion  above  it  resembling  a 
vestigial  reptilian  cone.^  In  those  species,  however,  wherein  the 
choroid  is  under-developed  (the  flying-phalanger,  Petaurus)  or  is 
insulated  from  the  retina  by  an  impermeable  retinal  tapetum,  a 
mammalian-like  retinal  circulation  exists,  paired  arteries  and  veins 
radiating  from  the  disc  in  the  inner  layers  of  the  retina,  clothed  in 
glial  sheaths  and  protruding  somewhat  into  the  vitreous  ;  in  the 
opossum,  Didelphys,  the  capillaries  penetrate  through  the  entire 
thickness  of  the  retina  to  the  external  limiting  membrane  (Plate  XIII). 


Fig.  552. — The  Visual  Cells  of  an  Australian  Marsupial. 

The  native  cat,  Dasyurus  viverrinus.  1,  outer  nuclear  layer  ;  2,  external 
limiting  membrane  ;  3,  visual  cells,  showing  the  filamentous  rods  and  the 
single  and  double  cones  with  oil-droplets  (in  both  members  of  the  latter) 
(O'Day). 


Koala, 
Phascolarctus 


In  the  Virginian  opossum,  Didelphys  virginiana,  a  retinal  tapetum 
exists,  a  unique  phenomenon  among  Mammals  apart  from  the  fruit- 
bat,  Pteropus.  The  tapetum  is  in  the  form  of  a  semi-circle  with  its 
straight  horizontal  lower  edge  at  the  level  of  the  disc  ;  in  this  area  the 
epithelial  cells  are  tall,  devoid  of  pigment  and  packed  with  guanine-like 
crystals  of  unknown  chemical  nature.  The  visual  cells  are  reptilian  in 
type  and  resemble  those  of  the  monotreme  eye  (O'Day,  1936-39)  ;  the 
retina,  in  fact,  is  that  of  a  Sauropsidan  in  the  eye  of  a  Mammal  (Figs. 
552-3).  The  rods  are  filamentous  and  outnumber  the  cones  which  are 
either  single  or  double  in  type,  lacking  paraboloids  but  possessing  oil- 
droplets.  It  is  interesting  that  in  all  Australasian  types  so  far  examined 
t:=  -  double  cones  have  oil-droplets  in  both  members  ;    this  is  a  rare 

^  p.  362.     Compare  also  the  Rodents,  p.  481. 


MAMMALS 


441 


condition  which  occurs  only  exceptionally  in  American  Marsupials  and 
it  is  noteworthy  that  in  American  opossums  some  of  the  single  cones 
lack  oil-droplets.  It  is  also  interesting  that  among  Mammals  only  the 
Monotremes  and  Marsupials  have  either  double  cones  or  oil-droplets. 


Fig.  553. — The  Visual  Cells  of  an  American  Marsupial. 

The  American  mouse-opossum,  Marmosa  mexicana,  showing  (from  left 
to  right)  a  single  cone  with  oil-droplet,  a  single  cone  without  oil-droplet,  a  double 
cone  with  an  oil-droplet  in  one  member,  and  a  long  filamentous  rod  (  X  1,000) 
(Gordon  Walls). 


Wombat, 
Phascolomys 


THE  OCULAR  ADNEXA  have  received  little  attention.  A  poorly 
developed  nictitating  membrane  is  present,  a  harderian  and  a  lacrimal 
gland  as  well  as  a  retractor  bulbi  muscle.  The  Virginian  opossum, 
Didelphys  virginiana,  has  no  true  nictitating  membrane  ;  two  folds  of 
conjunctival  tissue  arising  from  either  canthus  close  over  the  eye  in 
the  mid-line  while  the  globe  retracts  into  the  socket.  In  other  forms 
(the  bandicoot,  Perameles)  when  the  eye  is  touched  the  globe  rolls 
backwards  and  retracts  as  the  nictitating  membrane  flashes  over  it,  the 
lids  sometimes  closing  over  it  at  the  same  time. 


Rabbit  bandicoot, 
Peragale 


THE   PLACENTAL   EYE 

The  PLACENTALS  (eutheria)  Comprise  the  vast  majority  of  Mammals 
and  include  a  multitude  of  types.  These  can  be  arranged  in  15  orders,  the 
enumeration  of  which  will  facilitate  understanding  of  the  subsequent  discussion. 

(1)  insectivora,  the  most  primitive  type  of  Placentals  found  widely  in 
temperate  and  tropical  lands  except  S.  America  and  Australasia  (where 
insectivorous  opossums  exist). 

The  most  widely  known  representatives  are  the  true  shrews  (Soricidse),  the 
true  moles  with  vestigial  eyes  (Talpidse)  including  the  water-moles  or  desmans 
{Myogale),  and  the  hedgehogs  (Erinaceidae).  Further  types  are  the  otter-shrew 
of  W.  Africa  {Potamogale),  the  oriental  tree-shrews  (Tupaiidse)  (sometimes  classed 
among  the  Prosimians),  the  elephant-shrews  (Macroscelidae)  of  Africa  with  very 


442 


TYPICAL    MAMMALS  :   1 

{Drawn  not  to  scale  hut  to  a  standard  size) 

INSECTIVORA 


Golden  mole 


-;^.:^^ 


Tree -shrew 


CHIROPTERA 


DEKMOPTERA 


PRIMATES 


Flying  fox 


Flying  lemur 


Lemur 


Tarsier 


EDENTATA 


Armadillo 


Pangolin 


RODENTIA 


Aard-vark 


Beaver 


Porcupine 


Vizcacha 


MAMMALS  443 

large  eyes,  and  the  golden  mole  of  S.  Africa  {Chrysochloris),  the  eyes  of  which  are 
small  and  hidden  under  the  skin.  There  are  two  further  and  little  known 
representatives  extant — the  tenrecs  of  Madagascar  and  Solenodon  of  Cuba  and 
Haiti.  Most  are  terrestrial,  some  are  burrowers,  some  (the  tree-shrews)  arboreal, 
and  a  few  aquatic  {Myogale,  Potamogale).  Most  feed  on  insects  ;  some  arboreal 
forms  eat  leaves  as  well  ;   the  moles  eat  worms  ;   and  the  otter-types,  fish. 

From  the  Insectivora  three  orders  are  directly  derived — the  Chiroptera,  the 
Dermoptera  and  the  Primates. 

(2)  CHIROPTERA  (bats),  the  only  Placentals  capable  of  active  flight  ;  the 
arms  and  the  fingers,  with  the  exception  of  the  first,  the  hindlegs  and  (in  the 
Microchiroptera)  the  tail,  support  a  fold  of  skin  which  constitutes  the  wing. 

Two  sub-orders  exist  :  (1)  the  large  megachiroptera — the  huge  flying  foxes 
of  Africa  and  the  Pacific  countries  (Pteropus)  with  a  wing-span  of  up  to  5  feet 
and  large  eyes  (Fig.  750),  the  giant  bats  of  India  (Cynopterus)  and  of  the  Egyptian 
pyramids  (Xantharjayia)  ;  and  (2)  the  small  insectivorous  microchiroptera 
found  all  over  the  world — the  British  Vespertilio,  the  American  blood-sucking 
vampire,  Desmodus,  etc. 

(3)  DERMOPTERA  (flying  lemurs),  arboreal  vegetarians  which  glide  from  tree 
to  tree  buoyed  up  by  a  fold  of  hairy  skin  connecting  the  fore  and  hind  limbs. 
They  inhabit  Malaya  and  the  Philippines  (Galeopithecus). 

(4)  PRIMATES.  An  order  derived  from  the  primitive  Insectivores  ;  they 
were  primarily  and  still  mainly  remain  arboreal.  They  comprise  three  sub- 
orders :  the  Lemuroidea,  the  Tarsioidea  and  the  Anthropoidea,  the  flrst  being 
the  most  primitive  and  the  last  the  most  advanced  ;  the  first  two  are  frequently 
known  as  Prosimians,  the  last  constitvites  the  Simians. 

(a)  LEMUROIDEA,  Small  nocturnal  lemurs  of  Ethiopia  and  the  East,  have 
many  primitive  characters  in  common  with  the  Tvipaiidte  with  which  they  seem 
to  have  had  a  common  origin.  They  fall  into  two  groups — true  leinurs 
(Lemuridfe)  confined  to  the  island  of  Madagascar,  and  the  Lorisidoe,  never 
foimd  in  Madagascar — Loris  and  Nycticebus  of  the  E.  Indies,  the  potto,  Pero- 
dicticus  (Fig.  752),  and  the  agwantibo,  Arctocebus,  of  W.  Africa,  and  the  bush- 
baby,  Galago,  of  Africa. 

(b)  TARSIOIDEA,  of  which  there  is  only  one  survivor,  the  tarsier  (Tarsins), 
differ  from  the  lemurs  among  other  things  in  having  the  orbit  directed  forwards 
and  almost  completely  separated  from  the  temporal  fossa.  They  are  generally 
looked  upon  as  a  separate  line  of  evolution  which  branched  off  the  Primate 
stock  at  an  early  period  and  eventually  produced  the  Anthropoids. 

(c)  ANTHROPOIDEA,  comjjrising  5  families  of  essentially  diurnal  species, 
distributed  between  the  New  World  (Platyrrhini)  and  the  Old  (Catarrhini)  : 

(i)  HAPALiDyE — mai'mosets — the  most  primitive  monkeys,  small 
squirrel-like  creatures,  found  in  C.  and  S.  America  ; 

(ii)  CEBiD.E — the  American  monkeys — including  such  species  as  the 
capuchins  (Cebus)  imported  into  Europe  ;  Nyctipithecus 
(Aotes),  the  only  nocturnal  monkey  ;  the  bald-headed  sakis 
(Pithecia)  ;  the  long-liinbed  spider  monkeys  {Ateles)  ;  and  the 
howling  monkeys  (Alouatta)  ; 

(iii)  CERCOPiTHECiD^ — the  Old  World  monkeys,  including  the  African 
baboon  (Papio),  the  mandrill  (Mandrillus),  the  macaques 
(Macaca),  etc.  ; 

(iv)  siMiiD.-E — the  anthropoid  apes,  including  the  gibbon  (Hylobates), 
the  orang-utan  [Pongo),  the  chimpanzee  (Pan),  and  the  gorilla 
{Gorilla)  ; 


444 


Lynx 


TYPICAL    MAMMALS  :    II 

{Drawn  not  to  scale  but  to  a  standard  size) 

CARNIVORA 


Hyaena 


Raccoon 


Coati 


Civet  cat 


Polecat 


Badger 


Sea-lion 


ARTIODACTYLA 


Llama 


Gazelle 


Giraffe 


Chevrotain 


Zebra 


PERISSODACTYLA 


Rhinoceros 


Tapir 


HYRACOIDEA 


Hyrax 


Blue  V 


Hump-back  whale 


Sperm  whale 


Dolphin 


MAM:MALS  446 

(v)  HOMiNiD^,  with  several  extinct  genera  {Pithecanthropus,  etc.)  and 
the  single  living  genus,  Homo. 

(5)  XENAKTHEA — these  comprise  three  distinct  sub-orders  : 

(a)  the  solitary  nocturnal,  arboreal  sloths  (bradypodid^)  (3-toed 
Bradypus,  or  2-toed  Choloepua)  of  S.  and  Central  America,  vegetarian  in  habit, 
which  spend  a  sluggish  life  hanging  from  the  branches  of  trees  (Fig.  751)  ; 

(b)  the  terrestrial  or  arboreal  ant-eaters  (MYRMECOPHAGiDiE)  of  neo- 
tropical distribution  ; 

(c)  the  omnivorous  nocturnal  armadillos  (dasypodid^),  mainly  of  S. 
America,  with  a  dermal  armature  of  bony  scutes,  which  actively  run  and  burrow. 

(6)  PHOLIDOTA.  The  small  family  of  burrowing,  termite-eating,  scaly 
pangolins  {Manis)  of  Ethiopia  and  the  East. 

(7)  TUBULiDENTATA.  The  equally  small  family  of  shy.  nocturnal,  termite- 
eating  aard-varks  (Orycteropus)  of  Africa,  living  in  burrows. 

The  Xenarthra,  Pholidota  and  Tubulidentata  used  to  be  classed  together 
as  EDENTATA  Owing  to  the  simplicity  of  their  teeth  or  the  lack  of  them. 

(8)  RODENTIA,  the  largest  order  of  Mammals,  comprising  more  than  4,000 
species,  mainly  small,  terrestrial  and  vegetarian,  which  gnaw  their  food  in  a 
characteristic  way.  They  are  represented  by  two  sub-orders^  according  to  their 
dentition  : 

(a)  those  provided  with  two  pairs  of  upper  incisors  (lagomorpha) — the 
rabbit  {Oryctolagus),  the  hare  (Lepus)  and  the  pikas  or  calling  hares  (Ochotona)  ; 

(b)  those  provided  with  a  single  pair  of  upper  incisors,  which  are  con- 
veniently divided  into  three  groups  : 

(i)  the   sciurojiorpha — the  common  squirrel   (Sciurus),   the   souslik 

or   ground    squirrel    (Citellus),    the    prairie-dog    {Cynomys),    the 

flying  squirrel  (Pteromys),  the  marmot  (Marmota),  the  beaver 

(Castor)  ; 

(ii)  the   MYOMORPHA — the   rat    (Rattus),   the   mouse    (Mus).   the  vole 

(Microtua)  ; 
(iii)  the   hystricomorpha — the   porcupine    (Hystrix),    the   guinea-pig 
(Cavia),  the  chinchilla,  the  vizcacha  [Lagostomus) ,  the  coypu 
(Myocastor),  and  others. 

(9)  CARNivoRA.  A  large  amorphous  order  of  active  and  fierce  flesh-eaters 
of  wide  distribution  and  mostly  terrestrial.    It  is  comprised  of  2  sub-orders  : 

(o)  the  terrestrial  fissipedia,  including  7  families  :  the  cat-like  Felidae 
(cat,  lion,  tiger,  leopard,  cheetah,  jaguar,  lynx),  the  Viverridae  (civet  cats,  mon- 
goose, etc.),  the  Hyaenidae  (hyaenas),  the  dog-like  Canidae  (dog,  wolf,  jackal, 
fox,  etc.),  the  bear-like  Ursidae,  the  Procyonidae  (Himalayan  nandas,  and  the 
American  raccoon  and  coati),  and  the  Mustelidae  (otter,  sea-otter,  skunk,  badger, 
marten,  polecat,  ferret  and  weasel,  etc.)  ; 

(6)  the  aquatic  pinnipedia,  marine  flsh-eating  Carnivores,  clumsy  on 
land  where  they  come  for  breeding  purposes  :  Phocidae  (seals),  Otariidae  (sea- 
lions  or  eared-seals),  and  Odobaenidae  (walruses). 

(10)  artiodactyla.  Even-toed  hoofed  animals,  terrestrial  and  herbivorous 
in  habit,  wherein  the  hoof  is  formed  by  the  third  and  fourth  digits  showing  a 
cleft  between.    Of  these  there  are  four  extant  groups  : 

(a)  the  suoiDEA  (pigs  and  boars,  Suidae  ;  peccaries  of  America, 
Dicotylidae  ;   and  the  African  hippopotamus)  ; 

^  The  Lagomorpha  are  now  generally  accepted  as  a  separate  order. 


446  THE   EYE   IN   EVOLUTION 

(6)  the  TYLOPODA  (camel  and  dromedary  of  Africa  and  Asia,  and  the 
llama  of  S.  America)  ; 

(c)  the  PECORA  (Ruminants)  (deer  and  giraffe,  and  the  Bovidee — ox, 
bison,  sheep,  goat,  antelope,  gazelle)  ; 

(d)  the  TRAGULiNA,  Small  chevrotains  of  the  East  and  Africa. 

(11)  PERissoDACTYLA.  Odd-toed  hoofed  animals  wherein  the  foot  is 
essentially  formed  by  the  enlarged  third  digit — Equidse  (horse,  ass,  zebra), 
Rhinocerotidse  (rhinoceros),  Tapiridse  (tap ii"). 

(12)  HYRACOIDEA,  the  Small  rodent-like  hyraxes  ("  coneys  ")  of  Africa  and 
Syria  of  arboreal  habits. 

(13)  PROBOSCIDEA,  the  vegetarian  elephants  of  Africa  {Loxodonta  africaria) 
and  the  Orient  {Elephas  inaximus). 

The  Artiodactyla,  Perissodactyla,  Hyracoidea,  and  the  Proboscidea  used 
conveniently  to  be  classed  in  one  heterogeneous  group  of  ungulata  (hoofed 
animals). 

(14)  siRENiA.i  The  sluggish,  vegetarian,  and  fully  acjuatic  fish-like  sea- 
cows,  which  crop  grasses  in  shallow  littoral  waters — the  manatee  {Manatus  ; 
Trichechus)  of  S.  America  and  S.  Africa,  and  the  dugong  (Halicore)  of  Oriental 
and  Australian  coasts. 

(15)  CETACEA.  The  carnivorous  fish-like  whales  and  dolphins,  fully  adapted 
for  marine  life.     There  are  two  distinct  orders  : 

(a)  the  baleen  whales  (mystacoceti)  with  baleen  (or  whale-bone)  plates 
instead  of  teeth,  which  sound  to  greal  depths  and  feed  blindly  by  trawling  for 
plankton  which  they  strain  through  the  frayed  margins  of  their  plates  (the 
right-whale,  Balcena  ;  the  hump-back,  Megaptera  ;  the  blue  whale  or  rorqual, 
Balcenoptera,  etc.)  ;  the  great  rorquals  (particularly  the  blue  whale)  are  the 
largest  animals  in  existence,  over  100  feet  in  length  and  well  over  100  tons  in 
weight  ; 

(6)  the  toothed  whales  (odontoceti), squid-  and  fish-eating  animals  which 
use  their  vision  to  catch  their  prey  and  are  therefore  adapted  with  more  perfect 
eyes,  some  of  them  swimming  in  packs  like  wolves  attacking  the  unwieldy 
whale-bone  whales  (the  sperm-whale,  Physeter;  the  killer  whale,  Orca;  the  narwhal, 
Monodon  ;  the  porpoise,  Plioccena  ;  the  dolphin,  Delphinus).  There  is  a  small 
family  of  fresh-water  dolphins  (the  susu,  Platanista)  with  rudimentary  eyes. 

Within  the  many  orders  of  Placentals  a  considerable  range  of 
variations  in  the  structure  of  the  eye  occurs,  but  throughout  the  entire 
class  the  similarity  is  great.  It  seems  likely  that  the  first  representatives 
(Insectivora)  were  nocturnal  in  habit,  and  that,  as  occurs  in  snakes, 
the  eye  has  evolved  from  this  as  a  basis  showing  innumerable  adaptive 
changes  to  suit  the  many  environments  (diurnal,  arboreal,  aquatic,  etc.) 
to  wliich  the  prolific  class  has  suited  itself.  Only  in  a  few  instances 
among  the  Insectivores  (moles)  and  Rodents  has  the  burrowing  habit 
led  to  the  degeneration  of  the  eyes.^  The  general  characteristics  of 
the  jDlacental  eye  may  be  summarized  as  follows  (Figs.  554  to  563). 

'  The  legend  of  the  mermaid  is  said  to  derive  from  sailors'  fanciful  descriptions 
of  the  manatee  sitting  on  the  rocks  nursing  its  baby  in  its  arms  ;  hence  the  generic 
name,  Sirenia.  It  is  to  be  remembered  that  a  third  species,  Rhytina  (Steller's  sea- 
cow),  growing  to  enormous  dimensions  (25  feet  or  more),  was  found  in  great  herds  by 
Bering  in  1741  near  the  Asiatic  coasts  of  the  Bering  sea.  Sluggish  and  docile  in  habit 
itbecai.  ■  extinct  at  the  end  of  the  1 8th  century  owing  to  its  wholesale  massacre  for  food. 

"  p.  73.3. 


Figs.  554  to  561. — The  Eyes  of  Placentals. 


Fig.  554. — The  lynx, 
Felis  lynx. 


Fig.   555. — The  seal. 
Phoca  grcenlandicu. 


Fig.  556. — The  marmot, 
Marmota  alpinn. 


Fig.  559.— The  wolf, 
Cams  lujnis. 


Fig.  557. — The  horse, 
Equus  caballus.  Note 
the  flocculus  ill  the 
pupil. 


Fig.  558. — The  porcupine, 
Hystrix  cristata. 


Fig.  560.— The  elephant, 
Elephas  ■maximus. 


Fig.  561. — The  monkej', 
Simia  inuus. 


A  selection  of  Soemmerring's  engravings  illustrating  in  natural  size  the 
lower  half  of  the  liemisected  left  eve  in  each  case. 


448  THE   EYE   IN  EVOLUTION 

The  lack  of  any  scleral  support,  cartilaginous  or  bony,  results  in  a 
spherical  globe. 

The  choroid  is  of  the  standard  vertebrate  type,  usually  thinner  than  that 
of  man,  and  may  contain  a  tapetum.  The  ciliary  body  has  a  variable 
topography,  but  the  ciliary  muscle,  often  vestigial,  is  always  composed  of 
plain  muscle  fibres.  A  peculiarity  is  that  the  anterior  surface  of  the  iris 
is  partially  covered  by  a  mesodermal  leaf  additional  to  that  found  in  other 
Vertebrates.  The  angle  of  the  anterior  chamber  is  continued  by  a  cleft  of 
varying  depth,  extending  into  the  ciliary  region  bridged  across  by  delicate 
strands  of  uveal  tissue. 

The  lens — usually  lenticular  in  shape  but  round  in  aquatic  species — is 
suspended  freely  from  the  ciliary  processes  by  a  well-developed  zonule  and 
is  deformed  in  accommodation  {when  this  function  is  present)  by  the 
elasticity  of  its  capsule,  being  stretched  or  relaxed  by  the  ciliary  muscle. 

The  retina  with  few  exceptions  is  duplex  in  type  and  of  typical 
vertebrate  architecture. 

Most  of  these  characteristics  are  seen  in  some  form  or  another  in 
other  classes  of  Vertebrates  :  in  only  three  features  does  the  placental 
eye  differ  characteristically  from  all  others  : — 

1.  In  the  development  and  fate  of  the  hyaloid  system  of  vessels, 
the  persisting  renmants  of  which  frequently  supply  an  intra -retinal 
system  of  vascularization. 

2.  In  the  formation  of  a  mesodermal  layer  of  the  iris  superficial 
to  the  structures  found  in  other  Vertebrates. 

3.  In  an  accommodative  mechanism  depending  on  a  relaxation 
of  the  tension  normally  maintained  upon  the  capsule  of  the  lens. 

It  is  unnecessary  in  a  volume  of  this  type  to  describe  the  detailed 
morphology  of  the  placental  eye  which  conforms  closely  with  that  of 
man — to  which  an  entire  subsequent  volume  will  be  devoted.  It  will 
suffice  to  describe  those  features  which  show  marked  variations  from 
the  general  scheme  (Figs.  554  to  563). 

The  General  Shape  and  Size  of  the  Olobe,  In  shape  the  placental 
eye  is  spherical,  a  necessity  with  its  fibrous,  unbuttressed  sclera.  As  a 
rule  the  cornea  continues  the  scleral  curve,  although  sometimes  there 
is  a  shallow  corneo -scleral  furrow  with  a  protruding  cornea  having  a 
smaller  radius  of  curvature,  as  in  man  ;  alternatively,  while  the 
peripheral  zone  of  the  cornea  maintains  the  curve  of  the  sclera,  its 
apex  may  be  more  acutely  curved,  as  is  seen  in  Carnivores.  In 
Cetaceans  the  shape  of  the  globe  is  fish-like  ^  with  a  short  antero- 
posterior axis  ;  it  is  interesting  that  the  Pinnipedes,  less  wholly  adapted 
to  an  aquatic  existence  than  the  Cetaceans,  have  a  spherical  globe. 
In  some  nocturnal  prosimian  Primates  such  as  the  lemuroids  (galago 
and  Nycticebus)  and  Tarsius  the  shape  is  almost  tubular  (Fig.  743). 

1  p.  276. 


MAMMALS 


449 


Fig.  562. — Diagram  of  the  Eye  of  a  Placental. 

Ch,  choroid  ;  CM.  ciliary  muscle  ;  OX,  optic  nerve  ;  PL,  pectinate 
ligament  bridging  the  ciliary  cleft  ;  So,  sclei-a  ;  Z,  zonule.  Xote  the  relative 
simplicity  of  the  eye. 


Fig.    563. — Section   of  the   Eye   of  the   Cat   (  x  3-25)    (Xorman  Ashton). 


Tlie  size  of  the  globe  varies  within  wide  Hniits  ;  neglecting  the 
minute  degenerate  eyes  of  the  mole  (0-8  mm.  diam.)  and  one  or  two 
species  of  burrowing  rodents/  it  ranges  from  1  to  2  mm.  in  diam. 
in  the  shrews  and  bats  to  the  enormous  eyes  of  some  whales  (145  x 
129  X  107  mm.  in  the  great  blue  whale,  BalcenojJtera  musculus)  (Putter, 
1903).  In  comparison  with  the  size  of  the  body,  however,  that  of  the 
eye  is  more  uniform  ;  wliile  the  former  varies  as  1  :  60  among 
terrestrial  Placentals,  the  latter  only  varies  as  1  :  30.  The  eye  of 
the  seal  (internal  antero-posterior  diam.,  52  mm.)  is  comparatively 

1  p.  733. 


450  THE   EYE   IN   EVOLUTION 

much  larger  than  that  of  the  whale,  which,  in  fact,  measures  only 
1/250  to  l/600th  of  its  gigantic  body  (Figs.  555,  564)  ;  that  of  the 
elejjhant  (axis  35  mm.)  or  rhinoceros  (axis  23  mm.)  is  correspondingly 
small  (Fig.  560),  and  the  minute  eye  of  the  vole  (axis  175  mm.)  is  rela- 
tively greater  in  comparison  with  the  length  of  its  body  (10  cm.) 
than  is  the  eye  of  man.  Although  as  a  general  rule  Haller's  ratio  ^ — 
that  the  size  of  the  eye  varies  inversely  as  the  size  of  the  body- — holds 
good,  marked  variations  occur  with  the  visual  habits  of  the  animal.  In 
the  lower  orders  of  nocturnal  habits  which  depend  little  on  vision 
(Insectivores,  Chiroptera,  Edentates  and  some  Rodents)  the  eyes  are 
small  relatively  and  absolutely  ;  in  the  more  liighly  developed  and 
visually  alive  types  they  are  larger.  Among  these  it  varies  generally 
with  the  visual  efficiency  and  swiftness  of  movement,  and  is  generally 
larger  in  nocturnal  species.  Thus  the  eye  of  the  nimble  horse  (axis 
45  mm.)  is  larger  than  that  of  the  lethargic  elephant  (axis  35  mm.) 
(Fig.  557),  while  the  small  (usually  nocturnal)  Primates  have  com- 
paratively larger  eyes  than  the  large  diurnal  species  (with  the  con- 
spicuous exception  of  the  Hapalidse — marmosets  and  tamarins) 
(Ashley -Montague,  1943-44)  (Figs.  752  and  753). 

Measurements  of  the  various  placental  eyes  are  found  in  Emniert  (1886), 
Putter  (1903),  Hotta  (1906),  Kolmer  (1910),  Franz  (1912),  Linsenmeyer  (1912), 
Guist  (1923),  Wolfrum  (1926),  Rochon-Duvigneaud  (1943)  and  Steindorff  (1947)  ; 
their  weight  and  volume  in  Liebig  (1874),  Koschel  (1883),  Emmert  (1886), 
Welcker  (1903),  Schleich  (1922),  Vitello  (1931),  Steindorff  (1947)  and  Henderson 
(1950). 

The  corneoscleral  enveloj^e  corresponds  with  that  of  man  with  the 
exception  of  the  aquatic  Placentals,  apart  from  the  generalization  that 
the  eye  of  a  relatively  large  animal  tends  to  have  an  unusually  thick 
sclera — elephant,  rlmioceros,  etc.  The  envelope  is  entirely  fibrous 
without  any  supporting  skeletal  structures.^  Among  the  Cetaceans  par- 
ticularly the  sclera  is  enormously  thick,  a  feature  described  by  Bennett 
(1836)  ;   indeed,  the  sclera  at  the  posterior  pole  may  be  3/4  the  length 

1  p.  401. 

^  Magnitudo  oculorum  est  fere  in  ratione  inversa  animalium.  Bala?n£e,  Rhino- 
ceroti,  Elephanto  parvi  sunt  oculi.     Haller,  Et.  Phys.  IV-XVI  (1768). 

*  A  FIBROUS  SCLERA  is  also  fouiid  ill  Cyclostomcs,  pearl-fishes  and  some  eels,  adult 
Urodeles  (excluding  Triton  and  Hynohius,  and  degenerative  limicoline  types),  some  tree 
frogs,  snakes  and  Marsujjials  (excluding  Notoryctes). 

CARTILAGE  is  found  (rt)  in  the  form  of  a  posterior  cup  in  Fishes  (except  Teleosteans), 
adult  Aiuirans  (except  some  tree  frogs),  larval  Urodeles,  Keptiles  (excluding  snakes 
and  the  chameleon).  Birds  and  Monotremes  ;  (6)  in  the  form  of  a  ring  in  Teleosteans  ; 
(c)  as  islands  in  elephant  fishes,  Triton  and  Hynobius,  limicoline  Urodeles  (enormously 
large),  the  chameleon  (at  the  fovea)  and  Notoryctes;  {d)  calcified  in  some  Selachians 
and  some  Teleosteans. 

BONE  is  found  (a)  as  anterior  ossicles  in  most  Teleosts,  Chondrosteans,  Coelacanths, 
Reptiles  (excluding  snakes  and  Crocodilians)  and  Birds  ;  (6)  in  the  form  of  a  ring  in 
Xiphic-^  snd  Thunnus  (anteriorly),  Hypopaclius,  and  many  Birds  (posteriorly  as  the 
OS  opti 


MAMMALS 


451 


of  tlie  antero-posterior  axis  of  the  globe.  In  the  hump-back  whale, 
Megajitera,  for  example,  the  antero-posterior  diameter  of  the  eye  is 
40  mm.,  the  tliickness  of  the  sclera  at  the  posterior  pole  is  30  mm., 
wliile  its  thickness  at  the  limbus  is  only  3  mm.  (Rochon-Duvigneaud, 
1943)  (Fig.  564).  The  cornea  of  this  species  is  correspondingly  thin 
(1-5  mm.  at  the  jjeriphery  ;  0-5  mm.  at  the  apex).  In  addition,  the 
whale  has  an  immensely  thickened  accessory  optic  nerve  sheath 
composed  of  comiective-fatty  tissue  lying  outside  the  dural  sheath 


Fig.   564. — The  Eye  of  the  Whale. 

A  heniisection  to  sliow  the  enormous  thickening  of  the  .sclera  and  the 
accessory  optic  nerve  sheath.  Note  that  the  relatively  small  lens  is  kept  in  place 
artificially  by  a  glass  strut  (specimen  from  A.  Arruga  ;  Museum,  Institute 
of  Ophthalmology). 


encased  in  a  thick  aponeurotic-like  capsule.  Set  on  this  massive  stalk, 
the  globe,  of  course,  is  immobile.  A  similarly  tliick  accessory  sheath 
surrounds  the  optic  nerve  of  the  elephant  and  the  liippopotamus 
(Rochon-Duvigneaud.  1943)  :  in  both  of  these  the  sclera  is  very  thick 
and  the  eyes  are  capable  of  little  movement. 

The  phenomenal  tliickness  of  the  sclera  in  the  whale  is  often  said  to  be 
necessary  to  resist  the  enormous  pressures  involved  when  the  animal  sounds  to 
great  depths.  It  is  to  be  remembered,  however,  that  the  cornea  is  thin  and  that 
abyssal  fish  do  not  share  this  characteristic  ;  the  sclera  of  the  deeply 
diving  shark,  Etmopterus,  is  niicroscopicalh'  thin  and  that  of  the  Chimteras 
discontinuous.^     It  is  probable,  indeed,  that  reinforcement  in  this  sense  is  un- 

1  p.  290. 


452 


THE   EYE   IN   EVOLUTION 

Figs.  565  to  572. — The  Corneal  Epithelium  of  Mammals. 


Fig.  565. — Rabbit. 


Fig.  566.— Dog. 


^^  Rr 


j*****^ 


Fig.  567. — Guinea-pig. 


^i»4y  .-.  \.. 


Fig.  570. — Horse. 


i#^ 


Fig.  568.— Rat. 


»>«  , 


'#, 


Fig.  569.— Pig. 


,*« 


Ik 


I  > 


*. 


Fig.  571. — Ass. 


Fig.  572.— Ox. 


F^.      565. — Periodic  acid  Schiff's  stain  (Norman  Ashton).  ,  t,     \ 

F;        566  TO  572. — Masson's  trichrome  stain  (Calmettes,  Deodati,  Plane!  and  13ec). 


MAMMALS  453 

necessary  for  the  pressure  on  the  surface  is  equally  transmitted  to  all  the  fluid 
contents  of  the  body  including  the  inner  eye.  It  is  more  likely  that  the  rein- 
forcement of  the  posterior  region  of  the  sclera  is  necessary  to  maintain  the  non- 
spherical  shape  in  the  huge  cetacean  globe  rendered  mechanically  weak  by  ita 
great  size,  thus  taking  over  the  supportive  function  of  the  scleral  cartilage  in 
fishes  with  similarly  shaped  eyes. 

The  cornea  of  Placentals  is  usually  circular  or  almost  so,  but  in 
Cetaceans  and  in  a  great  number  of  the  Ungulates  (Equiclse,  Ruminants 
and  the  liippopotamus)  it  is  horizontally  oval  corresponding  to  the 
configuration  of  the  pupil.  In  many,  a  pigmented  ring  encircles  the 
limbus  sjDreading  a  considerable  distance  into  the  corneal  tissue  ; 
sometimes  this  is  confined  to  epidermal  pigment  (Rodents  such  as 
rabbit,  hare,  guinea-pig,  rat,  marmot,  etc.  ;  the  horse  and  the  gorilla) 
(Fig.  607)  ;  sometimes  to  this  is  added  pigment  in  the  deep  interstitial 
tissues  (Carnivores  such  as  the  cat,  dog,  fox,  lion  ;    Ruminants  such  as 


Fig.   57.3. — The  Endothelium    of  the  Cornea  of  the  Rabbit. 

Showing  a  sheet  of  corneal  endothelium  lining  the  anterior  chamber 
wliich  has  been  stripjjed  away  from  Descemet's  membrane.  No  nerve  tibres 
are  seen  but  there  are  a  few  circular  blobs  of  .stain  lying  between  the  cells 
(  X  400)  (Zander  and  Weddell). 

the  ox  and  deer  ;  the  jjorj^oise,  the  dolphin,  the  whale  and  the 
chimpanzee).  In  the  rhinoceros  the  pigmented  region  of  the  cornea 
is  vascularized.  The  ]iigmentation  may  be  an  anti-glare  device  for  it 
is  absent  in  crepuscular  or  nocturnal  animals. 

The  histological  structure  of  the  cornea  is  biult  on  the  typical 
vertebrate  plan  seen  in  man  excej^t  that  most  species  have  no  Bowman's 
membrane  ;  Descemet's  membrane  with  its  endotheliiun.  however,  is 
always  present  and  is  often  very  substantial.  Although  Bowman's 
membrane  is  a  relative  rarity,  the  basal  membrane  of  the  epithelium 
seems  always  to  be  present  (Calmettes  et  a!.,  1956  ;  Sheldon,  1956). 
The  thickness  of  the  epithelium  varies  considerably  (Figs.  565  to  572)^; 
that  of  the  endothelium  is  constant  (Fig.  573).  Blood  vessels  some- 
times invade  the  cornea  proper  from  the  limbus,  whereas  in  Primates 

1   20  layers  of  cells  in  the  horse  ;    10-12,  pig  ;    9-11,  ox;  8-10,  dog;   6-8,  rabbit  ; 
5-6,  guinea-pig,  rat  (Virchow,  1910  ;    Calmettes  et  al.,  1956). 


Figs.    574  to  576. — Corxkat.  Xerves    of   the   Rabbit  (Zander  and  Weddell). 


Fig.  574. — A  diagrammatic  representation  of  the  arrangement  of  the  nerve 
bundles  which  enter  the  periphery  of  the  cornea  in  different  planes  (methylene 
blue). 

Upper  left  cpadrant  :  the  nerve  bundles  entering  the  cornea  from  the 
episcleral  plane.  Upper  right  qviadrant  :  entering  from  the  subconjunctival 
plane.  The  lower  half  shows  the  manner  in  which  the  plexiform  pattern  of 
nerve  fibres  arises  from  these  bundles.  It  is  to  be  noted  that  they  are  not  by 
any  means  all  radially  disposed  and  that  some  fibres  pass  from  linibus  to 
limbus  across  the  centre  of  the  cornea. 


'^-l 


'11 


Fig.  575. 


Fig. 


Fig.  575. — Terminals  in  the  substantia  propria  arising  from  a  nerve  bundle 
(methylene  blue)  (  X  350). 

Fig.  576. — Nerve  terminals  in  the  epithelium  showing  the  axons  piercing 
1*1  nian's  membrane,  multiplying  and  passing  in  all  directions  in  the 
epi  :    lium.  The  stromal  plexus  is  out  of  focus  (methylene  blue)  (X  130). 


MAMMALS 

they  are  found  only  in  fcetal  life  ;  in  some  animals  they  persist  much 
longer  {e.g.,  cat),  while  in  others  they  may  be  permanent  (ox,  sheep, 
Gerlach,  1848).  In  most  Mammals  the  nerve  plexus  is  more  compli- 
cated than  in  man. 

Since  the  early  observations  of  Schlemm  (1831)  who  demonstrated  nerve- 
fibres  entering  the  cornea  in  stags  and  oxen,  a  considerable  amount  of  work 
has  been  done  on  this  jDroblem.  Most  of  the  early  work  ^  is  unconvincing,  but 
Cohnheim  (1866-67),  by  introducing  the  gold  chloride  impregnation  technique, 
demonstrated  their  presence  and  complexity  in  the  cornea  of  rabbits  and  guinea- 
pigs,  3S  well  as  in  frogs  and  birds.    This  advance  was  followed  by  a  large  number 


455 


.  t  4^-  .V:*  Vv'^^-ik*; 


Fig.   577. — The   Xerves  in  the   Corneal  Endothelium  in  the   Rabbit. 

Flat    section,    fixed    in    bromformalin,    stained   with   del   Rio   Hortega's 
"  jDanoptic  silver  carbonate  technique  "  (J.  R.  Wolter). 

of  contributions  which  were  assessed  in  the  important  papers  of  Waldeyer  and 
Izquierdo  (1880)  and  Ranvier  (1881)  wherein  the  innervation  of  the  cornea  of 
Fish,  Amphibians,  Reptiles  and  Birds  as  well  as  Mammals  was  assessed.  The 
introduction  of  the  inethylene  blue  method  of  staining  nerve  fibres  stimulated 
a  classical  paper  by  Dogiel  (1891)  dealing  with  the  monkey  and  man,  while  a 
considerable  number  of  Mammals  was  studied  using  the  silver  technique  by 
Crevatin  (1903),  Bielschowsky  and  Pollak  (1904)  and  Cajal  (1909).  This  work 
was  consolidated  chiefly  on  Mammals  by  Virchow  (1910),  Agababow  (1912)  and 
particularly  Attias  (1912).  More  recent  studies  using  a  variety  of  techniciues 
including  polarization  and  phase-contrast  microscopy  are  those  of  Boeke  and 
Heringa  (1924)  (monkey),  Nakajima  (1930)  (rabbit),  Egorow  (1934)  (guinea- 
pig),  Boeke  (1935)  (monkey),  Reiser  (1935-37)  (pig  and  guinea-pig),  Borr 
(1939)    (rat),  Peris  (1947-49)    (bull,  sheep,  rabbit,  pig,  cat,  etc.),  Rodger  (1950) 

1  Bochdalek  (1837-39)  (larger  Mammals),  Pappenheim  (1839-40)  (oxen),  Purkinje 
(1845)  (different  Mammals),  Kolliker  (1848-66)  (rabbits),  Lusphka  (1850)  (rabbits), 
Ciaccio  (1863-81)  (mice). 


456  THE   EYE   IN   EVOLUTION 

(rabbit),  Zander  and  Weddell  (1951)  (rat,  guinea-pig,  rabbit,  monkey  and  man, 
as  well  as  the  dogfish,  Scylliuni,  and  the  frog,  Rana),  Rexed  and  Rexed  (1951) 
(rabbit),  Itahashi  (1952)  (rabbit),  BeW  etal.  (1952)  (cat),  Palumbi  (1953)  (rabbit, 
rat,  cow,  horse,  and  man),  and  Wolter  (1955-56)  (rabbit). 

Branches  of  the  ciliary  nerves  derived  from  the  ophthalmic  division  of  the 
trigeminal  enter  the  cornea  at  the  limbus.  After  supplying  a  perilimbal  plexus, 
they  lose  their  myelin  sheaths  and  run  radially  into  the  corneal  stroma  in  some 
70  to  80  nerve-trunks  (Fig.  574).  As  these  branch  they  form  a  plexiform  arrange- 
ment at  all  levels  in  the  stroma,  more  dense,  however,  in  the  siiperficial  layers. 
Some  of  the  branches  terminate  in  the  stroma  in  bead-like  thickenings  (Fig.  575)  ; 
many  of  them  terminate  in  the  corneal  epithelium  penetrating  Bowman's 
membrane  when  this  structure  is  present.  In  this  layer  the  nerve  fibres  shed 
their  sheaths  of  Schwann  and  the  naked  axons  subdivide  to  form  a  delicate 


Fig.  578. — The  Posterior  Segment  of  the  Eye  of  the  Kitten. 

ch,   pigmented  vascular   choroid  ;     r,   retina  ;    s,   fibrous   sclera  ;     t,   tapetura 

(  X   150)  (Norman  Ashton). 

plexus  terminating  in  beaded  formations  in  all  layers  of  the  eiDithelium.  Although 
there  appear  to  be  histological  differences  between  the  fibres,  the  evidence 
suggests  that  these  nerves  are  all  of  a  sensory  nature  (Fig.  576). 

A  most  interesting  finding  has  been  reported  by  Wolter  (1957) — the  presence 
of  nerve  fibres  in  the  endothelium  of  the  cornea  in  the  rabbit  (Fig.  577);  their 
function  is  unknown,  nor  have  they  been  observed  in  other  Vertebrates. 

An  interesting  peculiarity  is  the  keratinization  of  the  corneal  epitheliufn  seen 
in  two  tyiDes  of  Placentals.  In  some  aquatic  forms  (seals,  dolphins  and  particu- 
larly in  whales)  the  epithelium  is  thick  and  keratinized  as  a  protection  against 
sea-wateri  ;  while  in  the  ant-eating  Placentals  (Xenarthra,  as  the  armadillo  ; 
Tubulidentata  such  as  the  aard-vark)  a  similar  keratinization  occurs,  correspond- 
ing to  that  seen  in  the  ant-eating  Monotremes  (the  echidna),  presumably  a 
protection  against  the  formic  acid  emitted  in  defence  by  the  termites.  The 
armadillo,  Dasypus,  is  peculiar  in  that  the  cornea  is  vascvilarized  to  its  apex, 
probabi     a  necessary  source  of  nutriment  since  the  heavily  cornified  epithelium 

1  Co;     nire  the  thick  corneal  epithelium  of  the  platypus,  Ornithorhynchiis  (p.  433). 


IVIAMVIALS  457 

is  impervious  to  tears  and  presumably  camiot  mediate  an  adequate  respiratory 
exchange. 

The  Choroid.  The  layers  of  the  choroid  in  the  placental  eye 
correspond  with  those  of  man  (Fig.  578), i  the  choriocapillaris  being 
usually  thin,  exceptionally  so  in  the  Sciuridse  (squirrels)  and  Gliridae 
(dormice)  ;  exceptions  to  this  are  aquatic  types  (Pinnipedes,  Cetaceans) 
Avherein  the  choroid  is  unusually  thick.  One  interesting  and  variable 
feature,  however,  is  the  tapetum  lucidum,^  an  adaptation  acquired 
by  certain  nocturnal  animals  to  improve  vision  in  dim  illumination. 
Optically  the  tapetum  acts  as  a  mirror  which,  lying  behind  the  rods 
and  cones,  reflects  the  incident  light  so  that  it  traverses  the  visual 
elements  twice,   thus   increasing   differences  in   apparent   brightness. 

The  tapetum  of  Placentals  was  first  adequately  described  by  Briicke 
(1845)  and  thereafter  the  subject  has  received  much  study  ;  its 
histological  characteristics  were  fully  elucidated  by  Sattler  (1876) 
while  its  ophthalmoscopic  variations  were  beautifully  illustrated  by 
Johnson  ( 1901 )  (Plates  XIV  and  XV).  It  lies  in  the  upper  posterior  part 
of  the  fundus  with  a  preference  for  the  temporal  side  which  is  used  for 
forward  vision.  Ophthalmoscopically  it  appears  as  a  bright  area  in 
the  fundus,  usually  of  triangular  shape  with  its  base  horizontal  just 
above  the  optic  disc,  sometimes  lying  entirely  above  this  structure 
(horse),  sometimes  including  it  (cat)  ;  it  varies,  however,  considerably 
in  extent,  being  unusually  large  in  the  Cetaceans  (dolphins  and 
whales),  while  in  the  PinniiDcdes  (seals)  it  occupies  the  entire  posterior 
area  of  the  fundus  up  to  the  equator  and  beyond  on  the  temporal  side. 
In  the  tapetal  area  pigment  is  lacking  in  the  retinal  epithelium  to  allow 
the  transmission  of  light,  and,  lying  between  the  choroidal  layer  of 
vessels  and  the  choriocapillaris,  it  is  traversed  by  small  vessels  to 
supply  the  latter,  visible  ophthalmoscopically  as  stellate  dark  dots  on 
the  bright  background — the  "  stars  "  of  Winslow.  The  tapetum  does 
not  appear  ophthalmoscopically  in  the  puppy  until  some  weeks  after 
birth  (Usher.  1924). 

Histologically  two  types  of  tapetum  are  found,  both  completely 
different  in  origin  and  structure — the  tapetum  fibrosum  and  the 
tapetum  cellulosum  (Figs.  579  and  580). 

The  TAPETUM  FIBROSUM  develops  from  the  thin  layer  of  elastic 
fibres  found  normally  in  the  inner  layer  of  small  vessels  of  the  choroid 
(Sattler,  1876).  It  is  composed  of  dense  fibrous  tissue  the  fibres  of 
which  are  closely  woven  together  so  that  the  entire  structure  glistens 
like  a  piece  of  fresh  tendon.  Among  Placentals  such  a  tapetum  is 
typically  foiuid  in  the  Ungulates,  among  which  it  is  almost  universal 

^  The  unique  structure  of  the  choroid  of  the  larger  bats  will  be  noted  subsequently, 
p.  459. 

^  Tapetum  lucidum,  bright  carpet. 


458 


THE   EYE   IN   EVOLUTION 


Fig.  579. — The  Tapetum  Fibrosum  of  the  Horse. 

Showing  the  dense  closely-woven  layex'  of  fibrous  tissue  ;    ch,  choroid 
r,  retina  ;    s,  sclera  ;    <,  tapetum  (  X   126)  (Norman  Ashton). 


Peccary 


^  n.       V*  •«  ^  \ 


Fig.   580. — The  Tai'I'Ti.m   (i: 


^UM  OF  THE  Kitten. 


Note  the  beautifully  an-anged  tiers  of  endothelial  cells  traversed  by  small 
vessels  running  from  the  choroid  to  supply  the  choriocapillaris.  c,  chorio- 
capillaris  ;     cJt,   choroid  ;     r,   retina  ;     t,   tapetum   (  ;■;  375)    (Norman   Ashton). 

(including  the  elephants)  with  the  exception  of  the  Suoidea  (pig, 
peccary,  liippopotamiis)  and  the  Tylopoda  (camels,  llama)  ;  it  also 
occurs  in  the  Cetaceans  (whales  and  doljDhins),  in  two  Rodents,  the 
spotted  cavy,  Cuniculus,  and  the  flying  squirrel,  Pferomys  magnificus, 
niid  in  the  only  nocturnal  Antln-opoid  (the  night  monkey,  Nycfipithecus, 
iji  which  it  is  extremely  brilliant). 


THAIVOIALS 


459 


The  TAPETUM  CELLULOSTJM,  on  the  other  hand,  develops  from  the 
ahnost  continuous  layer  of  endothelial  cells  which  separates  the  elastic 
layer  from  the  choriocapillaris  (Sattler,  1876).  It  is  formed  of  several 
closely  set  layers  ^  of  thin,  flat  endothelial  cells  arranged  in  tiers 
with  mason-like  regularity  resembling  plant  tissue  rather  than  animal, 
each  cell  being  jDacked  with  rod-like,  doubly  refracting  crystals  of  an 
unkno\Mi  chemical  composition  (?  lipoid)  (the  iridocytes  of  Bruni. 
1922)  (Miirr.  1925-27).  Such  a  tapetum  occurs  in  all  Carnivores 
(except  two  Viverrines.  Cynictis  and  Suricata)  including  the  Pinnipedes. 
and  also  in  Prosimians — the  lemuroids,  Loris.  Nycficebus,  Galago  and 
Lemur  catta. 


Suricate 


Fig.    581.- 


-The    Papillated    Choroid    of   the   Fruit-bat 
Pteropvs  Polwcephalvs  (O'Day). 


(Flyixg    Fox)  , 


It  is  interesting  that  the  pigment  epithelium  of  the  retina  in  IMammals  is 
rarely  densely  pigmented  nor  is  the  j^igment  migratory.  It  may  contain  reflecting 
material  ;  this  in  some  fruit -bats  (Pteropus)  serves  as  a  retinal  tapetum  in 
the  upper  jDart  of  the  fundus,  and  in  the  dog  is  said  to  augment  the  effect  of  the 
choroidal  tapetum. 

VASCULAR  CHOROIDAL  PAPILLAE  are  a  unicjue  phenomenon  in  the  animal 
world  found  among  the  ]\Iegachiroptera — fruit -bats  or  fl.ying  foxes  (Pteropus, 
Epo?nophorus)Ko\mev.  1910-24:  Fritsch.  1911;  Gerard  and  Rochon-Duvigneaud, 
1930)  (Fig.  581).  These  structures  which  stud  the  fundus  from  the  ora  to  the 
optic  disc,  form  conical  mesodermal  papilla?  each  with  a  vascular  core,  and  on 
this  irregular  surface  the  visual  cells  of  the  retina  are  arranged  like  trees  on  a 
range  of  hills.     Although  the  retina  is  entirely  avascular  all  its  layers  are  thus 

^  4  in  the  wolverine  ;  8-10  in  the  lion  ;  10  in  the  dog  ;  up  to  35  and  of  a  very 
large  size  in  the  seals. 


Flving  fox 


460  THE   EYE   IN   EVOLUTION 

intimately  supplied  with  choroidal  capillaries  ;  to  a  certain  extent,  also,  the 
irregular  arrangement  of  the  visual  cells  in  the  hills  and  craters  may  act  as  an 
accommodative  device.^ 

It  is  interesting  that  Rohen  (1954)  found  in  the  dog  thick  longitudinal 
mviscular  layers  in  the  walls  of  the  posterior  ciliary  arteries  and  in  the  arteries 
of  the  posterior  part  of  the  choroid  which  he  interpreted  as  a  vascular  shunt - 
apparatus  regulating  the  flow  of  blood  into  the  choroid.  Such  a  mechanism  he 
failed  to  find  in  the  cat,  rabbit,  rat  or  guinea-pig,  or  in  man. 

The  Ciliary  Region.  The  size  and  topograph}^  of  the  ciHary  region 
in  Placentals  vary  considerably,  the  dominating  factor  being  the  pre- 
sence or  absence  of  an  accommodative  mechanism.  Derived  from  noc- 
turnal ancestors  few  Placentals,  particularly  of  the  lower  species,  have 
any  marked  degree  of  accommodative  activity  ;   this,  indeed,  is  found 


Fig.  582. — The  Ciliary  Body  of  Primates. 

The  inner  aspect  of  the  anterior  part  of  the  eye  showing  the  ora  serrata, 
the  pars  plana,  ciliary  processes  and  posterior  surface  of  the  iris. 

only  in  the  squirrels  (Sciuridae),  the  large  Carnivores  and  the  Primates. 
On  this  essentially  depend  the  size  of  the  ciliary  body,  its  muscular 
development,  the  prominence  of  the  ciliary  processes,  a.nd  the  con- 
figuration of  the  angle  of  the  anterior  chamber.  In  most  small-eyed 
primitive  tyj^es  with  comparatively  large  lenses  (Insectivores,  Rodents, 
etc.)  the  ciliary  body  is  small  and  narrow  with  miniature  processes  ; 
in  the  slu'ews  it  is  a  simple  roll  without  processes,  as  in  snakes.^  In 
large-eyed  Placentals,  it  assumes  the  prominent  triangular  shape  with 
well-developed  processes  such  as  are  seen  in  man.  It  is  noteworthy, 
however,  that  from  the  aspect  of  joure  anatomy,  in  many  species  a 
considerable  degree  of  asymmetry  exists  ;  thus  in  animals  with  an 
ovoid  cornea  (and  pupil)  the  circular  ciliary  body  encroaches  far  into 
the  iri.<  nasally  and  temporally,  rendering  the  horizontal  segment  of 
1  p.  643.  -  p.  386. 


MAMMALS 


461 


the  pupil  relatively  immobile,  wliile  in  many  species  (Ungulates  and 
Carnivores)  tlie  tendency  towards  nasal  asymmetry  of  the  globe  in  the 
interests  of  binocular  vision  results  in  a  curtailment  of  the  ciliary  region 
and  the  practical  disappearance  of  the  orbicular  zone  on  the  nasal  side 
(Fig.  582). 

The  main  determinant  in  the  configuration  of  tliis  region  is  the 
degree  of  development  of  the  ciliary  muscle^  (FigS-  583-90).  Anteriorly 
the  ciliary  body  splits  into  two  leaves  ;  one,  the  outer  or  scleral  part, 
essentially  muscular  in  structure,  hugs  the  sclera  as  it  runs  to  the  corneo- 
scleral junction  ;    the  other,  sometimes  fibrous,  sometimes  muscular, 


Figs.  583  to  586. — The  Ciliary  Region  in  Mammals. 


Fig.  583.— Rabbit. 


Fig.  5S4.— Pi 


Fig.  585. — Dog. 


Fig.  586. — Ape. 


S,  the  ciliary  cleft  (or  sinus)  ;    Z,  zonular  ligament.     The  ciliary  muscle 
where  present  is  indicated  bj'  linear  shading. 


forming  the  base-plate  of  the  ciliary  body,  runs  inwards  towards  the  root 
of  the  iris  (Lauber,  1901)  ;  between  these  two  leaves  lies  a  triangular 
cleft  of  varying  depth,  the  ciliary  cleft,-  an  extension  of  the  anterior 
chamber  which  runs  backwards  deejDly  into  the  ciliary  region.  In  the 
small-eyed  and  more  primitive  Placentals  (Rodents,  etc.)  the  ciliary 
muscle  is  either  lacking  or  very  i-udimentary  and  probably  functionless  ; 
when  present  it  consists  of  a  few  slender  fascicules  lying  in  much 
connective  tissue  in  the  outer  leaf  of  the  ciliary  body  (Lauber,  1901  ; 
Colhns,  1921  ;  Davis,  1929)  (Figs.  583.  587).  In  these  animals  the 
ciliary  cleft  is  small.  In  Ungulates  the  muscle  is  also  confined  to 
meridional  fibres  running  close  to  the  sclera,  prolonged  to  find  attach- 
ment to  the  inner  layers  of  the  cornea  by  the  corneo-scleral  trabeculae 
(the  cribriform  ligament  of  Henderson,  1921)  ;    the  inner  leaf  of  the 

1  For  the  innervation,  see  Pines  and  Pinsky  (1932),  Boeke  (1933),  Warwick  (1952). 

2  This  formation  is  often  known  as  the  ciliary  sinus  ;    I  am  using  the  term  ciliary 
cleft  to  distinguish  it  from  the  ciliary  venous  sinus. 


462 


THE   EYE   IN   EVOLUTION 


ciliary  body  is  merely  a  simple  fibrous  base-plate  of  connective  tissue 
(Zimmermann,  1932  ;  Bonfanti,  1949)  (Figs.  584,  588).  In  Carnivores 
the  muscle  is  more  fully  developed  ;  both  leaves  of  the  ciliary  body 
are  provided  with  meridional  muscular  fibres,  while  the  inner  is  pro- 
vided with  radial  fibres  (Figs.  585,  589).    In  both  of  these  two  classes 


Figs.    587    and    5i 


-The   Ciliary   Body    of   Rodents    and    Ungulates 
(J.  Rohen). 


^■-''*l,-fc;Vii5' 


!<;.  587.— Rabbit  (X  92). 


Fig.  588.— Pig  [  ■    lilj. 


the  cleft  is  wide  and  deep  ;  but  in  Primates  the  muscle  has  developed 
to  such  an  extent  that  its  meridional  and  oblique  fibres  occupy  the 
entire  ciliary  body  ;  moreover,  its  massive  anterior  attachment  to  the 
scleral  spur  (and  through  it  by  the  scleral  trabeculse  to  the  deeper 
layers  of  the  cornea)  has  almost  entirely  obliterated  the  cleft  leaving 
only  ;i  remnant  of  it  at  the  angle  of  the  anterior  chamber  (Figs. 
586,  5.    : 


MAMMALS 


463 


In  the  lower  Placentals  tlie  anterior  gap  between  the  two  leaves 
of  the  ciliary  body  forming  the  ciliary  cleft  deprives  the  root  of  the 
iris  of  its  support  and  consequently,  to  serve  as  anchorage,  a  series  of 
strands  runs  from  the  iris  and  the  base-jDlate  of  the  ciliary  body  towards 
the  limbal  portion  of  the  cornea  where  they  j^icrce  Descemet's  membrane 

Figs.   589   and    590. — Thk   Ciliary   Body   of   Carnivores   and   Primates 

(.J.  Rohen). 


Fig.  589.— Dog  (  x  20). 


fSB 


i-IL,. 


-Ajie  (   •.   ati;. 


and  blend  with  the  deeper  layers  of  the  substantia  propria  (Fig.  596). 
These  strands  of  connective  tissue  covered  with  endothelium,  bridaing; 
over  the  cleft,  constitute  the  pectinate  ligament,  which  gives  supj^ort 
to  the  root  of  the  iris,  the  base-jDlate  of  the  ciliary  body  and  therefore 
ultimately  to  the  lens.  In  the  lower  Placentals  wherein  the  cleft  is 
rudimentary  and  accommodative  stram  is  lacking  and  m  Primates 
wherein  the  cleft  is  replaced  by  solid  tissue,  the  jjectinate  ligament  is 


464  THE   EYE   IN   EVOLUTION 

rudimentary  or  vestigial.  In  Rodents  this  ligament  is  made  up  of 
innumerable  short  fibres  at  the  opening  of  the  cleft,  which  itself  is 
empty  (Figs.  583,  591,  596)  ;  in  Ungulates  (such  as  the  horse,  ox,  pig 
and  sheep)  the  strands  over  the  opening  of  the  cleft  are  stout  and  well 
developed,  like  the  girders  of  a  bridge  spanning  the  ciliary  cleft,  while 
the  body  of  the  cleft  is  filled  by  a  close  irregular  meshwork  of  fine  fibres 
appearing  as  spongy  tissue  (Figs.  584,  592)  ;  in  Garni vora  (such  as 
the  dog  and  cat)  the  more  anterior  strands  supporting  the  root  of  the 
iris  are  thin  and  delicate  like  the  cables  of  a  suspension  bridge,  while 
the  depth  of  the  cleft  is  filled  with  fine  threads  running  a  fan-like 
course  with  no  resemblance  to  spongy  tissue  (Figs.  585,  593,  597)  ; 

Figs.  591  to  594. — The  Angle  of  the  Anterior  Chamber  of  Placentals. 

As  seen  gonioscopically,  showing  the  configuration  of  the  pectinate  ligament 
(from  drawings  from  Troncoso). 


■^4nmy^^»ti:^^,^ 


Fig.  591.— Rabbit.  Fn;.  .V.)l'.      I'm.  Fig.  593 


in  the  Pinnipedes  (seals)  the  anterior  strands  are  particularly  stout. 
In  the  Primates  (man)  the  pectinate  ligament  is  discernible  until  the 
6th  month  of  foetal  life  (Collins,  1899  ;  Seefelder,  1910),  but  owing 
to  its  subsequent  atrophy  it  can  hardly  be  said  to  exist  in  the  adult, 
the  support  of  the  lens  being  more  adequately  undertaken  by  the  dense 
muscular  and  trabecular  tissue  of  the  ciliary  body  (Figs.  586,  594). 

This  interesting  and  important  region  has  received  a  considerable  amount 
of  attention.  The  first  to  give  an  adequate  description  with  illustrations  was 
Murray  (1780)  at  Uppsala  who  called  the  cleft  at  the  angle  of  the  anterior 
chamber  of  the  ox  the  ciliary  canal.  In  the  following  year,  Felix  Fontana  (1781), 
the  anatomist  of  Pisa  and  Florence,  gave  a  description  of  the  same  region  and 
since  then  the  extensions  of  the  anterior  chamber  into  the  ciliary  region  of 
Mammals  have  variously  been  called  Fontana's  spaces  or  canals.  Shortly  there- 
after Kieser  (1804)  of  Gottingen  pointed  out  that  such  structures  did  not  exist 
in  man.  Subsequently  Hueck  (1839)  of  Dorj^at,  studying  the  cow's  eye,  described 
the  teeth-like  structures  stretching  over  Fontana's  spaces  from  the  root  of  the 
iris  to  the  sclero -corneal  junction  as  the  pectinate  ligament  (pecten,  a  comb),  an 
appropriately  descriptive  term  ;  since  then  it  has  been  called  by  many  names — 
the  suspensory  ligament  of  the  iris,  the  iVis  pillars,  and  so  on  (Fig.  595). 

Over  the  last  centviry  and  a  half  much  study  has  been  given  to  the  ciliary 
region  of  the  mammalian  eye — most  of  it  histological.^  More  recently  a  better 
perspective  has  been  put  on  the  anatomical  arrangements  by  the  gonioscopic 

1  Flamming  (1868),  Iwanoff  and  Rollett  (1869),  Angelucci  (1881),  Dostoiewsky 
(1886),  Virchow  (1886-1910),  Rochon-Duvigneaud  (1892-93),  Collins  (1899),  Asayama 
(1901)  uber  (1901),   Seefelder  and  Wolfram   (1906),  Henderson   (1908-50),   Rohen 

(1953- .. ,      md  de  Toledo  Piza  (1955). 


MAIVOIALS 


465 


Figs.  595  to  597. — The  Angle  of  the  Anterior  Chamber  of  Placentals. 

,c 


Fig.    595. — Diagram   of   the   Angle   of   the   Anterior   Chamber   of   the 

Horse. 

C,    cornea  ;     CB,    ciliary    body  ;     D,    Desceinet's    membrane  ;     /,    iris  ; 
PL,  pectinate  ligament  ;   SF,  spaces  of  Fontana. 


<*q;*(^' 


^llw    ' 


:^- 


!•  h 


iN    '<\'    I'll  !■:    A  N  ri:i:ii  ii;    »   ii  \.\i  ni-:i: 


Note  the  stout  fibre  of  the  pectinate  ligament  bridging  over  the  entrance 
of   the    ciliary    cleft    and    j^iercing    Descemet's   membrane    ( x    60)    (Norman 

Ashton). 


w--^~f*-     V 


r>*^B^P^«^  :  XV;  ill 


-^'*.-i. 


Fig.   597. — Section  of  the  Anterior  Chamber  of  the  Cat. 

Note   the   delicate   strands  of  the   pectinate   ligament    filling   the   ciliarj' 
cleft  {  X  60)  (Norman  Ashton). 
S.O.— VOL  I.  30 


466 


THE   EYE   IN   EVOLUTION 


and  micro -anatomical  methods  api^lied  by  Troncoso  and  Castroviejo  (1936)  and 
Troncoso  (1937).  Troncoso  called  the  cleft  the  cilio-scleral  sinus,  but  since  it 
does  not  sejaarate  the  ciliary  body  and  the  sclera  but  extends  into  the  ciliary 
body  itself,  ciliary  cleft  (or  sinus)  would  seem  a  more  appropriate  name. 

The  ciliary  2^rocesses  vary  considerably  in  their  form,  depending 
on  the  number  and  arrangement  of  the  zonular  fibres,  the  development 


Figs.  598  and  599. — The  Ciliary  Processes  of  Placentals 
(after  Franz,  1911). 


Fig.  598.— Felis  Ubyca. 

C  cornea  ;    I,  iris  ;    P,  pectinate  liga- 
ment ;   S,  sclera. 


Fig.  599. — Eleplias  maximus. 

C,  ciliary  processes  ;    /,  iris  ;    O,  orbi 
cuius  ciliaris  ;  S,  ora  serrata. 


of  which  depends  on  accommodative  activity. ^     Three  general  types 
exist  (Figs.  598  and  599). 

1.  In  the  lower  orders  as  exemplified  in  the  Rodents  (rabbit), 
the  processes  are  thin  and  blade-like  with  deep  valleys  between  ;  many 
of  them  extend  far  into  the  iris  as  is  seen  in  the  human  embryo, 
touching  the  lens  anterior  to  the  equator,  so  that  the  corona  ciliaris  is 
in  large  part  an  iridic  structure.  The  posterior  chamber  is  thus  exceed- 
ingly small. 

2.  In  the  Ungulates  as  exemplified  in  sheep,  jjigs  and  cattle,  the 
processes  are  thick  and  club-like  with  shallow  valleys  and  are  confined 

^  I'lr  the  comparative  anatomy  see  Wiirdinger  (1886),  Bayer  (1892),  Lauber 
(1901  ■  ;  .  Virchow  (1910),  Franz  (1912),  Hess  (1913),  Beauvieux  and  Dupas  (1926). 
Troncc.       !*)42),  Wislocki  (1952),  Rohen  (1953). 


MAMMALS 


467 


to  the  ciliary  region  ;  their  anterior  ends  form  a  soHcl  wall  not  encroach- 
ing u23on  the  iris  so  that  the  jjosterior  chamber  is  deep.  The  apices  of 
the  processes,  however,  touch  the  lens. 

3.  In  Carnivora,  as  exemi^lifiecl  in  the  cat.  dog,  and  lion,  the 
ciliary  processes  are  of  two  tyjies — Iviiife-like,  tall,  major  processes 
between  every  jDair  of  wliicli  lies  a  small  minor  process  ;  none  of  them 
reaches  the  lens.  In  the  Primates  the  general  arrangement  is  similar 
but  the  main  ciliary  processes  are  stouter  and  more  rounded  and 
several  stumpy  minor  folds  (plicte  ciliares)  lie  between  the  main 
processes. 


Fig.  600. — The  Iris  of  the  Fcetal  Guinea-pig. 

Xote  the  circulus  arteriosus  iridis  major  faintly  outlined  in  the  nasal  and 
temporal  parts  and  the  vessels  of  the  pupillary  membrane  spanning  the 
]3upil  (from  a  slit-lamp  drawing  by  Ida  INIann). 


4.  Finally,     the    ciliary    processes    are    absent    in    the    shrews 
(Soricidse).i 

Curious  nervous  structures  have  been  described  in  the  ciUary  body  of  certain 
Cetaceans  in  the  regiDU  of  the  angle  of  the  anterior  chamber  which  may  perhaps 
be  CILIAKY  RECEPTOR  ORGANS.  In  the  beaked  whale,  Hyperoodon,  Putter  (1912) 
found  elongated  nervous  structures  which  appeared  to  be  associated  with  the 
ciliary  nerves,  and  in  the  hump-back  whale,  Megaptera,  Rochon-Duvigneaud 
(1943)  described  oval  bodies  isolated  or  lying  in  groups,  resembling  pacchionian 
coipuscles  or  the  corpuscles  of  Herbst  in  the  bill  of  the  duck.  Their  function  is 
enigmatic,  but  it  has  been  suggested  that  they  are  sensory  pressure-organs  of 
value  to  the  animal  when  it  dives.  This  may  be  possible  in  view  of  the 
"  corpuscles  "  described  by  Kurus  (1955)  in  the  ciliary  body  of  man  which 
conceivably  may  act  as  receiptors  to  changes  in  the  intra-ocular  pressure. 

1  It  will  be  remembered  they  are  also  absent  in  Fishes  (except  Selachians), 
Sphenodon,  lizards  and  snakes. 


468  THE   EYE   IN   EVOLUTION 

The  Iris.  The  deeper  layers  of  the  iris  conform  to  the  general 
vertebrate  type.  Both  layers  of  the  retinal  epithelium  are  heavily 
pigmented  except  when  a  dilatator  papillae  muscle  is  present  in  which 
case  the  anterior  layer  lacks  its  pigment  except  near  the  pupillary 
border.  The  pupillary  muscles  are  non-striated  ;  a  spliincter  is  always 
present,  massed  particularly  near  the  pupillary  margin,  but  sometimes 
(in  aquatic  Placentals  such  as  the  otter,  the  Pinnipedes  and  the 
Cetaceans,  and  in  the  pig)  extending  peripherally  tlu-oughout  the  entire 
width  of  the  iris  ;  the  dilatator  is  absent  in  the  nocturnal  representa- 
tives of  the  lower  species. 

The  main  (deeper)  mesodermal  layer  of  the  iris  corresponds  with 
that  of  other  Vertebrates,  being  supplied  by  a  circular  artery  (the 
circulus  arteriosus  iridis  major)  derived  from 
the    anastomosis    of    each    of   the    two    long 
-P.R  posterior  ciliary  arteries.    This  arterial  circle  is 

usually  hidden  behind  the  limbus  but  can  some- 
times be  seen  on  the  anterior  surface  of  the  iris, 
as  in  the  guinea-pig  (Fig.  600)  ;    from  it  radial 

Fig.  GUI.— Structure  of      vessels  are  given  off  to  supply  the  sphincteric 
THE    Iris    of    Placen-  ®  .  x  i   ^  x 

TALs.  and   subsphincteric   plexuses,  the  blood  being 

SM,  DM,  superficial  drained  away  by  a  radial  system  of  veins. 
i:;is.'''^P/^?":hfTo  Superficially  to  this,  however,  lies  a  layer 
posterior    retinal    layers     unique  to  Mammals — the  anterior  ynesodermal 

thetoiefHSTrritrof     '«?'"■■     I"  embryonic  life  this  layer  grows  in 
the  optic  vesicle.  from  the  periphery  in  advance  of  the  deeper 

layer  of  mesoderm  and  the  retinal  epithelium, 
carrying  with  it  a  rich  vascular  supply  to  constitute  the  anterior  portion 
of  the  tunica  vasculosa  lentis.  The  central  (pupillary)  portion  of  this 
layer  is  diaphanous  and  almost  acellular  and  as  development  proceeds 
it  gradually  atrophies,  receding  to  a  sinuous  scalloped  line  peripheral 
to  the  pupillary  margin  where  tlie  superficial  radial  vessels  anasto- 
mose to  form  a  very  imperfect  circular  arcade,  the  circulus  arteriosus 
iridis  minor.  The  site  of  the  lesser  circle  which  marks  the  limits  of  the 
superficial  mesodermal  layer  is  fortuitous,  sometimes  being  close  to  the 
pupil,  sometimes  far  away  ;  it  varies  in  different  species,  between 
individuals  of  the  same  species,  and  in  different  parts  of  the  iris  in  the 
same  individual,  but  the  general  plan  of  vascularization  remains  the 
same  (Mann,  1931)  (Fig.  601).  In  most  Placentals  this  layer  is  com- 
pact and  covered  by  a  continuous  layer  of  endothelium  ;  in  some 
Rodents  (rabbit)  and  the  higher  Primates  {Macacus,  the  gorilla  and 
man)  it  tends  to  atroj^hy  so  that  an  incomplete  layer  is  formed  with 
the  development  of  open  crypts  (Wolfrum,  1926  ;  Vrabec,  1952).  As 
we  baA  e  seen,  from  its  periphery  are  given  off  strands  of  endothelial- 
lined      nnective  tissue  which  traverse  the  angle  of  the  anterior  chamber 


MAIIMALS  469 

to  find  anchorage  in  the  hmbal  region  of  the  sclera  (the  pectinate 
ligament)  ;  these  are  of  varying  develoj^ment  in  different  sjiecies  and 
are  only  vestigial  in  man. 

The  pigmentation  of  the  iris  is  much  more  drab  and  uniform  than  in  manj' 
other  classes  of  Vertebrates.  Except  in  albinotic  individuals  it  is  derived  merely 
from  melanin-containing  chromatophores,  and  depending  on  their  number  and 
the  density  of  pigment  within  them,  the  iris  is  a  varying  shade  of  bro\^^^.  tending 
to  yellow  when  the  jDigment  is  scarce  and  blue  (as  often  in  man)  for  reasons  of 
optical  transmission  when  the  stromal  pigment  is  sufficiently  sjDarse.  As  a  rule 
the  pigment  is  plentiful  and  the  eye  dark  brown  or  almost  black,  and  since  the 
chromatophores  He  superficial  to  and  between  the  vessels,  the  latter  are  visually 
completely  obscured  ;    only  in  albino  types  can  the  vascular  pattern  be  made 

Figs.   602  to  60fi. — Pupillary  Appendages  in  Placentals. 


Fig.  602. — The  horse.  Fig.  603.— The  gazelle. 


'\,""-    ««■ 

Fig.  604.— The  goat.  Fig.  60.").- The  camel.  Fig.  606.— The  hyrax. 

out.  Occasionally  and  \ery  rarely  this  simple  j^igmentary  scheme  is  complicated 
by  the  presence  of  other  pigments  and  iridocytes,  a  circumstance  which  gives 
rise  to  the  green  lustre  of  the  eyes  of  some  Carnivores,  .such  as  the  cat.  and  some 
Prosimians.  In  animals  provided  Mith  a  choroidal  tapetum,  representative 
elements  of  this  structure  are  found  in  the  iris — fibrous  elements  in  Herbivora, 
cellular  in  Carnivora  (W'olfrum.  1926). 

The  jiuiDillary  margin  is  occasionally  marked  by  special  appendages 
the  purpose  of  which  is  presumably  to  diminish  glare.  These  may  be 
of  two  types. ^  The  first,  the  corpora  nigra  (grape-seed  bodies  or 
FLOCCULi  of  Kieser,  1803),  are  immobile  and  are  formed  by  a  prolifera- 
tion of  the  pigmented  epithelium  as  highly  vascularized  cystic  pro- 
trusions of  the  marginal  sinus. ^  They  occur  among  the  higher  Ungulates 
(Figs.  602  to  605).  In  the  Ec[uidfe  (horse,  etc.)  they  are  relatively 
simple,  being  confined  to  the  upper  edge  of  the  pupil  (Fig.  557)  ;  in 

^  For  literature,  see  Bayer  and  Frohner  (1900),  Johnson  (1901),  Lange  (1901), 
Stein  (1902),  Zietzschmann  (1905),  Rirhter  (1909-11),  Schneider  (1930^,  Rohen 
(1951-52). 

^  The  embryonic  persistence  of  the  primary  optic  vesicle  between  the  two  layers 
of  epithelium  at  the  pupillary  margin. 


470  THE   EYE   IN   EVOLUTION 

some  Ruminants  they  are  more  fully  developed,  as  in  the  gazelle 
where  they  are  found  both  on  the  upper  and  lower  margins  of  the 
pupil,  or  in  the  sheep  where  there  are  as  many  as  20,  or  in  the  wild 
goat,  Capra  dorcas,  where  the  mesodermal  portion  of  the  iris,  beautifully 
striped,  participates  in  the  projection  ;  in  the  Tylopoda  (camel,  llama) 
they  reach  their  fullest  development,  forming  a  series  of  ridges  and 
hollows  on  the  upper  and  lower  margins  of  the  pupil  which  interlock 
on  miosis  (Zannini,  1932). 

The  second  type  of  structure,  called  the  umbraculum  by  Lindsay 
Johnson  (1901),  is  somewhat  reminiscent  of  the  operculum  of  some 
rays  1  (Fig.  606).  In  the  coneys  (hyraxes)  it  is  a  flap-like  fibro-cellular 
structure,  protruding  from  the  mesodermal  portion  of  the  iris  2  mm. 
from  its  free  edge.  It  is  provided  with  a  fan-like  arrangement  of 
(muscular  ?)  fibres  and  is  remarkably  contractile  ;  apparently  without 
regard  to  the  amount  of  light  and  perhaps  under  voluntary  control,  it 
can  be  retracted  out  of  the  pupillary  aperture,  extended  so  as  to  touch 
the  lower  margin  of  the  pupil  and  almost  totally  occlude  it,  or  protruded, 
flap-like,  to  touch  the  posterior  surface  of  the  cornea.  An  expansile 
operculum  is  also  seen  in  some  Cetaceans. 

The  2^M^^l  ii^  most  Placentals  is  round,  both  in  dilatation  and 
contraction.  A  slit-shajje  on  contraction  is  achieved,  however,  in 
some  Carnivora  either  as  a  protective  or  an  ojjtical  device.  The  slit- 
or  oval-shape  is  maintained  by  the  arrangement  of  the  fibres  of  the 
sphincter,  two  bundles  of  which  cross  above  and  below  the  pupil  and 
are  continued  out  to  the  periphery  of  the  iris,  a  scissor-like  action  which 
compresses  the  pupillary  aperture  laterally  (Michel,  1881  ;  Eversbusch, 
1885  ;  Raselli,  1923  ;  Theiler,  1950  ;  Rickenbacker,  1953)  (Figs.  608- 
10).  In  the  smaller  Felidse  and  Viverridae  and  in  some  Hysenidse  and 
Rodentia,  as  is  well  seen  in  the  cat  or  the  chinchilla,  the  slit-like 
contracted  pupil  affords  protection  to  an  essentially  nocturnal  animal 
against  excessive  light  A\hen  basking  in  the  sun.  In  some  of  the 
hyaenas  {Hycena  striata,  H.  hrunnea)  the  contracted  slit  has  a  constriction 
in  the  middle  giving  the  impression  of  two  pupils  (K.  M.  Schneider, 
1930).  Among  the  Pinnipedes,  in  the  seals  and  sea-lions  the  pupil  is 
dilated  and  circular  under  water,  but  contracts  to  a  vertical  slit  in  the 
air  (except  in  the  bearded  seal,  Phoca  barbata,  wherein  the  slit  is 
horizontal)  ;  this  is  almost  certainly  an  adaptation  for  aerial  vision 
which  will  be  discussed  at  a  later  stage  (Johnson,  1901).^  The  walrus, 
on  the  other  hand,  which  feeds  on  land,  has  a  broad,  horizontally  oval 
pupil  (Franz,  1934). 

V/hile  round  i^uj^ils  are  the  rule  among  Placentals,  oval  pupils  are 
found  in  a  considerable  number  of  species — usually  horizontally  oval 
amori:        rbivora  and  vertically  oval  among  Carnivora,  a  circumstance 

1  p.  287.  2  p.  641. 


mam:\la.ls 


471 


Figs.   607  to  610. — The  Pupils  of  Placenta ls. 


Fig.  607.— The  Eye  of  a  Poxy. 

Showing  the  tj'pically  horizontally  oval  pupil  of  an  Ungulate 
(photograph  by  Michael  Soley). 


Fig.  60S. — Primate. 


Fig.  609.— Cat. 


Fig.  610.— Horse. 


The  round  pupil  is  characteristic  of  diurnal  and  strictly  nocturnal  tyjDes. 
The  verticallj-  oval  pupil  is  characteristic  of  nocturnal  types  which  bask  in  the 
sun.  The  horizontally  oval  pupil  is  characteristic  of  Ungulates  and  several 
other  types  (see  text). 

In  the  round  pupil  the  sphincter  muscle  (solid  lines)  and  the  dilatator 
muscle  (broken  lines)  are  symmetrically  arranged.  In  the  vertically  oval  pupil 
part  of  the  sphincter  muscle  surrounds  the  pupil  but  criss-crossing  fibres 
extend  above  and  below  to  the  periphery  of  the  iris.  In  the  horizontally 
oval  pupil  most  of  the  sphincter  fibres  encircle  the  pupillary  aperture  but  other 
fibres  are  orientated  radially  on  each  side  to  be  anchored  in  connective  tissue 
(shown  stippled  in  Fig.  610)  in  the  nasal  and  temporal  parts  of  the  iris  ; 
these  areas  are  devoid  of  dilatator  fibres  (from  drawings  by  Eversbusch  and 
Gordon  Walls). 


depending  not  on  diet  l)ut  on  habit,  an  adaptation  in  the  fir.st  case  to 
suit  diurnal,  shade-loving  animals,  in  the  second,  crepuscular  or 
nocturnal  animals  requiring  protection  from  glare  during  daylight 
(Figs.  607-10). 

The  following  have  vertically  oval  pupils  : 

Many  Carnivora — the  larger  Feliclse  (lion,  tiger,  leopard,  jaguar)  ;  Canidfe 
(dog,  fox,  etc.)  ;  most  hyaenas,  and  Viverridfe  ;  ainong  the  Procyonidfe,  the 
panda  ;  some  Ursidfe  (the  arctic  white  bear,  Thalassarctos  maritimus,  and 
Melursiis  (Fig.  609)  ). 

Few-  Rodents — the  varying  hare  {Lepus  timidus),  the  nutria-bearing  coypu 


472 


THE   EYE   IN   EVOLUTION 


Vizcacha 


Mongoose 


Weasel 


Coati 


Aard-vark 


{Myocastor  coypiis),  the  S.  American  vizcacha  {Lagostomus  trichodactylus),  the 
Patagonian  cavy  {Dolichotis  patagonica),  the  chinchilla,  and  the  American  capy- 
bara  {Hydrochccrus  capybara). 

Few  Prosimians — Nycticebus  and  the  galago  of  Zanzibar  {Galago  zanziharicus) . 

The  following  Placentals  have  horizontally  oval  pupils  : 

Among  the  Ungvilates,  all  Artiodactyls  (Suoidea,  Tylopoda  and  Rviminants), 
all  Perissodactyls  (Equidse,  Rhinocerotidse)  except  the  Tapiridse  (Figs.  607, 
610). 

All  Cetaceans  (whales)  and  Sirenians  (sea-cows)  except  Manatus  inunguis. 

Among  the  Carnivora — a  few  Viverridae  (the  mongoose,  Herpestes  ;  Cynictis 
and  Suricata)  ;  a  number  of  Mustelidse  (the  ferret,  PiUorius  furo,  the  weasel, 
Mustela  nivalis,  the  ermine,  M.  erminea,  the  mink,  Lutreola,  the  wolverine, 
Gulo)  ;  among  the  Procyonidee,  the  coati  (Nasua).  Among  the  Pinnipedes,  the 
bearded  seal  {Phoca  barbata). 

Among  the  Rodents,  the  common  squirrel  {Sciiirus  vxdgaris),  the  African 
sciuirrel  [Xerus),  the  American  chipmunk  (Tamias),  the  prairie-dog  (Cynomys), 
the  marmot  {Marmot a). 

Among  the  Tubulidentata,  the  aard-vark  [Orycteropus). 

The  direct  pupillary  reaction  to  light  is  generally  present  (Hertel,  1907  ; 
K.  M.  Schneider,  1930  ;  Kahmann,  1930-32  ;  Rochon-Duvigneaud,  1933  ; 
Studnitz,  1934  ;  Nordmann,  1947)  ;  a  consensvial  reaction  has  been  noted 
in  many  species  (cat,  dog,  ox,  horse,  sheep,  etc.)  (Steinach,  1890-92  ;  Schleich, 
1922).  Dilatation  to  stimuli  such  as  pain  or  attention  occurs  in  such  species  as 
the  cat,  the  dog  and  monkeys  (Macacus)  (Levinsohn,  1902  ;  Amsler,  1924  ;  ten 
Cate,  1934),  reactions  particularly  evident  in  the  hyjena  (Schneider,  1930).  The 
pupils  of  Ungulates  are  remarkably  insensitive  to  all  stimuli  in  comparison 
with  those  of  other  Mammals,  but  the  pupils  of  all  Placentals  react  to  atropine 
(Johnson,  1901). 

The  chamiels  draiimig  the  aqueous  humour  from  the  angle  of  the 
anterior  chamber  are  relativ^ely  simple  in  most  Placentals. ^  Associated 
with  the  outer  wall  of  the  ciliary  cleft  there  is  a  rich  network  of  veins 
and  venous  capillaries  which  combine  to  form  an  intrascleral  plexus, 
the  main  part  of  which  lies  about  the  level  of  the  middle  of  the  cleft  ; 
this  drains  outwards  by  some  5-6  wide  scleral  veins  to  the  sub- 
conjunctival veins  (Fig.  611).  Originally  described  by  Hovius  (1716) 
in  the  dog,  and  often  called  the  circle  of  hovius,  this  plexus  varies 
considerably  in  richness  and  complexity  in  different  animals,  being 
relatively  sparse  in  Ungulates  and  elaborate  in  Carnivores.  That  these 
vessels  are  the  essential  exit -channels  of  the  aqueous  humour  has  been 
shown  by  the  injection  experiments  of  Nuel  and  Benoit  (1900),  Seidel 
(1923-24)  and  Kiss(1942-49),  and  when  they  reach  the  subconjunctival 
plane  some  of  them  may  contain  pure  aqueous  undiluted  with  blood 
(in  the  rabbit,  Schmerl,  1947  ;  Weekers  and  Prijot,  1950  ;  Greaves 
and  Perkins,  1951  ;  Wegner  and  Intlekofer,  1952  ;  Binder  and  Binder, 
IS)^/'^.    According  to  Rohen  (1956)  in  the  dog  this  plexus  anastomoses 


(193i 


or  literature,   see   Lauber   (1901) 
rroncoso  (1937-42). 


Maggiore   (1917),  Troncoso  and  Castroviejo 


MAMMALS 


473 


with,  branches  of  the  anterior  cihary  arteries  witli  shunt-hke  vessels 
which  can  be  opened  or  closed  by  large  epithelioid  cells.  In  the 
Primates,  as  we  have  seen,  the  ciliary  cleft  is  obliterated  by  the  great 
development  of  the  ciliary  muscle,  thus  cutting  off  the  possibility  of  tJie 
drainage  of  aqueous  by  this  route  ;  to  maintain  connections  with  the 
anterior  chamber  a  sj^ecial  sinus,  the  caxal  of  schlemm,  is  thus 
developed    as    a    diverticulum    from    the    intrascleral    venous    plexus, 


Figs.   611   and   612. — The  Drain.\ge  Channels  from  the  Angle  of  the 
Anterior  Chamber  in  Placentals. 


A,V.        A.C.V. 


C.B.        C.S.S. 


CB.      V.P 


Fig.  611. — A  lower  Placental  (rabbit) 


Fig.  612. — A  higber  Placental  (Primate). 


ACV,  anterior  ciliary  veins  ;  ..41^,  acjueous  vein  ;  C,  cornea  ;  CB,  ciliary 
body  ;  CSS,  ciliary  cleft  ;  EV,  efferent  ciliary  veins  ;  /,  iris  ;  IP,  intra- 
scleral ciliary  plexus  ;  .S',  sclera  ;  SC,  canal  of  Schlemm  ;  T,  trabeculte 
traversed  by  a  canal  of  Sondermann  ;    IP,  ciliary  venous  plexus. 

In  Fig.  611  the  essential  drainage  is  from  the  anterior  chamber  into  the 
ciliary  cleft,  thence  through  the  intrascleral  plexus  of  veins  into  the  anterior 
ciliary  veins.  In  Fig.  612  tlie  older  channels  are  represented  as  in  Fig.  611 
draining  from  the  ciliary  venous  plexus,  but  superimposed  on  this  is  a  new 
drainage  system  represented  by  Sondermann's  canals,  the  canal  of  Schlemm, 
an  anterior  extension  of  the  intrascleral  venous  plexus,  together  with  the 
intra.scleral  and  aqueous  veins  emptying  directly  into  the  anterior  ciliary  veins. 


placed  anteriorly  at  the  corneo-scleral  junction  at  which  level  the  angle 
of  the  anterior  chamber  is  now  closed  (Fig.  612).  This  structure,  which 
may  branch  to  have  more  than  one  lumen  and  is  lined  by  a  single  layer 
of  endothelium,  runs  circumferentially  around  the  globe  separated  from 
the  anterior  chamber  by  the  corneo-scleral  trabecidse  through  which 
pass  minute  channels,  the  canals  of  Sondermann  (1933),  and  is  con- 
nected to  the  intrascleral  venous  plexus  by  numerous  efferent  channels, 
some  of  which  reach  the  subconjunctival  region  directly  as  aqueous 
veins.  This  system,  added  to  the  intrascleral  venous  plexus  to  com- 
pensate for  the  closure  of  the  ciliary  cleft,  plays  the  major  part  in  the 
drainage  of  the  aqueous  humour  in  the  eyes  of  Primates. 


474 


THE   EYE   IN   EVOLUTION 


The  lens,  suspended  freely  from  the  ciliary  processes,  is  usually 
relatively  small  and  lenticular  in  shape  in  diurnal  species,  the  anterior 
surface  being  usually  the  more  convex  in  Garni vora,  the  posterior  in 
Herbivora  and  Primates  (Figs.  613  to  616)  ;  it  approaches  rotundity 
and  is  larger  in  nocturnal  species,  especially  in  the  small-eyed  lower 
forms,  and  is  round  in  aquatic  species  such  as  the  Cetaceans  and 
Pinnipedes.  Among  Sirenians  (sea-cows  such  as  the  manatee  and 
dugong)  the  lens  is  lenticular  in  shape  but,  to  suit  the  optics  of  an 


Figs.  613  to  616. — The  Lenses  of  Placentals. 


Fig.  613. 


Fig.  614.— Seal. 


Fig.  615.— Dog.      Fig.  616.— Primate. 


aquatic  environment,  approximated  closely  to  the  cornea  so  that  the 

anterior  chamber  is  very  shallow.     In  the  tree-shrew,  Tupaia,  and  in 

most  squirrels  (Sciurida?,  except  the  nocturnal  flying  squirrels),  the 

lens  is  tinted  yellow  (Merker,  1928  ;   Walls,  1931).     With  regard  to  its 

structure,  the  same  general  plan  of  a  series  of  radial  lamellae  is  apparent 

throughout  the  whole  vertebrate  phylum,  with  only  minor  modifications 

(Rabl,    1899)    (Fig.    617).      The    sutural    arrangements    are    usually 

simpler  than  in  man,  being  made  up  of  two  lines  having  a  vertical 

direction  anteriorly  and  a  horizontal  posteriorly  {e.g.,  rabbit).     Tliis 

forms  a  transient  stage  in  the  development  of  the 

lens  of  Primates  but  eventually  in  these  the  lines 

branch  into  a  tri-radiate  form  resembling  the  letter 

Y  standing  in  the  erect  position  anteriorly  and  the 

inverted  position  posteriorly  (Figs.  618  to  620). 

In  all  adult  Mammals,  the  subcapsular  epithelium 

ends  at  the  equator,  but  in  many  of  the  lower 

species  it  extends  farther  back.    The  cajjsule  is 

always  present  and  in  some  animals  it  is   very 

„        .,„     ^        ^         thick,    showina;   definite    striations    into    layers  ; 
Fig.     617.— The    Ra-         ,         .        ,       ,  i  .  ^     ■     •       i        1 

DiA.    t.amell^   of     thus  ni  the  horse  at  the  anterior  pole  it  is  about 

THE   lkns  of  the      Q'S  miu.  tlilck  aud  is  made  up  of  26  layers.    The 

Cham  •.  (after       ^         ,  .      .  •  ,  .   ,  ^  -r 

Rabl),  local  variations  m   thickness   are  not   umiorm  : 


MAIVIMALS 


476 


Figs.  618  to  620. — Sutural  Arrangements  of  the  Lens  in  Placentals. 


Fig.  618.— The  sutural 
arrangements  in  a 
lower  Mammal  (a  rab- 
bit), forming  a  transient 
stage  in  the  develop- 
ment of  the  lens  of 
Primates. 


Fig.  619. — The  general 
sutural  arrangements  in 
Primates. 


Fig.  620.— The  anterior 
surface  of  the  lens  in 
Primates. 


in  general,  among  Sanropsida  the  maximum  tliickness  is  at  the 
equator  ;  in  IMammaha  the  general  scheme  of  the  human  capsule 
is  followed,  but  the  thinning  at  the  anterior  pole  which  seems  to  be 
associated  with  the  formation  of  an  anterior  lenticonus  during  accom- 
modation is  peculiar  to  the  Primates  (Fincham,  1929)  (Figs.  787  to 
790). 

The  differences  in  configuration  in  the  ciliary  body  necessitate  variations 
in  the  arrangement  of  the  zonular  fibres  (Figs.  Q21-3).^  In  Rodents  with  ciliary 
processes  prolonged  onto  the  iris  the  zonular  fibres  arise  from  their  posterior 
halves  only  ;  in  Ungulates  they  arise  from  the  posterior  two-thirds  of  the  processes 
but  hug  them  anteriorly  to  their  apex.  In  both  ca.ses  they  run  along  the  floors 
of  each  valley  and  the  sides  of  the  adjoining  processes  to  proceed  in  discrete  bands 
towards  the  equator  of  the  lens.      In  Carnivora,  however,  with  their  greater 


Figs.  621  to  623. — The  Zonular  Fibres  of  Placentals. 


Fig. 


621. — An    Ungulate  Fig.     622. — A     Carnivore  Fig.  623. — A  Primate 

(pig).  (cat).  (monkey). 

The  zoiiular  fibres  are  outlined  in  continuous  lines,  the  major  ciliary 
processes  in  dotted  lines,  c,  cornea  ;  /,  iris  ;  /,  lens  ;  s,  sclera,  p  indicates 
the  smaller  perpendicular  bundles  of  fibres  associated  with  the  minor  ciliary 
processes  (from  Kallmann  and  Walls). 

1  For  the  comparative  anatomy  of  the  zonule,  see  particularly  Aeby  (1882), 
Kahmann  (1930),  Teulieres  and  Beauvieux  (1931),  Troncoso  (1942),  Wislocki  (1952), 
Fukamachi  (1953). 


476 


THE   EYE   IN  EVOLUTION 


accommodation,  the  pattern  of  the  zonule  becomes  ntiore  complex  as  it  traverses 
the  space  between  the  ciliary  body  and  the  lens  (Fig.  622).  Bundles  of  fibres 
arise  posteriorly  from  the  orbicular  portion  of  the  ciliary  body,  run  along  the 
valleys  hvigging  the  sides  of  the  major  processes  and  find  insertion  into  the  lens 
anterior  to  the  equator.  Other  fibres  arising  more  anteriorly  pass  backwards 
to  find  insertion  behind  the  equator,  while  the  space  between  the  two  major 
systems  is  filled  with  fibres  arising  mainly  from  the  minor  processes  and  running 
perpendicularly  to  find  insertion  mainly  into  the  posterior  part  of  the  attachment 
zone  of  the  lens.  In  the  Primates,  on  the  other  hand,  fibres  arising  posteriorly 
in  the  orbicular  region  are  inserted  into  the  anterior  lens  capsule,  while  those 
arising  more  anteriorly  are  inserted  into  the  posterior  capsule,  the  latter  being 
reinforced  by  perpendicular  fibres  arising  far  anteriorly  ;  between  these  two 
main  systems  of  fibres  a  space  (the  "  canal  "  of  Hannover,  1852)  exists  which  is 
traversed  by  a  few  of  the  fibres  of  the  posterior  system  finding  attachment  to 
the  equator  itself  (Fig.  623). 

The  vitreous  gel  is  constituted  as  in  man,  the  electron  microscope 
showing  a  system  of  fibrils  (ox,  calf,  sheep,  pig,  rabbit — Schwarz  and 
Schuchardt,  1950  ;    Schwarz,  1951). 


Figs.   624  to  626. — Types  of  HvALOin  Vessel  (Ida  Mann) 


Fig.  624.— Fishes. 


Fig.  625. — Anurans. 


Fig.  626. — Mammals. 


Figs.    627  to  630. — Types    of   Rktinal   Blood    Supply   in   Vertebrates 
(excluding  the  falciform  process  of  Teleosts). 


Flu    327.— The         Fig.  628.— The      Fig.  629.— The  mem-     Fig.  630.— The 
avas;       AT  retina.      pecten  or  conus.  brana  vasculosa         arteria  centralis 

retinae.  retinae. 


MAMMALS  477 

The  Retinal  Vascularization 

The  hyaloid  system  of  vessels  is  unique  m  its  development  in 
Mammals  (Figs.  624-630).  We  have  already  seen  in  Fishes  that  this 
system  of  vessels  runs  along  the  ventral  part  of  the  globe  in  the  oj^en 
foetal  fissure,  an  arrangement  seen  in  its  most  fully  developed  form  in 
the  falciform  process  of  Teleosteans.  In  many  Amphibians  this 
arrangement  is  extended  to  constitute  a  superficial  membrana  vasculosa 
retinae.  In  the  Sauropsida  the  hyaloid  vessel  on  entering  the  eye 
atrophies  except  for  the  formation  of  a  conus  or  pecten  at  the  disc  itself. 
In  ]\Iammals  the  hyaloid  artery  in  embryonic  life  runs  directly  to  the 
posterior  jjortion  of  the  tunica  vasculosa  lentis,  while  a  multitude  of 
vessels  ramifies  in  the  vitreous.  These  vessels  disappear  in  the  later 
stages  of  embryonic  life,  the  only  visible  remnant  being  a  small  residuum 
of  glial  tissue  lying  on  the  optic  disc  (Bergmeister's  pajDilla).  Some- 
times this  condition  remains  in  the  adult  mammalian  eye  so  that  the 
retina  itself  is  avascular  ;  more  usually  vessels  grow  out  from  the 
hyaloid  trunk  and  invade  to  a  greater  or  less  degree  the  substance  of 
the  retina  itself  ;  in  this  event  the  hyaloid  trunk  becomes  the  central 
retinal  artery.  With  the  exception  of  the  eel  and  a  colubrid  snake, ^ 
it  is  only  within  the  class  of  Mammals  among  all  Vertebrates  that  a 
retina  directly  supplied  by  capillaries  is  found. 

The  mode  of  entrance  of  the  central  artery  varies  in  different 
species.  It  is  derived  from  the  ciliary  branch  of  the  external  ophthalmic, 
sometimes  supplemented  by  anastomosis  with  the  small  internal 
ophthalmic  artery.^  In  some  species  such  as  the  rabbit  a  central  artery 
accompanied  by  a  central  vein  enters  the  optic  nerve  and  runs  upwards 
to  reach  the  centre  of  the  disc  ;  there,  just  before  or  just  after  emerging, 
it  divides  into  nasal  and  temporal  branches  (Bruns,  1882  ;  Hen- 
derson, 1903  ;  Davis,  1929).  In  the  cat  the  central  retinal  artery 
was  found  by  Davis  and  Story  (1943)  to  be  invariably  occluded  and 
vestigial,  the  retina  being  supplied  by  the  terminal  posterior  ciliary 
branches  of  the  ciliary  artery.  In  the  dog,  on  the  other  hand,  there  is 
no  centra]  retinal  artery  but  several  posterior  ciliary  vessels  pierce  the 
sclera  around  the  optic  nerve-head  whei^e  they  give  off  retinal  branches, 
appearing  at  the  margin  of  the  disc  as  cilio-retinal  arteries.  In  this 
animal  a  central  vein  is  sometimes  present  but  even  when  it  exists  it 
immediately  breaks  up  to  leave  the  eye  with  the  marginal  arteries  to 
enter  the  subarachnoid  space  (Wolff  and  Davies,  1931).  Subendothelial 
cushions  were  described  by  Moffat  (1952)  in  the  ciliary  arteries  of  the 
dog,  the  contraction  of  which  might  act  by  shutting  off  the  choroidal 
blood  supply  and  diverting  it  to  the  retina.  In  the  Primates  including 
man,  the  central  retinal  branch  of  the  ophthalmic  artery  supplies  the 
whole  retina  ajjart  from  small  anastomoses  from  the  posterior  ciliary 

1  p.  390.  2  p_  498 


478 


THE   EYE   IN   EVOLUTION 


arteries  through  the  circle  of  Zinn  (Wybar,  1956),  but  in  the  lower 
Mammals  the  tendency  is  for  the  posterior  ciliary  arteries  to  assume 
greater  imf)ortance.  It  is  to  be  remembered,  however,  that  the 
appearance  of  arteries  emerging  from  the  optic  nerve-head  onto  the 
retina  in  a  marginal  position  around  the  disc,  a  formation  suggestive  of 

Figs.     631     to     634. — Types    of    Placental    Retinal    Vascularization 
(See  also  Plates  XIV  and  XV.) 


iio.   bol. — The  FuNDL-i  wi    jiiL  Dot.. 
The  lightly  coloured  area  is  the  tapetum. 
There  is  a  venous  circle  at  the  disc. 


Fig.   G3_'. — The  Fundus  of  the  Cat. 
The  lightly  coloured  area  is  the  tapetum. 


Fig.    633. — The   Fundus   of   the   Rabbit. 

The  ves.sels  are  confined  to  the  leashes  of 
opaque  nerve  fibres. 


Fig.    634. — The    Fundus    of    the    Horse. 

The  lightly  coloured  area  above  the  disc 
is  the  tapetum. 


a  ciliary  origin,  does  not  jDreclude  their  derivation  from  a  central  artery 
that  has  broken  up  into  retinal  branches  in  the  substance  of  the 
nerve. 

Among  the  Placentals  almost  every  possible  variety  of  retinal 
vascularization  occurs,  ranging  from  a  complete  absence  of  vessels,  in 
whicl  ise  the  retina  is  nourished  entirely  from  the  choriocapillaris,  to 
an  elu'      ate  system  covering  the  entire  retina  in  which  the  capillaries 


I\L\MMALS 


479 


may  penetrate  as  far  as  the  nuclei  of  the  rods  and  cones. ^  Leber 
(1903)  divided  the  retinae  of  Placentals  in  this  respect  into  4  groups  : — 
{a)  HOLANGiOTic  (oAo?,  all  ;  dyyelov,  vessel)  (Plates  XIV,  XV  ; 
Figs.  631-2).  The  whole  retina  receives  a  direct  blood  supply  either 
from  a  central  artery  or  from  cilio -retinal  arteries  which  emerge  either 
as  a  single  trunk  or  as  several  branches  from  or  around  the  optic  disc. 
This  type  of  vascularization  occurs  in  some  Insectivores  (the  hedgehog, 
Erinaceus.  tlie  mole.  Talpa).  some  Rodents  (mouse,  squirrel,  marmot). 


Fig.  bo.J 


The  Fundus  of  the  Squirrel,  Scjcju': 
(Lindsay  Johnson). 


some  Carnivores   (Felidse,  Canidse,  Ursidse,  some  Viverridse   and  the 
Pinnipedia),  in  a  few  Ungulates  (pig.  ox),  and  the  Primates. - 

In  Primates  the  central  artery  emerges  from  the  disc  as  a  single  vessel, 
but  more  usually  several  large  arteries  emanate  therefrom  ;  in  Carnivores 
a  number  of  small  arteries  of  the  ciliary  type  emerge  from  the  margin  of  the 
disc.  In  the  squirrel  and  the  marmot  the  disc  is  a  long  horizontal  line  from  the 
entire  length  of  which  the  vessels  emerge  (Fig.  635). 

(b)  MERAXGiOTic  (jnepo?,  jDart)  (Fig.  633).  Part  of  the  retina  is 
supplied  with  vessels.  This  is  only  seen  in  the  Lagomorpha  (rabbit 
and  hare),  in  ^hich  the  vessels  are  limited  to  the  horizontal  expansions 
of  medullated  nerve  fibres  (Figs.  633,  637). 

1  For  literature,  see  particularly  H.  Muller  (1861).  Sattler  (1876),  Leuckart  (1876), 
His  (1880),  Brims  (1882),  Barrett  (1886),  Schuitze  (1892),  Johnson  (1901),  Leber  (1903), 
Darnel  and  Fortin  (1937)  (bat),  Michaelson  (1948-54),  Rohen  (1954)  (rabbit). 

^  Comijare  also  the  Marsupials,  Didelphys  and  Petaurus,  p.  440. 


480 


THE   EYE   IN   EVOLUTION 


(c)  PAURANGiOTic  {nocvpog,  small)  (Plate  XV  ;  Fig.  634).  The 
vessels  are  very  minute  and  extend  only  a  short  distance  from  the  disc. 
This  occurs  in  Perissodactyla  (horse,  tapir,  rhinoceros  which  has  only 
capillaries  around  the  disc),  the  elephant,  the  Hyracoidea,  the  Sirenia 
{Manatus,  Halicore)  and  among  the  Rodents  in  the  guinea-pig  {Cavia 
porcinus)  (Fig.  636). 

(d)  ANANGiOTic  (a,  privative)  (Plate  XV).  The  retina  is  without 
vessels.  This  group  comprises  the  more  primitive  Mammals  and 
includes  most  of  the  Chiroptera  (Ijats),  the  Xenarthra  (sloths  and 
armadillos),  and  certain  Rodents  (the  porcupine,  Hysfrix,  the  chin- 
chilla,   the  beaver,   Castor,   and  otliers).     Many   of  these   anangiotic 


Fig.  636. — Retinal  Vessels  of  the  Horse. 

A,  the  general  arrangement  of  tlie  retinal  vessels.  B,  a  portion  of  the 
vascularized  retina  of  the  horse  showing  the  peripheral  loops,  the  T-shaped 
loops  between  the  branches  of  the  main  vessel.  There  are  many  fine  vessels 
in  the  optic  nerve-head.     Specimen  injected  with  Indian  ink  (after  L.  Bruns). 


Fig.   637. — Retinal   \  essels  of  the   Young  Rabbit. 
•d  with  Indian  ink,  mounted  in  glycerine  (  X  16)   (I.  C.  Michaelson) 


Plates  XIV  and  XV 
THE  FUXDI  OF  PLACEXTALS 


PLATE  XIV 
The  Fundi  or  Placentals     I 


Fig.  1. — The  toque  monkey,  Macaca  pileata.       Fig.   2. — Monteiro's  galago.   GdUigo  nionteiri. 


Fig.  3. — The  raccoon.  Procyon. 


Fig.  4. — The  coruinDn  seal,  Phoca  vitidina.  Fig.  5. — The  hog  deer,  C'crous  porcinus 

(Figs.  1  and  .3,  Arnold  Sc)r.sl)y;  Figs.  2,  4  and  .'3,  Lindsay  -Tohnson.) 


PLATE  XV 

The  Fundi  of  Placextals  :  IT 

(Lindsaj^  Johnson) 


I-'ic.    1. — The    Indian    rhinocero.s.    lihiiioccros        Fio.    2. — The   Australian   fruit-hat.    Ptero/j/is 
iiii  icorii  is.  poUocephahif!. 


Fir;.  .'}. — The  common  heiluchog,  Eiiikiciiin  eiirop(run. 


Fk;.  4 — The  flsiiiL!  -iiuiinl.  I'h  roiiui-s  ulbori(fii.s.         l-"i(;.  5. — The  ('aiiailian   beaver,  (iistor  raiinr/eii.sis. 


MAMMALS 


481 


animals,  particularly  the  Rodents,  possess  a  capillary  rascularization 
on  the  optic  nerve-head  associated  with  a  button-like  projection 
visible  ophthalmoscopically,  reminiscent  of  the  papillary  conns 
of  Reptiles.  1  A  j^ersistent  hyaloid  artery  arising  from  the  disc  is 
more  connnon  and  is  normal  in  a  large  number  of  Rodents  and  all 
Ruminants. 

The  depth  to  wliicli  the  vessels  jjenetrate  the  retina  varies  con- 
siderably. In  some  Insectivora  (the  hedgehog  and  the  mole)  the  large 
vessels  lie  sui^erficially,   each   casting  a  shadow  ophthalmoscopically 


'^^^ 


^    Ah 


¥^ 


E«?^-'. 


"•       .>    * 


Fig.   G3S. — Section  of  the  Retina  of  the  Rabbit. 

Inclucliiig   tlie   niedullated   nerve   fibres.      Tlie   large   vessels   are   clearl\'   -pve- 
retiiial  (I.  C.  ]\Iichaelsoii). 


(Barrett.  1880)  :  similarly  in  some  Rodents  (mouse,  rabbit)  they  are 
also  verj^  superficial  and  only  ]jartially  embedded  (Fig.  638).  The 
capillaries  may  n(jt  penetrate  so  deeply  into  the  retinal  tissues  as  in 
man.  In  the  horse  and  the  rabbit  they  reach  the  nerve-fibre  layer  only  ; 
in  the  cat  the  ganglion  layer  ;  but  in  most  diurnal  types  with  a 
holangiotic  retina  the  capillaries  are  reflected  in  the  outer  plexiform 
laj^er  as  in  man.  In  these  the  reticular  capillary  system  is  usually  well 
developed  and  consists  of  t\\o  main  networks,  an  internal  lying  in  the 
nerve-fibre  layer,  and  an  external  lying  in  the  outer  portion  of  the  inner 
nuclear  layer,  the  meshes  of  the  deeper  net  being  smaller  than  the 


^   Compare  the  Marsupials,  p.  440. 


S.O.— TOL.  I. 


31 


482  THE   EYE   IN   EVOLUTION 

superficial.  In  most  cases  the  superficial  net  is  formed  by  the  end- 
branches  of  the  arterioles  which  do  not  reach  the  deeper  net  ;  the  two 
nets,  however,  intercommunicate  freely  by  perpendicular  or  oblique 
capillary  vessels,  while  the  latter  drains  into  the  retinal  veins  and  in  all 
cases  there  is  a  zone  free  from  capillaries  around  the  arteries  (His, 
1880  ;  Bruns,  1882).  In  some  species  of  Rodents,  however,  members 
of  the  family  Gliridse  (dormice)  such  as  Glis  and  Eliomys,  and  the 
flying  squirrel  {Pteromys),  the  capillaries  penetrate  more  deeply, 
reaching  to  the  outer  nuclear  layer  to  supply  the  bodies  of  the  visual 
cells  and  are  not  reflected  until  thej^  approach  the  external  limiting 
membrane  (Kolnier,  1929  ;  Rochon-Duvigneaud,  1943)  ;  in  these 
animals  it  is  interesting  that  the  choroid  is  unusually  thin. 

It  may  be  useful  at  this  point  to  summarize  the  vascularization  of  the 
vertebrate  retina.  The  retina  is  avascular,  novirished  indirectly  from  the  choroid 
in  Cyclostomes,  Selachians,  the  coelacanth,  Chondrosteans,  Urodeles,  Sphenodon, 
Chelonians,  Monotremes,  Marsupials  (except  Macropodida?,  Petaurus  and 
Didelphys),  as  well  as  anangiotic  Placentals.  This  source  may  be  supplemented 
by  a  specific  structure — a  falciform  process  in  most  Teleosts  (except  eels,  Cypri- 
noids  and  goby-fish)  and  Holosteans  ;  a  conus  occurs  in  lizards  and  the  kiwi 
(rudimentary  in  C'rocodilians  and  the  Macrojaodidte)  ;  a  pecten  in  Birds  (except 
the  kiwi). 

Direct  vascularization  occurs  by  means  of  a  membrana  vasculosa  retinae 
in  a  few  Teleosteans  (certain  eels,  Cyprinoids  and  goby-fishes),  Dipnoi, 
Polypterini,  Anurans  and  Ophidians  :  in  the  eel  and  in  Tarbophis  the  vessels 
penetrate  into  the  retinal  substance.  Retinal  vessels  occur  only  in  some 
Marsupials  [Petaurus  and  Didelphys)  and  most  Placentals. 

The  'placental  retina  is  of  the  ordinary  vertebrate  type  with  none 
of  the  specific  peculiarities  so  frequently  evident  in  other  species  (Fig. 
639).^  In  its  general  architecture  it  does  not  show  the  same  density  or 
purity  of  lamination  as  is  seen  in  Birds  ;  these  features  are  most  fully 
developed  in  some  of  the  more  active  diurnal  Rodents  (the  squirrel, 
Sciurus  ;  the  prairie-dog,  Cynom.ys).  The  visual  elements  in  most 
species  are  duplex,  the  rods  outnumbering  the  cones  ;  the  cones  are 
always  single  and  are  of  simple  construction,  without  oil-droplets  or 
paraboloids  (Figs.  266-7).  In  some  of  the  lowest  nocturnal  forms  rods 
alone  are  present  (among  Insectivores  in  the  hedgehog  and  the 
shrew  ;  in  the  Chiroptera  ;  among  Xenarthra  in  the  armadillo  ; 
and  among  Primates  in  the  small  nocturnal  lemuroids,  such  as  the 
galago  and  the  loris,  and  in  Tarsius  and  Nyctipithecus).  The  noc- 
turnal Rodents  have  frequently  been  said  to  have  a  pure-rod  retina, 

1  For  descriptive  anatomy,  see  H.  Muller  (1856),  SchuUze  (1866-71),  Schiefferdecker 
(1886),  Dogiel  (1888),  Chievitz  (1891),  Cajal  (1894),  Krause  (1895),  Greeff  (1900),  Ziirn 
(1902),  Detwiler  (1924-49),  Woollard  (1925-27),  Uyama  (1934)  (cat),  Kolmer  and 
Lauber  (1936)  (all  classes),  Parry  (1953)  (dog),  Vonwiller  (1954)  (ox),  and  others.  For 
the  rih  ;a-structure  of  the  rods  of  the  guinea-pig,  see  Sjostrand  (1949-53),  of  the  rabbit, 
see  d.    ■;obertis  (1956),  of  tlie  synapses  of  the  visual  cells  see  de  Robertis  and  Franchi 

(1956; 


MAIVOIALS 


483 


but  in  the  rat,  the  mouse  (Schwarz,  1935),  the  dormouse  (Vilter,  1953) 
and  the  guinea-pig  (Kohner  and  Lauber,  1936  ;  O'Day,  1947  ;  Vilter, 
1949),  cones  are  present  although  they  are  very  few  ;  according  to 
Detwiler  (1949)  they  are  absent  in  the  chinchilla  ;  in  the  Cetacea 
(dolphins  and  whales)  the  cones  are  also  few  or  non-existent.  Only  in 
the    Sciuridse     (squirrels,^    and    particularly    the    marmot,    the    most 


i*» 


'ilHf  m  *.**. 


%  I 


I  f  f 


|9 


Fig.   639. — A  Mixed  Rod-and-cone  Placental  Retina. 
Section  thioiigh  tlie  parafoveal  part  of  the  retina  of  the  rhesus  monkej' 
(Mallory's  triple  stain,    X  480)  (Katharine  Tansley). 

1,  optic  nerve  fibre  layer  ;  2,  ganglion  cell  layer  ;  3,  inner  jalexiforni  layer  ; 
4,  inner  nuclear  layer  ;  .5,  outer  plexiform  layer  ;  6,  outer  nuclear  layer  ; 
7,  external  limiting  membrane  ;  8,  visual  cells  ;  9,  pigmentary  epithelium  ; 
10,  choroid. 


diurnal  of  all  Mammals  which  appears  only  during  daylight)  is  a  pure- 
cone  retina  known  to  exist  (Rochon-Duvigneaud,  1929  ;  Karli,  1951  ; 
Vilter.  1954).- 

The  contrast  between  tlie  different  types  of  retinal  structure  in 
Placentals  is  best  brought  out  by  a  comparison  between  the  rod-rich 

1  Except  the  nocturnal  flyiiig  squirrel,  Pteromys. 

^  For  physiological  evidence  based  on  the  spectral  sensitivity,   see  Arden  and 
Tansley,  1955  ;   based  on  adaptation,  see  Tansley,  1957. 


A 


,V 


m^^  ^  '-^W*-    .1^ 


«:*,  -*"     ••'^ 


Fig.  640.— The  Rod-kich  Placental  Retina. 
The  retina  of  the  rabbit  (Katharine  Tansley). 


7.  > 
10, 

Fig.  : 
and  'i 
the  otl 


Fig.  641. — The  Cone-rich  Placental  Retina. 

The  retina  of  the  squirrel  (Katharine  Tansley). 

1,  optic  nerve  fibre  layer  ;   2,  ganglion  cell  layer  ;  3,  inner  plexiform  layer  ; 

•ner  nuclear  layer  ;     .T,   outer  plexiform  layer  ;  6,   outer  nuclear  layer  ; 

■rnal  limiting  membrane  ;    8,  visual  cells  ;    9,  pigmentary  epithelium  ; 
I'oicl. 

'e  the  few  cells  in  the  ganglion  cell  la^•er  and  outer  nuclear  layer  in 

in  contrast  to  the  larger  numbers  in  Fig.  641.     Compare  Figs.  754 

In  Fig.  641  note  that  the  cones  (8)  are  in  two  layers,  one  behind 


IVIAMMALS 


485 


retina  of  the  rabbit  and  the  pure-cone  (or  virtually  so)  retina  of  the 
squirrel  (Figs.  640  and  641).  In  the  rod-doniinated  retina  the  outer 
limbs  of  the  rods  are  long,  the  outer  nuclear  layer  is  thick,  there  are  few 
ganglion  cells  and  few  optic  nerve  fibres.  In  the  retina  of  the  squirrel, 
on  the  other  hand,  the  visual  cells  themselves  are  rather  unusual  and 
somewhat  atj^ical,  being  arranged  in  two  layers,  one  outside  the 
other.  Those  of  the  inner  layer  have  long  striated  outer  limbs,  while 
in  those  of  the  outer  layer  this  structure  is  shorter  and  buried  in  the 
pigment  epithelium.  The  inner  nuclear  layer  is  unusually  thick  as  also 
is  the  ganglion  cell  layer  ;  there  are  only  2  to  4  visual  cells  to  each 
ganglion  cell  and  therefore  to  each  optic  nerve  fibre,  so  that  the  latter 
layer  is  again  unusually  prominent  (Arden  and  Tansley,  1955). 
According  to  Vilter  (1954)  the  ratio  of  cone  nuclei  to  ganglion  cells  in 
the  souslik,  Citellus,  is  200.000  :  90,000  for  the  whole  retina. 

An  area  centralis  specifically  elaborated  for  acute  vision  is  found 
among  Placentals,  but  not  commonly  (Chievitz,  1891  ;  Slonaker, 
1897  ;  Ziirn.  1902)  ;  most  require  no  specific  differentiation  for  their 
panoramic  vision.  When  it  does  occur  it  may  take  one  of  two  forms 
— a  band  stretching  across  the  posterior  part  of  the  fundus  or  a  cir- 
cular area  lying  temporal  to  the  optic  disc  ;  occasionally  both  are 
combined. 

A  band-shaped  area  is  seen  in  Rodents,  most  jDronounced  in  the  temporal 
region  ;  in  the  rabbit  it  is  a  broad  streak  3-4  mm.  wide  in  its  central  part  running 
just  vinderneath  the  optic  disc,  and  throughout  its  extent  the  retina  is  thicker 
than  elsewhere  particularly  in  its  rod-and-cone  layers  and  in  the  layer  of  ganglion 
cells  (Chievitz,  1891).  According  to  Krause  (1895)  the  content  of  visual  purple 
is  greater  within  this  area  than  elsewhere  ;  and  external  to  it  the  choroid  is 
thickened  (Davis,  1929).  The  sciuirrel  has  a  similar  (pure-cone)  band  but  less 
well  defined.  Amonsr  the  Ungulates,  some  Artiodactyls  (Ruminants  such  as 
the  ox)  have  a  similar  band-shaped  area  running  horizontally  above  the  disc 
and  the  lower  part  of  the  tapetum.  associated  with  a  round  area  centralis  in 
the  temporal  region. 

Such  a  temporal  round  area  is  common  in  Ungulates  (sheep,  goat,  horse,  etc.)  ; 
it  is  also  typical  of  the  Carnivores,  particularly  the  Felidse,  lying  lateral  to  the 
optic  disc.  In  this  family,  particularly  in  the  cat,  the  tiger  and  the  lion,  the 
area  centralis  becomes  highly  differentiated  ;  the  visual  elements  (cones, 
according  to  Thieulin,  1927)  are  closely  packed  and  ganglion  cells  are  accumulated 
in  several  layers,  while  there  is  an  external  depression  (an  "  external  fovea  ")  on 
the  choroidal  aspect  (Borysiekiewicz,  1887,  tiger  ;  Ziirn,  1902,  cat  ;  Briickner. 
1949,  lion).^  In  the  dog  also  there  are  said  to  be  no  rods  in  the  central  area 
(Ziirn,  1902).  Among  the  Primates  a  central  area  is  present  in  the  Prosimians 
(Lemur  catta,  L.  macaco,  etc.)  and  among  the  Simians  in  the  nocturnal 
Nyctipithecus.  In  Tarsius,  one  of  the  Prosimians,  the  macvilar  region  shows  a 
sudden  increase  in  the  number  of  percipient  elements  :  the  number  of  bipolar 
and  ganglion  cells  also  increases,  showing  that  the  elements,  although  still 
retaining  the  morphological  characteristics  of  rods,  are  assuming  the  physiological 

1  According  to  Wolfflin  (1047),  who  examined  a  h\'pnotized  lion,  the  macula  is  not 
ophthalmoscopically  visible. 


Tarsier 


486 


THE   EYE   IN   EVOLUTION 


Primate 
(squirrel  monkey) 


characteristics  of  cones.     There  is,  however,  no  displacement  of  the  bipolar  cells 
or  nerve  fibres  and  no  true  fovea. 

A  fovea  occurs  only  in  the  Primates,  appearing  first  in  Tarsius  ; 
it  and  Nyctipithecus  have  a  pure-rod  fovea  (Polyak,  1957).  All  the 
Anthropoidea  except  Nyctipithecus  have  a  central  area  and  a  well- 
formed  pure-cone  fovea  of  the  same  type  as  man,  which  the  retinal 
vessels  approach  and  encircle  but  do  not  invade  (Fig.  642)  (Woollard, 
1926).! 

The  02ytic  disc  in  the  majority  of  Placentals  is  circular  as  in  man, 
but  in  some  Carnivores  (Canidse,  as  the  wolf,  jackal,  fox)  it  is  kidney- 
shaped  and  in  many  Ungulates  and  all  Equidse  it  is  horizontally  oval. 


|li!Sr*'i 


Fig.    642. — The   Fovea   of   a   Primate. 
Macaca  rhesus  (  X  114)  (Katharine  Tansley). 


In  most  Sciurida3  this  is  exaggerated  to  form  a  unique  type — a  long, 
thin,  tape-like  structure  stretching  horizontally  across  the  fundus 
above  the  axis  of  vision — which  reaches  its  greatest  development  in  the 
marmot  (Fig.  635)  ;  this  arrangement  gives  excellent  uj^ward  vision 
for  the  arboreal  family  of  squirrels.  The  optic  disc  lies  on  the  level  of 
the  surface  of  the  retina  except  in  Carnivores  and  the  flying  squirrel, 
Pteromys,  wherein  it  is  sunk  to  form  a  deep  pit.  It  varies  considerably 
in  colour  ;  usually  white  or  jDink,  it  is  red  in  the  Equidse,  bright  red  in 
the  hedgehog  and  mole,  pink  surrounded  by  a  green  ring  in  the  seal. 

The  02Jtic  nerve  is  of  the  standard  type  seen  in  man,  the  only 
excejitional   feature    being   the    enormously   thick    accessory    sheath 


1  Bliimenbach  (1805),  Albers  (1808),  and  Soemmerring  (1818)  in  several  of  the 
Simians;  Slonaker  (1897)  in  the  gorilla;  Wolfrum  (1908)  in  Macacus  ;  Franz  (1912) 
in  JJylobates  ;  Woollard  (1925-27)  in  several  of  the  Anthropoidea  ;  Detwiler  (1943) 
in  il  0  marmoset  and  the  rhesus  monkey. 


MAMMALS  487 

already  noted  ^  to  be  present  in  whales,  the  hippopotamus  and  the 
elephant  ;  some  of  the  fibres  are  non-myelinated  (Bruesch  and  Arey, 
1942).  A  minute  subdivision  of  the  fibres  into  fasciculi  is  common 
only  among  Mammals,  and  there  is  evidence  that  the  complexity  of 
the  glial  framework  increases  in  proportion  to  the  visual  development 
of  the  animal  in  the  evolutionary  scale  (Deyl.  1895). 

The  inner  architecture  and  septal  system  of  the  optic  nerve  throughout  the 
Vertebrates  is  interesting  in  this  respect.  As  occurs  ontogenetically  in  man, 
Cyclostomes  show  merely  a  central  column  of  ependymal  cells  which  have 
become  invaginated  within  the  developing  nerve,  and  from  them  processes 
radiate  outwards  towards  the  periphery.  The  same  arrangement  is  seen  in  the 
Dipnoan,  Protopterus.  In  some  Selachians  and  other  Dipnoans  and  in  snakes 
this  simple  arrangement  is  reduplicated  and  the  nerve  is  broken  up  into  a  number 
of  bundles  each  of  which  has  a  similar  core  of  cells.  In  the  remainder  of  the 
Vertebrates  the  pattern  is  altered  :  oligodendi'oglial  cells  (derived  from  the 
original  ependymal  cells)  are  scattered  throughout  the  nerve.  As  the  visual 
functions  become  more  highly  developed  in  the  higher  Vertebrates  and  man, 
the  fascicvilation  becomes  progressively  less  obvious,  the  number  of  fibre -bundles 
increasing  and  the  original  ependymal  system  becoming  more  uniformly  dispersed 
throughout  the  whole  structure. 

It  is  interesting  that  the  lamina  cribrosa  at  the  ojDtic  nerve-head  shows  wide 
variations.  In  general  it  may  be  said  that  in  those  Mammals  which  have  good 
day-vision  this  structure  is  well  developed  with  many  collagenous  fibres  (squirrel, 
cat,  monkey),  while  in  species  with  a  poor  visual  capacity  (Rodents  such  as  the 
rat,  mouse  and  rabbit)  the  lamina  is  absent  and  the  retina  may  even  herniate 
in  folds  into  the  optic  nerve  sheath  (Tansley,  1956)  (Figs.  643-6). 

In  all  Vertebrates  below  Mammalia  the  decussation  of  the  optic 
nerve  fibres  at  the  cliiasma  is  complete  (or  jjractically  so  in  some 
Reptiles  2)  so  that  each  eye  is  connected  solely  with  the  opposite  side 
of  the  brain  (Harris.  1904  :  Kappers,  1921)  ;  in  all  Placentals  it  is 
incomplete,  but  the  crossed  fibres  always  remain  the  more  numerous. 
In  Vertebrates  below  Mammals  the  fibres  remain  in  distinct  and 
separate  fasciculi  as  they  cross  ;  in  Placentals  they  become  intimately 
intertwined  and  interlaced  (Cajal.  1898  ;  Bossalino.  1909).  In  general 
the  number  of  imcrossed  fibres  varies  with  the  degree  of  frontality  of 
the  eyes  (Newton.  1704  ;  J.  Midler,  1826  ;  Gudden,  1879)  ^  ;  in  animals 
with  laterally  directed  eyes  they  are  relatively  few  *  ;  they  number 
about  1/6  of  the  total  in  the  horse. ^  1/4  to  1/3  in  the  dog  ^  and  cat," 
about  1/3  in  the  higher  Primates,  and  about  1/2  in  Man.^  TJiis  arrange- 
ment whereby  corresponding  half-fields  of  each  retina  are  connected  to 

1  p.  4.")1.  2  Snakes,  p.  392. 

^  A  relationship  sometimes  referred  to  as  the  Law  of  Xevvton-Miiller-Gudden. 

*  Rodents  such  as  the  rat  and  rabbit,  Bellonei  (1884),  Singer  and  Miinzer  (1 
Pick  and  Herrenheiser  (1895),  Brauwer  and  Zeeman  (1925),  Overbosch  (1926). 

5  Dexler  (1897). 

«  Vitzou  (1888). 

'  Nieati  (1878).  Brauwer  and  Zeeman  (1925),  Overbosch  (1926). 

*  Brauwer  and  Zeeman  (1925). 


488 


THE   EYE   IN  EVOLUTION 


Figs.  643  to  645. — The  Optic  Nerve-head  or  Placentals. 


Fk;.   643. — The  Optic  Xerve-head  of  the  Rabbit. 
Note  the  absence  of  collagen  fibres  at  the  site  of  the  lamina  cribrosa 
(Kolmer's  fixative  ;    Azan  ;     X  27)  (Katharine  Tansley). 


•  <• 


i 


^  ^      ^-'^ 


'•*'•'•- .  ■«.'^      •     -^S^j"^* 


Yw,.  CiH.      Tin:  ( )i']i(    Xerve-head  op  the  Mouse. 

Note  the  band  of  evenly  arranged  oval  nuclei  running  across  the  nerve 
(Kolmer's  fixative  ;    Feulgen  ;     x  369)  (Katharine  Tansley). 


Fig.  645. — The  Optic  Nerve-head  of  the 

Note  the  well-developed  collagenous  fibres  at  the  lamina 
fixati\o  ;   Azan  :    X  50)  (Katharine  Tansley). 


(Kolmer's 


MAMIMALS 


489 


the  same  side  of  the  bram  lays  the  foundation  for  full  coordination, 
visual  and  motorial,  between  the  two  eyes.^ 

The  semi-decussation  of  fibres  results  in  great  alterations  in  the  finer 
structure  of  the  lateral  geniculate  body,  the  relay  station  between  the  optic 
nerve  fibres  and  the  cerebral  cortex.  It  will  be  seen  -  that  in  the  lower 
Vertebrates  this  structure  is  insignificant  but  that  in  Mammals  in  which  visual 
projections  on  a  considerable  scale  are  first  relayed  to  the  cortex  it  becomes 
inuch  inore  complex,  particularly  the  dorsal  nucleus  to  which  this  function 
is  assigned.     In  the  lower  Mammals  this  structure  is  relatively  simple  and  it 


o. 


m^.M^ 


Fig.  646. — The  Lamina  Cribrosa  of  the  Kitten. 
Twenty-four  hours  before  birtli  (Wilder's  stain  ;     ;■,   160)  (Katharine  Tansley 


would  seem  that  each  optic  ner\e  fibre  connects  with  several  cells  in  the  geniculate 
body  which  itself  shows  no  ordered  lamination.  In  the  Australian  opossum, 
Trichosurus  viilpecula,  an  agile  arboreal  animal,  however,  the  dorsal  nucleus 
shows  a  four-layered  structure  (Packer,  1941),  while  in  Carnivores  and  Primates, 
six  layers  appear  (Le  Gros  Clark,  1941-42).  This  system  of  lamination  is  associa- 
ted with  the  partial  decussation  of  optic  nerve  fibres  in  the  chiasma — a 
characteristic  of  INIammalia  :  in  the  opossum  crossed  fibres  terminate  in  the 
1st  and  3rd  layers,  uncrossed  in  the  2nd  and  4th  ;  in  the  Primates  crossed  fibres 
terminate  in  the  1st,  4th  and  6th  layers,  uncrossed  in  the  2nd,  3rd  and  5th 
layers  (Figs.  647  and  648).  In  the  Primates  also  each  retinal  cell  is  projected 
onto  the  geniculate  body  in  a  point-to-point  manner.  The  reception  unit  for 
each  of  a  pair  of  retinal  corresponding  points  is  thus  a  band  of  cells  involving 
three  lainina?,  while  the  projection  unit  onto  the  visual  cortex  is  a  band  of  cells 
involving  all  six  layers. 

^  See  further,  p.  697. 
2  p.  541. 


490 


THE   EYE   IN   EVOLUTION 


Figs.  647  and  648. — The  Representation  of  the  Retina  on  the  External 
Geniculate  Body. 


4  3  21 

Fig.   647. — In  the  Australian  Opossum  (after  Packer). 


6  5  4   3  21 

Fig.   648. — In  the  Primate  (after  Le  Gros  Clark). 

Impulses  from  corresponding  points  (a,  b)  in  the  two  retinas  pass  up  the  optic 
tract.  Uncrossed  impulses  (a')  terminate  in  laminje  2  and  4  in  the  opossum, 
and  2,  3  and  5  in  the  Primate.  Crossed  impulses  (6')  terminate  in  laminse  1  and 
3  ill  the  opossum  and  1,  4  and  6  in  the  Primate.  These  fibres  terminate  in  a 
rec  otion  unit  in  the  lateral  geniculate  body  which  forms  a  band  of  cells 
rac!  ,_    from    the    hilum    of   the    nucleus.      The    projection    unit    from   the 

Iatei;i    i.niculate  body  (c)  to  the  visual  cortex  forms  a  band  of  cells  involving 
all  the  1  uninse  in  each  case. 


MAMIVIALS  491 


THE    OCULAR   ADNEXA 

The  conjunctivce  of  many  Mammals  show  large  papillae  (horse)  or 
follicles  (ox,  dog,  pig,  rabbit)  which  are  not  present  in  the  physiological 
state  in  man  (Bruch,  1853  ;  Morano,  1873  :  Miimi,  1935).  There  is 
usually  an  accumulation  of  pigment,  especially  near  the  limbus,  but  fre- 
quently continued  into  the  cornea,  contained  in  branched  contractile 
cells.  The  transition  from  the  conjunctival  to  the  corneal  epithelium 
is  usually  gradual,  but  in  some  animals  (horse)  it  is  abrupt  (Zietzsch- 
mann,  1904).  Variations  occur  in  the  conjimctival  glands  ;  thus  sweat 
glands  are  seen  in  the  bulbar  conjunctiva  of  the  pig.  the  goat  and  the 
ox.  Small  diverticuli  filled  with  epithelial  cells  somewhat  resembling 
epithelial  cell-nests  forming  tubular  depressions  near  the  limbus  were 
first  described  in  the  pig  as  the  glands  of  Manz  (Manz,  1859  ;  Stromeyer, 
1859),  vestigial  traces  of  which  may  be  seen  in  man.  Their  function  is 
uncertain  ;  according  to  Aurell  and  Kornerup  (1949)  they  are  the 
remnants  of  accessory  lacrimal  glands  which  develop  in  the  pig  in 
embryonic  life,  sorae rimes  persisting  in  the  form  of  epithelial  buds  and 
sometimes  as  tubules  with  poorly  developed  lumina. 

In  the  typical  Placental,  three  eyelids  are  present — an  upper,  a 
lower,  and  a  nictitating  membrane  (or  third  eyelid)  ;  the  aquatic 
Placentals,  however,  form  an  exception.^  Of  the  tlu-ee,  the  upper  lid, 
as  in  Selacliians,  is  the  more  fully  developed  and  with  few  exceptions 
(elephant,  deer,  hippopotamus,  mouse)  descends  more  than  the  lower 
ascends — a  reverse  of  the  action  seen  in  most  lower  Vertebrates  wherein 
the  lower  lid  is  the  more  mobile. ^ 

It  i.s  interesting  that  Mammalia  is  the  only  class  wherein  spontaneous 
shutting  and  ojDening  of  the  lids  or  blinking  is  highly  developed  ;  although 
sometimes  slow,  particularly  in  primitive  fomis,  the  blink-movements  are  usvially 
very  rapid,  and  except  in  types  with  completely  lateral  eyes,  the  blink 
reflexes  of  both  eyes  respond  when  one  is  threatened  or  touched. 

The  upper  lid  always  has  a  stiffening  tarsal  plate,  the  lower 
sometimes;  it  is  usually  comprised  of  dense  fibrous  tissue  but  is  occasion- 
ally cartilaginous  (in  the  hedgehog,  bat  and  leopard,  Anelli,  1936). 
Embedded  in  the  tarsi  and  opening  on  the  lid-margin  are  tarsal 
(meibomian)  glands  providing  an  oily  secretion  ;  in  view  of  the  fact 
that  they  evolve  from  the  glands  of  hair-follicles  it  is  understandable 
that  they  are  found  only  in  Mammals.  In  Mammals  the  tarsal  glands 
are  usually  smaller  than  in  man  :  they  are  absent  in  aquatic  types, 
replaced  by  Zeis"s  glands  in  the  elephant,  and  by  sebaceous  glands  on 
the  caruncle  in  the  camel  (Richiardi,  1877).   At  the  external  angle  they 

1  p.  501. 

^  The  lower  lid  is  the  more  mobile  in  Amphibian.s,  Reptile.?  (except  Anolis  alligator 
wherein  both  are  equally  mobile,  and  ?  Crocodilians)  and,  with  few  exceptions,  Birds. 


492  THE   EYE   IN  EVOLUTION 

are  large  and  modified  in  some  Rodents  (Loewenthal,  1931).  Glands 
of  Moll  are  present  in  many  Ungulates  (ox,  pig),  Carnivores  (dog,  cat), 
and  Primates  (apes,  man)  ;  but  in  Rodents  they  are  absent  (rabbit, 
guinea-pig,  rat,  mouse)  (Ikeda,  1953).  Most  Mammals  have  cilia 
(Zietzschmann,  1904),  the  whale,  elephant  and  hippopotamus  being 
exceptions  (Matthiessen,  1893)  ;  among  domestic  animals  those  of 
the  lower  lid  are  rudimentary,  while  localized  absences  occur,  such  as  in 
the  mid-region  of  the  upper  lid  of  the  horse  (F.  Smith,  1922).  Eyebrows 
are  specialized  in  many  Placentals  (particularly  the  cat)  into  long 
tactile  vibrissas  ;  the  camel  has  a  somewhat  similar  formation  on  its 
lower  lid. 

The  movements  of  the  two  main  lids  are  elaborately  controlled  by 
muscles.  In  terrestrial  Placentals  they  are  closed  by  the  con- 
traction of  the  annular  orbicularis  oculi  muscle  with  a  sphincter-like 
interlacing  system  of  fibres  (Zietzschmann,  1904  ;  Meinertz,  1932-42  ; 
Rohen,  1953-54).  All  are  provided  with  a  levator  palpebrae  superioris, 
except  the  aquatic  Cetaceans  which  have  a  dilatator  rimae  palpebrarum 
distributed  round  the  lids  (Stannius,  1846,  in  dolphins  ;  Virchow,  1910, 
in  whales).  The  elephant  has  a  depressor  palpebrae  inferioris  similar 
to  the  levator  of  the  upper  lid  (Virchow,  1910),  and  in  Herbivores  the 
external  malar  muscle  serves  as  a  depressor  of  the  former. 

The  palpebral  muscles  of  Miiller  are  more  fully  developed  in  lower  Mammals 
than  in  man  :  in  aquatic  Mammals  the  fibres  are  striated,  in  terrestrial  Mammals 
they  are  plain.  According  to  CJroyer  (1903)  they  are  developed  in  association 
with  the  superior  and  inferior  recti  :  these  divide  into  two  parts,  one  of  which 
is  striated  and  is  inserted  into  the  eyeball,  the  other  is  inserted  into  the  lids. 
Owing  to  the  great  development  of  the  upper  lid,  the  muscle  running  to  it 
divides  again  into  two,  forming  a  large  levator  muscle  anteriorly,  and  a  small 
palpebral  mviscle  posteriorly.  In  those  cases  wherein  the  palpebral  muscles  are 
composed  of  plain  fibres,  they  are  supplied  by  the  sympathetic  nerve,  but  where 
they  are  striated  they  are  supplied  by  the  nerves  to  the  recti. 

The  third  eyelid  in  Placentals  is  characteristically  rudimentary  ; 
although  often  reinforced  by  a  plate  of  hyaline  cartilage  it  lacks  a 
specific  musculature  as  is  found  in  so  many  lower  Vertebrates. 
Entirely  passive  in  its  movements,  it  is  rarely  functional,  slipping 
over  the  eye  when  the  globe  is  retracted.  Occasionally,  as  in  the  bear 
and  the  rhinoceros,  it  drifts  partly  across  the  cornea  when  the  animal 
becomes  sleepy.  The  mechanism  of  its  movement  is  much  less  specialized 
than  in  lower  Vertebrates,  for  any  muscular  elements  it  contains  are 
merely  vestigial.  It  seems  to  be  forced  out  from  the  canthus  across 
the  cornea  by  the  propulsive  action  of  the  retractor  bulbi  muscle  as  it 
pulls  the  eyeball  inwards  ;  while  the  return  of  the  membrane,  although 
probah\\  largely  due  to  its  own  elasticity,  may  be  helped  by  the  opposite 
action       the  orbital  muscle  of  Miiller.    It  is  most  rudimentary  in  the 


MAI^HVIALS 


493 


lower  forms  (Insectivora,  Chiroptera,  Edentata  and  Rodentia)  and  in 
Primates  ;  in  these  with  few  excejDtions  it  is  immobile  (Law,  1905  ; 
Anelli,  1935).  In  one  monkey  {Macacus  speciosus)  it  is  capable  of 
slight  movement  (Jolmson,  1901).  and  in  the  aard-vark,  Orycterojius, 
it  is  freely  motile  over  the  keratinized  cornea,  probably  acting  as  an 
added  protection  against  the  formic  acid  ejected  by  the  ants  on  which 
it  feeds.  In  the  C'arnivora,  ajiart  from  the  Mustelidse,  it  is  more  fully 
developed,  but  in  the  skunk,  with  its  proptosed  eyes,  it  is  altogether 
lacking.  In  a  few  Carnivores  it  is  larger  (cat,  giant  panda,  bear,  deer), 
wliile  in  Ungulates  it  is  most  highly  differentiated  ;  in  these  it  is 
sufficiently  large  to  be  swept  passively  but  rapidly  right  across  the 
cornea  when  the  globe  is  retracted  and  it  is  probable  that  it  serves  a 
valuable  function  in  these  animals  by  giving  protection  to  the  eyes 
from  long  grasses  when  they  graze. 

Among  Placentals  the  nictitating  membrane  has  a  basis  of  hyaline  cartilage 
in  most  domestic  animals  (horse,  donkey,  ox,  dog,  wolf,  pig,  goat,  cat,  hare, 
etc.)  ;  in  the  rabbit  (as  in  Birds)  its  basis  is  merely  cellular  parenchymatous 
tissue  (Naglieri,  1932).  Acinous  glands  resembling  the  lacrimal  gland  in  structure 
are  also  present  (Anelli,  1935)  ;   muscular  fibres  are  vestigial. 

Most  Placentals  possess  two  orbital  glands.  A  lacrimal  gland 
secreting  a  watery  fluid  is  situated  in  the  upper  temporal  quadrant  ; 
as  is  usually  the  case  among  Vertebrates  it  is  associated  with  the  more 
mobile  lid,  in  this  class,  the  upper.  We  have  seen  that  in  terrestrial 
Amphibians  in  which  the  gland  first  ap2:>ears  in  order  to  maintain  the 
watery  environment  of  their  ancestors  for  the  protection  of  the  cornea, 
it  is  situated  at  the  medial  canthus  in 
association  with  the  lower  lid;  in  Reptiles 
and  Birds  it  migrates  to  the  outer  canthus 
still  maintaining  the  same  association  with 
the  lower  lid  ;  in  Mammals  it  appears  at 
the  lateral  angle  beneath  the  upper  lid 
(Lor,  1898)  (Fig.  G49).  The  structure  of  the 
gland  varies  :  it  is  tubular  in  man,  but 
is  alveolar  in  some  Mammals  (horse,  pig, 
ox  ;  Mobilio,  1912-13)  ;  in  some  animals  it 
empties  by  a  single  duct  (Rodents). 
Sirenians,^  the  pronghorn,  Antilocapra 
americana,  and  the  mouse  family  are  said  to 
lack  a  lacrimal  gland  -  ;  in  the  pig  its 
secretion  is  mucoid  rather  than  watery,  and 
in  Cetaceans  it  is  oily.^ 

1  p.  502. 

*  A  lacrimal  gland  is  also  lacking  in  Cyclostomes,  Fishes,    aquatic   Amphibians, 
Sphenodon,  Ophidians,  penguins  and  owls. 
3  p.  502. 


Fig.    649. — The    Migration 

OF    THE    LaCRIM.\L    GlAND 

IN  Phylogenetic  Deve- 
lopment. 

^4,  position  in  Amphibians; 
/?,  position  in  Reptiles  and 
Birds  ;  .1/,  position  in  Mam- 
mals (after  Wiedershein). 


494  THE   EYE   IN   EVOLUTION 

The  tears  are  drained  away  by  the  lacrimal  passacjes.  Since  the 
lacrimal  gland  was  originally  situated  at  the  nasal  end  of  the  lower  lid, 
the  lacrimal  passages  are  always  located  in  this  region.  These  passages 
are  built  on  the  same  general  plan  throughout  the  Vertebrates  and 
only  minor  modifications  exist  (Walzberg,  1876  ;  Lichal,  1915  ; 
Rochat  and  Benjamins,  1916  ;  Sundwall,  1916).  The  puncta  usually 
open  on  the  inner  surface  of  the  lid,  not  on  the  margin  as  in  man.  The 
rabbit  has  one  (inferior)  canaliculus  (Monesi,  1906  ;  Rochat  and 
Benjamins,  1916  ;  Zaboj -Bruckner,  1924).  The  sac  is  rudimentary  or 
lacking  in  most  domestic  animals.  In  some  (such  as  the  rat)  the  naso- 
lacrimal duct  is  small  and  inconspicuous.  In  others  (such  as  the 
guinea-pig)  it  is  wide  with  a  well-developed  ciliated  epithelium  and 
surrounded  by  a  rich  venous  plexus  ;  in  others  again  (such  as  the 
horse)  it  is  relatively  narrow  (1  to  2  mm.)  with  several  dilatations 
(1  to  2  cm.)  throughout  its  length  (Kelemen,  1950  ;  and  others).  The 
passages  are  completely  lacking  in  aquatic  types  (the  Pinnipedes,  the 
Mustelidse,  the  hippopotamus,  and  the  Cetaceans)  and  the  elephant 
(Sardemann,  1884). 

The  two  lacrimal  puncta  separate  a  portion  of  the  lower  lid  to  form  the 
caruncle.  Since  it  is  isolated  from  the  margin  of  the  lower  lid  by  the  develop- 
ment of  the  canaliculus,  the  caruncle  is  absent  in  those  animals  which  have  no 
lacrimal  apparatus  (Bromann  and  Ask,  1910).  Frequently  its  cutaneous  origin 
is  emphasized  by  its  continuity  with  the  lid -margin  (calf  and  dog)  ;  it  may  be 
deeply  pigmented  (Fey,  1914),  and  contains  tubular  muc<jus  glands  (Caprino, 
1955). 

Harder' s  gland  (1694),  an  acino-tubular  gland  the  primary  function 
of  which  is  to  lubricate  the  nictitating  membrane,  lies  on  the  nasal 
side  of  the  orbit  ;  sometimes  it  is  very  large  extending  to  a  variable 
extent  over  the  posterior  aspect  of  the  globe  (particularly  in  the  mouse). 
According  to  Miessner  (1900)  it  is  absent  in  the  deer,  among  the  lower 
monkeys  it  is  rudimentary  (Giacomini,  1887),  and  in  the  Anthropoids 
and  man  it  is  represented  only  by  a  transitory  fcetal  structure  in  the 
infero -lateral  fornix  (Loewenthal,  1910).i  The  gland  of  Harder 
secretes  a  sebaceous  (Wendt,  1877)  or  a  mucous  material  (pig,  dog, 
sheep  ;  Virchow,  1910)  which  it  pours  into  the  conjunctival  sac  by 
two  ducts. 

The  extra-ocular  muscles  comprise  four  recti,  two  obliques  and 
(usually)  a  retractor  bulbi  muscle.  The  recti  are  arranged  as  in  man  ; 
the  mammalian  superior  oblique  differs  from  that  of  lower  Vertebrates  in 
the  migration  of  its  origin  to  the  apex  of  the  orbit,  the  reflected  tendon 
being  designed  to  retain  the  original  direction  of  action  (Poole,  1905) 
(Fig,  2!;3).    This  mode  of  development  is  emphasized  in  some  animals 

'  H:;  :■  /;ti's  gland  is  also  absent  in  Cyclostomes,  Fishes  and  aquatic  Amphibians. 


MAMMALS 


495 


(ass)  by  the  presence  of  accessory  muscles  accompanying  the  reflected 
tendon  ;  these  rejj resent  the  direction  of  the  original  muscle,  while  the 
trochlea  is  situated  at  the  origin  of  the  primitive  muscle  from  the 
orbital  wall  (Zimmerl,  1900  ;  Mobilio,  1912).  In  man  similar  super- 
numerary fasciculi  have  been  found  as  an  anomaly,  or  the  more 
primitive  arrangement  has  jjersisted  (Ledouble,  1897).  The  insertions 
of  the  obliques  vary.  In  man  and  the  chimpanzee  the  superior  oblique 
is  crossed  over  by  the  superior  rectus,  while  the  inferior  crosses  the 
inferior  rectus  (Fig.  ()50).  In  the  majority  of  Mammals  both  obliques 
are  crossed  by  the  recti  (Fig.  051)  ;  in  the  tiger  the  recti  pierce  the 
obliques  (Fig.  052),  and  in  the  lion  (as  in  the  tortoise)  the  superior  rectus 

Figs.  650  to  633. — The  Relation  of  the  Oblique  Muscles  to  the  Recti. 


Fig.  650.— 

Fig.  651.— 

Fig.  652.— 

Fig.  653. 

Man  and 

The  majority 

The  tiger. 

The  Hon 

chimjjanzee. 

of  Mammals. 

pierces  the  superior  oblicpie,  and  the  inferior  oblique  pierces  the  inferior 
rectus  (Fig.  053)  (Ottley,  1879  ;    Ovio,  1925). 

A  retractor  bulbi  muscle  {choanoid  muscle,  Motais,  1887)  occurs 
in  most  Mammals;  it  is  particularly  developed  in  Rodents,  Ungulates 
and  Sirenians.  but  is  present  only  in  a  vestigial  form  in  some 
monkeys  [Macacus)  and  is  absent  in  some  of  the  higher  Primates 
(F.  Smith,  1922  ;  Bradley,  1933  ;  Winckler.  1933  ;  Key-Aberg,  1934). i 
The  muscle  arises  from  the  apex  of  the  orbit,  and,  riuuiing  within  the 
muscle-cone,  envelops  the  oj^tic  nerve  and  the  posterior  part  of  the 
globe  to  be  inserted  into  the  sclera  behind  the  recti  (Fig.  054).  The 
insertion  shows  many  variations.  It  may  be  continuous  like  the 
gamopetalous  corolla  of  a  flower,  or  discontinuous  with  the  same 
general  arrangement  but  in  many  separate  bundles  varying  in  indivi- 
duals of  the  same  species  or  even  between  the  two  eyes  of  the  same 
individual,  or  it  may  be  divided  into  diverging  slips  (0  in  the  sloth-bear, 
Melursus  lahiatus  ;  4  in  the  cat  and  dog  ;  2  in  the  whale,  etc.)  (Fig. 
655).  It  is  sujjplied  by  nerve  VI  (Hopkins,  1910),  and  is  usually 
regarded  as  a  derivative  of  the  lateral  rectus  (Johnson,  1901  ;  Corning, 

^  The  muscle  is  also  absent  in  Cyclostomes,  Fishes,  O^jhidians  and  Birds. 


496 


THE   EYE   IN   EVOLUTION 


1900).  Its  action  is  probably  to  pull  back  the  eye,  a  function  eminently 
required  in  Herbivora  which  feed  with  the  head  lowered  and  also  in 
Sirenians  which  graze  at  the  water's  edge  ;  in  man  this  action  is  taken 
over  by  the  tonicity  of  the  recti  themselves  (Grimsdale,  1921).  In  the 
rhinoceros  and  at  least  one  species  of  the  Ursidse  {Melursus  labiatus)  a 
simultaneous  contraction  of  the  retractor  and  lateral  rectus  muscles 
flicks  the  eye  quickly  to  the  temporal  side  and  at  the  same  time  retracts 
it — a  substitute  for  blinking  movements  of  the  lids.  A  similar  move- 
ment is  seen  occurring  about  once  in  eacli  minute  in  the  okapi,  and  as 


M.  rectus 
laleralU 


FiG.     654. — The    Retractor    Bulbi 
Muscle  of  a  Sheep  (Bland-Sutton). 


Fig.  655. — The  Scleral  Insertion 
OF  the  Orbital  Muscles  of  the 
Dog. 

View  from  behind.  1-4,  the  inser- 
tions of  the  4  heads  of  the  retractor 
muscle  which  alternate  with  and  are 
closer  to  the  posterior  pole  than  the 
recti  (after  O.  C.  Bradley). 


the  eye  retracts  the  nictitating  membrane,  well  developed  as  in  most 
Ungulates,  sweeps  across  the  globe  (Briickner,  1950).  As  a  secondary 
action  it  helps  to  thrust  out  the  nictitating  membrane  by  pressure  from 
behind.  Watrous  and  Olmsted  (1941)  reported  that  after  excision  of 
all  the  other  extrinsic  muscles  in  the  dog,  the  retractor  bulbi  was 
eventually  capable  of  moving  the  eyeball  in  all  directions. 

In  the  higher  Primates  the  retractor  muscle  is  vestigial  or  absent.  In 
Macacus,  the  remnant  lies  above  the  lateral  rectus,  and  in  this  region  vestigial 
muscular  fibres  have  been  found  in  man  (Nussbaum,  1893  ;  Ledouble,  1897  ; 
Fleischer,  1907).  Indeed,  according  to  Lewitsky  (1910),  thei'e  is  always  a  well- 
marked  connective  tissue  strand  in  this  position  in  man,  running  from  the  back 
of  the  fascia  bulbi  to  the  apex  of  the  orbit.  Whitnall  (1911)  has  reported  a  case 
wherein  a  well-developed  muscle  of  four  strands  existed  (Fig.  656). 

The  orbital  muscle  of  Miiller  is  found  in  many  Vertebrates 
(An;  '  ihians.  Reptiles,  Birds)  as  a  well-developed  striated  muscle  mass  ; 
in  Mc     iuals  it  retrogresses  and  its  fibres  become  plain.    According  to 


MAMMALS 

Burkard  (1902)  it  is  a  derivative  of  the  maxillary  musculature,  wliich 
enters  the  orbit  tlirough  the  inferior  orbital  fissure  and  compensates 
for  the  deficiencies  of  a  lateral  wall.  It  is  possible  that  in  those 
animals  in  which  it  is  well  developed  it  may  act  as  a  protrudor  muscle 
by  pulling  forwards  the  fascia  occupying  the  fissure  and  thrusting  the 
eye  outwards. 

It  is  curious  that  despite  the  elaborate  provision  of  extra-ocular  muscles 
and  their  comparative  size,  the  ocular  movements  of  most  terrestrial  Vertebrates 
are  restricted. •"■  The  eye  of  the  elej^hant,  for  example,  is  almost  immobile  despite 
the  fact  that  the  size  of  its  extra-ocular  muscles  is  "  stupefying  "  (Soemmerring, 
1818),  corresponding  to  the  size  of  the  animal  rather  than  to  its  eye  which  is 
relatively  small  and  compares  in  bulk  with  that  of  the  ox.- 


497 


Co/mo//  7f/vDou  ofO/f/6//^ 

Of  Muse.  RCTR.  BULBI. 


Iat.  ffiCTu:,  '  ■  ~^^'///f/?Kf 


Fig.  656. — Ax  Abnormal  Retractor  Bulbi  Muscle  in  Man. 

Four  muscular  bundles  run  forwards  towards  the  globe,  each  fusing  with 
a  rectus  before  reaching  it.  One  bundle  is  innervated  by  nerve  VI  (indicated 
in  the  figT.u-e),  and  the  others  by  nerve  III  (Whitnall,  1911). 


We  have  seen  that  among  Ampliibians  the  orbit  oj^ens  freely  into 
the  cavity  of  the  pharynx  ;  and  among  most  of  the  lower  Vertebrates 
the  post ero-lateral  wall  remains  membranous,  opening  into  the  temporal 
fossa,  a  commmiication  wliich  persists  in  the  higher  Mammals  and  man 
as  the  inferior  orbital  fissure,  the  anterior  end  of  which  (in  man)  may 
exceptionally  encroach  upon  the  lateral  wall  to  form  a  "  spheno- 
zygomatic fissure"  (Tanzi,  1892  ;  Duckworth,  1904).  The  completeness 
of  the  orbital  bony  walls  varies  considerably^  owing  to  irregularities  in 
the  constituent  bones  ;  the  frontal  and  sphenoid  are  always  jDresent, 
the  ethmoid  and  the  palatine  usually  do  not  participate,  and  accessory 
ossicles  are  common  (Maggi,  1898).  Among  the  Rodents  the  orbit  is 
always  open,  particularly  so  m  the  rabbit  ;  in  this  animal  the  floor  of 
the  orbit  is  largely  muscular  (Davis,  1929).  In  the  elephant  and  some 
of  the  Artiodactyls  the  orbit  is  also  open  and  is  jiarticularly  so  among 
the  Carnivores,  an  adajDtation  resembling  that  seen  in  lizards  and  snakes 


p.  692  et  seq. 


p.  450. 


S.O.— VOL.  I. 


32 


498  THE   EYE   IN   EVOLUTION 

to  allow  ample  scope  for  a  wide  gape  of  the  jaws.  On  the  other  hand, 
among  many  Ungulates,  particularly  the  horse  and  all  horned  animals, 
the  orbit  is  enclosed  and  heavily  reinforced,  as  if  for  protection 
against  the  severe  injuries  caused  by  horns,  and  also  for  strengthening 
the  skull  for  combat.  Among  the  Prosimians  the  orbit  is  incompletely 
closed,  maintaining  continuity  with  the  temporal  fossa  ;  among  the 
Anthropoidea  it  is  completely  enclosed.  A  lining  periorbita  is  invariably 
present,  associated  with  muscular  elements  (Burkard,  1902  ;  Ashley- 
Montague,  1931).  The  orbits  vary  much  in  position  depending  on 
whether  the  eyes  look  frontally  or  laterally  (Koschel,  1883)  ^  ;  their 
capacity  compared  with  the  size  of  the  globe  also  varies  within  wide 
limits  (pig,  2-2  :  1  ;  sheep,  1-6:1;  horse,  3:1;  ox,  6:1;  man,  4-5  :  1, 
Dexler,  1893).  Even  among  the  Primates  themselves  the  size  of  the 
orbit  varies  only  very  loosely  with  that  of  the  globe,  large  Primates 
having  a  relatively  small  orbital  capacity  (Imai,  1934-36  ;  Schultz, 
1940  ;   Chamberlain,  1954). 

Tke  vascular  systein  is  extremely  variable  throughout  the  verte- 
brate phylum.  In  man,  the  entire  intra-ocular  blood  supply  and  most 
of  the  orbital  blood  supply  is  derived  from  the  internal  carotid  artery  ; 
in  the  lower  Mammals,  the  external  carotid  takes  the  larger  share  and 
sometimes  is  the  sole  source  of  supply.  In  Rodents  such  as  the  rat 
and  the  rabbit  the  arrangements  are  relatively  simple  (Fig.  657).  The 
main  blood  supply  to  the  globe  and  the  orbit  is  derived  from  the  internal 
maxillary  branch  of  the  external  carotid.  The  external  ophthalmic 
divides  into  several  branches  which  supply  the  muscles  and  tissues  of 
the  orbit,  as  well  as  the  long  and  short  ciliaries  wliich  enter  the  globe. 
A  second  artery  of  supply,  the  internal  ophthalmic  artery,  is  small.  It 
is  derived  from  the  circle  of  Willis  and  ultimately  from  the  internal 
carotid  ;  it  runs  tlu-ough  the  optic  foramen  into  the  orbit,  sends  an 
anastomotic  branch  to  the  nasal  long  ciliary  artery  and  enters  the 
optic  nerve  near  the  globe  to  supply  the  retina  as  a  central  retinal 
artery  (Krause,  1868  ;  Henderson,  1903  ;  Davis,  1929  ;  Daniel  et  al., 
1953  ;   Janes  and  Bounds,  1955). 

Among  the  Carnivores,  the  dog  and  cat  may  be  taken  as  typical. 
In  the  dog  the  arrangement  is  not  very  different  from  that  in  the 
rabbit  (Fig.  658).  Again,  the  main  blood  supply  to  the  orbit  and  globe 
is  by  way  of  the  external  oj3hthalmic  branch  of  the  internal  maxillary 
artery  which  is  ultimately  derived  from  the  external  carotid.  In  the 
same  way  an  internal  ophthalmic  artery  derived  from  the  circle  of  Willis 
(that  is,  ultimately  from  the  internal  carotid)  also  enters  the  orbit 
to  anastomose  with  the  ciliary  branch  of  the  external  ophthalmic. 
There  is,  however,  a  large  anastomotic  branch  (the  arteria  anastomotica) 
betv,      L  the  internal  carotid  and  the  external  ophthalmic  arteries,  so 

1  p.  672. 


MAMMALS 


499 


Figs.    657   to   662. — The   Carotid    Circulation   in   Mammals 
(after  Daniel  et  al.,  1953). 


Fig.  657.— The  rabbit. 


k  J<i 


Fig.  660.— Tlie  pig. 


Fig.  661.— The  sheep. 


'I  .k   4 


Fig.  659.— The  cat. 


Fig.  662.— The  ox. 


a,  arteria  aiiastoniotica  ;  h,  anterior  cerebral  artery  ;  c,  ascending  pharyn- 
geal artery  ;  (/,  ciliary  artery  ;  e,  common  carotid  artery  ;  /,  carotid  rete  ; 
g,  circle  of  Willis  ;  h,  external  carotid  artery  ;  i,  external  ethmoidal  artery  ; 
j,  external  ophthalmic  arteiy  ;  k,  frontal  artery  ;  /,  internal  carotid  artery  ; 
//(,  internal  ethmoidal  artery  ;  n,  internal  maxillary  artery  ;  o,  internal 
ophthalmic  artery  ;  p,  lacrimal  artery  ;  q,  middle  cerebral  artery  ;  r,  arteries 
of  extrinsic  ocular  muscles  ;  .s,  posterior  communicating  artery  and  jDroximal 
part  of  posterior  cerebral  artery  ;    t,  ramus  anastomoticus. 

large  that  the  intra-ocular  circulation  can  be  maintained  unimpaired 
either  by  the  external  or  internal  ophthalmic  arteries  (Ellenberger  and 
Baum,  1891  ;  Henderson,  1903  ;  Parsons,  1903  ;  Jewell,  1952  ; 
Daniel  et  al.,  1953).  It  is  interesting  that  in  association  with  this 
anastomotic  vessel  there  is  a  relatively  simple  arterial  network  (the 


500  THE   EYE   IN   EVOLUTION 

rete   of  Hiirlimann,   1912)   situated   intracranially   in    the  cavernous 
sinus. 

In  the  cat  the  circulation  is  unique  in  that  the  internal  carotid  in 
the  adult  is  vestigial,  being  reduced  to  imperforate  connective  tissue 
strands  (Fig.  659).  The  external  carotid,  on  the  other  band,  is  well 
developed  and  its  large  internal  maxillary  branch  provides  the  basis 
of  an  elaborate  anastomotic  network  (the  carotid  rete)  which  is  situated 
extracranially  near  the  apex  of  the  orbit.  From  this  rete  large  anasto- 
motic vessels  supply  the  circle  of  Wilhs  by  way  of  the  orbital  fissure. 
Also  from  this  rete  seven  independent  trunks  (corresponding  to  the 
ophthalmic  circulation  of  human  anatomy)  supply  the  orbital  tissues 
and  the  globe.  The  largest  branch  of  the  internal  maxillary ^ — the 
ciliary  artery — reaches  the  optic  nerve  where  it  breaks  up  into  its 
numerous  terminal  ciliary  branches  which  enter  the  eyeball  ;  there  is 
no  central  artery  of  the  retina  (Tandler,  1899-1906  ;  Hiirlimann, 
1912  ;  Daniel  et  al.,  1953  ;  etc.).  Davis  and  Story  (1943)  found  that 
from  the  circle  of  Willis  a  tenuous  ophthalmic  artery  sometimes  entered 
the  orbit  to  anastomose  with  the  ciliary  artery  ;  but  even  when  it 
occurs  it  is  small  and  incidental.  The  whole  of  the  orbit  and  eye  is 
therefore  supplied  from  the  external  carotid  as  well  as  the  greater  part 
of  the  circulation  of  the  brain. 

Among  Ungulates,  in  the  pig  the  circulation  resembles  that  of  the 
dog,  but  a  well-formed  rete  is  present  supplied  proximally  by  the 
ascending  pharyngeal  artery;  it  empties  into  a  large  trunk  which 
is  the  only  persistent  portion  of  the  internal  carotid  artery  and  con- 
tributes to  the  circle  of  Willis  (Fig.  660).  Arising  from  this  last  vessel 
there  is  a  tenuous  internal  ophthalmic  artery  which  anastomoses  with 
the  ciliary  (Versari,  1900  ;  Daniel  et  al.,  1953).  In  the  sheep,  goat,  ox 
and  horse,  the  external  ophthalmic  artery  may  arise  directly  from  the 
internal  maxillary,  as  it  does  in  the  dog,  or  from  one  of  the  group  of 
vessels  which  form  anastomotic  channels  tlu"Ough  the  carotid  rete  with 
the  circle  of  Willis.  As  in  the  dog,  a  tenuous  internal  ophthalmic 
artery  is  present  in  the  sheep  and  the  goat  but  not  in  the  ox.  In  the 
sheep  and  goat  the  rete  is  supplied  wholly  from  the  external  carotid 
and,  as  occurs  in  the  pig,  the  internal  carotid  only  exists  as  an  afferent 
vessel  from  this  arterial  network  to  the  circle  of  Willis.  In  the  ox  and 
horse,  however,  an  internal  carotid  vessel  is  present  (Figs.  661-2) 
(Zietzschmann,  1913  ;   Daniel  et  al.,  1953). 

The  orbital  veins  have  not  been  fully  worked  out  but  in  a  general 
way  they  correspond  with  the  arterial  supply.  In  man,  the  greater 
part  of  the  venous  system  returns  into  the  intracranial  system  ;  in  the 
lower  Mammals  the  return  is  more  and  more  to  the  extracranial  system. 
In  the  rabbit  the  veins  from  the  globe  and  orbit  empty  into  an  extensive 
ORBIT        SINUS   which  ramifies   throughout   the   apex   of  the   orbit, 


MAMMALS  501 

enveloping  the  muscles  and  extending  forwards  to  the  level  of  the 
equator  of  the  globe  :  its  main  exit  channels  are  into  the  posterior  and 
deep  facial  veins,  the  external  and  internal  maxillary  veins,  and  the 
vertebral  vein  (Davis,  1929). 

The  orbital  nerves  throughout  the  Placentals  conform  to  the  same 
general  plan.  The  branches  of  the  first  division  of  the  trigeminal  serve 
as  the  sensory  supply  ;  the  sympathetic  is  vasomotor  and  innervates 
the  smooth  orbital  muscle  ;  while  the  muscles  are  supplied  by  the 
Ilird,  IVth  and  Vlth  cranial  nerves  as  in  man  except  that  the  last 
nerve  supplies  the  retractor  bulbi  muscle  and  the  muscles  controlling 
the  nictitating  membrane  when  these  are  j) resent. 

The  CILIARY  (orbital)  ganglion  is  of  interest.  It  is  variable  in  nature 
but  is  always  primarily  associated  with  the  Ilird  nerve.  In  the  lower  Fishes 
(Selachians,  etc.)  it  is  represented  by  groups  of  cells  scattered  along  this  nerve 
(H.  Schneider,  1881  ;  Pitzorno,  1913)  ;  in  Teleosteans,  Amphibians  and 
Reptiles  the  ganglion  becomes  a  specific  entity  associated  with  this  nerve,  usually 
without  connection  with  the  Vth  or  synijDathetic  (Schwalbe,  1879).  In  Birds 
it  has  a  short  root  from  the  Ilird  nerve  and  a  slender  long  root  from  the  trigeminal 
(Lenhossek,  1911  ;  Carpenter,  1911).  Langendorff  (1900)  and  Lodato  (1900) 
were  unable  to  confirm  the  nicotine  reaction  for  the  motor  fibres  in  Birds  ;  it 
thus  appears  that  physiologically  as  well  as  anatomically  the  cells  in  these 
animals  are  cerebro-sjainal  in  type.  It  will  be  remembered  that  the  ciliary 
muscle  of  Birds  is  striated.  In  Mammals,  although  it  is  small  in  Equidse  (Mobilio, 
1912),  the  ciliary  ganglion  is  always  present,  and  in  them  the  connection  with 
the  Ilird  nerve  is  always  retained  (Schwalbe,  1879.;  Peschel,  1893  ;  Apolant, 
1896).  In  many  of  them  the  root  from  the  Vth  nerve  is  absent,  and  frequently, 
when  it  is  present,  it  conducts  fibres  of  passage  which  are  not  relayed  (Antonelli, 
1890  ;  Michel,  1894).  The  sympathetic  root  is  more  frequently  absent  ;  and 
both  of  these  roots  may  be  absent  in  man.  Among  Mammals  the  ciliary  ganglion 
is  often  rejaresented  by  more  than,  one  group  of  cells. ^  It  is  probable  that  in 
many  cases  some  of  these  different  colonies  of  cells  represent  outgrowths  of 
III  and  others  outgrowths  of  V.  When  the  ganglion  is  painted  with  nicotine 
the  motor  path  is  blocked,  showing  that  this  is  mediated  by  cell-stations  of  the 
autonomic  type  (Langley  and  Anderson,  1892),  while  the  sensitivity  of  the 
cornea  remains  unimi^aired,  showing  that  the  sensory  fibres  are  relayed  in  cell- 
stations  which  (if  present)  are  of  the  cerebro -spinal  type. 

The  ocular  adnexa  of  aquatic  Placentals  deserve  a  sjjecial  note. 
Some  are  only  partially  adapted  to  this  medium.  In  the  liippopotamus 
the  orbits  (like  the  nose)  are  elevated  so  that  the  eyes  are  readily  kept 
above  the  water-level,  the  lids  form  a  ring  rather  than  a  slit-shaped 
palpebral  aperture,  the  lashes  are  sparse,  and  naso -lacrimal  canals  are 
lacking.  In  the  Pinnipedes  (seals  and  walruses)  the  orbits  are  also 
directed  somewhat  ujd wards,  there  are  no  tarsal  glands,  the  lacrimal 
glands  (although  large  in  the  foetus)  are  small  in  the  adult  and  the 
harderian  glands  are  enormously  developed,  secreting  an  abundance  of 

1  Ox,  Muck  (1815)  ;  rabbit,  d'Erchia  (1895),  Mobilio  (1912)  ;   pig,  Antonelli  (1890). 


502 


THE   EYE   IN  EVOLUTION 


an  oily  substance  to  protect  the  keratinized  cornea  against  the  sea-water  ; 
in  the  absence  of  naso -lacrimal  canals,  this  secretion  j^ours  copiously 
over  the  face  when  the  animal  is  on  land  (Fig.  663).  In  Sirenians 
(sea-cows)  the  lashes  are  extremely  scanty  but  the  lids  freely  mobile, 
closing  completely  over  the  small  eye  when  it  is  pulled  backwards  by 
the  well-developed  retractor  muscle.  There  is  no  lacrimal  gland  but 
the  harderian  gland  is  well  developed,  as  in  Pinnipedes,  secreting  a 
copious  thick  mucoid  secretion  like  egg-white  (Fig.  664). 

The  Cetaceans  (whales  and  dolphins)  are  completely  adapted  to 
aquatic  life  :   the  lids  are  small,  without  tarsal  plates  or  tarsal  glands  ; 


Figs.  663  and  664. — Aquatic  Placental^. 


Phoca 


Showing  the  upwardly  directed  eyes, 
as  an  adajDtatioii  for  swimming  (Zool. 
Soc,  London). 


Fig.   664.— The    Head    of    the    Manatee, 
Trichechus  manatus. 

Showing    the    small     retractable     eyes 
(photograph  by  Michael  Soley). 


lashes  are  lacking  ;  a  "  lacrimal  "  gland  is  present  but  secretes  not 
tears  but  a  fatty  water-repellant  secretion,  and  the  same  hypertrophy 
of  the  harderian  gland  is  seen,  the  oily  secretion  of  which  is  augmented 
by  that  of  numerous  oil-glands  distributed  over  the  palj)ebral  conjunc- 
tiva. The  naso-lacrimal  conducting  mechanism  is  absent  as  also  is 
the  nictitating  membrane.  The  extra-ocular  muscles  are,  however, 
enormous,  more  in  keeping  with  the  size  of  the  animal  than  that 
of  the  small  eye  ;  each  rectus  is  comparable  to  the  biceps  of  man. 
In  the  whale  this  seems  curious  in  view  of  the  immobility  of  the 
downward-looking  eye  fixed  firmly  on  its  immensely  rigid  accessory 
optic  nervo  sheath  and  situated  low  down  on  a  level  with  the 
angk-  ''  the  mouth  about  one-third  of  the  length  of  the  huge  animal 
away  :      a  its  anterior  extremity.    It  has  been  said  that  the  enormous 


MAMMALS 


503 


muscles  might  be  of  value  in  keeping  the  eye  warm  by  their  tonic 
contraction  in  deep  diving  into  the  icy-cold  ocean  depths  since  here 
the  thick  layer  of  oily  fat  which  insulates  the  rest  of  the  body  is  absent  ; 
but  such  a  function  is  questionable.  It  would  seem  rather  that,  as  in 
the  elephant,  the  muscles  have  retained  a  size  compatible  with  that 
of  the  animal  while  the  globe  has  not. 

For  monographs  on  the  study  of  the  eyes  of  particular  species,  see  : 
Rodents — rabbit,     Davis     (1929)  ;      chinchilla,    Detwiler    (1949)  ;      mouse, 

Schwarz  (1935)  ; 
Ungulates — okapi,  Bruckner  (1950)  ; 
Carnivores — dog,  Ai-ey  et  al.  (1942)  ; 
Primates — Nycticebus,  Nyctipithecus,  Detwiler  (1939-41);  apes,  Hotta  (1906). 


Aeby.     v.  Graefes  Arch.  Ophthal.,   28   (1), 

111  (1882). 
Agababow.    v.  Graefes  Arch.  Ophthal.,  83, 

317  (1912). 
Albers.     Denkschr.  d.  Kgl.  Akad.  d.  Wiss., 

Miinchen  (1808). 
Amsler.    Arch.  e.vp.  Path.,  103,  138  (1924). 
Anelli.     Boll.  Oculist.,  14,  499  (1935). 

Ric.  Morfol.,  15,  233  (1936). 
Angelucci.      Arch,    niikr.    Anat.,    19,    152 

(1881). 
Antonelli.    Arch.  ital.  Biol.,  14,  132  (1890). 
Apolant.       Arch.    mikr.    Anat.,    47,    655 

(1896). 
Arden    and    Tansley.      J.    Physiol.,    127, 

592  ;    130,  225  (1955). 
Arey,  Bruesch  and  Castanares.     J.  comp. 

Neurol,  76,  417  (1942). 
Asayama.     v.  Graefes  Arch.  Ophthal.,    43, 

113  (1901). 
Ashley- Montague.       J.     Ayiat.,     65,     446 

(1931). 
Nature  (Lond.),  152,  573  (1943). 
Amer.  Anthropol.,  46,  141  (1944). 
Attias.    V.  Graefes  Arch.  Ophthal.,  83,  207 

(1912). 
Aurell     and     Kornerup.       Acta     Ophthal. 

(Kbh.),  27,  19  (1949). 
Barrett.    J.  Physiol.,  7,  230  (1886). 
Bayer.     Bildliche  Darstellung.  d.  gesunden 

u.   kranken  Auges  unserer  Haustiere, 

Wien  (1892). 
Bayer  and  Frohner.    Hb.  d.  tierdrztl.  Chir. 

u.  Geburts.,  Wien  (1900). 
Beauvieux    and    Dupas.       Arch.    Ophtal. 

(Paris),  43,  641  (1926). 
de  Beer  and  Fell.     Trans,  zool.  Soc.  Lond., 

23,  1  (1936). 
Bell,  Kirby  and  Rodger.    .7.  Physiol.,  117, 

56P  (1952). 
Bellonci.     Arch.  ital.  Biol.,  6,  405  (1884). 
Bennett.      Proc.   zool.  Soc.   Lond.,   Pt.   4, 

127  (1836). 
Bielschowsky  and  Pollak.     Neurol.   Zbl., 

23,  387  (1904). 


Binder     and     Binder.        Arch.     Ophthal. 

(Chicago),  56,  10  (1956). 
Blumenbach.     Hb.  d.   vergl.  Anat.,  Gott- 

ingen  (1805). 
Bochdalek.     Ber.  Versamml.  dtsch.  Natur- 

forsch.  Arzte,  Prag.,  182  (1837). 
Med.  Jb.   oesterr.  Staates,  29,   185,   398 

(1839). 
Boeke.      Z.    mikr. -anat.    Forsch.,   33,    233 

(1933)  ;   38,  594  (1935). 
Boeke  and  Heringa.     K.  Akad.  Wetensch. 

Amst.,  Proc.  Sec.  Sci.,  27,  24  (1924). 
Bonfanti.        Ateneo     Parmense,     20,     46 

(1949). 
Borri.     Z.  Zellforsch.  mikr.  Anat.,  29,  128 

(1939). 
Borysiekiewicz.    Untersuch.  il.  d.  feineren 

Ban  d.  Nelzhaut,  Leipzig  (1887). 
Bossalino.     Ann.  Ottal.,  38,  835  (1909). 
Bradley.    J.  Anat.,  68,  65  (1933). 
Brauwer  and  Zeeman.    J.  Neurol.  Psycho- 
path., 6,  1  (1925). 
Bromami     and     Ask.       Dtsch.    Siidpolar- 

E.vped.,  (1901-3),  12  (1910). 
Bruch.     Z.  wiss.  Zool.,  4,  282  (1853). 
Briicke.    Arch.  Anat.  Physiol.,  387  (1845). 
Bruckner.        Ophthalmologica,     118,      969 

(1949). 
Acta  trop.,  7,  123  (1950). 
Bruesch  and  Arey.     J.  comp.  Neurol.,  77, 

631  (1942). 
Bruni.    Ann.  Ottal.,  50,  469  (1922). 
Bruns.     Z.  vergl.  Augenheilk.,  1,  77  (1882). 
Burkard.     Arch.  Anat.   Physiol.,  Erg.   79 

(1902). 
Cajal.        Die     Retina     der      Wirbelthiere, 

Wiesbaden  (1894). 
Rev.  trim.  Micros.,  Madrid,  3,  141  (1898). 
Histol.  du  systeme  yierveux  de  Vhomnie  et 

des  vertebres,  Paris,  1,  460  (1909). 
Calmettes,  Deodati,  Planel  and  Bee.  Arch. 

Ophtal.  (Paris),  16,  481  (1956). 
Caprino.      Boll.  Soc.    ital.    Biol,   sper.,  31, 

1445  (1955). 
Carpenter.       Folia     Neuro-hiol.,     5,     738 

(1911). 


504 


THE   EYE   IN   EVOLUTION 


ten  Gate.     Arch,  nierl.  Physiol.,  19,  408, 

417  (1934). 
Chamberlain.     Trans.  Amer.  ophthal.  Soc, 

52,  751  (1954). 
Chievitz.      Arch.    Anat.    Physiol.,    Suppl. 
139  (1889)  ;    Anat.  Abt.,  332  (1890)  ; 
311  (1891). 
Ciaccio.    Quart.  J.  micr.  Sci.,  3,  77  (1863). 

Mem.  Acad.  med.  Oenova,  2,  577  (1881). 
Clark,  Le  Gros.   J.  Anat.,  75,  225,  419  ; 
76,  131  (1941)  ;   76,  369  (1942). 
Trans,  ophthal.  Soc.  U.K. ,62,  229  (1942). 
Cohnheim.    Zbl.  med.  Wiss.,  4,  401  (1866). 
Arch.    path.    Anat.    Physiol.,    38,    343 
(1867). 
Collins.       IX     Internat.    Cong.     Ophthal., 
Utrecht,  88  (1899). 
Trans,  ophthal.  Soc.  U.K.,  41,  10  (1921). 
Corning.     Morphol.  Jb.,  29,  94  (1900). 
Crevatin.    Anat.  Anz.,  23,  151  (1903). 
Damel  and  Fortin.     Arch.  Oftal.  B.  Aires, 

12,  762  (1937). 
Daniel,    Dawes    and    Prichard.       Philos. 

Trans.  B,  237,  173  (1953). 
Davis,   D.,   and    Story.      Field  Mus.   nat. 
Hist.,  Zool.  Ser.,  Chicago,  28,  5  (1943). 
Davis,  F.     Trans.  Amer.  ophthal.  Soc,  27, 

401  (1929). 
Detwiler.      J.     camp.     Neurol.,    37,     481 
(1924)  ;    55,  473  (1932). 
Anat.    Rec,   74,    129    (1939)  ;     76,   295 

(1940)  ;    80,  233  (1941). 
Vertebrate  Photoreceptors,  N.Y.  (1943). 
J.  Morphol.,  84,  123  (1949). 
Dexler.       Z.    vergl.    Augenheilk.,    7,     147 
(1893). 
Wien.  klin.  Wschr.,  10,  222  (1897). 
Deyl.    Anat.  Anz.,  11,  8  (1895). 

Bull,  internat.  Acad.  Sci.,  Prague,   120 
(1895). 
Dogiel.    Anat.  Anz.,  3,  133  (1888)  ;   5,  483 
(1890). 
Arch,  milcr.  Anat.,  37,  602  (1891). 
Dostoiewsky.     Arch.  mikr.  Anat.,  28,  91 

(1886). 
Duckworth.       Morphol.    and    Anthropol., 

Cambridge  (1904). 
Egorow.     V.  Graejes  Arch.    Ophthal.,   131, 

531  (1934). 
EUenberger  and  Baum.    Anat.  d.  Hundes, 

Berlin  (1891). 
Emmert.      Z.    vergl.    Augenheilk.,    4,    40 

(1886). 
d'Erchia.    Monit.  zool.  Ital.,  5,  235  (1894)  ; 

6,  157  (1895). 
Eversbusch.     Z.  vergl.  Augenheilk.,  3,  33 

(1885). 
Fey.    Arch,  vergl.  Ophthal.,  4,  182  (1914). 
Fincham.     Trans,  opt.  Soc,  30,  101  (1929). 
Fleischer.    Anat.  Anz.,  30,  465  (1907). 
Flemming.      Arch.    mikr.    Anat.,    4,    353 

(5  868). 
Fontan,;,     Traite  sur  le  venin  de  la  vipere, 
etc.,      orence,  2  (1781). 


Franz.    Arch,  vergl.  Ophthal,  2,  180  (1912). 
Bolk's  Hb.   vergl.   Anat.   d.    Wirbeltiere, 
Berlin,  2  (ii),  1200  (1934). 
Fritsch.     Z.  wiss.  Zool,  98,  288  (1911). 
Fukamachi.     Acta  Soc.  ophthal.  jap.,  57, 

408  (1953). 
Gerard  and  Rochon-Duvigneaud.      Arch. 

Biol.  (Li6ge),  40,  151  (1930). 
Gerlach.       Hb.     allg.     spec.     Qewebelehre, 

Mainz  (1848). 
Giacomini.    O.  Acad.  Med.,  Torino  (1887). 
Greaves  and  Perkins.     Brit.  J.  Ophthal., 

35,  119  (1951). 
Greeff.     Oraefe-Saemisch  Hb.  ges.   Augen- 
heilk., II,  1,  Kap.  5  (1900). 
Gresser  and  Noback.    J.  Morphol.,  58,  279 

(1935). 
Grimsdale.     Trans,  ophthal.  Soc.  U.K.,  41, 

357  (1921). 
Groyer.    S.  B.  Akad.  Wiss.  Wien,  112,  51 

(1903). 
Gudden.    v.  Graejes  Arch.  Ophthal.,  25,  1 

(1879). 
Guist.     Z.  Augenheilk.,  50,  195  (1923). 
Gunn.    J.  Anat.  Physiol.,  18,  400  (1884). 
Hannover.     Das  Auge,  Leijjzig  (1852). 
Harder.     Acta  erudit.  pub.  Lipsiae  (1694). 
Harris.     Brain,  27,  107  (1904). 
Henderson.      Roy.    Lond.    ophthal.    Hosp. 
Rep.,  15,  260  (1903). 
Trans,  ophthal.  Soc.  U.K.,  28,  47  (1908)  ; 

41,  465  (1921)  ;   46,  280  (1926). 
Principles    of    Ophthalmology,    London 
(1950). 
Hertel.    v.  Graejes  Arch.  Ophthal.,  65,  106 

(1907). 
Hess.    Arch,  vergl.  Ophthal.,  2,  3  (1912). 
Winterstein's  Hb.  vergl.  Physiol.,  Jena, 
555  (1913). 
Hines.    Philos.  Trans.  B,  217,  155   (1929). 
His.    Arch.  Anat.  Physiol.,  Anat.  Abt.,  224 

(1880). 
Hopkins.     Anat.  Rec,  11,  199  (1916). 
Hotta.    V.  Graejes  Arch.  Ophthal.,  62,  253 

(1906). 
Hovius.      De  circulari  humorum  motu  in 

oculis  (1716). 
Hueck.     Bewegung  d.  Krystallinse,  Dorpat 

(1839). 
Hiirlimann.     Internat.   Mschr.  Anat.,  29, 

371  (1912). 
Ikeda.      Folia  Anat.  jap.,  Tokyo,  25,  163 

(1953). 
Imai.    J.  med.  Assoc.  Formosa,  33,  1,  23, 
27  (1934)  ;    34,  155  (1935)  ;    35,  310 
(1936). 
Itahashi.     Acta  Soc.  ophthal.  jap.,  56,  42 

(1952). 
Iwanoff  and   Rollett.      v.    Graejes    Arch. 

Ophthal.,  15,  17  (1869). 
Janes  and  Bounds.      Ajner.  J.  Anat.,  96, 

357  (1955). 
Jewell.    J.  A7iat.,  86,  83  (1952). 
Johnson.    Philos.  Trans.  B,  194,  1  (1901). 


MAMMALS 


505 


Kahmann.     Zool.  Jb.,  Aht.  Zool.  Physiol., 

48,  509  (1930)  ;    52,  295  (1932). 
Kappers.      Vergl.  Anat.  d.  Nervensy stems, 

Haarlem,  2  (1921). 
Karli.     C.  R.  Soc.  Biol.  (Paris),  145,  1376 

(1951). 
Kelemen.      J.     Laryngol.    Otol.,    64,     131 

(1950). 
Kesteven  and  Furst.    J.  Anat.  (Lond.),  63, 

447  (1929). 
Key-Aberg.     Sven.  Ldk.  Sdllsk.  Hdl.,  60, 

117  (1934). 
Kieser.     Ophthal.  Bibl.,  2,  3,  73  (1803). 

De  anamorphosi  oculi,  Gottingen  (1804). 
Kiss.     Ophthalmologica,  106,  225  (1942). 

Szemeszet  (Budapest),  86,  1  (1949). 
Kolliker.     Mitt.  d.  naturf.  Ges.  Zurich,  1, 

89  (1848). 
Wiirzburg.  naturwiss.  Z.,  6,  121  (1866). 
Kolmer.      Z.  wiss.   Zool.,   97,   91    (1910)  ; 

125,  448  (1925). 
Anat.    Anz.,    40,    626    (1912)  ;     67,    156 

(1929). 
Z.  Anat.  Entwick.,  73,  645  (1924)  ;    93, 

679  (1930). 
Kolmer  and  Lauber.     Hb.  d.  mikr.  Ayiat. 

d.  Menschen,  Berlin,  3  (2),  411  (1936). 
Koschel.       Z.    vergl.    Augenheilk.,    2,    53 

(1883). 
Krause,  W.    Anat.  des  Kanichens,  Leipzig 

(1868-95). 
Internat.  Mschr.  Anat.,  12,  96  (1895). 
Kurus.     Kliti.  Mbl.  Augeyiheilk.,  127,  198 

(1955). 
Lange.     Arch.  wiss.  prakt.   Tierheilk.,  27, 

127  (1901). 
Langendorff.     Klin.  Mbl.  Augenheilk.,  38, 

307  (1900). 
Langley  and  Anderson.     J.   Physiol.,  13, 

460  (1892). 
Lauber.     Anat.  Hefte,  18,  371  (1901). 
Graefe-Saemisch    Hb.    ges.    Angeyiheilk., 

Leipzig,  II,  1  (2).  Kap.  3  (1931). 
Law.     Ophthal.  Rec.,  14,  431  (1905). 
Leber.    Graefe-Saemisch  Hb.  d.  ges.  Augen- 
heilk., II,  2,  19  (1903). 
Ledouble.     Traite  d.  variations  du  systeme 

niusculaire,  Paris,  1  (1897). 
Lenhossek.      Anat.    Anz.,    37,    Erg.,    137 

(1910)  ;   40,  74  (1911). 
Arch.  mikr.  Anat.,  76,  745  (1911). 
Leuckart.  Graefe-Saemisch     Hb.     ges. 

Augenheilk.,  I,  2,  171  (1876). 
Levinsohn.     Z.  Augenheilk.,  8,  518  (1902). 
Lewitsky.  Die  Anat.  u.  Path.  d.  Tenon'sche 

Kapsel,  Odessa  (1910). 
Lichal.    Anat.  Anz.,  48,  296,  341  (1915). 
Liebig.    Arch.  Anat.  Physiol.,  96  (1874). 
Linsenmeyer.     Arch,  vergl.  Ophthal.,  2,  37 

(1912). 
Lodato.     Arch.  Ottal.,  8,  165  {1900). 
Loewenthal.     Bib.  Anat.,  19,  301  (1910). 

Bull.  Histol.  appL,  8,  168  (1931). 
Lor.     J.    Anat.    Physiol.,    Paris,    34,    463 

(1898). 


Luschka.     Z.  rat.  Med.,  10,  20  (1850). 
Maggi.     Rend.  R.  1st.  Lombardo  Sci.  Lett., 

29  (1898). 
Maggiore.    Ann.  Ottal.,  45,  317  (1917). 
Mann.      Trans,  zool.  Soc.   Lond.,  21,   355 

(1931). 
Manz.     Z.  rat.  Med.,  5,  122  (1859). 
Matthiessen.     Z.  vergl.  Augenheilk.,  7,  77 

(1893). 
Meinertz.     Morphol.  Jb.,  69,   110  (1932)  ; 

75,   15  ;    76,   1    (1935)  ;    77,   124,  400 

(1936)  ;    87,  254  (1942). 
Merker.     Zool.  Jb.,  Abt.  Zool.  Physiol.,  45, 

535  (1928). 
Michaelson.    J.  Ayiat.,  82,  167  (1948). 
Retinal  Circulation  in  Man  and  Animals, 

Springfield,  111.  (1954). 
Michel.    V.  Graefes  Arch.  Ophthal.,  27  (2), 

171  (1881). 
VIII    Internat.    Cong.    Ophthal.,    Edin., 

195  (1894). 
Miessner.     Arch.  wiss.  ]}rakt.   Tierhk.,  26, 

122  (1900). 
Miimi.     Acta  Soc.   ophthcd.  Jap.,  39,   803 

(1935). 
Mobilio.    Monit.  Zool.  Ital.,  23,  80  (1912). 
Arch.  Sci.   R.  Soc.  Nat.    Veter.,   10,   97 

(1912). 
Anat.  Anz.,  44,  113  (1913). 
Moffat.    Nature  (Lond.),  169,  1015  (1952). 
Monesi.    Ann.  Ottal..  35,  868  (1906). 
Morano.     Arch.  Ottal.,  2,  73  (1873). 
Motais.     Anat.  appareil  moteur  de  Voeil  de 

Vhomme  et  des  vertebres,  Paris  (1887). 
Muck.      De,  ganglia   ophthalmico   et   nervis 

ciliaribus       animcdium,       Landishuti 

(1815). 
Muller,  H.     Z.  wiss.  Zool.,  8,  1  (1856). 

Wiirzburg.  naturwiss.  Z.,  2,  64  (1861). 
Muller,  J.     Vergl.  Physiol,  d.  Gesichtssinnes, 

Leipzig  (1826). 
Murr.      Z.   Zellforsch.  mikr.  Anat.,  2,   703 

(1925)  ;    6,  315  (1927). 
Murray.       Nova     acta     regice     Soc.     Sci. 

Upsaliensis,  3,  41  (1780). 
Naglieri.     Monit.  zool.  Ital.,  43,  17  (1932). 
Nakajima.    Keijo  J.  Med.,  1,  99  (1930). 
Newell.      Trans.  Amer.  ophthal.  Soc,  51, 

501  (1953). 
Newton.       Treatise    on    Opticks,    London 

(1704). 
Nicati.     C.  R.  Acad.  Sci.  (Paris),  86,  1472 

(1878). 
Nordmann.      Tabulae    Biol.,    22    (1),    298 

(1947). 
Nuel  and  Benoit.     Arch.  Ophtal.   (Paris), 

20,  161  (1900). 
Nussbaum.     Anat.  Anz.,  8,  208  (1893). 
O'Day.    J.  Anat.,  70,  4.55  (1936). 
Brit.  J.  Ophthal.,  22,  321  (1938). 
Med.  J.  Australia,  1,  326  (1938). 
Trans,    ophthal.    Soc.    Australia,    1,    12 

(1939)  ;    12,  95  (1952). 
Nature  (Lond.),  160,  648  (1947). 
Ottley.    Proc.  zool.  Soc.  Land.,  121  (1879). 


506 


THE   EYE   IN  EVOLUTION 


Overbosch.     Diss.,  Amsterdam  (1926). 
Ovio.      Anat.    e  fisiol.    delVocchio,    Milan 

(1925). 
Owen.     Anat.  and  Physiol,  of  Vertebrates, 

London,  2  (1868). 
Packer.    J.  Anat.,  75,  309  (1941). 
Palumbi.     Ric.  Morfol.,  £3,  201  (1953). 
Pappenheim.      Mschr.    Med.    Augenheilk. 

Ghir.,  2,  281  (1839)  ;   3,  84  (1840). 
Parry.     Brit.  J.  Ophthal.,  37,  385  (1953). 
Parsons.        Octdar     Circulation,     London 

(1903). 
Peris.    Arch.  esp.  Morfol.,  5,  475  (1947). 
Arch.    Soc.    oftal.     hisp.-amer.,    9,    237 

(1949). 
Peschel.   v.  Graefes  Arch.  Ophthal.,  39  (2), 

1  (1893). 
Pick    and    Herrenheiser.      Nova    Acta    d. 

Kal.    Leap. -Carol.     Dtsch.    Akad.    d. 

Naturforsch.,  66  (1895). 
Pines  and  Pinsky.     Anat.  Anz.,  75,    160 

(1932). 
Pitzorno.     Arch.  ital.  Anat.  Embriol.,  11, 

527  (1913). 
Polyak.    Vertebrate  Visual  System,  Chicago 

(1957). 
Poole.     J.  Anat.  Physiol,  39,  154  (1905). 
Purkinje.    Arch.  A7iat.  Physiol,  wiss.  Med., 

281  (1845). 
Putter.      Zool.    Jb.,    Abt.    Anat.,    17,    99 

(1903). 
Qraefe-Saemisch  Hb.  d.  ges.  Augenheilk., 

Leipzig,  III,  1,  Kap.  10  (1912). 
Rabl.     Z.  wiss.  Zool.,  67,  1  (1899). 
Ranvier.     Cornee.     In  Legons  d'anat.  gen. 
faites  au  College  de  France  (1878-79), 

Paris  (1881). 
Raselli.  v.  Graefes  Arch.  Ojyhthal.,  Ill,  309 

(1923). 
Reiser.       Arch.     Augenheilk.,     109,     251 

(1935)  ;    110,  253  (1936-7). 
Rexed  and  Rexed.     Brit.  J.  Ophthal.,  35, 

89  (1951). 
Richiardi.     Atti   R.   Acad.   Lincei,   1   (3), 

193  (1877). 
Richter.  v.  Graefes  Arch.  Ophthal.,  70,  407 

(1909). 
Arch,  vergl.  Ophthal.,  2,  327  (1911). 
Rickenbacher.     Acta  anat.  (Basel),  18,  48 

(1953). 
de  Robertis.     J.  biophys.  biocheni.  Cytol., 

2,  319  (1956). 
de    Robertis    and    Franchi.      J.    biophys. 

biochem.  Cytol.,  2,  307  (1956). 
Rochat  and  Benjamins,     v.  Graefes  Arch. 

Ophthal.,  91,  66  (1916). 
Rochon-Duvigneaud.  Arch.  Ophtal.  (Paris), 

12,  732  (1892)  ;    13,  20  (1893). 
XIII  Internal.  Cong.  Ophthal.,  Amster- 
dam, 1,  319  (1929). 
Ann.  Oculist.  (Paris),  170,  1  (1933). 
I.  "^  yeux  et  la  vision  des  vertebres,  Paris 

V    ^  "^). 
Rodger         rit.  J.  Ophthal,  33,  107  (1950). 


Rohen.     Ber.  ophthal  Ges.  Heidel,  57,  65 

(1951)  ;    58,  65  (1953). 

Morphol   Jb.,   91,    140  (1951);  92,  441 

(1952)  ;    93,  42  (1953). 

V.  Graefes  Arch.  Ophthal,  156,  90  (1954); 

157,  361  (1956)  ;    158,  310  (1957). 
Ophthalmologica,  128,  305  (1954)  ;    133, 

103  (1957). 
Rohen   and    Schrader.     v.    Graefes   Arch. 

Ophthal,  155,  213  (1954). 
Sardemann.     Zool  Anz.,  7,  569  (1884). 
Sattler.    v.  Graefes  Arch.  Ophthal,  22  (2), 

1  (1876). 
Schiefferdecker.      Arch.   mikr.   Anat.,   28, 

305  (1886). 
Schleich.       Graefe-Saemisch    Hb.    d.    ges. 

Augenheilk.,  II,  10b,  Kap.  21  (1922). 
Schlemm.    v.  Amnions  Z.  Ophthal,  1  (1), 

113  (1831). 
Schmerl.      Anier.    J.    Ophthal,    30,     187 

(1947). 
Schneider,    H.    Jena.    Z.   Naturwiss.,    15, 

215  (1881). 
Schneider,  K.  M.     Neue  psychol  Studien, 

6,  317  (1930). 
Schultz.    Amer.  J.  physiol  Anthropol,  26, 

389  (1940). 
Schultze,  M.     Arch.   mikr.  Anal,   2,    175 

(1866)  ;    7,  244  (1871). 
Schultze,    O.       Zur    Entwicklungsges.    d. 

Gefdsssy stems  im  Sdugetierauge,  Wiirz- 

burg  (1892). 
Schwalbe.    Jena.   Z.   Naturwiss.,   13,    173 

(1879). 
Schwarz.     Jena.    Z.   Naturwiss.,   70,    113 

(1935). 
Z.  Zellforsch.,  36,  45  (1951). 
Schwarz  and  Schuchardt.     Z.  Zellforsch., 

35,  293  (1950). 
Seefelder.       Graefe-Saemisch    Hb.    d.    ges. 

Augenheilk.,  II,  1  (2),  Abh.  1  (1910). 
Seefelder  and  Wolfrum.    v.  Graefes  Arch. 

Ophthal,  63,  430  (1906). 
Seidel.   v.  Graefes  Arch.  Ophthal,  112,  170 

(1923)  ;    114,  157  (1924). 
Sheldon.     J.   biophys.   biochem.   Cytol,   2, 

253  (1956). 
Singer  and  Miinzer.     Denkschr.  K.  Akad. 

Wiss.  Wien,  55,  163  (1888). 
Sjostrand.    J.  cell.  comp.  Physiol,  33,  383 

(1949)  ;    42,  15,  45  (1953). 
Slonaker.    J.  Morphol,  13,  445  (1897). 
Smith,  F.    J.  ^no^,  56,  366  (1922). 
Soemmerring,      D.      W.        De      oculorum 

hominisanimaliumque,   etc.,   Goettin- 

gen  (1818). 
Sondermann.    Acta  Ophthal,  2,  260  (1933). 
Stannius.       Lhb.    vergl    Anat.,    Berlin,    2 

(1846). 
Stein.      Klin.    Mbl    Augenheilk.,    40    (1), 

286  (1902). 
Steinach.     Pflitgers  Arch.  ges.  Physiol,  47, 

289  (1890)  ;   52,  495  (1892). 
Steindorff.     Tabulce  Biologicce,  22  (i),  166 

(1947). 


MAMMALS 


607 


Stromeyer.     Dtsch.  Klin.,  11,  247  (1859). 
Studnitz.     Zool.  Jb.,  Abt.  Zool.  Physiol., 

54,  119,  313  (1934). 
Siindwall.    Amer.  J.  Anat.,  20,  147  (1916). 
Tandler.    Denkschr.  K.  Akad.  Wiss.  Wien, 

67,  677  (1899). 
Morphol.  Jb.,  30,  275  (1902). 
Anat.  Hefte,  31,  235  (1906). 
Tansley-     Brit.  J.  Ophthal.,  40,  178  (1956). 

Ophthalmologica,  Suppl.  48,  7  (1957). 
Tanzi.    Sperimentale,  46,  187  (1892). 
Teulidres  and  Beauvieux.     Arch.  Ophtal. 

(Paris),  48,  465  (1931). 
Theiler.       Acta     anat.     (Basel),     10,     255 

(1950). 
Thieulin.     These,  Paris  (1927). 
de  Toledo  Piza.     Rev.  brasil.  Oftal.,  14,  59 

(1955). 
Troncoso.     XV  Internat.  Cong.   Ophthal., 

Cairo.  4  (2),  98  (1937). 
Amer.  J.  Ophthal.,  25,  1,  1153  (1942). 
A  Treatise  of  Gonioscopy,  Phila.  (1948). 
Troncoso     and     Castroviejo.       Amer.    J. 

Ophthal,  19,  371,  481,  583  (1936). 
Usher.     Brit.  J.  Ophthal.,  8,  357  (1924). 
Uvama.   v.  Graefes  Arch.  Ophthal.,  132,  10 

(1934). 
Versari.     Arch.  ital.  Biol.,  33,  145  (1900). 
Vilter.    C.  R.  Sac.  Biol.  (Paris),  143,  1509 

(1949)  ;    147,  561  (1953)  ;    148,  1768, 

1963  (1954). 
Virchow.     Morphol.  Jb.,  11,  437  (1886). 
Graefe-Saemisch  Hb.  d.  ges.  Augenheilk., 

Leipzig,  II,  1,  193,  280  (1910). 
Vitello.     Boll.  Soc.  itcd.  Biol,  sper.,  6,  514 

(1931). 
Vitzou.    C.  R.  Acad.  Sci.  (Paris),  107,  279 

(1888). 
Vonwiller.       Z.    iciss.    Mikrosk.,    62,     14 

(1954). 
Vrabec.     Ophthalmologica,  123,  20  (1952). 
Waldeyer    and    Izquierdo.      Arch,    viikr. 

Anat.,  17,  367  (1880). 
Walls.    Copeia,  125  (1931). 

The  Vertebrate  Eye,  Michigan  (1942). 
Walzberg.     Vber  den  Bau  der  Thrdnenwege 

der  Haussdugethiere,  Rostock  (1876). 
Warwick.    J.  Anat.,  86,  492  (1952). 
Watrous  and  Ohnsted.     Amer.  J.  Physiol., 

132,  607  (1941). 


Watson.       Philos.     Trans.     B,    207,     311 

(1916). 
Weekers  and  Prijot.   Ophthalmologica,  119, 

321  (1950). 
Wagner     and     Intlekofer.       Klin.     Mbl. 

Augenheilk.,  120,  1  (1952). 
Welcker.    Arch.  Anthrop.,  28,  1  (1903). 
Wendt.     Vber  die  Harder'sche   Driise  der 

Sdugetiere,  Petersburg  (1877). 
\Miitnali.       J.     Anat.     Phi/siol.,    45,     131 

(1910)  ;   46,  36  (1911)'. 
The   Anat.   of    Human    Orbit,    London 

(1921). 
Winckler.      Arch.   Anat.    (Paris),    17,    131 

(1933). 
Wislocki.    Anat.  Rec,  113,  579  (1952). 
WoLfflin.    Klin.  Mbl.  Augenheilk.,  Ill,  129 

(1947). 
Wolff  and  Davies.     Brit.  J.  Ophthal.,  15, 

609  (1931). 
Wolfrum.         Ber.      dtsch.      ophthal.      Ges. 

Heidel.,  35,  206  (1908). 
Graefe-Saemisch  Hb.  d.  ges.  Augenheilk., 

Leipzig,  II,  1  (2),  Kap.  3  (1926). 
Woher.     Z.  Zellforsch.,  41,  521  (1955). 
Klin.  Mbl.  Augenheilk.,  129,  20  (1956). 
Arch.  Ophthal.  (Chicago),  58, -liG  {Idol). 
Woollard.      Proc.   zool.  Soc.    Lond.,    1071 

(1925)  ;    1  (1927). 
Brain,  49,  77  (1926). 
Wtirdinger.     Z.  vergl.  Augenheilk.,  4,   121 

(1886). 
Wybar.     Brit.  J.  Ophthal.,  40,  65  (1956). 
Zahoj -Bruckner.     Brit.  J.  Ophthal.,  8,  158 

(1924). 
Zander   and   Weddell.      J.    Anat.,    85,    68 

(1951). 
Brit.  J.  Ophthal,  35,  61  (1951). 
Zannini.     Atti  Mem.  Accad.  Sci.  Modena, 

3,  75  (1932). 
Zietzschmann.    v.  Graefes  Arch.  Ophthal, 

58,  61  ;  59,  116  (1904). 
Arch.  mikr.  Anat.,  65,  611  (1905). 
Arch,  vergl  Ophthcd.,  3,  129  (1913). 
Zimmerl.     Di  un  nuovo  muscolo  motore  d. 

globo  oculare  nelVequus  asinus,  Napoli 

(1906). 
Zimmermarui.      Arch.    Tierheilk.,   65,    626 

(1932). 
Ziirn.      Arch.    Anat.    Physiol,    Suppl.    99 

(1902). 


508 


THE   EYE   IN   EVOLUTION 


C  ^  /<j^ ? /  ^' 1"  i  ^a^ /* /> 


i-^t^ 


Fig.  665. — Cornelius  Ubbo  Ariens  Kappers  (1877-1946). 


CHAPTER  XVI 
THE  CENTRAL  ORGANIZATION  OF  VISION 

A  consideration  of  the  phylogenetic  evolution  of  the  central  nervous  organization 
of  vision  is  suitably  introduced  by  a  photograph  of  Cornelius  ubbo  ariens  kappers 
(1877-1946)  (Fig.  665),  Director  of  the  Centraal  Instituut  voor  Hersenonderzoek  in 
Amsterdam  in  1909,  and  Professor  of  Xeuro -anatomy  at  the  University  of  Amsterdam 
in  1928.  In  his  generation  he  was  the  greatest  authority  on  the  comparative  structure 
of  the  nervous  system,  and  his  magnuin  opus.  Die  vergleichende  Anatomie  des  Nerven- 
systems  der  Wirbeltiere  und  des  Menschen  (1920),  still  remains  the  classical  work  on 
this  subject.  His  work  was  not  alone  concerned  with  the  factual  description  of  structure 
but  was  enlivened  and  coordinated  by  much  original  thovight.  AiTiong  his  speculative 
concepts  the  best  known  is  that  of  "  neurobiotaxis,"  a  hypothesis  by  which  he 
endeavoured  to  explain  the  complicated  migration  of  nerve  centres  and  tracts  in 
phylogenetic  history,  and  the  seemingly  peculiar  location  and  relation  in  which  this 
has  resulted  in  the  higher  animals.  This  suggestion,  that  the  final  arrangement  of 
neural  elements  is  determined  by  an  association  of  function,  perhaps  on  a  physico- 
chemical  basis,  is  seen  in  many  of  those  parts  of  the  central  nervous  system  which  are 
associated  with  visual  and  photostatic  functions — the  position,  for  example,  of  the 
ocular  motor  nuclei  in  close  relation  to  the  posterior  longitudinal  bundle  and  the 
vestibular  systeni,  their  secondary  changes  in  position  running  parallel  to  changes  in 
the  paths  of  the  optic,  vestibular  and  coordinative  reflexes,  or  the  gradual  development 
of  a  decussation  of  fibres  at  the  chiasma  so  that  fibres  from  regions  of  the  retinae  which 
work  together  run  in  contiguity. 

In  the  first  chapters  of  this  book  we  have  seen  that  fight  has  a  four-fold 
action  upon  fiving  organisms — upon  the  general  metabolism  including  the 
reproductive  cycle,  upon  the  control  of  movement,  upon  the  retinal  and 
integumentary  pigmentation,  and  upon  behaviour,  and  eventually  con- 
sciousness, through  visual  sensations.  In  the  more  primitive  animals  the 
first  two  assume  the  greatest  importance,  in  the  higher  the  last  becomes 
completely  dominant,  while  the  third  always  plays  a  somewhat  subsidiary 
role.  It  is  obvious,  however,  that  none  of  these  can  become  effective  unless 
the  local  effects  of  the  photochemical  reaction  mitiated  by  light  are  made 
available  to  the  organism  as  a  whole  and  coordinated  with  its  general 
activities.  For  this  purpose  two  mechanisms  are  available — in  the  first  the 
effects  of  the  stimulus  are  conveyed  by  chemical  means,  in  the  second  by 
nervous  conduction. 

The  problems  of  communication  and  coordmation  were  relatively 
simple  in  unicellular  organisms,  but  unless  evolution  were  not  to  pass  beyond 
the  stage  of  colonial  Protozoa  or  the  sponges  and  confine  itself  to  entities 
comprised  of  loosely  aggregated  and  relatively  independent  cells,  rapidity  of 
communication  and  control  became  essential  for  the  development  of  a 
multicellular  body  with  all  its  potentialities  of  specialization  in  structure 
and  function.    The  evolution  of  an  efficient  conductmg  mechanism  was  thus 


510  THE   EYE   IN   EVOLUTION 

a  necessity  at  an  early  stage  if  an  organism  were  to  combine  large  size  with 
mobility  and  reactivity — attributes  necessary  for  its  survival.  Even  in 
unicellular  organisms,  however,  a  foretaste  of  two  fundamentally  different 
methods  of  response  to  light  or  other  stimuli  is  evident — ^the  first  and  most 
primitive,  a  simple  quantitative  kinetic  resjwnse  the  mechanism  of  which 
is  essentially  chemical,  and  the  other,  a  more  qualitative  shock-reaction  the 
basis  of  which  is  electrical. 

In  the  kinetic  response  the  amount  of  light  absorbed  by  a  photo- 
sensitive substance  determines  a  proportional  increase  or  decrease  of  activity, 
a  change  which  may  be  transmitted  beyond  the  confines  of  the  cell  by  the 
spread  of  the  chemical  products  of  the  reaction.  In  the  shock-response,  the 
rate  of  change  in  the  amount  of  light  absorbed  by  the  photosensitive  tissue 
is  of  importance  ;  the  precarious  electro -chemical  balance  of  protoplasm  in 
cellular  form  is  maintained  until  the  strength  of  the  stimulus  is  sufficient 
to  fire  it  into  sudden  activity,  like  an  explosive,  by  a  trigger-action.  The 
first  type  of  reaction  is  seen  in  plants  and  is  typically  evident  as  a  regulator 
of  basic  activities  in  animals  ;  the  second  is  characteristic  of  the  animal 
world  and  is  seen  in  the  lower  organisms  in  their  orientation  to  light  and  in 
the  higher  is  typical  of  the  economy  -oi  nervous  activity. 

The  classical  distinction  between  plants  and  animals  as  given,  for  example,  by 
Haldane  and  Huxley  in  their  standard  work  on  biology  as  the  only  valid  differentiation, 
concerned  the  type  of  foodstuffs  they  utilized,  in  the  first  case  derived  innocently 
from  the  air  and  the  soil,  in  the  second,  from  the  syntheses  accomplished  by  other 
living  things.  With  some  exceptions,  such  as  insectivorous  orchids,  this  is  true, 
although  difficulties  arise  among  unicellular  organisms  on  the  border-line  between 
plants  and  animals  ;  thus  some  Flagellates  have  green  chromatophores,  others  are 
colourless  and  live  saprophytically  and  may  be  regarded  as  the  starting  point  on  the 
one  hand  of  unicellular  Thallophytes,  on  the  other  of  Protozoa.  A  more  fundamental 
differentiation,  however,  lies  in  the  mechanism  of  their  response  to  stimuli,  a  differentia- 
tion which  determines  the  relative  simplicity  and  serenity  of  vegetable  existence  with 
its  close  affinity  to  the  sun's  energy  and  the  earth's  chemistry,  in  contrast  with  the 
-     complexity  and  hurry-scurry  of  animal  life  with  its  mobility  and  independence. 

In  both  plants  (Blaauw,  1914-15)  and  animals  (Northrop  and  Loeb,  1923)  the 
stimulatory  mechanism  is  purely  photochemical,  but  there  is  a  fundamental  difference 
in  the  manner  of  conduction  and  in  the  effector  mechanism.  It  is  probable  that  all 
living  cells  are  able  to  conduct  waves  of  excitation,  the  common  mechanism  both  in 
plant  and  animal  cells  being  a  wave  of  depolarization  which  passes  along  the  plasma 
membrane  and  momentarily  increases  its  permeability.  But  in  plants  the  stimulus 
must  be  received  directly  by  each  cell,  and  propagation  of  the  stimulus  to  a  point  at 
a  distance  is  effected,  not  by  the  direct  transmission  of  an  imjxilse  from  cell  to  cell, 
but  by  the  transfer  of  the  products  of  the  primary  change,  photochemical  or  otherwise, 
by  a  process  somewhat  more  rapid  than  simple  diffusion. ^  Such  stimulatory  substances 
have  an  obvious  analogy  to  the  prodvicts  of  the  endocrine  glands  of  animals  but  none 
to  the  propagation  of  nervous  impulses.  We  have  seen  that  substances  of  this  type  are 
responsible  for  the  flowering  of  plants  ^  and  that  a  group  of  hormones,  particularly  the 
auxins,^  are  responsible  for  the  growth  and  movement  of  plants — substances  which 

^   10  mm.  per  hour  in  the  case  of  auxin,  p.  39. 
2  p.  10.  »  p.  39. 


CENTRAL   ORGANIZATION   OF  VISION  511 

can  diffuse  through  or  can  be  trapped  in  gelatine  and  thus  can  be  transferred  to 
another  plant,  therein  to  produce  the  typical  response.  The  exjoeriments  of  Ricca 
(1916)  on  the  highly  irritable  Mimosa  pudica,  or  of  Mangold  (1923)  on  insectivorous 
plants,  bring  out  the  same  point  ;  although  the  later  investigations  of  Bose  and  Das 
(1925),  Bose  (1926-28)  and  Molisch  (1929)  would  seem  to  indicate  that  in  these  very 
highly  specialized  forms  many  of  the  characteristics  of  nervous  activity  may  be  closely 
simulated.  The  difference,  however,  between  the  primitive  response  to  light  in  plants 
and  animals  is  merely  a  difference  of  method  ;  the  reaction  is  fundamentally  the  same, 
the  transformation  of  a  photochemical  change  into  a  motorial  response. 


THE  NERVOUS  CONTROL 

Although  hormonal  control  persists  in  animals,  particularly  in  the 
regulation  of  their  basic  activities,  their  movements  and  responses  to  external 
stimuli  are  active  rather  than  jDassive  ;  the  explosive  response  fired  by 
"  trigger-action  "  gives  them  mobility.  Even  in  the  most  primitive  animals 
the  energy  provided  by  the  photochemical  reaction  contributes  to  the 
chemical  activation  of  neighbouring  molecules,  thus  kindling  a  chain  of 
chemical  changes  by  means  of  which  a  phase  of  excitation  is  propagated 
through  the  protoplasm  from  the  site  of  stimulation  to  the  site  wherein 
the  response  is  produced.  It  is  interesting  that  in  organisms  as  lowly  as 
Protozoa,  differentiated  fibrils  are  evident  formed  by  basal  granules  arranged 
in  longitudinal  rows  within  the  single  cell,  one  at  least  of  the  functions  of 
which  is  to  coordinate  the  movements  of  the  cilia  (Neresheimer,  1903  ;  Gelei, 
1935).  The  evidence  is  convincing  that  some  of  these  are  paths  for  the 
propagation  of  stimuli,  since  microdissection  experiments  have  showTi  that 
when  they  are  cut  the  rhythm  of  the  movements  of  cilia  is  disrupted  (Taylor, 
1920-41  ;  MacDougall,  1928  ;  MacLennan,  1935).  There  is  also  evidence 
that  in  colonial  Protozoa,  conduction  can  in  this  way  proceed  from  cell  to 
cell  by  intercellular  fibrils  (Taylor,  1941)  (Fig.  666).  In  these  forms  this 
phenomenon  is  too  rapid  to  be  due  to  diffusion  and  too  slow  to  have  an 
electrical  basis,  and  it  is  probable  that  these  fibrils  result  from  the  preserva- 
tion through  natural  selection  of  chance  molecular  patterns  in  the  protoplasm 
which  favour  the  relay  of  a  train  of  chemical  reactions,  and  that  from  these 
strand-like  plastids  nervous  tissue,  with  its  specialization  as  a  conductor, 
had  its  origin  (Bovie,  1926). 

Once  an  effective  intracellular  means  of  conduction  has  been  established, 
the  obvious  method  of  advance  is  for  part  of  a  cell  to  stretch  and  become 
specialized.  In  this  way  certain  of  the  surface  cells  which,  because  of  their 
exposed  position  receive  stimuli  from  the  environment,  send  long  processes 
inwards  conveying  the  message  of  their  stimulation  to  neighbouring  parts 
of  the  organism.  Eventually,  stretching  many  times  their  own  breadth, 
they  leave  the  surface  layer  and,  abandoning  sensory  reception,  specialize 
in  conducting  the  excitations  of  other  cells  so  that  fuially  a  network  of 
conducting  paths  is  laid  down  underneath  the  integument  and  the  entire 


512 


THE   EYE   IN   EVOLUTION 

Figs.  666  to  670. — The  Evolution  of  the  Nervous  System. 


GXZ] 


Fig.  666. — Two  individuals  of  a 
protozoan  colony  joined  by  inter- 
cellular bridges. 


Fig.  667. — The  impossibility  of  a 
direct  cell-to-cell  link  in  a  complex 
multicellular  organism.  Five  cells 
require  10  two-way  channels. 


Fig.  668.- 


-The  nerve-net — a  common  network  linking  up  all  the  cells  with 
a  trunk  pathway  between  two  important  cells. 


^. 


^ 


^ 


^ 


'■J*.*-- 


Fig.     669. — The     ganglionic     nervous 
system  of  Arthropods. 


Fig.  670. — The  central  nervous  system 
of  Primates. 


organism  becomes  coordinated  in  its  response  to  a  single  stimulus.  Thus  a 
nervous  system  was  born.  A  subepithelial  nerve-net  of  this  type  made 
its  first  appearance  in  Coelenterates,  but  it  is  obvious  that  a  diffuse  network 
without  short-circuiting  and  centralization  is  both  wasteful  and  inefficient. 
Fig.  6G7  shows  that  to  link  up  a  large  number  of  cells  in  this  way  becomes 
a  practical  impossibility  :  to  link  up  5  requires  10  two-way  interconnections  ; 
the  most  that  can  reasonably  be  done  is  to  send  out  a  call  of  general  aware- 
ness. It  has  been  a  commonplace  to  compare  the  nervous  system  with  a 
telepl;  exchange  ;  if  any  single  subscriber  is  to  be  put  m  contact  with 
any  ot         conomically,  cables  rather  than  a  multiplicity  of  individual  wires 


CENTRAL   ORGANIZATION   OF  VISION 


513 


must  be  employed  and  central  exchanges  must  be  introduced.  And  so  the 
diffuse  network  became  canalized  into  trunk-pathways  between  important 
parts — a  stage  reached  in  Echinoderms — and  then  telephone  exchanges  were 
introduced  in  the  form  of  ganglia  which  are  characteristic  of  the  nervous 
system  of  the  worms,  Arthropods  and  Molluscs  ;  therein  not  only  the  relay 
but  the  integration  of  messages  became  possible  (Figs.  668-9).  All  through 
this  process  the  head-end  of  the  animal  tended  most  readily  to  encounter 
external  stimuli;  in  this  region  which  first  made  the  acquaintance  of  predators 
or  prey,  the  sense-organs  became  concentrated.  All  through  the  process 
the  degree  of  nervous  develoj)ment  depended  on  the  richness  of  the  stimuli 
provided  by  the  sensory  organs — at  first  the  tactile,  chemical  and  olfactory, 

Figs.  671-2.- — -Contractile  Myo-epithelial  Cells. 


Fig.  671. — In  the  sponge,  Sycon  gelalino- 
sum,the  myo-epithelial  cells  surround  the 
central  ajoerture,  which  is  capable  of 
being   contracted  or  dilated. 


Fig.  672. — An  isolated  cell  from  the 
Coelenterate,  Pelagia,  showing  the  flagel- 
lum  and  the  long  striated  muscular  base 
(after  Krasinska). 


but  eventually  the  visual  ;  and  so  at  the  head-end  became  concentrated  the 
main  exchange -centre  which  in  course  of  time  assumed  control  of  all  the 
others  for  the  common  good.  This  process  of  centralization  resulted  in  the 
final  development  of  the  brain  of  Vertebrates  (Fig.  670).  To  achieve  this  final 
development  the  whole  of  the  economy  of  the  body  has  been  subordinated; 
on  the  supremacy  of  the  main  cerebral  centre  the  eventual  predominance  of 
the  Vertebrates  and  of  man  is  built ;  and  in  the  end  the  evolution  of  vision  is 
determined  not  by  increasing  specialization  of  the  eye  but  on  progressively 
more  efficient  analysis  and  integration  by  the  cerebrum.  "  The  law  of 
progress  is  this — the  race  is  not  to  the  swift,  nor  to  the  strong,  but  to  the 
wise  "  (Gaskell.  190S). 

In  Protozoa  extracellular  conducting  nervous  tissue  was,  in  general, 
not  required  ;  in  the  sponges  (Porifera)  no  nervous  elements  exist,  for  these 
loose  afforegations  of  cells  with  little  community-life  and  without  observable 
cohesion  can  be  torn  in  pieces  and  reassemble  again.  These  organisms 
thus  exhibit  none  of  the  rapid  reactions  characteristic  of  the  higher  forms 

8.0. — VOL.  I.  33 


514 


THE   EYE   IN   EVOLUTION 


of  animal  life,  but  at  the  same  time  they  show  a  contractile  response  to 
tactile  stimuli  as  their  oscula  open  and  close  with  movements  of  the  sea- 
water.  This  is  effected  by  the  evolution  of  contractile  myo -epithelial 
CELLS,  epithelial  cells  which  acquire  the  power  to  contract  when  stimulated 
and  thus  act  as  combined  receptors  and  effectors  ;  in  higher  forms  these 
specialize  in  their  contractile  function  and  are  displaced  to  form  a  muscular 
layer  beneath  the  epithelium  (Figs.  671  and  672).  In  Parker's  (1911-18) 
view  these  muscular  "  independent  effectors  "  are  thus  more  primitive  than 
nerve  cells.     Nor,  indeed,  is  this  illogical,  for  since  all  primitive  responses 

Figs.  673  to  678. — The  Evolution  of  Receptors  and  Effectors. 


Fig.  673. 


Fig.  674. 


Fig.  675. 


n 


! 


Fig.  676. 


Fig.  677. 


Y     Y 
-o   -o 


'k 


IV; 


X 


Fig.  678. 


Fig.  673. — A  specialized  sensory  cell  (sponge). 

Fig.  674. — A  myo-epithelial  cell   (an  independent  receptor-effector)  (jellyfish). 

Fig.  675. — A  receptor-effector  system  consisting  of  a  sensory  cell  with  a 
"  nerve  "  fibril  leading  to  a  motor  effector  (muscle)  (sea-anemone). 

Fig.  676. — The  subepithelial  nerve-net  (jellyfish). 

Fig.  677. — An  intercalary  neurone  between  the  receptor  and  effector  (worms). 

Fig.  678. — A  sensory  organ,  an  afferent  nerve  (posterior  root  ganglion),  an 
intercalary  neurone  and  an  effector  organ  (Mammals). 

are  tropisms,  neither  an  independent  receptor  nor  a  conductor  would  be  of 
value  were  a  muscular  effector  not  available.  Initially  the  sense-muscle 
cell  was  stimulated  directly  ;  only  when  the  muscle  became  specialized 
would  specific  receptors  and  conductors  become  necessary  (Figs.  673  to  678). 


THE    NERVE -NET 

In  the  Coelenterates,  the  first  type  of  animal  to  require  a  wholly 
coordinated  body,  a  nervous  system  first  made  its  appearance  as  a  diffuse 
nerve-net, 1  lying  between  the  epithelial  layer  and  the  subepithelial  muscular 
layer.     Into  it  dip  down  nerve-like  processes  from  the  sensitive  epithelial 

^  For  :]ic  physiological  mechanism  of  the  nerve-net,  see  Romanes  (1876-77),  Bethe  (1903), 
Mayer  (li  8),  v.  Uexkull  (1909),  Parker  (1917-32),  Pantin  (1935-52),  Prosser  (general 
review)  (lUi  ,.. 


NERVE-NET 


515 


cells  which  establish  relay's  with  ganglion  cells  which  have  migrated  inwards 
from  the  surface  layer  and  have  formed  an  interlacing  network  ;  through 
these  the  underlying  muscular  layer  is  stimulated  (Figs.  679  and  680).  The 
early  histologists  pictured  such  a  net  as  a  sjmcytium  composed  of  anastomos- 
ing fibres  (Hadzi,  1909),  but  vital  staining  shows  that  the  fibres  run  parallel 
to  and  intertwine  with  each  other  without  actual  fusion  (Bozler,  1927  ; 
Woollard  and  Harpman,  1939)  ;  the  junctions,  however,  are  not  polarized 
as  in  true  sjaiapses.  Conduction,  therefore,  is  free  and  equal  in  all  directions 
so  that  any  stimulus  is  diffusely  spread  (Eimer,  1874  ;    Romanes,   1876); 


Figs.   679  axd   680. — The  Subepithelial  Xerve-net  of  Ccelexterates. 


Fig.  679.— The  nerve- 
net  of  Hydra  (after 
Clause,  Grobben  and 
Kiihn). 


Fig.    680. — Subepidermal     nerve-net    around     the      oral 
disc  of  Hydra. 

E,    epidermis  ;     G,    ganglion    cells    in    the    nerve-net  ; 
S,  epithelial  sensory  cells  (after  Hadzi). 


consequently  if  interdigitating  incisions  are  made  and  the  animal  is  cui/ 
into  zig-zag  strips  leaving  only  nervous  comiections,  impulses  pass  either 
way  and  round  corners  so  that  an  effective  res2)onse  is  obtained. ^ 
Indeed,  if  all  the  sense-organs  but  one  are  removed  from  a  jellyfish,  the 
rhythmic  impulses  for  swimming  movements  are  started  by  the  sole  survivor 
and  proceed  in  all  directions.  Control  is  thus  entirely  peripheral  and  execu- 
tion indiscriminate  without  evidence  of  central  mtegration,  and  to  any 
stimulus  the  response  is  monotonously  similar  and  universal. 

While  perijjheral  control  by  such  a  subepidermal  nerve-net  is  the  sole 
mechanism  available  to  Coelenterates,  it  persists  in  many  animal  groups — ■ 
Echinoderms,  worms  (Fig.  681).  Molluscs,  and  Balanoglos.sid.s — and  finds 
an  analogy  in  the  autonomous  visceral  plexuses  of  Vertebrates  such  as 
the  myenteric  plexus  ^\hich  coordinates  movements  of  the  intestine.  As 
evolution  proceeds,  ho^\•ever,  the  nerve-net  assumes  a  more  and  more  sub- 
sidiary role.     The  only  area  in  turbellarian  worms  wherein  the  primitive 

'  Jellyfish — Mayer  (1908);   sea-anemone — Parker  (1917);   colonial  Coelenterates — Parker 
(1920). 


516  THE   EYE   IN   EVOLUTION 

complete  independence  is  retained  is  in  the  proboscis,  which,  if  nervously- 
isolated,  amputates  itself  and  shows  independent  food-seeking  reactions 
(Kepner  and  Rich,  1918).  In  Annelids  and  Molluscs,  however,  the  nerve-net 
serves  only  as  a  relay  system  over  a  local  area  without  independent  activity, 
dealing  with  messages  from  the  nerve-cord  or  ganglia.  In  general,  the  peri- 
pheral system  is  the  more  important  in  sluggish  animals  but  as  rapidity  of 
response  and  general  activity  increase,  the  central  mechanism  takes  over  an 
increasing  share  of  control. 

Even  in  Ccelenterates,  however,  some  early  signs  of  specialization  are  seen  within 
the  nerve-net.  In  some  medusae  and  sea-anemones,  through-tracts  of  long  continuous 
fibres  form  nerve-trunks  for  rapid  conduction,^  and  in  sea-anemones  a  difference  in 
the  response  between  the  fi'ee  and  the  central  end  of  a  cut  tentacle  indicates  a  primitive 
type  of  polarity  (Parker,  1917  ;  Pantin,  1935),  Moreover,  the  possibility  of  the 
existence  of  crude  reflex  arcs  is  indicated  by  the  recij^rocal  contraction  of  circular  and 
radial  muscles  (Bozler,  1926). 

TRUNK-PATHWAYS 

Although  a  hint  of  preferential  conduction  appears  in  Coelenterates,  the 
advantage  is  obvious  of  short-circuiting  the  diffuse  and  indiscriminate 
conduction  in  a  nerve-net  through  trunk -pathways  composed  of  long  giant 
fibres  by  which  the  transmission  of  vital  messages  between  important  points 
is  rapid  and  direct  ;  this  is  first  achieved  in  Echinoderms  in  which  radial 
symmetry  has  been  attained.  In  the  starfish,  for  example,  there  is  a  diffuse 
nerve-net,  but  from  the  sensory  organs — the  important  olfactory  and 
statolith  organs  and  the  yet  unimportant  eyes — situated  at  the  tips  of  each 
of  the  five  arms  where  the  animal  first  contacts  the  dangers  or  opportunities 
of  its  environment,  there  arises  a  large  nerve-trunk  which  runs  down  to  the 
centre  of  the  body  where  the  five  trunks  combine  to  form  a  ring  encircling 
the  oral  aperture  (Fig.  166).  This  central  nerve-ring  with  its  five  radiating 
nerve -trunks  acts  as  the  main  directive  system  without  which  the  animal 
shows  sluggish  and  poor  coordination  in  such  activities  as  righting  move- 
ments (Cole,  1913)  ;  at  the  same  time  these  main  pathways  are  linked 
closely  with  the  peripheral  net,  which  even  in  isolation  can  effect  a  certain 
amount  of  coordination,  particularly  by  local  reflexes  between  neighbouring 
spines  (Langeloh,  1937  ;  Smith,  1937-50  ;  Kinosita,  1941).  At  this  stage 
central  control  is  neither  fixed  nor  complete  but  there  is  a  plastic  reciprocity 
between  it  and  the  still  important  peripheral  system.  It  is  probably  for 
this  reason  that  the  starfish,  although  showing  considerable  complexity  in 
behaviour  in  such  reactions  as  feeding,  righting  itself,  or  escaping  from 
restricted  confines,  yet  shows  no  ability  to  profit  by  experience  by  adopting 
persistent  modifications  in  its  conduct  (Jennings,  1907).  Indeed,  the  animal 
may  pull  itself  apart  by  the  antagonistic  activity  of  its  o^\^l  tube-feet 

1  Call       j's,  in  which  the  velocity  of  the  contractile  wave  is  1-2  m./isec,  compared  with 
0-15  m./set         the  nerve-net  (Pantin,  1935).    In  the  nerves  of  the  cat  it  is  119  m./sec. 


NERVE   TRUNK-PATHWAYS 


617 


(Kerkut,  1954-55).  The  primitiveness  of  the  central  coordmative  control 
at  this  stage  may  best  be  illustrated  by  the  analogy  used  by  von  Uexkiill 
(1897)  :  when  a  dog  runs  the  animal  uses  its  legs  ;  when  a  sea-urchin  runs 
the  spines  move  the  animal. 

As  evolution  proceeds,  we  shall  see  that  nerve-nets  with  directive  conducting 
trunks  get  progressively  less  important  in  worms,  Arthropods  and  Molhiscs  ;  but  it 
is  of  interest  that  the  most  primitive  Proto-chordates,  the  Balanoglossids  (Hemi- 
chordata),  have  a  comparable  non-integrated  system  of  dorsal  and  ventral  nerve-cords 
with  collar-connections  associated  with  a  peripheral  nerve-net  (Bullock,  1940).  It 
will  be  remembered  ^  that  these  worm-like  burrowing  creatures  are  without  eyes.  It  is 
of  interest  that  this  primitive  type  of  nervous  system  is  an  indication  of  the  great 
phylogenetic  age  of  the  emergence  of  the  chordate  stock^. 


Bethe.    AUg.  Anat.  Physiol,  d.  Xervensystems, 

Leipzig  (1903). 
Blaauw.     Z.   Botan.,  6,  641    (1914)  ;    7,  465 

(1915). 
Bose.      The   Nervous   Mechanism   of   Plants, 

N.Y.  (1926). 
The    Motor    Mechanisyn    in    Plants,    N.Y. 

(1928). 
Bose  and  Das.       Proc.   roy.  Soc.   B,  98,  290 

(1925). 
Bovie.     Biol.  Aspects  of  Colloid  and  Physiol. 

Chem.,  London  (1926). 
Bozler.     Z.  vergl.  Ph>/siol.,  4,  37  (1926). 

Z.  Zellforsch.,  5,  244  (1927). 
Bullock.     Biol.  Bull..  79,  91  (1940). 
Cole.     Biol.  Bull.,  24,  362  (1913). 
Eimer.      Verbdl.  physikal.-Med.   Ges.,  6,   137 

(1874). 
Gaskell.     The  Origin  of   Vertebrates,  London 

(1908). 
Gelei.     Z.  Zellforsch.,  22,  244  (1935). 
Hadzi.    Arb.  Zool.  Inst.  Wien,  17,  225  (1909). 
Jennings.      Univ.   Calif.    Publ.    Zool.,   4,    53 

(1907). 
Kepner  and  Rich.    J.  exp.  Zool..  26,  83  (1918). 
Kerkut.     Behaviour,  6,   206   (1954)  ;    8,   112 

(1955). 
Kinosita.    Jap.  .J.  Zool.,  9,  209,  221  (1941). 
Langeloh.     Zool.  Jb.,  Abt.  Zool.  Physiol.,  57, 

235  (1937). 
MacDougall.     Biol.  Bull.,  54,  471  (1928). 
MacLennan.        Arch.      Proti.stenk.,     86,      191 

(1935). 
Mangold.     Ergebn.  Physiol.,  21,  361  (1923). 
Mayer.     Publ.  Carnegie  Inst.,  Wash.,  No.  47 

(1906)  ;   No.  102,  1,  113,  115  (1908). 


1920). 
Phila. 


Molisch.    Nature  (Lond.).  123,  562  (1929). 
Neresheimer.    Arch.  Protistenk.,  2,  305  (1903). 
Northrop  and  Loeb.    J.  gen.  Physiol.,  5,  581 

(1923). 
Pantin.    J.  exp.  Biol.,  12,  119,  139,  156  (1935). 
Symposia  Soc.  exp.  Biol.,  4,  175  (1950). 
Proc.  roy.  Soc.  B,  140,  147  (1952). 
Parker.      Proc.   Amer.   philos.  Soc,   50.    217 
(1911). 
J.  exp.  Zool.,  22,  87  (1917)  ;   31,  475 
J.  gen.  Physiol.,  1,  231  (1918). 
The    Elementary    Nervous    Syste?n, 

(1919). 
J.  cell.  comp.  Physiol.,  1,  53  (1932). 
Prosser.     Physiol.  Rev.,  26,  337  (1946). 

Comparative    Animcd    Physiology,    London 
(1950).  ■ 
Ricca.    Arch.  ital.  Biol.,  65,  219  (1916). 
Romanes.        Philos.     Trans.     B,     166, 

(1876)  ;    167,  659  (1877). 
Smith,  J.   E.       Philos.    Trans.   B,  227, 
(1937). 
Biol.  Bev.,  20,  29  (1945). 
Symposia  Soc.  exp.  Biol.,  4,  196  (1950). 
Tavlor.      Univ.   Calif.    Publ.    Zool.,    19,    403 
(1920). 
Galkins   and   Summers's  Protozoa  in  Biol. 
Research,    Columbia    L^niv.    Press,     191 
(1941). 
v.  Uexkiill.    Z.  Biol.,  34,  298  (1897). 

Umu-elt     u.     Inner  aelt    der     Tiere,     Berlin 
(1909). 
Woollard  and  Harpman.  .7.  Anat.  (Lond.),  73, 
559  (1939). 


269 


111 


THE    GANGLIONIC    NERVOUS    SYSTEM 

When  bilateral  symmetry  was  gained  (as  in  worms)  a  further  great 
advance  in  neural  economy  became  j^ossible.  for  now  the  sensory  organs,  the 
food-and-danger  predictors  gathered  preferentially  at  the  anterior  end  of 
the  animal,  led  to  a  concentration  of  nerve-elements  here  also,  thus  inaugu- 

1  p.  227.  2  p_  233. 


518 


THE   EYE   IN   EVOLUTION 


rating  the  centralization  of  the  nervous  system.  In  this  way  the  enormous 
economic  benefit  of  central  exchanges  became  possible,  at  first  with  one  or 
more  trunk-pathways  running  from  the  dorsal  head-ganglion  down  the  length 
of  the  body,  and  then  as  segmentation  of  the  body  progressed,  with  the 
interposition  of  ganglia  in  the  central  chain,  each  ganglion  gathering  up  and 
issuing  incoming  sensory  and  outgoing  motor  nerves  to  its  owti  particular 
segment.  Within  and  between  the  segmental  ganglia  the  incoming  and 
outgoing  nerves  combined  with  associated  neurones  in  the  central  system 
itself  to  form  a  complicated  interconnecting  network,  the  neuropile,  on 
which  reflex  activity  could  be  built  ;  by  means  of  these  neurones  which  have 
no  direct  connection  with  the  exterior,  in  association  with  the  giant  fibres  of 
the  trunk-pathways,  the  activities  of  the  whole  organism  are  coordinated,  a 
foretaste  of  the  infinitely  complex  system  which  finally  constitutes  the 
cerebral  cortex  of  the  Primates.  In  this  way  peripheral  control  through  the 
subepidermal  nerve-net  gave  place  to  central  control  through  reflex  path- 
ways and  the  way  was  prepared  for  the  dominance  of  cephalic  sense-organs 
and  nerve-centres,  an  arrangement  seen  in  the  nervous  systems  of  worms, 
Arthropods  and  Molluscs. 

THE    NERVOUS    SYSTEM    OF    WORMS 

The  initial  stage  in  the  development  of  the  ganglionic  nervous  system 
is  thus  the  appearance  of  a  single  cephalic  ganglion  from  which  issues  a 
number  of  nerve-trunks  which  break  up  into  the  peripheral  nerve-net.    This 


Figs.  681  and  682. — The  Nervous  System  of  Unsegmented  Worms. 

Oc— 1 

_  PAIRED 

l^^^  5-'--" LATER  AL 
NERVES 


Fig.    681. — The    nervous     system     of 
a  primitive   turbellarian  worm. 

Consisting  of  a  cerebral  ganglion, 
CG,  Nvith  several  nerve  trunks  and  a 
subepi-.-.rmal  nerve-net. 


Fig.  682. — The  nervous  system  of 
a  higher  type  of  turbellarian 
worm. 

The  fused  cerebral  ganglion,  CG, 
with  two  closely  associated  ocelli,  Oc, 
and  paired  nerve-trunks  (after  Hat- 
schek  and  Stempel). 


GANGLIONIC  NERVOUS   SYSTEM 


519 


is  seen  in  the  simplest  unsegmented  worms,  such  as 
some  Turbellarians,  wherein  this  single  ganglion  is 
responsible  for  relaying  sensory  messages  and  co- 
ordinating motor  responses  (Fig.  681).  In  other  Turbel- 
larians, two  to  eight  nerve -cords  run  posteriorly  from 
the  ganglion  (Fig.  682)  ;  each  contains  nerve  cells,  not 
yet  grouped  into  ganglia,  and  gathers  afferent  fibres  ; 
and  so  long  as  these  are  left  intact — but  only  so  long — 
spontaneous  movement  and  coordinated  responses 
persist.  1  When  the  rudimentary  ocelli  are  few  they  are 
grouped  on  the  dorsal  aspect  of  the  anterior  end  and 
the  nerve  fibres  run  directly  into  the  cerebral  ganglion  ; 
when  they  are  many  and  diffusely  scattered,  they  enter 
the  peripheral  nerve-net.  The  former  arrangement  is 
also  seen  in  the  larvse  of  some  Insects  (Fig.  683). 

Again,  the  simple  system  of  a  single  ganglion  controlling 
a  peripheral  mechanism  is  seen  among  the  primitive  Proto- 

chordates  in  the  Tunicates  ;  when  the  ganglion  is  removed  the  Ascidian  may  slowly 
develop  reflexes  confined  to  a  single  siphon  when  stimulated,  but  all  inter-siphonal 
responses  and  general  coordination  are  lost  (Kinoshita,  1910  ;  Day,  1919  ;  Prosser, 
1946). 

In  SEGMENTED  WORMS  (annelids),  however,  the  nerve-cells  are  grouped 
into  ganglia,  each  subserving  the  receptor-effector  mechanism  of  its  own  and 
often  adjacent  segments.  The  simplest  form  of  such  a  system  is  seen  in 
Oligochaetes  such  as  the  earthworm,  Lumbricus  (Fig.  684).  Situated  dorsally 
in  the  third  segment  are  two  cerebral  ganglia  from  which  emerge  two 
nerve-cords  ;   initially  these  form  a  ring  around  the  pharjaix  beneath  which 


Fig.    683.— The    Eye 
OF    THE    Larva    of 

AciLlUS. 

The  fibre-like  pro- 
longations of  the  light- 
sensitive  cells,  R,  go 
directly  into  the  cere- 
bral ganglion,  G  (after 
Gaskell). 


Fig.  684. — Nervous  System  of  a  Segmented  Worm. 

Transverse  section  through  the  earthworm.  S.E.,  surface  epithelium  ;  CM., 
circular  muscles  ;  L.M.,  longitudinal  muscle  ;  S^,  sensory  cell  the  fibre  from  which 
terminates  directly  in  the  subepidermal  nerve-net  ;  S-,  sensory  cell  the  fibre  from 
which  goes  to  a  segmental  ganglion  to  merge  in  the  neurojjile  ;  A,  association  neurone, 
the  processes  from  which  do  not  leave  the  central  nervous  system  but  run  mainly  up 
and  down  the  ganglionic  chain  (perpendicular  to  the  page)  ;  M,  two  motor  neurones, 
the  dendrites  of  which  contribute  to  the  neuropile  ;  N,  neuropile,  comiDosed  of  pro- 
cesses of  the  three  types  of  cell — sensory,  motor  and  associative. 


1  Bardeen  (1901)  in  Planarians 
Rietschel  (19.35)  in  Cestodes. 


Eggers  (1924)   and  Friedrich  (1932)   in   Nemertines 


520 


THE   EYE   IN   EVOLUTION 


they  unite  as  the  first  ventral  ganghon  and  then  run  to  the  posterior 
extremity  of  the  body  to  form  a  double  but  compact  united  ventral  nerve- 
cord.  The  segments  are  short  and  the  segmental  paired  ganglia  which 
connect  with  the  subepidermal  nerve  plexus  are  almost  confluent  ;  and  down 
the  nerve-cord  there  run  three  dorsal  and  two  ventral  giant  fibres  which 
transmit  impulses  down  the  entire  length  of  the  worm,  mediating  rapid 

end-to-end  "  startle  "  reactions  (Stough, 
1926-30  ;  Smallwood  and  Holmes,  1927  ; 
Bullock,  1945).^  The  peripheral  nerve- 
plexus  is  largely  a  sensory  relay,  and 
although  occasional  connections  ^  between 
sense  organs  directly  to  the  underlying 
muscle  may  persist,  they  are  unimportant 
in  behaviour  over  which  the  central  nerve- 
cord  has  taken  complete  control  (Janzen, 
1931  ;  Coonfield,  1932  ;  Prosser,  1935  ; 
and  others). 

In  the  polychaete  worms,  the  segmen- 
tation becomes  more  obvious  :  the  well- 
formed  cerebral  ganglion,  the  oesophageal 
ring  and  the  commencement  of  the  ventral 
ganglionated  cord  of  Nereis  are  seen  in 
Fig.  685.  The  bi-lobed  cerebral  ganglion, 
which  resembles  structurally  the  cerebral 
ganglion  of  Arthropods,  receives  nerves 
from  the  tentacles  and  palpi  as  well  as 
the  short,  thick  of)tic  nerves  from  the  four 
simple  eyes  which  seem  almost  to  be  sit- 
ting upon  it. 


Fig.  685. — The  Nervous  System  of 

THE     POLYCH.'ETE     WoRM,     NeJUIS. 

CO,  cerebral  (supra-oesophageal) 
ganglion,  in  close  association  with 
which  are  the  4  eyes — a  paired 
anterior,  E^,  and  posterior,  E"^.  The 
infra- oesophageal  ganglion,  G,  marks 
the  beginning  of  the  ganglionated  nerve 
cord,  N,  connected  to  the  cerebral 
ganglion  by  circuni-oesophageal  con- 
nectives, C  (after  Q^iatrefages). 


The  progress  of  cephalic  dominance  in  the 
segmented  worms  is  interesting.  Normally,  the 
earthworm  is  negatively  phototactic  to  light, 
but  after  removal  of  the  cerebral  ganglion  the 
direction  of  the  response  is  reversed  ;  if  the  ventral  cord  is  sectioned  the  anterior 
part  of  the  animal  turns  away  from  the  light,  the  j^osterior  towards  it  (Hess,  1924  ; 
Nomura,  1926-27  ;  Prosser,  1934  ;  Howell,  1939).  The  negative  responses  are  thus 
controlled  by  the  brain,  the  positive  by  the  ventral  cord.  The  activity  of  the  cerebral 
ganglion  therefore  normally  dominates  that  of  the  lower  ganglia,  the  responses  of  which 
it  normally  opposes.  After  the  cerebral  ganglion  is  removed  from  the  earthworm,  the 
animal  remains  active,  eats,  burrows  and  copulates,  the  reactions,  however,  being  per- 
formed some  10  or  15  times  more  slowly  (30  as  compared  with  2  minutes)  ;  a  similar 
decrease  in  responses  is  induced  by  subnormal  temperatures  or  depressive  drugs.  The 
same  operation  in  Nereis,  on  the  other  hand,  leaves  it  overactive  in  its  responses  to 

^  Th(   -need  of  travel  in  the  giant  fibres  is  17  to  45  m./sec,  whereas  that  in  the  small  fibres 
of  the  eov    :  •  0-025  m./sec.  (Bovard,  1918  ;   Eccles  et  al.,  1933  ;   Bullock,  1945). 
«  Not  i     ,11(1  in  the  Polychrptes  (Just,  1924). 


GANGLIONIC   NERVOUS   SYSTEM 


521 


light  or  chemical  stimuli  but  unable  to  burrow.  If  the  suboesophageal  ganglion  is  then 
removed,  the  worm  lies  quiet  and  inert  (Loeb,  1894  ;  Maxwell,  1897  ;  Prosser,  1934). 
It  would  thus  seem  that  the  cerebral  ganglion  is  primarily  a  sensory  centre  exercising 
an  inhibitory  control  upon  the  motor  centres  in  the  suboesophageal  ganglion.  One  of 
the  main  functions  of  the  brain  is  thus  anticipated.  In  the  group  of  worms,  we  there- 
fore see  the  disappearance  of  peripheral  independence,  the 
establishment  of  central  control  and  the  beginning  of  cerebral 
dominance. 


THE    NERVOUS    SYSTEM    OF   ARTHROPODS 

THE   ARTHROPOD    NERVOUS   SYSTEM   is   bllilt  On  the 

same  plan  as  that  of  the  polychaete  worms.  In 
Crustaceans,  such  as  the  crayfish  {Astacus)  and  in 
Insects  there  is  a  bi-lobed  cerebral  ganglion  receiving 
sensory  nerves  from  the  eyes  and  the  first  two  antennae 
which  contain  the  organs  of  smell,  hearing,  taste  and 
equilibration  ;  this  connects  by  the  circum-oesophageal 
nerve-ring  with  the  fused  and  ganglionated  ventral 
nerve-cord  in  which  run  giant  fibres  as  well  as  asso- 
ciated neurones  (Fig.  686).  In  some  of  the  smaller 
Crustaceans  and  the  Onychophora  {Peripafus)  the  two 
nerve-cords  are  widely  separated.  On  the  other  hand, 
in  many  of  the  higher  Insects  such  as  flies  (Diptera) 
several  consecutive  ganglia  of  the  ventral  nerve-cord 
are  fused  (Figs.  687-91)  ;  in  crabs  (Decapoda),  sessile 
barnacles  (Cirripedia),  spiders  (Araneida)  and  bugs 
(Hemiptera)  the  fusion  is  complete  so  that  the 
ventral  ganglia  form  a  single  mass  (Figs.  688, 
691).  Moreover  the  higher  Crustaceans  and  Insects 
possess  a  simple  visceral  or  sympathetic  system  con- 
nected with  the  circum-oesophageal  ring,  which  passes 
backwards  on  the  alimentary  canal. 

The  optic  lobes  and  cerebral  ganglion  of  Arthropods 
are  illustrated  in  Figs.  692  to  696.  The  cerebral  ganglion 
consists  of  three  fused  segments  forming  one  mass  : 
(1)  the  PROTOCEREBRUM  or  optic  segment  forming  the 
greater  part  of  the  brain  and  receiving  nerves  from  the 
compound  eyes  and  ocelli,  (2)  the  deuterocerebrum 

derived  from  the  antennary  segment,  and  (3)  the  tritocerebrum  from  the 
third  segment  of  the  head  ^^•hich  supplies  the  region  of  the  mouth.  The 
whole  structure  contains  a  peripheral  layer  of  ganglion  cells  with  a  central 
mass  of  neuropile  containing  several  groups  of  associative  cells  forming  the 
CENTRAL  body,  the  PEDUNCULATE  BODIES  and  Other  smaller  accumulations 
of  cells  ;  these  are  comparatively  large  in  social  insects  and  are  generally 
regarded  as  regulating  behaviour. 


Fig.  686.— The  Ner- 
vous System  of  a 
Typical  Crusta- 
cean. 

CG,  cerebral  (supra- 
oesophageal)  ganglia  ; 
OR,  circum-CBsoiDha- 
geal  nerve  ring  ;  8 A, 
sternal  artery  running 
between  a  separation 
of  the  two  ventral 
nerve-cords  ;  SOG, 

sub-ojsojjhageal  gan- 
glion (consisting  of  6 
pairs  of  fused  ganglia); 
G,  a  pair  of  fused 
ganglia  of  the  ventral 
cord  (after  Thomson). 


522 


THE   EYE   IN  EVOLUTION 

Figs.  687  to  691. — The  Nervous  System  of  Insects. 


Fig.  687. 


Fig.  688. 


Fig.  687. — The  nervous  system  of  the  larval  stage  of  Lepidoptera  (caterpillar). 
Note  the  cerebral  (supra-oesophageal)  ganglia  connected  with  the  sub-oesophageal 
ganglion  by  the  circum-cesophageal  nerve  ring  and  the  chain  of  ganglia  of  the 
ventral  cord. 

Fig.  688. — The  nervous  system  of  Hemiptera  (water-bug).  The  ganglia  of  the 
ventral  cord  are  fused  into  one. 


Fig.  689. 


Fig.  690. 


Fig.  691. 


Figs.  689  to  691.^The  nervous  system  of  diptera,  showing  the  general  arrange- 
ment of  the  cerebral  and  sub-oesophageal  ganglia  closely  approximated  and  the 
thoracic  and  abdominal  ganglia  of  the  ventral  chain.  On  either  side  of  the  cerebral 
ganglion  the  enormous  optic  lobes  and  compound  eyes  project  laterally,  each  larger 
than  the  ganglion  itself  (modified  from  Lang). 

Fig.   689. — Chironornus,  with  three  thoracic  and  six  small  abdominal  ganglia. 

Fig.  690. — Tabanus,  with  one  (fused)  thoracic  ganglion  and  seven  abdominal 
ganglia  closely  approximated. 

Fig.  691. — Sarcophaga,  with  all  the  thoracic  and  abdominal  ganglia  of  the  ventral 
chain  united  in  one  mass. 


On  either  side  of  the  protocerebrum  there  emerge  the  relatively  enormous 
OPTIC  LOBES  contained  in  eye-stalks  which  bear  the  compound  eyes.  The 
reconstructed  eye-stalk  of  the  fresh-water  crayfish,  Cambarus,  is  seen  in 
Fig.  692  (Bernhards,  1916  ;  Welsh,  1941).  Herein  several  neuropile  masses 
form  opti     ianglia  ;   of  these,  as  a  general  rule  in  Crustaceans  and  Insects, 


GANGLIONIC  NERVOUS   SYSTEM 


523 


Figs.  692  and   693. — The  Right  Eye-stalk  of  the  Crayfish,  C am b arcs. 


OC,    OCj  ■  .  - 

Fig.    692. — The    dissected   eye-stalk,  with  the   cutk-ular  covering  and   the    sheath 
enveloping  the  optic  lobes  removed. 

F^,  fibre  tract  from  supra-oesophageal  ganglion  to  sinus  gland  ;  F^.,  fibre  tract 
from  medulla  terminalis  to  sinus  gland  ;  L,  lamina  ganglionaris  (optic  ganglion  I)  ; 
ME,  medulla  externa  (optic  ganglion  II)  ;  MI,  medulla  interna  (optic  ganglion  III)  ; 
MT,  medulla  terminalis  (optic  ganglion  IV)  ;  OC'i,  oculomotor  nerve  I  ;  0C.2, 
oculomotor  nerve  II  ;  SE,  supra-oesophageal  (cerebral)  ganglion  ;]  SG,  sinus  gland  ; 
XO,  x-organ  (J.  H.  Welsh,  J.  exp.  Zool.). 


__  / 


IV^ 


Fig.   693. — Section  through  the  ej'e-stalk. 

On  top  is  the  compound  eye  with  the  retinal  cells,  R,  at  the  proximal  end  of 
the  ommatidia.  The  sub-ocular" space,  S,  is  occupied  largely  by  pigment  and  between 
it  and  the  retinules  is  the  basement  membrane,  B.  Occupying  tlie  main  body  of 
the  stalk  are  the  four  optic  ganglia,  I  to  IV  (lamina  ganglionaris,  external  and 
internal  medulla^,  and  the  medulla  terminalis)  (Xorman  Ashton). 


524  THE   EYE   IN   EVOLUTION 

there  are  three — the  lamina  ganglionaris  (or  first  optic  ganghon),  the 
EXTERNAL  MEDULLA  (or  second  optic  gangHoii)  and  the  internal  medulla 
(or  third  optic  ganghon)  which  is  frequently  divided  into  two  or  more  parts. 
In  some  Decapods  there  are  two,  while  in  others,  as  the  crayfish,  Cambarus, 
there  are  four,  a  terminal  medulla  (or  fourth  optic  ganglion)  lying 
proximal  to  the  third.  The  fibres  from  the  visual  cells  of  the  compound 
eye  enter  the  first  optic  ganglion  directly  ;  between  the  ganglia  there  are 
two  well-marked  decussations  of  fibres,  and  from  the  proximal  ganglion  the 
afferent  fibres  enter  the  cerebral  ganglion  by  several  tracts  to  terminate  in 
the  primary  optic  association  areas,  particularly  the  pedunculate  body,  and 
to  decussate  over  to  the  opposite  side.  Removal  of  the  cellular  portion  of 
the  pedunculate  body  abolishes  certain  responses  to  light  (Bethe,  1897). 

From  the  ocelli  (when  they  are  present)  the  visual  fibres  end  in  a 
ganglion  just  proximal  to  the  eye  wherein  a  second  neurone  enters  the 
protocerebrum  and  after  making  connections  with  the  fibres  from  the  optic 
lobes,  seeks  the  visual  centres  (Fig.  696)^. 

From  the  optic  centres  fibres  pass  downwards  through  the  circum- 
oesophageal  commissures  into  the  thoracic  cord.  These  fibres  have  been 
divided  into  two  systems  by  Satija  (1957)  (Fig.  696)  :  several  ipsilateral 
fibre-tracts  pass  downwards  from  each  optic  ganglion  into  the  commissure 
on  the  same  side  while  a  single  large  fibre,  also  arising  from  each  optic 
ganglion,  crosses  in  the  midline  to  enter  the  contralateral  commissure.  On 
visual  stimulation  action  potentials  have  been  recorded  along  their  route 
(Parry,  1947  ;  Burtt  and  Catton,  1952-54)  and  they  presumably  link  up 
the  visual  stimuli  with  the  reflexes  mediated  by  the  nerve  cord. 

It  is  interesting  that  the  brain  of  Insects  is  large  in  those  with  the  more  complex 
behaviour  ;  thus  that  of  Dytiscus  is  1/400  of  the  body- volume,  of  the  bee  1/174 
(Wigglesworth,  1953).  Moreover,  the  size  of  the  visual  centres  varies  similarly  with 
the  degree  of  developinent  of  the  eyes.  In  Arachnids  and  Myriapods  with  simple 
eyes  the  visual  centres  are  some  0-3  to  2-8%  of  the  size  of  the  brain  ;  in  Crustaceans 
and  Insects  with  rudimentary  compound  eyes,  it  is  3  to  10%  ;  in  those  with  elaborate 
compound  eyes,  up  to  80%  (Hanstrom,  1928). 

It  is  noteworthy  that  synchronized  spontaneous  rhythms  resembling  those  of  the 
vertebrate  brain  have  been  found  in  the  ganglia  of  Arthropods  and  Molluscs,  indicating 
a  considerable  degree  of  coordination  and  a  high  level  of  excitability  in  the  constituent 
neurones. 2  This  type  of  activity,  it  will  be  remembered,  is  characteristic  of  integrative 
centres  and  absent  in  those  with  purely  distributive  and  sensory  functions. 

In  function,  the  cerebral  ganglion  of  Arthropods  plays  a  decisive  role 
in  the  animal's  conduct.     Apart  from  its  essential  purpose  as  a  receiving 

^  For  the  structure  of  the  nervous  system  of  Arthropods,  see  Cajal  (1918),  Snodgrass 
(1926),  Hanstrom  (1928-35),  Ehnbom  (1948)  ;  for  the  action-potentials  in  the  optic  ganglia 
on  stimulation  by  light,  see  Adrian  (1937)  in  the  water-beetle,  Dytiscus  :  Crescitelli  and  Jahn 
(1942),  Bernhard  (1942),  Burtt  and  Catton  (1956),  in  the  grasshopper,  Chortippus  ;  Antrum 
(1950),  Burtt  and  Catton  (1956),  in  the  blowfly,  CaUiphora  ;  and  Burtt  and  Catton  (1954-56), 
in  the  locust,  Locusta  niigratoria,  and  the  larva  of  the  dragon-fly,  Aeschna. 

^  The  '  ter-beetle,  Dytiscus — Adrian  (1937);  the  grasshopper,  Chortippus — Crescitelli 
and  Jahn  ;•_');  the  slug,  ^r('oZima.r— Bullock  (1945);  the  blowfly,  CaZ?i>/iom—Burkhardt 
(1954)  ;  the        jst,  Locusta  mi gr a toria— Burtt  and  Catton  (1956). 


GANGLIONIC  NERVOUS   SYSTEM 


625 


centre  for  optical  and  other  sensations  from  the  sense  organs  concentrated 
in  the  head,  it  acts  as  an  association  centre  and  exercises  an  important 
integrative,  particularly  inhibitory,  control  over  motor  activity  throughout 
the  body.  This  is  well  seen  in  ablation  experiments.  After  removal  of  this 
ganglion  either  in  Crustaceans  or  Insects,  spontaneous  locomotion  and 
coordinated  feeding  cease  but  local  segmental  reflexes  persist,  and  owing  to 
the  removal  of  inhibition  these  activities  tend  to  be  much  exaggerated, 
whether  they  control  reflex  movements,  locomotion  or  the  chromatophores. 
Section  of  one  circum-oesophageal  comiective  leads  to  unilateral  effects  and 
circus  movements  (Jordan,  1918  ;  Herter,  1931  ;  ten  Cate,  1931  ;  Prosser, 
1946).     This  inhibitory  action  of  the  cerebral  ganglion  over  the  ventral 

Figs.  694  to  695. — The  Optic  Lobes  and  Cerebral  Tracts  of  the  Insect. 


Fig.   694. — Vertical  section  through  the  head  of  a  bee. 

Showing,  centrally,  the  paired  protocerebnim  or  cerebral  ganglion,  underneath 
which  are  the  sub- oesophageal  ganglia.  Joining  the  compound  eye  wnth  the  central 
nervous  sj^steni  lie  the  optic  lobes  wherein  the  three  nuclei — the  lamina  ganglionaris 
externally,  the  external  medulla  and  internal  medulla  internally — are  well  differen- 
tiated (Xorman  Ashton). 


P  RO  T  O-C  £  R  E  B  R  U  M 


OPTIC        LOBE 


Fig.  695. — Scheme    of   the  visual    paths  from  the    eye  to    the  protocerebrum  in  a 

typical  insect. 

CE,  compound  eye,  from  which  nerve  fibres  go  directly  to  the  lamina  ganglionaris 
(optic  ganglion  I),  LG.  Thence  a  decussation  of  fibres,  the  external  chiasma,  EC,  leads 
to  the  external  medulla  (optic  ganglion  II),  EM.  Thence  a  third  relay  of  fibres,  the 
internal  chiasma,  IC,  leads  to  the  internal  medulla  (optic  ganglion  III),  IM,  which  may 
be  divided  into  two  parts.  Thence  filires  are  relajecl  to  the  optic  centres  in  the  cerebral 
ganglion — mainly  the  ojatic  tubercle,  OT,  and  the  pedunculate  body,  PB — as  well 
as  contributing  decussating  fibrt'S,  DF,  to  the  nuclei  of  the  other  side.  For  the 
descending  fibres,  see  Fig.  696. 


526 


THE   EYE   IN   EVOLUTION 


Fig.  696.- — Fkontal  Section  of  the  Cerebral  Ganglion  and  Optic  Lobes  of 

THE  Locust,  Locust  a. 

Showing  descending  tracts  to  the  nerve  cord  (reconstructed).  C,  central  body  ; 
CP,  corpora  pedunculata  ;  CV,  corpora  ventraha  ;  D,  deuterocerebrum  ;  DF, 
descending  tract  from  deuterocerebrum  ;  EF  and  EFX,  ipsilateral  and  contra- 
lateral fibres  from  optic  lobes  ;  LG,  lamina  ganglionaris  ;  ME,  external  medulla  ; 
MI,  internal  medulla  ;  ON,  ocellar  nerve  ;  PF  and  PFX,  ipsilateral  and  contra- 
lateral fibres  from  corpora  pedunculata  ;    TF,  descending  tract  from  tritocerebrum. 

With  the  incisions  indicated  by  numbered  black  pointers,  the  following  effects 
on  the  visual  responses  were  noted  :  1,  in  the  ventral  region  and  posterior  aspect  of  the 
optic  peduncle,  the  crossed  responses  were  abolished  ;  2,  on  the  dorsal  and  anterior 
aspect  of  the  optic  peduncle,  the  ipsilateral  responses  were  weaker  ;  3,  between  the 
two  halves  of  the  protocerebrum  ventrally,  the  crossed  responses  were  abolished  bi- 
laterally; 4,  between  the  two  halves  of  the  protocerebrum  dorsally,  no  effects  on  the 
visual  responses  were  found  (R.  C.  Satija,  J.  Physiol.). 


ganglia  was  well  demonstrated  by  Jordan  (1910)  who  showed  in  the  crab 
that  the  circus  movements  ceased  if  the  cut  end  of  the  connective  were 
electrically  stimulated. 

The  exaggeration  of  reflex  reactions  after  removal  of  the  cerebral  ganglion  is  seen 
in  the  elicitation  of  responses  to  stimuli  normally  vs^ithout  effect  and  the  continuation 
of  movements  (such  as  cleaning  movements  of  the  legs)  uninterruptedly  for  hours 
(Bethe,  1897  ;  Roeder,  1937  ;  and  others).  In  decapitated  females  of  Bomhyx, 
oviposition  can  be  induced  mechanically  before  mating  and  persists  until  all  the  eggs 
have  been  laid,  merely  by  pressing  the  ovipositor  (McCracken,  1907)  ;  the  same  type 
of  response  is  seen  in  the  stinging  reflex  of  the  bee  (v.  Buddenbrock,  1937).  In  the 
same  way  when  the  female  praying  mantis  devours  her  doomed  mate  head-first,  his 
copulatory  activity  increases  manyfold  in  violence  and  apparent  enthusiasm  when 
she  has  disposed  of  his  cerebral  and  sub-cesophageal  ganglia  (Roeder,  1935). 

The  .'  tivities  of  Arthropods  are  essentially  reflex  in  nature,  controlled 
with  ainaz     >;  precision  by  the  ganglionic  centres  ;    when  the  eye  of  the 


GANGLIONIC  NERVOUS   SYSTEM  527 

locust  is  stimulated  by  light,  for  example,  impulses  have  been  recorded  as 
far  caudally  as  the  last  thoracic  ganglion  (Burtt  and  Catton,  1952).  Never- 
theless, these  ganglia  do  not  act  merely  as  automatic  relay-stations.  As  we 
have  already  seen  ^  disturbances  of  the  normal  mechanism  of  locomotion  by 
the  amputation  of  a  limb  are  largely  corrected  by  suitable  alterations  in  the 
reflex  progression  (Bet he,  1930  ;  v.  Hoist,  1935  ;  ten  Gate,  1936  ;  and 
others).  Moreover,  within  the  nerve-cord,  the  available  connections  are 
multiple  and  after  experimental  interference  it  has  been  showTi  that  the 
choice  of  a  particular  pathway  depends  on  such  factors  as  the  strength  of 
stimulus  and  the  ease  of  transmission  (Prosser,  1935,  in  the  cra;yfish).  In 
view  of  the  complexity  of  the  instinctive  behaviour,  particularly  of  Insects, 
as  exemplified  in  the  complicated  social  behaviour  of  the  ant  or  the  dance 
of  the  honey-bee  by  which  it  indicates  to  its  fellows  the  location  of  a  honey- 
store,^  and  in  view  of  their  limited  but  very  definite  capacity  to  modify 
their  behaviour  by  learning  and  conditioning,  it  would  seem  that  the  gan- 
glionic organization  of  Arthropods  with  its  cerebral  dominance  has  reached 
a  very  high  level  indeed  of  integration.  It  must  be  remembered,  however, 
that  despite  their  complexity  and  seemingly  intelligent  basis,  these  complex 
patterns  of  behaviour  are  all  innate  and  their  performance  depends  on  the 
development  of  the  appropriate  parts  of  the  nervous  system  or,  in  the  case 
of  sexual  instincts,  on  the  development  of  hormones  at  a  somewhat  later 
stage  in  life.  Even  although  their  behaviovu"  does  seem  often  elaborate 
and  sometimes  full  of  intelligence,  however,  individual  adjustment  to  any 
peculiar  circumstances  is  relatively  unknown  in  their  totalitarian  lives  ; 
individuality  and  personality  cannot  be  attained  below  the  level  of  a  cen- 
tralized brain. 

THE    NERVOUS    SYSTEM    OF    MOLLUSCS 

In  MOLLUSCS  which  are  unsegmented  and  without  appendages,  the 
nervous  system  appears  to  be  different  but  nevertheless  is  basically  similar 
to  that  of  worms  and  Arthropods.  In  its  essentials  it  consists  of  paired 
dorsal  cephalic  ganglia  which  receive  sensory  fibres  from  the  eyes  and  other 
sense-organs  ;  these  ganglia  are  connected  by  a  short  circum-cesophageal 
nerve-ring  with  paired  pleural  and  pedal  ganglia.  Tj^ically,  as  an  offshoot 
from  this  bunched-up  ganglionated  ring  m  the  head-region,  a  stomato- 
gastric  loop  from  the  cerebral  ganglia  runs  below  the  gullet  bearing  two 
buccal  ganglia,  and  a  visceral  loop  provided  "wdth  visceral  ganglia  is  given 
off  from  the  pleurals  (Fig.  697).  In  some  types  the  ganglia  m  the  cephalic 
ring  are  separate  (Gastropods),  in  others  they  are  so  closely  associated  that 
some  appear  to  be  fused  (cerebro -pleural  in  Lamellibranchs),  while  in  Cephalo- 
pods  the  fusion  is  almost  complete.  In  these  last  the  three  pairs  of  ganglia  are 
crowded  into  the  head  region  around  the  oesophagus  so  closely  that  their 

1  p.  59.  *  p.  70. 


528 


THE   EYE   IN   EVOLUTION 


boundaries   are   appreciated  with   difficulty   (cerebral,   pedal   and   pleuro- 
visceral),  all  being  well  protected  by  investing  cartilages. 

In  the  Cephalopods,  the  sub -oesophageal  ganglionic  mass  contains  centres 
for  regulating  the  locomotor  and  visceral  activities  ;  here  lie  the  centres 
which  control  the  ocular  muscles,  the  pupil  and  the  chromatophores.  To 
the  supra-oesophageal  (cerebral)  ganglia  come  the  sensory  efFerents,  here  lie 
the  higher  motor  centres  controlling  movements  of  large  groups  of  muscles, 
and  here  also,  situated  in  the  upper  part  of  the  ganglion,  lies  a  large  associa- 
tive and  integrative  area,  ablation  of  which  does  not  impair  purely  reflex 


Fig.  697. — The  Nervous  System  of  a  Pulmonate  Mollusc,    Li  My  ^  a. 

A  pair  of  cerebral  ganglia,  C,  overlie  the  oesophagus,  below  which  is  a  mass  of 
ganglia  composed  of  2  pedal  ganglia,  P,  2  pleural,  PI,  and  2  parietal,  Pr,  while  ventrally 
in  the  centre  lies  the  visceral  ganglion,  V  (after  Spengel). 


activities  or  sensory  impressions  but  abolishes  initiative  in  behaviour  and 
plasticity  in  responses  ;  this  is  seen,  for  example,  in  such  reactions  as  chasing 
prey  round  blind  corners  or  in  attempting  expedients  to  escape  from  artificial 
restrictions  {Se2na,  Octopus — Buytendijk,  1933  ;  Sanders  and  Young,  1940). 
The  course  of  the  nerve-fibres  associated  with  vision  is  shown  in  Fig. 
698.1  The  axons  of  the  retinal  ganglion  cells  leave  the  eye,  decussate  in  the 
very  short  optic  nerve  and  enter  the  large  optic  lobes  situated  one  on  either 
side  of  the  paired  cerebral  ganglion  which  they  dominate  completely  by 
their  size.  Around  the  periphery  of  the  optic  lobe  run  two  layers  of  granular 
cells  separated  by  a  plexiform  layer  of  fibres,  while  in  the  centre  of  the  lobe 
are  two  nuclei,  a  central  and  a  peduncular  nucleus.  The  axons  of  the 
ganglion  cells  of  the  retina  enter  the  plexiform  layer  between  the  two 
granular  layers  and  here  they  meet  dendrites  of  these  cells  ;   the  pathway  is 


1  Foi 
Kappers  i 


anatomy  of  the  visual  fibres  of  Molluscs,  see  v.  Uexkiill  (1895),  Cajal  (1917), 
1936),  and  Sanders  and  Young  (1940). 


GANGLIONIC   NERVOUS   SYSTEM 
OPTIC    LOBE 


529 


OG 


Fig.    698. — Diagrammatic    Scheme    of   the   Visual   Paths   and   their  Central 
Connections  in  the  Cephaloiod   (after  Kajjpers). 

Axons  from  the  visual  cells  in  the  compound  eye,  a,  decussate  to  form  a  chiasma 
and  enter  the  optic  lobe,  terminating  in  the  plexiform  layer  between  the  inner,  IG, 
and  outer  granular  layers,  OG.  The  pathway  is  continued  by  axons  of  the  granular 
cells,  b,  sometimes  with  an  intercalated  neurone,  c,  to  the  central  and  pedunculate 
nuclei  of  the  optic  ganglion,  OGn.  Thence  a  further  relay,  rf'  to  (/*,  continues  the 
pathway  to  the  cerebral  ganglia  to  terminate  in  association  areas,  e,  and,  by  means 
of  commissural  fibres,  CF,  in  the  contralateral  oiDtic  lobe. 


continued  by  the  granular  cells,  sometimes  with  an  intercalated  neurone, 
to  a  central  mass  of  cells,  the  optic  ganglion,  consisting  mainly  of  a  central 
and  a  peduncular  nucleus  ;  from  this  a  fourth  relay  enters  the  cerebral 
ganglion  to  terminate  in  association  areas  anteriorly  and  posteriorly  and  to 
decussate  to  the  optic  lobe  on  the  other  side.  It  is  noteworthy  that  the 
large  and  complex  optic  lobes  (in  the  octopus)  serve  as  the  centres  for 
learning  to  attack  objects  that  provide  food,  a  demonstration  of  the 
effective  role  vision  plays  in  this  essential  activity  ;  thence  fibres  pass  to 
the  cerebral  ganglion  where  are  situated  the  cells  responsible  for  initiating 
attack-behaviour  (Young,  1953). 


Adrian.    J.  Physiol.,  91,  66  (1937). 
Antrum.     Z.  vergl.  Physiol,  32,  176  (1950). 
Bardeen.     Amer.  J.  Physiol.,  5,  175  (1901). 
Bernhard.    J.  Neurophysiol.,  5,  32  (1942). 
Bernhards.      Z.  uiss.   ZooL,  116,   649  (1916). 
Bethe.      Pflugers  Arch.  ges.  Physiol.,  68,  449 

(1897)  ;    224,  793,  821  (1930). 
Bovard.      Univ.   Calif.    Publ.    ZooL,   18,    103 

(1918). 
V.  Buddenbrock.     Grundriss  d.  vergl.  Physiol., 

Berlin,  2,  301  (1937). 
Bullock.    J.  Neurophysiol.,  8,  55  (1945). 

Yale  J.  Biol.  Med.,  17,  657  (1945). 
Burkhardt.     Z.  vergl.  Physiol.,  36,  595  (1954). 
Burtt  and  Catton.     Nature  (Lond.),  170,  285 

(1952). 
J.  Physiol.,  125,  566  (1954)  ;  133,  68  (1956). 

S.O.— VOL.  I. 


Buytendijk.      Arch,    neerl.    Physiol.,    18,    24 

(1933). 
Cajal.     Trab.  Lab.  Invest,  biol.  Univ.  Madrid, 

15,  1  (1917)  ;    16,  109  (1918). 
ten  Gate.     Ergebn.  Physiol.,  33,  137  (1931). 

Arch,  neerl.  PhysioL,  21,  562  (1936). 
Coonfield.    J.  comp.  Neurol.,  55,  7  (1932). 
Copeland.    J.  comp.  Psychol.,  10,  339  (1930). 
Copeland  and  Brown.      Biol.   Bull.,  67,   356 

(1934). 
Crescitelli  and  Jahn.     J.  cell.  comp.  Physiol., 

19,  47  (1942). 
Darwin.     The  Formation  of  Vegetable  Moulds 

through   the   Action    of    Worms,    London 

(1881). 
Day.    J.  exp.  ZooL,  28,  307  (1919). 
Eccles,  Granit  and  Young.     J.   Physiol.,  77, 

23P  (1933). 

34 


530 


THE   EYE   IN   EVOLUTION 


Eccles  and  Sherrington.     J .   Physiol.,  69,   1 

(1930). 
Eggers.     Z.  vergl.  Physiol,  1,  579  (1924). 
Ehnbom.      Opuscula  Entomol.,   Suppl.   VIII, 

Lund  (1948). 
Friedrich.     Zool.  Jb.,  Aht.  Zool.  Physiol.,  52, 

637  (1932). 
Hanstrom.      Vergl.   Anat.   des  N erven sy sterns 

der  wirbellosen  Tiere,  Berlin  (1928). 
Proc.  not.  Acad.  Set.,  21,  584  (1935). 
Kungl.  Fysiogr.  Sallsk.  Lund  Forhd.,  5,  156 

(1935). 
Heck.     Lotos  Naturw.  Z.,  Prag.,  67/68,   168 

(1920). 
Herter.     Z.  vergl.  Physiol,  14,  609  (1931). 
Hess,  W.  N.    J.  Morphol,  39,  515  (1924). 
V.  Hoist.     Biol.  Rev.,  10,  234  (1935). 
Howell.    J.  exp.  Zool,  81,  231  (1939). 
Janzen.     Zool.  Jb.,  Abt.  Zool.  Physiol,  50,  51 

(1931). 
Jordan.    P fingers  Arch.  ges.  Physiol,  131,  317 

(1910). 
Z.  allg.  Physiol,  17,  146  (1918). 
Just.     Z.  vergl  Physiol,  2,  155  (1924). 
Kappers,    Huber   and   Crosby.      Comparative 

Anat.  of  the  Nervous  System  oj  Vertebrates, 

including  Man,  N.Y.  (1936). 
Kinoshita.     Pflilgers  Arch.  ges.  Physiol,  134, 

501  (1910). 
Loeb.     Pfiugers  Arch.  ges.   Physiol,  56,  247 

(1894). 


McCracken.     J.   camp.  Neurol.   Psychol.,  17, 

262  (1907). 
Maxwell.    Pfiugers  Arch.  ges.  Physiol.,  67,  263 

(1897). 
Nomura.     Tohoku  Imp.  Univ.  Sci.  Rep.,  Sec. 

4,  1,  294  (1926)  ;    2,  1  (1927). 
Prosser.    J.  camp.  Neurol,  59,  61  (1934)  ;   62, 

495  (1935). 
Quart.  Rev.  Biol,  9,  181  (1934). 
J.  exp.  Biol,  12,  95  (1935). 
Physiol.  Rev.,  26,  337  (1946). 
Comparative    Aniinal    Physiology,    London 

(1950). 
Rietschel.     Zool.  Anz.,  Ill,  109  (1935). 
Roeder.     Biol.  Bull,  69,  203  (1935). 

J.  exp.  Zool,  76,  353  (1937). 
Sanders  and  Young.    J.  Neurophysiol,  3,  501 

(1940). 
Smallwood  and  Holmes.    J.  conip.  Neurol,  43, 

327  (1927). 
Snodgrass.    Smithsonian  Misc.  Coll.,  11,  No.  8 

(1926). 
Stough.     J.   comp.  Neurol,  40,  409   (1926)  ; 

50,  217  (1930). 
Swartz.    J.  comp.  Psychol,  9,  17  (1929). 
V.  Uexkull.     Z.  Biol,  31,  584  (1895), 

Ergebn.  Physiol,  3,  1  (1904). 
Welsh.    J.  exp.  Zool,  86,  35  (1941). 
Wigglesworth.        The     Principles     of    Insect 

Physiology,  London  (1953). 
Young.      Proc.    XIX    int.    physiol    Congr., 

Montreal,  p.  99  (1953). 


THE  CENTRAL  NERVOUS  SYSTEM 

A  central  nervous  system  is  characteristic  of  the  Chordates  which  possess 
a  brain  and  dorsal  nerve-cord  replacing  the  cerebral  ganglion  and  the 
ventral  cord  of  the  Invertebrates,  the  whole  being  initially  supported  by  a 
notochord  and  eventually  encased  in  a  protective  bony  skull  and  vertebral 
colunui.  In  the  Proto- chordates,  however,  the  nervous  system  is  exceed- 
ingly primitive. 

We  have  already  seen  ^  that  in  the  hemichordates  {Balanoglossus)  the  nervous 
system  is  essentially  a  peripheral  nerve-net  centred  round  a  dorsal  nerve-cord  arising 
as  a  longitudinal  groove  of  ectoderm  connected  by  a  band  around  the  collar  of  the 
animal  with  a  ventral  nerve.  There  is  as  yet  no  evidence  of  a  brain.  In  larval 
TUNicATES  there  is  a  poorly  developed  ganglionic  brain  connected  with  the  median  eye 
and  continued  in  a  dorsal  nerve-cord  -  ;  but  in  the  sessile  advxlt  Ascidian  the  nervous 
system  recedes  until  it  is  represented  merely  by  a  single  ganglionic  mass  from  which 
a  few  short  nerve -filaments  ennerge.^  In  the  acrania,  the  brain  of  Arnphioxus 
{Branchiostoma)  is  almost  undeveloped  and  is  represented  by  a  small  cerebral  vesicle, 
but  the  dorsal  cord  with  its  central  canal  is  well  formed  and  sends  off  two  anterior 
cerebral  nerves  and  a  pair  of  segmental  nerves,  dorsal  and  ventral,  to  each  myotome 
(Fig.  236). 

Among  VERTEBRATES  the  central  nervous  system  attains  a  structural 
compl(  ^-'ty  and  functional  coordination  unparalleled  in  the  animal  kingdom, 
1  p.  227.  2  p.  228.  3  p_  228. 


CENTRAL  NERVOUS  SYSTEM 


531 


until  eventually  it  acquires  a  plasticity  and  adaptability  sufficient  to  form 
a  structural  basis  for  the  physical  dexterity  and  intellectual  supremacy  of 
man.  In  contrast  with  the  types  of  nervous  s^^stem  we  have  just  discussed, 
the  activities  of  which  are  expressed  in  simple  and  immediate  reflexes 
concerned  with  the  ready  transformation  of  afferent  impulses  into  somewhat 
stereotyped  responses,  it  makes  provision  to  an  increasing  degree  for  the 
appreciation  of  broadly  correlated  sensory  patterns,  for  individual  adjust- 

FiGS.  699  TO  702. — The  Evolution  of  the  Bkain  of  Vertebrates. 


Fig.  700.— The  stage 
of  three  primary 
cerebral  vesicles. 


Fig.  701.— The  stage 
of  five  cerebral 
vesicles. 


Fig.  702.— The  final 
division  of  the 
telencephalon. 


Fig.  699.— The  ini- 
tial archencepha- 
lon  ;  a  vesicular- 
shaped  swelling  at 
the  ujjper  end  of 
the  medullary 

tube. 

The  fore-brain  and  its  derivatives  are  dotted  ;  the  mid-brain  is  in  solid  black  ; 
the  hind-brain  is  cross-hatched. 

CB,  cerebellum  ;  CH,  cerebral  hemispheres  ;  CS,  corpus  striatum  ;  DE, 
diencephalon  ;  FB,  fore-brain  (prosencephalon)  ;  HB,  hind-brain  (rhombence- 
phalon), divided  into  metencephalon  and  myelencephalon  in  Figs.  701-2  ;  MB,  mid- 
brain (mesencephalon)  ;  MO,  medulla  oblongata  ;  OL,  olfactory  lobe  ;  OT,  optic 
thalamus;  OV,  vesicle  which  becomes  the  iter  or  aqueduct  of  Sylvius:  TE.  telen- 
cephalon ;  I,  II,  III  and  IV,  ventricles. 


ments  in  response  and  eventually  for  the  emergence  of  thought  and  per- 
sonality. Within  the  Vertebrates,  however,  this  process  of  evolution  was 
slow  but  conformed  to  a  general  plan  whereby  the  reflex  mechanism  in  the 
lower  levels  became  gradually  subordinated  to  the  controlling  and  integrating 
influence  of  a  cerebral  cortex.  In  the  process,  changes  affecting  the  central 
visual  mechanism  played  a  predominating  part,  and  the  gradual  transference 
of  the  sensory  activities  of  vision  to  the  highest  level,  leaving  the  reflex 
photostatic  functions  at  a  lower  level,  formed  the  pivot  around  which  the 
nervous  system  of  the  higher  Vertebrates  eventually  became  reorganized. 

As  in  the  lower  C'hordates,  the  central  nervous  system  of  Vertebrates  is 
formed  from  the  dorsal  ectoderm  by  the  infolding  of  the  medullary  groove 


FORE-BRAIN 


532  THE   EYE   IN   EVOLUTION 

to  form  an  ectodermal  tube  enclosing  an  axial  canal, ^  the  anterior  end  of 
which  dilates  markedly  to  form  the  brain  while  the  remainder  forms  the 
segmented  dorsal  spinal  cord  ;  the  latter  acts  as  a  reflex  centre,  while  in 
addition  to  this,  the  former  assumes  controlling  and  integrating  functions 
of  ever-increasing  importance  so  that  as  evolution  proceeds  the  entire 
mechanism  shows  a  progressive  degree  of  cephalization. 

At  an  early  period  the  embryonic  cerebral  vesicle  shows  two  constric- 
tions dividing  it  into  three  primary  bulb-like  vesicles — the  fore-brain 
(prosencephalon),  the  mid -brain  (mesencephalon)  and  the  hind -brain 
(rhombencephalon)  (Figs.  699  to  709).  During  the  course  of  vertebrate 
evolution  these  three  primary  vesicles  differentiate  as  follows  : 

'TELENCEPHALON — olfactoiy  lobes,  cerebral  cortex  (pallivim),  basal 

nuclei  of  the  corpus  striatvun. 
DiENCEPHALON — thalamus,  epithalamus,  hypothalamus,  ejDiphysis, 
hypophysis. 

Tectum  (and  optic  lobes  or,  in  Mammals,  corpora 
MID -BRAIN  c^uadrigemina),  tegmentvim   (and,   in  Mammals, 

cerebral  peduncles). 

{METENCEPHALON — cerebclKun  and  part  of  medulla  oblongata   (in 
Mammals,  the  pons). 
MYELENCEPHALON — remainder  of  the  medulla  oblongata. 

In  some  fishes  this  division  into  five  main  segments  is  maintained,  but  in 
most  Vertebrates  the  telencephalon  grows  out  into  two  paired  lobes  (the 
cerebral   hemispheres),   each  containing  the  cavity  of  a  lateral  ventricle 

(Fig.  702). 

It  is  interesting  that  in  Cyclostomes  the  histological  structure  of  the  central 
nervous  system  is  extremely  primitive  and  its  organization  allows  for  the  most 
part  only  total  movements  of  the  whole  body  (mass  reflexes)  rather  than  complex 
adjustments  involving  precise  coordination.  It  is  thus  unspecialized,  j^lastic  and 
capable  of  differentiation  in  any  direction — a  very  suitable  primordial  ancestor  for 
the  Vertebrates  (Herrick,  1921).  The  central  nervous  systems  of  selachian  and 
teleostean  Fishes,  on  the  other  hand,  show  systems  of  nuclei  and  fibre-tracts  as  well 
defined  as  those  of  Mammals  ;  they  are  precisely  adapted  on  a  reflex  plane  to  a 
particular  environment,  and  although  they  are  thus  able  completely  to  dominate  this 
habitat,  their  central  nervous  systems  are  less  capable  of  free  adjustment  to  other 
conditions.  They  therefore  form  terminal  branches  of  the  phylogenetic  tree.^  The 
ancestors  of  the  Amphibians  were  the  more  primitive  Crossopterygii,  nearly  related  to 
which  are  the  lung-fishes  (Dipnoi).  Their  more  plastic  central  nervous  system  and 
the  more  complete  evagination  of  the  fore-brain  into  cerebral  vesicles,  particularly 
at  the  caudal  rather  than  the  olfactory  end,  allowed  them  to  become  adapted  to  the 
lessened  oxygen  supply  in  stagnant  swamps  and  ultimately  to  emerge  on  land.  On 
this  relatively  primitive  fish-brain  further  evolution  was  therefore  based. 

We  shall  now  outline  the  main  evolutionary  changes  in  the  development 
of  the  h'lin  of  Vertebrates  with  particular  reference  to  their  visual  systems 
(Figs.  7  =  ^    to  715). 

1  p.  239.  2  p.  234. 


CENTRAL  NERVOUS  SYSTEM 


533 


Figs.  703  to  709. — The  Brains  of  Vertebrates 
(after  Biitschli,  Gaupp,  Crosby,  Clark,  Kuenzi  and  Sisson). 


Fig.  703.— a  Cyclo- 
s'tome  :  the  lam- 
prey,   Petromyzon. 


Fig.  704.— a  Sela- 
chian :  the  shark, 
Scymnus. 


Fig.  705. — An  Am- 
phibian :  the  frog, 
Rana. 


Fig.     706.— a     Rep- 
tile :    the  alligator. 


Fig.      707. — A     Bird:       the      Fig.  708. — A  lower  Mammal  :      Fig.    709. — A    higher    Mam- 
goose,  Ayiser.  the  Insectivore,  Gymnura.  mal  :    tlie  horse,  Equus. 

C,  cerebrum  ;  Cb,  cerebellum  ;  D,  diencephalon  ;  MO,  medulla  oblongata  ; 
OB,  olfactory  bulb  ;  OL,  optic  lobe  ;  01. L,  olfactory  lobe  ;  P,  pineal  complex  ; 
Q,  corjjora  cjuadrigemina  ;  F,  ventricle  of  mid-brain  ;  V^,  third  ventricle  ;  V^, 
fourth  ventricle. 


The  hind-brcmi  essentially  continues  the  segmental  functions  of  the 
cord,  acting  as  a  reflex  centre  for  most  of  the  head-region  through  the  cranial 
nerves,  both  sensory  and  motor,  but  in  addition  it  assumes  integrating 
functions  for  such  general  autonomic  activities  as  circulation  and  respiration 
and  the  control  of  equilibration  and  posture.  The  last  is  subserved  by 
vestibular  centres  upon  which  the  cerebellum  is  built  as  an  integrating  centre, 
linking  up  the  vestibular  centres  with  the  sensory  organs  mediating  these 


534  THE   EYE   IN   EVOLUTION 

functions  (the  lateral  lines  ^  and  labyrinths  ^)  and  associating  them  with 
fibres  from  the  cord  and  the  mid-brain,  many  of  which  are  derived  from  the 
ocular  muscles.  In  addition,  in  all  Vertebrates  the  hind-brain  receives  the 
receptors  of  taste,  and  in  the  higher  Vertebrates  from  Amphibia  upwards, 
the  auditory  nerves.  The  cochlea,  which  makes  its  appearance  first  in 
Amphibia  and  is  attuned  to  respond  to  the  vibrations  of  the  new  medium 
(air),  belongs  to  the  same  system  of  vibratory  sense-organs  as  the  lateral 
line  and  labyrinth.^ 

Initially  the  postural  mechanism  of  the  hind-brain  was  relatively  self-svifficient  ; 
thus  after  transection  of  the  brain  cephalad  to  the  hind-brain,  Cyclostomes,  Fishes 
and  Amphibians  retain  their  locomotor  functions,  while  in  these  animals  the  cerebellum 
is  but  poorly  developed.  In  Reptiles,  Deiters'  nucleus  first  becomes  important  in 
immediate  relation  with  the  vestibular  system,  and  in  Birds  and  Mammals,  the 
integrating  and  inhibitory  functions  of  the  higher  centres  become  so  overwhelming 
that  transection  at  this  level  results  in  decerebrate  rigidity  so  that  independent 
locomotion  becomes  impossible,  while  ablation  of  the  cerebellum  results  in  the  complete 
breakdown  of  equilibration. 

The  mid-brain  contains  the  visual  and  oculomotor  centres  in  the  lower 
Vertebrates  and  acquires  auditory  centres  in  the  higher  ;  it  also  acts  as  an 
integrating  centre  for  proprioceptive  and  exteroceptive  impulses,  linking 
them  by  means  of  elaborate  connections  with  the  hind-brain  and  cerebellum 
and  in  an  ever-increasing  degree  with  the  higher  centres.  The  roof  of  the 
mid-brain  (the  tectum)  has  undergone  profound  changes  in  evolution  (Figs. 
710  to  715).  Originally  it  received  all  the  afferent  fibres  from  the  eyes 
which  were  primarily  photostatic.  In  Cyclostomes  the  tectum  is  rudimen- 
tary and  most  of  the  incoming  fibres  are  visual ;  from  it  issue  tecto-bulbar 
tracts  which  bring  the  movements  of  the  animal  under  the  control  of  optic 
and  other  sensory  impulses  (Fig.  710).  In  Fishes  this  region  becomes 
enormously  expanded  to  form  the  two  optic  lobes,  and  in  addition  to 
optic  fibres,  it  receives  spino-tectal  fibres  conveying  sensory  impulses  from 
the  body,  head  and  neck.  In  these  animals  the  tectum  thus  serves  not  only 
as  the  visual  centre  but  acts  as  the  coordinating  station  for  many  motor 
and  other  sensory  activities.  In  Amphibians,  the  differentiation  of  a  system 
of  receptors  for  the  cochlea  leads  to  the  appearance  of  two  separate  centres 
on  each  side,  one  for  the  eye  and  one  for  the  ear  :  the  bigeminal  body  becomes 
the  quadrigeminal.  In  the  higher  Vertebrates,  the  optic  lobes  are  thus 
divided  into  four  (the  corpora  quadrigemina)  and  while  the  anterior  paired 
bodies   (superior  colliculi)  receive  visual,   the  posterior   (inferior  colliculi) 

1  Present  in  aquatic  \'ertebrate.s — Cyclosto:ne.s,  Fishes,  all  urodele  and  larval  anuran 
Amphibians  ;   when  Vertebrates  left  the  water  for  the  land  the  lateral  line  disappeared. 

^  Present  in  all  Vertebrates.  In  Myxinoids  there  is  one  semicircular  canal,  in  other 
Cyclostomes.  two  (anterior  and  posterior),  in  other  Vertebrates,  three  (anterior,  posterior  and 
external).  The  free  opening  of  the  labyrinth  in  some  selachian  fishes  (dog-fish,  Acanthias  ; 
skate,  lio       indicates  the  analogy  to  lateral  line  organs. 

'  The  fulus  and  papilla  lagtenae  of  fishes  may  be  sensitive  to  auditory  vibrations 
(Piper,  19(M       Parker,  1903-12). 


CENTRAL  NERVOUS  SYSTEM 


535 


receive  auditory  afferents.  In  Reptiles  such  as  the  hzard  this  area  is  thus 
an  elaborate  structure  resembling  that  of  Birds  ;  in  the  latter  the  tectal 
region  reaches  its  highest  peak  of  development  and  the  superior  colliculi 
themselves  have  attained  the  importance  of  optic  lobes  with  a  cortex,  generally 
accepted  as  being  arranged  in  six  layers  of  nerve  cells  and  fibres  (C'ajal, 
1889  ;  Huber  and  Crosby,  1929  ;  Jungherr.  1945;  Shirasu,  1953).  The  first 
(the  stratum  zonale)  is  a  thin  layer  of  flat  small  cells  ;  into  the  second  (the 
stratum  opticum)  the  optic  fibres  arrive  to  terminate  in  the  third  (the 
stratum  griseum),  itself  divided  into  seven  layers  ;  the  remaining  layers  are 
concerned  with  the  cells  and  fibres  which  form  the  efferent  tracts  from  the 


>'er\p  II    — — 


TECTUM 


Brachium  terti 


.Nerve  VIII 

Xerve  V 

Post,  root  ganglia 


Fig.  710. — The  Visual  Pathways  in  a  Typical  Cyclostome. 


tectum.  In  Mammals,  however,  the  importance  of  the  optic  lobes  begins 
to  decline  ;  the  sensory  fibres  are  relayed  to  a  more  plastic  end-station  in 
the  cerebral  cortex  and  the  tectum  eventually  receives  only  the  fibres 
associated  with  the  primitive  photostatic  functions  of  vision. 

The  ventral  portion  of  the  mid-brain  (the  tegmentum)  contains  the  oculomotor 
nuclei  and  in  the  higher  Vertebrates  is  concerned  to  an  ever-increasing  degree  with 
the  integration  of  fibre-systems  from  the  general  proprioceptive  system  and  the 
octavus  (Vlllth  nerve)  system  with  the  higher  centres,  a  function  which,  in  Reptiles 
and  above,  is  centred  in  the  upper  part  of  the  mid-brain  ;  transection  at  the  level 
of  the  red  nucleus  in  Mammals  thus  leads  to  decerebrate  rigidity. 

In  the  lower  Vertebrates  (Cyclostomes.  Fishes  and  Amphibians)  the 
mid-brain  is  thus  the  region  of  the  highest  integration  of  their  sensory  and 
motor  activities  (apart  from  smell)  and  controls  the  most  complex  behaviour 
of  these  animals  ;  for  this  reason  electrical  stimulation  leads  to  coordinated 
movements  much  as  does  stimulation  of  the  cortex  of  Mammals.     In  Birds 


536 


THE   EYE   IN   EVOLUTION 


the  dorsal  area  of  the  mid-brain  assumes  immense  importance  as  a  correlating 
centre  for  sensory,  gravistatic  and  photostatic  impulses  ;  the  fact  that  these 
correlations  still  take  place  at  this  level  reflects  the  essentially  reflex  and 
instinctive  nature  of  these  animals  with  their  poor  adaptability  and  lack 
of  potentiality  for  further  evolution.  In  Mammals,  however,  the  tectum 
fails  to  meet  the  demands  of  complex  visual  differentiations  and  pluri- 
sensory  combinations,  a  shift  upwards  of  the  sensory  centres  to  a  higher  level 
of  greater  plasticity  is  necessitated,  and  this  region  merely  retains  the  regu- 
lation   of  restricted   photostatic  and  other  activities.     In  Mammals  the 


Nerve  II    —  j 


Brachiuni  tecti    __._AX— -4 


Lat.  geniculate  body   ______ 


TECTUM 

Isthmo-tectal  tract 

Nucleus  lentiformis 

Torus  seniicircularis 

Ganglion  Isthmi 


Lat.  lemniscus 


Nerve  VIII 

Nerve  V 

"Post,  root  ganglia 


Fig.   711. — The  Visual  Pathways  in  a  Teleostean  Fish. 


anterior  colliculi  and  tectum  are  therefore  much  reduced  owing  to  the 
diversion  of  the  mass  of  optic  fibres  to  the  lateral  geniculate  body.  In  the 
same  manner,  in  the  quest  for  more  ample  and  effectual  sensory  associations, 
the  inferior  colliculi  cease  to  be  an  end-station  for  hearing  and  serve  merely 
as  a  relay-station  to  the  cerebral  cortex,  but  nevertheless  they  retain 
considerable  importance  in  gravistasis  as  the  main  end-station  of  the  lateral 
lemniscus  (Nerve  VIII)  and  the  spino-  and  bulbo-mesencephalic  fibres. 

Destruction  of  the  optic  lobes  in  Fish  and  Amphibia  is  said  to  leave  the  vision 
normal  provided  the  rest  of  the  mid-brain  is  intact  (Loeser,  1905)  ;  but  in  Birds, 
removal  of  the  colliculi  disturbs  visual  reflexes  and  produces  virtual  blindness  (Marquis, 
1935).  On  the  other  hand,  in  Mammals  in  which  the  visvxal  fibres  are  relayed  to  the 
cortex,  lesions  of  the  colliculi  or  tectum  give  rise  to  no  observable  visual  defect  (rabbit, 
rat — Ghisolii,  1937)  ;  such  a  lesion,  moreover,  does  not  affect  the  pupillary  reflexes 
which  are  •  iitred  in  the  pretectal  area  (cat — Keller  and  Stewart,  1932  ;  Magoun, 
1935). 


CENTRAL  NERVOUS  SYSTEM 


537 


The  diencephalon,  where  the  central  canal  persists  as  the  third  ventricle, 
has  peculiar  visual  and  secretory  functions  in  addition  to  the  important 
integrative  activities  of  the  optic  thalamus.  From  its  ventro -lateral  aspects 
in  the  embryo  the  primary  optic  vesicles  which  form  the  lateral  eyes 
emerge  as  out-pouchings,  and  it  is  interesting  that  in  many  sjjecies  there 
is  evidence  that  the  cells  of  this  region,  particularly  those  of  the  ependyma 
lining  the  ventricle,  appear  to  retain  some  photosensory  functions. 


Thalamo-striatal  tract  ~"~ 


Xerve  II   -  — _ 
Brachiuin  tecti 


Lat.  geniculatL'  body 
Nucleus  dorsalis  (liffusus 


TECTUM 


Nucleus  dcirsalis  ant. 
Isthmo-tectal  tract 
Torus  seniicircularis 


l.iantrlion  isthnii 


Lat.  lemniscus 


Nerve  VIII 

Nerve  V 

Tost,  root  ganglia 


Fig.   71: 


-The  Visual  Pathways  ix  a  Typical  A.mphibiax. 


This  direct  photosensitivity  of  the  central  nervous  system,  especially  the 
diencephalon,  has  been  established  in  experiments  on  the  action  of  light  upon 
gonadotropic  activities  ^  and  changes  in  the  chromatophores  of  the  integument  in 
a  niunber  of  .species  by  several  workers,  notable  among  whom  are  von  Frisch  (1911) 
(fish),  Scharrer  (1928)  (minnow),  Nowikoff  (1934),  Young  (1935)  (lamprey),  and  Benoit 
(1937)  (ducks).  We  have  already  seen  that  Benoit  and  his  collaborators  (1952-53) 
showed  that  the  direct  stimulation  of  this  region  by  light  enhances  the  gonadotropic 
activity  of  ducks  from  which  both  eyes  had  been  removed  ;  and  Parker  and  his 
colleagues  (1952)  have  pointed  out  that  the  central  nervous  systein  of  most  Birds  and 
Mammals  contains  a  coproporphyrin  pigment  wath  absorptive  properties  which  could 
account  for  this  direct  photosensory  response. 

The  secretory  activities  of  the  diencephalon  are  equally  important.- 
From  its  thin  roof  which  consists  merely  of  a  single  layer  of  ependymal 

'■  p.  16.  ^  p.  .558. 


538 


THE   EYE   IN   EVOLUTION 


cells  reinforced  by  the  choroidal  plexus,  is  given  off  the  pineal  and  in  some 
Vertebrates  (Cyclostomes,  some  Fish  and  Reptiles)  the  parietal  organs  ; 
in  some  lower  Vertebrates  these  have  an  optical  function  but  in  the  higher 
types  the  pineal  body  has  only  a  glandular  function. ^  From  the  floor  a 
ventral  process,  the  infundibulum,  grows  in  front  of  the  anterior  extremity 
of  the  notochord  to  meet  a  diverticulum  from  the  pharynx  to  form  the  pitui- 
tary gland  (or  hypophysis),  and  with  it  are  associated  a  number  of  nuclei 
of  neuro-secretory  cells  which  not  only  control  the  potent  endocrine  products 


A'rostriatvim 

Thalanin-striatal  tract 

Thalamus 

Ventral  thalamic  nucleus 

TECTUM 


Nerve  I   -"~ 


Lat.  geniculate  body 
Brachium  tecti 


Torus  semicircularis 
Ganglion  islhmi 


Lat.  lemniscus 


VI  n.     Cochlear 

1 Vni.     Vestib. 


Nerve  V 


Post,  root  ganglia 


Fig.  713. — -The  Visual  Pathways  in  a  Typical  Reptile. 


of  the  pituitary  but,  through  it,  exercise  a  governing  influence  over  most 
of  the  endocrine  system. ^ 

The  OPTIC  THALAMUS  when  fully  developed  is  a  region  of  great  integrative 
importance.  Its  more  dorsal  nuclei  are  concerned  with  widespread  somatic 
sensory  functions,  the  special  senses  and  associative  sensory  functions.  In 
Vertebrates  below  Mammalia  it  is  the  part  of  the  brain  which  is  responsible 
for  the  affective  appreciation  of  experience  and  therefore,  in  the  last  resort, 
it  determines  behaviour  ;  the  cerebral  hemispheres  merely  form  the  receptive 
apparatvis  for  olfactory  impressions.  In  Mammals  it  is  the  principal  end- 
station  tor  all  the  sensory  systems  of  the  body  with  the  exception  of  the 
olfactorv      ojections  which  proceed  directly  to  the  cerebral  cortex.    In  these 


p.  716. 


p.  558. 


CENTRAL  NERVOUS  SYSTEM 


539 


animals  (dog,  etc.)  ablation  of  the  thalamus  leads  to  immediate  blindness 
which,  however,  is  soon  replaced  by  psychical  blindness  only  (Panizza, 
1855)  ;  this  demonstrates  that  a  function  resembling  that  of  the  cerebral 
cortex  is  still  to  some  extent  retained.  In  man  its  connections  are  of  an 
extremely  intricate  kind  since  it  forms  the  main  relay-station  of  all  the 
tracts  spreading  upwards  towards  the  cortex.  Those  parts  which  are 
concerned  particularly  with  the  special  senses  are  the  lateral  geniculate 


Neive  II 
Spiriform  nucleus 


Basal  optic  ganglion 
Brachium  tectl 

Lat.  geniculate  body 


Xeotriatuni 
Thalanio-cortical  tract 


Thalamus 
Nucleus  rotundus 


TECTUM 


Nucleus  lat.  mesencephali 
(torus) 

Ganglion  isthmi 
Nucleus  semilunaris 


Lat.  lemniscus 


VIII.     Cochlear 
VIII.     Vestib. 

Nerve  V 

Post,  root  ganglia 


FiCx.   714. — The  Visual  Pathw.\ys  in  a  Typical  Bikd. 


bodies  (vision)  and  the  medial  geniculate  bodies  (audition  and  possibly 
ec{uilil)ration)  while  the  pulvinar  has  indirect  visual  and  auditory  associations. 

The  ventral  part  of  the  diencephalon  is  occupied  by  the  hypothalamus,  a 
collection  of  nuclei  with  rich  intra-diencephalic  connections  which  in  the 
higher  Vertebrates  are  concerned  with  cardiac  acceleration,  elevation  of  the 
blood  pressure,  the  maintenance  of  the  intra-ocular  pressure,  pupillary 
dilatation,  retraction  of  the  nictitating  membrane,  pilo-erection,  and 
inhibition  of  the  gut,  as  well  as  such  vegetative  functions  as  the  regulation 
of  temperature,  water,  fat  and  carbohydrate  metabolism,  sleep  and  sexual 
activity. 

The  optic  thalamus  and  its  associated  nuclei  are  primitive  in  Cyclo- 
stomes,  being  chiefly  concerned  with  olfactory,  visual  and  visceral  sensory 


540 


THE   EYE   IN  EVOLUTION 


functions.  The  same  pattern  is  retained  in  Fishes  in  which  it  has  still  no 
frontal  connections.  In  Amphibians  there  are  no  fibres  from  the  fore-brain 
to  the  thalamus  but  the  earliest  phylogenetic  evidence  of  cortical  projection 
occurs  in  a  thalamo-cortical  tract  to  the  secondary  olfactory  cortex,  a  relay 
increased  in  Reptiles  in  which  the  dorsal  thalamus  is  large  and  highly 
differentiated.    In  Birds  the  sensory  thalamic  nuclei  for  the  first  time  send 

y^-— —  Visual  cortex 

;,————  — — .  Angular  gyrus 

-———  Optic  radiations 
Sensory  cortex  -  — —  — -vj  V-  — ^___  Thalamo-cortical  tract 

Sensory  tract  - 


Xerve  II  — — — ^ 


Lat.  geniculate  body{^.^°[^^{  I1~11"' 

Brachium  tecti  --  —  —  —  —  —  —  —' 

Med.  geniculate  body  ____, 
(gang,  isthitii) 


Superior  colliculus  (tectum) 


Inferior  colliculus  (torus) 


Lat.  lemniscus 


VIII.     Cochlear 

J Vlll.     Vestib. 

-  Xerve  V 

—  Post,  root  ganglia 


Fig.  71.5. — The  Visual  Pathways  in  a  Typical  Mammal. 


a  rich  supply  of  axons  to  the  frontal  and  occipital  areas  of  the  neopallium. 
In  Mammals  the  thalamus,  especially  its  dorsal  portion,  becomes  of  extreme 
importance,  being  the  chief  integrating  centre  for  common  sensitivity  as 
well  as  for  sensation;  all  the  thalamic  nuclei  send  copious  relays  of  fibres 
to  the  cortex  and  receive  cortical  efferents  equally  copiously,  many  of  them 
inhibitory  in  type. 

The  correlation  of  sensory  and  reflex  activities  in  the  thalamic  region 
of  the  diencephalon  still  requires  much  further  clarification,  but  it  is  apparent 
that  whi!<  he  coordination  of  the  relatively  simple  movements  of  the  lower 
Vertebral      i  akes  place  in  the  hind-  and  mid-brain,  the  thalamus  assumes 


CENTRAL  NERVOUS  SYSTEM  541 

responsibility  for  the  integration  of  the  very  complex  patterns  of  instinctive 
behaviour  characteristic  of  the  higher  Vertebrates. 

This  is  made  clear  by  the  researches  of  Briigger  (1943),  Hess  and  Briigger  (1943) 
and  Hess  (1943-44).  Probing  the  hypothalamic  region  of  cats  with  electrodes,  they 
found  areas  where  the  stimulus  elicited  complex  patterns  of  behaviour  in  their  entirety, 
such  as  fighting,  eating  and  sleeping,  all  displayed  in  perfect  coordination.  Thus 
the  cat  looked  around,  searched  for  a  suitable  corner  in  which  to  go  to  sleep,  and 
forthwith  went  to  sleep  ;  presumably  felt  hvmgry,  searched  for  food,  ate  the  food, 
rested,  and  so  on.  Here,  therefore,  lie  the  anatomical  bases  of  the  centres  controlling 
the  highest  instinctive  patterns,  set  between  the  receptors  and  effectors,  combining 
and  assessing  incoming  impressions  and  redisiDatching  instructions  in  an  integrated 
form,  at  the  same  time  relaying  on  to  the  cortex  those  reqtiiring  further  analysis. 
These  thalamic  centres  control  the  lower  centres  and  in  higher  animals  are  themselves 
influenced  and  controlled  by  higher  cortical  centres,  an  effect  seen,  for  example,  in  the 
"  sham  rage  "  and  evidences  of  general  sympathetic  hyperactivity  that  occur  in  the 
cat  after  its  cortico-thalamic  connections  have  been  cut  (Bard,  1928  ;    Cannon,  1929). 

The  two  nuclei  derived  from  the  thalamus  with  visual  connections  are 
the  lateral  geniculate  body  and  the  pulvinar. 

THE  LATERAL  GENICULATE  BODY.  The  aulagc  of  the  lateral  geniculate 
body  is  evident  even  in  the  primitive  Cyclostomes  (Herrick  and  Obenchain, 
1913)  ;  it  is  recognizable  in  most  Fishes  as  a  nest  of  cells  in  the  angle  between 
the  optic  tract  and  the  tectum  (Franz.  1912).  and  is  relatively  well  developed 
in  Teleosteans  (Kappers,  1920).  In  Amphibians.  Reptiles  and  Birds,  it 
remains  small  (see  Kappers,  1921)  and  is  not  j^rojected  onto  the  cortex 
(Elliot  Smith,  1928),  but  in  Mammals  it  shows  an  abrupt  development.  It 
is  well  represented  among  all  Mammals  excejDt  semi-blind  types  such  as 
the  mole  (Gan.ser.  1882  ;  Frankl-Hochwart.  1902).  and  it  assumes  many 
variations  of  structure  in  the  different  species. ^  In  the  more  primitive 
Mammals  (Marsupials)  it  has  a  dorsal  and  a  ventral  nucleus  showing  no 
lamination,  and  lies  vertically  on  the  surface  of  the  brain  (Fig.  715).  The 
ventral  nucleus  is  the  more  primitive  and  is  homologous  with  the  entire 
geniculate  body  of  Fishes,  Reptiles  and  Birds  :  the  dorsal  nucleus  only  is 
projected  to  the  cortex.-  As  evolution  proceeds,  changes  take  place  con- 
sisting of  a  disappearance  of  the  primitive  ventral  nucleus,  the  appearance 
of  rows  of  large  cells  along  the  periphery  of  the  dorsal  nucleus,  and  the 
lateral  rotation  of  the  whole  structure  so  that  the  original  external  surface 
lies  ventrally.  Its  highest  differentiation  is  seen  in  the  Primates,  in  which 
it  is  represented  almost  entirely  by  the  dorsal  nucleus.^  In  these  the 
primitive  ventral  nucleus  has  dwindled  almost  into  insignificance  ;  it 
probably  receives  only  crossed  optic  fibres  and  none  from  the  recently 
developed  macula   (^Minkowski.    1920),   and  from   it   issues   the    brachium 

1  v.  Monakow  (1883).  Cajal  (1904),  Sachs  (1909),  Xeiding  (1911),  Winkler  and  Potter 
(1914),  Horne-Craigie  (192.5),  Overbosch  (1926).  Putnam  (1926)"  Le  Gros  Clark  and  Penman 
(1934),  Packer  (1941).  Le  Gros  Clark  (1941). 

2  v.  Monakow  (1883),  Kappers  (1920),  Winkler  (1921),  Brouwer  (1923),  Putnam  (1926). 

3  Ziehen  (1903),  Sachs  (1909).  Friedemann  (1912),  Minkowski  (1913). 


542  THE   EYE   IN   EVOLUTION 

tecti  ;  it  is  related  to  the  reflex  centres  in  the  mid-brain  and  has  no  connec- 
tion with  the  cortex,  persisting  in  man  after  lesions  in  the  geniculo-calcarine 
path.^  The  ventral  nucleus  thus  probably  retains  the  primitive  photostatic 
functions,  while  the  higher  visual  functions  are  probably  all  taken  over  by 
the  more  lately  differentiated  dorsal  nucleus  with  its  elaborate  laminated 
structure  and  point-to-point  retinal  representation  ^  (Ingvar,  1923  ; 
Woollard,  1926  ;   Le  Gros  Clark,  1941-42). 

THE  PULViNAR.  This  nucleus  occupying  the  posterior  extremity  of  the  thalamus 
appears  late  in  phylogenetic  history,  becoming  of  considerable  size  only  in  Primates 
in  which  its  development  may  be  correlated  with  the  adoption  of  the  erect  posture. 
While  tindoubtedly  associated  with  visual  and  auditory  integrations,  its  connections 
with  these  systems  are  still  obscure.  It  would  appear  to  have  no  direct  connections 
with  the  retina  or  the  visual  cortex,  nor  with  the  ascending  somatic  tracts  (Minkowski, 
1913  ;  Brouwer  and  Zeeman,  1926)  but  projects  to  the  parastriate  area  of  the  cortex 
(area  18)  and  to  the  posterior  Sylvian  receptive  area  adjacent  to  the  auditory  area 

Figs.  716  to  718. — The  Development  of  the  Telencephalon. 

R 

DL        R  DL 


O   CD  00 

^—T^  VL        F  VI 


VL 

Fig.   716.  Fig.   717.  Fig.   718. 

Fig.  716. — Initially  the  telencephalon  appears  as  a  tube  with  thick  lateral 
walls  of  nervous  tissue  and  a  thin  non-nervous  roof,  R,  and  floor,  F.  The  lateral 
walls  are  divided  into  dorso- lateral,  DL,  and  ventro-lateral,  V L,  segments. 

Fig.  717. — During  further  development  the  lateral  walls  turn  inwards  leaving 
a  narrow  area  representing  the  roof  and  floor. 

Fig.  718. — The  inturned  dorsal  and  ventral  edges  of  each  lateral  wall  fuse, 
forming  out  of  the  unpaired  vesicle  two  cerebral  hemispheres,  each  containing  a 
lateral  ventricle.  The  dorso-lateral  wall,  DL,  forms  the  cortex  ;  from  the  ventro- 
lateral wall,  VL,  develop  the  nuclei  of  the  corpus  striatum. 

(area  22)  (Le  Gros  Clark  and  Northfield,  1937).  Its  association  with  the  cerebellum 
(Clarke  and  Horsley,  1905)  and  the  red  nucleus  (Sachs,  1909)  and  with  the  thalamo- 
cortical fibres  for  the  arm  region  in  the  precentral  convolution  of  the  brain  may  perhaps 
reflect  the  importance  of  the  hand  and  fingers  in  Primates  in  exploration  and  manipula- 
tion, and  the  nucleus  may  act  as  an  integrating  area  for  the  coordination  of  the  eye  and 
the  hand,  being  thus  related  to  the  higher  visual  functions  of  stereognosis  (Winkler, 
1919  ;   Kappers,  1920). 

The  telencephalon  is  present  in  all  Vertebrates,  the  dorsal  part  of  its  lateral 
walls  forming  the  cortex,  the  ventral  walls  the  nuclei  of  the  corpus  striatum 
(Figs.  716  to  718).  Initially  it  was  built  up  as  a  receptor  station  for  the 
olfactor\r  nerves,  and  the  dominance  of  the  higher  Vertebrates  is  essentially 
due  to  tlie  replacement  of  the  original  palseocortex  based  upon  the  sense  of 
smell  by  tlie  neocortex  built  around  the  sense  of  vision. 

1  B.,: '.vver  (1917-26),  Minkowski  (1920),  Winkler  (1921),  v.  Monakow  (1924). 
*  p.       :. 


CENTRAL   NERVOUS   SYSTEM  543 

In  Cyclostomes  and  Fishes  the  entire  telencephalon  and  much  of  the  diencephalon 
are  devoted  to  olfactory  activities.  In  Amphibians  are  seen  the  beginnings  of  the 
emergence  of  non-olfactory  systems  into  this  region  of  highest  integration  ;  although 
no  part  of  their  cerebral  hemispheres  is  free  from  olfactory  connections,  much  of  their 
thalamus  is  devoted  to  other  sensory  mechanisms,  and  it  is  significant  that  the  first 
indication  of  a  sensory  cortical  projection — the  thalamo -cortical  tract  of  Amphibians 
— is  not  visual  (Rubaschkin,  1903  ;  Herrick,  1917).  In  Reptiles  the  ascending  sensory 
systems  are  greatly  enlarged  so  that  they  monopolize  areas  of  the  corpus  striatum  and 
the  cortex,  while  in  Mammals  the  sensory  and  somatic  systems  dominate  the  cortex 
to  an  ever-increasing  degree  until  in  man  the  olfactory  centres  become  insignificant 
and  are  relegated  to  an  obscure  corner  while  the  visual  projections  are  prolific  and 
widespread. 

In  Cyclostomes  and  selachian  Fishes  the  entire  fore-brain  is  represented 
by  an  insignificant  paleocortex  with  purely  olfactory  functions,  which 
persists  as  the  pyriform  lobes  (the  primary  olfactory  cortex)  of  the  higher 
Vertebrates.  To  this  is  added  in  Teleosteans  the  archicortex,  still  entirely 
olfactory,  which  persists  as  the  hippocampus  (the  secondary  olfactory 
cortex).  It  is  interesting  that  in  Cyclostomes,  "  ganoid  "  and  teleostean 
Fishes  the  fore-brain  has  a  non-nervous  (ependymal)  roof.  In  Amphibians 
some  non-olfactory  fibres  reach  the  fore-brain  and  in  Reptiles  a  true 
cortex  first  appears.  In  Birds  this  structure  is  well  developed  and  the 
olfactory  lobes  have  become  small  ;  but  its  surface  is  still  smooth,  the  roof 
is  still  thin  and  its  main  mass  is  occupied  by  the  relatively  enormous  corpus 
striatum.  The  neopallium  as  we  know  it  is  a  characteristic  of  Mammals, 
serving  as  a  receptor  area  of  optic,  auditory,  tactile  and  other  sensory 
stimuli,  an  initiator  of  voluntary  movements  and  a  centre  for  associative 
memory  and  eventually  of  conceptual  thought.  As  the  scale  of  mammalian 
evolution  is  ascended  this  portion  of  the  cerebrum  becomes  increasingly 
important  and  the  olfactory  area  less  ;  m  Insectivores  or  the  rabbit,  for 
example,  the  cortex  is  only  slightly  convoluted  and  does  not  cover  the 
cerebellum  (Fig.  708)  ;  in  the  horse  and  the  dog  convolutions  have  become 
prominent  (Fig.  709),  while  in  the  Primates  both  anatomically  and  function- 
ally it  has  become  the  master-tissue  wherem  afferent  sensory  impressions 
are  assessed  and  stored  and  are  correlated  through  an  intricate  system  of 
association  fibres  with  the  complex  activities  of  these  animals. 

The  evohdion  of  the  visual  pathways  and  centres  will  be  readily  understood 
from  this  short  sketch  of  the  phylogenetic  development  of  the  brain  (Figs. 
710  to  715).  In  Cyclostomes  (apart  from  the  degenerate  Myxinoids^),  the 
optic  fibres  from  the  retina  are  jDrojected  into  the  superficial  layers  of  the 
tectum,  here  to  come  into  relation  with  the  bulbo-  and  spino-tectal  fibres 
arriving  to  the  deeper  layers  (Fig.  710)  ;  in  these  a  primitive  anlage  of  the 
lateral  geniculate  body  may  be  present  (Herrick  and  Obenchain,  1913).  In 
Fishes  a  few  collateral  fibres  are  given  to  the  still  very  rudimentary  lateral 

J   p.  734. 


544  THE   EYE   IN   EVOLUTION 

geniculate  bodies,  while  the  optic  axons  again  terminate  in  the  tectum  and 
its  dorsal  extensions,  the  optic  lobes  (Fig.  711).  Here  there  is  a  point-to-point 
representation  of  the  retina  (Lubsen,  1921  ;  Buser  and  Dusardier,  1953). 
In  Amphibians  the  tectum  is  more  highly  differentiated,  but  still  there  is 
no  higher  projection  of  visual  fibres  (Fig.  712)  ;  in  these  and  in  Reptiles 
optic  fibres  terminate  in  the  lateral  geniculate  body  which  emits  only  a 
geniculo-tectal  tract  (Fig.  713).  In  Birds  the  same  relations  are  maintained  ; 
here  again  a  point-to-point  representation  of  the  retina  has  been  physio- 
logically demonstrated  (Hamdi  and  Whitteridge,  1954).  In  addition  to  the 
main  end-station  in  the  tectum,  however,  a  bundle  of  optic  fibres  in  Birds 
has  a  thalamic  termination  in  a  basal  optic  ganglion  (the  ganglion  ecto- 
mammillare  of  Edinger)  (Fig.  714).  Near  the  anterior  border  of  the  tectum 
a  dorsal  thalamic  nucleus  (the  spiriform  nucleus)  receives  fibres  from  this 
basal  optic  ganglion,  in  addition  to  fibres  from  the  large  spinal  and  bulbar 
tracts  and  descending  fibres  from  the  occipital  area  of  the  cortex  and  corpus 
striatum  ;  it  has,  however,  no  ascending  projection,  and  the  function  of 
this  thalamic  system  is  therefore  still  entirely  photostatic. 

In  the  lower  Vertebrates  the  superior  colliculus  which  has  evolved 
from  the  optic  tectum  receives  the  mass  of  optic  fibres.  In  Mammals, 
however,  the  vast  majority  of  the  optic  fibres  (70  to  80%)  terminates  in 
the  dorsal  nucleus  of  the  lateral  geniculate  body  whence  they  are  relayed 
by  a  cortical  projection  to  the  occipital  cortex  ;  while,  as  in  the  lower 
Vertebrates,  the  minority  goes  either  directly  to  the  tectum  (superior  colli- 
culus) in  the  brachium  tecti  or  indirectly  after  being  relayed  in  the  ventral 
nucleus  of  the  lateral  geniculate  body.  In  the  colliculus  a  point-to-point 
representation  from  the  retina  has  been  reported  in  the  cat,  the  goat,  and 
the  rabbit  (Apter,  1945  ;  Coopered  aZ.,  1953  ;  Hamdi  and  Whitteridge,  1953). 
From  this  system  there  is,  as  always,  no  cortical  projection.  The  ventral 
geniculate  nucleus  is  thus  phylogenetically  the  older  and  corresponds  with 
the  entire  lateral  geniculate  body  of  the  lower  Vertebrates,  decreasing  in 
importance  as  the  visual  system  swings  from  a  tectal  to  a  cortical  orientation. 

It  is  clear,  therefore,  that  initially  the  visual  system  is  developed  in 
association  with  the  postural  and  gravistatic  systems  in  the  tectum — the 
meeting-place  of  optic,  static,  tactile,  gustatory  and  proprioceptive  impulses, 
an  area  which,  although  it  receives  fibres  from  the  cortex,  sends  no  fibres  to 
it.  It  is  easy  to  underestimate  the  great  importance  of  vision  in  orientation 
and  equilibration,  for  in  man  these  static  functions  are  readily  overshadowed 
by  the  apparent  preponderance  of  the  dynamic  aspects  of  vision  and  the 
overwhelming  importance  of  its  sensory  and  cognitive  functions.  The 
phylogenetic  importance  of  photostasis,  however,  is  obvious.  As  evolution 
proceeds,  sensory  functions  assume  greater  and  greater  preponderance,  and 
althougl]  the  reflex  and  photostatic  aspects  of  vision,  which  are  as  complex 
and  elal:  \te  in  Primates  as  in  the  lower  Vertebrates,  are  retained  in  the 
tectum,  I        tually  in  the  higher  Vertebrates  the  epicritic  visual  functions 


CENTRAL   NERVOUS   SYSTEM  545 

are  transmitted  through  thalamic  relay-stations  in  an  ever-increasing  degree 
to  the  cortex.  This  translation  from  a  reflex  to  a  highly  integrative  level 
allows  the  development  of  the  central  nervous  system  to  proceed  along  two 
main  lines — an  advance  from  mass  reflex  reactions  to  more  restricted  but 
complicated  patterns  of  behaviour,  and  an  advance  from  a  fixed  rigidity  to 
an  extreme  degree  of  plasticity  and  lability  of  resf)onse. 

It  follows  from  the  late  projection  of  vision  to  the  cerebral  cortex  that 
ablation  of  this  structure  in  the  lower  Vertebrates  involves  no  visual 
incapacity.  The  fore -brain  of  C'yclostomes  is  completely,  and  of  Fishes  and 
Reptiles  almost  completely  an  olfactory  brain  and  its  removal  has  no  visual 
effects,  and,  indeed,  entails  little  alteration  in  the  locomotion  and  the  general 
behaviour  of  the  animal  (Magendie,  1824  ;  Flourens.  1824).  Fishes, 
it  is  true,  lose  the  faculty  of  responding  to  unusual  stimuli  with  initiative, 
become  more  purely  reflex  creatures  than  they  already  are,  and  are  slower 
in  their  reactions  (Janzen,  1933  ;  Hosch,  1936  ;  Header,  1939  ;  and 
others)  ;  while  Amphibians  lose  spontaneity  and  initiative  in  their 
conduct  and  the  conditioning  of  reflexes  may  fail  (Diebschlag.  1934  ; 
Aronson  and  Noble,  1945).  Nevertheless,  a  decerebrate  frog  will  catch  flies 
quickly  and  without  difliculty  (Schrader,  1887).  It  is  not  until  Birds  are 
reached  that  removal  of  the  cerebral  hemispheres  induces  a  general  listless- 
ness  and  a  marked  lack  of  response  ;  without  a  cortex  the  pigeon  will  main- 
tain its  bodily  functions,  will  eat,  mate  and  rear  its  young  (Rogers,  1920-28), 
it  will  avoid  obstacles  and  select  its  food  visuall}^  although  some  emotional 
responses  can  be  elicited  to  visual  stimuli  (Schrader,  1888).  Thus  a 
decerebrate  jjigeon  shows  some  impairment  of  the  higher  faculties  of 
recognition  and  will  not  show  the  usual  reactions  to  a  threatening  approach 
(Visser  and  Rademaker,  1935).  Blindness  can  only  be  caused  by  destruction 
of  the  primary  centres  (Panizza.  1855  ;    Schrader,  1887  ;    Munk,  1890). 

It  is  only  in  Mammals  that  the  conduct  of  the  animal  is  seriously 
disturbed  by  removal  of  its  cerebral  cortex,  and  even  then  it  is  only  the 
Primates  that  are  rendered  blind  by  this  mutilation  ;  similarly  it  is  only 
among  Mammals  that  cortical  stinndation  involves  motorial  responses 
although  the  number  of  discrete  movements  that  can  be  elicited  in  this 
way  are  few  among  the  more  primitive  representatives  of  this  class  (less 
than  10  in  Monotremes  and  Marsupials,  v.  Buddenbrock,  1937).  In  the 
lower  Mammals  there  is  a  considerable  equipotentiality  of  function  m  the 
cortex  and,  depending  on  the  survival  of  incoming  tracts,  one  part  can 
readily  act  as  substitute  for  another.  Even  if  the  entire  cortex  is  removed, 
however,  rabbits,  after  an  initial  period  of  blindness,  can  later  differentiate 
between  light  and  darkness  (ten  Cate,  1935)  and  decerebrate  dogs  will  react 
and  exhibit  emotions  to  visual  stimuli  (Goltz.  1892  ;  Pavlov,  1927).  If, 
however,  the  occipital  cortex  alone  is  removed  from  Rodents  (rabbit,  rat), 
there  is  a  loss  of  form  vision  only,  while  the  faculties  of  perception  of  light 
and  spatial  localization  are  maintained  so  that  the  animal  can  move  around, 


546  THE   EYE   IN   EVOLUTION 

avoid  obstacles  and  recognize  food  by  sight  ^  ;  these  latter  more  fundamental 
aspects  of  vision,  therefore,  have  subcortical  integrations.  In  dogs  the 
incapacity  is  greater  ;  the  animal  retains  the  faculty  of  perception  of  light 
and  can  discriminate  differences  of  intensity  unimpaired,  but  in  imfamiliar 
surroundings  it  gropes  with  its  paws,  moving  cautiously  as  if  blind  (Goltz, 
1892  ;  Pavlov,  1927  ;  Lashley,  1931  ;  Marquis,  1934  ;  Wing  and  Smith, 
1942).  Cats  react  similarly  although  they  retain  orientation  and  the 
discrimination  of  objects  to  a  considerable  extent  in  the  dark  (Smith,  1937). 
Monkeys  suffer  much  more  incapacity  ;  light  perception  remains  but 
discrimination  between  brightness  is  lost  and  performance  is  greatly  impaired, 
particularly  in  bright  light  compared  with  conditions  involving  dark 
adaptation  (Marquis  and  Hilgard,  1937  ;  Kliiver,  1941).  If  part  of  the 
visual  cortex  of  rats  is  removed,  deficiencies  in  the  response  to  visual 
conditioned  reflexes  are  proportional  to  the  amount  removed  irrespective 
of  the  area  mutilated  (Lashley,  1922-34),  while  in  monkeys  some 
responses  which  are  lost  can  be  relearned,  presumably  by  a  new  area 
(Ades,  1946).  Similar  substitute  areas  can  be  utilized  for  auditory  responses 
in  dogs  (Allen,  1945). 

It  is  thus  apparent  that  although  a  considerable  degree  of  specificity 
of  function  appears  for  the  first  time  in  the  neocortex  of  Mammals,  it  is 
still  largely  plastic  with  imprecise  localization  ;  only  in  man  does  ablation 
of  the  occipital  cortex  lead  to  permanent  blindness  with  complete  loss  of  all 
sensations  of  light.  In  him  the  only  sub-cortical  visual  activity  is  pupillary, 
and  in  him  alone  is  vision  in  its  entirety  a  cortical  function. 

Ades.    J.  Neuropath.,  5,  60  (1946).  Cajal.     Rev.  trim.  Histol.  norm,  path.,  3-4,  65 

Allen.    Amer.  J.  Physiol.,  144,  415  (1945).  (1889). 

Apter.    J.  NeitrophysioL,  8,  123  (1945).  Internat.    Mschr.    Anat.    Physiol.,    8,    337 

Aronson  and  Noble.     Bull.  Amer.  Mus.  nat.  (1891). 

Hist.,  86,  83  (1945).  Te.vtura  del  sistema  nervioso  del  hombre  y  de 

Bard.    Amer.  J.  Physiol.,  84,  490  (1928).  los  vertebrados,  Madrid  (1904). 

Benoit.     Bidl.  Biol.,  71  (4),  393  (1937).  Cannon.     Bodily  changes  in  pain,  hunger,  fear 

Benoit  and  Assenmacher.     C.  R.  Acad.  Sci.  and  rage,  N.Y.  (1929). 

(Paris),  236,  2002  (1953).  ten    Cate.      Arch,    neerl.    Physiol.,    20,    467 

Benoit,    Assenmacher    and    Manuel.      C.    R.  (1935). 

Acad.  Sci.  (Paris),  235,  1695  (1952).  Clark,  Le  Gros.    J.  Anat.,  75,  225,  419  ;    76, 

C.  R.  Sac.  Biol.  (Paris),  147,  40  (1953).  131  (1941)  ;    76,  369  (1942). 

Benoit,  Assenmacher  and  Walter.    C.  R.  Soc.  Trans,  ophthal.  Soc.   U.K.,  62,  229  (1942). 

Biol.  (Paris),  147,  186  (1953).  Clark,  Le  Gros,  and  Northfield.   Brain,  60,  126 

Brouwer.     Mschr.    Psychiat.   Neurol.,   41,    9,  (1937). 

129,  203  (1917).  Clark,  Le  Gros,  and  Penman.  Proc.  Roy.  Soc. 

Schweiz.   Arch.  Neurol.   Psychiat.,   13,    118  £,114.291  (1934). 

(1923).  Clarke  and  Horsley.     Brain,  28,  13  (1905). 

Brouwer  and  Zeeman.  J.  Neurol.  Psychopath.,  Cooper,  Daniel  and  Whitteridge.    J.  Physiol., 

6,  1  (1925).  120,  471,  514  (1953). 

Brain,  49,  1  (1926).  Diebschlag.    Z.  vergl.  Physiol.,  21,  343  (1934). 

Briigger.    Helv.  physiol.  Acta,  1,  \SZ  (194:3).  Flourens.      Recherches   exper.    d.    syst.    nerv., 

V.  Buddenbrock.    Grundriss  d.  vergl.  Physiol.,  Paris  (1824). 

Berlin  (1937).  Frankl-Hochwart.     Arb.  neurol.  Inst.   Wien, 

Buser  and  Dusardier.    J.  Physiol.  (Paris),  45,  8,  190  (1902). 

67  (1953).  Franz.    Folia  neuro-biol.  (Lpz.),  6,  402  (1912). 

^  It  is  resting  that  in  amblyopia  in  squint,  light  perceptioia  and  spatial  orientation 

remain  norii.         hile  form  vision  suffers. 


CENTRAL  NERVOUS   SYSTEM 


547 


Friedemann.     J.  Psychol.  Neurol.  (Lpz.),  18, 

309  (1912). 
V.  Frisch.     Pfliigers  Arch.  ges.  Physiol.,  138, 

319  (1911). 
Ganser.     Morphol.  Jb.,  7,  591  (1882). 
Ghiselli.    J.  camp.  Neurol..  67,  451  (1937). 
Goltz.      Pfiiigers  Arch.  ges.   Physiol.,  51,  570 

(1892). 
Hamdi  and  Wliitteridge.  J.  Physiol.,  121,  44P 

(1953). 
Quart.  J.  exp.  Physiol..  39,  111  (1954). 
Herrick.     J.  comp.  Neurol.,  28,  215  (1917)  ; 

32,  429  (1921). 
Herrick  and  Obenchain.    J.  comp.  Neurol.,  23, 

635  (1913). 
Hess,    v.    R.      Helv.    jihysiol.    Acta,    1,    549 

(1943)  ;    2,  305  (1944). 
Hess,   W.    R.,   and   Brligger.     Helv.   physiol. 

Acta,  1,  33,  511  (1943). 
Horne-Craigie.     Introduction  to  the  Anatomy 

of  the  Central  Nervous   System,    Toi'onto 

(1925). 
Hosch.     Zool.  Jb.,  Abf.  Zool.  Physiol.,  57,  57 

(1936). 
Huber  and  Crosby.     J.  comp.  Neurol.,  48,  1 

(1929). 
Ingvar.    Acta  med.  scand.,  59,  696  (1923). 
Janzen.    Zool.  Jb.,  Abt.  Zool.  Physiol.,  52,  591 

(1933). 
Jungherr.    J.  comp.  Neurol.,  82,  55  (1945). 
Kappers.      Die    vergleichende    Anatoinie    des 

Nervensystems,  Haarlem  (1920-21). 
Keller  and  Stewart.     Amer.  J.  Physiol.,  101, 

64  (1932). 
Kluver.    J.  Psychol.,  11,  23  (1941). 
Lashley.    Amer.  J.  Physiol.,  59,  44  (1922). 
J.  comp.  Neurol.,  53,  419  (1931)  ;    60,  57 

(1934). 
Loeser.     J.  comp.  Neurol.   PsyclioL,  15,  355 

(1905). 
Lubsen.     Ned.  T.  Geneesk.,  2,  1258  (1921). 
Magendie.     J.  Physiol,  exp.   Path..  Paris,  3, 

153,  376  (1823)  ;   4,  169,  399  (1824). 
Magoun.     Amer.  J.  Physiol.,  Ill,  91  (1935). 
Marquis.     Pes.  Publ.  Assoc,  nerv.  ment.  Dis., 

13,  558  (1934). 
Arch.  Neurol.  Psychial.,  33,  807  (1935). 
Marquis  and  Hilgard.     Brain,  60,  1  (1937). 
Header.     Zoologica  (X.Y.),  24,  U  (1939). 
Minkowski.     Arb.   hirnanat.   Inst.   Zurich.,  7, 

255  (1913). 
Schiceiz.   Arch.   Neurol.    Psychiat.,   6,   201  ; 

7,  268  (1920). 


V.  Monakow.     Arch.  Psychiat.  Nervenhr.,  12, 

141  (1882)  ;   14,  699  (1883)  ;   16,  151, 317 

(1885). 
Lokalisation     iin      Grosshirn,     Wiesbaden 

(1924). 
Munk.      Uber  die   Functionen  der  Grosshirn- 

rinde,  Berlin,  I  (1881)  ;    II  (1890). 
Xeiding.      ^4^/;.    Kon.    preuss.    Akad.    Tr/.s5., 

Berlin,  Anhang  2,  1  (1911). 
Xowikoff.      Z.  Morphol.   Oekol.  d.    Tiere,  29, 

374  (1934). 
Overbosch.     Diss.,  Amsterdam  (1926). 
Packer.    J.  ^/ia^,  75,  309  (1941). 
Panizza.     G.  reale  1st.  Lombardo,  7,  237,  242 

(185.5). 
Mem.  reale  1st.  Lombardo,  5,  380  (1856). 
Parker.     Bull.   Bureau  Fisheries,  Wash.,  22 

(1903)  ;   30  (1912). 
Parker,    Hendricks,    Bortliwick   and   Jemier. 

Nature  (Lond.),  169,  242  (1952). 
Pavlov.    Conditioned  Refle.ves,  Oxford  (1927). 
Piper.     Zbl.  Physiol.,  20,  293  (1906). 
Putnam.    Arch.  Neurol.  Psychiat.,  16,  1,  285, 

566,  683  (1926). 
Rogers.     Amer.  J.  Physiol..  55,  310  (1920)  ; 

86,  639  (1928). 
J.  comp.  Neurol.,  35,  21  (1922). 
Rubaschkin.      Arch.    mikr.    Anat..    62,    207 

(1903). 
Sachs.     Brain,  32,  95  (1909). 
Scharrer.     Z.  vergl.  Physiol..  7,  1  (1928). 
Schrader.     Pfliigers  Arch.  ges.  Physiol.,  41,  75 

(1887)  ;   44,  175  (1888). 
Shirasu.    Acta  Sch.  ined.  Univ.  Kioto,  30,  279 

(1953)'. 
Smith,  Elliot.     Trans,  ophthal.  Soc.  U.K.,  48, 

Ixiv  (1928). 
Smith,  K.  U.    J.  genet.  Psychol..  50,  137  ;   51, 

329  (1937). 
Visser  and  Rademaker.    Arch,  neerl.  Physiol., 

20,  284  (1935). 
Wing  and  Smith.     J.  e.vp.  Psychol.,  31,  478 

(1942). 
Winkler.      Opera  Omnia.  Haarlem,  6   (1918- 

21). 
Winkler  and  Potter.  Anat.  Guide  to  Researches 

on  the  Cat's  Brain.  Amsterdam  (1914). 
Woollard.     Brain,  49,  77  (1926). 
Young.    J.  e.vp.  Biol.,  12,  254  (1935). 
Ziehen.      M,schr.    Psychiat.    Neurol.,    14,    54 

(1903). 


THE  HORMONAL  CONTROL 

The  control  of  the  activities  of  organisms  by  chemical  substances  either 
derived  from  the  external  environment  or  elaborated  in  the  internal  environ- 
ment is.  of  course,  imiversal.  In  plant  life  we  have  already  seen  ^  that  such 
chemical  substances  are  the  only  means  available  for  coordinating  the 
activities  of  different  parts  and  that  many  processes  including  flowering, 

1  pp.  10,  39. 


548 


THE   EYE   IN   EVOLUTION 


Fig.  719. — Ernest  Hknry  Starling  (1866-1927). 


HORMONAL   CONTROL 


549 


growth  and  phototropic  bending  are  mediated  by  such  substances,  the  most 
fully  knowai  among  which  are  auxins.  In  the  simplest  unicellular  animals  the 
same  mechanism  of  the  diffusion  of  the  chemical  products  of  metabolism 
plays  an  essential  role  in  the  activities  of  the  organism,  and  although  in  the 
higher  animals  greater  reliance  is  increasingly  placed  on  the  more  efficient 
and  adaptable  nervous  mechanism,  chemical  coordinators  are  still  retained, 
particularly  to  mediate  those  functions  for  which  the  controlling  influence 
is  required  to  last  over  considerable  periods  of  time — growth  and  cellular 
differentiation,  general  metabolism,  sexual  activity,  and  so  on.  The  spheres 
of  influence  of  nervous  and  chemical  control  are  by  no  means  mutually 
exclusive  for  while  a  sudden  response  may  be 
induced  by  the  nervous  mechanism,  it  is  frequently 
maintained  by  the  chemical,  as  is  exemplified  in  the 
reaction  of  the  sympathetic  and  the  adrenals  to 
situations  of  stress,  or  the  comj)lementary  activities 
of  nervous  and  chemical  agencies  in  effectmg  changes 
in  the  chromatophores  of  Insects  and  teleostean 
Fishes.  Chemical  stimulators  (or  inhibitors)  speci- 
fically elaborated  to  jjroduce  such  effects  are  termed 

HORMONES. 


Fig.  720. — Vesalius's 
Conception  of  the 
Funnel  (Infundibu- 
lum)  (B)  through 
WHICH  THE  Phlegm 
FROM  THE  Brain 
Trickled  into  the 
Pituitary  Gland  (A). 

The  four  iinaginary 
ducts  C,  D,  E,  F,  carried 
the  phlegm  from  the 
gland  (Zuckernian). 


The  conception  of  hormones  recalls  the  old  theory  of 
the  humours  which  derived  from  the  Aristotelian  conception 
that  all  things  were  inade  up  of  the  four  common  elements 
— earth,  water,  air  and  fire.  The  fovir  humours  which 
pervaded  the  body  and  determined  its  health — yellow  bile 
(choler)  from  the  gall-bladder,  black  bile  (melancholy)  from 
the  spleen,  blood  (sanguine)  froiu  the  liver,  and  pituita  (or 
phlegm)  from  the  brain.  The  conception  of  Vesalius  that  the 
phlegm   secreted   from   the    brain    escaped  by  way  of  the 

infundibulum  into  the  pituitary  gland  and  thence  was  distribvited  throughout  the 
body  is  very  akin  to  the  most  modern  conceptions  of  neuro -endocrine  secretion  that 
we  are  now  to  consider  (Fig.  720). 

The  fact  that  organs  deliver  the  products  of  their  activity  into  the  blood-current 
and  thus  influence  bodily  functions  was  known  to  Claude  Bernard  (1859)  who  introduced 
the  term  "  internal  seci'etions."  The  word  hormone  {op^doj,  to  rouse  to  activity), 
suggested  by  W.  B.  Hardy,  was  first  apjilied  to  animal  physiology  by  Starling  (1905) 
with  reference  to  the  discovery  of  the  manufacture  of  secretin  by  the  pancreas  (1902). 
The  word  was  first  applied  to  plant  physiology  by  Fitting  (1910)  who  found  that  a 
substance  in  the  pollen  of  the  orchid  caused  a  swelling  of  the  gynosteinium  of  the 
flower.  In  botany  the  teriu  phytohormones  is  often  used,  or,  as  the  Russians  have  it, 
florigens  (Cailahian,  1940).  Since,  in  association  with  Sir  William  Maddox  Bayliss, 
SIR  ERNEST  HENRY  STARLING  (1866-1927)  was  the  discoverer  of  the  first  specific 
hormone  and  in  view  of  his  immense  contributions  to  physiology  in  other  fields,  such 
as  the  nature  of  the  body-fluids,  the  control  of  the  intra-ocular  pressure  and  a  host 
of  other  equally  revolutionary  conceptions,  I  am  introducing  this  section  with  his 
photograph  (Fig.  719).  My  personal  indebtedness  to  him  as  Professor  of  Physiology 
in  University  College.  London,  where  he  initiated  me  into  the  techniques  of  research, 
is  indeed  great. 


550  THE   EYE   IN   EVOLUTION 

It  is  obvious  that  to  become  effective  to  a  multicellular  organism,  a 
hormone  must  be  distributed  through  the  circulation  ;  specialized  endocrine 
organs  are  therefore  found  in  Annelids,  Molluscs,  Arthropods  and  Chordates. 
It  is  not  surprising  that  with  a  function  akin  to  that  of  nervous  tissue,  these 
chemical  messengers — or  at  any  rate  those  which  have  been  investigated — 
are  initially  in  great  part,  both  phylogenetically  and  embryologically, 
associated  with  the  nervous  system.  Other  origins,  however,  are  common 
particularly  in  Vertebrates.  In  these,  neuro-endocrine  organs  are  found  in 
the  diencephalon — the  hyjjothalamus,  the  pituitary  and  pineal  glands — and 
in  the  medulla  of  the  adrenal,  a  tissue  of  autonomic  nervous  origin  which 
has  migrated  outside  the  central  organization  ;  but  in  addition,  from  the 
endoderm  there  arise  such  hormones  as  the  principles  of  the  anterior  lobe 
of  the  pituitary,  thyroxin,  and  insulin,  and  from  the  mesoderm,  the  sex 
hormones  and  the  steroids  of  the  adrenal  cortex. 

Those  hormones  which  mediate  the  migration  of  the  retinal  pigment  are 
concerned  with  the  sensory  aspects  of  vision  ;  several  others  have  associa- 
tions with  the  action  of  light  upon  organisms  and  are  therefore  of  interest 
from  our  immediate  point  of  view  ;  to  these  we  shall  mainly  confine  ourselves, 
and  since  some  of  their  reactions  have  already  been  discussed,  a  relatively 
short  note  is  all  that  is  called  for  at  this  stage.  All  of  these  concern  the 
products  of  the  neuro-endocrine  system.  We  have  already  seen  that  certain 
cells  of  the  central  nervous  system,  particularly  those  of  the  cerebral  ganglion 
in  Invertebrates  and  of  the  diencephalon  in  Vertebrates,  show  a  considerable 
degree  of  light-sensitivity  ^  ;  the  dual  function  of  the  pineal  body,^  some- 
times optical,  sometimes  endocrine,  is  an  example  of  the  same  association. 
It  is  not  surprising  therefore  that  nerve  cells  in  these  regions  should  some- 
times respond  by  the  secretion  of  hormones  to  the  direct  stimulus  of  light 
and  at  other  times  to  indirect  stimulation  through  the  eyes. 

In  general  terms  the  neuro-endocrine  system  exercises  a  controlling 
influence  over  («)  the  integumentary  pigmentary  system  and  the  ocular 
pigments,  (h)  growth,  differentiation  and  metamorphosis,  (c)  the  development 
of  the  gonads  and  the  regulation  of  the  reproductive  cycle,  and  {d)  a  number 
of  processes  in  intermediate  metabolism,  principally  affecting  water,  salts, 
oxygen  and  carbohydrates.  A  noteworthy  feature  of  many  of  its  activities 
is  the  rh3^thmic  variation  in  several  of  these  activities,  either  as  a  divirnal 
rhytlim  as  is  seen  in  the  control  of  pigment  migration  and  in  some  metabolic 
processes,  or  as  cycles  of  longer  duration  such  as  are  exemplified  in  moulting 
or  the  sexual  rhythms. 

NEURO -SECRETORY  CELLS,  that  is,  nerve  cells  ivhich  also  have  the  characteristics  of 
glandular  cells   in  that  they  show  cyiological  evidence  of  secretory  activity,^  were  first 

^  pp.  520,  52.5,  537.  "  p.  711. 

'  All  uorve  cells  "  secrete  "  active  substances  (e.g.,  acetylcholine)  :  this  may  be  termed 
neurohumo  i  activity.  Neurosecretion  is  a  term  best  reserved  for  the  activities  of  nerve  cells 
which  also  ;  sess  the  cytological  attributes  of  glandular  cells.  For  a  complete  discussion,  see 
Convegno  siil:     yieurosecrezione.  Pub.  della  Stazione  Zoologica  di  Napoli,  24,  Supp.  (1954). 


HORMONAL   CONTROL  551 

described  by  Dahlgren  (1914)  in  the  spinal  cords  of  Fishes.  They  were  later  studied 
in  the  hyjDothalamus  of  Teleosteans  by  E.  Scharrer  (1928)  and  in  the  eye-stalks  of 
Crustaceans  by  Hanstrom  (1931-34)  ;  but  our  present  concej^tions  of  the  nature  and 
function  of  neuro -endocrine  conij^lexes  within  the  nervous  system  date  essentially 
from  the  work  of  Berta  and  Ernst  Scharrer  (1937-45).  It  now  seems  obvious  that 
the  secretory  activities  of  the  central  nervous  system  or  of  cells  directly  derived 
therefrom  exert  a  considerable  influence  on  the  metabolism  and  activities  of  many 


"^^J^-i^ 


■  I  '  1 1  'I ■ I 
lO/t 


Fig.   721. — XEURO-sECKETOiiY  Cell. 


From  the  right  nucleus  paraventricularis  of  the  rat.  The  granules  of  neuro- 
secretory material  are  seen  in  all  the  neurones  and  their  axons.  Note  the  charac- 
teristic fusiform  enlargements  in  the  axon  emerging  from  the  large  cell  in  the  upper 
left  corner  of  the  figure.  The  granule-laden  segments  seen  everywhere  are  cut 
portions  of  the  axons  of  other  neurones  at  a  distance  from  theii-  cell  bodies  (Stuart  W. 
Smith,  Amer.  J.  Anaf.,  89,  229). 

species  of  animals  including  man.  The  secretions  are  elaborated  within  a  large  cell- 
body  wherein  they  appear  as  granules  and  colloid-like  material  which  are  extruded 
along  the  axons,  sometimes  to  be  stored  in  organs  in  which  the  enlarged  nerve-endings 
terminate  (Fig.  721).^  The  latter  are  gland-like  structures  which  serve  as  storage- 
release  centres  and,  since  it  appears  unlikely  that  the  specialization  for  secretion  has 
eliminated  the  capacity  of  these  cells  to  act  as  conductors,  a  neuro -secretory  cell  can 
presumably  trigger  the  release  of  its  owii  accumulated  secretion  by  conducting 
impulses  to  its  endings  at  the  storage-site.  It  follows  that  if  it  were  formed  from 
several  completely  independent  groups  of  jjarent  cells,  such  a  "  gland  "  might  well 
serve  as  the  storage-release  centre  for  several  hormones  (see  Brown,  1944^51  ;  Brown, 
Sandeen  and  Webb,  1951  ;   Brown  and  Hines,  1952  ;   B.  Scharrer,  1953  ;   and  others). 

^  The   secretory  products   are  most   dramatically  shown  by  staining  with  the  chrome 
alum-hfcmatoxylin-phloxine  technique  of  Gomori  (1941).     See  Bargmann  (1949). 


552  THE   EYE   IN    EVOLUTION 

The  occurrence  of  a  neuro -endocrine  system  consisting  of  well-defined 
groups  of  neuro -secretory  cells  among  Invertebrates  is  widespread.  In  its 
most  primitive  form  it  is  seen  in  polyclad  worms  (Turner,  1946),  but  it 
becomes  conspicuous  in  the  more  highly  developed  Annelids  among  which 
neuro -secretory  centres  are  prominent,  particularly  in  the  cerebral  ganglia 
where  they  inhibit  maturation  of  the  gametes  (Bliss,  1951  ;  Durchon, 
1951  ;  Bobin  and  Durchon,  1952).  Neuro -secretory  cells  have  also  been 
described  among  Molluscs  in  the  central  nervous  system  of  Opisthobranchs, 
Prosobranchs,  Scaphopods  and  Cephalopods  (Young,  1936  ;  Gabe,  1949- 
53)  ;  the  part  played  by  simple  hormones,  probably  of  the  nature  of  tyramme 
and  betaine,  in  the  regulation  of  the  integumentary  hormones  of  Cephalopods 
has  already  been  discussed. ^  A  similar  neuro -secretory  function  is  more 
common  and  effective  in  the  nervous  system  of  Arthropods  ;  indeed,  in 
this  phylum  which  does  not  possess  a  closed  vascular  system,  no  means  is 
available  for  free  circulation  other  than  the  rich  hsemolymph  supply  which 
bathes  the  nervous  system.  In  Crustaceans  the  neuro -endocrine  system  and 
its  functions  have  received  much  attention  ;  it  consists  of  an  x-organ  and 
other  groups  of  cells  in  the  optic  lobes  and  the  cerebral  and  (probably)  the 
first  thoracic  ganglia,  while  the  storage-release  organ  is  the  sinus  gland.  In 
Insects  the  homologous  system  is  the  intercerebralis-cardiacum-allatum 
system.  Among  Myriapods,  in  the  centipede  there  is  an  organ  homologous 
to  the  x-ORGAN  of  Crustaceans  (de  Lerma,  1951)  ;  while  among  Arachnids, 
the  chromatophorotropic  principle  of  the  nervous  system  can  be  correlated 
with  similar  neuro -secretory  cells  (Brown  and  Cunningham,  1941  ;  B. 
Scharrer,  1941).  In  Xiphosurans  the  neuro -secretory  system  is  large  and 
is  of  peculiar  ophthalmological  interest  in  so  far  as  the  lateral  rudimentary 
eye  of  the  king-crab,  Limulus,  as  well  as  the  central  nervous  system,  contains 
neuro-secretory  cells  (Scharrer,  1941  ;  Waterman  and  Enami,  1954).  Among 
the  Proto-chordates,  the  neural  gland  of  Ascidians  secretes  agents  affecting 
pressor,  melanophore  and  gonadotropic  activities  and  is  thus  homologous 
with  the  pituitary  gland  of  Vertebrates  (Carlisle,  1951).  And  in  the  latter 
phylum  the  neuro-secretory  system  reaches  its  zenith  in  the  hypothalamo- 
hjrpophyseal  complex  wherein  the  posterior  lobe  of  the  pituitary  is  linked 
with  neighbourmg  hypothalamic  nuclei.  In  Crustaceans,  Insects  and  Verte- 
brates the  neuro -endocrine  system  is  of  sufficient  interest  to  merit  special 
mention. 

THE   NEITRO-BNDOCRrNE    SYSTEM    OF    CRUSTACEANS 

Since  the  discovery  cf  the  small  accumulation  of  neuro-secretory  cells 
lying  on  the  surface  of  the  optic  lobe  in  Crustaceans  by  Hanstrom  (1931) 
and  called  by  him  the  x-organ,  several  other  ganglia  have  been  described 
in  the  eye-stalks,  the  cerebral  ganglion  and  possibly  in  the  thoracic  ganglionic 
mass  whid   'nave  comparable  histological  appearances  and  functions  ;   maps 

1  p.  93. 


HORMONAL  CONTROL 


553 


of  these  secretory  areas  are  shown  in  Figs.  722  to  725,  which  also  indicate 
the  position  of  the  sinus  gland,  a  gland-like  structure  also  lying  upon  the 
eye-stalk  which  acts  as  a  storage -release  depot  for  the  secretions  of  the 
neuro-endocrine  cells  (compare  Fig.  692). 

It  is  interesting  from  the  historical  point  of  view  that  the  sinus  gland  was  first 
considered  to  be  the  secretory  organ  of  these  hormones  since  most  of  the  physiological 

Figs.  722  to  72.5. — The  Neuro-endocrine  System  of  Crustaceans. 


Fig.  722. 


Fig.  723. 


Figs.  722  and  723. — Neuro -secretory  cells  in  the  eye-stalk  of  a  Crustacean, 
Fig.  722  dorsal,  and  Fig.  723  ventral  view  of  the  right  eye-stalk  of  Camharus. 
BST,  nerve  tract  from  the  cerebral  ganglion  to  the  sinus  gland  ;   E\,  the  x-organ; 

E2-5,   clusters  of  neuro-secretory  cells  ;     LG,  lamina  ganghonaris  ;     ME,  medulla 

externa;  iV//,  medulla  interna  ;   }l/ J",  medulla  terminalis  ;   PLC,  optic  lobe  peduncle; 

SG,  sinus  gland  ;    SGT,  tract  of  sinus  gland  ;    XST,  nerve  tract  from  the  x-organ 

to  the  sinus  gland;  1,  2,  3,  fibre  tracts  (Bliss  and  Welsh). 


Fig.   724.  Fig.   72.5. 

Figs.  724  and  72.5. — Neuro-secretory  cells  in  the  cerebral  ganglion  of  a 
Crustacean. 

Fig.  724  dorsal,  and  Fig.  72.5  ventral  view  of  the  cerebral  ganglion  oi  Camharus. 

B\-5,  regions  of  neuro-secretory  cells  ;  CC,  circum-a?sophageal  connective'; 
PLO,  optic  lobe  peduncle  (Bliss  and  Welsh). 


654  THE   EYE   IN   EVOLUTION 

results  attributable  to  the  activities  of  the  endocrine  system  were  initially  demonstrated 
by  experiments  involving  the  implantation  or  excision  of  this  gland  (Perkins,  1928  ; 
Perkins  and  Snook,  1932  ;  Hanstrom,  1933-40  ;  Welsh,  1941  ;  Kleinholz,  1942  ; 
Brown,  1940-48).  Later  experiments  on  several  species,  however,  showed  that 
although  these  effects  were  frequently  dramatic  if  the  entire  eye-stalk  were  removed, 
they  were  merely  partial  or  temporary  if  this  gland  alone  were  carefully  excised 
(Kleinholz,  1948-49  ;  Havel  and  Kleinholz,  1951  ;  Travis,  1951  ;  Welsh,  1951  ; 
Passano,  1951-52  ;  Bliss,  1951-53).  Svibsequent  histological  investigation  with  the 
appropriate  technique  demonstrated  that  this  strvicture  represented  a  gland-like 
accumulation  of  enlarged  nerve-endings  associated  with  the  axons  of  neuro -secretory 
cells  located  in  the  x-organ  and  elsewhere  in  the  eye-stalks  and  cerebral  ganglion, 
indicating  that  the  real  role  of  the  sinus  gland  is  a  storage -release  centre  of  the  colloid- 
like secretion  of  the  cells  of  the  neuro -secretory  system  (Bliss  and  Welsh,  1952  ; 
Carlisle,  1953  ;    Bliss  et  al.,  1954). 

The  functions  of  the  hormones  secreted  by  the  neuro -endocrme  system 
of  Crustaceans  are  complex  ;  those  of  greatest  interest  to  us  concern  the 
integumentary  and  retinal  pigmentation.  In  most  cases  there  is  no  precise 
knowledge  of  the  nature  of  these  hormones  or  the  site  of  their  elaboration 
within  the  many  ganglionic  masses  comprising  the  system.  The  integumen- 
tary chromatophores  are  regulated  by  three  or  four  different  chromato- 
PHOROTROPINS,  soHie  of  wliich  determine  the  concentration  of  pigment, 
others  its  dispersal.  These  have  already  been  discussed  ^  but  it  may  be 
useful  to  recapitulate  here  that  the  release  of  these  hormones  is  regulated 
by  the  degree  of  illumination  and  the  nature  of  the  background  ;  the 
receptor  organs  are  the  retinse,  differential  stimulation  of  the  dorsal  or 
ventral  areas  of  which  may  determine  the  release  of  different  hormones  so 
that  adaptation  to  the  background  is  attained. 

In  addition  to  these  environmental  variations,  we  have  already  seen  ^ 
that  in  many  species  a  diurnal  rhythmic  release  of  the  hormones  causes  a 
dispersal  of  pigment  by  day  and  its  concentration  by  night,  a  habit  which 
tends  to  persist  in  spite  of  artificial  disturbances  of  the  natural  day-night 
sequence  ;  this  rhythmic  behaviour  is  an  acquirement  of  the  neuro -secretory 
centres  (Roller,  1925-30  ;   Perkins,  1928  ;  Brown,  1940-46  ;  and  others). 

Betinal  2iigi'nentation  is  under  the  control  of  at  least  two  chromato- 
phorotropins  of  an  unknown  chemical  nature  different  from  those  responsible 
for  changes  in  the  colour  of  the  integument,  one  regulating  pigment  migration 
in  the  dark,  the  other  in  the  light.  Here  again,  illumination  and  background 
are  the  determining  factors  rn  the  release  of  the  hormones  and  the  effect  is 
abolished  if  the  optic  nerve  is  cut  (Smith,  1948  ;  Sandeen  and  Brown, 
1951-52)  ;  the  hormone  regulating  pigmentary  migration  in  the  dark  is  often 
liberated  in  a  persistent  diurnal  rhythm  which  gives  a  basic  24-hour  variation 
to  this  activity  also  ^  (Welsh,  1939-41  ;  Brown,  1951  ;  Brown  et  al,  1951). 
In  the  prawn,  Leander,  it  appears  that  migration  of  the  distal  retinal 
pigment  depends  on  the  hormones  of  the  sinus  gland  modified  by  illumination, 

1  p.  93.  2  p  i9_  3  p,  19. 


HORMONAL   CONTROL  555 

while  the  proximal  retinal  pigment  is  independent  of  it  (Knowles,  1949-50). 
So  far  as  the  migration  of  the  former  is  concerned,  the  most  likely  hj^jothesis 
is  that  pigmentary  migration  is  determined  primarily  by  a  dark-adapting 
and  a  light -adapting  hormone,  the  production  of  both  being  regulated  by  a 
nervous  centre  (in  the  prawn,  Palcemonetes,  Brown  et  al.,  1952-53). 

Rej)rodiiCtion  in  Crustaceans  is  controlled  by  hormones  differing  totally 
in  nature  from  the  chromatophorotropins  (Matsumoto,  1951  ;  Stephens, 
1952)  and  is  of  considerable  ophthalmological  interest  since,  as  we  have  seen,^ 
the  sexual  cycle  is  frequently  influenced  through  the  eyes  by  photo- 
periodism.  In  prawns  {Leander — Panouse,  1943-46),  crabs  and  crayfish 
(Brown  and  Jones,  1947-49),  such  a  hormone  inhibits  ovarian  maturation 
and  oogenesis,while  excision  of  the  gland  in  crabs  results  in  arrested  feminiza- 
tion or  increased  testicular  development  (Demeusy  and  Veillet,  1952  ; 
Demeusy,  1953  ;  Cornubert  et  al.,  1952-53  ;  Veillet  et  al.,  1953  ;  Cornubert 
and  Demeusy,  1955). 

The  control  of  growth  and  moulting  are  similarly  determined  (Bliss,  1951  ;  Havel 
and  Kleinholz,  1951  ;  Passano,  1951  ;  Stephens,  1955  ;  and  others),  and  in  association 
with  the  moulting  cycle  there  is  a  hormonal  regulation  of  the  metabolism  of  calcium  and 
phosphorus  (Kuntz,  1951  ;  Travis,  1951),  sugar  (Kleinliolz,  1950  ;  Scheer  and  Scheer, 
1951)  and  the  rate  of  oxygen  consumption  (Bliss,  1951  ;    Frost  et  al.,  1951). 

THE    NEURO-ENDOCRINE    SYSTEM    OF    INSECTS 

The  headquarters  of  the  neuro -endocrine  system  of  Insects  is  a  cluster 
of  neuro -secretory  cells  in  the  pars  intercerebralis  of  the  protocerebrum 
(Fig.  720)  ;  their  occurrence,  discovered  first  in  Hymenoptera  by  Weyer 
(1935),  has  been  confirmed  in  a  large  number  of  species,^  and  in  addition 
similar  groups  of  cells  have  been  found  not  only  in  the  cerebral  but  also  in 
the  frontal  and  the  sub-oesophageal  as  well  as  in  some  abdominal  ganglia 
(Day,  1940  ;  B.  Scharrer,  1941).  In  relation  with  these  cells,  situated  on 
the  dorsal  aspect  of  the  cerebral  ganglion,  are  two  paired  gland-like  organs, 
the  CORPUS  CARDiACUM  and  the  corpus  allatum,  both  closely  associated 
in  most  insects  and  m  some  macroscopically  inseparable  ;  the  first  is 
comprised  of  both  nervous  and  glandular  tissue,  the  second  is  without  nervous 
components  so  that  they  are  somewhat  analogous  to  the  posterior  and 
anterior  lobes  of  the  pituitary  body  of  Vertebrates  (Hadorn,  1937  ;  Scharrer 
andHadorn.  1938  ;  Vogt.  1942  ;  Bodenstein,  1943-44  ;  and  others).  These 
three  components  form  one  neuro -endocrine  complex,  the  corpus  cardiacum 
being  linked  directly  with  the  cerebral  centre  by  large  nerve-trunks  carrying 
neuro -secretory  material  (Pflugfelder,  1937  ;  Hanstrom,  1940  ;  Nesbitt, 
1941  ;   Thomsen,  1954). 

The  control  of  integumentary  coloration  by  chromatophorotropins  in 

1  p.  16. 

^  Hymenoptera  (bees,  wasps,  ants) — E.  and  B.  Scharrer  (1937);  Heiniptera  (bugs) — 
Wigglesworth  (1939-40)  ;  Lepidoptera  (butterflies) — Day  (1940)  ;  Coleoptera  (beetles), 
Trichoptera  (caddis-flies),    Diptera  (flies) — Day  (1940),  Vogt  (1942),  and  others. 


556 


THE   EYE   IN   EVOLUTION 


Insects  is  limited  to  a  small  number  of  species,  and  the  mechanism  whereby 
it  is  achieved  is  relatively  unexplored.  The  evidence  suggests,  however,  that 
the  main  source  of  the  hormones  is  the  cerebral  ganglion  since  its  extirpation 
inhibits  colour  adaptation  and  the  injection  of  extracts  redistributes  the 
integumentary  pigment  [Carausius — Dupont-Raabe,  1949-51).  The  hor- 
mones appear  to  be  distributed  through  the  agency  of  the  corpora  cardiaca 
while  the  allata  seem  to  be  inactive  in  the  process  (B.  Scharrer,  1952).  In 
some  species  the  eyes  are  the  sole  receptors  of  the  stimulation  and  their 
occlusion  or  section  of  the  optic  tracts  inhibits  all  responses  (the  stick 
insect,   Dixippus — Atzler,    1930).     The  diurnal  rhythm  in  the  migration 


COBDUS  ALLATUM , 


COKOiJi  CAQOJACUM 


rJCavUS  COftPOK/S  CAODIACI 


Fig.  726. — The  Neuro-secretory  System  of  an  Insect. 
A  general  diagrammatic  representation  (B.  and  E.  Scharrer,  1944). 

of  the  retinal  pigment  of  some  species  suggests  that  here,  also,  an  endocrine 
control  may  be  active  ^  (the  noctuid  moth,  Plusia  gamma — Kiesel,  1894  ; 
the  beetle,  Bolitotherus  cornutus — Park  and  Keller,  1932). 

The  important  gonadotrojjic  hormones  controlUng  reprodvictive  processes  and  the 
development  of  the  sex  organs  are  elaborated  mainly  in  the  corpora  allata  which  in 
some  species  may  be  under  the  control  of  the  cerebral  ganglion  (Altmann,  1952  ;  B. 
Scharrer,  1952),  while  the  complicated  processes  oi  growth,  moulting  and  differentiation 
with  all  their  spectacular  changes  are  integrated  by  hormones  mainly  elaborated 
in  the  prothoracic  gland. ^  Metabolic  processes  such  as  oxygen  consumption  are  effected 
through  the  pars  intercerebralis  and  the  corpora  allata  (Thomsen,  1949-52). 


THE    NEIJRO-ENDOCRINE    SYSTEM    OF    VERTEBRATES 

The  neuro -endocrine  mechanism  of  Vertebrates  is  centred  in  the 
extrenH'ly  complex  aggregation  of  nuclei  and  secretory  organs  known  as  the 
hypotlia-mio-hypophyseal  system  ;  from  the  hormonal  point  of  view  the 
most  interesting  section  in  this  part  of  the  central  nervous  system  is  the 


1  p.  l!i 
^  Revie, 


ee  Wigglesworth,  1934-40  ;   Bodenstein,  1942  ;   B.  Scharrer,  1953. 


HORMONAL   CONTROL 


557 


NEUROHYPOPHYSIS.  Several  of  the  hypothalamic  nuclei  are  made  up  of 
typical  neuro -secretory  cells  for  which  the  posterior  lobe  of  the  pituitary 
body  (pars  nervosa)  and  the  median  eminence  of  the  pituitary  stalk  serve 
as  a  storage -release  organ  (Fig.  727)  (Scharrer  and  Scharrer,  1945  ;  Weiss 
and  Hiscoe,  1948  ;  S.  W.  Smith,  1951  ;  Zuckerman,  1954  ;  van  Dyke  et  al., 
1955  ;  and  others).  The  posterior  lobe  of  the  pituitary  is  thus  homologous 
with  the  corpus  cardiacum  of  Insects,  the  anterior  (non-nervous)  lobe  with 
the  corpus  allatum.  In  Fishes  the  essential  centres  of  this  endocrine  function 
are  two  paired  nuclei — the  nucleus  pre -opticus  and  the  nucleus  lateralis 


-Pf^Rf^BNTRICULAR    NUCLEUS 
■  SUPRA-OPTIC     NUCLEUS 


Fig.  727.- 


PROCESSUS 
INFUNDieULARfS 


POSTAL    VESSELS 

-The  Neuro-endocrine  System  of  a  Primate. 


Diagram  to  indicate  the  relations  of  the  pituitary  gland  to  the  hypothalamus  (after 

Zuckerman). 

tuberis  (E.  Scharrer,  1928  ;  Palay,  1943-45)  ;  in  Amphibia  the  nucleus 
pre-opticus  alone  (E.  Scharrer,  1933  ;  Gaupp  and  Scharrer,  1935)  ;  in 
Reptiles  the  two  divisions  of  the  nucleus  pre-opticus  are  involved — the 
supra-optic  and  paraventricular  nuclei  (Gaupp  and  Scharrer,  1935)  ;  and  in 
Mammals  to  these  may  possibly  be  added  a  third  group  of  cells,  the  mammillo- 
infundibular  nucleus  ^  (S.  W.  Smith,  1951  ;  Hanstrom,  1952-53  ;  Zetler, 
1953  ;  and  others)  ;  all  of  these  are  connected  to  the  pars  nervosa  of  the 
pituitary  and  the  cells  of  the  median  eminence  of  the  stalk  by  the  hypo- 
thalamo -hypophyseal  tract  to  form  the  neurohypophysis.  The  possibility 
of  the  existence  of  secretory  cells  in  the  posterior  lobe  of  this  composite 
organ,  either  in  the  pars  nervosa  or  the  pars  intermedia,  is  a  matter  which 

^  These  three  nuclear  masses,  made  up  of  large  vacuolated  cells  with  eccentric  nuclei, 
form  the  anterior  group  of  hypothalamic  nuclei.  The  supra-optic  nucleus  lies  close  to  the 
pituitary  stalk  immediately  above  the  optic  chiasma  at  the  anterior  end  of  the  optic  tract 
and  projects  a  sliort  distance  along  the  anterior  aspect  of  the  tuber  cinereum.  The  neighbour- 
ing paraventricular  nucleus  is  a  flat  plate  lying  close  against  the  ependymal  lining  of  the 
thircl  ventricle.  The  mammiUo-infundihular  nucleus  is  close  to  the  cephalic  end  of  the  supra- 
optic nucleus. 


558  THE   EYE   IN   EVOLUTION 

requires  further  elucidation,  as  also  does  the  mechanism,  if  any,  whereby  the 
hypothalamus  may  control  the  anterior  lobe  of  the  pituitary  body  (see 
Zuckerman,  1954). 

The  activities  of  the  neuro -endocrine  system  in  Vertebrates  as  centred  in 
the  hypothalamo -hypophyseal  complex  are  extraordinarily  extensive  and 
varied,  for  the  hypothalamic  nuclei  exercise  a  supervisory  control  over  most 
of  the  other  endocrine  organs.  They  take  direct  control  of  the  pituitary 
body  itself  with  its  immense  influence  on  the  processes  of  pigmentation, 
growth,  diuresis  and  intermediary  metabolism  and  its  vasopressor  and 
oxytocic  effects  ;  in  addition,  they  exercise  a  quick-working  stimulation  of 
the  adrenal  medulla  through  the  sympathetic,  and  through  the  medium  of 
the  23ituitary  they  exert  a  slow-working  control  over  a  host  of  endocrine 
activities,  stimulating  the  thyroid  by  means  of  the  thyrotropic  hormone,  the 
steroids  of  the  adrenal  cortex  through  adrenocorticotropic  hormones,  as 
well  as  controlling  the  development  of  the  sex  organs  and  the  reproductive 
rhythms  through  the  gonadotropic  hormones.  The  holistic  nature  of 
endocrine  balance  is  seen  in  the  feed-back  from  these  peripheral  organs  to 
the  hypothalamus  by  hormones  of  opposing  nature  which  inhibit  the  exces- 
sive production  of  those  stimulatory  agents  by  the  neuro -endocrine  system. 
Most  of  these  activities  do  not  affect  the  eye  ;   but  some  do. 

The  role  of  hormonal  control  over  the  integume^itary  pigment  of  Fishes, 
Amphibians  and  Reptiles  has  already  been  discussed  at  length. ^  It  will  be 
remembered  that  environmental  changes  in  many  species  are  effected  solely 
by  the  control  of  mutually  antagonistic  hormones  associated  with  the 
pituitary,  the  release  of  which  is  determined  by  stimuli  operating  through 
the  eyes  (Cyclostomes,  Selachians,  Amphibians  ^  and  some  Reptiles)  ; 
in  other  species  a  nervous  control  is  partially  (Teleosts)  or  entirely  (chameleon) 
responsible.  Similarly,  the  cyclic  diurnal  variation  of  the  coloration  which 
occurs  in  many  of  these  tjrpes — Cyclostomes  such  as  the  lampern.  Amphibians 
such  as  salamander  larvse  and  frogs,  and  Reptiles  such  as  the  lizard,  Anolis, 
the  chameleon  and  the  American  horned  "  toad,"  Phrynosoma — is  due  to 
the  rhythmic  release  of  the  appropriate  hormones  by  the  pituitary  under 
the  control  of  its  associated  hypothalamic  centres.  Hypophysectomy 
abolishes  the  darkening  and  lightening  of  the  skin  of  the  frog  (Hogben,  1924), 
and  in  the  lizard,  Anolis,  suppresses  the  rhythmic  change  from  brown 
during  the  night  to  green  during  the  day  (Rahn  and  Rosendale,  1941). 

In  a  similar  manner  there  is  evidence  that  the  pigmentation  of  the  iris  in  the  frog 
is  influenced  by  the  hypophysis  (del  Castillo,  1955). 

The  migration  of  the  retinal  pigment  of  Vertebrates  ^  is  essentially  a  direct  response 
to  light  and,  unlike  that  of  Crustaceans,  shows  little  indication  of  hormonal  control. 

1  p.  06. 

-  After  removal  of  the  eyes  from  the  toad,  Bujo,  some  of  the  responses  of  the  melanophores 
to  illmninati'd  backgrounds  persist,  perhaps  due  to  the  direct  action  of  light  on  the  hypo- 
thalamus (}.    '8). 

»  p.  61. 


HORMONAL   CONTROL  559 

Some  evidence,  however,  has  been  made  available  in  the  frog.  Derman  (1949)  found 
that  while  hyiDophysectomy  had  no  effect  on  the  retraction  of  the  retinal  pigment 
during  dark-adaptation,  it  slowed  but  did  not  inhibit  the  migration  of  pigment  during 
light  adaptation,  while  injection  of  an  extract  of  the  intermediate  lobe  of  the  pituitary 
body  provoked  the  migration  characteristic  of  light-adaptation  in  the  dark-adapted 
hypophysectomized  frog.  This  action  was  abolished  after  section  of  the  optic  nerve. 
Damage  to  the  hypothalamus  has  also  been  said  to  influence  the  migration  of  the 
retinal  pigment  in  this  animal  (Kitashoji,  1953  ;  Nakamura,  1954),  an  effect  also  shared 
by  epinephrine  (Nakamura,  1955)  and  Pregnenolone,  a  relation  of  the  adrenal  cortico- 
steroids (Paiynarale,  1952).  It  is  clear,  however,  that  nervous  influences  predominate 
over  any  effect  that  may  be  exercised  by  the  pituitary-hypothalamic  system  in 
Amphibians. 

In  the  higher  Vertebrates  any  such  effect  is  even  more  insignificant.  It  may, 
however,  be  of  interest  that  Rubino  and  Pereyra  (1948-50)  have  claimed  that 
the  degree  of  light -sensitivity  in  man  undergoes  a  diurnal  rhythm,  being  increased 
during  the  night  ;  the  fact  that  this  faculty  is  maintained  unimpaired  in  the  amblyopic 
eye  or  in  patients  affected  by  primary  pigmentary  degeneration  suggests  that  this 
cyclic  change  is  centrally  determined.  There  is,  indeed  a  considerable  body  of  opinion 
which  maintains  that  this  latter  disease  may  sometimes  be  associated  primarily  with 
a  hypothalamic-endocrine  disturbance,  the  most  dramatic  instance  of  which  is  seen 
in  the  Laurence-Moon-Biedl  syndrome  (see  Zondek  and  Koehler,  1932  ;  Zondek  and 
VVolfsohn,  1940  ;    Alajmo  and  Rubino,  1952). 

The  gonadotropic  action  of  the  hormones  elaborated  in  the  anterior  lobe 
of  the  j^itiiitar}'  in  Vertebrates  is  well  established, ^  both  in  determining  the 
development  of  the  organs  of  sex  and  governing  the  cyclic  activities  of 
reproduction.  The  rate  and  rli}i:hmic  variation  of  the  secretion  of  the 
gonadotropic  hormone  in  Mammals  are  regulated  by  the  tuber  nuclei  of  the 
hj'jjothalamus,  isolated  injuries  to  which  have  caused  sexual  disturbances 
in  all  Mammals  so  far  studied  -  ;  delicacy  of  adjustment  and  integration  is 
thus  achieved  and  in  the  absence  of  this  nervous  control  the  secretion 
continues  without  coordinated  balance.  In  many  Vertebrates  the  sexual 
rhythm  is  adapted  to  the  most  favourable  season  of  the  annular  solar  cycle 
and  one  of  the  most  potent  influences  in  determining  this  process  is  light. 
We  have  already  seen  ^  that  the  sexual  maturation  of  many  Fishes,  Reptiles, 
Birds  and  Mammals  is  determined  in  this  way  by  jjhotoperiodism,  and  that 
the  process  can  be  accelerated  or  retarded  by  altering  the  relative  duration 
of  light  and  darkness  in  the  diurnal  cycle.  In  most  cases  the  stimulus  is 
retinal  in  origin  and  neural  in  conduction  along  the  optic  nerve  and  is  relayed 
not  to  the  visual  centres  of  the  brain  but  to  the  h;y|3othalamus  which 
activates  the  j^ituitary  (Le  Gros  Clark  et  ol.,  1937-39)  ;  and  blinding, 
hypophysectomy  or  section  of  the  nervous  connections  between  the 
hypothalamus  and  the  jjituitary  destroys  the  cycle,  while  the  injection  of 
pituitary  extract  activates  it  (Hill  and  Parkes,  1933  ;  Thomson,  1951-54  ; 
Thomson  and  Zuckerman,  1953-54  ;   Donovan  and  Harris,  1956).    In  some 

1  For  reviews,  see  Allen  (1939),  Burrows  (1949),  Brown  (1950),  Galgano  and  Mazzi  (1951). 

2  Guinea-pig,  rabbit,  ferret — Brooks  (1938-40),  Bard  (1940),  and  others. 
»  p.  16. 


560  THE   EYE   IN   EVOLUTION 

Birds,  on  the  other  hand,  and  perhaps  in  some  Mammals,  hght  appears  to 
activate  the  pituitary  or  the  central  nervous  system  directly,  perhaps  through 
the  spectral  sensitivity  of  a  coproporphyrin  (Parker  et  al.,  1952). ^  In  ducks, 
for  example,  Benoit  and  his  collaborators  (1952-54)  have  shown  that  light, 
concentrated  as  it  traverses  the  eye,  travels  through  the  orbit  and  reaches 
the  hypothalamus,  thus  regulating  the  gonadotropic  action  of  the  hypo- 
physis ;  excision  of  both  eyes  does  not  inhibit  but,  by  increasing  trans- 
missibility,  rather  enhances  the  gonadotropic  activity,  and  the  pituitary 
body  of  immature  ducks  stimulated  by  increased  illumination  can  excite 
cestrus  when  implanted  into  immature  mice. 

The  seasonal  migrations  associated  with  the  sexual  cycle  of  Birds  and 
Mammals  is  similarly  controlled  by  photoperiod,^  as  well  as  the  seasonal 
moults  and  changes  of  colour  in  the  feathers  or  hair  of  many  Birds  or 
Mammals.^  In  these  cyclic  changes  the  pituitary  is  the  most  potent  factor 
(Witschi,  1935  ;  Brown  and  Rollo,  1940  ;  Lesher  and  Kendeigh,  1941  ; 
Kobayashi  and  Okubo,  1955)  ;  similarly,  hypophysectomy  abolishes  the 
cyclic  moulting  of  ferrets  (Bissonnette,  1935-38).  It  would  seem,  indeed, 
that  the  pituitary  is  the  only  endocrine  organ  involved  in  these  activities 
in  Mammals  since  castration  or  thyroidectomy  has  no  such  effect  on  the 
varying  hare  (Lyman,  1943). 

The  influence  of  the  hypothalamo -hypophyseal  system  on  the  growth,  meta- 
morphosis and  metabolism,  of  Vertebrates  and  its  pressor  effects  on  the  circulation  are 
potent  but  are  without  marked  interest  in  our  survey  of  the  development  of  the  visual 
system.  An  associated  optic -diencephalic  relationship,  however,  may  be  seen  in  the 
observation  that  in  the  rabbit  exposure  to  light  increases  the  urinary  excretion  of 
17-ketosteroids  (Siliato,  1955).  Another  exception  niay  be  constituted  by  the  photo- 
glyccemic  reflex  recently  explored  by  Italian  workers  but  not  otherwise  investigated. 
It  was  originally  claimed  by  Cavallacci  (1937)  that  stimulation  of  the  retina  by  light 
altered  the  metabolism  of  sugar,  the  blood -sugar  curve  being  normally  different  if  the 
sugar  were  ingested  by  day  or  by  night.  This  finding  has  been  confirmed  by  Bassi 
(1945)  and  Rubino  and  his  collaborators  (1948)  who  concluded  that  abnormalities 
occurred  in  persons  affected  by  glaucoma  and  primary  pigmentary  degeneration  of 
the  retina,  both  of  which  diseases  may  have  hypothalamic  implications.  In  this 
connection  the  suggestion  that  dark-adaptation  is  impaired  in  adiposo -genital 
dystrophy,  a  disease  associated  with  hypothalamic  disturbances,  may  possibly  be  of 
interest  (Landau  and  Bromberg,  1955). 

A  relationship,  still  vague  but  yet  undoubted,  exists  between  the  intra-ocular 
pressure  and  the  endocrine  system,  particularly  the  hypothalamo -hypophyseal  complex, 
and  claims  have  been  put  forward  from  time  to  time  that  primary  glaucoma  is  often 
an  expression  of  a  diencephalic  disturbance  (Hess,  1945  ;  Zondek  and  Wolfsohn, 
1947  ;  Magitot,  1947  ;  Alajmo  and  Rubino,  1952  ;  and  many  others).  The  pupillary 
changes  described  by  Lowenstein  and  Schoenberg  (1944)  point  to  some  neurogenic 
sympathetic  disturbance  in  this  region  of  the  brain  in  this  disease.  That  a  hypo- 
thalamic  centre  exercises  some  control  over  the  intra-ocular  pressure   is  clear   (v. 

*  Ivanova  (1935)  produced  evidence  that  the  skin  may  also  be  a  possible  receptor  in  the 
house  span  iw,  Passer  domesticus. 
'  p.  16. 
^  p.  21. 


HORMONAL   CONTROL 


561 


Sallmann  and  Lowenstein,  1955  ;  Gloster  and  Greaves,  1957),  an  influence  which  is 
probably  responsible  for  the  cyclic  diurnal  variations  in  the  normal  intra-ocular  pres- 
sure and,  in  part  perhaps,  for  the  exaggeration  of  those  variations  that  characterize 
primary  glaucoma  (see  Duke-Elder,  1952-7)  ;  but  whether  its  action  is  mediated  by 
nervous  or  hormonal  factors  or  both  is  still  unknown.  Hypei-pituitarism  has  been 
most  commonly  associated  with  ocular  hypotony  (Imre,  1921  ;  Marx,  1923),  while 
the  reputed  cyclic  variation  of  the  ocular  tension  with  the  menstrual  cycle  or  in 
association  with  pregnancy,  falling  in  the  progestational  phase  of  both  and  rising  in 
the  oestrogenic  post -menstrual  period  or  after  delivery,  is  suggestive  (Salvati,  1923  ; 
Marx,  1923  ;  Becker  and  Friedenwald,  1953),  as  also  is  the  reported  reduction  of 
tension  in  glaucomatous  patients  by  progesterone  (Obal,  1950  ;  Posthumus,  1952  ; 
Becker  and  Friedenwald,  1953  ;  and  others).  The  most  positive  assertion  has  been 
made  by  Schmerl  and  Steinberg  (1948)  and  Schmerl  (1955)  who  claimed  that  the 
spinal  fluid  of  rabbits  contained  two  active  principles,  presumably  secreted  by  the 
posterior  lobe  of  the  pituitary  body  into  the  third  ventricle,  one,  acting  on  para- 
sympathetic centres  ("  hyperpiesine  "),  raising,  the  other,  acting  on  sympathetic 
centres  ("  miopiesine  "),  lowering  the  intra-ocular  pressvire.  In  the  rabbit  (a  nocturnal 
animal)  the  intra-ocular  pressure  is  said  to  increase  during  light  and  to  fall  during 
darkness  because  of  this  mechanism  ;  in  man  (a  diurnal  animal)  the  reverse  occurs. 
More  experimental  investigation,  however,  is  requu'ed  to  substantiate  these  claims 
which  are  still  somewhat  nebulous  and  are  not  yet  based  on  unequivocal  evidence. 
As  in  other  spheres  of  physiology  and  pathology,  our  knowledge  of  the  complex  and 
far-reaching  influence  of  the  diencephalic-hypophyseal  system  upon  the  vegetative 
physiology  of  the  eye  is  still  in  an  elementary  stage. 


Alajmo    and    Rubino.      Fisiopath.    e    clinica 

oculo-diencefalica,  Torino  (1952). 
Allen.       Sex     and     the     Internal    Secretions, 

Baltimore  (1939). 
Altmann.     Bienenforsch,  1,  124  (1952). 
Atzler.     Z.  vergl.  Physiol.,  13,  505  (1930). 
Bard.     Res.  Publ.  Ass.  nerv.  ment.  Dis.,  20, 

551  (1940). 
Bargmann.     Z.  Zellforsch.,  34,  610  (1949). 
Bassi.     Rass.  Neurol.  Veg.,  4-5,  1  (1945). 
Becker    and    Friedenwakl.      Arch.    Ophthnl. 

(Chicago),  50,  557  (1953). 
Benoit  and  Assenmacher.     C.  R.  Acad.  Sci. 

(Paris),    236.    2002    (1953)  ;     239,     105 

(1954). 
Benoit,    Assenmacher    and    Manuel.      C.    R. 

Acad.  Sci.  (Paris),  235,  1695  (1952). 
C.  R.  Soc.  Biol.  (Paris).  147,  40  (1953). 
Benoit,  Assenmacher  and  Walter.    C.  R.  Soc. 

Biol.  (Paris),  147,  186  (1953). 
Benoit,  Tauc  and  Assenmacher.    C.  R.  Acad. 

Sci.  (Paris),  239,  451,  508  (1954). 
Bernard,   Claude.      Le<;ons  sur  les  proprictes 

physiol.     et     les    cdterations    pathol.     des 

liquides  de  Vorganism,  Paris  (1859). 
Bissonnette.     Anat.  Rec,  63,  159  (1935). 

Endocrinology.  22,  92  (1938). 
Bliss.    Anat.  Rec,  111,  502  (1951). 

Endocrine    Control    of    Metabolism    in    the 

Decapod  Crustacean,  Gecarcinus  lateralis. 

Thesis,  Radcliff  Coll  (1952). 
Biol.  Bull.,  104,  275  (1953). 
Bliss,  Durand  and  Welsh.     Z.  Zellforsch.,  39, 

520  (1954). 
Bliss  and  Welsh.    Biol.  Bull.,  103,  157  (1952). 

S.O.— VOL.  I. 


Bobin  and  Durchon.     ^4rc^.  Anat.   micr.,  41, 

25  (1952). 
Bodenstein.     Cold  Spr.   Harb.  Syvip.   qiiant. 
Biol..  10,  17  (1942). 
Biol.  Bull.,  84,  34  (1943)  ;    86,  113  (1944). 
Brooks.     Arner.  J.  Physiol.,  121,  157  (1938). 
Res.   Publ.  Ass.  nerv.  ment.   Dis.,  20,   525 
(1940). 
Brown.     Physiol.  Zool.,  13,  343  (1940)  ;    19, 
215  (1946). 
Quart.  Rev.  Biol.,  19,  32,  118  (1944). 
The  Hormones,  New  York,  1,  159  (1948). 
Prosser's  Comparative  Animal   Physiologu, 

Phila.,  677  (1950). 
Anat.  Rec,  111,  442  (1951). 
The    Action    of   Hormones    in    Plants    and 
Invertebrates,  New  York,  171  (1952). 
Brown  and  Ctmningham.     Biol.  Bull.,  81,  80 

(1941). 
Brown  and  Fingerman.     Fed.  Proc,  10,  20 

(1951). 
Brown,  Fingerman  and  Hines.      Biol.  Bull., 
101,  217  (1951)  ;    102,  212  (1952). 
Physiol.  Zool.,  25,  230  (1952). 
Brown   and    Hines.      Physiol.    Zool.,   25,    56 

(1952). 
Brown  and  Jones.    Anat.  Rec,  99,  657  (1947). 

Biol.  Bull.,  96,  228  (1949). 
Brown  and  Rollo.     The  Auk.,  57,  485  (1940). 
Brown,  Sandeen  and  Webb.    Anat.  Rec,  111, 

569  (1951). 
Brown  and  Stephens.      Biol.   Bull.,   101,   71 

(1951). 
Brown,  Webb  and   Sandeen.     J.   cell.  comp. 
Physiol.,  41,  123  (1953). 


562 


THE   EYE   IN   EVOLUTION 


Burrows.   Biological  Action  of  Sex  Hormones, 

Cantab.  (1949). 
Cailahian.     G.    R.   Acad.  Sci.    U.R.S.S.,   27, 

160,  253,  374  (1940). 
Carlisle.    J.  exp.  Biol.,  28,  463  (1951). 
Quart.  J.  micr.  Sci.,  92.  201  (1951). 
C.  R.  Acad.  Sci.  (Paris),  236,  2541  (1953). 
del  Castillo.    Arch.  Soc.  oftal.  hisp. -artier.,  15, 

637  (1955). 
Cavallacci.    Arch.  Ottal.,  44,  101  (1937). 
Clark,  McKeown  and  Zuckerman.    J.  Anaf. 

(Lond.),  72,  152  (1937). 
Proc.  roy.  Soc.  B,  126,  449  (1939). 
Cornubert.      C.    R.   Acad.   Sci.    (Paris),   236, 

1082  (1953). 
Cornubert  and  Demeusy.     C.   R.  Acad.  Sci. 

(Paris),  240,  360  (1955). 
Cornubert,  Demeusy  and  Veillet.    C.  R.  Acad. 

Sci.  (Paris),  234,  1405  (1952). 
Dahlgren.  Science,  40,  862  (1914). 
Day.    Nature  (Lend.),  145,  264  (1940). 

Atiat.  Rec,  78,  Suppl.,  364  (1940). 
Demeusy.  C.  R.  Acad.  Sci.  (Paris),    236,  974 

(1953). 
Demeusy    and    Veillet.      C.    R.    Acad.    Sci. 

(Paris),  234,  1224  (1952). 
Derman.    Istanbul  Univ.  Tip.  Fak.  Mecmuasi, 

12,  88  (1949). 
Donovan  and  Harris.     J.  Physiol.,  131,   102 

(1956). 
Duke-Elder.    Amer.  J.  Ophthal.,  35,  1  (1952). 
Trans,  ophthal.  Soc.  U.  K.,  77,  205  (1957). 
Dupont-Raabe.    C.  R.  Acad.  Sci.  (Paris),  228, 

130  (1949)  ;    230,  873  (1950)  ;    232,  886 

(1951). 
Durchon.     C.  R.  Acad.  Sci.  (Paris),  232,  442 

(1951). 
van  Dyke,  Adamsons  and  Engel.     Rec.  Prog. 

Hormone  Res.,  11,  1  (1955). 
Fitting.     Z.  Botan.,  2,  225  (1910). 
Frost,  Saloum  and  Kleinholz.  Anat.  Rec,  111, 

572  (1951). 
Gabe.     C.   R.  Soc.    Biol.    (Paris),   229,    1172 

(1949)  ;   236,  323,  2166  (1953). 
Galgano  and  Mazzi.    Riv.  Biol.,  43,  21  (1951). 
Gaupp     and     Scharrer.        Z.     ges.     Neurol. 

Psychiat.,  153,  327  (1935). 
Gloster  and  Greaves.     Brit.  J.  Ophthal.,  41, 

513  (1957). 
Gomori.    Amer.  J.  Path.,  17,  395  (1941). 
Hadorn.    Proc.  nat.  Acad.  Sci.,  23,  478  (1937). 
Hanstrdm.     Z.  Morphol.  Oekol.  Tiere,  23,  80 

(1931). 
Zool.  Jb.,  Abt.  Anat.,  56,  387  (1933)  ;  58, 

101  (1934). 
Psychiat.  neurol.  BL,  Amst.,  38,  405  (1934). 
Ark.  Zool.  Stockholm,  26A,  No.  24  (1934)  ; 

4,  187  (1952). 
Proc.  nat.  Acad.  Sci.,  21,  584  (1935). 
Kunql.  Svensk.   Vetensk.  Akad.  Handl.,  16, 

1  (1937)  ;   18  (8),  1  (1940). 
Kungl.  Fijsiogr.  Sallsk.  Handl.,  22,  1  (1952). 
Z.  Zellf'jrsch.,  39,  241  (1953). 
Havel  and   Kleinholz.     Anat.  Rec,  111,  571 

(1951). 
Hess.   Arch . '  iphthal.  (Chicago),  33,  392  ( 1 945). 


Hill  and  Parkes.    Proc.  roy.  Soc.  B,  113,  530, 

537,  541  (1933)  ;    115,  14  (1934). 
Hogben.      The    Pigmentary   Ejfector  System., 

Edin.  (1924). 
Imre.     Orv.  Hetil.,  64,  291  (1920). 
Zbl.  ges.  Ophthal.,  4,  14  (1921). 
Ivanova.     Arch.   exp.   Path.   Pharmak.,  179, 

349  (1935). 
Kiesel.     S.   B.   Akad.    Wiss.    Wien.,   103.   97 

(1894). 
Kitashoji.     Acta  Soc.   ophthal.  jap.,   57,   862 

(1953). 
Kleinholz.     Biol.  Rev.,  17,  91  (1942). 
Anat.  Rec,  101,  665  (1948). 
Proc  nat.  Acad.  Sci.,  35,  215  (1949). 
Biol.  Bull.,  99,  454  (1950). 
Knowles.    Nature  (Lond.),  164,  36  (1949). 

Biol.  Bull.,  98,  66  (1950). 
Kobayashi    and    Okubo.      Science,    121,    338 

(1955). 
Roller.     Verh.  dtsch.  zool.  Ges.,  30,  128  (1925). 
Z.  vergl.   Physiol.,  5,    191    (1927)  ;    8,   601 

(1928)  ;    12,  632  (1930). 
Kuntz.     Fed.  Proc,  10,  77  (1951). 
Landau  and  Bromberg.    Brit.  J.  OphtJial.,  39, 

141  (1955). 
de  Lerma.      Annnar.    1st  Mus.   Zool.    Univ. 

Napoli,  3,  1  (1951). 
Lesher  and  Kendeigh.     Wilson  Bull.,  53,  169 

(1941). 
Lowenstein  and  Schoenberg.     Arch.  Ophthal. 

(Chicago),  31,  384,  392  (1944). 
Lyman.      Bull.  Mus.  comp.   Zool.,  Harvard, 

93,  391  (1943). 
Magitot.    Ann.  Oculist.  (Paris),  180,  1  (1947). 
Marx.    Ann.  Oculist.  (Paris),  160,  873  (1923). 
Matsumoto.       Zool.    Mag.     (Japan),    60,     13 

(1951). 
Nakamura.    Acta  Soc.  ophthal.  jap.,  58,  1628 

(1954)  ;    59,  650  (1955). 
Nesbitt.    Ann.  ent.  Soc.  Amer.,  34,  51  (1941). 
Obal.      Klin.    Mbl.    Augenheilk.,    117,    201 

(1950). 
Palay.    J.  comp.  Neurol.,  79,  247  (1943)  ;   82, 

129  (1945). 
Pamiarale.     Boll.  Soc.  ital.  Biol,  sper.,  28,  15 

(1952). 
Panouse.     C.  R.  Acad.  Sci.  (Paris),  217,  553 

(1943)  ;    218,  293  (1944). 
Ann.  Inst.  Oceanogr.,  23,  65  (1946). 
Park  and  Keller.    Ecology,  13,  335  (1932). 
Parker,   Hendricks,    Borthwick   and   Jenner. 

Nature  (Lond.),  169,  242  (1952). 
Passano.     A7iat.  Rec,  111,  502,  559  (1951); 

112,  460  (1952). 
Perkins.    J.  exp.  Zool.,  50,  71  (1928). 
Perkins  and   Snook.     J.   exp.   Zool.,  61,    115 

(1932). 
Pflugfelder.     Z.  wiss.  Zool.,  149,  477  (1937). 
Posthumus.     Ojihthalmologica,  124,  17  (1952). 
Rahn  and  Rosendale.     Proc.  Soc  exj).  Biol. 

Med.,  48,  100  (1941). 
Rowlands.    J.  e.vp.  Biol,  31,  151  (1954). 
Rubino  and  Esente.     Riv.  oto-neuro-oftal.,  23, 

149  (1948)  ;   25,  351  (1950). 


HORMONAL  CONTROL 


563 


Rubino    and   Pereyra.      Rii\    oto-neuro-ojtal., 

23,  69,  221  (1948)  ;   25,  12  (1950). 
Rubino  and  Sapuppo.      Riv.  oto-neuro-offal., 

23,  170  (1948)  ;    25,  16  (1950). 
von    Sallinann   and    Lowenstein.       Amer.  J. 

Ophthal.,  39,  11  (1955). 
Salvati.  Ann.  Oculist.  (Paris),  160,  568  (1923). 
Sandeen  and  Brown.     Biol.   Bull.,  101,  228 
(1951). 
Physiol.  Zool.,  25,  222  (1952). 
Scharrer,    B.      Xaturwissenschuflen,    25,    131 
(1937). 
J.  com]}.  Xeurol..  74,  93  (1941). 
Biol.  Bull.,  81,  96  (1941)  ;   102,  261  (1952). 
Anat.  Rec,  112,  386  (1952). 
The    Action    of   Hormones    in    Plants    and 

Invertebrates,  N.Y.,  125  (1952). 
Pfliigers  Arch.  ges.  Physiol.,  255,  154  (1952). 
Ann.  Rev.  Physiol.,  15,  457  (1953). 
Scharrer,  B.,  and  Hadorn.    Proc.  nat.  Acad. 

Sci.,  24,  236  (1938). 
Scharrer,  B.,  and  Scharrer,  E.   Biol.  Bull.,  87, 

242  (1944). 
Scharrer,  E.     Z.  vergl.  Phi/siol.,  7,  1  (1928). 

Z.  u-iss.  Zool.,  144,  1  (1933). 
Scharrer,  E.,  and  Scharrer,  B.  Biol.  Rev.,  12, 
185  (1937). 
Physiol.  Rev.,  25,  171  (1945). 
Proc.   Laurentian  Hormone  Conference,  10, 
183  (1954). 
Scheer,   B.   T.,  and  Scheer,  M.   A.    Physiol. 

comp.  (Amst.),  2,  198  (1951). 
Schmerl.     Klin.   Mbl.  Aiigenheilk.,  126,   598 

(1955). 
Schmerl  and  Steinberg.     A>ner.  J.  Ophthal., 

31,  155,  1097  (1948). 
Siliato.    Ann.  OttoL,  81,  367  (1955). 
Smith,  R.  I.     Biol.  Bull..  95,  169  (1948). 
Smith,  S.  W.    Amer.  J.  Anat.,  89,  195  (1951). 
Starling.     Lancet,  2,  339  (1905). 


Stephens.     Physiol.  Zool.,  25,  70  (1952). 

Biol.  Bull.,  i08,  235  (1955). 
Thomsen.  E.     J.  exp.  Biol.,  26,  137  (1949)  ; 
29,  137  (1952). 
Pubbl.   Staz.    zool.   Napoli,    24,   Suppl.,   48 
(1954). 
Thomson,    A.  P.    D.     J.   Physiol.,    113,    425 
(1951). 
Proc.  roy.  Soc.  B,  142,  146  (1954). 
Thomson,  A.  P.  D.,  and  Zuckerman.  Nature 
(Lond.),  171,  970  (1953). 
Proc.  roy.  Soc.  B,  142,  437  (1954). 
Travis.    Anat.  Rec.  Ill,  503  (1951). 
Turner.    J.  comp.  Neurol.,  85,  53  (1946). 
Veillet,  Cornubert  and  Demeusy.     C.  R.  Soc. 

Biol.  (Paris),  147,  1264  (1953). 
Vogt.    Naturwissenschaften,  30,  470  (1942). 
Waterman    and    Enami.     Pubbl.    Staz.    zool. 

Napoli,  24,  Suppl.,  81  (1954). 
Weiss  and  Hiscoe.     J.   e.rp.   Zool.,   107,   315 

(1948). 
Welsh.     Biol.  Bull.  77,  119  (1939). 
J.  exp.  Zool.,  86,  35  (1941). 
Anat.  Rec,  111,  442  (1951). 
Weyer.     Zool.  Anz.,  112,  137  (1935). 
Wigglesworth.     Quart.  J.  micr.  Sci.,  77,   191 
(1934)  ;    79,  91  (1936). 
Nature  (Lond.),  144,  753  (1939). 
J.  e.vp.  Biol.,  17,  201  (1940). 
Witschi.     Wilson  Bull,  47,  177  (1935). 
Young.     Quart.  J.  micr.  Sci.,  78.  367  (1936). 
Zetler.     Arch.  exp.  Path.  Pharmak.,  218,  239 

(1953). 
Zondek  and   Koehler.      Dtsch.   med.    Wschr., 

58,  2025  (1932). 
Zondek  and  Wolfsohn.    Schweiz.  med.  Wschr., 
21,  162  (1940). 
Amer.  J.  Ophthal.,  30,  596  (1947). 
Zuckerman.     Lancet,  1,  739,  789  (1954). 


PART  III 
THE  FUNCTION  OF  THE  EYES  OF  ANIMALS 

The  Vision  of  Invertebrates 
The  Vision  of  Vertebrates 


Fig.  728.— Karl  von  Frisch  (1886 ). 


CHAPTER  XVII 
THE  VISION  OF  INVERTEBRATES 

I  am  introducing  this  chapter  on  the  function  of  the  ej^es  of  Invertebrates 

with  the  photograph  of  karl  von  frisch  (1886 )  (Fig.  728),  who  has  devoted 

his  long  and  fruitful  life  to  the  fascinating  study  of  animal  behaviour — and  still 
continues  to  do  so.  Born  in  Vienna,  he  studied  in  Munich  and  successively 
became  Professor  and  Director  of  the  Zoological  Institutes  at  the  Universities 
of  Rostok  (1921),  Breslau  (1923),  Munich  (1925),  Graz  (1946),  and  again  Munich 
(1950)  where,  as  this  book  is  being  written,  he  is  still  pursuing  his  close  and 
intimate  study  of  the  habits  of  insects.  Taken  as  a  whole,  his  life  as  a  biologist, 
spent  observing  the  behaviour  of  his  experimental  friends  in  the  water  and  in 
the  covmtryside,  must  have  been  a  delightful  one  ;  he  obviously  enjoyed  it  and 
no  one  can  read  his  published  works  without  realizing  that  fact  can  indeed  be 
more  exciting  and  of  more  interest  than  fiction.  The  greater  part  of  the  first  years 
of  his  stvidies  was  devoted  to  the  vision,  and  particularly  the  colour  vision,  of 
fishes,  a  subject  in  which,  as  we  shall  see  in  the  following  chapter,  he  became  a 
great  avithority,  opposing  the  views  of  Carl  von  Hess  (Fig.  735)  and  eventually 
winning  the  battle.  The  latter  part  of  his  life  has  been  largely  spent  observing  the 
habits  of  bees.  Much  of  the  fruits  of  this  we  have  already  studied  in  the  chapter 
on  the  influence  of  light  on  movement  .^  There  are  few  romances  in  science  more 
pleasant  than  the  convincing  and  far-reaching  results  he  has  obtained  in  the 
study  of  the  extraordinarily  complex  behaviour  of  these  insects  in  the  meadows 
of  Central  Europe  ;  and  there  are  few  pieces  of  biological  work  carried  through 
with  greater  perseverance,  with  greater  thoroughness  and  to  greater  purpose. 

METHODS    OF    INVESTIGATION 

The  scientific  estimation  of  tlie  visual  capacity  of  animals  is 
notoriously  difficult.  It  is  a  difficult  problem  even  in  man  for  sensations 
are  individualistic  and  subjective  and  the  language  of  introspection 
is  usually  unsafe  ;  in  the  lower  animals  the  difficulties  become  in- 
finitely greater  for  the  only  criterion  whereon  we  can  pass  judgment  is 
the  observation  of  their  reactions  to  various  stimuli  ;  we  have  no 
knowledge  of  how  far  their  exj^eriences  coincide  with  our  own,  and  no 
right  to  equate  the  two.- 

From  the  scientific  point  of  view  the  observation  of  animal 
behaviour  in  ordinary  uncontrolled  circumstances  can  provide  much 
useful  information  regarding  their  sensory  experiences,  but  from  such 
evidence  our  conclusions  can  only  be  drawn  with  reserve.  This 
approach  is  full  of  j^itfalls  even  in  human  subjects.  A  red-green 
colour-blind  person  will  say  that  he  can  appreciate  red  and  green  and 
usually  behaves  as  if  he  does  so  ;    and  we  have  little  idea  of  what 

p.  70.  2  p.  108. 


568  THE   EYE   IN   EVOLUTION 

indeed  he  does  see.  For  this  reason  Konig  gave  up  the  method  of 
introspection  entirely  and  trusted  only  to  colour-matches  in  his 
investigation  of  colour-blindness  ;  only  if  every  colour  in  the  spectrum 
could  be  matched  by  a  mixture  of  a  given  pair  of  colours  should  the 
subject  be  considered  a  dichromatic  colour-blind.  There  are  occasions, 
however,  when  the  observation  of  the  behaviour  of  animals  in  their 
natural  surroundings  can  yield  satisfying  results.  We  have  already 
noted  many  instances  of  such  cecological  research,  for  example,  in  the 
study  of  the  conduct  of  different  Arthropods  in  their  orientation  towards 
light  ;  a  particularly  good  example  is  von  Frisch's  experiments  on 
bees,  or  the  means  of  orientation  employed  by  birds  in  navigation. 
These  methods,  however,  valuable  as  they  are,  are  applicable  only  to 
certain  restricted  types  of  complex  behaviour  of  a  nature  such  that 
other  incidental  variables  can  be  neglected. 

Two  more  generally  applicable  methods  of  research  are  available. 
In  the  objective  methods  of  approach  a  measurable  physical  phenomenon 
presumably  determined  by  a  specific  stimulus  is  observed — a  contrac- 
tion of  the  pupil  to  light,  for  instance,  or  an  electroretinographic 
response — and  it  is  assumed  that  this  reaction  bears  a  relatively 
constant  relation  to  events  on  the  sensory  level.  If  a  response  of  this 
nature  follows  stimulation  by  one  band  of  wave-lengths  of  light  and 
not  by  another,  for  example,  it  is  probable  that  the  first  gives  rise  to  a 
sensation  and  the  second  does  not.  A  further  analysis  is  possible  by  the 
study  of  reflex  responses.  If  an  animal  exhibits  characteristic  reflex 
reactions  to  varying  stimuli  it  is  reasonable  to  suppose  that  these 
affect  it  in  different  and  specific  ways.  The  optomotor  reaction 
illustrates  this.  If  an  animal,  be  it  insect  or  vertebrate,  is  faced  with 
a  revolving  striped  drum  and  reacts  to  the  succession  of  stimuli  thus 
presented  to  it  by  compensatory  movements  of  its  eyes  or  its  body,  we 
can  assume  that  the  alternating  stimuli  have  a  different  effectivity  ;  or 
if  an  animal  salivates  when  presented  with  one  stimulus  associated 
by  training  with  food  and  not  with  another,  the  deduction  seems 
inescapable  that  a  discrimination  is  made  between  the  two  stimuli  ; 
but  whether  the  differentiation  remains  on  the  reflex  level  or  is 
appreciated  as  a  sensation  is  sometimes  problematical. 

The  elicitation  of  such  reflex  responses,  however,  although 
suggestive,  gives  us  little  idea  of  the  conscious  appreciation  of  sensations 
and  their  effectiveness  in  determining  conduct.  A  more  satisfying 
approach  is  the  subjective  rnethod  of  the  study  of  what  appears  to  be 
conscious  behaviour.  The  simplest  technique  in  this  respect  is  a  study 
of  "  preference  "  :  if  an  animal  goes  towards  light  and  avoids  darkness, 
or  vice  versa,  it  evidently  can  distinguish  between  them  ;  a  similar 
argument  applies  to  a  fish  which  swims  towards  a  red  rather  than  a 
green  li^ht.     How  far  this  conduct  implies  that  the  discrimination  is 


THE   VISION   OF   INVERTEBRATES 

based  on  different  sensory  experiences  is,  however,  doubtful.  It  has 
been  generally  accepted  in  the  case  of  the  worm  which  emerges  in 
twihght  and  hides  again  in  daylight  ;  but  does  it  equally  apply  to  the 
protozoan  which  shows  the  same  response  ?  We  do  not  know  the 
answer  to  this  riddle.^ 

A  more  analytical  method  is  the  application  of  training  techniques 
which,  incidentally,  are  more  susceptible  to  scientific  control.  Thereby 
an  animal  is  trained  to  respond  to  or  reject  one  stimulus  to  the  exclusion 
of  all  others  by  an  appropriate  reward  or  punishment,  the  stimulus 


569 


Ur12in.-J 

Fig.  729. — Ground  Plan  for  Discrimination  Box. 

L,  light  box.  F,  food  ;  Z)i,  hinged  door  ;  D^,  hinged  door  with  3  X  3  in. 
opal  glass  panel  ;  G,  glass  partition  ;  R,  restraining  chamber.  The  box  is 
13  in.  high  (R.  Gunter,  J.  Physiol,  1951). 


being  more  minutely  differentiated  from  related  stimuli  as  the  process 
of  training  proceeds.  The  disadvantage  of  the  method  is  the  limitations 
of  its  applicability  since  it  requires  more  intelligence,  consistency  in 
behaviour  and  amenability  than  most  animals  possess  ;  moreover,  an 
experiment  of  this  type  must  excite  the  animal's  interest  so  that  the 
technique  would  be  expected  to  break  down  if  the  sensation  in  question 
were  not  of  importance  in  its  life. 

A  simple  and  typical  experimental  set-up  for  such  a  training  experiment  is 
seen  in  Fig.  729.  In  its  essentials  it  is  a  Y-shaped  "  discrimination  box  "  or 
maze  wherein  the  animal  is  first  retained  in  an  outer  chamber  and  then,  entering 

1  p.  102. 


570  THE   EYE   IN   EVOLUTION 

the  main  chamber,  is  offered  the  choice  of  two  stimuli  ;  these,  for  example,  may 
be  light  stimuli  made  up  of  two  illuminated  milk -glass  panels  set  into  hinged 
doors  and  lit  from  behind  so  that  they  can  be  suitably  varied  in  intensity,  hue 
or  saturation.  Either  of  these  the  animal  can  open  to  receive  a  reward  (food) 
or  punishment  (an  electric  shock).  Trained  initially  to  go  towards  one  (the 
positive)  of  two  well -differentiated  alternative  stimuli  and  to  avoid  the  other, 
the  negative  stimulus  is  approximated  progressively  to  the  first  until  the  limit 
of  discrimination  is  reached.  Thi'oughout  the  exjaeriment  the  relative  positions 
(right  or  left)  of  the  two  stimuli  are  randomly  alternated,  while  other  stimuli 
(olfactory,  etc.)  are  eliminated  as  by  j^lacing  similar  food  in  each  box,  that  in 
the  negative  box  being  inaccessible.  Such  training  techniques,  of  course,  are 
laborious,  several  hundred  "  runs  "  being  usually  required  in  each  experiment  ; 
moreover,  they  are  time-consuming  for  much  cannot  be  accomplished  at  one 
session  lest  fatigue  be  induced  or  interest  lost  ;  and  they  are  restricted  to  species 
which  are  relatively  intelligent  and  docile,  for  a  stupid  or  an  untrainable  animal 
or  one  that  gets  cross  or  sulks  is  useless. 

It  is  also  to  be  remembered  that  any  response  of  this  nature  made 
by  an  animal  depends  upon  complex  factors  ;  few  stimuli  are  in  fact 
simple,  most  involve  more  than  one  receptor,  and  all  responses  are 
complicated  by  mutual  excitations  and  inhibitions,  for  the  animal 
reacts  not  to  one  stimulus  alone  (such  as  food)  but  to  a  complex 
situation  wherein  each  stimulus  must  be  differentiated  against  a 
changing  background  and  varies  with  past  experience  and  its  present 
psychological  state.  Even  in  the  most  adequately  controlled  experi- 
ments in  the  laboratory  an  ideal  environment  can  rarely  be  realized. 
The  very  fact  of  the  artificial  isolation  of  the  stimulus  is  outside  the 
animal's  natural  experience  and  thereby  something  important  in  the 
experiment  is  lost.  It  follows  that  the  results  of  such  analyses  can  be 
accepted  only  with  reservation  ;  indeed,  any  claim  that  a  scientifically 
exact  appreciation  of  the  physiology  or  psychology  of  any  animal  can 
be  based  on  conditioning  experiments  is  illusory. 

Within  these  limits,  the  method  undoubtedly  produces  results  in 
terms  of  sensational  responses  of  greater  reliability  than  any  other 
and  forms  the  best  means  of  analysing  the  nature  of  the  sensation 
concerned.  Considering  these  difficulties,  however,  as  well  as  the  varia- 
tion in  psychology  between  different  members  of  the  same  species  and 
the  probable  differences  in  apperception  and  interpretation  between  any 
species  and  our  own,  it  is  not  surprising  that  the  results  thus  obtained 
have  often  been  inconsistent. 


THE    LOWER   LNVERTEBBATES 

PROTOZOA.  We  have  already  seen  that  Protozoa  exhibit  fixed 
reactions  to  a  variety  of  "  sensory  "  stimuli — light,  heat,  gravity, 
contact,  electrical  shock — the  only  observable  response  being  a  tropism. 
We  ha^     also  seen  that  there  is  no  observable  difference  in  behaviour 


THE   LOWER   INVERTEBRATES 


571 


in  respect  to  these  different  modalities  but  that,  on  the  other  hand, 
they  may  be  additive  in  their  effect.  Whether  the  reaction  is  positive 
or  negative  there  is  no  evidence  that  the  response  is  associated  with 
subjective  awareness  ;  and  although  a  temporary  process  of  condition- 
ing may  exist  due  to  the  cumulative  effects  of  previous  stimuli/  there 
is  little  evidence  of  any  true  capacity  for  learning.  Soest  (1937),  for 
example,  claimed  that  an  association  with  electric  shocks  could 
condition  an  avoidance  of  light  in  Paramoecium,  but  this  behaviour 
may  well  have  been  determined  by  the  accumulation  of  metabolites 
(Dembowski,  1950).  It  would  therefore  seem  that  apart  from  responses 
which  are  explicable  on  a  purely  physico-chemical  basis,  we  have  no 
knowledge  of  "  vision  "  in  the  sense  of  perceptual  awareness  in  this 
phylum  (see  Wichterman,  1953). 

CCELENTERATA.  Among  Coelenterates  there  is  more  evidence  for 
assuming  the  existence  of  a  lowly  organization  of  some  aspects  of 
conduct  on  a  reflex  level  as  well  as  the  presence  of  associated 
memory.  The  spontaneous  movements  exhibited  by  several  species 
either  of  swimming  or  "  stepping  "  whether  the  environment  is  changed 
or  remains  constant,  are  obviously  the  result  of  controlled  activation 
and  inhibition  -  ;  the  same  tyj^Q  of  conduct  is  seen  in  the  daily  rhythms 
in  the  activity  of  sea-anemones  and  jelly-fish,  such  as  those  determined 
by  tidal  changes,  which  may  persist  for  some  considerable  time  after 
the  stimulus  has  been  artificially  removed.^  That  purposive  reactions 
with  memory  associations  also  exist  is  suggested  by  such  types  of 
behaviour  as  the  assumption  by  the  anemone,  Actinia,  of  the  same 
position  in  an  artificial  aquarium  as  it  occupied  in  its  natural  rock 
(van  der  Ghinst,  1906  ;  Bohn,  1908),  the  apparent  intelligence  of  the 
anemone,  AntJioloba,  in  climbing  on  the  back  of  a  crab  (Brunelli,  1910), 
or  the  rejection  of  unsuitable  food  after  several  trials  by  such  anemones 
as  Actinia.  Tealia  and  Cribrina  (Fleure  and  Walton,  1907  ;  Gee,  1913  ; 
and  others).  In  spite  of  these  activities,  however,  so  far  as  we  know, 
the  phototactic  reactions  of  this  group  are  completely  automatic  and 
fixed,  and  indeed  have  been  found  to  remain  unchanged  after  two 
generations  have  been  exposed  to  abnormal  lighting  conditions  (Ewer, 
1947). 

ECHixoDERMATA.  In  this  pliylum,  again,  although  some  training 
ability  in  the  starfish,  Asterias,  is  suggested  by  the  observations  of 
Jennings  (1907)  on  its  capacity  to  right  itself,  or  of  Ven  (1921)  on  its 
ability  to  escape  from  a  confined  position,  there  is  no  proof  of  any 
visual  reaction  except  a  rigid  and  unvaried  phototactic  resjDonse 
without  detectable  evidence  of  subjective  appreciation. 


Paramcecium 


Sea-anemone 


Jcllvfish 


Starfish 


1  p.  36. 

^  Hang  (1933)  in  Hydra  ;  Batham  and  Pant  in  (19.50)  in  the  sea-anemone,  Metridium. 

^  Pieron(1909)  in  sea-anemones  ;  Horstniann  (1934)  in  the  jellyfish,  Aurelia. 


572 


THE   EYE   IN   EVOLUTION 


Planarian 


Leptoplana 


Lumbricus 


THE    VISION    OF    WORMS 

As  would  be  expected  from  the  extreme  primitiveness  of  their 
ocular  structures,  the  vision  of  worms  is  limited  to  an  appreciation  of 
the  presence  or  intensity  of  light  associated  with  a  light-shadow  reflex 
usually  of  a  photo -negative  type  ;  as  we  have  seen,  in  some  species  a 
directional  localization  may  be  possible.  In  the  unsegmented 
WORMS  the  simple  photo -negative  reaction  is  the  only  response. 
Planarians,  for  example,  are  always  found  in  dark  places  beneath 
stones  or  the  leaves  of  water  plants,  vigorously  retreating  from  light 
whenever  they  are  exposed  to  it  (Taliaferro,  1920).  Some  such  response 
to  light  still  remains  when  the  eyes  have  been  removed,  the  animal 
depending  on  hght-sensitive  cells  scattered  over  the  surface  of  the  body. 
There  is  evidence,  however,  for  the  first  time  in  the  animal  kingdom, 
that  the  rigid  phototactic  response  can  be  modified  in  a  very  crude 
manner  by  training.  The  Polyclad,  Lejptoplana,  for  example,  is 
quiescent  in  the  dark  and  moves  when  illuminated,  but  contact  of  the 
head -end  with  a  solid  object  stops  the  forward  movement.  Hovey 
(1929)  found  that  by  simultaneously  illuminating  the  worm  and 
touching  it  so  as  to  prevent  it  from  creeping  forward,  the  photo- 
kinetic  reaction  was  completely  inhibited  ;  a  similar  conditioning 
process  to  electric  shocks  was  demonstrated  in  Planaria  gonocephala 
by  Dilk  (1937).  After  removal  of  the  cerebral  ganglion  these  modifica- 
tions of  the  simple  phototactic  response  cannot  be  elicited,  so  that  this 
structure  is  necessary  for  the  development  of  this  elementary  learning 
process.  In  assessing  the  importance  of  these  reactions  to  light  in  the 
life  of  the  animal,  however,  it  must  be  remembered  that  the  general 
behaviour  of  unsegmented  worms  is  determined  not  so  much  by  their 
light-sense  as  by  the  more  fully  developed  chemical  sense  and  the 
sense  of  touch  which  responds  with  great  sensitiveness  to  the  slightest 
movement  of  the  water  in  which  they  live  or  to  objects  with  which 
they  come  in  contact. 

More  work  has  been  done  on  the  light -sense  of  segmented  worms, 
jjarticularly  upon  the  earthworm,  Lu7nbricus }  It  will  be  remembered  ^ 
that  in  this  animal  the  light-sensitive  cells  are  concentrated  mainly 
at  the  two  extremities.  In  very  dim  illumination  (less  than  0-00118 
m.c,  W.  N.  Hess,  1924)  the  animal  is  j)hoto-positive,  and  in  ordinary 
daylight  illumination,  photo-negative — it  must  avoid  light  since,  in 
fact,  exposure  to  strong  sunlight  for  one  hour  may  cause  paralysis, 
for  several  hours,  death.  It  follows  that  on  emerging  from  its  burrow 
at  any  time  except  at  night  or  in  the  dim  twilight  of  morning  or 


i  Hoffmeister  (1845),  R.  Hesse  (1896^  W.  N.  Hess  (1924),  v.  Buddenbrock  (1930), 
Sefe-dl  (1933),  Unteutsch  (1937-38). 
.  190. 


THE   VISION   OF   WORMS  573 

evening,  either  end  will  at  once  retract  into  the  safety  of  its  retreat. 
Its  more  complex  reactions  to  light  when  travelling  on  the  ground 
have  already  been  [described.^  A  similarly  high  degree  of  sensitivity  is 
seen  among  certain  polychaete  worms,  particularly  the  tubiculous 
types.  In  these  the  light-and-shadow  reflex  is  very  marked  ;  so 
sensitive  are  they  to  light  that  Andrews  (1891)  found  that  if  a  hand 
were  moved  in  the  air  at  a  distance  of  a  metre  from  the  water  containing 
the  animals,  they  withdrew  themselves  into  their  tubes  as  soon  as  the 
shadow  fell  upon  them. 

In  segmented  worms,  however,  the  potentialities  of  habituation 
and  learning  have  evolved  to  a  considerably  greater  extent  ;  that 
earthworms,  indeed,  have  a  modicum  of  intelligence  was  known  to 
Darwin  (1881)  who  noted  the  deft  way  in  which  by  trial-and-error, 
profiting  by  previous  experience,  they  transported  leaves  of  various 
types  to  their  burrow  or  collected  little  stones  to  guard  its  entrance.^ 
Again,  Hydroides,  if  collected  from  shallow  water,  reacts  promptly  to 
shadows  in  the  aquarium,  but  individuals  collected  from  deep  water 
remain  inactive  presumably  from  lack  of  experience  in  a  shadowless 
environment  ;  a  like  passivity  is  rapidly  assumed  by  reactive  specimens 
from  shallow  water  if  they  are  isolated  from  shadows  for  some  time  in 
the  laboratory  (A.  W.  Yerkes,  1906  ;  Hargitt,  1906-9).  Similar 
habituations  to  light-and-shadow  stimuli  have  been  found  also  in 
polychaete  worms  (Bohn,  1902)  and  leeches  (Gee,  1913).  Moreover,  in 
these  species  the  normal  response  can  be  varied  by  conditioning.  Thus 
the  polychaete.  Nereis,  if  presented  with  food  together  with  a  sudden 
increase  or  decrease  in  illumination,  can  be  trained  after  only  six  trials 
to  respond  to  the  change  in  illumination  alone  whether  it  is  positive 
or  negative  (Copeland,  1930),  while  by  a  similar  association  with  tasty 
food  or  other  stimuli  a  reversal  of  the  usual  reaction  to  light  can  be 
induced  in  a  number  of  worms  such  as  Hydroides  (A.  W.  Yerkes,  1906), 
Nereis    (Copeland    and    Brown,     1934),    Lumbricuhis    (Raabe,    1939)  Nereis 

and  Lumbricus  (Wherry  and  Sanders,  1941).  Finally,  several 
Oligochaetes  and  Polychaetes  have  shown  a  considerable  ability  to 
learn  the  correct  turning  in  a  simple  T-  or  Y-maze  ;  propelled  forwards 
by  illumination  of  the  hind  region,  rewarded  by  a  warm  dark  cell  or 
punished  by  an  electric  shock  or  an  unpalatable  salt  solution,  they  can 
after  many  trials  (up  to  200)  be  taught  to  turn  in  the  required  direction, 
a  capacity  unimpaired  by  excision  of  the  supra-oesophageal  ganglion.^ 

In  worms,  therefore,  in  which  a  ganglionated  nervous  system  first 
appears,  for  the  first  time  in  evolution  the  response  to  light  has  been  shown 

1  p.  53. 

2  See  also  Malek,  1927. 

3  In  Oligochsetes  :  AUolobophora  (R.  M.  Yerkes,  1912),  Eisenia  and  Lumbricus 
(Heck,  1920),  Heliodrilus  (Swartz,  1929)  ;  in  the  polychgete,  Nereis  (Copeland,  1930  ; 
Fischel,  1933  ;   Copeland  and  Brown,  1934). 


574 


THE   EYE   IN   EVOLUTION 


to  become  something  that  is  not  rigid  and  entirely  automatic  ;  it  can  be 
modified  by  experience  and  training,  while  vision,  although  still  a 
secondary  sense,  apparently  becomes  endowed  with  some  degree  of 
awareness  and  meaning. 


Snail 


Slug 


Avicula 


Anodonta 


Mya 


THE    VISION    OF   MOLLUSCS 

From  the  functional  point  of  view  in  most  Molluscs  vision  is 
secondary  to  the  olfactory  or  tactile  sense  ;  this  would  be  expected  in 
view  of  the  primitive  structure  of  the  eyes  of  most  types  for,  with  the 
exception  of  Cephalopods,  they  are  rarely  capable  of  detailed  visual 
resolution.  It  has  been  contended  that  land  Molluscs  (snails,  slugs,  etc.) 
which  seldom  emerge  except  in  twilight  and  retract  their  eyes  within 
their  tentacles  on  exposure  to  bright  light,  are  blind  (Yung,  1913)  (Fig. 
188).  A  directional  appreciation  of  light  is  possible,  however,  and  quick 
movements  can  be  readily  detected  (Fob,  1932  ;  Grindley,  1937)  ;  but 
there  is  no  evidence  of  the  appreciation  of  colour  (Mundhenke,  1955). 
These  animals,  however,  are  highly  myopic  and  experiment  has  shown 
that  objects  can  rarely  be  appreciated  more  than  a  few  centimetres 
away,  although  farther  in  subdued  than  in  bright  light  (Willem,  1892). 
Vision  does  not  thus  appear  to  dominate  behaviour.  On  the  other 
hand,  Gastropods  are  extremely  sensitive  to  the  slightest  movement 
of  the  air  or  any  jarring  of  the  surface  on  which  they  crawl,  while  their 
sense  of  smell  is  so  acute  as  to  dominate  most  of  their  behaviour  :  food, 
for  example,  is  sought  almost  by  scent  alone. 

In  littoral  lamellibranch  Molluscs  it  would  seem  probable  that 
vision  is  generally  limited  to  the  appreciation  of  light  and  shadow,  but 
this  appreciation  may  be  unusually  acute.  Whether  the  ocelli  are 
situated  on  the  siphon  or  the  mantle-edge  the  slightest  shadow  often 
induces  a  response.  Thus  Patten  (1886)  found  that  in  the  Noah's-ark 
shell.  Area,  the  mantle  contracted  and  the  valves  closed  quickly  if  the 
faint  shadow  of  a  hand  or  a  pencil  fell  upon  them.  It  is  interesting 
that  sensitivity-  does  not  always  vary  with  the  elaboration  of  the 
structure  of  the  eye,  for  the  same  observer  found  that  an  even  more 
sensitive  response  was  given  by  Avicula  which  is  provided  with  only  a 
few  ill-developed  ocelli;  even  the  eyeless  mussel,  Anodonta,  reacts  to 
a  passing  shadow  owing  to  its  dermal  sensitivity  to  light  (Braun  and 
Faust,  1954).!  The  rapidity  with  which  oysters  close  their  shells 
on  the  passing  of  the  shadow  of  a  man  or  a  boat  is  well  known. 
A  similar  sensitivity  to  passing  shadows  characterizes  the  ocelli  in  the 
siphons  of  littoral  Lamellibranchs  (Hecht,  1919  ;  Koller  and 
V.  Studnitz,  1934,  in  Mya)  ;  and  it  is  obvious  that  such  types  which  live 
between  the  tide-marks  and  protrude  their  siphons  and  occasionally 

1  p.  114. 


THE   VISION   OF  MOLLUSCS 


575 


portions  of  their  shells  outside  their  burrow,  will  depend  much  for 
their  survival  on  their  ability  to  withdraw  into  safety  before  the 
arrival  of  their  many  enemies.  Pecten,  with  its  elaborate  eyes,  is  an 
exception,  perhaps  because  this  animal  may  use  sight  to  direct  its 
unusual  activity  as  it  "  flies  "  on  the  water  for  considerable  distances 
by  flapping  its  valves  and  expellmg  water  from  the  apertures  near  the 
fringe.  Even  if  this  is  not  so,  the  experiments  of  Wenrich  (1916),  who 
determined  the  smallest  white  card  which  produced  a  shell-closing 
response  in  this  scalloj),  showed  that  the  animal  was  extremely  sensitive 
to  minimum  changes  in  brightness.  On  the  other  hand,  in  abyssal  or 
underground  Molluscs,  visual  organs  tend  to  be  less  elaborate,  and 
vision  takes  a  secondary  or  negligible  place  in  the  creature's  activities. 

Snails  have  been  trained  to  negotiate  a  T-  or  Y-maze  (Garth  and  Mitchell, 
1926  ;  Fischel,  1931  ;  Brandt,  1935),  while  a  number  of  Molluscs  demonstrate  a 
remarkable  ability  to  seek  their  habitual  homes  from  a  dLstance.^  The  mechanism 
employed  is  unkno^\^l  ;  an  association  of  several  senses  is  possibly  involved  among 
which  touch  probably  figures  largely  and  vision  little  if  at  all. 

CEPHALOPODS  are  visually  in  a  very  different  class.  There  can  be 
little  doubt  that  they  use  their  eyes  for  the  actual  observation  of 
objects  and  in  this  respect,  depending  on  vision  rather  than  smell,  they 
are  unique  among  Molluscs.  Functionally  their  eyes  are  capable  of  a 
considerable  degree  of  pattern- vision,  they  have  a  good  perception  of 
movement,  and  have  adaptive  and  accommodative  powers.  They  are 
the  only  Invertebrates  which  exhibit  pupillary  reactions  remotely 
resembling  those  characteristic  of  Vertebrates  (Magnus,  1902)  ;  these 
reactions  are  most  readily  excited  by  yellow-green  light  of  the  same 
spectral  range  which  induces  the  most  active  phototactic  responses. 
Although  many  Cephalopods  change  their  integumentary  colour  to 
harmonize  with  their  background  by  reflexes  originating  in  the  eyes,^ 
Carl  von  Hess  (1921-22)  found  no  evidence  to  suggest  that  colour 
vision  is  present  ;  and  the  positive  claims  made  by  Goldsmith  (1917), 
Bierens  de  Haan  (1926),  Tinbergen  (1939)  and  Kiihn  (1930-50)  that, 
as  judged  by  behavioural  experiments,  they  can  differentiate  hues  are 
open  to  serious  criticism  (Carter,  1948). 

The  visual  capacity  of  Octoinis  has  received  a  considerable  amount 
of  attention  by  such  writers  as  von  Uexkiill  (1905),  Polimanti  (1910), 
Goldsmith  (1917),  ten  Gate  and  ten  Cate-Kazejewa  (1938),  and 
particularly  by  Boycott  and  Young  (1950-56)  and  Young  (1956).  The 
standard  lay-out  of  their  experiments  was  to  allow  an  octopus  to  attack 
and  eat  a  crab  associated  with  a  particular  geometrical  figure,  but  to 

*  Chiton,  Pelseneer,  1935  ;  the  limpets,  Patella  and  others,  Davis,  1885-95  ;  Lloyd 
Morgan,  1894  ;  H.  Fischer,  1898  ;  Pieron,  1909  ;  Thorpe,  1956  ;  the  littoral  Pulmonate, 
Onchidium,  Arey  and  Crozier,  1918. 

8  p.  93. 


Pecten 


Octopus 


576  THE  EYE   IN   EVOLUTION 

punish  it  with  an  electric  shock  if  it  attempted  to  attack  a  crab  asso- 
ciated with  another  figure.  In  such  experiments  the  octopus  is  emi- 
nently trainable.  The  form  vision  of  the  animal  is  surprisingly  good. 
It  can  distinguish  a  square  of  4  cm.  from  a  square  of  2  or  8  cm.,  between 
a  square  and  a  rectangle  of  equal  area,  and  between  figures  of  various 
orientation  such  as  three  sides  of  a  square,  an  L,  a  vertical  or  horizontal 
line,  a  cross,  and  so  on  ;  curiously  it  was  found  that  difficulties  were 
experienced  in  differentiating  oblique  lines  or  a  circle  from  a  square. 
Further,  a  square  of  4  cm.  was  not  confused  with  a  square  of  8  cm.  at 
twice  the  distance,  a  differentiation  which  indicates  some  spatial 
perception. 

The  facility  of  Octopus  in  learning  to  differentiate  between  horizontal  and 
vertical  lines  and  its  relative  difficulty  in  differentiating  oblique  lines  or  such 
figures  as  a  diamond  and  a  triangle,  suggested  to  Sutherland  (1957)  and  Dodwell 
(1957)  that  the  vertical  and  horizontal  axes  have  a  special  status  in  the  dis- 
crimination of  shape.  On  this  basis  Sutherland  advanced  a  theory  that  the 
output  from  the  visual  cells  of  the  octopus  was  so  pi'ojected  in  the  optic  lobes 
as  to  correspond  with  a  vertical  and  horizontal  system  of  coordinates  ;  they 
would  thus  correspond  with  the  fundamental  coordinates  of  orientation  in  space — 
the  vertical  depending  on  gravity  and  the  horizontal  aligned  to  the  visual 
horizon,^  This  hypothesis  would  account  for  some  similar  experimental  results 
obtained  by  Fields  (1932)  and  Lashley  (1938)  on  the  sense  of  discrimination  in 
rats  ;  and  it  is  also  interesting  that  in  man,  reference  to  vertical  and  horizon- 
tal components  seems  to  be  of  primary  importance,  in  association,  of  course, 
with  other  systems  of  coordinates,  in  referring  a  point  in  the  environment  to 
the  centre  of  the  visual  field. 

Somewhat  similar  visual  reactions  can  be  elicited  in  the  cuttle- 
fish. Sepia  (Sanders  and  Young,  1940)  ;  and  the  perception  of  move- 
ment by  this  mollusc  is  good  with  an  optimum  angular  velocity  of 
about  7°  per  sec.  (Boulet,  1954).  Indeed,  it  would  seem  that  Sepia  is 
in  some  ways  more  amenable  to  training  than  Octopus  ;  if  a  prawn  is 
presented  as  prey  and  placed  behind  a  transparent  glass  partition,  the 
former  will  desist  attacking  after  several  attempts  while  Octopus  will 
persistently  swim  straight  into  the  screen  ;  moreover,  the  cuttlefish 
will  pursue  a  prawn  visually  round  a  corner,  while  Octopus  will  give  up 
the  hunt  unless  the  invisible  prey  is  reached  and  can  be  touched  by 
its  exploring  tentacles  (Sanders  and  Young,  1940  ;  Boycott,  1954) 
(Fig.  730).  It  would  seem,  therefore,  that  the  two  species  vary  con- 
siderably in  their  dependence  on  vision  for  hunting.  It  would  appear, 
also,  that  the  former  possesses  considerable  intelligence  in  that  it  can 
pursue  its  purposes  by  indirect  means  and  shows  some  capacity  for 
learning. 

There  seems  little  doubt,  however,  that  these  capacities  have  been 
exaggerated.     Pliny — that  prolific  purveyor  of  intriguing  inaccuracies — in  his 

1  p.  669. 


Sepia 


THE   VISION   OF  MOLLUSCS 


577 


Natural  History  described  how  Octopus  would  insert  a  stone  between  the  open 
shells  of  a  bivalve  so  that  the  soft  mollusc  could  be  devoured  at  leisure,  an  observa- 
tion repeated  by  Jeannette  Power  (1857)  to  demonstrate  the  importance  of 
vision  in  the  behaviour  of  this  creature.  In  her  ac^uarium,  she  wrote,  an  octopus 
holding  a  fragment  of  rock  in  one  of  its  arms,  intently  watched  the  lamellibranch, 
Pinna,  until  it  opened  its  valves.  As  soon  as  these  were  fully  opened,  she 
reported  that  with  incredible  address  and  promptitude  the  octopus  slipped  the 
stone  between  the  valves  so  that  they  could  not  close  again,  and  thereupon  set 
about  devouring  its  victim.^  Pieron  (1909)  claimed  that  Octopods  were  able  to 
uncork  a  bottle  \i\  order  to  obtain  crabs  seen  through  its  glass  walls  ;  and  other 
somewhat  similar  statements  appear  in  the  semi -scientific  literature.  In  view, 
however,  of  the  apparent  inability  of  the  octopus  to  use  a  "  tool,"  it  may  well 


Fig.   730. — The  Hunting  Capacity  of  Sepia. 

Within  a  tank  the  cuttle-fish  is  situated  at  X.  In  the  tank  is  a  circular 
opacjue  bucket  and  an  opaque  eiiamel  plate.  A  prawn  to  which  is  attached  a 
long  thread  is  placed  at  A  within  sight  of  the  octopod.  As  soon  as  its  attention 
had  been  drawn  to  it  and  it  liad  begun  to  follow  the  jjrawn,  it  was  pulled  by 
tlie  thread  to  position  B  behind  the  opaque  bucket.  The  octoj^od  followed, 
whereupon  the  prawn  was  pulled  behind  the  opaque  jilate  to  C,  again  out  of 
sight  of  its  pursuer.  The  latter  would  follow  around  B  and  thereupon  it  was 
allowed  to  devour  its  prey  (Sanders  and  Young). 

be  that  such  stories  are  fairy  tales  or  that  the  incidents  were  determined  rather 
by  chance  than  by  jaurposive  behaviour  (Boycott,  1954). 


THE    VISION    OF    ARTHROPODS 

ARTHROPODS  are  a  phylum  so  large  and  amori^hoiis  that  a  study 
of  the  visual  perceptions  of  the  various  types  must  be  taken  separately  ; 
this  diversity  in  function  follows  from  an  equally  marked  diversity  in 
habit  and  is  to  be  expected  within  a  group  which  contains  members 
smaller  than  some  Protozoa  with  great  simplicity  in  organization, 
and  others  (particularly  Insects)  which  are  rivalled  in  their  visual 
capacity  and  learning  ability  only  by  the  higher  Mammals.  Apart 
from    Insects,    however,    relatively    little    is    known    of    the    visual 

1  A  somewhat  similar  story  was  recorded  by  Leonardo  da  Vinci  (Manuscript  H  14) 
who  described  how  crabs  inserted  a  stone  or  twig  into  the  open  shell  of  an  oyster. 

S.O. — VOL.  I.  37 


678 


THE   EYE   IN   EVOLUTION 


Onychophore, 
Peripatus 


Centi-         Milli- 
pede pede 
(Myriapods) 


Daphnia 


Lobster 


der 


performance  of  Arthropods.  Among  the  lower  types  the  tactile  sense 
takes  pride  of  place  in  biological  utility  ;  in  Insects  vision  is  dominant 
with  the  sense  of  smell  (centred  in  the  antennae)  a  good  second. 

The  ONYCHOPHORA  are  provided  with  eyes  which  merely  differen- 
tiate the  presence  or  absence  of  light  from  which  the  creature 
persistently  flees.  A  crude  image-formation  is  possible  among  the 
MYRIAPODS  ;  although  Lithohius  is  trainable  to  the  extent  that  it  can 
master  the  single  turn  of  a  simple  T-maze,  it  does  so  by  its  tactile 
sense  on  the  basis  of  the  texture  of  the  walls  (Scharmer,  1935).  The 
visual  sense  of  the  smaller  crustaceans  is  almost  certainly  similarly 
crude,  but  light  perception  at  any  rate,  with  phototactic  responses 
while  swimming  is  well  developed.  In  the  Cladocera,  particularly  the 
water-flea,  Daphnia,  it  has  been  established  by  a  large  number  of 
observers  that  the  phototactic  response  varies  with  the  wave-length  of 
light  so  that  a  differential  sensitivity  would  appear  to  exist,  particu- 
larly affecting  red  and  bhie.^  Moreover,  an  elementary  degree  of 
training  is  possible  even  in  these  minute  creatures  since  the  positive 
taxis  of  Daphnia  to  a  source  of  light  through  a  narrow  tube  can  be 
rendered  less  clumsy  with  experience  (Blees,  1918)  ;  but  any  such 
feat  as  the  negotiation  of  the  single  turn  of  a  T-maze  seems  to  be  beyond 
the  capacity  of  the  small  Crustaceans  {Daphnia  and  Simocephalus, 
Agar,  1927).  These  creatures  thus  seem  to  be  inferior  to  earthworms 
in  this  respect. 2  Some  directional  sense  to  light  stimuli  is  probable, 
and  Exner  (1891)  suggested  that  the  Copepod,  Copilia,  made  the  most 
effective  use  of  its  simple  ocular  apparatus,  by  scanning  movements  of 
the  stalk-like  eye  controlled  by  its  system  of  muscles  (Fig.  139). 

Not  much  more  is  known  about  the  visual  functions  of  the  higher 
Crustaceans,  although  the  anatomical  elaboration  of  their  compound 
eyes  with  their  complex  nervous  connections  would  indicate  visual 
potentialities  of  considerable  proficiency.  In  the  lobster,  for  example, 
optomotor  reactions  are  readily  elicited  when  the  animal  is  confronted 
with  a  black-and-white  striped  rotating  drum  ^  ;  moreover,  reactions 
differ  depending  on  the  colour  of  the  stripe,  suggesting  the  presence  of  a 
colour  sense  or,  at  any  rate,  a  differential  reflex  action  to  different 
wave-lengths  of  light. ^  Many  of  these  animals,  however,  are  essentially 
nocturnal  or  frequent  ocean  depths  where  the  paucity  or  absence  of 
light  must  preclude  acute  vision.  It  is  probable,  indeed,  that  as 
determinants  of  behaviour  the  eyes  are  of  secondary  importance  to  the 

1  V.  Frisch  and  Kupelwieser  (1913),  Ewald  (1914),  Koehler  (1924),  Eckert  (1935), 
Heberdey  (1936),  Heberdey  and  Kupka  (1942),  Hmith  and  Baylor  (1953).  It  is  to  be 
remembered  that  these  differential  responses  may  be  served  by  different  mechanisms — 
tlie  dermatoptic  and  the  ocular. 

2  p.  573. 

^  Homarus — v.  Buddenbrock  et  al.  (1952). 

*  Schlieper  (1926-27),  Kastner  (1949)  in  the  crab,  Curcinus,  the  shrimp,  Crangon, 
a,'  the  prawn,  Leander. 


THE   VISION   OF   ARTHROPODS 


579 


sensory  bristles  which  are  distributed  all  over  the  body  and  appendages, 
particularly  the  antennae.  These  are  of  two  types,  being  sensitive  to 
touch  or  chemical  stimuli,  and  are  present  in  enormous  numbers  ;  in 
the  lobster,  for  example,  there  are  said  to  be  50,000  to  100,000  on  the 
pincers  and  walking  legs  alone. 

A  considerable  aptitude  to  training  is  evident  among  the  Malacostraca  but 
it  is  based  on  the  tactile  sense  rather  than  on  vision  ;  the  feat  of  mastering  a 
T-maze  is  easily  acquired  by  those  species  which  have  been  investigated  but  the 
aptitude  is  based  on  the  texture  of  the  walls  (Agar,  1927  ;  Gilhousen,  1929  ; 
ten  Cate-Kazejewa,  1934  ;  and  others),  and  is  equally  showTi  by  the  blind 
Isopod,  Asellus  (Bock,  1942). 


Asellus 


THE  \t:sio]S"  of  arachnids 

The  function  of  the  eyes  of  arachnids  is  very  variable  and  often 
crude.  The  smaller  species  (Acarines)  merely  respond  to  the  intensity 
of  light,  and  training  experiments  with  water-mites  (Hydracarina) 
utilizing  any  sense  have  been  unsuccessful  (Agar,  1927).  The  larger 
representatives,  however,  have  more  fully  developed  visual  functions. 
The  jerrymanders  have  relatively  good  vision  ;  but  with  the  exception 
of  spiders  the  other  Arachnids  probably  only  perceive  variations  in  the 
intensity  of  light  and  movement  ;  the  optics  of  their  ocelli  is  poor  and 
the  number  of  visual  cells  small,  while  visual  impressions  seem  to  play 
an  insignificant  part  in  their  behaviour. 

THE  VISION  OF  SPIDERS  has  received  more  attention  than  that  of 
any  other  type  (Petrunkevitch,  1907-11  ;  Homann,  1928-53  ;  Millot, 
1949  ;  Drees.  1952).  It  is  true  that  the  web-spinners  with  their 
rudimentary  ocelli  of  a  short  effective  visual  range  are  not  particularly 
visually  conscious,  for  their  behaviour  is  dominated  essentially  by 
their  exquisite  sense  of  touch  ;  any  tremor  on  the  web  caused  by  an 
alighting  insect  excites  their  immediate  attention,  probably  while  the 
object  causing  the  tremor  is  still  out  of  the  range  of  their  vision.  It 
is  interesting  that  this  sense  of  vibrotropism  is  purely  reflex,  for  photo- 
graphy has  showT;!  that  the  waiting  spider  orientates  itself  so  that  the 
vibrations  of  the  web  stimulate  the  legs  on  each  side  equally  and  then 
sets  out  in  a  straight  path  for  its  victim.  Similarly,  ripple-spiders  sit 
at  the  water's  edge  resting  their  forelegs  on  the  surface  waiting  to 
appreciate  the  ripples  set  up  by  an  alighting  insect.  In  the  same  way 
the  vibrations  of  a  tuning  fork  on  the  web  or  in  the  water  will  excite 
the  spider  to  run  out  as  if  to  capture  prey.  The  more  active  hunting 
types,  however,  which  move  abroad  to  chase  their  prey,  base  their 
behaviour  progressively^  upon  vision,  each  element  in  the  ocellar 
system  having  a  particular  function  and  the  whole  acting  in  a  curiously 
reflex  manner. 


Jeri'S'maudsr 


'eb-spinner, 
Arunea 


^v 


olf-spider, 

Lycosa 


580 


THE   EYE   IN   EVOLUTION 


Evarcha  blancardi 


The  behaviour  of  the  jumping  spider,  Evarcha  blancardi,  the  arrangement 
of  the  ocelli  of  which  is  shown  in  Fig.  216,  may  be  taken  as  an  example.  It  sees 
its  prey  (or  mate)  with  the  posterior  lateral  eyes  which,  situated  far  back  on  the 
head,  have  a  wide  field  of  vision  and  respond  to  moving  stimuli  only  ;  a 
stationary  object  excites  no  reaction.  As  the  image  of  the  moving  object 
crosses  the  retinae  of  these  ocelli,  the  spider  reflexly  turns  its  body  in  the  direction 
of  the  object  with  the  result  that  the  image  falls  on  the  retina  of  one  of  the 
anterior  lateral  ocelli,  whereupon  a  further  turning  movement  throws  the  image 
on  both  anterior  lateral  ocelli  and  the  two  central  ocelli.  If  the  former  ocelli 
are  covered,  this  second  turning  movement  does  not  occur.  It  would  seem  that 
the  function  of  these  ocelli  is  to  judge  distance  binocularly,  that  of  the  central 
ocelli,  which  have  a  small  field  and  a  short  range,  to  perceive  the  form  of  the 
prey  ;  in  each  the  lens  is  capable  of  forming  sharp  images.  A  male,  for  example, 
acts  as  if  it  can  distinguish  between  a  female  of  its  own  species  or  a  male  of  its 
own  or  another  species  at  a  distance  of  2  to  3  cm.  At  a  distance  of  1-5  cm.  it 
leaps  upon  its  victim  with  accuracy,  but  if  the  lateral  anterior  ocelli  are  covered 
the  distance  of  the  leap  is  misjudged.  The  posterior  lateral  ocelli  therefore  act 
as  the  peripheral  retina  of  man,  collecting  impressions  from  the  whole  visual 
field  ;  the  front  row  of  four  eyes  acts  together  as  the  human  fovea,  the  lateral 
pair  being  most  useful  binocularly  at  a  short  distance,  the  central  pair  being  the 
chief  agent  for  visual  analysis.  The  small  jaosterior  median  pair  of  ocelli,  on  the 
other  hand,  are  used  for  the  detection  of  movement  behind  the  sj^ider. 

The  reflex  nature  of  the  response  is  illustrated  by  the  automatic  movements 
of  the  limbs  following  retinal  stimulation.  Homann  found  that  on  covering  the 
two  median  ocelli  the  first  pair  of  legs  was  held  up  by  the  contraction  of  the 
femoral  muscles  and  as  the  animal  ran  forwards  they  merely  clawed  the  air 
instead  of  touching  the  ground  ;  if  one  of  these  eyes  were  covered  the  foreleg 
on  the  blind  side  alone  was  held  up  and  the  body  was  tilted  sideways. 

Despite  the  apparent  automatism  of  this  reflex  response,  however, 
spiders  display  a  very  considerable  degree  of  visual  intelligence. 
Nowhere  is  this  more  aptly  illustrated  than  in  the  stalking  of  a  fly  on  a 
creviced  wall  by  a  jumping  spider.  Spying  a  fly  settled  on  the  wall  some 
distance  away,  the  spider,  knowing  that  the  attention  of  the  fly  will  be 
excited  at  once  by  a  moving  object,  creeps  with  the  greatest  care  to  the 
nearest  crevice  in  the  brickwork.  Arrived  there,  knowing  that  the  fly 
will  soon  take  wing,  it  scampers  rapidly  along  the  crevice  hidden  from 
view  until  it  comes  within  range  of  its  victim  ;  thereupon,  anchoring  it- 
self by  a  life-line  of  silk  to  the  brickwork,  it  leaps  upon  its  victim  with 
incredible  rapidity,  hoisting  itself  back  to  safety  by  the  silken  cord. 

Moreover,  in  their  visual  activities  a  considerable  degree  of  sensory 
analysis  exists,  for  jumping  spiders  can  be  negatively  conditioned  to 
unpalatable  prey,  and  Drees  (1952)  found  that  their  form  vision  is 
sufficiently  effective  to  allow  negative  conditioning  by  means  of  an 
electric  shock  to  a  response  acquired  by  training  to  visual  stimuli  such 
as  triangles  and  crosses.  It  is  also  of  interest  that  the  jumping  spider 
has  been  shown  by  its  response  to  the  optomotor  reaction  to  have  a 
;-elective  sensitivity  to  orange  (Kastner,  1949),  a  response  which  may 
ijvlicate  some  degree  of  "  colour  vision  "  on  a  reflex  level. 


THE   VISION   OF   ARTHROPODS 


581 


THE    VISION    OF    INSECTS 

The  mastery  of  a  new  element  and  the  adventure  of  the  experiences 
afforded  by  a  third  dimension  would  be  expected  to  give  a  fillip  to  the 
sensory  reactions  of  Insects,  while  the  development  of  flight  with  the 
consequent  ease  and  speed  of  exploring  new  environments  must  stress 
the  importance  of  efficient  distance  recejDtors  in  the  gathering  of 
adequate  data  for  effective  orientation.  These  expectations  have  been 
realized  ;  and  to  Insects  much  the  most  important  recej^tor-organs  are 
the  eyes.  Indeed,  in  their  efficiency, 
theii'  capacity  to  resolve  a  pattern  or 
to  interpret  movements,  the  eyes  of 
Insects  excel  those  of  most  Verte- 
brates ;  moreover,  alone  among  In- 
vertebrates many  species  have  a  fully 
developed  colour  sense,  while  they 
have  assumed  a  faculty  apparently 
unique  to  Arthropods — the  power  to 
analyse  the  plane  of  polarization  of 
light  and  orientate  themselves  there- 
by. Finally,  small  though  the  insect 
brain  may  be,  and  dominated  though 
the  creature  is  by  automatic  and 
rigid  reflex  reactions,  it  shows  an 
amenability  to  learning  and  a  power 
to  remember  unique  in  the  inverte- 
brate world  ■^^*^"  ^'^^' — ■'-^^^  Head  of  the  Moth 

SHOWING  THE  EyES  AND  THE  EnOR- 

In     the     behavioural     activities     of  mous  Antenn.ts  (Richard  Cassell). 

Insects  other  senses  are  also  inijoortant. 

The  olfactory  sense,  indeed,  would  seem  to  be  more  fundamental  than  vision  ; 
thus  it  has  been  shown  by  Schremmer  (1941)  that  newly  emerged  specimens  of 
the  moth,  Plusia  gamma,  seek  flowers  by  scent  only,  this  faculty  being  presumably 
imiate,  but  that  once  an  association  with  a  particular  flower  has  thus  been 
established,  further  visits  are  determined  by  vision  and  scent.  Moreover,  in 
the  recognition  of  their  fellows  and  as  a  guide  to  homing  when  illumination  is 
ineffective,  odour  is  often  a  major  determinant  of  conduct  ;  the  male  moth,  for 
example,  with  its  extremely  sensitive  antennte,  is  said  to  find  a  female  a  mile 
or  more  distant  by  this  means  alone  (Fig.  731)  (Bonnett,  1779-83  ;  Turner, 
1907  ;     Schneirla,    1929-33  ;     Carthy,    1950  ;    Vowles,  1955  ;    Dethier,  1957). 

The  organs  of  smell  are  situated  on  the  last  8  segments  of  the  antenna? 
and  consist  of  minute  pits  -which  are  present  in  large  numbers,  sometimes  ujo  to 
a  thousand  on  a  single  joint.  The  taste  organs  occur  not  only  on  the  mouth 
and  labial  paljDS  but  also  sometimes  on  the  antemije  and  the  feet.  The  sense  of 
touch  is  subserved  by  minute  hairs  associated  with  the  antennae,  the  maxillie 
and  the  face  ;  the  sette  are  non-living  but  each  has  a  sensory  cell  at  its  base  with 
nervous  connections.  Many  species  are  without  ears  but  they  are  certainly  well 
develojDed  in  insects  cajDable  of  producing  sounds  :  when  they  are  present  each 


582 


THE   EYE   IN   EVOLUTION 


Caterpillar 


Sarcophagn 


ear  consists  of  a  pit  filled  with  air  or  fluid  across  the  opening  of  which  is  stretched 
a  drum-like  membrane.  In  some  Orthoptera  the  ears  are  on  the  shanks  of  the 
front  pair  of  legs  or  on  the  sides  of  the  abdomen  above  the  base  of  the  third  legs  ; 
in  others  on  the  first  segment  of  the  body  ;  in  blow-flies  under  the  bases  of  the 
wings  ;  in  gnats  on  the  bases  of  the  antennae  ;  and  so  on.  In  all  the  sense  organs 
there  is  a  considerable  variation  between  species,  while  there  may  well  be  one 
or  more  types  of  sense  organs  with  which  we  are  not  familiar  that  have  no 
counterpart  in  the  vertebrate  sensorium. 

The  visual  function  of  the  larv^  of  insects  is  relatively  crude, 
a  necessary  corollary  of  the  simplicity  of  the  structure  of  the  stemmata. 
In  the  more  simple  forms  a  crude  sensitivity  to  light  is  the  only  possible 
response,  but  in  the  more  elaborate  forms,  particularly  when  the  eyes 
occur  in  groups,  a  coarse  mosaic  imagery  with  some  degree  of  form 
vision  is  possible.^  It  may  well  be  that  the  pendular  movements  of  the 
anterior  part  of  the  body  exhibited  by  so  many  caterpillars  are  an 
expedient  to  mediate  form  vision  by  scanning  movements  with  the 
simple  apparatus  available,  the  visual  impressions  being  perhaps 
coordinated  with  proprioceptive  stimuli  derived  from  the  motion.  The 
entire  group  of  stemmata  functions  as  a  unit  and  if  all  are  covered 
except  one,  form  perception  is  lost  and  only  phototactic  responses 
remain  (Friederichs,  1931  ;  Dethier,  1942-43).  The  fact  that  the 
caterpillars  of  butterflies  {Va7iessa)  are  attracted  by  green  leaves  or 
paper  of  the  same  colour  suggests  the  possibility  of  a  crude  colour 
sense  (Gotz,  1936).  Finally,  the  stemmata  of  some  species  are  capable 
of  utilizing  the  pattern  of  polarization  of  light  as  a  means  of  orientation. ^ 

The  function  of  the  dorsal  ocelli  of  adults  is  more  proble- 
matical ;  since  their  principal  focus  does  not  coincide  with  the  retinal 
plane,  they  are  ill-designed  for  image-formation  although  well  adapted 
to  admit  hght  (Homann,  1924  ;  Wolsky,  1930-31  ;  Cornwell,  1955). 
Any  capacity  for  the  perception  of  form  is  therefore  probably  negligible. 
In  view  of  the  facts  that  some  insects  with  only  their  ocelli  uncovered 
behave  as  if  blind  and  that  the  reflex  responses  of  the  compound  eyes 
to  light  are  less  rapid  when  the  ocelli  are  covered,  it  has  been  suggested 
that  the  ocelli  are  stimulatory  organs  which  accentuate,  although  they 
do  not  initiate,  phototactic  responses. ^  In  other  species,  however, 
they  have  been  shown  to  participate  fully  in  the  activities  of  the 
animal,*  while  they  are  the  only  effective  organs  in  those  species  in 
which  compound  eyes  are  lacking.^  Moreover,  it  was  shown  by  Welling- 
ton (1953)  that  the  ocelli  of  the  flesh-fly,  Sarcophaga,  are  sensitive  to 

1  Larvse  of  the  tussock-moth,  Lymantria — de  Lepiney  (1928)  ;  of  the  beetle, 
Cicindela — Friederichs  (1931). 

2  Saw-fly,  butterfly— Wellington  et  al.  (1951),  Wellington  (1953)  (p.  66). 

3  In  ants — Homann  (1924)  ;  bees — Mliller  (1931)  ;  the  fly,  Drosophila — Bozler 
(1925),  Parry  (1947),  Cornwell  (1955). 

^  In  the  bug,  Cryptoti/mpana — Chen  and  Young  (1943)  ;    the  flesh-fly,  Sarcophaga 
--Wellington  (1953). 
5  p.  221. 


THE   VISION   OF  ARTHROPODS 


583 


changes  in  polarized  light  and  thus  aid  in  orientation.  In  the  locust, 
illumination  of  the  compound  eye  produces  on-  and  off-spike  potentials 
in  the  ventral  nerve  cord,  of  the  ocelli  off-responses  only  (with  perhaps 
a  very  brief  on-response,  Hoyle,  1955)  ;  the  former  responds  to  move- 
ments of  an  external  object  while  the  latter  does  not  (Burtt  and  Catton, 
1954-56).  It  would  thus  seem  obvious  that  the  function  of  the  ocelli 
of  Insects  varies  in  different  types  depending  on  such  factors  as  the 
degree  of  development  of  the  compound  eye  and  the  habits  of  the 
species. 


Locusta 


THE  COMPOUND  EYES  OF  INSECTS,  on  the  Other  hand,  possess 
functional  attributes  of  a  high  order  which  have  been  extensively 
investigated  ^  ;  their  appreciation  of  light  and  colour  as  well  as  form, 
movement  and  spatial  relationships  compares  well  with  that  of  many 
tjrpes  of  Vertebrates.  Moreover,  in  some  insects  the  compound  eye, 
occasionally  in  addition  to  the  ocelli,  can  appreciate  changes  in  the 
polarization  of  light. ^ 

More  study  has  been  devoted  to  the  function  of  the  compound  eye 
of  Insects  than  to  the  eyes  of  any  other  Invertebrate.  The  two 
classical  methods  of  apjJroach  ^  have  been  adopted — behavioural 
experiments  and  reactions  based  on  the  electro-physiological  charac- 
teristics of  the  eye  on  stimulation  by  light.  The  first  is  the  more 
informative  in  that  it  gives  some  idea  of  the  sensations  appreciated 
by  the  insect  concerned,  but  insofar  as  many  insects  are  untrainable 
perhaps  because  of  their  automatism,  perhaps  because  of  lack  of 
intelligence,  the  method  is  by  no  means  universally  applicable.  It 
is  always  to  be  remembered,  of  course,  in  interpreting  the  results 
of  the  second  method,  that  physiological  responses  on  a  reflex  level 
need  not  necessarily  ascend  into  the  level  of  consciousness  and  can 
only  be  translated  with  the  greatest  reserve  into  terms  of  sensation. 

Behavioural  eiyeriinents  depending  on  the  laying  down  of  con- 
ditioned reflexes  can  be  made  available  for  the  investigation  of  the 
responses  of  many  insects  ;  the  honey-bee,  A2}is,  for  example,  can  be 
trained  to  go  to  a  container  with  sugar  placed  beside  a  black  disc  and 
avoid  one  marked  with  a  black  cross  (v.  Buddenbrock,  1937). 
Unconditioned  reflex  responses  such  as  the  optomotor  reaction  to  black 
and  white  stripes  on  a  moving  drum  are  also  readily  elicited  in  many 
insects.  Again,  the  honey-bee  is  very  sensitive  to  stimulation  of  this 
type,  responding  if  stationary  by  a  reflex  sideways  movement  of  the 
head  and  thorax  ;  if  it  is  crawling  it  makes  a  sudden  change  of  direction 
opposite  in  sign  to  that  of  the  movement  of  the  environmental  pattern. 
In  similar    circumstances  the    fruit-fly.    Drosophila,    will    completely 

1  See  among  others,  Eltringham  (1933),  v.  Frisch  (1950),  Wigglesworth  (1953). 

2  p.  66.  »  p.  568. 


Apis 


Drosophila 


584 


THE   EYE   IN   EVOLUTION 


Vespa 


Dytiscus 


Cockroach 


reverse  its  direction  of  movement,  a  reaction  repeated  with  dramatic 
precision  on  each  occasion  and  in  rapid  succession  on  repeated  stimuli. 
If  the  field  is  kept  stationary  a  moving  insect  shows  the  same  type  of 
response  to  the  shift  of  the  retinal  image  produced  by  its  own  move- 
ment (v.  Buddenbrock  and  Moller-Racke,  1952). 

The  electro-physiological  characteristics  of  the  visual  mechanism 
have  recently  been  applied  with  considerable  success  to  the  physiology 
of  the  compound  eye.  Depending  on  the  type  of  electrical  response 
on  stimulation  by  light,  two  distinct  physiological  types  have  been 
differentiated  by  Autrum  and  his  co-workers  (1948-53). 

(1)  FAST  'EY'E.s,  found  in  rapidly  flying  diurnal  insects  (the  blow-fly, 
Calliphora,  the  bees,  A2ns  and  Bombus,  the  wasp,  Vespa,  and  so  on). 
On  stimulation  by  light  the  electro -physiological  characteristic  of  such 
an  eye  is  a  diphasic  wave  made  up  of  an  initial  positive  response 
indicating  the  on-effect,  followed  by  a  terminal  negative  response 
indicating  the  off-effect  ;  on  prolonged  stimulation  the  initial  positive 
response  subsides  rapidly.  In  such  an  eye  there  is  a  high  temporal 
resolution  with  a  response  to  intermittent  stimulation  in  the  form  of 
flicker  up  to  250  or  300  stimuli  per  sec.  The  absolute  threshold  of 
sensitivity  to  light  is,  however,  high  ;  the  reaction  is  little  affected  by 
light-  and  dark-adaptation  ;  and  the  optomotor  response  shows  an 
ability  to  discriminate  between  stimuli  of  200  per  sec. 

(2)  SLOW  EYES,  seen  in  nocturnal,  aquatic  or  slow-moving  insects 
such  as  the  grasshopper,  the  water-beetle,  Dytiscus,  and  cockroaches 
(as  well  as  Limulus).  Such  an  eye  is  characterized  by  a  low  threshold 
of  flicker  to  intermittent  stimulation  up  to  40  to  50  per  sec.  ;  the 
absolute  threshold  of  sensitivity  is  low  ;  the  reaction  changes  markedly 
in  light-  and  dark-adaptation  ;  and  the  subjective  optomotor  response 
can  be  obtained  only  by  stimuli  up  to  5  to  10  sec. 

The  experimental  evidence  makes  it  probable  that  the  characteristic 
properties  of  these  two  types  of  eye  are  attributable  more  to  the  central  neurones 
than  to  the  end -organ,  particularly  to  the  first  optic  ganglion  ^  (Autrum, 
1951-54  ;  Autrum  and  Gallwitz,  1951).  The  optic  lobes  of  both  types  are  the 
source  of  spontaneous  electrical  oscillations  ^  elicited  by  the  onset  or  cessation 
of  stimulation  ;  in  the  slow  type  of  eye  the  frequency  of  these  rhythms  lies  between 
20  and  35  cycles/sec;  in  the  fast  type,  between  120  and  160/sec.  (Adrian,  1937  ; 
Boeder,  1939-40  ;  Crescitelli  and  Jahn,  1942  ;  Massera,  1952  ;  Autrum,  1952  ; 
Burkhardt,  1954),  and  it  is  noteworthy  that  the  fast  type  can  be  converted  into 
the  slow  type  by  the  surgical  removal  of  portions  of  the  optic  lobe  (Autrum  and 
Gallwitz,  1951  ;    Autrum,  1951-52). 


In  general,  insects  respond  to  the  short  waves  of  the  spectrum 
rather  than  to  the  long.  The  cornea  (of  the  bee,  Apis,  and  the  flesh-fly, 
Sarcophaga)   is  transparent  to  wave-lengths  as  short  as  253mft,  the 


1  p.  524. 


p.  524. 


THE   VISION   OF   ARTHROPODS 


585 


tracheal  tapetiim  fluoresces  in  ultra-violet  light  and  it  would  seem 
probable  that  the  retinal  cells  are  sensitive  to  rays  of  this  type  (Lutz, 
1924-33  ;  Bertholf,  1930-32  ;  Lutz  and  Grisewood,  1934  ;  Carter, 
1948).  Photo -negative  insects  such  as  the  ant  thus  take  shelter  from 
ultra-violet  light  unseen  by  the  human  eye  (Lubbock,  1885  ;  Forel, 
1886)  and  light-seeking  insects  such  as  moths  and  bees  are  attracted 
by  it  (Fig.  732)  (Lutz,  1924-33  ;  Lutz  and  Grisewood,  1934).  On 
the  other  hand,  although  some  species  ^  undoubtedly  respond  to  red 
(up  to  690  m/x),  most  are  not  attracted  by  this  colovir  because  of  the 
high  threshold  but  treat  red  as  black. ^ 

In  optomotor  experiments  when  dark  and  light  grey  stripes  are 


57&  -  492  436  405 


365 


Fig.   732. — The  Spectral  Sensitivity  of  the  Honey-Bee. 

Indicating  the  attraction  of  the  ultra-violet  part  of  the  siDectrum.  The  numbei-s 
indicate  \va\-e-lengths  in  m/x   (Tinbergen,  after  Klihn). 


Ant 


Moth 


used,  the  discrimination  of  luminosity-differences  is  found  to  be  generally 
low — about  20  times  lower  in  the  bee  than  in  man.  and  in  some  other 
insects  poorer  still  (Wolf,  1933  ;  Hecht  and  Wald,  1934  ;  v.  Budden- 
brock,  1935  ;  Hundertmark,  1937-38).  When  coloured  light  is  used 
as  a  stimulus  it  is  found  that  the  most  effective  parts  of  the  spectrum 
are  generally  in  the  yellow-green  and  ultra-violet,  particularly  the 
latter  (Fig.  733).'^  The  spectral  location  of  the  first  region  corresponds 
closely  to  the  peak  of  the  luminosity-curve  in  man,  the  variation 
in   some  insects  resembling  the  human  dark-adapted  state  {Apis)  and 

1  Such  as  butterflies  (Pieris,  Vanessa — Use,  1928),  fire-flies  {Pholinus — Buck,  1937) 
and  locust  hoiDpers  (Locusta — Chapman,  1954). 

2  The  honey-bee,  Ajiis — v.  Frisch  (1914),  Kiihn  (1927)  ;  the  wasj},  Vespa — 
Schremmer  (194"l). 

^  553  m^  in  the  yellow-green  and  365  ni/tx  in  the  ultra-violet  for  the  bee,  Apis, 
(Bertholf,  1931-32  ;  Sander,  1933  ;  Weiss  et  al.,  1941-43  ;  and  others).  540  m/x  for 
the  equal  energy  spectrum  in  Drosophila  (Medioni,  1956).  The  same  applies  roughly 
to  Crustaceans  (p.  578). 


586 


THE   EYE   IN   EVOLUTION 


Calliphora 


in  others  the  human  Hght-adapted  state  (Pieris)  (SchHeper,  1927-28  ; 
Use,  1932).  The  electroretinogram  obtained  on  stimulating  the 
retina  with  different  wave-lengths  also  shows  a  curve  resembling 
the  absorption-curve  of  visual  purple  in  Vertebrates  (the  grasshopper, 
Melanoj)lus — Jahn,  1946).  The  occurrence  of  a  Purkinje  shift  towards 
shorter  wave-lengths  in  decreasing  intensity  of  light  in  some  insects 
suggests  the  presence  of  two  receptor  mechanisms  {Drosophila — 
Fingerman  and  Brown,  1952-53)  ;  in  this  connection  the  presence 
of  twin-peak  sensitivities  in  electroretinograms  is  also  of  interest  (at 
630  and  540  mfx  in  Calliphora — Antrum  and  Stumpf,  1953).  These, 
of  course,  are  measurements  of  the  threshold  of  physiological  response, 
not  of  sensation. 


YELLOW.  YELLOW-  GREEN    CREEN- 
-CREEN  -BLUE 

Fig.   733. — Colour  Vision  in  Insects. 

A  chart  showing  the  relative  number  of  visits  of  Gonepteryx  r^^anini  to 
papers  of  different  colours  during  the  feeding  phase  (after  Use). 


Cetonia 


Geotrupes 


The  capacity  for  colour  vision  in  insects  has  given  rise  to  some 
controversy.  It  would  seem  reasonable  to  suppose  that  the  brilliant 
colours  of  flowers  would  be  oecologically  linked  with  the  insect  visitors 
on  which  so  many  plants  depend  for  their  propagation.  kSuch  a  sugges- 
tion demands  that  flower-visiting  insects,  which  reciprocally  depend 
on  the  flowers  for  their  food,  should  appreciate  and  differentiate  the 
variegated  riot  of  colour  evolved  for  the  mutual  benefit  of  both.  It 
must  not  be  thought,  however,  that  colour  vision  in  insects  is  confined 
to  those  that  visit  flowers  or  that  its  function  has  been  evolved  specific- 
ally for  this  purpose  and  none  other  ;  the  flower-visiting  beetle,  Cetonia, 
for  example,  is  colour-blind,  whereas  the  dung-beetle,  Geotrupes,  is 
endowed  with  a  well-developed  colour  sense.  However  that  may  be, 
it  has  long  been  accepted  for  this  reason  that  most  insects  are  possessed 
of  colour  vision.  The  first  to  extricate  this  problem  from  the  vagueness 
of  speculation  and  subject  it  to  scientific  analysis  was  Sir  John  Lubbock 
(1885)  who  applied  the  relatively  simple  but  somewhat  inconclusive 
technique  of  "  preferential  choice."  ^  On  exposing  honey  on  coloured 
cards  and  recording  the  frequency  with  which  each  was  visited,  he 
found  that  the  honey-bee  exhibited  a  substantial  degree  of  colour 
differentiation  with  a  marked  preference  for  blue.     At  a  considerably 

1  p.  568. 


THE   VISION   OF   ARTHROPODS 


587 


later  date,  however,  Carl  von  Hess  (1913)  concluded  on  the  basis  of 
similar  experiments  that  this  insect  moved  towards  different  lights 
depending  on  their  relative  intensity  and  that  it  was  colonr-blind  ;  but 
von  Frisch  (1914-50),  in  a  long  series  of  well-controlled  experiments 
wherein  other  factors  were  excluded,  confirmed  Lubbock's  original  con- 
clusion and  demonstrated  that,  after  training,  the  bee  reacted  selectively 
when  presented  with  sugar-water  associated  with  differently  coloured 
squares  on  a  checkerboard,  preferring  blue  and  yellow  to  other  hues. 
These  results  were  corroborated  in  the  bee  by  Kiihn  and  Pohl  (1921) 
and  Kiihn  (1927),  who  used  pure  spectral  colours,  and  by  various  tech- 
niques in  other  species  (Fig.  733). ^ 

The  results  of  the  earlier  investigators  gave  the  impression  that 
the  bee  was  only  able  to  distinguish  between  two  groups  of  colours, 
the  yellow  group  and  the  blue-violet  group  ;  but  although  this  applies 
in  a  general  way  to  their  reaction  to  the  colours  of  flowers  in  nectar- 
hunting,  it  was  later  demonstrated  that  this  insect  was  able  to  dis- 
tinguish several  colours  within  each  group  if  trained  to  show  differential 
responses  (Lotmar,  1933).  Thus  after  training  to  bands  of  spectral  light, 
bees  have  been  found  to  distinguish  four  regions  :  650-500  m^u,  (red- 
green),  500-480  mfx  (green-blue),  480-400  m/x  (blue-violet),  and  400-310 
mjjt,  (ultra-violet),  the  last  being  probably  perceived  as  a  colour 
(Kiihn,  1927  ;  Hertz,  1939).  At  a  later  date  Daumer  (1956)  interpreted 
the  reactions  of  bees  as  mediated  through  3  types  of  receptors — yellow, 
blue,  and  ultra-violet.  Red  flowers  seem  to  be  distinguished  because 
of  their  reflection  of  ultra-violet.  The  colour  system  of  the  bee  is 
therefore  widely  different  from  that  of  man.-  Moreover,  on  testing 
optomotor  reactions,  von  Buddenbrock  and  Moller-Racke  (1952) 
concluded  that  butterflies  have  three  receptors — an  orange-red,  a 
yellow  and  a  green-blue.  It  would  thus  ajDpear  that  different  species 
have  different  types  of  colour  vision  (Use,  1928-49  ;  Schlegtendal, 
1934),  while  some  may  be  colour-blind.^  Finally,  various  regions  of 
the  compound  eye  may  react  differently  :  thus  the  antero -ventral 
jDortion  of  the  eye  of  the  water-boatman.  Notoiiecia,  is  equally  sensitive 
to  all  colours  while  the  dorso-posterior  part  shows  preferential  differ- 
ences in  colour-sensitivity  (Liidtke,  1938-54  ;  Rokohl,  1942  ;  Resch, 
1954). 

It  is  interesting  that  different  mechanisms  are  apphed  in  different  activities 
since  innate  reactions  show  a  selective  responsiveness  to  very  different  stimuli  ; 
one  reaction  inay  be  released  by  the  intensity  of  light,  another  by  its  wave- 

^  The  bee-fly,  Bombylius,  and  the  hawk-moth,  Macroglossa — Knoll  (1925-26)  ; 
butterflies,  Pieris,Go)iepteri/.v  and  Vanessa — Use  (1928).  Tinbergen  et  al.  (1942);  the  aphid, 
Myzus — ]Moricke  (1950)  ;  the  fruit-fly,  Drosophila — Fingerman  and  Brown  (1952-53). 

^  And  also  different  from  that  of  birds  which  are  attracted  preferentially  to  red 
flowers  (p.  630). 

^  Such  as  the  nocturnal  stick-insect,  Dixippus,  and  the  bug,  Troilus  (Hundertmark, 
1936-37;  Schlegtendal,  1934). 


Xotonecta 


588 


THE   EYE   IN  EVOLUTION 


Musca 


Butterfly,  Vanessa 


length  ;  in  one  response  the  bee  may  act  as  if  colour-blind,  in  another  as  if 
partially  so,  and  in  a  third  it  may  show  a  wide  discrimination  of  hues.  In  the 
same  way  the  hawk-moth,  Macroglossa,  selects  yellow  and  blue  objects  when 
hungry,  yellow-green  backgrounds  for  oviposition,  and  dark  surroundings  of 
any  colour  for  hibernation  (Knoll,  1925-26).  This  restriction  of  a  specific 
response  to  a  few  "  sign-stimuli  "  rather  than  to  all  possible  environmental  clues 
is  of  wide  application  ;  it  is  well  exemplified  in  the  ajaparent  blindness  of  the 
water-beetle,  Dytiscus,  in  its  hunting  reactions  ^  and  is  by  no  means  confined 
to  Insects.^ 

The  perception  of  form  in  insects  appears  to  be  rudimentary.  The 
visual  acuity  as  measured  by  responses  to  revolving  striped  drums  is 
relatively  low  (Hertz,  1929-39  ;  Hecht,  1931)— about  1/100  that  of 
man  in  the  bee,  1/1,000  in  Drosophila  (Baumgartner,  1928;  Hecht  and 
Wolf,  1929  ;  Hecht  and  Wald,  1934  ;  Gavel,  1939  ;  Roeder,  1953), 
while  in  the  house-fly,  Musca,  the  narrowest  stripe  that  can  be 
perceived  subtends  an  angle  of  5°  (Gaffron,  1934)  (in  man,  1').  These 
results  of  behavioural  experiments  correspond  with  the  theoretical 
acuity  deduced  from  the  structure  of  the  eye  (Piitter,  1908  ;  Best, 
1911).3 

As  would  be  expected  from  their  low  standard  of  visual  acuity, 
the  capacity  of  insects  to  analyse  a  pattern  is  relatively  poor.  It  is 
true  that  experiments  have  shown  that  bees  and  butterflies  can  be 
attracted  by  broken  or  checkered  figures  and  divided  contours  to 
which  they  have  been  trained,  a  response  which  confirms  the  biological 
value  of  "  honey  guides  "  on  flowers  (Zerrahn,  1933  ;  Hertz,  1935  ; 
Bolwig,  1938).^  It  is  also  true  that  the  honey-bee  can  be  trained  to 
seek  a  sugar-container  associated  with  a  black  disc  and  avoid  one 
associated  with  a  black  cross  or  can  differentiate  four  parallel  lines 
from  a  black  circle  ;  but  it  cannot  be  conditioned  to  distinguish 
between  a  black  cross  and  four  parallel  lines  on  a  white  surface  (von 
Buddenbrock,  1952).  In  order  to  allow  the  discrimination  of  patterns, 
therefore,  the  differences  must  be  gross.  It  is  probable,  indeed, 
particularly  in  so  far  as  the  "  fast  "  type  of  eye  is  concerned,  that  the 
response  is  less  to  the  recognition  of  the  configuration  of  objects  than 
to  the  frequency  of  change  of  retinal  stimulation  (Wolf,  1933-37)  and 
that  fast-flying  diurnal  insects  resolve  the  spatial  display  of  a  pattern 
into  a  temporal  display  of  sequential  stimuli.  The  method  of  interpreta- 
tion of  slow-moving,  nocturnal  or  aquatic  insects  is  not  yet  known. 

From  these  characteristics  it  follows  that  moving  objects  excite 

1  p.  103,  Fig.  74.  2  p.  664.  ^  p_  m 

^  It  must  not  be  thought  that  all  the  adult  bee's  activities  in  visiting  flowei's 
for  honey  are  determined  by  vision.  At  relatively  close  quarters  the  sense  of 
smell  is  important.  Bees  can  be  trained  to  react  to  scent  alone.  Moreover,  when  the 
insect  lands  on  the  flower,  taste-organs  which  occur  not  only  on  the  inouth  but  on 
tlic  antennse,  labial  palps  and  feet,  come  into  play.  In  the  search  for  honey,  therefore, 
tlio  ■,;yes  are  the  distance-receptors,  the  organs  of  smell  the  intermediate,  and  of  taste 
the  contact-receptors.     See  Bolwig  (1954)  and  others. 


THE   VISION   OF   ARTHROPODS 


589 


attention  and  stationary  objects  tend  to  be  neglected.  This  tendency- 
is  borne  out,  as  we  have  already  seen  ^  in  behavioural  experiments 
involvmg  the  optomotor  response  to  a  striped  drum  which  shows  a  high 
flicker-threshold  up  to  200  per  sec.  in  the  bee,^  the  corresponding 
figures  in  man  as  measured  by  the  fusion  frequency  of  flicker  being 
50  to  100  depending  on  the  intensity 
of  illumination  and  the  size  of  the 
fleld  stimulated  (Collins  and 
Hopkinson,  1954)  ;  similarly,  the 
fusion-frequency  as  measured  by  the 
changes  in  the  electrical  potential  of 
the  retina  in  many  insects,  particu- 
larly of  the  rapidly  flying  diurnal 
type,  may  reach  very  high  values,^  a 
capacity  doubtless  correlated  with 
the  need  to  resolve  succeeding  im- 
pressions during  flight.  It  would 
thus  seem  that  in  their  activities 
insects  depend  much  more  on  the 
primitive  faculty  of  the  appreciation 
of  movement  than  of  form.  The 
widely  over-lapping  visual  fields  of 
the  compound  ej^es  allow  jjerception 
of  distance,  a  power  of  judgment 
which  is  impaired  if  one  eye  is 
obscured  (Homann,  1924):  and  be- 
havioural experiments  show  that  a 
high  degree  of  spatial  appreciation 
and  localization  is  possible  (Tinbergen, 
1932-38  ;  Wiechert,  1938).  The 
extraordinary  capacity  of  some 
insects  for  memorizing  and  recogniz- 
ing landmarks  in  their  territory  has 
already  been  discussed  at  length.^ 

The  dependence  of  insects  on  visual  stimulation  by  moving  objects  is  seen 
in  the  every-day  behaviour  of  the  ordinary  house-fly  which  neglects  stationary 
objects  but  uTimediately  absconds  on  the  first  suggestion  of  movement.  It  is 
also  exemi^lified  in  a  striking  way  by  the  habits  of  the  j^raying  mantis  (Fig.  734)  ; 

1  13.  583. 

2  60  stimuli  per  sec.  in  Aeschna  nymphs,  Salzle  (1932),  and  in  Anax  nymj^hs, 
Crozier  et  al.  (1937)  ;    see  also  Autrum  and  Stocker  (1952),  Autrum  (1954). 

^  95  per  sec.  in  the  ocellus  of  the  bee  (Ruck,  1954)  and  of  the  order  of  165-300 
stimuli  per  sec.  in  the  compound  eye  of  this  insect,  or  265  per  sec.  in  the  blue-bottle 
CalUpliora  (Autrum  and  Stocker,  1950  ;  Autrum,  1952).  Corresi^onding  measurements 
ill  man  with  the  electroretinogram  are  25-30  for  the  scotojDic  and  70  for  the  photojjic 
fusion  frequencv  (  Wadensten,  1956  ). 

*  p.  78. 


Fig.     734. — The     Praying     Mantis, 

MaXTIS    RELiaiOSA 

Sitting  on  a  leaf.  Note  the  large 
and  prominent  eyes  and  the  "  praying  " 
position  of  the  front  legs.  The  ter- 
minal part  of  the  bent  fore -leg  with 
its  powerful  joint  resembles  a  pen- 
knife, normally  held  half  open  ready  to 
snap  shut  against  its  "  sheath  "  with 
the  prey  trapjaed  between  (photograjDh 
by  ^Michael  Soley). 


590 


THE   EYE   IN  EVOLUTION 


the  adjective,  incidentally,  applies  not  to  the  habits  of  the  insect  but  to  its 
characteristic  stance  with  its  front  legs  raised  as  if  in  an  attitude  of  prayer.  The 
female  is  a  particularly  anti-social  creature  who  will  eat  anything  in  sight, 
including  her  mate.  Since  she  can  only  see  moving  objects,  the  male  approaches 
her  with  staccato  movements,  standing  motionless  whenever  she  looks  in  his 
direction,  exactly  in  the  manner  of  the  children's  game.  Grandmother's  Footsteps. 
Fortunately,  the  male  has  better  vision  than  the  female  and  usually  manages 
to  approach  her  in  this  cautious  manner  until  he  can  leap  upon  her  ;  but 
the  end  is  usvially  the  same  because  he  is  generally  eaten  either  while  mating 
is  in  progress  or  after  it  is  finished. 


ACCOMMODATION    IN    INVERTEBRATES 


Cephalopod, 
Loligo 


The  relative  simplicity  of  the  eyes  of  Invertebrates  would  not 
lead  us  to  expect  elaborate  accommodative  facilities  ;  from  the 
functional  point  of  view,  of  course,  the  degree  of  visual  acuity  of  most 
types  would  not  merit  a  complicated  mechanism  of  this  nature.  In 
rare  cases  a  muscular  apparatus  provides  an  active  method  of  accom- 
modation somewhat  analogous  to  that  characteristic  of  Vertebrates. 
An  exceptional  device  is  a  forward  movement  of  the  lens  by  increasing 
the  contents  of  the  globe  by  secretory  activity.  More  often,  however, 
any  accommodation  that  is  present  is  static  in  nature  and  depends 
on  the  provision  of  different  optical  systems  in  the  same  eye  or  in 
different  eyes,  one  being  adapted  for  distant  vision  and  the  other  for 
near. 

An  active  muscular  apparatus  to  produce  an  accommodative  change  of 
focus  is  seen  in  its  most  elaborate  form  inainly  among  Molluscs  ;  it  acts  pri- 
marily by  compressing  the  globe,  that  is,  altering  the  position  of  the  lens  second- 
arily, a  method  of  accommodation,  incidentally,  adopted  by  snakes.^  Such  an 
accommodative  mechanism  is  seen  in  its  highest  form  in  the  eyes  of  Cephalopoda 
(Figs.  113,  114).  Beer  (1897),  Heine  (1908)  and  Pflugk  (1910)  considered  the  eyes 
of  Cephalo23ods  to  be  normally  myopic  (—  2  to  —  lOD),  but  v.  Hess  (1909)  found 
them  to  be  emmetropic  or  slightly  hypermetropic.  This  author  concluded  that 
a  considerable  degree  of  amplitvide  of  accommodation  is  effected  by  the  for- 
ward displacement — not  the  deformation — of  the  lens,  the  mechanism  being 
the  relatively  simple  one  of  compression  of  the  globe  by  the  contiaction  of  the 
ciliary  muscle,  an  action  which  raises  the  intra-ocular  pressvire  so  that  the 
vitreous  pushes  the  lens  forwards  passively,  thus  producing  a  positive  accom- 
modation of  10  to  14  dioptres  (v.  Hess,  1909;  Alexandrowicz,  1927) ;  this  effect 
can  be  abolished  by  atropine  (v.  Hess,  1909-12)  and  augmented  by  electrical 
stimulation  of  the  cerebral  ganglion  (Magnus,  1902). 

A  somewhat  similar  method  is  seen  in  the  Heteropod,  Pterotrachea  (v.  Hess 
and  Gerwerzhagen,  1914).  The  accommodation  of  the  pulmonate,  Onchidium, 
is  closely  allied  :  a  muscular  collar  surrounds  the  distal  part  of  the  eye  which, 
on  contraction,  alters  the  shape  of  the  globe  in  an  analogous  manner.  In  the 
cockle,  Cardium,  the  whole  globe  is  invested  with  muscvilar  fibres  the  contraction 
rif  which  may  serve  as  a  similar  and  very  primitive  accommodative  device. 


648. 


ACCOMMODATION  IN  INVERTEBRATES 


591 


A  different  type  of  muscular  mechanism  appears  to  occur  in  the  Copepod, 
Copilia  (Fig.  139)  ;  the  long  slender  muscle  running  along  the  side  of  the  elongated 
eye  may  not  only  move  this  organ  in  different  directions  but  also  act  by  altering 
the  distance  between  the  lens  and  the  receptor  elements  and  thus  provide  an 
accommodative  adjustment.  This  is  reminiscent  of  the  way  in  which  Cyclo- 
stomes  accommodate.^ 

A  unique  method  appears  to  be  present  in  the  elaborate  eyes  of  certain 
Polychietes  such  as  Alciopa  (Fig.  112).  It  is  said  that  stimulation  of  the  secretory 
cell  increases  the  volume  of  the  "  distal  vitreous  "  lying  immediately  behind 
the  lens,  and  it  has  been  suggested  that  this  pushes  the  lens  forwards  to  accommo- 
date the  eye  for  near  vision.  In  this  eye  there  is  in  addition  an  accommodative 
muscle  similar  to  that  in  Cephalopods  the  contraction  of  which  should  also  be 
effective  (Demoll,  1909  ;    v.  Hess,  1914). 

These  active  mechanisms,  however,  are  exceptional.  More  usually,  accom- 
modation is  achieved  by  the  static  device  of  the  presence  of  two  optical  systems 
in  different  parts  of  the  eye.  The  simplest  example  of  this  is  seen  in  the  ocelli 
insects.  In  the  grasshopper,  for  example,  there  is  a  double  curvature  on 
the  proximal  surface  of  the  corneal  lens  which  thus  acts  after  the  manner 
of  a  bifocal  spectacle  lens  and  seems  to  be  capable  of  producing  two  images  at 
different  distances  (TumjDel,  1914). 

By  its  nature  the  optical  arrangements  of  the  compound  eye  do  not  admit 
accommodative  adjustment,  but  this  is  rendered  unimportant  in  the  mosaic 
type  of  vision.  It  would  seem,  however,  that  the  different  optical  configurations 
seen  in  different  segments  of  certain  compound  eyes  which  are  so  arranged  that 
in  one  region  there  are  short  ommatidia  and  powerful  lenses  and  in  another 
region  long  ommatidia  and  weak  lenses,  may  provide  alternative  focusing 
mechanisms.  This  is  seen  in  its  most  dramatic  degree  in  composite  compound 
eyes  such  as  those  of  some  Ephemeroptera  and  Diptera  (Dietrich,  1919)  and  some 
Hemiptera  (Weber,  1934)  (Fig.  140),  and  of  certain  pelagic  Schizopods  wherein 
one  part  is  adapted  for  near  and  the  other  for  distant  vision  (Fig.  141)  (Hesse, 
1908). 

Finally,  two  separate  eyes  may  exist,  one  optically  adapted  for  distant 
objects  and  the  other  for  near.  This  is  exemplified  in  the  median  and  lateral 
ocelli  of  spiders, 2  while  the  same  expedient  is  also  adopted  in  the  dorsal  and 
ventral  compound  eyes  of  the  whirligig  beetle,  the  former  being  adapted  for 
aerial  and  the  latter  for  aquatic  vision  (Fig.  231;. 


Cardium 


Copilia 


Grasshopper 


Wliirligig  beetle 


Adrian.    J.  Physiol.,  91,  66  (1937). 
Agar.    J.  comp.  Psychol.,  7,  39  (1927). 
Alexaiidrowicz.     Arch.  Zool.  exp.  gen.,  66, 

76  (1927). 
Andrews.    J.  Morphol.,5,  271  (IS'tl). 
Arey  and  Crozier.      Proc.  nal.  Acad.  Sci. 

(Wash.),  4,  319  (1918). 
Autrum.       Naturtvissenschaften,     35,     361 
(1948)  ;    39,  290  (1952). 
E.vperientia,  7,  271  (1949). 
Z.  vergl.  Physiol.,  32,  176,  (1950). 
Verhdl.  dtsch.  zool.  Ges.,  133  (1951). 
Klin.  \V.schr.,  31,  241  (1953). 
Umschau,  54,  4  (1954). 


Autrum  and  Gallwitz.     Z.  vergl.  Physiol., 

33,  407  (1951). 
Autrum  and  Stocker.     Z.  N(iturfor.sch..  5b, 

38  (1950). 
Biol.  Zbl.,  79,  129  (1952). 
Autrum  and  Stumpf.      Z.  vergl.   Physiol., 

35,  71  (1953). 
Batham   and   Pantin.      J.    e.rp.    Biol.,   27, 

290  (1950). 
Baumgartner.      Z.    vergl.    Physiol.,    7,    56 

(1928). 
Beer.     Pfliigers  Arch.  ges.  Physiol.,  67,  541 

(1897). 


1   p.  644. 


-  p.  580. 


592 


THE   EYE   IN   EVOLUTION 


Bertholf.     J.  agric.   Res.,  42,  379  (1930)  ; 

43,  703  (1931). 
Z.  vergl.  Physiol.,  18,  32  (1932). 
Best.     Arch.  Augenheilk.,  68,  221  (1911). 
Bierens  de  Haan.      Z.  vergl.   Physiol.,  4, 

766  (1926). 
Blees.    Arch,  neerl.  Physiol.,  3,  279  (1918). 
Bock.     Z.  vergl.  Physiol.,  29,  595  (1942). 
Bohn.      Bull.  Inst.  gen.   Psychol.,   2,   317 
•    (1902). 

C.  R.  Ass.fr.  Avan.  Sci.,  37,  613  (1908). 
Bolwig.     Entom.   Meddel.    (Kbh.),   20,    80 

(1938). 
Brit.  J.  anim.  Behav.,  2,  81  (1954). 
Bonnett.      Oeuvres    Hist.    nat.    Philos.,    1 

(1779-83). 
Boulet.    C.  R.  Soc.  Biol.  (Paris),  148,  I486 

(1954). 
Boycott.      Piibl.   Staz.    Zool.    Napoli,    25, 

67  (1954). 
Boycott  and  Young.     Symposia  Soc.  exp. 

Biol.,  4,  432  (19.50). 
Proc.  roy.  Soc.  B,  143,  449  (1955). 
Proc.  zool.  Soc.  Land.,  126,  491  (1956). 
Bozler.     Z.  vergl.  Physiol.,  3,  145  (1925). 
Brandt.    Arch,  de  Psychol.,  27,  45  (1935). 
Braun   and  Faust.     Experientia,   10,   504 

(1954). 
Brunelli.      Atti    rend.    R.    Acad.    Lincaei, 

Roma,  19  (2),  77  (1910). 
Buck.     Physiol.  Zool.,  10,  45,  412  (1937). 
von  Buddenbrock.     Z.  vergl.  Physiol.,  13, 

164  (1930). 
Naturwissenschaften,  23,  98,  154  (1935). 
Biol.  Rev.,  10,  283  (1935). 
Grundriss     d.     vergl.     Physiol.,     Berlin 

(1937). 
Vergl.     Physiol.,    1,     Sinnesphysiologie, 

Basel  (1952). 
von      Buddenbrock     and     Moller-Racke. 

Experientia,  8,  62,  392  (1952). 
von      Buddenbrock,      Moller-Racke     and 

Schaller.    Experientia,  10,  333  (1954). 
Burkhardt.      Z.    vergl.    Physiol.,    36,    595 

(1954). 
Burtt  and  Catton.     J.  Physiol,  125,  566 

(1954)  ;    133,  68  (1956). 
Carter.    Nature  (Lond.),  162,  600  (1948). 
Carthy.     Nature  (Lond.),  166,  154  (1950). 
ten  Gate  and  ten  Cate-Kazejewa.     Arch. 

neerl.  Physiol.,  23,  541  (1938). 
ten  Cate-Kazejewa.    Arch,  neerl.  Physiol., 

19,  502  (1934). 
Chapman.     Brit.  J.  anim.  Behav.,  2,  146 

(1954). 
Chen  and  Young.    Sinensia,  14,  55  (1943). 
Collins    and    Hopkinson.        Trans,    ilium. 

Eng.Soc,  19,  135  (19.54). 
Copeland.      J.    co>7ip.    Psychol.,    10,    339 

(1930). 
Copeland  and  Brown.     Biol.  Bull,  67,  356 

(1934). 
Cornvell.    J.  exp.  Biol,  32,  217  (1955). 
CresciteUi     and     Jahn.       J.     cell     comp. 

Phylol,  19,  47  (1942). 


Crozier,  Wolf  and  Zerrahn-Wolf.     J.  gen. 

Physiol,  20,  363  (1937). 
Darwin.        The     Formation     of     Vegetable 

Moulds    by    the    Action    of    Worms, 

London  (1881). 
Daumer.    Z.  vergl.  Physiol,  38,  413  (1956). 
Davis.     Nature   (Lond.),  31,   200  (1885)  ; 

51,  511  (1895). 
Dembowski.     Acta  biol  exp.    (Poland),  15, 

5  (1950). 
Demoll.      Zool.   Jb.,   Abt.    Anal,   27,    651 

(1909). 
Dethier.     J.  cell.  comp.  Physiol,  19,  301 

(1942)  ;    22,  115  (1943). 
Survey  of  Biological  Progress,  N.Y.,  3, 

149  (1957). 
Dietrich.     Zool  Anz.,  32,  470  (1907). 

Z.  uiss.  Zool,  92,  465  (1909). 
Dilk.     Z.  vergl.  Physiol,  25,  47  (1937). 
Dodwell.        Nature     (Lond.),     179,     1088 

(1957). 
Drees.     Z.  Tierpsychol,  9,  169  (1952). 
Eckert.     Lotos,  83,  1  (1935). 
Eltringham.        The     Lenses     of     Insects, 

London  (1933). 
Ewald.     Z.  psychol  Physiol,  Abt.  II,  48, 

285  (1914). 
Ewer.      Proc.   zool  Soc.   Lond.,   117,    207 

(1947). 
Exner.       Die    Physiologic    d.    facettierten 

Augen     von     Krebsen     u.     Insekten, 

Leipzig  (1891). 
Fields.     Comp.  Psychol.  Monog.,  9,  No.  2 

(1932). 
Fingerman  and  Brown.    Science,  116,  171 

(1952). 
Physiol.  Zool,  26,  59  (1953). 
Fischel.   Z.  vergl.  Physiol,  15,    50  (1931). 

Biol.  Zbl,  53,  449  (1933). 
Fischer,  H.    J.  de  Conchyl,  46,  314  (1898). 
Fleure  and  Walton.     Zool.  Atiz.,  31,  212 

(1907). 
Foh.      Zool  Jb.,  Abt.   Zool.   Physiol,  52, 

1  (1932). 
Forel.     Rev.  Sci.  (Paris),  38,  660  (1886). 
Friederichs.     Z.  Morphol  Oekol  Tiere,  21, 

1  (1931). 
von  Frisch.     Zool.  Jb.,  Abt.  Zool  Physiol, 

35,  1  (1914)  ;    40,  1  (1923). 
Biol.  Zbl,  39,  122  (1919). 
Bees  :   their  Vision,  Chemical  Senses  and 

Language,  Ithaca  (1950). 
von  Frisch  and  Kupelwieser.     Biol  Zbl, 

33,  517  (1913). 
Gaffron.    Z.  vergl.  Physiol,  20,  299  (1934). 
Garth  and  Mitchell.    J.  comp.  Psychol,  6, 

103  (1926). 
Gavel.     Z.  vergl  Physiol,  27,  80  (1939). 
Gee.      Univ.   Calif.    Pub.    Zool,    11,    197 

(1913). 
v.  d.  Ghinst.     Bull  Inst.  gen.  Psychol,  6, 

267  (1906). 
Gilhousen.     Univ.  Calif.  Pub.  Physiol,  7, 

73  (1929). 
Gotz.     Z.  vergl  Physiol,  23,  429  (1936). 


THE   VISION   OF   INVERTEBRATES 


593 


Goldsmith.     C.  R.  Acad.  Sci.  (Paris),  164, 

448,  737  (1917). 
Grindley.      The   InteUigence   of  Animals, 

London  (1937). 
Hargitt.    J.  exp.  ZooL,  3,  295  (1906)  ;    7, 

157  (1909). 
Hartline,  Wagner  and  MacNichol.     Cold 
Spr.  Harb.  Symp.  quant.  Biol.,  17,  125 
(1952). 
Haug.     Z.  vergl.  Physiol.,  19,  246  (1938). 
Heberdey.     Biol.  Zbh,  56,  207  (1936). 
Heberdey  and  Kupka.     Z.  vergl.  Physiol., 

29,  541  (1942). 
Hecht.    J.  gen.  Physiol.,  1,  545,  657  (1919). 
Houe  Lab.  Ophthal.  Bull.,  No.  4  (1931). 
Hecht  and  Wald.    J.  gen.  Physiol.,  17,  517 

(1934). 
Hecht  and  Wolf.    J.  gen.  Physiol.,  12,  727 

(1929). 
Heck.    Lotos,  67-8,  169  (1920). 
Heine.    Physiol,  verein.  Kiel,  Mimch.  med. 

Wschr.,  55,  938  (1908). 
Hertz.     Z.  vergl.  Physiol.,  8,  693  ;   11,  107 
(1929)  ;     14,    629    (1931)  ;     19,    463 
^  (1933)  ;   20,  430  (1934)  ;   21,  579,  604 

(1935)  ;    25,  239  (1937). 
Naturuissenschaften.  23,  618  (1935). 
J.  exp.  Biol,  16,  1  (1939). 
von  Hess,  C.     Arch.  Augenheilk.,  64,  Erg., 
125  (1909)  ;    87,  81  (1921). 
Vergl.   Physiol,   d.   Gesichtssinnes,   Jena 

(1912). 
Zool.  Jb.,   Abt.    Zool.    Physiol.,   34,   81 

(1913). 
Pfliigers  Arch.   ges.    Physiol.,   122,    449 

(1918). 
Ergebn.  d.  Physiol,  20,  1  (1922). 
von  Hess,  C,  and  Gerwerzhagen.     Arch. 

vergl  Ophthal,  4,  300  (1914). 
Hess,  W.  X.    J.  Morphol,  39,  515  (1924). 
Hesse,  R.     Z.  iviss.  Zool,  61,  393  (1896). 
Das    Sehen    der    niederen     Tiere,    Jena 
(1908). 
Hoffmeister.     Die  bis  jetzt  bekannt  Arten 
a.  d.  Familie   d.  Regenicilrmer  (1845). 
Homann.        Z.    vergl.     Physiol,    1,     541 
(1924)  ;   7,  201  (1928)  ;   14,  40  (1931). 
Zool.  Jb.,   Abt.   Anal,   71,    56    (1950)  ; 

72,    345    (1952). 
Biol.  Zbl,  72,  373  (1953). 
Horstmann.     Pfliigers  Arch.  ges.  Physiol. 

234,  406  (1934). 
Hovey.     Physiol  Zool,  2,  322  (1929). 
Hoyle.    J.  exp.  Biol,  32,  397  (1955). 
Hundertmark.      Z.  vergl  Physiol,  24,  42, 
563  (1936-37). 
Biol  Zbl,  57,  228  (1937). 
Anz.  Schddlingskde,  14,  25  (1938). 
Use.    Z.  vergl  Physiol,  8,  658  (1928)  ;    17 
537  (1932). 
Biol.  Zbl,  52,  660  (1932). 
Nature  (Lond.),  140,   544   (1937)  ;    163, 
255  (1949). 
Jahn.    J.N.Y.    entom.  Soc,  54,  1  (1946). 
Jennings.     Univ.  Calif.  Pub.  Zool,  4,  53 
(1907). 

S.O.— VOL.  I. 


Kastner.       Naturwissenschaften,     36,     58 

(1949). 
Knoll.     Z.  vergl  Physiol,  2,  329  (1925). 
Abhandl    zool-bot.    Ges.     Wien,    12,     1 

(1926). 
Koehler.     Z.  vergl.  Physiol,  1,  84  (1924). 
Koller  and  v.  Studnitz.    Z.  vergl.  Physiol, 

20,  388  (1934). 
Klihn,  A.    Z.  vergl  Physiol,  5,  762  (1927); 

32,  573  (1950). 
Nachr.  Ges.  Wiss.  Gottingen,  Pt.  Ill,  10 

(1928-30). 
Kuhn,  A.,  and  Pohl.    Naturwissenschaften, 

9,  738  (1921). 
Lashley.  J.    gen.  Psychol,  18,  123  (1938) 
de  Lepiney.     Bull.  Soc.  Zool.  Fr.,  53,  479 

(1928). 
Lotmar.   Z.  vergl  Physiol,  19,  673  (1933). 
Lubbock,    J.      Ants,    Bees    and     Wasps, 

London  (1885). 
Llidtke.    Z.  vergl.  Physiol,  26,  162  (1938). 

Z.  Naturforsch.,  9b,  159  (1954). 
Lutz.     Ann.  N.    Y.  Acad.  Sci.,   29,    181 

(1924). 
Amer.  Mus.  Novit.,  No.  641  (1933). 
Lutz  and  Grisewood.     Amer.  Mus.  Novit., 

No.  706  (1934). 
MacNichol,  Wagner  and  Hartline.     XIX 

Internal  Physiol.  Cong.,  Abstr.,  p.  582 

(1953). 
Magnus.     Pfliigers  Arch.  ges.  Physiol,  92, 

623  (1902). 
Malek.     Biol.  Gen.,  3,  317  (1927), 
Massera.    Experientia,  8,  271  (1952). 
Medioni.     C.    R.  Soc.    Biol    (Paris),   149, 

2248  (.1956). 
]\Iillot.    Grasse's  Traite  de  Zool,  Paris,  6, 

533,  589  (1949). 
Moricke.     Z.  Tierpsychol,  7,  265  (1950). 
Moller-Racke.        Zool.     Jb.,     Abt.     Zool. 

Physiol,  63,  237  (1952). 
Morgan,  Lloyd.     Introduction  to  Compara- 
tive Psychologt/,  London  (1894). 
Muller,    E.      Z.    vergl    Physiol,    14,    348 

(1931). 
Mundhenke.    Zool  Jb.,  Abt.  Zool.  Physiol, 

66,  33  (1955). 
Parry.    J.  exp.  Biol,  24,  211  (1947). 
Patten.     Mitt.  zool.  Stat.  Neapel,  6,  546, 

568,  605  (1886). 
Pelseneer.      Essai  d'ethologie  zool.   d'apres 

Vetude  des  mollusques,  Bruxelles,  No.  1 

(1935). 
Petrunkevitch.       J.    exp.    Zool,    5,    275 

(1907). 
Zool.  Jb.,  Abt.  Syst.  Biol,  31,  355  (1911). 
Pflugk.     Ber.  dtsch.  ophthal.  Ges.  Heidel, 

36,  54  (1910). 
Pieron.       Bull   Sci.    Fr.    Belg.,    43,    183 

(1909). 
Bull  Inst.  gen.  Psychol,  9  (1909). 
Polimanti.    Arch,  de  Psychol,  Geneve,  10, 

84  (1910). 
Power.     Ann.  Mag.  nat.  Hist.,  20  (Ser.  2), 

336  (1857). 

38 


594 


THE   EYE   IN   EVOLUTION 


Piitter.        Oraefe-Saemisch     Hb.     d.     ges. 

Augenheilk.,  Ill,  1,  x  (1908). 
Raabe.     Z.  vergl.  Physiol,  26,  611  (1939). 
Resch.     Z.  vergl.  Physiol.,  36,  27  (1954). 
Roeder.     J.  cell.  comp.  Physiol.,  14,  299 

(1939)  ;   16,  399  (1940). 
Insect  Physiol.,  N.Y.  (1953). 
Rokohl.    Z.  vergl.  Physiol.,  29,  638  (1942). 
Ruck.     J.   cell.   comp.    Physiol.,   44,    527 

(1954). 
Salzle.    Z.  vergl.  Physiol.,  18,  347  (1932). 
Sander.     Z.  vergl.  Physiol.,  20,  267  (1933). 
Sanders  and  Young.    J.  Neurophysiol.,  3, 

501  (1940). 
Scharmer.     Zool.  Jb.,  Abt.  Zool.  Physiol., 

54,  459  (1935). 
Schlegtendal.     Z.  vergl.  Physiol.,  20,  545 

(1934). 
Schlieper.     Verh.  dtsch.  zool.  Ges.,  31,  188 

(1926). 
Z.  vergl.  Physiol,  6,  453  (1927)  ;   8,  281 

(1928). 
Schneirla.    Comp.  Psychol.  Monog.,  6,  No. 

30  (1929). 
J.  comp.  Psychol,  15,  243  (1933). 
Z.  vergl  Physiol,  19,  439  (1933). 
Schremmer.        Zool.     Jb.,     Abt.     System. 

Oekol,  74,  375  (1941). 
Z.  vergl.  Physiol,  28,  457  (1941). 
Segall.     Z.  vergl  Physiol,  19,  94  (1933). 
Smith  and  Baylor.     A7ner.   Nat.,   87,   49 

(1953). 
Soest.     Z.  vergl  Physiol,  24,  720  (1937). 
Sutherland.    Nature  (Lond.),  179,  U,  1310 

(1957). 
Swartz.    J.  comp.  Psychol,  9,  17  (1929). 
Taliaferro.    J.  exp.  Zool,  31,  59  (1920). 
Thorpe.    Learning  and  Instinct  in  Animals, 

London  (1956). 
Tinbergen.      Z.    vergl    Physiol,    16,    305 

(1932)  ;   21,  699  (1935). 
Arch,  neerl  Zool,  3,  323  (1939). 
Tinbergen  and  v.  d.  Linde.    Biol.  Zbl,  58, 

425  (1938). 
Tinbergen,  Meeuse,  Boerema  and  Varos- 

sieau.     Z.  Tierpsychol,  5,  182  (1942). 
Tiimpel.     Z.  uiss.  Inseckteyibiol,  10,  275 

(1914). 


Turner.    J.  comp.  Neurol.  Psychol,  17,  367 

(1907). 
von  Uexkiill.  Leitfaden  in  das  Studium  der 

experimental  Biologic  der  Wassertiere, 

Wiesbaden  (1905). 
Unteutsch.     Zool.  Jb.,  Abt.  Zool.  Physiol, 

58,  69  (1937-38). 
Ven.    Arch,  neerl  Physiol,  6,  163  (1921). 
Vowles.    Brit.  J.  anim.  Behav.,  3,  1  (1955). 
Wadensten.      Acta    Ophthal    (Kbh.),    34, 

311  (1956). 
Weber.    Zool.  Anz.,  108,  49  (1934). 
Weiss.    J.  Econ.  Ent.,  36,  1  (1943). 
J. N.Y.  Entom.  Soc,  52,  267   (1944)  ;  54, 

17  (1946). 
Weiss,  Soraci  and  McCoy.  J.  N.  Y.  Entom. 

Soc,  49,  1  (1941)  ;    50,  1  (1942)  ;    51, 

117  (1943). 
Wellington.      Nature    (Lond.),    172,    1177 

(1953). 
Wellington,  Sullivan  and  Green.     Canad. 

J.  Zool,  29,  339  (1951). 
Wenrich.    J.  anim.    Behav.,  6,  297  (1916). 
Wherry  and  Sanders.     Trans.  Illin.  Acad. 

Sci.,  34,  237  (1941). 
Wichterman.  The  Biology  of  Paramcecium, 

N.Y.  (1953). 
Wiechert.       Z.    vergl.    Physiol,    25,    455 

(1938). 
Wigglesworth.      The   Principles   of  Insect 

Physiology,  London  (1953). 
Willem.    Arch.  Biol,  Gand,  12,  57  (1892). 
Wolf.     Z.  vergl  Physiol,  20,  151  (1933). 
J.  gen.   Physiol,  16,  407,   773  ;    17,   7 

(1933). 
Naturuissenschaften,  23,  369  (1935). 
Wolf  v.nd  Zerrahn-Wolf.    J.  gen.  Physiol, 

20,  511  (1937). 
Wolsky.   Z.  vergl  Physiol,  12,  783  (1930)  ; 

14,  385  (1931). 
Yerkes,  A.  W.    J.  comp.  Neurol.  Psychol, 

16,  441  (1906). 
Yerkes,  R.  M.     J.  anim.  Behav.,  2,  332 

(1912). 
Young.    J.  exp.  Biol,  133,  709  (1956). 
Yung.     Arch.  Sci.  Phys.  nat.,  Geneve,  35, 

77  (1913). 
Zerrahn.    Z.  vergl.  Physiol,  20,  117  (1933). 


1 


596 


THE   EYE   IN  EVOLUTION 


Fig.  735. — Carl  von  Hkss  (1863-1923). 


CHAPTER  XVIII 
THE  VISION  OF  VERTEBRATES 

Of  the  many  research  workers  who  have  given  thought  to  the  subject  carl 
VON  HESS  (1863-1923)  (Fig.  735),  Professor  of  Ophthalmology  first  at  Marburg 
in  1896,  then  at  Wiirzburg  in  1900,  and  finally  at  Munich  in  1912,  did  more  than 
o-^.y  other  to  put  our  knowledge  of  the  visual  behaviour  of  animals  on  a  firm 
basis.  It  is  true  that  before  the  period  of  his  active  work  much  had  been  done 
on  this  question,  but  no  one  up  to  his  time  had  tackled  this  very  difficult  problem 
with  the  same  patience,  zeal  and  enthusiasm.  It  is  also  trvie  that  some  of  his 
conclusions  are  discredited  today,  particularly  because  of  his  habit  of  making 
sweeping  generalizations  from  experiments  which  time  has  shown  to  be  some- 
times uncritically  founded  ;  but  it  is  equally  true  that  by  the  comprehensiveness 
of  his  work,  the  ingenuity  of  the  procedures  he  introduced  and  the  diligence 
with  which  he  aj^plied  them,  he  did  more  than  any  other  to  excite  interest  in 
the  visual  life  of  animals  and  bring  this  subject  within  the  ambit  of  science.  In 
this  field  his  researches  covered  many  aspects,  particularly  on  the  mechanism 
of  accommodation,  the  activities  of  the  pupil,  the  light  sense  and,  above  all,  the 
colour  sense,  of  a  number  of  species.  Xor  did  his  interest  end  in  comparative 
physiology  ;  in  pathology,  both  clinical  and  experimental,  in  bacteriology  and 
surgerj^  his  contributions  to  ophthalmologj^  were  immense. 

The  Bole  of  Vision  in  Vertebrate  Life 

It  may  be  surprising  to  us  who  are  markedly  visual  creatures  and 
whose  most  intimate  contacts  are  with  Mammals  which  apjDear  to  rely 
largely  on  vision  in  their  ordinary  activities,  that  the  great  majority  of 
Vertebrates  are  much  more  nose-  and  ear-minded  than  eye-minded. 
Yet  such,  indeed,  is  the  case.  Even  the  dog  lives  in  a  colourless  world 
of  monotones  in  which,  it  is  true,  form-vision  and  luminosity  count 
highly,  but  its  life  is  dominated  to  a  very  considerable  extent  by  sounds 
which  we  cannot  hear  and  scents  of  the  acuity  and  diversity  of  which  we 
have  no  conception.  As  we  have  seen  to  be  the  case  with  Invertebrates, ^ 
for  the  mass  of  Vertebrates,  not  only  phj^ogenetically  and  ontogenetic- 
ally  but  also  in  daily  life,  the  chemo-,  the  tacto-  and  the  vibratory- 
recejitors  (the  lateral  line  of  Fishes  and  the  ears  of  land  animals  which 
have  evolved  therefrom)  are  more  dominant  than  the  eyes.  Moreover, 
it  must  always  be  remembered  that  even  those  species  to  which  vision 
is  important,  such  as  predators  that  hunt  their  prey,  may  possess  visual 
powers  very  different  from  our  own;  in  many,  reliance  may  be  placed 
almost  entirely  on  the  appreciation  of  luminosity  and  movement — not, 
as  in  Birds  and  Man,  on  visual  acuity — and  this  may  serve  them  well. 
In  an  attempt  to  reconstruct  the  visual  world  of  animals  it  is  easy  to 
fall  into  anthropomorphic  mistakes  of  this  type.^ 

1  Chaj^.  XVII.  -  For  a  fuller  discussion  see  p.  IDS. 

597 


598  THE   EYE   IN   EVOLUTION 

Among  the  pre-Fishes,  the  cyclostomes  have  Kttle  use  for  vision. 
For  the  greater  part  of  their  hves  most  of  them  are  parasitic  and,  as 
we  shall  see,  many  of  them  have  allowed  their  eyes  to  degenerate.^ 

The  activities  of  fishes  must  be  dominated  largely  by  chemo- 
receptors  and  the  vibratory  receptors  of  the  lateral  line  ;  organs  of 
tactile  sense  and  hearing  of  high  acuity  are  also  available  in  many 
species.  It  is  true  that  the  vast  number  of  pelagic  and  surface  fishes 
can — and  do — avail  themselves  of  vision,  a  fact  borne  out  by  the 
extraordinary  anatomical  development  and  high  functional  attain- 
ments of  the  teleostean  eye,  an  organ  capable  of  appreciating  colour 
and  sometimes  provided  with  a  fovea.  In  most  other  types,  however, 
the  high  refractive  error  and  the  frequent  absence  of  efficient  accom- 
modation entail  a  very  defective  visual  acuity  and  the  eye  is  geared 
essentially  for  the  appreciation  of  light  rather  than  form.  Moreover, 
apart  from  a  narrow  belt  beneath  the  surface,  the  intensity  of  light  in 
the  sea  is  insufficient  for  the  attainment  of  a  refined  degree  of  form 
vision  and  even  in  the  most  favourable  circumstances  the  amount  of 
light  reflected  laterally  from  objects  under  water  is  meagre.  In  any 
aquatic  environment  vision  at  any  great  distance  is  impossible  ;  in 
muddy  or  turbulent  waters  and  in  the  deeps  of  the  seas  light  is  practi- 
cally non-existent  and  in  the  clearest  water  is  completely  absorbed 
below  a  depth  of  500  metres  ^  ;  in  the  abyss  darkness  is  absolute. 
Here,  indeed,  the  only  light  available  is  created  by  the  fish  themselves 
by  their  luminous  organs,"*'  and  these,  presumably,  are  used  as  social 
signals  rather  than  visual  aids.  The  activities  of  vast  numbers  of  fish 
must  therefore  dejjend  of  necessity  largely  or  entirely  on  the  sensations 
of  taste,  smell,  touch,  hearing  and  vibration.  Most  fishes,  in  fact,  live 
happily  and  apparently  fully  without  vision  even  although  they  may 
be  provided  with  excellent  eyes  and  normally  use  them. 

Thus  the  trovit  and  other  Teleosteans  of  mountain  streams  live  and  seem  to 
thrive  as  well  when  the  melting  snows  towards  the  end  of  spring  convert  the  water 
to  an  opaque  turbulence  in  which  human  vision  is  impossible  for  a  distance  of 
more  than  a  centimetre  or  two  ;  again,  in  the  high  lakes  of  the  Alps  they  nourish 
themselves  as  well  during  the  7  or  8  months  when  the  water  is  covered  with 
a  layer  of  ice  and  snow  sufficiently  thick  to  preclude  all  light,  as  they  do  in  the 
months  of  summer.  Among  Selachians  vision  can  mean  little  more  than  the 
perception  of  light  and  movement  ;  even  among  Teleosteans  vision  is  usually 
a  subsidiary  sense  and  food  is  recognized  primarily  by  olfaction.*  A  blinded  fish 
in  an  aquarivim  may  acquire  his  food  and  conduct  himself  in  a  way  indistin- 
gviishable  from  a  normal  fish  (the  dog-fish,  Scyllium  ;  the  ray,  Torpedo — Verrier, 
1938).  Of  all  classes  of  Vertebrates,  indeed.  Fishes  seem  the  least  incapacitated 
by  the  deprivation  of  vision  ;  the  blind  cave-fishes  ^  are  as  alert  and  well  fed 
as  their  sighted  cousins. 

1  p.  734.  2  p.  722.  '  p.  736. 

*  See  p.  660.  «  p.  725. 


THE   VISION   OF   VERTEBRATES  599 

This  is  not,  however,  to  say  that  vision  among  Fishes  is  useless. 
When  it  can  be  utihzed  it  is  of  immense  biological  value  and  occasion- 
ally it  reaches  a  high  standard,  although  never  equal  to  that  found  in 
Birds  or  Primates.  Indeed,  it  would  seem,  as  Herter  (1953)  suggested, 
that  the  visual  capacity  of  many  fishes  is  so  high  that  it  cannot  be 
adequately  utilized  in  their  natural  life — an  example  of  a  wide  general- 
ization that  the  sensitivity  of  a  sensory  mechanism  is  usually  greater 
than  is  justified  by  the  apparent  biological  importance  of  the  stimuli 
concerned,  a  tendency  which  perhaps  allows  the  fullest  efficiency  at  the 
normal  level  of  stimulation. 

When  Vertebrates  left  the  water  to  seek  life  on  land,  the  better 
optical  medium  provided  by  air  allowed  a  higher  standard  of  vision. 
Among  AMPHIBIANS,  all  the  Apoda  and  many  of  the  Urodeles  remained 
in  lightless  surroundings,  living  a  secretive  sluggish  life  at  a  low 
potential,  burrowing  in  the  earth  or  in  mud  or  under  flat  stones  in 
shallow  water  ;  these  have  ill-developed  eyes  and  base  their  activities 
to  a  negligible  degree  upon  ^dsion.  On  the  other  hand,  the  more 
active  Amphibians  rely  largely  on  their  eyes,  and  in  the  Anurans 
vision  is  well  developed  ;  frogs,  indeed,  are  essentially  visual  animals, 
catching  their  food  and  recognizing  their  mate  some  distance  away  by 
vision  (Banta.  1914).  This  tendency  becomes  greater  in  reptiles. 
Even  among  the  turtles,  the  most  primitive  Reptiles  extant,  vision  is 
the  dominant  sense  ;  it  is  less  important  among  the  Crocodilians  but 
eminently  so  among  lizards.  The  visual  activity  and  accuracy  of  the 
chameleon  as  it  catches  insects  with  its  bifid  tongue  is  proverbial  ;  in 
this  otherwise  sluggish  animal  the  eyes,  indeed,  are  the  only  organs  to 
show  obvious  activity.  Yet  most  Reptiles  rely  to  a  large  extent  on 
other  senses.  Thus  snakes  and  lizards  follow  a  trail,  either  of 
prey  or  their  mate,  by  smell,  the  flickering  tips  of  the  tongue  picking 
up  odoriferous  particles  from  the  groimd  and  transferring  them  to  the 
extremely  well-developed  Jacobson's  organ  in  the  roof  of  the  mouth 
where  they  are  smelt  and  tasted.  The  rattlesnake,  Crotalus,  for 
example,  readily  recognizes  and  viciously  attacks  the  king-snake, 
LamprojJeltis,  and  will  do  so  with  equal  efficiency  and  zest  when 
blindfolded  ;  deprived  of  his  tongue,  however,  which  removes  an 
essential  part  of  his  olfactory  mechanism,  he  is  unable  to  recognize  his 
enemy  by  visual  clues  alone  and  remains  passive.  Similarly  nocturnal 
snakes,  which  have  particularly  good  olfactory  powers,  can  locate  and 
strike  their  prey  entirely  without  the  use  of  vision.  Apart  from  the 
visually  alive  arboreal  types,  snakes  are  probably  alerted  not  so  much 
by  vision  as  by  the  conduction  of  ground  vibrations  to  the  inner  ear 
through  the  lower  jaw  with  which  the  single  bone  corresponding  to  the 
aural  ossicles  of  man  connects;  while  the  sensory  facial  pits  of  some 
species  such  as  crotalid  vipers  locate  warm-blooded  prey  by  radiant 


600  THE   EYE   IN   EVOLUTION 

heat  with  astonishing  accuracy  even  when  the  snake  is  bhndfolded 
or  in  total  darkness.^ 

The  general  tendency  to  rely  increasingly  upon  vision,  however, 
becomes  much  more  marked  in  birds  among  which  the  sense  of  vision 
comes  fully  into  its  own  ;  with  the  other  senses  poorly  developed, 
particularly  olfaction,  the  intense  activity  of  bird-life  is  dominated 
almost  entirely  by  visual  impressions  and  their  eyes  can  attain  an 
order  of  excellence  unmatched  in  any  other  species  not  excepting  man. 


Fig.  736.  —  The  Giant  Ant-eater,  MmMEvoriiAGA  TuiDAcirLA 
Note  the  very  small  eyes  and  the  long  exploring  tongue  which  takes 
over  the  visual  functions  in  seeking  otit  ants  in  their  nest  (Zool.  Soc,  London). 

It  is  only  because  the  brain  of  the  bird  is  so  much  inferior  to  that 
of  the  higher  Mammals  that  its  visual  interpretation  may  be  less 
effective. 

MAMMALS  are  in  a  different  case.  The  early  Mammals,  small  and 
generally  timid  creatures  leading  a  restricted  life  of  nocturnal  habits, 
derived  from  an  ancient  reptilian  stock,  had  little  use  for  vision  even 
although  in  them  for  the  first  time  the  structural  basis  for  conjugate 
eye-movements  became  laid.-     In  Monotremes,  nocturnal  habits  in 

1  Tlie  facial  pit  of  crotalid  vipers  (rattlesnake,  moccasin,  etc.)  which  responds  to 
a  difference  in  temperature  as  mmute  as  0-L  C  between  a  small  object  and  its  back- 
ground, shows  its  highest  sensitivity  to  infra-red  wave-lengths  between  2,000  and  3,000 
m/x  ;  moreover,  its  capacity  for  directional  analysis  is  very  accurate  (Lynn,  1931  ; 
Noble  and  Schmidt,  1937  ;'  Bullock  and  Gowles,  1952  ;    Bullock  and  Diecke,  1956). 

"  p.  697. 


THE   VISION   OF   VERTEBRATES  601 

which  vision  plays  a  subsidiary  part  are  on  the  whole  retained.  ]\Iarsu- 
pials  and  Placentals,  however,  have  evolved  into  larger  and  more  active 
types  capable  of  wandering  freely  over  the  wide  spaces  during  the  day 
and  therefore  depending  more  and  more  on  vision  for  their  expanding 
activities.  Among  the  Marsupials  this  evolution  reaches  its  highest 
point  in  the  kangaroos,  and  the  same  sequence  is  seen  in  the  great 
placental  family.  To  the  Insectivores,  the  Chiroptera,i  and  the 
"  Edentates,"  vision  as  a  general  rule  is  a  subsidiary  faculty  ;  ant- 
eaters  and  armadillos,  for  example,  gather  their  prey  with  their  sticky 
tongues,  never  seeing  the  food  they  eat  (Fig.  736).  Even  to  the 
Rodents  (with  the  exception  of  the  squirrel  family),  mostly  small 
creatures  of  nocturnal  habits  living  near  to  the  ground  with  a  limited 
horizon,  the  eyes  are  usually  the  fourth  most  important  sense-organ  in 
day-to-day  activities,  coming  after  the  nose,  the  ears  and  the  tactile 
vibrissae.  It  is  true  that  in  some,  such  as  the  Lagomorpha  (rabbits, 
hares),  vision  is  eminently  useful,  but  the  retina  is  still  simple  in  struc- 
ture and  the  eyes  are  probably  used  largely  for  the  avoidance  of 
relatively  near  objects  ;  deprived  of  them,  however,  the  animal 
becomes  immobile.  In  the  Sciuridse  (squirrels  and  particularly 
marmots),  however,  the  eye  with  its  cone-rich  or  cone-pure  retina, 
becomes  for  the  first  time  a  dominating  organ.  Among  the  Ungulates, 
also,  the  eye  becomes  structurally  elaborate  and  vision  more  important, 
although  the  perception  of  movement  would  ai)pear  to  be  biologically 
more  useful  to  them  than  that  of  form  ;  among  the  Carnivores,  it 
is  equally  so  although  much  reliance  is  placed  on  the  other  senses. 
The  hearing  of  the  dog  is  said  to  be  up  to  16  times  more  acute  than 
that  of  man,  his  ability  to  locate  sound  t^vice  as  accurate,  and  his 
analysis  of  tone  is  good  ;  but  he  can  recognize  his  master  visually 
only  at  the  relatively  short  distance  of  some  500  metres,  while  a 
rabbit  excites  no  attention  if  it  does  not  move  ;  normal  recognition 
is  essentially  by  smell.  The  cat  has  a  less  acute  sense  of  smell,  but 
it  also  does  not  see  a  stationary  man  at  a  distance  of  12  metres,  while 
its  vision  in  the  dark,  although  better  than  that  of  man,  is  not  all- 
dominating,  for  deprived  of  its  tactile  \ibriss8e  it  walks  at  night  with 
great  hesitancy.  The  Cetaceans  are  poorly  equipped  visually  and  in 
the  analysis  of  its  environment  the  whale  j^robably  relies  mainly  on 
the  excellent  development  of  its  tympanic  bullae  for  the  detection  of 
vibratory  stimuli.  Apart  from  the  squirrels  it  is  only  when  the  Primates 
and  particularly  man  are  reached  that  vision  again  dominates  conduct 

1  The  agility  displaj-ed  by  bats  in  avoiding  obstacles  at  night,  such  as  strings 
stretched  across  a  dark  room,  has  given  the  imjDression  of  an  astonishing  acuity  in  night 
vision.  This  feat,  however,  is  due  to  hearing.  Bats  in  flight  emit  a  series  of  super- 
sonic squeaks  (with  vibrations  up  to  50,000  per  sec),  inaudible  to  man,  as  frequently  as 
100  times  a  second  or  more  ;  the  hearing  of  the  echos  from  obstructing  objects  probably 
provides  their  essential  means  of  guidance.  Bats  with  their  muzzles  covered  or  their 
ears  plugged  cannot  avoid  collision. 


602  THE   EYE   IN   EVOLUTION 

as  it  does  in  Birds  ;  and  with  eyes  of  relatively  simple  construction  as 
befits  their  direct  descent  from  primitive  Insectivores,  the  excellence 
of  their  visual  performance  depends  more  on  the  development  of  the 
central  nervous  mechanism  of  coordination  and  apperception  than  upon 
the  end-organ  itself. 

It  is  significant  that  only  among  the  anthropoid  apes  does  there  exist  the 
abiUty  of  actively  exploring  the  potentialities  of  vision  in  an  experimental 
fashion.  The  chimpanzee,  foi*  example,  will  amuse  himself  by  looking  at  the 
world  in  different  ways — by  standing  upside-down,  by  bending  down  and  looking 
through  his  legs,  by  punching  a  hole  in  a  leaf  and  peering  through  it,  or  by  making 
a  pool  of  urine  and  regarding  his  reflection  therein.  Vision  has  become  elevated 
from  the  reflex  level  of  biological  usefulness  to  that  of  sestheticism. 

THE  PERCEPTION  OF  LIGHT 

THE  LIGHT  SENSE,  by  wJiicli  light  is  perceived  as  such  and  gradations 
in  its  intensity  ajjjpreciated,  is  the  most  fundamental  of  the  visual  senses, 
a  direct  development  of  the  crude  phototropic  activity  of  the  lower 
invertebrate  organisms  ;  in  many  Vertebrates  it  is  highly  developed, 
more,  indeed,  than  in  man.  The  attainment  of  a  high  standard  of 
sensitivity  involves  certain  structural  specializations  in  the  eye  which 
in  their  purest  form  are  mutually  exclusive  of  excellence  of  colour 
and  form  vision  ;  the  eyes  of  those  animals,  therefore,  to  which  an 
acute  perception  of  light  is  a  biological  necessity  can  be  differentiated 
from  those  which  find  greater  use  in  keen  visual  acuity.  This 
differentiation  is  of  fundamental  importance  in  the  understanding  of 
the  visual  function  of  Vertebrates. 

From  this  point  of  view,  Vertebrates  can  be  divided  into  three 
main  classes  ;  at  each  of  two  extremes  there  is  a  high  degree  of  ocular 
specialization  and  a  consequent  loss  in  plasticity,  and  between  the 
extremes  a  combination  of  both  faculties  is  attained  by  modifications 
which,  while  lacking  the  efficiency  of  the  specialized  organ  found  at 
either  end  of  the  scale,  ensure  sufficient  plasticity  to  allow  a  considerable 
degree  of  adaptability  to  most  conditions. 

(1)  DIURNAL  ANIMALS,  the  cyes  of  which  are  primarily  adapted 
to  bright  light.  A  high  degree  of  diurnality  is  seen  in  the  passerine 
birds  which  rise  and  go  to  bed  with  the  sun  ;  an  extreme  degree  in 
the  turtle  or  the  marmot,  an  animal  which  never  conies  out  by  night. 
These  are  essentially  visual  animals  in  the  sense  that  their  activities 
are  dominated  by  their  eyes  ;  living  in  an  environment  flooded  with 
light,  the  perception  of  minute  amounts  or  fine  differences  of  illumina- 
tion is  comparatively  unimportant,  and  vision  is  used  for  the  appre- 
ciation of  form  and  perhaps  colour. 

(2)  NOCTURNAL  ANIMALS,  the  eyes  of  which  are  adapted  to  the 
near-darkness  of  night.  In  the  less  extreme  degrees,  a  crepuscular 
anima;    finds  its  optimum  environment  in  the  twilight  of  morning  or 


I 


THE   PERCEPTION   OF   LIGHT  603 

evening.  Such  animals  depend  essentially  on  senses  other  than  vision 
in  their  activities  ;  form  vision  need  only  be  crude  for  merely  a  hazy 
outline  is  visible,  and  colour  vision  would  appear  to  be  useless. 

(3)  ARHYTHMic  ANIMALS,  the  cycs  of  whicli  have  sufficient 
plasticity  to  adapt  themselves  either  to  bright  or  dim  illumination. 

It  can  be  assumed  that  diurnality  was  the  primitive  state  in 
Vertebrates  which  presumably  evolved  initially  in  shallow  waters. 
Nocturnality  has  probably  been  developed  for  two  reasons — to  escape 
from  danger  and  to  obtain  food.  It  is  likely  that  a  lightless  habitat 
was  first  sought  as  a  refuge  from  stronger  and  more  powerful  enemies, 
whether  it  be  the  abyss  of  the  seas,  the  recesses  of  a  cave,  the  shelter 
of  a  stone  or  a  burrow  in  the  earth,  or  merely  the  protection  afforded 
by  the  darkness  of  night.  When  in  the  early  Cenozoic  age  the  littoral 
or  pelagic  seas  became  increasingly  populated  by  larger  and  still  larger 
predators,  in  order  to  survive  more  and  more  of  the  defenceless  type 
of  fishes  sought  refuge  in  the  deej>er  and  darker  depths  where  light 
becomes  gradually  dimmer  and  is  ultimately  extinguished  ;  to  adapt 
itself  to  this  environment  the  eye  became  more  and  more  specialized  to 
pick  up  the  small  amount  of  light  available  and  vision  necessarily 
became  more  crude.  As  always  happens,  however,  the  security  of 
these  refugees  would  not  last,  for  predators  would  follow  in  increasing 
numbers  from  the  highly  populated  pelagic  zone  to  feast  with  less 
competition  on  the  untouched  store  of  food  available  in  the  darker 
waters.  Thus  the  primitive  Cyclostomes  are  diurnal  (except  Geotria)  ; 
the  Selachians,  the  Chondrosteans,  the  Dipnoans  and  the  Coelacanths 
have  all  become  nocturnal  ;  but  the  more  highly  developed  Holosteans 
are  diurnal  and  the  eminently  specialized  Teleosteans  which  have 
succeeded  in  establishing  themselves  as  over-all  masters  of  the  seas  are 
of  various  habits  as  if  to  suit  their  convenience,  and  some  of  them, 
such  as  the  belligerent  pike,  are  highly  diurnal. 

Similarly,  although  the  first  venturers  on  land  must  have  had  a 
safe  and  easy  time  in  their  new  environment  rich  in  vegetable  and 
insect  food  and  relatively  empty  of  powerful  enemies,  the  evolution  of 
more  specialized  types  with  a  more  efficient  armature  and  more  active 
habits  forced  many  of  the  primitive  species  to  seek  lightless  surround- 
ings or  the  cover  of  night  in  order  to  survive  ;  the  penalty  for  failure 
in  this  adaptation  was  usually  extinction.  Apart  from  the  frogs,  all 
Amphibians  which  have  survived  are  therefore  markedly  nocturnal  or 
secretive  in  habit  ;  apart  from  the  turtles,  all  Reptiles  which  have 
survived  are  also  nocturnal  except  the  majority  of  the  recently  developed 
lizards  and  their  off-shoot,  the  still  more  modern  snakes,  many  of 
which,  initially  nocturnal  and  burrowing,  have  acquired  a  new 
diurnality.  Freed  from  the  danger  of  land  animals  in  their  new 
aerial  environment,  most  Birds  can  afford  to  be  diurnal,  although 


604 


THE   EYE   IN  EVOLUTION 


Primitive 
Ampliibian 


Primitive 
Reptile 


in  their  search  for  food  many  have  become  crepuscular  and  a  few, 
particularly  the  owls,  essentially  nocturnal. 

Flightless  birds  are  therefore  in  a  peculiarly  precarious  position  and  many 
of  them  have  been  exterminated  :  the  nioas  in  New  Zealand  on  the  arrival  of 
man  (Fig.  737)  ;  the  dodo  of  Maviritius  on  the  arrival  of  mammals  (Fig.  738)  ; 
while  the  kiwi  of  New  Zealand,  even  althovigh  taking  refuge  in  nocturnality,  is 
now  almost  extinct  (Fig.  739). 

Similarly  in  their  search  for  safety  from  the  larger  Amphibians 
and  Reptiles  which  inhabited  the  earth  at  the  time  of  their  emergence, 
the  early  Mammals  were  nocturnal  or  crepuscular — all  the  Mono- 
tremes,  all  the  smaller  and  more  primitive  Marsupials  and  most  of 
the  primitive  Placentals.    Among  these  last,  only  a  few  have  acquired 


Fig.   737.— The  Moa. 


Fig.   738.— The  Dodo. 


Fig.  739.— The  Kiwi. 


Tupaia 


Castor 


diurnality,  particularly  the  tree-shrews  {Tupaia)  among  the  Insecti- 
vores,  and  the  squirrels  (except  the  flying  squirrels)  among  the  Rodents  ; 
to  these  the  diurnal  habit  was  possible  owing  to  the  relative  safety 
of  their  arboreal  life  and  its  acquirement  was  probably  stimulated  by 
the  necessity  for  constant  agility  in  their  environment.  The  other 
diurnal  Rodents  are  few — the  beaver,  Castor,  the  cavy,  Dolichotis,  and 
the  pika,  Ochotona;  the  coney,  Procavia,  is  of  the  same  habit.  The  small 
Carnivores,  except  the  viverrid,  Cynictis,  and  the  suricate,  Suricata, 
are  also  primarily  nocturnal  or  crepuscular,  but  the  larger  Marsupials 
and  the  Ungulates  and  the  larger  Carnivores  have  become  arhythmic, 
the  first  two  emerging  into  the  daylight  because  of  the  safety  provided 
by  their  agility  and  fieetness,  the  last  because  of  their  ferocity  and  the 
excellence  of  their  weapons  of  offence.  As  did  their  ancestors,  the 
Insectivores,  the  early  Primates  found  safety  in  nocturnality  ; 
practically  all  the  Prosimians  are  nocturnal  except  some  members  of 
the  family  of  lemurs, ^  but  having  acquired  safety  in  their  agility  and 
intelligence,  all  the  Simians  except  the  night-monkey  Nyctipithecus, 
are  diurnal  or  arhythmic. 

^  A  few  species  are  diurnal  such  as  Propithecus,  Inclris,  and  Hapalemur. 


THE   PERCEPTION   OF   LIGHT 


605 


We  have  noted  that  the  ocular  characteristics  of  a  nocturnal  and 
a  dinrnal  eye  are  essentially  incompatible  ;  in  the  arhythmic  eye  a 
compromise  is  reached.  The  nocturnal  eye  is  attuned  to  a  high  develop- 
ment of  the  light-sense  ;    in  the  diurnal  eye  this  gives  place  to  the 


Figs.  7'40  to  749. — Xocturnal,  Diurnal  and  Arhythmic  Types  of  Eye. 
(In  each  case  the  lens  is  unshaded.)    The  eyes  are  not  drawn  to  scale. 

Note  the  huge  size  of  the  lens  and  its  set-back  position  in  fully  nocturnal 
types  (Figs.  740-3),  and  its  small  size  and  anterior  position  in  fully  diurnal 
types  (Figs.  747-9). 


Fig.  744. — A  diurnal 
gecko. 


Fig.   745. — A  Ivnx. 


Fig.   746. — An  owl. 


Fig. 


chanie- 


FiG.  748. — A  chimpanzee. 


Fig.   749. — A  pigeon. 


apparatus  required  for  keen  visual  acuity.  In  order  to  attain  efficiency 
a  7iocturnal  eye  evolves  special  ijecuUarities  both  in  its  optical  system 
and  in  the  organization  of  the  retina. 

I.  The  opticeil  system  demands  a  large  eye  to  gather  as  much  light 
as  possible,  a  widely  dilated  pupil  to  allow  the  maximum  amount  of 
light  to  enter,  and  a  large  sjjherical  lens  set  far  back  from  the  cornea 
to  place  the  optical  centre  near  the  retina  so  that  light  transmitted 


606 


THE   EYE   IN  EVOLUTION 


through  the  dioptric  system  is  concentrated  into  a  small  image  of  the 
maximum  possible  brightness  (Figs.  740  to  743  ;  752  to  754). 

Enlargement  of  the  eye  in  the  interests  of  nocturnal  vision  is  common  but 
is  seen  in  its  most  extreme  degree  in  certain  deep-sea  Fishes  wherein  the  eyes  may 
be  larger  than  the  remainder  of  the  head  ;  this  tendency,  in  combination  with 
the  evolution  of  a  maximal  size  of  the  lens,  leads  to  the  development  of  a  tubular 
eye  when  the  head  is  not  sufficiently  big  to  accommodate  a  spherical  organ  of  the 
necessary  dimensions.^  The  large  lens  occupying  a  high  proportion  of  the  globe 
and  closely  approaching  the  retina  is  well  seen  in  the  eyes  of  the  smaller  bats 
and  Rodents  (Figs.  741).- 


FiGS.  750  AND   751. — The  Eyes  of  Birds. 
To  contrast  the  relatively  small  eyes  of  a  diurnal  bird  and  the  large  eyes 
and  widely  open  pupil  of  a  nocturnal  bird. 


Fig. 


^JO. — The     crowned     hawk     eagle, 
Stephanoaetus. 


Fig.     751. — Sa\igny's    eagle    owl,     Bubo 
ascalaphus. 


A  TAPETUM  LUCiDUM  is  an  accessory  to  the  optical  system  to  aid 
vision  in  dim  illumination  ;  it  is  essentially  a  mirror-arrangement  so 
that  light,  having  traversed  the  sentient  elements  of  the  retina,  is 
reflected  backwards  again  and  its  effective  intensity  is  thus  augmented.  ^ 
Not  only  is  the  amount  of  light  available  for  stimulation  thus  materially 
increased  but  slight  differences  in  luminosity  between  an  object  and 
its  backgroimd  are  proportionately  accentuated  so  that  the  total 
effectivity  of  vision  in  dim  illumination  is  correspondingly  improved. 
It  is  this  reflected  light  seen  by  an  observer  standing  beyond  the 


1  p.  322. 

-  It  is  to  be  remembered  that,  for  entirely  different  reasons  spherical  lenses  are 
also  found  in  aquatic  Vertebrates  (except  Sirenia) — Cyclostomes,  practically  all  Fishes 
(except  amphibious  tj'pes,  as  Periophthalmus) ,  aquatic  amphibians,  marine  turtles  and 
Crocodilians,  and  Cetaceans  and  Pinnipedes.  See  p.  277. 

'  The  effective  intensity  would  theoretically  be  doubled  by  a  perfect  mirror.  A 
tapetum  probably  ensures  an  increase  of  about  half  as  much — 40%  in  the  cat 
(Weale,  1"53). 


THE   PERCEPTION   OF   LIGHT 


607 


Figs.  752  to  755. — The  Eyes  of  Placentals. 

To  contrast  the  large  prominent  eyes  of  nocturnal  Placentals  (Figs.  752-4) 
with  the  relatively  small  eyes  of  an  arhythmic  Placental  (Fig.  755)  (Zool. 
Soc,  London). 


Fig.    752. — The    fruit    bat,     Pleropus. 


Fig.    753. — The    two-toed    sloth, 
Cholcenus. 


■  ■■'*:  ■■"-  ''     -.-. 

f/ 

I- 

i^' 

^'^ 

Fig.     754. — The     potto,     Perodicticus 
potto. 


Fig.    755. — The    langur,    Pithecus 
nemceus. 


608 


THE   EYE    IN   EVOLUTION 


Didelphys 


animal's  near-point  (10  to  20  feet  in  emmetropic  animals  with  little 
accommodation)  which  gives  rise  to  the  striking  "  eye -shine  "  in 
suitable  optical  conditions  so  familiar  in  the  cat  family. ^  The  peculiar 
hue  often  associated  with  a  beautiful  iridescent  effect  is  due  to  inter- 
ference phenomena  depending  on  the  size  and  stratification  of  the 
reflective  elements  of  the  tapetum  and  irregularities  on  its  surface 
(Briicke,  1845  ;  Hess,  1912  ;  Roggenbau,  1928),  an  effect  which  may 
perhaps  be  heightened  by  fluorescence  (Hosoya,  1929).^ 

To  be  effective  in  this  way  the  tapetum  must  lie  behind  the 
receptor  elements.  Two  sites  have  been  utilized,  either  the  pigmentary 
epithelium  of  the  retina  or  the  choroid,  and  in  both  cases  the  pigment 
normally  found  in  the  former  must  be  eliminated  or  reduced  to 
insigniflcant  proportions  to  allow  the  light  to  traverse  it.  Both  the 
utilization  of  diffusely  reflected  light  and  the  elimination  of  pigment, 
of  course,  militate  against  acuity  of  vision  in  bright  illumination  ;  it 
is,  therefore,  interesting  and  significant  that  although  a  tapetum 
frequently  occurs  with  an  area  centralis,  it  is  never  found  in  an  eye 
with  a  true  fovea.  Whereas  in  the  purely  nocturnal  eye  a  static 
tapetum  is  thus  an  effective  visual  aid,  an  occlusible  tapetum  wherein 
the  mirror  can  be  used  in  dim  light  and  obscured  in  bright  light 
is  a  much  more  efficient  and  plastic  mechanism  for  the  arhythmic 
eye.^ 

(i)  RETINAL  TAPETA.  The  pigmentary  epithelium  of  the  retina  is 
converted  into  a  mirror  by  a  packing  of  the  cells  of  this  layer  with 
guanine  (in  Teleosts  and  Crocodilians)  or  some  related  substance  (in 
Mammals).  Guanine  is  a  purine  related  to  uric  acid  and,  either  in  the 
pure  form  or  as  the  calcium  salt,  is  deposited  as  highly  reflecting 
crystals.  We  have  already  studied  its  effect  as  a  silver-coated  mirror 
in  the  scales  of  fishes  in  determining  the  colour  of  their  integument  ; 
deposited  in  the  retinal  epithelium  a  similar  reflection  of  incident  light 
is  attained.  In  a  tapetum  of  the  static  (non-occlusible)  type  the 
epithelial  cells  are  filled  with  reflecting  crystals  and  the  fuscin  is  reduced 
to  a  minimal  amount.  Such  a  tapetum  is  rare,  being  found  among 
some  abyssal  Teleosts  {Evermanella,  etc.),  in  Crocodilians,  and,  among 
Mammals,  in  the  larger  bats  (Megachiroptera)  (Fig.  581)  and  (occupy- 
ing the  entire  upper  half  of  the  fundus)  in  the  Virginian  opossum, 
Didelphys  virginiana.  Some  reflecting  crystals  are  also  seen  in  the 
retinal  pigmentary  epithelium  of  the  dog  which  probably  aid  the 
reflection  of  light  by  the  underlying  choroidal  tapetum. 

(ii)  CHOROIDAL  TAPETA  (of  the  non-occlusiblc  type)  may  be  of 
three  types  : 

^  For  this  reason  the  ancient  Egyptians  worshipped  the  cat.  the  eyes  of  which 
magically  reflected  the  light  of  the  Sun-god  even  at  night. 
^  Cf.,  the  diffractive  coloration  of  the  integument,  p.  89. 
3  p.  612. 


THE   PERCEPTION   OF  LIGHT 


609 


(a)  a  GUANINE  TAPETUM  in  certain  fishes — Chondrosteans,  the 
coelacanth  and  certain  bathypelagic  Teleosts — wherein 
compact  layers  of  cells  are  packed  with  guanine  crystals  ; 

(6)  a  TAPETUM  CELLULOSUM  (Fig.  580),  a  closely  packed  series  of 
layers  of  endothelial  cells  filled  with  doubly  refractive 
(?  lipoid)  rodlets,  found  in  a  relatively  small  area  of  the 
upper  half  of  the  fundus  of  all  Carnivores  except  Cynictis 
and  Suricata,  over  the  entire  posterior  part  of  the  fundus  of 
Pinnipedes,  and  in  the  nocturnal  lemuroids  ; 
and  (c)  a  tapetum  fibrosum  (Fig.  579),  formed  by  a  tendon-hke 
condensation  of  fibrous  tissue.  This  last  has  a  relatively 
widespread  distribution — in  many  pelagic  Teleosts,  in  certain 
Marsupials  (the  dasyure,  Dasyurus,  the  Marsupial  wolf, 
Thylacinus,  the  Tasmanian  devil,  Sarcophihis,  and  the 
flying  phalanger,  Petaurus),  among  the  Rodents  in  two 
species  (the  spotted  cavy,  Cu7iiculus,  and  the  flying  squirrel, 
Pteromys),  in  all  Ungulates  (except  the  Suoidea  and  Tylo- 
poda),  in  the  elephant,  the  Cetaceans,  and  in  the  only  noc- 
turnal Simian,  the  night-monkey,  Nyctipithecus,  in  which 
the  eye-shine  from  the  tapetum  is  unusually  brilliant. 

II.  The  organization  of  the  retina  of  the  nocturnal  eye  depends 
essentially  on  two  features — great  sensitivity  of  the  sentient  elements 
and  a  high  degree  of  summation  within  the  retinal  structure  so  that  a 
large  number  of  receptor  elements  can  combirue  to  stimulate  a  single 
optic  nerve  fibre  (Figs.  756,  757).  It  has  generally  been  accepted  that 
the  rods  were  particularly  sensitive  to  light,  a  property  which  was 
considered  due  to  the  great  sensitivity  of  rhodopsin  or  the  closely 
related  pigments  with  which  they  are  provided.  It  may  be  that  this 
assumption  is  incorrect,  for  the  evidence  now  available  points  to  the 
possibility  that  the  rods  and  cones,  considered  individually,  are  equally 
sensitive  to  light  and  that  the  apparent  superiority  of  the  rods  in  this 
respect  may  be  entirely  due  to  summation  by  which  a  ganglion  cell 
can  be  excited  into  activity  by  a  comparatively  large  number  of 
stimuli  each  of  which  acting  by  itself  would  be  subliminal.  In  the 
present  state  of  our  knowledge  it  would  be  dangerous  to  dogmatize  on 
this  problem  ;   it  has  most  recently  been  discussed  by  Weale  (1958). 

However  that  may  be,  the  rods,  either  by  reason  of  their  own 
properties  or  on  account  of  their  neural  connections,  are  specifically 
adapted  to  a  high  degree  of  sensitivity  and  therefore  subserve  scotopic 
vision,  while  the  cones  are  adapted  to  a  high  degree  of  analytical 
acuity  and  therefore  subserve  photopic  vision  ;  these  structures  are 
therefore  diff"erentiated  sharply  from  the  functional  point  of  view. 
Their  structural  difterentiation,   however,   is  not  always  easy  since 

S.O.— VOL.  I.  39 


Suricata 


Sarcophilus 


610 


THE   EYE   IN  EVOLUTION 


Myliohatis 


Armadillo 


intermediate  types  exist  ^  ;  in  general  it  may  be  said  that  in  most 
vertebrate  types  the  retina  is  duplex,  but  in  nocturnal  species  the 
retina  becomes  rod-rich  or  pure-rod  with  a  corresponding  reduction 
or  elimination  of  cones. 

A  PXJBE-ROD  RETINA  is  Seen  only  in  a  few  entirely  nocturnal  animals  ^ — the 
Selachians  (except  a  few  species,  e.g.,  the  ray,  Myliohatis,  the  dogfishes,  Mustelus 
and  Squatina);  a  few  deep-sea  Teleosteans  ;   among  the  Reptiles,  some  nocturnal 

Figs.   756  and  757. — Retina  of  Diurnal  and  Nocturnal  Animals. 


RECEPTORS 

(mostly  rods) 
summoted 
extensively 


BIPOLAR    CELLS 

finally 

sunnmated 

but  little 

in: 

GANGLION    CELLS* 


BIPOLAR   CELLS 

finally 

summated 

extensively 

in: 

GANGLION  CELLS 


Fig.   756. 


Fig.  757. 


Cseciliaii 


The  diagrams  represent  two  related  species,  one  of  which  is  diurnal  and 
the  other  nocturnal.  The  different  ratios  of  visual-cell  types  call  for  different 
relative  numbers  of  the  various  conductive-cell  types,  leading  to  varying 
degrees  of  summation  in  the  optic  nerve  fibres  and  producing  characteristic 
differences  in  the  i-elative  thickness  of  the  retinal  layers  (Gordon  Walls). 


lizards  (nocturnal  geckos)  and  snakes  (some  nocturnal  colubrids  as  Hypsiglena 
and  Phyllorhynchus)  ;  the  Monotreme,  echidna  ;  the  armadillo,  Dasypus  ;  and 
the  bats  (Chiroptera).  It  is  presumed  without  clear  histological  proof  to  occur 
in  a  few  other  types — in  the  Chimseras,  in  Lepidosiren  among  the  lung-fishes,  in 
the  Cascilians  among  Amphibians,  and  in  a  few  Mammals  such  as  the  hedgehog, 
the  shrew,  ?  in  the  chinchilla,  in  the  seals  (Phocidte),  the  whales  (Cetacea),  the 
nocturnal  lemuroids,  Tarsius,  and  the  night-monkey,  Nyctipithecus. 

A  ROD -RICH  retina  with  a  few  cones  occurs  in  certain  Teleosteans  such 
as  the  burbot.  Lota  (810,000  rods  and  3,400  cones  per  sq.  mm.,  Wunder,  1925), 
in  the  ccelacanth,  in  Sphenodo7i,  and  in  some  nocturnal  Rodents  {Rattus,  Mus, 
Cavia,  etc.,  in  which  the  projaortion  of  rods  to  cones  is  about  100  :  1). 


251. 


603. 


THE   PERCEPTION   OF   LIGHT  611 

So  far  as  the  rods  themselves  are  concerned,  sensitivity  is  further 
increased  by  several  expedients  all  of  which  tend  to  lower  their  threshold 
by  increasing  the  amoinit  of  rhodopsin  available  in  a  given  area.  Close 
packing  of  the  individual  elements  with  this  end  in  view  is  seen  carried 
to  its  greatest  lengths  in  certain  deep-sea  Selachians  {Efmopferus,  etc.) 
and  Chimaeras,  while  the  concentration  of  visual  cells  in  a  pure -rod  or 
rod-rich  area  centralis  probably  serves  a  similar  purpose.^  To  increase 
the  amount  of  available  visual  purple  still  further,  the  outer  segments 
of  the  rods  may  be  lengthened  to  a  remarkable  extent  as  is  again  seen 
in  certain  bathyjDelagic  Teleosts  {Lampanyctus,  Argyropelecus,  Verrier, 
1935;  Contino,  1939);  the  rods  may  be  arranged  in  layers  one  above 
the  other  (3  in  the  peripheral  retina,  6  in  the  fovea  in  Bathylogus) ; 
while  these  elements  may  become  massive  and  thickened  as  occurs  in 
Amphibians  and  some  nocturnal  geckos  (Fig.  433). 

The  degree  of  summation  in  the  retina  is  the  principal  expedient 
employed  to  increase  sensitivity  whereby  large  numbers  of  visual 
cells  converge  upon  a  single  bipolar  cell,  and  several  bipolar  cells 
themselves  converge  upon  a  single  ganglion  cell  and  optic  nerve  fibre 
so  that  a  meagre  stimulus  applied  to  each  of  a  large  number  of  visual 
receptors  can  be  summated  to  produce  one  nerve  impulse.  In  the 
organization  of  the  retina  summation  is  a  characteristic  of  the  rods. 
In  Osterberg"s  (1935)  counting,  there  are  110,000,000  to  125,000,000 
rods  and  6,300,000  to  6,800,000  cones  in  the  human  retina  associated 
with  about  1,000,000  optic  nerve  fibres,  that  is,  an  overall  summation 
of  the  order  of  125  :  1.  In  the  retinae  of  nocturnal  types  it  is  not 
uncommon  for  many  more  receptors  to  be  summated  to  a  single 
ganglion  cell. 

An  additional  summation  may  occur  more  proximally  in  the  visual  pathway  : 
thus  in  the  higher  Primates  there  is  a  one-to-one  relationship  between  the 
terminals  of  the  optic  nerve  fibres  and  the  cells  in  the  geniculate  body,  but  in 
the  cat,  which  has  a  high  degree  of  sensitivity  to  light,  it  would  appear  that  30 
to  40  optic  nerve  terminals  are  related  to  each  geniculate  cell  (Glees,  1941-42). 

The  characteristics  of  a  diurnal  eye  attuned  to  a  high  visual  acuity 
are,  as  we  shall  see,^  almost  precisely  the  opposite  of  those  of  a  nocturnal 
eye  (Fig.  747)  :  a  forward  location  of  the  optic  centre  so  that  a  large 
retinal  image  is  formed  to  allow  the  resolution  of  detail,  an  adequate 
pupillary  stop  to  eliminate  aberrations,  and  a  cone-rich  retina  with  a 
low  summation  to  the  ganglion  cells  so  that  the  retinal  image  can  be 
accurately  analysed. 

In  the  most  exclusively  diurnal  types  the  retina  inay  contain  cones  only  : 
such  a  PURE -CONE  BETiNA  is  found  among  Dipnoi  in  Neoceratodus  ;  among  the 
Polypterini   in  Calamoichthys  ;     in   niost   diurnal   lizards  ;     in   diurnal   colubrid        Calamoichthys 

1  p.  657.  «  p.  637. 


612 


THE   EYE   IN  EVOLUTION 


Dasyurus 


Hyaena 


Basking  shark 


Coney 


snakes  ;  and  in  diurnal  Sciuridse,  particularly  the  marmot.    A  practically  pure- 
cone  retina  is  found  in  Chelonians. 

The  characteristics  of  an  arhythinic  eye  are  necessarily  a  compromise 
between  the  first  two  types,  but  several  expedients  are  available  to 
protect  an  eye  adapted  to  scotopic  vision  from  excessive  light.  A 
purely  diurnal  eye  (such  as  that  of  most  Birds  or  some  lizards  and 
snakes  with  pure-cone  retinae)  is  completely  incapacitated  in  dim 
illumination,  but  an  eye  that  is  essentially  nocturnal  can  be  made  into 
a  useful  organ  in  the  brightest  daylight.  These  expedients  are  both 
optical  and  retinal  in  nature. 

{a)  A  markedly  contractile  pupil  is  the  simplest  and  most 
common  optical  device.  With  this  simple  expedient  alone  a  nocturnal 
animal  may  be  rendered  arhythmic.  From  the  structural  point  of 
view,  the  easiest  plan  is  contraction  to  a  stenopoeic  slit  as  is  commonly 
seen  in  some  selachian  Fishes,  many  Reptiles  {Sphenodon,  Crocodi- 
lians,  many  lizards  and  nocturnal  snakes)  in  some  Marsupials  {Dasyurus, 
Trichosurus),  the  dormouse,  Glis,  the  small  Carnivores  (such  as  the 
cat),  Pinnipedes,  the  hyaenas,  and  most  Prosimians  (Figs.  758-9).  Such 
a  slit-pupil,  if  the  aperture  is  sufficiently  narrow,  will  allow  an 
essentially  nocturnal  animal  to  hunt  effectively  in  bright  daylight  (the 
nocturnal  geckos  or  the  cat)  or  to  bask  in  comfort  in  the  sun  (the  croco- 
dile, a  nocturnal  snake  or  a  basking  shark).  Only  a  few  species  have  a 
sufficiently  powerful  sphincter  to  effect  the  mechanically  more  difficult 
feat  of  contracting  a  round  pupil  to  a  stenopoeic  pin-hole — the  teleostean 
pearl-fish,  Encheliophis  ;  sea-snakes  (Hydrophinae)  ;  the  two-toed 
sloth,  Choloepus  ;  the  African  jumping  hare,  Pedetes  ;  and,  above  all, 
the  Prosimians,  particularly  Tarsius,  the  large  round  pupil  of  which 
contracts  to  a  pin-hole  05  mm.  in  diameter  (Fig.  760).  Other  similar 
expedients  are  less  common  and  include  the  expansible  operculum 
associated  with  the  pupil  of  many  skates  and  rays,  teleostean  flat- 
fishes and  Cetaceans,  the  umbraculum  of  the  coneys  (Hyracoidea), 
or  the  parasol  provided  by  the  corpora  nigra  of  the  Ungulates. ^ 

(6)  An  occLusiBLE  TAPETUM  is  a  second  expedient  adopted  by 
certain  Fishes  to  achieve  some  degree  of  arhythmicity  ;  in  dim  light 
the  reflecting  surface  is  exposed  in  which  case  the  tapetum  acts  as  in 
a  nocturnal  eye,  but  in  bright  light  it  is  covered  with  migrating  pigment 
so  that  in  these  circumstances  the  animal  is  not  dazzled.  Such  a 
structure  is  seen  in  the  elaborate  choroidal  tapetum  of  Selachians  in 
which  the  mirror-like  guanine  plates  can  be  covered  when  necessary 
by  the  migration  of  the  melanin  in  the  choroidal  chromatophores  (Fig. 
300),'^  and  the  retinal  tapetum  of  certain  Teleosts  of  the  minnow 
(Cyprinidae)  and  perch  (Percidae)  families-'^  wherein  the  guanine  crystals 
in  the  inner  halves  and  processes  of  the  cells  of  the  pigmentary 
1  p.  649.  *  p.  283.  »  p.  305. 


THE   PERCEPTION   OF   LIGHT 


613 


Figs.   758  to   760. — The  Contractile  Pupils  of  Placentals. 


Fig.  758. 


Fig.   759. 


Figs.   758  and   759. — The  pupils  of  the  cat  m  dilatation   (Fig.   758)  and  in 
conti'action  showing  the_^extremely  narrow  vertical  slits  (Fig.  759). 


Fig.  760. — The  tarsier,  Tarsius,  to  show  the  jaupils  in  contraction  ;    they  are 
horizontal  slits  but  practically  circular  (johotograph  by  Douglas  Fisher). 


614 


THE   EYE   IN   EVOLUTION 


Xenojyus 


Amjuilla 


epithelium  can  be  swamped  and  obscured  by  the  migration  of  fuscin 
from  the  outer  halves  of  the  cells. 

(c)  Adaptation  both  to  scotopic  and  photopic  vision  is  also  to  a 
considerable  extent  facilitated  both  by  d3mamic  changes  in  the  retina 
and  in  its  static  organization.  Into  the  first  category  come  the 
RETINAL  PHOTO-MECHANICAL  CHANGES,  more  marked  in  the  lower 
Vertebrates  than  in  the  higher.  These  comprise  a  migration  of  the 
fuscin  from  the  bodies  of  the  cells  of  the  pigmentary  epithelium  into 
their  processes  which  dip  inwards  between  the  rods  and  cones  thus 
enveloping  them  in  a  dark  sheath  of  pigment  in  bright  illumination, 
and  its  return  back  to  the  cell-bodies  in  dim  illumination  so  that  the 
visual  elements  are  freely  exposed  to  any  light  there  may  be  available 
(Figs.  761  to  764).  A  corresponding  movement  may  involve  the 
visual  cells  themselves,  the  myoid  element  of  which  is  sometimes 
strongly  contractile.^  The  rods  are  usually  relatively  static  and  in 
the  few  species  wherein  they  migrate  they  elongate  towards  the  pigment 
of  the  epithelial  cells  to  take  refuge  from  bright  light.  The  cones,  on 
the  other  hand,  may  remain  stationary  or  contract  inwards,  away  from 
the  pigmentary  processes. 

The  migration  of  the  pigment  was  first  noted  in  the  frog  by  Czerny  (1867), 
Boll  (1877)  and  Angelucci  (1878), and  was  exhaustively  studied  by  Klihne  (1878), 
Engelmann  (1855),  v.  Hess  (1910),  and  a  host  of  others  (see  Arey,  1916)  ;  in  Rana 
temporaria  the  migration  occurs  even  in  the  excised  eye,  a  reaction  which  demon- 
strates that  a  local  control  exists  (Weale,  1956).  In  other  species  of  Anurans 
(Xenopus)  no  demonstrable  migration  of  pigment  occurs  (Saxen,  1953  ;  Weale, 
1956).  The  movement,  however,  is  relatively  slow,  being  fully  evident  within 
half  a  minute  but  is  not  complete  for  50  minutes,  while  its  return  in  darkness  is 
slower  still  (1  to  2  hours,  Arey,  1916).  Migration  is  inost  evident  in  the  lower 
Vertebrates  ;  it  is  absent  in  Selachians  for  in  the  greater  part  of  their  retina  there 
is  no  jjigment,  but  is  marked  and  extensive  in  many  Teleosteans,  less  extensive 
and  somewhat  slower  in  Anvirans,  still  less  and  slower  in  Urodeles,  slight  and 
slow  in  most  Reptiles  (turtles,  Crocodilians,  and  less  in  lizards),  more  marked 
and  raj^id  in  Birds,  but  has  never  been  adequately  demonstrated  in  Mammals 
although  in  this  class  the  retina  has  been  said  to  cling  more  tenaciously  to  the 
pigment  epithelium  after  ilkimination  (see  v.  Hess,  1912  ;  Detwiler,  1916-23  ; 
Laurens  and  Detwiler,  1921  ;   Holm,  1922  ;   Bayliss  et  al.,  1936). 

The  migration  of  the  rods  and  cones  on  illumination  is  more  rare  and  less 
dramatic,  but  takes  place  more  rapidly  (about  2  minutes)  and  with  less  intensities 
of  illumination  than  the  migration  of  pigment  (Arey,  1919)  ;  these  movements 
are  said  to  be  associated  with  swelling  on  illumination  and  subsequent  shrinkage 
of  the  rod  and  cone  nuclei  (Pviff,  1951-53).  It  is  most  marked  in  Ariiia  and 
teleostean  Fishes  (apart  from  the  flat-fishes),  but  the  eel,  Anguilla,  is  unique  in 
that  only  the  rods  participate  in  the  imovement.  Among  Teleosteans  these 
movements  have  received  a  considerable  amount  of  study. ^  The  rods  retract 
and  the  cones  elongate  to  enter  the  guanine  layer  of  the  retinal  tapetum  in  dark 
adaptation  (the  pike-perch,  Lucioperca — Wunder,  1930  ;    the  guppy,  Lebistes — 

^   Such  movements  may  occur  in  Invertebrates,  cf.,  Notonecta,  p.  170. 
^  For  the  diurnal  variation  in  the  migration  of  visual  cells,  see  p.  19. 


THE   PERCEPTION   OF   LIGHT 


615 


Figs.   761  to   764. — Photo-mechanical  Movements  (Katharine  Tansley). 


^  ^  Vr  ■  •  '  •■ 


Fig.   761. 


Fig.   76: 


FiCJS.      761      AND      762. — Pigmentary     migration     in     a     fish      (the     bleak 

Alburnus  lucidus). 

Fig.  761. — The  changes  in  light  adaptation.  Tlie  rods  have  moved 
outwards  and  the  cones  inwards  ;  while  the  pigment  has  moved  inwards  to 
shield  the  rods  and  envelop  the  outer  limbs  of  the  cones. 

Fig.  762. — The  changes  in  dark  adaptation.  The  cones  have  moved  out- 
wards and  the  rods  inwards  ;  while  the  pigment  has  migrated  outwards  to 
expose  the  rods. 


t^uw 


^ 

1 , 

1 

f 

-t 

%  ■ 

-*^^^ 

ilikJliiybiii^^ 

Fii 


7t3o. 


Fig.   764. 


Figs.    763  and  764. — Pigmentary   migi'ation  in  the  frog,    Fana  temjioraria. 

Fic;.  763. — The  retina  in  light  adaptation.  The  pigment  has  migrated 
inwards  to  shield  the  rods. 

Fig.  764. — The  retina  in  dark  adaptation.  The  pigment  has  moved 
outwards  to  expose  the  rods. 


616 


THE   EYE   IN   EVOLUTION 


Fundulus 


H.  Miiller,  1954  ;  and  others)  ;  the  excursions  are  often  considerable,  the  rods, 
for  example,  of  the  killifish,  Fundulus,  and  the  catfish,  Ameiurus,  changing  from 
a  length  of  90-lOOji.  in  light  adaptation  to  30-35ij.  in  the  dark-adapted  eye 
(Detwiler,  1943).  Among  Amphibians,  the  Anurans  show  a  more  marked  degree 
of  migration  than  Urodeles  and  in  each  case  the  cones  move  more  rapidly  and 
extensively  than  the  rods.  In  Reptiles  the  phenomenon  is  very  slight  and  slow, 
if  it  occurs  at  all  ;  in  Birds  cone  migration  is  sometimes  rapid  and  extensive  ; 
and  in  Mammals  no  movements  of  this  type  have  been  reported  except  by  Garten 
(1908)  in  monkeys  (Angelucci,  1892  ;  Garten,  1908  ;  Hess,  1912  ;  Detwiler, 
1916  ;  Laurens  and  Williams,  1917  ;  Kohlrausch,  1918  ;  Laurens  and  Detwiler, 
1921  ;    Loevenich,  1948). 

The  pupillary  response  and  these  retinal  photo -mechanical  changes 
are  supplementary  in  time  in  so  far  as  the  former  is  immediate  and 
rapid  in  its  action  while  the  latter  is  slow.  It  is  also  interesting  that 
their  efficiency  shows  a  mutual  relationship.  The  photo-mechanical 
migrations  in  the  retina  are  more  marked  in  the  lower  Vertebrates 
(apart  from  Selachians)  ;  in  Fishes  (apart  from  Selachians)  pupillary 
movements  are  slow  and  restricted  and  the  muscles  respond  auto- 
nomously to  light.  At  the  other  end  of  the  scale  the  nervously  con- 
trolled pupil  of  the  higher  Vertebrates  is  so  active  and  effective  that 
retinal  migrations  have  become  superfluous  and  have  disappeared. 

The  STATIC  ORGANIZATION  OF  THE  RETINA  is  of  importance  in 
arhythmic  animals.  Obviously  such  a  retina  must  be  duplex,  but  to 
attain  sensitivity  the  rod  population  must  be  considerably  higher  than 
that  of  the  cones.  The  most  effective  distribution  is  seen  in  Primates 
wherein  the  cones  are  massed  in  an  area  centralis  suitably  situated  to 
subserve  form  vision  ^  while  the  rods  are  particularly  numerous  in  the 
peripheral  retina  ;  in  such  a  case  the  central  area  is  relatively  blind 
in  dim  illumination,  a  circumstance  of  little  inconvenience,  however, 
since  acuity  is  impossible  in  these  circumstances  in  any  case  and 
light-perception  is  as  easily  served  by  the  peripheral  as  by  the  central 
retina. 


By  the  use  of  one  or  more  of  these  expedients  a  very  high  degree 
of  ABSOLUTE  SENSITIVITY  TO  LIGHT  Can  be  attained.  Theoretically  it 
would  be  expected  that  the  most  sensitive  eyes  in  the  vertebrate 
phylum  are  to  be  found  in  bathj^pelagic  fishes  which  make  use  of  the 
minute  available  traces  of  light  by  means  of  a  large  eye  with  a  huge 
pupil,  a  brilliant  tapetum  and  an  enormous  and  heavily  summated 
rod-population.  Among  Selachians  a  typical  example  of  such  a  com- 
bination is  seen  in  the  deep-sea  luminous  shark,  EtmojJterus  ;  it  is  also 
seen  in  the  Chimaeras  and  bathypelagic  Teleosts.  In  some  species  of 
the  latter  the  state  of  dark  adaptation  has  become  permanent,  the 
retinal  epithelium  losing  its  pigment  and  photo-mechanical  changes 

1  p.  6r)6. 


THE   PERCEPTION   OF   LIGHT  617 

being  eliminated.  The  owl  may  be  taken  as  typical  of  nocturnal  birds  ; 
Hecht  and  Pirenne  (1940)  taking  the  minimal  observable  contraction 
of  the  pupil  to  green  light  as  their  criterion,  reported  an  absolute 
threshold  of  1-5  x  10~"  ml.,  their  owti  threshold  under  the  same 
conditions  being  4-0  x  10"'^  ml.  The  astonishing  visual  performance 
possible  in  owls  in  dim  illumination  was  verified  by  Dice  (1945-47),  who 
found  that  the  barn-owl  can  detect  and  pounce  upon  dead  mice  at  a 
distance  of  6  feet  under  an  illumination  of  7-3  x  10~'  f.c.  It  is  to  be 
remembered  that  clear  starlight  has  a  much  higher  intensity  than  this, 
of  about  8  X  10-5  f.c.i 

Among  arh}i:hmic  animals,  adaptations  to  varying  luminosity 
may  also  reach  a  much  higher  efficiency  than  in  man  :  it  has  long  been 
traditional  that  the  wise  rider  relies  upon  the  horse  to  pick  its  own 
footsteps  during  the  night.  In  this  respect  most  scientific  work  has 
been  devoted  to  the  cat.  In  behavioural  experiments  involving  a  choice 
between  darkness  and  a  minimal  degree  of  light,  remarkably  constant 
results  for  the  absolute  limits  of  retinal  sensitivity  have  been  found 
—Mead  (1942),  1-3  X  lO""  ml.  ;  Bridgeman  and  Smith  (1942),  8-2  x 
10"^  ml.  ;  Gunter  (1951),  9-92  x  10"^  ml.,  the  average  threshold  for 
man  being  higher — of  the  order  of  5-8  X  10""  ml. 

While  the  sensitivity  to  light  in  most  Vertebrates  is  high,  the 
more  highly  evolved  faculty  of  the  discrimination  of  variations  in 
INTENSITY,  is  apparently  less  efficient,  although  in  many  cases  the 
failure  may  be  due  to  lack  of  attention  in  experimental  conditions 
rather  than  lack  of  appreciation.  Little  conclusive  work  has  so  far 
been  done  on  this  problem  and  some  of  it  is  contradictory,  v.  Hess  (1909) 
claimed  that  the  silverside,  Atherina,  responded  to  white  lights  differing 
only  by  1  :  1-23  in  brightness  ;  but  the  carefully  controlled  observations 
of  Bauer  (1909)  on  this  and  other  types  of  Teleosteans,  which  have 
since  been  confirmed,  tend  to  show  that  they  are  relatively  indifferent 
to  wide  variations  of  intensity  of  white  light  (Sgonina.  1933,  on  the 
minnow,  Phoxinus,  and  others).  Thus,  working  with  the  mud-fish, 
Umbra,  and  the  stickleback,  Eucalia,  White  (1919)  found  in  training 
experiments  that  they  had  difficulty  in  making  any  discrimination 
between  pigmentary  greys  and  whites  ;  this  she  corroborated  at  a 
later  date  (writing  under  the  name  of  Hineline,  1927).  Similarly,  Cora 
Reeves  (1919)  substantiated  that  the  dace,  Semofilus,  could  not  dis- 
tinguish differences  in  intensities  greater  than  1  :  4  although  the  sun- 
fish,  Lepomis,  showed  a  better  performance  (1  :  2),  an  observation 
corroborated  by  Hurst  (1953).     ^Moreover,  goldfish  have  been  taught  Goldfish 

to  choose  one  of  three  intensities,  and  to  choose  one  light  on  the  basis 
of  its  relationshii)  with  two  others  \\hen  the  intensities  as  well  as  the 

1  The  factor  to  convert  foot-candles  into  millilamberts  is   X  3-382. 


At  her 


618 


THE   EYE   IN   EVOLUTION 


Polecat 


positions  were  changed  after  each  trial  (Perkins  and  Wheeler,  1930  ; 
Perkins,  1931).  Within  limits,  therefore,  an  appreciation  of  differences 
of  intensity  is  possible  to  Fishes. 

Similarly,  in  training  experiments  Wojtusiak  (1933)  found  that 
turtles  had  great  difficulty  in  distinguishing  shades  of  grey.  According 
to  the  findings  of  Hamilton  and  Coleman  (1933)  training  experiments 
showed  that  a  diurnal  bird  (the  pigeon)  is  more  attentive  to  changes 
in  hue  than  in  brightness  ;  while  in  most  Mammals  the  opposite 
obtains.  Among  these,  in  most  of  the  nocturnal  types  which  have 
been  investigated,  the  discrimination  of  brightness  has  been  found  to 
be  excellent  (Cole  and  Long,  1909,  in  the  raccoon  ;  D.  Miiller,  1930,  in 
the  polecat  ;  Munn,  1932,  in  the  rat)  ;  in  the  guinea-pig,  however, 
Sgonina  (1936)  found  that  the  intensity  of  two  greys  had  to  differ  by 
1/3  before  differentiation  of  them  could  be  made.  Among  diurnal 
types  Salzle  (1936)  found  that  the  discrimination  of  brightness  was 
poor.  In  arhythmic  types,  on  the  other  hand,  it  may  be  very  good 
indeed.  Thus  Orbeli  (1909),  eliciting  conditioned  reflexes  in  salivary 
secretion  in  the  dog,  found  that  this  animal  was  capable  of  differentiat- 
ing perfectly  between  closely  related  shades  of  grey  {e.g.,  between  49 
and  50  of  the  Zimmermann  scale)  which  are  quite  indistinguishable 
to  the  human  eye,  whether  they  were  presented  successively  or 
simultaneously.  Indeed,  so  far  as  the  dog  is  concerned,  Pavlov 
(1911-27)  concluded  that  the  analysis  of  the  intensity  of  illumination 
is  so  highly  developed  that  a  human  experimenter  is  unable  to  determine 
its  limits. 


Angelucci.       Arch.    Anat.     Physiol.,     353 

(1878). 
Untersuch.    z.    Natur.    d.    Mensch.    u. 

Thiere,  14,  237  (1892). 
Arey.      J.    comp.    Neurol.,    26,    121,    213 

(1916)  ;    30,  343  (1919). 
Banta.     Biol.  Bull.,  26.  171  (1914). 
Bauer.     Zbl.  Phy.siol.,  23,  593  (1909). 
Pfliigers    Arch.    ges.     Physiol.,     133,     7 

(1910)  ;    137,  622  (1911). 
Bayliss,  Lythgoe  and  Tansley.     Proc.  roy. 

Soc.  B,  120,  95  (1936). 
Boll.     Arch.  Anat.  Physiol.,  Physiol.  Abt., 

4  (1877). 
Bridgeman    and    Smith.      Ayin.    Physiol., 

136,  463  (1942). 
Briicke.    Arch.  Anat.  Physiol.,  387  (1845). 
Bullock   and   Cowles.     Science,    115,    541 

(1952). 
Bullock  and  Diecke.    J.  Physiol.,  134,  47 

(1956). 
Cole  and  Long.    J.  comp.  Neurol.  Psychol., 

19,  657  (1909). 
Contino.     v.  Graefes  Arch.  Ophthal.,    140, 

390  (1939). 
Czerny.     S.   B.   Akad.    Wiss.,  Wien.,   56, 

409  (1867). 


Detwiler.     J.  exp.   Zool.,  20,   165  (1916)  ; 

37,  89  (1923). 
Vertebrate  Photoreceptors,  N.Y.  (1943). 
Dice.     Amer.  Nat.,  79,  385  (1945). 

Contrib.   Lab.  vert.   Biol.,    Univ.   Mich., 

No.  34,  1  (1947). 
Engelmann.     Pfliigers  Arch.  ges.  Physiol., 

35,  498  (1885). 
Garten.        Graefe-Saetnisch     Hb.    d.    ges. 

Augenheilk.,  II,  3,  Kap.  12,  Anhang, 

250  (1908). 
Glees.    J.  Anat.,  75,  434  (1941)  ;    76,  313 

(1942). 
Gunter.    J.  Physiol,  114,  8  (1951). 
Hamilton  and  Coleman.  J.  comp.  Psychol., 

15,  183  (1933). 
Hecht  and  Pirenne.     J.  gen.  Physiol.,  23, 

709  (1940). 
Herter.        Die     Fischdressuren     u.     ihre 

sinnesphysiologische  Grundlagen, 

Berlin  (1953). 
Hess.      Arch.    Augenheilk.,    64,    Erganz., 

1  (1909). 
Arch,  vergl.  Ophthal.,  1,  413  (1910)  ;    2, 

3  (1912). 
Vergl.    Physiol,  d.   Gesichtssinnes,  Jena 

(1912). 


THE    PERCEPTION   OF   LIGHT 


619 


Hineline.    J.  exp.  ZooL,  47,  85  (1927). 
Holm.     C.   R.  Soc.  Biol.   (Paris),  87,  465 

(1922). 
Hosoya.      Tohoku  J.   exp.   Med.,   12,    119 

('1929). 
Hurst.    J.  com  p.  phi/siol.  Psychol.,  46,  442 

(1953). 
Kohlrausch.  Arch.       Anat.       Physiol., 

Physiol.  Abt.,  195  (1918). 
Kiihne.     Untersuch.  a.  d.  physiol.  Inst.  d. 

Univ.  Heidelberg,  2,  89  (1878). 
Laurens  and  Detwiler.     J.  exp.  ZooL,  32, 

207  (1921). 
Laurens  and  Williams.    J.  exp.  ZooL,  23,  71 

(1917). 
Loevenich.      PJliigers  Arch.   ges.   Physiol., 

249,  539  (1948). 
Lynn.     Amer.  J.  Anat.,  49,  97  (1931). 
Mead.    J.  genet.  Psychol.,  60,  223  (1942). 
Miiller,    D.      Z.    vergl.    Physiol.,    12,    293 

(1930). 
Muller,  H.     Z.  vergl.  Physiol.,  37,  1  (1954). 
Munn.     J.  genet.  Psychol.,  40,  351  (1932). 
Noble  and  Schmidt.     Proc.  Amer.  philos. 

Soc,  77,  263  (1937). 
Orbeli.     Arch,  de  Sci.  Biol.,  14,  31  (1909). 
0sterberg.    Acta  ophthaL,  Supp.  6  (1935). 
Pavlov.    Ergeb.  d.  Physiol.,  11,  345  (1911). 


Pavlov.       Conditioned     Reflexes     (Trans. 

Anrep),  Oxon.  (1927). 
Perkins.    J.  exp.  Psychol.,  14,  508  (1931). 
Perkins    and    Wheeler.      Comp.    Psychol. 

Monog.,  7,  No.  31,  1  (1930). 
Puff.     Anat.  Am.,  97,  124  (1951). 

Morphol.  Jb.,  93,  14  (1953). 
Reeves.     Behaviour  Monogr.,  4  (1919). 
Roggenbau.        v.    Graefes   Arch.    OphthaL, 

119,  694  (1928). 
Salzle.     Z.  Sdugetierk.,  11,  106  (1936). 
Saxen.      An.    Med.    exp.   fenn.,    31,    254 

(1953). 
Acta  anat.    (Basel),  19,  190  (1953). 
Sgonina.     Z.  vergl.  Physiol.,  18,  516  (1933). 

Z.  uiss.  ZooL,  148,  350  (1936). 
Verrier.      Ann.    Sci.    not.    ZooL,    18,    205 

(1935). 
Les  yeux  et  la  vision,  Paris  (1938). 
Walls.     Biol.  Symposia,  7,  203  (1942). 
Weale.    ./.  Physiol.,  119,  30  (1953)  ;    132, 

257  (1956). 
Nature  (Lond.),  181,  154(1958). 
Wliite.    J.  e.rp.  ZooL,  27,  443  (1919). 
Wojtusiak.       Z.    vergl.    Physiol.,    18,    393 

(1933). 
Wunder.     Z.  vergl.  Physiol.,  3,   1   (1925)  ; 

11,  749  (1930). 


THE  PERCEPTION  OF  COLOUR 

We  have  already  seen  that  among  Invertebrates  the  phototactic 
reactions  of  some  Crustaceans  vary  with  the  wave-length  of  the 
stimulating  light  and  that  colour  vision  on  the  perceptual  level  has 
been  demonstrated  in  some  Insects  ;  in  the  vertebrate  j^hylum 
its  undoubted  occurrence  as  a  significant  factor  in  behaviour  has  been 
substantiated  in  only  a  few  classes — ^teleostean  Fishes,  a  few  Reptiles, 
Birds  and  the  higher  Primates.  The  subject,  however,  raises  many 
intriguing  questions.  So  far  as  the  evidence  goes,  the  eyes  of  all 
vertebrates  including  man  are  stimulated  by  approximately  the  same 
range  of  the  spectrum  (760  ni/M-SOO  m/x)  with  the  highest  sensitivity 
at  a  band  with  a  wave-length  varying  between  500  and  550  m/x  ;  it 
is  no  coincidence  that  this  corresponds  roughly  with  the  transmission 
spectrum  of  water.  The  visual  mechanism  of  Vertebrates  was  first 
evolved  in  ^^■ater  and  their  photo-pigments  were  presumably  developed 
as  sensitizers  to  allow  their  possessors  to  leave  the  brightly-lit  surface 
and  penetrate  more  deeply  into  the  darker  depths  of  the  sea  ;  and  it 
would  be  surprising  if  their  descendants  discarded  a  mechanism  which 
their  ancestors  had  found  of  such  value.  It  is  true  that  Hamilton  and 
Coleman  (1933)  demonstrated  in  the  homing  pigeon  a  capacity  of  hue- 
discrimination  slightly  beyond  the  limits  of  human  perception,  a 
faculty  which  may  apply  to  the  stickleback,  Gasterosteus,  in  the  ultra- 
violet region  of  the  spectrum  (Merker,  1934-39)  ;    but  in  general,  so 


620  THE   EYE   IN  EVOLUTION 

far  as  is  known,  the  spectral  limits  of  the  vision  of  all  Vertebrates  are 
approximately  the  same,  and  include  nothing  corresponding  to  the 
visibility  of  the  ultra-violet  to  insects.^ 

Within  this  spectral  range  the  human  eye  can  differentiate  many 
hues,  qualities  independent  of  the  luminosity  ;  and  to  man,  colour 
sensations  are  highly  overlaid  with  aesthetic  values.  These,  however, 
must  take  a  subsidiary  place  in  vertebrate  evolution  ;  in  the  animal 
hue-discrimination  is  never  developed  to  a  corresponding  extent  and 
although  in  certain  species  it  may  have  a  secondary  biological  veJue 
in  sexual  displays  or  as  a  means  of  concealment  and  advertisement,  it 
would  appear  to  be  essentially  a  mechanism  designed  to  increase  the 
visual  acuity  by  acting  as  an  adjuvant  to  the  discrimination  of  bright- 
ness. Evolved  out  of  the  light-sense  with  a  view  to  obtaining  a  more 
critical  analysis  than  could  be  provided  by  the  appreciation  of  differ- 
ences in  luminosity  alone,  there  is  no  legitimate  reason  to  assume  that 
different  bands  of  the  spectrum  excite  in  animals  the  perceptual 
experiences  recognized  as  colour  by  us.  Moreover,  as  would  be  expected 
from  its  biological  purpose,  hue-discrimination  is  found  largely  in 
intensely  visual  Vertebrates  with  highly  diurnal  activities  and  pro- 
vided with  a  cone-rich  retina,  a  fovea  and  an  effective  accommodative 
apparatus  ;  a  colour  sense,  in  fact,  is  associated  with  good  visual 
acuity,  and  that  we  shall  see  presently  ^  is  rare  among  Vertebrates. 
When  vision  is  vague  and  limited  largely  to  an  appreciation  of  luminosity 
and  movement,  the  refined  discrimination  provided  by  colour  vision 
is  likely  to  be  of  little  importance  ;  and  to  the  nocturnal  animal  such 
a  faculty  would  seem  to  be  meaningless. 

The  investigation  of  colour  vision  in  animals  has  excited  much 
attention  since  the  early  work  of  Graber  (1884-85)  on  fish.  Even  in 
human  experiments  this  is  a  notoriously  difficult  subject,  but  in  animals 
the  difficulties  increase  manyfold  ;  unless  the  stimulus  is  presented 
with  the  utmost  care  it  is  difficult  to  exclude  variants  other  than  hue- 
discrimination,  such  as  changes  in  luminosity,  in  any  choice  the  animal 
may  make.  Moreover,  the  tractability,  responsiveness  and  intelligence 
required  to  produce  a  consistent  response  are  frequently  lacking  so  that 
in  many  cases  a  lack  of  a  colour  sense  may  be  presumed  when  conduct 
may  have  been  determined  by  irritability,  untrainability  or  brainlessness. 
If,  for  example,  a  colour  sense  is  not  highly  developed  and  does  not 
play  a  prominent  part  in  the  everyday  behaviour  of  the  animal, 
experimental  testing  will  probably  involve  difficult  discriminations 
comparable  to  a  complicated  intelligence  test  in  man  in  which  the 
subject,  unable  to  grasp  completely  the  point  at  issue,  has  to  rely  on 

1  Owls  have  been  credited  with  vision  in  the  infra-red,  but  this  is  not  the  case 
— see  p.  630. 
*  p.  637. 


THE   PERCEPTION   OF   COLOUR  621 

guesses  which  may  often  be  misleading  and  are  rarely  consistent. ^ 
Because  this  limitation  has  not  been  realized,  much  of  the  work  on 
this  subject  has  been  scientifically  worthless  and  in  the  literature  many 
contradictions  are  to  be  found. 

The  methods  employed  in  the  exploration  of  the  colour  vision  of 
animals  embrace  the  two  classes  we  have  already  discussed  as  being 
available  for  the  analysis  of  other  visual  functions  ^ — objective  and 
subjective. 

THE  OBJECTIVE  METHODS  OF  APPROACH  depend  on  the  observation 
of  a  measurable  physical  phenomenon  presumed  to  be  determined  by 
a  specificity  in  the  retinal  response  to  different  wave-lengths  ;  they 
suffer  from  the  weakness  that  such  a  differential  response  does  not 
necessarily  imply  a  conscious  appreciation  of  hue.  The  luminosity 
curve  for  the  dark-adapted  human  eye,  for  example,  shows  a  differen- 
tial sensitivity  to  different  wave-lengths  and  yet  does  not  imply  a 
sensation  of  colour.  Even  although  more  than  one  retinal  mechanism 
may  be  stimulated  and  a  physical  basis  may  be  shown  to  exist  where- 
upon colour  vision  could  be  based,  vision  on  the  perceptual  level 
may  nevertheless  be  achromatic.  Indeed,  as  Pumphrey  (1949)  sug- 
gested, it  may  well  be  that  most  animals  with  highly  developed  eyes 
have  the  fundamental  mechanism  for  mediating  colour  vision,  but  it 
is  utilized  only  by  the  few  to  which  it  is  a  biologically  useful  attribute. 

Several  such  phenomena  have  been  utilized  : 

(a)  Dermal  colour  changes.  One  of  tlie  earliest  arguments  employed  in 
ascribing  the  faculty  of  colour  vision  to  aninials  was  the  occurrence  of  changes 
in  colour  in  the  integument  or  its  appendages  in  response  to  the  environment,^ 
a  study  which  was  first  applied  on  a  scientific  basis  by  Karl  von  Frisch  (1912) 
to  fishes  ;  it  seems  unlikely  that  Nature  wovild  evolve  a  complicated  method 
of  camouflage  based  on  colour  if  differences  in  hue  were  not  appreciated  by  the 
enemies  it  was  advisable  to  avoid,  while  the  assumption  of  brilliant  colours  as 
a  method  of  sexual  attraction  becomes  meaningless  if  the  potential  mate  is 
unresponsive  to  the  stimulus  so  elaborately  provided.  This  is  true  ;  but  it  is  to 
be  remembered  that  many  of  the  colour  changes  designed  to  mimic  an  environ- 
ment are  reflex  *  and  need  not  enter  into  consciousness,  and  even  if  they  are  it 
is  conceivable  that  in  some  cases  the  changes  appreciated  by  us  as  hue  may  be 
interjDreted  by  soine  animals  in  terms  of  luminosity,  providing  changes  in  contrast 
rather  than  in  quality.  This  approach  is  therefore  suggestive,  particularly  in 
the  case  of  teleostean  Fishes  and  Birds,  but  cannot  be  accepted  as  implying 
rigid  and  incontrovertible  proof  of  the  existence  of  true  colour  vision.  Moreover, 
if  it  is  used  at  all,  the  method  must  be  employed  only  on  adequately  controlled 
experiinental  trials. 

(6)  The  pupillary  reactions.  Observations  of  the  differential  effect  of  wave- 
bands in  the  spectruin  in  the  induction  of  pupillary  contractions  stem  fi'O in  the 
original  observation  of  Sachs  (1892-1900)  that  with  lights  of  ec^ual  energy  this 

1  See  Smith  (1912).  2  p.  568. 

3  p.  82.  *  p.  92. 


622 


THE   EYE   IN   EVOLUTION 


% 
80 


60- 


40 


30 


20 


NORMAI 

TOTAL 

^    COLOUR  BlInD 

\ 


Yellow 


Green 


5lue 


Fig. 


reaction  varies  directly  with  the  kiminosity  of  the  coloured  light  employed, 
Sachs  in  this  way  verified  the  occurrence  of  a  Purkinje  shift  in  the  pupillomotor 
activity  of  the  human  eye,  finding  a  maximal  reaction  in  the  yellow  in  light- 
adaptation,  in  the  blue-green  in  dark-adaptation  ^  ;  in  totally  colour-blind  sub- 
jects (rod-monochromats)  the  reaction  typical  of  dark-adaptation  is  obtained 
(Fig.  765).  This  technique  was  first  applied  by  Abelsdorff  (1907)  to  Birds  and 
later  and  on  a  much  larger  scale  to  Fishes  and  a  host  of  other  animals  by  v,  Hess 
(1907-22)  and  others.     In  some  cases  the  method  probably  gives  an  assessment 

of  the  spectral  range  and  relative  lumin- 
osity of  the  wave-lengths  which  stimulate 
the  retina,  but  its  interpretation  in  terms 
of  colour  vision  is  quite  illegitimate. 
Abelsdorff,  for  example,  showed  that  the 
pvipil  of  the  (diurnal)  pigeon,  or  (arhyth- 
mic)  dog  was  less  responsive  to  green  and 
blue,  and  that  of  the  (nocturnal)  owl  or  cat 
more  responsive  to  the  blue  than  the 
human  pupil,  v.  Hess,  however,  went 
much  further  and  argued  that  if  the 
maximal  pupillary  contraction  were  in  the 
yellow,  the  eye  was  photopic  in  type  and 
colour  vision  was  present,  if  in  the  green 
that  it  was  absent  ;  if  the  process  of 
adaptation  were  accompanied  by  a  de- 
creased sensitivity  for  the  red  end  of  the 
spectrum  and  an  increased  sensitivity  for 
the  blue,  colour  vision  was  presumed  to 
exist.  That  this  conclusion  is  illogical  is 
obvious,  since  it  begs  the  questions  that 
the  luminosity  curves  of  animals  are  the 
same  as  in  man,  that  the  presence  of  a 
duplex  retinal  mechanism  as  indicated  by 
the  Purkinje  shift  may  subserve  photopic  and  scotopic  vision  withovit  the  necessary 
presence  of  colour  vision  (as  occvirs  in  human  cone-monochromats,  Weale,  1953), 
and  that  the  pupillary  response  is  always  identical  with  the  retinal — a  question 
which  becomes  very  problematical,  for  example,  in  fishes  in  which  the  iris  muscu- 
lature reacts  autonomously. 

(c)  Electro-retinographic  responses  have  been  applied  to  the  study  of  colour 
vision  in  animals  since  the  demonstration  by  Himstedt  and  Nagel  (1902)  that 
the  retinal  action-cvirrents  of  the  frog  showed  a  Pui'kinje  shift,  the  peaks  of 
maximum  sensitivity  being  the  same  as  in  the  hviman  retina — 560  m[i  in  the 
light-adapted  and  507  m[x  in  the  dark-adapted  eye.  In  further  elaboration  of 
this  work,  Granit  and  his  co-workers  (1935-47)  found  that  there  were  at  least 
three  systems  in  the  frog's  retina  reacting  selectively  to  light  of  different  wave- 
lengths. Similarly  in  Birds,  Piper  (1905)  found  that  a  maximal  sensitivity  to 
monochromatic  lights  in  diurnal  types  (fowl,  etc.)  was  at  600  m[j..  while  that  of 
nocturnal  birds  (owl)  was  at  535  mpi.  A  similar  Purkinje  shift  has  been  recorded 
in  the  eyes  of  Fishes  (carp,  tench,  etc.)  and  Mammals  (cat)  with  a  duplex  retina, 
but  not  in  those  such  as  the  tortoise  with  a  ( ?)  pure-cone  retina,  nor  in  nocturnal 
types  with  few  cones  such  as  the  rat  and  guinea-pig  (Granit,  1947).  However 
that  may  be,  it  is  clear  that  althovigh  the  presence  of  different  visual  mechanisms 

'  For  the  pupillomotor  Purkinje  phenomenon  see  further — Engelking,  1919-24  ; 
Nakaytuna,  1921-22  ;    Rutgers,  1923  ;    Laurens,  1923. 


765. — The    Pupillomotor 
Reaction. 


The  relative  pupillomotor  values  of 
coloured  light  in  the  normal  (light- 
adapted)  eye  and  in  the  totally 
colour-blind  (after  Engelking). 


THE   PERCEPTION   OF   COLOUR  623 

has  been  proved  to  exist  which  could  be  used  for  the  differentiation  of  hues 
there  is  no  reason  why  the  animal  should  not  have  achromatic  vision.   Moreover 
in  using  electrophysiological  experiments  to  interpret  the  more  complex  visual 
mechanisms  such  as  colour  vision,   which  presumably  depends  on  the  simul 
taneous  recognition  of  unlike  messages  from  different  optic  nerve  fibres,  con 
elusions  cannot  be  based  on  the  discharges  picked  up  from  the  whole  retina  or 
optic  nerve  bv;t  only  froin  the  analysis  of  those  derived  from  individual  elements 
this  was  not  done  by  the  earlier  workers. 

(d)  Reflex  responses.  Conditioned  reflexes  have  been  employed  to  elucidate 
the  problem  of  colour  vision,  first  by  Orbeli  (1909),  in  Pavlov's  laboratory,  who 
studied  the  effect  of  conditioned  coloured  stimuli  on  salivary  secretion  in  dogs  ; 
the  results  were  inconclusive  and  largely  negative.  More  conckisive  evidence 
was  obtained  by  Bull  (1935)  working  on  conditioned  reflexes  established  on  a 
basis  of  wave-discrimination  by  the  blenny,  Blennius  pholis. 

Other  reflex  responses  have  been  vitilized  in  the  study  of  colour  vision, 
such  as  changes  in  the  respiration  rate  that  occur  when  some  fish  are  exposed 
to  lights  of  different  colours  (Reeves,  1919)  or  changes  in  the  reflex  action  of 
posture  when  the  two  eyes  are  unequally  stimulated  (Thibault,  1949).  All  svich 
methods  are  of  considerable  corroboratory  value  but  their  results  can  be 
translated  into  terms  of  sensation  only  with  diffidence. 

(e)  The  optomotor  reaction  has  been  pressed  into  the  service  of  the  exploration 
of  colour  vision.  Therein,  it  will  be  remembered,  the  animal  is  faced  with  a 
revolving  drum  with  vertical  stripes  and  if  these  can  be  differentiated,  com- 
pensatory movements  of  the  eyes  occur.  Schlieper  (1927)  reasoned  that  if  a 
shade  of  grey  were  found  which  elicited  no  movements  when  alternated  with 
stripes  of  a  colour,  the  field  must  appear  hoinogeneous  and  the  animal  must 
therefore  be  colour-blind  to  that  colovir  ;  from  this  negative  response  he  conckided 
that  the  fishes  and  lizards  with  which  he  experimented  only  responded  to  differ- 
ences in  brightness  and  not  in  hue.  Others  have  subsequently  exploited  the 
method,  particularly  Birukow  (1937-50)  with  Amphibians,  but  again,  the  presence 
of  a  reflex  response  on  a  physical  level,  although  suggestive,  does  not  demonstrate 
the  presence  of  colour  appreciation  on  the  physiological  level. 

SUBJECTIVE  METHODS  OF  BEHAVIOURAL  DISCRIMINATION  are  mUch 

more  satisfying  from  the  physiological  jDoint  of  view  than  objective 
responses  since  they  imply  the  presence  of  the  faculty  to  differentiate 
hues  as  sensations.  Unfortunately  much  of  the  earlier  work  on  this 
subject  is  lacking  in  adequate  control,  the  principal  fault  being  the 
failure  to  appreciate  the  importance  of  the  elimination  of  differences 
in  luminosity  from  the  stimulus  or,  alternatively,  the  widespread  tacit 
suggestion  that  the  appreciation  of  luminosity  (or  of  hue)  of  an  animal 
can  be  legitimately  equated  to  human  sensations  or  to  standards  based 
on  equality  of  energy.  The  assumption  that  the  appreciation  of  light 
or  colour  by  any  species  of  animal  resembles  that  of  any  other  species, 
including  man.  rests  on  inseciu'e  evidence. 

The  simplest  experimental  technique  is  that  of  colour-preference — the  simple 
observation  of  whether  the  animal  prefers  to  go  towards  one  colour  before  another. 
This  crvide  method  was  first  employed  by  Graber  (1884-85)  who  found  that 
certain  teleostean  fishes  preferentially  swam  to  a  light  rather  than  darkness, 
and  to  red  rather  than  green  rather  than  blue — the  "  step -wise  phenomenon." 


624 


THE   EYE   IN   EVOLUTION 


Such  a  technique  is,  of  covirse,  full  of  pit-falls  and  would  lead  to  the  con- 
clusion, for  example,  that  the  bull  recognizes  and  dislikes  red — which  has 
been  proved  untrue.  In  more  recent  years  it  has  been  superseded  by  the  training 
techniques.  The  first  to  apply  these  was  Zolotnitzky  (1901)  who  fed  fishes  on 
red  larvae  and  then,  when  they  had  been  trained  to  respond  to  this  stimulus, 
offered  them  pieces  of  wool  of  different  colours  ;  they  continued  to  choose  the 
red,  the  presumption  being  that  they  ajapreciated  it  as  such.  Subsequently 
more  adequately  controlled  techniques  have  been  employed  involving  the  use 
of  T-  or  Y-maze  experiments  such  as  we  have  already  described  ^  ;  their  value 
and  their  limitations  should  again  be  stressed. 

The  COLOUR  VISION  of  cyclostomes  is  entirely  unexplored. 


Syngnathus 


THE    COLOUR   VISION    OF    FISHES 

The  colour  vision  of  Fishes  has  received  much  attention,  but  none 
has  been  given  to  types  other  than  Teleosteans.  It  is  unlikely  that  the 
Selachians  have  colour  vision  with  their  pure-rod  retinae, ^  but  as 
Walls  (1942)  suggested,  it  is  conceivable  that  among  the  Holosteans, 
A^nia,  with  its  duplex  retina,  may  have  been  the  first  vertebrate  type 
to  develop  colour  vision.  However  that  may  be,  no  fish  has  been 
proved  not  to  have  colour  vision,  and  those  Teleosteans  which  have 
been  investigated  certainly  exhibit  this  faculty  in  a  considerable  degree 
of  development. 

We  have  already  noted  that  Graber  (1884—85)  first  showed  that 
the  teleostean  fish  with  which  he  experimented  (both  fresh-water, 
Barbatula  and  Albtiryms,  and  marine,  Spinachia  and  Syngnathus) 
showed  a  preference  for  certain  colours,  swimming  towards  red  in 
preference  to  green  and  green  in  preference  to  blue,  while  Zolotnitzky 
(1901)  confirmed  that  fish  could  be  trained  to  come  to  red.  The 
possibility  of  establishing  a  similar  association  of  red  with  food  despite 
variations  in  brightness  was  established  by  Washburn  and  Bentley 
(1906)  in  the  dace,  Semotilus,  while  Reighard  (1908)  found  that  the 
snapper,  Lutianus,  despite  confusional  variations  in  brightness, 
avoided  red  and  preferred  the  shorter  waves  of  the  spectrum.  This 
suggestion  that  fish  were  able  to  discriminate  hues  excited  a  consider- 
able amount  of  research  and  not  a  little  controversy.^  On  the  one 
hand,  v.  Hess  (1909-22),  applying  the  same  methods  of  colour  preference 
and  the  observation  of  the  degree  of  pupillary  contraction  to  different 
spectral  bands,  found  the  greatest  response  to  the  green  region  of  the 
spectrum  while  red  light  elicited  a  poor  or  negative  reaction  ;  since 
this  was  typical  for  scotopic  vision  or  total  colour-blindness  in  man, 
he  argued  that  fish  were  colour-blind,  an  argument  fortified  by  his 
contention  that,  if  sufficiently  intense  illuminations  were  used,  an  equal 

1  p.  .569. 

^  Except  Myliobatis  and  Mustelus. 

^  For  summary,  see  Warner,  1931. 


THE   PERCEPTION   OF   COLOUR 


625 


response  was  given  to  red  and  blue  alike.  This  reasoning,  as  we  have 
already  seen,  is  quite  invalid.  On  the  other  hand,  Bauer  (1909-11), 
working  with  several  species  {Charax,  Box,  Atherma,  3Iugil,  etc.), 
found  evidence  of  hue-discrimination  ;  light-adapted  fish  were 
found  to  avoid  red,  dark-adapted  specimens  to  prefer  it,  a  suggestion 
of  the  presence  of  a  Purkinje  phenomenon.  Shortly  thereafter  von 
Frisch  (1912-25)  initiated  a  long  series  of  experiments  based  both  on 
the  dermal  responses  to  coloured  backgrounds  and  on  training. 

With  a  view  to  interpreting  the  significance  of  dermal  changes  to 
conform  with  the  background,  which  are  mediated  through  the  eyes,^ 
von  Frisch  (1912)  used  a  species  of  minnow,  Phoxinus,  which  changes 
colour  rapidly  in  resjDonse  to  the  brightness  of  the  background  and 
turns  yellow  slowly  on  a  yellow-red  background.  He  was  able  to  match 
the  luminosity  of  grey  backgrounds  with  yellow  so  that  the  rapid 
change  was  abolished  but  still  found  that  after  an  interval  the  fish 
turned  yellow  on  a  yellow  background  but  never  on  that  of  a  matched 
grey  or  other  colour.  He  therefore  concluded  that  there  was  a  response 
to  colour  different  from  the  response  to  luminosity.  Further  work  on 
other  species  of  this  fish  was  in  some  cases  inconclusive  (Freytag,  1914), 
in  other  cases  corroboratory  (Haempel  and  Kolmer,  1914  ;  Reeves, 
1919  ;  Schnurmann,  1920).  Using  the  teleostean  Crenilabrus,  which 
reacts  to  red,  yellow,  green  and  blue  backgrounds,  v.  Frisch  (1912) 
again  fovmd  that  its  pigment  cells  reacted  to  hue  rather  than  brightness, 
a  conclusion  substantiated  by  the  observations  of  Sumner  (1911)  and 
Mast  (1916)  on  the  teleostean  flat-fishes  which  change  their  pattern  of 
colour  rapidly  and  dramatically  to  suit  the  changing  environment  while 
swimming  over  a  coloured  sea-bottom.^ 

Final  corroboration  of  this  general  conclusion  has  been  obtained 
by  the  study  of  more  objective  responses.  Reeves  (1919),  for  example, 
experimenting  on  fish  (the  mud-fish,  Umbra,  and  the  shiner,  Notrojns), 
found  that  the  respiration  rate  increased  considerably  when  the 
illumination  was  increased  but  was  more  than  doubled  when  white 
light  was  changed  to  red  even  although  its  intensity  was  simultaneously 
diminished — strong  presumptive  evidence  that  red  was  appreciated 
differently  from  white.  Bull  (1935),  employing  electric  shocks  to 
establish  conditioned  reflexes  on  the  basis  of  hue -discrimination  in 
the  blenny,  Blennius  pholis,  came  to  the  same  conclusion  ;  while 
Thibault  (1949),  basing  his  observations  on  the  fact  that  light  exerts  a 
tonic  influence  initiating  a  change  in  posture  when  the  two  eyes  are 
unequally  stimulated,  brought  forward  striking  evidence  that  the 
peripheral  mechanism  in  the  retina  of  the  carp,  Cyprinus,  contained 
receptors  which  were  individually  sensitive  to  red,  green  and  blue- 
violet. 


Phoxinus 


Blennius 


1  p.  82. 


p.  92. 


S.O.— VOL.  I. 


626  THE   EYE   IN   EVOLUTION 

von  Frisch  (1912-25)  also  conducted  an  elaborate  series  of  training 
experiments  on  Phoxinus  presenting  food  in  grey  and  coloured  tubes 
or  in  association  with  grey  or  coloured  papers.  He  found  that  his  fish 
readily  learned  always  to  seek  the  colour  to  which  they  had  been 
trained  in  preference  to  any  shade  of  grey,  even  if  the  food  were 
omitted  so  that  gustatory  or  olfactory  clues  were  eliminated  ;  red  and 
yellow  tended  to  be  confused,  but  blue  and  green  were  not,  either 
between  themselves  or  with  red  and  yellow.  This  work  seemed  to 
refute  the  conclusions  of  von  Hess  (1909-22)  based,  as  we  have  seen, 
on  more  doubtful  evidence,  and  was  corroborated  on  several  species  of 
Teleosts  by  Goldsmith  (1914),  White  (later  Hineline)  (1919-27),  Reeves 
(1919)  and  Hurst  (1953)  and  on  Phoxinus  by  Burkamp  (1923), 
Schiemenz  (1924),  Wolff  (1925),  Kiihn  (1925)  and  Hamburger  (1926). 
It  has  been  shown  that  once  a  food-relationship  had  been  adequately 
established  with  a  particular  colour,  this  colour  is  regularly  sought  by 
the  fish  even  when  the  factor  of  luminosity  has  been  experimentally 
eliminated,  while  Miss  Reeves's  experiments  with  a  hue-discrimination 
box  with  adequate  controls  can  only  be  interpreted  on  the  thesis  that 
the  two  species  which  she  employed  ^  appreciate  hues  as  such.  They 
can  be  trained  to  go  for  food  to  a  particular  colour  even  when  its 
position  and  intensity  are  varied  at  random,  and  are  not  confused  by 
any  other  colour  in  any  degree  of  brightness. 

This  mass  of  experimental  material  suggests  that  the  retina  of 
teleostean  fishes  contains  a  mechanism  adequate  to  subserve  colour 
vision  and  the  further  conclusion  would  seem  inescapable  that  these 
fishes  are  possessed  of  a  colour  sense  ;  they  appear  to  be  able  to 
appreciate  qualitative  differences  between  the  wave-bands  appreciated 
by  us  as  red,  yellow,  green,  blue,  violet  and  the  near  ultra-violet  (up 
to  365  m/x  and  j^erhaps  shorter,  Merker,  1934-39).  From  the  fact 
that  the  most  ready  confusion  exists  between  red  and  violet,  it  would 
appear  that  their  sensations  may  form  a  closed  colour-circle.  The 
fact  that  they  react  to  the  human  complementary  mixtures  of  yellow 
and  blue,  red  and  blue-green,  orange  and  blue-violet,  and  so  on,  as 
to  white  light  suggests  that  their  colour-system  is  closely  akin  to  our 
own  (Hamburger,  1926,  in  Phoxinus,  Beniuc,  1933,  in  the  Siamese 
fighting  fish,  Betta  splendens). 

Beniuc's  technique  was  ingenious.  He  trained  the  fighting  fish  to  respond 
positively  to  a  grey  disc  and  negatively  to  a  slowly  revolving  disc  of  two 
compleinentary  colours  in  sectors  yielding  grey  to  the  human  eye  in  rapid 
rotation  ;  when  the  speed  of  revolution  produced  130  sector  impressions  per  sec. 
the  fish  responded  positively  as  if  to  grey.  At  90  imiaressions  per  sec.  the  fish 
reacted  negatively  as  to  separate  impressions — their  fusion-frequency  is  therefore 
much  higher  than  that  of  man. 

^  The  dace,  Semotilus,  and  the  sun-fish,  Lepomis  ;  verified  by  Hurst  (1953)  on 
the  latter. 


Betta 


THE   PERCEPTION   OF   COLOUR 


627 


Although  it  may  be  thus  conchided  that  colour  vision  is  a  definite 
acquisition  of  teleostean  fishes,  it  is  more  difficult  to  say  how  far  it 
determines  their  conduct  in  comparison  with  other  visual  sensations. 
The  work  which  we  have  quoted,  particularly  that  of  Reeves  (1919), 
would  indicate  that  brightness  has  a  greater  attraction  than  colour, 
while  that  of  Horio  (1938),  a  Japanese  investigator  who  combined 
training  to  different  colours  with  different  forms  (triangles,  discs,  etc.), 
suggests  that  colour  is  a  more  clamant  stimulus  than  form.  It  would 
seem,  therefore,  that  as  a  determinant  of  behaviour,  the  colour  sense 
takes  a  place  intermediate  between  the  light  and  the  form  senses. 

That  it  does  influence  conduct  is  obvious  from  certain  observations.  Two 
of  these  may  be  noted.  We  shall  see  that  to  the  male  stickleback,  Gasterosteus, 
the  sight  of  red,  the  colour  of  the  belly  of  its  rival,  serves  as  a  release  of  the 
fighting  resjaonse  no  matter  what  the  object  with  which  the  red  is  associated.^ 
Young  jewel-fish  (Hemichroniis  himaculatus)  are  attracted  to  i-ed,  the  breeding 
colour  of  the  adults,  and  Noble  and  Curtis  (1939)  found  that  adult  females 
recognized  their  mates  as  individuals  by  the  colour-pattern  on  the  head  :  if  the 
head  were  painted  while  the  rest  of  the  body  retained  its  natural  colour,  no 
recognition  was  shown,  but  if  the  entire  body  except  the  head  of  the  male  were 
covered,  recognition  readily  occurred. 


Gasterosteus 


THE    COLOUR    VISION    OF    AMPHIBIANS 

Investigations  into  the  colour  sense  of  Amphibians  have  been 
largely  devoted  to  the  Anurans.  There  is  no  doubt  that  from  the 
anatomical  point  of  view  a  peripheral  mechanism  which  could  sub- 
serve colour  vision  is  present  in  the  retina  of  the  frog.  The  electro- 
retinogram  of  this  animal  shows  that  a  Purkinje  shift  exists  between 
the  light-adapted  and  dark-adapted  eye  (Himstedt  and  Nagel,  1902  ; 
Granit  et  oL,  1937-39),  but  we  have  already  seen  that  this  does  not 
imply  the  existence  of  a  colour  sense.  In  the  functional  behaviour  of 
this  animal  a  phototactic  response  can  be  elicited  to  light  which  varies 
with  the  wave-length  :  in  one  species,  Loeb  (1890)  found  a  negative 
phototactic  response  in  which  red  was  preferred  to  blue  ;  in  two 
other  species,  Torelle  (1903)  obtained  a  j^ositive  response  wherein  blue 
was  preferred  to  red.  It  is  to  be  noted  that  Cole  (1910)  found  that  the 
phototaxis  of  Bana  clamata  varied  A\'ith  the  temperatiu'e.  These 
observations,  however,  lead  to  no  definite  conclusion.  Moreover,  in 
the  hands  of  the  early  workers  training  experiments  invariably  gave 
inconclusive  results,  probably  because  the  learning  ability  of  the 
frog  is  practically  non-existent  (Yerkes,  1903  ;  v.  Hess,  1912-22)  ; 
but  R.  G.  Smith  (1948)  found  that  by  intensive  training  a  response 
could  be  elicited  in  the  frog,  Bana,  suggesting  that  a  discrimination 
might  be  possible  between  red  and  blue  ;    Thomas  (1953-55),  on  the 

^  p.  665. 


Rana 


628 


THE   EYE   IN   EVOLUTION 


Bufo 


other  hand,  obtained  entirely  negative  results  in  training  experiments 
involving  coloured  and  grey  papers  with  the  toad,  Bufo. 

Subjective  training  experiments  being  thus  inconclusive,  we  are 
left  with  evidence  based  on  objective  reflex  responses.  In  this  field 
the  work  of  Birukow  (1937-50)  who  exploited  the  optomotor  reaction, 
is  outstanding.  Using  this  method  he  found  that  young  tadpoles  had 
a  maximum  sensitivity  in  the  yellow  region  of  the  spectrum  at  all 
levels  of  illumination,  while  the  adult  frog,  Rana,  showed  a  Purkinje 
shift  with  a  maximum  sensitivity  in  the  yellow  in  light -adaptation  and 
in  the  green  in  dark-adaptation  ;  he  also  found  that  a  specific  colour 
reaction  could  be  obtained  in  this  animal  to  red  and  blue,  in  the  fire- 
bellied  toad,  Bomhina,  to  yellow  in  addition,  in  the  tree-frog,  Hyla 
arborea,  only  to  blue,  while  the  toads,  Bufo  and  Alytes  obstefricans, 
showed  no  evidence  of  the  possession  of  colour  vision.  Similarly,  six 
species  of  Urodeles  {Salamandra  and  Triturus)  exhibited  evidence  of 
a  differential  response.  Histological  examination  of  all  these  Amphi- 
bians showed  a  duplex  rod-and-cone  retina.  From  his  experiments 
Birukow  concluded  that  in  all  cases  the  peripheral  mechanism  for  colour 
vision  was  equally  present  and  that  the  lack  in  those  species  which 
appeared  to  be  colour-blind  was  in  the  central  mechanism.  When 
colour-deficiency  occurred  it  would  seem  that  yellow  and  yellow-green 
were  the  first  colours  to  be  missing,  leaving  a  neutral  region  in  the  centre 
of  the  spectrum,  then  red  and  blue -green,  and  finally  blue.  Whether 
these  reactions  are  associated  with  sensations  is  another  question,  and 
in  the  meantime  it  would  be  wise  to  conclude  that,  although  the 
required  mechanism  may  be  present,  there  is  little  evidence  that 
sensations  of  colour  enter  prominently  into  the  behaviour  of 
Amphibians. 


THE    COLOUR    VISION    OF   REPTILES 

Our  knowledge  of  the  colour  vision  of  Reptiles  is  meagre,  partly 
because  of  the  paucity  of  research  done  on  the  C][uestion  and  partly 
because  of  the  difficulty  of  using  such  animals  as  subjects  in  behavioural 
experiments.  The  colour  appreciation  of  Sphenodon  has  been 
unexplored  ;  among  the  Crocodilians  it  would  seem  from  the  evidence 
of  pupillary  contraction  that  a  Purkinje  shift  occurs  between  a 
maximum  sensitivity  of  544  m/z  in  light-adaptation  to  514  niju,  in  dark- 
adaptation  (Laurens,  1923)  ;  while  some  snakes  appear  to  be  amenable 
to  colour  training  experiments  (Kahmami,  1931  ;  Grodzinska,  1948,  on 
the  grass-snake,  Troiyido7iotus).  Sufficient  work,  however,  has  not  been 
done  with  these  reptiles  to  allow  us  to  draw  any  pragmatic  conclusions. 

Some  training  experiments  have  yielded  positive  results  with 
Ohelonians  and  Lacertilians.  v.  Hess  (1913)  found  that  turtles  showed 
spontaneous    colour-preferences,    while    Wojtusiak    (1933),    Quaranta 


THE   PERCEPTION   OF   COLOUR 


629 


(1949)  and  Quaranta  and  Evans  (1949)  have  shown  that  tortoises 
[Clemmys,  Testndo)  can  with  perseverance  be  made  responsive  to 
training  techniques  and  therein  show  discrimination  between  blue, 
green  and  orange  ;  as  in  fishes,  red  is  apparently  readily  confused  with 
violet.  So  far  as. lizards  are  concerned,  Schlieper's  (1927)  experiments 
with  Lacerta  vivipara  using  the  optomotor  reaction  gave  negative 
results  ;  a  positive  response  was  elicited  only  by  differences  in  bright- 
ness. MusolfF  (1955)  had  a  similar  experience  with  Angiiis  and  the 
nocturnal  ^.^-ko,  Hemidadylus.  Wagner  (1932),  on  the  other  hand, 
in  training  experiments  using  coloured  papers  associated  as  positive 
stimuli  with  food  or  as  negative  stimuli  with  salt  (which  the  lizard 
violently  dislikes),  obtained  evidence  that  colours  were  differentiated 
from  A\  hite  or  greys  and  that  separate  appreciation  could  be  made  of 
red,  yellow,  green  and  blue  ;  this  finding  was  corroborated  in  Anolis 
for  red,  yellow-green  and  green  but  not  for  yellow  and  blue  by  Musolff 
(1955)  using  the  optomotor  reaction  as  a  criterion.  It  would  appear, 
therefore,  that  those  Reptiles  that  have  been  investigated  show  the 
potentiality  of  colour  vision  and  that  some  lizards  can  base  their 
behaviour  upon  it. 

THE    COLOUR   VISIOX    OF    BIRDS 

That  Birds  possess  a  highly  developed  colour  sense  has  always 
been  accepted  partly  because  the  bright  colours  of  their  plumage 
obviously  adopted  as  an  attraction  in  mating  would  otherwise  be 
biologically  inexplicable,^  and  partly  because  of  the  proven  ability  of 
some  of  them  to  pick  out  preferentially  coloured  flowers  and  fruit  for 
feeding.  Recent  experimental  work  has  demonstrated  beyond  question 
that  this  is  indeed  the  case. 

The  first  scientific  investigations  were  objective  in  nature.  The 
electroretinogram  was  utilized  by  Piper  (1905)  who  showed  that  in 
diurnal  types  such  as  the  hen  the  maximal  response  occurred  to  wave- 
lengths of  600  m^.  in  nocturnal  types  such  as  the  owl,  to  535  m/x  ;  he 
concluded  that  neither  type  itself  showed  an  individual  Purkinje  shift 
but  that  this  phenomenon  could  be  demonstrated  between  the  two 
types.  Shortly  thereafter  AbelsdorfiF  (1907)  and  subsequently  Laurens 
(1923)  and  Erhard  (1924)  made  a  similar  study  on  the  differential 
contraction  of  the  pupil  when  the  eye  was  illuminated  by  various 
spectral  bands  and  it  was  shown  that  a  Purkinje  phenomenon  could  be 
elicited  in  a  diurnal  bird  (the  pigeon)  provided  an  luiusually  long  time 
(45  mins.)  was  allowed  for  dark-adaptation  to  develop.  From  an  analysis 
of  their  data  these  authors  concluded  that  the  mechanism  necessary 
for  hue-discrimination  existed  and  in  general  resembled  that  found  in 
man,  but  the  illegitimacy  of  these  conclusions  we  have  already  stressed. 

1  p.  104. 


Testudo 


Anijiiis 


Honidactylus 


630 


THE   EYE   IN  EVOLUTION 


Sparrow 


The  somewhat  surprising  suggestion  was,  however,  put  forward  by 
Vanderplank  (1934)  that  the  pupil  of  the  tawny  owl,  Strix,  contracted  to  long 
infra-red  rays  (900  mjA)  far  beyond  the  limits  of  human  visibility,  the  idea  being 
that  this  bird  "  saw  "  its  prey  in  the  dark  by  means  of  the  latter's  body-heat. 
This,  however,  has  been  refuted  by  Hecht  and  Pirenne  (1940)  in  another  species 
of  owl,  Asio,  while  Matthews  and  Matthews  (1939)  showed  that  the  ocular  media 
of  Strix  absorbed  completely  all  the  infra-red  radiation  in  this  spectral  area.  It 
may  therefore  be  accepted  that  the  objective  evidence  indicates  that  the  photo- 
chemical system  of  the  eyes  of  Birds  is  similar  to  that  of  man. 

Behavioural  experiments  have  borne  out  the  same  conclusion  in 
a  very  definite  way  although  they  have  been  somewhat  handicapped 
by  the  essential  stupidity  of  birds.  That  colour  vision  does  influence 
their  behaviour  was  shown  by  the  early  experiments  of  Lloyd  Morgan 
(1896)  with  chickens,  Porter  (1904-6)  with  the  sparrow  and  Rouse 
(1906)  with  the  pigeon  ;  these  birds  all  show  a  preference  for  certain 
colours  and  can  be  trained  by  food-association  to  pick  them  out.  The 
most  elaborate  investigations,  however,  were  undertaken  by  Carl  von 
Hess  (1912)  who  experimented  both  with  diurnal  (chickens,  pigeons) 
and  nocturnal  birds  (owls).  He  found  that  chickens,  for  example, 
picked  up  grains  of  rice  illuminated  on  a  white  ground  by  spectral 
lights  from  the  red  end  of  the  spectrum  to  the  green  but  refused  those 
illuminated  with  blue  light  ;  he  therefore  concluded  that  this  bird  had 
colour  vision  but  that  the  spectrum  was  much  shortened  at  the  short - 
waved  end  and  that  the  fowl  was  blue-blind.  It  is  interesting  in  this 
connection  that  in  contrast  to  the  yellow,  blue  or  white  flowers  pre- 
ferentially pollinated  by  bees,i  the  usual  bird-pollinated  flowers  are  red 
(Werth,  1915  ;  Pickens,  1930  ;  Porsch,  1931).  This  suggestion  of 
blue -blindness,  although  supported  by  Heiming  (1920),  has  not  stood 
the  test  of  time,  for  it  has  been  subsequently  shown  that  the  hen  and 
many  other  species  can  see  blue  and  violet,  but  that  training  is  necessary 
if  the  bird  is  not  to  reject  a  food  coloured  quite  unlike  anything  in 
nature  ;  there  is,  however,  a  certain  degree  of  blue -violet -weakness, 
probably  because  of  the  absorption  of  short-waved  light  by  the  retinal 
oil-droplets  (Watson,  1915  ;  Lashley,  1916  ;  Halm,  1916  ;  Honigmann, 
1921  ;  Blasser,  1926  ;  Bailey  and  Riley,  1931  ;  Hamilton  and 
Coleman,  1933  ;  Plath,  1935  ;  and  others).  It  would  seem  clear  that 
the  limits  of  spectral  visibility  and  the  discrimination  of  hues  resemble 
those  of  man  ;  that  the  colour-vision  system  might  possibly  be 
interpreted  on  a  trichromatic  basis^;  that  a  relatively  small  number  of 
hues  are  distinguishable  (20  by  the  pigeon  in  contrast  with  160  by 
man,  Hamilton  and  Coleman,  1933)  ;    while  by  training  birds  to  peck 

1  p.  587. 

*  It  is  always  to  be  remembered  that  by  trichromatic  vision  is  meant  the  ability  to 
match  all  colours  with  a  mixture  of  three,  and  only  three,  primary  colours.  This  must 
involve  colour-mixing  experiments  and  without  these  it  is  illegitimate  to  draw  any 
conclusions  as  to  the  number  of  mechanisms  involved. 


THE   PERCEPTION   OF   COLOUR 


631 


from  coloured  pieces  of  paper  on  large  grey  backgrounds,  Revesz  (1921) 
showed  that  the  phenomenon  of  simultaneous  contrast  could  be 
elicited  as  in  man.  It  would  seem,  indeed,  that  while  the  behaviour 
of  Birds  is  largely  determined  by  vision,  they  rely  more  upon  the 
discrimination  of  hue  than  of  luminosity,  and  respond  more  consistently 
to  clues  involving  colour  than  those  depending  on  form  (Jones,  1954). 

The  appreciation  of  "  warning  colours  "  displayed  by  insects  illustrates 
the  biological  value  of  colour  vision  to  the  bird  in  its  feeding  habits.  In  experi- 
ments with  the  swallow,  Hirundo,  Swymierton  described  vividly  how  one  bird 
would  watch  another  intently,  observing  its  reaction  to  a  new  test -insect  of  a 
particular  colour  as  if  with  the  intention  of  profiting  thereby  by  avoiding  the 
unpleasant  experience  of  eating  a  distasteful  species.  In  the  same  way  birds 
such  as  the  domestic  hen  can  be  trained  to  tasks  involving  the  discrimination 
of  colour  as  well  as  of  size  and  form,  both  singly  and  in  combination  (see  Altevogt, 
1951  ;   Thorpe,  1956). 

The  colour  vision  of  Birds  must  be  considerably  modified  by  the 
presence  of  coloured  oil-droplets,  a  circumstance  which  must  also 
apply  to  other  species  similarly  equipped.^  Initially,  owing  to  the 
inferior  quality  of  the  earlier  lenses  in  the  microscopes  employed  in 
histological  work,  droplets  of  a  much  larger  range  of  spectral  hues — - 
green,  blue  and  violet — were  described  in  the  retina  of  birds,  and 
Krause  (1863)  put  forward  the  theory  that  this  coloured  mosaic 
represented  a  peripheral  mechanism  whereby  colour  vision  could  be 
determined  in  the  avian  eye  by  the  absorption  of  all  wave-lengths 
except  one  by  a  particular  drojDlet  so  that  different  cones  were  stimu- 
lated only  by  a  single  narrow  sjjectral  band  of  light.  This  theory  held 
the  field  for  many  years.  Convincing  arguments,  however,  can  be 
advanced  against  it  for  oil -droplets  are  by  no  means  necessary  for 
colour  vision  :  fishes  (and  man)  have  colour  vision  and  no  coloured 
droplets  ;  lizards  have  a  colour-system  of  considerable  complexity  and 
only  yellow  droplets  ;  the  fovea  of  birds  with  its  excellent  appreciation 
of  colour  has  yellow  droplets  only  ;  and  in  the  periphery  of  the  avian 
retina  the  colours  of  the  droplets  bear  no  relation  to  the  spectral  range 
of  the  bird.  It  is  much  more  likely,  as  Walls  and  Judd  (1933)  suggested, 
that  these  droplets,  whatever  their  colour,  act  as  filters  with  the  triple 
function  of  increasing  contrast,  reducing  glare  and  lessening  chromatic 
aberration — that  they  are,  in  fact,  an  aid  to  visual  acuity. 

The  yellow  droplet  at  the  avian  fovea,  cutting  off  the  sjjectrum  at  515-520 
m(x  like  a  yellow-tinted  sjaectacle,  allows  the  transmission  of  many  hues  but 

>  It  may  be  useful  to  summarize  the  occurrence  of  oil-droplets  in  the  visual  elements 
of  Vertebrates  at  this  point.  They  are  found  in  the  rods  of  Lepidosiren;  in  the  cones 
of  Chondrosteans,  the  coelacanth  and  Protopterus  (all  colourless),  diurnal  Anurans 
(yellow),  lizards  (yellow  ;  some  nocturnal  types  colourless  or  none),  Chelonians 
(orange,  yellow,  red),  <S'jD/ieHodoM  (colourless  or  pale  yellow),  Birds  (red,  orange,  yellow, 
occasionally  green  or  colourless),  the  platypus  (colourless),  and  Marsupials  (except  some 
Didelphyidse)  (colourless). 


Swallow 


632  THE   EYE   IN   EVOLUTION 

eliminates  most  of  the  violet  and  some  of  the  blue,  thus  diminishing  glare  and 
at  the  same  time  considerably  reducing  chromatic  aberration,  a  phenomenon 
for  which  these  wave-lengths  are  partly  responsible.  This  colour  of  droplet  is 
thus  found  preferentially  in  the  central  and  ventral  parts  of  the  retina  where  it 
mvist  increase  acuity  and  enhance  contrast  by  eliminating  the  preponderating 
and  dazzling  blue  light  of  the  sky.  The  reduced  sensitivity  to  blue  light  of  the 
chicken  and  other  species  remarked  vipon  above  is  thus  explained,  as  well 
(perhaps)  as  the  tendency  of  such  birds  as  pollinate  flowers  (humming-birds, 
honey-birds)  to  choose  preferentially  red  blooms.  The  red  droplets,  cutting  off 
the  spectrum  at  580-590  mfj,,  will  be  particularly  valuable  in  damping  down  the 
excessive  long-waved  light  at  sunrise  or  sunset  (hence  their  large  numbers  in 
early-rising  song  birds  in  which  they  comprise  20%  of  the  total)  ;  they  will  have 
a  similar  effect  on  the  light  of  long  wave-lengths  reflected  from  the  water  (hence 
their  presence  in  quantity  in  turtles  or  the  kingfisher)  ;  they  will  be  of  less  value 
in  other  optical  conditions  (hence  their  paucity — 3  to  5% — in  late-rising  cre- 
puscular types  such  as  swifts  or  swallows)  ;  while  their  preferential  occvirrence 
in  the  dorsal  part  of  the  retina  will  give  maximal  contrasts  to  objects  seen  against 
a  green  backgrovind.  The  orange  droplets  will  provide  a  transition  between  the 
two. 

It  would  seem,  therefore,  that  the  oil-droplets  have  no  part  in  the 
mechanism  of  colour  vision,  but  at  the  same  time  they  must  influence 
the  appearance  of  coloured  objects  so  that  the  bird's  appreciation  of 
them  ought  to  be  quite  different  from  ours.  To  birds  that  possess  them, 
central  vision  probably  resembles  vision  through  yellow  spectacles, 
while  elsewhere  in  the  retina  with  the  constant  sudden  movements  of 
the  head,  each  object  is  scanned  and  analysed  now  through  one  filter, 
now  through  another,  the  kaleidoscopic  changes  allowing  an  unusually 
high  discrimination  of  tone  and  necessarily  increasing  contrast  and 
therefore  the  visibility  of  details.^  Looking  through  this  polychromatic 
mosaic,  a  bird  should  be  able  to  distinguish  objects  invisible  to  us  : 
thus  Judd  found  that  a  bird  could  readily  pick  up  crickets  mixed 
deliberately  with  dry  leaves  although  he  could  not  differentiate  between 
them,  while  Rabaud  (1920)  noted  that  sparrows  saw  at  once  and  ate 
green  phasmids,  which  as  far  as  he  was  concerned  mimicked  perfectly 
the  leaves  on  which  they  rested. 

THE    COLOUR    VISION    OF    MAMMALS 

As  we  would  expect  from  the  rarity  of  strongly  diurnal  Mammals, 
the  possession  of  colour  vision  by  the  members  of  this  class  is  apparently 
rare.  The  more  primitive  and  nocturnal  types  are  colour-blind;  some  of 
the  arhythmic  types  may  possess  some  degree  of  hue-discrimination  but 
this  faculty  plays  a  small  part  in  their  behaviour,  being  completely 
subservient  to  sensations  of  luminosity  ;  only  the  higher  Primates 
have  a  colour  sense  sufficiently  developed  to  influence  their  activities 
to  an  extent  that  can  be  experimentally  elicited  with  certainty. 

Of  the  colour  vision  of  monotremes  we  know  nothing  ;  among 
MARSUPIALS,  Salzle  (1936)  reported  negative  results  with  the  opossum, 

^  See  further  p.  662. 


THE   PERCEPTION   OF   COLOUR 


633 


Didelphys.  Among  insectivores,  only  the  hedgehog,  Erinaceus,  has 
been  examined  ;  in  experiments  wherein  brightness -differences  were 
inadequately  controlled,  Herter  and  Sgonina  (1933-34)  suggested  that 
this  animal  could  see  yellow  as  distinct  from  grey,  but  on  the  evidence 
this  conclusion  seems  unjustified. 

Among  the  rodents  a  considerable  number  of  species  has  received 
experimental  attention.  The  rat,  with  its  nocturnal  habits,  its  practical 
absence  of  cones  and  complete  absence  of  a  Purkinje  phenomenon  as 
measured  pupilloscopically  or  electroretinographically,  would  not  be 
expected  to  possess  a  colour  sense.  Training  experiments  with  spectral 
lights  (Watson  and  Watson,  1913)  or  coloured  papers  (Munn,  1932  ; 
Coleman  and  Hamilton,  1933  ;  Muenzinger  and  Reynolds,  1936)  have 
verified  this  expectation.  The  work  of  Walton  (1933),  Walton  and 
Bornemeier  (1938)  and  Cain  and  Extremet  (1954),  however,  suggested 
the  opposite  conclusion — that  this  animal  could  make  choices  on  the 
basis  of  hue-discrimination  particularly  between  red  and  green  ;  but 
this  view  is  unique.  Similarly  negative  results  were  obtained  by 
training  experiments  in  domestic  ynice  (Yerkes,  1907  ;  Trincker  and 
Brendt,  1957)  but  again,  one  investigator,  Hopkins  (1927),  claimed 
that  1  mouse  in  7  could  distinguish  red  from  white.  Wild  mice  were 
investigated  by  Salzle  (1936)  ;  one  variety,  the  European  field-mouse, 
Ajjodeinus,  showed  no  evidence  of  colour  vision,  but  the  red-backed 
vole,  Clethrionomys,  could,  in  his  view,  discriminate  between  red  and 
green,  although  not  between  green,  yellow  and  blue.  In  the  reports 
of  these  experiments,  however,  the  control  of  the  intensity  of  stimula- 
tion is  vague.  A  similar  criticism  applies  to  the  study  of  the  guinea-pig 
by  Sgonina  (1936)  who  assumed  that  this  animal  had  the  same  apprecia- 
tion of  brightness  as  he  himself  ;  but  in  well-controlled  experiments 
using  the  optomotor  reaction,  Trincker  and  Berndt  (1957)  obtained 
different  responses  with  red,  yellow,  green  and  blue.  Completely 
negative  results  were  obtained  in  the  rabbit  by  Washburn  and  Abbot 
(1912)  and  in  the  porcupine  by  Sackett  (1913).  The  evidence  therefore 
points  to  the  conclusion  that  these  rod-rich  nocturnal  rodents,  all  of 
which  show  a  low  sensitivity  to  red  light,  have  achromatic  vision. 

It  would  be  expected  that  the  highly  diurnal  squirrel  with  its  cone- 
rich  retina  would  be  in  a  different  case.  Here  the  evidence  is  confusing. 
In  experiments  in  which  brightness  was  considered  analogous  to 
its  appreciation  by  the  human  experimenter,  Colvin  and  Burford 
(1909)  and  Salzle  (1936)  concluded  that  the  European  tree-squirrel, 
Sciurus  vulgaris,  could  discriminate  hues  ;  but  in  more  adequately 
controlled  work  Locher  (1933)  found  that  one  squirrel  out  of  three 
could  with  great  difficulty  be  trained  to  differentiate  yellow  and 
light  green  ;  all  other  colours  were  equated  with  different  shades  of 
grey.    Meyer-Oehme  (1956),  on  the  other  hand,  claimed  that  squirrels 


Hedgehog 


Por: 


eupiiie 


634  THE   EYE   IN   EVOLUTION 

could  be  trained  in  behavioural  experiments  to  distinguish  red,  yellow, 
green  and  blue  papers  from  one  another  and  from  grey  of  equal 
brightness.  With  the  European  ground-squirrel  (souslik,  Citellus 
citellus),  Kolosvary  (1934)  concluded  that  a  colour-preference  existed 
for  blue.  None  of  these  experiments  is  fully  convincing,  but  it  seems 
that  a  weak  capacity  for  colour  vision  may  exist  in  some  species  of 
squirrel,  while  in  many  individuals  it  is  wholly  absent  ;  even  if  it  is 
occasionally  present,  it  seems  unlikely  that  it  can  determine  behaviour. 
Among  the  carnivores,  the  earlier  workers  gave  most  attention 
to  the  dog.  The  variable  results  initially  obtained  are  vitiated  by 
absence  of  the  adequate  control  of  intensity  (Lubbock,  1888  ;  Gates, 
1895  ;  Himstedt  and  Nagel,  1902  ;  Nicolai,  1907  ;  Orbeli,  1909  ; 
Colvin  and  Burfo^d,  1909  ;  Kahscher,  1909)  ;  while  the  better  con- 
trolled experiments  of  Samoiloff  and  Pheophilaktova  (1907)  and 
E.  M.  Smith  (1912)  led  to  the  conclusion  that  hues  have  little  significance 
for  this  animal  despite  its  undoubted  intelligence  and  amenability  to 
experimental  restraints.  Confusion  of  coloured  papers  with  greys  was 
practically  constant  although  after  prolonged  training  some  animals 
seemed  to  show  some  recognition  of  green.  It  will  be  remembered  that 
Orbeli  (1909)  in  Pavlov's  laboratory,  found  similarly  inconclusive 
results  on  attempting  to  establish  conditioned  reflexes  to  colours  in 
this  animal.^  All  observers  are  agreed  that  colours  have  no  significance 
whatever  for  the  cat  whether  attempts  at  training  have  been  made  by 
coloured  papers  or  spectral  lights  (de  Voss  and  Ganson,  1915  ;  Gregg 
et  al.,  1929  ;  Gunter,  1952-54  ;  Meyer  et  al,  1954)  ;  the  positive 
results  claimed  by  Colvin  and  Burford  (1909)  and  Kalischer  (1909)  can 
be  explained  by  inadequate  controls  and  the  mistake  of  equating 
relative  brightness  to  human  standards.  A  similar  criticism  applies  to 
the  claim  of  Cole  (1907)  and  Cole  and  Long  (1909)  that  the  raccoon  has 
some  degree  of  colour  vision  ;  Davis  (1907)  and  Gregg  and  his  co- 
.  workers  (1929)  obtained  completely  negative  results  with  this  animal, 
as  did  Miiller  (1930)  in  the  marten,  Martes,  and  the  pole-cat,  Putorius. 
It  would  seem,  therefore,  that  with  the  problematical  exception  of  the 
dog,'^  all  the  Carnivores  so  far  tested  have  proved  to  be  colour-blind 
or  have  indicated  that  colours  have  no  significance  for  them.  If  in 
some  dogs  some  discrimination  of  hue  is  possible,  the  faculty  seems  to 
be  without  importance  to  the  animal  and  is  entirely  dominated  by 
sensations  of  form  and  brightness. 

UNGULATES  which  have  been  investigated  have  been  found  to  be 
similar.  Cattle — even  the  fiajhting  bulls  of  Latin  Europe  and  America — 
are  completely  colour-bKnd  (Kittredge,  1923  ;    Stratton,  1923)  ;    they 

»  p.  623. 

"  See,  however,  Schubert  (1950)  who,  while  admitting  that  it  has  not  been  shown 
experimentally  that  dogs  have  hue-discrimination  analogous  to  man,  insists  that  these 
animals  are  not  colour-blind. 


THE   PERCEPTION   OF   COLOUR 


635 


are  enraged  by  the  flutter,  not  the  colour  of  the  matador's  cloak  and 
equally  enraged  whether  it  be  red,  green,  grey  or  white.  Grzimek 
(1952),  on  the  other  hand,  from  feeding  experiments  wherein  colours 
were  matched  with  shades  of  grey,  claimed  that  the  horse  possessed  a 
considerable  degree  of  colour  vision,  best  for  green  and  yellow  and 
least  for  red. 

PRIMATES  are  the  only  order  among  the  Mammalia  in  which 
colour  vision  exists  as  a  factor  capable  of  determining  behaviour,  and 
within  this  class  this  applies  only  to  the  higher  diurnal  species.  Most 
of  the  lower  Primates  are  nocturnal,  but  even  the  diurnal  lemur  has 
been  shown  to  be  either  totally  colour-blind,  confusing  all  colours  with 
greys,  or  to  possess  a  colour  sense  so  meagre  as  to  be  valueless,  com- 
parable to  that  which  may  exist  in  some  dogs  [Lemur  mongoz,  Bierens 
de  Haan  and  Frima,  1930).  Among  the  Anthropoidea,  on  the  other 
hand,  colour  vision  begins  to  become  evident.  The  primitive  capuchins 
(Cebus)  are  of  particular  interest  since  they  appear  to  show  a  dichro- 
matic colour  system  corresponding  to  a  protanopic  deficiency  in  man 
with  a  lowered  sensitivity  to  red  (Watson,  1909  ;  Grether,  1939). 
The  marmosets  have  not  been  studied  from  this  point  of  view  ;  but 
the  higher  Simians  all  show  a  well-developed  chromatic  system,  both 
the  New  World  Platja-rhines  and  the  Old  World  Catarrhines  and  Apes.^ 


Lemur 


Abelsdorff.       Arch.    Augenheilk.,    58,     64 

(1907). 
Altevogt.     Z.  TierpsychoL,  8,  75  (1951). 
Bailey    and    Rilev.       Trans,    roy.    Canad. 

hist.,  18,  47 '(1931). 
Bauer.     Zbl.  Physiol.,  23,  593  (1909). 
Pfliigers    Arch.     ges.     Physiol.,     133,     7 

(1910)  ;    137,  622  (1911). 
Beniuc.     Z.  vergl.  Physiol,  19,  724  (1933). 
Bierens   de    Haan    and    Frima.      Z.    vergl. 

Physiol.,  12,  603  (1930). 
Birukow.     Z.  vergl.  Physiol.,  25,  92  (1937)  ; 

27,  41.  322  (1939)  ;    31,  322  (1949)  ; 

32,  348  (1950). 
Blasser.  Zool.  Jb.,  Abt.   Zool.  Physiol.,  43, 

69  (1926). 
Brecher.  Z.  vergl.  Physiol,  23,  771    (1936). 
Bull.  J.  marine  Biol  Assoc.  U.K.,  20,  347 

(1935). 
Burkamp.     Z.     Psychol.    Physiol    Sinnes. 

Abt.  II,  55,  133  (1923). 
Cain    and    E.xtremet.      C.    R.    Soc.    Biol. 

(Paris),  148,  115  (1954). 
Cole.     J.  camp.  Neurol  Psychol,  17,  211 

(1907). 
Proc.    Amer.    Acad.   Arts  Sci.,   45,    161 

(1910). 
Cole  and  Long.    J.  comp.  Neurol.  Psychol, 

19,  657  (1909). 


Coleman  and  Hamilton.    J.  comp.  Psychol, 

15,  177  (1933). 
Colvin    and    Burford.       Psychol.    Monog. 

Supjjl,  11,  1  (1909). 
Davis.     Amer.  J.  Psychol,  18,  447  (1907). 
Engelking.     Z.   Psychol.   Physiol.  Sinnes., 

Abt.  II,  50,  319  (1919). 
Klin.  Mbl  Augenheilk.,  69,  177  (1922)  ; 

73,  1  (1924). 
Erhard.     Zool.  Jb.,  Abt.  Zool.  Physiol,  41, 

489  (1924). 
Freytag.      Arch,    vergl.    Ophthal,    4,    68 

(1914). 
von  Frisch.     Pfliigers  Arch.  ges.   Physiol, 

138,  319  (1911). 
Zool  Jb.,  Abt.  Zool.  Physiol,  32,   171  ; 

33,  107,  151  (1912)  ;    34,  43  (1913). 
Natnruissenschafte7i,  11,  470  (1923). 
Z.  vergl  Physiol,  2,  393  (1925). 
Gates.     Monist,  5,  574  (1895). 
Goldsmith.     Bull  Inst.  gen.  Psychol,  14, 

97  (1914). 
Graber.        Grundlinien     z.     Erjorsch.     d. 

Helligkeits-  u.  Farbensinnes  d.  Thiers, 

Prague  (1884). 
S.   B.   Akad.    Wiss.    Wien.,   91   (1),    129 

(1885). 
Granit.    J.  Physiol,  85,  421  (1935). 


^  The  spider  monkey,  Ateles,  the  baboon,  Papio,  the  macaque,  Nemestrmus,  the 
langur,  Pithecus,  the  rhesus  monkey,  Macaca  rhesus,  the  mangabey,  Cercocebus,  and 
the  chimpanzee,  Pan  (Kinnaman,  1902  ;  Kohler,  1918  ;  Kohts,  1918  ;  Trendelenburg 
and  Schmidt,  1930  ;    Kliiver,  1933  ;   Brecher,  1936  ;    Grether,  1939-41). 


636 


THE   EYE   IN   EVOLUTION 


Granit.    Sensory  Mechanisms  of  the  Retina, 

Oxon.  (1947). 
Granit    and     Svaetichin.       Upsala    Ldk. 

Forh.,  65,  161  (1939). 
Granit,    Therman    and    Wrede.       Skand. 

Arch.  Physiol.,  80,  142  (1938). 
Granit  and  Wrede.     J.  Physiol.,  89,  239 

(1937). 
Gregg,  Jamison,  Wilkie  and  Radinsky.    J. 

comp.  Psychol.,  9,  379  (1929). 
Grether.     Coinp.  Psychol.  Monog.,  15  (4), 

38  (1939). 
J.  comp.  Psychol.,  29,  167  (1940). 
J.  exp.  Psychol.,  26,  394  (1940)  ;   28,  419 

(1941). 
Grodzinska.      Biill.   Acad.    Polonaise  Sci. 

Lettres  (B),  225  (1948). 
Grzimek.     Z.  Tierpsychol.,  9,  23  (1952). 
Gunter.    J.  Physiol.,  117,  45P  ;    118,  49P 

(1952). 
J.    comp.    physiol.     Psychol.,    47,     169 

(1954). 
Haempel  and  Kolmer.     Biol.  Zbl.,  34,  450 

(1914). 
Hahn.     Z.  inss.  Zool.,  116,  1  (1916). 
Hamburger.      Z.    I'ergl.    Physiol.,    4,    286 

(1926). 
Hamilton  and  Coleman.    J.  comp.  Psychol., 

15,  183  (1933). 
Hecht  and  Pirenne.     J.  gen.  Physiol.,  23, 

709  (1940). 
Henning.       Pfliigers    Arch.    ges.    Physiol., 

178,  91  (1920). 
Herter.     Z.  vergl.  Physiol,  21,  450  (1934). 
Die     Fischdressuren     u.     ihre     sinnes- 

physiologische       Grundlagen,       Berlin 

(1953). 
Herter  and   Sgonina.      Z.   vergl.    Physiol., 

18,  481  (1933). 
von  Hess,  C.     Arch.  Augenheilk.,   58,  182 

(1907)  ;    64,  Erganz.,  1  (1909). 
Pfliigers    Arch.    ges.     Physiol.,     134,     1 

(1910)  ;    142,  405  (1911). 
Winterstein's    Hb.     d.    vergl.     Physiol., 

Jena,  4,  1  (1912). 
Zool.  Jb.,  Abt.   Zool.   Physiol.,  33,   387 

(1913). 
Ergebn.  d.  Physiol.,  20,  1  (1922). 
Himstedt  and  Nagel.      Fest.  d.   Albrecht- 

Liiduigs-Univ.,  Freiburg,  259  (1902). 
Hineline.    J.  e.rp.  Zool.,  47,  85  (1927). 
Honigmann.     Pfliigers  Arch.  ges.  Physiol., 

189,  1  (1921). 
Hopkins.     Z.  vergl.  Physiol.,  6,  299  (1927). 
Horio.     Jap.  J.  med.  Sci.,  Pt.  Ill,  4,  395 

(1938). 
Hurst.    J.  comp.  physiol.  Psychol.,  46,  442 

(1953). 
Jones,  L.  V.     J.  comp.  physiol.   Psychol., 

47,  253  (1954). 
Kahmann.     Zool.  Garten,  4,  27  (1931). 
Kalischer.       Arch.     Anat.     Physiol.,     303 

(1909). 
Kinnaman.      Amer.   J.    Psychol.,    13,    98, 

173  (1902). 


Kittredge.       J.     comp.     Psychol.,    3,     141 

(1923). 
Kliiver.  Behaviour      Mechcmisms       in 

Monkeys,    Chicago   (1933). 
Kohler.     Abhandl.  k.  joreuss.  Akad.  Wiss., 

3  (1918). 
Kohts.     J.   Psychol,  nortn.  path.,  25,  255 

(1918). 
Kolosvary.      J.    genet.    Psychol.,    44,    473 

(1934). 
Krause.     Z.  rat.  Med.,  20,  1  (1863). 
Kiihn.     Nachr.   k.   Ges.    Wiss.,   Gottingen 

(1924),  p.  66  (1925). 
LasBhley.    J.  anim.  Behav.,  6,  1  (1916). 
Laurens.    Amer.  J.  Physiol.,  64,  97  (1923). 
Locher.      Untersuch.  u.  d.   Farbensinn.  v. 

Eichhornchen,  Leiden  (1933). 
Loeb.       Der    Heliotropismus    der     Tiere, 

Wurzburg  (1890). 
Lubbock.      Senses,    Iristincts   and,    Intelli- 
gences of  Animals,  London  (1888). 
Mast.     Bull.   U.S.  Bureau  Fish.,  34,   175 

(1916). 
Matthews  and  Matthews.    Nature  (Lond.), 

143,  983  (1939). 
Merker.     Biol.  Rev.,  9,  49  (1934). 

Zool.  Jb.,  Abt.   Zool.   Physiol.,  59,   391 

(1939). 
Biol.  Zbl.,  59,  87  (1939). 
Meyer,    Miles    and    Ratoosh.      J.    Neuro- 

physiol.,  17,  289  (1954). 
Meyer-Oehme.      Naturuissenschaften,    43, 

167  (1956). 
Morgan.       Habit    and    Instinct,     London 

(1896). 
Muller,    D.      Z.    vergl.    Physiol.,    12,    293 

(1930). 
Muenzinger     and     Reynokls.       J.     genet. 

Psychol.,  48,  58  (1936). 
Munn.    J.  genet.  Psychol.,  40,  351  (1932). 
Musolff.     Zool.  Beitr.,  1,  399  (1955). 
Nakayama.     Nip.  Gank.  Zas.  (1921). 

Kiln.  Mbl.  Augenheilk.,  69,  143  (1922). 
Nicolai.      J.   f.    Psychol.    Neurol.,    10,    1 

(1907). 
Noble  and  Curtis.     Amer.  Mus.  nat.  Hist. 

Bull,  76,  1  (1939). 
Orbeli.     Ark.  Biol.  Nauk.,  14,  31  (1909). 
Pickens.     The  Auk,  47,  346  (1930). 
Piper.    Arch.  Anat.  Physiol.,  Physiol.  Abt., 

8uppl.,  133  (1905). 
Plath.     Z.  vergl.  Physiol.,  22,  691  (1935). 
Porsch.     Biol,  generalis,  7,  647  (1931). 
Porter.    A^ner.  J.  Psychol.,  15,  313  (1904)  ; 

17,  248  (1906). 
Pumphrey.     Proc.  Linn.  Soc.  Lond.,  161, 

95  (1949). 
Quaranta.     A^iat.  Rec,  105,  510  (1949). 
Quaranta  and  Evans.    Anat.  Rec,  105,  580 

(1949). 
Rabaud.     Elements  de  biol.  generale,  Paris 

(1920). 
Reeves.      Behaviour   Monog.,    4    (3),    106 

(1919). 
Reighard.    Carnegie  Inst.  Wash.,  Pub.  No. 

103,  257  (1908). 


THE   PERCEPTION   OF   COLOUR  637 

Revesz.       Z.     Psychol.     Physiol.    Sinnes.,  Trendelenburg    and    Schmidt.       Z.    vergl. 

Abt.  I,  87,  130  (1921).  Physiol.,  12,  249  (1930). 

Rochon-Duvigneaud.     Les  yeux  et  la  vision  Trinoker  and  Berndt.     Z.  vergl.   Physiol., 

des  Vertebrcs,  Paris  (1943).  39,  607  (1957). 

Rouse.     Harvard  Psychol.  Studies,  2,  o80  Vanderplank.        Proc.     zool.    Soc.     Lond., 

(1906).  50.5  (1934). 

Rutgers.     Klin.  Mbl.  Augenheilk.,  71,  449  de  Voss  and  Ganson.     J.  anim.  Behav.,  5, 

(1923).  115  (1915). 

Sachs.      Pfliigers  Arch.   ges.    Physiol,   52,  Wagner.     Z.  vergl.  Physiol.,  18,  37S  (1932). 

79  (1892).  Walls.        The     Vertebrate     Eye,     Michigan 
v.   Graefes  Arch.    Ophthal.,   39    (3),    108  (1942). 

(1893).  Walls  and  Judd.      Brit.  J.   Ophthal.,   17, 
Z.    Psychol.    Physiol.   Sinnes.,    22,    386  641.  705  (1933). 

(1900).  Walton.     J.  comp.  Psychol.,  15,  359,  373 
Sackett.     Behav.  Monog.,  2  {VJ\3).  (1933). 

Salzle.     Z.  Sdugetierk.,  11,  106(1936).  Walton  and  Bornemeier.  J.  r/e?ie?.  Psyc/(oZ., 
Samoiloff     and      Pheophilaktova.        Zbl.  52,  165  (1938). 

Physiol.,  21,  133  (1907).  Warner.     Qimrt.  Rev.  Biol,  6,  329  (1931). 

Schiemenz.       Z.    vergl.     Physiol.,    1,     175  Washburn  and  Abbot.     J.  anitn.   Behav., 

(1924).  2,  145  (1912). 

Schlieper.    Z.  vergl.  Physiol.,  6,  453  (1927).  Washburn  and  Bentlev.    J.  co?np.  Neurol. 
Schnurmann.     Z.  Biol.,  71,  69  (1920).  Psychol,  16,  113  (1906). 

Schubert.    Wien.  tierdrztl  Mschr.,  37,  127  Watson.     J.  comp.  Neurol.  Psychol,  19,  1 

(1950).  (1909). 

Sgonina.     Z.  wiss.  Zool,  148,  350  (1936).  Dept.  marine  Biol,  Carnegie  Inst.  Wash., 

Smith,    E.    M.      Brit.   J.    Psychol,   5,    119  7,  87  (1915). 

(191-)-  Watson  and  Watson.    J.  anim.  Behav.,  3, 
Smith,  R.  G.    J.  Psychol,  25,  171  (1948).  1  (1913). 

Stratton.       Psychol.    Rev.,    30,    321,    380  Weale.     J.   Phi/siol,  121,  548  (1953). 

(1923).  Werth.     Bofan.  Jb.,  53,  314  (1915). 

Sumner.    J.  e.ryj.  Zoo^,  10,  409  (191 1).  White.     J.  e.rja.  ZooZ.,  27,  443  (1919). 

Thibault.      Arch.    Sci.    Phi/siol,    3,     101  Wojtusiak.      Z.    vergl    Physiol,    18,    393 

(1949).  "^  (1933). 

Thomas.       Naturicisseyischajten,     40,     322  Wolff.     Z.  vergl  Physiol,  Z,  '219  (\925). 

(1953).  Yerkes.     Psi/chol  Monog.,  4,  579  (1903). 
Zool  Jb.,  Abt.   Zool   Physiol,   66,    129  The  Dancing  Mouse,  ^.Y .  {1901). 

(1955).  Zolotnitzkv.     Arch.   Zool   exp.   gen.,   9,   i 
Torelle.     Amer.  J .  Physiol,  9,  A:m  [1903).  (1901). 


THE  PERCEPTION  OF  FORM 

As  we  have  already  seen,  the  visual  acuity  of  most  Vertebrates 
(with  marked  exceptions)  is  low  ;  in  the  activities  of  animal  life 
greater  reliance  is  generally  placed  on  the  appreciation  of  differences 
of  luminosity  and  movement.  Although  on  this  account  the  eye  may 
often  be  a  relatively  poor  optical  instrument  in  the  resolution  of 
imagery,  that  is  not  to  say  by  any  means  that  it  is  not  biologically 
useful  ;  to  many  Vertebrates  living  in  an  aquatic  or  nocturnal 
environment  or  close  to  the  ground  with  a  restricted  horizon,  the 
appreciation  of  luminosity  and  movement  must  be  much  more  valuable 
than  an  ability  to  resolve  minutiae  in  form,  nor  would  an  eye  capable 
of  recording  elaborate  patterns  be  of  biological  utility  without  a  brain 
sufficiently  evolved  to  analyse  and  apjDreciate  and  utilize  such 
impressions. 

Apart  from  the  ability  of  the  brain  to  analyse  and  appreciate 


638  THE    EYE   IN   EVOLUTION 

visual  patterns,  the  acuity  of  vision  depends  on  two  factors — the  size 
and  optical  perfection  of  the  retinal  image  and  the  resolving  power  of 
the  retina.  So  far  as  optical  factors  are  concerned,  the  larger  the  eye, 
the  larger  and  therefore  the  more  analysable  the  image  ;  the  more 
transparent  the  media  and  the  more  perfect  the  refracting  system,  the 
higher  its  resolution  ;  and  if  objects  at  different  distances  are  to  be 
imaged  with  equal  clarity,  an  efficient  accommodative  mechanism  is 
a  necessity.  So  far  as  the  retinal  factors  are  concerned,  the  denser 
the  mosaic  of  recipient  elements  and  the  lower  the  ratio  of  these  to  the 
optic  nerve  fibres  (which  usually  means  the  greater  the  number  of 
cones),  the  higher  the  resolving  power  of  the  retina.  Before  assessing 
the  importance  of  visual  acuity  to  the  vertebrate  world  we  shall  take 
note  of  these  physical  factors  on  which  its  effectivity  is  based. 

THE    OPTICAL    SYSTEM 
THE    REFRACTION    OF    VERTEBRATES 

A  considerable  amount  of  work  has  been  devoted  to  the  estimation 
of  the  static  refractive  system  in  Vertebrates,  the  more  important 
results  of  which  are  summarized  below. 

CYCLOSTOMES — The  lamprey  is  myopic  to  the  extent  of  —  8  D  in  water,  a 
refraction  sviitable  for  a  parasitic  creature. 

FISHES — It  is  generally  agreed  that  selachians  are  all  strongly  hyper- 
metropic (in  water),  the  refraction  varying  from  +  8  to  +  15  D  with  some 
astigmatism  (Rochon-Duvigneaud,  1918  ;   Verrier,  1928-35  ;    Franz,  1931). 

In  TELEOSTEANS,  however,  the  position  is  not  so  clear.  Beer  (1894)  was  the 
first  to  study  this  question  intensively  ;  by  retinoscopy  he  found  the  eyes  of 
several  species  to  be  hypermetropic  but  he  discarded  these  results  in  favour  of  a 
theoretical  analysis  of  the  dioptric  system  of  the  eye,  which  led  him  to  conclude 
that  the  teleostean  eye  showed  a  degree  of  myopia  varying  in  different  species 
from  —3  D  to  —  12  D  in  water  (—40  to  —  90  D  in  air),  a  result  confirmed  or 
accepted  by  most  subsequent  writers  (Franz,  1931).  On  the  other  hand,  Rochon- 
Duvigneaud  (1918)  and  Verrier  (1928),  using  retinoscopy  vmder  water,  reaffirmed 
the  presence  of  a  hypermetropia  of  -f  8  or  -f  9  D  in  a  number  of  species  of 
pelagic  fishes,  and  Verrier  (1938),  placing  a  screen  in  the  coats  of  the  eye  at  the 
posterior  pole,  found  that  a  sharp  image  of  a  luminous  cross  could  not  be  obtained 
at  a  distance  less  than  40  cm.  under  water  ;  she  therefore  questioned  the 
accepted  view  that  myopia  was  characteristic  of  Teleosteans.  Her  results  were 
accepted  by  Rochon-Duvigneaud  (1943)  in  preference  to  those  of  Beer  ;  but 
the  optical  problem  is  difficult  and  the  position  is  obscure.  It  would  seem 
probable  that  some  Teleosteans  are  hypermetroiDic  while  some  may  be  myopic, 
particularly  deep-sea  types  wherein  a  myopia  may  be  present  up  to  —  12  or 
—  15  D.  In  this  connection  it  is  to  be  remembered  that  myopia  would  be  a 
useful  refraction  for  a  fish,  for  vision  under  water  at  any  considerable  distance 
is  impossible  in  any  case. 

AMPHIBIANS — Among  Anurans  the  refraction  of  the  frog  has  received  most 
study  ;  the  animal  is  essentially  terrestrial  in  its  visual  habits.  In  air,  retinoscopy 
shows  a  hypermetropic  error  of  the  order  of   +  3  D  with  +  2  D  of  astigmatism 


THE   PERCEPTION   OF   FORM  639 

with  the  axis  vertical.  If,  however,  a  theoretical  correction  is  made  for  the 
difference  of  level  between  the  reflecting  surface  of  the  retina  and  the  layer  of 
rods  and  cones,  Hirschberg  (1882)  concluded  that  the  hypermetropia  became 
converted  into  a  myopia  of  the  order  of  —  5  to  —  8  D  ;  Beer  (1898),  on  the 
other  hand,  assumed  a  smaller  degree  of  myopia.  Under  water,  of  course,  with 
the  elimination  of  the  corneal  refraction,  a  high  degree  of  hypennetropia  results 
(+  16  D,  Hirschberg  ;    +  25  D,  Beer). 

The  refraction  of  Urodeles  seems  to  be  suited  to  their  usual  environment. 
Among  aquatic  Urodeles  the  new^t  is  api^roximately  emmetropic  under  water 
and  strongly  myopic  in  air,  while  terrestrial  salamanders  tend  to  be  approximately 
emmetropic  in  air. 

REPTILES.  Little  is  known  of  the  refraction  of  Reptiles.  In  freshly 
decapitated  lizards  Kahmann  (1932)  usually  found  a  low  degree  of  hypermetropia, 
up  to  +  6  D  in  Lacerta  agilis.  The  Crocodilians  are  slightly  hypermetropic  in 
air  (+  7  to  +  8  D,  Abelsdoi-ff,  1898  ;  +  1  to  +  2  D,  Rochon-Duvigneaud, 
1943,  in  the  alligator)  ;  they  are  therefore  highly  hypemietropic  under  water. 
Most  tvirtles  are  emmetropic,  the  marine  species  in  water,  the  terrestrial  in  air. 
According  to  Beer  (1898)  snakes  are  usually  hypermetropic  (up  to  +  9  D). 

BIRDS.  The  majority  of  Birds  on  which  retinoscopy  has  been  undertaken 
has  been  found  to  be  emmetropic  or  slightly  hypermetropic,  the  notable 
exception  being  the  kiwi,  Apteryx,  which  Is  myopic  (Rochon-Duvigneaud,  1943)  ; 
the  aquatic  penguins  are«also  myopic  in  air. 

MAMMALS.  In  the  overwhelming  majority  of  Mammals  in  the  wild  state 
the  refraction  is  slightly  hypermetropic  (under  ID);  a  hypermetropia  of  greater 
degree  (+  2  to  +  5  D)  is  found  in  some  Marsvipials,  Edentates  and  Rodents  in 
natural  surroundings,  while  in  the  many  small  Mammals  equipped  with  small 
eyes  containing  a  relatively  large  lens  closely  ai^proximating  the  retina,  the 
hypermetropia  may  increase  up  to  +  7  or  +  10  D.  Most  of  such  IMammals  (as 
the  mouse)  are  nocturnal  in  type  and  obviously  depend  visually  on  the  apprecia- 
tion of  differences  in  luminosity  and  movement  rather  than  on  the  very  imperfect 
pattern-vision  of  which  their  eyes  are  capable.  The  similarly-sized  squirrel,  on 
the  other  hand,  which  is  highly  visual  in  its  habits,  is  practically  emmetropic  in 
natural  surrovmdings.  The  vmique  eyes  of  the  bats  (Chii'optera)  are  likewise 
strongly  hypermetropic  (+  15  D,  Rochon-Duvigneaud,  1943).  Myopia  in 
wild  and  natural  conditions  is  rare  and  sporadic,  being  confined  essentially  to 
some  Primates  (mandrils  and  baboons)  and  amphibious  types — Sirenians  (the 
dugong  is  —  5  D  in  air  but  strongly  hypermetropic  in  water)  and  Pinnipedes 
(seals,  sea-lions).  Thus  the  seal  may  have  —  4  D  of  myopia  combined  with 
—  9  D  of  astigmatism  with  the  axis  vertical  (Johnson,  1901).  According  to 
Matthiessen  (1886-93)  the  whale,  the  eyes  of  which  are  fully  adapted  for  aquatic 
vision,  is  slightly  hypermetropic  in  w^ater  ;  in  air,  of  course,  it  is  highly  myopic 
while  the  asymmetry  of  the  corneal  curvature  (neutralized  under  water)  results 
in  a  considerable  degree  of  astigmatism  (4  to  4-5  D).  Ungulates  are  generally 
emmetropic  but  tend  to  have  some  horizontal  astigmatism,  perhaps  an  adaptation 
to  extend  the  horizontal  visual  field.  Thus  most  horses  are  emmetropic  with 
small  variations  towards  hypermetropia,  myopia  or  astigmatism  (Rochon- 
Duvigneaud,  1943).  Similarly  dogs  and  cats  have  a  smaller  range  of  refraction 
than  luan  ;  the  majority  are  emmetropic  or  nearly  so  and  a  high  refractive 
error  is  a  rarity  (above  -\-  2  D),  although  errors  of  the  order  of  4  D  are  found 
more  commonly  in  n:iyopia  than  hypermetropia.  Among  domestic  animals, 
however,  the  refractive  error  tends  to  vary  considerably  'n\  all  directions  of  error  ; 
thus  many  animals  kept  in  hutches  such  as  rabbits,  guinea-pigs  and  so  on,  often 
develop  a  high  degree  of  myopia. 


640  THE   EYE   IN  EVOLUTION 


ACCOMMODATION    IN    VERTEBRATES 

While  an  emmetropic  static  refraction  is  necessary  for  the  attain- 
ment of  a  high  degree  of  visual  acuity,  the  capacity  to  adjust  the 
optical  system  for  near  or  distant  vision  is  almost  equally  important, 
particularly  in  such  activities  as  the  capture  of  prey.  In  an  amphibious 
life  if  any  adjustment  to  the  two  environments  is  attempted  the 
importance  of  accommodation  is  still  greater  owing  to  the  difference 
in  refractivity  between  water  and  air  ;  in  an  active  arboreal  life  a 
rapid  and  effective  adjustment  becomes  vital  for  safety  ;  while  the 
need  for  close  examination  of  objects  manipulated  by  the  hands 
becomes  of  crucial  importance  in  the  activities  of  the  higher  Primates 
and  man. 

Few  vertebrate  species  are  entirely  without  accommodation,  and 
to  these  vision  is  invariably  of  little  biological  importance.  Such  a 
mechanism  is  lacking  in  the  extant  representatives  of  the  primitive 
groups  of  Fishes — Chondrosteans,  Dipnoans  ^  and  the  coelacanth  ;  the 
function  of  the  campanular  muscle  of  Holosteans  has  not  been 
explored.  Among  Amphibians  and  Sauropsidans  an  accommodative 
mechanism  is  present  except  perhaps  in  Sphenodon.  Owing  to  their 
nocturnal  habits,  accommodation  is  lacking  or  exceedingly  feeble 
in  primitive  Mammals.  It  is  absent  in  Monotremes,  and  although  a 
ciliary  muscle  is  present  in  Marsupials,  no  accommodation  has  been 
demonstrated  in  any  species  of  this  group.  In  the  lower  Placentals 
accommodative  activity  is  similarly  lacking  for  the  ciliary  muscle  is 
vestigial  if,  indeed,  it  is  present  (except  in  squirrels)  ;  even  Ungulates 
such  as  the  horse,  sheep  and  pig  have  no  demonstrable  dynamic 
accommodation,  and  apart  from  the  feeble  accommodation  of  squirrels 
and  Carnivores,  an  effective  range  is  found  among  Mammals  only  in 
the  otter  and  in  the  Primates,  particularly  in  man. 

Within  the  vertebrate  phylum  accommodation  is  achieved  by  a 
great  variety  of  devices  ;  it  would  appear  as  if  at  one  time  or  another 
in  the  various  species  every  conceivable  means  of  adjusting  the 
dioptric  system  of  the  eye  to  various  distances  had  been  attempted. 
These  varying  expedients  may  be  classified  into  two  types — static 
devices  whereby  optical  elasticity  is  achieved  by  structural  peculiarities; 
and  djmamic  devices  depending  upon  an  active  alteration  in  the 
dioptric  system  brought  about  by  muscular  activity. 

Static  Devices 

In  the  first  place,  it  is  to  be  remembered  that  a  swmU  eye  to  a 
large  extent  obviates  the  need  for  an  active  accommodative  mechanism. 
A  small  lens  with  a  short  focal  length  has  a  greater  depth  of  focus  than 

'  The  eye  of  Neoceratodus  is  unexplored  from  this  point  of  view. 


THE   PERCEPTION   OF   FORM  641 

a  large  lens,  while  in  the  retina  of  such  an  eye  the  visual  elements  are 
relatively  large  so  that  the  image  still  falls  on  the  rods  and  cones  even 
although  it  suffers  a  considerable  (relative)  excursion.  It  is  probable, 
indeed,  that  small  eyes  (as  are  typical  of  the  more  primitive  Placentals 
which  are  without  accommodative  adjustment)  have  a  range  of  vision 
as  great  as  the  large  eyes  of  most  of  the  more  highly  developed 
Carnivores. 

In  many  cases,  however,  specific  expedients  are  found  which 
provide  a  varying  degree  of  accommodative  elasticity,  some  of  them 
probably  incidental,  others  obviously  adapted  for  the  purpose.  These 
may  concern  the  optical  system  of  the  eye  or  the  retina.  Among  these 
the  more  important  are  : 

(a)  A  stenojjoeic  jjupil  is  primarily  a  protective  adaptation  against 
excessive  light,  but  at  the  same  time  it  converts  the  optical  system  of 
the  eye  into  that  of  a  pin-hole  camera  in  which  accommodative 
adjustment  is  unnecessary — a  simple  expedient  which,  however,  suffers 
from  the  disadvantage  that  the  available  light  reaching  the  retina  is 
cut  do\m  in  proportion  as  the  diminution  of  the  aperture  becomes 
effective.  For  purely  mechanical  reasons  such  a  stenopoeic  aperture 
is  more  readily  and  therefore  more  frequently  attained  by  the  develop- 
ment of  a  slit -pupil  than  a  small  circular  pupil  which  requires  a 
difficult  muscular  effort.^  Since  it  abolishes  the  necessity  for  accom- 
modation this  method  is  most  dramatically  employed  as  a  means  of 
overcoming  the  enormous  accommodative  adjustment  required  to 
bridge  the  refractive  difference  between  aquatic  and  aerial  vision,  as  in 
seals  or  sea-snakes. ^ 

(b)  A  duplicated  ojitical  system  may  be  employed,  a  device  adopted 
by  various  amphibious  Vertebrates  to  overcome  the  large  step  between 
aerial  and  aquatic  vision.  This  is  attained  by  an  optical  asymmetry 
of  the  lens  which  is  pyriform  in  shape  so  that  it  is  emmetropic  in  one 
axis  and  hypermetropic  in  the  other.  Among  Fishes  the  use  of  the 
appropriate  system  is  ensured  in  Anableps  by  the  presence  of  two 
pupils.^  It  will  be  remembered  that  this  fish  swims  in  such  a  way 
that  the  water-line  cuts  the  middle  of  the  cornea  ;  the  upper  pupil, 
subserving  aerial  vision,  admits  a  pencil  of  light  along  the  shorter  axis 
of  the  lens  to  focus  on  the  lower  part  of  the  retina,  the  lower  pupil 
which  is  submerged  is  optically  associated  with  the  long  axis  of  the 
lens  and  the  upper  part  of  the  retina  (Fig.  766).  A  somewhat  analogous 
arrangement  is  seen  in  the  kingfisher,  Alcedo,  which  is  j^rovided  with 
two  fovea",  a  central  for  use  in  aerial  vision,  and  a  second  situated 
in  the  far  temporal  periphery  somewhat  evaginated  in  an  out -pocket 
of  the  sclera.    The  lens  is  egg-shaped  with  its  narrow  end  pointing  to 

1  p.  612.  2  p.  649. 

^  Compare  the  dorsal  and  ventral  compound  eyes  of  the  wliirligig  beetle,  p.  244. 

S.O.— VOL.  I  41 


Figs.  766  to  770. — Static  Accommodative  Devices. 

N 


Fig.   766. — The  eye  of  Anableps. 

Because  of  the  pyriform  shape  of 
the  lens  the  upper  pupil  and  lower 
retina  are  positioned  for  aerial 
vision  (A),  the  lower  pupil  and  upper 
retina  for  aquatic  vision  (W)  (c.f., 
Fig.  385). 


Fig.    767. — The  tubular  eye  of  a  deep- 
sea  fish. 

The  main  retina  is  used  for  near 
vision  with  a  myopic  optical  system 
(N)  ;  the  accessory  retina  for  distance 
vision  with  a  hypermetropic  optical 
system  (D). 


Figs.  768  and   769. — The  ramp-retina. 
Fig.    768.— The    eye    of    the    ray.  Fig.   769. — The  eye  of  the  horse. 

In  each  case  distance  vision  is  subserved  by  rays  striking  the  lower 
(hypermetropic)  part  of  the  retina  {D)  ;  near  vision  is  subserved  by  rays 
striking  the  upper  (myopic)  part  of  the  retma  (N). 


Fig.   770. — The  eye  of  the  fruit  bat. 

Distance  vision  is  subserved  by  retinal  elements  at  the  top  of  a  papilla  (D)  ; 
near  vision  by  elements  in  the  trough  between  two  papillae  (N)  {c.f..  Fig.  581). 


THE   PERCEPTION   OF  FORM  643 

the  temporal  fovea  and  its  long  axis  running  parallel  to  the  palpebral 
fissure  so  that  the  refraction  through  this  axis  is  extremely  myopic  ; 
this  system  is  brought  into  play  for  aquatic  vision  when  the  bird  dives 
under  water  for  its  prey  (Kolmer,  1924).^ 

(c)  An  extraneous  alteration  of  the  02)tical  system  by  the  inter- 
position of  the  nictitating  membrane.  This  is  a  curious  and  unique 
mechanism  seen  in  diving  ducks,  loons  and  auks  whereby  the  third 
eyelid  is  brought  over  the  cornea  when  the  bird  is  immersed  ;  the 
nictitating  membrane  has  a  transparent  window  with  a  high  refrac- 
tivity,  so  that  when  it  is  interposed  in  the  visual  axis  the  already 
powerful  intra-ocular  accommodative  mechanism  is  augmented. 

{d)  A  duplicated  retina  is  a  rare  accommodative  expedient  seen  in 
the  tubular  eyes  of  some  deep-sea  fishes  in  which  the  relatively  enormous 
size  of  the  spherical  lens  precludes  any  effective  accommodative 
adjustment  ^  :  the  princij^al  retina  in  the  axial  position  is  myopic 
compared  with  the  accessory  retina  situated  close  to  the  side  of  the 
lens  (Fig.  767).  In  addition  to  this  static  mechanism  we  shall  see 
presently  that  there  is  a  supplementary  dynamic  component  mediated 
by  a  muscle  of  accommodation.^ 

(e)  A  sloping  ramp-retina  is  a  somewhat  similar  device  whereby 
the  axial  length  of  the  globe  changes  continuously  in  the  vertical 
direction,  being  progressively  further  away  from  the  lens  in  its  superior 
segment.  Such  a  configuration  is  seen  in  some  Selachians  (Raja)  (Fig. 
768)  and  particularly  in  Ungulates  (Franz,  1934).  In  the  horse,  for 
example,  which  has  no  djTiamic  accommodation,  the  axial  retina  which 
is  used  for  forward  regard  is  emmetropic  while  the  upper  portion  of 
the  retina,  used  for  the  near  vision  required  in  grazing,  is  myopic 
(Fig.  769).  A  somewhat  similar  arrangement  is  seen  in  the  ocelli  of 
some  Invertebrates.^ 

(/)  The  corrugated  retina  of  the  larger  bats  (Megachiroptera)  ^ 
results  in  a  considerable  variation  in  the  distance  of  the  receptor 
elements  from  the  optical  centre  depending  on  whether  they  are 
situated  on  the  crests  or  the  sides  of  a  choroidal  papilla  or  in  the  valleys 
between  them  ;  from  the  optical  point  of  view  this  must  ensure  that  the 
images  of  objects  situated  at  varymg  distances  will  be  focused  on  some 
visual  cells  (Fig.  770). 

{g)  An  unusual  length  of  the  receptor  elernents  of  the  retina  will  have 
the  same  optical  effect  for  the  image,  while  yet  remaining  within  the 
receptor  layer,  will  be  able  to  traverse  a  considerable  axial  distance 
corresponding  to  a  relatively  great  movement  of  an  object  in  space. 
An  extreme  length  of  the  visual  elements,  as  is  seen  in  many  deep-sea 
Teleosteans  or  in  nocturnal  geckos  (Fig.  433),  is  doubtless  primarily  an 

1  p.  65.5.  2  p.  323.  3  p.  646. 

«  Fig.  106.  ^  p.  459. 


644 


THE   EYE   IN   EVOLUTION 


adaptation  to  increase  sensitivity  to  light  ^  ;     but 
dative  elasticity  is  thereby  also  rendered  possible. 


some  accommo- 


Dynamic  Devices 

Dynamic  accommodation  involves  one  of  two  expedients — a 
movement  of  the  lens  as  a  whole  or  its  deformation  ;  both  are  brought 
about  by  muscular  activity  and  in  every  case  the  essential  muscles 
involved  are  under  the  control  of  the  oculomotor  nerve.  In  the  first 
case  the  lens  may  either  be  pushed  or  pulled  backwards  or  forwards  ; 
in  the  second  it  can  be  deformed  by  direct  pressure  or  in  an  indirect 
way  through  varying  the  tautness  of  an  elastic  capsule. 

An  accoinmodative  function  has  been  ascribed  to  two  other  devices  on  inore 
questionable  grounds.  It  has  been  claimed  that  the  columns  of  connective  and 
muscle  tissue  traversing  the  thickness  of  the  choroid  of  Birds  may  pull  the 
retina  backwards.^  Such  an  axial  moveinent  of  the  retina  as  an  aid  to  accom- 
modation is,  however,  by  no  means  established.  A  still  more  questionable 
hypothesis  is  that  the  pecten  of  Birds  serves  as  an  adjuvant  to  accommodation.^ 

(a)  A  movemejit  of  the  lens  as  a  wJwle.  This  mechanism  is 
characteristic  of  the  more  primitive  Vertebrates.  The  firm  spherical 
lens  of  high  refractive  index  necessary  for  optical  purposes  in  an 
aquatic  environment  is  obviously  not  easily  susceptible  to  deformation  ; 
this  mechanism  is  therefore  seen  in  C-yclostomes  and  Fishes  and  has 
been  retained  by  Amphibians  ;  it  also  occurs  in  snakes,  the  eyes  of 
which,  as  we  have  remarked,*  are  essentially  primitive  in  most  of  their 
characteristics.    It  is  to  be  noted,  however,  that  in  the  last  an  entirely 

novel  and  distinct  technique  has  been  evolved 
bearing  no  relation  to  the  ichthyopsidan  plan. 
If  the  lens  is  moved  backwards  the  eye 
becomes  hypermetropic  and  vision  is  ad- 
justed for  distant  objects  (negative  accom- 
modation) ;  this  is  characteristic  of 
Cyclostomes  and  Teleosteans.  If  the  lens  is 
moved  forwards  the  eye  is  rendered  myopic 
and  accommodation  is  attained  for  near 
vision  ;  this  is  seen  in  Selachians  and 
Amphibians  ;  the  same  direction  of  move- 
ment is  also  seen  in  snakes. 

(i)  A  backward  ynoveynent  of  the  lens 
induced  by  corneal  jyressure.  This  mechanism 
is  seen  only  in  the  most  primitive  of  Verte- 
brates— the  CYCLOSTOMES  ;  to  these  it  is 
unique  and  an  intra-ocular  accommodative 


Fig 


1 7 1 . — Accommodation 
IN  Cyclostomes. 

N,  the  eye  adjusted  for 
near  vision  ;  D,  the  eye 
adjusted  for  distance  vision. 
The  cornealis  muscle,  CM, 
pulls  the  cornea  backwards 
which  in  turn  pushes  the 
lens  nearer  the  retina. 


pp.  305,  364. 
p.  416. 


p.  404. 
p.  383. 


THE   PERCEPTION   OF   FORM 


645 


mechanism  is  lacking  (Fig.  771).  In  the  lamprey  the  cornealis  muscle  ^ 
which  lies  outside  the  orbit  and  is  inserted  into  the  dermal  part  of  the 
cornea,  draws  the  cornea  taut  as  it  contracts,  flattens  it  and  thus  presses 
the  lens,  which  lies  in  contact  with  this  tissue,  backwards  to  approach 
the  retina.    It  may  be  that  a  contraction  of  the  extra-ocular  muscles 

Figs.  772  to  776. — Accommodation  in  Teleosts. 


Fig. 


772. — A  cliange  in  position  of  the  lens  ;    in  relaxation  for  near,  n,  and 
in  accommodation  for  distance  vision,  d. 


Fig.   773.  Fig.   774. 

Figs.  773  and  774. — The  left  eye  of  the  sea-bass,  Serranus  cabriUa  (after  Beer). 

Showing  the  aphakic  area  in  the  pupil  in  which  can  be  seen  the  inverted 
retinal  image  of  a  gas  flame  situated  in  the  temporal  jDai't  of  the  eye.  Fig.  773, 
at  rest  ;    Fig.  774,  in  active  accommodation. 


Fig. 


Fig.  776. 


Figs.    77")    and    776. — The    left   eye   of  the   Ijlenny,    Bhnniiis   sanguinolentis 

(after  Beer). 

Fig.  775,  at  rest  ;    Fig.   776,  in  active  accommodation  (seen  from  above 
the  fish). 


which  jacket  the  globe  has  the  opposite  effect  of  elongating  it  to  aid  the 
relaxation  of  accommodation  ;  but  this  is  conjectural.  The  spherical 
lens,  wedged  between  the  cornea  in  front,  the  relatively  solid  vitreous 
behind  and  the  immol;)ile  iris  at  the  sides,  has  no  suspensory  apparatus. 
This    mechanism   of  accommodation   is    both   simple    and   effective, 

1  p.  271. 


646  THE   EYE   IN   EVOLUTION 

providing  accommodation  for  distant  objects  and  giving  the 
normally  myopic  eye  a  fairly  high  degree  of  hypermetropia  ;  Franz 
(1934)  claimed  that  the  extraordinarily  wide  range  of  accommodation 
from  +  20  to  —  20  D  is  thus  rendered  available. 

(ii)  A  backward  {and  sideways)  movement  of  the  lens  induced  by 
direct  muscular  action  as  an  accommodative  mechanism  for  distant 
vision  is  unique  to  teleostean  fishes  among  which  it  is  of  general 
occurrence,  although  it  is  absent  or  ineffective  in  very  small-eyed 
forms  which  have  a  relatively  large  lens.  The  classical  view  put 
forward  by  Beer  (1894)  and  confirmed  by  most  authors  (Franz,  1905-31  ; 
Header,  1936  ;  Rochon-Duvigneaud,  1943)  is  the  following  (Fig.  772). 
As  in  the  lamprey,  the  spherical  lens  normally  approximates  the  cornea, 
suspended  naso-dorsally  by  a  zonular  ligament  on  which  it  can  swing 
pendulum-like  backwards  and  forwards.  A  backward  movement  is 
brought  about  by  the  retractor  lentis  muscle  (the  campanula  of  Haller), 
a  small  ectodermal  muscle  situated  naso- vent  rally  derived  from  the 
ectoderm  at  the  borders  of  the  falciform  process. ^  It  is  to  be  noted 
that  in  the  act  of  accommodation  the  lens  moves  as  much  temporally 
(towards  the  tail)  as  backward  into  the  eye,  if  not  more  so,  thus  moving 
the  image  sideways  across  the  retina  ;  by  this  inovement  the  image 
will  leave  the  temporal  fovea  (when  one  is  present)  which  is  used  in  the 
state  of  relaxation  for  convergence  upon  near  objects  (Figs.  773-6). 

While  this  is  the  most  generally  accepted  explanation  of  teleostean 
accommodation,  an  entirely  different  view  has  been  put  forward  by 
Bourguignon  and  Verrier  (1930).  Beer  ( 1 894)  had  found  that  on  electric 
stimulation  the  campanular  muscle  contracted  and  pulled  the  lens 
backwards.  The  former  authors  failed  to  substantiate  this  ;  on  the 
contrary,  on  electrical  stimulation  they  foimd  in  a  number  of  species 
(the  roach,  the  tench,  the  goldfish,  the  barbel  and  the  chub)  that  a 
deformation  of  the  globe  was  produced  by  the  tensor  choroideae  muscle 
which  encircles  the  eye  at  the  corneo-scleral  junction,  resulting  in  a 
lengthening  of  the  antero -posterior  axis.  If  the  average  teleostean  eye 
is  hypermetropic  ^  a  retraction  of  the  lens  would,  of  course,  increase 
the  optical  error  and  have  the  reverse  of  an  accommodating  effect  ; 
the  myopia  induced  by  an  increase  in  the  antero -posterior  axis  would 
be  effective  in  accommodating  for  near  vision.  On  the  other  hand,  if, 
as  Beer  claimed,  the  normal  refraction  is  myopic,  a  retraction  of  the 
lens  would  ensure  good  distance  vision  at  the  expenditure  of  muscular 
effort.  Further  experimental  exploration  of  this  mechanism  in 
teleostean  fish  is  required  to  clear  up  the  position  but  it  is  to  be 
remembered  that  with  the  spherical  lens  and  its  dense  central  core, 

*  p.  302.  Seen  also  in  a  well-develoiaed  form  in  tubular  ej^es  with  their  enormous 
lenses  (Fig.  380). 
-  p.  638. 


THE   PERCEPTION   OF   FORM 


647 


the  depth  of  focus  of  the  eyes  of  Fishes  is  so  great  as  not  to  demand 
much  from  accommodation. 

In  Holosteans  the  lens  is  slung  on  a  dorsal  suspensory  ligament  and  an 
ectodermal  lenticular  muscle  is  present  apparently  analogoiis  to  the  campanula  ; 
its  action,  however,  is  unknowTi. 

(iii)  A  forward  jnovement  of  the  lens,  rendering  the  eye  more  myopic 
to  accommodate  for  near  objects  is  brought  about  by  two  separate 
mechanisms  in  the  vertebrate  jih^'him — bj-  the  direct  action  of  a  sj^ecial 
muscle  in  Selachians  (and  possibly  Holocephalians)  and  Amphibians, 
and  indirectly  by  increasing  the  pressure  in  the  vitreous  cavity  as  a 
result  of  contraction  of  the  sphincter  of  the 
pupil,  a  mechanism  seen  in  snakes. 

In  SELACHIANS  the  lens  is  suspended  as 
in  Teleosteans  by  a  dorsal  suspensory  liga- 
ment, and  is  said  to  be  swung  forwards  by 
the  action  of  the  smooth  (ectodermal)  muscle 
fibres  in  the  ventral  ciliary  papilla  ^  (Fig. 
777).  Among  Selachians,  Franz  (1905-31) 
demonstrated  such  a  movement  in  the  rays, 
Raja  asterias,  and  Torpedo,  doubtfully  in  the 
dogfish,  Scyllium,  but  not  in  the  dogfish, 
Mustelus  ;  in  some  species  he  found  a  wide 
range  of  accommodation  (15  to  20  D).  It  is 
to  be  remembered,  however,  that  neither 
Beer  (1894)  nor  v.  Hess  (1912)  obtained  any 
such  response  to  electrical  stimulation,  while 

Verrier  (1930)  and  Rochon-Duvigneaud  (1943)  found  that  the  muscular 
fibres  in  the  ciliary  papilla  were  scanty  or  absent  ;  these  workers 
therefore  concluded  that  the  accommodation  of  the  Selachians  which 
they  investigated  was  minimal  or  lacking. 

In  those  amphibians  which  have  accommodation,  the  amplitude 
is  much  poorer^ — never  more  than  4  or  5  D  (Beer,  1898) — an  amount 
quite  useless  in  maintaining  good  visual  acuity  in  both  an  aerial  and 
an  aquatic  environment.  Our  knowledge  of  this  subject,  however,  is 
again  meagre  and  somewhat  conflicting.  Beer  (1898)  advanced  the 
theory  that  accommodation  for  near  vision  was  attained  through  the 
contraction  of  the  ciliary  muscles  compressing  the  vitreous  body  which 
in  turn  thrust  forwards  the  lens.  His  experimental  techniques  and 
conclusions,  however,  have  been  challenged,  particularly  by  v.  Hess 
(1912)  on  the  basis  of  his  findings  with  direct  electrical  stimulation.  It 
is  true  that  in  the  small  eyes  of  Amphibians  with  their  short  focal 
distance,  the  length  of  the  receptor  elements  would  allow  the  image 

1  p.  285. 


Fig.    777. — Accommodation 
IN  Selachians. 

The  ej-e  in  the  normal 
condition  of  rest  {D,  distance 
vision).  The  eye  in  accom- 
modation for  near  vision  (N) 
with  the  lens  moved  for- 
wards. 


648 


THE   EYE   IN   EVOLUTION 


of  objects  at  a  considerable  range  of  distances  from  the  eye  to  fall 
upon  the  visual  layer  so  that  an  efficient  and  active  mechanism  may 
not  be  required.  But  it  would  seem  that  in  anurans  the  lens  is  pulled 
forward  indirectly  by  two  protractor  lentis  muscles,  a  dorsal  and  a 
ventral.  Unlike  the  analogous  muscles  of  Fishes,  they  are  mesodermal 
in  origin  although  still  smooth  in  type.  They  arise  at  the  margin  of 
the  cornea,  traverse  the  iris  and  are  inserted  into  the  large  median 
ciliary  processes  ;  these  they  pull  forwards  thus  drawing  the  lens  in 
the  same  direction  through  its  anchorage  by  the  zonule.  In  urodeles 
a  single  ventral  protractor  lentis  muscle  inserted  into  the  single  mid- 
ventral  ciliary  process  acts  similarly,  and  less 
effectively. 

In  OPHIDIANS  the  mechanism  for  moving 
the  lens  forwards  is  entirely  different  (Beer, 
1898  ;  Leplat,  1921  ;  Kallmann,  1932  ; 
Michel,  1932-33).  The  interpretation  sug- 
gested by  Beer  (1898)  is  as  follows  (Fig.  778). 
In  snakes  we  have  already  seen  that  the 
ciliary  (mesodermal)  musculature  has 
migrated  to  the  iris  around  the  root  of  which 
it  forms  a  sphincteric  ring  ;  when  these 
fibres  contract  they  constrict  the  globe  at 
the  corneo -scleral  junction,  thus  increasing 
the  pressure  in  the  vitreous  chamber  so  that 
the  lens  is  pushed  bodily  forward  into  the 
pupillary  aperture,  sometimes  as  far  as  half- 
way towards  the  cornea.  At  the  same  time 
the  constriction  in  the  circumference  of  the  globe  in  the  ciliary  region 
may  be  compensated  by  a  slight  forward  bulging  of  the  cornea.  Beer 
(1898)  demonstrated  this  indirect  pressure -effect  through  the  vitreous 
by  removing  the  posterior  half  of  the  globe  ;  electrical  stimulation  of 
the  ciliary  muscle  then  led  to  a  backward  displacement  of  the  lens.  In 
the  intact  eye  an  accommodative  range  sufficient  to  overcome  their  +  8 
or  -f  10  D  of  hypermetropia  is  readily  available  to  snakes  (up  to 
—  17  D)  (Kallmann,  1932).  The  mechanism  resembles  that  seen  in 
Cephalopods.^ 

In  tree-snakes  with  a  horizontal  slit-shaped  puj^il,  a  nasal  aphakic  area 
and  a  temporal  fovea  ^  the  lens  moves  nasally  as  well  as  forwards  ;  this  has 
the  oj:»tical  effect  of  directing  incident  light  upon  the  fovea  and  corresponds  to 
the  nasal  movemeTit  of  the  lens  of  those  teleostean  Fishes  with  a  partially 
aphakic  pnpil  when  accommodation  is  relaxed  for  near  objects.^ 

In  terrestrial  snakes  the  main  effector  of  the  accommodative  effort 
is  the  mesodermal  sphincter  at  the  root  of  the  iris  ;   the  action  of  the 

1  p.  590.  2  p_  388.  3  p    304. 


Fig.    778. — Accommodation 

IN  Snakes. 

The  eye  in  relaxation  for 
distance  vision,  D  ;  the 
condition  in  accommoda- 
tion for  near  vision,  N.  Note 
that  both  the  lens  and  the 
cornea  have  moved  forward. 


THE   PERCEPTION   OF   FORM  649 

remaining  musculature  of  the  iris  is  insignificant  and  the  relatively- 
firm  lens  is  pushed  forwards  with  little  or  no  change  in  shape.  In 
water-snakes  a  supplementary  mechanism  exists,  for  in  the  transference 
from  aquatic  to  aerial  vision  such  an  animal  requires  an  immense 
range  of  accommodation.  In  the  European  water-snake,  Natrix 
(Tropidonottis)  tessellatus,  Beer  (1898)  found  that  the  lens  was  unusually 
soft  and  readily  mouldable,  and  it  would  appear  that  in  accommo- 
dation the  powerful  sphincter  muscle  of  the  pupil  moulds  the  anterior 
surface  into  a  conical  shape  as  it  is  thrust  forward  through  the  pupil — 
a  mechanism  common  to  other  reptiles,  particularly  the  turtle  (Figs. 
783-5). 1  In  this  case  the  lens  is  thus  both  displaced  and  deformed. 
Aquatic  snakes  such  as  the  marine  cobras  (Hydrophinse)  and  river  snakes 
(Homalopsinse),  as  we  have  seen,  make  use  of  a  stenopoeic  pupil  when 
the  eyes  are  out  of  water  to  achieve  the  necessary  accommodation,  a 
device  also  seen  in  the  seals. ^ 

(b)  A  deformation  of  the  lens  may  be  effected  by  direct  muscular 
pressure  upon  it  or  by  alteration  in  the  tension  of  an  elastic  capsule. 

(i)  A  direct  squeezing  of  the  2)eri2)hery  of  the  lens  by  the  ciliary  body 
is  a  mechanism  peculiar  to  Sauropsidans  (except  snakes)  ;  it  is  an 
entirely  original  and  very  effective  method  adopted  by  this  composite 
group  bearing  no  resemblance  to  the  accommodative  devices  seen  in 
Fishes  or  Amphibians.  For  this  reason  a  number  of  novel  anatomical 
features  is  introduced  into  the  sauropsidan  eye  by  virtue  of  which  a 
high  degree  of  accommodative  efficiency  is  reached.  It  is  significant 
that  the  smooth  muscle  fibres  of  the  Ichthyopsida  give  place  to  striated 
fibres  in  Sauropsida  and  a  large  muscle-mass  is  developed  divided 
sometimes  into  two,  sometimes  three  functional  segments.  Actual 
contact  between  the  lens  and  the  ciliary  body  is,  of  course,  necessary  ; 
for  this  purpose  a  large  annular  pad  has  Ijeen  developed  at  the  periphery 
of  the  lens  extending  it  equatorially,  and  the  ciliary  body,  provided 
with  well-developed  ciliary  processes,  is  pushed  axially  by  a  deep 
corneo-scleral  sulcus,  the  deformation  of  the  globe  being  maintained 
by  a  concave  ring  of  dove -tailed  ossicles  (lacking  only  in  Crocodilians 
— and  snakes).  In  addition,  in  order  to  facilitate  its  deformation  the 
lens  itself  is  unusually  soft  so  that  it  is  readily  mouldable  (Figs.  779  to 
782). 

The  optical  mechanism  of  accommodation  dej^ends  essentially  on 
a  deformation  of  the  lens  :  squeezed  laterally  by  the  ciliary  processes, 
steadied  posteriorly  by  the  vitreous  body,  and  with  the  peripheral  part 
of  the  anterior  surface  restrained  by  the  contraction  of  the  musculature 
of  the  iris,  the  central  area  of  the  anterior  surface  is  bulged  forwards 
in  a  lenticonus  thus  increasing  the  refractivity  of  the  lens  and  accom- 

'  p.  652.  2  p_  641 


650 


THE   EYE   IN  EVOLUTION 


modating  for  near  vision.  At  the  same  time  in  lizards  and  Birds  the 
deepening  of  the  corneo -scleral  surface  deforms  the  cornea,  producing 
a  peripheral  flattening  and  making  it  more  convex  at  the  apex  and 
thus  augmenting  the  increase  in  total  refractivity  (Kahmann,  1932-33)  ; 
this  mechanism  is  absent  in  diving  birds  in  which  it  would  be  ineffective 
since  the  corneal  refraction  is  eliminated  under  water. ^     The  entire 


Fig.  779. — Accommodation  in  Saukopsida. 

The  condition  of  relaxation  for  distance  vision,  D,  and  accommodation  for 

near  vision,  N. 

Figs.  780  to  782. — To  Illustrate  the  Effect  of  the  Annular  Pad  in 
Transmitting  an  Evenly  Distributed  Pressure  to  the  Lens  by 
the  Ciliary  Body. 


Fig.  780,  represents  a  balloon  filled  with  air.  If  it  is  compressed  directly  by 
a  relatively  small  body  such  as  the  fist  it  is  deformed  (Fig.  781)  ;  if,  however, 
the  iinpact  of  the  fist  is  distributed  regularly  by  means  of  an  open  hand,  a 
lenticular  shape  is  ensured  (Fig.  782). 


process  depends  on  lateral  pressure  by  the  ciliary  musculature  and 
pressure  from  the  vitreous  plays  no  active  role  apart  from  restraining 
any  change  in  the  posterior  surface  of  the  lens  :  in  contrast  to  the 
events  in  the  eye  of  the  snake,  the  process  takes  place  without  change 
if  the  posterior  segment  of  the  eye  is  removed  and  the  vitreous  is 
eliminated  (v.  Hess,  1912). 

The  factor  determining  the  act  of  accommodation  is  essentially  the  ciliary 
muscle — a  well -developed  striated  muscle  running  meridionally,  a  descendant 
from  the  minute  tensor  choroidese  of  Fishes,  but  inserted  not  into  the  choroid 

1  p.  276. 


THE   PERCEPTION   OF   FORM  651 

but  into  the  ciliary  body  itself.  In  most  Reptiles  it  is  a  simple  strip  running 
from  the  corneal  margin  to  the  base-plate  of  the  orbicular  zone  of  the  ciliary 
body,  but  in  lizards  and  in  Birds  (except  diving  birds)  it  is  divided  into  two — 
the  anterior  part,  Crampton's  muscle,  strung  like  a  bow-string  running  between 
the  periphery  of  the  cornea  and  the  sclera,  presumably  deforms  the  cornea  ; 
the  posterior  section,  Briicke's  muscle,  thrusts  the  ciliary  body  axially  on 
contraction  (Fig.  499).  In  some  Birds,  Briicke's  muscle  is  still  further  sub- 
divided, its  anterior  portion  being  known  as  Miiller's  muscle.^ 

A  further  muscle  is  seen  in  Clielonians  and  lizards — and  in  ( ?)  the  pigeon, 
Columba  :  the  transversalis  muscle,  a  strip  of  striated  muscle  originating 
ventrally  in  the  connective  tissue  between  the  ciliary  body  and  the  sclera  and 
inserted  into  the  zonular  fibres.  Its  action  is  to  pull  the  lens  nasally  thus  helping 
binocvilar  vision  on  accommodation  and  convergence.  In  a  sense  it  seems 
comparable  to  the  ventral  protractor  lentis  of  Amphibians  although  not  homo- 
logous with  it,  and  is  concerned  with  binocular  vision  rather  than  with 
accommodation.  Such  a  nasal  movement  is  also  aided,  particularly  in  Birds, 
by  the  asymmetry  of  the  ciliary  body  and  the  anterior  segment  of  the  globe. 

CHELONiANS  have  the  softest  and  most  readily  mouldable  lenses 
amongst  all  Vertebrates  ;  accommodation  in  these  animals  is  effected 
by  the  formation  of  an  anterior  lenticonus  by  the  action  of  the  powerful 
sphincter  pupilla?  (Beer.  1898  ;  v.  Pflugk,  1908  ;  v.  Hess,  1909-12)  ;  in 
these  reptiles  the  annular  pad  is  therefore  small  and  in  tortoises  and 
terrapins  the  ciliary  musculature  relatively  weak  (Figs.  783-5).  Sea- 
turtles  have  little  use  for  accommodation  but  the  undoubted  prowess 
of  terrestrial  forms  in  catching  insects  demonstrates  that  their  range 
of  accommodation  must  be  good. 

The  accommodation  of  crocodilians  has  not  been  thoroughly 
explored  ;  Abelsdorjff  (1898),  however,  concluded  that  it  extended  to 
a  range  of  8  D.  Similarly  S-pheiiodon  with  its  weak  ciliary  muscle  can 
only  accommodate  little — if  at  all  ;  the  greatest  effect  would  seem 
probably,  as  in  turtles,  to  come  from  the  deforming  effect  of  the 
sphincter  of  the  iris  on  the  anterior  surface  of  the  lens. 

LIZARDS,  on  the  other  hand,  have  good  accommodation,  their 
excellent  mechanism  being  aided  in  some  cases  (nocturnal  geckos)  by 
the  stenopoeic  contracted  pupil.  Electrical  stimulation  has  been  found 
to  increase  the  refraction  considerably — by  15  D  in  Iguana,  10  D  in 
Lacerta  (v.  Hess,  1909-12). 

In  BIRDS  the  accommodative  mechanism  is  superb,  the  most 
efficient,  indeed,  amongst  Vertebrates,  and  in  these,  as  in  turtles,  the 
formation  of  an  anterior  lenticonus  is  aided  considerably  by  the 
powerful  contraction  of  the  sphincter  muscle  of  the  pupil  which  acts 
as  a  "  compressor  lentis  "  (v.  Hess,  1910-12).  In  the  owl,  Bubo,  the 
range  is  small  (probably  some  4  D),  in  the  nocturnal  predators,  2  to  3  D 
and  exceptionally  4  D,  in  the  average  passerine  bird  some  8  to  12  D,  and 
in  the  predatory  birds  (hawks,  eagles,  etc.)  still  greater.     The  highest 

1  p.  406. 


652  THE   EYE   IN   EVOLUTION 

range  is  seen  in  aquatic  birds  such  as  the  cormorant,  Phalacrocorax ;  in 
it  the  lens  is  very  soft  and  plastic,  the  sphincter  of  the  iris  extremely 
powerful,  and  the  compression  and  moulding  of  the  lens  to  form  a 
marked  lenticonus  has  been  said  to  provide  an  accommodative  excur- 
sion of  up  to  50  D  in  vision  under  water  (v.  Hess,  1912). 


Figs.  783  to  785. — Accommodation  in  Chelonians. 

D 


Fig.  783. 


Fig.   784. 


Fig.   785. 


The  lens  at  rest  for  distance  vision  (D,  Fig.  783  ;    Fig.  784)  ;  deformed 
into  an  anterior  lenticonus  for  near  vision  (A'^,  Fig.  783  ;    Fig.  785). 


(ii)  A  deformation  of  the  lens  by  a  variatiori  in  the  elasticity  of  the 
capsule  is  a  mechanism  peculiar  to  mammals  and  has  no  analogy 
elsewhere  in  the  vertebrate  phylum.  According  to  the  most  generally 
accepted  hypothesis  of  Helmholtz  (1855)  and  Fincham  (1925),  the 
plastic  lens  retains  its  characteristically  flattened  shape  owing  to  the 
moulding  effect  of  the  elastic  capsule  stretched  by  the  pull  of  the 
zonule.  The  capsule  varies  considerably  in  thickness,  being  thinnest 
at  the  posterior  and  anterior  poles.  When  the  ciliary  muscle  contracts 
on  accommodation,  the  ciliary  body  approaches  the  lens,  the  zonule 
slackens  and  the  capsule  relaxes  allowing  the  plastic  lens  to  assume  a 
more  spherical  shape— the  shape,  in  fact,  which  it  assumes  when  removed 
from  the  eye.  Since  the  posterior  pole  is  restrained  by  the  support  of 
the  vitreous  body  and  the  capsule  is  relatively  thick  and  tough  in  the 
peripheral  region,  the  greatest  bulging  occurs  in  the  form  of  a  conus- 


THE   PERCEPTION   OF   FORM 

like  projection  on  the  anterior  surface,  thus  increasing  its  refractivity 
in  accommodation  for  near  objects  (Figs.  786  to  790). 

Compared  with  the  sauropsidan  plan,  such  a  mechanism  is 
inefficient ;  with  a  large  lens  much  deformation  cannot  occur,  and  if  the 
lens  loses  its  plasticity  any  deformation  is  impossible.  In  a  small  eye 
with  a  large  lens  accommodation  is  therefore  negligible  and  when  the 


653 


Fig.   786. — Accommodatiox  in  Mammals. 

The   condition    of  relaxation    for   distance    vision,    D  ;     and   accommodation 

for  near  vision,  A'. 


Figs.   787  to  790. — The  Lexs  Capsule  in  Mammals. 


Fig.   788. — Capuchin  monkey. 


Fig.   789.— Sheep. 


Fig.   790.— Man. 


Diagrams,   in  which  the  thickness  of  the  capsule  is  greatly  magnified, 
showing  the  relative  thicknesses  in  different  regions  (E.  F.  Fincham). 


lens  becomes  sclerosed  with  age  (as  in  man)  it  gradually  fails.  On  the 
whole  the  efficiency  of  mammalian  accommodation  is  therefore  poor. 
In  most  of  the  lower  Mammals  the  ciliary  muscle  is  vestigial  and  some- 
times absent  ;  the  more  primitive  Mammals  have  therefore  no  accom- 
modation. Among  RODENTS,  accommodation  is  known  only  among 
squirrels  (Sciurida^)  and  in  them  the  range  is  insignificant  (1  to  1-5  D). 
No  UNGULATE  appears  to  have  any  accommodation,  and  the  range  in 
CARNIVORES  is  small  (1  to  35  D)  ^  with  the  excejition  of  the  otter, 

1  The  range  of  accommodation  in  the  dog  has  been  reported  as  TO  D,  in  the 
wolf  as  2-75  D  (v.  Hess  and  Heine,  1898),  in  the  cat  as  varying  from  T75  D  (v.  Hess 
and  Heine,  1898)  to  3  D  (Marg  et  al.,  1954-5)  or  3-5  D  (Hartridge  and  Yamado,  1922). 


654  THE   EYE   IN   EVOLUTION 

Lutra  ;  this  animal  has  a  well-developed  ciliary  muscle  and,  in  addition, 
a  powerful  sphincter  of  the  iris  which  appears  to  aid  the  deformation 
of  the  lens  after  the  manner  of  Sauropsidans  so  that  its  accommodative 
range  can  cope  with  vision  in  air  and  also  under  water.  In  air  the 
animal  is  emmetropic  and  under  water  its  visual  acuity  is  sufficiently 
good  to  allow  it  to  capture  its  prey  with  considerable  agility,  primates 
as  a  class  possess  the  most  effective  range  before  senescence  sets  in 
(up  to  10  D  in  the  ape  ;  up  to  20  D  in  the  human  infant,  decreasing 
to  10  D  at  21  years,  thereafter  rapidly  diminishing). 

A  resume  of  the  occurrence  and  configuration  of  the  ciliary  musculature 
may  be  useful  at  this  stage.  It  is,  of  course,  absent  when  the  ciliary  body  as 
such  is  absent  or  reduced  to  a  flat  ciliary  zone  (Cyclostomes,  the  coelacanth, 
Dipnoans,  Chondrosteans  and  Csecilians)  ;  it  is  also  absent  in  Monotremes 
and  is  vestigial  in  Rodents,  Insectivora  and  Sirenia.  The  muscle  is  plain  in 
Fishes,  Amphibians  and  Mammals  ;  striated  in  Reptiles  and  Birds.  It  is 
represented  by  a  small  tensor  choroide^  in  Teleosts  and  Amphibians 
(discontinuous  in  two  strips  above  and  below).  This  becomes  a  ciliary 
MUSCLE  in  Reptiles,  Birds  and  Mammals.  Accessory  musculature  is  re- 
presented by  a  PROTRACTOR  LENTis  in  Selachians  (ectodermal)  and  Amphibians 
except  Csecilians  (mesodermal  ;  dorsal  and  ventral  in  Anurans,  ventral  in 
Urodeles)  ;  a  retractor  lentis  is  present  in  Teleosts  (except  eels)  and  Holo- 
steans.  A  transversalis  muscle  is  found  in  Chelonians,  lizards,  (?)  Sphenodon 
and  (?)  the  pigeon.  The  segmentation  of  the  ciliary  muscle  into  Crampton's  and 
Briicke's  muscle  in  most  Reptiles  and,  in  addition,  into  Miiller's  muscle  in 
Birds  has  already  been  noted.  In  snakes  the  ciliary  muscle  has  migrated  to 
the  iris. 

Among  all  the  activities  of  Vertebrates,  the  needs  of  the  amphibious  aninial 
which  reqviires  to  see  both  under  water  and  in  the  air  put  the  greatest  strain 
upon  accommodation,  a  circumstance  which  applies  both  to  fish  which  emerge 
into  the  air  and  to  land  animals  which  go  down  into  the  water.  The  elimination 
of  the  corneal  refraction  when  it  is  immersed  in  water  and  its  optical  value  in 
air  make  the  same  eye  strongly  hypermetropic  in  the  first  medium  and  strongly 
myopic  in  the  second.  So  difficult  is  this  optical  transition  that  it  is  not 
attempted  by  many  forms.  Thus  certain  fishes  such  as  the  climbing  perch, 
Anabas,  which  emerges  on  land  crawling  with  the  aid  of  the  spines  on  the  gill- 
covers  and  on  the  anal  fin,  may  be  without  effective  accommodation  or  any 
other  detectable  device  for  altering  their  relatively  emmetropic  state  in  water  ; 
in  these  vision  in  air  must  be  so  myopic  as  to  serve  merely  for  the  detection  of 
light  and  shadow.  Other  fish  such  as  the  Indian  mullet,  Mugil  corsula,  have  eyes 
of  the  type  designed  for  aerial  vision  with  a  lenticular-shaped  lens  ;  this  fish 
swims  feeding  on  the  surface  with  the  eyes  out  of  water  and  its  visual  acuity 
beneath  the  water  must  be  relatively  poor,  a  consideration  which  applies  also 
to  such  semi-aquatic  animals  as  the  ranid  frogs,  the  crocodiles  and  the  hippo- 
potamus. Conversely,  the  penguins  (unlike  most  other  birds)  are  very  myopic 
in  air  ;  while  Sirenians,  without  accommodation  and  with  a  slight  myopia  in 
air,  appear  to  have  so  little  visual  acuity  in  either  medium  that  vision  can  play 
only  a  small  part  in  their  activities. 

WTiere  the  attempt  is  made  to  bridge  over  the  optical  transition  demanded 
by  vision  in  two  media,  this  may  be  accomplished  in  several  ways.    In  the  first 


THE   PERCEPTION   OF   FORM  665 

place,  a  superlative  degree  of  accommodation  may  be  provided.  This  is  seen 
in  a  fish  such  as  the  mud-skipper,  Periophthaltnus,  which  can  become  emmetropic 
in  air  using  a  maximal  degree  of  accommodation.  Among  land  animals  a  similar 
excellent  accommodation  may  allow  the  nevitralization  of  the  hj'permetropia 
which  supervenes  on  immersion.  This  applies  mainly  to  representatives  of 
the  Sauropsida  which  employ  a  well-developed  ciliary  muscle  together  with  a 
hypertrophied  sphincter  mviscle  of  the  iris  to  mould  an  unusually  soft  lens — 
turtles,  water-snakes  and  birds  such  as  the  cormorant.  One  Carnivore,  the 
otter,  Lutra,  is  capable  of  a  similar  accomplishment. 

Apart  from  this  exceptionally  high  degree  of  accommodation,  several 
adaptive  expedients  which  we  have  already  mentioned,  all  of  them  both  interest- 
ing and  ingenious,  may  be  summarized  : 

(a)  The  provision  of  two  optical  systems  by  the  use  of  one  or  other  of  the 
two  main  axes  of  a  pyriform  lens  as  is  seen  in  Anahleps  with  its  two  pupils,  or 
in  the  kingfisher,  Alcedo,  with  its  two  fovefe.^ 

(6)  Contraction  of  the  pupil  either  to  a  stenopoeic  opening,  as  is  seen  in  the 
sea-snakes  (Hydrophinse)  or  a  stenopoeic  slit,  as  in  the  seals  (Phocidse).^ 

(c)  The  incorporation  of  the  nictitating  membrane  into  the  optical  system 
when  the  eye  is  immersed,  as  in  diving  dvicks,  loons  and  auks.' 

Other  optical  factors.  Apart  from  the  refractive  error  and  its 
susceptibility  to  adjustment,  the  sharpness  of  the  retinal  image  is 
influenced  by  other  optical  factors.  One  of  the  most  important  of 
these  is  the  size  of  the  eye,  a  consideration  which  essentially  deter- 
mines the  size  of  the  image,  and  therefore  the  degree  of  its  resolution  ; 
since  the  size  of  the  visual  elements  is  relatively  constant,  a  larger 
image  stimulates  more  of  them,  thus  allowing  a  finer  analysis.  On 
the  whole,  therefore,  those  animals  with  relatively  large  eyes,  such  as 
Birds,  have  the  higher  visual  acuity.  In  the  same  way,  a  flattening 
of  the  lens  and  an  approach  of  this  tissue  towards  the  cornea  in- 
crease the  distance  between  the  nodal  point  of  the  dioptric  system 
and  the  retina  and  again  increase  the  size  of  the  image  (Figs.  747-8)  ; 
this  expedient  is  well  seen  in  the  eyes  of  Birds  and  Primates.  The 
small  anterior  segment  with  the  forward  position  of  the  lens  and  the 
large  globular  posterior  segment  so  typical  of  diurnal  birds  are 
excellent  examples  of  this  adaptation  (Fig.  749).  Finally,  an  efficient 
pupillary  stop  to  eliminate  aberrations  by  the  peripheral  part  of 
the  lens  is  of  value  in  increasing  the  resolution  of  the  image  so  long 
as  excessive  contraction  does  not  diminish  the  visual  acuity  by  cutting 
down  too  drastically  the  entering  light. 

It  is  to  be  noted  that  when  the  lens  is  spherical,  the  aberrations  developed 
in  the  periphery  are  less  important.  This  is  seen  particularly  in  Fishes  in  which 
the  refraction  of  the  cornea  is  eliminated,  the  lens  is  spherical  with  a  graduated 
index  of  refraction,  and  the  retina  practically  concentric  with  the  lens 
(Matthiessen,  1886-93).  In  such  an  eye  the  optical  system  is  practically  aplanatic 
and  panoramic,  and  a  pupillary  stop  is  not  needed — and  is  seldom  provided. 

1  p.  641.  2  p_  641.  3  p_  643. 


656  THE   EYE   IN   EVOLUTION 

A  specific  device  developed  by  certain  species  in  order  to  increase 
the  visual  acuity  is  the  provision  of  intra-ocular  filters.  These 
increase  the  sharpness  of  the  image  in  the  same  way  as  tinted  spectacles 
do  when  appropriately  chosen  :  they  diminish  chromatic  aberration 
largely  by  eliminating  some  of  the  blue  and  most  of  the  violet  rays, 
while  at  the  same  time  they  cut  down  the  glare  and  dazzle  caused  by 
irregularly  scattered  light  from  a  bright  sky.  As  would  be  expected 
this  device  is  largely  confined  to  diurnal  Vertebrates  and  is  not  typical 
of  nocturnal  types  to  which  the  transmission  of  every  available  ray 
is  of  importance  (Walls  and  Judd,  1933). 

For  these  optical  purposes  a  yellow  filter  is  the  most  efficient  and 
is  the  most  widespread  optical  device  found  in  the  vertebrate  eye.  Thus 
a  yellow  cornea  is  found  among  Holosteans  in  Amia,  and  in  a  few 
highly  diurnal  Teleosteans  such  as  the  carp,  Cyjirinus,  and  the  pike, 
Esox  ;  a  yellow  lens  is  found  in  the  lampreys  (except  the  nocturnal 
Geotria),  in  the  diurnal  gecko,  Lygodactylus,  in  some  diurnal  snakes 
{Mal'polon,  DryojjJiis,  etc.),  in  the  tree-shrew,  Tujmia,  among  Insecti- 
vores,  and  in  most  squirrels  (Sciuridae,  except  the  nocturnal  flying 
squirrels)  ;  a  yellow  pigment  is  found  in  the  central  area  of  the  retina, 
possibly  in  the  chameleon  and  certainly  in  man,  converting  it  into  a 
macula  lutea  ;  and  yellow  oil-droplets  are  found  in  the  cones  of  the 
frog,  Sphenodon,  the  turtles,  diurnal  lizards  and  birds.  Finally,  as  was 
originally  pointed  out  by  Schultze  (1867),  the  blood  in  the  capillaries  in 
the  membrana  vasculosa  retinae  of  Holosteans,  many  Teleosteans,^ 
Anurans  and  snakes,  and  in  the  vascularized  retina  of  the  eel  and  some 
Mammals  ^  must  constitute  an  effective  yellow  filter  through  which 
light  must  pass  to  reach  the  cones. 

We  have  seen  that  orange  and  red  and  occasionally  green  droplets 
in  addition  to  yellow,  occur  in  the  cones  in  the  periphery  of  the  retinae 
of  turtles  and  diurnal  birds  ;  these  must  aid  visual  discrimination  by 
-    enhancing  colour-contrasts.^ 

THE  STRUCTURE  OF  THE  RETINA 

Not  only  does  the  visual  acuity  depend  on  the  efficiency  of  the 
dioptric  system  of  the  eye,  but  also — and  equally^ — on  the  ability  of 
the  retina  to  act  as  an  analytical  receptor.  This  ability  depends 
essentially  on  two  factors — the  fineness  of  the  mosaic  of  retinal 
receptors  and  the  degree  of  summation  in  this  tissue. 

If  the  simplest  pattern  of  two  object-points  is  to  be  analysed, 
each  must  stimulate  a  separate  receptor  element  while  an  intervening 
element  must  remain  unstimulated.  So  far  as  the  retinal  mosaic  is 
concerned,  therefore,  the  greater  the  number  of  visual  cells  and  the 
closer  tiieir  packing,  particularly  in  the  important  receptor  area  of  the 

1  p.  299.  2  p.  479.  3  p   g3i^ 


THE   PERCEPTION   OF   FORM  657 

retina,  the  higher  will  be  the  acuity.  For  this  reason  the  potential 
visual  acuity  of  the  tiger-snake,  Notechis,  with  its  immensely  bulky 
cones,  or  of  some  deep-sea  Teleosteans  (as  the  pike-perch,  Stizostedion) 
in  which  the  visual  cells  are  so  large  that  the  retinal  mosaic  can  be 
seen  ophthalmoscopically  (Figs.  345,348),  is  necessarily  much  inferior  to 
that  of  the  chameleon  which  has  756,000  visual  cells  per  sq.  mm.  at 
the  fovea,  or  the  hawk,  Buteo,  which  is  said  to  have  a  foveal  density 
of  1,000,000  cones  per  sq.  mm.  (Rochon-Duvigneaud,  1933).  In  this 
respect  the  sauropsidan  retina,  particularly  that  of  lizards  and  birds, 
is  supreme,  and  considerably  more  effective  than  that  of  any  mammal  : 
the  cone  population  at  the  human  fovea  is  approximately  200,000 
per  sq.  mm. 

In  order  to  promote  visual  acuity  a  specialized  area  centralis 
is  frequently  developed  wherein  the  receptor  elements  are  more  closely 
packed  than  elsewhere  in  the  retina.  Such  an  area,  as  we  have  seen, 
is  found  in  varying  states  of  differentiation  in  representatives  of  most 
of  the  classes  of  Vertebrates  and  is  characteristic  of  diurnal  types.  It 
is  absent  in  the  primitive  Cyclostomes,  in  Selachians  except  the  dogfish, 
Mustelus,  in  the  coelacanth,  Chondrosteans,  Holosteans,  in  Urodeles, 
in  nocturnal  lizards  and  snakes,  and  in  Mammals  except  some  Rodents 
particularly  the  squirrel  family  (Sciuridae),  the  Ungulates,  Carnivores 
and  Primates.  In  location  such  an  area  may  be  central  or  temporal  ; 
in  shape,  rounded,  band-like  or  (exceptionally)  crescentic  or  ring- 
shaped  (Anurans)  ;  it  is  usually  single  but  sometimes  is  duplicated.  In 
it  the  visual  elements  have  become  slender  and  closely  packed,  an 
increase  in  receptor  elements  which  involves  a  corresponding  increase 
in  the  number  of  bipolar  and  ganglion  cells  in  the  retina  and  therefore 
in  the  thickness  of  this  tissue. 

The  following  are  provided  with  an  area  centralis  (macula)  without  a 
fovea  :  dogfish,  Mustelus  (central  and  round),  most  Teleosteans  (mainly  temjDoral 
in  location,  except  in  Hippocampus  where  it  is  central),  Anurans  (crescentic 
in  shape  over  the  optic  papilla),  Crocodilians  (horizontal  band),  Chelonians 
(central,  round),  rabbits  and  squirrels  (ill-defined,  horizontal  band).  Ungulates 
(sometimes  a  broad  horizontal  band,  usually  temporal,  sometimes  a  temporal 
round  area,  sometimes  a  combination  of  both),  most  Carnivores  (well-defined  and 
central),  nocturnal  Prosimians  and  Nyctipithecus  (central  and  rovmd).  Two 
teleostean  fishes  have  two  areas  without  a  fovea,  the  killifish,  Fundulus,  with 
two  ventro-temporal  horizontal  ridges,  and  the  guppy,  Lebistes,  with  an  axial 
and  a  ventral  area. 

There  is  evidence  that  the  area  centralis  in  certain  sjiecies  acts  as  a  device 
to  increase  sensitivity  rather  than  acuity,  the  visual  elements,  mainly  rods,  being 
multiplied  for  this  purjaose.^  This  is  seen  j^articularly  in  nocturnal,  or,  at  any 
rate,  not  strictly  diurnal  types — the  Crocodilians,  the  echidna,  the  opossum, 
and  perhaps  most  Ungulates  and  some  Carnivores.  Such  a  function  would 
certainly  seem  to  apply  to  the  pure-rod  fovese  of  the  deep-sea  teleost, 
Bathytroctes,  of  the  gecko,  Sphcerodactylus  parkeri,  and  o{  Sphcnodon. 

1  p.  673. 

S.O.— VOL.t.  42 


658  THE   EYE   IN   EVOLUTION 

A  further  device  for  increasing  the  resolving  power  is  the  develop- 
ment of  an  excavated  fovea  within  the  central  area.  The  classical 
view  of  the  rationale  of  this  pit -like  configuration  is  that  the  out- 
spreading of  the  cellular  layers  of  the  retina  and  the  consequent 
thinning  of  this  tissue  in  the  central  pit  reduce  the  absorption  and 
scattering  of  the  light  as  it  traverses  the  retinal  layers  to  reach  the 
receptor  cells.  It  is  questionable,  however,  if  the  retinal  tissue  is  much 
less  transparent  than  the  vitreous  and  it  seems  probable  that  in  weU- 
developed  foveae  at  any  rate,  a  refractive  magnification  of  the  image 
is  a  more  important  optical  effect  (Walls,  1937).  It  was  shown  by 
Valentin  (1879)  that  the  refractive  index  of  the  retina  is  considerably 
higher  than  that  of  the  vitreous  ;  this  being  the  case,  incident  light 
will  be  diverged  as  it  strikes  the  curved  sides  of  the  pit  (Fig.  791). 

VISUAL  CELLS 


VITREOUS 

Fig.  791. — The  Magnifying  Effect  of  the  Fovea. 

Owing  to  the  fact  that  the  index  of  refraction  of  the  retina  is  higher  than  that 
of  the  vitreous,  incident  light  striking  the  chvus  of  the  foveal  depression  is 
refracted  laterally  so  that  the  image  is  magnified. 

This  theory,  advanced  by  Walls  (1937),  demands  that  the  most 
efficient  fovea  will  have  a  deej)  pit  with  highly  convex  sides,  and  this 
is  indeed  the  case  ;  in  Birds,  for  example,  the  linear  magnification 
thus  obtained  is  of  the  order  of  13%  and  the  areal  magnification,  30%. 
As  Walls  puts  it,  when  the  area  centralis  has  done  everything  possible 
to  increase  the  number  of  receptor  imits  over  which  an  image  will  fall, 
a  further  increase  in  efficiency  is  gained  optically  by  the  magnification 
of  the  image.  A  shallow  or  broad  fovea  thus  probably  acts  by 
eliminating  the  dispersion  of  light  as  it  traverses  the  retina,  a  deep 
well-formed  fovea  with  a  steeply  curving  clivus  acts  also  as  an  effective 
magnifying  device  (Figs.  792-5). 

A  further  and  equally  interesting  function  for  the  fovea  has  been  suggested 
by  Puniphrey  (1948).  From  the  optical  point  of  view  he  reasoned  that  a  deep 
convex -clivate  fovea  vi^ould  produce  a  distorted  image  peripherally  and  a  clear 
image  only  at  the  centre  of  the  depression  ;  the  shape  of  fovea  could  thus  be 
interpreted  as  a  mechanism  to  maintain  accurate  fixation  of  the  eye  and  might 
be  used  to  appreciate  in  exaggerated  form  the  angular  movements  of  objects 
which  are  being  fixated.     This  function,  of  course,  would  be  attained  at  the 


THE   PERCEPTION   OF   FORM 


659 


expense  of  the  visual  acuity.  Pumphrey  therefore  suggested  that  foveas  developed 
along  two  possible  lines — one,  the  shallow  fovea  towards  greater  acuity  as  in 
man,  and  the  other,  the  convex-clivate  fovea  for  the  purposes  of  rapid  alignment 
of  the  fixation  object,  as  in  birds  of  prey. 

A  relatively  inefficient  fovea  of  the  first  type  is  seen  in  a  number  of  Teleosts,^ 
in  Sphenodon,  in  A?nyda  among  the  turtles,  in  two  types  of  tree-snake, ^  in  most 
ground-feeding  and  domesticated  and  many  nocturnal  birds,  in  the  temporal 
fovea  of  bifoveate  birds  (except  the  eagle),  in  Tarsius  and  the  Simians.  A  deep 
fovea  combining  tenuity  of  the  retina  with  magnification  of  the  image  is  seen 
in  its  highest  form  in  lizards,  in  the  central  fovea  of  predatory  birds,  in  the 
temporal  foveas  of  the  eagle  and  the  swift,  Micropus,  and  in  the  marmoset, 
Hapale.  In  some  water-birds  (gulls,  shearwater,  flamingo)  the  fovea  is  hori- 
zontally oval  and  trough -like. 


Swift 


Figs.   792  to  795. — The  Shape  of  the  Fovea. 


Fig.  792. — Sphenodon. 


Fig.   793. — ^A  primate. 


Fig.  794. — The  chameleon. 


Fig.  795.— a  hawk. 


In  its  position  the  fovea  is  usually  central,  subserving  lateral  vision  when  the 
eyes  are  so  placed,  and  binocular  vision  when  the  visual  axes  are  frontally 
directed.  A  temporal  fovea,  situated  far  out  in  the  periphery  of  the  retina, 
subserving  forward  vision  with  laterally  placed  ej^es,  is  found  in  Teleosts,  the 
foveate  snakes,  in  the  owl  and  bifoveate  birds  ;  only  in  wing-feeding  passerine 
and  predatory  birds,  and  in  the  arboreally  active  lizard,  Anolis,  are  two  foveae 
fovmd,  a  central  for  uniocular  vision  and  a  temporal  for  binocular  vision.' 

In  the  structural  basis  for  visual  acuity  the  degree  of  summatio7i  iri 
the  retina,  that  is,  the  number  of  visual  elements  connected  to  a  single 
optic  nerve  fibre,  is  a  factor  as  important  as  the  density  of  the  retinal 
mosaic.  In  general,  in  the  interests  of  sensitivity  ^  many  rods  are 
associated  with  a  single  ganglion  cell  ;  in  the  interests  of  acuity  in 
ideal  circumstances  each  cone  would  relay  through  a  bipolar  cell  to  an 
individual  ganglion  cell,  the  impulse  from  which  would  be  relayed  to  the 
brain  by  a  separate  nerve-fibre.    Each  visual  element  would  thus  have 


1  p.  309. 

3  See  further  p.  684. 


p.  388. 
p.  609. 


Flamingo 


Anolis 


660 


THE   EYE   IN   EVOLUTION 


Motacilla 


Hawk,  Buteo 


a  "  private  telephone  wire  "  to  the  brain,  so  that  each  cone  would 
make  its  individual  contribution  to  the  resolution  of  a  pattern.  In 
an  eye  designed  to  attain  a  high  visual  acuity,  therefore,  the  retina  is 
rich  in  cones,  its  area  of  special  differentiation  or  fovea  is  pure-cone, 
the  inner  nuclear  layer  is  thickly  packed  and  composed  of  many 
layers  of  cells  and  the  ganglion  cells  are  necessarily  numerous  (Fig.  756)  ; 
in  such  a  retina  there  is  thus  little  summation  and  the  ratio  between 
the  optic  nerve  fibres  and  receptors  is  high. 

Thus  Franz  (1934)  estimated  that  the  great  summation  in  the  retina  of 
Selachians  (visual  cells  10,800/sq.  mm.,  ganglion  cells  1,500)  must  reduce  their 
visual  acuity  to  5%  of  that  of  man  (200,000  :  200,000  in  the  central  fovea), 
while,  also  owing  to  its  high  summation,  the  resolving  power  of  the  eye  of  the 
whale  can  be  only  2%  of  that  of  man. 

The  remarkable  superiority  of  the  retina  of  Birds  is  shown  not  only  in  the 
regularity  of  the  arrangement  of  the  cells  but  in  their  numbers,  so  that  the 
ratio  of  conductive  to  sensory  cells  is  exceptionally  high.  In  the  American 
"  robin  ",  Turdus  migratorius,  for  example,  cellular  counts  outside  the  foveal 
region  give  the  astonishing  figures  of  :  outer  nuclei,  3  rows  of  cells  ;  inner 
nuclei,  28  ;  ganglion  cells,  3  (Walls,  1942).  Even  in  the  week-old  chick  the 
corresponding  figures  for  the  peripheral  retina  are  :  2-5,  18,  2-5.  Similarly  in 
the  peripheral  retina  of  the  white  wagtail,  Motacilla  alba,  there  are  120,000 
visual  cells  per  sq.  mm.  with  a  corresponding  100,000  ganglion  cells  ;  in  the 
fovea  of  the  English  sparrow.  Passer  domesticus,  400,000  (Franz,  1934),  and  in 
the  hawk,  Buteo,  1,000,000  (Rochon-Duvigneaud,  1943).  In  the  human  fovea 
the  corresponding  figvire  is  200,000.  Even  in  the  peripheral  retina  of  the 
nocturnal  owl.  Bubo,  there  are  56,000  visvial  elements  per  sq.  mm.  summating 
3,600  ganglion  cells,  while  the  overall  summation  ratio  of  the  human  retina  is 
125  :  1  (Walls,  1942).  In  the  comparative  disability  of  daylight  the  owl  would 
thus  appear  to  have  a  potential  visual  acuity  greater  than  man,  while  the 
resolving  power  of  the  peripheral  retina  of  the  hawk  should  be  twice,  and  that 
of  its  fovea  eight  times  that  of  the  human  fovea. 


Minnow 


Stickleback 


THE    VISUAL    ACUITY    OF    VERTEBRATES 

Among  FISHES  the  general  acuity  is  probably  relatively  poor 
(v.  Hess,  1909-14),  but  among  some  Teleosts  the  complexity  of  the 
retina  and  the  provision  of  a  fovea  indicate  the  possibility  of  a  rela- 
tively high  grade  of  resolution.  Training  experiments  depending  on 
the  discrimination  of  form  in  a  number  of  Teleosts  have  furnished 
interesting  results.  Goldsmith  (1914)  and  Maes  (1930)  found  that 
goldfish  were  adept  at  this,  while  Rowley  (1934)  established  that  they 
could  distinguish  between  circles  held  in  front  of  them  the  diameters 
of  which  differed  by  only  3  millimetres  ;  Herter  (1929-53)  trained 
minnows  to  differentiate  between  circles,  squares,  triangles  and  crosses  ; 
and  Meesters  (1940)  obtained  similar  results  with  sticklebacks  with 
curved  figures.  It  is  obvious  from  the  experiences  of  deep-sea  divers 
such  as  Beebe  (1934)  and  Cousteau  (1953)  that  certain  fish,  at  any  rate, 
exhibit   a   degree   of  curiosity   regarding   strange   elements   in   their 


THE   PERCEPTION   OF   FORM 


661 


environment  which  can  only  be  explained  by  the  possession  of  a 
considerable  degree  of  form  vision  and  sufficient  appreciation  of  the 
meaning  of  objects  to  influence  their  ordinary  activities. 

Some  AMPHiBiAXS,  such  as  the  frog  and  toad,  are  essentially 
visual  animals  ;  they  catch  their  insect  food  with  great  dexterity,  a 
feat  demanding  considerable  visual  acuity,  and  recognize  their  mate 
by  sight  several  inches  away  (Banta,  1914).  Moreover,  there  is  some 
evidence  from  their  homing  ability  and  capacity  to  recognize  their 
LviTKor}  .\:^t  their  behaviour  is  determined  to  some  extent  by 
visual  memory  although  other  senses  undoubtedly  contribute,  some- 
times to  a  prejjonderant  degree  (Breder,  1925,  in  HyJa  ;  Czeloth,  1930, 
in  Triturus).  The  inertia  and  lack  of  intelligence  of  Amphibians,  however, 
make  experimental  exj^loration  of  their  form-sense  difficult.  On  the 
whole  it  would  appear  to  be  defective  :  in  this  respect  they  are  much 
inferior  to  fishes.  Thus  frogs  have  been  found  to  be  unable  to 
distinguish  between  a  lighted  space  and  a  white  solid  ;  trained  to  the 
former  they  would  attempt  to  struggle  into  a  solid  white  surface 
(Dickerson.  1906)  ;  but  Pache  (1932)  was  able  to  train  Hyla  to 
distinguish  between  a  triangle  and  a  circle.  It  would  seem  that 
movement -sight  plays  a  much  greater  part  than  form-sight  in  their 
visual  activity  both  in  natural  surroundings  and  experimental  training. 

Among  REPTILES  a  high  acuity  of  vision  is  seen  only  among 
lizards  and  to  a  less  extent  among  turtles.  We  would  expect  the 
excellent  fovea  of  lizards  to  provide  a  correspondingly  good  visual 
acuity,  an  expectation  borne  out  by  the  accuracy  of  their  fiy-catching  : 
the  unerring  aim  of  the  long  tongue  of  the  chameleon  is  proverbial.^ 
With  their  cone-rich  retinae  the  same  applies  to  Chelonians  ;  thus  a 
turtle  will  deftly  catch  an  insect  in  flight  and  a  domesticated  specimen 
is  said  to  recognize  the  person  who  feeds  it  at  a  distance  of  50  metres 
while  paying  no  attention  to  a  stranger  (Rollinat,  1936).  Moreover, 
in  training  experiments  turtles  have  been  found  to  be  able  to  dis- 
tinguish between  such  forms  as  horizontal  and  vertical  lines,  circles, 
triangles  and  squares  or  other  simple  geometrical  figures  (Casteel, 
1911  ;  Parker,  1922  ;  Kuroda,  1933  ;  Wojtusiak,  1933  ;  Myhiarski. 
1951).  It  would  thus  seem  that  these  animals  have  a  relatively 
high  capacity  for  form  vision.  On  the  other  hand,  the  comparatively 
crude  nocturnal  retinte  of  the  Crocodilians  and  oi  Sphenodon  necessitate 
a  low  acuity.  Among  the  Ophidians  the  tree-snakes  and  bird-snakes 
provided  with  a  fovea  -  and  binocular  vision  ^  are  the  only  species 
which  depend  essentially  on  their  eyes  in  striking  their  prey  ;  but 
the  visual  acuity  of  snakes  as  a  class  is  probably  the  lowest  among  all 
diurnal  Vertebrates,  mucli  more  dependence  being  placed  on  other 
senses  such  as  smell  and  touch. ^ 

1  p.   695.  -  p.  388.  3  p_  674,  4  p_  599, 


Hyla 
Triturus  (male) 


Chameleon 


Turtle 


662 


THE   EYE   IN  EVOLUTION 


Pigeon 


Shrike,  Lanius 


The  highest  visual  acuity  in  the  entire  vertebrate  phyhim  is  seen 
in  BIRDS  ;  this  we  would  expect  with  their  enormously  large  eyes  with 
an  anteriorly  placed  lens  and  a  globular  posterior  segment,  their 
emmetropic  refractive  condition  and  magnificent  accommodative 
mechanism,  the  multiplicity  of  oil-droplets  in  the  cones,  the  excellence 
of  their  foveae,  the  perfection  of  the  lamination  and  the  low  summation 
of  their  retinae.  This  is  indeed  the  case,  for  the  visual  resolution 
attained  by  some  of  the  passerine  wing-feeders  and  the  predators  is 
phenomenal.  Investigating  this  problem,  Pumphrey  (1948)  estimated 
that  a  resolution  of  about  10"  of  arc  should  be  possible  by  the  avian 
retina,  three  times  the  accuracy  attainable  in  the  human  retina,  and 
in  training  experiments,  Grundlach  (1933)  actually  demonstrated  a 
resolution  down  to  23"  in  pigeons  ;  in  these  birds  a  high  degree  of 
form -discrimination  can  be  developed  although  it  tends  to  be  primarily 
unidimensional  (Chard,  1939  ;  Towe,  1954  ;  Jones,  1954).  In  this 
connection  it  is  to  be  remembered  that  the  degree  of  resolution  capable 
by  a  bird  such  as  the  hawk  ought  to  be  of  a  considerably  higher  standard 
than  that  of  the  pigeon. 

This  potentiality  is  borne  out  in  the  everyday  activities  of  birds 
(von  Hess,  1912;  van  Eck,  1939;  Rochon-Duvigneaud,  1943  ;  Donner, 
1951  ;  and  others).  It  is  true  that  many  insect-catchers  such  as  the 
swallow  or  the  night-hawk  trawl  for  their  food  indiscriminately  on  the 
wing  particularly  during  the  twilight  hours  with  little  reliance  on  vision; 
but  the  visual  acuity  of  the  martlet  which  flies  high  and  at  intervals 
swoops  downward  upon  an  individual  insect  at  a  considerably  lower 
level,  or  that  of  the  humming-bird  which  opens  its  long  narrow  beak 
but  slightly  and  impales  minute  insects  individually  with  its  long  bifid 
tongue,  must  be  superb.  In  many  birds  the  visual  acuity  far  exceeds 
that  of  man  ;  the  reactions  of  fear  by  the  shrike,  Lanius,  which  the 
falconer  carried  with  him  in  a  cage,  let  him  know  the  whereabouts  of 
his  bird  of  prey  long  after  he  himself  had  lost  track  of  it  in  the  sky. 
Even  an  owl,  the  eye  of  which  is  specialized  for  night  vision,^  will 
detect  a  hawk  approaching  in  the  day-sky  at  a  height  at  which  it  is 
invisible  to  man.  The  excellence  of  the  optical  resolution  of  which  the 
avian  eye  is  capable  is  probably  aided  by  a  markedly  high  capacity 
to  differentiate  tones,  a  faculty  possibly  based  on  the  light -filtering 
effect  of  the  oil-droplets  of  their  cones  ^  ;  thus  dead  game  lying  on  the 
ground,  to  us  completely  camouflaged  by  its  surroundings,  will  be  seen 
by  the  African  vulture — and  it  will  recognize  that  it  is  dead — from  a 
height  of  3,000-4,000  metres,  a  height  so  great  that  a  man  cannot 
discern  the  bird  in  the  sky  with  its  3-metre  wing-span. 


^  See  p.  605.  It  is  to  be  noted  that  according  to  v.  Hess  (1912)  the  retina  of  the  owl 
contains  2,500,000  cones. 
2  p.  631. 


THE   PERCEPTION   OF   FORM  663 

This  superb  acuity  is  not,  of  course,  universal  among  birds.  Thus, 
testing  the  vision  of  domestic  hens  to  see  a  grain  of  wheat  in  strange 
surroundings,  Engelmann  (1952)  concluded  that  the  limiting  value  was 
determined  by  a  retinal  image  0-02  mm.  in  diameter.  Nor  is  their 
form  sense,  despite  the  excellence  of  its  physical  basis,  always  fully 
exploited.  Conditioning  experiments  have  been  undertaken  on  a 
considerable  scale  in  birds,  particularly  the  pigeon,  a  research  pioneered 
by  Popov  in  Pavlov's  school  (see  Razran,  1933)  (ten  Cate,  1923  ; 
Beritoff,  1926  ;  Riddle  and  Burns,  1931  ;  To  we,  1954  ;  Jones,  1954  ; 
and  others).  It  has  been  established  that  birds  are  eminently  trainable 
to  distinguish  between  different  kinds  of  geometrical  figures  of  equal 
area,  and  that  the  development  of  their  sense  of  form  is  relatively  high. 
At  the  same  time,  when  pigeons  are  offered  a  choice  of  a  number  of 
visual  variables  in  discriminative  problems  they  always  respond  con- 
sistently to  one  of  the  variables  only.  Jones  (1954)  established  that 
cues  based  on  colour  were  most  readily  followed,  those  depending  on 
position  came  next,  while  form  discrimination  was  the  most  difficult 
to  learn. 

The  excellence  of  the  form  perception  of  birds  is  also  seen  in  their 
extraordinary  powers  of  recognition.  This  is  a  well-attested  phenome- 
non ;  birds  rapidly  learn  to  recognize  each  other  even  when  two  weeks 
old  (the  coot,  Fulica,  Alley  and  Boyd,  1950)  and  recognition  is  often 
made  entirely  on  a  visual  basis  even  when  the  bird  in  question  is 
silent.  Robins  {Erithacus)  can  recognize  their  silent  mates  at  a  distance 
of  over  30  yards  even  although  they  are  partially  screened  by  trees 
(Lack,  1939)  ;  tits  {Parus)  can  distinguish  individuals  in  a  flock  at  60 
yards  distance  (Morley,  1942),  while  pintails  {Dafila)  can  identify  one 
another  300  yards  away  (Hochbaum,  1944).  An  artificial  change  of 
appearance  as  by  transferring  the  comb  to  the  side  of  the  head,  may 
destroy  recognition  (see  Thorpe,  1956).  Recognition  of  human  beings 
by  birds  is  also  well  kno^ii,  the  facial  characteristics  sometimes  being 
recognized  in  spite  of  a  change  of  clothing  (Poulsen,  1944  ;  Buxton, 
1946  ;  Ash,  1952  ;  Thorpe,  1956).  In  this  respect  also  the  visual 
memory  may  be  long  ;  it  is  true  that  in  some  species  impressions  may 
fade  after  a  few  days,  but  jackdaws  can  remember  individuals  for 
several  months  (Lorenz,  1935),  a  pigeon  has  been  said  to  remember  a 
particular  person  after  11  months  (Diebschlag,  1940),  and  a  hen  trained 
to  eat  off  a  certain  colour  performed  her  task  again  a  year  after  the 
training  had  ceased  (Claparede,  1926).  The  annual  return  of  many 
migratory  birds  to  the  same  spot  is  another  case  in  point. 

Most  MAMiNiALS  are  in  an  entirely  different  category  ;  only  the 
Sciuridse  (the  entire  retina  of  which  may  be  said  to  be  a  macula), 
a  few  Carnivores,  some  Ungulates,  and  Primates  have  a  highly  developed 
visual  acuity.     Thus  in  rats  and  mice  training  experiments  show  that 


664 


THE   EYE   IN   EVOLUTION 


Marmot 


form-discrimination  is  relatively  poor  (Karli,  1954  ;  and  others).  On 
the  other  hand,  the  care-free  agility  of  the  arboreal  squirrel  necessitates 
an  unusually  keen  vision,  while  the  marmots  in  the  Alps  with  their 
j)ure-cone  retina  will  whistle  as  they  spot  a  climber  long  before  he  can 
see  them.  In  dogs,  Pavlov  (1911-27)  found  that  conditioned  reflexes 
could  be  developed  depending  on  the  discrimination  between  ellipses 
and  a  circle  with  a  differentiation  of  the  semi-axes  of  only  8 : 9 — a 
very  high  standard  of  efficiency.  Among  the  Ungulates  the  acuity 
is  higher  than  would  be  expected  in  a  rod-rich,  afoveate  eye,  possibly 
because  their  eyes  are  usually  large  ;    the  horse  or  the  deer,  although 


Fig.  796. — The  Visual  Responses  of  the  Robin. 

On  the  left  is  a  mounted  young  robin  with  a  dull  brown  breast  ;  on  the 
right  a  tuft  of  red  feathers.  The  territory-holding  male  threatens  the  bundle 
of  red  feathers  rather  than  a  complete  robin  which  lacks  red  feathers  (from 
Lack  ;    Tinbergen,  Sfudy  of  Instinct  ;    Clarendon  Press). 


relying  largely  on  movement,  has  excellent  sight,  while  the  acuity  of  the 
higher  Primates  (and  man),  althougli  not  equal  to  that  of  Birds,  is 
sufficientl}^  high  for  vision  to  become  the  dominant  sense  in  regulating 
conduct. 

In  any  appreciation  of  the  visual  capacity  of  animals,  however, 
whether  Fishes,  Reptiles,  Birds,  or  Mammals,  it  is  to  be  remembered 
that  their  visual  perceptions  often  differ  from  our  own  in  that  they  are 
limited  to  one  or  a  few  relatively  simple  "  sign-stimuli  "  of  form,  colour 
or  movement,  and  not  to  all  the  visual  elements  of  the  situation.  For 
this  reason  the  pattern  of  innate  behaviour  can  be  released  by  the  exhi- 
bition of  crudely  coloured  models  in  which  resemblances  of  form  are  very 
inexact.  The  threat -display  in  the  male  robin,  for  example,  is  elicited 
by  an  isolated  bundle  of  red  breast  feathers  having  little  resemblance 
to  the  bird's  usual  rival  (Fig.  796)  (Lack,  1943),  or  that  of  the  lizard, 


THE   PERCEPTION   OF   FORM  665 

Lacerta  viridis,  by  a  crude  clay  model  so  long  as  it  has  a  blue  throat 
(Kitzler,  1941).^  The  feeding  reactions  of  young  herring-gulls  are 
initiated  by  crude  models  simulating  only  in  a  rough  and  ready  manner 
the  red  patch  on  the  parents'  mandible  which  forms  the  normal 
stimulus  (Tinbergen  and  Perdeck,  1950)  ;  and  despite  their  remarkable 
visual  acuity  birds  show  incubation  responses  to  objects  other  than 
eggs  so  long  as  they  are  small  and  round  (Kirkman,  1937),  or  exhibit 
escape  reactions  to  a  crude  dummy  as  if  it  were  an  enemy  bird  of  prey, 
no  matter  what  the  colour  or  the  shape  of  its  wings  and  tail  may  be,  so 
long  as  the  neck  is  short  (Lorenz,  1940).  So  also  will  the  male  stickle- 
back, Gasferosteus  aculateus,  react  differently  to  a  crude  model  of  a 
fish  :  in  the  head-up  position  it  will  exhibit  mating  activity,  in  the 
head-down  position  it  will  exhibit  fight  (Tinbergen,  1948)  and  it  will 
be  similarly  stimulated  by  a  truck  passing  outside  its  window  provided 
only  that  it  is  red  as  the  belly  of  its  natural  rival. 

The  differences  between  visual  acuity  in  these  members  of  the  vertebrate 
phyhim  which  have  been  experimentally  investigated,  and  particularly  the 
difference  between  diurnal  and  nocturnal  animals,  are  seen  in  the  following 
figures  which  refer  to  minutes  of  minimum  visual  angle  : 

Diurnal — man,   0-44  to   0-83  ;     chimpanzee,   0-47  ;    rhesus  monkey,   0-67  ; 

cebus  monkey,  0-95  ;    homing  pigeon,  0-38. 
Nocturnal — cat,    5-5  ;     alligator,    11-0  ;     opossum,    11-0  ;     rat     (pigmented) 
26-0,  (albinotic)  52-0. 

Abelsdorff.    Arch.  Anat.  Physiol.,  Physiol.  Dickerson..    The  Frog  Book,   X.Y.  (1906). 

Aht.,  155  (1898).  Diebschlag.      Z.    vergl.    Physiol,    28,    67 

Alley  and  Boyd.     The  Ibis,  92,  46  (1950).  (1940). 

Armstrong.     Bird  Display  and  Behaviour,  Donner.      Acta  zool.  Fenn.,    66,    1   (1951). 

London  (1947).  van  Eck.    Arch,  neerl.  Zool.,  3,  450  (1939). 

Ash.     Brit.  Birds,  45,  288  (1952).  Engelmann.     Z.  TierpsychoL,  9,  91  (1952). 

Banta.     Biol.  Bull.,  26,  171  (1914).  Fincham.     Trans,  opt.  Soc.  Lond.,  26,  239 

Beebe.    Zoologica,  16,  149  (1934).  (1925). 

Beer.     Pfliigers  Arch.  ges.  Physiol.,  5Z,  l"^ 5  Franz.      Jetia.    Z.    Naturuiss.,    40,     697 

(1893)  ;   58,  523  (1894)  ;   69,  507  ;   73,  (1905). 

501  (1898).  Zool.  Jb.,  Abt.   Zool.   Physiol.,  49,   323 

Beritoff.     Pfliigers  Arch.  ges.  Physiol.,  21Z,  (1931). 

370  (1926).  Bolk's  Hb.  d.  vergl.  Anat.  d.  Wirbelthiere, 

Bourguignon     and     Verrier.       Bull.    Soc.  Berlin,  2  (ii),  1093  ( 1934). 

ophtal.  Paris,  273  (1930).  Goldsmith.     Bull.  Inst.  gen.  Psychol.,  14, 

Breder.    Nat.  Hist.,  25,  325  (1925).  97  (1914). 

Buxton.     Contribs.  to  Psychol.   Theory,  2,  Grundlach.      J.    comp.    Psychol.,    16,    327 

75  (1946).  (1933). 

Casteel.    J.  aniiyi.  Behav.,  1,  1  (1911).  Hartridge  and  Yamado.    Brit.  J.  Ophthal., 

ten   Gate.      Arch,   neerl.    Physiol.,   8,   234  6,  481  (1922). 

(1923).  Helmholtz.     v.   Graefes    Arch.    Ophthal.  1 

Chard.     J.  e.vp.   Psychol.,  24,  588  (1939).  (2),  1  (1855). 

Claparede.    Arch,  de  Psychol.,  20  (78),  178  Herter.    Z.  vergl.  Physiol,  10,  688  (1929)  ; 

(1926).  11,  730  (1930). 

Cousteau.        The    Silent     World,     London  Die     Fischdressuren     u.      ihre     sinnes- 

(1953).  physiologische      Grundlagen,       Berlin 

Czeloth.     Z.  vergl.  Physiol,  13,  74  (1930).  (1953). 

1  The  literature  on  tliis  subject  is  now  comprehensive  :  see  Russell  (1934—43), 
Lorenz  (193.5-39),  Noble  (1936),  Marshall  (1936),  Matthews  (1938),  Huxley  (1938)! 
Armstrong  (1947),  Tinbergen  (1948-51),  and  others. 


666 


THE   EYE   IN   EVOLUTION 


V.  Hess,  C.     Arch.  Augenheilk.,  62,  345  ; 

63,  88  (1909). 
Arch,  vergl.  OphthaL,  1,  153  (1910). 
Zool.  Jb.,  Abt.   Zool.   Physiol.,  30,   339 

(1911)  ;    Suppl.  15  (3),  155  (1912). 
Vergl.   Physiol,   d.   Gesichtssinnes,   Jena 

(1912). 
Entw.    V.    Lichtsinn   u.    Farhensinn    in 

der  Tierreiche  (1914). 
V.    Hess     and    Heine.      v.    Graefes   Arch. 

OphthaL,  46,  243  (1898). 
Hirschberg.       Arch.    Anat.     Physiol.,    81 

(1882). 
Hochbaum.     The  Canvasback  on  a  Prairie 

Marsh,  Wash.  (1944). 
Huxley.    Atner.  Nat.,  72,  416  (1938). 
Johnson.    Philos.  Traris.   B,  194,  1  (1901). 
Jones,  L.  V.     J.  comp.  physiol.   Psychol., 

47,  253  (1954). 
Kahmann.     Zool.  Jb.,  Abt.  Zool.  Physiol., 

52,  295  (1932). 
Zool.  Anz.,  102,  177  (1933). 
Karli.     C.  R.  Soc.  Biol.  (Paris),  148,  575, 

1111  (1954). 
Kirkman.    Bird  Behaviour,  London  (1937). 
Kitzler.     Z.  Tierpsychol.,  4,  353  (1941). 
Kolmer.    Pfliigers  Arch.  ges.  Physiol.,  204, 

266  (1924). 
Kuroda.    Acta  psychol.  Keijo,  2,31(1933). 
Lack.     Proc.  zool.  Soc.  Lond.,  A,  109,  169 

(1939). 
The  Life  of  the  Robin,  London  (1943). 
Leplat.     Bull.  Acad.  belg.  Clin.  Sci.,  7,  748 

(1921). 
C.  R.  Assoc.  Anat.,  17,  195  (1922). 
Lorenz.     J.  Ornith.,  Leipzig,  83,  137,  289 

(1935). 
The  Auk,  54,  245  (1937). 
Verh.  dtsch.  zool.  Ges.,  41,  69  (1939). 
Maes.    Ann.  Soc.  roy.  Zool.  Belg.,  60,  103 

(1930). 
Marg  and  Reeves.    J.  opt.  Soc.  Amer.,  45, 

926  (1955). 
Marg,    Reeves    and    Wendt.      Amer.    J. 

Optom.,  31,  127  (1954). 
Marshall.      Philos.    Trans.     B,   226,    423 

(1936). 
Matthews.      Proc.  roy.  Soc.     B,   126,  557 

(1938). 
Matthiessen.     Pfliigers  Arch.  ges.  Physiol., 

38,  521  ;    39,  204  (1886). 
Z.  vergl.  Augenheilk.,  7,  77  (1893). 
Meader.     Yale  J.  Biol.  Med.,  8,  511  (1936). 
Meesters.      Z.    Tierpsi/choL,  4,   84   (1940). 
Michel.     Zool.  Anz.,  98,  158  (1932). 
Jena.  Z.  Naturwiss.,  66,  577  (1933). 


Morley.     Brit.  Birds,  35,  261  (1942). 
Mylnarski.     Bull,  internal.  Acad.  Pol.  Sci. 

et  Lett.,  Sci.  Ser.  B,  253  (1951). 
Noble.     The  Auk,  53,  269  (1936). 
Pache.     Z.  vergl.  Physiol.,  17,  423  (1932). 
Parker.    J.  comp.  Psychol.,  2,  425  (1922). 
Pavlov.  Ergeb.  d.  Physiol.,   11,  345  (1911). 
Conditioned     Reflexes     (Trans.     Anrep), 

Oxon.  (1927). 
V.  Pflugk.     Bull.  Soc.  frauQ.  Ophtal.,  25, 

155  (1908). 
Poulsen.     Dansk.  Orn.  Foren.  Tidskr.,  38, 

82  (1944). 
Pumphrey.     The  Ibis,  90,  171  (1948). 

J.  exp.  Biol.,  25,  299  (1948). 
Rabaud.    Elements  de  Biol,  generale,  Paris 

(1920). 
Razran.     Psychol.  Bull.,  30,  261  (1933). 
Riddle  and  Burns.      Proc.  Soc.  exp.  Biol. 

N.Y.,  28,  979  (1931). 
Rochon-Duvigneaud.      Bull.  Soc.  ophtal., 

Paris,  19  (1918). 
Recherches  sur  Voeil  et  la  vision  chez  les 

vertebres,  Paris  (1933). 
Les  yeux  et  la  vision  des  vertebres,  Paris 

(1943). 
RoUinat.      Vie   des   reptiles   de   la   France 

centrale,  Paris  (1936). 
Rowley.     Genet.  Psychol.  Monog.,  15,  245 

(1934). 
Russell.        The     Behaviour     of    Animals, 

London  (1934). 
Proc.  Linn.  Soc.  Lond.,  154,  195  (1943). 
Schultze.    Arch.  mikr.  Anat.,  3,  215  (1867). 
Thorpe.    Learning  and  Instinct  in  Animals, 

London  (1956). 
Tinbergen.     Wilson  Bull.,  60,  6  (1948). 

The  Study  of  Instinct,  Oxon  (1951). 
Tinbergen  and  Perdeck.     Behaviour,  3,  1 

(1950). 
Towe.    J.  comp.  physiol.  Psychol.,  47,  283 

(1954). 
Valentin.     Pfliigers  Arch.  ges.  Physiol.,  19, 

78  (1879). 
Verrier.     Bull.  Biol.  Fr.  Belg.,  Suppl.  11, 

137  (1928). 
Ann.  Sci.  7iat.  Zool.,  13,  5  (1930). 
Btdl.  Soc.  Zool.  Fr.,  59,  535  (1935). 
Les  yeux  et  la  vision,  Paris  (1938). 
Walls.     Arch.  OphthaL  (Chicago),  18,  912 

(1937)  ;    23,  831  (1940). 
The  Vertebrate  Eye,  Michigan  (1942). 
Walls  and  Judd.      Brit.  J.   OphthaL,  17, 

641,  705  (1933). 
Wojtusiak.      Z.    vergl.    Physiol.,    18,    393 

(1933). 


THE  PEKUEPTION  OF  SPACE 

An  appreciation  of  space  and  an  ability  to  localize  objects  therein 
are  essential  requirements  of  all  organisms.  It  is  obvious  that  any 
capacity  for  the  exploration  of  space  must  be  referred  to  some  system 


THE   PERCEPTION   OF   SPACE  667 

of  coordinates.  Plant  life  orientates  itself  with  regard  to  gravity 
(geotropism)  ;  equally,  in  animal  life  the  mechanism  which  maintains 
the  posture  of  the  body — the  basis  of  its  perception  of  space — uses  the 
same  fundamental  reference-frame,  and  when  a  vertebrate  is  at  rest  it 
utilizes  an  elaborate  system  of  static  postural  reflexes  designed  to 
maintain  its  equilibrium  and  provide  a  starting-point  for  its  contacts 
with  the  outside  world.  These  are  supj^lemented  by  a  further  system 
of  stato-kinetic  reflexes  which  serve  a  similar  jDurpose  to  the  animal 
in  motion  (Sherrington,  1904-6  ;  Magnus,  1924).  It  is  this  combina- 
tion which  maintains  the  organism  right-side-up  and  allows  it  to 
retain  its  relationships  with  its  environment. 

With  this  mechanism  as  basis,  space  is  explored  egocentrically  by 
the  various  senses,  every  one  of  which  contributes  in  some  degree  to 
the  common  aim.  The  immediate  vicinity  can  be  explored  by  the 
tactile  sense  ;  but  the  development  of  projicient  senses  is  necessary 
for  the  appreciation  of  anything  beyond  the  restricted  area  which  the 
animal  can  touch.  It  is  true  that  the  tactile  sense  can  be  projected 
to  some  extent,  as  by  the  appreciation  of  vibrations  as  is  seen  in  the 
ability  of  snakes  to  record  ground-vibrations  through  the  lower  jaw,^ 
a  facility  akin  to  that  displayed  by  web-spinning  and  ripple -spiders.  ^ 
The  olfactory  sense  and  to  a  greater  extent  the  auditory  sense  act  as 
adjuvants  for  this  purpose,  but  with  the  exception  of  the  astonishing 
development  of  the  auditory  powers  of  bats,'^  these  form  inefficient  and 
unreliable  guides.  The  remarkable  thermal  sense  of  certain  colubrid 
snakes  ^  forms  another  exception  ;  but  as  a  general  rule  throughout 
the  vertebrate  phylum  extended  spatial  judgments,  at  least  in  diurnal 
species,  are  essentially  dependent  on  vision  which  makes  by  far  the 
greatest  contribution  to  the  perceptual  range  of  the  animal  and  to 
the  accuracy  of  its  assessments. 

Visual  spatial  perceptions  may  be  classified  into  two  main  types 
each  of  which  may  be  divided  into  two  attributes  : 

(1)  Bi-dimensional  perceptions,  made  up  of 

[a]  the  perception  of  direction  which  allows  an  estimation  to  be 
made  of  the  position  of  an  object  relative  to  the  body  ; 
and    (6),    an   extension   of  this   faculty   into   the   perception   of  bi- 
dimensional  distance  (or  extensity)  allowing  an  estimate  to 
be  made  of  the  angular  extension  of  an  object. 

(2)  Tri -dimensional  perceptions,  made  up  of 

(a)  the  perception  of  depth  which  includes  the  capacity  of  stereo- 
scopic vision  when  binocularity  is  attained; 
and  (6),  an  extension  of  this  faculty  into  the  perception  of  size,  a 
psychological  appreciation  of  the  size  of  a  body  emerging  as 

1  p.  599.  2  p_  579. 

3  p.  601.  *  p.  600. 


668  THE   EYE   IN   EVOLUTION 

a  unitary  perception  based  upon  estimates  of  the  extent  of 
the  retinal  image  and  its  distance  away. 

Such  perceptions  depend  on  a  number  of  physiological  and 
psychological  factors.  The  primary  factor  in  a  visual  analysis  of  space 
is  the  characteristic  of  local  sign  in  the  retinal  elements — that  innate 
property,  possessed  by  all  distinguishable  parts  of  the  body,  whereby 
the  excitation  of  one  receptor  is  discriminated  from  the  excitation  of 
its  neighbours,  so  that  all  object -points  are  projected  visually  with 
regard  to  the  eye  as  spatial  entities  separate  from  all  other  points.    In 


FIXATION 
SPOT 


CENTRE 
OF  GRAVITY 

Fig.  797. — The  Frame  of  Refebence  in  Space 

The  two  fundamental  coordinates — the  vertical  determined  gravita- 
tionally  froin  the  earth's  centre  and  the  horizontal  determined  visually  from 
the  horizon. 

animals  possessed  of  an  area  centralis  or  fovea, ^  this  region  is  pre- 
eminently possessed  of  local  sign  and  forms  the  primary  point  of 
reference  ;  images  formed  thereon  are  projected  along  a  central  base 
line  (the  fixation  line)  in  relation  to  which  images  falling  on  eccentric 
retinal  points  are  correspondingly  located.  Such  a  mechanism  is 
applicable  to  each  eye  separately,  but  when  the  visual  fields  overlap, 
within  the  area  common  to  both,  sensory  impressions  are  S3aithesized 
into  a  unity  so  that  objects  in  space  are  projected  along  a  line  of 
direction  emanating  from  a  hypothetical,  centrally  situated  cyclopean 
eye.  It  is  the  simultaneous  presentation  to  consciousness  of  two 
slightly  dissimilar  images  in  this  way  that  forms  the  basis  of  stereo- 
scopic vision.  In  addition  to  this  retinal  mechanism  orientating  objects 
in  space  with  reference  to  the   eyes  and  establishing  an  egocentric 

1  p.  657. 


THE   PERCEPTION   OF   SPACE  669 

localization,  the  postural  mechanism  persists  which  extends  the  frame  of 
reference  to  provide  a  gravitational  localization  (Fig.  797).  Visual 
perceptions  are  synthesized  with  impressions  from  the  extra-ocular 
muscles,  the  neck  and  the  labjTinths,  so  that  visual  orientations  are 
related  to  movements  of  the  eyes  with  respect  to  the  head,  of  the  head 
in  respect  to  the  trunk,  and  of  the  trunk  in  respect  to  gravity,  and  thus 
an  exploration  of  space  is  attained  on  a  gravitational  basis.  These 
fundamental  mechanisms  on  the  physiological  level  are  irmate  and 
hereditarily  transmitted,  and  upon  them  is  erected  a  further  psycho- 
logical structure  determined  by  the  experience  of  each  individual  by 
which  the  accuracy  of  spatial  judgments  is  considerably  increased  and 
their  value  to  the  animal  augmented. 

It  will  be  seen  that  the  two  fundamental  coordinates  are  vertical  and 
horizontal  in  direction,  the  first  determined  gravitationally  from  the  earth's 
centre,  the  second  visually  from  the  horizon.  We  have  already  seen  that  the 
visual  responses  of  the  octopus  suggest  that  these  directions  have  a  special  status 
not  only  in  the  end-organ  but  also  in  its  projections  onto  the  primitive  central 
nervous  system,^  a  circumstance  which  indicates  their  phylogenetic  age  and 
practical  importance. 

Before  discussing  the  part  played  by  spatial  perceptions  in  the 
behaviour  of  Vertebrates,  it  wall  be  useful  to  discuss  the  basic  physio- 
logical factors  which  underlie  such  judgments — the  mutual  relation  of 
the  visual  fields,  the  occurrence  of  binocular  as  opposed  to  panoramic 
vision,  and  finally  the  nature  of  reflex  and  voluntary  ocular  movements 
and  their  relation  to  visual  perceptions. 

THE    UNIOCULAR   VISUAL    FIELDS    OF    VERTEBRATES 

The  uniocular  field  of  Vertebrates  is  relatively  constant,  averaging 
in  angular  size  about  170°.  The  estimation  can  be  made  theoretically 
by  optical  calculation  (Grossmaiui  and  Mayerhausen,  1877)  or  objec- 
tively and  more  effectively  by  observing  the  image  of  a  moving  light 
as  seen  by  transillumination  through  the  sclera,  a  method  introduced 
by  the  great  physiologist,  Johannes  Miiller  (1826),  in  his  study  of 
corresponding  retinal  points,  and  applied  to  the  determination  of  the 
uniocular  and  binocular  fields  by  Armin  Tschermak  (1902),  Rochon- 
Duvigneaud  (1921-23),  Verrier  (1930),  and  others.  Following  Miiller's 
lead,  finictional  confirmation  of  these  results  may  be  obtained  in 
animals  which  will  respond  suitably  by  the  subjective  method  of  noting 
the  angle  at  which  an  object  will  attract  attention. 

The  extent  of  the  field  varies  essentially  with  three  factors — the 
angular  extent  of  the  retina,  the  curvature  of  the  optical  surface 
admitting  the  light,  and  the  effective  pupillary  aperture.  The  first  of 
these  is  the  most  important,  and  is  relatively  constant.     Variations, 

^  p.  r)76. 


670 


THE   EYE   IN    EVOLUTION 

Figs.  798  to  803. — The  Unioculab  Fields  of  Vertebrates. 


Fig.   798. — A  teleostean  fish. 
IIO° 


Fig.   799. — The  chameleon. 
IbO" 


Fig.  800.— An  owl. 


200 


Fig.   801. — A  primato. 
215° 


Fig.   802.— The  cat.  Fig.   803.— The  horse. 

Horizontal  meridian.     N,  nasal  ;    T,  temporal. 

however,  occur  ;  thus  the  wide  visual  field  of  the  horse  in  the  obliquely 
horizontal  meridian  (215°  to  228°)  is  largely  due  to  the  marked  forward 
prolongation  of  the  retina  on  the  nasal  side,  while  the  relatively  small 
field  of  many  birds  (the  owl,  110°)  and  also  of  some  deep-sea  fish  is  a 
consequence  of  the  small  extension  of  the  retina  in  their  tubular  eyes 
(Figs.  798  to  803). 


THE   PERCEPTION   OF   SPACE 


671 


The  curvature  of  the  primary  oj^tical  surface  is  also  of  importance 
since  it  determines  the  extent  of  the  sohd  angle  within  which  light  can 
be  refracted  into  the  eye.  Thus  the  human  cornea  subtends  only  60° 
of  a  circle  and  the  visual  field  averages  150°  ;  the  cornea  of  the  cat 
forms  a  much  more  prominent  curve  subtending  170°  of  arc  and  its 
visual  field  averages  200°  ;  the  cornea  of  the  chameleon  is  largely 
covered  by  the  lids  which  leave  only  a  small  central  aperture  roughly 

"^^  REFLECTION  OF  BOTTOM  ^^ 

HORI ZON  \£$^/.-^^^- 
'ROCK^AH 


'^:@^: REFLECTION  OF  BOTTOM.^ 


WATER 
SURFACE-- 


FiG.   804. — The  Upper  Visual  Field  of  a  Submerged  Fish. 

In  the  lower  figure  the  fish  is  seen  swimming  in  fresh  water  and  the  paths 
of  the  rays  of  hght  are  dehneated. 

In  the  upper  figure  is  shown  the  view  seen  by  the  fish  with  the  central 
circular  window  of  aerial  vision  near  the  periphery  of  which  bodies  become 
progressively  foreshortened  ;  around  it  is  reflected  a  view  of  the  bottom  mir- 
rored on  the  surface  of  the  water  (after  Walls). 


concentric  with  the  pupil  so  that  it  is  restricted  to  tubular  vision,  a 
disability  neutralized  by  the  extraordinary  mobility  of  its  eyes  (Figs. 
799  and  845).  In  under-water  vision  the  cornea  is  ineffective  as  a 
refractive  element  and  the  lens  serves  as  the  determinant  of  the  visual 
angle  ;  for  this  reason  the  lens  is  circular  and  situated  far  forward, 
closely  approaching  the  cornea  in  fishes,  often  protruding  beyond  the 
level  of  the  surface  of  the  head  ;  in  such  an  eye  the  field  is  determined 
solely  by  the  angular  extent  of  the  retina.  The  pupillary  aperture  is 
a  less   important   factor,    but   the   transversely   elongated   pupiLs   of 


672  THE   EYE   IN   EVOLUTION 

Ungulates  such  as  the  horse  increase  the  extent  of  their  field  in  the 
horizontal  meridian,  as  does  the  pear-like  elongation  of  the  pupillary 
aperture  in  the  aphakic  area  in  some  teleostean  fishes  ^  or  the  key-hole 
pupil  of  some  arboreal  snakes. ^ 

The  following  estimations  have  been  made  of  the  uniocular  visual  fields 
(Figs.  798-803)  : 

Teleostean  fishes— 110°-170°  (Verrier,  1930). 
Lizards — slightly  less  than  180°  (Kahmann,  1932). 
Birds— pigeon,  165°  ;   owl,  110°  (Rochon-Duvigneaud,  1921-23). 
Mammals — guinea-pig,  135°  ;   cat,  over  200°  ;   cattle,  205°  ;   horse,  average 
190°-195°    with    a    transverse    extension    to    215°    or    more    (Rochon- 
Duvigneaud,  1943  ;    Bresson,  1955). 

The  upper  visual  field  of  under-water  fishes  deserves  special 
mention  (Fig.  804).  When  looking  directly  upwards  the  fish  sees 
through  a  "window"  into  the  air  ;  but  in  a  slantingly  upwards  direction 
a  progressively  greater  degree  of  refraction  occurs  at  the  water-air 
interface  until  the  critical  angle  is  reached  (48-8°  in  fresh  water)  when 
the  rays  of  light  run  horizontally  along  the  surface  ;  objects  in  this 
hemispherical  aerial  field  therefore  become  progressively  smaller, 
dimmer  and  foreshortened  as  the  periphery  of  the  "  window  "  is  reached. 
Once  the  critical  angle  has  been  exceeded  rays  suffer  total  reflection 
so  that  outside  his  circular  "  window  "  the  fish  must  see  the  bottom 
mirrored  on  the  surface  of  the  water. 

THE    BINOCULAR   VISUAL   FIELDS    OF    VERTEBRATES 

Since  the  angle  subtended  by  the  uniocular  field  is  relatively 
constant,  the  extent  of  the  binocular  field  is  determined  almost 
entirely  by  the  position  of  the  eyes  in  the  head.  It  is  often  stated  that 
there  is  a  tendency  for  the  eyes  to  swing  from  the  lateral  to  the  frontal 
position  during  the  course  of  evolution  so  that  binocular  vision  as  it 
is  seen  in  the  Primates  eventually  becomes  possible.  This,  of  course, 
is  not  the  case,  for  the  swing  forward  in  the  visual  axes  has  occurred 
independently  many  times  within  the  vertebrate  phylum,  depending 
on  the  habits  and  requirements  of  different  species.  Thus  most 
freely  swimming  fishes  have  laterally  placed  eyes  but  the  flat-fishes 
which  lie  on  the  sea-bottom  have  upward-looking  eyes,  and  in  some 
deep-sea  fishes  they  are  directed  frontally  (Figs.  376,  379)  ;  the  same 
variation  is  seen  in  the  Birds  which  show  similar  gradations  between 
laterality  and  frontality,  and  again  in  the  Mammals.  The  extent  of  uni- 
ocularity  is  determined  rather  by  the  need  of  a  wide  panoramic  field  for 
the  hunted  animal  whether  it  be  fish,  bird  or  mammal,  for  its  existence  de- 
pends on  the  early  detection  of  enemies  in  whatever  direction,  and  rapid 
escape  from  them  (Figs.  805  and  806)  ;   the  extent  of  binocularity,  on 

1  p.  304.  2  p.  674. 


THE   PERCEPTION   OF   SPACE 


673 


the  other  hand,  is  determined  by  the  greater  vahie  of  the  fine  judgment 
rendered  possible  by  binocular  vision  in  pursuit  and  attack  by  the  pre- 
dator, in  its  ordinary  activities  by  the  arboreal  animal,  or  by  the 
Primate  the  eyes  of  which  have  become  accurately  correlated  with  the 
use  of  its  hands.  In  each  species  a  compromise  is  reached  between  the 
biological  value  of  the  reflexes  of  self-preservation  and  those  of  aggres- 
sion ;  the  former  depend  on  the  largest  possible  total  field  of  vision,  the 
latter  on  the  visual  refinements  resulting  from  the  near-coincidence  of 
the  optic  and  visual  axes  when  the  latter  intersect  on  the  fixation  point. 
To  attain  this  end  a  swing  forwards  of  the  optic  axes  of  the  primitive 


Figs.  805  and  806. — Binocular  Fields. 


'^/A/ocuL^«^ 


Fig.  805. — The  panoramic  field  of  a 
hunted  animal  (the  rabbit)  with  a 
small  binocular  segment  in  front  (10°) 
and  behind  (9^),  and  a  large  uniocular 
area  (170-5°  on  each  side). 


^LlND  &0 


of     a 

large 


Fig.  806. — The  binocular  field 
predator  (the  cat)  showing  a 
anterior  binocular  area  (120°)  a  large 
posterior  blind  area  (80  )  with  rela- 
tively small  uniocular  area  (80°). 


fish  is  necessary  and  since  this  entails  the  sacrifice  of  much  of  the  total 
field  it  can  only  be  adopted  by  animals  amply  sure  of  themselves  either 
because  of  their  strength  and  ferocity  or  their  superior  intelligence. 
The  wide  panoramic  field  was  undoubtedly  the  more  primitive  in 
evolutionary  sequence  ;  frontality  for  the  increased  efficiency  of 
binocular  vision  is  attained  first  by  a  swivelling  forwards  of  the  eyes 
so  that  by  a  reduction  of  the  angle  gamma  the  visual  axes,  intersecting 
on  the  fixation  point  in  front,  will  more  nearly  coincide  with  the  optic 
axes,  and  secondly,  to  make  this  mechanically  possible,  by  a  reduction 
in  the  divergence  of  the  orbital  axes  (see  Figs.  811-3,  837). 

In  addition  to  the  biological  vahie  of  binocular  vision  as  an  asset  to  predacity 
and  fine  manipulation,  an  increase  in  sensitivity  to  light  may  be  a  third  factor 
in  determining  its  acquirement  (Weale,  1955).  The  binocular  sensitivity  to  light 
is  greater  than  the  uniocular  (by  10%  in  man,  Pirenne,  1943).  This  may  account 
for  the  parallelism  of  the  visual  axes  in  some  strongly  nocturnal  types  such  as 

S.O. — VOL.  I.  43 


674 


THE   EYE   IN   EVOLUTION 


deep-sea  fishes  with  tubular  eyes  or  in  such  species  as  the  owl  or  Tarsius.  To 
such  animals  a  significant  lowering  of  the  light-threshold  may  be  of  considerable 
survival-value,  while  the  loss  of  the  panoramic  field  is  compensated  by  the 
security  of  darkness. 

Apart  from  the  positioning  of  the  eyes  in  the  head,  several  devices 
have  been  adopted  to  increase  the  extent  of  the  binocular  field.  Most 
of  these  we  have  already  noted.  Some  of  them  concern  the  configura- 
tion  of  the  eye — ^the  prominence  of  the  corneal  curvature   (or  the 


Fig. 


Fig.  807. 

Fig.   807. — The    Emerald    Tree-Snake,    Passerita. 

Showing  the  deep  facial  grooves  to  allow  accurate 
binocular  vision  (the  long  body  of  the  animal  is  coiled  up 
behind  the  head)   (photograph  by  Michael  Soley). 

Fig.  808. — The  Key-hole  Shaped  Pupil  of  the  Tree- 
snake,  Drtophis. 
To  show  the  aphakic  area,  the  aperture  being  designed 
to  direct  light  onto  the  temporal  fovea  in  the  interests  of 
binocular  vision. 


lenticular  curvature  in  Fishes)  ;  the  occurrence  of  a  horizontally  oval 
pupil  as  in  Ungulates  or  some  snakes  and  fishes  so  that  the  overlap  of 
the  two  fields  is  increased  in  the  horizontal  plane  ;  the  nasal  shift  of 
the  lens  by  the  transversalis  muscle  in  turtles,  lizards  and  some  snakes 
(Dryophis)  on  accommodation  so  that  the  visual  axes  are  directed 
forwards  more  nearly  parallel  to  the  axis  of  the  body  when  the  eyes 
are  converging  on  near  objects  in  front  (Fig.  808)  ;  and  the  marked 
nasal  asymmetry  of  the  eye  in  so  many  types  (many  Fishes  and  lizards, 
all  Bii-ds,  Ungulates  and  Carnivores)  whereby  the  ciliary  region  is 
narrowed  and  the  visual  retina  is  allowed  to  advance  far  forwards  on 
the  temporal  side  while  the  cornea  and  lens  are  tilted  nasally  so  that 
the  visual  axes  are  encouraged  to  intersect  towards  the  mid-line.    This 


THE   PERCEPTION   OF   SPACE  675 

tendency  may  be  said  to  be  carried  to  its  extreme  in  the  tubular  eyes 
of  some  abyssal  fishes  provided  with  a  lateral  accessory  retina  to 
overcome  the  marked  deficiency  in  the  field  which  would  result  from 
the  use  of  the  main  retina  alone. ^  In  addition,  the  anatomical 
configuration  of  the  orbits  and  skull  is  frequently  modified  to  eliminate 
as  far  as  possible  any  obstruction  to  the  vital  frontal  field,  the  most 
dramatic  instance  of  which  is  the  deep  groove  running  nasally  in  the 
cheek  of  certain  tree-snakes  in  wliich  the  eye  is  set  so  that  it  has  an 


Fig.  809. — -The  Goliath  Heron,  Ahuea  goliatu. 

To  show  the  deep  groove  in  the  skull  and  bill  to  allow  the  accurate 
fixation  of  prey  by  the  frontally  directed  eyes. 

uninterrupted  view  straight  ahead  (Fig.  807)  or  the  groove  in  the 
side  of  the  bill  of  the  heron  so  that  it  can  see  accurately  to  fixate  its 
prey  (Fig.  809). 

The  first  to  investigate  the  extent  of  the  binocular  field  in  the  various 
classes  of  Vertebrates  was  Johannes  Miiller  (1826)  who  measured  the  angles 
between  the  planes  of  the  orbital  margins  in  190  vertebrate  types,  making  the 
unjustified  asstimption  that  the  visual  axis  was  perpendicular  to  this.  These 
measurements  were  repeated  by  Leuckart  (1875)  and  Grossmann  and  Mayer- 
hausen  (1877)  and  their  absurdity  soon  became  obvious.  Thus  although  there 
is  little  difference  between  the  optic  and  orbital  axes  in  most  Fishes,  there  is 
more  in  the  horse,  more  still  in  the  cat,  W'hile  in  man  the  optic  axes  are  almost 
parallel  and  the  orbital  axes  diverge  by  45°  (Fig.  810).  A  similarly  painstaking 
and  elaborate  investigation  w^as  therefore  carried  out  by  the  last  authors  who 
measured  the  apparent  divergence  of  the  eyes  as  indicated  by  the  optic  axis 

1  p.  323,  Fig.  380. 


676 


THE   EYE   IN  EVOLUTION 


ORBITAL/ 
AXIS 

Fig.  810. — Diagram  to  Show  the  Relation  between  the  Orbital  Axis 
AND  Visual  Axis  in  Man. 

estimated  from  the  centre  of  the  cornea.  Unfortunately,  however,  this  method 
is  also  gravely  at  fault  since  the  optic  axis  rarely  coincides  with  the  visual  axis 
— when  the  latter  exists.  Indeed,  unless  there  is  an  area  centralis  of  acute 
vision  through  which  an  animal  habitually  orientates  itself  towards  an  object 
and  around  which  spatial  orientation  is  centred,  the  whole  concept  of  fixation 
along  a  visual  axis  is  meaningless  ;  only  in  those  animals  provided  with  an  area 
of  acute  vision  is  such  a  concept  possible  and  in  these  the  angle  gamma  between 
the  optic  and  fixation  axes  varies  between  5°  in  man  to  80°  or  85°  in  some  Fishes 
or  the  rabbit  with  laterally  placed  eyes  (Figs.  811  to  813).     When,  however, 


Figs.  811  and  812. — The  Angle  Gamma  in  Vertebrates. 


Fig.  811. — The  small  angle  gamma  of 
the  cat. 


Fig.  812. — The  large  angle  gamma  of 
the  rabbit. 


The  angle  y  measures  the  deviation  between  the  optic  axis  (O)  and  the  fixation  axis  (F). 


THE   PERCEPTION   OF   SPACE 


677 


visual  axes  exist  and  are  nearly  central  in  location,  such  measurements  are  of 
more  value  ;  for  this  reason  Lindsay  Johnson's  (1901)  extensive  observations 
on  Mammals  give  a  good  indication  of  the  binocularity  within  this  class. ^ 

The  most  efficient  and  reliable  method  yet  evolved  for  the  determination 


Most  Fishes  and 
Lagomorpha  80-85° 

Giraffe  75° 


Dog  25° 


Lemur  15° 


Cat  13' 


Fig.  813. — The  Angle  Gamjl^  in  the  Vertebrate  Phylum. 


of  the  binocular  field  is  that  which  depends  on  clamping  the  dissected  head  of 
the  animal  in  the  central  position  on  a  perimeter,  moving  a  light  along  the 
arc  and  observing  its  image  as  seen  through  the  sclera;  on  moving  the 
light  in  all  directions  the  extent  of  the  field  within  which  the  image  falls  on  the 
retinse  of  both  eyes  simultaneously  can  be  plotted  out  (Fig.  814).  In  the  hands 
of  Tschermak  (1902),  Rochon-Duvigneaud  (1921-23),  Verrier  (1930),  Kahmann 
(1932)  and  Pisa  (1939)  this  technique  has  given  sat ivsfactory  results. 

1  p.  688,  Fig.  837. 


678 


THE   EYE   IN   EVOLUTION 


Lamprey 


Fig.  814. — The  Experimental  Measurement  of  the  Visual  Field. 
A   light    is   moved   along   the  arc  of  a  perimeter  and  the  image  is  seen 
trans- sclerally  behind  the  globe.      The  dissected  head  of  the  animal  (a  bird) 
is  clamped  centially.    T.  temporal,  C,  central  fovea  (Rochon-Duvigneaud). 

The  binocular  field  of  cyclostomes  is  small,  but  with  an  angle 
of  160°  between  its  optic  axes  the  lamprey  should  have  an  effective 
although  minute  binocular  field  some  distance  in  front  of  its  head. 

The  binocular  field  of  fishes  is  generally  relatively  small  and  is 
represented  both  in  the  horizontal  and  vertical  planes.  In  the  usual 
type  of  fish  with  laterally  directed  eyes  and  a  cigar-shaped  body  the 
binocular  field  is  confined  to  a  relatively  narrow  belt  widest  in  front, 


Fig.  815. — The  Binocular  Visual  Field  of  a  Torpedo-shaped  Fish 
WITH  Laterally  Directed  Eyes. 


THE   PERCEPTION   OF   SPACE 


679 


Fig.  816. 


-The  Binocular  Visual  Field  of  a  Flat-fish  with  Upwardly 
Directed  Eyes. 


and  extending  a  considerable  distance  dorsally  (some  135°  from  the 
horizontal)  and  considerably  less  ventrally  (some  60°)  (Fig.  815)  ;  the 
area  behind  and  below  is  often  blind.  The  binocular  field  in  front 
varies  in  width  considerably,  from  exceptionally  small  values  of  10°  or 
less  {Box)  to  35°  or  greater  in  such  active  predators  as  the  trout  or 
pike  (Verrier,  1930  ;  Kahmann.  1932).  The  smallest  binocular  field 
yet  measured  in  any  Vertebrate  is  that  of  the  gurnard  {TrigJa)  of  2° 
(Verrier,  1928)  ;  that  of  the  carp  {Cyiyriyius)  is  very  little  more  (Rochon- 
Duvigneaud,  1922).  Depending  on  the  configuration  of  the  body  of 
the  fish  a  small  overlap  in  the  unilateral  fields  may  occur  posteriorly, 
particularly  in  eel-shaped  forms,  but  it  is  probabl}^  of  little  functional 
value  (Fig.  817).  In  bottom-living  fishes  such  as  the  selachian  skates 
and  rays  and  the  teleostean  flat-fishes,  the  binocular  fields  are  increased 
overhead  but  not  so  much  as  might  be  expected  since  the  two  eyes  on 
the  upper  side  of  the  head  preserve  to  a  considerable  extent  their  lateral 


Trout 


Ray 


Fig.   817. — The  Deep-sea  Snipe-eel,   Bokodi.wla  isFAys, 

Lateral  (above)  and  dorsal  (below)  views.  Owing  to  the  narrowness  of 
its  body  and  the  protrusion  of  the  eyes  there  is  a  small  posterior  binocular 
field  (after  Bertin). 


680 


THE   EYE   IN   EVOLUTION 


Opisthoproctus 


direction  ;  they  thus  retain  an  extensive  panoramic  field  at  the 
expense  of  a  much  larger  blind  area  below,  where,  resting  on  or  skim- 
ming near  the  bottom,  vision  is  in  any  event  useless  (Fig.  816).  In 
other  upward -looking  fishes  such  as  the  stargazer  (Astroscopus, 
Uranoscopus,  etc.)  and  some  abyssal  types  such  as  Opisthoproctus,  the 
dorsal  binocular  field  may  vary  between  25°  and  40°  or  even  more 
(Fig.  901).  A  few  pelagic  and  surface  fishes  have  their  eyes  canted 
downwards  to  joroduce  a  small  ventral  binocular  field  within  which 
much  of  their  predatory  interests  lie  (the  needle-fish,  Belone  ;  the 
flying-fish,  Pantodon). 


Fig.  818. — The  Pipe-fish,  Stnonathus. 

Showing  the  frontally  directed  eyes  to  allow  accurate  binocular  vision 
in  the  region  of  the  upturned  jaws  (seen  in  profile  in  the  lower  figure). 


Few  fishes  have  forward-looking  eyes  ;  such  a  configuration  occurs  in  some 
deep-sea  Teleosts  provided  with  tubular  eyes  {Qiganturus,  etc.),^  but  this  overlap 
of  two  small  fields  is  probably  a  device  to  improve  sensitivity  in  the  darkness 
of  the  abyss  (Weale,  1955).  A  frontal  direction  of  the  eyes  with  well-developed 
binocularity  may,  however,  be  adopted  for  reasons  of  space -perception  in 
the  jaipe-fish,  Syngnathiis  (Fig.  818),  As  this  fish  lies  immobile  on  the  bottom 
it  catches  its  prey  by  opening  its  jaws  just  as  its  victim  floats  above  its  mouth  ; 
the  forward-looking  eyes  with  their  temporal  foveas  should  allow  accurate 
binocular  vision  in  the  region  of  the  upturned  jaws  which  protrude  far  forwards 
at  the  end  of  the  elongated  snout. 

BINOCULAR  FIELD 


Fig. 


28- 
BLIND  AREA 

819. — The  Binocular  Field  of  the  Lizard,   Lacebta. 
1  p.  322,  Fig.  379. 


THE   PERCEPTION   OF   SPACE 


681 


Figs.  820  to  822. — Laterality  and  Frontality  in  Birds. 


Fig.  820.— The  Barbarj^  turtle  dove,  Streptopelia  roseogrisea. 

A  bird  with  laterally  directed  eyes  and  panoramic  fields  (Zool.  Soc. 

London). 


Fig.   821. — The  Chilean  eagle,  Gernnoaetus 
(photograph  by  Michael  Solej'). 


Fig.    822. — Savigny's  eagle-owl.  Bubo  as- 
Cdlaphus  (Zool.  Soc,  London). 


Birds  of  prey  with  frontally  directed  eyes  and  highly  develoj^ed  binocularity 

and  stereoscopy. 


682 


THE   EYE   IN   EVOLUTION 


Trachysaurus 


The  binocular  fields  of  amphibians  have  not  been  thoroughly 
explored,  but  particularly  in  Anurans  it  must  be  of  considerable  extent 
(Schneider,  1957). 

The  binocular  fields  of  reptiles  have  been  extensively  studied 
by  Kahmann  (1932)  who  found  that  they  were  more  constant  than  in 
Fishes  :  the  average  extent  is  between  20°  and  30°  with  extremes  at 
14°  in  the  lizard,  Trachysaurus,  and  at  46°  in  the  exceptional  tree- 
snake,  Dryophis. 

Among  the  Chelonians,  as  elsewhere  in  the  vertebrate  phylum,  the 
extent  of  the  binocular  field  varies  with  the  habits  of  the  animal  ; 


Ftgs.  823  AND  824. 

BINOCULAR   FIELD 
■30°-^' 


^^//VOARE^^° 


The  Binocular  Fields  of  Birds. 

BINOCULAR   FIELD 
60= 


Fig.  823. — The  pigeon.  Showing  a  small 
anterior  binocular  field,  large  (pano- 
ramic) uniocular  areas  and  a  small 
blind  area  behind. 


•"^D  ARE^ 


Fig.  824. — The  owl.  Showing  the  large 
binocular  field,  small  uniocular  areas, 
and  a  large  blind  area  behind,  charac- 
teristic of  a  predator. 


Clemmys 


Iguana 


the  smallest  is  seen  in  the  placid  herbivorous  tortoise,  Testudo  (18°),  the 
more  active  terrapin,  Clemmys,  has  a  field  of  34°,  while  the  snapping 
marine  turtle,  Chelydra,  which  is  an  activu  predator  of  small  fishes,  has 
a  binocular  field  of  38°  (Kahmann,  1933). 

Those  Crocodilians  which  have  been  investigated  have  been  found 
to  have  a  binocular  field  averaging  25°  (alligator,  24°  ;    cayman,  26°). 

Lizards  show  much  the  same  range  as  turtles.  The  smaller  types 
retain  a  wide  panoramic  field  for  protective  purposes  so  that  the  avail- 
able binocular  range  is  low — Trachysaurus,  14°  ;  Anguis  fragilis,  16°  ; 
Lacerta  and  Iguana,  18°  (Fig.  819)  ;  while  the  larger  and  more  militant 
types,  safe  in  their  strength,  enhance  their  aggressiveness  by  improved 
binocularity  {Zonurus  giganteus,  22°  ;    Varamis,  32°). 

Snakes  show  a  considerable  variation  in  their  binocular  fields  from 
20°  to  46°.     Among  representatives  of  the  great  central  family  of 


THE   PERCEPTION   OF   SPACE 


683 


Figs.  825  to  827. — The  Foveal  Arrangements  of  Birds  (Casey  Wood). 


Fig.    825. — The  titmouse.  To  show  the 

laterally    directed    eyes  with    central 

fove£e  (/)  for  panoramic  vision  (visual 
axes,  GH,  GI;  p,  pecten) 


Fig.  826. — The  swallow.  To  show  the 
laterally  directed  eyes  with  central 
foveas  for  panoramic  vision  (visual  axes, 
NI,  NH)  and  temporal  fovete  for  bin- 
ocular vision  (visual  axes,  TL,  TR). 


Fig.    827. — The   owl.      To   show   the   frontallj-   directed  eyes  with  temporal 
fovea?  for  binocular  vision  (visual  axes,  TF;  P,  pecten). 


684 


THE   EYE   TN   EVOLUTION 


Eagle 


Colubrids  the  binocular  field  is  very  variable  {Coluber,  20°  ;  Tarbophis, 
24°;  Zamenis,  28-32°;  Tropidonotus,  34-42°;  Malpolon,  38°;  Uromacer, 
40°  ;  Dispholidus,  42°),  as  also  in  the  more  primitive  Boidae  {Constrictor, 
34°),  while,  as  we  have  noted,  the  active  tree-snakes  {Dryophis, 
Passerita)  have  the  maximal  binocular  field  of  46°. 

The  binocular  fields  of  birds  may  be  classified  into  two  distinct 
types — that  of  birds  with  narrow  heads  and  laterally  directed  eyes 
with  a  central  fovea,  which  have  a  wide  panoramic  field  of  about  300° 
and  a  relatively  small  binocular  field  varying  from  10°  or  less  (6°  in 


BLIND  AREA- 


BINOCULAR 
FIELD  40° 

Fig.  828. — The  Visual  Trident  of  Birds  of  Prey. 

The  foveal  projections  in  the  hawk,  c  and  c,  the  projections  of  the  central 
fovese  for  panoramic  searching,  t,  the  projections  of  the  two  temporal  fovese 
for  stereoscopic  vision  in  attack  (after  Rochon-Duvigneaud). 

parrots)  to  30°  (Figs.  820  and  823),  and  that  of  birds  with  rounded 
heads  and  frontally  directed  eyes  which  have  a  relatively  small  total 
field  of  about  180°  with  a  relatively  large  binocular  segment  varying 
from  35°  or  40°  to  60°  or  70°  (Figs.  821-2  and  824).  As  occurs  in  most 
species  of  animal  the  former  are  timorous  in  type  and  granivorous  in 
habit  ;  their  survival  depends  on  early  awareness  of  an  enemy  and 
rapid  flight  ;  typical  examples  are  the  song-birds  or  the  pigeon.  Those 
with  an  extensive  binocularity  are  the  predators — the  swallows,  the 
falcons,  the  hawks,  the  eagles,  the  owls,  and  so  on — and  in  these,  while 
the  laterally -looking  central  fovese  are  ideal  for  searching,  the  temporal 
fovese  have  a  common  projection  straight  ahead  in  the  binocular  field 
so  that  their  judgment  of  distances  for  swooping  on  their  prey  while 
in  rapid  flight  attains  an  accuracy  which  can  only  be  described  as 
extraordinary  (the  visual  trident  of  Rochon-Duvigneaud,  1933) 
(Figs.  825  to  828). 


THE   PERCEPTION    OF   SPACE 


685 


WTiile  these  constitute  the  main  types  of  field  in  Birds,  it  is  to  be  expected 
that  in  a  class  so  diversified  exceptions  exist.  Some  pengviins  {Spheniscus)  have 
no  binocular  field.  The  snipe  has  eyes  set  far  back  in  its  head  giving  a  consider- 
able jDOsterior  binocular  field  so  that  it  can  see  a  potential  enemy  behind  and 


Fig.  829. — The  Bittern,  Botavrus  stellaris. 
A  delightful  photograph  showing  how  adept  the  bittern  is  at  concealment. 
When  disturbed  among  the  reeds  it  stretches  its  neck  with  the  beak  pointing 
upwards  and  stands  motionless  so  that  the  dark  stripes  running  down  the 
neck  and  breast  feathers  blend  with  the  reeds  among  which  it  hides.  In  the 
meantime,  the  downwardly  directed  ej'es  get  an  tmimpeded  view  and  the  bird  is 
enabled  at  the  same  time  to  watch  its  larood  at  its  feet  (Burton's  iStor^  of  Animal 
Life,  Elsevier  Pub.  Co.). 

above  when  feeding,  while  the  bittern  with  its  downward-pointing  eyes  has  a 
ventral  binocular  field  so  that  it  can  still  see  dowTiwards  with  both  eyes  when 
standmg  camouflaged  among  the  reeds  with  its  beak  pointed  upwards  towards 
the  sky  to  simulate  another  reed  (Fig.  829).  Occasionally  a  single  tj^De  may 
differ  widely  from  the  characteristics  of  the  family  ;  thus  alone  among  parrots 
the  kakapo  of  New  Zealand  {Stringops  labroptilus)  and  alone  among  ducks  the 


Stringops 


686 


THE   EYE   IN   EVOLUTION 


Figs.  830  to  834. — Panoramic  Vision  in  Placentals. 


Fig.  830. — Prejvalski's  horse, 
Equus  przeualskii. 


Fig.  831. — Somali  wild 
ass,  Equus  soma- 
liensis. 


Fig.    832. — Cotton's    giraffe, 
Girajfa  camelopardalis. 


To  show  the  configuration  of  the  eyes  for  panoramic  vision  in  Ungulates. 
The  laterally  directed  eyes  of  the  horse  have  a  considerable  binocvilar  field 
particularly  in  the  horizontal  direction  (see  Fig.  838).  In  the  giraffe,  because 
of  its  long  neck,  the  eyes  are  directed  downwards  to  obtain  the  greatest  field 
on  the  ground  (Zool.  Soc,  London). 


Fig.  834. 


Figs.  833  and  834. — The  positioning  of  the  eyes  in  the  rabbit  to 
allow  for  the  wide  panoramic  field  (see  Fig.  805). 


THE   PERCEPTION   OF   SPACE 


687 


blue   duck   of    New   Zealand    {Hymenola-tmis   malacorhynchus)    have   frontally- 
directed  eyes  and  considerable  binocular  fields. 

The  binocular  fields  of  mammals  also  vary  within  wide  limits 
(Figs.  830-9).  Some,  particularly  timid  tj^pes,  have  divergent  optic 
axes  and  a  small  binocular  field  ;  in  others,  particularly  predators,  the 
optic  axes  tend  towards  frontal  parallelism  and  the  binocular  field  is 
more  extensive.  The  first  class  is  exemplified  by  the  Rodents.  In 
the  rabbit  there  is  an  overlap  of  the  circumferential  uniocular  fields 

Figs.  835  and  836. — Binocular  Vision  in  Placentals. 


Fu;. 


C^oo. lilt'     (Jill. 


Fig.   836.— The  gorilla  (Zool.  Soc,  London). 

In  the  cat  frontality  is  required  for  predatory  purposes  (Fig.  806) ;    in 
the  primate  for  finesse  in  manipulation  (Fig.  839). 


688 


THE   EYE   IN   EVOLUTION 


m  ^ 


H    -73 


M 

■~' 

h-l 

Q 

4) 

^ 

D 

-i: 

W 

-M 

« 

H 

o 

n 

tn 

Z 

11 

< 

-rt 

l4 

rn 

o 

M 

X 

•- 

<; 

.a 

„ 

Ui 

o  ^ 

W      O 


CO 

rr 

W 

<u 

i-J 

^ 

s 

<< 

w 

K 

H 

THE   PERCEPTION   OF   SPACE 


689 


so  that  binocularity  is  attained  both  in  front  (10°)  and  behind  (9°) 
(Dubar,  1924  ;  Pisa,  1939)  (Figs.  805,  833-4).  In  the  squirrel  with  its 
protruding  eyes  the  binocular  field  is  more  extensive  and  varies  from 
25-30°.  The  Ungulates  occupy  an  intermediate  position  with  a 
binocular  field  varying  from  60°  to  80°  (Kahmann,  1933).  The  horse 
has  a  wide  binocular  field  in  front  (60°-70°)  and  a  wide  panoramic 
uniocular  segment  of  146°  so  that  it  sees  behind  along  a  line  parallel 
to  the  axis  of  its  body  (Figs.  830-1,  838)  ;  by  adopting  a  number 
of  devices  such  as  the  forward  prolongation  of  the  functional  retina 
on  the  nasal  side,  and  the  horizontally  oval  puj^il,  this  animal  thus 


Figs.  838  and  839 
BINOCULAR  FIELD 
■65' 


-The  Binocular  Fields  of  Placentals. 


,,x>P.   fjUp 


^^'^O   ARt'^ 


BLIND  AREA 


Fig.  838. — The  horse.  Showing  a  small 
binocular  field,  large  panoramic  uni- 
ocular areas  and  a  minute  blind  area. 


Fig.  839.  —  A  primate.  Showing  a 
large  binocular  field,  small  uniocular 
areas  and  a  large  blind  area. 


achieves  a  remarkable  field,  with  a  broad  binocular  area  in  front  and 
below  to  survey  the  ground  on  which  it  is  feeding  or  over  which  it  is 
galloping,  and  a  minimal  blind  area  behind.  The  elephant  has  the 
wide  uniocular  area  of  190°  and  a  binocular  field  of  67°.  The  goat  has 
a  binocular  field  of  63°,  the  ox  of  51-78°  (Pisa,  1939  ;  Bresson,  1955). 
Carnivores  with  eyes  set  more  frontally  have  larger  binocular  fields, 
that  of  dogs  varying  from  80°  to  116°  (Thieulin,  1927)  and  of  cats 
extending  to  120°  (Fig.  806)  ;  while  in  monkeys,  apes  and  man  it 
may  extend  to  140° — in  this  class,  as  we  have  seen,  in  the  interests  of 
finesse  in  manipulation  (Fig.  839). 

THE    OCULAR    MOVEMENTS    OF    VERTEBRATES 

Ocular  movements  in  Vertebrates  are  of  three  types  all  of  which 
are  of  primary  importance  in  spatial  perceptions  : 

(1)  Involuntary  movements,  associated  with  the  postural  reflexes 


Spider 
monkey 


690  THE   EYE   IN   EVOLUTION 

the  essential  purpose  of  which  is  compensatory  in  nature,  tending  to 
maintain  the  visual  field  as  far  as  possible  in  its  normal  orientation. 

(2)  Voluntary  movements  made  spontaneously  for  the  purpose  of 
changing  the  visual  field  to  allow  the  deliberate  exploration  of  space. 
While  the  involuntary  movements  tend  to  maintain  constancy  in  the 
visual  field,  voluntary  movements  are  designed  to  achieve  its  variation. 

(3)  Reflex  corrective  movements  associated  with  fixation  and 
fusion. 

It  is  interesting  that  apart  from  retraction  and  elevation  (move- 
ments associated  with  the  contact  reflex  of  the  cornea  and  with 
swallowing^),  no  ocular  movements  have  been  seen  in  Anurans  ;  nor 
have  they  in  Crocodilians  but  these  reptiles  have  received  little 
study  in  this  respect  ;  while  in  many  Birds  the  eyes  are  immobile 
and  even  reflex  involuntary  movements  are  often  largely  undertaken 
by  the  unusually  flexible  neck.^ 

INVOLUNTARY  OCULAR  MOVEMENTS.  We  havc  already  seen  that 
the  primary  function  of  vision  is  to  control  the  movements  of  the 
animal  ;  indeed,  the  primitive  photokineses  and  phototaxes  of  the 
lower  Invertebrates  survive  in  the  fundamental  postural  reflexes  of  the 
Vertebrates.  The  early  aquatic  Vertebrates  (Cyclostomes,  Fishes, 
Urodeles  and  larval  anuran  Amphibians)  were  provided  with  an 
elaborate  system  of  lateral  line  organs  attuned  to  respond  to  vibrations 
in  a  watery  medium  associated  with  a  labyrinth  designed  to  subserve 
a  postural  mechanism.  When  Vertebrates  left  the  water  for  land  the 
lateral  organs  disappeared  to  be  replaced  by  a  new  organ,  the  cochlea, 
designed  to  respond  to  vibrations  in  the  new  medium  (air),  but  the 
labyrinth  was  still  retained  and  was  associated  with  proprioceptive 
impulses  from  the  neck  and  limbs.  The  stimuli  from  the  lateral  organs 
and  the  labyrinths  were  carried  to  the  tegmentum  and  the  tectum  where 
they  were  associated  with  visual  stimuli  ;  the  stimuli  from  the  more 
lately  developed  organs  took  a  similar  course,  and  in  the  mid-brain  an 
important  group  of  centres  became  aggregated  controlling  the  reflexes 
concerned  with  the  acquirement  and  maintenance  of  posture  and 
associating  them  with  the  eyes.^  The  mechanism  involved  is  elaborate 
and  has  been  elucidated  in  a  classical  series  of  researches  by  the  great 
Dutch  physiologist,  Rudolf  Magnus,  and  his  associate,  de  Kleijn,  whose 
work  was  inspired  by  Sherrington's  analysis  of  the  phenomena  of 
decerebrate  rigidity.^  To  the  basic  concepts  advanced  by  these  workers 
little  fundamental  has  yet  been  added. 

The  primary  function  of  the  ocular  movements  was  therefore 

1  p.  345.  2  p_  695_ 

3  See  Figs.  712-.5. 

*  See  Sherrington,  1904^6  ;   Magnus,  1924. 


THE   PERCEPTION   OF   SPACE 


691 


postiaral  in  nature,  designed  to  maintain  the  visual  field  constant  in 
spite  of  the  movements  of  the  animal  ;  the  primary  function  of  the 
extra-ocular  muscles,  to  put  the  matter  paradoxically,  was  to  keep  the 
eyes  immobile  in  sjxice.  In  Cyclostomes  and  most  Fishes  this  is  the  only 
type  of  movement  which  exists,  and  every  movement  of  the  head  is 


Figs.  840  to  842. — Posttjeal  Reflexes. 


Fig.  840. — Tonic  labjrinthine  reflexes. 

The  rabbit  on  the  left  is  in  the  nor- 
mal position  ;  the  rabbit  on  the  right 
has  been  rotated  so  that  its  right 
side  becomes  lower,  and  the  movements 
of  the  eyes  are  indicated  by  the 
arrows  (after  Magnus). 


Fig.  841. — Tonic  neck  reflexes. 

On  rotation  of  the  head  upon  the 
trunk  the  movements  of  the  eyes  are 
indicated  by  arrows. 


Fig.     842. — Compensatory    movements    of    the    eyes    on    inclination 

of  the  head. 


associated  with  a  compensatory  movement  of  the  eyes.  For  this 
reason  the  extra-ocular  muscles  of  Fishes  have  a  uniquely  simple 
arrangement  designed  merely  to  accomplish  horizontal,  vertical  or 
wheel  rotatory  movements,  the  recti  taking  origin  from  the  apex 
of  the  orbit  and  rotating  the  globe  around  the  vertical  and  transverse 
axes,  the  obliques  arising  from  the  orbital  margin  and  rotating  the 
globe  around  the  antero-posterior  axis  (Fig.  293).     Such  movements 


692  THE    EYE   IN   EVOLUTION 

are  found  throughout  the  entire  vertebrate  phylum  in  all  animals 
wherein  ocular  movements  occur,  so  that  in  postural  attitudes  the 
eyes,  so  far  as  is  possible,  maintain  the  same  position  in  space,  while 
the  head  revolves  around  them  (Figs.  840  to  842).  It  is  important  to 
remember  that  the  static  postural  reflexes  are  not  associated  with 
vision  and  for  this  reason  they  occur  in  the  blind  and  in  the  decerebrate 
animal. 

These  ocular  movements  are  precisely  correlated  with  the  bodily  movements  ; 
their  regularity  is  seen  when  their  excursion  is  plotted  diagrammatically  in  the 
form  of  a  graph.  Fig.  843  illustrates  such  a  graph  taken  from  Benjamins  (1920) 
on  fish  :    positive  values  indicate  deviations  of  the  anterior  pole  of  the  cornea 


O  41  90  lis         ISO       225        270        325      360 

Fig.  843. — Rotation  or  the  Eye  of  the  Perch  about  the  Visual  Axis 
IN  Response  to  Rotation  of  the  Body  about  a  Transverse  Axis. 

Positive  values  indicate  deviations  of  the  anterior  pole  of  the  eye 
towards  the  belly  ;   negative  towards  the  back. 

The  ordinates  indicate  the  angle  through  which  the  anterior  pole  of  the  eye 
has  rotated.  The  abscissiB  indicate  the  position  of  animal  in  degrees 
(Benjamins). 


towards  the  belly,  negative  values  towards  the  back  ;    the  ordinates  represent 
the  angle  through  which  the  eye  has  rotated. 

The  ocular  movements  take  place  with  extreme  rapidity,  their  latent 
periods  being  measured  in  milliseconds  in  contrast  to  the  slow  postural  adjust- 
ments of  the  head  and  limbs,  de  Kleijn  established  that  rabbits  can  compensate 
head  movements  of  100°  about  a  bitemporal  axis  with  ocular  movements  of  a 
rapidity  of  this  order.  In  the  pigeon  comi^ensation  is  perfect  only  up  to  move- 
ments of  10°  and  the  eyes  move  back  either  by  a  slow  drift  or  a  quick  flip  so  that 
during  flight  accurate  fixation  of  the  next  landing  point  is  rapidly  possible 
(Whitteridge,  1956).  In  man  compensation  is  complete  during  head  movements 
of  up  to  30°  and  it  is  interesting  that  during  the  excursion  visual  acuity  is  not 
affected  (Merton,  1956). 

VOLUNTARY  OCULAR  MOVEMENTS.  Voluntary  movements  of  the 
eyes  are  a  later  evolutionary  development  adopted  in  the  interests  of 
vision  as  a  perceptual  process.  Within  the  vertebrate  phylum  an 
important  evolutionary  step  is  seen.    In  all  Vertebrates  below  Mammals 


THE   PERCEPTION   OF   SPACE 


693 


(with  the  exception  of  the  occurrence  of  reflex  corrective  movements 
for  convergence  in  a  few  species)  voluntary  moveinents  are  incoordinated 
in  the  sense  that  the  eyes  move  independently  of  each  other.  In  Mammals, 
and  in  Mammals  alone,  the  ocular  mov^ements  are  coordinated  in  the 
sense  that  the  movements  of  both  eyes  are  conjugated  with  a  consider- 
able degree  of  exactitude.  In  the  former  case  the  movements  are 
generally  staccato  and  quick  ;  in  the  latter  they  tend  to  be  deliberate. 
In  the  former  case  neither  eye  moves  symmetrically  or  synchronously 
with  its  fellow  for  not  only  may  the  eyes  move  in  different  directions  at 
the  same  time,  but  one  may  move  while  the  other  remains  fixed.  In 
the  first  case  there  is  a  complete  decussation  of  the  optic  nerve  fibres 
at  the  chiasma  (with  the  known  exception  of  a  few  fibres  in  some 
snakes)  ^  and  each  retina  is  projected  in  its  entirety  onto  different 
hemispheres  of  the  cerebral  cortex  ;  in  the  latter  case  there  is  a  partial 
decussation  at  the  chiasma  and  both  retinae  are  projected  onto  each 
hemisphere  of  the  cortex. 


Among  FISHES  spontaneous  ocular  movements  are  relatively  rare 
and  as  a  general  rule  the  visual  field  is  changed  or  a  moving  object  is 
followed  by  movements  of  the  body  while  the  eyes  remain  still. 
Spontaneous  movements  occur,  however,  in  several  species  of  active 
and  lively  pelagic  fishes  particularly  those  ^^'ith  a  fovea, ^  for  in  these 
tj^es  fine  ocular  movements  are  essential  if  an  area  specialized  for  visual 
acuity  is  to  be  usefully  employed  for  fixation.  But  in  these  fishes, 
apart  from  temporary  convergence  of  the  temporal  fovea  upon  prey  in 
some  species,  the  eyes  (and  fovese)  are  used  uniocularly,  and  even  those 
t}^es  which  have  a  temporal  fovea  quite  frequently  use  it  for  uniocular 
fixation  as  well  as  for  convergence  (the  blenny,  Blennius  ;  the  sea- 
bass,  Serranus  ;  the  Hawaiian  wrasse,  Julis  ;  the  weever,  Trachinus, 
etc.)  ;  they  are,  indeed,  the  only  Vertebrates  which  can  employ  a 
temporal  fovea  uniocularly  (Walls,  1942).  Exceptionally  sluggish 
fishes  such  as  the  sea-horse,  Hvppocatwpus,  and  the  cling-fish, 
LejMdogaster.  show  quick,  darting  and  wholly  dissociated  movements 
of  the  eyes  resembling  those  of  the  chameleon  ;  while  bottom-fishes 
such  as  the  flounders  (Pleuronectidse)  and  the  soles  (Soleidse),  when 
they  lie  half-buried  in  the  sand,  explore  the  surrounding  water  by 
independent  movements  of  their  pediculated  eyes.  Rochon-Duvigneaud 
(1943)  observed  small  independent  movements  of  the  eyes  in  tjrpes 
such  as  the  carp,  Cyprinus,  and  the  European  wrasse,  Labrus,  as  they 
lay  immobile  on  the  bottom  of  an  aquarium. 

A  greater  degree  of  movement  is  sometimes  seen  in  atypical  fishes 
with  eyes  adapted  for  aerial  vision.  Thus  in  the  Indian  mullet,  Mugil, 
which  swims  along  the  surface  feeding  upon  algae  and  caddis-fly  larvae, 
1  p.  392.  2  p.  309. 


Serranus 


Hippocampus 


Sole 


694 


Triturus  (female) 


THE   EYE   IN   EVOLUTION 

the  protruding  eyes,  well  raised  above  the  water  to  search  for  a  meal,  are 
freely  motile,  particularly  antero -posteriorly;  this  motility  is  matched 
only  by  the  chameleon-like  movement  seen  in  the  turretted  eyes  of  the 
mud-skipper,  Periophthalmus,  as  it  skips  about  on  land  upon  its  fins 
seeking  its  insect  food  in  the  search  for  which  the  eyes  move  about  in 
all  directions,  even  downwards,  as  if  set  upon  universal  joints  (Fig.  844). 

The  eyes  of  amphibians,  whether  Anurans  such  as  the  frog  or  toad 
or  Urodeles  such  as  Triturus  or  Salainandra,  have  never  been  observed 
to  exhibit  voluntary  movements,  although  the  lizard-like  insect- 
catching  habits  of  many  would  suggest  that  these  would  be  biologically 
useful. 


Fig.  844. — The  Mud-skippek,  Periophtbalmvs 

The  fish  is  on  land  and  the  prominent,  freely-motile  turreted  eyes  are 
well  seen  (c./.,  Fig.  386)  (photograph  by  Michael  Soley). 


Heloderma 


REPTILES  with  some  marked  exceptions  are  not  characterized  by 
active  ocular  motility  ;  most  of  them  when  quiescent  maintain  com- 
plete immobility  of  the  eyes.  Rochon-Duvigneaud  (1943)  divided 
them  into  two  types  :  the  first — crocodiles,  geckos  and  snakes — with  a 
wide  palpebral  fissure  and  an  extensive  field,  in  which  the  eyes  appear 
to  be  immobile  ;  the  second — Chelonians  and  most  lizards,  particularly 
the  chameleon — with  a  small  palpebral  aperture  and  with  mobile  eyes. 
The  turtles  and  tortoises,  like  some  teleostean  fishes,  can  coordinate 
their  eyes  in  lateral  movements  for  binocular  vision,  but  all  vertical 
movements  are  independent.  The  more  active  lizards  show  a  con- 
siderable ocular  motility — in  Lacerta  viridis,  the  excursion  is  40° — but 
all  voluntary  movements  are  independent  and  incoordinated  ;  in  the 
more  sluggish  and  many  nocturnal  forms  the  eyes  are  relatively 
immobile  ;  in  some  forms,  such  as  the  Gila  monster,  Heloderma, 
ocular  movements  are  apparently  absent  ;  but  the  chameleon  is 
notorious  in  the  animal  kingdom  for  the  extraordinary  excursion  and 
rapidity  of  the  movements  of  its  eyes  (Rochon-Duvigneaud,  1933). 

The  eyes  of  this  animal  bulge  from  the  head  while  the  small 
circular  palpebral  aperture  considerably  restricts  the  visual  field  ^  (Fig. 

1  p.  671. 


THE   PERCEPTION   OF   SPACE  695 

845)  ;  in  seeking  and  catching  insects  a  high  degree  of  ocular  mobihty 
is  therefore  essential;  moreover,  as  in  the  sea-horse,  the  movements 
of  the  body  are  sluggish  and  the  eyes  and  the  tongue  are  the  only  parts 
of  the  animal  to  exhibit  the  activity  necessary  to  maintam  its  livelihood. 
As  it  sits  motionless,  the  eyes  constantly  and  diligently  explore  the 
surrounding  environment  uniocularly,  swivelling  like  turrets  through 
an  angle  of  180°  horizontally  and  90°  vertically  in  complete  incoordma- 
tion,  one  eye,  for  example,  looking  straight  forward  while  the  other 
looks  backwards.  When  an  insect  is  seen,  however,  the  eyes  suddenly 
become  coordinated  in  extreme  convergence  so  that  both  central  foveas 


Fig.   84."). — The  Chameleon,  Chameleon  bilepis. 

The    freely-motile    eyes    with    the   minute    palpebral    apertures    look   in 
different  directions  (c./..  Fig.  420)  (photograph  by  Michael  Soley). 

are  brought  to  bear  upon  the  prey,  and  the  long  sticky  tongue,  impelled 
by  its  own  elasticity  and  by  the  forcing  of  blood  into  the  hollow  spaces 
within  it,  shoots  out  as  far  as  the  length  of  its  body  with  extreme 
rapidity  and  infallible  accuracy  to  catch  any  insect  within  its  reach. 

Snakes  show  little  ocular  motility  ;  swinging  the  head  from  side 
to  side  pendulum-like,  they  examine  an  object  first  with  one  eye  and 
then  with  the  other  and  then  binocularly,  the  head-movements  taking 
the  place  of  ocular  movements  ;  even  those  possessed  of  a  temporal 
fovea,  such  as  the  tree-snakes,^  do  not  require  to  converge  their  eyes 
to  achieve  binocularity. 

BIRDS,  because  of  the  enormous  size  of  their  eyes  filling  the  bony 
orbits,  have  necessarily  very  restricted  movements — if  any.  Slight 
horizontal  movements  are  often  the  only  ones  to  be  represented  :  the 
eyes  of  the  owl,  for  example,  cannot  be  moved  passively  even  with  a 

1  p.  .388. 


696 


THE   EYE   IN   EVOLUTION 


Cormorant 


pair  of  pliers.  To  a  large  extent  this  immobility  is  compensated,  as  in 
snakes,  by  the  extreme  mobility  of  the  neck,  the  constant  agitated 
swivelling  and  nodding  movements  of  the  head  continually  varying 
the  visual  fields  ;  the  hawk,  for  example,  can  swivel  its  head  around 
through  an  angle  of  180°,  the  owl,  of  270°.  Moving  objects  are  thus 
followed  by  movements  of  the  head  and  gross  ocular  reflex  movements 
are  taken  over  by  neck  movements.  The  presence  of  two  fovese  also 
lessens  the  need  for  movements  of  the  eyes  while  the  nasal  asymmetry 
of  the  eye  and  its  dioptric  elements  supply  the  amount  of  convergence 
necessary  for  the  binocular  function  of  the  temporal  foveas  so  that 

convergent  movements  for  this  purpose 
are  not  usually  required.  It  is  true  that 
limited  ocular  movements  are  seen  in 
some  species,  particularly  the  parrots, 
large-beaked  birds  such  as  the  hornbills 
or  the  toucan,  and  aquatic  birds  such  as 
the  crane,  the  seagull,  the  penguins  and 
the  cormorant  (Rochon-Duvigneaud, 
1943).  In  these,  however,  movements 
of  the  two  eyes  are  always  dissociated 
except  for  movements  in  the  horizontal 
field  in  the  interests  of  convergence. 

MAMMALS  are  unique  in  their  ocular 
movements,  whether  lateral,  vertical, 
oblique  or  convergent,  in  so  far  as  they 
are  always  conjugated.  In  the  lower 
classes,  however — Insectivores,  Cliirop- 
tera,  Edentates  and  Rodents — move- 
ments are  very  restricted,  if,  indeed, 
they  exist  ;  even  visually  conscious 
Rodents  such  as  the  squirrel  and  the  marmot  hardly  move  their 
eyes  although  they  are  busily  engaged  in  exploring  space  intently 
all  the  while,  doubtless  because  in  their  cone-rich  retina  visual 
acuity  is  everywhere  excellent  (Rochon-Duvigneaud,  1943)  ;  con- 
versely in  the  mouse  or  the  rat  the  eyes  are  kept  motionless,  probably 
because  vision  is  everywhere  so  poor  (Walls,  1942).  In  Ungulates 
ocular  movements  are  more  conspicuous  ;  the  eyes  of  the  elephant, 
however,  are  relatively  immobile  despite  the  enormous  size  of  the 
extra-ocular  musculature. ^  In  the  larger  Carnivores  of  the  cat  and 
dog  families,  they  are  freer  ;  and  in  the  foveate  higher  Primates 
they  are  most  conspicuous  of  all.  In  all  cases,  however,  as  in  man,  they 
are  largely  supplemented  by  movements  of  the  neck,  and  the  head  is 

1  p.  497. 


Fig.  846. — A  Drawing  of  Tarsius. 

Looking  directly  behind  itself  ; 
to  show  the  extraordinary  mobility 
of  the  neck  to  compensate  for  the 
immobility  of  the  eyes. 


THE   PERCEPTION   OF   SPACE  697 

usually  turned  so  that  an  object  of  attention  is  brought  within  the 
binocular  field  ;  even  in  a  Primate  such  as  Tarsius,  the  large  eyes  of 
which  are  practically  immobile,  ocular  movements  are  largely  taken 
over  by  movements  of  the  neck  which  can  rotate  through  an  angle 
of  180°  so  that  the  animal  can  look  directly  behind  without  incon- 
venience (Fig.  846). 

UNIOCULAR   AND    BINOCULAR    VISION 

It  has  often  been  implied,  and  indeed  said,  that  animals  with 
laterally  placed  eyes  and  panoramic  vision  and  with  a  total  chiasmal 
decussation  cannot  fuse  the  two  uniocular  fields  ;  the  logical  implica- 
tion is  that  two  separate  uniocular  impressions  are  appreciated  so  that 
the  only  alternative  to  rivalry  or  diplopia  in  the  binocular  field  would 
be  that  suppression  alternates  between  the  two  retinae.  Partial 
decussation  of  the  sensory  paths  and  the  projection  of  each  half-field 
onto  the  same  hemisphere  has  thus  been  taken  as  the  anatomical  basis 
of  fusion  and  stereoscopy.  Such  a  view  is  without  firm  foundation.  It  is 
our  universal  experience  that  visual  impressions  from  our  semilunar 
uniocular  fields,  the  afferent  fibres  from  which  suffer  complete  decussa- 
tion and  are  relayed  to  separate  hemispheres  in  the  cortex,  are  in- 
extricably mixed  without  rivalry  with  those  from  the  binocular  field 
and  form  a  unity  with  them  ;  the  sensory  impression  is  comparable 
to  our  unitary  appreciation  of  an  object  such  as  a  pencil  when  touched 
with  the  fingers  of  each  hand.  There  is  no  reason  why  the  uniocular 
fields  of  animals  cannot  be  fused  to  form  a  single  perceptual  whole 
even  although  they  are  appreciated  by  different  halves  of  the  brain  just 
as,  if  we  close  one  eye,  the  two  segments  of  the  resulting  uniocular 
field  are  seen  as  one  although  they  are  perceived  by  the  synthesis 
of  the  activity  of  different  cortical  hemispheres.  The  whole  behaviour 
of  Vertebrates,  the  preference  for  binocular  vision  when  visual  accuracy 
is  required,  and  the  extreme  accuracy  in  spatial  judgments  of  bifoveate 
vision  in  a  chameleon  or  a  bird  of  prey  justify  the  conclusion  that, 
despite  total  decussation  at  the  chiasma,  the  Vertebrates  below 
Mammalia  enjoy  binocular  single  vision  with  a  considerable  degree  of 
depth  perception  and  stereopsis  in  the  overlapping  parts  of  the  fields 
owing  to  the  appreciation  of  binocular  parallactic  clues.  In  all 
Vertebrates,  whether  they  are  provided  with  a  complete  or  partial 
decussation  of  the  optic  nerve  fibres,  binocular  vision  is  a  percejJtual 
process,  the  singleness  of  which  represents  the  product  of  a  synthesis 
which  is  built  upon  already  elaborated  uniocidar  sensations. 

The    historical    evokition    of   these    ideas    is    interesting.      The    structural 
hypothesis,  depending  on  the  direct  continuity  of  the  neural  apparatus  particu- 
larly as  seen  at  the  chiasma,  was  taught  by  Galen  ^  and  elaborated  by  Isaac 
'   De  usu  partium  corporis  humani. 


698  THE   EYE   IN   EVOLUTION 

Newton  (1704),  WoUaston  (1824),  J.  Muller  (1826)  and  others.  An  alternative 
view  explained  the  phenomenon  of  binocular  vision  by  denying  its  existence  and 
assuming  that  one  eye  only  was  able  to  see  at  a  time  ;  this  was  originally  offered 
by  Porta  (1593)  and  elaborated  by  Gassendi  (1658)  and  du  Tour  (1743),  and  in 
miore  recent  times  by  such  natural  philosophers  as  Wundt  (1862).  A  third  view, 
originating  with  Kepler  (1611)  and  elaborated  by  Porterfield  (1759)  and  main- 
tained by  such  observers  as  Sherrington  (1906)  and  Ovio  (1927),  postulated  a 
purely  perceptual  basis  for  the  phenomenon  ;  so  far  as  sensory  perception  is 
concerned  the  chiasmal  decussation  or  the  laterality  of  the  cerebral  terminal  is 
immaterial,  for  a  mental  synthesis  can  deal  with  either  topographical  scheme. 

It  would  appear  that  a  reservation  may  have  to  be  made  in  this  generaliza- 
tion in  the  phenomenon  of  the  interocular  transfer  of  impressions.  In  man, 
an  eye  trained  to  a  task  while  the  other  eye  is  occluded  can  automatically 
be  replaced  by  the  latter  without  detriment  to  his  performance  ;  in  infant 
chimpanzees  such  a  transference  is  not  complete  but  the  task  can  be  re-learned 
by  the  second  eye  very  readily  (Chow  and  Nissen,  1955).  In  fish,  however, 
Sperry  and  Clark  (1949)  found  that  this  did  not  appear  to  be  the  case  ;  if  gobies 
(Bathygobius)  were  trained  to  swim  towards  the  upper  of  two  objects  with  one 
eye  occluded,  occlusion  of  the  other  eye  was  followed  by  a  large  increase  in 
mistakes  which  were  immediately  rectified  when  the  first  eye  was  again  occluded. 
In  pigeons,  however,  Seigel  (1953)  fovmd  that  they  were  able  to  effect  immediate 
transfer  of  a  circle-versus-triangle  discrimination  from  an  eye  used  in  training 
to  the  other  not  so  used  ;  such  an  immediate  transfer  occurs  in  cats  even  after 
section  of  the  crossed  fibres  of  the  chiasma  (Myers,  1955). 

If  decussation  of  the  optic  nerve  fibres  is  without  great  sensory 
significance,  the  occurrence  of  partial  decussation  in  the  Placentals  and 
the  gradual  increase  in  the  number  of  uncrossed  fibres  until  they  reach 
almost  50%  of  the  total  in  the  Primates — ^presumably  a  progressive 
element  in  evolution — must  receive  some  other  explanation.  The  fact 
remains  that  (with  the  exception  of  the  presence  of  some  non-decus- 
sating fibres  in  snakes  the  significance  of  which  is  unknown)  in  animals 
below  Placentals  decussation  is  complete  no  matter  how  large  the 
binocular  field,  in  Placentals  decussation  is  partial  no  matter  how 
small  the  binocular  field.  It  is  obvious  that  if  a  high  degree  of  stereo- 
scopic vision  is  to  be  attained,  a  mechanism  of  extreme  exactitude 
must  be  developed  to  ensure  that,  so  far  as  it  is  possible,  the  two  eyes 
move  as  a  unity,  preserving  a  mutual  relationship  so  that  in  all 
positions  the  images  of  each  object  binocularly  fixated  will  fall  on 
corresponding  points  of  the  retinse  which  have  become  functionally 
associated  with  each  other.  If  adequate  motorial  coordination  is  to 
be  attained  it  is  essential  that,  the  two  eyes  be  controlled  by  the  higher 
centres  as  a  unitary  organ  ;  just  as  binocular  sensations  are  regarded 
introspectively  as  balanced  in  the  median  sagittal  plane  of  the  head, 
the  taxis  of  the  eyeballs  must  be  transferred  each  from  its  own  sagittal 
plane  to  the  median  sagittal  plane  of  the  body.  As  is  seen  in  the  limbs, 
the  taxis  of  the  muscles  situated  (functionally)  to  the  right  (for  example, 
the  right  external  rectus  and  the  left  internal  rectus)    is  entrusted  to 


THE   PERCEPTION   OF   SPACE  699 

the  left  hemisphere.  Although  the  projection  of  the  two  corresponding 
retinal  areas  upon  the  same  cortical  field  is  not  essential  for  the  fusion 
of  their  several  sensory  impressions,  such  a  confluence  of  sensory- 
conductors  is  necessary,  as  was  pointed  out  by  Mott  (1905)  and 
Sherrington  (1906),  if  they  are  to  have  access  to  a  common  efferent 
(motor)  path  which  both  must  use  if  a  coordinated  mechanism  is  to 
result. 

The  complete  decussation  of  the  optic  nerve  fibres  at  the  chiasma 
in  Vertebrates  below  Mammalia  and  their  partial  decussation  in 
Mammalia  is  thus  associated  with  the  fact  that  the  latter  is  the  only 
class  of  Vertebrates  wherein  the  ocular  movements  are  coordinated. 
Moreover,  the  latter  is  the  only  class  of  Vertebrates  wherein  the  ocular 
motor  nuclei  in  the  mid-brain,  particularly  those  of  nerves  III  and  VI, 
are  intimately  related  with  a  system  of  crossed  association  fibres 
(Kappers,  1920).  The  anatomical  association  of  the  visual  fibres  is  thus 
an  evolutionary  adaptation  correlated  with  motor  rather  than  sensory 
events,  and  marks  a  distinct  stage  in  the  progress  of  the  development 
of  binocular  vision  into  a  highly  integrated  mechanism  of  ever-increasing 
exactitude.  Without  complete  motor  coordination  the  continually 
shifting  system  of  local  signs  of  direction  characteristic  of  animals 
with  uncoordinated  eyes  could  not  have  been  replaced  by  a  functionally 
established  system  of  corresponding  points  and  accurately  fixed  local 
signs  of  direction,  nor  would  it  have  been  possible  to  introduce 
additional  clues  to  the  judgment  of  distances  such  as  physiological 
diplopia.  With  such  coordination,  community  of  sensation  becomes 
reinforced  by  community  of  action.  Significantly,  the  appearance  of 
such  coordination  in  Mammals  coincides  with  the  fact  that  in  these, 
for  the  first  time,  the  visual  processes  are  transferred  from  the  tectum 
and  the  mid-brain  to  the  cortical  level  ^  ;  only  in  Mammals,  therefore, 
is  such  coordination  possible. 

Kappers  (1920)  accounted  for  the  partial  decussation  of  the  visual  fibres 
by  the  theory  of  neurobiotaxis,  a  hypothesis  by  which  he  has  endeavoured  to 
explain  the  complicated  migration  of  nerve  centres  and  nerve  tracts  in  phylo- 
genetic  history,  and  the  seemingly  peculiar  location  and  relation  in  which  this 
has  resulted  in  the  higher  animals.  In  its  essentials  the  theory  postulates  that 
the  migration  and  final  arrangement  of  neural  elements  are  determined  by  an 
association  of  function,  the  determining  force  being  physico-chemical.  The 
intimate  nature  of  such  a  force  or  the  manner  of  its  action  is,  of  course,  highly 
speculative — and  admittedly  so  ;  but  such  a  conception,  correlating  structure 
and  function,  Is  essentially  rational  in  its  biological  implications,  and  clears  up 
many  difficult  points  in  the  anatomy  of  the  central  nervous  system  of  the  higher 
animals,  in  its  comparative  anatomy,  and  in  its  embryology. 

Those  parts  of  the  central  nervous  system  which  are  associated  with  the 
photostatic  fimctions  of  vision  provide  several  peculiarly  apt  illustrations  of  this 
theory.      The   most   outstanding,   perhaps,    is   the   position   of  the   oculomotor 

1  p.  543. 


700  THE   EYE   IN   EVOLUTION 

nuclei,  with  their  close  anatomical  relationship  to  the  posterior  longitudinal 
bundle  and  the  vestibular  system,  their  secondary  changes  in  position  correspond- 
ing to  changes  in  the  paths  of  the  optic,  vestibular  and  coordinative  reflexes. 
In  the  present  case,  when  the  eyes  are  directed  frontally  but  are  in  a  non- 
converging  position,  the  nasal  fibres  of  one  retina  and  the  temporal  fibres  of  the 
other  are  stimulated  simultaneously  by  laterally  incident  light  ;  these  fibres 
therefore  rvm  in  contiguity  in  the  central  nervous  tract.  Again,  with  frontally 
incident  light,  the  image  is  formed  on  the  temporal  sides  of  the  retinae  of  both 
eyes.  Thus  the  temporal  region  of  one  retina  works  partly  with  the  opposite 
temporal  region  and  partly  with  the  opposite  nasal  region,  whereas  the  nasal 
regions  never  work  together.  Hence  the  temporal  fibres  from  both  sides  must 
also  run  in  contiguity,  and  therefore  there  are  both  direct  and  crossed  (macular) 
temporal  fibres  in  each  tract. 

Associated  with  the  motorial  coordination  of  the  eyes  the  pupillary  reactions 
are  interesting.  There  is  a  consensual  pupillary  reaction  in  the  selachian  rays 
and  in  the  pigeon,  but  so  far  as  is  known  in  all  the  other  lower  Vertebrates 
wherein  the  pupils  react  to  light — Fishes,  Amphibians,  Reptiles  and  Birds — the 
reaction  is  unilateral  and  confined  to  the  stimulated  eye  (Rochon-Duvigneaud, 
1943).  In  the  lower  Mammals  such  as  the  Rodents  the  same  unilaterality 
obtains  ;  a  faint  consensual  reaction  is  seen  in  Carnivores  such  as  the  cat  and 
dog  in  which  the  non-decussation  of  nerve  fibres  becomes  considerable  ;  while 
only  in  Primates  wherein  a  hemi-decussation  occurs  do  the  sensory  and  motorial 
reactions  become  fully  conjugated  and  the  responses  of  the  two  pupils  become 
almost  equal  when  one  eye  is  stimulated. 


SPATIAL   JUDGMENTS 

While  no  systematic  research  has  been  devoted  to  the  subject,  the 
visual  performance  of  Vertebrates  leaves  little  doubt  that  spatial 
perceptions  of  some  accuracy  are  a  universal  attribute  of  vertebrate 
vision,  probably  crude  in  the  uniocular  field,  often  of  great  accuracy  in 
the  binocular  field  and  sometimes  of  incredible  accuracy  with  bifoveate 
vision.  If  we  reason  from  our  own  subjective  impressions — always,  it 
is  to  be  remembered,  a  most  dangerous  thing  to  do — it  is  probable  that 
in  the  uniocular  field  these  perceptions  are  derived  from  such  factors 
as  the  retinal  size  of  the  images  of  known  objects,  overlap  of  contours, 
the  placement  of  shadows,  aerial  perspective  and  uniocular  parallax, 
often  with  the  help  of  accommodation.  Within  the  binocular  field 
clues  of  greater  accuracy  are  provided  by  the  disparity  of  the  retinal 
images  seen  by  the  two  eyes  and  the  effort  expended  in  convergence, 
while  in  Placentals  in  which  the  eyes  are  coordinated  physiological 
diplopia  probably  becomes  a  potent  factor  in  stereopsis  for  near  objects, 
together  with  parallactic  localization  of  an  object  in  space. 

That  uniocular  clues  do  play  a  considerable  part  in  spatial 
perceptions  in  animals  is  obvious  from  the  visual  judgments  formed 
by  many  animals  with  panoramic  vision,  and  is  confirmed  by  several 
observations.  We  have  already  noted  the  jerky  or  oscillatory  move- 
ments of  the  head  so  constantly  seen  in  many  birds   ;     viewing  space 


THE   PERCEPTION   OF   SPACE 


701 


in  this  way  from  a  succession  of  angles  in  rapid  succession,  parallactic 
observations  must  be  made  providing  a  basis  for  the  estimation  of 
distance  and  relief  ;  in  this  rapid  process  the  simultaneous  parallactic 
clues  of  binocular  vision  are  replaced  by  the  successive  clues  of  uniocular 
vision.  It  was  stressed  by  Grinnell  (1921)  that  before  pecking  their 
food  birds  adopt  the  similar  habit  of  "  rapid  peering  " — cocking  their 
heads  now  to  one  side  and  now  to  the  other  to  view  the  grain  or  the 
berry  from  different  aspects  and  localizing  it  against  the  background 
from  different  angles.  The  pendular  head  movements  of  snakes  and 
the  nodding  of  many  types  of  lizards  probably  come  into  the  same 
category.  It  was  found  by  Bemier  (1938),  for  example,  that  one-eyed 
chicks  peck  as  accurately  as  two-eyed  specimens,  relying  (presumably) 
largely  on  uniocular  parallax  for  the  accuracy  of  their  judgments  of 
distances.  The  importance  of  shadow-effects  was  also  brought  out  by 
Bemier  ;  if  the  seed-grains  were  illuminated  in  such  a  way  that  their 
shadows  were  eliminated,  his  chicks  neglected  them,  while  painted 
representations  of  shadowed  grains  deceived  them.  The  judgments  of 
distances  possible  by  uniocular  vision  may,  indeed,  be  of  extreme 
accuracy.  We  have  already  commented  on  the  deft  way  in  which  the 
chameleon,  suddenly  converging  both  eyes  upon  an  insect,  captures  it 
without  fail  with  its  long  tongue  ;  while  ordinarily  both  foveae  seem 
to  be  employed  in  this  action,  nevertheless  Canella  (1936)  found  that 
after  the  loss  of  an  eye  it  could  catch  its  prey  with  the  same  infallibility, 
retaining  while  so  handicapped  its  accurate  evaluation  of  three- 
dimensional  space. 

Binocularity,  however,  with  the  possibility  of  stereopsis  must  add 
considerably  to  the  animal's  appreciation  of  space  and  its  judgment  of 
distances,  particularly  near  at  hand.  That  such  judgments  are  often 
good  and  occasionally  superb  is  obvious  from  the  many  instances  of 
behaviour  that  could  be  cited.  The  extraordinary  agility  of  small 
FISHES  darting  rapidly  up  a  shallow  stream  so  quickly  as  almost  to 
escape  human  observation  and  at  the  same  time  avoiding  all  obstacles, 
provides  a  good  example  of  the  excellent  judgment  of  distances  possible 
in  some  species.  The  schooling  behaviour  of  many  species  induces  fine 
visual  judgments  :  vast  aggregations  of  fish,  both  fresh-water  and 
marine,  wherein  each  individual  maintains  its  position  alongside  its 
neighbours  retaining  a  constant  distance  between  each  other  like  ranks 
of  soldiers  on  parade  can  only  be  based  on  extremely  precise  visual 
orientations  (Morrow,  1948  ;   Gudger,  1949)  (Fig.  847). 

The  judgments  of  size  by  certain  fishes  is  exemplified  by  their 
response  to  visual  illusions.  Herter  (1930)  found  that  the  response  to 
such  illusions  was  the  same  as  in  human  beings  ;  fish  trained  to 
feed  from  the  larger  of  two  black  circles  chose  the  left-hand  circle  in 
Fig.  848.     The  astonishing  visual  accuracy  of  the  archer-fish,  Toxotes 


Toxotes  jaculator 


702  THE   EYE   IN   EVOLUTION 

jaculator,  has  frequently  been  quoted  to  illustrate  how  highly  developed 
the  judgment  of  distances  may  be  in  a  fish  ;  while  swimming  it  will 
spit  a  jet  of  water  at  an  insect  flying  three  feet  above  the  surface 
with  an  astonishing  accuracy,  overwhelming  it  in  the  air  and  devouring 
it  when  it  has  been  brought  down  to  the  surface  of  the  water.  An 
animal,  particularly  one  not  provided  with  a  fovea,  which  can  overcome 
the  visual  disabilities  of  localization  in  air  while  immersed  in  water  ^ 


Fig.  847. — The  Spatial  Orientation  of  Fishes. 

Resting  trout  lying  in  the  Brule  River,  Minnesota.  Note  their  arrange- 
ment in  regular  and  disciplined  ranks  (Gudger  ;  from  Thorpe's  Learning  and 
Instinct  in  Animals,  Methuen  and  Co.). 


and  can  still  so  deftly  impale  a  flying  insect  must  have  an  unusually 
excellent  judgment  of  distances. 

Similarly  in  amphibians  and  reptiles,  the  accuracy  of  the  insect- 
catching  activities  of  the  frog,  the  toad  or  the  lizard  betoken  well- 
developed  spatial  judgments  ;  but  in  some  birds  this  faculty 
appears  to  be  even  of  a  higher  standard.  This  particularly  applies 
to  birds  of  prey,  which  swoop  down  on  their  quarry  with  unerring 
accuracy  from  astonishing  heights,  a  feat  doubtless  rendered  possible 
by  the  bi-temporal  fovese.  The  accuracy  of  the  hawk,  provided  with 
two  temporal  foveae,  in  swooping  on  its  prey  upon  the  ground  at  great 
speed  and  with  great  precision  is  in  strong  contrast  to  the  conduct  of 

1  p.  672. 


THE   PERCEPTION   OF   SPACE 


703 


a  bird  such  as  the  gannet,  Sula  hassana,  which  is  provided  only  with 
laterally  directed  central  foveae,  and  feeds  by  diving  for  fish.  Portier 
(1923)  found  that  if  he  fastened  fish  to  floating  pieces  of  wood  the 
birds  dived  for  them  with  great  directional  accuracy  but,  misjudging 
the  distance,  impaled  their  open  beaks  in  the  wood,  a  lack  of  precision 
which  would  bear  no  penalty  were  the  fish  swimming  freely  in  the 
yielding  water. 


Fig. 


848. — Visual    Illusions    with    Cikculak    Figures    used    in    Training 

or  Fish. 


The  black  circle  surrounded  by  small  circles  appears  larger  than  a  circle 
of  the  same  size  surrounded  by  larger  circles  (after  Herter,  1930). 

It  is  interesting  that  the  visual  judgment  of  birds  is  subject  to 
the  same  illusions  as  ours,  showing  its  basic  similarity  on  the  perceptual 
level.  Thus  Revesz  (192-4-25)  showed  that  hens  and  chicks  trained  to 
peck  for  the  smaller  of  two  figures  (rectangles,  squares,  circles,  etc.) 
when  presented  with  two  drawings  illustrating  the  Jastrow  illusion, 
pecked  preferentially  from  the  upper  (Fig.  849).  Similarly  in 
experiments  with  doves  (Warden  and  Baar,    1929)  and  with  chicks 


Gannet 


Fig. 


849. — The    "  Jastrow  "    Illu- 
sion. 


Fig. 


850. — The    "  Muller-Lyer 
Illusion. 


(Winslow,  1933)  it  has  been  shown  that  their  response  to  the  Muller- 
Lyer  illusion  was  comparable  with  that  of  the  human  being  (Fig.  850). 
It  would  seem,  therefore,  that  the  form  as  a  whole  impresses  itself  on 
the  consciousness  of  the  bird,  thus  providing  evidence  for  the  Gestalt 
theory  of  perception.  The  rapid  assessment  and  recognition  of  a 
territory  of  the  homing  bird  seems  to  be  another  example  of  the  same 
process  (Thorpe,  1944  ;  von  Haartmami,  1949  ;  Fabricius,  1951  ; 
Wilkinson,  1952  ;    and  others)  ;   so  also  is  the  curious  phenomenon  of 


704 


THE   EYE   IN   EVOLUTION 


"  imprinting  "  whereby  a  newly  hatched  fleclghng  attaches  itself  to 
the  first  thing  it  sees,  usually  its  parent,  sometimes  a  bird  of  another 
species,  occasionally  a  human  being,  ^  or  experimentally  in  incubated 
birds  to  an  inanimate  object  (Lorenz,  1935  ;  Alley  and  Boyd,  1950  ; 
Ramsay,  1950  ;  and  others). 

Among  PLACENTALS  the  accuracy  of  visual  judgments  varies.  In 
most  of  the  lower  nocturnal  types  it  is  of  low  degree  ;  thus  Greenhut 
and  Young  (1953),  in  assessing  the  accuracy  of  jumps  by  rats,  found 
that  they  appeared  to  have  little  or  no  visual  perception  of  distance  ; 
little  difference  was  found  between  the  performances  of  normal, 
hooded  or  albino  animals.  On  the  other  hand,  the  agility  of  the 
arboreal  Placentals,  the  accuracy  of  the  larger  Felidae  in  leaping  on 
their  prey,  or  the  sure-footedness  of  the  swifter  Ungulates  in  galloping 
or  jumping  over  rough  country  is  testimony  that  accurate  spatial 
judgments  are  not  a  monopoly  of  the  Primates. 


Alley  and  Boyd.     The  Ibis,  92,  46  (1950). 
Benjamins.      Dtsch.   Physiol.   Ges.,   Ham- 

"burg,  2  (1920). 
Banner.     Z.  uiss.  Zool.,  151,  382  (1938). 
Boulet.    C.  R.  Soc.  Biol.  (Paris),  147,  1623 

(1953). 
Bressou.     C.   R.   Acad.  Set.   (Paris),  241, 

615,  639  (1955). 
Canella.      C.    R.   Soc.    Biol.    (Paris),    122, 

1221  (1936). 
Chow    and    Nissen.      J.    comp.    physiol. 

Psychol.,  48,  229  (1955). 
Dubar.     These,  Paris  (1924). 
Fabricius.    Acta  zool.  Fenn.,  68,  1  (1951). 
Gassendi.     Opera,  2,  395  (1658). 
Greenhut  and  Young.     J.  genet.  Psychol., 

82,  155  (1953). 
Grinnell.     Univ.  Calif.  Chron.,  392  (1921). 
Grossmann  and  Mayerhauseii.      ?'.  Graefes 

Arch.  Ophthal.,'22  (3),  217  (1877). 
Gudger.     Zoologica,  34,  99  (1949). 
von  Haartmann.     Acta  zool.  Fenn.,  56,  1 

(1949). 
Herter.     Z.  vergl.  Physiol.,  11,  730  (1930). 
Johnson,  Lindsay.    Philos.  Trans.   B,  194, 

1  (1901). 
Kahmann.     Zool.  Jb.,  Abt.  Zool.  Physiol., 

52,  295  (1932). 
Zool.  Anz.,  102,  177  (1933). 
Kappers.      Die    Vergl.   Anat.   des  Nerven- 

systems     der      Wirbeltiere,     Haarlem 
,(1920). 
Kepler.     Dioptrice  (1611). 
Leuckart.      Graefe-Saeinisch    Hb.    d.    ges. 

Augenheilk.,  I.  2,  145  (1875). 
Lorenz.     J.   Ornith.    (Lpz.),   83,    137     289 

(1935). 
Magnus.     Korperstellung ,  Haarlem  (1924). 
Merton.    J.  Physiol.,  132,  25P  (1956). 
Morrow.    Quart.  Rev.  Biol.,  23,  27  (1948). 


Mott.     Trans,  ophthal.  Soc.   U.K.,  25,  liii 

(1905). 
Miiller,  J.     Zur  vergl.  Physiol,  d.  Gesichts- 

sinnes    d.    Menschen    u.    d.     Thiere, 

Leipzig  (1826). 
Myers.      J.    comp.   physiol.    Psychol.,    48, 

470  (1955). 
Newton.     Opticks,  London  (1704). 
Ovio.     Anat.  et  physiol.  de  Voeil  dans  la 

serie  animale,  Paris  (1927). 
Pirenne.    Nature  (Lond.),  152,  698  (1943). 
Pisa.     v.   Graefes  Arch.   Ophthal.,    140,    1 

(1939). 
Porta.     De  refractione,  142  (1593). 
Porterfield.    On  the  Eye,  Edinburgh,  2,  285 

(1759). 
Portier.     Rev.fran^.  Ornith.,  15,  99  (1923). 
Ramsay.     The  Auk,  67,  456  (1950). 
Revesz.     Brit.  J.  Psychol.,  14,  387  (1924). 

Arch,  neerl.  Physiol.,  10,  417  (1925). 
Rochon-Duvigneaud.  Ann.        Oculist. 

(Paris),    158,    561    (1921)  ;     159,    561 

(1922)  ;     160,    769    (1923)  ;     170,    177 

(1933). 
Recherches   sur   Voeil   et   la   vision   chez 

les  vertebres,  Paris  (1933). 
Les  yen. I-  et  la  vision  des  vertebres,  Paris 

(1943). 
Seigel.    J.  comp.  physiol.  Psychol.,  46,  115, 

249  (1953). 
Schneider.       Z.    vergl.    Physiol.,    39,    524 

(1957). 
Sherrington.       Brit.    J.    Psychol.,    1,    26 

(1904). 
Integrative  Action  of  the  Nervous  System, 

N.Y.  (1906). 
Sperrv  and  Clark.     Physiol.  Zool.,  22,  372 

(1949). 
Thieuhn.     These,  Paris  (1927). 


*  This  phenomenon  was  known  to  Pliny  {Nat.  Hist.,  10,  37). 


THE   PERCEPTION   OF   MOVEMENT  705 

Thorpe.     Proc.  Linn.  Soc.  Lond.,  156,  70  Warden  and  Baar.     J.  conip.  Psychol.,  9, 

(1944).  275  (1929). 

du  Tour.    .4c/a,  Paris,  334  (1743).  Weale.     Nature  (Lond.),  175,  996  (1955). 

Tschermak.     Pfliigers  Arch.  ges.  Physiol.,  Whitteridge.     The  Advancement  oj Science, 

qn    ,  /,90-^^  ^°-  ^^  (1956)- 

,,           '  \;   „    !;•  ,    ^      j>  1       ^        ,11  Wilkinson.     J.  exp.  BzoL,  29,  532  (1952). 

\erner.    Bull.  Bwl.  Fr.  Beige,  Suppl.  11,  ^inslow.    Arch.    Psychol,,   153,   1    (1933). 

137  (1928).  WoUaston.      Philos.    Trans,  ray.  Soc.   (1), 

Ann.  Sci.  nat.  ZooL,  13,  5  (1930).  222  (1824). 

Walls.       The     Vertebrate    Eye,    Michigan  Wundt.       Beit.     z.     Theorie     d.     Sinnes- 

(1942).  ucihrnehmung,  Leipzig  (1862). 

THE  PERCEPTION  OF  MOVEMENT 

From  the  biological  point  of  view  the  two  critical  functions  of 
vision  are  the  control  of  the  movements  of  the  individual  and  the 
perception  of  the  movement  of  objects  in  the  outside  world  ;  it  is  for 
this  reason  that  eyes  are  found  essentially  in  actively  moving  animals 
while  m.  those  leading  a  sedentary  existence  they  degenerate.  ^ 
The  fundamental  visual  sensations  are  therefore  the  perception  of 
light  and  of  motion  ;  the  perception  of  form  and  of  colour  are 
accessory.  In  the  human  eye  the  latter  two  are  essentially  the 
prerogative  of  the  recently  evolved  central  area  and  the  periphery 
of  the  retina  is  primarily  concerned  with  the  former;  so  in  the  wide 
panoramic  field  of  the  lower  Vertebrates  the  perception  of  movement 
is  the  most  important  aspect  of  the  animal's  visual  experience.  Even 
in  creatures  so  lowly  as  the  larvae  of  Amby stoma,  Moore  and  Welch 
(1940)  obtained  an  association  by  training  between  food  and  movement 
or  between  food  and  light,  and  experimenting  on  the  frog,  Hijla,  Pache 
(1932)  found  that  recognition  of  forms  such  as  triangles,  circles  or  crosses 
depended  essentially  on  the  occurrence  of  some  movement.  It  is  well 
known  that  Am])hibians  such  as  the  frog  or  Reptiles  such  as  turtles, 
lizards  and  snakes  appear  not  to  see  motionless  prey,  just  as  the 
rabbit  in  flight  will  collide  with  a  motionless  man.  The  eyes  of  the 
lower  Mammals  can  see  little  else  beyond  light  and  movement,  while 
Schmid  (1936),  studying  the  visual  performance  of  the  dog,  concluded 
that  the  recognition  of  a  moving  object  was  possible  at  a  much  greater 
distance  than  of  the  same  object  when  stationary  (900  compared  with 
585  metres). 

From  the  physiological  point  of  view  the  perception  of  movement 
depends  on  two  factors— the  fineness  of  the  retinal  mosaic  and  the 
persistence-time  of  vision.  When  the  visual  elements  are  few  the 
retinal  area  served  by  a  single  optic  nerve  fibre  is  la]?ge  ;  in  such  a 
"  coarse-grained  "  retina  an  image  must  travel  a  considerable  distance 
before  it  excites  the  sensory  elements  associated  with  another  optic 
nerve  fibre  so  that  a  small  movement  may  not  be  appreciated.  Simi- 
larly, if  the  physiological  effect  of  stimulation  persists  for  a  long  time, 

1  p.  721 


S.O.— VOL.  T. 


706  THE   EYE   IN  EVOLUTION 

a  retinal  element,  once  stimulated,  cannot  react  quickly  to  a  new 
stimulus  ;  an  image  moving  across  such  a  retina  will  therefore 
appear  as  a  blurred  streak  and  not  as  a  clearly  defined  pattern.  The 
persistence-time  can  be  studied  by  the  well-known  method  of  flicker, 
and  can  also  be  determined  objectively  by  studying  the  electrical 
reactions  of  the  retina  to  intermittent  stimulation.  We  have  already 
seen  that  great  differences  exist  in  this  respect  between  the  "  fast  eyes  " 
of  swiftly  moving  diurnal  insects  and  the  "  slow  eyes  "  of  more  sluggish 
nocturnal  types.  Similarly  among  Vertebrates  the  persistence-time 
is  shortest  in  rapidly  moving  animals  of  diurnal  habit.  Both  a  fine 
retinal  "  grain  "  and  a  short  persistence-time  are  therefore  associated 
with  the  mechanism  required  for  good  visual  acuity  and  the  apprecia- 
tion of  movement. 

The  limits  of  the  perception  of  movement  in  Vertebrates  have 
not  received  much  study.  Boulet  (1953-54)  found  that  if  several 
perch  (Perca  fluviatilis)  were  confronted  by  a  moving  sphere  in  con- 
trolled conditions  to  excite  the  optomotor  reaction,  half  the  fish 
responded  with  eye  movements  when  the  angular  velocity  was  12°  per 
sec,  and  all  of  them  when  it  was  between  14°  and  26°  per  sec.  ;  move- 
ments quicker  than  78°  per  sec.  excited  no  response  and  were  probably 
not  perceived  as  such.  This  compares  poorly  with  the  performance  of 
the  human  fovea  where  the  minimum  angular  displacement  perceived 
is  from  6  to  10  sees,  of  arc  and  the  upper  perceivable  limit  of  speed 
corresponds  to  an  angular  velocity  between  140°  and  350°  per  sec. 

The  perception  of  movement  is,  of  course,  only  relative.  Beebe 
(1934)  brought  this  out  well  by  his  observations  on  the  conduct  of  fish 
in  his  oceanographic  studies.  When  standing  on  the  ocean  floor,  so 
long  as  he  stood  motionless  and  erect  he  excited  the  attention  and 
curiosity  of  the  surrounding  fish,  but  if  he  rocked  and  swayed  with  the 
current  in  keeping  with  the  weeds  of  the  sea-bottom,  they  paid  no 
attention  to  him  and  appeared  not  to  see  him. 

Animals  appreciate  stroboscopic  movement  in  much  the  same  way  as  we 
do.  Thus  Gaffron  (1934)  found  that  if  fish  were  contained  in  a  tank  surrounded 
by  a  revolving  striped  drum  illuminated  intermittently,  they  reacted  as  if  the 
drum  were  stationary  or  were  turning  in  the  actual  direction  of  motion  or  in  the 
opposite  direction  depending  on  the  frequency  of  the  illuminating  light,  the 
response  of  the  fish  being  precisely  similar  to  her  own  (Gaffron's).  Similarly, 
von  Schiller  (1934),  having  trained  the  minnow,  Phoxinus,  to  resiaond  positively 
to  the  upward  movement  of  a  white  square  at  a  definite  speed  in  feeding  experi- 
ments, found  that  the  same  response  could  be  elicited  if  two  squares  were 
successively  illuminated  at  time-intervals  such  that  the  stroboscopic  movement 
thus  appreciated  eorresjaonded  to  the  real  movement  in  the  initial  experiment. 
In  this  connection  Walls  (1942)  pointed  out  that  the  interest  of  the  dog  in  motion 
pictures  and  its  complete  indifference  to  still  pictures  is  a  demonstration  that 
to  it  also  an  appreciation  of  apparent  movement  corresponding  to  that  of  man 
is  a  real  perceptual  experience. 


THE   PERCEPTION   OF  MOVEMENT  707 

Beebe.     Zoologica,  16,  149  (1934).  von  Schiller.     Z.  vergl.   Physiol,  20,  454 

Boulet.    C.  R.  Soc.  Biol.  (Paris),  147,  1623  (1934). 

(1953)  ;    148,  583  (1954).  Schmid.     Zbl.  Kleintierk.  Pelztierk.,  12,  1 

Gaffron.    Z.  vergl.  Physiol.,  20,  299  (1934).  (1936). 

Moore  and  Welch.    J.  comp.  Psychol.,  29,  Walls.       The     Vertebrate    Eye,    Michigan 

283  (1940).  (1942). 
Pache.     Z.  vergl.  Physiol.,  17,  423  (1932). 


PART  IV 
EVOLUTIONARY  BY-WAYS 

Median  Eyes 
Rudimentary  Eyes 
Luminous  Organs 
Electric  Organs 


Fig.  851. — Rene  Descakte.s  (15<J6-1650). 


CHAPTER   XIX 
MEDIAN  EYES 

We  have  already  seen  ^  that  it  is  not  unusual  for  the  region  of  the 
mid-brain  (diencephalon)  of  certain  Vertebrates — and  particularly  the 
ependymal  cells  lining  the  posterior  portion  of  the  first  embryonic  vesicle 
which  persists  as  the  third  ventricle  of  the  brain — to  show  evidences  of  an 
optical  as  well  as  a  glandular  function.  From  this  region  the  optic  vesicles 
which  form  the  lateral  eyes  emerge  as  out-pouchings  ;  from  the  floor  is 
derived  the  neural  portion  of  the  pituitary  gland  ;  in  the  ventral  area  are 
nuclei  of  internal  secretion  ^  ;    and  from  the  thin  roof  is  given  off  the  pineal 


h 


Fig.  852. — Descartes's  Orkjinal  Diagram  Illustrating  the  Effect  of  Light 
UPON  THE  Rational  Soul  Lying  in  the  Pineal  Gland  (from  a  iDhotograph 
by  Prof.  J.  F.  Fulton). 

apparatus  (or  epipliysis),  which,  although  usually  glandular  in  function, 
becomes  differentiated  into  a  median  eye  in  some  species.  This  dorsal 
up-growth  of  the  roof  of  the  diencephalon  is  represented  in  varying  degrees 
in  all  Vertebrates  with  the  exception  that  the  pineal  process  is  absent  in 
the  dugong  {Halicore),  a  decadent  and  sluggish  sea-cow,  and  in  whales 
(Cetaceans),  while  the  pineal  body  is  absent  in  the  armadillo  {Dasypus)  and 
in  the  dolj>hin  {Dclphhius). 

The  significance  of  the  pineal  body  has  always  been  an  enigma.  The  ancient 
Romans  described  it  as  the  glandula  pinealis  and  by  snch  anatomists  as  William 
Cooper  (1666-1709)  and  Jacob  Henle  (1809-1885)  it  was  considered  as  a  lymphatic 
"  gland."  In  the  more  speculative  philosophy  of  Rene  Descartes  the  body  was  a 
machine  directed  by  a  "  rational  soul  "  which  dwelt  in  the  pineal  gland.  This  con- 
ception, sarcastically  derided  by  Voltaire,  is  illustrated  in  Fig.  852,  taken  from 
Descartes's  work  De  homine  figuris  et  latinitate  donatus  a  Florentio  Schuyl  (Leyden, 
1  p.  537.  2  p_  557^ 

711 


712 


THE   EYE   IN   EVOLUTION 


1662),  which  demonstrates  figuratively  the  effect  of  hght  upon  the  soul  lying  within 
the  gland. 

It  is  impossible  to  overestimate  the  influence  of  bene  descartes  (1596-1650), 
the  great  French  philosopher,  on  the  development  of  European  thought.  In 
contradistinction  to  Francis  Bacon,  the  great  empiricist  who  based  his  philosophy  on 
observed  facts,  he  disregarded  the  role  of  experimentation  and  sought  to  build  a 
mechanical  conception  of  the  universe  on  mathematical  principles.  In  pure  mathe- 
matics, he  invented  coordinate  geometry,  making  it  algebraic,  and  developed  the 
conception  that  mass  and  time  were  dimensions  as  fimdamental  as  those  of  space. 
Finding  the  intellectual  atmosphere  of  France  unsympathetic,  he  went  to  Holland 


Par       Pin 

Fig.  853. 


Par       Pin 
Fig.   854. 


Figs.  853  to  855. — The  Development  of 
THE  Median  Eye  in  the  Embryo  of  a 
Lizard,  Lacerta. 

Medial  sections  through  the  roof  of  the 
diencephalon  showing  the  development 
of  the  pineal  and  parietal  organs.  Fig.  853 
in  an  embryo  of  3  mm.  ;  Fig.  854,  5  mm.  ; 
and  Fig.  855,  7  mm. 

E,  epidermis  ;  A'^,  neural  ectoderm  of  the 
roof  of  the  diencephalon.  The  hatched  area 
represents  mesoderm.  Pin,  the  anlage  of  the 
pineal  organ  ;  Par,  the  anlage  of  the  parietal 
organ  ;  L,  the  anlage  of  the  lens  (after 
Novikoff). 


(1628)  and  there  published  his  two  great  works,  the  Discourse  on  Method  (1637)  and  the 
Principles  of  Philosophy  (1644),  both  of  which  were  placed  on  the  list  of  prohibited 
books  in  Rome  and  Paris  (1663).  Rejecting  the  classical  view  of  his  time  derived  from 
Aristotle  that  nature  was  a  single  system  hierarchically  ordered  with  a  Deity  at  the 
apex,  he  reasoned  that  the  material  vmiverse  was  a  homogeneous  mechanical  system 
composed  of  qualitatively  similar  activities  following  quantitative  mechanical  laws 
susceptible  to  mathematical  analysis.  Alongside  this  machine-world  which  included 
the  human  body,  animals,  plants  and  inorganic  natvire,  there  was  a  spiritual  world 
in  which  the  body  of  man  alone  of  all  material  things  participated  by  virtue  of  his 
soul.  Ever  since  his  time  this  dualism  of  the  Cartesian  philosophy  has  permeated 
European  thought  ;  and  although  to  us  today  the  designation  of  the  pineal  body  as 
the  meeting  place  of  the  two  worlds  may  seem  speculative  and  fanciful,  it  must  be 
admitted  that  regarding  the  function  of  this  organ  our  ideas  are  still  as  nebulous. 

In  its  most  elaborate  form  the  pineal  apparatus  consists  of  two  parts 
which  arise  from  the  middle  of  the  epiphyseal  arch,  the  most  posterior  of 


MEDIAN   EYES  713 

the  three  arches  of  the  roof  of  the  diencephalon — a  pineal  organ  or 
EPIPHYSIS  ^  lying  more  posteriorly  and  a  parietal  or  parapineal  organ 
lying  more  anteriorly,  sometimes  arising  in  association  with  the  pineal  body, 
but  sometimes  independently  of  it.  The  former  is  connected  with  the 
posterior  commissure  ;  the  latter  with  the  superior  (habenular)  commissure  ; 
their  development  in  the  embryo  of  the  lizard  {Lacerta)  is  seen  in  Figs. 
853-5).  The  pineal  body  is  connected  nervously  with  the  right  habenular 
ganglion,  the  parietal  with  the  left,  suggesting  that  originally  they  may  have 
been  right  and  left  members  of  a  pair. 

The  highest  development  of  a  median  eye  is  seen  in  the  most  primitive 
Vertebrates,  the  cyclostomes  (Fig.  856).  The  lamprey  {Petromyzon)  is 
provided  with  both  a  pineal  and  a  parietal  organ  having  the  structure  of  an 
eye  with  a  considerable  degree  of  retinal  differentiation  (Fig.  864)  ;  but  in 
Myxinoids  no  trace  of  either  is  seen.  The  presence  of  an  impression  in  the 
mid-line  of  the  roof  of  the  cranial  cavity  in  fossil  remains  of  the  closely- 
related  Agnatha  {Pteraspis,  Cephalasjns) — the  oldest  known  Vertebrates — 
is  an  indication  of  the  occurrence  of  a  pineal  organ  in  these  very  primitive 
types,  and  since  the  impression  is  often  duplicated  the  presumption  is  that 
the  median  eye  at  this  stage  in  evolution  was  paired  (Gaskell,  1908  ;  Wood- 
ward, 1922  ;   Heintz,  1932  ;   Hills,  1933). 

Among  FISHES  certain  old-fashioned  ganoid  types  retain  a  relatively 
well-developed  median  eye  somewhat  resembling  the  parietal  eye  of 
Cyclostomes.  In  the  sturgeon,  Acipenser,  in  addition  to  supporting  cells  of 
ependymal  character,  the  vesicle  contains  many  cells  of  a  sensory  type  with 
ganglion  cells  and  efferent  nerve  fibres  ;  the  structure  thus  resembles  the 
parietal  sense-organ  rather  than  a  secretory  gland.  A  somewhat  similar 
organ  is  seen  in  the  primitive  fish,  Polypterus,  found  in  African  rivers,  and 
the  Holostean,  Amia  (Hill,  1894  ;  and  others).  In  Selachians  (skate, 
shark,  dogfish,  etc.)  the  pineal  body  is  set  on  a  long  stalk  and  often  per- 
forates the  skull  through  a  pineal  foramen  to  appear  beneath  the  skin  as 
a  closed  vesicle  (Fig.  857)  ;  alternatively  it  may  lie  \\ithin  the  skull  in 
a  recess  in  its  cartilaginous  roof  (Holocephali).  In  these  fishes  the  eye- 
structure  has  disappeared,  the  vesicle  is  small  and  consists  of  ependymal 
cells,  and  the  tendency  is  probably  towards  glandular  formation  (Cattie, 
1882  ;  Locy,  1894).  In  Teleosteans  (trout,  salmon,  pike,  herring,  etc.) 
the  pineal  apparatus  is  not  so  well  developed,  and  is  somewhat  variable  ; 
in  contrast  to  "ganoid"  and  cartilaginous  fishes,  the  vesicle  tends  to  be  large 
and  the  stalk  short.  In  these  bony  fishes  it  rarely  reaches  the  under- 
surface  of  the  skull,  and  although  it  contains  cells  of  neural  and  glial 
character  among  the  ej^endymal  cells,  it  never  shows  a  developed  ocular 
structure.    It  is  interesting,  however,  that  in  this  class  of  fishes  the  superficial 

^  Galen  (c.  a.d.  130-200)  used  the  non-committal,  topographical  Greek  term — eTri,  upon, 
(f>vai^,  growth  ;  the  Latin  term  is  descri^Jtive  of  the  shape — pinus,  a  fir-cone.  The  term 
"  epiphysis  "  is  usually  applied  to  the  deeply  situated  glandular  organ  seen  in  Mammals  in 
contrast  to  the  sensory  "  pineal  eye  "  of  the  lamprey  or  Sphenodon. 


714 


THE   EYE   IN  EVOLUTION 


structures,  including  the  skull,  are  sometimes  transparent  while  occasionally 
the  degree  of  opacity  of  the  integument  is  regulated  by  chromatophores 
(Breder  and  Rasquin,  1950).  In  some  cases  (the  trout,  Salmo  trutta)  a 
smaller  off-shoot  from  the  roof  of  the  diencephalon  may  perhaps  represent  a 
vestigial  parietal  organ.  In  the  lung-fishes  (Dipnoi)  the  pineal  apparatus  is 
degenerate  and  makes  no  attempt  to  reach  the  surface  or  assume  a  sensory 
structure. 


Figs.  856  to  859. — The  Pineal  and  Parietal  Organs  in  Vertebrates. 

/PI 


Fig.  856. — In  Cyclostomcs  (the  lamprey' 


Fig.  857. — In  Selachians. 
Pa 


Fig.   858. — In  Amphibians. 


Ls  R  -Cp 

Fig.  859. — In  Rejitiles  {Sj)henodon). 


A,  accessory  parietal  body  ;  Cli,  habenular  commissure  ;  Cp,  posterior  commis- 
sure ;  H,  habenular  ganglion  ;  Ls,  lamina  terminalis  ;  n,  pineal  nerve  ;  np,  jiarietal 
nerve  ;  Pa,  i^ai'ietal  organ  ;  Pf,  parapliysis  ;  PI,  pineal  organ  ;  Ps,  i^ineal  stalk  ; 
Pt,  jDineal  tract  ;    R,  pineal  recess  (after  Tilney). 


Among  AMPHIBIANS,  the  primitive  tailed  class,  Urodela  (salamanders, 
newts,  Ambystoma,  Proteus,  etc.),  possesses  a  very  rudimentary  pineal 
organ,  but  the  occasional  possession  of  pigment  granules  (the  olm,  Proteus) 
and  even  of  some  nerve  fibres  suggests  some  affinity  with  a  photosensitive 
structure.  In  the  degenerate  blind  and  limbless  Csecilians  (Apoda)  the 
pineal  organ  is  similarly  degenerate.  In  the  tailless  Amphibians  (Anura), 
however,  it  is  more  fully  represented  in  the  early  stages  of  development. 
Thus  in  the  young  frog  (Rana)  the  pineal  body  comes  to  the  surface  above 
the  skull  as  an  eye-structure,  its  position  being  indicated  by  a  pale  area 
where  the  cutaneous  pigment  and  glands  are   scanty  or  absent,   but  it 


MEDIAN  EYES 


715 


Fig.  860. — The  Parietal  akd  Pineal  Bodies  of  SpHESoDoy  pvsctatvs. 

A  lateral  view  of  the  brain.  C,  cerebellum  ;  O,  optic  lobe  ;  OL,  olfactory  lobe  ; 
ON ,  optic  nerves  ;  Par,  parietal  eye ;  Pin,  pineal  body  (epiphysis) ;  IV,  fourth  ven- 
tricle.   The  structures  issuing  below  are  the  cranial  nerves,  III  to  XII. 

degenerates  and  disappears  in  adolescence  leaving  a  rudiment  of  an  eye 
connected  by  a  nerve  with  the  posterior  commissure  (Fig.  858)  (Leydig, 
1891  :   Braem.  1898  ;   and  others). 

In  the  primitive  reptiles  the  eye-structure  reaches  its  highest  develop- 
ment in  the  parietal  organ  (Figs.  859-860)  ;  in  the  New  Zealand  tuatara 
[Sphenodon).  for  example,  it  passes  through  the  skull  by  a  "  parietal  foramen" 
and  lies  beneath  the  skin,  the  scales  of  which  become  specialized  and 
transparent  in  this  region.  In  this  animal  as  well  as  in  some  other  types,  an 
ACCESSORY  PARIETAL  ORGAX  lies  coutiguoush'  ;  it  is  variable  in  structure, 
vesicular  or  sohd.  and  tends  to  disappear  with  maturity.  In  lizards  such  as 
Lacerta,  the  arboreal  lizard.  Iguana,  and  the  slow-worm,  Ancjuis  (a  limbless 
lizard),  the  parietal  eye  loses  connection  entirely  with  the  pineal  body  and 


Fig.    861.- 


-The    Pineal    Gland    in    Man    (from    Gladstone    and    ^Vakeley,    Tht 
Pineal  Organ). 


716  THE   EYE   IN   EVOLUTION 

has  an  independent  parietal  nerve  associated  with  a  near  by  parietal  centre, 
a  connection  which  in  many  cases  is  transitory  and  degenerates  before 
maturity  so  that  the  organ  would  appear  to  lose  its  function.  In  these 
species  the  pineal  body  is  always  rudimentary  and  the  vesicle  is  usually 
absent.  It  is  also  interesting  that  the  presence  of  a  parietal  opening  in  the 
roof  of  the  skull  of  fossil  labyrinthodont  amphibians  and  extinct  reptiles  of 
the  Palaeozoic  and  Mesozoic  eras  suggests  that  a  functional  eye  existed 
in  these  species  also.  In  the  more  recent  reptiles,  such  as  geckos,  snakes, 
tortoises,  turtles,  crocodiles,  and  alligators,  the  eye-structure  disappears  and 
the  epiphyseal  arch  gives  rise  to  a  glandular  organ,  an  arrangement  retained 
in  the  higher  animals.  In  some  birds  and  mammals  analogous  rudiments 
appear  in  embryonic  life  which  disappear  with 
development,^  but  in  these  types  the  pineal  organ 
has  a  glandular  structure  and  lies  snugly  hidden  on 
the  roof  of  the  diencephalon  between  the  cerebrum 
and  the  cerebellum  (Fig.  861).  It  is  thus  evident 
that  the  pineal  organ  constitutes  a  definitive  eye  only 
in  the  lamprey  and  to  a  less  extent  in  certain  primi- 
tive "ganoid  "  fishes,  while  the  parietal  organ  forms  an 
eye-like  structure  in  the  lamprey  and  also  in  primitive 
Fig.     862. — The     Lam-     reptiles  ;   Otherwise  the  latter  organ  is  vestigial. 

PREY,   PetROMYZOS. 

Dorsal  View  of  the  head  ^j^^    median    eye     of    the    lamprey    lies    under    a 

end  oi  the  animal  show-       ,        ,•      ,  r-  ,  ,      ^  ■  ,-,  ■  ^^■  c  ,^ 

ine  the  eve    E    the  nasal      localized   area   oi   transparent  skin  on  the  inidline  ot  the 

aperture,     N ,     and     the      dorsal  surface  of  the  head  immediately  behind  the  single 
pineal  area,  Pin.  median  nostril  (Fig.  862).   It  consists  of  two  diverticula  lying 

vertically  one  upon  the  other  (Ahlborn,  1883  ;  Beard,  1889  ; 
Stiidnicka,  1905  ;  Dendy,  1907  ;  Mygind,  1949).  The  more  superficial  and  dorsal 
vesicle  is  the  jDineal,  the  lower  the  parietal  eye  (Fig.  856).  Together  they  form  an  organ 
incapable  of  optical  iinagery  but  doubtless  able  to  appreciate  differences  in  light  in- 
tensity. Of  the  two  the  pineal  eye  is  the  more  elaborately  developed  (Figs.  863  and  864). 
It  forins  a  vesicle  lying  directly  underneath  the  skin  ;  the  cells  of  the  superficial  wall 
are  elongated  to  form  a  flat  and  imperfect  lens  ;  those  of  the  deeper  wall  form  a 
pigmented  retina  comprised  of  sensory  and  supporting  cells,  ganglion  cells  and  nerve 
fibres  which  pass  as  the  pineal  nerve  in  the  posterior  coiTimissure  to  the  right  habenular 
ganglion.  The  retinal  pigment  is  of  two  types — a  dark  melanin-like  pigment  and 
whitish -yellow  granules  corresponding  closely  to  the  guanine -like  pigment  of  the  skin  ; 
the  first  has  an  absorbent,  the  second  probably  a  reflective  function  analogous  to  the 
similar  pigment  in  the  compound  eyes  of  some  Arthropods.  The  free  ends  of  the 
sensory  ceils  face  the  lumen  of  the  vesicle  which  is  fllled  with  a  nucleated  syncytial 
"  vitreous."  The  parietal  organ  forms  a  somewhat  sunilar  vesicle  of  simpler  construc- 
tion, varying  considerably  in  size  ;  the  rudimentary  parietal  nerve  leads  through  the 
habenular  commissure  to  the  left  habenular  ganglion. 

THE  MEDIAN  EYE  OF  LiZABDS  and  Sphenodou  2  is  derived  from  the  parietal  body 
and  forms  a  remarkably  eye-like  organ  (Spencer,  1886  ;  Leydig,  1887  ;  Strahl  and 
Martin,   1888  ;    Klinckowstrom,    1893  ;    Vu-chow,   1901  ;    Studnicka,   1905  ;    Dendy, 

^  Pigeon  (Livini,  1905),  guinea-pig  (Chiarugi,  1919),  ox  (Favaro,  1904). 
2  p   379, 


MEDIAN   EYES 

Pin  At         HC  Mes 


717 


Fig.  863. — The  Median  Eye  in  the  Ammoccete  of  the  Lamprey,  Petromyzon. 
Longitudinal  section  through  the  roof  of  the  fore-  and  mid-brain.  AC,  anterior 
commissure  ;  At,  atrium  of  the  pineal  organ  ;  HC,  habenular  commissure  ;  HG, 
habenular  ganglion  ;  HT,  habenular  tract  ;  Mes,  mesencephalon  ;  Par,  parietal 
organ  ;  Pin,  pineal  organ  ;  PC,  posterior  commissure  ;  Pp,  paraphysis  (after 
Studnicka). 


Fig.   86-4. — The  Median  Eye  of  Lampetra   flvviatili^. 

Section  through  the  head  of  the  animal  showing  the  two  vesicular-like  structures 
in  the  centre  of  the  figure,  the  pineal  and  i?arietal  bodies,  lying  in  the  ventricle 
underneath  a  relatively  transparent  area  of  skin  and  subcutaneous  tissue.  The  two 
solid  masses  in  the  lower  portion  of  the  picture  represent  parts  of  the  brain  (Mallory's 
phospho-tungstic  acid  htematoxylin)  (  X  24)  (Katharine  Tansley). 

1907-11  ;  Nowikoff,  1910  ;  Gasson,  1947  ;  Trost,  1953).  It  is  situated  in  the 
parietal  foramen  of  the  cranial  roof  immediately  under  the  integument  and  is  covered 
by  a  specially  modified  scale  where  the  black  pigment  is  absent  and  the  green  is  only 
feebly  represented  so  that  it  is  relatively  transparent  (Fig.  459).  The  eye  takes  the 
form  of  a  flattened  vesicle  lying  in  a  connective  tissue  cajasule  ;  the  cells  of  the  distal 
wall  are  elongated  to  form  a  lens  which  sometimes  contains  a  central  jDigmented  area  ; 
the  cells  of  the  proximal  wall  are  differentiated  to  form  a  retina  (Fig.  865).  In  some 
types  such  as  the  American  "  chameleon  ",  Anolis,  the  latter  is  relatively  crude  but 
usually  there  is  a  reasonably  well-differentiated  sensory  layer  composed  of  visual  and 


718 


THE   EYE   IN  EVOLUTION 


intercalary  cells,  the  latter  being  laigmented  except  in  Sphenodon  in  which  the  pigment 
is  extracellular.  In  the  lizards  this  pigment  shows  adaptive  changes,  moving  towards 
the  sensory  terminations  of  the  cells  on  exposure  to  light  (Nowikoff,  1910).  Peripheral 
to  the  visual  cells  lies  a  layer  of  bipolar  ganglion  cells,  the  nerve  fibres  issuing  from 
which  form  the  j^arietal  nerve  which  runs  down  the  parietal  stalk  either  to  the  right 
(Anguis,  Lacerta)  or  left  {Sphenodon)  habenular  ganglion.  The  surfaces  of  the  visual 
cells  of  the  retina  as  well  as  those  of  the  lenticular  cells  facing  the  cavity  of  the  vesicle 
are  richly  provided  with  cilia  ;  the  cavity  itself  is  filled  with  a  delicate  syncytium 
with  a  few  oval  nuclei  enclosing  spaces  filled  with  fluid  constitviting  a  "  vitreous." 

It  is  to  be  noted  that  in  all  cases  the  svirface  ectoderm  takes  no  part  in  the 
formation  of  the  ocular  vesicle,  there  is  no  secondary  invagination,  and  the  retinal 
cells  are  verted,  resembling  the  eyes  of  Invertebrates  rather  than  the  paired  lateral 
eyes  of  Vertebrates. 


Fig.  865. — The  Parietal  Eye  of  the  Slow-worm,  Axains  fragilik. 
CC,   connective    tissue  ;     GC,   ganglion    cells  ;     L,   lens ;     PC,   pigment   cells 
PN,  parietal  nerve  ;    V,  vitreous  ;    VC,  visual  cells  (after  Nowikoff). 


The  function  of  the  pineal  organ  in  those  species  in  which  it  assumes  an 
ocular  formation  is  undoubtedly  optic  although  it  would  appear  that  it  is 
confined  to  the  directional  appreciation  of  light  and  is  incapable  of  optical 
imagery  (Mygind,  1949).  In  those  species  wherein  a  glandular  structure  is 
evident,  even  among  Mammals,  the  function  of  the  pineal  body  is  still 
obscure  despite  the  considerable  amount  of  research  which  has  been  devoted 
to  the  subject  by  morphologists,  histologists,  pathologists  and  clinicians. 
In  man  it  reaches  maturity  between  the  ages  of  G  and  7  years  whereafter 
involutive  phenomena  begin  to  appear  in  the  form  of  hyalinization,  calcifica- 
tion and  cystic  formation  (Rio-Hortega,  1922-29  ;  (dobus  and  Silber,  1931  ; 
and  others).  This  involution  after  puberty  together  with  the  variations  in 
the  size  of  the  organ  observed  during  pregnancy,  with  sexual  activity  or  after 
castration  both  in  human  subjects  ^  and  in  animals, ^  have  confirmed  the 
clinical  impression  that  its  main  association  concerned  skeletal  growth  and 
the  sexual  functions.    It  is  to  be  remembered,  however,  that  Pelizzi's  (1910) 

1  Brandenburg  (1929),  Frada  and  Micale  (1941). 
^  Santamarina  and  Venzko  (1953). 


MEDIAN   EYES  719 

classical  syndrome  of  macrogenitosoma  preecox  has  been  reported  as  occur- 
ring in  about  50%  of  cases  in  patients  without  pineal  disturbances,  while  the 
majority  of  cases  of  pineal  tumours  do  not  exhibit  sexual  syndromes 
(Haldeman,  1927).  It  may  even  be  that  when  these  symptoms  occur  they 
may  be  caused  by  pressure  on  neighbouring  structures  such  as  the  pituitary 
body  and  hypothalamus.  The  whole  question  of  the  existence  of  an 
endocrine  secretion  and  what  it  may  do  is  thus  unsolved. 

It  is  interesting  that  the  association  of  the  integumentary  pigment  with  the 
visual  system  is  maintained  in  some  amphibians  ;  thvis  pigmentary  changes  always 
occvir  in  10-day-okl  tadpoles  if  they  are  fed  on  pineal  tissue  (MeCord  and  Allen,  1917), 
while  the  injection  of  pineal  extract  induces  contraction  of  the  melanophores  of  the 
African  toad,  Xenopus  (Bors  and  Ralston,  1951). 

The  function  of  the  parietal  organ  remained  enigmatic  until  its  eye -like 
structure  in  lizards  was  described  by  Leydig  (1872)  and  confirmed  in  Ayiguis 
fragilis  by  De  Graaf  (1886)  and  in  Sphenodon  by  Baldwin  Spencer  (1886). 
From  these  observations  arose  the  view  that  the  pineal  apparatus  is  a 
primitive,  unpaired,  median,  upward-looking  eye,  which  has  degenerated 
except  in  a  few  instances.  It  is  more  probable,  however,  that  the  hypothesis 
of  Todaro  (1888)  is  the  more  correct,  that  although  often  apparently  un- 
paired, the  organ  is  the  result  of  the  fusion  of  a  pair  (see  Sterzi,  1912  ; 
Gladstone  and  Wakeley,  1940).  The  evidence  derived  from  fossil  remains  of 
extinct  Vertebrates,  the  duplication  of  the  organ  in  primitive  tyj^es,  its 
occasional  bifurcation  in  the  higher  species,  and  the  frequent  bilaterality  of 
its  nervous  connections,  is  convincing.  There  is  a  strong  case  to  be  made 
that  its  primary  function  was  sensory.  In  extinct  fossil  species  it  seems 
clear  that  a  median  eye  coexisted  with  lateral  eyes,  olfactory  organs  and 
static  organs,  and  the  closure  of  the  foramen  in  the  roof  of  the  cranium  even 
in  these  early  t^^es  indicates  a  regression  of  the  organ  and  the  loss  of  its 
visual  function  even  in  remote  geological  times,  a  tendency  possibly  due  to 
the  gradual  predominance  of  the  lateral  eyes.  Whether,  as  Patten  (1890- 
1912)  suggested,  the  pineal  organ  is  linearly  derived  from  the  median  eye  of 
arthropods,  particularly  primitive  arachnids,  is  a  more  debatable  question. 

On  the  other  hand,  the  view  has  been  put  forward  that  its  optical 
function  is  not  essentially  primitive  but  is  rather  the  result  of  a  secondary 
transformation,  in  which  case  the  pineal  body  of  Mannnals  cannot  be  looked 
upon  as  a  vestigial  and  metamorphosed  remnant  of  an  eye.  According  to 
Tilney  and  Warren  (1919)  the  histology  of  this  region  provides  evidence  that 
in  all  Vertebrates  this  portion  of  the  brain  possesses  a  pluripotential  activity. 
Usually  the  fundamental  tendency  is  in  the  direction  of  glandular  formation, 
the  secretion  being  contributed  in  a  few  cases  to  the  cerebro -spinal  fluid, 
but  in  most  cases  and  in  the  Mammalia,  to  the  blood  stream  as  a  hormone. 
In  some  species  (Cyclostomes,  Amphibians,  and  primitive  Reptiles)  the  arch 
has  become  specialized  with  a  visual  function,  an  adaptive   modification 


720 


THE   EYE   IN  EVOLUTION 


answering  the  needs  of  the  animal  which  in  most  cases  is  of  sluggish  habit 
with  slow  movements  and  a  limited  range  of  vision.  In  this  view  the  two 
tendencies  appear  to  rim  parallel  rather  than  to  be  linearly  derived.  Which 
theory  is  correct  must  still  remain  a  matter  for  discussion. 

For  the  phylogeny  of  the  pineal  body,  see  the  elaborate  inonograph  of  Gladstone 
and  Wakeley  (1940)  ;  its  morphology  and  histology  are  well  discussed  in  those  of 
Studnicka  (1905),  Tilney  and  Warren  (1919)  and  Rio-Hortega  (1932)  ;  its  physiological 
functions  (as  a  gland  of  internal  secretion)  are  fully  noted  by  Kidd  (1913),  Schafer 
(1926)  and  Bors  and  Ralston  (1951)  ;  the  vast  clinical  literature  is  found  in  Bailey 
and  Jelliffe  (1911),  Boehm  (1920),  Laignel-Lavastine  (1921),  Horrax  and  Bailey  (1925) 
and  Calvet  (1934)  ;    the  veterinary  literature  in  Santamarina  and  Venzke  (1953). 


Ahlborn.     Z.  wiss.  ZooL,  39,  191  (1883). 
Bailey  and  Jelliffe.     Arch,    intern.   Med.,   8, 

851  (1911). 
Beard.    Quart.  J.  micr.  Sci.,  29,  55  (1889). 
Boehm.  Frankfurt.  Z.  Path.,  22,  121  (1920). 
Bors  and  Ralston.    Proc.  Soc.  e.vp.  Biol.  Med., 

77,  807  (1951). 
Braem.     Z.  iviss.  ZooL,  63,  433  (1898). 
Brandenburg.     Endokrinologie,  4,  81  (1929). 
Breder  and  Rasquin.    Science,  111,  10  (1950). 
Calvet.     UEpiphyse,  Paris  (1934). 
Cattie.    Arch.  Biol.,  Gand,  3,  101  (1882). 
Chiarugi.     Moyiit.  ZooL  ital.,  30,  34  (1919). 
Dendy.    Quart.  J.  viicr.  Sci.,  51,  1  (1907). 

Philos.  Trans.  B,  201,  227  (1911). 
Favaro.     Monit.  ZooL  ital.,  15,  111  (1904). 
Frada  and  Micale.    Radiol.  Med.  (Torino),  28, 

209  (1941). 
Gaskell.    Origin  of  Vertebrates,  London  (1908). 
Gasson.     Optician,  37,  261  (1947). 
Gladstone  and  Wakeley.     The  Pinecd  Organ, 

London  (1940). 
Globus  and  Silber.     Arch.  Neurol.  Psychiat., 

25    937  (1931). 
De  Gra'af.     ZooL  Anz.,  9,  191  (1886). 
Haldeman.     Arch.  Neurol.  Psychiat.,  18,  724 

(1927). 
Heintz.    Archaic  Fishes,  N.Y.  (1932). 
Hill.    J.  MorphoL,  9,  237  (1894). 
Hills.     Ann.  Mag.  nat.  Hist.,  11,  634  (1933). 
Horrax  and  Bailey.     Arch.  Neurol.  Psychiat., 

13,  423  (1925). 
Kidd.    Rev.  Neurol.  Psychiat.,  11,  1,  55  (1913). 
Klinckowstrom.    Anat.  Anz.,  8,  289  (1893). 
Laignel-Lavastine.     L'Encephale  (J.  Mensuel 

Neurol,  psychiat.),  16,  225,  289,  361,  437 

(1921). 
Leydig.    Die  Arten  der  Saurier,  p.  72  (1872). 


Leydig.      ZooL  Anz.,  10,  534  (1887). 

Abhandl.  der Senckb.-Oes.  Frankfurt,  16,  441 

(1891). 
Livini.     Monit.  ZooL  ital.,  16,  123  (1905). 
Loey.    Anat.  Anz.,  9,  169  (1894). 

J.  MorphoL,  9,  115  (1894). 
McCord   and  Allen.     J.   e.x;p.    ZooL,   23,    207 

(1917). 
Mygind.       Acta    psychiat.    neuroL,    24,     607 

(1949). 
Nowikoff.     Z.  wiss.  ZooL,  96,  118  (1910). 
Patten.    Quart.  J.  micr.  Sci.,  31,  317  (1890). 
The  Evolution  of  Vertebrates  and  their  Kin, 

London  (1912). 
Pelizzi.     Riv.  ital.  NeuropaL,  3,  193  (1910). 
Rio-Hortega.     Arch.  Neuro-biol.  (Madrid),  3, 

359  (1922)  ;    9,  139  (1929). 
Penfield's  Path,  of  the  N ervous  System,  N.Y., 

1,  637  (1932). 
Santamarina  and  Venzke.    Amer.  J.  vet.  Res., 

14,  555  (1953). 
Schafer.     The  Endocrine  Organs,  2  (1926). 
Spencer.    Quart.  J.  micr.  Sci.,  27,  165  (1886). 
Sterzi .    //  sisiema  nervoso  centrale  del  vertebrati, 

Padova  (1912). 
Strahl    and    Martin.      Arch.    Anat.    Physiol., 

Anat.  Abt.,  146,  164  (1888). 
Studnicka.      Lehrb.   d.   vergl.   mikr.   Anat.,   5 

(1905). 
Tilney  and  Warren.  MorphoL  and  Evolutional 

Significance   of  the   Pineal   Body,   Amer. 

anat.  Mem.  (1919). 
Todaro.    XII  Cong.  Med.  Ital.,  1,  274  (1888). 
Trost.     Z.  Zellforsch.,  38,  185  (1953). 
Virchow.        Arch.    Anat.     Physiol.    (Physiol. 

Abt.),  355  (1901). 
Woodward.     Proc.  Linn.  Soc.  Lond.,  134,  27 

(1922). 


CHAPTER   XX 
RUDIMENTARY  EYES 

The  adoption  of  peculiar  habits  by  a  species  of  animal  frequently 
stimulates  the  development  of  structural  alterations  suited  to  the  unusual 
environment  ;  in  a  previous  chapter  we  have  discussed  the  many  striking 
modifications  adopted  by  the  vertebrate  eye  to  meet  different  conditions — 
aquatic  or  aerial  vision,  for  example.  Changes  in  the  opposite  sense  may  also 
occur  when  vision  is  no  longer  required,  in  which  case  the  eyes  may  become 
rudimentary  or  vestigial  or  even  disappear.  The  adoption  of  a  sessile  or 
sedentary  habit  involving  sluggishness  or  quiescence  so  complete  that  light 
stimuli  are  valueless  may  lead  to  the  development  of  a  state  of  quasi  or 
complete  eyelessness  in  this  way,  but  the  more  usual  stimulus  is  a  lightless 
habitat  as  in  abyssal  depths  of  the  sea,  dark  caves,  muddy  rivers,  burrows 
under  the  ground,  or  within  the  body  of  another  animal. 

A  sharp  distinction  should  be  noted  here  between  the  permanent  adoption  of  an 
environment  wherein  Hght  is  absent  and  the  periodic  adoption  of  nocturnal  habits  by 
many  species  for  purposes  of  concealment  or  hvmting — the  daily  use  of  caves  by  bats, 
for  example,  as  opposed  to  permanent  residence  in  a  cave  by  cavernicolous  fishes,  or 
the  use  of  a  burrow  as  a  home  by  the  tuatara  as  opposed  to  the  subterranean  life 
of  the  mole.  As  a  rule  these  nocturnal  animals  show  the  opposite  tendency  ;  their 
eyes  are  elaborately  developed  to  take  every  advantage  of  the  dim  illumination 
available,  being  often  provided  with  a  large  lens,  a  wide  pupil  and  a  rod-retina. 

This  tendency  for  the  structural  recession  and  loss  of  function  of  an  organ  which 
is  no  longer  biologically  useful  is  not,  of  course,  confined  to  the  eye:  the  fate  of  the 
human  appendix  and  coccyx  are  well-known  examples  of  the  regression  of  an  organ, 
while  the  loss  of  its  alimentary  canal  by  the  tapeworm  or  the  possible  reduction  of  a 
micro-organism  to  the  bare  bones  of  its  nucleo-protein  on  the  adoption  of  the  habit 
of  intracellular  parasitism  as  a  virus  may  be  cited  as  examples  of  the  complete 
disajjj^earance  of  unnecessary  characters.  The  biological  mechanism  of  the  trans- 
mission of  such  a  disappearance,  however,  is  not  clear  ;  it  is  as  if  development  has 
become  arrested  from  lack  of  use.  It  is  generally  accepted  that  biologically  useful 
characteristics  tend  to  be  I'etained  in  so  far  as  they  have  survival  value,  but  that 
those  which  are  no  longer  useful  should  be  purposely  discarded  as  excess 
baggage  is  an  expression  of  Lamarckian  regression  more  positive  than  many  would 
accept.  Regression,  however,  does  not  necessarily  imply  degeneration  as  the  term  is 
generally  understood.  Darwin  (1859)  in  his  Origin  of  Species  pointed  out  that  both 
the  vise  or  disuse  of  an  organ  might  equally  lead  to  inherited  changes  both  in  plants 
and  animals,  and  that  parasites  and  "  degenerate  "  creatures  are  as  inuch  a  product 
of  evolution  as  higher  organisms  ;  they  are  as  perfectly  adapted  to  their  restricted 
environment.^ 

1  The  opposing  argument  used  by  August  Weismann  in  his  Essay  on  Inheritance  and  Related 
Biological  Questions  (1892)  that  successive  generations  of  rats  the  tails  of  which  had  been  cut  off 
persisted  in  breeding  rats  with  normal  tails  is  inapposite  since  an  artificial  mutilation  bears  no 
biological  relation  to  a  purposive  evolutionary  regression.  See  Ray  Lankester,  Degeneration, 
a  Chapter  in  Darwinism  (1895)  ;  Demoor  and  others,  Evolution  by  Atrophy  in  Biology  and 
Sociology  (1894)  ;  Vandervelde,  Parasitism,  Organic  and  Social  (1895). 
S.O.— VOL.  I.  721  46 


722  THE   EYE   IN   EVOLUTION 

An  alternative  explanation  is  to  suppose  that  there  is  an  innate  tendency  for  the 
eye  to  disappear  which  is  normally  opposed  by  natural  selection  becavise  of  its  biological 
utility.  It  is  doubtless  true  that  a  loss-mutation  may  become  effective  and  the  organ 
may  disappear  if  its  utility  has  ceased.  It  is  to  be  remembered,  however,  that  individuals 
may  show  a  cajaacity  for  the  eye  to  retrogress  or  develop  according  to  its  usefulness. 
Thus  on  the  one  hand,  the  eyes  of  larval  cave-salamanders  {Proteus,  Typhlotriton) 
usually  regress  at  metamorphosis,  but  will  develop  if  the  larvto  are  grown  artificially 
in  the  light  (Kammerer,  1912)  ;  these  sightless  Amphibians  thus  appear  to  become 
blind  in  each  successive  generation.  On  the  other  hand,  Ogneff  (1911)  found  that  if 
goldfish  were  kept  in  the  dark  for  3  years  their  eyes  became  degenerate  and  functionless 
while  the  eyes  of  many  sj^ecies  of  ojaen-water  fish  become  redviced  if  their  biological 
value  is  lessened  by  increasing  their  food  and  eliminating  predators  from  their 
environment. 

We  have  already  seen  that  ocular  regression  of  this  type  may  occur  in 
most  Invertebrates,  particularly  worms,  Molluscs  and  Arthropods  ;  the 
phenomenon  is  also  encountered  in  all  classes  of  Vertebrates  with  the 
exception  of  Birds.  It  is  interesting  that  in  most  cases  there  is  a  correspond- 
ing increase  in  the  development  of  other  senses,  such  as  the  chemical, 
olfactory  or  tactile  sense,  which  are  of  greater  use  than  vision  in  dark 
surroundings. 

THE    SEDENTARY    HABIT 

A  SEDENTARY  HABIT  may  lead  to  the  eyelessness  in  sessile  forms.  Thus 
among  actively  swimming  Lamellibranchs  such  as  the  common  scallop, 
Pecten,  eyes  of  an  extremely  elaborate  type  are  found,  but  in  sluggish  and 
quiescent  forms  they  may  be  primitive,  as  in  the  bivalve,  Litna,  or  absent  as 
in  the  mussel,  Aiiodonta.  Among  Crustaceans,  those  species  of  the  Amphi- 
pod,  Gammarus,  which  live  in  pools,  or  the  Isopod,  Asellus,  which  lives  in 
holes  is  completely  blind.  In  other  species  eyes  may  be  present  in  the 
actively  swimming  nauplius  stage,  but  when  the  adult  becomes  sessile  these 
may  become  vestigial  (the  acorn-shell,  Balanus,  which  encrusts  rocks  ;  the 
ship-barnacle,  Lepas).  We  have  already  seen  ^  that  in  insects  the  degree  of 
ocular  development  is  generally  correlated  with  that  of  the  wings  (Kalmus, 
1945). 

THE    ABYSSAL   HABIT 

An  ABYSSAL  HABITAT  renders  eyes  useless  ;  for  in  the  deep  seas  there  is 
perpetual  night.  The  transparency  of  the  different  seas  varies  greatly,  a 
factor  which  depends  largely  on  the  concentration  of  plankton  organisms, 
but  at  370  metres  in  the  Mediterranean  and  at  1.500  metres  in  mid-Atlantic 
there  is  not  sufficient  light  to  affect  a  photographic  plate  unless  it  is  exposed  for 
2  hours ;  while  the  pelagic  zone  (down  to  200  metres)  is  illuminated,  the  bathy- 
pelagic  zone  (200  to  2,000  metres)  is  thus  very  dark,  and  on  the  deep-sea  floor 
(the  benthonic zone), which  may  be  several  miles  in  depth,  darkness  is  complete. 

1  p.  224. 


RUDIMENTARY   EYES 


723 


It  would  seem,  indeed,  that  all  the  inhabitants  of  this  still,  cold,  dark  world 
should  tend  to  lose  their  eyes  ;  possibly  they  would  were  it  not  for  the 
development  of  luminous  organs,  a  common  acquisition  by  the  inhabitants 
of  the  benthos. 1 

Thus  among  abyssal  Molluscs  {Chiton,  etc.)  the  eyes  tend  to  degenerate 
even  in  Cephalopods  wherein  these  organs  are  usually  well  marked  ;  the 
only  known  blind  C'ephalopod,  however,  is  Cirroihaiima  murrayi,  an  octopod 
which  inhabits  the  N.  Atlantic  at  depths  of  approximately  3,000  metres 
(Chun,  1911).  Similarly  among  Crustaceans  living  at  moderate  depths,  the 
arrangement  of  the  pigment  surrounding  the  ommatidia  of  the  compound 
eyes  remains  permanently  in  the  dark-adapted  position,  while  in  bathy- 


FiG.  866. — The  Eye  of  a  Blind  Sel.\chian  Fish,  BEyrHOBATis. 

The  ocular  structures  are  of  the  most  rudimentary  t\-pe.  BV,  blood  vessel 
C,  cornea  ;  Car,  cartilage  ;  CC,  connective  tissue  ;  /,  iris  ;  P.  retinal  pigment 
R,  retina  (after  Brauer). 


pelagic  tj'pes  various  stages  of  degeneration  appear  wherein  all  pigment  is 

absent  {C ydodorijypef'  or  the  ommatidia  entirely  disappear  and  the  eye-stalks 

become   fused   with   the    carapace    or   are    converted   into   tactile   organs 

{Cymonomus,  etc.)  (Doflein,  1904).    Paradoxically,  side-by-side  with  species 

with  degenerate  eyes  dwell  other  Crustaceans   (shrimps,   etc.)  with  fully 

developed  and  pigmented  eyes,  frequently,  however,  in  creatures  of  a  roving 

habit  (Edwards  and  Bouvier,  1892). '^    In  general  among  bathypelagic  fishes, 

species  which  penetrate  to  lower  and  lower  depths  develop  progressively 

better  eyes,  adopting  all  possible  expedients  to  improve  their  vision  in  dim 

illumination — a  telescopic  shape,  an  immense  lens,  a  huge  pupil,  a  brilliant 

tapetum,    and   a   multiplication   of  the   rods — until  these   organs   become 

relatively  larger  than  in  any  other  Vertebrate.     But  below  500  metres  in 

many  instances  the  struggle  is  given  up  and  the  eyes  shrink  so  that  among 

the  deeply  benthonic   fishes  they   are  often  vestigial  and  functionless  or 

1  p.  736.  2  p_  166. 

3  Compare  the  "  wondrous-eyed  hopper  "  (Fig.  203),  an  inhabitant  of  the  deep  seas. 


724  THE   EYE   IN   EVOLUTION 

absent  ;  in  this  event  it  is  interesting  that  some  species  maintain  projicience 
by  developing  long  filamentous  "  feelers  "  (the  "  feeler  fish,"  Bathypterois). 
It  is  true  that  most  of  the  inhabitants  of  the  sea-bottom  retain  their  eyes  and 
that  in  some  families  these  are  neither  unusually  large  nor  small  (such  as  the 
grenadiers,  Coryphsenoididse)  ;  it  is  also  true  that  the  only  biological  value 
of  these  visual  organs  is  to  catch  the  fitful  gleams  of  luminescence  ;  but  it  is 
also  true  that  many  lose  them  (Alcock,  1902). 

Thus  among  Selachians  the  eyes  are  vestigial  in  several  families  of  the  rays — 
TyiMonarke,  Bengalichthys  and  Benthohatis .  The  eye  of  the  last,  for  example,  has  a 
crude  cornea,  a  rudimentary  iris,  an  undifferentiated  retina,  and  no  lens  (Fig.  866) 
(Brauer,  1908).  Among  Teleosts  in  some  deeply  bathypelagic  forms  such  as  Saccopharynx 
and  Cetomimus  the  eye  is  vestigial.  In  the  latter  the  oval  globe  is  only  0-7  inm.  in 
diameter,  the  lens  and  retina  are  rudimentary  and  the  pigment  epithelium  unusually 
thick  (Brauer,  1908).  Among  some  benthonic  Teleosts  the  eyes  may  be  still  more 
rudimentary  and  covered  with  opaque  skin — Barathronus,  Typhlonus,  Aphyomis,  and 


Fig.   867. — The  Blind  Deep-sea  Teleost,  Ipxops  aoassizi. 
Found  at  2,000  m.  (^  natural  size)  (after  Garman,  Albatross  Report,  1899). 

Tauredophidiwm.  An  inhabitant  of  the  ocean  floor,  Ipnops,^  is  the  only  Vertebrate 
known  to  have  no  trace  of  eyes  (Eigenmann,  1909)  ;  this  is  a  small  black  fish  with 
two  luminous  areas  (resembling  lanterns)  in  its  head  under  the  translucent  bones  of 
the  skull  where  the  eyes  might  be  expected,  possibly  adaptations  of  these  organs 
(Fig.  867). 

THE    CAVEBNICOLOUS    OR    LIMICOLINE    HABIT 

A  CAVERNicoLOUS  OR  LIMICOLINE  HABIT,  whereby  life  is  spent  in  the 
darkness  of  caves  or  crevices  or  in  a  similarly  lightless  environment  in  mud  or 
beneath  stones,  also  leads  to  a  tendency  for  ocular  regression.  This  is  seen 
among  cave-dwelling  worms  such  as  the  planarian  Kenkiidse,  or  among 
Arthropods  inhabiting  a  similar  environment.  In  the  latter  phylum  typical 
examples  are  seen  in  two  species  of  Onychophores,  Peripatopsis  alba  which 
lives  in  lightless  caves,  and  Typhloperipatus,  found  under  rocks;  in  the 
cavernicolous  beetle,  Anophthalmus,  which  is  possessed  only  of  a  dermal  light 
sense  (Marchal,  1910)  ;  the  eyeless  white  cave-crayfish,  Cambarus  ayersii, 
which  retains  some  light-sensitivity  in  its  cerebral  ganglion  (Wells,  1952)  ; 
and  the  cave-spiders  {Anthrobia)  which  are  entirely  sightless  ;  but  the 
phenomenon  is  most  markedly  seen  in  cave-dwelling  Fishes  and  Amphibians. 

^  iTTvos,  a  lantern  ;   wip,  eye. 


RUDIMENTARY   EYES  725 

Among  Invertebrates  with  such  degenerate  eyes  the  Isopod  Typhlocirolana — a 
small  Crustacean  found  in  a  cave  in  the  island  of  Majorca — may  be  taken  as  an 
example.  The  compound  eyes  are  minute  degenerate  bodies  \  mm.  in  diameter, 
without  pigment  in  the  ommatidia,  while  the  crystalline  cone  and  the  proximal  part 
of  the  retina  are  grossly  atrophied  (Menacho,  1913). 

CAVE-FISHES  ^  are  all  Teleosteans  and  it  would  seem  probable  that  the 
ancestors  of  most  of  them  can  be  traced  from  species  in  which  a  pre- 
adaptation to  ocular  regression  had  already  been  present  owing  to  a  previous 
existence  in  deep  seas  or  muddy  bottoms^;  few  of  them  {e.g.,  catfishes  of  the 
genus,  Rhamdia)  have  well-formed  eyes  ;  and  some  types  {e.g.,  the  Mexican 
catfish,  Anopticlithys  jordani)  show  all  grades  of  reduction  of  the  eye  from 
normal  organs  to  rudimentary  remnants.  The  latter  are  hatched  with  small 
but  complete  eyes,  lacking,  however,  a  circulation,  and  as  the  fish  matures 
these  gradually  degenerate  until  all  that  is  left  in  the  adult  is  a  most  rudi- 
mentary organ  lying  deeply  buried  in  a  recognizable  orbit  associated  with 
hyj3oplasia  of  the  optic  lobes  (Gresser  and  Breder,  1940-41  ;  Breder,  1942  ; 
Liiling,  1953-55  ;  Kuhn  and  Kahling,  1954  ;  Stefanilli,  1954).  Some  of 
the  cave-fishes  derive  from  deep-sea  types  such  as  the  Brotulidse  which 
emigrated  to  the  surface  and  there  sought  the  darkness  of  crevices  in  reefs  or 
caves.  Three  species  have  made  the  still  more  remarkable  transition  to 
fresh  water — Lucifuga  and  Stygicola  which  are  found  in  caves  in  Cuba,  and 
TyjMias  in  Yucatan.  Eigenmann  (1909)  concluded  that  these  Cuban  fishes 
initially  inhabited  caves  in  the  coral  beaches  where  they  remained  as  these 
caves  were  elevated  and  became  filled  with  and  enlarged  by  fresh  water  ; 
in  his  view  the  fishes  are  older  than  the  island  of  Cuba.  The  eyes,  which  lie 
under  the  skin,  are  best  developed  before  birth;  thereafter  they  progressively 
degenerate  until  in  old  age  they  are  represented  by  a  shrivelled,  pigmented 
vesicle,  lying  deeply  in  the  large  orbit,  a  process  perhaps  determined  by  a 
disturbance  of  the  circulation.  The  bottom-grubbing  catfishes  which 
habitually  shun  the  light  are  the  ancestors  of  other  types.  These  Siluroids 
which  encyst  themselves  in  the  mud  often  have  rudimentary  eyes  (Cope, 
1864)  ;  thus  the  eye  of  the  bull-head  catfish,  Amevurus,  has  an  ill-formed 
lens  and  a  retina  wherein  the  rods  are  large,  the  cones  few  and  small,  while 
the  outer  nuclear  layer  is  represented  by  only  two  rows  of  nuclei,  the  inner 
by  one,  and  the  ganglion  cells  by  a  few  widely-scattered  elements. 

The  Aniblyopsidfe,  the  North  American  group  of  cave-fishes  characteristic  of  the 
caves  of  the  Mississippi  basin,  are  of  considerable  interest  (Telkampf,  1844  ;  Wyman, 
1850-54  ;     Kohl,    1892-93  ;     Eigenmami,    1899-1909  ;     Hubbs,    1938).      They    are 

1  A  monograph  by  Carl  H.  Eigenmann,  the  Professor  of  Zoology  of  Indiana  University 
gives  a  good  account  of  the  Cave-Vertebrates  of  America  (Carnegie  Inst.,  Washington,  1909), 
including  a  particularly  illuminating  and  interesting  studj^  of  the  cave-fishes  of  the  Mississippi 
Valley  and  Cuba.  A  subsequent  monograph  by  Hubbs,  Fishes  from  the  Caves  of  Yucatan 
{Carnegie  Inst.  Wash.,  Pub.  No.  491,  pp.  261-295.  1938),  lists  all  known  blind  fishes  apart  from 
deep-sea  types. 

^  Anoptichthys  is  an  exception  in  that  it  probably  entered  cave  life  as  a  stray  and  on  losing 
its  vision  was  constrained  to  remain. 


726 


THE   EYE   IN   EVOLUTION 


negatively  lohototactic  and  if  exposed  in  a  well-lit  pool  will  immediately  seek  refuge 
and  hide  under  rocks.  In  Amblyopsis  the  eye  lies  deeply  under  the  surface,  the  lens 
is  vestigial  or  absent,  the  iris  is  represented  by  a  pigment-free  membrane  and  the 
retina  contains  only  a  few  ill-formed  cones.  Similar  rudimentary  eyes  are  found  in 
the  two  other  related  genera,  Typhlichthys  and  Troglichthys  ;  and  in  the  only  non- 
cavernicolous  representative  of  this  family,  Chologaster,  which  inhabits  the  swamps  of 
Kentucky  and  Tennessee,  the  eyes  which  lie  under  a  patch  of  pigment-free  epidermis 
are  reduced  rather  than  degenerate  ;    the  fish  does  not  dei^end  on  its  eyes,  however, 

for  detecting  or  securing  its  prey  or  for  avoiding  obstacles. 
Although  possessed  of  ears,  experiments  have  shown 
that  the  sense  of  hearing  of  the  Amblyopsidse  is  limited  ; 
the  tactile  sense  is  the  one  on  which  they  rely  to  find  and 
locate  their  food  for  which  purpose  they  are  provided 
with  numerous  tactile  ridges  princijaally  in  the  region  of 
the  head  (Eigenmann,  1909). 

Some  goby  fishes  (Gobiidte),  particularly  the 
"  sleepers  "  living  on  muddy  bottoms  or  in  crevices,  also 
have  degenerate  eyes.  Typhlogohius  calif orniensis,  a  blind 
fish  which  CO -habits  rocky  crevices  on  the  Californian 
coast  with  a  blind  species  of  shrimp  on  which  it  depends 
for  food,  has  relatively  normal  eyes  in  the  larval  stage 
which  become  small,  functionless  and  rudimentary  in  the 
adult,  lying  under  the  thick  skin  (Ritter,  1893)  ;  they 
lack  tapetum,  cones  and  vitreous,  while,  curiously,  the 
lens  may  be  either  very  large  indeed  or  absent.  It  is  as 
if  a  brave  strviggle  were  made  to  collect  what  light  there 
is  or,  alternatively,  the  attempt  has  been  abandoned. 
Trypauchen  and  Trypmichenophrys,  littoral  crevice-dwellers  in  Japan,  and  other  limico- 
line  gobies  as  Austrolethops,  and  the  sole,  Typhlachirus,  have  similarly  minute  or 
rudimentary  eyes  (Fig.  868)  (Franz,  1910-34).  Undersized  eyes  are  also  usual  in  the 
fresh-water  fishes  which  inhabit  silty  rivers  such  as  are  common  in  the  great  plains  of 
America  ;  only  occasionally,  as  in  Lake  Balaton  in  Western  Hungary,  an  immense 
shallow  lake  the  waters  of  which  are  so  turbid  as  to  be  virtually  ojiaque,  is  an  effort 
made  to  increase  the  sensitivity  of  the  eye  by  the  liberal  dejoosition  of  guanine  in  an 
unusually  well-developed  tapetum  (Wunder,  1926-30). 

AMPHIBIANS.  Amongst  the  Urodeles,  the  salamanders  which  hve  a 
secretive  existence  in  shallow  water,  in  caves,  in  mud  and  under  flat  stones, 
have  little  use  for  eyes.  These  organs  are  well  differentiated  in  the  larvse 
but  regress  at  metamorphosis  (Zeller,  1888)  (Fig.  869)  ;   as  we  have  already 


Fig.  868. — The  Eye  of  the 
Goby    Fish,    TRi-PAUCHEy 

WAK.E. 

The  eye  is  rudimentary 
and  functionless  (after 
Franz). 


Fig.   869. — -The  Olm,  Proteus  a.xgujaus  (Zool.  Soe.,  London). 


RUDIMENTARY   EYES 


727 


Figs.   870  and   871. — The  Eye  of  Photeus  axguisus. 


E»- 


Fig.  870. — A  vertical  section  through  a  rudimentary  lateral  eye  in  an  animal  of 
normal  cavernicolous  habit.  The  eye  is  seen  to  be  a  sim]3le  vesicle  containing 
vitreous-like  material  centrally.  It  is  surrounded  by  jsigmentary  eijithelium  and, 
owing  to  the  absence  of  the  lens,  the  lips  of  the  optic  cup  meet  at  the  distal 
aspect  of  the  vesicle.  The  retina  is  unusually  thick  and  relativelj'  undifferenti- 
ated. The  entire  organ  lies  underneath  the  skin  (E.  F.  Finchani). 


^^^tr*»^' 


'^J^f" 


Fig.  871. — Mciidional  section  through  the  eye  of  an  animal  kept  in  daylight.  Note 

the  presence   of  the   ill-formed  cornea,   the   well-formed  lens  and  uveal  tract, 

the  hyaloid  type  of  vascularization  and  the  highly  differentiated  retina  (after 
Kammerer). 


728 


THE   EYE   IN   EVOLUTION 


noted,  however,  they  may  remain  large  and  relatively  well  formed  if 
development  from  the  larval  to  the  adult  stage  is  artificially  conducted  in 
bright  illumination  (Kammerer,  1912)  (Figs.  870-1).  In  natural  conditions, 
however,  they  are  concealed  under  the  skin,  microscopic  and  either  capable 
merely  of  a  directional  light  sense,  as  in  limicoline  types,  or  functionless,  as 
in  cave-living  types.  Other  Urodeles,  on  the  other  hand,  such  as  the 
newt  (Triturus)  or  the  North  American  axolotl,  Amhy stoma,  have  rela- 
tively simple  but  effective  eyes,  lacking  iris  folds  and  with  a  spherical  lens, 

while  in  terrestrial  salamanders  the  eyes,  though 

small,  are  well  formed.^ 

Among  the  cave  forms  the  olm,  Proteus  may  be 
taken  as  a  typical  example,  several  species  of  which 
inhabit  the  caves  of  Carinthia  and  Dalmatia  (Fig.  869.) 
The  eyes  of  the  adult  Proteus  anguinus  are  minute 
spheres  less  than  0-5  mm.  in  diameter  seen  as  shadows 
deep  underneath  the  skin.  They  form  simple  vesicles 
without  cornea  or  lens  ;  originally  a  inere  accumulation 
of  epidermal  cells  within  a  capsule,  the  capsule  disinte- 
grates and  the  cells  of  the  lens  are  replaced  by  connective 
tissue  (Fig.  870).  The  ocular  cavity  is  almost  entirely 
taken  up  by  a  retina  of  a  most  rudimentary  type  and 
between  it  and  the  external  epithelium  lie  the  open 
remains  of  the  optic  vesicle.  The  visual  cells  are  globular 
and  bear  no  resemblance  to  rods  or  cones  ;  there  is  an 
elementary  nuclear  layer  and  a  reticular  layer  while  the 
optic  nerve  is  vestigial  and  largely  neuroglial  (Fig.  872) 
(Configliachi  and  Rusconi,  1819  ;  Desfosses,  1882  ;  von 
Hess,  1889  ;  Kohl,  1889-92  ;  Benedetti,  1922  ; 
Stadtmiiller,  1929). 


Fig. 


872. — The   Retina  of 
Proteus  axguinus. 


G, 

ganglion 

cells  ; 

IN, 

inner 

nuclear 

layer  ; 

IR, 

inner 

reticular 

layer ; 

ON, 

outer 

nuclear 

layer ; 

OR, 

outer 

reticular 

layer 

V, 

visual  elements  (after  Kohl). 


Similarly  rudimentary  eyes,  even  more  degenerate  than  those  of  their 
cavernicolous  European  relatives,  are  found  in  related  types  such  as  the 
American  blind  salamanders,  TyjMomolge,  inhabiting  the  underground 
streams  of  Texas,  and  Haideotriton  ;  such  eyes  are  functionless.  The  eyes 
of  Typhlotriton,  however,  a  salamander  found  in  the  caves  of  the  Mississippi 
Valley,  normal  in  the  larva  but  degenerate  in  the  adult,  are  more  fully  formed 
with  a  lens  and  a  considerable  degree  of  retinal  differentiation  although  the 
rods  and  cones  disappear  in  the  fully  grown  animal  ;  these  constitute  a  link 
between  the  degenerate  eyes  of  the  Proteidae  and  the  normal  urodelan  eye 
(Eigenmann,  1909). 


THE    FOSSORIAL   HABIT 


The  FOSSORIAL  OR  BURROWING  HABIT  has  led  to  the  regression  of  the 
eyes  of  many  types  of  Invertebrates  and  Vertebrates. 

Thus  among  worms  which  burrow  on  the  land  {Lmnbricus  terrestris)  we 
have  already  seen  that  the  visual  organs  are  of  a  very  primitive  type,-  while 


p.  346. 


190. 


RUDIMENTARY   EYES  729 

those  Polychsetes  which  burrow  in  the  sand  or  mud  of  the  sea-shore  may  be 
without  visual  organs  (the  lob-worm,  Arenicola  marina)  ^  ;  sometimes  the 
larval  forms  have  eyes  which  disappear  on  reaching  adulthood  (Tampi, 
1949).  Similarly,  sand-burrowing  Molluscs  may  be  unprovided  with  eyes 
(elephant's  tooth  shell,  Dentalium)."  Among  Arthropods,  those  ]M\Tiapods 
which  burrow  in  moist  forest  debris  may  lack  eyes  (Pauropus),^  as  well  as 
certain  burrowing  tyf)es  of  woodlice  (Arcangeli,  1933).  Among  Insects 
the  primitive  minute  Protura  which  burrow  in  moist  soils  impregnated 
with  organic  debris  and  are  widely  found  in  Euroj^e,  America  and  India, 
are  without  eyes,  antennae  and  ^ings  ;  but  the  most  interesting  eyeless 
insects  are  termites  and  ants. 

Termites  (Isoptera),  often  mistakenly  called  "  white  ants,""  are  widely 
found  in  Europe,  Asia  and  Africa  but  are  unrepresented  in  Great  Britain  ; 


Fig.     873. — Termite  Fig.  874. — Male  Driver  Fig.   87.5. — Female   Dri- 

SoLDiER.  Ant.  ver  Ant. 

while  they  are  extremely  sensitive  to  light,  most  are  blind  and  are  completely 
without  eyes  (Fig.  873).  They  live  in  teeming  millions  in  vast  underground 
communities  governed  by  a  complex  and  efficient  social  system  and  alive 
with  an  immense  and  ordered  business  ;  nevertheless,  blind  and  eyeless 
though  they  are,  they  conduct  long  regimented  marches  overland  to  seek 
and  convey  back  the  wood  they  eat,  and  the  young  alates  temj)orarily 
develop  wings  in  a  frequently  disastrous  nuptial  flight  in  the  air. 

Most  ants  (Formicidse)  have  large  and  well-developed  compound  eyes 
but  in  some  forms  of  Dorylinte  which  dwell  under  the  ground,  eyes  are 
lacking.  The  wandering  ants  {Eciton)  of  Central  and  South  America  show 
eyes  in  various  stages  of  disappearance — small  eyes  without  an  optic  nerve. 
orbital  sockets  without  an  eye,  and  so  on — while  the  female  driver  ant 
{Dorylus)  of  Africa  has  no  evidence  of  ocular  or  orbital  remnants  whatever. 
It  is  interesting  and  perhaps  significant  that  in  the  latter  species  the  winged 
male  is  possessed  of  eyes  surpassing  those  of  most  insects,  while  all  females, 
whether  queen,  fighter  or  worker,  are  blind  (Figs.  874-5)  (Maeterlinck, 
1927-30  ;   Marais,  1937). 

It  would  seem  probable  that  like  all  other  members  of  the  Hymenojatera  (wasps, 
bees,  etc.)  all  ants  were  originally  sighted  and  it  might  seem  logical  that  the  under- 
ground types  might  tend  to  lose  their  eyes  ;  but  why  the  eyeless  female  should  continue 
1  p.  191.  2  p.  197.  3  p.  211. 


730  THE   EYE   IN   EVOLUTION 

to  produce  the  fully-eyed  male  is  not  clear.  Moreover,  although  their  nest  is  under- 
ground, these  ants  are  nomadic  on  the  surface  and  their  armies,  the  members  of  which 
are  completely  blind,  are  forever  on  the  move.  It  is  to  be  remembered  that  the 
big-eyed,  innocuous  male  driver  ant  is  a  gentle  and  relatively  useless  creature — merely 
a  stud  animal  with  a  momentary  function  as  likely  as  not  never  to  be  fulfilled  ;  while 
the  monstrous  regiment  of  his  sisters  ranks  among  the  most  ferocious  and  blood- 
thirsty creatures  the  world  knows.  It  has  been  suggested  that  these  unsexed  females 
which  march  ahead  against  any  obstacle  and  into  any  danger,  which  attack  and  devour 
anything  alive  in  their  line  of  march,  would  find  difficulty  in  maintaining  the  iron 
discipline  of  their  ranks  if  they  were  distracted  by  vision,  and  that  blindness  is  therefore 
an  asset  of  evolutionary  value  to  the  ferociovxs  and  purj^osive  female  but  not  to  the 
idle  and  harmless  male  (Crompton,  1954).  The  suppression  of  eyes  in  this  view  (which 
many  would  not  accept)  is  positive,  differing  entirely  from  the  mechanism  which 
usually  indvices  eyelessness. 

On  the  other  hand,  it  may  be  that  some  other  system  of  inter-communication 
exists  of  which  we  have  no  knowledge,  outside  the  visible  limits  of  the  electromagnetic 
spectrvim.  It  is  indeed  difficult  to  conceive  how  otherwise  the  extraordinarily  complex 
activities  within  these  underground  cities  could  be  conducted,  not  only  as  an  ordered 
routine  bvit  with  coordinated  variations  to  meet  unexpected  emergencies  of  construc- 
tion or  war  with  equal  facility,  in  which  each  member  of  the  community — cjueen,  king, 
soldier,  policeman  or  worker — finds  an  appointed  place.  It  may,  indeed,  be  that  eyes 
have  become  useless  owing  to  the  development  of  senses  other,  and  perhaps  more 
efficient,  than  our  own. 


Fig.   876. — Ichthyophis. 

A  subterranean  burrowing  Amphibian,  limbless,  somewhat  resembling  an  earth- 
worm ;    the  eyes  are  small,  functionless  and  covered  Ijy  skin  (head  on  right). 

Among  Vertebrates,  fossorial  Amphibians,  Reptiles  and  Mammals  are 
encountered  ;  in  a  sense  some  limicoline  fishes  (catfishes,  etc.)  which  we  have 
already  discussed  might  be  brought  into  this  category. 

Among  Amphibians,  the  Csecilians  (Apoda)  form  a  peculiar  archaic 
group  highly  specialized  for  burro wmg  (Fig.  876) — Ccecilia  of  South  America, 
Ichthyojjhis  of  Southern  Asia,  Hypogeophis  of  East  Africa,  Siphoiiops  of 
America  ;  with  the  exception  of  the  aquatic  Typhlonectes,  all  spend  most  of 
their  lives  underground.  Their  most  efficient  sensory  organ  is  a  retractile 
sensory  tentacle  situated  at  the  anterior  border  of  the  orbit,  while  the  eyes 
are  very  small  (less  than  1  mm.)  and  can  be  useful  only  in  light -detection. 

The  minute  eyes  of  the  Crecilians  are  attached  to  the  skin  and  lie  in  a  roomy 
orbit,  largely  filled  by  a  Harderian  gland  which,  however,  is  used  to  lubricate  the 
sensory  tentacle  ;  the  levator  bvilbi  muscle  of  Amphibians  is  vised  as  a  compressor 
of  this  gland  to  assist  in  its  evacuation.  Two  of  the  other  extra-ocular  muscles  are 
commandeered  to  move  the  tentacle  and  have  no  action  on  the  immobile  eye,  the 
retractor  bulbi  acting  as  a  retractor  of  the  tentacle  and  the  internal  rectus  as  a  retractor 
of  its  sheath.  The  cornea  is  fused  with  the  skin,  there  is  no  ciliary  body  or  mesodermal 
iris,  the  lens  is  large,  spherical  and  usually  cloudy,  while  the  retina  is  provided  only 


RUDIMENTARY   EYES 


731 


with  simple  but  massive  rods,  and  the  two  nv;clear  layers  and  the  ganglion  cells  are 
represented  by  a  few  rows  of  si:)arse  cells  (Kohl,  1892  ;  Hanke,  1912  ;  Engelhardt,  1924). 

Among  Reptiles,  burrowing  snakes  and  lizards  come  into  the  same 
category.  Within  the  group  of  snakes  (Ophidia)  the  lowest  types  are  the 
T\^3hlopidse.  blind  subterranean  burrowers  usually  smaller  than  earth- 
worms which  occur  in  most  of  the  w^armer  parts  of  the  earth.  The  eyes  are 
tiny  and  vestigial.     It  would  seem  that  when  the  snakes  originally  went 


FiC4.   877. — The  Eye  and  Orbit  of  the  Blind  Snake,    Ttphlops. 

The  globe  is  minute,  less  than  1  iTim.  in  diameter.  The  heavily  pigmented  uvea,  a, 
and  the  ill-formed  retina,  r,  are  well  seen.  Most  of  the  cavity  of  the  eye  is  taken 
up  by  the  large  lens.  Anterior  to  this  is  the  tenuous  cornea,  the  enclosed  conjunctival 
sac  and  the  dermal  "  sijectacle."    m  is  a  tenuous  extra-ocular  muscle  (0"Day). 

underground  the  eyes  became  vestigial,  and  when  they  again  emerged  from 
the  ground  the  eye  had  to  be  reconstructed,  but  those  of  this  primitive 
species  retained  their  simple  form  (Walls,  1942)^. 

The  eye  of  Typhlops,  a  blind  snake  widely  distributed  in  the  Southern  Hemisphere 
and  South  East  Europe,  which  lives  on  worms  and  insects  obtained  by  burrowing,  has 
a  rudimentary  uvea  and  a  small  embryonic  cellular  lens  ;  the  retina  contains  few  and 
rudimentary  visual  cells  and  insignificant  nuclear  and  ganglion-cell  layers  while  a 
central  area  is  lacking  (Kohl,  1892)  (Fig.  877).  A  similarly  primitive  eye  is  seen  in 
Typhlops  lumbricalis,  a  blind  snake  seen  in  the  West  Indies  and  Guiana  (Muhse,  1903), 
and  in  the  uropeltid  snake,  Rhinophis  (Baumeister,  1908). 

1  p.  383. 


Figs.   878  to  880. — The  Eye  of  the  Mole,   Talpa, 


Fig.   878. — Section  through  the  whole  eye. 
Note  the  pore-hke  opening  in  the  Uds,  the  elementary  uvea,  the  cellular  lens, 


and  the  hyaloid  form  of  the  central  retinal  arterj'  (after  Ciaccio). 


/IM 


»     *     •      '  • 


Fig.    879.— The   lens. 

Showing  the  immature  cellular  state 
and  the  persistence  of  the  vesicle  (after 
RabI). 


Fig.   880.— The  retina. 

The  layering  of  the  retina  is  relatively 
well-developed  :  G,  ganglion  cell  layer  ; 
IN,  inner  nuclear  layer  ;  ON ,  outer 
nuclear  layer.  Blood  vessels,  B  V ,  are  seen 
in  the  inner  layers  and  there  is  an  external 
limiting  membrane,  an  internal  limiting 
membrane,  IM,  and  nucleated  sui^porting 
fibres,  SF.  Three  types  of  visual  cells 
are  present  :  rods,  R,  cones,  C,  and 
"  indifferent  "   elements,   /    (after   Kohl). 


RUDIMENTARY   EYES  733 

Degenerate  subterranean  lizards  (Amphisbsenidge),  which  are  without  Hmbs  and 
almost  without  scales — such  as  the  worm-like  Atyiphisbaina  punctata  of  Cviba  or  the 
similarly  legless  Bhineura  floriclana  abundant  in  parts  of  Florida — have  eyes  equally 
minute  buried  beneath  ojaaque  skin,  rarely  consisting  of  more  than  a  capsule  of 
connective  tissue  enclosing  an  optic  cup  and  a  cellular  lens  without  fibre-formation  ; 
extra-ocular  muscles  and  iris  are  lacking  (Payne,  1906  ;  Eigenmann,  1909).  It  is 
interesting  that  both  in  these  snakes  and  in  lizards,  Harder's  gland  is  many  times 
larger  than  the  eye. 

Among  Mammals  a  similar  degeneration  of  the  eye  is  seen  in  a  small 
group  of  animals  with  btu'rowing  habits  which  have  led  to  a  life  of  permanent 
darkness.  These  fossorial  animals  have  little  vision  but  an  exquisitely 
developed  sense  of  smell  on  which,  indeed,  most  of  them  depend  for  their 
living  ;  the  eyes  are  minute  in  size  but  relatively  well  differentiated, 
almost  although  not  completely  covered  by  skin  to  which  they  are  adherent. 
In  the  common  European  mole  only  a  minute  pore,  0-1  mm.  in  diameter,  is 
left  in  the  skin  through  which  little  but  the  merest  perception  of  light  can  be 
possible.  In  the  blind  mole  of  Southern  Europe,  Talpa  cceca,  this  aperture 
is  said  to  be  usually  lacking  (Weber.  1904  ;  Kazzander,  1921).  In  addition 
to  the  European  moles,  this  group  includes  other  Insectivores — the  South 
African  and  Asian  golden  mole,  Chrysochloris  (Sweet,  1909),  the  American 
water-mole,  Scalops  aquaticus  (Slonaker,  1902) — as  well  as  the  marsupial 
mole,  Notoryctes  typhJoi^s  (Sweet,  1909)  and  the  rodent  ''  moles  "  such 
as  Spalax,  and  EUobius  which  belong  to  the  hamster  branch  of  the  mouse 
family. 

The  eye  of  the  mole,  Talpa,  may  be  taken  as  typical,  and  appears  as  if  it  had 
ceased  to  progress  from  an  early  stage  of  embryological  development  (Lee,  1870  ; 
Ciaccio,  1884  ;  von  Hess,  1889  ;  Kohl,  1892-95  ;  C.  Ritter,  1899  ;  Henderson,  1952) 
(Figs.  878-9).  The  corneal  epithelium  may  consist  of  a  single  layer  of  cells,  the  iris  is 
sinall  but  j^resent,  and  the  choroid,  unlike  the  mammalian  but  like  earlier  vertebrate 
types,  has  a  single  layer  of  vessels  ;  the  lens  is  embryonic  and  cellular,  while  the  central 
artery  of  the  retina  retains  a  hyaloid  form  and  grows  into  the  vitreous.  In  the  retina, 
rods  and  cones  are  distinguishable  and  intermingled  with  them  are  cells  of  an  inter- 
mediate type,  but  the  normal  layering  of  the  mammalian  retina  is  evident  (Fig.  880). 
The  non-neural  parts  of  the  eye  are  therefore  particularly  retarded,  and  it  is  interesting 
that  Tuscjues  (1954-55)  found  that  their  relatively  normal  development  could  be 
stimulated  by  large  doses  of  thyroxine  :  the  globe  increased  in  size,  the  lids  separated, 
the  lens  developed  with  the  jsroduction  of  fibres  and  the  entire  organ  began  to  take 
on  the  appearance  of  the  eye  of  sighted  animals. 

THE    PARASITIC    HABIT 

In  most  internal  parasites  the  eyes  are  rudimentary  or  absent  for  the 
inside  of  an  animal  is  as  lightless  an  environment  as  any  ;  moreover,  the 
sedentary  life  associated  with  parasitism  can  proceed  in  the  absence  of  other 
activities  so  that,  in  addition  to  the  recession  of  the  visual  organs,  those  of 
locomotion  and  often  of  digestion  are  reduced. 

In  the  large  number  of  endo-parasitic  Invertebrates,  eyes  are  lacking 


734 


THE   EYE   IN   EVOLUTION 


or  vestigial.  Thus  in  the  flukes  (Trematodes)  and  in  the  round-  or  thread- 
worms (Nematodes)  the  eyes  may  be  present  in  the  freely-swimming  larval 
stage  but  in  the  parasitic  adult  sense  organs  are  limited  to  papillse  on  the 
lips.  In  tape-worms  (Cestodes)  sense  organs  are  lacking.  Similarly  eyes  and 
other  sense  organs  are  not  found  in  parasitic  Crustaceans  such  as  Sacculina, 
an  organism  parasitic  on  the  abdomen  of  crabs.  A  similar  example  among 
Insects  is  provided  by  Stylops  ;  the  winged  male  has  many  ocelli  but  the 
minute  female  which  is  parasitic  within  bugs  and  bees  is  eyeless. 


Fig.  881. — The  Hag-fish,  Mr.xiyE  (after  Dean). 


Among  the  Cyclostomes,  the  hag-fishes  have  rudimentary  eyes  which 
give  no  response  to  light.  These  small  eel-like  creatures  live  partly  in  the 
mud  at  the  sea  bottom  and  are  partly  voraciously  parasitic  within  larger 
fishes.  The  glutinous  hag,  Myxirie,  with  a  wide  distribution  in  the  oceans, 
approaches  more  nearly  than  any  other  Vertebrate  the  condition  of  an 
internal  parasite  (Fig.  881)  ;  in  other  species  such  as  the  slime-hag,  Epta- 
tretus  in  the  Southern  Hemisphere  and  BdeUostorna,  found  in  South  African 
and  Pacific  waters,  the  eyes  are  not  so  degenerate  (see  Henckel,  1944).    The 

eyes  of  the  ecto-parasitic  lamprey,  on  the  other 

hand,  are  well-formed.^ 

In  Myxine  glutinosa,  the  eyeball,  about  0-5  mm.  in 
diameter,  is  merely  a  simple  vesicle  lying  in  fat  buried 
beneath  the  skin,  almost  entirely  filled  with  a  poorly 
differentiated  retina  doubled  over  upon  itself  (Fig.  882). 
Extra-ocvilar  muscles,  cornea,  iris  and  ciliary  body  are 
unrecognizable,  the  sclera  and  choroid  are  undifferen- 
tiated, the  lens  is  lacking,  and  there  is  no  pigment  either 
in  the  uvea  or  retina.  The  retina  retains  the  form  of  the 
cavity  of  the  optic  vesicle,  visual  cells  are  not  recogniz- 
able as  such,  layering  of  the  retinal  elements  is  crude  and 
the  optic  nerve  is  vestigial  (Kupffer,  1868  ;  Kohl,  1892  ; 
Retzius,  1893  ;  Allen,  1905  ;  Eigenmann,  1909  ;  and 
others). 

It  is  noteworthy  that  although  the  eyes  are  function- 
less,  a  dermal  sensitivity  to  light  exists  concentrated 
particularly  in  the  head  and  cloacal  regions  and  disappearing  when  the  animal  is  skinned. 
There  is  a  long  latent  period  of  about  20  sees,  before  the  animal  commences  to  swim  and 
thereafter  to  burrow.  The  photochemical  reaction  is  associated  with  vitamin  A  j^  and  the 
response  is  mediated  nervously  through  the  spinal  cord  (Newth  and  Ross,  1955  ;  Steven, 
1955). 


Fig.  882. — The  Eye  of  the 
Hag-fish,   Myxine    gluti- 

AOSA  . 

The  eye  is  a  simple  vesicle 
almost  entirely  filled  with 
poorly  differentiated  retina 
doubled  over  itself  (after 
Diicker). 


Endo -parasitic  Fishes  are  rare,  and  the  parasitic  habit  is  not  found  among  higher 
Vertebrates,    The  eel,  Simenchelys  parasitica,  an  inhabitant  of  deep  seas  and  parasitic 


263. 


RUDIMENTARY   EYES 


735 


in  halibut  and  other  large  fishes,  has  an  eye  covered  by  semi -opaque  skin,  but  it  is  not 
rudimentary  ;  nor  are  the  minute  eyes  of  the  other  j^arasitic  Teleost,  the  pearl-fish, 
Encheliophis  jordani,  which  spends  much  of  its  life  inside  the  cloacie  of  sea-cucumbers. 


Alcock.  A  Naturalist  in  Indian  Seas  (1902). 
Allen.    Anat.  Anz.,  26,  208  (1905). 
Arcangeli.    Arch.  zool.  ital.,  19,  389  (19.33). 
Baumeister.      Zool.  Jb.,  Abt.  Anat.,  26,  423 

(1908). 
Benedetti.      Atti  Cong.  Soc.  progr.  Sci.,  Roma, 

598  (1922). 
Brauer.     IJ'/.ss.  Ergebn.  dtsch.  Tiefssee  E.vped., 

Jena  (1908). 
Breder.     Zoologica  (N.Y.),  27,  7  (1942). 
Chun.     Cirrothauma,   ein  blinde  Kephalopod, 

Leipzig  (1911). 
Ciaccio.     Mem.    Accad.   Sci.    1st.    Bologna,   5 

(1884). 
Configliachi  and  Rusconi.     Del  proteo  anguino 

di  Laurenti,  Pavia  (1819). 
Cope.    Proc.  Acad.  nat.  Sci.  Phila.,  231  ( 1 864). 
Crompton.     Wai/s  of  the  Ant,  London  (1954). 
Desfosses.     Arch.  Ophtal.,  2,  406  (1882). 
Doflein.     Valdivia  E.vpedition,  6  (1904). 
Edwards  and  Bouvier.    .4?;/;.  Sci.  nat.  (Zool.), 

13,  185  (1892). 
Eigenmann.       Proc.  Indiana  Acad.  Sci.,  230 

(1898)  ;    239  (1899). 
Arch.  Entw.  Mech.  Org.,  8,  545  (1899). 
Proc.  Wash.  Acad.  Sci.,  4,  533  (1902). 
Cave    Vertebrates   of  America,    Washington 

(1909). 
Engelhardt.      Jena.    Z.    Xattirwiss.,    60,    241 

(1924). 
Franz.     Abh.  math.-phys.  Klas.se  Akad.  Wiss. 

Munchen,  Suppl.-Bd.,  4,  1  Abh.  (1910). 
Hb.  d.  vergl.  Anat.  d.  Wirbelliere,  2  (3),  989 

(1934). 
Gresser  and  Breder.  Zoologica  {X.Y.).  25,  1  13 

(1940):  26.  123  (1941). 
Hanke.     Arch,  vergl.  Ophthal.,  3,  323  (1912). 
Henokel.     Bol.  Soc.  Biol.  Concepcion,  19,  69 

(1944). 
Henderson.     Brit.  J.  Ophthal..  36,  637  (1952). 
von  Hess.  C.  v.  Graefes  Arch.  OpldJtal.,  35  (1), 

1  (1889). 
Hubbs.     Publ.  Carnegie  Inst.  Wash.,  No.  491, 

p.  261  (1938). 
Kalmus.     Proc.  roy.  ent.  Soc.  Lond.,  A,  20,  84 

(1945). 
Kammerer.  Arch.  Entw.  Mech.  Org.,  33,   349 

(1912). 
Kazzander.     Anat.  Anz.,  54,  440  (1921). 
Kohl.     Zool.  Anz.,  12,  383,  405  (1889)  ;    14, 

93  (1891). 


Kohl.  Bibl.  Zool.,  TeW  l.Heft  13,  1  (1892);  Tell 

2,  Heft  14,  1  (1893)  ;    Tail  3,  179  (1895). 
Kuhn    and    Kahling.      E.cperientia.    10,    385 

(19.54). 
Kupffer.      Studien    znr    vergl.    Entivickl.    der 

Cranioten,  ]Miinchen  (1868). 
Lee.     Proc.  roy.  Soc.  B.  18,  322  (1870). 
Luling.     Zool.  Anz.,  151,  289  (1953). 

Zool.  Jb.,  Abt.  allg.   Zool.   Physiol,  65,  9 

(1954). 
Xaturwiss.  Rundschau,  197  (1954). 
Zool.  Jb.,  Abt.  Anat.,  74,  401  (1955). 
Maeterlinck.       The    Life    of   the    White    Ant, 

London  (1927). 
The  Life  of  the  Ant.  London  (1930). 
Marais.     The  Soul  of  the  White  Ant  (Trans,  by 

de  Kok),  London  (1937). 
Marchal.     Richet's  Dictionnaire  de  Physiol. ,9, 

273  (1910). 
Menacho.     Arch,  vergl.  Ophthal.,  3,  1  (1913). 
Muhse.     Biol.  Bull.,  5,  261  (1903). 
Xewth  and  Ross.    J.  e.vp.  Biol..  32,  4  (1955). 
Ogneff.     Anat.  Anz.,  40,  81  (1911). 
Payne.     Biol.  Bull..  11,  60  (1906). 
Retzius.     Biologische  U ntersuchungen,  Stock- 
holm, 5  (1893). 
Ritter,  C.     Arch.  mikr.  Anat.,  53,  397(1899). 
Ritter,    W.    E.       Bull.     Mus.    comp.     Zool. 

Harvard,  24,  51  (1893). 
Slonaker.    J.  comp.  Neurol.  Psychol.,  12,  335 

(1902).- 
StadtmiUier.    Morphol.  Jb.,  61,  221  (1929). 
Stefanilli.    E.vperientia  (Basel),  10,  436  (1954). 
Steven.    J.  e.vp.  Biol.,  32,  22  (1955). 
Sweet.     Quart.  J.  micr.  Sci.,  50,  547  (1906)  ; 

53,  327  (1909). 
Tampi.      Proc.    Indian   Acad.   Sci.,    29,    129 

(1949). 
Telkampf.     Arch.  Anat.  Physiol.,  381  (1844). 
Tusques.     C.  B.  Acad.  Sci.  (Paris),  238,  2562 

(1954)  ;    240,  2015  (1955). 
Walls.     The  Vertebrate  Eye,  Michigan  (1942). 
Weber.     Die  Sdugetiere,  Jena  (1904). 
Wells.    Anat.  Rec,  113,  613  (1952). 
Wimder.     Z.  vergl.  Physiol.,  4,  22  (1926)  ;    11, 

749  (1930). 
Wyman.     Proc.  Bost.  Soc.  nat.  Hist.,  3,  349 

(1850)  ;    4,  359  (18.54). 
Amer.  J.  Sci.  Arts,  17,  258  (1854). 
Zeller.     Zool.  Anz.,  11,  570  (1888). 


CHAPTER   XXI 
LUMINOUS  ORGANS 


This  book  opened  with  a  discussion  on  the  action  of  Hght  upon  hving 
organisms  ;  a  suitable  postscript  to  this  Vohime  is  a  passing  (but  not  an 
exhaustive)  reference  to  the  opposite  process — the  production  of  hght  by 
organisms.  Moreover,  many  luminous  organs,  although  not  homologous 
with  eyes,  have  a  structure  so  similar  that  a  short  description  of  the 
phenomenon  of  bioluminescence  can  hardly  fail  to  interest  the  reader. 

Bioluininescence  is  one  of  the  most  fascinating  subjects  in  biology  and  it  is  not 
surprising  that  the  emission  of  hght  by  hving  creatures  attracted  attention  from  very 
early  times.  The  luminescence  of  rotting  vegetation  and  putrid  flesh  was  known  to 
Aristotle  and  classical  writers  such  as  Pliny  wrote  in  detail  of  the  phenomenon  as  seen 
in  fungi  on  land  and  marine  animals  which  are  responsible  for  the  phosphorescence 
of  the  sea.  The  early  literature  is  full  of  delightful  descriptions  of  the  beauty  of  some 
of  the  observed  phenomena,  but  modern  work  may  be  said  to  have  begun  with  the 
French  and  Italian  naturalists,  A,  de  Quatrefages,  whose  classical  works  appeared 
between  1843  and  1862,  and  P.  Panceri,  whose  observations  were  published  between 
1870  and  1878.  It  is  interesting  that  Max  Schultze,  the  great  anatomist  of  Bonn, 
published  a  detailed  account  of  the  luminous  organ  of  the  fire-fly,  Lampyris  splendidula 
(1865).  More  recently  the  researches  of  Raphael  Dubois  who  published  some  56 
important  papers  between  1884  and  the  appearance  of  the  masterly  svimmary  of  his 
ideas  on  the  j^roduction  of  animal  light  in  Richet's  Dictionnaire  de  Physiologie  (1928), 
laid  the  foundations  of  otir  biochemical  knowledge  of  the  problem  ;  most  of  his 
classical  work  was  done  on  the  mollusc,  Pholas,  and  from  experiments  on  the  elaterid 

beetle  he  conceived  the  idea  that  the  pro- 
duction of  light  was  caused  by  the  inter- 
action between  an  oxidizable  compound, 
luciferin,  and  an  oxidizing  enzyine,  luci- 
ferase.  In  modern  times  the  foundations 
laid  by  Dubois  have  been  consolidated  by 
the  Dutch  School  associated  particularly 
with  the  names  of  A.  J.  Kluyver  and  K.  L. 
van  Schouwenburg  of  Delft,  and  to  a  still 
greater  extent  by  E.  Newton  Harvey 
1887 — ),  Professor  of  Biology  at  Princeton 
University  (Fig.  883).  Harvey  has  made 
the  subject  of  bioluminescence  his  life-study, 
not  only  by  elucidating  the  complicated 
chemistry  which  underlies  the  production 
of  light,  but  also  by  travelling  far  and  wide 
over  land  and  sea  for  over  forty  years  with 
all  the  enthvisiasm  of  a  born  naturalist,  ob- 
serving the  phenomena  in  the  native  haunts 
of  light -producing  animals.  His  impressive 
output  of  over  80  papers  on  this  subject 

730 


Fig. 


883. — E.  Newton  Harvey 
(1887 ). 


LUMINOUS   ORGANS  737 

is  summarized  in  his  three  classical  books — The  Nature  of  Animal  Light  (1920),  Living 
Light  (1940),  and  Dioluminescence  (1952).  Rarely  has  a  biologist  made  a  subject  so 
peculiarly  his  own. 

The  Occurrence  of  Bioluminescence 

BiOLUMiNESCEXCE,  the  production  of  light  b}^  Hving  organisms,  is  a  very 
widespread  phenomenon,  for  it  is  seen  among  fungi, ^  in  many  types  of  bacteria 
and  in  scattered  representatives  of  all  the  animal  phyla  from  Protozoa  to 
Fishes.  Several  fungi  '^  have  this  property,  some  of  them  j^arasitic  on  living 
vegetation,  such  as  Agaricus  olearius  which  grows  at  the  foot  of  the  olive 

Figs.   884  and   885. — Luminous  Organs  associated  with  the  Eyes  in  Fish. 

In  both  fishes  the  himinous  organ  is  a  compact  mass  of  white  tissue  lying 
underneath  the  eye,  the  back  of  which  is  covered  with  black  pigment  to  keep  the  light 
from  the  eye  of  the  fish.  The  organ  is  composed  of  a  large  lunnber  of  glatidular  tubes 
containing  luminous  bacteria  in  great  abundance  which  seem  to  be  the  source  of  the 
light.  The  organ  is  constantly  luminous  but  the  two  fish  have  developed  different 
mechanisms  to  extinguish  the  luminescence  periodically  (after  Hein). 


(a) 

Fig.  885. 

Fig.  884. — Photoblepharon  palpebnitus,  showing  the  luminous  organ  (cross- 
hatched)  exposed  (a).  On  the  ventral  border  of  the  organ  is  a  fold  of  opaque  black 
tissue  which  can  be  drawn  up  over  the  surface  of  the  organ  like  an  eyelid,  thus 
extinguishing  the  light  (b).  On  its  retraction  the  luminescence  again  becomes 
evident  (c). 

Fig.  885. — Anomalops  katoptron.  The  luminous  organ  (cross-hatched)  is 
inverted  into  a  pocket  of  pigmented  tissue  so  that  the  light  is  periodically  obscured. 

trees  of  Southern  Europe  and  served  as  the  foiuidation  of  modern  experi- 
mental work  on  this  subject  by  Fabre  (1855),  while  to  others  is  due  the 
luminescence  of  decaying  wood  in  the  forests,  a  phenomenon  known  to 
Aristotle.  Bacteria  of  many  types — cocci,  bacilli,  pseudomonas,  vibrios — 
similarly  luminesce. ^  Micro-organisms  are  also  the  source  of  the  luminescence 
of  many  molluscs  and  fishes,  sometimes  saprophytic  on  the  surface  of  the 
animal,  sometimes  parasitic  within  it.  In  the  squid.  Loligo,  for  example, 
luminous  bacteria  are  retained  within  open  organs  and  in  some  shallow-water 
fishes  similar  symbiotic  bacteria  flourish  in  a  palisade  of  tubules  in  special 
organs  in  the  cheeks  or  lower  jaw.    In  contradistinction  to  the  luminescence 

1  Some  green  plants,  mosses,  for  example,  which  live  in  dark  caves,  appetir  to  luminesce, 
but  the  light  is  due  to  total  internal  reflection  from  spherical  cells. 

2  For  review,  see  Wassink  (1948)  who  listed  65  species  of  luminous  fimgi. 
^  For  reviews,  see  Molisch  (1912),  Johnson  (1947). 

S.O.  — vol,.  T.  ^"^ 


738  THE   EYE   IN   EVOLUTION 

of  animals  which  is  excited  only  on  stimulation,  as  a  rule  a  bacterial  or  fungal 
glow  is  continuous  both  by  night  and  day  so  long  as  a  supply  of  oxygen  is 
available ;  but  in  Photoblepharoii,  a  littoral  fish  from  the  Banda  Sea,  the 
luminous  organ  can  be  covered  at  will  with  an  opaque  shield,  while  in 
another  East  Indian  fish,  Anomalojys,  it  can  be  everted  or  withdrawn  into  a 
pouch  beneath  the  eye  where  it  is  hidden  from  view  so  that  the  illusion  of 
intermittency  is  given  (Figs.  884  and  885)  (Hein,  1913  ;  Harvey,  1940)  ;  as 
these  fish  swim  in  large  shoals  they  flash  their  lights  at  rhythmic  intervals, 
using  them  probably  as  a  social  signal.  Again,  infection  of  the  Amphipod, 
Talitrus,  sand-fleas,  squids  and  other  organisms,  with  luminous  bacteria 


Fig.  886. — Quatrefages's  famous  Figure  of  Noctiluca. 

Showing  the  u'l-egular  distribution  of  luminescence  and  the  points  of  light  coming 
from  granules  in  the  protoplasm  (E.  N.  Harvey's  Bioluminescence,  Academic  Press). 

makes  their  bodies  glow  ;  while  the  pale  luminescence  of  decaying  fish  or 
meat  is  due  to  harmless  organisms  such  as  Microspira  photogenica,  Pseudo- 
monas  lucifera,  or  Micrococcus  phosphoreus .  It  is  this  which  causes  the  pale 
glow  of  meat  hanging  in  refrigerators  or  sometimes  of  dead  bodies  in  the 
dissecting  room  at  night  ;  such  a  glow  used  to  be  a  welcome  sign  in  a  pre- 
Listerian  surgical  ward  for  these  organisms  were  non-suppurative. 

Protozoa,  however,  are  the  most  abundant  source  of  this  form  of  light, 
for  to  them  is  largely  due  the  "  phosphorescence  "  of  the  sea.  Much  of  this 
is  derived  from  the  vast  blankets  of  Radiolarians  and  Dinoflagellates,  and 
particularly  the  dinoflagellate,  Noctiluca  yniliaris}  which  make  up  a  large 
proportion  of  the  planktonic  fauna,  particularly  as  they  swarm  in  early 
summer  and  multiply  prodigiously  in  the  autumn.  These  marine  organisms 
do  not  emit  light  unless  at  night  and  until  the  water  in  which  they  float  is 
disturbed,  but  in  the  darkness  a  broken  surface  glows  with  sheets  of  cold 
fire  and  every  wave -crest  is  aflame,  while  the  tracks  of  the  schools  of  fish 
become  streaks  of  molten  metal  (Fig.  886).  "It  is  impossible  to  behold 
this  .  .  .  wonderful  and  most  beautiful  appearance  ...  as  if  [the  waters] 

1  The  luminescence  of  Noctiluca  formed  the  subject   of  the  early   classical  paper  by 
Quatrefages  (1850)  and  was  extensively  studied  by  Pratje  (1921).     See  sketch,  p.  179. 


LUMINOUS   ORGANS 


739 


Figs.  887  and  888. — Panceri's  Representation  of  a  Comb -Jelly. 


Fig.  887, 


Fig.   888. 


^       Fig.    887    bj'   clay  ;     Fig.    888   by   night    (E.    X.    Harvey's    Living   Light,   Princeton 

University  Press). 

were  melted  and  consumed  by  heat,""  wrote  Charles  Darwin  of  the  '"  burning 
of  the  sea  "  as  he  sailed  in  the  Beagle  off  the  coast  of  Brazil,  "  without 
being  reminded  of  ]\Iilton"s  description  of  the  regions  of  Chaos  and  Anarchy." 
Among  the  higher  animals,  numerous  Coelenterates  show  this  activity — 
many  hydroid  polyps  and  jellyfisli  (particularly  Pelagia  noctUuca  which 
forms  a  striking  object  in  the  Mediterranean  at  night)  and  possibly  all  the 
delicate  freely-swimming  Ctenophores  (comb-jellies),  luminescing  usually 
over  their  entire  surface  when  stimulated  (Figs.  887-8).  The  brittle-stars 
(Ophiuroiclea)  contain  the  only  luminescent  representative  of  the  Echino- 
derms.  Among  worms,  luminescence  is  restricted  to  some  species  of  terres- 
trial Oligochsetes  and  marine  Polychsetes  when  they  are  irritated,  while 
only  one  nemertean  worm  {Empledonema  kandai)  has  been  described  which 
luminesces  when  it  is  touched  or  stretched  (Kanda,  1939).  The  marine 
worm,  Chcetopterus,  which  lies  in  a  tube  buried  in  the  sand,  forms  a  very 
striking  picture  indeed  (compare  Fig.  896). 


Figs.   889  and   890. — The  Beetle,   Phesgodes 


Fig.   889. 


Fig.  890. 


Fig. 


889  the  beetle  by  day  ;    Fig.   890  the  beetle  photograpliecl  in  its  own  light 
(E.  X.  Harvey's  Living  Light). 


740  THE   EYE   IN   EVOLUTION 

The  Arthropods  contain  many  luminous  species,  most  of  them  Crus- 
taceans and  Insects,  a  few  of  them  Myriapods  and  Arachnids.  Luminescence 
among  Crustaceans  is  seen  at  its  best  in  Copepods  and  Ostracods  while  the 
brilliantly  luminous  shrimps,  Meganyctiphanes,  as  they  rise  in  immense 
shoals  with  the  cold  currents  from  the  depths  of  the  sea,  glitter  with 
millions  of  pin-points  of  light  as  they  surface  over  a  wide  area.  Several  species 
of  deep-sea  Crustaceans  have  luminous  organs,  one  of  peculiar  interest 
appearing  anatomically  as  a  segment  of  a  composite  compound  eye  {Stylo- 
cheiron  mastigophoruvn — Chun,  1896).i  Only  in  a  few  orders  of  Insects  are 
luminescent  types  found  such  as  the  Collembola  (springtails),  the  Hemiptera 
(lantern  flies)  and  the  Diptera  (fungus-gnat  larvae),  but  the  most  striking 
examples  are  found  among  the  beetles  (Coleoptera)  particularly  the  Lampy- 
rids  and  Elaterids  {Lampyris  noctiluca,  Photinus pyralis,  etc.)  (Figs.  889-90)  ; 


Fig.  891. — LrcoTECTHit!  diadema  as  it  might  look  in  the  Deep  Sea  (after 
Dahlgren,  from  a  drawing  by  Bruce  Horsfall ;  E.  N.  Harvey's  Biolutninescence, 
Academic  Press). 

the  fascination  of  the  signalling  of  the  winged  male  fire-fly  (or  more  correctly 
fire-beetle)  to  his  wingless  mate,  the  glow-worm,  or  the  beauty  of  the 
rhythmic  synchronous  flashing  of  a  cloud  of  fire-flies  in  a  tropical  evening 
has  long  attracted  attention  (Buck  1937-47)  (Figs.  893  and  894). 2 

Several  Molluscs  are  luminescent,  some  such  as  the  bivalve,  PJiolas, 
having  glandular  organs  in  the  siphon  which  secrete  a  luminous  slime,  while  in 
others  such  as  the  nudibranch,  Phyllirrhoe  (the  "flowing  leaf"  of  the 
Mediterranean  and  Atlantic),  they  are  distributed  over  the  whole  body 
(Trojan,  1910).  The  most  conspicuous  examples,  however,  are  found  among 
Cephalopods,^  about  half  the  species  of  which  emit  light.  So  elaborate  may 
the  mechanism  in  these  creatures  become  that  up  to  four  different  colours  of 
light  are  produced  by  the  highly  specialized  luminous  organs  in  certain 
deep-sea  squids  in  the  Pacific  Ocean  (the  "  wonder  lamp  "  Lycoteuthis — 
Okada  et  al,  1933  ;   Takagi,  1933)  (Fig.  891). 

Among  the  Protochordates,  some  species  of  Hemichordates  luminesce 
such  as  the  balanoglossid,  Ptychodera  (Crozier,  1920),  as  well  as  certain 
colonial  Tunicates  such  as  the  beautiful  Pyrosoma:  a  whole  colony  of 
the    latter  with  its  numerous  individuals  swims   as  one  creature  and  if 

1  p.  160.  2  p_  58^ 

^  For  review,  see  Berry  (1920). 


LUMINOUS   ORGANS  741 

irritated  exhibits  a  wave  of  photogenic  activity  which  merits  the  popular 
name  "phosphorescent  fire -flame  "  (Polimanti,  1911).  Among  Fishes, 
there  are  many  kiminous  examples,  both  Selachians  and  Teleosts,  most 
of  AA'hich  inhabit  the  deep  sea  or  the  ocean  bed  ;  it  is  interesting  that 
luminous  organs  are  unknown  among  cave-fishes  or  fresh-water  fish.^  Some 
shallow-water  fishes  luminesce  but  it  is  in  the  darkness  of  the  bathypelagic 
and  the  absolute  night  of  the  benthonic  zones  that  bioluminescence  has 
reached  the  zenith  of  its  development.  Here,  far  beneath  the  level  of 
the  plankton,  the  luminous  organs  of  the  molluscs  and  fishes  are  the  only 
source  of  light,  and  Beebe  (1934)  has  computed  that  two-thirds  of  bathy- 
pelagic species  of  fish  including  96-5%  of  all  individuals  are  luminous. 
Indeed,  to  catch  these  pale  gleams  of  light  would  seem  to  be  the  only  reason 


Fig.   892. — The  Hatchet  Fish,  AeGyRop£LEcr.<.  (reproduced  from  Dahlgren,  from  a 
drawing  by  Brure  Horsfall  ;   E.  X.  Harvej-'s  Living  Light). 

for  the  development  of  the  enormous  eyes  which  characterize  some  of  these 
inhabitants  of  the  great  depths."  Curiously,  in  bathypelagic  molluscs  and 
fishes  the  vast  majority  of  these  lights  are  directed  dowaiwards ;  some, 
differing  between  the  two  sexes,  point  horizontally  and  are  obviously  sexual 
recognition  marks,  but  luminous  organs  situated  dorsally  are  invariably 
minute  or  degenerate  (Hubbs,  1938)  (Figs.  892  and  895). 

The  biological  purpose  of  bioluminescence  is  sometimes  clear,  but  often 
obscure.  It  would  seem  that  the  light  is  never  employed  as  a  search-light 
whereby  to  see.  but  always  as  a  signal-lantern  as  a  lure,  a  label  or  a  means  of 
dazzling  ;  for  the  most  j)art  they  are  social  or  sexual  signals.  Luminous 
organs  of  great  complexity  thus  occur  in  dee^J-sea  fishes  in  which  the  eyes  are 
degenerate  or  even  absent  (c.(/.,  Ijmojjs^).  Their  sexual  value  as  an  aid  to 
courtship  is  the  most  securely  proven. 

Two  examples  will  make  this  matter  clear.  The  female  fire-wormi  of  Bermuda 
[Odontosyllis)  at  mating  time  seeks  the  surface  of  the  sea  where  she  circles  luminescing 
brilliantly  for  10  to  20  seconds  ;    the  male  swimming  in  the  deeper  water  makes  for 

1  The  onlv  fresh-water  luminescent  animal  described  is  an  acjuatic  glow-worm. 

2  p.  322.  ^  3  p.  724. 


742 


THE   EYE   IN   EVOLUTION 


her  ;  if  she  stops  emitting  light  he  wanders  off  aimlessly  but  if  he  reaches  her  in  time 
the  two  join  together  in  the  "  mating  dance,"  scattering  sj^erm  and  eggs  in  a  lunninous 
spiral  in  the  water  (Galloway  and  Welch,  1911).  The  mating  of  the  fire-fly,  Photinus, 
is  equally  pretty.  The  male  fire-fly  dances  in  the  air  in  the  evening  intermittently 
flashing  a  light  ;  in  the  grass  the  female  glow-worm  responds  by  an  answering  flash 
exactly  two  seconds  later,  turning  her  abdomen  with  its  luminous  organs  towards 
him  (Figs.  893-4),  and  immediately  the  male  flies  directly  towards  his  mate.^  Within 
a  species  the  timing  of  the  answering  flash  is  the  important  recognition  signal  and  the 
eager  male  can  be  tricked  by  a  flash-light  on  the  ground  provided  the  proper  interval 
is  maintained  (Buck,  1937). 

Luminous  flashes  also  serve  as  social  signals,  particularly  among  schools 
of  fishes  ;  while  a  protective  function  is  equally  well  established.    They  may 

Figs.  893  and   894. — The  Luminous  Organs  of  Lampyris  ><plesdidula 


Fig.  893.— The  ventral  surface  of  the 
female  glow-worm.  There  are  paired 
lateral  luminous  organs  on  segments 
2  to  6,  a  small  median  organ  on  seg- 
ment 3,  paired  median  organs  on  6,  and 
a  large  unpaired  organ  on  segment  7. 


t 


Fig.  894. — The  ventral  surface  of  the 
male  fire-flJ^  There  are  only  2  median 
luminous  organs  on  segments  5  to  6 
(after  Bongardt). 


scare  a  predator  or  even  serve  as  a  warning  to  other  members  of  the  species, 
while  they  act  as  a  means  of  concealment  by  dazzling  an  enemy.  Thus, 
when  attacked,  the  bathypelagic  shrimp,  Acanthe])hyra,  ejects  from  gland- 
like luminous  organs  a  luminescent  cloud  in  which  it  escapes  (Harvey,  1931) 
(Fig.  895)  ;  two  deep-sea  prawns  found  in  the  Indian  Ocean  emit  a  substance 
of  the  same  nature  from  their  antennary  glands  (Alcock,  1902)  ;  while  the 
deep-sea  squid,  Heteroteuthis,  ejects  a  similar  cloud,  the  counterpart  of  the 
black  ink  of  its  shallow- water  relative.  A  deep-sea  fish,  Malacocephalus 
Icevis,  uses  a  gland  near  the  anus  in  the  same  way  (Hickling,  1925-26).  A 
peculiar  sacrificial  protection  is  suggested  by  the  behaviour  of  the  scale- 
worm,  Acholoe  ;    if  it  is  cut  in  two  by  a  predator,  the  posterior  portion 

1  p.  58 


LUMINOUS   ORGANS 


743 


Fig.   895. — Battle  at  Sea. 

A  deep-sea  shrimp,  Acanthephijra  purpurea,  secreting  from  its  luminous  gland 
to  blind  its  foe  during  a  battle  with  the  fish,  Photostomias  guernei.  Note  the  luminous 
organs  behind  the  eye  and  on  the  vent ro- lateral  surface  of  the  latter  (reproduced  by 
special  permission  from  the  Xational  Geographic  Society,  after  a  painting  by 
E.  J.  Geske). 


luminesces  brightly,  presumably  to  attract  attention,  ^^hile  in  the  vital 
anterior  part  luminescence  is  inhibited,  perhaps  in  order  to  aid  in  its  escape 
in  the  dark  (Fig.  896). 

For  other  functions  such  as  the  luring  of  prey,  there  is  little  convincing  evidence, 
and,  indeed,  it  would  seem  that  in  inany  instances,  for  example  in  the  luminescence 
of  fungi  or  bacteria  or  in  many  lower  forms,  the  function  can  have  little  survival  value. 
It  may  be  that  in  those  cases  the  light  is  emitted  incidentally  as  a  by-product  of 
oxidative  metabolism,  a  potentiality  which  has  been  seized  upon  for  constructive 
purposes  by  certain  of  the  higher  species. 


744 


THE   EYE   IN   EVOLUTION 


The  Biological  Mechanism  of  Bioluminescence 

We  have  already  noted  the  exploitation  of  the  adventitious  hght 
produced  by  luminous  bacteria  which  occurs  in  certain  molluscs,  crustaceans 
and  fishes  ;    these  may  be  either  symbiotic  or  parasitic  in  habit.^     Apart 


Fig.  896. — Scale-worm  Attacked  by  a  Crab. 

The  rear  half,  used  as  a  sacrificial  lure,  is  brightly  luminescent  to  attract  the 
attention  of  the  crab,  while  the  front  portion  ceases  to  luminesce  and  crawls  away 
in  the  shadow  to  reproduce  a  new  tail  (reproduced  from  Dahlgren,  from  a  drawing  by 
Bruce  Horsfall  ;    E.  N.  Harvey's  Living  Light). 

from  these,  animals  produce  biohuninescence  in  one  of  two  ways — 
either  extracellularly  or  intracellularly.  In  unicellular  organisms  light- 
producing  granules  are  scattered  throughout  the  cytoplasm,  particularly 
near  the  periphery,  and  on  stimulation  a  glow  passes  like  a  wave  through- 
out the  cell  (Quatrefages,  1850  ;   Pratje,  1921).     In  multicellular  animals, 


UA^^^V^UJti^^^j^4^iiiiii 


Fig.   897. — Section  of  the  Aboral  Umbrella  Surface  of  Pelauia  .\oviiluca. 

Showing  luminous  cells,  I,  mucous  cells,  m,  and  cells  with  contents  discharged,  d 
(modified  from  Dahlgren) 

1  p.  737. 


LUMINOUS   ORGANS  745 

however,  special  luminous  organs  are  evolved  for  the  production  of  the 
photogenic  materials. 

In  extracellular  biohiminescence,  gland-like  organs  on  the  surface  of  the 
body  secrete  a  photogenic  material  which  becomes  luminous  on  contact  with 
the  oxygen  of  the  air  or  the  sea-water.  Such  glands  may  be  unicellular  or 
multicellular.  This  mechanism  accounts  for  the  luminescence  of  Coelente- 
rates  ;  in  the  jellylish.  Pelagia  nociihica,  for  example,  single  gland-like  cells 
lie  in  the  epidermis  and  stimulation,  as  by  touching  the  animal,  during  the 
evening  but  not  during  the  daylight  hours,  produces  the  secretion  of  a 
luminous  mucus  which  spreads  like  a  wave  over  it  and  can  be  rubbed  away 


Fig.    S!t8. — Section    of   the    Light   Organ   in   the    Esca    of   the   Anoi.er-fish, 

Sliowing  luminous  eiiithelium.  L  ;  roflector  layer,  R  ;  ])iginent  layer,  P  ;  and  the 
0]iening  of  the  lumen  into  a  second  cavity  which  commiuiicates  with  the  outside,  O 
(after  Brauer  ;    E.  X.  Harve\'"s  Biohiminescence ,  Academic  Press). 


with  the  finger  (Dahlgren.  1915-17  ;  Parker,  1920  ;  Harvey,  1921  ;  Moore, 
1926)  (Fig.  897).  Such  a  spread  indicates  transmission  of  the  stimulus  by 
a  nerve-net  ;  the  process  is  inhibited  in  the  absence  of  Ca  or  K,  and  irri- 
tability is  markedly  increased  in  the  absence  of  Mg  (Heymans  and  Moore, 
1924).  A  somewhat  similar  luminous  slime  is  produced  by  many  worms  ;  in 
the  luminous  earthworm  it  emerges  from  the  mouth  or  anus  or  from  dorsal 
pores  (Gates.  1925  ;  Komarek,  1934),  and  in  Polycha^tes  the  photogenic  cells 
are  situated  in  association  with  mucous  cells  in  the  hypodermis  {Chcefopferus 
— Dahlgren,  1916)  or  in  specific  locations  {e.g.,  in  specialized  nephridial 
funnels  in  the  transparent  marine  worm.  Tomopteris — Meyer,  1929).  Again, 
a  wave  of  light-production  from  the  point  of  excitation  indicates  a  spread 
by  nervous  means.  A  similar  slime  is  secreted  by  the  clam,  Pholas,  luminous 
Myriapods,  and  the  colonial  ascidian,  Pyrosoma.  CJlandular  organs  of  a 
more  complex  tyj^e  are  seen  in  Crustaceans  in  which  granules  are  secreted 


746 


THE   EYE   IN   EVOLUTION 


and  when  ejected  into  the  sea-water,  appear  as  a  luminous  cloud  (Fig.  895). 
In  Copepods  the  photogenic  cells  are  in  small  groups;  in  the  Ostracod, 
Cypridina,  there  is  a  complex  gland  of  4  types  of  cell  near  the  mouth  from 
which  granules  are  ejected  by  muscular  action  (Okada,  1926  ;  Takagi,  1936)  ; 
a  similar  mechanism  is  found  in  the  deep-sea  shrimps  and  squids  (Harvey, 
1931).  In  these  the  operative  mechanism  is  neuro-muscular.  Finally,  in 
some  bathypelagic  fishes  such  as  Malacocephalus  or  Gigantactis,  similar 
luminescent  granules  (which  may  be  bacterial)  are  expelled  on  the  ventral 
surface  of  the  body  from  sac-like  organs  when  the  fish  is  excited  (Fig.  898). 


The  intracellular  production  of  bioluminescence  is  more  widespread,  and, 
again,  may  be  effected  either  by  single  cells  or  elaborate  organs  equipped 

with  secretory  cells,  a  lens  and  cornea, 
light-absorbing  and  light -reflecting  struc- 
tures, the  whole  resembling  in  many  ways 
a  well-formed  eye.  Such  organs  are  called 
PHOTOPHORES.  The  luminous  brittle-stars 
and  the  nemertean  worm,  Emplect enema, 
have  single  light-producing  cells  scattered 
over  their  entire  surface  (Kanda,  1939). 
The  Arthropods,  however,  show  more 
specialized  photophores  as  are  seen  parti- 
cularly in  shrimps,  consisting  of  large 
granular  light -producing  cells  lying  under- 
neath an  epithelial  lens  and  upon  a 
reflecting  layer  (Fig.  899)  (Vallentin  and 
Cunningham,  1888  ;  Terao,  1917).  Organs 
of  a  somewhat  similar  type,  consisting  of 
photogenic  cells,  a  lens  and  a  reflector 
surrounded  by  pigment,  frequently  occur  in  Molluscs,  and  also  in  many 
deep-sea  Fishes  arranged  along  the  ventro -lateral  aspect  of  the  body. 
The  photophores  of  Insects  are  equally  elaborate.  In  the  fire-fly, 
Lampyris,  for  example,  the  luminous  organ  is  situated  ventrally  in  the 
posterior  part  of  the  abdomen  ;  it  consists  of  a  layer  of  light -producing  cells 
lying  under  the  surface  epithelium,  backed  by  a  layer  of  light -reflecting  cells 
which  owe  their  optical  property  to  small  particles  of  urates,  while  an 
abundance  of  oxygen  is  provided  by  a  rich  supply  of  tracheae  (air  tubes) 
equipped  with  end-cells  which  act  as  minute  pumps  or  valves  (Fig.  900) 
(Hess,  1922).  All  these  photophores  are  well  supplied  with  nerves  and 
apjoear  to  be  under  nervous  control  except  in  some  fishes  ;  studying  the 
luminous  organs  of  the  Californian  stinging  fish,  Porichthys,  Greene  and 
Greene  (1924)  failed  to  find  any  nerves  and  demonstrated  that  they  were 
under  hormonal  control,  the  whole  animal  remaining  alight  and  glowing  for 
over  an  hour  after  a  subcutaneous  injection  of  adrenalin.     It  is  noteworthy, 


Fig.  899. — Section  of  a  Photophore 
OF  THE  Decapod  Hkrimf,  Se rue f<Tjiti 

PREHEySILIX, 

Showing  the  leri.s  layers,  Lj  to  L,  ; 
photogenic  cells,  Ph  ;  reflector,  K  ; 
and  pigment,  P  (after  Terao  ;  E.  N. 
Harvey's  Bioluminescence,  Academic 
Press). 


LUMINOUS   ORGANS 


747 


as  we  have  already  seen.^  that  a  central  nervous  control  is  made  manifest 
in  many  species  by  the  presence  of  a  diurnal  rhythm,  whereby  the  24-hour 
phase  of  luminescence  persists  even  if  the  animal  is  kept  in  continuous 
darkness  for  some  time  (the  jellyfish.  Pelagia — Heymans  and  Moore,  1924  ; 
the  fire-fly,  Photinus — Buck,  1937  ;  the  balanoglossid,  Ptychodera — 
Crozier,  1920). 

The  Chemical  Mechanism  of  Bioluminescence 

Despite  the  expenditure  of  much  study  and  speculation  since  the  time 
of  Aristotle,  the  intimate  chemical  nature  of  bioluminescence  is  not  yet 


N 
7"  C  -   , 

ECN    -- 
H  - 


Fig.  900. — Cross-section  of  the  Light  Organ  of  .an  Insect. 
The  light  organ  of  the  adult  Photurus  pennsylvanica.     C,  cuticle  ;    ECX,  nucleus 
of  tracheal  end-cell  ;    H.  hypodermis  ;    X,  nucleus  of  photogenic  cell  ;    P,  photogenic 
layer  ;    R,  reflector  layer  f  T,  trachea  ;    TC,  tracheole  (W.  X.  Hess,  J.  MorphoL). 


clear.  The  process  is  the  reverse  of  a  photochemical  reaction  wherein  the 
absorption  of  light  induces  chemical  activity  ;  here  the  energy  derived  from 
a  chemical  reaction  is  converted  mto  light.  Such  a  chemical  reaction  is 
oxidative  in  nature  and  converts  a  substance  into  an  activated  state  in 
which  it  can  emit  light  as  it  lapses  again  into  the  non-activated  state.  The 
occurrence  of  chemiluminescence  in  the  inanimate  world  has  long  been 
known  ;  it  is  shoA\ii.  for  example,  by  phosphorus  -  and  a  multitude  of  organic 

1  p.  21. 

2  PHOSPHORESCENCE,  properly  defined,  is  a  delayed  fluorescence,  fluorescence  occurs 
when  a  substance,  on  radiation,  emits  light  of  a  waye-length  differing  from  the  incident  light. 
The  incident  light  is  absorbed  by  molecules  which  are  thereby  changed  into  an  actiyated  form  ; 
these  return  to  their  original  state  giying  off  energy  as  they  do  so  ;  this  energy,  being  absorbed 
by  other  molecules  capable  of  radiation,  is  emitted  as  fluorescent  light.  By  delaying  the  energy 
transfer,  the  emission  of  light  occurs  sometime  after  exposure  as  phosphorescence.  The 
commercial  sulphides  of  Ca,  Ba  and  Sr  possess  the  property  of  phosphorescence  and  are  used 
in  luminous  paints. 


748  THE   EYE   IN   EVOLUTION 

compounds  in  solution.  That  bioluminescence  is  also  a  simple  chemical 
reaction  not  associated  with  the  metabolic  integrity  of  living  cells  has  also 
been  appreciated  for  a  long  time,  for  on  desiccation  of  the  cells  or  their 
products,  luminescence  ceases  but  recommences  on  the  addition  of  water  in 
the  presence  of  oxygen.  The  role  of  the  cells  is  to  produce  and  store  the 
reacting  substances  and  bring  them  together  at  the  appropriate  time. 
Luminous  cells  are  always  granular  and  their  production  of  light  is  associated 
with  the  dissolution  of  the  granules,  either  on  their  extrusion  into  sea-water 
or  on  the  complete  breakdown  of  the  organization  of  the  cell  in  the  act  of 
secretion  (Hickling,  1925-26). 

For  Kiminescence  to  occur,  water  is  always  necessary,  and  in  most  cases  oxygen 
either  in  the  air  or  dissolved  in  water,  a  fact  first  discovered  by  the  great  English 
natural  philosopher,  Robert  Boyle  (1667).^  Sometimes,  as  in  the  case  of  certain 
radiolarian  Protozoa  and  some  Coelentefates  such  as  the  jellyfish,  Pelagia,  and  the 
comb-jelly,  Mnemiopsis,  luminescence  occurs  in  the  absence  of  free  oxygen  :  the  fact 
that  Harvey  and  Korr  (1938)  found  that  the  extract  of  the  last  organism  became 
luminous  in  the  presence  of  nascent  hydrogen  suggests  that  in  such  cases  bound  O^  is 
made  available  by  the  appropriate  stimulus. 

It  was  first  shown  by  Dubois  (1885-87),  studying  the  luminescence  of 
the  beetle,  Pyroi)horus,  and  the  clam,  Pholas,  that  the  reaction  involved 
two  substances,  the  one,  luciferase,  a  heat-labile,  non-dialysable,  protein- 
like substance  with  the  characteristics  of  an  enzyme,  the  other,  luciferin, 
a  readily  oxidizable,  diffusible  substance  of  low  molecular  weight  and 
undetermined  chemical  composition. ^  These  two  substances  have  beeii 
identified  in  some  polychsete  worms,  crustaceans  and  beetles,  and  although 
they  are  apparently  absent  in  most  luminous  species,  it  has  been  assumed 
that  a  system  resembling  luciferase-luciferin  is  the  basis  of  most  reactions. 
Luciferin  is  readily  oxidized  in  many  ways  but  luminescence  appears  only 
when  the  reaction  is  catalyzed  by  luciferase.  It  used  to  be  generally 
accepted  that  in  the  reaction  the  light  was  emitted  by  molecules  of  activated 
luciferase  (Harvey,  1917),  but  further  study  has  shown  that  the  matter  is 
probably  not  so  simple.  CJlucose  and  phosphates  appear  to  be  important  in 
the  reaction,  suggesting  a  relation  with  the  carbohydrate  metabolism 
(McElroy  and  Ballentine,  1944),  but  the  intimate  nature  of  the  process, 
whether  the  emitting  molecule  is  luciferase  or  luciferin  or  even  another 
unidentified  substance,  or  how  far  the  reactions  occurring  in  different 
species  are  alike,  are  all  matters  which  must  await  further  research  (see 
Chance  et  al,  1940  ;    Chase,  1940  ;    Harvey,  1940  ;    Kluyver  et  al.,  1942  ; 

1  New  Experiments  Physico-mechanical  touching  the  Spring  of  Air  and  its  Effects,  London, 
1660-82. 

2  Anderson  (193.3-36),  who  first  purified  luciferin,  considered  it  a  polyhydroxy  benzene 
derivative;  Chakravorty  and  Ballentine  (1941)  identified  a  ketohydroxy  side-chain  and  a 
hydroquinone  ring  ;  and  Eymers  and  van  Schoxiwenburg  (1936)  suggested  a  derivation  from 
flavine.  Using  chromatography,  however,  McElroy  and  Strehler  (1949)  found  that  the  com- 
pound generally  described  as  luciferin  had  at  least  three  constituents — a  bivalent  metallic  ion 
(Mg,  Mn,  Co),  adenosine  trijihosphate,  and  a  further  iniidentified  compound. 


LUMINOUS   ORGANS 


749 


McElroy  and  his  co-workers,  1944-51  ;  Johnson  et  al.,  1945  ;  and  others). 
Nor  is  it  known  how  the  reaction  in  vivo  is  inhibited  by  hght,  particularly 
short -waved  light,  whether  by  a  destruction  of  the  photogenic  precursors  or 
an  inhibition  through  the  controlling  nervous  (or  hormonal)  mechanism 
(Harvey,  1925  ;   Heymans  and  Moore,  1925). 

The  nature  of  the  hght  involved  in  biokiminescence  varies  with  different  species 
and  even  in  the  same  animal.  In  intensity  it  is  relatively  low  ;  in  the  fire-fly,  Photinus, 
for  example,  it  is  the  equivalent  of  from  0-0025  to  0-02  candles  (Coblenlz,  1912).  In 
colour  it  varies  from  blue  to  red,  usually  extending  over  a  considerable  range  and 
showing  a  continuous  spectrum  ;  but  ultra-violet  is  never  present  and  it  is  "  cold  "'  in 
the  sense  that  infra-red  is  also  absent  (Harvey,  1920  ;    Buck,  1941). 

The  large  bibliography,  particularly  of  the  biochemical  problems  involved,  will  be 
found  in  E.  N.  Harvey  (1920,  1940,  1952),  F.  A.  Brown  in  Prosser's  Comparative 
Animal  Physiology,  London,  p.  660  (1950),  and  H.  Davson's  Textbook  of  General 
Physiology,  London,  p.  600  (1951). 


Aleock.     A  Natural ist  in  Indian  Seas  (1902). 
Anderson.      J.    cell.    camp.    Physiol.,    3,    ■!.") 

(1933)  ;    8,  261  (1936). 
Beebe.     Zoologica  (X.Y.).  16,  149  (1934). 
Berry.     Biol.  Bull..  38,  141  (1920). 
Buck.     Physiol.  Zool..  10,  4.5.  412  (1937). 
Quart.  Rev.  Biol.,  13,  3(il  (1938). 
Proc.  Rochester  Acad.  Sci.,  8,  14  (1941). 
Ann.  N.Y.  Acad.  Sci.,  49,  397  (1947). 
Chakravorty  and  Ballentine.    J.  Amer.  cheni. 

Soc,  63,  2030  (1941). 
Chance,   Harvey,  Johnson  and  Millikan.     J. 

cell.  comp.''Phijsiol.,  15,  19.5  (1940). 
Chase.  J.  cell.  comp.  Ph>/.siol.,  15,  1.59  (1940); 

31,  175  (1948);  33,  113  (1949). 
Chun.  Bibl.  Zool.,  19,  193  (1896). 
Coblentz.      Publ.   Carnegie   Inst.    Wa.sh.,   No. 

164,  3  (1912). 
Crozier.    Anat.  Rec,  20,  186  (1920). 
Dahlgi-en.     J.   Franklin   Inst..  180,  513,   711 
(1915)  ;   181,  109,  243,  377,  525,  658,  805 
(1916);     183,    79,    211,    323,    593,    735 
(1917). 
Dubois.      C.    R.   Soc.    Biol.    (Paris),   37,    559 

(1885)  ;    39,  564  (1887). 
Eyniers  and  van  Schoiuvenbiu'g.    Enzyntoloyy, 

1,  107  (1936). 
Fabre.     Ann.  Sci.  )iat.,  4,  179  (1855). 
Galloway  and  Welch.   Trans.  Anier.  micr.  Soc, 

30,  13  (1911). 
Gates.     Rec.  Ind.  Mus.,  27,  471  (1925). 
Greene  and  Greene.     Anier.  J.   Physiol.,  70, 

500  (1924). 
Harvey.    Science,  46,  241  (1917). 

The  Xature  of  Aniinrd  Light,  Pliila.  (1920). 
Biol.  Bull..  4l,  28U  (1921)  ;  51,  89  (1926). 
J.    gen.    Physiol.,   4,    285    (1922)  ;     7,    679 

(1925). 
Amer.  J.  Physiol.,  77,  548  (1926). 
J.  biol.  Chem.,  78,  369  (1928). 
Zoologica  (N.Y.),  12,  70  (1931). 


Harvey.      Living  Light,  Princeton  (1940). 

Bioluminescencc.  X.Y.  (1952). 
Harvey  and  Korr.    J.  cell.  comp.  Physiol.,  12, 

319  (1938). 
Hein.  T.     ned.     Dierk.     Vereen,     12,     238 

(1913). 
Hess,  W.  N.    J.  Morphol..  36,  245  (1922). 
Heymans  and  Moore.    J.  gen.  Pliysiol.,  6,  273 

(1924)  ;    7,  345  (1925). 

Hickling.     J.   marine    Biol.    Assoc,    13,    914 

(1925)  ;    14,  495  (1926). 

Hubbs.    Ptibl.  Car)ieyie  Inst.   Wash.,  Xo.  491, 

261  (1938). 
Johnson.     Advanc.  Enzyniol.,  7,  215  (1947). 
Johnson,    Eyring,    Steblay,    Chaplin,    Huber 

and  Gerhardi.     J.  gen.  Physiol.,  28,  463 

(1945). 
Kanda.     Biol.  Bull.,  77,  166  (1939). 
Kluyver,  v.d.  Kerk,  v.d.  Burg,  G.,  and  v.d. 

Burg,  A.     Proc.  kon.  Akad.  Wet.,  45,  886 

962  (1942). 
Komarek.     Bull.  int.  Acad.  Sci.  Bohetne,  44, 

1  (1934). 
McElroy  and  Ballentine.    Proc.  )iat.  Acad.  Sci., 

30,"  377  (1944). 
McElrov  and  Harvey.    J.  cell.  comp.  Pliysiol., 

37,"  1  (1951). 
McElroy  and  Strehler.     Arch.   Biocheni.,  22, 

420  (1949). 
Meyer.     Zool.  Anz.,  86,  124  (1929). 
Molisch.     Leuchtende  Pflanzen,  Jena  (1912). 
Moore.    Amer.  J.  Physiol.,  76,  112  (1926). 

J.  gen  Physiol.,  9,  375  (1926). 
Okada.       Bull.    Soc.    zool.     France,    51,    478 

(1926-27). 
Okada,  Takagi  and  Sugino.    Proc.  Imp.  Acad., 

Tokyo,  10,  431  (1933). 
Parker.    J.  e.rp.  Zool.,  31,  475  (1920). 
Polimanti.     Z.  Biol.,  55,  505  (1911). 


750  THE   EYE   IN  EVOLUTION 

Pratje.     Arch.  Protistenk.,  42,  1,  423  (1921).  Takagi.     Annot.  Zool.  Japan.,  15,344(1936). 

Z.  Anat.  EntwQesch.,  62,  171  (1921).  Terao.    Anjiot.  Zool.  Japan.,  9,  299  (1917). 

BJoZ   Z6Z.,  41,  433  (1921)  Trojan,     ^rc/i.  wi'cr.  ^na^,  75,  473  (1910). 

Quatrefages.     Ann.  Sci.  Nat.   Zool.,  14,  23b  ^r  u     i-  j  /-i        •     u  /-i       <     r 

^       ns'^m  Vallentin  and  Cunningham.     Quart.  J.  micr. 

Schultze.     Arch.  mikr.  Anat.,  1,  124  (1865).  ^^^-^  28,  318  (1888). 

Takagi.      Proc.   Imp.   Acad.,   Tokyo,   9,   651  Wassink.      Rec.    Trav.   botan.   neerl.,  41,    150 
(1933).  (1948). 


CHAPTER  XXII 
ELECTRIC   ORGANS 

A  GREAT  many  fishes  are  possessed  of  an  electric  organ — a  curious 
specialization  found  only  in  this  class  of  Vertebrates.  They  are  all  developed 
from  modified  muscular  tissue  formed  into  plates  arranged  in  series  ;  the 
only  exception  is  that  of  the  electric  catfish.  Malopternrus,  which  is  developed 
from  cutaneous  glands  (Garten,  1910).    When  a  muscle  contracts  the  energy 


3r 


Fig.  901. — The  Starc^zer,    A-i hn^i  ,,i  i  -. 

The  electric  organs  are  seen  as  the  flat  areas  behind  the  eyes.  The  fish  normally 
lies  biu-ied  in  the  mud  with  only  the  eyes,  mouth,  electric  plates  and  a  fin  showing, 
so  that  the  small  fish  which  swim  too  near  are  electrocuted  and  fall  straight  into  the 
ugly  open  mouth  (Alice  Jane  Mansueti,  Chesapeake  Biol.  Lab.,  Maryland,  U.S.A.  : 
from  the  lUust.  Loud.  News). 

developed  is  expended  in  motion,  heat,  and  electricity  ;  in  electric  organs 
the  electrical  properties,  in  jjlace  of  being  subsidiary,  become  predominant. 
Among  Selachians,  in  electric  rays  {Hy2marce,  Torpedo)  the  organ  is  immense, 
running  through  the  entire  thickness  of  the  body  between  the  head  and 
the  pectoral  fin  ;  in  other  rays  and  in  the  teleostean  electric  eel,  Electro- 
pJiorus,  it  is  smaller  and  situated  at  the  sides  of  the  root  of  the  tail.  In  the 
American  stargazer,  Astroscopus,  however,  the  great  rarity  is  found  of  an 
electric  organ  situated  in  the  orbit  derived  from  the  extra-ocular  muscles, 
all  of  which  with  the  exception  of  the  inferior  rectus  and  the  inferior  oblique, 
while  retaining  to  some  extent  their  original  function,  have  become  modified 


752 


THE   EYE   IN   EVOLUTION 


for  this  purpose  (White,  1918  ;  Woelfflin,  1955)  (Fig.  901).  The  electric 
organ  of  the  stargazer  assumes  a  considerable  size,  about  1/10  of  the  length 
of  the  body,  and  occupies  most  of  the  space  of  the  enlarged  orbit  so  that  the 
small  eye,  protected  by  an  unusually  thick  sclera,  is  crowded  into  its  anterior 


Fig.  902. — The  Orbit  of  the  Stargazer. 
Showing  the  electric  organ  (Bland-Sutton). 


portion  (Fig.  902)  ;  although  the  organ  is  relatively  large,  the  shock  derived 
from  it,  while  somewhat  unpleasant,  is  a  mere  tickle  compared  with  that 
of  certain  electric  fishes  which  can  knock  a  man  off  liis  feet.  The  upward- 
looking  eyes  are  situated  on  the  upper  aspect  of  the  head  just  in  front  of 
the  mouth,  and  as  small  fishes  swim  over  the  stargazer,  it  paralyses  them 
with  an  electric  shock  so  that  they  tumble  into  its  gaping  mouth  (Dahlgren 
and  Sylvester,  1906). 


Dahlgren  and  Sylvester.     Anat.  Anz.,  29,  387 

(1906). 
Garten.     Winterstein's  Hb.  d.  vergl.  PliysioL, 

3,  105(1910). 


White.      Publ.  Carnegie  Inst.,  12,  252  (1918). 
Woelfflin.     Klin.  Mbl.  Augenheilk.,  126,  348 
(1955). 


EPILOGUE 

This  is  the  story  of  the  development  of  the  eye  from  the  primitive  undiffe- 
rentiated protoplasm  of  the  simplest  protozoon  to  become  the  most  highly  efficient 
sensory  mechanism  in  the  animal  kingdom  in  the  eyes  of  Birds.  It  is  the  story 
of  the  development  of  the  sense  of  vision  from  an  automatic  response,  associated 
at  some  stage  with  a  vague  awareness,  to  the  capacity  to  he  enraptured  by  a 
sunset  or  a  rainbow  or  to  create  a  thing  of  beauty.  The  first  story  is  factual; 
the  second  specidative. 

The  subject  of  the  second  is  fraught  withdiffictdties  sogreat  as  to  make  a  fined 
solution  impossible.  In  the  physiccd  world  matericd  things  are  incomprehensible 
to  each  other  and  can  he  analysed  only  on  a  higher  level  by  the  senses;  the  sense- 
organs  know  nothing  of  each  other  for  sensations  can  he  cnialysed  only  by  percep- 
tions; we  have  no  access  to  a  platform  wherefrom  to  look  down  upon  perceptions 
and  subject  them  to  analysis.  It  follows  that  our  consciousness  is  to  us  un- 
knoivable  and  ivill  probably  remain  so — until  or  unless  we  acquire  other  and 
higher  faculties.  And  if  we,  in  our  wordy  thinking,  cannot  mutucdly 
compare  the  symbolic  representation  that  each  of  us  creates  perceptually  of  the 
outside  world,  how  much  more  difficult  to  ancdyse  what  the  animal  world  in  its 
ivordless  thinking  makes  of  it. 

A  hypothesis  might  run  like  this.  There  are  three  stages  in  the  evolution 
of  visio7i.  It  started  as  a  motor  taxis,  appearing  initicdly  in  the  simplest 
unicellular  organisms  as  an  automatic  response  which  eventually  became  more 
plastic  to  reach  its  culmination  in  the  homing  bird;  as  such  it  need  not  enter 
consciousness.  From  this  emerged  perceptual  vision,  a  pragmatic  sense, 
essentially  a  passive  registration  of  objects  in  the  outside  world,  serving  priynarily 
the  biological  needs  of  hunger,  fear  or  sex.  Initially  a  minor,  it  eventually 
became  a  major  determinant  of  conduct.  Dependent  on  a  centred  nervous 
organization  to  create  its  symbolism ,  it  started  in  worms  and  reached  its  highest 
level  in  man.  From  this  emerged  imaginative  vision  with  its  aesthetic  and 
creative  qualities,  with  its  inquisitive,  exploratory  drive,  seeing  beauty.  It 
depended  on  the  almost  explosive  develojjment  of  the  frontal  brain  in  the  highest 
Primates.  It  first  appeared,  presumably,  during  the  ape-man  s  arboreal  adven- 
ture and  certainly  is  present  in  the  chimpanzee ;  it  was  well  established  when 
modern  man  migrated  northwards  folloiving  the  melting  of  the  ice  20,000  years 
ago  to  replace  his  Neanderthal  predecessors  and  establish  the  Aurignacian  and 
Magdalenian  cave-civilizations  in  south-west  Europe,  and  reaches  its  greatest 
development,  jjerhaps,  in  the  human  mind  relieved  of  the  chemical  servitude  of 
iyihihitions,  as  by  mescalin. 

It  is  a  fascinating  story  extending  back  to  where  life  started,  a  story  mostly 
of  steady  progress,  now  in  this  direction,  now  in  that,  as  one  expedient  after 
another  ivas  tried,  this  one  to  be  discarded,  that  to  be  perfected.  It  is  a  long 
story,  and  in  this  Volume  it  can  oidy  be  sketchily  told. 

In  the  volumes  of  this  series  which  follow  we  will  discuss  in  more  detail 
the  visual  apparatus  of  man — its  structure,  its  development,  its  function,  and 
the  effects  upon  it  of  disease  and  injury. 

S.O.— VOL.  I.  753  48 


APPENDIX 


ERAS 


CENOZOIC 

(K-ati^ds'  =  recent 
Iw^  =  life) 


PERIODS  AND  SYSTEMS 

fHOLOCENE 

I  (oAo?  =  complete  ; 
QUATERNARY   i  ^aivo?  =  recent) 
j  PLEISTOCENE 

^{TrXeiarog  =  most) 

PLIOCENE 

{■n-Xeiiop  =  more) 
MIOCENE 
{fji€iOJv  =  less) 
OLIGOCENE     . 
(oAt'yo?  =  few) 
EOCENE 
(7701?  =  dawn) 

I  PAL^OCENE  . 

LTT-aAato?  =  ancient) 


TERTIARY 


MESOZOIC  {ixiao^  =  middle) 


DATES  IN 
MILLIONS  OF 
YEARS  (Approx.) 
at  beginning  of  period 


1 

12 
29 
40 
60 
75 


CRETACEOUS  .  .  .135 

[Greta  =  chalk) 

i 

^  JURASSIC         .  .  .  .175 

I  (Jura  mountains) 

I  TRIASSIC  .  .  .  .210 

1^  (Threefold  division  in  Germany) 


PALEOZOIC 

(TT-aAatd?  =  ancient)        "* 


f  PERMIAN         .  .  .  .240 

I  (Permia  =  ancient  kingdom 
I  E.  of  Volga) 
Upper  ^  CARBONIFEROUS   .  .  .290 

(Coal-bearing) 

DEVONIAN      .  .  .  .320 

(Devon's  marine  rocks) 


r  SILURIAN        .  .  .  .350 

(Silures  =  ancient  tribe 

of  Welsh  borders) 

ORDOVICIAN  .  .  .  .420 

(Ordovices  —  ancient  tribe  of 

N.  Wales) 

CAMBRIAN       .         .         .         .500 

(Cambria  =  Wales) 


Lower  < 


PRE-CAMBRIAN  ERAS 


rPROTEROZOIC 

]  {TTpoTcpos  =  earlier) 
]  ARCHEOZOIC 
[_{dpxot.lo?  =  primaeval) 


PALi^ONTOLOGICAL   TABLE 


Australopithecus  ;   Pithecanthropus  ;   Homo 


Eutherian  mammals  become  numerous  and  diverse.  Grasses  appear  in  Miocene.  Braehiopods 
diminish  in  importance  ;  lamellibranchs  abundtint.  Insects  associated  with  flowering 
plants  radiate  now. 


First  appearance  of :  urodeles,  snakes,  marsupials,  insectivores,  modern-type  flowering 
plants.  At  end  of  period  extinction  of  saurischian  and  ornithischian  dinosaurs,  pterosaurs, 
plesiosaurs,  ichthyosaurs,  ammonites. 

First  appearance  of  :  plesiosaurs,  ornithischian  dinosaurs,  pterosaurs,  birds,  anurans,  flowering 
plants.     Radiation  of  cartilaginous  and  actinopterygian  fishes. 

First  appearance  of  :  saurischian  dinosaurs,  ichthyosaurs,  chelonians,  crocodiles,  rhj^ncho- 
cephalians,  lizards,  and,  at  end  of  period,  mammals.  First  moss.  Hexacorals  and 
lamellibranchs  rise  to  prominence  in  marine  faunas.  By  end  of  period  extinction  of 
"  labyrinthodonts  "  and  cotylosaurs. 

First  appearance  of  :  true  ammonites,  holostean  fish.  Trilobites  and  rugose  corals  extinct 
at  end  of  period,  also  acanthodians.  Endopterygote  insects  appear  at  beginning  of  period. 

First  appearance  of  :  reptiles  and  conifers  (upper  Carb.).  All  arachnid  groups  have  now 
appeared  except  possibly  mites.     Foraminifera  become  abundant. 

First  appearance  of  :  placoderms.  rhipidistia.  dipnoi,  sharks,  actinopterygians,  insects, 
myriapods,  and  at  end  of  period,  coelacanths  and  amphibia.  Placoderms  except  acantho- 
dians, become  extinct  at  end  of  period,  as  do  the  bony  ostracoderms. 

First  appearance  of  :  ammonoids,  scorpions  and,  at  end  of  period,  land-plants,  4  groups 
agnathan  fish,  acanthodians.  Graptoloids  become  extinct  at  end  of  period. 

First  appearance  of  :  corals,  echinoderms  (blastoids,  crinoids,  starfish,  echinoids),  lamelli- 
branchs, ectoprocts  (polyzoa),  ostracods,  graptolites,  ostracoderms  (fragmentary), 
eurypterids. 

First  appearance  of  :  sponges  (siliceous),  ccelenterates  (medusae),  echinoderms  (c^^stids  and 
some  which  are  probably  Holothurian).  annelids,  braehiopods  (small  "  horny  '"  hingeless), 
molluscs  (gastropods,  pteropods,  nautiloids),  arthropods  (onychophora,  trilobites, 
Crustacea),  graptolites.     Algae  present. 


(Table  reproduced  by  permission  of  Miss  P.  Lamplugh  Robinson,  University  College,  London.) 

755 


ZOOLOGICAL   GLOSSARY 

The  figures  in  bold  face  indicate  the  number  of  a  page  containing  an 

illustration  in  the  text;  those  in  italics  indicate  the  number  of  a  page 

showing  a  marginal  illustration. 

Ablepharus.     Skink:   a  reptile  of  the  lizard  family. 

AcANTHEPHYKA.     Deep -sea  shr imp:    decapod  crustacean. 

ACARiNA.     An  order  of  Arachnida,  many  of  them  minute  and  parasitic  (mites,  ticks). 

AccipiTER.     Sparrow-hawk:    bird-of-prey  (Falconiformes). 

AcEREMOMo.v.     Wingless,  eyeless  insect:    Protura,  218. 

AcHiAS  ROTHScHiLDi.     Stalk-oyed  fly:    dipterous  insect,  223. 

AcHOLOE.     Scale-worm:    free-swimming  polychsete  worm. 

Acinus.     Water-beetle:    coleopterous  insect. 

AciPEXSER.     Sturgeon,  sterlet:    chondrostean  fish,  317, 

ACNIDARIA.      Sub-phylum  of  non-stinging  coelenterates,  comprising  the  ctenophora. 

AcRiDA.     Short-horn  grasshopper:    an  orthopterous  insect  (Acrididse). 

Acrobat ES.     Flying  phalanger:   marsupial. 

AciixiA.     Sea-anemone:   coelenterate  (Anthozoa). 

Aedes.     Mosquito:    dipterous  insect. 

^OA.     A  crustacean  (Isopoda). 

ASoLixA  PRincA.     Trilobite:    extinct  arthropod,  157 

^scH.\A.     Dragonfly:    insect  (Odonata),  222,  225 

AoAMA  AOAMA.     Agamid  lizard:    a  lacertilian  reptile,  359 

Agaricus  olearius.     Limiinous  fungus. 

AONATHA.     Class  of  jawless  pre-fishes  :  the  earliest  vertebrates,  represented  today  only  by  the 

Cyclostomata. 
Ah.etulla  PICT  a.     Painted  tree  snake:    a  colubrid  snake. 
AiLUROPODA  MELANOLEUCA.     Giant  panda:    carnivore  (Procyonidae). 
AiLURUs  FULGENS.     Panda:   carnivore  (Procyonidae). 
Alaurina  prolifera.     Pelagic  Rhabdoccele:    turbellarian  worm. 
Albvrnus.     Teleostean  fish  (Cyprinidse). 
A.  LVciDus.     The  bleak. 
Alcedo.     Kingfisher:    Coraciiformes,  417 
ALCiD.'E.      The  auk  family  of  birds. 
Alcwpa.     Free-swimming  polychsete  worm. 
Alligator.     Reptile,  crocodilian. 
Allolobophora.     OHgochsete  worm. 
Alouatta.     Howling  monkey:    Primate  (Cebidse). 
Alytes  obstetricaas.     Obstetric  toad:    anuran  amphibian. 
Amblyomua  pomposum.     Tick:    Acarina  (Ixodides),  217 
Amblyopsis.     American  cave-fish:   teleostean  fish. 

Amblyrhynchus  cristatus.     Marine  iguanid  lizard  of  Galapagos  Islands  :  Reptile. 
Ambysioma  tigrixum.     N.  American  terrestrial  salamander  :  vn-odelan  amphibian,  346. 
Ameiurus.     Bullhead  cat-fish:    siluroid  teleost,  307 
Amia  calva.     Bowfin  of  N.  America:   holostean  fish,  321 
AMMOCCETES.     Larva  of  lamprey  :  cyclostome,  92 
Ammomaxes.     Desert  lark:    passerine  bird. 
Ammophila.     Digger  wasp:    insect  (Hymenoptera). 
Amceba  PROTEUS.     Protozoon  (Rhizopod),  179 

Amphioxus  (Bra.s-chiostoma).     Lancelet:    a  protochordate  (Cephalochordate),  229. 
Amphiporus.     Nemertine  worm,  189 

Amphiss.e.va  punctata.     Legless  blind  subterranean  lizard:    Reptile. 
Amphitretus.     Pelagic  octopus;    oephalopod  mollusc,  203 

Amphiuma.      "  Congo  snake  "  or  blind-eel,  a  salamander:   urodelan  amphibian,  349 

756 


ZOOLOGICAL   GLOSSARY  757 

Ay  ABAS  scAyDEXs.     Climbing  perch:    an  amphibious  teleostean  fish. 

AyABLEPS  TETROPBTHALMUs.     "  Four-eyed  "  fish:    a  cyprinodont  teleostean  fish,  325 

ANATID^.     Family  of  birds,  comprising  swans,  geese,  ducks. 

AyAX.     Dragonfly:   insect  (Odonata). 

AycALA  FASciATA.     Gadfly:   dipterous  insect  (Tabanidse). 

Ayoi'iLLA.     Common  genus  of  eel:   teleostean  fish,  46 

Ayoris  fragjlis.     Slow-worm:   legless  lizard,  reptile,  363 

Ay  1  ELL  A.     Worm-lizard:   Reptile. 

ANNELIDA.     The  phylum  of  segmented  worms,  comprising  Oligochsetes,  Polychsetes,  Leeches. 

AyoDoyTA.     Eyeless  swan-mussel:  fresh-water  bivalve  mollusc,  2(?i 

A-'\^i'><      American  "  chameleon  ",  iguanid  lizard:    Reptile,  361 

AyoMALOPS  KATOPTRos.     Lumiuous  fish:    teleost  (sea-bass  family). 

AyoPHELES.     Malaria-carrying  mosquito:    dipterous  insect. 

AyoPHTHALMi!i.     Blind  cavernicolous  beetle:    coleopterous  insect. 

ANOPLURA.      Order  of  in.sects  (wingless  lice,  parasitic  on  mammals). 

AyoPTicHTHYg  joRDAXi.     Blind  Mexican  cave-fish:    teleost. 

AysER.     Goose:    Anseriformes  (Anatidse). 

ANSERIFORMES.      Order  of  birds,  comprising  (mainly)  the  Anatidae. 

AyTHOLOBA.     Sea-anemone:    coelenterate  (Anthozoa). 

ANTHOZOA.     Class  of  ccelcntcrates  comprising  sea-anemones  and  corals  ("  flower  animals  "). 

AyiHROBiA.     Eyeless  cave-spider:   arachnid  (Araneida). 

ANTHROPOiDEA.      Sub-ordcr  of  Primates,  comprising  monkeys,  apes  and  man. 

AyriLOCAFRA.     Pronghorn:    a  ruminant  similar  to  antelope. 

ANURA.      Order  of  tail-less  amphibians  (frogs,  toads). 

APHANiPTERA.     An  Order  of  insects  comprising  the  wingless,  blcod-sucking  fleas. 

Aphis  roRBEffi.     Strawberry  root  louse:   hemipterous  insect. 

Aphrophora  spcmaria.     Frog-hopper  or  spittle-insect :    hemipterous  insect. 

APHroyus.     Blind  deep-sea  teleostean  fish. 

Apjs.     Honey-bee:   hymenopterous  insect,  5S 

Aplocheilichthts  rubrostigma.     Killifish:    cyprinodont  teleostean  fish. 

APODA.     Csecilians  :  an  order  of  worm-like,  subterranean  amphibians. 

Apodemvs.     Field-mouse:    a  rodent  (Muridte). 

Aptertx.     Kiwi:   flightless  New  Zealand  bird  (Ratitse),  398 

Apus  (Triors).     Fresh-water  crustacean  (Branchiopod),  208 

ARACHNID.^..     Class  of  artliropods,  comprising  spiders,  scorpions,  king-crabs,  etc. 

ARANEIDA.     Order  of  Arachnida,  comprising  spiders. 

ARAyECs  DiADEiiATUs.     Common  garden  spider:    arachnid  (Araneida),  214 

Arc  A.     Noah's  ark  shell:    bivalve  mollusc. 

ARCHiANXELiDA.     Class  of  marine  segmented  worms  (e.g.,  Dinophilus). 

Archistoma  besselsi.     Springtail:  primitive  wingless  insect  (Collembola). 

Arctocebus.     Agwantibo:    nocturnal  lemuroid  (Primate). 

Ardea.     Heron  (Ciconiiformes),  404. 

AREyicoLA  MARiyA.     Lob-worm:   burrowing  polychsete  worm,  190 

Aroyropelecus.     Hatchet  fish:    deep-sea  luminoas  teleostean  fish,  322 

Ariolimax.     Slug:    gastropod  mollusc  (Pulmonate). 

Arisielliger.     Gecko  :  reptile  of  the  lizard  family. 

Aristeomorpha.     Shrimp:    decapod  crustacean. 

Armadillidium.     Pill-bug,  a  terrestrial  woodlouse:    crustacean  (Isopoda),  4-5 

Artemia.     Brine-shrimp:    crustacean  (Branchiopod),  207 

ARTHROPODA.      Phylum    of   invertebrates,   coniprising   Onychoj)hora,   Crustacea,   Myriapoda, 

Aj-achnida,  Insecta. 
ARTioDACTYLA.     Order  of  placentals,  comprising  pig,  camel,  deer,  etc. 
AscARis.     Parasitic  round  worm:    nematode,  190 
AsciDTA.     Sea-squirt:   protochordate  (Tunicate),  228 
AsELLCs.     Blind  fresh-water  louse:    crustacean  (IsojDoda),  207 
Asio.     Long-eared  owl:    Strigidae. 
AsPLAycHyA.     A  genus  of  rotifer. 
AsTACus.     Crayfish:   decapod  crustacean,  164 


758  ZOOLOGICAL   GLOSSARY 

AsTERiAS.     Starfish:   an  echinoderm  (Asteroidea),  185 

ASTEBOIDEA.      Class  of  Echiiiodermata,  comprising  starfishes. 

AsTROScoPUS.     Stargazer:    teleostean  fish,  751 

AsTUR  PALUMBARius.     Goshawk:    bird-of-prey  (Falconiformes),  403 

Ateles.     Spider  monkey  of  S.  America:    Primate  (Cebidse),  689 

ATHERiyA.     Silverside:   teleostean  fish,  617 

AuRELiA.     Common  jellyfish:    a  coelenterate  (Scyphozoa),  183 

AvsTROLETBOPs.     Goby  fish :    teleostean  fish. 

AvicuLA.     Pearl  oyster:   bivalve  mollusc,  200 

Balms  A.     Right-whale:    a  cetacean. 

Bal.esoptera.     Blue  whale:   the  largest  cetacean,  444. 

Balasoglossvs.     Acorn  worm  :    a  protochordate  (Hemichordate),  227 

Balasvs.     Acorn-shell:    a  crustacean  (Cirripede),  209 

Balistes.     File-fish  (trigger-fish):    a  teleostean  fish. 

Baratbronvs.     a  deep-sea  teleostean  fish. 

Barbatula.     a  fresh-water  teleostean  fish. 

Bathothauma.     Deep-sea  squid:    a  cephalopod  mollusc,  203 

Bathygobius.     Goby  fish:    a  teleostean  fish. 

Bathtlaqvs  ben  edict  I.     Deep-sea  salmonid:    a  teleostean  fish,  310 

Bathypterois.     Feeler-fish:    a  deep-sea  teleostean  fish. 

Bathytevthis.     Deep-sea  octopod:    a  cephalopod  mollusc. 

Bathytroctes.     a  deep-sea  teleostean  fish. 

BATOiDEi.     Sub-order  of  flat  selachians  (skate,  ray). 

Bdellostoma.     Slime  hag:    a  cyclostome. 

Belidevs  scivreus.     a  squirrel-like  phalanger:    marsupial  (Phalangeridte). 

Belose.     Needle-fish  (garfish):    a  teleostean  fish. 

Besoalichthys.     Deep-sea  ray:    a  bat oid  selachian  fi.sh. 

Be.xthobatis.     Deep-sea  ray:    a  batoid  selachian  fish. 

Beryx.     a  deep-sea  teleostean  fish,  303 

Betta  pvaxAX  or  spies dexs.     Siamese  fighting  fish:    a  fre.sh-water  teleostean  fish,  84 

BiBio  MARci.     April  fly:    a  dipterous  insect. 

BiTis  ARiETASft.     African  puff  adder  :  a  snake  of  the  viper  family,  392 

BIVALVES  (Lamellibranchs).     Class  of  molluscs,  comprising  the  shell-fish  (clam,  cockle,  mussel). 

Blattella  oermamca.     German  cockroach:    insect  (Orthoptera). 

Blatta  oriestalis.     Common  cockroach,  black  beetle:   insect  (Orthoptera),  34 

BiEsyivs.     Blenny:    a  teleostean  fish,  310 

BOID^..     Family  of  snakes,  comprising  boas,  pythons,  etc. 

Bold  A  DEyDROPjjiLA.     Black-and-gold  tree-snake  (Mangrove  snake)  :    Opisthoglyph. 

BoLiTOTHEBVs  coRxuTus.     A  spccics  of  beetle:    insect  (Coleoptera). 

BoMBixATOR  {Bombixa)  loyEi's.     Fire-bcllied  toad:    an  anuran,  339 

BoMBTs.     Bumble-bee:    a  hymenopterous  insect,  219 

BoMBYLirs.     Bee-fly:  a  dipterous  insect,  219 

BoMBYx.     Silk-moth:    a  lepidopterous  insect. 

BoRODisuLA  iXFAys.     Snipc-eel:    a  deep-sea  teleostean  fish,  679 

Bos  TAURUS.     European  domestic  cattle  (ox,  cow):    Ruminants  (Bovidse). 

BoTAURUs.     Bittern:    a  bird  of  the  heron  family,  685 

BorroAixriLLBA.     Hydroid  colony:    a  coelenterate  (Hydrozoa). 

BOViD^.     Family  of  imgulates,  comprising  ox,  sheep,  goat,  etc. 

Box.     Sea-bream:    a  teleostean  fish. 

BRACHIOPODA.     Lamp-shells  :  a  phylum  of  Invertebrata. 

Bradypus  tridactylus.     Three-toed  sloth:    Xenarthra  (Bradypodidse). 

Braschelliox.     Leech:    an  annelid  (Hirudinea),  193 

Braxchiomma  tesiculosum.     A  marine  tubicolous  polychaete  worm,  192 

Braxchioxus.     a  genus  of  rotifer. 

BBANCHIOPODA.     An  Order  of  crustaceans,  comprising  Phyllopoda  and  Cladocera. 

Bubo.     Eagle-owl:    Strigida?,  422,  606 

B.  ASCALAPHUS.     Savigny's  eagle  owl. 


ZOOLOGICAL   GLOSSARY  759 

Bvso  LACTEDs.     Milky  eagle-owl. 

B.  oBiEyTALis.     Oriental  eagle-owl. 

BuccixuM.     Common  whelk  (buckie):    gastropod  mollusc,  197 

BUFO.     Common  genus  of  toad:    an  anuran  amphibian  (Bufonidse),  341 

B.  AREyARVM     S.  American  toad. 

B.  BUFO.     Common  toad. 

B,  MABiyus.     Giant  toad. 

B.  yiRiDis.     Green  toad. 

BvGULA.     Sea-mat;    colonial  Polyzoon,  46 

BvTEO  BCTEO.     Buzzard:    a  bird-of-prey  (Falconiformes),  417 

Casbita.     Indian  lizard:    Reptile. 

Cacatca  boseocapella.     Australian  cockatoo  :  Psittaciformes. 

Cacicts  cela.     Yellow  hang-nest:    passerine  bird  (oriole  family). 

Cecilia.     A  csecilian:    worm-like  amphibian  (Apoda). 

CAiMAy.     A  crocodilian  reptile  similar  to  the  alligator,  375 

CALAMoicBTHTf.     A  chondrostean  fish,  320 

CALAyus.     Salt-water  copepod  crustacean. 

Calious.     Fish-louse:    a  parasitic  copepod  crustacean. 

Calliactjs.     Sea-anemone:    a  ccelenterate  (Anthozoa). 

CALLioyTMus.     Dragonet:    a  teleostean  fish. 

Callipbora.     Bluebottle  (blow-fly):    a  dipterous  insect,  219 

Calotebmes.     Termite:    an  insect  (Isoptera). 

Caltpte.     Humming-bird:    Coraciiformes. 

Cambabvs.     Crayfish:    a  decapod  crustacean. 

Camelus  BACTBiAyus.     Camel:    an  artiodactyl  (Tylopoda). 

C.  DBOMEDABius.     Dromedary. 

CAyis  AUBEUg.     Jackal:    a  carnivore  (dog  family). 

C.    FAMILIABIS.       Dog. 

C.  LVPUS.      Wolf. 

Capra.     Goat:    a  ruminant  (Bovidse). 

Capbella.      "  Skeleton  shrimp  ":    an  amphipod  crustacean,  207 

Capbimvlous  eubopxvs.     Goat -sucker  (night -jar):    Coraciiformes,  410 

Cabassius  auratvs.     Goldfish:    a  cyprinoid  teleostean  fish,  292 

Cabausits.     Leaf-insect:    orthopterous  insect  (Phasmid). 

CABCBABoDoy.     White-tip  shark:    a  selachian  fish. 

CABciyrs.     Common  genus  of  crab:    a  decapod  crustacean. 

Cabditm.     Cockle:    a  bivalve  mollusc,  200 

Cabixaria.     Pelagic  heteropod:    a  gastropod  mollusc.  199 

CARiNAT^.     Sub-class  of  birds,  comprising  all  the  flying  birds. 

CARNivORA.     An  order  of  flesh-eating  mammals  comprising  the  Fissipedia  and  Pinnipedia. 

Castor.     Beaver  :   an  amphibious  sciuromorph  rodent,  442. 

Cascarics.     Cassowary:    flightless  bird  (Ratitse),  406. 

CATARRHiNES.      Old  World  monkeys  (Cercopithecidse  and  anthropoid  apes). 

Catscs  RHOMBEATrs.     Capeviper:    viperid  .snake. 

Cav/a  PORCELirs.     Guinea-pig:    a  rodent  (Hystricomorph). 

CEBiDiE.      American  monkej's  (Platyrrhines)  :  a  family  of  Primates. 

Cebvs.     Capuchin  monkey:    a  primate  (Cebidae). 

CEyTROPRORis  cALCErs.     Deep-sea  shark:    a  selachian  fish. 

CEyTRosTEPHAyi's  xo.v67.s\p/.vr.<.      Sea-urchin:    an  echinoderm  (Echinoidea),  117 

Cephala^pis.     Extinct  agnathous  fish,  234 

CEPHALOCHORDATA  (Acrania).      A  sub-phylum  of  chordates,  comprising  the  lancelets. 

CEPH.\LOPODA.      A  class  of  molluscs,  comprising  octopus,  squid,  nautilus,  etc. 

CBBATOPOGoy.     A  midge:    dipterous  insect. 

Cbbcocebus.     Mangabey  of  Africa:    a  primate  (Cebidae). 

Cebeopsis.     Australian  goose:    Anseriformes. 

Cebvvs  POBciyvs.     Hog-deer:    a  ruminant. 

CESTODA.      A  class  of  unsegmented  worms  comprising  the  parasitic  tape-worms. 


760  ZOOLOGICAL   GLOSSARY 

CETACEA.     An  order  of  mammals,  comprising  the  whales  and  dolphins. 

Cetomimus.     a  deep-sea  teleostean  fish. 

Cetonia.     Rose-chafer:    a  coleopterous  insect,  219 

CH^TOGNATHA.     Arrow-worms  :  a  phylum  of  invertebrates. 

Cs.eTOPTERus.     A  sedentary  polychsete  worm. 

Chammleon.     The  chameleon  :  reptile  of  the  lizard  family. 

CHAyo3.     Milk-fish:    a  clupeid  teleostean  fish. 

Char  AX.     Sea-bream:    a  teleostean  fish. 

Charixa.     Rubber-boa:    a  boid  snake. 

Chartbdea.     a  jelly-fish:   ca^lenterate  (Scyphozoa). 

Cbelidon.     Martlet,  a  common  European  martin  :  passerine  bird  of  the  swallow  family. 

Cbelodina  LosaicoLLis.     Murray  turtle:    a  chelonian  reptile. 

Chelonia  mydas.     The  green  or  edible  turtle  :  a  chelonian  reptile. 

CHELONiA.     An  order  of  reptiles,  comprising  the  tortoises  and  turtles. 

CHELONID^.     A  family  of  chelonians  comprising  the  marine  turtles. 

Cheltdra  sERPESTJyA.     The  alligator  terrapin  (snapping  turtle)  :  a  chelonian  reptile. 

CHILOPODA.     An  order  of  myriapods,  comprising  the  centipedes. 

Chim.era  MoysTROSA.     Rabbit-fish:    a  holocephalian  fish. 

Chinchilla.     The  chinchilla:    a  rodent  (Hystricomorpha). 

Chirosomvs.     a  dipterous  insect. 

CHiROPTERA.     An  Order  of  mammals  comprising  the  bats. 

Chiton.     "  Coat-of-mail  ":    a  mollusc  (Placophora),  198 

Chlamtdosavrus.     Frilled  lizard:    an  agamid  lizard,  35(5 

Gbol(epvs  didacttlus.     Two-toed  sloth:    Xenarthra  (Bradypodidse),  607 

Choloqaster.     Kentucky  cave-fish:    a  teleostean  fish  (Amblyopsida;). 

CHONDRiCHTHYES.     Class  of  Cartilaginous  fishes  comprising  the  selachians  and  holocephalians. 

CHONDROSTEi.     A  sub-class  of  bony  fishes  comprising  the  sturgeons  and  Polypterini. 

Chortippus.     a  grasshopper:    insect  (Orthoptera). 

Chrtsemts  picta.     Painted  terrapin:    a  chelonian  reptile. 

Chrisochloris.     Golden  mole:    a  mammal  (Insectivore),  442 

Chrtsops  marmoratus.     Horse-fly:    a  dipterous  insect  (Tabanidse). 

Chrtsotis.     Green  parrot:    Psittaciformes 

Chthonivs  iffCHNocHULES.     A  pseudo-scorpiou:    Arachnida,  215 

Ciohla.     a  cichlid:    fresh-water  teleostean  fish,  291 

CiciNDELA.     Tiger  beetle:    a  coleopterous  insect. 

cicoNiiFORMES.     An  Order  of  water  birds  comprising  herons,  spoonbills,  storks,  etc. 

CILIATA.      Order  of  Protozoa  comprising  Paramacium,  Stentor,  etc. 

CILIOPHORA.     A  class  of  Protozoa  comprising  Ciliata  and  Suctoria. 

CiNTXis  EROS  A.     Pitted  hinged  tortoise  :  a  I'eptile. 

CioNA.     A  protochordate  (Tunicata). 

CIRRIPEDIA.     An  order  of  crustaceans,  comprising  barnacles,  acorn-shells,  etc. 

Cirrothavma  murrati.     a  blind  deep-sea  octopod:    cephalopod  mollusc. 

Cist  ELLA.     A  lamp-shell:    Brachiopod. 

CiTELLVs  ciTELLVs.     Souslik  (grouud  squirrel):    a  rodent  (Sciuridse). 

CLADOCERA.     Sub-ordcr  of  branchiopod  crustaceans  comprising  the  water  fleas. 

Cladophora.     An  alga:  a  thallophyte. 

Clemmts.     Terrapin  (water-tortoise):    a  chelonian  reptile,  682. 

Clethrionomys.     Red  backed  vole:    a  rodent  (mouse  family). 

Clupea  harbngus.     Herring:    a  clupeid  teleostean  fish,  299 

C.  pilchardus.     Sardine. 

CLUPEID^.      Family  of  teleostean  fishes  including  herrings,  anchovies,  etc. 

CNiDARiA.     Sub-phylum   of  stinging   coelenterates,   including   jellyfish,   sea-anemones,   etc. 

COELACANTHINI.     Sub-class  of  bony  fishes,  with  a  single  extant  species — Latimeria. 

CCELENTERATA.     The  phylum  comprising  jellyfish,  hydroids,  sea-anemones,  etc. 

CoLAPTEs.     A  woodpecker  (flicker)  :  bird  of  the  family  Picidse,  420. 

Coleonyx.     a  gecko:    a  reptile  of  the  lizard  family. 

COLEOPTERA.     All  Order  of  insects  comprising  the  beetles. 

COLLEMBOLA.     An  Order  of  primitive,  wingless  insects  comprising  the  springtails. 


ZOOLOGICAL   GLOSSARY  761 

Coluber  guttaivs.     Corn  snake:    a  colubrid  snake. 

COLUBRIDJE.     The  largest  family  of  snakes,  containing  the  cobras,  grass  snakes,  rattlesnakes, 

etc. 
Coin  MBA.     Pigeon:    Columbidse. 

C.  iiviA.     Rock-dove,  from  which  domestic  pigeons  originated. 
C.  PALUMBus.     Wood-pigeon  or  ring  dove. 

COLUMBiD^.     Family  of  birds  comprising  the  pigeons  and  doves. 
CoNOLOPHVs  suBcRisTATua.     Galapagan  iguanid  lizard:    a  reptile. 
Constrictor  coysTRicioR.     Common  boa:    a  S.  American  bold  snake. 
COPEPODA.     An  order  of  free-swimming,  planktonic,  or  parasitic  crustaceans,  comprising  Copi- 

lia,  Cyclops,  CciUgus,  etc. 
CopiLiA.     A  free-swimming  copepod  crustacean,  209 
CoRDTLosAURvs.     Alizard:    lacertilian  reptile. 
CoREPHiuM.     A  placophoran  mollusc. 
CORVID^.     The  crow  family  of  birds  :  Passeriformes. 
CoRvus  MOSEDVLA.     A  jackdaw:   crow  family. 
CoRTCEVs.     A  copepod  crustacean. 
CoTTUs  BUBALis.     Bull-liead:    a  teleostean  fish. 
Craqo  {Craagos).     Common  shrimp:    a  decapod  crustacean,  205 
Cresilabrus.     a  teleostean  fish. 

Cribrixa  .     A  sea-anemone:   coelenterate  (Anthozoa). 
CRINOIDEA.     A  class  of  Echinodcrms,  comprising  sessile  sea-lilies  and  free-swimming  feather 

stars. 
CROCODILIA.     An  order  of  reptiles  comprising  the  crocodiles,  alligators,  gavials. 
Crocodilus.     Crocodile:    a  reptile,  378. 
C.  PORosus.     Salt-water  (estuarine)  crocodile. 
CROSSOPTERYGii.     A  sub-group  of  bony  fishes,  the  modern  representatives  of  which  are  the 

Dipnoans,  but  from  which  were  derived  the  Amphibians,  Reptiles,  Birds  and  Mammals. 
CROTALiD^.     A  family  of  viperine  snakes  comprising  the  pit  vipers  (rattlesnakes,  moccasin, 

etc.). 
Crotalvs.     Rattlesnake:    crotalid  snake. 
Crotaphttvs.     a  lizard:    lacertilian  reptile. 
CRUSTACEA.     A  class  of  Arthropoda  comprising  the  larger  crabs,  lobsters,  etc.,  and  the  small 

water-fleas,  copepods,  etc. 
CRTPTOBRAycHVs.     "  Hellbender  ",  American  salamander:    a  urodelan  amphibian. 
CRTPToirMPAyA.     A  cicada:    hemipterous  insect. 

CTENOPHORA.     A  class  of  nou-stinging  ccelenterates  comprising  the  comb-jellies. 
Cvlex.     a  mosquito:    dipterous  insect. 

CuNicVLVs.     Spotted  cavy  (paca):    a  rodent  (Hystricomorph). 
Ctaxocitta.     Blue-jay:    a  passerine  bird  of  the  crow  family,  414 
Ctclodorippe.     a  deep-sea  crustacean. 
CrcLOPs.     A  fresh-water  copepod  crustacean,  152 
CrcLosA  lysuLASA.     A  Malayan  spider:   arachnid  (Araneida). 
CYCLOSTOMATA.     An  extaut  sub-class  of  the  agnathous  fishes,  comprising  the  lampreys  and 

hag-fishes. 
Ctmonomus.     a  deep-sea  crustacean. 

Ctxictis.     a  viverrine  carnivore  of  the  mongoose  family. 

CryoMYS.     Prairie-dog  :  an  American  burrowing  rodent  of  the  squirrel  family. 
CrpRiDiyA.     Salt-water  ostracod  crustacean. 

CYPRINID^.     The  family  of  teleostean  fishes  comprising  the  carp,  miiniow,  goldfish,  etc. 
CrPRiyvs  CARPio.     The  carp:    cyprinoid  teleostean  fish,  291 
CrPRis  {Ci'prja).     Fresh-water  ostracod  crustacean,  152,  208 
CYSTOFLAGELLATA.      Planktonic  flagellate  Protozoa. 

Dacelo  gioas.     Laughing  jackass  (Australian  kingfisher):    Alcedinidae. 
DACTryoTUs  obscuras.     An  aphid:    hemipterous  insect  (Aphididae),  224 
Dafila  acvta.     Pintail  duck:    Anseriformes  (Anatidse). 
DAPHyiA  .     Water-flea:    a  branchiopod  crustacean  (Cladocera),  74,  208 


762  ZOOLOGICAL   GLOSSARY 

DABTCHoyE.     Tubicolous  polychsete  worm. 

Dastpeltis  scabra.     The  egg-eating  snake:    an  African  colubrid  snake,  392 

Dastpus.     Armadillo:    Xenarthra  (Dasypodidse),  442 

Dasturvs.     Australian  native  cat  or  dasyure:   marsupial  (Dasyuridse),  438 

DECAPODA.     An  order  of  larger  crustaceans,  comprising  the  lobster,  shrimp,  crab,  etc. 

Delphisus.     The  dolphin  :  a  small  toothed  whale,  444 

Demodex  folucvlorvm.     Follicle  mite:    an  arachnid  (Acarina). 

Dendroc(elum.     Flat-worm:    a  turbellarian  (Tricladida),  18S 

Desdrocopus  major.     Great  spotted  woodpecker:    Picidse,  414 

DEXDRocroNA.     Tree-duck:    Anseriformes  (Anatidse). 

DESTALinM.     Elephant's  tooth  shell:   scaphopod  mollusc,  197 

DERMAPTERA.     An  Order  of  insects,  comprising  the  earwigs. 

Dermochelts  coriacea.     Leathery  skinned  turtle:    a  chelonian  reptile. 

DERMOPTERA.     An  Order  of  mammals  comprising  the  flying  lemurs. 

Desmodus.     Vampire  bat:    Chiroptera. 

DiADEMA.     A  sea-urchin:    echinoderm  (Echinoidea),  185 

DiALOMMVs  Fvscvs.     Four-eyed  blenny:    a  teleostean  fish. 

DicoTTLES.     Peccary:   Artiodactyl  (pig  family),  458 

DiDELPHTs  rjRGixiAXA.     Virginian  opossum:    American  marsupial,  439 

DiSEurus.     A  whirligig  beetle:    coleopterous  insect  (Gyrinidse). 

DiNOFLAGELLATA.     Planktonic  flagellate  Protozoa,  179 

DisoPBiLVs.     A  marine  archiannelid  worm. 

DioMEDEA    CAUTA.     Albatross,     the     largest     of     the     sea-birds,     related     to     the     petrels: 

Procellariiformes,  418 
DiPLOPODA.     An  order  of  Myriapoda,  comprising  the  luillipedes. 
DIPNOI.     A  sub-class  of  bony  fishes,  coinprising  the  lung-fishes. 
DiPTERA.     An  order  of  insects  comprising  the  true  flies. 
DisPHOLiDvs.     A  colubrid  snake:    Ophidia. 
Dixippus.     Stick-insect:    an  orthopterous  insect,  218 
DoLicHOPTERTx.     A  decp-sca  teleostean  fish. 

DoLicHOTis  PATAQOMCA.     Patagonian  cavy:    a  rodent  (Hystricomorph). 
DoRTLus.     An  African  driver-ant:    a  blind  hymenopterous  insect  (Formicoidea). 
Drepaxophorus.     a  nemertine  worm. 
Drom.evs.     The  emu:    a  flightless  bird  (Ratitae),  397 
Drosophila.     The  fruit-fly:    a  dipterous  insect,  44 
Drtophis.     Long-nosed  tree-snake:    a  reptile. 
Drtopuiops.     a  relative  of  Dryophis. 
Dttiscus  MARGixAi.is.     Camivorous  water-beetle:    a  coleopterous  insect,  168 

ECHiNODERMATA.  A  phyluni  of  invertebrates,  comprising  starfishes,  sea-urchins,  feather- 
stars,  etc. 

ECHINOIDEA.     A  class  of  cchinoderms  (sea-urchins). 

EDENTATA.  A  former  title  for  three  orders  of  mammals — Xenarthra,  Pholidota  and  Tubuli- 
dentata. 

Eisexia  FOETiDA.     The  dung-hcap  earthworm :   an  oligochsete  worm. 

Elaphe  QUADRifiTATTA.     Chickeu  snake:    a  colubrid  snake. 

E.  quAToRLisEATA.     Four-liue  snake. 

elapidjE.     a  family  of  venomous  snakes,  including  the  cobras,  coral  snakes,  tiger  snakes,  etc. 

Elaps.     Coral-snake:    an  elapid  snake. 

ELATERiD^.     A  family  of  beetles  comprising  the  click-beetles  (fire-beetles)  :  Coleoptera. 

Electrophorus  electricus.     The  electric  eel:    a  teleostean  fish. 

Eledoxe.     An  octopod:    cephalopod  mollusc,  146 

Elephas  maximvs.     The  Indian  elephant:    Proboscidea. 

Eliomts.     a  dormouse:    a  myomorph  rodent  (Gliridae). 

Ellobivs.     a  rodent  mole:    mouse  family. 

Eltsia.     a  marine  gastropod  mollusc  (Opisthobranch). 

Emplectoxema  kaxdai.     a  luminous,  marine,  nemertine  worm. 

Emtda.     Soft-shelled  turtle:    a  chelonian  reptile. 


P 


ZOOLOGICAL   GLOSSARY  763 

Emtda  ORAyosA.     Burgoma  soft -shelled  turtle. 
Emts.     Fresh-water  tortoise:    a  chelonian  reptile  (Testudinidse). 
E.  ORBICULARIS.     European  pond  tortoise. 

EscHELioPBis  JORDASi.     Pearl-fish:    the    larval    form    of    Fierasfer   which  is   parasitic  in  sea- 
cucumbers  or  bivalves:    a  teleostean  fish  of  the  blenny  family. 
Ea'Gravlis.     The  anchovy:    a  clupeid  teleostean  fish. 
EsTospHEScs.     A  lamprey:   cyclostome. 

EPHEMEROPTERA.     An  order  of  insects  comprising  the  mayflies. 

Ephestia.     The  flour-moth:    lepidopterous  insect,  the  larvae  of  which  feed  on  flour. 
Epicrates.     a  tree-boa:    a  non-poisonous  boi'd  snake. 
Episephelcs.     Grouper  fish:    a  teleostean  fish  of  the  sea-bass  family,  92 
Epomophorvs.     An  Ethiopian  fruit -bat:    Megachiroptera. 
Epiatretvs.     The  Chilean  borer,  a  slime-hag:    myxinoid  cyclostome. 
Equcs  (Asiyus)  asisus.     Ass  (donkey):   Equidae. 
E.  CAS  a  LLCS.     The  domestic  horse. 

E.  PRZEWALSKii.     Prejvalski's  horse  (a  wild  horse  of  Asia),  686 
E.  soMALiExsis.     Somali  wild  ass,  686 

E.  ZEBRA.     The  zebra,  444 

Erax  rufibarbis.     a  robber-fly:    dipterous  insect. 

Eremias.     a  desert  lizard:   reptile  (Lacertidae). 

Erictmba.     Silverjaw  minnow:    a  cyprinoid  teleostean  fish. 

EniyACEi'-s.     Common  genus  of  hedgehog:    an  insectivorous  mammal,  442 

Eristalis.     Drone-fly:    a  dipterous  insect. 

Erithacus  rubecvla.     European  robin:    a  passerine  bird  (thrush  family). 

Errantia.     a  division  of  polychaete    worms  comprising    the  free-swimming  types   (such  as 

Nereis)  in  contrast  to  the  Sedentaria. 
Ertx.     Sand-boa:    a  boid  snake. 

Esox  LUCIUS.     The  northern  pike:    teleostean  fish  (Esocidae). 
Etmopterus.     a  deep-sea  luminous  shark:   selachian  fish. 
EucALiA.     A  stickleback:    teleostean  fish. 
Evdbsdrivm.     a  hydrozoan  coelenterate. 

Eudtptes  cbistatus.     Rock-hopper  penguin:    aquatic  bird  (Impennes),  408 
Euolesa.     Flagellate  protozoon  which  forms  green  scum  on  stagnant  water,  179 
EvyicE.     A  free-swimming  polychaete  worm. 
EuPAOURUs.     A  hermit-crab:   decapod  crustacean,  58 
Evphagus  ctasocephalvs.     a  blackbird:    passerine  bird  (thrush  family). 
EupoLTODosTES.     A  pelagic  free-.swimming  polychaete  worm. 
EuPROcTis,     Tussock  moth:    lepidopterous  insect  (Lymantrid). 
EURYPTERiDA.      An  extinct  order  of  aquatic  arthropods,  related  to  the  arachnids  (particularly 

the  king-crabs),  157 
EUSELACHii.     A  sub-class  of  selachian  fishes,  comprising  the  sharks  and  dogfishes. 
EvARCHA  BLAycARDi.     A  jumping  spider:    arachnid  (Araneida:    Salticidse),  580 
ErsRMAyELLA.     A  deep-sea  teleostean  fish. 

Fabricia.     a  free-swimming  polychaete  worm. 
Falco.     Falcon:    a  bird-of-prey  (Falconiformes). 

F.  TiyyuycuLCs.     The  kestrel. 

FALCONIFORMES.     An  order  of  birds,  comprising  the  birds-of-prey  (eagle,  hawk,  vulture,  etc.) 
Fasciola  hepatic  a.     The  liver-fluke:    a  trematode  worm,  189 
FsLis  domestica.     Cat:    a  carnivore  (Felidae). 
F.  LEO.     The  lion. 
F.  LiBTCA.     The  bush-cat. 
F.  iryx.     The  Ijtix,  444. 
F.  oycA.     The  jaguar. 
F.  parous.     The  leopard. 
F.  TIGRIS.     The  tiger. 

FissiPEDiA.     A  sub-order  of  mainly  terrestrial  carnivores,  comprising  the  cat,  dog,  bear  families, 
etc. 


764  ZOOLOGICAL   GLOSSARY 

FiTZROTA  LiNEATA.     A  teleostean  fish. 

FLAGELLATA.     A  class  of  Protozoa  with  undulating  flagella,  comprising  Euglena,  Volvox,  Nocti- 

luca,  etc. 
FORAMINIFERA.     An  Order  of  rhizopod  Protozoa  having  a  calcareous  shell,  179 
FoRFicvLA.     The  common  earwig:    an  insect  (Dermaptera),  218 
FvLicA.     The  coot:  an  aquatic  bird  (Ralliformes). 

FuLMARvs  GLACiALis.     The  fulmar  petrel;    an  aquatic  bird  (Procellariidae). 
FvNDULVs.     Killifish:    a  cyprinodont  teleostean  fish,  308 

Oadvs  uorrhua.     The  codfish:    a  teleostean  fish  (Gadidse),  299 

Oalago.     The  bush-baby:    a  nocturnal  lemuroid  (Primate). 

Oaleoriiixus.     The  school  shark:    a  selachian  fish. 

GALLiFORMES.     An  Order  of  birds,  comprising  the  game-birds  (chicken,  pheasant,  grouse,  etc.). 

Oallus  domesticus.     Domestic  fowl:    Galliformes. 

Qammarvs.     A  fresh-water  shrimp:    amphipod  crustacean. 

Oarrulvs.     The  jay:    a  passerine  bird  of  the  crow  family. 

Oasterostevs  aculeatu.i.     Three-spined  stickleback:    a  teleostean  fish,  84 

Oastropacha  RVBi.     A  lappet  moth :   lepidopterous  insect. 

GASTROPODA.     A  class  of  molluscs  comprising  the  snails,  whelks,  limpets,  etc. 

Oavia.     The  diver  or  loon:    a  fish-eating  diving  bird  (Colymbiformes). 

Oazella.     The  gazelle:    a  ruminant  (Bovidfe)  of  the  antelope  family,  444 

Oekko  gekko.     a  gecko:    lacertilian  reptile  (Geckonidse). 

Oelasimus  ARcvATUfi.     A  fiddler-crab:    decapod  crustacean,  205 

Oeonemertes.     a  terrestrial  nemertine  worm. 

Oeoplaxa  MEXicASA.     A  planarian  worm:   Turbellaria  (Tricladida),  188 

Oeotria  AUSTRALIA.     A  lamprey:    cyclostome. 

Oeotrupes.     The  dung-beetle:    a  coleopterous  insect,  61 

Oeraxoa'etus.     The  Chilean  eagle:    a  bird-of-prey  (Falconiformes),  398 

Oerrhosaurus  GRAXDif.     African  plated  lizard:    a  lacertilian  reptile. 

Oigaxtactis.     Angler-fish:    a  deep-sea  teleostean  fish. 

OiGAXTURUs  CHVxi.     Giant-tailed  fish:    a  deep-sea  teleostean  fish,  322 

QiLLicHTHYS  MiRABiLis.     Mud-sucker:    a  goby  fish  (Teleost). 

QiNGLTMosTOMA.     Nurse  shark:   a  selachian  fish. 

OiRAFFA  CAMELOPARDALis.     The  giraffe:    a  ruminant,  444 

OiRELLA.     Sea-bream:    a  teleostean  fish. 

Olossixa.     The  tsetse-fly:    a  dipterous  insect  (Muscidse),  45 

GoBivs.     A  goby-fish:    small  marine  teleostean  fish  (Gobiidse),  296 

OoxATODES  Fuscus.     A  gecko:    lacertilian  reptile  (Geckonidse). 

OoxEPTERYX  RHAMxi.     A  buttcrfly:   lepidopterous  insect. 

OoxjuM.     An  alga:    a  thallophyte. 

GoxoDACTYLvs.     A  stomatopod  crustacean,  60 

OoxTAVLAX.     A  dinoflagellate  protozoon,  179 

QoRiLLA  GORILLA.     The  gorilla:    an  anthropoid  ape  (Primate). 

Grus.     The  crane:    a  long-legged  bird  (Gruiformes). 

GuLo  Luscns.     The  wolverine:    a  badger-like  carnivore  (Mustelidse). 

Gi'MxoTHORAX.     The  Moray  eel:    a  teleostean  fish. 

Gtmxvra.     The  rat-shrew:    an  insectivore  of  the  hedgehog  family. 

GYRiNiD^.     The  aquatic,  carnivorous  whirligig  beetles  :  Coleoptera. 

H^MADipifA.     A  land  leech:    an  annelid  (Hirudinea),  190 

H.EMOPis.     A  horse-leech:    an  annelid  (Hirudinea). 

Hajdeotritox.     a  blind  salamander:    urodelan  amphibian. 

Hahaetvs  leucocephalvs.     The  bald  sea-eagle:    a  bird-of-prey  (Falconiformes),  410 

Halicore  (Dvgoxg).     The  dugong  or  sea-cow:    a  sirenian  mammal. 

Haliotis.     Ear-shell  or  abalone:    a  gastropod  mollusc  (Prosobranch). 

Hapalemvr.     a  Madagascan  lemur:    Primate  (Lemuridse). 

HAPALiD^.     A  family  of  New  World  monkeys,  comprising  the  marmosets. 

Hatteria.     See  Sphexodox. 


ZOOLOGICAL   GLOSSARY  765 

Heliodrilus.     An  oligochsete  worm. 

Helix.     The  common  genus  of  snail:    a  gastropod  mollusc  (Pulmonate),  142 

H.  ASPERSA.     Garden  snail. 

H.  POM  ATI  A.     Edible  (Roman)  snail. 

Heloderma.     The  Gila  monster  :  a  poisonous  lizard  of  Mexico  and  Arizona,  359. 

Helophilvs.     The  hover-fly:    a  dipterous  insect,  141 

HEMICHOKDATA.     A  sub-i3hylum  of  the  Protochordata,  including  Balanoglossus. 

Hemichromis  bimacvlatvs.     a  jewel  fish  (spotted  cichlid):    teleostean  fi.sh. 

Hemidacttlvs.     a  nocturnal  gecko:   lacertilian  reptile  (Geckonidse),  629 

Hemhitsis.     a  mysid  (opossum  shrimp):    schizopod  crustacean. 

HEMiPTEBA.     An  Order  of  insects,  comprising  the  bugs — Homoptera  (cicadas,  aphids,  etc.), 

and  Heteroptera  (bed-bug,  Notonecta,  etc.). 
Herpestes.     The  mongoose:    a  viverrine  carnivore,  472 
Heterodos  madaoascariensis.     Madagascar  sharp-nosed  snake:    a  reptile. 
Heterodostus  phillippi.     Port  Jackson  shark:    a  selachian  fish,  286 
HETEROPODA.      A  class  of  pelagic  gastropod  molluscs  (Prosobranchs),  including  Pterotrachea, 

Ckirinaria,  etc. 
Heteroteuthis.     A  deep-sea  luminous  squid:    cephalopod  mollusc. 
HioDo.y.     "Moon-eye":    a  fresh-water  teleostean  fish. 
Hippocampus.     The  sea-horse:    a  teleostean  fish,  related  to  pipe-fish,  310 
HiPPOLYTE  variaxs.     The  chameleon  jjrawn:    a  decapod  crustacean,  91 
Hippopotamus.     The  hippopotamus:    an  artiodactyl  of  the  pig  family  (Suoidea). 
HiRUDiNEA.     The  leech  family  :  annelid  worms. 
HiRUDo  MEDiciXALis.     The  medicinal  leech,  193 
Hirundo  rustica.     The  chimney  swallow:    a  passerine  bird,  414 
HOLOCEPHALIA.     A  sub-class  of  the  cartilaginous  fishes  comprising  the  chimseras. 
HOLOSTEI.      A  sub-class  of  bony  fishes,  comprising  the  gar-pike  and  the  bowfin. 
HoLOThURiA.     A  sea-cucumber:  echinoderm  (Holotliuroidea),  185 
HOLOTHUROiDEA.     A  class  of  Echinodemiata,  comprising  the  sea-cucumbers. 
homalopsintE.     a  sub-family  of  colubrid  snakes,  comprising  some  species  of  river-snake. 
HoMARUs  vuLOARis.     The  common  lobster:    a  decapod  crustacean,  206 
Hr.ENA.     The  hyaena:    a  nocturnal  carnivore  (Fissipede),  444 
H.  BRuyxEA.     Brown  hyaena. 
H.  STRIATA  (fir-EXA).      Striped  hyaena. 

Hi'DRA.     A  fresh-water  polyp:    hydrozoan  coelenterate,  i<^2 
HYDRACARiNA  (hydrachnida).     Watcr-mites  :  a  family  of  Acarina. 

HrDRocHCERus  CAPrSARA.     The  capybara:    the  largest  of  the  rodents  (Hystricomorpha). 
HYDROID.      Colonial   polyp    stage    of   a   hydrozoan    coelenterate,    from    which    free-swimming 

inedusoids  are  liberated. 
Htdroides.     a  genus  of  polychaete  worm. 

HYDROPHiN.E.     A  sub-family  of  the  Elapidse,  comprising  the  .sea-snakes. 
HYDROZOA.      A  class  of  ccelentcrates,  consisting  of  the  solitary  and  colonial  polyps  and  medu- 

soids. 
Htgrobates.     a  fresh -water  mite:    Hydracarina. 

HriA  arborea.     European  tree-frog:    an  anuran  amphibian  (Hylida^),  341 
H.  ccERULEA.     Australian  green  tree-frog. 
H.  VASTA.     Giant  tree-frog  of  Haiti. 

Hylobates.     The  gibbon:    an  anthropoid  ape  (Primate). 

HrMEXOL.EMUs  MALACORHi-ycHVs.     New  Zealand  Vjlue  duck:    Anseriformes  (Anatidae). 
HYMENOPTERA.     An  Order  of  insects  comprising  the  bees,  ants,   wasps   (Aculeata),  and  the 

sawflies,  ichneumon  flies,  etc. 
HyyoBius.     A  Japanese  salamander:    urodelan  amj^hibian. 
HrPERooDON.     The  beaked  or  bottle-nosed  whale:    a  cetacean  (Odontoceti). 
HrpyARCE.     An  electric  ray:    selachian  fish. 
HrpoOEOPMis.     A  caeeilian  amphibian. 

HrPOPACHUs  lycRASsATUs.     An  American  toad:    an  anuran  amphibian. 
HrpsiOLEyA.     Spotted  night  snake:    a  colubrid  snake. 
HrpsiPRYMyvs  RUPEscEys.     Rufous  rat-kangaroo:    a  marsupial  (Macropodidse). 


766  ZOOLOGICAL   GLOSSARY 

HYBACOiDEA.     An  Order  of  mammals  comprising  the  coneys  or  hyraxes. 

HYSTRICOMORPHA.     A  sub-ordcr  of  rodents,   comprising  the  porcupines,   eavies,   chinchilla, 

etc. 
HrsTRix  cRisTiTA.     The  Old  World  porcupine:    a  hystricomorph  rodent,  442 

IchthtomtzomS.      American  fresh-water  lamprey:    a  cyclostome. 

IcHTETOPHis.     A  caecilian  amphibian,  730 

ICHTHYOPSIDA.     A  group  of  vertebrates  comprising  the  fishes  and  amphibians  (contrasted 

with  the  Sauropsida  and  Mammalia). 
Idiacaxthus.     a   deep-sea  teleostean  fish,   the  larva  of  which   is  Stylophthalmus,   328 
Idotba.     Beach-louse:    an  isopod  crustacean. 

lauASA.     A  large,  crested  American  lizard:    lacertilian  reptile  (Iguanidae),  358 
I.  lUBERcuLATA.     Tuberculatcd  iguana  of  W.  Indies. 
IMAGO.     A  sexually  mature  adult  insect. 

IMPENNES  (Sphenisciformes).     A  family  of  birds  comprising  the  penguins. 
Indeis.     a  Madagascan  lemur:    Primate  (Lemuroidea). 

iNSECTivoKA.     A  primitive  order  of  mammals,  comprising  the  hedgehogs,  moles,  shrews,  etc. 
Ipxops.     a  blind  deep-sea  teleostean  fish,  724 
ISOPTERA.     An  order  of  insects  comprising  the  termites. 
IsTioPBORUs.     Sail-fish:    a  pelagic  teleostean  fish,  related  to  swordfish. 
IXODIDES.     A  sub-order  of  Acarina,  comprising  the  ticks. 

JvLis.  A  wrasse:  teleostean  fish  (Labridse). 
JuLVS.  A  millipede:  myriapod  (Diplopoda). 
Jvxco  HTMESALis.     An  American  finch:    a  passerine  bird  (finch  family). 

Kaloula  pvlchra.     Malayan  bull-frog:    an  anuran  amphibian. 

Labrvs.     a  wrasse:    teleostean  fish  (Labridse). 

Lacerta.     The  common  genus  of  lizard:    a  reptile. 

L.  MURALis.     The  wall-lizard,  355 

L.  viBiDis.     The  green  lizard. 

L.  viviPARA.     The  common  English  lizard. 

LACERTiLiA.  A  sub-order  of  reptiles  comprising  the  lizards  (geckos,  chameleon,  slow- worms, 
etc.). 

L.EMARons.     Greenland  shark:    a  selachian  fish,  281 

LAGOMORPHA.  The  family  of  rodents  (or,  more  recently,  a  separate  order  of  mammals),  com- 
prising the  rabbits  and  hares,  and  the  pikas. 

Laoopvs  mutvs.  The  ptarmigan  :  a  bird  of  the  northern  and  mountainous  regions  (grouse 
family). 

Laoostomus.     The  vizcacha:    a  hystricomorph  rodent,  442 

Lama.  The  llama  (alpaca,  vicugna)  of  S.  America:  an  artiodactyl  (Tylopoda).  relative  of 
the  camel,  444 

LAMELLIBRANCHS.       See  BIVALVES. 

Lamxa  coRyvBicA.     The  porbeagle  shark:    a  selachian  fish,  283 

Lampasyctus.     a  deep-sea  teleostean  fish. 

Lampetra  FLUviATiLis.     The  river  lampern:    a  cyclostome. 

L.  PLASERi.     The  brook  lampern. 

Lamprocolius  chaltbeus.     a  starling:    passerine  bird  (Sturnidae). 

Lampropeltis  getvlvs.     The  king-snake:    a  N.  American  colubrid  snake. 

LAMPYRiD^.     A  family  of  beetles  including  the  fire-flies  (male)  and  the  wingless  glow-worms 

(female  or  larva). 
Lampyris   (yocTiLUCA    and  sple.\didula).     Fire-flies  or  glow-worms  :  Coleoptera  (Lampyridae). 
Laxics.     Shrike  (butcher  bird):    a  passerine  bird  (Laniidas),  662. 
Lanthanotus.     a  lizard  of  Borneo,  related  to  Heloderma:   a  reptile. 
LARiD^.     The  gull  family  of  birds. 
Larvs  aroentatus.     The  herring-gull. 
Lasivs.     a  garden  ant:   hymenopterous  insect  (Formicidee). 


ZOOLOGICAL   GLOSSARY  767 

Latimeria.      The  coelacanth  :  a  bony  fish,  descended  from  the  crossopterygians,  thought  to  be 

extinct  but  recently  found  off  the  coast  of  Africa,  315 
Latrodectvs.     a  small  venomous  spider  (katipo)  of  Australasia:    arachnid  (Araneida),  84 
Leasder.     a  prawn:   decapod  crustacean,  578 

Lebistes  reticulatvs.     The  guppy  ("millions  fish"):    a  cyprinodont  teleostean  fish. 
Lemur  catta.     The  rat -tailed  lemur,  a  "  true  "  lemur  of  Madagascar:   Primate  (Lemuroidea). 
LEMUKOiDEA.     A  sub-order  of  Primates,  comprising  the  "  true  "  lemurs,  and  the  nocturnal 

lemuroids  (galago,  loris,  Xycticebus,  etc.). 
Leotichius  GLAVcoPis.     A  cave-bug:    a  hemipterous  insect,  222 
Lepadogaster.     Cling-fish:    a  carnivorous,  marine  teleostean  fish. 

Lepas.     The  ship-barnacle,  with  a  free-swimming  nauplius  larva:    a  cirripede  crustacean,  209 
LEPiDOPTERA.     An  Order  of  insects,  comprising  the  butterflies  and  moths. 
Lepidosires.     The  South  American  lung-fish:    a  dipnoan  fish,  312 
Lepidostevs.     The  gar-pike:    a  holostean  fish,  321 

Lepisma.     The  silver-fish:    a  primitive,  wingless  insect  (bristletail:    Thysanura),  218 
Lepomis.     a  sun-fish:    a  fresh-water  teleostean  fish. 
Leptisotarsa.     Colorado  beetle:    a  coleopterous  insect,  219 
Leptodeira  A.yM'LATA.     A  colubrid  snake. 

Leptodora.     a  water-flea:    a  branchiopod  crustacean  (Cladocera),  207 
LsPTOoyATUvs.     The  serpent -eel  of  New  Zealand:    a  teleostean  fish. 
Leptoplaxa.     a  leaf-like,  marine  turbellarian  worm  (Polycladida),  187 
Lepus.     The  genus  of  "  true  "  hare  :  Lagomorpha. 
L.  TiMiDus.     The  varying  hare. 
Lbvcosolesia.     a  sponge:    Porifera,  181 
LiGiA.     A  marine  isopod  crustacean,  95 

Lima.     An  active  bivalve  mollusc  which  swims  by  moving  its  shell-valves  and  mantle-lobes. 
LiMAX.     Grey  slug:    a  gastropod  mollusc  (Pulmonate),  197 

LiMs.Ei.     A  fresh-water  snail  (pond  snail):    a  gastropod  mollusc  (Pulmonate),  196 
LiMyESiA.     A  fresh-water  mite:    acarine  (Hydracarina). 
LiMVLCs  POLYPHEMUS.     X.  American  king-crab,  or  horseshoe  crab  :  an  arachnid  (Xiphosura), 

161,  211 
LiNEUS  RUBER.     An  aquatic  nemertine  worm,  189 
LiTHOBius.     A  centipede:    myriapod  (Chilopoda). 

LiTTORi.vA  yERiToiDES.     Periwinkle:    a  gastropod  mollusc  (Prosobranch),  45 
LizziA.     A  hydrozoan  coelenterate. 

Locust  A  migratoria.     The  migratory  locust,  or  grasshopper:    Orthoptera  (Acrididae),  69 
LoLiGo.     Common  squid:    a  dibranchiate  cephalopod  mollusc,  145 

LoPHORTTX  CALiFORsicus.     The  Califomian  valley  quail:  Galliformes  (pheasant  family),  417 
Loris  gracilis.     The  slender  loris:    a  nocturnal  lemuroid  primate. 
Lota.     The  burbot:    a  fresh-water  teleostean  fish  (cod  family:    Gadidse). 
Loxia.     The  cross-bill:    a  passerine  bird  (finch  family). 
Loxodosta  africana.     The  African  elephant:    Proboscidea. 
Lucifvga.     Cuban  blind  cave-fish:    a  teleostean  fish. 
Lvcioperca.     The  pike-perch:    a  teleostean  fish  (Percidae). 
LuMBRicuLUs.     An  earthworm:    oligochaete  worm. 

LvMBRicvs  terrestris.     The  common  earthworm:    oligochaete  worm,  190 
LuTiAyus.     The  snapper:    a  teleostean  fish  (sea-bass  family). 
LuTRA.     The  otter:    a  mustelid  carnivore. 
LuTREOLA.     The  mink:    a  mustelid  carnivore. 
LrcosA  AORicoLA.     Wolf-spider :   arachnid  (Araneida),  214 
LrcoTEVTHis    DiADEMA.     The    "wonder    lamp",    a   luminous,    deep-sea   squid:    dibranchiate 

cephalopod  molluse,  740 
LraoDACiTLUs.     A  gecko:    lacertilian  reptile  (Geckonidfe). 
LrMAyTRiA.     Tussock-moth:    a  lepidopterous  insect. 
LrTECHiyus.     Sea-urchin:    an  echinoderm  (Echinoidea). 

Mabufa.     a  genus  of  skink:    lacertilian  reptile  (Scincidae). 

Macaca  (Macacus).     Macaque  monkeys:    Old  World  monkeys  (Catarrhine). 


768  ZOOLOGICAL   GLOSSARY 

Maoaoa  pileata.     Toque  monkey. 

M.  RHESUS.     Rhesus  monkey. 

M.  BPEciosus.     Japanese  macaque. 

Macrobracujvm.     a  genus  of  fresh-water  shrimp:    decapod  crustacean. 

Macroolossa.     Hawk  moth:   lepidopterous  insect. 

Macronectes  GiGASTEUs.     Giant  fulmar:    a  sea-bird  (Procellariidse). 

MACROSCELiD.^.     The  elephant-shrew  family:  insectivores. 

MAGGOT.     The  larva  of  holometabolous  insects,  such  as  flies,  50 

Malacocephalus.     Grenadier:    deep-sea  teleostean  fish. 

MALACOSTRACA.^  A  sub-class  of  the  crustaceans,  comprising  the  Decapoda,  Amphipoda,  Isopoda, 

etc. 
Maloptervrus.     Electric  cat-fish:    siluroid  teleostean  fish. 
Malpolon.     a  genus  of  colubrid  snake:   reptile  (Ophidia). 
Manatus.     See  Trichechvs. 

Mandrillvs.     Mandrill:    Old  World  monkey  (Catarrhine). 

Mams.     The  pangolin,  or  scaly  ant-eater:   termite-eating  mammal  (Pholidota),  442 
Mantis  relioiosa.     The  praying  mantis:    an  orthopterous  insect  (Mantidae),  589 
Marmosa.     Mouse  opossum:   small  American  marsupial  (Didelphyidae). 
Marmota  {Arctomys).     Marmot:   member  of  the  squirrel  family  of  rodents,  4^/2 
Martes.     Marten:   mustelid  carnivore. 

Marthasterias.     a  genus  of  starfish :    echinoderm  (Echinoidea). 
Mastigoproctus  gigaxievs.     a  whip-tailed  scorpion:    an  arachnid  (Pedipalpi). 
MEDUSA.     Free-swimming  marine  jellyfish:   Scyphozoa. 
MEDUSOiD.     Free-swimming  form  of  Hydrozoa,  liberated  by  hydroid  colonies  ("  swimming 

bells  "). 
Meoabu.sus  diadema.     A  harvestman:    an  arachnid  (Phalangida). 
MEGACHiROPTERA.    A  sub-ordcr  of  Chiroptera  comprising  the  larger  bats,  usually  frugivorous, 

such  as  the  flying  foxes. 
Megalobatrachus  maximvs.     The  Japanese  giant  salamander,  the  largest  extant  amphibian: 

a  urodele,  349 
Megan rcTiPH AXES.     A  genus  of  deep-sea  luminous  shrimp:    decapod  cioistacean. 
Megaptera.     Hump-back  whale:    cetacean  (whale-bone  whale),  444 
Meoerlia.     a  genus  of  lamp-shell:    Brachiopod. 
Melanerpes  erythrocephalus.     Red-headed  woodpecker:    Picidae. 
Melanoplus.     American  migratory  locust:    orthopterous  insect  (Acrididae). 
Meleaoris  gallopavo.     The  American  turkey:    Galliformes  (pheasant  family). 
Meles  meles.     The  European  badger:    a  mustelid  carnivore,  444 

Melopsittacus  undulatus.     The  budgerigar,  an  Australian  parakeet:    Psittaciformes. 
Melvrsvs  vrsixvs.     The  Indian  sloth  bear:    a  carnivore  (Ursidae). 
Mephitis.     A  skunk:    mustelid  carnivore. 
metazoa:   The  sub-kingdom  of  multicellular  animals:   a  collective  name  for  all  animals  except 

Protozoa  and  Parazoa. 
Metopoceros  corxvtvs.     Horned  iguana  of  Haiti:    a  lacertilian  reptile. 
Metridwm.     a  genus  of  sea-anemone:    anthozoan  coelenterate. 
MiCROCHiROPTERA.     A  sub-order  of  Chiroptera  comprising  the  smaller  bats  (vampire  bat, 

Vespertilio,  etc.). 
Micrococcus  phosphoreus.     A  luminous  bacterium. 
MicROPUs  Apvs.     The  European  swift :   Apodidse  (Micropodidae),  r/()7 
Microspira  photogenic  a.     a  luminous  bacterium. 
Microtus.     a  field  vole:    myomorph  rodent. 
MiLvus.     A  kite:    bird-of-prey    (Falconiformes),  420 
MisGURNUs.     Loach:    cyprinoid  teleostean  fish,  310 

Mnemiopsis.     a  genus  of  luminous  comb-jelly:    a  coelenterate  (Ctenophora). 
MOBULiD.^.     Devil-fish  rays:  a  family  of  large  batoid  selachian  fishes. 
Mosodox.     Narwhal:    arctic  whale  of  the  family  Delphinidae,  the  male  of  which  has  a  long 

tusk  (sometimes  called  the  sea-unicorn). 
Mordacia.     a  genus  of  sea-lamprey  from  Chile  and  Tasmania:    a  cyclostome. 
MORMYRiD.*:.     The  elephant -fish  family  of  teleostean  fishes. 


ZOOLOGICAL   GLOSSARY  769 

MoTACiLLA  ALBA.     The  white  wagtail:    a  passerine  bird,  660 

MuoiL.     Grey  mullet:   teleostean  fish  (Mugilidse). 

MuREx.     A  genus  of  marine  gastropod  mollusc,  juice  from  the  glands  of  which  provided  the 

Tyrian  purple  dye  (Prosobranch),  197 
Mus  MuscuLVs.     The  house  mouse:   myomorph  rodent  (Muridae). 
MuscA  DOMESTicA.     The  house-fly:    a  dipterous  insect  (Muscidae),  172 
MvsTELA   ERMiSEA.     The  stoat  or  ermine   (in  its  winter  white)    (in   America,  a  weasel):    a 

mustelid  carnivore. 
M.  yiVALis.     The  weasel  (in  England),  472 
M.  puTORivs.     See  Pctorius  putorivs. 

MUSTELID^.     A  family  of  carnivores,  comprising  the  otter,  badger,  stoat,  skunk,  etc. 
MvsTELUs.     A  genus  of  dogfish  or  "  hound  ":    a  selachian  fish,  285 
Mta  A  res  ARIA.     The  long  clam:    a  bivalve  mollusc,  131 
Mtliobatis.     Eagle-ray:    batoid  selachian  fish,  283 
Mtocasior  corpus.      The    coypu:    a   South   American   aquatic   rodent,  the   fur  of  which  is 

"  nutria  "  (Hystricomorph). 
Mtooale.     Water-mole,  or  desman:    insectivore  (Talpidae). 
MYOMORPHA.     A  division  of  the  rodents  comprising  the  rat,  mouse,  vole,  etc. 
MYBiAPODA.     A  class  of  Aithropoda  comprising  the  Chilopoda  (centipedes)  and  Diplopoda 

(millipedes). 
Mfrmecobius.     Banded  ant-eater:    Australian  marsupial  (Dasyuridse),  437 
Mtrmecophaga.     The  giant  ant-eater:    South  American  mammal  (Xenarthra),  600 
MYSTACOCETi.     A  sub-order  of  Cetacea  comprising  the  baleen  or  whale-bone  whales. 
Mttilvs  EDVLis.     The  edible  mussel:    a  bivalve  mollusc,  200 
Mtxicola  ^sthetjca.     a  free-swimming  polychaete  worm. 
Mtxine  GLUTiyosA.     The  glutinous  hag-fish:   a  mud-dwelling  or  parasitic  cyclostome,    114, 

734 
Mrzus.     A  genus  of  aphid:   hemipterous  insect  (Aphididse). 

Naja  tripudiass.     The  Indian  cobra:    a  colubrid  snake  (Elapinae),  386 

Nasua.     The  coati:    American  carnivore  (Procyonidae),  444 

NAUPLius.     The  larval  stage  of  many  marine  crustaceans  [e.g.,  barnacles,  copepods,  etc.). 

Nautilus  pompilius.  The  pearly  nautilus:  the  only  extant  tetrabranchiate  cephalopod 
mollusc,  139 

Necrophorvs.     The  burying  beetle:    coleopterous  insect,  219 

Necturus.     Mud-puppy:    urodelan  amphibian  related  to  Proteus,  349 

NEMATODA.  A  phylum  of  unsegmented  worms  comprising  the  mainly  parasitic  round-  or 
thread-worms. 

NEMERTEA.  A  phj'luna  of  unsegmented  worms  comprising  the  mainly  marine  ribbon- 
worms. 

Nemestri.sus.     a  genus  of  macaque  monkey:    Primate  (Catarrhine). 

Neoceratodvs.     a  genus  of  lung-fish  of  Queensland:    dipnoan  fish,  312 

Neodiprio.v.     a  genus  of  saw-fly:    hymenopterous  insect  (Tenthredinidae). 

Nereis.     The  rag-worm:    free-swimming  polychaete  worm,  191 

NEtJROPTERA.     An  Order  of  insects  comprising  the  lace-wings,  ant-lions,  etc. 

Noctiluca.     a  genus  of  luminescent  dinoflagellate:    a  flagellate  protozoon,  179,  738 

NoTECHis.     Tiger  snake:  a  genus  of  crotalid  snake  (Elapidae). 

Notosecta.     Water-boatman,  or  water-bug:    a  genus  of  hemipterous  insect,  73 

NoTORTCTES  TTPHLOPs.     The  Australian  marsupial  mole,  437 

NoTROPis.     Shiner:  a  fresh-water  American  genus  of  cv'prinoid  teleostean  fish. 

NUDiBBANCHiA.     Sca-slugs:  an  order  of  gastropod  molluscs,  196 

NuiiiDA  PUCBERASi.     The  guinea-hen:    Galliformes  (pheasant  family). 

Ntcticebus.     Slow  loris:   lemuroid  primate. 

NrcTicoRAX.     The  night  heron:    Ciconiiformes,  413 

Ntctipithecvs  [Aotes).  The  night  monkey  or  Douroucouli:  American  nocturnal  monkey 
(Cebidae). 

NYMPH.  The  immature  stage  of  certain  insects  which  undergo  incomplete  metamorphosis 
(e.g.,  Orthoptera,  Hemiptera,  etc.). 

S.O.— VOL.  I.  49 


770  ZOOLOGICAL   GLOSSARY 

Obeli  A.     A  genus  of  marine  hydroid :   hydrozoan  ccelenterate,  152 

OcHoioNA.     The  pika,  or  calling  hare:    Lagomorpha. 

Octopus  vulgaris.     The  common  octopus:    a  dibranchiate  cephalopod  mollusc,  93,  202 

OcTDPODA  IPPENS.     The  racing  crab:    a  decapod  crustacean,  205 

ODONATA.     An  order  of  insects  comprising  the  dragonflies,  with  aquatic  larvae. 

ODONTOCETi.  A  sub-order  of  cetaceans  comprising  the  toothed  whales  (sperm-whale,  porpoise, 
dolphin,  etc.). 

Odostostllis.     The  fire-worm:    free-swimming  polychaete  worm. 

(EDicyEMUs.     Stone  curlew:    Charadriiformes. 

Ok  API  A.     The  okapi:   ruminant  of  the  giraffe  family. 

OLiGOCH^TES.     A  class  of  annelid  worms  comprising  the  earthworms,  etc. 

OycHiDiuM.     A  genus  of  pulmonate  mollusc. 

Oniscus.     a  woodlouse:   terrestrial  isopod  crustacean. 

ONYCHOPHORA.  A  class  of  Arthropoda  comjirising  the  caterpillar-like  Peripatus  and  its  rela- 
tives. 

Ophiops.     a  genus  of  lizard:    lacertilian  rejitile. 

Ophiotettix  limosina.     Grouse-locust:    an  orthopterous  insect,  223 

Ophisaurus  yentralis.     The  American  "  glass  snake  ":    a  lacertilian  reptile  (Anguidse). 

OPHiUROiDEA.     A  class  of  Echinodermata  comprising  the  brittle-stars. 

Ophryoessa  superciliosa.     The  Yrpha  iguana:    a  lacertilian  reptile. 

OPISTHOBRANCHIA.  An  Order  of  gastroiDod  molluscs  comprising  the  Nudibranchia,  sea-hares, 
etc. 

Opistuoproctus.     a  genus  of  deep-sea  teleostean  fish,  324 

Orca.     The  killer-whale:    a  genus  of  cetacean  (Delphinidae). 

Orectolobus.     The  carpet  shark:    selachian  fish. 

ORMTHORHYycHVs.     The  duck-billed  platypus:    Australian  monotreme,  430 

ORTHOPTERA.     An  Order  of  in.sects  comprising  the  cockroach,  stick-insect,  locust,  etc. 

Ortcteropus.     The  aard-vark:    a  mammal  (Tubulidentata),  442 

ORrcTOLAGUs.     The  rabbit:    Lagomorpha  (Leporidaj). 

OSTEICHTHYES.  The  class  of  bony  fishes,  including  the  Teleostei,  Chondrostei,  Dipnoi, 
etc. 

OsTEOL.EMUs  TETRAspis.     The  broad-fronted  crocodile:    a  reptile. 

OSTRACODA.     An  Order  of  small,  active,  mainly  fresh-water  crustaceans,  comprising  Cypris,  etc. 

Otus  BAKKAMCEyA.     The  Scops  owl:    Strigidse. 

Ovis.     Sheep:   Artiodactyl  (Bovidse). 

OxTBELis.     A  genus  of  tree-snake:    a  colubrid  snake. 

Pachi-dacttlus  maculatus.     a  gecko:    a  lacertilian  reptile  (Geckonidse). 

PAL.KMoy;     PAL.^MoysTEs.     Prawns:    decapod  crustaceans. 

Pax  sattbus.     The  chimpanzee:    an  anthropoid  ape. 

Pakdalus.     a  genus  of  deep-sea  prawn:   decapod  crustacean. 

PAyroDoy.     A  flying  fish  of  West  Africa:    a  teleostean  fish. 

Papio.     The  baboon  of  Africa:   catarrhine  monkey. 

PARACEyTRoius  LiviDvs.     A  sea-urchin:    an  echinoderm  (Echinoid). 

Paralichthys  albiouttus.     An  American  flounder:   teleostean  flat-fish  (Pleuronectidse). 

Param(ecium.     Slipper  animalcule:    a  genus  of  ciliate  Protozoa,  779 

PARAZOA.     A  sub-kingdom,  comprising  the  sponges,  in  contrast  to  Protozoa  and  Metazoa. 

Parus.     a  titmouse:    passerine  bird  (Paridse). 

Passer  domesticus.     The  hou.se  sparrow:    a  passerine  bird  (finch  family),  408 

PASSERiFORMES.     The  largest  order  of  birds  comprising  mainly  small  song  birds  and  birds  of 

perching  habits  (swallow,  thrush,  finch,  Corvidse,  etc.). 
Passerita  PRASiyA.     The  emerald  tree-snake:    a  colubrid  snake,  674 

Patella  vulgata.     The  common  European  limpet:    a  gastropod  mollusc   (Prosobratich),  197 
Pauropus.     a  genus  of  blind  myriapod  (Pauropoda). 
PECTEy.     The  scallop:    a  genus  of  bivalve  mollusc  which  swims  by  opening  and   closing  its 

shell-valves,  200 
PECTvycuLVs.     A  genus  of  bivalve  mollusc  of  the  family  Arcidae. 
Pedetes.     The  Cape  jumping  hare:    sciuromorph  rodent. 


ZOOLOGICAL   GLOSSARY  771 

Pediculvs.     Body-louse:    a  parasitic  insect  (Anoplura),  218 

PEDIPALPI.     An  order  of  Arachnida  comprising  the  whip-tailed  scorjiions. 

PelaQia  yociiLucA.     A  luminous  jellyfish:    a  ccslenterate  (Scyphozoa). 

PELECAyus.     The  pelican:    fish-eating  bird  (Pelecanidae),  410 

Pelobates  f  use  us.     The  European  spade-foot  toad:    a  burrowing  anuran  amphibian. 

Pelomtxa.     Amoeboid  protozoon:    Rhizopoda. 

Peraoale.     a  rabbit -bandicoot:    Australian  marsupial  (Peramelidse),  441 

Perameles.     A  bandicoot:    Australasian  marsupial  (Peramelidse). 

Perca  fluviatilis.     The  European  fresh-water  perch:    a  teleostean  fish  (Percidae). 

Perich.eta.     a  genus  of  annelid  worm  (Oligochaete). 

Periophthalmus.     The  mud-skipper,  amphibious  goby-fish:    a  teleostean  (Gobiidae),  326,  694 

Pbripaiopsis  alba,     a  South  African  relative  of  Peripatus. 

Peripatus.     a  genus  of  Onychophora:    a  nocturnal,  caterpillar-like  arthropod,  139,  204 

Periplaxeta.     An  American  cockroach:    orthopterous  insect  (Blattidse). 

PERISSODACTYLA.     Au  Order  of  mamnials  comjirising  the  odd-toed  ungulates — horse,    tapir, 

rhinoceros,  etc. 
Perms  aphorus.     The  honey-buzzard,  a  European  hawk:    bird-of-prey  (Falconiformes). 
Perodicticus  potto.     The  potto:    a  nocturnal  lemuroid  (Lorisida?),  607 
Petavrvs.     Flying  phalanger:    Australian  marsupial   (Phalangeridse). 
Petrogale.     Rock-wallaby:    Australian  marsupial  (Macropodidae). 
PETRoMrzos  MAR/yrs.     The  sea-lamprey:    a  cyclostome,  260,  716 
Phalacrocorax.     Cormorant:    aquatic  diving  bird  (Pelecaniformes),  404 
P.  BOUGAiyviLLii.     Peruvian  guano  cormorant. 
PuALAyGER   MACULATCS.       The  spotted  cuscus  (phalanger):    an  Australian  marsupial  (Phalan- 

geridse),  438. 
PHALANGERin.'E.      A    family    of   Australasian    marsupials    comprising    the    phalangers,    koala, 

wombat . 
PHALANGIDA.      An  Order  of  Arachnida,  comprising  the  small,  long-legged  "  harvestmen  ". 
Phascolarcius.     The  koala  or  native  bear:    Australian  marsupial  (Phalangeridae),  440 
Pbascolomys.     The  wombat:    Australian  marsupial  (Phalangerida?),  441 
Phexgodes.     Fire-beetle:    coleopterous  insect  (Cantharidae),  739 
PuiLAyTHus  TRiAyGULUM.     A  digger  wasp:    a  hymenopterous  insect  (Sphecidae). 
Phoca.     a  "  hair  "  seal:    pinnipede  (Phocidse). 
P.  barbata.     Bearded  seal. 

P.  GRKEyiAyDicA.     Common  arctic,  or  harp  seal. 
P.  viTVLiyA.     Common  (hai'bour)  seal,  502 
PaoceyA.     The  porpoi-se:   a  cetacean  (Delphinidae). 
PHOCiD^.     A  family  of  Pinnipedia  comprising  the  true  seals. 
PscsyjcoPTERUs.     The  flamingo:    long-necked  and  long-legged  wading  bird,  407 
Pholas.     a  genus  of  clam,  or  "  piddock  ":    a  wood-  or  rock-boring  bivalve  mollusc. 
PHOLIDOTA.     An  order  of  mammals  comprising  the  scaly  pangolins. 
Pholis.     Butter-fi.sli,  or  gunnel:   teleostean  fish. 

PuoTiyus.     A  genus  of  fire-fly  (or  glow-worm):  a  coleopterous  insect  (Lampyridae),  219 
PBoioBLEPHARoy.     Lamp-eyed  fish:    a  genus  of  luminous  teleostean  fish  (sea-bass  family). 
Photostomias  GUERyEi.     A  deep-sea,  luminous  teleostean  fish. 

Photurus  PEyysrLVAyicA.     An  American  fire-fly:    a  coleopterous  insect  (Lampyridffi). 
Phoxinvs.     A  genus  of  minnow^:    a  cyprinoid  teleostean  fish,  294 
PsRoyiMA  sEDEyTARiA.     An  amphipod  crustacean,  160 
PHRTyoMERUs.     A  gcnus  of  toad :    an  anuran  amphibian. 
PaRTyosoMA.     The  American  horned  "  toad  ":    iguanid  lizard,  365 
Phtllirrhce.      "  Flowing  leaf  ":    a  gastropod  mollusc  (Nudibranch). 

PHYLLOPODA.     A  sub-order  of  branchiopod  crustaceans,  comprising  Apus,  Artemia,  etc. 
PHYLLOKHrycHUs.     A  gcuus  of  colubrid  suakc :    an  ophidian. 
Phyllurus  milii.     a  gecko:    a  lacertilian  reptile  (Geckonidie). 
Physeter.     The  sperm  whale,  or  cachalot,  large  toothed  whale:    a  cetacean,  444 
PHYSJuyATHUs.     A  genus  of  water-dragon  of  Queensland  and  Cochin  China:  lacertilian  reptile. 
PiciD.«.     A  family  of  birds  comprising  the  woodpeckers,  flickers,  wrynecks. 
PiERis.     Cabbage  white  butterfly:    lepidopterous  insect. 


772  ZOOLOGICAL   GLOSSARY 

PINNIPEDIA.     A  sub-order  of  carnivores,  comprising  the  aquatic  seals,   sea-lions  and  walruses. 

PiPA  AMERICANA.     The  Surinam  toad:    an  anuran  amphibian,  339 

Pjscicola.     a  genus  of  leech:    annelid  worm  (Hirudinea). 

PiTBECiA.     Saki:    a  genus  of  platyrrhine  monkey  (Cebidse). 

PiTHECvs.     Langur,  of  India:    a  genus  of  catarrhine  monkey,  607 

PLACODEBMS.     An  extinct  class  of  fishes  with  an  armour  of  bony  plates,  234 

PLACOPHORA.     A  class  of  ancient,  marine  molluscs,  comprising  the  chitons. 

Plagiosiomvm.     a  genus  of  marine  flat -worm:    turbellarian  worm. 

PLANARIA.     A  group  of  elongated  flat-worms:   turbellarian  worms  (Tricladida). 

Planes.     A  genus  of  crab:    decapod  crustacean. 

PLATYHELMiNTHES.      A    phylum   of  unsegmonted   flat-worms,    comprising   Turbellaria,   Tre- 

matoda  and  Cestoda. 
PLATYRRHiNES.     The  New  World  monkeys  (Cebidse  and  Hapalidae). 
PLECOPTERA.     An  Order  of  insects  comprising  the  stone-flies,  218 
Plecostomus.     a  genus  of  catfish:    a  South  American  fresh-water  teleostean,  related  to  the 

siluroids. 
Plevrodeles.     a  genus  of  newt:   urodelan  amphibian. 
Pleuronectes  flesus.     The  flounder:    a  teleostean  flat-fish. 
P.  PL  AT  ESS  A.     The  plaice. 

Plexippus  siNVATus.     A  jumping  spider:    an  arachnid  (Araneida,  Salticidse),  212 
Plusia  oajuma.     Gamma  moth,  a  European  noctuid  moth:   lepidopterous  insect. 
Podargvs.     Frog-mouth:    an  Australian  bird,  related  to  goat -sucker. 
Polycelis.     a  genus  of  turbellarian  worm  (Tricladida). 
POLYCH^TES.     A  class  of  annelid  worms  comprising  free-swimming  types  (Errantia)  such  as 

Nereis,  and  tubicolous  types  (Sedentaria)  such  as  Branchio7)ima. 
POLYCLADiDA.     An  Order  of  leaf-like  Turbellaria,  comprising  such  types  as  Leptoplana. 
PoLTiPM's.     A  genus  of  deep-sea  stomiatid  teleostean  fish. 
PoLYODON.     Spoonbill  sturgeon  of  Mississippi:    a  chondrostean  fish. 
PoLYOPHTHALMUs.     A  gcuus  of  Sedentary  marine  polychsete  worm. 

Polypedates  (Rhacophorus)  rei.svvardti.     Javanese  flying  frog:    an  anuran  amphibian. 
Polyphemus.     A  genus  of  water-flea:    branchiopod  crustacean  (Cladocera),  209 
POLYPTERiNi.     A  group  of  African  chondrostean  fish  with  two  extant  genera. 
PoLYPTERVs.     The  bichir:    a  chondrostean  fish  (Polypterini),  320 

POLYZOA  (bryozoa).     A  phylum  of  aquatic,  plant-like  animals — sea-mats,  corallines,  194 
Pomolobus.     Skip-jack:    a  genus  of  clupeid  teleostean  fish. 
Poxao.     The  orang-utan:    anthropoid  ape. 
Pontellopsis  reoalis.     a  copepod  crustacean. 
Popillia.     a  Japanese  beetle:    coleopterous  insect. 
PoRicHTHYS.     Toadfish,  Californian  stinging  fish:    a  teleostean  fish. 
porifera.     a  phylum  of  multicellular,  sedentary,  aquatic  animals — the  sponges. 
PoRTHEsiA.     A  genus  of  tussock  moth:    lepidopterous  insect  (Lymantrid). 
PoRTuyvs.     Swimming  crab:    a  genus  of  decapod  crustacean. 
PoTAMiLLA.     A  genus  of  tubicolous  polychsete  worm. 
PoTAMoGALE.     Otter-shrcw:    aquatic  insectivore. 
PoucHETiA.     Dinofiagellate:    a  genus  of  flagellate  Protozoa. 
Pristis.     Saw-fish:  shark-like  batoid  selachian  fish,  279 
PROBOSCiDEA.     An  Order  of  mammals  comprising  the  elephants,   formerly  included  in  the 

Ungulata. 
Procavia.     Rock  hyrax  or  coney:    a  distant  relative  of  the  elephant  (Hyracoidea). 
P  ROC  ELL  ARIA  PELAGIC  A.     Storm    petrel    (Mother    Carey's    chickens):     an    oceanic    bird    (Pro- 

cellariidse),  420 
Proctacasthus.     Robber-fly:    a  genus  of  dipterous  insect. 

Procyox.     The  raccoon  of  North  America:    a  genus  of  Fissipedia  (Procyonidae),  444 
procyonidje.     a  family  of  carnivores,  comprising  the  raccoon,  panda,  coati,  etc. 
Propithecus.     Sifaka,  a  genus  of  Madagascar  lemur:    Primate  (Lemuroidea). 
PROSOBRANCHiA.     A  sub-class  of  gastrojiod  molluscs  comprising  the  aquatic  limpet,  whelk, 

periwinkle,  etc. 
Prosioma.     a  genus  of  fresh-water  ribbon-worm:   Nemertine. 


ZOOLOGICAL   GLOSSARY  773 

Proteus  Ayani.yus.     The  olm,  a  cave  salamander:    urodelan  amphibian,  726 
PROTOCHORDATES.      Primitive  chordates,  comprising  Hemichordata,  Tunicata  and   Cephalo- 

chordata. 
Protoptervs.     a  kmg-fish  of  West  Africa:    a  genus  of  dipnoan  fish,  312 
PROTOZOA.     A  phylum  comprising  the  lowest  and  simplest  unicellular  animals,  mainly  aquatic, 

such  as  Amoeba,  Euglena,  malaria  parasite,  etc. 
PROTUKA.     An  order  of  minute  insects,  lacking  wings,  eyes  and  antennae. 
PsEPHVRVs.      Sword-bill  sturgeon  found  in  the  Yangtze-Kiang,  China:  a  chondrostean  fi.sh. 
PsETTODES.     A  genus  of  flounder:    a  teleostean  flat-fish  (Pleuronectidse),  329 
PSEUDOSCORPiONiDEA.     An  Order  of  Arachnida  comprising  the  book-scorpions,  minute  aziimals 

resembling  scorpions  but  witliout  long  tail  and  sting. 
PsTLLA.     Jumping  plant-louse:    a  genus  of  hemipterous  insect. 
Pteraspis.     An  extinct  agnathous  fish,  234 

Pterocera  lambis.     Spider-  or  scorpion-shell:    a  gastropod  mollusc,  198 
Pterois.     Lion-fish  of  tropical  Pacific:    a  poi.sonous  teleostean  fish  (Scorpsenidse). 
Pteromts.     Flying  squirrel:   an  Asiatic  rodent  (Sciuridse). 

Pteropvs.     Flying  fox:    a  genus  of  fruit -eating  bat  (Megachiroptera),  442,  607. 
Pterotrachea.     A  shell-less  heteropod:    a  genus  of  gastropod  mollusc. 
Pttchodera.     a  balanoglossid:   hemichordate. 

PvFFiyvs  PVFFisvs.     Manx  shearwater:    an  oceanic  bird  (Procellariidae),  407 
PvLEX  IRRITASS.     The  human  flea:    a  blood-sucking  insect  (Aphaniptera),  219 
PULMONATA.     A  sub-class  of  gastropod  molluscs  comprising  the   terrestrial   snails   and   slugs 

and  fresh-water  snails. 
PuTORivs  FVRo.     The  ferret:    a  mustelid  carnivore. 
P.  pvTORius.     The  polecat,  444. 

PYCNOGONIDA.    An  Order  of  Arachnids  comprising  small  marine  animals — "  sea-spiders  ",  217 . 
Praopus    LEPiDOPVs.     Scale-footed    lizard:     a    snake-shaped    lizard    of   Australasia,    without 

forelimbs. 
Pfrophorus.     a  genus  of  fire-fly:    coleopterous  insect  (Elaterid). 
Ptrosoma.     a  luminous,  floating  colonial  tunicate  of  tropical  seas. 
Pyrrhvla.     Bullfinch:    a  genus  of  passerine  bird  (finch  family). 
Pythos.     Python:    a  genus  of  boid  snake. 
P.  MOLURVs.     Indian  python. 
P .  REGivs.     West  African  python. 
P.  reticplatus.     Reticulated  python  of  Malaya. 

RADIOLARIA.     An  Order  of  rhizopod  Protozoa  with  a  horny  or  siliceous  skeleton,  179 

Raja.     Ray:    a  genus  of  batoid  selachian  fish,  287 

R.  BATis.     The  skate. 

R.  CLAVATA.     Thornback  ray,  280 

R.  MoyxAGUi  {maculata).      Spotted  ray,  280 

Rasa.     The  common  genus  of  frog:    an  anuran  amphibian,  335 

R.  CATESBiASA.     BuU-frog. 

R.  EscuLEXTA.     Edible  water-frog. 

R.  piPiEss.     Leopard  frog,  342 

R.  TEMPORARiA.     Common  European  frog. 

Ranatra.     Water-scorpion:    a  genus  of  hemipterous  insect  (Nepid). 

Ranzama  truncata.     Truncated  sun-fish:    a  teleostean  fish. 

RATIT^  (PAL^OGNATH.^).      Running  birds,  such  as  kiwi,  ostrich,  emu,  etc. 

Rattvs.     Rat:    a  genus  of  myomorph  rodent  (Muridse). 

Rhacophorus  LEVcoMYSTAX.     Malayan   "flying"   tree-frog:     an  anuran  amphibian    (Ranidse). 

Rhamdia.     a  genus  of  cavernicolous  catfish:    siluroid  teleostean  fish. 

Rhea.     South  American  ostrich  or  rhea:    flightless  bird  (Ratitse),  410 

RniyEVRA  floridasa.     Florida  worm  lizard:    a  limbless  burrowing  reptile. 

RaiyocERos.     The  rhinoceros — a  large  perissodactyl  of  Asia  and  Africa,  444. 

Rhisoglexa.     a  wheel-animalcule — a  genus  of  rotifer. 

Rhixophis.     a  burrowing  snake  of  India:   a  genus  of  uropeltid  snake. 

RHIZOPODA  (sarcodina).     A  class  of  mainly  amoeboid  Protozoa. 


774  ZOOLOGICAL   GLOSSARY 

Rhytixa  (HrDRODAMALis)  sTELLARi.     Steller's  sea-cow:    an  extinct  sirenian. 

ROTiFERA.     A  phylum  of  beautiful,  microscopic,  aquatic  animals — wheel-animalcules,  194. 

RuTiLUS.     Roach:    a  genus  of  cyprinoid  teleostean  fish. 

Saccophartnx.     Gulper-eel:   a  deep-sea  teleostean  fish. 

Saccvlisa.      a  cirripede  parasitic  on  the  abdomen  of  crabs,  with  a  free-swimming  nauplius 

larva. 
Saoitta.     An  arrow-worm:    chaetognath,  194 
Salamaxdra.     a  genus  of  salamander:   urodelan  amphibian. 
S.  maculosa.     Spotted  salamander. 
Salmo  salar.     The  Atlantic  salmon:    a  teleostean  fish. 
S.  trutta.     River  or  brown  trout,  308 

SALMONiD^.     The  salmon-trout  family  of  teleosts,  with  a  few  deep-sea  forms  (Bathylagus,  etc.). 
Salpa.     a  free-swimming,  pelagic,  transparent  tunicate. 
Salticvs.     Jumping  spider:    an  arachnid  (Araneida,  Salticidse),  214 
Saxdalops.     a  genus  of  deep-sea  scjuid:    cephalopod  mollusc,  203 
Sapphirixa.     a  marine  planktonic  animal:    one  of  the  larger  copepod  crustaceans. 
Sarcophaua.     Flesh-fly:    a  dipterous  insect,  58 
Sarcophilvs.     Tasmanian  devil:    a  marsupial  (Dasyuridse),  438 

Sarcoptes  scAuiEi.     The  itch-mite:    a  parasitic  mite  causing  scabies  in  man  (Acarina),   216 
Sarsia.     Free  medusoid  form  of  a  hydrozoan  coelenterate,  139 
Saturxia  PERxri.     A  silk-moth:    lepidopterous  insect. 

Saxicola.     a  genus  of  passerine  bird  including  the  whinchat  (thrush  family),  417 
ScALOPS  AQUATicus.     An  American,  mainly  aquatic,  mole:    an  insectivore. 
ScAPHiopus.     American  spade-foot  toad:    an  anuran  amphibian. 
ScAPHiRHYxcHUs.     Shovel-nosed  sturgeon  of  North  America:    a  chondrostean  fish. 
SCAPHOPODA.     A  class  of  molluscs  with  cylindrical  shell,  which  burrow  in  the  sand — DentaUum, 

etc. 
ScELOPoRua.     A  lizard:    lacertilian  reptile. 

ScHisTOCERCA  GREGARiA.     Descrt  locust:    an  orthopterous  insect  (Acrididse). 
Schistosoma  h.ematobia.     The  parasitic  trematode  worm  causing  bilharzia,  187 
SCHIZOPODA.     An    order    of    Malacostraca    (crustaceans)    comprising   the   opossum  shrimps, 

mysids,  etc. 
SCiURiDvE.     A  family  of  rodents  comprising  the  squirrels,  marmot,  prairie-dog,  etc. 
sciUROMOBPHA.     A  division  of  rodents  comprising  the  squirrels,  beavers,  jumping  hares,  etc. 
SciuRus  vulgaris.     The  European  red  sciuirrel:    a  rodent. 
ScoLOPEXDRA  MORsiTAXs.     A  Centipede:   myriapod  (Chilopoda),  210 
SCOMBRID.^.     A  family  of  teleostean  fish  comprising  the  mackerel,  tunny,  etc. 
ScoPELARCHUs  AXALis.     A  decp-sea  teleostean  fish. 
ScoRP^xA.     Scorpion-fish:    a  poisonous  teleostean  fish,  302 
ScuTiGERA.     House  centipede:    a  genus  of  myriapod  (Chilopoda),  160 
Scy-LLioRHixus  CAXicuLA.     Europcau  spotted  dogfish:    a  selachian  fish,  280 
ScYLLiuM.     A  genus  of  dogfish:    selachian  fish. 
ScYMxus.     A  genus  of  shark:    selachian  fish. 
SCYPHOZOA.     A  class  of  ccelenterates,  comprising  the  jellyfish. 
SEDENTARIA.    A  division  of  polychsete  worms  comprising  the  tube-dwelling  (tubicolous)  forms, 

such  as  Branchiomma,  in  contrast  to  the  Errantia. 
Selache  maxima.     The  basking  shark:    a  selachian  fish,  283 
Semotilus.     Horned  dace  of  North  America:    a  cyprinoid  teleostean  fish. 
Sepia.     Cuttlefish:    a  dibranchiate  cephalopod  mollusc,  201 
Seps.     a  genus  of  skink:    lacertilian  reptile  (Scincidse). 

Sergestes  prehexsilis.     A  luminous  pelagic  shrimp:    decapod  crustacean. 
Serpextarius    cristatus.     The    African    secretary    bird:   a  bird-of-prey,   feeding  mainly  on 

reptiles  (Falconiformes),  413 
Serraxus.     Sea-bass,  or  sea-perch:    a  teleostean  fish,  693 
Sertularia.     a  hydrozoan  coelenterate. 
Si  A  LI  A.     Bluebird:    a  passerine  bird  (thrush  family). 
siLURiD^.     The  cat-fish  family  of  teleostean  fish. 


ZOOLOGICAL   GLOSSARY  775 

SiMEycHELYS  PARASITICA.      Snub-nosed  eel:     a  deep-sea  teleostean  fish,  some  species  of  which 

burrow  in  the  muscles  of  larger  fish. 
SiMocEPHALUS.     A  genus  of  water-flea:    branchiopod  crustacean  (Cladocera). 
SiPHOSOPs.     An  American  csecilian  amphibian. 

Sires.     Mud-eel:    a  North  American,  mud-burrowing  urodelan  amphibian. 
siRENiA.     An  order  of  aquatic  mammals,  comprising  the  sea-cows — manatee  and  dugong. 
SoLEA.     Dover  sole:  a  teleostean  flat-fish. 

SOLENOGASTRES.     A  class  of  molluscs  comprising  small  worm-like  animals  with  no  shell,  196 
SoLEyopsis.     Robber-ant:    a  genus  of  hymenopterous  insect  (Formicidse). 
SOLiruGvE.     An  order  of  arachnids  comprising  the  pugnacious,  nocturnal  jerrymanders. 
Spadella.     An  arrow-worm:    chaetognath,  194 
Spalax.     Mole-rat:    a  bm-rowing  myomorph  rodent. 
Sph.erodacttlus.     a  gecko:    lacertilian  reptile. 
Sph.eroma  lasceolata.     a  woodlouse:    an  isopod  crustacean,  206 
Spbemscus.     Jackass  penguin:    an  aquatic  bird  (Impennes). 
SpHESoDoy    pvycTATi'ff.     The    tuatara   of  New    Zealand:    the   only   extant   rhynchocephalian 

reptile,  379 
Sphtrxa  tibcro.     The  bonnet  shark:    a  selachian  fish,  327 
S.  ztOjExa.     The  hammerhead  shark,  327 

Spilotes  variboatus.     Diamond  python  of  Australia:    a  boid  snake,  384 
Spinachia.     Fifteen-spined  stickleback:   a  marine  teleostean  fish. 
Spirographis.     a  genus  of  marine  tubicolous  polychaete  worm. 
SposDrivs.     A  large,  usually  spinose,  bivah^e  mollusc,  201 
SqUALVS  ACASTHiAS.     Spiny  dogfish:    a  selachian  fish,  97 
SquATiNA.     Angel-shark,  monk-fish:    a  selachian  fish,  288 

Steatorms.     Oil  bird,  or  guacharo  of  South  America:    a  crepuscular  bird  (Coraciifornies). 
Stexostoxum.     a  genus  of  tubellarian  worm:    Rhabdoccele. 
Stentor.     a  trumpet -shaped  ciliate  protozoon:    Ciliophora,  179 
Stephanoa'etus.     Crowned  hawk  eagle:    a  bird-of-prey  (Falconiformes),  606 
Sterna  HiRuyoo.     Common  tern:    a  bird  of  the  gull  family,  419 
Stizostedios.     Pike-perch:    a  teleostean  fish  (Percidse). 
STREPSiPTERA.     An  Order  of  insects  comprising  bee-parasites,  such  as  Stijlops,  the  females  of 

which  are  parasitic  in  bees,  the  males  winged. 
Streptopelia  roseogrisea.     The  Barbary  turtle  dove:    Columbidfe,  398 
STRiGiD^.     The  owl  family  of  birds. 
SiRiyGops.     Owl-parrot:    Strigidse,  418 
Strix  aluco.     The  tawny  owl:    Strigidae. 
S.  FLAMMEA  [Trio  alba).     The  barn-  or  screech-owl. 
STRoyorLocEyTRoTUs.     A  sea-urchin:    echinoid  echinoderm. 
Struthio.     The  African  ostrich:    a  flightless  bird  (Ratitae),  405 
Sturnus  vulgaris.     The  common  Em-opean  starling:    a  passerine  bird  (Sturnidse). 
SrroicoLA.  A  Cuban  cave-fish:    a  fresh-water  teleostean  fish. 
Sttlaria  lacustris.     An  aquatic  oligochsete  worm. 
SmocHEiRoy  mastigophorvm.     An  abyssal  schizopod  crustacean,  160 
Sttlophorvs.     a  deep-sea  teleostean  fish,  322 

Sttlophthalmus  paradoxus.     The  stalk-eyed  larva  oi  Idiacaufhu-i,  q.v. 
Sttlops.     a  minute  bee-parasite:    an  insect  (Strepsiptera),  221 
SUCTORIA.     An  order  of  Protozoa  having  cilia  when  young;    the  adults  have  long  hollow 

"  tentacles  "  through  which  they  suck  the  protoplasm  of  their  prey,  179 
SUID,«.     The  pig  family  of  Artiodactyla,  comprising  the  pig,  boar,  wart-hog,  etc. 
Sula   BASSAyA.     The   common  North    Atlantic    gannet  :    an    aquatic,    fish-oating    bird    (Pele- 

caniformes),  407 
SUOiDEA.     A  sub-order  of  Artiodactyla  comprising  the  pig,  peccary  and  hippopotanrus  families. 
SuRicATA.     Suricate  of  South  Africa:   a  burrowing,  viverrine  carnivore,  allied  to  mongoose,  459 
Sus,     The  typical  genus  of  swine. 
S.  scROFA.     Wild  boar. 

Srcoy.     A  calcareous  sponge:    Porifera,  ISl 
SryAPTA.     A    sea-cucumber:    a  slender,   transparent,   burrowing    holothurian    (Echinoderm). 


776  ZOOLOGICAL   GLOSSARY 

Stnchmta.     a  genus  of  wheel-animalcule:    Botifer.  ' 

Stnonathus.     Pipe-fish:    a  teleostean  fish,  closely  related  to  sea-horse,  309 

Tabaxus.     Gadfly:    a  dipterous  insect  (Tabanidse),  219 

Tachtglossvs.     Echidna,  or  spiny  ant-eater  of  Austraha:    a  monotreme,  430. 

Tmnia  ECHiNococcvs.     A  tapeworm:    a  cestode,  187 

Talitrvs  saltator.     Sandhopper:    an  amphipod  crustacean,  61 

Talpa.     The  genus  of  true  moles:  an  insectivore. 

Tamjas.     Chipmvmk  of  North  America:    a  rodent  of  the  squirrel  family. 

Tapirvs.    Tapir:  shy,  water-loving  animals  of  Malaya  (T.  indicus)  and  America  (T.  terrestris): 

perissodactyl  (Tapiridse),  444 
Tarbophis.     a  colubrid  snake. 

TAREyioLA.     A  common  gecko  of  South  Mediterranean:    lacertilian  reptile. 
Tarsius.      The  tarsier,  a  small  lemur-like  animal  of  South-east  Asia  with  very  large  eyes: 

a  primate  (Tarsioidea),  442,  613 
Tautoqa  oxjTis.     Wrasse:    a  teleostean  fish  (Labridae). 
Tealia.     a  sea-anemone:    a  genus  of  anthozoan  coelenterate. 
Teqenaria  domestica.     The  common  house-spider:    an  arachnid  (Araneida),  214 
Texebrio.     a  beetle,  the  larvae  of  which  are  called  meal-worms:    a  coleopterous  insect. 
TESTUDiNiDiE.     The  family  of  chelonian  reptiles  comprising  the  true  tortoises. 
Testudo.     Land  tortoise,  including  the  giant  tortoises:    chelonian  reptiles. 
T.  CAROLiXA.     Box  tortoise. 
T.  ORAECA.     Greek  tortoise. 

Tetraqoxoptervs.     Bed-eyed  fish:    a  fresh-water  teleostean  fish. 
Tetraodox.     Puffer-fish,  or  globe-fish:    a  teleostean  fish. 

Thalassarctos  (Thalarctos)  maritimvs.     The  Arctic  polar  bear:   a  carnivore  (Ursidae). 
Thaumatops  magna.     The  "  wondrous-eyed  hopper  ":    an  amphipod  crustacean,  207 
Thelotorxis.     African  bird  snake:    a  colubrid  snake. 
Thuxxus.     Tunny:    a  teleostean  fish  (mackerel  family),  294 
Thtlacixvs.     Tasmanian  wolf:    a  marsupial  (Dasyuridae). 
THYSAKOPTERA.     An  Order  of  insects  comprising  the  small  thrips. 

THYSANURA.     An  Order  of  primitive  wingless  insects,  the  bristletails,  such  as  Lepisma. 
ToMOPTERis.     A  genus  of  free-swimming  polychaete  worm. 
TORNARiA.     The  larval  form  of  Hemichordata  {e.g.,  Balanoglossus). 
Torpedo.     Electric  ray:    a  selachian  fish,  281 

ToxoTES  JACULATOR.     Archer-fish:    a  fresh-water  teleostean  fish  of  East  Indies,  701 
Tracbixus.     Weever:    a  marine  teleostean  fish. 
Trachycepbalus.     a  genus  of  anuran  amphibian. 

Tracbtsauru!^.     Australian  skink:    a  lacertilian  reptile  (Scincidae),  682 
TRAGULiNA.     A  sub-order  of  Artiodactyla  comprising  the  small,  deer-like  chevrotains. 
TREMATODA.     A  class  of  flat-worms,  comprising  the  endo-  or  ectoparasitic  flukes,  such  as  the 

liver-fluke. 
Triakis.     Leopard  shark:    a  selachian  fish. 
Tricbecbus.     Manatee:    a  sirenian  mammal,  502 
TRiCHOMONADS.     Pear-shapcd  flagellate  protozoa,  common  in  digestive  tracts  of  vertebrates, 

179 
TRiCHOPTERA.     An  Order  of  insects  comprising  the  moth-like  caddis-flies,  with  aquatic  larvae. 
Tricbosvrvs  vulpecula.     Vulpine  phalanger,  an  Australian  brush-tailed  opossum:    a  marsupial 

(Phalangeridae) . 
TRICLADIDA.     An  Order  of  turbellarian  worms,  comprising  such  types  as  the  planarians,  Den- 

droccelurn,  etc. 
Trigla.     Gurnard:   marine  teleostean  fish. 
TRILOBITES.     A  class  of  extinct.  marine  arthropods,  157 
Trixotox  aculeatvm.     A  bird-louse:     a  small  biting   insect   (Anoplura). 
Tristomum  papillosum.     An  aquatic  trematode  worm,  ectoparasitic  on  fishes. 
Tritox;  Tritvrvh.     A  genus  of  aquatic  salamander  or  newt:    urodelan  amphibian,  346 
T.  CRisTATVs.     Crested  newt,  347 
T.  PTRRBOGASTER.     A  spccics  from  China  and  Japan. 


ZOOLOGICAL   GLOSSARY  777 

Triton  torosus.     Californian  newt. 

Troolichthts   ros.e.     a  cave-fish  from  American  rivers:    a  teleostean   (Amblyopsidse). 

Troilus.     Shield-bug:    a  genus  of  hemipterous  insect. 

Tropidoxotus.     a  genus  of  non-poisonous  colubrid  snake:    Ophidia. 

T.  FASciATus.     A  water-snake. 

T.  MATRIX  SATRix.     Common  European  grass-snake,  384 

Trfoos  (Dastatis).     Sting-ray:   a  genus  of  batoid  selachian  fish,  285 

Trtgosorhixa.     Fiddler-ray:    an  Australian  geniis  of  batoid  selachian  fish. 

TRYPANOSOMES.      Flagellate  protozoa,  mainly  parasitic  in  blood  of  higher  vertebrates,  179 

TRTPAUCHEy;  TRTPArcHEyoPHRrs.     Crevice-dwelling  goby-fishes:    teleosteans  (Gobiidae). 

TUBXJLIDENTATA.     An  Order  of  mammals,  comprising  the  nocturnal,  termite-eating  aard-varks. 

TuPAiA.     Oriental    tree-shrew,   a   small,    squirrel-like    mammal,    formerly    classed    with    the 

insectivores  but  recently  thought  to  be  more  nearly  related  to  the  lemurs,  442 
Tupi-VAMRis  yiQROPvycTATUS.     Blackpointed  "  teju  ":    an  American  lizard  (Tejidse). 
TURBELLARiA.     A  class  of  unsegmented  worms,  usually  leaf-like,  living  either  in  water  or  moist 

surroundings  on  land. 
TuRDus  MiGRAioRivs.     American   "robin",   a  migratory  thrush:    passerine  bird  (Turdidae). 
T.  viscivoRUs.     Mistletoe  or  missel  thrush,  402 
TuRRis.     Hydromedusa:    a  genus  of  hydrozoan  ccelenterate. 
TYLOPODA.     A  sub-order  of  Artiodactyla,   comprising  the   camel  and  dromedary,   and   the 

llama. 
TrPHLACHiRVs.     Blind  sole:    teleostean  flat-fish. 
TrPHLMoyiiAS.     A  genus  of  lizard:    lacertilian  reptile. 
TrPHLiAS.     A  genus  of  Cuban  cave-fish:    teleostean  fish. 

Ttphlichthts  svBTF.RRAyEUs.     A  cave-fish  from  American  rivers:  a  teleostean  (Amblyopsidse). 
TrPHLoriROLAyA.     A  small  cave-dwelling  genus  of  isopod  crustacean. 
Ttphlogobius  CALiFORyiEysis.     The  blind   goby:     a  very  small  teleostean  living  like  a  slug 

under  rocks  on  Californian  coasts. 
Ttphlomoloe.     Blind  colourless  salamander,   retaining  larval  form  throughout  life,   foimd  in 

underground  streams  in  Texas:  a  urodelan  amphibian,  allied  to  Proteus. 
TrPHLoyARKE.     Deep-sea  ray:    batoid  selachian. 
TrPHioypcTES.     American  aquatic  csecilian  amphibian. 
TrPHLoyvs.     Blind,  deep-sea,  blenny-like  fish:    a  teleostean. 
Ttphloperipatus.     a  blind  relative  of  Peripatus  found  in  Tibet:    Onychophore. 
TrPHLOPS.     A  genus  of  blind  burrowing  snake:    Typhlopidae. 
TrPBLOTRiToy.     Blind  cave-salamander:    urodelan  amphibian. 

Uca.     Fiddler-crab:    decapod  crustacean. 

Umbra.     Mud-fish:    fresh-water  teleostean  (pike  family). 

XJNGULATA.  Hoofed  animals:  a  former  division  of  mammals,  now  separated  into  four  orders — 
Artio-  and  Perissodactyla,  Hyracoidea  and  Proboscidea. 

UpAyoscopus.     Stargazer:    spiny-rayed  marine  teleostean  fish  from  tropical  seas. 

TJROCHORDATA  (Tunicata).  A  sub-phylum  of  marine  chordates,  comprising  fixed  and  free- 
swimming  forms,  such  as  sea-squirts  (Ascidians). 

URODELA  (Caudata).     An  order  of  amphibians,  comprising  tailed  newts  and  salamanders. 

Uromacer.     a  genus  of  colubrid  snake. 

XJRSiD^.      The  bear  family  of  carnivores. 

Vanadis.     Free-swimming  pelagic  polychaete  worm  (relative  of  Alciopa). 

Vanessa.     Genus  of  butterfly,    including  red   admiral,   peacock,   etc.:     lepidopterous   insect, 

170 
VARAyus.     Monitor:    a  genus  of  lizard  of  Africa,  Asia  and  Australia. 

VEyus  MERCEyARiA.     The  round  clam,  or  quahog,  of  North  America:  a  marine  bivalve  mollusc. 
Vermilia  lyFuyDiBULUM.     A  tubicolous  polychaete  worm. 
Vespa.     a   genus   of  social   wasps    (including   hornets):    hymenopterous   insect    (Vespidae), 

219 
Vespertilio.     a  genus  of  bat  of  world-wide  distribution:    Microchiroptera. 
ViPERA  BERUs.     Common  European  viper,  or  adder:    a  poisonous  snake  (Viperidse). 


778  ZOOLOGICAL   GLOSSARY 

viVEBRiD^.     A  family  of  carnivores  comprising  the  civets,  genets,  and  mongooses. 

Vol  vox.  An  actively  motile  colony  of  flagellate  protozoa,  found  in  fresh-water  pools:  some- 
times classed  as  a  green  alga,  179 

VoRTicELLA.  Bell-animalcule:  ciliate  protozoon  which  grows  on  the  stems  of  fresh-water  plants, 
179 

VuLPEs  vuLPES.     The  common  fox:    a  carnivore  (Canidae). 

WALCKEy\ERA  AcuMisATA.     A  spccics  of  Spider :    an  arachnid  (Araneida). 
WixTERiA.     A  deep-sea  teleostean  fish. 

Xanthvsia.     Mexican  night-lizard:    a  lacertilian. 

XENARTHBA.     An  Order  of  mammals  comprising  the  sloths,  ant-eaters  and  armadillos. 

Xenopvs  l^vis.     The  African  clawed  toad:    an  aquatic  anuran  amphibian,  337 

Xerus.     African  ground  squirrel:    a  rodent  (Sciuridse). 

Xiphias  OLADivs.     The  sword-fish:    a  teleostean  (relative  of  mackerel  family),  294 

xiPHOSURA.     An  order  of  arachnids  comprising  the  king-crabs  {Limulus,  etc.). 

Zaglossvs.     a  relative  of  the  echidna,  found  in  New  Guinea:    a  monotreme. 

Zamems.     a  genus  of  colubrid  snake  including  the  rat-snake  of  India  and  the  American 

black  snake:    Ophidia. 
Zesaidura    macroura.     The   mourning  dove  of  America,  so  called  because  of  its   plaintive 

note:    Columbidae. 
Zesiox.     Deep-sea  teleostean  fish  (relative  of  the  John  Dory). 
ZoyosAURus.     Malagasy  lizard:    lacertilian  reptile. 

ZoNURVs  GioANTEUs.     Great  girdled  lizard  of  Africa:    lacertilian  reptile. 
ZORAPTERA.     An  Order  of  minute  insects,  resembling  termites. 
ZosTEROPx  jAPOxivA.     Japanese  white-eye:    a  passerine  bird. 


INDEX 


The  figures  in  bold  face  type  indicate  the  number  of  a  page  containing  an 

ilhistration  in  the  text;  those  in  italics  indicate  the  number  of  a  page 

showing  a  marginal  illustration. 


Aard-vark,  442,  445 

cornea,  keratinized,  456 
nictitating  membrane,  493 
pupil,  472 
Ablepharus,  secondary  spectacle,  366,  367 
Abyssal  habit,  degenerate  eyes  due  to,  722 
Acanthephyra,  bioluminescence  in,  742,743 
Acarines,  216 
eyes  of,  216 
vision  of,  579 
Accipiter,  Miiller's  ciliary  muscle,  406 

orbit,  423 
Accommodation  in  invertebrates,  590 
in  vertebrates,  640 
amjahibians,  647 
ainphibious  animals,  654 
birds,  651 

chelonians,  651,  652 
crocodilians,  651 
cyclostomes,  644 
lacertilians,  651 
mammals,  652,  653 
sauropsidans,  649,  650 
selachians,  647 
snakes,  648 
teleosts,  645,  646 
dynamic,  644 
muscle  of,  in  Alciopa,  591 
in  cephalopods,  590 
in  snakes,  387 
See  also  Ciliary  muscles, 
pecten  and.  416 
static,  640 

structure  of  retina  and,  656 
Acerentomon,  218 
Achias  rothschildi,  223 
Acholoe,  bioluminescence  in,  742,  744 
Acilius  larva,  tlermal  sensitivity,   114 

eye  and  cerebral  ganglion,  519 
Acipenser,  315 

anterior  chamber,  319 
choroid,  319 


Acipenser 

median  eye,  713 
pupil,  317 
fulvescens,  visual  cells,  320 
ruthenus,  317 

eye,  318 
sturio,  eye,  275 
Acnidaria,  182 

See  also   Coelenterates,    Comb-jellies. 
Acone  eye,  167 

Acrania.     See  Cephalochordata. 
Acrida  turrita,  colour  changes  in,  94 
Acrobates.    See  Flying  phalanger. 
Actinia,  phototactic  reactions  of,  571 
Actinopterygii,  234,  235 
Acuity  of  vision.     See  Visual  acuity. 
Adiposo -genital  dystrophy,  560 
Adrenal  gland,  hormones  and,  550 
Aedes,  scototaxis  in,  60 
Aegd,  telotaxis  in,  56 
Aeglina  prisca,  157 

eyes  of,  157 
Aeschna,  225 

larvae,  optic  ganglia,  activity  of,  524 
optomotor  response  of,  589 
calif oniica,  222 
Esthetes,  in  Chiton,  196 
Agama  agama,  359 
iris,  359,  PI.  V 
Agaricus  olearius,  bioluminescence  in,  737 
Aggregate  eyes,  151 
Agnatha,  233 

jiineal  organ  in,  713 
See  also  Cyclostomes. 
Agwantibo,  443 

See  also  Lemuroids,  Priniates. 
AhcetuUa  picta,  iris,  387 
Alaurina  prolifera,  ocelli  of,  188 
Alburnus,  colour  preference  in,  624 
lucidus,  migration  of  pigment  in,  615 
visual  pigments,  121 
Alcedo,  417 

bifoveate  retina,  417 
vision  of,  641,  655 


780 


INDEX 


Alciopa,  192 

accommodation  in,  591 
ocelli  of,  143,  192 
Alligator,  375 
brain,  533 
visual  acuity,  665 
field,  binocular,  682 
chinensis,  fundus,  PI.  VIII 
mississippiensis,  visual  cells,  377 
Allolohophora,  conditioning  of,  573 
Alouatta.     See  Monkey,  howling. 
Alytes  obstetricans,  334 

colour  blindness  of,  628 
pupil  of,  339 
Amhlyomma  pomposum,  217 
Amblyopsidse,  725 
Amhlyopsis,  degenerate  eyes  in,  726 
Amblyrhynchus  cristahis,  356 
Ambystoma  tigrinum,  334,  346 
eyes  of,  346,  728 
larva.     See  Axolotl. 
Ameiurus,  307 

colour  changes  in,  97 
eyes  of,  725 

larvae,  phototaxis  in,  46 
optic  nerve,  310 
visual  cells,  307 

migration  of,  616 
Amia,  279,  321 

choroidal  gland,  321 
colour  vision  in,  624 
cornea,  295 
eye  of,  276,  321 
median  eye  of,  713 
visual  cells,  321 

migration  of,  614 
Ammocoetes,  92,  260 
colour  changes  in,  92 
eyes  of,  261 

light-sensitive  cells  in  tail,  132,  263 
median  eye  of,  717 
optic  nerve,  270 
Amtnomanes,  camouflage  in.  83 
Ammophila,  mnemotaxis  in,  79 
Amoeba  proteus,  179,  180 

diffuse  sensitivity  of,  113 
photokinesis  in,  35 
Amphibians,  333 

accommodation  in,  647 
brain,  533 

transection  of,  534 
ciliary  ganglion,  501 
cochlea,  534 


Amphibians,  colour  changes  in,  82 
control  of,  97,  558 
mechanism  of,  86 
pineal  organ  and,  719 
rhythmic,  20 
colour  vision  in,  627 
ojitomotor  reaction  and,  623 
dermatoptic  sensitivity  of,  32 
eyes  of,  334  j^. 

degenerate,  726,  730 
fore-brain,  543 

removal  of,  545 
iris,  contraction  to  light,  89 
lateral  geniculate  body,  541 
mid-brain,  535 
migration  of  retinal  pigment,  614 

visual  cells,  616 
movement,  perception  of,  705 
neuro -endocrine  system,  557 
nocturnality  of,  603 
ocular  movements  of,  694 
optic  thalamvis,  540 
pineal  apparatus,  714 

function  of,  719 
primitive,  234,  235 
pupillary  reactions,  89,  700 
refraction  of,  638 
reproductive  cycle  in,  17 
rods,  thickening  of,  611 
spatial  judgiuent  of,  702 
tectum,  534 
telencephalon,  543 
vision  of,  599 
visual  acuity  of,  661 
field,  binocular.  682 
pathways  of,  537,  544 
I^igments  of,  121 
See  also  Anurans,  Cfecilians,  Urodeles. 
Amphibious  eyes  in  fishes,  324 

vertebrates,  accommodation  in,  654 
duplicated  optical  system,  641 
Amphioxus,  229 

cells  of  Joseph,  229 
infundibular  organ,  229 
nerve-cord,  239^  530 
nervous  system,  530 
organs  of  Hesse,  230 
vertebrate  eye  developed  from,  244 
Amphiporus,  189 

ocelli  of,  189 
Amphisbcena  punctata,  degenerate  eyes  of, 

733 
Amphisbaenidse,  733 


INDEX 


781 


Amphisbsenidse,  degenerate  eyes  of,  733 
AmphitretMS,  203 

tubular  eyes  of,  203 
Amphimna,  349 

eyes  of,  349 
Anahas,  accommodation  in,  654 
Anableps  tetrophthalmus,  325 
ciliary  processes,  301 
eyes  of,  324,  326 

optics,  642 
vision  of,  641,  655 
Anangiotic  retina,  480 
Anax,  dorsal  light  reaction  in,  74 

optomotor  response,  589 
Ancala  fasciata,  eyes  of,  222 
Angle  gainma,  673 

in  vertebrates,  676,  677 
Anguilla,  46 

colour  changes  in,  96 
cornea,  295 
growth  of  eye  of,  273 
migration  of  rods,  614 
optic  nerve  of,  311 
phototaxis  in,  46 
retinal  vascularization,  300 
viveal  tract,  299 
Anguis  fragilis,  363 

colour  vision  in,  629 

conus,  363 

parietal  eye,  715,  718 

function  of,  719 
visual  field,  binocular,  682 
Amelia,  visual  cells  of,  364 
Annelids,  190 

dermal  sensitivity  in,  114 
eyes  of,  190 
light-sense  in,  572 
nerve-net,  516 
nervous  system,  519,  520 
neuro -endocrine  system,  550,  552 
See    also    Polychsetes,     Oligochsetes, 
Leeches. 
Annular  ligament,  characteristics  in 
chondrosteans,  317 
holosteans,  321 
lamprey,  267 
teleosteans,  295 
pad,  characteristics  in 
birds,  409 
chelonians,  372 
crocodilians,  377 
lacertilians,  360,  361 
marsupials,  439 


Annular  pad,  characteristics  in 
monotremes,  436 
snakes,  389 
Sphenodon,  381 
accommodation  and,  649,  650 
Anodonta,  201 

dermal  sensitivity  in,  114,  574 
eyes  absent  in,  201,  722 
Anolis,  361 

bifoveate  retina,  365,  366 
colour  changes  in,  87,  98,  105 
control  of,  558 
rhythmic,  20 
vision  of,  629 
parietal  eye,  717 
transparent  eyelids,  366 
alligator,  eyelids,  366 
fundus,  361,  PI.  VI 
argenteolus,  eyelids,  367 
carolinensis,  reproductive  cycle  in,  17 
lucius,  eyelids,  367 
Anomalops  katoptron,  luminous  organ  in, 

737,  738 
Anopheles,  scototaxis  in,  60 
Anophthalmus,  dermal  sensitivity  in,  114 

eyes  lacking  in,  724 
Anoplura,  218,  220 
eyes  of,  221 
See,  also  Pediculus. 
Anoptichthys  jorduni,  degenerate  eyes  in, 

725 
Anser,  brain,  533 
Anseriformes,  annular  jaad,  409 
infula,  417 
pecten,  412,  414 
See  also  Ducks,  Cereopsis,  etc. 
Ant,  219 

eyeless  types,  729 
homing  of,  68 
menotaxis  in,  68 
ocelli,  224 
time-memory  in,  22 
vision  of,  582,  585 
white.     See  Termites. 
Ant-eaters,  445 
banded,  437 
vision  of,  601 
giant,  600 

spiny.     See  Echidna. 
Antelope,  446 

Anterior  chamber  angle,  characteristics  in 
birds,  404,  405 
chelonians,  372 


782 


INDEX 


Anterior  chamber  angle,  characteristics  in 
chondrosteans,  317,  319 
coelacanth,  315 
crocodilians,  376 
dipnoans,  313 
holosteans,  321 
lacertilians,  359 
marsupials,  439 
placentals,  464,  465 
selachians,  285 
snakes,  386 
Sphenodon,  380,  381 
teleosts,  303 
urodeles,  347 
pad  of  lens,  in  snakes,  389 
Antholoha,  phototactic  reaction  of,  571 
Anthozoa,  182 

See  also  Sea-anemone,  Coelenterates. 
Anthrohia,  eyes  lacking  in,  724 
Anthropoidea,  443 
area  centralis,  485 
colour  vision  in,  635 
diurnal,  604 
fovea,  659 

nocturnal.     See  Nyctipithecus. 
optic  axis,  688 
orbit,  498 

visual  field,  binocular,  689 
See  also  Apes,  Primates. 
Antilocapra.     See  Pronghorn. 
Anurans,  334 

accomniodation  in,  648 

colour  vision  in,  627 

eyes  of,  ZMff.,  336,  PI.  Ill 

lateral  line  organs,  534 

migration  of  retinal  pigment,  614 

visual  cells,  616 
ocular  movements  in,  694 
pineal  organ,  714 
refraction  of,  638 
vision  of,  599 
visual  acuity  of,  661 

field,  binocular,  682 
Seealso  Hyla,  Rana,  Xenopiis,  etc. 
Apes,  anthropoid,  443 

ciliary  region,  461,  463 
Harder 's  gland,  494 
Moll's  gland,  492 
pectinate  ligament,  464 
vision  of,  602 
colour,  635 
visual  field,  binocular,  689 
See  also  Primates,  Chimpanzee,  etc. 


Aphaniptera,  219,  220 
Aphid,  225 

eyes  of,  224,  225 
Aphis  forbesi,   reproductive   cycle   in,    17 
Aphrophora    spumaria    larva,    ocellus    of, 

140 
Aphyonus,  degenerate  eyes  of,  724 
Apis,  58 

colour  vision  in,  587,  588 
conditioning  of,  583,  588 
cornea,  transparency  of,  584 
luminosity-curve  of,  585 
ommatidial  angle  of,  172,  173 
orientation   to   jDolarized   light,    66,    70 
spectral  sensitivity  of,  585 
telotaxis  in,  56,  58 
vision  of,  584,  585 
Aplocheilichthys,  iris,  PI.  II 
Apoda,  333 

eyes,  rudimentary,  of,  730 
pineal  organ,  714 
vision  of,  599 
Apodernus.    See  Mouse,  field- 
Apposition  eye,  169,  173 
Apteryx,  397,  398,  604 
annular  pad,  409 
extinction  of,  604 
eyes  of,  401 
fundus,  410,  PI.  XII 
pecten,  411,  413,  414 
refraction  of,  639 
Apus  (Triops),  76,  208 

dorsal  light  reaction  in,  75 
eyes  of,  209 
Aquatic  placentals,  502 
choroid,  457 

keratinization  of  cornea,  456 
lacrimal  passages  absent,  494 
lens,  474 

ocular  adnexa,  501 
sclera,  450 
shape  of  eye,  -448 
sphincter  muscle,  468 
See  also  Cetaceans,  Pinnipedes,  etc. 
vertebrates,  lateral  line,  534 
Aqueous   humour,   drainage  of,  in  mam- 
mals, 472 
origin  of,  in  cyclostomes  and  fishes, 
267 
Arachnids,  211 
eyes  of,  211 

compound,  160 
inverted  retinae  in,  149 


I 


INDEX 


783 


Arachnids,  luminous  organs  in,  740 
neuro -endocrine  system,  552 
vision  of,  579 
visual  centres,  524 
Araneida,  213 
eyes  of,  213 
nervous  system,  521 
vision  of,  579,  591 
Araneus  diadematus,  214 

eyes  of,  213 
Area,  eyes  of,  151,  201 

light -shadow  reflex  in,  574 
Archiannelids,  190,  193 

ocelli  of,  193 
Archicortex,  543 
Archistoma,  eyes  of,  221 
Arctocebiis.     See  Agwantibo. 
Ardea,  404 

goliath,  binocular  vision,  675 
Area  centralis,  characteristics  in 
anurans,  342 
birds,  417 
chelonians,  374 
crocodilians,  377 
lacertilians,  365 
placentals,  485 
selachians,  288,  289 
teleosts,  309 
function  of,  657 
occurrence  of,  657 
Arenicola  marina,  190 
diffuse  sensitivity  of,  191 
eyes  lacking  in,  729 
larva,  tropotaxis  in,  52 
visvial  pigment  in,  120 
Argentea,  characteristics  in 
chondrosteans,  317 
holosteans,  321 
lamprey,  267 
Latimeria,  315 
selachians,  285 
teleosts,  296 
function  of,  296 
Argyropelecus,  322 

eyes  of,  tubular,  323.  324 
luminous  organs,  741 
rods,  lengthening  of,  611 
Arhythmic  animals,  603 

eye,  characteristics  of,  612 
Ariolimax,    optic    ganglia,    activity    of, 

524 
Aristelliger,  triple  cones  in,  308,  364 
Aristeomorpha,  photopigments  in,   121 


A  rniad  ill  id  i urn ,  4  5 

tropotaxis  in,  54 

alteration  of  resjionse,  45 
Armadillo,  442,  445 

cornea,  keratinized,  456 

pineal  body  absent  ,711 

retina,  jjure-rod,  610 

visual  cells,  482 
Arrow-worms,  194 

See  also  Sagitta,  Spadella. 
Artemia,  207 

dorsal  light  reaction  in,  75 
Arteria  anastomotica  in  placentals,  498, 

499,  500 
Artery,  central  retinal,  477 
Arthrojiods,  204 

blind,  729 

cerebral  ganglion,  521 
activity  of,  524 
function  of,  524 

eyes  of,  204j^. 

degenerate,  724,  729 

luminous  organs  in,  740,  746 

nervous  system,  521 

neuro -endocrine  system,  550,  552 

vision  of,  577 

^ee  cdso  Insects,  Crustaceans,  etc. 
Artiodactyla,  445 

area  centralis,  485 

orbit,  497 

I^upil,  472 

See  also  Pig,  Deer,  etc. 
Ascaris,  187,  190 
Ascidia,  228 

larva,  228 
Ascidians.  228 

bioluminescence  in,  740 

eyes  of,  228 

larvse,  eyes  of,  228 

nervous  system,  519,  530 
vertebrate  eye  developed  from,   245 

nervous  system,  519,  530 

neuro-endocrine  systeni,  552 
Asellus,  207 

conditioning  of,  579 

eyes  lacking  in,  207,  722 
Asio,  infra-red  rays  and,  630 
Asplanchna,  dermatoptic  sensitivity  in,  32 
Ass  {Eqnus  asinus),  446 

corneal  epithelium,  452 

corpora  nigra,  469 

extra-ocular  muscles,  495 

nictitating  membrane,  493 


784 


INDEX 


Ass,  Somali  wild,  686 

See  also  Equidae 
Astacus,  164 

eyes  of,  164 

nervous  system,  521 
Astaxanthin,  120 

absorption  spectrum  of,  120 

in  Euglena,  48 
Asterias,  185 

phototactic  reaction  of,  571 

visual  organs  of,  185 
Asteroidea,  184 

See  also  Starfishes. 
Astroscopus,  751 

electric  organ  of,  751,  752 

sclera,  292 

visual  field,  binocular,  680 
Astur  palumbarius,  403 
ciliary  region,  406 
scleral  ossicles,  403 
Ateles.     See  Monkey,  spider. 
Atherina,  617 

colour  preference  in,  625 

threshold  to  light,  difference,  617 
Auditory  centre,  in  vertebrates,  534 

sense,  of  bats,  601 
dog,  601 
fishes,  598 

cave-,  726 
insects,  581 
spatial  judgments  and,  667 
Auks,  accommodation  in,  643 

nictitating  membrane  in,  424 
Aurelia,  183 

phototactic  reactions  of,  571 

aurita,  sen.se  organs,  183 
Austrolethops,   degenerate  eyes  in,   726 
Autochthonous  layer  of  cornea,  295 
Auxins,  39,  510 

isolation  of,  41 
Averna  sativa  (oat),  phototropism  in,  40, 

119 
Avicula,  200 

light-shadow  reflex  in,  574 

sense  organs,  200 
Axolotl,  346 

perception  of  movement  in,  705 

visual  cells,  348 


B 


j8-carotene,  119 
Baboon,  443 


Baboon,  colour  vision  in,  635 

refraction  of,  639 
Bacteria,  luminous,  737,  743 
Bacterium  photometricum,  activity  of,  34 
Badger  (Meles),  444,  445 
Balcena.    See  Whale,  right-. 
Balcenoptera.    See  Whale,  blue. 
Balanoglossus,  227 

nerve-net,  515,  530 

nervous  system,  517,  530 

sense  organs,  227 
Balanus,  209 

adult,  degenerate  eyes  in,  722 

larva,  eyes  of,  209 

shadow-reflex  in,  45 
Balistes,  fovea  of,  310 
Bandicoot,  441 

nictitating  membrane,  441 

pupillary  flocculi,  439 
Barathronus,  degenerate  eyes,  724 
Barbatula,  colour  preference  in,   624 
Bathothaunut ,  203 

stalked  eyes  of,  203 
Bathygohius,  interocular  transfer  in,   698 
Bathylagus  benedicti,  310,  323 

fovea,  310,  611 

visual  cells,  305,  611 
Bathypterois,  "  feelers  "  in,  724 
Bathyteuthis,  eyes  of,  146 
Bathytroctes,  fovea,  310 

visual  cells,  305 
Batoidei,  279 

eyes  of,  282 

See  also  Selachians,  Raja,  Torpedo,  etc. 
Bats,  443 

eyelids,  491 

eyes  of,  449 

hearing  in,  601 

lens,  606 

nictitating  membrane,  493 

ocular  movements  of,  696 

optic  axis,  688 

refraction  of,  639 

retina,  pure-rod,  610 

retinal  vascularization,  480 

vision  of,  601 

visual  cells,  482 
Bdellostoma,  eyes  of,  263,  734 
Bears,  445 

nictitating  membrane,  492,  493 

optic  axis,  688 

polar,  pupils,  471 

pupils,  471 


INDEX 


785 


Bears,  retinal  vascularization,  479 
sloth-,  pupil,  471 

retractor  bulbi,  495,  496 
Beaver,  442,  445 
diurnality  of,  604 
fundus,  PI.  XV 
optic  axis,  688 
retinal  vascularization,  480 
Bees,  219,  220 
brain,  524 

bumble-.     See  Bomhus. 
colour  vision  of,  587 
compound  eye,  166 
"  dancing  "  of,  70 
honey-.     See  Apis. 
ocelli  of,  vision  of,  582 
optic  centres,  525 
stinging  reflex,  526 
telotaxis  in,  56,  58 
time -memory  in,  22 
vision  of,  585 
visual  acuity  of,  588,  589 
Beetles.     See  Coleoptera. 
Belideus  sciureus,  fundus,  PI.  XIII 
Belone,  visual  field,  binocular,  680 
Bengalichthys,  eyes  of,  279,  724 
Beyithobatis,  eyes  of,  279,  723,  724 
Bergmeister's  papilla,  477 
Beryx,  303 

tensor  choroidese,  303 
Betta,  84 

pugnax,  colour  changes  in,  84 
splendens,  colour  vision  in,  626 
Bibio  marci,  eye  of,  161 
Bifoveate  retina,  in  Anolis,  365,  366 

in  birds,  418 
Bigeminal  body,  534 
Binocular  vision,  697 

visual  fields,  672 
Bioluminescence,  736 
extracellular,  745 
intracellular,  746 
mechanism  of,  biological,  744 

chemical,  747 
occurrence  of,  737 
photoperiodism  in,  21 
purpose  of,  741 
Birds  (Aves),  397 

accommodation  in,  651 
brain,  533 

transection  of,  534 
cerebral  cortex,  543 
removal  of,  545 

S.O.— VOL.  I. 


Birds,  ciliary  ganglion,  501 

colour  changes  in,  control  of,  560 
rhythmic,  21 
seasonal,  21 
vision  in,  621,  629 
distance,  judgment  of,  700,  702 
diurnal,  603 
eyes  of,  400,  401j^.,  606 

efficiency  of,  256 
flightless,  extinction  of,  604 
fovea,  function  of,  658 
fundus.  PI.  XII 
irides,  PI.  XI 

lateral  geniculate  body,  541 
mid-brain,  535 
migration  of,  17,  63 
of  cones,  616 
of  retinal  pigment,  614 
navigation  by,  63 
nocturnal,  604 
ocular  movements  in,  695 
oil-droplets  in,  631 
olfactory  sense  in,  600 
optic  lobes,  535 
thalamus,  540 
pineal  organ,  716 
pupillary  reactions,  700 
refraction  of,  639 
reproductive  cycle  in,  17 

control  of,  559 
size,  judgment  of,  703 
spatial  judgments,  702 
summation,  retinal,  660 
tectum,  535 
time-memory  in,  22 
vision  of,  600 
visual  acuity  of,  662 

fields,  binocular,  681,  683,  684 

uniocular,  672 
pathways,  539,  544 
Bison,  446 
Bitis  arietans,  392 

visual  cells,  391,  392 
Bittern.     See  Botaurus. 
Bivalves,  196 
eyes  of.  200 

degenerate,  722 
nervous  system,  527 
vision  of,  574 

See  also  Molluscs,  Avicula,  Mya,  etc. 
Blatta  orientalis,  34 
activity  of,  34 

50 


786 


INDEX 


Blattella  germanica,  photo-responses,  con- 
ditioning of,  108 
phototaxis  in,  43,  45,  114 
Blennius,  310 

fovea  of,  309,  310 
ocular  movements,  693 
pholis,  conditioned  reflexes  and  colour 

vision,  623,  625 
sanguinolentis,  accommodation  of,  645 
Blood  constituents,  diurnal  rhythm  in,  13, 

15 
Blood  supply  to  eye,  482 
characteristics  in 
anurans,  340 
birds,  415 
crocodilians,  378 
lacertilians,  362 
lamprey,  266 
marsupials,  439 
monotremes,  436 
placentals,  477,  498 
snakes,  390 
Sphenodon,  381 
teleosts,  299 
urodeles,  347 
vertebrates,  476 
Blow-fly,  blue-bottle.    See  Calliphora. 
Boa.     See  Constrictor,  Charina,  Epicrates. 
Boar  (Sus  scrofa),  445 
Boidte,  fundus,  389 
hyaloid  vessels,  390 
iris,  387 
lens,  389 
optic  disc,  390 
visual  cells,  392 

field,  binocular,  684 
Boiga  dendrophila,  iris,  387,  PI.  IX 
Bolitotherus    corriutus,     retinal    pigment, 
migration  of,  19 
control  of,  556 
Bombinator  ignetis,  339 
colour  changes  in,  84 

vision  in,  628 
pupil  of,  339 
Bombus,  219 

mnemotaxis  in,  79 
vision  of,  584 
Bonihylius,  219 

colour  vision  in,  587 
Bombyx,  reactions  of,  526 
Bony  fishes.     See  Osteichthyes. 
Book-lice,  218 
Borodinula  infans,  visual  field,  679 


Botaurus,  bifoveate  retina,  418 
binocular  vision,  685 
stellaris,  685 
Bovidje,  446 

See  also  Cattle,  Sheep,  Goat,  etc. 
Box,  colour  preference,  625 

visual  field,  binocular,  679 
Brachiopods,  195 

larvae  of,  ocelli  in,  195 
Brachium  tecti,  541 
Bradypus.     See  Sloth,  3-toed. 
Brain  of  vertebrates,  533 

development  of,  531,  532 
See  also  Cerebral  ganglion. 
Branchellion,  193 

ocelli  of,  193 
Branchiomma  vesiculosuni,  192 
ocelli,  151,  193 

phototropic  movements  in,  39 
Branchionus,   dermal   sensitivity   in,    114 
ocellus,  194 
tropotaxis  in,  53 
Branchiopods,  207 
eyes  of,  209 

See  also  Daphnia,  Apus,  etc, 
Branchiostoma  lanceolatum.     See  Am- 

phioxus. 
Brittle-stars,  184 

bioluminescence  in,  739,  746 
Briicke's   muscle    (ciliary)    in  birds,    405, 
406 
in  lacertilians,  357 
in  marsupials,  439 
Bryozoa.     See  Polyzoa. 
B-substance,  in  amphibians,  98 
Bubo,  accommodation  in,  651 
eyelids,  425 
pecten,  412 

summation,  retinal,  660 
ascalaphns,  606 

binocular  field  of,  681 
lacteus,  422 
orientalis,  iris,  408 

tensor  choroideae,  406 
Buccinuni,  197 

oceUi,  142,  197 
Bufo,  334,  341 

area  centralis,  344 
colour  blindness  of,  628 
fundus,  341 
arenaruni,  colour  changes  in,  97,  558 

iris,  337 
bufo,  iris,  337 


INDEX 


787 


Bufo  marinus,  fundus,  341 
iris,  337,  PL  III 

viridis,  iris,  337 
Bugula,  46 

phototaxis  in,  46 

flabellata  larva,  ocelli,  195 

turrila  larva,  ocelli,  195 
Bull.     See  Cattle. 
Bullfinch.     See  Pyrrhula. 
Burbot.     See  Lota. 
Burrowing  habit,  degenerate  eyes  due  to, 

728 
Bursalis  muscle,  in  birds,  424 

in  lacertilians,  368 
Bush -baby.     See  Galago. 
Bush-cat  {Felis  libyca),  ciliarv  processes, 

466 
Buteo,  417 

bifoveate  retina,  417,  418 

summation,  retinal,  660 

visual  acuity  of,  657 
Butterflies,  219,  220 

aggregate  eyes  in,  159 

colour  vision  in,  587 

neu'.o -secretory  cells,  555 

retinal  pigment  inigration  in,  170 

visual  acuity  of,  588 

See  also  Vanessa,  Pieris. 


Cahrita,  eyelids,  366 
Cacatua  roseocapella,  orbits,  425 
Cacicus  cela,  iris,  407 
Caddis-fiies,  219.  220 

larvae,  ocelli,  222 

neuro -endocrine  system,  555 
C Cecilia,  eyes,  730 
Csecilians,  334 

pineal  organ,  714 

retina,  pure-rod,  610 

rudimentary  eyes,  730 
Caiman,  375 

iris,  PL  VIII 

visual  field,  binocular,  682 
Calamokhthys,  278,  320 

eyes  of,  320 

retina,  pure-cone,  611 
Calanus,  207 
Caligus,  208 

eyes  of,  209 
Calliactis,  nerve  trunk,  516 


Callionymus,  visual  cells,  307 
Calliphora,  219 

electroretinographic  responses,  586 
ocellus,  140 

optic  ganglia,  activity  of,  524 
vision  of,  584 
visual  acuity  of,  588 
erythrocephala,  maggot,  50 

phototaxis  in,  47,  50 
vomitoria,  telotaxis  in,  56 
Calotermes  flavicollis,  lai'vas,  phototaxis  in, 
43 
telotaxis  in,  56 
Calypte,  bifoveate  retina,  418 
Cambarus,  eye-stalk,  523,  553 
nervovis  system,  522,  524 
neuro -endocrine  system,  553 
retinal  pigment,  migration  of,  19 
ayersii,    sensitivity   of,    104,    114,    115, 

724 
virilis,  metabolic  rhythm  in,  16 
photopigments  in,  121 
Camel  (Camehis  bactrianus),  446 
corpora  nigra,  469,  470 
eyelids,  491 
tactile  vibrissse,  492 
See  also  Tylopoda. 
Campanula  of  Haller,  in  holosteans,  321, 
647 
in  teleosts,  302,  646 
Canal  of  Schlemm,  473 
of  Sondermann,  473 
Canida>,  445 

ocular  movements,  696 
optic  disc,  486 
pupil,  471 

retinal  vascularization,  479 
See  also  Dog,  Fox,  etc. 
Capra.     See  Goat. 
Caprella,  207 

Caprimnlgus  europceus,  410 
fundus,  410,  PL  XII 
pecten,  412 
Capsule,  lens,  in  jDlacentals,  474,  653 

variation  in  elasticity,  652 
Capuchin  monkey.     See  Monkey, 

capuchin. 
Capybara,  pupils,  472 
Carassius  atiratus,  292 
double  cones  in,  308 
iris,  PL  II 
phototaxis  in,  45 
pigment  epithelium,  305 


788 


INDEX 


Carassius  auratus 
sclera,  292 
telescope-oyed,  324 

iris,  PI.  II 
visual  cells  of,  307 
Carausius,  colour  changes,  control  of,  556 
Carcharodon,  pupils,  286 
Carcinus,  colour  vision  in,  578 
eyes  of,  163 

metabolic  rhythm  in,  15 
Cardium,  200 

accommodation  in,  591 
eyes  of,  147,  200 
Carinaria,  199 
eyes  of,  199 
Carinatse,  397 
Carnivores,  445 

accommodation,  653 
area  centralis,  485 
arhythmic,  604 
blood  supply  to  eye,  498 
ciliary  muscle,  462 
processes,  467 
region,  460,  461,  463 
circle  of  Hovius,  472 
colour  blindness  of,  634 
cornea,  453 
iris  pigmentation,  469 
lateral  geniculate  body,  489 
Moll's  glands,  492 
nictitating  membrane,  493 
nocturnal,  604 
ocular  movements,  696 
optic  axis,  688 

disc,  486 
orbit,  497 

pectinate  ligament,  464 
pupil,  470,  471,  472,  612 

reactions  of,  consensual,  700 
retinal  vascularization,  479 
tapetvim  cellulosum,  459,  609 
vision  of,  601 
visual  acuity,  663,  664 
field,  binocular,  689 
zonular  fibres,  475 
Carotenoid  pigments,  88,  118 

absorption  spectra  of,  119 
Carotid  circulation,  in  placentals,  499 
Carp.    See  Cyprinus  carpio. 
Cartilage,  scleral,  characteristics  in 
anurans,  334 
birds,  403 
chelonians,  369 


Cartilage,  scleral,  characteristics  in 

chondrosteans,  317 

crocodilians,  376 

dipnoans,  313 

holosteans,  321 

lacertilians,  356 

Latimer ia,  315 

monotremes,  433 

Notoryctes  (nodules),  438 

selachians,  281 

Sphenodon,  380 

teleosts,  292 

urodeles,  347,  349 
occurrence  of,  450 
Cartilaginous  fishes.  See  Chondrichthyea, 
Cassowary.     See  Casuarius. 
Castor.     See  Beaver. 
Casuarius,  397,  406 
pecten,  311,  413 
tensor  choroideae,  406 
Cat  (Felis  doniestica),  445 
accommodation  in,  653 
angle  gamma,  676,  677 
anterior  chamber,  465 
area  centralis,  485 
blood  svipply  to  eye,  499,  500 
chiasma,  487 
colovir  blindness  of,  634 
cornea,  453 
eye  of,  449 
eyebrows,  492 
interocular  transfer,  698 
iris  pigmentation,  469 
lamina  cribrosa,  489 
MolFs  glands,  492 
nictitating  membrane,  493 
occipital  cortex,  removal  of,  546 
olfactory  sense  in,  601 
optic  nerve-head,  488 
pectinate  ligament,  464 
pupils,  470,  471 

contraction  of,  612,  613 
reactions  of,  472 
refraction  of,  639 

retinal  vascularization,  477,  478,  481 
retractor  bulbi,  495 
svimmation,  geniculate,  611 
tapetum  cellulosum,  457,  458 
threshold  to  light,  absolute,  617 
vision  of,  601 
visual  acuity  of,  665 

field,  binocular,  673,  687,  689 

uniocular,  670,  672 


INDEX 


789 


Caterpillar,  46 

colour  changes  in,  92 

nervous  system,  522 

ocelli,  222 

phototaxis  in,  46,  114 

vision  of,  582 
Catfishes.     See  Siluridae,  Ameiurus,  etc. 
Cattle  {Bos  taurus),  446 

area  centralis,  485 

blood  supply  to  eye,  499,  500 

cinary  ganglion,  501 

colour  blindness  of,  624,  634 

conjunctiva,  491 
glands  of,  491 

cornea,  453 

epithelium  of,  452 

lacrimal  gland.  493 

Moll's  glands.  492 

nictitating  membrane,  493 

optic  axis,  688 

orbit,  498 

pectinate  ligament,  464 

pineal  organ,  716 

pupillary  reactions,  472 

retinal  vascularization,  479 

visual  field,  binocular,  689 
uniocular,  672 

vitreous,  476 
Caudata.     See  Urodeles. 
Causus  rhombeatus,  visual  cells,   391 
Cave-fishes,  725 

degenerate  eyes  in,  725 

dermal  sensitivity,  114 
Cavemicolous  habit,  degenerate  eyes  due 

to,  724 
Cavia.     See  Guinea-pig. 
Cavy,  Patagonian,  diurnality  of,  604 
pupil,  472 

spotted,  optic  axis,  688 

tapetum  fibrosum,  458,  609 

See  also  Guinea-pig. 
CajTnan.     See  Caiman. 
Cebidse,  443 

See    also    Monkey,    capuchin  ;     Xycti- 
pithecus,  etc. 
Cebus.    See  Monkey,  capuchin. 
Cells  of  Hesse,  230 

of  Joseph,  229 
Centipedes,  210 

eyes  of,  210 

See  also  Myriapods. 
Central  body,  in  arthropods,  521 

nervous  sytem,  630 


Central  organization  of  vision,  509 
Centrophorus  calceus,  pupils,  286 
Centrostephanus  longispinus,  117 

pigment  in,  117 
Cephalaspis,  234 
eyes  of,  238 
pineal  organ,  713 
Cephalochordata,  228 
See  also  Amphioxus. 
Cephalopods,  196 

accommodation  in,  590 
blind,  723 

cerebral  ganglion,  528 
chromatophores,  85,  86 
colour  changes  in,  82,  93,  105 
eyes  of,  143,  201 

degenerate,  723 
iris,  contraction  to  light,  89 
luminovis  organs  in,  740 
nervous  system,  527 
neuro-secretory  cells,  552 
pupils,  146 

contraction  of,  89 
retina,  145 
vision  of,  575 

See  also  Octopus,  Sepia,  Nautilus,  etc. 
Cephalopsin,  120 
Cerambycidae,  eyes  of,  160 
Ceratopogon,  eye  of,  224 
Cercocebus.    See  Mangabey. 
Cerebral  cortex,  543 
ablation  of,  545 
Cerebral  (cephalic)  ganglion,  518 

in  arthropods,  521,  522,  525,   526 
activity  of,  524 
function  of,  524 
removal  of,  525 
molluscs,  527 

worms,  segmented,  519,  520 
unsegmented,  518,  519 
vesicles,  531,  532 
Cereopsis,  annular  pad,  409 

pecten,  412 
Cervus  porcinus,   fundus,   PI.   XIV 
Cestodes,  187 

nervous  system,  519 
sense  organs  lacking  in,  734 
Cetaceans,  446 
choroid,  457 
cilia  lacking,  492 
ciliary  receptor  organs,  467 
cornea,  453 

keratinized,  456 


790 


INDEX 


Cetaceans,    dilatator   rimse   palpebraruin, 
492 

eyes  of,  449,  451 

lacrimal  passages  lacking,  494 
secretion,  493 

lens,  474 

ocular  adnexa,  502 

pineal  apparatus  absent,  711 

pupil,  472 

operculum  of,  470 

refraction  of,  639 

retina,  pure-rod,  610 

retractor  bulbi,  495 

sclera,  450,  451 

sphincter  muscle,  468 

summation,  retinal,  660 

tapetum  fibrosum,  457,  458,  609 

vibratory  sense  in,  601 

vision  of,  601 

visual  cells,  483 
Cetomimus,  degenerate  eyes,  724 
Cetonia,  219 

colour  blindness  of,  586,  587 
Chsetognaths,  194 

eyes  of,  152,  194 

See  also  Sagitta,  Spadella. 
Chcetopterus,    biolumineseence    in,    739, 

745 
Chameleon,  355,  695 

annular  pad,  361 

ciliary  body,  356 

colour  changes  in,  87 
control  of,  558 
rhythmic,  20 

conus,  363 

eyelids,  366 

eyes  of,  605 

fovea,  365,  659 

fundus,  362,  PI.  VI 

lacrimal  gland  lacking,  368 

lens,  360 

ocular  movements  of,  368,  694 

scleral  cartilage,  356 

spatial  judgments,  701 

vision  of,  599 

visual  acuity,  657,  661 
field,  uniocular,  670,  671 
Chanos,  lids  in,  311 
Charax,  colour  preference  in,  625 
Charina,  ciliary  region,  385 
Charybdea,  183 

ocellus  of,  138 
Cheetah,  445 


Chelodina  longicollis,  fundus,  372 
transparent  eyelids,  374 
visual  cells,  373 
Chelonia  my  das,  conus,  372 

eye  of,  354 
Chelonians,  353 

accommodation  in,  651,  652 
colour  preference,  628 
eyes  of,  368j^.,  370,  PL  VII 
ocular  movements  of,  694 
pineal  organ,  716 
refraction  of,  639 
retina,  cone -rich,  612 
retinal  pigment,  migration  of,  614 
threshold  to  light,  difference,  618 
vision  of,  599 
visual  acuity  of,  661 
field,  binocular,  682 
Chelonidse,  369 

Chelydra  serpentina,  conus,  avascular,  in 
embryo,  372 
fundus,  372 
visual  cells  of,  374 
field,  binocular,  682 
Chemical  sense  of  crustaceans,  579 
Dytiscus,  103,  104 
fishes,  598 
Pecten,  103 
vertebrates,  597 
worms,  572 
Chemo -receptors,  116 
Chemotaxis,  33 

Chevrotain  {Tragulus),  444,  446 
Chiasmal  decussation,  487,  697,  698 
in  birds,  423 
placentals,  487 
selachians,  289 
snakes,  392 
teleosts,  311 
Chicken.     See  Gallus, 
Chilopoda,  210 
eyes  of,  210 
See  also  Myriapods. 
Chimcera  monstrosa,  290 
Chimaeras,  eyes  of,  290 
retina,  pure-rod,  610,  611 
threshold  to  light,  absolute,  616 
Chimpanzee,  443 

colovir  vision  in,  635 

cornea,  453 

extra-ocular  muscles,  495 

eye  of,  605 

interocular  transfer,  698 


INDEX 


791 


Chimpanzee,  vision  of,  602 

visual  acuity  of,  665 
Chinchilla,  445 
optic  axis,  688 
pupil,  470,  472 
retina,  pure-rod,  610 

vascularization  of,  480 
visual  cells,  483 
Chipmunk,  pupils,  472 
Chironorrnis,  nervous  system,  522 
Chiroptera.     See  Bats. 
Chiton,  196 

homing  ability  of,  575 
photosensitivity  of,  197 
sense  organs  of,  196,  723 
Chktmydosaurus,  3o6 

colour  changes  in,  84 
Chlorophyll,  5 

Choanoid  muscle.     See  Retractor  bulbi. 
Choloepus.     See  Sloth,  2-toed. 
Chologaster,  eyes  of,  726 
Chondrichthyes,  235,  278 
eyes  of,  279 

See  also  Selachians,  Holocephalians. 
Chondrosteans,  235,  278 

accommodation  lacking  in,  640 
choroidal  tapetum,  609 
eyes  of,  315,  318 
nocturnality  of,  603 
See  also  Acipenser,  Polypterini 
Chordates,  227 

central  nervous  system,  530 
See  also  Protochordates,  Vertebrates. 
Choroid,  characteristics  in 
anurans,  335 
birds,  404 
chondrosteans,  317 
dipnoans,  313 
holosteans,  321 
lacertilians,  356 
lamprey,  266 
Latimer ia,  315 
marsupials,  438 
placentals,  457 
selachians,  281 
snakes,  385 
Sphenodon,  380 
teleosteans,  296 
urodeles.  347 
Choroidal  gland  of  holosteans,  321 
of  teleosts.  297,  298 
papillse,  in  bats,  459 
Chortippus,  optic  ganglia,  activity  of,  524 


Chromatoblasts,  117 
Chromatophores,  85 
action  of  light  on,  89 
control  of,  92 

in  crustaceans,  94,  554 
insects,  93,  555 
vertebrates,  95,  558 
Chromatophorotropins,  93,  554,  555 
Chrysemys,  area  centralis,  374 
conus,  372 
iris,  370,  PI.  VII 
Chrysochloris.    See  Mole,  golden. 
Chrysops  marmoratus,  visual  cell  of,  128 
Chrysotis,  green  oil-droplets,  420 
Cichla,  291 

Cicindela,  larvae,  form  vision  in,  582 
Ciconiiformes,  annular  pad,  409 
See  also  Ardea,  Botaiirus,  etc. 
Cilia,  in  light-sensitive  cells,  128 
rhythniic  movements  of,  511 
(eyelashes),  in  mammals,  492 
Ciliary  canal.     See  Ciliary  cleft, 
cleft,  in  birds,  405 

in  mammals,  461,  466 
folds,  in  selachians,  285 
ganglion,  in  vertebrates,  501 
ligament.     See  Tensor  choroideae. 
muscle,  characteristics  in 
amphibians,  335 
birds,  405 
chelonians,  372 
crocodilians,  376 
lacertilians,  357 
inarsupials,  438 
I^lacentals,  461 
Sphenodon,  380 
teleosts,  302 
accommodation  and,  650 
configuration  of,  654 
occurrence  of,  654 
papilla,  in  chondrosteans,  317 
in  selachians,  284,  285,  647 
processes,  characteristics  in 
anurans,  336 
birds,  405 
chelonians,  372 
crocodilians,  376 
marsupials,  438 
monotremes,  433 
islacentals,  466 
selachians,  284 
urodeles,  347 
receptor  organs,  467 


792 


INDEX 


Ciliary  region,  chai'acteristics  in 
anurans,  335,  338 
birds,  403,  405,  406 
chelonians,  361,  372 
chondrosteans,  317 
crocodilians,  376 
lacertilians,  356,  358 
Latimeria,  315 
marsupials,  438,  439 
monotremes,  433,  434 
placentals,  460,  461 
selachians,  283 
snakes,  385,  388 
Sphenodon,  380 
teleosts,  301 
urodeles,  347 
roll,  in  snakes,  386,  388 
sinus.     See  Ciliary  cleft, 
venous  plexus,  in  placentals,  472,  473 
sinus,  characteristics  in 
anurans,  336 
birds,  408 
chelonians,  372 
crocodilians,  376 
lacertilians,  359 
marsupials,  439 
monotremes,  435 
snakes,  386 
Sphenodon,  380 
See  also  Schlemm's  canal, 
web,  in  mo"notremes,  435 
Ciliata,  180 
Ciliophora,  180 

Cilio-scleral  sinvis.     See  Ciliary  cleft, 
Cinyxis  erosa,  fundus,  PI.  VII 
Ciona,  pigmented  spots  in,  228 
Circle  of  Hovius,  472 
Circulus  arteriosus  iridis  major,   468 

minor,  468 
Circum-ocular  sulcus,  of  teleosts,  311 
Circum- oesophageal   ring,  in  crustaceans, 
521 
insects,  521,  522 
molluscs,  527 
Circus  movements,  54,  525 
Cirripedes,  208 
eyes  of,  209 

vestigial,  in  adults,  209 
nauplius  of,  208 

eyes  of,  209 
nervous  system,  521 
Cirrothauma  murrayi,  eyes  lacking  in,  723 
Cistella,  larva,  ocelli  in,  195 


Citellus  citellus.    See  Souslik. 
Civet  cat,  444,  445 
Cladocera,  207 

conditioning  of,  578 

orientation  to  polarized  light  in,  73 

phototactic  response  of,  578 

See  also  Daphnia,  Polyphemus,  etc. 
Cladophora,  eye -spot  in,  125 
Clemmys,  682 

iris,  370 

visual  field,  binocular,  682 
Clethrionomys.    See  Vole,  red-backed. 
Clupea  harengus,  299 

falciform  process,  299 
larvae,  activity  of,  34 

pilchardus,  visual  cells  of,  307 
Clupeidae,  adipose  lids  in,  311 

See  also  Clupea,  Engraulis,  Chanos. 
Cnidaria,  182 
Coati,  444,  445 

pupils,  472 
Cobra,  386 

See  also  Elapidae,  Naja. 
Cochlea,  534,  690 
Cockle.    See  Cardium. 
Cockroach,  218,  220 

nocturnality  of,  34 

vision  of,  584 

See  also  Blattella,  Blatta,  Periplaneta. 
Cod.    See  Oadus. 
Coelacanth,  235,  278,  315 

accommodation  lacking  in,  640 

choroidal  tapetum,  609 

eyes  of,  314,  316 

nocturnality  of,  603 

retina,  rod-rich,  610 
Coelenterates,  181 

bioluminescence  in,  739,  745,  748 
rhythmic,  22 

myo -epithelial  cell,  513 

nerve-net,  512,  514,  515 

phototactic  reactions  of,  571 

sense  organs  of,  182 
Colaptes,  choroid,  405 

auratus,  420 

green  oil-droplets,  420 
Coleonyx,  rods  of,  364 
Coleoptera,  219,  220 

eyes  of,  167,  224 

larvae,  ocelli  of,  141,  223 

luminous  organs  in,  740,  742,  748 

neuro-endocrine  system,  555 

See  also  Dytiscus,  Necrophorus,  etc. 


INDEX 


793 


Collembola,  217,-  218 

luminous  organs  in,  740 
ocelli,  159,  221 
Colliculi,  inferior,  534 

superior,  534 
Colcelus  monedula,  iris,  PI.  XI 
Colour  changes,  82 

colour  vision  and,  621,  625 
control  of,  92 

in  crustaceans,  554 
insects,  555 
vertebrates,  558 
demonstrative,  83 
mechanism  of,  85 
protective,  82 
rhythmic,  19 
preference,  623 
vision,  in  cephalopods,  575 
crustaceans,  578 
insects,  586 
spiders,  580 
vertebrates,  619 
in  amphibians,  627 
birds,  629 
cyclostomes,  624 
fishes,  624 
mammals,  632 
reptiles,  628 
investigation  of,  620 
methods  of  testing,  621 
Coluber  guttatus,  fundus,  389 
iris,  386 

visual  field,  binocular,  684 
Colubrids,  retina,  pure-cone,  611 
visual  cells,  391,  392 
field,  binocular,  684 
Columba,  64 

colour  vision  in,  630 

conditioning  in,  663 

decerebrate,  reactions  of,  545 

eye  of,  605 

hue  discrimination  in,  619 

interocvilar  transfer,  698 

iris,  407,  408,  PL  XI 

lens,  409 

ocular  movements  in,  692 

pecten,  414 

pineal  organ,  716 

pupillary  reactions,  consensual,  700 

Purkinje  phenomenon  in,  629 

retina,  417 

threshold  to  light,  difference,  618 

transversalis  muscle,  407 


Columba 

visual  acuity  of,  662,  665 
field,  binocular,  682,  684 
uniocular,  672 
livia,  iris,  408 

See  also  Homing  pigeon. 
palumbus,  pecten,  413 
Columbidae,  eyes  of,  402 

See  also  Columba,  Streptopelia,  etc. 
Comb-jelly,  182 

bioluminescence  in,  739 
sense  organs  of,  182 
Compound  eyes,  153 

composite,  160,  591 
of  crustaceans,  160 
of  insects,  1 60 
development  of,  156 
optical  system  of,  170 
structure  of,  155,  157 
of  arachnids,  160 
crustaceans,  163 
insects,  166 
Compressor  lentis,  in  birds,  651 
Conditioned  reflexes,  568 

colour  vision  and,  623 
Cone,  crystalline,  157 
Cones  (vertebrate),  250 

differentiation  from  rods,  251 
double,  253 

in  anurans,  342,  344 
birds,  419 
chelonians,  374 
holosteans,  321,  322 
lacertilians,  364 
marsupials,  440,  441 
platypus,  436 
Protopterus,  313,  314 
snakes,  391,  392 
teleosts,  307,  308 
urodeles,  348 
quadruple,  253 

in  teleosts,  308 
triple,  253 

in  anurans,  342,  344 
lacertilians,  364 
teleosts,  308 
twin,  253 

in  teleosts,  307,  308 
Coney.     See  Hyrax. 
Conjunctiva,  in  mammals,  491 
Conjunctival  bone,  in  sturgeon,  317 
Conolophus  subcristatus,  conus,  363 
fundus,  361,  362,  PI.  VI 


794 


INDEX 


Consciousness,  emergence  of,  108 
Constrictor,  ciliary  region,  385 
venovis  sinus,  386 
visual  field,  binocular,  684 
Contractile  pupils,  occurrence  of,  612 
Conus  papillaris,  in  crocodiles,  378 
lacertilians,  362 
avascular,  in  embryo  turtles,  372 
vestigial,  in  marsupials,  440 
Coot.     See  Fulica. 
Copepods,  207 
eyes  of,  209 

luminous  organs  in,  740,  746 
Copilia,  209 

accoininodation  in,  591 
eyes  of,  159,  160,  209 
vision  of,  578 
Copperhead  snake,  387 

posterior  segment  of  eye,  387 
Cordylosaurus,   transparent   eyelids   of, 

366 
Corephium.,  sense  organs  of,  196 
Cornea,  characteristics  in 
amphibians,  334 
Anableps,  324 
birds,  404 
chelonians,  369 
chondrosteans,  317 
coelacanths,  315 
crocodilians,  376 
dipnoans,  312 
fishes,  276 
holosteans,  321 
lacertilians,  356 
lamprey,  265 
marsupials,  438 
monotremes,  433 
placentals,  452,  453 
selachians,  281 
snakes,  385 
teleosts,  294 
yellow,  occurrence  of,  656 
Corneal  facet,  157 

nerves  in  mammals,  454,  455 
Cornealis  muscle,  in  lamprey,  271 

and  accommodation,  645 
Corpora  nigra,  469,  612 
Corpvis  allatum  in  insects,  555 

cardiacum  in  insects,  555 
Corvidae,  eyes  of,  402 

See  also  Corvus. 
Corvus  monedula,  iris,  408 
visual  acuity  of,  663 


Corycceus,  209 
Cottus,  cornea  of,  295 

bubalis,  eye  of,  302 
Cow.     See  Cattle. 
Coypu,  445 

optic  axis,  688 

pvipils,  472 
Crabs,  206 

eyes  of,  206 

nervous  system  of,  521 

sexual  cycle,  control  of,  555 

See  also  Decapods,  Carcinus,  etc. 
Crago  (Crangon)  vulgaris,  205 

colour  changes  in,  94 
vision  in,  578 

eyes  of,  165,  206 

ommochroines  in,  123 
Crampton's      muscle,      in      birds,      405, 
406 
in  lacertilians,  357 
Crane.     See  Orus. 
Crane-flies,  eyes  of,  167 
Crayfish,  206 

eyes  of,  164,  206 

sexual  cycle,  control  of,  555 

See  also  Crustaceans,  Astacus,  etc. 
Crenilabrus,    colour    changes    and    colour 
vision,  625 

rostratus,  dorsal  light  reaction,  76 
Crepuscular  animals,  602 
Cribriform  ligament,  461 
Cribrina,  phototactic  reaction  of,  571 
Crinoidea,  184 
Crocodile  tears,  379 
Crocodilians,  353,  375 

accommodation  in,  651,  654 

eyes  of,  376  ff.,  PL  VIII 

ocular  movements  of,  694 

pineal  organ,  716 

pupils,  contractile,  612 

Purkinje  shift  in,  628 

refraction  of,  639 

retinal  pigment,  migration  of,  614 
tapetum,  608 

vision  of,  599 

visual  acuity  of,  661 
field,  binocular,  682 
Crocodilus,  378 

porosus,  lacrimal  glands,  379 

sclerops,  eye  of,  354 
Crossopterygii,  234,  235 

central  nervous  system,  532 

See  also  Dipnoans. 


INDEX 


795 


Crotalidse,  facial  pit,  599,  600 

visual  cells,  391,  392 
Crotalus,  olfactory  sense  in,  599 

See  also  Crotalidae. 
Crotaphytus,  cones,  364 
Crustaceans,  206 

blind,  722,  724,  734 

cerebral  ganglion,  521 
removal  of,  525 

colour  changes  in,  82,  91,  94 
control  of,  554 
rhythmic,  20 

compound  eyes  of,  163,  206 

conditioning  of,  579 

deep-sea.     See  Deep-sea  Crustaceans. 

eyes  of,  206 

degenerate,  722,  723,  725 

eye-stalk,  523 

neuro -secretory  cells  in,  551,  553 

luminous  organs  in,  740,  744,  745,  748 

metabolic  rhythms  in,  15 
control  of,  555 

nervous  system,  521 

neuro -endocrine  system,  552,  553 

omjnochromes  in,  123 

retinal  jDigment  migration  in,  165 
control  of,  554 
rhythmic,  19 

spectral  sensitivity  of,  585 

time-memory  in,  22 

vision  of,  578 

visual  centres,  524 
pigments  in,  121 
Cryptobranchus,  eyes  of,  349 
Crypfotympana,  ocelli,  vision  of,  582 
Crystalline  cone,  157 

lens.     See  Lens. 
Ctenophora,  182 

luminescent,  739 
Cuckoo,  migration  of,  18 
Culex,  scototaxis  in,  60 
Cupulate  eyes,  137 
Cuttlefish,  85,  196 

colour  changes  in,  85,  93 

eyes  of,  143,  201 

See  also  Sepia. 
Cyanocitta,  414 

pecten,  413,  414 
Cyanopsin,  122 
Cybernetics,  106 

Cyclodorippe,  degenerate  eyes  of,  723 
Cyclops,  152 

composite  ocellus  of,  152,  208 


Cyclosa  rnsulana,  camouflage,  83 
Cyclostomes,  259 

accominodation  in,  644 

brain,  533 

transection  of,  534 

central  nervous  system,  532 

colour  changes  in,  95 
control  of,  558 
rhythmic,  20 
vision  in,  624 

dermal  sensitivity  in,  114 

diurnal  ity  of,  603 

eyes  of,  259 

degenerate,  734 

fore-brain,  543 
removal  of,  545 

labyrinths,  534 

lateral  genicvilate  body,  541 

mid-brain,  535 

ocular  movements  of,  691 

optic  thalamus,  539 

palaeocortex,  543 

jmrietal  eye,  713,  716,  717 

pineal  eye,  713,  716,  717 

refraction  of,  638 

secretory  inechanism  of,  267 

tectum,  534 

telencephalon,  543 

vision  of,  598 

visual  field,  binocular,  678 
pathways,  535,  543 
pigments  in,  121 
Cymonomus,  degenerate  eyes  of,  723 
Cynictis,  diurnality  of,  604 

pupil,  472 

tapetum  lacking,  459,  609 
Cynomys.    See  Prairie-dog. 
Cypridina,  207 

bioluminescence  in,  746 

composite  ocellus  of,  152 
Cyprinidse,  291 

cornea,  294 

retinal  tapetum,  305,  612 

See   also   Cyprinus,    Carassius,    Phoxi- 
nus. 
Cyprinus  carpio,  291 

colour  vision  in,  625 

cornea,  294,  295 

falciform  process,  299 

iris,  303 

ocular  movements,  693 

visual  field,  binocular,  679 


796 


INDEX 


Cypris  (Cypria),  152,  208 

composite  ocellus  of,  152 
Cystoflagellates,  180 


D 


Dacelo  gigas,  pecten,  413 
Dafila  acuta,  visual  acuity,  663 
"  Dancing  "  of  bees,  70 
Daphnia,  74,  208 

composite  ocellus  of,  152,  209 
compound  eye  of,  163,  209 
conditioning  of,  578 

dermatoptic  sensitivity  in,  32,  114,  578 
dorsal  light  reaction  in,  74 
Darwin,  Charles,  2,  3 
Dasychone,  ocelli  of,  192 
Dasypeltis,  392 

visual  cells,  392 
Dasypodida?,  445 
Dasypus.     See  Armadillo. 
Dasyure,  437,  438 
ciliary  muscles,  439 
pupils,  439,  612 
tapetum  fibrosum,  438,  609 
visvial  cells,  440 
Dasyuridse,  437 

See  also  Dasyure,  Tasmanian  devil,  etc. 
Decapods,  206 
eyes  of,  206 

nervous  system,  521,  524 
Decussation.     See  Chiasmal  decussation. 
Deep-sea  crustaceans,  eyes  of,  degenerate, 
207,  723 
enlarged,  207 
luminous  organs  in,  740,  742 
fishes,  eyes  of,  degenerate,  292,  723 

enlarged,  273,  281,  292,   323,   606, 

723 
stalked,  327 
tubular,  277,  322,  606 
optics  of,  642,  643 
luminous  organs  in,  741,  746 
pupils,  286 
refraction  of,  638 
retina,  pure-rod,  310,  610 
tapetum,  retinal,  608 
threshold  to  light,  674 
visual  acviity  of,  657 
cells,  305,  643 
field,  vmiocular,  670 
molluscs,  eyes  of,  degenerate,  723 


Deep-sea  molluscs,  eyes  of,  stalked,  203 
tubular,  203 
luminous  organs  in,  740,  742 
Deer,  446 
cornea,  453 

eyelids,  movements  of,  491 
Harder's  gland  absent,  494 
nictitating  membrane,  493 
optic  axis,  688 
visual  acuity  of,  664 
Degenerate  eyes,  721 
Deiters'  nucleus,  534 
Delphinus.     See  Dolphin. 
Demodex  folliculorum,  216 
Dendroccelum,  188 

klinokinesis  in,  36,  37 
ocelli  of,  136,  188 
Dendrocopus  major,  414 

pecten,  414 
Dendrocygna,  iris,  407,  408,  PI.  XI 
Dentalium,  197 

eyes  lacking  in,  729 
statocysts  of,  197 
Depressor  corneae.     See  Crampton's 
muscle, 
palpebrse  inferioris,  in  elephant,  492 
Depth  perception,  667 
Dermaptera,  218,  220 

See  also  Forficula. 
Dermatopsia,  114 
Dermatoptic  sensitivity,  32,  113 
of  echinoderms,  184 
of  rotifers,  194 
Derniochelys  coriacea,  369 
scleral  cartilage,  370 
Dermoptera,  443 
Descartes,  Rene,  710,  712 
Desman,  441,  443 
Desmid,  35 

response  to  light,  35 
Desmodus.    See  Vampire  bat. 
Deuterocerebrum,  in  arthropods,  521 
Diadema  antillarum,  185 

colour  changes  in,  89,  90 

rhythmic,  20 
dermal  sensitivity  in,  114,  185 
iridophores  in,  184 
phototropic  movements  in,  39 
setosum,  iridophores  in,  185 
Dia-heliotropism,  38 
Dialommus  fuscus,  double  cornea,  325 
Diatom,  35 

colour  changes  in,  82,  89 


I 


I 


INDEX 


797 


Diatom,  response  to  light,  35 
Dictyostelium    discoideum    (slime-mould), 

thermal  stimulation  in,  36 
Didelphyidte,  437 

Didelphys.     See  Oposum,  Virginian. 
Diencephalon,  532,  537 
photosensitivity  in,  537 
pineal  apparatus  and,  711 
secretory  activity,  537 
Dilatator  pupillse,  characteristics  in 
anurans,  337 
birds,  407 
lacertilians,  357 
placentals,  468 
selachians,  285 
snakes,  388 
Sphenodon,  381 
teleosteans,  303 
rimae  palpebrarum,  in  cetaceans,  492 
Dineutus,  eyes  of,  160 

assimilis,  circus  movements  in,  54 
grosstis,  224 
Dinoflagellates,  179,  180 
bioluininescence  in,  738 

rhythmic,  22 
eye -spot  of,  126 
Dinophilus,  ocelli  of.  193 
Dinosaurs,  234,  236 
Dioniedea  caiita,  418 
fundus,  PI.  XII 
infula  and  fovea,  418,  420 
Diplopoda.  210 
Dipnoans,  235,  278 

accommodation  lacking,  640 
central  nervous  system,  532 
eyes  of,  312,  313 
nocturnality  of,  603 
pineal  body,  714 
Diptera,  219,  220 

accominodation,  static,  in,  591 
eyes  of,  160,  222,  223 
luminous  organs  in,  740 
nervous  system,  521,  522 
neuro -endocrine  system,  555 
See  also  Drosophila,  Sarcophaga, 
Musca,  etc. 
Directional  eye,  132,  135 
Discrimination  box,  569 
Dispholidus,   visual   field,   binocular,    684 
Distance,  perception  of,  in  insects.  589 
in  vertebrates,  701 
receptors,  116 


Diurnal  animals,  602 

eye,  characteristics  of,  611 
retina  of,  610,  611 

rhythins.     See  Photoperiodism. 
Dixippus,  218 

colour  blindness  of,  587 
changes  in,  88,  93 
control  of,  556 
rhythmic,  20 

metabolic  rhythm  in,  15 
Dodo,  604 

extinction  of,  604 
Dog  {Canis  familiaris),  445 

accommodation  in,  653 

angle  gamma  in,  677 

area  centralis,  485 

blood  supply  to  eye,  498,  499 

cerebral  cortex,  543 
removal  of,  545 

chiasma,  487 

choroid,  shunt  apparatus,  460 

ciliary  region,  461,  463 

circle  of  Hovivis,  472 

colour  blindness  of,  634 

conditioned  reflexes  and,  623 

conjunctiva,  491 

cornea,  453 

epithelium  of,  452 

extra-ocular  muscles,  496 

Harder 's  gland,  494 

hearing  of,  601 

lacrimal  passages,  494 

lens,  474 

Moll's  glands,  492 

movement,  perception  of,  705,  706 

nictitating  membrane,  493 

occipital  cortex,  removal  of,  546 

olfactory  sense  in,  601 

optic  axis,  688 

pectinate  ligament,  464 

pigment  epithelium,  459,  608 

pupils,  471 

reactions  of,  472 

refraction  of,  639 

retinal  vascularization,  477,  478 

retractor  bulbi.  495,  496 

tapetum  cellulosum,  457,  459 

threshold  to  light,  difference,  618 

visual  acuity  of,  664 
field,  binocular,  689 
Dogfishes,  279 

eyes  of,  282 

See  also  Mustelus,  Squalus,  etc. 


798 


INDEX 


Dolichopteryx,  tubular  eyes  in,  324 
Dolphin,  444,  446 

cornea,  453 

keratinized,  456 

ocular  adnexa,  502 

pineal  body  absent,  71 1 
Dormouse,  choroid,  457 

pupils,  contractile,  612 

retinal  vascularization,  482 

visual  cells,  483 
Dorsal  light  reaction,  74 
Dorylus,  221 

eyes  lacking  in,  729 
Dragon-fly,  74 

compound  eyes  of,  172,  222 

See  also  Anax,  Aeschna. 
Drainage    channels    in    mammals,    472, 

473 
Drepanophorus,  ocellus  of,  134 
Driver  ant,  221,  729 

eyes  lacking  in,  729 
Droniceus,  397 
Dromedary  (Canielus  dromedarius),  446 

See  also  Tylopoda. 
Drosophila,  44 

colour  vision  of,  587 

dermal  sensitivity  in,  114 

electroretinographic  responses,  586 

ommochroines  in,  123 

optomotor  reaction  in,  583 

phototaxis  in,  44,  45 

spectral  sensitivity  of,  585 

telotaxis  in,  56 

time-memory  in,  22 

vision  of  ocelli  of,  582 

visual  acuity  of,  588 
Dryophiops,  pupils,  388 
Dryophis,  fovea,  388,  392 

pupils,  388,  674 

visual  field,  binocular,  682 
Ducks,  diving,  accommodation  in,  643 
ciliary  muscles,  407 
nictitating  membrane,  424 

gonadotrophic  activities  of,  18 
nervous  control  of,  537,  560 

visual  fields  of,  685 

See  also  Dafila,  Dendrocygna,  etc. 
Dugong,  446 

pineal  organ  absent,  711 

retinal  vascularization,  480 
Dytiscus  marginalis,  168 

brain,  524 

eyes  of,  168,  172 


Dytiscus  inarginalis 

larva,  dermal  sensitivity  in,  114 

ocelli  of,  221 
optic  ganglion,  activity  of,  524 
sensory  reactions  of,  103,  588 
vision  of,  584 

E 

Eagle,  accommodation  in,  651 

bald.     See  Haliaetus. 

bifoveate  retina,  417,  418 

Chilean.     See  Geranoaetus. 

visual  field,  binocular,  684 
Earthworm,  190 

bioluminescence  in,  745 

eyes  of,  190 

tropotaxis,  53 

visual  cells,  131 

See  also  Lumbricus. 
Eccentric  cell  in  compound  eyes,  158 
Echidna,  430,  431 

ciliary  processes,  433 
body,  434 

eye  of,  432 

fundus,  PI.  XIII 

optic  axis,  688 

retina,  435 
pure-rod,  610 

scleral  cartilage,  433 
Echinoderms,  183 

colour  changes  in,  82,  90 
rhythmic,  20 

dermal  sensitivity,  114 

luminescent,  739 

nerve-net,  515 

nervous  system,  516 

origin  of  vertebrates  through,  233 

phototactic  reactions  of,  571 

sense  organs  of,  184 
Echinoidea,  184 
Edentates,  445 

nictitating  membrane,  493 

ocular  movements  of,  696 

optic  axis,  688 

refraction  of,  639 

vision  of,  601 
Eels,  retina,  299,  301 

snipe-.     See  Borodinula. 

visual  cells  of,  307 

See  also  Anguilla. 
Eiseniafmtida,  conditioning  of,  573 
tropotaxis  in,  53 


INDEX 


799 


Elaphe  quadrivitatta,  iris,  387,  PI.  IX 

quatorlineata,  iris,  387,  PI.  IX 
Elapidfe,  iris,  386 

visual  cells,  392 
Elaps,  pupil,  388 

Elasniobranchs.     See  Chondrichthyes. 
Elaterid  beetles,  bioluininescence  in,  736, 

740 
Electric  organs  in  fishes,  751 
Electrophorus,  electric  organ  of,  751 
Electroretinograi^hic  responses,  and 

colour  vision,  622 
Eledone,  146 

eye  of,  146 
Elephants,  446 

African,  446 

cilia  lacking  in,  492 

eyelids,  movements  of,  491,  492 

eyes  of,  450 

immobility  of,  497,  696 

Indian,  446 

ciliary  processes,  466 
eye  of,  447 

lacrimal  passages  lacking  in,  494 

optic  axis,  688 

orbit,  497 

retinal  vascularization,  480 

sclera,  450 

tapetum  fibrosum,  458,  609 

visual  fields,  689 

Zeis's  glands,  491 
Elephas  maximus.     See  Elephant,  Indian. 
Eliomys.     See  Dormouse. 
Ellobius,  degenerate  eyes  of,  733 
Elysia  viridis,  menotaxis  in,  61 
Embioptera,  220 
Ernplectonema  kandai,  bi(jluininescence 

in,  739,  746 
Emu.     See  Dromceus. 
Emyda,  fovea,  374 

transparent  eyelid,  374 

granosa,  fundus,  372,  PI.  VII 
Emys,  scleral  ossicles,  369 

orbicidaris,  area  centralis,  374 
iris.  PI.  VII 
Enchelioph  is  Jordan  i,  735 
eyes  of,  735 
pupils,  304,  612 
sclera,  292 
Engraulis,  lids  in,  311 
Entosphenus,  visual  cells  of,  269 
Ephemeroptera,  218,  220 

accommodation,  static,  in,  591 


!   Ephemeroptera,  eyes  of,  160 
Ephestia,  larva,  tropotaxis  in,  52,  53 
Epicrates,  lens,  389 
Epinephelus,  92 

colour  changes  in,  92 
Epiphysis.     See  Pineal  organ. 
Epomophorus,  choroidal  papilla?,  459 
Eptatretus,  degenerate  eyes  in,  734 
Equidse,  446 

ciliary  ganglion,  501 

cornea,  453 

corpora  nigra,  469 

optic  disc,  486 

pupil,  472 

See  also  Horse,  Ass,  Zebra. 
Erax  rufibarbis,  telotaxis  in,  56 
Ereniias,    transparent   eyelids   of,    366, 

367 
Ericymba,  visual  cells  of,  305 
Erinaceus.     See  Hedgehog. 
Eristalis,  telotaxis  in,  56 

tropotaxis  in,  55 
Erithacus,  visual  acuity  of,  663 

visual  responses  of,  664 
Ermine,  colour  changes  in,  21 

pupil,  472 
Errantia,  190 
Erythrominatin,  123 
Erythrophores,  88 
Eryx,  ciliary  venous  sinus,  386 
Esocidse,  cornea  of,  294 
Esox  lucius,  cornea  of,  295 
eye  of,  275 

visual  field,  binocular,  679 
Etmopterus,  eyes  of,  281 

pupil,  286 

threshold  to  light,  absolute,  616 

visual  cells,  288,  290,  611 
Eucalia,  threshold  to  light,  difference,  617 
Eucone  eye,  167 

Eudendrium  hydroid,  phototropic 
movements  of,  39 
jjigment  in,  120 
Eudyptes  cristatus,  40S 

iris,  408,  PI.  XI 
Euglena,  179,  180 

gracilis,  eye-spot,  126 

virilis,  eye-spot,  126 

klinotaxis  in,  45,  48,  49 
pigment  in,  120 

inigration  of,  85,  89 
spectral  sensitivity  of,  120 
Eunice,  ocelli  of,  191 


800 


INDEX 


Eupagurus,  58 

orientation  to  polarized  light  in,  73 
telotaxis  in,  56,  58 
Euphagus  cyanocephalus,   iris,   408 
Euphausiopsin,  121 
Eupolyodontes,  ocelli  of,  192 
Euproctis,  larva,  phototaxis  in,  46 
Eurypterids,  157 
eyes  of,  157 

origin  of  vertebrates  through,  233 
Euselachii,  279 
eyes  of,  282 
Eutheria.     See  Placentals. 
Evarcha  blancardi,  580 

vision  of,  580 
Evermanella,  tapetum,  non-occlusible,  305, 
608 
tubular  eyes  in,  324 
Exocone  eye,  168 

Extra-ocular  muscles.     See  Muscles. 
Eyebrows,  in  mammals,  492 
Eyelids,  characteristics  in 
anurans,  344 
birds,  423 
chelonians,  374 
crocodilians,  378 
lacertilians,  366 
monotremes,  436 
placentals,  491 
selachians,  289 
snakes.  392 
teleosteans,  311 
urodeles,  349 
movements  of,  in  vertebrates,  491 
third.     See  Nictitating  membrane. 
Eyes,  characteristics  in 
invertebrates,  125 
arachnids,  160,  211 
brachiopods,  195 
chsetognaths,  194 
ccelenterates,  182 
crustaceans,  163,  206 
echinoderms,  185 
insects,  166,  220 
molluscs,  196 
myriapods,  210 
Peripatus,  204 
polyzoa,  194 
rotifers,  194 
worms,  188,  190 
protochordates,  227 
vertebrates,  248 
amphibians,  333 


Eyes,  characteristics  in 
anurans,  334 
urodeles,  346 
birds,  397 
cyclostomes,  259 

ammocoete  larva,  261 
lamprey,  263 
fishes,  273 

chondrosteans,  315 
coelacanths,  314 
dipnoans,  312 
holocephalians,  290 
holosteans,  321 
selachians,  279 
teleosts,  291 
mammals,  429 
marsupials,  438 
monotremes,  431 
placentals,  446 
reptiles,  353 

chelonians,  368 
crocodilians,  375 
lacertilians,  355 
snakes,  383 
Sphenodon,  379 
amphibious,  in  fishes,  324 

in  insects,  224,  225 
cerebral,  of  rotifers,  194 

of  vertebrates,  237 
compound,  153 
acone,  167 
apposition,  169,  173 
composite,  160 
eucone,  167 
exocone,  168 
fast,  584,  706 
pseudocone,  167 
slow,  584,  706 
superposition,  169,  174 
degenerate,  721 
emergence  of  vertebrate,  242 
evolution  of  vertebrate,  233 
median,  711 

migratory,  in  fishes,  328 
ontogeny  of  vertebrate,  239 
parietal,  713 

phylogeny  of  vertebrate,  237 
pineal,  713 
rudimentary,  721 
simple,  129 
aggregate,  151 
composite,  152 
cupulate,  137 


INDEX 


801 


Eyes,  simple,  directional,  132 

flat,  136 

multicellular,  132 

ommatidial,  159 

pallial,  201 

subepithelial,  132 

unicellular,  130 

vesicular,  141 
stalked,  in  fishes,  326 

in  insects,  223,  225 

in  molluscs,  203 
telescopic.     See  tubular, 
tubular,  in  fishes,  322 

in  molluscs,  203 
Eye-shine,  608 
Eye-spot,  125 
of  Euglena,  126 

Marthasterias,  PI.  I 

Pouchetia,  126 
Eye-stalk,  of  crustaceans,  522,  523 

neuro-secretory  cells  in,  551 


Fabricia,  ocelli  of,  191 

Facet,  corneal,  157 

Faceted  eye.     See  Compound  ej'es. 

Facial  pit  of  vipers,  117,  599,  600 

Falciform  process,  of  holosteans,  321 

of  teleosteans,  298,  299 
Falco,  eye  of,  399 

binocular  vision  of,  684 

subbuteo,  iris,  408 

tinnunculus,  ciliary  venous  sinus,  408 
fundus,  410,  PI.  XII 
pecten,  413 
Falconiformes,  bifoveate  retina,  417 

shape  of  eyes,  402 

See  also  Eagles,  Hawks,  etc. 
Fasciola  hepatica,  187,  189 

larva,  ocelli  of,  189 
Fast  eyes,  in  insects,  584,  706 

visual  acuity  of,  588 
Feather-stars,  184 
Feeding  responses,  104 
Felidae,  445 

area  centralis,  485 

eye-shine,  608 

ocular  movements  in,  696 

optic  axis,  688 

pupils,  470 

retinal  vascularization,  479 

S.O. — VOL.  I. 


Felidse,  spatial  judgments  in,  704 

^ee  also  Cat,  Lion,  Tiger,  etc. 
Ferret,  445 

moulting  cycle  of,  21,  560 
pupils,  472 

reproductive  cycle  of,  18 
control  of,  559 
Fibrils,  intercellular,  in  protozoa,  511,  512 
Fiddler-crab.     See  Gelasimus,  Uca. 
Fighting  fish.     See  Betta. 
Filters,  intra-ocular,  656 
Fire-flies,  eyes  of,  168 

luminous  organs,  740,  742 
See  also  Lampyris,  Photinus. 
Fishes,  278 

accommodation  in,  645,  647 
angle  gamma  of,  677 
blinded,  behaviour  of,  598 
brain,  533 

transection  of,  534 
cave-,  725 

central  nervous  system,  532 
chemo -receptors,  598 
ciliary  ganglion,  501 
colour  changes  in,  82,  91 
control  of,  95,  537,  558 
vision  of,  624 

optoinotor  reaction  and,  623 
respiration  rate  and,  623 
deep-sea.     See  Deep-sea  fishes, 
distance,  judgment  of,  701 
electric  organs  in,  751 
eyes  of,  273  j5^. 
amphibious,  324 
degenerate,  723,  725,  734 
median,  713 
migratory,  328 
stalked,  326 
tubular,  322 
fore-brain,  543 

removal  of,  545 
hearing  of,  598 
interocular  transfer  in,  698 
iris,  contraction  to  light,  89 
lateral  geniculate  body,  541 

line  organs,  534,  598 
luminous  bacteria  in,  737 

organs  of,  737,  741,  743,  746 
median  eye,  713 
inid-brain,  535 

movement,  perception  of,  706 
neuro-endocrine  system,  557 
neuro-secretory  cells,  551 

61 


802 


INDEX 


Fishes,  ocular  movements  of,  691,  692 
voluntary,  693 
optic  lobes,  534 
thalamus,  540 
pupillary  reactions,  89,  700 
refraction  of,  638 
reproductive  cycle  in,  17 

control  of,  559 
size,  judgment  of,  701 
spatial  orientation,  701,  702 
tactile  sense  of,  598 
tapetvim,  occlusible,  612 
tectvnn,  534 
telencephalon,  543 
vibra.tory  receptors  in,  534,  598 
vision  of,  598,  599 
visual  acuity  of,  660 
fields,  aerial,  672 
binocular,  678,  679 
uniocular,  670,  671,  672 
pathways,  536,  543 
piginents,  121 
See  also  Selachians,  Teleosteans,  etc. 
Fissipedia,  445 

See  also  Felida?,  Canidse,  etc. 
Fitzroya  lineata,  colour  changes  in,  105 
Flagellata,  180 

metabolism  of,  510 
phototaxis  in,  48 
See  also  Euglena,  Volvox,  etc. 
Flat  eyes,  136 
Flat-fishes,  328 

colour  changes  in,  92 

colour  vision  and,  625 
migratory  eyes  in,  328 
twin  cones  in,  308 
visual  field,  binocular,  679 
See  also  Soleidse,  Pleuronectes,  etc. 
Flat-worms,  187 

See  also  Planarians,  etc. 
Fleas.     See  Aphaniptera. 
Flicker,  threshold  of,  in  insects,  584,  589 
Flies.     See  Diptera. 
FloccLili,  pupillary,  in  marsupials,  439 

in  placentals,  469 
Floral  initiation,  10 
Florigens,  549 
Flounders.     See    Pleuronectes,    Para- 

lichthys,  Psettodes. 
Fluorescence,  747 
Flying  fox,  442,  443,  607 
choroidal  papilla?,  459 
fundus,  PI.  XV 


Flying  fox,  retina,  corrugated,  642 
tapetum  in,  459 
lemur,  442,  443 
phalanger,  437 

retinal  circulation,  440 
tapetum  fibrosuin,  438,  609 
squirrel,  445 
fundus,  PI.  XV 
optic  disc,  486 
retinal  vascularization,  482 
tapetum  fibrosum,  458,  609 
visual  cells,  483 
Fontana's  spaces  (canals),  464 
Foraminifera,  179,  180 
Fore-brain,  532 

See  also  Diencephalon,  Telencephalon, 
Forficula,  218 

ommatidial  angle  in,  172 
phototaxis  in,  46 
scototaxis  in,  60 
Form  vision,  in  arthropods,  578 
cephalopods,  576 
insects,  588 
spiders,  580 
vertebrates,  637 
See  also  Visual  acuity. 
Fossorial  habit,    degenerate  eyes  due  to, 

728 
Fovea,  characteristics  in 
birds,  417,  420,  421 
lacertilians,  365 
placentals,  486 
snakes,  392 
Sphenodon,  382 
teleosts,  309 
turtles,  374 
function  of,  658 
occurrence  of,  659 
pure-cone,  in  birds,  422 

in  priinates,  486 
pure-rod  in  geckos,  365 

noctvirnal  23rimates,  486 
Sphenodon,  382 
teleosts,  310 
shape  of,  659 
Foveolse  opticae,  239,  240 
Fox  (Vulpes),  445 
cornea,  453 

flying.     See  Flying  fox. 
optic  axis,  688 

disc,  486 
pupils,  471 
Franz,  Victor  Julius,  273,  274 


INDEX 


803 


von  Frisch,  Karl,  566,  567 
Frogs,  334 

colour  changes  in,  97 
control  of,  558 
rhythmic,  20 
eyes  of,  334 j^. 
iris  pigmentation,  337 

control  of,  558 
retinal  pigment,  migration  of,  614 

control  of,  559 
See  also  Anurans,  Hyla,  Bana,  etc. 
Fulica,  visual  acuity,  663 
Fulmar  us  glacialis,  retina,  417 
Fundulus,  308 

area  centralis,  309 
colour  changes  in,  89,  91,  97 
double  cones,  307,  308 
migration  of  rods  and  cones  in,  616 
Fundus,  characteristics  in 
anurans,  341,  PI.  Ill 
birds,  410,  PI.  XII 
chelonians,  372,  PL  VII 
crocodilians,  378,  PI.  VIII 
lacertilians,  361,  PI.  VI 
marsupials,  439,  PI.  XIII 
monotremes.  436,  PL  XIII 
placentals,  478.  479,  PL  XIV,  XV 
snakes,  389,  PL  X 
Sphenodon,  382,  PL  VIII 
teleosteans,  306 
urodeles,  347,  PL  IV 
See  also  Retina. 
Fungi,  Iviminous,  737,  743 
Fungus-gnat    larva\   luminous  organs  in, 

740 
Fusion  frequency,  in  fishes,  626 
in  insects,  589 


G 


Gadfly.     See  Ancala,  Tabanus. 
Gadus  morrhua,  299 

annular  ligament,  295 
eye  of,  275 

falciform  process,  299 
fundus,  306 
twin  cones,  308 
Galago,  443 

fundus,  PL  XIV 
pupils,  472 
shape  of  eye,  448 
tapetum  cellulosum,  459 


Galago,  visual  cells,  482 

See  also  Lemuroids. 
Galeopithecus.     See  Flying  lemnr. 
Oaleorhinus,  eyelids,  289 

pupil,  286 
Galliformes,  shape  of  eye,  402 

See  also  Gallus,  etc. 
Gallus  domesticus,  ciliary  region,  403 
colour  vision  in,  630,  631 
Crampton's  muscle,  406 
eye  of,  400 

oil-droi^lets,  green,  420 
pecten,  414 

posterior  segment  of  eye,  404 
retina,  417 

size,  judgment  of,  703 
summation,  retinal,  660 
visual  acuity  of,  663 
Galvanotropism,  33 
Gamma  angle.     tS'ee  Angle  gamma. 
Gammarus,  blind  species,  722 

pulex,  oiumochronies  in,  123 
Ganglion,  cerebral.     See  Cerebral 

ganglion. 
Ganglionic  nervous  system,  517 
in  arthropods,  521 
molluscs,  527 
worms,  518 
Garrulus,  pecten,  412 
Gasterosteus  aculeatus,  84 
colour  changes  in,  84 
hue  discrimination,  619 
visual  responses,  627,  665 
Gastropacha  rubi,  eye  of.  159 
Gastropods,  196 
eyes  of,  197 
nervous  system,  527 
vision  of,  574 
Gavia,  accommodation  in,  643 

nictitating  membrane,  424 
Gavial,  375 

Gazelle  (Gazella),  444,  446 
corpora  nigra,  469,  470 
Geckos,  355,  356 
annular  pad,  361 
ciliary  body,  356 
cornea,  356 
diurnal,  eye  of,  605 
pupils,  359 
visual  cells,  364 
fovea,  365 
fundus,  361 
iris,  358 


804 


INDEX 


Geckos,  lacrimal  gland  absent,  368 
nocturnal,  accommodation  in,  651 
conus,  363 
eye  of,  605 
fovea  absent,  365 
pupils,  359 

retina,  pure -rod,  364,  610 
rods,  thickening  of,  611 
ocular  movements  in,  694 
pineal  organ,  716 
pupils,  359 

secondary  "  spectacle  ",  366 
visual  cells,  364,  643 
See  also  Gekko,  Hemidactylus,  etc. 
Oekko  gekko,  visual  pigments  in,  122,  252 
Qelasimus  arcuatus,  205 
Geniculate  body,  lateral,  541 
functions  of,  542 
in  mammals,  489,  490,  536 
in  vertebrates,  541 
Qeonemertes,  ocelli  of,  190 
Oeoplana  mexicana,  188 

ocelli  of,  188 
Geotria  australis,  260 

visual  cells  of,  269 
Geotropism,  33,  667 
Oeotrupes,  61 

colour  vision  of,  586 
menotaxis  in,  61 
Geranoaetus,  398 

binocular  field,  681 
Gerrhosaurus  grandis,  iris,  PI.  V 
Gibbon,  443 
fovea,  486 

See  also  Apes,  anthropoid;   Primates. 
Gigantactis,  luminous  organ  of,  745,  746 
Giganturus  chuni,  323 
tubular  eyes  of,  323 
visual  field,  binocular,  680 
Gillichthys  mirahilis,  visual  pigments  in, 

122 
Ginglymostoma,  pupil  of,  286 
Giraffe  {Giraffa),  444,  446 
angle  gamma  in,  677 
optic  axis,  688 
panoramic  field,  686 
Girella,  fovea  of,  310 
Glandula  pinealis,  711 
Glaucoma,  diencephalon  and,  560 
photoglycsemic  reflex  and,  560 
Glis.     See  Dormouse. 
Glossina,  45 

phototaxis  in,  45 


Glow-worm,  740,  742 
Goat  (Capra),  446 

area  centralis,  485 

blood  supply  to  eye,  500 

conjunctival  glands,  491 

corpora  nigra,  469,  470 

nictitating  membrane,  493 

visual  field,  binocular,  689 

wild,  corpora  nigra,  470 
Goat -sucker.     See  Caprimulgus. 
Gobiidae,  degenerate  eyes  in,  726 

See  also  Gobius,  Periophthalmus,  Typh- 
logobius,  etc. 
Gobius,  296 

membrana  vasculosa,  299 

niger,  cornea,  296 

poecilichthys,  membrana  vasculosa,  300 
Goldfish,  degeneration  of  eyes  in,  722 

telescope-eyed,  324 

threshold  to  light,  difference,  617 

visual  acuity,  660 

See  also  Carassius. 
Gonadotrophic  activities,  diencephalon 
and,  537 
hormonal  control  of,  550 
in  crustaceans,  555 
insects,  556 
vertebrates,  559 
photoperiodism  in,  16 
Gonatodes   fuscus,    pure-cone    retina    of, 

365 
Gonepteryx  rhamni,  colour  vision  of,  586 
Gonium,  eye-spot  in,  125 
Gonodactylus ,  60 

phototaxis  in,  43 

scototaxis  in,  60 
Goose.    See  Anser,  Cereopsis. 
Gorilla,  443 

binocular  vision,  687 

cornea,  453 

fovea,  486 

iris  vascularization,  468 
Goshawk.     See  Astur. 
Grasshoppers,  218 

accommodation  in,  591 

colour  changes  in,  94 

vision  of,  584 

See  also  Acrida. 
Gregarian  inertia,  73 
Grouse,  402 

shape  of  eye,  402 
Growth,  control  of,  555,  556,  560 

hormones  in  plants.     See  Auxins. 


I 


INDEX 


805 


Grua,  iris,  408 

ocular  movements,  696 
Guanine,  89,  608 

in  integument,  89 

invertebrate  eyes.     See.  Tapetum. 
vertebrate  eyes.     See  Argentea, 
Tapetum. 
Guanophores,  89 
Guinea-pig  {Cavia  porcellus),  445 

colour  vision  of,  633 

cornea,  453 

epithelium  of,  452 

gonadotrophic  hormone,  control  of,  559 

ii'is,  467 

lacrimal  passages,  494 

pineal  organ,  716 

refraction  of,  639 

retina,  rod-rich,  610 
vascularization  of,  480 

threshold  to  light,  difference,  618 

visual  cells,  483 

field,  uniocular,  672 
Gulls,  herring-.    See  Larus  argentatus. 

navigation  by,  64 

ocular  movements  in,  696 

retina,  419 

sphincter  muscle,  407 
Gulo.     See  Wolverine. 
Guppy.     See  Lehistes. 
Gurnard.     See  Trigla. 
Gymnophiona.     See  Apoda. 
Gymnothorax,  pupil  of,  304 
Gymnura,  brain,  533 
Gyrinid  beetle.     See  Whirligig  beetle. 


H 


Habituation,  to  light  stimuli,  36 
Hcemadipsa,  190 

ocelli  of,  134 
Hcemopis,  ocelli  of,  193 
Hagfishes,  259 

See  also  Myxiyie. 
Haideotritoyi,  degenerate  eyes  in,  728 
Haliaetus,  410 

fundus,  410 
Halicore.     See  Dugong. 
Haliotis,  ocellus  of,  137,  139 
Haller's  ratio,  401,  450 
Hangnest.     See  Cacicus. 
Hapalemur,  diurnality  of,  604 


Harder's  gland,  345,  494 
characteristics  in 
anurans,  345 
birds,  425 
chelonians,  375 
crocodilians,  378 
lacertilians,  367 
marsupials,  441 
monotremes,  437 
placentals,  494 
snakes,  393 
Sphenodon,  383 
Hare  (true),  445 
cornea,  453 

nictitating  membrane,  493 
optic  axis,  688 
calling,  445 

diurnality  of,  604 
jumping,  pupils,  612 
varying,  coloiu"  changes  in,  21 
control  of,  560 
pupils,  471 
Harvestman,  215 

eyes  of,  215 
Harvey,  E.  Newton,  736 
Hatchet -fish.    See  Argyropelecus . 
Hatter ia.     See  Sphenodon. 
Hawks,  417 

accommodation,  651 
distance,  judgment  of,  702 
foveae,  417,  659 
lens,  409 

scleral  cartilaginous  cup,  403 
visual  acuity,  662 
field,  binocular,  684 
trident,  684 
See  also  Accipiter,  Buteo. 
Hearing.     See  Auditory  sense. 
Hedgehog,  441,  442 
colour  vision  in,  633 
eyelids,  491 
fundus,  PI.  XV 
optic  disc,  486 
retina,  pvu'e-rod,  610 

vascularization  of,  479,  481 
visual  cells,  482 
Helianthus  (sunflower),   phototropism  in, 

41 
Heliodrilus,  conditioning  in,  573 
Heliophags,  123 
Heliotropism,  38 
Helix,  142 

circus  movements  in,  54 


806 


INDEX 


Helix 

eyes  of,  142,  197 
menotaxis  in,  61 

aspersa,  198 
eyes  of,  197 

pomatia,  ocellus  of,  142 
visual  cell,  128 
Heloderma,  359 

ocular  movements  of,  694 

pupils,  359 

retina,  365 

visual  cells,  364 
Helophiliis,  141 

ocellus  of,  140,  141 
Hemichordata,  227 

eyes  of,  227 

luminous  organs  in,  740 

nervous  system,  530 

See  also  Balanoglossus . 
Hemichromis  himaculatus,  colour  reactions, 

627 
Hemidactylus,  629 

colour  vision  in,  629 

turcicus,  fundus,  PI.  VI 
Hetnimysis,  telotaxis  in,  58 
Hemiptera,  218,  220 

accommodation,  static,  in,  591 

eyes  of,  167,  222,  224 

luminous  organs  of,  740 

nervous  system,  521,  522 

neuro -secretory  cells,  555 

See  also  Notonecta,  Aphis,  etc. 
Hen.     See  Gallus  domesticus. 
Herons,  binocular  vision,  675 

See  also  Ardea,  Nycticorax. 
Herpestes.     See  Mongoose, 
von  Hess,  Carl,  596,  597 
Hesse,  Richard,  112,  113 

organs  of,  230 
Heterauxin,  41 
Heterodon  jnodagascariensis,  fundus,  PI.  X 

pupils,  388 
Heterodontus,  286 

pupil  of,  286 
Heteropods,  199 

See  also  Pterotrachea,  etc. 
Heteroteuthis,  biokiminescence  in,   742 
Hind-brain,  532,  533 
lliodon,  visual  cells  of,  305 
Hippocampus,  310 
fovea  of,  309,  310 
ocular  movements,  693 


Hippolyte  varians,  91 

colour  changes  in,  91 
rhythmic,  20 
Hippopotamus,  445 
cilia  lacking,  492 
cornea,  453 
eyelids,  491 

lacrimal  passages  lacking,  494 
ocular  adnexa,  501 
optic  axis,  688 
visual  acuity  of,  654 
Hirudinea,  190 
Hirudo  medicinalis,  193 

ocelli  of,  133,  193 
Hirundo  rustica,  414 

binocular  vision,  683,  684 
colour  vision  in,  631 
foveae,  421 
pecten,  413,  414 
Holangiotic  retina,  479 
Holocephalians,  235,  278 
accommodation  in,  647 
eyes  of,  290 
pineal  organ,  713 
Holosteans,  235,  279,  321 
accominodation,  640,  647 
diurnality  of,  603 
eyes  of,  321 

See  also  Amia,  Lepklosteus. 
Holothuria,  185 
pigments  in,  117 
surinamensis,  sensitivity  of,  184 
Holothuroidea,  184 
sensitivity  of,  184 
Homalopsinge,  accommodation  in,  649 
Homarus,  206 

colour  changes  in,  95 
eyes  of,  164,  206 
vision  of,  578 
Homing,  in  ants,  68 
birds,  63,  703 
molluscs,  575 
wasps,  78 
pigeon,  64 

hue  discrimination  in,  619 
navigation  by,  64 
visual  acuity  of,  665 
Homochromatism,  83 
Honey  guides,  588 
Hormonal  system,  547 

See  also  Nevu'o -endocrine  system. 
Hormones,  549 

biokiminescence  and,  22 


INDEX 


807 


Hormones,  controlling  colour  changes,  92 
photoperiodism,  in  animals,  18 
in  plants,  12 
plant.     See  Auxins. 
See  also  Pituitary,  Sinus  gland. 
Hombill,  ocular  movements,  696 
Horse  {Equns  caballus),  446 
accommodation,  642,  643 
angle  gamma,  677 
anterior  chamber,  465 
area  centralis,  485 
blood  supply  to  eye,  500 
brain,  533 
cerebral  cortex,  543 
chiasma,  487 
cilia,  492 

colour  vision  in,  635 
conjunctiva,  491 
cornea,  453 

epithelium  of,  452 
corpora  nigra,  469 
eyes  of,  447,  449,  450 
lacrimal  gland,  493 

passages,  494 
nictitating  membrane,  493 
optic  axis,  688 
orbit,  498 

pectinate  ligament,  464 
Prejvalski's,  686 
pupils,  471 

reactions  of,  472 
ramp  retina,  642,  643 
refraction  of,  639 

retinal  vascularization,  478,  480,  481 
tapetum  fibrosum,  457,  458 
visual  acuity,  664 
field,  binocular.  689 
uniocular,  670,  672 
See  also  Equidae. 
Hovius.  circle  of,  472 
Humming  birds,  visual  acuity,  662 

See  also  Calypte. 
Humours,  four,  of  Aristotle,  549 
Hycena,  444,  445 
optic  axis,  688 
pupils,  470,  471,  612 
reactions  of,  472 
brunnea,  pupils,  470 
striata,  pupils,  470 
Hysenidse,  445 

Hyaloid  vessels,  in  anurans,  340 
birds,  415 
placentals,  476,  477 


Hyaloid  vessels,  in  snakes,  390 

teleosts,  299 
Hydra,  182 

dermatoptic  sensitivity  in,  32 

nerve-net,  515 

phototactic  reactions  of,  571 
Hydracarina,  eyes  of,  216 

vision  of,  579 
Hydrochoerus  capybara.     See  Capj'bara. 
Hydroides,  conditioning  of,  573 

reactions  of,  573 
Hydrophinse.  accommodation  in,  641,  649 

pupils,  612,  655 
Hydrotropism,  33 
Hydrozoa,  182 

>SVe  also  Hydra,  Obelia,  etc. 
Hygrobates,  eyes  of,  216 
Hyla,  334 

area  centralis,  344 

fundus,  341 

iris,  337 

movement,  perception  of,  705 

visual  acuity,  661 

arborea,  341 

colour  changes  in,  86,  105 
vision  in,  628 

ccerulea,  eyelids,  345 
iris,  PL  III 
pupil,  339 

vasta,  pupil,  339 
Hylobates.     See  Gibbon. 
Hymenolcemus  malacorhynchus,  binocular 

field,  687 
Hymenoptera,  219,  220 

neuro-endocrine  system,  555 

jS'ee  also  Apis,  Bombus,  Vespa,  etc. 
Hynobius,  scleral  cartilage  in,  347 
Hyperoodon.    See  Whale,  beaked. 
Hyperpiesine,  561 
Hypnarce,  electric  organ  of,  751 
Hypogeophis,  eyes  of,  730 
Hypopachus  incrassatus,   scleral  bone   in, 

335 
Hypophysis,  538,  557 
Hypothalamo -hypophyseal  system,  552, 

556 
Hypothalamus,  539 

hormones  and,  550 

reactions  of,  541 
Hypotony  and  hyperpituitarism,  561 
Hypsiglena,  retina,  pure-rod,  610 

visual  cells,  391 
Hypsiprymnus.     See  Kangaroo,  rat-. 


808 


INDEX 


Hyracoidea,  446 

See  also  Hyrax. 
Hyrax  (coney),  444,  446 

diurnality  of,  604 

retinal  vascularization,  480 

umbraculum,  469,  470 
Hystricomorpha,  445 

See  also  Porcupine,  Chinchilla,  Guinea- 
pig,  etc. 
Hystrix.     See  Porcupine. 


Ichthyomyzon,  260 

visual  cells  of,  269  '  - 

Ichthyophis,  730 

degenerate  eyes  in,  730 
Ichthyopsida.     See  Fishes  and  Amphi- 
bians. 
Idiacanthus  fasciola,  328 

larva.     See  Stylophthalmus . 
Idotea,  colour  changes,  rhythmic,  in,   20 
Iguana,  355 

accommodation  in,  651 
parietal  eye,  715 
visual  field,  binocular,  682 
tuherculata,  358 
iris,  358 

furrow,  337 
Impennes  (Sphenisciformes),  397,  398 
ocular  adnexa,  425 
movements,  696 
refraction,  639,  654 
See  also  Eudyptes,  Spheniscus. 
"  Imprinting  "  in  birds,  704 
Indris,  diurnality  of,  604 
Infra-red  rays,  sensitivity  to    in  vipers, 
117,  600 
visibility  of,  in  owls,  620,  630 
Infula,  in  retina  of  birds,  417 
Infundibular  organ,  of  Amphioxus,  229 
Infundibulum,  538 

Vesalius's  drawing  of,  549 
Insectivores,  441 
brain,  533 
cerebral  cortex,  543 
ciliary  region,  460 
colour  vision  in,  633 
diurnal,  604 
degenerate  eyes  in,  733 
nictitating  membrane,  493 
ocular  movements  of,  696 


Insectivores,  optic  axis,  688 
retinal  vascularization,  479 
vision  of,  601 
See  also  Mole,  Shrew,  etc. 
Insects,  217 

accommodation  in,  591 
bioluminescence  in,  740,  746 

rhythmic,  22 
blind,  722,  729,  734 
cerebral  ganglion,  521 

removal  of,  525 
chromatophores,  86 
colour  changes  in,  82,  93 
control  of,  555 
rhythmic,  20 
vision  in,  586 
dermal  sensitivity  in,  114 
eyes  of,  compound,  166,  224 

simple,  224 
inactivity  in  light,  7 
larvae  of,  nervous  system,  519 
ocelli,  222 
vision  of,  582 

See  also  Caterpillar,  Maggot, 
luminous  organs,   742,   746,   747 
metabolic  rhythms  in,  15 

control  of,  556 
nervous  system,  521,  522 
neuro -endocrine  system,  552,  555,  556 
ommochromes  in,  123 
orientation  of,  out-of-doors,  67 
reproductive  cycle  of,  17 

control  of,  556 
retinal  pigment  migration  in,  170 
control  of,  556 
rhythmic,  19 
time-memory  in,  22 
vision  of,  581 
visual  acuity  of,  588 
centres  in,  524,  525 
pigments  in,  121 
Instincts,  108 
Integumentary    pigment.     See    Pigment, 

integumentary. 
Interocular  transfer  of  impressions,  698 
Intra-ocular  filters,  656 

pressvire.     See  Ocular  tension. 
Intrascleral  plexus.     See  Circle  of  Hovius 

and  Canal  of  Schlemm. 
Invertebrates,  accommodation  in,  590 
eyes  of,  degenerate,  722,  724,  728,  733 
morphology,  113 
systematic  anatomy,  178 


INDEX 


809 


Invertebrates,  nervous  system,  511 
neuro -endocrine  system,  552 
vision  of,  570 

See  also  under  various  classes. 
lodopsin,  122 
Ipnops,  292,  724 

eyes  absent  in,  724 

luminous  organs,  724,  741 
agassizi,  724 
Iridocytes,  in  integument,  89 

iris,  469 

tapetum  cellulosvim,  459 
Iridophores,  in  sea-urchins,  185 
Iris,  characteristics  in 

Anableps,  324 

anurans,  337,  PI.  II 

birds,  407,  PI.  XI 

chelonians,  370,  PI.  VII 

chondrosteans,  317 

crocodilians,  376,  PI.  VIII 

dipnoans,  313 

holosteans,  321 

lacertilians,  357,  PI.  V 

lamprey,  267 

marsupials,  439 

monotremes,  435 

placentals,  468 

selachians,  285 

snakes,  386,  PI.  IX 

Sphenodon,  380,  381 

teleosts,  303,  PI.  II 

urodeles,  347,  PI.  IV 
cells,  in  crustaceans,  165 

in  insects,  168 
pillars,  464 
Isoptera,  218,  220 
Istiophorus,  pupils,  304 
Ixodides,  216 


•Jackal  (Canis  aureus),  445 

optic  disc,  486 

See  also  Carnivores,  Canidae. 
Jackdaw.     See  Corvus,  Coloelus  monedula. 
Jacobson's    organ,    in    lacertilians,    368, 
599 
in  snakes,  393,  599 
Jaguar  {Felis  onca),  445 

pupils,  471 

See  also  Felidae,  Carnivores. 
Jastrow  illusion,  703 


Jay.     See  Garrulus. 

blue.     See  Cyanocitta. 
Jellyfish,  182,  183 

bioluminescence  in,  739 
rhythmic,  22 
See  also  Pelagia  noctiluca. 

myo-epithelial  cell,  514 

nerve-net,  514 

nervous  control  of,  515 

sense  organs,  183 

See  also  Aurelia,  etc. 
Jerrymanders,  216 

eyes  of,  216 

vision  of,  579 
Johnson,  George  Lindsay,  428,  429 
Joseph,  cells  of,  229 
Julis,  fovea,  309 

ocular  movements  of,  693 
Julus,  circus  movements  in,  54 
Junco  hyemalis,  reproductive  cycle  in,  17 


K 


Kaloula  pulchra,  iris,  337 
Kangaroo,  437 

ciliary  processes,  439 

rat-,  fundus,  PL  XIII 

vision  in,  601 
Kappers,  Cornelius  Ubbo  Ariens,  508,  509 
Keratinization  of  cornea,  in  monotremes, 
433 
in  placentals,  456 
aquatic,  502 
Kestrel.    See  Falco  tinnunculus. 
Kinesis,  33 

See  also  Photokinesis,  etc. 
King-crab.     See  Limulus. 
Kingfishers,  bifoveate  retina,  418 

See  also  Alcedo,  Dacelo. 
Kiwi.     See  Apteryx. 
Klinokinesis,  31,  34 
Klinotaxis,  31,  47 

definition  of,  43 
Koala,  440 


Labrus,  ocular  movements,  693 
bergylta,  visual  pigments,  121 
Labyrinths,  534,  690 


810 


INDEX 


Lacerta,  accommodation  in,  651 
embryo,  median  eye,  712,  713 
extra-ocular  muscles,  368 
lens,  360 

median  eye,  715,  718 
transverse  muscle,  357 
visual  field,  binocular,  680,  682 
galloti,  fundus,  361 
monitor.     See  Varanus. 
muralis,  355 
conus,  362 
viridis,  conus,  363 
iris,  358 

ocular  movements  of,  694 
visual  responses,  665 
vivipara,  colour  vision  in,  629 
vulgaris,  conus,  362 
Lacertilians,  353 

accommodation  in,  651 
colour  changes  in,  88 
vision  in,  623,  628 
eyes  of,  355  j^^.,  356 

degenerate,  733 
fundi,  PI.  VI 
irides,  PI.  V 

migration  of  retinal  pigment  in,  614 
ocvilar  movements  in,  694 
olfactory  sense  of,  599 
parietal  eye,  715,  716 

function  of,  719 
pupils,  contractile,  612 
refraction  of,  639 
retina,  pure-cone,  611 
vision  of,  599 
visual  acviity  of,  661 

fields,  binocular,  680,  682 
uniocvilar,  672 
See   also   Iguana,    Lacerta,   Chameleon, 
etc. 
Lacewings,  219,  220 
Lacrimal  glands,  characteristics  in 
anurans,  345 
birds,  425 
chelonians,  375 
crocodilians,  378 
lacertilians,  367 
marsupials,  441 
monotremes,  437 
placentals,  493 
urodeles,  349 
passages,  characteristics  in 
anurans,  345 
birds,  425 


Lacrimal  passages,  characteristics  in 
crocodilians,  378 
placentals,  494 
snakes,  393 
Lcemargus,  281 

scleral  cartilage,  281 
Lagomorpha,  445 
angle  gamma,  677 
retinal  vascularization,  479 
vision  of,  601 
See  also  Hare,  Rabbit. 
Lagostomus.     See  Vizcacha. 
Lamellibranchs.     See  Bivalves. 
Lamina  cribrosa,  in  placentals,  487,488,489 

ganglionaris,  in  arthropods,  524 
Lamna  cornubica,  283 
iris,  285 
pupils,  287 
tapetum,  283 
Lampanyctus,  visual  cells  of,  305,  611 
Lampetra,  260 
activity  of,  34 
colour  changes  in,  95 

nervous  control  of,  537,  558 
rhythmic,  20 
fluviatilis,  260 
eyes  of,  265 

median,  716,  717 
optic  nerve,  270 
retina,  268 
visual  cells,  269 
planeri,  eye  of,  264 
Lamprey,  260 
eyes  of,  263 

median,  713,  714,  716,  717 
larva.     See  Ammocoetes. 
visual  field,  binocular,  678 
See  also  Cyclostomes,  Lampetra, 
Petromyzon. 
Lamprocolius  chalybeus,  iris,  407 
Lampropeltis  getulus,  iris,  387 

optic  disc,  390 
Lamp -shells.     See  Brachiopods. 
Lampyridae.     See  Lampyris,  Photinus. 
Lainpyris,  bioluminescence  in,  746 
compound  eyes  of,  168,  172 
nod  Hit  ca,  740 

splendidula,    luminous   organs   of,    736, 
742 
Lancelets,  228 

See  also  Amphioxus. 
Langur,  607 

colour  vision  in,  635 


INDEX 


811 


Lanius,  662 

visual  acuity,  662 
Lankester,  Edwin  Ray,  232,  233 
Lantern  flies,  luminous  organs  in,  740 
Lanthanotus,  eyelids,  366 
Laridae.    See  Gulls. 
Larus  argentatus,  pecten,  413,  414 

visual  responses,  665 
Lasius,  scototaxis  in,  60 

niger,  menotaxis  in,  69 
Lateral  geniculate  body.     See  Geniculate 
body. 

line  organs,  534,  690 
Latimeria,  235,  278,  315 

eyes  of,  314,  316 
Latrodectus,  84 

colour  changes  in,  84 
Laurence-Moon-Biedl  syndrome,  559 
Leander,  578 

colour  vision  in,  578 

pigments  in,  123 

retinal,  migration  of,  554 

reproduction,  control  of,  555 
Lehistes  reticulatus,  area  centralis,  309 

colour  changes  in,  96,  97 

migration  of  rods  and  cones,  614 
Leeches,  190 

colour  changes  in,  93 

light-shadow  reflex  in,  573 

ocelH,  131,  133 

See  also  Hirudo,  Hcemadipsa,  etc. 
Lemniscus,  lateral,  536 
Lemur  catta,  area  centralis,  485 
tapetum  cellulosum,  459 

macaco,  area  centralis,  485 

mongoz,  colour  blindness  of,  635 
Lemuroidea,  443 

See  also  Lemurs,  Loris,  Galago,  etc. 
Lemuroids,  nocturnal,  443 
retina,  pure-rod,  610 
shape  of  eye,  448 
tapetum  cellulosum,  459,  609 
visual  cells,  482 
See  also  Galago,  Loris,  etc. 
Lemurs  (true),  442,  443 

angle  gamma,  677 

area  centralis,  485 

colour  blindness  of,  635 

eye  of,  605 

flying.    See  Flying  lemur. 

optic  axis,  688 
Lens  (crystalline),  characteristics  in 
Anableps,  324 


Lens  (crystalline),  characteristics  in 
anurans,  340 
birds,  408,  409 
cephalopods,  144,  145 
chelonians,  372 
coelacanth,  315 
crocodilians,  377 
fishes,  276 

tubular-eyed,  323 
invertebrate    compound    eyes.      See 
Crystalline  cone, 
simple  eyes,  125,  127,  129 
lacertilians,  360,  361 
lamprey,  267 
marsupials,  439 
monotremes,  436 
placentals,  474 
selachians,  287 
snakes,  388 
Sphenodon,  381 
teleosts,  304 
urodeles.  347 
cuticular,  136,  138,  139,  140,  143 
deformation  of,  in  accommodation,  649 
movement  of,   in  accommodation,   644 
backward,  644 
forward,  647 
spherical,  occurrence  of,  606 
vertebrate,  origin  of,  246 
yellow,  occurrence  of,  656 
Lentiform  body  of  teleosteans,  299 
Leopard  (Felis  pardus),  445 
eyelids,  491 
pupils,  471 

See  also  Felidae,  Carnivores. 
Lepadogaster,  ocular  movements,  693 
Lepas,  208,  209 

adult,  degenerate  eyes,  722 
larva,  eyes  of,  209 
Lepidoptera,  219,  220 

larvae  of.     See  Caterpillar. 
See  also  Butterflies,  Moths. 
Lepidosiren,  312 
eyes  of,  312 
forebrain,  239 
retina,  pure-rod,  610 
Lepidosteus,  279,  321 

eyes  of.  321 
Lepisma,  218 

circus  movements  in,  54 
scototaxis  in,  60 
Lepomis,  hue  discrimination  in,  626 
threshold  to  light,  difference,  617 


812 


INDEX 


Lepomis 

visual  cells,  307 
Leptinotarsa,  219 

metabolic  rhythm  in,  16 
Leptodeira  annulata,  retina,  390 
Leptodora,  207 

eyes  of,  163,  209 
Leptognathus,  pupils,  304,  325 
Leptoplana,  187 

activity  of,  34,  572 
Lepus.     See  Hare. 
Leuckart's  ratio,  401 
Leucosolenia,  181 

light-sensitive  cells  in,  130,  181 
Levator  bulbi  muscle,  in  anurans,  345 

palpebrae  superioris,  in  placentals,  492 
Lid-fold,  in  teleosts,  311 
Lids.     See  Eyelids. 

Ligament.     See  Suspensory,  Annular,  etc. 
Light,  activation  by,  7,  34 
dermal  sensitivity  to,  113 
diffuse  reaction  to,  113 
effect  on  chromatophores,  89 
metabolism,  7 
movement,  27 
pigmentation,  19,  82 
inactivation  by,  7,  34 
perception  of,  602 
Light-compass  reaction,  61 
Light -differences,  discrimination  by  in- 
sects, 585 
by  vertebrates,  617 
Light-sense,  in  vertebrates,  602 
Light-sensitive  cells,  127,  130 
apolar,  128,  131,  133 
bipolar,  127,  130,  134 
in  tail  of  ammocoetes,  263 
Light-sensitivity,  102,  113 

in  man,  photoperiodism  in,  559 
Light-shadow  reflex,  45 
in  molluscs,  574 
in  worms,  572,  573 
Ligia,  95 

colour  changes  in,  95 

rhythmic,  20 
eyes  of,  165 
Lima,  eyes  of,  139,  201,  722 
Limax,  197 

maximus,  visual  cells  of,  128 
Limicoline  habit,  degenerate  eyes  due  to, 

724 
Limncea,  196 

nervous  system,  528 


Limnesia,  eyes  of,  216 
Limulus,  161,  211 
activity  of,  34 

eyes  of,  compoimd,  162,  212 
mechanism  of,  158 
median,  141,  162,  212 
rudimentary,  163,  212 

neuro -secretory  cells  in,  552 
neuro-endocrine  system,  552 
orientation  to  polarized  light  in,  66 
vision  of,  584 
visual  pigments  in,  121 
Lineus  ruber,  189 
ocelli  of,  189 
orientation  in,  75 
Linnaeus,  Carl,  8,  9 

flower-clock,  10 
Lion  (Felis  leo),  445 
angle  gamma  of,  677 
area  centralis,  485 
cornea,  453 

extra-ocular  muscles,  495 
pupils,  471 

See  also  Felidae,  Carnivores. 
Lipophores,  88 

Liihohius,  conditioning  of,  578 
Littorina  neritoides,  45 
phototaxis  in,  45 
Lizards.     See  Lacertilians. 
Lizzia,  183 

ocellus  of,  136 
Llama  {Lama),  444,  446 
corpora  nigra,  470 
See  also  Tylopoda,  Ungulates. 
Local  sign,  668 
Localization  in  space,  666 
egocentric,  668 
gravitational,  669 
Locusta,  69 

menotaxis  in,  69 
ommatidial  angle  in,  172 
optic  tracts,  526 
vision  of,  585 
migratoria,  ommochromes  in,  123 
optic  ganglia,  activity  of,  524 
telotaxis  in,  56 
Locusts,  gregariousness  in,  73 
reactions  of,  527 
vision  of,  583 

See  also  Locusta,  Schistocerca. 
Loeb,  Jacques,  26,  28 
Loligo,  145 

eyes  of,  145,  202 


INDEX 


813 


Loligo 

luminous  bacteria  in,  737 
pealii,  visual  pigment  in,  120 
'oulgaris,  202 
Lophortyx  calif ornicus,  417 

retina,  417 
Loris,  slender  {Loris  gracilis),  443 
tapetum  cellulosum,  459 
visual  cells,  482 
slow  (Nycticebus),  443 
pvipils,  472 
shape  of  eye,  448 
tapetum  cellulosum,  459 
See  also  Lemuroids,  Primates. 
Lota,  retina,  rod -rich,  610 
Loxia,  choroid,  404 
Loxodonta  africana.     See  Elephant, 

African. 
Luciferase,  736,  748 
Luciferin,  736,  748 
Lucifuga,  degenerate  eyes  in,  725 
Lucioperca,  migration  of  rods  and  cones  in, 

614 
Lumbriculus,  conditioning  of,  573 
Lumbricus  terrestris,  190 

cerebral  ganglion,  removal  of,  520 
conditioning  of,  573 
light-sense  of,  572 
metabolic  rhythm  in,  16 
nervous  system,  519 
ocelli  of,  128,  131,  190 
reactions  to  light,  53,  520 
tropotaxis  in,  53 
visual  pigment  in,  120 
Luminosity-curve,  in  insects,  585 
Luminous  bacteria,  737 
fungi,  737 
organs,  736 

in  arthropods,  740 
coelenterates,  739 
echinoderms,  739 
fishes,  737,  741 
molluscs,  740 
protochordates,  740 
worms,  739 
protozoa,  738 
Lung-fishes.     See  Dipnoans. 
Lutianus,  colour  preference  in,  624 
Lutra.     See  Otter. 
Lutreola.     See  Mink. 
Lycosa  agricola,  214 
eyes  of,  213 


Lycoteuthis  diadema,  740 

luminous  organs  in,  740 
Lygodactylus,  lens,  361 
Lymantria,  larvae,  form  vision  in,  582 

menotaxis  in,  61 
Lynx  (Felis  lynx),  444,  445 

eye  of,  447,  605 

See  also  Felidse,  Carnivores. 
Lytechinus,  protection  from  light  in,   39 


M 


Mabuya,  transparent  eyelids  in,  367 
Macaca   {Macacus).     See  ]\Ionkey, 
macaque. 

pileata.    See  Monkey,  toque. 

rhesus.    See  Monkey,  rhesus. 
Mackerels.     See  Scombrid*. 
Macrobrachium,  retinal  pigment,  migration 

of,  19 
Macrogenitosoma  prsecox,  719 
Macroglossa,  colour  vision  in,  587,  588 
Macronectes  giganteus,  fovea  and  infula, 

418 
Macropodidse,  437 

See  also  Kangaroo,  Wallaby. 
Macropus.     See  Kangaroo. 
Macroscelidee,  441 
Macula,  xanthophyll  in,   122 

yellow  pigment  of,  122,  656 

See  also  Retma,  Fovea,  Area  centralis. 
Maggots,  inactivation  by  light,  7,  34 

klinotaxis  in,  50,  51 

ocelli  of,  137,  139 
Magpie,  403 

shape  of  eye,  402 
Malacocephalus  Icevis,  bioluminescence  in, 

742,  746 
Malacostraca,  206 

Malopterurus,  electric  organ  of,  751 
Malpolon,  visual  field,  binocular,  684 
Mammals,  429 

accommodation  in,  652,  653 

angle  gamma  in,  676,  677 

brain,  533 

transection  of,  534 

central  nervous  system,  532 

cerebral  cortex,  543 
removal  of,  545 

ciliary  ganglion,  501 


814 


INDEX 


Mammals,  colour  changes  in,  seasonal,  21 
control  of,  560 
vision  in,  632 
ditirnal,  604 
eyes  of,  429  Jf. 

degenerate,  733 
habits  of,  604 

lateral  geniculate  body,  489,  541 
lens  capsule,  653 

elasticity  of,  652 
marsupial.     See  Marsupials, 
metabolic  rhythms  in,  13 

control  of,  560 
mid-brain,  536 
migration  of  retinal  pigment  in,  614 

of  visual  cells,  616 
monotreme.     See  Monotremes. 
movement,  perception  of,  705 
neopallium,  543 
neuro -endocrine  system,  557 
nocturnal,  604 
ocular  movements  of,  696 
optic  axis,  688 
lobes,  535 
thalamus,  540 
pineal  organ,  716 

function  of,  718,  719 
placental.     See  Placentals. 
primitive,  236 
pupillary  reactions  of,  700 
receptor-effector  system,  514 
refraction  of,  639 
reproductive  cycle  in,  18 
control  of,  559,  560 
spatial  judgments  of,  704 
tectum,  536 
telencephalon,  543 
threshold  to  light,  difference,  618 
vision  of,  600 
visual  acuity  of,  663 

field,  binocular,  687,  689 

uniocular,  672 
pathways,  540,  544 
Mammillo-infundibular  nuclevis,  557 
Manatee,  446,  502 

retinal  vascularization,  480 
See  also  Sirenians. 
Mandrill  (Mandrillus),  443 
refraction  of,  639 
See  also  Primates. 
Mangabey,  colour  vision  in,  635 
Mania.    See  Pangolin. 


Mantis  religiosa,  589 

eyes  of,  139,  225 

reactions  of,  526 

vision  of,  589 
Manx  shearwater.    See  Puffinus  puffinus. 
Manz,  glands  of,  in  mammals,  491 
Markhor,  reproductive  cycle  of,  18 
Marmosa.     See  Opossum,  mouse. 
Marmosets,  443 

eyes  of,  450 

fovea,  486 

See  also  Primates. 
Marmot,  442,  445 

cornea,  453 

eye  of,  447 

ocular  movements,  696 

optic  disc,  486 

pupils,  472 

retina,  pure-cone,  612 
vascularization  of,  479 

visual  acuity  of,  664 
cells,  483 
Marsupials,  429,  437 

accommodation  lacking  in,  640 

arhythmic,  604 

colour  vision  in,  632 

fundi,  PI.  XIII 

eyes  of,  438 

lateral  geniculate  body,  489,  490,  541 

nocturnal,  604 

optic  axis,  688 

refraction  of,  639 

vision  of,  601 
Marsupium.     See  Pecten. 
Marten  (Martes),  445 

colour  blindness  of,  634 

See  also  Mustelidae. 
Marthasterias  glacialis,  PI.  I 

eye-spot  of,  PL  I 
Martlet  (Chelidon),  visual  acuity  of,  662 
Mast,  Samuel  O.,  26,  29 
Mastigophora.     See  Flagellata. 
Mastigoproctus  giganteus,  activity  of,  34 
Matthiessen's  ratio,  277 
Mayflies.     See  Ephemeroptera. 
Mazes,  569,  624 

conditioning  by,  in  ants,  70 
crustaceans,  578,  579 
myriapods,  578 
snails,  575 
worms,  573 
Mechano-receptors,  116 


INDEX 


815 


Median  eyes,  711 

of  lamprey,  716,  717 
lizards,  716,  718 
Sphenodon,  716 
Medulla,  external,  524 

internal,  524 

tenninal,  524 
MedusEe,  182 

nerve-trunks  in,  516 

See  also  Jellyfish. 
Medusoids,  182 

sense-organs  of,  182 
Megabunus  diadema,  215 
Megachiroptera,  443 

choroidal  papillte,  459 

corrugated  retina,  643 

retinal  tapetum,  459,  608 

See  also  Flying  fox. 
Megalobatrachus  7naximus,  349 

eyes  of,  349 
Meganyctiphanes,  bioluminescence  in,  740 
Megaptera.     See  Whale,  hump-back. 
MegerUa,  eyes  of,  195 
Meibomian  glands,  in  placentals,  491 
Melanerpes  erythrocephahis,  pecten,  412 
Melanin,  89,  118 
Melanoblasts,  118 
Melanophores,  87 

in  iris,  of  anurans,  337 
of  snakes,  386 

in  sclera,  of  snakes,  385 
Melanoplus,  electroretinographic   re- 
sponses, 586 
Meleagris  gallipavo,  retina,  417 
Meles.     See  Badger. 
Melopsittacus  undulatus,  iris,  407 
Melursus.     See  Bear,  sloth-. 
Membrana  vaseulosa  retinae,  482 
in  anurans,  341 
dipnoans,  313 
holosteans,  321 
pol;y^terini,  320 
snakes,  290 
teleosts,  299,  300 
Menotaxis,  31,  60 

definition  of,  44 
Merangiotic  retina,  479 
Mesencephalon.     See  Mid-brain. 
Metabolism,  diurnal  rhythm  of,  13 

effect  of  light  on,  7 

regulation  of,  555,  556,  560 
Metazoa,  181 
Metencephalon,  532 


Metopoceros  cornutus,  conus,  363 

fundus,  361,  PI.  VI 
Metndium,  phototactic  reactions  of,  571 
Microchiroptera,  443 

See  also  Vampire  bat,  Vespertilio. 
Micrococcus  pJwsplwreus,  luminescence  of, 

738 
Micropus  apus,  407 

ciliary  muscle,  407 

fovea,  418 

pecten,  412 
Microspira  photogenica,  luminescence  of, 

738 
Microtus.     See  Vole,  field-. 
Mid-brain,  532,  534 
Migration  of  birds,  17 

of  pigment.    See  Pigment,  migration  of. 

of  rods   and   cones.     See   Visual   cells, 
migration  of. 
Migratory  eyes  in  fishes,  328 
Millipede,  210 

eyes  of,  210 

See  also  Myriapods. 
Milvus,  420 

green  oil-droplets,  420 
Mimicry,  83 
Mimosa  pudica  (sensitive  plant),  response 

to  light,  511 
Mink,  pvipils,  472 
Minnow.     See  Phoxinus. 
Miopiesine,  561 
Misgurnus,  310 

optic  nerve,  310 
Mites,  216 

eyes  of,  216 

water,  eyes  of,  216 
Mitosis,  diurnal  rhythm  in,  13 
Mneyniopsis,  bioluminescence  in,  748 
Mnemotaxis,  31,  78 

definition  of,  44 
Moa,  604 

extinction  of,  604 
Mobulida?,  pupils,  287 
Mole  (true),  441 

eyes  of,  732,  733 
optic  axis,  688 

disc,  486 
retinal  vascularization,  479,  481 

golden,  442,  443 
eyes  of,  733 

marsupial,  437 
eyes  of,  733 
scleral  cartilaginous  nodules,  438 


816 


INDEX 


Mole,  rodent,  eyes  of,  733 

water.     See  Desman. 
Moll's  glands,  in  placentals,  492 
Molluscs,  195 

accommodation  in,  590 

blind,  723,  729 

cerebral  ganglion,  527,  528 

activity  of,  524 
deep-sea.     See  Deep-sea  molluscs, 
dermal  sensitivity  in,  114 
eyes  of,  196 

degenerate,  723 
inverted  retina  in,  147 
luminous  organs  in,  737,  740,  746 
metabolic  rhythms  in,  15 
nerve-net,  515,  516 
nervous  system,  527,  528 
neuro -endocrine  system,  550 
neuro -secretory  cells,  552 
reproductive  cycle  in,  17 
vision  of,  574 
visual  centres,  529 
See  also  Cephalopods,  etc. 
Mongoose,  445,  472 

pupils,  472 
Monkeys,  443 
capuchin,  443 

colour  vision  in,  635 

lens  capsule,  653 

visual  acuity  of,  665 
howling,  443 
macaque,  443 

iris  vascularization,  468 

nictitating  membrane,  493 

pupillary  reactions,  472 

retractor  bulbi,  495,  496 
New  World,  443 
nocturnal.     See  Nyctipithecus. 
Old  World,  443 
rhesus,  colour  vision  in,  635 

fovea,  486 

retina,  483 

visual  acviity  of,  665 
spider,  443,  689 

colour  vision  in,  635 
toque,  fundus,  PI.  XIV 
Monodon.     See  Narwhal. 
Monotremes,  429,  431 

accommodation  lacking  in,  640 
colour  vision  in,  632 
eyes  of,  431  j^. 
fundi,  PL  XIII 
nocturnality  of,  604 


Monotremes,  optic  axis,  688 

vision  of,  600 
Moon,  navigation  by,  73 
Mordacia,  260 

eyes  of,  265 
Mormyridae,  294 

scleral  cartilage  in,  294 
Mosaic,  retinal,  656,  705 

theory,  155,  170 
Mosquitoes,  eyes  of,  220 

orientation  to  polarized  light,  66 

See  also  Diptera,  Aedes,  Culex,  etc. 
Motacilla  alba,  660 

summation,  retinal,  660 
Moths,  219,  581 

behaviour  of,  63 

eyes  of,  159 

olfactory  sense  of,  581 

retinal  pigment,  migration  of,  170 

vision  of,  585 
Moulting,   photoperiodism  and,    21,   555, 

556,  560 
Mouse,  445 

colour  blindness  of,  633 

eyelids,  491 

field-,  colour  blindness  of,  633 

Harder's  gland,  494 

lacrimal  gland  absent,  493 

Moll's  gland  absent,  492 

ocular  movements  of,  696 

optic  axis,  688 
nerve-head,  488 

photoperiodism  in,  18 

refraction  of,  639 

retina,  rod-rich,  610 

vascularization  of,  479,  481 

visual  acuity,  663 
cells,  483 
Movement,  perception  of,  in  cephalopods, 
576 
in  insects,  589 
vertebrates,  705 

stroboscopic,  706 
Movements,    ocular.     See    Ocular    move- 
ments. 
Mucopolysaccharide,  in  anterior  chamber 

of  owls,  404 
Mugil,  colour  preference  in,  625 

eyelids,  311 

ocular  movements  in,  693 

corsida,  accommodation  in,  654 
Muller  (H),  fibres  (cells)  of,  248 
development  of,  240 


INDEX 


817 


Miiller  (H),  muscle  of  (ciliary),  in  birds, 
406 
(orbital),  in  mammals,  496 
(palpebral),  in  mammals,  492 
Johannes,  154 
Miiller-Lyer  illusion,  703 
Murex,  197 

ocelli  of,  142,  197 
regeneration  of  eye,  136 
Miis.     See  Mouse. 
Musca  domestica,  172 
eyes  of,  167,  172 
maggot  of,  50 
klinotaxis  in,  50 
ocellus  of,  137,  139 
visual  acuity  of,  588 
Muscles,    extra-ocular,    characteristics    in 
aniu-ans,  345 
birds,  424,  425 
fishes,  277,  278,  691 
hammerhead  shark,  327 
lacertilians,  368 
lamprey,  271 
m.onotreines,  437 
placentals,  494,  495 
selachians,  290 
teleosts,  312 
See  also   under  various   }nuscles. 
Mustela  erminea.     See  Ermine. 

nivalis.     See  Weasel. 
Mustelida?,  445 

lacrimal  passages  absent,  494 
nictitating  membrane,  493 
pupils,  472 
Alustelus,  285 

area  centralis,  289 
chromatophores,  96 
pupils,  285,  286 
tapetum,  283 
visual  cells,  288 
antarcticus,  pupil  of,  286 
My  a  arenaria,  131 

light -shadow  reflex  in,  574 
ocelli  of,  131,  200 
visual  pigment  in,  120 
Myelencephalon,  532 
Myliobatis,  283 
eyes,  281 
pupils,  287 
visual  cells,  288 
Myocastor  coypus.     See  Coypu. 
Myo-epithelial  cells,  513,  514 
Myogale.     See  Desman. 

S.O.-  VOL.  I. 


Myomorpha,  445 

See  also  Mouse,  Kat,  etc. 
Myriapods,  210 

blind,  729 

eyes  of,  151,  210 

luminous  organs  in,  740,  745 

neuro -endocrine  system,  552 

vision  of,  578 

visual  centres,  524 
Myrmecobiiis.     See  Ant-eater,   banded. 
MyrmecopJiaga.     See  Ant-eater,  giant. 
Mysids,  58 

telotaxis  in,  58 
Mystacoceti,  446 
Mytilus,  200 

sense  organs  of,  200 
Myxicola  cesthetica,  ocelli  of,  191 
Myxine  gluiinosa,  114,  734 

degenerate  eyes  of,  734 

dermal  sensitivity  of,  114 

secretory  mechanism  of,  267 
Myxinoids,  degenerate  eyes  in,  734 

labyrinths,  534 

median  eyes  absent,  713 

See  also  Bdellostoma,  Myxine. 
Myzus,  colour  vision  of,  587 


N 


Naja  tripudians,  386 

fundus,  PI.  X 
Narwhal,  446 
Nasal  asymmetry,  674 
Nasua.     See  Coati. 
Native  cat.    See  Dasyure. 
Natrix.     See  Tropidonotus. 
Nautilus,  130 

ocellus  of,  137,  201 
Navigation  by  birds,  64 

pecten  and,  416 
Necrojjhorus,  219 

eyes  of,  172 
Necturus,  349 

eyes  of,  349 

violet  rods,  350 
Nematodes,  187 

sense  organs  of,  190,  734 
Nemertines,  187 

bioluminescence  in,  739 

nervous  system,  519 

sense  organs  of,  189 
Nemestrinus,  colour  vision  in,  635 


818 


INDEX 


Neoceratodus,  312 
eyes  of,  312 
retina,  pvire-cone,  611 
Neodiprion,  orientation  to  i:iolarized  light 
in,  66 
telotaxis  in,  57 
Neognathfp.     See  Carinata:>. 
Neopallium,  543 
Nereis,  190,  191 

cerebral  ganglion,  removal  of,  520 
conditioning  of,  573 
nervous  system,  520 
ocelli  of,  isS,  191 
Nerve  trunk-pathways,  513,   516 
in  coelenterates,  516 
echincderins,  516 
Nerve-net,  subepithelial,  512,  514 
in  balanoglossids.  515,  517 
coelenterates,  512.  514,  515 
m.olluscs,  515 
worms,  515,  518,  520 
Nerves.     See  tmder  various  nerves  (Optic, 

Corneal,  etc.). 
Nervous  system,  511 
characteristics  in 

arthropods,  521,  522 
coelenterates,  514,  515 
echinoderms,  516 
molluscs,  527,  528 
protochordates,  530 
vertebrates,  530 
worms.  518,  519,  520 
central,  530 

development  of,  531 
evolution  of,  512 
ganglionic,  517 
Neurobiotaxis,  509,  699 
Neuro -endocrine  systein,  550 
of  crustaceans,  552 
insects,  555 
vertebrates,  556 
function  of,  558 
Neurohumoral  activity,  550 
Neurohypophysis.     See  Hypophysis. 
Neuropile,  518 
Neuroptera,  219,  220 
Nevirosecretion,  550 
Neurosecretory  cells,  550,  551 
Newts,  346 

See  also  Urodeles,  Triturus. 
Nictitating   membrane,    characteristics   in 
birds,  423,  424 
chelonians,  374 


Nictitating   membrane,   characteristics   in 
crocodilian*^,  378 
lacertilians,  367 
marsupials,  441 
placentals,  492 
platypus,  437 
selachians,  289 
Sphenodon,  383 
false,  in  teleosts,  312 

in  anurans,  345 
interposition  of,   in   accominodation, 
643 
Night -jar.     See  Caprinmlgus. 
Noctiluca,  179,  180,  738 
luminescence  of,  738 
miliaris,  luminescence  of,  738 
Nocturnal  animals,  602,  721 
eye,  characteristics  of,  605 
retina  of,  609,  610 
Notechis,  eye  of,  385 

anterior  segment,  386 
visual  acuity  of,  657 
Notonecta,  73 

circus  movements  in,  54 
colour  vision  of,  587 
migration  of  visual  cells,  170,  614 
orientation  of,  73 
Notoryctes  typhlops.     See  Mole,  marsupial. 
Notropis,  colour  vision  in,  625 
Nucleus  lateralis,  557 

pre-opticus,  557 
Nudibranchs,  196 

bioluminescence  in,  740 
Numida  pucherani,  retina,  417 
Nycticebus.     See  Loris,  slow. 
Nycticorax,  413 

pecten,  413 
Nyctipithecus,  443 
area  centralis,  485 
fovea,  pure-rod,  486 
nocturnal ity  of,  604 
retina,  pure-rod,  482,  610 
tapetviin  fibrosum,  458,  609 


O 


Obelia,  182 

Ocellus.     See  Eye,  simj^le. 
Octavus  system,  535 
Octopus,  93 

colour  changes  in,  85,  92,  93 

conditioning  of,  576 

eyes  of,  144,  202 


INDEX 


819 


Octopus 

optic  lobes,  529 
reactions  of,  528 
vision  of,  575 
vulgaris,  202 
Ocular  movements,  689 
involuntary,  690 
voluntary.  692 

in  amphibians,  345,  694 
birds,  425.  695 
chelonians,  374 
fishes,  278,  693 
lacertilians,  368 
mammals.  497,  696 

co-ordination  of,  693 
reptiles,  694 
snakes,  393 
tension,  diencephalon  and,  560 
diurnal  rhythm  in,  14,  561 
Oculiferous     tubercle,      in      harvestmen, 
215 
j errymanders,  216 
sea-spiders,  217 
Oculoir.otor  centres,  534 

nuclei,  535,  699 
Ocydpoda  ippens,  205 
Odonata,  220,  225 
eyes  of,  222,  225 
See  also  Aeschna.  Anax. 
Odontoceti,  446 

Odontosyllis,  bioluminescence  in,  741 
(Edicnenius,  pecten,  412 
Oil-droplets,  colour  vision  and,  631 

occurrence  of,  631,  656 
Okapi  (Okapia),  nictitating  membrane, 

496 
Olfactory  centres,  543 
sense,  of  bees,  588 
birds,  600 
fishes,  598 
gastropods,  574 
insects,  581 
mammals,  601,  733 
reptiles,  599 
predominance  of,  103 
spatial  judgments  and,  667 
Oligochaetes,  190 

bioluminescence  in,  739 
conditioning  of,  573 
nervous  system,  519 
ocelli,  190 
See  also  Lumbricus. 


Ommatidial  angle,  172,  173 
eye.     See  Compound  eyes, 
simple,  159 
Ommatidium,  155 
Ommatin,  123 
Ommin,  123 
Ommochromes,  123 
Onchidiuyn,  199 

accommodation  in,  590 
eyes  of,  148,  199 
homing  ability  of,  575 
Oniscus,  metabolic  rhythm  in,  15 
Ontogeny  of  vertebrate  eye,  239,  240 
Onychophores,  204 
eyes  of,  205 

degenerate,  724 
nervous  system,  521 
vision  of,  578 
See  also  Peripatus. 
Operculum  (pupillary).  612 
in  catfishes,  304,  329 
flat-fishes.  329 
mammals,  469,  470 
selachians,  287 
Ophidians,  353 

accommodation  in,  648 
colour  training  of,  628 
eyes  of,  373  j^.,  385 

degenerate,  731 
fundi,  PL  X 
irides,  PI.  IX 

ocular  movements,  694,  695 
olfactory  sense  in,  599 
pineal  organ,  716 
pupils,  contractile,  612 
refraction  of,  629 
vibi'atory  sense  in,  599 
vision  of,  599 
visual  acuity  of,  661 
field,  binocular,  682 
Ophiops,  eyelids  in,  366,  367 
Ophiotettix,  223 

Ophisauriis  ventralis,  fundus,  362 
Ophiuroidea,  184 

Ophrycessa  superciliosa,  iris,  PL  V 
'    Ophthalmic  artery,  in  anurans,  340 
j  in  placentals,  498 

[    Opiliones.     See  Phalangida. 
j    Opisthobranchs,  196 
!        neuro -secretory  cells,  552 

Opisthoproctus,  324 
j        tubular  eyes  of,  324 
1        visual  field,  binocular,  680 


820 


INDEX 


Opossum,  437 

Australian,  lateral  geniculate  body,  489, 
490 
pupils,  612 
eye  of,  605 
mouse,  ciliary  muscles,  439 

visvial  cells,  441 
Virginian,  439 

ciliary  muscles,  439 
colour  blindness  of,  633 
fundus,  PI.  XIII 
nictitating  membrane,  441 
optic  axis,  688 
retinal  circulation,  440 
tapetum,  440,  608 
visual  acuity  of,  665 
Optic  axis,  675,  688 

chiasma.     See  Chiasmal  decussation, 
disc,  characteristics  in 
birds,  410 
chelonians,  372 
crocodilians,  378 
lacertilians,  362 
marsupials,  440 
monotremes,  436 
placentals,  486 
polypterini,  320 
selachians,  288 
snakes,  390 
Sphenodon,  381 
teleosts,  310 
urodeles,  347 
ganglia,  in  arthropods,  523,  524,  525 
lobes,  of  arthropods,  521,  525,  526,  584 
of  birds,  535 

cephalopods,  528,  529,  576 
fishes,  534 
mammals,  535 
reptiles,  535 
norve,  characteristics  in 
anurans,  344 
birds,  422 
crocodilians.  378 
dipnoans,  313 
holosteans,  322 
lacertilians,  366 
lamprey,  270 
monotremes,  436 
placentals,  486,  488 
selachians,  288 
snakes,  392 
Sphenodon.  383 
teleosts,  310 


Optic  nerve,  characteristics  in 
urodeles,  350 
decvissation  of  fibres.     See  Chiasmal 

decussation, 
septal  system  of,  487 
pedicle,  in  selachians,  290 
pits,  239 
thalamus,  538 
vesicles,  239,  537,  711 
Optical  system,  of  vertebrates,  605,  638 

duplicated,  641 
Optics  of  compound  eye,  170 
Optomotor  reaction,  568 
in  crustaceans,  578 
insects,  73,  583,  584 
colour  vision  and,  587 
light -differences  and,  585 
visual  acuity  and,  588,  589 
spiders,  580 

vertebrates,  colour  vision  and,  623 
movement,    perception   of,  and, 
706 
Orang-utan,  443 

See  also  Apes,  Primates. 
Orbicularis  oculi,  in  placentals,  492 
Orbit,  characteristics  in 
anurans,  346 
birds,  423,  424,  425 
chelonians,  375 
crocodilians,  378 
hammerhead  shark,  327 
lacertilians,  368 
lamprey,  270 
monotremes,  437 
placentals,  497 
selachians,  290 
snakes,  393 
Sphenodon,  383 
teleosteans,  312 
Orbital  axis,  675,  676 

ganglion.     See  Ciliary  ganglion, 
nerves,  in  placentals,  5i31 
sinus,  in  rabbit,  500 
Orca.     See  Whale,  killer 
Orectolobus,  pupil,  286 
Organelle,  129 

Orientation  angle,  in  menotaxis,  61 
to  light,  27 

methods  of,  31 

See  Phototaxis,  etc. 
of  insects,  67 
of  plants,  27 
polarized,  66 


INDEX 


821 


Orientation,  to  visual  pattern,  73 

visual,  667 
Ornithorhynchus.     See  Platypus. 
Orthokinesis,  34 
Orthoptera,  218,  220 
eyes  of,  223 

See    also    Blattella,    Loc^tsta,   Di.vippus, 
etc. 
Orycteropiis.     See  Aard-vark. 
Oryctolagus.     See  Rabbit. 
Os  opticus  of  birds,  403 
Osseous    plaques     (scleral),     in    chondro- 
steans,  317 
in  Latimeria,  315 
Ossicle  of  Gemminger,  in  birds,  403 
Ossicles,  scleral,  accommodation  and,  649 
in  birds,  403 
chelonians,  369 
lacertilians,  356 
Sphenodon,  380 
teleosts,  294 
occurrence  of,  450 
Osteichthyes,  234,  235,  278 
eyes  of,' 291 

See  olso  Teleosteans,  etc. 
Osteolcemus  tetraspis,  iris,  PL  VIII 
Ostracods,  207 
eyes  of,  209 

luminous  organs  in,  740,  746 
See  also  Cypris,  etc. 
Ostrich,  African.     See  St  ruth  io. 
American.     See  Rhea. 
eye  of,  399 
Otariidae.     See  Sea-lions. 
Otter,  445 

accommodation  in,  654,  655 
optic  axis,  688 
shrew.     See  Shrew,  otter-, 
sphincter  muscle,  468 
Otus  bakkamcena,  iris,   PI.  XI 
Owls,  ciliary  muscle,  407 
colour  vision  in,  630 
eyes  of,  399,  605 
immobility  of,  695 
shape  of,  402 
fovea,  417,  418 
iris,  407 
lens,  409 
pecten,  411 
threshold  to  light,  674 

absolute,  617 
visibility  to  infra-red,  620,  630 


Owls,  visual  acuity  of,  662 

field,  binocular,  682,  683,  684 
uniocular,  670,  672 
See  also  Bubo,  Otus,  Strix. 
Ox.     See  Cattle. 
Oxybelis,  iris,  371 
Oysters,  196 

light-shadow  reflex,  574 
pearl.     See  Avicula. 


Pachydactylus  niaculatus,  eyelids  lacking 

in,  367 
Palcemon,  colour  changes  in,  91 

rhythmic,  20 
Palcemonetes,  colour  changes  in,  94 

retinal  pigment,  migration  of,  555 
Palfeocortex,  543 
Palseognatha?.     See  Ratitse. 
Pallial  eyes,  in  bivalves,  201 
Pan.     See  Chimpanzee. 
Panda  {Ailurus),  445 
pupils,  471 
giant  (Ailuropoda),  nictitating  mem- 
brane, 493 
Pandalus,  visual  pigments  in,  121 
Pangolin,  442,  445 

Pantodon,  visvxal  field,  binocular,  680 
Pantopoda.     See  Pycnogonida. 
Papio.     See  Baboon. 
Paracentrotus  Hindus,  sensitivity  of,  184 
Paralichthys  albiguttus,  colour  changes  in, 

92 
Paramoecium,  179,  180 
geotaxis  in,  45 
klinokinesis  in,  36 

modified  by  electric  shock,  571 
bursar  is,  reproductive  cycle  in,  16 
Paraj^ineal  organ.     See  Parietal  organ. 
Parasites,    external,    degenerate   eyes   in, 
734 
internal,  degenerate  eyes  in,  733 
Paraventricular  nucleus,  557 
Parazoa,  181 

See  also  Leucosolenia. 
Parietal  eye,  of  lamprey,  713,  716,  717 
lizard,  715,  716,  718 
Sphenodon,  715,  716 
origin  of,  242 
foramen,  in  Sphenodon,  715 
organ,  538,  713 


822 


INDEX 


Parietal  organ,  accessory,  715 

function  of,  719 
Parrots,  eyelids,  424 

eyes  of,  399 

ocular  movements  of,  696 

reproductive  cycle  in,  17 

visual  field,  binocular,  684,  685 

See  also  Chrysotis. 
Pars  intercerebralis,  in  insects,  555 
Parus,  panoramic  vision  in,  683 

visual  acuity,  663 
Passer  domesticus,  408 

ciliary  venous  sinus,  408 

colour  vision  of,  630,  632 

orbit  and  brain,  424 

reprodvictive  cycle  in,  17 

summation,  retinal,  660 

visual  acuity  of,  662 
cells,  419 
Passeriformes,  accommodation  in,   651 

bifoveate  retina,  418 

eyes,  shape  of,  402 

pecten,  412 

time-memory  in,  22 

See  also  Corvidse,  Hirundo,  Passer,  etc. 
Passerita  prasina,  674 
iris,  PI.  IX 
pupil,  388,  PI.  IX 
visual  field,  binocular,  684 
Patella,  197 

homing  ability  of,  575 

ocelli,  137,  197 
Paurangiotic  retina,  480 
Pauropus,  211 

eyes  lacking  in,  729 
Pearl-fish.    See  Encheliophis. 
Pearly  nautilus.     See  Nautilus. 
Peccary  (Dicotyles),  445,  458 

See  also  Suoidea. 
Pecora.     See  Ruminants. 
Pecten  of  birds,  410 

function  of,  415 

histology  of,  414 

pleated  type,  411,  412 

vaned  type,  411 
Pecten  (scallop),  200 

ocelli  of,  148,  200 

sensory  reactions  of,  103 

vision  of,  575 
Pectinate  ligament,  characteristics  in 
chelonians,  372 
crocodilians,  376 
lacertilians,  359 


Pectinate  ligament,  characteristics  in 
marsupials,  439 
placentals,  463,  464,  469 
Pectunculus,  ocelli  of,  151,  201 
Pediculus,  218 
ocelli  of,  139 
scototaxis  in,  60 
Pedipalpi,  214 

See  also  Whip-scorpions. 
Pedunculate  body,  in  arthropods,  521,  524 
Pelagia,  my o -epithelial  cells  in,  513 

noctiluca,  bioluminescence  in,  739,  744, 
745,  748 
rhythmic,  22,  747 
Pelecanus,  410 

conspic Hiatus,  fundus,  410 
Pelobates  fuscus,  pupils,  339 
Pelomyxa,  effect  of  light  on,  7 

latent  period  in,  36 
Penguin,  398 

rock-hopper.     See  Eudyptes. 
See  also  Impennes. 
Peragale.     See  Bandicoot,  rabbit, 
Perameles.     See  Bandicoot. 
Perca,  ocular  movements  of,  692 

fluviatilis,  optomotor  reaction  of,  706 
Perception  of  colour,  619 
depth,  667 
form,  637 
light,  602 
movement,  705 
size,  667 
space,  666 
Perch.    See  Perca. 

climbing.    See  Anabas. 
Percidse,  retinal  tapetum  in,  305,  612 

See  also  Perca,  Lucioperca. 
Perichceta,  phototaxis,  in,  45 
Periophthalmus,  326,  694 
accommodation  in,  655 
annular  ligament,  295,  296 
eyes  of,  326 

ocular  movements  of,  694 
Peripatopsis  alba,  degenerate  eyes  of,  724 
Peripatus,  139,  204 
nervous  system,  521 
eyes  of,  138,  205 
Periplaneta,  response  to  light  of,  34,   114 
Perissodactyla,  446 
pupils,  472 

retinal  vascularization,  480 
See  also  Equidae,  etc. 
Periwinkle.     See  Littorina. 


INDEX 


823 


Pernis  apivorus,  iris,  408 
Persistence -time  of  vision,  705 
Petaurus.     See  Flying  phalanger. 
Petrogale.     See  Wallaby. 
Pefromyzon  7)iarinns,  260,  716 
brain,  533 
eyes  of,  265  _ff. 
larva.     See  Ammocoetes. 
uveal  tract,  266 
visual  cells,  269 
See  also  Cyclostomes. 
Phseommatin,  123 
Phalacrocorax,  404 

accommodation  in,  652.  655 
annular  pad,  409 
ciliary  muscle,  407 
harderian  gland,  425 
iris,  407 
lens,  409 
^      ocular  movements  of.  696 
scleral  ossicles,  404 
sphincter  muscle,  407 
bougainvillii,  iris,  407 
Phalanger,  437 

fij'ing.     See  Flying  phalanger. 
spotted  (cuscus),  438 
vulpine.     See  Opossum,  Australian. 
Phalangeridte,  437 
Phalangida,  215 
Phalaris  canariensis  (grass),  phototropism 

in,  40 
Phascolarctin;p.  437 

See  also  Koala. 
Phascolomyinse,  437 
See  also  Wombat. 
Phengodes,  hnninescence  of,  739 
Philatithus  triangulinn,  mnemotaxis  in,  78, 

79 
Phobotaxis,  31 
Phoca.     See  Seal. 
Phoccena.     See  Porpoise. 
Phocidse,  445 

accommodation  in.  641 

cornea,  keratinized,  456 

eye  of,  449 

lens,  474 

ocular  adnexa,  501 

optic  axis,  688 

disc,  486 
pupil,  470,  641,  655 
refraction  of,  639 
retina,  pure-rod,  610 
Phoenicopterus,  407 


Phoenicopterus 
retina,  419 
ruber,  iris,  407 
Pholas,  bioluminescence  in,  736,  740,  745, 
748 
ocelli  of.  200 
visual  pigment  in,  120 
Pholidota,  445 
Pholis,  fovea,  310 
Phosphorescence,  747 
Photinus,  219 

bioluminescence  in,  742,  749 

rhythmic,  22,  747 
vision  of,  585 
pyralis,  bioluminescence  in,  740 
telotaxis  in,  58 
Photoblepharon,   luminous  organ   in,   737, 

738 
Photocytes,  251 
Photoglyctemic  reflex,  560 
Photokinesis.  31,  32.  33 
Photo-mechanical  changes  in  retina.  614, 

615 
Photoperiodism,  7 
in  animals,  13 

bioluminescence  and.  21,  747 
blood  constituents  and,  13 
centres  controlling,  14,  550 
general  activity  and,  15 
light  sensitivity  and,  559 
metabolism  and,  13,  555,  556.  560 
mitosis  and,  13 
ocular  tension  and,  14,  560 
pigment   migration   and,    19,    554, 

556,  558 
sexual  cycle  and,  16.  555,  556,  559 
temperature  and,  13 
lu'inary  output  and.  13 
in  plants,  9 
Photophores,  746 
Photopigments.     .See  Pigments. 
Photoseixsitivity,  4.  113 
diencephalon  and,  537 
Photostasis,  544 
PJwtostomkis  guernei,  luminous  organs  in, 

743 
Photosynthesis,  4 
Phototaxis,  31.  32,  42 

types  of,  47 
Phototropism,  31.  32,  38 
in  animals,  39 
in  plants,  38,  40 


824 


INDEX 


Photurus  pennsylvanica,   luminous  organ 

of,  747 
Phoxinus,  294 

colovir  changes  in,  92,  96 
diencephalon  and,  537 
vision  in,  625,  626 
metabolic  rhythm  in,  15 
multiple  cones  in,  308 
stroboscopic  movement  and,  706 
threshold  to  light,  difference,  617 
visual  acuity  of,  660 
Phronima  sedentaria,  160 

eyes  of,  160 
Phrynoinerus,  pupils,  339 
Phrynosoma,  365 

colour  changes  in,  98 
control  of,  558 
rhythmic,  20 
fovea,  365 
Phyllirrhce,  bioluminescence  in,  740 
Phyllopods,  207 

See  also  Branchiopods,  Apus,  etc. 
Phyllorhynchus,  pure -rod  retina,  610 
Phyllurus  milii,  visual  pigments  in,   122, 

252 
Phylogeny  of  vertebrate  eye,  237 
Physeter.     See  Whale,  sperm. 
Physignathiis,  fovea,  365 

iris,  PI.  V 
Phytohormones,  39,  549 
Pier  is,  colour  vision  of,  587 
luminosity -curve  of,  586 
vision  of,  585 
Pig  {Sus),  445 

angle  gamma,  677 

blood  supply  to  eye,  499,  500 

ciliary  ganglion,  501 

region,  461,  462 
conjunctiva,  491 
glands  of,  491 
cornea,  453 

epithelium  of,  452 
harderian  gland,  494 
lacrimal  gland,  493 
lens,  474 

Manz's  glands,  491 
Moll's  glands,  492 
nictitating  membrane,  493 
optic  axis,  688 
orbit,  498 

pectinate  ligament,  464 
retinal  vascularization,  479 
sphincter  muscle,  468 


Pig,  vitreous,  476 
Pigeon.     See  Cohimba. 

homing.     See  Homing  pigeon. 
Pigment  (s),  117 

activity  of  plants  and,  12 
carotenoid,  88,  118 
dermal  sensitivity  and,  114,  117 
integumentary,  85 
migration  of,  82 

control  of,  in  crustaceans,  554 
insects,  555 
vertebi-ates,  558 
pineal  organ  and,  719 
rhythmic,  19 
melanin,  87,  118 

retinal,  in  compound  eyes,   165,   168 
migration  of,   in  crustaceans,    165 
control  of,  554 
rhythmic,  19 
in  insects,  170 

control  of,  556 
rhythmic,  19 
in  vertebrates,  614,  615 
control  of,  558,  559 
visual,  118 

yellow,  in  cornea  of  Amia,  321,  656 
of  teleosts,  295,  656 
of  macula,  122,  656 
Pigmentary  degeneration,  primary,  light 
sensitivity  and,  559 
photoglycaemic  reflex  and,  560 
Pigmentation,  effect  of  light  on,  82 
Pika.     See  Hare,  calling. 
Pineal  apparatus,  711,  712 
eye,  in  fishes,  713 

lamprey,  713,  716,  717 
young  frog,  714 
origin  of,  242 
gland,  Descartes's  conception,  711 
in  mammals  and  birds,  716 
man,  715 
reptiles,  716 
organ,  538,  713 

hormones  and,  550 
fvinction  of,  718 
tumours,  719 
Pinnipedes,  445 
choroid,  457 
eyes,  shape  of,  448 
lacrimal  passages  lacking,  494 
lens,  474 

ocular  adnexa,  501 
pectinate  ligament,  464 


INDEX 


825 


Pinnipedes,  pupils,  470,  612 

refraction  of,  639 

retinal  vascularization,  479 

sphincter  muscle,  468 

tapetum  cellulosuni,  457,  459,  609 
Pipa  americana,  334,  339 

pupils,  339 
Piscicola,  ocelli  of,  193 
Pithecanthropus,  445,  755 
Pithecia.     See  Saki. 
Pithecus.     See  Langur. 
Pituitary  gland,  538 

hormones  and,  550 
intra-ocular  pressure  and,  561 
in  vertebrates,  557 

hormone,  photoperiodic  changes  and, 
19 
seasonal  changes  and,  21 
Placentals,  429,  441 

colour  vision  in,  633 

decussation,  chiasmal,  698 

diurnal,  604 

eyes  of,  446  #.,  607 

fundi,  PL  XIV,  XV 

nocturnal,  604 

panoramic  vision,  686 

pujiils,  contractile,  612,  613 

spatial  judgment,  704 

vision  of,  601 

visual  field,  binocular,  687,  689 

See  also  Mammals. 
Placode  theory  of  origin  of  vertebrate  eye, 

246 
Placoderms,  234,  235 
Placophora,  196 

ocelli  of,  196 

See  also  Chiton. 
Plagiostomum,  activity  of,  34 
Plaice.     See  Pleiironectes  platessa. 
Planaria  gonocephala,  ocellus  of,  134 
phototactic  reactions  of,  572 

lugubris,  phototaxis  in,  43,  45 

maculata,  tropotaxis  in,  55 

torva,  visual  cells  of,  128,  134 
Planarians,  34,  187 

cave-dwelling,  eyes  of,  724 

nervous  system,  519 

orthokinesis  in,  34 

phototactic  response  in,  33,  572 
Planes,  colour  changes  in,  92 
Plants,  distinction  from  animals,  510 

floral  initiation  in,  10 

hormones  in,  12,  39 


Plants,  long-day,  11 

photoperiodism  in,  9 

photoreceptors  in,  116 

photosynthesis  in,  4 

short -day,  11 
Platyhelminthes,  187 

contraction  in  light,  7 

sense  organs  of,  188 

See  also  Turbellarians,  etc. 
Platypus,  430,  431 

ciliary  body,  434 

eye  of,  432 

posterior  segment  of,  433 

retina,  435 

scleral  cartilage,  433 
Plecoptera,  218,  220 
Plecostomus,  pvipil,  304,  329 
Pleiirodeles,  iris  vascularization,  347 
Pleuronectes,  ocular  movements  in,  693 

flesus,  pupil,  304 

platessa,  camouflage  in,  83 
Plexippus  sinuatus,  eyes  of,  212 
Plusia  gamma,  olfactory  sense  of,  581 

pigment  migration  in,  19 
control  of,  556 
Podargus,  pecten,  412 
Poikilochromic  animals,  82 
Polarized  light,  orientation  to,  66 

mechanism  of,  174 
Polecat  {Putorius  putorius),  444,  445 

colour  blindness  of,  634 

threshold  to  light,  difference,  618 
Polycelis  coronata,  ocelli  of,  188 
Polychsetes,  190 

accommodation  in,  591 

bioluminescence  in,  739,  745,  748 

colour  changes  in,  93 

conditioning  of,  573 

degenerate  eyes  in,  729 

light-shadow  reflex  in,  573 

nervous  system,  520 

ocelli  of,  i91 

reproductive  cycle  of,  18 
Polyclad  worms,  187 
eyes  of,  188 

neuro -endocrine  system,  552 
See  also  Leptoplana. 
Polyipnus,  optic  nerve  of,  310 
Polyodon,  315 

Polyophthahnus  pictus,  ocelli  of,  130,  191 
Polypedates  reinwardti,  pupil,  339 
Polyphemus,  209 

eyes  of,  163,  209 


826 


INDEX 


Polypterini,  235,  278,  315 

eyes  of,  320 
Polypterus,  278,  320 

eyes  of,  320 

median  eye  of,  713 
Polyzoa,  194 

larva,  ocelli  of,  195 
Pomolobus,  eyelids  in,  311 
Pongo.     See  Orang-utan. 
Pontellopsis  regalis,  eyes  of,  159,  209 
Popillia,  response  to  light,  34 
Porcupine,  442,  445 

colour  blindness  of,  633 

eye  of,  447 

optic  axis,  688 

retinal  vascularization,  480 
Porichthys,  luminous  organs  of,  746 
Porifera.     See  Sponges. 
Porphyropsin,  122 
Porpoise,  446 

cornea,  453 

See  also  Cetaceans. 
Porthesia  caterpillar,  phototaxis  in,  46 
Portunus,  colour  changes  in,  92 
Postural  reflexes,  690,  691 
Potamilla,  ocelli  of,  192 
Potamogale.     See  Shrew,  otter-. 
Potto,  443,  607 

See  also  Lemuroids. 
Pouchetia,  eye -spot  of,  126 
Prairie-dog,  445 

pupils,  472 

visual  cells,  482 
Prawns,  166 

eyes  of,  163,  206 

luminous  organs  of,  742 

See  also  Hippolyte,  Palmynon. 
Praying  maiitis.    See  Mantis  religiosa. 
"  Preference  "  technique,  568 

colour  vision  and,  623 
Primates,  443 

accommodation  in,  654 

angle  gamma  of,  677 

area  centralis,  485 

canal  of  Schlemm,  473 

cerebral  cortex,  543 
removal  of,  545 

chiasmal  decussation,  487,  698 

ciliary  cleft,  463 
muscle,  462 
processes,  467 
region,  460,  463 

colour  vision  of,  635 


Primates,  diurnal,  604 

extra.-ocular  mvxscles,  495 

eyes  of,  450 

fovea,  486,  659 

harderian  gland,  494 

iris  vascularization,  468 

lateral  geniculate  body,   489,  490,   541 

lens,  474 
capsule,  653 
svitures  of,  474,  475 

Moll's  glands,  492 

neviro-endocrine  system,  557 

nictitating  membrane,  493 

nocturnal,  604 

occipital  cortex,  removal  of,  546 

ocular  movements  of,  696 

orbit,  498 

pectinate  ligament,  464 

pineal  organ,  715 

pulvinar,  542 

pupils,  471 

reactions  of,  consensual,  700 

refraction  of,  639 

retina,  483,  616 

vascularization  of,  477,  479 

retractor  bulbi,  495,  496 

spatial  judgments  of,  704 

summation,  geniculate,  611 

vision  of,  601 

visual  acuity  of,  663,  664 
cells,  482,'  483 
field,  binocular,  689 
uniocular,  670 

zonular  fibres,  475,  476 
Pristis,  279 
Proboscidea,  446 

See  also  Elephants. 
Procellaria  pelagica,  420 

green  oil-droplets,  420 
Proctacanthns,  circus  movements  in,  54 

telotaxis  in,  59 
Procyon.     See  Raccoon. 
Procyonidse,  445 

pupils,  471,  472 
Pronghorn,  lacrimal  gland  absent  in,  493 

See  also  Ruminants. 
Propithecus,  diurnality  of,  604 
Prosencephalon.     See  Fore-brain. 
Prosimians,  443 

area  centralis,  485 

diurnal,  604 

eyes,  shape  of,  448 

iris  pigmentation,  469 


INDEX 


827 


Prosimians,  nocturnal,  604 

optic  axis,  688 

orbit,  498 

pupils,  472,  612 

tapetum  cellulosum,  459 

See  also  Lemurs,  Tarsier. 
Prosobranchs,  196 

neuro -secretory  cells,  552 

See  also  Buccinum,  Patella,  etc. 
Proteus  anguinus,  334,  726 
eyes  of,  727,  728 
pineal  organ,  714 
retina,  728 
Protocerebrum,  in  arthropods,  521 
Protochordates,  227 

eyes  of,  227 

luminous  organs,  740 

nervous  system,  530 

neuro -endocrine  system,  552 

See     also     Balanoglossus,     Atnphio.vus, 
Ascidia. 
Protopterus,  312 

eyes  of,  312 
Prototheria.     See  Monotremes. 
Protozoa,  179,  180,  510 

bioluminescence  in,  738 

contraction  in  light,  7 

eye-spots,  125 

intercellular  fibrils,  511,  512 

reproductive  cycle  of,  16 

tropisms  in,  570 

See  also  Amoeba,  Euglena,  etc. 
Protractor  lentis  muscle,  in  anurans,  336. 
648 
in  selachians,  285 
Protura,  217,  218 

eyes  lacking  in,  729 
Psephurus,  315 
Psettodes,  329 

migratory  eyes  in.  329 
Pseudocone  eye,  167 
Pseudomoyias   lucifera,    luminescence     of, 

738 
Pseudoscorpions,  214,  215 

eyes  of,  214 
Psocoptera,  218,  220 
Psylla,  reproductive  cycle  in,  17 
Ptarmigan  (Lagopus  mutus),  coloiu" 

changes  in,  21 
Pier  as  pis,  234 

eyes  of,  238 

pineal  organ  of,  713 


Pterocera  lamhis,  198 

ocelli  of,  142,  197 
Pterois,  iris,  371 
Pteromys.     See  Flying  squirrel. 
Pteropus.     See  Flying  fox. 
Pterotrachea,  accommodation  in,   590 

eyes  of,  199 
Pterygotus  anglicus,  157 

eyes  of,  157 
Ptychodera,  kiminescence  in,  740 

rhythmic,  22,  747 
Pufflnus  puffiniis,  407 
iris,  408 

navigation  by,  63,  64 
retina,  417 

sphincter  muscle,  407 
Pulex  irritans,  219 
Pulmonates,  196 
eyes  of,  197 
nervous  system,  528 
See  also  Helix,  Limax,  etc. 
Pulvinar,  542 
Pupil,  characteristics  in 
anurans,  339 
birds,  408 
chelonians,  372 
chimferas,  290 
chondrosteans,  317 
crocodilians,  376 
holosteans,  322 
lacertilians,  359 
marsupials,  439 
yeoceratodus,  313 
placentals,  470,  471,  613 
selachians,  286 
snakes,  388 
Sphenodon,  381 
teleosteans,  303,  304 
urodeles,  347 
contractile,  occurrence  of,  612 
double,  in  Anableps,  324 

in  Leptognathus,  325 
stenopceic,  612,  641 
Pupillary  reactions,  colour  vision  and,  621 
consensual,  700 
in  amphibians.  339 
birds,  408 

cejahalopods,  146,  575 
crocodilians,  376 
lacertilians,  361 
placentals,  472 
teleosts,  304 
Purkinje  shift,  colour  vision  and,  622 


828 


INDEX 


Purkinje  shift,  in  birds,  629 
crocodilians,  628 
fishes,  625 
frogs,  627,  628 
insects,  586 
Pycnogonida,  217 
Pygopus  lepidopus,  conus,  363 

fundus,  362 
PyramidaUs  muscle,  in  birds,  424 
chelonians,  374 
crocodiUans,  378 
Pyrophorus,  luminescence  in,  748 
Pyrosoma,  luminescence  in,  740,  745 
Pyrrhula,  ciliary  venous  sinvis,  408 

lens,  409 
Python,  ciliary  venous  sinvis,  386 
iris,  386 

pupillary  contraction,  388 
sclera,  385 
molurus,  fundus,  390 
regius,  iris,  PL  IX 
reticulatus,  iris,  PI.  IX 
See  also  Spilotes. 


Q 


Quadratus  muscle.     See  Bursalis. 
Quadrigeminal  body,  534 


R 


Rabbit,  445 

angle  gamma  of,  676 
anterior  chamber,  465 
area  centralis,  485 
blood  supply  to  eye,  498,  499,  500 
cerebral  cortex,  543 
removal  of,  545 
ciliary  ganglion,  501 

region,  461,  462 
colour  blindness  of,  633 
conjunctiva,  491 
cornea,  453 

epithelium  of,  452 

nerves  of,  454,  455 
drainage  channels,  473 
gonadotrophic  hormone,  control  of,  559 
iris  vascularization,  468 
lacrimal  passages,  494 
lens  capsule,  653 

sutures,  474,  475 


Rabbit,  Moll's  glands  lacking,  492 
movement,  perception  of,  705 
nictitating  membrane,  493 
ocular  movements,  692 
optic  nerve -head,  488 
orbit,  497 

pectinate  ligament,  464 
refraction  of,  639 
retina,  481,  484,  485 

vascularization  of,  477,  478,  480 
urinary  secretion,  560 
visual  field,  binocular,  673,  686,  687 
vitreous,  476 
Raccoon,  444,  445 
colour  vision  of,  634 
fundus,  PI.  XIV 

threshold  to  light,  difference,  618 
Radiolaria,  179,  180 

luminescence  in,  738,  748 
Radio -receptors,  116 
Raja,  287 

accommodation  in,  647 
colour  changes  in,  95 
ramp -retina,  642,  643 
batis,  pupils,  287 
clavata,  280 
eye  of,  275 
pupils,  287 
miraletus,  visual  cells,  288 
montagui,  280 
Ramp-retina,  642,  643 
Rana,  334,  335,  342 
area  centralis,  344 
brain,  533 
colour  changes,  98 
eye  of,  334,  336 
fundus,  341 

hue  discrimination,  627 
pineal  organ,  714 
pupils,  339 
Purkinje  shift,  628 
visual  cells,  342 
cateshiana,  iris,  337 

pupils,  339 
clamata,   phototaxis   and   temperature, 

627 
esculenta,  area  centralis,  344 

iris,  337 
halecina,  pupils,  339 
pipiens,  visual  cells,  250,  344 
sphenocephala,  iris,  371 
temporaria,  fundus,  PI.  Ill 
iris,  PI.  Ill 


INDEX 


829 


Rana  temporaria 

migration  of  retinal  pigment,  614,  615 
pupillary  contraction,  340 
retina,  343 
triple  cones,  308,  342 
visual  cells,  344 
Ranatra,  telotaxis  in,  56 
Ranzania  truncata,  eyes  of,  273 
Rat,  445 

blood  supply  to  eye,  498 
colour  blindness  of,  633 
cornea,  453 

epithelium  of,  452 
distance,  judgment  of,  704 
eye  of,  605 

lacrimal  passages,  494 
Moll's  glands  lacking,  492 
neuro -secretory  cells,  551 
ocular  movements,  696 
optic  axis,  688 
retina,  rod-rich,  610 
threshold  to  light,  difference,  618 
visual  acuity,  663,  665 
cells,  483 
Ratita-,  397 

annular  pad,  409 
pecten,  411,  413 
See  also  Apteryx,  Struihio,  etc. 
Rattlesnake.     See  Crotalus. 
Rattus.     See  Rat. 
Raven,  402 

eye,  shape  of,  402 
See  also  Corvidae. 
Ray.    See  Raja. 

Reflexes,    conditioned.     See    Conditioned 
reflexes, 
pvipillary.     See  Pupillary  reactions. 
Refraction  of  vertebrates,  638 
amphibians,  638 
birds,  639 
cyclostomes,  638 
fishes,  638 
mammals,  639 
reptiles,  639 
Reptiles,  353 

accommodation  in,  648,  649 
brain,  533 

transection  of,  534 
cerebral  cortex,  543 
ciliary  ganglion,  501 
colour  changes  in,  82 
control  of,  98,  558 
mechanism  of,  87 


Reptiles,  colour  changes  in,  rhythmic,  20 
colour  vision  of,  628 
diurnal,  603 
eyes  of,  353  ff. 

degenerate,  731 

median,  715,  716 
fore-brain,  543 

removal  of,  545 
lateral  geniculate  body,  541 
median  eyes,  715,  716 
mid-brain,  535 
migration  of  retinal  pigment,  614 

of  visual  cells,  616 
movement,  perception  of,  705 
neuro -endocrine  system,  557 
nocturnal,  603 
ocular  movements  of,  694 
optic  thalamvis,  540 
primitive,  234,  235 
pupillary  reactions,  700 
refraction  of,  639 
reproductive  cycle  in,  17 

control  of,  559 
spatial  judgments  of,  702 
tectum,  535 
telencephalon,  543 
vision  of,  599 
visual  acuity  of,  661 

field,  binocular,  682 

pathways,  538,  544 
Respiration  rate  and  colour  vision,   623, 

625 
Rete  of  Hiirlimann,  500 
Retina,  characteristics  in 

Anableps,  325 

anurans,  341,  343 

birds,  418,  419 

cei^halopods,  145 

chelonians,  372,  373 

chimseras,  290 

chondrosteans,  318 

crocodilians,  377 

dipnoans,  313 

holosteans,  322 

invertebrates.     See  Retinule,  Visual 
cells,  etc. 

lacertilians,  361,  363 

lamjarey,  268 

Latinieria,  315 

marsupials,  439 

monotremes,  435,  436 

placentals,  482,  483,  484 

Pterocera,  142 


830 


INDEX 


Retina,  characteristics  in 
selachians,  287,  288 
snakes,  389,  390,  392 
Sphenodon,  381,  383 
teleosts,  304,  306 
tubular  eyes,  323 
urodeles,  347,  348 
vertebrates,  248,  249 
embryology  of,  239 
anangiotic,  480 
central  artery  of,  477 
converse,  146 
corrugated,  642,  643 
diurnal  eyes,  in.  610,  611 
duplicated,  in  tubular  eyes,  323,  643 
holangiotie,  479 
inverse,  146 
inverted,  146 

in  arachnids,  149 
molluscs,  147 
vertebrates,  241 
merangiotic,  479 
nocturnal  eyes,  in,  609,  610 
pavirangiotic,  480 
photo -inechanical  changes  in,  614 
pure-cone,  611 

in  Calamoichthys,  320 
colubrid  snakes,  392 
geckos,  365 
Sciuridse,  483 
pure -rod,  610 

in  chimseras,  290 

deep-sea  teleosts,  305 
echidna,  436 
Lep  idosiren  ,313 
nocturnal  geckos,  364,  365 

placentals,  482,  610 
selachians,  288 
ramp-,  642,  643 
rod -rich,  610 

structure  of,  and  accommodation,  656 
summation  in,  611,  659 
vascularization  of,  in  vertebrates,  476, 

477,  478,  482 
verted,  146,  241 
See  also  Visual  cells. 
Retinal  mosaic,  perception  of  movement 
and,  705 
visual  acuity  and,  656 
pigment.     See  Pigment,  retinal. 
Retinella,  129 
Retinule,  157 


Retractor  bulbi,  characteristics  in 
anurans,  345 
chelonians,  374 
lacertilians,  366,  368 
marsupials,  441 
monotremes,  437 
placentals,  495,  496,  501 
Sphenodon,  383 
abnormal,  in  man,  497 

bursalis  muscle,  in  lacertilians,  368 
Rhabdites,  128 
Rhabdome,  141,  158 
Rhacophorus  leucomystax,  iris,  PI.  Ill 
Rhamdia,  eyes  of,  725 
Rhea,  397,  410 

fundus,  410 

pecten,  413 
Rheotaxis,  73 

Rhineura  floridana,  degenerate  eyes  of,  733 
Rhinoceros,  444,  446 

cornea,  453 

eyes  of,  450 

fundus,  PI.  XV 

nictitating  membrane,  492 

optic  axis,  688 

pupils,  472 

retinal  vascularization,  480 

retractor  bulbi,  496 

sclera,  450 
Rhinoglena,  frontal  eye  of,  194 
Rhinophis,  eyelids,  393 

eyes,  degenerate,  731 
Rhipidistia,  234,  235 
Rhizopods,  180 

contraction  to  light,  7 

See  also  Amceba,  etc. 
Rhodopsin,  122 

Rhombencephalon.     See  Hind-brain. 
Rhynchocephalians,  353,  379 

eyes  of,  380 

See  also  Sphenodon. 
Rhythm,  diurnal.     See  Photoperiodism. 

tidal,  in  crustaceans,  15' 
molluscs,  15 
protozoa,  16 
Rhytina,  446 
Roach.     See  Rutilus. 
Robin.     See  Erithacus. 

American.     See   Turdus  migratorius. 
Rochon-Duvigneaud,  Andre-Jean- 

Fran9ois,  332,  333 
Rodents,  445 

accommodation  in,  653 


1 


INDEX 


831 


Rodents,  area  centralis,  485 
blood  supply  to  eye,  498 
chiasma,  487 
ciliary  muscle,  461 
processes.  466 
region,  460,  462 
colour  vision  in.  633 
cornea,  453 
diurnal,  604 
lacrimal  duct,  493 
lens,  606 

Moll's  glands  lacking,  492 
nictitating  membrane,  493 
occipital  cortex,  removal  of,  545 
ocular  movements  in,  696 
optic  axis,  688 
orbit,  497 

pectinate  ligament,  464 
pupils,  470,  471,  472 

reactions  of,  700 
refraction  of,  639 

retinal  vascularization.  479.  480,  481 
retractor  bulbi,  495 
tapetum  fibrosum,  458,  609 
vision  of,  601 
visual  field,  binocular,  687 
zonular  fibres,  475 

See  also  irtrious  species  (Rat.  Squirrel, 
etc.). 
Rods,  in  invertebrate  retina,  128 
in  vertebrate  retina,  250 

development  from  cones,   252 
differentiation  from  cones,  251 
double,  253 
green  (Schwalbe"s).  inanurans,  342, 

344 
violet,  in  anurans,  342 
in  urodeles.  349 
See  also  Visual  cells. 
Rorcjual.    See  Whale,  blue. 
Rotifera,  194 

cerebral  eye  of,  194 
dermal  sensitivity  of.  32.  114 
frontal  eye  of,  194 
Rudimentary  eyes,  721 

in  Limulus,  163,  212,  552 
Rviminants,  446 
area  centralis,  485 
cornea.  453 
corpora  nigra.  470 
hyaloid  artery,  481 
pupils,  472 
See  also  Sheep,  Cattle.  Deer,  etc. 


Riitilus,  double  cones  in,  308 
membrana  vasculosa,  299,  300 


S 


Saccopharynx,  degenerate  eyes  in.  724 
Sacculina,  208 

eyes  lacking  in  adult.  734 
Sagitta,  194 

ocelli  of.  194 
Saki,  443 
Salamanders,  346 
eyes  of,  346 

degenerate,  726 
larvsp,  colour  changes  in,  20 
control  of,  558 
See  also  Axolotl. 
See  also  Urodeles,  Anihystoma, 
Salamandra. 
Salamandra,  346 

colour  vision  of,  628 
retina,  347 
maculosa,  fimdus,  PI.  IV 
iris,  347 
Salmo  salar.  iris.  PI.  II 
trutta,  SOS 

choroidal  gland,  297 
chromatophores,  88 
eye  of,  276,  293 
pineal  apparatus,  714,  715 
retina,  306 
triple  cones,  308 
visual  field,  binocular,  679 
Salmonidne,  cornea,  294 
double  cones,  308 
eyelids,  312 
scleral  cartilage,  292 
Salpa,  eyes  of,  228 
Salticus,  214 
ocellus  of,  140 
scenicus,  eyes  of,  213 
Sandalops,  203 

stalked  eyes  of,  203 
Sapphirina,  eyes  of,  209 
Sarcodina.     See  Rhizopods. 
Sarcophaga,  58 

cornea,  transi^arency  of,  584 
nervous  system,  522 
orientation  to  polarized  light.  582 
telotaxis  in,  57 
Sarcophilus.     See  Tasmanian  devil. 
Sarcoptes  scabiei,  216 


832 


INDEX 


Sarsia,  139,  182, 
ocellus  of,  139 
Saturnia  pernyi,  development  of  eye,  156 
Sauropsida.     See  Reptiles  and  Birds. 
Saw-fly,  220,  223 

larvae,  ocelli  of,  141,  223 
See  also  Neodiprion. 
Saxicola,  417 

infula  in,  417 
Scallop.     See  Pecten. 

Scalops  aquaticus,  degenerate  eyes  in,  733 
Scaphiopus,  pupils,  339 
Scaphirhynchus,  315 

pupils,  317 
Scaphopods,  196 

neuro -secretory  cells,  552 
sense  organs,  197 
Sceloporus,  retinal  pigment  in,  361 
Schistocerca  gregaria,  dorsal  light  reaction 
in,  74 
ommochromes  in,  123 
Schistosoma,  187 
Schizopods,  eyes  of,  160,  591 

See  also  Stylocheiron,  Mysids. 
Schlemm,  canal  of,  473 
Sciuridse,  445 

accommodation  in,  653 
area  centralis,  485 
choroid,  457 
ciliary  region,  460 
colour  vision  in,  633 
diurnality  of,  604 
lens,  474 

ocular  movements  of,  696 
optic  axis,  688 

disc,  686 
refraction  of,  639 
retina,  485 

pure -cone,  612 
vascularization  of,  479 
vision  of,  601 
visual  acuity  of,  663 
cells,  483 

field,  binocular,  689 
Sciuromorpha,  445 

Sciurus  vulgaris.     See  Squirrel,  common. 
Sclera,  characteristics  in 
amphibians,  334 
birds,  403 
chelonians,  369 
chimseras,  290 
chondrosteans,  317 
dipnoans,  313 


Sclera,  characteristics  in 
holosteans,  321 
lacertilians,  356 
lamprey,  265 
Lati?neria,  315 
marsupials,  438 
monotremes,  433 
placentals,  450 
selachians,  281 
snakes,  385 
Sphenodon,  380 
teleosts,  292 
Scleral  cartilage.     See  Cartilage. 

ossicles.     See  Ossicles. 
Scolopendra  ■rnorsitans,  210 
Scombridse,  adipose  lids  in,  311 

See  also  Thunnus. 
Scopelarchus  analis,  tubular  eyes  of,  323 
Scorpcena,  302 
fundus,  306 
tensor  choroidese,  302 
twin  cones,  308 
Scorpion,  211 

ocellus,  lateral,  140,  141,  211 

median,  150,  212 
pseudo-.     See  Pseudoscorpions. 
whip-.     See  Whip-scorpions. 
Scotocytes,  251 
Scototaxis,  31,  60 
Scutigera,  160 

eyes  of,  160,  210 
Scylliorhinus,  287 

ciliary  papilla,  284 
optic  pedicle,  290 
pvipils,  286,  287 
canicula,  280 
Scyllium.  accommodation  in,  647 
blinded,  behaviour  of,  598 
colour  changes  in,  95 
Scymnus,  brain,  533 
Scyphozoa,  182 

See  also  Jellyfish. 
Sea-anemones,  182 
nerve  fibrils  in,  514 
nervous  responses,  515,  516 
phototactie  reactions  of,  571 
See  also  Actinia. 
Sea-cows.     See  Sirenians. 
Sea-cucumbers,  184 
sensitivity  of,  184 
See  also  Holothuria. 
Seagulls.     See  Laridae. 
Seal,  445 


INDEX 


833 


Seal,  bearded,  pupils,  470,  472 

common,  502 
fundus,  PI.  XIV 

harp,  eye  of,  447 

See  also  Phocida?,  Pinnipedes. 
Sea-lilies,  184 
Sea-lion,  444,  445 

pujDils,  470 

See  also  Pinnipedes. 
Sea-spiders,  217 

eyes  of,  149,  217 
Sea-squirts,  228 

See  also  Ascidia. 
Sea-urchins,  184 

sensitivity  of,  185 

See  also  Diadema. 
Secretary  bird.     See  Serpentarius. 
Sedentaria,  190 
Sedentary  habit,  degenerate  eyes  due  to, 

722 
Selache  maximiis,  283 

extra-ocular  muscles,  290 

pupils,  287 
Selachians,  235,  278 

accommodation  in,  647 

brain,  533 

central  nervous  sj'stem,  532 

ciliary  ganglion,  501 

colour  changes  in,  95 
control  of,  558 
vision  in,  624 

electric  organs  in,  751 

eyes  of,  279  if.,  282 
degenerate,  724 

labyrinths,  534 

luminous  organs  in,  741 

nocturnality  of,  603 

palseocortex,  543 

pineal  apparatus,  713,  714 

pupillary  reactions,  612 
consensual,  700 

refraction  of,  638 

retina,  pure-rod,  610 

secretory  mechanism,  267 

summation,  retinal,  660 

tapetum,  retinal,  612 

threshold  to  light,  absolute,  616 

vision  of,  598 

visual  field,  binocular,  679 
Seniotilus,  colour  preference  in,  624 

hue-discrimination,  626 

threshold  to  light,  difference,  617 

S.O.— VOL.  I. 


Sensitivity  to  light,  in  insects,  584 
in  vertebrates,  602 
absolute,  616 
binocular,  680 
dermal,  113 
Sepia,  201 

colour  changes  in,  85,  92 
conditioning  of,  576 
eyes  of,  145,  202 
reactions  of,  528 
vision  of,  576,  577 
Seps,  transverse  muscle  in,  357 
Sergestes  prehensilis,  photophore  of,  746 
Serpentarius  cristatus,  413 

pecten,  413 
Serranus,  fovea,  309,  310 
ocular  movements,  693 
cabrilla,  693 

accommodation  of,  645 
optic  nerve,  310 
Sertularia  hj^droid,  pigment  in,  120 
Sexual  cycle  in  animals,  16 

control  of,  in  crustaceans,  555 
in  insects,  556 
vertebrates,  559 
Shadow-reflex,  45,  572,  574 
Shearwater.     See  Puffmus. 
Sheep  (Ovis),  446 
angle  gamma,  677 
area  centralis,  485 
blood  supjDly  to  eye,  499,  500 
corpora  nigra,  470 
harderian  gland,  494 
lens  capsule,  653 
optic  axis,  688 
orbit,  498 

pectinate  ligament,  464 
photoperiodism  in,  18 
pupillary  reactions,  472 
retractor  bulbi,  496 
vitreous,  476 
Shell-eyes,  in  Chiton,  196 
Shock-reaction,  510 
Shrew,  441 
elephant,  441 
otter,  441,  443 
tree-,  441,  442 
diurnality  of,  604 
lens,  474 
true,  441 

ciliary  region,  460,  467 

eyes  of,  449 

retina,  pure-rod,  610 

53 


834 


INDEX 


Shrew,  visual  cells,  482 
Shrike.     See  Lanius. 
Shrimps,  206 

eyes  of,  163,  206 

luminescence  in,  740,  743,  746 

See  also  Crago,  etc. 
Sialia,  fundus,  410,  PL  XII 
Sign-stimuli,  in  insects,  588 

in  vertebrates,  664 
Siluridae,  blinded,   dermal  sensitivity  in, 
114 

degenerate  eyes  in,  725 

uveal  tract,  299 

visual  cells,  rhythmic  migration  of,  19 

See  also  Anieiurus. 
Simenchelys  parasitica,  734 

eyes  of,  735 
Simians,  443 

See  Anthropoidea. 
Simiidse,  443 

See  also  Apes,  anthropoid. 
Simocephalus,  conditioning  of,  578 
Simple  eyes,  129 
composite,  152 
ommatidial,  159 
Sinapsis  alba  (white  inustard),  helio- 

tropism  in,  38 
Sinus  gland,  in  crustaceans,  552,  553 

photoperiodic  changes  and,  19 
Siphonops,  eyes  of,  730 
Siren,  eyes  of,  349 
Sirenians,  446 

lacrimal  gland  lacking,  493 

lens,  474 

ocular  adnexa,  502 

pupils,  472 

refraction  of,  639 

retinal  vascularization,  480 

retractor  bulbi,  495,  496 

visual  acuity  of,  654 
Size,  perception  of,  667,  701 
Skunk  [Mephitis),  445 

nictitating  membrane  absent,  493 

optic  axis,  688 
Sleep -movements  in  plants,  9,  10 
Sleep-rhythms  in  mammals,  13 
Sloth,  445 

2-toed,  445,  607 
pupils,  612 

3-toed,  445 
Slow  eyes,  in  insects,  584,  706 
Slow-worm.     See  Anguis. 
Slugs,  196,  197 


Slugs,  eyes  of,  197 

vision  of,  574 

See  also  Gastropods,  Li?nax. 
Smell.     See  Olfactory  sense. 
Snails,  196,  198 

conditioning  of,  575 

eyes  of,  197 

reproductive  cycle  in,  17 

vision  of,  574 

See  also  Gastropods,  Helix. 
Snakes.     See  Ophidians. 

river-.     ^See  Homalopsinae. 

sea-.     See  Hydrophinse. 

tree-.     See  Dryophis,  etc. 
Snipe,  visual  field,  binocular,  685 
Soemmerring,  D.  W.,  258,  259 
Soleidfo,  328 

cornea,  296 

ocular  movements  of,  693 

scleral  cartilage,  294 
Solenogastres,  196 

sense  organs  of,  197 
Solenopsis,  compound  eyes  of,  172,  225 
Solifugaj,  216 

Sondermann,  canals  of,  473 
Souslik,  445 

colovir  vision  in,  634 

retina,  485 
Space,  perception  of,  in  insects,  589 

in  vertebrates,  666 
Spadella,  194 

ocellus  of,  135,  152,  194 
Spalax,  degenerate  eyes  of,  733 
Spatial  judgments,  700 
"  Spectacle,"  primary,  265,  266 
in  cyclostomes,  265 

secondary,  255,  266 
in  lizards,  366 
snakes,  385,  392 
teleosts,  312 
Spectral  sensitivity  of  honey-bee,  585 
Sphcerodactylus,  fusion  frequency  in,  252 

argus,  visual  cells,  365' 

parkeri,  visual  cells,  252,  365 
Sphceroma  lanceolata,  206 
Sphenisciformes.     See  Impennes. 
Spheniscus,  visual  field  of,  685 
Sphenodon  punctatus,  379 

accommodation  in,  651 

ciliary  region,  380 

colour  vision  of,  628 

eyes  of,  380  j^f. 

fovea,  382,  659 


INDEX 


835 


Sphenodon  punctatus. 
fvmdus,  PI.  VIII 
iris,  381 
parietal  eye,  715,  716,  718 

function  of,  719 
pineal  apparatus,  714,  715 
pupil,  contractile,  612 
retina,  382,  610 
visual  acuity,  661 
cells,  382 
Sphincter  pupilla?  muscle,  characteristics  in 
anurans,  337 
birds,  407 
lacertilians,  357 
monotremes,  436 
placentals,  468 
selachians,  285 
snakes,  387 
Sphenodoti,  381 
teleosteans,  303 
Sphyrna  tiburo,  327 
eyelids,  289 
eyes  of,  327 
zygcena,  327 

extra-ocular  muscles,  327 
optic  pedicle,  290 
Spiders,  213 

cave-.     See  Anthrobia. 
garden-.     See  Araneus. 
house-.     See  Tegenaria. 
jumping,  conditioning  of,  580 
vision  of,  580 
See  also  Evarcha,  Salt ic us. 
ocelli  of,  139,  140,  149,  150,  213 
ripple-,  vibrotropism  in,  579 
web -spinning,  menotaxis  in,  61 
vibrotropism  in,  579 
vision  of,  579 

See  also  Araneus,  Tegenaria. 
wolf-.     See  Lycosa. 
Spilotes  variegatus,  head  of,  384 
Spinachia,  colour  preference  in,  624 
Spirographis,  phototropic  movements  in, 

39' 
Spondylus,  201 

ocelli  of,  148,  201 
Sponges,  181 

myo -epithelial  cells,  513,  514 
reactions  of,  513 
See  also  Leucosoleiiia. 
Sporozoa,  180 

Springtails.     See  Collembola. 
Squalus,  97 


Squalus 

chromatophores,  97 
eye  of,  275 
ptipils,  285,  287 
Squatina,  288 
pupil,  286 
visual  cells,  288 
Squids,  196 

colour  changes  in,  85,  93 
eyes  of,  143,  202 
luininescence  in,  740,  746 
See  also  Loligo. 
Squirrel,  African,  pupils,  472 
common,  445 

colour  vision  of,  633 
pupils,  472 
retina,  484 

vascularization  of,  479 
visual  cells,  482 
flying.     See  Flying  squirrel, 
ground.     See  Souslik. 
See  also  Sciuridse. 
Stalked  eyes,  in  cephaloiDods,  203 
in  fishes,  326,  327 
insects,  223,  225 
Starfish,  184,  PI.  I 
nervous  system,  516 
reactions  of,  516 
visual  organs,  185 
See  also  Asterias. 
Stargazer.     See  Astroscopus,  Uranoscopus. 
Starling,  Ernest  Henry,  548,  549 

(bird).     See  Lamprocolius,  Sturnus. 
Statocysts,  in  cephalopods,  202 
in  comb -jellies,  182 
fishes,  74,  76 
scaphopods,  197 
tunicates,  228 
Stato-kinetic  reflexes,  667 
Steatornis,  iris,  407 
Stemmata,  220,  222 
Stenopoeic  pupils,  612 

accommodation  and,  641 
Stenostonum,  sense  organs  of,  189 
Stefitor,  179,  180 

cceruleus,  klmotaxis  in,  49,  50 
photosensitivity  of,  125 
Stephanoaetus,  606 
Stereoscopic  vision,  698,  700 
Sterria  hirundo,  419 

bifoveate  retina,  419 
Stick-insect.     See  Dixippus. 


836 


INDEX 


Stickleback,  visual  acuity  of,  660 

See  also  Gasterosteus,  Eucalia,  Spinachia. 
Stigma,  125 
Stizostedion,  visual  acuity  of,  657 

visual  cells,  307 
Stoneflies,  218 
Strepsiptera,  220,  221 
Streptopelia,  398,  681 
Strigidse.     See  Owls. 
Stringops,  418 

fovea,  418 

visual  field,  binocular,  685 
Strix  aluco,  anterior  chamber,  404 
fundus,  410,  PI.  XII 
head  of,  402 
visibility  of  infra-red  to,  630 

fiamtnea,  pecten,  412 
Stroboscopic  movement,  706 
Strongylocentrotus,  protection  from  light, 

39 
.Struthio,  397,  405 

ciliary  muscle,  406 

eye -shine,  405 

infula,  417 

pecten,  411,  413 
Sturnus  vulgaris,  reproductive  cycle  in,  17 
Stygicola,  degenerate  eyes  in,  725 
Stylaria  lacustris,  ocellus  of,  136 
Stylocheiron,  160 

eyes  of,  160,  161 

luminous  organ,  740 
Stylophorus,  322 

tubular  eyes  of,  324 
Stylophthalmus  paradoxus,  328 

eyes  of,  327 
Stylops,  221 

eyes  of,  151,  221,  734 
Suboesophageal  ganglion,   in  arthropods, 

521,  522 
Subscleral  sinus,  in  lamprey,  266 
Suctorians,  179,  180 
Suidae,  445 

See  also  Pig. 
Sula  bassana,  407 

area  centralis,  421 
ciliary  muscle,  407 
distance,  judgment  of,  703 
sphincter  muscle,  407 
Summation,  geniculate,  611 

retinal,  611 

visual  acuity  and,  659 
Sun-navigation.     See  Light-compass 

reaction. 


Suoidea,  445 
pupils,  472 

tapetum  lacking,  458,  609 
See  also  Pig,  Hippopotamus,  etc. 
Superposition  eye,  169,  174 
Supplementary  layer  of  cornea,  296 
Supi"a- oesophageal  ganglion.     See 

Cerebral  ganglion. 
Supra-optic  nucleus,  557 
Suricate,  459 

diurnality  of,  604 
pupils,  472 

tapetum  lacking,  459,  609 
Suspensory  ligament,  of  iris,  464 
of  lens,  in  chondrosteans,  317 
in  holosteans,  321 
selachians,  285 
teleosts,  302 
urodeles,  347 
See  also  Zonular  fibres. 
Sutures  (lens),  in  birds,  409 
in  placentals,  474,  475 
selachians,  287 
teleosts,  304 
Swallow,  bifoveate  retina  in,  418 

See  also  Hirundo. 
Swan,  eye  of,  399 
Sweat  glands,  conjunctival,  491 
Sycon,  181 

myo -epithelial  cells,  513 
Synapta,  sensitivity  of,  184 
Synchceta,  cerebral  eye  of,  194 
Syngnathus,  309 

colour  preference  in,  624 
fovea  of,  309 

visual  field,  binocular,  680 
Syrnium.     See  Strix. 


Tabanidse,  eyes  of,  225 

See  also  Tabanus,  Ancala. 
Tabanus,  219 

nervous  system,  522 
Tachyglossus.     See  Echidna. 
Tactile  sense,  116 

colour  changes  and,  105 
in  crustaceans,  579 
Dytiscus,  104 
fishes,  598 

cave-,  726 
insects,  581 


INDEX 


837 


Tactile  sense,  in  myriapods,  578 
Pecten,  103  ' 
spiders,  579 
vertebrates,  597 
worms,  572 
spatial  judgment  and,  667 
vibrissse,  of  camel,  492 
of  cat,  492,  601 
rodents,  601 
Taenia,  187 
Talitrus  saltator,  61 

luminous  bacteria  in,  738 
menotaxis  in.  61,  62 
orientation  to  polarized  light  in,  73 
time -memory  in,  22 
Talpa.     See  Mole. 
Tapetal  pigment,  migration  of,  19 
Tapetum   (lucidum),    in   compound   eyes, 
165,  168 
in  crustaceans,  165 
insects,  168 
in  simple  eyes,  147 

in  arachnids,  149,  150 
crustaceans,  152 
molluscs,  148 
in  vertebrate  eyes,  606 
cellulosum,  609 

in  placentals,  459 
choroidal,  non-occlusible,  608 
in  chondrosteans,  317 
Latimeria,  315 
occkisible,  612 
in  selachians,  281 
fibrosum,  609 

in  marsupials,  438 
placentals,  457 
teleosts,  297 
retinal,  non-occlusible,  608 
in  chondrosteans,  318 
crocodilians,  377 
deep-sea  teleosts,  305 
Didelphys,  440 
Fteropus,  459 
occlusible,  612 
in  teleosts,  305 
Tapir,  444,  446 
optic  axis,  688 
retinal  vascularization,  480 
Tarbophis,    retinal    vascularization,    301, 
390 
visual  cells,  392 

field,  binocular,  684 
Tarentola,  melanophores  of,  87 


Tarsal  glands,  in  mammals,  491 
Tarsier,  442,  443,  613 
area  centralis,  485 
eyes,  shape  of,  448 
fovea,  pure-rod,  486 
immobility  of  eyes,  696,  697 
pupils,  612,  613 
retina,  pure-rod,  482,  610 
threshold  to  light,  674 
Tasmanian  devil,  437,  438 
fvmdus,  PI.  XIII 
tapetum  fibrosum,  438,  609 
wolf,  tapetum  fibrosum,  438,  609 
Taste  receptors,  in  bees,  588 
insects,  581 
vertebrates,  534 
Tauredophidium,  degenerate  eyes  in,  724 
Tautoga  onitis,  visual  pigments  in,  121 
Tealia,  phototactic  reactions  of,  571 
Tectum,  534,  690 
in  birds,  535 

cyclostomes,  534 
fishes,  534 
mammals,  536 
Tegenaria  domestica,  214 
ej-es  of,  159,  213 

anterior  median,  140 
Tegmentum,  535,  690 
Telencephalon,  532,  542 

development  of,  542 
Teleosteans,  235,  279 

accommodation  in,  645,  646 
archicortex,  543 
blind,  724 

central  nervous  system,  532 
ciliary  ganglion,  501 
colour  changes  in,  84,  91,  96,  621 
control  of,  558 
pineal  body  and,  92 
vision  in,  621,  624 
diurnality  of,  603 
electric  organs  in,  751 
eyes  of,  291  jg^.,  293 

degenerate,  724,  725,  735 
irides,  PI.  II 
iris  furrow,  337 
lateral  geniculate  body,  541 
luminous  organs,  741 
migration  of  retinal  pigment,  614 

of  visual  cells,  614 
neuro -secretory  cells,  551 
olfaction  in,  598 
pineal  apparatus,  713 


838 


INDEX 


Teleosteans,  refraction  of,  638 
secretory  mechanism  of,  267 
tapetum,  choroidal,  609 

retinal,  612 
threshold  to  light,  absolute,  616 

difference,  617 
vision  of,  598 
visual  acuity,  660 
field,  binocular,  679 

uniocular,  670,  672 
pathways,  536 
Telescope -eyed  goldfish,  324 
Telescopic  eyes.     See  Tubular  eyes. 
Telo-menotaxis,  61 
Telotaxis,  31,  55 

definition  of,  43 
Temperature,  diiirnal  rhythm  in,  13 
Tenacular  ligament,  ciliary,  in  birds,  405 
in  lacertilians,  357 
orbital,  in  teleosts,  312 
Tenebrio  larvae,  photokinesis  in,  114 
Tensor  choroidese,  in  anurans,  335 
in  birds,  406 

teleosts,  295,  302,  646 
Tentaculocysts,  in  jellyfish,  183 
Termites,  218,  729 
eyes  lacking  in,  729 
See  also  Calotermes. 
Terrapin,  374 

See  also  Clemmys,  Chelonians, 
Testudinidse,  369 
Testudo,  369 

ciliary  musculature,  372 
colour  vision  in,  629 
eye  of,  370 
visual  cells,  373 

field,  binocular,  682 
Carolina,  iris,  371 
grceca,  scleral  ossicles,  369 
Tetragonopterus,  iris,  PI.  II 

scleral  cartilage,  294 
Tetraodon,  fovea,  310 
Thalamus,  optic,  538 

Thalassarctos  m-aritinius.    See  Bear,  polar. 
Thallophytes  (unicellular  plants),  510 
Thaumatops  magna,  eyes  of,  207 
Thelotornis,  fovea,  388,  392 

pupils,  388 
Therapsida,  234,  236 
Thermal  sense  of  snakes,  599,  600,  667 
Thermo -receptors,  116 
Thermotropism,  33 
Thigmotropism,  33 


Threshold  to  light,  absolute,  in  insects, 
584 
in  vertebrates,  616 
binocular,  673 
difference,  in  insects,  585 
in  vertebrates,  617 
Thrips,  218,  220 
Thrush,  402 

shape  of  eye,  402 
Thunnus,  294 

scleral  ossicles,  294 
Thylacinus.     See  Tasmanian  wolf. 
Thysanoptera,  218,  220 
Thysanura,  211,  218 

See  also  Lepisma. 
Ticks,  216,  217 

eyes  of,  216 
Tiger  (Felis  tigris),  445 

area  centralis,  485 

extra-ocular  muscles,  495 

pupils,  471 
Time -memory,  in  arthropods,  22 

in  birds,  22 

diurnal  rhythm  in,  22 
Tinamou,  397 
Titmouse.     See  Par  us. 
Toad.     See  Bufo. 

clawed.     See  Xenopus. 

fire-bellied.     See  Bomhinator. 

obstetric.     See  Alytes. 

Svirinam.     See  Pipa. 
Tomopteris,  luminescence  in,  745 
Topotaxis,  31 

Tornaria  of  Balanoglossus,  227 
Torpedo,  281 

accommodation  in,  647 

blinded,  behaviour  of,  598 

cornea,  281 

electric  organ  of,  751 

pupil,  287 
Tortoise,  372 

See  also  Che\onia,ns,,  Testudo. 
Toucan,  ocular  inovements  of,  696 
Touch.     See  Tactile  sense. 
Toxotes  jaculator,  701 

spatial  judgments  of,  701 
Tracheae,  in  compound  eyes,  168 
Trachinus,  fovea,  310 

ocular  movements,  693 
Trachycephalus,  pupils,  339 
Trachysaurus,  682 

visual  field,  binocular,  682 
Tragulina,  446 


INDEX 


839 


Training  techniques,  569 

colour  vision  and,  624 
Transversalis  inuscle.  in  chelonians,  372 
in  lacertilians,  357 

pigeon,  407 
function  of,  651 
Tree-frog.     See  Hyla. 
Tree-shrew,     See  Shrew,  tree- 
Tree-snakes,  accommodation  in,  648 
fovea,  392 

ocular  movements  of,  695 
pupils,  388 
visual  acuity  of,  661 
field,  675 
Trematodes,  187 

sense  organs  of,  189,  734 
Triakis,  pupil,  286 
Tricheclnis.     See  Manatee. 
Trichomonads,  179,  180 
Trichoptera,  219,  220 
Triclad  worms,  187 
eyes  of,  188 

See  also  Planar ians,  Dendrocoelum. 
Trigla,  visual  field,  binocular,  679 
Trilobite,  157 
eyes  of,  157 
Trinoton  aculeatum,  eyes  of,  221 
Triommatidion  in  aphids,  225 
Triops.     See  Apus. 

Tristomum  papillosurn,  ocellus  of,  130,  189 
Tritocerebrum,  in  arthropods,  521 
Tritiirits  {Triton),  334,  346 

cartilaginous  plaqvies,  347 
colour  vision  in,  628 
eyes  of,  346,  728 
iris  vascularization,  347 
retina,  347,  348 
visual  acuity  of,  661 
cristatus,  347 

colour  changes  in,  92 
pyrrhogaster,  iris,  347 
torosus,  u-is,  347,  371,  PI.  IV 
Troglichthys,  degenerate  eyes  in,  726 
Troihis,  colour  blindness  of,  587 
Tropidonotus  fasciatus,  optic  disc,  390 
natrix  natrix,  384 
chiasma,  392 
ciliary  region,  388 
colour  training,  628 
pupils,  388 
retina,  389 
visual  cells,  391 

field,  binocular,  684 


Tropidonotus  tessellatus,  accommodation, 

649 
Tropo-menotaxis,  61,  68 
Tropotaxis,  31,  52 

definition  of,  43 
Trout.     See  Salmo  trutta. 
Trygon,  285 

iris,  285 

pupils,  287 
Trygonorhina,  pupils,  286,  287 
Trypanosoma,  179,  180 
Trypauchen,  degenerate  ej^es  in,  726 
Trypauchenophrys,  degenerate  eyes  in,  726 
Tuatara.     See  Sphenodon. 
Tuber  nuclei  of  hypothalamus,  559 
Tubular  eyes,  in  cephalopods,  203 
in  fishes,  322,  323,  606 

by  artificial  selection,  324 
optics  of,  642,  643 
visual  field  of,  675,  680 
Tubulidentata,  445 

See  also  Aard-vark. 
Tunicates,  228 

See  also  Ascidians. 
Tunny.     See  Thunnus. 
Tupaia.     See  Shrew,  tree. 
Tupinamhis,  ciliary  region,  358 

nigropunctatus ,  iris,  PI  V 
Turbellarian  worms,  187 
dermal  sensitivity,  114 
nerve-net,  516,  518 
nervous  system,  518,  519 
sense  organs,  188 
See  also  Planarians,  etc. 
Turdus  migratorius,  retinal  summation  in, 

660 
Tvirkey,  nictitating  membrane,  423 

See  also  Meleagris. 
Turris,  sense  organs  of,  183 
Tui-tle,  369 

See  also  Chelonians,  Chrysemys,  Emys, 
etc.        ^'' 
Tylopoda,  446 

corpora  nigra,  470 

pupils,  472 

tapetum  lacking,  458,  609 
Typhlachirus,  degenerate  eyes  in,  726 
Typldceontias,  secondary  spectacle,  367 
TypMias,  degenerate  eyes  in,  725 
Typhlichthys,  degenerate  eyes  in,  726 
Typidocirolana,  degenerate  eyes  in,  725 
Typhlogobius  calif orniensis,  degenerate 

eyes  in,  726 


840 


INDEX 


Typhlomolge,  degenerate  eyes  in,  728 
Typhlonarke,  degenerate  eyes  of,  279,  724 
Typhlonectes,  eyes  of,  730 
Typhlonus,  degenerate  eyes  of,  724 
Typhloperipatus,  degenerate  eyes  in,  724 
Typhlopidse,  383 

eyes  of,  731 
Typhlops,  eye  of,  731 
Typhlotriton,  degenerate  eyes  in,  728 


U 


Uca,  colour  changes  in,  95 
metabolic  rhythm  in,  16 
retinal  pigment  migration  in,  19,  20 
Ultra-violet  light,  visibility  of,  in  insects, 
585,  587 
in  stickleback,  619 
Umbra,  colour  vision  in,  625 

threshold  to  light,  difference,  617 
Umbraculum,  pupillary,  470,  612 
Ungulates,  446 

accommodation  lacking  in,  653 
area  centralis,  485 
arhythmicity  of,  604 
blood  supply  to  eye,  500 
ciliary  muscle,  461 

processes,  466 

region,  461,  462 
circle  of  Hovius,  472 
colour  blindness  of,  634 
cornea,  453 
corpora  nigra,  469 
Moll's  glands,  492 
nictitating  membrane,  493,  496 
ocular  movements  of,  696 
optic  axis,  688 

disc,  486 
orbit,  498 

pectinate  ligament,  464 
pupils,  471 

reactions  of,  472 
ramp -retina,  643 
refraction,  639 
retinal  vascularization,  479 
retractor  bulbi,  495 
spatial  judgments,  704 
tapetum  fibrosum,  457,  609 
vision  of,  601 
visual  acuity  of,  664 

field,  binocular,  689 
uniocular,  672 


I  Ungulates,  zonular  fibres,  475 
See  also  various  genera. 
Uniocular  vision,  697 

visual  fields,  669 
Uranoscopus,  pupil,  329 

visual  field,  binocular,  680 
Urinary  output,  diurnal  rhythm  in,  13 
Urochordates.     See  Tunicates, 
Urodeles,  334 

accommodation  in,  648 
colour  vision  in,  628 
eyes  of,  MQff.,  PL  IV 

degenerate,  726 
lateral  lines,  534 
migration  of  retinal  pigment,  614 

of  visual  cells,  616 
ocular  movements  in,  694 
pineal  organ,  714 
refraction  of,  639 
vision  of,  599 
Uromacer,  visual  field,  binocular,  684 
Ursidae.     See  Bears. 
Uveal  tract,  characteristics  in 
amphibians,  335 
birds,  404 
chelonians,  370 
coelacanth,  315 
dipnoans,  313 
fishes,  277 
lacertilians,  356 
lamprey,  266 
marsupials,  438 
placentals,  457 
selachians,  281 
snakes,  385 
Sphenodon,  380 
teleosts,  296 
See  also  Choroid,  Ciliary  region.  Iris. 


V 

Vampire  bat,  443 
Vanadis,  eye  of,  143 
Vanessa,  170 

colour  vision  in,  587 

scototaxis  in,  56,  60 

vision  of,  585 
Varanus,  conus,  362 

eye  of,  354 

orbit,  368 

visual  field,  binocular,  682 
bengalensis,  iris  furrow,  337 


INDEX 


841 


Vascular  system  of  eye.     See  Blood  supi:)ly 

to  eye. 
Vena  media,  of  anurans,  342 
Ventral  light  reaction,  75 
Vemis  mercenaria,  metabolic  rhythm  in,  15 
Vermilia  infundibulum,  ocelli  of,  192 
Vertebrates,  accommodation  in,  640 
ancestry  of.  233 
angle  gamma  in,  676,  677 
brain  of,  531,  533 
central  nervous  system,  530 

development  of,  531,  532 
eyes  of,  259  ff. 

adaptations  of,  254 
degenerate,  723,  725,  730,  734 
embryology  of,  239 
evolution  of,  233 
ontogeny  of,  239 
origin  of,  242 

from  Arnphioxus,  244 
from  Ascidian,  245 
placode  theory  of,  246 
phylogeny  of,  237 
structure  of,  248,  254 
movement,  perception  of,  in,  706 
neuro -endocrine  system,  552,  556,  557 
ocular  movements  in,  689 
optic  axis,  688 
phylum  of,  233,  234 
pineal  apparatus,  711 
refraction  of,  638 
vision  of,  597 
colour,  619 
form,  637 
visual  acuity  of,  660 
fields,  binocular,  672 
uniocular,  669 
Vesicular  eyes,  141 
Vespa,  219 

vision  of,  584,  585 
See  also  Wasps. 
Vespertilio,  443 

Vibratorj-  receptors,  116,  534,  597 
in  cetaceans,  601 
fishes,  598 
snakes,  599,  667 
Vibrotropism,  in  spiders,  579 
Viper,  European.     See  Vipera  berus. 
horned,  392 
pit.     See  Crotalus,  etc. 
Vipera  berus,  optic  disc,  390 

visual  cells,  392 
Viperidse,  facial  pit  in,  117,  599,  600 


Viperidse,  visual  cells,  392 
Vision,  central  organization  of,  509 
hormonal,  547 
nervous,  511 
colour.     See  Colour  vision, 
form.     See  Form  vision,  Visual  acuity, 
genesis  of,  102 
imaginative,  753 
of  invertebrates,  570 
arachnids,  579 
arthropods,  577 
irisects,  581 
molluscs,  574 

cephalopod,  575 
worms,  572 
of  vertebrates,  597 
binocular,  697 
uniocular,  697 
perceptual,  753 
Visual  acuity,  of  insects,  588 
of  vertebrates,  660 
amphibians,  661 
birds,  662 
fishes,  660 
mammals,  663 
reptiles,  661 
axis,  675,  676,  683 
cells,  250 

characteristics  in 

invertebrates,  127,  128 
apolar,  131 
bipolar,  130 

See  also  Light-sensitive  cells, 
vertebrates,  250 
anurans,  342,  344 
birds,  419 

chelonians,  372,  374 
chondrosteans,  320 
crocodiliaixs,  377 
dipnoans.  313,  314 
holosteans,  321,  322 
lacertilians,  363,  364 
lamprey,  268,  269 
Latimer ia,  315 
marsupials,  440,  441 
monotremes,  436 
Periophthalmus,  327 
placentals,  482 
selachians,  288 
snakes,  391,  392 
Sphenodon,  382 
teleosts,  305,  307 
urodeles,  347,  348 


842 


INDEX 


Visual  cells,  development  of,  243 
lengthening  of,  643 
migration  of,  614,  615 

rhythmic,  19 
multiple,  253 
origin  of,  252 
centres,  evolution  of,  543 

in  mid-brain,  534 
fields,  binocular,  672 
of  amphibians,  682 
birds,  682,  684 
cyclostomes,  678 
fishes,  678,  679 
mamiTials,  687,  689 
reptiles,  682 
uniocular,  669,  670 
illusions,  703 
judgments,  700 
orientations,  669 

pathways,  cortical  projection,  544 
evolution  of,  543 
in  amphibians,  537 

arthropods,  524,  525,  526 
birds,  539 

cephalopods,  528,  529 
cyclostomes,  535 
fishes,  536 
mammals,  540 
reptiles,  538 
pigments,  118 
purple,  122 
trident,  684 
violet,  122 
Vital  spirits,  28 

Vitamin  A  pigment  system,  120 
in  arthropods,  121 
molluscs,  120 
vertebrates,  121 
Vitrellai,  in  compound  eyes,  167 
Vitreous,  characteristics  in 
placentals,  476 
selachians,  287 
teleosteans,  304 
Viverridse,  445 

pupils,  470,  471,  472 
retinal  vascularization,   479 
Vizcacha,  442,  445 

pupils,  472 
Vole,  field-,  445 
eye  of,  450 
red-backed,  colour  vision  in,  633 
Volvox,  179,  180 
globator,  klinotaxis  in,  49 


Vorticella,  179,  180 

Vulpes.     See  Fox. 

Vulture,  African,  visual  acuity  of,  662 

W 

Walckenae7-a  acuminata,  eyes  of,  214 
Wallaby,  437,  440 

ciliary  region,  439 

eye  of,  438 
Walls,  Gordon,  352,  353 
Walrus,  445 

ocular  adnexa,  501 

pupils,  470 

See  also  Pinnipedes. 
"  Warning  colours  ",  631 
Wasps,  219,  220 

digger-.     See  Philanthus. 

eyes  of,  160 

mnemotaxis  in,  79 

time-memory  in,  22 

See  also  Vespa. 
Water-beetle.     See  Dytiscus. 
Water-fleas.    See  Cladocera. 
Weasel,  445,  472 

pupils,  472 
Whale,  beaked,  ciliary  receptor  organs,  467 

blue,  444,  446 
eyes  of,  449 

hump-back,  444,  446 

ciliary  receptor  organs,  467 
sclera,  451 

killer,  446 

right-,  446 

sperm-,  444,  446 

See  also  Cetaceans. 
Whelk.    See  Buccinum. 
Whip-tailed  scorpion,  214 
activity  of,  34 
eyes  of,  149,  150,  214 
Whirligig  beetle,  74 

accommodation,  static,  591 
orientation  of,  74 
See  also  Dineutus. 
Winteria,  tubvilar  eyes  in,  324 
Wolf  {Canis  lupus),  445 

accommodation  in,  653 

eye  of,  447 

nictitating  membrane,  493 

optic  disc,  486 
Wolverine,  pupils,  472 
Wombat,  437,  441 
Wood,  Casey  Albert,  396,  397 


INDEX 


843 


Woodlice,  206 

eyes  of,  206 
lacking,  729 

See  also  Annadillidiuni,  Oniscus. 
Woodpecker.     See  Dendrocopus, 

Melanerpes. 
Worms,  186 

bilateral  symmetry  in,  186,  517 

bioluminescence  in,  739,  745 

eyes  of,  187 

nerve -net,  515,  518 

nervous  system,  518 

receptor-effector  system,  514 

segmented.     See  Annelids. 

unsegmented,  187 

phototactic  reactions  of,  572 
See  also  Platyhelminthes,  etc. 

vision  of,  572 
W-substance  in  amj^hibians,  97 


X 


Xanthophores,  88 

in  corneal  epithelium  of  fishes,  295 
Xanthophyll,  119 

in  human  macula,  122 
Xanthnsia,  foveal  pit,  365 
pupils,  359 
visual  cells,  252,  364 
Xenarthra,  445 

cornea,  keratinized,  456 
retinal  vascularization,  480 
visual  cells,  482 
Xenopus  Icevis,  334,  337 

colour  changes  in,  91,  98 

pineal  organ  and,  719 
iris,  337 

migration  of  pigment  absent,  614 
reproductive  cycle  in,  17 
retina,  343 


Xerus.     See  Squirrel,  African. 
Xiphias,  294 

dilatator  muscle,  303 

optic  nerve,  311 

scleral  ossicles,  294 
Xiphosura,  212 

neuro -endocrine  system,  552 

See  also  Limulus. 
X-organ,  in  crustaceans,  552,  553 

in  myriajDods,  552 


Zaglossus.     See  Echidna. 
Zamenis,  visual  field,  binocular,  684 
Zebra  (Equus  zebra),  444,  446 
corpora  nigra,  469 
See  also  Equidse. 
Zeis's  glands,  in  elejshant,  491 
Zenaidura  macroura,  reproductive  cycle  in. 

18 
Zenion,  eyes  of,  323 
Zonosaurus,  eyelids,  367 
Zonular  fibres,  characteristics  in 
anurans,  335 
■     birds,  410 

lacertilians,  361 
monotremes,  436 
placentals,  475 
selachians,  285 
snakes,  389 
Sphenodon,  381 
See  also  Suspensory  ligament. 
Zonurus  giganteus,  visual  field,  binocular, 

682 
Zoraptera,  220 

Zosterops  japonica,  reproductive  cycle  in, 
18 


I 


-4ri-[-*^r»T?r^^^;--