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J  Aug.  24,    1963                            I 

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THE  LIFE  OF 

VERTEBRATES 


THE  LIFE  OF 

VERTEBRATES 


BY 

J.  Z.  YOUNG 

M.A.,  F.R.S. 

PROFESSOR  OF  ANATOMY  AT 
UNIVERSITY   COLLEGE,    LONDON 


SECOND  EDITION 


OXFORD  UNIVERSITY  PRESS 

NEW  YORK  &  OXFORD 

1962 


©  Oxford  University  Press  ig^2 
Library  of  Congress  Catalogue  Card  Number:  62-21012 


First  Edition  1950 
Second  Edition  1962 


Printed  in  the  United  States  of  America 


ACKNOWLEDGEMENTS 

My  grateful  thanks  are  due  to  the  following,  who  spent  much  time  reading  and 
criticizing  various  parts  of  the  manuscripts  and  proofs: 

E.  H.  Ashton,  A.  d'A.  Bellairs,  Q.  Bone,  B.  B.  Boycott,  P.  M.  Butler,  S.  Crowell, 

D.  H.  Cushing,  F.  C.  Fraser,  R.  B.  Freeman,  H.  Greenwood,  I.  Griffiths,  R.  J. 
Harrison,  R.  A.  Hinde,  K.  A.  Kermack,  J.  Lever,  N.  B.  Marshall,  D.  R.  Newth, 
C.  Nicol,  F.  R.  Parrington,  P.  Robinson,  A.  J.  Sutcliffe,  H.  G.  Vevers,  E.  I. 
White,  M.  Whitear. 

Thanks  for  permission  for  reproductions  of  illustrations  are  due  to: 

G.  C.  Aymar,  E.  J.  W.  Barrington,  J.  Berrill,  T.  H.  Bullock,  A.  J.  E.  Cave, 
W.  E.  Le  Gros  Clark,  E.  Crosby,  F.  G.  Evans,  Helen  Goodrich,  A.  Gorbman, 
J.  Gray,  W.  K.  Gregory,  W.  J.  Hamilton,  J.  E.  Harris,  L.  Hogben,  A.  Holmes, 

E.  Hoskings,  W.  W.  Howells,  J.  S.  Huxley,  F.  Knowles,  D.  Lack,  N.  A.  Mackin- 
tosh, G.  H.  Parker,  A.  T.  Phillipson,  R.  J.  Pumphrey,  E.  C.  R.  Reeve,  A.  S. 
Romer,  E.  S.  Russell,  F.  K.  Sanders,  A.  H.  Schultz,  G.  G.  Simpson,  N.  Tinber- 
gen,  G.  L.  Walls,  L.  Waring,  T.  S.  Westoll,  E.  I.  White,  F.  F.  Zeuner, 

and  to  the  following  publishers  and  other  bodies: 

The  American  Museum  of  Natural  History;  Bailliere,  Tindall  and  Cox;  E. 
Benn,  Ltd. ;  Biological  Reviezvs ;  the  British  Medical  Journal;  the  British  Museum ; 
the  Cambridge  University  Press;  the  Company  of  Biologists,  Ltd.;  Dodd,  Mead 
&  Co.;  Editors  of  the  Ibis;  Longmans,  Green  &  Co.,  Ltd.;  the  Physiological 
Society;  Putnam,  Ltd.;  the  Scientific  Monthly;  the  Wilson  Bulletin;  the  Wistar 
Institute;  Zoological  Society  of  London. 


PREFACE  TO 
THE  SECOND  EDITION 

For  this  edition  every  part  of  the  book  has  been  revised  and  corrected, 
but  the  basic  plan  and  balance  of  interests  have  not  been  altered. 
Changes  of  arrangement  and  emphasis  might  have  suited  some  types 
of  reader  but  I  have  thought  it  better  that  the  book  should  continue 
to  show  the  idiosyncracies  and  interests  of  the  author.  One  of  the 
dangers  of  a  textbook  is,  surely,  that  unsophisticated  readers  may  sup- 
pose that  they  are  getting  the  authentic  and  complete  treatment  of  the 
subject.  Some  obvious  imbalances  may,  therefore,  even  be  an  advan- 
tage as  reminders  of  the  relativity  of  all  statements. 

Nevertheless,  I  have  attempted  to  make  the  treatment  rather  more 
complete  and  systematic  than  before.  For  example,  the  descriptions 
of  the  parts  of  the  body  are  now  arranged  more  nearly  similarly  for  all 
groups.  With  the  help  of  many  friends  mistakes  have  been  removed 
and  accounts  of  recent  work  added.  The  anatomy  of  Mammals  is  not 
dealt  with  in  the  same  detail  as  that  of  other  groups,  being  covered 
separately  in  The  Life  of  Mammals  (Clarendon  Press,  1957),  where 
also  there  is  a  fuller  account  of  the  comparative  embryology  of 
vertebrates. 

During  the  revision  I  have  become  even  more  conscious  of  the 
defects  of  the  work,  both  in  general  form  and  detailed  treatment.  It  is 
still  not  possible  to  see  more  than  the  vaguest  outlines  of  a  proper 
science  of  comparative  biology.  We  are  faced  with  a  great  series  of 
wonderful  systems,  differing  slightly  from  each  other  and  maintaining 
themselves  in  slightly  different  surroundings.  But  we  have  no  proper 
scientific  words  with  which  to  talk  about  them.  For  example,  it  is 
absurd  that  this  book  contains  so  little  reference  to  genetics,  bio- 
chemistry, or  control  theory.  No  doubt  this  is  partly  my  fault,  but  the 
fact  is  that  these  more  exact  sciences  have  yet  to  show  us  how  to  treat 
the  organization  of  a  whole  creature. 

Fortunately,  the  animals  remain  as  fascinating  as  ever,  indeed  the 
search  for  exact  ways  of  describing  makes  them  even  more  so.  Those 
of  us  who  have  revised  the  book  will  be  well  rewarded  for  our  trouble 
if  others  arc  helped  to  look  and  think  for  themselves.  If  they  do  they 
will  find  a  really  astonishing  array  of  experiments  made  by  natural 
selection  with  every  part  of  the  vertebrate  organization.  To  take  one 
example,  we  are  offered  the  opportunity  to  learn  how  the  endocrine 


vi  PREFACE  TO  SECOND  EDITION 

control  system  works  by  examining  hundreds  of  different  variants  of 
it.  The  more  one  thinks  of  it  the  more  surprising  it  is  that  biology 
has  made  so  little  use  of  the  experiments  that  have  been  done  for  us 
by  nature.  Surely  soon  someone  will  come  along  with  sufficient  know- 
ledge and  logical  and  mathematical  ingenuity  to  show  us  how  to  study 
vertebrate  organization. 

Besides  those  mentioned  below  who  have  assisted  in  the  revision  of 
particular  sections,  I  should  like  to  thank  the  many  people,  including 
teachers  and  students,  who  have  written  about  particular  points,  and 
especially  Professor  J.  Lever  of  Amsterdam  for  his  many  detailed 
comments.  My  grateful  thanks  are  also  due  to  Mrs.  J.  Astafiev,  who 
has  redrawn  many  of  the  figures,  Mr.  C.  Marmoy  for  assistance  with 
the  Bibliography,  Mr.  P.  N.  Dilly,  who  has  helped  throughout,  also 
my  secretaries  and  especially  Miss  S.  Thistleton  and  Miss  J.  Everard, 
for  continuous  help  with  the  manuscript.  It  is  also  a  pleasure  to  thank 
the  members  of  the  Clarendon  Press  and  in  particular  Miss  M.  Gregory 
for  the  help  with  the  revision. 

J.  Z.  Y. 

February  1962 


PREFACE  TO 
THE  FIRST  EDITION 

The  history  of  textbooks  is  often  dismissed  by  the  contemptuous 
assertion  that  they  all  copy  each  other — and  especially  each  other's 
mistakes.  Inspection  of  this  book  will  quickly  confirm  that  this  is  true, 
but  there  is  nevertheless  an  interest  to  be  obtained  from  such  a  study, 
because  textbooks  embody  an  attitude  of  mind;  they  show  what  sort 
of  knowledge  the  writer  thinks  can  be  conveyed  about  the  subject- 
matter.  It  may  be  that  they  are  more  important  than  at  first  appears 
in  furthering  or  preventing  the  change  of  ideas  on  any  theme. 

The  results  of  the  studies  of  scholars  on  the  subject  of  vertebrates 
have  been  summarized  in  a  series  of  comprehensive  textbooks  during 
the  past  hundred  years.  Most  of  these  works  are  planned  on  the  lines 
laid  down  by  the  books  of  Gegenbaur  (1859),  Owen  (1866),  and 
Wiedersheim  (1883),  lines  that  derive  from  a  pre-evolutionary  tradi- 
tion. This  partly  explains  the  curiosity  that  in  spite  of  the  great  impor- 
tance of  evolutionary  doctrine  for  vertebrate  studies,  and  vice  versa, 
vertebrate  textbooks  often  do  not  deal  directly  with  evolution.  They 
derive  their  order  from  something  even  more  fundamental  than  the 
evolutionary  principle.  The  essential  of  any  good  textbook  is  that  it 
should  be  both  accurate  and  general.  As  Owen  puts  it  in  his  Preface: 
Tn  the  choice  of  facts  I  have  been  guided  by  their  authenticity  and 
their  applicability  to  general  principles.'  The  chief  of  the  principles 
he  adopted  was  'to  guide  or  help  in  the  power  of  apprehending  the 
unity  which  underlies  the  diversity  of  animal  structures,  to  show  in 
these  structures  the  evidence  of  a  predetermining  Will,  producing 
them  in  reference  to  a  final  purpose,  and  to  indicate  the  direction  and 
degrees  in  which  organisation,  in  subserving  such  Will,  rises  from  the 
general  to  the  particular'.  He  confessed  'ignorance  of  the  mode  of 
operation  of  the  natural  law  of  their  succession  on  the  earth.  But  that 
it  is  an  "orderly  succession" — and  also  "progressive" — is  evident 
from  actual  knowledge  of  extinct  species.' 

These  principles  were  essentially  sound,  and  Owen's  treatment  was 
to  a  large  extent  the  basis  of  the  work  that  appeared  after  the  Dar- 
winian revolution.  In  English,  following  the  translation  of  Wieder- 
sheim's  book  by  W.  N.  Parker  (1886)  we  have  H.  J.  Parker  and 
Haswell's  work,  now  in  its  6th  edition.  The  books  of  Kingsley  and 
Neal  and  Rand  are  in  essentially  the  same  tradition,  though  they 


viii  PREFACE  TO  FIRST  EDITION 

incorporate  much  new  work,  especially  from  the  neurological  studies 
of  Johnston  and  Herrick.  Further  exact  studies  on  these  same  general 
morphological  lines  made  possible  the  books  of  Goodrich  (1930)  and 
de  Beer  (1935),  which  have  provided  the  morphological  background 
for  the  present  work.  Throughout  these  works  on  Comparative  Ana- 
tomy the  emphasis  is  on  the  evolution  of  the  form  of  each  organ 
system  rather  than  on  the  change  of  the  organization  of  the  life  of 
the  animal  as  a  whole. 

Meanwhile  many  other  treatises  appeared  dealing  with  the  life  and 
habits  of  the  animals,  rather  than  with  morphological  principles. 
Among  these  we  may  mention  Bronn's  Tierreich  (1859  onwards),  the 
Cambridge  Natural  History,  and  many  works  dealing  with  particular 
groups  of  vertebrates.  The  palaeontologists  produced  their  own  series 
of  textbooks,  mainly  descriptive,  such  as  those  of  Zittel  and  Smith 
Woodward,  culminating  in  Romer's  admirably  detailed  and  concise 
book,  to  which  the  present  work  owes  very  much.  The  results  of 
embryological  work  have  been  summarized  by  Graham  Kerr  (191 9), 
Korscheldt  and  Heider  (1931),  Brachet  (1935),  Huxley  and  de  Beer 
(1934),  and  Weiss  (1939),  among  others.  Unfortunately  there  has  been 
little  summarizing  of  what  is  commonly  called  the  comparative  physio- 
logy of  vertebrates.  Winterstein's  great  Handbuch  der  vergleichenden 
Physiologie  (191 2)  covers  much  detailed  evidence,  but  comes  no  nearer 
than  do  the  comparative  anatomists  to  giving  us  a  picture  of  the 
evolution  of  the  life  of  the  whole  organism. 

All  of  these  books  deal  in  some  way  with  the  evolution  of  vertebrates, 
and  vet  curiously  enough  they  speak  of  it  very  little.  It  is  hardly  an 
exaggeration  to  say  that  they  leave  the  student  to  decide  for  himself 
what  has  been  demonstrated  by  their  studies.  Huxley's  Anatomy  of 
Vertebrated  Animals  (1871)  is  an  exception  in  that  it  deals  with  the 
animals  rather  than  their  parts,  and  at  a  more  popular  level.  Brehm's 
Thierleben  (1876)  gives  a  picture  of  the  life  of  the  animals,  though  in 
this  case  not  of  their  underlying  organization.  Kukenthal's  great 
Handbuch  der  Zoologie  has  the  aim  of  synthesizing  a  variety  of  know- 
ledge about  each  animal-group,  and  some  of  the  volumes  dealing  with 
vertebrates  make  fascinating  reading- — notably  that  of  Streseman  on 
birds.  But  the  size  of  the  work  and  the  multiplicity  of  authors  make 
it  impossible  for  any  general  picture  of  vertebrate  life  to  appear  from 
the  mass  of  details. 

The  position  is,  then,  that  we  have  good  descriptions  of  the  struc- 
ture, physiology,  and  development  of  vertebrates,  of  the  discoveries 
of  the  palaeontologists  and  accounts  of  vertebrate  natural  history,  but 


PREFACE  TO  FIRST  EDITION  ix 

that  there  is  no  work  that  attempts  to  define  the  organization  of  the 
whole  life  and  its  evolution  in  all  its  aspects.  Indeed,  none  of  these 
works  defines  what  is  being  studied  or  tries  to  alter  the  direction  of 
investigation — all  authors  seem  prepared  to  agree  that  biological  study 
is  adequately  expressed  through  the  familiar  disciplines  of  anatomy, 
physiology,  palaeontology,  embryology,  or  natural  history.  In  passing, 
we  may  note  the  extraordinary  fact  that  there  are  no  detailed  works  on 
the  comparative  histology  or  biochemistry  of  vertebrates — surely  most 
fascinating  fields  for  the  future,  as  is,  indeed,  hinted  by  the  attempts 
that  have  been  made  in  older  works,  such  as  that  of  Ranvier  (1878), 
and  the  newer  ones  of  Baldwin  (1937  and  1945). 

The  present  book  has  gradually  grown  into  an  attempt  to  define 
what  is  meant  by  the  life  of  vertebrates  and  by  the  evolution  of  that 
life.  Put  in  a  more  old-fashioned  way,  this  represents  an  attempt  to 
give  a  combined  account  of  the  embryology,  anatomy,  physiology, 
biochemistry,  palaeontology,  and  ecology  of  all  vertebrates.  One  of 
the  results  of  the  work  has  been  to  convince  me  more  than  ever  that 
these  divisions  are  not  acceptable.  All  of  their  separate  studies  are 
concerned  with  the  central  fact  of  biology,  that  life  goes  on,  and  I 
have  tried  to  combine  their  results  into  a  single  work  on  the  way  in 
which  this  continuity  is  maintained. 

A  glance  through  the  book  will  show  that  I  have  not  been  successful 
in  producing  anything  very  novel — others  will  certainly  be  able  to 
go  much  farther,  and  in  particular  to  introduce  to  a  greater  extent  facts 
about  the  evolution  of  the  chemical  and  energy  interchanges  of  verte- 
brates, here  almost  omitted!  However,  I  have  very  much  enjoyed  the 
attempt,  which  has  provided  the  stimulus  to  try  to  find  out  many 
things  that  I  have  always  wanted  to  know. 

For  any  one  person  to  cover  such  a  wide  field  is  bound  to  lead  to 
inexactness  and  error  in  many  places.  I  have  tried  to  verify  from 
nature  as  often  as  possible,  but  a  large  amount  has  been  copied,  no 
doubt  often  wrongly.  Throughout,  the  aim  has  been  to  provide 
wherever  possible  an  idea  of  the  actual  observations  that  have  been 
made,  as  well  as  the  interpretations  placed  upon  them.  A  proper 
appraisal  of  general  theories  can  only  be  reached  if  there  is  first  a 
knowledge  of  the  actual  materials,  which  is  the  characteristic  feature 
of  scientific  observation.  A  book  such  as  the  present  has  value  only 
in  so  far  as  it  leads  the  reader  to  make  his  own  observations  and  helps 
him  to  know  the  world  for  himself. 

Mammalian  organization  requires  more  detailed  treatment  than 
that  of  other  groups,  and  in  providing  this  the  work  grew  to  beyond 


x  PREFACE  TO  FIRST  EDITION 

the  length  of  a  single  book.  Mammalian  structure,  function,  and 
development  will  therefore  be  dealt  with  in  a  separate  volume,  which 
will  also  include  a  survey  of  comparative  embryology. 

The  original  plan  was  that  the  palaeontological  parts  of  the  book 
would  be  written  by  J.  A.  Moy-Thomas.  Had  he  lived  this  aspect  of 
the  work  would  have  been  very  much  better,  and  his  common  sense 
and  laughter  would  have  lightened  the  whole.  I  have  tried  to  give 
some  compensation  at  least  by  the  speculation  that  is  possible  from  a 
single  point  of  view.  To  protect  the  reader  against  the  limitations  of 
my  ignorance  I  have  consulted  specialists  on  every  part  of  the  work, 
and  my  deepest  thanks  are  due  to  those  who  have  helped  in  this  way. 
They  have  done  wonders  in  correcting  mistakes,  but,  of  course,  are 
not  responsible  for  any  that  remain,  or  for  views  expressed.  Among 
those  who  have  helped  in  this  way  with  particular  parts  are  Professor 
G.  R.  de  Beer,  Mr.  R.  B.  Freeman,  the  late  Professor  W.  Garstang, 
Dr.  A.  Graham,  Professor  J.  B.  S.  Haldane,  Professor  W.  Holling- 
worth,  Dr.  W.  Holmes,  Dr.  J.  S.  Huxley,  Dr.  D.  Lack,  Mr.  Maynard 
Smith,  Dr.  F.  S.  Russell,  Dr.  Tyndell  Hopwood,  Mr.  H.  G.  Vevers, 
Professor  D.  M.  S.  Watson,  and  Professor  S.  Westoll.  They  have  been 
patient  and  severe  critics,  and  the  reader  and  I  owe  them  very  much. 

One  of  the  main  problems  of  such  a  work  is  its  illustration,  and  here 
I  have  been  extraordinarily  fortunate  in  having  the  help  of  Miss  E.  R. 
Turlington,  who  has  not  only  provided  brilliantly  clear  and  beautiful 
pictures,  but  has  taken  extremes  of  care  to  ensure  their  accuracy  by 
drawing  from  live  animals,  from  dissections,  and  from  skeletons,  as 
well  as  by  research  into  the  illustrations  of  others.  Miss  J.  de  Vere 
has  also  given  much  help  with  drawing.  We  have  borrowed  good 
pictures  unhesitatingly  and  should  like  to  thank  those  who  have  given 
permission  for  their  reproduction. 

I  should  also  like  to  thank  particularly  my  secretary,  Miss  P.  Codlin, 
who  has  played  a  large  part  in  making  the  book  possible,  and  my 
daughter  Cordelia  for  help  with  the  index. 

Finally,  I  have  to  thank  the  Secretary  and  members  of  Oxford 
University  Press  for  the  care  with  which  the  book  has  been  produced, 
and  for  their  friendly  co-operation,  which  has  made  the  work  a 
pleasure. 

J.  Z.  Y. 

1950 


CONTENTS 


I.  EVOLUTION  OF  LIFE  IN  RELATION  TO  CLIMATIC  AND  GEO- 

LOGICAL CHANGE 

i.  The  need  for  generality  in  zoology,  i ;  2.  What  do  we  mean  by  the  life  of  an 
animal  ?  2;  3.  Li ving  things  tend  to  preserve  themselves,  3;  4.  What  do  we  mean  by 
awareness  of  life  ?  5 ;  5.  The  influence  of  environment  on  life,  7 ;  6.  What  is  it  that 
heredity  transmits  ?  8 ;  7.  The  increasing  complexity  of  life,  9 ;  8.  The  progression 
of  life  from  the  water  to  more  difficult  environments,  9;  9.  Changes  of  climate  and 
geological  periods — (1)  Changes  of  level  of  the  continents,  11;  (2)  Changes  of 
climate,  13;  (3)  Geological  time,  16;  (4)  Classification  of  geological  history,  18; 
10.  Summary,  21. 

II.  THE  GENERAL  PLAN  OF  CHORDATE  ORGANIZATION:  AMPHI- 

OXUS 

1.  The  variety  of  chordate  life,  23;  2.  Classification  of  chordates,  24;  3.  Amphi- 
oxus,  a  generalized  chordate,  24;  4.  Movement  of  amphioxus,  26;  5.  Skeletal 
structures  of  amphioxus,  29;  6.  Skin  of  amphioxus,  29;  7.  Mouth  and  pharynx 
and  the  control  of  feeding,  30;  8.  Circulation,  33;  9.  Excretory  system  of 
amphioxus,  35;  10.  Nervous  system,  36;  11.  Gonads  and  development  of 
amphioxus,  41;  12.  Amphioxus  as  a  generalized  chordate,  46. 

III.  THE  ORIGIN  OF  CHORDATES  FROM  FILTER  FEEDING  ANIMALS 
1.  Invertebrate  relatives  of  the  chordates,  47;  2.  Subphylum  Hemichordata 
(=  Stomochordata),  50;  3.  Class  Pterobranchia,  58;  4.  Subphylum  Tunicata. 
Sea  squirts,  60;  5.  Development  of  ascidians,  66;  6.  Various  forms  of  tunicate, 
69;  7.   Class  Ascidiacea.  70;   8.   Class  Thaliacea,  70;  9.   Class  Larvacea,  72; 

10.  The  formation  of  the  chordates,  74. 

IV.  THE  VERTEBRATES  WITHOUT  JAWS.  LAMPREYS 

1.  Classification,  81;  2.  General  features  of  vertebrates,  81;  3.  Agnatha,  83; 
4.  Lampreys,  83;  5.  Skeleton  of  lampreys,  85;  6.  Alimentary  canal  of  lampreys, 
88;  7.  Blood  system  of  lampreys,  91;  8.  Urinogenital  system  of  lampreys,  93; 
9.  Nervous  system  of  lampreys,  97;  10.  The  pineal  eyes,  103;  1 1.  Pituitary  body 
and  hypophyseal  sac,  106;  12.  Lateral  line  organs  of  lampreys,  108;  13.  Vesti- 
bular organs  of  lampreys,  109;  14.  Paired  eyes  of  lampreys,  no;  15.  Skin  photo- 
receptors, in;  16.  Habits  and  life-history  of  lampreys,  112;  17.  The  ammocoete 
larva,  114;  18  Races  of  lampreys,  a  problem  in  systematics,  119;  19.  Hag-fishes, 
order  Myxinoidea,  122;  20.  Fossil  Agnatha,  the  earliest-known  vertebrates,  125. 

V.  THE  APPEARANCE  OF  JAWS.  THE  ORGANIZATION  OF  THE  HEAD 
1.  The  elasmobranchs :  introduction,  131;  2.  The  swimming  of  fishes,  133; 
3.  Equilibrium  of  fishes  in  water;  the  functions  of  the  fins,  136;  4.  Skin  of 
elasmobranchs,  141;  5.  The  skull  and  branchial  arches,  142;  6.  The  jaws,  145; 
7.  Segmentation  of  the  vertebrate  head,  148;  8.  The  pro-otic  somites  and  eye- 
muscles,  149;  9.  The  cranial  nerves  of  elasmobranchs,  152;  10.  Respiration,  157; 

11.  The  gut  of  elasmobranchs,  158;  12.  The  circulatory  system,  159;  13.  Urino- 
genital system,  162;  14.  Endocrine  glands  of  elasmobranchs,  164;  15.  Nervous 
system,  167;  16.  Receptor-organs  of  elasmobranchs,  170;  17.  Autonomic  nervous 
system,  173. 


81659 


xii  CONTENTS 

VI.  EVOLUTION  AND  ADAPTIVE  RADIATION  OF  ELASMOBRANCHS 
i.  Characteristics  of  elasmobranchs,  175;  2.  Classification,  175;  3.  Palaeozoic 
elasmobranchs,  176;  4.  Mesozoic  sharks,  180;  5.  Modern  sharks,  180;  6.  Skates 
and  rays,  182;  7.  Chimaera  and  the  bradyodonts,  184;  8.  Tendencies  in  elasmo- 
branch  evolution,  185;  9.  The  earliest  Gnathostomes,  Placoderms,  186. 

VII.  THE  MASTERY  OF  THE  WATER.  BONY  FISHES 

1.  Introduction:  the  success  of  the  bony  fishes,  190;  2.  The  trout,  191;  3.  The 
skull  of  bony  fishes,  193;  4.  Respiration,  196;  5.  Vertebral  column  and  fins 
of  bony  fishes,  199;  6.  Alimentary  canal,  201 ;  7.  Air-bladder,  201 ;  8.  Circulatory 
system,  201 ;  9.  Urinogenital  system  and  osmoregulation,  202;  10.  Races  of  trout 
and  salmon  and  their  breeding  habits,  204;  1 1.  Endocrine  glands  of  bony  fishes, 
206;  12.  Brain  of  bony  fishes,  209;  13.  Receptors  for  life  in  the  water,  212; 
14.  Eyes,  212;  15.  Ear  and  hearing  of  fishes,  216;  16.  Sound  production  in 
fishes,  218;  17.  The  lateral  line  organs  of  fishes,  218;  18.  Chemoreceptors. 
Taste  and  smell,  220;  19.  Touch,  222;  20.  Autonomic  nervous  system,  222; 
21.  Behaviour  patterns  of  fishes,  225. 

VIII.  THE  EVOLUTION  OF  BONY  FISHES 

1.  Classification,  228;  2.  Order  1.  Palaeoniscoidei,  228;  3.  Order  2.  Acipen- 
seroidei,  234;  4.  Superorder  2.  Holostei,  234;  5.  Superorder  3.  Teleostei,  236; 

6.  Analysis  of  evolution  of  the  Actinopterygii,  237. 

IX.  THE  ADAPTIVE  RADIATION  OF  BONY  FISHES 

I.  Swimming  and  locomotion,  244;  2.  Various  body  forms  and  swimming  habits 
in  teleosts,  248;  3.  Structure  of  mouth  and  feeding-habits  of  bony  fishes,  251; 
4.  Protective  mechanisms  of  bony  fishes,  252;  5.  Scales  and  other  surface  armour, 
252;  6.  Spines  and  poison  glands,  253;  7.  Electric  organs,  253;  8.  Luminous 
organs,  254;  9.   Colours  of  fishes,  255;    10.   Colour  change  in  teleosts,  258; 

II.  Aerial  respiration  and  the  air-bladder,  261;  12.  Special  reproductive 
mechanisms  in  teleosts,  265. 

X.  LUNG-FISHES 

1.  Classification,  268;  2.  Crossopterygians,  268;  3.  Osteolepids,  268;  4.  Coela- 
canths,  271;  5.  Fossil  Dipnoi,  273;  6.  Modern  lung-fishes,  275. 

XI.  FISHES  AND  MAN,  280 

XII.  TERRESTRIAL  VERTEBRATES:  AMPHIBIA 

1.  Classification,  296;  2.  Amphibia,  296;  3.  The  frogs,  298;  4.  Skin  of  Amphibia, 
298;   5.  Colours  of  Amphibia,  299;  6.  Vertebral  column  of  Amphibia,  303; 

7.  Evolution  and  plan  of  the  limbs  of  Amphibia,  307;  8.  Shoulder  girdle  of 
Amphibia,  309;  9.  Pelvic  girdle  of  Amphibia,  312;  10.  The  limbs  of  Amphibia, 
313;  1 1.  The  back  and  belly  muscles  of  Amphibia,  318;  12.  The  limb  muscles  of 
Amphibia,  322;  13.  The  skull  of  Stegocephalia,  325;  14.  The  skull  of  modern 
Amphibia,  328;  15.  Respiration  in  Amphibia,  332;  16.  Respiration  in  the  frog, 
333;  I7-  Respiratory  adaptations  in  various  amphibians,  334;  18.  Vocal  appara- 
tus, 334;  19.  Circulatory  system  of  Amphibia,  335;  20.  Lymphatic  system  of 
Amphibia,  338;  21.  The  blood  of  Amphibia,  339;  22.  Urinogenital  system  of 
Amphibia,  340;  23.  Digestive  system  of  Amphibia,  342;  24.  Nervous  system 
of  Amphibia,  344;  25.  Skin  receptors,  349;  26.  The  eyes  of  Amphibia,  350;  27. 
The  ear  of  Amphibia,  353;  28.  Behaviour  of  Amphibia,  354. 


CONTENTS  xiii 

XIII.  EVOLUTION  AND  ADAPTIVE  RADIATION  OF  AMPHIBIA 

i.  The  earliest  Amphibia,  356;  2.  Terrestrial  Palaeozoic  Amphibia.  Embolomeri 
and  Rhachitomi,  357;  3.  Aquatic  Amphibia  of  the  later  Palaeozoic,  359; 
4.  Tendencies  in  the  evolution  of  fossil  Amphibia,  362;  5.  Newts  and  Salaman- 
ders. Subclass  Urodela,  364;  6.  Frogs  and  Toads.  Subclass  Anura,  365;  7.  Sub- 
class Apoda  (—  Gymnophiona  =  Caecilia),  366;  8.  Adaptive  radiation  and 
parallel  evolution  in  modern  Amphibia,  366;  9.  Can  Amphibia  be  said  to  be 
higher  animals  than  fishes  ?  367. 

XIV.  LIFE  ON  LAND:  THE  REPTILES 

1.  Classification,  369;  2.  Reptilia,  371;  3.  The  organization  of  reptiles,  372; 
4.  Skin  of  reptiles,  373;  5.  Posture,  locomotion,  and  skeleton,  373;  6.  Feeding 
and  digestion,  378;  7.  Respiration,  circulation,  and  excretion,  378;  8.  Reproduc- 
tion of  reptiles,  380;  9.  Nervous  system  and  receptors  of  reptiles,  383. 

XV.  EVOLUTION  OF  THE  REPTILES 

1.  The  earliest  reptile  populations,  Anapsida,  386;  2.  Classification  of  reptiles, 
391;  3.  Order  1.  Chelonia,  392;  4.  Subclass  *Synaptosauria,  399;  5.  Order 
*Ichthyopterygia,  401 ;  6.  Subclass  Lepidosauria,  401 ;  7.  Order  Rhynchocephalia, 
402;  8.  Order  Squamata,  404;  9.  Suborder  Lacertilia,  407;  10.  Suborder 
Ophidia,  411;  11.  Superorder  Archosauria,  416;  12.  Order  *Pseudosuchia,  417; 
13.  Order  *Phytosauria,  417;  14.  Order  Crocodilia,  418;  15.  The  'Terrible 
Lizards',  Dinosaurs,  421;  16.  Order  *Saurischia,  422;  17.  Order  *Ornithischia, 
424;  18.  Order  *Pterosauria,  426;  19.  Conclusions  from  study  of  evolution  of  the 
reptiles,  429. 

XVI.  LIFE  IN  THE  AIR:  THE  BIRDS 

1.  Features  of  bird  life,  431 ;  2.  Bird  numbers  and  variety,  431 ;  3.  The  skin  and 
feathers,  432;  4.  Colours  of  birds,  436;  5.  The  skeleton  of  the  bird.  Sacral  and 
sternal  girders,  437;  6.  The  sacral  girder  and  legs,  440;  7.  Skeleton  of  the  wings, 
447;  8.  Wing  muscles,  449;  9.  Principles  of  bird  flight,  450;  10.  Wing  shape, 
452;  1 1.  Wing  area  and  loading,  452;  12.  Aspect  ratio,  453;  13.  Wing  tips,  slots, 
and  camber,  453;  14.  Flapping  flight,  455;  15.  Soaring  flight,  458;  16.  Soaring 
on  up-currents,  458;  17.  Use  of  vertical  wind  variations,  460;  18.  Speed  of 
flight,  461;  19.  Take-off  and  landing,  462;  20.  The  skull  in  birds,  464;  21.  The 
jaws,  beak,  and  feeding  mechanisms,  464;  22.  Digestive  system  of  birds,  468; 
23.  Circulatory  system,  470;  24.  Respiration,  471;  25.  Excretory  system,  474; 
26.  Reproductive  system,  475;  27.  The  brain  of  birds,  477;  28.  Functioning  of  the 
brain  in  birds,  479;  29.  The  eyes  of  birds,  482;  30.  The  ear  of  birds,  488;  31. 
Other  receptors,  490. 

XVII.  BIRD  BEHAVIOUR 

I.  Habitat  selection,  491;  2.  Food  selection,  491;  3.  Recognition  and  social 
behaviour,  492;  4.  Bird  migration  and  homing,  493;  5.  The  stimulus  to  migra- 
tion, 495;  6.  The  breeding-habits  of  birds,  496;  7.  Courtship  and  display,  497; 
8.    Bird   territory,    503;    9.    Mutual   courtship,    504;    10.    Nest-building,    505; 

I I.  Shape  and  colour  of  the  eggs,  507;  12.  Brooding  and  care  of  the  young,  507. 

XVIII.  THE  ORIGIN  AND  EVOLUTION  OF  BIRDS 

1.  Classification,  509;  2.  Origin  of  the  birds,  510;  3.  Jurassic  birds  and  the 
origin   of  flight,   510;   4.   Cretaceous   birds.   Superorder  Odontognathae,   513; 


xiv  CONTENTS 

5.  Flightless  birds.  Superorder  Palaeognathae,  514;  6.  Penguins.  Superorder 
Impennae,  515;  7.  Modern  birds.  Superorder  Neognathae,  516;  8.  Tendencies 
in  the  evolution  of  birds,  522 ;  9.  Darwin's  finches,  524 ;  1  o.  Birds  on  other  oceanic 
islands,  530;  11.  The  development  of  variety  of  bird  life,  532. 

XIX.  THE  ORIGIN  OF  MAMMALS 

1.  Classification,  533;  2.  The  characteristics  of  mammals,  534;  3.  Mammals  of 
the  Mesozoic,  536;  4.  Mammal-like  reptiles,  Synapsida,  539;  5.  Order  *Pely- 
cosauria  (=  Theromorpha),  540;  6.  Order  *Therapsida,  541;  7.  Mammals  from 
the  Trias  to  the  Cretaceous,  545;  8.  Original  cusp-pattern  of  teeth  of  mammals, 
548;  9.  Egg-laying  mammals.  Subclass  Prototheria  (Monotremata),  549. 

XX.  MARSUPIALS 

1.  Marsupial  characteristics,  557;  2.  Classification  of  marsupials,  562;  3.  Opos- 
sums, 563;  4.  Carnivorous  marsupials,  565;  5.  Marsupial  ant-eaters  and  other 
types,  566;  6.  Phalangers,  wallabies,  and  kangaroos,  566;  7.  Significance  of 
marsupial  isolation,  568. 

XXI.  EVOLUTION  OF  PLACENTAL  MAMMALS  AND  ITS  RELATION 
TO  THE  CLIMATIC  AND  GEOGRAPHICAL  HISTORY  OF  THE 
CENOZOIC 

1.  Eutherians  at  the  end  of  the  Mesozoic,  569;  2.  The  end  of  the  Mesozoic,  569; 
3.  Divisions  and  climates  of  the  Tertiary  Period,  571;  4.  Geographical  regions, 
572;  5.  The  earliest  eutherians,  574;  6.  Definition  of  a  eutherian  (placental)  mam- 
mal) 575;  7-  Evolutionary  trends  of  eutherians,  575;  8.  Conservative  eutherians, 
577;  9.  Divisions  and  classification  of  Eutheria,  577. 

XXII.  INSECTIVORES,  BATS,  AND  EDENTATES 

1.  Order  1.  Insectivora,  581;  2.  Order  Chiroptera.  Bats,  585;  3.  Order  Dermo- 
ptera,  592;  4.  Order  Edentata,  592;  5.  Armadillos,  595;  6.  Ant-eaters  and  sloths, 
597;  7.  Order  Pholidota:  pangolins,  601. 

XXIII.  PRIMATES 

1.  Classification,  602;  2.  Characters  of  primates,  603;  3.  Divisions  of  the  pri- 
mates, 607;  4.  Lemurs  and  lorises,  609;  5.  Fossil  Prosimians,  613;  6.  Tarsiers, 
614;  7.  Characteristics  of  Anthropoidea,  617;  8.  New  World  monkeys,  Ceboidea, 
620. 

XXIV.  MONKEYS,  APES,  AND  MEN 

1.  Common  origin  of  Old  World  monkeys,  apes,  and  men,  623;  2.  Old  World 
monkeys,  Cercopithecoidea,  623;  3.  The  great  apes:  Pongidae,  626;  4.  The 
ancestry  of  man,  633;  5.  Brain  of  apes  and  man,  633;  6.  The  posture  and  gait  of 
man,  634;  7.  The  limbs  of  man,  635;  8.  The  skull  and  jaws  of  man,  637;  9.  Rate 
of  development  of  man,  640 ;  10.  Growth  of  human  populations,  641 ;  1 1 .  Time  of 
development  of  the  Hominidae,  641;  12.  The  Australopithecinae,  643;  13.  Early 
Hominids,  *Pithecanthropus,  645;  14.  Man,  646;  15.  Human  cultures,  648. 

XXV.  RODENTS  AND  RABBITS 

1.  Characteristics  of  rodent  life,  652;  2.  Classification,  653;  3.  Order  Rodentia, 
654;  4.  Order  Lagomorpha,  660;  5.  Fluctuations  in  numbers  of  mammals,  663. 


CONTENTS  xv 

XXVI.  WHALES,  666. 

XXVII.  CARNIVORES 

i.  Affinities  of  carnivores  and  ungulates:  Cohort  Ferungulata,  677;  2.  Classifica- 
tion, 679;  3.  Order  Carnivora,  680;  4.  The  Cats,  680;  5.  *Suborder  Creodonta, 
683;  6.  Suborder  Fissipeda,  684;  7.  Suborder  Pinnepedia,  691. 

XXVIII.  PROTOUNGULATES 

1.  Origin  of  the  ungulates,  694;  2.  Ungulate  characters,  695;  3.  Classification,  699; 

4.  Superorder  Protoungulata,  700;  5.  South  American  ungulates.  *Order  Notoun- 
gulata,  701;  6.  *Order  Litopterna,  703;  7.  *Order  Astrapotheria,  703;  8.  Order 
Tubulidentata,  704. 

XXIX.  ELEPHANTS  AND  RELATED  FORMS 

1.  'Near-ungulates',  superorder  Paenungulata,  706;  2.  Classification,  706; 
3.  Order  Hyracoidea,  707;  4.  Elephants.  Order  Proboscidea,  709;  5.  *Order 
Pantodonta  (Amblypoda),  717;  6.  *Order  Dinocerata,  718;  7.  *Order  Pyro- 
theria,  718;  8.  *Order  Embrithopoda,  718;  9.  Order  Sirenia,  720. 

XXX.  PERISSODACTYLS 

1.  Perissodactyl  characteristics,  722;  2.  Classification,  723;  3.  Perissodactyl 
radiation,    724;    4.    Suborder    Ceratomorpha,    tapirs    and    rhinoceroses,    727; 

5.  Rhinoceroses,  728;  6.  *Brontotheres  (*Titanotheres),  730;  7.  *Chalicotheres 
(=  *Ancylopoda),  731;  8.  Palaeotheres,  732;  9.  Horses,  732;  10.  Allometry  in 
the  evolution  of  horses,  737;  11.  Rate  of  evolution  of  horses,  738;  12.  Conclu- 
sions from  the  study  of  the  evolution  of  horses,  739. 

XXXI.  ARTIODACTYLS 

1.  Characteristics  of  artiodactyls,  741;  2.  Classification,  745;  3.  The  evolution 
of  artiodactyls,  746;  4.  Pigs  and  hippopotamuses,  748;  5.  *Oreodonts,  750; 

6.  Camels,  751;  7.  Ruminants,  753;  8.  Chevrotains,  754;  9.  Pecora,  755; 
10.  Cervidae,  755;  II.  Giraffidae,  757;  12.  Antilocapridae  and  Bovidae,  760. 

XXXII.  CONCLUSION.  EVOLUTIONARY  CHANGES  OF  THE  LIFE  OF 
VERTEBRATES 

1.  The  life  of  the  earliest  chordates,  765;  2.  Comparison  of  the  life  of  early 
chordates  with  that  of  mammals,  767;  3.  The  increasing  complexity  and  variety 
of  vertebrates,  768;  4.  The  variety  of  evidence  of  evolutionary  change,  769; 
5.  Rate  of  evolutionary  change,  770;  6.  Vertebrates  that  have  evolved  slowly, 
771;  7.  Varying  rates  of  evolutionary  changes,  774;  8.  Vertebrates  that  have 
disappeared,  774;  9.  Successive  replacement  among  aquatic  vertebrates,  775; 
10.  Successive  replacement  among  land  vertebrates,  776;  11.  Is  successive  re- 
placement due  to  climatic  change?,  776;  12.  Convergent  and  parallel  evolution, 
777'.  !3-  Some  tendencies  in  vertebrate  evolution,  779;  14.  Evolution  of  the 
whole  organization,  780;  15.  Summary  of  evidence  about  evolution  of  verte- 
brates, 781;  16.  Conservative  and  radical  influences  in  evolution,  783;  17.  The 
direction  of  evolutionary  change,  784;  18.  The  influences  controlling  evolutionary 
progress,  785. 

REFERENCES  787 

INDEX  797 


THE  LIFE  OF 

VERTEBRATES 


I 

EVOLUTION  OF  LIFE  IN  RELATION  TO  CLIMATIC 
AND  GEOLOGICAL  CHANGE 

1 .  The  need  for  generality  in  zoology 

The  aim  of  any  zoological  study  is  to  know  about  the  life  of  the  ani- 
mals concerned.  Our  object  in  this  book  is,  therefore,  to  help  the 
reader  to  learn  as  much  as  possible  about  all  the  vertebrate  animal  life 
that  has  ever  been.  Thinking  of  the  great  numbers  of  types  that  have 
existed  since  the  first  fishes  swam  in  the  Palaeozoic  seas,  one  might 
well  be  appalled  by  such  a  task:  to  describe  all  these  populations  in 
detail  would  indeed  demand  a  huge  treatise.  However,  in  a  well- 
developed  science  it  should  be  possible  to  reduce  the  varied  subject- 
matter  to  order,  to  show  that  all  differences  can  be  understood  to  have 
arisen  by  the  influence  of  specified  factors  operating  to  modify  an 
original  scheme.  Animal  and  plant  life  is  so  varied  that  it  has  not  yet 
proved  possible  to  systematize  our  knowledge  of  it  as  thoroughly  as 
we  should  wish.  Thinking,  again,  of  the  variety  of  vertebrate  lives, 
it  may  seem  impossible  to  imagine  any  general  scheme  and  simple  set 
of  factors  that  would  include  so  many  special  circumstances.  Yet 
nothing  less  should  be  the  aim  of  a  true  science  of  zoology.  Too  often 
in  the  past  we  have  been  content  to  accumulate  unrelated  facts.  It  is 
splendid  to  be  aware  of  many  details,  but  only  by  the  synthesis  of 
these  can  we  obtain  either  adequate  means  for  handling  so  many 
data  or  knowledge  of  the  natures  we  are  studying.  In  order  to  know 
life — what  it  is,  what  it  has  been,  and  what  it  will  be — we  must 
look  beyond  the  details  of  individual  lives  and  try  to  find  rules  govern- 
ing all.  Perhaps  we  may  find  the  task  less  difficult  than  expected. 
Even  an  elementary  anatomical  and  physiological  study  shows  that 
all  vertebrates  are  built  upon  a  common  plan  and  have  certain  simi- 
larities of  behaviour.  Our  object  will  be  to  come  to  know  the  nature 
of  this  plan  of  life,  of  structure,  and  action,  to  show  how  it  is  modified 
in  special  cases  and  how  each  special  case  is  also  an  example  of  a 
general  type  of  modification. 

Since  the  problem  arises  from  the  variety  of  animals  that  have 
lived  and  live  today,  our  central  task  is  obviously  to  inquire  into  the 
reason  for  the  existence  of  so  much  difference.  If  vertebrate  life  began 
as  one  single  fish-like  type,  why  has  it  not  continued  as  such  until 
now?  Why,  instead  of  numerous  identical  fishes,  are  there  countless 


2  EVOLUTION   OF   LIFE  i.  i- 

different  kinds,  while  descendants  of  most  unfish-like  form  are  found 
living  out  of  the  water  and  even  in  the  air  and  under  the  ground  ? 

To  put  it  in  a  way  more  familiar,  though  perhaps  less  clear:  what 
are  the  forces  that  have  produced  the  changes  of  animal  form  ?  Know- 
ing these  forces,  and  the  original  type,  it  would  be  possible  to  con- 
struct a  truly  general  science  of  zoology,  with  sure  premisses  and 
deductions.  Even  if  we  cannot  reach  this  end,  we  should  at  least  try, 
hoping  that  after  investigation  of  the  biology  of  vertebrates  it  will  be 
possible  to  retain  something  more  than  a  mass  of  detailed  information. 
At  the  end  of  such  a  study,  if  we  deal  with  the  subject  right,  we  should 
surely  be  better  able  to  answer  some  of  the  fundamental  biological 
questions.  We  should  be  able  to  say  something  about  the  nature  of 
evolution  and  of  the  differences  between  types,  to  know  whether  there 
have  been  rhythms  of  change  at  work  to  produce  these  differences, 
and  also — the  acid  test  of  any  true  science — to  forecast  how  these 
changes  are  likely  to  proceed  in  the  future. 

2.  What  do  we  mean  by  the  life  of  an  animal? 

In  biology  we  make  much  use  of  analogies,  attempting  to  grasp  the 
nature  of  the  processes  at  work  by  comparison  with  man-made 
machines.  We  have  a  science  of  anatomy,  which  we  are  told  is  con- 
cerned with  the  'structure'  of  animals,  and  we  feel  that  we  understand 
what  'structure'  means.  Physiology  is  the  study  of  'function',  and 
this,  too,  we  seem  to  understand.  We  take  the  analogies  from  our 
machines,  which  have  what  we  call  'structure'  and  'function'.  How- 
ever, the  difficulty  at  once  arises  that  the  living  things  make  and  control 
themselves.  The  whole  scheme  fails  us  when  we  ask  what  is  it,  then, 
that  we  call  the  'life'  of  the  animal,  and  what  is  it  that  is  passed  on 
from  generation  to  generation,  and  that  changes  through  the  ages  by 
the  process  we  call  evolution  ?  It  has  gradually  become  apparent  that 
the  body  is  not  a  fixed,  definite  'structure'  as  it  appears  to  casual 
observation  or  when  dissected.  In  life  there  is  ceaseless  activity  and 
change  going  on  within  the  apparently  constant  framework  of  the  body. 
The  movement  of  the  blood  is  one  sign  of  this  activity,  and  since 
Harvey's  discovery  of  the  circulation  ( 1 628)  we  have  learnt  of  innumer- 
able others.  Everyone  knows  that  the  skin  is  continually  being  renewed 
by  growth  from  below,  and  many  other  types  of  cell  are  similarly 
replaced;  for  instance,  red  blood-cells  last  only  for  a  few  weeks  in 
man.  Even  in  the  cells  that  are  not  completely  destroyed  and  replaced, 
such  as  the  nerve-cells,  there  is  continual  change  of  the  molecules  that 
make  up  their  substance.  The  full  extent  of  this  exchange  has  been 


i.3  DEFINITION  OF  LIFE  3 

shown  by  using  isotopes  to  discover  for  how  long  individual  atoms 
remain  in  the  body;  the  work  of  Schoenheimer  (1942),  which  by  this 
means  first  clearly  established  the  rapidity  of  the  turnover,  is  a  classic 
of  modern  biology. 

There  are  no  man-made  machines  that  replace  themselves  in  this 
way,  but  in  recent  years  there  has  been  much  study  of  machines  that 
control  their  own  operations.  Such  work  provides  us  with  new  analo- 
gies and  new  mathematical  techniques  with  which  we  can  analyse 
the  control  of  living  systems  (see  Yockey  and  Quastler,  1958).  As  yet 
we  have  no  means  of  grasping  the  enormously  complicated  network 
of  activities  that  constitutes  a  single  life.  Throughout  this  book,  how- 
ever, an  attempt  will  be  made  to  approach  that  end  by  use  of  certain 
clues  to  help  us  to  concentrate  on  significant  features,  to  see  the 
rhythms  or  patterns  common  to  the  lives  of  the  animals,  and  thus  to 
carry  in  mind  many  details.  It  is  possible  in  this  way  to  bring  together 
information  collected  by  morphologists,  geneticists,  embryologists, 
physiologists,  biophysicists,  and  biochemists  to  give  a  single  view  of 
the  life  of  the  organisms  concerned.  The  task  is  admittedly  a  hard  one 
and  the  success  achieved  only  partial.  Continually  one  slips  into  the 
discussion  of  particular  structures,  substances,  or  processes,  forgetting 
the  whole  life.  A  detail  of  form  or  of  chemical  composition  attracts, 
and  thus  distracts,  attention;  perhaps  it  can  hardly  be  otherwise  if  we 
are  to  describe  exactly.  But  it  is  surprising  how  practice  improves  the 
powers  of  selecting  and  emphasizing  those  patterns  or  details  of 
knowledge  that  are  significant  for  the  study  of  each  life  as  a  whole. 

The  first  difficulty  is  to  force  oneself  to  remember  all  the  time  that 
a  living  animal  or  plant  system  is  in  a  continual  state  of  change.  When 
making  any  observations,  whether  by  dissection  or  with  the  micro- 
scope, with  a  test-tube,  microelectrode,  or  respirometer,  it  is  necessary 
continually  to  think  back  to  the  time  when  the  tissue  was  active  in  the 
living  body,  and  to  frame  the  observation  so  that  it  shall  reveal  some- 
thing significant  of  that  activity.  This  means  that  every  biologist 
must  know  as  much  as  possible  of  the  life  of  the  whole  organism  with 
which  he  deals ;  indeed,  something  of  the  whole  population  from  which 
the  specimen  was  drawn. 

3.  Living  things  tend  to  preserve  themselves 

The  clue  by  which  we  recognize  significant  features  during  any 
biological  study  is  that  living  activity  tends  to  ensure  the  continuance 
of  its  own  pattern.  The  processes  of  life  draw  materials  into  the 
system,  organize  them  there,  and  then  send  them  out  again,  all  in  such 


4  EVOLUTION  OF  LIFE  1.3- 

a  way  that  the  arrangement  or  pattern  of  the  processes  remains  almost 
unchanged  as  the  molecules  pass  through  it.  We  see  analogies  in  the 
way  that  a  waterfall  or  a  human  institution  such  as  the  Catholic 
Church  remains  the  same,  though  its  components  change.  Our 
business  is  to  try  to  describe  this  arrangement  or  pattern  of  processes 
that  is  preserved.  It  is  this  pattern  that  we  call  the  life  of  the  species. 
The  activities  that  go  to  make  up  one  sort  of  life  are  not  necessarily 
all  to  be  found  in  any  one  individual,  still  less  in  any  part  of  an  in- 
dividual. The  pattern  is  not  to  be  seen  in  any  single  creature  or 
part.  Though  we  speak  of  'individuals'  they  are  no  more  the  final 
units  than  are  the  cells,  the  heart,  or  the  brain,  the  bones,  hair,  or 
nails.  A  whole  interbreeding  population  is  the  unit  of  life  that  tends 
to  preserve  the  type,  assisted,  in  social  species,  by  individuals  that 
play  a  part  in  the  life  without  participation  in  reproduction,  such  as 
worker-bees. 

A  wide  range  of  activities,  therefore,  goes  to  make  up  any  one  type 
of  life,  and  we  shall  only  appreciate  these  activities  properly  if  we  study 
that  whole  life  as  it  is  normally  lived  in  its  proper  environment.  The 
way  to  study  animals  or  men  is,  first  and  foremost,  to  examine  them 
whole,  to  see  how  their  actions  serve  to  meet  the  conditions  of  the 
environment  and  to  allow  preservation  of  the  life  of  the  individual  and 
the  race.  Then,  with  this  knowledge  of  how  the  animal  'uses'  its  parts 
we  may  be  able  to  make  more  detailed  studies,  down  to  the  molecular 
level,  and  show  how  together  the  activities  form  a  single  scheme  of 
action. 

A  living  animal  is  continually  doing  things.  Even  when  it  is  asleep 
it  is  breathing,  its  heart  beating  and  brain  pulsing,  while  countless 
chemical  changes  go  on  throughout  its  tissues.  The  waking  life,  of 
course,  shows  this  restless  action  even  more  clearly.  Animals  may 
indeed  sometimes  be  still,  but  they  are  never  wholly  inactive.  It  is  not 
difficult  to  see  startling  glimpses  of  this  activity  if  we  watch  animals 
alive,  especially  when  they  are  in  groups.  A  hawk  wheeling,  a  pond 
full  of  tadpoles,  or  a  crowd  of  people  moving  on  a  city  street  will 
remind  us  that  if  we  are  to  see  the  interesting  side  of  life  we  have  to 
study  activity  and  not,  as  is  more  easy  to  do  and  so  often  done,  to 
spend  all  our  time  examining  the  'structure'  or  'chemistry'  of  the  dead. 

The  peculiarity  of  this  activity  of  animals  is  that  much,  perhaps 
most,  of  it  has  the  effect  of  maintaining  the  integrity  of  the  body  and, 
indeed,  even  of  increasing  the  bulk,  or  of  reproducing  more  bodies 
like  the  first  (homeostasis).  The  search  for  food  provides  raw  materials 
giving  to  the  muscles  energy  for  further  search.   If  the  situation 


i.4  ACTIVITIES  OF  LIVING  THINGS  5 

demands  still  greater  efforts  these  efforts  will  themselves  lead  to 
'hypertrophy',  or  increase  in  the  muscle  substance  and  power.  Simi- 
larly, the  muscular  movements  of  respiration  provide  the  oxygen  by 
which  these  same  movements  and  others  are  made  possible. 

We  could  go  on  indefinitely  describing  how  the  activity  of  each  part 
of  the  body  tends,  with  some  exceptions,  to  ensure  the  continuation 
of  the  whole.  The  mere  statement  of  the  existence  of  this  tendency  to 
self-maintenance  does  not,  perhaps,  sufficiently  emphasize  the  power 
that  it  represents.  It  is  one  of  the  great  'forces'  that  control  the 
matter  of  the  earth.  It  causes  huge  masses  of  material  to  be  moved 
annually  to  the  tops  of  high  trees  and  millions  of  wonderfully  built 
animals  to  roam  daily  to  find  and  consume  uncounted  tons  of  food 
or,  not  finding  it,  to  search  on  and  maintain  their  activity  while  any 
calorie  remains  available.  The  power  of  life  is  sufficient  to  bring  about 
the  incorporation  of  an  appreciable  part  of  the  matter  of  the  earth's 
surface  into  living  things.  Within  the  appropriate  range  of  conditions, 
found  chiefly  near  the  surface  of  the  sea  and  on  the  damper  parts  of 
the  earth,  life  dominates  the  lifeless  and  provides  a  main  influence  on 
the  matter  present. 

Animals  and  plants  are  able  to  take  these  actions  that  tend  to  their 
own  preservation  because  they  contain  stores  of  information  about 
the  conditions  that  are  likely  to  be  met  with  and  the  means  by  which 
adverse  changes  may  be  prevented.  A  fish  is  born  with  a  body  so 
shaped  that  it  may  swim,  a  gull  can  soar  on  air  currents,  and  a  monkey 
leap  from  branch  to  branch.  Every  type  may  thus  be  said  to  represent 
the  environment  in  which  it  lives,  that  is  to  say,  it  has  a  hereditary 
store  of  information  about  it.  Moreover,  this  hereditary  store  provides 
it  with  receptor  organs  and  brain  with  which  it  can  acquire  further 
information  during  its  lifetime.  The  study  by  engineers  of  the  means 
by  which  information  may  be  coded,  transmitted,  and  stored  has 
provided  biologists  with  further  means  for  study  of  the  living  memory 
stores,  which  are  comparable  in  some  ways  with  those  of  machines. 

4.  What  do  we  mean  by  awareness  of  life  ? 

A  man  states  that  he  is  aware  that  he  is  alive.  He  says  that  he  knows 
his  needs  and  that  he  feels  satisfaction  when  they  are  fulfilled.  One 
of  the  most  difficult  problems  of  biology  is  to  decide  how  to  relate 
such  statements  about  'subjective  experience'  to  what  may  be  called 
the  'objective'  descriptions  of  science.  This  is  clearly  a  philosophical 
problem  too  large  and  important  to  be  discussed  properly  here  but 
it  must  be  approached.  Perhaps  it  begins  to  find  a  solution  when  we 


6  EVOLUTION  OF  LIFE  1.4- 

remember  that  in  speaking  of  all  these  matters  we  are  using  the  words 
of  a  conventional  code,  trying  with  them  to  convey  information  to 
our  fellows  or  somehow  to  influence  them.  Then  we  shall  stop 
asking  such  questions  as  'what  is  consciousness  ?'  substituting  'what 
sort  of  information  does  he  transmit  when  he  says  "I  am  conscious"  ?' 

This  will  help  with  the  particular  aspect  of  the  problem  that  con- 
cerns us  here.  In  trying  to  define  what  we  mean  by  the  'life'  of  an 
animal  should  we  assume  that,  in  addition  to  the  actions  of  its  body, 
which  we  describe,  there  are  also  actions  of  some  other  entity,  its 
'mind'  ?  It  is  true  that  we  should  feel  that  any  description  of  our  own 
lives  that  left  out  'awareness'  was  ludicrously  incomplete.  Since  we 
have  evolved  from  animals,  so  the  argument  runs,  why  should  we 
deny  that  they  have  some  form  of  'consciousness'  ?  This  seems  logical 
but  overlooks  that  the  essential  feature  of  statements  such  as  T  am 
aware  that  I  am  alive'  or  T  feel  pain'  is  that  they  are  part  of  the 
means  by  which  man,  the  communicating  animal,  controls  and 
influences  his  environment.  Statements  are  part  of  human  life,  just 
as  swinging  from  branches  is  a  feature  of  the  life  of  monkeys  and 
flying  of  birds.  It  will  at  once  be  objected  that  these  animals  also 
communicate,  but  the  point  is  that  communication  must  be  considered 
as  a  part  of  the  life  system  of  each  animal,  like  respiration,  locomotion, 
or  reproduction. 

This  leaves  us  with  the  baffling  problem  of  finding  words  with 
which  to  describe  the  describing  system  itself.  Where  indeed  can  we 
find  a  sure  basis  from  which  to  start?  Here,  I  think,  we  can  only 
proceed  by  humbly  admitting  both  ignorance  and  inadequacy.  In 
our  language  we  have  a  communication  system  with  which  we  can 
convey  to  each  other  incomparably  more  information  than  passes 
between  other  animals.  Our  system  is  improving  every  year,  but  it  is 
still  grossly  inadequate  to  describe  the  more  subtle  features  of  the 
world,  and  especially  of  living  things.  We  may  show  the  greatest 
respect  for  the  depth  of  these  mysteries  by  recognizing  that  they  are 
still  too  great  for  us  to  describe  in  our  simple  language.  To  provide  a 
good  description  of  all  the  marvellous  features  of  the  life  of  a  man  or 
an  animal  requires  a  complicated  and  subtle  terminology,  for  which 
we  are  striving.  In  pre-scientific  language  all  such  problems  are 
simplified  by  supposing  that  the  actions  of  any  system  are  produced 
by  some  agent  rather  like  a  human  being  that  resides  within  it.  Thus 
a  child  says  that  the  clouds  move  'because  they  want  to'.  So  we  are 
accustomed  to  say  that  the  body  moves  because  it  is  guided  by  'the 
mind'.   This  may  indeed  be  the  best  way  of  speaking  for  some 


i.5  INFLUENCE  OF  ENVIRONMENT  7 

occasions,  with  our  imperfect  language,  but  it  is  a  feeble  descriptive 
technique.  I  do  not  believe  that  it  is  satisfactory  for  biology  and 
especially  not  for  zoology.  By  the  life  of  an  animal  we  mean  all  those 
activities  that  make  a  certain  pattern  and  serve  to  maintain  that 
pattern.  In  so  far  as  we  can  describe  this  as  a  whole  it  is  by  comparing 
it  with  other  self-maintaining  systems  and  particularly  with  those 
self-controlling  machines  that  we  have  made  for  ourselves.  Biology 
today  has  a  great  opportunity  to  explore  the  means  by  which  animals 
remain  alive,  using  many  sorts  of  descriptive  technique,  chemical, 
electrical  and,  not  least,  the  means  by  which  mathematicians  and 
engineers  describe  whole  complicated  self-maintaining  systems.  It 
is  in  such  language  that  a  fuller  and  richer  account  of  living  things 
can  be  given.  It  is  curious  that  objections  to  the  use  of  scientific 
terminology  often  claim  that  it  somehow  'reduces'  or  'restricts'  our 
view  of  life.  Exactly  the  reverse  is  the  case.  Explaining  human  or 
animal  life  in  terms  of  'spirits',  good  or  bad,  is  only  describing  them 
by  comparison  with  themselves.  Scientific  description  allows  us  to 
break  out  of  our  narrow  prison  and  to  show  how  each  of  the  many 
aspects  of  life  can  be  measured  and  compared  with  the  forces  that  can 
be  detected  throughout  the  universe. 

5.  The  influence  of  environment  on  life 

Growth  is  the  addition  of  material  to  that  which  is  already  organized 
into  a  living  pattern.  But  the  pattern  is  not  fixed  and  invariate,  even 
throughout  any  one  life.  Each  individual  changes  through  its  lifetime, 
develops,  as  we  say,  and  moreover  is  modified  by  the  action  upon  it 
of  its  surroundings.  Those  parts  that  are  exercised  by  the  interaction 
of  the  animal's  tendencies  and  the  surrounding  circumstances  increase 
in  amount  (hypertrophy),  while  any  disused  parts  undergo  atrophy  or 
reduction.  The  pattern  is  thus  able  to  conform  to  a  considerable 
extent  to  the  exigencies  of  change  in  the  external  world.  It  could  be 
imagined  that  a  sufficiently  plastic  animal  organization  would  be  able 
in  this  way,  if  its  tendencies  to  survival  were  strong  enough,  to  mould 
itself  to  all  the  changes  of  climate  through  the  millennia,  so  that  a 
great  variety  of  animal  tvpes  would  arise  by  use  and  disuse  alone. 
Only  a  limited  degree  of  change  is  possible  in  this  way,  however,  and 
it  is  not  such  changes  either  of  development  or  by  the  direct  influence 
of  environment  that  we  call  'evolution'.  There  is  abundant  evidence 
that  the  result  of  such  interaction  between  organism  and  environment 
is  not  handed  on  in  the  genetic  code.  Acquired  characters  are  not 
inherited. 


8  EVOLUTION  OF  LIFE  1.6- 

6.  What  is  it  that  heredity  transmit? 

What  is  passed  on  is  a  coded  pattern  or  plan  controlling  the 
organization  of  the  life  processes  of  the  next  generation.  The  plan 
takes  the  physical  form  of  a  series  of  molecules  of  deoxyribose 
nucleotides  (DNA)  in  the  chromosomes.  These  by  the  specific 
arrangements  of  the  four  types  of  base  that  they  contain  somehow 
organize  the  proper  linear  sequences  of  the  twenty  or  so  amino-acids 
that  make  up  the  proteins  of  each  species.  By  the  emergence  at  the 
proper  time  during  development  of  the  appropriate  proteins,  enzyme 
systems  are  produced  that  ensure  the  development  and  functioning  of 
the  embryo  and  later  the  adult.  We  cannot  fully  understand  how  all 
these  processes  are  regulated  but  we  see  in  outline  how  it  all  follows 
if  the  DNA  molecules  provide  a  code  from  which  natural  selection 
has  chosen  in  the  past  those  items  that  are  suitable  to  provide  viable 
organisms  for  a  particular  environment. 

The  organization  of  life  is  very  rarely  identical  in  any  two  indi- 
viduals; there  is,  therefore,  a  considerable  range  of  potential  patterns 
resident  in  all  those  animals  of  a  population  that  are  capable  of  mating 
together.  The  sum  of  those  variants  of  the  hereditary  materials  con- 
stitutes the  pattern  or  mould,  as  it  were,  of  the  life  of  the  whole  species. 
Evolution  consists  in  a  change  in  this  hereditary  genotype,  producing, 
of  course,  a  new  set  of  adults.  The  genotype  probably  rarely  stays  for 
long  quite  the  same.  Even  in  species  that  do  not  seem  to  be  changing 
rapidly  there  are  continual  adjustments,  for  example  in  the  power  to 
produce  antibodies  or  to  manufacture  enzymes.  Evolution,  proceeding 
by  mutation,  recombination,  and  selection,  is  not  some  remote  or 
rare  thing  occurring  only  sporadically.  It  is  a  'physiological'  process  as 
much  as  is  a  change  in  respiration  rate  or  in  number  of  red  cells,  but 
it  has  a  longer  time  course  than  these.  Evolution  is  the  process  by 
which  the  whole  population  adjusts  its  control  system  to  meet  chang- 
ing needs.  Over  long  periods  of  years  these  adjustments  produce  the 
new  forms  of  life  that  appear  as,  say,  the  first  fishes,  or  land  animals 
or  mammals.  Our  aim  is  to  try  to  discover  the  conditions  under 
which  each  new  main  group  of  vertebrates  arose  and  so  to  understand 
the  processes  that  have  been  at  work,  modifying  the  basic  organization. 

We  must  therefore  direct  our  studies  continually  to  populations, 
rather  than  to  single  individuals,  thinking  of  all  the  creatures  of  a 
kind,  spread  out  wherever  a  suitable  habitat  for  them  occurs.  They 
will  not  all  be  alike  genetically,  and  the  circumstances  of  the  lives  of 
some  members  of  the  group  may  become  sufficiently  dissimilar  to 


i.8  INCREASING  COMPLEXITY  OF  LIFE  9 

produce  further  divergences  by  use  and  disuse.  Limitations  of  inter- 
mating  may  occur  on  account  of  limitation  of  movement,  accentuated 
by  partial  and,  perhaps,  eventually  complete  geographical  barriers. 
Such  variations  in  external  circumstance  become  matched  by  diver- 
gences in  type,  until  two  new  races  are  produced,  at  first  relatively 
and  then  absolutely  infertile,  so  that  there  are  then  two  separate 
populations  or  species  instead  of  one. 

7.  The  increasing  complexity  of  life 

The  acquisition  of  new  matter,  and  hence  growth  and  reproduction, 
occurred  in  the  earliest  animals  by  relatively  simple  means,  as  it  still 
does  today  in  the  bacteria,  lower  plants,  and  some  protozoa.  It  is  not 
easy  to  provide  rigid  criteria  for  the  definition  of  'simple';  perhaps 
some  of  the  chemical  changes  involved  may  be  quite  complex,  but  the 
whole  system  can,  with  meaning,  be  said  to  be  simple.  The  number 
of  parts  that  it  contains  is  relatively  small  and  the  number  of  'adap- 
tive' actions  that  it  can  take  is  limited.  A  population  of  bacteria  in  a 
suitable  culture  medium  obtains  its  raw  materials  by  diffusion;  the 
chief  device  that  it  uses  to  secure  these  materials  is  to  provide  a  large 
number  of  spores,  so  that  some  may  come  to  rest  in  suitable  sur- 
roundings. Such  a  life  can  be  said  to  be  more  simple  than  that  of  a 
vertebrate,  whose  system  includes  many  special  devices  for  obtaining 
access  to  the  raw  materials  that  it  needs.  We  can  say  that  a  species  of 
bacteria  transmits  less  information  than  a  vertebrate.  LInfortunately 
there  are  no  satisfactory  counts  of  the  number  of  genes  available;  the 
amount  of  DNA  in  bacteria  is  said  to  be  about  0-05  mgm  per  gm 
and  in  rat  liver  2  mgm  per  gm.  Bacteria  of  any  one  species  are  able  to 
alter  their  enzymes  to  suit  the  substrates  available,  but  their  life  does 
not  depend  upon  the  differentiation  into  numerous  cell  types  each 
with  its  special  functions.  The  variety  of  information  available  in  the 
'higher'  genotypes  enables  them  to  take  actions  that  ensure  survival 
under  conditions  where  the  'lower'  organisms  would  die.  Of  course, 
each  type  has  its  own  special  'niche'  and  the  comparison  of  higher  and 
lower  is  only  possible  if  we  can  show  exact  quantitative  differences. 

8.  The  progression  of  life  from  the  water  to  more  difficult  environ- 
ments 

In  general,  the  new  environments  colonized  have  involved  ever 
wider  departures  from  that  watery  one  in  which  life  first  arose.  This 
is  shown  most  strikingly  if  we  contrast  the  simple  way  in  which  the 
means  of  life  are  obtained  by  a  marine  bacterium  with  the  complicated 


io  EVOLUTION  OF  LIFE  in- 

activities that  go  to  maintain  a  man  alive  in  a  city.  Yet  all  living 
systems,  even  those  that  have  changed  most  markedly  since  their  first 
origin,  are  still  watery,  and  must  have  salt  and  nitrogenous  com- 
pounds with  which  to  make  proteins  and  so  on.  Perhaps,  indeed,  the 
basic  plan  of  the  living  activity  differs  less  in  the  various  types  than 
one  might  suppose.  'Protoplasm'  is  certainly  not  identical  in  all 
creatures,  but  it  may  be  that  it  differs  less  than  do  the  outward  forms 
that  support  it. 

In  order  to  provide  the  conditions  necessary  for  the  maintenance  of 
such  a  watery  system,  in  very  different  environments,  many  auxiliary 
activities  have  been  developed.  It  is  these  that  give  added  complexity 
to  the  higher  animals  and  plants,  enabling  them  to  undertake  what 
can  be  called  more  difficult  ways  of  life.  In  order  to  do  this  their 
activity  must  also  be  physically  greater  than  is  necessary  in  more 
lowly  types.  It  may  be  presumed  that  more  energy  is  transferred  to 
maintain  a  given  mass  of  living  matter  in  the  less  'easy'  environments, 
and  in  this  sense  the  higher  animals  are  less  efficient  than  the  lower, 
by  a  very  crude  criterion  of  efficiency. 

According  to  this  conception,  then,  evolution  has  involved  a  change 
in  the  relationship  between  organism  and  environment.  Life  has 
come  to  occupy  places  in  which  it  did  not  exist  before.  Perhaps  the 
total  mass  of  living  matter  has  thus  been  greatly  increased.  It  must 
not,  of  course,  be  supposed  that  every  evolutionary  change  has  pro- 
duced an  increase  in  complexity  in  this  way;  examples  of  'degenera- 
tion' are  too  well  known  to  need  quoting.  We  have,  however,  a  clear 
impression  that  through  the  years  there  has  been,  in  general,  some 
change  in  animals  and  plants  and  that  in  a  sense  some  of  the  later 
organisms  are  'higher'  than  the  earlier.  It  is  hardly  possible  to  deny 
that  there  is  some  meaning  in  the  assertion  that  man  is  a  higher 
animal  than  amoeba.  Our  thesis  attempts  to  specify  more  clearly  what 
we  can  know  about  this  evolutionary  change,  by  saying  that  it  con- 
sists of  a  colonization  by  life  of  environments  more  and  more  different 
from  that  in  which  life  arose.  This  colonization  was  made  possible 
by  the  gradual  acquisition  of  a  store  of  instructions  enabling  adjust- 
ments to  be  made  by  which  life  could  be  maintained  in  conditions  not 
tolerable  before. 

It  is  not  easy  to  enumerate  the  complexity  of  any  animal  or  to 
define  quantitatively  the  nature  of  its  relations  with  its  environment, 
and  for  this  reason  it  is  difficult  to  prove  our  thesis  rigorously.  This 
book  nevertheless  makes  an  attempt  to  show  how  the  organization  of 
vertebrate  life  has  become  more  complex  since  it  first  appeared,  and 


1.9  INVASION  OF  NEW  ENVIRONMENTS  n 

that  the  increasing  complexity  is  related  to  the  adoption  of  modes  of 
life  continually  more  remote  from  the  simple  diffusion  of  substances 
from  the  sea.  Of  course,  even  the  earliest  vertebrates  had  already 
departed  a  long  way  from  the  first  conditions  of  life  and  were  quite 
complex  organisms.  However,  in  the  history  of  their  life  through 
nearly  500  million  years  since  the  Ordovician  period  we  can  trace  con- 
siderable further  changes  in  complexity.  During  this  time  vertebrate 
life  has  left  the  sea  to  live  in  fresh  water,  on  swampy  land,  and  finally 
on  dry  land  and  in  the  air.  It  has  produced  special  types  able  to  sup- 
port life  by  such  an  astonishing  variety  of  devices  that  we  cannot 
possibly  specify  them  all.  We  shall  only  direct  attention  to  a  few,  and 
thus  attempt  to  obtain  an  impression  of  the  scheme  of  life  of  the  vast 
hordes  of  vertebrate  animals,  which,  in  one  shape  or  another,  have 
swarmed  and  still  swarm  in  the  waters  and  over  the  earth.  We  shall 
try  to  discern  whether  there  is  reason  to  suppose  that  all  this  variety 
is  related  in  some  way  to  changes  in  the  surrounding  world  and  we 
may  therefore  finish  this  introduction  by  a  brief  survey  of  the  evi- 
dences for  climatic  and  geographical  changes  such  as  may  have  been 
responsible  for  the  changes  in  organic  life. 

9.  Changes  of  climate  and  geological  periods 

9.1.  Changes  of  level  of  the  continents 

Changes  of  geography  are  mostly  so  slow  that  they  cannot  in  them- 
selves influence  individual  lives.  On  the  other  hand,  nearly  all  living 
things  must  be  suited  to  daily  and  annual  cyclical  changes,  unless  they 
live  where  no  light  enters.  There  is  indirect  evidence  of  further 
changes  in  climate  and  geography,  occurring  with  such  long  periods 
that  they  are  without  appreciable  effect  on  individual  organisms,  but 
may  greatly  affect  the  history  of  the  race. 

The  idea  of  geographical  change  is  made  familiar  by  the  fact  that 
coast-lines  and  river-courses  have  changed  appreciably  in  historical 
times.  We  are  familiar  with  stories  of  destruction  of  some  houses  or 
of  a  village  by  the  sea,  though  it  may  come  as  a  shock  to  learn  that  the 
sea-level  has  changed  so  much  that  England  and  France  were  con- 
nected by  land  8,000  years  ago,  and  that  man-made  instruments  fished 
up  from  the  Dogger  Bank  show  that  it  was  an  inhabited  peat  bog 
6,000  years  B.C.  These  changes  in  height  of  the  land  are  signs  of  the 
'diastrophic  movements',  which  are  major  features  of  long-period 
geological  evolution.  The  earth  forces  that  produce  these  movements 
are  still  obscure  but  they  lead  to  repeated  elevation  and  sinking  of  the 
land  masses.  The  action  of  frost,  wind,  and  rain  continually  breaks  up 


12  EVOLUTION  OF  LIFE  1.9 

and  carries  away  the  surface  of  the  land,  at  a  rate  of  the  order  of  1  ft 
per  4,000  years,  the  processes  known  as  weathering  and  denudation. 
The  material  carried  away  is  deposited  in  the  river-beds  and  in  the 
lakes  and  shallow  seas  around  the  river  mouths  (sedimentation)  (Fig. 
1).  Here  it  builds  the  sedimentary  rocks,  which  may  be  many  thou- 
sands of  feet  in  thickness,  the  whole  continental  platform  continuing 
to  sink  for  long  periods,  perhaps  with  intervals  during  which  it  be- 
comes raised  above  the  water.  Fossil  remains  are  usually  the  result  of 


km 
8 

6- 
4- 


8,840m. 

High  mountain 
ranges 

Average  height     ^ 
r  of  land     trX$ 


\0km 


Fig.  i.  Curve  showing  the  areas  of  the  earth's  solid  surface  in  relation  to  the 
sea  level.  (From  Holmes.) 

the  preservation  of  the  harder  parts  of  animals  in  sedimentary  deposits, 
and  the  most  complete  series  of  fossils  are  likely  to  be  those  of  animals 
living  in  the  seas. 

The  surface  crust  of  the  earth  is  not  a  layer  of  uniform  thickness  and 
density  but  consists  of  irregular  masses  of  lighter  material,  rich  in 
silicon  and  aluminium  (sial),  forming  the  continents,  and  heavier 
material,  rich  in  magnesium  (sima),  under  the  ocean  beds.  The  reason 
for  this  non-uniform  distribution  is  obscure,  but  it  has  the  effect  of 
making  the  continents  stand  higher,  floating  on  the  plastic  denser 
medium  beneath  the  crust.  When  material  is  removed  from  the  con- 
tinents by  denudation  they  rise;  conversely  the  addition  of  millions 
of  tons  of  ice  will  depress  them.  The  continents  are  thus  said  to  rest 
in  isostatic  equilibrium,  and  following  the  small  changes  in  level  the 
sea  leaves  more  or  less  of  the  continental  shelf  uncovered.  Such 
upward  and  downward  movements  profoundly  influence  the  climate. 
Oceanic  climatic  influences  tend  to  produce  a  damp,  equable  climate, 
with  large  areas  of  marsh  and  forest.  When  the  land  stands  higher 


i.9  GEOLOGICAL  CHANGES  13 

extremes  of  climate  develop,  some  parts  being  cold,  others  forming 
large,  dry  interior  plains. 

Besides  changes  in  the  balance  produced  by  denudation  and  the 
advance  of  ice-caps  there  are  also  from  time  to  time  marked  move- 
ments of  uplifting  or  lowering  of  the  land,  which  may  be  called 
independent  earth  movements.  Such  vertical  movements  of  the  con- 
tinental masses  are  produced  by  internal  forces  of  unknown  origin. 
They  are  doubtless  related  to  a  second  series  of  major  movements  of 
crustal  deformation  that  are  due  to  tangential  forces  and  lead  to  the 
formation  of  new  mountain  ranges  (orogenesis)  by  compression,  or  to 
fracturing  by  tension.  The  upwelling  of  lava  from  the  inside  of  the 
earth  at  these  times  makes  the  igneous  rocks,  usually  devoid  of  fossils. 

Changes  in  geography  are,  then,  mainly  changes  in  the  height  of 
the  land  and  the  amount  of  it  that  is  above  water.  Where  the  con- 
tinent is  surrounded  by  a  rather  shallow  continental  shelf,  this  leads 
to  considerable  changes  in  appearance  of  the  land-masses.  The  general 
opinion  is  that  the  main  outline  of  the  continental  masses  has  remained 
much  as  at  present,  at  least  since  Cambrian  times.  However  there  have 
probably  been  considerable  movements  of  the  land-masses  in  relation 
to  each  other.  Some  hold  that  the  continents  of  lighter  material  are 
continually  expanding,  at  least  in  certain  directions,  having  grown 
from  small  centres  to  their  present  size.  According  to  the  hypothesis 
of  Wegener,  the  continents  have  all  been  formed  by  the  splitting  up 
of  one  or  a  few  land-masses.  There  is  indeed  evidence  from  both 
geophysics  and  biology  that  the  continents  have  been  drifting  apart 
(Bullard,  1959).  The  direction  of  magnetization  of  rocks,  which  is 
determined  at  the  time  of  their  formation,  shows  that  the  land-masses 
must  have  changed  their  positions  greatly.  For  example,  such  data 
show  that  during  the  Triassic  period  the  British  Isles  lay  in  the  tropics 
and  in  confirmation  of  this  we  find  that  many  salt  deposits  (formed 
only  in  very  warm  climates)  lie  in  the  Triassic  formation  (Droitwich, 
Bath,  Nantwich,  &c). 

9.2.  Changes  of  climate 

Evidence  of  marked  changes  of  climate  is  the  finding  in  England 
and  other  regions  now  temperate  of  animal  and  plant  remains  appro- 
priate to  warmer  or  colder  conditions  (corals  and  woolly  rhinoceros, 
for  instance).  There  is  thus  every  reason  to  think  that  there  have  been 
great  changes  from  hot  to  cold  and  wet  to  dry  conditions,  in  conjunc- 
tion with  the  changes  in  latitude  and  in  level  of  the  land. 

These  fluctuations  in  geography  and  climate  are  obviously  of  great 


14  EVOLUTION   OF  LIFE  1.9 

importance  to  the  biologist.  We  can  hardly  expect  to  treat  animals 
and  plants  as  stable  systems  if  the  environment  around  them  is 
changing.  In  order  to  be  able  to  assess  the  influence  of  such  changes 
on  life  we  must  know  more  about  the  rates  at  which  they  occur,  and 
careful  study  shows  that  some  of  the  climatic  changes  are  rhythmic. 
Rhythmic  changes  of  climate  are,  of  course,  very  familiar  to  us  in  the 
cycles  of  days,  months,  and  years,  and  the  immense  importance  of 
these  short-period  changes  for  animal  and  plant  life  must  not  be 
forgotten. 

Here  we  are  more  concerned  with  changes  of  longer  periodicity,  of 
which  the  best  known  are  fluctuations  of  the  amount  of  solar  radiation 
received  at  any  given  part  of  the  earth's  surface.  These  are  likely  to 
be  especially  important  since  plants,  and  hence  ultimately  animals, 
depend  for  their  energy  on  sunlight.  The  cycle  of  number  of  sun- 
spots  (n*4  years)  involves  a  change  in  amount  of  radiation,  and  this  is 
associated  with  some  biological  cycles,  for  instance  in  the  distribution 
of  the  rings  of  growth  made  by  trees.  Longer-period  fluctuations  in 
the  amount  of  radiation  received  on  any  part  of  the  earth's  surface 
depend  on  the  perturbations  of  the  earth's  orbit,  particularly  on 
changes  in  the  obliquity  of  the  ecliptic.  The  effect  of  these  perturba- 
tions can  be  calculated,  and  the  results  show  that  at  any  one  place 
there  are  rhythmical  variations  in  the  amount  of  radiation  received, 
and  in  its  seasonal  distribution.  The  periodicity  of  these  calculated 
changes  is  about  40,000  years,  with  considerable  irregularities  and 
variations  in  the  sizes  of  the  maxima  (Fig.  2). 

During  the  last  million  years  (the  Pleistocene  epoch)  there  has  been 
a  series  of  waves  of  glaciation  (ice  ages);  the  ice-caps  have  several 
times  advanced  towards  the  equator  and  then  retreated  again.  These 
changes  are  usually  classified  into  four  periods  of  glaciation,  separated 
by  interglacial  periods.  However,  the  last  (fourth  Pleistocene)  glacia- 
tion, of  which  we  know  the  most,  certainly  had  three  separate  climaxes 
of  cold.  The  correspondence  of  these  with  especially  marked  minima 
in  the  curve  of  solar  radiation  is  not  perfect  (Fig.  2),  but  it  suggests 
that  the  basic  periodicity  may  have  been  something  like  40,000  years, 
and  that  the  division  of  the  whole  Pleistocene  period  into  four  periods 
of  glaciation  obscures  a  change  with  much  shorter  periodicity.  From 
about  120,000  to  180,000  years  b.p.  (Before  Present)  there  were  no 
marked  minima  in  the  solar  radiation  curve,  and  this  agrees  with  other 
evidence  of  a  long  interglacial  period  (third  Pleistocene  interglacial). 
Two  marked  minima  agree  with  the  other  signs  of  a  penultimate  (third 
Pleistocene)  glaciation,  and  this  was  preceded  by  a  very  long  warmer 


i.9  CLIMATIC   CHANGES  15 

period,  the  second  inter-glacial.  As  we  go  farther  back  the  study 
becomes  more  and  more  difficult,  but  the  available  evidence  suggests 
that  fluctuations  of  climate  considerable  enough  to  alter  the  entire 
fauna  and  flora  may  have  taken  place  at  a  periodicity  of  something 
over  40,000  years.  It  is  a  measure  of  the  difficulty  of  geological 
science  that  we  cannot  yet  give  a  systematic  account  of  the  chronology 
or  climatic  changes  even  of  the  relatively  recent  Pleistocene  period 
(variously  estimated  at  600,000  to  1,800,000  years)  during  which  these 
glaciations  occurred. 


RM590       R.M550 
EGI  1  EGI  2 

EARLY GLACIATION 


RM476  RM  435 

ApGI  I  ApGI  2 

ANFEPENULTIMATE  GLACIATION 


Fig.  2.  Curve  of  solar  radiation  received  at  65 °  N.  lat.  in  the  summer.  The  radiation  is 
expressed  in  'canonic  units'  (related  to  the  solar  constant  in  calories).  Time  in  thousands 
of  years.  R.M.  25,  &c,  indicate  the  radiation  minima.  (From  Zeuner,  based  on  the  tables 

of  Milankovitch.) 

As  we  proceed  to  study  times  still  more  remote  our  vision  becomes 
increasingly  blurred.  We  can  now  only  rarely  distinguish  periodicities 
as  short  as  40,000  years,  though  there  is  evidence  that  they  existed,  for 
instance  from  varved  Cretaceous  sediments.  All  we  can  see  in  the 
study  of  geological  deposits  are  the  very  marked  changes  produced  by 
the  major  movements  of  orogenesis  and  by  the  isostatic  readjust- 
ments. The  surprising  thing  is  that  these  immensely  slow  changes 
have  been  sufficiently  regular  to  leave  layered  deposits,  allowing  the 
development  of  a  system  of  geological  classification.  The  process  of 
sedimentation  was  interrupted  by  periods  when  the  continental  shelf 
on  which  the  rocks  rest  was  raised  above  the  water  surface  and  under- 
went denudation  for  a  while,  before  being  again  lowered  below  the  sea 
and  covered  with  a  new  deposit.  During  the  interval,  while  the  shelf 
was  raised  above  the  water,  the  animals  and  plants  in  the  sea  became 


16  EVOLUTION  OF  LIFE  1.9 

changed;  thus  rather  sharp  breaks  appear  in  the  series  of  fossils.  The 
occurrence  of  these  breaks  has  been  used  by  geologists  to  define  the 
major  geological  periods,  which  thus  correspond  to  cycles  of  elevation 
and  depression  of  the  continents.  By  comparing  the  fossils  contained 
in  the  rocks  major  geological  periods  have  been  recognized  in  various 
parts  of  the  world.  The  times  of  submergence  and  emergence  differ 
from  region  to  region,  however,  and  no  very  close  detailed  comparison 
is  possible.  It  is  easy  to  forget  that  climates  and  land  levels  do  not 
always  change  in  the  same  direction  in  different  parts  of  the  world. 

9.3.  Geological  time 

Until  recently  most  geologists  assumed  that  there  was  a  regular 
cycle  of  raising  and  lowering  (diastrophism)  and  that  comparable 
periods  could  be  recognized  everywhere.  It  is  now  widely  doubted 
whether  there  has  been  any  such  'pulse  of  the  earth'.  The  rock  series 
are  not  the  same  in  all  the  continents.  For  example,  in  South  Africa 
three  long  series,  known  as  Cape,  Karoo,  and  Cretaceous  formations, 
occupy  the  time  covered  in  Europe  by  the  many  elevations  and  depres- 
sions between  Silurian  and  Cretaceous  times.  Probably  the  conditions 
under  which  rocks  were  formed  have  remained  about  the  same 
throughout  geological  time  but  have  been  interfered  with  by  periods 
of  elevation,  depression,  and  folding  that  are  peculiar  to  each  region. 

The  study  of  fossils  often  establishes  the  order  in  which  the  rocks 
were  laid  down,  but  other  methods  have  to  be  used  to  discover  the 
period  of  time  covered  by  each  stage.  This  is  especially  important  to 
the  biologist,  who  wants  to  know  the  rate  at  which  animals  or  plants 
have  evolved.  Reliable  knowledge  of  the  ages  of  the  rocks  has  only 
begun  to  accumulate  since  the  discovery  of  radioactivity.  Uranium 
and  thorium  disintegrate,  producing  lead,  at  rates  that  are  unaffected 
by  any  known  conditions.  The  age  of  any  rock  since  its  deposition  can 
therefore  be  calculated  if  we  can  estimate  the  amount  of  breakdown 
products  of  these  elements  present  in  it.  The  lead  present  in  a  rock  is 
often  not  all  derived  from  the  uranium  and  thorium  there,  but  separa- 
tion of  the  lead  isotopes  enables  those  of  radioactive  origin  to  be 
estimated,  and  the  age  of  the  deposit  can  then  be  determined,  assum- 
ing that  the  breakdown  of  uranium  to  lead  began  when  the  rock  was 
crystallized  in  its  present  position.  Other  methods  of  estimating  the 
ages  of  rocks  from  isotope  ratios  have  been  developed.  Especially 
promising  is  the  determination  of  the  ages  of  the  deposition  of  sedi- 
mentary rocks  from  the  ratio  of  A40/K40  and  Sr87/Rb87  in  deposits 
formed  by  erosion  of  micas  or  granites. 


1.9 


GEOLOGICAL  TIME 


17 


The  time  at  which  the  crust  of  the  earth  assumed  its  present  form 
is  now  thought  to  have  been  4,500  million  years  ago  (Holmes,  1959) 
but  the  rocks  laid  down  during  the  greater  part  of  this  long  period 
contain  no  undoubted  animal  or  plant  remains.  Cambrian  rocks, 
when  fossils  become  readily  discernible,  were  laid  down  about  600 
million  years  ago. 


25    60 
0  11    40   70 


MILLIONS    OF     YEARS 
135    180     225    270  305    350     400  440 


500 


600 


21 
42 

68 

98 
110 

£  161 

u.  205 


CEpliocene 
sTl   i     i  i 
^j-  MIOCENE 

"IjJ-o'ugocene 
~3JJeocene 


o 


235 
254 
2  74 
300 


O  , 


38 


372 


412 


452 


PRECAMBRIAN 


_i I I I I I I i l_ 


100 


200  300  400 

MILLIONS      OF     YEARS 


500 


■  ■  '  ■ 


600 


i  i i  i  . 


0 
50 
100 
150 
200 
250 
300 
350 
400 
450 


700 


Fig.  3  shows  the  maximum  thickness  of  sediment  in  each  period  plotted  against  estimates 
of  the  absolute  date.  The  error  attached  to  these  determinations  is  shown  by  the 
marginal  lines.  Apparently   the  rate  of  sedimentation  has  not  been  constant  (modified 

after  Holmes). 

Classical  geology  is  based  mainly  on  studies  in  Europe  and  North 
America.  Although  a  terminology  based  on  absolute  time  is  beginning 
to  emerge,  it  is  still  necessary  to  use  that  based  mainly  on  stratigraphic 
studies,  begun  by  William  Smith  in  the  British  Isles  early  in  the  nine- 
teenth century.  In  this  system,  the  time  since  the  Cambrian  is  divided 
into  eleven  major  periods,  but  several  of  these  were  double  or  triple 
periods  of  advance  and  retreat  of  the  sea.  Even  the  most  carefully 
compiled  radioactivity  data  are  not  yet  adequate  to  provide  us  with 
definite  estimates  of  the  durations  of  the  periods,  though  there  is 
agreement  on  a  total  period  of  about  600  million  years  since  the 
Cambrian.  Fig.  3  shows  the  maximum  thickness  of  sediment  in  each 
period  plotted  against  estimates  of  the  absolute  dates.   The  error 


18  EVOLUTION  OF  LIFE  1.9 

attached  to  these  determinations  is  shown.  Apparently  the  rate  of 
sedimentation  has  not  been  constant. 

It  is  conventional  to  postulate  a  series  of  crustal  revolutions.  The 
extent  of  the  movements  has  not  been  equal  throughout  and  some  of 
them,  more  marked  than  others,  were  times  of  building  of  great 
mountain  chains  such  as  the  Alps  or  Andes  (Fig.  4).  There  were  also 
many  lesser  rises  and  falls  and  changes  of  climate  with  shorter  periods, 

Table  I 

MAXIMUM    THICKNESSES   AND    REVISED    TIME-SCALE 

(ACCORDING    TO    HOLMES) 

THICKNESSES   IN  THOUSANDS   OF  FEET  TIME    SCALE  IN   MILLIONS   OF    YEARS 


WORLD 
MAXIMA 

6 

CUMULATIVE 

MAXIMA           PERIODS 

6           PLEISTOCENE 

SINCE 

BEGINNING 

OF  PERIOD 

1 

DURATION 

OF 

PERIOD 

1 

15 
21 

21 
42 

PLIOCENE 
MIOCENE 

11 
25 

10 

14 

26 

68 

OLICOCENE 

40 

15 

30 

98 

EOCENE 

60 

20 

12 

110 

PALEOCENE 

70  ±   2 

10 

51 

161 

CRETACEOUS 

35±   5 

65 

44 

205 

JURASSIC 

80  ±   5 

45 

30 

235 

TRIASSIC 

25±    5 

45 

19 

2014* 
26j46 

254 

300 

PERMIAN 

upper") 
CARBONIFEROUS 

LOWER  J 

70  ±    5 

•     350  ±10 

45 
80 

38 

338 

DEVONIAN 

400  ±10 

50 

34 

40 

372 
412 

SILURIAN 
ORDOVICIAN 

450+10 
500+15 

40 
60 

40 

452 

CAMBRIAN 

600  ±20 

100 

such  as  those  of  about  40,000  years  that  we  can  detect  in  the  later  part 
of  the  Pleistocene.  Many  modern  geologists  are  sceptical  about  the 
existence  of  any  regularities  or  rhythms  in  these  changes  (see  Herbert, 
1952,  and  Gilluly,  1949).  It  is  useful  when  trying  to  adjust  the  mind 
to  periods  of  30  million  years  to  remember  the  frequent  changes  of 
level  and  climate  that  have  occurred  in  the  last  100,000  years.  In 
spite  of  all  that  we  know  about  the  history  of  the  earth's  surface,  it  is 
necessary  every  time  that  we  make  statements  about  the  influence  of 
presumed  climatic  changes  on  organic  evolution  to  remember  how 
scanty  our  knowledge  is. 

9.4.  Classification  of  geological  history 

The  period  isolated  as  'Cambrian'  by  geologists  lasted  100  million 
years  and  almost  certainly  included  several  inundations,  perhaps 
three.  The  Ordovician  lasted  for  60  million  years  and  included  three 


i.9        RHYTHM  OF  GEOLOGICAL  CHANGES         19 

floods  in  North  America.  There  were  powerful  earth  movements  at 
the  end  of  this  period,  at  any  rate  in  North  America,  known  as  the 
Taconian  revolution.  The  Silurian,  lasting  for  40  million  years, 
apparently  included  a  single  main  cycle  of  inundation,  ending  in  an 
elevation  of  the  land,  which  though  slight  in  America,  was  marked 
in  Europe  as  the  Caledonian  revolution,  producing  the  range  of 
mountains  stretching  across  Scandinavia  to  Scotland  and  Ireland. 


GENERALIZED  CONTINENTAL 


SUBMERGENCES 


PALEOZOI     C 


ME    S  0  Z  O  I  C 


CEN0ZO1C 


CAMBRIAN  0RO0VICIAN       SIL       DEVONIAN       MISS  PENN       PERMIAN 


h-RiAssir   iiiRA«if     L0W         UpPER 
TRIASS'C  JURASSIC    CRET      CRETACEOUS 


Tai    n  1-  Acadian  Appalachian  Nevadian  Laramidt        Cascadian 


Fig.  4.  Diagrams  of  main  changes  of  areas  of  land  and  water  and  in  climatic  conditions 

since  the  Cambrian.  The  chief  times  of  mountain-building  (orogenesis)  in  America  are 

also  shown.  (Redrawn    by   permission   from  Textbook  of  General  Zoology,  2nd  ed.  by 

W.  C.  Curtis  and  M.  J.  Guthrie,  John  Wiley  &  Sons,  Inc.,  1933.) 

Throughout  these  early  Palaeozoic  periods  the  fossils  are  entirely 
those  of  aquatic  animals,  except  for  some  traces  of  land  plants  and 
arthropods  at  the  end  of  the  Silurian.  The  oldest  remains  of  verte- 
brates are  fish-scales  from  the  Ordovician  (p.  125).  Details  of  the 
Palaeozoic  climatic  changes  are  not  clear,  but  the  fact  that  corals, 
which  can  now  live  only  in  warm  water,  were  alive  over  a  considerable 
part  of  the  earth's  surface  suggests  that  conditions  were  warmer  than 
at  present  at  least  at  some  early  Palaeozoic  times. 

The  Devonian  is  considered  by  some  to  include  a  single  main 
period,  about  50  million  years  long,  with  one  flood  at  the  middle  and 
more  arid  conditions  at  the  end,  but  other  authorities  divide  it  into 
several  periods.  The  first  forests  appeared  at  this  time,  and  here,  also, 
are  found  tti3  first  signs  of  vertebrate  terrestrial  life,  in  the  form  of 
fossil  lung-fishes  and  amphibians  (p.  296).  The  period  recognized  as 
Carboniferous  in  Europe  includes  two  major  periods  of  about  40 


2o  EVOLUTION  OF  LIFE  1.9- 

million  years  each  in  America,  the  Mississippian  and  Pennsylvanian. 
Throughout  this  long  time  conditions  varied  widely  in  different  parts 
of  the  world.  In  the  early  Mississippian  there  were  many  swamps  in 
North  America.  In  the  northern  hemisphere  the  Pennsylvanian  was 
probably  a  time  of  warm,  moist  conditions,  with  no  cold  winters, 
but  there  are  signs  that  for  part  of  this  time  India  and  Africa  were 
covered  with  an  ice-sheet.  The  coal  measures  show  us  the  remains  of 
the  forests  of  spore-  and  seed-bearing  plants  that  were  then  pro- 
duced, and  the  land  conditions  evidently  favoured  the  life  of  the 
Amphibia. 

The  Permian  probably  constitutes  a  single  45-million-year  period, 
with  very  active  orogenesis,  leading  to  a  more  arid  climate,  perhaps 
showing  large  seasonal  changes,  with  deserts  in  some  parts  of  the 
world  and  glaciation  in  others.  These  conditions  continued  into  the 
Triassic,  when  the  continents  lay  high.  The  reptiles,  first  found  in 
the  Permian,  developed  throughout  the  Triassic  and  flourished  in  the 
succeeding  Jurassic  period,  which  probably  lasted  45  million  years. 
The  Cretaceous  period,  during  which  the  thick  chalk  deposits  were 
laid  down,  probably  lasted  for  rather  more  than  60  million  years, 
including  two  major  cycles  of  inundation.  The  lower  Cretaceous 
certainly  included  extensive  periods  of  flooding,  when  there  were 
large  shallow  seas.  Then  later,  towards  the  end  of  the  upper  Creta- 
ceous, there  were  extensive  orogenic  movements,  the  Laramide 
revolution,  producing  the  Rockies  and  the  Andes.  The  temperature 
was  warm  until  near  the  end  of  the  Cretaceous,  and  we  do  not  know 
what  condition  led  to  the  break  that  is  found  between  the  animals  of 
the  Cretaceous  and  Eocene.  Some  groups  of  dinosaurian  reptiles  seem 
to  have  died  out  suddenly,  but  it  is  important  to  notice  that  not  all 
disappeared  at  the  same  time,  for  instance,  the  stegosaurs  and 
pterodactyls  (p.  569)  disappeared  well  before  the  end  of  the  Cretaceous. 
However,  it  is  probable  that  great  changes  went  on  at  the  end  of  this 
period,  and  we  may  guess  that  a  factor  leading  to  the  development  of 
the  birds  and  mammals  was  the  great  rise  of  the  continents,  perhaps 
accompanied  by  a  fall  in  temperature  over  wide  areas  that  had  enjoyed 
warmer  weather.  As  always,  when  we  look  closely  at  such  problems, 
we  are  appalled  by  the  vast  lengths  of  time  involved  and  the  scanty 
nature  of  our  clues  about  them.  The  land  lay  very  high  at  this  time, 
and  the  apparent  abruptness  of  the  break  between  Cretaceous  and 
Eocene  fauna  may  be  an  artifact  due  to  the  scarcity  of  fossils.  In 
North  America  there  is  evidence  from  terrestrial  deposits  of  a  long 
Paleocene  period  between  the  Cretaceous  and  Eocene. 


i.  10  GEOLOGICAL  PERIODS  21 

It  is  usual  to  divide  the  last  main  geological  period,  the  Tertiary,1 
into  epochs,  Paleocene,  Eocene,  Oligocene,  Miocene,  Pliocene,  and 
Pleistocene,  the  names  originally  referring  to  the  percentage  of  fossil 
genera  surviving  to  the  present  day  (see  p.  571).  Probably  the  whole 
time  since  the  end  of  the  Cretaceous  has  been  about  70  million  years. 
During  the  early  part  of  the  Tertiary  period  the  climate  was  cold,  but 
as  erosion  of  the  mountains  that  had  been  produced  at  the  end  of  the 
Cretaceous  proceeded  the  conditions  became  warmer,  and  throughout 
the  Eocene  and  Oligocene  there  were  large  forests  and  humid  con- 
ditions. Then  during  the  Miocene  there  were  marked  earth  move- 
ments, leading  to  elevation  of  the  land  and  accompanied  by  more  arid 
conditions,  with  wide  areas  of  prairie  and  the  widespread  appearance 
of  important  new  food  plants — the  grasses.  The  weather  probably 
became  gradually  colder  through  the  Pliocene,  no  doubt  with  many 
fluctuations,  culminating  in  the  ice  ages  of  the  Pleistocene.  Here  we 
come  back  to  the  period  of  which  we  have  more  detailed  knowledge, 
and  are  reminded  that  the  ice  age  was  not  continuous,  but  interrupted 
by  many  wrarmer  periods. 

This  very  brief  survey  of  geological  history  in  the  northern  hemi- 
sphere can  hardly  do  more  than  remind  us  of  the  depths  of  our  ignor- 
ance. We  see  enough  to  be  sure  that  climatic  conditions  have  varied 
throughout  the  millions  of  years,  but  we  cannot  yet  see  sufficient 
details  to  allow  us  to  discover  whether  there  is  any  rhythm  of  major 
cycles.  It  is  easy  to  talk  glibly  of  'Carboniferous  forests'  or  'arid  con- 
ditions of  the  Permian',  forgetting  that  these  periods  lasted  for  a  time 
that  we  can  only  roughly  record  in  numbers  and  not  properly  imagine 
in  terms  of  our  experience,  although  we  are  among  the  longest  lived 
of  animals.  The  evidence  suggests  that  conditions  did  not  remain 
stable  for  such  a  vast  length  of  time  as  a  whole  geological  period,  but 
fluctuated  markedly,  either  irregularly  or  with  complicated  rhythms 
of  greater  and  lesser  magnitude.  We  must  not  forget  that  very  pro- 
found 'climatic'  changes  occur  every  day,  others  every  year,  and  some 
every  eleven  years.  It  is  not  impossible  that  these  shorter-period 
changes,  necessitating  continual  readjustment  of  animal  and  plant  life, 
have  been  as  important  as  the  slower  changes  in  producing  evolution. 

10.  Summary 

To  reduce  to  order  our  knowledge  of  vertebrate  life  we  shall  try 
to  discover  its  general  organization  and  then  examine  the  factors  that 

1  This  word  is  a  survival  from  an  old-fashioned  classification  of  rocks,  the  Tertiary  heing 
the  period  since  the  Cretaceous. 


22  EVOLUTION   OF  LIFE  i.  10 

have  produced  all  the  varied  types.  The  pattern  of  organization  we 
have  to  study  is  that  of  the  animal  as  an  active  system  maintaining 
itself  in  its  environment.  This  tendency  to  maintenance  and  growth 
is  the  central  'force'  that  produces  the  variety  of  life.  The  opportunity 
for  change  is  provided  by  the  fact  that  reproduction  seldom  produces 
an  exact  copy  of  the  parent,  and  thus  a  range  of  types  is  provided. 
The  tendencies  to  grow  and  to  vary  lead  animals  to  colonize  new  en- 
vironments and  produce  the  variety  of  life.  As  evolution  has  proceeded 
animals  have  come  to  occupy  environments  differing  ever  more  widely 
from  the  sea  in  which  life  probably  arose.  Life  in  these  more  difficult 
environments  is  made  possible  by  the  development  of  special  devices, 
making  the  later  animals  more  complex  than  the  earlier  and  in  this 
sense  'higher'.  It  remains  uncertain  what  influences  have  been  respon- 
sible for  producing  the  changes  in  organic  form.  Geological  evidence 
shows  that  there  have  been  many  changes  in  climate  and  geography, 
some  of  them  proceeding  at  very  slow  rates  in  comparison  with  the 
rhythms  of  individual  animal  lives.  It  is  uncertain  whether  evolution- 
ary changes  follow  these  slow  geological  changes,  or  are  a  result  of 
the  instability  imposed  on  living  things  by  climatic  rhythms  with 
shorter  periods,  such  as  those  of  days,  years,  and  the  sunspot  cycles. 


II 

THE  GENERAL  PLAN  OF  CHORDATE 
ORGANIZATION:  AMPHIOXUS 

1 .  The  variety  of  chordate  life 

The  Chordata  occupy  a  greater  variety  of  habitats  and  show  more 
complicated  mechanisms  of  self-maintenance  than  any  other  group  in 
the  whole  animal  kingdom.  They  and  the  arthropods  and  the  pulmon- 
ate  molluscs  have  fully  solved  the  problem  of  life  on  the  land — which 
they  now  dominate.  This  domination  is  achieved  by  most  delicate 
mechanisms  for  resisting  desiccation,  for  providing  support,  and  for 
conducting  many  operations  that  are  harder  in  the  air  than  in  water. 
By  even  more  wonderful  devices  the  body  temperature  is  raised  and 
kept  uniform  and  thus  all  reactions  accelerated.  Finally,  use  is  made  of 
this  high  rate  of  living  for  the  development  of  the  nervous  system  into 
a  most  delicate  instrument,  allowing  the  animal  not  only  to  change  its 
response  to  a  given  stimulus  from  moment  to  moment,  but  also  to 
store  up  and  act  upon  the  fruits  of  past  experience. 

Besides  these  more  developed  types  of  chordate  that  dominate  the 
land  and  air  there  are  also  great  numbers  of  extremely  successful 
aquatic  and  amphibious  types.  The  frog  is  often  referred  to  as  a  some- 
what lowly  and  unsuccessful  animal,  but  frogs  and  toads  are  found  all 
over  the  world.  The  sharks  and  bony  fishes  share  with  the  squids  and 
whales  the  culminating  ecological  position  in  the  food  chains  of  the 
sea,  while  the  bony  fishes  are  the  only  animals  that  have  achieved  con- 
siderable size  and  variety  in  fresh  water.  Among  the  still  more  lowly 
chordates  the  sea-squirts  take  a  very  important,  though  not  dominant, 
position  among  the  animal  and  plant  communities  that  occupy  the 
sea  bottom,  but  they  have  never  entered  fresh  water. 

One  could  continue  indefinitely  with  particulars  of  the  amazing 
types  produced  by  this  most  adaptable  phylum.  Yet  through  all  their 
variety  of  structure  the  chordates  show  a  considerable  uniformity  of 
general  plan,  and  there  can  be  no  doubt  that  they  have  all  evolved 
from  a  common  ancestor  of  what  might  be  called  a  'fish-like'  habit. 
In  the  very  earliest  stages  only  the  larva  was  fish-like,  and  the  life- 
history  probably  also  included  a  sessile  adult  stage,  such  as  the  tuni- 
cates  still  show  today  (p.  66).  This  bottom-living  phase  was  then 
eliminated  by  paedomorphosis,  the  larvae  becoming  the  adults.  There- 
fore the  essential  organization  of  a  chordate  is  that  of  a  long-bodied, 


24  CHORDATE  ORGANIZATION  n.  i- 

free-swimming  creature.  All  the  other  types  can  be  derived  from  such 
an  ancestor,  though  in  some  cases  only  by  what  is  often  called 
'degeneration'. 

2.  Classification  of  chordates 

We  may  conveniently  divide  the  Phylum  Chordata  into  four 
subphyla : 

Subphylum  i.  Hemichordata 

Balanoglossus;  Cephalodiscus;  Rhabdopleura 
Subphylum  2.  Cephalochordata  (=  Acrania) 

Branchiostoma 
Subphylum  3.  Tunicata 

Ciona,  Sea-squirts 
Subphylum  4.  Vertebrata 

The  Vertebrata,  the  largest  of  these  groups,  may  be  subdivided: 
Subphylum  Vertebrata 
Superclass  1.  agnatha 

Class  1.  Cyclostomata.  Lampreys  and  hag- fishes 

Class  2.  *Cephalaspidomorphi.  *Cephalaspis 

Class  3.  #Pteraspidomorphi.  *Pteraspis 

Class  4.  *Anaspida.  *Birkenia,  *Jamoytius 

Superclass  2.  gnathostomata 

Class  1.  *Placodermi.  *Acanthodes 

Class  2.  Elasmobranchii.  Dogfishes,  skates,  and  rays 

Class  3.  Actinopterygii.  Bony  fishes 

Class  4.  Crossopterygii.  Lung-fishes 

Class  5.  Amphibia 

Class  6.  Reptilia 

Class  7.  Aves 

Class  8.  Mammalia. 

3.  Amphioxus,  a  generalized  chordate 

It  has  long  been  realized  that  through  their  great  variety  all  these 
types  show  certain  common  features,  often  referred  to  as  the  typical 
chordate  characters.  It  is  better  to  regard  these  not  as  a  list  of  isolated 
'characters'  but  as  the  signs  of  a  certain  pattern  of  organization  that 
is  characteristic  of  the  group.  There  is  much  reason  to  suppose  that 
this  basic  chordate  organization  was  that  of  a  free-swimming  marine 
animal,  probably  feeding  by  the  collection  of  minute  particles.  We 
are  fortunate  in  having  still  alive  a  little  animal,  amphioxus,  the 


ii.  3  AMPHIOXUS  25 

lancelet,  which  shows  nearly  all  of  these  features  in  diagrammatic  form. 
Study  of  amphioxus  will  go  a  long  way  to  show  the  basic  plan  on  which 
all  later  chordates  are  built,  and,  indeed,  gives  us  a  strong  indication 
of  what  the  early  chordates  must  have  been  like. 

Though  it  can  swim  freely  through  the  water,  amphioxus  is  essenti- 
ally a  burrowing  animal,  and  many  of  its  special  features  are  connected 
with  this  habitat.  It  lives  in  the  sand,  at  small  depths,  and  has  been 
found  all  round  the  oceans  of  the  world.  Evidently,  in  spite  of  its 
simplicity,  it  is  a  successful  type.  It  is  found  on  British  coasts  and, 
indeed,  the  first  individual  described  was  sent  (preserved)  from  Corn- 
wall to  the  German  zoologist  Pallas,  who  supposed  it  to  be  a  slug  and 
called  it  Limax  lanceolatus  (1774).  It  was  first  figured  and  given  the 
name  Amphioxus  lanceolatus  by  Yarrell  in  1836.  However,  the  name 
Branchiostoma  had  been  given  in  1834  by  Costa  and  by  the  rules  of 
priority  this  is  the  official  name  of  the  genus.  We  may  keep  amphioxus 
as  a  common  name.  Some  eight  species  of  Branchiostoma  are  recog- 
nized, and  in  addition  there  is  a  group  of  six  species  referred  to  the 
genus  Asymmetron.  These  resemble  Branchiostoma  in  general  organi- 
zation, but  they  have  gonads  only  on  the  right  side. 

The  adult  Branchiostoma  lanceolatum  is  rather  less  than  2  in.  long 
and  has  the  typical  fish-like  organization,  whose  main  external 
features  are  related  to  the  methods  of  locomotion  and  feeding  (Fig. 
5).  The  body  is  elongated,  and  flattened  from  side  to  side.  The  skin 
has  no  pigment,  and  the  muscles  can  be  easily  seen  as  a  series  of 
blocks,  the  myotomes,  serving  to  bend  the  body  into  folds.  As  the 
name  implies,  the  body  is  pointed  at  both  ends;  there  is  no  recogniz- 
able head  separated  from  the  body.  Indeed,  there  are  no  separate  eyes, 
nose,  or  ears,  and  no  jaws,  so  that  the  fundamental  plan  of  chordate 
organization  appears  in  almost  its  fullest  simplicity  from  one  end  of 
the  body  to  the  other.  The  front  end  is,  however,  marked  by  a  series 
of  buccal  cirri,  which  form  a  sieve  around  the  opening  of  the  oral  hood 
and  are  provided  with  receptor  cells. 

Although  the  animal  is  provided  with  a  large  number  of  gill-slits 
these  do  not  appear  externally,  being  covered  by  lateral  folds  of  the 
body,  which  enclose  a  ventral  space,  the  atrium,  opening  posteriorly 
by  an  atriopore.  The  outside  edges  of  the  atrium  project  as  a  pair  of 
metapleural  folds,  giving  the  body  a  triangular  shape  in  transverse 
section.  The  alimentary  canal  opens  posteriorly  by  an  anus,  in  front 
of  the  hind  end  of  the  body,  thus  leaving  a  definite  tail — a  region  of 
the  body  not  containing  any  part  of  the  alimentary  canal. 

The  general  arrangement  of  the  organs  can  best  be  understood  by 


26  CHORDATE  ORGANIZATION  n.  3- 

considering  the  body  as  consisting  of  two  tubes,  the  outer  skin 
(ectoderm)  and  the  inner  alimentary  canal  (endoderm),  with  a  space 
between  (the  coelom)  lined  by  a  third  layer  (the  mesoderm).  This 
arrangement  is  actually  found  during  the  course  of  the  development 
(Fig.  18).  The  mesoderm  at  first  forms  thin  layers,  the  somatopleure 
applied  to  the  outer  body  wall  and  the  splanchnopleure  to  the  gut. 
Very  soon  the  inner  layer  becomes  much  thickened  where  it  is  applied 
to  the  nerve-cord  and  notochord,  and  here  it  forms  the  myotomes,  or 
muscle-blocks.  In  this  dorsal  part  of  the  mesoderm  the  coelom, 
known  here  as  the  myocoele,  soon  becomes  obliterated,  leaving  the 
ventral  splanchnocoele  around  the  gut.  Besides  the  muscle  that  forms 
in  the  myotomes,  non-myotomal  muscles  develop  in  the  somatopleure 
and  splanchnopleure.  These  are  not  divided  into  segments  and  are 
innervated  by  the  dorsal  nerve-roots,  the  ventral  roots  supplying  only 
the  myotomes. 

4.  Movement  of  amphioxus 

The  adult  myotomes  are  blocks  of  striated  muscle-fibres,  running 
along  the  body,  separated  by  sheets  of  connective  tissue,  the  myo- 
commas.  This  repetition  or  segmentation  is  characteristic  of  the 
organization  of  all  chordates.  The  myocommas  do  not  run  straight 
down  the  body  from  dorsal  to  ventral  side  but  are  V-shaped  (Fig.  5). 
However,  each  muscle-fibre  runs  straight  from  before  backwards,  and 
the  contraction  of  the  whole  myotome  therefore  bends  the  body.  A 
full  discussion  of  the  means  by  which  forward  motion  is  achieved  by 
such  a  system  will  be  given  later  (p.  133).  Essentially,  contraction  of 
the  myotomes  results  in  transverse  motion  of  the  body  inclined  at 
varying  angles  in  such  a  way  as  to  result  in  forward  propagation.  Each 
myotome  must  therefore  contract  after  that  in  front  of  it — the  effect 
being  to  produce  an  S-bend  that  moves  backwards  through  the  water 
as  the  fish  moves  forward. 

For  our  present  purpose  the  point  is  that  the  contraction  is  serial, 
that  is  to  say,  it  depends  on  the  breaking  up  of  the  longitudinal  muscle 
into  blocks.  It  was  probably  the  need  for  division  of  the  musculature 
that  led  to  the  development  of  the  segmentation,  and  this,  affecting 
primarily  the  muscles,  has  come  to  influence  a  great  part  of  chordate 
organization. 

Contraction  of  the  longitudinally  arranged  muscle-fibres  will  only 
produce  a  sharp  bending  of  the  body  if  there  is  no  possibility  of  short- 
ening of  the  whole.  To  prevent  telescoping,  an  incompressible  and 
elastic  rod,  the  notochord,  runs  down  the  centre  of  the  body.  It 


II.  4 


LOCOMOTION   OF  AMPHIOXUS 


27 


is  usually  stated  that  this  is  a 
'supporting  structure',  but,  of 
course,  an  animal  such  as  a  fish  in 
water  needs  no  'support'.  Nor  is 
the  notochord  a  lever  to  which 
muscles  are  attached,  as  they  are 
to  the  bones  of  many  higher  forms. 
No  muscles  pull  on  it  directly, 
though  the  myocommas  are  at- 
tached to  its  sheath.  Its  function 
is  to  prevent  the  shortening  of  the 
body  that  would  otherwise  be  the 
result  of  contraction  of  longitudi- 
nal muscles.  In  fact,  it  serves  to 
make  that  contraction  efficient  in 
bending  the  body;  its  elasticity 
may  also  play  an  important 
part. 

The  notochord  is  composed  of 
a  series  of  flattened  plates  sur- 
rounded by  a  fibrous  sheath.  The 
plates  are  arranged  in  a  regular 
manner  with  their  flat  surfaces  in 
the  transverse  plane  of  the  body. 
They  are  of  two  sorts,  fibrous 
and  homogeneous,  which  alternate 
with  each  other.  Each  plate  de- 
velops as  a  highly  vacuolated  cell, 
the  nuclei  being  later  pushed  aside 
to  the  dorsal  or  ventral  edge.  This 
structure  is  well  suited  by  the 
turgidity  of  its  cells  enclosed  in 
the  sheath  to  resist  forces  tending 
to  shorten  the  body.  The  cord  of 
amphioxus  is  peculiar  in  that  it 
extends  from  the  very  tip  of  the 
head  to  the  end  of  the  tail,  pro- 
jecting, that  is  to  say,  beyond  the 
level  of  the  myotomes,  a  condition 
presumably  associated  with  the 
burrowing  habit. 


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28 


CHORDATE   ORGANIZATION 


ii.  4- 


Amphioxus  probably  does  not  often  swim  free  in  the  water  and  the 
body  is  not  adapted  for  fast  movements.  It  has  no  elaborate  fins  such 
as  those  of  later  fishes,  which  ensure  static  stability  like  the  feathers 
on  an  arrow,  or  are  movable,  to  allow  active  control  of  the  direction 


Fig.  6.  Transverse  section  through  amphioxus  in  the  region  of  the  pharynx. 

atr.  atrium;  d.a.  dorsal  aorta;  d.  coel.  dorsal  portion  of  coelom;  div.  intestinal  diverticulum; 
d.n.1  and  d.n.2,  branches  of  the  dorsal  nerve-root;  end.  endostyle;  ep.gr.  epipharyngeal  groove; 
/.  fin-ray  box;  g.  gonad;  I  y.b.  primary  gill  bar  containing  coelom;  my.  myotome;  metapl. 
nietapleural  fold;  n.  notochord;  n.c.  nerve-cord;  ph.  pharynx;  sub. end. coel.  subendostylar 
coelom;  t.b.  tongue  bar;  v. a.  ventral  aorta;  v.n.  ventral  nerve-root.  (After  Krause.) 


of  swimming  (p.  136).  There  is  a  low  dorsal  ridge,  which  continues 
behind  as  a  small  caudal  fin.  There  are  no  definite  paired  fins,  but  the 
metapleural  folds  might  perhaps  be  considered  comparable  to  the 
lateral  fin  folds  from  which  all  vertebrate  limbs  are  probably  derived. 
They  are  distended  with  coelomic  fluid  and,  with  the  dorsal  ridge, 


II.  6 


SKELETAL  STRUCTURES  OF  AMPHIOXUS 


29 


probably  serve  to  protect  the  body  during  the  rapid  dives  by  means  of 
which  the  creature  enters  the  sand.  The  habit  of  swimming  with  the 
front  end  downwards  suggests  the  presence  of  a  gravitational  receptor 
mechanism.  The  larvae  of  lampreys  swim  in  a  similar  way  (p.  114). 


scut 


Fig.  7.  Section  of  the  skin  of  amphioxus. 

b.v.  blood-vessel;  cut.  cutis;  ep.  epidermis;  n.  nerves;  s.cut.  sub-cutis. 
(After  Krause.) 

5.  Skeletal  structures  of  amphioxus 

Around  the  notochordal  sheath  is  a  further  layer  of  gelatinous 
material  containing  fibres.  There  are  no  cells  within  this  material 
but  it  is  secreted  by  cells  around  the  outside,  which  retain  the  epithe- 
lial arrangement  of  the  mesoderm  from  which  they  were  derived. 
This  connective  tissue  continues  as  a  sheath  around  the  nerve-cord 
and  above  this  into  a  series  of  structures  known  as  fin-ray  boxes, 
which  support  the  median  ridge.  These  are  more  numerous  than  the 
segments  and  each  contains  a  more  rigid  material  referred  to  as 
'cartilage'.  The  relationship  of  these  structures  to  the  fin  supports  of 
vertebrates  is  obscure.  Other  skeletal  rods  occur  in  the  cirri  around 
the  mouth  and  in  the  gill  bars. 

6.  Skin  of  amphioxus 

The  epidermis  differs  from  that  of  vertebrates  in  being  very  thin, 
composed  of  a  single  layer  of  cells,  ciliated  in  the  young,  and  with  the 
outer  border  slightly  cuticularized  in  the  adult  (Fig.  7).  It  is  not 


3o  CHORDATE  ORGANIZATION  n.6- 

known  whether  this  cuticle  contains  a  substance  similar  to  the  keratin 
produced  by  the  many-layered  skin  of  later  forms.  There  are  receptor 
cells  but  no  glands  or  chromatophores  in  the  skin. 

Below  the  epidermis  is  a  fibrous  cutis,  and  below  this  again  a 
gelatinous  material  containing  fibres,  the  sub-cutis.  Both  these  layers 
are  secreted  by  scattered  cells  having  some  similarity  to  the  fibroblasts 


Fig.  8.  Anterior  end  of  amphioxus,  from  a  stained  and  cleared  preparation 
of  a  young  animal. 

b.c.  buccal  cirri;/,  fin-ray  box;  II. p.  Hatschek's  pit;  my.  myotome;  n.  notochord; 
n.c.  nerve-cord;  p.  pigment  spot;  ph.  pharynx;  v.  velar  tentacles;  zi.o.  wheel  organ. 

of  higher  forms.  They  contain  a  system  of  cutaneous  canals,  with 
endothelial  lining  (Fig.  14). 


7.  Mouth  and  pharynx  and  the  control  of  feeding 

Amphioxus  obtains  its  food  by  extracting  small  particles  from  a 
stream  of  water,  which  it  draws  in  by  means  of  cilia.  In  all  animals 
that  use  cilia  for  this  purpose  a  very  large  surface  is  provided  (e.g. 
lamellibranchs,  ascidians),  and  the  pharynx  and  gill  bars  of  amphioxus 
occupy  more  than  one-half  of  the  whole  surface  area  of  the  body. 
Special  arrangements  are  made  for  the  support  and  protection  of  this 
ciliated  surface,  the  wall  of  the  pharynx  being  so  greatly  subdivided 
that  it  needs  the  protection  of  an  outer  layer,  the  atrium. 

The  mouth  lies  covered  by  an  oral  hood  whose  edges  are  drawn  out 
into  buccal  cirri,  provided  with  sense-cells  (Fig.  8).  When  feeding  the 
cirri  are  curved  to  form  a  funnel-like  sieve  preventing  the  entry  of 
large  particles.  Around  the  mouth  itself  there  is  a  further  ring  of 


ii.  7 


FEEDING   OF  AMPHIOXUS 


3i 


sensory  tentacles,  the  velum.  The  oral  hood  contains  a  complex  set  of 
ciliated  tracts,  the  'wheel  organ'  of  Miiller,  and  this  plays  a  part  in 
sweeping  the  food  particles  into  the  mouth  (Figs.  8  and  9).  Near  its 
centre  is  a  groove,  Hatschek's  pit,  formed  as  an  opening  of  the  left 
first  coelomic  sac  to  the  exterior  (p.  44). 

The  main  operation  of  food  collec- 
tion is  performed  by  the  pharynx,  a 
large  tube,  flattened  from  side  to  side, 
whose  walls  are  perforated  by  nearly 
200  oblique  vertical  slits,  the  number 
increasing  as  the  animal  gets  older. 
The  slits  are  separated  by  bars  con- 
taining skeletal  rods  and  further  sub- 
division is  provided  by  cross-bars 
(synapticulae).  Since  the  bars  slope 
diagonally  many  of  them  are  cut  in  a 
single  transverse  section,  but  it  must 
be  remembered  that  they  are  essen- 
tially the  vertical  portions  of  the  main 
walls  of  body  and  pharynx,  where 
these  have  not  been  perforated  by  a 
gill-slit.  Such  a  portion  of  the  body 
wall  must  contain  a  coelomic  space 
and  this  can  in  fact  be  seen  in  the 
original  or  primary  gill  bars.  How- 
ever, an  increase  of  the  ciliary  surface 
is  produced  by  downgrowth  of  secon- 
dary or  tongue  bars  from  the  upper 
margin,   dividing  each  primary  slit; 

these  secondary  bars  contain  no  coelom.  The  coelomic  spaces  in  the 
primary  bars,  of  course,  communicate  above  and  below  with  con- 
tinuous longitudinal  coelomic  cavities  (Fig.  6). 

There  are  cilia  on  the  sides  and  inner  surfaces  of  the  gill  bars,  the 
lateral  ones  being  mainly  responsible  for  driving  the  water  outwards 
through  the  atrium  and  thereby  drawing  the  feeding  current  of  water 
in  at  the  mouth.  In  the  floor  of  the  pharynx  lies  the  endostyle,  con- 
taining columns  of  ciliated  cells,  alternating  with  mucus-secreting 
cells,  which  produce  sticky  threads  in  which  food  particles  become 
entangled.  Various  currents  then  draw  the  sticky  material  along  until 
it  reaches  the  mid-gut.  The  frontal  cilia  of  the  gill  bars  produce  an 
upward  current,  driving  the  mucus  from  the  endostyle  into  a  median 


Fig.  9.    Transverse  section  through 
front  end  of  amphioxus. 

b.c.  buccal  cirri;  e.  eyespot;  H.p.  Hats- 
chek's pit;  ?i.  notochord;  n.C.  nerve-cord. 


32  CHORDATE  ORGANIZATION  n.  7- 

dorsal  epipharyngeal  groove,  in  which  it  is  conducted  backwards. 
The  cilia  of  the  endostyle  also  move  mucus  along  the  peripharyngeal 
ciliated  tracts,  behind  the  velum,  to  join  the  epipharyngeal  groove. 
Radioactive  iodine  is  concentrated  by  one  of  the  columns  of  the  endo- 
style and  secreted  with  the  mucus.  Barrington  (1958)  suggests  that 
these  may  be  regarded  as  the  precursors  of  the  thyroid  cells,  serving 
to  produce  iodinated  mucoproteins,  which  are  then  absorbed  farther 
down  the  gut  (see  p.  119). 

The  pharynx  narrows  at  its  hind  end  to  open  dorsally  into  a  region 
best  known  as  the  mid-gut,  the  name  stomach  being  inappropriate. 

£{■  nig.  ant.        fg.post  (cft 

/  Ag 

T^^^'|l^|i|Mii)iifmiTn^r  .        y 


Fig.  10.  Currents  in  the  mid-gut  of  amphioxus,  showing  the  appearance  when  an 
animal  is  placed  in  a  medium  containing  carmine  particles.  Arrows  show  the  chief 

ciliary  currents. 

div.  diverticulum ;f.c.  food  cord;  h.g.  hind-gut;  i.c.r.  ileo-colon  ring;  m.g.ant.  and  m.g.post. 

anterior  and  posterior  parts  of  mid-gut;  oes.  oesophagus.  (After  Barrington.) 

A  large  mid-gut  diverticulum  reaches  forward  from  this  region  on  the 
right-hand  side  of  the  pharynx.  From  its  position  this  organ  is  often 
called  the  liver,  but  Barrington  has  given  reasons  for  supposing  that 
it  is  the  seat  of  the  production  of  digestive  enzymes.  Zymogen  cells, 
similar  to  those  of  the  mid-gut,  are  found  in  its  walls.  Its  strong  dorsal 
and  ventral  ciliation  maintains  in  it  a  circulation  of  food  materials  and 
secretion,  and  its  cells  are  capable  of  phagocytosis  as  well  as  secretory 
activity.  Amphioxus  thus  combines  intracellular  with  extracellular 
digestion,  doubtless  in  connexion  with  its  microphagous  habit. 
Particles  placed  in  the  diverticulum  are  swept  backwards  and  join  the 
main  food  cord  that  passes  through  the  mid-gut  (Fig.  10). 

The  hind  end  of  the  mid-gut  is  marked  by  a  specially  ciliated  region, 
the  ileo-colon  ring,  whose  cilia  rotate  the  cord  of  mucus  and  food.  The 
movement  is  transmitted  to  the  portion  of  the  food  cord  in  the  mid- 
gut and  presumably  assists  in  the  taking  up  of  the  enzymes  that 
emerge  from  the  diverticulum.  Extracellular  digestion  takes  place  in 
the  mid-gut  and  the  enzymes  responsible  have  been  studied  by  Bar- 
rington. The  pH  of  the  contents  varies  from  67  to  7-1.  An  amylase  is 
present  in  extracts  of  the  diverticulum,  mid-gut,  and  hind-gut,  but 
not  in  those  of  the  pharynx.  Lipase  and  protease  are  present  in  the 


ii.  8  FEEDING  OF  AMPHIOXUS  33 

same  regions,  the  latter  having  an  optimum  action  at  about  pH  8-o, 
being,  that  is  to  say,  a  tryptic  type  of  enzyme.  There  is  no  sign  of 
any  protease  with  an  acid  optimum,  similar  to  the  pepsin  of  higher 
forms. 

Behind  the  ileo-colon  ring  the  intestine  runs  as  a  straight  hind-gut 
to  the  anus.  Absorption  of  food  takes  place  here,  and  perhaps  also 
in  the  mid-gut,  apparently  partly  by  intracellular  digestion,  since 
ingested  carmine  particles  are  taken  into  the  cells. 

The  feeding  current  is  regulated  by  the  rate  of  beat  of  the  cilia  and 
the  degree  of  contraction  of  the  inhalent  and  exhalent  apertures.  The 
walls  of  the  atrium  contain  an  elaborate  system  of  afferent  and 
efferent  nerve-fibres.  The  receptors  include  a  set  of  large  peripheral 
nerve-cell  bodies,  lying  beneath  the  atrial  epithelium  and  sending 
axons  in  by  way  of  the  dorsal  roots.  The  motor  fibres  also  pass  through 
the  dorsal  roots  and  run  without  synapse  to  the  cross-striated  fibres 
of  the  pterygial  muscle,  which  forms  the  floor  of  the  atrium.  The 
stream  flowing  into  the  pharynx  is  tested  by  the  receptors  of  the  velum 
and  atrium,  and  if  noxious  material  is  present,  the  water  is  expelled  by 
closing  the  atriopore  and  contracting  the  pterygial  muscle,  producing 
a  'cough'.  The  system  can  distinguish  between  suspensions  of  food 
material  and  inorganic  particles.  When  sufficient  food  has  been  taken, 
collection  is  suspended  until  it  has  been  digested  (Bone,  i960). 

The  atrial  nervous  system  probably  regulates  spawning  as  well  as 
feeding.  It  has  often  been  compared  with  the  sympathetic  system  of 
craniates  but  there  are  almost  no  close  similarities.  The  nerve  cells  in 
it  are  receptors  and  there  is  no  sign  of  the  peripheral  synapse  on 
the  efferent  pathway  that  is  so  characteristic  of  the  true  autonomic 
system.  The  atrial  system  is  developed  in  relation  to  filter  feeding 
and  has  perhaps  been  completely  lost  in  higher  forms  that  feed  by 
other  methods  and  have  developed  new  methods  to  control  them 
(p.  117). 

8.  Circulation 

The  blood-vessels  of  amphioxus  show  in  diagrammatic  form  the 
fundamental  plan  on  which  the  circulation  of  all  chordates  is  based 
(Fig.  11).  Slow  waves  of  contraction  occur  in  various  separate  parts 
in  such  a  way  as  to  drive  the  blood  forwards  in  the  ventral  vessels, 
backwards  in  the  dorsal  ones.  Below  the  hind  end  of  the  pharynx 
there  is  a  large  sac,  the  sinus  venosus,  into  which  blood  from 
all  parts  of  the  body  is  collected.  From  this  there  proceeds  for- 
wards a  large  endostylar  artery  (truncus  arteriosus  or  ventral  aorta) 


34 


CHORDATE  ORGANIZATION 


II.  8- 


ant.  card- 


d.  cuv. 


>m 


d  ao: 


post,  card' 


d.ao. 


from  which  spring  vessels  carrying  blood  up  the  branchial  arches. 
At  the  base  of  each  primary  bar  there  is  a  little  bulb,  functioning  as 

a  branchial  heart.  From  the  gill  bars 
blood  is  collected  into  paired  dorsal 
aortae,  which  join  behind  the  pha- 
rynx. From  the  paired  and  median 
aortae  blood  is  carried  to  the  system 
of  lacunae  that  supplies  the  tissues. 
There  are  no  true  capillaries.  From 
the  lacunae  blood  is  collected  into 
veins,  the  most  important  of  which 
are  the  caudals,  cardinals,  and  a 
plexus  on  the  gut.  The  cardinals  are 
a  pair  of  vessels  in  the  dorsal  wall  of 
the  coelom,  and  they  collect  blood 
from  the  muscles  and  body  wall. 
They  lead  to  the  sinus  venosus  by 
a  pair  of  vessels,  ductus  Cuvieri, 
which  pass  ventrally  and  across  the 
coelom  to  join  the  sinus  venosus  on 
the  floor  of  the  gut.  The  caudal 
veins  join  the  plexus  on  the  gut, 
from  which  blood  is  collected  by 
a  large  subintestinal  vein  running 
on  to  the  liver;  from  here  another 
plexus  leads  to  the  sinus  venosus. 

Contractions  arise  independently 
in  the  sinus  venosus,  branchial 
bulbs,  subintestinal  vein,  and  else- 
where. The  rhythms  are  very  slow 
(once  in  two  minutes),  irregular, 
and  apparently  not  coordinated  by 
any  control  system. 

The  blood  is  colourless  and  is  not 
known  to  contain  any  respiratory 
pigment.  It  contains  no  cells.  Pre- 
sumably the  tension  of  dissolved 
oxygen  acquired  by  simple  solution 
is  sufficient  for  the  small  energy  needs  of  the  animal,  wrhich  spends 
most  of  its  life  at  rest.  It  is  by  no  means  certain  that  any  oxygenation 
of  the  blood  takes  place  in  the  gills.  Orton  has  suggested  that  since 


'subuit 


^ 


Fig. 


i  i.  Diagram  of  the  circulation  of 
amphioxus. 

aff.d.  afferent  vessel  of  diverticulum;  ant. 
card,  anterior  cardinal  vein;  br.a.  bran- 
chial arch;  d.ao.  dorsal  aorta;  d.cuv.  ductus 
Cuvieri;  eff.d.  efferent  vessel  of  diver- 
ticulum; post. card,  posterior  cardinal 
vein;  sin.  sinus  venosus;  subint.  subin- 
testinal vein;  v. a.  ventral  aorta.  (After 
Grobben  and  Zarnik.) 


II.  Q 


EXCRETION  OF  AMPHIOXUS 


35 


these,  through  their  cilia,  do  much  of  the  work  of  the  body,  the 
blood  actually  leaves  the  gills  less  rich  in  oxygen  that  when  it  enters 
them.  Oxygenation  probably  takes  place  chiefly  in  the  lacunae  close 
to  the  skin,  perhaps  especially  those  of  the  metapleural  folds. 

9.  Excretory  system  of  amphioxus 

One  of  the  most  mysterious  features  about  the  organization  of 
amphioxus  is  that  there  are  flame-cells,  comparable  with  those  found 


Fig.  12.  Solenocytes  of  amphioxus,  showing  the  nuclei,  long  flagella,  and  the  openings 
into  the  main  excretory  canal,  which  leads  to  the  atrium.  (After  Goodrich.) 

in  platyhelmia,  molluscs,  and  annelids.  The  excretory  organs,  there- 
fore, do  not  conform  to  the  basic  chordate  plan,  and  are  in  fact  very 
different  from  those  not  only  of  all  other  chordates  but  also  from  any 
found  in  the  remote  invertebrate  allies  of  the  chordates  which,  as  we 
shall  presently  see,  include  the  echinoderms,  brachiopods,  and  polyzoa. 
The  nephridia  lie  above  the  pharynx.  To  each  primary  gill  bar 
there  corresponds  a  sac,  opening  by  a  pore  to  the  atrium  and  studded 
with  numerous  elongated  flame-cells  (solenocytes)  (Fig.  12).  These 


36  CHORDATE  ORGANIZATION  n.  9- 

flame-cells  do  not  open  internally,  but  are  in  close  contact  with  special 
blood-vessels  (glomeruli)  whose  walls  separate  the  flame-cells  from 
the  coelomic  epithelium.  Assuming  that  there  are  200  of  these  nephri- 
dia,  each  with  500  solenocytes  50  \x  long,  Goodrich,  who  has  provided 
the  most  accurate  information  about  these  organs,  shows  that  the  total 
length  available  for  excretion  is  no  less  than  5  metres.  It  is  assumed 
that  excretion  takes  place  by  diffusion  through  the  flame-cell  wall,  the 
liquid  being  driven  down  the  tube  by  cilia.  Coloured  particles  injected 
into  the  blood-stream  are  not  excreted  by  the  nephridia. 

In  development  these  remarkable  organs  arise  from  groups  of  cells 
close  to  the  meeting-place  of  ectoderm  and  endoderm;  almost  cer- 
tainly they  are  derived  from  the  former.  They  have  no  relation  what- 
ever to  the  mesoderm  and  this  fact  alone  sufficiently  indicates  that 
they  are  in  no  way  comparable  to  the  pronephros  of  vertebrates,  as  is 
sometimes  stated.  There  is  no  organ  in  vertebrates  with  which  they 
can  be  compared,  nor  is  there  any  trace  in  amphioxus  of  organs  com- 
parable to  the  vertebrate  kidney  system.  In  fact  we  have  here  a 
remarkable  case  of  an  isolated  feature;  evidently  separate  items  of  the 
genotype  may  vary  independently,  and  the  whole  bodily  organization 
does  not  necessarily  change  together. 

The  brown  funnels  are  blind  sacs  at  the  front  of  the  atrium, 
invaginating  into  the  epibranchial  coelom.  They  are  probably  receptor 
organs.  Some  parts  of  the  atrial  wall  may  perform  excretory  functions. 
Masses  of  cells  in  the  atrial  floor,  the  atrial  glands,  contain  granules 
that  may  be  excretory  but  may  have  been  taken  up  from  the  food 
current. 

In  the  gonads,  especially  the  testes,  there  are  large  yellow  masses, 
containing  uric  acid,  which  are  extruded  with  the  gametes. 

10.  Nervous  system 

Amphioxus  possesses  a  hollow  dorsal  nerve-cord  similar  to  that  of 
vertebrates.  Though  this  is  somewhat  modified  at  the  front  end,  it  is 
not  there  enlarged  into  an  elaborate  brain.  The  nervous  system  is  con- 
nected with  the  periphery  by  a  remarkably  simple  set  of  nerve-roots, 
a  dorsal  and  a  ventral  on  each  side  in  each  segment.  The  roots  do  not 
join  (Fig.  13):  the  ventral  roots  lie  opposite  the  myotomes,  to  which 
they  carry  motor-fibres,  and  these  end  on  the  muscle-fibres  with 
motor  end-plates.  The  dorsal  root  runs  out  between  the  myotomes 
and  carries  all  the  afferent  fibres  of  the  segment  and  motor-fibres  for 
the  non-myotomal  muscles  of  the  ventral  part  of  the  body.  This  is  the 
fundamental  pattern  of  the  roots  in  all  vertebrates. 


NERVOUS   SYSTEM  OF  AMPHIOXUS 

d.n. 


37 


v.n. 


Fig.  13a.  Nerve-cord  of  amphioxus. 
d.n.  dorsal  nerve-root;  g.  'giant'  nerve-fibres;  v.n.  ventral  nerve-root.  (After  Retzius.) 


Ret 


rec 


v.m.c 


s.m  c 


median  giant  fibre 

Fig.  13ft.  Stereogram  illustrating  the  structure  of  the  spinal  cord  in  an  adult  amphioxus. 

The  receptor  system  is  made  up  of  a  more  or  less  continuous  column  of  bipolar  cells  of 
Retzius  (Ret.),  together  with  smaller  cells  of  various  types  (rec).  According  to  Johnston 
these  receptor  cells  (1,2  and  3)  can  be  regarded  as  equivalent  to  the  dorsal  root  ganglion 
cells  of  vertebrates.  The  other  type  of  receptor  cell  is  the  giant  Rohde  cell  (Roh.),  which  has 
a  large  axon  and  elaborate  dendritic  system.  It  is  probable  that  at  least  some  of  these  cells 
possess  a  peripheral  axon  running  in  the  dorsal  root.  I.e.  longitudinal  connective  cell. 

The  visceral  motor  cells  (v.m.c.)  are  arranged  segmentally,  one  per  segment. 

The  somatic  motor  cells  (s.m.c.)  lie  at  a  different  level  in  the  cord  from  the  ventral 
roots. 

Other  cells  in  the  cord  are  internuncials  of  various  types.  (After  Bone.) 

The  fibres  of  the  peripheral  nerves  differ  from  those  of  vertebrates 
in  that  they  have  no  thick  myelin  sheath  that  will  blacken  with 
osmium  tetroxide.  The  nerve  trunks  are  surrounded  by  an  epineurium 
with  connective  tissue  cells  but  there  seem  to  be  no  Schwann  cells 
accompanying  the  nerve-fibres  (Bone,  1958). 


38 


CHORDATE  ORGANIZATION 


The  afferent  fibres  of  the  dorsal  roots  are  unique  among  chordates 
in  that  the  cell  bodies  are  not  collected  into  spinal  ganglia  but  mostly 
lie  within  the  central  nervous  system.  At  least  three  types  of  central 
neuron  send  fibres  that  terminate  as  free  nerve  endings  in  the  skin.  In 
addition,  on  the  head  and  tail  there  are  peripheral  receptor  cells, 
sending  fibres  centrally,  also  complicated  encapsulated  organs  in  the 
metapleural  folds  (Bone,  i960).  There  are  numerous  large  multipolar 
nerve-cells,  presumably  afferent,  just  beneath  the  atrial  epithelium. 


5  cut. 


bucc.  ep 


Fig.  14.  Sagittal  section  through  the  front  end  of  amphioxus. 
bucc.ep.    buccal    epithelium;    cer.    cerebral    vesicle,    with    large    nerve-cells;    ep.    epidermis; 
my.  myotome;  n.  notochord;  p.  pigment  spot;  s.cut.  subcutis;  vent,  ventricle  of  cerebral  vesicle. 

(After  Krause.) 

These  cells  have  many  branched  dendrites  and  an  axon  that  runs 
through  a  dorsal  root  to  the  spinal  cord.  Their  status  is  discussed  on 

P-33- 

The  spinal  cord  has  only  a  narrow  lumen  and  its  elements  are 

arranged  as  in  vertebrates,  namely,  ependyma  close  to  the  canal,  cell 
layer  ('grey  matter'),  and  outer  fibrous  layer  ('white  matter').  The  cells 
are  not  arranged  clearly  in  horns  as  they  are  in  vertebrates.  The  most 
conspicuous  cells  are  the  giant  cells,  which  lie  dorsally  in  the  anterior 
and  posterior  parts  but  are  absent  from  about  the  13th  to  39th  seg- 
ments. Each  of  these  cells  has  many  dendrites,  branching  in  the  region 
of  entry  of  the  dorsal  root  fibres,  and  a  single  axon,  which  runs  back- 
wards in  the  front  part  of  the  body,  forwards  in  the  hind,  passing  in 
each  case  for  the  whole  length  of  the  cord.  A  median  giant  fibre, 
which  runs  ventrally  for  the  length  of  the  cord,  lies  close  to  the 
viscero-motor  cells  that  probably  produce  the  'coughing'  movements 
of  the  atrium  (p.  33). 


II.    IO 


RECEPTORS   OF  AMPHIOXUS 


39 


Ten  Cate  has  investigated  the  movements  of  amphioxus  and  found 
that  it  responds  to  all  stimuli  by  movements  of  'flight'.  There  are  no 
isolated  or  local  movements;  the  effect  of  any  stimulus  such  as  touch 
on  the  side  of  the  body  is  to  produce  waves  of  myotomal  contraction. 
These  may,  however,  vary  from  strong  waves  going  the  whole  length 


g-ep. 


s.ep. 


p.sp. 


B 


n.pr.    o.c.  t.po.h 


Fig.  15.  Diagram  of  (a)  the  anterior  end  of  the  nervous 
system   of  amphioxus   and   (b)   the   brain   of  a   fish 
(Polypterus). 

A.  Amphioxus.  g.ep.  granulated  ependyma  in  the  wall  of  the  'dorsal 
central  canal';  i.o.  infundibular  organ;  p.sp.  pigment  spot;  r.f. 
Reissner's  fibre  in  the  central  canal;  s.ep.  sensory  epithelium, 
u.  Polypterus,  a.c.  anterior  commissure;  aq.s.  aqueductus  Sylvii;  cer. 
cerebellum;  ep.  epiphysis;  m.  medulla  spinalis;  n.h.  neurohypophysis; 
n.pr.  nucleus  praeopticus;  o.c.  optic  chiasma;  r.f.  Reissner's  fibre  in 
fourth  ventricle;  s.c.o.  subcommissural  organ;  s.d.  saccus  dorsalis; 
s.v.  saccus  vasculosus  with  primary  sense  cells;  t.po.h.  tractus  praeop- 
tico-hypophyseus.   (After  Olson  and  Wingstrand.) 


of  the  body  to  single  rapid  twitches.  The  giant  cells  participate  in  the 
spread  of  these  waves.  It  seems  likely  that  the  arrangement  ensures 
that  touch  on  the  anterior  part  of  the  body,  normally  exposed  when 
feeding,  produces  backward  movement  (i.e.  withdrawal  into  the  sand) 
but  touch  on  the  hind  part  the  reverse  movement  of  emergence  and 
escape. 

At  the  front  end  the  central  canal  is  enlarged  to  form  a  cerebral 
vesicle  (Fig.  14).  The  whole  neural  tube  is  hardly  wider  here  than  in 
the  region  of  the  spinal  cord  and  there  is  no  thickening  of  the  walls, 


40  CHORDATE  ORGANIZATION  n.  10- 

which  are  indeed  mostly  formed  of  a  single  layer  of  ciliated  epithelial 
cells  (Fig.  15).  This  is  a  striking  indication  of  the  lack  of  cephalization 
of  the  animal.  From  the  region  of  the  cerebral  vesicle  spring  the  first 
two  dorsal  roots,  to  which  there  are  no  corresponding  ventrals.  These 
roots  carry  impulses  from  the  receptors  of  the  oral  hood  and  its 
tentacles. 

A  B  C 

Ifls  jT^o*~r$5fc 


Fig.  16.  Diagram  to  show  the  direction  of  the  eye-spots  of  amphioxus. 
A,  anterior,  B,  middle,  and  c,  posterior  regions  of  the  body.  The  eyes  are  shown  as  if  seen  from 
behind.  D  shows  the  direction  of  spiralling  of  the  animal  when  swimming — as  seen  from  in  front. 

(After  Franz.) 

The  infundibular  organ  (Fig.  15)  is  composed  of  tall  cells  with  long 
cilia,  which  beat  in  the  opposite  direction  to  those  of  the  rest  of  the 
vesicle.  From  them  fibres  run  backwards  down  the  cord.  The  organ 
is  also  the  site  of  origin  of  Reissner's  fibre  (Fig.  15).  This  is  a  thread 
of  non-cellular  material,  present  in  all  vertebrates  at  the  centre  of  the 
neural  canal.  It  is  secreted  at  the  front  end  and  then  passed  backwards 
and  is  often  collected  and  absorbed  in  a  sac  at  the  hind  end  of  the 
spinal  cord.  In  vertebrates  it  arises  from  secretory  ependymal  cells  of 
the  subcommissural  organ,  lying  dorsally  in  the  diencephalon  (Fig. 
1 5).  The  infundibular  organ  of  amphioxus  is  clearly  not  exactly  similar, 
yet  the  Reissner's  fibres  are  clearly  comparable ;  an  interesting  problem 
in  homology. 

A  further  complication  is  that  the  cells  of  the  infundibular  organ 
contain  material  that  stains  with  the  Gomori  method,  and  is  similar  to 
the  neurosecretory  material  found  in  the  fibres  of  the  hypophysial  tract 
(Fig.  15).  The  organ  thus  seems  to  occupy  a  central  position  in  the 
control  system  as  a  receptor,  originator  of  nerve-fibres,  and  of  two 
sorts  of  secretion.  There  is  clearly  much  to  be  learned  from  this  about 
the  origin  and  significance  of  the  control  systems  of  the  diencephalon. 

In  young  stages  the  cerebral  vesicle  opens  by  an  anterior  neuro- 
pore,  and  at  the  point  where  the  closure  takes  place  there  develops  a 
depression  of  the  skin,  lined  by  special  epithelium,  and  known  as 
Kolliker's  pit.  It  is  said  to  receive  no  special  innervation.  The  cells 
at  the  front  end  of  the  cerebral  vesicle  contain  pigment  and  there  have 


ii.  ii  RECEPTORS  OF  AMPHIOXUS  41 

been  attempts  to  show  that  this  represents  an  eye.  More  probably 
it  serves  to  prevent  rather  than  to  receive  photic  stimulation;  there 
are  other  cells  lying  in  the  spinal  cord  that  are  clearly  photoreceptors 
(Fig.  9).  In  the  front  part  of  the  body  these  are  unprotected  by  pig- 
ment, whereas  more  posteriorly  they  are  so  pigmented  as  to  be  pro- 
tected asymmetrically  from  the  light  (Fig.  16).  This  asymmetry  may 
be  connected  with  the  fact  that  when  swimming  free  in  the  water 
amphioxus  moves  spirally  about  its  axis,  turning  clockwise  as  seen 
from  behind.  It  was  established  by  Parker  that  a  small  beam  of  light 
produces  movements  of  amphioxus  only  when  it  is  directed  on  to  the 
region  of  the  body  or  tail,  not  when  it  shines  on  the  head.  Since  the 
animal  normally  lies  with  the  head  protruding  we  may  suppose  that 
the  pigment  spot  serves  to  prevent  light  that  strikes  down  vertically 
from  stimulating  the  photoreceptors  in  the  cord. 

Amphioxus  is  therefore  provided  with  receptor  and  motor  systems 
that  serve  to  keep  it  in  its  sedentary  position,  able  to  collect  food  from 
the  current  that  it  makes  by  the  cilia  (p.  33).  There  are  mechanisms 
that  help  it  to  make  appropriate  movements  of  escape  when  it  is 
touched  or  when  the  body  (but  not  head)  is  illuminated.  The  touch 
receptors  of  the  buccal  cirri  produce  rejection  of  large  particles  and 
those  of  the  velum  are  chemo-receptors.  The  infundibular  organ  may 
be  some  form  of  gravity  or  pressure  receptor.  By  means  of  these 
receptor  organs  and  its  simple  movements  of  swimming,  burrowing, 
and  closing  the  oral  hood,  the  animal  is  maintained,  probably  mainly 
by  trial  and  error  (phobotactic)  behaviour,  in  an  environment  suitable 
for  its  life.  There  are  none  of  those  elaborate  mechanisms  that  we  find 
in  higher  chordates  for  'seeking'  special  environments  or  for  so 
'handling'  or  managing  them  that  they  may  prove  habitable  by  the 
animal.  Amphioxus  must  take  and  leave  the  world  very  much  as  it 
finds  it.  The  'correct'  environment  is  chosen  for  it  by  the  selective 
settling  of  the  larvae. 

1 1 .  Gonads  and  development  of  amphioxus 

The  gonads  of  amphioxus  are  hollow  segmental  sacs  with  no  com- 
mon duct.  Each  sac  develops  from  mesoderm  cells,  perhaps  originally 
from  a  single  cell,  at  the  base  of  the  myotomes  in  the  branchial  region, 
the  genital  cells  themselves  developing  on  the  walls  (Fig.  6).  The  sexes 
are  separate  and  the  genital  products  are  shed  by  dehiscence  into  the 
atrium,  the  aperture  by  which  they  escape  closing  and  the  gonad 
developing  afresh. 

Extrusion  of  the  gametes  occurs  in  spring,  on  warm  evenings 


42 


CHORDATE  ORGANIZATION 


following  stormy  weather.  Fertilization  is  external  and  development 
then  occurs  free  in  the  water.  Numerous  eggs  are  produced  and  they  are 
small  but  yolky.  Complex  flowing  movements  take  place  in  them  after 
fertilization,  and  cleavage  is  then  rapid  and  complete,  producing  a 
blastula  composed  of  a  dome  of  somewhat  smaller  and  a  floor  of  rather 
larger  cells  (Fig.  17).  These  latter  then  invaginate  to  make  the  archen- 
teron,  opening  by  a  wide  blastopore,  which  later  becomes  the  anus. 
At  about  this  stage  the  gastrula  becomes  covered  with  flagella,  by 
which  it  rotates  within  the  egg  case. 


Fig.  17.  Three  stages  in  the  development  of  amphioxus  as  seen  in  stained 

preparations. 
a,  the  blastula;  b,  early,  and  C,  later  gastrula. 

The  creature  now  elongates  and  its  dorsal  side  flattens  and  eventu- 
ally sinks  in  to  form  the  neural  tube  (Fig.  18  a).  At  about  this  time 
the  dorsal  side  of  the  inner  layer  begins  to  fold  near  to  the  front  end, 
in  such  a  way  as  to  make  a  pair  of  lateral  pouches.  The  walls  of  these 
pouches  are  the  future  mesoderm  and  the  cavity  is  the  coelom.  As  in 
other  early  chordates,  therefore,  the  coelom  is  continuous  at  first 
with  the  archenteron.  The  roof  of  the  archenteron  also  arches  up 
dorsally  and  forms  the  notochord,  the  gut  wall  being  completed  by  the 
approximation  of  the  edges  of  the  remaining  portion  of  the  inner 
layer,  which  is  now  the  definitive  gut  wall  or  endoderm. 

The  analysis  of  the  processes  of  development  now  enables  us  to  say 
something  of  the  forces  by  which  these  formative  foldings  and  cell 
movements  are  produced.  The  formation  of  the  neural  tube,  meso- 
derm and  notochord  and  the  completion  of  the  gut  roof  all  involve  an 
upward  movement  of  cells  towards  the  mid-dorsal  line.  This  process 
of  'convergence'  is  a  very  marked  feature  of  the  development  of  all 
chordates  (Young,  1957,  p.  609). 

As  the  animal  elongates,  further  mesodermal  pouches  are  produced, 
each  separating  completely  from  the  endoderm  and  from  its  neigh- 


II.  II 


DEVELOPMENT  OF  AMPHIOXUS 


43 


bours.  The  cells  of  each  pouch  push  down  ventrally  on  either  side  of 
the  gut,  the  outer  ones  applying  themselves  to  the  body  wall  to  form 
the  somatopleure,  the  inner  to  the  gut  wall  as  splanchnopleure  (Fig. 
1 8  d).  The  inner  wall  of  the  mesoderm  on  either  side  of  the  nerve- 
cord  thickens  to  form  the  myotome,  and  a  tongue  of  cells  growing  up 
between  this  and  the  nerve-cord  forms  the  sheaths  of  the  latter  and 


lOOfJL 


my  coel. 


som.pl. 


A  B  C  D 

Fig.  i 8.  Further  stages  in  the  development  of  amphioxus  as  seen  in  transverse 

sections. 
A,  stage  of  three  somites;  B,  six  somites;  c,  nine  somites;  D,  eleven  somites,  arch,  archenteron; 
coel.  coelom;  tries,  mesoderm;  my.  myotome;  my. coel.  myocoele;  n.  notochord;  n.c.  nerve-cord; 
som.pl.  somatopleure;  spl.pl.  splanchnopleure;  spl.coel.  splanchnic  coelom.  (After  Hatschek.) 


neurp. 


g.  ioo  u. 

Fig.  19.  Young  amphioxus,  soon  after  hatching. 
g.  gut;  «.  notochord;  n.c.  nerve-cord;  nenr.c.  neurenteric  canal;  neur.p.  neuropore. 

probably  also  the  fin-ray  boxes  and  other  'mesenchymal'  tissues.  The 
upper  part  of  the  coelomic  cavity,  the  myocoele,  becomes  separated 
from  the  ventral  splanchnocoele.  Whereas  the  former  becomes  almost 
completely  obliterated,  the  latter  expands  to  form  the  adult  coelom, 
the  cavities  between  the  adjacent  sacs  breaking  down. 

While  this  differentiation  of  the  mesoderm  has  been  proceeding  the 
animal  has  elongated  into  a  definitely  fish-like  form.  The  neural  tube 
is  a  small  dorsal  canal,  opening  by  an  anterior  neuropore  and  con- 
tinuous behind  through  a  neurenteric  canal  with  the  gut  (Fig.  19). 
The  larva  hatches  when  only  two  segments  have  been  formed  and 
swims  at  the  sea  surface  by  means  of  its  ciliated  epidermis,  turning  on 
its  axis  from  right  to  left  as  it  proceeds  with  the  front  end  forwards. 

The  mouth  now  appears  as  a  circular  opening  and  then  moves 
over  to  the  left  side  and  becomes  very  large.  From  this  time  onward 
the  whole   development   is  markedly  asymmetrical,   presumably   in 


44 


CHORDATE  ORGANIZATION 


ii.  ii 


connexion  with  the  spiral  movement  and  method  of  feeding.  The  first 
gill-slit  also  forms  near  the  midline  but  moves  up  on  to  the  right  side 
(Fig.  20).  At  about  the  same  time  the  right  side  of  the  pharyngeal  wall 
develops  into  a  V-shaped  thickening,  the  endostyle.  Behind  this  there 
forms  a  tube,  the  club-shaped  gland,  joining  the  pharynx  to  the 
outside  and  formed  by  the  closure  of  a  groove  in  the  side  of  the 
pharynx.  The  significance  of  this  organ  is  still  obscure ;  it  is  presum- 
ably connected  with  the  feeding  process,  which  begins  at  this  stage. 
It  has  been  thought  to  represent  a  gill-slit. 


Fig.  20.  Larval  amphioxus  before  metamorphosis. 

an.  anus;  c.s.g.  club-shaped  gland;  end.  endostyle;  g.  gill-slits  lying  on  right 

side,  which  will  later  move  over  to  the  left.  H.p.  Hatschek's  pit  (left  first 

coelomic  sac);  m.  lower  edge  of  mouth,  lying  on  left  side;  n.  notochord; 

p.  pigment  spot. 


The  first  two  coelomic  pouches  differentiate,  asymmetrically,  at 
this  time.  That  on  the  right  becomes  the  coelomic  cavity  of  the  head 
region,  while  the  left  one  acquires  an  opening  to  the  exterior  and  a 
heavily  ciliated  surface.  This  is  perhaps  also  connected  with  the  feed- 
ing-systems and  becomes  developed  into  Hatschek's  pit  of  the  adult. 
Its  interest  to  the  morphologist  lies  in  the  fact  that  the  first  coelomic 
cavity  opens  to  the  exterior  in  other  early  chordates  and  in  some 
vertebrates  (p.  206).  The  pit  has  thus  some  claim  to  be  considered  the 
equivalent  of  the  hypophyseal  portion  of  the  pituitary  gland. 

Further  gill-slits  develop  in  the  mid-ventral  line  and  move  over  on 
to  the  right  side  until  fourteen  have  been  so  formed.  Meanwhile,  a 
further  row  of  eight  slits  appears  above  that  already  formed.  These  are 
the  definitive  slits  of  the  right  side  and  presently  the  larva  proceeds  to 
become  symmetrical  by  movement  of  eight  of  the  first  row  of  slits 
over  to  the  left  side,  the  remainder  disappearing.  At  this  'critical 


ii.  ii  LARVA  OF  AMPHIOXUS  45 

stage'  with  eight  pairs  of  slits  the  larva  pauses  for  some  time  before 
further  changes.  It  is  interesting  that  this  is  the  time  at  which  it  most 
nearly  represents  what  might  have  been  an  ancestral  craniate,  with 
eight  branchial  arches  (p.  145).  Further  slits  are  then  gradually  added 
in  pairs  on  both  sides.  Each  slit  becomes  subdivided,  soon  after  its 
formation,  by  the  downgrowth  of  a  tongue  bar.  The  atrium  is  absent 
from  the  early  larva.  Metapleural  folds  then  appear  on  either  side  and 
are  united  from  behind  forwards  to  form  a  tube  below  the  pharynx. 
During  the  later  stages  of  development  the  larva  sinks  and  finally  rests 
on  the  bottom  while  undergoing  the  migration  of  gill-slits  that  con- 
stitutes its  metamorphosis.  In  other  species  the  larva  remains  longer 
in  the  plankton,  becoming  large  and  even  showing  quite  large  gonad 
rudiments.  These  were  at  first  thought  to  be  adults  of  a  new  genus 
(Amphioxides). 

The  development  of  amphioxus,  like  its  adult  organization,  shows 
us  many  features  of  the  plan  that  is  typical  of  all  chordates  and  was 
presumably  present  in  the  earliest  of  them.  Thus  the  cleavage,  in- 
vagination, and  mesoderm  formation  recall  those  of  echinoderms  and 
other  forms  similar  to  the  ancestors  of  the  chordates,  and  also  show  a 
pattern  from  which  all  later  chordate  development  can  be  derived. 
Unfortunately  we  cannot  pursue  this  study  as  far  as  we  should  like 
because  of  the  difficulty  of  investigating  the  development  of  am- 
phioxus. Modern  embryologists  aim  at  tracing  the  morphogenetic 
movements  by  which  the  organism  is  built,  and  ultimately  at  dis- 
covering the  forces  responsible  for  these  processes.  We  still  remain 
ignorant  of  the  details  of  these  morphogenetic  movements,  and  can 
only  guess  that  the  system  of  cell  activities  by  which  an  amphioxus 
is  built  represents  quite  closely  the  original  set  of  morphogenetic 
processes  of  vertebrates  (Young,  1957,  p.  633). 

There  are,  of  course,  some  special  features  connected  with  the 
method  of  life  of  the  larva,  and  especially  with  its  asymmetry.  The 
strange  sequence  of  gill  formation,  the  immense  left-sided  larval 
mouth,  perhaps  the  club-shaped  gland,  and  Miiller's  organ,  may  show 
considerable  modifications  of  relatively  recent  date.  However,  the 
earliest  chordates  probably  fed  by  means  of  cilia  and  were  planktonic, 
so  we  must  not  too  hastily  assume  that  even  these  asymmetrical  features 
are  novelties. 

The  division  of  the  mesoderm  of  amphioxus  into  a  series  of  sacs 
presents  an  interesting  problem.  The  segmentation  of  the  mesoderm 
of  vertebrates  is  restricted  to  the  dorsal  region.  In  the  lowest  chord- 
ates (see  p.  51),  as  in  their  pre-chordate  ancestors,  there  are  three 


46  CHORDATE  ORGANIZATION  n.  11-12 

coelomic  cavities,  but  it  is  probable  that  the  many  segments  of  verte- 
brates arose  in  order  to  provide  a  set  of  muscles  able  to  contract  in  a 
serial  manner  for  the  purpose  of  swimming.  Their  segmentation  would 
thus  be  a  relatively  late  development,  not  related  to  the  segmentation 
of  annelids,  which  divides  the  whole  body  into  rings.  Accordingly  the 
ventral  part  of  the  vertebrate  coelom  usually  remains  unsegmented. 
But  in  amphioxus  (and  in  the  lamprey)  it  is  subdivided  from  its  first 
appearance  and  only  becomes  continuous  later.  The  best  interpreta- 
tion of  this  condition  is  to  suppose  that  in  order  to  provide  a  series  of 
myotomes  a  rhythmic  process  subdividing  the  mesoderm  was  adopted. 
In  its  earliest  stages  this  affected  the  whole  mesoderm,  ventral  as  well 
as  dorsal,  but  later  became  restricted  to  the  dorsal  region.  New 
morphogenetic  processes  may  often  pass  through  stages  of  refinement 
and  simplification  in  such  ways. 

12.  Amphioxus  as  a  generalized  chordate 

Amphioxus  provides  us,  then,  with  a  valuable  example  of  a  chordate 
that  retains  the  habit  of  ciliary  feeding,  which  was  probably  that  of  the 
earliest  ancestors  of  our  phylum.  No  doubt  in  connexion  with  this, 
and  the  bottom-living  habit,  there  are  many  specializations;  the 
enormously  developed  pharynx  with  its  atrium,  the  asymmetry,  and 
so  on;  but  the  general  arrangement  of  the  body  is  almost  diagram- 
matically  simple,  and  it  may  well  be  that  amphioxus  shows  us  a  stage 
very  like  that  through  which  the  ancestors  of  the  craniates  evolved. 
Perhaps  next  the  larva  remained  longer  in  the  plankton  and  became 
mature  there.  The  Amphioxides  larvae  show  signs  of  such  a  change. 

This  might  give  rise  to  a  suspicion  that  amphioxus  is  not  an 
ancestral  type  but  a  simplified  derivative  of  the  vertebrates,  perhaps 
a  paedomorphic  form.  It  possesses,  however,  sufficient  peculiar 
features  to  make  this  view  unlikely.  Neoteny  might  explain  the 
regular  segmentation,  separate  dorsal  and  ventral  roots,  and  other 
features,  but  can  hardly  account  for  the  method  of  obtaining  food, 
for  the  condition  of  the  skin,  or  for  the  presence  of  nephridia.  It  may 
be,  therefore,  that  amphioxus  shows  us  approximately  the  condition 
of  the  early  fish-like  chordates,  living  in  the  Silurian  some  400  million 
years  ago,  and  that  it  has  undergone  relatively  little  change  in  all  the 
time  since. 


Ill 

THE  ORIGIN  OF  CHORDATES  FROM  FILTER 
FEEDING  ANIMALS 

1 .  Invertebrate  relatives  of  the  chordates 

We  have  seen  in  the  organization  of  amphioxus  the  plan  of  chordate 
structure  as  it  may  have  existed  in  Palaeozoic  times.  Before  proceeding 
to  discuss  the  later  forms  that  evolved  from  animals  of  this  sort  we  may 
first  look  yet  farther  backwards  to  discuss  the  origin  of  the  whole 
chordate  phylum  from  still  earlier  ancestors.  The  great  difficulty  of 
such  an  inquiry  is  itself  a  stimulus  and  a  challenge.  Typical  fish-like 
chordates  were  undoubtedly  established  by  the  Ordovician  period, 
but  we  have  no  good  fossil  record  of  their  earliest  form  and  this  must 
therefore  be  deduced  from  study  of  amphioxus  and  later  animals.  No 
fossils  that  suggest  chordate  affinities  have  been  found  in  the  still 
earlier  rocks.  There  are,  however,  certain  strange  animals  alive  today 
which,  though  not  of  fish-like  type,  show  undoubted  relationship  with 
our  group.  These  might,  of  course,  be  degenerate  offshoots  from  later 
periods,  but  careful  comparison  suggests  that  they  have  been  separa- 
ted for  a  very  long  time  and  provide  us  with  relics  of  some  of  the  early 
stages  of  our  history. 

The  first  step  in  our  inquiry,  however,  before  discussing  these 
forms,  should  be  to  find  out,  if  possible,  which  of  the  main  lines  of 
invertebrate  animals  shows  the  closest  affinity  with  the  chordates. 
Almost  every  phylum  in  the  animal  kingdom  has  been  suggested, 
including  the  nemertines.  Many  still  suppose  that  the  annelids  and 
arthropods,  because  of  their  metameric  segmentation,  are  related  to 
the  chordates,  but  closer  examination  shows  that  the  similarities  are 
superficial.  The  segmentation  of  these  annulate  animals  is  an  almost 
complete  division  of  the  whole  body  into  rings,  and  all  the  organ 
systems  are  affected  by  it  to  some  extent.  In  chordates  only  the  dorsal 
myotomal  region  is  segmented;  even  the  mesoderm  is  not  divided  in 
its  ventral  region  in  most  animals.  Moreover,  the  whole  orientation 
of  the  body  differs  in  the  two  groups.  The  vertebrate  nerve-cord  is 
dorsal  to  the  gut,  in  annulates  the  nerve-cord  is  below  and  the  'brain' 
above.  The  blood  circulates  in  opposite  directions,  the  limbs  are 
based  on  quite  different  plans,  and  so  on.  Attempts  have  been  made 
to  get  over  these  difficulties  by  turning  the  invertebrate  upside  down! 
Patten  and  Gaskell  carried  such  theories  to  extremes  and  tried  to 


48  ORIGIN  OF  CHORDATES  in.  i 

show  a  relationship  of  chordates  with  the  eurypterids,  heavily  ar- 
moured arachnids  of  the  Cambrian  and  Silurian.  These  animals  show 
a  certain  superficial  resemblance  to  some  early  fossil  fishes,  the  cepha- 
laspids  of  the  Devonian  (Fig.  83),  and  these  workers,  with  great 
ingenuity,  claimed  to  find  in  them  evidence  of  the  presence  of  many 
chordate  organs. 

The  safest  evidence  of  affinity  is  a  similarity  of  developmental  pro- 
cesses :  animals  that  develop  very  differently  are  unlikely  to  be  closely 
related.  The  development  of  modern  annulates  is  utterly  different 
from  that  of  chordates.  The  cleavage  by  which  the  fertilized  egg  is 
divided  into  blastomeres  follows  in  annulates  a  'spiral'  plan,  in  which 
every  blastomere  arises  in  a  regular  way  and  the  future  fate  of  each 
can  be  exactly  stated.  In  later  annulates,  such  as  the  arthropods,  this 
plan  is  complicated  by  the  presence  of  much  yolk,  but  even  in  these 
animals  the  cleavage  does  not  resemble  that  of  chordates,  which  is 
radial  or  'irregular',  the  cells  not  forming  any  special  pattern.  This 
characteristic  has  been  used  to  divide  the  whole  animal  kingdom  into 
two  major  groups,  Spiralia  and  Irregularia. 

The  next  stage  of  development,  gastrulation,  by  which  the  ball  of 
cells  is  converted  into  a  two-layered  creature,  also  occurs  very  differ- 
ently in  the  two  groups.  Our  knowledge  of  the  mechanics  of  the  pro- 
cesses by  which  this  change  is  produced  is  still  imperfect,  in  spite  of 
recent  advances,  but  in  lower  chordates  it  occurs  by  invagination,  the 
folding  in  of  one  side  of  the  ball  of  cells  to  form  an  archenteric  cavity 
communicating  with  the  exterior.  In  annulates  this  is  never  seen; 
the  cells  that  will  go  to  form  the  gut  migrate  inwards  either  at  one 
pole  or  all  round  the  sphere  and  only  later  form  themselves  into  a 
tube,  which  comes  to  open  secondarily  to  the  outside.  It  is  probable 
that  when  we  know  more  of  the  forces  by  which  the  gastrulation  is 
produced  the  difference  will  appear  even  more  marked  than  it  does 
from  this  crude  and  formal  statement  that  gastrulation  in  chordates  is 
by  invagination,  in  annulates  by  immigration. 

The  same  applies  to  the  method  by  which  the  mesoderm  and  coelom 
are  formed.  In  lower  chordates  the  third  layer  is  produced  by  separa- 
tion from  the  endoderm,  so  that  the  coelom  is  continuous  with  the 
archenteron  and  is  said  to  be  an  enterocoele.  In  annulates  cells 
separate  in  various  ways  to  form  the  mesoderm  and  a  coelom  then 
arises  within  this  solid  mass  as  a  schizocoele.  It  is  true  that  in  some, 
indeed  many,  of  the  higher  chordates  the  coelom  is  never  continuous 
with  the  archenteron,  but  its  method  of  development  shows  it  to  be 
a  modified  enterocoele. 


in.  i  INVERTEBRATE  RELATIVES  OF  CHORDATES         49 

In  all  these  points  of  development  the  chordates  differ  from  the 
annulates,  but  resemble  the  echinoderms  and  their  allies.  Further 
features  support  this  latter  relationship.  One  of  the  most  important 
of  these  is  that  the  echinoderm-like  animals,  and  some  of  the  early 
chordates,  have  a  larva  with  longitudinal  ciliated  bands,  very  different 
from  the  trochophore  larva,  in  which  the  bands  run  transversely 
round  the  body,  which  is  found  in  the  other  line  of  animals.  The 
nervous  system  of  annulates  consists  of  a  set  of  ganglionated  cords, 
whereas  in  echinoderm-like  animals  it  is  a  diffuse  sheet  of  cells  and 
fibres  below  the  epidermis.  The  nerve-cord  of  the  chordates  can  be 
derived  from  the  latter  but  not  easily  from  the  former  condition. 
Many  further  points  could  be  cited,  for  instance,  the  presence  of  a 
mesodermal  skeleton  in  both  chordates  and  echinoderms,  but  not  in 
annulates.  It  may  be  that  there  are  also  fundamental  biochemical 
differences.  Most  of  the  spirally  cleaving  types  of  animal  conduct  their 
energy  transfers  with  arginine  phosphate,  whereas  vertebrates, 
amphioxus,  ascidians,  and  ophiuroid  echinoderms  use  creatine  phos- 
phate. Balanoglossus  and  echinoids  have  both. 

In  the  study  of  evolution  it  is  not  sufficient  merely  to  make  formal 
comparisons,  we  must  try  to  find  out  and  compare  the  plan  of  develop- 
ment and  structure  common  to  all  members  of  two  groups,  a  technique 
often  requiring  great  knowledge  and  good  sense.  When  this  is  done  in 
the  present  case  it  will  be  found  that  the  essential  plan  of  development 
of  annulates  involves  spiral  cleavage,  gastrulation  by  immigration, 
and  a  coelom  formed  as  a  schizocoele,  a  trochophore-like  larva,  and 
full  segmentation  of  the  mesoderm.  It  is  exceedingly  unlikely  that 
such  animals  have  given  rise  to  chordates  with  their  very  different 
development,  which  we  may  crudely  define  as  showing  radial  cleavage, 
gastrulation  by  invagination,  and  larva  of  echinoderm  type. 

Extending  this  method  we  may  divide  the  whole  world  of  Metazoa 
by  similar  criteria  into  Spiralia  or  Polymera  and  Irregularia  or  Oligo- 
mera.  The  former  include  besides  the  annulates  the  molluscs  and 
platyhelmia,  whereas  the  latter  group  contains,  in  addition  to  the 
chordates,  the  echinoderms,  brachiopods,  polyzoa  (ectoprocta),  grap- 
tolites,  pogonophora,  and  Phoronis.  The  animals  in  this  latter  group 
seem  at  first  sight  to  be  very  different  from  the  chordates  in  outward 
form,  but  the  farther  we  look  into  their  fundamental  organization,  the 
more  we  become  convinced  that  the  ancestors  of  the  fish-like  animals 
are  to  be  found  here.  By  study  of  the  relics  of  the  early  chordates  it  is 
possible  to  trace  the  history  of  this  strange  change  with  some  plausi- 
bility, though  its  full  details  will  probably  never  be  known. 


5Q 


ORIGIN  OF  CHORDATES 


III.  2 


2.  Subphylum  Hemichordata  (=  Stomochordata) 

Class  i.  Enteropneusta 

Balanoglossus ;  Glossobalanus ;  Ptychodera;  Saccoglossus 
Class  2.  Pterobranchia 

Cephalodiscus ;  Rhabdopleura 


Fig.  21.  Balanoglossus,  removed  from  its  tube  and  seen  from  the  dorsal  side. 
abd.  abdomen;  atr.  atrium;  an.  anus;  c.  collar;  h.c.  hepatic  caeca;  p.  proboscis;  ph.  pharynx. 

(From  van  der  Horst.) 


Fig.  22.  Balanoglossus  in  its  tube  in  the  sand.  (After  Stiasny.) 

In  the  Hemichordata  are  placed  animals  of  two  types,  the  worm- 
like Balanoglossus  and  its  allies  (Enteropneusta)  and  two  sedentary 
animals,  Cephalodiscus  and  Rhabdopleura  (Pterobranchia).  The  Entero- 
pneusta are  mostly  burrowing  animals  (Figs.  21  and  22)  varying  in 
different  species  from  2  cm  to  over  2  metres  long.  Several  genera  are 
recognized  (e.g.  Balanoglossus,  Saccoglossus,  Ptychodera)  and  they 
occur  in  all  seas.  Saccoglossus  occurs  around  the  British  coast.  The 
body  is  soft,  without  rigid  skeletal  structures,  and  divided  into 
proboscis,  collar,  and  trunk.  The  animals  are  very  fragile  and  it  is 
difficult  to  collect  specimens  in  which  the  hind  part  of  the  trunk 


III.  2 


MOVEMENT  OF  BALANOGLOSSUS 


5i 


('abdomen')  is  intact.  The  proboscis,  collar,  and  trunk  each  contain 
a  coelomic  cavity,  and  the  coeloms  of  the  proboscis  and  collar  are 
distensible  by  intake  of  water  through  a  single  proboscis  pore  and 
paired  collar  pores.  The  skin  is  richly  ciliated  all  over  the  body.  The 
outer  epithelium  is  thus  unlike  the  squamous,  layered  skin  of  higher 
forms  (Fig.  23).  It  contains  numerous  gland-cells,  whose  secretion 
is  very  copious,  so  that  the  animals  are  always  covered  with  slime. 


neur.s 


Fig.  23.  Section  of  the  epidermis  of  an  enteropneust. 
h.m.  basement  membrane;  ep.  epidermal  cell;  gl.  I  and  2,  different  types  of  gland  cell; 
neur.  neuron;  neur.s.  neuro-sensory  cell;  n.g.p.  process  of  epidermal  cell  acting  as  neuro- 
glia in  the  nerve  net.  (After  Bullock,  v.  der  Horst  and  Grasse.) 

A  characteristic  feature  is  an  unpleasant  smell,  resembling  that  of 
iodoform,  which  possibly  serves,  like  the  mucus,  as  a  protection. 

Below  the  skin  is  a  nerve  plexus  receiving  the  inner  processes  of 
receptor  cells  and  containing  ganglion  cells  (Fig.  23).  Deep  to  this  are 
muscles  running  in  various  directions.  It  is  said  that  the  animal  moves 
by  first  pushing  the  proboscis  and  collar  forward  through  the  sand 
and  then  drawing  the  body  after  it.  Protrusion  of  the  proboscis  can- 
not, however,  be  very  vigorous.  It  may  perhaps  be  produced  by  ciliary 
action  distending  the  coelom  as  is  usually  stated — more  probably  by 
circular  muscles,  but  these  are  weak.  Numerous  longitudinal  muscles 
are  present,  however,  in  the  proboscis  and  trunk  and  are  partly 
attached  to  a  plate  of  skeletal  tissue  in  the  collar.  This  tissue  is 
attached  to  the  ventral  side  of  a  forwardly  directed  diverticulum  of 
the  pharynx.  The  wall  of  this  is  thick,  composed  of  vacuolated  cells, 
and  bears  a  certain  resemblance  to  a  notochord  (Fig.  24).  A  notochord 
extending  throughout  the  length  of  the  body  would  clearly  be  dis- 
advantageous for  an  animal  whose  main  movements  are  lengthening 


52 


ORIGIN  OF  CHORDATES 


and  shortening.  It  is  possible  that  the  diverticulum  and  plate  found 
in  the  collar  represent  the  remains  of  a  notochord,  serving  as  a 
fixed  point  by  which  the  body  is  drawn  forward  on  to  the  proboscis. 
However,  many  prefer  to  call  it  a  'stomochord'  to  avoid  too  close  a 


card. 


Fig.  24.  Diagrammatic  section  of  front  end  of  Balanoglossus. 
c.  collar  coelom  ;  card.s.  sac  around  heart ;  div.  pharyngeal  diverticulum  ('stomochord') ;  dn 
dorsal  nerve-root ;  dv.  dorsal  vessel ;  gl.  glomerulus ;  £s.  gill-slit ;  Im.  longitudinal  muscles  of 
proboscis ;  n.c.  nerve-cord ;  p.p.  proboscis  pore ;  sk.  skeletal  plate.  (Modified  after  Spengel.) 

comparison  with  the  notochord.  The  external  cilia  probably  play  a 
considerable  part  in  locomotion;  possibly  they  are  the  chief  burrowing 
organs,  the  muscles  serving  mainly  to  perform  escape  movements. 

The  mouth  lies  in  a  groove  between  the  proboscis  and  collar  (Fig. 
25).  The  proboscis  contains  many  mucus-secreting  cells  and  the  food 
particles  are  captured  on  its  surface  and  conveyed  by  ciliary  currents 
to  the  mouth.  In  the  anterior  part  of  the  trunk  there  is  a  wide  pharynx, 
opening  by  a  series  of  gill-slits  (Figs.  24,  26).  These  resemble  the 
gills  of  amphioxus  in  the  presence  of  a  supporting  skeleton  in  the  gill 
bars;  there  are  also  tongue  bars  dividing  the  slits  from  above,  and 


III.  2 


FEEDING 


53 


Fig.  25.  Feeding-currents  on  proboscis  of  Glossobalanus,  shown  by  placing  the  animal 

in  water  containing  carmine  particles.  The  particles  (gra.)  are  either  taken  directly  into 

the  mouth  (?«.)  as  at  w.,  or  are  caught  up  in  strands  of  mucus  (sec.)  and  passed  backwards. 

(From  Barrington,  Quart.  J.  Micr.  Set.  82,  by  permission.) 


Fig.  26.  Transverse  section  of  the  pharynx  of  Glossobalanus. 

cil.  cilia  of  the  gill  bars;  dc.  dorsal  chamber  of  pharynx;  es.  epibranchial  strip;  gp.  gill  pore; 
VC.  ventral  chamber  of  pharynx.  (From  Barrington.  With  permission  as  for  Fig.  25.) 


horizontal  synapticulae  strengthening  the  gill  arches.  The  slits  open 
in  some  species  into  an  atrium  formed  by  lateral  folds,  usually  turned 
upwards  to  leave  a  long  mid-dorsal  opening.  In  some  species  each 
slit  opens  to  a  gill  pouch.  The  whole  branchial  apparatus  perhaps 


54 


ORIGIN  OF  CHORDATES 


III.  2 


assists  in  the  process  of  feeding,  probably  by  serving  to  filter  off  the 
excess  water  from  the  material  already  collected  on  the  proboscis, 
which  often  consists  of  large  amounts  of  sand  or  mud.  Relative  to  the 
size  of  the  animal  the  pharynx  is  less  extensive  than  in  amphioxus, 
presumably  because  ciliary  surfaces  are  provided  on  the  outside  and 
also  large  masses  of  sand  are  forced  into  the  mouth  during  locomotion. 
There  is  no  endostylar  apparatus,  but  the  ventral  part  of  the  pharynx 
is  often  partly  separated  from  the  rest  (Fig.  26).  Along  this  groove  the 
matter  ingested  is  passed  to  a  straight  oesophagus  and  intestine  open- 
ing by  a  terminal  anus.  There  is  no  true  tail  in  the  adult  but  a  post- 
anal region  is  present  in  some  species  during  development.  Numerous 


v'.v.  ph. 

Fig.  27.  Diagram  of  the  blood  system  of  Balanoglossus. 

col.  collar;  d.v.  dorsal  vessel;  glom.  glomerulus;  hp.  hepatic  caeca;  m.  mouth;  not.  'notochord'; 
p.  proboscis;  ph.  pharynx;  v.v.  ventral  vessel.  (After  Bronn.) 

hepatic  caeca  in  the  anterior  part  of  the  intestine  can  be  seen  from  the 
outside  as  folds  of  the  body  wall,  often  highly  coloured. 

The  blood  system  consists  of  a  complex  set  of  haemocoelic  spaces, 
communicating  with  large  dorsal  and  ventral  vessels  (Fig.  27). 
The  former  enlarges  into  a  sinus  anteriorly  and  this  is  partly  sur- 
rounded by  the  wall  of  a  pericardial  cavity,  which  contains  muscles 
and  may  be  said  to  be  the  heart,  though  clearly  lying  in  a  very  different 
position  from  that  of  other  chordates.  From  the  sinus,  vessels  proceed 
to  the  proboscis  and  round  the  pharynx  to  the  ventral  vessel.  The 
blood  is  said  to  move  forwards  in  the  dorsal  and  backwards  in  the 
ventral  vessels.  The  front  of  the  sinus  forms  a  series  of  glomeruli, 
covered  by  a  region  of  the  proboscis  coelom  specialized  to  form 
excretory  cells,  the  nephrocytes,  some  of  which  drop  off  into  the 
coelom.  The  blood  is  red  in  some  species  but  usually  colourless.  It 
contains  a  few  amoebocytes. 

The  nervous  system  is  one  of  the  most  interesting  features  of 
Enteropneusta.  It  resembles  that  of  echinoderms  in  consisting  of  a 
sheet  of  nerve-fibres  and  cells  lying  beneath  the  epidermis  all  over  the 
body  (Fig.  23).  This  sheet  is  thick  in  the  mid-dorsal  and  mid-ventral 


BEHAVIOUR  OF  BALANOGLOSSUS 


55 


lines,  and  in  the  dorsal  part  of  the  collar  region  it  is  rolled  up  as  a 
hollow  neural  tube,  open  at  both  ends  (Fig.  24).  These  unmistakable 
resemblances  not  only  to  the  uncentralized  sub-epithelial  plexus  of 
echinoderms  but  also  to  the  hollow  dorsal  nerve-cord  of  vertebrates 
are  most  instructive,  showing  the  affinity  of  the  groups  and  the  origin 
of  the  general  plan  of  the  vertebrate  nervous  system.  There  are  no 
organs  of  special  sense,  unless  this  is 
the  function  of  a  patch  of  special  cili- 
ated cells  on  the  collar.  Receptor  cells 
all  over  the  body  send  their  processes 
into  the  nerve  plexus  (Fig.  23),  on  the 
primitive  plan  of  neurosensory  cells 
found  elsewhere  in  vertebrates  only  in 
the  olfactory  epithelium  and  the  retina. 
The  plexus  is  remarkable  in  receiving 
fibres  from  the  outer  ciliated  epithelial 
cells,  which  thus  represent  the  epen- 
dyma,  the  earliest  form  of  neuroglia 
(Fig.  23).  Nothing  is  known  of  the 
organization  of  pathways  or  of  the 
connexions  with  the  muscles.  The 
collar  nerve-cord  contains  giant  nerve- 
cells  whose  axons  proceed  backwards 
to  the  trunk  and  forward  to  the  pro- 
boscis (Fig.  28).  They  are  probably 
responsible  for  rapid  contractions 
(Knight-Jones,  1951). 

Bullock  has  investigated  the  beha- 
viour of  the  animals  and  found  only 

one  clear-cut  reflex,  namely,  a  contraction  of  the  longitudinal  muscles 
in  response  to  tactile  stimulation.  Isolated  pieces  of  the  body  are  able 
to  show  reflex  responses,  moving  away  from  light  or  tactile  stimuli. 
Such  local  actions  are  an  interesting  sign  of  the  uncentralized  nature 
of  the  nervous  system,  and  similar  actions  are  found  in  echinoderms. 
A  further  sign  of  lack  of  special  conducting  pathways  is  that  stimula- 
tion of  flaps  of  body  wall  partly  severed  from  the  rest  produces 
generalized  contraction,  proving  that  conduction  can  occur  in  all 
directions.  The  dorsal  and  ventral  nerve-cords  do,  however,  act  as 
quick  conduction  pathways,  and  contraction  of  the  trunk  following 
stimulation  of  the  proboscis  is  delayed  or  absent  if  one,  and  especially 
if  both,  cords  have  been  cut. 


Fig.  28.  Diagram  of  certain  tracts  in 
the  nervous  system  of  Balanoglossus . 

com.  circular  connective;  col.coel.  collar 
coelom;  col.n.c.  collar  nerve-cord;  ep.pl. 
nerve  plexus  in  epidermis  of  trunk;  gp. 
gill  pore;  tr.  coel.  trunk  coelom;  tr.n.c. 
trunk  nerve-cord.  (From  Bullock,  J. 
Comp.  Neurol.,  vol.  80,  by  permission.) 


56  ORIGIN  OF  CHORDATES  m.  2 

Perhaps  the  most  interesting  behaviour  observed  was  the  activity 
shown  by  an  isolated  proboscis,  collar,  trunk,  or  portion  of  trunk. 
These  organs  may  move  around  vigorously  in  an  exploratory  manner; 
evidently  the  main  nerve-cords  are  not  necessary  for  the  initiation  of 
action,  as  is  the  central  nervous  system  of  higher  chordates. 

There  are  nerve-fibres  in  the  walls  of  the  pharynx  and  oesophagus, 
where  peristaltic  movements  have  been  observed.  Their  relationship 


an. 

Fig.  29.  Young  tornaria  larva,  seen  from  the  side. 

an.  anus;  ap.  apical  organ;  cb.  longitudinal  ciliated  band;  m.  mouth; 

pb.  posterior  ciliated  band;  pp.  proboscis  pore.  (After  Stiasny.) 

to  the  rest  of  the  nervous  system  is  unknown.  They  may  represent 
the  beginnings  of  an  autonomic  nervous  system. 

The  sexes  are  separate  in  enteropneusts  and  the  gonads  resemble 
those  of  amphioxus  in  being  a  series  of  sacs  developing  from  cells  just 
outside  the  coelom.  These  proliferate  and  bulge  into  the  coelom, 
covered  by  the  somatopleure.  They  acquire  a  cavity  and  each  opens 
by  a  narrow  duct  to  the  exterior,  fertilization  being  external.  The 
development  is  remarkably  like  that  of  echinoderms.  Cleavage  is  holo- 
blastic  and  resembles  that  of  amphioxus  and  ascidians,  gastrulation  is 
by  invagination,  and  the  coelom  is  formed  as  an  enterocoele,  later 
becoming  subdivided  into  proboscis,  collar,  and  trunk  coeloms.  Hatch- 
ing occurs  to  produce  a  pelagic  tornaria  larva,  with  a  ciliated  band  that 
has  exactly  the  relations  found  in  the  dipleurula  larva  of  echinoderms. 
The  band  passes  in  front  of  the  mouth,  down  the  sides  of  the  body, 
and  in  front  of  the  anus  (Fig.  29).  It  then  divides  into  more  dorsal 


III.   2 


DEVELOPMENT  OF  BALANOGLOSSUS 


57 


and  ventral  sections,  exactly  as  in  the  production  of  the  bipinnaria 

larva  of  a  starfish.  This  arrangement  differs  essentially  from  the  rings 

of  cilia  that  pass  round  the  body  in  the  trochophore  larva  found  in  the 

annelids  and  other  spirally  cleaving  forms.  In  later  tornaria  larvae 

there  is,  however,  in  addition  to  the  longitudinal  bands  always  a 

posterior  ring  of  stout  cilia  (telotroch),  and  in  large  oceanic  forms 

(which  may  reach  8  mm  in  length)  the  longitudinal  band  itself  is 

prolonged  into  prominent  tentacle-like  loops  (Fig.  30).  The  cilia  of 

the  posterior  ring  are  purely  locomotive,  while  those  of  the  band  set 

up  feeding-currents  converging  to  the 

mouth.  As  the  larva  becomes  larger  the 

ciliary  surface  needed  for  locomotion 

and  feeding  has  to  increase  relatively 

faster  than  the  increasing  mass  of  the 

body,  the  latter  following  the  cube  but 

the  former  only  the  square  of  the  linear 

dimensions.    Accordingly   the   cilia  of 

the  locomotive  ring  become  broadened 

and  flame-like,  while  the  convolutions 

of  the  longitudinal  (feeding)  band  reach 

fantastic  proportions.    In  some  types, 

however     (Saccoglossus),    the     pelagic 

phase  is  brief  and  the  telotroch  alone 

is  formed. 

Finally  the  larva  sinks,  becomes  con- 
stricted into  three  parts,  and  undergoes  metamorphosis  into  the  worm- 
like adult.  This  development  is  so  like  that  of  an  echinoderm  that  it 
would  be  necessary  to  consider  the  enteropneusts  to  be  related  to 
that  group  even  if  no  other  clues  existed.  Such  close  similarity  in 
the  fundamentals  of  development  cannot  be  due  to  chance. 

These  animals  thus  provide  a  very  remarkable  and  sure  demonstra- 
tion that  the  chordates  are  related  to  the  echinoderms  and  similar 
groups.  The  general  arrangement  of  the  nervous  system  as  a  sub- 
epithelial plexus,  as  well  as  the  whole  course  of  the  development,  show 
the  affinity  with  the  invertebrate  groups,  whereas  the  hollow  dorsal 
nerve-cord  and  the  tongue-barred  gill-slits  are  by  themselves  sufficient 
to  show  affinity  with  the  chordates,  this  affinity  being  also  perhaps 
suggested  by  other  features,  such  as  the  'notochord'.  As  we  have  seen 
already,  affinities  are  not  to  be  determined  by  single  'characters'  but 
by  the  general  pattern  of  organization  of  animals  and  especiallv  that  of 
their  development.  The  organization  of  the  enteropneusts  is  certainly 


Fig. 


30.  Older  tornaria  larva  seen 
from  ventral  surface. 


Letters  as  Fig.  29;  coel.  proboscis 
coelom.  (After  Stiasny.) 


58  ORIGIN  OF  CHORDATES  in.  z- 

highly  specialized  for  their  burrowing  life,  but  showing  through  the 
special  features  we  can  clearly  see  a  plan  that  has  similarity  with  both 
the  echinoderms  and  the  chordates.  The  special  value  of  study  of  these 
animals  is  that  it  proves  decisively  that  an  affinity  between  these 
groups  exists.  Exactly  how  they  are  all  related  is  a  more  speculative 
matter,  which  we  shall  deal  with  later  (see  p.  74). 

3.  Class  Pterobranchia 

These  are  small,  colonial,  marine,  sedentary  animals,  which  show 
some  signs  of  the  general  echinoderm-chordate  plan  of  organization 
we  have  been  discussing.  Cephalodiscus  (Fig.  31)  has  been  found  on  the 
sea  bottom  at  various  depths,  mainly  in  the  southern  hemisphere: 
there  are  several  species.  The  colony  consists  of  a  number  of  zooids 
held  together  in  a  many-chambered  gelatinous  house.  The  zooids  are 
formed  by  a  process  of  budding,  but  do  not  maintain  continuity  with 
each  other.  Each  zooid  has  a  proboscis,  collar,  and  trunk;  there  are 
coeloms  in  each  of  these  parts,  and  proboscis  and  collar  pores.  The 
collar  is  prolonged  into  a  number  of  ciliated  arms,  the  lophophore,  by 
means  of  which  the  animal  feeds.  There  is  a  large  pharynx,  opening 
by  a  single  pair  of  gill-slits,  which  serve  as  an  outlet  for  the  water 
drawn  in  by  the  cilia  of  the  tentacles  for  the  purpose  of  bringing  food. 
The  intestine  is  turned  upon  itself,  so  that  the  anus  opens  near  the 
mouth.  A  thickening  in  the  roof  of  the  pharynx  corresponds  exactly  in 
position  with  the  stomochord  and  contains  vacuolated  cells.  The  blood 
system  consists  of  a  series  of  spaces  arranged  on  a  plan  similar  to  that 
in  Balanoglossus.  There  is  a  dorsal  ganglion  in  the  collar,  but  this  is 
not  hollow.  The  gonads  are  simple  sacs  and  development  takes  place 
in  the  spaces  of  the  gelatinous  house.  Gastrulation  is  by  invagination 
at  least  in  some  species  and  the  coelom  is  formed  as  an  enterocoele. 
The  larva  somewhat  resembles  that  of  ectoproctous  polyzoa,  which 
is  not  closely  similar  to  the  echinoderm  larvae,  but  could  be  derived 
from  the  same  plan. 

Rhabdopleura  occurs  in  various  parts  of  the  world,  including  the 
North  Atlantic  and  northern  part  of  the  North  Sea.  The  zooids  are 
connected  together  and  have  proboscis,  collar,  and  trunk,  ciliated 
arms,  coelomic  spaces  with  pores  (not  'nephridia'  as  is  sometimes 
stated)  and  stomochord,  but  no  gill-slit.  The  development  is  not 
known. 

The  Pterobranchia  thus  show  undoubted  signs  of  the  enteropneust- 
chordate  plan  of  organization  and  provide  also  an  interesting  sug- 
gestion of  possible  affinities  with  Polyzoa,  Brachiopoda,  and  Phoronis. 


in.  3        PTEROBRANCHS  AND  POLYZOANS  59 

Like  the  Pterobranchia  the  Polyzoa  Ectoprocta  are  sessile,  with  mouth 
and  anus  pointing  upwards.  They  feed  by  means  of  the  cilia  borne  on 
a  horseshoe-ring  of  tentacles  (the  lophophore);  but  there  is  no  division 


Fig.  31.  Longitudinal  median  section  of  Cephalodiscus. 

a.  anus;  b.c.  1,  2,  and  3  body  cavities;  int.  intestine;  lo.  lophophore; 

m.  mouth;  nch.  'notochord';  n.s.  nervous  system;   oes.   oesophagus; 

op.  operculum  (collar);  ov.  ovary;  ph.  pharynx;  pp.  proboscis  pore; 

ps.  proboscis;  St.  stomach;  st.k.  stalk. 

(Modified  after  Harmer,  Cambridge  Natural  History,  Macmillan.) 

into  proboscis,  collar,  and  trunk,  and  no  tripartite  coelom.  The  nervous 
system  is  in  the  condition  of  a  sub-epithelial  plexus,  which  is  folded, 
around  the  base  of  the  lophophore,  to  form  a  hollow  tube — a  remark- 
able point  of  similarity  to  the  chordates.  Even  though  it  is  difficult  to 
compare  this  tube  exactly  with  the  nerve-cord  of  chordates,  it  is  at 
least  evidence  of  the  organization  of  the  nervous  system  on  a  plan  that 
allows  of  such  folding.  It  is  probable  that  the  modern  pterobranchs 
are  the  surviving  members  of  the  ancient  group  of  graptolites,  but 


6o 


ORIGIN  OF  CHORDATES 


in.  3- 


mu. 


gen 


these  are  known  only  from  the  skeleton.  The  Pogonophora  may  also 
be  distantly  related,  their  larva  can  be  regarded  as  of  tornaria  type, 
the  coelom  develops  as  in  enteropneusts  and  the  larval  body  shows 
three  parts,  as  does  that  of  the  adult  in  some  species. 

Although  it  would  be  unwise  to 
suggest  close  relationship  between  the 
polyzoans  and  the  pterobranchs,  the 
similarities  are  sufficient  to  suggest  that 
the  chordates  arose  from  sedentary 
creatures,  feeding  by  means  of  ciliated 
tentacles.  The  evidence  is  sufficiently 
strong  to  encourage  us  to  look  for  the 
presence  somewhere  in  the  line  of  verte- 
brate ancestry  of  an  animal  with  this 
habit.  The  difficulties  of  this  view  arise 
when  we  come  to  consider  how  the  fish- 
like organization  of  a  free-swimming 
animal  first  appeared,  a  question  better 
dealt  with  after  consideration  of  the 
tunicates. 

4.  Subphylum  Tunicata.  Sea  squirts 

In  the  adult  ascidians  or  sea  squirts 
there  is  no  obvious  trace  of  the  fish-like 
form  at  all.  The  majority  of  these 
animals  are  sac-like  creatures  living  on 
the  sea  floor  and  obtaining  their  food 
by  ciliary  action.  Often  the  separate 
individuals  are  grouped  together  to  form 
large  colonies,  but  in  Ciona  intestinalis, 
common  in  British  waters,  the  indi- 
viduals occur  separately,  and  this  is  possibly  the  primitive  con- 
dition for  the  group.  The  whole  of  the  outside  of  the  body  is  covered 
by  a  tunic,  in  which  there  are  only  two  openings,  a  terminal  mouth  and 
a  more  or  less  dorsal  atriopore,  both  carried  upon  siphons  (Fig.  32). 
The  tunic  is  made  mainly  of  a  carbohydrate,  tunicin,  closely  related  to 
cellulose,  with  which  is  combined  about  20  per  cent,  of  glycoprotein. 
It  is  secreted  by  the  epidermis  but  contains  special  cells  that  have 
arrived  there  by  migration  from  the  mesoderm.  In  some  tunicates 
calcareous  secretions  of  various  shapes  are  found  in  the  tunic.  The 
mantle  that  lines  the  tunic  is  covered  by  a  single-layered  epidermis. 


Fig.  32.  Diagram  of  structure  of 
Ciona. 

atr.p.  atriopore  ;  e.  endostyle ;  gen.d. 
genital  duct;  h.  heart;  int.  intestine; 
m.  mouth;  mu.  muscle;  oes.  oeso- 
phagus; ph.  pharynx;  st.  stomach. 
(After  Berrill.) 


in.  4 


ORGANIZATION  OF  CIONA 


61 


Ascidians  are  often  brightly  coloured,  the  pigment  being  either  in  the 
tunic  or  the  underlying  body,  which  shows  through  the  transparent 
tunic.  The  colour  can  change,  at  least  over  a  period  of  some  days.  Little 
is  known  about  the  origin  of  the  pigment,  but  it  is  sometimes  derived 
from  the  blood-pigment  and  may  lie  in  pigment  cells. 

The  mantle  is  provided  with  muscle-fibres  running  in  various 
directions  but  mainly  longitudinally,  and  serving  to  draw  the  animal 
together,  with  the  production  of 
the  jet  of  water  from  which  the 
animals     derive     their     common 
English  name. 

The  greater  part  of  the  body  is 
made  up  of  an  immense  pharynx, 
beginning  below  the  mouth  and 
forming  a  sac  reaching  nearly  to 
the  base  (Fig.  32).  The  sac  is 
attached  to  the  mantle  along  one 
side  (ventral)  and  is  surrounded 
dorsally  and  laterally  by  a  cavity — 
the  atrium.  This  pharynx  is,  of 
course,  the  food-collecting  appa- 
ratus ;  its  walls  are  pierced  by  rows 
of  stigmata  (gill-slits)  whose  cilia 
set  up  a  food  current  entering  at 
the  mouth  and  leaving  from  the 
atriopore.  The  entrance  to  the 
pharynx  is  guarded  by  a  ring  of 
tentacles,  which  may  be  compared 

with  the  velum  of  amphioxus.  The  stigmata  are  very  numerous 
vertical  cracks,  all  formed  by  sub-division  of  three  original  gill- 
slits.  Tongue  bars  grow  down  to  divide  each  slit  and  then  from  each 
tongue  bar  grow  horizontal  synapticulae.  This  arrangement  has  clear 
resemblance  to  that  of  amphioxus  and  results  in  the  production 
of  a  pharyngeal  wall  pierced  by  numerous  holes.  Immediately  within 
the  stigmata  there  is  a  series  of  papillae,  provided  with  muscles  and 
cilia.  There  is  an  endostyle,  which  has  three  rows  of  mucus  cells 
on  each  side,  separated  by  rows  of  ciliated  cells  and  with  a  single 
median  set  of  cells  with  very  long  cilia  (Fig.  33).  The  mucus  secreted 
in  the  endostyle  is  caught  up  on  the  papillae,  whose  muscles  move 
them  rhythmically,  spreading  a  curtain  of  mucus  over  the  inside  of 
the  pharynx.  Food  particles  are  caught  in  the  mucus,  which  moves 


Fig.  33.  Transverse  section  of  the  endo- 
style of  Ciona. 

lat.  cil.  lateral  cilia;  med.  cil.  long  median  cilia; 
mu.  mucous  cell.  (After  Sokoloska.) 


6z  ORIGIN  OF  CHORDATES  in.  4 

upwards  and  is  then  passed  back  to  the  oesophagus  by  the  cilia  of  a 
dorsal  lamina  or  of  a  series  of  hook-like  'languets'.  Autoradiographs 
made  from  tunicates  that  have  been  provided  with  isotopes  of  iodine 
show  that  iodination  occurs  in  certain  cells  lying  above  the  glandular 
tracts  of  the  endostyle.  Iodine  is  also  abundant  in  the  tunic,  as  it  is  in 
the  exoskeletal  structures  of  molluscs  and  insects.  When  it  became 
of  metabolic  value  its  production  may  have  become  concentrated  in 
the  pharynx  (see  p.  118). 

The  extensive  ciliated  surface  of  the  pharyngeal  wall  ensures  the 
passage  of  large  volumes  of  water  inwards  at  the  mouth  and  out  at  the 
atriopore.  Rapid  change  of  the  water  is  also  produced  by  periodic 
muscular  contractions  (p.  65).  The  pressure  of  the  exhalant  current  is 
sufficient  to  drive  the  water  that  has  been  used  well  away  from  the 
animal. 

The  oesophagus  leads  to  a  large  'stomach'  with  a  folded  wall  con- 
taining gland-cells,  which  produce  digestive  enzymes.  These  include 
much  amylase,  invertase,  small  amounts  of  lipase,  and  a  protease  of 
the  tryptic  type.  The  organ  is  therefore  not  to  be  compared  with  the 
stomach  of  vertebrates.  A  branching  'pyloric  gland'  opens  into  the 
lower  end  of  the  stomach.  From  the  stomach  a  rather  short  intestine 
leads  upwards  to  open  inside  the  atriopore;  this  is  apparently  the 
absorptive  region  of  the  gut. 

The  heart  lies  below  the  pharynx  and  is  a  sac,  surrounded  by  a 
pericardium  (see  p.  63)  and  communicating  with  a  system  of  blood 
spaces  derived  from  the  blastocoele.  The  larger  of  these  spaces  have 
an  endothelial  lining;  the  biggest  is  a  hypobranchial  vessel  below  the 
endostyle,  from  which  branches  pass  to  the  pharynx.  From  the  oppo- 
site end  of  the  heart  springs  a  large  visceral  vessel  and  others  pass  to 
the  dorsal  side  of  the  pharynx,  tunic,  body  wall,  &c.  The  heart  is 
peculiar  in  that  the  beat  can  proceed  in  either  direction.  After  passing 
blood  into  the  hypobranchial  vessel  and  gills  for  a  few  beats,  its  direc- 
tion reverses,  passing  the  blood  to  the  viscera.  This  reversal  is  pro- 
duced by  the  presence  of  two  pacemaker  centres,  each  capable  of 
initiating  rhythmical  contractions,  one  at  either  end  of  the  heart. 
Stimulation  of  these  by  warming  and  cooling  allows  control  of  the 
reversal  of  the  beat.  There  are  no  capillaries  and  the  blood  system  is 
a  haemocoele.  The  blood-plasma  is  colourless  but  contains  corpuscles, 
some  of  which  are  phagocytes,  while  others  contain  orange,  green,  or 
blue  pigment  (in  different  species).  The  green  and  other  pigments  are 
remarkable  in  that  they  contain  vanadium.  In  some  ascidians  (Molgula) 
some  individuals  contain  vanadium,  others  niobium  (Carlisle,  1958). 


III.  4 


ORGANIZATION  OF  CIONA 


63 


The  vanadocytes  contain  much  sulphuric  acid  and  the  metal  is 
associated  with  a  chain  of  pyrrol  rings.  This  haemovanadin  is  able  to 
reduce  cytochrome  but  it  remains  uncertain  what  part  the  pigment 
plays  in  respiration.  The  blood  turns  blue  in  air  but  cannot  take  up 
more  oxygen  than  can  sea  water. 

The  blood  is  isotonic  with  sea  water,  and  ascidians  appear  to  have 
little  or  no  power  of  regulating  their  osmotic  pressure;  none  of  them 
is  found  in  fresh  water.  They  are  not  even  able  to  colonize  brackish 
waters  or  those  of  low  salinity.  For  example,  they  are  rare  in  the 
Baltic  Sea,  from  which  only  six 
species  have  been  reported.  Only 
one  species,  Molgula  tubifera,  has 
been  reported  from  the  Zuider 
Zee  (salinity  8-4  per  mille). 

A  possible  reason  for  this  in- 
ability to  regulate  the  internal 
composition  is  perhaps  the  need 
to  expose  a  large  surface  to  the 
water.  There  are  no  tubular  ex- 
cretory organs  such  as  could  be 
used  to  maintain  an  osmotic 
gradient.  Ninety-five  per  cent  of 
the  nitrogen  is  excreted  as  am- 
monia. Cells  known  as  nephro- 
cytes  found  in  the  blood  and 
elsewhere  contain  concretions 
within  the  cytoplasm  and  these 
may  in  some  cases  be  stored  in  an  excretory  sac  until  the  animal  dies. 

There  has  been  much  debate  as  to  whether  the  tunicates  possess 
a  coelomic  cavity.  The  heart  develops  from  a  plate  of  cells  arising 
early  from  the  mesoderm  and  lying  between  ectoderm  and  endoderm. 
This  becomes  grooved  and  folded  to  make  the  heart  itself  and  the 
pericardium.  The  irregular  system  of  haemocoelomic  spaces  around 
the  pharynx  and  elsewhere  is  usually  said  to  consist  of  'mesenchyme' 
and  to  be  derived  from  the  blastocoel  and  therefore  not  coelomic,  but 
its  walls  are  mesodermal.  The  situation  is  complicated  by  the  presence 
of  a  pair  of  outpushings  from  the  pharynx,  the  epicardia,  or  perivis- 
ceral sacs,  which  end  blindly  on  either  side  of  the  heart  (Fig.  34). 
Berrill  and  others  have  suggested  that  these  epicardia  may  be  com- 
pared with  coelomic  cavities.  Their  function  in  the  open  condition 
in  which  they  are  found  in  Ciona  is  perhaps  to  allow  sea  water  to 


Fig.   34.   Section  through  base  of  Ciona, 

showing    heart,    fit.,    in    pericardium,    p., 

and  the  epicardia,  e.p.,  opening  into  the 

pharynx,  b.s. 

at.  atrium;  g.  gonad;  int.  intestine. 


64  ORIGIN  OF  CHORDATES  in.  4 

circulate  about  the  heart  and  hence  to  help  excretion  (and  respiration  ?). 
In  other  ascidians  the  epicardium  loses  its  connexion  with  the  pharynx. 
The  closed  sac  functions  in  some  cases  as  an  excretory  organ,  con- 
taining concretions  of  uric  acid,  whereas  in  other  animals  it  becomes 
the  main  source  of  the  cells  that  make  the  asexual  buds. 

The  central  nervous  system  consists  of  a  round,  solid  ganglion 
(Fig.  36),  lying  above  the  front  end  of  the  pharynx.  The  ganglion  has 
a  layer  of  cells  around  the  outside  and  a  central  mass  of  neuropil  and 
is  therefore  quite  unlike  the  nerve-cord  of  a  vertebrate.  From  the 
ganglion  nerves  proceed  to  the  siphons,  other  parts  of  the  mantle, 
muscles,  and  viscera.  Receptor  cells  with  nerve-fibres  ending  around 
the  base  have  been  described,  especially  in  the  siphons.  The  gut  is 
said  to  contain  a  plexus  of  cells  and  fibres,  whose  relation  to  the 
autonomic  system  of  higher  forms  remains  uncertain. 

Movement  consists  mainly  of  contraction  and  closure  of  the  aper- 
tures. Light  touching  of  either  siphon  causes  closure  proportional  to 
the  strength  of  the  stimulus.  Stronger  stimuli  cause  closure  of  both 
siphons  and  if  very  strong  there  is  contraction  of  the  whole  body  and 
ejection  of  the  water  in  the  pharynx  and  atrium.  Stimulation  just 
inside  either  siphon  produces  closure  of  the  other  one  and  also,  if 
strong  enough,  contraction  of  the  body,  ensuring  that  a  jet  of  water 
sweeps  out  the  aperture  that  received  the  stimulus.  These  crossed 
reflexes  depend  upon  the  integrity  of  the  ganglion. 

The  surface  of  the  body  is  sensitive  to  changes  in  light  intensity, 
and  these  are  followed  by  local  or  total  contractions,  according  to  their 
extent.  After  removal  of  the  ganglion  the  wider  reflexes  can  no  longer 
be  obtained  but  local  responses  continue,  suggesting  the  presence  of 
nerve-cells  in  the  body  wall.  Electrical  stimulation  also  provides  evi- 
dence of  this.  One  shock  may  produce  only  a  small  response  but  if  a 
second  shock  follows  shortly  afterwards  there  is  marked  facilitation 
and  a  large  contraction  occurs.  These  responses  are  also  seen  after 
removal  of  the  ganglion.  The  various  parts  of  the  body  are  not  all 
equally  sensitive  to  light,  the  highest  sensitivity  being  in  the  region 
of  the  ganglion.  The  'ocelli'  are  cup-like  collections  of  orange- 
pigmented  cells  around  the  siphons ;  according  to  Hecht  they  are  not 
photoreceptors. 

The  neuromuscular  system  thus  appears  to  function  mainly  as  a 
reflex  apparatus  for  producing  protective  movements  in  response  to 
certain  stimuli.  This  is  the  role  that  might  be  expected  of  it  in  an 
animal  that  remains  fixed  in  one  place.  The  'initiative'  for  food- 
gathering  activities  comes  from  the  continuous  action  of  the  cilia  of 


in.  4  MOVEMENTS  OF  ASCIDIANS  65 

the  pharynx.  The  nervous  system  shows  little  sign  of  those  continuous 
activities  that  produce  the  varied  and  'spontaneous'  acts  of  behaviour 
in  higher  forms.  Nevertheless,  it  would  be  unwise  to  suppose  that  the 
nerves  are  only  activated  by  external  stimuli.  There  are  some  sugges- 
tions that  even  in  these  simple  animals  rhythmical  activities  are 
initiated  from  within.  The  food-collecting  operations  of  the  pharyn- 
geal wall  involve  rhythmical  movement  of  the  papillae  by  their 
muscles.  Further,  in  many  species  of  ascidians  there  are  regular 
contractions  of  the  siphons  and  body  musculature  in  rotation,  with 


Fig.  35.  Rhythmical  'spontaneous'  contractions  of  Styela  shown  by  attaching  levers 

to  the  two  siphons.  Branchial  siphon  above,  atrial  siphon  below.  The  time-marker 

shows  intervals  of  5  minutes.  (From  Yamaguchi.) 

a  frequency  of  8-27  per  hour  (Fig.  35).  These  contractions  are 
especially  marked  when  the  animal  is  in  filtered  water  and  they  may 
be  some  form  of  'hunger'  contraction,  directed  towards  the  obtaining 
of  food.  More  water  is  moved  by  these  contractions  than  by  the  ciliary 
current.  Their  presence  is  a  striking  warning  of  the  dangers  of  assum- 
ing that  even  the  simplest  nervous  system  operates  only  when 
stimulated  from  outside. 

The  neural  gland  is  a  sac  lying  beneath  the  ganglion  and  opening 
by  a  ciliated  funnel  on  the  roof  of  the  pharynx.  It  arises  mainly  from 
the  ectoderm  of  the  larval  nervous  system,  in  part  from  the  pharynx. 
This  double  embryological  origin,  and  its  position,  suggest  that  the 
neural  gland  may  be  compared  with  the  infundibulum  and  hypophysis 
of  vertebrates.  There  is  an  obvious  similarity  with  Hatschek's  pit  of 
amphioxus.  Both  seem  to  be  receptor  organs,  testing  the  water  stream 
and  also  producing  mucus.  The  subneural  gland  has  also  been  held 
to  have  a  similarity  to  the  pituitary  in  that  it  controls  the  release  of 
gametes.  When  eggs  or  sperms  of  the  same  species  are  present  in  the 
water,  signals  from  the  neural  gland  apparently  produce  discharge 
from  the  gonad.  The  pathway  of  the  signals  is  said  to  be  partly  hor- 
monal, partly  nervous.  Discharge  is  produced  by  injection  of  extract  of 


66 


ORIGIN  OF  CHORDATES 


in.  4-5 


neural  gland  or  of  mammalian  gonadotropin,  but  these  act  through  the 
ganglion,  since  they  produce  no  effect  if  the  nerves  leading  from  this 
(and  the  dorsal  strand)  are  cut. 

Further  similarities  with  the  pituitary  have  been  claimed,  such  as 
the  presence  of  vasopressor  and  oxytocic  substances  in  the  subneural 
gland.  However,  oxytocin  is  present  elsewhere  in  the  tunicate  and  in 


Fig.  36.  Longitudinal  section  of  the  ganglion  (g.)  and  subneural  gland 
(s.n.g.)  of  an  ascidian. 

cil.  ciliated  funnel;  d.s.  dorsal  strand;  n.a.  and  n.p.  anterior  and  posterior  nerves; 
ph.  wall  of  pharynx.  (After  L.  Bertin  from  Grasse.) 

any  case  differs  from  that  of  vertebrates.  It  cannot  be  claimed  that  the 
relationship  with  the  pituitary  is  clear,  but  it  seems  likely  that  there 
is  some.  As  in  the  thyroid,  a  pharyngeal  mucus-secreting  organ 
stimulated  by  the  environment  has  evolved  into  a  glycoprotein- 
secreting  endocrine  organ,  controlled  by  substances  reaching  it  in  the 
blood.  (Barrington,  1959,  in  Gorbman,  Symposium  on  Comparative 
Endocrinology.) 

5.  Development  of  ascidians 

Tunicates  are  hermaphrodite,  the  ovary  and  testis  being  sacs  lying 
close  to  the  intestine  and  opening  by  ducts  near  the  atriopore.  Fer- 
tilization is  external  in  the  solitary  forms  but  internal  in  those  that 
form  colonies,  the  development  in  the  latter  taking  place  within  the 
parent.  The  details  of  cleavage  and  gastrulation  show  a  remarkable 
general  similarity  to  those  of  amphioxus.  Indeed,  the  whole  develop- 
ment is  so  strikingly  like  that  of  chordates  that  it  establishes  the 
affinities  of  the  tunicates  far  more  clearly  than  the  vague  indications 


(6?) 


end: 


Fig.  37.  Ascidian  tadpole  of  Clavelina. 


air.   atriopore;  c.   mantle;  cer.v.  cerebral  vesicle;   e.   eye-spot;   end.  endostyle;   ep.   epicardium; 
h.  heart;  m.  mouth;  mu.  muscle-cells;  n.c.  nerve-cord;  not.  notochord;  ot.  otocyst;  St.  stomach; 

sub.n.  subneural  gland. 


r.  C.  b. 


Fig.  37  A.  T.S.  ocellus  of  the  free  swimming  tadpole  stage  of  the  sea  squirt  Ascidia  nigra. 
(Drawing  from  an  electron  micrograph.) 

The  ocellus  is  situated  in  the  posterior  wall  of  the  cerebral  vesicle.  It  consists  of  three  parts,  a  lens 
cell,  a  pigment  cell,  and  a  retina.  The  lens  cell  usually  contains  three  lens  vesicles,  which  are  spheres 
of  cytoplasm  bounded  by  mitochondria.  The  pigment  cell  contains  granules  of  melanin,  which 
protect  the  photoreceptor  from  stray  light.  The  retinal  cells  have  processes  that  penetrate  the 
pigment  cell.  They  are  similar  to  vertebral  rods,  composed  of  a  pile  of  membranes,  closely  applied 

to  the  uaner  edge  of  the  lens  cell. 
a. p.  attachment  plaque,  a  membrane  specialization  thought  to  function  as  an  anchor  of  the  retinal 
cell  process  to  the  pigment  cell  membrane ;  b.m.  basement  membrane,  the  outer  limit  of  the  cerebral 
vesicle;  c.v.  cavity  of  the  cerebral  vesicle;  I.e.  lens  cell;  l.v.  lens  vesicle;  m.  mitochondrion;  p.c. 
pigment  cell;  p.g.  pigment  granule;  p.m.  piled  menbrane  of  photoreceptor  part  of  the  retinal  cell; 
r.c.b.  retinal  cell  body;  r.c.n.  retinal  cell  nucleus;  r.c.p.  retinal  cell  process. 
(From  a  preparation  by  N.  Dilly.) 


68  ORIGIN  OF  CHORDATES  in.  5- 

of  a  chordate  plan  of  organization  seen  in  the  adult.  The  result  of 
development  is  to  produce  a  fish-like  creature,  the  ascidian  tadpole, 
which  is  immediately  recognizable  as  a  chordate  (Fig.  37).  The 
cleavage  is  total  and  produces  a  blastula  with  few  cells,  whose  future 


mus.c. 


atr. 


mus.  c. 


Fig.  38.  The  ascidian  tadpole  (Ascidia  or  Ciona  type).   1.  Tadpole  ready  to  hatch. 
2.  Tadpole.  3.  Sensory  vesicle.  4.  Cross  section  of  tail. 

atr.    atrium;   end.   endostyle;  fol.   follicle   cells;   mus.c.   muscle  cells;   mus.f.  muscle   fibrils; 

n.c.  nerve-cord;  n.m.  nerve  to  tail  muscles;  not.  notochord;  oc.  ocellus;  ot.  otolith;  su.  sticking 

gland;  ves.  sensory  vesicle.  (After  Berrill.) 

potentialities  are  already  determined.  Gastrulation  by  invagination 
follows  and  the  creature  then  proceeds  to  elongate  into  the  fish-like 
larva.  This  possesses  an  oval  'head'  and  long  tail,  the  latter  supported 
by  a  notochord  formed  by  cells  derived  from  the  archenteric  wall. 
Forty  of  these  cells  make  up  the  entire  rod,  becoming  vacuolated  and 
elongated  by  swelling. 

On  either  side  of  this  notochord  run  three  rows  of  muscle-cells, 
eighteen  on  each  side,  derived  from  mesoderm  that  arises  from  yellow- 
pigmented  material  already  visible  in  the  egg  and  later  forming  part 
of  the  wall  of  the  archenteron.  Other  cells  of  this  tissue  migrate 
ventrally  to  make  the  pericardium,  heart,  and  mesenchyme.  The 


in.  6  DEVELOPMENT  OF  ASCIDIANS  69 

muscle-cells  contain  cross-striated  myo-fibrils  at  the  periphery,  these 
being  continuous  from  cell  to  cell. 

The  nervous  system  is  formed  by  folds  essentially  similar  to  those 
of  vertebrates,  making  a  hollow,  dorsal  tube,  extending  into  the  tail 
and  enlarged  in  front  into  a  cerebral  vesicle,  within  which  is  an 
ocellus  and  also  a  unicellular  otolith  (Fig.  37  a).  Nerve-fibres  proceed 
only  to  the  front  end  of  the  rows  of  muscles  and  the  rest  of  the  cord 
contains  no  nerve-cells  or  fibres  (Fig.  38). 

The  larva  takes  no  food  and  the  gut  is  not  well  developed.  There  is 
a  pharynx  with  usually  a  single  pair  of  gill-slits  opening  into  an 
atrium,  which  develops  as  an  ectodermal  inpushing.  Below  or  around 
the  mouth  various  forms  of  sucker  are  formed. 

The  whole  process  of  development  occupies  only  one  or  two  days, 
and  the  larva,  in  the  species  in  which  it  is  set  free,  is  positively  photo- 
tropic  and  negatively  geotropic  and  so  proceeds  to  the  sea  surface. 
But  its  life  here  is  also  limited.  Within  a  day  or  two,  depending  on  the 
conditions,  its  tropisms  reverse  so  that  it  passes  to  the  bottom,  turns 
to  any  dark  place  and  thus  finds  a  suitable  surface.  It  attaches  by  the 
suckers,  loses  its  tail,  develops  a  large  pharynx,  and  grows  into  an  adult 
ascidian.  Presumably  its  short  life  in  the  chordate  stage  is  sufficient 
to  ensure  distribution,  and  the  simple  nervous  system  serves  to  find 
a  place  in  which  to  live. 

In  addition  to  the  sexual  reproduction,  tunicates  have  great  powers 
of  regeneration  and  also  often  multiply  by  budding.  The  bud  consists 
of  an  outer  epicardial,  mesenchymal,  pharyngeal  or  atrial  tissue.  The 
epidermis  develops  only  more  tissue  like  itself  and  all  the  other  tissues 
are  formed  from  the  inner  mass.  This  occurs  by  a  process  of  folding 
to  make  a  central  cavity;  the  nervous  system,  intestine,  and  peri- 
cardium are  then  formed  by  further  foldings.  The  bud  thus  begins  in 
a  condition  comparable  to  a  gastrula  but  develops  directly  into  an 
adult,  without  passing  through  the  tadpole  stages.  The  fact  that  a 
complete  new  animal  is  thus  formed  from  one  or  two  layers  shows 
that  the  separation  into  three  layers  during  development  does  not 
involve  any  fundamental  loss  of  potentialities,  as  would  be  required 
if  the  'germ  layer'  theory  held  rigorously.  The  germinal  tissue  of  the 
bud  is  not  necessarily  derived  from  that  of  the  parent. 

6.  Various  forms  of  tunicate 

Besides  some  2,000  species  of  sessile  tunicates,  about  100  species 
have  become  secondarily  modified  for  a  pelagic  life.  These  pelagic 


70  ORIGIN  OF  CHORDATES  m.  6- 

animals  are  perhaps  all  related,  but  the  whole  subphylum  is  con- 
veniently subdivided  into  three  classes. 
Class  i.  Ascidiacea. 

Typical  bottom-living  forms  such  as  Ciona  (solitary),  Botryllus 
(colonial). 
Class  2.  Thaliacea. 

Pelagic  forms,  simple  or  colonial,  swimming  by  means  of  circular 
muscle  bands.  Salpa,  Doliolum,  Pyrosoma. 
Class  3.  Larvacea. 

Pelagic  tunicata  without  metamorphosis;  the  adult  has  a  tail  and 
resembles  the  tadpole  of  the  other  groups.  Oikopleura. 

7.  Class  Ascidiacea 

The  typical  sessile  ascidians  are  found  in  all  seas.  They  may  be 
divided  into  those  that  live  as  single  individuals  (Ascidiae  simplices) 
and  those  forming  colonies  (Ascidiae  compositae).  Both  types  include 
many  different  forms,  however,  and  the  division  is  not  along  phylo- 
genetic  lines.  The  colonial  forms  produced  by  budding  may  consist 
simply  of  a  number  of  neighbouring  individuals  {Clavelina)  or  of  a 
common  gelatinous  test  in  which  the  individuals  are  embedded 
{Botryllus,  Amaroucium).  The  form  of  the  body  is  related  to  the  type 
of  bottom  upon  which  they  are  found;  there  has  thus  been  an  adap- 
tive radiation  within  the  group;  a  great  variety  of  habitats  is  avail- 
able for  bottom  living  creatures,  and  the  animals  become  adapted 
accordingly. 

Most  of  the  species  live  in  the  littoral  zone,  but  a  few  deep-sea  forms 
are  known,  such  as  Hypobythius  calycodes,  found  below  5,000  metres. 

Many  ascidians  probably  live  only  for  a  short  time,  becoming 
mature  in  their  first  year  and  dying  thereafter.  In  some  species  the 
animals  live  over  a  second  winter,  during  which  they  become  reduced 
in  size,  growing  and  budding  again  in  the  following  spring  (Clavelina). 

8.  Class  Thaliacea 

These  are  pelagic  tunicates  living  in  warm  water.  They  have 
circular  bands  of  muscle,  enabling  the  animal  to  shoot  through  the 
water  by  jet  propulsion.  In  Doliolum  and  its  allies  the  muscle-bands 
pass  right  round  the  body  (Cyclomyaria),  whereas  in  Salpa  the  rings 
are  incomplete  (Hemimyaria).  The  mouth  and  atriopore  are  at 
opposite  ends  of  the  body.  The  tunic  is  thin  and,  like  the  rest  of  the 
body,  transparent. 

The  life-history  of  these  forms  involves  a  remarkable  alternation  of 


PELAGIC  TUN1CATES 


7i 


Fig.  39.  Doliolum,  gonozooid. 

I,  inhalent  aperture;  2,  ciliated  pit;  3,  ganglion  and  nerves;  4,  pharynx;  5,  mantle; 

6,  sense-cells,  7,  exhalant  aperture;  8,  ovary;  9,  intestine;  10,  heart;  11,  endostyle; 

12,  testis;  13,  ciliated  groove.  (After  Neumann.) 


atr 


muse 


ats 


an 


br.s 


Fig.  40.  Cyclosalpa  affinis,  oozooid  with  chain  of  five  wheels  of  blastozooids. 
an.  anus;  atr.  atrium;  at.s.  atrial  siphon;  hi.  blastozooid  with  egg;  br.s.  branchial  siphon;  en.  endo- 
style; gn.  ganglion;  gr.  gill  ridge;  ht.  heart;  muse,  muscle  ring;  ph.  pharynx;  s.  stomach. 
(  X  £  modified.  After  Ritter  and  Johnson  and  Berrill.) 

generations.  In  Doliolum  the  ascidian  tadpole  develops  into  a  mother 
or  nurse  zooid  (oozooid).  This  by  budding  gives  rise  to  a  string  of 
daughter  zooids,  which  it  propels  along  by  its  muscles.  The  daughter 
zooids  are  of  three  types:  (i)  sterile,  nutritive,  and  respiratory  indi- 
viduals, the  trophozooids,  permanently  sessile  on  the  parent;  (2) 
sterile  nurse  forms,  which  are  eventually  set  free  (phorozooids);  (3) 
sexual  forms  (gonozooids,  Fig.  39),  nursed  and  carried  by  the  phoro- 
zooids until  sexually  mature,  when  they  also  break  loose. 

In  Salpa  the  sexual  form  (blastozooid),  produces  only  a  single  egg, 


72  ORIGIN  OF  CHORDATES  in.  8- 

which  develops  within  the  mother  without  passing  through  a  tadpole 
stage,  nourished  by  a  diffusion  placenta,  whose  cells  also  migrate  into 
the  developing  embryo.  This  becomes  the  asexual  oozoid  and  pro- 
duces a  long  chain  of  blastozooids,  which  it  tows  about  until  these 
break  away  by  sections  (Fig.  40). 

The  pelagic  colonial  Pyrosoma  of  warm  seas  consists  of  a  number  of 
individuals  associated  to  form  an  elongated  barrel-shaped  colony. 
The  mouths  open  outwards  and  the  atria  inwards  into  a  single 
cavity  with  a  terminal  outlet  from  which  a  continuous  jet  emerges. 

The  mode  of  budding  from  the  epicardium 
and  other  features  suggest  an  affinity  with 
Doliolum  and  Salpa,  but  Pyrosoma  also 
resembles  the  ascidians  in  that  its  zooids 
are  all  sexual  and  capable  of  budding.  The 
yolky  eggs  develop  within  the  parent, 
without  forming  a  larva.  The  outstanding 
characteristic  of  the  creatures  is  the 
powerful  light  that  they  shine.  This  is 
Fig.  41.   Photogenic  cell  of     produced  in  photogenic  organs  on  each 

Pyrosoma.  (After  Kukenthal.)       r.  r  mi  1 

side  or  the  pharynx.  1  he  photogenic  cells 
contain  curved  inclusions  about  2^  in  diameter  (Fig.  41).  These 
are  considered  by  some  to  be  symbiotic  luminescent  bacteria,  but 
this  is  doubtful.  The  light  is  so  powerful  that  when  large  masses  of 
Pyrosoma  occur  together  the  whole  sea  is  illuminated  sufficiently  to 
allow  of  reading  a  book.  A  remarkable  feature  of  the  phenomenon 
is  that  the  light  is  not  produced  continuously  but  only  when  the  animal 
is  stimulated,  as  by  the  waves  of  a  rough  sea.  If  one  individual  is 
stimulated  others  throughout  the  colony  may  show  their  lights,  but 
the  mechanism  of  this  effect  is  not  known  and  the  groups  of  cells  that 
form  the  luminescent  organs  receive  no  nerves.  Other  types  of  animal 
with  luminescent  bacteria  emit  light  continuously.  The  sudden  flashes 
of  light  probably  serve  as  a  dymantic  reaction  (p.  302),  giving  protec- 
tion against  enemies  by  producing  a  flight-reaction  in  the  same  way 
as  do  sudden  manifestations  of  colour  or  black  spots  by  other  animals. 
It  has  been  observed  in  the  laboratory  that  colonies  of  Pyrosoma  that 
are  dying  and  do  not  light  up  may  be  eaten  by  fishes,  whereas  any 
that  light  up  when  seized  may  then  be  dropped. 

9.  Class  Larvacea 

The  (Appendicularia)  Larvacea  (Figs.  42  and  43)  are  minute  neo- 
tenous  tunicates  that  live  in  the  plankton.  Instead  of  the  test,  each 


ill.  9 


LARVACEA 


73 


Fig.  42.  Oikopleura,  one  of  the  Larvacea,  in  its  house,  showing 

the  feeding-currents. 

e.  exhalant  aperture;  e.e.  'emergency  exit';  f. p.  filter  pipes;  f.tv.  filter 

window;  g.  gill-slit;  m.  mouth;  r.  trough;  ta.  tail.  (After  Garstang; 

this  and  Figs.  44  and  45  by  permission  of  the  Editors  of  the  Quarterly 

Journal  of  Microscopical  Science.) 

individual  builds  a  'house',  by  secretion  from  a  special  part  of  the  skin, 
the  'oikoplastic  epithelium'.  The  tail  is  a  broad  structure  held  at  an 
angle  to  the  rest  of  the  body;  its 
movement  produces  a  current  in 
which  the  food  is  carried  and  caught 
by  a  most  elaborate  filter  arrangement 
ixi  the  house  (Fig.  42).  Water  enters 
the  house  by  a  pair  of  posterior 
'filtering  windows'  and  is  passed 
through  a  system  of  filter  pipes  in  the 
part  of  the  house  in  front  of  the 
mouth.  The  very  minute  flagellates 
of  the  nanonplankton  are  stopped  by 
these  pipes  and  sucked  back  to  the 
mouth.  The  pharynx  has  two  gill-slits, 
also  an  endostyle  and  peripharyngeal 
bands.  The  general  organization  is  that 
of  a  typical  ascidian  tadpole,  and  there 
can  be  no  doubt  that  these  forms  have 
arisen  from  tunicates  by  the  accelera- 
tion of  the  rate  of  development  of  the 
alimentary  organs  and  gonads  so  that 
the  metamorphosis  and  normal  adult 
stage  are  eliminated.  This  may,  of 
course,  have  happened  long  ago,  so 
that   the   modern   Larvacea   are  not     FlG-  «■   Appendicular* t  seen  from 

the  side  and  from  below. 

closely  related  to   any  living  forms,  (After  Lehmann.) 


74  ORIGIN  OF  CHORDATES  in.  9- 

but  the  fact  that  they  differ  in  many  ways  from  known  ascidian 
tadpoles  does  not  invalidate  the  hypothesis;  it  would  be  expected 
that  many  special  features  would  be  developed  during  evolution 
after  the  paedomorphosis.  Garstang,  however,  believed  that  there 
is  sufficient  evidence  to  show  that  the  Larvacea  are  related  to  the 
Doliolidae  and  suggested  an  ingenious  hypothesis  by  which  the  appendi- 
cularian  home  could  be  derived  from  the  doliolid  test,  the  animal 
itself  remaining  attached  at  the  front  end  by  gelatinous  threads,  which 
came  to  make  the  filter  tubes  (Fig.  44). 


Fig.  44.  Sequence  of  stages  by  which  the  Larvacea  may  have 
been  evolved  from  a  doliolid  type. 

A,  Thaliaccan  type  of  individual  in  its  test  (t).  b,  Paedomorphosis  has 
occurred  so  that  a  tailed  creature  is  found  in  the  test;  g.  gill-slit,  c,  The 
tadpole  has  moved  away  from  the  inhalant  aperture,  leaving  a  series 
of  threads  that  become  the  filter  pipes  (/./>.),  the  inhalant  aperture 
becoming  exhalant  and  vice  versa.  (After  Garstang.) 

The  tail  is  a  highly  developed  organ,  serving  for  locomotion,  nutri- 
tion, and  in  the  building  of  the  house.  It  has  a  wide,  continuous  fin 
and  is  supported  by  a  notochord  of  20  cells.  Bands  of  10  large  striped 
muscle-cells  extend  down  each  side,  giving  an  appearance  that  has 
been  compared  with  metameric  segmentation.  The  small  number  of 
the  cells  makes  any  such  comparison  very  difficult.  Moreover,  the 
muscles  are  not  developed  from  anything  resembling  myotomes.  The 
nerve-cord  is  a  hollow  tube  with  ganglionic  thickenings,  each  con- 
taining one  to  four  nerve-cells.  From  these  cells  fibres  proceed  to 
the  muscles  and  to  the  skin  in  a  series  of  roots  that  usually  remain 
separate,  the  motor  being  more  dorsal. 

10.  The  formation  of  the  chordates 

We  can  now  recapitulate  the  points  that  we  have  established  about 
the  origin  of  the  chordates  and  attempt  to  piece  together  the  evidence 
to  show  the  sequence  of  events  that  led  to  the  production  of  a  free- 


in.  10  LARVAL  ANCESTRY  OF  CHORDATES  75 

swimming,  fish-like  animal.  The  chordates  are  related  to  the  echino- 
derms  and  their  allies.  This  is  established  by  the  similarities  in  early 
development  (cleavage,  gastrulation,  mesoderm  formation);  by  the 
presence  in  early  members  of  both  groups  of  three  separate  coelomic 
cavities,  some  with  pores;  by  the  similarity  of  the  larva  of  entero- 
pneusts  to  the  dipleurula,  and  by  other  points  of  general  morphological 
and  biochemical  similarity  between  early  chordates  and  echinoderms, 
especially  the  arrangement  of  the  nervous  system  and  presence  of  a 
mesodermal  skeleton. 

The  echinoderms  we  have  to  consider  are  not  the  modern  star- 
fishes and  sea-urchins,  which  are  relatively  active  animals,  but  their 
sessile  Palaeozoic  ancestors.  These  were  sedentary,  often  stalked 
animals,  the  cystoids,  blastoids,  and  crinoids,  feeding  by  ciliary 
action.  Surviving  animals  of  related  phyla,  such  as  Polyzoa  Ecto- 
procta  and  Phoronis  suggest  that  the  ancestor  for  which  we  are  looking 
may  have  possessed  a  ciliated  lophophore  for  food-collecting.  For 
purposes  of  dispersal  its  life-history  presumably  included  a  larval 
stage  with  a  longitudinal  ciliated  band,  similar  in  plan  to  that  of  the 
auricularia. 

One  might  well  ask  how  such  an  animal  could  possibly  become 
converted  into  a  motile,  metameric  fish,  feeding  with  its  pharynx. 
Yet  the  evidence  of  the  lower  chordates  is  sufficient  to  establish  that 
this  change  has  occurred,  and  even  provides  us  with  an  outline  of  the 
main  stages  in  the  process  of  the  change.  Cephalodiscas,  which  is  in 
some  ways  the  most  primitive  of  surviving  chordates,  with  its  lopho- 
phore also  possesses  gill-slits.  This  suggests  that  the  pharyngeal 
mechanism  was  substituted  for  the  lophophore  as  a  means  of  feeding 
in  the  adult  stage.  There  are  other  possible  interpretations.  It  has 
been  suggested  that  Cephalodiscus  was  derived  from  a  larval  entero- 
pneust  (Burden-Jones).  However,  it  is  possible  that  ciliary  mechanisms 
developed  in  the  pharynx  first  to  deal  with  food  collected  outside  by 
tentacles  or  proboscis.  Later  the  pharynx  became  developed  into  a 
self-contained  feeding  mechanism,  making  unnecessary  the  tentacles, 
which  provide  a  tempting  morsel  for  predators.  The  adoral  band  of 
cilia  of  the  auricularia  probably  serves  to  carry  food  into  the  mouth, 
and  for  this  purpose  it  is  actually  turned  in  to  the  floor  of  the  pharynx. 
Garstang  suggests  that  the  endostyle  has  been  derived  from  this  loop 
of  the  adoral  band. 

The  pharyngeal  method  of  food-collecting  thus  replaced  the  ten- 
tacles in  the  adult  and  the  whole  apparatus  of  an  endostyle  and  an 
atrium  to  protect  the  gills  became  developed.  We  may  notice  here  the 


76 


ORIGIN  OF  CHORDATES 


III.  10 


remarkable  similarity  of  this  arrangement  of  the  pharynx  in  tunicates, 
amphioxus,  and  cyclostome  larvae,  and  the  partial  similarity  in 
Balanoglossus. 

The  tunicates  show  us  a  stage  in  which  branchial  feeding  has  fully 
replaced  tentacle  feeding  in  a  sessile  adult.  But  they  have  a  larva  that 
is  beyond  all  question  a  fish-like  chordate.  If  the  adult  tunicate  has 
evolved  from  a  modified  lophophore-feeding  creature,  how  has  the 


Fig.  45.  To  show  the  method  by  which  a  protochordate  animal  might  have  been 

derived  from  an  echinoderm  larva  such  as  the  auricularia. 

a.  Auricularia  in  side  view;  b.  protochordate  in  side  view;  c.  same,  dorsal  view.  ad.b.  adoral 

band;   an.   anus;   coel.  coelom;   end.   endostyle;  g.  gill-slit;   Lb.   longitudinal  ciliated  band; 

m.  mouth;  n.c.  nerve-cord;  not.  notochord.  (After  Garstang.) 


ascidian  tadpole  arisen  from  the  auricularia  larva  ?  Garstang's  auri- 
cularia theory,  first  propounded  in  1894,  provides  a  possible  answer. 
As  a  ciliated  larva  grows  its  means  of  locomotion  becomes  inadequate 
because  the  ciliated  surface  increases  only  as  the  square  of  the  linear 
dimensions,  the  weight  as  the  cube.  Muscular  locomotion  is  not  sub- 
ject to  this  difficulty,  and  some  of  the  starfish  larvae  actually  show 
flapping  of  the  elongated  processes,  movements  that  presumably 
assist  them  to  remain  at  the  surface.  Garstang  suggests  that  the  fish- 
like form  arose  by  development  of  muscles  along  the  sides  of  the 
elongated  body,  the  ciliated  bands  being  pushed  upwards  and  even- 
tually rolled  up  with  their  underlying  sheets  of  nerve  plexus  to  form 
the  neural  tube.  The  adoral  ciliated  band  might  then  well  be  the 
endostyle  (Fig.  45). 

This  theory  may  seem  at  first  sight  fantastic.  It  is  necessarily 
speculative,  but  it  has  certain  strong  marks  of  inherent  probability.  It 


in.  10  LARVAL  ANCESTRY  OF  CHORDATES  77 

violates  no  established  morphological  principles  and  certainly  enables 
us  to  see  how  a  ciliated  auricularia-like  larva  could  be  converted  by 
progressive  stages  into  a  fish-like  creature  with  muscular  locomotion, 
while  the  adults,  at  first  sedentary,  substituted  gill-slits  and  endostyle 
for  the  original  lophophore.  The  alternative  is  to  suppose  that  the 
ascidian  tadpole  arose  as  a  purely  tunicate  development,  providing 
sufficient  receptor  and  muscular  organs  to  allow  for  the  finding  of 
suitable  sites  on  the  bottom  (Berrill,  1955). 

We  may  plausibly  regard  the  adult  tunicate  organization  as  directly 
derived  from  that  of  sessile  lophophore-feeding  creatures,  and  the 
larval  organization  as  descended  from  an  echinoderm-like  larva. 
There  is  no  need,  on  this  view,  to  regard  the  sessile  adult  tunicate 
as  a  'degenerate'  chordate.  The  problem  that  remains  is  in  fact  not 
'How  have  sea-squirts  been  formed  from  vertebrates  ?'  but  'How  have 
vertebrates  eliminated  the  sea-squirt  stage  from  their  life-history?' 
It  is  wholly  reasonable  to  consider  that  this  has  been  accomplished  by 
paedomorphosis.  Advance  of  the  time  of  development  of  the  gonads 
relative  to  that  of  the  soma  is  well  known  to  occur  in  certain  special 
cases  such  as  the  axolotl.  The  example  of  the  Appendicularia  shows 
that  a  similar  process  can  happen  among  tunicates!  Various  workers 
have  stressed  the  differences  between  the  ascidian  tadpole  and  the 
adult  appendicularian,  in  attempts  to  show  that  the  two  are  not 
comparable.  But  the  differences,  though  considerable,  are  superficial : 
the  similarity  of  organization  is  profound.  Any  sensible  biologist  with 
an  understanding  of  the  way  in  which  the  characteristic  forms  of 
animals  arise  by  change  in  the  rate  and  degree  of  development  of 
features  can  see  how  the  Appendicularia  may  represent  modified 
ascidian  larvae. 

The  appendicularians  do,  indeed,  carry  certain  characters  of  the 
'adult'  sea-squirt,  in  particular  they  have  gill-slits,  though  of  simple 
form.  Nothing  is  more  likely,  however,  than  that  some  features  of  the 
sessile  adult  would  be  adumbrated  in  its  larva  and  capable  of  fuller 
development  therein  if  advantageous.  Larva  and  adult,  it  must  be 
remembered,  possess  the  same  genotype;  the  remarkable  feature  in  all 
animals  with  metamorphosis  is  the  difference  between  the  two  stages, 
not  the  similarity.  Any  characteristic  may  appear  at  either  larval  or 
adult  stage  or  be  transferred  by  evolutionary  selection  from  one  to  the 
other.  There  is  no  serious  objection  to  the  view  that  the  early  adult 
free-swimming  chordates  arose  by  paedomorphosis  of  some  tunicate- 
like  metamorphosing  form.  If  the  creatures  abandoned  the  habit 
of  fixation  it  would  be  possible  for  characters  previously  present 


78  ORIGIN  OF  CHORDATES  in.  10 

separately  in  larva  and  adult  to  become  combined  in  a  single  stage. 
This  is  indeed  what  has  happened  in  the  Appendicularia. 

Strangely  enough,  one  of  the  chief  difficulties  of  this  theory  is  to 
find  the  position  of  the  enteropneusts.  Since  the  larva  is  still  in  the 
ciliated-band  stage  there  should  be  no  sign  of  organs  characteristic  of 
the  muscle-swimming,  fish-like  pro-chordate.  Yet  such  signs  are 
present  in  the  adult  Balanoglossiis;  there  is  a  hollow  nerve-cord  and 
some  sign  of  a  notochord.  These  features  almost  compel  us  to  suppose 
that  the  group  has  at  one  time  possessed  a  free-swimming,  fish-like 
stage.  The  only  escape  from  this  conclusion  would  be  by  supposing 
the  hollow  nerve-tube  to  be  a  case  of  convergence,  for  which  a  parallel 
might  be  cited  in  the  hollow  nervous  system  of  Polyzoa.  But  there  is 
no  clear  reason  why  the  nerve-cord  should  become  rolled  up  in  the 
collar,  and  it  is  easier  to  suppose  it  a  vestige.  This  imposes  two  further 
hypotheses  on  us.  First  that  a  fish-like  stage  once  followed  an  advanced 
ciliated-band  stage  in  ontogeny,  and  secondly  that  this  fish-like  stage 
later  became  adapted  to  a  burrowing  life,  in  fact  that  Balanoglossus  is 
a  'degenerate'  chordate.  Neither  of  these  propositions  is  impossible, 
but  it  must  be  admitted  that  the  position  of  the  enteropneusts  is  not 
clear.  Showing  a  combination  of  ciliated  larva  and  chordate  characters 
they  provide  a  valuable  proof  of  the  affinity  of  chordates  and  echino- 
derm-like  creatures,  but  these  very  chordate  characters  become  an 
embarrassment  when  we  try  to  explain  in  detail  how  they  have  arisen! 

There  is  strong  reason  to  suppose  that  what  we  may  call  the  Bate- 
son-Garstang  theory  of  the  origin  of  chordates  is  correct.  There  is  little 
doubt  that  chordates  are  related  to  the  sessile  lophophore-feeding 
type  of  creature  rather  than  to  any  annulate,  and  we  can  reconstruct 
the  course  of  events  by  which  the  lophophore-feeder  may  have  come 
to  have  a  pharynx  with  gill-slits  and  its  larva  to  have  muscles,  a  noto- 
chord, and  a  nerve-tube.  Then  by  paedomorphosis  the  sessile  stage 
disappeared  and  the  free  chordates  began  their  course  of  evolution. 
There  are  some  reasons  for  supposing  that  a  type  such  as  amphioxus 
could  have  been  derived  from  a  creature  not  distantly  related  to  the 
simpler  Appendicularia  and  this  in  turn  from  a  neotenous  doliolid  or 
some  similar  ancestral  type. 

We  need  not,  however,  follow  the  theory  into  its  details,  which  are 
speculative.  The  whole  treatment  provides  a  conspicuous  example 
of  close  morphological  reasoning,  allied  with  proper  consideration  of 
general  biological  principles,  and  establishes  with  some  probability 
the  main  outlines  of  the  origin  of  our  great  phylum  of  active  creatures 
from  such  humble  sedentary  beginnings. 


80  ORIGIN  OF  CHORDATES  in.  10 

Can  we  see  in  the  production  of  the  first  fish-like  creatures  clear 
signs  of  an  'advance'  in  evolution  ?  In  acquiring  the  power  of  active 
muscular  locomotion  the  animals  became  able  to  live  and  feed  in  a 
variety  of  habitats,  either  at  the  sea  surface  or  on  the  bottom.  Forms 
with  a  sedentary  adult  stage  are  limited  by  the  necessity  for  the 
presence  of  a  sea  bottom  of  suitable  character.  The  larvae  were  evolved 
to  provide  the  information  to  make  sure  of  reaching  such  conditions. 
But  whereas  suitable  situations  on  the  bottom  are  not  common,  and 
are  liable  to  change,  the  sea  surface  provides  a  generalized  habitat  in 
which  there  is  always  abundant  food,  though  no  doubt  also  strenuous 
competition  for  it.  Paedomorphosis  in  this  case,  as  in  others,  allows 
the  race  to  eliminate  from  its  life-history  the  stage  passed  in  a  'special' 
environment,  which  is  difficult  to  find.  Although  the  fish-form  that 
was  thus  produced  proved  to  have  great  possibilities  for  further 
evolution,  the  change  was  not  at  first  a  strikingly  progressive  one. 
The  surface  of  the  sea  is  perhaps  the  most  general  of  all  environments ; 
possibly  it  was  the  seat  of  the  origin  of  life.  Races  that  have  devised 
means  of  living  on  the  sea  bottom  may  therefore  be  said  to  have 
advanced,  because  they  have  invaded  a  more  difficult  habitat.  To 
abandon  the  sedentary  life  might  in  this  sense  be  regarded  as  a  retro- 
grade step.  The  peculiar  feature  of  the  early  fishes,  however,  was  that 
they  developed  powers  of  active  movement  in  a  relatively  large 
organism  provided  with  efficient  receptors,  and  by  making  use  of  the 
feeding  mechanism  developed  at  first  by  the  bottom-living  adult  were 
able  to  live  successfully  at  the  sea  surface.  They  acquired  their 
dominance  at  this  stage  not  by  invading  new  habitats  but  by  develop- 
ing effective  means  of  living  in  the  richly  populated  plankton. 


IV 

THE  VERTEBRATES  WITHOUT  JAWS.  LAMPREYS 

1.  Classification 

Phylum  Chordata 

Subphylum  4.  Vertebrata  (=  Craniata) 
Superclass  1.  Agnatha 
Class  1.  Cyclostomata 
Order  1.  Petromyzontia 

Petromyzon;  Lampetra;  Entosphenus;  Geotria;  Mordacia 
Order  2.  Myxinoidea 
Myxine;  Bdellostoma 

Class  2.  *Osteostraci.  Silurian-Devonian 
*Cephalaspis;  * Tremataspis 

Class  3.  *Anaspida.  Silurian-Devonian 
*Birkenia;  *Ja?noytius 

Class  4.  *Heterostraci.  Ordovician-Devonian 
*Astraspis;  *Pteraspis;  *Drepanaspis 

Class  5.  *Coelolepida.  Silurian-Devonian. 
*Thelodus;  *Lanarkia 

Superclass  2.  Gnathostomata 

2.  General  features  of  vertebrates 

All  the  remaining  chordates  are  alike  in  possessing  some  form  of 
cranium  and  some  trace  of  vertebrae;  they  make  up  the  great  sub- 
phylum  Vertebrata,  also  called  Craniata.  The  organization  of  a  verte- 
brate is  similar  to  that  of  amphioxus,  but  with  the  addition  of  certain 
special  features.  A  few  of  these  novelties  may  now  be  surveyed,  with 
emphasis  on  those  that  provide  the  basis  for  the  capacity  to  live  in 
difficult  environments  that  is  so  characteristic  of  the  vertebrates. 
Firstly  the  front  end  of  the  nervous  system  is  differentiated  into  an 
elaborate  brain,  associated  with  special  receptors,  the  nose,  eye, 
and  ear.  Through  these  receptors  the  vertebrates  are  able  to  respond 
to  more  varied  aspects  of  the  environment  than  are  any  other  animals. 
Some  of  them  have  the  ability  to  discriminate  between  visual  shapes 
and  colours,  and  in  the  auditory  field  between  patterns  of  tones,  also 
between  a  host  of  chemical  substances.  The  motor  organization 
allows  the  performance  of  delicate  movements  to  suit  the  situations 


82  VERTEBRATES  WITHOUT  JAWS  iv.  2- 

that  the  receptors  reveal.  The  swimming  process,  by  the  passage 
of  waves  down  the  body,  is  itself  perfected  by  improvements  in  the 
shape  of  the  fish,  allowing  rapid  movements  and  turns.  Besides  the 
median  fins  there  develop  lateral  paired  ones,  serving  at  first  a 
stabilizing  and  steering  function  and  then  converted,  when  the  land 
animals  arose,  into  organs  of  locomotion  on  the  ground  or  in  the  air 
and  finally,  in  the  shape  of  the  hands,  into  a  means  of  altering  the 
environment  to  suit  the  individual. 

The  brain  itself,  at  first  mostly  devoted  to  the  details  of  sensory 
and  motor  function,  comes  increasingly  to  preside,  as  it  were,  over 
all  the  bodily  functions,  and  to  give  to  the  vertebrates  the  'drive'  that 
is  one  of  their  most  characteristic  features.  The  skull  is  developed  as 
a  skeletal  thickening  around  the  brain,  probably  at  first  mainly  for 
protection,  but  later  serving  for  the  attachment  of  elaborate  muscle 
systems.  The  study  of  vertebrates  is  especially  identified  with  study 
of  the  skull,  because  in  so  many  fossils  this  is  the  only  organ  preserved. 

The  food  of  the  earliest  vertebrates  was  collected  by  ciliary  action, 
but  this  habit  has  long  been  abandoned  and  only  in  rare  cases  today 
does  the  food  consist  of  minute  organisms.  The  pharynx  of  most 
vertebrates  is  small,  there  are  relatively  few  gill-slits  and  these  are 
respiratory.  In  all  except  the  most  ancient  forms  the  more  anterior  of 
the  arches  between  the  gills  became  modified  to  form  jaws,  serving  not 
only  to  seize  and  hold  the  food  but  also  to  'manipulate'  the  environ- 
ment. 

The  blood  system  shows  two  of  the  most  characteristic  vertebrate 
features,  namely,  the  presence  of  a  heart  that  has  at  least  three 
chambers  and  thus  provides  a  rapid  circulation,  and  of  haemoglobin 
within  corpuscles,  serving  to  carry  large  amounts  of  oxygen  to  the 
tissues.  The  efficiency  of  this  system  must  have  been  a  major  factor 
in  producing  the  dominance  of  the  vertebrate  animals.  In  the  air- 
breathing  forms,  and  especially  the  warm-blooded  birds  and  mam- 
mals, the  respiratory  and  circulatory  systems  allow  the  expenditure  of 
great  amounts  of  energy  per  unit  mass  of  animal,  so  that  quite  extra- 
vagant devices  can  be  used,  allowing  survival  under  conditions  that 
would  otherwise  not  support  life. 

The  excretory  system  is  based  on  a  plan  quite  different  from  that 
of  amphioxus.  It  consists  of  mesodermal  funnels,  leading  primarily 
from  the  coelom  to  the  exterior.  It  may  be  that  this  type  of  kidney 
arose  in  connexion  with  the  abandoning  of  the  sea  for  fresh  water. 
Probably  all  but  the  earliest  vertebrates  have  passed  through  a  fresh- 
water stage,  and  it  is  significant  that  all  except  Myxine  have  less  salt  in 


iv.  4  AGNATHA  83 

their  blood  than  there  is  in  sea  water.  Elaborate  devices  for  regulation 
of  osmotic  pressure  have  been  developed,  and  the  mesodermal  kidneys 
play  a  large  part  in  this  regulation. 

This  outline  only  gives  a  few  suggestive  features  of  vertebrate 
organization.  The  details  differ  bewilderingly  in  the  different  types 
and  it  is  our  business  now  to  survey  them.  In  the  earliest  forms  the 
more  special  mechanisms  are  absent  or  at  least  function  only  crudely, 
and  passing  through  the  vertebrate  series  we  find  more  and  more 
devices  adopted,  along  with  more  and  more  delicate  co-ordination 
between  the  various  parts,  culminating  in  the  extremely  highly 
centralized  control  of  almost  every  aspect  of  life  that  is  exercised  by 
the  mammalian  cerebral  cortex. 

3.  Agnatha 

The  earliest  vertebrates,  while  showing  most  of  the  characteristic 
features  of  the  group,  differ  from  the  rest  in  the  absence  of  jaws  and 
are  therefore  grouped  together  in  a  superclass  Agnatha,  distinguished 
from  the  remaining  vertebrates,  which  have  jaws,  and  are  therefore 
called  Gnathostomata.  The  only  living  agnathous  animals  are  the 
Cyclostomata,  lampreys  and  hag-fishes,  but  the  first  vertebrates  to 
appear  in  the  fossil  series,  mostly  heavily  armoured  and  hence  known 
as  'ostracoderms',  found  in  Silurian  and  Devonian  strata,  also  show 
the  agnathous  condition,  and  have  some  other  features  in  common 
with  the  Cyclostomata.  This  group  of  agnathous  vertebrates  shows 
some  interesting  experimentation  in  methods  of  feeding,  before  the 
jaw-method  became  adopted.  The  modern  cyclostomes  are  parasites 
or  scavengers,  in  the  adult  state,  but  as  larvae  the  lampreys  still  feed 
on  microscopic  material,  using  an  endostyle  resembling  that  of 
amphioxus  in  many  ways,  but  making  use  of  muscular  contraction 
rather  than  ciliary  action  to  produce  a  feeding  current.  The  methods 
of  feeding  of  the  Devonian  forms  are  not  known  for  certain,  but 
probably  included  shovelling  detritus  from  the  bottom. 

The  Cyclostomata  are  therefore  worth  special  study  as  likely  to 
show  us  some  of  the  characteristics  possessed  by  the  earliest  vertebrate 
populations. 

4.  Lampreys 

The  most  familiar  cyclostomes  are  the  lampreys,  of  which  there  are 
various  sorts  found  in  the  temperate  zones  of  both  hemispheres.  All 
lampreys  have  a  life-history  that  includes  two  distinct  stages:  the 
ammocoete  larva  lives  in  fresh  water,  buried  in  the  mud,  and  is 


84  VERTEBRATES  WITHOUT  JAWS  iv.  4- 

microphagous:  the  adult  lamprey  has  a  sucking  mouth,  and  usually 
lives  in  the  sea,  where  it  feeds  on  other  fishes.  Lampetra  the  lamprey 
(Fig.  47),  is  a  typical  example,  common  in  Great  Britain.  The  adult 
is  an  eel-like  animal  about  30  cm  long,  black  on  the  back,  and  white 
below.  The  surface  is  smooth,  with  no  scales.  The  skin  is  many- 
layered  (Fig.  48).  The  outermost  cells  have  a  striated  cuticular  border. 
Mixed  with  these  epithelial  cells  the  lamprey,  like  most  aquatic 
vertebrates,  has  many  gland-cells  for  producing  slime.  Below  the 
epidermis  lies  the  dermis,  a  layer  of  bundles  of  collagen  and  elastin 


Fig.  47.  Brook  lampreys,  Lampetra  planer i. 

A,  ripe  female,  with  anal  fin;  B,  ripe  male;  note  shape  of  dorsal  fin  and  presence  of 

copulatory  papilla.  (Curves  due  to  fixation.) 

fibres,  running  mostly  in  a  circular  direction.  This  tissue  is  sharply 
marked  off  from  a  layer  of  subcutaneous  tissue  containing  blood- 
vessels and  fat,  as  well  as  connective  tissue.  There  are  pigment  cells 
in  the  dermis  and  a  thick  layer  of  them  at  the  boundary  of  dermis  and 
subcutaneous  tissue.  The  chromatophores  are  star-shaped  cells  whose 
pigment  is  able  to  migrate,  making  the  animal  dark  or  pale.  This 
change  is  especially  marked  in  the  larva  and  is  produced  by  variation 
in  the  amount  of  a  pituitary  secretion  (p.  107). 

The  head  of  the  lamprey  bears  a  pair  of  eyes  and  a  conspicuous 
round  sucker.  On  the  dorsal  side  is  a  single  nasal  opening,  and  behind 
this  there  is  a  gap  in  the  pigment  layers  of  the  skin  through  which  the 
third  or  pineal  eye  can  be  seen  as  a  yellow  spot.  There  are  seven  pairs 
of  round  gill  openings,  which,  with  the  true  eyes  (and  some  miscount- 
ing or  perhaps  inclusion  of  the  nasal  papilla),  are  responsible  for  the 
familiar  name  'nine  eyes'.  There  is  no  trace  of  any  paired  fins,  but  the 
tail  bears  a  median  fin,  which  is  expanded  in  front  as  a  dorsal  fin. 
There  are  sex  differences  in  the  shape  of  the  dorsal  fins  of  mature 
individuals  and  the  female  has  a  considerable  anal  fin  (Fig.  47). 


iv.  5 


SWIMMING   OF  LAMPREYS 


85 


The  lamprey  swims  with  an  eel-like  motion,  using  its  myotomes  in 
the  serial  manner  that  has  been  mentioned  in  amphioxus  and  will  be 
discussed  later  (p.  133).  The  waves  that  pass  down  the  body  are  of 
short  period  relative  to  the  length,  so  that  the  swimming  is  mechani- 
cally inefficient;  lampreys  show  great  activity,  but  their  progress  is 
not  rapid.  The  animal  often  comes  to  rest,  attaching  itself  with  the 
sucker  to  stones  (hence  the  name,  'suck-stone')  or  to  its  prey.  In  this 
position  water  cannot  of  course  pass  in  through  the  mouth,  but  both 


s.  cut. 


Fig.  48.  Section  of  skin  of  lamprey. 

c.  club  cells;  der.  dermis;  ep.  epidermis;  gr.  granular  gland-cells;  m.  myotomal  muscle; 
pig.  pigment  cells;  s.cut.  subcutaneous  connective  tissue.  (After  Krause.) 

enters  and  leaves  by  the  gill  openings.  When  swimming  the  backward 
jet  of  water  may  assist  in  locomotion. 

The  trunk  musculature  consists  of  a  series  of  myotomes  separated 
by  myocommas.  Each  myotome  has  a  W-shape,  instead  of  the  simple 
V  of  amphioxus.  The  muscle-fibres  run  longitudinally  and  they  are 
striped,  but  of  a  somewhat  peculiar  fenestrated  type. 

5.  Skeleton  of  lampreys 

The  skeleton  of  lampreys  consists  of  the  notochord  and  various 
collections  of  cartilage.  This  latter  is  partly  of  the  typical  vertebrate 
type,  that  is  to  say,  consists  of  large  cells  in  groups,  separated  by  a 
matrix  of  the  protein  chondrin,  which  they  secrete.  In  other  regions 
a  tissue  containing  more  cells  and  less  matrix  is  found,  the  so-called 
fibro-cartilage,  and  this  more  nearly  resembles  fibrous  connective 
tissue  and  serves  to  emphasize  that  no  sharp  line  can  be  drawn 
between  these  tissues.  There  is  also,  in  the  larva,  a  tissue  known  as 


86  VERTEBRATES  WITHOUT  JAWS  iv.  5 

muco-cartilage,   which   is   an  elastic   material  serving  more   as   an 
antagonist  to  the  muscles  than  for  their  attachment. 

The  notochord  remains  well  developed  throughout  life  as  a  rod 
below  the  nerve-cord.  It  consists  of  a  mass  of  large  vacuolated  cells, 


Fig.  49.  Transverse  section  through  notochord  of  lamprey. 
c.  cells;  s.  sheath.  (After  Krause.) 


anc 


Fig.  50.  Lateral  view  of  skeleton  of  head  and  branchial  arches  of  Petromyzon. 

ac.  auditory  capsule;  adc.  antero-dorsal  cartilage;  anc.  annular  cartilage;  ha.  branchial 
arch;  bd.  basidorsal;  hac.  hyoid  cartilage;  hbc.  hypo-branchial  rod;  lit.  horizontal  bar;  n. 
notochord;  ?ic.  nasal  capsule;  oc.  orbital  cartilage;  per.  pericardial  cartilage;  pdc.  postero- 
dorsal  cartilage;  pic.  posterolateral  cartilage;  st.  styliform  cartilage;  /.  tendon  of  tongue; 
II-X,  cranial  nerves.  (After  Parker.) 

enclosed  in  a  thick  fibrous  sheath  (Fig.  49).  The  rigidity  of  the  whole 
rod  depends  on  the  turgor  of  the  cells  and  it  often  collapses  com- 
pletely in  fixed  and  dehydrated  material  (Fig.  59).  No  doubt  in  life  it 
serves,  like  the  notochord  of  amphioxus,  to  prevent  shortening  of  the 
body  when  the  myotomes  contract. 

The  notochordal  sheath  is  continuous  with  a  layer  of  connective 
tissue,  which  also  surrounds  the  spinal  cord  and  joins  the  myocom- 


iv.  s  SKELETON  OF  LAMPREYS  87 

mas  and  thus  eventually  the  subcutaneous  connective  tissue.  Within 
this  connective  tissue  there  develop  certain  irregular  cartilaginous 
thickenings  that  are  of  special  interest  because  they  may  be  compared 
with  vertebrae,  perhaps  with  the  basi-dorsal  element  (p.  132).  They 
lie  on  either  side  of  the  spinal  cord  (Fig.  50),  that  is  to  say,  above  the 
notochord,  and  consist  either  of  one  nodule  on  each  side  of  the  seg- 
ment, through  the  middle  of  which  the 
ventral  nerve-root  emerges,  or  of  two 
separate  nodules,  with  the  nerve  between 
them.  Rods  of  cartilage  extend  dorsally 
and  ventrally  into  the  fins,  but  are  not 
attached  to  the  'vertebrae'. 

The  lamprey  skull  shows  even  in  the 
adult  the  basic  arrangement  found  only 
in  the  embryo  of  higher  vertebrates.  The 
floor  is  formed  of  paired  parachordals  on 
either  side  of  the  notochord  and  in  front 
of  this  paired  trabeculae.  Attached  to  this 
base  is  a  series  of  incomplete  cartilagi- 
nous boxes  surrounding  the  brain  and 
organs  of  special  sense  (Fig.  51).  To 
this  skull  is  attached  the  skeleton  that 
supports  the  sucker  and  gills.  The 
arrangement  of  the  skull  differs  consi- 
derably from  that  of  later  vertebrates. 
The  cranium  has  a  floor  around  the  end 
of  the  notochord,  and  in  front  of  this 
there  is  a  hole  containing  the  pituitary 
gland.  The  side  walls  are  strong  but  the  roof  is  composed  only  of 
a  tough  membranous  fibro-cartilage.  The  auditory  capsules  are 
compact  boxes  surrounding  the  auditory  organs  at  the  sides.  The 
olfactory  capsule,  imperfectly  paired,  is  also  almost  detached  from 
the  cranium.  Other  ridges  of  cartilage  lie  below  the  eyes  and  there  is 
a  complex  support  for  the  sucker. 

The  skeleton  of  the  branchial  region  consists  of  a  system  of  vertical 
plates  between  the  gill-slits,  joined  by  horizontal  bars  above  and 
below  them.  This  cartilage  lies  outside  the  muscles  and  nerves  and  is 
therefore  difficult  to  compare  with  the  branchial  skeleton  of  higher 
fishes,  which  lies  in  the  wall  of  the  pharynx.  The  elastic  action  of  the 
cartilages  produces  the  movement  of  inspiration.  A  backward  exten- 
sion of  the  branchial  basket  forms  a  box  surrounding  the  heart. 


Fig.  51.  Dorsal  view  of  skull  of 

Petromyzon. 

Lettering    as    Fig.    50.   /,    olfactory 

nerve;  /.  hole  in  roof  of  cranium. 

(After  Parker.) 


88  VERTEBRATES  WITHOUT  JAWS  iv.  6 

6.  Alimentary  canal  of  lampreys 

The  sucker  is  bounded  at  the  edges  by  a  series  of  lips,  which  besides 
being  sensory  serve  also  to  make  a  tight  attachment  when  the  lamprey 
sucks  (Fig.  52).  In  the  sucker  are  numerous  teeth,  whose  arrangement 
varies  in  the  different  types  of  lamprey.  These  teeth  are  horny  epi- 
dermal thickenings,  supported  by  cartilaginous  pads,  and  are  there- 
fore not  comparable  with  the  teeth  of  vertebrates,  which  are  derived 


Fig.  52.  Sucker  of  Petromyzon  show-  Fig.  53.  Section  through  tooth  of  lamprey 

ing  outer  circular  lip,  teeth,  and  tongue,  1,  horny  cap;  2,  stellate  tissue;  3,  cap  to  replace 

with  special  teeth,  at  the  centre.  , ;  4>  connective  tissue;  5,  epidermis  of  mouth; 

(After  Parker.)  6,  cartilage; 7,  proliferative  layers  of  epidermis 

that  produce  the  horny  cells. 
(After  Hansen,  from  Kukenthal.) 

mainly  from  mesodermal  tissues  (Fig.  53).  The  sharper  and  larger 
teeth  are  borne  on  a  movable  tongue,  which  is  used  as  a  rasp  (Fig.  54). 
An  annular  muscle  runs  round  just  above  the  lips  of  the  sucker  and 
presumably  serves  to  narrow  the  margin  and  hence  to  release  the  fish. 
The  remaining  muscles  are  mostly  attached  to  the  tongue  and  base 
of  the  sucker.  The  largest  of  these  muscles,  the  m.  cardioapicalis,  is 
attached  posteriorly  to  the  cartilage  surrounding  the  heart  and  in  front 
is  prolonged  into  a  conspicuous  lingual  tendon,  which  is  attached  to 
the  tongue  and  serves  to  pull  it  backwards.  Presumably  the  action  of 
this  muscle  deepens  the  oral  cavity  and  is  thus  the  main  agent  securing 
attachment  of  the  sucker.  There  is  a  collar  of  circular  fibres  around 
the  front  end  of  the  cardio-apical  muscle,  serving  to  lock  the  tendon 
and  maintain  the  suction.  Dorsal  and  ventral  to  the  main  tendon  are 


iv.  6 


FEEDING   OF  LAMPREYS 


groups  of  muscles  that  rock  the  tongue  up  and  down  to  produce  a 
rasping  action.  The  muscles  of  the  sucker  are  all  derived  from  the 
lateral  plate  and  are  innervated  from  the  trigeminal  nerve;  their  fibres 
are  striated. 

The  mouth  is  a  small  opening  above  the  tongue  and  leads  into  a 
large  buccal  cavity.  At  the  hind  end  this  divides  into  a  dorsal  passage, 
the  oesophagus,  for  the  food,  and  a  ventral  respiratory  tube,  which 
leads  to  the  gill  pouches  but  is  closed  behind.  At  the  mouth  of  the 


ann. 


m.  card.ap. 


circ.m. 


mus.2  mus.t 


Fig.  54.  Longitudinal  section  through  head  of  lamprey. 

ann.  annular  muscle  of  sucker;  b.  brain;  circ.m.  circular  fibres  of  tongue-muscles;  oes.  oeso- 
phagus; g.  gill  aperture;  h.s.  hypophysial  sac;  m.card.ap.  cardio-apical  muscle;  mus.  1  and 
2,  muscles  that  rock  the  tongue;  n.  notochord;  nas.  nasal  sac;  nos.  nostril;  p.  pineal;  pit. 
pituitary  gland;  t.  tooth;  tend,  tendon  of  tongue,  pulled  back  by  m.card.ap.;  to.  tongue.  (Partly 

after  Tretjakoff.) 

respiratory  tube  is  a  series  of  velar  tentacles,  corresponding  exactly  in 
position  to  those  of  amphioxus,  and  serving  to  separate  the  mouth 
and  oesophagus  from  the  respiratory  tube  while  the  lamprey  is  feed- 
ing. The  seven  branchial  sacs  are  lined  by  a  folded  respiratory  epi- 
thelium and  surrounded  by  muscles,  and  these,  together  with  the 
elastic  cartilages  and  appropriate  valves,  ensure  the  pumping  of  the 
water  tidally,  in  and  out  of  the  external  openings.  In  front  of  the  first 
sac  is  the  remains  of  an  eighth  pouch,  whose  surface  is  not  respiratory. 
The  'salivary'  glands  are  curious  organs  of  which  little  is  known. 
They  are  a  pair  of  pigmented  sacs,  embedded  in  the  hypobranchial 
muscles.  Each  has  a  folded  wall,  from  which  a  duct  proceeds  forward 
to  open  below  the  tongue.  The  salivary  glands  produce  a  secretion 
that  prevents  coagulation  of  the  blood  of  the  fishes  on  which  the  lam- 
prey feeds.  The  nature  of  this  secretion  is  not  known,  but  it  rapidly 
turns  black  on  exposure  to  the  air  and  the  glands  for  this  reason 
appear  to  be  pigmented.  It  has  been  observed  that  in  lampreys  taken 
from  fishes  the  intestine  is  filled  with  red  corpuscles,  and  there  is 
therefore  no  doubt  that  they  feed  mainly  on  the  blood  of  their  prey. 


90  VERTEBRATES  WITHOUT  JAWS  iv.  6- 

Little  is  known  of  the  habits  of  lampreys  in  the  sea,  but  in  North 
America  there  are  races  of  lampreys  that  are  land-locked  and  feed  on 
the  fishes  in  the  lakes,  where  they  have  recently  become  a  most  serious 
pest  (Fig.  55). 

The  oesophagus  (fore-gut)  leads  directly  into  a  straight  intestine 
(mid-gut);  there  is  no  true  stomach  in  lampreys  (Fig.  56).  The  surface 
of  the  intestine  is  increased  by  a  typhlosole,  running  a  somewhat 
spiral  course.  There  is  a  liver,  gall-bladder,  and  bile-duct  of  typical 
vertebrate  plan,  but  no  separate  pancreas.  However,  in  the  wall  of  the 


Fig.  55.  Lake  lamprey  attached  to  a  bony  fish,  which  also  shows  the  scars  of  the 
attacks  of  other  lampreys.  (After  Gage.) 

anterior  part  of  the  intestine  there  are  large  patches  of  cells  that 
resemble  those  of  the  acini  of  the  pancreas  of  higher  forms  and  con- 
tain secretory  granules.  Barrington  has  shown  that  extracts  of  this 
region  have  a  high  proteolytic  power,  the  enzyme  being  of  the  tryptic 
type,  with  its  optimum  between  pH  7-5  and  7-8.  Some  of  this  tissue  is 
collected  in  the  walls  of  short  diverticula,  reaching  forwards.  The 
situation  is  therefore  essentially  similar  to  that  found  in  amphioxus, 
and  we  may  regard  these  patches  of  zymogen  cells,  or  the  diverticula, 
as  the  forerunners  of  the  exocrine  portions  of  the  pancreas.  In  the 
lampreys  the  endocrine  portion,  not  yet  identified  in  amphioxus,  also 
appears.  Around  the  junction  of  the  fore-gut  and  intestine  are  groups 
of  follicles  that  do  not  communicate  with  the  lumen  of  the  intestine. 
These  'follicles  of  Langerhans'  were,  appropriately  enough,  first  seen 
by  the  discoverer  of  the  islets  in  higher  forms,  and  Barrington  has 
now  shown  that  following  destruction  of  this  tissue  by  cautery  there 
is  a  rise  in  blood-sugar.  Moreover,  after  injection  of  glucose,  vacuola- 
tion  of  the  cells  occurs.  We  may  safely  conclude  that  these  cells  are 
involved  in  carbohydrate  metabolism,  but  only  one  type  of  cell  is 
present. 


iv.  7 


(9i) 


7.  Blood  system  of  lampreys 

The  blood  vascular  system  is  arranged  on  the  same  general  plan 
as  in  amphioxus  but  there  is  a  well-developed  heart.  This  lies  behind 
the  gills  and  can  be  considered  as  a  portion  of  the  sub-intestinal  vessel, 
folded  into  an  S-shape  and  divided  into  three  chambers.  The  heart 
is  suspended  in  a  special  portion  of  the  coelom,  the  pericardium, 
whose  walls  are  supported  by  cartilage.  In  the  larva  the  heart  first 
appears  as  a  straight  tube  and  owing  to  an  abnormality  of  development 
it  sometimes  fails  to  develop  its  S-shape.  Contractions  can  neverthe- 


Fig.  56.  Mid-gut  of  larval  lamprey. 

ai.  anterior  region  of  intestine;  bd.  bile-duct;  ca.  coeliac  artery;  gb.  gall-bladder;  hp.  hepatic 

portal   vein;   /.   liver;   oes.   oesophagus;  p.   position   of  'pancreas',   containing   islet   tissue; 

pi.  posterior  intestine;  y.  yellow  area  where  wall  of  intestine  contains  zymogen  cells. 

(From  Barrington.) 

less  be  seen  in  these  abnormal  hearts,  passing  from  behind  forwards 
along  the  straight  tube.  Similarly  in  the  normal  heart  contraction 
proceeds  in  the  chambers  from  behind  forwards.  The  most  posterior 
chamber  is  a  thin-walled  sinus  venosus,  into  which  the  veins  pour 
blood.  This  leads  to  an  auricle  (atrium),  also  thin-walled,  lying  above 
the  sinus.  The  atrium  passes  blood  into  the  ventricle  below  it,  a 
thick-walled  chamber,  providing  the  main  force  for  sending  the  blood 
round  the  body. 

The  heart  receives  nerve-fibres  from  the  vagus  nerve  and  contains 
nerve-cells,  some  of  which  give  a  chromaffin  reaction  suggesting  the 
presence  of  adrenalin-like  substances.  Stimulation  of  the  vagus  nerve 
produces  acceleration  of  the  heart-beat,  followed  by  slowing.  Acetyl 
choline  also  accelerates  the  heart.  In  Myxine  there  are  no  nerves  to 
the  heart  or  nerve-cells  in  it  and  acetyl  choline  has  no  effect.  Both 
hearts  contain  much  adrenaline  and  similar  substances  but  show  little 
change  when  adrenaline  is  added  to  a  perfusate. 

Blood  leaves  the  ventricle  by  a  large  ventral  aorta,  running  forwards 


92  VERTEBRATES  WITHOUT  JAWS  iv.  7- 

between  the  gill  pouches,  to  which  it  sends  a  series  of  eight  afferent 
branchial  arteries.  These  break  up  into  capillaries  in  the  gills,  and 
efferent  branchial  arteries  collect  to  a  pair  of  dorsal  aortae,  running 
backwards,  which  join  and  form  the  main  dorsal  aorta.  This  passes 
down  the  trunk  and  carries  blood  to  all  the  parts  of  the  body  by  means 
of  series  of  segmental  arteries  and  special  vessels  to  the  gut,  gonads, 
and  excretory  organs.  A  curious  feature  is  that  many  of  these  arteries 
are  provided  with  valves  at  the  point  at  which  they  leave  the  main 

trunks  (Fig.  57).  It  may  be  significant 
that  such  valves  are  not  found  where 
the  efferent  branchials  join  the  dorsal 
aorta,  nor  at  the  points  of  exit  of  the 
renal  arteries,  so  that  perhaps  the 
valves  serve  to  reduce  the  pressure  in 
the  majority  of  the  arteries,  while 
leaving  it  high  in  those  to  the  kidneys. 
The  removal  of  large  quantities  of 
water  is  an  important  problem  in  all 
freshwater  animals  and  is  facilitated 
by  a  high  pressure  in  the  kidneys. 
This  must  be  difficult  to  maintain  in 
an  animal  with  a  branchial  circulation 
and  hence  a  double  set  of  capillaries. 
The  venous  system  consists  of  a 
network  of  sinuses,  with  contractile 
venous  hearts  in  various  places. 
There  is  a  large  caudal  vein,  dividing 
where  it  enters  the  abdomen  into  two  posterior  cardinals.  These 
run  forward  in  the  dorsal  wall  of  the  coelom,  collecting  blood  from 
the  kidneys,  gonads,  &c,  and  opening  into  the  heart  by  a  single 
ductus  Cuvieri  on  the  right-hand  side,  this  being  the  remains  of  a  pair 
found  in  the  larva.  Anterior  cardinals  collect  blood  from  the  front 
part  of  the  body,  and  there  is  also  a  conspicuous  ventral  jugular  vein 
draining  venous  blood  from  the  muscles  of  the  sucker  and  gill  pouches. 
Besides  the  veins  proper  there  is  a  large  system  of  venous  sinuses, 
especially  in  the  head.  Blood  from  the  gut  passes  by  a  hepatic  portal 
vein  through  a  contractile  portal  heart  to  the  liver,  from  which  hepatic 
veins  proceed  to  the  heart. 

The  blood  of  lampreys,  like  that  of  all  vertebrates,  contains  the 
respiratory  pigment  haemoglobin,  enclosed  in  corpuscles,  here  nucle- 
ated.  This  arrangement  immensely  increases  the  oxygen-carrying 


Fig.    57.    Valves    at    the    origin    of 
segmental  arteries  of  a  lamprey. 

1,  notochord;  2,  segmental  artery;  3, 

aorta. 

(From  Kukenthal,  after  Keibal.) 


iv.  8  EXCRETION  IN  LAMPREYS  93 

power  of  the  blood.  Haemopoietic  tissue  occurs  in  the  intestinal  wall 
of  the  larva  and  this  has  been  regarded  by  some  as  representing  the 
spleen.  In  the  adult  the  blood-forming  tissue  lies  below  the  spinal 
cord  and  in  the  kidney.  White  corpuscles  resembling  lymphocytes 
and  polymorphonuclear  cells  occur,  produced  by  lymphoid  tissue  in 
the  kidneys  and  elsewhere.  However,  there  is  no  distinct  system  of 
lymphatic  channels. 

8.  Urinogenital  system  of  lampreys 

The  excretory  and  genital  systems  of  vertebrates  consist  of  a  series 
of  tubes  opening  from  the  coelom  to  the  exterior  and  serving  to  carry 
away  both  excretory  and  genital  products.  This  plan  of  organization  is 


Fie.  58.  Diagram  to  show  arrangement  of  the  pronephros  in  a  freshly  hatched 

lamprey. 
g.  gonad;  pr.  pronephros;  prd.  pronephric  duct.  (After  Wheeler.) 

quite  different  from  that  found  in  amphioxus  and  represents  a  new 
acquisition  by  the  vertebrates.  It  is  not  clear  whether  the  excretory 
or  genital  component  of  the  complex  is  the  primary  one,  nor  indeed 
why  they  are  associated.  The  gonads  develop  from  the  walls  of  the 
coelom  in  all  animals  possessing  that  cavity;  some  hold  that  the  coelom 
represents  an  enlargement  of  a  sac  that  at  first  served  purely  as  a 
gonad.  Genital  ducts  leading  from  the  coelom  to  the  exterior  are 
common  in  invertebrates,  and  we  may  guess  that  at  their  first  appear- 
ance the  urinogenital  tubules  of  vertebrates  served  only  for  genital 
products. 

The  conversion  of  these  tubules  to  excretory  purposes  may  have 
been  a  result  of  the  adoption  of  the  freshwater  habit.  The  blood  of 
lampreys,  when  in  fresh  water,  contains  a  higher  concentration  of  salts 
than  the  surrounding  water.  Little  is  known  about  the  condition  in 
sea  lampreys,  where  blood  is  probably  hypotonic  to  the  sea.  When  in 
the  river  the  animals  must  deal  with  the  tendency  for  water  to  flow  in. 
This  water  must  be  removed  without  losing  salt ;  accordingly  in  most 
freshwater  animals,  including  vertebrates,  we  find  some  system  by 
which  the  separation  can  be  achieved. 


94  VERTEBRATES  WITHOUT  JAWS  iv.  8 

The  region  that  gives  rise  to  the  kidney  during  development  lies 
between  the  dorsal  scleromyotome  and  the  more  ventral  lateral  plate 


card  v 


glom 


on.  t 


oes. 


pron.  F 


Fig.  59.  Section  through  newly  hatched  larvae  of  Lampetia  hehind  the  pharynx. 

ao.  aorta;  card.v.  cardinal  vein;  glom.  glomerulus;  fit.  heart;  my.  myotome;  n.c.  nerve-cord; 
not.  notochord,  which  has  collapsed  because  of  lack  of  turbidity  after  fixation;  oes.  oeso- 
phagus; pron.f.  ciliated  funnel  of  pronephros;  pron.t.  twisted  pronephric  tubule;  sp.  space 

around  nerve-cord. 


Fig.  60.  Kidney  system  of  a  22-millimetre  larva  of  Lampetra. 

tnes.  mesonephric  tubules;  mesg!.  mesonephric  glomeruli;  pr.  pronephric  funnels; 
prd.  pronephric  duct;  prgl.  pronephric  glomeruli.  (After  Wheeler.) 

mesoderm;  it  is  known  as  the  nephrotome.  This  tissue  differentiates 
during  development  from  in  front  backwards,  making  a  series  of 
segmental  funnels,  opening  into  a  common  archinephric  duct  (Fig. 
58).  The  most  anterior  funnels  open  into  the  pericardium;  usually 
there  are  four  of  these  in  a  freshly  hatched  larva,  opening  into  a  single 


iv.  8 


EXCRETION  IN  LAMPREYS 


95 


mid 


duct,  which  reaches  back  to  an  aperture  near  the  anus.  Close  to  each 
funnel  there  develops  a  tangle  of  blood-vessels,  the  glomerulus  (Figs. 
59  and  6o).  Presumably  the  osmotic  flow  of  water  into  the  body  is 
relieved  by  the  pressure  of  the  heart-beat  forcing  water  out  from  the 
glomeruli  into  the  coelomic  fluid,  whence  it  is  removed  by  the  funnels, 
with  the  aid  of  their  cilia.  The  tubules  become  longer  and  twisted 
after  hatching  and  may  perhaps  serve  for  salt-reabsorption. 

These  anterior  funnels  constitute 
the    pronephros.    As    the    animal 
grows  they  are  replaced  by  a  more 
posteror    set,     the    mesonephros. 
There     is,     however,     a    gap     of 
several    segments     in     which     no 
tubules  appear  (Fig.  6o),  a  strange 
and     unexplained      discontinuity, 
common   to   all  vertebrates.    The 
pronephric  tubules  gradually  dis- 
appear and  finally  in  the  adult  all 
that  remains  of  the  organ  is  a  mass 
of  lymphoid  tissue.  Meanwhile  the 
mesonephros  develops  as  a  much 
larger  fold,  hanging  into  the  coelom 
and  containing  very  extensive  wind- 
ing tubules.  These  do  not  open  to 
the  coelom  (at  least  in  the  adult)  but 
each  to  a  small  sac,  the  Malpighian 
corpuscle,  which  contains  a  portion 
of  the  coelom  and  the  glomerulus. 
This  is  obviously  a  more  efficient  method  for  allowing  the  heart  to 
pump  excess  water  out  of  the  blood  and  down  the  tubules.  The  latter 
themselves  have  become  greatly  elongated  and  make  up  the  main 
bulk  of  the  organ  (Fig.  6i).  The  segmental  arrangement  is  there- 
fore much  obscured  and  as  extra  glomeruli  are  added  it  disappears 
completely.  The  mesonephros  extends  at  its  hind  end  as  the  animal 
grows,  until  it  forms  the  adult  kidney,  a  continuous  ridge  of  tissue 
reaching  back  to  the  hind  end  of  the  coelom.  Besides  the  excretory 
apparatus  the  kidney  also  contains  much  lymphoid  tissue  and  fat,  and 
it  probably  plays  a  part  in  the  formation  and  destruction  of  red  and 
white  corpuscles. 

The  gonads  are  unpaired  ridges  medial  to  the  mesonephros.  Pri- 
mordial germ-cells,  set  aside  very  early  in  development,  migrate  into 


Fig.  6i.  Transverse  section  of  kidney  of 
hampetra. 

gl.    glomerulus;     mid.     middle    section     of 

tubule;  pr.  proximal  region  of  tubule;  term. 

terminal  region,  opening  into  W.d.  Wolffian 

duct. 

(After  Krause.) 


iv.  8- 


96  VERTEBRATES  WITHOUT  JAWS 

these  ridges  and  develop  into  eggs  or  sperms.  The  differentiation  of 
the  gonad  occurs  relatively  late  in  lampreys,  so  that  in  young  am- 
mocoetes  the  organ  is  'hermaphrodite',  containing  developing  oocytes 
and  spermatocytes  together.  The  ripe  ovary  consists  of  ova  each  sur- 
rounded by  single-layered  follicular  epithelium,  which  finally  ruptures 
and  liberates  the  egg  into  the  coelom,  whence  it  escapes  by  pores  to  be 
described  presently.  The  testis  consists  of  a  number  of  follicles  con- 
taining sperms;  it  is  unique  among  vertebrates  in  that  the  follicles 


CL         U9. 

Fig.  62.  Cloacal  region  of  fully  adult  Lampetra. 

C.  coelom;  CI.  lips  of  cloaca;  Ct.  connective  tissue;  D.  duct  leading  from  coelom  to  the 

mesonephric   duct;   Df.    dorsal   fin;   M.   muscle;   Md.   mesonephric   ducts;   N.   notochord; 

R.  rectum;  Ug.  urinogenital  papilla.  (After  Knowles.) 

have  no  ducts;  when  ripe  they  rupture  into  the  coelom,  which  becomes 
filled  with  spermatozoa  and  these  escape,  like  the  ova,  by  pores. 

These  apertures  by  which  the  gametes  escape  are  similar  in  the 
two  sexes  and  consist  of  short  channels,  one  on  each  side,  leading  from 
the  coelom  to  the  lower  end  of  the  kidney  duct  (Fig.  62).  They  nor- 
mally become  open  only  a  few  weeks  before  spawning,  but  Knowles 
has  shown  that  injections  of  oestrone  or  anterior  pituitary  extract  will 
cause  perforations  of  the  ducts  in  young  lampreys,  indeed  even  in  the 
ammocoete  larve. 

Fertilization  is  external,  but  there  are  modifications  of  the  cloaca  in 
the  two  sexes  to  assist  in  ensuring  fertilization  and  proper  placing  of 
the  eggs  in  the  'nest'  (p.  113).  The  lips  of  the  cloaca  of  the  ripe  male 
are  united  to  form  a  narrow  penis-like  tube.  The  cloacal  lips  of  the 


iv.  9  NERVOUS  SYSTEM  OF  LAMPREYS         97 

female  are  enlarged  and  often  red;  in  addition  she  has  an  anal  fin, 
probably  used,  as  in  salmon  and  trout,  to  make  a  nest.  These  sex 
differences,  which  develop  shortly  before  spawning,  can  also  be 
initiated  by  injection  of  anterior  pituitary  extracts  (p.  107). 

9.  Nervous  system  of  lampreys 

The  nervous  system  of  the  cyclostomes  is  very  much  better 
developed  than  that  of  amphioxus  and  shows  the  characteristic  plan 
that  is  present  in  all  vertebrates.  The  essence  of  the  vertebrate  ner- 
vous organization  may  be  said  to  be  that  it  consists  of  large  amounts 
of  tissue  and  is  highly  centralized.  The  brains  of  vertebrates  contain 
much  larger  aggregates  of  nervous  tissue  than  are  to  be  found  in  any 
other  animals,  and  this  tissue  produces  by  its  actions  the  most  charac- 
teristic features  of  vertebrate  life.  Vertebrates  are  active,  exploratory 
creatures,  and  their  behaviour  is  much  influenced  by  past  experience. 

We  shall  return  later  to  detailed  discussion  of  the  organization  of 
the  central  nervous  system;  now  we  may  look  briefly  at  the  plan 
found  in  the  lamprey,  as  an  introduction  to  that  of  other  vertebrates. 
As  compared  with  amphioxus  there  has  been  a  very  high  degree  of 
cephalization.  The  front  end  of  the  spinal  cord  is  enlarged  into  a 
complicated  brain,  and  the  nerves  connected  with  a  number  of  the 
more  anterior  segments  have  become  modified  to  form  special  cranial 
nerves. 

The  spinal  nerves,  however,  still  show  the  plan  found  in  amphioxus 
in  that  the  dorsal  and  ventral  roots  do  not  join.  In  amphioxus  the 
ventral  roots  contain  motor-fibres  for  the  myotomes  and  some 
proprioceptive  fibres,  while  the  dorsal  roots  contain  sensory  fibres  and 
motor-fibres  for  the  lateral  plate  musculature  (p.  36).  The  details  of 
the  composition  of  the  nerves  of  lampreys  are  still  unknown,  but  there 
are  hints  of  considerable  deviations  from  this  plan.  The  ventral  roots 
contain  many  motor  fibres  passing  to  the  myotomes.  The  dorsal  roots 
consist  largely  of  sensory  fibres  with  bipolar  cell  bodies  collected  into 
dorsal  root  ganglia  including  proprioceptor  fibres  from  the  myotomes: 
it  is  not  known  whether  the  dorsal  roots  also  contain  any  efferent 
fibres.  In  the  young  larva  many  of  the  afferent  fibres  are  the  processes 
of  cells  lying  in  the  spinal  cord  (Rohon-Beard  cells),  which  are 
typical  of  the  early  stage  of  many  chordates.  There  are  few  types 
of  cells  in  the  cord  at  this  time,  allowing  for  only  the  simplest 
reflex  arcs. 

The  autonomic  nervous  system  shows  some  generalized  and  some 
special  features.  The  gut  is  mainly  innervated  by  the  vagus,  which 


98  VERTEBRATES  WITHOUT  JAWS  iv.  9 

extends  far  back  along  the  intestine.  There  is  little  contribution  of 
fibres  from  the  spinal  nerves  to  the  alimentary  canal,  since  this  has  no 
mesentery,  being  attaached  only  at  its  cranial  and  caudal  ends.  There 
are,  however,  numerous  fibres  from  the  spinal  nerves  to  the  rectum, 
ureters,  and  cloacal  region,  and  numerous  postganglionic  neurons 
are  found  here.  Nerve-cells  are  also  found  in  the  intestinal  plexuses. 

The  sympathetic  system  consists  of  isolated  fibres  running  in  both 
dorsal  and  ventral  roots.  Many  of  these  run  directly  to  their  endings, 
for  instance  in  the  arteries,  without  interpolation  of  neurons.  A  few 
postganglionic  cells  are  present,  however,  but  they  are  seldom  collec- 
ted into  ganglia.  The  system  is  therefore  even  more  scattered  than 
in  elasmobranchs  (p.  173).  The  'adrenal'  system  is  also  diffuse.  There 
are  scattered  masses  of  interrenal  (cortical)  tissue  and  large  groups 
of  suprarenal  (medullary)  cells,  especially  in  the  walls  of  the  veins  and 
the  heart.  The  suprarenal  tissue  receives  'preganglionic'  fibres  from 
the  spinal  nerves.  Its  cells  sometimes  seem  to  be  connected  with  each 
other  by  fibres  like  those  of  neurons  and  they  may  operate  a  form  of 
control  intermediate  between  nervous  and  hormonal  (Johnels,  1956). 

The  nerve-fibres  in  the  nervous  system  of  cyclostomes  are  not  pro- 
vided with  myelin  sheaths ;  in  this  they  resemble  the  nerves  of  amphi- 
oxus.  Conduction  is  slow  in  such  non-medullated  fibres,  the  only  case 
actually  investigated  in  cyclostomes  being  the  lateral  line  nerve  of 
Bdellostoma,  found  by  Carlson  to  conduct  at  the  low  rate  of  5  metres 
a  second  (frog  about  50  m/sec,  mammals  up  to  100  m/sec). 

The  spinal  cord  is  of  a  uniform  transparent  grey  colour  and  is 
flattened  dorso-ventrally,  apparently  to  allow  access  of  oxygen,  and 
metabolites,  no  blood-vessels  being  present  within  the  cord.  How- 
ever, vessels  are  present  in  Myxine  in  which  the  cord  is  also  flat.  The 
nerve-cell  bodies  lie,  as  in  higher  vertebrates,  towards  the  centre,  but 
the  synaptic  contacts  are  not  made  in  this  'grey'  matter  but  at  the 
periphery,  in  what  would  correspond  to  the  white  matter  of  higher 
forms.  The  outer  part  of  the  cord  is  thus  made  up  of  a  neuropil  or 
nerve  feltwork,  formed  of  the  terminations  of  the  incoming  sensory 
fibres  and  the  dendrites  of  the  motor-cells.  These  cells  (Fig.  63)  lie 
in  the  ventral  part  of  the  cord,  their  axons  running  out  to  make  the 
large  fibres  of  the  ventral  roots  and  their  dendrites  passing  to  all  parts 
of  the  peripheral  regions  of  both  the  same  and  the  opposite  sides  of  the 
cord.  They  are  thus  presumably  able  to  be  stimulated  directly  by 
impulses  in  the  processes  of  the  afferent  fibres  that  end  in  these 
regions. 

Direct  control  of  the  spinal  cord  from  the  brain  is  obtained  through 


(99) 


neur.p. 


Fig.  63.  Cells  of  the  spinal  cord  of  the  larva  of  Lampetra. 
A  „nH  R   We  motor-cells   with  dendrites  reaching  to  the  opposite  side;  C,  small  cells  with 
^p^SSno  axon;   «.   axon;   M/.   Mailer's   fibres;   „*«,.>.   neuropil   at 
P  periphery  of  spinal  cord.  (After  Tretjakoff.) 


VERTEBRATES  WITHOUT  JAWS 

opt.L. 


IV.  9 


cer. 


hi/pot. 


Fore. 
cerh.  h. 


Mid-  Hind-  brain. 

opt.L  med.    c^or 


Fore.  -         Mid-  Hind-  brain. 


Lam.i 


Fore. 


Mid. 


Hind  — brain. 


Fig.  64.  Brain  of  the  lamprey. 

A,  side  view;  B,  dorsal  view  with  choroid  plexus  intact;  c,  after  removal  of  choroid,  cereb. 
cerebellum;  cer. h.  cerebral  hemisphere;  chor.  choroid  plexus;  hypot.  hypothalamus;  it.  iter 
between  third  and  fourth  ventricles;  lam.t.  lamina  terminalis  (thickened  anterior  wall  of 
third  ventricle);  med.  medulla  oblongata;  opt.L  optic  lobe;  pin.  pineal  eye;  thai,  thalamus; 
3rd  v.,  4th  v.,  third  and  fourth  ventricles.  (After  Sterzi.) 

a  number  of  very  large  Miiller's  fibres,  originating  from  giant  cells  in 
the  reticular  formation  of  the  brain,  whose  large  dendrites  (Fig.  65) 
receive  fibres  from  several  higher  centres,  providing  an  uncrossed  final 
common  pathway  to  the  spinal  cord.  There  is  some  difference  of 
opinion  as  to  whether  any  branches  of  these  large  fibres  proceed 


iv.  9  BRAIN  OF  LAMPREYS  101 

directly  into  the  ventral  roots;  probably  they  do  not  do  so  but  the 
dendrites  of  the  motor-cells  branch  around  them  and  thus  receive 
stimulation  (Fig.  63).  In  the  earliest  larva  co-ordination  is  by  a  pair  of 
giant  Mauthner  cells,  with  dendrites  among  the  entering  fibres  of  the 
eighth  nerve  and  an  axon  descending  on  the  opposite  side.  Such  cells 
are  present  in  the  earliest  stages  of  nearly  all  fishes  and  amphibians. 

Other  nerve-cells  in  the  more  dorsal  parts  of  the  cord  have  no  long 
axons  and  apparently  serve  to  connect  the  neuropil  of  the  various 
regions.  The  afferent  fibres  reaching  the  cord  in  the  dorsal  roots  give 
off  branches  that  ascend  for  a  short  distance  and  descend  for  long 
distances.  The  pathways  to  the  brain  thus  pass  through  multiple 
relays. 

The  brain  itself  (Fig.  64)  is  built  on  the  typical  vertebrate  plan,  as 
an  enlargement  of  the  front  end  of  the  spinal  cord,  with  thickenings 
and  evaginations  corresponding  to  the  various  organs  of  special  sense. 
Although  we  know  little  of  its  internal  functional  organization  in 
lampreys,  it  is  probably  not  far  wrong  to  regard  it  as  chiefly  consisting 
of  a  series  of  hypertrophied  special  sensory  centres;  thus  the  forebrain 
is  connected  with  smell,  midbrain  with  sight,  hind-brain  with 
acoustico-lateral  and  taste-bud  systems.  The  forebrain  and  olfactory 
sense  are  moderately  well  developed  in  adult  lampreys,  as  is  the  visual 
sense,  with  its  chief  centre  in  the  midbrain.  The  auditory  and  acoustico- 
lateral  systems  are  not  very  well  marked,  and  the  cerebellum  is  small. 
Taste  is  also  much  less  developed  than  in  the  higher  fishes  (p.  220). 

Parts  of  the  brain 

Forebrain  (prosencephalon)  Cerebral  hemispheres  (telen- 

cephalon) 
Between-brain  (diencephalon) 
Midbrain  (mesencephalon)  Optic  lobes 

Hind-brain  (rhombencephalon)  Cerebellum  (metencephalon) 

Medulla    oblongata    (myelen- 
cephalon) 

The  upper  surface  of  the  brain  is  covered  by  an  extensive  vascular 
pad,  the  choroid  plexus  or  tela  choroidea  (Fig.  64).  This  extends  into 
the  ventricles  of  the  brain  at  three  points — into  the  third  ventricle  of 
the  diencephalon,  into  the  iter  (duct)  leading  through  the  midbrain 
from  third  to  fourth  ventricles,  and  into  the  fourth  ventricle  itself. 
The  roof  of  the  brain  is  thus  non-nervous  in  these  regions.  In  later 
vertebrates    the   choroid    extends   only   into   the   third    and    fourth 


io2  VERTEBRATES  WITHOUT  JAWS  iv.  9- 

ventricles.  Presumably  the  vascular  membranes  of  the  brain  are  highly 
developed  in  lampreys  because  of  the  absence  of  cerebral  blood 
vessels. 

From  the  lower  part  of  the  mid-  and  hind-brain  arise  all  the  cranial 
nerves  except  the  olfactory  and  optic.  These  nerves  follow  the  same 
plan  as  those  of  gnathostomes  but  they  are  difficult  to  make  out  by 
dissection  in  the  lamprey  and  will  be  left  for  consideration  in  con- 
nexion with  the  dogfish,  in  which  they  can  easily  be  dissected.  The 

beet.  opt. 
chor.  pL3 

chor.pt,  4. 


otf.ep  — IM-<^9  % 


/nterped. 


Fie.  65.  Sagittal  section  through  head  of  lamprey. 

cereb.  cerebellum;  cer.h.  cerebral  hemisphere;  chor.pl.  3  &  4,  choroid  plexuses  of  the  3rd  and 
4th  ventricle,  extending  also  into  the  midbrain;  h.s.  naso-hypophysial  tube;  hab.  habenular 
region;  hyp.  hypothalamus;  interped.  interpeduncular  region;  med.  medulla  oblongata;  Mull. 
M Oiler's  cell;  not.  notochord;  o.  glandular  organ  of  nasal  sac;  olf.ep.  olfactory  epithelium; 
olf.n.  olfactory  nerve;  p. ant.,  p. int.,  and  p.nerv.  partes  anterior,  intermedia,  and  nervosa  of  the 
pituitary  gland;  parap.  parapineal;  pin.  pineal;  ted. opt.  tectum  opticum. 

cranial  nerves  represent  nerves  similar  to  the  dorsal  and  ventral  nerve- 
roots  of  the  trunk,  much  modified  as  a  result  of  the  special  develop- 
ment of  the  head  (p.  148).  They  carry  afferent  fibres  from  the  skin  of 
the  head  and  gills  and  motor-fibres  for  moving  the  eyes,  sucker,  and 
branchial  apparatus. 

From  the  relative  sizes  of  the  parts  of  the  brain  it  can  be  seen  that 
the  various  special  sensory  centres  are  still  small.  The  largest  part  of 
the  brain  is  the  medulla  oblongata,  which  is  well  developed  because 


iv.  io  PINEAL  EYES  OF  LAMPREYS  103 

of  the  extensive  sucking  apparatus,  innervated  from  the  trigeminal 
nerve. 

The  forebrain  consists  of  a  pair  of  large  cerebral  hemispheres  and 
these  open  by  the  foramina  of  Munro  into  a  median  third  ventricle, 
whose  walls  constitute  the  diencephalon  or  between-brain  (Fig.  65). 
This  diencephalon,  besides  connecting  the  forebrain  with  the  mid- 
brain, includes  the  thalamus  and  serves  important  functions  of  its  own. 
Its  ventral  part,  the  hypothalamus,  is  well  developed  in  all  vertebrates 
as  a  central  organ  controlling  visceral  activities  and  the  internal  life 
of  the  organism.  Nerve-fibres  from  the  supraoptic  nucleus  of  the 
hypothalamus  proceed  to  the  pars  nervosa  of  the  pituitary  and,  as  in 
other  vertebrates,  are  filled  with  granules  of  neurosecretory  material, 
which  presumably  controls  pituitary  action.  A  simple  portal  system 
of  blood-vessels  connects  the  hypothalamus  with  the  pituitary. 

10.  The  pineal  eyes 

The  diencephalon  is  also  the  region  of  the  brain  from  which  the 
eyes  are  formed.  In  lampreys,  besides  the  usual  pair  of  eyes,  there  is 
also,  attached  to  the  roof  of  the  between-brain,  the  so-called  third, 
epiphysial,  or  median  eye,  better  developed  in  these  animals  than  in 
any  other  living  vertebrate  except  perhaps  certain  reptiles. 

This  organ  is  actually  not  median  but  consists  of  an  unequally 
developed  pair  of  sacs,  that  on  the  right,  the  pineal,  being  larger  and 
placed  dorsal  to  the  morphologically  left  parapineal  (Fig.  66).  The 
sacs  form  by  evagination  from  the  brain  and  remain  connected  with 
the  dorsal  epithalamic  or  habenular  region  of  the  between-brain  by 
two  stalks.  The  two  organs  are  similar  in  structure,  consisting  of 
irregular  flattened  sacs  with  a  narrow  lumen.  Both  upper  and  lower 
walls  of  each  organ  contain  receptor  cells,  with  processes  that  project 
into  the  lumen  and  nerve-fibres  directed  outwards.  These  fibres 
apparently  mostly  end  within  the  organ,  in  contact  with  ganglion 
cells  whose  axons  run  to  unequal  right  and  left  habenular  ganglia. 
In  addition  there  are  supporting  and  pigment  cells  in  the  retinas. 
Knowles  has  shown  that  the  retinal  cells  of  the  pineal  make  movements, 
being  arranged  differently  under  conditions  of  illumination  and  dark- 
ness. The  significance  of  these  photomechanical  changes  is  unknown 
but  they  demonstrate  that  the  pineal  cells  are  sensitive  to  light. 

The  structure  of  these  pineal  organs  shows  that  they  consist  of 
portions  of  the  diencephalic  wall  where  the  ciliated  cells  of  the  epen- 
dyma  are  specialized  as  photoreceptors.  They  show  the  same  general 
plan  as  the  paired  eyes,  but  with  no  differentiated  dioptric  apparatus. 


IV.   IO 


104  VERTEBRATES  WITHOUT  JAWS 

It  has  been  possible  to  find  out  something  of  the  part  that  these 
organs  play  in  the  life  of  the  lamprey.  When  a  bright  spot  of  light  is 
directed  upon  the  pineal  region  of  a  stationary  ammocoete  larva  move- 
ment is  usually  initiated,  but  only  after  illumination  for  many  seconds. 


o.s.s. 


Fig. 


t.s.s.,  o.s.s 


66.  Pineal  and  parapineal  organs  of  adult  Lampetra  fluviatilis 
A.  larva,  B.  adult.  Sagittal  section. 

,  inner  and  outer  sensory  cells;  p.  process;  pin.  pineal;  p. pin.  parapineal. 
(After  Tretjakoff.) 


Moreover,  these  movements  can  be  elicited  even  after  the  pineal 
organs  have  been  removed!  In  the  larval  lamprey  the  paired  eyes  are 
deeply  buried  below  pigmented  skin,  so  the  movement  is  not  likely 
to  be  due  to  them;  indeed  it  continues  when  they  too  have  been  taken 
out!  Evidently  there  must  be  still  other  receptors,  able  to  respond  to 
changes  of  light  intensity  in  the  wall  of  the  diencephalon.  This  recalls 
the  fact  that  photoreceptors  are  found  within  the  substance  of  the 
nervous  system  of  amphioxus.  This  power  of  response  to  changes  of 
illumination  has  been  retained  in  the  vertebrates,  and  persists  in  some 


FUNCTION  OF  PINEAL  EYES 


105 


as  yet  unknown  cells  in  the  brain,  even  after  the  paired  and  pineal 
eyes  have  become  specialized  for  light  reception.  The  whole  study  is 
of  special  interest  as  showing  the  stages  by  which  the  eyes  may  have 
been  evolved.  Higher  fishes  also  show  the  power  of  responding  to 

PINEALS  REMOVED 
1 


rm — 1 1  1  1  1 1  1  1 1  1  M  15. 


I  I  I  i  I  I  I  I  1  !  !  I  I  I  I  II  1  I  I  II  I  I 


\t     up 


hi 


Y  f 


15  20  25  30     I  S 

I   I  M   I   I  I   I   I   I   I   I   I   I   I  I   I  I   I   I  I  I  I  I   I  I 

DECEMBER  JANUARY 


2S26 
I    I 


17 

nil 


10       15   ■ 
' ''  1 1  1 1 1 1 1 1 


MARCH 


Fig.  67.  Colour-changes  of  larval  lampreys,  measured  by  the  melanophore  index  (see 
p.  300).  Animals  kept  out  of  doors  except  as  shown  along  the  line  AB,  where  rect- 
angles above  the  line  show  illumination  with  electric  light  and  below  the  line  total 
darkness.  Normal  animals  show  a  regular  daily  rhythm,  becoming  pale  at  night. 
Reversal  of  normal  day  and  night  illumination  stops  the  change.  On  19  December 
the  pineal  eyes  were  removed  from  five  out  of  the  ten  individuals  and  these  there- 
after remained  dark  (upper  chart);  the  other  five  continued  to  show  the  normal 
rhythm,  until  placed  in  total  darkness.  (After  Young.) 

changes  of  illumination  after  the  paired  eyes  and  epiphysis  have  been 
removed  (p.  210). 

If  the  pineal  eyes  are  not  essential  for  the  initiation  of  movement, 
what  is  then  their  function  ?  In  the  ammocoete  larva  there  is  a  daily 
rhythm  of  change  of  colour,  the  animals  becoming  dark  in  the  day- 
time and  pale  at  night.  After  removal  of  the  pineal  eyes  this  change  no 
longer  occurs:  the  animals  remain  continually  dark  (Fig.  67).  This 
effect  on  the  colour  is  produced  by  the  action  of  influences  from  the 
pineal,  passing  to  the  pituitary  gland  (see  p.  103).  It  seems  that 
the  pineal  apparatus  is  an  organ  concerned  with  adjustment  of  the 
internal  activities  of  the  animal  to  correspond  to  the  changing  con- 
ditions of  illumination.  The  control  may  be  effected  by  impulses 


io6 


VERTEBRATES  WITHOUT  JAWS 


carried  in  the  large  tract  that  proceeds  from  the  habenular  ganglion 
to  the  hypothalamus,  in  the  floor  of  the  diencephalon.  The  latter  is 
known  to  be  concerned,  throughout  the  vertebrate  series,  with  the 
integration  of  the  internal  activities  of  the  animal. 


¥dY 


pner. 


p.  int. 


pant 


Fig.  68.  Sagittal  section  of  the  pituitary  gland  of  lamprey. 

dien.  diencephalon;  inf.  infundibulum;  p.ant.,  p.int.,  and  p. tier,  partes  anterior,  intermedia, 

and  nervosa,  there  are  two  types  of  cell  in  the  pars  anterior;  3rd  V.  third  ventricle. 

(After  Stendell.) 


3  4  5  6 

Hours  after  operation 

FlG.  69.  Onset  of  pallor  in  a  larval  lamprey  after  removal  of  the  pituitary  gland, 
as  shown  by  the  decline  in  the  melanophore  index.  (From  Young.) 

1 1 .  Pituitary  body  and  hypophysial  sac 

The  lower  portion  of  the  diencephalon,  the  hypothalamus,  forms 
a  prominent  pair  of  sacs,  the  lobi  inferiores,  which  contain  a  partly 
separated  diverticulum  of  the  third  ventricle  and  end  below  in  the 
infundibulum  (Fig.  65).  The  pituitary  gland  (hypophysis)  is  pressed 
against  the  underside  of  the  hypothalamus  (Fig.  68).  The  lower  wall 
of  the  brain  in  this  region  consists  not  of  nerve-cells  but  of  a  single 


IV.  II 


PITUITARY  OF  LAMPREYS 


107 


-^fMvn/w^^ 


epithelial  layer,  corresponding  to  the  pars  nervosa  of  the  pituitary  of 
higher  forms.  The  major  portion  of  the  pituitary  gland  is  a  mass  of 
secreting  cells  in  which  two  parts  can  be  recognized,  the  partes 
anterior  and  intermedia.  After  experimental  removal  of  the  inter- 
mediate portion  of  the  pituitary  lam- 
preys become  permanently  pale  in 
colour  (Fig.  69),  showing  that,  as  in 
other  vertebrates  (p.  299),  a  melano- 
phore-expanding  substance  is  liberated 
into  the  blood  by  this  gland,  the  secre- 
tion being  presumably  under  the  control 
of  the  pineal  eyes  (p.  105).  The  lamprey 
pituitary  has  been  shown  to  contain 
oxytocic  and  'water  balance'  hormones 
as  well  as  one  producing  melanophore 
expansion.  Moreover  injections  of 
mammalian  anterior  pituitary  extracts 
induce  appearance  of  the  secondary 
sexual  characters  of  lampreys.  Evi- 
dently the  functions  of  the  pituitary 
have  remained  essentially  the  same 
through  the  whole  chordate  series. 

The  pituitary  of  lampreys  is  peculiar 
because  of  great  development  of  the 
naso-hypophysial  sac  (Fig.  70).  Charac- 
teristically in  vertebrates  the  pituitary 
body  develops  by  the  formation  of  a 
pocket  of  buccal  ectoderm,  whose  walls 
then  become  folded,  so  that  the  part 
in  front  of  the  lumen  becomes  the  pars 
anterior,  that  behind  the  pars  inter- 
media. In  nearly  all  vertebrates  the 
lumen  then  loses  its  connexion  with  the 
exterior.  In  lampreys  the  hypophysial 
rudiment  is  continuous  with  that  of  the 
olfactory  epithelium.  The  latter  then 
moves    dorsally    and    the   two   remain 

connected  throughout  larval  life  by  a  strand  of  cells.  At  metamorphosis 
this  acquires  a  lumen  and  forms  a  tube  extending  from  the  nostril 
below  the  pituitary  and  brain.  Because  of  its  development  this  is 
sometimes  called  the  naso-hypophysial  tube  but  others  doubt  that 


Fig.  70.  Dissection  of  lamprey  from 
the  ventral  surface  after  injection 
of  coloured  gelatine  to  show  the 
outline  of  the  naso-hypophysial  sac 
(.1)  and  its  duct  (d),  which  is  shown 
dotted  where  it  runs  upwards  be- 
tween the  nasal  sacs  («).  g,  gill 
pouches.  Contraction  of  the  bran- 
chial apparatus  squeezes  the  sac  s, 
so  that  water  is  drawn  in  at  each 
relaxation. 


io8 


VERTEBRATES  WITHOUT  JAWS 


IV.  II- 


it    represents  the    cavity   of   the   hypophysis  and  prefer  the  name 
nasopalatine  canal. 

Inside  the  single  nostril,  guarded  by  a  valve,  are  openings  into  the 
nasal  sacs,  which  are  cavities  with  folded  walls.  Some  of  the  cells  of 
these  walls  are  the  olfactory  receptors  and  give  off  the  axons  that  make 
up  the  olfactory  nerves,  entering  the  olfactory  bulbs  on  the  anterior 
end  of  the  hemisphere  (Fig.  65).  Behind  the  nasal  sacs  lie  numerous 
glandular  follicles  opening  into  the  sac  in  the  larva,  but  completely 
closed  in  the  adult  (Fig.  65).  They  may  be  comparable  to  Jacobson's 
organ  (p.  405). 


Fig.  71.  Section  of  lateral  line  organ  of  tail  of  adult  Lampetra. 

p.  pigmented  cells  around  the  pit;  s.c.  receptor  cells 
(not  showing  long  hairs).  (After  Young.) 

The  naso-hypophysial  tube  proceeds  back  behind  the  pituitary  to 
a  closed  sac  lying  between  the  first  pair  of  gill  pouches  (Fig.  70). 
During  the  movements  of  respiration  this  sac  is  squeezed  and  water 
is  expelled  with  some  force  through  the  nostril.  When  the  gills  relax 
water  flows  in  at  the  nostril,  and  in  this  way  the  olfactory  organ  is 
provided  with  samples.  If  the  naso-hypophysial  opening  is  closed  with 
a  plug  of  plasticine  the  lamprey  no  longer  reacts  to  solutions,  for 
instance  of  alcohol,  to  which  it  normally  responds  by  freeing  its 
sucker  and  swimming  away. 

12.  Lateral  line  organs  of  lampreys 

The  lateral  line  receptors,  peculiar  to  fish-like  vertebrates,  are  little 
patches  of  sensory  cells  found  along  certain  lines  on  the  head  and 
trunk.  They  are  all  innervated  by  cranial  nerves,  those  on  the  body 
and  tail  being  served  by  a  special  backward  branch  of  the  vagus  nerve. 
The  receptor  cells  carry  long  hairs  and  are  thus  able  to  detect  either 
movement  of  the  water  relative  to  the  fish  or  of  the  fish  itself.  Objects 
moving  nearby  set  up  disturbances  that  may  also  be  detected  (p.  218). 


v.  i3 


LABYRINTH  OF  LAMPREYS 


109 


In  the  lamprey  the  lateral  line  organs  are  very  simple  (Fig.  71),  being 
open  to  the  exterior  and  not  sunk  in  a  canal  as  in  higher  forms.  The 
rows  are  somewhat  irregular,  especially  those  on  the  body. 

13.  Vestibular  organs  of  lampreys 

The  labyrinth  may  be  considered  as  a  specialized  portion  of  the 
lateral  line  system,  concerned  with  recording  the  position  of  the  head 

end. 


mac.laq.  \        mac.ut. 
3  mac.  sac. 


smp.p. 


amp  a. 


Fig.   72.   Labyrinth  of  right  side,  seen  in  lateral  view.  A  and  B, 

Lampetrci,  c,  Myxitie. 

a.c.  anterior  canal;  amp. a.  and  p.  anterior  and  posterior  ampullae;  cil. 

ciliated  chamber;    cr.a.  and  p.  cristae;    end.  endolymphatic  duct;  lag. 

lagena;    mac.    lag.,    neg.,    sacc,    ut.    maculae    of    the    lagena,    neglecta, 

saccule,  and  utricle;  p.c.  posterior  canal.  (After  de  Burlet.) 

and  angular  accelerations.  There  is  no  evidence  to  decide  whether 
lampreys  can  respond  to  sound.  The  labyrinth  develops  by  an  in- 
pushing  of  the  wall  of  the  head,  and  this  then  becomes  closed  off  from 
the  exterior.  Internal  foldings  divide  up  the  sac  into  a  number  of 
chambers,  which  differ  considerably  from  those  of  gnathostomes. 
There  is  a  large  central  vestibule,  into  which  open  below  several 
partially  separate  sacs,  provided  with  patches  of  sensory  hairs.  These 
correspond,  from  in  front  backwards,  to  the  maculae  of  the  utricle, 
saccule,  and  lagena  of  higher  forms  (Fig.  72).  The  hairs  of  the  maculae 
are  loaded  with  otoliths.  There  are  only  two  broad  semicircular 
canals,  corresponding  to  the  anterior  and  posterior  vertical  canals 
of  other  vertebrates,  each  with  an  ampulla,  containing  a  receptor 
ridge,  the  crista.  Also  opening  to  the  vestibule  are  two  large  sacs, 


no  VERTEBRATES  WITHOUT  JAWS  iv.  13- 

covered  with  cilia  (Fig.  72),  whose  beat  produces  complicated 
counter  currents  in  the  dorso-ventral  plane.  It  has  been  suggested 
that  these  function  as  a  gyroscope,  compensating  for  the  absence  of 
a  horizontal  canal. 

In  Myxine  the  condition  is  even  simpler,  there  being  only  a  single 
vertical  semicircular  canal  (Fig.  72).  However,  it  is  claimed  that  this 


Fig.  73.  Horizontal  section  of  the  eye  of  a  lamprey. 

er.,  ir.,  sr.,  external,  internal,  and  superior  rectus  muscles;  v.v.  venous  sinuses  which  cushion 
the  eye.  (From  Walls,  The  Vertebrate  Eye,  Cranbrook  Institute  of  Science.) 

has  cristae  at  both  ends.  The  macular  system  also  does  not  show  the 
characteristic  subdivisions  but  is  a  single  macula  communis. 


14.  Paired  eyes  of  lampreys 

The  structure  of  the  paired  eyes  is  similar  to  that  in  other  verte- 
brates. They  are  formed,  like  the  pineal  eyes,  by  evaginations  of  the 
wall  of  the  diencephalon;  the  so-called  optic  nerve  is  therefore  not 
really  a  peripheral  nerve  but  a  portion  of  the  brain;  it  should  strictly 
be  called  the  optic  tract.  The  eyes  are  moved  by  extrinsic  muscles 
arranged  in  a  somewhat  unusual  manner.  Accommodation  is  effected 
by  a  process  found  in  no  other  vertebrates.  The  cornea  consists  of  two 
distinct  layers,  separated  by  a  gelatinous  substance.  Attached  to  the 
outer  (or  dermoid)  cornea  is  a  cornealis  muscle,  apparently  of  myo- 
tomal  origin,  which  flattens  the  cornea  and  pushes  the  lens  closer 
to  the  retina  (Fig.  73).  There  is  an  iris,  outlining  a  round  pupil,  which 
changes  little,  if  at  all,  in  diameter  under  different  illuminations.  Most 
species  of  lampreys  are  diurnal  animals.  They  are  said  to  move  towards 


iv.  is 


PHOTORECEPTORS  OF  LAMPREYS 


white  objects  and  probably  use  both  the  eyes  and  the  nose  to  find 
their  prey.  In  the  ammocoete  larva  the  paired  eyes  are  buried  below 
the  pigmented  skin  and  the  animal  makes  no  movements  when  light 
is  shone  on  to  this  region. 

The  optic  tracts  of  adult  lampreys  end  in  the  roof  of  the  midbrain 
(tectum  opticum)  which  is  a  highly  differentiated,  stratified  region. 
Besides  the  optic  fibres  it  receives  also  impulses  from  fibres  ascending 
from  the  spinal  cord  and  others  from  the  auditory  and  lateral  line 


Fig.  74.  Experiment  to  show  behaviour  of  larval  lampreys  when  illuminated.  The 
tank  is  left  in  total  darkness  and  the  larvae  settle  in  all  parts.  When  the  light  is 
switched  on  those  in  the  illuminated  part  begin  to  swim  and  continue  to  do  so  until 
by  chance  they  arrive  in  the  darkened  part,  where  they  settle  down.  (From  Young.) 

centres.  The  midbrain  is  therefore  undoubtedly  one  of  the  most 
important  parts  of  the  brain  in  lampreys,  though  nothing  is  known  in 
detail  of  its  functions.  Its  cells  control  movements  of  the  animal,  by 
means  of  fibres  that  run  to  make  connexion  with  the  dendrites  of  the 
large  Midler's  cells,  whose  axons  pass  down  the  spinal  cord;  other 
fibres  from  the  tectum  opticum  reach  to  various  parts  of  the  brain, 
and  it  is  probable  that  its  activities  are  closely  correlated  with  those  of 
many  other  regions. 


15.  Skin  photoreceptors 

Like  many  lower  vertebrates  the  lamprey  has  light-sensitive  cells  in 
the  skin,  as  well  as  those  in  the  eyes.  These  receptors  are  abundant  in 
the  tail  and  if  a  light  is  shone  on  to  this  region  the  animal  rapidly 
moves  away  (Figs.  74  and  76).  If  the  spinal  cord  is  cut  just  behind  the 
head  and  a  light  then  shone  on  to  the  tail,  the  head  will  be  seen  to 
move.  This  suggests  that  the  impulses  are  carried  forwards  by  means 
of  the  lateral  line  nerves,  which  is  confirmed  by  the  fact  that  if  these 
latter  are  sectioned,  leaving  the  spinal  cord  intact,  then  no  movements 
follow  when  the  tail  is  illuminated.  This  sensitivity  of  the  lateral  line 


ii2  VERTEBRATES  WITHOUT  JAWS  iv.  15- 

organs  to  light  is  not  found  in  other  fish-like  vertebrates.  Indeed  the 
receptors  are  not  strictly  lateral  line  organs  but  pigmented  epidermal 
cells.  The  sensitivity  curve  shows  a  sharp  peak  at  530  m/x,  this  being 
the  region  of  the  spectrum  at  which  light  penetrates  farthest  into  sea 
water.  The  pigment  is  probably  a  porphyropsin  (Steven,  1950). 

In  hag-fishes  (Myxine)  the  head  and  cloacal  regions  are  more 
sensitive  to  light  than  is  the  rest  of  the  body.  The  impulses  from  the 
skin  are  conducted  through  the  spinal  nerves  in  these  animals,  not 
the  lateral  line  nerves. 

16.  Habits  and  life-history  of  lampreys 

We  have  very  little  information  about  the  life  of  lampreys  during 
the  time  that  they  are  in  the  sea.  They  are  caught  in  considerable 
number  attached  to  other  fishes.  It  is  not  known  how  many  years  a 
lamprey  spends  in  the  sea,  but  it  returns  only  once  to  the  river  for 
spawning  and  dies  after  this  act.  The  up-river  migration  of  L.  fluvi- 
atilis  occurs  in  the  autumn,  for  instance  large  numbers  come  up  the 
River  Severn  and  are  caught  in  traps  on  the  way,  for  use  as  food.  The 
spawning  migrations  of  lampreys  may  take  them  for  hundreds  of 
miles,  for  example,  those  of  the  eastern  Pacific  ascend  to  the  head- 
waters of  the  Columbia  River.  They  are  said  to  perform  remarkable 
feats  of  climbing,  leaping  from  stone  to  stone  and  hanging  on  by  their 
suckers.  During  this  period  of  migration  some  lampreys  assume 
brilliant  orange  and  black  colour  patterns.  On  the  other  hand,  lam- 
preys land-locked  in  the  lakes  of  New  York  (Petromyzon  marinus 
unicolor)  feed  in  fresh  water  and  ascend  only  a  few  miles  up  streams 
to  breed. 

Once  in  the  river  the  lampreys  do  not  feed  again  but  live  over  the 
winter  on  the  reserves  accumulated  in  the  form  of  fat,  especially  under 
the  skin  and  in  the  muscles.  During  the  winter  the  gonads  ripen  pro- 
gressively and  the  secondary  sexual  characters  begin  to  become  appar- 
ent only  in  February.  The  females  then  develop  a  large  anal  fin,  while 
in  the  male  a  penis-like  organ  appears  (Fig.  47)  and  the  base  of  the 
dorsal  fin  becomes  thickened. 

Spawning  occurs  in  the  spring  and  is  preceded  by  a  form  of  nest- 
building.  Numerous  lampreys  collect  together,  usually  at  a  place 
below  a  weir  where  the  water  is  shallow  and  rather  swift,  and  the 
bottom  both  stony  and  sandy.  Stones  are  then  dragged  by  the  mouth 
in  such  a  way  as  to  make  a  small  depression.  Fertilization  is  secured 
by  a  process  of  copulation  in  which  the  male  fixes  by  the  sucker  on  to 
the  fore-part  of  the  female  and  the  two  then  become  intertwined  and 


iv.  1 6 


REPRODUCTION   OF  LAMPREYS 


"3 


undergo  rapid  contortions,  the  eggs  being  squeezed  into  the  water, 
while  sperms  are  ejected  through  the  'penis'  (Fig.  75).  Fertilization 
is  therefore  external,  but  the  sperms  must  be  placed  very  close  to  the 


Fig.  75.  Spawning  lampreys  seen  in  their  nest. 
(After  Gage.) 

eggs,  for  they  remain  active  only  for  about  one  minute  after  entering 
the  fresh  water,  which  provides  the  stimulus  that  activates  them.  The 
eggs  and  sperms  are  not  all  laid  at  once;  mating  is  repeated  several 
times  until  all  the  products  have  been  shed,  after  which  the  animals 
are  exhausted  and  soon  die.  The  movements  of  the  animals  stir  up 
the  sand  in  the  nest  (this  is  probably  the  function  of  the  anal  fin  of 
the  female)  ensuring  that  the  eggs  are  covered  up  as  they  are  carried 
away  by  the  current. 


ii4  VERTEBRATES  WITHOUT  JAWS  iv.  17 

17.  The  ammocoete  larva 

The  eggs  contain  a  considerable  quantity  of  yolk,  but  their  cleavage 
is  total  and  proceeds  in  a  manner  not  unlike  that  of  the  frog.  After 
about  three  weeks  the  young  hatches  as  the  ammocoete  larva,  about 
7  mm  long.  At  first  this  is  a  tiny  transparent  creature,  but  its  larval 
life  lasts  for  a  long  time,  during  which  it  grows  into  an  opaque  eel-like 
fish,  up  to  170  mm  long  (Fig.  76). 


Fig.  76.  Ammocoete  larva  of  Lampetra planeri,  showing  the  effect  of  shining  a  narrow 

beam  of  light  on  to  various  parts  of  the  side  of  the  body.  Illumination  of  1,  2,  or  8  is 

followed  by  movement  after  a  few  seconds,  but  no  movement  follows  illumination  at 

points  3-7.  (From  Young.) 


end. 


Fig.  77.  Young  ammocoete  larva  of  lamprey  fixed  while  feeding  on  green  flagellates 
and  detritus  and  then  stained  and  cleared. 

an.  auditory  sac;  br.  brain  (covered  by  meninges);  e.  eye;  end.  endostyle  \f.c.  food  cord  in 
pharynx;  h.  heart;  /.  liver;  m.  mid-gut;  oes.  oesophagus;  v.  velar  fold. 

This  portion  of  life  is  spent  buried  in  the  mud,  the  animals  emerg- 
ing only  occasionally  to  change  their  feeding-ground,  presumably  if 
the  mud  is  not  sufficiently  nutritious.  There  is  no  sucker,  the  mouth 
being  surrounded  by  an  oral  hood  rather  like  that  of  amphioxus  (Fig. 
77).  The  paired  eyes  are  covered  by  muscles  and  skin.  The  head  at 
this  stage  is  little  sensitive  to  light,  but  the  animal  quickly  begins  to 
swim  if  the  tail  is  illuminated.  We  have  seen  already  (p.  108)  that  in 
lampreys  there  are  photoreceptors  in  the  tail,  connected  with  the 
lateral  line  nerves.  In  the  larva  these  are  the  main  photoreceptors,  and 
they  ensure  that  the  animal  lies  completely  buried. 

If  a  number  of  larvae  are  left  in  a  vessel  with  a  layer  of  mud  on  the 


iv.  i7 


AMMOCOETE  LARVA 
r  2  3 


H5 


Fig.  78.  Development  of  the  endostyle  of  the  lamprey.  Sagittal  sections  through 

the  head  at  three  stages. 

1,  auditory  sac;  2,  medullary  tube;  3,  myotome;  4,  conus  arteriosus;  5,  endostyle;  6,  first 

gill-slit;  7,  first  arterial  arch;  8,  notochord;  9,  inpushings  which  cut  off  the  endostyle  from 

the  pharynx;  10,  aorta;  11,  stomodaeum.  (After  Dohrn,  from  Kukenthal.) 

bottom  they  rapidly  disappear  and  remain  hidden  indefinitely,  the 
heads  perhaps  just  visible  in  small  depressions  made  by  the  rhythmic 
respiratory  movements.  When  disturbed  they  always  swim  with  the 
head  downwards  and  in  contact  when  possible  with  the  ground.  This 
habit  leads  them  to  burrow  rapidly.  It  is  not  known  whether  they 
have  other  receptors  to  guide  them  to  mud  rich  in  possible  food 
organisms.  The  nasal  and  hypophysial  sacs  are  poorly  developed  in  the 
larva,  and  the  sense  of  smell  can  hardly  serve  this  purpose. 


(n6) 


t.m 


bEd. 


Fig.  79.  A,  Transverse  section  of  endostyle  of  ammocoete  larva. 

cav.  cavity  of  the  gland;  cil.g.  ciliated  groove  in  floor  of  pharynx;  lam.  lamellae  of  gills; 
ph.  cavity  of  pharynx;  seer,  mucus-secreting  cells  of  the  gland. 

b,  Transverse  section  of  thyroid  follicles  of  adult.  (After  Young  and  Bellerby.) 

C,  Cross  section  of  endostyle  of  ammocoetes  larva  of  Petromyzon  tnarinus  at  level 
where  it  is  connected  by  a  duct  to  the  pharynx.  Autoradiograph  showing  distribu- 
tion of  protein-bound  I131.  The  radioactive  clumps  of  cellular  debris  in  the 
glandular  lumen  and  in  the  duct  suggest  that  the  material  represents  a  holocrine 
secretion,  which  will  probably  be  absorbed  in  the  intestine. 

d.  duct;  hs.  cellular  debris;  ph.  pharynx;  t  II  d.  type  II  dorsal  cells; 
t  III  epithelial  cells, 


iv.  17  FEEDING  OF  AMMOCOETE  LARVA  117 

Feeding  takes  place  by  the  intake  of  water  through  the  mouth  and 
the  separation  of  small  food  particles  from  it  in  the  pharynx  (Fig.  77). 
For  this  purpose  there  is  used  a  great  quantity  of  mucus,  which  is 
secreted  by  the  endostyle  and  gathered  into  a  strand  by  the  cilia  of 
the  pharynx.  This  endostyle  is  a  most  remarkable  organ,  forming  early 
in  development  as  a  sac  below  the  pharynx  (Fig.  78).  It  consists  of  a 
pair  of  tubes,  on  the  floor  of  which  there  are  four  rows  of  secretory 
cells  (Fig.  79).  There  is  a  single  opening  to  the  pharynx,  by  a  slit 
at  about  the  middle  of  the  length.  As  development  proceeds  the  inner 
rows  of  cells  at  the  hind  part  of  the  organ  become  coiled  upwards,  and 
at  the  end  of  larval  life  the  endostyle  therefore  forms  a  very  large  mass 
below  the  pharynx,  composed  of  tubes  lined  partly  by  secretory  and 
partly  by  ciliated  cells.  Probably  no  enzymes  are  secreted  by  the 
endostyle,  its  function  being  to  produce  mucus  in  which  the  food 
particles  become  entangled.  Although  it  resembles  the  endostyle  of 
amphioxus  in  the  arrangement  of  the  secretory  columns,  there  is  a 
difference  in  that  the  organ  in  the  ammocoete  larva  is  not  an  open 
groove.  There  is,  however,  a  ciliated  groove  in  the  floor  of  the  pharynx, 
that  is  to  say,  on  the  roof  of  the  endostyle  (Fig.  79). 

The  details  of  the  feeding-currents  of  the  ammocoete  larva  are  not 
understood.  An  important  difference  from  the  arrangement  in  am- 
phioxus is  that  the  current  is  produced  by  muscular  rather  than  ciliary 
action.  The  velum,  a  pair  of  muscular  flaps,  provides  the  main  current 
when  the  animal  is  at  rest.  The  branchial  basket  can  also  be  expanded 
and  contracted  by  an  elaborate  system  of  muscles.  It  is  not  easy  to 
observe  how  the  food  particles  are  taken  up  from  the  current,  but 
apparently  a  strand  of  mucus  shoots  from  the  endostyle  and  occupies 
the  whole  of  the  centre  of  the  pharynx  (Fig.  77).  This  strand  probably 
rotates  and  as  it  passes  backwards  into  the  eosophagus  it  catches  the 
particles. 

Evidently  the  system  enables  the  animals  to  feed  efficiently  on  the 
small  unicellular  algae  and  bacteria  of  the  mud.  In  amphioxus  the 
ciliated  pharynx,  occupying  a  considerable  proportion  of  the  whole 
surface,  is  only  able  to  support  a  tiny  creature,  but  the  muscular 
feeding-system  of  the  ammocoete  allows  a  relatively  small  pharynx  to 
feed  a  fish  170  mm  long  and  weighing  up  to  10  grams.  This  use  of 
muscles  for  moving  the  gills  was  evidently  an  important  step  in 
chordate  evolution.  It  allowed  the  animals  to  escape  from  the  limita- 
tion of  size  imposed  by  the  ciliary  method  of  feeding.  After  the 
development  of  jaws  to  form  a  still  more  efficient  feeding  mechanism 
the  rhythmic  movement  of  the  branchial  apparatus  persisted  for  the 


n8  VERTEBRATES  WITHOUT  JAWS  iv.  17- 

purpose  of  respiration.  We  cannot  be  certain  about  changes  which 
occurred  so  long  ago,  but  it  seems  likely  that  the  respiratory  move- 
ments of  a  fish  were  first  introduced  to  provide  food  rather  than 
oxygen. 

The  endostyle  therefore  shows  the  survival  of  the  primitive  feeding- 
methods  of  chordates,  but  it  also  undergoes  at  metamorphosis  an 
astonishing  change  into  a  thyroid  gland.  The  mucus-secreting  columns 
shrink  and  the  whole  organ  becomes  reduced  to  a  row  of  closed  sacs, 
lying  below  the  pharynx  (Fig.  79  b).  Each  of  these  sacs  is  lined  by  an 
epithelium,  contains  a  structureless  'colloid'  substance,  and  is  there- 
fore closely  similar  to  a  thyroid  vesicle.  Moreover,  experiments  have 
shown  that  extracts  of  this  organ  contain  iodine  and  exert  an  accelerat- 
ing effect  on  the  metamorphosis  of  frog  tadpoles.  Although  nothing  is 
known  of  the  part  played  by  the  secretion  of  this  gland  in  the  life  of 
the  adult  lamprey,  we  may  safely  conclude  that  we  have  here  the 
conversion  of  an  externally  secreting  feeding-organ  into  a  gland,  of 
internal  secretion.  The  actual  mucus-secreting  cells  are  not  trans- 
formed into  those  of  the  thyroid  follicles,  these  latter  are  derived  from 
epithelial  cells  in  the  wall  of  the  larval  organ.  One  cannot  avoid  specu- 
lating on  this  extraordinary  change  of  function.  It  may  perhaps  be 
significant  that  the  endocrine  gland  that  regulates  basal  metabolism 
(the  thyroid)  is  derived  from  the  part  of  the  feeding-system  that  in 
the  earliest  chordates  was  responsible  for  providing  the  raw  materials 
of  metabolism.  Experiments  with  radioactive  iodine  show  that  this 
element  is  concentrated  in  certain  cells  of  the  larval  endostyle  (Fig. 
79  c).  Moreover,  after  addition  of  the  anti-thyroid  substance  thiourea 
to  the  water  there  are  changes  in  the  endostyle.  Thyroxine  has  been 
extracted  from  the  gland  and  it  probably  has  an  endocrine  function 
as  well  as  secreting  mucus,  though  no  one  has  ever  produced  any 
changes  in  larval  lampreys  by  administering  thyroid  hormones. 
Lampreys  thus  show,  as  larvae,  a  stage  in  which  the  accumulation  of 
iodoproteins,  previously  widespread,  becomes  concentrated  in  the 
pharynx.  Perhaps  at  this  site  there  were  already  cells  specialized  for 
halide  transport  (cf.  the  chloride-secreting  cells  of  teleosts,  used  for 
osmogulation,  p.  203).  In  adult  lampreys  and  all  higher  chordates  the 
iodoprotein  is  secreted  into  the  blood  under  the  control  of  blood- 
borne  signals  (Fig.  80).  The  change  may  well  be  related  to  develop- 
ments in  the  regulation  of  metabolism,  which,  in  the  animals  with  a 
fully  endocrine  thyroid  becomes  more  nearly  independent  of  varia- 
tions in  the  external  supply  of  iodine. 

The  great  change  in  the  endostyle  is  only  part  of  the  complete 


RACES  OF  LAMPREYS 


119 


metamorphosis  by  which  the  ammocoete  larva  changes  into  an  adult 
lamprey.  The  mouth  becomes  rounded  and  its  teeth,  tongue,  and 
complex  musculature  develop.  The  paired  eyes  (previously  buried) 
appear;  the  olfactory  organ  becomes  internally  folded,  and  the  olfac- 
tory nerve  and  tracts  much  enlarged.  The  naso-hypophysial  sac  grows 
backwards  to  the  gills.  In  the  pharynx  the  gills  develop  into  sacs 
opening  to  the  branchial  chamber.  Changes  also  take  place  in  the 


B 


Fig.  80.  Diagram  to  show  distribution  of  iodoproteins,  at  first  in  exoskelctal  struc- 
tures, as  in  many  invertebrates  and  in  tunicates  (a).  Some  of  this  material  is 
concentrated  in  the  pharynx.  This  tendency  is  exaggerated  in  amphioxus  and  the 
ammocoete  larva,  and  in  the  adult  lamprey  and  later  animals  this  pharyngeal 
material  forms  the  thyroid.  A.  Many  invertebrates  and  tunicates ;  n.  Amphioxus ; 
c.  Ammocoetes;  D.  Metamorphosis  of  ammocoetes;  e.  General  vertebrate  type. 
(After  Gorbmann,  A.,  in  Comparative  Endocrinology.  Wiley,  New  York.) 

intestine.  The  yellow-brown  colour  of  the  larva  gives  place  to  the 
black  with  silver  underside  of  the  adult.  The  animal  more  and  more 
frequently  leaves  the  mud  and  finally  migrates  to  the  sea  to  begin  its 
parasitic  life. 

18.  Races  of  lampreys,  a  problem  in  systematics 

Besides  the  river  lampreys,  such  as  L.  fliwiatilis  (Linn.),  which 
show  this  characteristic  migratory  life-history,  there  are  also  in  various 
parts  of  the  northern  hemisphere  small  brook  lampreys  ('prides'), 
such  as  L.  planeri  Bloch,  which  remain  throughout  their  life  in  fresh 
water.  These  prides  are  very  abundant  in  many  English  rivers  and 
streams,  but  since  the  greater  part  of  their  life  is  passed  in  the  am- 
mocoete stage  they  are  not  often  seen.  The  larvae  remain  in  the  mud 


izo  VERTEBRATES  WITHOUT  JAWS  iv.  18 

probably  for  three  years  and  undergo  metamorphosis  in  late  summer 
and  autumn.  The  characteristic  of  this  type  of  lamprey  is  that  the 
adults  never  migrate  and  never  feed.  The  gonads  are  already  well 
developed  at  metamorphosis  and  ripen  during  the  winter.  Spawning 
takes  place  in  March  or  April  and  the  animals  then  die. 

There  has  been  much  dispute  about  the  status  of  these  freshwater 
races.  In  structure  the  adult  L.  planeri  is  nearly  if  not  quite  identical 
with  an  adult  L.fiuviatilis,  except  that  the  latter  is  much  the  larger  and 
has  sharper  teeth.  Crossing  of  the  two  sorts  could  presumably  never 
take  place  in  nature,  on  account  of  the  size  difference,  but  by  artificial 
stripping  of  the  adults  cross-fertilization  in  both  directions  can  easily 
be  achieved.  Unfortunately  the  hybrid  larvae  have  never  been  reared 
to  maturity;  we  cannot  therefore  say  whether  the  small  size  and 
failure  to  migrate  of  the  planeri  forms  are  inherited  characters  or 
are  produced  by  the  influence  of  the  environment.  The  effect  of  the 
non-migratory  condition  is  to  enable  the  lampreys  to  colonize  very 
fully  rivers  that,  because  of  effluents,  they  would  be  unable  to  occupy 
if  a  migration  to  the  sea  was  necessary.  By  this  process  of  acceleration 
of  the  development  of  the  gonads  a  dangerous  stage  in  the  life-history 
has  been  avoided. 

Similar  pairs  of  migratory  and  non-migratory  forms  of  lamprey  are 
found  in  Japan  and  in  North  America.  Indeed,  the  condition  appears 
to  be  developing  independently  in  several  river  systems  in  the  United 
States.  Since  it  may  be  difficult  for  the  brook  lampreys  to  spread 
from  one  river  system  to  another  it  is  possible  that  many  of  the 
planeri  forms  have  evolved  separately,  perhaps  quite  recently.  If  so, 
this  is  a  remarkable  example  of  a  similar  response  produced  in  different 
parts  of  a  population  by  a  similar  environmental  stimulus,  in  this 
case  the  effluents.  This  process  of  alteration  in  the  relative  times  of 
metamorphosis  and  sexual  maturity  (paedomorphosis)  has  occurred 
also  in  certain  amphibians  (the  axolotl)  and  in  tunicates  (Larvacea). 
Similar  changes  in  rates  of  development  may  have  been  essential 
factors  in  the  development  of  the  whole  chordate  phylum  (p.  77). 

In  one  race,  found  in  Italy,  ammocoetes  with  mature  gonads  have 
been  reported.  However,  in  most  of  these  lampreys  the  paedomor- 
phosis is  only  partial :  metamorphosis  does  take  place,  but  is  immedi- 
ately followed  by  maturity.  Since  in  mammals  injections  of  anterior 
pituitary  extracts  accelerate  development  of  the  gonads,  it  was  thought 
possible  that  complete  neoteny  might  be  produced  by  making  such 
injections  into  larvae  of  L.  planeri.  No  completely  sexually  mature 
ammocoetes  have  yet  been  produced  by  this  method,  but  following 


iv.  18  NOMENCLATURE  FOR  LAMPREYS  121 

the  injections  the  larvae  assumed  the  secondary  sexual  characters, 
which  are  normally  shown  only  at  maturity,  namely,  swelling  of  the 
cloaca,  opening  of  the  pore  from  coelom  to  exterior,  and  the  changes 
in  body  form.  No  signs  of  metamorphosis  were  produced  by  these 
injections  and  we  are  left  without  information  as  to  the  cause  of  that 
change  in  the  lamprey.  In  Amphibia  even  very  young  larvae  undergo 
metamorphosis  when  treated  with  thyroid  extracts,  but  similar  treat- 
ment of  ammocoete  larvae  has  failed  to  produce  any  change.  Further 
investigation  of  the  problem  should  be  very  interesting,  since  it  seems 
likely  that  the  differences  between  the  fluviatilis  and  planeri  forms  are 
the  result  of  an  endocrine  factor  accelerating  the  onset  of  sexual 
maturity  in  the  latter.  The  fact  that  the  change  is  occurring  in  various 
parts  of  the  world  adds  further  interest  to  this  example  of  evolution 
in  progress. 

Besides  all  these  relatively  small  lampreys,  there  is  a  much  larger 
form,  the  sea  lamprey,  Petromyzon  marinns  Linn.,  reaching  to  over  a 
metre  in  length.  This  animal  differs  from  Lampetra  in  body  form, 
structure  of  sucker,  and  other  features,  as  well  as  in  size.  Like  most 
other  groups  of  animals  lampreys  therefore  present  several  problems 
of  nomenclature.  Linnaeus  included  the  three  types  that  occur  in 
Europe  in  the  one  genus  Petromyzon ;  since  they  are  all  rather  alike  in 
shape  this  is  in  some  ways  a  reasonable  procedure.  But  are  we  then 
also  to  include  in  the  same  genus  forms  that  differ  more  widely,  such 
as  those  occurring  in  the  southern  hemisphere  ?  As  so  often  happens, 
systematists  have  chosen  the  course  of  splitting  up  the  Linnaean 
genus,  even  though  several  of  the  resulting  genera  have  only  one 
species.  Thus  Gray  suggested  the  genus  Lampetra  for  the  brook  and 
river  lampreys,  keeping  Petromyzon  for  the  larger  species  of  sea 
lamprey.  Other  genera  have  been  added,  such  as  Entosphenus  Gill  for 
some  of  the  North  American  forms  and  Mordacia  Gray  and  Geotria 
Gray  for  the  forms  from  the  southern  hemisphere  (Chile,  Australia, 
and  New  Zealand).  Such  distinctions,  though  they  may  seem  irritating 
at  first  sight,  are  an  advantage  in  that  they  call  attention  to  the  differ- 
ences which  exist.  For  instance,  it  is  a  striking  fact  that  lampreys  are 
found  in  temperate  waters  of  both  hemispheres,  but  not  in  the  tropics, 
and  it  is  interesting  to  learn  that  the  forms  from  New  Zealand, 
Australia,  and  South  America  (there  are  none  in  South  Africa)  show 
distinct  peculiarities.  Thus  Geotria  possesses  a  large  sac  behind  the 
sucker. 

A  special  problem  of  nomenclature  arises  from  the  fact  that  the 
river  and  brook  lampreys  are  almost  identical  in  structure  and  differ 


i22  VERTEBRATES  WITHOUT  JAWS  iv.  18- 

mainly  in  size,  time  of  sexual  maturity,  and  habits.  A  further  com- 
plication is  that  the  germ-cells  of  the  two  races  allow  cross-fertiliza- 
tion, although  this  probably  never  occurs  in  nature!  We  may  take 
Dobhzansky's  definition  of  species  as  'groups  of  populations  which 
are  reproductively  isolated  to  the  extent  that  the  exchange  of  genes 
between  them  is  absent  or  so  slow  that  the  genetic  differences  are  not 


Fig.  8i.  Myxine,  partly  dissected. 

i,  cloaca;  2,  testis;  3  and  4,  ovary  with  eggs;  5,  liver;  6,  branchial  opening;  7,  mouth; 
8,  nostril;  9  and  11,  slime  glands;  10,  intestine.  (After  Retzius,  from  Kukenthal.) 

diminished  or  swamped',  and  in  this  sense  we  may  retain  the  specific 
names  L.  fluviatilis  and  L.  planeri  for  the  two  populations. 

19.  Hag-fishes,  order  Myxinoidea 

The  hag-fishes,  Myxine  and  Bdellostoma  (Fig.  8 1 ),  are  animals  highly 
modified  for  sucking.  They  live  buried  in  mud  or  sand  and  probably  eat 
polychaetes  and  other  invertebrates,  as  well  as  scavenging  dead  fishes. 
The  eyes  are  functionless  rudiments,  though  the  animals  are  sensitive 
to  changes  of  illumination,  through  skin  receptors.  There  are  sensory 
tentacles  around  the  mouth,  and  in  both  hag-fishes  the  teeth  and 
sucking  apparatus  are  well  developed.  They  burrow  into  the  bodies 
of  dead  or  dying  fishes.  As  many  as  123  Myxine  have  been  taken  from 
a  single  fish.  Since  the  introduction  of  trawling  they  have  become  less 
common  in  the  North  Sea,  where  they  used  to  be  a  serious  source  of 
loss  to  fishermen  by  their  attacks  on  fishes  caught  in  drift  nets  or  on 
lines.  They  seem  to  find  fish  when  they  are  dying  or  just  dead,  and 
entering  by  the  mouth  of  their  prey  eat  out  the  whole  contents  of  the 
body,  leaving  a  sack  of  skin  and  bones.  When  they  are  themselves 


IV.  19 


HAG-FISHES 


123 


caught  on  lines  (for  instance,  with  a  salted  herring  bait)  the  hook  is 
swallowed  so  deeply  that  it  may  be  found  near  the  anus! 

The  gills  are  modified  into  pouches  (6-14  in  Bdellostoma,  6  in 


-5 


Fig.  82.  Arrangement  of  gills  in  Bdellostoma  and  Myxine. 

1,  tentacles;  2,  wall  of  pharynx ;  3,  branchial  sac  opened  to  show  gill  lamellae;  4,  branchial 

duct;  5,  branchial  sac;  6,  mouth;  7,  common  branchial  aperture  in  Myxine. 

(From  Kukenthal  after  Dean.) 

Myxine),  opening  by  tubes  into  the  pharynx,  and  to  the  exterior  (Fig. 
82).  In  Myxine  all  the  tubes  are  joined  and  open  by  a  single  posterior 
aperture  on  each  side.  Water  enters  at  the  nostril  and  is  pumped  back- 
wards by  a  muscular  velum  through  the  gill  chambers  and  out  behind. 
There  is  also  a  single  posterior  oesophago-cutaneous  duct  on  the  left 
side,  which  is  probably  closed  during  normal  respiration  but  is 
opened  to  allow  expulsion  of  large  particles.  If  the  nostril  is  closed 
experimentally  with  a  plug  no  water  enters  by  the  mouth  or  posterior 
apertures  but  the  fish  survives  well,  presumably  respiring  through  the 
skin. 


124  VERTEBRATES  WITHOUT  JAWS  iv.  19- 

The  thyroid  gland  consists  of  a  long  series  of  sacs  formed  by 
evagination  from  the  floor  of  the  pharynx. 

Down  the  sides  of  the  body  are  pairs  of  slime  glands,  able  to  secrete 
large  amounts  of  mucus,  which  may  be  protective  and  is  said  also  to 
be  produced  under  the  operculum  to  hasten  the  end  of  a  dying  fish 
that  the  hag  has  attacked. 

A  curious  difference  from  the  nervous  system  of  lampreys  is  that 
the  dorsal  and  ventral  roots  join,  though  the  details  suggest  that  the 
union  is  not  similar  to  that  found  in  gnathostome  vertebrates.  The 
brain  shows  several  features  of  reduction  and  simplification  and  no 
pineal  eyes  are  present.  There  is  only  one  semicircular  canal  in  the  ear 
(p.  109).  The  kidneys  show  a  more  generalized  condition  than  in  any 
other  vertebrate  in  that  the  pronephros  persists  in  the  adult  and  is 
hardly  marked  off  from  the  mesonephros,  so  that  an  almost  continu- 
ous series  of  funnels  and  glomeruli  can  be  recognized.  Moreover,  there 
is  a  regular  series  of  mesonephric  glomeruli,  a  pair  in  each  segment. 

The  development  is  known  only  in  Bdellostoma,  where  the  egg  is 
yolky  and  cleavage  partial,  leading  to  the  formation  of  an  embryo 
perched  on  a  mass  of  yolk.  It  is  often  stated  that  Myxine  is  a  protandric 
hermaphrodite,  because  individuals  are  found  in  which  the  front  end 
of  the  gonad  contains  eggs,  whereas  the  hind  part  is  testis-like  (Fig. 
81).  No  ripe  sperms  have  ever  been  found  in  this  region,  however, 
and,  moreover,  individuals  with  fully  testicular  gonads  do  occur. 
Since  it  is  known  that  in  other  vertebrates  (including  the  lampreys) 
the  gonads  go  through  a  hermaphrodite  stage  during  development  it 
seems  likely  that  Myxine  is  not  a  functional  hermaphrodite  but  that 
the  double-sexed  gonad  shows  a  rather  late  persistence  of  the  indeter- 
minate stage. 

The  hag-fishes  all  live  in  the  sea  and  their  blood  differs  from  that  of 
other  chordates  in  that  it  is  isosmotic  with  sea  water.  However,  the 
individual  ions  are  regulated;  sodium  and  phosphate  exceed  their 
values  in  sea  water,  and  the  other  ions  are  present  in  lower  concentra- 
tion. It  is  usually  assumed  that  fishes,  with  their  glomerular  kidneys, 
evolved  in  fresh  water.  However,  the  very  earliest  fragments  of 
armoured  agnathans  are  from  Ordovician  deposits  that  may  be  littoral 
or  marine  and  it  might  be  that  the  condition  of  the  blood  and  kidney 
of  Myxine  is  that  of  the  earliest  agnathans  and  that  the  glomerulus  was 
not  evolved  as  an  adaptation  to  freshwater  life,  as  is  often  supposed 
(Robertson,  1954). 

The  organization  of  the  lampreys  and  hag-fishes  shows  that  they 
preserve  many  characteristics  from  a  very  early  stage  of  chordate 


IV.  20 


FOSSIL  AGNATHANS 


125 


evolution,  probably  that  of  about  the  Silurian  period.  Their  special 
interest  for  us  is  in  giving  an  insight  into  the  organization  possessed 
by  the  vertebrates  before  jaws  were  evolved.  However,  no  doubt  many 
changes  have  gone  on  during  cyclostome  evolution  and  we  must  not 
suppose  that  all  Silurian  vertebrates  were  like  lampreys.  Indeed,  we 
may  now  complete  our  picture  of  this  stage  of  evolution  by  examining 
the  fossil  fishes  known  to  have  existed  at  that  period.  We  shall  find 
them  superficially  so  different  from  modern  cyclostomes  that  only 
careful  morphological  comparison  reveals  the  similarities.  The  inquiry 
will  show  us  once  again  how  a  common  plan  of  organization  can  be 
found  in  animals  of  very  different  superficial  form  and  habits. 


Fig.  83.  A  ccphalaspid  restored  (Hemicyclaspis). 

d.  dorsal  fin;  bf.  lateral  field;  pec.  pectoral  fin;  p.  pineal;  sclr.  sclerotic  ring. 
(From  Stcnsio.) 

20.  Fossil  Agnatha,  the  earliest-known  vertebrates 

The  ostracoderms  are  fossil  forms  from  freshwater  Silurian  and 
Devonian  deposits.  They  are  therefore  the  oldest  fossil  vertebrates 
known  to  us  (except  for  a  few  Ordovician  fragments),  and  this  makes 
it  specially  interesting  that  they  show  affinity  with  the  cyclostomes. 
These  are  fossils  that  are  rarely  found  complete,  particularly  the 
pteraspids,  but  a  quarry  in  Herefordshire  yielded  numerous  whole 
specimens  of  Cephalaspis  and  Pteraspis  of  Old  Red  Sandstone  age, 
probably  all  from  a  single  dried-up  pool. 

In  the  cephalaspids  (Osteostraci)  the  head  was  flattened  and  com- 
posed largely  of  a  shield.  The  rest  of  the  body  was  fish-like,  with  an 
upturned  tail  (heterocercal,  see  p.  136)  covered  with  heavy  bony  scales 
(Fig.  83).  A  pair  of  flaps  behind  the  gills  may  have  functioned  like 
pectoral  fins. 

On  the  dorsal  surface  of  the  shield  are  two  median  holes,  one 
behind  the  other,  which  served  a  naso-hypophysial  opening  and  a 
pineal  eye.  The  whole  outline  of  the  cranial  cavity  is  preserved  and 
shows  a  brain  remarkably  like  that  of  a  lamprey,  with  a  naso-hypo- 
physial canal  below  it  (Fig.  84).  There  were  paired  eyes  and  only  two 


(126) 


eFf.pm 


l.br.l 


Fig.  84.  Head  shield  of  the  ccphalaspid  Kiaeraspis,  see  from  below.  5  X  natural  size. 

car. a.  internal  carotid;  d.ao.  dorsal  aorta;  eff.br. 4.  4th  efferent  branchial;  eff.pm.  efferent  branchial 

of  1st  arch;  i.br.i.  1st  interbranchial  ridge;  oes.  oesophagus;  orb.  depression  made  by  orbit;  vest. 

depression  made  by  vestibular  apparatus.  V1-X2.  Cranial  nerves. 

(After  Stensio.) 


hup.  foss 


orb 


■  C3p  tat 


Mf/m 


Fig.  85.  Cast  of  the  endocranium  and  system  of  canals  in  the  head  shield  of  Kiaeraspis. 
amp.  ampulla  of  posterior  semicirculr  canal;  can.  canal  leading  to  field;  car. a.  carotid  artery; 
hyp.foss.  hypophysial  fossa;  /./.  lateral  'electric'  fields;  med.  medulla  oblongata;  nas.c.  naso- 
hypophysial    canal;  orb.  orbit;  v.cap.lat.  vena  capitis  lateralis;  vest,  vestibular  apparatus;  III-X 

cranial  nerves.  (After  Stensio.) 


iv.  2o  CEPHALASPIDS  127 

semicircular  canals.  Long  tubes  leading  through  the  shield  contained 
the  cranial  nerves,  which  can  be  reconstructed  in  detail  (Fig.  85). 
On  the  under  side  of  the  shield  is  a  series  of  ridges,  which  outline  a 
set  of  ten  pairs  of  branchial  pouches.  The  first  of  these  lies  far  forward 
at  the  sides  of  the  mouth  and  the  ridge  in  front  of  it  is  probably  the 
premandibular  arch;  it  carries  the  profundus  nerve  (p.  152),  which 
was  large.  The  ventral  surface  of  the  head  was  flat  and  covered  with 
small  scales.  Probably  the  gills  were  pouches,  as  in  lampreys.  The 
canals  of  the  aorta,  epibranchial  arteries,  and  some  features  of  the  veins 
and  heart  have  been  preserved. 

The  mouth  was  a  slit  at  the  extreme  front  end  with  which  the 
animals  may  have  scooped  decaying  matter  from  the  lake  floor. 
On  the  dorsal  surface  there  are  sunken  areas,  covered  by  small  scales, 
known  as  the  median  and  lateral  fields,  and  supposed  by  some  to  have 
contained  electric  organs.  They  were  apparently  served  by  a  very  rich 
blood-supply  and  a  system  of  wide  canals  leads  to  the  vestibular 
region.  These  canals  might  have  contained  nerves,  but  Watson  makes 
the  far  more  likely  suggestion  that  they  housed  tubular  extensions  of 
the  labyrinth  and  served  to  carry  pressure  waves  to  the  ear,  perhaps 
providing  a  substitute  reinforcement  for  the  defective  lateral  line 
system. 

We  therefore  know  in  some  respects  as  much  about  these  fossils  as 
of  many  living  fishes.  They  show  in  the  complete  segmentation  of  the 
head  the  most  primitive  condition  known  among  craniates.  Many  of 
their  features  are  very  like  those  of  modern  lampreys  and  there  can  be 
little  doubt  that,  as  Stensio  suggests,  the  latter  represent  their  sur- 
viving descendants,  which  have  lost  the  bony  shield. 

The  Anaspida  (mostly  Silurian)  are  placed  by  Stensio  near  the 
Cephalaspids  but  they  are  less  well  known.  They  were  small  fishes 
(up  to  7  in.  in  length)  covered  with  rows  of  bony  scales  (Fig.  87).  The 
tail  shows  a  lower  lobe  larger  than  the  upper  ('hypocercal').  This 
would  presumably  serve  to  drive  the  head  end  upwards  perhaps  to 
compensate  for  the  weight  of  its  armour.  The  opposite  ('heterocercal') 
condition,  found  in  cephalaspids  and  many  modern  fishes  (for 
instance,  the  dogfish),  produces  a  tendency  to  negative  pitch  and  is 
associated  with  the  presence  of  pectoral  fins  (p.  136).  The  anaspids 
possessed  a  curious  ventral  or  ventro-lateral  fin  fold  (Fig.  87)  or 
perhaps  a  series  of  them.  There  were  large  paired  eyes,  median  holes 
presumed  to  be  nasal  and  pineal  and  a  series  of  up  to  fifteen  small 
round  gill  openings. 

We  may  consider  here  the  fossil  Jamoytius  from  the  Silurian.  The 


i28  VERTEBRATES  WITHOUT  JAWS  iv.  20 

notochord  was  persistent  and  there  was  no  calcined  endoskeleton. 
There  were  long  continuous  lateral  fin  folds  and  a  hypocercal  tail.  A 
series  of  transverse  structures  were  at  first  interpreted  as  myotomes 


Pterolepis 


Rhyncholepis 


sec/. 


pec. 


Rhyncholepis 


Figs.  86  and  87.  Anaspids  seen  in  dorsal  and  lateral  views. 

an.  anal  fin;  na.  nasal  aperture;  orb.  orbit;  pec.  pectoral  spine;  pi.  pineal  foramen; 
ros.  rostrum;  sc.d.  dorsal  scales.  (After  Stensio  and  Kiaer  and  Grasse.) 

but  Stensio  and  Ritchie  (i960)  consider  these  to  be  scales  and  place 
Jamoytins  with  the  Anaspida.  In  either  case,  the  form  is  of  the  greatest 
interest,  and  represents  as  White  says  'the  most  primitive  of  the 
"vertebrate"  series  of  which  we  have  knowledge'.  It  is  suggested  that 
it  might  be  the  ammocoete  larva  of  an  ostracoderm  (Newth). 

The  Heterostraci  are  actually  the  oldest  known  craniates,  since  their 
scales  occur  in  the  Ordovician.  They  were  common  in  the  Silurian 


IV.  20 


HETEROSTRACI 


129 


and  lower  Devonian.  There  were  ventral  as  well  as  dorsal  shields  (Fig. 
88),  and  a  long  series  of  gill  pouches,  but  only  a  single  pair  of  exhalent 
branchial  apertures,  suggesting  to  Watson  respiration  by  a  moving 
flap  (velum).  The  shields  were  of  cell-less  bone  (isopedin)  covered 
with  dentine.  The  body  was  covered  with  scales  of  similar  material. 
The  tail  was  hypocercal  and  there  were  lateral  horizontal  keels  but 
no  fins.  Theie  were  paired  eyes,  two  semicircular  canals  and  clearly 


Fig.  88.  Three  views  of  a  restoration  of  Pteraspis. 
d.sp.  dorsal  spine;  e.  eye;  m.  mouth;  r.  rostrum.  (From  White.) 


marked  lateral  line  canals.  There  was  a  pineal  opening,  closed  in  the 
adult,  but  no  sign  of  the  nostril,  which  may  have  opened  into  the 
mouth.  The  latter  was  surrounded  by  long  plates,  suggesting  that  it 
formed  a  protrusible  apparatus,  which  could  be  pushed  out  to  form 
'a  kind  of  scoop  or  shovel  (Fig.  88)  whereby  mud  and  decaying  refuse 
could  be  taken  off  the  bottom,  for  it  seems  likely  that  such  were  their 
food  and  habit'  (White). 

The  coelolepids  or  thelodonts  are  the  least  known  group  of  agna- 
thans.  The  outer  surface  was  covered  with  fine,  placoid-like  scales  or 
hollow  spines,  which  in  isolation  are  often  found  in  late  Silurian  and 
Early  Devonian  rocks.  The  anterior  end  was  usually  flattened  and 
wide  but  the  body  behind  was  narrow,  with  a  forked,  probably 
hypocercal  tail.  Structures  that  are  probably  eye-spots  occurred 
widely  separated  near  the  front  margin.  The  mouth  was  ventral  and 
traces  of  seven  branchial  arches  have  been  found.  There  were  flap-like 


i3o  VERTEBRATES  WITHOUT  JAWS  iv.  20 

extensions  on  each  side  of  the  head  but  no  paired  fins.  The  only 
median  fin  was  the  anal. 

The  affinities  of  these  ostracoderm  fossils  with  each  other  and  with 
the  cyclostomes  have  been  much  disputed.  Lankester  claimed  that 
pteraspids  were  related  to  cephalaspids  'because  they  are  found  in  the 
same  beds,  because  they  have  a  large  head  shield  and  because  there  is 
nothing  else  with  which  to  associate  them'.  At  the  other  extreme 
Stensio  holds  that  we  have  sufficient  evidence  to  assert  that  the 
pteraspids  have  given  rise  to  the  myxinoids,  and  the  cephalaspids  to 
the  lampreys.  Except  for  the  absence  of  jaws  there  is  indeed  little  in 
common  among  the  fossil  forms.  The  differences  in  the  shape  of  the 
tail  are  especially  baffling.  As  White  points  out,  an  animal  with  a 
heterocercal  tail  and  pectoral  fins  can  hardly  have  lost  either  of  these 
organs  independently.  He  suggests  that  the  earliest  vertebrates  pos- 
sessed straight  ('diphycercal')  tails  and  that  from  these  were  evolved 
on  the  one  hand  the  pteraspids  with  hypocercal  tails  and  on  the  other 
the  cephalaspids  with  upturned  heterocercal  tails.  The  modern  cyclo- 
stomes are  perhaps  derived  from  the  latter,  but  which,  if  either,  group 
gave  rise  to  the  earliest  gnathostomes  is  unknown. 

The  Agnatha  were  the  first  animals  of  the  chordate  type  to  become 
large,  and  they  apparently  all  did  so  by  feeding  on  the  detritus  at  the 
bottom  of  rivers  and  lakes.  They  evolved  into  various  types,  mostly 
rather  heavily  armoured  and  perhaps  slow-moving  forms.  The  lam- 
preys and  hag-fishes  have  been  derived  from  early  Agnatha  by  the 
evolution  of  a  sucking  mouth,  perhaps  with  loss  of  the  bony  skeleton 
and  paired  limbs.  However,  it  was  the  unknown  forms  that  evolved 
a  biting  mouth  that  made  the  next  great  advance  in  vertebrate 
evolution. 


V 

THE  APPEARANCE  OF  JAWS. 
THE  ORGANIZATION  OF  THE  HEAD 

1 .  The  elasmobranchs  :  introduction 

In  all  parts  of  the  sea  there  are  to  be  found  members  of  the  class  of 
the  elasmobranchs  (literally  'plate-gilled'  fishes),  including  sharks 
ranging  from  monsters  of  50  ft  long  to  the  common  dogfish  Scylio- 
rhinus  caniculus  of  1-2  ft.  Nearly  all  the  fishes  in  the  group  are  carni- 
vorous or  scavengers:  the  skates  and  rays  are  bottom-living  relatives, 
feeding  mostly  on  invertebrates.  Although  they  are  not  quite  so  fully 
masters  of  the  water  as  are  the  bony  fishes,  they  are  yet  well  enough 
suited  to  that  element  to  survive  in  great  numbers  in  all  oceans. 
Perhaps  the  skill  and  cunnning  of  a  shark  is  exaggerated  by  the 
frightened  boatman  or  bather,  who  is  apt  to  mistake  a  keen  nose  and 
the  persistence  of  hunger  for  intelligence,  especially  when  he  is  faced 
at  intervals  with  a  well-armed  mouth;  but  the  sharks  have  a  large 
brain  and  their  active,  predacious  habits  enable  many  of  them  to 
live  by  eating  the  more  elaborately  organized  bony  fishes. 

Evidently  such  active  creatures  have  changed  considerably  if  they 
have  been  evolved  from  the  heavily  armoured  and  probably  slow- 
moving  agnathous  vertebrates  that  shovelled  up  food  from  the  bottom 
of  Palaeozoic  seas.  It  used  to  be  supposed  that  these  elasmobranch  or 
cartilage  fishes  represent  a  very  primitive  stock,  but  we  now  realize 
that  there  have  been  great  changes  since  the  biting  mouth  was  first 
evolved;  we  cannot  be  sure  that  any  features  we  find  in  the  elasmo- 
branchs were  possessed  by  the  earliest  gnathostomes. 

The  typical  shark  is  a  long-bodied  fish,  swimming  by  the  passage  of 
waves  of  contraction  along  tne  metamerically  arranged  muscles.  As  in 
the  lampreys  and  eels,  the  wave  that  passes  down  the  body  is  of  short 
period,  relative  to  the  length  of  the  fish,  and  is  therefore  evident  as  it 
travels  along.  This  is  probably  a  less  efficient  system  than  is  provided 
by  the  longer  period  waves  of  the  most  highlv  developed  bonv  fishes; 
the  sharks  are  good  swimmers,  but  except  for  the  mackerel  sharks 
(Isuridae)  not  among  the  swiftest.  Stability  and  control  of  direction 
are  ensured  by  the  upturned  tail  and  the  fins.  The  tail,  with  its  dorsal 
lobe  larger  than  the  ventral,  is  called  heterocercal,  and  tends  to  drive 
the  head  downwards.  This  is  corrected  by  the  flattened  shape  of  the 
head  itself  and  by  the  pectoral  fins,  which  act  as  'aerofoils',  allowing 


i32  THE  APPEARANCE  OF  JAWS  v.  i- 

steering  in  the  horizontal  plane  (p.  140).  There  are  two  dorsal  fins, 
which  secure  stability  against  rolling,  and  also  assist  in  making  possible 
the  vertical  turning  movements. 

The  muscles  for  the  production  of  these  movements  are  a  serial 
metameric  set,  with  longitudinal  fibres,  essentially  like  those  of  the 
lamprey  or  amphioxus.  The  central  axis  is  no  longer  simply  a  rod; 
the  notochord  has  become  surrounded  and  partly  replaced  by  a  series 


df       f    sP.byLd 


ac. 


bw. 


msv.     pr  b. 

Fig.  89.  Diagram  of  the  organization  of  a  vertebrate. 

ac.  wall  of  abdominal  coelom ;  b.  body  wall ;  bd.  basidorsal ;  bv.  basiventral ;  bw.  body  wall ;  dr.  dorsal 

rib;  i.  intestine;  iv.  interventral;  m.  myocomma;  ms.  mesentery;  msd.  median  dorsal  septum;  msv. 

ventral  mesentery;  nes.  neural  tube;  ns.  notochordal  sheath;  pr.  ventral  (pleural)  rib;  sp.  neural 

spine;  ts.  horizontal  septum.  (From  Goodrich.) 

of  vertebrae  (Fig.  89).  These  develop  as  two  pairs  of  cartilaginous 
nodules  in  each  segment,  the  basidorsals  and  basiventrals  behind,  and 
smaller  elements,  the  interdorsals  and  interventrals,  in  the  front.  The 
basiventrals,  lying  on  either  side  of  the  notochord,  form  the  centrum 
of  each  vertebra,  invading  and  almost  interrupting  the  notochord, 
which  widens  again,  however,  between  the  vertebrae.  The  vertebrae 
are  held  together  by  ligaments,  but  are  not  articulated  by  complex 
facets  as  they  are  in  land  animals.  The  basidorsals  form  neural  arches 
above  the  nerve-cord,  and  the  interdorsals  make  intercalary  arches. 
The  interventrals  partly  separate  the  centra.  Attached  to  each  basi- 
ventral is  a  pair  of  transverse  processes,  which  in  the  anterior  region 
bear  short  ribs  and  in  the  tail  are  fused  in  the  midline  to  make  the 
haemal  arches. 

The  median  and  paired  fins  are  supported  by  cartilaginous  rods, 
the  radials,  and  their  edges  are  further  strengthened  by  special  horny 


SWIMMING  OF  FISHES 


i33 


rays,  the  ceratotrichia.  The  radials  of  the  paired  fins  form  a  series 
attached  to  larger  rods  at  the  base.  These  more  basal  rods  are  attached 
to  a  'girdle'  of  cartilage  embedded  in  the  body  wall.  The  pectoral 


Fig.  90.  Successive  positions  of  a  swimming  dogfish  at  intervals  of  o-i  sec.  The 
lines  are  3  in.  apart.  The  passage  of  a  wave  is  marked  by  dots.  (After  Gray.) 


Fig.  91.  Successive  positions  of  a  swimming  eel  at  intervals  of  005  sec.  Scale  3  in. 
The  wave-crests  are  marked.  (After  Gray.) 

girdle  is  a  hoop  extending  some  way  round  the  body,  but  the  pelvic 
girdle  is  simply  a  transverse  rod  in  the  abdominal  wall.  The  origin  of 
these  girdles  and  of  the  fins  will  be  discussed  later  (p.  136). 

2.  The  swimming  of  fishes 

The  propulsive  forces  that  move  a  fish  through  the  water  are  usually 
produced  by  the  longitudinal  muscle-fibres  of  the  myotomes,  but  in 
some  forms  the  propulsion  is  produced  by  movement  of  the  fins, 
whose  function  is  usually  rather  to  give  the  fish  its  stability,  enabling  it 
to  keep  on  a  constant  course,  and  also  to  change  its  course. 


i34  THE  APPEARANCE  OF  JAWS  v.  2 

The  myotomes  consist  of  blocks  of  longitudinal  muscle-fibres, 
placed  on  either  side  of  an  incompressible  central  axis,  the  notochord 

or  vertebral  column.  The  effect  of 
contraction  of  the  muscle-fibres  in  any 
myotome  is  therefore  to  bend  the  body. 
In  forward  swimming  the  contraction 
of  each  myotome  takes  place  after  that 
in  front  of  it.  In  this  way  waves  of 
curvature  are  passed  down  the  body, 
alternately  on  each  side.  This  can  be 
illustrated  by  a  series  of  photographs 
of  a  fish  such  as  the  dogfish  or  eel  in 
which  the  amplitude  of  the  waves  is 
large  (Figs.  90  and  91). 

In  other  fishes  the  waves  are  not  so 
immediately  obvious,  but  serial  photo- 
graphs show  that  even  in  such  forms  as 
the  mackerel  and  whiting  there  is  a 
backward  movement  of  waves.  The 
number  of  waves  per  minute  in  steady 
swimming  varies  from  54  in  the  dog- 
fish to  170  in  the  mackerel,  the 
corresponding  velocities  of  the  waves 
being  55  and  77  and  of  the  whole  fish 
29  and  42-5  cm /sec. 

Gray  has  shown  how  the  muscle 
contractions  produce  movements  of 
the  parts  of  the  body,  related  to  one 
another  in  such  a  way  as  to  transmit 
a  backward  momentum  to  the  water. 
Fig.  92  shows  superposed  drawings  of 
an  eel,  made  from  successive  photo- 
graphs. The  region  marked  XY  is 
moving  from  right  to  left  and  that 
X1Y1  from  left  to  right  and  evidently, 
as  Gray  puts  it,  'all  parts  of  the  fish's 
body  which  are  in  transverse  motion  have  their  leading  surfaces  directed 
backwards  and  towards  the  direction  of  transverse  movement,  but 
the  angle  of  inclination  is  most  pronounced  when  the  segment  is 
crossing  the  axis  of  longitudinal  motion,  and  at  this  point  the  segment 
of  the  body  is  travelling  at  its  maximum  speed.  Each  point  of  the  body 


Fig.  92.  Enlarged  drawings  of  suc- 
cessive photographs  of  a  young  eel 
superimposed  on  each  other  so  that 
the  tips  of  the  head  are  on  the  same 
transverse  axis  and  the  longitudinal 
axes  of  motion  (ab)  are  made  to 
coincide.  As  the  wave  passes  the 
section  XY  it  first  moves  to  the  left 
and  is  directed  backwards  and  to 
the  left,  whereas  Xx  Y\  moves 
in  the  opposite  direction.  The  tip 
of  the  tail  follows  a  figure  of  8. 
(From  Gray) 


v.  2  SWIMMING  OF  FISHES  135 

is  travelling  along  a  figure  8  curve  relative  to  a  transverse  line  which  is 
moving  forward  at  the  average  forward  velocity  of  the  whole  fish. 
The  track  of  any  point  on  the  body  (relative  to  the  earth)  is  a  sinu- 
soidal curve  whose  pitch  or  wave  length  is  less  than  that  of  a  curve 
which  defines  the  body  of  the  fish.  There  is  therefore  a  definite  angle 
between  the  surface  of  the  fish  and  its  path  of  motion.' 

Each  portion  of  the  side  of  the  fish  can  thus  be  considered  as  moving 
like  the  blade  of  an  oar  used  for  sculling  at  the  back  of  a  boat.  The 
principle  used,  that  of  an  inclined  plane,  is  the  same  as  in  screw  pro- 
pulsion, the  essential  feature  being  that  the  moving  surface  is  inclined 
at  an  angle  to  its  line  of  motion.  The  effect  of  the  movement  is  greatly 
increased  by  the  fact  that  the  amplitude  of  the  oscillations  grows 
passing  backwards,  as  is  necessary  to  produce  additive  effects  in  any 
coupled  system  of  screws  or  turbines.  The  whole  fish  thus  operates 
as  a  single  self-propelling  system. 

The  magnitude  of  the  forward  thrust  thus  generated  depends 
among  other  things  on  (a)  the  angle  that  the  surface  of  the  fish  makes 
with  its  own  path  of  motion,  (b)  the  angle  between  the  surface  of 
the  fish  and  the  axis  of  forward  movement  of  the  whole  fish,  and 
(c)  the  velocity  of  transverse  movement  of  the  body  (Gray).  These  are 
evidently  factors  that  will  vary  with  the  shape  of  the  body  and  the 
action  of  its  muscles.  The  body  form  of  the  faster-moving  types  of 
bony  fishes  provides  substantial  advantages  for  swimming  over  that 
of  the  more  elongated  types.  The  essential  differences  are  that  the 
bony  fishes  have  (1)  large  caudal  fins,  (2)  a  much  smaller  length  of  the 
body  relative  to  its  depth,  (3)  less  flexibility. 

The  role  of  the  large  caudal  fin  is  to  resist  transverse  movements; 
its  effect  is,  again  quoting  Gray,  'to  keep  the  leading  surface  of  the 
body  directed  obliquely  backwards  during  both  phases  of  its  trans- 
verse movements  and  thereby  to  exert  a  steady  pressure  on  the  water'. 
Since,  however,  the  tail  does  execute  transverse  movements,  and  at 
the  same  time  is  being  rotated  towards  and  away  from  the  axis  of 
motion,  it  exerts  a  very  large  propulsive  effect,  probably  as  much  as 
40  per  cent,  of  the  total  thrust. 

The  effect  of  the  caudal  fin,  combined  with  the  shortness  of  body 
and  reduced  flexibility,  is  that  the  front  part  of  a  bony  fish  makes  only 
small  transverse  movements;  the  track  of  the  head  is  therefore  nearly 
straight  and  the  whole  front  of  the  body  presents  a  streamlined 
surface  with  little  resistance.  Further,  the  muscles  just  in  front  of  the 
tail  exert  their  tension  with  very  little  change  in  length. 

No  doubt  the  shape  of  the  body  also  has  an  important  influence  on 


136  THE  APPEARANCE  OF  JAWS  v.  2- 

the  effect  of  the  fish  on  the  water  and  hence  on  the  turbulence  in  the 
flow  of  water  and  the  resistance  that  must  be  overcome.  Gray  has 
shown  that  in  a  dolphin  the  resistance  cannot  be  that  of  a  rigid  model 
towed  at  the  speed  at  which  the  animal  moves,  since  this  would  require 
that  the  muscles  generate  energy  at  a  rate  at  least  seven  times  greater 
than  is  known  in  the  muscles  of  other  mammals.  By  watching  the 
flow  of  particles  past  the  body  of  fish-like  models  he  showed  that 
movements  such  as  those  produced  in  swimming  accelerate  the  water 
in  the  direction  of  the  posterior  end,  and  this  would  greatly  reduce 
the  turbulence. 

Something  is  known  of  the  nervous  mechanism  responsible  for  the 
production  of  the  swimming  waves.  An  eel  can  swim  if  its  whole  skin 
has  been  removed.  If  a  region  of  the  body  is  immobilized  by  a  clamp, 
swimming  waves  can  pass  along.  Therefore  the  rhythm  is  determined 
by  some  intrinsic  activity  of  the  spinal  cord  and  not  by  any  mechanism 
such  as  proprioceptor  impulses  arising  in  active  muscles  and  causing 
others  to  contract. 

Experiments  in  which  the  spinal  cord  was  cut  across  show  that  in 
the  eel  the  rhythm  is  only  initiated  when  suitable  impulses  reach  the 
cord  either  from  spinal  afferents  or  from  the  brain.  Thus  the  spinal 
eel  can  be  made  to  swim  either  by  fixing  a  clip  on  to  its  caudal  fin  or  by 
electrical  stimulation  of  the  cut  end  of  the  spinal  cord.  Though  the 
cord  requires  such  afferent  stimuli  for  its  functioning,  they  do  not 
determine  the  frequency  of  the  rhythm,  which  bears  no  relationship 
to  that  of  the  applied  stimuli. 

In  the  dogfish  the  isolated  spinal  cord  is  able  to  initiate  rhythmic 
swimming.  After  transection  behind  the  brain  the  posterior  portion 
of  the  fish  exhibits  continuous  swimming  movements  for  many  days. 
Light  touch  on  the  sides  of  the  body  inhibits  these  movements,  but  some 
sensory  impulses  are  necessary  for  their  initiation;  after  complete  de- 
afferentation,  by  section  of  all  the  dorsal  roots,  the  movements  cease. 

The  information  available  does  not  yet  enable  us  to  understand 
fully  how  the  swimming  rhythm  is  initiated  and  maintained,  nor  how 
it  is  influenced  by  the  brain.  It  would  be  very  interesting  to  have 
further  knowledge  on  these  topics,  especially  because  the  locomotor 
rhythms  of  land  animals  are  probably  based  on  the  serial  contractions 
of  their  fish  ancestors. 

3.  Equilibrium  of  fishes  in  water ;  the  functions  of  the  fins 

Making  use  of  the  methods  of  investigation  of  aeronautical  engineers, 
studies  have  been  made  of  the  forces  that  operate  to  keep  a  fish  stable 


v.  3  EQUILIBRIUM  OF  FISHES  137 

as  it  moves  through  the  water,  or  allow  it  to  become  temporarily  un- 
stable and  hence  to  change  direction.  Instead  of  attempting  to  study  a 
living  or  dead  fish  moving  in  water,  Harris  made  models  and  supported 
them  in  a  wind-tunnel  in  an  apparatus  suitable  for  measuring  the 
forces  at  work  in  the  various  directions.  Such  a  method,  in  which  no 
compensating  movements  of  the  fins  are  allowed,  makes  it  possible 
to  investigate  the  so-called  'static  stability'  of  the  fish,  that  is  to  say, 


Fig.  93.  Diagram  of  model  of  the  dogfish  Mustelus,  showing  the  conventional  terms 
for  describing  deviations  of  motion.  The  longitudinal  axis  X  is  that  of  the  wind 
tunnel  and  Y  (horizontal)  and  Z  (vertical)  are  at  right  angles  to  it.  The  arrows  show 
the  directions  known  as  positive  rolling,  pitching,  and  yawing,  which  occur  about  the 
X,  Y,  and  Z  axes  respectively,  a.  is  the  angle  of  attack  between  the  axis  of  the  model 
and  the  X  axis.  (From  Harris,  J.  exp.  Biol.  13.) 


to  see  whether  the  body  and  fins  are  so  shaped  as  to  provide  forces 
that  tend  to  bring  the  fish  back  into  its  previous  line  of  movement  after 
it  has  deviated  in  any  direction.  Any  body  such  as  a  fish  or  aeroplane 
is  said  to  be  in  stable  motion  if  when  it  veers  slightly  from  its  line  of 
progress  the  new  forces  produced  upon  its  planes  tend  to  restore  the 
original  direction  of  motion. 

The  forces  acting  on  the  fish  are  measured  along  three  primary  axes, 
longitudinal,  horizontal,  and  vertical.  Deviation  from  the  line  of 
motion  about  the  longitudinal  axis  is  known  as  rolling,  about  the 
transverse  axis  as  pitching,  and  about  the  vertical  axis  as  yawing 
(Fig.  93).  The  forces  along  these  three  axes  are  known  as  drag,  lateral 
force,  and  lift. 

In  order  to  discover  the  effect  of  the  median  fins  and  tail  on  the 
stability,  these  fins  were  removed,  the  heterocercal  tail  being  replaced 
by  a  cone  having  the  same  taper  as  the  actual  caudal  fin.  The  model 
was  then  placed  in  the  wind-tunnel  with  a  wind  at  40  m.p.h.,  which 


138  THE  APPEARANCE  OF  JAWS  v.  3 

corresponds  to  a  motion  of  3  m.p.h.  in  water.  The  lateral  force  was 
measured  when  the  body  was  made  to  yaw  at  various  angles.  The 


+0-2 
+  0-1 

-15       -ipl^^f 


-0 

-0-2 


+5°       +10°     +15° 


D 


+  5"oXS+Yo°  +iV 


+  0  6 

y 

+  05 

/ 

+0-4/ 

/ 

/ 

/ 

/o-z 

+03 
*0-1 

+5°       +10* 

+15 

-0-1 

02 

03 

-04 

-0-5 

-0-5 


Fig.  94.  A.  Results  of  yawing  test  on  model  of  Mustelus  without  fins.  The  lateral  force 
is  plotted  as  a  light  full  line,  drag  force  as  a  light  broken  line;  yawing  moment  about 
centre  of  gravity  as  full  heavy  line.  Abscissae  show  the  angle  of  attack  in  degrees, 
ordinates  the  lateral  force  and  drag  in  pounds  weight,  yawing  moment  in  in. -lb.  X  ^j. 
n.  Yawing  test  similar  to  (a)  but  with  the  fins  behind  the  centre  of  gravity  in  place. 

C.  Yawing  test  with  all  median  fins  in  place. 

D.  Pitching  test  on  model  of  Mustelus  with  all  fins  intact  and  pectoral  fins  set  at  an 
angle  of  incidence  of  8°.  Lift  force  is  shown  as  a  light  full  line,  drag  force  as  a  light 
broken  line,  pitching  moment  about  the  centre  of  gravity  as  a  heavy  full  line. 

(From  Harris.) 

results  showed  that  the  equilibrium  in  this  plane  is  quite  unstable;  a 
slight  turn  off  the  direct  course  would  produce  a  turning  moment 
tending  to  increase  still  further  the  deflection  (Fig.  94).  This  is  a 
well-known  property  of  all  airship  hulls,  and  is  known  as  the  'unstable 
moment'  of  the  hull.  It  is  corrected  in  the  airship  by  the  addition  of 


v.  3  FUNCTION  OF  FINS  139 

suitable  horizontal  and  vertical  fin  surfaces  at  the  rear  end,  when  the 
airship  becomes  in  effect  a  feathered  arrow.  The  forces  operating  on 
the  fins  tend  to  bring  the  body  back  into  the  original  line  of  motion. 
The  fins  of  the  fish  operate  in  a  similar  manner.  If  the  experiment 
is  performed  with  a  model  to  which  all  the  fins  behind  the  centre  of 
gravity  have  been  added,  namely,  the  caudal,  anal,  and  second  dorsal 
fins,  it  is  found  that  the  curve  for  the  yawing  moment  now  has  a  steep 
negative  slope  (Fig.  94  b),  that  is  to  say,  every  deviation  produces 
forces  that  tend  to  give  directional  stability.  With  the  first  dorsal  fin 
also  in  position  the  model  possesses  a  remarkable  neutral  equilibrium 
(Fig.  94  c).  Deviations  by  as  much  as  io°  produce  no  resultant  yawing 
moment  about  the  centre  of  gravity.  The  form  of  the  dorsal  fins  is 
therefore  definitely  such  as  to  maintain  stable  swimming  and  prevent 
yawing. 

Turning  of  a  fish  is  produced  either  by  the  propagation  of  a  wave- 
down  one  side  only  of  the  body  or  by  asymmetrical  braking  with  the 
pectoral  fins  (see  below).  The  former  type  of  turn  has  been  investi- 
gated by  Gray  in  the  whiting,  where  there  is  a  large  caudal  fin.  This 
gives  great  lateral  resistance,  so  that  the  first  part  of  the  turn  is 
executed  by  bending  the  front  part  of  the  fish  on  the  tail  as  a  fulcrum. 
This  enables  the  animal  to  turn  through  1800  within  a  circle  of  the 
diameter  of  its  own  length.  After  removal  of  the  caudal  fin  the  turns 
are  much  less  effective. 

In  both  elasmobranchs  and  teleosts  the  dorsal  fins  are  well  developed 
in  the  active  swimmers.  In  most  elasmobranchs  they  are  fixed,  but  in 
many  teleosts  the  dorsal  fin  can  be  folded  up  and  down,  and  it  is 
observed  that  the  fin  is  raised  during  turning.  This  would  have  the 
effect  of  increasing  the  yawing  moment  produced  by  asymmetrical 
action  of  the  body  muscles  or  by  unilateral  braking  with  the  pectoral 
fins. 

Since  the  body  is  so  markedly  flexible  in  the  lateral  plane  and  there 
are  powerful  muscles  available  for  turning  it  in  this  direction,. the  part 
played  by  the  fins  in  determining  the  stability  is  important  mainly 
when  the  body  is  held  straight.  The  fish  thus  has  the  double  advantage 
of  great  stability  (by  keeping  the  body  straight)  and  great  control- 
lability (by  bending  it).  In  a  body  unable  to  change  its  shape  in  this 
way,  stability  and  controllability  would  be  inversely  related.  This  is 
the  case  for  the  stability  of  the  fish  in  the  vertical  plane,  in  which  the 
body  is  little  flexible.  Fig.  94  n  shows  the  positive  slope  of  the  curve 
for  the  pitching  moment  and  clearly  the  equilibrium  in  this  plane  is 
quite  unstable.  The  pectoral  fins  contribute  more  than  any  others  to 


Ho  THE  APPEARANCE  OF  JAWS  v.  3- 

movement  in  this  plane,  and  since  they  lie  in  front  of  the  centre  of 
gravity  they  greatly  increase  the  instability.  The  fish  must  be  able  to 
alter  direction  in  the  vertical  plane,  and  it  has  apparently  sacrificed 
static  stability  for  controllability.  The  equilibrium  in  this  plane  is  a 
dynamic  one,  controlled  by  the  movable  pectoral  fins,  and  it  is  so 
unstable  that  only  a  small  movement  of  these  fins  is  necessary  to 
produce  a  deflecting  force  that  restores  the  original  direction  of 
motion. 

The  pectoral  fins,  lying  in  front  of  the  centre  of  gravity,  tend  to 
produce  a  movement  of  positive  pitch,  that  is  to  say,  they  force  the 
head  upwards.  This  effect  is  normally  compensated  by  a  component 
produced  by  the  heterocercal  tail.  The  upper  lobe  of  this  is  rigid  and 
the  lower  more  flexible,  therefore  the  lateral  motion  given  by  the 
swimming  movements  of  the  body  produces  a  vertical  lift  force  on  the 
tail,  giving,  of  course,  negative  pitch.  After  amputation  of  the  hypo- 
caudal  lobe  and  anal  fin  a  dogfish  swims  continually  along  the  bottom 
of  the  tank :  in  order  to  compensate  for  the  absence  of  negative  pitch 
the  pectoral  fins  are  held  horizontally  and  hence  there  is  no  moment 
to  counteract  the  weight  of  the  fish.  If  the  pectoral  fins  are  then  also 
removed  the  anterior  end  of  the  body  is  pointed  upwards,  often  so 
much  so  as  to  cause  the  fish  to  swim  with  its  head  out  of  the  water. 
This  is  the  result  of  an  over-strenuous  attempt  to  compensate,  by 
raising  the  head,  for  the  negative  pitch  produced  by  the  tail.  The 
system  is  no  longer  suitable  for  making  the  continuous  adjustments 
necessary  to  ensure  stability. 

This  analysis  makes  it  clear  why  a  heterocercal  tail  is  found  in 
almost  all  the  primitive  swimming  chordates;  it  is  almost  a  necessity 
for  an  animal  with  a  specific  gravity  in  excess  of  the  medium  and  little 
flexibility  in  the  vertical  plane.  The  component  of  positive  pitch 
could  be  provided  by  the  flattened  head  or  by  continuous  lateral  fin 
folds,  such  as  may  have  been  present  in  early  fishes,  and  adjusted 
by  the  limited  flexibility  possible  in  the  fin.  The  development  of 
movable  pectoral  fins  confers  much  greater  control.  Since  the  useful 
portions  of  a  fin  fold  for  this  purpose  would  be  those  well  in  front  of 
and  behind  the  centre  of  gravity,  we  can  perhaps  see  the  reason  why 
the  intervening  portion  has  become  lost.  In  the  modern  sharks  the 
pelvic  fins  have  little  influence  on  the  stability  and  are  perhaps  retained 
only  for  their  modification  as  claspers. 

It  is  not  surprising  that  races  of  fishes  with  stability  ensured  by 
systems  of  this  sort  should  tend  to  adopt  a  bottom-living  habit,  with 
dorso-ventral  flattening,  such  as  is  found  in  the  skates  and  rays. 


v.  4 


SKIN  OF  ELASMOBRANCHS 


141 


Expansion  of  the  front  end  is  developed  at  first  to  compensate  the 
effect  of  the  tail,  but  the  pectoral  fin  becomes  expanded  to  allow  ver- 
tical adjustments  and  then  reduction  of  the  hypocaudal  lobe  of  the  tail 
accompanies  the  adoption  of  life  on  the  sea  bottom.  Eventually  all 


Fig.  95.  Development  of  denticles  in  the  dogfish. 

A  and  b,  first  gathering  of  odontoblasts  (sc.)  below  the  basement  membrane  (brn.);  ml.  are  the 

epidermal  cells  that  will  become  modified,  c,  first  deposition  of  dentine  (d.).  In  D  there  is 

more  dentine  and  a  pulp  cavity  (p.)  is  seen.  In  E  are  shown  stages  in  the  formation  of  enamel 

(e.)  and  of  the  basal  plate  (bp.)  while  the  denticle  cuts  the  epidermis  (ep.). 

(From  Goodrich,  Vertebrata,  A.  &  C.  Black,  Ltd.) 

locomotion  is  produced  by  undulatory  movements  of  the  fins,  which 
were  at  first  used  only  to  raise  the  fish  off  the  bottom. 

4.  Skin  of  elasmobranchs 

Being  swift  and  predatory  animals,  more  attackers  than  attacked, 
the  sharks  do  not  possess  a  very  heavy  external  armament.  The  skin 
itself  is  tough,  being  covered  by  layers  of  epidermis.  Beneath  this  is  a 
thick  dermis  of  connective  tissue  with  fibres  arranged  at  right  angles 


142  ORGANIZATION  OF  THE  HEAD  v.  4- 

as  in  a  carpet,  giving  a  tissue  of  great  strength  and  flexibility,  able  to 
maintain  the  shape  of  the  body.  Scattered  over  the  skin  are  the  charac- 
teristic denticles  or  placoid  scales  (Fig.  95).  Each  of  these  consists  of  a 
pulp  cavity,  around  the  edge  of  which  lies  a  layer  of  odontoblasts 
secreting  the  calcareous  matter  of  the  scale,  known  as  dentine.  This 
has  a  characteristic  structure  resulting  from  the  fact  that  the  odonto- 
blasts send  fine  processes  throughout  its  substance.  The  outside  of  the 
dentine  is  covered  by  a  layer  of  enamel,  secreted  by  the  overlying 
ectoderm.  Usually  the  denticles  pierce  through  the  ectoderm,  after 
which  no  further  enamel  can  be  added  to  their  surface.  Obviously  the 
scales  are  similar  to  teeth,  which  are  indeed  to  be  considered  as 
specialized  denticles  developed  on  the  skin  of  the  jaws.  It  has  often 
been  supposed  that  the  denticle  is  the  primitive  type  of  fish  scale, 
from  which  others  have  been  derived,  but  it  now  seems  more  likely 
that  the  earliest  covering  was  a  continuous  layer,  later  broken  into 
large  scales,  from  which  the  denticle  was  ultimately  derived  (p.  269). 
The  skin  also  gives  protection  to  the  fish  by  its  colour,  produced 
by  a  layer  of  chromatophores  beneath  the  epidermis.  Many  sharks 
have  a  spotted  or  wavy  pattern,  which  breaks  up  their  visible  outline 
as  they  move  in  the  water,  especially  near  the  surface.  They  are  able 
to  change  their  colour,  though  only  slowly,  becoming  darker  on  a  dark 
background  (see  p.  164). 

5.  The  skull  and  branchial  arches 

In  general  organization  a  dogfish  follows  closely  the  fish  plan, 
which  we  have  already  considered.  Most  of  its  special  new  features 
are  in  the  head,  and  we  may  now  turn  to  a  consideration  of  the 
organization  of  the  head  and  jaws  of  a  gnathostome  vertebrate.  The 
jawless  vertebrates  of  the  Silurian  and  Devonian  included  fresh- 
water animals  of  various  sorts,  but  the  vertebrate  type  began  to 
flourish  and  increase  more  abundantly  with  the  appearance  of  creatures 
with  jaws  in  the  late  Silurian.  From  this  stage  onwards  we  have  to 
follow  the  parallel  history  of  numerous  orders  and  families,  as  the 
vertebrate  plan  of  structure  became  adapted  for  various  habitats.  It 
seems  likely  that  the  development  of  a  biting  mouth  greatly  increased 
the  range  of  possibilities  of  vertebrate  life.  The  most  obvious  use  of 
a  mouth  is  for  attacking  other  animals,  but  it  may  also  have  been  used 
to  collect  plant  food  from  all  sorts  of  situations  where  it  would  not 
be  available  to  the  microphagous  or  shovelling  Agnatha.  Probably  the 
mouth  was  also  early  used  for  defence,  and  in  this  way  influenced  the 
whole  bodily  organization,  making  unnecessary  the  heavy  armature 


v.  5  DEVELOPMENT  OF  THE  JAWS  143 

that  is  so  characteristic  of  many  early  vertebrates.  Modern  research 
has  shown  that  the  armour  has  become  progressively  reduced  along 
various  lines  of  iish  evolution.  Older  ideas  of  comparative  anatomy 
regarded  the  'cartilage  fishes'  as  showing  a  primitive  stage,  preceding 
the  appearance  of  bone.  We  now  realize  that  this  is  the  opposite  of  the 
truth  and  that  the  dogfish  and  its  relatives  represent  a  higher  type, 


rosC 


Fig.  96.  Skull  and  branchial  arches  of  the  dogfish  (Scyliorliimts). 
au.c.  auditory  capsule;  b.b.  basibranchial;  b.li.  basihyal;  c.  centrum;  cer.b.  ceratobranchials; 
cer.h.  ceratohyal;  d.r.  foramen  for  dorsal  root;  e.b.  extrabranchials;  e.c.f.  external  carotid 
foramen;  e.l.  ethmoid  ligament;  ep.b.  epibranchials;  gr.  groove  for  anterior  cardinal  sinus; 
g.r.  gill  rays;  hy.a.  foramen  for  hyoid  artery;  hymd.  hyomandibula;  i.d.  interdorsal;  io.c. 
interorbital  canal;  I.e.  labial  cartilages;  M.c.  Meckel's  cartilage;  na.  neural  arch;  nas.c.  nasal 
capsule;  o.n.f.  orbito-nasal  foramen;  op.  foramen  for  ophthalmic  nerve;  op.g.  groove  for 
op.V;  op.V,  op. VII  ophthalmic  branches  of  V  and  VII;  orb.  orbit;  ph.b.  pharyngobranchials ; 
p.sp.l.  prespiracular  ligament;  r.  rib;  rost.  rostral  cartilages;  spd.  supradorsals ;  tr.  transverse 
process;  vr.  foramen  for  ventral  root;  II-IX,  foramina  for  cranial  nerves.  (After  Borradaile.) 

able  to  defend  themselves  by  mobility,  by  biting,  and  by  efficient 
sensory  and  nervous  organization.  Heavy  defensive  armour  is  a 
primitive  form  of  protection  for  animals,  as  for  man. 

Besides  its  use  in  feeding  and  defence,  the  mouth  can  also  be  used  as 
a  means  of  'handling'  the  environment,  for  instance  in  the  nest-build- 
ing activities  of  many  fishes.  Indeed,  it  is  difficult  for  us  to  realize  the 
utility  of  the  jaws  for  an  animal  not  provided  with  any  other  means  of 
seizing  hold  of  objects. 

The  development  of  the  mouth  to  a  point  at  which  it  could  be  used 
in  these  varied  ways  was,  therefore,  a  very  important  stage  in  evolution. 
Recognition  of  the  Gnathostomata  as  a  separate  group  of  animals  is 
far  more  than  a  matter  of  classificatory  convenience,  it  marks  the 
achievement  of  the  possibility  of  life  in  a  greatly  increased  range  of 
environments. 


144  ORGANIZATION  OF  THE  HEAD  v.  5- 

Morphological  analysis  enables  us  to  see  how  this  biting  mouth 
was  produced,  by  modification  of  one  or  more  of  the  gill-slits.  The 
main  differences  that  separate  the  gnathostome  from  cyclostome  ver- 
tebrates are  therefore  in  the  head  and  its  skeleton.  Although  the 
modern  elasmobranchs  show  the  skull  and  jaws  in  a  modified  and 
reduced  condition,  they  provide  by  their  simplicity  a  good  starting- 
point  for  discussion.  The  'skull'  of  a  dogfish  consists  of  a  series  of 


ac. 


pan 


--dao 


Fig.  97.  Diagram  of  skull  of  selachian  embryo  before  fusion  of  the  main  cartilages; 
cranial  nerves  black,  numbered;  arteries  cross-lined. 

ac.  auditory  capsule;   bra.  epibranchial;   dao.   dorsal  aorta;   eps.  efferent  pseudobranchial; 

ha.  efferent  hyoid;  hv.  hypophysial  vein;  i.e.  internal  carotid;  nc.  nasal  cartilage;  oc.  orbital 

cartilage;  oca.  occipital  arch;  op.  optic;  oph.  ophthalmic;  or.  orbital;  pan.  pila  antotica;  pf. 

profundus  nerve;  pch.  parachordal;  poc.  polar  cartilage;  tr.  trabecula.  (From  Goodrich.) 

cartilaginous  boxes  surrounding  the  brain  and  receptor  organs  (Fig. 
96).  The  nasal  capsules,  orbital  ridges,  and  auditory  capsules  are 
largely  fused  with  the  main  cranium,  producing  a  single  continuous 
structure,  the  chondrocranium.  It  is  interesting  to  consider  how  this 
structure  has  arisen  during  the  process  of  cephalization.  Presumably 
parts  of  it  represent  the  modified  sclerotomes  of  trunk  regions.  We 
shall  see  presently  that  there  is  strong  evidence  that  the  head  has  arisen 
by  modification  of  a  segmental  arrangement  such  as  is  seen  in  the 
trunk;  the  morphogenetic  processes  that  build  the  skull  must  there- 
fore be  related  in  some  way  to  those  of  the  vertebrae.  The  first  rudi- 
ment of  the  skull  in  the  embryo  consists  of  two  pairs  of  cartilaginous 
rods,  the  parachordals  and  trabeculae  (Fig.  97).  The  former  lie  on 
either  side  of  the  notochord,  the  trabeculae  in  front  of  the  notochord. 
These  first  rods  fuse  up  to  make  a  continuous  plate;  from  this  grow 
sides  and  roof,  completing  the  cartilaginous  neuro-cranium  around  the 
brain.  Meanwhile  cartilaginous  capsules  form  around  the  nose,  eyes, 
and  ears,  and  become  joined  to  the  neuro-cranium.  Posteriorly,  behind 


v.  6  BRANCHIAL  ARCHES  145 

the  auditory  capsules,  the  cranium  is  completed  by  the  addition  of  a 
number  of  segmented  elements,  evidently  modified  vertebrae. 

The  problem  is,  therefore,  to  determine  the  nature  of  the  pro-otic 
part  of  the  skull.  Before  we  can  settle  this  we  must  consider  the 
visceral  or  branchial  arches.  These  are  pairs  of  rods  of  cartilage 
developed  in  the  walls  of  the  mouth  and  pharynx,  between  the  gill- 
slits.  In  the  dogfish  each  typical  branchial  arch  (Fig.  96)  consists  of  a 
series  of  four  pieces,  the  pharyngo-,  epi-,  cerato-,  and  hypo-branchials. 
Ventrally  some  of  the  arches  join  a  median  basibranchial  plate.  These 
rods  lie  in  the  pharynx  wall  and  on  their  outer  sides  carry  a  series  of 
projecting  rods,  the  branchial  rays  and  extrabranchial  cartilages, 
whose  function  is  to  support  the  lamellae  of  the  gills. 

There  are  five  such  branchial  arches,  differing  only  slightly  from 
each  other.  In  front  of  these  lie  two  arches,  the  hyoid  and  mandibular, 
which,  though  modified,  are  obviously  of  the  same  series.  The  hyoid 
the  more  nearly  resembles  a  typical  branchial  arch.  Its  most  dorsal 
element,  the  hyomandibular  cartilage,  is  a  thick  rod  attached  dorsally 
to  the  skull  by  ligaments  and  at  its  lower  end  forming  the  support 
for  the  hind  end  of  the  jaw.  It  apparently  corresponds  to  the  epi- 
branchials.  The  more  ventral  elements,  cerato-  and  basihyal,  resemble 
the  corresponding  members  of  more  posterior  arches.  The  jaws  them- 
selves (mandibular  arches)  depart  more  widely  from  the  form  of  a 
typical  branchial  arch,  but  the  two  thick  rods  of  which  each  is  com- 
posed, the  upper  palato-pterygo-quadrate  bar  and  the  lower  Meckel's 
cartilage,  are  recognizably  members  of  the  branchial  series.  Looking 
at  the  whole  apparatus  with  a  thought  to  the  embryological  processes 
that  have  produced  it,  with  as  it  were  a  manufacturer's  eye,  we  can 
see  at  once  that  the  jaws  and  hyoid  arch  have  been  produced  by  a 
modification  of  the  processes  that  make  the  branchial  arches. 

6.  The  jaws 

Study  of  the  serial  relationship  of  the  jaws  and  branchial  arches 
gives  us  an  understanding  of  the  course  of  evolution  of  the  mouth. 
We  may  suppose  that  the  ancestors  of  the  gnathostomes  possessed  a 
nearly  terminal  mouth,  either  on  the  front  end  of  the  body  or  on  the 
ventral  surface.  The  pharynx  was  pierced  by  a  series  of  gill  pouches, 
beginning  shortly  behind  the  mouth  and  separated  by  arches,  each 
containing  a  set  of  cartilaginous  bars  (Fig.  96).  There  is  some  evidence 
that  this  condition  persisted  in  the  cephalaspids  (p.  125),  where  there 
is  found  to  be  a  series  of  ten  pairs  of  gill-slits,  beginning  far  forward 
on  either  side  of  the  mouth.  The  muscles  moving  the  more  anterior 


146  ORGANIZATION  OF  THE  HEAD  v.  6 

parts  of  the  pharynx  wall  and  the  anterior  arches  could  be  called  into 
play  to  help  in  the  collection  of  food.  In  this  way  the  mouth  came  to 
be  used  for  prehension,  and  the  grasping  jaws  of  the  gnathostomes 
appeared  as  the  more  anterior  arches  became  modified  to  allow  more 
efficient  seizing,  and  the  skin  over  them  was  modified  to  form  the 
teeth.  The  mouth  probably  shifted  backwards  during  this  process  and 
its  lateral  edges  joined  the  first  gill-slit.  The  rods  supporting  the 
posterior  wall  of  that  slit  thus  became  bent  over  into  the  characteristic 
position  of  the  vertebrate  jaws. 

There  is  some  uncertainty  as  to  the  means  of  support  of  the  jaws 
in  the  earlier  stages  of  their  evolution.  The  front  end  of  the  palato- 
pterygo-quadrate  bar  is  attached  to  the  cranium  in  the  dogfish  by  the 
ethmo-palatine  iigament'.  In  most  elasmobranchs  the  hind  end  of  the 
upper  jaw  is  not  fixed  to  the  cranium  but  is  slung  from  the  latter  by 
the  hyomandibula  and  by  a  prespiracular  ligament.  This  means  of 
support,  known  as  hyostylic,  was  for  long  supposed  to  have  been  the 
original  one.  But  the  earliest  gnathostomes  (the  acanthodians)  do  not 
have  this  arrangement  (p.  187),  indeed,  their  hyoid  arch  is  an  almost 
typical  branchial  arch,  not  modified  to  support  the  jaw.  In  the  primi- 
tive condition  one  would  not  expect  the  hyoid  arch  to  have  any  con- 
nexion with  the  mandibular.  In  the  acanthodians  the  jaw  is  supported 
by  direct  attachments  to  the  cranium  at  its  hind  as  well  as  front  end, 
a  condition  known  as  autodiastylic. 

The  early  elasmobranchs  themselves  do  not  have  a  hyostylic  jaw 
support,  but  an  arrangement  in  which  the  upper  jaw  is  both  attached 
to  the  cranium  and  also  supported  by  the  hyomandibula.  This 
amphistylic  condition  persists  to-day  in  the  primitive  shark  Hexan- 
chus.  Apparently  the  jaws,  which  at  first  swung  from  the  skull,  later 
became  fixed  at  the  hind  end  to  the  hyoid,  and  this  finally  became  the 
only  means  of  support  posteriorly.  The  advantage  of  this  last  arrange- 
ment is  presumably  that  it  allows  a  wide  gape  for  swallowing,  the  prey 
whole.  As  the  sharks  sought  to  eat  larger  and  larger  fishes,  those  in 
which  the  hind  end  of  the  upper  jaw  was  less  firmly  fixed  to  the  skull 
were  the  more  successful  and  so  the  hyostylic  condition  was  achieved. 

If  this  theory  of  the  origin  of  the  jaws  is  correct  we  may  expect  to 
find  some  trace  of  a  cartilaginous  support  for  the  side  wall  of  the 
pharynx  in  front  of  the  original  first  gill-slit,  a  premandibular  visceral 
arch.  Many  sharks  have  two  pairs  of  labial  cartilages  in  this  position, 
which  have  been  held  to  represent  arches.  However,  there  are  strong 
grounds  for  believing  that  this  is  represented  by  the  trabeculae  cranii, 
the  rods  lying  on  each  side  in  front  of  the  parachordals  and  contribut- 


v.  6  ORIGIN  OF  THE  JAWS  147 

ing  to  the  floor  of  the  skull  (Fig.  98).  Many  points  indicate  that  these 
rods  are  not  part  of  the  axial  skeleton.  The  main  axis  of  the  body 
presumably  ends  at  the  front  end  of  the  notochord,  that  is  to  say,  at 
the  level  of  the  front  ends  of  the  parachordals.  Indeed  there  is  much 
confirmatory  evidence  to  show  that  this  level  represents  the  end  of  the 


^  12.2m    R £ 


gsX  rn.a.'ka'.'*br.a.l"        9s-9 
Yt  ¥2,3. 


gut 


FlG.  uS.  Diagrams  to  show  the  condition  of  the  visceral  arches  and 
jaws  in  early  vertebrates. 
A.  cephalaspid;  B.  acanthodian;  C.  elasmobranch.  (i.e.  auditory  capsule; 
"br.  a.  1"  first  branchial  arch;  c.n.c.  nerve-cord;  e.  eye;  gs.  I.  first  gill-slit; 
//.  hypophysis. /i.a.  hyomandibular arch;  m. a.  mandibular  arch;  m.  mouth;  not. 
notochord;  p.m.a.  premandibular  arch  (trabecula);  sp.  spiracle;  Vi,  pro- 
fundus nerve;  V2,  3,  trigeminal  nerve;  VII,  facial;  IX,  glossopharyngeal; 
X,  vagus.  (Modified  after  Westoll.) 

segmented  part  of  the  body,  everything  in  front  of  this  level  being  as 
it  were  pushed  forward  from  above  or  below.  The  trabeculae  have 
exactly  the  relations  to  the  most  anterior  nerves  and  blood-vessels 
that  would  be  expected  of  visceral  arches.  Confirmation  of  the  theory 
comes  from  the  discovery  that  the  cartilage  of  the  front  part  of  the 
trabeculae,  like  that  of  the  visceral  arches,  is  formed  by  material 
streaming  down  from  the  neural  crest,  that  is  to  say,  from  ectoderm. 
The  branchial  arches,  hyoid,  jaws,  and  trabeculae  thus  all  constitute 
a  single  series,  the  result  of  the  working  of  a  repetitive  or  rhythmic 
process,  appropriately  modified  at  each  level. 


148  ORGANIZATION  OF  THE  HEAD  v.  7- 

7.  Segmentation  of  the  vertebrate  head 

The  rhythmicity  or  metamerism  seen  in  the  cartilages  can  be  traced 
throughout  the  structure  of  the  head.  Although  in  higher  vertebrates 
the  head  appears  as  a  distinct  structure,  separated  from  the  body  by 
a  neck,  yet  there  is  every  reason  to  think  that  it  has  arrived  at  that 
state  by  gradual  modification  of  the  anterior  members  of  an  originally 
complete  metameric  series.  The  jaws,  the  receptor-organs,  and  the 
brain  have  become  developed  at  the  front  end  of  the  body,  producing 
what  zoologists  conveniently  if  pretentiously  call  cephalization. 

The  fundamental  segmentation  of  the  head  is  not  very  easily  appar- 
ent to  superficial  observation;  the  working  out  of  its  details  is  an 
excellent  exercise  in  morphological  understanding.  Recognition  of  the 
segmental  value  of  the  various  structures  also  makes  them  the  more 
easily  remembered.  For  instance,  the  nerves  found  in  the  head  have 
been  named  and  numbered  for  centuries  by  anatomists  in  an  arbitrary 
series: 

I.  Olfactorius 
II.  Opticus 

III.  Oculomotorius 

IV.  Trochlearis  (patheticus) 
V.  Trigeminus 

VI.  Abducens 
VII.  Facialis 
VIII.  Acousticus 
IX.  Glossopharyngeus 
X.  Vagus 
XI.  Accessorius 
XII.  Hypoglossus 

Morphological  study  has  shown  that  these  nerves  are  not  isolated 
structures,  each  developed  independently,  but  that  they  represent  a 
regular  series  of  segmental  dorsal  and  ventral  roots  of  the  head 
somites.  The  satisfaction  and  simplification  given  by  this  generaliza- 
tion is  one  of  the  clearest  advantages  of  morphological  insight.  More 
important  still,  such  understanding  of  the  morphology  of  a  structure 
shows  us  how  to  look  for  the  morphogenetic  processes  that  produce  it; 
such  knowledge  of  how  organs  are  made  is  an  essential  step  in  mending 
or  remaking  them. 

The  idea  of  the  essential  similarity  of  structure  of  the  head  and 
trunk  was  early  developed  by  Goethe,  who  tried  to  show  that  the 
mammalian  skull  is  a  series  of  modified  vertebrae.  Unfortunately  this 


v.  8 


PRO-OTIC  SOMITES 


149 


view  cannot  be  maintained  in  detail  and  the  theory  was  brought  to 
ridicule  by  T.  H.  Huxley  and  others.  The  segmental  value  of  the  skull 
floor  and  sides  is  not  at  all  easy  to  determine;  the  parachordals  arise 
as  a  pair  of  unsegmented  rods  on  either  side  of  the  notochord. 


ma:  ha 


Fig.  99.  Diagram  of  the  segmentation  of  the  head  of  a  dogfish. 

cr.  limit  of  neurocranium;  vr.  limit  of  visceral  arch  skeleton;  a.  auditory  nerve;  aa.i,  pre- 
occipital arch;  aa.2,  occipital  arch;  ab.  abducens  nerve;  ac.  auditory  capsule;  ah.  anterior 
head  cavity;  c.  coelom;/.  facial  nerve;  gl.  glossopharyngeal  nerve;  ha.  hyoid  arch;  hm.  hypo- 
glossal muscles;  hy.  hypoglossal  nerve;  la.  pila  antotica;  m.  mouth;  m.2-6,  myomere  2-6; 
ma.  mandibular  arch;  tnb.  muscle-bud;  nc.  nasal  capsule;  om.  oculomotor  nerve;  prf.  pro- 
fundus nerve;  scl.  sclerotome  of  segment  10;  sp.1-2,  ganglion  of  spiral  nerve  1-2;  t.  trochlear 
nerve;  tr.  trigeminal  nerve;  v.  vagus  nerve;  vgl.  vestigial  ganglion  of  segment  7;  vc.  ventral 
coelom;  vr.  ventral  root  of  segment  6.  (From  Goodrich.) 

8.  The  pro-otic  somites  and  eye-muscles 

Ideas  about  the  segmentation  of  the  head  were  first  correctly  for- 
mulated by  F.  Balfour.  In  his  studies  of  the  development  of  elasmo- 
branchs  (1875)  he  showed  that  three  myotomes,  the  pro-otic  somites, 
can  be  recognized  during  development  in  front  of  the  auditory  capsule 
(Fig.  99).  The  auditory  sac,  pushing  inwards  and  becoming  sur- 
rounded by  cartilage,  then  breaks  the  series  of  myotomes,  so  that 
several  are  missing  in  the  adult,  though  the  series  is  complete  in  the 
embryo. 

If  this  analysis  is  correct  we  should  be  able  to  recognize  that  the 
nerves  of  the  head  belong  to  a  series  of  dorsal  and  ventral  roots, 
similar  to  that  in  the  trunk,  the  ventral  roots  being  those  for  the 
myotomes  and  the  dorsal  roots,  running  between  the  myotomes, 
carrying  sensory  fibres  for  the  segment  and  motor-fibres  for  any  non- 
myotomal  musculature  present  (p.  36).  In  the   spinal    region   the 


i5o  ORGANIZATION  OF  THE  HEAD  v.  8 

dorsal  and  ventral  roots  join,  but  this  is  not  the  primitive  condition 
(witness  amphioxus  and  the  lampreys),  and  in  the  head  region  the 
earlier  state  of  affairs  is  retained,  the  dorsal  and  ventral  roots  remain 
separate.  Presumably  the  arrangement  we  find  in  the  head  today  was 
laid  down  in  very  early  times,  in  the  Silurian  period  or  earlier,  when 
the  dorsal  and  ventral  roots  were  still  separate.  The  head,  in  spite  of 
its  specializations,  preserves  for  us  a  relic  of  that  ancient  condition. 

The  branchial  nerves,  such  as  the  glossopharyngeal,  show  clear 
signs  of  this  condition.  Each  has  a  small  pre-trematic  branch  in  front 
of  the  slit,  a  larger  post-trematic  branch  behind  it,  and  a  pharyngeal 
branch  to  the  wall  of  the  pharynx.  The  pre-trematic  branch  usually 
contains  mostly  sensory  fibres  from  the  skin,  the  pharyngeal  branch 
visceral  sensory  fibres,  including  those  from  taste  buds.  The  post- 
trematic  branch  contains  both  motor  and  sensory  fibres.  In  addition 
to  these  more  ventral  branches  the  branchial  nerves  also  usually 
provide  dorsal  rami  to  the  skin  of  the  back. 

The  three  pro-otic  somites  become  completely  taken  up  in  the 
formation  of  the  six  extrinsic  muscles  of  the  eye,  arranged  similarly 
in  all  gnathostome  vertebrates.  The  four  recti  roll  the  eye  straight 
upwards,  downwards,  forwards,  or  backwards,  and  the  two  obliques, 
lying  farther  forward,  turn  it,  as  their  name  suggests,  upward  or 
downward  and  forward  (Fig.  ioo).  Of  these  muscles  the  superior, 
anterior,  and  inferior  rectus  and  inferior  oblique  are  all  derived  from 
the  first  myotome  and  are  innervated  by  the  oculomotor  (third  cranial) 
nerve.  The  superior  oblique,  innervated  by  the  trochlear  nerve  (fourth 
cranial),  is  the  derivative  of  the  second  and  the  posterior  rectus 
(external  rectus  of  man),  innervated  by  the  abducens  (sixth  cranial), 
of  the  third  somite.  These  three  nerves  are  evidently  the  ventral  roots 
of  the  three  pro-otic  somites.  At  some  early  stage  of  vertebrate 
evolution  all  the  myotomal  musculature  of  the  front  part  of  the  head 
became  devoted  to  the  movement  of  the  eyes.  The  muscles  originally 
forming  part  of  the  swimming  series  became  attached  to  a  cup-like 
outgrowth  from  the  brain. 

Most  of  the  rest  of  the  musculature  of  the  head,  including  that  of 
jaws  and  branchial  arches,  is  derived  from  the  somatopleure  wall  of  the 
coelom  and  is  therefore  lateral  plate  or  visceral  musculature.  This 
lateral  plate  muscle  is  indeed  better  developed  in  the  head  than  in 
the  trunk,  where  all  the  muscles,  even  of  the  more  ventral  parts  of  the 
body,  are  formed  by  downward  tongues  from  the  myotomes.  The 
lateral  plate  origin  of  the  jaw-muscles  at  once  gives  us  the  clue  to 
the  nature  of  some  more  of  the  cranial  nerves,  the  fifth,  seventh,  ninth, 


V. 


THE  ORBIT 


151 


and  tenth.  These  nerves  all  carry  ganglia  containing  the  cell  bodies 
of  sensory  fibres  and  these  are  comparable  to  the  spinal  dorsal  root 


'  op  prof 


olf.b. 


cbl  sip. 


c'd.a. 


Fig.  100.  Orbit  of  the  dogfish. 

ant. reel,  anterior  rectus;  cereb.  cerebellum;  cil.a.,  cil.p.  anterior  and  posterior  ciliary  nerves; 
epa.  anterior  carotid  artery;  ep.  epiphysis;  g.cil.  ciliary  ganglion;  inf. obi.  inferior  oblique; 
lam.  lamina  terminalis  of  cerebrum;  O.V.  and  VII,  superficial  ophthalmic  branch  of  trigeminal 
and  facial;  obi. sup.  superior  oblique;  olf.b.  olfactory  bulb;  opt. I.  optic  lobe;  post.rect.  posterior 
rectus;  r. op. prof,  ramus  ophthalmicus  profundus  of  trigeminal;  rs.  sensory  root  of  ciliary 
ganglion;  sup.rect.  superior  rectus;  thai,  thalamus;  //  to  A',  cranial  nerves. 
(After  Young,  Quart.  J.  Micr.  Sci.  75.) 


ganglia.  But  the  nerves  also  transmit  motor-fibres  to  the  muscles  of 
the  jaws  and  branchial  arches.  They  are  in  fact  mixed  roots,  just  as 
we  have  seen  that  the  primitive  dorsal  roots  should  be,  carrying  the 
sensory  fibres  for  the  segment  and  motor-fibres  for  the  non-myotomal 
muscles  (p.  36). 


152  ORGANIZATION  OF  THE  HEAD  v.  8- 

9.  The  cranial  nerves  of  elasmobranchs 

These  nerves  are  more  easily  studied  in  elasmobranchs  than  in  any 
other  vertebrates,  because  of  the  relatively  soft  and  transparent 
cartilage  through  which  they  run.  We  may  therefore  take  this  oppor- 
tunity to  examine  the  whole  series  of  cranial  nerves  in  some  detail  in 
the  dogfish,  beginning  with  the  oculomotor  nerve,  the  first  ventral 
root.  Examination  after  removal  of  the  brain  will  show  clearly  in  any 
vertebrate,  including  man,  that  this  nerve  arises  from  the  ventral 
surface,  at  the  level  of  the  hind  end  of  the  midbrain  (optic  lobes). 
This  is  not  true  of  the  trochlear  or  pathetic  nerve,  which  emerges 
from  the  dorso-lateral  surface  of  the  brain  but  nevertheless  is  the 
ventral  root  of  the  second  segment.  Its  cells  of  origin  lie  close  behind 
those  of  the  oculomotor  nerve,  in  the  ventral  part  of  the  brain.  The 
reason  for  the  dorsal  emergence  is  that  the  muscle  lies  dorsally  and  the 
nerve  has  been  modified  so  as  to  reach  its  muscle  by  running  partly 
within  the  tissues  of  the  brain.  The  third  ventral  root  (abducens), 
which  is  very  short,  is  clearly  ventral. 

In  looking  for  the  dorsal  roots  that  correspond  to  these  three 
segments  we  have  to  examine  the  trigeminal,  facial,  and  auditory 
nerves.  The  trigeminal  of  the  dogfish,  like  that  of  man,  has  ophthalmic, 
maxillary,  and  mandibular  branches  (Fig.  ioo),  but  can  be  shown  to 
represent  the  dorsal  roots  of  the  two  first  segments.  The  ophthalmic 
branch  is  a  sensory  nerve  carrying  fibres  for  skin  sensation  from  the 
snout.  The  maxillary  branch  supplies  sensory  fibres  to  the  upper  jaw, 
whereas  the  mandibular  is  a  mixed  nerve  to  the  skin  and  muscles  of 
the  lower  jaw.  Besides  these  main  branches  there  is  also  a  small  but 
important  sensory  branch  from  the  trigeminal  to  the  eyeball  (Fig. 
ioo).  This  joins  a  motor  root  from  the  oculomotor  nerve  where  the 
latter  swells  slightly  to  form  a  ciliary  ganglion.  Two  ciliary  nerves 
then  carry  motor  and  sensory  fibres  to  the  eyeball.  In  some  specimens 
a  branch  of  the  more  anterior  ciliary  nerve  leaves  the  eyeball  anteriorly, 
runs  between  the  oblique  muscles,  and  out  of  the  orbit  again  to  end 
in  the  skin  of  the  snout  (Fig.  ioo).  Though  this  branch  is  small  and 
inconstant  in  the  dogfish,  its  course  corresponds  exactly  with  that 
of  a  much  larger  nerve  in  the  related  shark  Mustelus  and  in  skates  and 
rays.  In  these  animals  there  are  two  ophthalmic  branches  of  the 
trigeminal  nerve;  one,  having  a  course  similar  to  that  of  the  main  nerve 
in  the  dogfish,  is  the  ramus  ophthalmicus  superficialis;  the  second, 
the  ramus  ophthalmicus  profundus,  runs  across  within  the  orbit,  gives 
off  the  long  ciliary  nerve  to  the  eyeball,  passes  between  the  oblique 


v.  9  PARTS  OF  THE  TRIGEMINAL  153 

muscles,  and  leaves  the  orbit  for  the  skin  of  the  snout.  In  higher 
vertebrates  the  nasociliary  nerve  and  the  long  ciliary,  innervating  the 
eyeball,  represent  the  profundus,  while  the  rest  of  the  ophthalmic 
nerve  of  mammals  corresponds  to  the  superficial  ophthalmic  of 
elasmobranchs. 

The  relations  of  these  nerves  to  other  structures  shows  that  the 
so-called  trigeminal  nerve  really  includes  the  dorsal  roots  of  two 
segments  combined.  The  profundus  can  be  traced  back  in  develop- 
ment to  a  nerve  that  is  obviously  the  dorsal  root  of  the  first  somite, 
of  which  the  oculomotor  nerve  is  the  ventral  root.  Indeed  it  may  be 
noticed  that  the  profundus  and  oculomotor  partly  join,  at  the  ciliary 
ganglion.  The  ramus  ophthalmicus  profundus  and  the  oculomotor 
nerve  thus  constitute  the  dorsal  and  ventral  roots  of  the  first  or  pre- 
mandibular  somite,  whose  corresponding  branchial  arch  is  presumably 
the  trabecula  cranii  (p.  147).  The  dorsal  root  does  not  show  the  full 
structure  of  a  branchial  nerve,  presumably  because  there  is  no  gill-slit. 
The  profundus  represents  only  the  dorsal  branch  of  a  typical  branchial 
nerve,  innervating  the  skin. 

The  ramus  ophthalmicus  superficialis,  and  the  maxillary  and  mandi- 
bular branches  together  constitute  the  dorsal  root  of  the  second  pro- 
otic  somite,  whose  ventral  root  is  the  trochlear  nerve.  The  correspond- 
ing gill  arch  is  the  mandibular  (palato-pterygo-quadrate  bar  and 
Meckel's  cartilage),  whose  gill-slit  we  have  suggested  has  been  in- 
corporated with  the  edge  of  the  mouth.  The  trigeminal  nerve  shows 
considerable  similarity  to  a  branchial  nerve,  its  maxillary  branch  repre- 
sents the  pre-trematic  and  the  mandibular  the  post-trematic  ramus, 
while  the  ophthalmicus  superficialis  is  the  dorsal  branch  to  the  skin. 
There  is  no  pharyngeal  branch.  An  anomalous  feature  of  the  trige- 
minal is  that  it  contains  sensory  fibres  whose  cells  of  origin  lie  within 
the  brain  (mesencephalic  root).  These  fibres  are  probably  proprio- 
ceptors from  the  masticatory  muscles  and  eye-muscles.  The  latter  run 
from  the  eye-muscle  nerves  to  join  the  trigeminal. 

The  dorsal  root  of  the  third  segment,  whose  ventral  root  is  the 
abducens,  includes  the  whole  of  the  facial  and  also  the  auditory  nerve. 
The  facial  is  a  large  mixed  nerve  in  the  dogfish.  Its  ophthalmic  branch 
runs  to  the  snout,  carrying  mainly  fibres  for  the  organs  of  the  lateral 
line  system  that  lie  there.  A  large  buccal  branch  supplies  sensory 
fibres  to  the  mouth  and  a  palatine  branch  joins  the  trigeminal.  A  small 
prespiracular  branch  carries  sensory  fibres  from  the  skin  in  front  of  the 
spiracle,  and  the  main  portion  of  the  nerve  continues  behind  the 
spiracle  as  the  hyomandibular  nerve,  dividing  up  into  motor  branches 


i54  ORGANIZATION  OF  THE  HEAD  v.  9 

for  muscles  of  the  hyoid  arch  and  sensory  ones  for  the  skin  of  that 
region. 

This  nerve  is  obviously  the  branchial  nerve  to  the  spiracle;  we  can 
safely  say  that  the  facial  and  abducens  are  the  dorsal  and  ventral  roots 
of  the  third  or  hyoid  segment.  The  auditory  nerve  is  included  as  part 
of  the  dorsal  root  of  the  third  somite  because  the  auditory  sac  is 
formed  by  sinking  in  of  a  portion  of  the  ectoderm  within  the  territory 
of  the  facial  nerve.  The  labyrinth  still  communicates  with  the  surface 
of  the  head  in  the  adult  dogfish  by  a  canal,  the  aquaeductus  vestibuli. 
The  nerve  that  innervates  the  auditory  sac,  whatever  complexities  it 
may  acquire,  is  to  be  regarded  morphologically  as  a  portion  of  the 
dorsal  root  of  the  hyoid  segment. 

The  segmental  nature  of  the  structures  in  the  pro-otic  region  can 
therefore  be  made  out  without  serious  difficulty.  The  disturbance 
introduced  by  the  auditory  capsule  makes  the  segmental  arrangement 
of  the  more  posterior  region  of  the  head  somewhat  confused.  The 
series  of  dorsal  roots  is  uninterrupted;  the  ninth  (glossopharyngeal) 
nerve  is  the  dorsal  root  of  the  fourth  segment  of  the  series  and  runs 
out  through  the  cartilage  of  the  auditory  capsule.  The  dorsal  roots  of 
the  succeeding  segments  are  then  fused  to  form  that  very  puzzling 
nerve  the  vagus.  The  branches  it  sends  to  the  gills  are  clearly  typical 
branchial  nerves,  but  why  should  they  all  come  off  together  from  the 
medulla  oblongata,  and  if  there  is  any  advantage  in  this  union,  why 
is  the  ninth  nerve  not  also  so  incorporated?  Above  all,  why  does 
the  vagus  send  two  branches  far  outside  the  segments  of  its  origin,  the 
lateral  line  branch  carrying  fibres  to  the  organs  right  to  the  tip  of  the 
tail  and  the  visceral  branch  fibres  to  the  heart,  stomach,  and  probably 
small  intestine? 

Evidently  these  'wanderings',  from  which  the  vagus  gets  its  name, 
began  very  long  ago.  The  nerve  reaches  as  far  back  in  cyclostomes  as 
in  any  other  vertebrates.  It  is  easy  to  understand  that  if  visceral 
functions  are  to  be  directed  from  the  medulla  oblongata  there  is  an 
advantage  in  having  sensory  impulses  sent  direct  to  that  region  of  the 
brain  and  motor  impulses  sent  out  direct  to  the  viscera.  It  may  be 
that  these  advantages  allowed  the  centralization  of  these  visceral 
functions,  while  the  need  for  serial  contraction  of  the  swimming 
muscles  led  to  the  retention  of  the  segmental  arrangement  of  the 
spinal  cord.  It  is  an  interesting  thought  that  but  for  the  swimming 
habits  of  our  ancestors  our  nervous  system  might  by  now  consist  of  a 
central  ganglion  with  nerves  passing  from  it  direct  to  all  the  organs. 
Indeed  we  are  tending  in  that  direction,  as  the  spinal  cord  shortens 


v.  9  VAGUS  NERVE  155 

and  becomes  more  and  more  nearly  a  simple  pathway  between  the 
brain  and  the  periphery. 

However  this  may  be,  the  vagus  is  certainly  a  nerve  compounded 
of  the  dorsal  roots  of  several  segments  and  it  is  a  mixed  nerve,  con- 
taining both  receptor  and  motor  fibres.  Some  of  the  more  posterior 
rootlets  of  this  series  are  separated  off  in  higher  animals  (not  the  dog- 
fish) to  form  the  eleventh  cranial  nerve,  the  accessorius  or  spinal 
accessory,  which  in  mammals  sends  motor-fibres  to  certain  muscles 
of  the  neck,  the  sternomastoid,  and  part  of  the  trapezius.  Its  motor 
nature  has  led  some  to  suppose  that  this  nerve  is  a  ventral  root,  but 
these  muscles  are  derived  from  lateral  plate  musculature  and  the 
accessorius  represents  the  motor  portion  of  the  hinder  dorsal  roots 
of  the  vagus  series. 

The  ventral  roots  of  this  post-otic  region  have  become  much 
reduced.  Several  myotomes  are  always  missing  completely,  so  that 
there  are  no  ventral  roots  corresponding  to  the  glossopharyngeal  and 
first  three  or  four  vagal  segments.  The  more  anterior  of  the  surviving 
post-otic  somites  are  to  be  found  not  in  the  dorsal  region  but  ventrally, 
as  the  hypoglossal  musculature  of  the  tongue.  The  muscle-buds  have 
grown  round  into  this  portion  behind  the  gill-slits,  and  the  nerve 
(hypoglossal)  that  innervates  them  represents  the  ventral  roots  of  the 
more  posterior  segments  of  the  vagus-accessorius  series  (Fig.  104). 
The  origin  of  this  nerve  from  the  floor  of  the  medulla  is  a  clear  sign 
that  it  is  a  ventral  root. 

Thus  the  entire  series  of  cranial  nerves  is : 


Segment 

Arch 

Dorsal  root 

Ventral  root 

Pre-mandibular 

Trabecula 

R.  op.  profundus  V 

Oculomotorius  III 

Mandibular 

Palato  -  pterygo  -  quad- 

Rr.   op.    superficialis, 

Trochlearis  IV 

rate  bar  and  Meckel's 

maxillaris,  and  man- 

cartilage 

dibularis  V 

Hyoid 

Hyoid 

Facialis  VII 
Acousticus  VIII 

Abduccns  VI 

1st  Branchial 

1  st  Branchial 

Glossopharyngeus  IX 

(absent) 

2nd  Branchial 

2nd  Branchial^ 

Vagus  X 

3rd  Branchial 

3rd  Branchial  1 

+ 

Hypoglossals  XII 

4th  Branchial 

4th  Branchial  j 

Accessorius  XI 

5th  Branchial 

5th  Branchial  J 

Two  cranial  nerves  have  not  yet  been  considered,  the  first,  olfactory, 
and  second,  optic.  Our  thesis  is  that  all  connexions  between  centre 
and  periphery  are  made  by  means  of  a  segmental  series  of  dorsal  and 
ventral  roots  and  therefore  these  nerves,  too,  should  be  fitted  into  the 
series.  No  embryological  or  other  studies  have  enabled  this  to  be  done 


156  ORGANIZATION  OF  THE  HEAD  v.  9- 

and  the  reason  in  the  case  of  the  optic  nerve  is  quite  clear.  It  is  not 
morphologically  a  peripheral  nerve  at  all.  The  eye  is  formed  as  a 
vesicle  attached  to  the  brain ;  the  optic  'nerve'  therefore  develops  as  a 
bundle  of  fibres  joining  two  portions  of  the  central  nervous  system;  in 
fact  it  is  now  usually  called  the  optic  tract,  not  the  optic  nerve. 

This  reasoning  will  not  apply  to  that  very  peculiar  and  interesting 
structure  the  olfactory  nerve.  This  is  unique  among  all  craniate 
nerves  in  consisting  of  bundles  of  fibres  whose  cell  bodies  lie  at  the 
periphery.  The  cells  of  the  olfactory  epithelium,  like  the  sensory  cells 
in  invertebrates  and  some  of  those  of  amphioxus,  are  neurosensory 
cells,  that  is  to  say,  their  inner  ends  are  prolonged  to  make  the  actual 
nerve-fibres  that  pass  into  the  brain.  This  fact  does  not  by  itself  solve 
the  problem  of  fitting  the  nerve  into  the  series  of  dorsal  and  ventral 
roots,  but  it  reminds  us  that  the  nerve  is  very  ancient,  and  suggests 
that  it  does  not  fall  into  the  rhythm  of  the  rest  of  the  series  because  it 
precedes  the  other  cranial  nerves  either  in  time  or  space,  or  perhaps 
even  both.  The  olfactory  nerve  may  have  existed  before  any  seg- 
mental structure  appeared,  possibly  as  the  nerve  of  sense-organs  on 
the  front  end  of  the  ciliated  larva  which  we  suppose  gave  rise  to  our 
stock  (p.  76).  Alternatively  we  can  say  that  the  olfactory  nerve  is  as 
it  is  because  it  lies  in  front  of  the  region  over  which  the  segmenting 
process  operates;  it  is,  as  it  were,  'prostomial'.  If  we  wish  we  can  hold 
both  these  views  together. 

There  are  one  or  two  other  exceptions  to  the  rhythmic  arrangement 
of  nerves,  perhaps  more  difficult  to  account  for  than  the  first  and 
second  cranial  nerves.  If  all  connexions  between  centre  and  periphery 
are  made  by  dorsal  and  ventral  roots  what  is  the  status  of  the  fibres 
that  run  down  the  infundibular  stalk  to  reach  the  cells  of  the  pituitary 
body?  This  glandular  tissue,  derived  from  the  epithelium  of  the 
hypophysial  folding  of  the  roof  of  the  mouth,  is  undoubtedly  a  peri- 
pheral organ.  Does  it  receive  its  nerve-fibres  direct  from  the  brain  ? 
If  so  presumably  we  must  say  that  the  pituitary,  like'  the  nose, 
is  prostomial,  lying  in  front  of  the  segmental  region,  and  this  is 
reasonable  enough  from  its  position.  There  is  good  reason  to  believe 
that  it  is  an  extremely  ancient  organ,  already  present  in  the  earliest 
chordates. 

A  still  more  puzzling  exception  is  the  nervus  terminalis.  This  is 
a  small  bundle  leaving  the  brain  ventrally  behind  and  below  the  olfac- 
tory nerves  and  running  to  the  olfactory  mucosa  or  to  the  accessory 
olfactory  organ  of  Jacobson,  where  this  is  present  (p.  350).  In  some 
vertebrates   it   carries   a   small   ganglion.   The   fibres   are   probably 


v.  io  RESPIRATION  157 

afferents  and  they  run  backwards  through  the  brain  tissue  to  the 
pre-optic  nucleus  of  the  hypothalamus.  A  possible  clue  to  its  origin  is 
that  this  is  the  region  of  the  brain  where  the  morphologically  ventral 
region  of  the  neuraxis  ends  (p.  147).  The  nervus  terminalis  may  repre- 
sent the  ventral  olfactory  nerve,  the  much  larger  main  nerve  being 
morphologically  dorsal. 

A  further  puzzle  of  some  importance  which  may  be  mentioned  here 
is  the  course  of  the  proprioceptor  fibres  for  those  muscles  that  are 
supplied  purely  by  ventral  roots.  The  eye-muscles  contain  proprio- 
ceptor organs  and  Sherrington  and  others  have  shown  that  the  affer- 
ent fibres  connected  with  these  run  to  the  brain  through  the  third, 
fourth,  and  sixth  nerves,  that  is  to  say,  through  ventral  roots.  Simi- 
larly, it  has  been  shown  that  there  are  afferent  fibres  in  the  hypo- 
glossal nerves  in  mammals.  Conversely  it  is  now  known  that  there  are 
efferent  fibres  running  from  the  brain  to  many  receptor  organs.  For 
example,  such  fibres  run  in  the  auditory  nerve.  To  pursue  these  ques 
tions  farther  would  lead  us  into  discussion  of  the  factors  that  control 
the  making  of  connexions  within  the  nervous  system  Here  we  are 
concerned  only  with  analysis  of  the  plan  that  produces  the  main  out- 
lines of  the  structures  in  the  head,  a  plan  which,  with  all  its  modifica- 
tions, is  essentially  segmental. 

10.  Respiration 

The  function  of  the  branchial  arches  is  not  merely  to  support  the 
gills  but  to  allow  the  movements  of  the  pharynx  wall  by  which  the 
respiratory  current  of  water  is  produced.  It  is  for  this  reason  that 
the  jointed  system  of  rods  is  present.  The  respiratory  movements  con- 
sist in  a  lowering  of  the  floor  of  the  mouth  by  means  of  the  hypo- 
glossal muscles,  with  at  the  same  time  an  expansion  of  the  walls  of 
the  pharynx.  This  causes  an  inrush  of  water  through  the  mouth, 
which  is  then  closed  and  the  floor  raised,  forcing  the  water  out  through 
the  gill-slits.  The  whole  movement  is  worked  by  the  'visceral'  (lateral 
plate)  muscles  of  the  pharynx  wall,  innervated  by  the  trigeminal, 
facial,  glossopharyngeal,  and  vagus  nerves,  in  co-operation  with  the 
myotomal  hypoglossal  muscles,  innervated  by  the  hypoglossal  nerve. 

The  gill  filaments  bear  lamellae  that  meet  at  the  tips,  leaving  minute 
channels  for  the  water.  The  blood  flows  through  the  lamellae  in  the 
opposite  direction  to  the  water  so  that  just  before  leaving  the  gills 
the  blood  meets  the  highest  concentration  of  oxygen  and  lowest  of 
carbonic  acid. 


158 


ORGANIZATION  OF  THE  HEAD 


1 1 .  The  gut  of  elasmobranchs 

The  digestive  system  of  sharks  shows  several  changes  from  the  plan 
found  in  lampreys,  especially  the  presence  of  a  true  stomach,  charac- 
teristic of  all  gnathostomes.  Apparently  little  or  no  digestion  goes  on 
in  the  mouth  and  pharynx.  The  teeth  consist  of  rows  of  backwardly 
directed  denticles  (Fig.  ioi).  They  are  carried  on  special  folds  of  skin 
lining  the  jaws  and  are  continually  replaced  as  they  are  worn  away  on 


Fig.  ioi.  Sections  through  the  jaws  of  a,  dogfish  (Scyliorhinus),  and  n,  sand-shark 

(Odontaspis),  showing  the  transitions  between  dermal  denticles  (d)  and  teeth  (t). 

(From  Norman,  partly  after  Gegenbaur.) 

the  edge.  The  replacement  of  milk  by  permanent  teeth  in  mammals 
is  a  relic  of  such  serial  replacement  in  a  fish.  The  'gill  rakers'  arc 
rods  attached  to  the  branchial  cartilages  and  serving  to  prevent 
the  escape  of  prey.  The  basihyal  supports  a  short  non-protrusible 
tongue. 

The  wall  of  the  pharynx  is  lined  by  a  stratified  epithelium  on  to 
which  open  numerous  mucous  glands,  sometimes  complex.  The  mucus 
serves  to  assist  the  passage  of  the  food,  but  probably  has  no  strictly 
digestive  function,  though  the  salivary  glands  of  higher  vertebrates 
no  doubt  originate  from  a  modification  of  these  mucous  glands. 

The  pharynx  narrows  to  an  oesophagus  with  thick  muscular  walls, 
leading  without  sharp  transition  to  the  stomach.  We  have  seen  that  in 
cyclostomes  the  oesophagus  opens  directly  into  the  region  of  gut  that 
receives  the  bile  and  pancreatic  secretion.  The  stomach,  which  we 


v.  12  DIGESTION  IN  ELASMOBRANCHS  159 

now  meet  for  the  first  time,  has  probably  been  formed  as  a  special 
portion  of  the  oesophagus.  Barrington  suggests  that  it  evolved  with  the 
jaws,  serving  originally  as  a  receptacle  for  the  large  pieces  of  food,  or 
even  whole  fishes,  which  could  now  be  swallowed.  The  mucous  glands 
became  modified  to  produce  acid,  since  this  prevents  bacterial  decay. 
Finally,  an  enzyme,  pepsin,  was  evolved  able  to  digest  proteins  in 
acid  solution.  In  the  dogfish  this  condition  has  been  fully  established 
and  the  stomach  has  essentially  the  structure  and  functions  found  in 
all  higher  vertebrates.  However,  in  the  gastric  glands  only  one  type 
of  cell  is  recognizable,  there  are  no  separate  pepsin-secreting  and 
acid-producing  cells.  Nevertheless,  there  is  a  pepsin-like  enzyme 
present  and  the  contents  are  acid.  The  stomach  is  divided  into  two 
parts,  a  descending  cardiac  and  ascending  pyloric  limb,  the  signifi- 
cance of  the  divisions  being  unknown. 

The  region  where  the  stomach  joins  the  intestine  is  guarded  by  a 
powerful  pyloric  sphincter,  immediately  beyond  which  open  the  bile 
and  pancreatic  ducts.  The  liver  is  a  large  two-lobed  organ,  receiving 
the  hepatic  portal  blood  from  the  gut.  It  serves  as  a  storage  organ 
containing  much  glycogen  and  fat  and  sometimes  the  hydrocarbon 
squalene.  It  probably  also  plays  a  part  in  the  destruction  of  red  blood 
corpuscles.  Bile  is  carried  away  to  a  gall-bladder,  from  which  a  bile- 
duct  leads  to  open  at  the  front  end  of  the  spiral  intestine. 

The  pancreas,  hardly  recognizable  as  a  distinct  organ  in  the  lamprey, 
forms  in  the  dogfish  an  elongated  body  between  the  stomach  and 
intestine.  It  contains  both  exocrine  and  endocrine  cells  and  its  duct 
enters  the  intestine  shortly  below  the  pylorus.  The  'small'  intestine 
of  elasmobranchs  is  of  a  peculiar  form,  being  short  but  with  its 
surface  greatly  increased  by  the  presence  of  a  spiral  ridge  or  'valve'. 
The  intestinal  contents  are  alkaline  and  contain  trypsin,  amylase, 
and  lipase.  There  is  no  constant  fauna  of  commensal  bacteria.  Ab- 
sorption presumably  takes  place  wholly  in  this  organ,  for  the  remain- 
ing length  of  gut  consists  only  of  a  short  rectum,  to  which  is  attached 
an  organ  of  unknown  function,  the  rectal  gland,  containing  branched 
glands  and  much  lymphoid  tissue. 

12.  The  circulatory  system 

The  heart  develops  as  a  specialization  of  the  subintestinal  vessel 
between  the  place  where  it  receives  the  veins  from  the  liver  and  the 
body  wall  and  the  gills,  which  are  to  be  supplied  under  high  pressure. 
It  consists  of  a  single  series  of  three  main  chambers,  sinus  venosus, 


i6o 


ORGANIZATION  OF  THE  HEAD 


atrium,  and  ventricle,  all  of  which  are  muscular,  and  there  is  also  a 
muscular  base  to  the  ventral  aorta,  the  conus  arteriosus,  provided  with 
valves  (Fig.  102). 

The  five  afferent  branchial  arteries  carry  blood  to  the  gill  lamellae, 
whence  it  is  collected  by  a  system  of  four  efferents  and  connecting 
vessels  into  a  median  dorsal  aorta,  carrying  blood  to  all  parts  of  the 
body.  Oxygenated  blood  is  supplied  to  the  head  from  three  sources. 
(1)  From  the  top  of  the  first  gill  a  carotid  artery  leaves  the  efferent 
branchial  and  runs  forwards  and  towards  the  midline:  it  then  divides 


f.       eF  pef 


Fig.  102.  Diagram  of  the  branchial  circulation  of  an  elasmobranch  fish. 

aa.  median  anterior  prolongation  of  aorta;  ac.  anterior  carotid;  afa.  afferent  vessel  of  spiracu- 
lar  gill;  aef.  afferent  vessel  from  last  hemibranch;  af.  anterior  efferent  vessel;  a/.2-6,  five 
afferent  vessels  from  ventral  aorta;  afa.  afferent  artery  of  spiracular  gill;  c.  conus  leading  to 
ventral  aorta;  cl.  coeliac  artery;  d.  ductus  Cuvieri;  da.  dorsal  aorta;  ef.  epibranchial  artery; 
h. a.  hyoid  afferent  vessel;    hp.  hepatic  veins;    ht.  heart;   pc.  posterior  carotid;  pef.  posterior 

efferent  vessel;  s.  spiracle;  va.  ventral  artery;  I-V,  branchial  slits. 

(From  Goodrich,  Vertebrata,  A.  &  C.  Black,  Ltd.,  after  Parker.) 


into  an  external  carotid  to  the  upper  jaw  and  internal  carotid  to  the 
brain.  (2)  The  dorsal  aorta  divides  at  its  front  end  into  branches, 
which  join  the  carotids  before  their  division.  (3)  From  the  vessel 
that  collects  blood  from  the  first  gill  arises  a  hyoidean  artery,  carry- 
ing oxygenated  blood  to  the  spiracle.  From  here  the  hyoidean  artery 
runs  on  as  the  anterior  carotid  (Fig.  102)  across  the  floor  of  the  orbit 
to  join  the  internal  carotid  within  the  brain-case. 

The  heart  is  supplied  by  a  cardiac  artery  arising  from  the  dorsal 
aorta  behind  the  gills.  The  blood-pressure  in  the  ventral  aorta  is  30-40 
mm  Hg  and  there  is  a  drop  of  10-20  mm  Hg  across  the  gills.  The 
circulation  is  slow,  with  a  mean  circulation  time  as  low  as  2  minutes. 
The  venous  return  of  the  fishes  is  ensured  by  a  system  of  very  large 
sinuses.  The  pericardium  is  almost  completely  enclosed  in  a  carti- 
laginous framework  by  the  basibranchial  plate  above  and  pectoral 
girdle  below  it.  It  may  be  that  this  produces  a  negative  pressure  in 


v.  iz     VASCULAR  SYSTEM  OF  ELASMOBRANCHS      161 

the  veins.  There  is  a  passage  of  unknown  function,  the  pericardio- 
peritoneal canal,  leading  from  the  pericardium  to  the  abdominal 
coelom  and  the  hinder  end  of  this  is  very  narrow. 

A  caudal  sinus  from  the  tail  opens  into  a  renal  portal  system  above 
the  kidneys.  From  the  latter,  and  from  the  muscles  of  the  back,  blood  is 
collected  into  the  pair  of  very  large  posterior  cardinal  sinuses,  lying  on 
the  dorsal  wall  of  the  coelom.  Above  the  heart  these  receive  the  open- 
ings of  other  large  sinuses,  such  as  the  anterior  cardinal  sinus,  running 
above  the  gills  and  collecting  blood  from  the  head  by  way  of  an  orbital 
sinus,  and  the  jugular,  lateral  cardinal,  subclavian,  and  other  sinuses  from 
the  body  wall.  Blood  then  passes  round  the  oesophagus  in  the  two 
ductus  Cuvieri  into  the  sinus  venosus,  where  hepatic  sinuses  also  open. 

The  resistance  offered  by  a  vessel  to  flow  within  it  decreases  with 
approximately  the  fourth  power  of  the  diameter,  therefore  the  large 
size  of  these  vessels  substantially  assists  in  allowing  return  to  the 
heart.  The  heart-muscles,  like  any  others,  require  antagonists;  they 
can  contract  in  one  direction  only,  and  each  chamber  therefore  needs 
to  be  actively  dilated.  It  will  be  noted  that  the  fish  heart  consists  of 
a  series  of  three  muscular  chambers,  presumably  because  the  low 
venous  pressure  is  able  to  dilate  only  a  chamber  with  very  thin  walls, 
such  as  the  sinus  venosus.  Contraction  of  the  sinus  then  inflates  the 
auricle,  and  the  auricle  inflates  the  ventricle,  which  thus  constitutes 
the  third  step  in  this  serial  pressure-raising  system.  In  the  land  animals, 
where  most  of  the  blood  only  passes  through  a  single  set  of  capillaries, 
a  two-step  system  (auricle  and  ventricle)  is  sufficient  for  each  part  of 
the  circulation. 

Little  is  known  of  the  control  of  the  circulation  but  it  is  probably 
less  effective  than  in  higher  animals.  There  is  a  cardiac  branch  from 
the  vagus  ending  in  an  elaborate  plexus  in  the  sinus  venosus  (Fig.  104). 
Stimulation  of  this  nerve  slows  the  heart.  There  is  no  anatomical  or 
physiological  evidence  of  a  sympathetic  nerve  to  the  heart,  but 
abundant  sympathetic  fibres  run  to  the  arteries.  Small  doses  of  adren- 
aline cause  prolonged  rise  of  blood-pressure. 

There  are  receptors  in  the  efferent  branchial  vessels  and  in  the  post- 
branchial  plexus  above  the  cardinal  veins  (p.  175).  Nerve  impulses 
from  these  receptors  can  be  recorded  in  the  vagus  at  each  systole  and 
are  increased  by  raising  the  blood-pressure.  Their  reflex  effects  are 
to  slow  the  heart  and  respiration  and  decrease  the  blood-pressure, 
perhaps  for  protection  of  the  gill  capillaries.  These  reflexes  are  pre- 
sumably the  ancestors  of  the  carotid  sinus  and  similar  reflexes  of  land 
vertebrates. 


162  ORGANIZATION  OF  THE  HEAD  v.  13 

13.  Urinogenital  system 

The  blood  of  the  elasmobranchs  differs  from  that  of  all  other  verte- 
brates in  its  very  high  content  of  urea.  As  measured  by  the  depression 
of  the  freezing-point  the  blood  is  isotonic  with  the  surrounding  sea 
water  (say,  3-5  per  cent.  NaCl);  it  may  even  be  slightly  hypertonic. 
But  there  is  far  less  salt  in  the  blood  than  in  the  sea,  in  fact  only 
about  1-7  per  cent.  NaCl.  Although  the  blood  is  nearly  isotonic  with 
the  sea  its  composition  is  therefore  regulated  (homeosmotic).  This 
arrangement  is  apparently  a  legacy  of  the  fact  that  the  ancestors  of  the 
elasmobranchs  were  originally  fresh- water  animals  (p.  187).  The 
return  passage  to  the  sea  has  been  accomplished  by  the  elasmobranchs 
through  the  device  of  urea  retention.  The  gill  surfaces,  in  which  alone 
the  blood  comes  into  close  contact  with  sea  water,  are  not  permeable 
to  urea,  but  this  substance  penetrates  freely  into  the  tissues,  as  it  does 
in  other  animals.  Elasmobranch  tissues  if  placed  in  sea  water  are 
therefore  in  contact  with  a  strongly  hypertonic  medium.  They  are  so 
habituated  to  the  presence  of  urea  that  they  are  unable  to  function 
unless  it  is  present  in  a  concentration  that  would  be  toxic  to  most 
animals. 

This  arrangement  has  presumably  been  responsible  for  the  fact 
that  few  of  the  elasmobranchs  have  returned  to  fresh  water.  In  the 
case  of  the  saw-fish  Pristis,  which  lives  some  hundreds  of  miles 
up  the  Mississippi  and  various  rivers  in  China,  Smith  found  that  a 
considerable  concentration  of  urea  is  still  maintained  in  the  blood, 
thus  further  increasing  the  work  that  these  fishes,  like  any  fresh-water 
animal,  must  do  in  order  to  maintain  an  osmotic  concentration  above 
that  of  the  surrounding  water.  One  shark  (Carcharhinus  nicaraguensis) 
and  some  rays,  Trygon,  also  live  in  fresh  water. 

In  the  ordinary  marine  elasmobranchs  the  high  urea  concentration 
is  maintained  by  the  presence  of  a  special  urea-absorbing  section  of 
the  kidney  tubules.  The  urinary  apparatus  is  a  mesonephros  and 
these  fishes  show  a  considerable  specialization  in  that  the  urinary 
functions  of  this  organ  are  separated  from  its  generative  ones  in  the 
male.  The  hinder  part  of  the  kidney  (sometimes  called  opisthone- 
phros,  the  term  metanephros  should  be  used  only  for  the  definitive 
kidney  of  amniotes,  which  has  a  different  method  of  development) 
consists  of  a  mass  of  tubules  ending  in  very  large  glomeruli,  and  a 
section  of  each  tubule  has  the  function  of  urea  absorption.  All  the 
tubules  join  to  form  a  series  of  five  urinary  ducts  and  these  enter  a 
urinary  sinus,  opening  to  the  cloaca.  The  sinus  can  be  compared 


v.  13  URINOGENITALS  OF  ELASMOBRANCHS  163 

functionally  with  a  bladder,  but  it  is  a  mesodermal  structure,  derived 
from  the  main  kidney  duct,  and  not  strictly  comparable  to  the  endo- 
dermal  bladder  of  tetrapods.  The  urinary  sinus  is  a  small  organ  and 
the  volume  of  liquid  excreted  is  small. 


Fie.  103.  A.  Urinogenital  system  of  the  female,  B,  of  the  male  dogfish. 
ah.p.  abdominal  pores;  cl.  cloaca;  cp.  claspers  of  the  male;  F.  rudiment  of  the  oviducal  opening 
in  the  male;  Md.  urinary  ducts;  mtn.  hinder  (excretory)  part  of  mesonephros;  od.  oviduct; 
oe.  cut  end  of  oesophagus;  of.  oviducal  funnel;  og.  oviducal  gland;  ov.  ovary;  P.f.  pelvic  fins; 
R.  rectum;  s.s.  sperm-sacs;  T.  testis;  up.  urinary  papilla  in  the  female;  ugp.  urogenital  papilla 
in  the  male;  vs.  urinary  sinus;  vc.  vasa  efferentia;  vs.  vesicula  seminalis;  WD.  Wolffian  duct; 
Wg.  Wolffian  gland  or  mesonephros.  (After  Bourne,  from   Goodrich,   Vertebrata,  A.  &  C. 

Black,  Ltd.) 

The  genital  system  is  highly  specialized  to  allow  internal  fertiliza- 
tion and  the  production  of  a  few  very  yolkv  and  well-protected  eggs. 
There  is  a  single  large  ovary,  from  which  the  eggs  are  carried  by  the 
cilia  of  the  peritoneum  to  a  pair  of  funnels  lying  on  either  side  of  the 
liver  behind  the  heart  (Fig.  103).  These  are  apparently  formed  from 
proncphric  funnels  and  the  Mullerian  duct  (oviduct)  separates  from 
the  original  nephric  duct.  In  the  adult  it  becomes  a  thick-walled 
muscular  tube,  bearing  a  swelling,  the  nidamental  gland,  the  upper 
part  of  which  produces  albumen,  the  lower  the  horny  egg  case. 


1 64  ORGANIZATION  OF  THE  HEAD  v.  13- 

The  testes  are  paired  and  sperms  are  collected  at  their  front  ends 
by  vasa  efferentia  leading  into  the  anterior  or  reproductive  portion  of 
the  mesonephros.  This  consists  of  a  much  coiled,  thick-walled,  vas 
deferens,  whose  glands  produce  material  that  aggregates  the  sperms 
into  spermatophores.  The  vas  expands  into  a  broader  ampulla 
(seminal  vesicle),  which  at  its  lower  end  gives  off  a  forwardly  directed 
blind  diverticulum,  the  sperm  sac,  developmentally  the  lower  end  of 
the  Miillerian  duct,  reduced  of  course  in  the  male;  small  funnels  are 
still  visible  at  the  upper  end. 

Transmission  of  the  sperms  is  produced  by  a  large  and  complicated 
pair  of  claspers.  These  are  modified  parts  of  the  pelvic  fins  of  the 
male,  developed  into  scroll-like  organs  and  containing  a  pumping 
mechanism  and  erectile  tissue;  they  are  inserted  into  the  female 
cloaca.  The  mechanism  of  erection  is  operated  by  nerves  and  may 
involve  the  liberation  of  adrenaline;  experimental  injection  of  that 
substance  will  produce  erection,  and  it  is  perhaps  significant  that  the 
male  possesses  a  reserve  of  adrenaline-producing  tissue  (see  p.  167). 

Development  of  elasmobranchs  is  by  partial  cleavage,  producing  a 
blastoderm,  perched  on  the  top  of  a  large  mass  of  yolk.  The  egg  is 
protected  by  an  elaborate  egg-case,  the  'mermaid's  purse',  within 
which  development  proceeds  until  the  yolk  has  been  used  up. 

In  several  elasmobranchs  development  is  viviparous,  the  oviduct 
forming  a  'uterus'.  In  Mustelus  there  is  a  yolk-sac  placenta,  but  in 
Trygon  'uterine  milk'  is  secreted  into  the  embryo  by  villi  (trophone- 
mata)  inserted  through  the  spiracles. 

14.  Endocrine  glands  of  elasmobranchs 

Elasmobranch  fishes  possess  the  full  complement  of  endocrine 
glands,  but  these  show  some  interesting  differences  from  those  of 
higher  vertebrates.  The  pituitary  body  lies  in  the  usual  place  below 
the  diencephalon  and  anterior,  intermediate,  tuberal,  and  neural 
divisions  can  be  recognized.  Little  is  known  of  the  functions  of  the 
gland.  The  gonads  of  the  dogfish  retrogress  after  removal  of  the  pitui- 
tary. Little  or  no  vasopressin  or  oxytocin  is  present.  The  neuro- 
intermediate  lobe  contains  a  substance  that  produces  the  expansion 
of  melanophores.  Hogben  and  Waring  have  also  produced  evidence 
that  the  pars  anterior  produces  a  substance  causing  contraction  of  the 
melanophores,  but  this  has  not  yet  been  isolated  and  the  evidence  for 
its  existence  is  indirect. 

The  thyroid  is  formed  by  a  downgrowth  from  the  floor  of  the 
pharynx,  to  which  it  often  remains  attached  by  a  narrow  stalk  con- 


v.  i4 


ADRENAL  TISSUE 


165 


sp  n 


Fig.  104.  Dissection  of  suprarenal  bodies  and  sympathetic  nervous  system  of  the 

dogfish. 
b.a.  brachial  artery;  c.a.  coeliac  artery;  d.a.  dorsal  aorta;  g.  first  sympathetic  ganglion;  hyp. 
hypoglossal  nerve;  I.e.  longitudinal  sympathetic  'chain';  n.card.  cardiac  branch  of  vagus; 
p.b.p.  post-branchial  plexus;  r.c.  ramus  communicans;  s.  sensory  fibre;  s.a.  segmental  artery; 
sg.  sympathetic  ganglion;  sp.a.  anterior  splanchnic  nerve;  sp.m.  middle  splanchnic  nerve; 
spa.  spinal  nerve;  sup.  suprarenal  body;  v.  ventricle;  v.d.  vas  deferens;  vs.  vago-sympathetic 
anastomosis;  X.  vagus;  X.br.  branchial  branch  of  vagus;  X.visc.  visceral  branch  of  vagus. 
(After  Young,  Quart.  J.  Micr.  Sci.  75.) 

taining  a  small  ciliated  pit,  a  reminder  that  the  organ  was  once  a 
ciliated  mucus-secreting  gland. 

The  adrenal  tissue  is  especially  interesting  because  the  two  parts, 
so  closely  associated  in  mammals,  are  here  found  widely  separated.  A 
segmental  series  of  glands,  the  suprarenals,  are  rich  in  noradrenaline. 
They  project  into  the  dorsal  wall  of  the  posterior  cardinal  sinus  and  can 
be  seen  when  it  is  opened  (Fig.  104).  The  more  anterior  ones  are 
fused  to  form  an  elongated  structure  on  either  side  of  the  oesophagus. 


(i  66) 


n  v 


Fig.  105.  Diagram  of  transverse  section  through  hind  region  of  mesonephros  of 

dogfish. 

cv.  cardinal  vein;  da.  dorsal  aorta;  int.  interrenal  body;  k.  mesonephros;  I  c.  longitudinal 

sympathetic  connective;    n  c.  sympathetic    nerve-cells    scattered   in    suprarenal    body;    nv. 

sympathetic  nerves;  re.  ramus  communicans;  sg.  sympathetic  ganglion;  sv.  subcardinal  vein; 

sup.  suprarenal  body.  (From  Young,  Quart.  J.  Micr.  Sci.  75.) 


Fig.  106.  Diagram  of  arrangement  in  hinder  mesonephric  region  of  dogfish. 
Lettering  as  Fig.  105.  tr.  transverse  sympathetic  nerve.  (From  Young,  Quart.  J.  Micr.  Sci.  75.) 


v.  i4-i5  BRAIN  OF  ELASMOBRANCHS  167 

The  sympathetic  ganglia  are  closely  associated  with  these  suprarenal 
bodies,  as  would  be  expected  from  their  common  origin  from  cells 
of  the  neural  crest.  The  segmental  series  continues  along  the  whole 
length  of  the  abdomen,  the  more  posterior  members  being  embedded 
in  the  kidney  tissue  (Fig.  105).  These  posterior  suprarenal  bodies  are 
larger  in  the  male  than  in  the  female,  but  only  the  central  part  of  the 
male  glands  shows  the  reaction  with  chrome  salts  that  indicates  the 
presence  of  adrenaline.  The  peripheral  portion  of  each  gland  appears 
to  consist  of  non-functioning  cells,  possibly  a  reserve  used  only  during 
reproduction  (see  p.  164). 

The  part  of  the  adrenal  corresponding  to  the  cortex  of  mammals  is 
represented  in  elasmobranchs  by  the  interrenal  bodies,  lying  medially 
in  some  species,  paired  in  others,  in  the  kidney  region  (Figs.  105  and 
106).  The  cells  of  these  organs  resemble  cortical  adrenal  cells.  Since 
they  are  not  in  contact  with  the  suprarenals  at  any  point,  it  would  seem 
that  the  association  of  the  two  parts  is  not  necessary  for  their  function- 
ing, at  least  in  these  animals.  Removal  of  the  interrenal  is  always  fatal. 
The  gland  is  stimulated  by  'stress'  or  by  mammalian  ACTH.  Extracts 
of  it  prolong  the  life  of  adrenalectomized  rats.  There  is  evidence  that 
it  influences  carbohydrate  metabolism  and  activity  of  the  gonads  but 
not  electrolyte  balance. 

The  islets  of  Langerhans  contain  two  cell  types  as  in  mammals. 
The  pineal  body  is  small  and  without  any  trace  of  eye-like  structure. 

The  gonads  contain  endocrine  organs,  producing  steroid  hormones. 
These  are  formed  by  interstitial  cells  in  the  testes.  Oestrogens  probably 
come  from  the  outer  (theca)  cells  of  the  follicles  that  surround  the 
eggs.  The  inner  (granulosa)  cells  of  the  capsule  assist  in  yolk  produc- 
tion but  may  also  produce  progesterone  and  in  viviparous  species 
they  develop  into  a  distinct  corpus  luteum  after  ovulation. 

15.  Nervous  system 

The  brain  is  large  and  well  developed  in  elasmobranchs,  having  a 
structure  characteristically  different  from  that  of  both  the  cyclostomes 
and  bony  fishes  (Fig.  100).  The  forebrain  is  large  and  has  cerebral 
hemispheres  thickened  both  in  floor  and  roof,  whereas  in  teleosts  the 
roof  is  thin.  The  hemispheres  are  wide  relative  to  their  length  and  the 
end  of  the  unpaired  portion  of  the  forebrain  between  the  hemispheres, 
the  lamina  terminalis,  is  also  much  thickened.  Attached  to  the  ends 
of  the  cerebral  hemispheres  are  large  olfactory  bulbs  and  there  are 
also  large  nasal  sacs.  Evidently  the  olfactory  sense  is  well  developed 
in  these  animals  and  they  depend  greatly  on  it  for  hunting. 


1 68 


ORGANIZATION  OF  THE  HEAD 


v.  15 


All  parts  of  the  cerbral  hemispheres  receive  fibres  from  the  olfac- 
tory bulbs  and  the  forebrain  serves  mainly  for  analysing  the  olfactory 
impulses.  However,  it  is  stated  that  there  are  fibres  reaching  forward 
to  one  area  at  the  back  of  the  roof  of  the  hemispheres  from  other 
centres.  Johnston  therefore  called  this  region  the  'general  somatic 
area'  and  suggested  that  it  represents  the  beginnings  of  that  develop- 
ment so  characteristic  of  mammals  by  which  all  the  senses  are  centred 
on  the  cerebral  hemispheres.  Further  work  is  needed  to  confirm  the 


Dec  interhemisph 


.,  Tr  medianus 


Ventr  o/f 


Tr  olFacb. 

Tr  olFacb.  epistr  cruc. 


Fiss  Urn  tel. 


Ventrical,  /at. 


Fig.  107.  A  cross-section  through  the  forebrain  of  a  shark. 

Dec. interhemisph.   decussatio   interhemispherica;    Fiss.lim.tel.    fissura    limitans   telencephali; 

Prim. hip.    primordium    hippocampi;    5.    septum;    Striat.    striatum;    Tr. medianus.    tractus 

medianus;    Tr.oljact.    tractus    olfactorius;    Tr.olf act. epistr. cruc.   tractus   olfacto-epistriaticus 

cruciatus;  Ventricul.lat.  ventriculus  lateralis;  Ventr. o.f.  ventriculus  olfactorius. 

(From  Kappers,  Huber,  and  Crosby.) 

existence  of  this  pathway,  and  even  if  present  its  significance  must 
not  be  exaggerated.  There  is  of  course  no  cortical  arrangement  of 
tissue  in  the  hemispheres.  The  cells  form  thick  masses  around  the 
ventricle  (Fig.  107).  The  roof  is  quite  thick  and  contains  decussating 
fibres  in  the  midline.  The  sides  and  floor  make  up  the  main  bulk  of  the 
organ,  the  lateral  wall  being  known  as  the  striatum,  its  upper  part  the 
epistriatum.  The  medial  wall  is  known  as  the  septum  and  its  upper 
portion  is  often  referred  to  as  the  primordium  hippocampi,  having  a 
position  similar  to  that  of  the  hippocampus  of  mammals.  The  main 
efferent  pathways  are  tracts  leading  to  the  hypothalamus  and  to  the 
optic  lobes.  After  removal  of  the  forebrain  the  sense  of  smell  is  lost 
but  the  fish  shows  no  obvious  disturbance  of  posture,  locomotion,  or 
behaviour. 

The  diencephalon  is  a  narrow  band  of  tissue,  there  are  no  extensive 
tracts  leading  forward  through  it,  and  the  optic  and  other  pathways 
do  not  end  here  as  they  do  in  higher  animals.  The  lower  part  of  the 


v.  15  BRAIN  OF  ELASMOBRANCHS  169 

between-brain,  the  hypothalamus,  is,  however,  as  well  developed 
(relatively)  in  these  animals  as  in  mammals.  Its  hind  part  (inferior 
lobes)  receives  olfactory  impulses  via  the  forebrain  (the  'fornix'  of 
higher  vertebrates)  and  gustatory  pathways  from  the  medulla.  Its 
efferent  fibres  run  to  reticular  centres.  The  more  anterior  part  of  the 
hypothalamus  lies  above  the  pituitary  and  contains  the  supraoptic 
nucleus,  whose  axons  form  the  hypophysial  tract,  ending  in  the  inter- 
mediate lobe.  The  supraoptic  cells  of  all  vertebrates  are  large  and 
contain  granules  of  neurosecretory  material  that  is  probably  passed 
down  the  axons  and  liberated  in  the  pituitary.  The  anterior  hypo- 
thalamus is  a  higher  centre  for  visceral  control,  regulating,  for 
example,  circulation,  respiration,  and  many  metabolic  activities. 
Attached  to  the  hind  end  of  the  hypothalamus  of  fishes  is  a  peculiar 
organ,  the  saccus  vasculosus,  with  folded,  pigmented  walls.  It  has 
been  suggested  that  this  acts  as  a  pressure  receptor,  since  it  is  well 
developed  in  deep-sea  fishes.  It  is  one  of  the  characteristic  features 
that  the  sharks  and  bony  fishes  have  in  common. 

The  midbrain,  as  in  cyclostomes  and  teleosteans,  is  very  large  and  is 
perhaps  the  dominant  centre  of  the  brain.  The  optic  tracts  end  in  its 
roof  (tectum  opticum)  after  complete  decussation  below  the  brain. 
The  cells  of  the  tectum  are  arranged  in  a  complicated  pattern  of 
layers.  Other  sensory  centres  that  send  tracts  to  the  optic  lobes  are 
the  olfactory  (cerebral  hemispheres),  acustico-lateral,  cerebellar, 
gustatory,  and  probably  also  the  general  cutaneous  centres  of  the 
spinal  cord.  Efferent  tracts  leave  the  midbrain  roof  to  the  base  of 
the  midbrain  and  extend  backwards  into  the  medulla,  perhaps  into  the 
spinal  cord.  The  efferent  midbrain  fibres  have  direct  influence  on 
the  spinal  cord,  and  electrical  stimulation  of  points  on  the  tectum 
opticum  produces  various  movements  of  the  fins,  suggesting  a  system 
of  control  similar  to  that  exercised  over  spinal  centres  by  the  cerebral 
cortex  of  mammals  through  the  pyramidal  tract.  Various  forced 
movements  follow  injury  to  the  midbrain. 

The  cerebellum  is  a  very  large  organ  in  clasmobranchs,  as  in  all 
animals  that  move  freely  in  space.  Its  main  source  of  sensory  fibres  is 
from  the  ear  and  from  the  organs  of  the  lateral  line  system,  whose 
afferent  fibres  enter  through  the  seventh,  ninth,  and  tenth  cranial 
nerves.  The  internal  structure  of  the  cerebellum  is  very  uniform  and 
essentially  similar  in  all  vertebrates.  Removal  of  portions  of  it  from 
dogfishes  produces  aberrations  of  swimming. 

The  medulla  oblongata  is  the  region  from  which  most  of  the  cranial 
nerves  spring  and  especially  those  that  regulate  the  respiration  and 


i7o  ORGANIZATION  OF  THE  HEAD  v.  15- 

visceral  functions.  In  mammals  this  control  is  indirect,  but  in  fishes 
the  nerves  that  spring  from  the  medulla  directly  innervate  the 
respiratory  muscles  of  the  gills  and  floor  of  the  mouth.  It  is  no  doubt 
for  this  reason  that  the  centre  for  the  initiation  of  the  respiratory 
rhythm  developed  in  the  medulla. 

16.  Receptor-organs  of  elasmobranchs 

The  paired  nasal  sacs  have  much-folded  walls.  Water  enters  by  a 
single  opening  but  this  may  be  partly  divided  by  a  fold,  making  a 
groove,  which  may  open  to  the  mouth.  There  are  taste-buds  scattered 
over  the  wall  of  the  pharynx.  It  has  been  shown  experimentally  that, 
as  in  higher  animals,  these  are  receptors  for  sampling  the  food  after 
it  has  been  brought  close  to  the  animal,  whereas  the  nose  acts  as  a 
distance  receptor.  Smell  and  taste  are  therefore  different  senses  for  a 
dogfish,  as  for  us.  By  training  fishes  to  discriminate  between  various 
substances  it  can  be  shown  that  those  that  we  should  smell  are 
detected  by  the  nose  in  the  dogfish,  but  its  organs  of  taste,  like  ours, 
can  discriminate  only  between  a  few  qualities,  including  salt,  sour, 
and  bitter. 

The  eyes  are  well  developed  in  sharks  and  no  doubt  serve  as  an 
important  means  of  finding  the  prey  and  avoiding  enemies.  However, 
the  retina  usually  contains  only  rods,  and  visual  discrimination  is 
probably  poor,  but  there  are  cones  in  Mustelus  and  Myliobatis.  Unfor- 
tunately details  as  to  the  functional  performance  of  the  eyes,  ability  to 
discriminate  shapes,  &c,  are  scanty.  Behind  the  retina  there  is  often  a 
reflecting  layer,  the  tapetum  lucidum.  This  may  be  provided  with 
pigment  cells,  which  expand  in  the  light  but  contract  in  darkness, 
allowing  the  underlying  guanophores  to  reflect,  thus  increasing 
sensitivity.  The  lens  is  spherical  and  very  hard,  as  in  all  fishes,  since 
it  must  perform  the  whole  work  of  refraction.  It  is  provided  with  a 
protractor-lentis  muscle,  presumed  to  produce  active  accommodation 
for  near  vision  by  swinging  the  lens  forward.  The  iris  is  peculiar  in 
those  elasmobranchs  that  hunt  by  day;  when  it  narrows  it  divides 
the  pupil  into  two  slits  by  the  descent  of  an  upper  flap  or  operculum. 
The  muscles  of  the  iris  are  better  developed  in  elasmobranchs  than 
in  most  bony  fishes  and  the  pupil  makes  wide  excursions.  The 
sphincter  iridis  muscle,  which  narrows  the  pupil,  works  as  an  inde- 
pendent effector.  It  is  stimulated  to  contract  by  light,  but  its  move- 
ments are  not  controlled  by  any  nervous  mechanism.  The  radial 
dilatator  fibres,  which  open  the  pupil,  receive  motor-fibres  from  the 
oculomotor   nerve.    The   closure   of  the   iris   when   illuminated   is 


v.  i6  RECEPTORS  OF  ELASMOBRANCHS  171 

relatively  slow.  If  the  whole  eye  is  cut  out  from  the  head,  in  the  dark, 
the  sphincter,  being  an  independent  effector,  still  closes  when  illumi- 
nated. The  muscle,  being  without  nerves,  is  not  affected  by  any  of  the 
usual  drugs  that  mimic  action  of  the  autonomic  nervous  system, 
though  some  of  these  affect  the  innervated  dilatator  muscle.  We  have 
therefore  the  curious  situation  that  no  'autonomic'  drugs  applied  to 
the  isolated  dark  adapted  eye  cause  closure  of  the  pupil ;  this  can  only 
be  produced  by  illumination  (Fig.  108). 

The  ear  of  elasmobranchs  contains  receptors  concerned  (1)  with 
maintenance  of  muscle  tone,  (2)  with  angular  accelerations,  (3)  with 

Red 


Red 


White 


Adrenaline  j//00,000 


Minutes 


Fig.  108.  Movements  of  margin  of  pupil  of  an  isolated  iris  of  the  shark  Mustelus, 
followed  by  plotting  with  a  camera  lucida  and  here  shown  magnified  53  X  .  Addition 
of  adrenaline  causes  slight  dilation  of  the  already  dilated  pupil  and  illumination  then 
causes  closure.  Acetyl  choline  even  in  concentrations  of  1  in  10,000  has  a  similar 
dilatory  effect.  (From  Young,  Proc.  Roy.  Soc.  B.  112.) 

gravity,  (4)  perhaps  with  hearing.  There  are  three  pairs  of  semi- 
circular canals,  each  with  an  ampulla  containing  receptor  cells,  whose 
hairs  are  embedded  in  a  gelatinous  cupula.  This  behaves  as  a  highly 
damped  torsion  pendulum,  swinging  with  movement  of  the  fluid. 
These  receptors  discharge  impulses  continuously  and  during  angular 
rotations  the  frequency  is  either  increased  or  decreased  in  the  appro- 
priate ampullae,  initiating  compensatory  movements  of  the  eyes  and 
fins. 

The  otolith  organs  include  three  patches  of  receptor  cells  in  par- 
tially distinct  sacs,  the  utricle,  saccule,  and  lagena.  The  endolym- 
phatic duct  is  an  open  canal  and  in  some  species  serves  to  admit  sand 
grains,  which  are  attached  to  the  maculae  as  gravity  receptors.  The 
utricle  seems  to  be  the  main  receptor  producing  appropriate  postures 
in  relation  to  gravity.  The  lagena  shows  a  maximum  discharge  rate 
near  the  normal  position  of  the  head  and  thus  serves  as  an  'into  level' 
receptor.  The  areas  of  these  maculae  that  carry  otoliths  do  not 
respond  to  vibrational  stimuli  but  carry  only  gravitational  receptors. 
Vibration  responses  in  the  form  of  nerve  impulses  have  been  seen 
in  rays  but  only  up  to  120  c/sec,  although  vestibular  microphonics 
up  to  750  c/sec  occur.  At  high  intensity  there  is  much  synchronization 


172  ORGANIZATION  OF  THE  HEAD  v.  16- 

of  units.  These  results  suggest  that  the  ear  may  function  as  a  vibration 
receptor,  but  there  are  no  conditioning  experiments  to  show  whether 
these  fishes  can  hear. 

There  is  a  well-developed  system  of  lateral  line  organs,  whose 
function  is  considered  later  (p.  218).  The  organs  of  this  system  on  the 
head  are  highly  modified  in  elasmobranchs  to  form  the  ampullae  of 
Lorenzini,  long  canals  filled  with  mucus.  Sand  showed  that  these 


Fig.  109.  Drawing  of  a  sympathetic  ganglion  and  related  structures  in  a  dogfish. 
Lettering  as  in  Figs.  104  and  105.  s.o.  sense-organs.  (After  Young,  Quart.  J.  Alter.  Sci.  75.) 

organs  increase  their  discharge  of  nerve  impulses  with  very  slight 
falls  of  temperature,  and  he  suggested  that  their  function  is  to  detect 
such  changes.  They  are  also  sensitive  to  weak  tactile  stimulation  and  to 
small  voltage  gradients  in  the  water.  Their  function  therefore  remains 
uncertain.  It  may  be  related  to  determining  changes  of  hydrodynamic 
pressure  distribution  over  the  surface  of  the  aerofoil-like  body, 
especially  in  skates  and  rays.  They  may  thus  act  as  mechano-receptors 
detecting  local  changes  of  pressure  near  the  body  surface. 

No  doubt  elasmobranchs,  like  other  animals,  have  many  senses 
referred  to  the  skin,  such  as  we  call  touch,  pain,  and  the  like,  but  few 
studies  of  these  exist.  Sand  has  shown  the  presence  of  volleys  of 
impulses  in  the  nerves  connected  with  muscles  when  the  latter  are 
stretched.  Proprioceptors  have  been  demonstrated  histologically  in 
the  muscles  of  Raja.  This  agrees  with  the  fact  that  after  severance  of 
the  spinal  cord  the  swimming  rhythm  only  continues  if  some  afferent 
nerves  are  intact. 


v.  17 


SYMPATHETIC   OF   ELASMOBRANCHS 


173 


17.  Autonomic  nervous  system 

The  sympathetic  system  of  elasmobranchs  consists  of  an  irregular 
series  of  ganglia,  approximately  segmental,  lying  dorsal  to  the  pos- 
terior cardinal  sinus  and  ex- 
tending back  above  the  kidneys. 
These  ganglia  contain  motor 
nerve-cells  (post  -  ganglionic 
cells)  whose  ascons  end  in  the 
smooth  muscles  either  of  the 
arterial  walls  or  of  the  viscera. 
The  cells  themselves  are  con- 
trolled by  pre-ganglionic  nerve- 
fibres  whose  cell  bodies  lie  in 
the  spinal  cord  and  whose  pro- 
cesses run  out  in  the  ventral 
spinal  roots  and  rami  com- 
municantes  (Fig.  109).  In 
higher  animals  the  sympa- 
thetic ganglia  send  postgangli- 
onic fibres  back  to  the  spinal 
nerves  for  distribution  to  the 
skin  ('grey  rami  communi- 
cantes')  but  these  are  absent  in 
elasmobranchs  and  correspon- 
dingly there  is  no  evidence  of 
sympathetic  control  of  skin 
functions  (e.g.  chromato- 
phores);  a  very  different  con- 
dition is  found  in  bony  fishes 
(p.  222).  Another  peculiarity 
of  the  sympathetic  system  of 
elasmobranchs  is  that  it  does 
not  extend  into  the  head.  This 
condition  is  unique  among 
vertebrates,  but  it  is  not  clear 
whether  it  is  primary  or  the 
result  of  a  secondary  loss. 

In  mammals  it  is  usual  to 
recognize  a  parasympathetic 
system  acting  in  antagonism  to 


symp 


Fig.   i  10.  Diagram  of  the  autonomic  nervous 

system  of  the  dogfish. 
art.  artery;  card.n.  cardiac  nerve;  cil.g.  ciliary  gang- 
lion; ft.  heart;  in.  intestine;  k.  mesonephros;  ov. 
oviduct;  ph.  pharynx;  pr.  profundus  nerve;  py. 
pylorus;  st.  stomach;  symp.  sympathetic  ganglion 
(with  suprarenal  near  it);  u.s.  urinogenital  sinus; 
III,   V,   VII,  IX,  X,  cranial  nerves.  (From  Young, 

Quart.  J.  Micr.  Sci.  75.) 


i74  ORGANIZATION  OF  THE  HEAD  v.  17 

the  sympathetic,  but  this  is  not  easy  to  define  in  the  elasmobranchs 
(Fig.  no).  The  vagus,  it  is  true,  is  well  developed,  with  branches 
to  the  heart  and  gut,  but  little  is  known  of  autonomic  fibres  in  the 
other  cranial  nerves,  or  of  a  special  'sacral'  parasympathetic  system. 
Stimulation  of  either  the  vagus  or  the  sympathetic  nerves  causes 
contraction  of  the  stomach.  A  ciliary  ganglion  connected  with  the 
oculomotor  nerve  is  present  as  in  other  animals,  but  there  is  no 
sense  in  which  it  can  be  called  antagonistic  to  the  sympathetic 
system,  since  the  latter  does  not  extend  into  the  head.  The  post- 
branchial  plexus  is  a  network  of  fibres  and  cells  connected  with  the 
vagus  but  stretching  back  above  the  posterior  cardinal  sinus 
(Fig.  104).  Receptors  in  this  plexus  and  in  the  afferent  branchials 
(Fig.  109)  may  be  concerned  with  vascular  reflexes  (p.  161). 


VI 


EVOLUTION  AND  ADAPTIVE  RADIATION  OF 
ELASMOBRANCHS 

1 .  Characteristics  of  elasmobranchs 

The  organization  of  a  shark  used  to  be  considered  to  show  the  earlier 
stages  of  fish  evolution,  but  we  have  seen  evidence  that  this  is  a  mis- 
take (p.  131).  The  sharks  and  skates  and  rays  are  highly  developed 
creatures;  in  particular,  the  absence  of  bone  is  a  secondary  feature; 
they  have  been  able  to  give  up  their  defensive  armour  because  of  the 
development  of  other  means  of  protection,  swift  swimming,  good 
sense-organs  and  brain,  and  powerful  jaws.  We  can  now  examine  the 
history  of  these  changes  and  study  the  varied  creatures  that  can  be 
classified  as  elasmobranchs.  As  usual  in  examining  such  histories  we 
must  try  to  discover  evidence  about  the  forces  that  have  operated  to 
produce  the  changes  of  type,  and  look  for  signs  of  any  consistent 
trends,  persisting  for  long  periods  of  years. 

2.  Classification 

Superclass  Gnathostomata 
Class  Elasmobranchii  (  =  Chondrichthyes) 
Subclass  1.  Selachii 
*Order  1.  Cladoselachii.  Devonian-Permian 

*CIadoselache;  *Goodrichia 
*Order  2.  Pleuracanthodii.  Devonian-Trias 

*Pleur  acanthus 
Order  3.  Protoselachii.  Devonian-Recent 

*Hybodiis;  Hetcrodontus 
Order  4.  Euselachii.  Jurassic-Recent 
Suborder  1.  Pleurotremata.  Jurassic-Recent 
Division  1.  Notidanoidea.  Jurassic-Recent 
Hexanchus ;  Clilamydoselache 
Division  2.  Galeoidea.  Jurassic-Recent 

Scyliorhinus;  Mustelus;  Cetorhinus;  Carcharodon 
Division  3.  Squaloidea.  Jurassic-Recent 
Squalus;  Sqaatina;  Pristiophorus ;  Alopias 
Suborder  2.  Hypotremata.  Jurassic-Recent 
Raja;  Rhinobatis;  Pristis;  Torpedo;  Trygon 


176         EVOLUTION  OF  ELASMOBRANCHS       vi.  2-3 

Superclass  Gnathostomata  (cont.) 

Subclass  2.  Bradyodonti.  Devonian-Recent 
*Order  1.  Eubradyodonti.  Devonian-Permian 

*HeIodus 
Order  2.  Holocephali.  Jurassic-Recent 

Chimaera 

The  elasmobranchs  form  a  very  compact  group  of  fishes,  nearly 
always  marine  and  of  predaceous  habit,  having  a  great  quantity  of 
urea  in  the  blood,  with  no  bone  in  the  skeleton,  no  operculum  over 
the  gills,  and  no  air-bladder.  The  tail  is  usually  heterocercal.  The 
pectoral  fin  is  anterior  to  the  pelvic  and  the  latter  is  usually  provided 
with  claspers,  fertilization  being  internal.  The  body  is  more  or  less 
completely  covered  with  placoid  scales  (denticles)  and  these  are 
specialized  in  the  mouth  to  form  rows  of  teeth.  The  intestine  is  short 
and  provided  with  a  spiral  valve.  The  typical  cartilage-fishes  with 
these  characters  may  be  placed  in  the  subclass  Selachii,  to  distinguish 
them  from  an  early  aberrant  offshoot  the  Bradyodonti,  represented 
today  by  the  peculiar  creature  Chimaera  (p.  184). 

3.  Palaeozoic  elasmobranchs 

The  selachians  are  among  the  most  numerous  of  the  various  pre- 
datory animals  in  the  sea.  There  have,  however,  been  many  side- 
branches  of  the  main  shark  line  and  we  may  now  survey  the  history 
of  the  group  from  its  first  appearance.  The  characters  we  have  used 
in  our  definition  mark  the  elasmobranchs  off  from  the  earliest-known 
gnathostomes,  the  acanthodians  and  other  placoderm  types  (Fig.  1 1 1), 
which  we  shall  consider  later  (p.  186).  Presumably  the  elasmobranchs 
were  derived  from  some  placoderm,  but  the  earliest  evidence  of  the 
existence  of  true  sharks  is  in  the  form  of  isolated  teeth  and  scales  from 
Middle  Devonian  deposits,  and  the  earliest  type  about  which  full 
information  exists  is  *Diade?nodus  from  the  Upper  Devonian,  'an 
early  and  not  distant  offshoot  from  the  primitive  Chondrichthyan 
stock,  the  main  line  of  which  led  through  *Ctenacanthus  and  the 
hybodonts  to  the  modern  elasmobranchs ;  *Cladoselache  is  a  specialized 
side-line  of  this  main  stock  and  is  not  an  appropriate  ancestral  type 
for  the  Chondrichthyes'  (Harris).  The  teeth  of  *Diademodus  are 
many-cusped  and  resemble  the  scales  more  closely  in  sculpturing 
than  in  other  primitive  sharks.  The  jaw  suspension  was  amphistylic 
and  the  notochord  unconstricted.  The  pectoral  fin  was  continuous 
posteriorly  with  the  body  wall  and  there  was  no  well-developed 


(i77) 


Cenozoic 


Cretaceous 

100- 


Jurassic 


^5 


Triassic 


Perm/an 
200 


Carbonifcrou. 


,tha 


,.  .„,  Torpedo- 

II.        HIP 


AcMtnedu  ^V^vxi  L I  f) 


Silurian 


S.     * 


DieiroleP'i 


Ordoi/iaan 


400- 


Cambrian 


FlG.  hi.  The  early  evolution  of  vertebrates. 


i78 


EVOLUTION  OF  ELASMOBRANCHS 


VI.  3 


pectoral  girdle.  The  tail  was  heterocercal  and  there  are  no  signs  of  skele- 
tal support  for  lateral  keels.  All  of  these  Harris  regards  as  primitive 
features;  *Diademodus  was  specialized  in  having  no  spines  in  front 
of  the  dorsal  fin  and  no  clasper  on  the  head.  Both  of  these  features  are 
frequent  in  hybodonts  and  in  *Cladoselache  there  is  a  large  spine 


zd    nsi 


Fig.  112.  Development  of  the  fins  of  the  dogfish,  i,  Adult  showing  the  nerve-supply 
of  the  fins ;  2,  adult  with  the  fins  shown  expanded  and  their  nerves  and  muscles  shown 
as  if  concentration  had  not  taken  place;  3,  a  19-mm.  embryo,  showing  the  actual 

condition. 

a.  anal  fin;  ac.  anterior  collector  nerve  of  first  dorsal  fin;  cr.  (black)  cartilaginous  radial 

partially   hidden   by  the  radial   muscle;  n.    1-57,  spinal  nerves  and  ganglia;  pc.  collector 

nerve  of  second  dorsal  fin;  pi.  pelvic  fin;  pt.  pectoral  fin;  rm.  radial  muscle;  id.  and  2d. 

first  and  second  dorsal  fins.    (From  Goodrich,  Vertebrata,  A.  &  C.  Black,  Ltd.) 

in  front  of  the  first  dorsal  fin.  These  fishes  were  thus  like  modern 
sharks  in  their  general  form,  but  the  fins  were  remarkable  in  having 
a  broad  base,  not  sharply  marked  off  from  the  body- wall.  It  has  been 
suggested  by  Goodrich  and  others  that  this  was  the  earliest  condition 
of  the  pectoral  fin,  perhaps  showing  its  derivation  from  a  continuous 
or  extended  fin-fold  (Fig.  113).  This  theory  has  the  advantage  that  it 
agrees  with  the  embryological  development  of  the  fin  by  concentration 
of  a  series  of  segments  (Fig.  112).  It  also  seems  likely  that  anterior 
and  posterior  fins  expanded  in  the  horizontal  plane  would  be  neces- 
sary for  stabilization  (p.  136).  Moreover,  this  theory  of  the  origin  of 
paired  fins  has  the  great  advantage  that  it  compares  them  with  the 
median  fins,  which  are  also  continuous  folds.  It  has  been  argued, 


vi.  3  PALAEOZOIC  ELASMOBRANCHS  179 

however,  that  the  cladoselachians  are  very  far  from  the  earliest  known 
fishes  and  that  in  both  ostracoderms  (p.  125)  and  placoderms  (p.  186) 
fins  are  known  that  have  a  narrowly  constricted  base.  We  cannot 
yet  say  for  certain  what  has  been  the  course  of  evolution  of  the  paired 
fins,  but  the  fin-fold  theory  has  much  plausibility,  in  spite  of  the 
difficulties  raised  by  palaeontologists. 


Fig.  113.  Pectoral  fins  of  various  fishes. 
a,  *Cladoselache\  b,  *Pleur acanthus;  c,  Ncoccratodus;  d,  Gadits.  (From  Norman.) 

The  cladoselachians  represent  the  ancestral  Devonian  sharks,  from 
which  all  later  forms  have  been  derived.  Animals  of  similar  type 
were  fairly  common  in  late  Devonian  and  Carboniferous  seas.  The 
ctenacanths,  such  as  *Goodrichia,  reached  a  length  of  8  ft.  Later 
radiation  of  the  selachians  took  place  along  three  different  lines, 
represented  by  the  three  remaining  orders  shown  in  the  classification. 
The  pleuracanthodians  (*Pleuracanthus)  were  a  specialized  group  of 
freshwater  carnivores.  The  tail  was  straight  (diphycercal)  and  the 
paired  fins  had  become  modified  accordingly  (see  p.  137).  The  axis 
was  completelv  freed  from  the  body  wall  to  give  a  paddle-like  fin, 
with  pre-  and  post-axial  rays,  a  type  known  as  archipterygial  (Fig. 
113),  because  it  was  once  supposed  to  be  ancestral  to  all  others.  A 
large  spine  on  the  head  gives  the  group  its  name.  Claspers  were  pre- 
sent. These  animals  were  common  in  the  Carboniferous  and  Lower 


180  EVOLUTION  OF  ELASMOBRANCHS  vi.  3- 

Permian,  but  in  subsequent  times  they  disappeared  without  leaving 
descendants. 

4.  Mesozoic  sharks 

After  flourishing  in  Palaeozoic  seas  the  shark  line  seems  to  have 
become  nearly  extinct  during  the  Permian  and  Trias.  During  this 
period  there  was  probably  little  fish  life  in  the  sea  and  the  stock 
seems  only  to  have  survived  by  adopting  a  varied  diet,  including 
invertebrate  food.  The  protoselachian  or  heterodont  sharks  of  this 
period  had  two  types  of  tooth,  pointed  ones  in  front  and  flattened 
ones,  for  crushing  molluscs,  behind.  Heterodontus,  the  Port  Jackson 
shark  of  the  Pacific,  is  a  surviving  form  having  a  dentition  of  this 
type. 

There  is  total  cleavage  of  the  yolk  of  the  egg.  The  meroblastic  form 
typical  of  modern  elasmobranchs  and  teleosts  was  therefore  a  rela- 
tively late  development  and  other  survivors  of  the  mesozoic  period 
besides  Heterodontus  also  show  holoblastic  cleavage  (pp.  184-236).  In 
later  Triassic  times  sharks  again  became  more  abundant,  and  this 
agrees  with  the  presence  of  numerous  bony  fish  types,  on  which  they 
presumably  fed.  Some  of  the  Triassic  sharks  still  possessed  a  hetero- 
dont dentition  (*Hybodus),  though  otherwise  much  like  the  modern 
forms. 

In  Jurassic  times  or  earlier,  however,  the  sharks  divided  into  the 
main  lines  that  exist  today.  In  the  suborder  Pleurotremata  or  true 
sharks  the  teeth  all  became  sharp  and  the  animals  swift  swimmers.  In 
the  suborder  Hypotremata,  on  the  other  hand,  the  teeth  remained 
flattened  and  sometimes  became  highly  specialized  for  a  mollusc- 
eating  diet  (Fig.  1 14),  producing  the  flattened  bottom-living  creatures, 
the  skates  and  rays.  The  stages  of  this  transition  can  be  followed,  and 
some  of  the  intermediate  types  still  exist.  Thus  in  Rhifiobatis,  the 
banjo-ray  (Fig.  in),  the  pectoral  fins  are  enlarged  but  still  distinct 
from  the  body.  Almost  identical  creatures  have  been  found  in  Jurassic 
rocks.  It  is  probable  that  several  separate  lines  showed  this  flattening 
of  the  body. 

5.  Modern  sharks 

The  Pleurotremata  may  be  divided  into  three  divisions  all  dating 
from  the  Jurassic.  The  Notidanoidea  show  many  primitive  features, 
such  as  an  amphistylic  jaw,  the  presence  of  six  or  seven  gill-slits,  and 
an  unconstricted  notochord.  Hexanckus  and  Heptranchias,  are  long- 
bodied,  slow-moving  sharks  from  warm  waters.  They  are  viviparous 


vi.  5 


SHARKS 


181 


but  without  placentae.  Chlamydoselache,  the  frilled  shark,  lives  in 
deep  water  and  feeds  on  cephalopods.  The  division  Galeoidea  is  much 
larger  and  includes  the  sharks  with  two  dorsal  fins,  not  supported  by 
spines.  Here  belong  the  dogfishes  Scyliorhinus  and  Miistelus,  both 
mainly  bottom-living  animals  feeding  on  a  mixed  diet,  including 


Fig.  114.  Teeth  of  various  elasmobranch  fishes. 

1,  Man-eater  (Carcharodon);  2,  tiger  shark  (GalaeocerJo);  3,  comb-toothed  shark  (Hexanchus); 

4,   sand-shark  (Odontaspis);   5,   blue  shark  (Carcharinus);   6,   nurse  shark  (Ginglymostoma); 

7,  guitar  rish  (Rhina),  8,  eagle-ray  {Myliobatis),  (After  Norman.) 


crustaceans  and  molluscs.  In  Cetorhimis,  the  basking  shark,  the  pre- 
daceous  habit  of  the  group  has  been  abandoned  in  favour  of  straining 
small  food  directly  from  the  plankton  by  means  of  special  combs  on 
the  gills  (gill  rakers),  an  arrangement  recalling  that  of  the  whalebone 
whales.  The  great  effectiveness  of  this  method  of  feeding  may  be  seen 
in  the  length  of  35  ft  or  more  attained  by  some  of  these  sharks.  Bask- 
ing sharks  produce  very  numerous  small  eggs,  which  develop  within 
an  'uterus',  but  without  placentae.  Rhineodon,  the  whale  shark,  is  also 


1 82  EVOLUTION  OF  ELASMOBRANCHS  vi.  5-6 

a  plankton  feeder  and  becomes  very  large.  It  is  not  closely  related  to 
the  basking  sharks.  It  moves  up  and  down  vertically,  the  mouth  open, 
sucking  in  plankton.  In  this  group  there  are  also  many  of  the  fiercest 
man-eating  sharks,  such  as  Carcharodon,  often  30  ft  long,  found  in 
many  seas.  Some  fossil  forms  of  this  genus  are  estimated  to  have 
reached  a  much  greater  length,  possibly  of  90  ft. 

The  division  Squaloidea  includes  those  sharks  in  which  there  is 
a  spine  in  front  of  each  dorsal  fin.  They  are  not,  however,  otherwise 
different  in  habits  from  the  other  sharks.  The  spiny  dogfish  (Squalus) 
is  a  well-known  type  and  here  belong  also  the  saw-sharks  (Pristio- 
phorus)  and  a  group  of  bottom-living  forms,  the  angel-fishes  or  monks 
[Squatina),  which  acquire  a  superficial  similarity  to  the  skates  and 
rays.  Alopias,  the  thresher,  is  said  to  differ  from  most  sharks  in  that 
instead  of  seizing  the  prey  as  it  is  presented,  it  hunts  systematically, 
several  sharks  working  together  and  using  their  whip-like  tails  to 
drive  smaller  fishes  such  as  mackerel  into  shoals,  where  they  are  then 
seized. 

6.  Skates  and  rays 

The  Hypotremata,  skates  and  rays,  have  become  specialized  for 
life  on  the  bottom  of  the  ocean  in  shallow  waters,  feeding  mainly  on 
invertebrates,  and  usually  having  blunt  teeth  (Fig.  114).  Locomotion 
is  no  longer  by  transverse  movements  of  the  body  but  by  waves  that 
pass  backwards  along  the  fins.  In  the  earlier  stages,  such  as  Rhino- 
bath,  the  banjo-ray,  which  has  existed  from  the  Jurassic  period  to  the 
present,  the  edges  of  the  fins  are  still  free  and  the  tail  is  well  developed. 
In  Pristis,  another  saw-fish  type,  outwardly  similar  to  Pristiophorus 
and  known  since  the  Cretaceous,  the  head  is  drawn  out  into  a  long 
rostrum  armed  with  denticles.  Its  use  is  uncertain  but  the  head  strikes 
from  side  to  side  among  shoals  of  fishes.  There  are  species  in  India, 
China,  and  the  Gulf  of  Mexico  that  live  in  fresh  water.  In  Raja,  first 
found  in  the  Cretaceous,  the  pectoral  fins  are  attached  to  the  sides  of 
the  body  and  the  median  fins  are  very  small,  whereas  in  the  more 
recent  Trygon  and  other  sting-rays  the  tail  is  reduced  to  a  defensive 
lash,  the  dorsal  fin  persisting  as  a  poison  spine.  In  the  eagle-rays 
(Myliobatis)  the  teeth  are  flattened  to  form  a  mill  able  to  grind  mollusc 
shells  (Fig.  114).  The  sea-devils  (Mobula)  have  expansions  of  the  fins 
at  the  front  of  the  head,  which  they  use  to  chase  fishes  to  the  mouth, 
hunting  in  packs.  In  Torpedo,  the  electric  ray,  the  fins  extend  so  far 
forward  that  the  front  of  the  animal  presents  a  rounded  outline.  The 
animal  is  protected  by  a  powerful  electric  organ,  formed  by  modified 


(i83) 


Torpedo 


Raja 

FIG.  115.  Various  elasmobranch. fishes. 


Chimaera         ^T 


184  EVOLUTION  OF  ELASMOBRANCHS  vi.  6- 

latcral  plate  muscle,  innervated  by  cranial  nerves.  Several  species  of 
Raja  have  weak  electric  organs  perhaps  used  for  guidauce  (p.  253). 

Life  on  the  bottom  has  produced  many  further  modifications  in  the 
skates  and  rays.  In  those  that  live  in  shallow  and  hence  well-illuminated 
waters  the  colour  of  the  upper  surface  is  often  elaborate,  the  under 
side  being  white.  In  certain  species  of  Raja,  for  example,  there  is  a 
pattern  of  black  and  white  marks,  which  probably  serves  to  break  up 
the  outline  of  the  fish. 

The  eyes  of  the  skates  and  rays  have  moved  on  to  the  upper  surface 
of  the  head  and  are  protected  by  well-developed  lids.  In  most  forms 
the  pupil  is  able  to  vary  widely  in  diameter  and  often  has  an  operculum 
by  which  the  aperture  can  be  reduced  to  two  small  slits. 

There  is  a  special  modification  of  the  respiratory  system  so  that 
water  is  drawn  in  not  through  the  mouth  but  by  the  spiracle,  which  is 
provided  with  a  special  valve  that  shuts  at  expiration,  as  the  water  is 
forced  out  over  the  gills.  The  Hypotremata  have  therefore  developed 
many  special  features  for  their  bottom-living  habits  and  have  diverged 
among  themselves  into  many  varied  lines.  They  have  been  very 
successful  and  are  among  the  commonest  fishes  in  the  sea. 

7.  Chimaera  and  the  bradyodonts 

Finally  we  must  consider  an  aberrant  group,  the  bradyodonts,  which 
diverged  from  the  main  stock  at  least  as  early  as  the  Carboniferous 
and  preserves  for  us  today  some  features  of  elasmobranch  life  at  that 
time  as  the  strange  Chimaera,  the  rat-fish  of  deep  seas  (Fig.  115). 
Instead  of  the  usual  large,  toothed  mouth  these  Holocephali  have  a 
small  aperture  surrounded  by  lips,  giving  the  head  a  parrot-like 
appearance.  The  teeth  are  large  plates  firmly  attached  to  jaws,  and 
the  upper  jaw  is  remarkable  in  being  fused  to  the  skull  ('holostylic'), 
the  hyoid  arch  being  free.  There  is  no  stomach  or  spiral  intestine. 
These  peculiarities  are  probably  associated  with  a  capacity  to  eat 
small  pieces  of  animal  food.  The  Holocephali  differ  further  from  the 
Selachii  in  the  presence  of  an  opercular  flap  attached  to  the  hyoid 
arch.  There  are  also  extra  claspers  in  front  of  the  usual  pelvic  ones 
and  an  organ  on  the  head  of  the  male  known  as  the  cephalic  clasper, 
whose  function  is  obscure.  The  notochord  is  unconstricted  and  the 
vertebrae  reduced  to  separate  nodules.  The  cleavage  is  holoblastic, 
as  in  other  fishes  with  features  of  mesozoic  type  (p.  180). 

Many  of  the  internal  features  resemble  those  of  selachians,  for 
instance  the  conus  arteriosus,  and  urinogenitals  in  which  there  are 
separate  urinary  and  spermatic  ducts.  The  brain  has  a  peculiar  shape 


vi.  8  TENDENCIES  IN  EVOLUTION  185 

on  account  of  the  large  size  of  the  eyes,  which  almost  meet  above  the 
brain,  so  that  the  diencephalon  is  long  and  thin. 

These  strange  creatures  appear  in  the  Jurassic,  apparently  de- 
scended from  the  somewhat  similar  bradyodonts  (such  as  *Helodus), 
which  were  common  in  the  Carboniferous  and  Permian.  They  pre- 
serve some  primitive  features  (vertebrae,  jaw  support,  open  lateral 
line  canals,  cleavage)  but  have  developed  many  specializations  in  the 
teeth,  operculum,  fins,  and  brain,  probably  in  connexion  with  life  on 
the  bottom  of  deep  seas. 

8.  Tendencies  in  elasmobranch  evolution 

The  elasmobranchs  have  been  in  existence  ever  since  the  Devonian, 
and  for  much  of  this  long  period  of  nearly  400  million  years  we  can  fol- 
low their  changes  with  some  accuracy.  This  type  of  fish  was  first 
formed  by  loss  of  the  heavy  bony  armour  of  the  earliest  gnatho- 
stomes,  associated  with  the  adoption  of  a  rapidly  moving  and  car- 
nivorous habit.  The  resulting  shark-like  form  has  remained  with 
relatively  little  change  through  the  whole  history  of  the  group;  clado- 
selachians  from  the  Devonian  are  remarkably  like  modern  sharks,  and 
it  would  be  difficult  to  assert  that  the  latter  show  clear  signs  of  being 
in  any  way  of  a  'higher'  type.  Both  are  in  fact  suited  to  the  same  mode 
of  life. 

If  our  interpretation  of  the  evidence  is  right,  however,  the  modern 
shark  type  has  been  evolved  from  the  Devonian  type  through  a  hetero- 
dont  stage.  During  the  late  Permian  and  Trias  there  was  little  fish 
food  for  the  sharks  and  they  appear  to  have  taken  to  living  on  inverte- 
brates. Eating  this  diet  was  presumably  easier  for  animals  possessing 
the  two  types  of  teeth  described  on  p.  180,  and  the  animals  also 
became  rather  flattened  with  their  life  on  the  bottom.  On  the 
reappearance  of  numerous  fishes  in  the  sea,  in  the  Jurassic,  some  of 
these  heterodonts  resumed  the  shark-like  habit,  lost  the  crushing 
teeth,  and  developed  into  the  varied  fish-eating  types  alive  today. 
Others  of  the  heterodonts,  however,  became  still  more  specialized  for 
bottom  life,  as  the  modern  skates  and  rays. 

It  is  difficult  to  see  any  persistent  tendency  in  all  this,  except  to  eat 
other  animals  of  some  sort.  When  fishes  are  available  sharks  will  eat 
them,  and  the  bodily  organization  for  doing  so  seems  to  have  been 
evolved  at  least  twice.  Similarly  other  members  of  the  same  stock  ate 
molluscs  and  Crustacea  and  became  modified  for  this.  The  tendency 
is  for  survival  or  continuance  of  the  animals  and  this  leads  them 
to  adopt  whatever  habits  are  possible  given  their  surroundings.  In 


i86  EVOLUTION  OF  ELASMOBRANCHS  vi.  8- 

meeting  the  circumstances  certain  types  will  be  suitable  at  one  time, 
others  at  another.  We  know  that  genetic  variations  will  produce  fluctua- 
tions of  type — at  a  time  when  circumstances  force  the  animals  to  strive 
in  one  direction  those  with  a  particular  bodily  type,  say,  broad,  'hetero- 
dont'  teeth  will  be  selected.  When  fish  food  again  becomes  available 
those  animals  born  with  quicker  habits  and  sharper  teeth  will  be  able 
to  eat  the  fish  and  the  shark  type  returns. 

The  method  of  ensuring  stability  in  the  pitching  plane  adopted  by 
elasmobranchs  (p.  136)  necessitates  a  certain  flattening  of  the  front 
end  of  the  animal.  It  is  not  therefore  surprising  that  this  tendency  is 
often  exaggerated  and  has  several  times  produced  flattened  bottom- 
living  creatures,  such  as  the  skates  and  rays.  The  Actinopterygii 
show  the  opposite  tendency,  to  lateral  flattening  (p.  248).  We  might 
imagine  that  most  of  the  modern  skates  and  rays  had  become  so 
modified  in  structure  that  only  life  on  the  bottom  is  possible  for  them 
and  that  there  could  be  no  return  to  a  free-swimming,  fish-eating 
habit,  but  it  would  not  be  true  to  say  that  this  is  certain  or  that  the 
past  history  of  the  group  shows  undoubted  evidence  of  such  irrever- 
sible specialization. 

The  only  general  conclusion  from  our  study  of  elasmobranchs  since 
the  Devonian,  then,  is  that  they  have  tended  to  keep  alive  by  eating 
fish  or  invertebrates,  that  some  have  changed  little  during  this  time 
but  that,  judging  especially  from  the  modern  forms,  the  group  tends 
to  produce  varied  types  at  any  one  time,  each  able  to  find  its  food  in  a 
special  manner.  It  is  not  clear  that  the  group  has  advanced,  in  any 
sense,  since  the  Devonian.  The  type  has  always  been  a  successful  one, 
able  to  produce  specialized  carnivores.  We  do  not  know  enough  to  be 
sure  whether  the  number  of  creatures  with  this  organization  has 
changed  greatly,  but  it  seems  that,  except  for  a  reduction  in  numbers 
in  the  Triassic,  they  have  always  been  moderately  abundant  and  are 
perhaps  at  present  on  the  increase. 

9.  The  earliest  Gnathostomes,  Placoderms 

*Class  Placodermi  (=  Aphetohyoidea) 

*Order  1.  Acanthodii.  Silurian-Permian  (*Climatius) 
*Order  2.  Arthrodira.  Silurian-Devonian  (*Coccosteus) 
*Order  3.  Macropetalichthyida.  Devonian  (*Lunaspis) 
*Order  4.  Antiarchi  (=  Pterichthyomorphi).  Devonian  (*Bothri- 

olepis) 
*Order  5.  Stegoselachii.  Devonian-Carboniferous  (*Gemundina) 
*Order  6.  Palaeospondyli.  Devonian  {* Palaeospondylus) 


vi.  9  PLACODERMS  187 

It  has  already  been  mentioned  that  the  earliest  gnathostome  verte- 
brates found  in  the  rocks  do  not  have  the  shark-like  form,  and  present 
so  many  peculiarities  that  they  are  placed  in  a  distinct  class.  In  the 
past  the  fossils  included  here  have  been  referred  to  various  groups, 
usually  either  to  the  agnatha  or  the  elasmobranchs,  and  there  is  still 
some  doubt  as  to  their  position.  In  many  respects  they  are  highly 
specialized,  but  they  all  have  one  feature  that  may  be  presumed  to 
have  existed  in  the  ancestral  gnathostome,  namely,  that  the  hyoid  arch 
played  no  part  in  the  support  of  the  jaws  and  the  spiracle  was  there- 
fore a  typical  gill-slit.  For  this  reason  they  are  often  given  the  name 
Aphetohyoidea,  but  we  shall  prefer  to  call  them  Placodermi,  to  em- 
phasize that  they  all  have  a  heavy  armour  of  bone-like  material.  The 
class  contains  several  orders,  not  obviously  very  closely  related  to 
each  other;  all  are  fossil  forms,  none  of  which  is  known  to  have  sur- 
vived the  Permian. 

The  best-known,  earliest,  and  perhaps  most  interesting  group  is 
the  acanthodians,  found  in  freshwater  deposits  extending  from  the 
Upper  Silurian  to  the  Permian  but  chiefly  in  the  Devonian.  These 
were  small  fishes  with  a  fusiform  body  (Fig.  115),  with  heterocercal 
tail  and  two,  or  later  one,  dorsal  fins.  The  lateral  fins  consisted  of  a 
series  of  pairs,  often  as  many  as  seven  in  all,  down  the  sides  of  the 
body.  The  effect  of  these  in  stabilizing  the  fish  would  presumably  be 
different  from  that  of  a  continuous  fold,  and  the  problem  of  the  form 
and  function  of  the  earliest  paired  fins  remains  obscure.  The  fins  were 
all  supported  by  the  large  spines  from  which  the  group  derives  its 
name. 

The  whole  surface  of  the  body  was  covered  with  a  layer  of  small 
rhomboidal  scales,  composed  of  layers  of  material  ressembling  bone, 
covered  with  a  shiny  material  similar  to  the  ganoin  of  early  Actino- 
pterygii.  On  the  head  these  scales  were  enlarged  to  make  a  definite 
pattern  of  dermal  bones,  numerous  at  first  but  fewer  in  the  later  forms. 
The  pattern  of  the  bones  has  no  close  similarity  to  that  of  later  fishes. 
The  reduced  bones  of  the  later  acanthodians  are  related  to  the  lateral 
line  canals,  which  have  an  arrangement  similar  to  that  in  other  fishes, 
but  run  between  and  not  through  the  scales  and  bones  of  the  head. 
The  teeth  are  formed  as  a  series  of  modified  scales.  The  skull  is  partly 
ossified — important  evidence  that  the  boneless  condition  of  elasmo- 
branchs was  not  typical  of  all  early  gnathostomes. 

The  jaws  of  acanthodians  were  attached  by  their  own  processes  to 
the  skull  (autodiastyly)  and  are  remarkable  in  that  four  separate 
ossifications  take  place  in  them  (two  in  the  upper  and  two  in  the  lower 


1 88  EVOLUTION  OF  ELASMOBRANCHS  vi.  9 

jaw),  making  a  series  of  elements  similar  to  that  found  in  the  typical 
branchial  arches.  The  hyoid  was  an  unmodified  branchial  arch.  At 
first  the  mandibular,  hyoid,  and  each  of  the  branchial  arches  were  pro- 
vided with  small  flap-like  opercula,  but  in  later  forms  the  mandibular 
operculum  became  especially  developed  and  covered  all  the  gills. 

These  animals  might  well  represent  the  ancestors  of  many  if  not  all 
other  groups  of  gnathostomes.  They  have  not  the  peculiar  features 
that  we  characterize  as  shark-like,  and  though  they  may  well  have 
been  carnivorous  they  are  not  very  highly  specialized  for  that  mode  of 
life.  Whether  or  not  the  known  acanthodians  represent  the  actual 
ancestors  of  the  other  gnasthostome  groups,  it  is  clear  that  knowledge 
of  their  anatomy  forces  us  to  discard  two  conclusions  which  have 
often  been  accepted  in  the  past,  namely,  that  lack  of  bone  and  an 
amphistylic  jaw  support  are  primitive  gnathostome  features.  Here 
already  in  the  Silurian  we  find  animals  that  possessed  both  endo- 
chondral bone  and  scales  composed  of  bony  substance.  Moreover, 
some  of  them  have  no  trace  of  denticles  and  we  must  therefore  regard 
with  suspicion  any  theory  that  considers  the  placoid  scale  as  the 
original  type  of  all  scales.  It  is  at  least  as  likely  that  scales  composed  of 
simple  layers  of  bone  in  the  dermis  were  the  ancestral  type  and  that 
placoid  forms  with  a  pulp  cavity  were  a  later  specialization. 

Several  other  types  of  placoderm  fish  are  known,  mostly  from  the 
Devonian  strata.  The  Arthrodira,  Macropetalichthyida,  and  Anti- 
archi  (Fig.  in)  were  mostly  heavily  armoured  fishes  with  dermal 
bones  on  the  head  and  often  a  large  shield  over  the  body.  There  was 
usually  a  heterocercal  tail  and  a  covering  of  scales.  The  earlier  fishes 
were  mostly  from  fresh  water,  the  later  from  the  sea.  Many  were 
rather  flattened,  probably  bottom-living  and  invertebrate-eating 
forms.  The  bony  plates  on  the  head  were  often  arranged  in  charac- 
teristic patterns,  none  of  which,  however,  shows  close  similarity  to 
the  pattern  of  bones  on  the  head  of  bony  fishes  or  tetrapods.  Lateral 
line  canals  of  typical  arrangement  were  present  and  the  'bones'  follow 
these  to  some  extent. 

*Gemundina  was  a  flattened  animal,  superficially  similar  to  a  skate, 
from  marine  Lower  Devonian  deposits.  The  skin  was  covered  with 
denticles,  but  under  these  were  large  plates,  apparently  of  bone.  This 
fish  is  placed  in  a  special  order  Stegoselachii  and  its  affinities  are 
unknown,  but  it  shows  again  that  the  tendency  to  develop  a  flattened 
form  has  been  present  from  the  earliest  appearance  of  fishes.  *Palaeo- 
spondylus  from  the  Devonian  is  another  isolated  form,  in  the  past  often 
classed  with  the  cyclostomes.  Moy-Thomas  showed,  however,  that 


vi.  9  PLACODERMS  189 

jaws  were  present  and  that  probably  the  hyomandibula  was  not  sus- 
pensory. He  therefore  classed  the  fish  with  the  placoderms,  in  spite 
of  the  absence  of  any  dermal  skeleton.  So  far  as  can  be  discovered, 
all  these  placoderm  fishes  except  the  acanthodians  were  specialized 
types  and  have  not  left  any  later  descendants.  Indeed  it  may  well  be 
that  they  have  been  preserved  only  because  of  the  great  extent  of  their 
armour;  less  heavily  protected  relatives  may  have  existed  but  have 
not  survived  as  fossils.  The  remains  that  are  known  are  sufficient  to 
establish  the  fact  that  there  were,  in  the  Devonian  period,  numerous 
types  of  fish  possessing  a  bony  skeleton. 


VII 

THE  MASTERY  OF  THE  WATER.  BONY  FISHES 

1 .  Introduction :  the  success  of  the  bony  fishes 

The  acanthodians  and  some  other  of  the  late  Silurian  and  Devonian 
gnathostome  fishes  possessed  bony  skeletons;  from  these,  or  some 
placoderm  animals  like  them,  may  have  been  derived  not  only  the 
elasmobranchs  but  also  the  bony  fishes  and  the  lung-fishes,  which 
gave  rise  to  the  land  animals.  These  presumed  descendants  of  the 
placoderms  can  be  divided  into  three  groups :  first  the  elasmobranchs, 
secondly,  the  crossopterygians,  the  lobed-fin  or  lung-fishes,  including 
the  Devonian  forms  that  led  to  the  amphibia,  and  thirdly,  the  actino- 
pterygian  or  rayed-fin  fishes,  culminating  in  the  modern  bony  fishes. 
In  Devonian  times  the  Crossopterygii  and  Actinopterygii  were  very 
alike  and  both,  like  the  placoderms,  contained  bone.  The  term  bony 
fishes  or  Osteichthyes  is  often  applied  to  these  two  groups  together, 
since  they  have  some  features  in  common  and  distinct  from  the 
elasmobranchs. 

The  great  group  of  Actinopterygii,  which,  for  all  the  importance  of 
the  elasmobranchs,  must  be  reckoned  as  the  dominant  fish  type  at  the 
present  time,  includes  most  of  our  familiar  fishes,  perch,  pike,  trout, 
herring,  and  many  other  types  of  'modern'  fish.  In  addition  there  are 
placed  here  some  surviving  relics  of  the  stages  that  have  been  passed 
before  reaching  this  condition,  such  as  the  bichir,  sturgeons,  bow-fin, 
as  well  as  related  fossil  forms. 

Many  groups  of  animals  have  been  successful  in  the  water;  Crus- 
tacea, for  instance,  are  very  numerous  and  so  are  cephalopod  molluscs 
and  echinoderms,  but  the  success  of  the  bony  fishes  surpasses  that  of 
all  others.  From  a  roach  or  perch  in  a  stream,  to  a  huge  tunny  or  a  vast 
shoal  of  herrings  in  the  sea,  they  all  have  the  marks  of  mastery  of  the 
water.  They  can  stay  almost  still,  as  if  suspended,  dart  suddenly  at 
their  prey  or  away  from  danger.  They  can  avoid  their  enemies  by 
quick  and  subtle  changes  of  colour.  Elaborate  eyes,  ears,  and  chemical 
receptors  give  news  of  the  surrounding  world  and  complex  be- 
haviour has  been  evolved  to  meet  many  emergencies.  Reproductive 
mechanisms  may  be  very  complex,  involving  elaborate  nest-building 
and  care  of  the  young;  social  behaviour  is  shown  in  swarming  move- 
ments, which  may  be  accompanied  by  interchange  of  sounds  (p.  217). 


vii.  1-2  THE  TROUT  191 

Bony  fishes  abound  not  only  in  the  sea  but  also  in  fresh  water, 
which  has  never  been  effectively  colonized  by  cephalopods  or  elasmo- 
branchs.  They  can  exist  under  all  sorts  of  unfavourable  or  foul- 
water  conditions  and  a  considerable  number  of  them  breathe  air  and 
live  for  a  time  on  land.  Perhaps  the  majority  are  carnivorous,  but 
others  feed  on  every  type  of  food,  from  plankton  to  seaweeds. 

To  whatever  feature  of  fish  life  we  turn  we  find  that  the  bony  fishes 
excel  in  it  in  several  different  ways  in  different  species.  It  is  small 
wonder  that  with  all  these  advantages  they  are  excessively  numerous. 
There  are  some  3,000  species  of  living  elasmobranchs,  but  more  than 
20,000  species  of  bony  fish  have  been  described. 

The  number  of  individuals  of  some  of  the  species  must  be  really 
astronomical.  For  instance,  at  least  3,000  million  herrings  are  caught 
in  the  Atlantic  Ocean  each  year,  so  that  the  whole  population  there 
can  hardly  be  less  than  a  million  million.  Again,  it  is  estimated  that  a 
thousand  million  blue-fish  collect  every  summer  off  the  Atlantic  coast 
of  the  United  States  and,  being  very  voracious  carnivores,  they  con- 
sume at  least  a  thousand  million  million  of  other  fishes  during  the 
season  of  four  months.  This  gives  some  idea  of  the  tremendous 
productivity  of  the  sea,  and  of  the  way  the  bony  fishes  have  made 
use  of  it.  Needless  to  say,  man  has  also  made  considerable  use  of  the 
bony  fishes,  which  indeed  provide,  with  the  elasmobranchs,  a  not 
inconsiderable  portion  of  the  total  of  human  food. 

2.  The  trout 

Salmo  trutta,  the  brown  trout,  may  be  taken  as  an  example  of  a  bony 
fish;  we  shall  also  refer  at  intervals  to  conditions  in  other  common 
freshwater  fish  such  as  the  dace,  Leuciscus,  and  perch  (Perca  fluvi- 
atilis).  There  is  considerable  confusion  about  the  various  types  of 
trout  and  their  close  relatives  the  salmon.  The  brown  trout  is  abundant 
in  rivers  and  streams  throughout  Europe  and  is  commonly  about 
20  cm  long  at  maturity,  though  it  may  grow  larger.  It  is  grey  above 
and  yellowish  below,  with  a  number  of  dark  spots  scattered  down 
the  sides  of  the  body  (Fig.  116). 

The  body  form  is  typical  of  that  of  teleostean  fishes  in  being  short, 
narrow  in  the  lateral  plane  but  deep  dorso-ventrally,  in  fact  more  ob- 
viously streamlined  than  the  shape  of  elasmobranchs.  The  movements 
of  a  trout  do  not  at  first  sight  obviously  involve  the  bending  of  the  body 
into  an  S;  nevertheless,  the  method  of  swimming  is  essentially  by  the 
propagation  of  waves  along  the  body  by  the  serial  contraction  of  the 
longitudinally  directed  fibres  of  the  myotomes  (p.  133). 


192 


BONY  FISHES 


VII.   2- 


The  tail  differs  from  that  of  elasmobranchs  in  being  outwardly 
symmetrical,  though  internally  there  are  still  traces  of  the  upturned 
tip  of  the  vertebral  column  (Fig.  118).  Besides  the  typical  caudal 
'fish-tail',  supported  by  bony  rays,  there  are  two  dorsal  fins  and  a 
ventral  fin,  but  the  hinder  dorsal  fin  differs  from  the  others  in  having 
no  rays  to  support  it  and  is  called  an  adipose  fin,  because  of  its  flabby 
structure.  The  paired  fins  are  rather  small  and  it  is  from  their  struc- 
ture that  the  whole  group  derives  the  name  Actinopterygii  or  rayed-fin 
fishes.  There  is  no  lobe  projecting  from  the  body  and  containing 


Fig.  i  i 6.  Male  and  female  brown  trout  (Salmo  trutta)  spawning.  The  male  is  quivering — a 

short  sequence  of  rapid  shudders  of  whole  body  which  excites  the  female. 

(After  J.  W.  Jones,  The  Salmon.) 

basal  fin  supports,  as  there  is  in  the  fin  of  lung-fishes.  All  the  basal 
apparatus  of  the  fin  is  contained  within  the  body  wall  and  only  the  fin 
rays  project  outwards,  as  a  fan.  The  pelvic  fin  of  bony  fishes  often 
lies  relatively  far  forward;  in  the  trout,  however,  it  is  unusually  far 
back,  just  in  front  of  the  anus;  in  other  types  it  may  be  level  with  the 
pectoral  fin,  or  even  anterior  to  it  (Fig.  118).  The  significance  of  the 
shape  of  the  body  and  fins  in  swimming  will  be  discussed  later  (p.  244). 
The  skin  consists  of  a  thin  epidermis  and  thicker  dermis,  the  former 
has  stratified  squamous  layers  but  contains  no  keratin  (Burgess,  1958). 
It  contains  mucous  glands.  The  mucus  of  some  eels  and  other  fishes 
has  remarkable  powers  of  precipitating  mud  from  turbid  water.  The 
mesodermal  dermis  provides  an  elaborate  web  of  connective  tissue 
fibres.  It  also  contains  smooth  muscle,  nerves,  chromatophores,  and 
scales.  The  latter  are  thin  overlapping  bony  plates,  covered  by  skin, 
that  is  to  say,  they  do  not  'cut  the  gum'  as  do  placoid  denticles.  The 
exposed  part  of  each  scale  bears  the  pigment  cells,  which  control  the 
colour  of  the  animal,  in  a  manner  presently  to  be  described.  The  bone 
of  the  scales  is  absorbed  at  intervals  by  scleroclasts,  making  a  series 
of  rings,  which,  like  the  growth-rings  on  a  tree,  are  due  to  the  fact 
that  growth  is  not  constant  but  occurs  fast  in  the  spring  and  summer 


VII.  3 


FISH  SCALES 


193 


and  hardly  at  all  in  the  winter.  The  age  of  the  fish  can  therefore  be 
determined  from  these  rings  (Fig.  117),  or  from  the  similar  markings 
on  the  ear  stones  (p.  216).  While  an  adult  salmon  is  in  fresh  water  no 
growth  occurs,  leaving  a  spawning  mark  on  the  scale. 

The  head  of  the  trout  shows  some  of  the  most  specialized  and  typical 
teleostean  features  (Fig.  119).  There  are  two  nostrils  on  each  side,  but 
no  external  sign  of  ears.  The  mouth  is  very  large  and  its  edges  are 
supported  by  movable  bones,  to  be  described  below.  The  maxillary 
and  mandibular  valves  are  folds 
of  the  buccal  mucosa,  serving  to 
prevent  the  exit  of  water  during 
respiration.  The  tongue,  as  in 
Selachians,  has  no  muscles,  but 
may  carry  teeth  and  taste-buds. 
Behind  the  edge  of  the  jaw  is  the 
operculum,  a  flap  covering  the 
gills  and  also  supported  by  bony 
plates.  In  connexion  with  these 
special  developments  of  jaws  and 
gills  the  skull  has  become  much 
modified  and  has  developed  com- 
plex and  characteristic  features 
(Fig.  118). 


Fig.  117.  Spawning  mark  (sp.  ?nk.),  the 
result  of  erosion  or  absorption  of  the  scale 
margin  due  to  a  calcium  deficiency  fasting 
period.  (After  J.  W.  Jones,  The  Salmon.) 


1st  river  winter.  2.  2nd  river  winter. 
3.  1  st  sea  winter. 


3.  The  skull  of  bony  fishes 

The  main  basis  for  the  skull 
is  a  chondrocranium  and  set  of 

branchial  arches,  exactly  comparable  to  those  of  the  elasmobranchs. 
In  the  early  stages  of  development  there  is  a  set  of  cartilaginous  boxes 
around  the  nasal  and  auditory  capsules,  brain  and  eyes,  and  a  series 
of  cartilaginous  rods  in  the  gill  arches.  Bones  are  then  added  in  two 
ways:  either  (i)  as  cartilage  bones  (endochondral  bones)  by  the  re- 
placement of  some  parts  of  the  original  chondrocranium,  or  (2)  as 
membrane  or  dermal  bones,  laid  down  as  more  superficial  coverings 
and  considered  to  be  derived  from  a  layer  of  scales  in  the  skin.  This 
outer  position  of  the  bones  can  be  clearly  seen  in  many  cases  by  the 
readiness  with  which  the  membrane  bones  can  be  pulled  away  from 
the  rest  of  the  skull. 

The  skull  bones  are  arranged  in  a  regular  pattern,  whose  broad 
outlines  can  be  seen  in  all  fishes  and  in  their  tetrapod  descendants. 
However,  there  are  many  confusing  variations  and  the  naming  of 


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vii.  3  SKULL  OF  TELEOSTS  195 

bones  has  given  much  controversy.  No  generally  acceptable  theory 
has  yet  appeared,  perhaps  because  we  know  little  of  the  factors  that 
cause  separate  bony  elements  to  develop.  There  is  some  evidence  of 
relations  between  bones  and  teeth  and  bones  and  lateral  line  organs 
and  the  pattern  of  the  latter  may  play  a  large  part  in  determining  the 
plan  of  the  skull  (p.  325).  Provisionally  we  may  recognize  four  classes 
of  dermal  bones  (1)  canal  bones,  (2)  tooth  bones,  (3)  'ordinary'  bones, 
whose  determination  is  unknown,  (4)  extra  bones,  filling  special  areas 
(Wormian  bones). 

The  arrangement  of  the  numerous  bones  is  made  less  difficult  to 
understand  and  remember  if  they  are  considered  in  the  following 
order.  First  the  endochondral  ossifications  in  the  original  neuro- 
cranium,  then  the  dermal  bones  that  cover  this  above  and  below;  next 
the  endochondral  bones  formed  within  the  original  cartilaginous  jaws, 
then  the  dermal  bones  that  cover  the  edges  of  the  jaws,  and  finally  the 
ossifications  in  the  branchial  arches  and  pectoral  girdle,  which  latter 
is  in  bony  fishes  attached  to  the  skull. 

The  endochondral  ossifications  may  be  considered  by  beginning  at 
the  hind  end  of  the  skull:  here  the  floor  ossifies  as  the  basioccipital, 
the  sides  as  the  exoccipitals,  and  the  roof,  over  the  spinal  cord,  as  the 
supra-occipital  bone;  these  posterior  bones  are  not  well  marked  off 
from  each  other  in  the  adult  skull.  In  the  auditory  capsule  are  five 
separate  otic  bones,  of  these  the  epiotic  and  pterotic  can  be  seen 
externally  (Fig.  118). 

The  floor  in  front  of  the  basioccipital  is  occupied  by  a  basisphenoid 
bone  and  the  walls  above  this  by  alisphenoids.  The  eyes  nearly  meet  in 
the  midline  and  the  orbits  are  here  separated  only  by  a  thin  orbito- 
sphenoid.  The  only  more  anterior  part  of  the  chondrocranium  to 
ossify  is  the  region  between  the  nasal  capsule  and  the  orbit,  forming 
the  ectethmoid. 

The  dermal  bones  that  cover  this  partly  ossified  neurocranium  may 
be  identified  as  on  top  and  in  front  a  pair  of  frontals  and  a  median 
supraethmoid,  behind  which  are  large  paired  parietals  and  small 
paired  post-parietals.  These  names  have  been  inferred  from  study  of 
crossopterygians  and  early  amphibians  (p.  325),  which  showed  that 
the  homologies  earlier  accepted  were  wrong.  Fig.  118  carries  the  old 
nomenclature  in  which  the  large  paired  bones  were  called  frontals. 
Around  the  eyes  is  a  ring  of  circum-orbitals,  and  on  the  floor  of  the 
skull  two  median  bones,  the  parasphenoid  and  vomer. 

The  jaw  bones  are  numerous,  including  both  endochondral  and 
dermal  elements,  and  the  relation  of  the  method  of  support  to  that 


196  BONY  FISHES  vn.  3- 

found  in  other  animals  is  not  clear.  In  the  embryo  palato-pterygo- 
quadrate  bars  and  Meckel's  cartilages  are  seen.  The  upper  jaw  bears 
inward  projections,  which  extend  towards  the  chondro-cranium  and 
probably  represent  the  traces  of  an  autostylic  means  of  support  (see 
p.  187).  But  the  effective  support  in  the  adult  is  achieved  by  the  ossi- 
fied hyomandibular  cartilage.  The  palato-pterygo-quadrate  bar  ossifies 
in  several  parts  and  palatine,  pterygoid,  mesopterygoid,  metaptery- 
goid,  and  quadrate  bones  appear,  some  of  them  partly  formed  in  mem- 
brane. The  only  part  of  Meckel's  cartilage  to  ossify  is  the  articular 
bone,  at  the  hind  end.  The  actual  edges  of  the  jaws  are  supported  by 
membrane  bones,  the  premaxilla,  maxilla,  and  jugal,  covering  the 
upper  jaw.  The  dentary  covers  most  of  the  lower  jaw,  except  for  a 
small  bone,  the  angular,  that  lies  on  the  inner  side  at  the  posterior  end. 

The  hyomandibular  bone  runs  from  an  articulation  with  the  otic 
capsule  to  the  upper  end  of  the  quadrate.  The  symplectic  is  a  small 
separate  ossification  at  the  lower  end  of  the  hyomandibula.  The  rest 
of  the  hyoid  arch  is  present  as  epi-,  cerato-,  and  hypohyals,  which 
support  a  large  toothed  tongue.  Bony  fishes  only  rarely  possess  an 
open  spiracle  and  immediately  behind  the  hyoid  are  attached  the 
bones  supporting  the  operculum  that  covers  the  gills.  The  branchial 
arches  are  formed  of  several  pieces,  as  in  elasmobranchs,  each  being 
ossified  separately. 

The  effect  of  this  complicated  set  of  bones  is  to  provide  an  efficient 
apparatus  for  the  protection  of  the  brain  and  sense-organs,  support 
of  the  jaws  and  teeth  and  of  the  respiratory  apparatus.  Teeth  are  found 
on  the  vomers,  palatines,  premaxillae,  maxillae,  dentary,  and  on  the 
tongue.  Covering  the  typical  dentine  (orthodentine)  is  a  layer  of 
harder  vitrodentine,  poor  in  organic  matter  and  perhaps  derived 
partly  from  ectodermal  ameloblasts.  The  teeth  are  usually  spikes 
pointing  in  a  backwards  direction,  used  to  prevent  the  escape  of  the 
food  and  not  usually  for  biting  or  crushing.  They  may,  however,  form 
plates  or  be  firmly  attached  to  the  bones.  Folds  of  the  mucous  mem- 
brane, supported  by  cartilage  and  carrying  gill-rakers,  are  found  in 
species  that  feed  on  small  prey. 

4.  Respiration 

Limitations  are  imposed  on  the  respiration  of  fishes  by  the  facts 
that  water  is  800  times  more  dense  than  air  and  the  dissolved  oxygen 
is  30  times  more  dilute.  The  cost  of  respiration  is  therefore  high.  There 
is  a  70  per  cent,  increase  in  metabolism  when  a  trout  increases  its 
ventilation  volume  four  times  in  water  poor  in  oxygen. 


vir.  4 


RESPIRATION 


197 


Respiration  is  produced  by  a  current  passing  in  a  single  direction, 
as  in  elasmobranchs,  namely,  in  at  the  mouth  and  out  over  the  gill 
lamellae,  but  the  mechanism  by  which  the  current  is  produced  is  some- 
what different.  The  pumping  action  is  produced  by  a  buccal  pressure 
pump  and  opercular  suction  pumps,  resulting  from  sideways  move- 


A  B 

Fig.  119.  Arrangement  of  organs  of  head  and  gills  in  A,  a  shark,  and, 

B,  a  teleostean  fish. 

gb.  gill  bar;  GC.  outer  opening  of  gill  cleft;  GF.  gill  filament;  gr.  gill-rakers;  cv.  gill  vessels; 

J,  ]'.  upper  and  lower  jaw;  M.  mouth;  N,  n'.  openings  of  nasal  chamber;  op.  operculum; 

sp.    spiracle;   ST.   septum   between   gill   filaments.    (From    Dean,   Fishes,    Living    &   Fossil, 

The  Macmillan  Co.) 

ments  of  the  operculum,  enlarging  the  branchial  cavity.  The  branchio- 
stegal  folds,  below  the  operculum,  prevent  inflow  of  water  from 
behind.  When  the  operculum  moves  inward  dorsal  and  ventral  flaps 
in  the  throat  prevent  the  exit  of  water  forwards. 

The  gill  lamellae  differ  from  those  of  elasmobranchs  in  the  great 
reduction  of  the  septum  between  the  respiratory  surfaces  (Fig.  119). 
This  has  the  effect  of  leaving  the  lamellae  as  free  flaps,  increasing  the 
surface  available  for  respiration. 

The  area  of  the  gills  varies  greatly,  being  relatively  larger  in  more 
active  species.  The  rate  of  respiration  is  controlled  by  a  medullary 
centre  but  the  most  active  rate  of  respiratory  exchange  is  only  some 
four  times  the  standard  rate  (as  against  twenty  times  in  man).  The 


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vii.  4-5  BACKBONE  OF  FISHES  199 

area  of  the  respiratory  surface  is  thus  an  important  limiting  factor  in 
the  movement  and  growth  of  fishes.  During  activity  of  a  fish  lactic 
acid  accumulates  in  the  blood  and  the  pH  falls.  The  fish  is  thus  able 
to  display  a  considerable  burst  of  activity  and  then  to  repay  the 
oxygen  debt  over  a  long  subsequent  period. 

5.  Vertebral  column  and  fins  of  bony  fishes 

The  vertebral  column  of  bony  fishes  performs  the  same  function  as 
in  other  fishes,  namely,  to  prevent  shortening  of  the  body  when  the 
longitudinal  muscles  contract.  It  has,  however,  become  very  compli- 
cated and  with  the  ribs  and  neural  and  haemal  arches  forms  an 
elaborate  system  serving  to  maintain  the  body  form  under  the  stresses 
of  fast  swimming.  Like  other  parts  of  the  skeleton  it  is  extensively 
ossified,  and  the  necessary  lateral  flexion  is  obtained  by  division  of 
the  column  into  a  series  of  sections  joined  together.  Typically  there 
is  one  such  section  (vertebra)  corresponding  to  each  segment,  but  in 
the  tail  region  of  Amia  there  are  twice  as  many  vertebrae  as  segments. 

Each  vertebra  consists  of  a  centrum,  neural  arch  and  neural  spine, 
and  in  the  tail  region,  in  addition,  haemal  arch  and  haemal  spine. 
These  parts  are  formed  partly  by  ossification  of  cartilaginous  masses, 
the  basidorsal  and  basiventral,  interdorsal  and  interventral,  such  as 
we  saw  in  elasmobranchs,  and  partly  by  extra  ossification  in  the  sclero- 
genous  tissue  around  the  notochord  and  nerve-cord  and  between  the 
muscles.  The  vertebrae  are  inter-segmental,  the  middle  of  each  lying 
opposite  the  myocomma  that  separates  two  muscle  segments. 

The  centra  are  concave  both  in  front  and  behind  (amphicoelous), 
and  in  the  hollows  between  them  are  pads  made  of  the  remains  of  the 
notochord,  an  arrangement  that  allows  the  column  to  resist  longi- 
tudinal compression  and  yet  remain  flexible;  similar  flat  or  concave 
articulations  of  the  centra  are  found  in  other  aquatic  vertebrates  from 
the  elasmobranchs  to  the  whales.  Extra  processes  on  the  front  and 
back  of  the  vertebrae  ensure  the  articulation  and  are  comparable  to  the 
zygapophyses  found  in  tetrapods.  The  ribs,  which  are  so  prominent 
in  the  backbone  of  many  fishes,  are  of  two  sorts;  pleural  ribs  between 
the  muscles  and  the  lining  of  the  abdominal  cavity,  and  more  dorsal 
intramuscular  ribs.  Both  sorts  are  attached  to  the  centrum.  The  bony 
rods  attached  above  the  neural  and  below  the  haemal  arches  are  often 
called  neural  and  haemal  spines,  though  it  is  doubtful  whether  they 
correspond  to  the  neural  spines  of  land  vertebrates.  They  form  the 
supporting  rods  or  radials  of  the  median  fins  and  are  usually  divided 
into  two  or  three  separate  bones  in  each  segment.  In  addition  to  these 


200 


BONY  FISHES 


vii.  5- 


radials  the  fins  are  also  supported  by  a  more  superficial  set  of  bony- 
rods,  the  dermal  fin  rays  (dermotrichia  or  lepidotrichia),  which  may 
be  considered  as  modified  scales  and  accordingly  lie  superficial  to  the 
radials.  These  dermal  fin  rays  are  usually  forked  at  their  tips.  They 
make  an  extra  support  for  the  fin  margin  and  to  them  are  attached  the 
muscles  that  serve  to  throw  the  fin  into  folds. 

In  the  tail  region  the  internal  skeleton  is  not  quite  symmetrical  and 
shows  signs  of  origin  from  an  animal  with  a  heterocercal  tail.  The 


<ev.msx. 


3<j-mand. 

Fig.  121.  Muscles  of  a  teleostean  fish,  mainly  based  on  Mullus. 
ad-mand.  adductor  mandibulae;  ep.  epaxonic  muscles;  h.  horizontal  myoseptum;  hy.  hypo- 
branchial  muscles;   hyp.   hypaxonic   muscles;   lev.   max.   levator  maxillae;   my.   myocomma; 
op.  operculum.  (From  Ihle.) 

notochord  turns  up  sharply  at  the  tip,  so  that  the  neural  spines  are 
very  much  shorter  than  the  haemal  spines,  known  here  as  hippural 
bones.  The  final  portion  of  the  notochord  is  often  surrounded  by  a 
single  ossification,  the  urostyle,  and  the  whole  makes  a  rigid  support 
for  the  dermotrichia  of  the  tail.  Such  a  tail  with  internal  asymmetry 
but  external  symmetry  is  said  to  be  homocercal. 

The  myotomes  are  arranged  in  a  complicated  pattern  having  the 
effect  that  contraction  of  each  affects  a  considerable  section  of  the 
body  (Fig.  121);  in  fast  swimmers  such  as  the  tunny  each  myotome 
may  overlap  as  many  as  nineteen  vertebrae.  Between  the  lateral  and 
ventral  muscle  masses  there  is  in  many  fishes  a  layer  of  red  muscle 
and  this  is  especially  well  developed  in  the  tunnies  and  bonitos. 

The  paired  fins  are  similarly  supported  by  ossified  radials,  covered 
by  dermal  fin  rays.  At  the  base  the  radials  are  connected  with  'girdles' 
lying  in  the  body  wall.  The  pectoral  girdle  (Fig.  118)  consists  of  a 
cartilaginous  endo-skeletal  portion  in  which  ossify  the  scapula,  cora- 
coid,  and  sometimes  mesocoracoid,  while  dermal  bones,  large  cleith- 
rum,  and  one  or  more  small  clavicles,  become  attached  superficially. 


vii.  8  ALIMENTARY  CANAL  201 

Above  these  a  further  series  of  dermal  bones,  the  supra-clavicle  and 
post-temporal,  attach  the  pectoral  girdle  to  the  otic  region  of  the  skull. 
The  pelvic  girdle  is  very  simple,  consisting  only  of  a  single  bone, 
the  basipterygium. 

6.  Alimentary  canal 

The  food  of  the  trout  consists  mainly  of  small  invertebrates  such  as 
Gammarus,  Cyclops,  and  other  crustaceans,  and  aquatic  insects  and 
their  larvae,  together  with  the  fry  of  other  fishes  and  perhaps  some- 
times larger  pieces  of  'meat'.  The  food  is  mostly  swallowed  whole, 
being  helped  down  the  pharynx  by  the  mucous  secretions,  but  these, 
as  in  elasmobranchs,  contain  no  enzymes.  The  entrance  to  the  stomach 
is  guarded  by  a  powerful  oesophageal  sphincter,  no  doubt  serving  to 
prevent  the  entry  of  the  water  of  the  respiratory  stream.  The  stomach 
is  divided  into  cardiac  and  pyloric  portions,  though  the  distinction  is 
less  clear  than  in  elasmobranchs.  The  duodenum  is  beset  by  a  number 
of  wide-mouthed  pyloric  caeca,  serving  to  increase  the  intestinal 
surface  (Fig.  120).  The  intestine  and  caeca  are  lined  throughout  by  a 
simple  columnar  epithelium  and  there  are  no  specialized  multicellular 
glands  such  as  the  Brunners  glands  or  crypts  of  Lieberkiihn  of  mam- 
mals. The  exocrine  pancreas  consists  of  numerous  diffuse  glands  in 
the  mesentery.  The  endocrine  portion,  however,  forms  a  compact 
mass  of  tissue.  This  is  very  rich  in  insulin  and  after  its  removal  a  fish 
shows  hyperglycemia  and  glycosuria.  The  intestine  is  relatively  longer 
than  in  elasmobranchs  and  often  coiled;  its  internal  surface  may  be 
increased  by  folds,  but  there  is  no  true  spiral  valve,  though  this  was 
present  in  the  ancestors  of  the  Teleostei  (p.  233).  There  is  no  gland 
attached  to  the  rectum. 

7.  Air-bladder 

Dorsal  to  the  gut  is  a  very  large  sac  with  shiny,  whitish  walls,  the 
air-bladder,  filled  with  oxygen.  A  narrow  pneumatic  duct  connects 
this  with  the  pharynx  in  the  more  primitive  forms.  The  origin  and 
functions  of  the  air-bladder  will  be  discussed  below  (p.  261);  it  serves 
as  a  hydrostatic  organ,  enabling  the  animal  to  remain  suspended  in 
the  water  at  any  depth. 

8.  Circulatory  system 

The  general  plan  of  the  circulation  is  similar  to  that  of  an  elasmo- 
branch  (Fig.  122),  that  is  to  say,  there  is  a  single  circuit  and  all 
the  blood  passes  through  at  least  two  sets  of  capillaries.  The  heart 


202  BONY  FISHES  vu.  8- 

contains  a  series  of  three  chambers,  sinus,  auricle,  and  ventricle,  but  the 
muscular  conus  arteriosus  is  absent,  there  being  only  a  thin-walled 
bulbus  arteriosus  at  the  base  of  the  ventral  aorta.  The  walls  of  the 
bulbus  are  elastic  but  not  muscular,  and  study  of  its  action  by  means 
of  X-rays  shows  that  it  is  dilated  by  the  ventricular  beat  and  then 
contracts,  thus  maintaining  the  pressure  against  the  capillaries  of  the 
gills.  The  ventral  aorta  is  short,  but  the  arrangement  of  the  afferent 
and  efferent  branchial  vessels  is  essentially  as  in  elasmobranchs. 

The  blood-pressure  in  the  ventral  aorta  is  less  than  40  mm  Hg  in 
most  fishes  at  rest,  and  in  the  dorsal  aorta  about  half  this.  The  venous 
pressures  are  around  zero,  the  pericardium  being  fibrous  but  not 
rigid  as  it  is  in  elasmobranchs  (p.  160).  There  is  no  communication 
between  the  pericardial  and  peritoneal  chambers.  There  is  a  vagal 
cardiac  depressor  nerve,  but  no  sympathetic  nerve  to  the  heart. 

There  is  a  well-developed  lymphatic  system  beneath  the  skin  and 
in  the  muscles  and  viscera.  Lymphoid  tissue  is  abundant  in  various 
organs  but  there  are  no  lymph-nodes  along  the  vessels.  There  is  a 
large  spleen  concerned  with  haemopoiesis,  which  also  proceeds  in  the 
kidneys.  The  red  cells  are  smaller  in  bony  fishes  (8-10  ix)  than  in 
elasmobranchs  (up  to  20  /z).  A  continuous  series  of  white  cells  is 
present  and  acidic  and  basic  granules  may  occur  in  the  same  cell. 

9.  Urinogenital  system  and  osmoregulation 

The  kidneys  are  mesonephric  in  the  adult  and  consist  of  an  elon- 
gated brown  mass  above  the  air-bladder.  The  ducts  of  the  two  kidneys 
join  posteriorly  and  are  swollen  to  form  a  bladder  which,  being  meso- 
dermal, must  be  distinguished  from  the  endodermal  cloacal  bladder 
of  tetrapods.  The  urinary  duct  opens  separately  behind  the  anus, 
there  being  no  common  cloaca. 

Nitrogenous  elimination  is  a  function  mainly  of  the  gills,  which 
excrete  as  ammonia  and  urea  more  than  six  times  as  much  nitrogen  as 
the  kidneys.  The  latter  excrete  creatine,  uric  acid,  and  the  weak  base 
trimethylamine  oxide,  which  is  present  in  large  amounts  in  the  blood 
of  marine  teleosts. 

One  of  the  most  striking  features  of  the  life  of  bony  fishes  is  that 
they  occur  both  in  fresh  water  and  the  sea,  and  many,  such  as  the 
trout  itself,  can  move  from  one  to  the  other.  It  is  supposed  by  some 
that  the  earliest  gnathostomes  were  freshwater  animals  (p.  187),  and 
the  bony  fishes  might  be  said  to  show  evidence  of  this  in  that  the 
concentration  of  salt  in  their  blood  is  always  less  than  in  the  sea,  in  the 
neighbourhood  of  1-4  per  cent.  NaCl  against  3-5  per  cent,  outside. 


vii.  9  BLOOD  OF  TELEOSTS  203 

In  fishes  in  fresh  water  the  blood  is  more  dilute,  about  o-6  per  cent. 
NaCl,  but  is,  of  course,  more  concentrated  than  the  surrounding 
medium,  which  contains  only  traces  of  inorganic  ions.  Freshwater 
fishes  are  able  to  take  up  salts  from  the  water  through  the  gill  surfaces. 
The  kidney  apparatus,  with  its  filtration  system  of  glomeruli  and 
tubules  for  salt  reabsorption,  was  probably  developed  for  life  in  fresh 
water  and  still  serves  in  this  way  in  the  freshwater  forms.  Various 
special  devices  are  adopted  in  fresh  water  for  minimizing  the  tendency 


Fig.  122.  Diagram  of  the  branchial  circulation  of  a  teleostean  fish. 
ab.  artery  to  air-bladder;  a/3-6,  four  afferent  vessels  from  ventral  aorta;  ca.  carotid  artery; 
cc.  circulus  cephalicus;  cl.  coeliac  artery;  d.  ductus  Cuvieri;  da.  dorsal  aorta;  ef3.  efferent 
vessel  of  first  branchial  arch;  ep.  epibranchial  artery;  ha.  hyoidean  artery  (afferent  vessel  of 
pseudobranch);  hp.  hepatic  vein;  ht.  heart;  mis.  mesenteric  artery;  oa.  ophthalmic  artery 
(efferent  vessel  of  pseudobranch);  ps.  pseudobranch  (hyoidean  gill,  possibly  with  spiracular 
gill);  s.  position  of  spiracle  (closed);  va.  ventral  aorta;  I-V.  five  branchial  slits.  (From 
Goodrich,  Vertebrata,  A.  &  C.  Black,  Ltd.,  after  Parker.) 

to  gain  water  and  lose  salt.  The  skin  is  little  vascularized  and  probably 
makes  an  almost  waterproof  layer.  The  production  of  mucus  assists 
in  this  waterproofing,  and  abundant  mucus  is  secreted  when  an  eel  is 
transferred  from  salt  to  fresh  water:  the  full  change  cannot  be  made 
suddenly  without  killing  the  fish. 

In  marine  teleosts  the  problem  is  the  opposite  one  of  keeping  water 
in,  or  keeping  out  salt.  The  usual  kidney  mechanism  is  clearly  ill 
suited  for  this  and  it  is  found  that  the  glomeruli  are  few,  or  often 
completely  absent  from  the  kidneys.  This  no  doubt  reduces  the  loss 
of  water,  but  is  not  enough  by  itself  to  solve  the  problem,  which  is 
met  by  taking  in  water  and  salts  and  excreting  the  salts.  For  this 
purpose  special  chloride-secreting  cells  are  present  in  the  gills  and  it 
has  been  shown  that  the  amount  of  oxygen  they  use,  and  hence  the 
work  they  do  in  diluting  the  blood,  is  proportional  to  the  difference  of 
concentration  between  the  inside  and  the  outside.  A  marine  fish  is 
able  to  drink  and  absorb  sea  water  in  spite  of  the  fact  that  this  is  more 


204 


BONY  FISHES 


vir.  9- 


concentrated  than  its  blood.  The  chloride-secreting  cells  dispose  of 
the  excess  salts.  It  remains  to  explain  the  means  by  which  a  solution 
passes  against  the  osmotic  gradient  from  the  cavity  of  the  gut  to  the 
blood;  the  membranes  here  must  have  some  special  properties  of 
which  we  are  ignorant.  Sodium  and  chloride  enter  with  the  water  but 
magnesium  is  excluded  and  may  be  precipitated  in  the  intestine. 

The  genital  system  is  nearly  completely  separated  from  the  excre- 
tory in  both  sexes.  The  testes  (soft  roes)  are  a  large  pair  of  sacs  opening 

into  the  base  of  the  urinary 
ducts.  The  ovaries  (hard  roes) 
are  also  elongated  in  the  trout 
and  the  eggs  are  shed  free  into 
the  coelom  (Fig.  123)  and 
passed  to  the  exterior  by 
abdominal  pores.  This  condi- 
tion is  unusual  among  teleosts, 
in  most  the  ovaries  are  closed 
sacs,  continuous  with  the  ovi- 
ducts. 

Fertilization  is  external  and 
the  eggs  of  the  trout  are  shed 
in  small  pits  or  depressions  in 
the  sand;  being  sticky,  they 
become  attached  to  small 
stones.  The  eggs  are  very 
yolky  and  cleavage  is  therefore  only  partial,  forming  a  cap  of  cells, 
the  blastoderm,  which  eventually  differentiates  into  the  embryo. 
After  hatching,  the  young  fish  may  still  carry  the  yolk  sac  and 
obtain  food  from  it  for  some  time,  while  beginning  to  eat  the  small 
crustaceans  and  other  animals  that  are  its  first  food. 

10.  Races  of  trout  and  salmon  and  their  breeding  habits 

There  is  considerable  confusion  about  the  various  races  of  trout 
and  their  allies  the  salmon.  In  both  trout  and  salmon  the  adult 
originally  spent  the  great  part  of  its  life  in  the  sea  but  returned  to  the 
rivers  to  breed.  Trout  and  salmon  that  do  this  are  still  abundant  on 
the  West  Atlantic  coasts  and  ascend  all  suitable  rivers  to  breed,  the 
process  being  known  as  the  'run'.  But  the  trout  has  produced  many 
races  of  purely  fluviatile  animals,  living  either  in  lakes  (where  they  often 
become  very  large)  or  rivers,  and  never  returning  to  the  sea  to  breed. 
These  freshwater  races  differ  in  small  points  from  each  other  and  are 


Fig.    123.   Ovaries   and  kidneys  of  A,   typical 

teleostean  fish,  B,  trout  and  some  other  fishes 

where    the    eggs    are    shed    into    the    coelom. 

(From  Norman,  after  Rey.) 


VII.    IO 


LIFE  CYCLE  OF  SALMO 


205 


given  various  common  names  (phinock,  Severn,  Loch  Leven  trout, 
brook  trout,  &c).  There  can  be  no  doubt  that  interesting  genetic 
differences  between  these  forms  exist,  but  they  have  not  yet  been 
fully  studied.  The  salmon  are  much  less  prone  to  form  purely  fresh- 
water races,  though  such  are  known. 

During  the  breeding-season  characteristic  changes  take  place  in  the 
fishes  and  differences  between  the  sexes  appear.  In  the  salmon  the 
jaws  become  long,  thin,  and  hooked,  especially  in  the  male.  The 
animals  make  pairs  and  the  males  fight  with  others  that  approach  the 
female.  As  the  gonads  ripen,  the  other 
parts  of  the  fish,  which  were  well  supplied 
with  fat  at  the  beginning  of  the  run, 
become  progressively  more  watery. 
Finally,  spawning  takes  place,  the  female 
laying  the  eggs  in  a  shallow  trough  (redd), 
which  she  has  'cut'  in  the  gravel  by  move- 
ments of  her  tail,  while  the  male  sheds 
sperms  over  them.  She  then  covers  the 
eggs  with  gravel  by  further  cutting  move- 
ments. The  young  male  salmon  (parr), 
which  have  not  yet  been  to  the  sea,  may 
become  sexually  mature.  They  accompany 
the  fully  grown  fish,  hanging  around  the 
cloacal  region  and  shedding  their  sperms 
at  the  same  time  as  the  large  male.  It  is  possible  that  this  develop- 
ment of  a  kind  of  third  sex  serves  to  increase  the  variability  of  the 
population.  The  spent  parr  eat  some  of  the  eggs  and  they  then  proceed 
to  grow,  migrate  to  the  sea,  and  return  later. 

Male  trout  will  follow  a  spawning  salmon  and  fertilize  her  eggs  if 
her  own  male  is  not  looking.  Hybrids  formed  in  this  way  can  develop, 
but  are  said  to  be  less  fertile  than  the  normal  types;  indeed,  the  males 
are  wholly  sterile. 

After  fertilization  the  salmon  are  very  exhausted  (known  as  kelts) ; 
the  males  seldom  return  to  the  sea.  The  females,  however,  may  recover 
and  after  a  period  in  the  sea  return  to  breed  again,  and  this  process 
may  be  repeated  several  times. 

Very  young  trout  or  salmon  are  known  as  alevins  or  fry  and  remain 
mostly  among  the  stones  (Fig.  124).  When  they  emerge  they  are  called 
parr  and  have  a  number  of  characteristic  parr-marks  along  their  sides. 
After  two  to  four  years  spent  as  parr  in  fresh  water  salmon  acquire  a 
silver  colour  and  pass  to  the  sea  as  smolts.  Young  salmon  returning  for 


Fig.   124.    Three   stages   in  the 

development     of     the    salmon. 

I  and  II   are  alevins;    III,  parr. 

(From  Norman.) 


206 


BONY  FISHES 


the  first  time  to  breed  are  called  maidens.  If  they  have  spent  only  one 
and  a  half  years  in  the  sea  they  are  called  grilse  and  may  then  return 
to  the  sea  as  kelts.  Others  ascend  for  the  first  time  after  three  years 
or  more  at  sea. 

It  is  well  established  that  salmon  nearly  always  return  to  breed  in 
the  river  in  which  they  were  born,  and  it  is  certain  that  they  may 
journey  for  considerable  distances  in  the  sea.  The  mechanisms  by 
which  these  migrations  are  initiated  and  guided  are  only  partly  known. 


Fig.  125.  Pituitary  gland  of  the  primitive  teleost  Elops,  showing  the  persistent 
Rathke's  pouch  in  the  form  of  a  hollow  bucco-hypophysial  canal,  piercing  the 

parasphenoid  bone. 

ah.  adenohypophysis ;  b.h.c.  bucco-hypophysial  canal;  h.v.  blood-vessel;  c.  continuation  with 

pharynx;  i.  infundibulum;  n.h.  neurohypophysis;/)^,  parasphenoid. 

(After  Olsson.) 

They  probably  involve  endocrine  changes,  for  example  the  thyroid 
is  very  active  in  the  smolt  as  they  begin  to  migrate.  The  return  to  the 
home  river  may  be  a  result  of  olfactory  conditioning  (see  p.  221). 

11.  Endocrine  glands  of  bony  fishes 

The  pituitary  gland  occupies  the  same  central  part  in  the  endocrine 
signalling  system  that  it  has  in  mammals.  Neural  and  glandular 
regions  are  present  and  the  adenohypophysis  has  three  parts,  the 
two  more  posterior  corresponding  to  the  mammalian  intermediate  and 
anterior  lobes.  The  most  anterior  glandular  region  may  be  comparable 
to  the  pars  tuberalis.  Experiments  by  removal  and  injection  have 
shown  that  the  middle  portion  produces  hormones  that  stimulate 
growth,  the  gonads,  the  thyroid,  adrenal,  and  probably  the  pancreas. 
The   posterior   lobe  produces   a   melanophore-dispersing   hormone 


ENDOCRINE  GLANDS 


207 


(p.  260)  and  there  may  be  a  melanophore-concentrating  one  in  the 
anterior  lobe.  Oxytocin  and  vasopressin  are  present  but  there  is  no 
evidence  that  excretion  is  controlled  by  the  pituitary. 

The  thyroid  tissue  is  not  aggregated  into  a  compact  gland  but  forms 
scattered  masses  along  the  ventral  aorta.  Its  hormones  appear  to  be 


ns.a. 


Fig.  126.  Urohypophysis  of  A,  eel;  b,  loach  (Misgurnus);  c,  the  same  in  a  loach 

after  sectioning  the  spinal  cord  and  injecting  hypertonic  saline. 

b.  blood-vessels;  ep.  ependyma;//.  filum  terminate;  /;/.  lumps  of  secretion  (? 'Herring  bodies'); 

tie.  nerve  endings;  ns.a.  neurosecretory  axon;  ns.c.  neurosecretory  cells;  s.d.  storage  depot  of 

neurosecretion.  (After  F.nami,  N.,  in  Symposium  on  Comparative  Endocrinology.    Wiley,  New 

York.) 

identical  with  those  of  mammals,  including  mono-  and  di-iodotyrosine 
and  thyroxin.  Thyroid  follicles  are  often  found  in  the  kidneys,  heart, 
eye,  and  elsewhere  in  the  body  of  fishes,  especially  those  deprived  of 
iodine. 

The  suprarenal  and  interrenal  tissues  are  partly  associated  in  masses 
around  the  thickened  walls  of  the  posterior  cardinal  veins.  Because  of 
the  difficulty  of  isolating  these  tissues  there  is  little  information  as  to 
their  function.  The  corpuscles  of  Stannius  are  groups  of  gland  cells 
dorsal  to  the  kidnevs,  they  have  been  held  to  be  related  to  the  adrenals, 
but  their  nature  is  still  uncertain. 


208 


BONY  FISHES 


The  ultimobranchial  gland  is  a  mass  of  cells  developed  from  the 
last  branchial  pouch  and  perhaps  related  to  the  parathyroids. 

The  hormone  rennin,  which  raises  the  blood  pressure,  is  said  to  be 
present  in  freshwater  teleosts,  with  their  high  glomerular  filtration, 
but  not  in  marine  ones. 

The  gonads  produce  steroid  hormones  as  in  elasmobranchs  (p. 
167).  The  secondary  sex  characters  depend  upon  their  presence,  thus 


ns.  c. 


n.e 


Fig.   127.  Comparison  of  pattern  of  organization  of  the  caudal  neurosecretory 
system  (b)  with  the  hypothalamo-hypophysial  system  (a). 

ah.  adenohypophysis;  b.v.  blood-vessels;  c.c.  central  canal; /.i.  filum  terminale;  h.  'Herring 
bodies',  neurosecretory  products;  n.  neurohypophysis;  n.e.  nerve  endings;  ns.c.  neurosecre- 
tory cells;  o.c.  optic  chiasma;  p.  pituicytes;  p.v.  hypophysial  portal  vessels;  r.f.  Reissner's  fibre; 
11.  urohypophysis;  v.  vtntricle.  (After  Enami,  N.,  in  Symposium  on  Comparative  Endocrinology. 

Wiley,  New  York.) 


the  gonopodium  of  the  male  of  viviparous  fishes  (p.  267)  is  developed 
if  sex  hormone  is  added  to  the  water. 

At  the  hind  end  of  the  spinal  cord  of  fishes  is  a  small  lump  consisting 
of  masses  of  secretion  produced  by  neurosecretory  cells  of  the  spinal 
cord  and  hence  called  the  urohypophysis  (Figs.  126  and  127).  In 
function  it  appears  to  be  connected  with  salt  regulation;  injection  of 
hypertonic  NaCl  produces  hypersecretion,  the  products  accumulating 
at  the  cut  surface  if  the  cord  has  been  severed.  Injection  of  extracts 
produces  changes  in  the  sodium  content  of  the  fish  and  also  changes 


VII.   12 


FOREBRAIN 


209 


in  buoyancy,  perhaps  due  to  an  influence  on  the  carbonic  anhydrase 
of  the  gas  bladder. 

12.  Brain  of  bony  fishes 

The  brain  of  bony  fishes  is  built  on  the  same  general  functional  and 
structural  plan  as  that  of  elasmobranchs,  namely,  the  development  of  a 
number  of  separate  centres,  one  concerned  with  each  of  the  main 
receptor  systems.  The  forebrain  is  often  large,  but  it  is  characterized 


chiasma 
opticum 


rec.  pr. 


Fig.  127  {a).  Cross-section  of  the  forebrain  of  the  cod. 
lat.tr.  and  tn.tr.  lateral  and  medial  tracts  between  olfactory  region  and  hypothalamus;  hyp. 
hypothalamus;  m.  membranous  roof  of  forebrain;  n.mag.  nucleus  magnocellularis  preopticus; 
n.opt.  optic  tracts  (that  on  the  right  has  atrophied  in  this  specimen) ;  rec.  pr.  preoptic  recess ; 
str.  hind  end  of  striatum;  thai,  thalamus;   3rd  v.  third  ventricle.  (From  Kappers,   Huber, 

and  Crosby.) 

by  great  development  of  its  ventral  regions  (the  'corpus  striatum'),  the 
roof  being  wholly  membranous  (Figs.  127  (a),  128).  This  condition  is 
known  as  'eversion'  and  is  the  very  opposite  to  the  inverted  or  thick- 
roofed  forebrains  that  are  found  in  the  lung-fishes,  close  to  the  line 
of  tetrapod  descent  (p.  278).  The  whole  of  this  forebrain  is  reached  by 
olfactory  fibres,  and  there  is  little  evidence  that  fibres  from  other 
receptor  centres  reach  forward  to  it;  it  is  mostly  a  smell  brain. 
Extirpation  of  the  telencephalon  from  various  teleosts  has  not 
produced  changes  in  locomotion,  balance,  or  vision;  there  may  be 
slight  changes  in  general  activity  and  social  behaviour.  No  movements 
have  been  seen  following  electrical  stimulation  of  it. 

The  diencephalon  is  not  large,  since  most  of  the  optic  fibres  end 
not  here,  but  in  the  midbrain.  The  roof  is  everted  to  form  a  pineal 
body,  and  this  and  other  parts  of  the  diencephalon  may  contain 


210  BONY  FISHES  vn.  12 

receptors  sensitive  to  light.  The  minnow  Phoxinus  has  a  transparent 
patch  on  the  head  in  this  region,  and  it  has  been  found  possible  to 
train  the  fish  to  give  appropriate  responses  to  changes  of  illumination 
even  after  removal  of  the  paired  eyes  and  the  pineal  body.  Evidently 
there  are  light-sensitive  cells  in  other  parts  of  the  walls  of  the  dien- 
cephalon,  besides  those  that  become  evaginated  to  form  the  eyes. 
Experiments  on  lampreys  also  showed  the  presence  of  such  cells 
(p.  105).  The  hypothalamus  is  well  developed  and  receives  large  tracts 
from  the  forebrain.  Below  and  behind  it  is  a  large  saccus  vasculosus 
in  some  forms  (p.  169). 

The  midbrain  is  often  the  largest  part  of  the  brain.  The  cells  spread 
out  over  its  roof  (tectum  opticum)  are  not  all  collected  round  the 
ventricle  but  have  migrated  away  to  make  an  elaborately  layered 
system.  Into  this  midbrain  cortex  there  pass  not  only  the  great  optic 
tracts  but  also  ascending  tracts  from  the  sensory  regions  of  the  spinal 
cord,  lateral  line  system,  gustatory  systems,  and  cerebellum.  Large 
motor  tracts  pass  back  towards  the  spinal  cord;  the  details  of  their 
endings  have  not  been  traced,  but  they  certainly  exercise  control  over 
motor  functions.  Electrical  stimulation  of  the  optic  lobes  produces 
well-coordinated  movements  of  local  groups  of  muscles,  for  instance 
those  of  the  eyes  or  fins.  It  can  hardly  be  doubted  that  this  well- 
developed  midbrain  apparatus  thus  controls  much  of  the  behaviour  of 
the  fish  and  is  able  to  mediate  quite  elaborate  acts  of  learning  and 
other  forms  of  more  complex  behaviour.  After  removal  of  the  tectum 
of  one  side  a  minnow  is  blind  in  the  opposite  eye.  Each  part  of  the 
retina  is  mapped  on  to  a  distinct  area  of  the  tectum  and  if  the  optic 
tract  is  cut  and  allowed  to  regenerate  this  projection  is  exactly  replaced. 
When  a  goldfish  is  trained  to  respond  to  some  visual  stimulus  the 
learning  process  occurs  in  the  midbrain  and  continues  unaffected  after 
removal  of  the  forebrain.  Conversely,  olfactory  learning  takes  place 
in  the  latter  and  is  undisturbed  by  injury  to  the  tectum  opticum. 

The  base  of  the  midbrain  (tegmentum)  contains  motor  centres. 
Electrical  stimulation  here  produces  abrupt  and  massive  responses  of 
the  locomotor  apparatus,  very  different  from  the  sequences  of  co- 
ordinated movements  that  appear  after  stimulation  of  the  roof  of  the 
tectum. 

The  cerebellum  is  very  large  in  teleosts,  especially  in  the  more 
active  swimmers,  and  a  forwardly  directed  lobe  of  it,  the  valvula 
cerebelli,  extends  under  the  midbrain.  Various  disorders  of  movement 
have  been  reported  after  removal  of  the  cerebellum,  such  as  swaying 
when  moving  quickly.  Presumably  it  plays  an  important  part,  as  in 


HKA1N  OF  TELEOSTS 


Fie.  128.  Transverse  sections  of  forcbrain  in  various  vertebrates  to  show  the  condition 

of  inversion  (thick  roof)  in  A,  n,  and  c  and  eversion  (thin  roof)  in  D,  E,  and  F. 

A,  lamprey;  B,  frog;  C,  chelonian;  D,  chimaera;  E.  sturgeon;  F,  teleostean;  pall,  pallium; 

sep.  septum;  str.  striatum.  (From  Kappers,  Huber,  and  Crosby.) 

m. 


Fig.  129.  Sagittal  section  of  brain  of  the  gurnard,  showing  the  swellings  in  the 

spinal  cord  at  the  point  of  entry  of  the  nerves  from  the  fin. 

C.  cerebral  hemisphere;  ce.  cerebellum;  hy.  hypothalamus;  in.  midbrain;  no.  swellings  of 

spinal  cord;  v.  valvula.  (From  Scharrer,  Z.  verg.  Physiol.  22.) 

other  vertebrates,  in  producing  precise  and  correctly  timed  movements. 
It  is  enormous  in  the  Mormyridae,  where  it  may  assist  in  direction- 
finding  by  electrical  pulses  (p.  253),  perhaps  acting  as  a  timing  device. 
The  medulla  oblongata  is  also  well  developed,  having  special  lobes 
connected  with  the  entry  of  the  lateral  line  nerves  and  gustatory  fibres 
of  the  cranial  nerves.  In  the  gurnard,  Trigla,  there  are  chemical 
receptors  in  the  elongated  fins.  These  are  innervated  from  spinal 
nerves,  and  there  are  swellings  of  the  dorsal  part  of  the  spinal  cord  at 
the  points  where  these  nerves  enter  (Fig.  129). 


212  BONY  FISHES  vn.  13- 

13.  Receptors  for  life  in  the  water 

The  features  of  the  environment  that  are  relevant  for  life  are  very 
different  in  air  and  water.  Man  is  so  well  used  to  the  air  that  it  is  not 
easy  to  appreciate  fully  the  conditions  underwater,  where  changes  of 
illumination,  though  obviously  important,  provide  less  detailed  evid- 
ence of  the  sequence  of  distant  events  than  they  do  in  air.  We  can 
say  that  light  carries  less  information  for  a  fish;  to  put  it  in  another 
way,  fewer  distinct  choices  between  alternative  behaviour  pathways 
are  made  on  the  basis  of  visual  clues  by  a  fish  than  by  a  man. 

On  the  other  hand,  the  water  around  the  fish  provides  mechanical 
stimuli  both  at  low  and  high  frequency  that  are  more  closely  related 
to  distant  events  than  is  generally  true  in  air.  Both  hearing  and  touch 
are  of  great  importance  in  the  water  and  the  lateral  line  system  pro- 
vides a  system  of  'distant  touch'  that  is  perhaps  wholly  outside  our 
experience.  Localization  of  distant  objects  by  such  a  sense,  perhaps 
assisted  by  echo-location  by  water  movements,  provides  the  fish  with 
many  relevant  clues.  It  is  interesting  that  these  receptors  are  connected 
with  a  very  large  cerebellar  system,  perhaps  concerned  with  measur- 
ing time  differences. 

Chemical  changes  in  the  water  also  provide  much  information  and 
both  taste  and  smell  are  well  developed.  That  smell  is  analysed  by  a 
distinct  system  in  the  forebrain,  not  directly  related  to  the  cerebellar 
system,  is  one  of  the  fundamental  principles  of  control  of  vertebrate 
behaviour.  Distant  chemical  changes  provide  the  first  clue  to  the 
presence  of  food,  a  mate,  or  an  enemy,  whereas  the  detailed  finding 
of  these  involves  eyes,  ears,  touch,  and  an  accurate  timing  system. 
There  thus  arises  the  distinction  between  the  systems  for  initiation  of 
action  in  the  forebrain  ('emotive')  and  for  its  fulfilment  (executive) 
by  centres  farther  back. 

14.  Eyes 

An  animal  provided  with  suitable  receptors  can  obtain  much 
information  about  the  environment  from  the  changes  in  illumination. 
Control  of  the  whole  physiology  to  follow  the  rhythm  of  day  and  night 
may  have  been  the  original  reason  for  the  development  of  photo- 
sensitivity in  the  diencephalon  (see  p.  105).  At  the  stage  of  evolution 
reached  by  teleosts  information  is  gained  from  the  fact  that  light 
varies  in  frequency  (colour)  and  intensity  (brightness)  and  that  it  is 
reflected  from  many  substances,  revealing  their  movement  and  shape. 
The  greatest  sensitivity  of  the  fish  eye  is  in  the  yellow-green,  which 


vii.  14  EYE  OF  TELEOSTS  213 

is  the  wavelength  that  penetrates  farthest  into  the  water.  In  order  to 
extract  the  maximum  of  information  at  high  as  well  as  low  intensities 
it  is  necessary  to  adjust  the  sensitivity,  and  hence  the  signal/noise 
ratio.  For  this  purpose  teleosts  have  developed  retinas  with  distinct 
rods,  cones,  and  twin-cones  and  in  some  there  is  a  fovea  composed  of 
numerous  thin  cones  (e.g.  in  Blennius).  The  pupil  usually  varies  little 
in  diameter,  and  adjustment  of  sensitivity  is  by  migration  of  pigment 


scleral  cartilage 


epichorioKJal  lymph  space 


choriad 
'glond 


Fig.  130.  Diagrammatic  vertical  section  of  a  typical  teleostean  eye.  Not  all  the  structures 
here  shown  are  found  in  all  species.  (From  Walls,  The  Vertebrate  Eye.) 

between  the  receptors  and  contraction  of  a  'myoid'  segment  of  the 
latter.  In  bright  light  the  pigment  expands,  the  cones  contract  for- 
ward, towards  the  light  and  the  rods  contract  back,  beneath  the  pig- 
ment. These  photo-mechanical  changes  thus  serve  the  same  end  as 
changes  of  pupil  diameter  in  other  vertebrates. 

The  photochemical  change  in  the  rods  of  marine  fishes  is  the  same 
as  that  of  land  vertebrates,  namely  the  breakdown  of  the  rose- 
coloured  'visual  purple'  (rhodopsin)  first  to  the  yellow  retinene  and 
then  to  colourless  vitamin  Av  In  freshwater  fishes  there  is  a  different 
pigment  porphyropsin,  or  visual  violet,  which  breaks  down  to  vita- 
min A2.  Intermediates  between  these  may  be  found. 

In  all  fishes  there  is  a  very  large,  dense,  spherical  lens,  to  which  is 
attached  a  retractor  muscle  (campanula  Halleri)  inserted  on  to  a  fal- 
ciform ligament,  which  occupies  the  persistent  choroidal  fissure  in  the 
retina  (Fig.  130).  The  eye  is  usually  said  to  be  myopic  at  rest  and  to  be 
accommodated  for  distant  vision  by  pulling  the  lens  nearer  to  the 


214  BONY  FISHES  vn.  14 

retina.  However,  this  has  recently  been  disputed  by  Verrier,  who 
denies  that  the  campanula  is  muscular  and  believes  the  eye  to  be 
hypermetropic  at  rest  and  accommodated,  if  at  all,  by  fibres  of  the 
ciliary  body,  as  in  other  vertebrates.  It  may  be  that  the  fixed  focus  is 
already  sufficiently  deep  and  the  campanula  perhaps  serves  mainly 
to  steady  the  lens. 

It  is  unwise,  however,  to  generalize  about  teleostean  eyes,  for  they 
are  very  varied.  Whereas  the  trout,  like  most,  has  a  round  pupil, 
which  varies  little  if  at  all  in  size,  other  fishes,  whose  eyes  are  more 
exposed  to  light  from  above,  have  a  more  mobile  iris.  In  flat-fishes 
and  the  angler-fishes,  such  as  Lophius,  and  the  Mediterranean 
Uranoscopus,  the  star  gazer,  the  iris  has  an  'operculum'  and  is  very 
muscular;  its  movements  are  controlled  by  nerves  and  not,  as  in 
selachians,  by  the  direct  effect  of  light.  The  sympathetic  system  sends 
branches  into  the  head  in  these  animals  (Fig.  138)  and  its  fibres  cause 
contraction  of  the  sphincter  of  the  iris,  whereas  fibres  in  the  oculo- 
motor nerve  cause  contraction  of  the  dilatator,  the  opposite  arrange- 
ment to  that  in  mammals.  In  the  eel  the  pupil  is  also  capable  of  wide 
changes  of  diameter,  but  here  the  control  is  mainly  by  the  direct 
response  of  the  circular  sphincter  iridis  muscle  to  light  incident  upon 
it.  The  pupil  of  the  isolated  eye  of  an  eel  closes  when  illuminated  and 
reopens  again  in  darkness  (Fig.  131).  Presumably  because  of  its  lack 
of  nervous  control  this  iris  is  not  affected  by  many  of  the  usual 
'autonomic'  drugs.  For  instance,  closure  will  occur  in  the  presence  of 
atropine  and  the  dark-adapted  pupil  remains  unchanged  when  placed 
in  a  solution  as  strong  as  1  per  cent,  pilocarpine,  but  then  closes 
immediately  on  illumination  (Fig.  132).  The  isolated  pupil  of  Urano- 
scopus, however,  closes  when  pilocarpine  is  applied  (Fig.  133),  and 
in  this  case  the  sphincter  muscle  is  innervated  by  sympathetic  nerve- 
fibres.  Adrenaline  also  causes  the  sphincter  to  contract  and  acetyl 
choline  in  moderate  concentrations  causes  dilatation 

The  eyes  may  be  small  or  absent  in  fishes  living  in  caves,  muddy 
waters,  or  the  deep  sea.  In  this  last  habitat,  however,  many  have  ex- 
ceptionally large  eyes,  with,  apparently,  high  acuity  as  well  as  sensi- 
tivity. They  may  be  elongated  ('telescopic')  and  with  large  binocular 
fields  and  a  fovea  of  'rods'.  In  Bathylagus  the  rods  reach  a  density 
of  800,000  mm2  and  are  arranged  in  six  superimposed  layers,  which 
presumably  come  into  action  successively  as  an  object  approaches. 
The  cells  of  the  deeper  layers  are  less  closely  packed. 

The  tropical  fish  Anableps  lives  with  the  head  half  out  of  water  and 
the  eyes  are  adapted  for  use  in  both  media.  The  upper  part  of  the 


(215) 

Red 

White  light 

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Time, 


15 

minutes 


20 


25 


Fig.  131.  Closure  of  the  pupil  of  the  isolated  eel's  eye,  followed  by  plotting  the  move- 
ment of  its  margin  with  a  camera  lucida.  The  movements  are  shown  magnified  54  X  , 

Time  in  minutes. 


U- 


2-35 


Ringer 


2;Z0 

-2-05 
-1-90 
1-75 
1-60 
145 
1-30 
1-15 


Acetul  choline   .    .  ,   L  ■■ 
Vmnnnnn       Acetylcholine 

1/100.000  Atropine  7100,000 


Vl  .000.000 


Red  light 


White 


Red 


15 


20  11 


35 


40 

i 


45 


50 


55 


Time,  minutes 

Fig.   132.  Changes  of  diameter  of  isolated  eel's  iris  in  Ringer's  solution  with  the 

addition  of  various  drugs.  Acetyl  choline  produces  some  closure,  atropine  some 

opening.  Light  still  produces  closure  after  application  of  atropine. 


Pilocarpine 


Fig.  133.  Movements  of  margin  of  pupil  in  isolated  iris  of  Uranoscopus  in  isotonic 

solution.  Pilocarpine  produces  closure  and  atropine  opening  of  this  pupil  whose 

sphincter  muscle  is  innervated  by  sympathetic  nerve-fibres. 

(From  Young,  Proc.  Roy.  Soc.  B.  107.) 


2l6 


BONY  FISHES 


vii.  14- 

cornea  is  thickened,  the  iris  provides  two  pupils,  the  lens  is  pear- 
shaped,  and  there  are  two  retinas  in  each  eye. 

15.  Ear  and  hearing  of  fishes 

The  ear  provides  receptors  that  ensure  the  maintenance  of  a  correct 
position  of  the  fish  in  relation  to  gravity  and  to  angular  accelerations. 
In  addition,  in  many  species  it  serves  for  hearing.  The  inner  ear  is 
completely  enclosed  in  the  otic  bones.  There  is  a  perilymphatic  space 
only  in  those  species  that  hear  well. 


ant. 


Ns  Sag.  S.  L. 

Fig.  134.  Diagram  of  ear  of  the  minnow  Phoxinus. 

Ast.  asteriscus;  L.  lagena;  N.I.,  N.s.  nerves  of  lagena  and  saccule; 

S.  saccule;  Sag.  sagitta;   U.  utricle.  (From  V.  Frisch,  Z.  vergl. 

Physiol.  25.) 

Each  ear  sac  is  subdivided  into  three  semicircular  canals  and  three 
other  chambers,  the  utriculus,  sacculus,  and  lagena  (Fig.  134).  In 
each  chamber  is  carried  an  ear  stone  (otolith)  and  these  are  given 
special  names,  the  lapillus,  sagitta,  and  asteriscus,  occupying  the  above 
three  chambers  respectively. 

The  sensitive  macula  of  the  utricle  lies  horizontally,  with  the 
lapillus  resting  upon  it,  whereas  the  maculae  of  the  saccule  and  lagena 
are  vertical.  These  receptors  with  otoliths  have  double  or  triple 
functions.  At  rest  they  act  as  static  receptors,  signalling  the  position 
of  the  fish  in  relation  to  gravity  and  setting  the  fins  and  eyes  in  appro- 
priate positions.  In  movement,  together  with  the  semicircular  canals, 
they  signal  angular  accelerations,  initiating  compensatory  movements. 
Thirdly,  some  of  the  otolith  organs  respond  to  sonic  vibrations. 

In  the  fishes  that  hear  well  there  is  a  connexion  between  the  air 
bladder  and  the  ear.  This  may  be  either  direct,  by  means  of  a  sac 
extending  forwards  (in  Clupeidae  and  others)  or  indirectly  by  a  chain 
of  modified  vertebrae,  the  Weberian  ossicles  (Fig.  135).  This  latter 
arrangement  is  found  in  the  freshwater  Ostariophysi,  which  hear 


vii.  15  HEARING  OF  FISHES  217 

particularly  well.  In  these  fishes  the  receptors  are  in  the  inferior  part 
of  the  ear  (saccule  and  lagena,  Fig.  134).  The  sagitta  carries  a  special 
wing  projecting  into  the  cavity  and  is  so  suspended  as  to  serve  to 
amplify  vibrations.  Near  to  it  is 
a  thin  portion  of  the  wall  of  the 
sac,    which    would    favour    the 
passage  of  variations  of  pressure 
transmitted  to  the  endolymph  by 
the  ossicles. 

These  Ostariophysi  respond  to 
sounds  between  about  60-6,000 
vibrations/sec.  After  removal  of 
the  pars  inferior  responses  con- 
tinue only  up  to  120/sec.  If  the 
air  bladder  is  punctured  a  min- 
now can  still  respond,  but  only 
up  to  3,000/sec  and  with  a  sen- 
sitivity diminished  by  more  than 
fifty  times. 

Minnows  can  be  trained  to 
discriminate  between  warbled 
notes  separated  by  I  tone.  Non- 
ostariophyse  fishes  have  mostly 
a  much  lower  upper  limit  of 
hearing  and  lower  capacity  for 
discrimination.  The  Mormyridae 
(p.  254),  however,  approach  the 
minnows  in  this  respect  and  here 
there  is  a  special  isolated  portion 
of  the  air  bladder  within  the  otic 
bone. 

In  the  best  cases  the  sense  of 
hearing  of  fishes  thus  approaches 
that  of  man,  in  spite  of  the 
absence  of  a  coiled  cochlea  and 

basilar  membrane  with  fibres  of  different  lengths.  Clearly  the  discrimi- 
nation of  tones  cannot  here  depend  upon  differential  resonance  as  the 
theory  of  Helmholtz  requires.  In  spite  of  the  considerable  powers 
of  pitch  discrimination  there  is  little  evidence  of  capacity  to  localize 
sounds  except  when  they  are  loud  and  near. 


Sch. 

Fig.   135.    Position  of  ear  in  Ostariophysi 

and  its  relation  to  the   Weberian   ossicles, 

which  are  shown  in  black. 

C.tr.  transverse  canal  between  the  two  sacculi; 
//.  brain;  /.  'incus';  L.  lagena;  M.  'malleus'; 
S.  sacculus;  Sch.  swim-bladder;  S.i.  sinus  impar 
(perilymphatic  space);  St.  'stapes';  U.  utriculus. 
(From  V.  Frisch.) 


218  BONY  FISHES  vii.  16- 

16.  Sound  production  in  fishes 

A  surprisingly  large  number  of  fishes  can  produce  sounds  audible 
to  ourselves,  and  these  noises  are  used  by  the  fishes  either  for  shoaling, 
or  to  bring  the  sexes  together,  or  to  warn  or  startle  enemies.  Some  fish 
may  use  the  sounds  they  produce  for  echo-location.  Among  the  loudest 
of  the  sounds  is  that  produced  by  the  drum-fish  (Pogonias)  of  the 
Eastern  Atlantic.  The  'whistling'  and  other  noises  of  the  'maigre' 
(Sciaend)  are  supposed  to  be  the  origin  of  the  song  of  the  Sirens,  since 
they  can  easily  be  heard  above  the  water.  In  both  these  fishes  the 
sounds  are  made  mostly  if  not  wholly  in  the  breeding  season.  In 
others,  such  as  siluroids  and  Diodon,  the  noise  is  associated  with  the 
presence  of  spines  and  may  be  a  warning.  In  Congiopodas  the  nerves 
that  innervate  the  muscles  of  sound  production  also  supply  muscles 
that  raise  the  spines  (Packard). 

The  mechanism  for  sound  production  is  very  varied,  involving 
either  stridulation  by  the  vertebrae  (some  siluroids),  operculum 
(Cottus,  the  bull-head),  pectoral  girdle  (trigger-fishes),  teeth  (some 
mackerel  and  sun-fish),  or  phonation  by  the  air  bladder.  The  latter 
may  be  involved  either  by  its  use  for  'breathing'  sounds  in  physosto- 
matous  forms  (p.  261)  or  as  a  resonator.  Noise  production  is  common 
in  some  families  (Triglidae,  Sciaenidae,  Siluridae)  but  almost  absent 
from  others.  The  advantages  to  be  obtained  from  sound  production 
underwater  have  led  to  parallel  evolution  of  similar  mechanisms  in 
several  different  groups. 

17.  The  lateral  line  organs  of  fishes 

The  lateral  line  organs  occur  partly  as  rows  of  distinct  pits,  partly 
in  canals  that  communicate  with  the  surface  through  pores  in  the 
scales.  Besides  the  main  canal  running  down  the  body  and  served 
by  the  lateral  line  branch  of  the  tenth  cranial  nerve,  there  are  also 
lines  following  a  definite  pattern  on  the  head,  namely,  supra-  and 
sub-orbital  lines,  a  line  on  the  lower  jaw,  and  a  temporal  line  across 
the  back  of  the  skull.  The  canals  on  the  head  are  innervated  mainly 
from  the  seventh,  partly  from  the  ninth  cranial  nerve.  The  nerve- 
fibres  enter  the  very  large  acoustico-lateral  centres  of  the  medulla  and 
valvula  cerebelli. 

Fishes  possess  the  capacity  to  react  to  an  object  moving  some  dis- 
tance away  in  the  water  ('distant  touch  sense')  and  this  is  reduced  or 
absent  after  section  of  the  lateral  line  nerve.  Presumably  the  moving 
object  sets  up  currents  in  the  water,  which  move  the  fluid  (or  mucus) 
in  the  canals.  It  has  also  been  suggested  that  the  canals  serve  to  record 


vii.  17 


FUNCTION  OF  LATERAL  LINE 


219 


displacements  produced  by  the  swimming  movements  of  the  fish 
itself,  but  this  has  not  been  proved.  Fishes  deprived  of  the  lateral 
line  show  no  muscular  incoordination,  although  if  blind  they  collide 
frequently  with  solid  objects.  It  has  often  been  suggested  that  these 
organs  serve  for  hearing,  perhaps  at  low  frequencies,  but  this  is 
probably  not  so. 


Fig.  136.  Responses  of  a  single  end  organ  in  a  lateral  canal  of  a  ray,  shown  with  an 
oscillograph  after  amplification.  Time  signal  10  sec.  intervals.  The  movements  of 
the  continuous  white  line  show  A,  the  beginning  of  a  headward  flow,  increasing  the 
frequency  of  discharge;  B,  the  end  of  this  flow;  c,  return  of  spontaneous  discharge 
after  an  interval  of  28  sec;  D,  spontaneous  discharge  60  sec.  later;  E,  beginning  of 
a  tailward  perfusion,  inhibiting  the  discharge;  F,  the  end  of  this  perfusion;  G,  the 
spontaneous  discharge  10  sec.  later.  (From  Sand,  Proc.  Roy.  Soc.  B.  123.) 


Study  of  the  electrical  activities  of  these  organs  in  rays  has  shown 
that  many  of  them  discharge  impulses  all  the  time,  even  when  not 
under  the  influence  of  any  external  stimulation  (Fig.  136).  By  passing 
currents  of  water  along  the  tubes  Sand  showed  that  a  tailward  flow 
checks  and  a  headward  flow  accelerates  this  'spontaneous'  discharge  of 
impulses.  Such  changes  in  the  streams  of  impulses  arriving  at  the 
brain  could,  no  doubt,  form  the  basis  for  initiation  of  movements  of 


220 


BONY  FISHES 


vii.  17- 


the  fish.  This,  however,  still  leaves  open  the  question  of  what  agency 
initiates  movement  of  the  fluid  in  the  canals  during  life.  It  has  been 
shown  that  when  small  streams  of  water  are  directed  against  the  side 
of  the  tail  some  fish  make  escaping  movements,  but  that  these  no 
longer  appear  when  the  lateral  line  nerve  has  been  cut.  The  lateral 
line  organs  thus  provide  signals  when  agitation  of  the  water  causes 
pressure  changes.  In  fact  they  provide  the  animal  with  a  kind  of 
water  touch,  though  it  is  not  certain  whether  this  is  their  only  func- 

/^v     Lat.d. 
gust. 


max 


Lat.v. 
pelv.         pect. 

Fig.  137.  Dissection  of  whiting  to  show  the  cranial  nerves,  and  especially  the 
nerves  for  the  taste-buds. 

an.  anal  fin;  gust,  gustatory  branch  of  facial;  lat.d.  and  lat.v.  dorsal  and  ventral  lateral  line 

nerves  of  vagus;   mand.   and  max.   mandibular  and  maxillary  divisions  of  trigeminal;   op. 

ophthalmic;  pect.  pectoral  fin;  pelv.  pelvic  fin;   VII,  hyomandibular  branch  of  facial;  IX, 

glossopharyngeal;  X.visc.  visceral  branch  of  vagus. 

tion.  Why  this  type  of  receptor  should  need  such  a  peculiar  apparatus 
of  canals,  rather  than  a  system  of  nerve-fibres  in  the  skin,  innervated 
by  the  spinal  dorsal  roots,  is  not  clear,  nor  do  we  know  the  significance 
of  the  pattern  of  lines  on  the  head.  The  lateral  line  system  must  cer- 
tainly be  of  great  importance  in  aquatic  life,  for  it  is  found  in  all  types 
of  fishes  and  also  in  the  early  Amphibia  and  in  the  aquatic  larvae  of 
modern  members  of  that  group.  The  distant  touch  receptors  could 
obviously  be  used  in  many  ways,  not  only  to  locate  moving  objects 
and  water  currents  but  to  serve  for  echo-location,  by  computing  the 
time  relation  of  reflected  waves  set  up  by  the  fish  itself. 

18.  Chemoreceptors.  Taste  and  smell 

As  in  all  vertebrates,  there  are  two  separate  chemical  senses,  taste 
and  smell.  The  former  serves  mainly  to  produce  appropriate  reactions 
to  food  near  the  body,  such  as  snapping,  swallowing,  or  movements 
of  rejection.  Smell,  on  the  other  hand,  is  a  'distance  sense',  by  which 
the  whole  animal  is  steered.  The  distinction  between  the  two  types 
of  receptor  is  somewhat  obscured  in  bony  fishes  by  the  fact  that  taste- 
buds  are  not  restricted  as  they  are  in  mammals  to  the  tongue  and 


vii.  i8  TASTE  AND  SMELL  221 

pharynx  but  may  occur  on  the  whiskers  and  all  over  the  body.  They 
are  innervated  by  branches  of  the  seventh,  ninth,  and  tenth  cranial 
nerves,  which  may  reach  far  backwards  (Fig.  137).  In  some  species  it 
has  been  shown  that  the  fish  is  able  to  turn  and  snap  at  a  piece  of  food 
placed  near  the  tail.  This  power  is  lost  if  the  branches  from  the  cranial 
nerves  are  cut.  In  mammals  taste-buds  serve  to  discriminate  only  four 
qualities  (salt,  sour,  bitter,  and  sweet),  most  of  our  so-called  'tasting' 
being  in  reality  the  smelling  of  the  food  in  the  mouth.  In  fishes,  also, 
the  four  taste  qualities  are  discriminated  by  the  taste-bud  system,  and 
it  has  been  shown  that  the  minnow  (Phoxinus)  continues  to  make  such 
discriminations  after  the  forebrain  has  been  removed.  Other  chemical 
discriminations  are  made  by  the  nose,  however,  and  can  only  be 
performed  with  an  intact  forebrain.  Thus  Phoxinus  tastes  and  smells 
the  same  classes  of  substances  as  man  does.  The  taste-buds  are 
exceedingly  sensitive,  the  threshold  for  sweet  substances  being  500 
times  and  for  salt  200  times  lower  than  in  man.  On  the  other  hand, 
some  substances  that  are  very  bitter  for  us  produce  little  reaction  in 
Phoxinus. 

In  many  fishes  the  nose  is  one  of  the  chief  receptors  (macrosmatic). 
There  are  two  nostrils  on  each  side,  allowing  for  the  sampling  of  a 
stream  of  water  (Fig.  119).  The  nose  does  not  communicate  with  the 
mouth,  except  in  a  few  fishes  that  live  buried  in  the  sand  (Astroscopus). 
The  sense  of  smell  is  used  to  find  food  and  for  recognition  of  the 
sex  of  members  of  the  same  species.  Minnows  can  be  trained  to  give 
distinct  reactions  to  extracts  made  from  the  skin  of  other  species  of 
fish  living  in  fresh  water.  In  the  presence  of  'alarm  substances'  pro- 
duced by  damaged  skin  of  a  member  of  the  same  species,  minnows 
(and  other  fishes)  show  a  'fright  reaction',  scattering  and  refusing  food. 
The  state  of  development  of  the  nose  is  very  varied.  It  is  large  in 
macrosmatic  solitary  predators  such  as  Anguilla  and  in  many  schooling 
species  that  also  have  well-developed  eyes  {Phoxinus,  Gobio).  Daylight 
predators,  on  the  other  hand,  are  microsmatic  (Esox,  Gasterosteus). 
Other  evidence  shows  that  fishes  can  discriminate  between  the  smells 
of  water  plants  and  between  the  waters  of  different  streams.  It  is 
likely  that  this  provides  part  of  the  mechanism  by  which  salmon 
return  to  the  stream  in  which  they  were  born,  having  been  conditioned 
as  fry  to  the  smell  of  its  water.  It  has  been  suggested  that  they  might 
be  decoyed  to  return  to  a  stream  other  than  that  where  they  were 
hatched  by  conditioning  them  as  fry  to  a  substance  such  as  morpholene 
to  which  they  have  a  high  sensitivity  although  it  is  neither  an  attract- 
ant  nor  repellant. 


222 


BONY  FISHES 


vii.  19- 


Fig.  138.  Diagram  of  ventral  view  of  the 
sympathetic  system  of  the  front  part  of  the 
body  of  Uranoscopus,  showing  the  fibres 
in  the  sympathetic  and  oculomotor  that  are 
responsible  for  the  light  reflex. 
(From  Young.) 

cil.brev.  cil.long.,  short  and  long  ciliary  nerves; 
cil.gn.,  ciliary  ganglion;  dors.r.  dorsal  root;  dil. 
dilatator  muscle;  hypo,  hypoglossal;  n.splanch. 
splanchnic  nerve;  opt.  optic  nerve;  p.  pupil; 
pal.  VII,  palatine  branch  of  facial ;  prof,  profun- 
dus; r.b.  short  root  of  ciliary  ganglion;  r.comm. 
ramus  communicans;  r.l.  long  root  of  ciliary 
ganglion;  sph.  sphincter  muscle;  ventr.r.  ven- 
tral root;  1II-X,  cranial  nerves  with  their 
sympathetic  ganglia  (V.symp.  &c.);  VII  hyo. 
hyomandibular  branch  of  facial;  r— 4  sp.symp. 
spinal  sympathetic  ganglia. 


19.  Touch 

Touch  is,  of  course,  well 
developed  in  fishes,  and  in  many 
species  there  are  special  sensory 
filaments,  which  presumably  serve 
this  sense.  They  are  usually  de- 
veloped around  the  mouth,  as  in 
the  catfish;  in  other  fishes  they 
are  modifications  of  the  fins,  for 
instance,  the  pectoral  fins  of 
gurnards,  which  also  contain 
chemoreceptors. 

20.  Autonomic  nervous  system 

The  autonomic  nervous  system 
of  bony  fishes  is  organized  on  a 
plan  rather  different  from  that 
both  of  elasmobranchs  and  of 
land  animals.  There  is  a  chain  of 
sympathetic  ganglia,  extending 
from  the  level  of  the  trigeminal 
nerve  backwards,  a  ganglion 
being  found  in  connexion  with 
each  of  the  cranial  dorsal  roots 
(Figs.  138  and  139).  These  gan- 
glia do  not  receive  pre-ganglionic 
fibres  from  the  segments  in  which 
they  lie,  but  by  fibres  that  run  out 
in  the  ventral  roots  of  the  trunk 
region  and  thence  forwards  in  the 
sympathetic  chain.  This  emer- 
gence of  the  pre-ganglionic  fibres 
for  the  head  in  the  trunk  region 
recalls  the  arrangement  in  land 
animals. 

Each  trunk  sympathetic  gan- 
glion, besides  receiving  a  white 
ramus  communicans  of  pre-gan- 
glionic fibres  from  its  spinal  nerve, 
also  sends  a  grey  ramus  back  to 


VII.  20 


AUTONOMIC  NERVES  OF  TELEOSTS 


223 


that  nerve,  this  ramus  carrying  post-ganglionic  fibres  to  the  skin. 
Some  of  these  fibres  control  the  melanophores,  causing  them  to 
contract  (p.  259).  In  elasmobranchs  there  are  no  grey  rami  communi- 
cantes  and  no  sympathetic  system  in  the  head  (p.  173);  the  differences 
between  the  two  groups  are  therefore  very  striking. 


HI    prof    Viymp 


Fig.  139.  Diagram  of  the  autonomic  nervous  system  of  Uranoscopus  seen  from  the  side. 

bl.  mesonephric  bladder;  cil.gn.  ciliary  ganglion;  dors,  dorsal  root;  n.sph.  nerve  to  anal 
sphincter;  n.spl.  splanchnic  nerve;  prof,  nervus  ophthalmicus  profundus;  rad.  brev.  short 
root  of  ciliary  ganglion;  r.comm.  ramus  communicans  (including  both  white  and  grey  fibres); 
stan.  'corpuscle  of  Stannius'  (adrenal  cortical  tissue?);  ventr.  ventral  root;  ///,  oculomotor 
nerve;   V— X  symp.  sympathetic  ganglia  associated  with  the  cranial  nerves.    (From  Young, 

Quart.  J.  Micr.  Sci.  75.) 


Fig.  140.  Tracing  of  the  contractions  of  a  strip  of  the  stomach  muscle  of  the  angler- 
fish,  Lophins,  attached  to  a  lever.  Time  in  minutes.  At  A,  faradic  stimulation  of  the 
vagus  nerve.  Drugs  then  added  to  the  solution  to  make,  at  B  acetyl  choline  1/1,000,000; 
at  c  acetyl  choline  1/100,000;  at  D  adrenaline  1/100,000. 
(From  Young,  Proc.  Roy.  Soc.  120.) 

Little  is  known  about  the  parasympathetic  system  of  bony  fishes. 
The  oculomotor  nerve  carries  fibres  to  the  iris,  which  work  in  the 
opposite  direction  to  fibres  from  the  sympathetic  (p.  214).  There  is 
also  a  well-developed  vagal  system,  but  so  far  as  is  known  no  para- 
sympathetic fibres  in  other  cranial  nerves  and  probably  no  sacral 
parasympathetic  system.  Electrical  stimulation  of  the  vagus  nerve 


224  BONY  FISHES  vn.  20- 

produces  movements  of  the  stomach  but  not  of  the  intestine;  the 
latter,  however,  shows  movements  when  the  splanchnic  nerve  is 
stimulated.  In  most  of  the  viscera  acetyl  choline  causes  initiation  of 


nnnnnnnnnnnnnnnnnnnnnnnnnnnnnnnr 


11111111111J1I. 

Fig.  141.  Tracing  of  contractions  of  the  muscle  of  the  urinary  bladder  of  Lopliius, 

attached  to  a  lever.  At  A,  D,  and  F  faradic  stimulation  of  vesicular  nerve.  Drugs  added 

to  make,  at  b  acetyl  choline  1/2,000,000;  at  c  adrenaline  1/500,000;  at  E  ergotoxine 

1/50,000.  Time,  minutes.  (From  Young.) 


Fig.  142.  Tracing  to  show  effect  of  atropine  1/50,000  added  at  A,  on  the  contractions 

of  the  bladder  of  Lophius  produced  by  faradic  stimulation  of  the  vesicular  sympathetic 

nerve.  Time,  minutes.  (From  Young.) 

rhythmic  contractions  and  these  are  inhibited  by  adrenaline  (Figs. 
140  and  141).  In  Lophius  this  is  true  of  the  stomach,  with  motor-fibres 
from  the  vagus,  intestine,  with  sympathetic  motor-fibres,  and  of  the 
muscles  of  the  bladder,  which  contract  on  stimulation  of  the  hinder 
sympathetic  ganglia.  However,  in  the  trout  adrenaline  causes  contrac- 
tion of  the  stomach  (Burnstock,  1958).  The  effect  of  the  nerves  to  the 


vii.  21  BEHAVIOUR  OF  FISHES  225 

bladder  is  prevented  by  atropine  (Fig.  142)  but  not  by  ergotoxine 
(Fig.  141),  though  the  latter  is  the  drug  that  in  mammals  often  inhibits 
sympathetic  motor-fibres.  In  these  fishes,  therefore,  it  is  not  possible 
to  divide  up  the  autonomic  nervous  system  into  sympathetic  and 
parasympathetic  divisions  by  either  anatomical,  physiological,  or 
pharmacological  criteria.  Presumably  the  two  'antagonistic'  systems 
found  in  mammals  are  a  late  development,  allowing  for  a  delicate 
balancing  of  activities  for  the  maintenance  of  homeostasis. 

21.  Behaviour  patterns  of  fishes 

The  well-developed  receptors  and  brain  of  the  teleostean  fishes 
constitute  perhaps  the  most  important  of  all  factors  in  giving  them 


Fig.  143.  The  red  belly  of  the  stickleback  releases  attacking  behaviour  in  other  males 

and  following  by  females.  Of  the  above  models  only  the  two  on  the  left  acted  as 

releasers.  (From  Tinbergen,  Wilson  Bulletin,  1948.) 

their  great  success.  Varied  habits  and  quick  actions  enable  the  fish  to 
make  full  use  of  the  possibilities  provided  by  the  special  features  of 
their  structure — the  air  bladder,  mouth,  and  so  on.  The  receptors  and 
brain  make  it  possible  for  the  fish  to  learn  to  react  appropriately  to 
many  features  of  its  surroundings.  Thus  the  eyes  besides  orientating 
the  fish  to  movements  in  the  visual  field  allow  the  discrimination  of 
wavelengths  and  distinct  reactions  to  differing  shapes  (see  Bull,  1957). 

The  social  behaviour  of  many  species  includes  the  development  of 
special  'releasers',  shapes,  colours,  or  postures  that  are  displayed  by 
one  individual  and  elicit  specific  reactions  in  another  (Fig.  143). 

There  is  no  doubt  that  fishes  possess  great  powers  of  learning. 
They  can  form  conditioned  reflexes  involving  discrimination  of  tones, 
also  second-order  conditioned  reflexes,  in  which  after  the  animal  has 
learnt  to  give  a  certain  behaviour  in  response  to  a  visual  stimulus  it  is 
then  taught  to  associate  the  latter  with  an  olfactory  stimulus.  There 
are  many  other  examples  of  such  powers,  but  unfortunately  we  have 
as  yet  little  information  as  to  the  way  in  which  they  are  brought  about 
by  the  brain.  Nor  have  the  naturalists  provided  us  with  very  clear 
examples  of  the  use  of  these  powers  by  fishes  in  nature.  There  are 


226 


BONY  FISHES 


VII.  21 


many  tales  of  carp  coming  to  be  fed  at  the  ringing  of  a  bell,  and  similar 
powers  of  association  must  play  a  part  in  the  life  of  fishes  in  more 
natural  situations.  Bull  has  shown  that  fishes  can  be  trained  to  dis- 
criminate between  very  small  differences  of  water  flow,  temperature, 
salinity  or  pH,  and  no  doubt  it  is  by  means  of  such  powers  that  they 
normally  find  a  suitable  habitat. 


Fig.  144.  Migrations  of  the  eels.  The  European  species  (A.  anguilld)  occurs  along  the 
coasts  outlined  with  lines,  the  American  species  {A.  rostrata)  where  there  are  dots. 
The  curved  lines  show  where  larvae  of  the  lengths  indicated  (in  millimetres)  are  taken. 

(After  Norman.) 

The  migrations  of  fishes  have  attracted  much  attention,  but  are 
still  imperfectly  understood.  They  vary  from  the  'catadromous'  down- 
ward migration  of  young  animals  to  the  sea  and  the  reverse  'anadro- 
mous'  movement  to  breed,  to  the  astounding  journeys  of  the  eels, 
3,000  miles  westwards  from  Europe  or  eastwards  from  America  to 
their  breeding-place  in  the  Sargasso  Sea  (off  Bermuda)  and  the  return 
of  the  elvers  to  the  homes  of  their  parents  (Fig.  144).  No  one  has  yet 
discovered  the  factors  that  direct  these  movements,  currents  may  play 
a  part,  but  can  hardly  be  the  only  influence.  Indeed  it  has  been 
suggested  that  European  eels  never  complete  the  journey  but  die  in 


vii.  21  MIGRATION  OF  EELS  227 

their  own  continental  waters.  The  populations  of  so-called  European 
eels  {Anguilla  anguilld)  would  then  be  maintained  by  reinforcements 
of  larvae  of  the  American  A.  rostrata,  the  differences  between  the 
two  being  due  to  temperature  and  other  factors  (Tucker,  1959). 

Social  behaviour  is  marked  in  many  species  and  shoals  of  some 
fishes  may  contain  many  thousands  of  individuals.  The  animals  are 
presumably  kept  together  in  most  species  by  visual  stimuli,  though 
sounds  may  play  a  part.  Shoaling  gives  protection  to  small  fishes,  and 
in  some  species  the  animals  come  together  in  shoals  to  breed  (her- 
rings). There  may  also  be  some  advantage  for  the  finding  of  suitable 
feeding  conditions,  but  on  all  these  points  we  can  do  little  more  than 
speculate  and  hope  for  further  information. 


VIII 

THE  EVOLUTION  OF  BONY  FISHES 

1 .  Classification 

Class  Actinopterygii 
Superorder  i.  Chondrostei 

Order  i.  Palaeoniscoidei.  Devonian-Recent 

*Cheirolepis;  *Palaeoniscus;  * Amphicentrum;  *Platysomus, 
*Dorypterus ;  *Cleithrolepis;  *Tarrasius;  Polypterus,  bichir 
Order  2.  Acipenseroidei.  Jurassic-Recent 

*Chondrosteus;  Acipenser,  sturgeon;  Polyodon,  paddle-fish 
Order  3.  Subholostei.  Triassic-Jurassic 
*Ptyeholepis 
Superorder  2.  Holostei.  Triassic-Recent 

*Acentrophorus;  *Lepidotes;  *Dapcdius;  *Microdon;  Amia, 
bowfin;  Lepisosteus,  gar-pike 
Superorder  3.  Teleostei.  Jurassic-Recent 
Order  1.  Isospondyli 

*LeptoIepis;  *Portheus;  Clupea,  herring;  Salmo,  trout 
Order  2.  Ostariophysi 

Cyprinus,  carp;  Tinea,  tench;  Silurus,  catfish 
Order  3.  Apodes 

Angnilla,  eel;  Conger,  conger  eel 
Order  4.  Mesichthyes 

Esox,  pike ;  Belone;  Exoeoetus,  flying  fish ;  Gasterostens,  stickle- 
back; Syngnathns,  pipe-fish;  Hippoeampus,  seahorse 
Order  5.  Acanthopterygii 

*HopIopteryx;  Zens,  John  Dory;  Perca,  perch;  Labrus,  wrasse; 
Uranoscopns,  star  gazer;  Blennins,  blenny;  Gadus,  whiting; 
Pleuronectes,  plaice;  Solea,  sole;  Lophius,  angler-fish 

2.  Order  1.  Palaeoniscoidei 

The  actinopterygian  stock  has  been  distinct  since  Devonian  times. 
The  early  representatives  lacked  many  of  the  specializations  that  we 
find  in  the  successful  bony  fishes  today  and  showed  features  of  simi- 
larity to  the  Crossopterygii.  These  Devonian  Actinopterygii  had  not 
yet  acquired  the  striking  signs  of  full  mastery  of  the  waters,  which  are 
so  characteristic  of  the  group  today.  They  resembled  their  ancestors 
the  placoderms  and  their  cousins  the  crossopterygians  in  being  rather 


VIII.  2 


PALAEONISCIDS  229 

clumsy,  heavily  armoured  creatures.  From  this  early  type  many  lines 
have  been  derived  and  can  be  followed  with  some  completeness  to 
their  extinction  or  modern  descendants.  Various  classifications  have 
been  suggested.  The  one  used  here  is  simple  but  for  that  very  reason 
obscures  the  multiplicity  of  parallel  lines.  A  recent  classification 
recognizes  fifty-two  orders  of  Actinopterygii  (Grasse). 

d. 


Fig.  145.  Scales  of  some  early  fishes. 
A,  hypothetical  condition  with  denticle-like  substance  (d.)  attached  to  a  basal  bony  plate  lying 
in  the  connective  tissue  (ct:)\  B,  'cosmoid'  scale  of  early  crossopterygians,  showing  the  cosmine 
layer  (co.) ;  epidermis  (ep.) ;  vascular  canals  (hv.)  and  underlying  'isopedin'  {is.);  C,  palaeoniscoid 
scale  with  layers  of  'ganoin'  (ga.);  d,  lepidosteoid  scale  of  the  gar-fish  with  tubules  (/.).  (From 
Goodrich,  Vertebrata,  A.  &  C.  Black,  Ltd.) 

The  Devonian  and  Carboniferous  forms  are  grouped  together  in 
the  order  Palaeoniscoidei,  and  animals  of  similar  type  survive  today 
as  Polypterus,  the  bichir  of  African  rivers,  which  though  showing  some 
specializations  remains  in  its  general  organization  near  the  palaeoniscid 
level. 

A  typical  Palaeozoic  palaeoniscid  such  as  *Cheirolepis  was  a  long- 
bodied  creature  (Figs.  146  and  147)  with  a  heterocercal  tail,  single 
dorsal  fin,  and  pelvic  fins  placed  far  back  on  the  body.  The  pectoral 
and  pelvic  fins  had  broad  bases  and  the  radials  fanned  out  from  a  small 
muscular  lobe,  present  in  all  early  actinopterygians  but  lost  in  later 
forms.  The  body  was  covered  with  thick  rhomboidal  scales  very 
similar  to  those  of  acanthodians.  They  articulated  by  peg  and  socket 
joints  and  have  a  structure  known  as  palaeoniscoid  (Fig.  145).  The 
scale  is  deeply  embedded  and  grows  by  addition  both  to  the  bony  or 
isopedin  portion  and  to  the  shiny  surface-layer,  the  ganoin,  which 
thus  becomes  very  thick.  There  is  a  middle  layer  of  'pulp'  correspond- 
ing to  the   cosmine  layer  of  the  cosmoid  scale  of  Crossopterygii 


230  BONY  FISHES  vm.  a 

(p.  269)  and  the  two  types  have  obvious  similarities,  though  it  is  not 
clear  how  they  are  related. 

The  skull  was  built  on  a  distinctly  different  plan  from  that  of 
Crossopterygii,  in  that  there  was  no  joint  such  as  was  present  in  those 
fishes  to  allow  the  front  part  to  flex  on  the  hind.  The  jaw  support  was 
amphistylic,  in  the  sense  that  the  palatoquadrate  was  attached  to  the 
neurocranium  by  a  basal  process,  but  the  otic  process  did  not  reach 
the  skull  and  the  hind  end  of  the  jaw  was  supported  by  the  hyomandi- 
bula.  There  were  even  more  dermal  bones  than  are  found  in  modern 
Actinopterygii,  arranged  so  as  to  form  a  complete  covering  for  the 
chondrocranium  and  jaws.  These  bones  were  derived  from  the  original 
scaly  covering  of  the  head  and  the  naming  and  comparing  them  with 
the  bones  of  other  forms  is  a  matter  of  some  difficulty.  Some  of  the 
main  bones  resemble  in  appearance  and  shape  those  found  in  tetra- 
pods,  but  there  are  others  for  which  no  such  homologues  can  be 
found,  and  sometimes  there  is  considerable  difficulty  in  recognizing 
even  the  main  outlines  of  the  pattern.  The  problem  is  that  we  have 
no  rigid  criterion  by  which  to  set  about  giving  names  to  the  skull 
bones.  No  system  yet  discovered  is  wholly  satisfactory,  and  we  must 
admit  to  insufficient  knowledge  of  the  factors  that  determine  that 
bone  shall  be  laid  down  in  certain  areas  and  that  sutures  shall  separate 
these  from  each  other.  However,  some  of  the  dermal  bones  lie  in 
relation  to  the  lateral  line  canals  (or  rows  of  neuromasts),  which  latter 
may  provide  the  stimulus  to  bone  formation.  The  lines  are  remarkably 
constant,  perhaps  because  of  their  function  in  detecting  water  move- 
ments in  relation  to  swimming,  and  this  is  the  factor  that  determines 
the  position  of  many  of  the  bones.  Others  fill  in  the  spaces  between 
(anamesic  bones).  Yet  others  may  be  differentiated  in  relation  to  the 
teeth.  However,  the  number  of  bones  along  any  one  line  may  vary 
greatly  even  in  one  species  (e.g.  in  Amid).  The  whole  pattern  is  more 
variable  in  fishes  than  in  higher  vertebrates,  but  it  is  usual  to  consider 
that  the  bones  of  early  Actinopterygii  resemble  those  of  Crossopterygii 
and  of  the  early  amphibians  (Fig.  194). 

The  roof  of  the  skull  usually  shows  a  large  pair  of  parietals  between 
the  eyes,  and  post-parietals  behind  these.  Between  the  parietals  and 
the  nostrils  there  are  frontal  bones  and  the  front  of  the  head  usually 
also  carries  a  number  of  rostral  bones,  not  found  in  higher  forms. 
Behind  the  post-parietals  in  the  midline  is  a  series  of  extrascapular 
bones. 

The  side  of  the  skull  of  palaeoniscids  is  covered  by  numerous  bones, 
including  a  series  of  pre-  and  post-frontals,  post-orbitals,  and  jugals 


VIII.  2  PALAEONISCIDS  231 

around  the  eyes.  The  outer  margin  of  the  upper  jaw  is  covered  by 
premaxillae  and  maxillae,  which  are  the  main  tooth-bearing  bones. 
Behind  the  orbital  series  of  bones  the  cheek  is  very  variable.  Sometimes 
there  is  a  large  bone  identifiable  as  a  pre-opercular,  with  a  series  of 
opercular  bones  behind  it.  The  lower  portion  of  the  throat  was  covered 
by  a  series  of  gular  plates.  The  spiracle  in  these  early  forms  opened 
above  the  opercular  bones.  The  pectoral  girdle  was  attached  to  the 
back  of  the  skull  by  a  supracleithrum,  below  which  a  cleithrum  and 
clavicle  made  a  series  of  dermal  bones  behind  the  gills,  covering  the 
cartilaginous  girdle.  The  roof  of  the  mouth  contained  a  median  para- 
sphenoid,  with  paired  prevomers  in  front  of  it,  and  a  series  of 
pterygoid  bones  occupied  the  space  between  it  and  the  edge  of  the 
jaws,  the  palatine,  ectopterygoid,  pterygoid,  and  sometimes  others. 
Finally  the  lower  jaw,  besides  the  main  dentary  carrying  the  teeth, 
shows  many  small  bones  such  as  the  pre-articular  and  coronoid  on 
the  inner  surface;  splenial,  angular,  and  surangular  on  the  outside. 

It  will  be  clear  that  this  skull  of  *Cheirolepis  may  be  closely  com- 
pared with  the  skull  of  a  crossopterygian  or  a  modern  teleostean. 
The  general  plan  is  related  to  that  of  the  lateral  line  organs  arranged 
along  occipital,  supratemporal,  and  infra-orbital  lines.  The  numerous 
small  bones  are  evidently  similar  in  the  different  groups,  though  it  is 
not  easy  to  assign  a  suitable  name  to  every  one  of  the  more  numerous 
bones  of  the  earlier  forms. 

These  palaeoniscids  from  the  Middle  Devonian  were  rather  rare 
freshwater  fishes ;  they  had  sharp  teeth  and  probably  lived  on  inverte- 
brates. We  have  no  information  about  their  internal  anatomy,  but  it 
seems  not  unlikely  that  the  air-bladder  possessed  a  wide  opening  to 
the  pharynx  (as  it  still  does  in  Polypterns,  descended  from  this  stock) 
and  that  they  breathed  air,  as  did  other  Devonian  fishes.  However, 
they  did  not  have  internal  nostrils,  which  are  found  in  the  old  crosso- 
pterygians. 

During  the  Carboniferous  and  Permian  the  palaeoniscids  were 
numerous,  mostly  as  small,  sharp-toothed  fishes.  Several  distinct  lines 
became  laterally  flattened  and  acquired  an  outwardly  symmetrical  tail 
and  blunt  crushing  teeth  (Fig.  147).  These  characteristics  probably 
indicate  a  habit  of  feeding  in  calm  waters,  perhaps  mainly  on  corals, 
and  they  have  appeared  several  times  in  the  actinopterygian  stock 
(p.  241).  Palaeoniscids  of  this  type  were  formerly  placed  together  in 
a  family  Platysomidae,  but  it  is  now  considered  probable  that  the 
type  arose  independently  several  times;  thus  * Amphicentrum  is  found 
in  the  Carboniferous,  *PIatyso?nus  and  *Dorypterus  in  the  Permian, 


(232) 


Solea 


Uranoscopus 


Fig.  146.  Various  actinopterygians. 


viii.  2  PALAEONISCIDS  233 

*Cleithrulepis  in  the  Triassic.  Similar  forms  arose  again  later  among 
the  holosteans  and  teleosteans  and  we  have  therefore  evidence  that 
this  type  of  animal  organization  tends  to  evolve  into  deep-bodied 
creatures.  *Dorypterus  further  resembles  modern  teleosteans  in  a  great 
reduction  of  its  scales  and  in  the  forward  movement  of  the  pelvic  fins. 

Towards  the  end  of  the  Triassic  animals  of  typical  palaeoniscid 
type  became  rare;  they  were  replaced  by  their  more  active  and  speedy, 
mainly  marine  descendants,  the  Holostei  (p.  234).  Certain  of  the  lines 
that  branched  off  in  the  Palaeozoic  have,  however,  survived  to  the 
present  time,  and  in  spite  of  subsequent  specializations  they  give  us 
some  idea  of  the  characteristics  of  these  early  Actinopterygii.  Perhaps 
the  most  interesting  of  these  survivals  are  Polypterus,  the  bichir,  and 
the  related  Calamoichthys,  both  inhabiting  rivers  in  Africa.  The  air- 
bladder  shows  some  similarity  to  a  lung.  It  forms  a  pair  of  sacs  lying 
ventrally  below  the  intestine  and  opening  to  the  pharynx  by  a  median 
ventral  'glottis'  (Fig.  157).  This  is  the  arrangement  found  in  lung- 
fishes  (except  Ceratodus)  and  in  tetrapods,  and  it  seems  reasonable  to 
suppose  that  it  has  survived  in  Polypterus  from  Palaeozoic  times. 
However,  it  is  not  certain  to  what  extent  the  air-bladder  is  still  used 
as  a  lung,  for  Polypterus  cannot  survive  out  of  the  water. 

This  fish  shows  many  other  ancient  characteristics.  The  covering 
of  thick  rhomboidal  scales,  hardly  overlapping,  gives  the  animal  an 
archaic  appearance;  the  structure  of  the  scales  is  'palaeoniscoid'.  In 
the  skin  there  is  a  layer  of  denticles  outside  the  scales.  The  presence 
of  a  spiracle,  the  arrangement  of  the  skull  bones,  and  many  other 
features  suggest  that  Polypterus  is  essentially  a  palaeoniscid  surviving 
to  the  present  day.  In  the  intestine  there  is  a  spiral  valve,  which 
appears  to  have  been  present  in  the  early  Crossopterygii  and  Actino- 
pterygii (as  judged  from  fossilized  'coprolites')  and  occurs  today  not 
only  in  the  Dipnoi  but  also  in  sturgeons  and,  though  much  reduced,  in 
Lepisosteus  and  Amia.  There  is  a  single  pyloric  caecum  in  Polypterus 
(the  caeca  are  well  developed  in  sturgeons,  Lepisosteus,  and  Amid). 
The  tail  of  Polypterus  is  no  longer  markedly  heterocercal,  but  shows 
distinct  signs  of  that  condition.  We  can  even  find  a  parallel  among 
Carboniferous  palaeoniscids  for  some  of  the  special  features  of  Poly- 
pterus. The  long  body  and  dorsal  fin  are  found  in  the  fossil  *Tarrasius, 
which  may  have  been  close  to  the  ancestry  of  Polypterus,  though  it 
lacks  the  covering  of  scales.  The  pectoral  fin  in  *Tarrasius,  as  in 
Polypterus,  has  a  peculiar  lobed  form,  which  has  been  compared  with 
the  'archipterygial'  pattern  (p.  269)  and  hence  held  to  show  that 
these  animals  are  related  to  the  Crossoptergyii.  The  resemblance  is, 


234  BONY  FISHES  vm.  2- 

however,  only  superficial  and  the  plan  of  the  fin  is  essentially  actino- 
pterygian.  In  the  brain  there  is  a  thin  pallium,  thick  corpus  striatum, 
and  a  valvula  cerebelli.  The  pituitary  is  remarkable  in  that  the  hypo- 
physial sac  remains  open  to  the  mouth.  In  this  and  other  features 
(persistent  pronephros)  there  are  signs  of  neoteny. 

3.  Order  2.  Acipenseroidei 

The  sturgeons  are  a  rather  isolated  line  descending  from  the  palaeo- 
niscids  and  characterized  by  reduction  of  bone.  This  was  already 
apparent  in  the  Jurassic  *Chondrosteus.  Acipenser  and  other  modern 
sturgeons  live  in  the  sea  but  migrate  up  the  river  to  breed.  They  may 
reach  a  very  large  size  (1,000  kg)  and  since  a  tenth  of  this  is  caviar 
they  are  exceedingly  valuable.  They  feed  on  invertebrates,  which  they 
collect  from  mud  stirred  up  from  the  bottom  by  a  long  snout.  This  is 
flattened  into  a  pear-shaped  structure  in  Polyodon,  the  purely  fresh- 
water paddle  fish  of  the  Mississippi  and  in  Psephurus  in  China.  The 
mouth  of  all  sturgeons  is  small  and  the  jaws  weak  and  without  teeth. 
In  Polyodon  there  is  a  filtering  arrangement  of  gill-rakers  in  the 
pharynx.  The  jaws  of  sturgeons  hang  free  from  the  hyomandibular 
and  symplectic,  and  can  be  swung  downward  and  forward  during 
feeding.  The  skull  and  skeleton  is  almost  wholly  cartilaginous  and  the 
dermal  skeleton  much  reduced.  The  tail  is  covered  with  rhomboidal 
scales,  but  on  the  front  of  the  body  there  are  five  lines  of  bony  plates 
bearing  spines,  with  the  skin  in  between  carrying  structures  similar  to 
denticles.  There  is  an  open  spiracle.  The  internal  anatomy  of  the 
sturgeons  shows  various  features  that  have  been  held  to  show  affinity 
with  the  elasmobranchs ;  for  instance,  besides  the  spiral  valve  there  is 
a  conus  arteriosus  in  the  heart  and  a  single  pericardio-peritoneal  canal. 
However,  there  can  be  no  doubt  that  they  are  descended  from  an 
early  offshoot  from  the  actinopterygian  line.  They  retain  some  fea- 
tures lost  by  most  members  of  the  line,  but  resemble  the  Teleostei  in 
other  characters,  for  instance  a  thin  roof  to  the  cerebral  hemispheres. 

The  palaeoniscids  and  sturgeons  may  be  grouped  together  in  a 
Superorder  Chondrostci  and  placed  with  them  is  a  third  Order  Sub- 
holostei,  probably  a  mixed  group,  including  forms  that  resemble 
palaeoniscids,  but  show  various  trends  towards  the  holostean  grade 
of  organization  i*Ptycholepis). 

4.  Superorder  2.  Holostei 

During  the  later  Permian  period  the  palaeoniscids  gave  rise  to 
fishes  of  a  different  type,  which  replaced  their  ancestors  almost  com- 


viii.  4  HOLOSTEANS  235 

pletely  during  the  Triassic  and  flourished  greatly  in  the  Jurassic.  We 
may  group  together  the  fishes  of  this  type  as  Holostei  but  the  term 
is  used  variously  by  different  authors  and  includes  several  lines,  whose 
relationships  are  not  clear.  The  earliest  holostean,  *Acentrophorus 
from  the  upper  Permian,  is  much  like  a  paleoniscid  but  with  a  small 
mouth,  shorter,  deeper  body  and  slightly  upturned  tail.  This  'abbrevi- 
ated heterocercal'  tail  was  presumably  made  possible  by  the  changed 
swimming  habits  resulting  from  the  use  of  the  air-bladder  as  a  hydro- 
static organ.  If  the  fish  floats  passively  there  is  no  need  for  a  hetero- 
cercal tail  to  direct  the  head  downwards  (p.  140).  Similarly,  the  head 
does  not  need  to  be  flattened  to  produce  an  upward  lift.  The  develop- 
ment of  the  air-bladder  has  thus  made  possible  the  lateral  flattening 
and  shortening  of  the  body  so  characteristic  of  later  Actinopterygii. 
The  body  of  holosteans  was  at  first  covered  with  thick  ganoid  scales, 
but  these  became  thinner  in  later  types.  The  jaw  suspension  is 
characteristic,  the  maxilla  being  freed  from  the  pre-opercular.  As  a 
result  the  lower  jaw  could  now  be  protruded  forwards  in  front  of  the 
upper  and  a  'sucking'  action,  characteristic  of  teleosts  was  evolved, 
the  prey  being  drawn  into  the  mouth  from  a  distance  (Gardiner, 
i960).  By  a  change  in  the  insertion  of  the  adductor  mandibulae 
muscle  a  more  powerful  jaw  action  then  became  possible.  Some  of  the 
holosteans  achieved  crushing  teeth  and  replaced  the  dipnoans  in  the 
early  Mesozoic.  There  are  various  smaller  distinctive  holostean 
features,  such  as  the  loss  of  the  clavicle. 

We  do  not  know  whether  fishes  of  this  type  arose  from  a  single 
palaeoniscid  stock;  it  is  very  likely  that  the  change  occurred  several 
times,  and  that  throughout  the  Triassic  and  Jurassic  there  were 
several  lines  with  these  holostean  characteristics,  evolving  separately. 
During  the  Cretaceous  they  became  fewer,  being  replaced  by  their 
teleostean  descendants,  but  two  holosteans  survive  today,  Lepisosteus 
the  gar-pike  (often  written  Lepidosteus)  and  Amia  the  bow-fin.  These 
are  freshwater  fishes,  living  in  the  American  Great  Lakes  and  other 
parts  of  eastern  North  America,  but  the  group  is  mainly  a  marine  one, 
having  taken  to  the  sea  in  the  Trias  at  a  time  when  other  groups  were 
doing  the  same  (palaeoniscids,  coelacanths,  elasmobranchs).  The 
basic  cause  of  this  movement  is  not  known,  but  perhaps  there  was  an 
increase  of  planktonic  and  invertebrate  life  on  which  the  fish  depended. 

Lepisosteus  shows  a  rather  primitive  structure  and  must  have 
remained  at  approximately  the  Triassic  stage.  With  its  complete 
armour  of  thick  scales  (Fig.  146)  it  presents  all  the  appearance  of 
a  primitive  fish.   The  air-bladder  opens  to  the  pharynx  and  the 


236  BONY  FISHES  vm.  4- 

gar-pikes  come  to  the  surface  to  gulp  air.  On  the  other  hand,  it  has 
developed  certain  special  features,  especially  the  long  jaws,  with  which 
it  catches  other  fishes,  and  the  nearly  symmetrical  tail.  Fossils  similar 
to  the  modern  gar-pike  are  found  in  the  Eocene. 

Some  of  the  later  holosteans  became  deep-  and  short-bodied  and 
developed  a  small  mouth  with  flat  crushing  teeth  or  a  beak,  for 
instance,  *Lepidotes  (Trias  to  Cretaceous),  and  *Dapedius  (Jurassic). 
They  probably  browsed  on  corals,  like  the  modern  parrot  fishes 
(Scaridae).  *Microdon  and  other  'pycnodonts'  became  laterally 
flattened,  like  some  palaeoniscids  and  the  modern  sea  butterflies 
(Chaetodontidae). 

Another  line  of  holostean  evolution,  developing  from  the  original 
stock,  retained  the  streamlined  body  and  from  these  both  the  modern 
teleosteans  and  the  amioids  were  evolved  (Fig.  147).  *Caturus  (Trias 
to  Cretaceous)  was  covered  with  thick  scales,  but  in  *Pachycormns 
(Cretaceous)  they  are  thinner;  these  were  active  pelagic  predators. 
In  Amia  the  scales  became  reduced  to  single  bony  cycloid  scales,  as  in 
Teleostei.  Meanwhile  other  changes  took  place,  the  tail. fin  becoming 
externally  completely  symmetrical  and  the  maxilla  and  other  cheek 
bones  reduced.  Amia  has  nearly  reached  the  teleostean  stage  but 
retains  certain  primitive  features  in  the  skeleton  and  the  small  eggs 
with  holoblastic  cleavage. 

5.  Superorder  3.  Teleostei 

The  groups  so  far  considered  have  been  nearly  completely  replaced 
by  the  Teleostei,  fishes  derived  from  a  holostean  stock,  which  have 
carried  still  farther  the  tendencies  to  shortening  and  symmetry  of  the 
tail,  reduction  of  the  scales,  and  various  changes  in  the  skull,  such  as 
reduction  of  the  maxilla.  The  type  apparently  arose  in  the  sea  in  late 
Triassic  times,  but  remained  rare  until  the  Cretaceous,  by  which  time 
several  different  lines  of  evolution  had  already  begun  *Pholidophorus 
from  the  Trias  still  carried  an  armour  of  thick  scales  but  may  well 
have  given  rise  to  *Leptolepis  from  the  Jurassic  and  Cretaceous,  which 
is  generally  considered  to  be  close  to  the  ancestry  of  all  Teleostei  and 
may  be  placed  close  to  the  order  Isospondyli,  many  of  which  are 
still  alive.  *Leptolepis  was  a  long-bodied  fish  with  the  pelvic  fins  placed 
far  back,  a  skull  with  a  full  complement  of  bones,  and  a  large  maxilla. 
The  scales  still  show  traces  of  the  ganoin  layer. 

From  some  fish  like  these  leptolepids  have  been  derived  the  20,000 
or  more  species  of  bony  fish  found  today.  It  is  natural  that  in  any 
group  of  animals  that  has  evolved  relatively  recently  classification  will 


viii.  6  TELEOSTS  237 

be  difficult,  because  the  separate  twigs  of  the  evolutionary  bush  will 
show  little  difference  from  each  other  and  there  may  be  much  parallel 
evolution.  It  is  only  when  intermediate  forms  have  become  extinct 
that  clear-cut  major  groups  appear.  It  is  therefore  not  easy  to  find 
useful  subdivisions  of  Teleostei;  we  may  divide  them  among  five 
orders  but  most  classifications  require  many  more. 

The  first,  Isospondyli,  fish  with  soft  rays,  show  primitive  features 
in  the  large  maxilla,  which  forms  the  posterior  margin  of  the  upper 
jaw,  the  persistence  of  an  open  duct  to  the  air-bladder,  and  the 
posterior  position  of  the  pelvic  fins.  Fishes  of  essentially  similar  type 
are  known  as  far  back  as  the  Cretaceous  (* Port hens).  Several  familiar 
fishes  are  of  this  type,  including  the  salmon  and  trout  (Salmo)  and 
herrings  (Clupea).  The  order  Ostariophysi  is  a  large  group  of  fresh- 
water fishes,  related  to  the  Isospondyli.  The  anterior  vertebrae  are 
modified  to  form  a  chain  of  bones,  the  Weberian  ossicles,  joining  the 
swim-bladder  to  the  ear  (p.  217).  Here  belong  the  carp  and  gold- 
fish (Cyprinus),  roach  (Leucisciis),  and  cat-fishes  (Silurus).  The  eels 
(order  Apodes)  are  rather  isolated  teleosts  that  diverged  early  from 
the  main  stock  and  retain  many  primitive  features.  The  fourth  order, 
the  Mesichthyes,  includes  fishes  such  as  the  pike  (Esox)  and  stickle- 
back (G  aster  osteus)  of  structure  intermediate  between  that  of  the 
more  primitive  forms  and  the  latest  spiny-finned  teleosts.  The 
pipe-fishes  {Syngnathus)  and  sea-horses  (Hippocampus)  are  probably 
related  to  the  sticklebacks.  The  flying-fish  (Exocoetus)  also  belongs  in 
this  group. 

The  members  of  the  order  Acanthopterygii  are  the  most  highly 
developed  fishes,  characterized  by  the  stiff  spines  at  the  front  of  the 
dorsal  and  anal  fins.  The  maxilla  is  short,  the  duct  of  the  air-bladder 
is  closed,  the  body  shortened,  and  the  pelvic  fins  far  forward.  Fishes 
of  this  type  already  existed  in  the  Cretaceous  (*Hoplopteryx)  and  the 
condition  may  have  been  evolved  along  several  different  lines;  the 
group  includes  a  vast  array  of  modern  types.  Here  belong  the  perches 
(Perca),  mullet  (Mugil),  wrasse  (Labrus),  John  Dories  (Zeus),  blennies 
(Blennius)  as  well  as  the  gadid  fishes  such  as  the  whiting  (Gadus). 
Anglers  (Lophius),  gurnards  (Trigla),  and  the  flat-fishes,  the  plaice 
(Pleuronectes)  and  sole  (Solea)  and  others,  are  further  members  of 
this  very  large  order. 

6.  Analysis  of  evolution  of  the  Actinopterygii 

Our  knowledge  of  the  history  of  the  Actinopterygii  is  sufficiently 
complete  for  us  to  be  able  to  state  more  definite  conclusions  about  the 


238  BONY  FISHES  vm.  6 

process  of  evolution  than  has  been  possible  from  consideration  of  the 
more  ancient  and  less  perfectly  known  groups  of  fishes.  First  of  all 
we  may  emphasize  the  persistence  of  change.  No  actinopterygian 
fish  living  in  the  Devonian  is  to  be  found  today.  Polypterns  may  be 
regarded  as  a  living  palaeoniscid,  showing  features  that  were  common 
in  the  Carboniferous,  but  it  has  undergone  many  changes  since  that 
time.  Similarly  the  living  sturgeons  show  the  stage  of  organization 
present  in  the  Jurassic  Chondrostei,  but  they  also  have  changed  much. 
Lepisostens  is  in  general  structure  similar  to  a  Triassic  holostean  such 
as  *Lepidotes  and  Amia  to  a  Jurassic  one  such  as  *Caturus,  but  both 
have  their  own  more  recent  specializations.  It  is  not  until  we  come  to 
the  Tertiary  history  of  fishes  that  types  belonging  to  recognizable 
modern  genera  can  be  found. 

The  Actmopterygii  have  therefore  been  changing  slowly,  but  con- 
tinuously, throughout  the  period  of  their  existence.  Was  this  change 
dictated  in  some  way  by  a  change  in  their  surroundings?  Unfortu- 
nately we  cannot  answer  this  question  very  clearly.  The  sea  is  a 
relatively  constant  medium,  though  not  as  'unchanging'  as  is  some- 
times supposed.  In  particular  the  relative  extent  of  sea  and  fresh- 
water changes  frequently  and  perhaps  because  of  such  a  change  the 
early  freshwater  actinopterygians  took  to  the  sea.  Probably  the  life 
in  the  sea  is  not  constant  over  long  periods.  Almost  certainly  the 
available  nitrogen,  phosphorus,  and  other  essential  elements  change 
in  amount.  We  have  reason  to  suspect  that  there  was  an  increase  in 
the  extent  and  productivity  of  the  sea  during  the  Triassic  period.  It 
may  be  that  such  gradual  changes  in  the  life  in  the  water,  depending 
ultimately  on  climate  or  inorganic  changes,  have  been  responsible  for 
the  continual  change  of  the  fish  population.  However,  it  cannot  be 
said  that  we  can  detect  evidence  of  any  such  relationship ;  there  is  no 
clear  proof  that  the  changes  in  the  fish  populations  follow  changes  in 
the  environment.  For  the  present  we  can  only  note  the  fact  that  change 
occurs,  even  in  animals  living  in  the  relatively  constant  sea. 

Very  striking  is  the  fact  that  as  evolution  proceeds  not  merely  does 
each  genus  change  but  whole  types  disappear  and  are  replaced  by 
others.  Thus  the  palaeoniscid  type  of  organization  had  disappeared 
almost  completely  by  the  Trias  and  become  replaced  by  the  holostean. 
A  few  members  retained  the  old  organization  and  still  survive  today 
as  Polypterus  and  the  sturgeons.  Similarly  the  Holostei,  with  their 
abbreviated  heterocercal  tails,  hardly  survived  into  the  Tertiary,  but 
were  replaced  by  the  Teleostei,  only  Lepisosteas  and  Amia  remaining 
to  show  the  earlier  organization. 


(239) 


240  BONY  FISHES  vm.  6 

This  replacement  of  one  type  by  another  appears  much  more 
remarkable  when  we  reflect  that  by  a  'type',  say  the  palaeoniscid,  we 
do  not  mean  a  homogeneous  set  of  similar  organisms  all  interbreeding. 
Quite  the  contrary;  the  palaeoniscids  included  many  separate  lines, 
each  with  its  own  peculiarities.  When  one  'type'  therefore  is  thus 
replaced  by  another  it  must  mean  either  that  some  one  of  these  many 
stocks  gives  rise  to  a  specially  successful  new  population,  which  ousts 
the  old  ones  or  that  all  the  members  of  the  stock  are  changing  their 
type  together.  It  is  not  easy  with  a  record  such  as  that  of  the  fish, 
which  is  far  from  continuous,  to  say  which  of  these  is  true  in  any 
particular  case,  but  we  have  sufficient  evidence  to  be  sure  that  either 
of  them  is  possible. 

There  is  no  certain  example  in  the  Actinopterygii  of  a  single  new- 
type  replacing  all  the  former  ones,  but  the  origin  of  the  Teleostei  may 
perhaps  show  a  case  of  this  sort.  It  is  possible  that  the  Teleostei  is  a 
monophyletic  group,  arising  from  a  single  type  such  as  *Leptolepis 
and  proving  so  successful  that  nearly  all  creatures  of  previous  types 
soon  disappeared. 

The  Actinopterygii  provide  also  examples  of  the  other  and  perhaps 
even  more  interesting  process,  the  parallel  evolution  of  a  number  of 
different  lines.  There  can  be  no  doubt  that  from  Palaeozoic  times 
onwards  several  independent  lines  of  fishes  have  shown  similar 
changes.  The  tail  has  become  shorter  and  more  nearly  symmetrical, 
the  body  has  become  flattened  and  deepened  dorso-ventrally,  while 
the  pelvic  fins  have  moved  forward  and  the  scaly  armour  has  been 
reduced,  all  of  these  being  signs  of  a  more  effective  swimming  and 
steering  system  (p.  244).  As  we  come  closer  to  modern  times  and  the 
geological  record  becomes  more  complete  we  obtain  more  and  more 
critical  evidence  that  such  changes  have  occurred  in  separate  popula- 
tions. Thus  in  the  descendants  of  the  holosteans  we  can  recognize  at 
least  three  such  lines,  that  leading  to  the  round-shaped  *Microdo?i, 
another  leading  through  *Caturus  to  Amia,  and  a  third  through 
*Leptolepis  to  the  Teleostei;  probably  there  were  many  others.  The 
important  point  is  that  although  each  line  possessed  peculiar  speciali- 
zations of  its  own,  they  all  showed  some  shortening,  development  of 
symmetry  of  the  tail,  and  thinning  of  the  scales. 

It  is  a  considerable  advance  to  be  able  to  recognize  such  tendencies 
within  a  group.  We  begin  to  see  the  possibilities  of  a  general  state- 
ment on  the  matter.  Instead  of  examining  a  heterogeneous  mass  of 
creatures  called  Actinopterygii  we  can  recognize  an  initial  palaeoniscid 
type  and  state  that  in  subsequent  ages  this  has  become  changed  in 


viii.  6  EVOLUTIONARY  CHANGES  241 

certain  specified  ways  and  even  at  a  specified  rate.  Imperfect  though 
our  knowledge  still  is,  it  enables  us  to  approach  towards  the  aim  of  our 
study,  to  'have  in  mind'  all  the  fishes  of  actinopterygian  type. 

This  is  to  make  the  most  of  our  knowledge:  there  remains  a  vast 
ignorance.  We  cannot  certainly  correlate  this  tendency  of  the  fishes 
to  change  with  any  other  natural  phenomena.  Put  in  another  way, 
we  do  not  know  why  these  changes  have  occurred.  The  sea  certainly 
did  not  stay  the  same,  but  it  does  not  seem  likely  that  its  changes  have 
been  responsible  for  those  in  the  fishes.  It  would  be  very  valuable  to 
be  able  to  make  a  more  certain  pronouncement  on  this  point,  for  the 
case  is  one  of  crucial  importance.  On  land  the  conditions  are  con- 
stantly changing,  and  therefore  we  often  find  reason  to  suspect  that 
changes  in  the  animals  are  following  environmental  changes.  But 
can  this  be  so  in  the  water? 

The  evolutionary  changes  in  the  Actinopterygii  certainly  involve  a 
definite  difference  in  the  whole  life.  By  development  of  the  air- 
bladder  as  a  hydrostatic  organ  the  animals  have  become  able  to 
remain  at  rest  at  any  level  of  the  water,  and  thus,  by  suitable  modifica- 
tion of  the  shape  of  the  body  and  fins,  to  dash  about  with  remarkable 
agility  in  pursuit  of  prey  or  avoidance  of  enemies.  This  has  enabled 
them  to  dispense  with  the  heavy  armour  and  thus  further  to  increase 
their  mobility.  But  what  made  it  necessary  to  adopt  these  changes? 
Not  surely  any  actual  change  in  the  sea  itself.  We  must  look  then  for 
some  factor  imposed  on  the  situation  by  the  fishes  themselves  or  the 
neighbouring  animals  that  constituted  their  biotic  environment.  Is 
it  the  pressure  of  competition  that  has  been  responsible  for  the  change 
in  fish  form  ?  It  may  well  be  that  the  presence  of  an  excess  of  fishes 
has  led  them  continually  to  search  for  food  more  and  more  actively, 
and  in  new  places,  with  the  result  that  those  types  showing  the  greatest 
ability  have  survived.  Given  the  initial  genetic  make-up  of  the 
palaeoniscids,  further  agility  is  most  easily  acquired  by  those  fishes 
in  which  competition  tended  to  produce  shorter  tails,  thinner  scales, 
and  the  other  characteristics  towards  which  the  animals  of  this  group 
tend. 

The  fact  that  the  same  set  of  changes  can  be  produced  independently 
from  several  different  populations  of  approximately  similar  type 
(and  presumably  genetic  composition)  is  strikingly  shown  by  the 
specialized  creatures  evolved  for  life  in  coral  reefs.  Animals  with 
rounded  bodies  and  small  mouths,  sometimes  with  grinding  teeth, 
have  appeared  independently  several  times;  in  the  Carboniferous, 
*Amphicentrnm\   Permian,   *Platysomus  and    *I)oryptents;    Triassic 


242  BONY  FISHES  vm.  6 

*Cleithrolepis\  Jurassic  *Microdon  and  *Dapedius,  and  in  some  modern 
teleosteans  such  as  parrot  fishes  (Scaridae)  and  butterfly  fishes 
(Chaetodontidae).  This  is  very  valuable  evidence  of  the  way  in  which  a 
common  stimulus  can  work  on  genetical  constitutions  that  are  simi- 
lar but  not  identical.  In  this  example  the  stimulus  is  a  particular  set  of 
environmental  conditions;  in  other  cases  a  similar  effect  may  be  pro- 
duced by  the  stimulus  of  competition  between  animals,  which  was 
probably  the  'cause'  of  the  common  changes  that  affected  so  many 
descendants  of  the  palaeoniscids. 

The  history  of  these  fishes  therefore  gives  plausible  ground  for  the 
belief  that  the  driving  'forces'  that  have  produced  evolutionary  change 
are  the  tendencies  of  living  things  to  do  three  things:  (i)  to  survive 
and  maintain  themselves,  (2)  to  grow  and  reproduce,  (3)  to  vary  from 
their  ancestors,  all  of  these  operating  under  the  further  stress  of  any 
slow  change  in  the  environment. 

Finally  we  must  consider  whether  this  change  in  the  fishes  can  in 
any  way  be  considered  to  be  an  advance.  Several  times  we  have  found 
ourselves  implying  that  this  is  so,  that  the  later  teleosts  are  'higher' 
than  their  Devonian  ancestors.  We  shall  be  wise  to  suspect  this  judge- 
ment as  a  glorification  of  the  present  of  which  we  are  part.  However, 
perhaps  this  danger  is  less  marked  when  we  are  dealing  with  fishes  not 
ancestral  to  ourselves,  whose  'advance'  does  not  therefore  bring  them 
nearer  to  man.  The  judgement  can  be  put  into  quite  specific  terms: 
the  later  Actinopterygii  are  'higher'  than  the  earlier  ones  because  they 
are  more  mobile,  quicker,  and  can  live  free  in  the  water  with  lesser 
expenditure  of  energy  than  their  ancestors.  Unfortunately  we  have 
no  means  of  estimating  the  total  amount  or  biomass  of  fish  matter 
that  is  supported  by  the  teleostean  organization,  but  it  seems  possible 
that  it  is  absolutely  greater  than  that  of  any  previous  type,  say  the 
holostean  or  palaeoniscid.  If  this  is  true,  the  change  in  plan  of  struc- 
ture has  perhaps  led  to  an  increase  not  only  in  fish  biomass  but  in  the 
total  biomass  of  all  life  in  the  sea. 

The  teleostean  plan  has  certainly  allowed  for  the  development  of  a 
great  range  of  specializations,  fitting  the  animals  to  all  sorts  of  situa- 
tions in  the  sea  and  fresh  water.  We  must  therefore  not  forget  this 
adaptability  in  judging  the  status  of  the  group:  it  seems  likely  that 
modern  teleosts  are  more  varied  than  any  of  their  ancestors.  This 
power  to  enter  a  wide  range  of  habitats  not  previously  occupied  is 
perhaps  the  clearest  sign  of  all  that  a  group  has  'advanced',  and  we 
have  already  suggested  that  it  is  in  this  sense  of  suiting  animals  to 
new  modes  of  life  that  there  has  been  a  progress  in  evolution.  It  is 


vm.  6  PROGRESS  IN   FISH  EVOLUTION  243 

true  that  the  sea  and  fresh  water  have  been  in  existence  relatively 
unchanged  throughout  the  period  that  we  are  considering:  in  a  sense 
the  fishes  have  not  found  a  'new'  environment.  But  they  have  found 
endless  new  ways  of  living  in  the  water. 


IX 

THE  ADAPTIVE  RADIATION  OF  BONY  FISHES 

The  variety  of  Actinopterygii  is  so  great  that  it  would  be  impossible 
to  try  to  give  a  complete  idea  of  it  and  the  best  that  we  can  do  is  to 
consider  various  functions  in  more  detail  and  specify  some  of  the  ways 
in  which  the  animals  have  become  specially  modified. 

1 .  Swimming  and  locomotion 

The  teleosts  have  perfected  in  various  ways  the  process  of  swim- 
ming by  the  propagation  of  waves  of  contraction  along  the  body. 
The  situation  is  different  from  that  of  elasmobranchs  on  account  of 
the  presence  of  the  air-bladder,  serving  to  maintain  the  fish  steadily 
at  any  given  level  in  the  water.  The  stabilization  of  the  animal  during 
locomotion  has  therefore  become  a  wholly  different  problem,  and  the 
fins  are  correspondingly  changed.  In  the  sharks  the  pectoral  fins  serve 
to  correct  a  continual  tendency  to  forward  pitching  and  by  adjustment 
of  their  position  they  are  used  to  steer  the  animal  upwards  or  down- 
wards in  the  water. 

With  an  air-bladder  the  fishes  have  become  freed  from  the  tendency 
to  remain  at  the  bottom,  which  was  prevalent  in  the  more  primitive 
forms  and  is  still  so  common  in  sharks  that  it  has  several  times  pro- 
duced wholly  bottom-living  ray-like  types.  A  fish  with  an  air-bladder 
needs  only  very  little  fin  movement  to  maintain  it  at  a  constant  depth 
or  to  change  its  depth.  As  Harris  puts  it,  'the  elaborate  mechanism 
of  pectoral  "aerofoils"  and  a  lifting  heterocercal  tail  is  no  longer  needed 
for  the  maintenance  of  a  constant  horizontal  cruising  plane.  Con- 
comitant with  the  loss  of  the  heterocercal  tail  in  evolution  occurs  a 
rapid  and  tremendous  adaptive  radiation  of  the  pectoral  fin  in  form 
and  function.'  A  stage  in  this  process  seems  to  have  been  the  use  of 
the  paired  fins  to  produce  oscillating  movements  during  hovering, 
and  this  is  still  found  in  Amia  and  Lepisosteus,  fishes  that  remain 
relatively  slow  and  clumsy. 

Many  of  the  lower  teleosteans  are  relatively  poor  swimmers  and 
some  of  them,  like  so  many  elasmobranchs,  have  become  bottom- 
living.  Thus  in  the  catfishes  there  is  a  large  anal  fin,  acting,  like  a 
heterocercal  tail,  to  give  lift  and  negative  pitch.  The  pectoral  fins  are 
used  to  balance  this  tendency,  very  much  as  in  sharks. 


IX.   I 


FUNCTION  OF  FINS 


245 


In  the  more  specialized  teleosteans,  however,  the  pectorals  are 
placed  high  up  on  the  body  and  are  used  as  brakes  (Fig.  148).  The 
plane  of  the  fins'  expansion  is  vertical  and  they  thus  produce  a  large 
drag  force  and  a  small  lift  force.  This  lift,  of  course,  tends  to  make  the 
fish  rise  in  the  water  when  stopping,  and  there  is  also  a  pitching 


Fig.  148.  Use  of  the  paired  fins  for  braking.  A.  Forces  produced  by  the  fins  of 
Lepomis  during  deceleration.  The  pectoral  and  pelvic  fin  planes  are  represented  by 
the  heavy  lines.  P  and  V,  the  resultant  forces  on  the  pectoral  and  pelvic  fin  respectively. 
Dotted  line  and  force  P',  condition  during  action  of  pectoral  fins  only,  pelvic  fins  being 
held  in  'neutral'  position.  G,  position  of  centre  of  gravity.  B.  Sun-fish  stopping  by 
extending  pectorals.  Pelvic  fins  amputated.  Although  body  remains  horizontal,  the  fish 
rises  during  the  stop.  c.  Front  view  of  sun-fish  producing  a  rolling  moment  by  the  action 
of  one  pelvic  fin.  //  and  /,  horizontal  and  lateral  forces.  (From  Harris,^,  exp.  Biol.  15.) 


moment,  depending  on  the  position  of  the  fin  in  relation  to  the  centre 
of  gravity,  usually  positive.  That  the  fish  does  not  rise  in  the  water,  or 
pitch,  when  it  stops  is  apparently  due  to  the  anterior  position  of  the 
pelvic  fins,  so  characteristic  of  higher  Actinopterygii,  which  has 
puzzled  many  morphologists.  Experiments  on  the  sun-fish  (Lepomis) 
have  shown  that  after  amputation  of  the  pelvic  fins  the  fish  rises  in  the 
water  when  stopping  and  raises  its  head  (positive  pitch).  In  fact  the 
pelvic  fins  are  able  to  produce  a  downward  moment  and  they  tilt 
the  nose  downwards.  By  alterations  in  their  position  they  can  be  used 
to  control  the  rising  or  diving  movements  and  turning  one  of  them 
outwards  produces  rolling  (Fig.  148).  It  has  been  suggested  that  the 


246 


BONY  FISHES 


pelvic  fins  function  as  keels  to  prevent  rolling,  but  their  amputation 
in  Lepomis  does  not  produce  excessive  rolling.  Stability  in  the  trans- 
verse plane  is  presumably  assured  by  the  dorsal  and  anal  fins.  The 


Fig.  149.  Differences  in  form  of  fishes. 

A,  mackerel  (Scomber);  B,  trunk-fish  (Ostracion);  C,  sun-fish  (.Mola);  D,  globe-fish 
(Chilomycterus);  E,  sea-horse  (Hippocampus.);  f,  eel  (Anguilla).  (From  Norman.) 

use  of  the  fins  for  stopping  was  also  developed  in  some  Mesozoic 
fishes,  for  instance,  in  the  Triassic  coelacanth,  *Laugia,  which  pos- 
sessed high  pectorals,  and  pelvic  fins  in  the  anterior  position. 

In  the  fishes  with  high  pectoral  fins,  therefore,  the  pelvics  are 
usually  found  far  forward.  In  the  flying-fish  (Exocoetus),  however 
(Fig.  151),  high  pectoral  fins  are  found  with  posterior  pelvics.  In  this 
position  the   pelvics   would   tend   to   help   rather  than   hinder   any 


ix.  i  BODY  FORM  OF  FISHES  247 

tendency  by  the  pectorals  to  produce  a  rise;  the  condition  is  exactly 
that  which  would  be  expected  in  a  flying-fish. 

With  these  increased  opportunities  for  delicate  control  of  movement 
without  the  devices  of  flattening  of  the  front  part  of  the  body  and  a 
heterocercal  tail,  the  bony  fishes  have  also  been  able  to  make  many 
other  improvements  in  the  efficiency  of  their  swimming.  The  caudal 
fin  has,  of  course,  adopted  its  symmetrical  shape  and  is  used  to  increase 
the  efficiency  in  turning.  After  its  amputation  a  fish  is  not  able  to  turn 
in  its  own  length  as  normally. 

With  shortening  of  the  body  and  its  lateral  flattening  all  sorts  of 
new  factors  in  streamlining  the  body  are  developed,  but  the  details 
are  difficult  to  understand.  The  nature  of  the  turbulence  produced 
by  the  movements  of  such  a  complicated  structure  is  far  from  clear, 
but  it  seems  probable  that  the  shape  of  the  higher  fishes  is  such 
as  to  reduce  the  total  skin-friction  and  to  increase  the  efficiency  of 
swimming.  Other  factors  such  as  the  flexibility,  which  has  an  impor- 
tant influence  on  the  efficiency  of  the  propulsive  mechanism,  have 
also  been  changed,  again  in  ways  not  fully  understood,  by  the  special 
developments  of  the  vertebral  column  and  ribs.  The  speed  that  can 
be  reached  increases  with  the  length  of  the  fish.  Cruising  speeds,  which 
are  maintained  for  hours,  are  of  the  order  of  three  to  six  times  the 
body-length  per  second,  the  relationship  varying  with  the  species. 
During  sudden  bursts  the  speed  may  be  much  greater.  Thus  Bain- 
bridge  found  that  10  L/sec  could  be  maintained  only  for  one  second, 
5  L/sec  for  10  sec,  and  4  L/sec  for  20  sec  (in  dace,  goldfish,  and  trout). 

The  locomotion  of  each  type  of  fish  is  adapted  to  its  habits.  Most 
freshwater  fishes  are  'sprinters'  but  there  are  varying  degrees  of 
staying  power.  Thus  we  may  distinguish  (1)  typical  sprinters  (pike 
and  perch),  (2)  sneakers  (eel)  with  some  staying  power,  (3)  crawlers 
(rudd,  bream),  with  considerable  staying  powers  for  escape,  (4) 
stayers,  either  for  migration  (salmon)  or  for  feeding  (carp).  In  the  fish 
with  staying  powers  there  is  a  lateral  strip  of  narrow  red  muscle  fibres 
in  addition  to  the  characteristic  broad  white  fibres  of  fish  muscles. 

Bathypelagic  fishes,  living  in  deep  waters,  below  the  thermocline 
at  about  75  m,  encounter  special  problems.  Here  currents  and  tur- 
bulence are  low,  but  since  the  water  is  cold  it  is  very  viscous,  making 
swimming  difficult  but  sinking  slow.  Many  deep-sea  fishes  have 
elaborate  lures,  often  phosphorescent.  They  may  be  described  as 
'floating  fish  traps'.  They  often  have  no  swim-bladder  and  achieve 
an  almost  neutral  buoyancy  by  great  reductions  of  the  skeleton  and 
muscles  (e.g.  Ceratias).  The  only  parts  to  be  well  ossified  are  the 


248 


BONY  FISHES 


IX.  i- 


jaws.  On  the  other  hand,  deep-sea  fishes  that  retain  the  swim-bladder 
have  a  well-developed  skeleton  and  powerful  muscles  (Marshall, 
i960). 

2.  Various  body  forms  and  swimming  habits  in  teleosts 

Departures  from  the  streamlined  body  form  typical  of  pelagic  fishes 
have  been  very  numerous;  in  nearly  every  case  they  are  associated 
with  a  reduction  in  the  efficiency  of  swimming  as  such  and  the 
development  of  some  compensating  protective  mechanism  (Fig.  149). 
Lateral  flattening,  which  is  already  a  feature  of  all  teleostean  organiza- 
tion, is  carried  to  extremes  in  many  types.  Thus  the  angel-fish, 


P£5tl£!! 


Fig.  150.  The  angler-fish,  Lophius. 

Pterophyllum,  often  seen  in  aquaria,  is  provided  with  long  filaments 
and  a  brilliant  coloration,  which,  in  its  natural  habitat  (rivers  of 
South  America),  give  it  a  protective  resemblance  to  plants,  among 
which  it  slowly  moves.  The  flat-fishes  (plaice,  sole,  halibut,  &c.)  have 
carried  this  flattening  to  extreme  lengths.  They  feed  on  molluscs  and 
other  invertebrates  on  the  sea  bottom  and  lie  always  on  one  side. 
The  upper  side  becomes  darker  and  protectively  coloured,  the  lower 
side  white.  In  order  to  have  the  use  of  both  eyes  the  whole  head  is 
twisted  during  the  post-larval  period.  These  forms  are  mostly  poor 
swimmers,  but  their  coloration  gives  them  a  remarkable  protective 
resemblance  to  the  background  (p.  257). 

The  John  Dory  (Zeus  faber)  has  made  a  different  use  of  lateral 
flattening.  The  fish  is  so  thin  that  its  swimming  is  very  slow,  but 
being  inconspicuous  when  seen  from  in  front  it  can  approach  close  to 
its  prey,  which  it  then  catches  by  shooting  out  its  jaws. 

Flattening  in  the  dorso-ventral  plane  is  less  common  among  teleosts 
than  selachians.   The  flattened  forms  are  mostly  angler-fishes,   of 


ix.  2  BODY  FORM  OF  FISHES  249 

which  there  are  several  different  sorts;  Lophius piscatorins  (Fig.  150) 
is  common  in  British  waters.  It  is  much  flattened,  with  a  huge  head 
and  mouth  and  short  tail.  It  'angles'  by  means  of  a  dorsal  fin,  modified 
to  form  a  long  filament  with  a  lump  at  the  end,  which  hangs  over  the 
mouth.  Swimming,  though  vigorous,  is  slow,  and  protection  (both  for 
attack  and  defence)  is  obtained  by  sharp  spines,  protective  coloration, 
and  flaps  of  skin  down  the  sides  of  the  body,  which  break  up  the 
outline.  There  is  even  a  special  fold  of  pigmented  skin  over  the  lower 
jaw,  serving  to  cover  the  white  inside  of  the  mouth. 

Other  anglers  are  the  star-gazers,  Uranoscopiis  of  the  Mediter- 
ranean and  Astroscopes  from  the  Western  Atlantic  seaboard.  Their 
lure  is  a  red  process  attached  to  the  floor  of  the  mouth  and  they  lie  in 
wait  buried  in  the  sand,  with  the  mouth  opening  upwards  and  only 
the  eyes  showing.  The  colour  is  protective,  there  are  poison  spines, 
and  in  Astroscopus  there  are  electrical  organs  located  near  the  most 
vulnerable  spot,  the  eyes,  and  formed  from  modified  eye-muscles 

(P-  253)- 

Other  fishes  abandon  the  swift-moving  habit  for  the  protection 
afforded  by  the  development  of  heavy  armour,  such  as  that  of  the 
trunk-fish  (Ostracion)  and  the  globe-fish  (Chilomycterus)  (Fig.  149). 
Special  spinous  dorsal  rays,  such  as  those  of  the  sword-fish  {Xiphias) 
may  be  developed,  without  loss  of  the  swift-moving  habit;  indeed 
these  fish  are  among  the  fastest  swimmers.  There  are  many  groups  in 
which  an  elongated  body  form  like  that  of  the  eel  has  been  developed. 
In  Anguilla  itself  this  is  associated  with  the  habit  of  moving  over  land. 
The  Syngnathidae,  sea-horses  and  pipe-fishes,  no  longer  swim  with 
the  typical  fish  motion  but  by  passing  waves  along  the  dorsal  fins. 
The  long  and  often  grotesquely  cut-up  body  form  gives  a  strong 
protective  resemblance  to  the  weeds  among  which  they  live  and  on 
which  they  feed.  The  tail  of  the  sea-horses  has  lost  its  caudal  fin  and 
is  used  as  a  prehensile  organ,  being  wrapped  around  the  stems  of 
sea-weeds  for  attachment. 

Evidently  the  mastery  that  the  Actinopterygii  have  acquired  in  the 
water  has  depended  to  a  large  extent  on  the  freedom  given  by  the  use 
of  the  air-bladder  as  a  hydrostatic  organ.  This  gives  special  interest  to 
the  question  of  how  this  use  first  began.  If  we  are  right  in  supposing 
that  the  bladder  was  first  a  respiratory  diverticulum  of  the  pharynx, 
can  we  suppose  that  its  value  as  a  hydrostatic  organ  depended  on  any 
exertion  of  effort  of  the  fishes,  or  was  this  a  case  in  which  those  born 
with  the  organ  better  developed  found  themselves  with  an  advantage  ? 
It  would  seem  that  the  latter  orthodox  Darwinian  interpretation  is  the 


BONY  FISHES 


250  BUIM     fiStltb  IX.  2- 

more  likely;  we  can  hardly  imagine  the  fishes  striving  to  make  their 
bladders  bigger.  But  it  must  be  remembered  that  only  those  that  were 
active  swimmers,  continually  venturing  into  new  waters,  would  be 
able  to  make  full  use  of  the  new  organ. 


Fig.  151.  Various  fishes  showing  special  conditions  of  the  pectoral  fins. 

A,   eagle-ray  (Myliobatis);   B,  dog-fish  (Scyliorhimis);  c,   tunny  (Thynmis) ;   D,   thread   fin 

(Polynemus) ;   e,   sun-fish   (Lepomis);   f,   mud-skipper   (Periophtlialmus);   c,   scorpion   fish 

(Pterois);   n,   cirrhitid   fish   (Paracirrhites);   J,  flying-fish   (Exocoetus);   K,   catfish   (Doras); 

L,  gurnard  (Trigla).  (From  Norman.) 


Many  different  fishes  are  able  to  jump  out  of  the  water,  presumably 
to  escape  enemies.  Salmon  and  tarpon  can  jump  to  8  or  9  ft  above 
the  water.  The  flying-fishes  have  special  structures  to  assist  in  such 
jumps.  In  Exocoetus  (Fig.  151)  the  enlarged  pectoral  fins  serve  for 
gliding  for  distances  up  to  400  metres,  but  in  the  flying  gurnards 
(Dactylopterus)  they  are  actually  fluttered  up  and  down,  though  the 
flight  is  feeble. 

Several  types  of  fish  have  the  pectoral  fin  modified  to  allow  'walk- 
ing'. The  gurnards  (Trigld)  move  in  this  way  over  the  sea  bottom 
(Fig.  151),  and  the  mud-skipper  (Periophtlialmus)  chases  about  catch- 


ix.  3  FEEDING  HABITS  251 

ing  Crustacea  and  insects  on  land,  using  the  pectoral  fins  as  levers, 
provided  with  special  anterior  and  posterior  muscles. 

Fishes  that  live  in  situations  from  which  they  are  likely  to  be  carried 
away  develop  suckers.  Thus  in  the  gobies,  found  between  tide-marks, 
the  pelvic  fins  form  a  sucker.  The  cling-fishes  (Lepadogaster)  are  another 
group  with  the  same  habit.  The  remoras  have  developed  a  sucking- 
plate  from  the  first  dorsal  fin  and  by  means  of  this  they  attach  them- 
selves to  sharks  and  other  large  fish.  In  order  to  catch  their  food  they 
leave  the  transporting  host,  though  they  also  feed  on  its  ectoparasites. 

3.  Structure  of  mouth  and  feeding-habits  of  bony  fishes 

Although  perhaps  the  majority  of  fishes  are  carnivorous,  there  are 
species  with  all  sorts  of  other  methods  of  feeding.  The  more  active 
predators  have  strong  jaws  and  sharp  teeth,  such  as  those  of  the  pike 
(Esox),  cod  (Gadus),  and  very  many  others.  The  teeth  on  the  edge  of 
the  jaw  serve  to  bite  and  catch  the  prey,  those  on  the  walls  of  the 
pharynx  to  prevent  its  escape  if,  as  is  often  the  case,  it  is  swallowed 
whole.  The  teeth  can  often  be  first  lowered  to  allow  entrance  of  the 
prey  and  then  raised  to  prevent  its  exit  (e.g.  in  Lophius).  In  connexion 
with  this  habit  the  walls  of  the  oesophagus  and  even  stomach  are 
often  composed  of  striped  muscle,  capable  of  quick  and  powerful 
contraction. 

Many  carnivorous  fishes  are  very  fierce.  For  instance,  the  blue  fish 
(Potnatomas)  of  the  Atlantic  move  in  shoals,  cutting  up  every  fish 
they  meet,  making  a  trail  of  blood  in  the  sea.  The  barracuda  (Sphy- 
raena)  of  tropical  waters  may  attack  man.  They  are  said  to  chase 
shoals  of  fish  into  shallow  waters  and  to  keep  them  there  to  serve  for 
food  as  required. 

Other  fishes  feed  on  invertebrates  and  are  then  usually  bottom- 
feeders.  Thus  the  plaice  (Pleurojiectes)  has  developed  chisel-like  teeth 
on  the  jaws  and  flattened  crushing  teeth  in  the  pharynx;  it  feeds 
largely  on  molluscs.  The  Labridae  (wrasses)  also  have  blunt  teeth 
and  eat  molluscs  and  crabs.  The  sole  {Soled)  has  a  weaker  dentition 
and  eats  mostly  small  Crustacea  and  worms.  Fish  such  as  the  herring 
{Chipea)  that  live  on  the  minute  organisms  of  the  plankton  have  small 
teeth  and  weak  mouths,  but  are  provided  with  a  filtering  system  of 
branched  gill-rakers,  making  a  gauze-like  net,  comparable  with  the 
filtering  system  found  in  basking  sharks  (p.  181),  paddle-fish  (p.  234), 
and  whale-bone  whales  (p.  669). 

Herbivorous  and  coral-eating  fishes  have  crushing  teeth  similar  to 
those  of  the  mollusc-eaters;  indeed,  many  forms  with  such  dentition 


252  BONY  FISHES  ix.  3- 

will  take  either  form  of  food.  The  parrot-fishes  (Scaridae)  have  a  beak 
and  a  grinding  mill  of  flattened  plates  in  the  pharynx.  With  this  they 
break  up  the  corals,  rejecting  the  inorganic  part  from  the  anus  as  a 
calcareous  cloud.  The  Cyprinidae,  including  many  of  our  commonest 
freshwater  fishes  (goldfish,  carp,  perch,  and  minnow),  have  no  teeth 
on  the  edge  of  the  jaw,  hence  the  name  'leather-mouths'.  There  are, 
however,  teeth  on  the  pharyngeal  floor,  biting  against  a  horny  pad 
on  the  floor  of  the  skull.  These  fishes  are  mainly  vegetarians,  but  many 
take  mouthfuls  of  mud  and  extract  nourishment  from  the  plants  and 
invertebrates  it  contains. 

4.  Protective  mechanisms  of  bony  fishes 

In  general  teleosts  depend  for  protection  against  their  enemies  on 
swift  swimming,  powerful  jaws,  good  receptors,  and  brain.  The 
majority  of  them  have  thus  been  able  to  abandon  the  heavy  armour 
of  their  Palaeozoic  ancestors.  In  many  cases,  however,  subsidiary 
protective  mechanisms  have  been  developed,  and  are  especially  pro- 
minent in  fishes  that  have  given  up  the  fast-swimming  habit  and  taken 
either  to  moving  slowly  among  weeds  or  to  life  on  the  bottom.  These 
developments  are  a  striking  example  of  the  way  in  which,  following 
adoption  of  a  particular  mode  of  life,  appropriate  subsidiary  modifica- 
tions take  place,  presumably  by  selection  of  those  varieties  of  struc- 
ture that  are  suited  to  the  actions  of  the  animal. 

These  protective  devices  may  be  classified  as  follows : 

1.  Protective  armour  of  the  surface  of  the  body. 

2.  Sharp  spines  and  poison  glands. 

3.  Electric  organs. 

4.  Luminous  organs. 

5.  Coloration. 

5.  Scales  and  other  surface  armour 

The  typical  cycloid  teleostean  scales  have  already  been  described. 
They  form  a  covering  of  thin  overlapping  bony  plates,  providing  some 
measure  of  protection,  but  not  interfering  with  movement.  The 
hinder  edges  of  the  scales  are  sometimes  provided  with  rows  of  spines, 
and  are  then  said  to  be  ctenoid.  In  many  fishes  the  scales  bear 
upstanding  spines  and  possess  a  pulp  cavity,  which  recalls  that  of 
denticles.  In  the  tropical  globe-fishes  (or  puffers)  and  porcupine- 
fishes  (Diodon)  these  spines  are  very  long  and  sharp  and  the  puffers 
are  able  to  inflate  themselves  and  cause  the  spines  to  project  outwards, 
a  very  effective  protective  device.  In  a  few  fishes  the  scales  have 


ix.  7  SPINES  AND  POISON  GLANDS  253 

become  developed  to  form  a  bony  armour  even  more  complete  than 
that  of  the  Palaeozoic  fishes.  Thus  in  the  trunk-  or  the  coffer-fishes 
(Ostracion)  the  scales  are  enlarged  and  thickened  into  a  rigid  box, 
from  which  only  the  pectoral  fins  and  tail  emerge  as  movable  struc- 
tures, the  former  apparently  assisting  the  respiration,  the  latter  the 
swimming.  These  fishes  live  on  the  bottom  of  coral  pools  and  have 
a  narrow  beak  with  which  they  browse  on  the  polyps. 

6.  Spines  and  poison  glands 

Sharp  protective  spines  are  often  found  in  teleosts,  especially  on  the 
operculum  and  dorsal  fins.  These  may  be  provided  with  modified 
dermal  glands  that  inject  poison  into  the  wound.  Thus  the  European 
weever  (Trachinus)  lives  buried  in  the  sand  and  has  poison  spines  on 
the  operculum  and  the  dorsal  fins.  It  is  suggested  that  the  dark 
colour  of  the  fins  serves  as  a  warning.  Some  catfishes,  scorpion  fishes, 
and  toad-fishes  also  have  poison  spines.  Spines  may  be  effective  even 
if  not  poisonous;  the  stargazer,  Uranoscopus,  of  the  Mediterranean 
and  tropical  waters  has  powerful  spines  on  the  operculum,  which 
inflict  a  most  unpleasant  wound  if  the  animal  is  disturbed  by  hand 
or  foot  while  lying  in  the  sand  angling  for  its  prey  (p.  249).  Lophius, 
the  angler,  is  also  armed  with  dangerous  spines.  Several  species  of 
catfish  have  large  spines,  sometimes  serrated.  In  the  trigger-fishes 
(Balistidae  and  related  families)  of  the  tropics  one  or  more  of  the  fins 
is  modified  to  make  a  spine  that  can  be  raised  and  locked  in  that  posi- 
tion. These  fishes  have  very  brilliant  coloration,  but  since  some  of 
them  live  in  the  highly  coloured  surroundings  of  coral  reefs  it  cannot 
be  considered  certain  that  the  colours  serve  as  a  warning. 

7.  Electric  organs 

The  power  to  produce  electric  discharges  has  been  developed 
independently  in  four  distinct  families  of  teleosts,  as  well  as  in 
torpedoes  and  rays.  The  electric  organs  arise  bilaterally  from  modified 
muscle  fibres,  the  cells  of  which  are  plate-like  and  arranged  in  rows, 
the  electroplaques.  Each  plate  is  innervated  on  only  one  surface  by 
motor  neurons  whose  activity  is  controlled  from  the  forebrain,  in 
some  fish  there  is  a  controlling  nucleus  located  in  the  medulla.  The 
physiological  properties  of  transmission  at  the  nerve  endings  with  the 
electroplaques  are  similar  to  those  of  motor  end  plates.  Unlike  other 
electrogenic  tissues  such  as  muscle  or  nerve,   electric  organs  can 


254  BONY  FISHES  ix.  7- 

develop  appreciable  voltages  in  the  surrounding  fluid,  up  to  550  volts 
in  Electrophorus,  the  electric  eel  of  the  Amazon.  These  voltages  are 
achieved  by  series  summation  of  the  electromotive  forces  generated 
by  the  individual  cells. 

The  columnar  array  of  several  hundreds  or  thousands  of  electro- 
plaques  in  series  in  the  strongly  electric  fish,  Electrophorus,  Malapterurus 
and  Torpedo  are  paralleled  so  that  the  electric  organs  of  these  fish  can 
generate  considerable  current  at  high  voltage.  A  maximum  peak  power 
of  up  to  600  watts  has  been  observed  in  T.  nobiliana.  The  electric 
organs  form  the  major  part  of  the  body  of  the  strongly  electric  fish. 
The  discharges  are  used  for  offence  and  defence.  The  weakly 
electric  fish  (Gymnotidae,  Mormyridae)  have  only  a  few  columns 
of  series  arrays,  and  relatively  few  electroplaques  in  each  column. 
However,  many  of  the  species  emit  pulses  of  low  voltages  more 
or  less  continuously  and  regularly  (60-400/sec).  These  pulses  prob- 
ably serve  as  the  power  components  in  an  electrical  guidance 
system.  All  species  of  the  continuously  emitting  fish  are  sensitive  to 
changes  in  the  conductance  of  the  water.  Presumably  the  fish  sense 
the  altered  electric  field  of  their  discharges;  although  the  receptors 
have  not  yet  been  identified  specialized  lateral  line  organs  (mormyro- 
masts)  are  often  present. 

8.  Luminous  organs 

Fishes  of  many  different  families  live  at  great  depths  and  95  per 
cent  of  individuals  caught  below  100  fathoms  are  luminescent.  The 
development  of  luminescent  organs  is  therefore  a  further  example  of 
parallel  evolution.  The  organs  usually  show  as  rows  of  shining  beads 
of  various  colours  on  the  sides  and  ventral  surface  of  the  fish. 

In  many  species  the  light  is  due  to  organs  containing  luminous 
bacteria,  whose  appearance  may  be  controlled  by  the  movement  of  a 
fold  of  skin,  or  of  the  whole  organ,  or  of  chromatophores.  Some 
teleosts,  however,  have  self-luminous  photophores  and  these  are  also 
found  in  Spinax  and  a  few  other  Squalidae.  They  are  formed  from 
modified  mucous  glands,  and  may  be  provided  with  reflectors  and 
even  lenses.  They  can  be  flashed  on  and  off,  probably  by  sympathetic 
stimulation. 

The  luminous  organs  probably  often  serve  for  recognition  of  the 
sexes  and  often  show  distinctive  patterns.  They  may  serve  to  startle 
attackers  and  in  a  few  cases  to  illuminate  the  prey.  In  the  deep-sea 
anglers  (Ceratias)  the  luminous  tip  of  the  fin  is  used  as  a  lure. 


IX.  9  (255) 

9.  Colours  of  fishes 

The  bony  fishes  show  perhaps  the  most  brilliant  and  varied  colora- 
tion of  any  animals,  rivalling  even  the  Lepidoptera  and  Cephalopoda 
in  this  respect.  The  enormous  range  of  colour  and  pattern  provides 
an  excellent  example  of  the  detailed  adjustment  of  the  structure  and 
powers  of  animals  to  enable  them  to  survive.  A  great  difficulty  is 
introduced  into  the  study  of  animal  coloration  by  the  fact  that  we  are 
usually  ignorant  of  the  capacity  for  visual  discrimination  possessed 
by  the  animals  likely  to  act  as  predators.  Moreover,  it  is  very  difficult 
for  us  to  obtain  this  information.  When  we  examine  any  two  objects 
we  are  able  to  say  not  merely  that  they  are  different  but  that  one  is 
red  and  the  other  green.  A  person  or  animal  that  is  colour-blind  may 
also  be  able  to  detect  a  difference,  but  yet  remain  unaware  of  any 
distinction  of  colour;  the  objects  appear  to  him  only  as  differing  in 
brightness.  In  order  to  decide  whether  animals  are  able  to  distinguish 
between  light  of  two  wavelengths  we  must  present  them  with  objects 
of  different  colour  but  the  same  brightness. 

We  are  therefore  faced  with  the  possibility  that  some  of  the  colours 
that  appear  to  us  so  brilliant  are  to  other  animals  merely  differences  of 
tone,  and  animals  to  us  conspicuous  because  coloured,  when  seen  in 
monochrome,  may  be  protected.  Some  of  the  colours  of  fishes  may 
be  only  a  means  of  producing  a  pattern  of  protective  greys,  as  seen 
through  the  eyes  of  an  attacker.  However,  there  is  no  doubt  that  some 
fishes  are  able  to  discriminate  between  illuminated  bodies  which 
though  of  different  wavelength  reflect  light  of  equal  brightness.  In 
the  subsequent  description  of  fish  coloration  we  shall  not  be  able  to 
consider  predators  further,  but  shall  describe  the  colours  as  they 
appear  to  the  eye  of  a  normal  man. 

The  colour  of  fishes  is  produced  by  cells  in  the  dermis,  (a)  the 
chromatophores  and  (b)  the  reflecting  cells  or  iridocytes  (Fig.  152). 
The  chromatophores  are  branched  cells  containing  pigment,  which 
may  be  either  black  (melanin)  or  red,  orange,  or  yellow  (carotenoids 
or  flavines).  The  iridocytes  contain  crystals  of  guanin,  making  them 
opaque  and  able  to  reflect  light  so  as  to  produce,  where  no  chroma- 
tophores are  present,  either  a  white  or  a  silvery  appearance.  This 
material  is  used  in  the  manufacture  of  artificial  pearls,  the  scales  of  the 
cyprinoid  Alburnus  lucidus  (the  bleak)  being  used  for  the  purpose. 
The  iridocytes  may  be  either  outside  the  scales,  when  they  produce 
an  iridescent  appearance,  or  inside  them,  giving  a  layer,  the  argenteum, 
that  produces  a  dead  white  or  silvery  colour.  By  a  combination  of  the 


256  BONY  FISHES  ix.  9 

chromatophores,  and  of  these  with  the  iridocytes  to  produce  inter- 
ference effects,  a  wide  range  of  colour  is  produced.  Thus  by  mixing 
yellow  and  black  either  brown  or  green  is  produced.  Blue  is  usually 
an  interference  colour. 

The  use  of  the  colour  by  the  fish  may  be  classified,  according  to  the 
scheme  introduced  by  Poulton,  as  cryptic  or  concealing,  sematic  or 
warning  patterns,  and  epigamic  or  sex  coloration.  Cryptic  coloration 


TpT  Black  chromabophore 
^pa  Yellow  chroma tophore 
o    Iridocyte 

Fig.  152.  Coloration  elements  in  the  skin  of  the  upper  side  of 
a  flounder  (Platichthys).  (After  Norman.) 

may  be  achieved  in  various  ways  and  may  be  subdivided  into  two 
main  types:  (1)  assimilation  with  the  background,  (2)  breaking  up  the 
outline  of  the  fish.  Assimilation  is  common,  but  is  often  associated 
with  some  degree  of  disruption  of  outline.  The  absence  of  all  pig- 
mentation in  pelagic  fishes,  for  instance  the  Leptocephalus  larvae  of 
eels,  is  an  example  of  assimilation.  Fishes  living  among  weeds,  such 
as  the  sea-horses  and  pipe-fishes,  or  Lophius  the  angler,  often  resemble 
the  weeds  in  colour,  and  in  addition  develop  'leaf-like'  processes. 
The  colour  of  many  familiar  fishes,  such  as  the  green  of  the  tench, 
may  be  said  to  resemble  that  of  the  surroundings  by  assimilation. 
When  we  consider  the  much  more  numerous  examples  of  patterns 
involving  several  colours  the  distinction  between  assimilation  and  dis- 
ruption is  more  difficult  to  draw.  Many  free-swimming  pelagic  fishes 
have  the  upper  side  dark  and  striped  with  green  or  blue,  whereas  the 
under-side  is  white,  the  beautiful  pattern  that  is  seen  in  the  mackerel 
(Scombei).  This  gives  them  protection  from  above  and  below,  the 


IX.  9 


COLOUR  OF  FISHES 


257 


striping  probably  making  the  animal  less  conspicuous  in  disturbed 
water  than  it  would  be  if  of  uniform  colour.  The  white  under-side  also 
serves  to  lessen  any  shadows,  an  important  factor  for  animals  that  live 
in  shallow  water;  similar  shading  is  used  by  land  animals. 


Fig.  153.  Colour  patterns  of  various  tropical  fishes. 

A,  Muraena  {Gymnothorax);  b,  bat-fish  (Platax);  c,  butterfly  fish  (Holacanthus);  n,  butterfly 

fish  {Cliaetodon);  e,  perch  (Grammistes).  (From  Norman.) 

Devices  of  spots  and  stripes  are  found  on  fishes  that  live  against  a 
variegated  background  (Fig.  153).  The  beautiful  red  and  brown  mark- 
ings of  a  trout  are  a  good  example.  Flat  fishes,  living  on  sandy  or 
gravelly  bottoms,  adopt  a  spotted  pattern,  which  gives  them  a  high 
degree  of  protection,  and  we  shall  see  later  that  they  are  able  to  change 
colour  to  suit  the  ground  on  which  they  rest.  The  brilliant  colours 
of  many  tropical  fishes  probably  serve  mainly  to  break  up  the  outline, 
though  no  doubt  the  surroundings  in  which  they  live  are  also  brilliant. 
Great  variety  of  colours  may  be  found  on  a  single  fish,  especially  in 


258  BONY  FISHES  ix.  9- 

thc  trunk-fishes  (Ostracioti),  one  species  of  which  is  described  as 
having  a  green  body,  yellow  belly,  and  orange  tail,  while  across  the 
body  are  bands  of  brilliant  blue,  edged  with  chocolate-brown.  More- 
over, the  female  has  another  colour  scheme  and  was  for  long  con- 
sidered as  a  different  species! 

Colour  differences  between  the  sexes  are  frequent  in  fishes,  the  male 
being  usually  the  brighter.  Thus  in  the  little  millions  fish,  Lebistes, 
there  are  numerous  'races'  of  males  with  distinctive  colours,  but  the 
females  are  all  of  a  single  drab  coloration.  The  genetic  factors  that 
produce  the  various  types  of  male  are  carried  in  the  Y  chromosome. 
Presumably  the  colour  of  the  males  acts  as  an  aphrodisiac  as  a  part 
of  the  mating  display,  but  the  significance  of  the  different  races  is  not 
known. 

Sematic  or  warning  coloration  involves  the  adoption  of  some  strik- 
ing pattern  that  does  not  conceal  but  reveals  the  animal.  This  type 
of  colouring  is  found  in  animals  that  have  some  special  defence  or 
unpleasant  taste  (such  as  the  sting  of  the  wasp),  and  its  use  implies  that 
animals  likely  to  attack  are  able  to  remember  the  pattern  and  the 
unpleasant  effects  previously  associated  with  it.  It  is  not  easy  to  be 
certain  when  colours  are  used  in  this  way,  but  it  is  possible  that  the 
conspicuous  spots  on  the  electric  Torpedo  ocellata  have  this  function. 
Among  teleosts  there  is  the  black  fin  of  the  weevers  {Trachinus),  pos- 
sibly a  warning  of  their  poison  spines,  and  the  spiny  trigger-fishes 
and  globe-fishes  (p.  253)  also  have  conspicuous  colours. 

10.  Colour  change  in  teleosts 

In  spite  of  the  reputation  of  the  chameleon  the  teleosts  are  the 
vertebrates  that  change  their  colour  most  quickly  and  completely. 
The  melanophores  are  provided  with  nerve-fibres  (Fig.  154),  and 
these  cause  contraction  of  the  pigment  and  hence  a  paling  of  the  skin 
colour.  The  processes  of  the  cells  themselves  are  not  withdrawn,  the 
colour  change  is  produced  by  a  movement  of  pigment  within  them. 

The  nerve-fibres  in  question  are  post-ganglionic  sympathetic  fibres, 
leaving  the  ganglia  in  the  grey  rami  communicantes  (Fig.  139)  to  all 
the  cranial  and  spinal  nerves.  The  pre-ganglionic  fibres  that  operate 
them,  however,  emerge  only  in  a  few  segments  in  the  middle  of  the 
body  (Fig.  235),  so  that  severance  of  a  few  spinal  roots  will  affect  the 
colour  of  the  whole  body.  When  a  nerve  to  any  part  of  the  skin  is  cut 
the  chromatophores  in  that  region  at  first  expand,  making  a  dark  area 
(Fig.  155).  After  a  few  days,  however,  the  skin  involved  gradually 
becomes  lighter,  the  process,  it  is  alleged,  beginning  at  the  edges  and 


IX.   IO 


COLOUR  CHANGE 


259 


moving  inwards.  Parker,  who  has  made  a  careful  study  of  these 
phenomena,  believes  that  they  indicate  the  presence  of  melanophore- 
expanding  nerve-fibres  (said  to  be  of  'parasympathetic'  nature).  Fol- 
lowing the  cut  these  fibres  are  supposed  to  be  stimulated  to  repetitive 
discharge  and  hence  to  make  the  dark  band.  Later  the  band  pales 


Fig.  154.  Nerves  of  the  melanophores  of  a  perch.  (From  Ballowitz.) 


Fig.  155.  Diagrams  showing,  left,  a  cut  in  the  tail  of  the  fish  Funduhis  producing 

a  band  of  dark  melanophores;  right,  when  the  dark  band  has  faded  a  second  cut 

makes  the  melanophores  again  dark.  (After  Parker,  Quart.  Rev.  Biol.  13.) 

because  the  stimulating  substances  ('neurohumors')  produced  at  the 
nerve-endings  of  the  melanophore-contracting  fibres  in  the  neigh- 
bouring areas  diffuse  in  gradually. 

This  hypothesis  involves  two  physiological  propositions  which  are 
so  novel  that  they  would  require  detailed  evidence  for  acceptance. 
Firstly  the  act  of  cutting  is  presumed  to  set  up  a  discharge  of  impulses 
lasting  for  several  days,  which  is  unlikely.  Moreover,  the  discharge  is 
presumed  to  be  only  in  the  melanophore-expanding  fibres  and  not  in 
those  that  produce  contraction.  Secondly,  electrical  stimulation  of 
nerves  in  teleosts  always  produces  paling  and  never  darkening  (except 


26o  BONY  FISHES  ix.  10- 

after  the  use  of  ergotamine).  We  must  assume,  therefore,  that  this 
form  of  stimulation  has  the  opposite  effect  to  section  and  only  stimu- 
lates the  melanophore-contracting  nerve-fibres.  Since  neither  of  these 
propositions  is  adequately  demonstrated,  we  must  reject  the  hypo- 
thesis and  say  that  there  is  not  sufficient  evidence  of  melanophore- 
expanding  nerve-fibres. 

There  is,  however,  another  agent  that  causes  expansion  of  melano- 
phores  in  a  wide  variety  of  vertebrates,  namely  the  posterior  lobe  of 
the  pituitary(see  p.  206),  and  there  is  evidence  that  this  works  also  in 
teleosts.  Hypophysectomized  specimens  of  the  Atlantic  minnow 
Fiindulns  are  nearly  always  lighter  than  normal  individuals,  especially 
when  on  a  dark  background.  Injection  of  posterior  pituitary  extracts, 
or  placing  of  isolated  scales  in  the  extract,  causes  expansion  of  the 
chromatophores  of  any  teleost.  We  may  conclude  that  colour  change 
is  produced  by  the  nerve-fibres  tending  to  make  the  animals  pale  and 
secretion  of  the  posterior  pituitary  to  make  them  dark.  Adrenaline 
induces  contraction  of  chromatophores,  and  is  presumably  similar  to 
the  sympathetic  transmitter. 

It  is  more  difficult  to  decide  how  external  influences  are  linked  with 
this  internal  mechanism.  Fishes  mostly  become  pale  in  colour  on  a 
light  background  and  vice  versa,  and  the  effect  is  produced  pre- 
dominantly through  the  eyes.  There  may  also  be  a  slight  direct  effect 
of  light  on  the  chromatophores.  The  change  in  colour  begins  rapidly, 
but  its  completion  may  take  many  days.  Analysis  of  the  rates  of 
change  in  normal  fishes  and  in  those  with  anterior  and  posterior 
pituitary  removal  has  led  to  the  suggestion  that  the  anterior  lobe 
produces  a  substance  tending  to  make  the  fish  lighter  in  colour,  at 
least  in  the  eel.  A  similar  hypothesis  has  been  fully  worked  out  by 
Hogben  and  his  colleagues  in  amphibia  (p.  300).  The  colour  is  also 
influenced  by  the  pseudobranch,  a  secretory  tissue  in  the  first  gill 
arch.  After  removal  of  this  a  fish  becomes  dark  and  the  choroid  gland 
of  the  eye,  which  receives  blood  from  the  pseudobranch,  degener- 
ates. It  is  suggested  that  the  pseudobranch  produces  a  hormone, 
whose  entry  into  the  circulation  is  controlled  by  the  choroid  gland. 

The  value  of  the  colour  change  in  bringing  the  animals  to  the  same 
tint  as  their  surroundings  is  considerable.  Fishes  kept  on  a  light  back- 
ground are  very  conspicuous  for  the  first  few  minutes  when  trans- 
ferred to  a  dark  one.  The  fisherman  acknowledges  this  by  painting 
the  inside  of  his  minnow-can  white,  to  ipake  the  bait  conspicuous.  In 
the  flat  fishes,  living  on  the  sand,  the  protection  assured  by  the  colour 
change  is  of  special  importance.  It  has  been  suggested  that  it  is  pos- 


RESPIRATION 


261 


sible  for  the  fish  to  assume  a  pattern  similar  to  that  of  the  ground 
on  which  it  lies,  but  it  is  probable  that  the  degree  of  expansion  of  the 
chromatophores  is  adjusted  to  suit  the  amount  of  light  reflected  from 
the  ground;  by  increasing  or  decreasing  the  areas  of  dark  skin,  effects 
approximately  appropriate  to  various  backgrounds  are  produced. 


Fig.  156.  Special  respiratory  apparatus,  A,  in  climbing  perch  (Anabas);  b,  Indian 
catfish  (Saccobranchus);  c,  African  catfish  (Clarias).  (From  Norman.) 

11.  Aerial  respiration  and  the  air-bladder 

Many  fishes  are  able  to  live  outside  the  water.  The  excursions  on  to 
the  land  vary  from  the  wriggling  of  the  eel  through  damp  grass  to  the 
life  of  the  Indian  climbing  perch  {Anabas)  spent  almost  entirely  on 
land.  In  the  eel  there  is  no  special  apparatus  for  breathing  air  (though 
oxygen  may  be  taken  in  through  the  skin).  The  climbing  perch  is  pro- 
vided with  special  air  chambers  above  the  gills  (Fig.  156)  and  even 
when  in  water  it  comes  to  the  surface  to  gulp  air  and  will  'drown'  if 
prevented  from  doing  so,  even  though  it  is  placed  in  well-oxygenated 
water. 

Many  other  fishes  gulp  air,  especially  those  living  in  shallow  tropical 
waters,  which  readily  become  deoxygenated.  There  may  be  other 
special  mechanisms  for  gaseous  interchange.  In  the  Indian  catfish 


262 


BONY  FISHES 


IX.  11 


Saccobranchns  there  are  large  air  sacs  growing  a  long  way  down  the 
body  from  the  gill  chambers  (Fig.  156). 

The  air-bladder,  which  has  contributed  so  largely  to  the  success  of 
the  later  teleosts,  may  have  arisen  as  an  accessory  respiratory  organ, 


STURGEON  AND 
MANY  TELEOSTS 


LEPIDOSTEUS 
g=       AND  AMIA 


ERYTHRINUS 


CERATODUS 


POLYPTERUS  AND 
CALAMOICHTHYS 


LEPIDOSIREN  AND 
PROTOPTERUS 


REPTILES 

BIRDS 

MAMMALS 


Fig.  157.  Air-bladder  of  various  fishes,  seen  from  in  front  and  from  the  left  side. 

A,  air-  or  swim-bladder;  ad,  air-duct;  D,  digestive  tract.  (From  Dean,  Fishes,  Living  & 

Fossil,  The  Macmillan  Co.,  after  Wilder.) 

used  in  the  same  way  as  those  described  above.  In  all  the  more 
primitive  teleosts  (Isospondyli)  the  air-bladder  preserves  in  the  adult 
its  opening  to  the  pharynx  ('physostomatous'),  whereas  in  higher 
forms  it  becomes  completely  separated  ('physoclistous').  Survivals  of 
still  earlier  Actinopterygii  have  the  opening  especially  well  developed, 
though  it  varies  from  group  to  group  (Fig.  157).  Thus  in  the  stur- 
geons there  is  a  wide  opening  into  the  dorsal  side  of  the  pharynx. 
In  Amia  and  Lepisostens  the  opening  is  also  dorsal  and  the  walls  of 
the  sac  are  much  folded  and  used  for  respiration.  In  Polypterus 
the  opening  is  ventral  and  the  bladder  has  the  form  of  a  pair  of  lobes 
below  the  gut.  This  arrangement  recalls  that  of  the  tetrapod  lungs  and 


ix.  ii  THE  AIR-BLADDER  263 

is  also  found  in  the  modern  lung- fishes  and  presumably  in  their 
Devonian  ancestors, from  which  we  may  suppose  that  the  tetrapods 
arose  (p.  276).  This  ventral  position  of  the  air-bladder  was  one  of  the 
features  that  for  a  long  time  led  zoologists  to  suppose  that  Polypteriis 

A  B 


Fig.  158.  Diagrams  illustrating  the  blood-supply  of  the  air-bladder  in  A,  Polypterus, 
b,  Ceratodus,  c,  Aviia,  and  d,  a  teleost.  The  blood-vessels  are  seen  from  behind,  and 

cut  short  in  transverse  section. 
a.  dorsal  aorta;  aad.  anterior  dorsal  artery  from  the  coeliac;  aav.  ant.  ventral  artery; 
ab.  air-bladder;  aid.  anterior  dorsal  vein  to  the  cardinal;  bar\  4th  aortic  arch  (6th  of  the 
series);  d.  ductus  Cuvieri;  ev.  coeliac  artery;  la.  left  pulmonary  artery;  oe.  oesophagus; 
pr.  portal  vein  receiving  posterior  vein  from  air-bladder;  ra.  rii^ht  'pulmonary'  artery ;  rpv. 
right  (branch  of)  'pulmonary''  vein;  rv.  right  vein  from  air-bladder;  v.  left  'pulmonary' 
vein.  (From  Goodrich,  Vertebrata,  A.  &  C.  Black,  Ltd.) 

was  a  member  of  the  crossopterygian  line  of  fishes.  It  is  probable, 
however,  that  the  affinity  is  only  that  which  persists  between  all 
primitive  members  of  both  Actinopterygii  and  Crossopterygii  and 
is  to  be  taken  as  an  indication  that  the  air-bladder  was  originally  a 
widely  open  respiratory  sac,  or  perhaps  pair  of  sacs.  Once  the  power 
to  produce  a  pharyngeal  diverticulum  had  been  developed  it  is  easy 
to  imagine  that  the  actual  position  of  the  opening  might  shift  either 
dorsally,  as  in  the  later  Actinopterygii,  or  ventrally,  as  in  the  tetrapods. 
The  blood-supply  of  the  air-bladder  should  provide  some  indica- 
tions both  of  its  origin  and  function.  In  Polypterus  and  Dipnoi  there 
are  pulmonary  arteries  springing  from  the  last  (sixth)  branchial  arch 


264  BONY  FISHES  ix.  n- 

and  presumably  containing  venous  blood  (Fig.  158).  Blood  returns 
to  the  heart  by  pulmonary  veins.  Essentially  the  same  arrangement 
is  found  in  Amia,  but  in  all  other  Actinopterygii  oxygenated  blood  is 
supplied  to  the  bladder  from  the  dorsal  aorta  (or  sometimes  from  the 
coeliac  artery).  Probably,  then,  the  original  function  of  the  air-bladder 
was  respiratory,  and  this  may  still  be  its  main  function  not  only  in 
Amia  and  Lepisosteus  but  also  in  some  of  the  physostomatous  Tele- 
ostei.  However,  in  the  majority  of  teleosts  its  dorsal  position,  closed 
duct,  and  arterial  blood-supply  show  that  it  has  some  other  function 
and  it  has  long  been  supposed  that  this  is  concerned  in  some  way  with 
flotation.  The  air-bladder  is  absent  from  bottom-living  forms,  such 
as  flat-fishes,  Lophius  and  Uranoscopus,  though  it  may  be  present  in 
their  pelagic  larvae. 

The  bladder  is  provided  with  special  glands  by  which  it  is  filled 
and  the  gas  they  secrete  is  mostly  oxygen;  only  in  some  physosto- 
matous forms  is  the  bladder  filled  by  gulping  air.  Nitrogen  and  carbon 
dioxide  are  also  present  and  the  former  even  constitutes  the  main  gas 
in  some  freshwater  fishes  at  great  depths.  In  the  more  primitive  forms 
gas  is  secreted  all  over  the  surface  of  the  bladder,  but  later  there 
develop  special  anterior  oxygen-secreting  and  posterior  oxygen- 
absorbing  regions.  The  former,  known  as  the  red  gland,  has  a  special 
apparatus  of  blood-vessels,  the  rete  mirabile,  and  the  latter,  or  'oval', 
which  may  be  developed  from  the  closed  end  of  the  pneumatic  duct, 
has  a  special  sphincter  by  means  of  which  it  can  be  closed  off. 

The  pressure  of  the  gases  in  the  swim-bladder  is  adjusted  to  make 
the  fish  neutrally  buoyant,  which  is  achieved  when  the  bladder 
occupies  7-10  per  cent  of  the  total  volume  in  fresh-water  and  5  per 
cent  in  marine  fishes.  This  may  involve  partial  pressures  of  oxygen, 
carbon  dioxide,  and  nitrogen  many  times  greater  than  those  in  the 
blood.  The  mechanism  by  which  the  gases  are  secreted  against  a 
diffusion  gradient  of  several  atmospheres  has  been  much  discussed. 
Carbonic  anhydrase  is  present  in  the  gas  gland  and  the  oxyhemo- 
globin of  fish  blood  is  especially  sensitive  to  carbon  dioxide,  giving  up 
its  oxygen  even  at  high  oxygen  concentration. 

If  weights  or  floats  are  attached  to  a  fish  it  maintains  its  position 
in  mid-water  by  swimming  while  gas  is  secreted  or  absorbed.  The 
receptors  concerned  are  therefore  not  activated  by  the  tension  in  the 
bladder  but  perhaps  by  the  movements  that  are  necessary  when  the 
fish  is  not  in  equilibrium.  The  bladder  is  innervated  by  the  vagus  and 
sympathetic  nerves  and  after  severing  the  former  gas  secretion  ceases. 

The  various  diverticula  connecting  the  bladder  with  the  ear  (and 


IX.   12 


REPRODUCTION 


265 


the  Weberian  ossicles,  p.  217)  may  be  associated  with  pressure  recep- 
tors that  assist  in  the  control  of  the  bladder.  Loaches  are  famous  as 
fish  barometers,  whose  behaviour  can  be  used  to  predict  weather 
changes. 

12.  Special  reproductive  mechanisms  in  teleosts 

The  teleosts  show  great  variation  in  breeding  habits,  the  eggs  being 
sometimes  left  to  develop  entirely  by  themselves,  in  other  cases  looked 
after  by  one  or  both  parents,  while  in  a  few  species  they  develop 


Fig.  159.  Deep-sea  fish  Photocorynus  with  parasite  male  attached.  (From  Norman.) 

viviparously  within  the  mother.  Hermaphrodite  individuals  are  not 
uncommon  and  in  some  species  of  Sparidae  and  Serranidae  are 
invariably  monoecius  and  self-fertilizing.  The  method  of  association 
of  the  sexes  is  correspondingly  varied  and  there  are  numerous  devices 
for  bringing  sexes  together,  such  as  colour  differences,  sound  produc- 
tion, and  the  liberation  of  stimulating  substances  into  the  water.  In 
some  deep-sea  fishes  the  male  is  much  smaller  than  the  female,  to 
which  it  remains  permanently  attached  (Fig.  159).  Breeding  is  often 
preceded  by  a  migration  of  the  fishes  to  suitable  situations  and  the 
association  into  large  shoals. 

The  eggs  may  be  classified  as  either  pelagic,  if  they  float,  or  demersal, 
if  they  sink  to  the  bottom.  In  the  former  case  they  are  sometimes  pro- 
vided with  an  oil  globule  and  are  exceedingly  numerous.  Thus  a 
single  female  turbot  has  been  calculated  to  contain  nearly  10  million 
eggs,  a  cod  7  million,  and  a  ling  28  million,  whereas  the  herring, 
whose  eggs  sink  to  the  bottom,  probably  does  not  lay  more  than 


266  BONY  FISHES  ix.  12 

50,000  eggs.  The  large  numbers  laid  by  the  pelagic  species  are  pre- 
sumably an  insurance  against  failure  of  fertilization  and  especially 
against  random  elimination  of  the  eggs  and  young.  The  greater  the 
care  devoted  to  the  young  by  the  parents  the  smaller  the  number  of 
eggs  produced  (see,  however,  p.  283). 

Demersal  eggs,  especially  of  freshwater  animals,  are  usually  laid 
with  some  special  sticky  covering,  by  means  of  which  they  are 
attached  to  each  other  and  to  the  bottom  or  to  stones,  weeds,  &c. 
Thus  the  eggs  of  many  cyprinids  (carp,  &c.)  are  attached  to  weeds. 
The  eggs  of  salmon  and  trout,  however,  though  demersal,  are  not 
sticky.  From  depositing  eggs  on  weeds  it  is  only  a  short  step  to  the 
building  of  a  nest  and  guarding  of  the  eggs  by  one  or  both  parents. 
Thus  the  sand  goby  (Gobius  minutus)  lays  its  eggs  in  some  protected 
spot,  where  they  are  guarded  by  the  male,  who  aerates  them  by  his 
movements.  Quite  elaborate  nests  may  be  built,  as  by  the  sticklebacks 
(Gasterosteus),  where  pairs  remain  together  throughout  the  breeding- 
season.  A  still  further  development  is  the  retention  of  the  young 
within  the  body.  In  some  catfishes  they  develop  within  the  mouth  of 
either  parent.  In  pipe-fishes  and  sea-horses  the  males  are  provided 
with  special  pouches  for  the  young. 

Although  external  fertilization  is  usual,  various  teleosts  show 
internal  fertilization  and  the  young  then  develop  within  the  ovary 
(Zoarces,  Gambnsia,  Lebistes).  The  mechanisms  by  which  mating  and 
the  nutrition  of  the  embryos  are  assured  in  these  cases  show  some 
interesting  parallels  with  the  conditions  in  mammals,  including  the 
formation  of  placentae  or  nutritive  material.  In  Lebistes  the  female 
adopts  a  special  position  of  readiness  for  copulation,  and  this  has  been 
shown  to  depend  partly  on  an  internal  factor  in  the  female  and  partly 
on  a  substance  secreted  into  the  water  by  the  male.  The  embryos  are 
not  attached  to  the  wall  of  the  ovary  but  develop  free  in  the  sac,  feed- 
ing upon  an  'embryotrophic'  material,  apparently  produced  by  the 
discharged  ovarian  follicles,  which  become  highly  vascular  and  remain 
throughout  the  several  months  of  'pregnancy'. 

Rhodeus  amarus,  the  bitterling  (Cyprinidae),  shows  somewhat 
similar  conditions  (Fig.  160).  Association  of  the  sexes  at  mating  is 
here  made  necessary  by  the  fact  that  the  eggs  are  laid  within  the 
siphon  of  a  swan  mussel.  For  this  purpose  the  cloaca  of  the  female 
develops  into  a  tubular  ovipositor.  This  development  takes  place 
under  the  influence  of  a  hormone  produced  by  the  ovary.  Addition  of 
progesterone  and  related  substances  to  the  water  containing  the  fish 
causes  growth  of  the  ovipositor. 


REPRODUCTION 


267 


The  full  growth  of  the  ovipositor  and  preparation  of  the  female  for 
spawning  depends  on  the  presence  in  the  water  of  the  male  and  also 
of  the  swan  mussel.  Water  in  which  males  have  been  kept  stimulates 
growth  of  the  ovipositor.  When  the  female  is  ready  to  deposit  the  eggs 
she  adopts  a  vertical  position  in  the  water  and  the  spawning  male,  in 


&ii?9£z&*i 


Fig.  160.  Male  and  female  bitterling  (Rhodeits)  with  swan  mussel 
in  which  eggs  are  about  to  be  deposited.  (From  Norman.) 

full  nuptial  coloration,  swims  around  her.  An  egg  passes  into  the 
oviduct  and  erection  of  the  ovipositor  is  produced  by  pressure  of  the 
urine,  produced  by  contraction  of  the  walls  of  the  urinary  bladder,  the 
exit  being  blocked  by  the  egg.  The  extended  ovipositor  is  thus  able 
to  place  the  egg  within  the  siphon  of  the  mussel  and  the  male  then 
immediately  thereafter  sheds  his  sperms  over  the  opening  and  they 
are  presumably  carried  in  by  the  current.  The  whole  process  shows 
the  elaborate  interplay  of  internal  devices  and  external  stimuli  neces- 
sary for  the  perfection  of  this  remarkable  method  of  caring  for  the 
young.  Yet  the  various  features  are  all  developments  of  systems  found 
in  other  vertebrates. 


X 

LUNG-FISHES 

1.  Classification 

Class  Crossopterygii 
Order  i.  Rhipidistia.  Devonian-Recent. 

Suborder  i.  *Osteolepidoti.  Devonian-Carboniferous 

*Osteolepis;  *Sauripterus;  *Diplopterax;  *Eiisthenopteron 
Suborder  2.  Coelacanthini  (=  Actinistia).  Devonian-Recent 
*Coelacanthus;  *Undina;  Latimeria 
Order  2.  Dipnoi.  Devonian-Recent. 

*Dipterus;  *Ceratodns;  Neoceratodas;  Protopterus;  Lepidosiren 

2.  Crossopterygians 

Although  the  lung-fishes  and  their  allies  are  here  considered  last  of 
all  the  groups  of  fishes,  because  they  lead  on  to  the  amphibia,  it  is 
important  to  realize  that  in  many  features  they  stand  close  to  the 
ancestral  stock  of  gnathostomes.  It  is  a  mistake  to  consider  them  as 
'higher'  animals  than,  say,  the  elasmobranchs  or  actinopterygians. 
Only  four  genera  belonging  to  this  group  are  found  at  the  present 
time,  Neoceratodus,  Lepidosiren,  Protopterus,  the  lung-fishes  of  Aus- 
tralia, South  America,  and  Africa  respectively,  and  Latimeria,  recently 
discovered  off  the  east  coast  of  South  Africa  and  the  Comoro  Islands 
off  Madagascar.  These  are  relics  of  a  group  that  can  be  traced  back 
with  relatively  little  change  to  the  Devonian,  and  there  is  little  doubt 
that  at  about  that  period  the  first  amphibia  arose  from  some  similar 
line.  The  characters  of  the  modern  crossopterygians  are  therefore  of 
extraordinary  interest,  because  they  show  an  approach  to  the  condition 
of  the  ancestors  of  all  tetrapods. 

3.  Osteolepids 

Osteolepis  itself  (Fig.  161),  from  the  middle  Devonian,  was  the 
earliest  and  most  primitive  member  of  the  group.  In  appearance  it 
shows  an  obvious  similarity  both  to  palaeoniscids  and  to  early  Dipnoi 
and  it  was  probably  close  to  the  line  of  descent  from  some  placoderm 
ancestor  to  both  of  these  groups  and  to  the  amphibia.  The  body  was 
long  and  the  tail  heterocercal.  A  feature  distinguishing  all  early  Cros- 
sopterygii from  early  Actinoptergyii  was  the  presence  of  two  dorsal 


x.  1-3  OSTEOLEPIDS  269 

fins  in  the  former.  The  paired  fins  have  a  characteristic  scaly  lobed 
form,  from  which  the  group  derives  its  name,  and  the  skeleton  of  the 
pectoral  fin  contained  a  basal  element  attached  to  the  girdle  and  a 
branching  arrangement  at  the  tip  (Fig.  180).  This  plan  is  distinctively 
different  from  that  of  the  rayed  fin  of  the  Actinopterygii,  but  could 
also  easily  have  led  to  the  evolution  of  a  tetrapod  limb  (p.  307). 

The  body  was  covered  with  thick,  pitted  rhomboidal  scales,  with  an 
appearance  very  similar  to  that  of  the  palaeoniscid  scale.  These  scales 
have,  however,  a  characteristic  structure  known  as  cosmoid.  Each  scale 
(Fig.  145)  may  be  considered  as  composed  of  an  upper  layer  of  dentine 
(the  cosmine),  with  a  hard  covering  of  shiny  vitrodentine,  possibly  com- 
parable with  enamel.  Below  the  cosmine  is  a  'vascular  layer'  consisting 
of  pulp  cavities  in  which  lay  odontoblasts  whose  processes  made  the 
dentine.  This  layer  in  turn  rests  on  a  bony  layer  of  isopedin.  The  struc- 
ture appears  to  have  some  relation  to  that  of  placoid  scales  and  no 
doubt  the  morphogenetic  processes  that  give  rise  to  the  isolated  pulp 
cavities  of  placoid  scales  are  similar  to  those  that  produce  the  cosmoid 
plates.  It  is  usual  to  suggest  that  the  latter  are  formed  of  'fused  den- 
ticles', but  this  is  of  course  only  a  manner  of  speaking.  Denticles  do 
not  fuse,  but  morphogenetic  processes  may  occur  in  such  a  way  as  to 
produce  flat  plates  of  dentine.  Indeed,  it  is  possible  that  the  evolution 
occurred  in  the  other  direction,  that  is  to  say  that  the  placoid  scale 
is  a  special  case  of  the  cosmoid.  The  condition  in  which  a  substance  is 
formed  nearly  uniformly  all  over  the  surface  of  the  body  is  a  more 
general  one  than  that  in  which  such  formation  occurs  only  in  isolated 
areas.  Indeed,  the  discontinuous  arrangement  is  a  very  remarkable 
condition,  for  which  we  have  at  present  no  explanation.  The  relation- 
ship of  the  cosmoid  to  the  ganoid  scale  of  early  Actinopterygii  is  not 
quite  clear,  but  the  ganoid  type  seems  to  show  a  reduction  of  the 
pulp  cavities  and  development  of  the  shiny  surface-layer.  The  early 
Dipnoi  of  the  Devonian  possessed  cosmoid  scales.  In  later  osteolepids 
and  Dipnoi  there  has  been  a  thinning  of  the  scales,  as  among  the 
Actinopterygii,  so  that  the  later  Dipnoi  are  covered  with  thin,  over- 
lapping, 'cycloid'  scales. 

The  skull  of  osteolepids  (Fig.  161)  was  well  ossified;  there  was  a 
series  of  bony  plates  arranged  according  to  a  pattern  with  a  general 
similarity  to  that  of  palaeoniscids  (p.  230)  and  which  might  well  have 
been  ancestral  to  that  of  amphibia.  There  was,  however,  a  joint  across 
the  top  of  the  skull  between  the  parietal  and  post-parietal  bones,  and 
an  unossified  gap  in  the  base  of  the  skull.  A  movable  joint  at  this  level 
persists  in  the  living  coelacanth  (p.  272). 


270 


LUNG-FISHES 


x.  3- 


A  most  important  feature,  common  to  all  crossopterygians,  was 
that  the  attachment  of  the  jaws  was  autostylic,  that  is  to  say,  similar 
to  the  arrangement  in  amphibia  and  remotely  similar  to  the  earliest 
gnathostomes  (aphetohyoids)  but  different  from  that  of  modern  elas- 


qj.      pop. 

Fig.  161.  Skull  of  Osteolepis. 

d.  dentary;  en.  external  nostril;  esc.  extrascapulars;  gu.  gular;/.  jugal;  la.  lachrymal;  1-gu. 
lateral  gular;  fngu.  median  gular;  mx.  maxilla;  op.  opercular;  pa.  parietal;  pm.  premaxilla; 
po.  postorbital;  pop.  preopercular;  ppa.  postparietal;  prf.  prefrontal;  qj.  quadratojugal; 
sop.  subopercular;  sq.  squamosal;  sut.  supratemporal;  ta.  tabular.  (After  Save-Soderbergh 
and  Westoll,  Biol.  Rev.  1943.) 

mobranchs  and  actinopterygians.  The  teeth  of  osteolepids  were  simple 
cones,  not  flattened  plates  such  as  are  characteristic  of  Dipnoi,  but  the 
teeth  on  the  palate  show  a  somewhat  broad  folded  surface  and  each 
tooth  is  replaced  by  another  growing  up  near  it,  both  of  these  being 
features  found  in  the  earliest  amphibia.  Sections  of  the  teeth  show  a 
peculiar  infolding  of  the  enamel  to  make  a  labyrinthine  structure, 
which  is  not  found  in  other  fishes  but  is  characteristic  of  the  teeth  of 
the  first  amphibians  (p.  327). 

There  was  only  one  pair  of  nostrils  on  the  surface  of  the  head  and 
there  are  gaps,  which  are  considered  to  be  internal  nostrils,  at  the  front 


x.  4  COELACANTIIS  271 

end  of  the  palate,  bordered  by  the  premaxillae,  maxillae,  palatines,  and 
prevomers.  These  fishes  may  have  breathed  air;  they  certainly  also 
possessed  gills,  covered  with  an  operculum. 

Animals  of  this  sort  seem  to  have  been  abundant  in  Devonian 
waters  and  by  the  end  of  that  period  had  diverged  into  several  different 
lines.  It  is  interesting  that  the  tendencies  shown  by  these  lines  arc- 
similar  to  those  that  we  discovered  in  the  evolution  of  the  Actino- 
pterygii.  Some  of  the  later  osteolepids  became  shorter  in  body,  the 
tails  tended  to  become  symmetrical  (diphycercal)  and  the  scales  to 


Fig.  162.  Coelacanth,  Latimeria  chalumnae,  female.  Length  142  cm.  Caught  1954 
near  Anjouan.  (After  Grasse.) 

become  thinner  and  overlapping.  *Dip!opterax  and  *Eiistheiiopteron 
represent  separate  lines  from  the  late  Devonian,  both  showing  these 
characters.  Probably  the  development  of  these  features  depends  on 
the  use  of  the  air-bladder  as  a  hydrostatic  organ  and  the  associated 
changes  in  the  method  of  swimming. 


4.  Coelacanths 

The  osteolepids  became  rare  in  the  Carboniferous  and  disappeared 
after  the  early  Permian,  but  a  line  descended  directly  from  them 
remained  common  through  the  Mesozoic  and  still  survives  today. 
These  coelacanths  (Fig.  162)  show  certain  very  characteristic  features, 
which  enabled  the  strange  fish  brought  to  the  museum  at  East 
London,  South  Africa,  to  be  recognized  immediately  as  belonging  to 
the  group.  They  are  rather  deep-bodied  animals,  with  a  characteristic 
three-lobed  diphycercal  tail.  The  type  first  appeared  in  the  late 
Devonian  and  was  obviously  derived  from  osteolepid  ancestry  having 
two  dorsal  fins,  diphycercal  tail,  lobed  fins,  and  a  rhipidistian  pattern 
of  skull  bones,  including  in  most  forms  a  fronto-parietal  joint.  There 
was  a  calcified  air-bladder.  *CoelacantJius  and  other  Carboniferous 


272  LUNG-FISHES  x.  4- 

forms  lived  in  fresh  water,  but  *Undina  and  other  Jurassic  and  Creta- 
ceous types  lived  in  the  sea. 

The  first  living  specimen  of  the  group  was  fished  off  the  east  coast 
of  South  Africa  and  eleven  others  have  since  been  caught  around  the 
Comoro  Islands  (Madagascar)  (Fig.  162).  All  are  referred  to  the  genus 
Latimeria.  They  have  been  caught  near  the  bottom  at  considerable 
depths  (150-400  m).  Unlike  most  of  their  fossil  ancestors  they  are 
large  fishes,  weighing  up  to  80  kg;  they  are  dull  blue  in  colour.  The 
whole  body  is  covered  with  heavy  cosmoid  scales. 

The  notochord  is  a  massive  unconstricted  rod.  The  skull  possesses 
a  well-marked  joint  between  a  condyle  on  the  hind  end  of  the  basi- 
sphenoid  and  a  glenoid  cavity  on  the  front  of  the  base  of  the  oto- 
occipital  region.  This  joint,  together  with  fibrous  unions  between 
other  bones  allows  of  movement  of  the  front  part  of  the  head  on  the 
hind.  A  large  pair  of  muscles  runs  from  the  parasphenoid  up  and 
back  to  the  pro-otic  and  serves  to  raise  the  front  part  of  the  head  on 
the  hind.  Coraco-mandibular  muscles  attached  to  the  palato-quadrate 
have  the  reverse  action  and  the  movement  is  presumably  concerned 
with  catching  the  prey.  There  are  numerous  small  teeth  on  the  jaws 
and  palate.  Latimeria  lives  on  other  fishes,  apparently  swallowed  whole 
by  the  powerful  oesophagus.  There  is  a  well-developed  spiral  intes- 
tine. 

The  'air-bladder'  arises  by  a  ventral  opening  from  the  oesophagus 
and  proceeds  backwards  and  dorsally  for  the  whole  length  of  the 
abdominal  cavity.  The  lumen  is  very  small  and  the  organ  is  95  per 
cent  fat.  It  may  serve  to  reduce  the  specific  gravity.  Respiration  is  by 
the  gills.  The  heart  shows  a  linear  'embryonic'  condition,  with  the 
sinus  venosus  and  auricle  behind  the  ventricle.  There  are  four  rows  of 
valves  in  the  conus.  The  red  cells  are  large,  as  in  elasmobranchs, 
Dipnoi,  and  Amphibia.  Nothing  is  known  of  the  development, 
except  that  the  eggs  are  large. 

The  brain  lies  far  back  in  the  cranium,  of  which  it  occupies  less 
than  one-hundredth  part,  the  rest  being  filled  with  fat.  Its  structure 
is  somewhat  like  that  of  a  teleostean,  with  a  thin  fore-brain  roof,  and 
large  striatum,  but  without  eversion.  There  is  no  valvula  to  the  cere- 
bellum. The  pituitary  cleft  is  large  and  the  gland  remains  in  continuity 
with  the  roof  of  the  mouth. 

There  are  anterior  and  posterior  nares  but  both  open  on  the  surface 
of  the  head  and  they  have  nothing  to  do  with  respiration.  The  rostral 
organ  is  a  large  median  sac  opening  to  the  surface  by  three  pairs  of 
canals  and  richly  innervated  by  the  superficial  ophthalmic  nerve. 


x.  5  FOSSIL  DIPNOI  273 

A  similar  sac  occurs  in  fossil  coelacanths  back  to  the  Devonian  but  its 
function  is  quite  unknown.  The  eye,  inner-ear,  and  lateral  line  system 
are  well  developed. 

It  is  hard  to  see  what  features  have  enabled  Latimeria  to  survive 
with  little  change  since  the  Jurassic  or  earlier  (see  p.  771).  It  clearly 
cannot  be  by  special  development  of  the  brain  or  receptors.  Its 
habitat  is  isolated,  but  not  especially  protected  and  its  population 
seems  to  be  small  since  even  by  exceptional  efforts  so  few  specimens 
have  been  found.  Perhaps  they  are  more  numerous  in  deeper  waters. 
In  some  of  its  features  it  shows  developments  parallel  to  those  of  the 
Teleostei  rather  than  to  the  Dipnoi,  whose  remote  ancestry  it  shares. 
Several  of  its  characteristics  are  paedomorphic.  These  can  hardly  be 
alone  responsible  for  such  a  long  survival,  but  some  of  them  also 
appear  in  the  other  survivors  from  the  Paleozoic,  Polypterus,  stur- 
geons, and  Dipnoi. 

5.  Fossil  Dipnoi 

The  Devonian  Dipnoi  were  more  like  their  osteolepid  relatives  than 
are  the  surviving  modern  forms  (Fig.  163).  The  early  members  of  this 
group,  such  as  *Dipterns  (Fig.  211),  showed  the  typical  elongated 
body,  thick  cosmoid  scales,  heterocercal  tail,  lobed  fins,  and  well- 
ossified  skull.  The  pattern  of  the  bones  was  obscured  by  a  seasonal 
deposit  of  cosmine,  this  being  periodically  absorbed  to  allow  of  growth. 

The  individual  bones  have  a  certain  similarity  to  those  of  osteolepids, 
but  there  are  extra  bones  that  are  difficult  to  name.  There  was  no 
premaxilla  or  maxilla,  nor  any  teeth  along  the  edge  of  the  jaw;  instead 
broad,  ridged  tooth-plates  were  developed  on  the  palate  and  inside 
of  the  lower  jaw,  presumably  as  an  adaptation  for  eating  molluscs 
and  other  invertebrates.  These  crushing-plates  are  characteristic  of 
the  Dipnoi  and  preclude  even  the  earliest  of  them  from  being  the 
actual  ancestors  of  the  amphibia.  By  the  end  of  the  Devonian  the 
Dipnoi  were  showing  changes  similar  to  those  of  the  osteolepids  and 
palaeoniscids.  The  body  became  shorter,  the  first  dorsal  fin  dis- 
appeared, the  tail  became  diphycercal,  and  the  scales  lost  their  shiny 
surface-layer  and  became  thin.  The  teeth  of  *Ceratodus  appear  in  the 
Triassic  and  were  known  to  geologists  long  before  the  related  living 
animal  was  discovered.  There  has  been  very  little  change  in  this 
animal  in  more  than  150  million  years,  though  the  recent  members  are 
placed  in  a  distinct  genus  Neoceratodns. 

The  evolution  of  Dipnoi  is  especially  interesting  because  the  rate 
of  change  has  actually  been  measured  (Westoll,  1949).  Twenty-six 


(274) 


&£? ->'■#?£'? 


Fig.  163.  The  three  living  lung-fishes  and  their  distribution. 
A,  Protopterus;  b,  Lepidosiren;  c,  Neoceratodns.  (From  Norman.) 


90 

80 

^r  • 

70 

60 

50 

T 

£  40 
0 

1 

^30 

f 

20 

J 

10 

j    1 

1                          1                          L 

1                          ' 

I 

350 


250 


150 


Age  / Millions  of  years) 


Fig.  164.  Rate  of  evolution  in  lung-fishes.  Each  point  represents  the  index  of  a  single 
genus  obtained  by  taking  twenty-six  characters  and  rating  them  with  grades  of  struc- 
ture. The  lowest  value  was  given  for  the  most  primitive  condition,  the  highest  for  the 
most  modern  one.  (After  Westoll  and  Simpson.) 


x.  5~6 


MODERN  LUNG-FISHES 


275 


different  characteristics  such  as  proportion  of  skull,  nature  of  dermal 
bones  or  dentition  were  divided  into  3-8  grades.  Each  fossil  genus 
was  thus  given  a  score,  the  minimum  being  for  characters  appearing 
in  the  oldest  lung-fish,  the  hypothetical  ancestor  being  o.  Actual 
scores  ranged  from  4  for  the  earliest  to  100  for  two  of  the  living  genera. 
Plotting  against  time  we  see  that  there  was  an  early  acceleration  of 
evolution  followed  by  very  slow  or  zero  change  in  the  last  150  million 
years  (Fig.   164).    It  has  also 


been  shown  that  a  similar 
method  applied  to  the  evolu- 
tion of  coelacanths  gives  a 
curve  of  similar  shape  (Schaef- 
fer,  1952). 


6.  Modern  lung-fishes 

The  three  surviving  genera 
of  lung-fishes  (Fig.  163)  are 
mainly  inhabitants  of  rivers 
(though  Protopterm  lives  in 
large  lakes)  and  they  all 
breathe  air.  Neoceratodas  lives 
only  in  the  Burnett  and  Mary 

rivers  in  Queensland,  the  pools  of  which  become  very  low  and  stagnant 
in  summer.  Lepidosiren  from  the  rivers  of  tropical  South  America,  and 
Protopterus  from  tropical  Africa,  can  survive  when  the  rivers  dry  up 
completely.  They  dig  into  the  mud,  leaving  a  small  opening  for  breath- 
ing, and  can  remain  in  this  state  for  at  least  six  months.  Remains  of 
cylindrical  burrows  found  associated  with  dipnoan  bones  show  that 
this  habit  of  aestivation  has  been  adopted  by  the  group  at  least  since 
Permian  times.  The  three  survivors  all  show  similar  deviations  from 
the  conditions  found  in  *Dipterus,  but  Neoceratodus  has  diverged  less 
than  the  other  two.  The  tail  fin  is  symmetrical  (diphycercal)  in  all 
three,  with  no  trace  of  separate  dorsal  fins.  The  paired  fins  are  of 
'archipterygial'  type  in  Neoceratodus,  with  an  axis  and  two  rows  of 
radials  (Fig.  165).  The  scapula  is  covered  by  clavicles,  cleithra,  and 
post-temporals,  the  latter  articulating  with  the  skull.  The  scales  are 
reduced  to  bony  plates. 

The  vertebrae  are  cartilaginous  arches,  the  notochord  remaining 
as  an  unconstricted  rod.  In  the  skull  there  is  also  a  great  reduction  of 
ossification,  the  dorsal  bones  consisting  of  a  few  bony  plates,  forming 
a  pattern  not  obviously  comparable  with  that  of  other  forms  (Fig. 


Fig.  165.  Neoceratodus,  showing  the  method  of 
walking  on  the  bottom.  A,  forwards;  B,  back- 
wards; C,  resting.  (From  Ihle,  after  Dean.) 


276 


LUNG-FISHES 


x.  6 


166).  The  jaw-suspension  is  autostylic.  The  food  consists  of  small 
invertebrates  and  decaying  vegetable  matter,  which  is  eaten  in  large 
amounts.  In  the  gut  there  is  no  stomach  and  the  intestine  is  ciliated. 
There  are  no  hepatic  caeca,  but  a  well-developed  spiral  valve  is 
present. 


PP-  qc.  Pa 


Fig.  166.  Skull  of  Neoceratodus.  Above,  Lateral  view;  below,  view  of  medial  surface 

of  right  half. 
a.  angular;  bh.  basihyal;  br.  fifth  branchial  arch;  ch.  ceratohyal;  cr.  'cranial'  rib;  d.  dentary; 
eo.  'exoccipital';  hm.  hyomandibula;  hn.  hyomandibular  nerve;  hr.  hypohyal;  Ip.  lateral 
plate;  ma.  median  anterior,  and  mp.  median  posterior  plate;  na.  neural  arch;  nac.  cartilage 
of  neural  arch;  ns.  notochordal  sheath;  nsp.  neural  spine;  nt.  notochord;  o.  opercular,  and 
oc.  its  cartilage;  pa.  parasphenoid;  />/.  post-frontal;  pp.  pterygopalatine;  pt.  palatine  tooth; 
pto.  pterotic  (?),  and  g.  its  downward  process  covering  the  quadrate  cartilage,  qc;  s.  sub- 
opercular;  so.  suborbital;    sp.  splenial;    st.  splenial   tooth;    vt.   vomerine   tooth.    (From 

Goodrich.) 

The  external  nostrils  lie  just  at  the  edge  of  the  mouth  and  the 
internal  nostrils  open  into  its  roof.  The  air-bladder  is  developed  into 
a  definitely  lung-like  structure  (there  is  one  in  Neoceratodus,  a  pair  in 
each  of  the  others),  divided  into  many  chambers.  Neoceratodus  has 
been  observed  to  come  to  the  surface  to  breathe  air  and  is  said  to  be 
able  to  survive  in  foul  water  that  kills  other  fishes,  but  it  cannot  live 
out  of  the  water.  Lepidosiren  and  Protopterus  have  been  shown  to 
obtain  98  per  cent  of  their  oxygen  from  the  air.  The  wall  of  the  air- 
bladder  of  all  forms  contains  muscle-fibres  and  the  cavity  is  subdivided 
into  a  number  of  pouches  or  alveoli  (Fig.  157).  In  Protopterus  and 
Lepidosiren  the  edges  of  the  slit-like  glottis  are  controlled  by  muscles 
and  there  is  an  epiglottis.  The  lung  is  supplied  with  blood  from  the 
last  branchial  arch  in  Neoceratodus  (Fig.  167),  but  in  the  other  Dipnoi 


x.  6 


CIRCULATION 


277 


there  is  a  more  elaborate  arrangement.  The  second  and  third  gill- 
arches  bear  no  lamellae  and  their  afferent  and  efferent  branchial  vessels 
are  directly  continuous,  so  that  blood  flows  from  the  ventral  to  the 
dorsal  aorta  and  carotids.  The  pulmonary  artery  springs  from  the 
dorsal  aorta.  Blood  returns  in  a  special  pulmonary  vein  to  the  partly 


Fig.  167.  Branchial  circulation  of  A  Neoceratodus  and  b  Protopterus. 

abr.  anterior  efferent  vessel;  ac.  anterior  carotid,  a/3"6,  four  afferent  vessels  (corresponding 
to  the  original  arches  4-6) ;  ah.  afferent  hyoidean ;  c.  conus ;  cl.  coeliac  artery ;  da.  dorsal  aorta ; 
dl.  dorso-lateral  aorta;  eb-~*.  second  and  fourth  epibranchial  arteries;  eg.  external  gills; 
eh.  efferent  hyoidean;  ht.  heart;  hyp.  median  hypobranchial;  L.  air-bladder;  la.  lingual 
artery;  mes.  mesenteric  artery;  pa.  pulmonary  artery;  pc.  posterior  carotid;  pv.  pulmonary 
vein;  5.  position  of  closed  spiracle;  va.  ventral  artery;  vx.  vena  cava  inferior;  I-V  five 
branchial  slits. 

The  gills  are  represented  on  the  hyoid  and  next  four  branchial  arches.  (From  Goodrich.) 


separated  left  side  of  the  sinus  venosus.  The  auricle  is  partly  divided 
into  two  and  the  ventricle  is  almost  completely  divided  by  a  ridge 
and  a  series  of  muscular  trabeculae.  The  ventral  aorta  is  shortened 
into  a  spirally  twisted  truncus  arteriosus,  provided  with  a  system  of 
valves  such  that  the  blood  from  the  left  side  of  the  auricle  is  directed 
mostly  into  the  first  two  branchial  arches,  that  from  the  right  side 
into  the  last  two.  In  this  way  some  separation  of  pulmonary  and 
systemic  circulations  is  achieved.  Indeed,  although  there  is  every 
reason  to  believe  that  the  mechanism  has  been  in  existence  for  nearly 
300  million  years,  it  shows  us  most  clearly  a  possible  intermediate 
stage  between  aquatic  and  pulmonary  respiration.  It  seems  likely  that 
the  earliest  amphibia  employed  a  similar  system.  There  is  a  coronary 
artery  arising  from  the  anterior  efferent  branchial  arches  (Fig.  167). 


278 


LUNG-FISHES 


x,  6 


16 


A  further  amphibian  feature  of  the  blood-vascular  system  is  the 

presence  of  an  inferior  vena  cava,  a 
vessel  collecting  blood  from  the  kidneys 
and  reaching  to  the  heart  by  passing 
round  to  the  right  of  the  gut  in  the 
mesentery.  The  more  dorsal  cardinal 
veins,  joining  the  ductus  Cuvieri,  remain 
present,  however,  and  there  is  a  renal 
portal  system. 

The  adrenals  of  Dipnoi  are  represented 
by  two  separate  masses  of  tissue.  The 
perirenal  tissue  of  Protopterus  is  a  con- 
siderable mass  of  material  around  the 
kidney,  containing  lipid,  steroid,  and 
round-cell  (lymphoid)  tissues,  as  well 
as  endothelial  and  pigment  cells.  The 
steroid  tissue  shows  histochemical  pro- 
perties similar  to  those  of  mammalian 
adrenal  cortex  and  undergoes  changes 
after  injection  of  mammalian  ACTH. 
This  tissue  thus  shows  a  collection  of 
functions,  haematopoietic,  phagocytic, 
storage,  endocrine,  and  pigmentary, 
which  may  show  the  starting  point  of 
the  evolution  of  the  tetrapod  adrenal 
cortex.  Cells  that  give  the  chrome 
reaction,  the  adrenal  medullary  tissue,  lie 
in  the  walls  of  the  intercostal  branches 
of  the  dorsal  aorta.  This  condition  could 
have  given  rise  to  that  of  amphibia. 

The  arrangement  of  the  urinogenital 
system  is  similar  to  that  of  amphibia  and 
is  probably  closer  to  that  of  the  ancestral 
gnathostome  than  in  any  living  elasmo- 
branch  or  actinopterygian.  In  the  male 
there  are  vasa  efFerentia  by  which  sperms 
are  passed  through  the  excretory  portion 
of  the  mesonephros.  In  the  female  eggs 
are  shed  free  into  the  coelom  and  carried 
out  by  a  Mullerian  duct,  whose  opening  lies  far  forward.  An  in- 
teresting feature  is  that  the  Mullerian  duct  is  very  well  developed  in 


— 1 

Fig.  168.  Dorsal  view  of  the  brain 
of  Protopterus. 

I,  spinal  cord;  2,  dorsal  root  of  first 
spinal  nerve;  3,  diverticula  of  4,  the 
saccus  endolyinphaticus;  5,  medulla 
oblongata;  6,  fourth  ventricle;  7, 
cerebellum;  8,  mesencephalon  (fused 
optic  lobes);  9,  stalk  of  pineal  body; 
10,  thalamencephalon;  11,  velum 
transversum;  12,  pineal  body;  13, 
lobushippocampi;  i4,choroidplexus ; 
15,  cerebral  hemisphere;  16,  olfac- 
tory lobe.  (After  Burckhardt,  from 
Goodrich.) 


x.  6  EVOLUTION  OF  DIPNOI  279 

the  male.  This  is  one  of  several  details  (lack  of  ossification,  un- 
constricted  notochord)  which  raise  the  suspicion  that  the  living 
Dipnoi  have  acquired  their  special  characters  by  a  process  of 
paedomorphosis  or  partial  neoteny,  that  is  to  say,  becoming  sexually 
mature  in  an  early  stage  of  morphogenesis. 

The  development,  again,  shows  similarity  to  that  of  amphibia  and 
dissimilarity  from  the  other  groups  of  fishes  in  that  cleavage  is  total 
and  gastrulation  takes  place  to  form  a  yolk  plug.  There  is  therefore 
no  blastoderm  or  extra-embryonic  yolk  sac.  However,  the  cells  of  the 
vegetative  pole  contribute  little  to  the  shape  of  the  embryo  and  indeed 
may  form  a  partially  separate  yolk  sac.  The  larvae  show  distinct  simi- 
larity to  those  of  amphibia,  especially  the  larvae  of  Lepidosiren  and 
Protopterus,  in  which  there  is  a  sucker  and  external  gills. 

The  nervous  system  shows  the  same  affinities  as  the  rest  of  the 
organization  (Fig.  1 68).  The  forebrain  is  evaginated  into  a  well-marked 
pair  of  cerebral  hemispheres.  The  roof  of  these,  though  not  very 
thick,  is  nervous  and  therefore  is  definitely  of  the  inverted  type,  not 
everted  as  in  Actinopterygii.  The  optic  lobes  are  little  developed,  the 
mesencephalon  being  hardlv  wider  than  the  diencephalon.  The  cere- 
bellum is  small.  A  peculiar  feature  is  the  development  of  the  inner  ear 
to  form  a  special  lobed  saccus  endolymphaticus,  lying  above  the 
medulla  oblongata.  The  significance  of  this  is  not  known,  but  it  is 
interesting  that  similar  backward  extensions  of  the  ear  are  found  in 
amphibia. 

In  many  features,  then,  the  Dipnoi  differ  from  modern  fishes  and 
resemble  the  amphibia,  which  evolved  from  the  same  stock.  The  early 
crossopterygians  probably  competed  somewhat  precariously  with 
other  fishes,  as  do  the  Dipnoi,  and  indeed  many  urodeles,  today.  It 
was  only  after  tens  of  millions  of  years  of  evolution  during  the  Car- 
boniferous and  Permian  times  that  numerous  land  animals  arose, 
in  the  form  of  the  later  amphibian  and  reptilian  types  (Fig.  211). 


XI 

FISHES  AND  MAN 

Man's  influence,  which  has  so  altered  the  face  of  the  land,  also  reaches 
out  into  the  water.  During  the  last  half-million  years  or  so  fishing  has 
grown  continually,  until  at  the  present  time  in  fresh  and  shallow  sea 
waters  man  has  become  the  most  important  source  of  mortality  of  fish. 
However,  he  still  leaves  vast  regions  of  the  sea,  as  of  the  land,  almost 
untouched.  It  may  be  that  methods  of  catching  the  fish  that  swim 
above  deep  waters  will  eventually  produce  changes  there  too,  pro- 
viding a  substantial  extension  of  the  food-supplies  of  man  and 
effecting  great  alteration  in  the  population  of  the  sea. 

Man  has  caught  fish  from  his  earliest  times  and  he  uses  many  parts 
of  their  bodies.  The  skin,  especially  of  elasmobranchs,  makes  a  useful 
leather  and  also  a  polishing  material.  The  scales  of  the  bleak  (Alburnus) 
yield  a  substance  that  when  coated  on  to  the  inside  of  glass  beads 
makes  artificial  pearls.  The  lining  of  the  air-bladder,  especially  of 
sturgeons,  makes  isinglass,  a  shiny  powder  used  for  various  purposes 
as  an  adsorbent  (i.e.  in  wine-making).  Fish-glue  is  obtained  from  the 
connective  tissue  of  the  skin  and  other  parts.  Fish  oils  are  used  as 
food,  and  are  also  valuable  in  the  manufacture  of  soap  and  other  things. 
Besides  their  direct  use  as  human  food,  fish  products  may  be  fed  to 
animals,  and  the  liver  makes  excellent  manure. 

Fish  therefore  provide  the  raw  material  for  many  human  activities, 
but  it  is,  of  course,  principally  for  food  that  they  are  caught.  From  a 
fish  diet  one  can  obtain  not  only  abundant  calorific  value,  especially 
if  the  fish  be  fat,  but  also  various  proteins,  often  the  fat-soluble 
vitamins  A  and  D,  and  usually  considerable  amounts  of  combined 
phosphorus  and  other  elements.  Herring  and  mackerel  are  probably 
the  cheapest  source  of  protein  available  to  many  people  in  Britain. 
Fish  are  undoubtedly  good  food,  and  what  is  perhaps  even  more 
important  they  are  esteemed  as  such;  most  people  think  that  they 
taste  good. 

It  is  not  possible  to  give  an  accurate  estimate  of  the  amount  of  fish 
caught  every  year;  20  million  tons,  of  value  £200  million,  is  certainly 
not  an  overestimate  for  the  catch  of  the  whole  world  in  each  of  the 
years  between  the  Great  Wars.  An  appreciable  fraction  of  the  nutri- 
ment of  the  human  race  is  derived  from  fish.  The  annual  catch  was 
estimated  at  26  million  metric  tons  in  1951 .  The  greatest  national 


xi  METHODS  OF  FISHING  281 

catch  was  by  Japan  (3-8  million),  followed  by  U.S.S.R.  (2-5),  U.S.A. 
(2-3),  and  Great  Britain  (i-i). 

By  far  the  greater  part  of  all  fishing  is  in  the  sea.  In  Great  Britain 
the  total  catch  in  fresh  water  annually  is  reckoned  at  only  2,000  tons 
and  the  entire  stock  at  8,000  tons.  However,  there  are  important 
fishing  industries  in  the  American  Great  Lakes,  the  African  lakes,  and 
in  many  parts  of  the  world  carp  are  raised  on  fish  farms,  the  water 
being  manured  to  yield  a  good  crop  of  the  freshwater  plants  and 
invertebrates  on  which  the  carp  feed.  The  milk  fish  (Chanos  chanos), 
which  feeds  directly  on  algae,  provides  high  yields  in  many  tropical 
and  subtropical  fish-ponds. 

Fishing  in  the  sea  is  limited  mainly  by  two  considerations.  First, 
the  labour  is  only  really  profitable  when  the  fish  population  is  dense. 
Secondly,  fish  do  not  keep  well  unless  they  are  treated  in  some  special 
way  and  they  are  therefore  best  caught  near  to  their  market.  For  these 
reasons  the  big  commercial  fisheries  are  mostly  in  the  relatively  shal- 
low waters  of  the  continental  shelf  (down  to  200  fathoms)  and  in  the 
northern  hemisphere.  However,  by  packing  the  fish  in  ice  or  cooling 
by  other  means,  the  vessels  are  now  able  to  go  longer  distances  than 
formerly.  Japanese  and  American  vessels  now  fish  for  tuna  and  salmon 
in  the  open  ocean. 

For  catching  purposes  fish  may  be  divided  into  those  that  swim 
away  from  the  bottom,  the  pelagic  forms,  such  as  herring  or  mackerel, 
and  the  bottom-living  or  demersal  fishes,  such  as  the  skates  and  rays, 
flat-fishes  and  angler-fishes.  For  the  first  the  gear  employed  is  usually 
drift-net.  This  is  of  narrow  mesh  and  is  shot  and  left  overnight,  drifting 
vertically  near  the  surface,  often  making  a  barrier  two  or  three  miles 
in  length.  The  fish,  such  as  herrings,  swim  into  them,  and  become 
enmeshed,  and  are  removed  as  the  nets  are  hauled  in. 

The  success  of  such  fishing  with  drift-nets  depends  on  laying  the 
nets  in  the  path  of  large  shoals  of  fish  and  it  is  therefore  practised 
especially  in  regions  where  fish  congregate  seasonally.  For  instance, 
in  the  North  Sea  between  East  Anglia  and  Holland  the  herring  con- 
gregate in  the  autumn;  at  certain  times,  for  unknown  reasons,  all  the 
fish  in  the  area  begin  to  move,  making  'the  swim',  and  they  are  then 
caught  in  great  numbers.  Herring  are  usually  caught  at  slack  water. 
At  the  October  full  moon,  slack  water  occurs  just  after  dusk  and  just 
before  dawn  and  catches  are  higher  then.  Other  drift-net  fisheries 
depend  on  intercepting  the  fish  when  rising  to  feed.  Evidently  these 
methods  demand  a  close  knowledge  of  the  habits  and  migrations  of 
the  fish.  The  fishermen  have  learned  to  know  when  and  where  to 


282  FISHES  AND  MAN  xi 

expect  the  larger  and  nearer  aggregations,  but  there  is  still  much  to 
be  done  in  tracing  the  migration  and  behaviour  of  pelagic  fishes. 
It  is  not  impossible  that  other  pelagic  fisheries  could  be  developed 
that  would  be  at  least  as  advantageous  as  the  herring  fishery.  Besides 
those  eaten  fresh,  others  are  preserved  as  kippers  by  salting  and  smok- 
ing, or  are  heavily  salted  and  smoked  to  make  'red  herrings'  for  which 
there  has  been  a  large  export  market. 

Lining  is  a  method  that  can  be  used  for  either  pelagic  or  demersal 
fish.  For  instance,  the  cod  fishery  of  Newfoundland  uses  lines  with 
several  thousand  baited  hooks.  Inshore  fishing  may  be  accomplished 
by  beach  seining,  a  process  of  enclosure  of  the  fish  from  the  shore. 
There  are  also  various  forms  of  trap  into  which  the  fish  swim  and 
cannot  escape.  Danish  seining,  or  purse  seining,  completely  surrounding 
the  fish  and  sometimes  then  also  drawing  the  bottom  of  the  net 
together,  is  another  effective  method. 

The  greatest  quantities  of  fish  are  caught,  however,  by  the  various 
forms  of  trawling.  These  depend  essentially  on  dragging  a  bag  along 
the  bottom  of  the  sea,  and  the  different  types  adopt  various  means  of 
keeping  the  bag  open.  The  earlier  way  of  doing  this  was  by  means  of 
a  rigid  bar  and  these  beam  trawls  sometimes  used  poles  over  50  ft 
long.  More  recently  otter-trawling  has  replaced  the  beam  trawl,  the 
otter  boards  being  flat  wooden  structures  attached  at  each  end,  so  as 
to  sheer  away  when  they  are  dragged  through  the  water,  thus  opening 
the  net.  Various  devices  are  used  to  stir  up  the  fish  from  the  bottom; 
in  particular  the  otter  boards  are  now  usually  separated  from  the  net 
by  long  wires  and  a  'tickler'  chain  is  attached  in  front  of  the  mouth. 

With  such  methods  very  large  amounts  of  fish  can  be  taken  from 
the  sea  bottom.  In  i860  sailing-ships  landed  500  tons  of  fish  at 
Grimsby;  by  190 1,  176,000  tons  were  landed  from  the  steam  traw  lers 
50,000  tons  of  plaice  alone  are  taken  annually  from  the  North  Sea. 
There  is  evidence  that  the  taking  of  such  amounts  of  fish  from  rela- 
tively confined  waters  has  a  large  influence  on  the  population.  For 
instance,  it  is  estimated  that  45  per  cent  of  the  stock  of  plaice  is 
caught  each  year  in  the  North  Sea.  Under  these  conditions  man  pro- 
vides the  main  source  of  mortality  for  the  fishes.  It  is  less  clear 
exactly  how  such  mortality  influences  the  total  population  of  the  fish 
in  the  area.  There  is  reliable  evidence  that  intensive  fishing  reduces 
the  productivity  of  fishing  effort  in  some  cases,  but  there  is  also 
evidence  that  by  reducing  competition  fishing  may  produce  faster 
growth  of  the  fish.  The  problem  is  worth  some  further  discussion 
since,  besides  its  economic  importance,  it  gives  us  an  insight  into  the 


xi  NUMBER  OF  FISHES  283 

life  of  the  vast  populations  of  the  sea  and  a  glimpse  of  the  factors  that 
control  the  numbers  of  each  animal  species. 

It  used  to  be  held  that  one  of  the  chief  dangers  of  fishing  was  that 
it  would  destroy  the  breeding-stock,  on  the  grounds  that  it  is  axio- 
matic that  something  is  wrong  if  fish  are  destroyed  before  they  have 
an  opportunity  to  breed.  We  may  detect  something  of  anthropocentric 
sentimentality  here,  for  reflection  shows  at  once  that  it  is  impossible 
for  every  fish  that  is  hatched  to  survive  and,  further,  that  the  total 
annual  supply  of  fish  can  be  provided  by  relatively  few  adults.  The 
number  of  fish  in  the  sea,  indeed,  bears  no  obvious  relation  to  the 
number  of  eggs.  A  cod  may  shed  as  many  as  8  million  eggs  (usually 
fewer),  which  float  at  the  sea  surface  and  hatch  into  planktonic  young. 
Yet  herrings,  which  are  much  more  numerous  as  adults,  lay  fewer 
eggs,  usually  less  than  30,000  each.  Presumably  the  risks  of  life  are 
less  for  the  herring,  but  we  cannot  see  clearly  why;  the  herring's  eggs 
are  sticky  and  become  attached  to  gravel  or  seaweeds,  which  may  give 
them  some  protection;  they  are  known  to  be  eaten  by  other  fishes, 
perhaps  on  a  smaller  scale  than  planktonic  eggs.  Both  herring  and 
cod  fry  are  planktonic  and  feed  on  the  nauplius  and  other  larval 
stages  of  Calamis  and  other  copepods.  The  cod,  like  other  bottom- 
fishes,  has  to  undergo  the  risks  of  metamorphosis,  but  this  hardly 
seems  sufficient  to  explain  the  much  greater  abundance  of  herring, 
especially  since  many  fishes  feed  on  the  latter,  including  the  cod  them- 
selves! As  Graham  puts  it,  'no  one  really  knows  why  the  herring, 
which  nearly  everything  eats,  should  be  able  to  manage  with  a  less 
rate  of  reproduction  than  the  cod,  which  eats  nearly  everything'. 
The  greater  part  of  the  mortality  of  pelagic  fish  larvae  is  due  to  pre- 
dation,  including  that  by  members  of  the  same  species.  This  probably 
provides  a  method  of  regulation,  the  number  of  each  species  eaten 
being  dependent  on  their  frequency. 

This  brings  us  to  face  the  difficult  question  of  the  pressure,  force, 
or  potential  that  ensures  and  controls  the  number  of  animals.  Re- 
production is  only  a  part  of  the  source  of  this  pressure,  the  other 
element  being  the  feeding  and  growth  of  the  animals  as  a  result  of  the 
skill  and  persistence  with  which  they  seek  and  consume  their  food. 
It  is  somewhat  easier  to  study  these  questions  in  a  marine  than  in  a 
land  community,  the  whole  population  being  enclosed  in  one  vast 
bath,  the  additions  and  subtractions  to  which  can  be  known. 

We  must  not  forget,  however,  that  conditions  are  far  from  con- 
stant, even  in  the  'unchanging  sea'.  For  instance,  the  extent  to  which 
fish-fry  hatch  and  successfully  overcome  the  hazards  of  the  early 


(284) 


3  4   5   6  7   8   9  10  11  12  13  14  15  16  17  18  19  20  21 


Ifllll 


1907 


■  ■*■ 


1908 


I 


1909 


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1910 


J 


1911 


1 


1912 


I 


1913 


1 


1914 


M^^— 


A 


1915 


A 


1916 


JLL 


1 


1917 


Id 


1 


1918 


II      -  .1    1919 


:20 

20 


40 
20 


:60 

40 

20 


60 
40 
20 

60  ^ 
40  £ 

60  <* 
40  ^ 

Z03 

-40  ^ 

:20 


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-120 


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■20 


Fig.  i 


3  4    5   6   7   8   9   10  11  12  13  14  15  16  17  18  19  20  21 
Age  of  fish  -years 

69.  Age  composition  of  Norwegian  herring  catches  1907-19,  showing 
the  preponderance  of  particular  year-classes.  (After  Hjort.) 


xi  FISH  CYCLES  285 

stages  of  life  varies  most  mysteriously  from  year  to  year.  By  study  of 
the  markings  on  the  scales,  bones,  and  otoliths  it  is  possible  to  show 
the  age  composition  of  a  fish  population  and  it  is  found  that  the 
hatches  of  certain  years  predominate.  Thus  the  herring  hatched  in 
1904  dominated  the  population  in  some  parts  of  the  North  Sea  for 
years  afterwards  (Fig.  169).  Subsequent  good  herring  years  occurred 
in  1913  and  1918.  Similarly  there  were  good  cod  years  in  1904  and 
191 2.   Haddock  broods  in  the  North  Sea  follow  a  rather  regular 


r< 


1919 


12-2 


10-0 

\ 

8-1 

/ 

8-8 

/ 

67 

is 

4-8* 

3-8 

2-3' 

2-6 

0-8* 

(0-2 

Vo  2 

TO 

12J 

09s 

1920    1921     1922     1923    1924    1925    1926    1927    1928    1929    1930     1931     1932     1933    1934 

Year  class 


Fig.  170.  Relative  strengths  of  haddock  broods  in  the  North  Sea,  showing  cyclical 
fluctuations.  (After  Raitt,  from  Russell,  The  Overfishing  Problem.) 

rhythm  with  a  period  of  about  three  years  (Fig.  170).  These  cyclical 
changes  in  hatching  do  not  appear  to  produce  fluctuations  in  the  total 
population  of  that  species,  though  we  have  inadequate  data  on  the 
point.  It  seems  likely  that  there  is  a  limit  set  to  the  total  of  fish  of  the 
species,  irrespective  of  age-grouping. 

In  addition  to  such  cyclical  changes  there  are  also  larger  ones,  such 
as  the  increase  of  cod  in  the  far  north  around  Bear  Island  in  recent 
years,  apparently  due  to  a  northerly  extension  of  warm  water,  the 
reason  for  which  is  not  known.  Since  so  many  changes  are  going  on 
in  the  eternal  sea  is  it  to  be  wondered  at  that  the  animals  in  it  are 
changing?  We  might  be  surprised  rather  at  the  slowness  of  their 
evolution. 

All  the  fish-life  in  the  sea  depends  ultimately  on  the  diatoms, 
flagellates,  and  other  green  organisms  of  the  plankton,  reaching  the 
fish  usually  after  passage  through  one  or  more  animals,  especially 
copepods.  Bottom-living  fishes  also  depend  on  plankton,  in  this  case 


286  FISHES  AND  MAN  xi 

after  it  has  died  and  passed  through  a  bottom-living  invertebrate. 
Thus  plaice  feed  on  lamellibranchs  and  worms,  soles  on  worms  alone, 
haddock  on  star-fish,  molluscs,  and  worms.  The  phytoplankton  is, 
of  course,  built  up  by  photosynthesis  from  carbon  dioxide,  water, 
nitrates,  phosphates,  and  small  quantities  of  other  substances.  The 
limiting  factors  in  the  plankton  growth,  granted  adequate  temperature 
and  sunlight,  may  be  nitrate,  ammonia,  and  phosphate,  the  latter 
present  only  to  the  extent  of  less  than  one  part  in  20  million.  During 
the  spring  and  early  summer  nearly  all  the  phosphate  in  the  water  may 
be  taken  up  into  the  phytoplankton,  which  increases  rapidly.  The 
zooplankton  (Cala?ius,  Sec.)  increases  somewhat  later  and  by  mid- 
summer grazes  down  the  phytoplankton  to  a  considerable  extent.  It 
is  at  this  midsummer  period  that  the  pelagic  fishes  feed  most  easily, 
and  a  little  later  it  is  the  turn  of  the  bottom-living  invertebrates  and 
fish,  as  some  of  the  zooplankton  dies  and  falls  to  the  bottom.  At  the 
end  of  the  season  there  may  be  a  second  increase  in  the  phytoplankton, 
the  recovery  being  due  to  breakdown  of  the  discontinuity  layer  (see 
below),  and  then  with  the  onset  of  winter  the  plants  die  off  and  most 
of  the  phosphate  is  returned  to  the  inorganic  condition. 

Thus  to  take  the  case  of  the  cod,  whose  food  chain  is  one  of  the 
longest:  the  activity  of  the  plants  turns  carbon  dioxide,  nitrate,  and 
phosphate  into  organic  matter:  the  activity  of  the  copepods  makes 
this  available  to  the  herrings  and  the  cod  eat  the  herrings.  There  are, 
of  course,  many  intermediate  effects:  Sagitta  eat  some  of  the  cope- 
pods,  fish-fry  and  large  cod  eat  younger  cod,  and  so  on,  but  in  general 
we  shall  not  go  wrong  if  we  assume  that  the  cycle  depends  on  the 
activity  of  diatoms,  calanoids,  herrings,  and  codfish— all  seeking, 
eating,  growing,  reproducing,  and  dying. 

The  pressure  of  these  various  activities  produces  a  complicated  set 
of  interrelations  that  may  without  undue  extravagance  of  fancy  be 
called  a  macro-organism.  The  activities  of  all  the  members  contribute 
to  the  balance  that  is  set  up.  Sometimes  shortage  of  materials,  such  as 
phosphorus,  at  key-points  may  determine  the  whole  cycle. 

The  phosphate  in  the  sea  is  increased  to  a  small  extent  by  drainage 
from  the  land  and,  further,  in  a  restricted  area  such  as  the  North  Sea, 
by  the  influx  of  water  from  more  open  areas,  in  that  case  the  Atlantic. 
Not  all  the  phosphate  in  a  given  area  of  sea  is  available  for  organic 
growth,  because  there  is  usually  a  separation  between  upper  and  lower 
layers  owing  to  the  upper  layer  becoming  warmer  and  less  dense.  The 
phosphate  in  the  water  below  this  limiting  discontinuity  layer,  usually 
lying  20-100  metres  down,  is  thus  not  available,  though  it  may  be 


xi  SIZES  OF  FISH  CAUGHT  287 

made  available  in  certain  areas  by  particular  conditions  that  lead  to 
up-currents  and  mixing  of  the  layers. 

With  these  facts  in  mind  we  can  now  make  further  inquiry  into  the 
effects  on  the  population  of  the  sea  of  removal  by  man  of  large  quanti- 
ties of  organic  matter  in  the  shape  of  fish.  There  are  enough  data  to 
give  us  hints  of  the  changes  that  follow,  and  the  hope  that  with  further 
study  we  may  eventually  understand  the  Great  Sea  Beast  sufficiently 
well  to  be  able,  if  we  can  control  ourselves,  to  regulate  its  growth  to 
our  advantage. 

In  a  few  cases  it  has  been  possible  to  follow  the  course  of  a  fishery 
from  its  early  beginnings,  with  few  vessels  and  simple  apparatus, 
through  stages  in  which  the  fishing  was  progressively  more  intense. 
The  statistics  are  seldom  adequate  to  provide  us  with  wholly  satis- 
factory conclusions,  but  they  suggest  that  (1)  as  fishing  becomes  more 
intense,  the  yield  per  unit  of  fishing  power  declines ;  that  is  to  say,  the 
industry  becomes  relatively  less  profitable;  (2)  in  spite  of  this,  the 
total  yield  may  remain  constant,  or  somewhat  increase,  even  though 
(3)  the  average  size  of  the  fish  caught  decreases. 

For  example,  fishing  for  plaice  in  the  Barents  Sea,  north  of  Nor- 
way, was  begun  in  1905,  and  the  almost  'virgin'  population  in  1907 
showed  great  preponderance  of  large  mature  fish;  whereas  in  the 
North  Sea,  which  had  already  been  fished  for  many  years,  the  average 
size  was  much  smaller  and  few  of  the  plaice  were  mature.  The  fish 
taken  in  the  Barents  Sea  were  old  and  had  grown  slowly.  Transplanta- 
tion of  fish  of  this  stock  to  the  North  Sea,  however,  proved  that  they 
were  able  to  grow  as  rapidly  as  the  local  fish.  Some  measure  of  the 
intensity  of  fishing  is  given  by  the  number  of  days'  absence  of  vessels 
fishing  in  a  given  area.  No  doubt  the  measure  is  inexact,  particularly 
if  the  methods  used  are  changed,  but  it  provides  the  best  estimate 
available.  The  landing  of  plaice  taken  from  the  Barents  Sea  per  day's 
absence  was  347  cwt  in  1906,  50-4  cwt  in  1909,  and  then  fell  to  46-3, 
33-7,  and  20-5  cwt  in  the  following  years.  The  total  yield  showed  some 
decline.  The  sequence  of  events  is  typical  of  what  happens  when  a 
stock  of  mature  fish  is  first  exploited. 

Graham  described  a  good  example  of  a  similar  situation  in  Lake 
Victoria-Nyanza,  where  he  found  two  stocks  of  the  carp-like  fish 
Tilapia,  one  fished  heavily  and  the  other  with  primitive  devices  only. 
The  less  heavily  fished  stock  contained  five  times  as  many  fish  as  the 
other  and  they  were  much  older.  Yet  by  the  intensive  fishing  the 
poorer  stock  was  being  made  to  yield  a  ten  times  greater  weight  than 
the  richer  stock.  This  desirable  state  of  affairs  for  man  in  general  is 


288  FISHES  AND  MAN  xi 

considered  unsatisfactory  by  the  fishermen,  since  the  yield  per  unit  of 
effort  is  much  greater  when  the  richer  stock  is  fished. 

The  yield  of  haddock  in  the  North  Sea  per  day's  absence  averaged 
5 -8  cwt  between  1906  and  191 3,  rose  to  15-8  cvvt  in  19 19,  averaged 
6-5  cvvt  in  1 922-1 929,  and  3-7  cwt  in  1930-7.  The  fish  are  divided  into 
large,  medium,  and  small  categories,  and  the  percentage  of  the  last 
category  was  50  before  the  war,  70  in  1922-9,  and  85  in  1930-7; 
evidently  the  fish  were  becoming  smaller  throughout  this  period,  yet 
the  total  haddock  catch  changed  only  slightly,  from  121  million  kg 
( 1 910-13)  to  138  million  kg  (1922-9)  and  94  million  kg  (1930-6). 
Fishing  seems  to  have  made  the  population  consist  of  smaller  fish, 
giving  a  smaller  yield  per  unit  of  fishing  effort.  This  is  a  true  index 
of  stock  and  its  decline  shows  the  extent  of  reduction. 

The  figures  available  for  plaice  and  cod  taken  from  the  North  Sea 
show  much  the  same  tendencies.  Over  a  long  period  fishermen  have 
been  afflicted  by  the  consequences  of  the  decline  in  yield  per  unit 
effort  indicated  by  such  statistics.  Already  in  the  last  century  those 
giving  evidence  before  Royal  Commissions  expressed  an  uneasy  feel- 
ing that  the  profitability  of  the  industry  was  declining.  This  situation 
has  been  met  by  continual  improvement  in  methods  of  fishing  and  the 
exploitation  of  new  grounds.  The  proportion  of  the  total  English 
catch  that  is  obtained  from  the  nearer  waters  of  the  North  Sea  is  now 
much  less  than  formerly,  although  the  catch  is  no  greater.  We  have 
already  seen  that  steam  trawling  and  better  gear  all  mean  increased 
labour  for  the  crews,  at  greater  distances  from  port.  With  all  the 
improvements  in  technique  and  discovery  of  new  grounds  we  succeed 
in  obtaining  from  the  sea  little  more  fish  than  at  the  end  of  the  last 
century;  and  there  is  no  greater  profit  for  those  engaged  in  the 
industry. 

The  'Great  Law  of  Fishing',  as  Graham  calls  it,  'that  fisheries  that 
are  unlimited  become  unprofitable'  has  been  tested  on  at  least  three 
occasions.  During  the  two  Great  Wars  the  intensity  of  fishing  in  the 
North  Sea  was  reduced  and  thereafter  both  of  the  expected  changes 
were  seen :  (a)  fishing  became  more  profitable,  (b)  there  were  found  to 
be  more  old  fishes  in  the  stock.  Perhaps  more  encouraging  is  a  case 
where  the  intensity  of  fishing  has  been  regulated  not  by  war  but  by 
law.  The  halibut  fishery  of  the  Pacific  coast  of  North  America  showed 
the  typical  history  of  increasing  effort  and  decreasing  yield.  Fishermen 
went  farther  and  farther  afield  in  larger  and  more  expensive  boats, 
setting  ever  more  and  more  lines,  but  yet  brought  home  the  same  or 
a  smaller  amount  of  fish.  Thus  in  1907  there  were  1,800,000  sets  of 


xi  REGULATION  OF  FISHERIES  289 

lines  used,  in  1930,  6,400,000  sets,  but  instead  of  the  50  million 
pounds  of  fish  caught  in  the  first  year  there  were  only  23  million 
pounds  in  1930!  Then  in  1932  a  limitation  of  23  million  pounds  was 
imposed  on  the  total  catch  allowed.  Thereafter  the  stocks  rapidly 
increased  and  it  was  found  possible  to  collect  the  standard  catch  in 
five  months  instead  of  nine,  with  greatly  increased  profit. 

Other  attempts  to  regulate  fisheries  have  been  made;  in  particular 
by  the  mesh  regulations,  designed  to  avoid  taking  small  fishes.  The 
aim  of  regulation  is  nowadays  not  so  much  to  save  the  stock  from 
undue  reduction  or  extinction  but  rather  to  crop  it  in  such  a  way  as 
shall  make  fishing  profitable.  Whatever  we  do  it  is  unlikely  that  we 
shall  destroy  all  the  stocks  of  any  species,  but  there  is  reason  to  think 
that  the  rate  at  which  the  stocks  grow  varies  with  the  intensity  of 
fishing.  If  this  is  so,  it  may  be  possible  to  find  an  optimum  that  suits 
both  the  fish  and  the  fisherman. 

In  order  to  regulate  a  fishery  effectively  it  is  necessary  to  express  its 
characteristic  parameters  in  a  comprehensive  equation.  This  has  been 
done  by  fisheries  research  workers  who  have  provided  mathematical 
models  such  as  are  so  often  used  in  operational  research  (Beverton 
and  Holt  in  Graham,  1956).  These  equations  show  the  effects  that  are 
likely  to  follow  variation  in  such  a  factor  as  the  size  of  the  mesh  of  the 
cod  end  of  the  trawl  net,  which  is  one  of  the  means  used  to  regulate 
a  fishery.  Fishing  is  a  form  of  hunting,  not  of  agriculture,  and  if  we 
cannot  improve  the  yield  by  cultivation  we  may  be  able  to  do  so  by 
working  out  the  best  way  to  fish. 

Four  primary  factors  are  considered  in  the  model,  recruitment  (R), 
growth  (W),  mortality  due  to  natural  causes  (M),  and  mortality  due 
to  fishing  (F).  The  relation  of  these  factors  to  the  yield  by  weight  of 
the  fishery  ( Yw)  is  considered  and  a  theoretical  equation  for  Yw  is 
derived.  If  the  theory  is  correct  the  equation  should  be  able  to  de- 
scribe the  yield  of  various  fisheries  in  the  past.  It  proves  to  do  this 
well  and  forecasts  that  improvements  in  yield  could  be  obtained  by 
changing  methods  of  fishing  in  the  future.  The  data  for  testing  the 
theory  come  from  statistics  of  the  fishes  caught,  which  give  catches 
per  unit  effort  in  each  year  class  and  their  lengths.  These  are  available 
for  several  fisheries  and  we  may  consider  the  plaice  in  the  North  Sea 
for  the  years  1929-38.  Fish  are  said  to  be  recruited  when  they  first 
enter  the  fished  area  of  deeper  water  at  2-3  years  old,  being  much  less 
than  1  per  cent  of  the  original  batch  of  eggs.  The  value  R  for  a  given 
mesh  size  is  obtained  from  the  number  of  fishes  in  the  youngest 
year  class  in  the  catch,  with  corrections  to  allow  for  the  fact  that 


(29°) 


300 


200 


g.   100 


V  X 

Age-group 


2000 


1500 


«    1000 


500 


o>     300 


200 


100 


005  100  1-50 

073  r 


500r 


400 


50         100  150         200      250 

Cod-end   mesh   size  (mm) 


Fig.  171A.  Mortality  rate  of  plaice.  Natural  logarithms  of  average  number  caught  of  each 
age-group  of  North  Sea  plaice  per  100  hours'  fishing,  1929-38.  The  slope  of  the  line  gives 
the  estimate  (F+M)  =  0-83.  The  first  three  points  are  lowered  by  absence  of  fish  from 
the  exploited  area  (some  individuals  still  remaining  in  the  nursery  areas)  and,  possibly, 

by  rejection  at  sea. 

Fig.  171B.  Growth  in  weight  of  plaice.  Average  weight  of  fish  of  each  age-group,  1929-38, 
and  the  fitted  von  Bertalanffy  equation  for  growth  in  weight. 

Fig.  171c.  Annual  steady  yield  of  plaice  plotted  against  fishing  intensity.  Yield  of  plaice 

per  recruit  (YWIR)  as  a  function  of  fishing  mortality  coefficient  (F)  with  tp'  =  3-72  years, 

corresponding  to  a  70  mm  gauge  mesh  in  trawls,  double  twine.  The  vertical  line  at  F  =  0-73 

corresponds  to  the  average  pre-war  fishing  intensity. 


Fig.  17 id.  Effect  of  growth  rate  changing  with  density.  The  yield  of  plaice  per  recruit 
(YWIR)  is  shown  as  a  function  of  mesh  size  with  fishing  intensity  constant  at  F  =  073, 
but  in  calculating  curve  (b)  the  growth-rate  was  assumed  to  be  reduced  progressively  as 
the  density  of  stock  increases.  The  differences  from  the  use  of  constant  growth-rate,  curve 
(a),  are  considerable.  Not  only  is  the  benefit  from  increase  of  mesh  estimated  to  be  less,  but 
the  maximum  yield  is  reached  at  a  considerably  smaller  mesh  size. 


xi  MORTALITY  OF  FISH  291 

recruitment  is  not  simultaneous  or  sudden.  For  the  plaice  in  the  North 
Sea,  with  70  mm  mesh,  R  has  been  computed  at  280  million  fish  for  the 
area  considered,  with  mean  age  of  3  -7  years.  A  check  from  consideration 
of  numbers  and  mortality  of  eggs  gave  320  million.  Theoretically,  we 
also  require  to  know  the  length  of  the  life  of  the  fish.  Few  plaice  are 
caught  older  than  15  years  and  almost  none  over  20  years.  Since 
there  are  very  few  in  these  older  age-classes  the  upper  limit  is  un- 
important. 

The  coefficients  of  mortality  M  and  F  are  estimated  from  the 
numbers  {N t)  of  the  original  recruits  R  that  survive  at  time  t,  N  (  = 
Re—M  (t  —  tp),  where  e  is  the  natural  base  of  logarithms  and  tp  the 
age  at  entry  of  the  recruits.  The  total  mortality  (F-\-M)  (due  to  natural 
causes  (M)  and  to  fishing  (F))  is  estimated  from  the  catches  (Fig. 
1 71  a).  The  part  due  to  fishing  alone  is  found  by  consideration  of  how 
the  catch  varies  when  there  are  known  differences  in  the  fishing  effort, 
for  example  in  the  number  of  hours  fished.  In  the  extreme  case,  we 
have  the  war-time  periods,  when  there  was  no  fishing.  Confirmatory 
evidence  of  the  likelihood  that  a  fish  will  be  caught  can  be  obtained  from 
marking  experiments,  giving  the  time  between  release  and  recapture. 
For  the  plaice  (F-\-M)  has  been  estimated  over  the  years  1929-38  as 
0-83.  This  is  the  mean  for  all  the  age-classes  together,  though  for 
some  purposes  it  can  be  calculated  for  each  separately.  That  the  rate 
is  indeed  constant  is  shown  by  the  close  fit  of  Fig.  171  a.  The  first 
three  points  do  not  fit  because  recruitment  of  these  classes  was  still 
incomplete.  This  method  of  treatment,  in  which  the  contributions  of 
year  classes  of  the  same  age  recruited  in  different  years  are  considered 
together,  has  the  effect  of  averaging  out  this  variation  in  recruitment, 
which  would  be  difficult  to  estimate. 

The  value  of  the  natural  mortality  of  plaice  cannot  be  obtained  for 
these  years  from  variations  in  fishing  effort,  since  these  were  only 
slight.  However,  since  there  was  almost  no  fishing  in  the  southern  part 
of  the  North  Sea  from  1940  to  1945,  we  can  compare  the  age  groups 
V  and  VI  of  samples  taken  before  the  war  with  their  surviving  fellows 
in  the  years  after  1945.  This  gives  a  value  for  A/of  o-i,  and  subtracting 
this  from  0-83  as  the  total  mortality  we  obtain  073  as  the  mortality 
due  to  fishing.  Marking  experiments  give  a  value  of  0-69,  which  is  a 
satisfactory  agreement  considering  that  the  conditions  were  not  en- 
tirely similar.  Moreover,  the  conclusions  from  marking  involve  other 
problems,  such  as  damage  to  the  fish  and  rate  of  movement  away 
from  the  point  of  release.  The  conclusion  that  fishing  is  the  most 
important  source  of  mortality  in  such  areas  is  not  new,  but  is  obviously 


292  FISHES  AND  MAN  xi 

of  very  great  importance.  If  man  is  the  chief  predator,  then  change  in 
his  activities  will  greatly  influence  the  populations. 

Knowing  the  number  of  fishes  available  and  the  rates  at  which  they 
are  removed  by  natural  causes  and  fishing  in  a  given  case,  we  still  have 
the  even  more  difficult  task  of  formulating  the  way  in  which  the  popu- 
lation grows  and  then  deciding  whether  some  other  method  of  fishing 
would  be  more  profitable.  Probably  there  is  a  maximum  total  biomass 
of  fish  of  any  given  sort  that  can  be  supported  in  any  area,  determined 
ultimately  by  the  supply  of  inorganic  salts.  In  the  absence  of  fishing 
this  biomass  is  carried  mainly  in  the  form  of  large  fish,  whose  presence 
makes  the  growth  of  all  fish  in  the  population  slow.  The  effect  of  fish- 
ing is  to  remove  mainly  these  larger  animals,  with  a  resultant  increased 
growth  from  all  younger  groups.  The  curve  showing  the  relationship 
between  the  yield  per  recruit  and  the  intensity  of  fishing  effort  shows 
a  maximum  (Fig.  171c).  It  should  be  possible  to  define  a  fishing  mor- 
tality rate  at  which  the  decrease  in  numbers  is  balanced  by  the  incre- 
ments in  weight  of  the  survivors. 

There  is  every  reason  to  hope  that  with  further  study  of  growth, 
mortality,  reproductive  potential,  and  utilization  of  food  by  fish  the 
yield  could  be  increased  and  the  effort  of  getting  it  reduced,  making 
fishing  more  profitable  to  the  fisherman  and  providing  the  maximum 
amount  of  food.  At  present  the  economic  conditions  and  psychology 
of  the  fishing  populations  interact  with  the  factors  limiting  the  stocks 
and  the  growth  of  the  fish  to  produce  a  complicated  system  of  inter- 
relations that  is  unstable  and  unsatisfactory  to  all  parties. 

The  increase  in  weight  of  the  population  is  perhaps  the  most  diffi- 
cult feature  of  the  pattern  to  express  mathematically.  Weight  plotted 
against  age  shows  an  asymmetrical  sigmoid  shape,  with  an  inflexion 
(Fig.  171B).  The  curve  fitted  is  arbitrarily  chosen,  being  that  deduced 
from  the  hypothesis  of  Bertalanffy,  that  the  weight  is  subject  to 
opposing  forces  of  anabolism  and  catabolism,  taken  as  proportional  to 
the  absorbing  surfaces,  that  is,  to  the  squares  of  the  linear  dimensions. 
As  before,  the  fit  is  poor  for  the  lower  points,  probably  because  there 
are  incompletely  recruited  classes.  Elsewhere  the  fit  is  good  but  the 
important  point  for  us  is  the  inflexion,  since  it  indicates  that  the 
growth-rate  decreases  in  the  later  part  of  life.  The  older  plaice  are 
from  this  point  of  view  inefficient  in  providing  more  biomass.  Fur- 
ther, the  longer  a  fish  has  to  be  kept  alive  in  the  sea  before  it  is  eaten, 
the  more  of  the  limited  raw  materials  are  devoted  to  this  end  and  the 
less  to  providing  human  food.  With  present  methods  it  is  not  possible 
to  give  full  weight  to  all  of  these  factors  in  deciding  what  is  the  best 


xi  YIELD  EQUATION  293 

way  to  fish.  However,  the  theoretical  equation  derived  by  Beverton 
and  Holt  gives  us  the  yield  Yw  in  terms  of  the  parameters  already 
discussed  with  in  addition  the  maximum  weight  W^  and  a  factor  K 
related  to  the  catabolism 

d^  =  FNlW.  (1) 

The  number  Nt  at  the  time  t  is  given  by 

Nt  =  R^F+MXt-t,^  (2) 

and  the  weight  Wtby 

Wt=  W^i-e-w-1*?).  (3) 

This  last  is  best  handled  as  a  cubic  of  the  form 

Wt=    W^2Q-ne'UK(l-tti)- 
n  =  0 

Substituting  (2)  for  Nt  in  (1),  and  (3)  for  Wt  we  obtain 

at  ri=o 

This  provides  the  basic  equation  with  which  forecasts  of  effects  of 
changing  the  various  factors  are  made. 

Empirical  values  can  be  obtained  for  the  yield  per  recruit  (YWIR) 
for  various  values  of  F,  with  a  mesh  of  70  mm.  Such  a  yield/intensity 
curve  of  North  Sea  plaice  is  shown  in  Fig.  171c.  The  graph  shows  that 
with  infinite  effort  all  fish  would  be  caught  at  recruitment  and  would 
yield  their  initial  weight  of  123  g.  At  the  pre-war  fishing  mortality  of 
0-73  the  yield  was  200  g.  But  the  curve  has  a  clear  maximum  at  over 
250  g,  with  a  fishing  mortality  of  only  0-22.  Therefore  if  these  pre- 
dictions are  correct,  a  lesser  intensity  of  fishing  should  provide  a 
greater  yield. 

One  possible  way  of  reducing  fishing  intensity  is  to  increase  the 
size  of  the  mesh  of  the  cod  net.  If  the  age  at  recruitment  were  in- 
creased to  ten  years  the  yield  per  recruit  would  be  as  high  as  400  g 
(Fig.  17 id,  curve  a).  Beyond  this  maximum,  the  yield  falls  because  of 
the  death  of  fish  by  natural  causes  before  entering  the  exploited  phase. 
However,  this  curve  assumes  that  the  growth-rate  is  independent 
of  density  and  it  ignores  the  complex  problem  of  the  competition  of 
old  and  young  fishes  for  a  limited  supply  of  raw  materials.  Curve  b 
of  Fig.  17 id  has  assumed  a  reduced  growth-rate  with  increasing 
density  and  it  will  be  seen  that  the  advantage  of  increasing  mesh  size 
is  much  reduced. 


(294) 


500 


400 


^  300 


200 


100  • 


500 


400 


300- 


>T*  200- 


100 


\  c 

\           J£- 

, ' 

/\                                     / 
I             \                          ' 

If    !  -\Xb) 

/   A     X(cK 

MP 

Running  costs 

zp\~- 

FlG.  172A.  Annual  steady  yield  of  plaice  plotted  against  mesh  at  various  fishing  intensities. 

The  yield  per  recruit  (  YW\R)  as  a  function  of  tp'  for  various  values  of  F,  to  show  how  the 

height  and  location  of  the  maximum  changes  with  F. 

Fig.  172B.  Eumetric  Yield  curve  for  plaice.  If  a  change  of  mesh  accompanies  a  change  in 
fishing  intensity  in  such  a  way  that  each  value  of  F  is  matched  by  the  mesh  that  would 
give  the  maximum  steady  yield  at  that  value,  the  resultant  curve  of  steady  annual  yield 
per  recruit  (YwjR)  for  plaice  differs  widely  from  that  of  Fig.  171c,  particularly  in  having 

no  maximum. 

Fig.  172c.  An  exercise  in  bionomics.  Curve  (a)  is  a  eumetric  curve  in  which  steady  yield 
instead  of  being  expressed  in  weight  is  now  in  money  value,  which  is  plotted  against  the 
economic  equivalent  of  intensity  of  fishing,  namely,  running  costs.  From  those  are  derived 
(6)  the  annual  profit  and  (c)  the  profit  expressed  as  a  rate  on  running  costs,  which  in  many 
situations  bear  a  constant  relation  to  capital  outlay. 


MP  =  maximum  profit  point;  ZP  =  zero  profit  point. 


xi  CONTROL  OF  FISHING  295 

In  practice  it  is  much  more  economical  to  reduce  the  fishing  mor- 
tality by  lowering  the  number  of  hours  fished  than  by  increasing  the 
mesh  size.  We  require,  therefore,  to  know  the  optimum  mesh  size  for 
each  level  of  fishing  effort.  This  we  can  obtain  by  plotting,  as  in  Fig. 
1 72 a,  a  series  of  yield/mesh  curves  for  different  sizes  of  mesh,  that 
is,  ages  of  recruitment  tp.  From  the  maximum  of  these,  plotted  against 
the  corresponding  fishing  mortality,  we  obtain  Fig.  172B,  known  as 
the  eumetric  yield  curve.  This  shows  an  increasing  yield  towards  an 
asymptote  as  fishing  increases,  but  without  a  maximum. 

Evidently  the  greatest  yield  is  obtained  at  the  highest  fishing  inten- 
sity, but  this  could  be  achieved  only  at  a  prohibitive  cost.  In  order  to 
obtain  the  greatest  possible  yield,  we  have  to  consider  the  cost  of  unit 
effort  of  fishing  and  the  value  of  the  yield.  This  has  been  done,  making 
certain  assumptions,  in  Fig.  172c.  Here  the  eumetric  yield  curve  is 
expressed  by  plotting  value  of  catch  against  running  costs.  Another 
line  shows  the  profit  (total  value  minus  total  cost)  whose  maximum 
might  be  said  in  one  sense  to  be  the  'best'  level  of  fishing.  This  curve 
also  crosses  the  x-axis,  where  there  is  no  profit  in  fishing — -this  being 
the  condition  which  an  uncontrolled  fishery  tends  to  approach. 

Of  course  the  actual  'best'  level  of  fishing  for  any  given  situation 
may  be  affected  by  many  social  and  political  factors.  However,  from 
studies  such  as  these  it  begins  to  be  possible  to  understand  the  vari- 
ables that  are  affecting  a  fishery  and  to  express  them  precisely.  The 
value  of  such  work  is  shown  by  the  fact  that  international  regulation 
of  some  fisheries  has  been  agreed.  For  example,  since  1954  the  white- 
fish  populations  of  the  North  Sea  have  been  regulated  by  control  of 
the  size  of  mesh  used  for  fishing. 


XII 

TERRESTRIAL  VERTEBRATES:  AMPHIBIA 

1 .  Classification 

Class  Amphibia 

*Subclass  i.  *Stegocephalia.  Devonian-Trias 
Order  i.  *Labyrinthodontia.  Devonian-Trias 
Suborder  i.  *Ichthyostegalia.  Upper  Devonian 

*Ichthyostega;  *Elpistostege 
Suborder  2.  *Embolomeri.  Carboniferous 

*Eogyrimis;  *Loxomma 
Suborder  3.  *Rhachitomi.  Carboniferous-Triassic 

*Eryops,  Lower  Permian ;  *Cacops,  Lower  Permian 
Suborder  4.  #Stereospondyli.  Triassic 

*Capitosaurus,  Upper  Triassic;  *Buettneria,  Upper  Triassic 
Order  2.  *Phyllospondyli.  Carboniferous-Lower  Permian 

*Bra?ichiosaurus,  Lower  Permian 
Order  3.  *Lepospondyli.  Carboniferous-Permian 

*Dohchosoma,  Carboniferous ;  *DipIocaulus,  Permian ;  *Micro- 
brachis,  Permian 
Order  4.  *Adelospondyli.  Carboniferous-Lower  Permian 
*Lysorophns,  Carboniferous 
Subclass  2.  Urodcla  (=  Caudata).  Jurassic-Recent 

Molge;  Salamandra;  Ambystoma;  Necturus 
Subclass  3.  Anura  (=  Salientia).  Carboniferous-Recent 
*Miobatrachus;  *Protobatrachiis ; 
Rana;  Bufo;  Hyla;  Pipa 
Subclass  4.  Apoda  (=  Gymnophiona  =  Caecilia).  Recent 
Ichthyophis;  Typhlonectes 

2.  Amphibia 

During  the  later  part  of  the  Devonian  period  a  population  of  lung- 
fishes  lived  in  the  pools  and  there  is  every  reason  to  suppose  that  some 
of  these  animals,  first  crawling  from  pool  to  pool  and  then  spending 
more  time  on  the  land,  gave  rise  to  the  terrestrial  populations  that 
we  distinguish  as  amphibia.  No  doubt  the  early  efforts  at  land  life 
were  crude.  The  whole  locomotory  and  skeletal  system  comes  under 
a  completely  new  set  of  forces  when  the  support  of  the  water  is  with- 


xii.  1-2  AMPHIBIA  297 

drawn  and  the  effects  of  gravity  become  insistent.  At  the  same  time 
the  skin  must  be  changed  to  resist  desiccation,  the  respiratory  system 
adapted  to  use  gaseous  oxygen,  the  receptors  to  signal  the  strange  new 
configurations  of  stimuli.  It  is  not  surprising  that  these  new  conditions 
produced  greater  changes  in  vertebrate  organization  than  had  occurred 
in  tens  of  millions  of  years  previously.  Nevertheless,  so  slow  is  the 
pace  of  evolution,  the  only  known  Devonian  amphibia,  and  many  of 
the  Carboniferous  ones  too,  still  looked  and  presumably  behaved  very 
like  fishes.  Animals  of  this  sort  (e.g.  *Eogyrinus)  floundered  about  on 
land  for  30  million  years  or  more  before  producing  definitely  terrestrial 
types  such  as  the  Permian  *Eryops. 

Of  all  the  features  that  arose  at  this  time  in  connexion  with  the  new 
life  on  land  the  presence  of  pentadactyl  limbs  is  perhaps  the  most 
conspicuous.  It  is  appropriate  that  this  should  be  marked  in  zoological 
nomenclature:  the  amphibia  are  the  first  of  the  great  group  of  land 
vertebrates,  the  Tetrapoda. 

All  existing  amphibia  have  been  much  modified  since  their  Devonian 
ancestry,  yet  they  retain  many  features  that  show  how  the  transition 
from  water  to  land  was  produced.  These  modern  forms  are  by 
no  means  a  precariously  existing  remnant  but  are  quite  numerous 
and  successful  in  the  ecological  niches  that  they  occupy;  they  form 
an  important  element  in  many  food  chains.  There  are  some  2,000 
species  at  present  recognized,  placed  in  250  genera.  However,  con- 
trasting this  with  the  numerous  species  of  teleosts,  of  birds,  and  of 
mammals  we  shall  see  that  the  amphibians,  though  well  adapted  for 
certain  situations,  do  not  succeed  in  maintaining  themselves  in  many 
different  types  of  habitat.  Broadly  speaking  they  are  unable  to  survive 
for  long  except  in  the  proximity  of  water.  There  are  desert  toads,  such 
as  Chiroleptes  of  Australia,  but  these  survive  by  burrowing  and  by 
special  abilities,  such  as  the  power  to  hold  large  amounts  of  water, 
associated  with  loss  of  the  glomeruli  of  the  kidneys. 

Modern  amphibia  belong  to  three  sharply  separated  subclasses. 
Urodela  (newts  and  salamanders)  retain  the  original  long-bodied, 
partly  fish-like  form.  The  Anura  (frogs  and  toads)  have  lost  the  tail 
and  become  specialized  as  jumpers.  The  Apoda  are  limbless,  blind, 
burrowing  animals  found  in  the  tropics.  The  urodeles  and  anurans 
are  found  as  fossils  back  to  the  Cretaceous  and  Trias  respectively,  but 
we  have  only  scanty  information  about  their  connexion  with  the 
earlier  amphibians,  which  are  grouped  loosely  together  as  the  Steno- 
cephalia. These  are  found  in  rocks  about  275-160  million  years  old, 
that  is  to  say  from  the  late  Devonian  to  the  Trias  (Fig.  211). 


298  AMPHIBIA  xii.  3- 

3.  The  frogs 

Perhaps  the  most  successful  of  all  amphibia  are  those  belonging 
to  the  genus  Rana,  abundant  in  every  part  of  the  world  except  in 
the  south  of  South  America,  on  oceanic  islands,  and  New  Zealand. 
Ranid  frogs  are  typical  of  the  highly  specialized  subclass  Anura,  whose 
members  usually  inhabit  damp  places  such  as  marshes  or  ditches, 
living  for  most  of  their  life  in  the  grass  or  undergrowth  and  feeding  by 
catching  flies  and  other  insects  with  their  tongue.  They  are  preyed 
upon  by  birds,  fishes,  and  especially  snakes,  and  escape  from  these  by 
their  hind  legs,  used  either  for  jumping  or  swimming.  The  young 
develop  as  tadpoles  in  the  water,  where  they  are  omnivorous.  The 
various  species  differ  in  size  and  small  points  of  colour,  though  there 
are  also  some  that  depart  widely  from  the  usual  habits,  e.g.  R.  fossor 
which  burrows.  R.  temporaria  is  the  species  found  in  Great  Britain, 
R.  esculenta  is  a  slightly  larger  form  found  on  the  continent  of  Europe 
and  occasionally  in  east  England,  R.  pipiens  is  the  common  small 
North  American  frog;  R.  catesbiana  the  giant  bull-frog,  whose  body 
is  up  to  9  in.  long,  also  lives  in  North  America.  R.  goliath  of  the 
Cameroons  is  over  a  foot  long,  but  is  mainly  aquatic. 

4.  Skin  of  Amphibia 

The  earliest  amphibia  possessed  the  scales  of  their  fish  ancestors, 
but  these  were  soon  lost  in  most  lines,  though  retained  in  some 
Apoda;  perhaps  they  were  too  heavy  to  be  worth  while  for  creatures 
contending  for  the  first  time  with  gravity,  unaided  by  water.  Some 
frogs  carry  dermal  plates  on  the  back,  however,  fused  to  the  neural 
spines  (Brachycephahis  of  Brazil).  Amphibia  differ  from  reptiles  in 
that  the  skin  is  moist  and  used  for  respiration;  on  the  other  hand,  the 
skin  also  shows  a  character  typical  of  land  animals  in  having  heavily 
cornified  outer  layers.  The  epidermis  therefore  consists  of  several 
layers  in  the  adult  frog  and  is  renewed  at  intervals  by  a  process  of 
moulting.  The  moult  is  under  the  control  of  the  pituitary  and  thyroid 
glands  and  does  not  occur  if  either  of  these  be  removed,  the  kera- 
tinized cells  merely  accumulating  in  those  circumstances  as  a  thick 
skin.  Local  thickenings  of  the  epidermis  often  occur  in  amphibia,  for 
instance  to  form  the  horny  teeth  by  which  the  larva  feeds.  Such  thick- 
enings are  also  a  conspicuous  feature  of  the  warty  skin  of  the  toads 
(Bufo),  which  mostly  have  a  drier  skin  and  are  more  fully  terrestrial 
than  are  the  frogs.  The  fact  that  the  epidermis  of  amphibia  can  pro- 
duce local  thickenings  is  of  interest  in  considering  the  origin  of 
feathers  and  hairs.  In  larval  amphibians  the  skin  is  ciliated. 


xii.  5  SKIN  OF  AMPHIBIA  299 

The  glands  of  the  skin  are  more  highly  developed  than  in  fishes, 
and  are  of  two  types,  mucous  and  poison  glands.  Both  of  these  consist 
of  little  sacs  of  gland-cells,  derived  from  the  epidermis.  The  mucus 
serves  to  keep  the  skin  moist,  this  being  essential  if  the  skin  is  to 
respire;  the  secretion  may  perhaps  also  serve  for  temperature  regula- 
tion. The  problem  of  regulation  of  temperature  is  important  for  all 
terrestial  animals,  since  air  conducts  heat  much  less  well  than  water 
and  therefore  violent  changes  of  temperature  are  met.  Evaporation 
produces  large  influences  on  temperature  and  no  doubt  it  was  the 
adjustment  of  these  effects  that  led  to  the  development  of  temperature- 
regulating  mechanisms  in  birds  and  mammals.  Frogs  in  dry  air  are 
always  found  to  be  colder  than  their  environment,  the  difference 
being  sometimes  as  much  as  50  C.  It  is  probable  that  in  some  cir- 
cumstances use  is  made  of  this  cooling,  since  tree-frogs  (Hyla)  may 
be  found  fully  exposed  to  tropical  sunlight,  which  would  be  expected 
to  raise  their  temperatures  to  a  lethal  level.  On  the  other  hand,  the 
loss  of  water  involved  by  evaporation  in  this  way  would  presumably 
soon  become  serious. 

The  poison  glands  or  granular  glands  are  less  developed  in  Rana 
than  in  Bufo  ('the  envenom'd  toad')  where  they  are  collected  into 
masses,  the  parotoid  glands.  The  effect  of  the  poison  on  man  is  to 
produce  an  irritation  of  the  eyes  and  nose;  only  rarely  does  it  affect 
the  skin  of  the  hands.  When  swallowed  it  produces  nausea  and  has 
a  digitalis-like  action  on  the  heart.  The  poison  of  Dendrobates  of 
Colombia  is  used  on  arrows;  it  acts  on  the  nervous  system. 

Some  amphibia  have  characteristic  smells,  produced  by  secretions, 
and  these  are  probably  used  to  attract  the  sexes  to  each  other.  In 
some  male  newts  (Plethodontidae)  there  are  special  collections  of  these 
gland-cells  below  the  chin. 

Another  use  of  glandular  secretions  is  to  keep  the  eyes  and  nostrils 
free  from  obstruction.  The  demands  of  terrestrial  life  require  the 
production  of  numerous  such  special  devices  and  lead  to  the  com- 
plexity that  we  recognize  as  an  attribute  of  these  'higher'  animals. 

5.  Colours  of  Amphibia 

The  use  of  colour  is  also  highly  developed  in  amphibia.  The 
animals  are  often  greenish  and  the  colour  is  produced  by  three  layers 
of  pigment  cells,  melanophores  lying  deepest,  guanophores,  full  of 
granules,  which  by  diffraction  produce  a  blue-green  colour,  and  yellow 
lipophores,  overlying  these  and  filtering  out  the  blue.  Change  of  colour 
is  produced  by  expansion  of  the  pigment  in  the  melanophores  under 


300 


AMPHIBIA 


xii.  5 


the  action  of  the  secretion  of  the  pituitary  gland  (Fig.  173).  Move- 
ments in  the  other  chromatophores  can  also  affect  the  colour,  yellow 
being  produced  by  disarrangement  of  the  guanophores  and  so  on. 
Other  colours  may  contribute  to  the  patterns,  blue  (though  rarely) 
by  the  absence  of  the  lipophores,  red  by  pigment  in  the  lipophores. 
Changes  in  the  melanophores  may  be  of  two  sorts,  primary  or 
direct  and  secondary  or  visual.  The  primary  response  depends  on  the 


Fig.  173.  Stages  of  dispersal  of  pigment  in  the  melanophores  in  the  web  of 

the  frog  Xenopus,  as  used  by  Hogben  to  assess  the  melanophore  index. 

(After  Hogben  and  Slome,  Proc.  Roy.  Soc.  B.  108.) 

direct  effect  of  light  on  the  skin,  causing  expansion.  The  secondary 
effect  consists  in  contraction  of  the  pigment  if  the  animal  is  illumin- 
ated on  a  light-scattering  surface  (light  background)  but  expansion 
(and  hence  darkening  of  the  animal)  when  it  is  illuminated  from  above 
on  a  light-absorbing  (dark)  background.  There  are,  therefore,  distinct 
responses  from  different  parts  of  the  retina.  Illumination  of  the  dorsal 
part  produces  contraction,  of  the  ventral  part  expansion  of  the 
melanophores. 

Hogben  and  his  co-workers  have  shown  that  the  control  of  the 
colour  change  of  amphibians  is  mediated  by  variation  in  the  secretion 
of  the  pituitary  gland ;  there  is  no  direct  nervous  control  of  the  melano- 
phores. There  is  still  some  doubt  whether  the  pituitary  produces  its 
effects  by  means  of  one  hormone  or  two.  The  most  fully  known  in- 
fluence is  that  of  the  posterior  lobe,  producing  a  B  substance,  also 
known  as  intermedin,  which  makes  the  melanophores  expand.  Ex- 


xii.  5 


COLOUR  CHANGE  IN  AMPHIBIA 


301 


tracts  of  the  pituitary  of  mammals  (or  other  vertebrates)  produce  this 
effect  when  injected  into  frogs,  and  after  removal  of  the  pituitary  a 
frog  becomes  pale  in  colour.  There  is  also  some  evidence  for  secre- 
tion bv  the  anterior  lobe  of  a  W  substance  that  causes  paling.  After 
removal  of  the  whole  pituitary  the  melanophores  are  found  to  be  not 
in  the  wholly  contracted  stage  1  of  Hogben's  melanophore  index  (Fig. 
173)  but  in  a  state  (stage  2  or  3)  intermediate  between  this  and  full 
expansion  (stage  5).  If,  however,  the  posterior  lobe  alone  is  removed 
the  animal  becomes  completely  pale  (stage  1).  This  certainly  suggests 


10      12     14 
Hours 

Fig.  174.  Effect  of  an  extract  containing  the  b  (melanophore-expanding)  substance  on 

three  groups  of  Xenopus.  All  were  of  the  same  weight  and  received  the  same  dose. 

A,  whole  pituitary  removed;  D,  intact  animals;  c,  posterior  lobe  only  removed. 

(From  Waring,  after  Hogben  and  Slome.) 

the  secretion  of  a  W  substance  by  the  pars  anterior.  There  are  also 
differences  in  the  response  to  injection  of  B-containing  extracts  after 
total  and  partial  removal  of  the  pituitary  (Fig.  174).  The  position  is 
complicated  by  the  fact  that  extracts  of  mammalian  pineal  or  adrenal 
medulla  will  cause  contraction  of  amphibian  melanophores,  though  it 
is  uncertain  whether  these  effects  have  any  physiological  significance. 

In  amphibia  there  is  no  direct  control  of  the  pigment  cells  by 
nerve-fibres  such  as  are  present  in  bony  fishes  (p.  259).  The  colour 
change  is  therefore  rather  slow.  After  removal  of  the  pituitary  the 
melanophores  still  show  slight  changes  correlated  with  change  of  in- 
cident illumination,  indicating  a  small  degree  of  direct  response  as 
independent  effectors.  Temperature  and  humidity  also  influence  the 
colour  in  many  amphibia.  In  frogs  contact  with  water  accentuates  the 
black-background  response  and  in  darkness  produces  expansion.  On 
the  other  hand,  drying  induces  contraction  of  the  melanophores,  even 
upon  a  black  background. 

The  colour  patterns  adopted  are  usually  cryptic  or  concealing  in 
their  effect,  but  the  colour  also  has  an  important  influence  on  the 
temperature  and  varies  with  it  and  with  the  humidity,  as  well  as  with 
the  incident  illumination.  The  uniform  brilliant  green  of  tree-frogs 


3o2  AMPHIBIA  xii.  5- 

makes  them  very  difficult  to  see  among  the  leaves;  on  the  other  hand, 
R.  temporaria  and  other  species  living  among  grass  show  a  pattern  of 
dark  marks,  which  breaks  up  their  outline.  In  other  amphibians,  how- 
ever, the  colour  makes  the  animal 
conspicuous,  for  instance  the 
black  and  yellow  markings  of 
Salamandra  maculosa.  Conspi- 
cuous colour  is  often  associated 
with  great  development  of  the 
poisonous  parotoid  glands  and 
is  therefore  presumably  sematic 
or  warning  coloration,  allowing 
recognition  by  possible  attackers. 
This  correlation  is  not  always 
found,  however;  the  toad  Cera- 
tophrysamericanaisd\i\\co\o\irtd 
but  poisonous,  whereas  C.  dor- 
sata  has  a  bright  pattern  but  is 
harmless. 

Many  frogs  make  a  sudden 
exposure  of  brightly  coloured 
patches  on  the  thighs  when  they 
jump.  This  presumably  serves 
to  startle  the  attacker  and  such 
colours  may  be  called  dymantic 
or  startling.  A  similar  use  of 
colour  is  made  by  the  cuttle- 
fish (Sepia),  which  may  suddenly 
produce  two  black  spots  when 
alarmed,  and  also  by  some  Lepi- 
doptera.  It  is  interesting  that  the 
colour  used  in  this  way  so  often 
takes  the  form  of  black  spots 
('eye-spots'),  which  have  an  es- 
pecially striking  quality.  In  some  anurans  these  colours  are  irregular 
dark  marks,  but  in  Mantipus  ocellatus  they  take  the  form  of  definite 
'eye-spots'. 

It  must  not  be  forgotten  that  the  presence  of  pigment  serves  to 
protect  the  organs  from  the  effects  of  light,  which  may  cause  contrac- 
tion when  it  falls  directly  upon  muscles.  Dark  colour  may  also  assist 
in  the  absorption  of  heat,  both  in  the  adults  and  in  the  eggs. 


(a)  (b) 

Fig.  175.  Record  of  the  movements  of 
Ambystoma  walking  on  a  smoked  drum, 
a,  in  rapid  locomotion  (with  the  body  on 
the  ground);  b,  in  slow  locomotion  (raised 
up  on  the  legs).  (From  Evans,  Anat.  Rec. 
95.) 


xn.  6 


(3°3) 


6.  Vertebral  column  of  Amphibia 

The  general  build  of  the  body  is  essentially  fish-like  in  stegocepha- 
lian  and  urodele  amphibians.  Such  forms  have  two  means  of  locomo- 
tion. When  they  are  frightened  and  move  fast  they  wriggle  along  with 
the  belly  on  the  ground,  the  effective  agent  being  serial  contraction 
of  the  segmentally  arranged  myotomal  musculature,  by  means  of  which 
the  animal  as  it  were  'swims  on  land',  with  the  legs  hardly  touching 
the  ground  (Fig.  175).  When  moving  deliberately,  on  the  other  hand, 


Fig.  176.  Drawings  made  from  photographs  of  a  newt  (Triturus) 
in  slow  locomotion.  (After  Evans,  Anat.  Rec.  95.) 

a  newt  raises  up  its  body  on  the  legs,  which  then  propel  it  along  as 
movable  levers,  the  main  part  of  the  action  being  produced  by  drawing 
back  the  humerus  or  femur,  the  more  distal  muscles  of  the  limbs 
serving  to  maintain  the  digits  pressed  against  the  ground  (Fig.  176). 
The  carrying  of  the  weight  on  four  legs  places  an  entirely  new  set 
of  stresses  on  the  vertebral  column.  Instead  of  being  mainly  a  com- 
pression member  as  it  is  in  fishes  it  comes  to  act  as  a  girder,  carrying 
the  weight  of  the  body  and  transmitting  it  to  the  legs.  This  new 
function  produces  a  column  whose  parts  are  largely  bony  and  articu- 
lated together,  flexibility  becoming  less  important  than  strength.  The 
new  types  of  strain  involve  new  muscle  attachments  and  the  develop- 
ment of  special  processes  and  parts  of  the  vertebrae  (p.  307).  These 
changes,  however,  have  not  proceeded  very  far  in  the  amphibians; 
many  urodeles  spend  much  time  in  the  water  and  their  vertebrae  often 
show  a  lack  of  ossification,  parts  of  the  notochord  persist  and  provide 
the  main  compression  member  required  for  swimming. 


3°4 


AMPHIBIA 


xii.  6 


In  the  anurans  the  entire  skeletal  and  muscular  system  has  become 
specialized  for  the  peculiar  swimming  and  jumping  methods  of  loco- 
motion, by  means  of  extensor  thrusts  of  both  hind  limbs,  acting 


Fig.  177.  Reflexes  associated  with  the  transition  from  swimming  to  walking  in  toads. 
The  shaded  outlines  show  successive  positions  as  the  animal  emerges  on  to  solid  ground. 
The  first  effective  contact  is  by  the  left  fore-limb  whose  retraction  and  extension 
elicits  a  crossed  protraction  reflex  in  the  right  fore-limb  (Lj),  a  diagonal  extensor 
response  in  the  right  hind-limb  (L2),  and  a  placing  response  in  the  left  hind-limb  (L3). 
The  right  fore-limb  then  touches  the  ground  and  produces  corresponding  responses 
Rx-3.  The  left  fore-limb  in  response  to  stretch  of  its  protractor  muscles  swings  forward 
and  this  produces  retraction  of  the  left  hind-limb  (L4)  and  protraction  of  the  right 
hind-limb  (L5).  Fixation  of  the  right  hind  foot  then  produces  a  crossed  flexor  response 
(RHJ.  (From  Gray,  J.  exp.  Biol.  23.) 

together.  Frogs,  and  especially  toads,  also  walk  on  land,  bringing  into 
play  a  set  of  myotactic  (proprioceptor)  reflexes  that  depend  on  the 
contraction  of  the  muscles  against  an  external  resistance  (Fig.  177). 

The  actions  of  jumping  and  walking  are  possible  because  of  pro- 
found changes  in  the  arrangement  of  the  skeleton  and  muscles.  The 
myotomal  muscles  no  longer  perform  their  primitive  function  of  pro- 
ducing metachronal  waves  of  contraction,  and  accordingly  the  verte- 
bral column  (Fig.  178)  has  lost  its  original  flexibility.  Instead,  it  is 


xii.  6 


VERTEBRAL  COLUMN 


305 


Fig.   178.   The  skeleton  of  the  frog,  seen  from  the  dorsal  surface;  the  left 
suprascapular  and  scapular  have  been  removed. 

a.  astragalus;  c.  calcaneum;  d.  suprascapular;  e.  exoccipital ; /.  femur;//),  frontoparietal; 
g.  metacarpals;  h.  humerus;  i.  ilium;  k.  metatarsals;  /.  carpus;  m.  maxilla;  w.  nasal;  o.  pro- 
otic;  p.   pterygoid;  pm.   premaxilla;  q.   'quadratojugal';   r.   radio-ulna;  J.   squamosal;  se. 
sphenethmoid;  s.v.  sacral  vertebra;  t.  tibio-fibula;  u.  urostyle. 
(After  Marshall,  The  Frog,  Macmillan.) 

attached  to  the  pelvic  girdle  and  acts  as  a  support  by  which  the 
movement  of  the  hind  limbs  is  transmitted  to  the  rest  of  the  body. 
There  is  no  longer  any  sinuous  motion  and  the  number  of  vertebrae 
is  very  low  (nine  in  the  adult  Ra?ia),  and  behind  them  is  an  unseg- 
mented  rod  of  'hypochordal'  bone,  the  urostyle.  Shortening  of  the 
body  is  a  characteristic  feature  of  the  change  from  aquatic  to  terrestrial 


(3o6) 


Fig.  179.  Transformation  of  crossopterygian  pectoral  girdle  and  fin  into 
pentadactyle  limb.  Oblique  front  view  of  left  side. 

a,  *Eusthenopteron\  b,  *Eogyrinus;  c,  *Eryops;  clt.  cleithrum;  civ.  clavicle; 

h.   humerus;    p.  pubis;   sc.    scapula;   s.cl.   supracleichrum.   (Modified  from 

Gregory  and  Raven,  Ann.  N.Y.  Acad.  Sci.  42.) 


Fig.  180.  Transformation  of  crossopterygian  pelvic  fin  into  tetrapod  limb. 

a,  *Eusthenopteron;  B,  hypothetical;  c,  *Trematops.  f.  femur;  fi.  fibula;  il.  ilium; 
is.  ischium;  t.  tibia.  (Modified  from  Gregory  and  Raven.) 


xii.  6-7  AMPHIBIAN  LIMBS  307 

life,  and  is  seen  in  many  lines  of  amphibian  and  reptilian  evolution. 
It  has  proceeded  farther  in  the  frogs  than  in  any  other  tetrapods. 

The  second  to  eighth  vertebrae  of  Rana  are  concave  in  front,  con- 
vex behind  (procoelous),  and  have  large  transverse  processes.  In  other 
amphibians  they  may  be  amphicoelous  or  opisthocoelous.  They  fit 
together  by  complex  zygapophyses.  The  first  vertebra  has  two  con- 
cave facets  for  articulation  with  the  two  condyles  of  the  skull;  its 
centrum   and  transverse  processes  are  much   reduced.   The   ninth 


Fig.  181.  Diagrams  illustrating  the  probable  changes  in  position  during  the 
evolution  of  a  pelvic  fin  into  a  tetrapod  limb.  A  as  in  Ceratodus;  B,  double 
flexure  to  give  knee  and  ankle  joints,  leaving  foot  direct  backwards;  c  and 
D,  rotation  of  tarsus  and  digits  turning  foot  forward.  (From  Gregory  and 
Raven,  after  Romer  and  Byrne.) 

(sacral)  vertebra  has  large  transverse  processes,  which  articulate  with 
the  ilia  of  the  pelvic  girdle.  There  are  free  ribs  in  the  primitive  frogs 
Ascaphus  and  Leiopelma. 

7.  Evolution  and  plan  of  the  limbs  of  Amphibia 

The  girdles  of  the  paired  limbs  have  become  much  changed  from 
their  fish-like  condition  (Figs.  179  and  180).  Their  basic  pattern  is 
similar  in  the  two  limbs  and  has  been  retained  throughout  the  wrhole 
tetrapod  series.  Whereas  in  fishes  the  girdles  are  rather  small  carti- 
lages and  bones,  the  pelvic  girdle  being  restricted  to  the  ventral  region 
of  the  body,  in  amphibians  they  become  enlarged  in  connexion  with 
the  wTeight-bearing  function  of  the  limbs. 

The  details  of  the  sequence  of  stages  by  which  a  tetrapod  limb 
arose  from  a  fish  fin  are  still  somewhat  disputed.  It  is  probable  that 
the  ancestral  crossopterygian  possessed  a  lobed  fin,  rather  like  that 
seen  in  *Eusthenopteron  (Fig.  179).  As  the  fishes  came  on  land  the  fin 


3o8  AMPHIBIA  xn.  7- 

would  be  used  as  a  lever,  giving  greater  effect  to  the  wave-like  motions 
by  which  the  creature  'swam  on  land'.  The  muscles  of  the  limb,  con- 
tracting in  a  serial  manner,  would  tend  to  move  it  backwards  and 
forwards  relative  to  the  body,  thus  assisting  in  locomotion.  At  first 
the  limb  perhaps  carried  only  little  weight,  but  as  tetrapod  evolution 
proceeded  the  limbs  became  elongated  and  turned  under  the  body, 
raising  it  off  the  ground.  To  work  effectively  in  this  way  the  limbs 
came  to  be  held  bent  down  at  elbow  and  knee  (Fig.  181)  and  a  firm 
application  to  the  ground  was  produced  by  bending  outwards  at 
wrist  and  ankle.  Finally  the  limbs  were  brought  in  to  the  side  of  the 


Fig.  182.  Suggested  protetrapod  stage,  between  crossopterygian  and  labyrinthodont. 
(From  Oregon-  and  Raven.) 


body  by  rotation,  such  that  the  elbow  pointed  backward  and  the  knee 
forward. 

These  are  the  changes  that  must  have  occurred  at  some  time  to 
produce  the  full  tetrapod  condition,  but  we  cannot  follow  exactly  the 
order  in  which  they  took  place.  Their  effect  is  to  convert  a  paddle- 
like fin,  whose  main  movements  were  up  and  down,  and  were  used 
for  stabilization  in  the  horizontal  swimming  plane,  into  an  elongated 
jointed  strut,  on  which  the  animal  can  balance,  and  which  can  be 
moved  as  a  lever  to  produce  locomotion. 

The  limbs  and  girdles  and  their  muscles  show  a  remarkable  con- 
stancy of  pattern  throughout  the  tetrapods.  The  muscles  of  the  fins  of 
fishes  are  concerned  mainly  with  lowering  and  raising  (Fig.  192),  and 
they  run  from  a  girdle  in  the  body  wall  to  the  basal  radials  in  the  fin, 
and  between  the  radials.  After  the  animals  came  on  land  the  muscles 
served  not  only  to  raise  and  lower  the  limbs  but  also  to  draw  them 
forwards  and  backwards;  indeed,  many  fishes  already  make  such 
movements,  including  Protopterns.  The  muscles  therefore  become 
arranged  around  the  shoulder  and  hip  joints  into  groups  serving  as 
adjustable  braces,  by  which  the  body  is  balanced  on  its  legs  and  by 
whose  contraction  the  latter  are  moved.  Those  muscles  that  draw 
the  limb  towards  and  away  from  the  mid-ventral  line  can  be  called 


xii.  8  SHOULDER  GIRDLE  309 

medial  and  lateral  braces  (adductors  and  abductors)  and  the  muscles 
drawing  the  leg  backwards  and  forwards  are  posterior  and  anterior 
(retractor  and  protractor)  braces.  For  the  attachment  of  these  muscles 
proximally  the  pectoral  and  pelvic  girdles,  small  in  fishes,  become 
expanded  into  plates  (Figs.  180  to  182),  and  these  are  divided  into 
a  number  of  characteristic  pieces,  though  the  mechanical  reason  for 
the  division  is  not  clear. 

8.  Shoulder  girdle  of  Amphibia 

The  earliest  labyrinthodonts  (e.g.  *Eogyrinus)  inherited  a  shoulder 
girdle  almost  exactly  like  that  of  their  osteolepid  ancestors  except  that 
a  new  dermal  element,  the  interclavicle,  was  added  to  the  ventral 
surface.  Although  the  presence  of  a  sternum  has  never  actually  been 
recorded,  it  is  generally  assumed  that  a  cartilaginous  structure  of  this 
type  was  present  between  the  hindermost  margins  of  the  epicoracoid 
cartilages.  As  in  gnathostomes  generally  (except  elasmobranchs)  the 
shoulder  girdle  was  a  dual  structure  consisting  of  (a)  a  primary  or 
endochondral  component  evolved  from  the  basal  fin  elements  of  the 
ancestral  fish  form  and  serving  to  provide  an  articulatory  surface  for 
the  limb  as  well  as  points  of  attachment  for  the  limb  musculature,  and 
(b)  a  dermal  ring  of  bony  elements  (skin  scales)  which  had  sunk 
inwards  and  applied  themselves  to  the  ventro-anterior  surfaces  of  the 
endochondral  girdle  which,  consequently,  they  braced  and  supported. 

The  endochondral  girdle  consisted  of  two  half  rings,  which  over- 
lapped in  the  ventral  midline.  Each  half  was  a  single  unit  but,  by 
topographical  comparison  with  girdles  of  later  tetrapods,  it  is  often 
arbitrarily  divided  into  two  regions,  a  dorsal  scapula  and  a  ventral 
coracoid.  Between  these  two  regions  a  screw-shaped  glenoid  received 
the  humerus.  The  one  endochondral  ossification  is  usually  homo- 
logized  with  the  scapula  of  amniotes  (Watson,  191 7).  Later  forms 
(e.g.  * Seymonria,  *Diadectes)  possessed  a  second  bony  element  which 
is  generally  interpreted  as  a  precoracoid.  The  endochondral  girdle  was 
small  in  the  earliest  amphibia  (e.g.  *Eogyrinus).  In  later  genera  its  size 
progressively  increased,  presumably  to  withstand  the  greater  thrust 
transmitted  by  the  larger  limbs  of  these  forms  and  to  provide  attach- 
ment for  the  increased  mass  of  brachial  musculature. 

The  dermal  girdle  consisted,  typically,  of  paired  cleithra,  clavicles, 
and  interclavicle.  The  latter,  a  new  element,  lay  between  and  often 
beneath  the  clavicles  and,  together  with  the  sternum,  probably  formed 
a  locking  mechanism  preventing  the  complete  separation  of  the  epi- 
coracoid  cartilages.  In  the  earliest  rhachitomes  (e.g.  *Eogyrinus)  the 


310  AMPHIBIA  xii.  8 

dermal  girdle  was  attached  to  the  post-temporal  region  of  the  skull, 
as  in  bony  fish.  This  connexion  was  soon  lost  in  later  forms,  pre- 
sumably to  permit  greater  mobility  of  the  head.  This  foreshadowed 
the  reduction  and  loss  that  was  the  subsequent  fate  of  the  dermal, 
shoulder  girdle  elements  in  tetrapod  evolution. 

Of  the  modern  amphibia,  the  Salientia  most  nearly  approach  the 
condition  of  the  fossil  forms  and  they,  alone,  of  recent  tetrapods,  have 
retained  a  cleithrum.  Each  half  of  the  endochondral  girdle  consists 
of  a  dorsal,  bony  scapula  with  a  cartilaginous  suprascapula,  and  a 
ventral  coracoid  bone  connected  to  an  anterior  precoracoid  cartilage 
by  a  mesial  epicoracoid  cartilage.  The  precoracoids  are  invested  by 
the  clavicles  and,  as  in  all  modern  amphibians,  the  interclavicle  is 
absent. 

Anuran  shoulder  girdles  may  be  divided  into  two  broad  categories 
according  to  whether  the  two  epicoracoid  cartilages  are  fused  mesi- 
ally  (a)  along  their  entire  lengths  (firmisternal  condition)  or  (b)  along 
their  anterior  edges  only  (arciferal  girdles).  The  latter  occurs  typically 
in  'walking',  toad-like  Anura  (e.g.  Bufonidae,  Pelobatidae)  and  in  the 
aquatic  xenopids.  The  clavicles  are  the  main  struts  for  keeping  the 
glenoids  apart  and,  consequently,  they  are  well  developed  and  never 
lost.  The  coracoids,  on  the  other  hand,  may  only  be  moderately  well 
developed.  Immediately  behind  their  point  of  fusion  the  epicoracoid 
cartilages  diverge  and  overlap  and  their  posterior  margins  are  con- 
tinued as  epicoracoid  horns,  which  run  in  lateral  grooves  on  each  side 
of  the  sternum.  The  posterior  tip  of  each  horn  has  a  muscle  attach- 
ment connecting  with  abdominal  recti.  This  type  of  sternum/epi- 
coracoid  system  permits  a  certain  degree  of  independent  movement  of 
the  girdle  halves  whilst,  at  the  same  time,  preventing  the  epicoracoid 
cartilages  from  being  forced  too  far  apart.  The  mechanism  clearly 
facilitates  the  independent  arm  movements  characteristic  of  locomo- 
tion in  the  arciferal  frogs. 

The  firmisternal  girdle  is  a  rigid  structure  allowing  no  independent 
movement  of  the  two  halves  (Fig.  183).  It  occurs  typically  in  frogs 
with  a  jumping  habit  (e.g.  Ranidae,  Microhylidae)  and  provides  an 
excellent  landing  mechanism.  The  glenoids  are  braced  apart  by  the 
large  coracoids.  The  clavicles  and  precoracoids  are  thus  deprived  of 
their  strutting  function  and  frequently  become  reduced  or  even  com- 
pletely lost.  No  epicoracoid  horns  are  present  and  the  sternum,  no 
longer  involved  in  locking  the  girdle  halves,  serves  principally  for  the 
attachment  of  pectoral  muscles.  This  function  is  also  performed,  in 
some  frogs,  by  a  prezonal  (omosternal)  element,  which  is  really  an 


(3ii) 


FROG 


TOAD 


Fig.  183.  Amphibian  pectoral  girdles. 

b.  precoracoid  bridge;  c.  coracoid;  cl.  clavicle;  c.p.  coracoid  process;  c.t.  cleithrum;  d.b. 
dorsal  blade;  e.l.  precoracoid  cartilage;  e.m.  epicoracoid  muscle;  g.  glenoid;  g.f.  glenoid 
fossa;  /;.  epicoracoid  horn;  i.cl.  interclavicle;  /.  left  epicoracoid  cartilage;  pc.  prezonal 
cartilage;  p.o.  prezonal  bone;  po.t.  posterior  temporal;  r.  epicoracoid  cartilage;  s.  sternum; 
sc.  scapula;  sk.  scapulo-coracoid ;  s.o.  sternal  bone;  s.r.  ventral  blade;  ss.  suprascapular 
cartilage;  st.c.  sternal  cartilage;  su.  coraco-cleithral  suture;  sup.ct.  supra-cleithrum. 


312 


AMPHIBIA 


xn.  8- 


extension  of  the  precoracoid  cartilages.  This  structure,  although 
present  in  some  arciferal  girdles  (e.g.  Leptodactylidae),  is  more  usually 
associated  with  the  firmisternal  pattern  and  a  jumping  habit. 

The  shoulder  girdles  of  modern  urodeles  are  greatly  simplified,  the 
only  ossification  being  a  scapulo-coracoid  encircling  the  glenoid.  The 
two  epicoracoids  overlap  broadly,  and  anteriorly  are  quite  free  of 
each  other;  posteriorly  they  are  usually  rather  weakly  locked  by  a 


LEPTODACTYLUS 

Fig.   183(a).   Leptodactylus  pragnathus.   Ventral  view  showing  sternal  articulation  with 
girdle.  The  left  half  of  the  ventral  sternal  blade  has  been  removed.  Labelling  as  in  Fig.  1 83 . 

cartilaginous  sternum.  The  Apoda,  of  course,  retain  no  vestiges  of 
either  limbs  or  limb  girdles. 


9.  Pelvic  girdle  of  Amphibia 

The  pelvic  girdle  is  much  larger  in  land  animals  than  the  small 
ventral  cartilages  found  in  fishes.  It  is  formed  of  three  main  cartilage 
bones  in  all  tetrapods  (Fig.  184),  but  it  is  not  clear  how  these  origin- 
ated, nor  whether  the  division  has  mechanical  significance.  The  dorsal 
ilium  becomes  attached  to  specially  modified  transverse  processes  of 
one  or  more  sacral  vertebrae.  This  ilium  can  be  regarded  mechanically 
as  the  ossification  along  a  line  of  compression  stress  due  to  the  weight- 
bearing. 

The  ventral  portion  of  the  girdle  consists  of  an  anterior  pubis  and 
posterior  ischium,  the  three  bones  meeting  at  the  acetabulum,  where 


XII.   IO 


PELVIC  GIRDLE 


313 


the  femur  articulates.  The  girdle  thus  provides  a  plate  to  which  the 
muscles  that  brace  the  limb  can  be  attached  in  such  a  way  as  to 
balance  the  body  on  the  leg. 

In  urodeles  the  pelvic,  like  the  pectoral,  girdle  becomes  reduced  and 
mainly  cartilaginous.  The  pelvic  girdle  of  anurans  is  highly  specialized 
and  unlike  that  of  any  other  vertebrate.  The  ilia  are  very  long  and 
directed  forward  to  articulate  with  the  transverse  processes  of  the  single 
pair  of  sacral  vertebrae.  The  base  of  the  ilium  is  expanded  to  make  the 


ac.  Cryptobranchus 

is.  it-    % 


Eryops 


Necturus  p. 


Iguana 

Fig.  184.  Pelvic  girdles  of  lower  tetrapods.  Regions  mainly  cartilaginous  are  stippled. 
ac.  acetabulum;  /'/.  ilium;  is.  ischium;  of.  obturator  foramen;  p.  pubis.  (After  Evans.) 

dorsal  portion  of  a  disk,  of  which  the  pubis  is  the  anterior,  the  ischium 
the  posterior  part,  with  the  acetabulum  at  the  centre.  The  girdle  is 
thus  developed  into  a  long  lever  for  transferring  force  from  the  limb 
to  the  vertebral  column  during  jumping. 

Considerable  movement  is  possible  at  the  ilio-sacral  joints,  at  least 
in  Salientia  (Whiting,  1961).  In  Rana  the  ilia  may  rotate  through  an 
angle  of  over  900  on  the  sacral  ribs  in  the  vertical  plane.  This  move- 
ment is  used  during  a  strong  leap.  In  Discoglossus  the  sacrum  can  be 
turned  laterally  on  the  pelvis  through  20°.  The  movement  is  used  both 
in  turning  to  take  food  and  in  locomotion.  In  Xenopus  the  sacrum 
can  slide  backwards  and  forwards  on  the  pelvis,  producing  a  con- 
siderable shortening  and  lengthening  of  the  whole  animal.  This 
movement  is  probably  used  in  driving  into  the  mud. 

10.  The  limbs  of  Amphibia 

The  pattern  of  bones  and  muscles  in  fore  and  hind  limbs  of  tetrapods 
is  surprisingly  constant  in  spite  of  the  various  uses  to  which  the  limbs 


3'4 


AMPHIBIA 


XII.  10 


are  put.  Evidently  similar  morphogenetic  processes  are  at  work  in 
both  limbs.  There  are  nearly  always  three  main  joints  in  each  limb, 
at  shoulder  (hip),  elbow  (knee),  and  wrist  (ankle).  The  hand  and  foot 
provide  basically  similar  five-rayed  levers,  with  several  joints  in  the 
digits  (Figs.  185  and  186). 

The  bones  of  the  limbs  can  be  plausibly  derived  from  those  of  a 
crossopterygian  fin,  and  indeed  the  condition  in  *Eusthenopteron 
already  distinctly  suggests  that  of  the  limb  of  an  early  amphibian  (Figs. 
179  and  180).  We  know  less  about  the  origin  of  the  hind  than  of  the 
front  leg,  but  the  two  are  so  similar  that  they  may  be  treated  together 
for  elementary  analysis.  There  is  a  basal  humerus  (femur),  articulating 
distally  with  two  bones  in  each  case,  a  more  anterior  (pre-axial)  radius 
(tibia)  and  a  posterior  (post-axial)  ulna  (fibula).  These  bones  articu- 
late at  the  wrist  or  ankle  with  a  carpus  or  tarsus,  consisting,  in  the  fully 
developed  condition,  of  three  rows  of  little  bones,  namely  3  in  the 
proximal  row,  about  3  centrals,  and  5  distals.  Each  of  the  latter  carries 
a  digit,  composed  of  numerous  jointed  phalanges.  In  naming  these 
bones  of  the  carpus  and  tarsus  it  is  convenient  to  call  the  proximal 
carpals  by  their  position  radiale,  intermedium,  and  ulnare  and  the 
tarsals  tibiale,  intermedium,  and  fibulare.  The  centrals  and  distal 
carpals  may  then  be  numbered  beginning  with  1  at  the  pre-axial 
border  in  each  case.  Unfortunately  other  less  explicit  systems  of 
naming  are  in  use,  as  shown  in  the  following  table. 

Plan  of  the  Tetrapod  Carpus  and  Tarsus.  {The  names  used  for  the  bones 
in  man  are  shown  in  brackets.) 

Carpus 


Pre-axial 

Post-axial 

Proximal 

radiale  (scaphoid) 

intermedium 
(lunate) 

ulnare  (triquetral) 

Central 

centrale  (tubercle 
of  scaphoid) 

Distal 

carpal  i 

2 

3 

4  and  5 

(trapezium) 

(trapezoid) 

Tarsus 

(capitate) 

(hamate) 

Pre-axial 

Post-axial 

Proximal 

tibiale  (talus  or 
astragalus) 

intermedium  (os 
trigonum) 

fibulare  (calcaneum) 

Central 

centrale  (navicular) 

Distal 

tarsal  i 

2 

3 

4  and  5 

(medial  cuneiform)    (intermediate 

(lateral  cuneiform) 

(cuboid) 

cuneiform) 

The  plan  of  the  carpals  and  tarsals  can  well  be  imagined  to  have  been 
derived  from  that  of  a  fin  such  as  is  seen  in  the  fish  *Eusthenopteron 
(Fig.  179),  which  might  be  said  to  have  humerus,  radius,  and  ulna, 


(315) 


^•^        Nee  tar  us 
Cryptobranchus 

Fig.  185.  Front  legs  of  various  lower  tetrapods. 
H.  humerus;  R.  radius;  u.  ulna.  (Modified  from  Evans,  J.  Morph.  74.) 


1    m    w 

Trematops 


I 

Cryptobranchus 


Fig.  186.  Hind  legs  of  various  tetrapods. 
F.  femur;  FI.  fibula;  T.  tibia.  (Modified  from  Evans.) 


(3i6) 


Fig.  187.  R.  temporaria  dissected  from  the  back. 

add.  adductor;  anc.  anconeus  ('triceps');  c.  calcar;  c.sacr.  coccygeo-sacralis;  cocc.il.  coc- 
cygeo-iliacus ;  cue.  cucullaris ;  delt.  deltoid ;  dep.  mand.  depressor  mandibulae ;  dors.se.  dorsalis 
scapulae;  ext.obl.  obliquus  externus  abdominis;  fasc.  dors,  dorsal  fascia;  fl.hr.  flexor  brevis; 
gastr.  gastrocnemius;  glut,  gluteus;  il.  ilium;  il.ext.  iliacus  externus;  il.fib.  ilio-fibularis; 
lat.dors.  latissimus  dorsi;  I. dors,  longissimus  dorsi;  n.  nostril;  peron.  peroneus;  pir.  piri- 
formis; rhomb,  rhomboideus;  semi.m.  semimembranosus;  semi.t.  semitendinosus;  t.Ach. 
tendo  Achillis;  t.f.lat.  tensor  fasciae  latae;  tib.ant.  tibialis  anterior;  tr.  transversus  abdo- 
minis; tymp.  tympanum.  (Partly  after  Gaupp.) 


xii.  io  AMPHIBIAN   LIMBS  317 

carpals,  and  7  or  8  digits.  In  the  amphibian  *Eryops  most  of  the  digits 
radiate  from  the  radius,  in  later  forms  mostly  from  the  ulna.  Moreover, 
in  the  hand  of  *Eryops  there  seem  to  have  been  six  digits  and  it  is 
usually  stated  that  the  first  of  these  is  a  pre-pollex  'not  comparable 
with  the  pollex  of  higher  forms'. 

The  effect  of  this  system  is  to  provide  a  lever  that  can  be  held 
firmly  against  the  ground  while  it  is  moved  by  the  muscles  running 
from  the  girdles  to  the  humerus  or  femur.  In  addition  the  lever  is 
itself  extensible  by  means  of  its  own  muscles.  Whatever  may  have 
been  their  origin  in  fishes  these  muscles  in  tetrapods  work  in  such  a 
way  as  to  bend  each  segment  up  and  down.  The  shoulder  and  thigh 
joints  usually  allow  movement  in  several  planes,  both  towards  and 
away  from  the  midline  (adduction  and  abduction),  and  forwards  and 
backwards  (protraction  and  retraction).  As  we  have  seen,  the  animal 
balances  at  these  joints  by  muscles  arranged  round  them.  Movements 
of  rotation  are  also  possible  at  these,  and  sometimes  at  other  joints, 
the  distal  bone  turning  about  its  own  axis  on  the  proximal  one.  Such 
movements  may  be  very  important  for  the  proper  placing  of  the  limbs 
in  walking.  Pronation  is  the  rotation  of  the  radius  about  the  ulnar 
bone,  so  that  the  manus  is  directed  caudally,  supination  being  the 
opposite  movement.  The  terms  flexion  and  extension  are  convenient 
at  certain  joints  (e.g.  the  elbow),  but  have  no  consistent  meaning  with 
reference  to  the  main  axes  of  the  body. 

The  limbs  of  the  earlier  amphibians  were  ponderous  affairs,  with 
large  bones  and  widely  expanded  hands  and  feet  (Figs.  181  and  182). 
It  is  not  certain  exactly  how  they  were  used ;  probably  they  were  held 
out  sideways,  giving  a  wide  base  on  which  the  somewhat  precarious 
balance  was  maintained,  the  body  being  often  slumped  on  to  the 
ground.  In  modern  urodeles  the  limbs  retain  the  full  pattern  of  parts, 
but  with  imperfect  ossification,  as  would  be  expected  since  they  carry 
little  weight. 

In  frogs,  specialized  for  jumping,  the  radius  and  ulna  are  united  and 
the  carpals  are  reduced  in  number.  There  are  only  four  true  digits,  the 
first  digit  (thumb  or  pollex)  being  reduced.  There  is,  however,  a  small 
extra  ossification,  the  pre-pollex,  which  becomes  well  developed  as  a 
copulatory  organ  in  the  male  and  may  be  compared  with  a  similar 
digit  found  in  some  stegocephalians.  It  is  to  be  expected  that  in  a 
system  of  repeated  parts,  such  as  a  tctrapod  limb,  multiplications  and 
reductions  will  be  common.  It  can  be  imagined  that  they  can  be 
produced  by  changes  in  the  rhythm  of  morphogenetic  processes,  and 
it  is  surprising  that  there  is  such  constancy  in  number  of  digits. 


3i8 


AMPHIBIA 


The  hind  legs  of  frogs  are  long,  giving  a  good  leverage  in  jumping. 
The  tibia  and  fibula  are  united  and  the  proximal  row  of  tarsals  is 
reduced  to  two,  greatly  elongated  and  known  as  the  tibiale  (astragalus 
or  talus)  and  fibulare  (calcaneum).  The  distal  tarsals  are  reduced  to  a 
total  of  three,  bearing  five  'true'  digits  and  an  extra  one,  the  calcar  or 
prehallux. 


semL  m 


Fig.   188.  Deeper  dissection  of  muscles  of  back 
of  frog. 

i.lr.  inter-transversarii;  ur.  urostyle;  v.  vertebra;  other 
letters  as  Fig.  187.  (Partly  after  Gaupp.) 


1 1 .  The  back  and  belly  muscles  of  Amphibia 

With  the  change  in  the  method  of  locomotion  the  muscular  system 
has  become  greatly  modified  from  that  found  in  fishes.  In  urodeles, 
which  still  use  the  old  method  and  hence  may  be  said  to  swim  on  land, 
the  dorsal  musculature  is  well  developed  (Fig.  189),  but  in  anurans  the 
dorsal  portions  of  the  myotomes,  the  epaxial  musculature,  no  longer 
have  to  produce  the  locomotory  effect  by  lateral  flexion.  They  remain 
in  frogs  only  as  muscles  that  bend  the  body  dorsally,  serving  to  brace 
the  vertebral  column  on  the  sacrum  (Figs.  187  and  188).  Short 
muscles  run  between  the  vertebrae,  and  dorsal  to  these  is  a  continuous 
sheet  of  longitudinally  arranged  fibres,  the  longissimus  dorsi  muscle, 
running  from  head  to  sacral  vertebra  and  urostyle.  This  muscle, 


XII.  II 


MUSCLES  OF  THE  BACK 


3i9 


though  forming  a  continuous  band,  is  crossed  by  a  tendinous  inter- 
section, showing  its  segmental  origin.  At  the  hind  end  the  coccygeo- 
sacralis  and  coccygeo-iliacus  muscles  brace  the  urostyle  on  the  pelvic 
girdle. 

The  pectoral  girdle  is  attached  to  the  axial  skeleton  by  a  series  of 
muscles.  Rhomboid  and  levator  scapulae  muscles  run  from  the  supra- 
scapula  to  the  vertebrae  and  skull.  The  cucullaris  muscle  corresponds 


rect. 


Fig.  189.  Muscles  of  larval  Amby stoma.  A,  b,  and  c  show  successive  layers. 

ep.  epaxial  muscles;  ext.o.  external  oblique;  h.  horizontal  septum;  hyp.  hypobranchial 

muscles;  int.o.  internal  oblique;  my.  myocomma;  rect.  rectus  abdominis;  tr.  transversus 

abdominis.  (From  Ihle,  after  Maurer.) 

to  the  mammalian  sternomastoid,  running  from  the  skull  to  the 
suprascapula;  it  is  derived  from  lateral  plate  musculature  and  in- 
nervated by  the  vagus.  The  naming  of  these  muscles  of  the  scapula, 
and  indeed  all  amphibian  muscles,  meets  the  difficulty  that  many  of 
the  bundles  of  fibres  are  similar  in  their  general  course  to  muscles 
found  in  mammals  and  yet  differ  sufficiently  to  raise  serious  doubts 
about  the  wisdom  of  using  the  mammalian  names.  The  similarity  of 
arrangement  of  the  limb  muscles  is  so  striking  throughout  the  tetra- 
pods  that  there  is  probably  no  harm  in  keeping  to  the  well-established 
system  of  names,  but  we  know  so  little  of  the  hereditary  or  mechanical 


(32°) 


svbmax, 
om 
sub.hy. 


ext.  obi. 


Fig.  190.  R.  temporaria  dissected  from  the  ventral  surface. 

add.  aductor  magnus;  add.  long,  adductor  longus ;  anc.  anconeus;  br.r  brachio-radialis ; 
cl.  clavicle ;  co.  coracoid ;  cr.  cruralis ;  delt.  deltoid ;  ep.  episternum ;  ext. obi.  obliquus  externus 
abdominis ;  fix.  rad.  flexor  carpi  radialis ;  fl.c.uln.  flexor  carpi  ulnaris  ;  gastr.  gastrocnemius ; 
grac.  ma},  and  min.  gracilis  major  and  minor;  il.int.  iliacus  internus;  o.h.  omohyoid;  om. 
omosternum;  pect.  pectoralis;  r.s.  rectus  sheath;  red.  rectus  abdominis;  sart.  sartorius; 
st.h.  sterno-hyoid;  submax.  submaxillary;  sub.hy.  subhyoid;  t.Ach.  tendo  Achillis;  t.f.lat. 
tensor  fasciae  latae;  tars. a.  and  tars. p.  tarsalis  anterior  and  posterior;  tib.ant.br.  and  long. 
tibialis  anterior  brevis  and  longus;  tr.  transversus  abdominis;  .yj.  xiphisternum. 
(Partly  after  Gaupp.) 


XII.  II 


VENTRAL  MUSCLES 


321 


factors  that  control  the  arrangement  of  muscle-fibres  into  'muscles' 
that  discussion  of  homologies  is  difficult. 

The  hypaxial  musculature,  formed  from  the  more  ventral  portions 
of  the  myotomes,  is  more  developed  than  in  fishes  and  differentiated 
into  several  parts,  for  the  purpose  of  slinging  the  viscera,  which  of 
course  need  support  in  air  in  a  way  that  is  unnecessary  in  water. 

sub.  max. 


dep.  mand. 

d.        rorrad 
deU. 

h.. 


Fig.  191.  Dissection  of  muscles  of  frog  from  ventral  surface. 

cor.br.  coraco-brachialis;  cor.rad.  coraco-radialis;  dep. mand.  depressor  mandibulae;  h.  head  of 

humerus;  s.  sternum;  other  letters  as  Fig.  190.  (Partly  after  Gaupp.) 

These  muscles  are  differentiated  into  layers  whose  fibres  run  in 
different  directions.  The  plan  found,  with  modifications,  in  all 
tetrapods  is  seen  in  amphibian  larvae  and  includes  four  sets  of  fibres. 
The  external  obliques  run  caudally  and  ventrally;  inside  this 
layer  is  the  internal  oblique,  running  in  the  opposite  direction,  and 
within  this  again  the  transversus  abdominis  running  approximately 
dorso-ventrally  (Fig.  189).  The  rectus  abdominis  consists  of  fibres  in 
the  midline  running  antero-posteriorly. 

In  the  adult  frog  three  of  these  sets  of  fibres  can  be  recognized.  In 
the  mid-ventral  region  (Fig.  191)  are  the  longitudinally  arranged 
fibres  of  the  rectus  abdominis,  making  a  sling  between  the  sternum 
and  the  pubis.  These  fibres  are  interrupted  at  intervals  by  transverse 
fibrous  tendinous  inscriptions,  giving  an  appearance  of  segmentation. 
In  the  mid-ventral  line  is  the  tendinous  linea  alba.  The  sling  formed 


322 


AMPHIBIA 


by  the  rectus  abdominis  is  supported  laterally  by  thin  sheets  of 
muscle-fibres  running  up  to  the  vertebral  column,  the  obliquus  exter- 
nus  and  transversus  abdominis  (Fig.  191). 

In  the  anterior  region  the  hypaxial  muscles  have  become  restricted 
to  the  throat,  where  they  form  the  hyoid  musculature,  which  by  raising 


Fig.  192.  a.  Lateral  surface  of  the  fin  of  Neoceratodus,  showing  the  abductor 

muscle-bundles,  b.  Section  through  the  fin  in  the  transverse  plane,  showing  the 

arrangement  of  the  muscle-bundles  as  abductors  and  adductors. 

ab.    abductor   muscles;    ad,  adductor   muscles;   g.  pectoral   girdle;    h.    horny    fin    rays; 

r.  radials.  (From  Ihle,  after  Braus.) 

and  lowering  the  floor  of  the  mouth  is  the  main  agent  of  breathing. 
The  submaxillary  muscle  runs  transversely  between  the  rami  of 
the  jaw.  Deep  to  this  lie  other  muscles,  including  the  sternohyoid, 
close  to  the  midline,  which  is  a  forward  continuation  of  the  rectus 
abdominis. 

12.  The  limb  muscles  of  Amphibia 

The  muscles  of  the  limbs  were  presumably  derived  from  the  radial 
muscles  that  moved  the  fins  of  fishes.  These  are  formed  from  the 
myotomes  and  they  are  mainly  arranged  so  as  to  raise  and  lower  the 
fin  (Fig.  192).  In  modern  amphibia  the  limb  musculature  is  still  partly 
formed  from  myotomes  (Griffiths,  1959).  The  segmental  origin  of  the 


xii.  12  LIMB  MUSCLES  323 

limbs  is  also  shown  by  the  fact  that  they  are  innervated  by  branches 
of  the  spinal  nerves  of  several  segments  (2  for  the  fore-limb,  4  for  the 
hind-limb  in  the  frog).  Presumably  the  original  arrangement  was  such 
as  to  move  the  limbs  in  association  with  the  waves  of  contraction 
passing  down  the  body.  In  modern  urodeles  the  limb  is  brought 
forward  and  its  joints  flexed  as  the  epaxial  muscles  at  the  level  of  its 
front  end  contract,  and  then  passes  back  and  extends  as  the  wave  of 
contraction  moves  past.  This  may  have  been  the  primitive  movement, 
making  the  limb  more  useful  as  a  lever  during  the  early  attempts  to 
'swim  on  land'  (Fig.  176). 

The  muscles  of  the  limbs  of  tetrapods  are  presumably  derived  from 
those  that  raise  and  lower  the  fins  of  fishes,  modified,  as  we  have  seen, 
to  brace  the  limbs  and  move  them,  allowing  standing  and  walking. 
The  muscles  that  run  from  the  girdles  to  the  humerus  and  femur  are 
therefore  able  to  draw  the  leg  forward  and  backward,  as  well  as  to 
raise  and  lower  it  in  the  transverse  plane.  The  actions  of  the  various 
bundles  are  of  course  not  confined  to  a  single  plane:  all  the  muscles 
running  from  the  back  to  the  humerus  can  raise  (abduct)  the  upper 
limb,  but  the  more  anterior  members  also  protract,  the  more  posterior 
retract  it.  Similarly  there  is  a  ventral  series  whose  anterior  members 
work  with  the  anterior  dorsal  muscles  as  protractors,  although  they 
antagonize  the  action  of  raising  the  whole  limb.  Moreover,  many  of  the 
muscles  have  a  rotating  action  on  the  humerus  and  femur.  It  is,  how- 
ever, possible  to  consider  the  muscles  of  the  arm  and  leg  in  two  great 
groups;  first  a  more  anterior  and  ventral  ('ventro-lateral')  set  serving 
to  draw  the  limb  mainly  forward  and  towards  the  midline  (protraction 
and  adduction)  and  to  flex  its  more  distal  joints,  second  a  more 
posterior,  dorsal  ('dorso-medial')  mass  serving  mainly  to  draw  the 
limb  backwards  and  away  from  the  body  (retraction  and  abduction) 
and  to  extend  its  joints. 

In  the  fore-limb  the  proximal  members  of  the  ventral  group  make  a 
sheet  of  fibres  running  transversely  to  the  main  body  axis  and  attached 
to  the  sternum  and  hypaxial  muscles  at  one  end  and  to  the  humerus  at 
the  other  (Fig.  190).  Within  this  sheet  can  be  recognized  the  del- 
toideus,  pectoralis,  coraco-radialis,  and  coraco-brachialis  muscles.  In 
the  limb  itself  this  group  is  continued,  there  being,  roughly  speaking, 
a  set  of  muscles  in  each  segment  that  serves  to  flex  it  on  the  next. 
Thus  the  brachio-radialis  flexes  the  elbow  joint  and  in  the  forearm 
the  flexor  carpi  radialis  and  flexor  carpi  ulnaris  flex  the  wrist.  The 
flexor  digitorum  longus  muscle  arises  from  the  medial  epicondyle  of 
the  humerus  and  is  inserted  by  tendons  to  the  carpus  and  terminal 


324  AMPHIBIA  xn.  12- 

phalanges.  Flexor  digitorum  brevis  muscles  arise  from  this  tendon 
for  insertion  on  the  digits. 

Of  the  dorsal  muscle  mass  (Fig.  187)  the  latissimus  dorsi  and 
dorsalis  scapulae  are  the  most  proximal,  running  from  the  middle  of 
the  back  to  the  humerus  and  serving  to  abduct  and  draw  back  the 
whole  limb.  The  triceps  (anconeus)  serves  to  extend  the  elbow;  in 
the  forearm  are  extensor  carpi  ulnaris  and  radialis  and  extensors  for 
the  fingers. 

According  to  this  plan  protractor  (flexor)  muscles  lie  mainly  an- 
terior to  retractors  (extensors),  corresponding  to  the  ancient  move- 
ment by  which  the  limb  was  drawn  first  forward  then  back  as  a  swim- 
ming wave  passed  down  the  body.  In  all  tetrapods  flexor  muscles  are 
in  general  innervated  by  spinal  roots  anterior  to  those  for  the  exten- 
sors. The  locomotory  movements  of  the  limbs  therefore  still  show  the 
passage  of  an  excitation  wave  backwards  along  the  spinal  cord,  a  relic 
of  the  swimming  rhythm  of  fishes.  However,  the  changes  that  have 
taken  place  in  the  relative  positions  of  the  parts  of  the  limbs  make  it 
difficult  to  follow  out  this  simple  pattern  in  detail.  It  must  also  con- 
tinually be  remembered  that  many  muscles  produce  rotation  as  well 
as  movement  in  the  main  planes  of  the  body. 

In  the  hind  limb,  muscles  of  the  same  two  general  types  can  be 
recognized,  namely  anterior  muscles,  which  draw  the  limb  forward 
and  flex  and  adduct  its  joints,  and  posterior  ones,  which  draw  it  back 
and  extend  and  abduct.  The  specialization  of  the  main  muscle  masses 
has  gone  much  farther,  however,  so  that  more  individual  muscles  are 
found,  especially  round  the  hip  joint,  each  serving  to  move  the  limb 
in  a  special  way. 

In  the  thigh  (Figs.  187  and  190)  the  muscles  of  the  anterior  group, 
lying  on  the  ventral  surface,  are  the  pectineus  and  the  adductors, 
running  from  the  pelvic  girdle  to  the  femur  and  thus  serving  to  move 
the  whole  limb  inwards  (adduction).  The  sartorius,  biceps,  semi- 
membranosus, and  semitendinosus  are  two-joint  muscles  mainly  pro- 
ducing flexion  at  the  knee  as  well  as  at  the  hip. 

The  more  posterior  and  dorsal  group  of  muscles  includes  the 
gluteus  and  tensor  fascia  lata  from  girdle  to  femur,  extending  the 
thigh  joint,  and  the  very  large  cruralis  (including  the  rectus  femoris 
and  triceps  femoris)  running  from  girdle  and  femur  to  tibia.  This  is 
the  main  extensor  of  the  knee,  being  helped  by  gracilis  and  semi- 
membranosus. This  extension  is  obviously  an  important  part  of  the 
jumping  movement  of  the  frog. 

In  the  shank  the  arrangement  of  the  flexors  and  extensors  into  the 


Y 
ppa 


/><! 


pa 

ML 


/ 


o& 


ac. 

St. 


0 


s 


p  rose. 


xii.  13  LIMB  MUSCLES  325 

anterior  and  posterior  groups  is  much  modified.  The  more  con- 
spicuous muscles  are  the  tibialis  anterior  and  peroneus  running  from 
the  femur  to  the  tarsus  so  as  to  flex  the  ankle  joint.  Long  and  short 
flexors  move  the  toes,  as  in  the  fore-limb.  At  the  back  of  the  tibio- 
fibula  the  gastrocnemius  (plantaris  longus)  runs  from  the  femur  to 
be  attached  by  the  tendo  Achillis  to  the  tarsus.  Its  main  action  is  to 
extend  the  ankle  in  the  movements  of  jumping  and  swimming.  Tibialis 
posterior  runs  from  the  tibia 
to  the  tarsus.  Within  the  foot 
there  is  an  elaborate  system  of      n  — i~~Pm- 

small  muscles  for  bending  and 
stretching  the  toes  and  abduct- 
ing them  away  from  each  other, 
so  as  to  expand  the  web  for 
swimming. 

The  whole  system  is  de- 
signed to  produce  the  charac- 
teristic sudden  simultaneous 
extension  movement  of  all  the 
joints  of  both  hind  limbs,  by 
which  the  frog  moves  both  in 
water  and  on  land.  The  hind 
limbs  can  also  be  used  for 
alternate  walking  movements, 
especially  in  toads  (Fig.  177). 

13. 


V 


ttPi 


pa 


t 


hm 


Fig.  193.   Diagram  of  skull  bones  and  other 
structures,  a,  an  osteolepid ;  B,  astegocephalian. 

Letters  for  this  and  Fig.  194:  ac.  auditory  capsule; 
ex.  extrascapular;  jr.  frontal;  hm.  hyomandibula ; 
it.  intertemporal;  j.  jugal;  /.  lachrimal;  na.  nasal; 
?nx.  maxilla;  p.  pineal;  pa.  parietal;  pi.  pituitary; 
pm.  pre-maxilla;  po.  post-orbital;  pof.  post-frontal; 
ppa.  post-parietal;  prf.  pre-frontal;  p.rost.  post- 
rostrals;  qj.  quadratojugal;  sq.  squamosal;  st.  stapes; 
sut.  supratemporal;  t.  tabular. 
(After  Westoll.) 


The    skull    of   Stenoce- 
phalia 

The  skull  of  the  Devonian 
and    Carboniferous    amphibia 

was  essentially  like  that  of  the  osteolepid  fishes  in  the  arrangement  of 
the  bones,  but  the  proportions  had  been  altered  so  that  the  pre-optic 
region  was  relatively  large  and  the  more  posterior  'table'  of  the  skull 
short  (Fig.  193). 

The  nasals  and  frontals,  which  were  small  in  crossopterygians, 
were  quite  long  in  stegocephalians,  whereas  the  parietals  were  shorter 
and  the  post-parietals  absent  altogether  in  the  later  forms.  The  differ- 
ence is  so  marked  that  for  a  long  time  people  were  deceived  in  identifi- 
cation of  the  bones  and  it  was  said  that  the  pineal  opening  lay  between 
the  frontal  bones  in  fishes  but  between  the  parietal  bones  in  tetrapods. 
The  bones  identified  as  'frontal'  in  the  fish  types  were,  of  course, 


326 


AMPHIBIA 


xii.  13 


parietals,  whereas  the  'parietals'  were  the  post  parietals,  which  have 
gone  completely  from  most  amphibians,  though  still  present  in  the 
earliest  Devonian  forms  (Fig.  194).  This  is  an  excellent  example  of  how 
study  of  changes  of  proportion  can  clear  up  morphological  difficulties. 
The  opercular  apparatus  covering  the  gills  was  lost  early  in 
amphibian  evolution;  perhaps  the  reduction  of  the  whole  posterior 
part  of  the  head  was  effected  by  a  single  morphogenetic  change.  In 


ppa.  "— — 

Osteo/epis 


F/p/ftOStCLJC 


Ichthyostega 


sub 

Palaeogurinus  RomerJa  Dimetrodon 

(Cotylosaur)  (Pelycosaur) 

Fig.  194.  Skulls  of  a  crossopterygian  and  various  early  tetrapods  to  show  the 
shortening  of  the  posterior  region.  Lettering  as  Fig.  193.  (After  Westoll.) 

modern  amphibia  the  skull  is  much  flattened  and  its  ossification 
reduced,  so  that  large  spaces  are  left;  in  the  earlier  forms,  however, 
the  skull  was  of  the  more  usual  domed  shape  and  the  roof  and  jaws 
were  covered  by  a  complete  set  of  dermal  bones.  Presumably  the  loss 
of  bone  was  another  development  producing  a  reduction  of  weight 
advantageous  to  a  terrestrial  animal. 

Lateral  line  organs  are  present  in  aquatic  amphibians  and  their 
position  is  marked  on  the  bones  of  the  fossil  skulls  by  rows  of  pits. 
By  using  these  lines  as  reference  marks  it  is  possible  to  compare  the 


xii.  i3  STEGOCEPHALIAN  SKULL  327 

pattern  of  the  bones  on  osteolepid  and  early  amphibian  skulls  and  to 
confirm  the  remarkable  similarity.  The  main  new  development  found 
in  the  skull  of  early  amphibians  was  correlated  with  the  modification 
of  the  Eustachian  tube  in  connexion  with  the  sense  of  hearing,  and 
the  need  for  a  sensitive  resonator  to  pick  up  the  air  vibrations.  Already 
in  the  earliest  amphibians  the  opercular  coverings  of  the  gills  were 
lost  (there  was  a  small  pre-opercular  bone  in  *Ichthyostega)  and  the 
spiracular  opening  thus  uncovered  acquired  a  tympanic  membrane. 
The  hyomandibular  cartilage,  no  longer  concerned  (if  it  ever  had 
been)  with  supporting  the  jaw,  was  modified  to  form  the  columella 
auris,  serving  to  carry  vibrations  across  to  the  inner  ear.  At  first, 
however,  there  was  no  trace  of  the  fenestra  ovalis,  the  hole  in  the 
auditory  capsule  into  which  the  columella  fits  in  the  frog.  In  modern 
urodeles  the  whole  ear  apparatus  is  much  modified,  there  being  no 
tympanum.  Instead  the  columella  is  fused  to  the  squamosal  and  the 
ear  thus  receives  its  vibrations  from  the  ground. 

Other  small  changes  in  the  skull  in  passing  from  the  fish  to  the 
amphibian  stage  include  the  increase  in  size  of  the  lachrymal  bone, 
which  also  came  to  have  a  hole  to  carry  the  tear  duct,  draining  the 
orbit.  A  series  of  small  bones  surrounds  the  orbit  in  early  amphibians, 
as  in  fishes;  large  squamosals  and  quadrat ojugals  support  the  quad- 
rate. At  the  back  of  the  skull  these  stegocephalians  possessed  various  of 
the  small  bones  that  are  found  in  fishes  but  not  in  modern  amphibians, 
the  supratemporal  and  intertemporal,  post-parietal  (much  smaller 
than  in  crossopterygians)  and  tabulars.  In  fact  there  are  numerous 
small  bones,  arranged  in  a  pattern  clearly  recalling  that  of  the  fish 
ancestor,  but  showing  some  reductions  and  less  variation  than  in  those 
very  variable  fish  skulls.  This  simplification  (which  was  later  carried 
farther),  together  with  some  changes  in  the  shape,  are  the  chief  trans- 
formations that  have  converted  the  fish  skull  into  the  amphibian 
skull. 

The  palate  of  the  early  amphibians  also  resembled  that  of  crosso- 
pterygians, showing  a  complete  plate  made  of  vomer,  palatines, 
pterygoids,  and  ecto-pterygoids.  These  bones,  as  well  as  the  pre- 
maxillae  and  maxillae,  often  carried  folded  teeth  (hence  'labyrin- 
thodonts'),  with  a  pit  for  a  replacing  tooth  beside  each  one,  an 
arrangement  similar  to  that  of  their  fish  ancestors  (p.  270).  The 
internal  nostril  opened  far  forward,  through  the  palate.  The  lower 
jaw  was  covered  by  a  number  of  dermal  bones  (Fig.  208),  but  the 
actual  jaw  articulation  was  made  between  cartilage  bones,  the  upper 
quadrate,  and  the  lower  articular. 


328 


AMPHIBIA 


xii.  14 


14.  The  skull  of  modern  Amphibia 

Modern  amphibia  share  several  cranial  features  that  distinguish 
them  from  typical  labyrinthodonts.  The  number,  extent,  and  thick- 
ness of  the  dermal  elements  are  greatly  reduced  so  that  the  otic 


b   p. 


Fig.  195.  Skull  of  the  frog.  a.  Ventral  view.  b.  Side  view. 

ac.  anterior  cornu  of  hyoid ;  art.  articular ;  as.  angulosplenial ;  col.  columella  auris ;  d.  dentary ; 
ex.  exoccipital ;  fp.  fronto-parietal;  m.  maxilla;  m.m.  mento-Meckelian;  n.  nostril;  na.  nasal; 
pa.  palatine;  par.  parasphenoid;  pc.  posterior  cornu  of  hyoid;  pm.  premaxilla;  pro.  pro-otic; 
pt.  pterygoid;  q.  quadrate;  qj.  quadrato-jugal;  se.  sphenethmoid;  sq.  squamosal;  v.  vomer; 
//,  IX,  and  A',  nerve  foramina.  (After  Marshall,  The  Frog,  Macmillan.) 

capsules  are  generally  exposed.  The  orbits  and  interpterygoid  vacui- 
ties are  large,  the  mandibular  ramus  is  short  and  the  skull  as  a  whole 
much  flattened.  The  occiput  is  shortened  so  that  the  hypoglossal  nerve 
emerges  behind  the  skull  and  (with  the  few  exceptions  noted  below) 
the  parietal  foramen  has  been  lost. 

The  skull  of  the  frog  (Fig.  1 95)  shows  great  reduction  and  specializa- 
tion from  the  early  amphibian  type.  It  may  be  considered  as  consisting 
of  a  series  of  cartilaginous  boxes  or  capsules,  in  whose  walls  some 
ossifications  occur,  partly  covered  by  dermal  bones.  The  cartilaginous 


xii.  14 


MODERN  AMPHIBIAN  SKULLS 


329 


o.F  P{ar     F- 


cpt.  %■  o.pt,  cp- ps.^v.  m 

apt.     c.M. 


o.c  I  c-c-        SALAMANDER 

bc.p. 


ICHTHYOPHIS 

Fig.  196.  Skulls  of  amphibians. 

a.,  articular;  be,  basicranial  fenestra;  bc.p.,  posterior  basicranial  fenestra;  c.c,  carotid  canal; 
<-..V.,  Meckel's  cartilage;  c.p.  coronoid  process;  cpt.  pterygoid  cartilage;  c.r.  process  of 
internasal  plate;  d.  dentary;  e.o.  exoccipital;/.  frontal ;fen.ol.  olfactory  fenestra;  in.  internal 
naris;_/.  jugal;  m.  maxillary;  m.M.  mento-Meckelian;  ;;.  nasal;  o.c.  occipital  condyle; 
o.f.  optic  foramen;  o.p.  occipito-petrosal;  ope.  operculum;  o.pt.  pterygoid  bone;  o.s.  orbito- 
sphenoid;  p. a.  pre-articular;  par.  parietal;  p.f.  prefrontal;  p. I.  palatine;  p.m.  premaxilla; 
po.f.  postfrontal  (enclosing  orbit);  p.q.  palato-quadrate;  pr.ba.  basal  process;  p.s.  para- 
sphenoid;  p.v.  prevoma;  q.  quadrate  bone;  sq.  squamosal;  st.  stapes;  /.  tentacular  groove; 

v.  vomer. 


boxes,  well  seen  in  a  tadpole's  skull,  are  the  central  neurocranium 
around  the  brain,  and  the  olfactory  and  auditory  capsules.  Ossifications 
occur  especially  at  the  points  of  compression  stress,  namely,  around 
the  foramen  magnum  (the  exoccipitals),  where  the  auditory  capsule 
joins  the  cranium  (the  pro-otic),  and  at  the  base  of  the  nasal  capsules 
(the  mesethmoid).  The  paired  occipital  condyles  are  found  only  in 


33°  AMPHIBIA  xn.  14 

modern  amphibia,  and  are  formed  by  the  failure  of  the  basioccipital 
to  become  ossified.  Paired  occipital  condyles  have  also  arisen,  inde- 
pendently, in  the  mammal-like  reptiles. 

The  dermal  bones  covering  the  roof  of  the  skull  are  the  nasals  and 
frontoparietals,  while  on  the  floor  is  the  large  dagger  bone,  the 
parasphenoid,  and  a  small  tooth-bearing  vomer.  The  remains  of  the 
cartilaginous  palato-pterygo-quadrate  bar  can  be  recognized  as  a  rod, 
covered  in  front  by  premaxillae  and  maxillae,  and  dividing  behind 
into  an  otic  process  fixing  it  to  the  skull  (autostylic)  and  a  cartilaginous 
quadrate  region  articulating  with  the  lower  jaw.  This  region  is  covered 
by  the  pterygoid  ventrally,  the  quadrato-jugal  laterally,  and  the 
squamosal  dorsally.  The  palatines  are  membrane  bones  forming  the 
anterior  wall  of  the  orbit.  The  upper  jaw  is  thus  supported  by  struts 
formed  from  the  nasals  and  palatines  in  front  and  the  squamosal  and 
pterygoid  behind,  an  arrangement  that  gives  a  large  mouth  for  res- 
piration and  eating  insects,  combined  with  the  advantages  of  strength, 
mobility  of  the  lower  jaw,  and  lightness  in  weight. 

The  lower  jaw  consists  of  Meckel's  cartilage,  covered  on  its  outer 
surface  by  a  dentary  and  on  its  inner  by  an  angulo-splenial  bone. 
The  anterior  tips  of  the  cartilages  ossify  as  the  mento-Meckelian  bones . 

The  visceral  arches  are  well  formed  in  the  tadpole  but  are  much 
modified  in  the  adult  frog.  In  the  tadpole  the  skeleton  of  the  hyoid 
arch  consists  of  a  large  pair  of  ceratohyals  attached  to  a  basal  hypo- 
hyal.  As  a  result  of  subsequent  metamorphosis  the  ceratohyals  later 
form  the  long  anterior  cornu  of  the  hyoid,  attached  to  the  pro-otic 
bone.  The  body  of  the  hyoid  is  a  plate  lying  in  the  floor  of  the  mouth 
and  formed  from  the  hypohyal  and  from  the  hypobranchial  plate  at 
the  base  of  the  remaining  arches.  The  posterior  cornua  support  the 
floor  of  the  mouth  and  the  whole  apparatus  assists  in  respiration.  The 
sixth  and  seventh  of  the  series  of  branchial  arches  give  rise  respec- 
tively to  the  arytenoid  and  cricoid  cartilages  of  the  larynx. 

The  lateral  plate  muscles  of  the  branchial  arches  are  well  developed 
only  as  the  muscles  of  the  jaws.  Certain  muscles  of  the  scapula  (the 
cucullaris  (p.  319)  and  interscapularis)  are  innervated  from  the  vagus 
and  recall  the  sternomastoid  and  other  muscles  innervated  by  the 
spinal  accessory  nerve  in  mammals. 

The  muscles  of  the  hyoid  arch,  innervated  by  the  facial  nerves, 
remain  mainly  as  the  depressor  mandibulae  (Fig.  197)  running  from 
the  back  to  the  angle  of  the  jaw  and  serving  to  lower  the  floor  of  the 
mouth.  The  jaw-closing  muscles,  m.m.  adductor  mandibulae,  belong 
to  the  mandibular  segment  and  are  innervated  by  the  trigeminus. 


xii.  14  EVOLUTION  OF  THE  SKULL  331 

They  run  from  the  hind  end  of  the  jaw  to  the  surface  of  the  skull  and 
squamosal. 

The  skull  and  jaws  of  the  frog  thus  constitute  a  protection  for  the 
brain  and  special  sense-organs,  a  feeding  apparatus,  and  a  means  of 
respiration.  The  heavy  protection  afforded  by  the  dermal  bones  of 
fishes  and  early  amphibians  has  been  largely  dispensed  with,  probably 
for  lightness.  The  front  part  of  the  skull,  concerned  with  the  nose, 
eyes,  and  brain,  has  become  increased  in  size  and  the  hind  part, 
originally  concerned  with  the  gills  and  pharynx,  greatly  reduced. 

dep.mand. 

Fa  se.  dors, 
iat.  dors. 


cor  rad 
FL.  c  uin. 


Fig.  197.  Muscles  of  head  and  neck  of  frog  dissected  from  the  side. 
add.  adductor  mandibulae.  Other  letters  as  in  Figs.  187  and  191.  (Partly  after  Gaupp.) 

These  changes,  carried  to  extremes  in  frogs,  have  been  in  progress 
throughout  the  evolution  of  amphibia.  It  is  not  difficult  to  imagine 
that  they  have  been  the  result  of  rather  simple  genetic  changes,  affect- 
ing the  relative  growth  of  various  parts  of  the  skull.  We  are  still  far 
from  the  knowledge  necessary  to  say  exactly  what  developmental 
changes  have  occurred,  but  we  know  enough  to  imagine  how  selection 
through  millions  of  years  has  changed  the  quantities  of  certain  sub- 
stances so  as  to  produce  gradually  less  bony  and  shorter  heads,  such 
as  enabled  their  possessors  to  maintain  sufficient  mobility  to  hold  a 
place  in  a  world  peopled  by  the  reptiles  and  other  still  more  active 
descendants  of  the  early  amphibians. 

The  preceding  account,  particularly  with  regard  to  the  osteology, 
should  not  be  regarded  as  diagnostic  of  all  anurans.  Bufonid  skulls 
are  completely  devoid  of  teeth  but  they  possess  a  supratemporal  bone, 
which  fuses  with  the  squamosal  and  roofs  the  otic  capsule.  Hylids 
frequently  develop  secondary  dermal  ossifications  to  form  expanded 
helmets;  this  trend  also  occurs  in  leptodactylids  (e.g.  Calyptocephalus), 
where  the  skull  may  be  so  completely  roofed  and  sculptured  as 
to  simulate  the  condition  of  the  extinct  branchiosaurs.  Pseudoteeth 


332  AMPHIBIA  xn.  14- 

(serrations  of  the  jaw  elements)  frequently  occur  on  the  dentary  and 
pre-articular  (e.g.  Amphodus)  but  the  only  modern  form  to  possess 
true  teeth  on  the  lower  jaw  is  Amphignathodon.  No  recent  frog  retains 
the  large  parietal  foramen  so  typical  of  the  fossil  amphibia  but  some 
leptodactylids  and  the  aquatic  xenopids  have  a  small  canal  perforating 
the  fronto-parietal,  through  which  runs  a  fibro-nervous  tract  from  the 
pineal  organ  to  the  habenular  ganglion  (Griffiths,  1954).  The  anuran 
skull  is  always  easily  distinguished  from  those  of  all  other  Amphibia 
by  the  fact  that  the  frontals  are  fused  with  the  parietals. 

Urodele  skulls  are,  in  some  respects,  less  specialized  than  those  of 
Anura.  The  frontals  and  the  parietals  remain  discrete  and  in  certain 
species  both  lacrimals  and  prefrontals  are  present.  In  other  respects 
they  are  clearly  more  degenerate  (or  paedomorphic  ?).  No  urodele  has 
either  a  jugal  or  quadrato-jugal  (except  Tylotriton)  and  in  perenni- 
branchs  even  the  maxillaries  and  nasals  are  lost.  Urodeles  are  further 
distinguished  from  frogs  (but  not  from  caecilians)  by  the  great  size 
of  the  prevomers  (each  consisting  really  of  a  prevomer+ palatine)  and 
by  the  possession  of  a  tooth-bearing  coronoid,  as  well  as  a  dentary 
and  a  prearticular. 

The  apodan  skull  is  a  much  more  rigid  structure  than  that  of  either 
of  the  above  subclasses  and,  at  first  sight,  approaches  more  closely  to 
the  ancestral  pattern.  The  number  of  bones  present,  however,  is  no 
greater  than  in  any  of  the  other  modern  groups.  The  overall  compact- 
ness is  effected  particularly  by  the  expansion  of  the  nasals  and  of  the 
marginal  elements  of  the  upper  jaw  and  is  probably  correlated  with  the 
burrowing  habits  of  the  group.  Lower  as  well  as  upper  jaws  carry 
teeth  and  a  toothed  coronoid  is  present  in  the  mandible. 

15.  Respiration  in  Amphibia 

The  new  problems  presented  by  life  on  land  have  led  to  the  produc- 
tion of  very  varied  means  of  respiration  among  amphibia.  In  a  ter- 
restrial habitat  oxygen  is  available  in  plenty;  the  difficulty  is  evidently 
to  arrange  for  a  regular  interchange  of  air  in  contact  with  adequately 
moistened  surfaces.  The  interchange  is  provided  for  in  most  cases 
by  modifications  of  the  apparatus  used  in  fishes,  but  pumping  air 
presents  new  problems  and  it  seems  that  these  are  not  easily  solved, 
since  in  many  amphibians  the  skin  is  used  as  an  accessory  respiratory 
mechanism.  The  retention  of  moisture  becomes  more  difficult  as  the 
ventilation  becomes  efficient;  probably  for  this  reason  air  is  often 
only  transferred  to  the  lungs  after  it  has  remained  for  some  time  in  the 
mouth.  We  see  again  that  the  new  way  of  life,  in  a  medium  remote 


xii.  1 6  RESPIRATION  333 

from  water,  makes  it  necessary  to  possess  more  complicated  methods 
of  self-maintenance. 

16.  Respiration  in  the  frog 

The  lungs  of  the  frog  are  paired  sacs,  opening  to  a  short  laryngeal 
chamber,  which  communicates  with  the  pharynx  by  a  median  aper- 
ture, the  glottis.  The  glottis  and  laryngeal  chamber  are  supported  by 
the  arytenoid  and  cricoid  cartilages.  The  arytenoids  guard  the  open- 
ing of  the  glottis  and  are  moved  by  special  muscles.  During  breathing 
the  mouth  is  kept  tightly  closed,  the  lips  being  so  arranged  as  to  make 
an  air-tight  junction.  Air  is  sucked  in  through  the  nostrils  by  lowering 
the  floor  of  the  mouth  by  means  of  the  hypoglossal  musculature,  and 
can  then  either  be  breathed  out  again  or  forced  into  the  lungs  by 
raising  the  floor.  The  external  nares  are  closed  by  a  special  pad  on  the 
anterior  angle  of  the  lower  jaw,  supported  by  the  mento-Meckelian 
bones.  This  pad  is  thrust  upwards  and  pushes  the  premaxillaries 
apart,  so  altering  the  position  of  the  nasal  cartilage  that  the  nostrils 
are  closed.  This  is  a  special  mechanism,  found  only  among  anurans. 
In  urodeles  the  nostrils  are  closed  by  valves  provided  with  smooth 
muscles.  Such  valves  are  present  in  the  frog  but  are  said  to  be  func- 
tionless. 

The  movements  of  the  floor  of  the  pharynx  are  not  continuously  of 
the  same  amplitude.  After  a  period  of  relatively  slight  movements  the 
nostrils  are  kept  closed  while  the  throat  is  lowered.  Air  is  thus  drawn 
from  the  lungs  and  then  again  returned  to  them  once  or  twice  before 
the  nostrils  are  reopened.  The  whole  procedure  presumably  ensures 
the  maximum  gaseous  interchange  for  the  minimum  water-loss. 

This  method  of  taking  in  air  is  clearly  derived  from  the  movements 
of  the  floor  of  the  mouth  of  fishes,  by  which  water  is  passed  over  the 
gills.  In  amphibian  larvae  water  is  pumped  in  this  way  and  there  is 
direct  continuity  between  the  mechanism  of  larva  and  adult.  The 
basic  rhythmic  mechanism,  centred  on  the  nerve-cells  of  the  medulla 
oblongata,  is  no  doubt  the  same  throughout,  but  the  anurans  have 
improved  upon  it  by  the  addition  of  special  features,  requiring  intri- 
cate coordination  of  the  muscles  of  the  larynx  and  the  apparatus  for 
closing  the  nostrils. 

The  skin  is  very  vascular,  and  especially  so  in  the  buccal  cavity.  It 
plays  a  large  part  in  respiration,  actually  serving  to  remove  more 
carbon  dioxide  than  do  the  lungs.  There  is,  however,  little  power  to 
vary  the  amount  of  exchange  through  the  skin,  which  is  therefore 
constant  throughout  the  year.  There  is  considerable  regulation  of  the 


334  AMPHIBIA  xh.  16- 

exchange  in  the  lungs.  The  rate  of  breathing  depends,  as  in  mammals, 
on  the  effect  of  the  carbon  dioxide  tension  of  the  blood  on  a  respira- 
tory centre  in  the  medulla.  There  is  also  a  vasomotor  control  of  the 
blood-supply  to  the  lungs  and,  through  the  vagus  nerve,  of  the  state 
of  contraction  of  the  latter.  By  such  means  the  rate  of  respiratory 
exchange  is  greatly  increased  during  the  breeding  season,  and  made 
to  vary  with  the  activity  of  the  animal. 

17.  Respiratory  adaptations  in  various  amphibians 

The  skin  and  the  lungs  show  many  variations  according  to  the 
habitat  of  the  species,  special  devices  being  adopted  to  enable  the 
animals  to  live  in  particular  environments.  The  lungs  vary  from  the  well 
vascularized  sacs  with  a  highly  folded  surface  found  in  the  frogs, 
and  especially  in  the  drier-skinned  toads,  to  small  simple  sacs  in  some 
stream-living  amphibia.  The  lung  will  serve  to  lift  the  animal  in  the 
water;  for  this  reason  it  is  reduced  in  the  frog  Ascaphus,  which  lives  in 
mountain  streams  in  the  eastern  U.S.A.  In  newts  this  hydrostatic 
function  of  the  lungs  is  predominant  and  the  inner  surface  is  often 
quite  simple.  The  lung  is  entirely  lost  in  stream-living  salamanders, 
such  as  the  European  alpine  S.  atra.  The  coldness  of  the  water  reduces 
activity  and  lowers  the  need  for  respiratory  exchange  to  a  level  at 
which  it  can  be  fully  met  by  the  skin.  The  skin  shows  increased  vascu- 
larity in  these  forms  with  reduced  lungs,  capillaries  reaching  nearly 
to  the  outermost  layers  of  the  epidermis.  In  the  African  frog  Astylo- 
sternus,  in  which  the  lungs  are  vestigial,  the  male  develops  vascular 
papillae  on  the  waist  and  thighs  during  the  breeding  season. 

Gills  are  present  in  amphibian  larvae,  and  also  in  certain  adult 
urodeles  that  may  be  considered  as  larvae  that  have  failed  to  undergo 
metamorphosis  (p.  364).  The  gills  are  extensions  of  the  branchial 
arches,  and  carry  branched  villi,  richly  supplied  with  blood.  Where 
the  main  trunk  is  long  the  gill  projects  and  is  'external',  whereas  in 
other  cases,  as  in  the  later  frog  tadpole,  the  filaments  are  directly 
attached  to  the  arches  and  are  called  'internal'.  There  are  no  profound 
differences  between  the  two  types. 

18.  Vocal  apparatus 

Sound  is  produced  as  a  protective  (fear)  response  and  by  the  male 
frog  as  a  call  to  attract  the  female.  Both  sexes  have  vocal  organs,  but 
those  of  the  female  are  much  the  smaller.  The  noise  is  produced  by 
the  vibration  of  the  elastic  edges  of  a  pair  of  folds  of  epithelium  of  the 
laryngeal  chamber,  the  vocal  cords.  Air  is  passed  backwards  and 


xii.  iQ 


(335) 


Uroddd,  larva 


FlG.  198.  Diagrams  illustrating  development  and  fate  of  aortic  arches  in  Amphibia, 

left-side  view  completed.  Vessels  carrying  most  arterial  blood  white,  most  venous 

blood  black,  and  mixed  blood  stippled. 

a1-6,  Primary  arterial  arches;  ca.  conus  arteriosus;  cb.  carotid  gland;  cc.  common  carotid; 
da.  median  dorsal  aorta;  db.  ductus  Botalli;  dc.  left  ductus  Cuvieri;  ec.  external  carotid; 
eg.  blood-supply  to  external  gill;  ic.  internal  carotid;  la.  left  auricle;  Ida.  lateral  dorsal 
aorta  (d.  obliterated  part,  ductus  caroticus);  Ig.  lung;  oph.  ophthalmic;  or.  orbital;  pa. 
pulmonary  artery;  pea.  pulmo-cutaneous  arch;  pv.  pulmonary  vein;  s.  closed  spiracular  slit; 
sa.  systemic  arch;  sv.  sinus  venosus;  tra.  truncus  arteriosus  (ventral  aorta);  v.  ventricle; 
vci,  vena  cava  inferior.  (From  Goodrich.) 

forwards  between  the  lungs  and  a  large  pair  of  sacs  (or  a  single  median 
sac),  the  vocal  pouches,  formed  below  the  mouth.  These  also  serve  as 
resonators,  and  are  developed  only  in  the  male. 


19.  Circulatory  system  of  Amphibia 

The  venous  and  arterial  systems  arc  less  fully  separated  in  Am- 
phibia than  in  lung-fishes.  The  auricles  are  completely  divided  by  an 
inter-auricular  septum,  venous  blood  returning  to  the  right,  arterial 
to  the  left  auricle.  There  is  only  a  single  ventricle,  but  this  is  provided 
with  spongy  projections  of  its  wall,  which  may  prevent  the  mixing  of 
the  blood.  The  ventral  aorta  (conus  arteriosus),  springs  from  the 


336  AMPHIBIA  xn.  19 

right  side  of  the  ventricle  and  may  thus  receive  first  the  venous  blood. 
The  conus  arteriosus  has  transverse  and  longitudinal  valves. 

The  ventral  aorta  is  very  short  and  the  arches  much  modified  in  the 
adult  (Fig.  198).  Of  the  original  six  that  can  be  recognized  the  first 


Ophth 


A  a .  abdom 


Ailiaca  comm 
A.epiy.-ves 


A.  ischiadica 


Fig.  199.  Diagram  to  show  the  chief  arteries  and 
their  anastomoses  in  the  frog.  (After  Gaupp.) 

two  disappear,  the  third  on  each  side  gives  rise  to  the  carotid  artery, 
the  fourth  remains  complete  and  forms  the  systemic  arch.  The  fifth 
remains  also  in  some  urodeles,  but  disappears  in  anurans.  The  sixth 
arch  becomes  the  pulmonary  artery  and  loses  its  connexion  with  the 
dorsal  aorta:  special  'cutaneous  arteries'  carry  de-oxygenated  blood 
from  this  arch  to  the  skin  (Fig.  199).  These  pulmonary  arches  prob- 
ably offer  a  lesser  resistance  than  do  the  systemic  and  carotid  ones; 
the  pressure  in  the  latter  is  said  to  be  increased  by  a  special  network, 
the  'carotid  gland',  though  it  may  well  be  that  this  organ  is  a  receptor, 


xii.  iq  CIRCULATION  337 

connected  with  regulation  of  the  blood-pressure.  However,  it  is 
claimed  that  the  first  blood  leaving  as  the  ventricle  contracts  flows  to 
the  lungs.  In  anurans  this  separation  may  be  further  assisted  by  an 
arrangement  such  that  the  pulmonary  arteries  join  at  their  base  and 


V pulmon  dext 


Vjug  int 
Vjug  ext 
v  subscap 
Vanonyma 
—  Vsubc/avia 
V.  brachlabs 
V.  cutan.  magna 


V  cava  ant 

PuLmo  dext. 

V  bulb  cord,  post 


V cava  post 

V  dorso-lumb. 
V.  abdomen 
Vjacobsonn 
V  oviduct- 
Oviduct 
V  dxaca  communis 


V 'renal  reveh 


V  hepat.  (revehens) 


Intestlnum 

V  porta e  hepat 

Ovarium 

V.ovarica 


R.abdommaUs  (VfemorJ 

V  dica  ext 

V  ilica  transversa 

V  ischiadica 

V  FemoraliS. 


Fig.  200.  Diagram  to  show  the  chief  veins  of  the  frog.  (After 

Gaupp.)  The  r.  abdominalis  is  often  called  the  pelvic  and  the 

v.  iliaca  communis  the  renal  portal  vein. 

open  to  the  dorsal  part  of  the  truncus  arteriosus  (cavu'm  pulmo- 
cutaneum),  which  is  partly  separated  from  the  more  ventral  cavum 
aorticum,  leading  to  the  carotid  and  aortic  arches.  The  classical  view 
of  this  system  is  that  as  the  pressure  rises  the  truncus  contracts  and 
the  spiral  valve  moves  in  such  a  way  as  to  force  all  the  blood  that 
leaves  the  ventricle  during  the  later  part  of  its  contraction  into  the 
ventral  portion  and  hence  to  the  systemic  and  carotid  arches.  In  this 
way  a  separation  of  blood  from  the  right  and  left  auricles  would  be 
achieved.  The  view  that  the  heart  allows  such  a  separation  has,  how- 
ever, been  challenged  on  the  basis  of  experiments  made  by  injection 


338  AMPHIBIA  xn.  19- 

of  X-ray  opaque  material,  allowing  the  course  of  the  circulation  to 
be  watched.  It  is  stated  that  by  this  method  it  can  be  shown  that 
blood  returning  to  either  auricle  reaches  all  parts  of  the  ventricle  and 
that  no  separation  occurs.  Since  the  blood  from  the  skin  returns  to 
the  right  auricle  (Fig.  200)  it  is  not  clear  that  a  separation  of  the 
streams  would  be  advantageous.  It  may  be  that  the  undivided  con- 
dition of  the  ventricle  in  amphibians  is  a  secondary  development, 
perhaps  not  present  in  the  earlier  forms  such  as  *Eogyrimis,  which 
reached  a  larger  size  (Foxon,  1955).  The  spongy  walls  of  the  ventricle 
may  allow  metabolic  exchange  since  the  heart  is  provided  only  with 
very  small  coronary  arteries. 

The  venous  system  (Fig.  200)  is  based  on  the  same  plan  as  that  of 
Dipnoi.  The  posterior  cardinal  veins  are  replaced  early  in  life  by  a 
vena  cava  inferior.  Most  of  the  blood  from  the  hind  limbs  passes 
through  the  renal  portal  system,  but  there  is  an  alternative  path 
through  pelvic  veins  and  a  median  anterior  abdominal  vein,  which 
breaks  into  capillaries  in  the  liver. 

The  blood-pressure  is  regulated  by  the  extrinsic  nerves  of  the  heart, 
fibres  from  the  vagus  tending  to  slow  and  from  the  sympathetic 
nervus  accelerans  tending  to  speed  the  beat.  The  latter  nerve  is  a 
new  development,  there  being  no  sympathetic  innervation  of  the 
heart  in  fishes  (the  condition  in  Dipnoi  is  unknown).  The  diameter 
of  the  arteries  throughout  the  body  is  also  under  control  from  sym- 
pathetic vasoconstrictor  and  perhaps  also  vasodilatator  nerves.  The 
arterioles  in  the  web  of  the  foot  can  be  seen  to  constrict  when  the 
medulla  oblongata  is  stimulated.  Substances  extracted  from  the 
posterior  lobe  of  the  pituitary  and  from  the  adrenal  medulla  also  serve 
to  cause  constriction  of  the  arteries  and  perhaps  also  of  the  capillaries. 

There  is  therefore  a  complex  mechanism  for  ensuring  that  the  pres- 
sure of  the  blood  is  maintained  and  the  flow  directed  into  the  part  of 
the  body  that  requires  it  for  the  time  being. 

20.  Lymphatic  system  of  Amphibia 

The  transfer  of  substances  between  the  cells  and  the  blood-stream  is 
effected  in  any  vertebrate  by  a  transudation  through  the  walls  of  the 
capillaries  into  the  tissue  fluids.  Under  the  pressure  of  the  heart-beat 
water  and  solutes  leave  the  capillaries,  passing  through  their  walls, 
while  proteins  remain  behind.  The  blood  passing  into  the  venous 
ends  of  the  capillaries  therefore  has  a  high  colloid  osmotic  pressure 
and  this  serves  to  suck  back  fluid  from  the  tissues.  In  this  way  a 
circulation  from  the  capillaries  into  the  spaces  around  the  cells  is 


xii.  21  BLOOD  OF  AMPHIBIA  339 

produced.  Clearly,  however,  it  is  essential  for  this  mechanism  that 
the  pressure  of  the  ventricular  heart-beat  shall  exceed  the  colloid 
osmotic  pressure  of  the  blood.  This  it  does  by  about  three  times  in  the 
frog. 

The  lymphatic  system  consists  of  a  set  of  spaces  which,  in  the  frog 
at  least,  communicate  with  the  tissue  spaces  around  the  capillaries. 
Injection  of  gum  into  the  lymphatic  system,  by  increasing  the  colloid 
osmotic  pressure  in  the  tissue  spaces,  prevents  the  back  suck  of  fluid 
into  the  venules  and  hence  leads  to  swelling  of  the  part  injected.  The 
lymph  spaces  in  the  tissues  join  to  form  larger  channels  and  great 
sinuses,  such  as  that  below  the  loose  skin  of  the  back  of  the  frog.  The 
lymph  is  kept  circulating  by  the  action  of  lymph  hearts.  In  the  frog 
there  are  anterior  and  posterior  pairs  of  these,  opening  into  veins.  The 
more  posterior  pair  lies  on  either  side  of  the  coccyx  and  can  be  seen  if 
the  skin  is  removed.  The  lymphatic  vessels  also  assist  in  the  process 
of  repair.  If,  after  injury,  red  cells  come  to  lie  in  the  tissues  the  lym- 
phatics send  out  sprouts  for  as  far  as  -^  mm  to  pick  them  up  and 
return  them  to  the  blood-stream. 

21.  The  blood  of  Amphibia 

The  red  corpuscles  of  amphibia  are  much  larger  than  those  of 
mammals,  reaching  in  the  urodele  Amphiuma  the  immense  size  of 
yofx;  they  nearly  always  exceed  20  fi.  The  red  cells  are  formed  mainly 
in  the  kidney,  and  are  destroyed,  after  a  life  of  about  100  days,  by  the 
spleen  and  liver.  The  bone-marrow  is  a  source  of  red  cell  formation 
in  Ra?ia  temporaria  but  not,  except  during  the  breeding-season,  in 
R.  pipiens.  A  process  of  breaking  up  of  the  red  cells  occurs  after  they 
have  entered  the  blood-stream,  giving  a  number  of  enucleated  frag- 
ments, and  this,  when  the  part  remaining  with  the  nucleus  is  small, 
produces  a  result  like  the  extrusion  of  the  nucleus  during  the  develop- 
ment of  the  red  cell  of  mammals.  In  Rana  only  small  portions  of  the 
cytoplasm  are  broken  off  in  this  way,  but  in  Batrachoseps  a  large 
proportion  of  enucleated  corpuscles  is  produced. 

The  haemoglobin  of  the  frog  has  a  lower  affinity  for  oxygen  than 
that  of  mammals,  even  when  both  are  considered  at  the  same  tempera- 
ture, and  in  this  respect  is  notably  less  efficient.  Also,  although  the 
power  of  the  blood  to  combine  with  carbon  dioxide  is  great,  there  is  a 
less  delicate  regulation  of  the  reaction  of  the  blood  than  in  mammals. 

The  white  cells  of  amphibia  are  of  three  types,  lymphocytes,  with  a 
large  nucleus  and  small  cytoplasm,  monocytes,  which  are  larger 
phagocytic    macrophages,    and    polymorphonuclear    granulocytes. 


34°  AMPHIBIA  xn.  21- 

These  last  may  be  neutro-,  eosino,  or  basiphil  and  are  migratory  and 
phagocytic.  Thus  the  white  cell  picture  with  which  we  are  familiar  in 
mammals  was  evidently  established  a  very  long  time  ago. 

There  is  a  globular  spleen  near  the  tail  of  the  pancreas. 

The  blood  of  frogs  also  contains  numerous  small  platelets  (thrombo- 
cytes), which  probably  break  down  when  in  contact  with  foreign 
surfaces  to  produce  the  thrombin  that  combines  with  the  fibrinogen 
of  the  blood-plasma  to  produce  clotting. 

22.  Urinogenital  system  of  Amphibia 

The  excretory  organs  of  adult  amphibia  are  always  the  tubules  of 
the  mesonephros.  In  Rana,  where  there  is  a  general  shortening  of 
the  body,  these  extend  over  only  a  small  number  of  segments  and  the 
kidneys  are  compact.  In  urodeles  and  the  primitive  frog  Ascaphus 
the  kidneys  are  elongated  and  show  some  evidence  of  their  segmental 
nature.  The  mesonephros  consists  essentially  of  a  series  of  tubules 
leading  from  the  nephric  funnels  to  the  Wolffian  duct.  In  the  frog  the 
funnels  do  not  open  into  the  tubules,  however,  but  into  the  veins; 
moreover,  they  form  independently  of  the  rest  of  the  tubule.  In  the 
adult  there  are  some  2,000  glomeruli,  from  each  of  which  a  short 
ciliated  tube  leads  to  the  proximal  convoluted  tubule.  There  follows 
a  second  short  ciliated  region,  corresponding  in  position  to  the  Henle's 
loop  of  mammals,  and  leading  to  a  distal  convoluted  tubule,  which 
joins  the  Wolffian  duct. 

The  blood-supply  of  the  kidney  differs  from  that  of  mammals  in 
that  blood  arrives  from  two  distinct  sources;  the  branches  of  the 
renal  artery  run  mainly  to  the  glomeruli,  those  of  the  renal  portal 
vein  to  the  tubules.  This  corresponds  to  the  functions  now  well 
established  for  those  two  parts,  namely  that  the  glomerulus  filters  off 
water  and  crystalloids,  some  of  which  are  then  reabsorbed  by  the 
tubule.  Many  details  of  this  process  are  not  clear,  however,  for 
instance  how  the  urea  concentration  in  the  urine  is  raised  many  times 
above  that  of  the  blood. 

The  frog,  having  a  moist  skin,  is  presumably  in  constant  danger  of 
osmotic  flooding  with  water  when  it  is  submerged,  and  of  desiccation 
when  on  land.  The  flooding  is  prevented  by  the  efficient  functioning 
of  the  glomeruli;  they  allow  the  frog  to  excrete  as  much  as  one-third 
of  its  weight  of  water  per  day  (man  i/50th).  The  mechanisms  for 
resistance  to  desiccation  are  less  perfect.  There  is  no  long  water 
reabsorbing  segment,  the  part  of  the  tubule  corresponding  to  Henle's 
loop  being  short.  There  is,  however,  a  large  cloacal  (allantoic)  bladder 


xii.  22  REPRODUCTION  341 

(to  be  distinguished  from  the  mesodermal  bladder  of  fishes)  from 
which  water  can  be  reabsorbed.  Certain  desert  amphibia  (Chiroleptes) 
conserve  water  by  losing  the  glomeruli  altogether.  Rana  cancrivora  is 
euryhaline  and  may  have  2-9%  of  urea  in  the  blood  (Gordon  1961). 

The  Miillerian  duct,  by  which  eggs  are  carried  to  the  exterior, 
develops  separately  from  the  Wolffian  system  in  the  frog,  but  arises 
from  the  latter  during  development  in  urodeles.  In  this,  as  in  many 
other  features,  the  frog  shows  a  greater  degree  of  specialization  of  its 
developmental  processes.  The  ovaries  are  mere  folds  of  the  peri- 
toneum, having  no  solid  stroma  such  as  is  found  in  mammals.  There 
are,  however,  follicle  cells  around  each  egg;  these  presumably  pro- 
duce the  ovarian  hormones.  Sections  of  an  ovary  show  eggs  in  various 
stages  of  development,  but  not  all  those  that  begin  complete  their 
maturation;  many  degenerating,  atretic  eggs  are  found.  Ripening  of 
the  eggs  proceeds  under  the  influence  of  a  hormone  produced  by  the 
anterior  lobe  of  the  pituitary.  This  in  turn  is  controlled  by  external 
environmental  factors  to  ensure  breeding  in  the  spring.  Suitable 
injections  of  mammalian  anterior  pituitary  extracts  will  ensure  ripen- 
ing of  the  ovaries  and  ovulation  at  any  time  of  year.  The  'prolans' 
excreted  in  the  urine  of  pregnant  women  have  a  similar  effect,  and 
the  production  of  ovulation  in  Xenopas  is  used  as  a  test  for  the  diagno- 
sis of  human  pregnancy. 

Having  left  the  ovary  the  eggs  find  their  way  to  the  mouths  of  the 
oviducts  mainly  by  ciliary  action  of  the  latter.  The  walls  of  the  oviduct 
are  glandular  and  secrete  the  albumen;  they  are  dilated  at  the  lower 
end  to  form  uterine  sacs,  in  which  the  eggs  are  stored  until  laid. 

The  testes  discharge  directly  through  the  mesonephros  by  special 
ducts,  the  vasa  efferentia,  formed  by  outgrowths  from  the  mesone- 
phros into  the  gonad.  This  is  presumably  a  secondary  development 
from  the  original  vertebrate  condition  in  which  the  sperms  were 
carried  away  by  the  nephrostomes.  The  fact  that  the  sperms  pass 
through  the  kidney  emphasizes  that  the  amphibia  have  diverged  at 
a  very  early  stage  of  the  evolution  of  the  vertebrate  stock,  and  remain 
still  in  many  respects  at  a  lower  level  of  evolution  than  the  modern 
fishes,  all  of  which  have  acquired  separate  urinary  and  genital  ducts. 
In  Alytes,  in  many  ways  primitive,  the  sperms  do  not,  however,  pass 
through  the  kidney! 

In  some  frogs  (R.  temporaria)  there  is  a  special  diverticulum,  the 
vesicula  seminalis,  leading  by  several  small  channels  to  the  lower  end 
of  the  Wolffian  duct.  It  contains  spermatozoa  during  the  breeding- 
season  and  its  appearance  suggests  a  secretory  activity. 


342  AMPHIBIA  xn.  22- 

Most  of  the  amphibia  have  failed  to  effect  the  complete  transfer  to 
land  life :  they  return  each  year  to  the  water  to  breed.  Special  modifica- 
tions of  the  reproductive  system  for  land  life  are  therefore  not  found. 
Secondary  sexual  differences  are  marked  in  many  species.  In  frogs 
the  males  precede  the  females  to  the  water  and  then  attract  the  latter 
by  their  vocal  apparatus.  The  male  clings  to  the  back  of  the  female 
by  means  of  a  'nuptial  pad',  developed  as  an  extra  digit,  prepollex, 
on  the  hand  (p.  317).  Injection  of  male  hormones  or  implantation 
of  testis  will  cause  this  organ  to  develop  in  young  female  frogs. 

In  newts  fertilization  is  ensured  by  an  elaborate  courtship.  Sperms 
are  made  into  spermatophores  by  special  pelvic  and  cloacal  glands 
and  there  are  also  abdominal  glands,  which  produce  a  secretion  attrac- 
tive to  the  female.  After  a  courtship  ceremony  the  spermatophores  are 
picked  up  by  the  cloaca  of  the  female  and  stored  in  a  spermathecal 
chamber. 

23.  Digestive  system  of  Amphibia 

Nearly  all  adult  amphibia  feed  on  invertebrates,  mainly  insects, 
partly  also  worms,  slugs  and  snails,  spiders  and  millipedes.  The  larval 
stages  are  usually  omnivorous,  but  they  may  be  cannibalistic,  feeding 
on  the  tadpoles  of  the  same  or  other  species — an  interesting  form  of 
provision  for  the  next  generation  by  excess  productivity  of  the 
mother.  There  are  only  minor  modifications  of  particular  species  in 
relation  to  their  diet;  as  regards  their  food  amphibia  occupy  a  general- 
ized or  'easy'  habitat.  The  fact  that  they  are  not  particular  in  choice 
of  diet  has  no  doubt  been  part  of  the  secret  of  their  success. 

The  tongue  is  the  characteristic  organ  for  catching  the  food  and  is 
one  of  the  special  features  required  for  terrestrial  life,  being  reduced 
in  aquatic  amphibia.  In  Rana  it  is  attached  to  the  floor  of  the  mouth 
anteriorly  and  flicked  outwards  by  its  muscles.  To  keep  it  moist  and 
sticky  a  special  inter-maxillary  gland  is  found.  From  the  shape  of  the 
premaxillae  it  can  be  deduced  that  this  gland  was  present  in  labyrin- 
thodonts.  The  saliva  contains  a  weak  amylase  and  some  protease.  It 
is  suggested  that  these  serve  to  release  sufficient  substances  for  tasting. 
Special  tracts  of  cilia  carry  the  secretion  from  the  intermaxillary 
glands  to  the  vomero-nasal  organ  and  palatal  taste-buds  (Francis, 
1 961). 

Another  feature  made  necessary  by  terrestrial  life  is  the  presence  of 
cilia  to  keep  the  fluids  moving  over  the  oral  surfaces.  These  cilia  are 
absent  in  aquatic  amphibia. 

The  teeth  on  the  premaxillae,  maxillae,  and  vomers  are  used  only 


xii.  23  FEEDING  343 

to  prevent  the  escape  of  the  prey;  few  amphibia  bite.  Biting  teeth 
are  present,  however,  in  the  adult  Ceratophrys  ornata,  whose  larvae 
also  have  powerful  jaws  and  are  cannibalistic.  The  South  American 
tree-frog  Amphignaihodon  has  teeth  in  the  lower  as  well  as  the  upper 
jaw  and  presumably  has  redeveloped  them,  a  remarkable  case  of  the 
reversal  of  evolution.  Teeth  are  also  present  on  the  lower  jaw  of  most 
urodelcs. 


dhc 


Fig.  201.  Transverse  section  of  the  spinal  cord  of  a  frog,  showing  cells  in  the  grey 
matter  with  their  axons  and  dendrites  spreading  into  the  'white'  matter. 

ax.  axon  of  ventral  horn  cell,  leaving  cord  in  ventral  root;  d.  dendrite  of  ventral  horn  cell; 

dhc.  small  cells  of  dorsal  horn;  dr.  dorsal  root  entry;  m.  cell  body  of  ventral  horn  cell;  tieur. 

neuropil  at  periphery  of  spinal  cord;  vhc.  small  cell  of  ventral  horn.  (After  Gaupp.) 


The  oesophagus  is  not  sharply  marked  off  from  either  mouth  or 
stomach  and  the  latter  is  a  simple  tube.  Its  lining  epithelium  of 
mucus-secreting  cells  is  folded  and  simple  tubular  glands  open  at  the 
base  of  the  folds.  These  glands,  unlike  those  of  mammals,  are  com- 
posed of  only  a  single  type  of  cell,  which  secretes  both  the  acid  and  the 
pepsin  found  in  the  stomach. 

The  intestine  is  marked  off  from  the  stomach  by  a  pyloric  sphincter. 
It  is  relatively  short  and  dilates  into  a  large  intestine,  there  being  a 
valve  interposed  in  the  frogs,  though  not  in  all  amphibia.  The  liver 
and  pancreas  have  the  structure  common  to  all  vertebrates  and  pro- 
duce juices  of  the  usual  type.  The  intestine  of  the  omnivorous  tadpole 
is  more  coiled  than  that  of  the  adult  frog.  The  type  of  food  taken 
depends  on  what  is  available,  most  species  of  amphibia  are  not  par- 
ticular feeders.  However,  they  can  learn  with  only  one  or  two  trials 
to  avoid  distasteful  insects.  Frogs  and  toads  devour  large  numbers  of 
insects.  If  the  common  insects  available  are  pests  the  amphibian's  part 
in  controlling  their  number  works  to  the  advantage  of  man. 


(344) 

24.  Nervous  system  of  Amphibia 

The  organization  of  the  nervous  system  of  amphibia  might  be  said 
to  be  essentially  similar  to  that  of  fishes.  In  both  groups  there  are 
highly  developed  special  centres  in  the  brain,  each  centre  related  to  a 


verb.  7. 


n.S 


n.10 


n.11 


Fig.  202.  Ventral  branches  of  the  spinal  nerves  (2-1 1)  of  the  frog.  The  sympathetic  chain 

is  also  shown. 

g.X,  vagus  ganglion;  int. a.  intestinal  artery;  n.spl.  splanchnic  nerve;  n.  (2-1 1),  spinal  nerves; 
sub.  subclavier  artery,  sym.  sympathetic  chain;  vert.  1,  1st  vertebra.  (After  Gaupp.) 

special  receptor  system.  In  neither  group  is  there  a  dominant  part, 
integrating  the  activity  of  the  whole,  as  does  the  cerebral  cortex  in 
mammals. 

The  plan  of  the  spinal  cord  is  like  that  of  fishes,  but  well-marked 
dorsal  and  ventral  horns  are  present.  The  large  motor-cells  of  the  cord 
have  dendrites  that  spread  widely  in  the  white  matter,  where  their 


XII.  24 


BRAIN 


345 


synaptic  connexions  are  made  in  a  complicated  'neuropil'  (Fig.  201). 
This  is  a  simpler  arrangement  than  is  found  within  the  grey  matter  of 
the  mammalian  curd. 


n.otf. 


cer.h. 


cereb. 


n.  9, 10,11 


Fig.  203.  The  brain  of  Rana,  dorsal  view. 

cer.h.  cerebral  hemisphere;  cereb.  cerebellum;  epi.  epiphysis;  hth.  hypothalamus;  hyp.  pitui- 
tary gland;  lam.t.  lamina  terminalis;  olf.l.  olfactory  lobe;  n.olf.  olfactory  nerve;  n.  3-1 1  cranial 
nerves;  «.  (1  and  2),  spinal  nerves;  opt.  c.  optic  chiasma;  opt.l.  optic  lobe;  opt.t.  optic  tract. 
(Modified  from  Gaupp.) 

The  arrangement  of  the  spinal  nerves  is  much  modified  by  the 
development  of  the  limbs.  Ten  spinal  nerves  are  found  but  since  an 
embryonic  first  one  is  missing  they  are  sometimes  numbered  2-1 1  (Fig. 
202).  Two  spinal  segments  contribute  to  the  brachial  and  four  to  the 
sciatic  plexuses  in  the  frog.  From  these  plexuses  fibres  are  distributed 
to  the  muscles  and  skin  of  the  limbs  (Fig.  202). 


346  AMPHIBIA  xii.  24 

The  brain  (Figs.  203  and  204)  resembles  that  of  Dipnoi  very  strik- 
ingly. The  prosencephalon  is  based  on  an  inverted  plan  (p.  211);  the 
large  evaginated  cerebral  hemispheres  therefore  have  a  thick  nervous 
roof  as  well  as  floor.  In  the  frog  there  is  only  a  short  unpaired  region 
of  the  forebrain  (diencephalon)  but  this  is  longer  in  urodeles.  The 
walls  of  each  hemisphere  may  be  divided  into  a  dorsal  pallium,  medial 
ventral  septum,  and  latero-ventral  striatum  (Fig.  205).  The  cell  bodies 
lie  around  the  ventricle  in  all  parts  of  the  hemisphere  and  there  are 
several  layers  of  them.  The  cells  are  pyramidal  in  shape  and  the  con- 
nexions are  made  in  the  outer  'white'  matter. 

Nearly  all  parts  of  the  hemisphere  are  reached  by  olfactory  tract 
fibres,  the  axons  of  the  mitral  cells  of  the  olfactory  bulb  (Fig.  205). 
In  the  frog  there  are  regions  at  the  hind  end  of  the  hemispheres  that 
receive  forwardly  directed  fibres,  some  probably  connected  with  tactile 
and  others  certainly  with  optic  impulses.  There  is  therefore  some 
opportunity  for  the  hemispheres  to  act  as  correlating  centres,  but  we 
have  little  information  as  to  the  functions  performed  in  them.  Their 
backward  projections  are  made  by  means  of  two  large  tracts,  the 
lateral  and  medial  forebrain  bundles,  but  these  reach  only  to  the 
thalamus,  hypothalamus,  and  midbrain,  not  back  to  the  cord.  Elec- 
trical stimulation  of  the  forebrain  does  not  produce  movements  of  the 
animal;  presumably  such  a  crude  method,  though  it  may  excite  a 
few  neurons,  cannot  imitate  the  more  subtle  patterns  in  which  they 
are  normally  active. 

Removal  of  the  cerebral  hemispheres  is  said  to  have  little  influence 
on  the  normal  feeding  and  other  reactions  of  the  frog.  After  this 
operation  the  animals  are  said  to  be  more  sluggish,  to  show  less 
'spontaneity',  and  to  learn  less  well.  If  the  latter  is  true  it  shows  a 
considerable  advance  in  the  functioning  of  the  hemispheres  over  the 
stage  reached  in  fishes,  whose  learning  can  certainly  take  place  in 
other  parts  of  the  brain,  and  is  apparently  little  affected  by  removal 
of  the  forebrain  (p.  210). 

Some  indication  of  the  function  of  the  cerebral  hemispheres  is  given 
by  the  fact  that  by  placing  electrodes  connected  with  a  suitable  am- 
plifier upon  them,  rhythmical  changes  of  potential  can  be  recorded 
(Fig.  206).  These  are  most  marked  in  the  olfactory  bulb  and  probably 
propagate  backwards  along  the  hemisphere.  The  rhythms  continue 
even  in  a  brain  that  has  been  removed  from  the  head.  They  are  there- 
fore a  sign  of  some  intrinsic  activity  of  the  brain,  rather  than  of  re- 
sponse to  peripheral  stimulation. 

The  diencephalon  is  interesting  chiefly  for  the  considerable  number 


tam.t. 


Fig.  204.  Two  further  views  of  the  brain  of  Rana. 
Above:  ventral  view.  Below:  lateral  view.  (Modified  after  Gaupp.) 
Lettering  as  Fig.  203. 


(34§) 


Lateral 


Medial 


m.Fb. 


olFtr 


Fig.  205.  Diagrams  of  the  structure  and  probable  cell  connexions  in,  A,  the  olfactory  bulb, 
and  b,  the  cerebral  hemisphere  of  the  frog. 

glom.  glomerulus  in  which  fibres  of  olfactory  nerve  make  contact  with  dendrites  of  mitral  cells ; 
gran,  granule  cell  (cell  without  any  axon);  l.f.b.  lateral  forebrain  bundle;  m.f.b.  medial  forebrain 
bundle;  wit.  mitral  cell;  olf.n.  fibres  of  olfactory  nerve;  olf.tr.  olfactory  tracts;  p.c.  periglomerular 
cell.  The  electrodes  are  shown  as  they  would  be  placed  for  recording  the  potentials  shown  in  Fig. 

206.  (From  Gerard  and  Young.) 


XII.  24-25  B  R  A I N  349 

of  optic  tract  fibres  that  end  in  its  walls;  other  sensory  projections 
also  reach  here.  In  anurans,  but  not  in  urodeles,  there  is  a  partial 
division  into  separate  thalamic  sensory  nuclei,  such  as  are  found  in 
mammals,  for  touch,  sight,  and  other  receptor  modalities. 

The  pineal  organ  shows  evidence  of  a  retina  in  a  few  amphibia; 
in  most  it  is  a  simple  sac. 

The  pituitary  body  is  well  developed  and  the  usual  partes,  anterior, 
intermedia,  nervosa,  and  tuberalis  can  be  recognized,  though  they  are 
not  in  the  same  relative  position  as  in  mammals. 


Fig.  206.  Rhythmical  changes  of  potential  between  electrodes  placed  on  the  surface 
of  the  olfactory  bulb  of  the  frog  as  in  Fig.  205.  (After  Gerard  and  Young.) 

The  midbrain  is  very  well  developed  and  shows  many  similarities  to 
that  of  fishes.  The  cells  it  contains  do  not  all  lie  round  the  ventricle, 
many  have  moved  out  to  make  an  elaborate  system  of  cortical  layers. 
Electrical  stimulation  of  various  parts  of  the  optic  tectum  produces 
movements  of  the  limb  and  other  muscles;  there  can  be  no  doubt 
that  this  region  plays  a  dominant  part  in  behaviour.  Most  of  the  fibres 
of  the  optic  tract  end  here,  and  there  are  also  other  pathways  from 
the  olfactory,  auditory,  medullary  (gustatory?),  and  spinal  regions. 
Efferent  fibres  leaving  the  tectum  pass  to  the  midbrain  base,  medulla, 
and  perhaps  back  into  the  cord.  This  region  therefore  has  wider  con- 
nexions than  any  other  part  of  the  nervous  system  and  thus  nearly 
reaches  the  status  of  a  dominant  integrating  organ. 

The  cerebellum  of  amphibia,  on  the  other  hand,  is  very  small; 
perhaps  because  these  are  mostly  animals  that  do  not  have  to  adjust 
themselves  freely  in  space  during  locomotion,  they  move  mainly  in  a 
single  plane.  There  is  little  need  for  control  of  speed  or  distance  of 
movement,  except  of  the  head  and  tongue,  which  are  controlled  by 
the  tectum. 

25.  Skin  receptors 

Lateral  line  organs  are  present  in  the  skin  of  all  aquatic  amphibian 
larvae  and  in  some  aquatic  adults,  such  as  those  of  the  anuran  family 
Pipidae.  They  are  of  simple  form,  consisting  of  groups  of  cells  in  an 


350  AMPHIBIA  xn.  25- 

open  pit.  In  newts  they  are  present  in  the  larvae,  which  are  aquatic, 
but  are  covered  by  epidermal  layers  during  the  first  post-larval  stage 
during  which  the  newt  lives  on  land.  In  the  final  aquatic  adult  stage 
the  organs  reappear. 

The  skin,  of  course,  also  contains  tactile  organs,  and  in  addition  is 
often  sensitive  to  chemical  stimuli.  This  chemical  sense  is  mediated 
by  fibres  running  in  the  spinal  nerves,  not  by  special  elements  such  as 
the  taste-buds  found  spread  out  over  the  body  in  fishes.  The  skin  is 
also  sensitive  to  heat  and  cold,  and  there  is  some  evidence  that  these 
senses  are  served  by  fibres  different  from  those  that  mediate  touch, 
pain,  or  the  chemical  senses.  Histologically,  however,  there  is  little 
sign  of  the  development  of  the  special  sensory  corpuscles  that  are 
so  conspicuous  in  the  skin  of  birds  and  mammals.  All  the  nerve- 
endings  are  of  the  type  known  as  'free  nerve-endings',  except  for  a  few 
touch  corpuscles  on  special  regions  such  as  the  feet.  In  this  the 
amphibia  again  resemble  the  fishes  and  show  less  differentiation  than 
do  the  higher  animals. 

The  taste-buds  on  the  tongue  and  palate  are  probably  able  to 
respond  to  the  presence  of  only  two  of  the  four  types  of  substance 
that  are  discriminated  by  mammals.  Applications  to  the  tongue  of  the 
frog  and  recordings  of  nerve-impulses  in  its  nerves  show  that  there 
are  chemoreceptors  present  able  to  respond  to  salt  and  sour  substances, 
but  that  no  reaction  is  given  to  substances  that  in  mammals  are  classed 
as  sweet  or  bitter. 

The  olfactory  organ  functions  both  on  land  and  in  the  water,  special 
mucous  glands  being  present  to  keep  it  moist  when  in  air.  A  continual 
circulation  of  water  or  air  is  maintained  over  the  olfactory  epithelium 
by  cilia  or  the  movements  of  respiration.  The  internal  nostril  may 
have  originally  developed  from  the  double  nostril  of  fishes,  in  order  to 
make  a  circulation  around  the  olfactory  receptors  possible.  Jacobson's 
organ  is  a  special  diverticulum  of  the  olfactory  chamber,  serving  to 
test  the  'smell'  of  food  in  the  mouth. 

The  Apoda,  being  blind,  have  a  great  development  of  the  sense  of 
smell,  including  a  hollow  tentacle  or  olfactory  tube. 

26.  The  eyes  of  Amphibia 

Provided  that  certain  requirements  are  met  the  air  gives  more  scope 
for  the  use  of  photoreceptors  than  does  the  water.  Light  is  trans- 
ported with  less  disturbance  through  the  air  and  image  formation  is 
facilitated  by  the  refraction  of  the  air-corneal  surface.  The  amphibia 
have  exploited  these  advantages  and  sight  has  become  the  dominant 


xii.  26  THE  EYE  351 

sense  of  most  of  the  forms.  For  clear  vision  it  is  essential  that  the 
surface  of  the  eye  be  protected,  kept  moist  and  free  of  particles,  and 
for  these  purposes  the  eyelids  and  lachrymal  glands  are  present.  The 
upper  lid  is  fixed,  but  the  lower  is  very  mobile  and  folded  to  make  a 
transparent  structure,  the  nicitating  membrane,  able  to  move  rapidly 
across  the  surface  of  the  eye. 


nm 


C    % 


Fig.  207.  The  amphibian  eye  and  its  accommodation. 

a,  anuran  eye  in  vertical  section,  ac.  area  centralis;  to.  inferior  oblique;  ir.  inferior  rectus; 
//.  lower  lid;  Im.  lens  muscles  (protractors);  n.  optic  nerve;  nm.  nictitating  membrane; 
pn.  pupillary  nodules;  sc.  scleral  cartilage;  so.  superior  oblique;  sr.  superior  rectus;  ul.  upper 
lid;  z.  zonula  Zinnii.  b,  anterior  segment  of  Bufo  in  relaxation.  C,  in  accommodation;  note 
forward  movement  of  lens.  (From  Walls,  after  Franz  and  Ueer.) 


The  eyeball  is  almost  spherical,  with  a  rounded  cornea.  The  lens  is 
farther  from  the  cornea  than  in  fishes  and  is  flattened,  more  so  in 
anurans  than  in  urodeles.  These  modifications  allow  focusing  of  a 
more  distant  image.  There  is  an  iris,  with  a  rapidly  moving  aperture, 
operated  by  powerful  circular  (sphincter)  and  radial  (dilatator) 
muscles.  Although  these  muscles  are  partly  actuated  by  a  nervous 
mechanism  they  are  also  directly  sensitive  to  light,  and  the  pupil  of 
the  isolated  eye  of  the  frog  shows  wide  excursions  with  change  of 
illumination. 

Accommodation  is  effected  by  protractor  lentis  muscles,  attached 
to  the  fibres  by  which  the  lens  is  supported  (Fig.  207).  These  muscles 


352  AMPHIBIA  xil.  26- 

move  the  lens  forward,  whereas  the  muscles  of  the  lens  of  teleostean 
fishes  move  it  backwards.  Other  fibres,  the  musculus  tensor  chorioi- 
deae,  run  radially  and  around  the  lens.  They  may  help  the  protractors, 
and  are  probably  the  ancestors  of  the  ciliary  muscles  of  higher 
forms. 

In  amphibia  living  in  the  water  the  eye  is  based  much  more  on  the 
fish  plan  and  the  lens  is  rounder.  There  are  then  no  lids  or  lachrymal 
glands  and  the  eye  is  enabled  to  make  an  image,  in  spite  of  the  absence 
of  the  air-corneal  interface,  by  a  thickening  of  the  inside  of  the  cornea. 

Rods  and  cones  are  present  in  the  retina,  the  former  containing 
visual  purple,  which  may  be  red  or  greenish.  The  two  sets  of  receptor 
are  apparently  found  throughout  the  retina  in  urodeles,  but  in  Rana 
there  is  a  macular  region  in  which  the  cones  are  in  excess  and  this  is 
still  further  developed  in  Bufo.  Study  of  the  impulses  in  the  optic 
nerves  of  Rana  shows  that  six  types  of  detector  operate  upon  the  infor- 
mation provided  by  the  rods  and  cones.  (1)  Contrast  detectors  give  a 
sustained  response  when  a  sharp  edge  moves  into  the  visual  field ;  (2) 
convexity  detectors  respond  to  objects  that  are  curved,  the  discharge 
being  greater  the  more  curved  (smaller)  they  are.  These  two  types 
together  may  be  called  'on'  fibres;  (3)  moving-edge  detectors  ('on/off' 
fibres)  respond  with  a  frequency  proportional  to  the  velocity  of  move- 
ment; (4)  dimming  detectors  respond  on  reduction  of  illumination 
('off'  fibres);  (5)  darkness  detectors  fire  with  frequency  inversely  pro- 
portional to  illumination.  These  types  of  fibre  project  to  different 
depths  in  the  tectum  as  sheets  of  endings,  and  the  arrangement  of  the 
retina  is  accurately  reproduced  there  although  the  fibres  are  interwoven 
in  the  nerve  (perhaps  to  prevent  'cross-talk').  Moreover,  if  the  nerve 
is  severed  the  fibres  regenerate  in  such  a  way  as  to  reconstitute  the 
map.  The  sixth  type  of  fibre  is  sensitive  to  blue  light  and  is  connected 
with  the  thalamus. 

These  operations  serve  to  provide  reports  of  the  types  of  change 
relevant  to  the  animal.  Thus  the  second  type  might  be  called  'insect 
detectors',  responding  when  a  small  dark  object  enters  the  field 
and  moves  about  intermittently.  More  complex  visual  discrimina- 
tions are  also  possible,  for  example  toads  can  distinguish  between 
shapes. 

The  skin  is  probably  sensitive  to  light  in  all  amphibians :  frogs  react 
to  light  even  after  removal  of  the  eyes  and  cerebral  hemispheres.  This 
skin  sense  is  especially  developed  in  certain  cave-living  urodeles, 
Proteus,  in  which  the  eyes  are  not  functional.  A  similar  degeneration 
also  occurs  in  Apoda. 


XII.  27  (353) 

27.  The  ear  of  Amphibia 

The  inner  ear  is  divided  into  a  utricle,  from  which  the  semicircular 
canals  arise,  and  a  saccule,  from  which  there  is  a  diverticulum,  the 
lagena,  part  of  whose  receptor  surface  is  covered  with  a  tectorial 
membrane  somewhat  similar  to  that  of  mammals.  There  is,  however, 
no  coiled  cochlea.  The  middle  ear  of  the  frog  consists  of  a  funnel- 
shaped  tympanic  cavity  communicating  with  the  pharynx  and  closed 
externally  by  a  tympanum  supported  by  a  tympanic  ring.  Sound 
waves  are  transmitted  across  the  cavity  by  a  rod,  the  columella,  fitting 
by  an  expanded  foot,  the  otostapes,  into  the  fenestra  ovalis,  a  hole  in 
the  wall  of  the  auditory  capsule.  This  hole  is  also  partly  occupied  by 
a  second  plate,  the  operculum,  which  is  joined  to  the  scapula  by  a 
special  opercular  muscle.  The  operculum  and  otostapes  develop  with- 
in the  wall  of  the  auditory  capsule  and  the  middle  part  of  the  colu- 
mella (mediostapes)  forms  as  an  outgrowth  from  the  otostapes.  The 
outer  part  of  the  columella  (extra-columella)  and  the  tympanic  ring 
develop  close  to  the  quadrate  and  probably  from  its  cartilage. 

The  columella,  therefore,  shows  no  developmental  relationships  to 
the  hyoid  arch.  The  tympanic  cavity  is  developed  from  the  spiracular 
cleft,  after  a  strange  series  of  changes.  The  original  cleft  degenerates 
six  days  after  hatching  but  about  six  of  its  lining  cells  persist  and  at 
the  end  of  the  tadpole  stage  form  a  tympanic  vesicle,  which  becomes 
connected  with  the  pharynx  by  a  rod  of  cells.  This  rod  then  degener- 
ates again  and  an  open  air  passage  to  the  vesicle  of  the  drum  is  not 
established  until  some  thirty  days  after  emergence  from  the  water, 
when  a  pouch  from  the  pharynx  joins  the  tympanic  cavity.  These 
events  show  the  complexities  that  may  result  from  the  modification 
of  developmental  processes,  and  they  emphasize  the  difficulty  in 
assigning  'homologies'.  It  is  still  debated  to  what  extent  the  middle 
ear  of  the  frog  can  be  compared  with  that  of  amniotes.  The  hyo- 
mandibular  nerve,  which  divides  above  the  middle  ear  of  amniotes 
(and  above  the  spiracle  of  the  dogfish)  lies  behind  the  tympanic  cavity 
of  the  frog  and  branches  below  it. 

The  arrangement  for  conveying  vibrations  to  the  ear  varies  con- 
siderably among  amphibians.  In  urodeles  there  is  no  tympanum.  In 
some  of  them  the  columella  is  attached  to  the  squamosal,  perhaps  in 
connexion  with  a  semi-aquatic  or  burrowing  habit.  A  similar  arrange- 
ment may  have  been  present  in  the  earliest  amphibians,  which  have 
a  columella  but  no  oval  window.  In  other  urodeles  (Plethodontidae) 
the  columella  is  attached  to  the  quadrate  and  there  may  be  a  second 


354  AMPHIBIA  xn.  27- 

ossicle,  the  operculum,  working  in  parallel,  with  its  inner  end  in  the 
oval  window  caudal  to  the  columella  and  its  outer  end  attached  by  a 
muscle  to  the  scapula.  In  terrestrial  forms  the  columella  becomes  fused 
with  the  window  at  metamorphosis  and  its  function  is  taken  over  by 
the  operculum,  probably  receiving  vibrations  from  the  fore-legs.  The 
more  aquatic  forms  (Cryptobranchus)  retain  the  larval  condition  and 
never  develop  an  operculum.  The  tympanum  and  columella  are  also 
reduced  in  some  terrestrial  anurans  {Bombinator)  but  in  the  aquatic 
Xenopus  and  Pipa  the  operculum  and  its  muscle  are  lost,  perhaps  a 
paedomorphic  feature. 

The  sense  of  hearing  is  certainly  well  developed,  especially  in 
Anura,  which  respond  to  vibrations  from  50  to  10,000  a  second.  The 
hearing  is  used  especially  in  the  breeding-season,  when  the  croaking 
serves  to  attract  both  sexes  to  the  water.  The  prey  may  also  be  located 
by  sound.  Urodeles  have  been  shown  to  give  no  response  to  the  ring- 
ing of  a  bell  suspended  from  the  ceiling,  which,  however,  produces 
reactions  in  Rana  and  Bufo. 

A  peculiar  feature  of  many  Anura  is  an  immense  backward  develop- 
ment of  the  perilymphatic  space  of  the  inner  ear,  forming  a  sac 
extending  above  the  brain  and  on  either  side  of  the  spinal  cord  as  far 
back  as  the  sacrum.  Portions  of  this  sac  emerge  between  the  vertebrae, 
showing  as  whitish  masses  on  account  of  the  granules  of  chalk  they 
contain.  The  calcium  salts  in  these  sacs  diminish  greatly  during 
metamorphosis  and  they  then  refill.  The  system  may  serve  as  a 
calcium  reserve  also  for  the  adult. 

28.  Behaviour  of  Amphibia 

The  habits  of  amphibia,  like  their  special  structures,  enable  them 
to  deal  with  the  various  emergencies  that  threaten  the  continuation  of 
life  on  land.  Frogs  and  toads  have  a  strong  sense  of  place  and  they 
show  distinct  'homing'  reactions.  They  are  able  to  learn  to  find  their 
way  out  of  mazes  and  to  remember  the  way  for  periods  of  at  least 
thirty  days. 

Complex  migrations  are  made  by  many  species;  nearly  all  migrate 
to  the  water  in  spring.  In  this  migration  the  males  usually  precede 
the  females,  then  attract  the  latter  by  their  calling.  The  receptors  for 
the  orientation  towards  the  water  are  known  in  the  osmoreceptors  in 
the  mouth  of  the  frog.  This  orientation  is  particularly  clear  in  uro- 
deles, in  which  sound  plays  no  part  in  the  migration.  The  power  to 
find  water  is  obviously  of  first  importance  for  any  animal  living  on 
land,  and  further  study  of  the  receptors  involved  would  be  interesting. 


xii.  28  BEHAVIOUR  355 

The  search  for  food  and  the  avoidance  of  enemies  are  not  in  prin- 
ciple more  difficult  on  land  than  in  the  water,  but  they  probably 
demand  new  mechanisms.  For  example,  the  greater  range  of  visibility 
can  be  a  disadvantage,  especially  when  it  is  exploited  by  one's  success- 
ful and  predatory  descendants.  A  hawk  or  owl  makes  fuller  use  of  its 
opportunities  in  this  respect  than  does  the  frog,  who  can  only  remain 
safe  from  them  by  behaviour  that  keeps  it  concealed.  Similarly  there 
are  dangers  in  certain  situations,  for  instance  of  desiccation,  which 
are  additional  to  those  that  are  met  by  an  animal  in  the  water. 

In  the  emergence  of  the  first  land  vertebrates  we  thus  see  a  con- 
spicuous example  of  the  invasion  by  living  things  of  a  medium  far 
different  from  themselves.  This  produces  a  situation  that  calls  forth 
all  the  powers  of  the  race  to  produce  new  types  of  individual,  and 
necessitates  that  the  individuals  make  full  use  of  their  capacities. 
New  patterns  of  structure  and  behaviour  are  developed  as  the  various 
possible  situations  emerge.  The  types  of  organization  that  at  first 
manage  to  survive  gradually  give  place  to  others,  still  more  complex 
or  'higher'.  Some  traces  of  the  organization  of  the  early  venturers  can 
still  be  seen  in  the  amphibia,  which  today  exploit  the  damper  situa- 
tions on  the  earth. 


XIII 

EVOLUTION  AND  ADAPTIVE  RADIATION  OF 

AMPHIBIA 

1 .  The  earliest  Amphibia 

There  are  such  close  resemblances  between  the  skulls  of  the  earliest 
amphibians  and  those  of  the  Devonian  crossopterygian  fishes  that 
there  can  be  no  doubt  of  the  relationship  (Fig.  194).  At  present  there 
is,  however,  no  detailed  fossil  evidence  of  the  stages  of  transition 
from  the  one  type  to  the  other.  The  fossils  that  appear  to  be  closest 
to  the  possible  tetrapod  ancestor  are  the  osteolepids  of  the  Lower  and 
Middle  Devonian  periods,  about  375  million  years  ago.  These  were 
definitely  fishes,  though  they  may  have  breathed  air.  *Elpistostege  is 
a  single  Upper  Devonian  skull  intermediate  between  such  fishes  and 
the  earliest  undoubted  tetrapods,  *Ichthyostega  and  similar  forms, 
found  recently  in  freshwater  beds  of  Greenland.  These  are  dated  as 
very  late  Devonian  or  early  Carboniferous,  that  is  to  say  about  350 
million  years  ago.  They  are  the  oldest  members  yet  found  of  the 
great  group  of  Stegocephalia,  which,  throughout  the  succeeding  100 
million  years  of  the  Carboniferous  and  Permian  periods,  flourished 
and  developed  many  different  lines,  one  giving  rise  to  the  reptiles  and 
others  to  the  modern  amphibia.  The  term  Stegocephalia  is  convenient 
to  cover  the  whole  group  of  palaeozoic  amphibia,  all  probably  of 
common  descent.  At  least  seven  types  can  be  recognized  (p.  296),  but 
attempts  to  group  these  have  not  been  altogether  successful;  the 
nomenclature  remains  confused.  The  Labyrinthodontia  were  the  central 
stock  and  were  in  the  main  terrestrial  forms,  giving  off  at  intervals  lines 
that  returned  to  the  water.  A  characteristic  labyrinthodont  feature  is 
a  folded  pattern  of  the  teeth,  similar  to  that  of  their  crossopterygian 
ancestors. 

The  earliest  Stegocephalia  were  definitely  tetrapods  and  already 
showed  sharp  changes  from  the  fish  type.  *Ichthyostega  is  known 
chiefly  from  the  skull  (Fig.  208),  which  shows  all  the  characteristic 
amphibian  features,  but  retained  traces  of  fish  ancestry  in  its  shape, 
with  a  short,  wide  snout  and  long  posterior  region  (table),  and  pre- 
sence of  a  preopercular  bone.  The  nostril  lies  on  the  very  edge  of  the 
upper  lip,  apparently  partly  divided  by  a  flange  of  the  maxilla  into 
internal  and  external  openings. 


XIII.    1-2 


(357) 


2.  Terrestrial  Palaeozoic  Amphibia.  Embolomeri  and  Rhachitomi 

We  possess  more  complete  information  about  the  slightly  later 
forms,  the  Embolomeri,  such  as  *Eogyrinus,  from  the  Lower  Carboni- 
ferous (Fig.  21 1).  These  were  long-bodied  animals,  rather  newt-like, 
and  their  small  limbs  cannot  have  made  very  effective  progress  on 
land.   They  probably  lived  mostly  in  the  water,   eating  fish.   The 


Fig.  208.  Skull  of  Ichthyostega.  (From  Westoll,  after  Save-Soderbergh.) 

d.  dentary;  en.  external  nostril;  ept.  ectopterygoid ;  jr.  frontal;  in.  internal  nostril;  ina. 
internasal;  /.  jugal;  la.  lachrymal;  mx.  maxilla;  na.  nasal;  pa.  parietal;  pal.  palatine;  pm. 
premaxilla;  pn.  postnarial;  po.  postorbital;  poj.  postfrontal;  pop.  preopercular;  ppa.  post- 
parietal;  prj.  prefrontal;  ps.  parasphenoid ;  pt.  pterygoid;  q.  quadrate;  qj.  quadratojugal ; 
san.  sur-angular;  sq.  squamosal;  sut.  supratemporal ;  /.  tabular;  v.  vomer. 

pectoral  girdle  was  still  joined  to  the  skull  by  a  process  of  the  tabular 
bone,  as  in  fishes.  The  pelvic  girdle  did  not  form  a  full  articulation 
with  the  sacral  vertebrae  but  was  apparently  attached  only  by  liga- 
ments. 

The  structure  of  the  vertebrae  has  given  rise  to  much  controversy. 
In  the  earliest  amphibia  we  find  three  elements,  a  more  dorsal  neuro- 
pophysis  and  a  centrum  composed  of  two  parts,  pleurocentrum  and 
hypocentrum,  the  latter  associated  with  a  ventral  arch  and  rib.  These 
elements  can  be  identified  in  the  vertebrae  of  crossopterygians  but  it 
is  still  not  clear  what  relationship,  if  any,  they  have  to  the  two  pairs  of 
vertebral  'arches'  alleged  to  be  present  in  elasmobranchs  (see  Williams, 

J959)- 


Triturus 


Fig.  209.  Various  urodele  amphibians,  not  all  to  same  scale  (mostly  from  life). 


xin.  2-3  FOSSIL  AMPHIBIA  359 

The  skull  shows  the  full  series  of  bones  that  we  have  already  dis- 
cussed; there  is  therefore  no  reason  to  suppose  that  these  animals 
represent  a  secondarily  'degenerate'  branch,  which  had  returned  to 
the  water.  They  were  probably  very  close  to  the  ancestors  of  all 
tetrapods.  They  were  numerous  in  the  Carboniferous  swamps,  but 
disappeared  early  in  the  Permian.  So  close  were  these  Embolomeri 
to  the  ancestry  of  the  reptiles  that  many  workers  classify  them  near 
the  Permian  *  Seymour  ia>  which  we  shall  consider  as  a  cotylosaurian 
reptile  (p.  386). 

Throughout  the  Carboniferous,  Permian,  and  Triassic  there  were 
abundant  amphibia  of  partly  terrestrial  habit,  the  Rhachitomi,  in 
which  both  vertebral  centra  were  present,  the  pleurocentrum  being 
the  larger.  *Eryops  (Fig.  211)  was  a  typical  form  living  in  the  Permian, 
about  250  million  years  ago.  The  animals  were  5  ft  or  more  in  length, 
rather  like  crocodiles,  relatively  shorter  in  body  and  tail  than  *Eogy- 
rinus  and  with  stronger  limbs.  Nevertheless  they  probably  lived  partly 
in  the  water  and  may  have  been  fish-eaters.  The  skull  was  long  and 
narrow  in  the  front  and  short  in  the  'table'  behind  the  eyes,  continuing 
the  previous  tendency.  A  characteristic  feature  of  later  labyrinthodonts 
now  began  to  appear,  namely  a  dorso-ventral  flattening  of  the  skull. 
The  pectoral  girdle  was  no  longer  attached  to  the  skull,  but  there  was 
a  joint  between  the  pelvic  girdle  and  the  sacrum.  Some  Permian 
Rhachitomi  became  still  more  completely  terrestrial  than  *Eryops, 
for  instance  *Cacops  had  very  large  limbs  and  protective  plates  along 
its  back. 

3.  Aquatic  Amphibia  of  the  later  Palaeozoic 

Other  lines  of  amphibia,  however,  show  an  accentuation  of  the 
tendency  to  return  to  the  water.  In  the  vertebrae  the  anterior  hypo- 
centrum  became  large,  while  the  pleurocentrum  disappeared.  At  the 
same  time  the  skull  became  very  flattened  and  the  limbs  weak.  Several 
stages  are  known  leading  from  the  Rhachitomi  to  these  fully  aquatic 
forms  of  the  Trias,  which  are  placed  in  the  suborder  Stereospondyli. 
*Capitosaurus  and  *Buettneria  are  typical  of  the  group,  which 
remained  numerous  until  near  the  end  of  the  Triassic  period,  about 
150  million  years  ago.  Probably  this  change  from  rhachitomous  to 
stereospondvlous  condition  occurred  on  several  independent  lines  of 
descent.  Thus  amphibia,  after  becoming  semi-terrestrial  in  the  Car- 
boniferous and  then  probably  giving  rise  to  the  early  reptiles,  later 
returned  to  the  water. 

We  also  have  record  of  various  other  secondarily  aquatic  amphi- 


(36o) 


Ascaphus 


Breviceps 


Polype  dates 


Ran  a 

Fig.  210.  Various  anuran  amphibians,  not  all  to  one  scale. 

(Ascaphus,  Nectophrynoides,  and  Polypedates  after  Noble,  Breviceps  after  Thompson, 
Gastrotheca  after  B.M.  Guide,  others  from  life.) 


xiii.  3  AQUATIC  AMPHIBIA  361 

bians  whose  affinities  are  less  certain.  They  have  in  common  a  reduc- 
tion of  ossification  in  general  and  in  particular  in  the  centra,  which 
seem  not  to  be  formed  from  separate  cartilaginous  elements  as  in 
labyrinthodonts  but  as  thin  continuous  sheets  of  bone.  Some  of  these 
animals  classed  as  Phyllospondyli  or  'Branchiosaurs'  were  almost 
certainly  larval  Rhachitomi;  the  external  gills  can  be  recognized  and 
stages  found  connecting  them  with  known  adults  of  that  group.  It  is 
necessary,  however,  to  retain  the  order  for  the  present. 

Other  early  aquatic  amphibia  are  less  easy  to  classify  and  are 
grouped  for  convenience  as  an  order  Lepospondyli,  all  having  verte- 
brae composed  of  a  single  piece,  and  a  continuous  notochord.  They 
show,  however,  at  least  three  distinct  lines,  probably  separate  off- 
shoots from  the  main  labyrinthodont  stock.  *Dolichosoma  and  other 
forms  from  the  Carboniferous  were  like  snakes  and  had  lost  the  limbs. 
*Diplocaulus  from  the  Permian  possessed  remarkable  horned  skulls. 
These  creatures  with  broad  flat  heads  and  upward-looking  eyes  and 
small  limbs  were  presumably  bottom-dwellers  and  the  development 
parallels  that  of  the  Stereospondyli.  A  third  aberrant  group  placed 
here,  the  Microsaurs,  such  as  *Microbrachis,  were  animals  with  long 
bodies  and  small  limbs,  presumably  aquatic,  but  showing  many 
similarities  to  the  reptiles  in  the  skull. 

The  order  Adelospondyli  has  been  created  for  a  further  collection 
of  presumably  secondarily  aquatic  amphibia  such  as  *Lysorophus,  in 
which  the  neural  arch  and  centrum  are  not  fused  but  articulate  by 
means  of  a  jagged  suture.  The  skull  shows  reduction  and  variation 
of  the  bones,  and  for  this  and  other  reasons  it  has  been  suggested  that 
the  urodeles  may  have  arisen  from  an  adelospondylous  line. 

The  relationship  of  the  modern  amphibia  to  these  palaeozoic 
stegocephalians  remains  uncertain.  The  earliest  anuran  is  *Proto- 
batrachus  of  the  Triassic,  possessing  ribs  and  a  tail,  but  with  elongated 
ilia  and  an  anuran  type  of  skull.  It  is  probably  a  larva  in  metamor- 
phosis. *Miobatrachus  of  the  Carboniferous  is  a  form  in  which  the 
posterior  portion  of  the  skull  is  shortened  and  the  temporal  bones  lost. 
In  other  respects  the  skull  is  like  that  of  a  rhachitome  and  suggests 
that  the  frogs  diverged  from  the  labyrinthodonts  at  this  very  early 
stage. 

The  urodeles  can  be  traced  back  only  to  the  Jurassic.  It  is  often 
suggested  that  both  they  and  the  Apoda  have  arisen  from  aquatic 
Lepospondyli,  such  as  the  microsaurs,  but  there  is  no  real  evidence 
of  this. 


362  AMPHIBIA  xiii.  4 

4.  Tendencies  in  the  evolution  of  fossil  Amphibia 

The  changes  in  the  form  of  amphibia  can  be  followed  from  the 
beginning  of  the  Carboniferous  to  the  end  of  the  Triassic  period,  and, 
indeed,  in  the  form  of  their  reptilian  descendants  far  beyond.  There 
are  signs,  however,  of  very  many  distinct  lines  (as  we  should  expect), 
and  it  is  not  possible  to  trace  details  of  the  history  or  fate  of  par- 
tieular  populations.  Two  distinct  tendencies  appear  over  this  period: 
(i)  to  become  fully  terrestrial,  (2)  to  return  to  the  water.  The  terres- 
trial forms  became  very  gradually  shorter  in  body  and  stronger  in  leg. 
The  skull  remained  fairly  high  and  domed  and  the  otic  notch  became 
deeper,  as  a  more  effective  tympanum  developed.  In  the  vertebrae 
the  hypocentrum  became  reduced  as  muscles  developed  attached  to 
the  pleurocentrum. 

Return  to  the  water  led  to  animals  of  two  distinct  types,  (a)  snake- 
like or  (b)  flattened,  but  in  both  there  was  a  reduction  of  limbs  and 
a  secondary  lengthening  of  the  body,  with  return  to  the  sinuous 
movements  of  fish-like  locomotion.  In  the  bottom-living  forms,  such 
as  some  Stereospondyli  and  *Diplocaahis  among  Lepospondyli,  the 
skull  became  flattened,  with  the  eyes  looking  upwards,  the  otic  notch 
being  shallow.  The  snake-like  *Dolichosoma  retained  the  more  normal 
skull  shape  but  became  immensely  elongated  and  lost  the  limbs 
altogether. 

These  observed  tendencies  can  be  understood  to  result  from  the 
situation  that  developed  as  the  vertebrates  first  colonized  the  land. 
The  earlier  amphibia,  such  as  *Eogyrinus,  were  partly  aquatic,  by 
force,  one  might  say,  of  inexperience.  Throughout  the  Carboniferous 
various  lines  of  them  became  more  fully  equipped  for  terrestrial  life, 
moving  faster,  seeing  and  hearing  better,  and  so  on.  The  competition 
and  predatory  attacks  of  these  more  successful  lines  then  drove  others 
back  into  the  water  and  so  the  process  continued,  until  later  the  earlier 
reptilian  lines,  themselves  driven  back  to  the  water  by  their  own 
descendants,  removed  most  of  the  amphibians  from  the  waters  as 
well  as  from  the  land,  leaving  only  some  few  remaining  populations, 
from  which  the  modern  orders  have  evolved. 

It  certainly  does  not  seem  necessary  to  postulate  any  special 
directive  force  to  explain  all  this.  We  could  wish,  of  course,  for 
much  more  information,  but  it  seems  reasonable  to  imagine  that 
these  changes  were  produced  by  the  action  of  the  animals  with  each 
other  and  with  the  environment,  supposing  that  the  animals  con- 
tinually strive  to  feed,  grow,  and  reproduce  others  rather,  but  not 
quite,  like  themselves. 


(363) 


Ichthyophis 


Fig.  2ii.  Chart  of  evolution  of  amphibia. 


364  AMPHIBIA  xiii.  4- 

It  must  be  stated,  however,  that  Watson,  who  has  contributed  more 
than  anyone  to  knowledge  of  amphibian  evolution,  believes  that  it  is 
possible  to  recognize  a  number  of  non-adaptive  trends,  which  are 
independent  of  environmental  influences.  Changes  suggested  by 
Watson  and  others  as  non-adaptive  include  flattening  of  the  skull, 
doubling  of  the  occipital  condyles,  reduction  of  the  number  of  roofing 
bones  and  loss  of  ossification  in  the  neurocranium,  the  changes  in  the 
vertebrae  already  mentioned,  and  many  other  features.  It  is  not 
entirely  clear  how  the  'non-adaptive'  nature  of  these  features  is  estab- 
lished. SevertzofT  has  suggested  that  the  flattening  of  the  head  is 
connected  with  the  development  of  a  large  mouth  for  buccal  respira- 
tion. Palaeontology  necessarily  deals  with  small  points  of  structure, 
whose  significance  for  the  animal  may  be  difficult  to  determine,  but 
it  does  not  follow  because  we  are  not  able  to  discern  the  significance 
of  a  part  that  it  therefore  has  none.  It  is  not  at  all  easy  in  biology  to 
hold  the  balance  between  credulous  acceptance  of  a  function  for 
every  character  and  a  sceptical  attitude  that  insists  on  regarding  the 
organic  world  as  a  jumble  of  unrelated  substances.  The  only  safe  rule 
is  to  search  continually  for  signs  of  regular  recurrence  of  similarities 
of  structure  and  action,  and  then  to  make  hypotheses  about  function, 
which  can  be  tested  by  experiment. 

5.  Newts  and  Salamanders.  Subclass  Urodela 

The  urodeles,  also  called  Caudata  or  tailed  amphibia,  show  less 
deviation  from  the  general  form  and  habitats  of  the  amphibia  as  a 
whole  than  do  the  specialized  anurans  (Fig.  209).  The  adult  and  larval 
urodeles  differ  little  from  each  other,  and  characters  suitable  for 
aquatic  life  are  frequently  found  in  the  adult.  Indeed,  all  stages  of 
suitability  for  land  occur,  from  the  terrestrial  salamanders,  such  as 
Salamandra  maculosa,  the  European  salamander,  which  is  viviparous, 
to  the  fully  aquatic  forms,  for  instance  Necturus,  the  mud-puppy  of 
North  America.  In  many  of  the  aquatic  animals  there  is  a  tendency  to 
retain  in  the  adult  characters  usually  found  in  larvae.  This  process  of 
paedomorphosis  has  developed  to  various  extents,  and  independently 
in  several  groups.  Thus  the  giant  salamander  Megalobatrachus,  5!  ft 
in  length,  in  China  and  Japan,  has  no  eyelids,  but  loses  its  gills  in 
the  adult.  In  Cryptobranchus,  the  hell  bender  of  the  United  States, 
the  spiracle  remains  open  and  is  used  for  the  outlet  of  water  during 
respiration. 

Amphiuma,  also  from  the  southern  U.S.A.,  is  a  very  elongate  form, 
with  absurdly  small  legs,  no  eyelids,  and  four  branchial  arches.  In 


xiii.  6  MODERN  AMPHIBIA  365 

the  still  more  modified  forms,  such  as  Necturus,  external  gills  are 
present  and  the  lung  is  so  reduced  that  the  animals  can  live  walking 
along  the  bottom.  Proteus  from  European  caves  is  a  blind  urodele 
with  external  gills  and  no  pigment.  Siren  shows  almost  entirely  larval 
characteristics  and  has  no  hind  limbs. 

The  more  typical  terrestrial  newts  are  of  several  sorts.  In  North 
America  the  common  genus  Amby stoma  (usually  written  Amblystoma) 
has  eleven  species,  many  adapted  to  special  habits,  including  A.  mexi- 
canum,  in  which  some  races  become  mature  without  metamorphosis, 
because  of  lack  of  iodine  in  the  water,  whereas  others,  the  axolotls  of 
Mexico,  are  genetically  neotenous. 

The  common  British  newt  Triturus  vulgaris  is  a  typical  example  of 
the  more  definitely  terrestrial  urodeles,  though  it  is  not  able  to  live  in 
very  dry  situations.  However,  the  limbs  support  much  of  the  weight 
of  the  body,  and  their  soles  are  applied  to  the  ground  and  turned 
forwards.  The  tail  shows  various  degrees  of  reduction  to  a  circular 
organ,  but  in  the  breeding-season,  when  both  sexes  return  to  the 
water,  it  develops  a  large  fin,  especially  in  the  male.  The  common 
newts  of  America  form  a  distinct  family,  including  Plethodon  and 
many  specialized  forms,  such  as  the  blind  Typhlomolge,  inhabiting  the 
waters  of  caves. 

6.  Frogs  and  Toads.  Subclass  Anura 

Among  the  frogs  and  toads  are  very  many  suited  for  special  modes 
of  life,  and  it  must  again  be  emphasized  that  this  is  far  from  being  a 
static  and  precariously  surviving  group.  We  have  already  mentioned 
the  frog  Ascaphns,  which  lives  in  mountain  streams  in  the  north-west 
of  the  United  States  and  has  reduced  lungs,  showing  a  combination 
of  specialized  and  primitive  features.  Internal  fertilization  is  assured 
by  a  penis-like  extension  of  the  cloaca.  In  this  genus  and  the  New 
Zealand  Leiopelma  (Fig.  210)  there  are  several  primitive  features, 
including  tail  muscles  (absent  in  all  other  anurans),  amphicoelous 
vertebrae,  free  ribs,  abdominal  ribs,  and  persistent  posterior  cardinal 
veins. 

In  Alytesy  the  midwife  toad  of  Europe,  the  male  carries  the  eggs 
wrapped  round  the  legs.  Pipa  is  a  related  and  still  more  specialized 
aquatic  frog  from  South  America;  it  has  no  tongue,  and,  curiously 
enough,  has  developed  an  elaborate  arrangement  by  which  the  young 
are  carried  in  pits  on  the  back.  Xenopus  of  Africa  is  related  to  Pipa, 
but  without  the  habit  of  carrying  its  young  (Fig.  210). 

The  bufonid  toads  are  among  the  most  successful  of  all  amphibian 


366  AMPHIBIA  xm.  6- 

groups  and  are  more  fully  adapted  than  most  for  a  terrestrial  life,  but 
return  nearly  always  to  the  water  to  breed.  Bufo  itself  is  found  in 
almost  all  possible  parts  except  in  Australia  and  Madagascar;  related 
genera,  many  of  them  with  special  features,  are  found  all  over  the 
world.  Curiously  enough  only  one  genus,  Nectophrynoides  from  East 
Africa,  is  viviparous,  the  young  being  in  that  case  provided  with  a 
long  vascular  tail,  by  means  of  which  they  maintain  contact  with  the 
wall  of  the  'uterus',  even  though  embedded  in  a  mass  of  embryos. 

Hyla  and  other  tree-frogs,  very  widely  distributed,  are  similar  to 
the  bufonids  but  have  pads  on  the  toes  by  which  they  climb,  and 
many  other  adaptations  to  arboreal  life.  Gastrotheca  (=  Nototrema), 
the  marsupial  frog,  is  a  genus  in  which  the  young  develop  in  a  sac  on 
the  back  of  the  female,  this  sac  being  in  one  species  protected  by 
special  calcareous  plates.  Rana  and  its  allies,  the  true  frogs,  are  also 
cosmopolitan.  A  number  of  frogs  related  to  Rana  have  taken  to  a  tree- 
living  habit,  developing  pads  on  the  toes.  Polypedates  is  a  widespread 
genus  and  there  are  several  others,  each  independently  derived  from 
ranids.  This  is  therefore  a  striking  illustration  of  parallel  evolution — 
the  hylid  tree-frogs  having  arisen  from  bufonids  and  probably  several 
sorts  of  polypedatids  from  ranids. 

Burrowing  with  the  legs  has  also  been  evolved  several  times  by 
anurans.  In  Breviceps  (Fig.  210),  which  digs  for  ants,  there  is  a  large 
snout,  as  in  other  anteaters. 

7.  Subclass  Apoda  (=  Gymnophiona  =  Caecilia) 

These  (such  as  Ichthyophis)  are  burrowing,  limbless  creatures  living 
like  earthworms,  in  the  tropics.  They  show  several  interesting  primi- 
tive features,  including  the  retention  of  small  scales  in  the  skin.  They 
are  specialized,  however,  in  having  a  very  short  tail  and  some  features 
suited  to  their  terrestrial  life,  such  as  copulatory  organs.  The  animals 
are  blind,  the  place  of  the  eyes  being  taken  by  special  sensory  ten- 
tacles. The  eggs  are  large  and  yolky  and  cleavage  is  meroblastic;  they 
are  laid  on  land  and  the  embryos  develop  around  the  yolk  sac,  but 
often  have  long,  plumed  gills.  Vivipary  is  common,  including  in  the 
aquatic  form  Typhlonectes. 

8.  Adaptive  radiation  and  parallel  evolution  in  modern  Amphibia 

Even  this  superficial  study  of  the  250  genera  and  about  2,000  species 
of  modern  amphibians  shows  that  the  features  we  have  already 
recognized  in  fish  evolution  are  found  also  in  evolution  on  land.  It  is 
difficult  in  a  short  time  to  gain  an  impression  of  the  very  great  variety 


xiii.  9  AMPHIBIAN  EVOLUTION  367 

that  is  characteristic  of  any  group  of  animals  when  closely  studied. 
Besides  the  main  types  that  can  be  distinguished,  countless  lesser 
variations  will  be  found,  and  one  realizes  that  the  characteristics  of  the 
populations  are  still  today  in  process  of  continual  and  perhaps  rapid 
change.  Anyone  trying  to  discover  the  relationships  of  the  various 
derivatives  of  ranids  or  bufonids  must  be  impressed  by  the  presence 
of  series  of  parallel  lines  of  development,  so  that  it  is  impossible  to 
disentangle  the  relationships.  Evolution  viewed  at  close  quarters  by 
the  student  of  abundant  modern  animals  looks  very  different  from 
the  simple  picture  seen  by  the  lucky  collector  of  a  few  rare  fossils, 
who  can  arrange  his  types  in  genealogical  trees  and  is  apt  to  forget  that 
they  represent  only  an  infinitesimally  small  sample  of  abundant  and 
varied  populations. 

We  can  perhaps  find  certain  tendencies  in  the  modern  amphibian 
populations  that  are  similar  to  the  tendencies  of  the  fossil  series.  Many 
return  to  the  water,  especially  among  the  urodeles.  Others  become 
more  fully  terrestrial,  either  by  climbing  trees  or  by  burrowing  into 
the  earth.  Both  these  habits  have  been  independently  adopted  many 
times  by  recently  evolved  lines  and,  no  doubt,  still  more  often  in  the 
past  by  creatures  that  have  died  out,  leaving  no  trace. 

9.  Can  Amphibia  be  said  to  be  higher  animals  than  fishes? 

It  is  not  easy  to  decide  whether  there  is  a  clear  sense  in  which 
amphibians  can  be  said  to  have  advanced  over  their  fish  ancestors. 
They  have  moved  from  the  water  into  environments  that  are  in  a 
sense  less  suitable  for  life.  In  order  to  maintain  a  watery  system,  such 
as  a  frog  or  toad,  outside  the  water,  various  special  structures  and 
methods  of  behaviour  have  been  evolved.  The  presence  of  such 
additional  systems  can  be  said  to  add  complexity  to  the  organization. 
It  is  difficult  to  make  a  count  of  the  number  of  'parts'  involved  in  the 
organization  of  any  animal.  Amphibia  possess  many  special  devices, 
for  instance,  for  respiration  without  loss  of  moisture,  for  control  of 
water  intake  and  water  loss,  for  return  to  water  to  breed,  and  so  on. 
Even  without  making  a  proper  quantitative  computation  it  seems 
reasonable  to  say  that  these  add  up  to  make  an  organization  more 
complicated  than  that  of  a  fish.  The  integration  of  the  action  of  so 
many  parts  requires  an  elaborate  nervous  system,  and  there  is  evi- 
dently some  connexion  between  the  increased  size  and  importance  of 
the  nervous  system  and  the  development  of  this  more  complicated 
organization  that  enables  life  to  continue  in  a  different  environment. 

Considering  the  matter  in  this  way  it  is  hardly  sensible  to  ask  the 


368  AMPHIBIA  xm.  9 

question  'Are  the  amphibians  more  efficient  than  the  fishes?',  the 
work  that  they  do  in  maintaining  life  is  so  different  that  a  comparison 
of  'efficiency'  is  fallacious.  One  method  of  assessing  living  efficiency 
might  be  to  judge  each  animal  organization  by  the  extent  to  which  it 
maintains  its  constancy — by  its  power  of  homeostasis.  Data  about  the 
fluctuations  of  the  internal  environment  are  so  scanty  among  lower 
vertebrates  that  we  cannot  proceed  very  far  on  these  lines.  It  is 
probable  that  the  blood  of  fishes  shows  greater  fluctuations,  for 
instance  in  osmotic  pressure  or  lactic  acid  content,  than  does  that  of 
amphibians,  such  fluctuations  being  perhaps  even  an  advantage  in 
allowing  life  in  waters  of  differing  salinity.  In  fact,  to  say  that  the 
whole  mechanism  of  homeostasis  becomes  more  complicated  in  land 
animals  is  only  to  say  over  again  that  they  are  'higher'  because  they 
have  more  special  work  to  do  to  maintain  themselves  in  a  difficult 
environment.  Almost  every  part  of  the  body  shows  signs  of  this  greater 
complexity;  the  central  nervous  system  becomes  larger,  the  autonomic 
nervous  system  develops  more  elaborate  control  of  the  viscera.  The 
endocrine  glands  become  more  numerous  and  differentiated,  the 
muscular  system  shows  more  distinct  parts,  enabling  the  animal  to 
act  in  new  ways. 

However  difficult  such  comparisons  may  be  it  is  hardly  possible 
to  deny  them  some  validity.  Amphibian  organization  differs  from 
that  of  fishes  and  may  be  said  to  be  'higher'  in  the  sense  that  it  is  more 
elaborate  and  allows  life  in  conditions  that  the  fish  organization 
cannot  tolerate. 


XIV 

LIFE  ON  I  AND:  THE  REPTILES 

1 .  Classification 

Class.  Reptilia 
Subclass  i.  Anapsida 

Order  i.  *Cotylosauria.  Carboniferous-Trias 

*Seymouria;  *Captorhimis;  *Diadectes 
Order  2.  Chelonia.  Permian-Recent 

*Eunotosaurus;     *Triassochelys;     Chelys;     Emys;     Chelone; 

Testudo 

Subclass  2.  *Synaptosauria 

Order  1.  *Protorosauria.  Permian-Trias 

*Araeoscelis;  *  Tanystropheus 
Order  2.  *Sauropterygia.  Trias-Cretaceous 

*Lariosaurus;  *PHosaurus;  *Plesiosaurus;  *Placodus 

Subclass  3.  #Ichthyopterygia 

Order  1.  *Ichthyosauria.  Trias-Cretaceous 
*Mixosaurus;  *  Ichthyosaurus 

Subclass  4.  Lepidosauria 

Order  1.  *Eosuchia.  Permian-Eocene 

*  Yoimgina;  *Prolacerta 
Order  2.  Rhynchocephalia.  Trias-Recent 

*Homoesaurus;  * Rhynchosaurus ;  Sphenodon  (=  Hatteria) 
Order  3.  Squamata.  Trias-Recent 

Suborder  1.  Lacertilia  (=  Sauria).  Trias-Recent 
Infraorder  1.  Gekkota.  Mainly  Recent 

Gecko 
Infraorder  2.  Iguania.  Cretaceous-Recent 
Iguana;  Anolis;  Phrynosoma;  Draco;  Lyriocephahis ;  Agama; 

Chamaeleo 
Infraorder  3.  Scincomorpha.  Eocene-Recent 
Lacerta;  Scincus;  Amphisbaena 
Infraorder  4.  Anguimorpha.  Cretaceous-Recent 
*Dolichosaurus;  * Aigialosaurus ;  *Tylosaurus;  Varanus;  Lan- 
thanotus;  Atwuis 


37° 


REPTILES  xiv.  i- 


1.   Classification  {cont.) 

Suborder  2.  Ophidia  (=  Serpentes).  Cretaceous-Recent 
*Palaeophis;  Python;  Natrix;  Naja;  Vipera 

Subclass  5.  Archosauria 

Order  1.  *Pseudosuchia  (=  *Thecodontia).  Trias 

*Enparkeria;  *Saltoposuchns 
Order  2.  *Phytosauria.  Trias 

*Phytosaurus;  *Mystriosuchus 
Order  3.  Crocodilia.  Trias-Recent 

*Protosuchus;  Crocodilus;  Alligator;  Caiman;  Gavialis 
Order  4.  *Saurischia.  Trias-Cretaceous 
Suborder  1.  *Theropoda 

*Compsog?iathus;     *Ornitholestes;     *  Allosaurns ;     *Tyranno- 
saurus;  * Strnthiomimus 
Suborder  2.  *Sauropoda 
*Apatosaurus  (=  *Brontosaurus);  *Diplodocus;  *Yaleosaurus; 
*Plateosanrus;  Brachiosaurus 
Order  5.  *Ornithischia.  Trias-Cretaceous 
Suborder  1.  *Ornithopoda 

*Camptosaurus;  *Iguanodon;  *Hadrosaurus 
Suborder  2.  #Stegosauria 

*  Stegosaurns 
Suborder  3.  *Ankylosauria 

* Ankylosaurus ;  *Nodosanrus 
Suborder  4.  *Ceratopsia 

*  Triceratops 

Order  6.  *Pterosauria.  Jurassic-Cretaceous 
*Rhamphorhynchns ;  *Pteranodon 

Subclass  6.  *Synapsida.  Carboniferous-Permian 

Order  1.  #Pelycosauria  (=  #Theromorpha) 

*  Varanosaurus;  *Edaphosaurus;  *Dimetrodon 
Order  2.  *Therapsida.  Permian-Jurassic 

*Scym?iognathus;   *Cyiiognathus;   *Bauria;   *Dromatherium; 
* Dicynodon 
Order  3.  *Mesosauria  (—  Proganosauria).  Permian 
*Mesosaurus 


xiv.  2  (370 

2.  Reptilia 

Towards  the  end  of  the  Devonian  period,  say  350  million  years 
ago,  the  vertebrate  organization  produced  a  population  of  amphibian 
creatures  and  from  this  has  been  derived  not  only  various  modern 
groups  classed  as  amphibia  but  also  the  more  fully  terrestrial  popula- 
tions that  do  not  need  to  breed  in  water — the  Amniota.  Since  that 
time  many  divergent  lines  have  evolved  from  this  stock,  including  the 
birds  and  the  mammals,  and  it  is  evident,  therefore,  that  it  is  likely  to 
be  difficult  to  specify  what  is  meant  by  a  reptile,  as  distinct  from  an 
amphibian  or  a  bird  or  mammal.  The  term  does  not  define  a  single 
vertical  line  of  development  or  branch  of  an  evolutionary  tree,  but 
is  rather  a  horizontal  division,  marking  a  band  on  the  evolutionary 
bush,  specifying  a  level  of  organization  beyond  that  of  an  amphibian 
but  before  that  of  either  bird  or  mammal.  Attempts  have  been  made 
to  divide  the  reptiles  vertically  into  sauropsidan  (bird-like)  and 
theropsidan  (mammal-like)  lines,  but  such  a  division,  although  it  has 
some  foundation,  obscures  the  fact  that  their  bush-like  evolutionary 
radiation  has  produced  not  two  but  many  types. 

The  existing  reptiles  belong  to  four  out  of  the  dozen  or  more  main 
lines  that  have  existed.  The  most  successful  modern  forms  are  placed 
in  the  order  Squamata,  the  lizards  and  snakes,  the  latter  being  of 
relatively  recent  appearance  in  their  present  state.  Secondly,  the 
tuatara,  Sphenodon,  of  New  Zealand  is  a  relic  surviving  with  little 
change  from  the  Triassic  beginnings  of  this  group.  Thirdly,  the 
crocodiles  are  an  older  offshoot  from  the  stock  from  which  the  modern 
birds  were  derived.  Finally  the  tortoises  and  turtles  (Chelonia)  have 
retained  in  some  respects  the  organization  of  still  earlier  times, 
perhaps  through  the  special  protection  of  their  shells.  Though  they 
are  much  modified  in  some  ways,  they  still  show  us  several  character- 
istics of  the  earliest  Permian  reptiles. 

These  four  modern  types  are  all  that  remain  of  the  reptiles  that 
flourished  throughout  the  Mesozoic,  culminating  in  the  giant  dino- 
saurs of  the  Jurassic  and  Cretaceous.  Evidently  a  profound  change 
affected  the  population  of  the  world,  including  the  sea,  between  the  end 
of  the  Cretaceous  and  the  Eocene.  This  change  will  be  discussed 
further  in  Chapter  XXI,  but  we  must  briefly  discuss  here  the  possible 
relation  of  the  decline  of  the  reptile  populations  to  the  rise  of  their 
descendants,  the  birds  and  mammals.  It  can  hardly  have  been  only 
the  more  efficient  organization  due  to  the  warm  blood  that  gave 
these  their  opportunity,  for  there  were  forms  in  the  Trias  so  similar 


372  REPTILES  xiv.  z- 

to  mammals  in  their  skeletons  that  we  may  reasonably  (though 
not  certainly)  suppose  them  to  have  been  warm-blooded.  There  were 
birds  with  feathers  in  the  Jurassic,  and  it  is  probable  that  they  also 
already  had  warm  blood.  However,  as  a  working  hypothesis,  we  may 
suppose  that  the  climate,  which  had  been  suitable  for  reptiles  in  the 
Mesozoic,  became  less  so  in  the  early  Tertiary,  and  the  most  obvious 
suggestion  is  that  colder  conditions  developed  all  over  the  earth's 
surface.  The  modern  reptiles  for  the  most  part  live  in  the  temperate 
and  tropical  zones,  indeed  they  flourish  only  in  the  latter.  However,  it 
must  be  remembered  that  climate  fluctuates  continually  (p.  13);  it  is 
dangerous  to  make  generalizations  about  conditions  over  such  long 
periods  as  the  Cretaceous. 

3.  The  organization  of  reptiles 

The  organization  we  call  reptilian  is,  generally  speaking,  suitable  for 
life  in  warm  countries,  though  two  species,  the  common  lizard 
(Lacerta  vivipara)  and  the  adder  ( Vipera  berus),  are  found  as  far  north 
as  the  Arctic  Circle.  No  doubt  the  distribution  of  reptiles  is  limited 
largely  by  the  fact  that  they  cannot  maintain  a  temperature  above  that 
of  the  surroundings  by  production  of  heat  from  within.  The  wide- 
spread idea  that  reptiles  have  no  means  of  regulating  their  body 
temperature,  however,  has  been  overemphasized.  Bogert  and  his 
collaborators  in  the  U.S.A.  have  shown  that  in  the  wild  (though  not 
as  a  rule  under  laboratory  conditions)  reptiles  are  often  able  by  suitable 
behaviour  to  maintain  their  body  temperatures  at  a  remarkably  high 
and  constant  level  throughout  much  of  the  day,  by  varying  their 
exposure  to  the  available  sources  of  heat.  When  they  get  cold  they 
bask  in  the  sun  or  rest  on  warm  rocks;  when  they  get  too  hot  they 
shelter  under  vegetation  or  in  holes.  In  some  species,  too,  colour 
change  plays  a  part  in  temperature  control,  the  animals  becoming 
darker  or  lighter  in  colour,  according  to  whether  heat  absorption  or 
reflection  is  the  appropriate  response. 

It  has  also  been  shown  that  each  species  of  reptile  has  an  optimum 
range  of  temperature,  below  which  the  animals  become  inactive  and 
above  which  they  quickly  die.  In  some  desert  lizards  the  upper  limit  is 
above  400  C.  The  range  tends,  as  one  would  expect,  to  be  higher  in 
diurnal  than  nocturnal  forms,  and  is  in  general  higher  in  lizards  than 
it  is  in  snakes  or  alligators. 

The  reptilian  method  of  temperature  control  differs  essentially 
from  that  of  mammals  in  that  it  depends  on  the  availability  of  external 
sources  of  heat  such  as  the  sun,  rather  than  on  the  ability  to  conserve 


xiv.  5  SKIN  OF  REPTILES  373 

or  lose  heat  generated  within  the  body.  For  this  reason  reptiles  are 
sometimes  termed  'ectothermic'  and  mammals  'endothermic'.  These 
terms  are  perhaps  preferable  to  'poikilothermic'  (having  a  variable 
temperature)  and  'homoiothermic'  (having  a  constant  temperature) 
which  are  in  more  general  use. 

The  ectothermic  method  of  temperature  control  presupposes  some 
sensitive  mechanism  for  registering  slight  changes  in  the  temperature 
of  the  surroundings.  There  is  evidence  that  the  pineal  complex  is  the 
receptor  and  that  the  hypothalamus  may  be  involved  in  thermal 
homeostasis. 

It  remains  true  to  say,  however,  that  no  reptile  can  retain  an  inde- 
pendent body  temperature  for  a  long  period.  For  this  reason,  reptiles 
living  in  temperate  climes  must  hibernate  during  the  winter,  while  in 
warm  countries  some,  conversely,  aestivate  during  the  hottest  months. 

4.  Skin  of  reptiles 

The  skin  is  characteristically  dry;  unlike  the  skin  of  amphibians  and 
mammals  it  contains  few  or  no  glands.  The  Malphigian  layer  of  the 
epidermis  produces  the  horny  scales,  which  are  periodically  shed  in 
flakes,  or,  as  in  snakes,  cast  as  a  single  slough.  Beneath  the  horny 
scales  many  reptiles  (some  lizards,  crocodiles,  some  dinosaurs)  develop 
bony  plates  in  the  dermis  (called  osteoderms).  These  may  be  re- 
stricted to  the  head,  where  they  lie  superficial  to  the  skull  bones,  or 
may  cover  most  of  the  body.  The  tortoise's  shell  contains  both  horny 
(epidermal)  and  bony  (dermal)  components  (p.  394).  The  horny 
scales  are  often  modified  to  form  crests,  spines  and  other  appendages. 

Many  reptiles,  particularly  lizards  and  snakes,  have  bold  and 
elaborate  colour  patterns.  These  may  play  a  part  in  concealment 
(though  they  often  seem  conspicuous  in  captive  specimens  away  from 
their  normal  terrain).  In  some  forms,  especially  lizards,  there  are 
marked  colour  differences  between  the  sexes  (see  p.  407).  The  well- 
known  phenomenon  of  colour  change,  which  is  much  more  marked 
in  certain  lizards  than  in  any  other  known  reptiles,  is  discussed  on 
p.  410. 

5.  Posture,  locomotion,  and  skeleton 

The  elongated  body  and  small  laterally  projecting  legs  of  many 
reptiles  recall  those  of  a  urodele,  and  the  method  of  locomotion  is  in 
general  similar  in  the  two  groups.  Many  retain  the  primitive  five  digits 
in  both  hand  and  foot.  With  the  similarity  of  movement  goes  a  general 
similarity  in  plan  of  the  skeleton:  there  are,  however,  certain  most 


374  REPTILES  xiv.  5 

significant  features,  characteristic  of  the  reptiles.  The  head  is  carried 
off  the  ground,  on  a  well-developed  neck.  The  two  first  cervical 
vertebrae  are  modified  to  form  the  atlas  and  axis.  The  atlas  is  a  ring 
of  bone  without  centrum,  but  with  a  facet  in  front  for  the  occipital 
condyle  and  one  behind  for  the  odontoid  process,  a  peg  attached  to 
the  front  of  the  axis  but  derived  in  development  from  the  centrum  of 
the  atlas  segment. 


-sc. 


Fig.  212.  Shoulder  girdle  and  sternum  of  a  lizard  (Iguana). 

el.   clavicle;    cor.   coracoid;   gl.   glenoid;   int.cl.   interclavicle;  pr.   procoracoid 
process;  sc.  scapula;  st.r.  sternal  rib;  St.  sternum.  (From  Reynolds,  after  Parker.) 


The  vertebrae  articulate  with  each  other  by  a  system  of  interlocking 
processes  much  more  elaborate  than  that  found  in  fish-like  vertebrates 
and  presumably  serving  to  allow  the  column  to  carry  weight.  As  a 
rule,  each  centrum  is  concave  in  front,  covering  the  convex  hind  end 
of  the  vertebra  next  to  it,  a  condition  known  as  procoelous.  In  aquatic 
vertebrates  the  centra  articulate  by  flat  surfaces  and  this  condition  was 
retained  in  the  amphicoelous  vertebrae  of  many  primitive  reptiles. 
Besides  this  articulation  of  the  centra  the  vertebrae  are  also  united  by 
the  zygapophyses,  facets  on  the  neural  arches,  so  arranged  that  the 
upwardly  facing  surfaces  of  the  anterior  zygapophyses  slide  over  the 
down-facing  surfaces  of  the  posterior  zygapophyses,  an  arrangement 
that  is  found  throughout  the  amniotes. 

Ribs  are  well  developed  in  the  middle  or  trunk  region;  each  arti- 
culates with  the  body  of  the  vertebra  by  a  single  capitular  facet. 


xiv.  5  GIRDLES  AND  LIMBS  375 

The  vertebrae  can  often  be  divided  into  four  sets.  The  cervical 
vertebrae,  which  are  very  variable  in  number,  have  short  ribs,  not 
reaching  the  sternum.  Sternal  ribs  occur  in  the  thoraco-lumbar  seg- 
ments (Fig.  212).  The  ribs  of  the  two  sacral  vertebrae  are  short  and 
broad  and  articulate  with  the  ilia.  The  numerous  caudal  vertebrae 
show  reduction  of  all  parts,  especially  towards  the  tip  of  the  tail.  The 
chevron  bones  are  ossicles  attached  to  the  caudal  centra  and  represent- 
ing the  reduced  intercentra. 

The  girdles  and  limbs  (Figs.  183-6  and  212)  show  the  same  general 
structural  and  functional  features  as  those  of  amphibia.  The  limbs 
form  the  main  locomotor  system,  the  metachronal  contraction  of  the 
myotomes  playing  a  lesser  part  than  in  urodele  amphibians.  The 
humerus  and  femur  are  normally  held  in  such  a  position  that  their 
outer  ends  lie  higher  than  the  inner,  that  is  to  say,  in  a  position  of 
abduction.  The  radius  and  ulna  and  tibia  and  fibula  proceed  down- 
wards towards  the  ground  (at  right  angles  to  the  proximal  bones)  and 
the  hand  and  foot  are  turned  outwards  at  right  angles,  to  rest  on  the 
ground.  The  main  muscles  thus  draw  the  humerus  and  femur  back- 
wards and  forwards  as  well  as  downwards,  and  the  ventral  regions  of 
the  girdles  are  large  and  flattened  to  receive  these  muscles;  in  mam- 
mals, with  a  different  system  of  progression,  the  more  dorsal  parts 
of  the  girdles  have  become  developed. 

The  pectoral  girdle  (Figs.  183,  212)  consists  of  a  dorsal  scapula  and 
a  large  ventral  coracoid,  which  may  be  fenestrated.  Distinct  pro-  and 
post-coracoid  elements  are  probably  only  found  in  the  extinct  mam- 
mal-like reptiles.  The  dermal  components  are  represented  by  the 
paired  clavicles  and  median  interclavicle.  A  cleithrum  is  found  in  a 
few  very  primitive  forms. 

In  the  pelvic  girdle  (Fig.  184)  the  usual  dorsal  ilium,  anterior  pubis, 
and  posterior  ischium  are  found,  the  last  two  meeting  their  fellows  in 
midline  symphysis. 

The  characteristic  modifications  of  the  reptilian  skull  are  discussed 
on  p.  391.  The  general  plan  is  similar  to  that  of  primitive  amphibians, 
but  in  all  except  the  most  primitive  reptiles  there  is  a  development  of 
holes  (fossae)  in  the  temporal  region  to  provide  space  for  the  bulging 
temporal  muscles.  The  skull  roof  is  in  some  respects  more  primitive 
than  that  in  modern  amphibians  (Figs.  213  and  214).  It  is  made  up  of  a 
large  series  of  dermal  bones,  including  the  nasals,  prefrontals,  frontals, 
supra-orbitals,  and  parietals.  The  side  of  the  skull  is  usually  less  com- 
plete, composed  of  the  tooth-bearing  premaxillaand  maxilla,  lacrymal, 
jugal,    post-orbital,    squamosal,    supratemporal   and   quadrate.    The 


376  REPTILES  xiv.  5 

naming  of  some  of  the  smaller  bones  round  the  orbit  and  above 
the  quadrate  is  a  matter  of  controversy. 

The  margins  of  the  palate  are  formed  by  flanges  of  the  premaxillae 


Fig.  213.  Skull  and  lower  jaw  of  Lacerta. 

A,  dorsal  view;  13,  ventral  view;  C,  from  left  side;  D,  right  half  of  lower  jaw  from  inner 
side,  showing  the  pleurodont  arrangement  of  the  teeth.  E.P.  ectopterygoid;  Ep.P.  epiptery- 
goid;  F,  Fr.  frontal ;  jug.  jugal;  Lac.  lachrymal;  Max.  maxillary;  N,  Na.  nasal;  N,  in  B, 
inner  narial  opening;  Pal.  palatine;  Par.  parietal;  Pmx.  premaxillary ;  Pr.f.  prefrontal; 
Pt.f.  post-orbital;  Pt.f2.  post-frontal;  Ptg.  pterygoid;  Q.  quadrate;  S.ang.  supra-angular; 
Sq.  squamosal;   '.  'o.  vomer.  The  regions  of  persistent  cartilage  are  not  shown  in  detail. 

(After  Gadow.) 

and  maxillae  and  the  small  ectopterygoids.  The  internal  nostrils 
usually  lie  forwards  between  the  maxillae,  vomers,  and  palatines. 
More  posteriorly  the  floor  of  the  skull  is  made  up  mainly  by  pterygoid 
bones  and  the  parasphenoid,  which  is  partly  fused  with  the  lower 
surface  of  the  basisphenoid.  Occipital  bones  surround  the  foramen 
magnum  and  make  up  the  single  occipital  condyle,  which  in  some 


xiv.  5  SKULL  377 

forms  is  indented  to  form  three  partly  distinet  lobes.  In  many  reptiles 
there  is  an  epipterygoid  bone  on  either  side  of  the  brain-case  behind 
the  orbits;  this  is  regarded  as  an  ossification  in  the  ascending  process 
of  the  palato-quadrate.  The  lower  jaw  usually  consists  of  six  bones, 
the  articular  forming  the  joint  with  the  quadrate,  and  the  dentary 
carrying  teeth. 

The  anterior  part  of  the  chondrocranium,  surrounding  the  front  of 
the  brain,  and  the  nasal  capsule,  remain  more  or  less  unossified,  and 


Fig.  214.  Diagram  of  the  skull  of  lizard  to  show  temporal  fossa. 

a.  articular;  an.  angular;  bo.  basioccipital;  bs.  basisphenoid;  c.  coronoid;  d.  dentary;  da. 
dermal  articular;  do.  dermal  supraoccipital;  ept.  ectopterygoid;  eo.  exoccipital ;  fr.  frontal; 
j.  jugal;  /.  lachrymal;  mx.  maxilla;  n.  nostril;  na.  nasal;  o.  orbit;  op.  opisthotic;  pa.  parietal; 
pal.  palatine;  pv.  prevomcr;  pm.  premaxilla;  po.  post-orbital;  pof.  post-frontal;  pr.  pro-otic 
pra.  prearticular;  pr}.  prefrontal  ;ps.  presphenoid;  pt.  pterygoid;  q.  quadrate;  qj.  quadrato- 
jugal;  sa.  surangular;  sf.  upper  temporal  fossa  (this  is  shown  diagrammatically,  as  it  occurs 
in  many  lizards;  in  Lacerta  it  is  largely  covered  by  an  extension  of  the  post-frontal — see 
Fig.   213);  so.  supraoccipital;  sp.  splenial;  sq.  squamosal;  St.  supratemporal;  v.  vomer. 

(From  Goodrich.) 

in  places  may  be  membranous.  There  may,  however,  be  small  ossified 
orbitosphenoids  and  farther  back  pleuro-  or  laterosphenoids,  which 
develop  in  the  pila  pro-otica  uniting  the  orbital  cartilage  with  the 
otic  capsules.  Between  the  eyes  there  is  in  most  reptiles  a  thin  sheet 
of  cartilage  known  as  the  interorbital  septum,  which  may  be  partly 
ossified  by  small  presphenoid  elements.  The  posterior  part  of  the 
chondrocranium  ossifies  to  form  the  following  bones;  occipital  com- 
plex, basisphenoid,  and  the  ossifications  in  the  otic  capsule  (pro-otic, 
opisthotic,  &c). 

In  many  reptiles  the  upper  jaw  and  front  part  of  the  skull  can  move 
to  some  extent  in  relation  to  the  occipital  region  and  cranial  base, 
such  movement  being  termed  kinesis  (p.  405).  This  is  often  associated 
with  mobility  of  the  quadrate,  as  in  lizards,  snakes,  and  certain  dino- 
saurs. Kinesis  helps  to  widen  the  gape  and  may  provide  a  shock- 
absorbing  effect  when  the  jaws  are  snapped  together. 

The  postmandibular  visceral  arches  play  no  part  in  jaw  support  but 
are  incorporated  into  the  ear  and  hyoid  apparatus.  There  is  a  rod-like 


378  REPTILES  xiv.  5- 

columella  auris  with  a  small  cartilaginous  element  (extra-columella) 
at  its  outer  end.  The  columellar  system  usually  conducts  vibrations 
from  the  tympanum,  lying  behind  the  quadrate,  to  the  fenestra  ovalis 
and  inner  ear.  In  some  forms,  e.g.  snakes,  however,  the  tympanum  is 
absent  and  the  outer  end  of  the  columella  is  applied  to  the  quadrate. 
These  animals  may  be  deaf  to  air-borne  sounds  but  sensitive  to 
ground  vibrations,  transmitted  through  the  bones  of  the  jaw. 

The  hyoid  apparatus  consists  of  a  basal  plate,  which  projects  into 
the  tongue,  and  three  pairs  of  ascending  horns.  These  represent  the 
remains  of  the  hyoid  and  branchial  arches. 

6.  Feeding  and  digestion 

Food  is  seized  either  by  the  teeth  or,  in  some  specialized  lizards 
such  as  the  chameleon,  with  the  elongated  tongue.  The  teeth  are 
situated  along  the  edges  of  the  jaws  and  often  also  on  some  of  the 
bones  of  the  palate.  Typically,  they  are  all  of  the  same  conical  shape, 
but  may  be  slightly  serrated,  or  modified  to  form  crushing  plates, 
poison  fangs,  and  other  devices.  As  a  rule,  tooth  succession  is  con- 
tinuous throughout  life,  though  exceptions  to  this  are  found  among 
the  lizards.  Salivary  glands  are  well  developed  in  some  forms;  in 
snakes  and  one  genus  of  lizards  (Heloderma)  some  of  them  are  modified 
to  form  poison-glands.  The  tongue  is  very  variable,  being  hardly 
movable  in  some  reptiles  (e.g.  crocodiles)  but  long,  forked,  and  highly 
mobile  in  others  (e.g.  snakes). 

Digestion  proper  begins  in  the  stomach.  The  alimentary  canal  is 
built  on  the  typical  vertebrate  plan,  with  a  tubular  stomach,  rather 
short  small  intestine,  and  wider  large  intestine,  leading  to  a  short 
caecum. 

There  is  a  well-marked  cloacal  chamber  in  all  reptiles,  subdivided 
into  a  coprodaeum  for  the  faeces,  and  a  urodaeum  for  the  products  of 
the  kidneys  and  genital  organs.  These  two  chambers  open  into  a  final 
common  proctodaeum,  closed  by  a  cloacal  sphincter.  This  division 
of  the  cloaca  is  associated  with  the  necessity  for  the  retention  of  water, 
the  cloacal  chambers  serving  for  water  reabsorption  from  both  the 
faeces  and  urinary  excreta  (p.  380). 

7.  Respiration,  circulation,  and  excretion 

The  typical  method  of  respiration  is  a  backward  movement  of  the 
ribs,  produced  by  the  muscles  attached  to  them.  There  is  no  complete 
separation  of  the  thorax  from  the  abdomen,  but  a  partial  diaphragm 
may  be  present.  The  glottis  is  a  slit  at  the  back  of  the  mouth  and  leads 


xiv.  7  CIRCULATION  379 

into  a  larynx  with  supporting  cricoid  and  arytenoid  cartilages.  Many 
reptiles  are  able  to  produce  small  sounds,  but  the  voice-box  is  less 
developed  than  in  either  amphibia  or  birds. 

The  lungs  are  sacs  whose  walls  are  folded  into  ridges,  separating 
a  number  of  chambers  or  bronchioles.  The  hinder  part  of  the  lung  is 


car.  int. 


car.  ex t. 


Fig.  215.  Diagram  of  heart  and  arteries  of  Lacerta. 

car.ext.  external  carotid;  car. int.  internal  carotid;  c.car.  common  carotid;  coel.  coeliac  artery; 

d.a.  dorsal  aorta;  d.B.  ductus  Botalli  (arteriosus);  d.car.  ductus  caroticus;  l.aur.  left  auricle; 

p.a.  pulmonary  artery;  p.v.  pulmonary  vein;  r.aur.  right  auricle;  scl.  subclavian  artery; 

sept,  interventricular  septum;  v.c.  eaval  veins.  (From  Ihle,  after  Goodrich.} 

nearly  smooth  and  in  some  lizards,  as  in  birds,  it  becomes  developed 
into  characteristic  air  sacs.  The  tendency  is  for  the  more  anterior  por- 
tion of  the  lung  to  become  the  effective  vascular  and  respiratory  region, 
allowing  the  air-stream  to  be  drawn  across  it  at  both  inspiration  and 
expiration. 

The  circulation  (Fig.  215)  of  lizards  shows  a  partial  separation  of 
venous  and  arterial  blood;  there  are  two  auricles,  but  only  one  ven- 
tricle, this  being  partly  divided  by  a  septum  into  right  and  left  sides. 
Three  arterial  trunks  arise  directly  from  the  ventricle,  these  being  the 


380  REPTILES  xiv.  7- 

right  and  left  aortae,  and  the  pulmonary  trunk.  The  opening  of  the 
latter  lies  opposite  the  right  side  of  the  ventricle  and  receives  pre- 
dominantly venous  blood.  The  left  systemic  arch  opens  opposite  to 
the  incomplete  ventricular  septum  and  receives  mixed  blood,  whereas 
the  right  systemic  arch  opens  from  the  left  side  of  the  ventricle  and 
carries  almost  pure  arterial  blood.  The  carotid  arteries  of  both  sides 
arise  from  the  right  systemic  arch.  This  'classical'  view  of  the  cir- 
culation of  the  blood  in  the  reptilian  heart  has  recently  been  confirmed 
by  the  radiographical  studies  of  Foxon  and  his  colleagues  on  the  green 
lizard.  Variations  may  be  found,  however,  in  different  species. 

The  venous  system  is  based  on  the  same  plan  as  that  of  the  frog, 
with  pelvic  veins  receiving  blood  from  the  tail  and  hind  legs  and 
returning  it  to  the  heart  through  either  an  anterior  abdominal  vein 
or  renal  portals,  and  the  inferior  vena  cava. 

In  the  urinogenital  system  is  seen  another  feature  characteristic  of 
amniotes,  the  development  of  a  posterior  region,  the  metanephros, 
concerned  solely  with  excretion,  leaving  the  mesonephric  (Wolffian) 
duct  to  function  as  the  vas  deferens  in  the  male.  There  is  sometimes 
an  endodermal  (allantoic)  bladder. 

The  waste  nitrogen  is  largely  excreted  as  uric  acid  and  this  allows 
the  reabsorption  of  much  of  the  water  in  the  urodaeum,  with  precipita- 
tion of  the  organic  matter  as  a  chalky  white  mass  of  urates.  The 
advantage  of  this  method  of  excretion  is  that  it  allows  for  a  greater 
economy  of  water  than  would  be  possible  if  the  end  product  was  the 
more  soluble  urea.  There  is,  however,  some  variation  in  the  mode  of 
excretion  among  certain  members  of  the  group  and  this  may  depend 
on  the  manner  of  life  of  the  species  and  the  necessity  for  water  con- 
servation. Thus  among  Chelonia  the  more  aquatic  forms  (Emys)  pro- 
duce considerable  amounts  of  ammonia  and  urea,  but  relatively  little 
uric  acid,  whereas  the  last  is  the  main  excretory  product  of  the  fully 
terrestrial  types,  such  as  the  Grecian  tortoise  (Testudo  gracca),  which 
can  live  under  almost  desert  conditions. 

8.  Reproduction  of  reptiles 

Fertilization  has  become  internal,  and  in  all  modern  reptiles  except 
Sphenodon  special  organs  of  copulation  derived  from  the  cloacal  wall 
are  developed  in  the  male.  In  crocodiles  and  tortoises  there  is  a  single 
median  penis,  but  in  lizards  and  snakes  there  are  a  pair  of  these  struc- 
tures, though  only  one  is  inserted  at  a  time.  The  mechanism  of  erec- 
tion involves  both  muscular  action  and  vascular  engorgement.  The 
sperms  pass  from  the  vasa  deferentia  into  the  urodaeum,  and  after 


xiv.  8  REPRODUCTION  381 

traversing  this  region  they  are  carried  into  a  groove  along  each  penis. 
In  snakes  the  sperms  may  survive  within  the  female  for  long  periods, 
and  instances  are  known  of  isolated  individuals  laying  fertile  eggs 
after  months,  sometimes  even  years,  in  captivity. 

Some  of  the  most  serious  difficulties  in  the  colonization  of  the  land 
are  concerned  with  reproduction,  and  these  problems  have  been 
largely  solved  in  the  reptiles,  allowing  the  animals  to  reproduce  with- 
out returning,  as  many  amphibia  must  do,  to  the  water. 

The  eggs  of  oviparous  reptiles  are  always  laid  on  land.  They  there- 
fore require  a  firm  physical  support  and  protection  against  desic- 
cation, as  well  as  an  adequate  supply  of  food  and  special  means  of 
gaseous  exchange  and  storage  of  waste  products.  These  requirements 
are  met  by  the  development  of  a  shell,  secreted  by  the  walls  of  the 
oviduct  and  often  hardened  by  lime  impregnation,  by  the  formation 
of  special  embryonic  membranes,  the  amnion  and  allantois,  and  by 
the  provision  of  a  large  quantity  of  yolk  enclosed  in  a  bag,  the  yolk- 
sac.  The  method  of  embryonic  cleavage  is  affected  by  the  great 
amount  of  yolk,  and  as  in  birds  is  only  partial.  An  albumen  or  egg- 
white  layer  is  present  in  the  eggs  of  crocodiles  and  tortoises  and  pre- 
sumably serves  as  a  reservoir  of  water;  in  the  eggs  of  lizards  and 
snakes,  however,  the  albuminous  layer  is  poorly  developed  or  absent. 

The  formation  of  the  amnion  and  allantois  is  one  of  the  most 
remarkable  features  of  the  development  of  reptiles ;  it  is  characteristic 
of  all  higher  vertebrates,  distinguishing  them  sharply  from  the  lower 
types.  The  amnion  is  developed  from  folds,  which  cover  the  embryo 
and  enclose  a  sac  filled  with  fluid,  where  development  can  proceed 
in  the  absence  of  the  pond  that  was  necessary  for  the  earlier  verte- 
brates. The  allantois  began  as  an  enlarged  bladder,  serving  for  the 
reception  of  the  waste  products  during  the  life  within  the  shell.  Coming 
close  to  the  surface  and  fusing  with  the  chorion,  it  then  becomes  the 
vehicle  for  the  transport  of  oxygen  to  the  embryo. 

The  evolution  of  eggs  and  embryonic  membranes  of  the  kind  de- 
scribed must  have  been  an  event  of  critical  importance  in  tetrapod 
history.  Romer  has  suggested  that  this  advance  took  place  under 
climatic  conditions  of  alternate  drought  and  flooding,  so  that  eggs 
laid  above  the  high-water  mark  had  the  best  chance  of  survival.  Since 
many  of  the  early  reptiles  are  thought  to  have  spent  much  of  their 
time  in  the  water,  it  is  possible  that  the  egg  preceded  the  adult  in  the 
process  of  adaptation  to  terrestrial  life. 

Most  reptiles  lay  their  eggs,  but  in  many  lizards  and  snakes  these 
are  retained  within  the  oviduct  until  the  young  are  ready  or  nearly 


382  REPTILES  xiv.  8- 

ready  to  hatch  (e.g.  Lacerta  vivipara,  Anguis  fragilis,  Vipera  berus). 
This  method  of  reproduction  is  termed  ovoviviparous ;  in  forms  that 
practise  it  the  eggshell  is  reduced  to  a  thin  membrane  or  is  lost 
altogether.  In  some  species  (e.g.  certain  skinks  and  other  lizards, 
sea-snakes)  a  placenta  is  developed  from  the  chorio-allantois  or  the 
yolk-sac  or  both.  The  placenta  may,  as  in  Lacerta  vivipara,  serve  only 
for  the  transfer  of  water  and  gases,  but  in  the  more  advanced  forms  it 
probably  provides  a  means  of  transport  for  food  (supplementing  the 
yolk)  and  excretory  products. 

Young  born  alive  are  perhaps  less  susceptible  to  the  hazards  of 
weather  than  those  left  to  hatch  in  the  sun  or  among  rotting  vegeta- 
tion, and  it  is  interesting  that  most,  if  not  all,  of  the  few  reptiles  that 
live  in  places  where  the  climate  is  really  severe  are  ovoviviparous. 

Young  reptiles  have  special  devices  to  assist  their  escape  from  the 
egg.  In  Sphenodon,  Chelonia,  and  Crocodilia,  as  in  birds,  there  is  a 
horny  epidermal  egg-breaker  on  top  of  the  snout  tip,  called  the  egg- 
caruncle.  In  the  Squamata,  a  true  egg-tooth,  projecting  from  the  front 
of  the  upper  jaw,  has  the  same  function.  The  egg-tooth  is  present, 
though  sometimes  rudimentary,  in  ovoviviparous  forms. 

Some  reptiles  make  a  simple  nest  but  the  group  is  not  noted  for 
maternal  care,  usually  abandoning  their  new-laid  eggs  or  newborn 
young.  There  are,  however,  some  exceptions  to  this;  female  pythons 
and  certain  other  snakes  and  lizards  brood  their  eggs,  and  female 
alligators  are  said  to  guard  their  nests. 

Many  reptiles  exhibit  well-marked  courtship  and  display  pheno- 
mena during  the  breeding-season,  the  males  fighting  and  displaying, 
either  to  intimidate  each  other  or  to  evoke  a  suitable  response  from 
the  female.  This  is  particularly  striking  in  certain  lizards,  notably 
those  of  the  iguanid  and  agamid  groups,  where  the  males  are  often 
brightly  coloured  and  may  be  adorned  with  crests  and  distensible  fans 
under  the  throat.  In  these  lizards  bobbing  movements  of  the  head 
and  front  part  of  the  body,  often  accompanied  by  colour  change,  form 
an  important  part  of  the  display.  As  in  birds,  courtship  may  be  associ- 
ated with  territory,  a  male  holding  an  area  of  ground  on  which  females, 
but  not  rival  males,  are  tolerated.  Breeding  behaviour  and  sexual 
coloration  are,  of  course,  under  the  control  of  the  endocrine  system, 
especially  the  anterior  pituitary  and  the  gonads,  and  may  be  modified 
by  castration.  The  onset  of  the  breeding  season  is  also  influenced  by 
climatic  conditions;  most  reptiles  breed  only  once  or  twice  a  year, 
but  a  few  species  living  in  warm  stable  climates  may  breed  at  intervals 
nearly  all  the  year  round. 


XIV. 9  (383) 

9.  Nervous  system  and  receptors  of  reptiles 

All  the  modifications  of  structure  that  fit  the  reptiles  for  life  on 
land  would  be  useless  without  the  development  of  appropriate  be- 
haviour. This  in  turn  depends  on  suitable  structure  and  function  of 


cer.h. 


cLf.b. 


<?**  warn 


hypoth. 


Fig.  216.  Three  views  of  the  brain  of  a  lizard. 

cereb.  cerebellum;  cer.h.  cerebral  hemispheres;  hypoph.  hypophysis; 

hypoth.  hypothalamus;  olf.b.  olfactory  bulb;  tect.opt.  tectum  opticum; 

II— XII,  cranial  nerves.  (After  Frederikse.) 

the  nervous  system.  The  brain  accordingly  shows  some  interesting 
developments.  The  cerebral  hemispheres  are  relatively  larger  in 
reptiles  than  in  amphibians  (Fig.  216).  The  increased  bulk  lies  mainly 
in  the  basal  parts  of  the  hemisphere  (the  corpus  striatum),  as  in  birds 
(Fig.  217).  The  roof  (pallium)  is  little  developed  and  lacks  the  elabor- 
ate cortical  differentiation  found  in  mammals.  The  thalamus  is  well 
developed  and  receives  connexions  from  the  optic  tracts,  which  no 
longer  run  mainly  to  the  midbrain.  There  are  also  many  fibres  from  the 
thalamus  to  the  cerebral  hemispheres.  This,  together  with  the  other 
features  mentioned,  may  be  evidence  for  the  transfer  of  many  nervous 


384  REPTILES  xiv.  9 

functions  from  lower  levels  of  the  nervous  system  to  the  cerebral 
hemispheres,  a  process  that  has  been  carried  much  farther  in  mam- 
mals. In  most  respects,  however,  the  brains  of  modern  reptiles  are 
more  like  those  of  birds  than  of  mammals. 

The  behaviour  of  reptiles,  despite  the  elaborate  courtship  of  some 
forms,  remains  of  a  relatively  stereotyped  character.  The  eyes  are 
usually  the  main  exteroceptive  sense-organs  and  are  usually  provided 


co it  dors. 


cort.  hipp. 
sutc  Llm 


cert  Cat 


.ircfnstr 


■palaeostr 


Fig.  217.  Transverse  section  through  forebrain  of  Lacerta. 

archistr.  archistriatum  (upper  part  of  corpus  striatum);  cort. dors,  dorsal  cortex;  cort. hipp. 
medial  (hippocampal)  cortex;  cort.lat.  lateral  (pyriform)  cortex;  palaeostr.  paleostriatum 
(basal  part  of  corpus  striatum);  sept,  septum;  sidclim.  sulcus  limitans.  (After  de  Lange 

and  Kappers.) 

with  movable  eyelids,  including  a  third  eyelid  or  nictitating  membrane. 
The  lacrymal  and  Harderian  glands  provide  secretions  that  keep  the 
surface  of  the  cornea  moist.  The  eye  is  supported  in  most  reptiles  by 
a  scleral  cartilage  and  a  ring  of  bony  scleral  plates.  Accommodation  is 
produced  by  the  striated  ciliary  muscles,  so  arranged  that  they  cause 
the  ciliary  process  to  squeeze  the  lens,  making  its  anterior  surface  more 
rounded  (Fig.  218).  In  many  reptiles  the  retina  possesses  both  rods 
and  cones,  the  latter  predominating  in  diurnal  types. 

The  pineal  complex  is  often  well  developed,  and  in  Sphenodon  and 
many  lizards  a  'pineal'  or  parietal  eye  is  present  with  lens-like  and 
retina-like  components.  In  such  forms  there  is  a  pineal  foramen  in 
the  parietal  bone  near  the  fronto-parietal  suture.  Similar  foramina 
are  found  in  many  fossil  reptiles,  especially  the  more  primitive  types. 
The  function  of  the  reptilian  pineal  is  still  rather  obscure,  but  there 
is  evidence  that  in  lizards  it  registers  solar  radiations,  and,  perhaps 
by  the  secretion  of  hormones,  influences  the  animal's  thermoregula- 


xiv.  g 


RECEPTOR  ORGANS 


385 


tory  behaviour  in  exposing  itself  to  sunlight.  It  is  also  possible  that  the 
pineal  complex  plays  some  part  in  the  control  of  reproduction. 

In  the  majority  of  reptiles  the  olfactory  region  of  the  nose  is  quite 
well  developed,  but,  except  in  crocodiles,  there  is  only  a  single  nasal 
concha.  The  organ  of  Jacobson  (vomero-nasal  organ),  a  specialized 
and  sometimes  separate  region  of  the  nose,  innervated  by  a  separate 


THIS   SIDE, 
RELAXATION 


THIS   SIDE, 
ACCOMMODATION 


Fig.  218.  Diagram  to  show  the  mechanism  of  accommodation  in  the  eye  of 

reptiles. 

ap.  annular  pad  of  lens;  bm.  Brucke's  muscle;  bp.  base  plate  of  ciliary  body;  c.  cornea;  ch. 
chorioid;  cp.  ciliary  process;  1.  iris;  lb.  lens  body;  ot.  ora  terminalis;  pi.  pectinate  ligament; 
s.s.  sclera;  sc.  scleral  cartilage;  scs.  sclerocorneal  sulcus;  so.  scleral  ossicle;  sr.  sensory  retina; 
tbm.  tendon  of  Brucke's  muscle  (continuous  with  inner  layers  of  corneal  substantia  propria); 
//.  tenacular  ligament;  z.  zonule.  (From  Walls,  The  Vertebrate  Eye.) 


branch  of  the  olfactory  nerve,  is  present  in  turtles,  Sphenodon,  and 
Squamata.  In  the  latter  it  is  usually  very  highly  developed  (see 
p.  405). 

The  tympanum  when  present  lies  at  the  back  of  the  jaws,  sunk  a 
little  below  the  surface.  The  range  of  response  to  sound  waves  is  not 
known  in  lizards,  but  the  ears  of  certain  tortoises  are  very  sensitive 
to  sound  over  a  narrow  range  of  about  no  cycles  per  second;  appar- 
ently there  is  some  resonating  mechanism,  perhaps  the  columella  auris, 
which  vibrates  at  this  frequency.  Generally  speaking,  the  sense  of 
hearing  is  best  developed  among  reptiles  in  the  Crocodilia  and  certain 
lizards. 


XV 

EVOLUTION  OF  THE  REPTILES 

1.  The  earliest  reptile  populations,  Anapsida 

The  organization  of  a  reptile  is  well  suited  to  maintain  life  on  land. 
Many  features  show  a  considerable  advance  in  this  respect  over  the 
amphibia,  for  example,  the  dryness  of  the  skin,  the  method  of  repro- 
duction, and  the  devices  for  economizing  in  the  use  of  water.  The 
immense  radiation  of  the  reptiles  into  every  sort  of  land  habitat  during 
the  Mesozoic  period  shows  the  efficiency  of  these  mechanisms,  which 
were  probably  present,  at  least  in  imperfect  form,  in  the  earliest  Car- 
boniferous and  Permian  offshoots  from  the  ancestral  Stegocephali 

(P-  356). 

We  have  sufficient  knowledge  to  be  able  to  trace  the  early  stages  of 
reptilian  evolution  with  considerable  certainty.  An  animal  known  as 
*Seymonriai  found  in  the  lower  Permian  of  Texas  (perhaps  250  million 
years  old),  is  of  critical  importance  in  our  understanding  of  reptile 
origins  (Figs.  219,  220).  It  was  a  lizard-like  creature,  about  2  ft  long, 
probably  living  on  insects  and  perhaps  some  larger  animals.  Its  charac- 
teristics are  so  exactly  intermediate  between  those  of  amphibians  and 
reptiles  that  it  is  not  possible  to  place  it  definitely  with  either  group ; 
many  zoologists  class  it  with  the  Amphibia.  This  intermediacy  is 
shown  in  almost  every  structure  of  the  body  and  is  often  a  subtle 
matter  of  the  shape  or  size  of  the  parts.  Although  a  list  of  anatomical 
features  is  apt  to  give  an  unreal  picture  of  any  living  organization  it  is 
the  only  method  available  to  us  in  the  absence  of  any  more  ingenious 
calculus,  and  we  may  therefore  give  first  some  of  the  characteristically 
reptilian  features  of  *Seymouria.  (1)  The  neural  arches  of  the  verte- 
brae were  convex  dorsally  so  that  they  have  a  'swollen'  appearance 
which  is  also  seen  in  early  reptiles;  (2)  a  canal  for  the  lachrymal  duct 
was  present;  (3)  the  occipital  condyle  was  single;  (4)  the  pectoral 
girdle  possessed  a  long  interclavicle;  (5)  the  pelvic  girdle  was  attached 
to  the  vertebral  column  by  two  sacral  vertebrae ;  (6)  the  blade  of  the 
ilium  was  expanded  for  the  attachment  of  the  large  muscles  used  in 
walking;  (7)  there  were  five  digits  in  the  hand  instead  of  four  as  in 
many  labyrinthodonts  and  in  living  amphibia;  (8)  the  phalangeal 
formula  was  2:3:4:5:3  or  4,  approximating  to  the  reptilian,  rather 
than  the  usual  labyrinthodont  condition,  in  which  the  phalanges  are 
less  numerous. 


Fig.  219.  Skeleton  of  Seymouria.  Actual  length  20  in. 
(From  Williston,  Osteology  of  the  Reptiles,  Harvard  University  Press.) 


Fig.  220.  Skull  and  pectoral  girdle  of  Seymouria  (after  Williston). 

c.  coracoid;  cl.  clavicle;  id.  interclaviclc;  j.  jugal;  /.  lachrymal;  m. 
maxilla;  po.  post-orbital;  qj.  quadratojugal;  sc.  scapula;  sq.  squamosal. 


xv.  i  SEYMOURIA  389 

On  the  other  hand,  there  are  many  considerations  that  would  lead 
one  to  classify  this  fossil  as  an  amphibian.  (1)  The  skull  bones  were 
conspicuously  pitted  or  'sculptured' ;  (2)  the  pattern  of  the  bones  was 
very  like  that  of  early  amphibians ;  for  instance  an  intertemporal  bone 
was  present;  (3)  the  teeth  still  showed  a  labyrinthine  structure  and 
the  palatal  teeth  were  distributed  in  pairs  as  in  many  labyrinthodonts ; 
(4)  the  structure  of  the  otic  notch,  across  which  the  tympanic  mem- 
brane was  stretched,  and  certain  other  features  of  the  auditory  appara- 
tus suggest  amphibian  rather  than  reptilian  affinities;  (5)  other  fossils 
are  known  which,  though  clearly  related  to  *Seymouria,  show  trends 
such  as  flattening  and  reduced  ossification  of  the  skull  that  are  charac- 
teristic of  late  labyrinthodonts  rather  than  early  reptiles;  (6)  perhaps 
the  most  significant  point  of  all  is  that  some  adult  specimens  show 
signs  of  the  presence  of  lateral  line  canals.  Since  the  structure  of  the 
skeleton  of  *Seymouria  suggests  terrestrial  habits,  the  presence  of 
these  canals  suggests  that  the  animal  may  have  passed  through  an 
aquatic  larval  stage  in  which  they  were  functional.  Hence  the  case  for 
classifying  * Seymouria  as  an  amphibian  becomes  very  strong. 

It  must  be  added  that  * Seymouria  may  show  other  features  charac- 
teristic of  both  early  amphibians  and  primitive  reptiles.  The  neck, 
for  example,  was  short,  with  the  pectoral  girdle  lying  close  behind  the 
skull.  There  was  little  differentiation  between  the  vertebrae,  all  those 
in  the  cervical  region  bore  ribs.  The  ribs  were  double-headed,  a 
feature  that  has  been  retained  by  some  more  advanced  reptiles. 

*Seymouria  itself  existed  too  late  to  have  been  a  direct  ancestor  of 
the  more  advanced  groups  of  reptiles,  since  some  of  the  latter  had 
already  appeared  by  the  early  Permian.  Whether  it  should  actually 
be  classified  as  an  amphibian  or  a  reptile  is  uncertain;  in  Romer's 
recent  Osteology  of  the  Reptiles  it  and  its  allies  are  placed  in  the  latter 
group.  It  may  be  regarded  as  a  most  interesting  link  between  the 
labyrinthodonts  and  the  primitive  stem-reptiles  (Cotylosauria),  from 
which  soon  arose  a  great  variety  of  descendants,  which  came  to 
dominate  not  only  the  land  but  also  the  sea  and  air  throughout  the 
subsequent  Mesozoic  period. 

The  cotylosaurs  must  have  existed  throughout  the  later  part  of  the 
Carboniferous,  though  they  did  not  become  prominent  before  the 
beginning  of  the  Permian.  From  the  Red  Beds  of  Texas  we  have, 
besides  ^Seymouria,  forms  such  as  *Limnoscclis,  *Captorhinusy  and 
*Labidosaurus,  all  with  the  rather  high  narrow  skulls  and  pointed  nose 
characteristic  of  reptiles  rather  than  amphibians,  but  differing  from 
the  latter  in  the  absence  of  the  otic  notch.  This  and  other  features 


39Q 


REPTILES 


suggest  that  these  animals  were  related  to  the  early  mammal-like  rep- 
tiles (p.  539).  *Limnoscelis,  however,  was  a  particularly  primitive  form, 
and  may  have  been  partly  aquatic  in  habits. 

Other  rather  later  cotylosaurs  were  larger  forms,  such  as  *Diadectes 
(Fig.  222)  and  *Bradysaunis  and  other  'pareiasaurs'  from  the  Permian 
and  Triassic  of  Europe,  Africa,  and  America.  These  were  up  to  10  ft 


Limnosce'is 


Captorhinus 


Labidosaurus 


Diadectes 


Triassochelys 


Bradysaurus 
Fig.  222.  Skulls  of  various  early  reptiles.  After  Romer  and  various  authors. 

long  and  probably  carried  the  body  well  off  the  ground,  the  limbs 
being  held  underneath  the  body  and  showing  some  reduction  of 
specialized  digits.  This,  together  with  the  large  size  of  the  animals  and 
their  specialized  teeth,  suggest  that  they  may  have  been  one  of  the 
first  of  the  many  types  of  large  herbivore  to  appear  on  the  land  (see 
p.  429).  In  some  of  them  the  skull  developed  grotesque  protective 
protuberances,  a  feature  recalling  similar  later  developments  in 
reptiles  (Ceratopsia,  p.  426)  and  mammals  (amblypods,  p.  717).  A 
characteristic  structural  feature  was  the  presence  of  an  otic  notch  low 
down  on  the  side  of  the  skull.  This  distinguishes  the  pareiasaurs  from 
the  more  mammal-like  forms  and  suggests  affinity  with  some  of  the 
other  reptilian  descendants  of  the  early  cotylosaurs.  These  cotylo- 
saurs multiplied  and  became  very  diversified  throughout  the  45  million 


XV.  2 


CLASSIFICATION 


39i 


years  of  the  Permian  period,  by  which  time  the  main  reptilian  types 
had  appeared.  The  individual  reptilian  orders  nearly  all  became 
established  during  the  subsequent  45  million  years  of  the  Trias  and 
most  of  them  reached  their  maximum  development  in  the  Jurassic 
and  Cretaceous. 

2.  Classification  of  reptiles 

Since  our  knowledge  of  reptiles  depends  mainly  on  fossil  remains 
it  is  convenient  to  classify  them  by  means  of  the  skull  into  four  great 


Psrapsida 


Diapsida 


Fig.  223.  Diagrams  of  reptilian  skulls  to  show  arrangement  of  the  temporal  openings. 

Anapsida,  no  opening.  Synapsida,  a  lower  opening,  with  post-orbital  and  squamosal 

meeting  above  it.  Parapsida,  an  upper  opening  with  post-orbital  and  squamosal 

meeting  below  it.  Diapsida,  two  openings,  separated  by  a  bar. 

.jugal;  pa.  parietal;  po.  post-orbital;  sq.  squamosal.  (From  Romer,  Vertebrate  Paleontology, 
Chicago  University  Press.) 

groups  (Fig.  223).  Such  a  classification  is  in  some  ways  artificial,  but 
it  serves  to  indicate  in  a  broad  way  the  main  lines  of  evolution  within 
the  class. 

In  the  cotylosaurs  the  dermal  bones  of  the  temporal  region  of  the 
skull  presented  an  unbroken  surface  and  there  were  no  temporal 
fossae.  There  were  therefore  no  arches  or  'apses'  of  bone  in  the  tem- 
poral region.  Such  forms  are  placed  in  the  subclass  Anapsida.  The 
jaw  muscles  took  origin  from  the  deep  surface  of  the  temporal  side 
wall,  between  it  and  the  brain-case,  and  they  passed  down  through 
holes  in  the  palate  to  be  inserted  on  the  lower  jaw.  This  represents  the 
most  primitive  condition  found  in  reptiles,  and  resembles  that  in  the 
early  amphibians.  It  is  still  seen  today,  though  often  in  a  modified 
form,  in  the  Chelonia,  which  are  hence  placed  in  the  anapsid  sub- 
class. 

In  more  advanced  groups  of  reptiles  fossae  bounded  by  bony 
arches  appear  in  the  temple  region,  enabling  the  jaw  muscles  to  extend 


392  REPTILES  xv.  2- 

through  them  on  to  the  outer  surface  of  the  skull,  an  arrangement 
that  increases  their  mechanical  advantage. 

In  many  reptiles,  two  such  fossae  appeared,  the  condition  being 
termed  diapsid.  This  is  seen  in  the  subclasses  Lepidosauria  and  Archo- 
sauria,  perhaps  the  most  successful  groups  of  reptiles.  In  lepidosaurs 
of  the  order  Squamata,  however,  the  lower  temporal  arch  is  always 
incomplete,  having  no  quadrato-jugal  bone  and  the  jugal  separated 
from  the  squamosal.  In  some  lizards  and  in  snakes  the  upper  arch 
is  also  lost. 

In  other  groups  only  a  single  fossa  and  arch  is  present.  When  this 
is  situated  high  on  the  skull  the  condition  is  known  as  parapsid. 
Parapsid  skulls  are  seen  in  the  subclasses  Ichthyopterygia  (icthyo- 
saurs)  and  Synaptosauria  (plesiosaurs,  &c).  Formerly,  these  two  sub- 
classes were  placed  together  in  a  group  known  as  the  Parapsida,  as  is 
shown  in  Fig.  221,  but  this  classification  is  now  regarded  as  artificial, 
since  the  ichthyosaurs  and  sauropterygians  are  not  closely  related; 
in  fact  a  careful  analysis  shows  that  the  bony  relationships  of  their 
single  temporal  fossae  were  rather  different. 

In  the  remaining  subclass,  the  Synapsida,  there  is  also  a  single 
fossa,  but  in  the  earlier  forms  at  least  it  is  placed  low  down,  and  is 
bounded  below  by  the  jugal  and  squamosal.  The  term  synapsid, 
meaning  'fused  arch',  is  actually  a  misnomer,  due  to  the  fact  that 
early  workers  believed,  wrongly,  that  the  single  arch  was  formed  from 
the  fusion  of  the  two  seen  in  diapsids. 

The  synapsids  comprise  the  mammal-like  reptiles,  but  in  the  later 
members  of  the  group,  such  as  *Cynognathas,  and  in  their  descendants 
the  mammals,  the  temporal  fossa  has  greatly  enlarged,  and  has  lost 
its  primitive  relationships. 

3.  Order  1.  Chelonia 

Shut  away  in  their  boxes  the  tortoises  and  turtles  have  retained 
some  of  the  features  of  the  earliest  anapsid  reptiles.  Even  today  they 
are  a  not  unsuccessful  and  quite  varied  and  widespread  group,  with 
more  than  200  species.  These  include  terrestrial  animals,  such  as 
Testudo  graeca,  the  Grecian  tortoise  of  south  Europe,  which  is  her- 
bivorous; the  freshwater  tortoises,  such  as  Chrysemys  and  other 
American  terrapins,  and  Emys  the  European  water-tortoise,  all  of 
which  are  carnivorous.  The  marine  Chelonia,  usually  known  as 
turtles,  are  often  very  large.  Dermochelys,  the  leathery  turtle,  which 
has  no  horny  shell,  is  over  6  ft  long  and  weighs  half  a  ton.  Chelone 
my  das,  the  green  or  edible  turtle,  is  over  3  ft  long. 


xv.  3 


CHELONIANS 


393 


The  characteristic  of  chelonian  organization  is  the  shortening  and 
broadening  of  the  body,  together  with  the  development  of  bony 
plates,  forming  a  box  into  which  the  head  and  limbs  can  be  with- 
drawn. The  total  number  of  segments  is  only  about  8  in  the  neck,  io 
in  the  trunk,  and  a  series  of  reduced  caudals;  the  body  is  therefore 


Fig.  224.  Skeleton  of  turtle  (Chelone). 

carp,  carpus  (note  hook-shaped  5th  metacarpal);  cen.  centrum  of  vertebra;  cor.  coracoid; 
fern,  femur ;fib.  fibula;  h.  humerus;  il.  ilium;  isch.  ischium;  mar.  marginal  plate;  nuch.  nucal 
plate;  pr.  'proscapular'  process  or  acromion;  pub.  pubis;  rad.  radius;  rib,  rib,  partly  fused 
with  costal  shell-plate;  sc.  scapula  (foreshortened);  tib.  tibia;  uhi.  ulna.  (After  Shipley  and 

McBride  and  Reynolds.) 

morphologically  shorter  than  in  any  other  vertebrate  except  the  frog. 
Probably  this  shortening  and  broadening  is  the  result  of  some  quite 
simple  change  in  morphogenesis. 

The  shell  is  usually  considered  to  include  a  dorsal  carapace  and 
ventral  plastron.  Each  of  these  is  made  up  of  inner  plates  of  bone, 
covered  by  separate  outer  plates  of  horny  material,  comparable  to  the 
scales  of  other  reptiles.  The  carapace  includes  five  rows  of  bony  plates, 
namely,  median  neurals,  and  paired  costals  and  marginals  (Fig.  225). 
These  plates  are  ossifications  in  the  dermis,  attached  to  the  vertebrae 


394  REPTILES  xv.  3 

and  ribs,  but  not  actually  formed  from  the  latter.  The  plastron  is 
developed  from  the  expanded  dermal  bones  of  the  pectoral  girdle, 
together  with  dermal  ossifications  comparable  to  the  abdominal  ribs 
found  in  crocodiles  and  other  reptiles.  The  whole  is  covered  in  most 
chelonians  by  rows  of  special  smooth  epidermal  plates  forming  the 
'tortoise  shell'  (Fig.  225).  A  new  and  larger  layer  is  added  to  each  of 
these  plates  each  year,  the  old  one  remaining  above  it,  thus  making  a 
number  of  'growth  rings'  from  which  some  indication  of  the  age  of  the 


Neur.  S. 


Neur.  PL. 


Mar  (j.  S. 


Pect.  S. 


Fig.  225.  Diagram  of  the  arrangement  of  the  shell  of  the  tortoise 

(Testudo).  The  horny  shields  are  shown  only  on  the  left. 

cap.  capitulum  of  rib;  cost.pl.  costal  plate;  cost.s.  costal  shield;  7tiarg.pl.  marginal 

plate;  marg.s.  marginal  shield;  ncur.pl.  neural  plate;  tieur.s.  neural  shield;  pect.s. 

pectoral  shield;  plast.  plastron;  sp.c.  spinal  cord.  (After  Gadow). 

tortoise  can  be  calculated,  though  the  outer  members  often  become 
rubbed  off. 

In  order  to  support  this  box  the  limb  girdles  have  become  much 
modified  and  lie  inside  the  encircling  ribs.  The  pectoral  girdle  has 
three  prongs,  a  scapula  that  meets  the  carapace  dorsally  and  carries  a 
long  'acromial  process'  and  a  backwardly  directed  coracoid,  the  two 
last  being  attached  bv  ligaments  to  the  plastron.  The  ilia  are  attached 
to  two  sacral  vertebrae  and  the  ischia  and  pubis  are  broad.  The  limbs 
are  stout,  but  otherwise  typically  reptilian,  with  five  digits  in  each. 
In  the  marine  turtles  they  are  transformed  into  paddles. 

The  interpretation  of  the  skull  is  still  somewhat  doubtful,  but  it 
seems  not  unlikely  that  the  turtle,  Cheloue,  shows  the  simplest  case, 
namely,  the  original  anapsid  condition  (Fig.  226).  Here  the  roofing  is 
complete,  the  dermal  bones  being  widely  separated  from  the  brain- 
case,  forming  a  tunnel  for  the  jaw  muscles  and  those  producing 
retraction  of  the  neck.  The  tympanum  is  stretched  across  a  sort  of  otic 
notch,  bounded  by  the  squamosal,  quadrato-jugal  and  quadrate,  the 


xv.  3  SKULL  395 

columella  auris  articulating  with  the  latter.  In  other  groups  of  Che- 
Ionia,  however,  the  dermal  roofing  has  been  reduced  or  'emarginated', 
presumably  to  give  still  better  attachment  for  the  jaw  and  neck  muscles 


Chelone 


Trionyx 


Fig.  226.  Skulls  of  Chelone  and  Trionyx.  Lettering  as  Fig.  214,  p.  377. 
(After  Goodrich  from  Parker  and  Haswell,  and  Zittel.) 

(Fig.  226).  It  has  been  argued  that  the  condition  in  Chelone  is  second- 
ary, but  there  is  no  evidence  of  true  temporal  fossae  in  any  chelonian, 
and  since  the  early  form  *Triassochelys  also  had  a  fully  roofed  skull 
there  seems  no  reason  for  denying  that  we  have  here  essentially  an 
anapsid  condition. 

A  peculiarity  of  recent  Chelonia  is  the  entire  absence  of  teeth,  alike 


(396) 


Testudo 


Fig.  227.  Various  chelonians,  not  all  to  same  scale.  (Emys  and  Chelys  after  Gadow, 
Dermochelys  after  Deraniyagala.) 


xv.  3  EGGS  OF  CHELONIA  397 

in  the  herbivorous  and  carnivorous  forms.  The  edges  of  the  jaws  form 
sharp  ridges,  covered  with  a  formidable  horny  beak. 

The  similarity  of  the  soft  parts  of  Chelonia  to  those  of  other 
surviving  reptiles  (which  are  all  diapsids)  suggests  that  the 
general  organization  of  the  group  has  changed  little  since  the  Per- 
mian. The  heart  possesses  a  partly  divided  ventricle  and  there  are  two 
equal  aortic  arches  (Fig.  244).  Respiration  is  modified  by  the  rigidity 
of  the  body  wall;  the  lungs  are  spongy  structures  attached  to  the 
dorsal  surface  of  the  shell,  sometimes  enclosed  in  a  separate  pleural 
cavity  (Testudo).  Breathing  is  mainly  brought  about  by  the  contraction 
of  the  modified  abdominal  muscles,  which  function  in  a  manner 
comparable  with  that  of  the  mammalian  diaphragm,  and  by  means  of 
pumping  movements  of  the  pharynx.  Some  aquatic  forms  {Emys)  also 
respire  by  taking  water  into  special  vascular  sacs,  diverticuli  of  the 
urodaeum.  The  metabolism  of  tortoises  is  slow  and  they  can  remain 
for  long  periods  without  breathing.  In  temperate  climates  all  species 
hibernate  regularly. 

The  kidney  is  metanephric  and  the  nitrogenous  excreta  are  mainly 
uric  acid,  there  being  a  typical  subdivision  of  the  cloaca  and  reabsorp- 
tion  of  water  to  form  a  solid  whitish  excretory  product  (see  p.  380). 
There  is  a  single  copulatory  organ  and  the  eggs  are  whitish,  with  hard 
or  soft  shells.  Like  other  aquatic  reptiles  that  lay  eggs,  turtles  all  come 
ashore  to  breed.  Thus  the  marine  Chelone  breeds  in  the  West  Indies, 
in  the  Straits  of  Malacca,  and  on  the  coast  of  West  Africa;  they  are 
caught  as  they  come  ashore  and  made  into  turtle  soup.  On  the  Amazon 
chelonian  eggs  are  (or  at  least  were)  so  plentiful  that  large  numbers 
were  eaten.  The  eggs  are  usually  carefully  placed  in  holes  made  by 
boring  with  the  tail  and  scooping  with  the  feet  (Emys).  The  traces  of 
the  nest  are  then  covered,  often  with  considerable  success.  Neverthe- 
less Bates  reckoned  that  at  least  48  million  eggs  were  taken  annually 
on  the  upper  Amazon.  The  chief  enemies  of  the  young  are  vultures 
and  alligators,  and  these  were  presumably  the  ultimate  losers  when 
collection  by  man  began,  though  the  numbers  of  turtles  have  also 
decreased  as  a  result  of  the  human  depredations. 

The  proverbial  slowness  of  the  tortoise  is  a  necessary  corollary  of 
its  heavy  armour,  but  the  nervous  organization  and  behaviour  is  more 
complex  than  is  sometimes  supposed.  The  brain  shows  well-developed 
cerebral  hemispheres,  with  not  only  the  basal  regions  but  also  the 
pallium  quite  large.  This  was  therefore  probably  true  also  of  the 
earliest  reptiles,  as  it  is  of  amphibians.  In  the  mammals,  also  derived 
from  cotylosaur  ancestors,  there  has  been  still  further  development  of 


398  REPTILES  xv.  3- 

the  dorsal  regions  of  the  hemispheres  to  form  the  cerebral  cortex, 
whereas  in  the  remaining  reptile  groups,  and  in  the  birds,  the  ventral 
portion  has  become  large,  the  dorsal  thin.  The  eyes  are  probably  the 
chief  receptors  of  chelonians,  but  the  nose  is  also  well  developed  and 
the  animals  are  very  sensitive  to  vibration.  The  tympanum  is  often 
covered  with  ordinary  skin  and  hearing  is  probably  not  acute  (p.  385). 
The  voice  is  also  small. 

The  various  species  show  many  special  habits,  some  of  them  com- 
plicated and  ingenious,  especially  among  the  aquatic  forms  (Fig.  227). 
For  instance,  the  snapping  turtles  (Chelydra)  and  alligator  turtles 
(Macroclemys)  of  North  America  and  Emys  in  Europe  show  con- 
siderable care  and  skill  in  stalking  and  capturing  not  only  fish  but 
also  young  ducks  and  other  birds.  Similarly  the  smaller  turtles,  such 
as  Chrysemys  picta,  the  painted  terrapin,  with  bright  yellow,  black, 
and  red  colours,  feed  not  only  on  insect  larvae,  but  also  on  flies,  which 
they  catch  near  the  water  surface.  Many  observers  have  shown  that 
the  common  Grecian  tortoise  has  a  marked  sense  of  locality,  returning 
to  a  favourite  spot  even  after  hibernation. 

Our  knowledge  of  the  geological  history  of  the  Chelonia  extends 
back  to  the  Trias.  *Triassochclys  (Fig.  222)  was  an  early  turtle,  with 
a  shell  like  that  of  modern  forms,  but  still  possessing  teeth  on  the 
palate.  The  skull  was  anapsid  and  the  pectoral  girdle  contained  inter- 
clavicles,  clavicles,  and  perhaps  cleithra;  these  dermal  bones  were 
already  somewhat  enlarged  and  incorporated  in  the  plastron.  The 
head,  tail,  and  limbs  could  not  be  withdrawn  into  the  shell  and  were 
protected  by  spines.  In  the  later  evolution  of  the  Chelonia  retraction 
of  the  head  became  possible  by  one  of  two  methods.  In  the  suborder 
Pleurodira,  'side-neck  turtles',  the  neck  is  folded  sideways.  The  group 
is  known  from  the  Cretaceous  and  survives  today  in  tropical  Africa 
(Chelys),  South  America,  and  Australia.  The  more  successful  group 
is  the  suborder  Cryptodira,  in  which  the  neck  is  curved  in  a  dorso- 
ventral  plane.  This  type  is  also  known  from  the  Cretaceous  and 
includes  most  of  the  modern  types.  The  aquatic  chelonians  show 
various  modifications  and  it  is  probable  that  several  lines  have  inde- 
pendently returned  to  the  water.  As  a  result  of  this  habit  the  bony 
shell  is  often  reduced,  presumably  in  the  interests  of  lightness  and 
because  of  absence  of  enemies.  This  had  occurred  already  in  *Archelon 
of  the  Cretaceous,  which  is  very  similar  to  the  modern  Chelone. 
Dcrmochclys,  the  leathery  turtle,  has  a  curious  'carapace'  consisting 
only  of  a  mosaic  of  small  bony  plates  beneath  its  leathery  skin, 
and  Trionyx  is  a  freshwater  turtle  with  a  soft  shell  and  no  horny 


xv.  4  SYNAPTOSAURS  399 

plates.  All  of  these  forms  are  best  considered  as  aberrant  crypto- 
dirans. 

We  can  trace  the  history  of  the  Chelonia  back  rather  satisfactorily 
to  the  Triassic,  but  unfortunately  there  is  little  to  show  how  they 
evolved  to  that  stage  from  some  Carboniferous  cotylosaurian  ances- 
tor. * Eunotosaurus  from  the  Permian  of  South  Africa  had  a  small 
number  of  vertebrae,  with  very  broad,  expanded  ribs.  This  perhaps 
suggests  some  affinity  with  Chelonia,  though  in  the  latter  the  ribs 
themselves  are  not  expanded.  There  is  therefore  little  to  tell  us  how, 
when,  or  why  one  of  the  early  reptilian  populations  shortened  its 
bodies  and  covered  them  with  armour  for  protection  against  the 
hazards  of  the  land  they  had  recently  invaded. 

4.  Subclass  *Synaptosauria 

Order  *Protorosauria 

All  the  Synaptosauria  characteristically  possessed  a  single  temporal 
fossa  in  the  upper  or  parapsid  position.  The  earliest  forms  were  small 
terrestrial  lizard-like  creatures  such  as  *Araeoscelis  from  the  lower 
Permian  (Fig.  228).  A  few  more  specialized  forms,  including  the 
remarkable  Triassic  *  T any stropheus  with,  a  long  neck  and  short  body, 
are  known,  but  the  protorosaurs  seem  never  to  have  been  an  impor- 
tant element  of  the  early  reptilian  fauna.  Their  relationships  are  not 
well  understood  but  it  is  possible  that  they  gave  rise  to  the  sauro- 
pterygians.  The  theory  that  the  Squamata  were  derived  from  proto- 
rosaurs by  the  emargination  of  the  lower  temporal  region  is  now  held 
to  be  unlikely. 

Order  *  Saw  o pterygia 

This  was  a  very  successful  line  of  marine  reptiles,  extending  from 
the  Trias  to  the  end  of  the  Cretaceous.  The  earlier  nothosaurs,  such  as 
*Lariosaurus  (Fig.  228)  from  marine  Triassic  deposits,  were  small 
(3  ft  long)  and  had  a  long  neck,  and  limbs  partly  converted  into 
paddles.  The  upper  temporal  fossa  was  enlarged  and  the  nostrils  lay 
rather  far  back,  as  in  many  water  reptiles. 

All  of  these  features  were  further  developed  in  the  plesiosaurs  of 
the  Jurassic  and  Cretaceous,  such  as  *Miiraenosaurns  (Fig.  228).  In 
some  the  neck  became  very  long,  presumably  for  catching  fish;  76  cer- 
vical vertebrae  have  been  recorded.  In  others  the  neck  was  shorter 
and  the  skull  longer.  The  limbs  were  developed  into  huge  paddles, 
the  ventral  portions  of  the  girdles  being  large  for  the  attachment  of 
muscle  masses  inserted  on  the  flattened  humerus  and  femur.  The 


400 


REPTILES 


xv.  4- 


dorsal  portion  of  the  girdles,  so  well  developed  in  terrestrial  reptiles, 
was  here  small:  the  ilium  hardly  articulates  with  the  sacral  verte- 
brae. The  hands  and  feet  were  enlarged  by  increase  in  number  of 
joints  (hyperphalangy),  but  there  was  no  increase  of  digits  (hyper- 


^^ammssk 


-.-E» 


Lariosaurus 


^^^Mmmrn^0^ 


Muraenosaurus 


y 


Ichthyosaurus    \  Jf 

Fig.  228.  Icthyosaurs,  plesiosaurs,  and  their  allies.  (Partly  after  Romer.) 

dactyly)  such  as  is  seen  in  ichthyosaurs.  The  skull  was  as  in  notho- 
saurs,  but  with  the  nostril  still  further  displaced  on  to  the  upper 
surface. 

These  animals  were  numerous  in  Jurassic  and  Cretaceous  seas  and 
some  of  them  reached  50  ft  in  length.  They  were  obviously  fish- 
eaters,  but  little  is  known  of  their  habits.  It  is  not  known  whether  they 
were  viviparous  or  came  ashore  to  lay  eggs.  *Placodus  and  related 


xv.  6  ICHTHYOSAURS  401 

Triassic  forms  were  related  to  the  plesiosaurs  and  were  specialized  for 
mollusc-eating  by  the  development  of  large  grinding  teeth  on  the 
jaws  and  palate. 

5.  Order  *Ichthyopterygia 

These  animals,  found  mainly  in  the  Triassic  and  Jurassic  seas, 
were  even  more  modified  for  aquatic  life  than  the  plesiosaurs  (Fig. 
228).  They  occupied  a  position  comparable  to  that  of  the  dolphins 
and  whales  during  the  Tertiary  period.  The  body  possessed  a  stream- 
lined fish  shape  and  swimming  was  by  lateral  undulatory  movements. 
The  vertebrae  were  amphicoelous  disks  and  there  were  large  dorsal 
and  caudal  fins,  with  the  vertebral  column  apparently  continued  into 
the  lower  lobe  of  the  latter.  The  paired  fins  were  small  and  presumably 
used  as  stabilizing  and  steering  agents.  The  pelvic  girdle  did  not 
articulate  with  the  backbone.  In  the  limbs  the  number  of  digits  was 
often  greater  or  less  than  the  usual  five,  and  there  was  often  hyper- 
phalangy.  Evidently  this  type  of  skeleton  gives  better  support  for  a 
fish-like  paddle  than  does  the  pentadactyl  tetrapod  type  and  it  is 
interesting  to  find  it  evolved  again  in  vertebrate  stocks  that  returned 
to  the  water.  This  seems  in  a  sense  to  be  a  case  of  reversal  of  evolution. 

The  head  was  much  modified  for  aquatic  life,  with  a  very  long 
snout  armed  with  sharp  teeth,  and  nostrils  set  far  back.  The  eyes 
were  large  and  surrounded  by  a  ring  of  sclerotic  bony  plates.  The 
temporal  fossa,  though  in  the  parapsid  position,  had  boundaries 
different  from  that  in  the  synaptosaurians. 

The  Triassic  ichthyosaurs  were  already  greatly  modified  and  we 
have  no  trace  of  the  origin  of  the  group.  Romer  has  suggested  a  pos- 
sible derivation  from  cotylosaurs  related  to  the  ancestors  of  mammal- 
like reptiles.  The  ichthyosaurs  were  more  highly  adapted  to  aquatic 
life  than  any  other  reptiles  known.  They  seem  to  have  been  viviparous, 
since  the  skeletons  of  small  specimens  have  been  found  within  larger 
ones.  Like  the  plesiosaurs  they  developed  a  special  mollusc-eating 
type,  *Omphalosanriis,  in  the  Triassic. 

6.  Subclass  Lepidosauria 

Most  of  the  animals  popularly  considered  as  characteristic  of  the 
period  of  reptilian  dominance  have  a  two-arched  or  diapsid  skull.  This 
condition,  or  some  modification  of  it,  is  found  in  all  the  surviving 
reptiles  except  the  Chelonia,  and  in  the  birds.  Formerly  all  the  two- 
arched  reptiles  were  placed  in  a  single  subclass,  the  Diapsida,  but  it 
is  now  customary  to  divide  them  into  two  subclasses,  the  Lepidosauria, 


402  REPTILES  xv.  6-7 

which  includes  Sphenodon,  the  lizards  and  snakes,  and  the  Archo- 
sauria,  including  the  crocodiles,  dinosaurs,  pterosaurs,  and  the  an- 
cestors of  birds.  It  is  not  known  if  the  archosaurs  were  derived  from 
primitive  lepidosaurs  such  as  *  Yonngina,  or  whether  the  two  groups 
arose  independently  from  cotylosaurian  ancestors. 

Order  *Eosuchia 

The  earliest  lepidosaurs  belong  to  the  order  Eosuchia.  The  best 
known  of  these,  *  Youngina  (Figs.  229  and  230),  was  a  lizard-like 
creature,  found  in  the  Upper  Permian  of  South  Africa,  and  retaining 
many  cotylosaurian  features,  for  instance,  teeth  on  the  palate  and  no 
opening  between  the  bones  of  the  snout  (antorbital  vacuity).  The 
two  fossae  at  the  back  of  the  skull  immediately  show  the  affinity  with 
other  diapsids.  Little  is  known  of  the  post-cranial  skeleton.  The  fifth 
metatarsal  does  not  show  the  hooked  shape  that  is  found  in  other 
diapsids  and  also  in  Chelonia.  It  is  difficult,  however,  to  ascribe  very 
great  weight  to  this  single  point,  as  against  the  general  features  of  the 
skull,  which  indicate  that  *  Youngina  could  have  given  rise  to  the  later 
two-arched  reptiles  and,  by  loss  of  the  lower  margin  of  the  lower 
temporal  fossa,  also  to  the  lizards  and  snakes.  *ProIacerta,  from  the 
Lower  Trias,  shows  how  this  may  have  come  about;  it  is  so  like 
*  Youngina  that  it  is  classed  as  an  eosuchian,  but  there  is  a  gap  in  the 
lower  temporal  arch,  suggesting  that  the  animal  may  have  been  near 
the  ancestry  of  lizards. 

7.  Order  Rhynchocephalia 

Sphenodon  ( =  Hatteria),  the  tuatara  of  New  Zealand,  is  the  oldest 
surviving  lepidosaurian  reptile;  it  still  remains  in  essentially  the 
eosuchian  condition.  Very  similar  Mesozoic  fossils  (e.g.  *Homoeo- 
saurus  from  the  Jurassic)  show  the  continuity  of  the  type  (Fig.  221). 
Among  the  many  primitive  features  that  this  race  has  preserved  un- 
changed for  200  million  years  are  the  two  complete  temporal  fossae 
(Fig.  231),  the  well-developed  pineal  eye  (the  pineal  foramen  is 
marked  in  the  early  diapsid  fossil  skulls),  and  the  amphicoelous  verte- 
brae with  intercentra.  Sphenodon,  alone  of  surviving  reptiles,  has  no 
copulatory  organ.  The  large  wedge-shaped  front  teeth  are  among  the 
few  specialized  characters. 

The  tuatara  was  once  widespread  throughout  New  Zealand  but 
became  much  reduced  and  in  danger  of  extinction.  Recently  rigid 
conservation  measures  seem  to  have  allowed  it  to  recover  in  numbers 
on  some  small  northern  islands.  The  animals  are  up  to  2  feet  long  and 


(4°3) 


Fig.  229.  Diagrams  of  skulls  of  A,  eosuchian,  B, 
pseudosuchian,  showing  the  plan  of  the  diapsid  skull. 
Lettering  as  Fig.  214.  //.  lower  temporal  fossa;  pi.  pre- 
orbital  fossa;  sf.  upper  temporal  fossa.  (From  Goodrich.) 


<U 


J 


Fig  230  Skull  of  Youngina.  Lettering  as  Fig.  214.  (After  Romer,  Vertebrate  Paleontology , 

Chicago  University  Press.) 


4<h  REPTILES  xv.  7- 

are  insectivorous  and  carnivorous.   They  live  in  burrows,  often  in 
association  with  petrels.  The  eggs  take  over  a  year  to  hatch. 

Sphenodon  evidently  shows  us  a  type  that  has  departed  relatively 
little  from  the  condition  of  diapsids  in  the  late  Permian.  Yet  its  appear- 
ance, habits,  and  soft  parts  are  very  like  those  of  lizards,  and  provide 
us  with  evidence  that  these  animals  remain  in  essentials  rather  close 
to  the  original  amniote  populations.  A  few  other  extinct  rhyncho- 


itf.     fr. 


Fig.  231.  Skull  of  Sphenodon.  Lettering  as  Fig.  214.  (After  Romer, 
Vertebrate  Paleontology,  Chicago  University  Press.) 

cephalians  are  known;  these  include  the  rhynchosaurs,  in  which  the 
tip  of  the  upper  jaw  had  a  hooked  beak-like  appearance. 

8.  Order  Squamata 

The  lizards  and  snakes  are  the  most  successful  of  modern  reptiles, 
numbering  between  them  over  5,000  species.  Probably  the  groups 
arose  from  eosuchians  related  to  *Prolacerta.  Such  forms  would  also 
have  been  close  to  the  Rhynchocephalia,  differing  from  them,  however, 
in  a  tendency  to  lose  the  lower  temporal  arch  and  to  develop  a  movable 
quadrate. 

It  has  now  been  shown  that  the  lizards  are  a  more  ancient  group 
than  was  formerly  supposed,  and  had  appeared  by  the  end  of  the 
Triassic.  Furthermore,  some  of  the  early  forms  were  already  con- 
siderably specialized.  Our  knowledge  of  the  early  lacertilian  radiation 
is  still  incomplete,  however,  and  none  of  the  existing  lizard  families 
are  known  much  before  the  Cretaceous.  The  earliest  undoubted  snake 
occurs  in  the  upper  Cretaceous  and  the  group  does  not  seem  to  have 
become  abundant  until  the  Oligocene. 


xv.  8  LIZARDS  AND  SNAKES  405 

Although  typical  lizards  preserve  a  number  of  primitive  reptilian 
features,  the  Squamata  as  a  group  show  several  interesting  specializa- 
tions that  are  absent  in  Sphenodon,  and  to  which  their  success  may 
be  partly  attributed.  In  the  majority  of  forms,  especially  in  the  snakes, 
the  skull  is  highly  kinetic,  having  a  freely  movable  quadrate,  which 
imparts  its  motion  to  the  bones  of  the  upper  jaw.  Paired  copulatory 
organs  of  a  unique  type  are  present  in  the  male.  There  is  a  widespread 
tendency  towards  limb  reduction,  which  has  apparently  occurred 


Fig.  232.  Jacobson's  organ.  Diagram  of  reconstructed  L.S.  of  snout  of  lizard  showing  nose 
and  organ  of  Jacobson,  both  seen  in  section  from  the  lateral  side. 

ex.n.  region  of  external  nostril;  in.  internal  nostril;  j.o.  (/.)  Jacobson's  organ  lumen  ;/.o.  (s.e.) 
Jacobson's  organ  sensory  epithelium;  l.d.  lachrymal  duct,  front  end,  cut;  l.n.  lining  of  nose; 
n.j.o.   nerves  to  Jacobson's  organ;   o.b.  olfactory  bulb;  o.n.  olfactory  nerves;   /.   tongue. 

independently  in  members  of  about  half  the  existing  families  of 
lizards,  and  in  snakes. 

The  paired  organs  of  Jacobson  are  highly  elaborated  and  of  great 
functional  importance.  In  snakes  and  in  most  lizards  these  organs 
(Fig.  232)  are  hollow  domed  structures  above  the  front  of  the  palate, 
each  opening  into  the  mouth  by  means  of  a  slender  duct.  The  lachry- 
mal duct  opens  into  or  near  the  duct  of  Jacobson's  organ,  instead  of 
into  the  nose,  suggesting  that  the  secretions  of  the  eye  glands  may  have 
some  special  function  related  to  that  of  the  organ.  Odorous  particles 
are  carried  to  the  ducts  of  Jacobson's  organs,  or  to  the  immediate 
neighbourhood  of  them,  by  the  tongue  tip,  which  is  forked  in  snakes 
and  many  lizards.  The  lumen  of  the  organ  is  partly  lined  by  sensory 
epithelium,  supplied  by  a  separate  branch  of  the  olfactory  nerve. 
Experiments  by  Noble  and  others  have  shown  that  the  organs  assist 
in  such  functions  as  sex  recognition  and  following  trails  left  by  prey. 


(4o6) 


*&m. 


Sphenoaon    /p^^f^i -^  ^-    ;--<# 

^§3&> "'  -"^V,- r  -  .    ,  •  '*   ...  -/     A mphisbaena 


Lyriocephalus 

Fig.  233.  Various  Squamata  {Draco  after  B.M.  Guide). 


xv.  8-9  LIZARDS  407 

In  some  lizards  and  all  snakes,  the  eyelids  are  modified  to  form  an 
immovable  transparent  spectacle  covering  the  cornea,  with  the  loss  of 
the  nictitating  membrane.  The  adaptive  significance  of  this,  which  is 
foreshadowed  in  some  lizards  by  the  development  of  a  window  in  the 
lower  eyelid,  is  not  always  clear,  since  although  it  is  found  in  many 
that  burrow  or  live  in  sand,  it  also  occurs  in  arboreal  forms. 

9.  Suborder  Lacertilia 

The  modern  lizards  show  extensive  adaptive  radiation  (Fig.  233) 
and  include  terrestrial,  arboreal,  burrowing,  and  aquatic  forms.  The 
majority  are  carnivorous  but  there  are  some  herbivores.  It  is  difficult 
to  say  which  of  the  twenty  or  so  living  families  is  the  most  primitive, 
and  the  grouping  of  these  into  infraorders  is  a  matter  of  some  difficulty. 

The  Gekkota  contains  the  geckos  and  a  small  group  of  Australasian 
limbless  forms,  the  pygopodids.  Geckos  are  mainly  small  nocturnal 
and  arboreal  insectivorous  lizards  of  warm  climates,  with  ridged  pads 
on  the  toes  and  sharp  claws  that  enable  them  to  climb  an  almost 
smooth  surface.  Some  species  have  taken  to  living  in  houses.  The 
tree-gecko  Ptychozoon  has  webs  of  skin  on  the  limbs  and  along  the 
sides  of  the  body,  which  perhaps  act  as  a  parachute  to  break  its  fall. 
Many  geckos  live  in  colonies  and  unlike  most  lizards  are  extremely 
vocal,  making  clicking  and  cheeping  sounds.  Their  hearing  is  probably 
acute.  The  endolymphatic  ducts  of  the  inner  ear  are  greatly  expanded 
to  form  sacs  in  the  neck  containing  calcareous  deposits,  but  the  func- 
tional significance  of  this  is  obscure.  Their  eyes  are,  as  a  rule,  covered 
by  a  spectacle.  Geckos  are  the  only  Squamata  that  lay  hard-shelled 
eggs,  those  of  other  forms  being  leathery  in  texture. 

The  Iguania  is  a  large  group  comprising  the  agamids,  iguanids,  and 
chameleons.  The  first  two  include  terrestrial,  arboreal,  and  amphibious 
types,  sometimes  of  large  size,  and  often  furnished  with  crests,  dew- 
laps, expansible  throat-fans  and  other  appendages  that  play  a  part 
in  rivalry  and  courtship.  The  males  are  often  brightly  coloured  and 
the  whole  group  is  characterized  by  a  visually  dominant  behaviour 
pattern.  In  some  arboreal  forms,  as  in  the  chameleons,  the  sensory 
parts  of  the  nose  and  the  organ  of  Jacobson  are  reduced. 

The  agamids  are  found  in  the  Old  World  and  Australasia  and  in- 
clude such  well-known  types  as  the  oriental  'blood-sucker'  (Calotes), 
so-called  because  of  the  red  colour  of  the  throat,  the  spiny  lizards 
(Uromastix)  of  the  north  African  and  Indian  deserts,  and  the  Aus- 
tralian frilled  lizard  (Chlamydosaarns)  (Fig.  240).  The  Indo-Malayan 
genus  Draco  has  a  large  lateral  web,  supported  by  the  ribs,  which  can 


4o8  REPTILES  xv.  9 

be  spread  out  and  used  for  gliding,  though  it  is  not  moved  in  true 
flight.  Lyriocephalus  from  Ceylon  is  an  agamid  with  a  remarkable 
convergent  similarity  to  the  chameleons.  Some  agamids  (and  other 


Fig.  234.  Chameleon  catching  a  fly,  showing  its  changes  in  colour. 

A,  cream  with  yellow  patches,  the  usual  night  colour.  B,  grey-green  with 
darker  patches.  C,  dark  brown  patches  and  yellow  spots.  D,  reaction  pro- 
duced by  pinching  tail,  inflation  and  darkening  of  all  spots.  (After  Gadow.) 

lizards)  can  run  on  their  hind  legs  when  they  are  in  a  hurry  (Fig.  240). 
In  agamids  the  teeth  are  set  squarely  on  the  summit  of  the  jaw,  as  in 
Sphenodon;  this  condition  is  termed  acrodont.  In  most  other  lizards 
the  teeth  are  attached  obliquely  to  the  inner  side  of  the  jaw  (pleuro- 
dont). 

The  iguanids  are  found  mainly  in  the  New  World  and  parallel  the 
agamids  in  many  ways.  Anolis  is  a  small,  common  North  American 
form.  Iguana  from  south  and  central  America  reaches  6  ft  in  length. 


xv.  9  LIZARDS  409 

Amblyrhynchus,  found  only  in  the  Galapagos  Islands,  is  remarkable 
as  the  only  existing  marine  lizard,  though  it  spends  much  of  its  time 
on  shore,  basking  and  feeding  on  the  sea-weed  left  at  high  tide.  Phryno- 
soma,  the  horned  toad,  with  spikes  on  the  head  and  back,  is  found  in 
the  deserts  of  North  America  and  burrows  in  the  sand.  This  is  one  of 
the  few  ovoviviparous  iguanids. 

The  chameleons  are  highly  modified  arboreal  lizards  from  Africa, 
Madagascar,  and  India.  Some  species  have  casques  on  the  head,  or 
one  or  more  horns  on  the  snout.  The  tail  is  prehensile  and  the  digits 
are  arranged  in  groups  of  two  and  three  so  as  to  be  opposable  and 
allow  the  grasping  of  branches.  Chameleons  live  on  insects,  caught 
by  means  of  the  very  long  tongue  (Fig.  234),  which  has  an  adhesive 
clubbed  tip  and  is  projected  by  a  remarkable  muscular  mechanism. 
Their  movements  are  slow  and  deliberate,  but  they  show  considerable 
care  in  stalking  their  prey;  as  they  approach  it  their  eyes,  which 
normally  move  independently,  converge  so  as  to  bring  the  prey  into 
binocular  vision,  presumably  serving  to  judge  its  distance.  Their 
powers  of  colour  change  are  described  on  p.  410. 

The  Scincomorpha  are  another  large  assemblage,  including  Lacerta, 
common  in  Europe  and  North  Africa,  and  the  skinks,  many  of  which 
are  modified  for  burrowing,  sometimes  in  the  sand.  Many  skinks 
have  well-developed  limbs,  but  others  show  all  degrees  of  limb  reduc- 
tion, either  the  fore-  or  hind-limbs,  or  both,  being  lost.  The  most 
highly  fossorial  of  all  lizards,  the  worm-lizards  or  Amphisbaenidae, 
may  also  belong  to  the  Scincomorpha,  though  they  show  many 
remarkable  specializations.  Their  eyes  are  rudimentary,  their  tails  are 
blunt  and  resemble  the  head,  and  they  are  able  to  move  freely  in 
either  backward  or  forward  direction.  External  limbs  are  usually 
absent. 

The  Anguimorpha  contains  the  anguids,  of  which  the  European 
slow-worm  Anguis  is  a  familiar  limbless  example,  and  the  monitor 
lizards  (Varanus)  and  their  allies,  which  are  placed  in  the  superfamily 
Platynota.  The  monitors  of  the  Old  World  and  Australia  include  the 
largest  of  existing  lizards,  one  species,  the  Komodo  Dragon,  growing 
to  at  least  10  ft  long.  They  are  carnivorous,  killing  vertebrates  as  well 
as  insects,  and  are  often  semi-aquatic.  Three  related  groups,  now 
extinct,  occurred  in  the  Cretaceous.  The  aigialosaurs  and  dolichosaurs 
were  amphibious  lizards  of  moderate  size,  but  the  later  mosasaurs, 
such  as  *Tylosawus,  were  huge  creatures,  sometimes  30  ft  long,  and 
were  highly  adapted  for  marine  life,  with  long  jaws  and  paddle- 
like limbs  showing  some   hypcrphalangy.  The  strikingly  coloured 


410  REPTILES  xv.  9- 

heloderms  from  North  and  Central  America  are  also  playtnotids  and  are 
of  special  interest  as  the  only  known  poisonous  lizards.  Another  allied 
form  is  the  rare  earless  monitor,  Lanthanotus,  from  Borneo,  which 
seems  to  be  a  survivor  of  the  primitive  platynotid  stock. 

Many  lizards  are  able  to  change  colour,  the  chameleons,  Anolis 
(often  called  'American  chameleons'),  and  certain  agamids  being  the 
most  notable  for  this.  The  colour  may  change  with  the  environment, 
serving  the  obvious  purpose  of  concealment.  Special  colour  patterns 


Fig.  235.  Diagram  of  the  nervous  control  of  the  melanophores  in  the  chameleon 
(above)  and  minnow  (below). 

c,  spinal  cord;  f,  pathway  of  pigmentomotor  fibres  (the  synapse  in  the  sympathetic  ganglia 

is  omitted);  M,  melanophore;  n,  spinal  nerve;  p,  pigmentomotor  centre;  s,  sympathetic. 

(From  Sand,  minnow  after  v.  Frisch.) 

are  displayed  in  courtship  or  threat,  and  colour  change  may  also 
occur  in  response  to  temperature  and  other  environmental  changes. 
The  physiological  mechanism  of  colour  control  varies  in  different 
reptiles.  In  Anolis  there  are  probably  no  nerves  to  the  melanophores, 
which  are  controlled  by  hormones  produced  by  the  posterior  pituitary 
and  possibly  other  glands.  In  chameleons,  however,  the  melanophores 
are  controlled  partly  or  entirely  by  the  autonomic  nervous  system 
(Fig.  235). 

Many  lizards  are  able  to  break  off  their  tails  when  threatened  or 
seized  by  a  predator;  this  ability,  known  as  autotomy,  is  due  to  the 
presence  of  special  planes  of  weakness  through  the  bodies  of  the  caudal 
vertebrae.  Such  fracture  planes  are  also  found  in  Sphenodon,  but  not 
in  snakes.  After  autotomy  the  tail  regenerates,  but  the  new  member 
is  not  a  replica  of  the  normal.  The  vertebrae,  for  instance,  are  not 
regenerated,  their  place  being  taken  by  an  unsegmented  tube  of  car- 
tilage. It  has  been  shown  experimentally  that  in  Anolis  regeneration 
will  not  occur  if  the  motor-nerves  are  prevented  from  growing  back 


xv.  io  SNAKES  411 

from  the  stump.  The  new  sensory  innervation  of  the  skin  is  derived 
entirely  from  the  surviving  dorsal  roots,  whose  cells  become  greatly 
enlarged. 

10.  Suborder  Ophidia 

The  snakes  are  obviously  descended  from  lizards  of  some  kind,  but 
their  precise  mode  of  origin  is  obscure.  Some  workers  believe  that 
their  nearest  living  relatives  are  the  platynotid  lizards  (monitors,  &c). 
There  is  evidence  that  the  snakes  passed  through  a  burrowing  stage  in 
their  early  history,  although  no  known  platynotids  show  marked  fos- 
sorial  adaptation.  A  burrowing  ancestry  is  particularly  suggested  by 
the  structure  of  the  eye,  which,  as  Walls  has  pointed  out,  differs 
widely  from  that  in  typical  lizards  (Fig.  238).  Thus  there  are  no 
scleral  ossicles  or  cartilages  in  snakes,  and  accommodation  is  brought 
about  in  a  manner  unusual  for  reptiles,  involving  displacement  of  the 
lens.  The  visual  cells  include  cones  of  a  peculiar  type,  which  have 
apparently  been  derived  from  rods.  The  yellow  retinal  droplets  that 
serve  to  protect  lacertilian  retinae  from  excessive  light  are  absent, 
and  instead  some  diurnal  snakes  protect  their  retinas  by  a  yellow- 
tinted  lens.  These  features  can  all  be  interpreted  on  the  supposition 
that  the  ophidian  eye  was  once  drastically  reduced,  but  has  sub- 
sequently been  refurbished  in  response  to  the  needs  of  life  above 
ground.  Other  characters  that  seem  to  point  in  the  same  direction 
include  the  structure  of  the  ears  which,  as  in  many  burrowing  lizards, 
have  apparently  degenerated.  The  ear  drums,  tympanic  cavities,  and 
Eustachian  tubes  are  absent,  and  the  columella  auris  articulates  with 
the  quadrate.  It  seems  unlikely  that  snakes  can  hear  airborne  sounds 
at  all  well,  though  doubtless  they  are  sensitive  to  ground  vibrations 
transmitted  through  the  bones  of  the  jaw. 

The  snakes  show  many  other  interesting  peculiarities,  the  most 
obvious  being  the  complete  absence  of  limbs.  Only  in  a  few  of  the 
more  primitive  forms  such  as  the  boas  and  pythons  can  rudiments  of 
the  hind  limbs  and  their  girdles  be  found;  in  these  snakes  claws  may 
be  present  externally  on  either  side  of  the  cloaca  and  are  said  to  play 
a  part  in  coitus. 

Locomotion  is  produced  by  the  lateral  undulation  of  the  body, 
which  exerts  pressure  on  surrounding  objects  and  pushes  the  snake 
forwards;  the  enlarged  transverse  ventral  scales  of  most  species  help 
to  prevent  slipping.  A  few  snakes  (e.g.  some  boas  and  vipers)  can  also 
progress  by  muscular  movements  of  the  ventral  scales,  with  their 
bodies  stretched  out  almost  in  a  straight  line.  The  spine  is  strengthened 


4i2  REPTILES  xv.  10 

by  additional  intervertebral  articulations  known  as  the  zygantra  and 
zygosphenes. 

The  skull  is  highly  modified,  permitting,  in  all  except  a  few  bur- 
rowing forms,  an  enormous  gape  and  the  swallowing  whole  of  large 
prey.  The  premaxilla  is  small  and  usually  toothless,  and  the  bones  of 
the  upper  jaw  are  loosely  attached  to  the  rest  of  the  skull.  The  two 
halves  of  the  lower  jaw  are  united  only  by  ligaments.  The  sharp 
recurved  teeth  are  carried  on  the  palate  bones  as  well  as  on  the  maxilla 


pro.     /  WSW5" 
sm.  pi. 


Fig.  236.  Diagram  of  skull  in  ophidians. 
d.  dentary;  ec.  ectopterygoid ;  jr.  frontal;  mx.  maxilla;  ».  nostril;  na.  nasal;  0.  orbit;  pa. 
parietal;  pf.  postfrontal;  pi.  palatine;  pm.  premaxilla;  prf.  prefrontal;  pt.  pterygoid;  q.  quad- 
rate; s.  squamosal  or  supratemporal;  sf.  upper  temporal  fossa  (this  is  shown  diagram- 
matically,  as  it  occurs  in  many  lizards;  in  Lacerta  it  is  largely  covered  by  an  extension  of 
the  postfrontal — see  Fig.  213);  sm.  septomaxilla.  (Modified  from  Goodrich.) 

and  dentary.  The  brain-case  is  strong  and  compact,  the  brain  being 
protected  from  mechanical  injury  during  swallowing  by  the  massive 
parasphenoid  and  by  flanges  of  the  frontals  and  parietals,  which  lie 
between  the  orbits,  so  that  there  is  no  interorbital  septum. 

In  the  normal  ophidian  kinetic  mechanism  the  upper  jaw  as  a  whole 
is  raised  as  the  result  of  forward  rotation  of  the  lower  end  of  the  freely 
mobile  quadrate,  which  is  attached  to  the  back  of  the  pterygoid.  The 
well-developed  protractor  muscles  of  the  pterygoid  and  quadrate  play 
an  important  part  in  the  process.  In  the  viperid  snakes  a  further 
elaboration  of  this  mechanism  is  seen,  the  maxilla  being  very  short 
and  able  to  rotate  on  the  prefrontal  so  that  the  fangs  can  be  erected 
(Fig.  237).  A  slip  from  one  of  the  muscles  is  attached  to  the  poison 
gland  and  helps  to  expel  the  venom  as  the  snake  bites. 

The  respiratory  system  and  viscera  of  snakes  are  also  much  modi- 
fled.  The  glottis  can  be  protruded  so  as  to  keep  the  airway  clear  while 
prey  is  being  swallowed,  and  in  some  forms  a  part  of  the  trachea  is 
specialized  for  respiration  as  a  tracheal  lung.  The  left  of  the  two  paired 


XV.   IO 


SNAKES 


4i3 


lungs  is  usually  reduced,  often  to  a  rudiment,  as  in  some  limbless 
lizards,  and  the  other  paired  viscera  tend  to  lie  at  different  levels  on 
the  two  sides.  The  heart  usually  lies  a  quarter  to  a  third  of  the  way 
down  the  body,  and  the  carotid  arches  are  asymmetrical,  the  right 
common  carotid  artery  tending  to  be  suppressed. 


max 


temp  ant 


Fig.  237.  Skull  of  rattle-snake  (Crotalus)  with  jaws  partly  and  fully  opened. 

Lettering  as  Fig.  214;  sph-pt.  the  protractor-pterygoid  muscle,  which  pulls  the  pterygoid 
forward,  causing  it  to  push  the  ectopterygoid,  which  rotates  the  maxilla  and  erects  the 
fang;  di.  the  digastric  muscle  that  assists  in  opening  the  jaw;  temp. ant.  the  anterior  temporal 
which  shuts  the  mouth.  The  diagrams  at  the  right  show  the  actions  of  the  levers  that  erect 
the  fang;  g  is  the  groove  characteristic  of  crotaline  snakes.  (Modified  after  Gadow.) 

The  snakes  show  nearly  as  much  adaptive  radiation  as  the  lizards, 
though  there  is  less  structural  variation  among  them.  The  more  pri- 
mitive forms,  with  pelvic  rudiments,  include  a  number  of  small  bur- 
rowers  such  as  Typhlops,  as  well  as  the  large  boas  and  pythons  of  the 
family  Boidae,  which  tend  to  be  arboreal  and  amphibious  in  habits 
and  kill  their  prey  by  constriction.  In  general,  the  pythons  lay  eggs, 
whereas  the  boas  are  ovoviviparous. 

The  majority  of  living  snakes  belong  to  the  family  Colubridae,  which 
contains  many  medium-sized  harmless  snakes  such  as  the  grass-snake 
(Natrix)  and  some  moderately  poisonous  ones  with  grooved  fangs  at 


Ectodermal 
sphincter,  ci!at< 


Base  pi <. 


Canal  of  Schlemm 
'in  sclera) 
Ciliary  processes 
lacking 

Scleral  ossicle 
■art/  muscle 


■Sclera  (cartilage) 
'Choribid 

'Retina  (avascular 
cone  a!  droplets      and  with  standard 
double  cones) 


Lizard 


Spectacle 


Mesodermal 
sphincter,   dilatator 


raconjunctiysl  space 


Canal  cf  Schlemm 
(in  cornea) 


No  cone  oil  droplets 

No  epichoricidal  lymph  spaces 


Mesodermal  Afcht^Sc'er3  (™™4 

Con  us        / // /y^Lhorioid 

■Retina  (with 
unique  double  cones) 


Snake 


Fig.  238.  Diagrams  of  eyes  of  lizard  and  snake,  to  show  the  marked  contrasts 

resulting  from  presumed  loss  during  underground  life  and  later  acquisition  by  the 

snakes  of  features  paralleling  those  present  in  their  ancestors.  The  dotted  arrows 

show  the  direction  of  application  of  force  during  accommodation. 

(From  Walls,  The  Vertebrate  Eye.) 


XV.   IO 


SNAKES 


4i5 


the  back  of  the  maxillae;  these  are  known  as  back- fang  snakes  or 
opisthoglyphs.  The  South  African  boomslang  (Dispholidus)  is  one  of 
the  few  whose  bite  may  be  lethal  in  man.  Dasypeltis,  the  egg-eating 
snake,  is  also  a  member  of  this  group ;  it  swallows  the  eggs  whole  and 
crushes  them  with  special  tooth-like  processes  of  the  neck  vertebrae. 
The  family  Elapidae  contains  the  cobras,  kraits,  and  coral  snakes, 
all  highly  poisonous  with  quite  small  and  relatively  non-movable  fangs 
at  the  front  of  the  maxilla,  and  a  venom  predominantly  neuro-toxic  in 


<l'S       tp 


Fig.  239.  Head  of  crotaline  snake  (Lachesis)  after  removal  of  skin. 

d.  duct  of  poison  gland,  bending  at  base  of  fang;  dig.  digastric  muscle;  g.  sensory  pit  or 

groove ;  n.  nostril ;  p.g.  poison  gland ;  ta.  and  tp.  anterior  and  posterior  portions  of  temporalis 

muscle;  tr.  trachea.   (From  Gadow.) 

action.  All  the  poisonous  Australian  snakes  belong  to  this  group.  The 
hood  of  the  cobra  is  expanded  by  the  long  cervical  ribs  and  probably 
has  a  warning  (sematic)  function.  The  king  cobra  (Hamadryas)  is  the 
largest  poisonous  snake  and  reaches  18  feet  in  length. 

The  very  poisonous  sea-snakes  (Hydrophiidae)  are  related  to  the 
elapids.  Their  tails  are  vertically  compressed  for  swimming;  some 
species  can  hardly  move  on  land.  Like  many  freshwater  snakes  they 
are  (with  a  few  exceptions)  ovoviviparous. 

The  family  Viperidae  consists  of  the  vipers  of  the  Old  World  and 
the  rattle-snakes  and  pit-vipers,  mainly  from  the  New  World.  The 
two  latter  groups,  placed  in  the  subfamily  Crotalinae,  are  distinguished 
by  the  presence  of  a  remarkable  sensory  pit  on  each  side  of  the  head 
between  eye  and  nostril  (Fig.  239).  This  is  highly  sensitive  to  tem- 
perature changes  and  helps  the  snake  to  detect  warm-blooded  prey. 
The  rattle-snakes  are,  of  course,  also  noted  for  their  caudal  append- 
ages, which  are  composed  of  articulated  rings  and  modified  skin.  One 
ring  is  formed  at  each  moult,  though  the  older  and  most  posterior 
ones  break  off  periodically.  The  rattle  is  vibrated  voluntarily  as  a 


416  REPTILES  xv.  10- 

vvarning  and  perhaps  prevents  the  snake  from  being  trodden  on  by 
large  mammals. 

Most  of  the  Viperidae  are  highly  poisonous,  though  the  bite  of  the 
European  adder  {Vipera  berus)  is  seldom  fatal  to  man.  The  venom  is 
predominantly  haemolytic  in  action.  The  fangs  are  canalized,  the 
canal  having  apparently  being  evolved  by  the  progressive  deepening 
of  a  groove  until  its  margins  have  come  into  apposition.  The  fact 
that  the  fangs  are  erected  when  the  snake  strikes  and  can  be  folded 
back  along  the  roof  of  the  mouth  when  not  in  use,  makes  it  possible 


Fig.  240.  Drawings  of  three  frilled  lizards  (Chlamydosaurus)  and  a  Grammatophora 

(at  right)  to  show  the  bipedal  habit.  (Drawings  made  by  Heilmann  from  photographs 

of  the  lizards  running  at  full  speed,  taken  by  Saville  Kent.) 

for  these  structures  to  be  very  long,  about  1  inch  in  the  case  of  a  large 
puff  adder. 

Some  of  the  American  pit-vipers  are  very  large,  the  dreaded  bush- 
master  (Lachesis)  reaching  about  10  ft.  The  majority  of  the  Viperidae 
bear  their  young  alive  and  the  finding  of  late  embryos  within  the 
bodies  of  female  adders  and  rattle-snakes  may  have  given  rise  to  the 
tale  and  that  these  reptiles  temporarily  hide  their  young  by  swallowing 
them  in  the  face  of  danger. 

1 1 .  Superorder  Archosauria 

We  have  seen  that  about  130  million  years  ago  the  diapsid  stock 
produced  the  most  successful  modern  reptile  group,  the  Squamata 
(Fig.  221).  Much  earlier  an  even  more  successful  type  had  developed 
from  the  Eosuchia,  having  as  its  outstanding  feature  the  habit  of  walk- 
ing on  the  hind  legs.  Creatures  of  this  type  were  the  dominant  land 
animals  of  the  later  Mesozoic,  and  they  include  the  dinosaurs  and 
pterosaurs.  Crocodiles  are  the  only  living  descendants  of  the  group 


xv.  i3  ARCHOSAURS  417 

that  have  remained  at  the  reptilian  level.  They  have,  of  course,  aban- 
doned the  bipedal  habit  and  survive  as  a  specialized  amphibious 
remnant.  The  birds,  which  are  also  undoubtedly  descendants  of  this 
archosaurian  group,  give  us  in  some  ways  a  better  idea  of  the  charac- 
teristic structure  than  do  the  crocodiles. 

All  the  lines  of  archosaurs  are  characterized  by  certain  common 
tendencies,  mostly  associated  with  bipedalism,  which  is  possible  also 
in  some  lizards  (Fig.  240);  features  barely  indicated  in  the  earlier 
forms  become  developed  in  the  later.  In  all  archosaurs  the  hind  legs 
were  much  longer  than  the  front  and  the  acetabulum  formed  a  cup, 
open  below,  so  that  the  legs  were  held  vertically  below  the  body.  At 
the  same  time  the  ischium  and  pubis  became  elongated,  presumably 
to  allow  for  the  attachment  of  muscles  producing  a  fore-and-aft  move- 
ment (see  p.  375).  In  later  forms  the  ilium  became  fused  with  several 
sacral  vertebrae.  The  femur  has  a  lateral  head  and  the  tibia  becomes 
long  and  strong  and  sometimes  fused  with  the  proximal  tarsals;  the 
distal  tarsals  may  fuse  with  the  metatarsals  as  in  birds,  and  the  digits 
are  reduced,  usually  to  three  long  ones  turned  forward  while  the  first 
is  turned  back.  The  skull  is  typically  diapsid,  but  tends  to  have  cer- 
tain modifications,  such  as  the  development  of  antorbital  vacuities 
behind  the  nostrils  and  other  spaces  in  the  palate,  presumably  serving 
to  give  lightness  without  loss  of  strength. 

12.  Order  *Pseudosuchia 

The  earliest  archosaurs  were  the  Triassic  pseudosuchians,  creatures 
evidently  not  far  removed  from  the  Permian  eosuchians.  These 
animals  (*Saltoposuchus)  can  be  visualized  as  lizards  that  ran  on  their 
hind  legs  (Fig.  241).  They  were  small  and  carnivorous,  having  sharp 
teeth  set  in  sockets  along  the  edges  of  the  jaws  (hence  'thecodont'). 
The  skeleton  showed  all  the  archosaur  characters  in  a  most  interesting 
incipient  form.  Thus  the  bones  of  the  pelvis  were  still  plate-like,  but 
arranged  in  the  characteristic  triradiate  manner.  The  front  legs  were 
already  much  shorter  than  the  hind.  Antorbital  vacuities  were  present 
and  there  was  no  pineal  foramen. 

13.  Order  *Phytosauria 

Even  in  the  Triassic  at  least  one  line,  the  phytosaurs,  abandoned 
the  bipedal  habit,  becoming  amphibious.  These  creatures  were  not 
actually  ancestral  to  the  crocodiles,  but  show  remarkable  parallelism 
to  them  in  the  elongated  jaws  and  general  build  (Fig.  241).  How- 
ever the  nostrils  were  set  far  back.  There  can  be  no  doubt  that  the 


418  REPTILES  xv.  13- 

phytosaurs  were  derived  from  pseudosuchians  and  the  two  groups  are 
often  placed  together  in  an  order  Thecodontia. 


Compsognnthus 

Fig.  241.  The  skeletons  of  various  archosaurian  diapsids. 
(Modified  after  various  authors.) 

14.  Order  Crocodilia 

In  the  crocodiles  the  nostrils  are  at  the  tip  of  the  snout  and  the  air 
is  carried  back  in  a  long  tube,  the  maxillae,  palatines,  and  pterygoids 
forming  a  bony  secondary  palate,  as  in  mammals.  There  is  a  flap  on 
the  hind  end  of  the  tongue,  which,  with  a  fold  of  the  palate,  enables 
the  mouth  to  be  closed  off  from  the  respiratory  passage  and  hence 
kept  open  under  water.  The  nostrils  can  also  be  closed  by  a  special 


xv.  14 


CROCODILES 


419 


set  of  muscles,  and  the  ear-drums  are  protected  by  scaly  movable 
flaps.  The  Eustachian  tubes  are  very  complicated,  and  parts  of  the 
skull  are  pneumatized  by  extensions  from  the  middle  ear  cavity,  as  in 
birds. 


Fig.  242.  Diagram  of  the  skull  of  Crocodilia. 
Lettering  as  Fig.  214,  p.  377.  (From  Goodrich.) 


Fig.  243.  Anterior  cervical  vertebrae  of  Crocodilus. 

c.  capitulum;  lip.  hypocentrum;  wa1-4,  neural  arches;  pa.  pro-atlas;  pi.  1-4,  pleurocentra; 
prz.  prezygapophysis;  ptz.  postzygapophysis;  r.  rib;  t.  tuberculum;  tp.  transverse  process. 
The  first  neural  arch  and  the  pro-atlas  of  the  left  side  have  been  removed  to  show  the  first 
pleuro-centrum  (pi1)  which  is  the  odontoid  process.  (From  Goodrich.) 

The  crocodiles  use  all  four  limbs  in  walking,  but  the  front  are 
shorter  than  the  hind,  indicating  bipedal  ancestry.  The  pelvis  of  the 
crocodiles  shows  signs  of  the  typical  triradiate  structure,  but  there 
are  only  two  sacral  vertebrae.  Rapid  swimming  is  produced  by  lateral 
movements  of  the  tail,  but  when  moving  slowly  the  partly  webbed 
feet  are  used  to  push  the  animal  along.  The  ribs  (Fig.  243)  are  two- 
headed  and  there  is  a  proatlas  element  between  the  skull  and  atlas. 
The  scutes  of  the  back  and,  in  some  forms,  of  the  belly,  are  rein- 
forced by  osteoderms,  and  there  are  well-developed  abdominal 
ribs. 


420 


REPTILES 


xv.  14- 


The  soft  parts  of  the  crocodiles  are  of  special  interest  because  croco- 
diles are,  except  the  birds,  the  only  living  creatures  closely  related  to 
the  great  group  of  dinosaurs.  The  heart  (Fig.  245)  shows  a  complete 
division  of  the  ventricle,  but  there  are  still  two  aortic  arches.  The 
truncus  arteriosus  is  divided  in  a  spiral  manner  to  its  base,  so  that 
the  aortae  cross  and  the  right  arch  opens  from  the  thick-walled  left 


car  int. 


car.  cxt 


car.  int. 

I  1        1 1  „  car.  ext 


v.c. 
Che  Ionian 


Crocodile       J 


Fig.  244.  Fig.  245. 

Diagram  of  heart  and  arterial  arches  of  a  chelonian  and  of  a  crocodile,  seen  from  below. 
Lettering  as  Fig.  215,  p.  379.  (From  Ihle,  after  Goodrich.) 

ventricle,  while  the  left  opens  with  the  pulmonary  arteries  from  the 
weaker  right  ventricle.  The  left  arch  would  therefore  contain  venous 
blood,  but  an  aperture,  the  foramen  of  Panizza,  connects  the  two 
arches  near  the  base  and  presumably  the  higher  pressure  in  the  left 
ventricle  ensures  that  the  left  arch  receives  at  least  some  oxygenated 
blood.  Possibly,  however,  the  pressure  in  the  right  ventricle  is  in- 
creased when  the  crocodile  dives  and  the  blood  flows  through  the 
foramen  from  right  to  left. 

The  lungs  are  well  developed,  having  a  system  of  tubes  ending  in 
sacs.  A  transverse  partition  separates  off  a  thoracic  from  the  main 
abdominal  cavity.  This  'diaphragm'  is  not  itself  muscular,  but  is 
continued  into  a  diaphragmatic  muscle  attached  to  the  abdominal 
sternal  plates.  This  muscle,  innervated  by  abdominal  spinal  nerves, 


xv.  15  DINOSAURS  421 

presumably  assists  in  respiration.  It  is  a  development  for  this  purpose 
quite  distinct  from  the  mammalian  diaphragm.  It  is  not  impossible 
that  the  dinosaurs  possessed  further  developments  of  this  arrangement 
of  the  heart  and  lungs,  and  that  they  owed  some  of  their  success  to 
this  mechanism. 

The  modern  crocodiles  represent  only  the  survivors  of  a  once  much 
more  abundant  group.  Crocodilus  is  the  most  widespread  genus, 
occurring  in  Central  America,  Africa  and  Asia,  Malay  and  East 
Indies,  and  North  Australia.  Alligator,  with  each  fourth  lower  tooth 
penetrating  into  a  hole  in  the  maxilla,  is  found  in  North  America  and 
in  China.  Caiman  of  Central  and  South  America  is  related  to  Alligator. 
The  length  of  the  snout  varies  considerably  in  different  species,  and 
is  extremely  long  and  slender  in  the  fish-eating  Gavialis,  Indian 
gharial,  and  Tomistoma  of  the  East  Indies.  Crocodiles  lay  hard-shelled 
eggs  in  large  clutches,  depositing  them  in  the  sand  or  in  nests  com- 
posed of  vegetation.  The  crocodiles  seem  to  have  changed  little  since 
they  first  appeared  in  the  late  Triassic,  perhaps  190  million  years  ago. 
*Protosuchns  of  that  time  had  a  pelvis  like  that  of  crocodiles  but  was 
otherwise  very  like  a  pseudosuchian.  There  were  numerous  types  of 
crocodile  in  the  Jurassic  and  Cretaceous,  living  both  in  fresh  water 
and  in  the  sea.  In  these  forms  the  palate  was  closed  only  as  far  back  as 
the  palatine  bones;  the  addition  of  flanges  of  the  pterygoids  took 
place  only  in  the  Eocene  crocodiles,  which  were  numerous  in  many 
parts  of  the  world,  including  northern  continental  regions  that  today 
are  too  cold  for  such  animals.  In  spite  of  their  specializations  for 
aquatic  life,  the  crocodiles  show  us  many  features  that  were  present 
in  the  earliest  archosaurs  and  they  therefore  give  some  idea  of  the 
characteristics  of  the  ancestors  of  the  pterodactyls,  dinosaurs, 
and  birds. 


15.  The  'Terrible  Lizards',  Dinosaurs 

In  the  10  million  or  so  years  at  the  end  of  the  Triassic  some  of  the 
descendants  of  the  pseudosuchians  became  very  successful  and  numer- 
ous and  many  of  them  were  very  large.  The  large  size  was  not  a 
characteristic  only  of  one  line  but  of  two  quite  distinct  ones,  each  with 
several  sub-divisions.  The  term  dinosaur  is  applied  to  all  of  them,  but 
the  two  main  lines  have  little  in  common  beyond  the  characters 
common  to  all  archosaurs.  The  desire  to  explain  this  extraordinary 
exuberance  of  reptiles  has  attracted  much  attention  to  these 
giants. 


xv.  1 6 


Fig.  246.  The  skeletons  of  various  saurischian  dinosaurs. 
(Modified  after  various  authors.) 


16.  Order  *Saurischia 


These  include  forms  with  a  triradiate  pelvis,  very  like  that  of  the 
pseudosuchians.  The  earlier  types,  like  their  ancestors,  were  bipedal 
carnivores  of  no  great  size,  such  as  *Compsognathus  from  the  Jurassic 


xv.  16  THEROPODS  423 

of  Europe  and  *Ornitholestes  from  that  of  North  America  (Fig.  241). 
The  front  legs  were  short,  with  4  or  3  digits,  provided  with  claws ;  the 
pectoral  girdle  was  reduced  to  scapula  and  small  coracoid,  with  no 
trace  of  clavicles.  Some  members  of  this  line,  the  theropods,  soon 
developed  into  large  carnivores,  such  as  *Allosanrus  (Fig.  246),  over 
30  ft  long  (Jurassic,  North  America).  These  animals  apparently 
swallowed  their  food  whole  and  to  help  with  this  the  quadrate  was 
movable  and  there  was  a  joint  between  the  frontals  and  parietals,  as 
in  many  lizards.  In  other  respects  the  skull  was  very  similar  to  that  of 
the  pseudosuchians. 

At  the  end  of  the  Cretaceous  this  theropod  line  produced  the  largest 
carnivores  that  have  appeared  on  the  earth,  such  as  *Tyrannosaurus 
rex,  nearly  50  ft  long  and  20  ft  high,  from  North  America.  All  the 
previously  mentioned  tendencies  were  here  accentuated,  producing 
creatures  with  bipedal  habit,  very  powerful  head  and  jaws,  and  much- 
reduced  fore-limbs.  They  presumably  preyed  upon  the  large  herbi- 
vorous dinosaurs  of  the  Cretaceous  and  became  extinct  with  their 
prey,  either  from  a  common  inability  to  meet  the  rigours  of  the  climate 
or  in  competition  with  the  mammals  and  birds.  Throughout  most 
of  the  Jurassic  and  Cretaceous  the  theropods  were  the  dominant 
carnivores  of  the  world,  taking  the  place  occupied  earlier  by  the 
synapsid  reptiles  (p.  540)  and  later  again  by  descendants  of  the  synap- 
sids,  the  carnivorous  mammals. 

In  the  Cretaceous  the  organization  of  this  saurischian  line  also 
produced  some  exceedingly  bird-like  forms,  *Struthiomimus  and 
*Ornitho)ithnus,  walking  on  three  toes  and  having  three  also  in  the 
hand,  one  opposable  and  used  for  grasping.  The  skull  became  very 
lightly  built  and  the  teeth  disappeared,  possibly  in  connexion  with  an 
egg-eating  habit  (Fig.  246). 

All  these  carnivorous,  bipedal  saurichians  may  be  grouped  into  a 
suborder  Theropoda.  Another  line  of  organization,  starting  from 
bipedal,  carnivorous  Triassic  theropods,  adopted  a  herbivorous  diet 
and  reverted  to  the  quadrupedal  habit.  These  animals,  the  suborder 
Sauropoda,  culminated  in  the  immense  Jurassic  forms,  * Apatosaurus 
(=  *Brontosaurus)  and  *Diplodocus,  the  largest  of  all  terrestrial 
vertebrates.  Several  stages  of  the  transition  from  bipedal  to  quad- 
rupedal habit  can  be  traced.  *  Yaleosaimis  from  the  Trias  was  a  bipedal 
creature  6  ft  long  but  with  rather  long  front  and  short  hind  legs. 
*Plateosaurns,  also  of  the  Trias,  was  20  ft  long,  but  still  bipedal.  Soon 
the  front  limbs  became  larger  and  more  used  for  walking,  though  the 
disparity  always  remained.  The  neck  was  immensely  elongated  and 


424  REPTILES  xv.  16- 

the  head  very  small,  with  a  lightly  built  skull.  The  nostrils  lay  on  the 
top  of  the  head  and  in  *Diplodocus  formed  a  single  opening.  This 
seems  to  indicate  that  the  animals  were  aquatic  or  amphibious,  as 
would  in  any  case  be  suspected  from  the  very  large  size,  making  it 
unlikely  that  the  legs  could  bear  the  full  weight.  *Diplodocus  and 
*Brachiosaurns  were  over  80  ft  long  and  the  weight  of  the  latter  must 
have  been  nearly  50  tons.  However,  the  structure  of  the  vertebral 
column  shows  that  much  weight  was  carried  on  the  legs,  for  the  verte- 
brae are  strong,  though  hollowed  in  places.  Footprints  of  the  animals 
have  been  found.  One  or  more  of  the  digits  bore  claws.  The  skull 
became  relatively  short  and  broad,  and  among  the  many  puzzling 
features  of  these  giant  animals  is  the  weakness  of  the  jaws  and  small 
size  of  the  teeth,  mostly  crowded  towards  the  front  of  the  mouth. 
These  teeth  would  have  served  well  enough  for  cropping,  but  there 
are  no  teeth  on  the  hind  part  of  the  jaws  and  no  provision  for  grinding 
the  food.  Animals  of  large  size  can  only  have  been  supported  by  this 
feeble  apparatus  if  some  very  nutritious  food  was  readily  available. 
This  perhaps  agrees  with  the  small  size  of  the  brain,  which  was 
several  times  smaller  than  the  lumbar  enlargement  of  the  cord. 

17.  Order  *Ornithischia 

The  second  main  group  of  dinosaurs  appeared  later  than  the  sauro- 
pods  and  possessed  a  4-radiate  pelvis,  with  the  pubis  directed  back- 
wards and  an  extra  pre-pubic  bone  pointing  forwards.  The  teeth  were 
restricted  to  the  hind  part  of  the  jaws,  the  front  bearing  a  beak.  At  the 
front  end  of  the  lower  jaw  there  was  an  extra  bone  (predentary). 
These  were  herbivorous  forms  and  they  appeared  in  the  Jurassic  and 
achieved  their  maximum  in  the  Cretaceous,  by  which  time  the  sauro- 
pods  had  become  less  common.  The  earliest  of  the  ornithischians 
were  bipedal  animals,  included  in  a  suborder  Ornithopoda,  from  the 
Jurassic  and  Cretaceous.  These  animals,  such  as  *Iguanodon,  were 
built  on  the  same  general  lines  as  the  pseudosuchians,  from  which 
they  were  presumably  derived.  The  skull  was  heavily  built  and  adapted 
for  a  herbivorous  diet,  with  powerful  muscles  attached  to  a  coronoid 
process  of  the  lower  jaw.  The  bipedalism  was  less  marked  than  in 
saurischians  and  the  fore-limbs  less  reduced.  Several  separate  lines 
then  reverted  to  a  quadrupedal  habit.  The  trachodonts  (*Hadro- 
saurus)  were  a  very  successful  group  of  amphibious  forms  in  the 
Cretaceous,  with  webbed  feet.  The  teeth  were  suited  for  grinding, 
parallel  rows  being  present,  making  as  many  as  2,000  teeth  in  one 
animal.  In  several  types  of  hadrosaur  the  top  of  the  head  was  pro- 


xv.  i7 


DINOSAURS 


425 


Triceratops 


Fig.  247.  The  skeletons  of  various  ornithischian  dinosaurs. 
(Modified  after  various  authors.) 


longed  in  various  ways,  giving  a  structure  that  perhaps  allowed  the 
nostrils  to  remain  above  water  while  the  animal  was  feeding  below. 
These  animals  reached  30  ft  in  length  and  may  have  supplanted  the 
sauropods  as  marsh-living  forms,  possibly  when  the  soft  foods  gave 
place  to  harder  plants. 

Other  lines  of  ornithischians  became  more  fully  terrestrial  and 
quadrupedal  and  were  mostly  heavilv  armoured.  Thus  the  stegosaurs 
of  the  Jurassic  carried  immense  spines  on  the  back  and  the  tail  bore 


426  REPTILES  xv.  17- 

sharp  spikes.  The  hind  legs  were  much  longer  than  the  front,  a  relic  of 
bipedal  ancestry.  The  feet  carried  hoof-like  structures.  The  skull  was 
very  small  and  the  brain  much  smaller  than  the  lumbar  swelling  of 
the  cord.  The  teeth  were  in  a  single  row  and  small.  The  ankylosaurs 
of  the  Cretaceous  were  covered  all  over  with  bony  plates,  somewhat 
in  the  manner  of  the  mammalian  glyptodonts  (*Nodosaurus,  Fig.  247). 
Finally,  the  ceratopsians,  such  as  * Triceratops  of  the  late  Cretaceous, 
developed  enormous  heads,  with  huge  horns  and  a  large  bony  frill, 
formed  by  extension  of  the  parietals  and  squamosals  to  cover  the  neck. 
These  later  Cretaceous  animals  appear  to  have  lived  on  dry  land  and  to 
have  walked  on  all  fours,  although  the  bipedal  ancestry  is  shown  in 
the  shortness  of  the  front  legs.  There  are  several  indications  that  the 
climate  at  the  close  of  the  Cretaceous  was  becoming  drier  and  the 
organization  of  the  giant  reptiles  became  modified  accordingly.  They 
survived  successfully  for  a  while,  but  were  ultimately  replaced  by  the 
mammals,  perhaps  as  a  result  of  still  further  change  in  the  climate 
(see  p.  538). 

18.  Order  *Pterosauria 

The  Triassic  archosaurian  reptiles  gave  rise  to  two  independent 
stocks  that  took  to  the  air,  the  pterodactyls  and  the  birds.  Both  of 
these  appear  first  in  the  Jurassic  as  animals  already  well  equipped  for 
flight,  although  obviously  basically  of  archosaurian  structure.  We 
cannot  therefore  say  anything  about  the  steps  by  which  their  flight 
was  evolved  and  can  only  speculate  about  the  influences  that  drove 
them  to  take  to  the  air.  The  early  archosaurs  were  bipedal  animals, 
and  the  fore-limbs  were  therefore  free  and  available  for  use  as  wings. 
There  has  been  much  speculation  about  the  intermediate  stages  by 
which  flight  was  produced.  Other  reptiles,  such  as  Draco,  the  flying 
lizard  (p.  407),  develop  a  membrane  between  the  limbs  and  the  body 
to  assist  them  in  making  soaring  jumps.  The  flight  of  pterodactyls 
and  birds  may  have  originated  thus  or,  as  suggested  by  Nopcsa,  by 
the  flapping  of  the  fore-limbs  during  rapid  running  on  the  ground, 
the  animals  then  becoming  airborne  for  longer  and  longer  periods. 

The  stages  of  the  evolution  of  flight  may  have  been  different  in  the 
two  cases,  for  whereas  the  birds  are  obviously  bipedal  animals  and  the 
similarity  to  such  reptiles  as  * Strnthiomimus  and  *Ornithomimus  is 
obvious,  the  pterodactyls  probably  could  not  walk  on  their  hind  legs 
and  may  have  used  the  wing  more  for  soaring  than  for  flapping  flight. 
In  spite  of  great  differences  there  are  interesting  parallelisms  in  the 
structure  of  the  fully  evolved  fliers  of  the  two  groups,  for  instance  the 


xv.  1 8 


PTERODACTYLS 


427 


limb  bones  became  light,  the  skull  bones  fused,  and  the  jaws  toothless 
and  beaked.  This  parallelism  in  lines  known  to  be  distinct,  although 
of  remote  common  origin,  is  similar  to  that  which  we  have  noticed 
before  in  aquatic  animals,  and  it  can  be  interpreted  as  showing  that 


f¥. 


Fig.  248.  The  skeleton  of  a  pterodactyl. 

A,  extra  wrist  bone;  C,  coracoid;  D,  elongated  digit;  F,  femur;  FF,  fin;  H,  humerus; 
MC,  metacarpal;  P,  pelvis;  RU,  radio-ulna;  SC.  scapula;  ST,  sternum;  7',  tail;  TF. 
tibio-fibula;  lowing.  (From  Thompson,  The  Biology  of  Birds,  Sidg\vick&  Jackson,  Ltd.) 

populations  with  similar  genotypes  will  respond  to  similar  environ- 
mental stimuli  in  the  same  way. 

The  pterodactyls  are  most  commonly  found  in  the  Jurassic  strata, 
less  often  in  the  Cretaceous.  Many  specimens  have  been  found  in 
marine  deposits  and  seem  to  have  been  fish-eaters.  The  characteristic 
features  that  have  produced  the  pterodactyl  structure  from  a  thecodont 
ancestry  may  be  described  as  a  lengthening  of  the  head  and  neck, 
shortening  of  the  body  and  ultimately  of  the  tail,  lengthening  of  the 
arms  and  especially  of  the  fourth  digit,  shortening  of  the  legs,  and 
development  of  the  ventral  parts  of  the  limb  girdles.  These  are  the 


428  REPTILES  xv.  18- 

changes  that  can  be  recognized  in  the  bony  parts  available  for  study; 
no  doubt  there  were  many  others  in  the  soft  parts  also  paralleling  the 
evolution  of  birds,  for  instance  the  animals  may  have  been  warm- 
blooded. However,  there  is  no  evidence  that  they  possessed  feathers; 
the  wing  was  a  membrane  (patagium). 

*Rhamphorhynchns  of  the  Jurassic  is  still  recognizably  of  archo- 
saurian  structure,  especially  in  the  skull,  which  has  two  fossae  and 
large  forward-sloping  teeth  (Fig.  248).  The  fore-limb  was  elongated, 
but  the  carpus  still  short,  with  an  extra  'pteroid'  bone  in  front,  pre- 
sumably to  support  the  wing.  The  first  three  digits  were  short  and 
hooked,  the  fourth  long,  supporting  the  wing,  and  the  fifth  absent. 
The  hind-limb  was  slender,  with  five  hooked  digits.  There  was  a  long 
tail,  ending  in  an  expanded  'fin'.  Both  girdles  had  well-developed 
ventral  regions  and  there  was  a  large  'sternum',  keeled  in  front.  The 
scapula  articulated  directly  with  the  vertebral  column. 

*Ptera?wdon,  of  the  Cretaceous,  showed  further  modifications.  The 
trunk  became  shortened  to  ten  or  fewer  segments  and  the  fore-limb 
further  lengthened,  the  carpus  being  long  and  the  fourth  digit  much 
longer  than  the  other  three.  The  hind-limb  remained  small  and  the 
tail  became  very  short.  The  very  large  and  elongated  head  gradually 
lost  its  teeth,  presumably  acquiring  a  horny  beak.  In  the  latest  forms 
the  skull  was  drawn  out  backwards  into  an  extraordinary  process. 
Some  earlier  related  forms  were  only  a  few  inches  long,  but  *Pterano- 
don  itself,  of  the  late  Cretaceous,  had  a  wing-span  of  25  ft. 

Zoologists  have  not  yet  succeeded  in  reconstructing  the  life  of  these 
animals,  and  it  is  hard  to  see  how  they  could  have  walked  on  land. 
The  membrane,  which  stretched  between  both  legs  and  the  body,  and 
perhaps  also  included  the  head,  must  have  been  easily  torn.  The 
feathers  of  birds  can  be  ruffled  without  breaking  and  the  loss  of  a  few 
does  no  great  harm:  the  bat's  wing  can  be  torn,  but  at  least  it  is 
supported  by  many  digits,  whereas  that  of  the  pterodactyl  was  a  huge 
continuous  membrane  supported  by  a  single  finger.  Again  it  is  difficult 
to  see  how  the  animals  can  have  perched ;  if  they  hung,  as  the  claws 
suggest,  was  it  with  the  front  or  with  the  hind  legs?  And  how  can 
they  have  staged  a  take-off,  which  in  birds  is  greatly  helped  by  the 
jump  of  the  hind  legs?  It  is  possible  that  they  always  came  to  rest 
hanging  from  cliffs,  which  they  could  leave  by  soaring.  Even  the  flight 
itself  presents  many  difficulties.  Although  there  is  a  sternum  and  a 
strong  humerus,  neither  suggests  the  presence  of  muscles  sufficiently 
strong  to  carry  a  creature  as  large  as  *Pteranodon.  We  cannot  solve  any 
of  these  mysteries,  but  one  clue  is  that  the  biggest  pterodactyls  were 


xv.  19  EVOLUTION  OF  REPTILES  429 

mostly,  if  not  all,  marine.  The  largest  flying  birds  alive  today  are  the 
albatrosses,  which  use  their  great  weight  to  gain  height  with  the 
increasing  velocity  of  the  wind  a  few  feet  above  the  sea  (p.  460).  It  is 
possible  that  the  pterodactyls  used  a  similar  method  of  soaring.  They 
were  presumably  unable  to  compete  with  the  birds,  however,  and  died 
out  at  the  end  of  the  Cretaceous,  along  with  so  many  other  reptiles. 

19.  Conclusions  from  study  of  evolution  of  the  reptiles 

Many  of  the  conclusions  that  have  been  drawn  from  study  of  verte- 
brate evolution  in  the  water  also  apply  to  the  forms  that  have  come 
on  land.  The  fossil  record  leaves  no  doubt  that  almost  all  the  popula- 
tions have  changed  very  markedly.  Few  forms  of  reptile  alive  today 
are  closely  similar  to  any  found  in  the  Permian  or  Triassic  periods. 
Sphenodon  has  shown  relatively  less  change  than  most  others ;  it  may 
be  significant  that  it  is  found  in  an  isolated  island  region  (but  see 

P-  772). 

The  data  are  not  sufficient  to  show  the  rate  of  evolutionary  change. 

We  cannot  be  sure  whether  it  has  been  constant  or  even  continuous, 

but  particular  types  are  found  only  from  a  limited  range  of  strata  and 

there  is  little  evidence  that  any  terrestrial  form  remains  unchanged  for 

more  than  a  few  million  years,  at  most.  Each  type  is  successful  for  a 

while  and  then  the  niche  that  it  fills  becomes  occupied  by  another 

type,  either  descended  from  the  first  or,  more  usually,  from  some 

related  stock.  Thus  the  earliest  large  land  herbivores  were  probably 

the  pareiasaurs;  these  were  replaced  by  other  reptilian  types  such  as 

the  herbivorous  mammal-like  reptiles,  and  later  the  sauropods  (in  so 

far  as  these  were  terrestrial)  and  various  types  of  ornithischians ;  then 

perhaps  by  the  hadrosaurs  in  the  more  watery  habitats  and  the  stego- 

saurs,  ankylosaurs,  and  ceratopsia  on  drier  ground.  Finally,  all  these 

gave  place  to  the  earliest  mammalian  herbivores,  which  were  in  turn 

replaced  by  others  (p.  776). 

Throughout  early  tetrapod  evolution  there  is  a  tendency  to  return 
to  the  water,  perhaps  under  some  pressure  of  competition  from 
descendants  on  land.  This  is  marked  among  reptiles,  where  besides 
the  chelonians  and  ichthyosaurs  and  plesiosaurs  there  are  the  phyto- 
saurs  and  crocodiles,  and  among  Squamata  the  mosasaurs  and  tylo- 
saurs,  not  to  mention  the  sea-snakes. 

The  large  size  of  many  reptiles  has  been  one  of  their  most  striking 
features,  but  it  is,  of  course,  not  true  to  say  that  there  is  a  strong 
tendency  for  size  to  increase  in  all  reptile  groups.  While  many 
have  become  enormous,  others,  such  as  the  lizards,  have  produced 


43o  REPTILES  xv.  19 

probably  as  great  a  biomass  spread  over  a  large  number  of  small  in- 
dividuals. Large  size  in  a  reptile  may  help  to  conserve  heat  (p.  372), 
but  could  also  endanger  the  animal  from  overheating,  since  the  ratio 
of  surface  area  to  volume  decreases  as  the  absolute  size  increases,  and 
heat  cannot  be  lost  so  readily  through  the  skin.  Up  to  a  point  size  may 
be  a  protection,  but  it  involves  the  dangers  of  those  who  place  all  the 
eggs  in  one  basket ;  incidentally,  the  actual  eggs  of  these  large  animals 
must  have  provided  formidable  physical  problems  for  their  support. 

Parallel  evolution  of  several  lines  descended  from  a  single  stock  is 
as  common  among  reptiles  as  among  other  groups  of  vertebrates. 
Thus  the  bipedal  habit,  with  hind  legs  longer  than  the  front,  has  been 
adopted  independently  by  a  number  of  diapsids;  again,  elongated  jaws 
are  found  among  fish-eaters,  whether  ichthyosaurs,  plesiosaurs,  phyto- 
saurs,  crocodiles,  or  mosasaurs. 

Although  it  is  difficult  to  see  in  all  this  any  persistent  tendency 
except  to  change,  yet  the  very  fact  that  each  type  is  so  rapidly  replaced 
suggests  that  descendants  in  some  way  more  efficient  are  continually 
appearing.  In  the  case  of  the  reptiles  the  more  interesting  of  these 
are  the  birds  and  mammals,  and  we  shall  therefore  leave  the  problem 
of  serial  replacement  among  amniotes  for  later  discussion.  Meanwhile 
we  may  note  once  again  that  the  reptiles  surviving  today,  although  not 
of  larger  size  nor  obviously  better  suited  for  life  than  their  mesozoic 
ancestors,  yet  exist  in  considerable  numbers  alongside  and  even  in 
competition  with  the  birds  and  the  mammals. 


XVI 

LIFE  IN  THE  AIR:  THE  BIRDS 

1 .  Features  of  bird  life 

The  quality  we  define  as  'life'  is  perhaps  more  fully  represented  in 
birds  than  in  other  vertebrates,  or  indeed  in  any  animals  whatsoever. 
It  is  difficult  to  find  units  by  which  accurate  comparisons  can  be  made 
of  such  matters,  but  there  is  a  meaning  in  the  statement  that  the  life  of 
a  bird  is  more  intense  than  that  of,  say,  a  reptile  or  a  fish.  Following 
out  our  definition  of  the  life  of  a  species  as  the  total  of  the  activities  by 
which  that  particular  type  of  organization  is  preserved,  we  shall  find 
that  the  birds  have  many  and  very  varied  activities,  by  means  of  which 
a  great  deal  of  matter  is  collected  into  the  bird  type  of  organization. 
Moreover,  this  is  achieved  under  conditions  remote  from  those  in 
which  life  first  arose;  the  birds  get  a  living  by  moving  in  the  air,  the 
most  difficult  medium  of  all. 

Flight  is  of  course  the  characteristic  that  gives  us  most  fully  the 
feeling  that  the  birds  are  active  animals ;  it  impresses  us  as  a  technical 
marvel  and  as  a  means  by  which  the  animals  obtain  a  most  enviable 
and  valuable  freedom,  enabling  them  to  avoid  their  enemies  and  to 
seek  new  habitats.  Almost  equally  important  items  in  the  active  life  of 
birds  are  the  high  and  constant  temperature  and  large  brain.  These 
features  have  been  acquired  independently  by  birds  and  mammals, 
and  have  led  to  profound  changes  in  behaviour.  A  homoiothermic 
animal  does  not  need  to  change  its  activity  with  the  changes  in  environ- 
mental temperature;  it  can  be  continuously  active,  and,  perhaps  even 
more  important,  its  steady  continuity  of  life  makes  possible  the  accurate 
recording  of  past  experience  in  the  memory.  Probably  only  with  a  high 
and  constant  temperature  can  full  use  be  made  of  the  possibilities  of 
delicate  balance  of  activities  within  large  masses  of  nervous  tissue.  In 
homoiothermic  birds  and  mammals  we  find  larger  brains  and  more 
elaborate  social  and  family  habits  than  in  any  other  animals. 

2.  Bird  numbers  and  variety 

Flight  necessitates  a  large  surface-weight  ratio,  therefore  birds  do 
not  become  so  large  as  some  mammals;  nevertheless,  an  immense 
biomass  is  produced  by  their  very  large  numbers.  Any  attempt  to 
enumerate  the  bird  population  is  largely  guess-work,  but  the  density 
of  breeding  birds  in  different  habitats  in  Britain  has  been  estimated, 


432  THE  BIRDS  xvi.  z- 

and  varies  from  200  per  10  acres  in  woodland  to  20  on  agricultural  land 
and  10  or  less  on  moorland.  Calculating  from  such  figures  Fisher 
estimates  that  there  may  be  100  million  land  birds  in  Great  Britain 
and  100,000  million  birds  in  the  world  altogether,  including  sea  birds. 
This  is  perhaps  a  low  estimate ;  it  would  represent  a  total  biomass  of 
the  same  order  as  that  of  3,000  million  human  beings.  With  all  their 
activity,  therefore,  the  birds  organize  less  matter  into  themselves  than 
do  the  mammals. 

One  of  the  most  striking  features  of  bird  life  is  that  although  the 
basic  organization  remains  fairly  constant  differing  types  show  a  great 
variety  of  special  features,  fitting  them  for  numerous  habitats.  Besides 
differences  in  behaviour,  in  body  form,  and  in  powers  of  flight  there 
are  found  others  in  the  shape  of  the  bill,  and  hence  of  food  habits,  and 
in  the  details  of  many  other  parts,  such  as  the  feet,  that  make  fascinat- 
ing studies  in  adaptation  to  environment. 

3.  The  skin  and  feathers 

The  skin  of  birds  differs  from  that  of  mammals  in  being  thin,  loose, 
and  dry;  there  are  no  sweat  glands,  indeed  the  only  cutaneous  gland 
present  is  the  uropygial  gland  or  preen  gland  at  the  base  of  the  tail. 
The  bird  cleans  its  feathers  with  its  beak,  obtaining  oil  from  this  gland, 
which  is  especially  well  developed  in  aquatic  birds. 

The  keratin-producing  powers  of  the  skin  are  of  course  mostly 
devoted  to  producing  feathers,  but  scales  like  those  of  reptiles  are 
present  on  the  legs  and  feet  and  sometimes  elsewhere.  The  bill  (p.  466) 
and  claws  are  also  specialized  scale-like  structures  and  are  sometimes 
moulted. 

Nerve-endings  are  present  throughout  the  skin,  and  the  cere  at  the 
base  of  the  bill  is  perhaps  an  organ  of  touch.  The  bill  may  itself  have 
special  endings,  such  as  the  corpuscles  of  Grandry  found  in  the  ducks. 

The  feathers  of  modern  birds  provide  a  covering  whose  uses  vary 
from  heat  insulation  and  flight  to  protective  coloration  and  sexual 
display.  It  is  likely  that  in  evolutionary  history  the  function  of  heat 
regulation  came  first.  The  two  main  functions  of  heat  conservation  and 
flight  are  indeed  today  performed  by  feathers  of  different  types  (Fig. 
249).  The  down-feathers  or  plumules,  which  form  the  covering  of  the 
nestling  and  may  be  present  also  in  the  adult,  are  simpler  than  the 
contour  feathers  or  pennae,  and  the  elaborate  flattened  flight  feathers. 
Filoplumes  are  a  third  type,  being  very  fine,  hair-like  feathers.  Usually 
several  generations  of  feathers  are  produced ;  first  the  nestling  feathers 
(neoptiles),  then  one  or  more  generations  of  juvenile  feathers,  which 


xvi.  3 


FEATHERS 


433 


Fig.  249.  Various  types  of  feather. 

A,  filoplumes;  B,  nestling  down-feather;  C,  primary  wing  feather  of  pigeon;  D,  permanent 

down  feather;  E,  feather  with  free  barbs;  F,  emu's  feather  with  long  aftershaft;  G,  contour 

feather  of  pheasant  with  aftershaft.   (Partly  after  Thompson,    The  Biology  of  Birds, 

Sidgwick  &  Jackson,  Ltd.) 

may  be  of  various  types,  prefiloplumes,  preplumules,  and  prepennae; 
finally,  the  adult  feathers  (teleoptiles). 

Each  feather,  of  whatever  type,  is  formed  from  a  dermal  papilla  or 
follicle,  over  whose  surface  keratin  is  produced.  In  down-feathers  the 


434  THE  BIRDS  xvi.  3 

surface  of  the  papilla  is  ridged  all  round  and  the  result  is  to  produce  a 
number  of  fine  threads  or  barbs  of  keratin,  covering  the  body  with 
a  coat  of  fluff,  which  acts  as  a  heat  insulator  by  preventing  air  circula- 
tion. 

Feathers,  like  other  epidermal  structures,  are  moulted,  either  at  a 
certain  stage  in  the  life-cycle  or  seasonally,  a  new  generation  being 

d  flflb 

v.    r  / 


Fig.  250.  The  structure  of  a  feather. 
I.  Whole  feather  showing  calamus  (quill),  C;  rhachis  (shaft),  R;  and  vane,  V.  On  the  right 
side  a  small  area  is  shown  as  it  appears  under  a  lens;  B,  barb;  Bs,  barbule.  II.  A  section  cut 
at  right  angles  to  two  barbs  in  the  plane  of  the  barbules  of  the  anterior  series  (Bsa).  Note 
how  the  hamuli,  H,  of  the  anterior  barbs  interlock  with  ridges  (r)  on  the  posterior  barbules 
{Bsp).  III.  Shows  one  anterior  and  two  posterior  barbules  isolated.  (After  Pycraft,  A  History 
of  Birds,  Methuen  &  Co.,  Ltd.) 

produced  from  the  old  papillae.  Most  birds  moult  after  the  breeding- 
season,  some  a  second  time  during  the  year.  The  down-feathers  of  the 
nestling  are  partly  replaced  by  contour  feathers;  the  follicle,  instead 
of  producing  equal  barbs,  now  forms  two  large  ones  at  one  side,  which 
together  become  the  central  axis  (rhachis),  carrying  a  series  of  further 
barbs  that  spread  at  right  angles  to  it  to  form  the  vane  (vexillum).  Each 
feather  (Fig.  250)  thus  consists  of  a  central  rhachis,  forming  the  hollow 
calamus  or  quill  below  and  carrying  the  barbs,  which  make  the  vane. 
The  calamus  opens  at  the  base  by  the  inferior  umbilicus,  the  entrance 
of  the  mesodermal  papilla,  and  at  the  beginning  of  the  vane  there  is  a 
second  hole,  the  superior  umbilicus.  At  this  point  there  is  often  a  loose 


xvi.  3  FEATHERS  435 

tuft  of  barbs  or  an  extra  shaft,  the  aftershaft,  perhaps  in  some  way 
representing  the  down-feather. 

The  barbs  or  rami  that  make  up  the  vane  are  held  together  by  rows 
of  barbules  (radii)  running  nearly  at  right  angles  to  the  barbs  and 
carrying  hooks  (hamuli)  by  which  the  barbules  of  one  radius  become 
fixed  to  grooves  in  those  of  the  next  (Fig.  250).  Anyone  who  has  played 
with  a  feather  knows  that  these  connexions  can  be  broken  down  so  that 
the  barbs  become  separate,  but  can  be  joined  again  by  'preening'  the 
whole  feather. 

The  feathers  are  provided  with  muscles  at  the  base  and  the  control 
of  their  position  is  important  for  the  regulation  of  heat  loss,  for  flight, 
and  in  many  other  activities,  for  instance  sexual  display.  Like  the  hairs 
of  mammals  the  feathers  are  also  used  as  organs  for  the  sensation  of 
touch,  nerve-fibres  being  wound  round  the  base  of  the  papilla.  In  owls 
and  other  night-birds  special  vibrissae,  analogous  to  those  of  mam- 
mals, are  present.  Various  specialized  feathers  are  used  for  eyelashes, 
ornament,  and  other  purposes,  and  in  some  birds  patches  of  special 
feathers  without  rhachis  break  up  to  make  a  greasy  'powder  down'. 

The  feathers  are  not  spread  uniformly  over  the  body  but  are  localized 
to  certain  tracts,  the  pterylae,  separated  by  bare  areas,  apteria.  Among 
the  contour  feathers  it  is  usual  to  recognize  the  remiges  of  the  wing 
and  rectrices  of  the  'tail'.  The  former  are  divided  into  primaries  on 
the  hand  and  secondaries  on  the  forearm  (Fig.  256).  Each  large  feather, 
whether  in  wing  or  tail,  is  usually  covered  above  and  below  by  several 
rows  of  upper  and  under  coverts.  In  many  birds  there  is  a  peculiar  gap 
in  the  secondary  feathers  of  the  wing,  the  fifth  remex  feather  being 
absent  (diastataxis);  the  condition  in  which  this  feather  is  present  is 
called  eutaxis.  The  feathers  have  a  remarkably  flexible  structure,  so 
that  they  adopt  different  shapes  with  different  positions  of  the  wing. 
The  shape  of  the  quill  and  barbs  varies  between  feathers  and  parts  of 
a  feather,  for  instance  the  barbs  at  the  tip  of  the  primary  feathers 
provide  a  stream-lined  cross-section,  like  that  of  certain  aeroplane 
propellers  (p.  453).  The  small  covert  feathers  at  the  front  of  the  wing 
stand  up  vertically,  but  have  a  right-angle  bend,  thus  providing  the 
wing  camber. 

The  rectrices  vary  greatly,  being  almost  absent  in  birds  that  live 
near  to  the  ground,  such  as  the  wrens,  but  very  large  in  fast-moving 
birds  that  change  direction  quickly  (swallows).  In  these  latter  the  outer 
rectrices  are  enlarged  for  steering  purposes.  The  rectrices  may  be  put 
to  special  uses,  as  in  the  woodpeckers,  where  they  make  a  rigid  brace, 
or  in  the  peacocks,  whose  display  feathers  are  the  tail  coverts. 


436 


THE  BIRDS 


xvi.  4- 


4.  Colours  of  birds 

Birds  possess  colour  patterns  more  vivid  than  those  of  any  other 
vertebrates,  using  them  not  only  for  concealment  but  also  as  the  chief 
means  of  recognition  and  sexual  stimulation  and  hence  as  the  basis  of 
their  social  life.  Like  other  animals  that  live  far  from  the  ground  and 
move  fast  (primates)  the  birds  have  a  poor  sense  of  smell,  often  none 

at  all,  but  they  have  very  good 
vision,  and  in  many  species  the 
turning  of  discriminating  eyes 
by  one  sex  upon  the  other  has 
led  to  the  development  of  a  very 
gorgeous  covering.  The  feathers 
alter  the  appearance  of  the  bird 
so  completely  that  it  is  not  fan- 
tastic to  compare  their  effect  with 
that  of  clothing  in  man. 

As  in  other  animal  groups  the 
colours  are  produced  partly  by 
pigments  and  partly  by  reflection 
and  diffraction  effects  (structural 
coloration).  The  most  common 
pigments  are  melanins,  ranging 
from  black  through  brown  to 
yellow,  and  laid  down  in  the 
feathers  by  special  cells  in  the 
papilla.  The  processes  of  these 
amoeboid  chromatophores  con- 
vey pigment  to  the  epidermal  cells 
(Fig.  251).  Carotenoid  pigments 
(soluble  in  organic  solvents)  are  also  found,  such  as  the  yellow  xantho- 
phyll  of  the  duck's  bill  and  feet  and  the  red  astaxanthin  of  pheasant 
wattles.  White  is  usually  given  by  reflection.  In  blue  colours  incident 
light  is  reflected  from  a  turbid  porous  layer  overlying  a  deposit  of 
melanin  pigment.  In  iridescent  feathers  interference  of  light  in  thin 
surface  films  gives  colours  like  those  of  soap  bubbles.  The  more 
specialized  iridescent  feathers  produce  Newton's  rings,  with  colours 
of  the  second  and  even  third  orders.  The  turacos  or  plantain-eaters  of 
Africa  contain  two  very  peculiar  pigments,  a  copper-containing  red 
porphyrin  turacin,  which  is  soluble  in  weakly  alkaline  water  and  dis- 
solves out  in  the  rain,  and  the  green,  iron-containing  turacoverdin. 


Fig.  251.  Deposition  of  pigment  in  feather 
germ.  Transverse  section  through  a  develop- 
ing arm  feather. 

c.b.  cell  body  of  pigment  cell;  p.  process  of  pig- 
ment cell;  r.  cells  forming  a  radius;  sh.  sheath  of 
feather  germ.  (After  Strong,  from  Streseman.) 


xvi.  5  COLOURS  OF  BIRDS  437 

The  actual  colour  patterns  vary  with  the  habits  of  the  bird.  Con- 
cealing (cryptic)  coloration  is  very  common;  even  the  brighter  colours 
may  serve  this  purpose,  by  breaking  up  the  outline  of  the  bird  when  at 
rest  or  in  motion.  Most  birds  are  dark  above  and  white  below.  The 
feathers  often  show  mottled  or  speckled  patterns  rather  than  a  homo- 
geneous colour.  Finches  and  other  birds  living  in  the  sunlit  upper 
branches  show  bright  yellow,  yellow-green,  and  blue  colours,  either 
singly  or  combined.  Birds  living  in  thickets,  such  as  the  thrush  and 
blackbird,  are  usually  duller  brown  or  black.  An  example  of  disruptive 
coloration  that  is  easy  to  observe  is  the  white  patch  on  the  throat  of  a 
thrush.  If  the  nest  is  approached  while  the  bird  is  sitting  the  head  is 
held  rigidly  still  with  the  beak  upwards ;  the  white  mark  on  the  neck 
breaks  the  outline  and  instead  of  an  obvious  bird's  head  there  appear 
only  the  meaningless  shapes  of  the  sides  of  the  jaws.  In  most  species 
coloration  is  a  compromise  between  concealment  and  conspicuous- 
ness.  Sometimes  selection  has  acted  so  that  the  female  is  cryptic,  the 
male  conspicuous  (e.g.  ducks).  In  hole-nesting  shelducks  both  sexes 
are  conspicuous.  In  other  birds  bright  colours  are  concealed  most  of 
the  time  (e.g.  the  robin's  red  breast  is  underneath,  many  waders  have 
conspicuous  colours  under  their  wings). 

Some  colour  patterns  seem  to  make  the  bird  conspicuous  and  may 
be  a  warning  of  a  distasteful  quality.  The  black  and  white  pattern 
shown  by  the  magpie  may  be  an  example  of  such  sematic  coloration; 
certainly  this  bird  is  seldom  preyed  upon,  no  doubt  partly  because  of 
its  large  size.  The  conspicuous  black  of  rooks  and  starlings  may  be 
connected  with  their  social  life,  making  it  desirable  that  the  birds 
should  easily  follow  each  other,  the  group  being  protected  by  the  com- 
bined receptors  of  its  many  members  and  the  quick  response  of  all 
to  escape  movements  by  any  one. 

The  protective  functions  of  the  colour  often  give  place  in  one  or 
both  sexes  to  garments  used  for  communication  between  individuals, 
for  such  purposes  as  pair  formation,  aggression  between  males,  nest 
site  selection,  or  rearing  the  young. 

5.  The  skeleton  of  the  bird.  Sacral  and  sternal  girders 

The  arrangement  of  the  whole  locomotor  apparatus  is  based  on  the 
plan  of  the  bipedal  archosaurian  reptiles,  modified  and  simplified  for 
the  purposes  of  flight  and  balancing  and  walking  on  two  legs.  The 
bones  are  very  light  and  often  of  tubular  form,  but  sometimes  with 
internal  strutting  well  suited  to  the  stresses  they  must  bear  (Fig.  252). 
Many  of  the  bones  contain  extensions  of  the  air-sacs;  even  the  wing 


438  THE  BIRDS  xvi.  5 

and  leg  bones  are  pneumatized  in  this  way  in  very  good  fliers,  such  as 
some  birds  of  prey  and  the  albatross.  Fusion  of  bones  has  proceeded 
so  far  that  the  skeleton  consists  of  a  few  hollow  girders  and  large 
plates  of  special  shape  (p.  441).  This  result  is  achieved  by  limiting 
the  joints  at  which  movement  occurs  and  simplifying  the  muscular 
system.  The  long  bones  ossify  from  a  single  diaphysis,  there  are  no 
epiphyses  at  the  ends. 

The  skeleton  of  the  backbone  and  limb  girdles  is  so  modified  as  to 
allow  the  weight  of  the  body  to  be  carried  in  two  quite  distinct  ways, 


Fig.  252.  Metacarpal  bone  from  the  wing  of  a  vulture,  sectioned  to  show  the 
arrangement  of  the  struts  similar  to  that  known  to  the  engineer  as  a  Warren's  truss, 
such  as  is  often  used  in  aeroplane  wings.  (After  Prochnow  and  D'Arcy  Thompson.) 

on  the  wings  or  on  the  legs.  For  this  purpose  there  are  two  plate-like 
girders,  the  sternum  and  the  synsacrum,  curved  in  opposite  directions. 
The  muscles  around  the  shoulder  and  hip  joints  balance  the  weight 
on  these  girders  and  produce  propulsion.  The  main  thrusts  come  from 
the  pectoralis  major  in  flying  and  from  the  leg  retractors  in  walking. 
Perhaps  no  other  animals  are  suited  so  perfectly  for  locomotion  by  two 
distinct  means,  and  of  course  many  birds  can  swim  as  well  as  fly  and 
walk. 

The  whole  axis  of  a  bird  is  morphologically  shorter  than  that  of  any 
other  vertebrate  except  a  frog  or  a  tortoise  (Fig.  253):  only  the  neck 
remains  a  long  and  mobile  structure.  The  number  of  cervical  verte- 
brae varies  and  is  greater  in  the  birds  with  longer  necks;  there  are 
fourteen  in  the  pigeon,  if  we  include  two  that  bear  ribs  not  articulating 
with  the  sternum.  The  cervical  centra  have  saddle-shaped  surfaces, 
the  concavity  running  from  side  to  side  on  the  front  and  up  and  down 
behind,  allowing  great  mobility  in  all  directions. 

There  are  four  or  five  thoracic  vertebrae,  all  except  the  last  united 
into  a  single  mass.  The  ribs  are  large,  double-headed,  and  jointed  to 
the  vertebrae.  They  bear  uncinate  processes  on  their  vertebral  por- 
tions, hook-like  projections  overlapping  the  rib  next  behind  and  thus 
strengthening  the  whole  thoracic  cage.  There  is  a  well-marked  joint 


xvi.  s  SKELETON  439 

between  the  vertebral  and  sternal  portions  of  the  ribs.  The  latter  are 
bony,  not  cartilaginous  as  in  mammals,  and  are  jointed  to  the  sternum, 
which  is  a  very  large  keeled  structure  in  all  flying  birds,  serving  to 


Sunsacrum 
(1  thoracic,  5  lumbar 
Z  sacral,  S  caudal ) 


vac. 


Fig.  253.  Skeleton  of  the  pigeon  (Columba). 

at.  atlas;  fl.v.  axis;  C12,  12th  cervical  vertebra;  car.  keel  of  sternum;  carp,  carpus;  cor.  cora- 
coid;  c.r.  cervical  rib;  delt.r.  deltoid  ridge  of  humerus ;  fern,  femur  ;fib.  fibula ;fur.  furcula; 
hyp.  hypapophysis;  il.  ilium;  isch.  ischium;  m.  auditory  meatus;  mc.  2  and  3,  metacarpals; 
pub.  pubis;  pyg.  pygostyle;  rad.  radius;  sc.  scapula;  St.  body  of  sternum;  tar. met.  tarso- 
metatarsus;  tib.tar.  tibio-tarsus;  uln.  ulna;  up.  uncinate  process;  vac.  vacuity  in  side  of  skull. 

carry  the  weight  of  the  body  to  the  wings  by  the  attachment  of  the 
main  wing  muscles  (Fig.  254).  The  pectoralis  major,  which  depresses 
the  wing  in  flight,  is  attached  to  the  edge  of  the  sternum  and  the  great 
depth  of  the  keel  serves  to  increase  the  length  and  mechanical  advan- 
tage of  the  fibres  of  the  muscle  and  also,  by  its  shape,  to  strengthen 
the  sternum.  When  the  bird  is  in  the  air  the  sternum  is  carrying  a  large 
part  of  the  weight.  By  this  arrangement  the  centre  of  gravity  is  kept 
well  below  the  centre  of  pressure,  giving  great  stability. 


44°  THE  BIRDS  xvi.  5- 

The  last  thoracic  (rib-bearing)  veitebra  is  united  with  about  five 
that  can  be  regarded  as  lumbars,  two  sacrals  and  five  caudals  to  make 
a  synsacrum,  which  is  also  fused  with  the  ilium.  This  produces  a  very 
thin  plate-like  structure,  whose  ridged  shape  gives  it  sufficient  strength 
to  carry  the  bird's  weight.  Finally,  there  is  a  short  bony  tail  of  about 
six  free  caudal  vertebrae,  carrying  four  that  are  fused  together  to  form 
the  upturned  pygostyle,  supporting  the  tail  feathers. 

The  joints  of  the  vertebral  column  are  therefore  reduced  so  as  to 
allow  movement  only  in  the  cervical  region,  between  the  thorax  and 


>c±ggs; 


Fig.  254.  Diagrams  of  the  pectoral  and  pelvic  girdles  of  an  eagle,  to  show  the  methods  of 

support  in  flying  and  walking.  In  each  case  the  weight  is  carried  on  an  arch,  the  strength 

of  which  is  obtained  by  the  peculiar  kinked  shape  of  the  thin  sheets  of  bone. 

synsacrum  and  in  the  tail.  The  axial  muscles  have  been  correspond- 
ingly reduced.  Those  of  the  neck  are  large  and  the  hinder  cervical  and 
the  thoracic  vertebrae  have  special  ventral  hypapophyses  for  attach- 
ment of  the  flexor  muscles  of  the  neck.  The  other  back  muscles,  except 
those  of  the  tail,  are  reduced  and  the  whole  back  forms  a  single  rigid 
strut,  carrying  the  weight  of  the  breast  and  viscera  through  the  ribs 
and  the  abdominal  muscles  either  to  the  pelvic  girdle  or  to  the  sternum. 
In  flying  this  weight  is  suspended  on  the  wings  and  there  is  therefore 
a  compression  stress  throughout  the  ribs,  and  this  no  doubt  accounts 
for  the  ossification  of  their  ventral  parts.  The  weight  of  the  bird  when 
resting  on  its  wings  (Fig.  254)  is  thus  carried  by  the  pectoralis  major 
as  a  tension  member,  through  the  plate-like  sternum;  the  ribs,  and 
especially  the  coracoid,  act  as  compression  members.  The  last-named 
bone  lies  nearly  in  the  plane  of  the  pectoralis  major  and  is  very  strongly 
built. 

6.  The  sacral  girder  and  legs 

In  standing,  perching,  and  walking  the  weight  is  balanced  on  two 
legs.  To  achieve  this  posture  the  type  of  girder  found  in  the  vertebral 


xvi.  6  SACRAL  GIRDER  441 

column  of  other  terrestrial  vertebrates  has  been  abandoned,  and  with 
it  the  system  of  braces  (back  muscles)  holding  up  the  weight  of  the 
forepart  of  the  body.  Instead  the  whole  axis  is  so  shortened  that  the 
centre  of  gravity  lies  far  back,  low,  and  over  the  feet.  This  is  not 


Fig.  255.  Diagram  of  muscles  of  the  hind  leg  of  a  bird.  Tendons  shown  dotted. 

1,  Mm.  ilio-trochanterici;  2,  M.  ilio-femoralis;  3,  M.  obturator;  4,  M.  ischio-femoralis; 
5,  M.  caud-ilio-femoralis;  6,  M.  pub-ischio-femoralis;  7,  M.  ilio-tibialis  posterior;  "ja, 
M.  ilio-tibialis  anterior;  8,  M.  sartorius  (ilio-tibialis  internus);  9,  M.  femoro-tibialis  medius ; 
ga,  M.  femoro-tibialis  externus;  11,  M.  ilio-fibularis;  12,  M.  ischio-flexorius;  13,  M. 
caud-ilio-flexorius;  14,  M.  gastrocnemius;  15,  M.  peroneus  superficialis;  16,  M.  peroneus 
profundus;  17,  M.  tibialis  anterior;  18,  Mm.  rlexores  digitorum;  19,  Mm.  extensores 
digitorum.  si.  sling  for  M.  ilio-fibularis.  (After  Stolpe.) 

apparent  from  Fig.  255,  which  is  not  in  a  normal  perched  position. 
Birds  whose  feet  are  placed  far  back  for  swimming  must  hold  the  body 
nearly  upright  to  achieve  a  stable  position  with  the  centre  of  gravity 
over  the  feet  (auks,  penguins).  The  ribs  and  abdominal  muscles  trans- 
fer the  weight  to  the  greatly  elongated  ilia,  which  are  fused  to  the 
vertebrae,  making  a  long  girder  of  approximately  parabolic  form. 
Though  this  is  composed  of  bone  of  almost  paper  thinness,  it  is 
strengthened  by  longitudinal  ridges  (Fig.  254).  Its  strength,  like  that 
of  the  sternum,  lies  not  in  its  arched  shape  in  the  transverse  plane,  but 
in  the  distribution  of  weight  that  is  achieved  by  its  longitudinal  curve 
and  peculiar  kinked  shape.  The  whole  pelvic  girdle  is  modified  to  allow 


(442) 


Fig.  256.  Dissection  of  pigeon  from  back. 

c-h.  coraco-humeral;  caud-il-fem.  caud-ilio-femoralis;  delt.  deltoid;  e.c.r.  extensor  carpi 
radialis;  ex.dig.  extensor  digitorum;  ex. poll,  extensor  pollicis;  fl.dig.  flexor  digitorum; 
fl.met.uln.  flexor  metacarpi  ulnaris;  fl. poll. long,  flexor  pollicis  longus;  gastr.  gastrocnemius; 
il-caud.  ilio-caudalis;  il-fib.  ilio-fibularis  (cut);  il-tr.  ilio-trochantericus;  int.  interosseus; 
isc.f.  ischio-femoralis;  lat.d.  latissimus  dorsi;  lat.lig.  lateral  ligament  of  knee;  m.  external 
auditory  meatus;  n.  sciatic  nerve;  nos.  nostril;  per.  peroneus;  pub. isc. fern,  pub-ischio-femo- 
ralis;  rh.  rhomboid;  sart.  sartorius;  sc.  scapula;  s.c.h.  scapulo-humeral  (cut);  serr.  serratus 
anterior;  5/.  sling  for  tendon  of  ilio-fibularis;  t.  tongue;  tend,  tendon  of  pectoralis  minor; 
tens. ace.  tensor  accessorius;  tens. long,  tensor  longus;  tri.  triceps;  ur.gl.  uropygial  gland; 

vin.  vinculum  elasticum. 


xvi.  6  LEGS  443 

this  arrangement.  The  ischium  and  pubis  are  directed  backwards  and 
do  not  meet  in  a  symphysis,  which  would  prevent  the  underslinging 
of  the  viscera. 

The  legs  are  used  for  balance  and  walking  or  hopping  in  ways  that 
show  interesting  similarities  and  differences  from  those  of  man.  The 
femur  is  turned  under  the  body  and  articulates  with  the  acetabulum 
in  such  a  way  that  movement  is  almost  restricted  to  the  antero- 
posterior direction.  The  bird  balances  on  its  hips  only  in  the  sagittal 
plane;  there  are  no  movements  of  abduction  and  adduction  such  as  are 
found  in  man.  Abduction  of  the  leg,  or  the  falling  medially  of  the 
bird's  body  when  standing  on  one  leg,  is  prevented  by  the  fact  that 
besides  the  ball  and  socket  articulation  of  the  femoral  head  there  is 
also  a  second  joint  surface  between  the  trochanter  and  an  anti- 
trochanter  of  the  ilium.  The  ligaments  across  the  top  of  this  joint  are 
very  strong  and  they  limit  abduction  movements,  while  movements 
of  adduction  are  restricted  by  a  strong  ligamentum  teres  attached  to 
the  femoral  head. 

In  life  the  femur  is  held  nearly  horizontal,  bringing  the  legs  well 
forward.  The  bird  replaces  the  movements  of  abduction  and  adduc- 
tion, which  we  make  at  the  hip  during  walking  in  order  to  prevent 
falling  over  while  only  one  leg  is  on  the  ground,  by  movements  of 
rotation  at  the  knee.  The  muscles  around  the  hip  joint  form  a  system 
of  braces  allowing  balancing  and  locomotion  much  as  in  man,  but  they 
are  well  developed  only  anteriorly  and  posteriorly;  the  lateral  and 
medial  (abductor  and  adductor)  elements  are  weak  (Figs.  255-8).  The 
anterior  group  (protractors)  includes  a  sartorius  (ilio-tibialis  internus) 
running  from  the  ilium  to  the  tibia,  an  ilio-femoral,  and  a  large 
anterior  ilio-tibial  inserted  through  a  patella  to  a  ridge  on  the  front  of 
the  tibia.  Associated  with  this  muscle,  w*hich  crosses  both  hip  and 
knee  joints,  there  are  also,  as  in  man,  femoro-tibial  muscles,  making 
up  with  the  longer  muscles,  the  extensor  system  of  the  knee. 

The  lateral  side  of  the  hip  joint  is  supported  by  rather  small  ab- 
ductor braces,  the  ilio-trochanteric  muscles,  corresponding  to  our 
glutei,  and  acting  mainly  as  medial  rotators,  opposed  by  obturator  and 
ischio-femoral  muscles,  which  work  as  lateral  rotators.  The  main  loco- 
motor muscles  are  the  posterior  braces  or  retractors,  lying  behind  the 
hip  joint  and  including  muscles  knowrn  as  the  posterior  ilio-tibial, 
ilio-fibular,  caud-ilio-flexorius,  pub-ischio-femoral,  ischio-femoral, 
and  caud-ischio-femoral.  Some  of  these  also  act  with  the  obturator 
muscle  as  lateral  rotators,  and  those  placed  more  medially  function 
as  adductors  or  medial  braces,  so  far  as  such  are  required. 


444  THE  BIRDS  xvi.  6 

The  femur  articulates  with  both  tibia  and  fibula  at  the  knee.  The 
fibula  is  distinct  at  its  upper  end,  fused  with  the  tibia  below.  The 
joints  of  the  foot  are  greatly  simplified  by  the  union  of  the  proximal 


Fig.  257.  Leg  of  pigeon  dissected  from  lateral  side. 
amb.  ambiens  tendon;  dist.fi.  flexors  of  distal  phalanges ;  fib.  fibula;  gastr.  gastrocnemius; 
il-fib.  ilio-fibularis;  il-tib.  ilio-tibialis;  isch-fl.  ischio-flexorius;  lig.  lateral  ligament  of 
knee;  peron.brev.  peroneus  brevis;  peron.long.  peroneus  longus;  pr.fi.  flexors  of  proximal 
phalanges;  sort,  sartorius;  sen.  sciatic  nerve;  si.  sling  for  tendon  of  ilio-fibularis;  t.t.  tibio- 
tarsus;  t.mt.  tarso-metatarsus. 

tarsals  with  the  tibia  to  make  a  tibio-tarsus,  articulating  at  an  inter- 
tarsal  joint  with  the  remaining  three  tarsal  and  metatarsal  bones,  fused 
to  make  a  single  tarso-metatarsus.  There  are  usually  four  digits  arti- 
culating with  the  tarso-metatarsus;  three  directed  forwards  and  one 
backwards.  In  standing,  the  weight  is  usually  balanced  in  tripod 
fashion  on  three  of  the  four  points  provided  by  the  front  and  back 
portions  of  the  feet. 


(445) 


Fig.  258.  Pigeon  dissected  from  ventral  surface. 

amb.  ambiens;  bas.  bastard  wing;  br-rad.  brachio-radialis;  b.  biceps;  b.t.  biceps  tendon; 
caud-il-flex.  caud-ilio-flexorius;  cl.  clavicle;  c.br.  coraco-brachialis;  cor.  coracoid;  d.II. 
2nd  digit;  e.c.r.  extensor  carpi  radialis;  ex.  extensor;  ext.obl.  external  oblique;  fl.carp.uln. 
flexor  carpi  ulnaris;  gastr.  gastrocnemius;  oes.  oesophagus;  il-tib.  ilio-tibialis;  int. obi. 
internal  oblique;  lig.  lateral  ligament  of  knee;  nic.  nictitating  membrane;  pect.  pectoralis 
major;  p.m.  pectoralis  minor  (supracoracoideus);  per. long,  peroneus  longus;  pr.long.  pro- 
nator longus;  pub-isc-fem.  pub-ischio-femoralis;  sart.  sartorius;  tens.acc.  tensor  accessorius; 
tib.ant.  tibialis  anterior;  trac.  trachea;  tri.  triceps;  uln.  ulnar. 


446  THE  BIRDS  xvi.  6- 

The  knee  joint  has  some  remarkable  similarities  to  that  of  man.  It  is 
stabilized  by  lateral,  medial,  and  cruciate  ligaments  and  contains  a  pair 
of  lunate  cartilages  or  'menisci'.  The  joint  allows  movements  of  flexion 
and  extension  and  the  femur  as  it  extends  on  the  tibia  in  walking 
rotates  laterally  because  of  the  arrangement  of  the  joint  surfaces.  The 
bird  thus  balances  in  the  medio-lateral  plane  by  rotation  at  the  knee, 
somewhat  as  we  do  by  abduction-adduction  at  the  hip  (Fig.  259). 
When  it  makes  a  step  forward  the  weight  is  brought  by  this  rotation 
at  the  knee  over  the  leg  that  remains  on  the  ground. 


Fig.  259.  Drawings  from  photographs  of  a  goose,  A,  standing;  B,  step- 
ping. The  centre  of  gravity  S  is  brought  over  the  foot  on  the  ground  by 
lateral  rotation  of  the  femur  on  the  tibia.  Note  the  position  of  the  tail 
in  B.  (After  Heinroth,  from  Stolpe.) 

The  intertarsal  joint  allows  mainly  movements  of  flexion  and  exten- 
sion. It  is  largely  supported  by  ligaments  and  has  a  very  strong  capsule 
and  lateral  and  cruciate  ligaments  rather  like  those  of  the  knee;  there 
is  even  a  meniscus  on  the  lateral  side.  The  back  of  the  tibia  is  occupied 
by  the  gastrocnemius  and  the  flexor  muscles  of  the  toes  and  at  the  front 
there  is  a  tibialis  anterior  acting  across  the  inter-tarsal  joint,  and  also 
extensors  of  the  toes.  The  calf  muscles  are  mainly  concerned  with  pro- 
ducing flexion  of  the  toes  in  the  act  of  perching  and  they  form  an 
elaborate  system  of  tendons  attached  to  the  phalanges.  These  tendons 
often  act  as  a  single  unit,  and  there  is  an  arrangement  by  which  the 
flexion  is  passively  maintained  by  the  weight  of  the  body,  even  during 
sleep.  Many  of  the  muscles  are  specially  arranged  to  allow  support  of 
the  joint  whether  in  the  flexed  or  extended  position.  The  ilioflbular 
muscle  passes  through  a  conspicuous  sling  for  this  purpose  (Figs.  255 
and  257).  The  flexor  muscles  of  the  toes  are  inserted  largely  above  the 
knee  and  thus  tend  to  tighten  as  the  bird  sinks.  In  this  they  may  be 
assisted  by  the  ambiens,  a  muscle  found  in  reptiles  and  some  birds, 
which  takes  origin  from  the  ilium.  The  muscle  belly  lies  on  the  medial 


xvi.  7  SKELETON  OF  WINGS  447 

side  of  the  thigh,  and  its  tendon  runs  beneath  the  patella  on  to  the 
lateral  surface  of  the  lower  leg,  where  it  is  attached  to  the  upper  end 
of  the  muscles  that  flex  the  toes.  This  arrangement  provides  a  single 
string  crossing  hip,  knee,  and  ankle  and  allows  the  weight  of  the  body 
to  flex  the  toes  as  the  joints  bend. 

The  second  mechanism  for  maintaining  the  bird  on  its  perch  is  a 
locking  device  that  holds  the  toes  flexed.  The  under-surface  of  the 
flexor  tendon  is  ridged  at  the  metatarso-phalangeal  joint,  where  the 
weight  of  the  body  presses  it  against  a  branch.  The  upper  side  of 
the  tendon  sheath  is  also  ribbed  and  as  the  bird  settles  on  its  perch 
the  two  sets  of  ridges  interlock. 

The  feet  show  a  wide  variety  of  adaptations  for  special  habitats  (Fig. 
260).  In  the  cursorial  and  walking  birds  there  are  often  long  digits  in 
front  and  behind  to  give  a  long  base  for  balance,  but  the  number  may 
be  reduced — to  two  in  running  birds,  such  as  the  ostrich.  Hopping  is 
used  by  small  birds  on  the  ground  and  in  the  trees  and  produces  quick 
movement.  It  is  expensive  because  of  the  large  displacements  of  the 
centre  of  gravity,  and  for  long  distances  or  large  animals  walking  is 
more  efficient.  Many  different  groups  of  birds  have  acquired  webbed 
feet  for  swimming.  In  birds  exposed  to  cold  the  digits  may  be  enclosed 
in  a  coat  of  feathers.  Birds  of  prey  develop  long  raptorial  talons. 
Throughout  the  great  group  of  perching  birds  one  digit  is  directed 
backwards,  allowing  firm  grasp  of  a  branch.  In  climbing  birds  the 
fourth  digit  is  often  directed  backwards  as  well  as  the  first,  so  that  the 
foot  forms  a  sort  of  pincer,  with  long  curved  claws. 

7.  Skeleton  of  the  wings 

The  wing  is  designed  to  have  a  minimum  moment  of  inertia  about 
an  axis  parallel  to  the  sagittal  plane  and  passing  through  the  shoulder 
joint.  Movements  are  produced  by  muscles  lying  either  outside  the 
arm  or  in  its  proximal  part,  with  long  tendons.  The  wing  feathers  are 
carried  along  the  post-axial  border  of  the  humerus,  ulna,  and  hand, 
and  the  shape  of  the  wing  depends  on  the  position  in  which  the  feathers 
are  held  by  their  muscles,  as  well  as  on  membranes,  the  pre-  and  post- 
patagia,  developed  where  the  limb  joins  the  body.  The  active  move- 
ments of  flight  are  produced  mainly  by  the  pectoral  muscles;  the  joints 
and  muscles  of  the  wing  itself  serve  to  spread  the  wing  and  to  adjust  its 
shape  during  each  beat.  The  humerus  is  short  and  broad  with  a  large 
head  and  an  expanded  surface  for  attachment  of  the  pectoral  muscles. 
Radius  and  ulna  are  both  large,  especially  the  latter.  There  are  only 
two  free  proximal  carpals  and  the  remainder  of  the  wrist  is  formed  of 


448 


THE  BIRDS 


xvi.  7- 


three  metacarpals,  one  short  and  two  long  and  fused.  Only  one  digit, 
probably  representing  the  second,  is  well  developed,  having  two  broad 
phalanges;  the  third  and  the  first  digits  consist  of  single  rods,  the 


Fig.  260.  Various  types  of  feet  in  birds. 

1,   shag  (swimming);   2,   crow  (perching,   lifting);    3,   ptarmigan  (stockinged   by 

feathers);  4,  jungle  fowl  (walking,  scraping);  5,  coot  (lobate,  swimming);  6,  jacana 

(suited  for  walking  on  floating  plants);  7,  sea-eagle  (raptorial).  (From  Thompson, 

Biology  of  Birds,  Sidgwick  &  Jackson,  Ltd.) 

latter,  standing  somewhat  apart  at  the  front  of  the  base  of  the  hand,  is 
capable  of  independent  movement ;  it  carries  the  bastard  wing  (alula  or 
ala  spuria). 

The  glenoid  cavity  is  formed  at  the  union  of  a  blade-like  scapula  and 
a  stout  coracoid.  The  former  lies  horizontally  and  is  attached  by 
muscles  to  the  vertebral  column  and  ribs.  The  coracoid  holds  the  wing 


xvi.  8  WING  MUSCLES  449 

away  from  the  sternum,  with  which  it  makes  a  joint.  The  furcula, 
probably  consisting  of  the  combined  clavicles  and  interclavicles,  is 
loosely  attached  to  the  sternum  and  carries  the  origin  of  muscles  that 
rotate  the  humerus  about  its  long  axis. 

8.  Wing  muscles 

Depression  of  the  wing  is  produced  mainly  by  a  single  mass  of 
muscle,  the  huge  pectoralis  major,  making  up  as  much  as  one-fifth  of 
the  whole  weight  of  the  body.  It  runs  from  the  sternum  and  furcula  to 
the  under  side  of  the  humerus,  to  which  it  is  attached,  at  some  distance 
from  the  joint,  by  a  complicated  tendon  of  insertion.  The  fibres  of  this 
muscle  are  very  red  in  strongly  flying  birds  and  often  contain  numerous 
lipoid  inclusions.  In  the  fowl  the  fibres  are  white  and  contain  glycogen, 
but  little  lipoid.  Elevation  of  the  wing  is  produced  by  a  muscle  also 
attached  to  the  sternum,  lying  deep  to  the  pectoralis  major  and  often 
called  the  pectoralis  minor,  but  more  properly  supracoracoideus.  Its 
tendon  passes  through  the  foramen  triosseum,  between  the  furcula, 
scapula,  and  coracoid,  to  be  inserted  on  the  upper  side  of  the  humerus. 
It  is  assisted  by  latissimus  dorsi  and  deltoid  muscles. 

The  chief  muscles  of  the  shoulder  are  thus  a  massive  set  serving  to 
raise  and  lower  the  wing.  There  is  little  development  of  the  other 
muscles  such  as  are  present  in  other  vertebrates  for  the  purpose  of 
balance  and  drawing  the  limb  backwards  and  forwards  for  standing 
and  locomotion.  Such  a  system  of  braces  all  round  the  joint  is  unneces- 
sary; the  bird  balances  on  its  wings  mainly  by  the  action  of  the  pec- 
toralis major  as  the  chief  brace,  between  the  sternum  and  the  humerus, 
with  the  coracoid  as  a  compression  member  between.  Stresses  must  of 
course  arise  in  other  directions  besides  those  tending  to  produce  a 
vertical  fall  and  these  are  met  by  the  muscles  that  produce  rotation  of 
the  humerus  and  various  other  movements  of  the  wing,  especially  a 
pronation,  depressing  the  leading  edge.  The  muscles  used  in  other 
tetrapods  to  sling  the  weight  of  the  body  to  the  pectoral  girdle  and 
fore-limb  are  little  developed.  The  scapula  is  held  to  the  vertebral 
column  by  small  rhomboid  muscles  and  there  is  a  short  series  of  slips 
attached  to  the  ribs,  the  serratus  anterior. 

Other  muscles  running  from  the  body  to  the  humerus  produce 
rotation  of  the  humerus  at  the  glenoid  and  adjustments  of  the  patagia, 
movements  that  are  very  important  in  flight.  From  the  outer  surface 
of  the  scapula  arises  a  scapulo-humeral  muscle,  inserted  in  such  a  way 
as  to  produce  adduction  and  lateral  rotation  of  the  humerus,  raising 
the  hinder  edge  of  the  wing.  The  coraco-humeral  muscle  is  a  compact 


45©  THE  BIRDS  xvi.  8-9 

bundle  attached  near  to  the  last  and  producing  the  opposite  effect  of 
abduction  and  medial  rotation,  lowering  the  hinder  aspect  of  the  wing. 

The  deltoid  muscle  is  divided  into  several  parts  and  besides  its  main 
abductor  action  on  the  wing  also  has  slips  inserted  into  the  skin  of  the 
anterior  patagium,  muscles  known  as  the  long  and  short  tensors  of 
that  membrane.  There  is  also  a  tensor  accessorius,  running  from  the 
surface  of  the  biceps  to  the  skin  of  the  leading  edge  of  the  wing. 

The  muscles  within  the  arm  itself  serve  to  extend  or  fold  the  whole 
wing  and  to  alter  the  positions  of  the  parts,  especially  by  pronation  and 
supination  during  flight.  Large  triceps  and  smaller  biceps  muscles  act 
at  the  elbow.  In  the  forearm  there  is  a  large  extensor  carpi  radialis  and 
an  extensor  carpi  ulnaris,  serving  to  keep  the  wing  extended  at  the 
wrist.  Flexor  carpi  ulnaris  folds  the  wing.  There  are  also  two  large 
pronators,  brevis  and  longus  (brachio-cradialis),  rotating  the  radius 
medially  and  lifting  the  back  of  the  wing.  A  system  of  digital  flexors 
and  extensors,  inserted  into  the  distal  phalanx  of  the  main  digit,  keeps 
the  wing  tip  spread  out  or  folds  it.  The  position  of  individual  feathers 
is  controlled  by  an  elaborate  system  of  tendons  and  muscles  along  the 
back  of  the  hand.  The  first  digit  is  moved  independently  by  abductor 
and  adductor  pollicis  muscles,  controlling  the  position  of  the  bastard 
wing,  which  increases  the  angle  of  stall  and  thus  allows  slow  flying 
speeds  in  take-off  and  landing. 

9.  Principles  of  bird  flight 

A  plane  surface  moved  through  the  air  in  a  direction  inclined  at  an 
angle  to  this  plane  is  known  as  an  aerofoil.  The  forces  generated  can 
be  resolved  into  a  lift  force  acting  upwards  and  a  drag  force  tending  to 
stop  the  motion.  On  this  fact  depends  the  power  of  supporting  weight 
in  the  air  that  is  possessed  by  birds  and  human  heavier-than-air 
machines.  Both  lift  and  drag  forces  are  proportional  to  the  square  of 
the  speed,  and  the  requirement  for  sustained  flight  in  still  air  is  that 
the  object  shall  have  sufficient  speed  to  generate  a  lift  force  equal 
to  its  weight. 

The  flow  of  air  over  the  upper  surface  of  the  wing  reduces  the 
pressure  there  and  provides  the  main  portion  of  the  lift  (Figs.  261-2). 
By  tilting  the  wing  (increasing  the  'angle  of  attack')  the  pressure  on  the 
underside  can  be  increased,  but  the  air  flow  now  tends  not  to  follow 
the  upper  surface  but  to  become  turbulent,  especially  at  the  hind  edge, 
destroying  the  lift  (Figs.  261-2).  When  an  aerofoil  falls  below  this 
critical  speed  it  stalls;  that  is  to  say,  drops  suddenly,  being  no  longer 
supported.  The  smooth  flow  of  air  over  the  wing  tends  to  be  especially 


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452  THE  BIRDS  xvi.  9- 

disturbed  at  its  hinder  ('trailing')  edge  and  by  eddies  round  the  end 
('tip  vortex').  The  proportion  of  length  to  breadth  (aspect  ratio)  in  the 
wing  suitable  for  a  particular  type  of  flight  depends  on  the  need  to 
provide  a  sufficiently  large  undisturbed  area. 

The  shape  of  the  aerofoil  is  of  critical  importance  in  determining  its 
aerodynamic  capacities.  For  birds,  as  for  aeroplanes,  there  are  differing 
shapes,  suitable  for  various  types  of  flight.  To  understand  them  we 
must  classify  the  means  by  which  birds  attain  the  necessary  forward 
velocity.  First  and  most  obvious  is  flapping  flight.  Though  the  details 
of  this  are  varied  and  not  fully  understood,  it  can  be  regarded  as  a 
screw-like  motion  of  the  wings,  providing  forward  and  upward  com- 
ponents (p.  455). 

In  still  air  the  only  alternative  to  flapping  flight  is  to  glide  down- 
wards, which  obviously  cannot  continue  indefinitely.  Yet  some  birds, 
such  as  the  gulls,  and  especially  the  albatrosses  and  the  buzzards, 
condors,  and  other  birds  of  prey,  can  be  seen  to  soar  for  many  minutes, 
gaining  height  without  flapping  the  wings.  Lord  Rayleigh  showed  how 
they  can  do  this  by  making  use  of  the  fact  that  the  air  is  seldom  still. 
Theoretically  the  bird  can  use  three  types  of  air  movement :  (1)  ascend- 
ing currents,  usually  thermal ;  (2)  variations  in  the  wind  velocity  at  any 
one  level  (gusts);  (3)  differences  in  wind  velocity  at  different  levels. 
The  first  method  is  that  used  by  human  sail-planes  and  is  certainly 
adopted  by  many  soaring  land  birds.  The  gustiness  of  the  wind  is 
probably  turned  to  advantage  by  gulls,  rooks,  and  many  other  birds, 
and  the  decrease  in  wind  velocity  near  the  sea  surface  is  used  by  marine 
soaring  birds,  notably  the  albatross. 

10.  Wing  shape 

A  wing  of  the  shape  that  allows  an  albatross  or  swift  to  make  its 
superb  manoeuvres  would  stall  immediately  at  the  speed  of  flight 
adopted  by  a  crow.  In  discussing  wing  shape  the  chief  factors  to  be 
considered  are  (1)  the  wing  area,  (2)  the  aspect  ratio  (wing  length/ 
breadth),  (3)  the  w7ing  outline  and  taper,  (4)  the  presence  of  holes  or 
slots,  (5)  the  camber  or  curvature  of  the  wing. 

1 1 .  Wing  area  and  loading 

A  small  wing  area  is  necessary  for  fast  flight,  since  the  dragoc  areaX 
speed2,  at  least  for  high  speeds.  For  this  reason  fast  aeroplanes  and 
birds  have  small  wings,  but  in  the  bird  the  fact  that  the  wing  provides 
the  forward  momentum  as  well  as  the  lift  greatly  complicates  matters. 
For  flapping  flight  the  wings  must  be  moved  relatively  fast  and  for  this 


xvi.  i3  ASPECT  RATIO  453 

small  size  is  an  advantage.  On  the  other  hand,  a  large  wing  area  allows 
slow  flight  (lift  oc  area  X  speed2)  and  is  found  in  hawks,  vultures, 
storks,  and  other  birds  that  fly  slowly  to  hunt,  especially  if  they  soar 
on  thermal  currents,  for  which  a  large  lift  is  necessary  (p.  458). 

The  loading  of  the  wing  varies  considerably.  Since  the  weight 
increases  with  the  cube  but  the  wing  area  only  with  the  square  of  the 
linear  dimensions,  it  follows  that  large  birds  must  have  relatively  larger 
wings  than  small.  However,  the  larger  birds  usually  have  a  heavier 
loading  of  the  wing,  for  instance,  10  kg./m.2  in  the  duck  (Anas),  20  in 
the  swan  (Cygnns) ,  1  in  the  goldcrest  (Regains),  3  in  the  crow  (Corvus). 
A  considerable  'safety  margin'  remains  in  most  birds;  for  instance, 
pigeons  were  found  to  be  able  to  fly  until  as  much  as  45  per  cent  of 
the  wing  surface  was  removed ;  hawks  and  owls  have  an  especially  high 
safety  margin  and  they  can  carry  prey  almost  as  heavy  as  themselves. 

12.  Aspect  ratio 

Although  a  small  wing  area  reduces  drag,  many  fast-flying  birds 
have  a  large  wing-span.  The  aerodynamic  advantages  of  this  allow  a 
low  rate  of  descent  when  gliding,  reducing  the  expenditure  of  energy 
necessary  to  sustain  flight.  High  aspect  ratio  is  therefore  found  in  birds 
that  fly  fast  by  flapping  flight  (swifts  and  swallows)  and  especially  in 
those,  such  as  the  albatross,  that  glide  fast  in  order  to  obtain  sufficient 
kinetic  energy  to  convert  into  altitude.  However,  these  wings  with  very 
high  aspect  ratio  stall  at  relatively  high  speeds  and  the  birds  that  soar 
slowly  on  thermal  up-currents  over  the  land  mostly  have  a  low  aspect 
ratio.  Some  figures  for  aspect  ratios  are: 


Albatross  (Diotnedea)  .  .  .25 

Gull  (Lartis)         .  .  .  .11 

Swift  (Apus)        .  .  .  .11 

Shearwater  (Puffinus)  .  .  .10 


Vulture  {Neophron)        .  .  .6 

Rook  (Corvus)       .  .  .  .6 

Sparrow  (Passer)  .  .  .  .5 


13.  Wing  tips,  slots,  and  camber 

A  pointed  wing  tends  to  stall  first  at  its  tip  and  is  therefore  only 
suitable  for  fast  fliers.  Such  birds  show  great  development  of  the  hand 
feathers,  producing  a  long  narrow  wing,  whereas  birds  built  for  slower 
flight  and  manoeuvre  have  a  shorter  broader  wing  with  long  arm 
feathers  (Fig.  263). 

The  condition  of  the  air  around  the  wing  is  of  first  importance  for 
the  maintenance  of  lift;  if  there  is  not  a  smooth  stream  over  the  upper 
and  under  surfaces  the  air  becomes  turbulent,  and  the  aerofoil  stalls 
(Figs.  261-2).  This  tends  to  happen  either  if  the  speed  falls  too  low  or  if 
the  angle  of  the  wing  relative  to  the  line  of  motion  increases  above  about 


454  THE  BIRDS  xvi.  13- 

200.  Turbulence  is  mitigated,  however,  by  the  provision  of  openings, 
known  as  slots,  which  let  through  part  of  the  air  and  provide  the 
necessary  smooth  stream.  The  spaces  that  occur  between  the  feathers, 
especially  towards  the  wing  tip,  almost  certainly  function  as  slots. 
Probably  the  arrangement  provides  a  series  of  such  apertures,  giving 
a  very  efficient  high-lift  device.  Such  slots  are  conspicuous  in  slow 


Aca'piter 


Fig.  263.  Wings  built  for  speed  (falcon,  Falco)  and  for  manoeuvring 
(hawk,  Accipiter).  The  former  is  long  and  narrow,  with  relatively 
large  hand  feathers.  The  latter  is  short  and  broad,  the  arm  feathers 
being  long  and  the  primaries  arranged  to  make  slots.  (After  Fuertes.) 

fliers  (rooks)  and  especially  in  those  that  soar  on  thermal  up-currents 
(vultures).  The  feathers  of  such  birds  are  often  individually  tapered 
(Fig.  263).  Slots  are  also  found  in  the  wings  of  large  birds  that  are  fast 
fliers  (pheasants),  the  wing  being  liable  to  stall  in  certain  phases  of  the 
down  strokes.  It  is  possible  that  the  bastard  wing  acts  as  a  slotting 
device;  indeed,  consideration  of  it  played  a  part  in  development  of  the 
theory  of  turbulence  and  slotting. 

The  shape  of  the  wing  has  a  very  important  influence  on  the  air 
stream.  In  most  birds  there  is  a  stiff  leading  edge  and  a  thinner  trailing 
edge.  Nearly  all  wings  are  cambered,  that  is  to  say,  they  taper  from 
the  leading  to  the  trailing  edge,  especially  in  the  region  of  the  forearm 


xvi.  14 


FLAPPING  FLIGHT 


455 


(Figs.  261-2).  This  arrangement  directs  the  air  stream  over  the  upper 
surface  of  the  wing  in  such  a  way  as  to  provide  an  extra  lift  by  creating 
a  'suction  zone'  of  reduced  pressure.  HowTever,  high  camber,  like  low 
aspect  ratio,  reduces  the  speed  of  the  bird. 

14.  Flapping  flight 

Flapping  flight  involves  a  complex, 
screw-like  motion  of  the  wing,  down- 
wards and  forwards  then  upwards 
and  backwards,  more  rapid  upwards 
than  downwards  (Fig.  264).  The 
action  of  the  wings  differs  during 
take-off  or  landing  from  that  in  sus- 
tained flight  (Brown,  1953).  In  the 
former  conditions,  when  the  speed 
is  slow,  forward  velocity  is  provided 
by  backward  movement  of  the  wings. 
During  each  stroke,  beginning  with 
the  wings  raised,  they  are  first  moved 
downward  and  then  forward,  pro- 
viding lift  (Figs.  264,  265).  This 
movement  is  produced  mainly  by 
the  pectoralis  major.  During  the 
upstroke  the  wing  is  first  adducted, 
folded  and  flexed,  and  supinated  at 
the  wrist,  by  the  actions  of  pectoralis 

minor  and  other  muscles.  A  very  rapid  backward  flick  then  follows, 
produced  by  upward  and  forward  rotation  of  the  humerus,  extension 
of  the  wing,  and  pronation  of  the  manus.  The  effect  of  these  move- 
ments, produced  largely  by  the  triceps  and  other  extensors,  is  to 
provide  a  forward  component. 

This  form  of  flight  involves  mainly  the  primary  feathers.  It  is 
evidently  very  tiring  and  can  only  be  continued  for  a  few  seconds.  In 
sustained  flight  the  downstroke  is  as  in  slow  flight  but  the  upstroke  is 
much  simpler,  with  only  a  slight  backward  flick  of  the  primary  feathers. 
The  action  is  such  that  the  inner  part  of  the  wing  provides  lift,  the 
tip  propulsion.  The  upstroke  in  fast  flight  is  thus  mainly  passive, 
produced  by  the  pressure  of  air  against  the  under  surface.  The  major 
part  of  the  effort  needed  to  provide  lift  and  forward  propulsion  is  thus 
provided  by  the  pectoralis  major.  This  muscle  weighs  as  much  as  one- 
fifth  of  the  body  weight  in  flappers,  such  as  the  lapwing,  as  little  as 


Fig.  264.  Pathway  of  the  wing  tip  and 
wrist  joint  relative  to  the  body  during 
free  flapping  flight  of  a  gull.  Equal 
time-intervals  are  shown.  Note  the 
great  speed  of  the  upward  beat  and 
that  the  forearm  is  raised  before  the 
wing  tip.  (After  Demoll.) 


(456) 


Fig.  265.  Pigeon  (Columba)  with  wings  at  bottom  of  stroke  during  rising.  From  a 

photograph  taken  at  very  short  exposure.  Note  forward  position  of  wings  but 

upward  and  backward  curled  primary  feathers.  (After  Aymar.) 


■UW'. 


m^. 


D 


Fig.  266.  Drawings  from  four  photographs  from  film  of  a  take-off  by  an  eagle 
(Aquila).  A.  The  legs  are  jumping  and  the  upper  arms  nearly  vertical  before  the 
wrist  joint  is  extended.  B.  Wing  fully  extended  with  bastard  wing  spread  out, 
some  pronation.  C.  Marked  pronation  as  the  upper  arm  reaches  its  lowest  point. 
D.  The  upper  arm  is  proceeding  upwards,  although  the  hand  has  not  yet  reached 
its  lowest  point.  (Drawn  from  photographs  by  Knight,  from  Streseman.) 


xvi.  i4  FLAPPING  FLIGHT  457 

one-ninth  in  soarers,  such  as  the  gull.  It  does  nearly  all  the  work,  the 
other  muscles  serving  to  give  extra  lift  when  needed. 

The  feathers  are  held  by  an  ela- 
borate system  of  tendons  and  in 
some  birds  they  are  allowed  to 
twist  only  when  the  wing  is  being 
raised  and  the  barbs  of  the 
feathers  themselves  are  so  ar- 
ranged that  they  open  like  the 
vanes  of  a  blind  when  unaer 
pressure  from  above,  but  close 
when  the  pressure  is  from  below 
(Fig.  268).  In  other  birds,  especi- 
ally those  that  fly  fast  with  a  slow 
wing  beat,  such  as  gulls  and 
swans,  the  wing  is  probably  rigid 
on  the  up  as  well  as  on  the  down 


Fig.  267.  Bill-fisher  leaving  its  hole  in  a 
bank,  showing  wings  half-way  through  the 
upstroke.  The  upper  arm  has  reached  its 
highest  point  and  the  forearm  is  just  starting 
upwards;  its  primary  feathers  have  opened 
on  the  right  wing,  reducing  resistance. 
(Drawn  from  photograph  by  Aymar,  Bird 
Flight,  published  by  John  Lane,  The  Bod- 
ley  Head,  Ltd.) 


strokes,  and  is  twisted  so  as  to 

produce  forward  and  upward  components  on  the  up  stroke 


vinculum 


PRIMA 


RIBS 


5  6  78  910  II  12  13  #. 
S£CO/VDARlES 


Fig.  268.  Diagram  of  wing  to  show  arrangement  of  the  flight  feathers. 
(From  Pycraft,  A  History  of  Birds,  Methuen  &  Co.,  Ltd.) 

The  whole  upward  movement  is  usually  faster  than  the  downward 
one.  Before  the  wing  tip  has  reached  its  highest  point  the  upper  arm 
is  already  beginning  to  descend  and  in  this  way  the  line  of  flight  is 


45« 


THE  BIRDS 


xvi.  14-16 


maintained  almost  straight  and  does  not  follow  a  wavy  path  as  it  would 
do  if  the  parts  of  the  wing  vibrated  together.  In  small  birds  the  wing 
works  more  nearly  as  a  whole  and  the  flight  differs  in  several  respects 
from  that  of  larger  birds.  In  general  the  wing  is  a  very  labile  system 
and  regulates  itself  automatically  with  changes  in  the  aerodynamical 
forces.  This  regulation  is  produced  partly  by  feather  plasticity  and 
joint  mobility,  with  participation  of  reflex  muscular  adjustments  that 
are  little  understood. 

The  whirring  flight  of  some  small  birds,  especially  of  humming 
birds,  enables  them  to  remain  almost  in  one 
place  in  the  air,  or  even  to  move  backwards. 
The  wings  beat  backwards  and  forwards 
(Fig.  269),  often  as  fast  as  200  times  a  second, 
and  the  'pectoralis  minor'  is  almost  as  large  as 
the  major. 


15.  Soaring  flight 

Many  birds  economize  the  energy  needed 
for  flapping  flight  by  making  skilful  use  of 
the  possibilities  presented  by  movement  of  the 
air.  All  birds  glide  for  short  distances,  some 
small  birds  with  wings  folded,  others  with 
wings  outstretched.  Sustained  gliding  and 
soaring  upwards  without  flapping  the  wings 
is  found  only  in  large  birds,  probably  because 
considerable  weight  is  necessary  to  provide 
kinetic  energy  sufficient  to  ensure  continuous 
flight  and  efficient  use  of  wind  variations.  As 
has  been  suggested,  there  are  two  distinct  types  of  soaring  birds: 
(1)  land  birds  using  thermal  up-currents,  (2)  marine  birds  using 
variations  in  wind  above  sea  level. 


Fig.  269.  Spotted  fly- 
catcher hovering.  The 
wings  are  passing  back- 
wards and  there  are  spaces 
between  the  feathers. 
(Drawn  from  a  photo- 
graph by  E.  Hosking, 
with  permission.) 


16.  Soaring  on  up-currents 

Up-currents  of  air  arise  in  the  neighbourhood  of  large  objects  on 
the  ground  (cliffs  or  even  a  ship)  and  particularly  from  variations 
in  the  rate  of  heating  of  the  earth's  surface  in  the  sun,  over  rocks, 
vegetation,  mountain  shadows,  &c.  Birds  using  such  currents  usually 
proceed  upwards  in  a  series  of  small  circles,  a  behaviour  seen  in 
buzzards  and  other  hawks  and  especially  characteristic  of  vultures, 
which  may  ascend  in  this  way  above  1,000  ft  (Figs.  270-2).  The 
characteristic  features  of  such  thermal  soarers  are  large  wing  area, 


(459) 


wind 


FlG.  270.  Flight  of  an  eagle  (Aquila). 

a-b,  flapping  flight;  B-C,  soaring  at  constant  height;  C-D, 
soaring  in  ascending  spirals;  d-e,  gliding.  (After  Ahlborn.) 


Fig.  271.  Soaring  flight  of  kite  (Milvus). 

Losing  height  downwind  and  gaining  it  upwind.  Time-marks  one  second. 
(After  Hankin.) 


Fig.  272.  Wings  of  vulture  (Gyps). 

A,  soaring  upwind,  gaining  height;  B,  upwind  on  level;  c,  downwind,  losing  height; 
D-F,  gliding  flight.  (After  Ahlborn.) 


460 


THE  BIRDS 


xvi.  16- 


low  aspect  ratio,  and  wings  broad  at  the  tip  and  usually  provided 
with  well-marked  slots. 

17.  Use  of  vertical  wind  variations 

The  decreasing  effect  of  surface  friction  causes  the  wind  to  blow 
faster  at  greater  heights  and  this  phenomenon  is  used  by  some  birds 
at  sea,  where  conditions  are  presumably  more  uniform  than  over  the 


Fig.  273.  Wings  of  the  albatross  (Diomeded),  used  for  soaring  flight.  Wing  very 
narrow,  with  long  upper  arm  region.  (Drawn  from  photograph  by  Aymar.) 

land.  The  albatross  (Diomeded)  (Fig.  273)  is  the  classic  example  of  this 
type  of  bird,  proceeding  in  a  regular  series  of  movements,  without 
flapping  the  wings,  downwind  losing  height  and  gaining  speed  and 
then  upwind  gaining  height  and  passing  into  a  faster-moving  layer. 
Each  downwind  tack  is  longer  than  the  upwind  one.  During  the  upwind 
tack  the  wings  are  spread  forwards,  downwind  backwards.  The  alba- 
tross remains  all  the  time  within  50  ft  of  the  sea  surface,  because  the 
variations  in  wind  velocity  are  marked  only  at  low  levels.  The 
albatross  shows  the  characteristics  suitable  for  this  type  of  flight, 
namely,  large  size  (it  is  the  largest  of  all  flying  birds),  great  wing  span 
(11  ft),  high  aspect  ratio  (25),  and  pointed  wing  tips,  without  slots. 
Other  sea  birds,  such  as  the  gulls,  though  not  so  highly  specialized, 


xvi.  1 8 


SPEED  OF  FLIGHT 


461 


can  take  advantage  of  variations  in  horizontal  wind  velocity,  including 
gusts  at  any  one  level.  The  bird  moves  upwards  as  it  meets  an  accele- 
rating gust  and  turns  when  the  wind  decelerates.  Gulls  also  use  up- 
currents  at  cliff  faces  and,  no  doubt,  air  movements  of  all  sorts  are 


Fig.  274.  Heron  (Ardea)  leaving  its  perch.  The  legs  have  been  used  to  make  a  jump 
and  the  wings  are  fully  spread.  (Drawn  from  photograph  by  Aymar.) 

widely  used,  especially  by  large  birds.  However,  it  is  evident  that  the 
wing  equipment  only  allows  the  bird  a  limited  range  of  choice  and 
probably  even  the  slightly  different  wing  shapes  of  related  species 
depend  on  the  differing  conditions  they  are  called  upon  to  meet.  A 
vulture  could  no  more  zoom  backwards  and  forwards  over  the  waves 
than  an  albatross  could  circle  slowly  on  a  gentle  thermal  up-current. 
A  pigeon  cannot  equal  a  gull  at  steady  gliding  and  soaring,  but  the 
pigeon  can  rise  more  steeply  or  descend  more  rapidly  without  stalling. 

18.  Speed  of  flight 

Estimation  of  the  speed  of  flight  involves  distinguishing  between  air 
and  ground  speed.  The  speed  relative  to  the  ground  may  be  very  high ; 
there  are  records  of  birds  covering  more  than  100  land  miles  in  an 


462 


THE  BIRDS 


hour,  with  the  help  of  the  wind.  Racing  pigeons  can  average  40  miles 
an  hour  or  more  for  considerable  periods.  Air  speeds  of  30-50  m.p.h. 
can  certainly  be  reached  by  many  birds:  swifts  are  said  to  reach  100 
m.p.h.  in  still  air. 


Fig.  275.  Pigeons  (Columba),  photographed  during  take-off,  with  exposures  of 
1/825  second.  A,  front,  and  b,  rear  view,  with  wings  together,  c,  nearly,  and  d, 
quite  at  bottom  of  downstroke;  note  pronation  and  forward  movement  of  wing. 
E  and  F,  wings  during  the  upstroke;  in  f  the  primary  feathers  have  opened;  note 
that  the  wing  moves  backwards  and  that  the  motion  is  faster  than  on  the  down- 
stroke.  (From  photographs  by  Aymar.) 

19.  Take-off  and  landing 

At  the  take-off  the  bird  has  to  acquire  sufficient  forward  momentum 
to  provide  lift,  and  yet  must  leave  the  air  sufficiently  undisturbed  for 
subsequent  beats  to  be  effective.  In  many  birds,  especially  the  smaller, 
the  jump  provided  by  the  legs  is  adequate  for  the  take-off  (Fig.  274). 
Large  birds  must  run  or  swim  rapidly  to  obtain  sufficient  speed.  Eagles 
are  said  to  be  unable  to  rise  without  a  long  run,  and  many  large  birds 
nest  on  a  cliff  or  tree,  which  gives  them  an  up-current  for  the  take-off. 
Swifts  usually  come  to  rest  high  up  and  can  only  rise  off  the  ground 
with  difficulty.  The  albatross  is  unable  to  take  off  from  the  sea  surface 
in  a  dead  calm. 

The  first  beats  are  usually  very  large,  beginning  with  the  wings 
above  the  back  and  held  at  such  an  angle  as  to  produce  a  large  forward 


xvi.  19 


LANDING 


463 


component.  The  wings  may  be  heard  actually  clapping  together  in 
pigeons  (Fig.  275).  During  rapid  ascent,  as  in  the  larks,  the  body  is 
nearly  vertical  and  the  wing  changes  its  angle  at  the  shoulder  very 


Fig.  276. Jackdaw  about  to  land. 
The  wings  are  fully  extended  on 
the  downbeat,  and  the  tail  is 
fanned  out  and  bent  downwards. 
(From  photograph  by  Aymar.) 


Fig.  277.  Hawk  striking  at  a  dummy  owl. 
Note  long  legs  and  the  method  of  braking. 
The  wings  are  broad  and  rounded,  giving  a 
large  safety  factor.  (From  photograph  by 
Aymar.) 


sharply  between  the  downward  and  recovery  strokes.  The  bastard 
wing  is  held  in  such  a  position  that  the  beat  provides  extra  forward 
momentum. 

Landing  is  also  a  delicate  operation,  especially  since  it  often  involves 
coming  to  rest  suddenly  on  a  branch  (Fig.  276).  This  is  achieved  by 
lowering  and  fanning  out  the  tail,  which  thus  acts  as  a  flap,  providing 
both  lift  and  braking.  The  legs  are  then  lowered;  often  one  further 
wing  stroke  is  given  to  bring  the  bird  forward  to  drop  onto  the  perch. 
The  adjustment  of  braking  in  such  a  way  as  to  prevent  stalling  involves 
a  very  special  system  of  coordination  (Fig.  277).  Other  methods  of 


464  THE  BIRDS  xvi.  19- 

landing  are  possible,  for  instance,  rooks  may  make  a  roll  and  sideslip 
to  the  ground. 

20.  The  skull  in  birds 

The  arrangement  of  the  parts  of  the  bird's  skull  is  similar  to  that  of 
archosaurian  reptiles  (Fig.  242).  Individual  bones  can  be  recognized 
in  the  young,  but  they  mostly  become  united  in  the  adult  to  form  a 
continuous  thin-walled  structure  that  encloses  the  brain  and  sense- 
organs  and  supports  the  beak  (Fig.  278).  Most  birds  are  microsmatic; 
the  nasal  passages  are  simple  and  the  turbinals  reduced.  There  is 
seldom  a  complete  bony  secondary  palate,  such  as  there  is  in  mammals, 
instead  the  internal  nostril  opens  into  the  mouth  relatively  far  forward. 
The  large  size  of  the  brain  and  reduction  of  its  olfactory  portions  are 
responsible  for  the  rounded  form  of  the  top  of  the  head,  and  there  are 
very  large  orbits  at  the  sides,  separated  by  an  ossified  septum.  The 
base  of  the  skull  is  formed  by  a  basioccipital  behind,  carrying  a  single 
occipital  condyle.  There  is  a  large  basisphenoid,  covered  ventrally  by 
a  pair  of  basitemporals,  probably  representing  the  parasphenoid,  the 
front  part  of  which  makes  a  'basisphenoid  rostrum',  as  in  archosaurs. 

The  jaws  are  characteristically  slender  and  elongated;  in  the  more 
advanced  birds  they  have  a  very  special  form  of  support.  The  upper 
part  of  the  front  of  the  skull  is  composed  of  the  enlarged  premaxillae, 
the  nostrils  lying  very  far  back  and  the  nasal  bones  being  small.  The 
palatines  are  long  and  fused  far  forward  with  the  maxilla,  while  they 
articulate  movably  behind  with  the  pterygoids  and  base  of  the  skull. 
The  pterygoid  is  a  slender  rod,  itself  movably  articulated  with  the 
skull  and  with  the  quadrate,  which  is  a  triangular  bone  with  clearly 
separate  otic  and  basal  articular  processes.  The  upper  jaw  is  thus  a 
long  thin  bar  composed  of  maxillae,  quadrato-jugal,  and  jugal,  and  as 
in  many  reptiles  it  is  capable  of  considerable  movement  ('kinesis'). 
It  is  raised  when  the  lower  end  of  the  quadrate  moves  forwards.  This 
mechanism  is  particularly  well  developed  in  parrots,  where  the  beak 
is  freely  hinged  on  the  skull.  This  type  of  palatal  arrangement  is  known 
as  neognathous.  In  some  birds,  such  as  the  flightless  ratites,  the 
palatines  are  shorter,  the  vomer  larger,  and  the  pterygoids  less  mov- 
able, a  condition  called  palaeognathous  (p.  514).  The  lower  jaw,  also 
elongated,  consists  of  the  articular  bone  and  four  membrane  bones. 

21.  The  jaws,  beak,  and  feeding  mechanisms 

There  is  a  complete  lower  temporal  bar,  composed  of  jugal  and 
quadrato-jugal  bones.  The  temporal  region  is  hard  to  interpret,  but 


XVI.  21 


JAWS 


465 


Fig.  278.  Skull  of  young  gosling  (Anser). 
A.  angular;  Ar.  articular;  As.  alisphenoid;  Bo.  basioccipital;  Bsh.  basisphenoid ;  D.  dentary; 
E.  ethmoid;  Eo.  exoccipital;  F.  frontal;  Ip.  interparietal;  J.  jugal;  L.  lachrymal;  Mx. 
maxillary;  Ar.  nasal;  O.  supra-occipital;  Op.  opisthotic;  P.  parietal;  Pa.  palatine;  Pm.  pre- 
maxillary;  Po.  postorbital;  Pt.  pterygoid;  Q.  quadrate;  Qj.  quadrato-jugal;  R.  rostrum  of 
basisphenoid;  S.  squamosal;  Sa.  sur-angular;  V.  vomer.  (From  Heilmann,  The  Origin  of 
Birds,  H.  F.  &  C.  Witherby,  Ltd.) 

has  presumably  been  derived  from  the  diapsid  archosaurian  condition. 
Typically,  there  is  a  single  large  fossa,  communicating  with  the  orbit, 
but  this  is  often  partly  subdivided  by  bony  processes;  occasionally, 
there  is  a  complete  post-orbital  bar  (parrots).  There  are  moderately 
large  temporal  and  pterygoid  muscles,  but  the  jaws  are  not  usually 


466 


THE  BIRDS 


XVI.  21 


Fig.  279.  Various  bird  beaks. 

1,  Merganser;  2,  Flamingo;  3,  Shoveller;  4,  Scissor-bill  (adult);  5,  Scissor-bill  (young); 
6,  Anastomus;  7,  Hornbill;  8,  Hummingbird;  9,  Avocet;  10,  Parrot;  11,  Parrot;  12,  Spoon- 
bill;  13,  Crossbill;  14,  Nightjar;  15,  Eagle;  16,  Balaeniceps.  (From  Pycraft,  A  History  of 
Birds,  Methuen  &  Co.,  Ltd.) 

very  powerful,  though,  of  course,  formidable  in  carnivores.  Having 
completely  lost  the  teeth,  the  birds  must  rely  largely  on  internal 
processes  to  break  up  the  food.  The  beak  is,  however,  characteristically 
modified  according  to  the  food  habits  (Fig.  279).  There  is  very  great 
variety  in  the  feeding,  as  in  so  much  of  the  life  of  birds,  and  though 
many  species  keep  strictly  to  one  diet  others  are  able  to  adapt  them- 
selves to  the  food  available.  The  ingenuity  and  persistence  with  which 
birds  seek  and  collect  food  must  be  a  main  factor  in  their  success. 

Many  birds  with  a  moderately  long  bill,  such  as  the  song-thrush 
(Turdus),  can  eat  either  flesh  (snails,  earthworms,  or  caterpillars)  or 


XVI.  21 


BEAKS 


467 


fruit.  Incidentally  we  may  notice  the  ingenious  behaviour  by  which 
the  snail's  shell  is  cracked  open  to  obtain  the  food,  by  beating  it  against 
a  stone.  Birds  that  mainly  eat  seeds,  such  as  the  finches,  usually  have 
short,  thick,  strong  bills.  Large  strong  bills  are  present  in  the  hornbills 
and  toucans ;  they  push  through  dense  foliage  to  obtain  the  fruit,  which 
may  have  a  hard  case.  In  parrots  the  beak  is  moved  on  the  skull, 
pushed  up  by  the  upper  jaw  when  the  latter  is  pulled  forward  by  the 
digastric  muscle. 


Fig.  280.  The  Galapagos  woodpecker  finch  (Camarhynchus  pallidus)  using 
its  stick.  (From  Lack,  drawn  by  R.  Green  from  photograph  by  R.  Leacock.) 

The  carnivorous  birds,  such  as  most  eagles  and  owls,  have  short 
and  sharp  beaks,  whereas  fish-eating,  as  in  other  vertebrates,  results 
in  long  jaws.  Another  widely  found  arrangement  is  the  flattened  bill 
of  some  ducks,  similar  to  those  of  some  sturgeons  and  of  the  platypus, 
which  also  sift  out  food  from  water  or  mud.  The  long,  thin  beak  of  the 
curlew  selects  food  from  mud  in  a  different  way,  mostly  worms  and 
other  soft-bodied  invertebrates.  Lesser  flamingos  feed  on  blue-green 
algae  and  microscopic  phytoplankton,  collected  by  a  filter  system  on 
the  jaws,  using  a  current  of  water  produced  by  the  sucking  mouth  and 
piston-like  tongue.  Some  insectivorous  birds  have  long  beaks  for 
finding  their  prey  under  bark.  The  woodpeckers  have  a  strong  beak 
like  a  pick-axe  for  excavating  in  wood,  and  most  elaborate  special 
modifications  for  the  purpose  of  licking  up  insects;  there  is  an  enor- 
mously long  protusible  tongue  and  special  hyoid.  The  woodpecker 
finch  {Camarhynchus  pallidus)  on  the  Galapagos  Islands  probes  insects 
from  the  bark  by  means  of  a  cactus  spine,  a  remarkable  case  of  the  use 
of  a  tool  by  a  bird  (Fig.  280).  Among  the  most  specialized  feeders  are 


468 


THE  BIRDS 


XVI.  21- 


the  humming-birds,  eating  nectar,  the  beak  being  long  or  short  accord- 
ing to  the  type  of  flower  visited,  and  the  tongue  provided  with  a 
special  tubular  tip. 

i  net 

22.    Digestive    system   of 
birds 

Once  the  food  is  in  the 
mouth  it  is  manipulated  by 
the  long,  thin  tongue,  mois- 
tened with  saliva,  which 
usually  consists  of  mucus 
but  is  said  to  contain  diasta- 
tic  enzyme  in  some  seed- 
eating  finches.  Food  swal- 
lowed down  the  oesophagus 
may  be  stored  in  a  large 
receptacle,  the  crop,  found 
especially  in  grain-eating 
birds;  its  lining  is  of  oeso- 
phageal structure  (Fig.  281). 
The  true  stomach  is  divided 
into  two  parts,  a  glandular 
proventriculus  and  a  muscu- 
lar gizzard.  The  structure  of 
the  anterior  chambers  of  the 
gut  varies  greatly  with  the 
diet.  In  grain-eating  birds, 
such  as  the  pigeon,  the  crop 
is  large  and  the  seeds  are 
first  macerated  by  storage 
there.  They  are  then  mixed 
with  peptic  enzymes  in  the  proventriculus  and  ground  up  in  the  mus- 
cular gizzard,  which  in  pigeons  has  a  horny  lining  and  also  contains 
numerous  small  stones.  In  insectivores  and  carnivores  the  crop  is 
usually  smaller  or  absent,  but  is  very  large  in  some  fish-eating  birds. 
In  carnivores  the  gizzard  has  the  character  of  a  more  normal  stomach. 
It  was  stated  by  John  Hunter  that  herring  gulls,  normally  living  on 
fish,  readily  take  to  eating  grain,  and  that  after  a  year  or  so  of  this 
diet  the  gizzard  becomes  muscular  and  has  horny  walls. 

The  peptic  juice  has  powerful  digestive  powers  and  many  carni- 
vorous and  fish-eating  birds  dissolve  even  the  bones  of  their  prey, 


b.d 


Fig.  281.  Dissection  of  pigeon, 
bile-ducts;  cl.  cloaca;  coec.  coeca;  cr.  crop;  giz. 
gizzard;  int.  intestine;  k.  kidney;  /.  liver;  oes.  oeso- 
phagus; p.  pancreas;  p.d.  pancreatic  ducts;  pr.  pro- 
ventriculus ;  sp.  spleen ;  test,  testis.  (After  Schimkewitsch 
and  Streseman.) 


XVI.  22 


ALIMENTARY  CANAL 


469 


though  in  owls  these  are  regurgitated  with  fur  or  feathers,  making 
characteristic  pellets.  The  crop  of  pigeons  is  also  remarkable  for  the 
milk  it  produces  to  nourish  the  young.  There  are  special  glands  for 
this  purpose  and  they  become  active  in  the  breeding-season  under 
the  influence  of  a  pituitary  hormone,   prolactin,  which  has  been 


ur&vj 


Fig.  282.  Diagrammatic  section  through  cloaca  of  pigeon. 
ap.   external   aperture;   b.Fab.   bursa   Fabricii;   ep.   epidermis;   m.sph. 
sphincter  muscle;  muc.  mucous  glands;  r.  rectum;  ur,  &  vd.  papillae 
for  ureter  and  vas  deferens  (or  oviduct).  (After  Clara,  from  Streseman.) 

crystallized  and  is  probably  protein  in  nature.  Prolactin  causes 
regression  of  testes  and  ovaries  and  involution  of  secondary  sexual 
characters,  but  induces  brooding  behaviour  in  the  female.  Its  action 
is  comparable  with  that  of  the  galactogenic  hormone  of  the  mam- 
malian pituitary. 

The  duodenum  and  coiled  intestine  are  of  characteristic  vertebrate 
tvpe,  relatively  rather  short,  though  somewhat  longer  in  grain-eating 
birds.  The  bile  and  pancreatic  ducts  usually  open  into  the  distal  limb 
of  the  duodenum;  in  pigeons  the  left  bile-duct  enters  close  to  the 
pylorus  (Fig.  281).  There  is  a  peculiar  pair  of  coeca  at  the  junction  of 
rectum  and  intestine.  The  food  enters  these  coeca,  but  it  is  not  clear 
what  function  they  perform,  possibly  it  is  related  to  the  absorption  of 
water.  The  arrangements  of  the  cloaca  are  certainly  concerned  with 
this  end  (Fig.  282).  The  rectum  opens  into  a  coprodaeum  and  this  in 
turn  receives  a  urodaeum,  which  is  the  terminal  portion  of  the  urinary 
and  genital  ducts.  A  final  chamber,  the  proctodaeum,  opens  at  the 
anus.  The  urinary  products  are  made  solid  by  subtraction  of  water  in 
the  urodaeum  and  the  walls  of  the  other  chambers  serve  a  similar 


47°  THE  BIRDS  xvi.  22- 

purpose.  The  bursa  Fabricii  is  a  blind  sac  with  much  lymphoid  tissue, 
opening  into  the  proctodaeum;  its  function  is  probably  to  protect 
locally  against  infection  and  to  produce  lymphocytes  for  the  blood- 
stream, hence  it  has  been  called  a  'cloacal  thymus'.  Like  the  thymus, 
it  is  prominent  in  young  animals  and  usually  much  reduced  in  the 
adult. 

The  large  surface  area,  high  temperature,  and  great  activity  of  birds 
necessitate  a  high  food  intake,  especially  in  the  smaller  types.  This  is 
made  possible  by  rapid  passage  of  food  through  the  gut.  Thus  a  shrike 
(Lanius)  is  said  to  digest  a  mouse  in  3  hours,  and  hens  take  only  12-24 
hours  over  the  most  resistant  grain.  The  amount  of  food  taken  per 
day  may  reach  nearly  30  per  cent  of  the  body  weight  (6  g)  in  the  very 
small  goldcrest  (Regains)  but  is  about  12  per  cent  in  a  starling 
(Sturnus)  weighing  75  g. 

23.  Circulatory  system 

Many  of  the  features  characteristic  of  birds  depend  on  an  efficient 
circulation,  allowing  of  a  high  rate  of  metabolism,  and  hence  a  high 
and  constant  temperature.  It  is  significant  that  the  birds  and  mammals 
are  the  only  vertebrates  that  have  achieved  complete  separation  of  the 
respiratory  and  systemic  circulations,  making  possible  a  high  arteriolar 
pressure,  which  allows  materials  to  reach  the  tissues  rapidly. 

The  heart  shows  its  sauropsidan  characteristics  clearly  in  that  the 
ventral  aorta  is  split  to  its  base  into  aortic  and  pulmonary  trunks.  The 
former  arising  from  the  left  ventricle  curls  round  the  pulmonary 
trunk  to  form  a  single  right  aortic  arch.  The  heart  has  lost  the  sinus 
venosus;  as  in  mammals  no  such  extra  chamber  is  necessary  to  step 
up  the  venous  return  pressure.  The  ventricles  are  large,  especially  the 
left.  The  right  auricle  and  ventricle  are  separated  by  a  flap-like  valve, 
the  left  side  having  valves  with  chordae  tendinae,  somewhat  as  in 
mammals.  There  are  enormous  innominate  arteries  to  supply  the 
pectoral  muscles.  In  the  venous  system  there  are  renal  portal  veins. 

The  size  of  the  heart  and  rate  of  heart-beat  vary  with  the  size  and 
activity  of  the  bird,  larger  birds  having  in  general  relatively  smaller 
and  less  rapid  hearts.  In  a  turkey  the  rate  of  beat  may  be  less  than  100 
per  minute,  in  a  hen  about  300,  and  in  a  sparrow  nearly  500. 

The  red  corpuscles  of  birds  differ  from  those  of  mammals  in  being 
oval  and  nucleated.  They  carry  a  large  amount  of  a  haemoglobin  that 
gives  up  its  oxygen  suddenly  at  a  relatively  high  oxygen  tension.  The 
red  corpuscles  are  smaller  in  actively  flying  birds  than  in  the  larger 
flightless  ratites.  Haemopoetic  tissue  is  widespread  in  the  young, 


xvi.  24  R  ESPI  RAT  ION  47 1 

restricted  mainly  to  the  marrow  in  the  adult,  although  it  may  also  be 
found  in  the  liver  and  spleen.  The  white  corpuscles  are  more  numerous 
than  in  mammals.  They  include  neutrophils  laden  with  crystals,  and 
thrombocytes,  as  well  as  the  mammalian  types.  Lymphatic  tissue  is 
dispersed  rather  than  aggregated  into  nodes.  There  is  a  pair  of  lymph 
hearts  in  the  sacral  region  of  the  embryo  and  these  may  persist  in  the 
adult.  There  is  a  high  basal  metabolic  rate  and  a  temperature  con- 
siderably higher  than  that  of  mammals,  usually  about  420  C,  reaching 
nearly  45 °  C  in  some  cases.  The  means  by  which  this  is  kept  constant 
in  the  absence  of  sweat  glands  are  not  known  certainly.  Heat  loss  is 
minimized  by  the  absence  of  vascularized  extremities,  the  feet  being 
little  more  than  keratin  and  collagen.  The  formation  of  the  wing  from 
large  avascular  surfaces  has  no  doubt  been  a  large  part  of  the  secret 
of  the  success  of  birds. 

The  air-sacs  may  serve  to  conserve  heat  by  providing  an  air  cushion 
for  the  viscera,  with  perhaps  the  alternative  possibility  of  losing  heat 
in  this  way,  by  ventilation,  when  necessary.  There  is  a  system  of 
direct  arterio-venous  connexions  in  the  feet,  and  elsewhere.  The  anas- 
tomotic regions  have  powerful  muscles,  whose  contraction  closes  them 
and  forces  the  blood  through  the  capillary  system.  There  must  be  a 
whole  system  of  nervous  pathways  for  the  control  of  upward  and  down- 
ward temperature  regulation,  evolved  independently  of  that  found  in 
mammals.  At  least  one  species  (the  nightjar)  is  known  to  hibernate, 
and  certain  humming  birds,  whose  small  size  render  heat  loss  a 
serious  problem,  become  temporarily  poikilothermic  at  night. 

24.  Respiration 

Special  arrangements  are  present  to  provide  the  large  supply  of 
oxygen  necessary  for  the  active  metabolism  and  these  are  based  on  the 
plan  found  in  some  reptiles.  Beyond  the  respiratory  portion  of  the 
lung,  which  is  relatively  small,  there  are  membranous  air-sacs,  which 
are  filled  at  inspiration  and  then  sweep  the  used  air  out  of  the  lungs 
at  expiration,  thus  avoiding  the  'dead  space'  of  unrespired  air,  which 
is  considerable  in  mammals.  When  the  bird  is  at  rest  the  air-sacs  con- 
tain air  with  a  high  content  of  C02,  but  during  periods  of  activity  the 
abdominal  air-sacs  fill  with  fresh  air  containing  little  C02;  they  then 
serve  not  only  as  a  means  of  ventilating  the  lungs  but  also  for  regula- 
tion of  the  body  temperature.  The  exact  direction  of  the  air  currents 
passing  through  the  lungs  and  the  different  air-sacs  is  not  fully  under- 
stood. 

The  larynx  of  birds  is  a  small  structure  guarding  the  entrance  to  the 


472 


THE  BIRDS 


XVI.  24 


trachea.  The  latter  is  often  long  and  coiled,  perhaps  to  warm  the  air. 
The  tracheal  rings  are  bony  and  complete.  The  voice  is  produced  in 
the  syrinx,  a  slight  enlargement  at  the  lozver  end  of  the  trachea,  con- 
taining a  pair  of  semilunar  membranes  with  muscles  that  alter  the 
pitch  of  the  sound.  The  apparatus  is  simple  in  many  birds,  but  the 
muscles  are  very  complicated  in  the  singing  birds  and  are  especially 


s.cerv 


s  clav 


s.  thor 
ant 


s  Lhorpost 


s.abd. 


Fig.  283.  Diagram  of  lungs  and  air-sacs  of  pigeon,  seen  from  ventral  side  on  left, 

dorsal  on  right.  On  the  left  side  only  the  ventral  surface  of  the  lungs  and  the 

expiratory  bronchi  and  air-sacs  are  shown  (dotted).  On  the  right  are  the  inspiratory 

bronchi  and  air-sacs  (in  black). 

B.  main  bronchus;  C.  cervical  ventrobronchus;  M.  mesobronchus;    V.  vestibule;  s.abd. 

abdominal  air-sac;  s.cerv.  cervical  air-sac;  s.clav.  clavicular  air-sac  with  diverticulum  (ax.) 

in  axilla;  s. thor. ant.  and  post,  thoracic  air-sacs.  (After  Brandes  and  Ihle.) 

large  in  the  males.  Many  varieties  of  sound  are  produced,  from  simple 
cries  appropriate  to  each  sex  to  elaborate  songs.  In  many  species  the 
song  is  given  in  its  full  complexity  by  individuals  that  have  had  no 
opportunity  of  hearing  others  sing,  but  in  some  the  song  is  largely 
learnt  by  the  young  and  may  show  considerable  local  variation.  The 
voice  is  used  for  communication  in  various  ways,  including,  in  social 
birds  such  as  rooks,  the  giving  of  warning  and  the  frightening  away 
of  intruders.  The  language  may  include  as  many  as  fifteen  sounds  used 
under  different  circumstances  (chaffinch).  The  more  elaborate  song  of 
male  birds  is  used  in  courtship  both  as  a  sexual  stimulant  and  as  a 
threat  to  other  birds  invading  the  chosen  territory  (p.  503). 


xvi.  24  RESPIRATION  473 

The  lungs  are  rather  small  spongy  organs,  with  little  elasticity.  The 
air  passes  backwards  in  a  large  main  bronchus  running  through  the 
lungs  and  giving  off  branches  to  the  lung  substance,  but  continuing 
beyond  to  the  inspiratory  air-sacs  (Figs.  283  and  284).  These  are  thin- 
walled  chambers,  divided  into  two  sets,  the  posterior  inspiratory  and 
anterior  expiratory.  The  posterior,  inspiratory,  air-sacs  are  the  ab- 
dominal and  posterior  thoracic  and  they 
are  filled  by  the  air  rushing  into  them 
through  the  main  bronchus.  The  anterior 
or  expiratory  air-sacs  include  an  anterior 
thoracic,  median  interclavicular,  and  cer- 
vical, these  often  communicating  with 
spaces  in  the  bones.  At  expiration  the 
air  passes  from  the  more  posterior  sacs 
through  the  lungs  by  special  recurrent 
bronchi  into  the  anterior  sacs.  From 
these  the  air  may  be  expelled  to  the 
exterior,  return  to  the  lungs  being  pre- 
vented by  closure  of  sphincters.  In  some 
conditions,  however,  especially  in  diving 
birds,  the  air  may  be  passed  backwards 
and  forwards  through  the  lungs  several 
times,  until  all  its  oxygen  has  been  used. 
The  branches  of  the  bronchi  in  the  lungs 
do  not  end  blindly  in  alveoli,  but  make  an 
elaborate  system  of  lung  capillaries.  Air 
sweeps  through  the  larger  channels  at 
inspiration  and  expiration,  but  probably 
reaches  the  finer  capillaries  by  diffusion. 

The  mechanism  by  which  the  ventilation  is  produced  is  complicated 
and  depends  largely  on  the  movements  produced  during  locomotion. 
The  upper  surface  of  the  lung  adheres  to  the  ribs,  its  lower  surface  is 
covered  by  a  special  membrane  derived  from  the  peritoneum  and 
known  as  the  pulmonary  aponeurosis  (Fig.  285).  This  is  connected 
with  the  ribs  by  costopulmonary  muscles.  The  floor  of  the  thoracic 
air-sacs,  which  lie  below  the  lungs,  is  also  covered  by  a  fibrous  mem- 
brane, the  oblique  septum,  but  the  walls  of  the  remaining  air-sacs  are 
very  thin.  Quiet  respiratory  movements  are  produced  by  the  inter- 
costal (inspiratory)  and  abdominal  (expiratory)  muscles,  acting  upon 
the  thoracic  and  abdominal  cavities  so  as  to  enlarge  and  contract  the 
thorax,  drawing  air  in  and  out  of  the  air-sacs,  through  the  lungs.  During 


Fig.  284.  The  air-sacs  of  a  bird. 

1..  right  lung;  c.  cervical  air-sac;  ICL. 
interclavicular;  A.S.  outgrowth  into 
humerus  (h.);  A.th.  anterior  thoracic 
air-sac;  p.TH.  posterior  thoracic; 
AnD.  abdominal  air-sac;  tr.  trachea. 
(From  Thompson,  Biology  of  Birds, 
Sidgwick  &  Jackson,  Ltd.) 


474  THE  BIRDS  xvi.  24- 

flight  the  movements  of  the  pectoral  muscles  provide  the  ventilation, 
the  sternum  moving  towards  and  away  from  the  vertebral  column. 

25.  Excretory  system 

The  kidneys  are,  of  course,  metanephric  and  are  relatively  large, 
elongated,  and  lobulated.  They  are  provided  with  venous  blood  by 


-thas 


obi-- 


rpr 


ms/ 


st 


Fig.  285.  Diagram  of  transverse  section  through  the  thorax  of  a  bird. 

ec.  Excurrent  passage  from  lung  to  air-sac  through  pulmonary  aponeurosis;  h.  heart; 
lis.  left  liver-sac;  Ig.  lung;  m.  muscle;  ms.  mesentery  below  oesophagus;  obi.  oblique  septum; 
p.  pericardial  coelom;  pa.  pulmonary  aponeurosis;  pic.  reduced  pleural  coelom;  r.  dorsal 
rib;  re.  recurrent  bronchus  from  sac  to  lung;  rl.  right  lobe  of  liver;  rpr.  right  pulmonary 
recess;  St.  sternum;  thas.  posterior  thoracic  air-sac;  vr.  sternal  rib.  (From  Goodrich.) 

the  renal  portal  veins  and  arterial  blood  from  the  renal  arteries.  The 
arrangement  is  essentially  as  in  amphibia  and  reptiles,  with  the  renal 
arteries  supplying  the  glomeruli  and  the  portal  veins,  which  break  up 
into  inter-lobular  branches,  sending  blood  to  the  renal  tubules,  whence 
it  is  collected  into  a  central  intra-lobular  vein.  It  is  not  certain,  how- 
ever, exactly  how  the  system  operates,  and  it  is  possible  that  much  of 
the  blood-flow  is  directly  from  the  renal  portal  to  the  renal  veins, 
making  little  contact  with  the  tubule  walls. 

The  excretory  system  is  highly  specialized  for  water-saving.  For 
this  purpose  the  end  product  of  nitrogenous  metabolism  is  the  rela- 
tively insoluble  uric  acid,  synthesized  in  the  liver,  probably  from 
ammonium  lactate.  After  excretion  by  the  kidney  the  urine  is  con- 
centrated in  the  cloacal  chambers  and  the  uric  acid  precipitates  as 


XVI.  26 


REPRODUCTION 


475 


whitish  granules.  There  is  no  urinary  bladder  in  the  adult  bird.  More 
soluble  excretory  end  substances,  such  as  urea,  would  reach  toxic  con- 
centrations. The  glomeruli  are  much  more  numerous  and  smaller 
than  those  of  mammals.  The  urinary  tubules  effect  a  considerable  con- 
centration of  the  urine  by  means  of  long  loops  of  Henle.  The  viscous 
fluid  that  enters  the  urodaeum  then 
passes  up  into  the  coprodaeum, 
where  further  water  is  abstracted, 
and  the  mixed  faeces  and  urinary 
products  are  then  excreted  as  the 
characteristic  semi-solid  white 
guano.  The  water-conservation  sys- 
tem is  certainly  very  effective,  and 
some  desert-living  birds  are  said  to 
be  able  to  survive  for  many  weeks 
without  water.  In  this  respect  the 
birds  have  freed  themselves  from 
the  original  aquatic  environment  to 
a  remarkable  degree. 


RR.OVD 
OPUR 


OPOVD 
CL 


Fig.  286.    Female  reproductive  organs 
of  a  hen. 

ov.  ovary;  K.  kidneys;  f.t.  funnel;  ovd. 
oviduct;  m.ovd.  muscular  part  of  oviduct; 
OP. OVD.  opening  of  oviduct;  ur.  ureters; 
op.ur.  opening  of  right  ureter;  r.r.ovd. 
rudimentary  right  oviduct;  cl.  cloaca.  (From 
Thompson,  Biology  of  Birds,  Sidgwick  & 
Jackson,  Ltd.) 


26.  Reproductive  system 

The  testis  consists  of  coiled 
tubules  of  the  usual  type,  joining  to 
form  a  long  epididymis  and  vas 
deferens,  opening  into  the  urodaeum 
by  an  erectile  papilla  that  is  the  only 
copulatory  organ  of  most  birds. 
During  copulation  the  proctodaea 
of  male  and  female  are  everted  and 
pressed  together,  so  that  the  sperm 
is  ejaculated  direct  into  the  female  urodaeum  and  finds  its  way  up 
the  oviduct.  A  definite  penis  (and  also  clitoris)  is  found  in  ratites, 
anseriformes,  and  a  few  other  birds.  The  condition  of  the  testis  and 
its  ducts  varies  greatly  with  the  time  of  year,  the  weight  of  the  gland 
being  as  much  as  1,000  times  greater  in  the  breeding-season  than  it  is 
in  the  non-breeding,  when  it  contains  only  spermatogonia. 

The  provision  of  material  sufficient  for  the  development  of  a  warm- 
blooded creature  is,  of  course,  made  possible  in  birds  by  the  extremely 
yolky  eggs,  so  large  that  they  allow  room  for  development  of  only  one 
ovary,  nearly  always  the  left  (Fig.  286).  The  right  ovary  remains  present 
as  a  rudiment  and  if  the  left  is  destroyed  by  operation  or  disease  the 


476 


THE  BIRDS 


xvi.  26- 


right  is  able  to  differentiate,  but  then  forms  not  an  ovary  but  a  testis. 
Complete  sex  reversal  can  thus  occur,  at  least  in  some  races  of 
domestic  fowl,  and  the  transformed  bird  may  acquire  cock  plumage 
and  tread  and  fertilize  hens  (Fig.  287).  Sex  reversal  rarely,  if  ever, 
takes  place  in  the  opposite  direction.  We  must  suppose  that  there  is 
some  switch  over  in  the  balance  of  male  and  female  determining 


Fig.  287.  Secondary  sexual  characters  of  the  fowl  (Gallus). 

Left  cocks,  right  hens. 

A,  normal;   B,  castrated;   C,  cock  with  implanted  ovary  and  hen 

with  implanted  testis.  (After  Zawadowsky.) 

processes,  taking  place  relatively  early  in  the  case  of  normal  definitive 
males  but  later  on  in  life  also  in  'females',  so  that  all  birds  become 
potentially  'male'  at  the  end  of  their  life. 

Of  the  large  number  of  oocytes  only  few  ripen  to  make  the  enormous 
follicles.  After  each  follicle  has  burst  it  quickly  regresses;  there  is  no 
'corpus  luteum'. 

The  egg  is  taken  up  by  the  ciliated  and  muscular  funnel  of  the  left 
oviduct,  and  passes  down  a  tube  with  circular  and  longitudinal  muscles 
and  a  glandular,  ciliated  mucosa.  The  albumen  of  the  egg  is  produced 
by  long  tubular  glands,  opening  to  the  lumen.  The  oviduct  has  various 


xvi.  27  BRAIN  477 

parts,  the  upper  secreting  mainly  albumen,  the  lower  producing  the 
shell,  and  the  lowest  mucus,  to  assist  the  act  of  laying.  The  blue  back- 
ground colour  of  the  egg  (oocyanin)  is  produced  during  shell-forma- 
tion in  the  upper  part  of  the  tube ;  spots  of  red-brown  ooporphyrin  are 
added  lower  down.  The  pigments  are  derived  from  the  bile,  ultimately 
from  haemoglobin. 

As  much  as  a  third  of  the  weight  of  calcium  in  the  whole  skeleton 
is  needed  for  the  shells  of  the  two  eggs  laid  by  a  pigeon.  A  reserve  is 
collected  as  the  ovarian  follicles  mature.  The  oestrogen  they  produce 
increases  the  uptake  of  calcium  from  the  food  and  stimulates  its 
deposition  in  the  bones.  After  ovulation  the  oestrogen  level  falls,  the 
calcium  is  mobilized  from  the  bones,  and  its  concentration  in  the 
blood  becomes  very  high,  until  used  by  the  eggs. 

27.  The  brain  of  birds 

The  brain  is  larger  relative  to  the  body  in  birds  than  in  any  other 
vertebrates  except  mammals  (Fig.  288),  and  there  is  no  doubt  that  one 
result  of  the  high  temperature  has  been  to  allow  opportunity  for  an 
elaborate  nervous  organization  and  complicated  behaviour.  Unfortu- 
nately we  have  little  information  about  the  w^ay  in  which  the  large 
masses  of  tissue  of  the  brain  function ;  they  are  certainly  different  from 
anything  found  in  mammals.  There  are  considerable  differences  in  the 
development  of  the  parts  in  various  birds,  for  instance,  the  forebrain  is 
especially  large  in  the  rooks  and  crows  (Corvus)  and  in  the  parrots,  the 
behaviour  of  which  also  shows  signs  of  outstanding  'intelligence'. 

In  the  spinal  cord  the  most  characteristic  feature  is  the  relatively 
small  size  of  the  dorsal  funiculi,  and  their  nuclei  in  the  medulla  are 
also  small.  Evidently  the  sense  of  touch  is  less  well  developed  over  the 
body  than  it  is  in  mammals,  perhaps  less  than  in  reptiles.  No  doubt 
movement  of  the  feathers  provides  impulses  leading  to  reflex  actions, 
but  it  is  not  surprising  that  the  loose  covering  does  not  allow  elaborate 
organization  of  the  sense  of  touch.  The  finer  senses  of  birds  are 
restricted  to  the  eyes,  ears,  and  bill.  On  the  other  hand,  there  are  large 
spino-cerebellar  tracts,  presumably  proprioceptive  and  concerned  with 
the  delicate  adjustments  necessary  for  flight.  The  spinal  cord  is  con- 
trolled by  large  efferent  tracts  from  the  brain,  including  cerebello- 
spinal, vestibulo-spinal,  and  tecto-spinal  pathways.  There  is  no  direct 
tract  from  the  forebrain  to  the  spinal  cord,  but  the  influence  of  the 
large  corpora  striata  is  probably  exercised  through  fibres  running  to 
the  red  nucleus  and  tegmentum  of  the  midbrain,  from  which  others 
pass  to  the  cord. 


478 


THE  BIRDS 


xvi.  27 


XII 
IX,X,XI 
Vllanc/VIII 


The  cerebellum  is  also  large  (Fig.  288),  a  state  of  affairs  perhaps 
connected  with  the  precise  timing  and  control  of  movement  in  all 
planes  of  space  during  flight.  Besides  large  spino-cerebellar  and 
vestibulo-cerebellar  pathways  there  are  also  tecto-cerebellar  and 
strio-cerebellar  tracts,  the  latter  perhaps  conducting  in  both  directions. 
The  effect  of  the  cerebellum  on  other  parts  of  the  brain  is  exercised 
through  cerebellar  nuclei,  the  cells  of  which  give  origin  to  the  cerebello- 
spinal tract. 

The  optic  tracts  are  completely 
crossed  and  end  mainly  in  the 
midbrain,  as  in  lower  verte- 
brates. However,  a  considerable 
portion  of  the  optic  tracts  passes 
to  the  thalamus,  and  the  mid- 
brain and  thalamus  are  both 
highly  developed  and  have  inti- 
mate and  reciprocal  connexions 
with  the  striata  of  the  cerebral 
hemispheres.  The  optic  lobes 
also  receive  ascending  fibres  from 
the  trigeminal  nuclei  and  from 
the  spinal  cord.  Their  efferent 
pathways  run  to  the  oculomotor 
nuclei,  to  the  underlying  teg- 
mentum, and  to  the  medulla  and 
spinal  cord.  Evidently  they  play 
a  large  part  in  correlating  visual  with  other  afferent  impulses.  The 
thalamus  is  large  and  its  dorsal  part  well  differentiated  into  nuclei. 
It  receives,  besides  optic  fibres,  also  projections  from  tactile,  pain, 
temperature,  and  perhaps  auditory  sources.  There  are  large  thalamo- 
striatal  tracts,  probably  conducting  in  both  directions.  The  ventral 
thalamus  receives  impulses  from  the  striatum  and  sends  them  to  the 
tegmentum,  this  being  the  main  efferent  pathway  of  the  forebrain. 
The  hypothalamus  is  rather  small,  probably  because  of  the  reduction 
in  the  olfactory  system. 

The  cerebral  hemispheres  are  much  larger  than  any  other  part  of  the 
brain  and  show  an  exaggeration  of  the  condition  found  in  the  lizards 
(Fig.  289).  The  ventro-lateral  portions  are  enormously  developed, 
whereas  the  medial  ventral  walls  are  thin  and  the  pallium  is  quite 
small,  thin,  and  not  folded.  The  olfactory  regions  of  the  brain  are 
small,  including  the  hippocampus. 


Fig.  288.  Brain  of  a  duck  (Anser) 

c.h.  cerebral  hemisphere;  cereb.  cerebellum;  cp. 

epiphysis;/?,  flocculus;  h.  hypophysis;  o./.  optic 

lobe;   olf.  olfactory  lobe;   str.   striatum;   1I-XII, 

cranial  nerves.  (After  Butschli  and  Ihle.) 


XVI.  28 


FUNCTION  OF  BRAIN 


479 


The  corpus  striatum  is  a  huge  solid  mass  of  tissue,  receiving  projec- 
tions forward  from  the  thalamus  and  sending  them  back  through  the 
latter,  to  the  midbrain  roof  and  floor,  to  the  cerebellum,  and  thence  to 
the  medulla  and  spinal  cord.  This  very  characteristic  striatum  can  be 
divided  into  various  regions.  The  part  representing  the  'original'  or 
lower  striatum  is  called  the  'paleostriatum' ;  other  parts,  lying  above 
this,  are  known  as  the  mesostriatum  and  hyperstriatum. 


Fig.  289.  Transverse  section  through  forebrain  of  sparrow. 

hip.  hippocampus;  hyp.str.  hyperstriatum;  mes.str.  mesostriatum;  n.pr.  preoptic  nucleus; 
pal.str.  palaeostriatum;  pall,  pallium.  (Partly  after  Kappers,  Huber,  and  Crosby.) 

28.  Functioning  of  the  brain  in  birds 

Loss  of  one  complete  hemisphere  by  a  pigeon  is  not  followed  by  any 
gross  motor  defect  or  asymmetry  of  movement.  This  suggests  that  the 
corpora  striata  do  not  control  individual  muscle  movements,  which 
agrees  with  the  fact  that  there  is  no  direct  pathway  from  the  forebrain 
to  the  spinal  cord,  corresponding  to  the  pyramidal  tract  of  the  mam- 
mals. Electrical  stimulation  does  not  produce  movements;  the  striata 
are  'silent  areas'  to  stimulation. 

Complete  removal  of  both  hemispheres  does  not  reduce  a  pigeon  to 
a  helpless  state.  The  animal  can  still  maintain  its  temperature  and  its 
balance  and  can  feed  itself  if  the  food  is  placed  near  to  it.  However,  a 
bird  so  treated  is  far  from  normal.  It  may  show  a  lack  of  activity, 
remaining  inert  for  long  periods,  and  then  become  aimlessly  restless 
for  a  while.  Evidently  the  normal  balance  of  excitation  and  inhibition 
has  been  upset.  Deficiencies  in  vision  can  be  detected  in  birds  with 
various  portions  of  the  cerebral  hemispheres  removed,  and  the  mating 
and  nestine  behaviour  are  also  affected.  Even  small  removals  of  the 


480  THE  BIRDS  xvi.  28 

cortex  and  top  of  the  striatum  are  said  to  prevent  incubation  (though 
not  copulation)  and  with  deeper  lesions  the  whole  process  of  rearing 
the  young  becomes  impossible. 

These  observations  on  the  functions  of  the  brain  of  pigeons  may  not 
be  applicable  to  birds  in  general.  The  forebrain  is  larger  in  many  other 
birds  than  in  the  pigeon,  and  there  is  some  evidence  that  in  the  parrots 
movements  and  even  'phonation'  can  be  elicited  by  electrical  stimula- 
tion of  the  corpora  striata,  which  are  especially  large.  Removal  of  one 
particular  area  is  said  to  lead  to  disturbances  of  'speech'. 


B 


B 

Fig.  290.  A.  Models  used  by  Lorenz  and  Tinbergen.  Small  birds  reacted  with 

escape  movements  to  the  models  marked  +  .  B.  The  model  induced  escape  reactions 

when  towed  to  the  right  ('hawk')  but  not  when  towed  to  left  ('goose'). 

(From  Tinbergen.) 

It  seems,  therefore,  that  the  large  masses  of  nerve-cells  in  the  striata 
are  concerned  in  some  way  with  the  elaboration  of  the  more  complex 
acts  of  behaviour.  This  is  a  very  vague  statement,  but  is  the  best  that 
we  can  give  at  present.  It  may  be  that  further  investigation  of  the 
reciprocal  actions  of  striatum  and  thalamus  will  show  whether  the 
essentials  of  their  action  consist  in  some  reverberating  or  scanning 
systems  and  whether  these  actions  are  at  all  similar  to  those  in  the 
forebrain  of  mammals.  The  fact  that  the  striatum  consists  of  solid 
masses  of  tissue  suggests  that  the  arrangement  does  not  depend,  as 
does  the  mammalian  cerebral  cortex,  on  the  projection  of  patterns  of 
excitation  onto  an  extended  surface. 

Birds  are  usually  said  to  show  more  stereotyped  patterns  of  instinc- 
tive behaviour  than  primitive  mammals.  Once  they  have  embarked  on 
a  line  of  action,  even  a  complex  one  like  nest-building>  they  are  sup- 
posed to  pursue  it  in  a  given  manner,  without  ability  10  adapt  them- 
selves to  unusual  happenings.  Watching  the  exploratory  behaviour  of 
a  robin  or  a  tit  it  is  difficult  to  feel  that  the  existence  of  this  difference 


xvi.  28  BEHAVIOUR  481 

is  adequately  proved,  but  whatever  distinction  exists  is  presumably  a 
reflection  of  the  difference  between  the  functions  of  large  masses  and 
spread-out  sheets  of  nervous  tissue.  Certainly  birds  can  count  as  well 
as  rodents,  and  their  performance  in  mazes  and  puzzle  boxes  is  at 
least  comparable  to  that  of  most  mammals. 

There  are  many  signs  that  a  suitable  initial  stimulus  sets  off  in  the 
bird  a  whole  train  of  behaviour,  organized  from  within.  On  the  other 
hand,  inappropriate  stimuli  may  sometimes  set  off  a  reaction,  as  if  the 
'keys'  to  these  cerebral  'locks'  were  not  very  elaborate  or  specific.  A 


Fig.  291.  Pintail  ducks  (Anas  acuta).  Males  displaying  dark  brown  feathers 
of  neck  with  white  bands  on  either  side.  (From  Tinbergen,  after  Lorenz.) 

robin  held  in  the  hand  may  burst  into  song,  cock  ostriches  frightened 
by  an  aeroplane  fall  to  the  ground  in  their  characteristic  sexual  display. 
Birds  frightened  or  disturbed  may  proceed  to  the  actions  of  bathing, 
preening,  feeding,  or  drinking,  performed  in  a  ritual  and  cursory 
manner  for  a  long  time.  Such  displacement  activities  show  that  the 
organization  of  the  bird's  nervous  system,  like  that  of  a  mammal,  pro- 
vides for  some  strange  deviations,  whose  study  may  reveal  much  about 
the  method  of  working  of  the  brain. 

Many  complex  forms  of  behaviour  are  responses  to  only  limited 
parts  of  the  natural  stimulus  situation.  Thus  when  the  models  shown 
in  Fig.  290  were  towed  above  certain  young  birds,  only  the  models 
marked  with  a  cross  induced  escape  reactions:  apparently  the  con- 
figuration of  the  short  neck  is  the  essential  feature.  Much  of  the 
elaborate  social  life  of  birds  depends  on  such  sign  stimuli  displayed 
by  one  bird  (the  'actor')  and  serving  as  releasers  setting  off  particular 
actions  or  trains  of  action  in  another  bird  (the  'reactor').  Many  of  the 
elaborate  forms  of  display  evolved  by  birds  (p.  497)  are  releasers  of 
this  sort  (Fig.  291),  and  structures  and  actions  on  the  part  of  the 
young  release  the  appropriate  behaviour  of  the  parent.  The  red  breast 


482  THE  BIRDS  xvi.  28- 

of  the  robin  (Erithacus)  is  the  agent  that  releases  attacks  by  other  birds 
(Fig.  292).  Similar  phenomena  are  known  in  fishes  and  other  verte- 
brates (p.  225),  and  it  remains  to  be  shown  whether  they  can  be  attri- 
buted to  any  single  or  particular  neural  basis. 

29.  The  eyes  of  birds 

Birds  depend  more  on  their  eyes  than  on  the  other  senses;  they  are 
perhaps  more  fully  visual  than  are  any  other  animals.  The  eyes  are 
extremely  large :  those  of  hawks  and  owls,  for  instance,  may  be  abso- 
lutely larger  than  in  man.  The  shape  is  not  spherical,  the  lens  and 


Fig.  292.  The  red  tuft  of  feathers  is  attacked  by  male  robins  holding  territory,  but 
the  complete  juvenile  bird  (withou   red)  is  left  alone.  (After  Lack,  from  Tinbergen.) 

cornea  bulge  forwards  in  front  of  the  posterior  chamber,  this  form 
being  maintained  by  a  ring  of  bony  sclerotic  plates  (Fig.  293).  In  most 
birds  the  whole  eye  is  thus  broader  than  it  is  deep,  but  in  those  with 
very  acute  sight  it  is  longer,  and  in  some  eagles  and  crows  becomes 
almost  tubular.  The  great  distance  between  lens  and  retina  allows 
broadening  of  the  image,  thus  improving  the  fine  two-point  discrimin- 
ation that  is  needed  by  these  diurnal  birds.  The  shape  of  the  back  of 
the  eye  is  such  that  'the  retina  lies  almost  wholly  in  the  image  plane, 
so  that  all  distant  objects  within  the  visual  angle  are  sharply  focused 
on  the  photosensitive  cells,  whereas  in  the  human  eye  this  is  only 
true  of  objects  lying  close  to  the  optic  axis'  (Pumphrey;  Fig.  294). 
The  lens  is  usually  soft  and  accommodation  is  effected  by  changing 
its  shape,  and  especially  the  curvature  of  its  anterior  surface,  by  the 
pressure  upon  it  of  the  ciliary  muscles  behind.  These,  like  the  iris 
muscles,  are  striated,  presumably  allowing  for  the  quick  accommoda- 
tion necessary  in  a  rapidly  moving  bird,  though  it  must  not  be  for- 
gotten that  these  muscles  are  also  striated  in  lizards.  The  ciliary 
muscle  is  characteristically  divided  into  'anterior'  and  'posterior'  por- 
tions, the  muscles  of  Crampton  and  Briicke  (Fig.  293).  The  latter 
draws  the  lens  forward  into  the  anterior  chamber  so  that  since  the 


ACCOMMODATION 


XVI.  29  A^V^UiVli\lUJL»/\  1  IKJ1S  483 

shape  of  the  eye  is  fixed  by  the  sclerotic  plates,  the  lens  becomes  more 
curved  and  hence  accommodated  for  near  vision;  contraction  of  the  iris 
sphincter  assists  in  the  process.  Crampton's  muscle  is  so  arranged  as 
to  pull  on  the  cornea,  shortening  its  radius  and  further  assisting  in 


lb) 


(3) 


tenacular  Ligament:  v     /  / 
Cramp  tons  m.       \/' 

scleral  ossicle 


lens 


Bruckes  m. 


cdiary 
body 


zonule 


Fig.  293.  The  mechanism  of  accommodation  in  a  bird's  eye; 

the  positions  during  near  vision  are  shown  dotted,  b.  The  lens  of 

the  cormorant's  eye  at  rest  (full  line)  and  fully  accommodated 

(dotted  line).  (From  Pumphrey,  after  Franz  and  Hess.) 


■cornea- 


scleral  ossicle 


pecten 


Fig.  294.  Diagrams  of  right  eye  of  man  and  left  eye  of  swan  to  show  the  difference 
in  shape.  The  position  of  the  image  plane  in  man  is  shown  dotted;  it  lies  behind 
the  retina  except  near  the  centre.  The  arrows  point  forward.  (From  Pumphrey.) 

accommodation.  This  double  method  of  active  accommodation  for 
near  vision  is  most  fully  developed  in  diurnal  predators,  such  as  the 
hawks,  less  so  in  night-birds.  In  aquatic  birds  Crampton's  muscle  is 
reduced,  and  the  cornea  is  of  little  importance  in  image-formation. 
Special  arrangements  are  found  in  diving  birds,  for  instance  in  the 
cormorants  Briicke's  muscle  is  large  and  there  is  a  very  powerful  iris 
muscle,  which  assists  the  ciliary  muscles  to  give  the  great  change  in 
shape  of  the  soft  lens,  allowing  accommodation  of  40-50  diopters  (about 


4«4  THE  BIRDS  xvi.  29 

10  in  man).  The  kingfishers  are  said  to  possess  an  amazing  arrangement 
of  double  foveas,  placed  at  different  distances  from  the  lens,  so  that 
as  the  bird  dives  under  water  the  image  is  transferred  from  one  fovea 
to  the  other  without  any  change  in  the  dioptric  apparatus.  These  details 


Herring  Gull 
(Larus) 


Shearwater 
rPuffinus) 


Great:  Bustard 
(Otis) 


Coot 
(Fulica) 


Ostrich 
(Struthio) 


Cormorant 
(Phalacrocorax) 


Humming  Bird 
fCalypte) 


Shrike 
fLanius) 


King  Fisher 
(filcedo) 


Fig.  295.  The  appearance  of  the  retina  of  various  birds  as  seen  with  an 

ophthalmoscope  through  the  pupil. 

cm.  central  area;/,  fovea;  p.  pecten;  t.a.  temporal  area.  (After  Wood,  from  Pumphrey.) 

of  the  visual  system  show,  like  so  many  other  features  of  bird  ana- 
tomy, how  readily  the  structure  conforms  to  special  habits  of  life. 

The  retina  of  day-birds  consists  largely  but  not  wholly  of  cones; 
these  animals  are  more  fully  diurnal  than  is  man.  The  high  resolving 
power  and  hence  high  powers  of  discrimination  and  of  movement- 
detection  depend  on  the  great  density  of  the  cones,  as  many  as 
1  million  to  each  square  millimetre  in  the  fovea  of  a  hawk,  three  times 
denser  than  in  man.  Nocturnal  birds,  on  the  other  hand,  have  retinas 
composed  mainly  or  completely  of  rods,  and  the  differences  between 
the  behaviour  of  these  two  types  of  eye,  found  in  birds  as  in  mammals, 
have  been  a  powerful  support  for  the  duplicity  theory  of  vision.  There 
are  usually  one  or  more  areae,  regions  of  the  retina  consisting  of  tightly 


xvi.  29  RETINA  485 

packed  receptors.  In  birds  that  live  on  the  sea,  in  the  desert,  or  other 
open  spaces  the  area  often  has  the  form  of  an  elongated  horizontal  band 
(Fig.  295),  whereas  in  tree-living  birds  it  is  circular.  Some  birds  have 
two  areae,  a  central  one  in  the  optic  axis  and  a  second  placed  on  the 
temporal  surface  of  the  eye,  so  that  the  image  of  objects  in  front  of  the 
head  falls  on  the  temporal  areae  of  both  eyes.  This  arrangement  is 
common  in  birds  that  follow  moving  prey  (shrike,  Lanius)  or  for 


Fish  (Serrjnus) 

fovea 
(dFcer  Kahmjnn) 


Reptile  [Chameleon) 

Fovea 
(aFter  Detwiler) 


uila  \    X  Aquila 

central  fa  ea      \      temporal  Fovea 

(after  Polijak)      \    (after  Pol  yak) 


Alcedo 
central  fovea 
(after  Kolmerj  "<~ 

(after  Detwiler) 


Fig.  296.  Forms  of  the  fovea  in  various  vertebrates,  showing 
the  development  from  moderately  to  sharply  convexiclivate  types 
in  foveas  adapted  for  detection  of  movement,  but  flattening  of 
the  fovea  where  there  is  binocular  vision.  (From  Pumphrey.) 

some  other  reason  require  accurate  perception  of  distance  (swallows, 
humming-birds;  the  latter  feed  their  young  on  insects  caught  on  the 
wing).  The  density  of  the  cones  is  so  high  in  diurnal  birds,  even  outside 
the  areae,  that  they  probably  obtain  a  good  detailed  picture  in  all 
directions.  They  do  not,  therefore,  scan  the  world  with  the  central 
area  of  the  retina  as  we  do;  indeed,  the  eyes  move  relatively  little. 
Instead  the  bird  is  able  to  detect  very  small  movements  anywhere  in 
its  surroundings.  The  bird's-eye  view  usually  lacks  stereoscopic  solidity 
and  it  is  possible  that  in  compensation  for  this  the  animals  appreciate 
distance  by  movements  of  the  intrinsic  eye-muscles.  The  familiar 
cocking  of  the  head  of  a  bird  before  pecking  may  be  its  means  of 
judging  distance. 

As  in  man  there  is  often  within  the  central  area  of  the  eye  a  fovea 
or  pit,  and  in  many  birds  the  sides  of  this  pit  are  steeply  curved  (Fig. 
296).  Walls  has  suggested  that  since  the  vitreous  humour  and  retina 
differ  in  refractive  index  this  curvature  serves  to  magnify  the  image 


486  THE  BIRDS  xvi.  29 

and  increase  acuity.  Pumphrey  points  out  that  any  such  advantage 
would  be  counteracted  by  the  aberration  introduced  and  he  makes  the 
suggestion  that  this  disturbance  of  the  picture  by  the  'convexiclivate' 


x 


iT 


^ 


Fig.  297.  Effect  of  refraction  produced  by  the  curvature  of  the  fovea 
of  the  golden  eagle.  An  image  of  the  form  shown  with  dotted  lines  is 
distorted  by  the  fovea  to  the  form  shown  in  solid  lines.  The  circle 
represents  a  radius  of  io/j.  at  the  centre  of  the  fovea.  (From  Pumphrey.) 


Fig.  298.  Distortion  by  the  fovea.  The  lines  represent  the  successive  images  at 
equal  time-intervals  of  the  boundary  of  a  regular  object  when  the  object  moves 
steadily  across  the  visual  field.  If  this  picture  is  viewed  at  7  m  the  area  of  irregu- 
larity subtends  an  angle  about  equal  to  the  angle  subtended  by  the  central  part  of 
the  hawk  fovea.  It  will  be  found  that  the  irregularity  is  very  evident  to  the  human 
eye  at  this  distance  though  the  lines  are  resolvable  with  difficulty. 
(From  Pumphrey.) 

fovea  is  itself  an  advantage,  improving  the  power  of  fixation  and  sensi- 
tivity to  movement,  at  the  sacrifice  of  acuity.  Such  an  arrangement 
would  serve  to  emphasize  angular  displacements,  transforming  a 
radially  symmetrical  image  into  an  asymmetrical  one,  except  when 
there  is  coincidence  between  the  axes  of  symmetry  of  the  fovea  and  of 


xvi.  29  COLOUR  DISCRIMINATION  487 

the  object  (Figs.  297  and  298).  Foveas  with  steep  sides  are  found  in 
birds  of  prey,  kingfishers,  and  others  that  have  very  high  powers  of 
detecting  movement;  a  similar  but  less  pronounced  arrangement  is 
found  in  fishes  and  reptiles.  It  is  probable  that  the  primitive  functions 
of  the  eyes  were  fixation  and  detection  of  movement,  rather  than  reso- 
lution of  detail  and  recognition  of  patterns.  Some  birds  have  one  con- 
vexiclivate  and  one  flatter  fovea  (Figs.  295  and  296),  the  latter  being  on 
the  temporal  surface  of  the  retina  and  used  in  binocular  vision.  The 
fovea  is  also  flat  in  the  retinae  of  primates  with  binocular  vision;  evi- 
dently the  optical  errors  of  a  curved  fovea  cannot  be  tolerated  where 
there  is  fusion  of  the  two  retinal  images. 

Birds  undoubtedly  discriminate  colours,  apparently  on  a  trichro- 
matic basis  similar  to  that  of  mammals.  No  other  animals,  except 
perhaps  primates,  show  such  responsiveness  to  colour  in  their 
surroundings,  including  the  food  and  other  members  of  the  species. 
In  animals  that  move  so  freely  recognition  and  attraction  of  the  sexes 
is  more  efficiently  performed  in  this  way  than  by  touch  or  odour. 
The  cones  of  birds  often  contain  red  and  yellow  droplets,  which  may 
heighten  visual  acuity  by  reducing  the  effects  of  chromatic  aberration. 
The  droplets  in  the  central  area  are  always  yellow.  The  presence  of 
droplets  of  various  colours  in  adjacent  cones  may  also  increase  powers 
of  discrimination.  Sometimes  the  droplets  are  so  arranged  as  to  allow 
accentuation  of  different  contrasts  in  the  parts  of  the  visual  field.  The 
lower  part  of  the  pigeon's  retina  contains  red,  the  upper  yellow  filters, 
increasing  the  contrast  of  blues  and  greens  respectively,  as  required 
for  vision  against  the  sky  in  the  one  case  and  the  ground  in  the  other. 
There  have  been  many  investigations  of  the  distribution  of  sensitivity 
in  the  retina;  probably  many  birds  are  rather  insensitive  to  the  blue 
end  of  the  spectrum.  There  is  no  truth  in  the  suggestion  that  the  eyes 
are  sensitive  to  infra-red  radiation. 

Although  the  eyes  of  some  birds  are  directed  forwards,  so  that  their 
fields  overlap,  they  are  said  not  to  have  binocular  vision  and  decussa- 
tion of  the  optic  tracts  is  complete.  Perception  of  distance,  a  very 
important  function  for  the  bird,  must  be  performed  in  some  other 
manner.  In  many  birds  the  eyes  are  directed  sideways,  and  the  fields 
of  view  may  even  overlap  behind  the  head,  for  example  in  waders. 
This  may  serve  to  give  warning  of  predators.  Many  functions  have 
been  suggested  for  the  most  enigmatic  organ  of  the  bird's  eye,  the 
pecten,  a  pleated  highly  vascular  fold,  projecting  from  the  retina  into 
the  vitreous.  It  is  possible  that  the  irregular  shadow  cast  by  this  organ 
provides,  as  it  were,  numerous  small  blind  spots  and  hence  by  a 


4«S 


THE  BIRDS 


xvi.  29- 


stroboscopic  action  increases  the  number  of  on-and-off  effects  pro- 
duced by  a  small  object  in  the  visual  field,  increasing  contrast  and 
allowing  detection  of  its  movement.  This,  however,  is  only  one  of  the 
numerous  suggestions  about  the  function  of  the  pecten,  and  the  only 
real  support  for  the  idea  is  that  the  body  is  large  and  much  pleated  in 
predatory  birds,  which  detect  minute  movements  at  great  distances, 


Fig.  299.  Tracing  of  the  shadow  of  the  pecten  on  the  retina 
in  various  birds.  (After  Pumphrey  and  Menner.) 

and  is  small  and  smooth  in  nocturnal  birds  (Fig.  299).  However,  it  is 
almost  certain  that  the  original  function  of  the  pecten  was  to  bring 
nourishment  to  the  vitreous  and  retina.  It  has  often  been  suggested 
that  the  pecten  is  in  some  way  connected  with  accommodation;  it  is 
not  likely  that  it  actually  assists  in  focusing,  for  instance,  by  pressing 
forward  the  lens,  and  no  changes  have  been  seen  in  it  during  accom- 
modation. However,  it  might  possibly  assist  by  adjusting  the  intra- 
ocular pressure,  which  must  be  increased  by  the  extensive  changes  in 
the  lens  during  accommodation. 

30.  The  ear  of  birds 

Both  vestibular  and  auditory  parts  of  the  ear  are  well  developed  in 
birds.  The  former  are  not  known  to  possess  special  peculiarities,  but 
the  large  connexions  with  the  cerebellum  suggest  great  importance  in 
the  operations  of  flight,  presumably  especially  by  the  semicircular 
canals.  There  is  a  distinct  cochlea,  slightly  curved  and  especially  well 


xvi.  30  EAR  489 

developed  in  owls  and  in  parrots  (Fig.  300).  In  this  there  is  a  basilar 
membrane,  with  fibres  increasing  in  length  towards  the  tip  and  carry- 
ing an  organ  of  Corti  with  hair-cells  in  contact  with  a  tectorial  mem- 
brane (Fig.  301),  as  in  mammals.  At  the  tip  of  the  cochlea  is  a  special 
sensory  region,  the  lagena,  similar  to  that  of  lower  vertebrates  and 
perhaps  responsible  for  reaction  to  lower  notes,  the  basilar  membrane 


Bind 


Mammal 


Fig.  300.  Labyrinths  of  various  vertebrates,  to  show 

varying  development  of  cochlea  (c)  and  lagena  (l). 

s,  saccule;  u.  utricle.  (From  v.  Frisch.) 

responding  to  the  higher  frequencies.  Birds  are  known  to  be  more 
sensitive  to  distant  gunfire  and  other  low-frequency  vibrations  than  is 
man.  Transmission  of  vibration  from  the  tympanum  to  the  inner  ear 
is  effected  by  the  columella  auris,  derived  from  the  cartilages  of  the 
hyoid  arch.  The  inner  portion  of  the  columella  is  rod-like  (stapes),  but 
the  outer  end  makes  contact  with  the  tympanum  by  means  of  three 
processes,  of  somewhat  irregular  shape. 

Hearing  is,  of  course,  acute  and  the  song-birds  must  be  able  to  dis- 
criminate between  simple  tunes;  some  of  them  are  surprisingly  good 
mimics.  Ability  to  localize  sound  is  high  and  owls  and  other  night- 
birds  probably  find  their  prey  largely  by  ear.  For  the  purpose  of 
direction-finding  they  have  developed  an  asymmetrical  arrangement 
of  the  ear  cavities  (Strix)  or  asymmetrical  external  ears  (Asio).  A  few 
birds  that  live  in  caves  have  the  power  of  avoiding  obstacles  by  echo- 
location  (Steatornis,  the  oil  bird,  Collocalia,  swiftlet).  They  emit  up 
to  5  to  6  clicks  a  second  at  4  to  5  Kc.  The  rate  varies  inversely  with 
the  amount  of  light  and  increases  when  obstacles  are  met. 


4QO 


THE  BIRDS 


xvi.  31 


31.  Other  receptors 

The  corpuscles  of  Grandry  in  the  bill  of  ducks  and  other  birds  are 
probably  touch  receptors,  comparable  to  Meissner's  corpuscles  in 
mammals.  The  corpuscles  of  Herbst,  found  in  the  dermis  elsewhere  in 


Fig.  301.  a.  Diagram  of  section  of  bird's  ear. 

b.m.    basilar   membrane;    col.    columella;    ex.   extra-columella;    E.t.    Eustachian   tube; 

f.r.  round  window;  h.c.C.  hair-cells  of  Corti's  organ;  h.c.l.  hair-cells  of  lagena;  sacc. 

sacculus;  s.t.  scala  tympani;  s.v.  scala  vestibuli;  t.m.  tectorial  membrane;  t.v.  tegmentum 

vasculosum;  tym.  tympanic  membrane. 

b.  Diagram  of  section  across  cochlea  of  a  bird. 
G.cochl.  cochlear  ganglion;  s.m.  scala  media;  other  lettering  as  in  A.  (From  Pumphrey, 

after  Satoh.) 

the  body,  resemble  Pacinian  corpuscles.  They  may  be  receptors  for 
vibration  and  are  numerous  in  certain  situations,  for  example  in  the 
feather  follicles,  the  beak,  between  the  tibia  and  fibula,  and  in  the  tip 
of  the  tongue  of  a  woodpecker. 

Chemoreceptors  for  taste  and  smell  are  little  developed.  There  are 
few  taste-buds  on  the  tongue.  The  nasal  cavity  is  large  but  the 
olfactory  epithelium  restricted.  It  is  doubtful  whether  most  birds  use 
the  nose  as  a  distance  receptor;  they  may  use  it  to  test  air  coming  from 
the  internal  nostril.  In  kiwis,  however,  which  are  nocturnal  and  terres- 
trial, the  olfactory  sense  is  well  developed. 


XVII 

BIRD  BEHAVIOUR 


1 .  Habitat  selection 


The  success  of  bird  life  has  been  largely  due  to  the  great  variety  and 
ingenuity  displayed  in  finding  situations  suitable  for  providing  food 
and  allowing  reproduction.  Their  powers  of  habitat  selection  allow 
diversification  of  species  by  reducing  interspecific  competition.  Species 
living  in  the  same  area  rarely  eat  the  same  food,  especially  if  it  is 
scarce.  It  is  often  said  that  birds  are  creatures  of  stereotyped  habits, 
yet  they  have  certainly  exploited  their  mobility  to  the  full;  they  obtain 
the  means  of  life  in  most  various  ways.  This  mobility  makes  it  difficult 
to  specify  the  'environment'  of  a  bird.  For  instance,  a  swallow  may 
pass  part  of  its  life  in  the  tropics,  part  near  the  Arctic  Circle.  A  gull 
may  nest  on  a  rock,  eat  grain  in  a  field,  and  then  fish  in  the  sea,  all 
within  a  few  hours.  Observation  of  the  familiar  birds  of  town  and 
country  soon  shows  that  they  are  at  home  in  a  much  greater  variety 
of  situations  than  could  be  supported  by  most  animals,  and  that  within 
limits  they  can  adapt  their  behaviour  to  each  situation.  Birds  show, 
therefore,  in  a  marked  degree,  two  of  the  features  most  commonly  used 
as  criteria  for  the  recognition  of  a  higher  animal,  namely,  freedom  to 
move  to  different  conditions  and  ability  to  obtain  a  living  in  unpromis- 
ing circumstances. 

Nevertheless  each  species  nests  in  a  limited  variety  of  habitats  and 
feeds  in  a  limited  variety  of  habitats.  There  is  evidence  that  the 
appropriate  habitat  is  recognized  by  a  relatively  small  number  of 
conspicuous  features,  independently  of  learning. 

2.  Food  selection 

Where  the  food  is  very  specific  substitutes  will  only  be  accepted 
under  unusual  conditions  of  starvation,  but  many  birds  are  more 
catholic  in  tastes  and  some  of  these  are  among  the  most  common,  for 
instance  rooks,  starlings,  thrushes,  blackbirds,  and  gulls.  Both  field 
observation  and  experiment  suggest  that  birds  quickly  learn  from 
experience  where  and  how  food  may  be  obtained.  They  will  remember 
to  visit  an  abundant  source  of  supply  and  there  are  numerous  stories 
of  the  ingenuity  of  such  birds  as  the  jackdaws  in  obtaining  it.  This 
short-term  memory  is  probably  of  great  importance  in  allowing  the 


492  BIRD  BEHAVIOUR  xvn.  2- 

bird  to  establish  an  effective  routine  for  each  part  of  its  life,  especially 
as  it  is  combined  with  the  power  to  explore  elsewhere  when  conditions 
change. 

Food  selection  thus  depends  on  species-characteristic  motor  patterns 
and  structures,  whose  use  varies  to  suit  the  circumstances.  There  is  an 
initial  responsiveness  to  a  wide  range  of  stimuli,  later  modified  by 
learning.  In  young  birds  these  actions  are  not  necessarily  related  to 
appropriate  objects  or  situations.  Thus  young  chaffinches  or  tits  peck 
at  spots  of  many  sizes,  but  only  when  they  are  not  hungry.  When  they 
are,  they  beg  from  the  parents.  Young  kestrels  'play'  at  hunting  pine 
cones,  even  after  obtaining  food  by  real  hunting  (see  Hinde,  1959). 

This  range  of  response  is  then  narrowed  by  learning.  Objects  that 
provide  food  are  pecked  again,  those  that  do  not  or  are  distasteful  are 
avoided.  The  range  of  learning  that  is  possible  must,  however,  be 
influenced  by  the  hereditary  equipment.  Thus  chaffinches  never  use 
the  foot  to  hold  objects  but  goldfinches  and  tits  do  so  and  can  thus 
learn  to  pull  over  a  grass  stem  and  peck  off  insects  otherwise  out  of 
reach,  or  indeed  to  open  milk  bottles! 

3.  Recognition  and  social  behaviour 

Great  mobility  has  made  it  necessary  for  birds  to  develop  specific 
means  for  recognizing  their  fellows,  their  enemies,  and  their  com- 
petitors; from  this  power  an  elaborate  social  life  has  developed  in 
many  species.  In  spite  of  their  freedom  many  birds  are  not  indivi- 
dualists, they  live  much  of  their  lives  together  in  flocks;  the  unit  of 
life  is  larger  than  the  'individual'  body.  Species  feeding  on  the  ground, 
such  as  rooks,  starlings,  and  partridges,  commonly  move  about  in 
groups  during  the  winter  and  obtain  the  advantage  that  the  alertness 
of  each  single  bird  serves  to  warn  for  many.  The  lack  of  procryptic 
coloration  in  some  of  these  social  birds  is  a  measure  of  the  effectiveness 
of  the  protection  afforded  by  the  society;  indeed,  it  may  be  advanta- 
geous that  the  birds  should  be  conspicuous  to  their  fellows.  Starlings 
carry  the  communal  life  farther  by  collecting  together  in  large  numbers 
each  night  to  roost.  As  many  as  100,000  may  be  found  in  one  roost, 
the  birds  flying  home  from  their  feeding-grounds  every  night  for 
distances  of  many  miles.  Possibly  in  this  way  the  disadvantage  of  the 
conspicuous  outline  is  minimized  while  roosting.  Rooks  show  some- 
what similar  behaviour,  but  it  is  not  found  in  the  protectively  coloured 
partridge. 

Many  different  means  are  adopted  by  birds  for  recognition  of  other 
members  of  the  species  and  of  the  same  and  opposite  sex;  bird-life 


xvii.  4  MIGRATION  493 

contains  elaborate  social  and  sexual  rituals  for  many  occasions.  For 
example,  relief  of  the  one  bird  by  the  other  at  the  nest  is  accompanied 
by  a  peculiar  wing-flapping  ceremony  in  herons  and  other  birds. 
Greeting  ceremonies  are  common  in  many  species,  and  there  is  a  host 
of  sexual  recognition  and  courtship  rituals,  to  be  considered  later, 
serving  the  immediate  function  of  regulating  the  aggressiveness  that 
otherwise  arises  when  two  individuals  approach  each  other  closely. 
Such  ceremonies  prevent  attempted  copulation  with  the  same  sex  and 
ensure  it  with  a  member  of  the  opposite  sex,  and  of  the  right  species. 
Apart  from  sexual  behaviour  birds  show  many  complex  mutual  and 
social  reactions.  Thus  in  communities  of  hens  or  pigeons  there  is 
quickly  established  a  rank  of  'pecking  order',  such  that  each  bird  is 
submissive  to  the  one  above  it,  the  order  changing,  however,  when  age, 
moulting,  or  experiment  (e.g.  sex-hormone  injection)  alters  the  state 
of  the  birds.  More  pleasing  communal  habits  are  the  dances  and 
corporate  flights,  which  are  well  known  in  cranes  and  other  species. 

4.  Bird  migration  and  homing 

Among  the  remarkable  devices  of  birds  is  their  habit  of  seasonal 
movements  to  obtain  the  advantage  of  the  favourable  conditions 
offered  in  more  northerly  regions  only  during  the  summer.  The  most 
familiar  migrations  are  those  north  and  south  (sometimes  north-east 
and  south-west)  over  the  land  masses  of  the  northern  hemisphere,  but 
there  are  similar  movements  also  in  the  southern  hemisphere,  though 
they  are  of  lesser  extent.  Some  tropical  birds  migrate  to  breed  in  the 
rainy  season  in  the  outer  tropics,  removing  to  the  central  tropics  in 
the  dry  season.  Marine  birds  also  may  make  extensive  migrations. 
Thus  the  great  shearwater  (Puffinus)  breeds  on  Tristan  da  Cunha,  but 
comes  as  far  north  as  Greenland  or  Iceland  in  May,  returning  again 
after  months  of  wandering  at  sea,  apparently  without  making  a  land- 
fall. The  Arctic  tern  (Sterna)  breeds  in  the  north  temperate  zone,  and 
migrates  to  the  Antarctic  along  both  sides  of  the  Atlantic.  Penguins 
make  migrations  by  swimming.  Distances  up  to  6,000  miles  from 
Northern  Europe  to  South  Africa  have  been  recorded  for  swallows 
and  storks,  and  even  farther  for  the  Arctic  tern.  The  factors  deter- 
mining the  direction  and  course  of  migration  are  beginning  to  be 
known.  It  has  been  shown  that  the  power  to  follow  a  given  course 
depends  partly  on  the  ability  to  navigate  by  observation  of  the  position 
of  the  sun  or  stars  (Matthews,  1955;  Sauer,  1957).  Birds  certainly  do 
not  learn  the  routes  from  their  elders,  indeed  the  young  often  leave 
first.  However,  juveniles  return  only  approximately  to  their  birthplace, 


BIRD  BEHAVIOUR 


494  lilKU    bLHAVlUUK  XVII.  4- 

whereas  older  individuals  return  to  their  old  nesting  sites.  Individual 
memory  therefore  plays  a  part.  The  birds  often  migrate  singly  and 


Fig.  302.  Direction  of  migration  of  the  stork  (Ciconia).  The  black  spots  represent  points 

of  recovery  of  birds  ringed  in  Germany.  The  dotted  areas  show  the  pathways  produced 

by  ecological  and  geographical  factors.  (After  Schulz  and  Stresemann.) 

experiments  in  a  planetarium  have  shown  that  warblers  turn  accurately 
in  the  appropriate  direction  as  given  by  the  stars. 

The  available  evidence  therefore  suggests  (a)  that  for  most  species 
at  least  there  is  a  preferred  direction  for  migration,  which  is  indepen- 
dent of  experience.  Hand-reared  warblers  will  orient  correctly  by  the 
stars  without  previous  experience;  (b)  that  they  may  be  deviated  by 
features  of  the  environment  such  as  coastlines  or  hills;  (c)  that  after 


xvii.  5  MIGRATION  495 

experience  they  can  do  more  than  just  steer  a  course — they  can  navi- 
gate, that  is  fix  position,  calculate  the  course  to  steer,  and  follow  it. 

Powers  of  'homing'  are  remarkable  in  birds,  altogether  apart  from 
migration.  It  is  probable  that  these  feats  are  performed  by  the  use  of 
visual  clues,  combined  with  a  tendency  to  follow  coastal  outlines  and 
other  conspicuous  geographical  features.  Pigeons  are  trained  to  'home' 
by  release  at  progressively  increasing  distances  and  can  acquire  the 
ability  to  return  from  more  than  500  miles. 

It  has  now  been  satisfactorily  proved  that  pigeons  return  home  after 
release  from  a  distant  point  even  if  they  have  never  been  there  before, 
nor  have  had  any  previous  training  in  returning  from  situations  out  of 
sight  from  the  loft.  Matthews  (1955)  and  others  have  shown  that  upon 
release  the  birds  fly  off  towards  home  provided  that  they  can  see  the 
sun.  This  capacity  to  navigate  by  the  sun  must  depend  upon  deter- 
mination of  position  on  two  coordinates  by  observations  of  the  sun's 
altitude,  azimuth,  and/or  movement.  This  implies  the  use  of  a  very 
accurate  chronometer  as  a  means  of  determining  the  difference  be- 
tween home  and  local  time.  It  is  hard  to  believe  that  all  this  could  be 
achieved  in  the  few  seconds  following  release,  but  the  facts  demand 
some  such  hypothesis.  Moreover,  experiments  designed  to  upset  the 
'chronometer'  by  altering  the  period  of  daylight  have  been  claimed  to 
be  effective  in  altering  the  direction  of  flight  of  birds  upon  release. 

Other  birds  are  also  able  to  return  home  from  spectacular  distances, 
an  instance  being  the  Manx  shearwater  removed  from  its  nest  (burrowr) 
on  Skokholm  Island  off  the  Welsh  coast  and  sent  to  Boston  by  air:  it 
returned  in  12  days,  the  distance  being  3,067  miles  across  the  Atlantic. 
In  another  experiment  three  out  of  ten  untrained  terns  returned  to 
their  nests  from  a  distance  of  855  miles,  in  about  6  days.  There  are 
many  peculiar  and  unexplained  features  about  such  long  journeys. 

5.  The  stimulus  to  migration 

It  is  probable  that  the  north-to-south  migrations  of  birds  in  the 
northern  hemisphere  take  place  under  some  stimulus  provided  by  the 
internal  condition  of  the  gonads,  these  being  themselves  affected  by 
the  seasonal  change.  Rowan  has  made  extensive  experiments  with 
juncos,  birds  that  are  summer  visitors  to  Alberta,  Canada.  If  the  birds 
are  caged  in  the  autumn  and  illuminated  to  compensate  for  the  shorten- 
ing day  the  gonads  do  not  regress  as  they  normally  do  at  that  season, 
so  that  full  breeding  song  continues  on  into  the  middle  of  winter. 
Rowan  had  the  interesting  idea  of  releasing  these  birds  in  the  winter 
and  found  that  they  immediately  moved  away,  perhaps  northwards, 


496  BIRD  BEHAVIOUR  xvn.  5- 

conditions  being  then  appropriate  if  anything  for  that  direction.  On 
the  other  hand,  control  birds,  which  had  been  kept  in  Alberta  but 
without  extra  light,  showed  no  tendency  to  move  away  if  released  in 
mid- winter.  Since  the  gonads  of  these  controls  had,  of  course,  by  then 
undergone  reduction,  the  stimulus  to  migrate  south  was  not  felt.  This 
would  agree  with  the  fact  that  only  some  individuals  of  species  such 
as  the  thrush  and  blackbird  migrate.  These  experiments  suggest  that 
seasonal  changes  in  illumination  may  be  an  important  factor  deter- 
mining migration.  However,  they  leave  many  points  unsettled.  For 
instance,  is  there  a  stimulus  that  starts  the  bird  migrating  north  again 
if  it  has  'wintered'  near  the  equator,  where  there  is  little  or  no  seasonal 
change  ?  It  may  be  that  once  alteration  of  the  gonads  has  been  started, 
say,  by  reduction  in  light,  a  cycle  will  be  set  up,  the  gonads  developing 
again  with  the  longer  days  in  the  south  and  thus  driving  the  bird  north 
again,  and  so  on. 

6.  The  breeding-habits  of  birds 

The  complexity  and  variety  of  bird  behaviour  show  especially  in 
their  breeding;  perhaps  in  no  other  creatures  except  men  is  such 
elaborate  behaviour  involved  in  bringing  the  birds  together  and  caring 
for  the  young.  In  order  to  ensure  adequate  provision  for  the  develop- 
ment of  a  warm-blooded  animal  and  its  nourishment  until  it  can  fend 
for  itself  it  is  necessary  either  to  keep  it  within  the  mother  or  to  provide 
a  means  of  incubating  the  eggs.  In  either  case  a  long  period  of  care  is 
necessary  after  birth;  the  young  animals,  having  a  large  surface  area, 
require  a  great  amount  of  food  to  keep  warm.  Thus  young  starlings 
and  crows  may  eat  as  much  as  their  own  weight  of  food  each  day. 

Mammals  and  birds  set  about  providing  for  this  warmth  and  food 
in  different  ways.  Since  a  female  mammal  can  move  about  and  get 
food  while  pregnant  the  father  can  desert  her  altogether,  though  fre- 
quently he  does  not  do  so.  In  birds  the  eggs  and  young  cannot  be  left 
cold  for  long  and  it  is  therefore  especially  desirable  that  the  father 
should  help.  In  birds,  therefore,  perhaps  even  more  than  in  mammals, 
the  breeding-habits  involve  the  development  of  elaborate  systems  of 
mutual  relations,  serving  not  only  to  bring  the  parents  together  but  also 
to  keep  them  together  throughout  the  period  of  incubation  and  while 
feeding  the  young.  The  actual  building  of  the  nest  may  be  an  intricate 
business  in  which  both  birds  collaborate  and  a  further  factor  is  that 
the  pair  occupies  a  territory  around  the  nest,  which  they  defend  against 
others  of  the  same  species. 

The  type  of  association  of  the  sexes  varies  greatly.  In  the  ruff  and 


xvii.  7  COURTSHIP  497 

certain  game  birds  (blackcock)  there  is  no  pair  formation :  display  and 
copulation  occur  at  communal  display  grounds.  The  wren  {Troglodytes) 
and  a  few  other  birds  are  polygamous,  each  male  forming  continuous 
association  with  several  females.  The  great  majority  of  birds  form  pairs 
throughout  a  single  season,  occasionally  they  change  mates  for  the 
second  brood.  The  same  pair  may  mate  in  successive  years  (crows, 
swifts)  and  a  few  birds  stay  together  through  the  year  (ducks). 

7.  Courtship  and  display 

The  breeding  of  birds  is  nearly  always  seasonal,  even  in  the  tropics 
where  conditions  are  apparently  almost  uniform  throughout  the  year. 
In  temperate  latitudes  breeding  begins  in  spring  as  the  gonads  develop, 
probably  under  the  influence  of  increasing  illumination.  The  changes 
in  behaviour  with  ripening  of  the  gonads  vary,  of  course,  greatly  with 
the  species.  Birds  that  have  been  social  through  the  winter,  for  instance 
buntings,  begin  to  leave  their  flocks,  and  the  voice  of  the  male  changes 
from  the  simple  winter  notes  to  the  more  complex  breeding  song.  The 
production  of  the  elaborate  secondary  sexual  characters  of  the  plumage 
and  other  features  used  in  display  is  controlled  partly  by  direct  genetic 
effects  on  the  tissues,  partly  through  hormones.  Injections  of  male  or 
female  sex  hormones  or  anterior  pituitary  extracts  influence  the  pro- 
duction of  some  characters  but  not  others,  according  to  the  species. 
In.  the  majority  of  birds  there  is  a  breeding-season,  initiated,  at  least 
in  many,  by  the  effect  of  increasing  length  of  day  in  the  spring,  acting 
through  the  pituitary  on  the  gonads.  Other  factors  such  as  degree  of 
activity  and  food  taken  play  their  parts,  especially  near  the  equator, 
where  there  is  little  seasonal  variation. 

The  song  is  one  feature  of  the  elaborate  business  of  display  and 
courtship.  It  has  somewhat  different  functions  from  species  to  species. 
In  the  simplest  case  the  display  serves  to  bring  the  sexes  together,  to 
enable  recognition,  and  at  a  later  stage  as  a  stimulus  to  copulation. 
Moreover,  in  some  birds  (doves,  budgerigars,  and  canaries),  the  dis- 
play serves  as  part  of  the  stimulus  to  ovulation.  Involved  in  the  display 
actions,  however,  is  often  a  threat  to  other  males.  The  aggressive 
displays  are  usually  different  from  the  courtship  displays,  though  in 
many  species  the  male's  first  response  to  a  potential  mate  is  an 
aggressive  one.  When  the  female  does  not  flee  or  fight  back,  as  a  male 
would  do,  he  gradually  changes  over  to  courtship  display.  Finally, 
some  forms  of  courtship,  especially  those  that  are  mutual,  seem  to 
serve  to  keep  the  partners  together  for  the  period  of  incubation  and 
feeding. 


498  BIRD   BEHAVIOUR  xvn.  7 

We  may  recognize  in  courtship,  therefore,  three  elements,  first 
sexual  stimulation,  secondly  threat  to  other  males,  and  thirdly  mutual 
stimulation  while  rearing  a  family,  but  the  various  types  of  display 
are  combined  in  so  many  different  ways  that  any  classification  or 
analysis  is  bound  to  be  arbitrary  and  only  a  few  examples  that  have 
been  thoroughly  studied  can  be  given.  There  are,  of  course,  also 
begging  displays,  given  by  young  to  parents,  various  displays  given 
to  potential  predators,  and  others. 

Song  and  displays  that  bring  the  sexes  together  are  responsible  in 
part  at  least  for  many  of  the  pronounced  secondary  sexual  characters 
in  which  the  male  and  female  differ.  The  beautiful  plumage  of  the 
cock  pheasant  or  peacock  and  the  more  bizarre  combs  and  wattles  of 
turkeys  are  displayed  before  the  female  in  a  manner  that  is  clearly  an 
excitant  to  copulation.  The  secondary  sexual  characters  by  which  the 
sexes  are  differentiated  may  affect  features  as  different  as  the  colour, 
length,  and  structure  of  the  feathers,  the  colour  of  the  iris  and  size  of 
the  pupil,  the  shape  and  size  of  the  body,  the  voice,  the  ornamentation 
of  the  head,  and  the  spurs  on  the  feet.  The  importance  of  species 
recognition  in  leading  to  differentiation  of  male  plumage  is  shown  by 
Darwin's  finches  (p.  524)  which,  in  the  isolation  of  the  Galapagos 
Islands,  where  there  are  few  other  passerine  birds,  have  abandoned 
the  highly  coloured  male  plumage  found  in  other  finches.  The  recogni- 
tion of  individuals  of  the  same  species  in  this  case  is  based  on  the 
characteristics  of  the  beak;  a  male  will  begin  to  attack  an  intruder  only 
when  the  face  is  seen. 

Display  takes  place  either  by  one  bird  to  the  other  or  mutually,  and 
has  the  effect  of  bringing  the  animals  together  and  keeping  them 
together  for  periods  varying  from  a  few  minutes  to  several  years.  Long 
unions  are  common  in  the  large  birds  of  prey  and  are  often  a  result  as 
much  of  mutual  association  with  the  nest  as  with  display  by  the  other 
bird.  Some  birds  pair  in  the  winter  long  before  the  gonads  are  ripe 
(ducks),  but  more  usually  after  two  birds  pair  off  the  display  produces 
a  gradual  heightening  of  tension,  leading  to  nest-building,  copulation, 
and  ovulation  within  a  few  days.  Probably  the  process  of  bringing  the 
birds  together  and  ensuring  coition  requires  even  more  elaborate 
stimulation  in  birds  than  other  animals  because  of  their  great  mobility 
and  the  fact  that  the  male  cannot  grasp  the  female.  Before  he  can 
tread  her  in  such  a  way  as  to  ensure  coition  she  must  be  brought  into 
a  suitably  receptive  state.  The  function  of  the  display  is  certainly 
largely  to  induce  this  state  in  the  female,  though  much  more  is 
involved   in   addition.   The   processes   of  sexual   stimulation,   nest- 


xvii.  7  DISPLAY  499 

building,  incubation,  and  caring  for  the  young  necessitate  a  particular 
state  of  excitability  that  must  last  a  long  time,  and  the  display  serves 
to  provide  this  condition  in  both  birds.  The  reproductive  process  may 
be  interrupted  at  any  time  if  the  stimuli  are  inadequate.  Thus  ovula- 


Fig.  303.  Incidents  in  the  courtship  of  the  great  crested  grebe.  1.  Mutual  head 
shaking.  2.  The  female  is  displaying  before  the  male  who  has  dived  and  shoots  out 
of  the  water  in  front  of  her.  3  and  4.  Further  views  of  the  male  rising  from  the 
water.  5.  Both  birds  have  dived  and  brought  up  weeds.  (From  Huxley,  Proc.  Zool. 
Soc,  1914,  by  permission  of  the  Zoological  Society.) 


tion  may  depend  upon  courtship  and  copulation  (pigeons)  and  eggs 
are  often  deserted  if  the  birds  are  interfered  with  in  any  way,  or  if 
they  fail  to  stimulate  each  other. 

The  actual  procedure  of  display  is  as  varied  as  any  other  feature  of 
bird  life.  When  the  sexes  are  alike  in  colour  and  shape  the  performance 
is  usually  mutual,  as  in  the  great  crested  grebes  (Podiceps),  which 


5°o 


BIRD  BEHAVIOUR 


xvn.  7 


approach  each  other  over  the  water  and  go  through  various  actions 
such  as  the  head-shaking  ceremony  (Fig.  303).  Where  the  male  is  more 
strongly  coloured,  provided  with  a  special  comb,  &c,  he  often  displays 
before  the  female,  who  adopts  a  more  passive  role.  A  very  common 
element  in  the  procedure  of  courtship  is  the  sudden  revelation  of  some 


Fig.  304.  Display  of  various  birds  of  paradise. 

1  and  4,  Paradisea;  2,  Diphy  Modes;  3,  Cicinnurus. 
(From  Streseman,  after  Seth  Smith.) 

feature  or  pattern,  serving  as  it  were  to  arrest  and  awaken  the  female 
and  at  the  same  time  almost  to  reduce  her  to  passiveness.  The  actual 
movements  involved  are  very  various.  An  excellent  example  is  the 
peacock,  who  approaches  showing  his  dull-coloured  back  and  then 
suddenly  turns  on  his  hen,  revealing  the  pattern  of  spots  (which  we 
have  noted  elsewhere  to  be  an  arresting  shape),  shaking  his  'tail'  with 
a  rustling  noise  and  himself  emitting  a  scream,  in  a  way  that  can  easily 
be  believed  both  arresting  and  fascinating.  It  is  a  common  charac- 


xvii.  7  RITUAL  FEEDING  5°i 

teristic  of  all  bird  displays  that  they  involve  sights  and  actions  that 
have  a  peculiar  and  exaggerated  quality  for  us  and  probably  also  for 
the  partner  (Figs.  304,  305).  Watching  the  effects  of  such  appearances 
on  the  female  one  has  the  impression  that  this  vision  acts  as  it  were  as  a 
key  or  'releaser',  opening  in  her  the  appropriate  course  of  behaviour. 
Under  its  influence  she  acts  as  if  'mechanically',  moving  towards  the 
male  and  adopting  the  receptive  position,  while  his  display  activity 
passes  over  into  that  of  mounting  and  coition.  This  sort  of  behaviour 
we  have  seen  elsewhere  in  bird  life;  there  must  be  in  the  nervous 


Fig.  305.  Display  of  the  pheasant,  Centrocercus.  i.  Beginning  of  inflation. 

2.   Complete  display  with  cervical  air-sacs  inflated.  (From  Stresemann, 

after  Horsfall.) 


organization  a  receptive  matrix  ('the  lock')  ready  to  be  actuated  by  the 
appropriate  'key',  which  may  be  the  display  of  structures  as  bizarre 
as  the  wattles  and  tippets  of  a  turkey. 

Many  displays  are  modified  versions  of  everyday  actions  of  the 
birds  and  some  at  least  of  these  seem  to  be  symbolic.  Thus,  in  many 
birds  courtship  and  coition  include  ritual  feeding  of  the  female  by  the 
male.  Involved  in  this  is  a  reversion  by  the  female  to  an  infantile  con- 
dition. She  may  beg  for  food,  often  with  actions  similar  to  those  she 
used  as  a  nestling.  The  prime  significance  of  this  feeding  is  not  in  the 
nourishment  provided  but,  in  many  cases  at  least,  in  the  fact  that  it  is 
the  male  who  provides  it.  This  is  proved  by  the  fact  that  the  female 
(robin,  for  instance)  will  not  feed  herself  when  food  is  all  around,  but 
will  beg  the  male  to  give  it  to  her.  Female  herring  gulls  bringing  back 
fish  may  even  beg  to  be  fed  by  the  male,  who  has  not  left  the  rock! 
There  are,  of  course,  many  cases  of  practical  feeding  of  the  sitting 
female  by  the  male,  but  it  is  possible  that  these  have  been  derived  from 
the  ritual  feeding,  rather  than  vice  versa. 


502  BIRD  BEHAVIOUR  xvn. 7- 

The  various  forms  of  billing  and  gaping  ceremony  probably 
represent  a  further  degree  of  abstraction  from  ritual  feeding.  A  variety 
of  birds  touch  bills  during  courtship,  for  instance,  gulls,  ravens,  great 
crested  grebes,  and  some  finches.  The  inside  of  the  mouth  is  some- 
times brilliantly  coloured  in  adults,  as  it  is  in  so  many  nestlings;  it  is 
green  in  some  birds  of  paradise,  yellow  in  many  birds.  During  display 
it  may  be  opened  suddenly,  producing  an  obvious  effect  on  the  mate, 
who  approaches  fascinated  into  a  state  of  passive  acceptance  by  this 
surprising  revelation,  perhaps  recalling  a  possibility  of  satisfaction 
remembered  from  childhood. 

Other  aspects  of  the  courtship  may  show  this  reversion  to  infantile 
behaviour.  Thus,  in  female  sparrows  and  many  other  birds  one  or 
both  wings  are  held  drooping  and  fluttering  during  display,  as  they 
are  by  the  chick  craving  food  or  by  the  frightened  adult ;  a  behaviour 
known  as  injury  feigning  or  distraction  display.  The  female  hedge- 
sparrow  may  quiver  with  one  wing  and  open  her  bill  to  the  male  at  the 
same  time.  This  injury- feigning  also  has  survival  value  in  distracting 
the  attention  of  a  predator  from  the  nest,  as  can  be  well  seen  in  plovers 
and  other  ground-nesting  birds.  Some  plovers  have  different  displays 
for  use  against  different  types  of  nest  enemy. 

The  effects  of  bird  display  are  by  no  means  restricted  to  ensuring 
mutual  recognition  of  males  and  females  and  stimulating  them  to 
coition,  especially  important  though  such  functions  must  be  in  'flighty' 
creatures.  The  element  of  threat  and  even  fighting  with  other  males 
is  very  common.  It  is  seen  in  its  purest  form  in  such  birds  as  the 
blackcock  and  ruff,  which  are  promiscuous.  The  male  ruffs  congre- 
gate on  a  chosen  'courting  ground'  and  go  through  an  elaborate  series 
of  ritual  fights.  The  females  ('reeves')  do  not  take  part  in  this  pro- 
cedure, but  at  intervals  one  of  them  will  'select'  a  male  by  fondling 
him  with  her  bill  and  then  adopt  the  receptive  attitude  for  copulation. 
Selous,  who  observed  this  display,  noted  that  males  with  large  ruffs 
were  chosen  especially  often.  Such  selection  of  males  by  females  was 
the  basis  of  Darwin's  theory  of  sexual  selection,  the  supposition  being 
that  the  males  chosen  would  be  the  most  gorgeous,  victorious,  and 
hence  most  vigorous  and  effective  breeders.  Selous  recorded  that  in 
one  area,  during  a  period  of  3!  hours,  there  were  12  copulations,  10  of 
them  with  a  single  male.  It  must  be  very  difficult  when  observing 
birds  to  establish  exactly  the  actions  and  relationships  of  males  and 
females  and  hence  to  distinguish  between  the  'stimulation'  of  female 
by  male  and  'selection'  of  male  by  female.  Perhaps  there  is  only  a 
verbal  difference  between  the  two. 


xvii.  8  (503) 


8.  Bird  territory 


The  element  of  threat  in  singing  and  display  has  a  further  impor- 
tance in  connexion  with  the  territories  that  many  birds  establish 
around  their  nests.  Eliot  Howard  especially  has  developed  the  con- 
cept of  bird  territory  as  a  result  of  observation  mainly  of  warblers 
and  buntings.  For  instance,  in  the  warblers  (Sylviidae)  the  males, 
returning  from  migration  some  days  earlier  than  the  females,  establish 
themselves  on  a  certain  area,  singing  often  from  a  tall  tree  or  other 
headquarters  near  its  centre.  As  other  males  arrive  boundaries  develop, 
so  that  the  region  becomes  divided  up  into  a  number  of  areas,  at  first 
each  of  about  2  acres,  later  reducing  to  1.  When  the  females  arrive 
they  pair  off  with  the  males  and  throughout  the  whole  season  the  two 
birds  occupy  a  single  territory,  driving  off  other  birds  that  encroach 
and  in  this  way  establishing  quite  definite  boundaries  to  their  area. 

Howard  supposed  that  this  arrangement  was  widespread  in  birds 
and  that  it  has  four  desirable  effects  for  the  species. 

1.  Uniform  distribution  over  the  habitable  area  is  ensured. 

2.  Females  are  assisted  to  find  unmated  males. 

3.  The  two  birds  are  kept  together  and  are  not  distracted  by 
wanderings  far  from  home. 

4.  It  is  possible  to  find  adequate  food  without  travelling  far  from 
the  nest,  this  being  especially  important  during  the  period  of  incuba- 
tion and  rearing  of  the  young.  There  is  no  doubt  that  many  birds  do 
remain  mostly  in  the  area  around  their  nest  and  that  they  may  resist 
invasion.  It  is  probable,  however,  that  the  territory  is  usually  less 
rigid  than  Howard  implied,  and  there  is  certainly  much  variety 
between  different  species.  According  to  Lack  the  territory  is  often 
mainly  associated  with  the  sexual  display  of  the  male;  it  is  his  area, 
part,  as  it  were,  of  the  method  he  adopts  to  stimulate  the  female  and 
to  keep  the  pair  together.  By  establishing  a  territory  he  ensures  the 
opportunity  to  display  and  copulate  without  disturbance,  a  very 
necessary  precaution  since  he  is  vulnerable  at  these  times  and  other 
individuals  may  attack  a  copulating  male,  trying  to  displace  him. 
The  complicated  song,  characteristic  of  so  many  male  birds  at  the 
breeding-season,  is,  on  this  view,  partly  an  attraction  to  the  female, 
but  largely  also  a  threat  to  warn  off  other  males.  We  cannot  exclude 
that  it  serves  as  a  stimulus  to  the  male  himself.  The  impression  is 
strong  when  one  hears  a  thrush  'singing  for  joy'  at  his  headquarters 
or  a  lark  soaring  above  his  patch  of  ground. 

Territory  is  therefore,  according  to  Lack,  put  to  various  uses  in 


5o4  BIRD  BEHAVIOUR  xvn.  8- 

different  species.  It  may  be  either  (i)  a  mating  arena  only,  as  in  the 
ruff  and  blackcock  mentioned  above,  or  (2)  it  may  be  a  mating  station 
and  nest  as  in  the  plover  and  swallow,  which  birds  will  not  allow 
others  near  the  nest,  although  all  mix  freely  for  feeding.  (3)  In 
sparrows  and  herring  gulls  the  nest  is  likewise  defended,  but  is  not  a 
mating  station.  (4)  In  the  warblers  investigated  by  Howard  the  ter- 
ritory, besides  being  a  mating  station,  is  also  a  feeding-ground.  The 
significance  of  this  in  spacing  out  the  birds  remains,  however,  doubt- 
ful. It  may  limit  the  effect  of  predators,  by  ensuring  dispersal.  (5)  In 
still  other  birds,  such  as  the  robin,  it  is  a  feeding-ground  mainly,  and 
therefore  it  is  kept  throughout  the  winter.  Examination  of  the  ter- 
ritory concept  thus  shows  that  birds  have  a  strong  sense  of  place 
and  that  they  associate  this  in  various  ways  with  their  life,  especially 
during  the  breeding-season.  It  is  certain  that  the  occupation  of  ter- 
ritory helps  in  the  initiation  and  maintenance  of  the  pair,  but  not  yet 
proved  that  it  serves  to  limit  the  breeding  density  and  ensure  a  food- 
supply  for  the  young. 

9.  Mutual  courtship 

In  many  birds  courtship  displays  do  not  necessarily  end  in  coition 
and  may  continue  long  after  the  eggs  have  been  laid.  A  classic  example 
of  this  sort  is  the  great  crested  grebe,  a  water-bird  watched  by  J.  8. 
Huxley  (Fig.  303).  The  male  and  female  birds  do  not  differ  greatly 
and  the  ceremonies  are  mutual.  One  bird  may  dive  and  come  up 
close  to  the  other  and  they  then  approach  with  necks  stretched  out  on 
the  water,  giving  a  curious  ripple  pattern  that  Huxley  called  the 
plesiosaur  appearance.  When  they  meet  the  birds  come  together  neck 
to  neck  and  a  period  of  swaying  ensues  and  may  sometimes  end  by 
the  mounting  of  one  bird  by  the  other,  not  necessarily  the  female  by 
the  male.  At  other  times  the  diving  bird  comes  up  with  pieces  of  nest- 
building  material  and  elaborately  presents  them  to  its  mate.  This  is 
apparently  a  symbolic  act;  the  material  is  not  actually  used  to  make  the 
nest  and  it  is  not  far-fetched  to  suppose  that  such  behaviour  is  an 
expression  of  the  mutual  activity  in  which  the  birds  are  engaged.  In  so 
far  as  it  has  a  biological  function  it  serves,  like  the  rest  of  the  ritual, 
including  post-ovulatory  copulation,  to  keep  the  two  individuals 
together  while  rearing  the  young. 

As  already  mentioned,  courtship  may  include  ritual  feeding  of  the 
other  sex  during  display  and  often  before  coition,  for  instance,  in 
pigeons  and  gulls,  and  this  again  may  have  a  symbolic  function.  It  is 
perhaps  not  fantastic  to  find  analogies  between  behaviour  of  this  sort 


xvii.  io  NEST-BUILDING  5°5 

and  the  elaborate  and  prolonged  courtship  and  frequent  copulation  of 
man,  continuing  without  cyclical  breeding-seasons  for  as  long  as  the 
pair  remain  together  and  rear  their  young.  In  birds,  as  in  man,  the 
'procreation  of  children'  is  not  fully  accomplished  by  a  single  act 
of  fertilization. 

10.  Nest-building 

As  in  every  other  aspect  of  their  life  we  find  the  nest  of  birds  varied 
in  many  ways  to  suit  different  manners  of  life.  It  is  suggested  that  the 
habit  of  making  a  nest  may  have  arisen  from  the  'sex-fidgeting'  that 
is  commonly  seen  before,  during,  and  after  copulation.  This  fidgeting 
may  take  various  forms,  including  making  a  'scrape'  in  the  soil  or 
picking  up  pieces  of  grass,  &c,  after  copulation.  There  is  certainly, 
in  many  birds,  a  close  connexion  between  nest-building  and  copula- 
tion. Ritual  offering  of  nest-material  is  an  important  element  in  many 
courtship  displays  and  in  some  species  (e.g.  magpie)  male  birds  may 
build  extra  nests. 

The  nest  is  therefore  often  at  first  a  sex  site  and  its  position  may  be 
chosen  by  the  male.  The  actual  building  of  the  nest  is  done  very 
variously.  Sometimes  the  male  brings  the  material  and  the  female 
uses  it.  She  may  do  the  fetching  as  well,  perhaps  accompanied  by  the 
lazy  male;  or  he  may  have  nothing  to  do  with  the  whole  business.  The 
nest  is  built  by  means  of  a  limited  number  of  stereotyped  movements, 
which  are  characteristic  of  the  species.  The  integration  of  these  move- 
ments into  a  functional  sequence  of  behaviour  depends,  however,  on 
experience.  Nest  building  and  copulation  occur  at  about  the  same 
stage  of  the  reproductive  cycle  and  both  can  be  induced  by  oestrogen 
(in  canaries). 

The  complicated  forms  of  nest  are  found  only  in  passerine  birds; 
in  others  it  is  usually  simply  a  hollow  in  the  ground  or  a  heap  of  sticks. 
The  more  elaborate  nests  show  many  protective  devices ;  in  temperate 
regions,  where  predators  come  largely  from  below,  the  nests  are  often 
open,  but  where  there  are  many  snakes  they  are  mostly  domed  or 
hung  from  branches  or  provided  with  a  long  tubular  entrance  (weavers). 

In  building  the  nest  the  bird  follows  a  set  pattern,  laid  down  in 
some  way  by  the  method  of  working  of  its  brain  and  showing  no  sign 
of  foreknowledge  of  the  result.  Young  birds,  however,  build  rougher 
nests  than  mature  ones.  Weaver  birds  reared  by  hand  for  four  genera- 
tions made  perfect  nests  of  a  type  which,  of  course,  they  had  never 
seen.  On  the  other  hand,  it  has  been  claimed  that  canaries  deprived  of 


5°6 


BIRD  BEHAVIOUR 


XVII.  10- 


nest-building  materials  for  some  generations  then  build  clumsily  at 
first,  though  they  quickly  improve. 

The  methods  used,  of  course,  vary  with  the  materials.  Many  of  them 
involve  most  elaborate  tying  of  grasses  to  the  branches,  which  is  done 
with  the  beak  or  the  feet  or  both  (Fig.  306).  The  shape  and  construc- 
tion of  the  nest  varies  with  the  habits  of  the  bird.  Many  sea-birds, 
nesting  safely  on  the  cliffs,  make  only  very  simple  nests  or  none  at  all. 


Fig.  306.  Process  of  nest-building  by  a  weaver  bird  (Quelea).  The  arrows  show 

directions  in  which  the  piece  is  pulled.  A,  the  points  of  holding  by  the  beak; 

4,  5,  and  6  show  successive  stages  of  co-operative  weaving  by  the  foot  and  beak. 

(From  Stresemann,  after  Friedmann.) 

In  such  birds  as  the  plovers  or  larks  the  nest  is  a  cup  in  the  earth,  the 
eggs  being  procryptically  coloured  with  a  blotched  green  and  brown 
pattern,  so  that  it  is  very  difficult  to  see  them  on  the  spring  ploughland 
or  partly  green  earth.  Nests  constructed  in  trees  vary  from  the  simple 
sticks  of  rooks  or  pigeons  to  the  elaborate  domed  and  lined  nests  of 
many  passerines.  The  nest  is  woven  from  materials  brought  in  with 
the  beak  and  often  lined  with  moss  or  in  ducks  with  feathers  from  the 
breast  of  the  bird.  The  thrush  lines  its  nest  with  mud  moistened  with 
saliva  and  the  swift  makes  nearly  the  whole  nest  of  saliva.  Many  birds 
build  roughly  and  often  use  the  old  nests  of  others,  for  instance,  kes- 
trels are  often  found  using  the  nests  of  crows.  Others  build  in  burrows, 


xvii.  ia  EGGS  507 

either  accidental  or,  in  kingfishers,  made  by  the  bird  itself.  Similarly, 
holes  already  in  trees  may  be  used  (tit-mice),  but  the  woodpeckers 
drill  their  own  holes.  The  female  hornbill  walls  herself  into  a  hole 
in  a  tree  with  the  help  of  mud  brought  by  the  male  and  for  the  three 
months  of  incubation  she  is  fed  by  the  male  through  a  small  aperture. 
In  the  brush  turkeys  (Megapodes)  the  eggs  are  not  incubated  by  the 
bird  but  are  buried  in  a  mound  of  decaying  material,  which  provides 
the  necessary  heat;  the  young  bird  is  independent  from  the  moment 
it  hatches. 

The  bower-birds  of  Australia  and  New  Guinea  are  passerines  in 
which  the  male  builds  an  elaborate  structure  of  plants,  ornamented 
with  bright  objects.  Here  he  displays  to  a  female  and  sings.  A  bower 
that  is  left  may  be  destroyed  by  another  male  and  its  decorations 
stolen.  The  male  constantly  refurbishes  his  bower  and  gyrates  round 
it,  tossing  the  decorations  violently.  This  seems  to  be  a  form  of  dis- 
placement activity.  When  the  female  ultimately  becomes  receptive 
copulation  occurs,  the  bower  often  being  demolished  in  the  act.  The 
eggs  are  laid  in  a  nest  nearby. 

11.  Shape  and  colour  of  the  eggs 

Eggs  are  as  varied  as  the  rest  of  bird  structures.  The  shape  is 
determined  by  the  pressure  of  the  oviducal  wall  and  the  blunt  end 
always  emerges  first.  With  lesser  pressure  from  behind  the  egg 
approaches  a  spherical  shape.  The  pointed  end  may  serve  to  prevent 
the  eggs  rolling  away  (guillemot)  or  to  help  the  eggs  to  fit  together 
(plover).  The  pigment  is  laid  down  at  the  end  of  the  travel  along  the 
oviduct  and  is  derived  from  the  bile  pigments.  The  coloration  is 
usually  procryptic  in  eggs  laid  on  the  ground,  whereas  those  laid  in 
holes  are  white  and  birds  like  the  pigeons  that  do  not  attempt  to 
protect  themselves  or  their  nests  by  concealment  also  have  light- 
coloured  eggs.  The  significance  of  the  varied  colours  of  eggs  that  are 
not  procryptic  is  obscure.  It  is  likely  that  they  serve  as  a  stimulus  to 
the  brooding  bird,  who  will  sometimes  leave  a  nest  when  a  wrong- 
coloured  egg  is  inserted.  A  further  sign  of  this  is  that  there  are 
various  races  of  cuckoo,  each  laying  eggs  appropriate  to  the  nest  it 
parasitizes;  but  the  genetics  and  behaviour  of  cuckoos  are  still  very 
obscure  subjects. 

12.  Brooding  and  care  of  the  young 

Usually  it  is  the  hen  who  broods  the  eggs,  but  the  cock  may  assist 
and  in  a  very  few  species  he  does  all  the  brooding.  Brooding  is  not  a 
mere  sitting  on  the  eggs,  but  depends  on  the  development  of  a  vascular 


5o8  BIRD  BEHAVIOUR  xvn.  12 

response  in  a  part  of  the  skin,  the  brood  spots,  produced  by  a  local 
moult  of  the  feathers.  At  hatching  the  parents  may  assist  the  action  of 
the  caruncle  of  the  young.  The  care  of  the  nestlings  is  a  very  elaborate 
business  in  most  birds,  involving  many  separate  actions.  The  young 
are  warmed,  fed,  and  occasionally  watered,  and  in  many  species  the 
nest  is  kept  clean  by  careful  removal  of  the  faeces,  which  may  be 
produced  as  pellets  enclosed  in  a  skin  of  mucus;  these,  being  shining 
white,  are  eaten  by  the  parents.  In  warm  climates  the  parents  may 
shield  the  nestlings  from  the  sun  during  the  heat  of  the  day. 

The  work  of  caring  for  the  young  birds  is  often  performed  by  both 
parents  and  there  are  various  adaptations  to  ensure  this.  The  young 
react  strongly  to  the  return  of  the  parents  to  the  nest,  usually  by  open- 
ing the  beak  and  displaying  the  coloured  inside  of  the  mouth,  an 
action  that  strongly  stimulates  the  parent,  releasing  the  feeding 
behaviour,  which  varies  with  the  species.  The  young  pigeon  thrusts 
its  bill  into  the  throat  of  the  adult  to  collect  the  milk  secreted  by  the 
crop.  It  is  probable  that  this  careful  attention  by  the  parents  is 
ensured  by  a  series  of  somewhat  simple  stimulus  reactions.  For 
example,  Eliot  Howard  showed  that  a  female  linnet  responds  to  its 
own  nest  rather  than  to  its  own  young.  When  its  young  were  put  into 
an  abandoned  nest  and  the  latter  placed  near  to  its  own  the  hen 
usually  returned  to  its  nest  and  neglected  the  young,  though  the  male 
gave  them  some  food.  Cuckoos  similarly  make  use  of  this  undiscrimin- 
ating  'instinctive'  behaviour;  birds  will  feed  any  young  that  provide 
the  appropriate  stimulus  and  if  no  young  appear  they  will  make  little 
effort  to  find  them. 

The  rate  of  development  after  hatching  varies  greatly.  In  the  gal- 
linaceous birds,  in  many  ways  a  primitive  group,  the  young  are  well- 
developed  at  hatching  and  soon  fend  for  themselves  (nidifugal).  In 
nidicolous  species,  on  the  other  hand,  the  young  is  naked  and  helpless, 
it  is  a  growing  machine,  with  a  large  liver  and  digestive  system  but 
little  developed  nervous  system.  Yet  the  birds  of  these  species  ulti- 
mately have  much  larger  brains  and  are  more  'intelligent'  than  those 
that  leave  the  nest  soon  after  hatching. 


XVIII 

THE  ORIGIN  AND  EVOLUTION  OF  BIRDS 

1.  Classification 

Class  Aves. 
^Subclass  i.  Archaeornithes.  Jurassic 

*Archaeopteryx 
Subclass  2.  Neornithes 
*Superorder  i.  Odontognathae.  Cretaceous 

*Hesperomis;  *Ichthyornis 
Superorder  2.  Palaeognathae.  Ratites.  Cretaceous-Recent 

Struthio;  Rhea;  Dromiceius;  Casuarius;  *Dinortiis;  *Aepyornis; 
Apteryx;  Tinamus 
Superorder  3.  Impennae.  Penguins.  Eocene-Recent 

Spheniscus;  Aptenodytes 
Superorder  4.  Neognathae.  Cretaceous-Recent 
Order  1.  Gaviiformes.  Loons 

Gavia,  loon 
Order  2.  Colymbiformes.  Grebes 

Colymbus  (=  Podiceps),  grebe 
Order  3.  Procellariiformes.  Petrels 

Fulmarus,  petrel;  Puffinus,  shearwater;  Diomedea,  albatross 
Order  4.  Pelecaniformes.  Cormorants,  Pelicans,  and  Gannets 
Phalacrocorax,  cormorant;  Pelecanus,  pelican;  Sida,  gannet 
Order  5.  Ciconiiformes.  Storks  and  Herons 

Ciconia,  stork;  Ardea,  heron;  Phoenicopterus,  flamingo 
Order  6.  Anseriformes.  Ducks 

Anas,  duck;  Cygnus,  swan 
Order  7.  Falconiformes.  Hawks 
Falco,  kestrel;  Aquila,  eagle;  Buteo,  buzzard;  Neophron,  vulture; 
Milvus,  kite 
Order  8.  Galliformes.  Game  birds 

Gallus,  fowl;  Phasianus,  pheasant;  Perdix,  partridge;  Lagopus, 
grouse;  Meleagris,  turkey;  Numida,  guinea  fowl;  Pavo,  pea- 
cock; Opisthocomns,  hoatzin 
Order  9.  Gruiformes.  Rails 

FnJica,    coot;    Gallinula,    moorhen;    Crex,    corn-crake;    Grus, 
crane;  *Phororhacos;  *Diatryma 


5io  EVOLUTION  OF  BIRDS  xvm.  i- 

1.  Classification  (cont.) 

Order  10.  Charadriiformes.  Waders  and  Gulls 

Numenius,  curlew;  Capella,  snipe;  Calidris,  sandpiper;  Vanellus, 
lapwing;  Scolopax,  woodcock;  Larus,  gull;  Uria,  guillemot; 
Plautus,  little  auk 
Order  n.  Columbiformes.  Pigeons 
Columba,  pigeon;  *Raphus,  dodo 
Order  12.  Cuculiformes.  Cuckoos 

Cuculus,  cuckoo 
Order  13.  Psittaciformes.  Parrots 
Order  14.  Strigiformes.  Owls 

Athene,  little  owl;  Tyto,  farm  owl;  Strix,  tawny  owl 
Order  15.  Caprimulgiformes.  Nightjars 

Caprimulgus,  nightjar 
Order  16.  Micropodiformes.  Swifts  and  humming-birds 

Apus,  swift,  Trochilus,  humming-bird 
Order  17.  Coraciiformes.  Bee-eaters  and  kingfishers 

Merops,  bee-eater;  Alcedo,  kingfisher 
Order  18.  Piciformes.  Woodpeckers 

Picus,  woodpecker 
Order  19.  Passeriformes.  Perching  birds 

Corvus,  rook;  Sturnns,  starling;  Fringilla,  finch;  Passer,  house- 
sparrow;  Alauda,  lark;  Anthus,  pipit;  Motacilla,  wagtail; 
Certhia,  tree-creeper;  Parus,  tit;  Lanius,  shrike;  Sylvia, 
warbler;  Turdus,  thrush;  Erithacus,  British  robin;  Luscinia, 
nightingale;  Prunella,  hedge-sparrow;  Troglodytes,  wren; 
Hirundo,  swallow 

2.  Origin  of  the  birds 

Many  characteristics  of  birds  show  close  resemblance  to  those  of 
reptiles  and  in  particular  to  the  archosaurian  diapsids.  Already  in  the 
early  Triassic  period  the  small  pseudosuchians  such  as  *Enparkeria 
(p.  417)  showed  the  essential  characteristics  of  the  bird  group,  especi- 
ally those  associated  with  a  bipedal  habit.  From  some  such  form 
the  birds  have  almost  certainly  been  derived,  by  a  series  of  changes 
parallel  in  many  cases  to  those  found  in  other  descendants  of  the 
pseudosuchians,  such  as  the  crocodiles,  dinosaurs,  and  pterosaurs. 

3.  Jurassic  birds  and  the  origin  of  flight 

We  have  no  detailed  evidence  of  the  stages  by  which  cold-blooded 
terrestrial  reptiles  were  transformed  into  warm-blooded  flying  birds, 


xviii.  3 


ARCHAEOPTER  YX 


5" 


mfL^d, 


Fig.  307.  Restored  skeleton  of  *Archaeopteryx,  compared  with  the  skeleton  of  a 

pigeon  drawn  on  a  more  reduced  scale. 

c.  carpal;  el.  clavicle;  eo.  coracoid;  d.  digits;  /.  femur;  fi.  fibula;  /*.  humerus;  i.  ilium; 

is.  ischium;  trie,  metacarpals;  mt.  metatarsals;  p.  pubis;  py.  pygostyle;  r.  radius;  s.  scapula; 

st.  sternum;   t"i.  tarso-metatarsus;   It.   tibiotarsus;   u.  ulna;  v.  ventral  ribs;   I-IV,  toes. 

(From  Heilmann,  The  Origin  of  Birds,  II.  F.  &  C.  Witherby,  Ltd.) 

but  two  fossil  specimens  from  the  upper  Jurassic  rocks  of  Bavaria 
show  us  one  intermediate  stage  on  the  way  (Fig.  307).  These  *Archae- 
opteryx  certainly  had  achieved  some  powers  of  flight  or  gliding,  but 
they  were  less  specialized  for  the  purpose  than  are  modern  birds. 
The  whole  body  axis  was  still  elongated  and  lizard-like.  The  vertebrae 
articulated  by  simple  concave  facets  as  in  reptiles,  without  the  saddle- 


EVOLUTION  OF  BIRDS 


512  £,VUL,UIlUi\    Ur    I31KJJS  XVIII.  3- 

shaped  articular  facets  of  the  centrum  seen  in  birds.  The  dorsal 
vertebrae  were  not  fixed  and  only  about  five  went  to  make  up  the 
sacrum.  There  was  a  long  tail,  with  feathers  arranged  in  parallel  rows 


Fig.  308.  Skulls  of  A,  *Euparkeria;  B,  *Archaeopteryx;  C,  Culumba. 

A.  angular;  Al.  adlachrymal ;  Ar.  articular;  Bo.  basi-occipital;  C.  condyle;  D.  dentary; 
E.  eye  with  sclerotic  ring ;  F.  frontal ;  J.  jugal ;  L.  lachrymal ;  Mx.  maxilla ;  N.  nasal ;  O.  occi- 
pital; Op.  opisthotic;  P.  parietal;  Pa.  palatine;  Pf.  post-frontal;  Pm.  premaxilla;  Po.  post- 
orbital;  Pt.  pterygoid;  Q.  quadrate;  Qj.  quadratojugal;  S.  squamosal;  Sa.  sur-angular; 
Sp.  splenial.  (From  Heilmann,  The  Origin  of  Birds,  II.  F.  &  C.  Witherby,  Ltd.) 

along  its  sides,  probably  an  important  organ,  as  in  other  animals 
that  live  in  trees  and  jump  and  glide.  The  fore-limb  ended  in  three 
clawed  digits,  with  separate  metacarpals  and  phalanges,  the  hallux 
being  opposable.  The  limb  was  used  as  a  wing,  for  the  fossils  show 
feathers  on  the  back  of  the  ulna  and  hand,  but  the  wing  area  was  small 
and  the  shape  rounded,  like  that  of  the  wing  of  birds  that  fly  for 


xviii.  4  CRETACEOUS  BIRDS  513 

short  distances  only.  There  was  a  furculum  and  a  small  sternum.  The 
ribs  were  slender  and  had  no  uncinate  processes.  The  pelvic  girdle 
and  hind  limb  resembled  those  of  archosaurs,  with  elongated  ilium 
and  backwardly  directed  pubis.  Only  six  vertebrae  were  fused  to  form 
the  sacrum  (at  least  eleven  in  birds).  The  fibula  was  complete  and  the 
proximal  tarsals  were  free,  but  the  distal  ones  were  united  with  the 
metatarsals. 

In  the  skull  of  *Archaeopteryx  (Fig.  308)  there  were  teeth  in  both 
jaws.  The  shape  was  more  reptilian  than  bird-like,  with  rather  small 
eyes  and  brain,  and  premaxillae  and  frontals  much  smaller  than  in 
modern  birds.  There  was  a  large  vacuity  in  front  of  the  eye  and  prob- 
ably there  were  post-frontal  and  post-orbital  bones.  The  condition 
of  the  temporal  region  is  unfortunately  not  clear  on  account  of  the 
crushing  of  the  material.  The  brain-case  was  large  and  many  of  the 
bones  were  united,  as  in  modern  birds.  The  bones  were  not  pneuma- 
tized.  The  cerebral  hemispheres  were  elongated  as  in  reptiles  and  the 
cerebellum  was  small. 

These  very  interesting  fossils  suggest  that  the  birds  arose  from  a 
race  of  bipedal  arboreal  reptiles,  living  in  forests  and  accustomed  to 
running,  jumping,  and  gliding  among  the  branches  (Fig.  309).  There 
has  been  much  controversy  about  the  origin  of  flight,  some  maintain- 
ing that  the  earliest  birds  were  terrestrial  and  used  the  wings  to 
assist  in  running,  leading  eventually  to  a  take-off,  perhaps  at  first  for 
short  distances.  The  claws  and  long  tail  of  *Archaeopteryx  speak 
definitely  against  this  view  and  in  favour  of  a  gliding  origin  for  flight. 

4.  Cretaceous  birds.  Superorder  Odontognathae 

These  Jurassic  fossils  are  so  distinct  from  other  birds  that  they  are 
placed  in  a  distinct  subclass  *Archaeornithes.  All  other  known  living 
and  extinct  birds  have  a  short  tail,  reduced  hand,  a  sternum,  and  other 
characteristics  of  the  subclass  Neornithes.  A  few  fossils  are  known 
from  the  upper  Cretaceous  in  which  certain  reptilian  characteristics 
are  still  preserved.  *Hesperornis  probably  possessed  teeth.  Another 
Cretaceous  bird  skull  (*Ichthyornis)  was  found  associated  with  a  toothed 
jaw,  but  the  latter  is  now  believed  to  have  belonged  to  a  mosasaur. 
However,  the  two  birds  are  placed  in  a  superorder  *Odontognathae. 
They  were  aquatic  birds,  and  the  former  was  a  diver  that  had  lost  the 
power  of  flight. 

Already  in  the  Cretaceous  there  were  some  birds  that  had  lost  the 
teeth  and  can  be  referred  to  orders  found  alive  today.  Birds  are  not 
commonly  found  as  fossils,  however,  and  it  is  not  possible  to  give 


5H  EVOLUTION  OF  BIRDS  xvm.  4- 

a  detailed  history  of  the  evolution  of  the  various  orders  that  are 
recognized.  We  do  not  even  know  whether  bird  life  first  became 
abundant  after  the  Cretaceous,  at  the  same  time  as  the  mammals 
began  to  be  numerous. 

5.  Flightless  birds.  Superorder  Palaeognathae 

The  flightless  birds  or  'ratites',  such  as  the  ostrich,  cassowary,  and 
kiwi,  with  reduced  wings  and  no  sternal  keel,  long  legs  and  curly 
feathers,  have  in  the  past  been  placed  in  a  distinct  group  and  regarded 
as  primitive.  Indeed,  it  has  even  been  suggested  that  they  diverged 
so  early  from  the  ancestral  avian  stock  that  they  never  passed  through 
a  flying  stage.  Recently,  however,  de  Beer  and  others  have  pointe'  out 
that  certain  of  their  allegedly  primitive  characters,  such  as  the  arrange- 
ment of  the  palate  bones,  may  be  regarded  as  manifestations  of  neoteny 
and  do  not  indicate  a  truly  primitive  condition.  Some  neognathous 
birds  pass  through  a  palaeognathous  stage  during  development.  The 
evidence  strongly  suggests  that  the  'ratites'  have  been  descended  from 
flying  birds  and  are  not  a  natural  group,  but  represent  several  different 
evolutionary  lines.  The  detailed  relationship  of  these  is  still  obscure 
and  for  convenience  they  are  retained  in  a  superorder  Palaeognathae. 

The  various  ratite  birds  have  been  placed  in  as  many  as  eight  dis- 
tinct orders,  but  the  orders  of  the  ornithologist  generally  represent 
lesser  degrees  of  difference  than  are  usual  elsewhere  in  the  animal 
kingdom.  The  ostriches  (Struthio)  are  the  largest  living  birds,  now 
limited  to  Mesopotamia.  The  rhea  (Rhea)  occupies  the  same  ecological 
position  in  South  America  and  the  emu  (Dromiceius)  and  cassowary 
(Casuarius)  in  Australasia.  The  moas  (*Dinornis)  were  another  type; 
several  species  lived  in  New  Zealand  until  recent  times.  The  elephant- 
birds  (*Aepyornis)  were  similar,  with  several  species  in  Madagascar 
in  the  Pleistocene.  Some  were  larger  than  ostriches,  with  eggs 
estimated  to  weigh  more  than  10  kg,  presumably  the  largest  single 
cells  that  have  existed! 

The  kiwis  (Apteryx)  of  New  Zealand  are  smaller,  terrestrial  birds 
whose  relationship  to  the  ratites  is  doubtful.  They  are  nocturnal  and 
insectivorous  or  worm-eating,  with  a  long  beak  and  small  eyes.  The 
sense  of  smell  and  the  parts  of  the  brain  related  to  it  are  better 
developed  than  in  other  birds;  it  is  not  clear  whether  this  is  the 
retention  of  a  primitive  feature.  The  palate  shows  large  basipterygoid 
processes.  There  is  a  penis,  as  in  other  ratites. 

Still  more  doubtful  is  the  position  of  the  tinamus  (Tinamus),  ter- 
restrial birds  rather  like  hens,  of  which  about  fifty  species  are  found 


xvm.  6 


PENGUINS 


5*5 


Fig.  309.  Restoration  of  hypothetical  proavian.  (From  Heilmann,  The  Origin  of  Birds, 

H.  F.  &  C.  Witherby,  Ltd.) 

throughout  South  America.  They  show  similarities  to  the  ratites  in 
the  palate  and  other  features  and  may  be  placed  among  the  Palaeo- 
gnathae.  Probably,  like  the  more  typical  ratites,  they  are  an  early 
offshoot  that  has  long  developed  independently. 


6.  Penguins.  Superorder  Impennae 

The  penguins  (Spheniscus)  are  birds  that  early  lost  the  power  of 
flight  and  became  specialized   for  aquatic  life.  They  may  have  a 


5i6  EVOLUTION  OF  BIRDS  xvm.  6- 

common  ancestry  with  the  petrels.  Unlike  most  other  water-birds  they 
swim  chiefly  by  means  of  the  fore-limbs,  modified  into  flippers;  the 
feet  are  webbed.  The  penguins  are  mainly  confined  to  the  southern 
hemisphere.  They  come  ashore  to  breed;  many  make  no  nests,  but 
sometimes  carry  the  one  or  two  eggs  on  the  feet  throughout  the 
incubation  period.  The  emperor  penguin  breeds  in  winter  on  the 
Antarctic  ice  and  is  the  only  bird  that  never  comes  on  land.  The  egg 
is  supported  on  the  feet. 

7.  Modern  birds.  Superorder  Neognathae 

All  the  remaining  birds  have  the  characteristic  palate,  sternum,  and 
other  features  already  described  and  are  placed  in  a  single  group  as  the 
superorder  Neognathae.  Birds  of  this  type  probably  existed  in  the 
Cretaceous  and  many  of  the  orders  are  known  from  Eocene  times,  but 
the  fossil  evidence  is  not  adequate  for  us  to  be  able  to  say  when  they 
became  numerous  and  differentiated  as  they  are  now.  The  existing 
birds,  as  has  already  been  suggested,  show  very  great  variety  of  details 
of  structure  and  habits,  superimposed  on  a  common  basic  plan. 
Classification  of  the  vast  number  of  genera  involves  recognition  of 
over  forty  distinct  orders  and  even  then  one  of  the  orders,  the  Passeri- 
formes,  contains  about  half  of  all  the  species.  Unfortunately,  little  can 
be  done  in  a  short  space  towards  describing  the  great  variety  of  bird 
life.  We  can  only  list  the  important  orders,  mentioning  a  few  of  the 
characteristics  of  some  of  the  more  interesting  types.  Birds  are  so 
conspicuous  that  their  species  have  been  very  fully  described,  there 
are  about  25,000  well-defined  species  and  subspecies.  The  arrange- 
ment of  the  orders  adopted  for  the  survey,  Birds  of  the  World,  by 
J.  L.  Peters  has  been  used  here. 

Order  1.  Gaviiformes.  Loons 

The  divers  are  aquatic  birds  retaining  some  primitive  characteristics. 
They  are  birds  of  open  waters,  feeding  mainly  on  fishes.  Various 
species  of  Gavia  live  mostly  on  the  sea,  but  breed  by  lakes  throughout 
the  holarctic  region. 

Order  2.  Colymbiformes.  Grebes 

The  grebes  (Colymbus  =  Podiceps)  (Fig.  303)  are  also  aquatic  birds, 
almost  unable  to  walk  on  land.  They  resemble  the  divers  in  some 
ways,  but  are  perhaps  not  closely  related  to  them.  They  nest  on  lakes, 
laying  a  small  number  of  white  eggs  in  a  floating  nest. 


xviii.  7  ORDERS  OF  BIRDS  517 

Order  3.  Procellariiformes.  Petrels 

The  petrels  (Fulmarus),  shearwaters  (Puffinus),  and  albatrosses 
(Diomedea)  are  birds  highly  modified  for  oceanic  pelagic  life,  some  of 
them  very  large.  They  lay  one  white  egg,  often  in  burrows.  Their 
long  narrow  wings  are  specialized  for  soaring  flight  (Fig.  273). 

Order  4.  Pelecaniformes.  Cormorants,  Pelicans,  and  Gannets 

This  is  another  order  of  aquatic  birds,  much  modified  for  diving 
and  fishing  and  including  the  cormorants  (Phalacrocorax),  pelicans 
(Pelecanus),  and  gannets  (Sida).  They  nest  in  colonies  on  rocks  or 
trees;  the  eggs  are  usually  unspotted  and  covered  with  a  rough  chalky 
substance.  These  birds  make  spectacular  dives  when  fishing;  gannets 
may  plunge  from  more  than  50  feet. 

Order  5 .  Ctconiiformes.  Storks  and  Herons 

The  storks  (Ciconia),  herons  (Ardea)  (Fig.  274),  and  flamingoes 
(Phoenicopterus)  are  large,  long-legged  birds,  living  mostly  in  marshes 
and  feeding  mainly  on  fish.  They  are  strong  flyers  and  some  of  them 
perform  extensive  migrations.  Nests  are  usually  in  colonies  and  may 
be  used  year  after  year;  there  are  elaborate  display  ceremonies.  Eggs 
are  few  and  unspotted. 

Order  6.  Anseriformes.  Ducks 

The  ducks  (A?ias)  and  swans  (Cygnns)  represent  yet  another  group 
of  birds  specialized  for  aquatic  life.  The  characteristic  flattened  bill 
is  used  to  feed  on  various  diets.  Some  are  vegetarians,  a  few  filter- 
feeders;  some  eat  molluscs,  others  fish.  The  numerous  eggs  are  usually 
white  or  pale  and  the  nest  is  built  on  the  ground. 

Order  7.  Falconiformes.  Hawks 

This  order  includes  the  birds  of  prey  that  hunt  by  day,  having 
sharp,  strong,  curved  bills  and  powerful  feet  and  claws.  The  retina 
contains  mainly  cones.  Many  different  types  are  found  throughout 
the  world.  Most  feed  on  birds  or  mammals,  some  on  carrion,  and  a 
few  on  fish  or  reptiles.  Typical  examples  are  the  kestrel  (Falco),  eagle 
(Aquila),  buzzard  (Buteo),  and  vulture  (Neophron).  The  eggs,  few  in 
number,  are  usually  spotted  and  the  nests  are  generally  made  on  cliffs, 
tree-tops,  or  other  inaccessible  places;  some,  however,  are  on  the 
ground. 


5i8 


EVOLUTION  OF  BIRDS 


xviii.  7 


Order  8.  Galliformes.  Game  birds 

These  are  mainly  terrestrial,  grain-eating  birds,  capable  only  of 
short,  rapid  flights ;  some  of  their  structural  characters  and  habits  are 
certainly  primitive.  The  palate  differs  from  both  that  of  ratites  and 
of  most  modern  birds,  suggesting  an  early  divergence.  There  is  often 
a  marked  difference  in  plumage,  and  sometimes  in  size,  between  the 
sexes.  The  nest,  usually  made  on  the  ground,  is  simple  and  the  eggs 
numerous,  white,  or  spotted.  The  young  develop  very  quickly  after 
birth.  The  order  contains  many  successful  types  and  is  of  world- 


^3== 


Fig.  310.  Claws  on  hand  of  the  hoatzin 

(Opisthoco??ius),  I,  in  nestling;  II,  adult. 

(After  Parker  and  Heilmann.) 

wide  distribution.  It  includes  Gallus,  the  jungle-fowl  of  India,  and  all 
its  domesticated  descendants,  also  Phasianus  and  other  pheasants, 
Perdix  (partridge),  Lagopus  (grouse),  Meleagris  (turkey),  Numida 
(guinea-fowl)  and  Pavo  (peacock).  The  Megapodes  or  mound- 
builders  of  the  Australasian  and  east  Indian  regions  lay  their  eggs  in 
mounds  of  decaying  leaves  and  earth.  In  Opisthocomus,  the  hoatzins 
of  tropical  South  America,  one  of  the  few  tree  forms,  the  young 
possess  well-marked  claws  on  the  digits  of  the  wing  (Fig.  310),  which 
they  use  for  climbing.  These  claws  are  usually  considered  to  be  a 
secondary  development ;  their  resemblance  to  the  claws  of  *Archaeo- 
pteryx  is  remarkable. 

Order  9.  Gruiformes.  Rails  and  Cranes 

The  rails  are  mostly  secretive,  terrestrial  birds,  compressed  laterally 
and  often  living  in  marshy  country  and  having  an  omnivorous  diet; 
common  British  members  are  the  coots  (Fulica)  and  moorhens  (Gal- 
linula).  They  run,  swim,  and  dive  easily,  but  are  poor  flyers;  they 
build  rather  simple  nests  and  lay  numerous,  often  dark-spotted  eggs. 
Crex  (the  corncrake)  and  other  landrails  are  of  more  terrestrial 
habit.  The  cranes  (Grus)  are  long-legged  birds  found  in  swamps 


win.  7  ORDERS  OF  BIRDS  519 

and  probably  allied  to  the  rails  rather  than  to  the  waders  as  is  still  often 
supposed. 

Possibly  related  to  the  rails  are  the  cariamas  of  South  America, 
carnivorous  birds  with  very  long  legs,  hardly  able  to  fly,  living  largely 
on  reptiles.  The  Miocene  *Phororhacos  was  a  similar  bird,  reaching 
6  feet  high;  evidently  the  group  was  successful  in  a  region  free  of 
mammalian  carnivores.  *Diatryma  was  an  even  larger  flightless  car- 
nivorous bird,  found  in  the  Eocene  of  Europe  and  North  America 
and  perhaps  also  related  to  the  early  ancestors  of  the  Gruiformes, 
though  usually  classified  in  a  separate  order,  or  near  the  herons. 

Order  10.  Charadriiformes.  Waders  and  Gulls 

This  is  a  large  order  including  the  wading  birds  and  the  gulls,  terns, 
and  auks,  which  have  evolved  from  them.  The  typical  waders  are 
birds  that  live  mainly  on  the  ground,  often  inhabiting  open  watery 
places  or  marshes.  They  are  usually  gregarious  out  of  the  breeding- 
season  and  are  often  very  numerous  on  the  sea-shore.  They  often 
have  long  legs  and  long  bills  and  feed  chiefly  on  small  invertebrates. 
The  curlews  (Numenius),  snipe  (Capella),  and  sandpipers  (Calidris)  are 
well-known  examples.  The  lapwings  (Vanellus)  and  related  plovers 
are  birds  found  on  drier  land  than  is  usual  among  other  waders;  the 
woodcocks  (Scohpax)  inhabit  swampy  woods. 

The  gulls  (e.g.  Larus)  are  a  very  important  group  of  birds  derived 
from  the  waders  and  adapted  to  life  by  and  on  the  sea.  Usually  they 
have  a  grey  or  white  colour,  often  with  black  head  and  wing-tips.  The 
young  are  usually  darker  than  the  adults  and  mottled  with  brown. 
The  guillemots  (Uria)  and  little  auks  (Plautus)  are  more  fully  marine 
animals,  breeding  in  very  large  colonies  on  the  cliffs. 

Order  1 1 .  Columbijormes.  Pigeons 

The  pigeons  are  tree-living,  grain-  or  fruit-eating  birds,  mostly 
good  flyers  but  retaining  some  primitive  features.  They  are  of  world- 
wide distribution.  There  is  little  sexual  dimorphism;  the  nest  is 
usually  simple  and  the  eggs  normally  one  or  two  and  white.  The  young 
are  born  very  little  developed  and  are  nourished  by  the  'milk'  secreted 
by  the  crop  (p.  508).  The  dodo  (*Raphus  =  *Didus)  was  a  pigeon  that 
adopted  a  terrestrial  habit  in  the  island  of  Mauritius  and  grew  to  a 
large  size,  but  was  exterminated  by  man  in  the  seventeenth  century. 

Order  12.  Cuculiformes .  Cuckoos 

The  cuckoos  include  some  species  that  build  nests  but  many  lay 
their  eggs  in  those  of  other  birds.  In  the  common  cuckoo  (Cuculus), 


520  EVOLUTION  OF  BIRDS  xvm.  7 

any  one  individual  female  lays  mostly  in  the  nests  of  a  single  foster 
species,  in  England  often  the  meadow-pipit  or  hedge-sparrow.  She 
watches  the  building  of  the  nest  and  lays  her  egg  on  the  same  day  as 
the  foster  parent,  removing  one  of  the  clutch  before  she  does  so. 
Often  about  twelve  eggs  are  laid  in  this  way,  each  in  a  different  nest ; 
even  more  have  been  recorded.  The  eggs  are  usually  strongly  mimetic 
with  those  of  the  host,  variable  in  colour,  more  so  when  varied  host 
nests  are  available.  The  young  hatch  before  the  host  eggs,  which  are 
then  ejected  from  the  nest  by  the  young  cuckoo. 

Order  13.  Psittaciformes.  Parrots 

The  parrots  are  birds  found  mainly  in  warm  climates,  living  among 
the  trees  and  having  many  special  characteristics.  With  the  crows, 
they  are  usually  reckoned  to  be  the  most  'intelligent'  birds  and  cer- 
tainly have  considerable  powers  of  memory.  They  are  predominantly 
vegetarian  and  some,  though  by  no  means  all,  make  use  of  the  beak 
for  breaking  open  hard  shells.  The  eggs  are  usually  laid  in  holes  and 
are  white  and  round.  The  period  of  parental  care  after  hatching  is 
unusually  long  (2-3  months). 

Order  14.  Strigiformes.  Owls 

The  owls,  specialized  for  hunting  at  night,  resemble  the  hawks,  by 
convergence,  in  their  beaks,  claws,  and  in  other  ways.  The  food  is 
swallowed  whole.  They  probably  detect  their  prey  mainly  by  sound, 
and  show  various  specializations  in  the  ears.  The  eyes  contain  mostly 
rods  and  are  directed  forwards ;  they  are  very  large  and  they  cannot  be 
moved  in  the  orbits,  the  movements  of  the  neck  compensating  for  this 
restriction.  The  feathers  are  so  arranged  as  to  make  very  little  noise 
in  flight.  The  eggs  are  white  and  laid  in  holes  or  in  the  old  nests  of 
other  birds,  some  on  the  ground.  Many  genera  are  recognized  from 
all  parts  of  the  world,  examples  being  the  barn  owls  (Tyto)  and  the 
eared  owls  (Asio). 

Order  15.  Caprimulgiform.es.  Nightjars 

The  nightjars  (Caprimulgus)  are  a  rather  isolated  group  of  cre- 
puscular birds,  feeding  on  insects  taken  on  the  wing.  Two  mottled 
eggs  are  laid  on  the  bare  ground. 

Order  16.  Micropodiformes .  Swifts  and  Humming-birds 

The  swifts  (Apus)  and  humming-birds  (Trochilus)  are  perhaps  more 
fully  adapted  to  the  air  than  are  any  other  birds.  The  wings  are  very 


xvm.  7  ORDERS  OF  BIRDS  521 

long,  composed  of  a  short  humerus  and  long  distal  segments.  The 
swifts  are  insectivorous  and  have  very  large  mouths,  adapted  for 
feeding  on  the  wing.  The  nests  are  made  in  holes,  the  eggs  are  white, 
and  the  young  helpless  at  birth. 

Order  17.  Coraciiformes.  Bee-eaters  and  Kingfishers 

This  is  a  large  group  of  birds,  including  the  bee-eaters  (Merops), 
mainly  tropical  and  often  brightly  coloured.  The  three  anterior  toes 
are  united  (syndactyly).  The  nests  are  usually  made  in  holes  and  the 
eggs  are  white.  The  kingfishers  (Alcedo)  are  modified  for  diving  into 
the  water  to  catch  fish. 

Order  18.  Piciformes.  Woodpeckers 

The  woodpeckers  (Picus)  are  highly  specialized  climbing,  insecti- 
vorous, and  wood-boring  birds.  The  bill  is  very  hard  and  powerful 
and  the  tongue  long  and  protrusible  and  used  for  removing  insects 
from  beneath  bark.  The  tail  feathers  are  used  to  support  the  bird  as 
it  climbs  the  tree-trunk.  The  nest  is  made  in  a  hole  in  a  tree  and  the 
eggs  are  white. 

Order  19.  Passeriformes.  Perching  birds 

The  great  order  of  perching  birds  contains  about  half  of  all  the 
known  species.  They  are  birds  mostly  living  close  to  the  ground, 
rather  small,  and  of  very  varied  habits.  There  are  always  four  toes 
arranged  to  allow  the  gripping  of  the  perch.  The  display  and  nesting 
behaviour  is  usually  complicated,  with  a  well-developed  song  in  the 
male.  Many  species  build  very  complicated  nests  and  the  eggs  are 
often  brightly  coloured  and  elaborately  marked.  The  young  are  help- 
less at  birth.  Only  a  few  of  the  many  and  varied  types  can  be  men- 
tioned here. 

The  rooks  and  jackdaws  (Corvus)  are  the  largest  passerines  and 
perhaps  'highest'  of  all  birds;  they  are  mostly  colonial.  The  starlings 
(Sturnus)  are  also  partly  colonial  and  nest  in  holes.  The  finches 
(Frifigilla,  &c.)  are  seed-eating  birds  with  a  short,  stout,  conical  bill. 
The  house-sparrows  (Passer)  are  closely  related  to  the  finches  and 
have  become  commensals  of  man  all  over  the  world.  The  larks  (Alauda) 
make  their  nests  on  the  ground.  The  pipits  (Anthus)  and  wagtails 
(Motacilla)  are  somewhat  like  the  larks,  largely  terrestrial  birds  with 
slender  bills.  The  tree-creepers  (Certhia)  are  tree-living,  insectivorous 
birds  with  long  bills,  showing  some  convergent  resemblance  to  wood- 


522  EVOLUTION  OF  BIRDS  xvm.  7- 

peckers.  The  tits  (Parus,  &c.)  are  a  large  group  of  woodland  birds; 
they  chiefly  eat  insects,  also  buds  and  fruits.  The  shrikes  (Lanius) 
are  peculiar  among  passerines  in  being  mainly  carnivorous,  using 
their  strong  bills  to  eat  other  birds,  amphibia,  reptiles,  and  large 
insects. 

The  warblers  (Sylvia,  &c.)  make  a  very  large  group  of  woodland 
birds,  living  in  trees  or  scrub.  Related  to  them  are  the  thrushes  and 
blackbirds  (Turdus),  the  British  robins  (Erithacus),  and  nightingales 
(Luscinia),  mainly  eating  small  invertebrates,  also  fruits.  They  have  a 
very  wide  distribution  and  are  among  the  most  recently  evolved  and 
successful  members  of  the  whole  class.  The  hedge-sparrows  (Pru- 
nella) are  small  omnivorous  passerines,  possibly  related  to  the  thrush 
group.  The  wrens  (Troglodytes)  are  small  and  mainly  insectivorous. 
The  swallows  (Hirundo)  form  a  very  distinct  family  of  passerines, 
suited  for  powerful  flight  and  feeding  on  insects  caught  in  the  air. 
The  very  long  pointed  wings  and  'forked'  tail  allow  rapid  manoeuvring 
in  the  air  and  the  insects  are  taken  in  a  wide  mouth.  These  features, 
together  with  the  elaborate  migrations,  mark  the  swallows  as  among 
the  most  specialized  of  all  birds. 

8.  Tendencies  in  the  evolution  of  birds 

The  bird  plan  of  structure,  originating  in  the  Jurassic  period, 
perhaps  150  million  years  ago,  has  become  modified  to  produce  the 
great  variety  of  modern  birds.  In  trying  to  discover  the  factors  that 
have  influenced  this  modification  we  are  handicapped  by  the  poverty 
of  fossil  remains ;  it  is  not  possible  to  trace  out  individual  lines  as  it  is 
in  other  vertebrate  groups.  It  is  clear  that  the  process  of  change  has 
been  radical,  the  later  types  often  completely  replacing  the  earlier 
ones:  no  long-tailed  or  toothed  birds  remain  today. 

Our  knowledge  of  direction  of  the  change  is  largely  dependent  on 
study  of  the  variety  of  birds  existing  today,  which  is  perhaps  more 
thoroughly  known  than  in  any  other  group  of  animals.  In  the  reports 
of  those  who  have  studied  this  variation  there  are  two  distinct,  indeed 
opposite,  tendencies.  Many  have  observed  that  adaptive  radiation  has 
occurred;  birds  are  found  occupying  a  wide  variety  of  habitats,  with 
modifications  appropriate  to  each  way  of  life.  Other  workers,  record- 
ing minor  differences  between  races  occurring  in  different  areas, 
have  found  difficulty  in  believing  that  these  have  adaptive  significance. 
The  existence  of  such  'subspecies'  with  a  geographical  limitation  is  a 
striking  characteristic,  especially  conspicuous  in  widely  distributed 
species  such  as  the  chaffinch  (Fringilla).  On  continental  areas  such 


xviii.  8  BIRD  EVOLUTION  523 

subspecies  usually  grade  into  each  other  (making  'clines')  and  are 
interfertile  at  the  areas  where  they  meet.  On  the  other  hand,  where  a 
group  of  individuals  becomes  isolated  on  an  island,  or  by  some  other 
geographical  barrier,  it  may  become  infertile  with  the  'parent'  species. 
If  the  two  groups  again  come  to  occupy  a  common  area,  then  either 
one  eliminates  the  other  or  slight  modifications  of  habits  enable  the 
two  to  survive  side  by  side  as  two  distinct  'species'. 

Definite  cases  of  formation  of  new  species  in  this  way  have  been 
recorded  in  birds,  which  are  especially  suitable  for  such  study.  Thus 
in  the  Canary  Islands,  besides  a  local  form  of  the  European  chaffinch 
{Fringilla  coelebs)  there  is  the  blue  chaffinch  (F.  teydea),  which  was 
probably  originally  an  offshoot  from  the  European  form.  On  the 
mainland  F.  coelebs  inhabits  both  broad-leaved  and  coniferous  forests, 
but  in  Grand  Canary  F.  teydea  occupies  the  pine  woods,  F.  coelebs  the 
chestnut  and  other  woods.  On  the  island  of  Palma,  however,  the  blue 
chaffinch  is  absent  and  the  European  form  occupies  both  habitats.  It 
is  presumed  that  the  blue  form  is  more  suited  to  the  coniferous  woods, 
but  this  could  not  be  deduced  from  its  specific  characters  as  recorded 
by  a  systematist.  The  adaptive  significance  of  the  differences  between 
groups  of  animals  may  not  be  easy  to  discover,  but  it  is  most  unwise  to 
assume  that  it  does  not  exist  until  a  very  thorough  study  has  been 
made.  Detailed  observation  generally  shows  small  differences  in  habits 
and  behaviour  between  animals  occupying  what  seems  at  first  to  be 
a  single  'habitat'.  As  Lack,  who  has  studied  this  question  in  detail, 
puts  it,  'A  quick  walk  through  the  English  countryside  might  suggest 
that  there  is  a  wide  ecological  overlap  between  the  various  song-birds. 
In  fact,  close  analysis  shows  that  there  are  extremely  few  cases  in 
which  two  species  with  similar  feeding  habits  are  found  in  the  same 
habitat.'  The  differences  may  be  in  the  breeding  habitat,  as  in  the 
case  of  the  meadow,  tree,  and  rock  pipits  (Anthus pratensis,  A.  trivialis, 
and  A.  spinoletta).  The  spotted  and  pied  flycatchers  (Muscicapa  striata 
and  M.  hypoleuca)  catch  their  food  in  slightly  different  ways  and  the 
chiff-chaff  (Phylloscopus  collybita)  feeds  higher  in  the  trees  than  the 
willow  warbler  (P.  trochilus). 

A  complicating  factor  is  that  birds  that  occupy  similar  habitats 
for  one  part  of  the  year  may  migrate  to  different  regions,  for  instance, 
the  tree  and  meadow  pipits  and  the  chiff-chaff  and  willow  warbler. 

Birds  are  able  to  get  their  food  and  to  breed  in  many  different  ways, 
and  when  a  race  finds  a  situation  occupied  it  perhaps  often  survives 
by  a  slight  change  of  habits,  creating  a  new  'habitat'  not  previously 
occupied.  This  presumably  results  from  the  action  of  certain  indi- 


524 


EVOLUTION  OF  BIRDS 


xviii.  8- 


viduals  whose  constitution  differs  from  the  mean  of  the  race,  enabling 
them  to  pioneer.  It  is  not  certain  to  what  extent  individual  birds  are 
able  to  'adapt  themselves'  in  this  way  to  new  habitats.  Probably  the 
majority  of  the  members  of  any  population  are  limited  by  their 
structure  and  behaviour  pattern  to  a  rather  narrow  habitat  range. 

9.  Darwin's  finches 

A  remarkable  example  of  evolution  and  adaptive  radiation  is  pro- 
vided by  the  birds  of  the  Galapagos  Islands.  It  was  these  birds  and 


90°W 


85  W 


80  W 


90  W 


85  W 


80UW 


Fig.  311.  Position  of  the  Galapagos  Islands.  (From  Lack,  Darwin's  Finches, 
Cambridge  University  Press.) 

the  giant  tortoises  (after  which  the  islands  are  named)  that  started 
Darwin  on  his  study  of  evolution.  'In  July  opened  first  note-book  on 
"Transmutation  of  Species".  Had  been  greatly  struck  from  about 
month  of  previous  March  on  character  of  S.  American  fossils — and 
species  on  Galapagos  Archipelago — These  facts  origin  (especially 
latter)  of  all  my  views'  (Darwin's  Diary  1837). 

These  islands  are  volcanic  and  probably  of  Tertiary  ( ?  Miocene) 
date.  They  lie  on  the  equator,  600  miles  west  of  Ecuador,  the  only 
other  nearby  land  being  the  island  of  Cocos,  600  miles  north-west 
(Fig.  311).  Though  it  has  been  suggested  that  the  islands  were  con- 


xviii.  9  GALAPAGOS  BIRDS  525 

nected  by  a  land  bridge  with  South  America,  it  is  much  more  probable 
that  their  limited  stock  of  plants  and  animals  has  arrived  across  the 
sea.  Of  hundreds  of  species  of  land  birds  on  the  mainland,  descendants 
of  only  seven  species  are  found  in  the  Galapagos.  The  only  land 
mammals  are  a  rat  and  a  bat.  The  land  reptiles  include  giant  tortoises, 
iguanas,  a  snake,  one  lizard,  and  one  gecko.  There  are  no  amphi- 
bians and  only  a  limited  number  of  land  insects  and  molluscs.  There 
are  large  gaps  in  the  flora;  for  instance,  no  conifers,  palms,  aroids,  or 
Liliaceae.  This  fragmentary  flora  and  fauna  strongly  suggest  that  the 
islands  have  been  colonized  by  chance  transportation  across  the  sea, 
and  that,  once  arrived,  the  animals  and  plants  have  proceeded  to  settle 
not  only  in  the  habitats  they  occupied  on  the  mainland  but  also  in 
others,  not  filled,  as  in  their  homeland,  by  rivals.  Thus  the  tortoises 
and  iguanas,  arriving  presumably  by  chance,  have  grown  to  large  size, 
to  occupy  the  ecological  position  usually  taken  in  other  faunas  by 
mammalian  herbivores.  The  composite  plant  Scalesia  and  the  prickly 
pear,  Opimtia,  have  become  tall  trees  in  the  Galapagos.  We  have  here, 
therefore,  an  example  of  the  results  of  evolution  over  a  relatively 
limited  period  of  time  (perhaps  less  than  20  million  years)  from  a 
limited  number  of  initial  creatures,  and  this  provides  an  excellent 
opportunity  for  trying  to  discern  the  forces  that  have  been  at  work. 
There  are  thirteen  larger  islands  in  the  Galapagos  group,  the  largest 
80  miles  long.  They  are  separated  by  distances  of  up  to  100  miles  and 
several  of  the  peculiar  Galapagos  animals  have  formed  island  races. 
The  land  birds  present  perhaps  the  most  interesting  features  of  the 
whole  strange  fauna.  Besides  two  species  of  owls  and  a  hawk  they 
consist  of  five  passerine  types  and  a  cuckoo,  all  very  close  to  others 
found  on  the  South  American  mainland,  and  a  group  of  fourteen 
species  of  finches,  placed  in  a  distinct  subfamily,  Geospizinae.  These 
finches  are  related  to  the  family  Fringillidae,  which  is  represented  in 
South  America,  but  they  cannot  be  derived  from  any  single  species 
nowr  existing  there.  Like  the  other  animals  in  the  islands  the  birds  tend 
to  become  differentiated  into  distinct  island  races,  but  this  process  has 
gone  to  varying  extents.  The  cuckoo,  warbler,  martin,  and  tyrant 
flycatcher  are  similar  in  all  the  islands  and  it  is  significant  that  they  are 
all  very  close  to  species  occurring  in  South  America.  Presumably  they 
are  recent  arrivals.  The  vermilion  flycatcher,  also  a  South  American 
species,  has  three  island  races.  The  mocking-bird,  Nesomimus,  is 
placed  in  a  genus  distinct  from  that  on  the  mainland  and  has  different 
races  on  each  island,  some  of  them  being  reckoned  as  separate  species. 
The  extreme  of  island  differentiation  is  shown  by  the  finches,  now 


526  EVOLUTION  OF  BIRDS  xvm.9 

reckoned  to  belong  to  fourteen  species,  classed  in  four  genera  (Fig. 
312),  one  of  these  being  found  on  the  distant  Cocos  Island. 

Evidently  these  finches  have  been  in  the  archipelago  for  a  consider- 
able time  and  the  specially  interesting  feature  is  that  not  only  have 
they  formed  races  recognizably  distinct,  but  they  have  radiated  to 
form  a  series  of  birds  that  have  quite  varied  habits,  many  of  them 
very  un-finchlike.  The  main  differences  are  in  the  form  of  the  beak, 
which  varies  greatly  with  the  food  habits  (Fig.  313).  The  central 


C  pan  id  us 


|woodpecker-like| 
C  heliobates 


G  magnirostns 
6  Fortis 


6  scandens 


C.psittacula 
C  pauper 
C.  parvu/us 


Cxrassirostns 


PINAROIOXIAS 
inornata 


FRINGILLiD 
ANCESTOR 


Fig.  312.  Suggested  evolutionary  tree  of  Darwin's  finches.  (From  Lack.) 


species,  which  are  also  the  nearest  to  the  presumed  Fringillid  ancestor, 
are  the  ground-finches,  Geospiza,  of  which  there  are  five  species, 
feeding  mainly  on  seeds.  Two  further  species  of  Geospiza  have  left 
the  ground  and  taken  to  eating  cactus  plants.  The  tree-finches,  placed 
in  a  distinct  genus  Camarhynchns,  include  one  vegetarian  and  five 
mainly  insectivorous  species,  one  of  the  latter,  C.  paiiidus,  having 
acquired  the  habit  of  climbing  up  the  trees  like  a  woodpecker  and 
excavating  insects  with  a  stick  (Fig.  280).  A  third  group  of  this 
remarkable  subfamily  has  acquired  a  convergent  likeness  to  warblers : 
Certhidea  has  a  long  slender  beak  and  eats  small  soft  insects ;  by  many 
it  has  been  regarded  as  distinct  from  the  other  Galapagos  finches,  but 
it  has  now  been  shown  to  resemble  them,  not  only  in  structure  but 
also  in  breeding-habits.  Nevertheless  it  probably  diverged  some  time 
ago  and  is  found  on  all  the  islands.  Presumably  its  success  is  due  to 
the  absence  of  other  warbler-like  birds,  since  the  true  Galapagos 
warbler  is  a  recent  arrival.  The  fourth  genus  of  the  Geospizinae  is 


xviii.  9  DARWIN'S   FINCHES  527 

Pitiaroloxias,  the  Cocos-finch,  found  on  Cocos  Island  600  miles  away, 
and  also  having  warbler-like  characteristics. 

These  birds  provide  a  remarkable  example  of  adaptive  radiation 
'with  seed-eaters,  fruit-eaters,  cactus-feeders,  wood-borers  and  eaters 
of  small  insects.  Some  feed  on  the  ground,  others  in  the  trees — 


(i)  Seeds 


(ii)  Seeds 


(Hi)   Seeds 


(iv)     Leaves 


(vii)  Insects,  buds 


(v)  Seeds,  Cactus  flowers 
&  Fruit 


(vi)  Buds,  Fruit 


( vi/i J  Insects,  buds 


fix)  Insects  in  wood 


fx)   Insects  in  wood  (xi)  Small  so Fc  insects  (xii)  Small  soft  insects 

Fig.  313.  Beaks  of  Darwin's  finches. 

(i)  Geospiza  magnirostris;  (ii)  Geospiza  fortis;  (iii)  Geospiza  fuliginosa;  (iv)  Geospiza  difficilis 

debilirostris;  (v)  Geospiza  scandens;  (vi)  Camarhynchus  crassirostris;  (vii)  Camarhynchus  psit- 

tacula;  (viii)  Camarhynchus  parvulus;  (ix)  Camarhynchus  pallidus;  (x)  Camarhynchus  helio- 

bates;  (xi)  Certhidea  olivacea;  (xii)  Pitiaroloxias  inornata.  (After  Swarth,  from  Lack.) 

originally  finch-like,  they  have  become  like  tits,  like  woodpeckers  and 
like  warblers'  (Lack).  This  is  interesting  enough,  but  more  can  be 
learned  from  this  extraordinary  natural  experiment  than  from  other 
examples  of  adaptive  radiation.  Another  most  striking  feature  is  that 
the  birds  are  very  variable,  and  are  by  no  means  uniformly  distributed 
over  the  islands.  The  outlying  islands  lack  certain  species  and  their 
place  is  then  taken  by  variants  of  others,  with  corresponding  modifica- 
tion of  the  beak.  In  some  such  cases  the  local  subspecies  can  be  clearly 
seen  to  have  an  adaptive  significance,  but  this  is  by  no  means  always 
so.  Some  races  found  on  one  or  more  islands  differ  in  minor  features 


5z8  EVOLUTION  OF  BIRDS  xvm.  9 

of  colour  or  size.  It  remains  to  be  shown  whether  these  are  themselves 
significant  or  connected  with  other  significant  factors. 

The  striking  feature  is  that  so  many  distinct  races  should  appear, 
even  in  birds,  which  could  easily  cross  the  distances,  mostly  less  than 


o 

Culpepper 

Wenman° 


75% 


Cocos 


O  100A 


m 


(J3  Abingdon 
Blnd/oeC^J, 


Tower 


207, 


Narborough 
A  Ibemarle 


10    20     30    40     50 

»  I  ' L I 

Scale  in  land   miles 


IndeFatigable 


Chatham 


Charles 


o\ 


Hood  cC5> 


£7% 

U°/o 

Fig.  314.  Percentages  of  endemic  forms  of  Darwin's  finches  on  each  island,  showing 
the  effects  of  isolation.  (From  Lack.) 

50  miles,  between  the  islands.  Evidently  the  birds  tend  to  remain  at 
home,  and  there  is  no  doubt  that  degree  of  geographical  separation  is 
a  main  factor  in  producing  the  races.  Thus  the  central  islands  of  the 
group,  lying  close  together,  have  no  endemic  subspecies,  whereas  the 
forms  in  the  outlying  islands  are  mostly  distinct  (Fig.  314).  It  is 
evident  that  isolation  is  tending  to  break  up  the  population  into  a 
number  of  distinct  units  and  it  is  remarkable  that,  in  spite  of  the  large 
amount  of  variation,  intermediates  are  rare  between  species  and  even 


xvm.  9  ISLAND  BIRDS  529 

between  subspecies.  The  species,  of  course,  do  not  cross  in  nature,  and 

such  as  have  been  tested  in  captivity  mate  only  with  their  own  species. 

It  is  still  not  possible  to  give  an  entirely  clear  idea  of  the  factors 


QiUngdor,     \MBEU 


Scale  in  land  miles 


\                   _          )                      0      10    20    30   40    50 
\      Bind/oeQ      J  ff         ' '       '      '         "* 

\ 
\ 
\ 

\    /    James 

V 
\ 


\PSITTACULA    , 
o^  \(SENS  STRICT) 

\>    \  7  Indefatigable 

DunoanK  5  \ 

^ — ^      Barrinqton 

/  /  / 

1 1        PSITTACULA 
'SrLh*  (SENS-  STRICT) 
(O)       AND 

CHARLES  ^-^      PAUPER     C5 


.pauper 


Caff  in  is 


C.  psittacuia 


C.  habeli 


Fig.   315.   Development  of  distinct  forms   from  a  single  one  in  the   Galapagos 

finch  Camarliynchus.  Charles  Island  has  two  forms  derived  independently  from 

the  central  form  C.  affinis.  (From  Lack,  partly  after  Svvarth.) 


responsible  for  the  development  of  varied  animals,  even  in  this  much 
simplified  case.  There  is  no  clear  line  between  subspecific  differences, 
say  of  the  beak  that  are  not  obviously  adaptive  and  those  with  clearly 
adaptive  character.  Since  favourable  mutations  will  spread  through  a 
population  the  easiest  assumption  is  that  all  these  differences  are  in 
fact  adaptive,  or  linked  with  unseen  adaptive  characters.  The  easiest 
assumption  is  not  necessarily  correct,  but  the  demonstrably  adaptive 


53Q  EVOLUTION  OF  BIRDS  xvm.  9-10 

character  of  many  of  these  differences  certainly  constitutes  a  case  for 
considering  that  the  others  are  also  of  this  nature.  In  very  small 
populations  ( <  1 ,000)  unfavourable  characteristics  may  become  estab- 
lished by  chance  ('genetic  drift',  Wright,  1940),  and  this  factor  may 
be  responsible  for  some  of  the  island  races. 

It  is  especially  interesting  that  in  the  Galapagos  animals  special 
reasons  have  made  it  possible  for  variety  to  arise.  If,  as  seems  likely, 
the  earliest  Geospizas  were  among  the  first  birds  to  arrive  in  the 
archipelago,  they  found  there  neither  competitors  nor  enemies.  Be- 
cause of  the  distance  from  the  mainland  this  condition  has  remained 
with  little  change  ever  since.  Even  today  the  six  passerines  not  be- 
longing to  the  Geospizinae  do  not  provide  serious  rivals,  and  the 
local  owls  and  hawks  are  apparently  not  serious  predators  on  the 
finches. 

The  other  great  factor  that  has  led  to  differentiation  is  the  splitting 
up  of  the  area  into  a  number  of  isolated  units.  This  has  allowed  slightly 
different  races  to  emerge,  and  we  may  suppose  that  if  these  again 
came  into  contact  with  each  other  they  would  find  slightly  different 
optimal  conditions,  and  therefore,  with  partial  or  complete  inter- 
sterility,  would  continue  as  distinct  species.  This  has  almost  certainly 
happened  with  the  Canary  chaffinch  (p.  523),  and  in  Galapagos  there 
is  a  similar  case  in  that  two  species  of  the  large  insectivorous  tree- 
finch  Camarhynchus  occur  together  on  Charles  Island.  Both  are 
derived  from  a  single  population,  offshoots  from  which  have  inde- 
pendently colonized  the  island  (Fig.  315). 

10.  Birds  on  other  oceanic  islands 

While  the  case  of  Darwin's  finches  is  very  striking  it  is  important  to 
recognize  that  similar  radiation  from  a  few  species  is  not  found  on  all 
oceanic  islands.  For  instance,  there  are  numerous  birds  on  the  Azores 
and  they  differ  little  from  those  of  Europe.  Whereas  migrants  are 
frequent  in  the  Azores  they  are  rare  in  the  Galapagos;  evidently  there 
are  special  factors  producing  the  isolation  of  the  latter. 

A  radiation  similar  to  that  of  the  Galapagos  has,  however,  occurred 
in  Hawaii,  where  there  are  only  five  passerine  forms  and  one  of  these, 
a  finch-like  bird,  the  sicklebill,  has  produced  an  even  greater  variety 
than  Darwin's  finches  (Fig.  316).  Some  of  these  sicklebills  feed  on 
insects,  others  on  nectar,  fruit,  or  seeds,  and  the  beaks  have  developed 
accordingly.  One  species  climbs  like  a  woodpecker,  digs  for  beetles 
with  a  short  lower  mandible,  and  probes  them  out  with  a  long  curved 
upper  one. 


(53i) 


s«*«.  WU£«^_ 


EiU 


0  I*  2". 

Fig.  316.  Adaptive  radiation  of  sicklebills  in  Hawaii.  (From  Lack,  after  Keulemanns.) 


532  EVOLUTION  OF  BIRDS  xvm.  n 

1 1 .  The  development  of  variety  of  bird  life 

This  and  similar  evidence  from  the  study  of  the  relatively  recent 
evolution  of  birds  might  be  summarized  by  saying  that  the  production 
of  variety  of  animal  types  is  largely  due  to  the  interplay  of  biotic 
factors.  The  particular  characteristics  that  each  population  acquires 
depend  partly  on  physical  and  geographical  conditions,  but  the 
stimulus  to  change,  or  the  check  on  change,  comes  from  the  inter- 
action of  the  animals  and  plants  with  each  other. 

It  has  already  been  suggested  that  the  tendencies  to  increase  and  to 
vary  are  important  among  these  factors  influencing  animal  evolution 
and  there  is  evidence  that  both  have  been  at  work  in  the  development 
of  the  population  of  Galapagos  finches  and  other  animals.  It  is  safe  to 
say  that  there  are  more  and  varied  finches,  tortoises,  iguanas,  and 
mocking-birds  than  there  were  when  each  arrived.  The  other  factors 
that  we  are  now  able  to  isolate,  by  their  absence  in  this  case,  are  the 
competitors  and  the  predators.  In  more  fully  developed  continental 
populations  these  probably  tend  to  limit  the  development  of  variety, 
allowing  only  those  individuals  of  a  population  showing  the  mean  or 
'normal'  structure  and  behaviour  to  survive.  Extreme  variants  that 
venture  to  brave  the  enemies  and  seek  new  habitats  are  eliminated. 
Variation  will  arise  when  these  checks  are  weak.  In  a  crowded  habitat 
this  may  occur  as  a  result  of  some  peculiar  swing  of  the  elaborately 
balanced  interacting  system  of  biotic  factors,  or  by  some  external 
physical  change.  We  still  do  not  know  which  of  these  is  the  more 
important  in  producing  the  changes  of  these  complicated  mainland 
populations,  but  the  evolutionary  laboratories  provided  by  the  vol- 
canoes of  the  Galapagos  and  other  islands  suggest  that  evolutionary 
change  does  not  follow  only  on  climatic  or  other  physical  changes. 
A  single  population  will  become  divided  into  several  distinct  ones 
by  its  own  tendencies  to  growth  and  variation,  given  absence  of 
competitors  and  predators  and  some  means  of  isolating  the  animals 
in  different  parts  of  the  range. 


XIX 

THE  ORIGIN  OF  MAMMALS 

1 .  Classification 

Class  Reptilia 
Subclass  *Synapsida 
Order   i.   *Pelycosauria  (=  Theromorpha).   Carboniferous-Per- 
mian. 
*  Varanosaurus ;  *Edaphosaurus ;  *Dimetrodon 
Order  2.  *Therapsida.  Permian-Jurassic 
Suborder  i.  *Dicynodontia 

*Gakpus;  *Moschops;  *Dicynodon;  *Kannemeyeria 
Suborder  2.  *Theriodontia 

*Cy?iog?iathus;  *  Scymnognathns  ;  *Bauria;  *Dromatherium; 
*Tritylodon;  *Oligokyphus 

Class  Mammalia 
Subclass  1.  Eotheria 
#Order  Docodonta.  Trias-Jurassic 

*Morganucodon,  Trias,  Europe;  *Docodon,  Jurassic,  N.  America 
and  Europe 
Order  inc.  sed.  *Diarthrognathus 

Subclass  2.  Prototheria 
Order  Monotremata.  Pleistocene-Recent.  Australasia 

Tachyglossus  ( =  Echidna),  spiny  anteater,  Australia;  Zaglossus 
(=  Proechidna),  New  Guinea;  Ornithorhytichus,  platypus, 
Australia 

^Subclass  3.  Allotheria 
*Order    Multituberculata.     Jurassic-Eocene.     Europe    and    N. 
America 
*Plagiaulax,    Jurassic,    Europe;    *Ptilodus,    Palaeocene,    N. 
America 

Subclass  4.  Theria 

*Infraclass  1.  Pantotheria 

*Order  1.    Eupantotheria.  Jurassic.  Europe  and  N.  America 

*A  mphitherium 
*Order  2.  Symmetrodonta.  Jurassic.  Europe  and  N.  America 
* Spalacotherium 


534  ORIGIN   OF   MAMMALS  xix.  i- 

1.  Classification  (cont.) 

Infraclass  2.  Metatheria 

Order  Marsupialia 
Infraclass  3.  Eutheria  (=  Placentalia) 

#Order  inc.  sed.  Triconodonta.  Jurassic.  Europe  and  N.  America 
*Amphilestes;  *Triconodon 

2.  The  characteristics  of  mammals 

The  idea  that  the  mammals  include  the  highest  of  animals  can 
easily  be  ridiculed  as  a  product  of  human  vanity;  we  shall  find,  how- 
ever, that  in  many  aspects  of  their  structure  and  activities  they  do 
indeed  stand  apart  as  animals  that  are  'higher'  than  others,  in  the 
sense  in  which  we  have  used  the  word  throughout  this  study.  The 
mammals  and  the  birds  are  the  vertebrates  that  have  become  most 
fully  suited  for  life  on  land;  among  them  are  many  species  in  which 
the  processes  of  life  are  carried  on  under  conditions  far  remote  from 
those  in  which  life  first  arose.  The  mammalian  organization  includes 
a  great  number  of  special  features  that  together  enable  life  to  be 
supported  under  conditions  that  seem  to  be  extravagantly  improb- 
able or  'difficult'.  For  example,  the  surface  of  the  body  is  waterproofed, 
and  elaborate  devices  for  obtaining  water  are  developed.  A  camel  and 
the  man  he  is  carrying  through  the  desert  may  perhaps  contain  more 
water  than  is  to  be  found  in  the  air  and  sandy  wastes  for  miles  around. 
This  is  only  an  extreme  example  of  the  'improbability'  of  mammalian 
life,  which  is  one  of  its  most  characteristic  features. 

The  faculty  of  maintaining  a  high  and  constant  temperature  has 
opened  to  the  birds  and  mammals  many  habitats  that  were  closed  to 
the  reptiles.  Besides  making  life  possible  under  extremely  cold  con- 
ditions, such  as  those  of  the  polar  regions,  the  warm  blood  vastly 
extends  the  opportunities  for  life  in  more  temperate  climates.  Mam- 
malian races,  which  can  feed  all  through  the  winter,  can  of  course 
expand  more  rapidly  than  their  reptilian  cousins,  which  must  hiber- 
nate for  much  of  the  year,  during  which  period  they  consume  rather 
than  produce  living  matter. 

The  success  of  the  mammals  in  maintaining  life  in  strange  environ- 
ments is  largely  due  to  the  remarkable  powers  they  possess  of  keep- 
ing their  own  composition  constant.  All  living  things  tend  to  do 
this,  but  it  seems  probable  that  the  mammals  maintain  a  greater 
constancy  than  any  other  animals,  except  perhaps  the  birds.  Claude 
Bernard's  famous  dictum  'La  fixite  du  milieu  interieur  c'est  la  con- 
dition de  la  vie  libre'  may  be  doubtful  of  vertebrates  in  general,  but  it 


xix.  2  ADJUSTMENT   TO    ENVIRONMENT  535 

can  certainly  be  applied  to  mammals.  They  have  a  life  that  is  more 
free  than  that  of  other  groups,  in  the  sense  that  they  can  exist  and 
grow  in  circumstances  that  other  forms  of  life  would  not  tolerate, 
and  they  can  do  this  because  of  the  elaborate  mechanism  by  which 
their  composition  is  kept  constant.  Besides  the  regulation  of  tempera- 
ture there  is  also  a  regulation  of  nearly  all  the  components  of  the 
blood,  which  are  kept  constant  within  narrow  limits.  Barcroft  has 
pointed  out  that  the  achievement  of  this  constancy  has  enabled  the 
mammals  to  develop  some  parts  of  their  organization  in  ways  not 
possible  in  lower  forms.  For  instance,  an  elaborate  pattern  of  cerebral 
activities  requires  that  there  shall  be  no  disturbances  by  sudden 
fluctuations  in  the  blood. 

We  shall  expect  to  find  in  the  mammals,  therefore,  even  more 
devices  for  correcting  the  possible  effects  of  external  change  than  are 
found  in  other  groups.  Besides  means  for  regulating  such  features  as 
those  mentioned  above  we  shall  find  that  the  receptors  are  especially 
sensitive  and  the  motor  mechanisms  able  to  produce  remarkable 
adjustments  of  the  environment  to  suit  the  organism,  culminating  in 
man  with  his  astonishing  perception  of  the  'World'  around  him  and 
his  powers  of  altering  the  whole  fabric  of  the  surface  of  large  parts  of 
the  earth  to  suit  his  needs. 

Such  devices  for  maintaining  stability  often  take  peculiar  and 
specialized  forms  in  particular  cases.  The  activity  and  'enterprise'  of 
mammals  has  led  many  of  them  to  make  use  of  particular  structures 
and  tendencies  in  order  to  develop  very  odd  specializations,  which  en- 
able them  to  occupy  peculiar  niches.  What  could  be  more  bizarre 
than  the  development  of  the  muscles  of  the  nose  until  a  huge  mobile 
trunk  appears,  so  that  the  heaviest  of  four-footed  beasts,  while  using 
its  legs  for  support,  can  also  handle  objects  more  delicately  than  almost 
any  other  animal  ? 

The  mammals  have  developed  along  many  special  lines  and  many 
of  these  have  already  become  extinct;  others,  especially  among  rodents 
and  primates,  remain  among  the  dominant  land-animals  today. 
Warmth,  enterprise,  ingenuity,  and  care  of  the  young  have  been  the 
basis  of  mammalian  success  throughout  their  history.  The  most 
characteristic  features  of  the  modern  mammals  are  thus  seen  to  be 
largely  in  their  behaviour  and  soft  structures.  Mammalian  life  is  above 
all  else  active  and  exploratory.  Mammals  might  well  be  defined  as 
highly  percipient  and  mobile  animals,  with  large  brains,  warm  blood, 
and  a  waterproofed,  usually  hairy  skin,  whose  young  are  born  alive. 
Since  it  is  difficult  to  recognize  such  characters  as  these  in  fossils  we 


536  ORIGIN    OF    MAMMALS  xix.  2- 

cannot  say  exactly  when  they  arose,  and  our  technical  definition  of  a 
mammal  must  be  made  on  the  basis  of  hard  parts. 

The  whole  series  of  mammal-like  forms  from  Carboniferous  anap- 
sids  onwards  forms  a  natural  unit,  and  it  is  only  by  an  arbitrary 
convention  that  we  separate  the  reptilian  subclass  Synapsida  from 
the  class  Mammalia.  The  present-day  mammals  form  a  distinct  group 
of  animals,  which  we  identify  superficially  by  their  possession  of  hair. 
For  instance,  the  duck-billed  platypus  is  immediately  referred  because 
of  its  hair  to  the  mammalia,  and  we  class  it  apart  from  reptiles  or 
birds,  even  though  its  internal  organization  and  the  fact  that  it  lays 
eggs  show  it  to  have  many  similarities  with  reptiles,  and  its  bill  is  like 
that  of  a  duck.  The  technical  characteristic  of  the  class  Mammalia  is 
conventionally  given  by  the  presence  of  a  single  dentary  bone  in  the 
lower  jaw,  the  articular  and  other  bones  forming,  with  the  quadrate, 
part  of  the  mechanism  of  the  middle  ear.  However,  fossils  showing 
intermediate  conditions  are  now  known  from  the  upper  Trias,  say  180 
million  years  ago,  and  all  stages  can  thus  be  traced  in  the  jaws.  The  full 
mammal-like  condition  was  established  by  the  middle  Jurassic  period, 
about  150  million  years  ago.  The  reduction  of  the  jaw  bones  may  per- 
haps have  been  associated  with  the  habit  of  chewing  the  food,  in  order 
to  obtain  the  large  amounts  necessary  to  maintain  a  high  temperature. 

It  would  not  be  very  rash  to  suggest  that  by  Jurassic  times  the 
synapsids  had  developed  the  other  mammalian  characters,  such  as 
active  habits,  large  brain,  warm  blood,  hair,  and  perhaps  also  a 
diaphragm,  four-chambered  heart,  and  single  left  aortic  arch.  They 
may  even  have  been  viviparous,  for  the  surviving  monotremes,  which 
lay  eggs,  probably  diverged  at  a  still  earlier  period,  perhaps  in  the 
Trias  (p.  556). 

3.  Mammals  of  the  Mesozoic 

In  spite  of  all  the  uncertainties  of  the  fossil  record  it  is  now  possible 
to  follow  the  history  of  the  Mammalia  back  to  their  origin  from  coty- 
losaurian  reptiles  of  the  Permian,  more  than  225  million  years  ago. 
Sufficient  information  is  available  for  us  to  be  quite  sure  that  some 
population  of  early  anapsid  reptiles,  such  as  * Seymouria  of  the  Car- 
boniferous and  Permian  times,  besides  giving  rise  to  all  the  modern 
reptiles,  to  the  dinosaurs,  and  to  the  birds,  also  produced  the  mam- 
mals. The  evidence  for  this  connexion  rests  on  a  most  interesting 
series  of  fossils,  together  with  some  'living  fossils'  such  as  the  mono- 
tremes of  Australia.  The  fossil  history  is  not  at  all  times  equally  clear. 
The  mammalian  stock  first  became  distinct  in  late  Carboniferous 


xix.  3  ANCESTRY    OF    MAMMALS  537 

times,  as  a  special  type  of  cotylosaurian  reptile,  with  a  tympanum 
placed  behind  the  jaw  and  later  a  lateral  temporal  aperture.  This  stock 
quickly  became  very  abundant  and  successful  as  the  theromorphs 
and  therapsids  of  Permian  and  Triassic  times,  but  then  nearly  died 
out  in  the  Jurassic,  during  which  period  we  know  of  the  mammals 
only  from  fragmentary  remains  of  a  few  small  animals.  Then,  in  the 
Cretaceous,  some  of  these  small  forms  became  more  numerous  and 
from  them  arose,  before  the  Eocene,  a  variety  of  different  types  of 
mammal,  from  which  the  histories  of  the  modern  orders  can  be  fol- 
lowed in  some  detail. 

We  have,  therefore,  abundant  evidence  of  the  earliest  stages  of 
mammalian  evolution,  say,  20  million  years,  from  fossils  in  the  Per- 
mian Red  Beds  of  Texas.  For  the  next  following  40  million  years  or 
so  we  have  also  a  rich  material,  from  the  Upper  Permian  and  Triassic 
Karroo  beds  of  South  Africa.  In  these  early  times  the  mammal  line 
was  a  flourishing  one,  more  so  indeed  than  the  diapsids  or  any  other 
of  the  descendants  of  the  cotylosaurs.  The  animals  were  mostly 
carnivorous,  though  there  were  also  herbivorous  types.  Many  of  these 
early  mammal-like  forms  became  quite  large  and  numerous,  in  fact 
this  stock  dominated  the  land  scene  in  the  Permian.  In  the  later  Trias, 
however,  if  our  fossil  evidence  is  a  safe  guide,  their  numbers  became 
reduced,  perhaps  the  carnivorous  dinosaurs  took  their  place.  How- 
ever, already  at  this  time  many  of  the  essential  features  of  mammalian 
organization  had  been  developed,  so  far  as  these  can  be  judged  from 
the  bones.  Possibly  the  soft  parts  of  these  Permian  forms  were  also 
mammal-like,  the  animals  may  have  been  active  and  'intelligent',  have 
possessed  hair  and  warm  blood.  However,  their  brains  were  small  and 
reptilian  in  structure. 

Throughout  the  succeeding  100  million  years  of  Jurassic  and  Creta- 
ceous times  our  knowledge  of  the  mammalian  stock  is  dim.  Mammals 
of  a  somewhat  rodent-like  type,  the  multituberculates,  became  quite 
numerous  and  produced  some  large  forms,  but  then  became  extinct 
in  the  Eocene.  Unless  we  have  been  singularly  unlucky  in  the  pre- 
servation of  mammalian  remains,  no  other  mammal-like  animals 
larger  than  a  polecat  existed  throughout  this  long  period.  Since  we 
possess  detailed  information,  based  on  numerous  fossils,  about  scores 
of  large  and  small  diapsid  reptilian  types,  it  can  hardly  be  only  an 
accident  that  mammal-like  fossils  are  so  rare. 

We  must  conclude  that  the  mammalian  organization,  after  an  initial 
success  in  the  Permian  and  Triassic,  was  almost  supplanted  in  the 
Jurassic  and  Cretaceous  by  the  various  diapsid  creatures.  However, 


538  ORIGIN    OF    MAMMALS  xix.  3- 

a  few  very  rare  fossils,  mostly  lower  jaw  bones,  give  us  some  idea  of 
the  nature  of  the  animals  that  carried  our  type  of  organization  through 
the  Jurassic  period.  Then  from  the  top  of  the  Cretaceous,  about  70 
million  years  ago,  come  the  first  fossil  remains  of  mammals  similar  to 
those  alive  today;  rare,  insectivorous  creatures,  not  widely  different 
from  modern  hedgehogs.  This  was  the  time  of  the  beginning  of  an 
astonishing  revolution,  which  completely  altered  the  life  on  the  face 
of  the  earth.  The  descendants  of  these  shrew-like  animals  multiplied 
exceedingly  in  the  new  conditions,  and  by  the  earliest  Palaeocene 
times,  70  million  years  ago,  they  had  produced  recognizable  ancestors 
of  most  of  the  modern  orders  of  mammals. 

Our  knowledge  about  this  revolution  is  still  very  dim.  Some  people 
claim  that  it  accompanied  one  of  the  major  geological  crises,  a 
period  in  which  the  surface  of  much  of  the  earth  became  unstable, 
there  were  great  volcanic  outflows  and  the  building  of  vast  mountain 
chains.  It  is  possible  that  such  upheavals  led  to  the  disappearance  of 
the  swampy  conditions,  which  had  been  so  suitable  for  large  reptiles, 
and  to  the  appearance  of  dry  uplands  on  which  the  mammals  and  birds 
flourished,  especially  where  the  climate  was  cold.  We  must  be  careful 
here,  however,  not  to  argue  in  a  circle.  Our  evidence  about  the  climate 
is  derived  from  the  changes  in  the  populations,  as  revealed  by  the 
fossils.  Study  of  the  plant  remains,  however,  confirms  the  supposition 
that  conditions  became  drier  during  this  time. 

Our  knowledge  of  the  origins  of  mammals  derived  from  fossils  is 
supplemented  by  certain  surviving  mammals,  whose  structure  shows 
them  to  have  diverged  rather  early  from  the  main  stock,  especially  the 
monotremes  (duck-billed  platypus  and  Echidna)  and  the  marsupials 
(kangaroos,  opossums,  &c).  Unfortunately  it  is  still  not  clear  exactly 
how  these  survivors  are  related  to  the  main  stocks  as  revealed  by  the 
fossils.  The  monotremes  are  unknown  except  as  Pleistocene  fossils; 
tantalizingly  enough  we  know  only  little  about  the  affinities  of  this 
ancient  group.  The  characteristics  of  their  bony  skeleton  show  that 
they  must  have  diverged  from  other  mammals  well  back  in  Mesozoic 
times.  For  instance,  the  pelvic  and  pectoral  girdles  are  very  'reptilian' 
in  structure.  It  is  therefore  not  wild  speculation  to  use  the  characters 
of  the  soft  parts  of  monotremes  to  deduce  those  of  the  mammalian 
stock  in  late  Triassic  or  early  Jurassic  times,  say,  180  million  years 
ago.  The  marsupials  appear  as  fossils  in  the  late  Cretaceous.  Some  of 
the  earliest  forms  are  very  like  modern  opossums,  and  we  may  con- 
clude that  the  condition  of  modern  marsupials  throws  some  light  on 
the  probable  condition  of  the  soft  parts  of  mammals  70  or  80  million 


xix.  4  SYNAPSIDS  539 

years  ago.  However,  it  has  been  realized  in  recent  years  that  many 
features  in  marsupial  organization  are  special  developments,  not 
'primitive'  characteristics  carried  over  from  the  ancestral  condition. 

The  piecing  together  of  all  this  evidence  to  give  a  reliable  picture 
of  the  history  of  mammals  is  a  valuable  exercise  in  zoological  and 
geological  method,  as  well  as  a  means  of  becoming  familiar  with  a 
fascinating  story.  We  may  now  return  to  the  Carboniferous  times  to 
examine  the  evidence  more  in  detail  (see  Fig.  221). 

4.  Mammal-like  reptiles,  Synapsida 

All  our  evidence  about  the  origin  of  mammals  must  of  course  be 
based  upon  the  study  of  hard  parts,  which  can  become  fossilized,  and 
in  particular  on  the  skull.  The  characteristic  feature  of  the  skull  in  the 
populations  that  led  to  the  mammals  is  the  development  of  a  hole  in 
the  roof,  low  down  on  the  side  of  the  temporal  region,  the  lower 
temporal  fossa  (Fig.  223).  This  hole  was  at  first  bounded  above  by  the 
post-orbital  and  squamosal  bones,  below  by  the  jugal  and  squamosal. 
It  was  at  one  time  supposed  that  this  single  fossa  was  formed  by  union 
of  the  two  present  in  diapsid  reptiles,  and  thus  the  whole  group 
acquired  the  inappropriate  name  Synapsida.  Animals  having  this 
characteristic  appear  in  the  rocks  at  the  same  time  as  the  cotylosaurs, 
with  no  hole  in  the  skull  roof  (Anapsida),  from  which  they  were  pre- 
sumably derived.  We  have  only  fragmentary  knowledge  of  anapsids 
from  the  Carboniferous ;  most  of  our  information  comes  from  lower 
Permian  forms,  such  as  * Seymouria ;  yet  there  are  quite  well-preserved 
synapsids  of  Upper  Carboniferous  date.  Therefore  we  have  no  com- 
plete series  of  successive  types  to  show  how  the  earliest  mammal-like 
types  arose;  nevertheless  we  can  see  something  of  the  probable  stages 
of  this  progress  within  the  Permian  Anapsida.  One  of  the  charac- 
teristics of  the  skull  of  * Seymouria  was  the  presence  of  an  'otic  notch', 
in  which  lay  the  tympanic  membrane,  at  the  back  of  the  skull  (Fig. 
220).  In  *Captorhinus  and  similar  anapsid  fossils  from  the  Lower 
Permian  this  notch  has  disappeared  (Fig.  222).  The  tympanum 
apparently  lay  behind  the  quadrate,  leaving  the  whole  side  of  the  skull 
as  a  rigid  support  for  the  jaw.  A  long  series  of  subsequent  evolutionary 
changes  led  to  one  of  the  most  characteristic  features  of  the  skeleton 
of  mammals,  namely,  the  conversion  of  the  hinder  jaw  bones  (quad- 
rate and  articular)  into  ossicles  for  the  transmission  of  vibrations  to  the 
ear  (p.  550). 

*Captorhinus  and  its  allies  were  two  or  more  feet  in  length  and 
showed  some  development  of  the  limbs  towards  the  mammalian 


54Q  ORIGIN    OF   MAMMALS  xix.  4- 

condition,  in  that  the  bones  were  moderately  elongated  and  slender 
and  the  limbs  perhaps  tended  to  be  held  vertically  under  the  body. 
However,  there  was  no  great  development  of  a  backwardly  directed 
elbow  and  forward  knee.  The  teeth  were  considerably  specialized, 
possibly  for  eating  molluscs,  and  there  were  several  rows  of  crushing 
teeth  on  the  edge  of  the  jaw,  and  long  overhanging  ones  in  the 
premaxillae. 

5.  Order  *Pelycosauria  (=  Theromorpha) 

The  synapsid  line  began  when  an  early  offshoot  from  some  such 
anapsid  as  *Captorhinus  developed  a  temporal  fossa.  This  must  have 


Dimebrodon  Varanosaurus 

Fig.  317.  Skulls  of  two  early  synapsids.  (After  Romer,   Vertebrate  Paleontology, 
University  of  Chicago  Press,  and  Abel.) 

occurred  in  the  middle  of  the  Carboniferous,  nearly  300  million  years 
ago,  producing  in  the  later  part  of  that  period,  and  in  various  Pennsyl- 
vanian  and  Lower  Permian  strata,  especially  in  North  America,  these 
earliest  synapsid  populations,  classified  together  as  pelycosaurs  or 
Theromorpha.  *Varanosaurus  (Fig.  317),  from  the  Texas  Red  Beds, 
is  a  typical  example,  a  carnivore,  about  3  ft  long,  showing  a  lizard-like 
appearance  little  different  from  that  of  anapsids  or  primitive  diapsids. 
Intercentra  were  found  all  along  the  vertebral  column,  as  in  anapsids, 
and  there  were  abdominal  ribs.  The  teeth  showed  the  beginnings 
of  the  mammalian  differentiation  in  that  one  or  more  near  the  front 
of  the  series  were  elongated  as  'canines'.  The  skull  of  pelycosaurs  also 
showed  tendencies  in  the  mammalian  direction  in  having  a  long 
anterior  region  and  a  relatively  high  posterior  part,  giving  a  large 
brain-case  and  deep  jaw. 

Other  pelycosaurs  developed  long  neural  spines,  in  more  than  one 
line,  *Edaphosaurus  and  its  allies  being  herbivores,  some  of  them  as 
much  as  12  ft  long,  whereas  *Dimetrodon  (Fig.  317)  was  a  carnivore. 
The  spines  presumably  supported  a  web,  perhaps  used  in  temperature 
regulation.  These  animals  were  important  in  the  late  Carboniferous 
and  early  Permian  fauna,  preying  on  the  other  early  reptiles  and  on 


xix.  6  THERAPSIDS  541 

rhachitomous  amphibia.  They  did  not  survive  long,  however,  being 
apparently  replaced  by  their  descendants.  From  some  form  similar 
to  *Dimetrodon  arose  a  whole  series  of  lines  classed  together  as  Therap- 
sida  and  leading  on  to  the  mammals. 

6.  Order  *Therapsida 

In  these  animals  there  was  never  any  trace  of  the  bipedalism  that 
developed  in  the  Archosauria;  the  fore-limbs  were  always  at  least  as 
long  as  the  hind,  and  tended  to  be  turned  under  the  body  and  to  carry 
it  off  the  ground.  The  skull  became  deeper  and  its  brain-case  enlarged ; 
a  bony  secondary  palate  developed  from  flanges  of  the  premaxillae, 
maxillae,  palatines,  and  pterygoids.  The  teeth  became  differentiated 
for  various  functions  and  the  bones  of  the  lower  jaw,  except  the 
dentarv,  were  gradually  reduced. 

These  features  seem  to  have  developed  in  several  different  lines 
descended  from  pelycosaur  ancestors;  the  sorting  out  of  the  various 
genealogies  is  not  yet  complete.  It  is  therefore  still  difficult  to  decide 
for  certain  the  interesting  question  whether  parallel  evolution  occurred, 
and  especially  whether  similar  mammalian  features  appeared  inde- 
pendently in  animals  of  different  habits.  The  fossils  are  nearly  all 
found  in  South  Africa  and  have  been  studied  in  great  detail  by  R. 
Broom. 

Much  of  the  surface  of  the  southern  part  of  Africa  is  covered  by 
rocks  known  as  the  Karroo  system.  These  consist  partly  of  shales  and 
mud-stones  formed  by  the  matter  brought  down  by  a  large  Mesozoic 
river,  and  the  remainder  are  sandstones  composed  of  blown  sand. 
Both  sorts  of  rock  were  particularly  favourable  for  the  preservation 
of  the  remains  of  terrestrial  animals.  Unfortunately  the  absence  of 
marine  fossils  makes  it  difficult  to  give  dates  for  these  rocks.  Altogether 
the  "strata  present  a  thickness  of  some  15,000  ft,  laid  down  over  a 
period  corresponding  probably  to  that  from  the  Middle  Permian  to 
the  Upper  Trias  in  Europe,  that  is  to  say,  from  250  to  180  million 
years  ago. 

The  therapsids  fall  into  two  groups,  the  mainly  herbivorous  di- 
cynodonts  and  the  carnivorous  theriodonts,  probably  preying  upon 
the  former.  *Gafepus  (Fig.  318)  perhaps  shows  a  stage  of  evolution  of 
dicynodonts  from  pelycosaurs.  The  temporal  opening  was  small,  the 
teeth  all  alike  and  the  bones  at  the  hind  end  of  the  jaw  large.  The 
early  dicynodonts  include  the  herbivorous  'dinocephalia',  such  as 
*Moschops,  which  retained  many  primitive  features,  but  the  legs  were 
turned  under  the  body  and  the  phalanges  became  reduced  to  the 


542  ORIGIN    OF    MAMMALS  xix.  6 

mammalian  formula  of  2.3.3.3.3.  The  roof  of  the  head  was  expanded 
into  a  large  dome,  giving  the  name  to  the  group.  The  later  dicynodonts 
were  a  still  more  specialized  and  successful  offshoot,  the  first  of  the 
many  great  tetrapod  herbivores.  They  became  the  commonest  of  all 
reptiles  in  the  later  Permian.  They  were  large  creatures  (*Kanne- 
meyeria  and  *Dicynodon,  Fig.  318),  some  probably  living  in  marshes. 
The  margins  of  the  jaws  were  covered  with  a  horny  beak  and  the 
teeth  reduced  to  a  single  pair  of  upper  'canine'  tusks. 

The  most  interesting  of  the  therapsid  reptiles  are,  however,  those 
placed  in  the  suborder  #Theriodontia,  which,  by  the  early  Trias,  had 
produced  a  very  mammal-like  type  of  organization,  apparently  in 
several  independent  lines.  The  temporal  opening  became  progres- 
sively wider,  presumably  for  the  accommodation  of  larger  jaw  muscles, 
so  that  the  parietal  bone  entered  into  the  margin  of  the  fossa  and  post- 
orbital  and  squamosal  bones  no  longer  met  above  it.  Eventually  the 
post-orbital  bar  itself  became  incomplete,  leading  to  the  typical  mam- 
malian condition,  with  the  orbit  and  temporal  fossa  confluent.  There 
was  a  large  columella,  articulating  broadly  with  the  quadrate  and 
perhaps  serving  to  brace  the  latter  as  well  as  to  transmit  vibrations 
to  the  inner  ear.  A  bone  of  this  size  could  act  as  an  efficient  vibrator 
(Hotton,  1959).  The  brain-case  was  high  and  large  and  the  cerebellum 
better  developed  than  in  modern  reptiles.  The  cerebral  hemispheres, 
however,  though  large,  probably  remained  mainly  olfactory  structures, 
as  indeed  they  were  in  many  Eocene  mammals  and  are  in  some  that 
survive  today. 

The  ribs  were  well  developed  and  seem  to  have  formed  a  cage, 
which  may  have  been  used,  with  a  diaphragm,  for  respiration.  The 
limbs  came  to  support  the  body  off  the  ground,  and  the  dorsal  parts 
of  the  girdles  were  developed  accordingly,  the  scapula  becoming  large 
and  bearing  an  acromial  spine  for  muscle  attachments,  the  coracoids 
being  reduced.  The  anterior  portion  of  the  ilium  became  large  and 
a  hole  appeared  between  the  pubis  and  ischium.  The  head  of  the 
femur  lay  at  the  side,  and  a  special  knob,  the  great  trochanter,  ap- 
peared on  it  for  the  attachment  of  muscles  running  from  the  front 
part  of  the  ilium.  In  the  hands  and  feet  the  toes  show  a  reduction  of 
the  formula  to  2.3.3.3.3.  The  teeth  became  differentiated  into  incisors, 
canines,  and  cheek  teeth,  the  latter  having  several  cusps  in  place  of  the 
cone  of  a  typical  reptile  tooth.  In  most  forms  the  tooth  replacement 
was  as  in  reptiles  but  in  some  it  was  more  limited. 

These  features  were  little  developed  in  the  earliest  theriodonts, 
such  as  *Scy?nnognathus  and  other  Permian  forms  (Fig.  318).  The 


(543) 


a'.  sa.    an.  ^sp. 

Galepus 
Pp.  f-   prF., 

■L  n.         sqy 
-sm. 
■pm. 


po.      L      prf. 


nnx. 


am  sa.  ft     \L 

D'icynodon 


arT     J     d. 
Scumnognathus 


Bauria 


An  kbidosaurian 


Kannemeyeria. 

Fig.  318.  Skull  and  skeleton  of  various  synapsid  reptiles,  abbreviations  as  Fig.  214, 

p.  377.  (After  Romer,  Vertebrate  Paleontology,  University  of  Chicago  Press,  from 

Broom,  Watson,  Gregory,  &  Pearson.) 


544 


ORIGIN    OF    MAMMALS 


xix.  6- 


temporal  fossa  still  resembled  that  of  pelycosaurs,  there  was  a  single 
condyle,  no  secondary  palate,  and  a  phalangeal  formula  of  2.3.4.5.3. 
*Cynognathus  and  other  Triassic  forms  were  typical  theriodonts, 
showing  the  above  'mammalian'  features.  They  were  carnivores,  of 
distinctly  dog-like  appearance,  although  they  still  retained  many  signs 
of  a  heavy  reptilian  build.  *Bauria  was  of  another  type,  still  more 
advanced  than  *Cynognathus  in  that  the  orbit  and  temporal  fossa  were 


Symphysis 


Outer  Aspect 


Articular"* 
Angular  Angular' 

Cynognabhus 


Inner  Aspect        Symphysis 


Fig.  319.  Reduction  of  the  articular  and  other  bones  and  increase  in  the  dentary  in 

therapsid  reptiles.   (From  Neal  and  Rand,   Comparative  Anatomy,  The   Blakiston 

Company,  after  Watson.) 


confluent  (Fig.  318).  The  foramina  of  the  maxilla  of  some  of  these 
animals  suggest  the  passage  of  nerves  and  blood-vessels  for  a  facial 
musculature,  which  is  characteristic  of  mammals  but  absent  in  other 
vertebrates.  Other  types  of  theriodont  were  more  specialized,  with 
rodent-like  features  (*Tritylodon,  *Oligokyphus). 

These  #Theriodontia  were  the  dominant  carnivores  of  the  early 
Trias,  but  by  the  end  of  that  period  they  had  almost  disappeared. 
The  latest  synapsids  include  in  some  classifications  the  *Ictidosauria, 
such  as  *Diarthrognathus  of  the  Upper  Trias.  They  are  rare  fossils, 
showing  almost  completely  mammal-like  structure.  There  was 
no  post-orbital  bar  and  no  prefrontal,  post-frontal,  or  post-orbital 
bones.  A  well-developed  secondary  palate  was  present.  The  bones 
at  the  hind  end  of  the  lower  jaw  had  become  very  small  (Fig.  319).  In 
at  least  one  form  the  dentary  articulates  with  the  squamosal,  though 


xix.  7  MESOZOIC    MAMMALS  545 

there  was  also  a  quadrate-articular  joint.  This  fossil  has  been  appro- 
priately named  *Diarthrognathus.  It  shows  that  it  is  not  possible  to 
find  an  absolutely  rigid  definition  of  a  'mammal',  even  by  means  of 
the  condition  of  the  jaw.  We  shall  classify  this  fossil  as  a  mammal. 

Study  of  the  synapsids,  mainly  from  the  Karroo  system,  shows  us, 
therefore,  a  series  of  types,  of  which  the  earliest  were  very  like  the 
first  reptiles  and  the  latest  very  like  true  mammals.  There  can  be  no 
doubt  of  the  general  tendency,  but  the  series  is  not  complete  enough 
to  enable  us  to  follow  the  details  of  the  evolution  of  the  populations. 
These  fossils  are  revealed  by  denudation  and  can  be  given  only 
approximate  dates.  It  is  certain  that  some  of  the  mammal-like  features 
appeared  independently  in  lines  whose  evolution  proceeded  separately 
from  a  common  ancestor.  Thus  the  dicynodonts  and  later  theriodonts 
all  had  the  mammalian  phalangeal  numbers,  but  each  of  these  lines 
has  certainly  evolved  independently  from  pelycosaur-like  ancestors 
having  a  greater  number  of  phalanges. 

The  influences  that  produced  the  evolution  of  these  populations 
must  have  been  quite  complex,  since  they  did  not  affect  all  parts  of  the 
body  at  once.  For  instance,  some  early  therapsids,  in  spite  of  their 
mammalian  phalangeal  formula,  still  showed  pelycosaur  features  in 
the  absence  of  a  secondary  palate,  and  presence  of  a  single  occipital 
condyle  and  small  dentary.  If  the  presence  of  a  squamo-dentary 
articulation  is  taken  as  the  criterion  of  'a  mammal'  this  condition  was 
almost  certainly  reached  independently  by  several  different  lines  (see 
Simpson,  1959).  We  still  know  too  little  to  be  able  to  specify  clearly 
the  conditions  controlling  such  evolutionary  changes,  but  it  seems 
possible  that  the  gradual  appearance  of  terrestrial  life  and  of  large 
herbivores  led  various  animals  of  a  suitable  structure  and  disposition 
to  a  carnivorous  life.  For  this  purpose  certain  changes  of  the  ancestral 
structure  would  be  suitable,  leading  to  parallel  evolution  in  related 
stocks.  However,  at  present  we  can  hardly  do  more  than  pose  questions 
about  such  matters  and  resolve  to  be  rigorous  in  interpretation  of  the 
available  evidence. 

7.  Mammals  from  the  Trias  to  the  Cretaceous 

The  types  classified  as  synapsid  reptiles,  which  we  have  been  con- 
sidering, are  not  found  later  than  the  early  Jurassic,  170  million  years 
ago ;  mammals  of  approximately  the  modern  type  appear  in  the  late 
Cretaceous.  For  the  enormous  time  of  more  than  90  million  years 
between  these  dates  the  mammalian  organization  maintained  itself 
in  the  form  mostly  of  small  insectivorous  animals,  perhaps  arboreal 


546  ORIGIN    OF    MAMMALS  xix.  7 

and  nocturnal;  few  remains  of  these  are  found  as  fossils,  but  dis- 
coveries now  made  have  helped  to  bridge  the  gap  (Kermack  and  Mus- 
sett,  1958).  No  doubt  many  types  existed  of  which  we  have  no  fossil 
remains,  but  the  Mesozoic  mammals  that  we  know  can  be  divided 
into  five  orders,  *Docodonta,  *Multituberculata,  *Triconodonta, 
#Symmetrodonta,  and  *Eupantotheria  (=  *Trituberculata).  The  last  of 
these  may  perhaps  be  directly  related  to  the  animals  that  gave  rise  to 
the  modern  mammals,  the  other  four  lines  are  specialized  offshoots. 
All  of  them  were  true  mammals  in  that  the  articulation  of  the  lower 
jaw  was  between  dentary  and  squamosal,  though  there  is  evidence  that 
the  articular  and  other  bones  remained  relatively  large  in  the  doco- 
donts.  The  brain-case  (where  known)  was  high  and  the  temporal 
fossa  joined  with  the  orbit.  The  post-cranial  skeleton  is  little  known 
and  indeed  many  forms  are  known  only  from  lower  jaws.  However, 
the  pectoral  girdle  of  docodonts  includes  the  same  bones  as  that  of 
monotremes  in  an  even  more  reptilian  form.  This  and  other  features 
suggest  that  the  monotremes  have  evolved  from  animals  like  the 
*Docodonta  and  that  they  have  preserved  to  the  present  day  many 
features  that  characterized  the  mammalian  stock  during  the  Mesozoic 
period.  Some  of  the  'Mesozoic  mammals',  however,  had  advanced 
beyond  the  stage  of  the  monotremes,  for  instance  the  limb  girdles  of 
multituberculates  resemble  those  of  modern  mammals  rather  than 
reptiles. 

For  purposes  of  classification  we  can  most  conveniently  divide  the 
class  Mammalia  into  four  subclasses,  the  Eotheria  for  the  docodonts, 
Prototheria  for  the  monotremes,  Allotheria  for  the  multituberculates, 
and  the  Theria  for  the  modern  mammalian  line.  This  latter  subclass 
can  then  be  subdivided  into  three  infraclasses,  Pantotheria  for  those 
'Mesozoic  mammals'  that  probably  led  to  the  rest,  Metatheria  for  the 
marsupials,  and  Eutheria  for  the  placentals.  The  triconodonts  must 
be  left  as  of  uncertain  affinities.  This  classification  is  based  upon  that 
provided  by  G.  G.  Simpson  of  the  American  Museum  of  Natural 
History,  who  has  not  only  greatly  increased  our  knowledge  of  many 
orders  of  mammals  but  also  provided  a  complete  systematic  review  of 
the  group. 

The  *Docodonta  are  known  from  isolated  teeth  and  jaws  in  North 
America  and  more  abundant  remains  from  the  latest  Triassic  of  South 
Wales,  which  include  parts  of  the  skull  and  shoulder  girdle.  The  molar 
teeth  carry  three  cusps  in  a  row,  a  condition  known  as  'triconodont'. 
There  is  a  well-marked  condyle  on  the  dentary  and  on  the  lower  margin 
of  the  jaw  a  process  (the  'angle').  Above  this  is  a  conspicuous  trough, 


MESOZOIC    MAMMALS 


xix.  7  ivi£,t>uz,ui^    iMAiviiviAJua  547 

quite  unlike  anything  found  on  the  dentary  of  therian  mammals.  This 
is  presumed  to  have  contained  the  articular  and  perhaps  other  bones, 
fragments  of  which  can  be  seen  (Fig.  320).  A  similar  groove  appears 
on  the  jaws  of  later  theriodonts.  Jaws  carrying  triconodont  teeth  but 


Fig.  320.  A,  triconodont  (Priacodon)  from  the  Jurassic;  B,  lingual  view  of  lower  jaw 
of  a  docodont;  C,  multituberculate  {Ptilodus)  from  the  Palaeocene.  c.a.  canine  alveo- 
lus; gr.  groove;  m.  molars;  m.j.  mandibular  foramen;  p.m.  premolar;  ri.  ridge;  tr. 
trough.  (A  and  C  after  Lull,  Organic  Evolution,  copyright  191 7,  1929  by  The 
Macmillan  Company  and  used  with  their  permission.  B  after  Kermack  and  Mussett.) 

without  the  groove  have  long  been  known  from  the  Jurassic  (*Amphi- 
lestes).  They  may  represent  an  offshoot  from  a  stock  like  the  doco- 
donts. 

The  multituberculata  were  the  most  numerous  and  long-lasting 
Mesozoic  mammals,  surviving  from  the  early  Jurassic  period  to  the 
lower  Eocene.  They  were  herbivorous  and  sometimes  of  large  size 
(Fig.  320).  Between  the  incisors  and  the  molariform  teeth  there  was 
a  gap  (diastema),  as  in  other  mammals  that  chew  large  amounts  of 


548  ORIGIN    OF    MAMMALS  xix.  7- 

vegetable  matter.  The  cheek  teeth  carried  longitudinally  arranged 
rows  of  cusps,  presumably  used  for  grinding  the  food.  The  arrange- 
ment of  the  muscles  can  be  deduced  from  the  jaws.  The  temporal 
muscle  was  small  and  there  was  a  small  coronoid  process  on  the  man- 
dible for  its  attachment.  There  was  therefore  no  wide  sweeping  up  and 
down  movement  of  the  jaw  as  in  carnivores.  On  the  other  hand,  there 
was  a  large  masseter,  pulling  anteriorly,  and  pterygoid  transversely 
and  a  shallow  glenoid  fossa.  All  these  features  will  be  found  again  in 
placental  herbivores.  The  relationship  of  these  animals  to  earlier  and 
later  types  is  quite  uncertain.  It  has  been  suggested  that  the  multi- 
tuberculates  gave  rise  to  the  monotremes  or  marsupials,  but  the 
features  they  have  in  common  with  these  are  mostly  those  of  all 
primitive  mammals. 

The  symmetrodonts  and  eupantotheres  are  imperfectly  known  but 
probably  included  various  carnivorous  and  omnivorous  types,  not 
unlike  modern  opossums  and  some  insectivores.  The  lower  jaw 
was  formed  of  a  single  dentary  bone,  the  hinder  jaw  bones  having 
presumably  already  formed  ear  ossicles.  In  * Amphitherium  there  were 
4  pairs  of  incisors  on  each  side  of  the  lower  jaw,  one  canine  and  11 
cheek  teeth,  4  of  these  being  preceded  by  milk  teeth  and  hence  classed 
as  premolars.  Several  different  sorts  of  eupantotherian  are  known  from 
the  Jurassic  and  could  have  given  rise  to  the  earliest  placental  insec- 
tivores, which  appear  in  the  late  Cretaceous  (p.  583).  The  reason  for 
believing  in  this  relationship  is  the  cusp-pattern  of  the  teeth. 

8.  Original  cusp-pattern  of  teeth  of  mammals 

In  the  symmetrodonts  and  pantotheres  the  teeth  were  so  arranged 
as  to  bite  against  each  other.  The  lower  cusps  formed  a  triangle,  with 
a  surface  behind,  the  talonid  or  heel,  with  which  the  main  cusp  of  the 
upper  molar  made  contact  (Fig.  321).  The  upper  cusps  also  formed 
approximately  a  triangle  and  this  'tribosphenic'  condition  of  the 
molars  is  believed  to  have  been  the  plan  from  which  the  modern 
mammalian  condition  is  derived.  The  apical  cusp,  which  lies  on  the 
inner  side  of  the  upper  molars  and  the  outer  side  of  the  lower  molars, 
was  at  one  time  believed  to  represent  the  original  reptilian  cone  and 
was  therefore  called  the  protocone  in  the  upper  and  protoconid  in  the 
lower  molars.  The  other  two  cusps  are  called  the  paracone  (paraconid) 
in  front  and  metacone  (metaconid)  behind  (Fig.  321).  The  separation 
between  these  latter  cones  is  not  sharp  in  the  pantotheres,  especially 
in  the  upper  jaw,  and  we  shall  find  this  condition  again  in  the  earliest 
placental  mammals. 


xix.  9 


CUSPS    OF   TEETH 


549 


There  have  been  various  theories  about  how  the  triangular  plan  was 
reached.  The  original  tritubercular  theory  supposed  that  there  was 
a  'rotation'  into  a  triangular  position  from  the  three  cusps  in  line  of  a 
triconodont.  Even  if  this  could  be 
shown  to  have  happened  in  a  series  of 
fossil  teeth,  we  should  still  require  a 
knowledge  of  the  change  of  morpho- 
genetic  process  by  which  the  'rota- 
tion' was  produced.  There  have  also 
been  attempts  to  explain  the  many- 
cusped  mammalian  tooth  as  due  to 
the  'fusion'  of  a  number  of  reptilian 
tooth  germs,  either  those  making  one 
series  on  the  gum  or  the  teeth  of 
successive  series.  It  is  plausible  that 
changes  in  relative  time  and/or  place 
of  tooth  development  could  occur  in 
this  way,  leading  to  a  partial  'fusion' 
and  the  production  of  many-cusped 
structures.   At  present   there   is  too 

little  information  to  decide  how  the  reptilian  became  changed  into 
the  mammalian  tooth,  but  there  can  be  little  doubt  that  the  tritu- 
bercular theory  shows  us  approximately  the  nature  of  the  earliest 
mammalian  cusp  patterns.  Indeed  it  was  originally  put  forward 
because  nearly  all  the  Eocene  representatives  of  the  various  mamma- 
lian orders  showed  signs  of  a  triangular  cusp  pattern. 


pad.  met  d. 

•^ LinguaL 

anterior 

Fig.  321.  Arrangement  of  occlusion 

of  cusps  of  tritubercular  teeth.  Upper 

molars     continuous     outline,     lower 

dotted. 

met.  metacone ;  metd.  metaconid ;  pa.  para- 
cone;    pad.    paraconid;    pr.    protocone; 
prd.  protoconid;  t.  talonid  (heel).  (After 
Osborn.) 


Fig.  322.  Duck-billed  platypus 
(Ornithorhynchus).  (From  photographs.) 


Fig.  323.  Five-toed  echidna 
(Tachyglossus).  (From  photographs.) 


9.  Egg-laying  mammals.  Subclass  Prototheria  (Monotremata) 

The  duck-billed  platypus  (Ornithorhynchus)  and  spiny  ant-eater, 
usually  called  Echidna  but  strictly  Tachyglossus  (Figs.  322  and  323),  are 
Australasian  mammals,  basically  similar  to  each  other,  but  so  different 


550  ORIGIN    OF    MAMMALS  xix.  9 

from  other  mammals  that  it  is  certain  that  they  left  the  main  stock 
far  back  in  the  Mesozoic.  Their  organization  possibly  shows  us  many 
of  the  characteristics  of  mammalian  populations  at  that  time. 

Since  we  are  comparing  the  platypus  and  echidna  chiefly  with 
Mesozoic  reptiles  we  shall  deal  first  with  their  hard  parts,  examining 


Fig.  324.  Diagram  of  arrangement  of  jaw  and  auditory  ossicles.  A,  in  a  reptile; 

B,  in  a  mammal. 
ang.  angular;  art.  articular;  cor.  coronoid;  d.  dentary;  ex. col.  extracolumella;  hv.  hyoid; 
inc.   incus   (quadrate);  jon.   gonial;   mall,   malleus   (articular);    Meek.    Meckel's   cartilage; 
pr.fol.  processus  folianus  (goniale);  q.  quadrate;  st.  stapes;  suran.  surangular;  tymp.  tym- 
panic (angular).  (After  Ihle,  from  Gaupp.) 


Fig.  325.  The  temporary  upper  teeth  of  the  duck-billed  platypus. 
(From  British  Museum  Guide.) 

the  living  animals  as  if  they  were  fossils.  The  lower  jaw  consists  of  a 
single  dentary  bone.  The  quadrate,  articular,  and  tympanic  have 
entered  the  ear,  but  the  malleus  is  large,  the  incus  small,  and  the 
stapes  elongated  (Fig.  324).  The  tympanic  bone  forms  a  partial  ring 
around  the  tympanum,  and  the  whole  apparatus  is  not  enclosed  in  a 
bony  'bulla'  as  it  is  in  modern  mammals.  Neither  animal  possesses 
true  teeth  in  the  adult,  the  platypus  having  a  flattened  bill  covered 
with  soft  skin  and  used  for  'paddling'  for  the  small  aquatic  animals, 
especially  mussels  and  snails,  on  which  it  lives.  Tachyglossus  and  the 
related  New  Guinea  form  Zaglossus  have  long  'beaks'  for  eating 
ants.  However,  in  the  young  platypus  flattened,  ridged  teeth  are 


xix.  9  SKULL   OF    MONOTREMES  551 

present,  unlike  those  of  any  other  mammals  (Fig.  325).  These  true 
teeth  are  replaced  by  horny  structures,  formed  by  an  ingrowth  of 
epidermis  beneath  them  and  apparently  used  for  breaking  the  shells 
of  the  molluscs.  It  is  particularly  unfortunate,  since  most  of  our 
knowledge  of  early  mammalian  affinities  comes  from  their  teeth, 
that  we  can  deduce  so  little  from  those  of  the  monotremes. 


bas.  cpisth. 

Fig.  326.  Skull  of  platypus  seen  from  below. 

dl.  alisphenoid;  has.  basioccipital;  ep.  epipterygoid;  ex.  exoccipital;  glen,  glenoid  facet  of 
squamosal;  jug.  jugal;  max.  maxilla;  opisth.  opisthotic;  pal.  palatine;  pm.  premaxilla; 
pv.  prevomer;  sq.  squamosal;  v.  'vomer'- — basisphenoid.  (From  Ihle,  after  van  Benneden.) 

The  skull  (Fig.  326)  is  specialized  in  both  genera,  particularly  at  the 
front  end,  and  many  of  the  bones  fuse  early.  There  is  a  wide  com- 
munication between  the  orbit  and  temporal  fossa.  There  are  many 
'reptilian'  features;  for  instance,  separate  pterygoid  bones.  The  'dumb- 
bell-shaped bones'  are  perhaps  the  remains  of  the  prevomer  but  may 
be  vestiges  of  the  palatine  processes  of  the  premaxillae.  Small  pre- 
frontal and  postfrontal  bones  are  present.  In  the  temporal  region  there 
is  a  narrow  canal  that  apparently  represents  the  posterior  temporal 
fossa  of  Therapsida.  A  curious  feature  is  that  the  lateral  wall  of  the 
brain-case  is  formed  by  an  anterior  extension  of  the  petrosal  and 
not  by  the  alisphenoid. 


ORIGIN    OF    MAMMALS 


552  UKlLrllN      Ul"      1V1A1V11V1AI^»  XIX.  9 

The  vertebrae  are  very  reptile-like,  especially  the  cervicals,  which 
bear  separate  ribs,  as  in  the  synapsid  reptiles.  There  are  seven  cervical 
vertebrae,  but  in  the  dorsal  region  differentiation  has  proceeded  less 
far  than  in  other  mammals,  there  being  16  ribs  in  the  spiny  ant-eaters 


Fig.  327.  Skull  and  skeleton  of  a  female  platypus. 

at.  atlas;  c.  coracoid;  cl.  clavicle;  ep.  epipubic  bone;  /.  femur;  fib.  fibula; 
h.  humerus;  id.  interclavicle;  is.  ischium;  j.  jugal;  m.  maxilla;  pc.  precora- 
coid;  pm.  premaxilla;  pub.  pubis;  pv.  prevomer;  r.  radius;  sc.  scapula;  st. 
sternum;  sq.  squamosal;  t.  tooth;  ti.  tibia;  u.  ulna.  (Modified  after  Owen.) 

and  17  in  the  platypus,  with  3  or  4  lumbars  in  the  former  and  only  2 
in  the  latter.  The  ribs  articulate  only  with  the  bodies  of  the  vertebrae, 
not  with  the  transverse  processes.  The  tail  is  vestigial  in  Zaglossus, 
but  forms  a  flattened  swimming-organ  in  the  platypus.  The  limbs  and 
their  muscles  and  girdles  are  remarkably  reptilian  (Fig.  327).  They 
tend  to  be  held  laterally  rather  than  beneath  the  body  and  in  general 
the  ventral  parts  are  far  better  developed  than  in  modern  mammals, 
and  this  is  sometimes  spoken  of  as  a  'plate-like'  condition.  In  the 
pectoral  girdle  there  are  separate  clavicles  and  a  median  interclavicle. 
The  coracoid  region  includes  two  quite  large  and  separate  bones,  the 


xix.  9  EGGS    OF    MONOTREMES  553 

coracoid  and  'precoracoid'.  There  is  no  spine  on  the  scapula.  The 
ventral  portion  of  the  pelvic  girdle  is  enlarged  by  the  development  of 
epipubic  bones,  presumably  partly  for  the  support  of  the  marsupial 
pouch.  There  is  a  large  and  broad  humerus  in  both  animals,  held 
horizontally.  In  Omithorhynchus  the  fibula  is  expanded  at  its  upper 
end  like  the  ulna  of  other  mammals,  for  the  attachment  of  the  large 
muscles  that  produce  the  swimming  action. 

The  condition  of  the  skeleton  is  therefore  quite  sufficient  to  establish 
the  early  divergence  of  the  monotremes  from  other  mammals  and  we 
are  justified  when  looking  at  the  soft  parts  in  supposing  that  many  of 
the  characters  were  possessed  by  the  synapsid  reptiles.  However,  it 
must  always  be  borne  in  mind  that  many  of  the  'mammalian'  charac- 
ters could  conceivably  have  been  produced  by  parallel  evolution,  sub- 
sequent to  the  divergence  of  the  two  lines. 

Perhaps  the  outstanding  non-skeletal  feature  is  the  egg-laying 
habit.  The  large  yolky  eggs  have  a  whitish  shell  and  in  the  spiny  ant- 
eater  are  transferred  by  the  mother  to  a  special  marsupial  pouch, 
which  develops  at  the  breeding  season.  The  female  platypus  makes  a 
nest  in  a  burrow  for  her  two  or  three  eggs  and  remains  with  them 
continuously  until  after  hatching.  Monotremes  are  unique  in  possess- 
ing a  caruncle  on  the  head  as  well  as  the  egg-tooth,  suggesting  that 
both  were  present  in  the  ancestor  of  Amniotes  as  means  of  breaking 
out  of  the  shell.  After  incubation  and  hatching  the  young  enter  the 
pouch  and  are  fed  by  milk.  The  post-natal  care  of  the  young  therefore 
developed  before  the  egg-laying  habit  was  lost.  Both  genera  produce 
milk  from  specialized  sweat  glands  on  the  ventral  abdominal  wall  of 
the  female,  but  the  ducts  of  these  are  not  united  to  open  on  nipples. 

The  presence  of  hair  again  gives  us  a  valuable  clue.  Unless  this 
feature  has  been  separately  evolved  on  several  lines  we  may  conclude 
that  the  Mesozoic  mammals  and  perhaps  even  the  synapsids  had  made 
some  progress  in  temperature  regulation.  The  mechanism  is  still 
imperfect  in  monotremes,  whose  temperature  is  lower  and  more 
variable  than  that  of  other  mammals.  The  platypus  has  a  fine  short 
fur  of  dark  brown  colour;  in  the  spiny  ant-eater  the  back  carries  a 
mixture  of  spines  and  hairs,  the  belly  carries  hairs  alone. 

The  rectum  and  urinogenital  system  open  to  a  common  cloaca,  a 
'reptilian'  feature  found  also  in  marsupials  (Fig.  328).  The  testes  are 
undescended.  The  penis  of  the  male  is  a  simple  groove  in  the  cloacal 
floor  and  is  used  only  for  the  passage  of  sperm,  the  urine  entering  the 
cloaca  by  a  special  urinary  canal.  A  curious  feature  found  in  both 
monotremes  but  in  no  other  mammals  is  a  grooved  poison  spine  on 


554  ORIGIN    OF    MAMMALS  xix.  9 

the  tarsus  of  the  male,  served  by  a  gland  in  the  thigh.  It  is  possible 
that  this  is  used  to  immobilize  the  female  during  coition. 

The  brain  is  relatively  large  and  arranged  essentially  on  the  mam- 
malian plan  (Fig.  329).  The  pallial  portion  of  the  cerebral  hemispheres 
is  well  developed,  not  the  striatal  portion  as  in  reptiles,  and  the  surface 
is  actually  convoluted  in  spiny  ant-eaters,  though  smooth  in  the 


J 


fibr 


Fig.  328.  Comparison  of  the  cloaca  and  penis  of  tortoise  (a)  with  monotreme 
(b  and  c).  The  penis  is  shown  erect  in  B,  withdrawn  in  c.  (From  Ihle.) 

bl.  bladder;  cl.  cloaca \fibr.  corpus  fibrosum;  p.s.  preputial  sac;  spong.  corpus  spongiosum; 
sp.d.  sperm  duct;  urogen.  urogenital  canal;  a.c.  urinary  canal;  v.d.  vas  deferens;  w.  ureter. 

platypus.  Perhaps,  therefore,  the  large  brain  and  active,  memorizing 
habits  appeared  early  in  the  Mesozoic,  but  an  interesting  feature  is  that 
there  is  no  corpus  callosum  joining  the  hemispheres. 

The  soft  parts  also  show  mammalian  characteristics.  The  diaphragm 
is  fully  developed  and  the  heart  and  single  left  aortic  arch  resemble 
those  of  other  mammals.  These  animals  have  therefore  advanced  in 
their  circulatory  system  beyond  the  anapsid  condition,  such  as  is 
probably  shown  today  in  Chelonia  (p.  397). 

With  all  their  archaic  features  the  monotremes  also  show  many 
specializations.  The  platypus  is  highly  modified  for  aquatic  life.  Apart 
from  its  bill  there  are  the  webbed  feet,  dorsal  nostrils,  long  palate, 


MONOTREMES 


xix.  9  iviuiNU  i  K£-iviiiS  555 

short  fur,  thick  tail,  and  perhaps  absence  of  external  ears.  The  animals 
burrow  in  the  banks,  making  nests  in  which  the  young  are  reared. 
They  are  not  uncommon  in  the  rivers  of  southern  and  eastern 


Fig.  329.  Brain  of  the  platypus. 

ac.  anterior  commissure;  bo.  olfactory  bulb;  cl.  cerebellum;  fl.  flocculus ;  fM.  foramen  of 
Munro;  hab.  habenula;  he.  hippocampal  commissure;  hip.  hippocampus;  hp.  hypophysis; 
ht.  hypothalamus;  mo.  medulla  oblongata;  ol.  optic  lobe;  on.  olfactory  nerve;  pal.  pallium; 
pV.  pons  Varolii;  pyr.  pyriform  lobe;  tc.  tuber  cinereum;  th.  thalamus;  to.  tuberculum 
olfactorium;  II— XII.  cranial  nerves.  (From  Kingsley,  Comparative  Anatomy  of  Vertebrates, 
The  Blakiston  Company.  After  Elliot  Smith.) 

Australia  and  Tasmania  and  fortunately  are  difficult  to  catch  and 
therefore  in  no  danger  of  extinction,  though  their  fur  and  flesh  are 
both  useful. 

Several  species  of  spiny  ant-eater  are  known  and  they  occur  in  New 
Guinea  as  well  as  Australia.  They  show  specializations  for  ant-eating 
similar  to  those  of  Myrmecophaga  (p.  397),  namely,  long  snout,  long 
tongue,  and  large  salivary  glands.  The  clawed  feet  are  used  to  make 
burrows  for  the  young,  as  well  as  for  digging  up  the  nests  of  ants.  It  is 


556  ORIGIN    OF   MAMMALS  xix.  9 

perhaps  significant  that  both  of  these  very  early  mammals  burrow  and 
make  nests  to  assist  in  the  protection  of  their  young. 

The  Monotremata  thus  show  a  peculiar  mixture  of  mammalian  and 
reptilian  characteristics.  In  their  brain,  hair,  warm  blood,  heart,  and 
diaphragm  they  are  mammalian,  but  in  skeleton  and  egg-laying  habit 
they  resemble  reptiles.  A  large  part  of  their  interest  is  that  they  sug- 
gest an  intermediate  stage,  in  many  features,  between  the  two  groups. 
Thus  the  pectoral  girdle  appears  to  be  that  of  a  reptile  partly  changed 
to  a  mammal.  There  are  certainly  many  things  to  be  discovered  from 
these  extraordinary  creatures,  which  have  remained  with  little  change 
in  fundamental  organization  for  possibly  nearly  150  million  years. 
The  characters  they  show  literally  provide  us  with  a  view  of  the  past, 
yet  the  facts  that  these  two  alone  have  survived  and  that  they  show 
special  features  of  their  own  remind  us  sharply  that  evolutionary 
change  is  almost  universal :  new  types  replace  the  old  almost  if  not 
quite  completely. 


XX 


ft 


MARSUPIALS 


1.  Marsupial  characteristics 

The  pouched  mammals  are  essentially  very  similar  to  placentals, 
though  they  undoubtedly  diverged  from  some  early  stage  of  the  main 
mammalian  stocks.  They  parallel,  in  the  isolation  of  Australasia,  the 


Fig.  330 


fnc  m*  m 


Fig.  331 

Figs.  330-1.  Skulls  of  thylacine  (330),  and  rat  kangaroo  (Bettongia)  (331). 
(From  Flower  and  Lyddeker,  Mammals,  Living  &  Extinct,  A.  &  C.  Black,  Ltd.) 

adaptive  radiation  accomplished  in  other  parts  of  the  world  by  the 
placentals.  Many  of  their  features  are  specialized,  so  that  they  re- 
present not  a  stage  on  the  way  to  placental  evolution  but  a  specialized 
side  branch.  Today  some  230  species  are  found  in  the  Australasian 
region,  and  there  are  successful  representatives  in  North  and  South 
America.  In  Eocene  times  they  occurred  in  Europe. 

The  skull  shows  many  characters  found  also  in  Insectivora  and 
other  early  mammalian  groups  (Figs.  330-1).  The  brain-case  is  small 


558  MARSUPIALS  xx.  i 

and  the  top  of  the  skull  therefore  rather  flat.  The  orbit  and  temporal 
fossa  remain  fully  confluent  and  there  is  no  post-orbital  bar.  The  bony 
palate  is  incomplete  posteriorly,  there  being  large  holes  in  the  palatine 
portion  of  it.  The  jugal  bone  always  reaches  back  to  the  glenoid 
articulation  of  the  jaw.  The  lower  jaw,  consisting  of  course  of  a  single 
dentary,  has  a  characteristically  inturned  or  'inflected'  inner  'angle'. 
Other  special  features  of  the  skull,  not  usually  found  in  placentals, 
are  that  the  foramen  for  the  optic  nerve  and  that  for  the  eye-muscle 
and  trigeminal  ophthalmic  nerves  are  not  separated  from  each  other 


Fig.  332.  Teeth  of  the  upper  jaw  of  the  opossum  (Didelphys)  showing  the 

last  premolar,  whose  place  is  occupied  in  the  young  by  a  molariform  tooth. 

(From  Flower  and  Lyddeker.) 

and  that  the  lachrymal  bone  extends  outside  the  orbit.  More  interest- 
ing than  these  apparently  trivial  and  unconnected  diagnostic  features 
is  the  fact  that  the  auditory  region  is  not  protected  by  the  formation  of 
a  bulla  of  the  petrous  bone  as  it  is  in  other  mammals;  instead  the 
alisphenoid  bone  sends  a  wing  over  the  middle  ear. 

The  teeth  are  not  easy  to  interpret  (Fig.  332).  The  incisors  are 
more  numerous  than  in  placentals,  as  many  as  5  on  each  side  in  the 
upper  and  3  in  the  lower  jaw.  Of  the  cheek  teeth  only  one,  the  third 
of  the  series,  is  replaced  in  modern  forms,  and  if  this  is  regarded  as 
the  last  premolar  we  have  a  dentition  of  3  premolars  and  4  molars,  as 
against  the  4  and  3  of  a  typical  placental.  However,  fossil  marsupials 
with  three  replacing  teeth  have  been  found  (p.  566)  and  the  signifi- 
cance of  the  peculiar  condition  of  the  modern  forms  remains  obscure; 
it  may  be  connected  with  the  specialization  of  the  mouth  of  the  young 
for  life  in  the  pouch.  The  cusps  of  the  teeth  of  many  marsupials  (e.g. 
opossum)  show  a  close  approach  to  the  presumed  primitive  plan 
(p.  549),  but  in  addition  to  the  main  triangle  other  cusps  are  present, 
especially  on  the  outside.  As  in  placentals  the  herbivorous  types  of 
marsupial  develop  grinding  surfaces  on  the  teeth. 


XX.   I 


MARSUPIAL    SKELETON 


559 


The  general  plan  of  the  muscles  and  backbone  is  essentially  that 
found  in  placentals  and  has  been  greatly  changed  from  the  reptilian 
or  monotreme  condition.  There  are  no  cervical  ribs.  The  thoracic 
region  consists  of  about  13  rib-bearing  vertebrae,  as  in  placentals,  and 
there  are  about  the  usual  7  lumbars.  The  pectoral  girdle  shows  no 
interclavicle,  but  the  clavicle  remains  large.  The  coracoid  is  reduced, 


Fig. 333  Fig.  334  FIG.  335.  pOUch  young  of 

Figs.  333-4  Hind  foot  of  A,  Trichosurus,  Dasyurus  about  10  days  old. 

and  B,  Macropas,  showing  elongation  of  (After  Hill  and  Osman  Hill.) 

the  toes  of  the  latter  and  reduction  of  the 
1st,  2nd,  and  3rd  toes.   (From  Zittel, 
Text-book  of  Palaeontology,  Macmillan, 
after  Dollo.) 

as  in  placentals,  and  the  scapula  enlarged  and  provided  with  a  spine. 
In  fact  all  the  developments  of  the  dorsal  region  of  the  girdle  that  are 
typical  of  the  mammalian  method  of  locomotion  have  taken  place.  In 
the  pelvic  girdle  there  are  epipubic  bones,  reminiscent  of  those  of 
monotremes;  they  take  the  special  stresses  produced  by  the  abdominal 
muscles  and  pouch,  but  are  reduced  in  the  fully  terrestrial  and  quad- 
rupedal Tasmanian  wolf.  The  hands  usually  carry  five  digits,  armed 
with  claws,  but  the  number  of  toes  is  often  reduced  and  they  may 
bear  hoof-like  structures  (Figs.  333—4). 

The  Miillerian  ducts  are  paired  and  differentiated  into  upper 
'uterine'  and  lower  'vaginal'  portions.  In  many  species  the  latter  are 
provided  with  median  diverticula,  the  two  meeting  in  the  mid-line 
as  a  median  vagina  (Fig.  336).  This  ends  blindly  until  the  young  are 
about  to  be  born,  when  an  opening  is  formed  through  the  tissues — the 


560 


MARSUPIALS 


XX.   I 


pseudo-vagina  or  birth  canal.  This  may  then  close  until  the  next 
parturition.  As  in  monotremes  the  rectum  and  urinogenital  sinus  open 
together  at  a  common  cloaca,  though  this  is  not  very  long,  longer  in 
the  female  than  the  male  (Fig.  337).  There  is  a  well-developed  penis, 
often  bifid  at  the  tip,  in  which  case  the  clitoris  is  also  double,  the 


Fig.  336.  Kangaroo,  female  genitalia.  Note  that  the  sinus  vaginalis  opens 
directly  into  the  urogenital  sinus.  Labelling  as  for  Fig.  337.  (After  Brass  and 

Ottow.) 


arrangement  presumably  ensuring  fertilization  of  both  oviducal  tubes. 
The  testes  descend  to  a  scrotum. 

The  reproduction  of  marsupials  shows  a  viviparous  condition  that 
is  not  closely  similar  to  any  found  in  placentals.  The  egg  is  rather 
yolky  and  covered  with  albumen  and  a  membrane;  cleavage  is  very 
unequal.  In  some  forms  (Dasyurus)  there  is  a  contact  of  the  vascular 
wall  of  the  yolk-sac  with  the  somewhat  hypertrophied  uterine  wall 
(omphaloidean  placenta).  Only  in  the  bandicoot,  Perameles,  does 
the  allantois  develop  a  nutritive  function  to  some  extent.  In  most  mar- 
supials no  placental  arrangement  develops  at  all,  instead,  uterine  milk 
may  be  taken  up  by  the  yolk-sac.  The  embryos  are  born  very  young, 
as  little  as  8  days  from  conception  in  the  opossum  (Fig.  335).  They 
crawl  along  a  track  of  saliva  that  is  laid  between  the  cloaca  and  the 


MARSUPIAL  REPRODUCTION 


561 


pouch  by  the  mother  with  her  tongue.  They  become  attached  to  the 
teats  and  remain  for  a  long  time  in  the  pouch. 

This  is  not  by  any  means  a  primitive  plan  of  development,  it 
involves  many  specializations.  To  make  the  journey  to  the  pouch  the 
fore-limbs  and  their  nervous  centres  are  precociously  developed,  being 
fully  functional  at  birth,  when  the  hind-limbs  are  mere  buds.  The 
method  of  suckling  also  involves  special  developments  of  both  mother 


Fig.  337.  Phalanger  sp.  Female  genitalia.  Note  caudal  blind  ending  of  the 

sinus  vaginalis. 

u.h.  uterine  horn;  s.v.  sinus  vaginalis;  v. I.  vagina  lateralis;  ug.s.  urogenital 

sinus.  (After  Brass  and  Ottow.) 

and  foetus,  so  that  milk  is  injected  into  the  latter  without  choking  it. 
The  sides  of  the  lips  grow  together  round  the  teat,  which  is  thrust  far 
back  in  the  pharynx,  the  larynx  extending  forwards  into  the  nasal 
passage.  Milk  is  pressed  out  by  a  special  muscle  (homologue  of  the 
male  cremaster)  attached  to  the  epipubic  bones. 

The  brain  shows  some  reptilian  features.  The  cerebral  hemispheres 
are  small  for  a  mammal,  and  the  olfactory  bulbs  large.  The  hemi- 
spheres are  not  prolonged  backwards  over  the  cerebellum,  which  is 
itself  small  and  simple.  There  are  dorsal  (hippocampal)  and  ventral 
(anterior)  commissures  but  no  corpus  callosum.  The  cochlea  of  the 
ear  is  spirally  coiled. 


562 


MARSUPIALS 


xx.  2- 


2.  Classification  of  marsupials 

Marsupials  are  often  divided  into  two  suborders,  the  more  primitive 
insectivorous  or  carnivorous  polyprotodonts,  found  outside  as  well  as 
within  Australasia,  and  the  diprotodonts,  more  specialized  and  re- 
stricted. The  distinction  is  based  on  the  presence  of  more  than  three 

m 


Fig.  338.  Hind  feet  of  marsupials,  a,  opossum,  with  grasping  hallux,  arboreal; 
B,  kangaroo,  without  hallux,  digits  II  and  III  syndactyl,  cursorial;  c,  tree  kangaroo, 
without  hallux,  arboreal  (secondarily).  (After  Bensley,  from  Lull,  Organic  Evolution, 
copyright  1914,  1929  by  The  Macmillan  Company,  and  used  with  their  permission.) 

pairs  of  incisors  in  each  jaw  in  the  first  group  while  in  the  other  only 
two  remain  in  the  lower  jaw  and  protrude.  A  further  interesting  feature 
is  that  in  most  diprotodonts  the  second  and  third  digits  of  the  hind- 
limb  are  fused  to  make  a  comb  for  cleaning  the  hair  (Fig.  338).  This 
character  is  absent  in  nearly  all  polyprotodonts,  which  are  hence  said 
to  be  didactylous,  and  this  is  no  doubt  the  primitive  condition.  How- 
ever, the  comb-like  condition  (syndactyly)  is  found  not  only  in 
diprotodonts  but  also  in  the  polyprotodont  bandicoots;  conversely 
the  curious  South  American  opossum-rat  (Caetiolestes),  though 
didactylous,  has  diprotodont  teeth. 


xx.  3  CLASSIFICATION  563 

The  fact  is  that  marsupials,  having  radiated  perhaps  over  60  million 
years  ago,  present  us  today  with  a  number  of  distinct  types  of 
organization.  Simpson  groups  them  into  six  superfamilies  and  it  is 
perhaps  better  not  to  attempt  any  higher  grouping  of  these.  The 
absence  of  Australian  Tertiary  deposits  before  the  Pleistocene  in- 
creases the  difficulties  of  study  of  marsupial  phylogenesis. 

Infraclass  2.  Metatheria 
Order  Marsupiala 
Superfamily  1.  Didelphoidea.  Upper  Cretaceous-Recent.  Europe 
and  America 
*Eodelphis.  Upper  Cretaceous,  N.  America;  Didelphis,  opos- 
sum, Pliocene-Recent,  N.  and  S.  America;  Chironectes,  water 
opossum,  Central  and  S.  America 
*Superfamily  2.  Borhyaenoidea.  Palaeocene-Pliocene.  S.  America 

*Thylacosmihis,  Miocene;  *Borhyaena,  Oligocene-Miocene 
Superfamily  3.  Dasyuroidea.  Pleistocene-Recent.  Australasia 
Dasyurus,  native  cat;  Sarcophilus,  Tasmanian  devil;  Thylacinus, 
Tasmanian  wolf;  Myrmecobius,  banded  ant-eater;  Notoryctes, 
marsupial  mole;  Sminthopsis,  pouched  mouse 
Superfamily  4.  Perameloidea.  Pleistocene-Recent.  Australasia 

Perameles,  Bandicoot 
Superfamily  5.  Caenolestoidea.  Eocene-Recent.  S.  America 
*Palaeothentes  (=  *Epanorthiis),   Oligocene-Miocene;   Caeno- 
lestes,  opossum-rat,  Ecuador,  Colombia,  Peru 
Superfamily  6.  Phalangeroidea.  Pliocene-Recent.  Australasia 
Trichosurns,  Australian  opossum;   Petaiirns,   flying  opossum; 
Phascolarctos,   koala   bear;    Vombatus,   wombat;    Macropus, 
kangaroo;  Bettongia,  rat  kangaroo;  *Diprotodon,  Pleistocene; 
*ThyIacoleo,  Pleistocene. 

3.  Opossums 

The  opossums  (Didelphoidea)  were  the  earliest  group  to  appear 
and  the  other  families  have  probably  evolved  from  them,  with  syn- 
dactyly appearing  twice.  They  are  arboreal,  mainly  nocturnal  and 
omnivorous  or  insectivorous  animals,  with  a  prehensile  tail,  occurring 
over  the  southern  United  States  and  Central  and  South  America  (Fig. 
339).  The  pouch  is  generally  absent.  Similar  forms  are  found  back  to 
the  Upper  Cretaceous  (*Eodelphis)  and  the  American  opossums  are 
certainly  the  closest  of  living  marsupials  to  the  ancestors  of  the  group, 


564  MARSUPIALS  xx.  3- 

perhaps  they  are  the  least  modified  of  all  therian  mammals.  Chiro- 
nectes  is  a  related  South  and  Central  American  otter-like  form,  with 
webbed  feet. 


Fig.  339.  American  opossum 
(Didelphis).  (From  photographs.) 


Fig.  341.  Tasmanian  devil  (Sarcophilus). 
(From  photographs.) 


Fig.  342.  Tasmanian  tiger  cat  (Dasyurus). 
(From  photographs.) 


Fig.  340.  Tasmanian  wolf  (Thylacinus).  (From  photographs.) 


The  bandicoots  (Perameles)  of  Australia  and  New  Guinea  are  bur- 
rowing animals,  rather  rabbit-like  but  mainly  insectivorous.  They 
have  a  polyprotodont  dentition,  quadritubercular  grinding  molars, 
syndactyly  of  the  hind  toes,  and  an  allantoic  placenta.  Their  affinities 
are  uncertain. 


xx.  4  (565) 

4.  Carnivorous  marsupials 

The  Dasyuroidea  include  some  nocturnal  carnivorous  polyproto- 
donts  that  show  remarkable  convergence  with  placental  carnivores,  the 
teeth  being  modified  for  cutting  flesh  in  a  way  similar  to  the  carnivore 


Fig.  343.  Eastern  native  cat  (Dasyurus).  (From  photographs.) 


Fig.  344.  Banded  ant-eater  (Myrmecobius). 
(From  photographs.) 


Fig.  345.  Marsupial  mole 

(Notoryctes). 

(From  photographs.) 


Fig.  346.  Pouched  mouse 

(Stninthopsis). 

(From  photographs.) 


Fig.  347.  Kangaroo  (Macropus). 
(From  photographs.) 


carnassial.  Thylacinus  (Fig.  340),  the  Tasmanian  wolf,  is  now  nearly 
or  quite  extinct.  Sarcophilus,  the  Tasmanian  devil  (Fig.  341),  is  rare, 
but  (Dasyurus  (native  cat)  (Figs.  342  and  343)  includes  several  species 
of  cat-like  creatures  common  in  Australia  and  New  Guinea.  Successful 
carnivorous  marsupials  formerly  existed  in  South  America.  They 
may  perhaps  be  related  to  the  Dasyuridae;  *Borhyaena  shows  many 


566  MARSUPIALS  xx.  4- 

similarities  to  Thylacinus.  *Thylacosmilus  was  a  Miocene  sabre-tooth, 
the  size  of  a  panther,  whose  huge  upper  canine  and  other  features  closely 
parallel  the  placental  *Smilodon  (p.  689).  It  is  said  that  in  some  of  these 
borhyaenoids,  two  or  more  milk  teeth  were  replaced ;  if  true  this  sug- 
gests that  the  condition  in  modern  marsupials  is  secondary. 

5.  Marsupial  ant-eaters  and  other  types 

Myrmecobius  is  an  ant-eating  form,  with  elongated  snout  (Fig.  344). 
Notoryctes,  the  marsupial  mole  (Fig.  345),  from  South  Australia,  has 
reduced  eyes,  well-developed  fore-limb,  fused  cervical  vertebrae,  and 
many  features  suiting  it  for  burrowing  and  feeding  upon  ants.  Its 
pouch  opens  backwards.  Sminthopsis,  the  pouched  mice  (Fig.  346), 
are  small  marsupials  occupying  the  niche  taken  in  other  parts  of  the 
world  by  the  shrews. 

Caenolestesy  the  opossum-rat  of  the  forests  of  the  Andes,  is  an 
interesting  shrew-like  creature,  with  the  polyprotodont  number  of 
incisors  but  procumbent  lower  incisors,  resembling  those  of  diproto- 
donts.  There  is  no  syndactyly.  It  is  the  survivor  of  a  group  formerly 
abundant  in  South  America,  some  with  teeth  similar  to  those  of 
multituberculates. 

6.  Phalangers,  wallabies,  and  kangaroos 

The  diprotodont  marsupials  form  a  compact  group  (leaving  out 
Caenolestes)  of  Australian  forms,  here  included  as  the  superfamily 
Phalangeroidea.  Their  fossil  history  is  little  known,  but  they  have 
become  specialized  for  various  modes  of  life,  mainly  as  herbivores,  in 
Australia  and  the  neighbouring  islands.  The  kangaroos  and  wallabies 
(Macropodidae)  (Fig.  347)  have  become  mostly  terrestrial  and 
developed  a  bipedal  method  of  progression,  involving  modification  of 
the  ilia  and  thigh  muscles,  for  whose  attachment  the  tibia  bears  a 
marked  anterior  crest.  The  foot  gains  increased  leverage  by  elongation 
of  the  metatarsal  of  digit  4.  Digits  2  and  3  are  very  small  and  syn- 
dactylous.  There  are  several  modifications  for  a  herbivorous  diet;  the 
single  pair  of  lower  incisors  is  directed  forwards  and  their  sharp  inner 
edges  can  be  moved  in  such  a  way  as  to  cut  grass  like  shears.  This  con- 
dition recalls  that  of  Rodentia  (p.  655)  and,  as  in  that  group,  a  special 
transverse  muscle  is  developed  (m.  orbicularis  oris),  but  in  this  case  it 
is  part  of  the  facial  musculature  and  innervated  from  the  seventh  nerve, 
whereas  the  analogous  muscle  of  the  rodents  is  a  part  of  the  mylohyoid 
and  innervated  from  the  trigeminal.  The  molar  teeth  are  modified 
for  grinding,  by  the  fusion  of  the  cusps  to  make  two  transverse  ridges, 


xx.  6 


PIIALANGERS 


567 


recalling  those  of  ruminants.  The  stomach  has  a  special  sacculated 
non-glandular  chamber,  presumably  allowing  digestion  by  symbionts. 
Bettongia  and  other  'rat  kangaroos'  are  terrestrial  and  bipedal  jumpers, 
and  also  have  a  prehensile  tail  (Fig.  348). 


Fig.  348.  Rat  kangaroo 

(Bettongia). 

(From  photographs.) 


Fig.  349.  Cuscus  (Phalatiger). 
(From  photographs.) 


Fig.  351.  Flying  opossum  (Petaurus). 
(From  photographs.) 


Fig.  350.  Koala  bear  (Phascolarctos). 
(From  photographs.) 


The  Australian  opossums  or  phalangers  are  less  modified  than  the 
kangaroos  and  are  arboreal  animals,  with  a  prehensile  tail  and  various 
special  modifications,  mostly  for  herbivorous  diets ;  Trichosurus  is  the 
common  phalanger,  with  four-cusped  upper  molars.  Phalanger,  the 
cuscus  (Fig.  349),  eats  mainly  leaves.  The  koala  or  native  bear,  Phasco- 
larctos (Fig.  350),  lives  on  the  leaves  of  Eucalyptus;  it  has  cheek- 


S68 


MARSUPIALS 


xx.  6-7 

pouches,  an  enlarged  caecum,  and  a  reduced  tail.  Three  distinct 
genera  of  phalangers  have  developed  extensions  of  the  skin  for  pur- 
poses of  soaring;  Petaurus  (Fig.  351)  is  the  best  known  of  these  flying 
phalangers.  Vombatus,  the  wombat  (Fig.  352),  is  a  large,  burrowing, 
tailless  animal,  with  rodent-like  grinding  teeth;  it  eats  roots.  *Dipro- 
todon  was  a  very  large  marsupial,  of  the  size  and  form  of  a  rhinoceros, 
which  lived  in  Australia  in  the  Pleistocene.  *Thylacoleo  was  a  marsu- 
pial lion  in  which  the  incisors  were  developed  as  fangs. 


Fig.  352.  Wombat  (Vombatus).  (From  photographs.) 

7.  Significance  of  marsupial  isolation 

The  explanation  of  the  curious  distribution  of  the  marsupials 
remains  uncertain.  The  fossil  evidence  suggests  a  palaearctic  distribu- 
tion in  the  Eocene,  followed  by  radiation  in  South  America  and 
Australia  with  later  reduction  in  the  former.  An  antarctic  bridge  has, 
however,  been  postulated  by  some  authors. 

The  opossums  show  that  marsupial  life  can  continue  effectively  in 
competition  with  placentals.  But  it  can  hardly  be  an  accident  that  the 
diversification  of  marsupials  in  Australia  has  been  accomplished  in 
isolation.  It  is  true  that  there  are  108  species  of  placentals  in  Australia, 
as  against  119  marsupials,  but  the  placentals  are  almost  all  bats  (40 
species)  and  murid  rodents.  The  marsupials,  on  the  other  hand,  have 
become  differentiated  into  numerous  types,  arboreal,  fruit-eating, 
grazing,  gnawing,  digging,  burrowing,  ant-eating,  insectivorous  or 
carnivorous,  in  each  case  with  appropriate  structure.  It  will  be  interest- 
ing to  see  how  this  assemblage  stands  up  to  competition  with  placentals 
in  the  future.  Carnivores,  ruminants,  lagomorphs,  rodents,  and  pri- 
mates have  recently  become  firmly  established  in  Australia  and  it  can 
hardly  be  an  accident  that  some  of  the  corresponding  marsupial  types 
are  already  becoming  rare  or  extinct. 


XXI 

EVOLUTION  OF  PLACENTAL  MAMMALS  AND  ITS 

RELATION  TO  THE  CLIMATIC  AND 
GEOGRAPHICAL  HISTORY  OF  THE  CENOZOIC 

1 .  Eutherians  at  the  end  of  the  Mesozoic 

Several  different  lines  of  evidence  converge  to  show  that  all  the 
eutherians  (placentals)  have  been  derived  from  small,  perhaps  noc- 
turnal, insectivorous  or  omnivorous  animals,  living  in  the  Cretaceous 
period  about  ioo  million  years  ago.  Many  features  of  marsupials 
and  placentals  alike  suggest  origin  from  a  small  Cretaceous  shrew-like 
form,  perhaps  itself  descended  from  some  animal  like  the  Jurassic 
pantotheres.  It  is  especially  interesting,  therefore,  that  fossil  evidence 
is  now  available  to  show  that  both  opossums  (p.  563)  and  placental 
insectivores  (p.  583)  existed  in  the  Cretaceous.  We  may  be  reasonably 
sure  that  the  population  from  which  those  groups  were  derived 
resembled  both  of  these  animals,  which  are  indeed  basically  similar. 
At  this  Cretaceous  period  the  arrangements  for  nourishing  the  young 
were  presumably  not  yet  fully  developed  and  in  the  marsupials 
(Metatheria)  they  have  remained  at  a  simple  level,  little  above  ovo- 
viviparity,  though  the  condition  in  Perameles  makes  it  doubtful 
whether  an  allantoic  placenta  has  been  lost  by  the  other  marsupials. 
The  stock  that  was  to  give  rise  to  the  eutherians  was  therefore 
already  differentiated  in  the  Cretaceous;  as  the  revolution  proceeded 
these  animals  began  to  flourish  and  to  develop  into  several  divergent 
populations.  The  only  placental  types  known  to  have  lived  during 
Cretaceous  times  were  insectivores;  yet  by  the  very  beginning  of  the 
Cenozoic  period,  in  the  formations  known  as  the  Palaeocene,  several 
different  types  of  placental  are  found. 

2.  The  end  of  the  Mesozoic 

It  is  not  easy  to  discover  any  close  connexion  between  the  climatic 
changes  and  this  early  flowering  of  the  placentals.  Throughout  the 
period  of  the  Cretaceous  earth  movements  the  land  gradually  became 
higher  and  the  climate  probably  colder,  at  least  in  some  parts  of  the 
world.  Indeed,  this  process  had  been  going  on  intermittently  through- 
out the  Mesozoic.  In  the  Permian  there  was  a  series  of  glaciations  even 


570  PLACENTAL    MAMMALS  xxi.  2- 

more  profound  than  those  of  the  Pleistocene  and  it  has  been  suggested 
that  this  may  have  been  responsible  for  the  production  of  mammal-like 
characteristics  among  the  synapsids  (p.  538).  It  is  tempting  to  make 
similar  suggestions  about  the  development  of  placental  mammals  at 
the  end  of  the  Cretaceous.  The  presence  of  cold  uplands  may  indeed 
have  been  responsible  for  such  success  as  the  multituberculates  and 
other  Mesozoic  mammals  achieved  during  the  Cretaceous.  But  this 
slow  revolution  does  not  explain,  by  itself,  the  success  of  the  placen- 
tal, because  they  only  became  differentiated  into  varied  groups 
towards  the  end  of  the  Cretaceous.  There  is  some  evidence  that  this 
latter  time  was  not  very  cold,  and  it  will  be  remembered  that  some 
dinosaurs  persisted  to  the  very  close  of  the  Mesozoic.  On  the  other 
hand,  pterodactyls  had  died  out  earlier  and  so  had  some  groups  of  the 
dinosaurs. 

Although  there  may  well  have  been  large  climatic  changes  at  the 
end  of  the  Cretaceous  period  it  is  unwise  to  make  simple  statements 
about  their  relation  to  the  evolution  of  the  mammals.  The  whole 
Cretaceous  period  lasted  for  more  than  60  million  years  and  we  can- 
not trace  in  detail  the  numerous  changes  of  climate  that  must  have 
taken  place,  probably  in  different  directions  in  different  parts  of  the 
world.  Even  the  marine  faunas  were  affected;  for  instance,  the  ich- 
thyosaurs  and  plesiosaurs  died  out  before  the  end  of  the  Cretaceous 
and  were  followed  by  the  mosasaurs  (p.  409),  which  had  a  sudden 
period  of  success  lasting  for  some  millions  of  years. 

The  change  of  fauna  at  the  end  of  the  Cretaceous  was  as  remarkable 
for  the  animals  that  appeared  as  for  those  that  were  lost.  The  remain- 
ing dinosaurs  died  out  on  land,  as  did  the  mosasaurs,  and  also  am- 
monites and  belemnites,  in  the  sea.  At  the  same  time  there  appeared 
not  only  numerous  placental  mammals,  but  also  a  great  variety  of  true 
birds,  and  in  the  seas  teleostean  fishes  and  cephalopods  of  modern 
type. 

The  apparent  suddenness  of  the  change  may  be  deceptive.  Our 
knowledge  of  the  conditions  at  the  beginning  of  the  Cenozoic  period 
is  fragmentary.  It  was  a  time  when  the  land  stood  high,  at  least  in  the 
regions  we  know  best.  A  great  part  of  the  continental  shelf  was  above 
water,  and  therefore  producing  few  fossils.  Most  of  our  information 
about  the  fossils  laid  down  at  this  time  comes  not  from  marine  beds, 
but  from  the  Talaeocene'  continental  deposits,  known  chiefly  in 
America.  These  deposits  lie  on  top  of  undoubted  Cretaceous,  dino- 
saur-containing beds,  and  they  contain  a  variety  of  placental  mammals. 
At  the  upper  end  these  Palaeocene  deposits  are  continuous  with  beds 


xxi.  3  DIVISIONS    OF   THE   TERTIARY  571 

that  can  be  correlated  with  the  previously  known  Eocene  marine  beds 
in  other  parts  of  the  world,  at  which  level  there  is  a  still  wider  variety 
of  placentals. 

It  is  clear,  therefore,  that  there  was  a  period  of  time  of  unknown 
duration,  following  the  disappearance  of  the  dinosaurs,  during  which 
the  placentals  were  becoming  differentiated.  The  old  belief  in  the 
sudden  appearance  of  various  types  in  the  Eocene  was,  therefore, 
perhaps  chiefly  an  artefact  of  the  conditions  of  fossilization  at  the 
time. 


3.  Divisions  and  climates  of  the  Tertiary  Period 

The  whole  Tertiary  or  Cenozoic  period  is  now  divided  as  follows: 


Time  from  beginning 

Per  cent 

of  epoch  to  present 

modem 

Epoch 

(millions  of  years) 

species 

Recent     ..... 

100 

Pleistocene  ('most  recent') . 

1 

90 

Pliocene  ('more  recent') 

10 

50 

Miocene  ('less  recent') 

25 

20 

Oligocene  ('few  recent') 

40 

10 

Eocene  ('dawn  recent') 

60 

5 

Palaeocene  ('ancient  recent') 

70 

0 

The  names  were  originally  given  by  Lyell  to  indicate  the  percentages 
of  modern  species  of  shells;  for  curiosity  these  latter  are  given  (ap- 
proximately) in  the  third  column.  During  the  Palaeocene,  Eocene, 
and  Oligocene  the  mountains  raised  during  the  Laramide  revolution 
were  eroded.  The  climate  was  cold  in  the  palaearctic  region  early  in 
the  period,  but  it  later  became  warmer  and  damper  and  there  were 
probably  extensive  forests  during  the  later  Eocene  and  Oligocene. 
Palms  then  grew  over  much  of  Europe  and  there  were  forests  where 
are  now  immense  areas  of  steppe.  The  climate  probably  showed 
marked  seasonal  changes,  at  least  in  many  parts  of  the  world,  and 
deposits  of  the  time  often  show  a  lamination  ('varving')  that  indicates 
an  alternation  of  wet  and  dry  seasons.  During  this  first  part  of  the 
Cenozoic  there  was  some  invasion  of  the  land  by  water,  but  this  was 
on  a  much  smaller  scale  than  during  the  inundations  of  earlier  periods ; 
indeed,  the  main  land-masses  have  remained  approximately  constant 
throughout  the  Tertiary. 

During  the  early  Miocene  there  was  a  time  of  intense  crustal 
disturbance,  the  Cascadian  revolution.  In  this  many  of  the  earth's 
main  mountain  chains,  the  Rockies,  Andes,  Alps,  Himalayas,  as  well 


572  PLACENTAL    MAMMALS  xxi.  3- 

as  humbler  ranges  such  as  the  English  chalkdowns,  were  raised  into 
their  present  form.  This  revolution  marks  the  subdivision  of  the 
Cenozoic  into  two  periods.  After  it  there  was  a  further  denudation 
during  the  Miocene  and  Pliocene,  with  some  renewed  sea  invasion. 
The  uplifting  of  the  land  during  the  Miocene  probably  produced  arid 
conditions  unfavourable  to  the  growth  of  forests,  and  at  this  time  there 
emerged  several  types  of  animal  suitable  for  life  on  open  prairies. 
Conditions  probably  became  gradually  colder  throughout  the  Plio- 
cene, and  the  subsequent  Pleistocene  epoch  was  characterized  by  the 
extensive  glaciations  of  the  'Ice  Ages',  occurring  in  at  least  four  peaks 
of  maximum  cold,  during  each  of  which  the  ice  caps  advanced  over 
large  parts  of  the  continents  (p.  648). 

Study  of  the  history  of  the  Cenozoic  in  the  palaearctic  region  there- 
fore gives  us  some  idea  of  the  climatic  changes  that  have  taken  place, 
and  we  can  try  to  correlate  these  with  the  succession  of  types  of  animal 
life.  On  the  other  hand,  it  is  important  not  to  be  over-impressed  with 
any  simple  account  of  climatic  changes.  The  periods  of  time  involved 
are  enormously  long  and  it  is  unsafe  to  assume  that  conditions 
remained  constant  for  any  length  of  time  that  can  be  easily  imagined, 
or  even  that  conditions  varied  at  a  constant  rate.  For  example,  in 
Yellowstone  Park,  U.S.A.,  there  are  exposures  of  the  remains  of 
Eocene  tree-trunks  and  these  are  arranged  in  layers,  showing  that  at 
least  twenty  forests  grew  up  and  were  covered  by  volcanic  ash  one 
after  the  other.  Each  of  these  eruptions  presumably  produced  a  major 
revolution  for  the  animals  and  plants  in  the  area  concerned;  we  do  not 
know  how  wide  that  area  may  have  been.  Obviously  no  broad 
generalization  about  the  presence  of  'humid  conditions  and  forests' 
throughout  the  Eocene  can  give  us  any  clear  picture  of  the  ecological 
conditions  even  in  one  area.  The  geological  history  shows  us  that 
conditions  were  continually  changing,  though  perhaps  often  at  a  rate 
very  slow  in  comparison  with  the  duration  of  animal  lives.  We  can 
well  imagine  that  these  slow  changes  were  responsible  for  producing 
new  conditions  and  hence  new  types  of  life,  but  the  data  of  the  rocks 
are  too  obscure  to  show  us  the  detailed  circumstances  of  the  emergence 
of  any  particular  type. 

4.  Geographical  regions 

Although  the  main  land-masses  have  varied  little  during  the  Ter- 
tiary period,  there  have  been  considerable  changes  in  the  opportuni- 
ties for  communication  between  them,  both  by  the  making  and  breaking 
of  narrow  land-bridges  and  by  the  development  of  sharp  tempera- 


xxi.  4  GEOGRAPHICAL   REGIONS  573 

ture  gradients  and  desert  areas.  Zoogeographers  divide  the  land  into 
six  regions  (Fig.  353),  Palaearctic  (Central  and  N.  Asia,  Europe), 
Nearctic  (N.  America),  Neotropical  (Central  and  S.  America), 
Ethiopian  (Africa),  Oriental  (S.  Asia  and  E.  Indies),  and  Australasian. 
The  Palaearctic  and  Nearctic  have  similar  climates  and  have  been 


Fig.  353.  Polar  projection,  showing  the  zoogeographical  realms.  (From  Lull, 

Organic  Evolution,  copyright  191 7,  1929  by  The  Macmillan  Company,  and 

used  with  their  permission.) 


connected  several  times  during  the  Tertiary  by  an  Alaska-Siberian 
bridge;  they  are  therefore  often  grouped  together  as  Holarctic.  The 
Ethiopian  region  is  now  separated  from  the  Palaearctic  by  the  sudden 
change  of  temperature  and  desert  conditions  of  North  Africa,  but  in 
earlier  times  the  animals  of  the  two  regions  mixed  freely.  The  same 
is  true  of  the  Palaearctic  and  Oriental  regions.  South  America  was 
connected  with  the  Nearctic  region  in  the  Eocene,  but  the  bridge  was 
then  broken  until  the  Pleistocene;  the  Neotropical  land  faunas  there- 
fore differ  considerably  from  the  others.  Australasia  east  of  Wallace's 
line  has  been  separated  since  the  late  Cretaceous. 

The  land  masses  have  therefore  been  connected,  in  the  main,  in  the 
north  and  separated  in  the  south.  In  other  words,  America,  North 


574  PLACENTAL    MAMMALS  xxi.  4- 

and  South  Africa,  and  the  Oriental  regions  are  capes  projecting  into 
the  sea  from  the  central  Palaearctic  (Eurasian)  land-mass.  There  is 
evidence  that  many  forms  of  animal  life  evolved  in  this  central  area 
and  migrated  away  towards  the  extremities.  Several  of  the  types 
that  evolved  earlier  remain  as  vestiges  at  these  'ends  of  the  world', 
long  after  newer  types  have  replaced  them  nearer  to  the  centre.  The 
lung-fishes  are  a  conspicuous  example  of  this  and  at  another  extreme 
it  is  perhaps  no  accident  that  Australian  Aborigines  and  South  African 
Bushmen  are  among  the  more  primitive  of  men.  This  is  the  most  prob- 
able explanation  of  the  similarity  in  the  fauna  between  these  southern 
continents,  but  many  suggestions  of  Antarctic  land  bridges  and  con- 
tinental drift  have  been  put  forward,  in  particular  one  connecting 
South  Africa  and  South  America  in  the  early  Tertiary.  For  example, 
we  have  to  explain  the  appearance  of  porcupine-like  animals  (p.  660) 
in  Africa  and  South  America  at  the  same  time  (Oligocene). 

5.  The  earliest  eutherians 

Fossil  placentals  found  in  the  Cretaceous  period  have  all  been  in- 
sectivorans  (p.  583).  Those  of  the  Palaeocene  include  also  some  that 
can  be  referred  to  the  primates  and  to  the  carnivora,  but  they  are  very 
unlike  modern  members  of  those  groups  and  could  almost  equally 
well  be  classed  as  Insectivora.  Similarly,  the  ungulates  and  various 
other  types  that  appeared  in  the  Palaeocene  could  have  had  an  in- 
sectivoran  ancestry.  Evidently,  therefore,  during  the  late  Cretaceous 
and  Palaeocene,  the  original  placental  stock  was  branching  out  into 
various  habitats,  and  the  branching  was  rapid.  Simpson's  careful 
classification  recognizes  twenty-six  orders  of  placentals  (p.  577),  and 
nearly  all  of  these  had  become  distinct  by  the  Eocene.  Ten  of  them 
have  since  become  extinct.  Evidently  the  great  period  of  mammalian 
expansion  was  in  the  earlier  part  of  the  Cenozoic  and  the  group  may 
be  considered  to  have  passed  its  peak  for  the  present.  Only  the  bats, 
rodents,  lagomorphs,  and  perhaps  the  primates  and  carnivores  can 
be  considered  really  successful  land  animals  at  the  present  time;  to 
these  we  may  add  the  whales  in  the  sea.  The  Artiodactyla  are  also 
abundant,  but  most  of  the  remaining  placental  orders  are  today 
poorly  represented  in  numbers. 

In  order  to  gain  a  comprehensive  general  understanding  of  the  great 
placental  history  during  its  80  million  or  so  years  duration,  we  will 
first  give  a  technical  definition  of  a  placental,  then  the  characteristics 
of  the  earlier  types,  and  finally  try  to  list  some  of  the  tendencies  to 
change  that  are  widely  found  in  different  groups.  For  simplification 


xxi.  7  DEFINITION    OF   A   EUTHERIAN  575 

we  can  attempt  some  grouping  of  the  great  list  of  orders,  before  deal- 
ing with  them  individually. 

6.  Definition  of  a  eutherian  (placental)  mammal 

The  distinguishing  characteristics  of  placentals  are  often  listed 
somewhat  as  follows :  The  young  are  retained  for  a  considerable  time 
in  the  uterus  and  nourished  by  means  of  an  allantoic  placenta;  there 
is  no  pouch  or  epipubic  bones.  In  the  skull  there  is  usually  a  separate 
optic  foramen,  no  palatal  vacuities,  and  no  in-turned  angle  of  the  jaw. 
The  tympanic  bone  is  either  ring-like  or  forms  a  bulla,  there  is  never 
an  alisphenoid  bulla.  The  brain  has  large  cerebral  hemispheres  con- 
nected by  a  corpus  callosum.  There  is  no  cloaca.  The  dental  formula 

3.1.4.3 
is ,  or  some  number  reduced  from  this. 

3-M-3 

Many  of  these  are  obviously  small  points  of  formal  definition,  arti- 
ficially abstracted  for  the  purpose  of  classification.  They  are  not  really 
satisfactory  as  a  definition  of  the  life  of  a  placental,  such  as  we  may 
hope  to  have  in  a  more  developed  biology.  The  early  population  of 
Cretaceous  insectivores  presumably  possessed  most  of  these  features, 
and  showed  characteristics  that  are  common  to  all  the  earlier  mam- 
mals. Among  these  we  may  list  (1)  small  size;  (2)  short  legs  with  a 
plantigrade  type  of  foot,  having  five  digits;  (3)  the  full  eutherian 

3.1.4.3 

number  of  teeth  ,  the  molariform  teeth  being  based  on  the 

_  3-I-4-3  8 

tuberculo-sectorial  pattern  (p.  549);  (4)  long  face  and  tubular  skull, 
enclosing  a  relatively  small  brain. 

7.  Evolutionary  trends  of  eutherians 

In  the  descendants  of  these  early  mammals  we  can  recognize  changes 
in  each  of  these  four  sets  of  characters ;  changes  occurring,  indepen- 
dently, in  some  members  at  least  of  all  the  later  lines.  (1)  Many  of 
the  mammals  became  larger.  Increase  in  size  seems  to  be  advantageous 
to  many  animal  types  and  may  be  connected  with  the  advantages  of  a 
large  brain  storing  much  information  during  the  life  of  the  animal 
and  so  allowing  slow  reproduction.  It  is  presumably  especially  so  for 
warm-blooded  animals  in  cold  climates,  since  it  reduces  the  relative 
area  of  heat  loss,  though  also  introducing  new  problems  of  obtaining 
adequate  amounts  of  food.  This  may  have  to  be  finely  ground  by  tooth- 
surfaces  whose  increase  with  size  is  less  rapid  than  that  of  the  weight  of 
tissue  they  must  support.  (2)  The  limbs  became  longer  and  specialized 


PLACENTAL    MAMMALS 


576  ^LAL-tlN  1AL     IVJLAiVllVlAl^S  XXI.  J- 

in  various  ways  for  locomotion,  often  by  raising  the  heel  off  the  ground, 
so  that  the  animals  came  to  walk  on  the  digits  instead  of  the  sole  of 
the  foot  (Fig.  354)  and  the  number  of  toes  became  reduced.  (3)  The 
number  of  teeth  became  reduced  and  their  shape  specialized,  often 


Fig.  354  Fig.  355 

Fig.  354.  Postures  of  the  foot  in  mammals.  A,  plantigrade  (bear);  B,  digitigrade  (hyaena); 
C,  unguligrade  (pig).  (From  Lull,  after  Pander  and  D 'Alton.) 

FlG.  355.  Comparison  of  pairs  of  brains  of  archaic  (left)  and  modern  (right)  mammals  of 
similar  size.  Olfactory  lobes  dotted,  cerebral  hemispheres  oblique  lines,  cerebellum  and 
medulla,  dashes.  A,  *Arctocyon  and  Canis;  B,  *P/ienacodus  and  Sus;  C,  *Coryphodon  and 
Rhinoceros;  D,  Uintatherium  and  Hippopotamus.  (After  Osborn,  from  Lull,  Organic 
Evolution,  copyright  1917,  1929  by  The  Macmillan  Co.,  and  used  with  their  permission.) 


by  the  addition  of  cusps  and  their  fusion  to  make  transverse  or  longi- 
tudinal grinding  ridges  in  herbivorous  animals  or  cutting  blades  in 
carnivores.  (4)  The  brain  of  the  earlier  mammals  resembled  that  of 
reptiles  (Fig.  355);  later  forms  showed  increasing  development  of  the 
non-olfactory  part  of  the  cortex,  increase  of  the  frontal  lobes,  and  other 
changes  probably  correlated  with  more  complicated  behaviour  and 
better  memory.  It  has  often  been  supposed  that  the  brain  becomes 
relatively  larger  in  later  forms,  but  Edinger  has  shown  by  study  of 


xxi.  9  CONSERVATIVE    EUTHERIANS  577 

fossil  horse  brains  that  as  the  body  size  increases  the  brain-body 
ratio  decreases. 

8.  Conservative  eutherians 

Much  of  this  change  was  the  result  of  adopting  a  fully  terrestrial 
and  often  herbivorous  mode  of  life,  in  place  of  the  earlier  arboreal  and 
insectivorous  or  carnivorous  one.  Changes  in  these  four  directions 
have  taken  place  in  many  separate  mammalian  lines,  but  the  evidence 
contradicts  the  thesis  that  they  are  the  result  of  some  force  of  ortho- 
genesis, driving  the  animals  infallibly  along.  In  nearly  every  group 
there  are  examples  of  some  animals  that  have  remained  nearly  un- 
changed for  long  periods,  e.g.  opossums  and  shrews  since  the  Creta- 
ceous (80  million  years),  lemurs  and  tarsiers  since  the  Eocene  (50 
million  years),  pigs  and  tapirs  since  the  Oligocene  (35  million  years), 
and  deer  since  the  Miocene  (20  million  years),  to  name  only  a  few. 

It  is  important  to  study  such  animals  in  which  there  has  been  little 
change;  they  form  the  'controls',  and  may  enable  us  to  recognize  the 
factors  inducing  change  when  it  does  occur.  Moreover,  in  many 
further  lines  there  has  been  change  in  some  but  not  all  of  the  above 
directions,  for  instance,  many  of  the  most  successful  mammals  have 
remained  small.  There  may  even  be  changes  in  the  directions  opposite 
to  those  listed,  for  instance,  some  edentates  and  whales  have  more 
than  the  original  number  of  teeth.  Mammals  do  not  commonly  de- 
crease in  size  during  evolution  (but  they  may  do  so),  and  they  prob- 
ably never  reacquire  lost  digits,  though  in  a  few  claws  have  reappeared 
after  they  had  been  lost. 

9.  Divisions  and  classification  of  Eutheria 

Infraclass  3.  Eutheria 
Cohort  1.  Unguiculata 
Order  1.  Insectivora 
Order  2.  Chiroptera 
Order  3.  Dermoptera 
*Order  4.  Taeniodonta 
*Order  5.  Tillodontia 
Order  6.  Edentata 
Order  7.  Pholidota 
Order  8.  Primates 
Cohort  2.  Glires 

Order  1.  Rodentia 
Order  2.  Lagomorpha 


578  PLACENTAL    MAMMALS  xxi.  9 

Classification  (cont.) 

Cohort  3.  Mutica 

Order  Cetacea 
Cohort  4.  Ferungulata 
Superorder  1.  Ferae 

Order  Carnivora 
Superorder  2.  Protungulata 

*Order  1.  Condylarthra 

#Order  2.  Notoungulata 

*  Order  3.  Litopterna 

*Order  4.  Astrapotheria 

Order  5.  Tubulidentata 
Superorder  3.  Paenungulata 

Order  1.  Hyracoidea 

Order  2.  Proboscidea 

#Order  3.  Pantodonta 

#Order  4.  Dinocerata 

*Order  5.  Pyrotheria 

*Order  6.  Embrithopoda 

Order  7.  Sirenia 
Superorder  4.  Mesaxonia 

Order  Perissodactyla 
Superorder  5.  Paraxonia 

Order  Artiodactyla 

For  purposes  of  phylogenetic  study  as  well  as  classificatory  con- 
venience it  is  desirable  to  attempt  to  discover  how  the  original 
eutherian  population  became  divided  at  its  Cretaceous  origin,  and 
whether  there  were  main  trunks  of  the  placental  tree.  By  Eocene 
times  most  of  the  existing  orders  were  already  well  established  (Fig. 
356)  and  it  is  often  stated  that  the  branching  of  the  population  occurred 
relatively  rapidly,  though  it  is  doubtful  if  we  may  use  this  term  for  a 
process  occupying  perhaps  30  million  years  during  the  late  Cretaceous 
and  Palaeocene!  This  early  expansion  into  varied  branches,  occurring 
at  a  time  when  few  fossils  were  being  formed,  makes  it  difficult  to 
discover  the  outlines  of  the  main  divisions.  Nevertheless,  careful 
piecing  together  of  evidence  suggests  grouping  of  the  twenty-six 
eutherian  orders  into  four  main  cohorts,  and  the  division  corresponds 
in  the  main  to  the  classification  originally  proposed  by  Linnaeus  in 
1766  on  a  basis  of  the  foot  structure.  The  Unguiculata  include  orders 
in  which  the  original  characteristics  of  the  mammalian  type  have  been 


.*•' 


es  S3 

E  2 


bo 

c 

1 


580  PLACENTAL    MAMMALS  xxi.  9 

largely  preserved,  the  Insectivora  themselves  and  the  Chiroptera  (bats), 
the  Primates  and  the  Edentata  (sloths,  ant-eaters,  and  armadilloes), 
all  of  which  can  be  easily  and  directly  derived  from  the  insectivores. 
Here  also  probably  belong  the  scaly  ant-eater,  Manis  (Pholidota), 
and  the  extinct  *Taeniodontia  and  *Tillodonta,  which  survived  only 
for  a  short  time  and  of  which  little  is  known  and  they  will  not  be 
mentioned  further.  The  Rodentia  and  the  rabbits  and  hares  (Lago- 
morpha)  are  often  also  considered  to  belong  here,  but  they  appear 
fully  developed  in  the  Eocene  and  must  have  diverged  very  early  and 
are  therefore  placed  alone  in  a  separate  cohort  Glires.  Similarly  the 
whales  (Cetacea)  have  certainly  been  distinct  since  the  Eocene.  Their 
affinities  are  quite  obscure,  and  they  are  classed  as  a  separate  cohort 
named  by  Linnaeus  Mutica  (most  inappropriately  since  they  com- 
municate by  sounds). 

All  the  remaining  mammals  show  signs  of  a  common  origin  and 
Simpson  suggests  grouping  them  together  as  a  cohort  Ferungulata. 
It  has  long  been  realized  that  the  hoofed  animals  include  two  distinct 
types,  those  with  an  uneven  number  of  toes,  Perissodactyla,  and  those 
with  even  toes,  Artiodactyla.  The  former  can  be  derived  from  the 
Palaeocene  and  Eocene  animals  known  as  *Condylarthra.  The  Carni- 
vora  seem  at  first  sight  to  have  no  similarity  to  either  of  the  ungulate 
types,  but  it  has  been  suspected  for  some  time  that  the  ancestral  Carni- 
vora,  the  *Creodonta,  resembled  the  earliest  artiodactyls.  Further  study 
has  shown  that  creodonts  and  condylarths  are  often  so  alike  as  to  be 
hardly  separable  (they  are  also  very  like  Insectivora).  Simpson's  sug- 
gested cohort  Ferungulata  recognizes  the  existence  of  this  common 
creodont-condylarth  stock,  perhaps  in  early  Palaeocene  times.  The 
cohort  may  then  conveniently  be  subdivided  into  five  superorders, 
Ferae  for  the  Carnivora,  Protungulata  (  = 'first  ungulates')  for  the  con- 
dylarths, the  extinct  South  American  ungulates  (*Liptopterna  and 
#Notoungulata),  the  obscure  *Astrapotheria  and  Tubulidentata 
(Orycteropus,  the  Cape  ant-eater).  The  third  superorder  Paenungulata 
(  =  'near  ungulates')  includes  the  elephants  (Proboscidea),  hyraxes 
(Hyracoidea),  and  sea  cows  (Sirenia),  as  well  as  the  extinct  *Panto- 
donta,  #Dinocerata,  #Pyrotheria,  and  *Embrithopoda.  The  fourth 
superorder  Perissodactyla  is  then  made  to  include  only  the  horses, 
tapirs,  and  rhinoceroses;  and  the  fifth  superorder  Artiodactyla  the 
pigs,  camels,  and  ruminants.  This  system  gives  us  a  means  of  group- 
ing that  is  phylogenetically  reasonably  accurate  and  also  conveniently 
close  to  the  usually  accepted  uses  of  familiar  names. 


XXII 

INSECTIVORES,  BATS,  AND  EDENTATES 

1.  Order  1.  Insectivora 

#Suborder  i.  Deltatheridioidea.  Upper  Cretaceous-Eocene.  Asia  and 
N.  America 
*Deltatheridium,  Cretaceous,  Asia 
Suborder  2.  Lipotyphla 
Superfamiiy  1.  Erinaceoidea.  Paleocene-Recent.  Holarctic,  Oriental, 
Africa,  N.  America 
Echinosorex,    moonrat,    Asia;    Erinacens,    hedgehog,   Miocene- 
Recent,  Old  World 
Superfamiiy  2.  Soricoidea.  Paleocene-Recent 

Family  Soricidae.  Oligocene-Recent.  Holarctic,  Africa 

Sorex,  shrew,  Miocene-Recent;  Neomys,  water  shrew,  Eurasia 
Family  Talpidae.  U.  Eocene-Recent.  Holarctic 

Talpa,  mole,  Miocene-Recent;  Myogale,  desman,  water  mole 
Family  Solenodontidae.  Recent.  W.  Indies 

Solenodon,  alamiqui 
Family  Tenrecidae.  Miocene-Recent.  Africa,  Madagascar 
Pota?nogale,  otter  shrew,  W.  Africa;  Tenrec  (=  Centetes),  ten- 
rec,  Madagascar 
Family  Chrysochloridae.  Miocene-Recent.  Africa 
Chrysochloris,  golden  mole,  S.  Africa 
Suborder  3.  Menotyphla 
*Superfamily  1.  Leptictoidea.  Upper  Cretaceous-Oligocene 

*Zalambdalestes,  Cretaceous,  Asia.;*Ictops,  Oligocene,  N.  America 
Superfamiiy  2.  Macroscelidoidea.  Miocene-Recent.  Africa 

Macroscelides,  elephant  shrew 
Superfamiiy  3.  Tupaioidea.  Oligocene-Recent.  Asia 

*AnagaIe,  Oligocene;  Tupaia,  tree  shrew;  Ptilocerais,  pen-tailed 
tree  shrew 

Modern  insectivores  are  mostly  small,  nocturnal  animals,  main- 
taining, possibly  because  of  some  special  habitat,  the  earliest  mam- 
malian features.  They  have  persisted  with  little  change  since  the 
Cretaceous.  Apart  from  the  retention  of  primitive  characters,  they 
have  little  else  in  common.  With  them  have  been  classified  a  number 
of  early,  primitive  eutherians  that  cannot  be  placed  in  any  other  order. 


582  INSECTIVORES  xxn.  1 

The  order  Insectivora  is  thus  a  convenience  rather  than  a  natural 
group. 

The  full  dentition  of  is  usually  preserved,  and  the  cusps  have 

diverged  little  from  the  tritubercular-tuberculo-sectorial  pattern  but 
two  extra  cusps  are  often  added  on  the  outer  side  of  the  tooth  to  make 
a  W  pattern  ('dilambdodont').  The  skull  (Fig.  357)  shows  many 
primitive  features.  The  orbit  is  broadly  continuous  with  the  temporal 
fossa  (except  in  tree  shrews).  There  is  an  incomplete  bony  palate  and 
an  open  tympanic  cavity,  in  which  the  tympanic  bone  (the  old  angular) 

forms  a  partial  ring.  Non-primitive 

____^-r£5^r^;£^  characters  include  the  incomplete 

^^^^^^^^■^^r^^)l       bony  palate  of  the  hedgehog  and 

/_/.      i%t~\j "Jm^  _yfff       the  loss  of  the  zygomatic  arch  in 

ffa^^?^^  tenrec  and  the  shrews.  In  the  post- 

^^^^^^^Ql    ?K^f  cranial   skeleton   there  is  usually 

^^^^^^^^^  found  a  clavicle,  five  digits  with 

claws  in  both  limbs,  and  the  method 

Fig.  357-  Skull  of  hedgehog  (Erinaceus).        Qf    locomotion    IS    plantigrade.     A 

specialization  of  the  Lipotyphla  is 
reduction  or  elimination  of  the  pubic  symphysis.  In  the  soft  parts  the 
primitive  characters  again  predominate.  The  stomach  is  simple.  The 
brain  has  large  olfactory  bulbs  and  small  cerebral  hemispheres,  com- 
posed mainly  of  large  pyriform  lobes  (rhinopallium),  usually  not 
covering  the  corpora  quadrigemina  or  cerebellum,  and  with  little 
convolution.  The  neopallium  and  corpus  callosum  are  small.  Besides 
the  nasal  receptors  insectivores  have  a  sensitive  snout  often  drawn  out 
into  a  short  trunk.  There  are  vibrissae  and  acute  hearing  (especially 
in  moles).  The  eyes  are  large  in  Menotyphla  but  smaller  in  Lipotyphla, 
sometimes  rudimentary  (moles).  In  many  species  the  retina  contains 
only  rods  but  there  are  cones  in  some  species  of  Sorex  and  in  the  tree 
shrews,  Tupaia.  Some  insectivores  retain  the  cloaca.  The  uterus  is 
bicornuate  and  the  testes  are  never  fully  descended  into  a  scrotum.  The 
placenta  is  discoidal  and  haemochorial,  that  is  to  say  of  a  type  not 
obviously  close  to  the  presumed  ancestral  mammalian  condition. 
Numerous  young  are  produced  (up  to  32  in  Tenrec).  Many  insectivores 
hibernate  in  winter  and  are  provided  with  special  reserves  of  fat  for 
this  purpose.  Most  insectivores  are  solitary  but  some  have  social  habits, 
exchanging  auditory  and  olfactory  signals  {Solenodoii).  They  may  make 
simple  nests. 

*Deltatheridinm  is  a  fossil  insectivore  found  in  the  Upper  Cretaceous 


XXII.   I 


INSECTIVORES 


583 


of  Mongolia  and  having  characters  very  close  to  those  of  the  ancestor 
not  only  of  insectivores  but  of  all  placental  mammals.  The  skull  was 
tubular  and  elongated,  but  without  the  special  snout  of  some  modern 
forms.  The  teeth  are  of  special  interest  in  that  in  the  upper  molars  the 
central  cusp  (amphicone)  showed  only  partial  division  into  paracone 
and  metacone.  There  were  large  canines  and  other  features  suggesting 
creodonts. 

Classification  of  the  various  lines  of  insectivores  has  been  difficult, 
as  might  be  expected  in  a  group  containing  surviving  ancient  as  well 


Fig.  358.  Tenrec. 
(From  photographs.) 


Fig.  359.  Solenodon,  alamiqui. 
(After  Cambridge  Natural  History.) 


as  modified  types.  It  is  not  feasible  here  to  discuss  the  possible 
affinities  of  the  various  groups. 

Tenrec  (Fig.  358)  from  Madagascar,  and  Solenodon,  the  alamiqui 
(Fig.  359),  from  the  West  Indies  are  remarkably  similar  animals, 
showing  in  their  dentition,  brain,  and  other  features  characters  more 
primitive  even  than  those  of  other  insectivores.  The  teeth  have  a 
tritubercular  V  pattern,  by  which  they  are  sometimes  distinguished 
as  'zalambdodont'  from  the  remaining  or  'dilambdodont'  insectivores. 
The  resemblance  of  the  alamiqui  and  the  tenrec  has  often  been  cited 
as  evidence  of  a  land  bridge,  but  is  probably  a  result  of  retention  of 
primitive  features.  Potamogale  (the  otter  shrew)  is  a  related  aquatic 
African  form,  feeding  on  fish. 

The  golden  moles  (Chrysochloris)  of  Africa  are  burrowing  animals, 
with  interesting  features  of  similarity  to  the  marsupial  and  true  moles. 
Hedgehogs  (Erinaceiis)  (Fig.  360)  are  mainly  nocturnal  creatures, 
feeding  on  a  mixed  animal  diet  of  insects,  slugs,  small  birds,  and  snakes 
or  even  fruit.  They  have  a  remarkable  immunity  to  snake-bite  and 
indeed  to  bacterial  and  other  toxins.  Related  genera  in  South-east 
Asia,  such  as  Echtnosorex,  are  more  primitive  in  that  the  hairs  of  the 
back  are  normal,  and  not  converted  into  spines  as  in  the  hedgehogs. 
In  the  Oligocene  and  Miocene  of  Europe  both  types  were  equally 
common.  The  shrews  (Soricidae)  are  mouse-like,  insectivorous  and 
omnivorous  animals  of  various  types,  some  terrestrial,  others  aquatic, 


5§4 


INSECTIVORES 


XXII.  i- 


found  throughout  the  world.  The  incisors  are  specialized  as  pincers. 
Sorex  (Fig.  361)  is  a  very  ancient  genus,  found  from  the  Miocene 
onwards  with  little  change.  Moles  (Talpa)  (Fig.  362)  are  related  to 
shrews  and  are  found  throughout  the  Holarctic  region.  They  are  highly 
specialized  for  burrowing,  with  rudimentary  eyes  (sometimes  covered 


f*r- 


Fig.  360.  Erinaceus,  hedgehog. 
(From  photographs.) 


Fig.  361.  Sorex,  common  shrew. 
(From  photographs.) 


Fig.  363.  Tupaia,  tree  shrew. 
(From  photographs.) 


Fig.  362.  Talpa,  common  mole. 


Fig.  364,  Macroscelides,  elephant 
shrew.  (From  a  photograph.) 


with  opaque  skin)  and  no  external  ears,  smooth  fur,  fused  cervical 
vertebrae,  massive  pectoral  girdle,  including  a  procoracoid,  and  broad 
digging  claws  on  the  hands.  They  feed  mainly  on  earthworms. 
Myogale,  the  desman,  of  south  Europe  is  an  aquatic  mole,  with  webbed 
feet. 

Apart  from  these  familiar  forms  the  Insectivora  includes  the  interest- 
ing oriental  tree  shrews  {Tupaia)  (Fig.  363)  and  African  jumping 
shrews  or  elephant  shrews  {Macroscelides)  (Fig.  364),  sometimes  placed 
together  in  a  separate  suborder  ('Menotyphla').  This  group  can  be 
traced  back  to  the  Oligocene  and  more  primitive  precursors  {*Leptic- 
toidea)  of  the  Cretaceous,  where  *ZalambdaIestes  is  found  in  the  same 
deposits  as  *Deltatheridium.  The  Menotyphla  are  interesting  in  that 
they  show  in  several  ways  indications  of  primate  organization.  The 
brain  is  larger  than  in  the  insectivores  that  we  have  already  considered 


xxii.  2  BATS  585 

('Lipotyphla').  There  are  various  genera  of  elephant  shrews  in  Africa, 
all  with  long  trunk-like  snouts.  They  are  partly  diurnal  and  proceed 
by  a  series  of  jumps  with  their  long  back  legs.  There  are  five  digits  in 
hand  and  foot.  The  tree  shrews,  Tupaia  and  its  allies,  are  diurnal, 
arboreal,  squirrel-like  creatures  with  a  long  tail.  They  feed  on  insects 
or  fruit  and  show  many  lemuroid  characters.  For  instance,  there  is  a 
complete  post-orbital  bar,  and  the  brain  has  larger  hemispheres 
than  in  Macroscelides  or  other  insectivores,  and  less  development  of 
the  olfactory  regions.  The  eyes,  lateral  geniculate  body,  and  visual 
cortex  are  well  developed.  These  animals,  though  they  are  like 
insectivores,  have  a  life  very  like  that  of  lemurs  and  they  are  often 
classified  with  the  primates ;  they  show  how  narrow  is  the  gap  between 
the  two  groups,  but  we  need  not  worry  unduly  whether  they  'really' 
belong  in  one  group  or  the  other. 

2.  Order  Chiroptera.  Bats 

Cohort  Unguiculata 
Order  2.  Chiroptera 

Suborder  1.  Megachiroptera.  Oligocene-Recent 
Family  Pteropidae.  Asia,  Australia,  Africa 
Pteropus,  fruit  bat 
Suborder  2.  Microchiroptera.  Eocene-Recent 
18  families,  including: 
Family  Rhinolophidae 

Rhinolophus,  horseshoe  bats,  Europe,  Asia,  Australasia 
Family  Phyllostomatidae 

Desmodus,  vampire  bats,  S.  America 
Family  Vespertilionidae 

Vespertilio,  European  bats,  Palaearctic 
Order  3.  Dermoptera.  Palaeocene-Recent 

Cynocephalus  (=  Galeopithecus),  colugo  or  flying  lemur,  Asia 
#Order  4.  Taeniodonta.  Palaeocene-Eocene.  N.  America 

*Psittacotherium 
*Order  5.  Tillodontia.  Palaeocene-Eocene.  Europe,  N.  America 
*  Tillotherium 

Except  for  their  specializations  for  flight  the  bats  stand  very  close  to 
the  insectivores.  They  diverged  early,  however,  and  their  characteristics 
were  already  developed  in  the  Eocene.  They  are  the  only  mammals 
that  truly  fly,  by  flapping  the  wings,  as  distinct  from  the  soaring  of 
flying  phalangers,  colugos,  and  others.  The  wing  is  a  patagium  or  fold 


XXII.  2 


586  BATS 

of  skin,  involving  all  the  digits  of  the  hand  except  the  first,  and 
extending  also  along  the  sides  of  the  body  to  include  the  legs  (but  not 
the  feet)  and,  usually,  the  tail.  The  chief  skeletal  modification  is  there- 
fore a  great  elongation  of  the  arm,  and  especially  of  its  more  distal 
bones  (Fig.  365).  The  sternum  carries  a  keel  for  the  attachment  of  the 


Fig.  365.  Skeleton  of  fruit  bat  (Pteropus). 

cl.  clavicle;/,  femur;  fib.  fibula;  //.  humerus;  il.  ilium;  isc.  ischium;  pub.  pubis;  r.  radius; 
sc.  scapula;  st.  sternum;  tib.  tibia;  u.  ulna.  (From  Reynolds,  The  Vertebrate  Skeleton,  after 

Shipley  and  MacBride.) 


large  pectoral  muscles  and  the  clavicle  is  stout,  often  fused  with  the 
sternum  and  with  the  scapula.  Since  the  thorax  is  used  as  a  fixation 
point  for  the  flight  muscles  the  ribs  move  relatively  little  on  each  other 
and  respiration  is  mainly  by  the  diaphragm.  The  ribs  are  flattened  and 
may  indeed  be  fused  together  and  with  the  vertebrae.  The  charac- 
teristics of  the  arms  and  thorax  are  rather  similar  in  these  flying 
animals  to  those  found  in  brachiating  arboreal  creatures,  such  as 
gibbons,  which  also  have  long  arms  and  large,  fixed  thoracic  cages. 
The  humerus  is  very  long  and  carries  a  large  greater  tuberosity, 
which   may   acquire   a   special    articulation   with   the   scapula.   The 


XXII.  2 


SKELETON    OF    BATS 


587 


flight  movements  occur  mostly  at  the  shoulder,  with  the  rest  of  the 
limb  held  stiff.  The  radius  is  long  and  the  ulna  reduced  and  fused 
with  the  radius;  the  elbow  joint  allows  only  flexion  and  extension. 
The  carpus  is  much  specialized  by  fusion  of  bones,  allowing  flexion- 
extension  and  spreading  of  the  digits.  Of  the  five  fingers  the  first 
is  stout  and  free  of  the  wing;  it  bears  a  claw  in  Microchiroptera,  as 


Time.  10  minute  intervals 


Fig.  366.  Temperature  chart  of  greater  horseshoe  bat.  Manipulation  during 
attachment  of  thermocouple  to  back  has  caused  warming  at  beginning  of  experiment. 
Bat  stimulated  at  points  marked  s.  The  black  rectangles  mark  periods  during  which 
the  animal  was  shivering  or  moving.  Room  temperature  15-5°  C.  (From  Burbank 

and  Young.) 


does  the  second  also  in  fruit  bats.  The  remaining  metacarpals  and 
proximal  phalanges  are  enormously  elongated  to  support  the  wing,  the 
distal  phalanges  being  relatively  short.  As  in  birds  the  wings  are  short 
and  broad  in  the  slower  fliers  (horseshoe  bats),  long  and  narrow  in 
those  that  fly  faster,  with  long  rapid  beats  (noctules).  On  landing 
horseshoe  bats  turn  a  somersault  forwards  and  catch  on  with  the  hind 
legs.  Others  land  on  all  fours  and  can  walk  reasonably  well. 

The  pelvis  is  rotated  so  that  the  acetabulum  lies  dorsally  and  the 
limb  is  held  outwards  and  upwards.  The  ventral  portions  of  the  girdle 
are  thus  drawn  apart  and  are  often  not  united  in  a  symphysis.  The 
hind  legs  are  weak  and  carry  five  clawed  digits,  by  which  the  animal 
is  suspended  upside  down  when  at  rest,  the  tendons  providing  a  catch 


588 


BATS 


XXII.  2 


mechanism  so  that  no  muscular  effort  is  needed.  Even  a  large  fruit  bat 
remains  suspended  if  shot  while  hanging. 

The  great  development  of  the  arm  and  patagium  makes  it  impossible 
for  bats  to  walk  actively,  but  they  can  climb  and  crawl.  When  not 
flying  they  usually  hang  head  downwards.  When  they  excrete  they 

turn  up  and  hang  by  the  claw  of 
the  pollex,  so  that  the  wing  is  not 
soiled.  When  a  bat  is  hanging,  there 
is  no  upward  temperature  regula- 
tion. The  animal  becomes  cold 
every  time  it  rests  (Fig.  366).  When 
stimulated  it  can  walk,  open  the 
mouth  and  cry  out,  but  can  only 
fly  after  a  period  of  some  minutes 
of  warming  up  by  jerking  the  legs 
and  shivering.  Hibernation  is  pro- 
bably only  an  accentuated  form  of 
this  daily  sleep,  the  animal  living 
formonthsona'hibernation  gland', 
the  subcutaneous  fat  reserve. 

The  typical  microchiropteran  is 
an  insectivore,  often  with  molars 
of  the  ancestral  tritubercular  type 
arranged  in  a  dilambdodont  W 
pattern.  Insects  are  caught  on  the 
wing  with  the  large  mouth  and  the 
wings  bitten  off  neatly.  Diets  differ 
considerably :  some  lick  nectar  from 
flowers,  which  they  thus  pollinate. 
The  vampires  Desmodus  and 
Diphylla  of  South  America  drink 
blood  and  have  the  upper  incisors 
modified  into  cutting  blades.  Other  Microchiroptera  eat  fruit,  fish,  or 
flesh,  and  the  Megachiroptera  (flying  foxes)  of  the  tropics  are  wholly 
fruit-eaters  and  have  flattened  grinding  teeth.  The  skull  of  flying  foxes 
retains  many  primitive  features  and  resembles  that  of  an  insectivoran, 
in  the  Microchiroptera  it  is  shorter.  There  is  an  annular  tympanic  bone 
and  no  post-orbital  bar. 

Bats  obtain  the  major  part  of  their  information  through  the  ears, 
and  the  reflection  of  the  sound  waves  that  they  themselves  emit.  The 
cerebral  hemispheres  are  small  and  the  olfactory  portions  reduced, 


*'• /'„*<,,- 


Fig.  367.  Heads  of  two  bats. 

A.  Lesser  horseshoe  bat,  Rhinolophus 
hipposideros. 

B.  Whiskered  bat,  Myotis  mystacinus. 
(After  Grasse.) 


XXII.  2 


ECHOLOCATION 


589 


but  the  inferior  eorpora  quadragemina  and  cerebellum  are  large.  The 
eyes  are  often  moderately  large  and  presumably  used  in  twilight;  the 
retina  contains  mainly  rods.  The  touch  receptors  are  well  developed, 
especially  on  the  wings. 

The  echolocation  is  performed  by  discrete  pulses  of  high  intensity 
and  up  to  120  kc  frequency.  These  are  produced  by  the  very  large 
larynx,  whose  cartilages  are  ossified  to  make  a  rigid  framework.  The 


Fig.  368.  Big-eared  bat  (Plecotus). 
(After  American  Mammals,  by  W.  J.  Hamilton,  McGraw-Hill  Book  Company.) 

strong  cricothyroid  muscles  put  great  tension  on  the  light  vocal  cords. 
In  the  horseshoe  bats  there  are  special  resonating  chambers  and  the 
face  is  elaborately  modified  to  beam  the  sound  forwards  (Fig.  367). 

The  ears  of  bats  are  greatly  specialized,  often  with  very  large  pinnae. 
The  cochlea  is  large  and  the  basilar  membrane  narrow  and  tightly 
stretched.  The  tensor  tympani  and  stapedius  muscles  are  large. 

The  bat  is  almost  entirely  dependent  on  echolocation  for  avoiding 
obstacles  and  catching  insects.  If  the  larynx  is  damaged  or  the  ears 
blocked  it  blunders  against  even  large  obstacles.  The  normal  animal 
can  avoid  wires  less  than  0.5  mm  thick  in  complete  darkness  and  if 
blinded.  The  presence  of  loud  noise  at  high  frequency  disturbs  the 
bat,  but  lower  frequencies  do  not.  This  is  evidence  that  the  bat  hunts 
by  echolocation  and  not  (usually)  by  listening  to  the  sounds  made  by 
the  insects. 

The  mechanism  adopted  is  not  fully  understood  and  certainly  is  not 
always  the  same.  In  Vespertilionidae  the  sound  is  emitted  by  the 
mouth  in  pulses  of  1-4  m.  sec.  duration.  The  note  falls  through  about 


59Q 


BATS 


an  octave  in  each  pulse.  The  pulse  repetition  rate  varies  from  less  than 
io/sec  at  rest  to  over  ioo/sec  when  avoiding  obstacles  or  hunting.  The 
pinna  of  these  bats  is  very  large  and  folded  below  to  form  an  anti- 
tragus  (Figs.  367,  368).  Vespertilionids  commonly  detect  insects  at 
50  cm  and  may  do  so  at  1  m. 

In  the  horseshoe  bats  the  pulse  is  much  longer  (40-100  m.  sec), 
and  of  high  and  constant  frequency  (85-100  kc).  It  is  emitted  through 
the  nose  (Dijkgraaf)  and  beamed  by  interference  at  the  nostrils,  which 


Fig.  369.  Diagram  showing  interference  pattern  of  the  ultrasonic  waves  from  the 

nares  of  a  horseshoe  bat.  Peaks  are  indicated  by  a  continuous  line,  valleys  by 

dashes.  The  dotted  lines  limit  the  sector  in  which  the  waves  are  most  intense, 

maximal  in  the  sagittal  plane. 

n.  nares;  s.p.  sagittal  plane.  (After  Mohres.) 

are  set  half  a  wavelength  apart  (Fig.  369).  The  pulse  repetition  rate  is 
low  (<io/sec).  This  mechanism  is  even  more  effective  than  the  other 
and  is  said  to  detect  insects  even  at  6  m  (Mohres). 

It  was  first  suggested  by  Hartridge  by  analogy  with  early  audio- 
location  and  radar  devices  that  bats  estimate  distance  by  measuring 
the  echo  delay.  The  middle  ear  muscles  and  intra-aural  reflexes  do 
indeed  allow  a  very  rapid  recovery  of  sensitivity  after  short  loud 
sounds,  as  would  be  necessary,  forming  a  sort  of  transmit-receive 
switch  (Griffin,  1958).  Yet  it  hardly  seems  possible  that  the  reflex 
can  work  fast  enough  to  allow  accuracy  at  short  distances.  An  alter- 
native hypothesis  is  that  the  bat  measures  the  loudness  of  the  echoes, 
especially  the  horsehoe  bats,  with  their  long  pulses  (Mohres).  The 
beam  movements  might  give  direction  and  searching  movements  the 
range  by  triangulation.  This  theory  seems  to  require  a  very  complete 
acoustic  separation  of  ear  and  nasopharynx  and  special  cerebral 
capacities  for  calculation. 

A  third  suggestion  is  that  the  ear  receives  both  the  outgoing  and 


XXII.  2 


HEARING    IN    BATS 


59i 


reflected  notes  and  constructs  difference  or  summation  tones  by  the 
introduction  of  a  specific  non-linear  device  (Pye,  i960).  Since  the 
sound  is  used  only  for  location  its  absolute  qualities  are  not  important 
for  a  bat  as  they  are  for  man.  With  this  method  any  object  within 
range  will  be  located  by  the  variation  in  the  beat  notes  that  are  pro- 
duced as  its  position  changes. 

The  distortion  required  to  produce  the  beat  notes  might  perhaps 
be  a  function  of  the  middle  ear  muscles,  but  is  more  probably  a 
property  of  the  cohlea.  Distortion  of 
cochlear  microphonic  potentials  is 
known  to  occur  in  other  animals  at 
sound  intensities  lower  than  those 
emitted  by  bats.  Such  a  mechanism 
could  thus  readily  have  been  evolved 
from  a  more  conventional  hearing 
system  without  any  fundamental 
change  either  in  the  ear  or  brain. 
Only  the  cochlear  microphonics  need 
to  follow  the  high  notes  of  the  bat's 
voice.  The  auditory  nerve  carries  in- 
formation only  about  the  difference 
notes  of  a  few  kc,  which  could  be 
readily  recognized  by  the  brain. 

Horseshoe  bats  often  seem  to  search 
around  when  they  are  stationary  and 
there  is  some  evidence  that  under 
these  conditions  they  introduce  an 
artificial  velocity  factor,  and  hence  a 
Doppler  shift,  by  movements  of  the 
ears,  which  may  occur  at  as  much  as 
50/sec.  However,  it  is  not  clear  exactly  how  this  is  achieved  or  how  it 
is  related  to  a  second  opening  of  the  meatus  that  lies  at  the  non- 
moving  base  of  the  pinna  and  leads  by  a  groove  to  the  nose-leaf, 
with  its  lance  and  shield  (Fig.  367). 

Some  bats  (Hipposideridae)  may  use  both  methods,  the  later  part 
of  each  pulse  being  modulated.  All  bats  also  produce  sounds  of  lower 
frequency,  perhaps  as  specific  recognition  signals. 

The  placenta  is  of  a  discoidal  form  and  haemochorial,  at  least  in 
some  types.  A  peculiar  feature  is  that  copulation  occurs  in  the  autumn 
and  the  sperms  remain  alive  (but  presumably  not  active)  within  the 
female  until  fertilization  takes  place  in  the  spring.  The  young  are  well 


Fig.  370.  Diagrammatic  view  from 
above  the  head  of  a  horseshoe  bat, 
showing  a  possible  means  of  estimating 
distances  using  the  principle  of  differ- 
ences in  intensities. 

The  left  ear  does  not  receive  an 
echo,  but  the  right  ear  because  it  is 
turned  inwards,  receives  the  reflected 
waves.  The  thick  black  line  that  limits 
the  pinna  anteriorly  is  the  antitragus, 
which  is  used  as  the  echo  receptor. 

m.l.  the  median  line  is  the  zone  of  maxi- 
mum intensity  of  the   ultrasonic  waves ; 
g.  is  an  object  in  the  wave  field. 
(After  Mohres.) 


592  BATS  xxii.  2- 

formed  at  birth  and  have  then  already  cut  the  milk  dentition  of  special 
teeth,  with  sharp,  backwardly  directed  hooks,  which,  with  the  claws, 
enable  the  baby  to  remain  attached  to  the  mother  in  flight.  Most  bats 
live  massed  together  in  colonies  during  the  day,  with  a  considerable 
social  organization.  They  spread  out  at  night  and  home  accurately. 
After  artificial  displacement  marked  bats  return  home  from  ioo  km  or 
more.  Some  species  hibernate  in  large  colonies  where  there  are  suitable 
caves  and  then  migrate  for  1,000  km  or  more  and  return  to  the  same 
cave  next  winter. 

The  Megachiroptera,  fruit  bats  or  flying  foxes,  are  quite  large 
animals  (with  wing  span  up  to  5  ft.)  living  in  Asia,  the  Pacific,  Aus- 
tralia, and  Africa.  In  spite  of  their  diet  they  are  in  some  ways  the 
less-specialized  group,  having  a  snout,  head,  and  ears  of  normal 
mammalian  form. 

The  Microchiroptera  is  one  of  the  most  successful  groups  among 
modern  mammals,  including  a  large  number  of  families,  genera,  and 
species,  with  differing  habitats.  As  would  be  expected,  the  families 
often  have  wide  geographical  ranges,  vespertilionids,  for  instance,  are 
found  all  over  the  world.  It  is  interesting,  however,  that  the  genera 
mostly  have  a  rather  restricted  range.  For  instance,  Vespertilio  is 
limited  to  the  Palaearctic,  though  Pipistrellus  is  found  also  in  North 
America.  The  vampire  bats  (Phyllostomatidae)  are  restricted  to  Central 
and  South  America.  The  fact  that  even  flying  mammals  should  be  so 
restricted  is  good  evidence  that  the  simple  problem  of  communication 
is  one  of  the  least  of  the  difficulties  standing  in  the  way  of  the  dispersal 
of  an  animal  type. 

3.  Order  Dermoptera 

The  colugo  or  flying  lemur  of  the  orient,  correctly  called  Cyno- 
cephalus  (—  Galeopitheciis),  was  probably  an  early  offshoot  from  the 
insectivoran  stock,  with  a  patagium  developed  for  parachuting.  The 
wing  differs  from  that  of  bats  in  that  the  fingers  are  not  elongated  and 
the  wing  is  not  flapped.  The  animals  are  nocturnal  and  feed  on  leaves 
and  fruit.  A  peculiarity  is  the  forwardly  projecting  lower  incisors  with 
tips  divided  to  form  a  comb,  as  in  lemurs.  A  related  Palaeocene  form 
shows  that  this  line  has  been  separate  for  more  than  50  million  years. 

4.  Order  Edentata 

Cohort  Unguiculata 
Order  6.  Edentata 
^Suborder  1.  Palaeanodonta.  Palaeocene-Oligocene.  N.  America 
*Metacheiromys,  Eocene 


xxn.  4  EDENTATES  593 

Suborder    2.    Xenarthra.    Palaeocene-Recent.    Central    and    S. 
America 

Infraorder  1.  Cingulata.  Palaeocene-Recent 
Superfamily  1.  Dasypodoidea.  Armadillos 

Dasypus,  nine-banded  armadillo 
*Superfamily  2.  Glyptodontoidea.  Upper  Eocene-Pleistocene 

*Glyptodon 

Infraorder  2.  Pilosa.  Upper  Eocene-Recent.   Central  and  S. 
America 
*Superfamily   1.   Megalonychoidea.   Ground  sloths.   Upper 
Eocene-Pleistocene 
* Megatherium ;  *Mylodon 
Superfamily  2.   Myrmecophagoidea.   Ant-eaters.   Pliocene- 
Recent 
Myrmecophaga,  giant  ant-eater;  Tamandua,  tamandua; 
Cyclopes,  two-toed  ant-eater 
Superfamily  3.  Bradypodoidea.  Sloths.  Recent 

Bradypus,  three-toed  sloth;  Choloepus,  two-toed  sloth, 
unau 

Order  7.  Pholidota 

Family  Manidae.  Oligocene-Recent 

Manis,  scaly  ant-eater  (pangolin),  Asia,  Africa 

The  reduction  or  loss  of  the  teeth  with  adoption  of  a  diet  of  soft 
invertebrates  and  especially  ants  has  occurred  independently  at  least 
five  times  among  mammals ;  this  habit  is  indeed  to  be  expected,  since 
the  whole  mammalian  stock  was  at  first  insectivorous.  We  have  already 
noticed  the  occurrence  of  ant-eating  characteristics  in  the  echidnas  and 
in  Myrmecobius,  the  marsupial  ant-eater.  Among  eutherians  the  habit 
is  well  developed  in  animals  of  three  different  types,  (1)  the  ant-eaters 
of  South  America,  Myrmecophaga  and  its  allies,  (2)  the  pangolins  of 
Africa  and  Asia,  Manis,  and  (3)  the  aardvark  or  Cape  ant-eater 
(Orycteropus) .  These  ant-eating  animals  have  many  features  in  com- 
mon. They  all  possess  a  long  snout  and  tongue,  very  large  salivary 
glands,  and  reduced  teeth;  because  of  these  similarities  they  were  for 
a  long  time  classed  together  as  Edentata.  It  has  gradually  become 
apparent,  however,  that  the  three  groups  of  placental  ant-eaters 
have  evolved  separately.  The  aardvark  was  probably  an  early  offshoot 
from  the  ferungulate  stock  (p.  704).  The  pangolins  are  placed  in  the 
Unguiculata,  but  they  represent  a  separate  line,  diverging  from  the 


594  EDENTATES  xxn.  4- 

insectivoran  stock  very  early  (p.  601).  The  South  American  ant- 
eaters  form  a  natural  group  with  the  armadillos  and  sloths,  having, 
like  the  South  American  ungulates  and  other  animals,  proceeded  along 
several  courses  of  evolution  of  their  own  during  the  long  isolation  of 
their  continent  throughout  the  Cenozoic  period.  The  term  Edentata  is 
now  reserved  for  this  South  American  group. 

In  many  ways  the  Edentata  remain  close  to  the  basic  eutherian 
condition.  The  characteristic  feature  has  been  a  simplification  of  the 
teeth,  which  are  absent  altogether  in  the  ant-eaters  themselves.  In 
sloths  and  armadillos  the  front  teeth  are  absent  and  the  hinder  ones 
are  rows  of  similar  pegs,  with  no  covering  of  enamel.  Except  in  sloths, 
there  is  considerable  elongation  of  the  snout  and  the  whole  cranium 
is  of  tubular  form,  with  a  low  brain-case,  containing  a  small  brain  with 
poorly  developed  hemispheres,  having  a  large  olfactory  region.  The 
jugal  bar  is  often  incomplete,  but  the  hind  end  of  the  jugal  carries  a 
large  downward  extension  in  sloths  and  ground  sloths.  A  characteristic 
common  to  all  the  Edentata  is  the  presence  of  extra  articulations  be- 
tween the  lumbar  vertebrae,  a  striking  feature  in  view  of  many  different 
modes  of  locomotion  in  the  group.  From  these  articulations  the  group 
gets  its  name,  Xenarthra.  Several  other  peculiar  features  of  the 
skeleton  are  common  to  most  or  all  these  animals,  such  as  a  fusion  of 
the  coracoid  with  the  acromion  to  enclose  a  coracoscapular  foramen 
and  a  union  between  the  ischium  and  the  caudal  vertebrae.  The  feet 
have  well-developed  claws,  often  used  for  digging,  and  the  animals 
may  walk  on  the  outside  of  the  claws,  though  some  species  are  arboreal 
and  use  the  claws  for  hanging. 

Many  of  the  characteristics  of  the  group  are  obviously  those  of  all 
generalized  eutherians,  the  edentates  having  departed  little  from  the 
original  mammalian  plan.  For  example,  they  all  have  rather  low 
temperatures,  fluctuating  widely  with  the  environment.  Their  features 
are  mostly  the  result  of  special  ways  of  life,  often  leading  to  bizarre 
external  appearances,  such  as  the  long  snout  of  the  great  ant-eater  or 
the  carapace  of  the  armadillo. 

The  order  Edentata  is  divided  into  two  suborders,  the  first  *Palae- 
anodonta  for  a  few  Palaeocene  and  Eocene  types  such  as  *Meta- 
cheiromys,  which  had  not  yet  acquired  the  structure  of  the  vertebrae 
found  in  all  the  remaining  edentates  (suborder  Xenarthra).  The 
palaeanodonts  are  found  in  North  America  and  are  held  by  some  to  be 
survivors  of  the  original  stock,  existing  before  the  separation  of  the 
continents.  The  xenarthrous  population  itself  split  up  early  and  we 
can  recognize  two  main  groups  (infraorders),  the  Cingulata  for  the 


xxii.  5  ARMADILLOS  595 

armadillos  and  glyptodons,  and  Pilosa  for  the  ant-eaters,  sloths,  and 
ground  sloths. 

5.  Armadillos 

The  armadillos  (Dasypodidae)  (Fig.  371)  have  departed  least  from 
the  ancestral  plan  and  are  a  very  ancient  group,  already  differentiated 
in  Palaeocene  times.  They  are  nocturnal  and  fossorial  and  obtain 
protection  by  the  development  of  bony  plates  in  the  skin,  these  being 


\Mku; 


Fig.  371.  Hairy  armadillo,  Dasypus.  (From  photographs.) 


Fig.  372.  Glyptodon.  (From  a  reconstruction  lent  by  the  Trustees  of  the  British  Museum.) 

covered  by  horny  scutes.  The  plates  are  usually  arranged  in  rings 
round  the  body  and  in  some  genera  they  allow  the  animal  to  roll  up 
into  a  ball.  The  vertebrae  tend  to  be  fused  to  support  the  shield,  and 
many  vertebrae  unite  in  the  sacrum.  The  teeth  are  simple  uniform  pegs, 
without  enamel,  and  with  open  roots  and  continuous  growth.  They  are 
often  more  numerous  than  in  other  mammals  (as  many  as  twenty-five 
in  each  jaw);  with  simplification  of  the  system  of  tooth  morphogenesis, 
repetition  becomes  possible,  as  we  see  also  in  whales.  The  armadillos 
are  insectivores  and  omnivorous  scavengers  in  tropical  Central  and 
South  America ;  there  are  many  different  genera  and  species.  The  nine- 
banded  armadillo  (D.  novemcinctatus)  is  a  very  active  burrower  and  is 


596 


EDENTATES 


xxii.  5 


Fig.  373.  Giant  South  American  edentates  of  the  Pleistocene.  Megatherium,  the 

giant  ground  sloth,  was  the  size  of  a  modern  elephant.  The  glyptodonts  were 

related  to  the  armadillos.  (From  a  mural  by  C.  R.  Knight.) 


Fig.  374.  Great  ant-eater,  Myr?necophaga,  from  life. 


Fig.  375.  Lesser  ant-eater,  Tamandua.  (From  photographs.) 

Fig.  376.  Tree  ant-eater,  Cyclopes,  showing  one  of  the 

peculiar  attitudes  adopted,  perhaps  to  startle  an  attacker 

(dymantic  posture).  (From  a  photograph.) 

spreading  northwards  in  the  United  States  with  the  destruction  of  its 
carnivore  enemies  by  man.  The  haemochorial  placenta,  at  first  diffuse 
then  discoidal,  is  modified  as  a  result  of  the  process  of  polyembryony. 
After  cleavage  the  embryo  divides  into  eight  or  twelve  secondary 
embryos,  all  developing  within  a  single  amnion. 


xxii.  6 


SKULLS   OF  ANT-EATERS 


597 


During  the  Pleistocene  and  earlier  periods,  besides  the  modern 
armadillos,  there  were  also  giant  armadillos.  The  glyptodonts  (Fig. 
372)  were  a  related  type,  diverging  as  early  as  the  Upper  Eocene,  with 
a  skull  and  carapace  composed  of  many  fused  small  pieces  and  some- 
times the  well-known  'battle-axe'  tail.  They  show  a  remarkable  con- 
vergence with  tortoises  and  some  dinosaurs  and  probably  lived  in 
deserts. 

6.  Ant-eaters  and  sloths 

The  modern  soft-skinned  edentates  (ant-eaters  and  sloths)  are  very 
specialized  and  not  superficially  like  the  armadillos.  The  enormous 
ground  sloths  (Fig.  373),  of  which  there  were  several  families  living 


T  L 


Fig.  377.  Side  views  of  adult  skulls  of  A,  Myrmecophaga;  B,  Tamandua;  C,  Cyclopes. 

Tamandua  and  Cyclopes  are  approximately  i  J  and  3  times  the  scale  of  Myrmecophaga. 

T.L.  measurement  of  total  length;  M.L.  of  maxilla  length.  (From  Reeve.) 

between  the  Oligocene  and  Pleistocene,  were  in  some  respects  inter- 
mediate between  the  two  types.  They  were  quadrupedal  animals,  but 
the  fore-limbs  were  shorter  than  the  hind  and  provided  with  long 
claws.  Probably  the  ground  sloths  were  largely  bipedal,  perhaps  crawl- 
ing slowly  about  with  their  fore-limbs  among  the  branches  and  bearing 
them  down  with  their  weight.  The  brain  was  small  but  the  teeth  large 
and  hypsodont.  Nearly  fifty  genera  of  ground  sloths  have  been  recog- 
nized and  they  were  evidently  successful  in  the  South  American 
forests.  * Megatherium  was  larger  than  an  elephant  and  a  similar  form, 
*Neomylodon}  persisted  nearly  to  the  present  day.  Pieces  of  its  skin  have 
been  found,  and  these,  even  in  the  favourable  conditions,  can  hardly 


598 


EDENTATES 


xxii.  6 


have  maintained  their  appearance  for  more  than  a  few  hundreds  or  at 
the  most  thousands  of  years. 

The  ant-eaters  (Myrmecophagidae)  have  a  characteristic  elongated 
snout,  without  teeth.  There  are  three  genera,  differing  in  size,  and 


20 


30  40         50  70  90 

Cranium  Length  Logarithmic  scale  mm. 


1Z0  160 

Scale  for  A\ 


Fig.   378.   Logarithmic  plots   of  lengths  of  maxillae   (a's)   and   nasals   (u's) 

against  cranium. 
The  suffixes  represent:  1,  Myrmecophaga;  2,  Tamandua;  3,  Cyclopes.  Scale  for  B  graphs 
is  shifted  to  the  right  compared  with  a's.  Crosses  at  bottom  of  lines  for  A2  and  B, 
represent  a  very  young  Tamandua.  The  lines  were  fitted  to  each  sample  by  least  squares. 

(From  Reeve.) 

the  larger  species  have  relatively  much  the  longer  snouts.  The  great 
ant-eater  Myrmecophaga  (Fig.  374)  has  an  enormously  elongated 
face,  but  this  is  much  shorter  in  the  smaller  Tamandua  (Fig.  375),  and 
the  very  small  tree-living  Cyclopes  (Fig.  376)  has  a  head  of  normal 
mammalian  shape.  Analysis  shows  that  there  is  little  difference  be- 


xxii.  6  SLOTHS  599 

tween  the  relative  rate  of  growth  of  the  faee  in  these  three  genera,  and 
the  differing  final  forms  result  mainly,  though  not  wholly,  from  the 
differences  in  absolute  size  (Figs.  377  and  378).  In  all  ant-eaters  the 
face  becomes  relatively  longer  as  the  animal  increases  in  size,  and  the 
enormous  snout  of  the  great  ant-eater  is  produced  by  a  relative  growth- 
rate  only  slightly  higher  than  that  found  in  Tamandua  and  Cyclopes. 
This  is  an  excellent  example  of  the  way  in  which  the  proportions  of  an 
organ  will  vary  in  animals  of  different  sizes  if  its  growth  is  allometric, 


Fig.  379.  Two-toed  sloth,  Choloepus.  (From  a  photograph  in  Scott, 

Land  Mammals,  copyright  1913,  1937  by  the  American  Philosophical 

Society  and  used  with  the  permission  of  the  Macmillan  Company.) 

that  is  to  say,  relatively  faster  or  slower  than  that  of  the  body  as  a 
whole  (p.  737). 

The  hard  palate  is  prolonged  backwards  in  Myrmecophaga  by  union 
of  the  pterygoids,  a  condition  found  also  in  some  armadillos  (Dasypus). 

The  great  ant-eater  is  a  fine  animal,  over  6  ft  long,  with  a  long  hairy 
coat,  including  a  very  bushy  tail  and  with  a  black  stripe  edged  with 
brown  at  the  shoulder.  It  has  a  long  thin  tongue  for  collecting  ants, 
and  enormous  submaxillary  salivary  glands.  The  claws  of  the  front 
legs  are  very  large  and  used  for  defence  as  well  as  for  digging.  Taman- 
dua and  Cyclopes  differ  from  Myrmecophaga  in  other  features  besides 
the  length  of  snout.  They  are  arboreal  and  the  tail  is  prehensile. 

The  sloths  (Bradypodidae)  (Fig.  379)  are  fully  adapted  for  arboreal 
life  and  can  hardly  walk  on  the  ground.  They  show,  as  do  the  bats, 
how  the  mammalian  skeleton  can  be  used  with  surprisingly  little 
change  to  support  weight  by  hanging,  the  limbs  being  used  as  tension 
members  rather  than  as  pillars.  In  marked  contrast  to  the  ant-eaters 
the  face  is  short  and  the  head  rounded,  with  large  frontal  air  sinuses. 
The  neck  is  peculiar  for  the  presence  of  nine  or  ten  cervical  vertebrae 
in  the  three-toed  sloth,  Bradypus.  This  might  be  supposed  to  provide 
a  flexible  neck  for  an  animal  that  must  often  face  backward,  were  it  not 
that  in  the  two-toed  sloth  Choloepus  there  are  but  six  cervical  vertebrae. 


6oo 


EDENTATES 


xxii.  6- 


The  limbs  are  long,  especially  the  fore-limbs,  and  the  digits  carry 
hooked  claws  for  hanging  (Fig.  380).  In  the  pectoral  girdle  the  clavicle 
articulates  with  the  coracoid,  a  unique  condition  among  mammals.  As 
in  ant-eaters  the  acromion  is  connected  with  the  coracoid,  enclosing  a 
coraco-scapular  foramen.  The  significance  of  these  special  features  is 
not  clear,  but  the  habit  of  hanging  upside  down  has  produced  some 
obvious  modifications,  for  instance  all  the  vertebral  neural  spines  are 


Fig.  380.  Skeleton  of  three-toed  sloth,  Bradypus.  (After  Blainville.) 

low  and  the  pelvis  is  short.  Even  here,  however,  we  find  peculiar 
similarities  to  the  ant-eaters,  in  the  union  of  the  ischium  with  caudal 
vertebrae,  a  feature  whose  adaptive  significance  is  obscure. 

The  sloths  live  on  foliage,  but  this  herbivorous  diet  is  perhaps 
secondary  to  a  long  period  of  insectivorous  life,  during  which  there 
was  a  reduction  of  the  teeth  and  loss  of  enamel.  On  adoption  of  the 
new  way  of  life  the  enamel  could  not  be  restored,  but  a  grinding  surface 
is  provided  by  the  presence  of  cement  and  continuous  growth  of  the 
teeth.  The  stomach  is  large  and  divided  into  several  chambers,  recall- 
ing those  of  ruminants.  The  rectum  is  enormous  and  the  masses  of 
faeces  are  retained  for  several  days,  intestinal  peristalsis  being  as  slow 
as  all  the  other  movements  of  these  creatures.  Interesting  features  con- 
nected with  this  slow  life  are  the  small  size  of  the  thyroid  and  adrenals. 

The  sloths  live  in  the  rain  forests  of  South  and  Central  America, 


xxii.  7 


PANGOLINS 


60 1 


moving  very  slowly  among  the  branches,  which  they  come  to  resemble 
closely  by  the  growth  of  blue-green  algae  in  special  grooves  in  the 
hairs.  Their  upside-down  posture  has  led  to  many  changes  from  the 
typical  mammalian  organization,  including,  it  is  said,  a  reversal  of  the 
usual  mechanism  for  maintaining  posture.  When  a  normal  mammal 
is  decerebrated  its  legs  assume  a  pillar-like  extensor  rigidity,  because 
of  the  overaction  of  the  reflexes  of  standing.  A  decerebrate  sloth  is  said 
to  show  the  opposite,  flexor  rigidity. 

7.  Order  Pholidota  :  pangolins 

The  pangolins  or  scaly  ant-eaters,  Manis  (Fig.  381)  of  the  Old  World 
(Africa  and  Asia)  have  many  features  superficially  like  those  of  the 
New  World  ant-eaters  and  the  groups 
may  be  remotely  related.  Unfortu- 
nately nothing  is  known  of  the  fossil 
history  of  Manis  and  its  position 
among  the  unguiculates  is  therefore 
provisional.  The  body  is  up  to  5  ft 
long,  covered  with  horny  epidermal 
scales,  interspersed  with  hairs.  The 
absence  of  teeth,  the  elongated  snout, 
long  thin  tongue,  simple  stomach, 
reduced  ears,  and  long  claws  are  all 
features  found  in  the  other  ant-eaters. 
Rods  of  cartilage  extending  backwards 
from  the  xiphisternum  have  been 
compared  with  the  abdominal  ribs  of 
reptiles,  but  are  probably  a  special 
development,  connected  with  the  pro- 
trusion of  the  enormous  tongue,  which 
is  carried  in  a  special  sac  and  operated 

by  muscles  attached  to  the  xiphisternal  processes.  The  animals  are 
macrosmatic,  with  small  eyes.  The  brain  is  very  small,  but  the  hemi- 
spheres are  folded.  The  placenta  is  diffuse  and  epithelio-chorial,  with 
a  large  allantois  and  a  yolk-sac  persisting  until  birth.  Evidently  the 
pangolins  preserve  many  very  ancient  mammalian  features.  There  are 
various  species  of  Manis;  some  live  in  open  savannah,  others  are  able 
to  climb  trees.  All  are  nocturnal  and  eat  ants  and  termites. 


Fig.  381.  Black-bellied  tree  pangolin, 
Manis.  (From  photographs.) 


XXIII 

PRIMATES 


1.  Classification 


Order  8.  Primates 
Suborder  I.  Prosimii.  Palaeocene-Recent 
Infraorder  i.  Lemuriformes.  Palaeocene-Recent 

*Family    i.    Plesiadapidae.    Palaeocene-Eocene.    Europe,    N. 
America 
*Plesiadapis,  Palaeocene 
*Family  2.  Adapidae.  Eocene.  Europe,  N.  America 

*Notharctus ;  *Adapis 
Family  3.  Lemuridae.  Pleistocene-Recent.  Madagascar 

*Megaladapis,  Pleistocene;  Lemur,  common  lemur 
Family  4.  Indridae.  Pleistocene-Recent.  Madagascar 

Ifidri,  indris 
Family  5.  Daubentoniidae.  Recent.  Madagascar 
Daubefitonia  (=  Cheiromys),  aye-aye 
Infraorder  2.  Lorisiformes.  Pliocene-Recent.  Asia  and  Africa 
Family.  Lorisidae. 

Loris,    slender    loris,    India;    Galago,    bush    baby,    Africa; 
Perodicticus,  potto,  Africa 
Infraorder  3.  Tarsiiformes.  Palaeocene-Recent.  Holarctic,  Asia 
*Family  1.  Anaptomorphidae.  Palaeocene-Oligocene 

*Necrole?nur,  Eocene,  Europe;  *Pseudoloris,  Eocene,  Europe 
Family  2.  Tarsiidae.  Recent.  E.  Indies 
Tarsius,  tarsier 
Suborder  2.  Anthropoidea.  Oligocene-Recent 
Superfamily    1.    Ceboidea.    New    World    monkeys.    Miocene- 
Recent.  S.  America 
Family  1.  Callithricidae.  Recent 

Callithrix  (=  Hapale),  marmoset 
Family  2.  Cebidae.  Miocene-Recent 

*Ho?nu?icuhis,    Miocene;    Cebus,    capuchin;    Ateles,    spider 
monkey;  Alouatta,  howler  monkey 
Superfamily  2.  Cercopithecoidea.  Oligocene-Recent 
*Family  1.  Parapithecidae.  Oligocene.  Africa 
*Parapiihecus 


xxiii.  1-2  PRIMATE   CHARACTERS  603 

Family  2.  Cercopithecidae.  Old  World  monkeys.  Oligocene- 
Recent.  Africa,  Asia 
*Mesopithecus,  Miocene;  Macaca,  rhesus  monkey,  macaque, 
Asia,  N.  Africa;  Papio,  baboon,  Africa;  Mandrillus, 
mandrill,  Africa;  Cercopithecus,  guenon,  Africa;  Presbytis, 
langur,  E.  Asia;  Colobus,  guereza,  Africa 
Superfamily  3.   Hominoidea 

Family  1.  Pongidae.  Apes.  Oligocene-Recent 

*Propliopithecus,  Lower  Oligocene,  Egypt;  *Pliopithecus, 
Lower  Miocene,  Europe,  Africa;  *Dryopithecus,  Miocene, 
Africa,  Asia;  *Oreopithecus,  Pliocene,  Europe;  *  Australo- 
pithecus, Pleistocene,  S.  Africa;  *  Proconsul,  Miocene, 
Africa;  Hylobates,  gibbon,  SE.  Asia;  Pongo,  orang-utan, 
E.  Indies;  Pan,  chimpanzee,  Africa;  Gorilla,  gorilla,  Africa 
Family  2.  Hominidae.  Man.  Pleistocene-Recent 

* Pithecanthropus  (=  *Sinanthropus),  Java  and  Pekin  man, 
Pleistocene,  E.  Asia;  Homo,  man  (all  living  races).  Pleisto- 
cene-Recent 

2.  Characters  of  primates 

Linnaeus  reserved  his  order  Primates  for  the  monkeys,  apes,  and 
men,  distinguishing  them  thus  from  the  other  mammals,  Secundates, 
and  all  other  animals,  Tertiates.  The  term  primate  carries  with  it 
the  implication  that  the  animals  in  the  group  are  not  only  the  nearest 
to  ourselves  but  are  also  in  some  sense  the  first  or  most  completely 
developed  members  of  the  animal  world.  We  shall  try  to  examine  this 
belief  in  accordance  with  the  principles  adopted  earlier  and  to  inquire 
whether  we  and  our  relatives  can  be  said  to  be  the  highest  animals  in 
the  sense  that  we  possess  a  system  of  life  able  to  survive  under  the 
most  varied  and  unpromising  conditions. 

The  earliest  eutherians  of  the  Cretaceous  were  probably  arboreal ; 
the  primates  have  continued  this  habit  and  with  it  they  retain  many 
of  the  features  present  at  the  beginning  of  mammalian  history,  for 
instance  the  five  fingers  and  toes  and  the  clavicle.  Primates  already 
existed  in  the  Palaeocene,  65  million  years  ago  and  have  a  longer  geo- 
logical history  than  any  other  placentals  except  the  insectivores  and  car- 
nivores. It  is  not  surprising,  therefore,  that  it  is  difficult  to  separate  the 
primates  from  the  insectivores;  the  tree  shrews,  for  instance  (p.  584), 
have  several  times  been  transferred  from  the  one  order  to  the  other. 

The  primates  have  retained  many  primitive  mammalian  features, 
some  of  which  have  become  strongly  accentuated  for  arboreal  life. 


6o4  THE   PRIMATES  xxm.  2 

Their  characters  are  those  of  animals  raised  up  from  the  ground ;  the 
opportunities  offered  in  the  trees  for  the  use  of  hand  and  brain  have 
no  doubt  been  important  influences  in  the  shaping  of  man. 

The  general  plan  of  primate  life  has  thus  been  to  retain  the  original 
eutherian  conditions,  with  emphasis  on  those  features  important  for 
tree  life.  In  such  an  existence  continual  quick  reaction  to  circum- 
stances is  likely  to  be  necessary,  the  environment  is  varied,  and  the 
mechanical  supports  it  offers  are  often  precarious.  Under  these  condi- 
tions safety  is  achieved  by  quick  reactions  rather  than  by  stability; 
thus  primate  more  than  any  other  life  tends  to  be  a  matter  of  con- 
tinual exploration  and  change.  The  information  that  ensures  the  life 
of  the  species  is  obtained  by  the  individuals  and  stored  in  their  brains, 
rather  than  by  selection  among  large  numbers  of  rapidly  breeding 
individuals.  The  time  taken  for  development  thus  increases  in  the 
primate  series.  Growth  continues  for  about  3  years  in  prosimians,  7  in 
monkeys,  9  in  gibbons,  12  in  other  apes,  and  20  in  man.  To  obtain 
this  information  receptors  are  obviously  of  first  importance,  but  in  the 
tree-tops  one  cannot  hunt  by  smell;  the  eyes  and  ears  therefore  became 
developed,  at  the  expense  of  the  nose.  Primates  are  microsmatic,  with 
reduction  of  the  number  and  length  of  the  turbinal  bones  and  hence 
of  the  long  snout  that  houses  them.  Consequently  the  eyes  come  to 
face  forwards,  so  that  their  fields  overlap,  binocular  vision  becomes 
possible,  and  central  areas  appear  in  the  retinas.  Monkeys  are  certainly 
more  dependent  on  vision  than  are  most  animals  and  for  this  reason 
they  approach  the  birds  in  the  adoption  of  colour  patterns  for  sexual 
recognition  and  excitation. 

The  changes  in  the  receptors  were  accompanied  by  conspicuous 
changes  in  the  brain,  which  becomes  very  large  in  later  primates,  with 
cerebral  hemispheres  reaching  far  backwards.  The  olfactory  bulbs  and 
rhinopallium  become  small  and  the  neopallium  very  large,  differen- 
tiated into  areas  and  provided  with  a  large  corpus  callosum.  The 
occipital  pole,  concerned  with  vision,  and  the  frontal  areas,  become 
especially  well  developed  in  the  apes  and  man.  Stereoscopic  eyes  with 
numerous  cones  would  be  of  no  value  without  a  central  analyser  to 
allow  the  animal  to  discriminate  shapes,  retain  the  impression  of  past 
situations,  and  otherwise  make  use  of  the  available  information.  The 
marked  differences  in  the  rate  of  growth  of  the  brain  of  different 
primates  are  shown  in  Fig.  382,  from  Schultz's  careful  measurements. 
At  early  stages  of  development  all  the  primates  studied  have  the  same 
(high)  relative  brain  weight,  but  in  the  adults  the  brain  is  relatively 
and  absolutelv  larger  in  man  than  in  monkeys  or  apes. 


xx  hi 


CRANIAL  CAPACITY 


O05 


The  special  developments  of  the  receptors  and  brain  have  marked 
effects  on  the  skull,  whose  facial  portion  becomes  shorter  and  the 
brain-case  relatively  larger  and  rounder;  the  foramen  magnum  comes 
to  face  downwards,  rather  than  backwards.  As  the  eyes  are  directed 
forwards  the  orbits  become  closed  off  from  the  temporal  fossae  behind. 


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1  1 

1  ', 

1 

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xi 

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^ 

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-L. 

^ 

k 

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2-\r= 


10        20 


30       40 
Body  1 


50       60 
ighb  Kg. 


70       80        90 


Fig.  382.  The  relative  cranial  capacity  as  a  function  of  body-weight  in  various  primates. 
The  brain  grows  relatively  faster  in  man  than  in  either  monkeys  or  apes.  The  curves  are 
constructed  by  measuring  cranial  capacity  and  body-weight  of  individuals  of  differing 
ages.  The  monkeys  included  various  Cercopithecidae,  the  apes  only  gorillas,  chimpanzees, 
and  orangs.  (Modified  after  Schultz,  Am.  J.  phys.  Anthropol.  28.) 

The  head  is  more  clearly  marked  off  from  the  body  than  is  usual  in 
mammals  and  the  neck  is  very  mobile,  allowing  the  eyes  to  be  turned 
in  all  directions. 

The  skeletal  and  muscular  systems  become  arranged  to  allow  jump- 
ing, swinging,  and  grasping.  The  pentadactyl  plan  is  retained,  without 
the  loss  of  digits  or  fusion  of  bones  that  are  found  in  most  mammals, 
but  the  hand  and  foot  are  made  suitable  for  grasping  by  development 
of  adduction  movements  of  pollex  and  hallux.  The  digits  mostly  have 
sensitive  pads  and  the  original  claw  is  replaced  by  a  flat  nail.  The 
clavicle  remains  large  and  indeed  is  specially  developed  in  primates  to 
allow  mobility  of  the  fore-limb,  the  muscles  being  arranged  to  allow 
rotation  of  the  scapula,  increasing  the  range  of  movement.  Still  further 


0o6 


THE    PRIMATES 


XXIII.  2- 


mobility  is  provided  by  improving  the  joints  between  radius  and 
ulna  and  humerus  at  which  movements  of  pronation-supination 
take  place. 

The  primates  early  ceased  to  feed  only  on  insects,  and  took  to  a 
mixed  diet;  the  teeth  have  not  become  so  specialized  as  in  ungulate 
mammals.  The  hands  are  frequently  and  ingeniously  used  to  obtain 


Fig.  383.   Upper  and  lower  dentition.   A.  Modern  lemur,  Lemur 
varius.  B,  Fossil  adapid,  Notharctus  osborni.  c,  Tarsius,  Tarsius 
spectrum,   D,  Platyrrhine  monkey,  Cebus.   E.  Catarrhine  monkey, 
Macaca.  (After  Le  Gros  Clark.) 

food.  Omnivorous  or  frugivorous  diets  are  common,  and  the  molars 
have  become  quadritubercular  (Fig.  383),  the  upper  adding  a  hypo- 
cone  and  the  lower  losing  the  paraconid  of  the  original  pattern,  leaving 
the  metaconid  and  protoconid,  while  the  hypoconid  and  entoconid 
become  raised  to  make  a  posterior  pair,  sometimes  with  addition  of 
a  fifth  cusp,  the  hypoconulid,  posteriorly.  The  cusps  are  usually  not 
of  the  sharp  insectivorous  type,  but  are  low  (bunodont)  cones  and 
extra  ones  may  be  added,  or  the  cusps  joined  to  make  ridges.  These 
changes  are  associated  with  the  adoption  by  many  primates  of  a  diet 
of  fruit  or  leaves,  requiring  treatment  by  biting  and  grinding. 

The  method  of  reproduction  is  one  of  the  most  characteristic  of 
primate  features.  The  uterus  retains  signs  of  its  double  nature  in  the 
earlier  types  but  later  becomes  a  single  chamber.  The  number  of 


xxm.  3  CLASSIFICATION    OF    PRIMATES  607 

young  produced  is  small,  as  in  other  animals  with  large  brains  that 
learn  well.  There  is  often  only  a  single  pair  of  teats  and  in  association 
with  the  arboreal  habit  these  are  pectoral.  The  arrangements  for 
placentation  involve  elaborate  changes  in  the  uterine  mucosa  in 
preparation  for  reception  of  the  embryo,  followed  by  breakdown  at 
regular  intervals  (menstruation).  This  special  nature  of  the  uterine 
mucosa  makes  possible  the  efficient  haemochorial  form  of  placenta- 
tion. Besides  these  arrangements  for  nutrition  of  the  young  the  pri- 
mates also  extend  parental  care  for  a  long  time  after  birth. 

In  many  features  of  their  life,  therefore,  the  primates  show  to  a  high 
degree  the  adjustability  and  power  to  obtain  sustenance  from  varying 
environments  that  is  characteristic  of  all  life.  The  receptors,  brain,  and 
hand  provide  means  for  doing  this  in  more  elaborate  ways  than  are 
used  by  any  other  animals.  The  monkeys  and  apes  have  exploited 
these  powers  to  a  considerable  extent  and  are  successful  animals, 
living,  as  we  might  say,  by  their  wits,  in  a  wide  variety  of  circumstances. 
However,  non-human  primates  are  unable  to  adjust  to  conditions 
outside  the  tropical  and  subtropical  regions.  Man  has  made  still  better 
use  of  his  talents  and  by  creating  his  own  environment  manages  to 
support  a  population  of  nearly  3,000  million  large  individuals, 
scattered  all  over  the  globe. 

3.  Divisions  of  the  primates 

Fortunately  many  of  the  changes  of  habit  characteristic  of  primates 
involved  changes  in  the  skull  and  these  can  be  followed  in  the  fossils. 
Our  knowledge  of  the  evolutionary  development  of  primate  life, 
though  far  from  complete,  is  less  so  than  might  be  expected  from  the 
rarity  of  preservation  of  arboreal  skeletons.  During  the  50  million 
years  since  the  Eocene  the  various  primate  stocks  have,  of  course, 
divided  and  subdivided  many  times,  and  invaded  many  special  habitats. 
The  forms  at  present  known,  living  and  as  fossils,  are  placed  by  Simp- 
son in  150  genera,  two-thirds  of  them  extinct,  70  of  these  being  pro- 
simians.  Most  of  primate  evolution  has  occurred  in  the  Old  World; 
there  are  no  fossil  primates  known  from  North  America  between  the 
Oligocene  and  modern  times.  Only  ten  fossil  primates  throughout  the 
whole  Tertiary  are  even  moderately  well  known,  probably  because 
animals  living  in  trees  are  seldom  preserved  as  fossils. 

Bitter  controversy  still  rages  around  the  question  of  the  best  means 
of  classification  of  Primates.  Earlier  zoologists  tended  to  postulate 
a  series  of  stages  successively  closer  to  man,  the  latest  product  of 
evolution.  There  has  been  increasing  awareness  of  the  unwisdom  of 


608  THE   PRIMATES  xxm.  3- 

this  procedure.  Recognition  that  many  of  the  surviving  stocks  have 
been  separate  for  a  long  time  has  led  systematists  to  emphasize  the 
distinctions  between  the  groups  more  sharply.  Thus  lemurs,  far  from 
being  regarded,  as  they  were  formerly,  as  rather  primitive  monkeys, 
are  now  often  placed  in  a  distinct  order,  having  in  common  with  other 
primates  only  'the  retention  of  certain  primitive  characters  and  an 
adaption  to  arboreal  life'  (Wood  Jones).  There  is  no  general  agreement 


Fig.  384.  Ring-tailed  lemur,  Lemur. 
(From  life.) 

about  the  best  means  of  classification;  the  more  traditional  schemes, 
such  as  that  adopted  here,  probably  give  an  over-simplified  idea  of  a 
progression  of  forms.  A  classification  on  more  'natural'  or  phyletic 
lines  could  be  devised,  but  would  necessitate  the  postulation  of  a  large 
number  of  distinct  categories,  unless  these  were  simplified  by  admitting 
speculations  about  the  affinities  of  the  lines. 

We  shall,  as  usual,  in  the  main  follow  Simpson.  His  arrangement 
retains  the  order  Primates  and  recognizes  two  great  suborders, 
Prosimii  and  Anthropoidea.  The  division  is  'horizontal'  rather  than 
'vertical';  the  two  groups  are  not  separate  and  divergent  lines,  they 
contain  respectively  the  ancestral  and  the  'developed'  forms.  Two 
primate  stocks  are  indeed  known  to  have  existed  in  the  Palaeocene 
and  these  are  both  included  in  the  prosimians,  whereas  no  anthro- 
poids are  known  before  the  Oligocene.  The  Prosimii  includes  three 
sorts  of  primate,  all  'primitive'  in  the  sense  of  retaining  insectivoran 
characters,  such  as  long  face,  lateral  eyes,  and  small  brain;  they  are 
grouped  here  as  three  infraorders:  Lemuriformes  for  the  lemurs  of 


xxiii.  4  LEMURS  609 

Madagascar  and  their  fossil  allies;  Lorisiformes  for  the  rather  similar 
animals  outside  Madagascar;  and  Tarsiiformes  for  the  living  tarsier 
and  its  Eocene  relatives.  The  suborder  Anthropoidea  includes  two 
distinct  types,  first  the  New  World  monkeys,  superfamily  Ceboidea, 
secondly  the  Old  World  monkeys,  apes  and  man,  grouped  together  as 
Cercopithecoidea. 


Fig.  385.  Skeleton  of  ring-tailed  lemur. 

We  propose,  therefore,  to  arrange  our  examination  of  primates 
around  the  idea  of  three  main  stocks  diverging  in  the  Palaeocene, 
namely  lemurs,  lorises,  and  tarsiers,  with  an  anthropoid  stock  arising 
from  one  of  these,  probably  the  tarsioid,  in  the  Eocene,  and  itself 
early  becoming  separated  into  two  lines,  the  New  World  monkeys 
on  the  one  hand,  and  Old  W'orld  monkeys  and  apes  on  the  other 
(Fig.  416). 

4.  Lemurs  and  lorises 

The  lemurs  (Fig.  384)  living  in  Madagascar  today  resemble  certain 
fossils,  known  as  plesiadapids  and  adapids,  that  existed  in  various  parts 
of  the  world  in  Palaeocene  and  Eocene  times.  We  may,  therefore,  per- 
haps assume  that  they  show  us  the  characters  of  part  at  least  of  the 
primate  stock  more  than  50  million  years  ago.  Lemurs  show  their 
'primitive'  nature  in  their  habits  and  appearance,  as  well  as  in  the  de- 
tails of  their  structure.  They  are  mostly  nocturnal,  arboreal,  insecti- 
vorous, omnivorous,  or  fruit-eating  animals;  the  name  means, 'ghost', 
but  it  is  more  interesting  that  they  are  often  said  to  be  rather  like 


6io 


THE   PRIMATES 


xxm.  4 


squirrels  in  behaviour.  The  brain  (Fig.  386)  has  relatively  small 
cerebral  hemispheres,  not  overlapping  the  cerebellum,  but  with  olfac- 
tory regions  large  for  a  primate,  though  smaller  than  in  insectivores  or 
other  primitive  mammals.  The  nose  has  numerous  well-developed 
turbinal  bones  (Fig.  394).  The  cerebral  sulci  tend  to  run  longitudinally, 


37  79         18 

Homo 


Cercopithecus 


Fig.  386.  Brains  of  hedgehog  and  various  primates  to  show  the  relative  development  of 
various  parts.  The  numbers  refer  to  the  areas  recognized  by  Brodmann  on  a  basis  of  their 
structure.  4  and  6  are  the  precentral  motor  areas,  8-12  the  frontal  and  prefrontal  areas, 
lacking  in  the  earliest  forms.  1-3  are  the  end  station  of  skin  sensations,  and  5  and  7  are  also 
concerned  with  these.  17  is  the  visual  end  station,  and  18  and  19  are  also  concerned  with 
this  sense.  22  is  the  auditory  end  station,  bol,  bulbus  olfactorius;  tol,  tuberculum  olfac- 

torium.  (From  Brodmann.) 

rather  than  transversely  as  in  anthropoids.  The  whole  behaviour  is  not 
like  that  of  a  monkey;  the  animals  move  from  branch  to  branch  by 
sudden  leaps,  balancing  with  the  long,  bushy  tail,  which  is  not  pre- 
hensile. Social  habits  are  little  developed. 

The  snout  is  long,  with  a  cleft  and  moist  upper  lip,  the  eyes  are 
directed  sideways,  and  the  retina  contains  only  rods  except  in  the 
genus  Lemur,  which  is  diurnal  and  possesses  cones.  There  is  no  fovea 
and  no  binocular  vision.  The  external  ears  may  be  large,  as  in  other 
nocturnal  animals.  In  the  skull  (Fig.  387)  there  is  a  post-orbital  bar, 
but  the  temporal  fossa  opens  widely  to  the  orbit.  The  tympanic  region 
shows  several  peculiar  features.  The  tympanic  bone  forms  a  ring,  lying 


xxiii.  4 


PRIMATE  SKULLS 


611 


Tarsi  us 


Lemur 


Notharctus 

Fig.  387.  Skulls  of  early  primates.  (After  Gregory  and  Flower  and  Lydekker, 
Mammals,  Living  and  Extinct,  A.  &  C.  Black,  Ltd.) 


Fig.  388.  Tympanic  ring  and  tympanic  bulla. 

A,   Primitive   mammalian   condition,   floor  of  cavity  unossified.    B,    Lcmuriformes,   ring 

enclosed  within  bulla.  C,  Lorisiformes  and  platyrrhines,  ring  part  of  bulla.  D,  Tarsius  and 

catarrhines,  bony  meatus.  (After  Le  Gros  Clark,  Early  Forerunners  of  Man.) 

within  a  petrosal  bulla,  but  not  fused  with  it  (Fig.  388),  a  condition 
like  that  in  Tupaia,  but  not  found  in  higher  primates.  The  pollex  and 
hallux  are  used  for  grasping;  most  of  the  digits  have  nails,  but  the 
second  digit  of  the  foot  has  a  toilet  claw.  The  fourth  digit  is  usually  the 
longest,  whereas  in  anthropoids  the  whole  symmetry  of  the  hand  and 
foot  is  arranged  about  a  long  third  digit.  The  teeth  show  the  typical 

2.1.'}.'? 
primate  number  ,  but  the  upper  incisors  are  very  small  and  the 

2.1.3.3 
lower  incisors  and  canines  are  procumbent,  that  is  to  say  directed 

forwards  and  are  used  for  combing  the  fur.  The  first  lower  premolar 


6 1 


THE   PRIMATES 


xxiii.  4- 

is  caniniform.  The  molars  are  triangular  in  some  genera,  in  others  a 
hypocone  gives  them  a  square  shape.  The  lower  molars  are  of  typical 
tuberculosectorial  type,  with  a  heel.  The  reproduction  shows  several 
primitive  features.  There  are  marked  breeding-seasons  and  the  females 
are  polyoestrous.  The  uterus  is  bicornuate  and  the  placenta  of  a 


Fig.  389.  Aye-Aye,  Daubentonia. 
(From  a  photograph.) 


Fig.  390.  Slender  loris,  Loris. 
(From  life.) 


Fig.  391.  Bush-baby,  Galago, 
(From  photograph.) 


remarkably  simple  type,  epithelio-chorial  and  diffuse,  with  villi  all 
over  the  surface  of  the  chorion,  which  is  vascularized  directly  by  a 
large  allantois,  filled  with  fluid.  The  amnion  arises  as  folds  and  not  by 
cavitation  as  in  higher  primates. 

Ten  genera  of  lemurs  occur  today  in  Madagascar,  where  they  have 
evidently  flourished  in  isolation  throughout  the  Tertiary.  Indri,  the 
largest,  is  an  animal  nearly  3  ft  long,  able  both  to  jump  and  to  walk  on 
its  hind  legs.  Earlier  lemurs  became  larger  still,  the  skull  of  the 
Pleistocene  *Megaladapis  was  nearly  a  foot  long.  Daubentonia 
(=  Cheiromys),  the  aye-aye  (Fig.  389)  of  Madagascar,  is  like  the 
lemurs  in  many  ways  but  has  large,  continually  growing  upper  and 
lower  incisors,  like  a  rodent.  It  has  a  very  long  and  thin  third  finger, 
which  it  uses,  with  its  teeth,  to  find  insects  deep  in  the  bark.  It  also 
eats  the  inside  of  bamboo  and  sugar-canes  among  which  it  lives. 


xxm.  5  FOSSIL   PROSIMIANS  613 

The  Lorisformes  (Fig.  390)  include  the  slow  lorises  and  other  lemur- 
like animals  that  are  found  outside  Madagascar.  They  are  known  as 
fossils  back  to  the  Miocene.  The  slow  lorises  (Nycticebus  and  Loris)  of 
India  and  Ceylon  are  arboreal  and  nocturnal,  proceeding  by  remark- 
ably slow  and  deliberate  movements  and  often  hanging  upside  down. 
They  eat  fruit  or  small  animals.  Lorises  also  show  some  features  that 
recall  the  higher  primates,  for  instance  the  tympanic  ring  is  fused  to 
the  petrosal  bulla.  In  some  of  them  the  face  is  shorter  and  the  brain- 
case  rounder  than  in  true  lemurs.  It  is  therefore  possible  that  they 

A 

(x4) 


(x3) 


Fig.  392.  Dentition  of  Plesiadapis  anceps.  A.  Right  upper  teeth  showing 
P3P4  and  3  molars.  B.  Lower  dentition.    (After  G.  G.  Simpson.) 

are  survivors  of  an  earlier  stock,  closer  to  our  own  than  are  the  lemurs, 
and  some  of  the  features,  such  as  procumbent  incisors,  may  be 
developed  independently  in  the  two  groups.  However,  traces  of  very 
early  features  remain,  including  a  transverse  skin  fold  on  the  abdomen 
of  the  female,  which  is  considered  by  some  to  represent  a  marsupium. 
On  the  African  mainland  there  are  also  two  successful  genera  of  this 
type,  Galago,  the  bush  baby  (Fig.  391),  and  Perodkticus,  the  potto. 
The  former  are  jumping  animals  and  can  leave  the  trees;  their 
elongated  tarsus  somewhat  recalls  that  of  Tarsius. 

5.  Fossil  Prosimians 

The  earliest  primates  of  the  Palaeocene  and  Eocene  were  insecti- 
vorous and  fruit-eating  animals.  They  may  be  distributed  among  five 
families,  whose  relationships  are  difficult  to  decide.  The  *Plesiadapidae, 
from  the  Paleocene  and  Eocene  of  both  Old  and  New  Worlds,  had 
large  upper  and  lower  incisors  and  have  been  considered  as  related 
both  to  tree-shrews  and  to  the  aye-aye  (Fig.  392).  They  are  probably 
too  specialized  to  be  directly  ancestral  to  either  the  lemurs  or  higher 


614 


THE   PRIMATES 


xxiii.  5- 


primates,  but  may  be  close  to  both.  *Plesiadapis  is  the  only  primate 
genus  except  Homo  that  occurs  in  both  Old  and  New  Worlds. 

The  Adapidae  were  also  Palaeocene  and  Eocene  animals,  like  lemurs 
in  many  ways  but  without  procumbent  incisors.  The  Old  World 
members  of  the  family  (* Adapts)  could  have  given  rise  to  both  the 

lemurs  and  lorises.  The  adapids 
were  large  creatures  with  heads 
a  foot  or  more  long.  The  brain 
case  was  small  (*Notharctus, 
Fig.  387)  but  carried  temporal 
crests.  There  was  a  very  full 

dentition  (*'').  The  incisors 
2.1.4.3 

were  not  procumbent  but  the 
canines  were  incisiform.  The 
tympanic  ring  was  included  in 
the  bulla.  These  animals  there- 
fore showed  many  features 
common  to  other  early  mam- 
mals but  with  distinctly  lemur- 
oid  tendencies. 

6.  Tarsiers 

The  third  group  of  the 
Prosimii,  the  Tarsiiformes,  in- 
cludes one  living  form,  Tarsius, 
and  a  number  of  early  Tertiary 
fossils,  placed  in  a  separate 
family  *Anaptomorphidae. 
The  whole  group  could  be  described  by  saying  that  its  members 
show  many  characteristics  similar  to  those  of  Insectivora  and  lemurs, 
but  also  others  suggestive  of  the  anthropoid  primates.  Yet  there  are 
present  specializations  that  rule  out  the  possibility  that  these  animals 
are  in  the  direct  line  of  descent  of  the  higher  forms,  and  we  must 
therefore  regard  them  as  an  early  offshoot,  showing  us  something  of 
the  characteristics  that  were  possessed  by  the  anthropoid  stock  in 
Palaeocene  or  early  Eocene  times. 

Tarsius  itself  (Fig.  393)  is  an  arboreal,  nocturnal,  insectivorous 
creature,  the  size  of  a  small  rat,  living  in  the  East  Indian  islands.  The 

2.1  ."2. T 

dental  formula  is  — '^-^  ;  the  molars  retain  a  very  simple  tritubercular 
i-T-3-3 


Fig.  393.  Spectral  tarsier,  Tarsius. 
(From  life.) 


xxiii.  6 


TARS1ERS 


615 


pattern  and  the  incisors  and  canines  do  not  show  the  specializations 
found  in  lemurs  (Fig.  383).  The  head  is  more  like  that  of  a  monkey 
than  of  a  lemur;  it  is  set  on  a  mobile  neck,  indeed  the  animal  has  the 
uncanny  power  of  turning  its  head  through  1800  so  that  it  faces  back- 
wards, while  the  eyes,  like  those  of  owls,  are  so  large  that  they  are 
little  movable.  The  foramen  magnum  opens  downwards.  The  eyes 
face  more  nearly  forwards  than  in  lemurs,  the  snout  is  shortened,  and 
the  turbinals  of  the  nose  reduced.  The  nose  thus  resembles  that  of  a 


mt.(cut) 

Lemur  mt     I  LL 

Fig.  394.  The  nasal  passages  of  various  mammals. 
cp.  choanal  passage;  mt.  maxillo-turbinal;  nt.  naso-turbinal;  I-IV,  endo-turbinals. 
(From  Cave,  B.M.A.  Ann.  Proc.  1948.) 

monkey  (Fig.  394),  and  there  is  neither  a  cleft  in  the  upper  lip  nor  a 
moist  rhinarium,  such  as  is  present  in  most  mammals  and  in  lemurs, 
but  absent  in  anthropoids.  This  reduction  of  the  snout  as  a  tactile 
organ  perhaps  goes  with  the  development  of  the  hand  for  that  purpose. 
The  eyes  are  enormous,  relatively  larger  than  in  any  other  Primate, 
but  suited  for  night  vision,  with  the  retina  containing  only  rods, 
though,  nevertheless,  possessing  a  yellow  macula  and  a  small  fovea. 
The  external  ears  are  large  and  mobile  and  the  sense  of  hearing  is  keen. 
The  orbit  is  partly  divided  off  from  the  temporal  fossa  (Fig.  387).  The 
tympanic  bone  is  not  only  fused  to  the  very  large  petrosal  bulla  but 
also  somewhat  drawn  out  into  a  spout,  as  in  anthropoids  (Fig.  388). 
The  brain  is  small  and  shows  a  curious  mixture  of  early  mammalian 
and  advanced  primate  characters.  The  olfactory  regions  are  small  and 
the  cerebral  hemispheres  large,  though  smooth.  The  visual  (occipital) 


6i6 


THE   PRIMATES 


xxiii.  6- 


ca. 


Fig.  395.  Bones  of  hind  leg  and  foot  of  various  primates  (not  to  the 

same  scale). 

a.  astragalus  (talus);  c.  cuboid;  ca.  calcaneum;  cun.  medial  cuneiform;/,  femur; 

fi.   fibula;  gt.   greater  trochanter;   h.   head;   m.   first  metatarsal;   n.   navicular; 

p.  proximal  phalanx;  pa.  patella;  t.  tibia. 

cortex  shows  remarkably  well-differentiated  layers.  The  corpus  cal- 
losum  is  small  and  the  anterior  commissure  large.  The  cerebellum  is 
small  and  simple.  The  posterior  corpora  quadragemina  are  large. 

Tarsiers  are  said  to  live  in  pairs  with  no  social  organization.  The 
reproduction  shows  much  similarity  to  that  of  Anthropoidea.  There 
is  a  menstrual  cycle.  The  uterus  is  double,  as  in  lemurs,  but  the 


xxiii.  7  FOSSIL  TARSIOIDS  617 

placenta  is  of  discoidal  shape  and  haemochorial  organization,  with  a 
much  reduced  allantois,  almost  like  that  of  apes  and  men.  The  amnion 
is  formed  by  folding. 

Some  of  these  characters  indicate  a  type  of  organization  so  similar 
to  that  of  anthropoids  that  the  resemblance  can  hardly  be  entirely  due 
to  convergence.  Many  of  the  monkey-like  features  of  the  head  could, 
however,  be  due  to  the  large  size  of  the  eyes.  Moreover,  the  reduction 
of  the  turbinals  has  taken  place  differently  in  Tarsius  and  anthropoids. 

In  its  legs  (Fig.  395)  Tarsius  shows  considerable  specialization  for  its 
jumping  method  of  progression,  the  fibula  being  fused  with  the  tibia 
and  the  calcaneum  and  astragalus  elongated  so  as  to  provide  an  extra 
leg  segment  while  retaining  the  grasping  foot.  Both  first  digits  can  be 
used  for  grasping  and  the  digits  bear  adhesive  pads;  all  have  nails 
except  the  second  and  third  in  the  hind-limb,  which  carry  claws  used 
for  cleaning  the  fur.  As  in  other  jumping  animals  the  ilium  is  very 
long.  There  is  also  a  long  tail. 

The  *Anaptomorphidae  are  fossil  tarsioids  found  from  Palaeocene 

to  Oligocene  in  Europe  and  America.  At  least  20  genera  are  known, 

mostly  from  skulls  and  teeth;  where  limb  bones  are  found  they  already 

have  the  tarsioid  specializations.  In  most  the  eyes  were  large  and  the 

face  short.  The  brain  was  like  that  of  Tarsius  but  with  olfactory  regions 

better  developed.  The  teeth  of  some  (*PsendoIoris)  were  remarkably 

3.1.3.3 
like  those  of  Tarsius  but  of  very  generalized  pattern  (v )  and 

tribosphenic  (Fig.  383).  Other  lines  were  specialized,  for  instance  by 
reduction  of  the  lower  incisors  and  procumbency  of  the  canines 
{*Necrolemur).  Some  of  these  animals  may  have  been  close  to  the 
primate  ancestry,  but  it  must  be  recognized  that  the  tarsioids  show 
more  similarity  to  the  Anthropoidea  than  to  the  lemurs.  We  are 
ignorant  of  tarsioid  history  from  the  Oligocene  to  recent  times,  but 
it  seems  likely  that  they  have  remained  an  isolated  stock,  their  rela- 
tionship to  higher  primates  being  one  of  common  ancestry  in  early 
Tertiary  times,  when  all  these  primates  were  so  alike  that  it  is  best  to 
class  them  together  as  Prosimii,  some  of  which  went  on  to  develop  into 
anthropoids  (Fig.  416). 

7.  Characteristics  of  Anthropoidea 

The  monkeys,  apes,  and  men  form  a  natural  group,  almost  certainly 
of  common  descent  from  some  Eocene  population.  They  first  appear 
as  fossils  in  the  Oligocene  and  have  flourished  greatly  since;  Simpson 
lists  66  genera  in  the  suborder,  of  which  only  30  are  extinct;  evidently 


618  THE   PRIMATES  xxm.  7 

the  type  has  been  successful  and  is  expanding.  The  outstanding 
characteristic  of  the  anthropoids  might  be  said  to  be  their  liveliness 
and  exploratory  activity,  coming  perhaps  originally  from  life  in  the 
tree-tops,  necessitating  continual  use  of  eye,  brain,  and  limbs.  With 
this  is  associated  the  development  of  an  elaborate  social  life,  based  not, 
as  in  most  mammals,  on  smell,  but  on  sight.  Monkeys  show  more 
bright  colours  than  do  other  mammals,  especially  the  curious  reds  and 
blues  worn  on  the  head  and  rear.  The  species  may  become  subdivided 
into  distinct  races  showing  great  differences  of  coat  colour  (Fig.  400). 
Communication  between  individuals  is  ensured  by  elaborate  systems 
of  vocal  signals  and  the  platysma  muscle  becomes  differentiated  into 
a  set  of  facial  muscles  used  to  signal  'emotions'. 

Many  of  the  characters  of  the  group  are  those  of  Tarsius,  listed 
already,  but  the  Anthropoidea  are  mostly  diurnal  and  microsmatic, 
with  a  short  snout,  large  forwardly-directed  eyes,  many  cones,  a  well- 
marked  central  area  in  the  retina  and  partial  decussation  in  the  optic 
tract,  features  that  are  associated  with  binocular  vision  and  large  powers 
of  visual  form  discrimination.  The  external  ears,  no  longer  serving  as 
tactile  organs  or  for  direction-finding,  are  small  and  the  edge  is  usually 
rolled  over.  The  orbit  is  closed  off  behind.  The  tympanic  bone  is 
fused  to  the  petrosal  and  in  later  forms  drawn  out  to  a  spout.  The 
tactile  sense  is  greatly  developed  on  the  fingers  and  toes,  which  carry 
characteristic  ridges.  The  brain  (Fig.  386)  is  relatively  much  larger 
than  in  lemurs  or  Tarsius  and  its  cerebral  hemispheres  are  especially 
well  developed,  overhanging  the  cerebellum  and  medulla.  The  olfac- 
tory parts  of  the  brain  are  reduced  and  the  pyriform  lobe  becomes 
displaced  on  to  the  medial  surface  by  the  extension  of  the  neopallium. 
The  surface  of  the  neopallium  is  highly  fissured,  showing  a  charac- 
teristic form  of  Sylvian  fissure,  and  a  well-marked  central  sulcus, 
separating  the  motor  and  sensory  areas.  A  parieto-occipital  sulcus 
separates  these  lobes  and  a  large  lunate  sulcus  marks  the  visual  area, 
especially  in  monkeys  (simian  fissure).  The  neocortex  thus  shows  four 
distinct  lobes,  frontal,  parietal,  occipital,  and  temporal.  The  occipital 
(visual)  and  frontal  regions  are  especially  large. 

The  head  is  rounded  to  fit  the  brain,  with  the  foramen  magnum 
below,  so  that  the  head  is  carried  up  on  a  mobile  neck.  The  gait  of 
monkeys  is  typically  quadrupedal  and  plantigrade  when  on  the  ground, 
with  the  fore-limbs  somewhat  longer  than  the  hind.  In  the  trees 
some  may  be  described  as  low  canopy  runners  (e.g.  guenons)  others 
are  high  canopy  acrobatic  types  (spider  monkeys).  Only  the  great 
apes   habitually   swing   along   with   the   arms    (brachiation).    Some 


xxnr.  7 


TEETH    OF   PRIMATES 


619 


A  B 

CEBUS  MACACA 

Fig.  396.  Tooth  rows  of  New  World  and  Old  World  monkeys.  (After 
Le  Gros  Clark.) 

Tarsius.    Amphipibhecus.  Parapibhecus.  Proconsul.  Cercopibhecus 
Pa<^  meb.  ^^  spr. 


FlG.  397.  Diagram  of  the  right  lower  molar  cusp  pattern  in  some  Primates,  to  show  the 
presumed  evolutionary  stages  in  the  development  of  the  cusp  pattern.  Tarsius  shows  the 
primitive  (tribosphenic)  type.  The  paraconid  is  involved  in  the  formation  of  the  trigonid. 
*Amphipithecus  shows  the  paraconid  undergoing  reduction  while  the  talonid  and  trigonid 
portions  of  the  crown  are  at  the  same  level.  *Parapithecus:  the  paraconid  has  completely 
disappeared,  the  talonid  bears  the  hypoconid,  the  entoconid,  and  a  relatively  well- 
developed  hypoconulid;  the  trigonid  portion  bears  the  metaconid  and  protoconid. 
*Proconsul:  the  five  cusps  are  more  or  less  equally  developed  and  separated  by  a  charac- 
teristic pattern  of  intervening  grooves.  Cercopithecus  shows  the  characteristic  bilophodont 
pattern,  with  transverse  ridges. 

ent.   entoconid;   hid.   hypoconulid;   hy.   hypoconid;   met.   metaconid;  pa.   paraconid;  pr. 
protoconid.  (After  Le  Gros  Clark.) 

monkeys  have  become  terrestrial  (baboons).  The  pollex  and  hallux  are 
opposable  and  the  digits  all  carry  nails.  The  hands  and  feet  are  used 
for  feeding  as  well  as  for  locomotion. 

The  characteristic  of  the  tooth  row  is  a  tendency  to  shortening, 
presumably  connected  with  the  shortening  of  the  face.  There  are  three 
premolars  in  the  earlier  Anthropoidea,  later  reduced  to  two  (Fig.  383). 
In  the  line  leading  to  man  there  is  a  tendency  to  still  further  reduction, 
with  the  last  molar  becoming  smaller  than  the  others.  The  cusp- 
pattern  is  tritubercular  in  earlier  anthropoids,  but  later  the  molars 
become  square  and  have  four  or  more  bunodont  cusps  in  higher 


620 


THE   PRIMATES 


xxiii.  7- 


anthropoids  (Fig.  383).  The  incisors  become  spatulate,  rather  than 
pointed,  and  the  premolars  bicuspid  (Figs.  396,  397). 

The  reproduction  is  characterized  by  the  presence  of  menstrual 
cycles,  continuing  throughout  the  year.  Ovulation  occurs  once  in  each 
cycle,  often  accompanied  by  the  development  of  sexual  signals  and 
behaviour  patterns  by  the  female.  There  is  a  discoidal,  haemochorial 
placenta,  with  very  early  development  of  the  extra-embryonic  meso- 
derm and  reduction  of  the  yolk-sac,  amniotic  folds,  and  allantois. 
Usually  a  single  offspring  is  produced  and  there  is  one  pair  of  pectoral 
mammae.  The  young  are  looked  after  for  a  long  period.  The  social 
life  is  often  based  upon  families  of  one  male  and  several  females  and 
young. 


Fig.  398.  Spider  monkey,  Ateles.  (From  life.) 

8.  New  World  monkeys,  Ceboidea 

The  continent  of  South  America  houses  a  special  type  of  monkeys, 

as  of  so  many  other  mammalian  groups.  These  platyrrhine  (flat-nosed) 

monkeys  have  presumably  been  isolated  since  Eocene  times.  They 

could  not  have  been  a  later  immigration  from  North  America  because, 

so  far  as  we  know,  no  cercopithecoids  or  hominoids  reached  that 

continent  until  man  came.  The  differences  from  the  Old  World 

monkeys    are   not   very   profound,    however;    therefore   either   the 

characteristic  monkey  organization  had  appeared  in  the  Eocene  or  the 

platyrrhines  and  catarrhines  have  evolved  on  parallel  lines. 

2.1.3.3  .    . 

In  the  teeth  the  second  premolar  is  retained  ( ),  whereas  it  is 

2.1.3.3 

lost  in  all  Old  World  forms;  the  molars  are  quadritubercular  (Figs. 

383  and  396).  The  brain  is  relatively  larger  in  marmosets  even  than 

in  man,  but  this  results  from  the  small  size  of  the  animal.  The  smaller 

species  show  little  Assuring,  but  this  develops  in  the  larger  ones  (Ateles), 

showing  a  pattern  similar  to  that  of  Old  World  monkeys.  The  nasal 


xxiii.  8  NEW   WORLD    MONKEYS  621 

apparatus,  though  smaller  than  in  lemurs,  is  larger  than  in  Old  World 
monkeys,  producing  the  wide  separation  of  the  nostrils,  from  which 
the  name  platyrrhine  derives.  Facial  vibrissae  are  present,  but  usually 
small.  In  the  ear  the  tympanic  bone  is  a  ring,  fused  with  the  petrosal, 
but  is  not  drawn  out  into  a  tube  as  it  is  in  catarrhines,  and  there  is  a 
large  bulla,  which  is  absent  in  the  latter.  The  coecum  is  relatively  large. 
The  reproductive  system  does  not  show  the  full  'anthropoid'  pattern; 
for  instance,  there  are  at  most  only  slight  signs  of  menstrual  bleeding 
at  the  end  of  the  luteal  phase  of  the  oestrus  cycle.  Social  life  is  well 


Fig.  399.  Common  marmoset,  Callithrix.  (From  life.) 

developed  but  the  sexual  signalling  system  is  probably  less  complicated 
than  in  catarrhines.  Thus  the  colour  is  seldom  brilliant,  and  the  facial 
musculature  around  the  mouth  relatively  simple.  The  loud  voice  of 
the  howler  monkeys  (Alouatta),  which  have  special  laryngeal  sacs,  is 
used  in  the  assertion  of  territorial  rights  by  the  clan.  This,  unlike  the 
families  of  most  monkeys,  includes  several  mature  males  as  well  as 
females  and  young.  Cooperation  is  ensured  by  a  language  of  at  least 
nine  distinct  sounds  with  separate  'meanings'.  Spider  monkeys 
(Ateles,  Fig.  398)  have  a  somewhat  similar  organization. 

These  New  World  monkeys  are  very  well  adapted  for  arboreal  life, 
with  long  limbs,  delicate  hands,  and  tail  for  balancing  or  seizing.  The 
tail  pad  has  special  tactile  sensitivity,  with  ridges  like  those  on  the 
digits  and  a  large  representation  in  the  cerebral  cortex.  The  animals 
swing  along  freely  among  the  branches  and  may  make  jumps  in  which 
they  advance  by  as  much  as  15  ft  while  falling  50  ft. 

The  fourteen  living  genera  of  New  World  monkeys  are  divided  into 
two   families,    the   marmosets,    Callithrix  (=  Hapale),   being   more 


622  THE   PRIMATES  xxm.  8 

primitive  than  the  remainder  (Cebidae).  The  marmosets  (Fig.  399)  are 
very  small  insect-  and  fruit-eating  animals,  of  somewhat  squirrel-like 
appearance  and  habits,  living  in  tropical  South  America.  They  have 
a  thick  non-prehensile  tail  and  there  are  claws  on  all  the  digits  except 
the  first,  allowing  the  animals  to  run  up  trunks  they  cannot  grasp. 
These  are  probably  true  claws  and  not  secondarily  modified  nails.  The 
pollex  is  not  opposable.  Three  premolars  are  present,  but  the  molars 
are  reduced  to  two,  a  condition  found  in  no  other  anthropoid.  The 
cusp-pattern  is  tritubercular.  Unlike  other  anthropoids  the  marmosets 
give  birth  to  two  or  three  young  and  there  are  signs  of  ancient  condi- 
tions in  the  placenta,  where  the  yolk-sac  becomes  larger  than  in  most 
primates. 

Unfortunately,  little  is  known  of  the  evolutionary  history  of  the  New 
World  monkeys ;  fossils  are  known  only  back  to  the  Miocene  of  South 
America  (*Homunculus).  In  view  of  the  isolation  and  compactness  of 
the  group  we  may  feel  reasonably  confident  that  it  has  evolved  in- 
dependently since  its  origin  from  Eocene  tarsioids. 


XXIV 

MONKEYS,  APES,  AND  MEN 

1.  Common  origin  of  Old  World  monkeys,  apes,  and  men 

The  seventeen  living  genera  of  Old  World  monkeys,  apes,  and  men 
are  sometimes  classified  together  as  Catarrhina  because  of  the  common 
characteristics  in  which  they  contrast  with  the  New  World  monkeys. 
Perhaps  this  union  is  justified  and  the  Catarrhina  is  a  monophyletic 
group,  with  a  common  ancestor  in  the  late  Eocene.  However,  these 
creatures  are  obviously  much  more  diverse  than  the  New  World 
monkeys  and  have  entered  a  wide  variety  of  habitats.  The  Old  World 
monkeys  proper,  the  super-family  Cercopithecoidea,  diverged  very 
early  from  the  apes  and  men  (Hominoidea).  Some  distinguish  between 
the  monkey  and  ape-human  branches  of  the  stock,  by  calling  the 
former  cynomorphs,  the  latter  anthropomorphs  or  hominoids.  Others 
regard  all  three  groups  as  widely  separate.  However,  the  earliest 
definite  catarrhine  known,  *Parapithecus  of  the  Oligocene,  is  close 
to  the  origin  of  all  three  groups,  so  we  may  reasonably  keep  them 
together. 

2.  Old  World  monkeys,  Cercopithecoidea 

The   cercopithecid   or   Old  World   monkeys   do   not   differ  very 

strikingly  in  general  habits  and  organization  from  the  monkeys  of  the 

New  World,  though  they  are  mostly  larger.  We  must  conclude  either 

that  the  two  groups  have  made  many  changes  in  parallel  or  that  in  the 

Eocene  there  were  already  animals  with  the  good  senses,  active  brains, 

and  skilled  movements  of  the  monkeys.  The  distinguishing  features  of 

the  Old  World  types  are  rather  trivial,  for  instance  they  sit  upon 

ischial  callosities,  surrounded  by  naked  and  often  highly  coloured  skin, 

which  becomes  enlarged  in  the  female  before  ovulation.  There  are 

often  cheek  pouches  in  which  to  store  food,  usually  complicated 

laryngeal  sacs,  a  bony  tympanic  tube,  and  never  a  prehensile  tail.  The 

great  reduction  of  the  olfactory  turbinals  leaves  the  nostrils  close 

2.1.2.3 
together  and  pointing  downwards.  The  dentition  is  reduced  to  -      — , 

the  upper  molars  carry  four  cusps,  and  the  lower  four  except  for  the 
last,  which  has  five  (Figs.  383  and  396).  The  diet  of  the  more  gener- 
alized cercopithecids  is  omnivorous,  including  insects,  lizards,  eggs, 


624 


MONKEYS 


XXIV.  2 


and  fruit,  but  many  monkeys  are  specialized  fruit-eaters,  and  the 
molar  teeth  are  quadrangular,  with  the  four  cusps  united  to  make  two 
transverse  ridges  used  for  grinding,  somewhat  as  in  ungulates.  These 
specialized  molars  make  it  unlikely  that  the  modern  cercopithecids 
could  have  been  ancestral  to  the  apes  or  man.  The  colon  usually  has 
a  sigmoid  flexure  and  a  small  caecum  and  appendix.  The  reproduction 
is  similar  to  that  of  apes  and  man;  there  is  menstrual  bleeding  and 
haemochorial  placenta.  The  ano-genital  region  (sexual  skin)  of  the 
female  may  show  marked  signals  (swelling  and  coloration)  at  the  time 


A  BCD 

Fig.  400.  Coloration  types  of  various  sub-species  of  Colobus  polykomos.  a.  C.p. 
vellerosus  Graff,  b.  C.p.  caudatus  Thomas,  c.  C.p.  abyssinicus  Oken.  D.  C.p. 
angolensis  Sclater.  (After  P.  Rodt.) 

of  ovulation.  The  male  shows  continuous  spermatogenesis,  without  a 
breeding  season.  In  some  species  there  are,  however,  seasonal  fluctua- 
tions in  the  number  of  births. 

The  cerebral  cortex  is  always  large  and  fissured  and  its  frontal 
regions  well  developed.  Behaviour  is  exploratory  and  manipulative 
and  learning  powers  high.  Social  behaviour  is  elaborate  and  often 
based  upon  polygamous  families.  The  coat  colour  is  often  ornate  (Fig. 
400)  and  there  are  elaborate  communication  systems  by  the  facial 
musculature  and  vocal  apparatus. 

The  Cercopithecoidea  include  a  number  of  variant  types,  many 
common  and  well  known.  Macaca,  the  rhesus  monkey  (Fig.  401), 
has  many  species  in  Asia  and  North  Africa,  one  reaching  Gibraltar. 
Cercopithecus,  the  guenons,  are  similar  animals  in  Africa,  many  highly 
coloured.  The  baboons,  Papio  (Fig.  402),  of  Africa  and  related  forms 
in  Arabia,  and  mandrills,  Mandrillus  (Fig.  403)  of  West  Africa  have 
become  secondarily  terrestrial  and  quadrupedal  and  the  face  has 
become  elongated  ('dog-face'),  allowing  for  a  long  tooth-row  of  grind- 
ing molars.  The  Colobinae  are  fully  arboreal,  leaf-eating  monkeys, 
without  cheek  pouches  but  with  the  stomach  sacculated ;  the  guerezas 


XXIV.  2 


OLD    WORLD    MONKEYS 


625 


(Colobus)  live  in  tropical  Africa 
and  the  langurs  or  leaf  monkeys 
{Presbytis  =  Semnopiihecus)  in 
south  Asia. 

The  monkey  type  thus  shows 
us  something  of  the  condition  of 
catarrhines  in  Oligocene  and  Mio- 
cene times.  A  fragment  of  a  lower 
jaw  from  the  Lower  Oligocene  of 
Egypt,  *Apidium,  may  have  been  a 


Fig.  401.  Rhesus  monkey,  Macaca. 
(From  life.) 


Fig.  402.  Sacred  baboon,  Papio.  (From  life.) 


Fig.  403.  Mandrill,  Mandrillus.  (From  life.) 

very  early  catarrhine,  if  it  belongs  to  a  primate  at  all.  The  molars  carry 
a  quadrangle  of  four  cusps  and  a  hypoconulid  behind.  *Parapithecus 
from  the  same  deposits  is  known  from  a  single  mandible  (Figs.  397 
and  409)  and  was  an  animal  the  size  of  a  squirrel,  which  might  have 
been  derived  from  the  anaptomorphids  and  led  on  to  the  catarrhines. 
The  two  rami  diverge  posteriorly,  as  in  tarsioids,  rather  than  running 
parallel.  However,  the  number  of  teeth  is  reduced  to  that  of  catarrhines 


626  APES  xxiv.  2-3 

and  the  canines  are  incisiform.  The  molars  carry  five  cusps,  not  united 
by  ridges.  The  cercopithecid  type  was  well  established  by  the  Miocene 
and  abundant  remains  are  available  of  *Mesopithecus,  with  the  molar 
cusps  united  to  ridges. 

3.  The  great  apes  :  Pongidae 

The  question  of  the  exact  degree  of  affinity  between  the  existing 
apes  and  man  remains  unsettled.  There  were  plenty  of  fossil  apes  in 


Fig.  404.  Gibbon,  Hylobates.  (From  life.) 

Miocene  times  and  man-like  creatures  are  found  in  the  early  Pleisto- 
cene, but  we  have  no  undoubted  evidence  of  human  remains  from  the 
Pliocene  and  it  is  therefore  impossible  to  say  whether  the  human  stock 
was  derived  from  apes  after  Miocene  times  or  whether  it  separated 
much  earlier,  either  from  the  ancestral  catarrhine  stock,  say,  in  the 
Oligocene,  or,  as  a  few  believe,  even  earlier  still,  from  some  Tarsius- 
like  prosimian.  Evidence  of  definitely  man-like  creatures  that  can  be 
placed  with  certainty  in  a  family  Hominidae  is  found  only  back  to 
about  1  million  years  ago,  whereas  the  longest  of  the  above  estimates 
would  say  that  our  stock  has  been  distinct  and  evolving  separately  for 
nearly  60  million  years,  without  leaving  any  remains.  Although  the 
view  that  men  have  descended  from  apes  is  probably  the  more  widely 
held,  we  shall  first  survey  the  structure  of  the  great  apes  by  treating 
them  as  members  of  a  separate  family  Pongidae. 

The  living  apes  include  the  gibbon,  Hylobates  (Fig.  404),  and  orang- 
utan, Pongo  =  Simia  (Fig.  405),  from  east  Asia  and  the  chimpanzee, 
Pan  (Fig.  406),  and  Gorilla  (Fig.  407)  from  Africa.  They  and  related 
fossil  forms  are  marked  off  from  the  cercopithecids  by  their  teeth  and 
methods  of  locomotion.  Many  apes  are  rather  large  animals  and  this 
has  made  it  impossible  for  them  to  walk  along  the  branches  as  monkeys 
do.  They  therefore  swing  by  the  arms,  which  are  longer  than  the  legs 


(627) 


Fig.  405.  Orang-utan,  Pongo. 
(From  life.) 


Fig.  406.  Chimpanzee,  Pan. 
(From  life.) 


Fig.  407.  Gorilla,  Gorilla.  (From  life.) 


(628) 


Fig.  408.  Skeletons  of  gibbon  and  man. 

a.  astragalus  (talus);  car.  carpus;  cl    clavicle;  ca.  calcaneum;  co.  coracoid;  fi.  fibula; 

h.  femur;  hu.  humerus;  il.  ilium;  is.  ischium;  mc.  metacarpals;  pu.  pubis;  pa.  patella; 

r.  radius;  sc.  scapula;  St.  sternum;  t.  tibia;  u.  ulna. 


xxiv.  3  BRACHIATORS  629 

and  are  provided  with  very  powerful  muscles,  the  hands  and  feet  being 
efficient  grasping  organs.  There  is  no  tail.  These  brachiating  habits 
have  affected  the  entire  skeleton.  All  the  apes  and  men  differ  from  the 
cercopithecids  in  having  wider  chests,  longer  necks,  longer  limbs,  and 
larger  heads  (Fig.  408).  The  cervical  and  sacral  regions  are  longer  in 


Fig.  409.  Mandibles  of  A,  *Parapithecus;  B,  *Propliopithecus;   C,  *Pliopithecns, 
D,  Hylobates.  Dental  arches  of  E,  Gorilla;  F,  *Dryopithecus;  G,  *Plesianthropus; 

H,  Homo. 

(A-D  after  Le  Gros  Clark,  B.M.  Guide,  and  Gregory;  E-H  after  Howells, 

Mankind  So  Far,  Doubleday  and  Company,  Inc.) 

apes  than  in  the  monkeys  and  the  lumbar  region  shorter.  When  pro- 
ceeding on  the  ground  the  apes  cannot  balance  on  two  legs  for  long; 
instead,  the  long  forearms  prop  up  the  front  of  the  body  and  produce 
a  semi-erect  position.  The  hands  are  specialized  for  brachiating,  with 
a  short  thumb  and  long  metacarpals  and  digits  (Figs.  410  and  411). 
The  foot  is  in  general  similar  but  in  the  chimpanzee  and  gorilla  it  is 
more  suited  for  walking,  with  broader  sole  and  shorter  toes.  In  the 
terrestrial  Gorilla  gorilla  beringei  the  hallux  lies  parallel  to  the  other 
toes  almost  as  in  man. 

The  teeth  (Fig.  409)  are  of  a  rather  generalized  type.  The  canines 
are  often  large,  especially  in  males,  and  the  lower  front  premolar  forms 


630  APES  xxiv.  3 

a  sectorial  blade.  The  molars  carry  grinding  tubercles  and  often  show 
a  crenation  of  the  enamel,  which  is  characteristic  of  apes,  though  found 
as  an  abnormality  in  monkeys  and  man.  The  trigon  is  still  present  in 
the  upper  molar,  the  hypocone  being  small.  The  lower  molars  have  a 
hypoconulid,  making  five  cusps,  as  contrasted  with  the  four  of  monkeys. 
All  the  apes  are  mainly  vegetarians,  but  they  may  eat  meat  occasion- 
ally. The  use  of  the  teeth  for  grinding  is  associated  with  powerful 
masticatory  muscles  and  the  development  of  temporal  and  occipital 
crests.  The  supraorbital  ridges  are  also  large.  The  canines  are  used  for 
attack  and  defence.  In  the  digestive  system  apes  and  man  differ  from 
other  primates  in  the  presence  of  a  vermiform  appendix. 

The  brain  is  much  larger  than  in  cercopithecids,  and  shows  a 
pattern  of  convolutions  similar  to  that  of  man,  though  more  simple. 
The  behaviour  provides  many  signs  of  efficient  memory,  leading  to 
the  attitudes  that  we  characterize  as  imitation  and  association  of  ideas. 
There  are  extensive  powers  of  manipulation  and  for  obtaining  ends  by 
indirect  means. 

The  communication  system  is  highly  developed.  The  young  chim- 
panzee is  said  to  be  able  to  make  at  least  thirty-two  distinct  sounds. 
The  facial  musculature  is  more  highly  differentiated  than  in  monkeys 
and  produces  a  wide  range  of  expressions  such  as  of  rage,  surprise, 
pleasure,  and  laughter. 

Social  organization  is  always  well  developed.  The  gibbons  are  mono- 
gamous, the  family  consisting  of  a  pair  and  the  young  of  current  and 
previous  years.  Chimpanzees,  and  so  far  as  is  known  gorillas,  live  in 
bands,  led  by  a  dominant  male.  The  individuals  of  a  band  cooperate 
in  helping  each  other  and  the  groups  show  differing  social  traditions. 
The  apes  are  diurnal  animals,  eating  in  the  day.  They  make  platforms 
on  which  they  rest  at  night  (except  the  gibbons). 

Reproduction  is  based  on  a  menstrual  cycle  of  thirty-five  days  in 
chimpanzees,  with  a  great  development  of  the  sexual  skin  at  mid-cycle. 
Gestation  is  long,  as  is  the  growth  period,  seven  to  nine  years  in  the 
gibbon,  ten  to  twelve  in  the  chimpanzee.  The  life  span  is  also  long, 
reaching  forty  years  in  chimpanzees,  perhaps  fifty  in  gorillas. 

The  gibbons  are  fully  arboreal,  swinging  rapidly  with  their  ex- 
tremely long  arms  (Fig.  404).  This  extreme  brachiation  may  be  a  quite 
recent  specialization.  They  eat  mainly  fruit  and  leaves,  also  insects  or 
eggs.  Gibbons  are  numerous  throughout  south  Asia  and  the  type  is 
certainly  the  most  successful  among  modern  great  apes.  The  charac- 
teristic cries  are  part  of  the  defence  of  the  territory  that  is  occupied  by 
each  group.  The  orang-utan  of  Borneo  and  Sumatra  is  larger  and  also 


xxiv.  3  PRIMATE  HANDS  AND  FEET  631 

has  very  long  arms.  The  chimpanzees  {Pan)  and  gorillas  (Gorilla), 
living  in  the  forests  of  tropical  Africa,  are  so  alike  that  it  is  doubtful 


Fores t 
Gonlla 


Mountain 
Gorilla 


Fig.  410.  Manus  and  pes  of  a  series  of  Primates. 
Ml.  manus;  p.  pes.  (After  Le  Gros  Clark,  Morton  &  Fuller.) 

if  the  generic  separation  is  justified.  The  chimpanzee  is  the  smaller 
and  less  muscular  animal,  lacking,  for  example,  the  large  parietal  and 
occipital  crests  found  in  the  male  gorilla.  There  is  a  corresponding 
difference  of  temperament,  the  chimpanzee  being  lively  and  sometimes 
tameable,  the  gorilla  gloomy,  ferocious,  and  unafraid.  Gorillas  are 


632  APES  xxiv.  3- 

mainly  terrestrial,  walking  on  all  fours  and  sleeping  either  on  the 
ground  (males)  or  at  a  small  height  (females  and  young).  Like  the 
other  apes  they  show  much  local  variation  but  all  may  be  referred  to 
a  single  species,  G.  gorilla.  G.  gorilla  beringei  is  a  mountain  form  that  is 
more  fully  terrestrial  than  the  others  (Fig.  410). 

The  similarities  and  differences  between  these  animals  and  man 
will  be  discussed  later.  Their  relationship  with  the  other  catarrhines  is 
clearer.  The  lower  jaw  of  *Parapitheais  of  the  Egyptian  lower  Oligo- 
cene  contained  teeth  of  a  pattern  that  could  have  given  rise  to  those  of 
the  Pongidae  as  well  as  the  Cercopithecidae  (Fig.  397).  In  the  same 
beds  was  found  another  jaw,  which  is  definitely  that  of  an  ape, 
*Propliopithecus.  Here  the  molars  have  a  distinctly  five-cusped  pattern, 
with  protoconid  and  metaconid  in  front  and  a  large  heel,  carrying  a 
hypoconid  laterally  and  entoconid  medially,  and  also  a  posterior 
hypoconulid.  Some  such  animal  could  have  given  rise  to  *Limnopi- 
thecus  of  the  Miocene  and  *Pliopithecus  of  the  Pliocene,  animals 
similar  to  the  gibbons  and  living  in  the  woods  of  Europe  and  Africa. 
Great  apes  were  found  quite  widely  in  the  Old  World  during  the 
Miocene  and  Pliocene.  The  earliest  of  these,  *Proconsul  from  the 
lower  Miocene  of  Kenya,  showed  a  combination  of  characters  of 
cercopithecids,  great  apes,  and  man.  The  skull  was  more  lightly  built 
than  in  apes,  with  no  brow  ridges.  The  tooth  rows  converged  anteriorly 
as  in  *Parapithecns.  The  incisors  were  small  and  like  those  of  man  but 
the  canines  were  large  and  the  first  lower  premolar  was  sectorial  as  in 
apes.  The  limb  bones  suggest  that  the  gait  was  terrestrial  and  quad- 
rupedal, and  that  the  brachiating  habit  had  not  yet  evolved. 

*Dryopithecus  from  the  middle  and  upper  Miocene  of  Africa, 
Europe,  and  India  was  closer  to  the  apes,  with  U-shaped  dental 
arcades.  On  the  other  hand,  *Ramapithecus  from  the  Miocene  and 
Pliocene  of  India  showed  human  characteristics  in  the  rounded  upper 
arcade  of  the  teeth,  small  canines,  and  other  features. 

Several  other  types  are  known  and  evidently  the  apes  were  wide- 
spread, varied,  and  successful  animals  in  the  Miocene  and  there  are 
among  them  plenty  of  signs  of  the  characteristics  both  of  the  modern 
apes  and  men.  The  remains  of  *Oreopithecus  from  the  Pliocene  of 
Italy  show  a  curious  mixture  of  characters.  It  was  not  a  brachiator, 
but  its  method  of  locomotion  is  not  clear.  The  lower  molars  have  four 
cusps  arranged  in  pairs  as  in  monkeys  but  not  united  by  ridges.  The 
upper  molars  resemble  those  of  apes  but  the  small  canines,  absence 
of  diastema,  and  bicuspid  first  lower  premolar  have  led  some  to  place 
it  close  to  man. 


xxiv.  5  (633) 

4.  The  ancestry  of  man 

In  order  to  discover  the  position  of  man  in  relationship  to  the  living 
and  fossil  ape  populations  we  may  try  to  specify  the  characters  distinc- 
tive of  the  family  Hominidae  and  then  discuss  whether  they  could  have 
been  derived  from  those  of  monkeys  or  apes.  Schultz,  who  has  made 
careful  measurement  of  many  features  of  primates,  lists  the  following 
as  the  chief  specializations  of  man:  (i)  elaboration  of  the  brain  and 
behaviour,  including  communication  by  facial  gestures  and  speech; 
(2)  the  erect  posture;  (3)  prolongation  of  post-natal  development;  and 
(4)  the  great  rise  in  population  in  recent  years.  Others  might  make  up 
the  list  differently,  but  we  may  use  it  as  a  basis  for  discussion  of  the 
differences  between  men  and  other  creatures. 

5.  Brain  of  apes  and  man 

The  brain  is  much  larger  absolutely  and  relatively  in  man  than  any 
living  ape;  Fig.  382  shows  that  man  stands  farther  apart  from  the  apes 
in  this  respect  than  they  do  from  other  anthropoids.  The  cranial 
capacity  for  males  of  modern  (Caucasian)  man  may  be  taken  as  1,500 
c.c,  whereas  that  of  chimpanzees  is  given  as  410,  gorillas  as  510,  and 
orangs  as  450.  The  general  arrangement  of  function  within  the  brains 
is  similar  in  man  and  apes,  but  the  parts  especially  well  developed  in 
man  are  the  frontal  and  occipital  lobes.  The  latter  are  concerned  with 
the  sense  of  sight  and  are  related  to  our  intensely  visual  life.  The 
frontal  lobes,  so  far  as  is  known,  serve  to  maintain  the  balance  between 
caution  or  restraint  and  sustained  active  pursuit  of  distant  ends,  which, 
above  all  else,  ensures  human  survival  in  such  a  variety  of  situations, 
and  makes  possible  the  social  life  by  which  so  great  a  population  is 
maintained.  The  difference  of  behaviour  between  men  and  apes 
exceeds  all  the  structural  differences;  our  lives  are  so  widely  different 
from  theirs  that  any  attempt  to  specify  the  divergences  in  detail  is  apt 
to  seem  ridiculous.  Perhaps  the  more  striking  of  them  are  related  to 
the  powers  of  communication  by  speech  which,  besides  its  obvious 
social  advantage,  gives  to  man  the  power  of  abstract  thought.  Whatever 
we  may  think  about  the  consciousness  of  animals  there  is  no  doubt 
that  our  own  awareness  of  life,  being  expressed  in  words,  is  widely 
different  from  that  of  all  other  creatures.  The  speech  system  depends 
upon  a  complex  of  features  of  the  brain,  larynx,  tongue,  mouth, 
and  auditory  apparatus.  In  addition,  the  facial  musculature  is  more 
fully  differentiated  even  than  in  apes,  especially  around  the  eves  and 
mouth. 


634  MAN  xxiv.  6- 

6.  The  posture  and  gait  of  man 

The  gait  of  man  differs  from  that  of  any  ape  in  that  the  body  can  be 
fully  and  continuously  balanced  on  the  two  legs.  This  involves  con- 
siderable modifications  throughout  the  skeleton  and  musculature  (Fig. 
408).  The  backbone,  instead  of  the  single  thoracic  curve  of  quadrupeds, 
has  an  S  shape,  being  convex  forward  in  the  lumbar,  backward  in  the 
thoracic,  and  again  forward  in  the  cervical  region.  The  thoracic  curve 
develops  before  birth,  but  the  cervical  only  as  the  baby  holds  its  head 
up  and  the  lumbar  as  it  begins  to  walk.  The  vertebral  column,  which 
in  quadrupeds  is  a  horizontal  girder,  in  man  becomes  vertical,  carrying 
bending  and  compression  stresses  along  its  length.  This  entirely  alters 
the  arrangement  of  its  secondary  struts  and  ties.  The  bodies  of  the 
vertebrae  carry  much  of  the  weight  and  are  massive,  tapering  in  size 
upwards.  They  are  separated  by  well-developed  intervertebral  disks, 
acting  as  elastic  cushions.  The  weight  of  the  head  is  balanced  on  the 
backbone  through  the  neck,  and  the  thorax  acts  as  a  bracket  from  which 
the  viscera  are  suspended.  The  muscles  of  the  back,  the  ties  of  the 
vertebral  girder,  though  arranged  on  the  same  general  morphological 
plan  as  in  quadrupeds,  now  carry  very  different  stresses  and  no  long 
neural  spines  or  large  transverse  processes  develop,  since  the  girder  is 
not  now  of  cantilever  type.  For  the  same  reason  there  is  no  sharp 
change  in  the  direction  of  the  neural  spines  at  the  hind  end  of  the 
thoracic  region;  the  girder  is  now  one  unit,  with  bending  stressing 
along  its  whole  length. 

The  balancing  of  the  body  on  the  legs  also  involves  many  changes. 
The  muscles  around  the  hip  joint  achieve  this  balance,  and  the  changes 
to  allow  this  affect  especially  the  gluteal  muscles  and  the  ilium  and 
sacrum  to  which  they  are  attached,  these  being  the  extensor  and 
abductor  muscles,  which  raise  the  body  from  the  quadrupedal  position 
and  prevent  it  falling  medially  when  the  weight  is  on  one  leg.  The 
buttocks  are  therefore  a  characteristic  human  structure.  The  adoption 
of  a  bipedal  position  imposes  entirely  new  requirements  on  the 
musculature  of  the  limbs.  In  quadrupedal  progression  the  retractor 
muscles  are  the  main  means  of  locomotion,  drawing  the  leg  backward 
at  the  hips  while  straightening  the  knee.  In  man  the  propulsive  thrust 
is  obtained  mainly  from  the  calf  muscles  and  in  particular  from  the 
soleus,  which  runs  from  the  tibia  to  the  heel,  the  gastrocnemius,  since 
it  tends  also  to  bend  the  knee,  being  reduced.  The  quadriceps  femoris 
becomes  very  large,  serving  to  keep  the  knee  extended  both  while  the 
calf  muscles  develop  their  thrust  and,  as  a  check  to  the  forward 
momentum,  when  the  foot  touches  the  ground. 


xxiv.  7  LIMBS  635 

The  ilium  is  very  broad  in  man,  increasing  the  surfaces  for  attach- 
ment of  the  glutei,  iliacus  (a  flexor  of  the  hip),  and  for  the  abdominal 
muscles,  which  are  attached  along  its  crest  and  have  an  important  part 
to  play  in  carrying  the  weight  of  the  viscera. 

7.  The  limbs  of  man 

Many  changes  would  be  needed  to  convert  an  ape-like  leg  and  foot 
to  the  human  condition  (Fig.  395).  The  femur  of  man  is  straight  and 
the  articular  surface  at  its  lower  end  set  at  an  angle  to  the  shaft.  This 
allows  the  lower  legs  and  feet  to  be  as  nearly  as  possible  below  the 
centre  of  gravity  in  standing,  in  other  words,  for  the  knees  to  be  held 
together  although  the  femoral  heads  are  wide  apart.  At  the  ankle  joint, 
on  the  other  hand,  the  articular  surface  is  at  right  angles  to  the  tibia  in 
man,  at  an  oblique  angle  in  apes,  since  in  the  latter  the  foot  is  turned 
outwards.  In  ourselves  the  weight  is  transferred  from  the  tibia  to  the 
talus  and  then  partly  backwards  to  the  calcaneum  and  partly  forwards 
through  the  tarsus  to  the  metatarsal  heads  (Fig.  412).  The  calcaneum  is 
modified  for  this  weight-bearing  and  the  tarsus  and  digits  even  more 
so,  the  whole  foot  being  converted  into  an  arched  system,  no  trace  of 
which  is  found  in  apes.  With  this  arrangement  the  hallux  is  not  used 
for  grasping  and  is  very  large.  It  is  held  in  line  with  the  other  digits  and 
the  whole  forms  a  compact  wedge  with  a  joint  at  the  metatarsal  heads. 
In  walking,  when  the  foot  is  raised  by  the  calf  muscles,  the  toes  remain 
on  the  ground,  to  prevent  slipping  forwards.  The  condition  in  which 
the  first  toe  is  the  longest  is  peculiar  to  man,  but  in  some  monkeys  and 
apes  the  axis  tends  to  shift  from  the  third  digit  medially  and  the 
human  condition  is  an  accentuation  of  this  change,  with  the  metatarsal 
and  first  phalanx  of  the  first  digit  becoming  long  and  strong.  Even  in 
modern  human  populations  the  second  toe  as  a  whole  is  often  longer 
than  the  first;  this  condition  was  perhaps  commoner  in  historical 
antiquity  (the  'Grecian  toe'),  and  may  be  a  cause  of  foot  trouble,  the 
long  second  digit  being  unsuited  to  the  stresses  it  is  made  to  bear. 

The  differences  between  apes  and  men  in  the  arms  and  hands  (Fig. 
410)  are  marked,  though  perhaps  less  striking  than  in  the  feet.  The 
human  fore-limb  is,  of  course,  relatively  much  shorter  than  that  of  any 
ape  and  its  muscles  far  less  powerful.  In  order  to  carry  the  whole 
weight  of  the  large  body  an  ape  needs  enormous  muscles  all  along  the 
limb.  Thus  the  serratus  anterior,  which  pulls  the  body  up  on  the 
scapula,  is  very  large  and  the  ribs  to  which  it  is  attached  have  large 
flattened  surfaces,  are  very  long,  and  extend  far  caudally;  the  chest  of 
man  is  much  more  lightly  built.  Similarly,  the  muscles  of  the  shoulder 


636  MAN  xxiv.  7- 

and  the  flexor  muscles  of  the  elbow,  wrist,  and  hand  are  all  much 
larger  in  apes,  as  are  the  ridges  to  which  they  are  attached,  for  instance 
on  the  palmar  surfaces  of  the  phalanges  (Fig.  411).  The  human 
arm  has  specialized  in  mobility.  The  hand  can  be  brought  into  almost 
any  position  in  relation  to  the  body  by  virtue  of  the  wide  range  of 


Homo  Cap-  Gorilla 

Fig.  411.  Bones  of  the  left  hands  of  man  and  gorilla,  palmar  view. 

cap.  capitate;  h.  hamate;  /.  lunate;  mc.  metacarpal;  />.  pisiform;  sc.  scaphoid;  t.  trapezium; 
tr.  triquetral;  tz.  trapezoid. 

Notice  the  large  bony  points  of  attachment  of  the  flexor  muscles  of  the  gorilla  on  the  trapez- 
ium, scaphoid,  hamate,  and  proximal  phalanges. 

movement  at  the  shoulder,  pronation  and  supination  of  the  forearm 
and  movements  at  the  wrist. 

In  the  hand  itself  the  thumb  is  characteristically  long  in  man  and 
moved  by  powerful  muscles.  Man  is  the  only  animal  in  which  the 
thumb  can  be  in  the  fullest  sense  opposed  to  the  other  digits,  so  that 
the  pads  face  each  other.  This  is  achieved  by  special  development 
of  the  joint  between  the  first  carpal  and  metacarpal.  The  third  digit 
is  the  longest  in  apes,  as  in  men,  but  the  second  digit  (index)  of  man  is 
generally  at  least  as  long  as  the  fourth,  often  longer  (the  'Napoleonic 


xxiv.  8  SKULL   AND   JAWS  637 

finger').  In  lower  primates  the  digits  of  the  ulnar  side  are  relatively 
much  longer.  Apart  from  proportions  and  skeletal  features  the  human 
hand  also  has  a  very  well  developed  sensory  supply,  which  is  essential 
for  its  use  as  a  handling  organ. 


Notharctus 

Fig.  412.  Foot  skeleton  of  a  series  of  Primates. 
(After  W.  K.  Gregory.) 

8.  The  skull  and  jaws  of  man 

Comparisons  between  the  skulls  of  apes  and  men  have  attracted 
special  attention  because  so  many  of  the  finds  of  early  human  types 
have  been  of  skulls  (Fig.  413).  The  differences  are  mainly  referable  to 
changes  in  the  brain,  dentition,  and  method  of  balancing  the  head  upon 


638 


MAN 


xxiv.  8 


the  neck.  The  enlargement  of  the  brain  has  been  in  the  occipital  and 
especially  in  the  frontal  region  (p.  633),  giving  a  high  forehead  and  the 
characteristic  upright  face.  At  the  same  time  the  jaws  have  receded,  so 
that  the  human  tooth-row  is  unusually  short.  Moreover,  the  dental 


Pithecanthropus 


H.  sapiens 


Fig.  413.  Skulls  of  apes  and  man.  The  face  and  back  of  jaw  of 

* 'Pithecanthropus   has   been   restored.    (Partly  after  Romer, 

Vertebrate  Paleontology,  University  of  Chicago  Press.) 

arcade  is  characteristically  rounded  in  front,  that  of  apes  is  U-shaped, 
with  large  canines  at  the  bend  (Fig.  409).  In  man  the  canines  are  small 
and  incisiform;  the  first  lower  premolar  is  bicuspid,  like  the  rest  and 
not  sectorial  as  in  other  catarrhines.  The  molars  show  a  characteristic 
pattern  that  may  be  regarded  as  based  on  four  cusps  above  and  five 
below.  The  cusps  are  arranged  roughly  as  a  rectangle,  so  that  the 
grooves  between  them  make  a  +  as  compared  with  the  Y  patterns 
typical  of  the  dryopithecine  molar  (Fig.  414).  Thus  the  protoconid 
meets  the  entoconid  in  the  human  but  not  in  the  earlier  type.  However, 


xxiv.  8  TEETH   AND   JAWS  639 

there  is  great  variation  in  these  patterns,  both  in  man  and  apes.  Little 
can  be  said  therefore  about  a  single  tooth,  but  the  proportion  of 
molars  with  four  cusps  and  a 
-f-  pattern  is  higher  in  man  than  in 
apes  (Fig.  415).  The  last  molar  (wis- 
dom tooth)  is  smaller  than  the  others 
in  man,  but  not  in  modern  apes. 
There  are,  however,  many  signs  of 
possible  ape-like  ancestry  in  our 
teeth;  for  instance  the  canine  has 
a  long  root  and  erupts  late. 

The  lower  jaw  of  man  is  less 
shortened  than  the  upper;  whereas 
in  apes  it  is  strengthened  by  a 
'simian  shelf  of  bone  on  its  inner 
side,  in  man  this  strengthening  is  on 
the  outside,  making  the  chin.  The 
jaw  is  less  massive  in  man  than  in 
apes,  especially  its  posterior  ramus; 


Fig.  414.  Mandibular  molar  patterns 
in  the  Liberian  chimpanzee  and  human 
dentition.  The  chief  distinguishing 
feature  between  Y  and  +  patterns  is  the 
relationship  of  cusps  2  and  3  to  each 
other.  In  the  Y  pattern  they  are  in 
contact,  in  the  +  pattern  they  are 
separated  by  cusps  1  and  4. 

B,  buccal;  D,  distal;  L,  lingual;  M,  mesial; 
1  protoconid;  2,  metaconid;  3,  hypoconid; 
4,  entoconid;  5,  hypoconulid.  (After  Schu- 
man  and  Brace.) 


Chimp. 


Pecos 


Europ. 
white 


others 


Fig.   415.    Proportions   of  the   various   mandibular   molar  patterns   found   in 
Chimpanzees,    Pecos    Indians,    and    European    Whites.    (After   Schuman    and 

Brace.) 

the  muscles  for  moving  it  are  less  powerful.  Correlated  with  this  weaken- 
ing of  the  jaw  has  been  a  rounding  of  the  surface  of  the  skull.  Occipital 
and  temporal  crests  for  the  attachment  of  the  neck  and  jaw  muscles  are 
well  developed  in  the  male  gorilla,  suggested  in  other  apes,  but  absent  in 
man.  The  brow  ridges,  also  characteristic  of  the  apes,  are  large  masses 


640  MAN  xxiv.  8- 

of  bone  above  the  eyes,  probably  produced  to  meet  the  compression 
stresses  set  up  by  the  powerful  action  of  the  jaw-muscles.  Their 
absence,  together  with  the  large  forehead,  produces  the  human  type 
of  face.  The  large  external  nose  is  presumably  another  corollary  of 
the  shortened  face;  it  provides  some  extension  of  the  nasal  cavity, 
necessary  for  warming  and  filtering  the  air. 

The  balancing  of  the  head  on  the  neck  is  a  result  of  the  adoption  of 
the  upright  position.  Movement  of  the  foramen  magnum  to  a  position 
beneath  the  skull  has  been  noted  as  a  primate  characteristic  and  it 
reaches  its  extreme  in  man,  allowing  considerable  reduction  of  the 
musculature  at  the  back  of  the  neck;  the  splenius  and  semispinalis 
capitis  muscles  are  much  smaller  in  man  than  in  apes.  The  small  size 
of  the  trapezius  is  partly  a  consequence  of  the  good  balance  of  the 
head,  partly  of  the  absence  of  brachiating  habits.  Reduction  of  these 
muscles  leads  to  simplification  of  the  bones  at  both  ends  of  them.  The 
area  of  their  attachment  to  the  occipital  surface  of  the  skull  becomes 
much  reduced  and  remains  smooth,  instead  of  being  roughened  and 
even  raised  into  ridges  as  in  apes.  At  the  same  time  the  spines  of  the 
cervical  vertebrae,  very  long  in  the  gorilla,  are  short  and  almost 
vestigial  in  man.  When  the  head  is  properly  balanced  on  the  backbone 
it  can  be  freely  turned  around,  and  for  this  purpose  the  sternomastoid 
muscles  are  well  developed  and  the  large  mastoid  ('breast-like') 
swellings  where  they  are  attached  to  the  base  of  the  skull  provide  a 
characteristic  human  feature. 

9.  Rate  of  development  of  man 

One  of  the  most  striking  differences  between  man  and  apes  is  the 
slow  rate  of  our  own  growth  and  development;  there  is  a  strong 
suspicion  that  many  of  our  features  are  due  to  retardation  of  the  time 
of  onset  of  maturity.  Schultz  has  shown  that  in  the  apes  growth  ceases 
between  the  ages  of  10  and  12  and  that  the  epiphyses  finally  close 
between  12  and  14.  Many  of  the  features  of  man,  such  as  the  reduction 
of  hair  and  the  large  head,  presence  of  a  prepuce  on  the  penis  and 
hymen  in  the  vagina,  are  those  to  be  found  in  foetal  apes,  and  it  is 
therefore  suggested  that  one  of  the  main  changes  leading  to  our 
development  has  been  delay  in  the  rate  of  differentiation  and  onset  of 
maturity.  This  might  well  depend  on  the  endocrine  balance,  perhaps 
particularly  on  the  action  of  the  anterior  lobe  of  the  pituitary.  It  is 
only  possible  to  guess  at  the  process  of  habit  change  and  selection  by 
which  the  appropriate  genetic  change  has  occurred.  It  may  well  be 
that  those  family  organizations  were  more  efficient  in  which  individuals 


xxiv.   ii.  GROWTH    OF   POPULATIONS  641 

developed  late  and  were  therefore  better  behaved,  in  early  years 
because  of  immaturity,  and  later  by  the  great  development  of  the 
'inhibitory'  or  balancing  functions  made  possible  by  growth  of  the 
frontal  lobes  (p.  633).  Families  composed  of  such  slow-developing  and 
restrained  individuals  would  therefore  survive  and  the  genetic  factors 
involving  delay  of  maturity  be  selected. 

10.  Growth  of  human  populations 

This  increase  of  the  post-natal  developmental  period  may  well  be 
connected  with  the  appearance  of  the  fourth  outstanding  feature  of 
man  noted  by  Schultz  (p.  633),  the  great  population  increase  in 
recent  times.  No  exact  figures  are  available,  but  it  is  probable  that  a 
first  increase  occurred  when  the  Neolithic  agricultural  civilization 
developed,  perhaps  10,000  years  ago.  This  development  presumably 
depended  on  factors  making  for  orderly  and  restrained  behaviour, 
such  as  we  have  been  discussing;  it  is  no  accident  that  family  customs 
are  closely  linked  with  those  of  tribes  and  nations  in  all  stages  of 
society.  A  further  great  increase  of  human  population,  probably  at 
least  a  doubling,  has  occurred  during  the  past  200  years,  and  we  may 
associate  this  with  the  further  extension  of  habits  of  thought  and 
restraint  in  the  conduct  of  affairs,  making  possible  the  development 
of  logic  and  science  and  their  application  to  human  productivity. 

1 1 .  Time  of  development  of  the  Hominidae 

Thus  there  are  seen  to  be  profound  differences  between  man  and 
the  existing  apes,  and  it  must  be  remembered  that  we  have  considered 
mainly  skeletal  features  and  hardly  touched  on  the  details  of  the  inner 
life  of  the  animals,  or  their  powers  of  communication  or  social  organi- 
zation. The  most  significant  difference  between  man  and  all  other 
animals  is  in  the  size  of  the  brain  (Fig.  382)  and  the  difference  of  life 
and  behaviour  that  goes  with  this.  In  studying  the  documents  of  our 
history,  however,  we  can  discover  only  little  of  the  brains  and  less  of 
the  behaviour  of  our  ancestors;  we  must  rely  mainly  on  study  of  the 
skeleton. 

No  undoubted  human  remains  are  found  before  the  beginning  of 
the  Pleistocene,  less  than  1-5  million  years  ago.  They  are  not  common 
until  500,000  years  later,  but  their  total  absence  from  the  Pliocene, 
Miocene,  and  Oligocene  epochs  must  certainly  be  considered  sus- 
picious. During  those  periods  we  have  admittedly  only  few  remains  of 
apes,  but  they  do  occur  and  men  do  not;  there  is  therefore  a  prima 
facie  case  for  considering  that  men  have  evolved  from  the  same 


(642) 


OWOH 
SndOaH±NV33Hlld 

sn33HiidO"ivai.snv 


vmiaoo 

NVd 


S31V901AH 


V3ai3  3Hi/cyo^N\ 


&r 


--ivfr*0 


wisoyd  | 


XXIV.   11-12 


AUSTRALOPITHECINAE 


643 


Miocene  stock  as  the  apes.  Some  hold,  however,  that  the  human  line 
has  been  distinct  for  a  much  longer  period,  perhaps  even  back  to  a 
separate  tarsioid  ancestor  in  the  Eocene. 

A  survey  of  the  evidence  about  the  affinities  of  man  and  apes  will 
probably  lead  the  unprejudiced  to  the  conclusion  that  although  we  do 
not  know  enough  to  be  certain,  the  human  stock  probably  diverged 
from  that  of  the  apes  in  early  Miocene  times,  perhaps  from  a  form  like 
*Proco?isul,  before  the  brachiating  habit  had  become  fully  developed. 
Fig.  416  shows  the  possible  relationship  based  on  this  hypothesis,  but 


Fig.  417.  Skull  of  Paranthropus.  (From  a  cast.) 

we  shall  remain  uncertain  of  the  exact  course  of  our  descent  until 
Pliocene  and  Miocene  fossils  that  could  have  been  our  ancestors  are 
found. 


12.  The  Australopithecinae 

A  series  of  fossils  found  in  Africa  shows  a  curious  combination  of 
the  characters  of  men  and  apes.  The  specimens  occur  in  lime  deposits 
probably  of  early  Pleistocene  date.  Tools  occur  associated  with  them 
but  the  cranial  capacity  was  between  500  and  750  c.c,  hardly  greater 
than  in  living  apes.  Several  types  occur  and  it  is  not  agreed  whether 
all  should  be  included  in  the  single  genus  * Australopithecus.  The  first 
skull  found,  in  1924,  is  that  of  a  young  individual,  whose  rather 
prognathous  jaws  and  low  cranium  have  an  ape-like  appearance, 
though  the  brow  ridges  and  crests  are  slight  (Fig.  413).  Later  finds 
include  a  different  type  (* Paranthropus)  with  marked  brow  ridges  and 
sagittal  and  occipital  crests  (Fig.  417).   Evidently  the  muscles  of 


644 


MAN 


XXIV.   12- 


mastication  were  powerful  and  the  jaws  are  massive.  However,  the 
dental  arcades  are  smoothly  rounded,  as  in  man,  with  little  develop- 
ment of  the  canines,  small  incisors,  and  bicuspid  lower  first  premolar. 
The  molars,  however,  are  heavily  built  and  the  third  is  the  largest. 
They  carry  cusps  with  a  'dryopithecus'  pattern  (Fig.  418). 


Fig.  418.  A,  diagrammatic  reconstructions  of  palate  of  an  australopithecine  for 
comparison  with  that  of  gorilla  (B);  right  side  of  pelvis  of  chimpanzee  (C),  modern 
man  (D),  and  an  australopithecine  (E)  (not  to  the  same  scale).  The  missing  part  of 
the  front  of  the  ilium  of  E  extended  farther  forward  than  the  dots  show.  (After 
Le  Gros  Clark,  B.M.  Guide.) 

There  is  much  evidence  that  these  creatures  walked  upright.  The 
foramen  magnum  lies  far  forward  and  the  area  for  attachment  of 
nuchal  muscles  is  reduced  (Fig.  413).  Several  specimens  of  the  pelvis 
have  been  found  and  they  show  a  broad  ilium  very  different  from  that 
of  apes  (Fig.  418).  The  lower  end  of  the  femur  and  the  astragalus  also 
show  human  characteristics.   It  may  be  that  these  creatures  were 


xxiv.  i3  EARLY   HOMINIDS  64S 

bipeds,  though  it  has  not  yet  been  established  that  the  ilium  was 
placed  as  in  man  or  that  the  gluteus  medius  and  minimus  acted  as 
abductors,  f 

This  complicated  mixture  of  human  and  ape  features  makes  it 
difficult  to  assess  the  correct  position  of  these  fossils.  They  suggest 
that  the  upright  gait  was  not  necessarily  associated  with  a  large  brain. 
Although  the  skull  and  dentition  have  undoubtedly  many  similarities 
with  those  of  man  there  are  also  great  differences,  especially  in  the 
*Paranthropus  type.  These  points  make  it  doubtful  whether  the 
Australopithecines  lie  close  to  the  direct  ancestry  of  man,  which  would 
perhaps  be  unlikely  in  any  case  because  of  their  late  date.  They  may 
well  be  descendants  of  the  Pliocene  population  that  gave  rise  to  the 
true  hominids. 

13.  Early  Hominids,  *Pithecanthropus 

Fossil  remains  that  are  beyond  doubt  those  of  creatures  close  to 
man  have  been  found  from  the  first  interglacial  period  of  the  Pleisto- 
cene onwards.  The  most  primitive  type,  ^Pithecanthropus,  was  first 
named  from  fossils  found  in  Java,  but  similar  bones  have  since  been 
found  in  China;  although  named  * Sinanthropus  by  some  investigators 
Pekin  man  is  often  included  in  the  same  genus  as  the  Java  man.  These 
creatures  had  a  long,  low  brain-case,  with  low  forehead,  large  brow 
ridge,  and  a  very  thick  skull  (Fig.  413).  The  cranial  capacity  was  about 
900-1,000  c.c,  much  less  than  in  modern  men,  but  more  than  in  any 
known  ape.  The  face  was  rather  prognathous,  the  lower  jaw  long  and 
strong,  but  with  a  receding  chin.  The  teeth  were  in  general  of  human 
type,  but  with  large  canines  in  the  males.  The  head  must  have  been 
quite  well  balanced  on  the  neck,  for  the  mastoid  processes  were  large. 
Further  evidence  that  the  creature  walked  erect  is  found  in  the  straight 
and  very  modern  femur,  but  the  post-cranial  skeleton  is  not  well 
known. 

The  differences  between  these  people  and  modern  man  are  sufficient 
to  make  the  use  of  a  separate  generic  name  a  convenience,  yet  they 
must  have  been  in  many  ways  very  like  ourselves.  There  is  evidence 
from  the  caves  of  the  use  of  fire  and  pottery,  and  also  the  bones  there 
show  clear  signs  of  being  broken  open  for  their  marrow.  There  is, 

f  The  most  recent  Australopithecine  finds  have  been  referred  to  a  separate  genus  *Zin- 
janthropus,  somewhat  similar  to  *Paranthropus.  Its  canine  teeth  are  even  more  human  than 
those  of  previous  finds.  Further  interesting  features  are  that  the  fossil  was  found  in 
association  with  primitive  stone  tools  (Chellean  or  pre-Chellean)  and  finally  that  the 
potassium-argon  method  gives  a  date  of  one  and  three-quarter  million  years  for  the  stratum. 
(Leakey  1961.) 


B 


646  MAN  xxiv.  13- 

however,  a  slight  possibility  that  the  fire,  the  instruments,  and  the 
cannibalism  were  all  the  work  of  later  invaders,  of  a  still  more  human 
type!  The  remains  undoubtedly  belonging  to  *  Pithecanthropus  all 
come  from  the  Far  East,  but  some  large  jaws  from  the  middle  Pleisto- 
cene of  Algeria,  named  *Atlantropus,  may  be  related. 

14.  Man 

All  the  remaining  finds  are  usually  referred  to  the  genus  Homo. 

All  living  races  of  man  are  included  in 
a  single  species  H.  sapiens,  but  some  of 
the  fossils  are  placed  in  other  species, 
H.  heidelbergensis  and  H.  neandertalensis. 
The  first  of  these  is  the  name  given  to  a 
jaw  of  the  first  interglacial  period.  It  is 
of  a  very  heavy  type,  rather  like  that  of 
*  Pithecanthropus,  but  with  a  chin  and 
without  a  simian  shelf.  The  teeth  are  not 
far  from  the  modern  type.  The  true 
position  of  this  Heidelberg  man  is  un- 
certain and  so  therefore  the  age  of  the 
genus  Homo.  Much  more  abundant 
remains  are  found  in  the  third  inter- 
glacial and  last  glacial  period  and  are 
referred  to  as  Neanderthal  man  (Figs. 
419  and  420).  The  brain-case  was  larger 
than  that  of  many  modern  men  (nearly 
1,600  c.c),  but  was  long  and  low  and 
especially  prominent  behind.  The  brow 
ridges  are  large,  the  face  rather  progna- 
thous, and  the  chin  present  but  receding. 
The  whole  structure  of  the  skull  was 
stouter  than  our  own,  with  a  thick 
jugal  bar,  thick  roof  bones,  and  large 
mandible.  The  teeth  were  larger  than  in  modern  man  and  the  Y5 
pattern  is  said  to  be  frequent.  The  third  molars  were  smaller  than  the 
second,  however.  The  foramen  magnum  pointed  rather  backwards 
and  it  is  possible  that  Neanderthal  man  did  not  walk  fully  upright. 
Long  cervical  spines  have  been  described,  but  these  are  very  variable 
and  do  not  justify  the  reconstruction  of  these  people  as  having  a 
slouching  gait. 

Casts  of  the  brain  show  that  it  differed  in  several  ways  from  our 


Fig 
the 


419.  Comparisons  between 
geometric     outlines    of    the 

skulls  of:   A.  Modern  European; 

B.  *Homo  neandertalensis  (La  Cha- 
pelle);  c.  Chimpanzee. 

a.  prosthion;  b.  basion;  br.  bregma; 
ct.  upper  border  of  the  cerebellum; 
e.  ephippion;  fe.  fossa  ethmoidalis; 
i.  inion;  /.  lambda;  w.  nasion; 
o.  opisthion.  (After  Boule.) 


NEANDERTHAL   MAN 


647 


XXIV.  14 

own,  especially  in  the  relatively  small  frontal  lobes  and  backwardly 
extending  occipital  region. 

Typical  Neanderthal  skeletons  are  common  in  Europe  but  the  type 
was  probably  widespread  since  similar  fossils  have  been  found  in 


FlG.  420.  Skeletons  of  Neanderthal  and  modern  man.  (After  Howells,  Mankind 
So  Far,  Doubleday  and  Co.  Inc.) 


South  Africa  (*H.?i.  rhodesiensis)  and  Java  (*H.n.  soloensis),  the  latter 
showing  primitive  features  that  perhaps  connect  it  directly  with 
^Pithecanthropus. 


648  MAN  xxiv.  15 

15.  Human  cultures 

All  of  these  early  men  were  hunters,  living  apparently  in  small 
families,  in  caves.  They  used  fire,  but  their  only  known  instruments 
were  of  wood  or  stone.  Chipped  flints  found  from  the  time  of  the  first 


Plioce 


roe 


QEOLOQICAL 
PERIODS 


FOSSIL 

MEN 


ICE 


STONE 
CULTURES 


CULTURE 
PERIODS 

TIME  in  millions 
of1  years 


Lower 
Pleistocene 


Pleistocene 
MMc 

Pleistocene 


Recent 


Upper 
Pleistocene 


PithecanrhropiLS      "' 
Australopithecus 


1°?i°  .SffiLSlL 

Neanderthal 


IpswichiaiiY}^.^^  Clactonian  (hfT\§  Levalloisian 

Abbevillian  Acheulian  Mousterian 


10 


LOWER.       PALEOLITHIC 


0-5 


IIS" 
52to 


01 


Fig.  421.  Diagram  of  Pleistocene  time  and  some  stages  of  human  cultural  evolution. 
(After  Howells,  Mankind  So  Far,  Doubleday  and  Co.  Inc.) 

glaciation  and  following  warm  period  are  so  crude  as  to  be  hardly 
recognizable  as  artefacts  and  these  'eoliths'  are  said  to  be  signs  of  a 
pre-palaeolithic  culture.  More  definitely  shaped  flints,  used  as  axes, 
are  found  during  the  second  ice  age,  second  interglacial,  and  third  ice 
advance  and  are  referred  to  the  lower  Palaeolithic  (Chellean  and 
Acheulian)  stages.  The  third  interglacial  and  last  glacial  period  con- 
stitute the  middle  Palaeolithic  (Mousterian),  with  well-made  flints, 
probably  produced  by  Neanderthal  man.  The  making  of  tools  is 
therefore  probably  characteristic  of  the  creatures  we  refer  to  the  genus 
Homo.  This  power  may  be  connected  with  the  capacity  for  communi- 
cation by  symbols  that  indicate  abstractions,  which  marks  off  men 
from  animals  more  clearly  than  any  other  feature.  The  recession  of  the 
last  main  glaciation  began  less  than  100,000  years  ago  and  at  that  time 


xxiv.  is  RACES    OF   MAN  649 

there  were  a  series  of  upper  Palaeolithic  cultures  (Aurignacian,  Solu- 
trean,  and  Magdalenian)  in  which  besides  wonderfully  chipped  flints 
there  were  also  fine  bone  and  ivory  needles,  blades,  and  other  instru- 
ments. These  were  probably  made  by  men  of  H.  sapiens  type,  whose 
skulls  first  became  abundant  in  caves  and  deposits  of  the  last  glacial 
period. 

The  question  of  the  first  appearance  of//,  sapiens  is,  however,  com- 
plicated by  the  skulls  found  at  Swanscombe  and  Fontechevade,  from 
Middle  and  Upper  Pleistocene  levels.  These  'presapiens'  fossils  lack 
the  Neanderthal  characters  (brow  ridges,  occiput,  &c.)  but  are  thick 
and  more  heavily  built  than  modern  skulls.  Evidently  from  the  Middle 
Pleistocene  onwards  there  has  been  a  considerable  variety  in  the 
human  populations,  but  all  may  be  included  in  one  species. 

The  details  of  the  replacement  of  these  species  and  races  by  each 
other  remain  obscure.  Probably  invading  races  often  took  over  parts 
of  the  cultures  of  their  victims,  as  well  as  bringing  in  their  own  culture, 
so  that  the  whole  story  becomes  very  confused.  It  is  usually  con- 
sidered that  H.  neanderthalensis  did  not  evolve  into  H.  sapiens,  at  least 
in  Europe,  but  was  replaced  by  a  wave  of  invaders  coming  from  central 
Asia.  Similarly,  at  the  end  of  the  Palaeolithic  period,  about  14,000 
years  ago,  the  hunters  of  that  time  gave  place  first  to  a  series  of  little- 
known  Mesolithic  invaders,  builders  of  the  lake-dwellings  found  in 
various  parts,  and  then  to  the  Neolithic  people,  who  were  farmers  and 
city-builders  and  from  about  9000  B.C.  onwards  dominated  the  Middle 
East  and  south  Mediterranean  region  and  thence  spread  outwards, 
developing  the  series  of  cultures  known  as  the  Bronze  and  Iron  Ages. 

The  history  of  man,  like  that  of  so  many  other  mammals,  has  there- 
fore possibly  been  of  a  series  of  invasions  from  the  central  Asiatic 
land-mass,  and  it  is  not  surprising  that  remnants  of  earlier  types  should 
be  found  surviving  today  on  the  tips  of  the  continents,  towards  the 
south.  The  most  conspicuous  of  these  are  the  Australian  Aborigines, 
who  show  several  primitive  features,  both  of  structure  and  of  culture. 
The  brow  ridges  are  better  developed  than  in  any  other  men  and  the 
forehead  and  chin  recede.  These  Blackfellows  are  nomadic  hunters, 
without  fixed  abode,  and  their  social  organization  and  instruments  are 
those  of  a  Palaeolithic  stage  of  life. 

In  something  the  same  way  the  Bushmen  of  South  Africa,  though 
not  physically  of  a  primitive  type,  preserve  traces  of  Palaeolithic  culture, 
including  art  conventions  similar  to  those  used  by  the  Aurignacian 
people  who  painted  bison  and  mammoths  in  the  caves  of  Altamira  in 
Spain  50,000  years  ago. 


650  MAN  xxiv.  15 

There  is  much  evidence  that  change  of  the  physical  characteristics 
of  human  populations  has  continued  during  the  last  10,000  years.  Thus 
H.  sapiens  before  the  Mesolithic  period  was  long-headed  (dolicho- 
cephalic). Short,  broad  skulls  (brachycephalic)  first  appeared  at  that 
time  and  are  now  found  in  more  than  half  the  population  of  the  world. 
Changes  in  the  shape  of  the  jaw  and  face  and  reduction  of  the  teeth, 
which  have  been  going  on  for  a  long  time,  probably  continue  today. 

Study  of  the  gradual  mixing  and  changing  of  human  populations, 
besides  its  personal  interest,  is  of  value  to  a  zoologist  in  calling  the 
process  of  evolution  to  our  imagination  and  showing  us  its  complexity 
and  slowness.  Without  undue  difficulty  we  can  have  in  mind  a  picture 
of  great  populations  of  human  beings,  composed  of  individuals  differ- 
ing slightly  in  structure  and  habits,  warring  and  competing  with  each 
other,  so  that  one  group  comes  to  dominate  another,  the  invader  taking 
over  some  of  the  genes  and  the  gods  of  its  victims.  We  can  at  least  guess 
how  such  a  process  would  lead  the  population  of  any  area  to  change, 
either  if  a  set  of  individuals  arises  that  is  more  active  or  in  some  way 
more  efficient  than  another,  or  following  a  change  in  conditions  that 
gives  preference  to  a  particular  set  of  structures  or  habits.  Though 
evolution  is  a  slow  process  it  is  always  going  on  before  us,  and  the  best 
way  to  see  it  is  to  look  at  our  own  species,  vastly  more  familiar  and  re- 
vealing than  any  other.  All  sheep  or  shrews  look  to  us  much  alike,  but 
we  can  more  readily  tell  what  sort  of  man  or  woman  we  are  meeting 
and  what  they  are  likely  to  do  in  the  world.  Moreover  we  can  recon- 
stitute their  capacities  by  the  remains  of  their  cultures  and  recognize 
clearly  how  different  our  ancestors  were  from  ourselves  50,000  years 
ago  and  still  more  so  at  500,000  years.  In  this  way  we  may  get  some 
faint  picture  of  the  slow  and  confused  changes  that  constitute  evolu- 
tion. Even  with  such  a  slow  breeding  species  as  our  own  the  effort  of 
thought  is  very  great.  Allowing  only  so  few  as  four  generations  per 
century  we  may  conclude  that  we  are  separated  from  ^Pithecanthropus 
populations  by  40,000  generations.  If  we  ever  had  an  ape-like  hairy 
ancestor  it  was  perhaps  our  great-grandfather  500,000  times  removed, 
counting  back  only  to  the  beginning  of  the  Pliocene.  Yet  men  and 
apes  are  zoologically  much  alike. 

Many  factors  have  been  suggested  to  account  for  the  appearance  of 
man's  particular  characteristics.  Disappearance  of  forests  may  have 
favoured  a  terrestrial  bipedal  life  and  use  of  the  hands.  The  great  size 
of  the  brain  might  have  followed  from  this.  It  has  been  claimed  that 
this  might  have  resulted  from  single  mutations  that  increased  the 
number  of  divisions  of  the  neuroblasts  from  31  in  apes,  giving  about 


xxiv.  15  PAEDOMORPHOSIS  651 

2-5  X  io9  cortical  cells,  to  32  in  *  Pithecanthropus  (4-3  X  io9)  and  33 
in  Homo  (ioxio9). 

In  development  of  powers  of  obtaining  information  with  the  nervous 
system  man  is  only  showing  an  accentuation  of  the  characteristics  of 
mammals  in  general  and  especially  primates.  With  this  goes  the  low 
reproduction  rate,  slow  development,  and  great  post-natal  care.  The 
retardation  of  development  of  somatic  characters  seems  to  have  been 
the  basis  of  many  human  features.  As  Bolk  pointed  out  man  resembles 
in  many  ways  a  foetal  ape,  rather  than  an  adult  one.  Thus  the  position 
of  the  head,  at  right  angles  to  the  vertebral  column,  is  that  found  in 
foetal  apes.  The  late  fusion  of  ossification  centres,  lack  of  hair,  external 
genitalia,  structure  of  hand  and  foot  and  many  other  features  point  the 
same  way.  In  addition  to  this  general  retardation  there  have  no  doubt 
been  many  special  developments,  such  as  formation  of  the  nose, 
lengthening  of  the  pollex  and  elaboration  of  the  organs  of  speech  and 
the  muscles  of  expression. 

This  paedomorphosis  in  man,  producing  teachable,  cooperative 
individuals  may  well  be  the  factor  that  has  made  possible  the  develop- 
ment of  complex  societies  and  their  tools.  By  efficient  communication 
man  is  able  to  produce  a  cumulative  store  of  information  outside  his 
mortal  body  and  passed  on  not  only  to  few  individuals,  as  is  the  genetic 
store,  or  that  passed  by  word  of  mouth,  but  to  many.  Each  individual 
thus  'inherits'  not  from  two  or  few  parents  but  from  the  accumulated 
memory  store  of  a  large  population.  It  is  perhaps  this  'multi-parental' 
inheritance  of  information  that  has  changed  man  so  rapidly  in  the  past 
and  is  likely  to  do  so  even  faster  in  the  future.  Success  will  clearly  be 
for  those  populations  that  are  able  so  to  cooperate  as  to  discover  and 
transmit  more  and  more  information. 


XXV 

RODENTS  AND  RABBITS 

1 .  Characteristics  of  rodent  life 

The  animals  loosely  known  as  rodents  are  the  most  successful  of 
modern  mammals  other  than  man.  They  live  in  all  parts  of  the  world, 
from  the  tropics  nearly  to  the  poles.  Three  thousand  species  are  known, 
as  many  as  are  found  in  all  other  mammalian  orders  put  together.  They 
inhabit  a  considerable  variety  of  ecological  niches,  mostly  on  the  land, 
often  in  burrows,  but  many  in  the  trees  and  some  in  the  water.  This 
most  successful  type  of  mammalian  life  is,  however,  in  several  ways  un- 
typical of  the  rest  and  indeed  has  been  isolated  since  the  early  Tertiary. 
One  striking  point  is  that  the  animals  have  never  become  large  in  size, 
although  such  increase  is  a  tendency  found  in  almost  all  other  mam- 
malian groups.  The  South  American  capybara,  the  largest  living 
rodent,  is  the  size  of  a  small  pig,  and  few  fossil  forms  were  much  larger. 
Rodent  life  has  specialized  in  rapid  breeding  and  this  system  of  pro- 
duction of  large  numbers  of  small  animals  has  been  very  successful. 
The  total  rodent  biomass  today  may  well  be  greater  than  that  of  the 
whales,  which  are  at  the  other  extreme,  and  have  all  the  advantages  of 
aquatic  life.  The  rapid  reproduction  presumably  brings  considerable 
evolutionary  advantages,  enabling  the  population  to  make  the  adjust- 
ments necessary  to  meet  changing  circumstances.  One  of  the  charac- 
teristics of  rodent  populations  today  is  their  great  fluctuations  (p.  663), 
notorious  in  the  case  of  the  voles,  mice,  and  lemmings,  but  marked  also 
in  rats  and  other  forms.  The  pressure  of  rodent  life  is  such  that  no 
stable  equilibrium  is  reached  with  the  environment  and  extreme  oscil- 
lations occur,  often  with  results  of  great  importance  to  man  and  to  his 
crops. 

In  spite  of  the  similarities  of  all  these  animals  with  gnawing  teeth, 
zoologists  consider  that  the  rabbits  and  hares  are  not  closely  related  to 
the  others  and  are  therefore  to  be  placed  in  a  distinct  order  Lagomorpha, 
the  order  Rodentia  being  retained  for  all  other  'rodents'.  It  is  not  even 
certain  that  the  two  orders  are  in  any  way  related.  Fossil  rodents  (in 
the  strict  sense)  certainly  occurred  in  the  late  Palaeocene  period  and  a 
probable  lagomorph  is  reported  from  the  same  time.  Both  groups 
retain  many  primitive  mammalian  characters,  for  instance,  a  long,  low 
skull,  with  small  brain  and  small  cerebral  hemispheres,  temporal  fossa 


xxv.  i-2  CLASSIFICATION  653 

widely  open  to  the  orbit,  pentadactyle  limbs,  separate  radius  and  ulna, 
and  so  on.  These  features,  being  found  in  all  early  mammals,  indicate 
no  closer  affinity  of  the  two  orders  than  depends  on  evolution  from  a 
common  stock.  It  is  not  even  clear  exactly  how  the  two  groups  are 
related  to  the  ancestral  eutherians,  and  we  must  be  content  to  say  that 
it  is  probable  that  animals  with  rodent  specializations  diverged  from 
the  insectivoran  eutherian  stock  in  the  late  Cretaceous  or  Palaeocene 
and  then  rapidly  became  differentiated  into  lagomorphan  and  rodent 
types.  The  two  orders  are  therefore  placed  together  in  an  isolated 
cohort  Glires. 

2.  Classification 

Cohort  2.  Glires 
Order  1.  Rodentia  (=  Simplicidentata) 
Suborder  1.  Sciuromorpha 
Thirteen  families,  including 

*Family    Ischyromyidae.    Palaeocene-Miocene.    Eurasia,    N. 
America 
*Paramys,  Palaeocene-Eocene 
Family  Aplodontidae.  Eocene-Recent 

Aplodontia,  mountain  beaver,  N.  America 
Family  Sciuridae.  Squirrels.  Miocene-Recent 

Scinriis,  squirrel,  Holarctic;  Marmota,  marmot,  woodchuck, 
Holarctic;    Tatnias,   chipmunk,   N.   America;   Petaurista, 
flying  squirrel,  Eurasia 
Family  Geomidae.  Gophers.  Oligocene-Recent.  N.  America 

Geomys,  pocket  gopher 
Family  Castoridae.  Beavers.  Oligocene-Recent.  Holarctic 
Castor,  beaver 
Suborder  2.  Myomorpha 
Nine  families,  including 
Family  Dipodidae.  Jerboas.  Pliocene-Recent.  Palaearctic 

Dipus,  jerboa,  Eurasia 
Family    Cricetidae.     Voles.     Oligocene-Recent.    World-wide 
(except  Australasia) 
Peromyscus,   deer  mouse,   N.  America;   Lemmus,  lemming, 
Holarctic;  Microtiis,  vole,  Holarctic 
Family  Muridae.  Rats  and  mice.  Pliocene-Recent.  Native  to 
Old  World 
Apodemus,  field  mouse;  Rattus,  rat;  Mas,  house  mouse;  Gits, 
dormouse;  Notomys,  jerboa-rat 


654  RODENTS   AND    RABBITS  xxv.  2- 

2.  Classification  (cont.) 

Family  Zapodidae.  Jumping  mice.  Oligocene-Recent.  Holarctic 
Zapus,  jumping  mouse 
Suborder  3.  Hystricomorpha 
Nineteen  families,  including 

Family  Hystricidae.  Oligocene-Recent.  Palaearctic,  Africa 
Hystrix,  porcupine,  Asia,  Africa;  Erethizon,  N.  American 
porcupine,  N.  America 
Family  Caviidae.  Pliocene-Recent.  S.  America 

Cavia,  guinea-pig 
Family  Hydrochoeridae.  Pliocene-Recent.  S.  America 

Hydrochoeras,  capybara 
Family  Dasyproctidae.  Recent.  S.  America 

Cuniculus,  agouti  (pacas) 
Family  Chinchillidae.  Oligocene-Recent.  S.  America 

Lagostomns,  vizcacha 
Family  Bathyergidae.  Pleistocene-Recent.  Africa 
Bathyergus,  mole-rat 
Order  2.  Lagomorpha  (=  Duplicidentata) 
Family  1.  *Eurymylidae.  Palaeocene 

*Eurymylus,  Asia 
Family  2.  Ochotonidae.  Upper  Oligocene-Recent 

Ochotona  (=  Lagomys),  pika  (cony),  N.  America 
Family  3.  Leporidae.  Upper  Eocene-Recent 

Lepus,  hare,  Pleistocene-Recent,  Palaearctic,  N.  Africa; 
Oryctolagus,  rabbit,  Pleistocene-Recent,  Europe,  N.Africa; 
Sylvilagus,  cotton-tail,  Pleistocene-Recent,  N.  and  S. 
America 

3.  Order  Rodentia 

Rodents  are  mostly  herbivorous  and  their  most  characteristic 
features  are,  of  course,  in  their  teeth,  especially  the  incisors,  one  pair 
only  of  which  persists  in  each  jaw;  hence  they  were  the  suborder 
'Simplicidentata'  of  the  older  order  Rodentia,  which  included  also  the 
rabbits  and  hares.  These  latter  have  a  second  pair  of  upper  incisors, 
hence  'Duplicidentata'.  The  incisor  has  enamel  only  on  its  labial 
surface  and  thus  maintains  a  cutting  edge.  It  is  worn  away  at  the  rate 
of  perhaps  several  millimetres  a  week  and  is  replaced  by  continual 
growth,  for  which  it  has  a  very  wide  open  pulp  cavity,  or  in  the  con- 
ventional term  is  said  to  be  a  'rootless'  tooth.  The  incisors  are  often 
very  large  and  curved  and  their  gnawing  action  against  each  other 


xxv.  3  TEETH    OF   RODENTS  655 

gives  them  chisel  edges.  If  one  incisor  is  lost  the  other  continues  to 
grow  round  in  a  spiral,  until  it  enters  the  skull. 

The  remaining  incisors,  canines,  and  anterior  premolars  are  missing, 
leaving  a  large  diastema  in  front  of  the  cheek  teeth.  Folds  of  skin  can 
be  inserted  into  this  gap  to  close  off  the  front  part  of  the  mouth,  so 
that  material  bitten  off  during  gnawing  is  not  necessarily  swallowed. 
A  distinct  anterior  chamber  of  the  mouth  is  thus  formed,  and  may  be 
prolonged  into  deep  pockets  in  which  food  is  stored  for  transport  to 


Fig.  422.  Diagrams  of  lower  jaws  of  Sciurus. 

A,  at  rest;  B,  opened  for  seizing;  C,  closed  for  gnawing  or  to  prise  open  a  nut. 

mlp.  deep  part  of  lateral  masseter;  mis.  superficial  part  of  the  same;  tm.  trans- 

versus  mandibulae.  (From  Weber  after  Krumbach.) 

the  hoards  that  are  collected  by  many  species.  The  teeth  are  not  used 
only  for  obtaining  food ;  rats  will  gnaw  their  way  through  a  lead  pipe. 
The  premolars  are  reduced  to  two  above  and  one  below  in  the  more 
primitive  squirrels;  even  fewer  are  present  in  other  rodents.  The 
molars  and  premolars  are  usually  alike  in  pattern  and  show  modifica- 
tions similar  to  those  found  in  the  grinders  of  other  herbivorous 
mammals.  The  cusps  of  the  original  eutherian  molar  can  still  be 
recognized  in  the  squirrels,  but  they  are  arranged  in  transverse  rows, 
paracone  and  protocone  in  front,  metacone  and  hypocone  behind.  The 
cusps  become  joined  in  pairs  to  form  ridges,  giving  a  bilophodont 
grinding  tooth.  In  most  of  the  rodents  further  ridges  are  then  added 
in  front,  behind,  and  between  the  original  ones,  and  these  are  also 
joined  by  cross-ridges,  giving  a  multi-lophodont  molar.  Similar 
changes  occur  in  the  lower  teeth.  The  teeth  also  become  very  high- 
crowned  or  'hypsodont'  and  the  enamel,  dentine,  and  bone  ('cement') 
wear  at  differing  rates.  The  roots  remain  wide  open  and  the  teeth 
grow  continually.  All  of  these  features  are  like  those  arrived  at  in 
ungulates  by  a  convergent  process  of  evolution.  A  further  feature  of 


656 


RODENTS   AND    RABBITS 


xxv.  3 


the  rodents  is  that  the  upper  tooth-rows  are  set  closer  together  than  the 
lower  and  bite  inside  the  latter,  often  giving  an  oblique  grinding  surface. 
The  milk  teeth  are  shed  very  early  and  are  not  functional. 

The  lower  jaw  and  its  muscles  show  many  modifications.  The 
articulation  is  very  long,  and  the  lower  jaw  moves  backwards  and 
forwards  on  the  upper;  indeed  the  lower  incisors  are  thrust  so  far 
forward  that  while  gnawing  the  molar  surfaces  no  longer  occlude.  A 


Fig.  423.  The  masseter  of  rodents. 

A,  Aplodontia,  primitive  sciuromorph :  the  muscle  takes  origin  from  the  zygomatic  arch ; 

B,  myomorph:  the  deep  masseter  passing  through  the  orbit  is  also  attached  to  the  face; 
c,  advanced  sciuromorph:  the  superficial  masseter  is  attached  to  the  skull  in  front  of  the 
orbit;  D,  hystricomorph:  superficial  masseter  unspecialized,  large  foramen  for  deep  portion. 

(After  Romer,  Vertebrate  Paleontology,  University  of  Chicago  Press.) 

curious  feature  is  that  the  mandibles  are  not  united  in  a  symphysis  but 
are  freely  movable,  with  a  joint  cavity  between  them.  A  special  portion 
of  the  mylohyoid  muscle,  known  as  the  m.  transversus  mandibulae, 
draws  the  two  mandibles  together,  causing  the  lower  incisors  to 
separate  (Fig.  422).  The  action  of  the  lateral  portions  of  the  masseters 
then  brings  the  two  teeth  together  again  with  a  scissor  action. 

The  jaw-muscles  are  very  large  and  modified  to  produce  the  back- 
ward and  forward  motion  of  the  jaw  (Fig.  423).  In  the  more  primitive 
condition,  found  in  squirrels  (Sciuromorpha),  the  masseter  is  attached 
to  the  zygomatic  arch  as  it  is  in  other  mammals,  but  is  divided  into 
a  more  lateral  portion  with  simple  up  and  down  action,  and  a  medial 
part  that  pulls  the  jaw  forward.  In  more  advanced  rodents  both  of 
these  parts  of  the  muscle  obtain  extra  insertions.  In  rats  and  mice 
(Myomorpha)  the  lateral  part  extends  forward  on  to  the  face  and 


xxv.  3  RODENT  CHARACTERS  657 

the  medial  passes  out  of  the  orbit  through  the  much-enlarged  infra- 
orbital canal.  In  the  porcupines  and  their  allies  (Hystricomorpha) 
the  lateral  portion  remains  simple  and  the  medial  proceeds  to  a  large 
insertion  on  the  face  below  (but  not  through)  the  infra-orbital  canal. 
The  lower  jaw  often  carries  a  large  flange,  for  the  attachment  of  the 
masseter  muscle.  The  pterygoid  muscles  and  their  attachments  are  also 
often  large,  but  the  temporal  muscle  is  usually  small. 

Apart  from  their  gnawing  mechanism  the  rodents  remain  rather 
unspecialized  mammals.  The  gait  is  plantigrade,  the  fore-limbs  often 
shorter  than  the  hind  and  used  for  handling  the  food.  In  some  this 
tendency  is  carried  to  the  extent  of  producing  a  hopping,  bipedal  gait. 
The  gut  shows  a  large  coecum  and  food  is  passed  twice  through  the 
gut  (p.  662).  A  division  of  the  stomach  is  found  only  in  mice,  which 
have  a  horny  cardiac  region.  Rodents  are  macrosmatic,  with  large 
olfactory  bulbs  and  relatively  small,  smooth  neopallium.  The  eyes  are 
often  well  developed,  especially  in  arboreal  rodents  and  those  living 
in  open  country  or  steppe.  Hearing  is  often  good,  and  in  some  desert 
species  the  tympanic  bulla  is  greatly  dilated,  perhaps  to  detect  sounds 
made  by  the  widely  separated  individuals.  Many  rodents  have  well- 
developed  social  habits,  with  olfactory  and  visual,  as  well  as  auditory 
and  tactile  signalling. 

Rodents  are  mostly  polyoestrous,  often  breeding  throughout  the 
year,  at  least  in  captivity.  Numerous  young  are  produced  and  are  often 
cared  for  in  a  nest.  The  uterus  is  usually  double  and  the  placentation 
usually  of  the  discoidal  and  haemochorial  type. 

No  thoroughly  satisfactory  scheme  for  grouping  the  various  types 
of  rodent  has  been  devised ;  the  best  that  we  can  do  is  to  keep  to  the 
classical  division  of  the  order  into  three  suborders,  Sciuromorpha, 
Myomorpha,  and  Histricomorpha.  The  first  includes  besides  the  more 
primitive  surviving  forms,  Aplodontia,  the  mountain  beaver  of  North 
America,  also  the  most  ancient  fossil  rodents  (*Ischyromyidae)  and 
some  families  of  uncertain  affinities.  The  characteristics  of  the  sub- 
order are  that  there  are  two  upper  premolars  and  one  lower  and  a 
masseter  muscle  that  does  not  pass  through  the  infra-orbital  canal. 
The  suborder  includes  the  squirrels  (Sciuridae)  found  in  all  major 
regions  except  Australasia.  They  are  diurnal,  with  large  eyes  and  often 
bright  colouring.  The  flying  squirrels,  Petaurista,  glide  for  long  dis- 
tances by  means  of  the  patagium,  whose  muscles  enable  them  to 
change  direction  in  the  air  (Fig.  424). 

The  marmots  (Marmota,  Fig.  425),  ground  squirrels  (Citellus),  and 
prairie  dogs  {Cynomys)  are  burrowers,  with  elaborate  underground 


(658) 


Fig.  424.  Flying  squirrel,  Petaurista.  (From  a  photograph.) 


Fig.  425.  Marmot,  Marmota. 
(From  photograph.) 


Fig.  426.  Beaver,  Castor. 
(From  photographs.) 


Fig.  427.  Lodge  and  food  store  of  the  beaver.  (From  American  Mammals, 
by  W.  J.  Hamilton,  McGraw  Hill  Book  Company.) 


xxv.  3  BEAVERS  659 

societies.  The  gophers  (Geomys)  and  kangaroo  rats  (Dipodumys)  of  the 
United  States  are  also  sometimes  placed  here.  They  are  jumpers, 
paralleling  the  jerboas,  gerbils,  and  jerboa-rats. 

Possibly  also  in  this  group  are  the  beavers,  Castoridae,  found 
throughout  the  Holarctic.  These  are  aquatic  rodents  (Fig.  426)  that 
show  remarkable  habits  in  preparing  a  house  and  store  of  food  for 
the  winter  (Fig.  427).  The  house  ('lodge')  is  built  on  a  mass  of  debris 
so  as  to  be  surrounded  by  water.  Sticks  are  built  up  to  make  a  wall 
round  the  platform  and  the  whole  finally  closed  by  a  dome  of  sticks 


Fig.  428.  Jerboa,  Dipus.  (From  life.) 

and  mud,  which  is  carried  by  the  beavers  with  their  fore-paws.  When 
this  damp  structure  freezes  it  makes  a  strong  protection  against  bears 
and  other  enemies,  and  the  beavers  keep  warm  inside  it.  Food  is 
obtained  from  the  bark  of  branches  kept  in  a  store  under  water  and 
brought  up  to  the  lodge  through  a  plunge  hole.  The  beaver  dams  are 
made  by  the  beavers  during  the  summer  in  order  to  deepen  the  streams ; 
they  may  reach  a  height  of  12  ft  and  a  length  of  several  hundred.  The 
lodges  and  dams  are  the  result  of  cooperative  work  by  successive 
generations.  The  beavers  work  compulsively,  repairing  the  structures 
whether  they  need  it  or  not.  Like  other  rodents  they  mark  their 
territory  by  smell,  there  being  large  anal  oil-glands.  When  an  animal 
smells  a  deposit  it  visits  it  and  adds  its  own  'castoreum'. 

The  Myomorpha  is  a  very  large  group,  including  the  rats,  mice, 
voles,  jerboas,  and  other  types,  all  having  the  medial  portion  of  the 
masseter  running  through  the  infra-orbital  canal,  but  probably  not 
really  closely  related.  They  include  many  families  and  genera,  with 
specializations  for  individual  ecological  niches.  The  jerboas,  Dipodidae 
(Fig.  428),  are  members  of  this  group,  with  limbs  specialized  for 
hopping,  but  in  other  respects  with  somewhat  primitive  characteristics. 
There  has  been  a  great  elongation  of  the  metatarsals  of  the  three 
central  digits,  which  alone  are  well  developed.  The  gerbils  (GerbiHus) 
are  yet  another  family  of  jumping  animals,  living  in  deserts.  The 
Muridae  (Fig.  429)  are  among  the  most  successful  of  all  mammals  and 
are  an  ancient  family,  recognizable  back  to  the  Pliocene  and  invading 


660  RODENTS   AND    RABBITS  xxv.  3-4 

all  parts  of  the  world,  including  in  relatively  recent  times  South 
America  and  Australasia,  reaching  the  latter  before  man.  They  are 
the  only  mammals  indigenous  to  New  Zealand.  The  family  includes 
an  enormous  variety  of  mice,  rats,  dormice,  field  mice,  hamsters  and 
so  on,  and  also  some  special  forms  such  as  the  jerboa- rat  (Notomys) 
of  Australia,  which  has  paralleled  the  true  jerboas  in  its  jumping  habits. 
The  rats  and  mice  may  be  considered  as  parasites  of  man  and  are  still 
changing  their  distribution.  Rattus  has  been  widely  spread  in  recent 
centuries.  The  black  rat  (R.  rattus)  prefers  warmer  and  drier  condi- 
tions than  the  brown  rat  (R.  norvegicus)  but  the  two  often  compete. 

The  voles  (Cricetidae)  are  a  related  family,  including  partly  aquatic 
as  well  as  terrestrial  forms.  The  field  vole  (Microtus  agrestis)  is  apt  to 
increase  greatly  in  numbers,  producing  notoriously  destructive  plagues. 
Lemmus,  the  lemming  (Fig.  430),  is  a  mouse-like  form  living  on  grasses 
and  roots  on  the  Norwegian  mountains.  At  irregular  intervals  of  3-5 
years  the  population  grows  greatly  by  increase  in  the  numbers  in  the 
litters  and  in  the  number  of  litters  in  the  season.  The  population 
becomes  too  great  for  the  area  to  support  and  large  numbers  emigrate 
to  the  lowlands  and  die  of  starvation  or  from  predators.  Others  reach- 
ing the  sea-shore  swim  out  and  are  drowned. 

The  histricoid  rodents  are  also  a  large  group,  with  the  infra-orbital 
canal  enlarged  for  the  medial  part  of  the  masseter,  but  with  the  lateral 
part  attached  to  the  zygoma.  They  include  the  porcupines  (Hystrix) 
of  Africa  and  Asia  (Fig.  431)  and  the  somewhat  different  porcupines 
of  North  America,  but  all  the  rest  of  the  group  occurs  in  South 
America,  an  area  invaded  by  hardly  any  other  rodents.  Fossil  histrico- 
morphs  are  found  in  South  America  from  the  Oligocene.  The 
Hystricidae  all  have  long  spines,  used  for  attack  by  a  rapid  backward 
movement  as  well  as  for  defence.  The  cavies  and  capybaras  (Fig.  432) 
are  closely  related  South  American  forms,  the  latter  being  a  large  semi- 
aquatic  animal  with  a  greatly  enlarged  and  folded  last  upper  molar. 
The  agoutis  (Fig.  434)  are  also  rather  large,  for  rodents,  and  are 
terrestrial,  often  burrowing  forms.  The  vizcachas,  Lagostomus  (Fig. 
433),  also  burrow  underground,  often  making  large  colonies. 

Possibly  related  to  the  hystricomorphs  are  still  more  modified  digging 
animals,  the  Bathyergidae  or  African  mole-rats,  which  have  lost  most 
of  the  hair  and  developed  long  claws  on  the  forelimbs. 

4.  Order  Lagomorpha 

The  rabbits  and  hares  are  nowadays  considered  to  be  a  very  isolated 
offshoot  of  the  early  eutherian  stock,  whose  similarities  to  the  Rodentia 


(66i) 


Fig.  429.  Common  brown  rat, 
Rattus.  (From  photographs.) 


Fig.  430.  Lemming,  Lemmus. 
(From  a  photograph.) 


Fig.  431.  Porcupine,  Hystrix. 
(From  a  photograph.) 


P'ig.  432.  Capybara,  Hydrochoerus. 
(From  a  photograph.) 


Fig.  433.  Vizcacha,  Lagostomus. 
(From  a  photograph.) 


/<  r 


Fig.  434.  Agouti,  Dasyprocta.  (From  life.) 


662 


RODENTS    AND    RABBITS 


XXV.  4- 


may  be  only  superficial.  The  two  orders  are  kept  together  in  one  cohort 
Glires,  more  as  a  convenience  than  because  of  characters  they  have  in 
common.  The  arrangements  for  gnawing  found  in  the  lagomorphs 
have  indeed  a  superficial  similarity  to  those  of  rodents,  but  on  inspec- 
tion the  differences  appear  profound.  Continually  growing  incisors 


Fig.  435.  a.  Diagram  of  stomach  of  Lepus:  dashes,  cardiac  zone;  dots,  fundus; 
crosses,  pyloric  glands.  B.  L.S.  of  rabbit  stomach,  c.  Diagram  showing  the  passage 
of  food  and  caecotrophs  traversing  the  digestive  tracts.  In  the  stomach,  under  the 
mechanical  action  of  peristalsis  the  caecotrophs  are  mixed  with  the  food.  In  the  lowest 
part  of  the  caecum,  the  chyme  under  the  action  of  bacteria  is  made  into  caecotrophs, 
which  the  animal  eats  soon  after  they  are  expelled  from  the  anus. 

ca.  caecotrophs;  cae.  caecum;  cr.  waste  pellets;    ma.  alimentary   mass;   oe.   oesophagus; 

p.  pylorus;  za.  zone  where  the  caecotrophs  are  mixed  with  the  alimentary  mass;  zc.  zone 

of  formation  of  caecotrophs.  (b.  and  c.  after  W.  Harder.) 


are  present  in  both  groups,  but  in  lagomorphs  the  upper  pair  is  accom- 
panied by  a  small  second  pair  (hence  'Duplicidentata').  The  diastema  is 
common  to  the  two  groups,  and  both  have  cheek  pouches  with  similar 
functions.  The  similarity  of  the  molariform  teeth  is  only  superficial, 
however;  in  the  lagomorphs  three  premolars  remain  in  the  upper  jaw 
and  two  in  the  lower.  The  premolars  and  the  molars  all  acquire  sharp 
transverse  ridges,  usually  two  each,  used  for  cutting  rather  than 
grinding,  the  upper  teeth  biting  outside  the  lower  ones,  not  inside  as 
in  rodents.  The  masseter  is  powerful,  but  simpler  than  in  rodents,  and 
it  does  not  extend  into  the  infra-orbital  canal.  The  temporalis  muscle 


xxv.  5  FEEDING  663 

is  reduced  in  both  groups,  but  the  lagomorphs  lack  the  power  of  move- 
ment between  the  two  halves  of  the  lower  jaw. 

Taken  all  together,  therefore,  the  differences  are  as  great  as  the 
similarities,  even  in  the  gnawing  mechanism,  which  the  rabbits  share 
with  the  other  rodents.  In  the  remaining  parts  there  are  few  points  of 
close  similarity,  other  than  those  due  to  the  fact  that  neither  set  of 
animals  has  departed  far  from  the  original  eutherian  condition.  More- 
over, serological  studies  do  not  show  any  signs  of  closer  affinity  of  the 
lagomorphs  with  the  rodents  than  with  other  mammalian  orders.  If 
anything  they  are  more  like  artiodactyls.  However,  the  lagomorphs 
share  with  rodents  the  habit  of  passing  food  twice  through  the 
alimentary  canal  (caecotrophy).  Dried  faecal  pellets  are  produced  only 
during  the  day.  At  night  soft  pellets  covered  with  mucus  are  formed 
in  the  caecum  and  are  immediately  taken  from  the  anus  by  the  lips. 
They  are  stored  in  the  stomach  and  later  mixed  with  further  food 
taken  (Fig.  435).  The  double  passage  of  the  food  is  necessary  for 
the  life  of  mice  and  guinea  pigs  as  well  as  rabbits.  The  animals  die 
in  two  to  three  weeks  if  prevented  from  reaching  the  anus.  The  moist 
pellets  probably  contain  the  metabolites  that  have  been  produced  by 
breakdown  of  cellulose  by  the  bacteria  of  the  caecum,  wrhich  cannot 
be  absorbed  by  the  organ  itself. 

Rabbits  and  hares  have  characteristically  developed  the  hind  legs 
for  a  jumping  method  of  locomotion  and  there  has  been  a  reduction 
of  the  tail.  The  rabbits  show  a  number  of  specializations  for  burrow- 
ing life.  They  are  among  the  most  successful  of  all  mammals,  especially 
in  the  Holarctic  region,  but  have  made  relatively  little  progress  in 
Africa  or  South  America.  Their  enormous  spread  in  Australia  since 
introduction  by  man  in  the  eighteenth  century  shows  how  accidental 
limitations  of  access,  and  their  alteration,  affect  the  distribution  of 
animal  life. 

Fossil  lagomorphs,  quite  like  modern  hares  and  rabbits,  are  found 
back  to  the  Oligocene.  Few  remains  are  known  from  the  Eocene,  but 
there  is  evidence  that  the  type  was  already  distinct  in  the  Palaeocene 
and  has  persisted  with  relatively  little  change  ever  since. 

5.  Fluctuations  in  numbers  of  mammals 

Fluctuation  in  numbers  is  characteristic  of  many  rodents  and  other 
small  mammals.  The  phenomenon  is  usually  first  recorded  as  a 
'plague'  of  the  rats,  mice,  voles,  or  rabbits,  and  these  may  be  cases  of 
local  and  sporadic  abundance.  Study  of  some  species  has  shown,  how- 
ever, that  there  are  rather  regular  cyclical  fluctuations  in  numbers, 


664  RODENTS   AND    RABBITS  xxv.  5 

extending  over  many  years.  Thus  figures  for  the  furs  collected  by 
trappers  for  the  Hudson  Bay  Company  enable  the  variations  in  numbers 
of  the  varying  hare  to  be  followed  back  to  1850  (Fig.  436).  The  cycle 
is  surprisingly  regular,  with  a  period  of  9-7  years.  During  the  periods 
of  abundance  of  the  hares  the  mammal  and  bird  predators  of  these  also 
increase  and  fall  off  a  little  later  than  the  herbivore  populations, 
changes  in  food  taken  by  the  predators  producing  all  sorts  of  secondary 
effects  on  the  animals  of  the  area. 


160,000 
1-1 

j$   120,000 
0    80,000 


3   40,000 


1850      1860       1870       1880 


1890       1900 
Year 


1910        1920        1930       1940 


1890       1900 
Year 


1930      1940 


Fig.  436.  Fluctuations  in  numbers  of  varying  hares  (above),  and  lynx  (below). 

Estimated  from  the  Hudson  Bay  Company's  fur  returns.  (From  W.  J.  Hamilton, 

American  Mammals,  McGraw  Hill  Book  Company.  After  MacLulich.) 


The  existence  of  these  fluctuations  is  striking  evidence  that  animal 
populations  are  not  maintained  in  any  stable  equilibrium.  It  is  often 
suggested  that  the  cycles  depend  on  changes  in  the  physical  conditions, 
for  instance,  on  the  sunspot  cycles,  but  no  close  correspondences  have 
been  discovered.  The  sunspot  cycle  has  a  period  of  1 1  -i  years,  whereas 
rodent  and  lagomorph  cycles  varying  from  the  9-7  years  for  the  hares 
to  5  years  for  lemmings  and  3  for  voles  have  been  recorded.  Changes 
in  the  amount  of  solar  radiation  no  doubt  produce  considerable  effects 
on  the  animals.  There  is  some  evidence  for  a  direct  effect  of  diet 
increasing  the  fertility.  In  South  America  plagues  of  rats  have  been 
observed  to  coincide  with  abundance  of  bamboos.  But  it  seems  likely 
that  the  cycles  of  numbers  depend  on  the  particular  balances  set  up 
within  the  animal  communities.  These  presumably  depend  on  the 
interactions  of  the  reproductive  pressures  of  the  plants,  herbivores, 
carnivores,  and  parasites,  and  it  is  easy  to  believe  that  in  some  condi- 


xxv.  s  FLUCTUATIONS    IN    NUMBERS  665 

tions  these  factors,  either  alone  or  in  association  with  cycles  of  solar 
radiation  or  other  climatic  factors,  would  produce  an  oscillatory 
system. 

When  the  numbers  are  at  a  maximum  the  animals  show  unusual 
behaviour  patterns,  including  migration,  and  may  enter  into  a  patho- 
logical state,  becoming  cold  and  torpid  and  with  a  very  low  blood- 
sugar  content.  Probably  the  pressure  of  competition  and  lack  of  food 
operates  on  the  hypophyso-adrenal  system  to  produce  a  state  of  shock. 
It  is  this,  rather  than  disease  or  predators,  that  finally  reduces  the 
numbers. 

Such  phenomena  are  probably  not  peculiar  to  small  mammals,  but 
appear  markedly  in  them  because  the  rapid  breeding  and  short  life 
provide  cycles  of  relatively  short  period.  The  facts  are  all  consistent 
with  the  interpretation  already  reached  that  the  control  of  animal 
populations  depends  very  largely  on  the  interaction  of  biotic  factors. 
This  continual  pressure  of  the  animals  on  each  other  is  probably 
the  main  factor  responsible  for  the  great  variations  in  the  charac- 
teristics of  animal  populations  in  different  parts  of  their  range,  which 
is  found  wherever  sufficiently  careful  study  is  undertaken.  This 
variation  in  turn  leads  to  the  phenomenon  of  organic  evolution  and 
the  continual  replacement  of  types  by  their  descendants,  which  appears 
so  clearly  as  one  follows  the  history  of  the  vertebrates. 


XXVI 

WHALES 

Cohort  3.  Mutica 
Order  Cetacea 
^Suborder  1.  Archaeoceti.  Eocene-Miocene 

*Protocetus,  Eocene;  *Basilosaurus  (=  *Zeuglodon),  Eocene 
Suborder  2.  Odontoceti.  Toothed  whales.  Eocene-Recent 
*Superfamily  1.  Squalodontoidea.  Eocene-Miocene 

*Squalodo?i,  Miocene 
Superfamily  2.  Platanistoidea.  River  dolphins.  Miocene-Recent 

Platanista,  Ganges  dolphin,  Recent 
Superfamily  3.  Physeteroidea.  Miocene-Recent 
Hyperoodon,    bottle-nosed    whale,    N.    Atlantic,    Antarctic; 
Physeter,  sperm  whale,  all  oceans 
Superfamily  4.  Delphinoidea.  Miocene-Recent 
Mo?wdon,  narwhal,  Arctic;  Delphinus,  dolphin,  all  oceans; 
Phocaena,  porpoise,  all  oceans 
Suborder  3.  Mysticeti.  Baleen  whales.  Oligocene-Recent 

Balaenoptera,    rorqual,    all    oceans;    Balaena,    right    whale, 
temperate  and  polar  seas 

The  whales  are  a  successful  set  of  populations  of  aquatic,  carnivorous 
mammals,  which  diverged  from  the  eutherian  stock,  possibly  from  the 
creodont  branch,  at  a  very  remote  date.  Their  specializations  for 
aquatic  life  involve  divergences  from  the  typical  mammalian  plan 
greater  than  those  found  in  any  other  order,  and  their  organization 
shows  in  a  remarkable  way  the  effects  of  habit  of  life  and  environment. 
In  many  respects  the  whales  have  reverted  to  the  characteristics  of  a 
fish  form  of  life,  most  noticeably  in  the  body  shape,  with  elongated 
head,  no  neck,  and  tapering  'streamlined'  body.  In  terrestrial 
mammals  the  air  resistance  is  not  a  serious  factor  and  the  body  shape 
does  not  conform  to  it,  but  in  water  it  becomes  of  first  importance. 

The  swimming  mechanism  depends  on  up-and-down  oscillations 
of  the  flukes  and  tail  stock,  and  the  efficiency  of  the  system  is  shown 
by  Gray's  demonstration  that  the  power  necessary  to  drag  a  wooden 
model  of  a  dolphin  through  the  water  with  the  speed  of  the  animal 
would  necessitate  a  horse-power  in  the  muscles  several  times  greater 
than  that  of  any  known  mammal.  Probably  in  life  the  accommoda- 


xxvi  MOVEMENT  667 

tion  of  the  skin  by  deformation  absorbs  part  of  the  turbulence  energy 
and  reduces  drag.  The  surface  is  completely  smoothed  off  by  the  loss 
of  all  hair,  except  for  a  few  sensory  bristles  round  the  snout  in  some 
species.  There  is  a  thick  layer  of  dermal  fat  (blubber),  which,  besides 
acting  as  a  heat  insulator,  may  also  provide  a  reservoir  of  food  and 
perhaps,  when  metabolized,  of  water.  The  fat  also  reduces  the  specific 
gravity  of  the  animal  and  perhaps  provides  an  elastic  covering  to  allow 
for  changes  in  volume  during  deep  diving.  There  are  no  glands  in  the 
skin. 

The  propulsive  thrust  comes  largely  from  the  horizontally  placed 
tail  flukes,  which  constitute  a  cambered  aerofoil  that  is  moved  up  and 
down  by  the  tail  muscles.  These  consist  of  upper  and  lower  sets  of 
longitudinal  fibres  inserted  in  the  tail-stock  vertebrae  by  means  of 
long  tendons  from  muscles  originating  from  more  forwardly  situated 
vertebrae.  More  caudally  placed  muscles  inserted  on  the  hindmost 
vertebrae  in  the  tail  flukes  allow  movement  of  the  flukes  relative  to  the 
tail  stock  to  produce  the  forward  thrust.  The  arrangement  allows  the 
whole  tail  to  be  bent  up  and  down  on  the  body,  while  the  fluke  is  bent 
relative  to  the  tail  and  produces  the  thrust.  Stability  is  provided  by  the 
paddle-like  fore-limbs,  and  there  is  often  a  large  dorsal  fin,  especially 
in  fast  swimmers  such  as  the  killer- whales  (Oirinus).  The  plasticity  of 
animal  form  is  shown  by  the  fact  that  the  flipper  is  a  modification  of 
the  ambulatory  fore-limb,  whereas  the  dorsal  fins  and  tail  flukes  are 
'neomorphs',  folds  of  skin  with  no  skeletal  support,  radical  innovations 
indeed:  it  is  not  easy  to  imagine  by  what  alterations  of  habit  an  early 
eutherian  could  come  to  develop  fins  out  of  such  folds  of  skin.  Equally 
remarkable  has  been  the  disappearance  of  the  hind-limb,  leaving  no 
external  trace  and  internally  only  paired  pelvic  vestiges  with  addi- 
tional bony  nodules  in  some  whales  representing  limb  bones.  These 
rods  serve  as  attachments  for  the  corpora  cavernosa  of  the  penis  and 
may  therefore  be  regarded  as  ischia. 

The  vertebral  column  (Fig.  437)  carries  no  weight  except  when  the 
animal  jumps  out  of  the  water.  In  the  vertebral  column  the  zyga- 
pophyses  are  reduced,  and  the  centra  are  well  developed  to  make  a 
compression  strut,  as  in  fishes.  The  vertebral  epiphyses  remain  separate 
to  a  late  age.  The  neural  spines  and  transverse  processes  are  well 
developed  for  the  attachment  of  muscles  in  a  typically  mammalian 
manner  giving  a  dorso-ventral  movement  of  the  body,  this  being  in 
contrast  with  the  lateral  movement  produced  by  the  segmental  myo- 
tome arrangement  of  fishes.  The  neck  is  very  short  and  the  cervical 
vertebrae  partly  or  wholly  fused  together.  The  ribs,  as  in  other  aquatic 


668  WHALES  xxvi 

vertebrates,  are  rounded  and  mobile;  they  are  the  chief  agents  of 
respiration,  the  diaphragm  containing  little  muscle. 

In  the  fore-limb  the  humerus  is  short,  the  elbow-joint  hardly 
mobile,  and  the  hand  increased  in  length  and  sometimes  expanded 
(right  whales,  killers,  river  dolphins).  The  number  of  fingers  is  often 
reduced  to  four;  the  phalanges  of  some  of  the  digits  may  be  con- 
siderably increased  in  number  (hyperphalangy).  The  scapula  is 
flattened  and  there  is  no  clavicle. 

Some  striking  modifications  are  seen  in  the  head.  The  skull  shows  a 
curious  telescoping  of  the  bones  over  each  other.  The  maxilla  of 
toothed  cetaceans  extends  above  the  frontal,  combining  with  the  latter 
to  make  a  roof  to  the  temporal  fossa.  Thus  the  maxilla  almost  reaches 
the  supra-occipital.  In  baleen  whales  the  backward  prolongation  of 
the  maxilla  is  mainly  below  the  supraorbital  process  of  the  frontal, 
although  there  is  a  medial  process  extending  dorsally  towards  the 
supra-occipital.  This  telescoping  occurs  only  towards  the  end  of  foetal 
life.  A  further  curious  feature  is  that  the  skull  in  the  toothed  whales  is 
asymmetrical,  the  vertex  being  shifted  over  to  the  left  side;  no  satis- 
factory explanation  for  this  phenomenon  has  yet  been  offered.  The 
jaws  are  always  greatly  elongated,  in  the  Greenland  right  whales  they 
make  up  one-third  of  the  total  body  length.  The  masticatory  muscles 
and  the  coronoid  process  are  reduced,  the  latter  most  extremely  in 
Balaena  in  which  it  is  distinguished  only  as  an  inconspicuous  ridge. 

Whales  are  microsmatic  or  even  in  some  species  anosmatic  (with  no 
olfactory  nerve).  The  brain-case  is  therefore  short  and  rounded  while 
the  nostrils  have  moved  backwards  and  open  upwards.  The  nasal 
bones  have  become  reduced  in  length  and  no  longer  roof  over  the 
nasal  cavity.  The  process  has  proceeded  somewhat  differently  in  the 
toothed  and  in  the  whalebone  whales.  The  auditory  region  is  much 
modified  and  the  whole  petrosal  bone  is  free  from  the  rest  of  the  skull ; 
there  is  a  large  tympanic  bulla,  fused  with  the  petrosal.  Extensions  of 
the  middle  ear  cavity  form  pneumatic  sacs,  below  the  base  of  the  skull, 
which  serve  to  insulate  sound  and  equilibrate  the  varying  pressures 
experienced  under  water. 

The  feeding  arrangements  provide  further  special  features.  Many 
of  the  toothed  whales,  such  as  the  porpoises  and  dolphins,  eat  mainly 
fish  and  the  teeth  form  a  row  of  numerous  (65/58),  similar  peg-like 
structures,  usually  in  both  jaws.  With  elongation  of  the  jaws  the 
masticatory  function  of  the  teeth  has  been  reduced  and  they  probably 
serve  to  hold  the  prey.  Orcinus,  the  killer-whale,  has  large  powerful 
jaws  and  teeth  and  its  diet  includes  dolphins,  birds,  seals,  and  the 


xxvi  FEEDING  669 

flesh  of  large  whales.  Squids  are  also  eaten,  but  in  species  that  feed 
predominantly  on  these  there  is  some  tendency  to  a  reduction  in  the 
number  of  teeth.  For  example,  in  the  sperm  whale  functional  teeth 
are  confined  to  the  lower  jaw  and  in  the  bottle-nosed  or  beaked  whales 
only  one  or  two  pairs  of  teeth  are  visible.  In  whalebone  whales 
(Mysticeti),  however,  there  are  teeth  only  in  the  foetus;  the  food  is 
plankton.  This  is  collected  by  the  fringed  baleen,  which  consists  of 
rows  of  transverse  plates  of  keratin.  The  tongue  of  the  right  whales  is 
powerfully  muscular  and  forces  the  water  from  the  mouth.  In  the 


Fig.  437.  Skeleton  and  outline  of  the  right  whale  {Balaena). 
(After  British  Museum  Guide.) 

rorquals  the  same  purpose  is  achieved  by  the  contraction  of  sub- 
cutaneous muscles  associated  with  the  external  throat  grooving.  The 
shrimp-like  'krill'  {Euphausia)  and  other  organisms  are  then  swallowed 
through  the  narrow  oesophagus  to  a  special  stomach  with  several 
chambers.  The  first  stomach  is  non-glandular  and  is  a  crop-like 
oesophageal  specialization,  the  hindmost  stomach  into  which  the  bile 
and  pancreatic  ducts  open  is  a  specialized  intestinal  cavity.  The  in- 
testine may  be  as  much  as  sixteen  times  as  long  as  the  body. 

Both  types  of  nutrition  are  evidently  efficient  and  the  whales  are 
abundant  and  of  course  very  large.  It  is  more  easy  to  see  the  advantage 
of  large  size  for  aquatic  than  for  land  animals.  There  are  no  problems 
of  support  of  weight,  and  on  the  other  hand  a  great  premium  is  placed 
on  large  size  by  the  fact  that  skin  friction  is  thereby  relatively  reduced, 
and  this,  which  forms  but  a  small  element  in  the  work  to  be  done  by 
a  land  animal,  must  be  important  in  the  water.  Further,  the  heat  loss 
is  greatly  reduced  by  the  size,  and  this  may  be  a  large  factor  in  cold 
water,  with  its  high  thermal  conductivity  (Parry,  1949).  However,  it 
has  also  been  claimed  that  downward  temperature  regulation  may  be 
a  problem  and  that  the  flippers  and  fins  act  as  'radiators'. 

The  respiratory  system  shows  many  special  developments  in  the  air 
passages,  lungs,  and  nostrils.  There  are  valves  for  closing  the  nostrils 


670  WHALES  xxvi 

during  diving,  and  special  cartilaginous  rings  and  muscles  in  the 
bronchioles.  The  epiglottis  is  extended  as  a  tube  inserted  into  the 
posterior  narial  cavity  so  that  an  uninterrupted  air  passage  is  provided 
from  the  blow-hole  to  the  lungs.  The  very  elastic  and  extensible  lungs 
can  thus  be  quickly  filled  with  large  volumes  of  air.  In  spite  of  the 
enlarged  tracheo-bronchial  tree  the  respiratory  surface  is  small,  but 
there  are  special  arrangements  of  valves  and  venous  plexuses  to  ensure 
economical  distribution  of  the  air  and  blood.  Some  whales  can  remain 
submerged  for  half  an  hour  and  reach  depths  of  500  metres  or  more. 
There  is  relatively  little  experimental  evidence  about  the  means  by 
which  they  obtain  oxygen  and  resist  compression.  The  whole  arrange- 
ment ensures  the  taking  down  of  a  maximum  of  air.  There  is  rapid 
ventilation  while  on  the  surface,  followed  by  slower  heart-beat  and 
presumably  reduced  tissue  respiration  while  below,  so  that  the  whale 
can  take  down  enough  oxygen  to  last  throughout  its  dives.  However, 
the  heart  rate  slows  only  to  one-half  in  the  only  cetacean  fully 
investigated  (Tursiops)  and  there  is  no  evidence  about  retention  in 
venous  sinuses  or  other  means  of  reducing  circulation  such  as  are 
found  in  seals  (p.  692).  The  respiratory  centre  in  the  medulla  has  a 
lesser  sensitivity  to  C02  than  in  land  animals. 

Besides  the  air  in  the  lungs  there  may  also  be  some  provision  for 
storage  of  extra  oxygen  in  the  large  blood-volume  of  the  retia  mira- 
bilia,  networks  of  blood-vessels,  which  abound  throughout  the  body, 
especially  in  the  thorax.  However,  the  function  of  the  retia  mirabilia 
is  probablv  connected  with  the  accommodation  of  the  animal  to  varying 
hydrostatic  pressures.  They  expand  and  contract  to  occupy  the  space 
in  the  thorax  as  the  air  in  the  lung  is  diminished  or  increased  as  the 
animal  rises  or  descends  while  swimming.  There  is  much  myoglobin 
in  the  muscles.  The  brain  is  supplied  with  blood  entirely  from  menin- 
geal arteries,  which  draw  on  the  thoracic  retia.  The  basilar  artery  and 
intracranial  carotid  close  early. 

No  doubt  the  metabolism  is  also  arranged  to  allow  accumulation  of 
a  high  oxygen  debt,  but  the  special  metabolic  peculiarities  that  allow 
for  this  are  not  known.  It  is  perhaps  not  necessary  for  whales  to  have 
a  special  defence  against  caisson  sickness  if  they  are  using  oxygen 
reserves.  There  is  no  continuous  addition  to  the  nitrogen  dissolved  in 
the  blood  such  as  would  lead  to  the  formation  of  the  bubbles  that 
occurs  when  miners  or  divers  rise  suddenly  after  breathing  air  at  great 
depths.  The  sudden  expiration  on  surfacing  produces  a  cloud  of 
foetid  vapour,  the  blow.  This  is  generally  supposed  to  be  due  to 
condensation,  but  it  occurs  even  if  the  air  is  hot. 


xxvi  RECEPTORS  671 

The  brain  is  absolutely  larger  in  whales  than  in  any  other  animals 
(up  to  7,000  g),  and  the  hemispheres  are  elaborately  folded.  The 
cerebellum  is  very  large.  Little  is  known  in  detail  about  the  sensory 
equipment  or  powers  of  the  animals.  The  eyes  are  small  (vestigial  in 
Platanista)  and  in  all  whales  much  modified  for  aquatic  life  and  diving. 
The  cornea  is  more  flattened  than  in  subaerial  mammals,  and  the  lens 
rounded;  in  these  respects  the  whales  have  returned  to  fish-like  condi- 
tions. The  whale  eye  is  enclosed  in  a  thickened  sclera  and  further  has 
special  lid  muscles.  The  tear  glands  and  their  duct  are  absent;  instead, 
the  surface  of  the  eye  is  protected  by  a  special  fatty  secretion  of  the 
Harderian  glands. 

The  ear  provides  the  major  receptor  system.  The  auditory  nerve, 
lateral  lemniscus,  superior  olive,  inferior  colliculus,  and  medial  genicu- 
late are  all  very  large.  Presumably  much  of  the  cortex  serves  the  sense 
of  hearing.  The  apparatus  concerned  with  reception  of  air-borne 
vibrations  is  reduced.  The  external  opening  is  very  small  and  the 
long  meatus  is  often  filled  with  secretion.  The  tympanum  is  thick  and 
ligamentous.  It  is  to  a  normal  ear  drum  as  a  closed  umbrella  is  to  an 
open  one.  The  tip  of  the  tympanic  'ligament'  is  attached  only  to  the 
tip  of  manubrium  mallei.  The  distal  end  of  the  processus  gracilis  of 
the  malleus  is  fused  to  the  adjoining  bone  of  the  tympanic  bulla.  The 
ossicles  have  articulations  with  one  another  as  in  terrestrial  mammals 
and  the  tip  of  the  stapes  is  movable  in  the  foramen  ovale. 

The  petro-tympanic  bone  is  free  from  the  skull,  rests  on  a  thick 
fibrous  pad  and  is  otherwise  almost  completely  enveloped  in  a  system 
of  foam-filled  air  sinuses.  The  whole  arrangement  is  believed  to  be 
designed  to  isolate  the  essential  organ  of  hearing  from  vibrations 
extraneous  to  those  reaching  it  by  means  of  the  meatus  and  auditory 
ossicles,  and  so  to  provide  the  means  for  directional  hearing. 

In  the  ears  of  terrestrial  mammals  the  ossicles  provide  an  arrange- 
ment for  converting  the  relatively  large  displacement  at  low  amplitudes 
of  air-borne  waves  at  the  tympanum  to  waves  with  a  sixtyfold  greater 
pressure  amplitude  at  the  fenestra  ovalis.  The  physical  properties  of 
water-borne  vibrations,  however,  differ  markedly  from  those  that  are 
air-borne.  The  pressure  amplitude  for  the  same  intensity  and  fre- 
quency of  water-borne  and  air-borne  sound  is  in  the  ratio  61 : 1,  and 
the  displacement  amplitude  1 :6i.  It  can  be  shown  that  adjustments  of 
amplitude  and  pressure  to  values  normally  experienced  in  the  cochlea 
by  terrestrial  mammals  are  achieved  in  cetaceans  by  the  modifications 
of  the  middle  ear  mechanism  (Fraser  and  Purves,  1959). 

Whales  emit  a  variety  of  sounds  but  little  is  known  of  their  method 


672 


WHALES 


of  production  or  use.  Tursiops  in  a  tank  recognize  the  sex  of  a  new 
arrival  in  another  tank,  out  of  sight.  Several  such  social  reactions  have 
been  reported,  for  example,  between  mother  and  young.  Tursiops  can 
also  avoid  obstacles  in  the  dusk  and  since  they  react  to  frequencies  up 
to  120  kc/sec  it  is  possible  that  they  emit  these  for  echolocation. 


Fig.  438.  Blue  whale,  Balaenoptera.  (After  Mackintosh  and  Wheeler.) 


Fig.  439.  Killer-whale,  Orcinus.  (After  British  Museum  Guide.) 


Fig.  440.  Porpoise,  Phocaena.  (After  British  Museum  Guide.) 


Fig.  441.  Dolphin,  Delphinus.  (After  British  Museum  Guide.) 

The  head  of  odontocetes  carries  an  organ  known  as  the  'melon', 
which  is  possibly  a  receptor.  It  is  a  mass  of  fat  in  front  of  the  nostril, 
traversed  by  muscle-fibres  and  richly  innervated  by  the  trigeminal.  It 
may  serve  to  detect  pressure  changes  in  the  water,  substituting  for  the 
vibrissae  of  seals.  In  the  sperm  whale  it  is  enormous  (p.  674). 

The  behaviour  of  whales  is  undoubtedly  elaborate,  involving  social 
life,  communication  by  sound,  and  probably  much  learning.  There  is 
cooperation  between  individuals  in  helping  to  keep  a  wounded  com- 
panion or  a  new-born  at  the  surface.  Play  is  common  and  rhythmical 


xxvi  REPRODUCTION  673 

'dancing'  has  been  observed  and  also  homosexual  behaviour,  in  cap- 
tivity. Many  species  migrate,  for  example,  the  humpbacks  (Megaptera) 
and  others  spend  the  summer  in  the  Antarctic  feeding  on  krill  and 
then  come  north  to  tropical  waters  to  breed. 

The  reproduction  shows  various  modifications  for  aquatic  life.  The 
testes  do  not  descend  into  sacs,  but  to  a  position  just  below  the  body 
surface.  The  penis  is  very  long,  and  curled  when  not  erect.  The  uterus 
is  bicornuate,  but  only  one  young  is  carried  and  is  retained  for  a  long 
time  (more  than  a  year  in  large  whales),  so  that  it  is  as  much  as  a  third 
the  length  of  the  mother  at  birth.  The  placenta  is  diffuse  but  with  a  few 
villosities  like  cotyledons.  Its  structure  is  epitheliochorial  and  there  is 
a  large  allantois.  There  is  a  pair  of  teats  in  the  inguinal  region  and  the 
mammary  glands  are  provided  with  a  special  receptacle  and  muscle 
so  that  milk  is  pumped  into  the  mouth  of  the  young.  Some  species  of 
dolphins  migrate  to  shallow  protected  water  at  the  time  of  parturition. 

It  is  clear  that  many  factors  have  collaborated  to  concentrate  the 
biomass  of  whale  life  into  large  units.  Indeed,  whales  include  the 
largest  known  animals,  either  fossil  or  recent.  The  blue  whale, 
Balaenoptera  musculus  (Fig.  438),  reaches  nearly  150  tons,  with  a 
length  of  100  ft.  This  is  one  of  the  whalebone  whales,  which  are  in 
general  larger  than  the  odontocetes,  perhaps  because  of  the  immense 
sources  of  food  directly  available  in  the  plankton;  they  have  grown 
fat  by  eliminating  the  'middle-men'  upon  which  all  toothed  whales 
must  feed.  These  mysticetes  appeared  in  the  Oligocene  and  radiated 
in  the  Miocene  and  since  into  a  relatively  small  number  of  types,  all 
of  large  size.  Balaena,  the  right  whale  of  the  Arctic,  is  now  very  rare. 
The  chief  modern  prey  of  the  whalers  are  the  fin  whales  {Balaenoptera 
physalus)  of  the  Antarctic. 

The  odontocete  whales  are  a  more  varied  group;  their  history  can 
be  traced  back  to  the  late  Eocene.  The  squalodonts  of  the  Oligocene 
and  Miocene  were  like  the  porpoises,  but  with  triangular  teeth.  Most 
of  them  disappeared  in  the  Miocene,  but  the  river-porpoise  Platanista 
of  the  Ganges,  and  related  forms  in  the  Amazon  and  in  China  may  be 
descendants.  The  modern  porpoises  (Delphinoidea)  are  a  very  success- 
ful and  numerous  group  of  relatively  small  animals,  with  a  dorsal  fin 
and  teeth  in  both  jaws.  They  are  all  active  predators,  but  the  habits  vary 
from  those  of  the  killer-whale  Orchitis  (Fig.  439),  which  is  a  fierce  and 
cunning  hunter,  attacking  even  the  largest  whales,  to  the  omnivorous 
porpoise  Phocaena  (Fig.  440),  whose  food  includes  Crustacea  as  well  as 
fishes  and  cephalopods.  This  is  the  commonest  and  smallest  British 
cetacean,  the  largest  individuals  reaching  6  ft;  the  jaws  are  rather  short, 


674  WHALES  xxvi 

especially  the  upper  one,  and  the  teeth  are  spade-shaped.  The  true 
dolphins,  Delphinus  (Fig.  441),  are  larger  animals  (8  ft),  living  mostly 
on  fish  and  having  long,  many-toothed  jaws,  the  upper  forming  a  beak. 
They  are  very  fast  swimmers,  reaching  20  knots.  The  narwhal,  Monodon 
(Fig.  442),  is  a  large  delphinoid  (15  ft  long)  with  a  single  tooth,  usually 
the  left  upper  incisor,  remaining  in  the  male  and  growing  continually 


Fig.  442.  Narwhal,  Monodon.  (After  Norman  and  Fraser.) 


Fig.  443.  Sperm  whale,  Physeter.  (After  Flower  and  Lydekker, 
Mammals,  Living  and  Extinct,  A.  &  C.  Black,  Ltd.) 


Fig.  444.  Bottle-nosed  whale,  Hyperoodon.  (After  Norman  and  Fraser.) 

to  make  the  spirally  twisted  horn,  up  to  9  feet  long,  whose  use  is  not 
known.  The  female  retains  a  pair  of  small  incisors  buried  in  the 
premaxillae. 

In  the  sperm  whales,  Physeteroidea  (Fig.  443),  the  rostrum  is  over- 
laid by  an  enormous  reservoir  containing  spermaceti,  a  pure  white 
waxy  liquid  solidifying  in  air.  Either  this,  or  some  other  feature, 
enables  them  to  reach  a  larger  size  than  other  toothed  whales  (60  It). 
Sperm  whales  have  functional  teeth  only  in  the  lower  jaw  and  vestigial 
ones  in  the  upper.  They  feed  on  cephalopods,  the  remains  of  whose 
jaws,  combined  with  solid  secretions  to  make  stones  in  the  intestine, 
form  the  substance  ambergris  used  as  an  absorbent  in  the  manufacture 
of  scent.  The  bottle-nosed  whales,  such  as  Hyperoodon  (Fig.  444)  of 
polar  seas,  are  also  cephalopod  feeders  and  reach  30  ft  in  length. 


XXVI 


PRIMITIVE   WHALES  675 

The  whales  known  from  the  Eocene  were  different  from  either  of 
the  modern  groups  and  are  placed  in  a  separate  suborder  *Archaeoceti 
(Fig.  445).  The  body  was  very  long  (up  to  70  ft)  and  apparently 
thinner  than  in  modern  whales,  suggesting  a  sea-serpent  form, 
probably  of  low  swimming  efficiency.  The  hind  legs  had  already  disap- 
peared, though  vestiges  of  their  skeleton  remained.  The  skull  was 


Fig.  445.  Change  in  position  of  the  blow-hole  (nos.)  during  the  evolution  of  whales.  The 
two  upper  figures  show  the  condition  in  the  Eocene  *Basilosawus,  the  lower  figures  a 

Miocene  squalodont. 

/.  frontal;  m.  maxilla;  n.  nasal;  />.  parietal;  pm.  premaxilla;  sq.  squamosal.  (Modified  after  Romer, 
Man  and  the  Vertebrates,  University  of  Chicago  Press.) 

long,  the  nostril  had  moved  some  way  back.  The  teeth  were  of  the 
normal  mammalian  number,  44,  and  were  heterodont.  The  molars  had 
sharp  crenated  edges,  as  in  other  fish-eaters,  and  the  animals  were 
obviously  carnivorous,  suggesting  a  possible  creodont  ancestry.  Casts 
of  the  brain  show  large  olfactory  centres  but  a  small,  little  folded, 
cortex.  The  cerebellum  was  enormous  (if  it  has  been  correctly  recon- 
structed). 

These  animals,  such  as  *Basilosaiirns  (=  *Zeuglodon)y  had  already 
developed  a  long  way  from  the  main  eutherian  stock  by  middle  Eocene 
times.  This  is  an  example  of  relatively  rapid  evolutionary  change;  it 
may  be  presumed  that  their  ancestors  had  been  in  the  condition  of 
small  insectivores  not  much  later  than  the  end  of  the  Cretaceous,  at 
the  most  20  million  years  earlier.  The  basilosaur  type  persisted  to  the 
Miocene,  but  the  exact  connexions  with  the  two  modern  sorts  of 


676  WHALES  xxvi 

whale  are  not  clear.  Whales  have  been  abundant  throughout  the 
Tertiary,  but  there  is  not  yet  sufficient  evidence  available  to  recon- 
struct their  full  phylogenetic  history.  In  broad  outlines,  however,  it 
is  clear  that  there  has  been  a  progressive  adoption  of  features  suitable 
for  aquatic  life,  the  long-bodied,  heterodont  basilosaurs  giving  place 
to  the  shorter,  stream-lined  modern  whales,  provided  with  suitable 
stabilizing  fins  and  with  the  mouth  highly  specialized  for  eating  fish, 
cephalopods,  or  plankton.  It  is  impossible  to  say  whether  the  changing 
of  the  populations  is  due  to  indirect  influences  of  climatic  changes  or 
to  factors  within  the  animal  populations  themselves.  The  course  of 
whale  evolution,  like  that  of  teleosts,  appears  to  have  produced  increas- 
ing efficiency  within  a  single  habitat,  rather  than  a  progressive  coloniza- 
tion of  new  fields;  but  this  appearance  may  be  only  a  reflection  of  our 
ignorance  and  lack  of  knowledge  of  the  varied  and  changing  condition 
of  the  sea. 


XXVII 

CARNIVORES 

1.  Affinities  of  carnivores  and  ungulates  :  Cohort  Ferungulata 

The  union  of  the  modern  carnivores  and  hoofed  animals  in  a  single 
cohort  Ferungulata  is  based  on  palaeontological  work  that  has  shown 
how  both  groups,  together  with  some  isolated  surviving  types  such 
as  the  elephants  and  sea-cows,  and  many  other  forms  now  extinct, 
all  arose  from  a  common  population  in  Palaeocene  times.  The 
ungulates  have  been  grouped  together  for  a  long  time  because  of  their 
obvious  common  characteristics  of  herbivorous  diet  and  hoofed  feet, 
but  it  is  clear  that  'ungulates'  include  two  very  different  sorts  of 
creature,  the  even-toed  artiodactyls,  such  as  the  pigs,  sheep,  and  cows, 
and  the  uneven-toed  perissodactyls,  the  rhinoceroses  and  horses. 
The  latter  can  be  traced  backwards  to  a  very  ancient  group,  the 
Condylarthra  of  the  Palaeocene  and  Eocene,  and  they  were  therefore 
for  some  time  placed  rather  widely  apart  from  the  Artiodactyla,  whose 
origin  was  mysterious.  It  has  now  been  shown,  however,  that  there 
is  a  resemblance  between  the  Eocene  artiodactyls  and  some  of  the 
creodonts,  animals  that  were  also  the  ancestors  of  the  modern  Car- 
nivora.  The  creodonts  and  condylarths  are  in  many  ways  alike,  and  it 
now  seems  probable  that  the  whole  group  makes  a  single  unit,  diverging 
first  from  the  insectivorous  eutherian  ancestral  population  in  the  late 
Cretaceous  or  Palaeocene,  probably  as  a  carnivorous  stock.  Some 
members  then  diverged  almost  at  once  to  make  the  condylarths, 
perhaps  from  a  stock  that  already  possessed  hoofs  and  then  proceeded 
later  to  produce  the  Artiodactyla  (Fig.  446). 

It  is  a  convenience  to  use  these  relationships  as  a  basis  for  classifica- 
tion, but  it  must  be  recognized  that  modern  carnivores  have  little 
more  in  common  with  ruminants  than  with,  say,  monkeys  or  rats. 
The  three  great  groups  that  make  up  the  Ferungulata  diverged  from 
each  other  only  a  short  time  after  their  common  stock  had  diverged 
from  that  of  the  other  mammals;  at  that  time  all  eutherians  were  so 
alike  that  we  should  probably  place  them  in  a  single  order  if  they  had 
left  no  descendants. 

The  Ferungulata  have  become  much  more  diversified  than  the 
other  cohorts  into  which  we  have  divided  the  Eutheria  and  we  have 
to  recognize  no  fewer  than  fifteen  orders  in  the  group.  It  is  therefore 


XXVII.   I- 


678  CARNIVORES 

convenient  to  make  further  subdivision  into  five  superorders.  The 
first  of  these,  Ferae,  makes  the  central  group,  including  the  Carnivora. 
The  second  superorder,  Protoungulata,  includes  the  earliest  ungulates, 
the  condylarths,  and  it  is  convenient  to  place  here  also  certain  early 
offshoots,  such  as  the  South  American  ungulates  and  one  living 
survivor,  the  aardvark.  The  third  superorder  is  known  as  Paenungulata 


PLEISTOC£NE 


FISSIPEDIA 


Fig.  446.  Chart  of  the  evolution  of  Carnivora. 


('near  ungulates')  and  includes  a  group  of  orders  with  rather  primitive 
organization,  most  of  them  extinct.  The  elephants,  hyraxes,  and  sea- 
cows  remain  as  isolated  vestiges  of  this  great  group,  which  included 
the  huge  pantodonts  and  dinocerates,  formerly  classed  together  as 
amblypods,  also  the  pyrotheres,  elephant-like  animals  from  South 
America,  and  the  embrithopods,  large,  horned  animals  from  Africa. 
The  fourth  superorder,  Mesaxonia,  includes  only  the  Perissodactyla, 
descended  from  the  condylarths,  while  the  fifth  superorder,  Paraxonia, 
contains  the  artiodactyls,  derived  a  little  later  from  the  condylarths. 
Of  all  this  assembly  of  varied  types  only  the  carnivores  and  ruminant 
artiodactyls  remain  successful  types  at  the  present  day,  abundant  in 
species  and  individuals,  the  remaining  orders  are  either  extinct  or  are 
represented  only  by  few  species. 


XXVII.  2  (679  ) 

2.  Classification 

Cohort  4.  Ferungulata 
Superorder  1.  Ferae 
Order  Carnivora 

*Suborder  1.  Creodonta.  Palaeocene-Pliocene.  Holarctic 

*Family  1.  Arctocyonidae.  Palaeocene-Eocene 

*Arctocyon,  Paleocene;  *Tricentes,  Palaeocene 
*Family  2.  Mesonychidae.  Palaeocene-Eocene 

*Mesonyx,  Eocene 
*Family  3.  Oxyaenidae.  Palaeocene  Eocene 

*Oxyaena,  Palaeocene-Eocene 
#Family  4.  Hyaenodontidae.  Eocene-Pliocene 

*Hyaenodon,  Eocene-Oligocene;  *Apataeluru$,  Eocene 

Suborder  2.  Fissipeda.  Palaeocene-Recent 
*Superfamily  1.  Miacoidea.  Palaeocene-Eocene,  Holarctic 
*Family  Miacidae 

*Miacis,  Eocene;  *Vulpavns,  Eocene 

Superfamily  2.  Canoidea 

Family  1.  Canidae.  Dogs.  Eocene-Recent 

Canis,  wolves,  dogs,  jackals,  Pliocene-Recent,  world  wide, 
but  not  originally  wild  in  S.  America  or  Australia ;  Vitlpes, 
fox,  Miocene-Recent,  Holarctic,  N.  Africa 
Family  2.  Ursidae.  Bears.  Miocene-Recent 
Ursiis,  bear,  Pliocene-Recent,  Holarctic 
Family  3.  Procyonidae.  Raccoons.  Miocene-Recent 

Procyon,  raccoon,  Pliocene-Recent;  N.  and  S.  America; 
Aihirus,  panda,  Recent,  Asia,  Ailuropoda,  giant  panda, 
Recent,  Asia 
Family  4.  Mustelidae.  Weasels.  Oligocene-Recent 

Mustela,  weasel,  ferret,  stoat,  Miocene-Recent,  Holarctic, 
S.  America,  N.  Africa;  Meles,  badger,  Pliocene-Recent, 
Eurasia;  Taxidea,  American  badger,  Pliocene-Recent, 
N.  America;  Mephitis,  skunk,  Recent,  N.  America; 
Lutra,  otter,  Pliocene-Recent,  Holarctic,  S.  America, 
Africa;  Maries,  marten,  Pliocene-Recent,  Holarctic 


680  CARNIVORES  xxvn.  2- 

2.  Classification  (cont.) 

Superfamily  3.  Feloidea 

Family   1.   Viverridae.   Civets  and   mongooses.   Oligocene- 
Recent 
Viverra,  civet,   Miocene-Recent,   Asia;   Herpestes,   mon- 
goose,  Oligocene-Recent,   Eurasia,   Africa,   and   intro- 
duced to  W.  Indies 
Family  2.  Hyaenidae.  Miocene-Recent.  Eurasia,  Africa 

Hyaena,  hyena,  Pliocene-Recent,  Asia,  Africa 
Family  3.  Felidae.  Cats.  Upper  Eocene-Recent 

Felis,  cats,  pumas,  ocelots,  leopards,  lions,  tigers,  jaguars, 
Pliocene-Recent,  world-wide;  *Hoplopho?iens,  sabre- 
tooth,  Oligocene-Miocene;  *Smihdon,  sabre-tooth,  Plei- 
stocene 

Suborder  3.  Pinnipedia 

Family  1.  Otariidae.  Eared  seals.  Miocene-Recent 

Eumetopias,  sea  lion,  Atlantic  and  Pacific 
Family  2.  Odobenidae.  Walruses.  Miocene-Recent 

Odobenas,  walrus,  Arctic 
Family  3.  Phocidae.  Seals.  Miocene-Recent 

Phoca,  seal,  Atlantic  and  Pacific;  Halichoerus,  grey  seal, 
N.  Atlantic. 

3.  Order  Carnivora 

The  earliest  Cretaceous  mammals  were  probably  insectivorous  and 
it  is  not  therefore  surprising  that  some  of  their  descendants  became 
flesh-eating;  indeed  it  is  curious  that  a  single  stock  has  provided 
nearly  all  the  hunters  found  among  the  mammals  ever  since,  though 
the  marsupials  have  produced  carnivorous  types  in  South  America 
and  Australasia.  It  is  difficult  to  see  why  carnivores  have  not  developed 
more  often  from  the  insectivoran  or  some  other  stock;  that  they  have 
not  done  so  may  remind  us  that  special  circumstances  are  necessary 
for  the  origin  even  of  a  type  for  which  a  means  of  life  would  seem  to  be 
readily  available. 

4.  The  Cats 

The  changes  that  convert  a  mammal  into  an  effective  hunter  occur  in 
many  parts  of  the  body,  without,  as  it  were,  radically  distorting  any. 
We  may  illustrate  this  by  considering  the  most  specialized  members 


xxvn.  4  THE   CATS  681 

of  the  group,  the  cats  (Fig.  447).  The  head  is  large,  with  long  ears, 
long  whiskers,  and  nose  with  many  turbinals.  The  brain  is  large,  the 
cerebral  hemispheres  overlap  the  cerebellum;  the  olfactory  centres  are 
large.  As  is  usual  with  carnivores,  behaviour  is  complicated;  in  order 
to  continue  pursuit  of  prey  that  cannot  be  seen,  or  perhaps  even 
smelt,  the  animals  learn  to  associate  the  presence  of  food  with  obscure 
clues  such  as  footmarks,  and  to  make  use  of  these  clues  they  must  lie  in 


Fig.  447.  Skeleton  of  the  cat  (Felis). 

wait  for  the  prey.  All  of  this  involves  an  elaborate  balance  of  internal 
motivation  with  activity  and  restraint.  This  power  of  'abstraction'  of 
ultimate  satisfaction  from  the  immediate  situation  may  perhaps  be 
associated  with  the  familiar  play  of  the  kitten  or  the  less  edifying 
treatment  of  a  captured  mouse  by  an  adult  cat. 

Social  or  family  groups  are  commonly  well  marked  in  carnivores  and 
there  are  usually  characteristic  odours  for  recognition,  often  associated 
with  large  anal  glands,  especially  well  known  as  producers  of  civet  and 
the  'poison'  of  the  skunks.  The  back  of  the  head  is  enlarged  to  take 
the  brain  and  there  is  a  well-developed  snout  for  the  nose,  but  the  face 
is  nevertheless  short,  and  it  is  characteristic  of  the  specialized  carni- 
vores that  the  tooth-row  is  shortened,  developed  especially  at  the 
front  end,  producing  the  incisors  for  piercing,  canines  for  tearing, 
and  premolars  and  anterior  molars  for  cutting.  In  contrast  to  the 
ungulate  type  of  dentition  the  hinder  molars,  not  being  needed  for 
grinding,  are  reduced.  In  the  cats,  as  in  all  modern  carnivores  except 


682  CARNIVORES  xxvn.  4- 

seals,  the  teeth  most  favourably  placed  for  biting  by  their  position 
relative  to  the  jaw  muscles,  namely,  the  last  upper  premolar  and  first 
lower  molar  are  specially  developed  into  cutting-blades,  the  carnas- 
sials.  This  is  done  by  formation  of  a  ridge  along  the  outer  side  of  the 
upper  molar,  the  paracone  and  metacone  making  a  single  cutting- 
edge.  The  protocone  remains  as  an  inwardly  projecting  ridge  at  the 
front  of  the  tooth,  which  otherwise  makes  a  single  blade,  shearing 
outside  a  similar  blade  formed  by  the  paraconid  and  protoconid  of 
the  lower  molar.  This  restriction  to  long  sharp  ridges  also  affects  the 
teeth  in  front  of  the  carnassials,  but  behind  them  the  molars  are  so 
reduced  that  in  true  cats  they  are  represented  only  by  a  single  vestige 
in  each  jaw.  More  of  the  posterior  molars  remain  in  some  of  the 
primitive  carnivores  (dogs),  and  in  some,  such  as  the  bears,  they  may 
acquire  a  bunodont  surface  and  hence  the  power  of  grinding. 

The  jaws  are,  of  course,  powerful  in  carnivores,  the  articulation 
being  a  tight,  transverse  hinge,  allowing  none  of  the  rotatory  move- 
ments found  in  other  mammals.  The  jaw-muscles  include  especially 
powerful  temporals,  for  whose  attachment  there  is  a  large  coronoid 
process  on  the  jaw  and  often  large  sagittal  crests  on  the  top  of  the  skull. 
The  temporal  fossa  is  very  wide  and  never  closed  off  from  the  orbit, 
since  there  is  no  need  for  specially  increased  surfaces  for  the  masseter, 
which  is  only  moderately  strong.  The  pterygoid  muscles  (and  their 
fossa)  are  reduced,  since  the  jaw  has  no  rotary  action. 

The  post-cranial  skeleton  shows  a  generalized  mammalian  build, 
with  specializations  for  sudden  leaping  movements.  There  are  five 
digits  in  the  hand  and  four  in  the  foot  in  cats;  in  other  carnivores 
the  number  is  never  less  than  four.  The  toes  are  armed  with  the 
characteristic  claws,  which  are  held  drawn  back  by  elastic  ligaments 
and  pulled  out  when  needed  by  the  action  of  the  flexor  digitorum 
profundus  muscles  on  the  terminal  phalanx,  to  which  the  claw  is 
attached.  The  weight  of  the  body  is  carried  on  special  pads  on  the 
second  interphalangeal  joints  and  the  metatarsal  heads.  A  curious 
feature  of  the  carpus  of  all  modern  carnivores  is  the  fusion  of  the 
scaphoid  and  lunate  bones.  The  arrangement  of  the  limbs  and  back- 
bone is  that  of  a  quadruped  able  to  proceed  over  uneven  surfaces  and 
also  steeply  upwards  and  downwards,  especially  in  the  carnivores  that 
are  arboreal.  This  involves  a  long  body,  with  much  of  the  weight 
carried  on  the  fore-limbs;  the  thoracic  neural  spines  are  therefore 
high.  On  the  other  hand,  the  vertebral  girder  has  to  take  the  strain  of 
powerful  sacrospinalis  muscles  for  leaping;  the  transverse  processes 
are  broad  in  the  lumbar  region,  and  again  in  the  neck  for  the  muscles 


xxvii.  5  CREODONTS  683 

that  move  the  head.  The  clavicle  is  reduced.  The  tail,  well  developed 
for  the  maintenance  of  balance  in  wild  cats,  tends  to  become  reduced 
under  domestication,  the  extreme  being  the  Manx  variety,  with  only 
three  caudal  vertebrae. 

As  in  so  many  carnivores,  the  alimentary  canal  is  short  and  the 
stomach  never  complex  or  the  coecum  large.  The  uterus  retains  the 
primitive  mammalian  bicornuate  form.  The  chorio-vitelline  placenta 
is  important  early  in  pregnancy.  The  chorio-allantoic  placenta  is  of 
a  type  known  as  vasochorial  with  the  villous  portion  of  the  chorion 
restricted  to  a  characteristic  band  around  the  embryo  (hence  'zonary' 
placenta). 

5.  *Suborder  Creodonta 

Besides  animals  such  as  the  cats,  adapted  in  this  detailed  way  for 
hunting  live  prey,  the  order  Carnivora  contains  a  variety  of  less- 
modified  forms,  such  as  the  dogs  and  their  offshoot  the  bears,  which 
are  partly  scavengers.  Others  are  suited  for  special  types  of  carni- 
vorous life,  such  as  the  weasels,  mongooses,  and  other  small  animals. 
The  seals  and  walruses  are  carnivores  much  changed  by  aquatic  life. 

Great  numbers  of  fossil  carnivores  are  known  and  we  can  trace 
much  of  the  history  of  the  order.  The  *Creodonta  (=  'flesh-tooth') 
of  the  Palaeocene  and  Eocene  included  four  distinct  families,  one,  the 
*Arctocyonidae,  is  perhaps  close  to  the  ancestry  of  the  whole  Fer- 
ungulate  stock,  the  other  three  are  more  specialized.  The  earliest  creo- 
donts,  such  as  *Tricentes  of  the  North  American  Palaeocene,  were 
small  semi-plantigrade  creatures,  very  like  the  contemporary  small 
insectivores,  which  were  the  prototype  of  all  eutherian  mammals. 
The  skull  was  long  and  low,  with  a  small  macrosmatic  brain,  but 
already  having  sagittal  crests  for  the  temporalis  muscle.  The  denti- 
tion included  the  full  number  of  teeth  and  these  carried  sharp  cusps, 
arranged  in  the  tritubercular  pattern,  with  the  beginning  of  the 
development  of  a  hypocone  in  the  upper  molar.  There  was  no  car- 
nassial,  however;  animals  of  this  type  could  therefore  well  have  given 
rise  to  non-carnivorous  forms,  such  as  the  ungulates.  Other  differences 
from  modern  carnivores  were  that  the  scaphoid  and  lunate  were  not 
fused  and  there  was  no  ossified  auditory  bulla. 

It  is  not  surprising  that  these  early  creodonts  were  for  a  long  time 
classed  as  Insectivora.  Their  descendants  soon  began  to  show  various 
specializations.  Thus  *Arctocyon  of  the  Upper  Palaeocene  of  Europe 
was  a  large  animal,  with  tuberculated  molars,  probably  omnivorous 
like  a  hear.  Some  Eocene  descendants  of  this  type,  such  as  *Mesonyx 


684  CARNIVORES  xxvn.  5- 

(Fig.  448),  retained  the  triangular  molars  and  became  very  large, 
perhaps  they  were  scavenging  creatures.  Their  toes  carried  hoofs, 
and  this,  together  with  their  simple  dentition  and  other  features,  has 
suggested  to  some  that  smaller  members  of  the  group  may  have  been 
ancestral  to  the  Artiodactyla.  Other  Eocene  creodonts,  however, 
became  more  typical  carnivores,  with  shearing  carnassials,  developed 
from  various  teeth,  often  the  upper  first  and  lower  second  molar. 


Fig.  448.  The  skulls  of  some  early  carnivores. 

a,  *Mesonyx\  B,  *Oxyaena;  c,  *Sinopa;  d,  *Vulpavus.  a-c  are  creodonts,  D  is 

a  rniacid  fissipede.  (After  Romer,  a  after  Scott,  b  and  c  after  Wartmann,  and 

D  after  Matthew.) 

These  early  carnivores  radiated  into  lines  that  parallel  those  found 
today.  Thus  *Dromocyon  resembled  a  dog,  *Oxyaena  an  otter,  *Dis- 
sacus  a  cat,  and  *Sinopa  a  weasel.  *Hyaenodon  and  its  allies  were 
abundant  hyena-like  animals  of  various  sizes;  they  survived  until  the 
Eocene.  *Apataelurus  was  an  Eocene  sabre-tooth.  By  their  similarities 
to  later  carnivores  these  arrays  of  early  carnivore  types  constitute  a 
remarkable  example  of  convergent  evolution. 

After  their  abundance  in  the  Eocene  the  creodonts  declined, 
although  a  few  genera  survived  until  the  Pliocene.  Perhaps  the  type, 
though  able  to  catch  the  cumbrous  early  herbivores,  was  unable  to 
make  a  living  from  the  later,  faster-moving  ungulates. 

6.  Suborder  Fissipeda 

Towards  the  end  of  the  Eocene  a  new  type  of  carnivore  became 
abundant.  The  earliest  of  these,  the  *Miacidae,  were  so  like  creodonts 
that  they  are  sometimes  classified  in  that  group,  sometimes  with  the 
Fissipeda.  Thus  miacids  of  the  Eocene  (Fig.  448)  were  small  animals, 
perhaps  arboreal,  very  close  to  the  *Arctocyonidae  and  still  with 


xxvii.  6  THE    DOGS  685 

triangular  molars,  unossified  bulla,  and  separate  carpal  bones.  There 
was,  however,  a  sign  of  the  beginning  of  the  fissipede  carnassials,  the 
fourth  upper  premolar  and  first  molar  being  elongated,  the  cusps 
partly  united  to  form  a  ridge.  At  the  end  of  the  Eocene  and  beginning 
of  the  Oligocene  early  representatives  of  the  various  fissipede  families 
appeared  and  were  presumably  derived  from  these  miacids.  The  dogs 
(Canidae)  (Fig.  449)  appeared  very  early  and  have  since  changed 
relatively  little,  the  modern  Canis  being  practically  a  survivor  show- 
ing us  the  Eocene  stage  of  carnivore  evolution.  Numerous  fossil  dogs 


Fig.  449.  Wolf,  Canis.  (From  a  photograph.) 

are  known  and  the  type  has  been  a  very  successful  one.  The  diet  is 
varied  and  partly  herbivorous.  The  European  red  fox,  for  instance, 
feeds  on  mice,  hares,  rabbits,  and  chickens,  but  also  on  snails,  insects, 
and  berries.  The  type  is  not  suited  for  climbing  but  for  running  in 
open  country,  for  which  purpose  long  legs  and  a  digitigrade  habit 
have  been  developed,  the  pollex  and  hallux  being  reduced  (Fig.  354). 
The  teeth  have  remained  unspecialized,  with  at  least  two  post-carnas- 
sial  grinding  molars  and  still  distinct  signs  of  the  triangular  form  in 
the  carnassial  (Fig.  450).  Dogs,  wolves,  and  foxes  are  found  through- 
out the  world,  including  South  America,  but  not  in  Madagascar  or 
New  Zealand.  So  many  types  are  known  that  the  exact  ancestry  of  the 
various  wolves  and  foxes  has  not  been  fully  disentangled. 

The  bears  (Ursidae)  (Fig.  451)  were  a  Miocene  offshoot  from  this 
dog  stock  and  here  the  tendency  to  non-carnivorous  diet  became 
accentuated;  there  are  no  carnassials  and  the  molars  acquire  bunodont 
grinding  surfaces.  The  gait  is  plantigrade.  Various  types  are  found 
through  the  Holarctic  region  and  South  America.  The  raccoons 
(Procyonidae)  (Fig.  452)  are  a  rather  similar  though  smaller  type 
of  animal,  with  dentition  suited  to  an  omnivorous  diet,  the  upper 


686 


CARNIVORES 


xxvii.  6 


carnassial  having  developed  ( ?  redeveloped)  a  hypocone.  They  are 
all  American,  except  Ailurus  and  Ailuropoda,  the  panda  and  giant 
panda  (Fig.  453),  large,  herbivorous  creatures  living  in  Asia.  The 
latter  has  a  special  bone  near  the  pollex,  making  a  grasping  organ  for 
holding  bamboo  shoots. 


■Labial  view 


Cat  Dog  Bear 

Fig.  450.  Carnassial  teeth  of  carnivores. 

The  top  row  shows  the  last  left  upper  premolar  from  the  labial  side ;  middle  row 

the  same  from  below;  bottom  row  the  first  left  lower  molar  from  the  labial  side. 

/;.  heel  (talonid);  me.  metaconc;  md.  metaconid;  pa.  paracone;  pd.  paraconid;  pr. 

protocone.  (Partly  after  Flower  and  Lydekker.) 


These  families  of  rather  primitive  carnivores  are  united  in  a  super- 
family  Canoidea,  and  with  them  we  may  associate  the  weasels  (Muste- 
lidae),  which  are  the  typical  small  carnivores  found  throughout  the 
world  and  retain  many  primitive  characters.  They  have  well-developed 
carnassials  and  never  more  than  one  post-carnassial  molar.  They  can 
be  recognized  back  to  the  Eocene  and  now  include  the  stoats  and 
weasels,  Mustela  (Fig.  455),  which  live  on  rats  and  mice,  rabbits,  and 
other  small  herbivores;  Meles  the  badger  (Fig.  454),  which  is  omni- 
vorous and  has  a  hypocone;  Mephitis  the  skunk  (Fig.  456),  a  burrow- 
ing animal  that  ejects  a  stream  of  foul-smelling  liquid  from  special 
anal  glands;  and  the  otters,  Lutra  (Fig.  457),  with  webbed  feet,  short 
fur,  small  ears,  and  other  features  suited  for  life  in  the  water.  In  many 


(687) 


Fig.  451.  Brown  bear,  Ursus.  (From  life.) 


Fig.  452.  Raccoon,  Procyon. 
(From  a  photograph.) 


Fig.  453.  Giant  panda,  Ailuropoda. 
(From  a  photograph.) 


Fig.  454.  Badger,  Meles 
(From  photographs.) 


Fig.  455.  Stoat,  Mustela. 
(From  a  photograph.) 


Fig.  456.  Common  skunk,  Mephitis. 
(From  photographs.) 


(688) 


Fig.  457.  Otter,  Lutra.  (From  photographs.) 


Fig.  458.  Indian  mongoose,  Herpestes. 
(After  a  photograph  by  F.  W.  Bond.) 


Fig.  459.  Hyena,  Hyaena.  (From  photographs.) 


Fig.  460.  Sabre-tooth,  *Smilodon.  (After  Scott.) 


tem 


tt.rn 


tern 


xxvii.  6  SABRE-TOOTHS  689 

mustelids  there  is  delayed  implantation  of  the  blastocyst  and  other 
interesting  reproductive  phenomena. 

The  most-modified  Carnivora  are  placed  in  the  superfamily  Feloidea. 
The  civets  and  mongooses  (Viver- 
ridae)  (Fig.  458)  are  survivors 
that  show  us  many  of  the  charac- 
ters possessed  by  this  type  in  the 
Oligocene.  They  are  the  small 
carnivores  that  occupy  in  the 
Old  World  tropics  the  position 
taken  farther  north  by  the  weasels. 
In  general  they  are  like  the  ances- 
tral miacids,  with  long  skull, 
small  brain,  and  short  legs.  Her- 
pestes,  the  mongoose,  is  abundant 
throughout  Africa  and  Asia. 

The  hyenas  (Fig.  459)  have 
become  large  running  creatures, 
with  massive  teeth  specialized 
for  crushing,  and  hence  allowing 
a  scavenging  life.  The  true  cats 
(Felidae)  were  already  differenti- 
ated from  the  miacid  ancestry  in 
the  Eocene,  but  at  that  early 
period  they  all  had  the  very  great 
development  of  the  upper  canines 
as  cutting  and  piercing  sabre- 
teeth  (Figs.  460,  461).  There 
were  numerous  genera  with  this 
characteristic  from  the  Eocene 
onwards  until  the  Pleistocene, 
when  they  disappeared  simulta- 
neously from  Europe,  Asia,  and 
America.  Probably  they  attacked 
large,  thick-skinned  herbivores. 
The  jaw  could  be  opened  to  a  right  angle  to  allow  the  fang  to  strike, 
and  there  were  such  associated  developments  as  large  mastoid  pro- 
cesses for  the  sterno-mastoid  muscles  that  pulled  the  head  down- 
wards and  forwards  in  the  strike.  The  closing  muscles  of  the  jaw  and 
the  coronoid  process  were,  however,  small  in  the  sabre-tooths. 

The  cats  themselves,  with  smaller  canines,  appeared  in  the  Oli- 


Fig.  461.  Neck  and  jaw  muscles  of  A,  sabre- 
tooth,  *Smilodon,  compared  with  those  of  a 
modern  cat  B,  to  show  modifications  for 
striking  with  the  whole  head  and  biting, 
respectively. 

c.  condyle;  cl.  m.  cleidomastoid;  dig.  digastric; 
m.  mastoid  process;  mas.  masseter;  st.  m.  sterno- 
mastoid;  tern,  temporalis.  (From  Lull,  Organic 
Evolution,  copyright  191 7,  1929  by  The  Mac- 
millan  Company  and  used  with  their  permission, 
after  Matthew.) 


690 


CARNIVORES 


xxvii.  6- 


gocene.  They  are  very  successful  carnivores,  partly  arboreal  and  hence 
most  common  in  tropical  regions,  where  there  are  large  forests.  There 
is  much  difference  in  detailed  habits  between  the  many  species  of  the 
family,  but  all  are  alike  in  bony  structure.  Numerous  attempts  have 
been  made  to  divide  the  group  into  genera  and  subgenera,  but  all  may 
reasonably  be  retained  in  a  single  genus  Felis.  Lions  (F.  led)  have  many 
distinct  races  in  Africa  and  Asia  and  are  mainly  terrestrial,  hunting 


Fig.  462.  Tiger,  Felis.  (From  photographs.) 


in  open  country.  Tigers  (F.  tigris)  (Fig.  462)  occur  throughout  Asia 
to  Siberia,  are  usually  solitary,  and  often  frequent  damp  places.  They 
also  have  many  races,  and  in  captivity  lions  and  tigers  can  be  crossed. 
Other  cats  are  mostly  smaller  and  more  fully  arboreal  than  the  lion 
and  tiger.  The  leopard  (F.  pardus)  of  Africa  and  Asia  reaches  5  ft  in 
body  length.  Felis  catus,  the  wild  cat,  formerly  common,  still  exists  in 
Britain  and  has  a  Palearctic  distribution.  The  domestic  cat  probably 
arose  in  Egypt  from  the  caffre  cat,  F.  ocreata.  The  jaguar  (F.  ofica), 
puma  (F.  cougar),  and  ocelot  (F.  pardalis)  are  large  Central  and  North 
American  cats,  which  have  recently  invaded  South  America. 

Felis  is  thus  one  of  the  most  widespread  of  all  mammalian  genera, 
occurring  in  all  main  parts  except  Australasia,  Madagascar,  and 
oceanic  islands.  Because  of  their  striking  and  familiar  characteristics 
we  can  form  a  vivid  picture  of  all  these  slightly  different  sorts  of  cat, 
pursuing  varying  prey  in  the  different  regions.  In  order  to  visualize 
past  evolution  properly  we  should  need  to  have  an  equally  detailed 
knowledge  of  past  populations.  It  is  difficult  enough  to  classify  and 
describe  a  modern  population  of  this  sort  and  we  need  not  be  sur- 


xxvi  i.  7  SEALS  691 

prised  that  the  palaeontologist,  who  has  to  consider  also  variations 
with  time,  finds  that  the  growth  of  his  material  introduces  intolerable 
problems  of  classification. 

7.  Suborder  Pinnepedia 

The  seals,  sea-lions,  and  walruses  are  marine  carnivores  that  have 
existed  since  the  Miocene.  Their  exact  affinities  are  doubtful;  they 
show  some  similarities  to  otters,  perhaps  due  to  common  ancestry 
but  possibly  to  convergence.  They  also  have  a  remote  likeness  to  the 
bears. 


Fig.  463.  Skeleton  of  the  seal,  Phoca.  (After  Blainville.) 

In  the  seals  (Phocidae)  the  body  is  streamlined,  covered  with  thick 
fur,  below  which  is  a  thin  epidermis  and  a  thick  layer  of  blubber, 
making  a  quarter  of  the  weight  of  the  animal.  Swimming  is  by  means 
of  the  paddle-like  limbs  and  flexion  of  the  whole  body,  there  is  web- 
bing between  the  digits,  and  the  tail  is  reduced  to  a  short  rudiment. 
The  basal  segments  of  the  limbs  are  shortened  and  some  of  the  digits 
lengthened,  without  any  increase  in  their  number,  though  there  are 
some  extra  phalanges.  The  speed  of  swimming  may  reach  15  knots  if 
the  seal  is  frightened.  The  cervical  vertebrae  are  massive,  with  com- 
plex articulations,  but  the  hinder  ones  are  simplified  and  the  column 
very  flexible,  so  that  it  can  be  bent  dorsally  or  laterally,  allowing 
sudden  turns  in  the  water  and  complicated  balancing  feats  on  land 
(Fig.  463).  All  the  seals  leave  the  water  to  breed  and  therefore  need 
some  support  for  their  large  bodies. 

The  teeth  show  a  reduction  in  number  and  are  rows  of  nearly 
similar,  laterally  compressed  spines.  They  may  carry  three  cusps  in 
a  row,  a  reversion  to  'reptilian'  conditions,  which  serves  to  prevent 
escape  of  the  slippery  prey.  There  are  large  canines.  The  milk  denti- 
tion is  lost  very  early,  sometimes  in  utero.  The  intestine  is  long.  The 
water-supply  is  obtained  from  metabolic  water. 


692  CARNIVORES  xxvu.  7 

The  pinnipedes  resemble  the  whales  in  being  microsmatic  but  have 
good  eyes,  with  flat  cornea,  round  lens,  and  a  muscular  palpebral 
sphincter.  The  eyes  are  directed  upwards  and  prey  is  often  caught 
from  below.  The  external  ears  are  reduced  but  hearing  is  probably 
acute;  the  auditory  ossicles  are  massive.  There  are  numerous  large 
vibrissae  on  the  muzzle.  The  brain  is  large  and  rounded,  with  con- 
voluted hemispheres  and  large  midbrain  and  cerebellum.  There  is  an 
elaborate  vocal  communication  system,  the  calls  varying  to  human 
ears  from  booming  to  chirping. 

Young  seals  can  remain  submerged  for  up  to  25  minutes  and  have 
been  shown  to  be  able  to  stand  a  pressure  equivalent  to  a  dive  to  95  m. 
Larger  seals  can  remain  submerged  even  longer  and  at  greater 
depths.  The  nostrils  are  closed  by  special  muscles.  The  lungs  are 
large  and  the  bronchi  contain  myoelastic  valves.  During  a  dive  the 
heart  slows  from  120  to  4  beats  a  minute.  There  is  no  drop  in  blood- 
pressure,  because  of  a  widespread  reflex  vaso-constriction,  which 
prevents  blood  reaching  the  tissues,  except  the  brain  and  heart 
muscle.  Blood  from  the  brain  returns  to  the  abdomen,  by  a  large 
vessel  above  the  spinal  cord,  and  then  accumulates  there  in  extensive 
sinuses,  including  a  huge  dilatation  of  the  vena  cava  above  the  liver, 
which  is  occluded  by  a  sphincter  of  striated  muscle  above  the  dia- 
phragm. There  are  few  true  retia  mirabilia  but  abundant  venous 
plexuses.  The  blood  can  carry  as  much  as  35  c.c.  of  oxygen  for  100 
c.c.  of  blood  (20  c.c.  in  man  under  the  same  conditions),  and  there  is 
much  myoglobin  in  the  muscles.  The  respiratory  centre  tolerates  a 
high  C02  level.  Lactic  acid  accumulates  in  the  muscles,  reducing 
metabolic  levels.  By  these  means  the  animal  is  provided  with  sufficient 
oxygen  for  the  dive,  without  absorbing  nitrogen  and  risking  'bends'. 

Copulation  takes  place  in  the  water  in  most  seals  and  the  penis 
bone  is  very  large,  especially  in  the  walrus.  The  external  genitalia,  like 
the  nipples,  are  withdrawn  into  folds  of  the  surface.  The  eggs  are 
fertilized  shortly  after  parturition,  the  two  horns  of  the  uterus  carrying 
alternate  pregnancies.  Implantation  of  the  blastocyst  is  delayed  for 
two  months  or  more.  As  in  other  carnivores  the  placenta  is  zonary, 
with  coloured  margins  due  to  the  presence  of  bilirubin. 

In  the  sea-lions  (Otariidae)  (Fig.  464)  the  legs  can  still  be  turned 
forward  for  use  on  land,  and  there  are  other  primitive  features,  in- 
cluding external  ears.  They  are  more  mobile  on  land  than  are  the  seals 
and  can  even  climb  cliffs.  The  family  dates  back  to  the  Miocene.  The 
walrus,  Odobenus,  is  a  related  form,  highly  specialized  for  eating 
bottom-living  molluscs,  which  it  digs  up  with  its  enormous  canines. 


xxvii.  7  SEALS  693 

The  Phocidae  are  the  modern  seals,  found  in  all  seas  and  fully  aquatic, 
the  hind  limbs  being  attached  to  the  tail.  They  come  ashore  only  for 
short  periods  in  isolated  places  to  breed,  and  can  only  just  drag  them- 
selves along  the  beaches.  Many  seals  migrate  for  long  distances  to 


Fig.  464.  Sea-lion,  Eumetopias.  (From  a  drawing  belonging  to 
the  Zoological  Society.) 

particular  breeding-places,  such  as  the  Pribilof  Islands  in  the  case  of 
the  fur  seals  (Callorhinus).  The  males,  arriving  first,  fight  furiously 
with  each  other,  the  victors  then  collecting  harems  of  twenty  or  more 
females,  who  give  birth  to  their  young  and  are  soon  afterwards 
impregnated  again.  The  bulls  remain  on  shore  without  feeding,  guard- 
ing the  family,  while  the  females  return  to  suckle  the  young  at  each 
tide  for  a  period  of  about  three  weeks. 


XXVIII 

PROTOUNGULATES 

1 .  Origin  of  the  ungulates 

No  herbivorous  eutherians  are  known  from  the  Cretaceous  period, 
but  during  the  Palaeocene  epoch  a  number  of  animals  abandoned  the 
insectivorous  habit  and  began  to  eat  plants.  These  condylarths  rapidly 
radiated  into  numerous  types,  so  that  by  the  end  of  the  Palaeocene 
several  distinct  orders  descended  from  this  stock  can  be  recognized. 
In  North  America  and  elsewhere  there  appeared  large,  clumsy  ani- 
mals, the  *Pantodonta  (Amblypoda)  and  *Dinocerata,  while  in  South 
America  a  special  fauna,  the  *Notoungulata  and  *Litopterna,  de- 
veloped. Further  types  then  arose  in  the  Eocene,  including  the  early 
elephants  and  Perissodactyla.  The  Artiodactyla  first  appeared  in  the 
lower  Eocene,  as  rather  pig-like  creatures;  their  origin  is  uncertain 
but  they  may  have  come  from  some  form  not  very  distinct  from  the 
*Condylarthra. 

During  the  Eocene  and  Oligocene  there  were,  therefore,  numerous 
large,  heavy-bodied  herbivorous  mammals,  perhaps  mainly  suited  to 
forest  life  and  living  upon  relatively  soft  green  food,  since  their  teeth 
were  mostly  not  highly  developed  for  grinding.  They  were,  however, 
gradually  replaced  during  the  Miocene  by  swifter,  grazing  animals 
suited  to  the  plains  of  that  period. 

Following  Simpson  we  shall  classify  the  numerous  orders  of  her- 
bivorous (ungulate)  mammals  into  four  superorders.  The  Proto- 
ungulata,  including  *Condylarthra,  *Litopterna,  *Notoungulata, 
*Astrapotheria,  and  Tubulidentata,  include  the  oldest  forms,  together 
with  various  early  offshoots  and  one  living  creature  the  aardvark 
or  Cape  ant-eater,  which  is  difficult  to  place  elsewhere.  A  second 
superorder,  Paenungulata,  includes  a  number  of  descendants  of  the 
condylarths  that  early  achieved  success,  the  *Pantodonta  and  *Dino- 
cerata  of  the  Holarctic  region,  *Pyrotheria  of  South  America,  and 
*Embrithopoda  in  Africa.  With  these  are  placed  the  Proboscidea, 
which  succeeded  them  as  large  herbivores  in  the  Miocene.  The  conies 
(Hyracoidea)  are  an  isolated  group  that  still  shows  some  of  the  Eocene 
characteristics  of  this  Paenungulate  group,  and  the  sea-cows  (Sirenia) 
are  an  early  offshoot  that  took  to  aquatic  life.  Finally,  the  orders 
Perissodactyla  and  Artiodactyla  occupy  two  separate  superorders, 
Mesaxonia  and  Paraxonia. 


xxviii.  2  UNGULATE    CHARACTERS 

at. 

.3JC. 


695 


Fig.  465.  Skeletons  of  horse  and  cow.  (After  Ellenbergcr  and  Sisson.) 

a.  astragalus;  at.  atlas;  ax.  axis;  c.  calcaneum,  £2-4,  distal  carpals;  cb.  cuboid;  cn3.  3rd 

cuneiform;  Di.  1st  thoracic  vertebra;/,  femur;  fib.  fibula;  /;.  humerus;  i.  intermedium; 

il.   ilium;   is.   ischium;   Li.    1st   lumbar   vertebra;    n.   navicular;   r.   radius,   rad.   radials; 

sc.  scapula;  /1-3.  distal  tarsals;  tib.  tibia;  u.  ulna;  ul.  ulnae,  II  IV,  metatarsals. 

2.  Ungulate  characters 

When  mammals  adopt  a  herbivorous  diet  they  assume  certain 
characteristics,  which  it  is  convenient  to  recognize  before  dealing  with 
the  individual  groups  (Fig.  465).  The  animals  often  become  large,  but 
it  must  be  remembered  that,  outside  the  ungulates,  the  rodents  include 


696 


PROTO UNGULATES 


XXVIII.  2 


many  successful  small  herbivores,  and  that  conversely  among  the 
ungulates  the  hyraxes  are  small.  The  skin  is  often  thick  and  a  variety 
of  protective  coloration  schemes  of  spots  and  stripes  appear,  the  under 
side  usually  being  paler  to  eliminate  shadows.  Defensive  weapons  such 
as  tusks  or  horns  are  common,  but  the  problem  of  security  often  leads 
an  unaggressive  animal  to  the  development  of  a  swift  gait.  For  this 
the  limbs  are  lengthened  by  raising  up  on  the  toes  (p.  576),  producing 
first  digitigrade  and  then  unguligrade  locomotion.  When  this  happens 


n.+  cb. 


Fig.  466.  Skeletons  of  feet  of  horse  and  cow. 
Lettering  as  Fig.  465. 

the  more  lateral  digits,  failing  to  reach  the  ground,  become  reduced 
and  may  disappear,  leaving  finally  the  characteristic  one  or  two.  The 
movement  of  the  limb  becomes  restricted  to  a  fore-and-aft  direction, 
and  the  joints  assume  a  pulley-like  form,  especially  characteristic  in 
the  trochlea  of  the  talus,  deeply  grooved  in  artiodactyls  but  markedly 
so  also  in  perissodactyls  (Fig.  466).  The  carpal  and  tarsal  bones  of 
these  swift-moving  animals  become  arranged  on  the  so-called  inter- 
locking plan,  by  which  each  elongated  metapodial  thrusts  up  against 
two  carpals  or  tarsals.  No  movements  of  pronation  occur,  and  the  ulna 
and  fibula  tend  to  be  reduced  and  fused  with  the  radius  and  tibia. 
The  hoofs  themselves  are  a  characteristic  development,  the  terminal 
phalanx  is  broadened,  and  the  claw  becomes  modified  to  surround  it, 
while  a  pad  forms  below.  The  elongation  of  the  limbs  is  mainly  in  the 
lower  sections,  the  humerus  and  femur  being  short.  Locomotion  is  by 
movement  of  the  whole  limb  by  the  action  of  its  proximal  muscles, 
the  hind-limbs  being  the  main  propellents  and  the  fore-limbs  weight- 
bearers,  with  corresponding  modification  of  the  vertebral  girder  (p. 
728).  The  neural  spines  are  very  high  above  the  fore-legs  and  the  ribs 


xxviii.  2  UNGULATE    CHARACTERS  697 

are  numerous,  so  that  the  girder  has  large  compression  struts  above 
and  below  and  it  balances  largely  on  the  fore-legs  and  is  pushed  from 
behind.  The  ilium  is  broad  and  raised  vertically,  providing  large  attach- 
ments for  the  glutei,  which  are  the  important  locomotor  muscles,  and 
for  the  abdominal  muscles,  which  carry  the  weight  of  the  belly.  This 
arrangement  of  the  column  is  essentially  preserved  even  in  the  very 
large  animals,  such  as  elephants,  rhinoceroses,  and  many  extinct  types, 
which  are  said  to  be  'graviportal'.  In  these  latter,  however,  the  legs 
are  arranged  on  a  different  plan,  since  the  great  weight  can  only  be 
carried  by  very  massive  struts  of  large  cross-section.  The  proximal 
parts  are  therefore  enlarged  and  several  digits  are  retained  to  make 
broad  supports  for  the  pillars,  as  is  well  seen  in  the  elephant's  foot. 

In  many  ungulates  the  neck  becomes  considerably  lengthened, 
probably  both  in  order  to  reach  up  or  down  for  food  and  also  to  give 
a  good  look-out  for  the  head.  The  ears  are  long  and  hearing  acute,  so 
that  the  direction  of  sounds  may  be  easily  detected.  Sight  is  not  especi- 
ally developed,  but  the  pupil  is  often  horizontal  in  animals  that  live 
on  the  plains,  giving  a  wide  visual  angle.  The  sense  of  smell  is  well 
developed  and  the  animals  often  graze  advancing  up-wind,  using 
for  this  purpose  the  receptors  of  the  moist  muzzle.  The  tongue  is  large 
and  taste  receptors  sensitive. 

The  brain  is  large  and  the  life  of  these  herbivores  is  conducted  with 
the  use  of  much  information  learned  during  each  lifetime.  This 
enables  them  to  range  over  large  territories  and  to  vary  these  with  the 
seasons,  in  search  of  food  and  water.  They  show  a  remarkable  alertness 
to  changes  of  sound  or  scent. 

Many  herbivores  are  social  animals,  and  information  is  shared 
among  a  large  group.  They  have  elaborate  means  of  communication 
by  scent  glands,  which  are  used  to  mark  trails  and  territory,  as  well  as 
for  exchange  of  signals  between  individuals.  Their  sexual  organization 
is  complicated,  involving  elaborate  interchange  of  visual,  auditory, 
and  olfactory  signals  and  often  combat  between  males.  The  establish- 
ment of  a  leader  is  apparently  often  needed  to  allow  the  advantages  of 
social  organization  for  protection  and  finding  food.  Gestation  is  long 
and  relatively  few  young  are  produced  (as  in  other  large  animals  with 
efficient  brains).  The  new-born  is  well  developed  and  soon  able  to  run 
with  the  herd. 

Perhaps  the  most  significant  modifications  are  in  the  means  of 
obtaining  and  digesting  the  food.  The  triangular  molar  pattern  gives 
place  to  a  square  one,  by  development  of  a  hypocone  on  the  posterior 
interior  side  of  the  upper  molar.  The  lower  molar  also  becomes 


698 


PROTO UNGULATES 


XXVIII.  2- 


square,  by  loss  of  the  paraconid  and  raising  the  heel,  whose  outer 
hypoconid  and  inner  entoconid  make  a  pair,  behind  the  metaconid 
and  protoconid  (Fig.  467).  Even  more  characteristic  is  the  change  in 
the  cusps  themselves.  Instead  of  the  original  sharp  points  they  develop 
first  low  cones,  giving  so-called  bunodont  grinding  surfaces.  Then,  in 
later  evolutionary  stages,  ridges  or  lophs  appear  between  the  cusps; 
an  ectoloph  between  paracone  and  metacone,  transverse  protolph  at 
the  front  of  the  tooth  (between  protocone  and  protoconule),  and 
metaloph  behind  between  hypocone  and  metaconule.  All  sorts  of 


B 


Fig.  467.  Hyracotheriwn.  Upper  (a)  and  lower  (b)  premolars  and  molars. 

(After  Wortmann  from  Outlines  of  Vertebrate  Palaeontology,  Cambridge 

University  Press.) 

further  developments  and  cross-connexions  may  then  take  place  in 
such  lophodont  molars;  moreover,  the  whole  tooth  becomes  sur- 
rounded by  'cement'  (bone),  so  that  the  ridges  are  supported  as  they 
wear  away  and  continually  maintain  a  rough  surface  for  grinding. 
Short  (brachydont)  molars,  which  would  wear  away  too  quickly,  are 
replaced  by  deep  (hyposodont)  ones,  which  grow  continually  from 
open  roots  in  extreme  instances. 

In  these  animals  that  need  to  increase  the  grinding  surfaces  the 
whole  set  of  teeth  is  usually  retained  and  the  molar  structure  extends 
forwards  to  the  premolars.  This  molarization  may  be  said  to  be 
the  opposite  of  the  condition  in  carnivores,  where  the  tooth  row  is 
shortened  and  the  hinder  teeth  come  to  have  cutting  edges  like  the 
front  ones.  The  incisors  of  ungulates  become  specialized  for  cropping 
the  food;  in  artiodactyls  the  upper  ones  are  lost  and  the  lower  work 
against  a  horny  upper  lip.  The  canine  is  often  absent,  leaving  a 
diastema.  The  cropping  and  grinding  mechanisms  involve  various 
modifications  of  the  lips,  palate,  tongue,  and,  of  course,  the  jaws  and 
their  muscles.  The  articulation  of  the  jaw  with  the  skull  is  usually  made 


xxviii.  3  CLASSIFICATION  699 

by  a  flattened  facet,  allowing  rotatory  action  of  the  lower  jaw.  The 
pterygoid  and  masseter  muscles  are  well  developed,  the  temporal  less 
so  and  the  skull  is  flat  and  without  a  sagittal  crest,  in  contrast  with 
carnivores.  To  provide  lateral  attachment  for  these  muscles  there 
is  a  tendency  for  a  redevelopment  of  the  post-orbital  bar. 

In  the  digestive  system  of  ungulates  there  is  usually  some  chamber 
in  which  bacterial  action  upon  cellulose  can  take  place,  but  this  has 
evidently  evolved  independently  in  the  different  groups,  being  in  the 
stomach  of  artiodactyls  but  in  the  caecum  of  perissodactyls. 

This  set  of  'ungulate'  characteristics  has  developed  independently 
many  times  in  descendants  of  the  insectivoran  eutherian  ancestor, 
and  shows  strikingly  how  the  adoption  of  a  particular  method  of  life 
leads  to  selection  of  variations  of  structure  tending  in  similar  direc- 
tions. There  is  no  special  difficulty  in  understanding  how  this  has 
happened  if  we  imagine  that  each  part  varies  genetically  in  its  dimen- 
sions. A  herbivorous  diet  will  be  easier  for  animals  with  ridged  teeth 
and  long  legs,  whereas  those  with  sharper  teeth  can  become  carni- 
vores. Types  are  selected  that  combine  a  nervous  organization  leading 
to  certain  habits  with  other  features  that  make  these  habits  successful. 
In  the  evolution  of  any  population  there  is  evidently  an  elaborate  inter- 
play between  variation  in  different  directions  in  various  organ  systems 
and  changes  in  the  environmental  circumstances. 

3.  Classification 

Superorder  2.  Protoungulata 
*Order  1.  Condylarthra.  Palaeocene-Eocene 

*Family  1.  Hyopsodontidae.  Palaeocene-Eocene.  N.  America 

*Mioclaenus,  Palaeocene;  *Hyopsodiis,  Eocene 
*Family  2.  Phenacodontidae.  Palaeocene-Eocene.  Holarctic 

*Tetraclaenodon,  Palaeocene;  *Phenacodns,  Palaeocene-Eocene 
*  Family  3.  Didolodontidae.  Palaeocene-Miocene.  S.  America 

*Didolodns 
*Family  4.  Periptychidae.  Palaeocene.  N.  America 

*Periptychus 
*Family  5.  Meniscotheriidae.  Palaeocene-Eocene 
*Meniscotherium,  Holarctic 
*Order  2.  Notoungulata.  Palaeocene-Pleistocene 

*Palaeostylops,  Palaeocene,  Asia;  *Notostylops,  Eocene,  S. 
America;  *Toxodon,  Pleistocene,  S.  America;  *Homalo- 
dotherium,  Miocene,  S.  America;  *Hegetotherinm,  Oligo- 
cene-Miocene,  S.  America 


700 


PROTOUNGULATES 


XXVIII.  3- 


3.  Classification  (cont.) 

*Order  3.  Litopterna.  Palaeocene-Pleistocene.  S.  America 
*Thoatherium,  Miocene;  *Macrauchenia,  Pleistocene 

*Order  4.  Astrapotheria.  Eocene-Miocene.  S.  America 
*Astrapotherium,  Oligocene-Miocene 

Order  5.  Tubulidentata.  Pliocene-Recent 

Orycteropus,  aardvark,  Cape  ant-eater,  Africa 


Fig.  468.  Skeleton  of  *Phenacodus  as  found  in  the  rock. 
(Simplified  after  S.  Woodward  and  Cope.) 


4.  Superorder  Protoungulata 

*Order  Condylarthra 

This  group  includes  animals  so  close  to  the  central  eutherian  stock 
that  it  is  still  disputed  whether  some  of  them  should  be  classified  as 
insectivores,  primates,  or  creodonts.  Five  families  are  recognized,  all 
from  the  Palaeocene  and  Eocene  periods.  The  more  'primitive'  in 
structure,  such  as  the  Eocene  *Hyopsodus,  had  a  complete  row  of 
bunodont,  quadritubercular  teeth,  and  also  short  legs  with  clawed 
digits.  They  were  small  (1  ft  long)  and  perhaps  arboreal,  and  there- 
fore could  be  classified  with  lemurs  or  insectivores.  *Mioclaenus  is 
an  even  older  type,  which  possessed  sharp-cusped  teeth.  *Phenacodus 
(Fig.  468)  is  perhaps  the  best  known  condylarth.  It  was  an  Eocene 
form  with  ungulate  characters  already  present,  including  hoofs  and 
square  bunodont  molars.  The  build  was,  however,  still  that  of  a 
generalized  carnivorous  or  insectivorous  mammal,  with  a  markedly 


xxvm.  s  NOTOUNGULATES  701 

curved  spine,  small  brain-case,  sagittal  crests,  rather  short  limbs  with 
slightly  elongated  metapodials,  the  central  digit  the  longest,  complete 
ulna  and  fibula,  carpus  and  tarsus  not  interlocking,  and  a  long  tail. 
The  animal  was,  however,  rather  large  (4  ft  long).  Smaller  Palaeocene 
phenacodonts,  such  as  *Tetraclaenodon,  still  possessed  claws  and  may 
have  been  very  close  to  the  ancestry  of  all  protoungulate  types.  Evi- 
dently some  10  million  years  of  herbivorous  life  in  the  Palaeocene  had 
produced  only  suggestions  of  the  'ungulate'  facies.  Other  condylarths 
became  more  specialized  in  the  Eocene.  Thus  *Meniscotherium  had 
lophodont  grinders,  though  retaining  the  clawed  digits.  *Didolodus 
and  similar  forms  from  South  America  are  condylarths  that  may 
perhaps  have  given  rise  to  some  of  the  characteristic  South  American 
ungulates  though  they  themselves  survived  to  the  Miocene.  The 
#Periptychidae  were  Eocene  condylarths  probably  ancestral  to  the 
pantodonts.  They  also  show  similarities  to  the  surviving  Orycteropus, 
which  may  be  descended  from  them. 

5.  South  American  ungulates 
*Order  Notoungulata 

The  ungulate  fauna  of  South  America  provides  a  case  of  geographic 
isolation  as  striking  as  that  of  the  marsupials  in  Australia.  In  Palaeo- 
cene times  there  were  ungulates  common  to  South  America  and  the 
rest  of  the  world.  Besides  the  condylarths,  considered  above,  there 
was  the  *Palaeostyhps,  in  the  Palaeocene  of  Asia,  and  the  similar 
*Notostylops  found  in  North  and  South  America.  These  earliest 
notoungulates  showed  only  a  slight  advance  in  size  and  other  features 
from  the  basal  condylarth  condition.  The  teeth  possessed  simple 
ridges.  From  some  such  beginnings  there  quickly  developed,  after  the 
isolation  of  South  America  in  the  Eocene,  a  very  rich  fauna,  including 
many  large  animals.  Specimens  of  these  peculiar  animals  were  first 
collected  by  Darwin  during  the  voyage  of  the  Beagle  and  were  later 
described  by  Owen.  Darwin  records  that  their  characteristics  were 
among  the  earliest  stimuli  that  turned  his  thoughts  to  evolution  (see 
p.  524).  A  characteristic  of  the  group  was  the  very  large  tympanic 
bulla.  The  brain  was  small  and  especially  the  cerebral  hemispheres. 

As  many  as  nine  families  of  notoungulate  can  be  recognized  in  the 
Oligocene;  after  this  period  they  became  less  numerous.  Some  of  them 
persisted  throughout  the  Tertiary,  but  all  became  extinct  in  the 
Pleistocene,  after  the  connexion  with  North  America  was  re-made  and 
competition  was  felt  from  more  modern  types,  both  ungulates  and 
carnivores.  The  notoungulates  known  as  toxodonts  were  very  large 


PROTO UNGULATES 


702  I'KUlUUWLrULAlJiS  XXVIII.  5- 

graviportal  animals,  the  tooth  row  being  curved  to  form  a  bow,  from 
which  the  group  takes  its  name.  The  limbs  were  massive,  with  as  few 
as  three  digits,  the  middle  the  longest,  bearing  hoofs.  *Toxodon  itself 


Macrauchenia       JtfK* 


Thoatherium 


/fy^)) 


Macrauchenia 


Fig.  469.  Various  ungulates.  (After  Zittel,  K.  A.,   Text-book  of  Palaeontology  (revised 

A.  S.  Woodward),  Macmillan  &  Co.,  Romer,  Vertebrate  Paleontology,  Chicago  University 

Press,  and  Scott,  Land  Mammals,  The  Macmillan  Co.)  Lettering  as  Fig.  465. 


(Fig.  469)  survived  to  the  Pleistocene  and  was  a  creature  nearly  10  ft 
long,  with  enormous  head,  short  front  and  long  hind  legs.  *Homalodo- 
therium,  on  the  other  hand,  had  front  legs  longer  than  the  hind,  and 
provided  with  claws.  The  incisors  were  small  but  formed  rows  suitable 
for  cropping.  Probably  the  animals  reared  up  on  their  hind  legs  to 
reach  branches  and  the  large  ischia  show  that  the  muscles  for  this 
were  strong  (p.  634).  The  typotheres  and  hegetotheres  were  small 


xxviii.  7  THOATHERIUM  703 

rabbit-like  creatures  with  gnawing  incisors.  The  notoungulates  thus 
radiated  to  form  various  types  and  for  many  millions  of  years  they 
were  the  dominant  herbivores  of  the  South  American  forests. 


6.  *Order  Litopterna 

Some  descendants  of  the  condylarths  in  South  America  developed 
along  lines  astonishingly  similar  to  the  horses.  The  didolodonts 
already  show  tendencies  in  this  direction  and  are,  indeed,  sometimes 
removed  from  the  condylarths  and  placed  with  the  South  American 
horse-like  forms  in  the  *order  Litopterna.  A  series  of  fossils  shows 
that  members  of  this  order  became  first  digitigrade  and  then  unguli- 
grade,  the  central  metapodials  elongating  and  the  lateral  ones  reduc- 
ing, first  to  three  and  then,  in  *Thoatheriwn  (Fig.  469),  to  a  single  one, 
with  splint  bones  even  smaller  than  remain  in  our  horses.  The  general 
appearance  of  the  limbs  was  very  horse-like,  for  instance  in  the 
grooved  talus,  but  the  carpus  never  became  interlocking.  Other 
respects  in  which  these  litopterns  developed  less  far  than  the  horses 
were  that  the  tooth  row  remained  nearly  complete  and  the  molars 
low-crowned,  though  provided  with  ridges.  A  post-orbital  bar  was 
developed.  These  differences  from  our  horses  are  as  interesting  as  the 
similarities,  and  they  show  that  the  features  of  the  ungulate  facies  do 
not  necessarily  all  evolve  together.  It  is  impossible  to  say  what 
difference  in  conditions  was  responsible  for  forming  horse  feet  on  an 
animal  whose  head  was  only  partly  horse-like. 

These  ungulates  were  presumably  evolved  to  meet  conditions  on 
the  South  American  plains  in  the  Miocene.  It  is  interesting  that  the 
three-toed  types  outlived  the  one-toed  *Thoatherium,  lasting  into  the 
Pliocene.  *Macranchenia  (Fig.  469),  a  creature  looking  like  a  camel 
but  perhaps  living  in  swamps,  was  the  only  Pleistocene  survivor. 


7.  *Order  Astrapotheria 

This  order  includes  some  Oligocene  and  Miocene  South  American 
ungulates,  with  a  short  skull  but  long  lower  jaw,  long  canines,  and 
massive  molar  teeth  (Fig.  469).  There  was  probably  a  proboscis.  The 
feet  were  small  and  perhaps  rested  on  pads.  The  weak  vertebral  spines 
and  transverse  processes  suggest  that  the  animals  may  have  been 
aquatic  and  the  large  lower  canines,  diverging  in  older  animals, 
resemble  those  of  a  hippopotamus. 


7o4  PROTOUNGULATES  xxvm.  8 

8.  Order  Tubulidentata 

The  aardvark  ('earth-pig')  or  Cape  ant-eater,  Orycteropus  (Fig. 
470),  is  a  zoologically  very  isolated  form,  of  unknown  affinities,  placed 
by  Simpson  with  the  Protoungulata,  because  it  is  possibly  not  very 
remote  from  the  condylarths.  It  is  the  size  of  a  small  pig,  with  a  highly 
curved  back,  and  is  much  given  to  digging,  both  for  protection  and  to 
obtain  termites,  which  are  its  main  food.  It  occurs  from  South  Africa 
to  the  Sudan.  There  is  an  elongated  snout,  round  mouth,  and  long 
tongue,  as  in  other  ant-eaters.  The  peglike  teeth  are  unlike  those  in 
any  other  mammal.  They  consist  of  numerous  hexagonal  columns 


1 

Fig.  470.  Orycteropus,  the  aardvark.  (From  life.) 

of  dentine,  separated  by  tubes  of  pulp.  There  is  no  enamel,  though 
enamel  organs  are  present  in  the  tooth  germs.  In  the  adult  there  are 
about  five  teeth  in  each  jaw,  but  there  is  a  full  series  of  rudimentary 
milk  teeth. 

There  are  special  arrangements  in  the  mouth  and  throat  to  allow 
the  animal  to  bury  its  snout  in  a  mass  of  termites  and  then  to  swallow 
them  while  continuing  to  breathe.  There  are  large  salivary  glands. 
The  digits  (4  in  hand  and  5  in  foot)  are  covered  by  structures  some- 
times referred  to  as  compressed  nails,  sometimes  as  hoofs.  There  is 
a  strong  clavicle  and  complete  radius  and  ulna  and  tibia  and  fibula. 
The  limbs  are  thus  specialized  for  digging,  but  retain  the  characters 
of  the  earliest  mammals.  The  head  is  long  and  the  brain  small  and  of 
an  extremely  primitive  type,  with  extensive  olfactory  regions  and  very 
small  neopallium.  The  olfactory  turbinals  are  better  developed  than 
in  any  other  mammal;  the  aardvarks  find  termites  by  their  scent. 
The  animals  are  nocturnal  and  the  retina  has  only  rods,  and  a  tapetum. 
The  ears  are  long  and  hearing  acute  and  there  are  bristles  on  the  long 
mobile  snout.  The  uterus  is  paired  and  the  placenta  of  a  zonary  type, 
somewhat  like  that  of  carnivores.  There  is  a  very  large  allantois. 


xxviii.  8  AARDVARKS  705 

Orycteropus  occurs  as  fossils  back  to  the  Miocene.  Its  earlier  history 
is  unknown,  but  similar  teeth  have  been  reported  from  the  Eocene, 
and  many  features  of  the  skeleton  are  strikingly  like  those  of  condy- 
larths.  The  animal  obviously  retains  many  characters  that  were 
present  in  the  earliest  eutherians,  the  fact  that  it  is  placed  by  some  as 
an  edentate  or  insectivore  and  by  others  close  to  the  base  of  the  un- 
gulate stock  suggests  that  it  has  diverged  relatively  little  from  the 
ancestor  of  all  eutherians. 


XXIX 

ELEPHANTS  AND  RELATED  FORMS 

1.  'Near-ungulates',  superorder  Paenungulata 

From  the  Palaeocene  ungulate  stock,  when  it  was  yet  hardly  differ- 
entiated from  that  of  other  mammals,  there  diverged  several  lines  of 
herbivorous  animals  and  these  rapidly  increased  and  diversified  in  the 
Eocene,  many  of  them  becoming  very  large.  Most  of  these  lines 
declined  in  the  Oligocene  and  only  the  huge  elephants  and  tiny 
hyraxes  remain  today  to  show  approximately  the  structure  of  this 
range  of  Eocene  pantodonts,  dinocerates,  and  other  forms.  The  highly 
specialized  Sirenia  (sea-cows)  were  also  an  early  offshoot  of  this  type 
of  animal.  The  various  lines  diverged  so  very  long  ago  that  we  should 
hardly  expect  to  find  that  they  have  much  in  common  that  they  do  not 
share  with  other  ungulates,  or  indeed  with  all  mammals,  but  it  has 
long  been  recognized  that  there  is  a  loose  grouping  of  orders  around 
the  elephants  and  hyraxes.  Simpson  suggests  the  name  Paenungulata 
('near  ungulates')  for  these  forms  that  are  all  slightly,  but  not  much, 
beyond  the  protoungulate  level.  The  legs  of  all  of  them  remain  rather 
primitive,  with  long  upper  segments,  complete  ulna  and  fibula,  and 
several  digits,  and  without  well-marked  hoofs.  The  incisors  and 
canines  often  become  reduced  to  single  pairs  of  large  tusks  in  each 
jaw  and  the  molars  are  specialized  for  grinding,  with  the  development 
of  cross-ridges. 

2.  Classification 

Superorder  3.  Paenungulata 
Order  1.  Hyracoidea.  Oligocene-Recent.  Palearctic,  Africa 
Procavia  (=  Hyrax),  hyrax,  Africa,  Asia 

Order  2.  Proboscidea.  Eocene-Recent 

#Family  1.  Moeritheriidae.  Eocene-Oligocene.  Africa 

*Moeriiherium 
*Family  2.  Deinotheriidae.  Miocene-Pleistocene.  Eurasia,  Africa 

*Deinotherium 
*Family  3.  Gomphotheriidae.  Oligocene-Pleistocene.  Holarctic, 
S.  America,  Africa 
*Palaeomastodon,  Lower  Oligocene,  Africa;  *Phiomia,  Oligo- 
cene, Africa;  *Gomphotherium  (=  *Trilophodon),  Miocene- 


xxix.  i-3  CLASSIFICATION  707 

Pliocene,  Holarctic,  Africa;  *Serridentinns,  Miocene -Plio- 
cene, Holarctic;  *Anancus  (=  *Pentalophodon),  Pliocene- 
Pleistocene,  Eurasia;  *Stegomastodo?ii  Pliocene-Pleistocene, 
N.  and  S.  America 

*Family  4.  Mammutidae.  Miocene-Pleistocene.  Holarctic 
*Mammut  ( =  *  Mastodon  =  *  Zygolophodon  =  *  Turicins) 

Family  5.  Elephantidae.  Pliocene-Recent.  Holarctic,  Africa 
*Stegolophodon,  Miocene-Pleistocene,  Eurasia;  *Stegodon, 
Pliocene-Pleistocene,  Asia;  *Mammuthus  (  =  *Mammontens 
=  *Archidiskodon),  mammoth,  Pleistocene,  Holarctic, 
Africa,  S.  America;  Loxodonta,  African  elephant,  Pleisto- 
cene-Recent; Elephas,  Indian  elephant,  Pleistocene-Recent. 

*Order  3.  Pantodonta.  Palaeocene-Eocene.  Holarctic 

*Pantolambda,  Palaeocene;  *Coryphodon,  Palaeocene-Eocene 

*Order  4.  Dinocerata.  Palaeocene-Eocene.  Holarctic 

*  Uintatherium,  Eocene 

*Order  5.  Pyrotheria.  Palaeocene-Oligocene.  S.  America 

*  Pyrotherium,  Oligocene 

*Order  6.  Embrithopoda.  Oligocene.  Africa 
*A  rsinoitherium 

Order  7.  Sirenia.  Sea-cows.  Eocene-Recent 

*Protosiren,  Eocene;  Dugong  (=  Halicore),  sea-cow,  Indian 
Ocean  and  Pacific;  Manatus  (=  Trichechus),  manatee, 
Atlantic 


3.  Order  Hyracoidea 

The  hyraxes  or  conies  (Fig.  471)  are  animals  that  live  in  Africa  and 
neighbouring  regions  and  have  persisted  throughout  the  Tertiary  as 
small  herbivorous  creatures,  occupying  similar  niches  to  rabbits,  which 
they  resemble  superficially  in  some  ways.  Fossils  are  known  in  Africa 
back  to  the  Oligocene  and  probably  the  group  existed  before  that  time 
and  therefore  shows  us  something  of  the  appearance  of  smaller  Eocene 


708  ELEPHANTS  xxix.  3- 

and  Oligocene  ungulates.  The  gait  is  plantigrade,  with  four  anterior 
and  three  posterior  digits,  carrying  somewhat  hoof-like  nails,  except 
for  a  sharp  bifid  claw,  used  for  toilet  purposes,  on  the  inner  hind  toe 
(Fig.  472).  There  is  a  single  pair  of  continually  growing  incisors  in  the 
upper  and  two  in  the  comb-like  lower  jaw.  There  is  a  diastema  and 
seven  grinding  molariform  teeth  of  bunoselenodont  type,  with  trans- 
verse ridges,  recalling  those  of  brontotheres.  The  lower  jaw  is  very 
deep,  for  the  attachment  of  the  masseter  muscle,  and,  as  is  usual  in 


Fig.  472.  Skeleton  of  Procavia. 

ungulates,  the  post-orbital  bar  is  nearly  or  quite  complete.  There  is  a 
serial  carpus  with  a  centrale,  an  unusually  primitive  feature  for  an 
ungulate.  The  intestine  provides  chambers  for  digestion  by  symbionts. 
In  the  large  median  caecum  are  found  enormous  ciliates  (Pycnothrtx), 
up  to  5  mm  long,  and  a  fauna  of  cellulose-splitting  bacteria.  Beyond 
this  lies  a  further  pair  of  caeca. 

The  brain  is  of  macrosmatic  type.  As  in  the  elephants,  the  testis 
fails  to  descend  and  remains  close  to  the  kidney,  there  being  no  sign 
of  a  scrotum  or  inguinal  canal.  The  uterus  is  paired,  and  the  placenta 
at  first  covered  with  foetal  villi,  later  restricted  to  a  zonary  arrange- 
ment, superficially  similar  to  that  of  carnivores,  but  with  a  haemo- 
chorial  structure  with  a  resemblance  to  that  of  Tarsius.  There  is  a 
single  pair  of  pectoral  mammae. 

Various  species  of  Procavia  are  common  throughout  Africa  (not 
Madagascar),  Arabia,  Palestine,  and  Syria,  living  in  desert  regions  in 
colonies  under  rocks.  They  do  not  dig  burrows,  the  feet  being  flat- 
tened and  well  suited  for  moving  over  smooth  rock  surfaces.  The 


xxix.  4  GENERA   OF   ELEPHANTS  709 

related  Dendrohyrax  live  in  the  trees.  Earlier  hyraxes  were  sometimes 
as  large  as  small  horses  (*Megalohyrax  from  the  Oligocene). 

4.  Elephants.  Order  Proboscidea 

The  late  Henry  Fairfield  Osborn,  one  of  the  greatest  zoologists  of 
his  time,  devoted  a  great  part  of  a  long  working  life  and  the  large 
resources  available  to  him  at  the  American  Museum  of  Natural 
History  to  the  study  of  the  evolution  of  elephants.  It  cannot  be  said 
that  he  was  able  as  a  result  of  all  this  study  to  draw  conclusions  that 
have  revolutionized  biology,  and  this  failure  is  in  a  sense  a  measure 
of  the  immaturity  of  our  science.  The  elephants  have  shown  great 
and  relatively  rapid  changes  in  recent  geological  times  and  have  left 
abundant  remains,  especially  of  their  large  and  hard  teeth.  We  may 
therefore  take  knowledge  about  evolution  of  elephants  as  a  fair  example 
of  the  most  that  can  be  known  of  the  evolutionary  processes  in  large 
mammals ;  if  the  study  of  this  great  mass  of  material  leaves  us  in  a  state 
of  confusion  rather  than  of  certainty  we  shall  be  warned  to  suspect  the 
apparent  clarity  of  other  alleged  evolutionary  sequences,  and  to  dis- 
trust dogmatic  statements  about  the  'causes'  of  evolutionary  change. 

The  two  existing  types  of  elephant,  referred  to  distinct  genera,  live 
still  in  considerable  numbers  in  Africa  (Loxodonta)  and  Asia  (Elephas). 
They  are  survivors  of  a  much  larger  population,  reaching  its  greatest 
variety  in  Pliocene  times.  The  essential  feature  of  the  type  is  the  great 
size  (11 1  ft  high  in  Loxodonta)  and  the  presence  of  a  special  food- 
collecting  system  able  to  gather  enough  raw  material  to  support  such 
a  large  living  mass.  Of  the  various  factors  influencing  the  optimum 
size  for  a  given  animal  type,  all  those  favouring  increase  must  be 
present  in  the  ingredients  of  elephant  life.  Elephants  are  larger  than 
any  other  land  animals,  living  or  extinct,  except  perhaps  the  huge 
Oligocene  rhinoceros  *Baluchitherium  and  some  of  the  largest  dino- 
saurs (if  these  were  indeed  terrestrial). 

The  basal  metabolism  of  a  mammal  increases  only  with  about  the 
two-thirds  power  of  its  weight,  so  that  larger  animals  need,  on  this 
account,  relatively  less  food.  But,  as  Watson  (1946)  has  pointed  out, 
the  output  of  energy  by  the  muscles  is  proportional  to  the  weight  of 
the  muscle;  the  total  intake  needed  is  therefore  proportional  to  some 
power  between  two-thirds  and  the  first  power  of  the  weight  of  the 
whole,  being  'larger  the  greater  and  more  continuous  the  activity  of 
the  animal'.  Elephants,  as  he  further  comments,  are  very  active  when 
wild,  their  playfulness  and  strength  are  proverbial,  and  often  a 
nuisance  to  man.  They  manage  to  collect  their  food  with  sufficient 


710  ELEPHANTS  xxix.  4 

economy  of  energy,  though  to  do  this  they  must  eat  throughout  a 
large  part  of  the  day,  perhaps  for  as  much  as  18  hours.  Here  another 
factor  has  to  be  considered,  namely,  the  area  of  tooth  available  for 
grinding  the  food.  This  will  vary  approximately  as  the  two-thirds 
power  of  the  total  weight;  as  the  animals  become  larger  the  tooth 
surface  needs  therefore  to  be  relatively  increased. 


Fig.  473.  Section  of  tooth  of  elephant.  The  front  part  of  the 

crown  (on  the  left)  is  already  worn  away.  Notice  the  upstanding 

enamel  lamellae,  which  reach  to  the  base  of  the  tooth.  Dentine 

is  shown  dotted,  cement  by  lines  (From  Weber.) 

With  these  factors  in  mind  we  shall  recognize  that  the  significant 
features  in  the  organization  of  elephants  are  that  they  are  very  large 
animals,  with  an  efficient  nervous  organization  for  finding  the  food, 
efficient  means  of  collecting  it,  and  large  surfaces  for  grinding  it. 

The  trunk  is  the  main  means  of  collection — an  enormously  elongated 
nose  and  upper  lip,  with  appropriate  muscles  and  sensitive  grasping 
tip.  The  muscles  have  been  developed  chiefly  from  the  parts  of  the 
facial  musculature  that  are  responsible  for  moving  the  sides  of  the 
nose.  The  trunk  probably  developed  rather  quickly,  in  late  Miocene 
times,  perhaps  10-15  million  years  ago;  the  earlier  elephants  of  the 
Miocene  possessed  very  long  lower  jaws,  which  became  shortened 
as  the  trunk  developed.  Any  tall  animal  must  have  means  of  reaching 
the  ground  and  the  trunk  is  probably  superior  even  to  a  very  long 
neck  for  this  purpose,  because  it  can  reach  upwards  and  sideways  as 
well  as  downwards. 

Only  one  pair  of  continually  growing  incisors  remains  in  modern 


xxix.  4  TEETH  711 

elephants,  forming  the  two  enormous  upcurved  tusks,  up  to  11^  ft 
long  in  Loxodonta,  composed  of  solid  dentine  except  for  a  temporary 
cap  of  enamel  at  the  tip.  This  mass  of  ivory  is  no  doubt  useful  for 
defence  and  perhaps  in  food  collection,  but  it  seems  to  be  a  consider- 
able waste  of  calcium  and  phosphorus,  not  to  mention  of  the  energy 
necessary  to  carry  the  350  lb  weight.  This  weight  is  balanced  against 
that  of  the  body,  upon  the  pillar-like  front  legs,  and  it  is  perhaps  not 
fantastic  to  suggest  that  the  tusks  serve  partly  as  counterweights,  for 


/77./  rn.m.4 


Fig.  474.  Skull  of  young  Indian  elephant.  The  roots  of 

the  teeth  have  been  exposed. 
al.  alisphenoid;  bo.  basioccipital;  eo.  exoccipital ; /.  frontal; 
j.  jugal;  m.  maxillary;  m.i.  first  molar;  tn.m.  J  and  4.  third  and 
fourth  milk  molars;  p.  parietal;  pm.  premaxillary ;  so.  supra- 
occipital;  sq.  squamosal.  (After  Reynolds,  The  Vertebrate 
Skeleton,  Cambridge  University  Press.) 

purposes  of  balance  (see  p.  697),  extravagant  though  such  an  arrange- 
ment may  be.  However,  the  weight  of  the  head  is  reduced  by  extensive 
development  of  air  sinuses  between  the  inner  and  outer  tables  of  the 
bones  of  the  skull.  The  tusks  are  smaller  in  females  and  in  the  Indian 
than  in  the  African  elephant;  in  the  female  Indian  elephant  they  do 
not  project  beyond  the  lips.  This  difference  may  be  connected  with 
the  relatively  small  size  of  these  females. 

The  essential  features  of  the  grinding  apparatus  are  the  immensely 
large  molars  (Fig.  473),  with  numerous  sharp  transverse  ridges,  by 
which  all  sorts  of  plants,  including  hard  grasses,  are  chopped  into 
small  fragments.  There  are  three  small  premolars,  which  are  soon 
shed,  and  the  three  molars  are  then  developed  in  a  series  and  used 
one  after  the  other.  By  a  special  arrangement  of  the  palate  (Fig.  474) 
the  teeth  are  allowed  to  form  high  up  in  the  skull,  so  that  each  tooth 
has  a  very  great  area,  made  up  by  the  fusion  of  as  many  as  twenty- 


712 


ELEPHANTS 


xxix.  4 


seven  separate  'plates',  which  develop  as  separate  cones  of  dentine 
and  enamel,  each  with  its  own  pulp  cavity,  the  cones  being  finally 
joined  together  by  cement.  The  teeth  are  placed  just  above  the 
ascending  ramus  of  the  mandible,  so  that  the  large  jaw-muscles  work 
at  maximum  advantage.  For  their  attachment  the  skull  becomes 
extremely  short  and  high,  with  the  development  of  large  air  spaces 


Fig.  475.  Skeleton  of  an  Indian  elephant.  (From  Owen,   The  Anatomy  of  Vertebrates, 

Longmans,  Green  &  Co.) 


between  its  tables.  This  shape  also  allows  a  large  occipial  region  for 
the  muscles  that  hold  up  the  head. 

With  this  head  structure  the  elephants  have  been  able  to  grow  to  a 
size  that  must  approach  the  limit  possible  for  a  fully  terrestrial 
animal.  The  backbone  (Fig.  475)  is  based  on  a  'single  girder'  plan, 
with  as  many  as  twenty  ribs,  and  high  thoracic  neural  spines,  forming 
together  a  huge  beam  that  carries  the  weight  of  the  abdomen  and 
balances  it  on  the  fore-legs  against  the  weight  of  the  head,  the  hind- 
legs  acting  as  propellents.  The  ilium  is  nearly  vertical  and  expanded 
transversely  for  the  attachment  of  the  large  gluteal,  iliacus,  abdominal 
and  sacrospinalis  muscles.  The  acetabulum  faces  downwards. 

As  in  other  heavy  animals  the  legs  are  enormous  pillars,  with  long 


xxix.  4  ELEPHANT    CHARACTERS  713 

upper  segments  and  no  great  extension  of  the  lower.  The  ulna  and 
fibula  are  complete  and  bear  part  of  the  weight,  the  ulna  and  radius 
being  held  permanently  crossed  in  a  fixed  position  of  pronation. 
Walking  is  of  a  modified  digitigrade  type;  all  three  of  the  short 
phalanges  of  each  digit  reach  the  ground,  but  the  greater  part  of  the 
weight  is  taken  by  a  pad  of  elastic  tissue  at  the  back  of  the  foot. 
There  are  five  digits  in  each  foot,  united  by  a  web  to  make  a  firm  basis, 
and  having  small,  flat,  somewhat  hoof-like  nails  at  the  tips.  The  ribs 
carry  so  much  weight  that  respiration  is  almost  wholly  diaphragmatic 
and  the  lungs  are  fused  to  the  walls  of  the  thoracic  cavity  by  elastic 
tissue. 

The  soft  parts  of  elephants  show  some  features  retained  unmodified 
from  their  early  ungulate  ancestry.  Thus  the  cerebral  hemispheres 
are  relatively  rather  small  and  leave  the  cerebellum  uncovered.  In 
other  respects  the  brain  is  well  developed,  it  has  a  greater  absolute 
size  than  that  of  any  other  land  mammal  (6,700  cm3).  The  proverbial 
intelligence  and  memory  capacity  have  been  verified  by  experiment. 
Smell,  hearing,  and  the  tactile  organs  of  the  trunk  provide  the  main 
receptors,  vision  being  less  developed.  Like  many  other  animals  with 
large  brains  there  is  a  long  period  of  post-natal  growth  and  life  is  social. 
Much  information  is  no  doubt  learned  from  other  individuals,  and 
it  has  been  shown  that  elephants  can  learn  to  discriminate  between 
upwards  of  100  pairs  of  visual  situations. 

In  spite  of  the  specialization  of  the  head  for  a  herbivorous  diet,  the 
stomach  and  intestine  remain  simple  and  there  is  no  special  large 
fermentative  chamber,  though  the  caecum  is  long  and  sacculated  and 
there  is  an  ileocaecal  sphincter. 

The  testes  are  remarkable  in  that,  as  in  other  paenungulates,  they 
lie  close  to  the  kidneys,  and  have  made  no  movement  of  descent  into 
a  scrotum.  The  two  horns  of  the  uterus  remain  separate,  though  united 
externally.  Only  one  young  is  born  at  a  time,  after  a  gestation  of 
twenty-two  months.  The  placenta  has  a  superficial  similarity  to  the 
zonary  arrangement  of  carnivores,  but  in  structure  resembles  that  of 
hyraxes  and  sirenians.  At  the  poles  are  areas  of  diffuse,  non-deciduate 
placenta  while  in  an  annular  zone  round  the  middle  there  is  much 
invasion  of  the  trophoblast,  the  details  of  which  are  not  known. 
Development  is  slow  and  Asian  elephants  reach  puberty  at  about  13- 
14  years,  African  elephants  rather  earlier. 

The  earliest-known  member  of  the  elephant  line,  * Moeritherium, 
from  the  Upper  Eocene  of  Egypt,  was  only  2  ft  high  and  was  probably 
partly  aquatic,  with  eyes  and  ears  placed  high,  as  in  the  hippopotamus. 


(7H) 


Fig.  476.  Chart  of  the  evolution  of  the  paenungulate  orders.  The  animals  are  shown 
reconstructed  following  Andrews,  Osborn,  and  others  and  their  size  is  indicated  approxi- 
mately. Some  stages  in  development  of  the  molar  teeth  are  also  shown. 


xxix.  4  EVOLUTION  OF  ELEPHANTS  715 

The  skull  was  elongated  and  small  tusks  were  present,  but  the  denti- 

'2. 1. 'J. "3 

tion  was  nearly  complete,  .  The  molars  were  bunodont  and 

2.0.3.3 

carried  only  two  cross  lophs,  a  condition  easily  derived  from  that  of 

a  condylarth  quadritubercular  tooth.  From  some  such  animal  arose 

ultimately  so  great  a  collection  of  types  that  Osborn  in  his  study  of  the 

group  recognized  350  species,  only  two  living  at  the  present  day. 

*Moeritherium  survived  into  the  Lower  Oligocene,  where  there  is 

found  also  *Phiomia,  about  twice  as  large.  Both  upper  and  lower  jaws 

of  this  animal  carried  tusks  and  the  whole  front  of  the  head  was 

greatly  elongated,  with  formation  of  a  long  diastema.  The  wear  of  the 

lower  incisors  shows  that  they  were  used  for  digging.  The  molars 

carried  three  low  ridges  and  were  all  used  together,  not  successively. 

The  similar  *Palaeomastodon  lived  at  the  same  time  and  was  about 

6  ft  high. 

After  this  period  there  is  a  gap,  probably  covering  10  million  years 
or  more,  in  our  knowledge  of  elephant  evolution,  but  it  is  clear  that 
throughout  this  long  period  the  stock  must  have  continued  with  little 
change,  as  a  race  of  animals  with  long  digging  tusks  and  rather  mobile 
face  and  lips,  becoming  gradually  larger  and  elongating  the  face  more 
and  more  to  enable  the  ground  to  be  reached.  In  the  Miocene  is  found 
a  considerable  variety  of  these  long-jawed  animals,  the  various  species 
of  the  genus  *Gomphotherium  (=  *Trilophodon).  The  teeth  of  the 
earliest  of  these  long-faced  elephants  were  used  all  at  once,  not  in 
series;  later  the  premolar  teeth  tended  to  be  reduced  and  the  molars 
became  covered  with  an  increasing  number  of  cusps,  arranged  to  make 
a  number  of  cross-ridges,  seldom,  however,  more  than  five.  From  the 
low  cusps  they  are  known  loosely  as  'mastodonts',  but  the  colloquial 
terms  for  description  of  elephants  are  used  in  senses  almost  as  varied 
as  the  'scientific'  names;  as  in  other  branches  of  knowledge,  great 
abundance  of  information  has  led  to  confusion  of  terminology. 

From  this  Miocene  stage  onwards  the  study  of  proboscidean  evolu- 
tion becomes  a  desperate  attempt  to  sort  out  huge  numbers  of  fossil 
specimens  (often,  however,  only  molar  teeth)  into  truly  phylogenetic 
lines.  Osborn  made  an  heroic  effort  to  recognize  only  fully  docu- 
mented sequences,  but  even  with  the  wealth  of  material  available  it 
is  rarely  possible  to  say  with  complete  certainty  that  one  type  has 
evolved  into  another.  The  interpretations  of  the  sequences  and  their 
expression  in  classificatory  terms  vary  considerably  even  in  the  hands 
of  the  most  careful  interpreters  of  Osborn's  work.  However,  it  is 
probable  that  in  this  mass  of  material  there  can  be  seen  several  distinct 


716  ELEPHANTS  xxix.  4- 

lines,  in  which  evolution  proceeded  in  a  parallel  manner.  From  the 
end  of  Miocene  times  onwards  the  very  elongated  jaws  began  to 
shorten,  and  it  was  presumably  at  this  time  that  the  trunk  became 
long  and  the  typical  elephant-like  habit  was  adopted.  Certainly  not 
all  animals  having  elephant-like  appearance  belong  to  the  'main' 
elephant  line,  and  the  shortening  of  the  lower  jaw  took  place  at 
different  times  in  the  various  stocks.  Thus  the  members  of  the 
Pliocene  and  Pleistocene  genus  *Anancus,  though  extremely  like 
elephants  in  general  shape,  had  bunomastodont  molars.  This  line 
retained  little  cusps  between  the  main  ridges,  such  as  were  present  in 
the  Miocene  gomphotheres.  *Stegomastodon  was  a  related  animal  that 
lived  on  in  South  America  until  as  late  as  a.d.  200. 

The  species  of  * Serridentinus  represent  another  line.  Here  there 
were  no  little  cusps  on  the  teeth,  but  the  grinding  area  was  increased 
by  extra  'serrate'  ridges.  This  type  retained  the  long  lower  tusks  into 
the  Pliocene,  but  then  tended  to  shorten  them,  though  never  to  the  full 
elephant  condition.  The  line  that  produced  the  modern  elephants  can 
first  be  recognized  in  the  Lower  Miocene,  by  the  fact  that  the  cusps 
are  united  into  sharp  ridges.  This  condition  presumably  marks  the 
transition  to  feeding  on  hard  grasses,  which  have  to  be  cut,  rather 
than  on  softer  stalks,  which  can  be  ground.  Some  members  of  this 
'zygolophodont'  stock  retained  few  ridges,  and  presumably  a  browsing 
diet,  even  into  the  Pleistocene,  although  they  acquired  short  lower 
jaws  like  those  of  the  elephants.  These  animals  are  therefore  'masto- 
dons', and  it  is  unfortunate  that  the  rules  of  priority  require  that  they 
shall  be  called  *Mammut  (=  *Zygolophodori).  In  * Stegolophodon  and 
*Stegodon  of  the  Upper  Pliocene  and  Pleistocene,  however,  the  lower  jaw 
was  already  short  and  the  arrangement  of  the  skull  elephant-like,  with 
huge  curved  upper  tusks.  From  some  such  form  the  two  modern  ele- 
phants {Loxodonta  and  Elephas)  and  the  mammoths  (*Mamtnuthus) 
have  been  derived,  but  the  details  of  the  evolutionary  sequence  become 
here  even  more  involved.  We  possess  such  great  numbers  of  teeth,  show- 
ing all  sorts  of  detailed  differences,  that  to  arrange  them  in  evolutionary 
sequences  is  mostly  a  matter  of  guesswork.  Osborn  preferred  not  to 
deal  with  individual  teeth  but  only  with  the  fifty  or  so  complete  skulls 
that  have  been  found,  and  these  fall  into  three  groups.  The  mam- 
moths, * Mammuthus  (=  * Archidiskodon  =  *Mammonteus)  had  very 
long  curved  tusks,  turned  upwards  at  the  tips.  There  were  several 
'species',  including  such  forms  as  M.  primigenius,  the  woolly  mam- 
moth, common  in  Europe  during  the  Pleistocene  and  surviving  until 
recently  in  Alaska  and  Siberia.  Many  carcasses  of  these  animals  have 


xxix.  5  PARALLEL  EVOLUTION  717 

been  found  in  frozen  soil  and  glaciers,  allowing  study  of  the  soft  parts 
and  contents  of  the  stomach. 

Loxodonta,  the  African  elephant,  has  straighter  tusks  and  the  sur- 
face of  the  molars  wears  to  a  diamond-shaped  pattern.  In  Elephas 
the  tusks  are  also  nearly  straight  and  the  molar  ridges  are  parallel. 
There  are,  of  course,  numerous  other  differences  between  the  two 
modern  elephants  and  it  is  not  possible  to  trace  out  in  detail  the 
ancestry  of  the  two  types  and  of  the  mammoths.  In  fact  one  lesson  to 
be  learned  from  the  study  of  elephant  evolution  is  that  mammalian 
fossil  remains  are  seldom  sufficiently  abundant  to  allow  study  of  the 
details  of  evolutionary  history.  There  is  usually  some  doubt  about  the 
exact  relationship  of  the  bones  and  teeth  that  are  found.  Phyletic 
lines  are  constructed  by  careful  comparison  of  the  characters  of  the 
fossils,  there  is  seldom  direct  evidence  of  the  genetic  relationship  of 
any  two  types.  In  the  present  instance  it  is  probable  that  from  the 
gomphotheres  of  Miocene  times  onwards  the  lower  jaw  began  to 
shorten  and  the  skull  to  achieve  an  elephant-like  form  in  at  least  four 
separate  stocks  (perhaps  far  more).  *Anancus  and  the  true  elephan- 
tines  evolved  faster  in  this  direction  than  * Serridentinns  and  *Mammut, 
both  of  which  retained  the  'mastodont'  characters  associated  with 
browsing  even  into  the  Pleistocene.  The  existence  of  parallel  evolu- 
tion may  be  regarded  as  established  beyond  reasonable  doubt  in  this 
case ;  evidently  there  was  some  feature  either  in  environmental  change 
or  internal  'tendency',  or  in  both,  leading  all  these  stocks  to  change  in 
similar  ways,  though  at  different  times  and  rates. 

*Deinotheriam  was  a  distinct  type  of  elephant,  separate  from  all 
others  from  Miocene  times  or  earlier.  There  were  down-turned  lower 
tusks  and  probably  also  a  trunk.  There  were  several  molars  in  the 
tooth  row  and  the  full  elephant  specializations  did  not  develop.  The 
animals  remained  similar  in  structure  for  a  long  period,  but  became 
very  large  before  they  disappeared  in  the  Pleistocene.  This  is  a  good 
example  of  the  development  of  different  variants  of  a  type;  deinotheres 
had  the  trunks  but  not  the  molars  of  elephants. 

5.  *Order  Pantodonta  (Amblypoda) 

During  the  Palaeocene  and  Eocene  the  ungulate  stock  produced 
various  large  herbivores  and  these  may  be  referred  to  the  paenungulate 
group.  The  relationships  of  the  numerous  types  discovered  are  still 
obscure  and  classification  is  probably  not  yet  final.  The  animals  here 
placed  (following  Simpson)  in  the  order  *Pantodonta  were  formerly, 
with  others,   known  as  amblypods  ('blunt  feet').   The  Palaeocene 


7i8  ELEPHANTS  xxix.  5-8 

* Pantolambda  was  about  3-4  ft  long,  with  a  long  face  and  tricuspid 
molars.  The  limbs  were  short  and  broad,  and  the  pelvis  very  like  that 
of  Phetiacodus . 

Later  members  of  the  group,  such  as  *Coryphodon  (Fig.  477),  were 
over  8  ft  long  and  heavily  built,  with  some  formation  of  ridges  on  the 
teeth,  and  feet  with  five  digits;  some  had  simple  hoofs,  others  claws. 
The  brain  was  small  and  evidently  these  were  clumsy  creatures,  suc- 
cessful for  a  time  in  Europe,  Asia,  and  America,  but  unable  to  com- 
pete with  later  herbivores. 

6.  *Order  Dinocerata 

These  were  even  larger  animals,  of  the  same  general  graviportal 
build  as  the  Pantodonta,  and  were  previously  classed  with  the  latter 
as  Amblypoda.  The  two  pairs  of  horns  as  well  as  nasal  protuberances 
and  very  large  dagger-like  canines  provided  weapons  of  defence.  The 
molars  showed  folds  and  ridges  and  provided  a  reasonably  efficient 
grinding  battery.  *Uintatherhim  (Fig.  477)  was  a  typical  Eocene  form; 
even  though  the  brain  was  small  and  the  gait  clumsy,  the  animals  were 
evidently  successful  at  the  time,  and  reached  a  size  as  great  as  that 
achieved  by  any  other  land  mammals  except  the  elephants. 

7.  *Order  Pyrotheria 

*Pyrotherium  and  its  allies  (Fig.  477)  were  Eocene  and  Oligocene 
South  American  ungulates  and  they  are  usually  classed  with  Notoungu- 
lata,  but  more  for  geographical  than  phylogenetic  reasons.  They  were 
remarkably  similar  to  elephants,  for  instance  in  their  large  size  and  in 
the  dorsal  nostril,  suggesting  the  presence  of  a  trunk.  The  incisors 
were  developed  into  tusks  and  the  molar  teeth  carried  two  transverse 
rows  of  cusps,  as  in  bilophodont  early  proboscidians.  The  similarities 
of  the  two  groups  are  striking,  but  they  probably  indicate  only  com- 
mon early  ungulate  derivation  and  provide  another  instance  of 
convergence. 

8.  *Order  Embrithopoda 

*Arsinoitherium  from  the  Lower  Oligocene  of  Egypt  was  another 
large  creature  that  may  be  placed  here.  Its  limbs  resembled  those  of 
elephants,  with  five  semi-plantigrade  digits.  There  was  a  pair  of 
enormous  nasal  horns,  with  a  keratinous  covering  like  that  of  rumin- 
ants, also  smaller  frontal  horns.  There  was  a  regular  tooth  row,  with 
no  enlargement  of  the  incisors  or  canines  and  hypsodont  molars. 


(719) 


Pyrotherium 


Coryphodon 


Uintatherium 


Fig.  477.  Skeletons  of  a  pantodont,  a  dinocerate,  and  a  pyrothere.  (After 

Woodward,  Outlines  of  Vertebrate  Palaeontology,  Cambridge  University  Press, 

Flower  and  Lydekker,  Mammals,  A.  &  C.  Black,  Ltd.,  and  Romer,  Vertebrate 

Paleontology,  University  of  Chicago  Press.) 


720  ELEPHANTS  xxix.  9 

9.  Order  Sirenia 

The  sea-cows  are  herbivorous  creatures,  living  along  the  coasts 
and  in  rivers,  and  highly  adapted  to  aquatic  life.  There  is  little  doubt, 
however,  that  they  have  reached  this  condition  by  modification  of  a 
basic  ungulate  type  of  organization,  probably  not  very  different  from 
that  of  the  early  proboscidians.  The  two  modern  forms,  the  manatee 
of  the  Atlantic  (Fig.  478)  and  dugong  of  the  Pacific  and  Indian  oceans, 
are  different  in  many  respects  and  represent  lines  that  have  been 
separate  for  a  long  time,  probably  since  the  Eocene.  Manatus  (  = 
Trichechus)  has  three  species  on  the  Atlantic  coasts  and  in  the  rivers  of 


Fig.  478.  Manatee,  Manatus.  (From  photographs.) 

Africa  and  America.  Dugong  (=  Halicore)  is  a  purely  marine  animal 
extending  from  the  Red  Sea  throughout  the  Indian  Ocean  to  Formosa 
and  Australia.  Rhytina  (Steller's  sea-cow)  was  an  Arctic  form  that 
became  extinct  in  the  eighteenth  century. 

Sea-cows  have  a  'streamlined'  body-form,  with  few  hairs  and  thick 
'blubber'.  There  are  no  hind-limbs  and  the  pelvic  girdle  remains  only 
as  small  rods  to  which  the  corpus  cavernosum  is  attached  in  the 
male.  The  fore-limbs  are  large,  the  digits  joined  to  form  paddles, 
with  a  full  pentadactyl  structure  and  no  hyperphalangy  or  hyper- 
dactyly.  The  caudal  vertebrae  are  well  developed  and  swimming  is 
effected  by  the  body  and  tail,  the  latter  carrying  a  terminal  horizontal 
fin.  The  vertebrae  articulate  with  each  other  by  flat  surfaces,  as  in 
other  aquatic  forms,  but  there  are  zygapophyses,  and  the  whole 
column  is  not  quite  reduced  to  the  condition  of  a  simple  compression 
strut.  The  bones  have  a  characteristic  structure  (pachyostosis),  prob- 
ably produced  by  lack  of  stressing.  The  manatee  has  only  six  cervical 
vertebrae.  The  ribs  are  round  and  the  diaphragm  is  oblique,  as  in  ele- 
phants and  whales,  allowing  the  lungs  to  reach  far  back.  Respiration 
is  probably  mainly  by  means  of  the  barrel-like  ribs.  The  lungs  contain 


xxix.  9  SEA-COWS  721 

large  air-sacs.  Sea-cows  remain  submerged  only  for  relatively  short 
periods  (10  minutes).  The  blood  system  shows  retia  mirabilia  in  the 
brain  and  elsewhere,  as  in  other  aquatic  mammals  (p.  692).  The  brain 
is  small  and  the  ventricles  exceptionally  large.  The  forebrain  is 
rounded  but  the  rhinencephalon  less  reduced  than  might  be  expected 
by  comparison  with  whales.  The  neopallium  is  smaller  and  less  folded 
than  in  almost  any  other  mammal  of  comparable  size.  The  eyes  are 
small  and  protected  by  muscular  lids;  the  animals  do  not  see  well. 
The  external  auditory  meatus  is  reduced  to  a  channel  a  few  milli- 
metres wide,  as  in  whales.  Little  is  known  of  the  hearing  but  reports 
are  that  it  is  acute. 

In  the  manatees,  the  upper  lip  is  greatly  developed  to  form  a  strong 
yet  sensitive  pad,  used  for  cropping.  The  front  parts  of  the  jaws  carry 
horny  pads  for  chewing.  The  teeth  form  a  series  of  pegs,  with  two 
transverse  ridges;  there  may  be  up  to  twenty  of  them  and  those  in 
front  drop  out  when  worn.  It  has  been  supposed  that  there  is  a  con- 
tinual replacement  from  behind,  as  in  elephants,  but  this  is  doubtful. 
In  the  dugong  the  teeth  are  much  reduced  and  the  lower  jaw  carries 
a  horny  pad;  the  upper  carries  a  pair  of  tusks  in  the  male  and  the  pre- 
maxillae  are  very  large.  The  stomach  is  complex  but  not  like  that  of 
either  the  whales  or  other  ungulates.  The  intestine  is  very  long. 

The  reproductive  system  shows  such  primitive  features  as  ab- 
dominal testes  (with  no  signs  that  there  was  a  descent  in  the  ancestors) 
and  a  bicornuate  uterus.  The  placenta  shows  a  zonary  arrangement 
and  haemochorial  structure,  resembling  that  of  elephants  and  conies. 
The  young  are  born  in  the  water  and  nursed  at  pectoral  teats,  which 
habit,  with  other  features,  may  have  produced  some  of  the  legends 
of  mermaids. 

Eocene  fossils  are  known  (*Protosiren)  which,  while  definitely 
sirenians,  show  distinct  similarity  to  the  ungulates  of  those  times. 
The  nostrils  were  directed  dorsally  as  in  modern  forms,  but  the  tooth 
row  was  complete  and  a  small  hind-limb  was  present. 


XXX 

PERISSODACTYLS 


1.  Perissodactyl  characteristics 

The  protungulate  and  paenungulate  herbivorous  types  achieved  their 
chief  radiation  and  greatest  numbers  early  in  the  Tertiary  period. 
Their  organization  was  not  profoundly  different  from  that  of  the 
original  eutherians  and  although  a  few  of  them,  such  as  the  elephants, 
have  persisted  to  the  present  day,  most  have  been  supplanted  by 
ungulates  that  appeared  by  later  modification  of  the  original  type. 
Very  roughly  we  may  say  that  the  protungulate  is  the  chief  Palaeo- 
cene  mammalian  herbivorous  type  and  the  paenungulate  that  of  the 
Eocene.  The  Perissodactyla,  including  horses,  rhinoceroses,  tapirs, 
and  certain  early  extinct  types,  then  represent  a  third  or  Oligocene- 
Miocene  development,  supplanting  the  paenungulates  and  itself  then 
largely  replaced  in  Pliocene,  Pleistocene,  and  Recent  times  by  the 
Artiodactyla.  This  analysis  must  of  course  be  taken  only  as  a  very 
rough  approximation,  especially  as  it  is  given  unsupported  by  the 
quantitative  data  that  it  evidently  requires.  It  is  subject  to  many  ex- 
ceptions, for  example  the  large  development  of  the  elephants  in  post- 
Miocene  times. 

The  early  perissodactyls  were  much  like  all  other  early  ungulates 
and  it  is  not  easy  to  characterize  the  group  as  a  whole.  The  limb 
structure  developed  the  mesaxonic  condition,  with  the  digits  arranged 
around  the  third  as  the  main  weight-bearing  member,  the  others 
being  reduced.  With  the  power  of  fast  movement  the  lower  part  of 
the  limbs  became  elongated  and  the  upper  segments  shortened,  with 
reduction  of  the  ulna  and  fibula,  but  these  are  characters  found  also 
in  artiodactyls.  A  distinctive  feature  of  the  perissodactyls  was  the 
plan  of  the  carpus  and  tarsus  (Fig.  466).  One  distal  carpal,  the  capitate 
(magnum),  became  enlarged  and  interlocked  with  the  proximal  car- 
pals,  while  in  the  foot  the  ectocuneiform  developed  into  a  large  flat 
bone,  transmitting  the  thrust  through  a  flat  navicular  to  the  talus, 
which  has  a  flat  undersurface,  not  a  pulley-like  one  as  in  Artio- 
dactyla. Modifications  of  the  backbone  for  carrying  great  weight  or 
for  running  were  similar  to  those  of  other  orders  (elephants,  Dino- 
cerata),  including  increase  in  the  number  of  ribs  and  the  vertical 
position  of  the  ilium  (p.  697). 


xxx.  i-2  FEEDING  723 

The  feeding  meehanism,  though  it  has  been  the  basis  of  the  success 
of  the  perissodactyls,  is  in  several  ways  less  specialized  than  that  of 
artiodactyls.  The  incisors  are  preserved  and  used  for  cropping,  having 
a  pit  on  the  free  surface,  so  that  sharp  edges  are  presented  as  the  tooth 
wears  away  (incidentally  allowing  the  age  of  the  animal  to  be  deter- 
mined). The  canine  may  be  reduced  or  absent,  and  there  is  often  a 
diastema.  The  molars  of  many  of  the  earlier  types  remained  bunodont 
and  low-crowned,  but  those  of  the  later  rhinoceroses  and  horses 
developed  an  elaborate  grinding  surface.  This  was  achieved  by  forma- 
tion of  a  longitudinal  ectoloph  along  the  outer  edge  of  the  upper  molar 
and  parallel  transverse  ridges,  the  protoloph  and  metaloph  (Fig.  465). 
Even  with  the  secondary  complications  of  the  latest  forms  these  teeth 
remain  recognizably  of  quadritubercular  pattern,  and  the  same  might 
be  said  of  the  lower  molars.  The  premolars  come  to  resemble  the 
molars,  giving  a  long  battery  of  teeth.  The  gut  shows  less  specializa- 
tion than  in  artiodactyls,  the  stomach  being  undivided,  but  in  horses 
there  is  a  large  cardiac  area  of  non-glandular,  oesophageal  structure. 
Digestion  of  cellulose  takes  place  in  the  caecum  and  large  intestine, 
which  may  be  greatly  developed.  The  brain  of  Perissodactyla  is 
relatively  small,  especially  in  the  earlier  forms,  such  as  the  tapirs.  It 
is  of  macrosmatic  type  and  the  sensory  portion  of  the  nose  is  highly 
developed. 

The  reproductive  system  also  shows  primitive  features.  The  uterus 
is  bicornuate  and  the  placenta  of  the  diffuse  epitheliochorial  type,  with 
a  large  allantoic  sac.  The  yolk  sac  grows  to  a  large  size  and  forms  a 
yolk-sac  placenta  during  the  early  part  of  the  development. 

2.  Classification 

Superorder  4.  Mesaxonia 
Order  Perissodactyla 
Suborder  1.  Hippomorpha 
*Family  1.  Palaeotheriidae.  Eocene-Oligocene.  Eurasia 

*Palaeotherium 
Family  2.  Equidae.  Horses.  Eocene-Recent 

*Hyrac other ium  (=  *Eohippus),  Lower  Eocene,  Holarctic; 
*Orohippns,  Eocene,  N.  America;  *Epihippus,  Upper 
Eocene,  N.  America;  *Mesohippus,  Oligocene,  N.  America; 
*Miohippm,  Oligocene-Miocene,  N.  America;  *Anchi- 
therium,  Miocene,  Holarctic;  *Parahippns,  Miocene,  N. 
America;  *Merychippus,  Miocene,  N.  America;  *Hipparion, 
Pliocene,     Holarctic,     Africa;     *Pliohippus,     Pliocene,     N. 


724  PERISSODACTYLS  xxx.  2-3 

Superorder  4.  Mesaxonia.    Family  2  (cont.) 

America;    *Hippidion,    Pleistocene,    S.    America;    Equus, 
horses,  asses,  zebras,  Pliocene-Recent,  world-wide 
*  Family  3.  Brontotheriidae  (=  *Titanotheridae).  Eocene-Oligo- 
cene.  Holarctic 
*Lambdotherium,    Eocene;    *Eotitanops,    Eocene;    *Brontops, 
Oligocene 
*Family  4.  Chalicotheriidae.  Eocene-Pliocene.  Holarctic 

*Eomoropus,    Eocene;    *Chalicotherium,    Oligocene-Pliocene, 
Eurasia,  Africa;  *Moropus,  Miocene,  N.  America 
Suborder  2.  Ceratomorpha 
Superfamily  1.  Tapiroidea.  Tapirs.  Eocene-Recent 

*Homogalax,  Eocene;   Tapirus,  tapir,  Miocene-Recent,  Asia, 
S.  America 
Superfamily  2.  Rhinocerotoidea.  Rhinoceroses.  Eocene-Recent 
^Family  Hyrachyidae.  Eocene.  Holarctic 

*Hyrachyns.  Eocene 
#Family  Hyracodontidae.  Eocene-Oligocene.  Holarctic 

*Hyracodon,  Oligocene 
*Family  Amynodontidae.  Eocene-Miocene.  Holarctic 

*Amy7iodon,  Eocene 
Family  Rhinocerotidae.  Oligocene-Recent 

*Aceratherium,  Oligocene-Pliocene ;  *Balachitherium>  Oligo- 
cene-Miocene,  Asia;  Rhinoceros,  Indian  and  Javan  rhino- 
ceros, Pliocene-Recent,  Asia;  Diceros,  black  African  rhino- 
ceros, Pleistocene-Recent,  Africa 

3.  Perissodactyl  radiation 

The  fossil  history  of  animals  with  the  perissodactyl  structure  is 
perhaps  better  known  than  that  of  any  other  mammals;  the  type 
reached  its  peak  during  a  period  from  which  many  fossils  have  been 
preserved  and  we  have  therefore  a  better  opportunity  to  study  the 
development,  flowering,  and  decay  of  the  group  than  in  the  case  of 
forms  whose  maximum  development  occurred  either  earlier  or  later. 
Here  if  anywhere  we  should  be  able  to  learn  lessons  about  the  nature 
of  the  evolutionary  process  and  to  study  the  forces  that  produce 
change  in  animal  form.  Because  of  the  very  abundance  of  the  fossils 
it  is  necessary,  however,  to  be  cautious  in  interpretation  and  to  recog- 
nize exactly  what  can  be  proved  from  the  evidence. 

The  known  types  of  horses  are  divided  into  350  species,  but  only 
a  small  proportion  of  these  can  be  confidently  placed  close  to  the 


(725) 


Hyracotherium 


Brontops 


Palaeotherium 


Moropus 


Fig.   479.   Skeletons   of  some   early   perissodactyls.   (After  Woodward,    Palaeontology, 
Cambridge,  Osborn,  Abel,  and  Scott,  Land  Mammals,  The  Macmillan  Company.) 


726  PERISSODACTYLS  xxx.  3- 

direct  line  of  evolution  to  Equus.  Abundant  though  the  material  is, 
we  have  not,  therefore,  anything  like  a  complete  series  of  fossils  to 
show  every  shade  and  grade  of  change  of  the  populations  throughout 
the  50  million  years  or  so  of  their  evolution.  Our  knowledge  is  based 
on  a  small  sample  of  individuals,  preserved  at  random  at  scattered 
intervals.  The  remains  often  suggest  evolutionary  sequences  and  many 
accounts  speak  confidently  of  changes  and  trends.  We  shall  try,  even 


CERA  TOMORPH A 


HIPPOMORPHA 


Fig.  480.  Chart  of  the  evolution  of  the  perissodactyls. 


in  this  brief  account,  to  describe  the  actual  discoveries  and  to  indicate 
clearly  what  evidence  is  available  for  evolutionary  speculation.  With 
all  the  mass  of  information  we  possess  it  must  yet  be  realized  that  the 
study  of  the  details  of  perissodactyl  evolution  has  hardly  been  begun, 
for  example  we  have  little  quantitative  information  about  the  vari- 
ability of  the  characters  concerned. 

The  earliest  perissodactyls  had  departed  but  little  from  condylarth 
conditions.  *Hyracotherium{=  *Eohippns)  from  the  Eocene  of  Europe 
and  North  America  (Fig.  479)  was  the  size  of  a  dog  and  resembled  the 
condylarth  *Phenacodus.  The  tooth  row  was  complete,  with  square 
bunodont  molars  (Fig.  467).  In  addition  to  the  four  main  upper  molar 
cusps  an  anterior  protoconule  and  posterior  metaconule  are  suggested, 
and  between  these  and  their  neighbours  the  dentine  is  partly  built  up 
to  form  two  transverse  ridges.  The  premolars  were  tritubercular.  The 


xxx.  4 


TAPIRS 


727 


gait  was  digitigrade,  with  rather  long  metapodials  and  with  hoofs,  the 
front  leg  having  four  and  the  hind-leg  three  toes,  the  central  ones  the 
longest.  These  animals  were  already  distinctly  horse-like,  in  spite  of 
their  small  size,  and  they  probably  lived  in  forests,  browsing  on  the 
leaves. 

From  a  population  of  animals  of  this  type  there  evolved  a  varied 


Fig.  481.  Malayan  tapir,  Tapirus.  (From  photographs.) 


Fig.  482.  Skull  of  the  tapir.  (After  Reynolds,  The  Vertebrate 
Skeleton,  Cambridge.) 

host  of  herbivores  (Fig.  480),  which  may  be  divided  into  six  main 
types:  the  tapirs,  remaining  with  little  change;  the  rhinoceroses, 
becoming  large  and  heavy-bodied;  brontotheres  (titanotheres),  also 
becoming  large;  palaeotheres,  an  early  horse-like  line;  chalicotheres, 
which  secondarily  acquired  claws,  and  finally  the  horses  themselves. 
Of  course  each  of  these  lines  had  many  subdivisions  and  branches, 
producing  a  most  complex  evolutionary  bush. 

4.  Suborder  Ceratomorpha,  tapirs  and  rhinoceroses 

The  modern  tapirs  of  Central  and  South  America,  Malaya,  and  the 
East  Indies  (Fig.  481)  are  nocturnal  creatures,  mostly  living  in  forests 
on  damp,  soft  ground;  they  have  retained  many  of  the  conditions  of 


728  PERISSODACTYLS  xxx.  4- 

the  ancestors  of  all  Perissodactyla.  There  are  four  digits  in  the  fore- 
foot and  three  in  the  hind;  the  ulna  and  fibula  are  complete  and  dis- 
tinct. The  tooth  row  is  complete  (42  teeth  in  tapirs),  but  the  pre- 
molars are  molariform,  though  of  a  simple  square  pattern,  with  low 
crowns  (Fig.  482).  The  nose  has  developed  into  a  short  trunk,  with 
characteristic  shortening  of  the  nasal  bones.  The  stomach  is  like  that 
of  horses  and  there  is  a  large  caecum.  The  placenta  is  diffuse.  The 
brain  is  relatively  smaller  than  in  horses. 

Fossil  tapirs,  very  similar  to  modern  forms,  are  found  back  to  the 
Oligocene,    and   somewhat   more   primitive   Eocene   related   forms 


Fig.  483.  Indian  rhinoceros  (Rhinoceros). 

(*Homogalax)  might  have  been  close  to  the  ancestors  of  *Hyraco- 
therium.  We  may  say  therefore  with  some  confidence  that  the  modern 
tapirs  show  us  with  little  change  the  condition  of  the  perissodactyl 
stock  in  late  Eocene  or  Oligocene  times,  perhaps  40  million  years  ago. 
Fossils  almost  exactly  similar  to  the  existing  genus  occur  back  to  the 
Miocene,  say,  20  million  years  ago,  and  the  tapirs  were  then  of  wide- 
spread distribution.  We  may  notice  once  again  the  important  fact  that, 
given  suitable  environments,  types  persist  with  little  change  even  when 
their  relatives,  moving  into  other  conditions,  become  greatly  changed. 

5.  Rhinoceroses 

The  rhinoceroses  (Fig.  483)  are  the  only  surviving  large  perissodac- 
tyls ;  they  show  the  graviportal  type  of  body  form  that  was  adopted  by 
many  of  the  extinct  forms  (brontotheres,  &c.)  and  also  by  many  other 
large  eutherians.  Dinocerates,  elephants,  hippopotamuses,  and  rhino- 
ceroses all  show  the  same  type  of  skeleton.  The  vertebral  column  (Fig. 
484)  has  long  neural  spines  above  the  fore-legs,  there  are  many  ribs, 
reaching  back  nearly  to  the  pelvis.  The  whole  column  thus  makes  a 
girder  balanced  on  the  fore-legs,  and  the  head,  being  very  heavy, 


RHINOCEROS 


XXX.  5  KllllNULLKUS  729 

counterbalances  the  body  weight.  The  hind-legs  provide  the  main 
locomotor  thrust.  It  is  characteristic  of  this  'single-girder'  type  of  back- 
bone that  the  ilia  are  wide  and  vertically  placed.  The  feet  are  basically 
similar  in  all  these  groups  in  that  several  digits  (usually  three  in  the 


Fig.  484.  Belozo:  Skeleton  of  the  Indian  rhinoceros.  (From  Owen.)  Above:  Skull  and 
teeth  of  a  young  Indian  rhinoceros.  The  grinding  surface  is  made  up  of  four  milk  pre- 
molars and  one  adult  molar  on  each  jaw.  The  remaining  permanent  teeth  have  not  erupted. 
/.  frontal;/,  jugal;  na.  nasal;  pa.  parietal;  sq.  squamosal.  (After  Reynolds,  The  Vertebrate 

Skeleton,  Cambridge.) 

rhinoceros)  are  preserved,  making  supports  of  large  area.  The  brain  of 
the  rhinoceros  is  small  and  the  chief  receptors  are  those  of  smell  and 
hearing;  the  eyes  are  mainly  used  in  weak  light.  Like  the  tapirs  they 
are  essentially  timid  animals,  mainly  nocturnal,  though  defending 
themselves  with  a  charge  if  attacked.  They  live  singly  or  in  pairs. 

The  earliest  members  of  the  rhinoceros  group,  such  as  *Hyrachyus 
of  the  Eocene,  were  very  like  other  primitive  perissodactyls,  mostly 


730  PERISSODACTYLS  xxx.  5- 

small  and  with  a  complete  tooth  row,  in  which  the  molars  already 
show  an  ectoloph  and  the  parallel  transverse  lophs  characteristic  of  the 
group.  The  *Hyracodonts  were  an  Eocene  and  Oligocene  line  speci- 
alized for  swifter  movement  ('running  rhinoceroses')  with  long  legs 
and  three  toes  in  each  foot,  much  as  in  the  earlier  horses.  The  members 
of  another  line,  the  *Amynodonts,  were  larger,  probably  semi-aquatic 
forms.  The  true  rhinoceroses  appear  in  the  Oligocene,  already  as 
large  creatures,  fully  terrestrial  and  hence  with  stout  limbs  and  a  good 
grinding  battery,  with  molarized  premolars.  *Baluchitherium  became 
of  enormous  size,  as  much  as  18  ft  high.  Rhinoceroses  became  numer- 
ous in  the  Miocene  and  Pliocene  (*Aceratherium).  Various  types  per- 
sisted through  the  Pliocene  and  Pleistocene,  and  the  modern  single- 
horned  Rhinoceros  of  Asia  and  two-horned  Dicerorhinns  of  the  East 
Indies  and  Diceros  of  Africa  are  derived  from  some  of  these.  Extinct 
types  such  as  the  woolly  rhinoceros  are  known  from  Palaeolithic  draw- 
ings and  from  partly  embalmed  specimens.  Modern  rhinoceroses  all 
have  a  very  thick,  almost  hairless  skin,  with  characteristic  folds.  The 
tendency  to  active  keratin  development  also  produces  the  horns, 
either  one,  two,  or  occasionally  three  median  outgrowths  on  the  head, 
often  compared  to  clumped  masses  of  hairs  but  essentially  similar  to 
the  horns  of  ruminants  but  without  a  bony  core. 

6.  *Brontotheres  (*Titanotheres) 

These  were  early,  heavily  built  ungulates,  reaching  large  size  in  the 
later  Eocene  and  Oligocene,  in  fact  preceding  the  rhinoceroses  as 
large  herbivores.  The  fully  developed  forms,  such  as  *Brontops  (Fig. 
479)  of  the  Lower  Oligocene,  were  of  typical  graviportal  type,  up  to 
8  ft  high,  with  high  thoracic  spines,  numerous  ribs,  vertical  and 
laterally  expanded  ilia,  and  rather  short  legs,  with  four  digits  in  front 
and  three  behind.  The  tooth  row  was  complete  and  the  molars  large 
but  low-crowned,  with  a  ridge  along  the  outer  side,  but  isolated  cusps 
on  the  inner  (hence  'bunolophodont').  A  single  pair  of  large  horns 
was  carried  on  the  front  of  the  skull.  The  brain  was  even  smaller  than 
that  of  rhinoceroses. 

The  earliest  fossils  that  can  be  referred  to  this  type,  * Lambdotherium 
of  the  Lower  Eocene,  were  much  smaller,  and  without  horns;  they 
could  well  have  been  derived  from  *Hyracotherium.  *Eotitanops  from 
the  Middle  Eocene  was  larger,  but  still  hornless.  From  some  such 
stage  numerous  lines  probably  diverged,  each  becoming  larger  and 
independently  acquiring  horns.  For  obvious  reasons  it  is  difficult  to 
obtain  a  proper  idea  of  the  evolution  of  such  giants,  as  Simpson  points 


xxx.  7  CHALICOTHERES  731 

out,  genera  and  perhaps  even  subfamilies  have  probably  been  created 
on  a  basis  of  differences  that  may  be  only  sexual  or  individual. 

7.  *Chalicotheres  (=  *Ancylopoda) 

One  remarkable  side-line  of  perissodactyl  evolution,  while  becoming 
large  and  horse-like  in  some  ways,  acquired  structures  resembling 
claws  instead  of  hoofs  (*Moropus,  Fig.  485).  These  chalicotheres,  all 
rather  alike,  existed  from  the  Eocene  to  the  Pleistocene  and  were 
therefore  a  successful  group.  The  terminal  phalanges  of  the  three  toes 
of  each  foot  were  cleft  and  undoubtedly  carried  a  nail  or  claw  of  some 


Fig.  485.  Feet  of  a  chalicothere.  (After  Romer,  Vertebrate 
Paleontology,  University  of  Chicago  Press.) 

sort,  though  not  necessarily  one  like  that  of  true  unguiculates.  There 
is  no  doubt  that  in  a  sense  this  is  a  case  of  reversal  of  evolution,  but 
we  cannot  assert  much  about  its  possible  genetic  implications  unless 
we  can  find  details  of  the  nails. 

When  chalicothere  digits  were  first  discovered  in  1823  Cuvier 
applied  his  'law  of  correlation'  and  suggested  that  this  was  the  remains 
of  an  ant-eater,  'un  Pangolin  gigantesque',  while  teeth  and  other 
bones  found  near  by  he  referred  to  an  ungulate.  It  was  only  when 
skeletons  were  found  in  such  a  position  that  the  association  of  the 
bones  could  not  be  denied  that  the  danger  of  this  attempt  to  apply 
deductive  principles  in  biology  was  exposed.  The  other  parts  of  the 
skeleton  are  unambiguously  perissodactyl  (Fig.  479),  the  teeth  rather 
like  those  of  brontotheres.  There  may  have  been  a  short  proboscis. 
The  neck  vertebrae  of  some  forms  show  very  strong  zygapophyses, 
and  it  has  been  suggested  that  the  snout  and  claws  were  used  for 
digging  for  roots  or  water.  It  is  more  probable  that  the  chalicotheres 
reared  up  on  their  hind-legs  and  used  the  claws  to  cling  to  tree-trunks 
while  reaching  for  leaves  with  their  flexible  necks,  or  perhaps  to  drag 
down  branches.  Like  the  toxodont  *Homalodotherinm  they  had  long 
front  legs  and  large  ischia.  Moreover,  their  remains  are  found  in 


732  PERISSODACTYLS  xxx.  7-9 

association  with  those  of  forest  dwellers.  The  attraction  of  speculating 
about  these  creatures  has  not  diminished  with  the  demonstration  of 
its  dangers. 

8.  Palaeotheres 

These  animals,  from  the  later  Eocene  and  early  Oligocene  of 
Europe,  were  an  early  offshoot  that  paralleled  in  many  ways  the 
evolution  in  North  America.  For  example,  they  developed  three-toed 
feet,  and  the  premolars  became  molarized.  The  teeth  developed  ridges 
on  a  similar  plan  to  the  horses,  but  differing  in  details.  Some  forms 
became  hypsodont.  Several  lines  of  descent  are  included  in  the  group. 
*Palaeotherium  became  large,  though  not  so  large  as  the  gravi- 
portal  brontotheres  and  rhinoceroses.  The  shortness  of  its  nasal  bones 
suggests  that  it  had  a  proboscis  like  a  tapir.  Palaeotheres,  like  horses, 
have  probably  been  derived  from  a  *Hyracotherium-\ike  stock.  They 
illustrate  the  importance  of  parallelism  in  evolution,  and  serve  to  warn 
us  against  the  easy  assumption  that  a  character  that  is  shown  by  two 
animals  must  have  been  present  in  their  common  ancestor. 

9.  Horses 

The  horse,  besides  its  special  interest  as  one  of  our  oldest  and  most 
useful  commensals,  has  provided  a  rather  complete  and  convincing 
record  of  its  origin.  We  shall  therefore  first  describe  its  present 
structure  and  then  analyse  the  fossil  record  to  discover  exactly  what 
can  be  demonstrated  about  the  evolution.  Existing  horses,  asses,  and 
zebras,  all  referred  to  the  genus  Equns  (Figs.  486-88),  are  highly 
specialized  for  swift  movement  and  eating  grasses  (p.  697).  Only  the 
third  digits  are  developed  and  covered  with  hoofs.  These  are  ela- 
borately organized  pads,  including  several  sorts  of  keratin,  harder  in 
front,  more  elastic  behind.  The  metapodials  of  digits  II  and  IV  are 
present  as  small  splint-bones.  There  is  a  horny  callosity  on  the  inner 
side  of  the  fore-limb  in  all  species  (also  on  the  hind-limbs  in  E.  cabal- 
lus,  the  domestic  horse),  representing  the  vestigial  hoofs  of  lateral 
digits. 

There  are  three  incisors  in  each  jaw,  usually  one  small  canine  (the 
'tush',  absent  in  females).  The  first  premolar  is  vestigial  in  each  jaw 
('wolf-tooth');  the  remaining  three  resemble  the  three  molars.  All  the 
cheek  teeth  are  hypsodont,  square  in  cross-section,  with  ectoloph  and 
transverse  protoloph  and  metaloph,  joined  by  longitudinal  ridges  that 
give  the  tooth  a  certain  resemblance  to  the  selenodont  molars  of  artio- 
dactyls,  hence  'selenolophodont'.  The  skull  is  modified  to  allow  space 


(733) 


Fig.  486.  Zebra  (Eqaus).  (From  photographs.) 


:   •••'T-2$L:~V' 


f  n  r 


Fig.  487.  Racehorse  (Equus).  (From  a  photograph.) 


Fig.  488.  Shire  horse  (Equus).  (From  a  photograph.) 


734  TERISSODACTYLS  xxx.  9 

for  the  deep,  continually  growing  teeth  and  for  the  large  jaw-muscles, 
and  there  is  a  complete  post-orbital  bar. 


S.AMERICA  -  50 


EURASIA 


NORTH       AMERICA 


Fig.  489.  Table  to  show  the  evolution  of  horses.  (Based  on  Stirton.)  The  approximate 
condition  of  the  limbs  and  teeth  at  each  epoch  are  shown  to  the  left  and  right. 


The  hair  is  long  all  over  the  body  and  tends  to  show  the  pattern  of 
vertical  stripes  that  is  so  marked  in  zebras,  often  clear  in  asses,  and 
occasionally  present  in  horses.  The  tail  is  long,  its  hairs  beginning 
close  to  the  base  in  horses,  half-way  along  in  the  others. 

All  horses  in  the  native  state  live  in  herds,  as  do  so  many  herbivores 


xxx.  9  EVOLUTION    OF   HORSES  735 

that  dwell  on  plains.  The  brain  is  large,  and  although  the  organs  of 
smell  are  well  developed  the  eyes  are  also  large  and  the  neopallium  is 
extensive.  Receptors  for  touch  are  well  developed  in  the  muzzle,  in 
the  skin  beneath  the  hoofs,  and  elsewhere.  Hearing  is  exceptionally 
acute.  Besides  the  keen  senses  common  to  many  herbivores  the  horse, 
with  its  large  brain,  also  has  considerable  powers  of  learning  and 
ability  to  vary  and  restrain  its  behaviour.  There  is  an  elaborate  com- 
munication system,  involving  not  only  sounds  but  movements  of  the 
ears,  tail,  and  lips.  In  these  respects  horses  and  elephants,  and  perhaps 
also  modern  artiodactyls,  are  probably  very  different  from  the  small- 
brained  herbivores  of  the  Eocene,  though,  of  course,  we  can  only  guess 
at  the  behaviour  of  these. 

Modern  horses  show  considerable  genetical  diversity  (Figs.  487  and 
488),  but  none  of  the  'species'  are  mutually  sterile,  though  the  F  1 
resulting  from  the  cross  may  be  nearly  so,  as  in  the  case  of  the  mule, 
produced  from  the  horse-ass  cross.  Evidently  the  population  is  in  pro- 
cess of  divergence.  The  domestic  horse  E.  cabalhis  is  not  found  truly 
wild,  but  E.  przewalskii  of  central  Asia  may  be.  There  are  several 
species  of  wild  asses,  such  as  E.  onager  of  Asia  and  E.  asinus  of  Africa. 
Several  species  of  zebra  live  in  Africa,  one  of  them  being  E.  zebra. 

Between  the  modern  Equns  and  the  lower  Eocene  *Hyracotherium 
a  great  number  of  fossil  stages  can  be  recognized  (Fig.  489).  The  chief 
changes  that  can  be  followed  may  be  listed  as  (1)  increase  of  size, 
(2)  lengthening  of  the  distal  portion  of  the  legs,  (3)  reduction  of  lateral 
digits,  (4)  increase  in  the  relative  length  of  the  front  part  of  the  skull, 
(5)  increase  of  depth  (hypsodonty)  and  of  the  grinding  lophs  of  the 
molars,  (6)  approximation  of  premolars  to  molar  structure,  (7)  com- 
pletion of  post-orbital  bar.  No  doubt  there  has  been  change  also  in 
many  other  characteristics,  for  instance  the  brain  and  behaviour;  these 
are  difficult  to  follow  in  a  fossil  series,  but  study  of  cranial  casts  sug- 
gests that  a  rapid  increase  in  size  and  folding  of  the  cerebrum  occurred 
relatively  early  in  the  evolution. 

The  fossil  remains  are  not  usually  available  in  long  series  of  layered 
beds,  such  that  we  can  be  sure  that  one  population  has  evolved  into 
the  next.  However,  the  dating  of  the  fossils  can  often  be  done  with 
considerable  accuracy  by  means  of  the  associated  animals,  and  a  series 
can  thus  be  produced  such  as  would  be  expected  in  the  progress  from 
*Hyracotherium  to  Equns.  There  are,  however,  many  fossils  that  show 
special  developments,  and  cannot  be  fitted  into  the  direct  series. 
These  are  presumed  to  be  divergent  lines:  it  must  be  emphasized  that 
this  is  an  arbitrary  though  probably  justified  procedure.  These  'side- 


736  PERISSODACTYLS  xxx.  9- 

lines'  are  so  numerous  that  they  immediately  throw  doubt  on  the  idea 
that  there  has  been  any  single  uniform  'trend'  in  horse  evolution.  At 
least  twelve  types  sufficiently  marked  to  be  classified  as  genera  are 
known,  in  addition  to  those  directly  on  the  line  leading  to  Equus\ 
of  course  there  is  a  much  larger  number  of  shorter,  independent, 
evolutionary  lines  within  these  genera.  We  have  enough  evidence  to 
glimpse  the  extraordinary  complexity  that  would  be  revealed  by  the 
complete  evolutionary  'bush',  even  in  this  single  family.  A  further 
complication  is  produced  by  migrations.  It  is  at  present  believed  that 
the  main  course  of  horse  evolution  went  on  in  North  America,  with 
migration  at  various  times  to  the  Old  World  and  South  America. 
Certainly  a  more  continuous  series  of  forms  has  been  revealed  in 
North  America  than  elsewhere,  but  it  must  be  remembered  that  they 
have  been  looked  for  intensively,  and  brilliantly  studied.  It  is  not 
impossible  that  further  study  of  Old  World  horses  will  produce  still 
greater  complications  by  revealing  sequences  of  evolution  within  that 
area. 

Throughout  the  Eocene  epoch  the  horses  all  possessed  four  toes 
in  each  limb.  The  fossils  classed  as  *Orohippns  and  *Epihippus  from 
the  Middle  and  Upper  North  American  Eocene  are  little  different 
from  *Hyracotherium,  except  for  molarization  of  the  hinder  premolars. 
The  size  remains  small. 

The  Oligocene  horses,  *Mesohippus  and  *Miohippns,  walked  with 
three  toes  on  the  ground,  and  all  the  premolars  were  molarized.  The 
ectoloph  was  well  formed  but  the  inner  cusps  were  still  separate,  and 
the  teeth  low-crowned.  Some  horses  of  this  type  (*Anchitherium  and 
its  descendant  *Hypohippus)  persisted  into  the  Miocene,  presumably 
surviving  as  browsers  in  forests,  while  other  descendants  took  to  the 
plains.  These  browsing  horses  migrated  to  the  Old  World  in  the 
Miocene,  then  died  out  there,  as  they  did  also  in  North  America. 

*Parahippus  of  the  American  Lower  Miocene  shows  the  beginning 
of  the  adaptation  for  life  on  the  plains.  The  lateral  digits  II  and  IV 
still  carried  hoofs,  but  since  the  central  proximal  phalanx  was  much 
the  longest  and  strongest,  it  is  probable  that  the  lateral  ones  touched 
the  ground  only  to  maintain  balance  over  uneven  surfaces,  or  in  soft 
conditions.  The  teeth  were  still  rather  low,  but  were  beginning  to  be 
elongated  and  to  show  cement  on  the  crowns.  The  protoloph  and 
metaloph  were  connected  by  a  narrow  bridge.  There  was  a  partial 
post-orbital  bar. 

*Merychippus  comes  from  later  Miocene  beds  and  could  have  been 
directly  derived  from  *Parahippus  by  increase  in  the  depth  of  the 


xxx.  io  RELATIVE    GROWTH-RATES  737 

teeth  and  reduction  of  the  lateral  digits  to  short  stumps,  still  three- 
jointed  and  carrying  hoofs,  but  vestigial  in  the  sense  of  never  touching 
the  ground.  The  presumption  is  that  this  type  of  structure  was  found 
advantageous  for  life  on  large  grassy  plains  produced  by  arid  Miocene 
conditions,  the  high-crowned  teeth  being  needed  to  grind  the  tough 
siliceous  grasses. 

Apparently  the  type  was  very  successful  and  in  the  Pliocene  it 
produced  various  populations.  *Hipparion,  with  the  two  lateral  toes 
remaining  as  vestiges,  spread  through  Eurasia  in  the  Pliocene.  *Nan- 
nippus  was  a  small  form  that  remained  in  America.  *Pliohippns  was 
another  American  descendant  from  *Merychippus,  and  here  the  lateral 
digits  were  lost  altogether  in  the  Pliocene,  the  metapodials  remaining 
as  long  thin  vestiges.  When  the  land  connexion  with  South  America 
became  open  this  type  of  horse  migrated  there  and  produced  a  special 
development,  *Hippidion  of  the  Pleistocene,  with  rather  short  legs, 
perhaps  correlated  with  a  mountain  habit. 

Meanwhile  in  the  late  Pliocene  or  early  Pleistocene  the  *Pliohippus 
stock  of  North  America  finally  reduced  the  lateral  metapodials  to  short 
splint  bones  and  produced  the  Equus-type,  which  spread  thence  over 
all  the  available  land-masses,  becoming  then  extinct  in  North  and  South 
America  until  reintroduced  by  man. 

10.  Allometry  in  the  evolution  of  horses 

Although  Eqvus  is  certainly  a  very  different  creature  from  *Hyraco- 
therium,  we  are  fortunate  in  that  many  of  the  differences  are  due  to 
measurable  changes  in  proportions.  A  beginning  has  been  made  with 
attempts  to  estimate  the  rate  of  evolutionary  change,  as  a  preliminary 
to  study  of  the  factors  that  influence  it.  Some  of  the  changes  in  pro- 
portion seen  during  horse  evolution  are  a  consequence  of  the  increase 
in  size.  If  an  organ  grows  relatively  faster  or  slower  than  the  body 
as  a  whole  it  is  obvious  that  its  proportions  will  differ  in  animals  of 
differing  adult  size.  The  size  of  an  organ,  y,  in  relation  to  that  of 
the  body,  x,  is  often  expressed  as  y  —  bxky  where  the  constant  k 
describes  the  relative  growth  rate.  If  k  >  1  the  organ  becomes  larger 
in  larger  animals  and  is  said  to  be  positively  allometric  (J.  S.  Huxley). 
The  demonstration  that  growth  actually  follows  this  law  in  particular 
cases  is  not  easy,  and  the  underlying  assumptions  have  been  questioned. 
It  is  probably  true,  however,  that  organs  do  sometimes  differ  in  rela- 
tive growth-rates,  and  the  method  provides  a  means  of  investigation 
of  the  proportions  of  an  organ  not  only  at  one  stage  but  throughout 
the  growth  period,  and  indeed  also  between  adults  throughout  an 


738  PERISSODACTYLS  xxx.  10- 

evolutionary  sequence.  Thus  Robb  (Fig.  490)  shows  that  the  length 

of  a  horse's  face  increases  between  embryo  and  adult  along  a  line 

similar  to  that  found  in  the  series  *Hyracotherium  to  Equus,  and  that 

adult  horses  of  different  sizes  vary  similarly  in  face  proportion.  A 

nearly  fitting  line  gives  constants  b  =  0-25   and  k  =  1-23.   Other 

methods  of  plotting,  for  instance  face  length  against  cranium  length, 

give  somewhat  different  results  and  it  cannot  be  considered  certain 

that  no  new  genetic  factors  have 

A Huracotnerium- Equus  u         •        1     j   •      ^.u 

?        „        „„    y  been  involved  in  the  increase 

B Equus, 5mo-25u.  /  r  r        .         ,      ,  .  , 

r  c         pa  a/    f         •••'  01  face-length  throughout  the 

C  ********  Equus,  Snet/ancf-        /n  b.  b 

7       Percheron      /  u  whole  evolutionary  sequence. 

-^ Lj=Z5x  Ji-  Again,  reduction  of  the  lateral 

digits  of  the  toes  is  perhaps  not 
based  on  any  steady  genetic 
change  except  that  related  to 
size.  However,  in  this  case 
there  was  probably  one  rela- 
tively sudden  change  in  the 
constant  b  (which  may  be  said 
to  express  the  body  size  at 
which  the  toe  begins  to  form). 
Thus  in  the  three-toed  horses 
the  length  (y)  of  the  side  toes 
is  related  to  that  of  the  cannon 
x,  log  skull  length  bone  of  the  central  digit  (x)  by 

Fig.  490.  Relative  rates  of  growth  in  horses,  the  equation 
The  lines  show  regression  of  log  skull  length  0>g7 

on  log  face  length;  in  A,  the  line  of  horse  phylo-  J   ~~   *  5 

geny ;  B,  the  ontogeny  of  Equus;  c,  various  races  j  ,        one-toed    horses    from 

of  Equus  of  different  sizes;  D,  y  =  025  .v123.  in    ™    °ne  XOetl    Ilorbeb    iroin 

(After  Simpson  from  the  data  of  Robb.)  *PUoMppuS  Onwards 

y  =  o-8  x°-". 

There  has  therefore  been  little  change  in  the  relative  growth-rate, 
which  is  negatively  allometric  in  all  horses,  so  that  the  lateral  toes 
are  relatively  smaller  in  the  larger  animals. 

1 1 .  Rate  of  evolution  of  horses 

Study  in  the  same  way  of  other  horse  characters,  for  instance  those 
involved  in  hypsodonty,  shows  that  special  genetic  changes  may  be 
involved  and  that  genetic  change  does  not  go  on  at  a  constant  rate. 

Estimates  of  rate  of  evolution  for  the  whole  animal  have  also  been 
made  by  Matthew,  Simpson,  and  others.  Assuming  that  the  genus  is 


5) 


J I I L 


xxx.  iz  RATE   OF   EVOLUTION   OF   HORSES  739 

assessed  as  a  comparable  entity  throughout  (a  large  assumption,  this!) 
and  dividing  the  eight  genera  (excluding  Eqiiiis)  on  the  direct  line  into 
the  time  involved  between  *Hyracotherium  and  *Pliohippns  (50 
million  years),  we  should  have  6-3  million  years  per  genus.  However, 
there  is  reason  to  suppose  that  individual  genera  lasted  for  very 
different  times,  *Miohippus,  for  instance,  less  than  a  third  of  the  time 
of  *Merychippus.  Therefore  if  the  criterion  of  a  genus  is  constant,  the 
rate  of  evolution  must  vary. 

Sufficient  fossil  horse  material  is  available  to  allow  consideration 
whether  known  rates  of  mutation  are  likely  to  be  adequate  to  account 
for  the  observed  evolutionary  changes.  Simpson  calculates  that  from 
* Hyracotherium  to  Equus  there  must  have  been  at  least  15  million 
generations,  which,  with  a  population  in  North  America  of  100,000 
(a  low  estimate),  gives  a  total  of  1-5  x  io12  individuals  in  the  'real  and 
potential  ancestry  of  the  modern  horse'.  One  in  a  million  is  a  moderate 
rate  for  large  mutations  at  any  locus  in  Drosophila,  and  this  would 
give  1  -5  million  such  mutations  for  a  single  locus  in  the  horse  ancestry. 
It  would  be  safe  to  assume  that  one-fifth  of  these  (300,000)  were  in  the 
direction  favoured  by  selection  and  that  one-tenth  of  all  such  genes 
affect  a  structural  change,  such  as  ectoloph  length.  The  actual  increase 
in  this  length  between  * Hyracotherium  and  Equus  was  from  8  to  40  mm 
which,  divided  into  300  steps,  gives  an  increase  per  mutation  of 
only  o-i  mm.  This  is  a  reasonable  figure,  and  such  calculations 
suggest  that  observed  mutation  rates  are  quite  adequate  to  account 
for  the  evolutionary  changes,  even  neglecting  possible  multiple  actions 
and  interactions  of  genes,  by  which  the  speed  of  evolution  could  be 
further  increased. 

12.  Conclusions  from  the  study  of  the  evolution  of  horses 

Careful  consideration  of  the  fossil  horse  material  therefore  shows 
reason  to  suppose  that  evolution  has  proceeded  by  gradual  change. 
As  more  and  more  evidence  becomes  available  the  series  becomes 
more  and  more  complete,  and  incidentally  the  nomenclature  increas- 
ingly confusing.  Incompleteness  of  material  may  give  an  impression 
of  evolution  by  jumps  and  saltation,  especially  when,  as  in  the  Old 
World  horses,  there  have  been  successive  migrations  into  one  region 
from  another.  The  European  palaeontologists,  finding  *Hyraco- 
therium,  *Anchitherium,  *Hipparion,  and  Equus,  without  intermediate 
forms,  interpreted  the  evidence  as  showing  evolution  by  saltation. 
This  was  indeed  a  reasonable  deduction  from  the  facts,  but  was  not 
the  only  possible  one,  as  has  since  been  shown  by  the  discovery  of 


74o  PERISSODACTYLS  xxx.  12 

the  much  fuller  sequence  in  North  America.  It  is  probable  that  there 
are  many  equally  unjustified  conclusions  in  our  current  beliefs  about 
evolution. 

The  outstanding  conclusion  from  a  study  of  horse  evolution  is  that 
it  is  very  difficult  to  describe  the  change  as  occurring  in  a  single 
direction,  as  supposed  by  believers  in  'orthogenesis'.  Apart  from  the 
fact  that  many  'side-lines'  can  be  detected  beside  the  line  that  happens 
to  have  survived,  it  is  important  to  remember  that  not  every  line 
evolves  in  the  same  direction.  Thus  in  at  least  two  genera  of  horses 
size  became  progressively  smaller  (*Nannippus  and  *Archaeohippus). 
However,  it  is  certainly  true  that  in  some  lines  evolution  may  proceed 
for  long  periods  in  one  direction.  We  have  no  clear  evidence  why  this 
should  be  so,  but  it  is  reasonable  to  suppose  that  it  is  due  to  'ortho- 
selection', that  is  to  say,  the  survival  of  animals  that  adopt  a  particular 
method  of  life  for  which  they  are  suited  by  a  particular  make-up. 
The  effect  of  this  would  be  gradually  to  select  all  those  genetic  factors 
that  make  for  success  in  one  environment  (say,  grazing  on  grassy 
plains)  and  hence  to  produce  evolutionary  change  in  one  direction. 


XXXI 

ARTIODACTYLS 

1.  Characteristics  of  artiodactyls 

The  even-toed  ungulates,  though  they  can  be  traced  as  a  distinct 
line  back  to  the  Eocene,  may  be  considered  as  the  latest  mammalian 
herbivores,  having  radiated  out  chiefly  in  the  Miocene  and  attained 
then  a  dominance  that  has  persisted  to  the  present  day.  Except  for 
man  and  the  horse  all  the  large  mammals  really  well  established  and 
successful  at  the  present  time  are  artiodactyls.  Any  attempt  to  be 
dogmatic  about  the  reasons  for  the  success  of  a  group  of  animals  is  apt 
to  be  superficial,  but  it  is  not  unreasonable  to  suggest  that  in  this  case 
the  result  is  due  to  swiftness  of  foot,  combined  with  keenness  of  sense 
and  brain,  efficient  cropping  and  grinding  mechanisms,  and  especially 
a  complex  stomach,  allowing  the  digestion  of  cellulose  by  symbionts. 
Two  families  of  artiodactyls  survive  without  these  special  features, 
the  pigs  and  hippopotamuses,  water-  and  forest-living  remnants  that 
show  us  approximately  the  condition  of  the  group  in  the  Eocene. 

The  characters  of  artiodactyls  show  a  fascinating  'similarity  with  a 
difference'  to  those  of  perissodactyls.  The  common  origin  of  the  two 
groups  (p.  694)  was  little  above  the  insectivore  stage  and  nearly  every 
feature  has  been  evolved  independently;  the  general  structural  simi- 
larities and  detailed  differences  therefore  show  the  effect  produced  by 
similar  ways  of  life  on  slightly  differing  populations.  For  example,  a 
postorbital  bar  developed  in  both  groups,  for  attachment  of  the  large 
masseter  muscle,  but  whereas  in  the  horses  it  is  formed  wholly  of  a 
process  of  the  frontal  bone,  in  ruminants  there  is  a  union  of  processes 
of  the  jugal  and  frontal.  Many  such  similarities  and  differences  are 
seen  throughout  the  body,  and  especially  in  the  limbs. 

The  skull  of  later  artiodactyls  shows  changes  of  shape  to  accom- 
modate the  very  deep  molars  and  to  support  the  horns  that  are  com- 
monly found.  It  becomes  very  high  (as  in  horses),  and  there  is  a  sharp 
kink  between  the  basisphenoid  and  presphenoid,  so  that  the  face 
slopes  steeply  downward.  The  facial  bones  become  large  and  the 
parietals  restricted  to  the  vertical  posterior  face  of  the  skull,  to  which 
the  powerful  neck-muscles  are  attached.  In  many  ruminants  there  is 
a  scent-gland,  lying  in  a  pre-orbital  fossa  of  the  skull  and  opening  on 
the  side  of  the  head.  The  pre-lacrymal  fossa  is  a  gap  in  the  skull,  where 
the  nasal  cavity  is  separated  from  the  outside  only  by  the  skin. 


742  ARTIODACTYLS  xxxi.  i 

The  vertebral  column  shows  the  characteristics  of  other  large 
mammals  in  the  development  of  high  thoracic  spines.  Some  of  the 
heavier  types  have  a  long  rib  series  and  graviportal  'single  girder' 
structure,  but  the  tendency  has  been  to  retain  and  develop  the  break 
in  structure  of  the  vertebral  column  behind  the  thoracic  region,  giving 
a  long  lumbar  region  with  forwardly  directed  transverse  processes. 
In  rabbits  and  other  mammals  this  division  of  the  column  is  associated 
with  the  jumping  habit,  and  this  is  also  found,  though  in  a  different 
form,  in  ruminants  (Young,  1955,  p.  139)-  Associated  with  this  method 
of  progress  is  a  fore-and-aft  elongation  of  the  pelvic  girdle,  the 
ischium  being  well  developed  for  the  attachment  of  the  retractor 
muscles  of  the  thigh.  In  making  the  jumping  movements,  which  are 
common  in  all  artiodactyls  and  are  especially  used  by  the  mountain- 
loving  types,  the  extensor  muscles  of  the  back  (sacrospinalis  and 
multifidus)  work  with  the  retractors  of  the  two  hind  limbs  to  give  a 
powerful  thrust. 

The  characteristic  of  the  limbs  is,  of  course,  the  equal  development 
of  digits  III  and  IV,  with  reduction  of  the  rest.  The  gait  was  at  first 
plantigrade,  then  digitigrade;  hoofs,  differing  from  those  of  perisso- 
dactyls,  have  developed  on  the  toes.  The  elongation  of  the  lower  seg- 
ments of  the  limbs  and  shortening  of  the  upper  has  been  similar  to 
that  of  perissodactyls,  but  the  long  metapodials  have  become  united 
in  later  forms  to  make  the  'cannon  bone'.  The  ulna  and  fibula  become 
reduced,  as  in  horses.  The  presence  of  two  digits  has  led  to  the  reten- 
tion of  two  bones  in  the  distal  row  of  carpals,  the  hamate  and  fused 
magnum-trapezoid,  and  these  articulate  in  interlocking  fashion  with 
the  three  proximal  carpals  (Fig.  466).  Similarly  in  the  foot  the  two 
lateral  cuneiforms  are  fused  to  thrust  upon  the  third  digit,  while  the 
fourth  sends  its  thrusts  to  the  cuboid  and  the  latter  is  fused  with  the 
navicular.  Between  this  compound  bone  and  the  talus  there  is  a  very 
characteristic  joint,  the  under  surface  of  the  talus  being  grooved  like 
its  upper  surface.  These  joints  of  the  carpus  and  tarsus  are  evidently 
an  important  part  of  the  apparatus  of  locomotion ;  probably  in  both 
limbs  they  serve  to  take  strain  when  the  animal  is  moving  over  un- 
even ground,  and  in  the  leg  they  are  also  the  seat  of  a  considerable 
propulsive  thrust  from  the  calf-muscles.  In  walking,  the  limb  of  artio- 
dactyls is  moved  as  a  whole  at  the  shoulder  and  hip,  by  action  of  the 
upper  muscles.  The  wrist  and  ankle  joints  bend  just  enough  to  raise 
the  feet  off  the  ground,  and  the  elbow  and  knee  joints,  lying  so  high 
as  to  be  hardly  visible  externally,  also  bend  little.  The  essence  of 
artiodactyl  locomotion  is  the  use  of  the  upper  limb  muscles;  indeed 


xxxi.  i  RUMINANT    STOMACHS  743 

the  hinder  part  of  the  vertebral  column  has  almost  become  part  of 
the  limb! 

The  dentition   of  artiodactyls  is  highly  specialized.   The  upper 


Fig.  491.  Stomach  of  camels  and  ruminants. 
A  shows  the  relationship  of  the  normal  mammalian  stomach  (stippled)  to  that  of  ruminants. 
The  rumen  (r.)  represents  the  cardiac  region,  the  reticulum  {ret.)  the  body.  The  oeso- 
phageal groove  (g.)  and  omasum  (0.)  are  derived  from  the  lesser  curvature  as  far  as  the 
incisura  angularis  and  the  abomasum  (ab.)  represents  the  pyloric  antrum;  d.  duodenum; 

oe.  oesophagus. 

The  omasum  and  abomasum  are  shown  as  if  pulled  downwards.  In  the  camel  zv.c.  are 

the  water  cells.    The  abomasum   is  mostly  lined   with   stratified  squamous  epithelium; 

fundic  glands  are  found  only  in  the  dotted  area.  (Material  for  figure  kindly  supplied  by 

Dr.  A.  T.  Phillipson,  partly  after  Pemkopf.) 


incisors  are  lost  in  later  types,  which  crop  by  means  of  their  gums. 
The  canines  may  form  tusks.  Premolars  are  not  molarized,  but  an 
efficient  grinding  battery  is  often  provided  by  the  very  elongated, 
hypsodont  molars.  These  acquire  a  grinding  surface  by  the  develop- 
ment of  each  of  the  four  original  cusps  into  a  longitudinal  ridge — 


744  ARTIODACTYLS  xxxi.  i- 

the  selenodont  ('moon-tooth')  condition.  The  effect  is  similar  to 
that  arrived  at,  by  very  different  means,  in  horses,  and  the  enamel, 
dentine,  and  cement,  wearing  at  differing  rates,  provide  a  continually 
roughened  surface.  The  temporo-mandibular  joint  is  flattened,  allow- 
ing rotary  movements  of  the  jaw,  produced  by  the  powerful  pterygoid 
muscles. 

The  tongue  is  large  and  is  an  important  part  of  the  cropping  and 
grinding  mechanism;  it  is  very  mobile,  protrusible  and  pointed,  and 
the  papillae  covering  it  are  often  horny.  Elaboration  of  the  stomach 
is  common  to  all  artiodactyls.  In  the  pigs  and  hippopotamuses  there 
is  a  pocket  close  to  the  opening  of  the  oesophagus  and  the  whole  car- 
diac side  secretes  only  mucus,  pepsin  being  produced  on  the  right  side. 
In  the  fully  developed  stomach  of  Ruminantia  there  are  four  chambers 
(Fig.  491),  rumen,  reticulum,  omasum  (=  psalterium  or  manyplies), 
and  abomasum.  The  first  three  are  lined  by  a  stratified  epithelium  of 
oesophageal  type,  folded  into  muscular  ridges.  These  are  low  in  the 
rumen,  form  a  network  in  the  reticulum,  and  are  overlapping  leaves 
in  the  omasum.  Food  is  first  swallowed  into  the  rumen,  where  it  is 
mixed  with  mucus  and  acted  upon  by  a  fauna  of  anaerobic  cellulose- 
splitting  bacteria,  whose  enzymes  break  up  the  walls  of  the  plant  food 
and  reduce  the  whole  to  pulp.  Organic  acids,  from  acetic  acid  upwards, 
are  produced,  absorbed  into  the  circulation,  and  metabolized.  There 
is  also  a  fauna  of  ciliates  in  the  rumen,  which  digest  cellulose  and  are 
themselves  later  digested. 

The  process  of  rumination  depends  upon  an  oesophageal  groove 
running  from  the  cardia  to  the  opening  of  the  omasum.  When  the  lips 
of  this  are  brought  together  food  does  not  enter  the  reticulum  and  is 
returned  from  the  rumen  to  the  mouth.  After  chewing,  the  bolus  is 
again  swallowed,  the  groove  opens,  and  the  food  passes  to  the  reti- 
culum and  omasum.  Here  water  is  pressed  out  and  absorbed  and  the 
remainder  proceeds  to  the  abomasum,  the  'true'  stomach,  with  peptic 
glands.  This  elaborate  digestive  mechanism  has  no  doubt  contributed 
largely  to  the  success  of  the  artiodactyls,  allowing  them  to  eat  their 
food  rapidly  and  then  retire  to  digest  it  in  security.  The  efficient 
cellulose-splitting  system  also  enables  them  to  make  use  of  hard 
grasses  and  other  unpromising  sources  of  nutriment. 

The  brain  is  moderately  well  developed  in  later  artiodactyls,  but 
even  here  the  cerebral  hemispheres  only  partly  cover  the  cerebellum, 
and  in  the  earlier  forms  the  brain  was  relatively  small,  as  it  is  today  in 
hippopotamuses  and  pigs.  The  olfactory  organ  and  related  parts  of 
the  brain  are  well  developed  and  most  artiodactyls  also  have  large 


xxxi.  2  CLASSIFICATION  745 

eyes,  with  a  horizontal  pupil,  and  long  ears  and  an  acute  sense  of 
hearing. 

Artiodactyls  have  an  elaborate  system  of  scent-glands,  on  the  head, 
between  the  digits,  in  the  inguinal  region,  and  elsewhere,  though  not 
usually  around  the  anus.  These  glands  are  used  for  marking  territory 
and  in  the  sexual  and  social  life,  which  is  often  elaborately  organized. 
The  colour  of  the  coat  and  especially  the  form  of  the  head  and  horns 
also  play  an  important  part  in  the  communication  system  between 
individuals. 

The  reproductive  system  remains  rather  close  to  the  presumed 
original  eutherian  condition.  The  uterus  is  bicornuate  and  in  pigs  the 
placenta  is  of  the  diffuse  epitheliochorial  type.  In  ruminants  there  is 
a  cotyledonary  placenta,  but  the  contact  between  maternal  and  foetal 
tissues  is  never  very  close  (syndesmo-chorial)  and  the  allantois  is 
usually  large. 

2.  Classification 

Superorder  5.  Paraxonia 
Order  Artiodactyla 
Suborder  1.  Suiformes 

Infraorder  1.  Palaeodonta.  Pigs  and  peccaries.  Eocene-Recent 
*Diacodexis,    Lower    Eocene,    N.    America;    *Homacodon, 
Middle  Eocene,  N.  America;  *Entelodon,  Lower  Oligocene, 
Holarctic;  Sus,  pigs,  Lower  Pliocene-Recent,  Eurasia  (then 
world-wide);  Phacochoerus,  wart-hog,  Pleistocene-Recent, 
Africa;  Dicotyles,  peccary,  Pleistocene-Recent,  Central  and 
S.  America;  Potamochoerus,  water-hog,  Pleistocene-Recent, 
Africa 
Infraorder  2.  Ancodonta.  Hippopotamuses.  Oligocene-Recent 
* Anihr  ac  other  ium,  Oligocene-Pliocene;  Hippopotamus,  Plio- 
cene-Recent, Eurasia,  Africa 
*Infraorder  3.  Oreodonta.  Eocene-Pliocene.  N.  America 
*Merycoidodon    (=  *Oreodori),     Oligocene;     *Agriochoerus, 
Oligocene-Miocene 
Suborder  2.  Tylopoda.  Camels.  Eocene-Recent 

*Protylopus,  Eocene,  N.  America;  *Poebrotherium,  Oligocene, 
N.  America;  *Proca?neIus,  Miocene-Pliocene,  N.  America; 
*Alticamehts,  Miocene-Pliocene,  N.  America;  Lama, 
alpaca,  Pleistocene-Recent,  S.  America;  Camelus,  camel, 
dromedary,  Pleistocene-Recent,  Asia 


746  ARTIODACTYLS  xxxi.  2- 

Ordcr  Artiodactyla  (cont.) 

Suborder  3.  Ruminantia.  Eocene-Recent 

Infraorder  1.  Tragulina.  Eocene-Recent.  Holarctic,  Africa 
*Archaeomeryx,  Eocene.  Asia;  Tragulus,  chevrotain,  Pliocene- 
Recent,  Asia;  Hyemoschus,  water  chevrotain,  Pleistocene- 
Recent,  Africa 
Infraorder  2.  Pecora.  Oligocene-Recent.  Holarctic,  Africa,  S. 
America 
Family  1.  Cervidae.  Oligocene-Recent.  Holarctic,  S.  America 
*Blasto?neryx,   Miocene-Pliocene,   N.   America;   *Palaeo- 
meryx,  Miocene,  Europe ;  Moschus,  musk-deer,  Pliocene- 
Recent,   Asia;    Cervus,   red   deer,   American   elk,    &c, 
Pliocene-Recent,  Holarctic;  Dama,  fallow  deer,  Pleisto- 
cene-Recent, Eurasia;  Rangifer,  reindeer,  Pleistocene- 
Recent,  Holarctic;  Capreolns,  roe  deer,  Pliocene-Recent, 
Eurasia;  Alee,  moose,  European  elk,  Pleistocene-Recent, 
Holarctic 
Family  2.  Giraffidae.  Miocene-Recent.  Eurasia,  Africa 
Giraffa,  giraffe,  Pliocene-Pleistocene,  Asia;  Recent,  Africa; 
Okapia,  okapi,  Recent,  Africa;  *Palaeotragus,  Miocene- 
Pliocene,  Eurasia;  *Sivatherium,  Pleistocene,  Asia 
Family  3.  Antilocapridae.  Miocene-Recent.  N.  America 
*Merycodus,  Miocene-Pliocene;  Antilocapra,  prong-buck, 
Pleistocene-Recent 
Family  4.  Bovidae.  Miocene-Recent 

*Eotragns,  Miocene,  Europe,  Africa;  Gazella,  gazelles, 
Pliocene-Recent,  Eurasia,  Africa;  Taurotragus,  eland, 
Pleistocene-Recent,  Africa;  Aepyceros,  impala,  Recent, 
Africa;  Bos,  cattle,  yak,  Pleistocene-Recent,  Eurasia  and 
N.  America,  now  world-wide;  Bison,  buffalo,  Pleisto- 
cene-Recent, Holarctic;  Capra,  goat,  Pleistocene- 
Recent,  Eurasia,  Africa  (now  world-wide);  Ovis,  sheep, 
Pliocene-Recent,  Holarctic,  Africa  (now  world-wide). 

3.  The  evolution  of  artiodactyls 

Although  abundant  fossil  material  is  available,  the  lines  of  evolu- 
tion within  the  artiodactyls  are  not  altogether  clear,  and  numerous 
classificatory  arrangements  have  been  suggested.  We  shall,  as  usual, 
follow  that  of  Simpson,  who  recognizes  three  suborders.  The  sub- 
order Suiformes  contains  the  ancestral  Eocene  forms  and  some  of  their 
little-modified  descendants;  it  is  represented  today  by  the  pigs  and 


xxxi.  3  ORIGIN    OF   ARTIODACTYLS  747 

hippopotamuses.  Probably  no  members  of  this  group  developed  the 
ruminating  habit,  and  they  are  sometimes  called  'non  ruminantia'. 
The  suborder  Tylopoda  is  for  the  camels,  and  the  third  suborder, 
Ruminantia,  includes  all  the  other  modern  forms  of  artiodactyl. 
The  earliest  artiodactyls  (Fig.  492),  included  in  the  Suiformes,  were 

SUIFORMES  RUMINANTIA 


Fig.  492.  Chart  of  the  evolution  of  the  Artiodactyla. 


close  to  the  ancestral  stock  of  all  placentals.  In  *Diacodexis  from  the 
North  American  Lower  Eocene  there  were  tritubercular  molars  and 
it  was  probably  a  small,  running,  omnivorous  form,  with  four  toes  on 
each  foot.  These  animals  could  indeed  almost  equally  well  be  classified 
as  insectivores  or  creodonts,  and  the  only  reason  for  placing  them  as 
artiodactyls  is  that  the  talus  had  the  typical  pulley-like  lower  surface. 
Later  Eocene  and  early  Oligocene  forms  developed  a  bunodont  con- 
dition, with  sometimes  six  cusps  in  the  upper  molars,  protocone, 
paracone,  metacone,  hypocone,  protoconule,  and  metaconule.  In  some 
later  forms  these  cusps  show  a  selenodont  condition. 


748  ARTIODACTYLS  xxxi.  4 

4.  Pigs  and  hippopotamuses 

The  pigs  have  remained  essentially  in  this  Eocene  condition; 
Simpson  recognizes  this  by  classifying  them  with  the  Eocene  forms 
in  one  infraorder  Palaeodonta,  distinct  from  the  amphibious  Anco- 
donta   (hippopotamuses  and  anthracotheres)  and  the  *Oreodonta. 


Fig.  493.  Above,  skull  of  the  oreodont  *Merycoidodon  (after  Scott);  below,  skeleton  of 
*Entelodon.  (After  Woodward,  Palaeontology y  Cambridge  University  Press.) 

Close  relatives  of  the  pigs  are  found  from  the  Eocene,  with  bunodont 
molars.  Several  lines  can  be  recognized,  including  the  entelodonts, 
giant  pigs  of  the  Oligocene,  over  5  ft  high  and  12  ft  long  and  of  gravi- 
portal  structure  (Fig.  493).  The  modern  pigs  (Fig.  494)  show  a  nearly 
complete  dentition,  with  persistently  growing  canine  tusks,  used  for 
defence  and  for  digging  roots.  The  orbit  is  continuous  with  the  tem- 
poral fossa.  There  are  no  horns.  There  are  four  toes,  but  only  two 
reach  the  ground.  The  brain  is  small.  They  mostly  live  in  marshy, 
forest  conditions  and  are  omnivorous,  digging  with  the  long  snout  for 
food  detected  by  smell.  The  neck  muscles  are  very  large.  Pigs  live 


xxxi.  4 


PIGS    AND    PECCARIES 


749 


in  families  or  small  troops.  A  large  number  of  young  are  produced 
and  the  male  produces  a  great  volume  of  semen.  Sus  is  mainly  an  Old 
World  genus,  found  from  the  Miocene  onwards.  It  was  represented 
in  Great  Britain  by  the  wild  boar,  common  until  the  sixteenth  cen- 


FiG.  494.  Skeleton  of  the  pig.  (Modified  after  Ellenberger  from  Sisson 
and  Grossman,  Anatomy  of  Domestic  Animals,  3rd  edition  1938,  published 
by  W.  B.  Saunders  Company,  Philadelphia.) 


Fig.  495.  The  wart-hog,  Phacochoerus.  (From  photographs.) 


tury.  The  African  wart-hog  (Phacochoerus)  (Fig.  495)  is  not  very  dis- 
similar. Potamochoerus  is  the  red  river-hog  of  Africa.  The  peccaries 
of  Central  and  South  America  are  similar  to  the  pigs,  but  have  been 
distinct  since  the  Oligocene.  There  are  two  small  lateral  digits  in  the 
fore-foot  and  one  in  the  hind.  A  large  scent-gland  opening  on  the  back 
resembles  a  second  navel,  hence  the  name,  Dicotyles. 

An  offshoot  of  the  palaeodont  line  in  the  Eocene  led  to  the  develop- 
ment of  a  race  of  large  amphibious  animals,  the  anthracotheres  and 


75o  ARTIODACTYLS  xxxi.  4- 

hippopotamuses  (Figs.  496-7),  classed  together  as  an  infraorder 
Ancodonta  of  the  Suiformes.  They  have  an  enormous  barrel-like 
thorax,  with  large  lungs,  short,  relatively  thin  legs  with  four  digits, 
and  a  complete  dentition  with  low-crowned  bunodont  molars,  wearing 
to  a  foliage  pattern.  The  stomach  is  enormous  and  partly  divided. 


Fig.  496.  Hippopotamus,  Hippopotamus.  (From  photographs.) 


Fig.  497.  Skeleton  of  the  hippopotamus.  (From  Owen,  The  Anatomy  of  Vertebrates, 
Longmans,  Green  &  Co.) 

There  are  many  specializations  for  life  in  the  water,  including  eyes, 
ears,  and  nose  on  the  top  of  the  head,  muscles  for  closing  the  nostrils, 
and  a  broad  muzzle.  They  can  remain  submerged  for  five  minutes. 
Modern  hippopotamuses  are  found  only  in  Africa,  but  they  were 
widespread  throughout  the  Old  World  until  recent  times. 

5.  *Oreodonts 

The  oreodonts  were  abundant  and  successful  herbivores,  living  in 
North  America  from  the  Eocene  to  the  early  Pliocene  (Fig.  493). 
They  had  long  bodies  and  short  legs  and  perhaps  somewhat  resembled 


xxxi.  6 


OREODONTS 


751 


pigs.  There  were  four  functional  digits  in  each  foot,  and  a  complete 
tooth  row,  including  molars  whose  cusps  were  selenodont  and  in  some 
later  forms  quite  high-crowned.  Although  Eocene  intermediate  forms 
have  not  been  found,  it  may  be  presumed  that  the  oreodonts  arose 
from  a  basal  palaeodont  ancestor.  They  pursued  an  independent 
evolution  in  North  America  parallel  in  some  ways  to  that  of  the  rumin- 
ants in  the  Old  World.  Unlike  the  latter,  they  were  at  a  disadvantage 
in  the  changed  conditions  of  the  Pliocene  and  then  died  out. 


Jr 


Fig.  498.  Llama,  Lama.  (From  photographs.) 

* 'Agriochoerus  and  its  relatives  were  oreodonts  that  acquired  claws 
and  therefore  represent  a  parallel  to  ancylopod  perissodactyls,  with 
which  they  were  for  a  long  time  confused.  It  has  been  guessed  by  some 
that  the  claws  were  used  for  digging  roots,  by  others  that  they  were 
for  climbing. 

6.  Camels 

All  other  artiodactyls  chew  the  cud  and  are  often  included  in  a 
single  group  Ruminantia.  However,  the  camels  have  been  a  separate 
stock  since  the  Eocene  and  are  so  distinct  from  the  remainder  that  it 
is  convenient  to  keep  them  in  a  separate  suborder  Tylopoda.  They 
have  been  common  animals  since  the  late  Eocene,  flourishing  especi- 
ally in  North  America,  although,  like  the  horses,  they  died  out  there 
very  recently  and  survive  today  only  as  remnants,  which  migrated 
from  North  America  in  the  Pleistocene,  the  camels  to  the  Old  World 
and  the  llamas  to  South  America.  The  bactrian  camel  of  the  Gobi 
Desert  in  central  Asia  is  perhaps  a  wild  form,  all  others  being  com- 
mensals of  man.  The  llamas  (Fig.  498),  though  similar  in  basic 
structure  to  the  camels,  differ  in  the  smaller  size,  long  hair,  and  lack 


752  ARTIODACTYLS  xxxi.  6- 

of  hump.  When  wild  they  are  mainly  mountain-dwellers.  The  spitting 
of  the  llama  is  a  protective  device,  the  whole  contents  of  the  stomach 
being  thrown  at  the  attacker! 

The  Tylopoda  show  some  features  retained  from  the  Eocene  condi- 
tion, some  developments  parallel  to  those  found  in  the  Ruminantia, 
and  various  special  features  of  their  own,  the  latter  mainly  in  charac- 
ters that  suit  them  for  life  in  sandy  desert  conditions.  In  the  limbs 


Fig.  499.  Skeleton  of  dromedary.  (From  Owen,  The  Anatomy  of  Vertebrates, 
Longmans,  Green  &  Co.) 

(Fig.  499)  there  has  been  complete  loss  of  the  lateral  digits  and  of  some 
carpals  and  tarsals,  but  not  the  fusion  of  navicular  and  cuboid  that  is 
so  characteristic  of  the  Pecora.  A  specialized  feature  is  the  loss  of  the 
hoofs.  They  were  present  in  early  camels  but  are  replaced  in  modern 
forms  by  a  nail  and  large  pad.  The  toes  thus  spread  sideways  and  en- 
able the  animals  to  walk  on  soft  or  sandy  ground.  The  large  hump  of 
fat  on  the  back  provides  water  as  well  as  calories  when  metabolized. 
The  ruminating  mechanism  is  different  from  that  of  the  Pecora  and 
simpler  (Fig.  491). 

The  wall  of  the  rumen  contains  a  number  of  pockets  separated  by 
muscular  walls.  These  are  usually  called  water  pockets  and  have  been 
supposed  to  have  a  storage  function,  with  sphincters.  However  their 
walls  are  glandular  and  their  function  may  be  digestive.  There  is  no 
external  separation  of  omasum  and  abomasum,  which  form  a  single 


xxxi.  7  CAMELS  753 

tubular  organ  with  glandular  lining.  These  differences  suggest  that 
the  ruminating  habit  may  have  been  evolved  separately  in  camels  and 
Ruminantia  (Bohlken,  i960). 

In  the  head  there  are  many  features  of  similarity  to  the  Pecora. 
Cropping  is  by  means  of  procumbent  lower  incisors,  working  against 
specialized  premaxillary  gums ;  but  an  upper  incisor  and  canine  are  still 
present  (three  incisors  in  the  young).  The  molars  have  a  typical 
selenodont  pattern,  and  the  structure  of  the  skull  shows  the  develop- 
ments so  commonly  seen  as  a  result  of  herbivorous  life,  such  as  closure 
of  the  post-orbital  bar.  The  lips  and  tongue  are  tough  and  able  to 
chew  spiny  desert  plants.  A  peculiar  feature  of  camels  is  that  the  red 
blood  corpuscles  are  oval,  as  in  no  other  mammal.  The  placenta  is  of 
a  diffuse  (non-cotyledonary)  syndesmochorial  type. 

There  is  no  doubt  that  many  of  these  features  have  developed 
independently  in  camels  and  Pecora;  the  Eocene  camel-ancestors  did 
not  show  them.  At  the  stage  of  *Protylopus  the  camels  were  small  and 
had  short  limbs,  with  separate  radius  and  ulna  and  four  digits  in  the 
manus.  Throughout  the  Oligocene  many  primitive  features  still 
remained.  *Poebrotherium  was  about  3  ft  high,  with  a  complete  denti- 
tion, and  orbit  only  partly  closed  behind.  However,  the  lateral  toes 
had  been  lost  and  the  digits  began  to  diverge  distally,  though  probably 
still  carrying  hoofs.  The  remaining  increase  of  size,  and  the  develop- 
ment of  other  special  camel  features  can  be  traced  slowly  through  such 
types  as  *Procamelus  of  the  Miocene  and  Pliocene.  During  the  dry 
Miocene  times  the  type  was  very  successful  in  North  America  and 
developed  various  lines,  such  as  *Alticamelus,  the  giraffe- camels,  with 
long  necks. 

7.  Ruminants 

The  most  successful  modern  artiodactyls,  the  deer  (Cervidae)  and 
cattle,  sheep,  and  antelopes  (Bovidae),  have  flourished  only  since  the 
Miocene  and  are  thus  the  most  recent  ungulate  group,  largely  re- 
placing the  tylopods,  oreodonts,  perissodactyls,  and  still  earlier  prot- 
ungulate  and  paenungulate  types.  They  have  always  been  mainly  an 
Old  World  group  and  this  remains  their  headquarters,  though  some 
have  reached  other  parts  of  the  world.  The  early  ancestors  of  the 
ruminants  can  be  traced  to  Oligocene  and  late  Eocene  forms  very  like 
the  early  camels,  oreodonts,  and  other  primitive  artiodactyls;  the 
modern  chevrotains  (Tragulns)  retain  some  of  the  features  of  this 
early  stage. 

The  characteristic  features  of  the  ruminants  are  the  full  develop- 


754 


ARTIODACTYLS 


xxxi.  7- 


ment  of  the  feeding  system  described  on  p.  743,  with  loss  of  the  upper 
incisors  and  often  also  of  the  canines,  development  of  selenodont 
molars,  and  of  a  four-chambered  stomach.  In  the  legs  only  two  digits 
are  functional,  though  traces  of  others  may  be  found.  Besides  loss  of 
the  extra  carpal  and  tarsal  bones  there  is  fusion  of  those  that  remain 
and  in  particular  of  the  navicular  and  cuboid.  Protection  is  afforded 
mainly  by  swift  running  and  keen  senses,  but  in  nearly  all  ruminants 
also  by  antlers  or  horns  on  the  head. 

This  definition  will  not  quite  cover  all  members  of  the  groups.  The 
chevrotains  keep  so  many  primitive  features  that  although  they  are 


Fig.  500.  Chevrotain,  Tragulus.  (After  Beddard,  Cambridge  Nat.  Hist.,  Macmillan  &  Co.) 

certainly  related  to  the  ancestors  of  the  other  ruminants  it  would  be 
almost  as  easy  to  class  them  with  the  camels.  This  is  another  case 
where  it  is  difficult  to  decide  whether  to  make  horizontal  or  vertical 
classificatory  divisions;  any  system  is  bound  to  be  arbitrary. 

8.  Chevrotains 

The  deerlets  or  mouse-deer  of  Africa  and  Asia  (Fig.  500)  are  peculiar 
little  creatures,  only  a  foot  high,  with  more  external  resemblance  to  a 
rodent  than  to  modern  deer.  In  some  features  they  show  suggestive 
similarity  to  the  pigs.  There  are  no  horns,  but  the  upper  canines  are 
large  and  tusk-like.  The  upper  incisors  have  been  lost  and  the  molars 
are  selenodont,  but  the  stomach  has  only  three  chambers.  The  feet 
have  four,  hoofed  digits  in  each  limb,  and  although  the  two  main 
metatarsals  are  fused  to  form  a  cannon  bone  the  metacarpals  are  still 
partly  separate.  The  navicular,  cuboid,  and  external  cuneiform  make 
a  single  bone,  this  being  a  'diagnostic'  ruminant  character.  The 
placenta  is  diffuse,  as  in  camels.  The  individuals  live  alone  in  the 
forests,  pairing  only  for  breeding. 

In  many  of  these  characteristics  the  chevrotains  show  signs  of 


XXXI.  io 


PECORA 


755 


retention  of  an  ancient  organization,  and  fossil  forms  similar  to  them 
are  found  in  the  Pliocene.  Animals  not  very  different  (*Archaeo- 
meryx)  are  found  back  to  the  Eocene  and  were  then  like  the  early 
camels  or  palaeodonts;  they  may  well  be  close  to  the  ancestry  of  all 
ruminants.  Several  similar  types  and  lines  can  be  recognized.  Evi- 
dently the  group  represents  a  population  persisting  with  rather  little 
change  since  the  Eocene,  and  this  status  is  represented  bv  recognizing 
an  infraorder  Tragulina  of  the  Ruminantia,  contrasting  with  the 
Pecora,  which  includes  all  the  higher  ruminants. 

9.  Pecora 

The  true  ruminants  show  the  full  development  of  artiodactyl 
characteristics.  They  have  been  an 
actively  expanding  group  since  the 
Miocene  and  are  now  the  most  success- 
ful of  the  ungulates,  existing  in  vast 
herds  in  Africa  and  to  a  lesser  extent 
in  Asia  and  North  America,  though 
strangely  enough  hardly  penetrating  to 
South  America.  The  modern  and  fossil 
forms  are  of  three  types.  The  deer 
(Cervidae),  browsing  creatures  with 
bony  deciduous  antlers,  are  closest  to  the 
central  stock,  from  which  have  been  derived  on  the  one  hand  the 
giraffes  and  on  the  other  the  great  groups  of  grazing  ruminants  or 
Bovidae,  including  the  primitive  prong-buck  and  the  host  of  sheep, 
goats,  cattle,  and  antelopes. 

10.  Cervidae 

The  ancestral  population  from  which  these  forms  arose  must  have 
been  quite  similar  to  the  Eocene  traguline  *Archaeomeryx,  but  the 
group  does  not  become  distinctly  recognizable  until  the  Oligocene. 
The  early  members  either  had  large  canines  and  no  antlers,  as  in 
*Blastomcryx  of  the  Miocene  of  North  America,  or,  as  in  *Palaeo- 
meryx  of  the  Miocene  of  Europe,  they  possessed  a  bony  outgrowth 
covered  with  skin  and  not  shed.  Moschus,  the  musk-deer  (Fig.  501) 
of  central  Asia,  also  has  large  permanently  growing  canines  and  no 
antlers  and  is  probably  a  survivor  of  this  Miocene  stage  of  evolution. 
It  is  intermediate  in  many  respects  between  Traguhis  and  the  Cer- 
vidae and  some  classify  it  with  the  former.  Musk-deer  are  about  2  ft 
high  and  the  individuals  live  alone  in  mountain  forests.  The  much- 


Fig.  501.  Musk-deer,  Moschus. 

(After  Beddard,  Cambridge  Natural 

History,  Macmillan  &  Co.) 


(756) 


Fig.  502.  Growth  of  the  antlers  of  a  mule  deer.  The  bony  outgrowth  is  covered  with  very 
vascular  skin  (velvet)  which  is  shed  when  growth  is  complete,  shortly  before  the  rut.  The 
antlers  are  then  shed.  (From  American  Mammals,  by  W.  J.  Hamilton,  McGraw  Hill  Book 

Company.) 


XXXI.   IO-II 


DEER 


757 


valued  musk  of  the  male  is  a  pre-putial  gland,  in  the  form  of  a  sac. 
The  true  deer,  Cervidae,  have  developed  antlers  in  the  males  (Fig. 
502),  bony  growths  shed  each  year  and  forming  progressively  more 
branches  as  the  animal  grows 
older  (Fig.  503).  In  the  reindeer 
the  females  also  have  antlers.  A 
sign  of  the  rather  primitive  nature 
of  the  deer  is  the  retention  of 
definite  rudiments  of  the  first  two 
phalanges  of  the  lateral  digits. 
The  molars  are  brachydont,  but 
the  placenta  cotyledonary  as  in 
bovidae.  The  deer  (Fig.  504) 
have  been  common  since  the 
Pliocene,  as  browsing  animals  of 
the  forests  of  the  Holarctic  region 
and  South  America,  but  not 
Africa.  They  live  in  herds  with 
an  elaborate  social  organization, 
based  on  the  supremacy  of  a 
leading  male,  maintained  by  a  suc- 
cession of  'fights'  with  his  rivals. 
These  fights  are  very  fierce,  but 
do  not  necessarily  result  in  death, 
and  indeed  the  complicated  horns 
interlock  in  such  a  way  as  to 
mitigate  their  danger  to  the  chal- 
lenger. Red  deer  (Cervus  elaphus) 
are  still  wild  in  Britain  in  Scot- 
land, the  Lake  District,  Exmoor, 
and  the  New  Forest.  The  antlers 
have  six  or  more  points.  Roe  deer 
(Caproelus)  have  smaller  antlers  (three  points).  They  are  also  indigenous 
in  Great  Britain;  fallow  deer  (Dama)  have  been  introduced,  and  are 
usually  spotted,  with  palmate  antlers. 

1 1 .  Giraffidae 

The  giraffes  (Fig.  505),  like  the  Cervidae,  from  which  they  diverged 
in  the  Miocene,  are  browsing  animals,  now  restricted  to  tropical 
Africa.  The  teeth  are  low-crowned  and  the  head  bears  up  to  five 
simple  skin-covered  bony  prongs  in  both  sexes.  This  has  been  held  to 


1st  year 

Fig.  503.  Series  of  antlers  in  the  British 

Museum  (Natural  History)  showing  the 

increasing  number  of  tines  in  successive 

years.  (After  Romanes.) 


758 


ARTIODACTYLS 


XXXI.   II 


be  a  condition  similar  to  that  of  Miocene  cervids,  whereas  others 
believe  that  the  bony  core  is  of  dermal  origin,  as  in  bovids,  fusing 
later  with  the  frontal.  In  the  okapi  there  is  a  rudimentary  keratinous 
horn  at  the  tip.  The  lateral  digits  are  completely  absent  and  the  legs 
are  very  long;  the  whole  structure  is  specialized  to  carry  the  great  bulk 
on  the  fore-legs,  the  head  and  neck  balancing  the  weight  of  the  body 
and  the  hind-legs  being  used  mainly  for  propulsion.  In  walking  the 
fore-  and  hind-legs  of  one  side  move  together;  since  the  weight  is 
balanced  on  the  fore-legs  there  is  no  use  of  the  tripodal  method  of 


Fig.  504.  Deer,  Cervus.  (From  life.) 


movement  that  is  usual  in  quadrupeds.  This  is  an  extreme  develop- 
ment of  the  type  of  vertebral  organization  in  which  the  weight-carry- 
ing beam  ends  in  the  middle  of  the  back,  there  being  a  small  number 
of  ribs,  so  that  the  hinder  part  of  the  column  functions  as  an  upper 
segment  of  the  hind  limbs  and  the  extensor  muscles  of  the  back  aid  in 
propulsion.  The  long  neck  makes  it  possible  to  balance  the  great 
weight  on  the  fore-legs,  and  is  of  use  not  only  for  reaching  high 
branches  but  also  as  a  look-out  among  the  long  grasses.  The  rare 
Okapia  (Fig.  506),  discovered  in  1900  in  the  Belgian  Congo,  is  a  form 
with  shorter  legs  and  neck,  very  similar  to  *Palaeotragas  and  other 
Pliocene  animals,  all  possessing  small  horns.  Other  lines  (*Sivatherinm) 
acquired  a  pair  of  large  non-deciduous  horns,  a  course  of  evolution 


(759) 


Fig.  505.  Giraffe  (Giraffa).  (From  photographs.) 


Fig.  506.  Okapi,  Okapio.  (From  photographs.) 


760 


ARTIODACTYLS 


parallel  to  that  found  in  Cervidae.  The  exact  origin  and  affinities  of 
the  family  remain  uncertain. 

12.  Antilocapridae  and  Bovidae 

The  remaining  Pecora  are  all  rather  alike  and  are  often  placed  in  a 
single  family,  Bovidae.  However,  the  prong-buck,  Antilocapra  (Fig. 
507)  of  the  North  American  west,  and  its  numerous  fossil  allies,  all 

New  World  forms,  have  been  distinct 
since  before  the  Miocene  from  the  true 
bovids,  evolving  in  the  Old  World.  The 
origin  of  the  two  groups  is  obscure  and 
we  have  no  Eocene  or  Oligocene  fossils 
that  are  certainly  on  the  bovid  line 
of  evolution.  As  already  mentioned 
*Archaeomeryx  and  other  Eocene  tragu- 
lines  show  us  a  type  of  population  from 
which  the  Pecora  could  all  have  been 
evolved,  but  the  stages  of  the  transforma- 
tion have  not  been  found. 

Antilocaprids  and  bovids  are  alike  in 
living  in  herds  and  in  their  grazing  habits, 
with  which  are  associated  deeply  hypso- 
dont  molars.  The  side  toes  have  been  almost  or  completely  lost,  a  de- 
velopment occurring  parallel  to  that  of  the  cervids,  since  the  common 
ancestry  almost  certainly  possessed  lateral  toes,  which  are  indeed 
present  in  rudimentary  form  in  some  bovids.  In  Antilocapra  (Fig.  507) 
the  horns,  present  only  in  the  males,  are  two-branched  and  have  a  bony 
core  and  rather  soft  keratinous  covering,  the  latter  but  not  the  former 
being  shed.  This  therefore  suggests  how  a  skin-covered  antler,  such  as 
that  of  the  Cervidae,  may  have  become  converted  into  the  bovid  horn.  In 
earlier  antilocaprids,  such  as  the  Miocene  *Merycodus,  the  horns  were 
more  elaborately  branched;  evidently  the  group  has  developed  a  horn 
structure  parallel  to  that  of  the  Cervidae.  In  all  true  bovids  the  horns 
are  permanent  coverings  for  the  bony  core.  They  are  unbranched, 
though  curved  and  twisted  in  various  geometrically  interesting  ways. 
Moreover,  they  are  usually  borne  in  both  sexes  (though  often  larger 
in  the  male)  and  their  function  is  definitely  defensive,  as  well  as  social 
and  sexual.  Correspondingly  the  social  organization  is  often  into  large 
herds,  rather  than  into  the  small  family  groups  under  a  dominant  stag, 
such  as  are  found  among  Cervidae.  Grazing  on  open  plains  and 
mountains  has  presumably  led  to  the  formation  of  the  larger  herds, 


Fig.  507.  Prong-buck,  Antilo- 
capra. (From  a  photograph.) 


xxxi.  iz  BOVIDAE  761 

smaller  and  more  closely  knit  groups  being  more  suitable  for  forest 
life.  The  placenta  is  cotyledonary. 

The  Bovidae,  with  more  than  100  genera,  is  much  the  largest 
ungulate  family.  The  original  centre  of  evolution  of  the  family  was  in 
Eurasia,  where  they  are  now  less  common,  whereas  in  Africa  they  are 
particularly  successful  at  present.  A  few  types,  such  as  the  bison,  reached 
North  America,  but  none  entered  South  America  until  man  showed 
that  they  can  flourish  there,  and  indeed  also  in  Australia.  The  fact  that 
we  possess  numerous  fossil  remains  and  that  the  group  is  still  at  the 
height  of  its  development  makes  classification  very  difficult.  This  is  the 
situation  that  we  should  expect,  remembering  that  evolution  consists 
in  the  slow  change  of  the  characteristics  of  populations.  At  first  thought 
it  may  seem  paradoxical  that  in  a  group  so  recently  evolved  and  of 
which  we  know  so  much  it  should  be  exceptionally  difficult  to  trace 
affinities  and  lines  of  descent.  The  fact  is  that  the  numerous  remains  of 
fossil  bovids  from  the  Pliocene  and  Miocene  are  still  quite  insufficient 
to  enable  us  to  reconstruct  the  changes  in  the  populations.  It  is  not 
really  to  be  expected  that  the  relatively  few  specimens  of  these  large 
animals  that  can  be  collected  and  studied  should  show  us  the  detailed 
changes,  extending  over  20  million  years  or  more,  by  which  a  popula- 
tion of  perhaps  a  million  small  creatures  such  as  *Eotragus  of  the 
Miocene,  developed  into  the  present  bovid  population  of,  say,  a 
thousand  million  animals,  divisible  into  hundreds  of  non-interbreeding 
populations  that  range  in  structure  and  habits  from  the  gazelle  to  the 
bison.  An  imaginative  look  at  the  details  of  evolutionary  change  reveals 
a  terrifyingly  complicated  system,  which  we  can  hardly  hope  to  follow 
in  detail.  The  geological  information  can  surely  never  be  sufficient  to 
show  us  the  necessary  facts  about  the  variation  of  such  great  popula- 
tions, and  their  gradual  changes,  at  least  in  the  case  of  animals  as  large 
and  rarely  preserved  as  Bovidae.  We  know  hardly  anything  about 
variation  and  heredity  in  our  own  cattle,  so  how  can  we  hope  to  follow 
the  genetics  of  their  ancestors  ?  Yet  nothing  less  than  a  full  view  of  the 
gradual  population  changes  will  show  us  how  the  evolution  of  a  group 
has  proceeded. 

Following  types  of  organization  over  long  geological  periods  gives  a 
deceptively  simplified  idea  of  the  stages  traversed.  We  recognize  the 
'stages'  because,  fortunately  for  us,  only  tiny  remnants  of  the  popula- 
tions have  been  preserved,  and  perhaps  some  'primitive'  types  remain 
to  the  present  day.  Thus  in  the  long  history  of  the  perissodactyls  we 
can  refer  all  our  modern  and  fossil  forms  to  some  160  genera;  the  tapirs 
are  there  to  show  us  a  very  ancient  condition,  and  we  know  just  enough 


762 


ARTIODACTYLS 


XXXI.    12 


fossil  horses  to  arrange  them  in  a  number  of  series  with  side  branches, 
so  that  we  feel  that  we  can  imagine  the  whole  evolution  of  the  group. 
It  is  interesting  that  the  sequence  of  evolution  used  as  a  type-specimen 
for  students  is  so  often  that  of  the  horses  and  not  of  the  bovids, 
although  we  have  very  much  more  material  for  the  latter,  at  least  in 
the  later  stages.  It  would  be  wise  to  study  the  two  together  and  to  learn 
from  the  difficulty  of  recognizing  clear-cut  boundaries  among  the 

millions  in  the  herds  of  intergrading 
sheep,  goats,  oxen,  and  antelopes 
that  the  most  important  result  of  the 
discovery  of  evolutionary  change 
was  the  realization  that  our  logic 
and  use  of  words  can  no  longer 
depend,  as  the  ancients  thought  and 
many  backward-lookers  still  wish 
today,  on  the  recognition  of  a  cer- 
tain number  of  'species',  to  one  of 
which  every  individual  can  be  re- 
ferred. 

In  trying  to  classify  the  Bovidae 
we  may  perhaps  recognize  a  central 
group  of  'antelopes',  but  the  term 
is  vague  and  certainly  includes 
several  diverse  lines;  it  is  not  even 
possible  to  find  criteria  for  saying 
'this  is  an  antelope,  that  a  cow, 
and  this  other  a  sheep'.  'Typical' 
antelopes  (Fig.  508)  live  in  Eurasia  and  Africa,  especially  the  latter. 
They  are  rather  tall  and  slender,  with  smooth  hair  and  backward- 
curving  horns,  living  mostly  on  warm  or  tropical  plains.  The  gazelles 
may  be  taken  as  an  example  among  many.  The  oxen  are  heavier 
animals,  often  almost  of  graviportal  structure,  but  with  very  high 
thoracic  spines;  they  live  in  cooler  conditions  on  more  northern  plains 
and  have  more  and  shaggier  hair.  Their  horns  curve  forwards  and  are 
not  twisted.  They  originated  in  Eurasia.  The  domestic  cattle  and  yaks, 
Bos  (Fig.  509),  are  good  examples,  and  the  Bison  (Fig.  510)  are  related 
creatures,  now  almost  restricted  to  North  America.  There  are  animals, 
however,  that,  with  the  criteria  used,  cannot  be  classed  as  either 
'antelopes'  or  'oxen';  for  instance,  the  elands  (Taurotragus)  (Fig.  511) 
of  Africa  are  large  and  cow-like,  but  have  backwardly  directed  and 
twisted  horns.  Similarly  the  ovine  (sheep  and  goat)  section  of  the 


Fig.   508.    Impala  antelope,  Aepyceros 
(From  life.) 


(763) 


Fig.  509.  Central  Asian  Yak,  Bos.  (From  photographs.) 


Fig.  510.  American  bison,  Bison.  (From  photographs.) 


tppps^iHr- 


Fig.  511.  Eland,  Taurotragus.  (From  photographs.) 


764 


ARTIODACTYLS 


XXXI.   12 


family  is  not  clearly  marked  off  from  the  antelopine.  The  goats  (Capra) 
are  characteristically  mountain-living  animals  of  the  Holarctic  region, 
with  backwardly  curved  but  not  twisted  horns,  and  the  sheep,  Ovis 
(Fig.  512),  are  closely  related,  but  addicted  to  less  mountainous 
country  and  with  a  slight  spiral  on  the  horns.  The  beard  and  scent 
glands  of  the  male  are  signs  that  there  are  great  differences  in  social 
and  sexual  organization  between  sheep  and  goat  life,  in  spite  of  the 
similarity  in  structure. 

Thus  there  is  very  great  variety  of  life  and  structure  in  the  modern 
bovids,  and  one  of  the  most  striking  conclusions  about  the  group  is 
that  the  specialists  have  not  yet  succeeded  in  finding  an  agreed  system 
of  classification.  More  important  perhaps  than  these  problems  is  the 
fact  that  with  their  fine  cropping  mechanism,  grinding  battery  and 
stomach  the  bovids  provide  the  only  satisfactory  intermediary  by 
which  grass  can  be  used  as  a  contributor  to  human  life.  This,  with  their 
peaceful  and  gregarious  disposition,  has  made  them  our  most  impor- 
tant commensal.  If  there  were  no  Bovidae  there  would  be  fewer  human 
beings  in  the  world,  and  our  social  organization  would  be  very  dif- 
ferent. The  obverse  is  also  true ;  it  is  probable  that  their  lives  and  ours 
will  continue  to  evolve  together  and  mutually  to  modify  each  other. 


FlG.  512.  Barbary  sheep,  Ovis.  (From  life.) 


XXXII 

CONCLUSION.  EVOLUTIONARY  CHANGES 
OF  THE  LIFE  OF  VERTEBRATES 

1 .  The  life  of  the  earliest  chordates 

We  set  out  to  try  to  define  the  features  that  are  characteristic  of 
vertebrate  life,  hoping  then  to  show  how  these  features  have  changed 
during  evolutionary  history.  We  may  now  summarize  the  evidence 
collected  and  see  how  far  it  is  possible  to  make  general  statements 
about  vertebrate  life  and  the  factors  that  change  it. 

The  vertebrate  type  of  organization  has  proved  capable  of  support- 
ing life  under  a  wide  variety  of  circumstances;  most  of  its  modern 
forms  operate  under  conditions  very  different  from  those  in  which 
the  type  first  appeared.  According  to  the  most  probable  theory  (p.  47) 
chordate  life  began  at  the  sea  surface,  as  the  ciliated  larvae  of  some 
creatures  rather  like  sessile  echinoderms.  The  first  fish-like  animals, 
with  the  characteristic  chordate  organization,  appeared  when  such 
larvae  acquired  powers  of  rhythmic  metachronal  muscular  movement, 
in  order  to  allow  support  of  a  large  weight.  We  can  still  see  approxi- 
mately this  stage  today  in  amphioxus.  It  is  not  possible  to  summarize 
the  nature  of  this  organization  in  any  brief  general  statement.  The 
science  of  morphology  is  still  young  and  ill  equipped  with  general 
principles;  it  does  not  allow  us  to  define  the  varieties  of  living  organiza- 
tion with  precision  and  completeness.  At  present  we  cannot  give  a 
full  description  such  as  we  might  wish  for,  specifying  the  composition 
and  activities  of  an  organism  or  the  inherited  code  of  instructions 
under  which  it  operates.  We  can  only  describe  some  of  the  methods 
by  which  the  system  maintains  itself,  for  example  its  means  of  nutri- 
tion, respiration,  and  reproduction. 

The  earliest  chordates  showed  a  rather  low  level  of  metazoan  organi- 
zation, with  a  relatively  small  number  of  distinct  cell  types  and  few 
special  organs.  Nitrogen  and  other  raw  materials  were  obtained  in  the 
form  of  minute  plants,  collected  by  ciliary  action  of  the  pharynx  and  gill- 
slits.  The  food  was  broken  down  by  a  system  of  enzymes  working  in 
alkaline  solution,  and  absorbed  through  the  walls  of  a  simple  intestine. 
There  was  probably  no  specialization  of  cells  of  the  walls  of  the  gut  to 
produce  enzymes  or  to  perform  particular  operations  of  conversion  or 
storage;  at  least  no  special  liver,  pancreas,  or  other  organs  were  present 
for  these  purposes.  There  were  no  special  respiratory  surfaces  and  the 


766  CONCLUSION  xxxn.  i- 

oxygen  was  carried  to  the  tissues  in  simple  solution  in  colourless  blood. 
The  circulatory  system  perhaps  at  first  involved  little  more  than  an 
irregular  set  of  spaces  among  the  cells,  but  quite  early  there  must  have 
appeared  the  distinct  contractile  vessels,  containing  a  blood  with 
composition  distinct  from  that  of  the  surrounding  lymphatic  or  tissue 
spaces.  The  method  of  excretion  of  the  earliest  chordates  is  not  clearly 
known;  it  perhaps  involved  no  highly  specialized  cells,  but  occurred 
all  over  the  body  surface.  Since  the  animals  were  marine  there  were 
no  serious  osmotic  problems.  Movement  was  by  the  metachronal  con- 
traction of  a  series  of  blocks  of  longitudinally  arranged  muscle-fibres 
and  this  serial  repetition  of  the  muscles  and  their  attendant  nerves  and 
blood-vessels  has  left  a  large  mark  on  the  chordate  plan  of  life. 

The  nervous  organization  was  at  first  based  on  a  system  of  nerve- 
cells  and  fibres  lying  spread  out  below  the  epidermis,  but  then  became 
concentrated  dorsally  in  the  walls  of  a  neural  tube.  The  special 
receptor  organs  were  probably  simple  and  lay  either  in  the  skin  or 
within  the  tube,  perhaps  along  its  whole  length,  with  little  concentra- 
tion at  the  front  end  and  no  definite  anterior  enlargement  or  brain. 
The  system  functioned  as  a  series  of  more  or  less  separate  reflex  arcs, 
activation  coming  from  the  stimulation  of  receptor  organs  by  changes 
in  the  world  around.  There  were  no  large  masses  of  nervous  tissue 
and  little  possibility  of  sustained  independent  action  by  the  creatures, 
which  probably  showed  little  flexibility  of  behaviour  or  variation  of 
action  with  experience.  The  only  endocrine  influences  were  the  effects 
of  cell  by-products  on  neighbouring  tissues;  there  were  no  specialized 
glands  of  internal  secretion. 

Reproduction  was  presumably  sexual  (perhaps  also  by  budding)  and 
development  followed  the  pattern  of  radial  (indeterminate)  cleavage 
and  gastrulation  by  invagination,  with  chordo-mesoderm  separating 
from  the  endoderm.  The  young  were  provided  with  yolk  for  their 
development,  but  were  probably  not  otherwise  cared  for  by  their 
parents. 

This  gives  a  rough  picture  of  chordate  organization  in  the  Cambrian 
period  when  it  probably  first  arose,  500  million  years  ago,  after  the 
paedomorphic  change  by  which  a  previously  larval  creature  became 
sexually  mature.  It  was  an  organization  that  had  already  proceeded  far 
from  the  aggregation  of  similar  cells  that  presumably  characterized  the 
first  metazoans.  Its  embryological  processes  were  already  sufficiently 
elaborate  to  produce  a  creature  with  well-marked  organ  systems, 
though  these  did  not  have  the  numerous  cell  types  and  anatomically 
separate  parts  that  are  found  later. 


XXXII.  2  (767) 

2.  Comparison  of  the  life  of  early  chordates  with  that  of  mammals 

Such  an  early  chordate  is  immensely  complicated  when  considered 
as  a  chemical  system,  yet  it  lacks  the  specializations  that  later  became 
so  characteristic  of  vertebrates.  The  difference  appears  very  clearly  if 
we  contrast  the  organization  and  life  of  some  such  simple,  amphioxus- 
like  chordate  with  those  of  a  mammal.  In  almost  every  part  of  the  body 
of  the  latter  we  find  cell  types  and  organs  that  are  not  yet  differentiated 
in  the  former.  For  illustration  of  this  difference  we  can  look  at  almost 
any  tissue,  say  the  skin,  the  blood,  the  gut,  or  the  brain.  In  a  mammal 
the  skin  contains  far  more  types  of  cell  than  are  present  in  amphioxus; 
there  are  hairs  and  these  are  different  in  various  parts  of  the  body; 
there  are  several  types  of  gland  and  of  receptor  organ.  The  blood, 
again,  circulates  with  great  rapidity  and  in  two  circuits ;  it  is  delicately 
adjusted  in  composition  so  as  to  allow  rapid  flow  of  materials  to  the 
tissues ;  it  contains  haemoglobin  in  special  corpuscles.  In  addition  there 
are  numerous  types  of  cell  able  to  be  used  for  defence,  and  a  system  of 
antibodies  for  the  same  purpose  that  is  almost  certainly  also  far  beyond 
anything  found  in  the  earlier  creature.  Digestion  in  a  mammal  involves 
an  elaborate  arrangement  of  mouth,  oesophagus,  stomach,  and  intes- 
tine, each  with  a  controlled  pH  and  special  masses  of  cells  aggregated 
into  groups,  such  as  the  salivary  glands,  pancreas,  and  liver,  the  latter 
a  most  elaborate  chemical  workshop.  Finally  the  nervous  system 
possesses  an  enormous  number  of  cells  and  elaborate  receptor  organs. 
It  gives  the  power  to  react  to  many  aspects  of  environmental  change 
that  cannot  be  discriminated  by  the  simpler  organism.  Nervous  con- 
duction is  rapid,  allowing  these  large  creatures  to  be  well  coordinated. 
The  nervous  system,  working  through  the  many  contractile  parts  that 
are  provided  by  the  muscular  system,  enables  the  performance  of 
numerous  elaborate  acts,  helpful  in  obtaining  food,  escaping  enemies, 
and  perhaps  particularly  in  providing  for  the  care  of  young,  which  is 
another  characteristic  mammalian  feature.  The  pattern  of  behaviour 
does  not  always  follow  one  single  course,  but  is  adaptable  and  suited  to 
the  conditions  that  are  likely  in  view  of  past  experience  to  be  en- 
countered. There  is  an  elaborate  system  of  chemical  signalling  by 
many  endocrine  glands. 

No  doubt  this  greater  complexity  found  in  mammalian  organs 
reflects  a  similar  complication  of  the  metabolic  processes  throughout 
the  body,  though  as  yet  we  have  little  information  about  this.  More- 
over, an  organism  with  so  many  diverse  parts  presumably  depends  for 
its  propagation  on  a  genetical  system  that  is  very  elaborate.  There  is 


768  CONCLUSION  xxxn.  z- 

evidence  that  the  genetic  mechanism  is  more  complicated  in  the  more 
elaborately  organized  later  animals.  In  reptiles,  birds,  and  mammals 
each  individual  has  a  genetic  constitution  so  specific  that  a  piece  of 
tissue  grafted  from  one  individual  to  another  of  the  same  species  (a 
homograft)  nearly  always  sets  up  an  immunity  reaction  and  is  ulti- 
mately destroyed.  However,  in  urodeles  such  homografts  are  success- 
ful, presumably  because  the  genetic  mechanism  is  less  specific. 

3.  The  increasing  complexity  and  variety  of  vertebrates 

The  above  comparison  is  not  intended  to  be  a  complete  analysis  of 
the  organization  of  early  and  late  chordates,  but  only  an  indication 
that  the  difference  between  the  two  is  in  the  greater  number  of  diverse 
parts  and  actions  found  in  the  later  type.  At  every  stage  of  the  life- 
cycle  there  are  more  alternative  possible  actions  available  and  better 
methods  for  selecting  the  appropriate  one.  In  other  words  in  higher 
organisms  more  information  passes  through  the  system.  It  was  sug- 
gested in  the  first  chapter  that  this  greater  complexity  of  the  higher 
animals  enables  their  life  to  be  carried  on  under  conditions  that  would 
have  been  impossible  for  the  simpler  ancestors.  The  survey  of  the 
evolution  of  chordates  has  certainly  shown  that  since  the  Cambrian 
the  chordate  organization  has  invaded  situations  very  different  from  the 
sea  surface  in  which  it  probably  arose.  It  would  not  be  profitable  now 
to  recapitulate  all  the  stages  of  this  change — they  have  already  been 
described  throughout  the  book.  If  we  consider  ecological  niches  in 
detail  the  number  of  fresh  situations  invaded  by  vertebrate  life  is 
almost  as  great  as  that  of  the  species  in  the  group.  Among  the  earlier 
changes  were  the  transfer  from  the  sea  surface  to  other  waters  and  to 
the  sea  bottom.  The  entrance  into  fresh  water  must  have  called  into 
play  many  special  mechanisms  of  adjustment.  Development  of  jaws, 
perhaps  350  million  years  ago,  probably  from  the  anterior  branchial 
arches,  gave  the  possibility  not  only  of  eating  new  types  of  food 
(including  fellow  fishes)  but  also  of  performing  simple  acts  of  'handling' 
of  the  environment.  The  heavy  armour  of  the  early  types  was  given 
up  and  the  body  form  was  then  greatly  improved  from  a  hydrodynamic 
point  of  view  and  with  development  of  the  air-bladder  into  a  hydro- 
static organ  the  fishes  achieved  their  full  mastery  of  the  water. 

Meanwhile  other  fishes  left  the  water,  probably  in  the  Devonian 
period,  rather  less  than  300  million  years  ago.  At  first  they  operated 
with  little  modification  of  the  method  of  life  they  had  used  in  the  water, 
but  they  later  developed  all  sorts  of  devices  to  meet  the  new  conditions, 
the  earlier  types  dying  out  as  the  later  developed.  This  process  has 


xxxii.  4        INCREASING  COMPLEXITY  OF  VERTEBRATES  769 

been  going  on  ever  since,  to  produce  the  modern  amphibia,  reptiles, 
birds,  and  mammals,  inhabiting  a  great  variety  of  situations. 

In  the  water  tetrapods  are  found  at  all  levels,  including  great  depths 
and  in  perpetually  dark  caverns.  They  live  in  the  most  varied  situa- 
tions on  the  land  and  also  by  burrowing  beneath  its  surface.  Not  a  few 
are  able  to  move  in  the  air,  some  even  to  feed  there.  It  is  hardly  possible 
to  overestimate  the  great  variety  of  vertebrate  life;  at  each  new  ex- 
amination of  any  phase  one  is  amazed  at  the  extraordinary  number 
of  special  modes  of  life  that  are  adopted  by  variants  of  each  type. 

There  are  no  sure  means  of  telling  the  number  of  types  or  of  indi- 
viduals constituting  the  biomass  that  was  present  in  past  times,  but  it 
is  probable  that  by  means  of  the  above  special  devices  the  vertebrate 
stock  has  increased  and  colonized  new  regions,  though  not  perhaps 
continuously  or  at  a  uniform  rate.  It  is  not  unlikely  that  today  there 
are  more  and  more  varied  vertebrates  than  at  any  previous  period.  It 
has  been  pointed  out  that  the  number  of  species  described  from 
deposits  tends  to  increase  geometrically  with  time  (Caillaux,  1950). 
This  is  not  an  artefact  due  to  poor  preservation. 

Moreover,  as  Lotka  has  pointed  out,  the  total  energy  flux  through 
the  system  has  probably  also  been  enlarged.  It  would  not  be  easy  to 
demonstrate  these  conclusions  rigorously  with  our  present  knowledge : 
it  is  difficult  to  believe  that  they  are  true  of  all  populations.  We  should 
return  from  these  speculations  to  reconsider  the  nature  of  the  evidence 
about  evolutionary  change,  to  discover  the  changes  that  we  are  sure 
have  taken  place  since  the  vertebrate  organization  first  appeared. 

4.  The  variety  of  evidence  of  evolutionary  change 

At  various  points  throughout  the  book  attention  has  been  called  to 
the  conclusions  that  the  evidence  allows  us  to  draw,  and  it  is  important 
to  notice  that  they  vary  considerably  from  group  to  group  within  the 
chordates.  For  example,  we  can  draw  from  morphology  some  con- 
clusions about  the  changes  that  produced  the  original  fish-like  verte- 
brate, but  these  conclusions  are  unsupported  by  fossil  evidence.  The 
fossils  available  for  study  of  evolution  of  the  earliest  gnathostomes  are 
too  few  to  allow  us  a  detailed  view  of  the  change  from  jawless  ostraco- 
derm  to  placoderms  with  jaws,  and  from  these  to  more  modern  fish. 
At  the  other  end  of  the  scale,  there  are  so  many  fossil  elephants'  teeth 
to  be  studied  that  only  an  obscure  picture  of  parallel  lines  of  evolution 
has  emerged.  Again,  in  some  groups,  for  instance  birds,  palaeontology 
is  only  of  limited  help  in  studying  evolutionary  change,  but  nevertheless 
we  have  a  considerable  knowledge  about  the  course  of  evolution  from 


77o  CONCLUSION  xxxn.  4- 

study  of  the  existing  forms,  because  the  birds  are  conspicuous,  well 
known,  and  varied  (p.  522). 

A  proper  appraisal  of  the  nature  of  evolutionary  change  demands  an 
understanding  of  the  fact  that  evidence  about  it  comes  from  very 
different  sources  and  varies  in  different  animal  groups.  We  may  there- 
fore profitably  extract  from  the  results  of  various  parts  of  our  study 
such  simple  propositions  as  are  strictly  justified  by  the  evidence  and 
provide  us  with  a  sure  foundation  of  knowledge  about  the  subject. 

5.  Rate  of  evolutionary  change 

It  has  recently  become  possible  to  consider  several  ways  of  measur- 
ing the  rate  of  evolutionary  change.  Simpson  (1953)  distinguishes 
between  measurement  of  (1)  genetic  rates,  (2)  morphological  rates, 
(3)  taxonomic  rates,  and  we  may  add  as  a  possibility  (4)  rates  of  change 
of  information  flow.  Although  the  first  and  last  of  these  are  biologically 
the  most  instructive,  they  are  impossible  to  measure  on  a  large  scale  or 
in  extinct  populations.  Rates  of  change  of  linear  or  other  dimensions 
can  be  estimated  in  suitable  cases  such  as  horses'  teeth  (p.  738). 
Haldane  suggests  that  changes  should  be  considered  on  a  percentage 
rather  than  an  absolute  basis,  for  instance  by  considering  the  time 
needed  for  a  unit  increase  in  the  natural  logarithm  of  a  variate  or  one 
standard  deviation.  Change  of  one  s.d.  per  million  years  might  be 
called  a  'darwin';  the  horse  tooth  change  (p.  737)  being  then  at  a 
rate  of  40  millidarwins. 

The  only  easily  available  quantitative  data  about  large  groups  of 
animals  are  the  number  of  taxonomic  units  (species,  genera,  &c.)  into 
which  they  are  divided.  If  it  were  true  that  differences  between,  say, 
genera,  meant  the  same  when  used  by  different  authors  and  in  different 
animal  groups  then  we  could  measure  rates  of  evolutionary  change  by 
the  numbers  appearing  at  each  taxonomic  level.  The  condition  is 
unfortunately  not  strictly  fulfilled  and  there  are  inevitably  examples  of 
what  has  been  called  'monographic  evolution'.  Nevertheless,  the  defini- 
tion of  a  difference  as  of,  say,  'generic'  or  'ordinal'  rank  by  a  competent 
worker  is  in  effect  a  kind  of  measure  of  general  morphological  difference. 
Indeed  in  view  of  the  subtle  efficiency  of  the  human  receptors  and 
brain  for  this  sort  of  comparison,  the  measure  is  perhaps  as  accurate 
as  could  be  expected  to  result  from  any  artificial  'morphometer' 
that  can  at  present  be  imagined. 

Using  taxonomic  criteria  it  is  clear  that  rates  of  evolution  vary  in 
different  groups.  Thus  the  living  prosimians  have  changed  little  since 
the  Eocene  while  their  descendants  have  gone  on  to  produce  the  whole 


xxxii.  6  RATE    OF    CHANGE  771 

range  of  modern  primates.  The  rate  of  evolution  of  horses  and  chalico- 
theres  has  been  about  the  same  (0-13  genera  per  million  years)  and 
much  faster  than  that  of  ammonites  (0-05),  assuming  that  'genus'  has 
a  similar  meaning  in  the  two  cases. 

Using  taxonomic  rates  it  has  been  shown  that  many  vertebrate 
major  groups  seem  to  evolve  fast  at  their  'first  appearance'.  This  rapid 
evolution  (tachytely)  is  presumably  the  result  of  moving  into  a  new 
adaptive  zone,  which  we  notice  ex  post  facto  as  the  beginning  of  a 
higher  taxonomic  group.  The  chances  of  finding  these  transition  types 
as  fossils  may  be  unduly  small  if  evolution  is  rapid  and  especially  if  it 
occurs  in  a  small  population  (or  a  large  one  divided  into  small  units; 

5.  Wright).  Claims  to  have  found  the  'centre  of  origin'  of  a  major 
group  must  therefore  be  looked  upon  with  suspicion.  In  any  case, 
parallel  evolution  may  carry  several  lines  over  the  arbitrary  line  we  use 
to  mark  a  higher  taxonomic  order;  at  least  five  lines  of  therapsid 
reptiles  crossed  to  become  mammals  (p.  545). 

This  discussion  may  make  it  seem  unreal  to  speak  of  'origins'  of 
higher  taxonomic  groups.  Indeed,  it  is  probably  misleading  to  look 
for  major  'branches'  in  what  must  be  a  multiple  evolutionary  'bush'. 
Nevertheless  there  is  evidence  that  rate  of  change  is  not  constant. 
Apart  from  such  examples  as  those  already  discussed,  there  are  many 
others.  Bats,  as  Simpson  points  out,  have  certainly  evolved  more 
slowly  since  they  first  got  wings  and  'broke  through'  to  a  new  en- 
vironment than  in  the  period  of  that  change  itself. 

6.  Vertebrates  that  have  evolved  slowly 

We  may  accept  then  the  concept  of  bursts  of  rapid  evolution, 
followed  by  slower  change.  In  many  lines  after  the  rapid  change  there 
is  a  period  over  which  many  genera  become  extinct.  However,  a  few 
linger  on  for  times  longer  than  would  be  expected  (bradytely).  This 
general  pattern  can  be  seen  for  fishes  in  Fig.  5 13^.  This  phenomenon 
of  bradytely  produces  phylogenetic  relicts,  of  which  there  seem  to  be  so 
many  that  some  general  explanation  of  them  is  desirable.  Neoceratodus 
has  a  good  claim  to  be  considered  the  'oldest'  living  vertebrate;  it  is 
very  similar  to  fossils  found  in  the  Triassic,  nearly  200  million  years 
ago.  Even  in  this  case,  however,  there  have  been  slight  changes  and 
the  Triassic  form  is  placed  in  a  distinct  genus  *Ceratodiis.  Latimeria 
provides  us  with  an  example  of  survival  with  little  change  for  nearly 
100  million  years,  as  well  as  the  humbling  thought  that  no  fossil 
relatives  are  known  throughout  that  time.  Heterodontus,  the  Port 
Jackson  shark,  is  another  very  ancient  fish;  it  is  closely  similar  to 


772 


CONCLUSION 


xxxii.  6 


fossils  found  in  the  Triassic;  indeed,  all  sharks  are  quite  like  their 
Palaeozoic  ancestors. 

Sphenodon  has  changed  little  since  Permian  times  and  hardly  at  all 
since  the  Jurassic,  perhaps  140  million  years  ago.  Among  mammals, 


FISHES 


FIRST    APPEARANCES 
PER    MILLION    YEARS 


GENERA 
•-----•  FAMILIES 
o        a   ORDERS 


C.    F.    O. 
16  1.8.36 


-  16  1.6.32 


S  1     D    '     C      '  Pi    T    '   J 
Geological    Periods 

Fig.  513a.  Graphs  showing  the  first  appearances  per  million  years  of  known  orders, 

families,  and  genera  of  the  four  classes  of  'fishes'.  O.  orders;  F.  families;  and  G. 

genera  per  million  years.  Time  scale  is  in  geological  periods.  (After  Simpson.) 

the  opossums  and  hedgehogs  are  quite  similar  to  those  of  Cretaceous 
times,  nearly  100  million  years  ago,  and  there  are  several  mammals 
that  have  survived  with  little  change  for  the  50  million  years  since  the 
Eocene,  for  instance  dogs,  pigs,  and  lemurs.  In  none  of  these,  however, 
has  a  form  survived  absolutely  without  change ;  they  are  examples  of 
the  persistence  of  a  type  of  organization  rather  than  of  superficial 
details. 


xxxir.  6  SLOW    RATES    OF    EVOLUTION  773 

It  is  most  interesting  to  consider  possible  reasons  for  these  very 
slowly  evolving  (bradytelic)  populations  (Simpson,  1953).  (1)  It 
might  be  low  mutation  rate  or  low  variability,  but  there  is  no  evidence 
that  opossums  (say)  are  less  variable  than  other  mammals  and  indeed 
they  have  undergone  much  speciation.  (2)  It  is  often  implied  that 
survival  is  assisted  by  some  special  habit,  such  as  being  nocturnal  or 
abyssal,  but  others  with  the  same  habits  evolve  fast.  (3)  Survival  some- 
times seems  to  be  assisted  by  isolation  (e.g.  lemurs)  but  there  is  no 
evidence  that  this  is  necessarily  a  factor  (Latimeria).  (4)  Low  rate  of 
evolutionary  change  is  not  a  function  of  'primitive'  organization  as 
such,  indeed  as  we  have  seen  the  reverse  is  true.  In  any  case  Sphenodon 
and  Crocodylm  were  not  especially  'primitive'  when  they  stopped  evol- 
ving in  the  Triassic  and  Cretaceous.  (5)  Long  survival  must  depend 
upon  some  special  relationship  between  the  genetical  and  information- 
carrying  powers  of  the  species,  the  risks  imposed  by  the  environment, 
and  the  stability  of  the  latter.  (6)  If  the  adaptive  zone  is  a  narrow  one 
it  must  be  stable  and  persist.  This  would  seem  to  be  unlikely  in  very 
'difficult'  habitats  such  as  deserts  or  impermanent  ones  (salt  lakes)  or 
variable  ones,  such  as  Alps.  (7)  Long  survival  is  perhaps  more  to  be 
expected  in  a  broad  adaptive  zone  such  as  the  ocean  or  shore,  lowland 
rivers  or  forest  belts,  especially  in  the  tropics.  Such  environments 
present,  however,  many  niches  that  can  be  considered  as  'corridors', 
leading  to  diversification,  and  it  is  surprising  that  forms  nevertheless 
remain  stable  in  them.  Thus  opossum-like  creatures  gave  rise  to 
various  offshoots  in  South  America  but  themselves  changed  little.  (8) 
Bradytelic  populations  must  be  genetically  so  integrated  that  any  devia- 
tion is  subject  to  counter-selection  (though  in  that  case  it  is  hard  to  see 
how  the  offshoots  have  arisen).  (9)  Simpson  concludes  that  these  brady- 
telic organisms  'have  run  the  whole  repertory  of  baffles  and  .  .  . 
persist  indefinitely'.  Most  organisms  are  turned  off  into  one  or  other 
of  the  corridors  presented  by  the  environment;  when  a  group  has  met 
and  passed  them  all  it  persists. 

The  discussion  of  organisms  that  have  evolved  only  very  slowly  is 
thus  a  stimulus  to  considering  the  whole  balance  of  factors  by  which 
a  population  of  organisms  maintains  its  homeostasis.  Evidently  there 
are  some  circumstances  in  which  it  can  do  this  with  little  genetic 
change.  In  the  great  majority,  however,  change  of  the  genes  and  hence 
of  the  structure  and  physiology  is  a  part  of  the  very  mechanism  by 
which  the  living  system  continues  to  survive  in  spite  of  changes 
around  it. 


774 


CONCLUSION 


xxxn.  7- 


7.  Varying  rates  of  evolutionary  changes 

Although  gradual  modification  of  living  organization  is  almost  uni- 
versal it  is  clear  that  the  change  is  often  extremely  slow.  The  transition 
from  an  osteolepid  fish,  say  *Sauripterus}  through  stages  like  *Eogyrinns 
to  *Seymonria  took  nearly  90  million  years.  The  change  of  the  horses 
from  *Hyracotheruim  to  Equus  is  not  very  profound,  considering  that 
it  took  at  least  50  million  years.  Probably  few  populations  stay  the 
same  for  long  periods,  but  there  may  be  marked  differences  in  rate 
of  change  in  groups  not  otherwise  dissimilar.  Thus  some  lines  of 

"FISHES"  FIRST  AND  LAST  APPEARANCES 
ORDERS  PER  MILLION  YEARS 


TETRAPODS 


S'D'C'P'T'J'C 

Geological    Periods 

Fig.  513&.  Graphs  showing  first  and  last  appearances  of  orders  per 
million  years  in  'fishes'  and  in  tetrapods.  (After  Simpson.) 

elephant  shortened  the  lower  jaw  earlier  and  faster  than  others  (p.  716). 
Whereas  the  majority  of  elephant  populations  changed  greatly  between 
the  Oligocene  and  the  Pliocene,  the  deinotheres  remained  almost  the 
same  throughout  this  long  period. 

Taxonomic  methods  show  that  for  each  class  of  vertebrates  the  rate 
of  diversification  increases  rapidly  shortly  after  the  origin  of  a  class 
and  thereafter  falls  though  sometimes  showing  a  second  rise  (Fig.  5 1 30). 
The  maximum  rate  of  formation  of  new  orders  precedes  that  of  forma- 
tion of  new  genera  by  25-50  million  years  in  each  case.  Rates  of  first 
and  last  appearances  follow  each  other  rather  closely  (Fig.  513&)  sug- 
gesting continuous  replacement  in  the  populations. 

8.  Vertebrates  that  have  disappeared 

Set  against  the  few  examples  of  relative  constancy  of  organization 
there  are  the  wholesale  extinctions  that  we  deduce  from  study  of  the 
rocks.  The  ostracoderms,  osteolepids,  stegocephalians,  dinosaurs,  and 
pterodactyls  (to  mention  only  a  few)  became  completely  extinct  or 


xxxii.  9  REPLACEMENT  775 

changed  into  some  very  different  type  of  animal.  Looking  at  any  of 
the  evolutionary  trees  in  this  book,  which  represent,  as  it  were,  the 
summary  of  the  evidence  about  the  populations,  one  notices  at  once 
how  frequently  types  common  in  earlier  periods  become  extinct  or  are 
replaced  by  their  own  descendants.  Occasionally  some  line  is  recorded 
as  continuing  over  a  long  period,  but  the  common  picture  is  of  change, 
each  type  disappearing  after  a  span  of  years. 

9.  Successive  replacement  among  aquatic  vertebrates 

Does  the  examination  of  the  sequences  of  types  enable  us  to  say 
anything  about  the  nature  of  these  evolutionary  changes?  Can  we 
record  any  sense  in  which  it  represents  a  'progress'  or  'advance'  ?  One 
striking  feature  that  we  have  noticed  is  that  often  one  type  of  organism 
seems  to  replace  another.  There  is  always  a  difficulty  in  establishing 
that  this  has  occurred,  because  the  fossil  record  does  not  leave  us 
sufficient  information  to  show  for  certain  that  the  two  types  occupied 
identical  'niches'.  However,  if  we  take  broad  'habitats',  and  particu- 
larly those  that  change  relatively  little,  such  as  the  waters,  we  cannot 
but  be  impressed  with  the  succession  of  tenants  that  appears,  each 
replacing  the  one  before  (p.  237).  Thus,  among  fish-like  vertebrates 
we  can  recognize  ostracoderms,  placoderms,  crossopterygians,  palaeo- 
niscids,  holosteans,  and  teleosteans,  each  almost  completely  replacing 
the  one  before. 

Again,  there  has  been  an  astonishing  series  of  tetrapods  returning 
from  the  land  to  water,  developing  characters  suitable  for  aquatic  life 
and  then  becoming  extinct,  apparently  displaced  by  later  migrants, 
also  returning  from  the  land.  To  name  only  a  few  of  these  returners 
we  have  among  amphibians  the  phyllospondyls,  lepospondyls,  bran- 
chiosaurs,  and  some  urodeles;  among  reptiles  the  phytosaurs,  croco- 
diles, plesiosaurs,  ichthyosaurs,  mesosaurs,  mosasaurs,  aigialosaurs, 
dolichosaurs,  and  snakes.  Finally  of  the  mammals  there  are  the 
basilosaurs,  modern  whales,  seals,  and  sea-cows,  as  well  as  some  less 
completely  aquatic  types. 

However  much  we  make  allowance  for  the  fact  that  the  sea  itself 
may  be  changing,  it  is  difficult  not  to  find  in  these  facts  a  suggestion 
that  the  later  types  are  replacing  the  earlier  by  their  greater  'efficiency'. 
These  returned  aquatics  are  especially  interesting  because  each  type 
when  it  first  re-enters  the  water  seems  to  be  not  very  well  suited  to 
that  medium — because  of  its  shape  for  instance — and  would  therefore 
be  expected  to  be  at  a  disadvantage  in  relation  to  the  'streamlined' 
creatures  that  were  already  there. 


776  CONCLUSION  xxxn.  10- 

10.  Successive  replacement  among  land  vertebrates 

It  is  equally  easy  to  trace  out  successions  of  types  occupying  habitats 
on  land,  though  here  it  is  even  more  difficult  to  be  sure  that  the  succes- 
sive animals  are  occupying  identical  niches.  There  has  been  a  long 
series  of  large  land  herbivores,  including  the  labyrinthodonts,  pareia- 
saurs,  herbivorous  synapsids,  various  dinosaurs,  multituberculates, 
condylarths,  dinocerates,  pantodonts,  brontotheres,  horses,  pigs, 
rhinoceroses,  elephants,  and  artiodactyls.  Clearly  not  all  of  these  lived 
in  similar  surroundings  (and  there  were,  of  course,  other  herbivores), 
but  the  succession  is  impressive.  As  with  the  aquatic  animals  we  have 
the  curious  phenomenon  that  the  earlier  members  of  each  group  seem 
to  be  clumsy  creatures,  no  better  fitted  for  their  life  than  those  they 
are  replacing.  The  early  mammalian  herbivores,  with  their  large  limbs 
and  small  brains,  do  not  seem  greatly  superior  to  the  stegosaurs  and 
ceratopsians  of  the  Cretaceous.  It  is,  of  course,  exceedingly  difficult  to 
know  enough  to  settle  such  questions,  for  instance  to  assess  the  value 
of  warm-bloodedness. 

If  we  look  at  other  ecological  niches  we  see  the  same  picture  of  con- 
tinued replacement.  Thus  there  has  been  a  succession  of  land  carni- 
vores, first  synapsid  reptiles,  then  archosaurian  reptiles,  followed  in 
the  Tertiary  period  by  the  creodonts,  which  were  replaced  by  modern 
carnivores  and  carnivorous  birds. 

1 1 .  Is  successive  replacement  due  to  climatic  change  ? 

A  very  careful  analysis  is  needed  before  we  can  venture  to  say  much 
about  the  nature  of  this  successive  replacement  of  types.  We  have 
several  times  noticed  how  easy  and  dangerous  it  is  to  find  superficial 
'causes'  for  evolutionary  change.  The  periods  of  time  involved  are  so 
long  that  a  stern  discipline  is  needed  to  prevent  oneself  from  using 
analogies  that  are  really  only  applicable  to  much  shorter  periods 
(p.  572).  We  have  to  try  to  imagine  vast  communities  of  animals  of 
various  sorts,  interacting  with  each  other  to  produce  fluctuating  popu- 
lations, all  living  in  climatic  conditions  that  vary  from  year  to  year  and 
also,  very  slowly,  through  the  centuries.  Only  if  we  hold  such  a  picture 
in  mind  can  we  begin  to  answer  questions  about  whether  the  stimulus 
to  evolutionary  change  comes  from  the  changing  environment. 

It  is  now  very  doubtful  whether  there  have  been  periods  of  'revolu- 
tionary' geological  change  (p.  16).  Local  rises  and  falls  and  foldings 
of  the  crust  have  certainly  occurred  and  must  have  influenced  the 
fauna.  Even  so  it  is  not  certain  that  the  new  types  appearing  after  such 
events,  originated  during  them.  They  may  well  have  evolved  elsewhere 


xxxii.  i2  INFLUENCE    OF   CLIMATIC    CHANGE  777 

and  migrated  into  the  area  to  meet  the  new  conditions  left  after  the 
'revolution'. 

In  the  past  it  has  been  usual  to  try  to  find  rather  simple  correlations 
of  this  sort.  We  are  told  that  emergence  of  land  vertebrates  was  due 
to  drying  up  of  large  areas  of  sea  during  the  Devonian,  that  the 
mammals  emerged  because  of  the  colder  conditions  at  the  end  of  the 
Cretaceous,  or  the  horses  because  of  the  appearance  of  wide  plains  in 
the  Miocene.  For  the  reasons  already  given  we  must  regard  such 
suggestions  with  suspicion,  especially  when  they  relate  to  conditions 
extending  over  a  long  period  of  time.  There  are,  however,  certainly 
some  valid  correlations  of  climatic  and  faunistic  changes,  especially  in 
relatively  recent  periods.  Thus  the  finding  in  Britain  of  woolly  mam- 
moths, cave  bears,  and  other  animals  to  be  expected  in  a  cold  climate 
may  reasonably  be  associated  with  advances  of  the  ice  cap  (p.  572). 
Indeed  we  have  evidence  of  the  climatic  change  independent  of  the 
animal  remains.  No  doubt  change  of  climate  has  been  one  of  the 
variable  factors  that  has  led  to  the  continual  change  of  vertebrate  life, 
which  we  are  seeking  to  understand.  It  is  probable,  however,  that 
animal  populations  change  their  character  independently  of  any  climatic 
change.  It  is  not  easy  to  find  critical  situations  to  test  this  belief,  but 
examples  such  as  the  faunas  of  the  Galapagos  and  other  islands  (p.  524) 
suggest  that  diversity  can  arise  as  animals  explore  the  possibilities  of 
their  environment,  especially  if  there  are  factors  that  divide  up  a 
population  into  a  number  of  nearly  isolated  units. 

Often  a  population  undergoes  an  'adaptive  radiation',  branching  out 
to  form  a  number  of  types,  each  suited  for  a  particular  environment  or 
niche.  The  phenomenon  is  so  widespread  that  it  suggests  a  type  of 
evolution  common  at  least  to  many  populations.  The  conception  of 
adaptive  radiation  originally  put  forward  by  Osborn  was  that  each 
'stem  form'  (of  mammals)  diverged  in  five  directions,  giving  cursorial, 
fossorial,  scansorial,  volant,  and  aquatic  types.  These  are,  of  course, 
only  particular  aspects  of  the  radiation.  When  we  examine,  say,  the 
Galapagos  finches,  or  the  marsupials,  we  obtain  the  strong  impression 
that  members  of  a  particular  animal  population  seek  out  a  variety  of 
new  habitats,  and  gradually  become  suited  for  them,  until  a  range  of 
new  types  is  thus  produced.  This  is  the  history  of  each  of  the  groups  of 
vertebrates,  they  radiate  into  many  different  types  and  then  disappear. 

12.  Convergent  and  parallel  evolution 

A  remarkable  fact  that  has  appeared  many  times  in  our  survey  is  that 
during  these  radiations  similar  features  repeatedly  appear  in  distinct 


778 


CONCLUSION 


lines.  It  is  as  if  the  vertebrate  organization  produced  time  after  time 
slightly  different  variations  on  a  series  of  themes.  Thus  animals  that 
feed  on  fishes  acquire  long  jaws  and  numerous  teeth.  We  have  examples 
of  these  characteristics  among  the  fishes  themselves  (garpike,  Belone) 


Fig.  514.  Skeleton  of  the  hand  in  various  mole-like  mammals. 

a,    Talpa;   b,   Chrysochloris;   c,   Notoryctes  (palmar  view);   d,   dorsal 

view  of  the  same.  r.  radius;  rs.  radial  sesamoid;  u.  ulna.  (From  Lull, 

Organic  Evolution,  copyright  1917,  1929  by  The  Macmillan  Company 

and  used  with  their  permission.) 

and  in  the  crocodiles,  phytosaurs,  ichthyosaurs,  plesiosaurs,  birds,  and 
mammals.  Perhaps  even  more  remarkable  are  the  'duck-bills'  of 
animals  that  sift  small  invertebrates  from  mud.  There  is  a  distinct 
similarity  in  the  structures  used  for  this  purpose  by  Polyodon,  the 
ducks  themselves,  and  the  platypus.  One  could  continue  with  endless 
examples  of  the  same  sort,  for  instance,  the  large  mouth  of  insect- 
eating  animals — the  frogs,  swallows,  swifts,  and  bats.  The  five  sorts 
of  ant-eater  found  among  mammals  provide  another  remarkable 
example  of  this  'convergence' ;  all  have  an  elongated  snout,  long  sticky 


xxxn.  13  PARALLEL    EVOLUTION  779 

tongue,  large  salivary  glands,  and  other  features.  The  hands  of  the 
moles  show  how  a  similar  result  may  be  arrived  at  by  various  slightly 
differing  means  (Fig.  514). 

There  can  be  no  doubt  that  vertebrates  adopting  a  given  mode  of 
life  tend  to  acquire  a  particular  structure.  There  is  also  evidence  of 
what  we  might  call  the  converse,  namely  that  animals  with  a  particular 
form  tend  to  develop  in  certain  directions.  This  is  one  of  the  forms  of 
the  situation  described  by  some  as  'pre-adaptation'.  The  elasmobranch 
fishes  maintain  equilibrium  in  the  horizontal  plane  by  a  heterocercal 
tail,  driving  the  head  downwards,  and  horizontal  pectoral  fins  and 
flattened  front  end  of  the  body,  having  the  opposite  effect  (p.  140). 
From  this  type  of  organization  creatures  of  ray-like  type  have  several 
times  developed,  flattened  dorso-ventrally  and  obtaining  their  pro- 
pulsive thrust  from  the  pectoral  fins.  Conversely  among  teleosts, 
where  the  compression  is  in  a  transverse  plane,  the  bottom-living 
types  are  flattened  laterally,  as  in  the  sole  or  plaice.  Where  the  swim- 
bladder  has  been  lost,  however,  there  may  be  dorso-ventral  flattening. 
The  more  closely  we  examine  the  evolution  of  populations  the 
more  signs  of  these  similar  tendencies  in  evolution  appear.  Parallel 
evolution  is  so  common  that  it  is  almost  a  rule  that  detailed  study 
of  any  group  produces  a  confused  taxonomy.  Investigators  are  un- 
able to  distinguish  populations  that  are  parallel  new  developments 
from  those  truly  descended  from  each  other.  Examples  we  have 
noticed  from  study  of  modern  populations  are  the  various  types  of 
tree-living  and  burrowing  anurans  (p.  366).  The  'tree-frog'  and 
'burrowing'  conditions  have  been  evolved  both  from  true  frogs  and 
from  toads,  probably  several  times  in  each  case.  Again,  the  habit  of 
burrowing  underground,  with  loss  of  the  limbs,  has  appeared  in  a 
number  of  squamate  reptiles;  the  slow- worms,  amphisbaenas,  and 
subterranean  skinks  are  certainly  distinct  lines,  possibly  each  contains 
more  than  one,  and  the  snakes  are  probably  derived  from  another 
group  that  went  underground. 

13.  Some  tendencies  in  vertebrate  evolution 

These  are  only  a  few  scattered  examples,  but  they  already  suggest 
that  the  evolutionary  changes  of  vertebrate  populations  follow  certain 
patterns.  Although  in  the  history  of  each  type  there  is  no  doubt  that 
much  is  unique,  yet  most  types  tend  to  follow  along  certain  lines, 
according  to  the  situations  they  have  reached.  It  is  not  possible  yet 
for  the  systematic  morphologist  to  make  any  complete  classification 
or  analysis  of  these  tendencies.  He  can  only  point  to  a  few  of  them, 


780  CONCLUSION  xxxn.  13- 

already  so  familiar  as  to  be  almost  banal.  Thus  vertebrates  that  move  in 
the  water  tend  to  have  the  fish  form,  with  streamlined  body,  vertebrae 
with  flat  articulations  and  paddle-like  limbs.  We  are  so  used  to  this 
that  perhaps  its  interest  is  often  overlooked,  especially  the  fact  that  the 
pectoral  limb  may  revert  from  an  elongated  pentadactyl  structure  to  a 
paddle,  sometimes  with  increased  number  of  digits  and  of  phalanges. 
Evidently  this  form  of  limb  is  suitable  for  the  uses  demanded  in  the 
water  and  tends  to  be  developed  again  when  needed. 

Similar  examples  that  can  be  called  in  a  sense  a  reversal  of  evolution 
are  interesting  not  only  from  genetic  and  embryological  points  of  view, 
but  especially  because  they  show  strikingly  that  under  given  conditions 
vertebrate  populations  tend  to  react  alike,  giving  us  the  possibility 
of  developing  a  reasonable  science  of  morphology.  Thus  vertebrates 
that  take  to  the  air  develop  light  and  thin  bones,  those  that  burrow 
underground  often  lose  their  limbs  (but  among  mammals  these  are 
often  the  main  digging  agents).  Similar  general  evolutionary  principles 
could  probably  be  developed  for  each  organ  system.  Thus  the  eyes 
develop  cone-like  structures  in  diurnal,  rod-like  in  nocturnal  species, 
and  they  become  buried  under  the  skin  or  lost  altogether  in  popula- 
tions that  live  in  the  dark. 

14.  Evolution  of  the  whole  organization 

For  an  analysis  of  the  nature  of  the  changes  occurring  during  evolu- 
tion to  be  satisfactory  it  would  have  to  deal  not  only  with  the  evolution 
of  isolated  parts  but  with  that  of  the  whole  organization  of  the  activities 
of  the  population.  In  our  present  ignorance  of  the  morphogenetic 
processes  it  is  very  difficult  for  us  to  provide  descriptions  of  the  nature 
of  the  whole  organization  that  will  be  satisfactory.  We  know  enough  of 
the  underlying  hereditary  material  and  the  way  it  produces  the  chemi- 
cal action  systems  and  organs  of  the  body  to  be  able  to  say  that  there 
are  some  genetic  factors  that  affect  almost  the  entire  organization, 
but  also  that  sometimes  individual  parts  change  separately.  Changes 
in  the  activities  inherited  through  the  egg  and  sperm  may  affect  a  single 
process,  such  as  the  deposition  of  pigment  in  the  skin,  but  usually  they 
influence  a  wide  range  of  activities  and  the  form  of  many  organs. 
Conversely  each  gene  is  usually  influenced  in  its  action  by  several, 
perhaps  many,  others,  and  the  consequent  wide  range  of  expression 
of  each  character  provides  the  basis  of  variability  on  which  natural 
selection  can  act. 

There  are  indications  that  during  evolution  sets  of  characters  tend  to 
evolve  together.  For  instance,  the  various  features  of  the  mammal-like 


xxxii.  is  EVOLUTION    OF   ORGANIZATION  781 

organization  appeared  several  times  during  the  Mesozoic — the  teeth, 
jaw  and  skull  bones,  and  limbs  apparently  evolving  together.  On  the 
other  hand  differing  combinations  are  also  undoubtedly  possible;  the 
notoungulate  *Thoatherium  developed  the  limbs  but  not  the  teeth  of 
a  horse;  * Australopithecus  had  the  legs  but  not  the  brain  of  a  man. 

Unfortunately  we  have  no  very  satisfactory  techniques  for  describ- 
ing the  organization  and  its  changes.  All  populations  are  homeostatic 
self-reproducing  systems.  They  are  able  to  remain  alive  by  selecting 
from  their  repertoire  of  possible  actions  those  that  ensure  survival. 
This  selection  may  be  done  either  between  the  genes  ('natural  selection') 
or  between  possible  courses  of  morphogenesis  ('functional  adaptation') 
or  between  possible  actions  of  the  neuromuscular  system  ('behaviour'). 
We  need  means  for  measuring  the  information  flow  involved  in  these 
selections  and  the  amount  that  is  stored  in  the  memory  system  of  the 
species. 

Change  in  the  genetic  system  (evolution)  is  one  of  the  means  adop- 
ted to  ensure  homeostasis,  and  evolution  is  a  feature  that  is  essential 
for  prolonged  maintenance  of  the  organization.  If  storage  powers  are 
effective  and  adequate  such  a  system,  as  it  receives  information,  must 
presumably  develop  a  widening  repertoire  of  responses,  both  mor- 
phogenetic  and  behavioural.  The  appearance  of  increasing  complexity 
as  organisms  become  as  we  say  'more  highly  evolved'  is  a  measure 
of  the  extent  to  which  they  have  found  ways  of  encoding  new  in- 
formation about  the  environment  and  so  channeling  it  as  to  produce 
responses  that  keep  the  species  alive  in  the  face  of  new  risks.  The  higher 
organisms  are  thus  those  that  pass  the  greater  amounts  of  information, 
using  more  complex  codes.  Unfortunately  we  have  little  quantitative 
information  about  genetic,  morphogenetic,  or  neural  codes  to  support 
such  an  assertion. 

15.  Summary  of  evidence  about  evolution  of  vertebrates 

The  evidence  about  the  history  of  vertebrates  may  be  said,  then, 
to  show  us  the  following  facts:  (1)  In  all  or  nearly  all  populations 
the  organization  of  life-processes  changes,  though  often  only  slowly. 
(2)  The  later  types  of  organization  usually  replace  the  earlier  in  any 
one  environment.  (3)  Evolutionary  change  is  not  always  obviously 
associated  with  environmental  change,  though  it  may  be  so.  (4)  When 
different  populations  adopt  the  same  habit  of  life  they  often  develop 
similar  but  not  identical  organizations.  Probably  no  population  is 
stable  either  in  numbers  or  in  genetic  or  phenotypic  characteristics. 
The  evidence  suggests  that  in  most  species  evolution  is  going  on  now 


782  CONCLUSION  xxxn.  15- 

and  all  the  time.  The  number  of  animals  in  a  population  is  seldom  if 
ever  constant.  Probably  the  genetic  and  phenotypic  characters  of  the 
members  also  vary  with  time,  perhaps  actually  in  correlation  with  the 
fluctuations  of  number. 

We  have,  therefore,  a  picture  of  an  animal  species  as  a  set  of  indi- 
viduals that  are  similar  but  not  all  identical,  interbreeding  with  each 
other,  though  perhaps  with  degrees  of  difficulty  that  vary  with  genetical 
and  geographical  differences  (themselves  probably  correlated).  The 
characteristic  features  of  such  a  population  are  given,  as  we  have  seen 
in  Chapter  I,  by  its  power  and  ability  to  produce  later  populations, 
both  like  and  unlike  itself.  Unfortunately,  we  know  little  about  these 
powers  in  vertebrates,  or  indeed  other  organisms;  the  present  study 
has  not  dealt  with  them  fully.  They  are  presumably  influenced  by  such 
variables  as  the  frequency  of  reproduction,  number  of  offspring  pro- 
duced, and  the  viability  of  these  in  the  face  of  various  climatic  and 
biotic  factors,  availability  of  food,  persistence  of  predators,  and  so  on. 
It  has  been  pointed  out  by  Haldane  that  these  factors  may  lead  to  the 
development  of  various  distinct  sorts  of  organization.  If  the  death- 
rate  is  low  the  productivity  will  also  be  low  and  those  members  of  the 
population  will  be  selected  whose  characters  allow  for  a  long  life — for 
example,  hypsodont  molars  will  develop.  In  populations  with  a  high 
death-rate  to  predators  or  disease,  however,  selection  will  choose  those 
individuals  with  high  productivity  and  rapid  development,  incidentally 
perhaps  also  allowing  greater  variability,  by  which  the  predators  and 
pathogens  may  be  avoided. 

There  must  be  a  complicated  relationship  between  such  factors  as 
the  frequency  of  reproduction  and  numbers  of  young,  rate  of  growth, 
time  of  maturity,  size,  likelihood  of  death  from  predators  and  patho- 
gens, capacity  to  'adapt'  during  the  lifetime  and  especially  to  store 
information  in  the  nervous  system.  Members  of  species  that  breed  fast 
usually  also  grow  fast,  learn  little,  and  are  killed  before  they  grow  old. 
Where  there  is  a  brain  with  a  large  memory  it  usually  directs  a  massive 
individual  and  keeps  it  alive  for  a  long  time. 

Evidently  the  particular  characteristics  of  a  population  (including 
its  productivity)  will  depend  on  the  influences  to  which  it  is  subjected. 
Many  of  these  variables  act  with  an  intensity  that  depends  on  the 
activity  of  the  adult  organisms  and  the  energy  and  ingenuity  with 
which  these  find  situations  suitable  for  the  life  of  themselves  and  their 
offspring.  Since  this  adult  activity  is  itself  influenced  by  hereditary  and 
by  environmental  factors  it  is  clear  that  the  productivity  and  increase 
of  a  population  depend  on  a  very  complicated  system  of  inter-connected 


xxxii.  16  INFLUENCES    IN    EVOLUTION  783 

variables.  J.  B.  S.  Haldane,  R.  A.  Fisher,  Sewall  Wright,  and  others 
have  made  some  progress  towards  analysing  this  situation  into  its 
elements  by  mathematical  reasoning,  but  we  have  at  present  estimates 
for  only  few  of  the  variables  involved  and  no  approach  to  an  exact 
solution  is  possible. 

16.  Conservative  and  radical  influences  in  evolution 

In  such  a  system  we  have  factors  that  tend  to  keep  the  population 
the  same  and  others  that  tend  to  make  it  vary;  according  to  the  pre- 
ponderance of  one  or  the  other  the  characters  of  the  populations  will 
either  stay  steady  about  a  mean  or  tend  continually  to  change,  that  is 
to  say,  to  evolve.  We  cannot  make  any  very  precise  list  of  the  factors  in 
the  two  classes.  Those  tending  to  reduce  evolutionary  change  presum- 
ably include  (1)  The  copying  or  reproductive  tendency  that  makes  like 
produce  like.  Here  we  may  include  the  restraints  imposed  by  the  fact 
that  development  is  a  highly  integrated  process,  so  that  any  wide 
departures  from  normality  are  liable  to  interfere  with  it.  (2)  Anything 
that   reduces  the   productivity   in   terms   of  number   of  offspring. 

(3)  Prevalence  of  predators,  if  these  act  so  as  to  prohibit  minor  devia- 
tions from  the  previous  mode  of  life.  (4)  Absence  of  geographical 
barriers.  (5)  Existence  of  stable  external  climatic  and  other  physical 
factors.  (6)  Characteristics  within  the  population  tending  to  keep  the 
animals  in  their  existing  conditions,  rather  than  to  seek  new  ones; 
'adventurousness'  is  essential  if  the  individuals  are  to  enter  new  con- 
ditions; it  corresponds  to  the  adaptations  for  dispersal  that  are  found 
among  plants  (Salisbury,  1942). 

The  contrary  circumstances,  those  that  encourage  evolutionary  de- 
velopment, are  presumably  (1)  High  rate  of  mutation,  that  is  to  say, 
failure  of  the  tendency  to  copy.  Spurway  has  pointed  out  that  the 
extent  to  which  change  in  the  hereditary  and  developmental  pattern 
can  be  varied  probably  differs  in  different  populations.  In  some  almost 
any  change  is  lethal  and  the  population  appears  immutable,  whereas 
other  organizations  can  stand  considerable  variations,  allowing  the 
possibility  of  rapid  evolution.  (2)  High  productivity,  if  it  leads  to  high 
intra-specific  competition  and  hence  pressure  to  find  new  conditions 
for  life.  (3)  Absence  of  predators,  if  this  makes  new  adventures  possible. 

(4)  Presence  of  geographical  barriers,  which  allow  separation  into 
various  races  that  do  not  interbreed  (or  only  seldom  do  so)  and  hence 
become  more  and  more  distinct.  (5)  Change  in  external  conditions. 
(6)  Presence  of  a  high  power  of  adaptability  and  'adventurousness'  in 
the  various  action  systems  of  the  animals.  (7)  Haldane  has  suggested 


784  CONCLUSION  xxxii.  16- 

that  the  influence  of  pathogens  also  puts  a  premium  on  variation.  The 
disease  organism,  being  small,  can  usually  evolve  more  rapidly  than 
the  host,  and  it  is  therefore  an  advantage  for  a  member  of  the  host 
population  to  be  different  from  the  majority,  to  which  the  pathogen  is 
adapted. 

During  the  present  study  there  has  been  little  progress  towards 
demonstrating  that  these  are  the  factors  influencing  evolution,  though 
there  are  clear  signs  that  some  of  them  are  at  work,  for  instance, 
geographical  isolation.  They  are  treated  in  detail  by  such  works  as 
those  of  Huxley  (1942)  and  Simpson  (1953)  and  there  properly  dis- 
cussed. These  questions  are  raised  here  only  as  a  reminder  that  they 
will  have  to  be  further  considered  if  any  satisfactory  general  evolu- 
tionary theory  is  to  emerge  and  to  be  applicable  to  the  vertebrates. 

17.  The  direction  of  evolutionary  change 

Since  we  cannot  closely  specify  the  factors  influencing  evolution 
we  can  hardly  expect  to  go  far  towards  the  solution  of  the  still  more 
difficult  problem  of  the  direction  of  evolutionary  change.  The  facts 
of  importance  that  have  emerged  from  the  evidence  about  vertebrates 
are  (1)  That  populations  tend  to  be  replaced  by  others  of  different 
form,  often  themselves  descended  from  the  first.  (2)  That  the  later 
populations  often  have  more  complicated  organizations  than  the  earlier 
ones;  we  can  hardly  be  said  to  have  established  this  last  clearly  as  a 
rule  in  vertebrates,  but  it  has  repeatedly  been  suggested  that  the 
evidence  supports  some  such  thesis.  (3)  Some  later  populations  invade 
habitats  not  previously  occupied  by  vertebrates  (e.g.  the  land). 

Facts  of  this  sort  have  led  us  repeatedly  to  the  suspicion  that  the 
later  types  are  often  in  some  way  better  able  to  carry  on  the  self- 
maintenance  of  life  than  their  predecessors,  and  that  vertebrate  life  is 
continually  invading  new  situations.  With  this  goes  the  suspicion  that 
the  total  biomass  of  vertebrate  life  (perhaps  of  all  life)  has  been  increas- 
ing and  the  energy  flux  becoming  more  rapid,  though  we  have  no  exact 
estimates  to  verify  this. 

For  organizing  our  knowledge  about  the  evolution  of  vertebrates  or 
other  animals  the  above  three  facts  about  the  progress  or  direction  of 
change  are  of  great  value.  The  invasion  of  new  habitats  is  of  particular 
interest,  because  it  is  usually  made  possible  by  the  increase  of  com- 
plexity, this  provides  a  system  of  elaborate  adjustments  that  maintains 
the  internal  conditions  nearly  constant  in  face  of  fluctuations  in  the 
environment.  This  internal  constancy  or  homeostasis  is,  of  course, 


xxxii.  18  EVOLUTIONARY   PROGRESS  785 

only  a  development  of  the  general  tendency  to  self-maintenance,  which 
characterizes  all  living  organisms;  but  it  is  carried  to  its  extreme  in  the 
higher  vertebrates,  giving  them  the  power  to  maintain  life  under  varied 
and  unpropitious  conditions. 

18.  The  influences  controlling  evolutionary  progress 

Our  analysis  of  the  factors  affecting  evolution  gives  us  clues  about 
the  influences  that  have  produced  this  increase  of  complexity.  Excess 
productivity  and  intra-specific  competition  force  sections  of  the  popu- 
lation to  try  new  habits.  Those  with  the  ability  to  do  so  may,  if  they 
can  tolerate  new  external  conditions,  find  situations  in  which  they  can 
flourish.  So  a  new  type  becomes  developed,  only  to  meet  later  the 
competition  of  its  own  descendants  or  other  invaders  and  hence  be 
driven  to  extinction  or  to  the  colonization  of  still  other  fields. 

If  we  have  interpreted  the  situation  correctly  there  can  be  said  to 
be  an  evolutionary  path  that  is  progressive,  in  the  sense  of  enabling 
life  to  be  lived  effectively  under  wider  and  wider  conditions.  Lotka 
has  suggested  that  it  is  possible  to  recognize  a  'basic  principle  defining 
the  direction  of  organic  evolution',  namely,  that  the  collective  effects 
of  organisms  'tend  to  maximize,  on  the  one  hand,  the  energy  intake 
of  organic  nature  from  the  sun,  and  on  the  other,  the  outgo  of  free 
energy  by  dissipative  processes  in  living  and  in  decaying  dead  organ- 
isms'. This  increasing  turn-over  of  energy  is  presumably  a  sign  of  the 
development  of  more  and  more  complicated  mechanisms  for  ensuring 
homeostasis  in  spite  of  external  changes.  These  mechanisms  in  turn 
depend  upon  an  increasing  store  of  instructions  in  the  genotype.  If  this 
view  is  correct  there  is  a  tendency  for  organisms  to  come  to  represent 
more  and  more  features  of  the  environment,  which  is  another  way  of 
saying  that  they  have  more  information  about  it.  More  simply  still  we 
may  say  that  they  come  to  be  able  to  live  under  ever  more  'difficult' 
conditions,  gathering  and  expending  more  energy  in  order  to  keep 
alive  (Young,  1938).  It  seems  reasonable  that  this  increase  of  complexity 
should  be  progressive;  as  the  organisms  acquire  more  information 
about  the  environment  they  also  gain  in  possibility  of  acquiring  still 
more.  In  particular  those  that  develop  mechanisms  for  learning  directly 
with  the  nervous  system  will  be  successful  and  will  evolve  fast.  It  is 
possible  in  this  way  to  see  the  basis  for  the  direction  of  evolutionary 
change.  Such  a  formulation  is  far  from  exact,  however,  and  the  process 
clearly  depends  upon  many  conditions  not  here  specified,  for  example 
as  to  the  nature  of  environmental  changes  and  the  effects  of  interaction 
between  organisms. 


786  CONCLUSION  xxxii.  18 

During  the  present  study  we  have  not  been  able  to  show  rigorously 
that  all  evolution  follows  such  principles,  but  the  data  are  not  incon- 
sistent with  this.  It  may  be  that  vertebrates  have  proceeded  farther 
along  the  path  suggested  than  any  other  animals.  The  birds  and 
mammals  probably  turn  over  energy  faster  than  other  vertebrates.  The 
point  that  must  not  be  overlooked  is  that  they  do  this  in  order  to 
provide  the  means  by  which  they  can  remain  constant,  in  spite  of 
fluctuations  in  the  external  conditions  of  an  environment  that  is 
different  in  composition  from  the  living  system. 

We  cannot  then  at  present  discern  with  certainty  the  principles  that 
determine  the  change  of  animal  form,  but  we  can  see  something  of  the 
influences  that  have  modified  the  original  vertebrate  type  to  produce 
the  great  variety  of  creatures  that  has  existed  and  remains  today.  We 
cannot  give  tables  of  numbers  to  show  how  the  variables  have  operated 
to  keep  Ceratodus  nearly  constant  for  200  million  years  while  related 
descendants  have  gone  on  to  produce  the  whole  variety  of  tetrapod  life. 
But  we  can  suggest  that  it  is  worth  while  pursuing  the  study  as  a  means 
of  building  a  truly  general  science  of  zoology.  We  begin  to  see  signs  of 
the  principles  according  to  which  the  vast  populations  of  animals 
interact  with  each  other,  with  the  plants,  and  with  the  inorganic  world. 
The  changes  that  these  interactions  produce  seem  to  be,  if  not  con- 
stantly in  one  direction,  at  least  often  such  as  to  allow  the  appearance 
of  more  varied  and  complicated  forms  of  life,  ever  more  able  to  maintain 
themselves  constant  and  apart  from  the  environment,  and  hence  to 
exist  in  a  wider  range  of  conditions.  The  effect  of  this  evolutionary 
change  has  probably  been  to  increase  the  amount  of  material  organized 
into  living  things,  while  the  total  energy  flux  through  the  system  has 
also  been  enlarged. 

This  finding  is  not  a  mere  rehabilitation  of  the  complacent  anthro- 
pocentric  prejudices  of  the  nineteenth  century.  The  conclusion  that 
there  is  a  sense  in  which  the  mammals  and  man  are  among  the  highest 
animals  should  be  based  on  objective  analysis  of  the  behaviour  of  the 
populations  of  vertebrates  and  the  flow  of  information  and  energy 
through  them.  However,  it  has  been  repeatedly  emphasized  that  we 
still  have  a  long  way  to  go  before  we  have  the  knowledge  necessary  to 
understand  these  very  slow  changes.  It  has  only  been  possible  in  this 
volume  to  suggest  certain  principles  that  may  one  day  make  possible 
a  satisfactory  systematic  study  of  the  life  of  vertebrates. 


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CHAPTERS   V-X.    FISHES 

Berg,  L.  S.    1940.    Classification  of  Fishes,  Both  Recent  and  Fossil.    Moscow  (with 

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Brown,  M.  E.    1957.    The  Physiology  of  Fishes.   2  vols.   New  York. 
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Burnstock,  G.    1958.    'The  Effect  of  Drugs  on  the  Spontaneous  Motility  and  on 

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1953-    Hozv  Animals  Move.    Cambridge. 

Harris,  J.  E.    1936-8.    'The  Role  of  the  Fins  in  the  Equilibrium  of  the  Swimming 

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CHAPTER  XI.    FISHERIES 

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CHAPTERS   XII,   XIII.     AMPHIBIA 

Bellairs,  A.  d'A.,  and  Boyd,  J.  D.    1950.    'Jacobson's  Organ.'    Proc.  zool.  Soc. 

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CHAPTERS   XIV,   XV.     REPTILES 

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Foxon,  G.  E.  H.,  Griffith,  J.,  and  Price,  Myfanwy.     1956.     'The  Mode  of 

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Swinton,  W.  E.    1934.    The  Dinosaurs.    London. 

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CHAPTERS  XVI-XVIII.     BIRDS 

Aymar,  G.  C.    1936.   Bird  Flight.   London. 

Beddard,  F.  E.    1898.    The  Structure  and  Classification  of  Birds.   London. 

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INDEX 


Major  topics  are  shown  in  Bold  Type,  genera  in  italic, 
and  authors'  names  in  Capitals  and  small  capitals 


Aardvark,  704. 
Acanthodii,  186. 
Acanthopterygii,  237. 
Accipiter,  wing,  454. 
Accommodation,  see  Eyes. 
Acentrophorus,  235. 
Aceratherium,  730. 
Acipenser,  234. 
Actinistia,  268. 
Actinopterygii,  190,  228,  772. 
Adapts,  614. 
Adaptive  radiation,  777. 

amphibia,  366. 

birds,  527. 

carnivora,  684. 

elasmobranchs,  175. 

lizards,  407. 

marsupials,  557,  568. 

snakes,  413. 

teleostei,  236,  244. 

tunicates,  69. 
Adder,  416. 

Adelospondyli,  296,  361. 
Adrenal 

actinopterygii,  207. 

amphibia,  301. 

dipnoi,  278. 

elasmobranchs,  165. 

lamprey,  98. 
Aepyceros,  762. 
Aepyornis,  514. 
Agamids,  407. 
Age,  of  rocks,  16. 
Agnatba,  24,  83,  125,  772. 
Agouti,  661. 
Agriochoerus,  751. 
Aigialosaurs,  409. 
Ailuropoda,  686. 
Ailnrns,  686. 
Air  bladder,  201,  217,  235,  244,  249, 

262,  272,  276,  280. 
Air  sacks,  birds,  471. 

reptiles,  379. 
Alarm  substances,  221. 
Alauda,  521. 
Albatross,  460,  517. 
Alburnns,  255,  280. 
Alcedo,  521. 
Alevins,  205. 
Allantois,  381. 
Alligator,  421. 
Allometry,  599,  737. 


Allosaurus,  423. 
Alopias,  182. 
Alouatta,  621. 
Alticamelus,  753. 
Alytes,  341,  360,  365. 
Amaroucium,  70. 
Amblypoda,  716. 
Amblyrhynchus,  408. 
Ambystoma,  358,  365. 
Amia,  199,  233,  235,  244,  262. 
Ammocoete  larva,  114. 
Amnion,  reptiles,  381. 
Amniota,  371. 
Amphibia,  296,  356,  362. 
Amphicentrum,  231. 
Amphignathodon,  332,  343. 
Amphilestes,  547. 
Amphioxides,  45,  46. 
Amphioxus,  23. 
Amphisbaena,  409. 
Amphitherium,  548. 
Amphiuma,  339,  358,  364. 
Amphodus,  332. 
Ampullae  of  Lorenzini,  172. 
Amylase,  amphioxus,  32. 

Ciona,  62. 
Amynodonts,  687. 
Anabas,  261. 
Anableps,  214. 
Anancus,  716. 
Anapsida,  386. 
Anaptomorphidae,  614. 
Anas,  517. 
Anaspida,  81,  127. 
Anchitherium,  736. 
Ancodonta,  748. 
Ancylopoda,  731. 
Angel  fishes,  248. 
Angler  fishes,  237,  248,  253,  254. 
Anguilla,  221,  226,  246,  249. 
Anguis,  382,  409. 
Ankylosaurs,  426. 
Anolis,  408. 
Anseriformes,  517. 
Ant-eaters,  Cape,  704. 

marsupial,  566. 

parallel  evolution  in,  593,  779. 

scaly,  601. 

spiny,  555- 

Xenarthra,  593. 
Antelopes,  760. 
Anthracotheres,  748. 


798 


INDEX 


Anthropoidea,  617. 
Anthus,  521. 
Antiarchi,  186. 
Antilocapra,  760. 
Antlers,  757. 
Anura,  361,  365. 
Apataelurus,  684. 
Apatosaurus,  423. 
Aphetohyoidea,  see  Placodermi. 
Apidium,  625. 
Aplodontia,  657. 
Apoda,  366. 
Apodes,  237. 
Appendicularia,  72. 
Apteryx,  514. 
Apus,  520. 
Aquila,  456. 
Araeoscelis,  399. 
Archaeoceti,  675. 
Archaeohippus,  740. 
Archaeomeryx,  755. 
Ardiaeopteryx,  509. 
Archelcn,  398. 
Archidiskodon,  716. 
Archosauria,  402,  416. 
Arctocyonidae,  683. 
Ardea,  461,  517. 
Arginine,  49. 
Armadillos,  595. 
Arsinoitherium,  718. 
Arteries,  amphibia,  335. 

amphioxus,  34. 

birds,  470. 

dipnoi,  277. 

elasmobranchs,  160. 

Lampetra,  92. 

mammals,  536. 

reptiles,  378,  397,  420. 

teleosts,  201. 
Arthrodira,  186. 
Artiodactyla,  741. 
Ascaphus,  307,  334,  360,  365. 
Ascidians,  60,  70. 
Ascidian  tadpole,  67. 
Asio,  520. 

Astrapotherium,  703. 
Astroscopus,  221,  249. 
Astylosternus,  334. 
Asymmetron,  25. 
Ateles,  620. 
Atrium,  Amphioxus,  25. 

Balanoglossus,  53. 

tunicates,  61,  70. 
Auditory  organs,  see  Ear. 
Auk,  519. 
Australian  aboriginals,  649. 

mammals,  568. 
Australopithecinae,  643,  781. 
Autonomic  nerves,  amphioxus,  33. 


actinopterygii,  214,  222,  258. 

amphibia,  338. 

chromatophores,  258,  410. 

elasmobranchs,  161,  171,  173. 

Lampetra,  91,  97. 

reptiles,  410. 

tunicates,  64. 
Autotomy,  410. 
Aves,  509. 
Awareness,  5. 
Aye-aye,  610. 
Azores,  birds  of,  530. 

Baboon,  624. 

Badger,  686. 

Balaena,  673. 

Balaenoptera,  672. 

Balanoglossus,  50,  78. 

Balfour,  F.,  149. 

Ballistes,  253. 

Baluchitherium,  709,  730. 

Barracuda,  251. 

Barrington,  E.  J.  W.,  32. 

Basilosaurus,  675. 

Bathyergidae,  660. 

Bathyglagus,  214. 

Bathypelagic  fishes,  247,  254,  265. 

Bat  fish,  257. 

Bats,  585. 

Batrachoseps,  339. 

Bauria,  544. 

Bdellostoma,  98,  122. 

Beak,  birds',  464. 

Bear,  685. 

Beaver,  657. 

Bee-eater,  521. 

Behaviour, 

amphibia,  354. 

amphioxus,  39,  41. 

birds,  472,  480,  491. 

carnivora,  681. 

chameleon,  409. 

enteropneusta,  55. 

evolutionary  significance,  781. 

fishes,  225. 

insectivores,  582. 

lampreys,  no,  113. 

mammals,  525. 

primates,  610,  620. 

reptiles,  382,  407,  409. 

tunicates,  64. 

ungulates,  697. 

whales,  672. 
Bernard,  C,  534. 
Berrill,  N.  J.,  63. 
Bettongia,  567. 
Biomass,  birds,  432. 

fishes,  242,  283. 

increase  in  evolution,  242,  769. 


INDEX 


799 


Biomass  (cont.) 

man,  641. 

rodents,  652. 
Bipedalism,  birds,  446. 

man,  646. 

reptiles,  416. 
Birds,  classification,  509. 

number,  432. 

origin,  510. 
Bison,  761. 
Bitterling,  266. 
Blackbird,  522. 
Blackcock,  502. 
Bladder,  actinopterygii,  202,  223. 

elasmobranchs,  163. 

reptiles,  381. 
Blastomeryx,  755. 
Blastula,  amphioxus,  42. 

tunicates,  68. 
Blennius,  237. 
Blood,  actinopterygii,  202. 

amphibia,  339. 

amphioxus,  34. 

Balanoglossus,  54. 

birds,  470. 

Ciona,  62. 

elasmobranchs,  162. 

hag-fishes,  124. 

Lampetra,  92. 

mammals,  766. 
Blue  fish,  251. 
Blue  whale,  672. 
Boa,  413. 
Bombinator,  354. 
Bone,  actinopterygii,  193. 

agnatha,  127,  129. 

birds,  437. 

placoderms,  187. 

types  of,  195,  230. 
Bone,  Q.,  33,  37. 
Borhyaena,  565. 
Bos,  761. 
Bothriolepis ,  186. 
Botryllns,  70. 
Bovidae,  760. 
Bower-birds,  507. 
Bow-fin,  235. 
Brachiopoda,  49,  58. 
Brachiosaurus,  423. 
Brachycepfialus,  298. 
Bradyodonts,  184. 
Brady  pus,  599. 
Bradysaurus,  390. 
Brady tely,  771. 
Brain,  aardvark,  704. 

actinopterygii,  209,  234. 

amphibia,  346. 

amphioxus,  39. 

artiodactyls,  744. 


birds,  477,  501. 

carnivora,  681. 

chelonia,  397. 

dinosaurs,  426. 

dipnoi,  279. 

earliest  chordates,  766. 

edentates,  594,  601. 

elasmobranchs,  167. 

elephant,  713. 

eutherians,  576. 

horses,  722,  735. 

insectivora,  582. 

Lampetra,  10 1. 

Latimeria,  272. 

mammals,  576. 

man,  633,  650. 

marsupials,  561. 

monotremes,  554. 

Orycteropus,  704. 

platypus,  554. 

Polypterus,  234. 

primates,  604,  618,  630,  633,  650. 

reptiles,  383. 

sea  cows,  721. 

seals,  692. 

synapsids,  542. 

ungulates,  697. 

whales,  671. 
Brain  waves,  amphibia,  349. 
Branchial  skeleton,  acanthodii,  187. 

actinopterygii,  196. 

amphibia,  330,  353. 

amphioxus,  25. 

Balanoglossus,  52. 

cephalaspids,  127. 

elasmobranchs,  145. 

lamprey,  87. 

mammals,  550. 

reptiles,  378. 

segmentation,  155. 

synapsids,  521. 

tunicates,  61. 
Branchiosaurs,  361. 
Branchiostoma,  25. 
Bream,  247. 
Breviceps,  360,  366. 
Brontops,  730. 
Brontosaurus,  423. 
Brontotheres,  730. 
Broom,  R.,  541. 
Brown  funnels  (amphioxus),  36. 
Budding,  tunicates,  69,  72. 
Buettneria,  359. 
Bitfo,  298,  360,  365. 
Bull,  H.  O.,  225. 
Bullock,  T.  H.,  55. 
Bull-head,  218. 
Bush-baby,  613. 
Bushmen,  649. 


8oo 

Butterfly  fishes,  257. 
Buzzard,  517. 

Cacops,  359. 

Caecilia,  366. 

Caenolestes,  566. 

Caiman,  421. 

Calamoichthys,  233. 

Calidris,  519. 

Callithrix,  621. 

Callorhinus,  693. 

Calotes,  407. 

Calyptocephalus,  331. 

Camarhynchus,  467,  526. 

Camels,  751. 

Cams,  685. 

Capella,  519. 

Capitosanrus,  359. 

Capra,  764. 

Capreolus,  757. 

Caprimulgiformes,  520. 

Captorhinas,  389,  539. 

Capybara,  661. 

Carcharhinus,  162. 

Carcharodon,  182. 

Cardiac  nerves,  amphibia,  338. 

elasmobranchs,  161. 

lamprey,  91. 
Cariama,  519. 
Carnivora,  680. 

Carnivores,  succession  of,  776. 
Carotid  body,  amphibia,  336. 

fishes,  161. 
Carp,  237,  247. 
Carpus,  298,  see  Limbs. 
Caruncle,  382,  553. 
Castor,  659. 
Casnarins,  514. 
Cat,  680. 
Catarrhina,  623. 

Cat-fish,  237,  244,  250,  261,  266. 
Catnrus,  236. 
Cavia,  660. 
Cebidae,  620. 
Centrocercus,  501. 
Centrum,  see  Vertebrae. 
Cephalaspida,  see  Osteostraci. 
Cephalaspis,  125. 
Cephalization,  148. 
Cephalodiscus,  50,  58,  75. 
Ceratias,  247,  254. 
Ceratodus,  262,  268,  771. 
Ceratomorpha,  727. 
Ceratophrys,  302,  343. 
Ceratopsia,  426. 
Ceratotrichia,  133. 
Cercopithecidae,  623. 
Cere,  432. 
Certhia,  521. 


INDEX 


Certhidia,  526. 
Cervidae,  755. 
Cervus,  757,  751. 
Cetacea,  666. 
Cetorhinus,  181. 
Chaetodon,  257. 
Chaffinch,  472,  522. 

migration,  523. 
Chalicotheres,  731. 
Chameleon,  408. 
Chanos,  281. 
Charadriiformes,  519. 
Cheirolepis,  229. 
Cheiromys,  610. 
Chelone,  393,  396. 
Chelonia,  392. 
Chelydra,  396. 
Chelys,  396. 

Chemoreceptors,  «■?  Olfactory  or- 
gan, Taste. 
Chevrotain,  754. 
Chilomycterus,  246,  249. 
Chimaera,  184. 
Chimpanzee,  626. 
Chiroleptes,  297,  341. 
Chironectes,  564. 
Chiroptera,  585. 
Chlamydosaurus,  407,  416. 
Chlamydoselache ,  181. 
Choloepns,  599. 
Chondrocranium,  5^  Skull. 
Chondrostei,  234. 
Chordata,  origin  of,  47,  74,  765. 

affinities  of,  75. 

characteristics,  23. 

classification,  24. 
Choroid  gland,  260. 
Choroid  plexus,  Lampetra,  101. 
Chromatophores,  actinopterygii,  255. 

amphibia,  299. 

elasmobranchs,  142. 

innervation,  410. 

Lampetra,  84,  107. 
Chrysemys,  392,  396. 
Chrysochloris,  583,  778. 
Ciconia,  517. 
Cilia,  amphioxus,  31. 

Balanoglossus,  51. 

Ciona,  61. 
Ciliary  ganglion,  actinopterygii,  223. 

elasmobranchs,  151,  174. 
Cingulata,  595. 
Ciona,  60,  70. 
Circulation,  actinopterygii,  201. 

amphibia,  335. 

amphioxus,  33. 

Balanoglossus,  54. 

birds,  470. 

Cephalodiscus,  58. 


INDEX 


80 1 


Circulation  (cont.) 

Ciona,  62. 

dipnoi,  277. 

earliest  chordates,  766. 

elasmobranchs,  159. 

Lampetra,  91. 

monotremes,  554. 

reptiles,  378,  420. 

seals,  692. 

tunicates,  62. 

whales,  670. 
Citellus,  657. 
Civet,  689. 

Cladoselache,  176,  178. 
Clarias,  261. 

Classification,  see  Evolution,   syste- 
matic. 
Clavelina,  67. 
Cleavage,  actinopterygii,  204,  236. 

amphioxus,  42. 

Balanoglossas,  55. 

elasmobranchs,  180,  184. 

radial,  48. 

spiral,  48. 
Cleithrolepis,  233. 
Climatic  change,  actinopterygii,  238. 

cretaceous,  570. 

evolution,  13. 
Climatius,  186. 
Climbing  perch,  261. 
Cline,  523. 
Cling-fish,  251. 
Clitoris,  see  Fertilization. 
Cloaca,  bird,  469. 

insectivores,  582. 

Lampetra,  96. 

marsupials,  560. 

monotremes,  554. 
Club-shaped  gland,  44. 
Clupea,  237,  251. 
Cobra,  415. 
Coccosteus,  186. 
Cod,  food  of,  257,  286. 

reproduction,  265,  283. 
Coelacanthini,  271. 
Coelolepida,  81,  129. 
Coelom,  amphioxus,  26,  31,  42. 

Balanoglossus,  51. 

birds,  473. 

Cephalodiscus,  58. 

development,  42,  45,  48. 

elasmobranchs,  148,  161. 

Lampetra,  93. 

mammals,  554. 

reptiles,  420. 

segmentation,  45,  148. 

tunicates,  63. 
Collocalia,  489. 
Colobus,  624. 


Colour,  actinopterygii,  255. 

amphibia,  299. 

birds,  436. 

birds'  eggs,  477,  507. 

cryptic,  256,  437. 

dymantic,  302. 

elasmobranchs,  142. 

lampreys,  84. 

mammals,  604,  618. 

primates,  604,  624. 

reptiles,  373,  410. 

sematic,  258,  437. 

tunicates,  61. 

ungulates,  696. 
Colour   change,    actinopterygii,    258, 
410. 

amphibia,  300. 

elasmobranchs,  142,  164. 

Lampetra,  105. 

reptiles,  373,  410. 

tunicates,  61. 
Colour  vision,  birds,  487. 

fishes,  212,  255. 

primates,  604,  618. 
Colubridae,  413. 
Colugo,  592. 

Columba,  439,  456,  468,  495,  519. 
Colymbiformes,  516. 
Communication,  amphibia,  334. 

birds,  472,  492. 

carnivores,  681. 

fishes,  218. 

horses,  735. 

primates,  621,  624,  630,  633,  648. 

seals,  692. 

ungulates,  697. 

whales,  672. 
Compsognathus,  422. 
Conditioning,  see  Learning. 
Conduction  velocity,  98. 
Condylartha,  700. 
Coney,  707. 
Congiopodus,  218. 
Continental  drift,  13. 
Continents,  level  of,  II. 
Convergent  evolution,  777. 
Coot,  518. 
Coraciiformes,  520. 
Coral  fishes,  233,  241,  252. 
Cormorant,  517. 
Corn-crake,  518. 
Corpuscles,  see  Blood. 
Corvus,  477. 
Coryphodon,  718. 
Cosmine,  229,  269. 
Cottus,  218. 
Cotylosauria,  389. 
Courtship,  actinopterygii,  267. 

amphibia,  342. 


3F 


802 


INDEX 


Courtship  (cont.) 

birds,  497. 

lampreys,  112. 

reptiles,  382. 
Cow,  695. 
Crane,  493,  518. 
Cranial  capacity,  601. 
Cranial  nerves,  cephalaspids,  127. 

elasmobranchs,  148. 

segmentation,  148. 
Craniata,  81. 
Creatine,  49. 
Creodonta,  683. 
Crex,  518. 
Crocodilus,  418. 
Crossopterygii,  268,  356. 
Crotalus,  415. 

Cryptobranchus,  354,  358,  364. 
Cryptodira,  398. 
Ctenacanths,  176. 
Cuckoo,  507. 
Cuculiformes,  507,  519. 
Culture  stages,  648. 
Curlew,  467,  519. 
Cuscus,  567. 
Cycles,  food,  285. 
Cyclomyaria,  70. 
Cyclopes,  596. 
Cyclostomata,  81. 
Cygnus,  517. 
Cynocephalus,  592. 
Cynognathus,  544. 
Cynomys,  657. 
Cyprinus,  237,  252,  266. 

Dactylopterus,  250. 
Dama,  757. 
Dapedins,  236. 
Darwin's  finches,  524. 
Darwin's  notebook,  524. 
Dasypeltis,  415. 
Dasyprocta,  661. 
Dasypus,  595. 
Dasyurus,  560,  564. 
Daubentonia,  610. 
De  Beer,  G.  R.,  514. 
Deer,  756. 
Deinotheriam,  717. 
Delphinoidea,  673. 
Deltatheridium,  582. 
Dendrobates,  299. 
Dendrohyrax,  709. 
Denticles,  see  Scales,  placoid. 
Dentine,  dipnoi,  269. 

elasmobranchs,  142. 

pteraspida,  129. 
Dermochelys,  392,  396. 
Dermoptera,  592. 
Dermotrichia,  200. 


Desmodus,  588. 

Development,  actinopterygii,  204. 

amphibia,  342,  465. 

amphioxus,  41. 

Balanoglossus,  56. 

birds,  508. 

Cephalodiscus,  58. 

edentates,  596. 

elasmobranchs,  164. 

elephants,  713. 

dipnoi,  278. 

Lampetra,  114. 

man,  640. 

marsupials,  560. 

monotremes,  554. 

primates,  640. 

reptiles,  381. 

tunicates,  66. 
Diacodexis,  747. 
Diadectes,  309,  390. 
Diademodus,  177. 
Diaphragm,  420,  473,  554,  668. 
Diapsida,  391,  402. 
Diarthrognathus,  544. 
Diastrophic  movements,  12. 
Diatryma,  519. 
Dicerorhinus,  730. 
Diceros,  730. 
Dicotyles,  749. 
Dicynodon,  541. 
Didactyly,  562. 
Didelphys,  563. 
Didolodus,  701. 
Digestion,  actinopterygii,  201. 

amphibia,  342. 

amphioxus,  32. 

Balanoglossus,  52. 

birds,  468. 

Ciona,  62. 

elasmobranchs,  158. 

Lampetra,  87. 

reptiles,  378. 

trout,  201. 
Dimetrodon,  326,  540. 
Dinocephalia,  541. 
Dinocerata,  716. 
Dinornis,  514. 
Dinosaurs,  421. 
Diodon,  218,  252. 
Diomedea,  460,  517. 
Diphylla,  588. 
Diplocaulus,  361,  362. 
Diplodocus,  423. 
Diphpterax,  268. 
Dipnoi,  268. 
Dipodomys,  659. 
Diprotodon,  568. 
Diprotodont  marsupials,  562. 
Dipterus,  268. 


INDEX 


803 


Dipus,  659. 
Direction-finding,  bats,  566. 

birds,  493. 
Discoglossus,  313. 
Disphclidus,  415. 
Display,  birds,  481,  497. 
Dissacus,  684. 
Distraction  display,  502. 

DOBHZANSKY,  T.,   122. 

Docodonta,  546. 

Dodo,  519. 

Dogfish,  134,  181,  250. 

Dogs,  685. 

Dolichosaurs,  409. 

Dolichosoma,  361. 

Doliolum,  70,  72. 

Dolphin,  666. 

Doras,  250. 

Dorypterus,  231. 

Draco,  407,  426. 

Drift  nets,  283. 

Dromiceius,  514. 

Dromocyon,  684. 

Drum  fish,  218. 

Dryopithecus,  632. 

Duck,  437,  467,  497,  517,  778. 

Duck-bills,  778. 

Ducts,  genital,  see  Reproduction. 

Dugong,  720. 

Dymantic  coloration,  302. 

Eagle,  456,  517. 

Eagle-ray,  250. 

Ear,  actinopterygii,  216,  489. 

amphibia,  327,  353,  489. 

bats,  588. 

birds,  488. 

chelonia,  398. 

elasmobranchs,  171. 

Lampetra,  109. 

mammals,  489. 

monotremes,  550. 

reptiles,  378,  385,  407,  411. 

snakes,  411. 

stegocephalia,  327. 

synapsids,  542. 

whales,  668,  671. 
Echidna,  549. 
Echinoderms,  49,  57,  75. 
Echo-sounding,  bats,  588. 

birds,  489. 

whales,  672. 
Ecliptic,  changes,  14. 
Edaphosanrus,  540. 
Edentata,  592. 
Eel,  133,  226,  237,  246,  261. 
Efficiency  of  organisms,  10,  769,  775. 
Egg  tooth,  382,  553. 
Eggs,  amphibia,  341,  365,  366. 


actinopterygii,  265,  283. 

amphioxus,  42. 

birds,  475,  507. 

chelonia,  397. 

dipnoi,  278. 

elasmobranchs,  163,  180,  181. 

hag-fishes,  124. 

lampreys,  113. 

marsupials,  560. 

monotremes,  551. 

reptiles,  381,  421,  430. 

seals,  692. 
Eland,  763. 
Elapidae,  415. 

Elasmobranchs,  131,  175,  772. 
Electric  organ,  actinopterygii,  253. 

cephalaspida,  127. 

Torpedo,  182. 
Electrophorus,  254. 
Elephant,  706,  709. 
Elephant-bird,  514. 
Elephant-shrews,  584. 
Elephas,  706. 
Elpistotege,  326,  356. 
Embolomeri,  357. 
Embrithopoda,  718. 
Emu,  514. 

Emys,  380,  393,  396. 
Endostyle,  amphioxus,  32,  44. 

Ciona,  61. 

evolution  of,  76. 

Lampetra,  1 17. 
Energy  flux,  increase  of,  10,  769. 
Entelodon,  748. 
Enterocoele,  48. 
Enteropneusta,  50. 
Entosphenus ,  121. 
Enzymes,  see  Digestion. 
Eodelphis,  563. 

Eogyrinus,  297,  309,  357,  774. 
Eohippus,  726. 
Eosuchia,  402. 
Eotitanops,  730. 
Eotragus,  761. 
Epicardium,  63,  66,  68. 
Epihippus,  726,  736. 
Equus,  732,  774. 
Erinaceus,  583. 
Erithacus,  482. 
Eryops,  297,  359,  522. 
Esox,  221,  237,  251. 
Eunotosauras,  399. 
Euparkeria,  510. 
Easthenopteron,  268,  307,  314. 
Eutheria,  origin  of,  574. 
Evolution,  absence  of,  771. 

adaptive  radiation,  244,  366. 

convergent,  777. 

definition,  8. 


804 


INDEX 


Evolution  (cont.) 

direction  of,  9,  769,  784. 

evidences,  769. 

extinction,  775. 

increasing  complexity,  768. 

large  size,  429,  542,  575,  735. 

non-adaptive,  362. 

organization,  9,  767,  780. 

persistence,  238,  430,  784. 

populations,  8. 

rate,  738,  770. 

replacement,  10,  238,  429,  775. 

return  to  water,  359,  362,  409,  429, 

775-  . 
succession  in  habitats,  776. 
factors,  238,  785. 

accelerating,  532,  783. 

barriers,  568,  783. 

climate,  21,  371,  776,  783. 

competitors,  241,  362,  532. 

mutation,  8,  242. 

pathogens,  783. 

predators,  355,  362,  532,  783. 

productivity,  242,  783. 

retarding,  773. 

sea,  238. 
parallel,  777. 

actinopterygii,  240. 

amphibia,  366. 

elephants,  715. 

mammals,  545,  575. 

reptiles,  427,  430. 

synapsids,  545. 

ungulates,  699. 
progress,  9,  80. 

actinopterygii,  242. 

amphibia,  367. 

early  chordates,  80. 

elasmobranchs,  185. 

eutherians,  575. 

land,  775. 

land  herbivores,  776. 

mammalia,  534. 

water,  775. 

whales,  676. 
reversal,  780. 

amphibia,  343. 

birds,  518. 

eutherians,  545. 

reptiles,  401. 
systematic 

actinopterygii,  228,  237. 

agnatha,  81,  122. 

amphibia,  296,  356. 

artiodactyls,  747. 

birds,  509. 

carnivora,  678. 

chordates,  47,  78,  81. 

elasmobranchs,  175,  185. 


elephants,  714. 

eutherians,  533. 

horses,  734. 

lampreys,  81. 

mammals,  533. 

man,  648. 

perissodactyls,  723. 

primates,  642. 

reptilia,  369,  389. 

ungulates,  699. 

vertebrates,  summary,  768. 
tendencies,  779. 

actinopterygii,  237. 

amphibia,  362. 

birds,  522. 

elasmobranchs,  185. 

eutherians,  575. 

horses,  735. 

reptiles,  429. 

ungulates,  699. 

vertebrates,  779. 
Excretion,  actinopterygii,  202. 
amphibia,  340. 
amphioxus,  35. 
Balanoglossiis,  54. 
birds,  474. 
chelonia,  397. 
Ciona,  63. 

elasmobranchs,  162. 
Lampetra,  93. 
reptiles,  378. 
Exocoetus,  237,  246,  250. 
Eye-muscles,  150. 
Eyes,  actinopterygii,  212,  485. 
amphibia,  350. 
amphioxus,  40. 
birds,  482. 
chameleon,  409. 
elasmobranchs,  170. 
insectivores,  582. 
Lampetra,  103,  no. 
ophidia,  411. 

primates,  485,  604,  615,  618. 
reptiles,  384,  409,  411,  485. 
seals,  692. 
squamata,  407. 
tunicates,  64,  67. 
whales,  671. 

Falco,  454. 

Falconiformes,  517. 

Feathers,  432. 

Feeding,  actinopterygii,  201. 

amphibia,  342. 

amphioxus,  30. 

anaspids,  129. 

artiodactyls,  697. 

Balanoglossiis,  52. 

bats,  588. 


INDEX 


805 


Feeding  (cont.) 

birds,  466,  491. 

cephalaspids,  127. 

Cephalodiscus,  58. 

chameleon,  408. 

Ciona,  6 1 . 

dinosaurs,  423,  424. 

dipnoi,  276. 

earliest  chordates,  765. 

elasmobranchs,    158,    179,    180,   181, 
182,  184. 

elephants,  709. 

flamingo,  467. 

fox,  685. 

hyrax,  708. 

lamprey,  88,  1 14. 

perissodactyls,  697,  722. 

primates,  606,  623,  662. 

pteraspids,  129. 

reptiles,  378,  408,  423. 

rodents,  662. 

sea  cows,  721. 

snakes,  413. 

trout,  201. 

ungulates,  697. 

whales,  668. 
Feet,  see  Limbs. 
Felis,  680,  689. 
Fertilization,  actinopterygii,  204,  266. 

amphibia,  342,  365. 

amphioxus,  41. 

Balanoglossus,  56. 

bats,  591. 

birds,  475. 

chelonia,  397. 

elasmobranchs,  164. 

Lampetra,  95,  112. 

marsupials,  559. 

monotremes,  554. 

reptiles,  380,  411. 

snakes,  41 1. 

trout,  204. 

tunicates,  66. 
Ferungulata,  677. 
Finches,  521,  524. 
Fins,  acanthodii,  187. 

actinopterygii,  179,  192,  229,  235,245. 

amphioxus,  28. 

Cladoselache,  178. 

development,  178. 

dipnoi,  179,  275,  322. 

elasmobranchs,  130,  176. 

function,  133,  136,  307. 

Gadus,  173. 

Jamoytius,  128. 

Lampetra,  84,  113. 

muscles,  194,  293,  305. 

Neoceratodns,  179,  275,  322. 

ostracoderms,  125,  127. 


palaeoniscids,  229. 

Pleur  acanthus,  179. 

rays,  200. 

reptiles,  401. 

sirenia,  720. 

whales,  660. 
Fish-eaters,  parallel  evolution,  778. 
Fish  yields,  280,  287. 
Fisher,  R.  A.,  783. 
Fishing  methods,  281. 
Fissipeda,  684. 
Flamingo,  467,  517. 
Flat  fishes,  248,  256,  262. 
Flight,  birds,  450. 

origin  in  birds,  426,  513. 

pterodactyls,  428. 
Flints,  648. 
Flycatcher,  458. 
Flying  fish,  237,  246,  250. 

squirrel,  657. 
Food,  see  Feeding. 
Food  cycles,  285. 
Fovea,  213. 
Fox,  685. 

Fright  reaction,  221. 
Fringilla,  521,  522. 
Frisch,  K.  v.,  207,  467. 
Frogs,  298. 
Fidica,  518. 
Fulmarus,  493. 
Fundulus,  260. 

Gadus,  237,  251. 

Galago,  613. 

Galapagos  Islands,  524. 

Galeoidea,  181. 

Galeopithecus,  592. 

Galepus,  541. 

Galliformes,  518. 

Gallitiula,  518. 

Gallus,  518. 

Gambusia,  266. 

Gannet,  517. 

Ganoin,  187,  229,  235,  236. 

Garstanc,  W.,  74. 

Gasterosteus,  221,  237,  266. 

Gastrotheca,  360,  366. 

Gastrulation,  42,  48,  68. 

Gavialis,  421. 

Gaviiformes,  516. 

Gecko,  406. 

Gemundina,  186. 

Genetic  drift,  530. 

Geographical  distribution,  bats,  592. 

carnivora,    641. 

dipnoi,  268. 

man,  649. 

marsupials,  568. 

isolation,  birds,  524. 


8o6 


INDEX 


Geographical  isolation  (cont.) 

marsupials,  568. 
Geographical  regions,  573. 
Geography,  changes  of,  11,  573. 
Geological  periods,  11,  571. 
Geomys,  659. 
Geospizinae,  525. 
Geotria,  121. 
Gerbillus,  659. 
Germ  layers,  26,  69. 
Giant  nerve  cells,  amphioxus,  38. 

Lampetra,  97. 
Gibbon,  626. 
Gills,  actinopterygii,  197. 

amphibia,  315. 

amphioxus,  30. 

Balanoglossus,  53. 

Cephalaspis,  127,  145. 

Cephalodiscus,  58. 

Ciona,  61. 

elasmobranchs,  157. 

hag-fishes,  123. 

lamprey,  89,  1 17. 

Pteraspis,  129. 
Giraffes,  757. 
Glires,  653. 

Globe-fishes,  246,  249,  252,  258. 
Glossobalanus,  50. 
Glottis,  amphibia,  333. 

dipnoi,  261. 

reptiles,  360. 
Glyptodon,  595. 

Gnathostomata,  24,  143,  175,  186. 
Goats,  720. 
Gobio,  221,  251,  266. 
Goldcrest,  470. 
Goldfish,  237,  252. 
Gomphotherium,  715. 
Gonads,  see  Reproduction,  Fertiliza- 
tion. 
Goodrich,  E.  S.,  35,  178. 
Goodrichia,  175,  179. 
Gopher,  659. 
Gorilla,  626. 
Graham,  M.,  287. 
Grammatophora,  416. 
Grammistes,  257. 

Grandry,  corpuscles  of,  432,  490. 
Graptolites,  49,  59. 
Graviportal  animals,  697,  728,  742. 
Gray,  J.,  134. 
Grebe,  499,  516. 
Grilse,  206. 
Ground-sloths,  596. 
Grouse,  518. 

Growth,  relative,  599,  737. 
Gruiformes,  518. 
Grus,  518. 
Guanin,  255. 


Guenon,  624. 
Guereza,  625. 
Guillemot,  519. 
Guinea  fowl,  518. 
Gull,  468,  491,  519. 
Gurnard,  237,  250. 
Gymnophiona,  366. 
Gymnothorax,  257. 
Gymnotus,  254. 
Gyps,  459- 

Habitat  selection,  birds,  491. 
Haddock,  cycles  of,  285. 

yields  of,  285. 
Hadrosaurus,  424. 

Haemoglobin,  see  Pigments,  blood. 
Haemopoiesis,  actinopterygii,  202. 

amphibia,  339. 

birds,  470. 

dipnoi,  278. 

lamprey,  93. 
Hag-fish,  see  Myxine  Bdellostoma. 
Haldane,  J.  B.  S.,  770. 
Hamadryas,  415. 
Hapale,  621. 

Harris,  J.  E.,  137,  178,  244. 
Hatscheks  pit,  31,  44,  65. 
Hatteria,  see  Sphenodon. 
Hawaii,  birds  of,  531. 
Hawk,  482,  517. 
Head,  actinopterygii,  193. 

amphibia,  326. 

amphioxus,  32. 

birds,  464. 

elasmobranchs,  142. 

lamprey,  84. 

organization,  142. 
Hearing,  see  Ear. 
Heart,  actinopterygii,  201,  234. 

amphibia,  334. 

birds,  470. 

chelonia,  397. 

Ciona,  62. 

crocodile,  420. 

dipnoi,  277. 

elasmobranchs,  159. 

lamprey,  91. 

Latimeria,  z'jz. 

reptiles,  379,  397,  413,  420. 

snakes,  413. 

tunicates,  62. 

whales,  670. 
Hedgehog,  583. 
Hedge-sparrow,  522. 
Heilmann,  G.,  488. 
Heloderma,  378,  410. 
Helodus,  185. 
Hemichordata,  24,  50. 
Heptranchias,  180. 


INDEX 


S07 


Herbivores,  succession  of,  542. 
Herbst,  corpuscles,  490. 
Heron,  461,  493. 
Herpestes,  688. 
Herring,  237,  251. 

reproduction,  265,  283. 

shoaling,  281. 
Hesperornis,  513. 
Heterodontus,  180,  771. 
Heterostraci,  81,  128. 
Hexanchus,  146,  180. 
Hibernation,  bats,  588. 

birds,  471. 

insectivores,  582. 
Hipparion,  737. 
Hippidion,  737. 

Hippocampus,  237,  246,  249,  256,  266. 
Hippopotamus,  748. 
Hippural  bones,  200. 
Hirundo,  522. 
Histricomorpha,  657. 
Hoatzin,  518. 
Hogben,  L.,  164,  300. 
Holacanthus,  257. 
Holmes,  A.,  17. 
Holocephali,  184. 
Holostei,  234. 
Homalodotherium,  702. 
Homeostasis,  4,  773,  781. 

amphibia,  368. 

mammals,  534. 
Homeothermy,  amphibia,  299. 

evolution,  372. 

reptilia,  372. 
Homing,  birds,  493. 
Homo,  633. 
Homoeosaurus ,  402. 
Homogalax,  728. 
Homunculus,  622. 
Hoplopteryx,  237. 
Hornbill,  467. 
Horns,  696,  741,  758. 
Horse,  695. 
Howard,  Eliot,  503. 
Humming-birds,  520. 
Huxley,  J.  S.,  504,  737. 
Huxley,  T.  H.,  149. 
Hyaena,  688. 
Hyaenodon,  684. 
Hybodus,  180. 
Hydrochoerus,  661. 
Hydrophiidae,  415. 
Hyla,  299,  360,  366. 
Hylobates,  626. 
Hyoid,  see  Branchial  arches. 
Hyopsodus,  700. 
Hyperoodon,  674. 
Hypobythius,  70. 
Hypohippus,  736. 


Hypophysial  sac,  Lampetra,  106. 
Hypophysis,  see  Pituitary. 

Hypotremata,  180,  182. 
Hyrachyus,  729. 
Hyracodonts,  730. 
Hyracoidea,  707. 
Hyracotherium,  726,  774. 
Hystricomorpha,  657. 
Hystrix,  661. 

Ice  Ages,  15,  648. 
Ichthyophis,  366. 
Ichthyopterygia,  40 1 . 
Ichthyornis,  513. 
Ichthyosauria,  401. 
Ichthyostega,  326,  356. 
Ictidosauria,  544. 
Iguana,  407. 

limbs,  315. 
Iguanodon,  424. 
Impala,  762. 
Indri,  610. 

Insect-feeders,  paraliel  evolution,  778. 
Insectivora,  581. 
Interrenal,  see  Adrenal. 
Intestine,  actinopterygii,  201,  233. 

amphibia,  343. 

amphioxus,  32. 

Balanoglossus,  54. 

birds,  469. 

Ciona,  62. 

elasmobranchs,  159. 

lampreys,  90. 
Iodine,  amphioxus,  32. 

Lampetra,  117. 

tunicates,  62. 
Iridocytes,  255. 
Iris,  see  Eyes. 
Irregularia,  48. 
Ischyromyidae,  657. 
Isinglass,  280. 
Island  faunas,  524. 
Isopedin,  129,  269. 
Isospondyli,  237. 
Isostasy,  12. 
Isotopes,  3,  16. 
Isuridae,  131. 

Jackdaw,  463,  521. 

Jacobson's  organ,  156,  342,  350,    385, 

405- 
Jamoytius,  127. 
Jaws,  acanthodii,  146,  187. 

actinopterygii,  195,  230,  234,  235. 

amphibia,  327,  330. 

birds,  464. 

carnivora,  682. 

crossopterygians,  270,  273. 

dinosaurs,  423. 


8o8 


INDEX 


Jaws  (cotit.) 

clasmobranchs,  145,  176,  184. 

elongated,  430,  778. 

frog,  331. 

mammals,  536. 

marsupials,  558. 

monotremes,  550. 

origin  of,  145. 

ostracoderms,  127. 

palaeoniscoidea,  230. 

primates,  637. 

reptiles,  377,  396,  412,  423,  430. 

rodents,  656. 

snakes,  412. 

sturgeon,  234. 

suspension,  145. 

synapsids,  544. 

ungulates,  698. 

whales,  668. 
Jerboa,  659. 
John  Dory,  237,  248. 

Kangaroo,  566. 
Kannemeyeria,  542. 
Karroo,  537. 
Kelts,  205. 
Kestrel,  517. 
Kidney,  see  Excretion. 
Kinesis,  272,  377. 
Kingfisher,  484,  521. 
Kiwi,  490,  514. 
Knowles,  F.,  96,  103. 
Koala,  567. 
Kolliker's  pit,  40. 
Komodo  dragon,  409. 
Krait,  415. 

Labidosaurus,  389. 
Labrus,  237,  251. 
Labyrinthodontia,  296,  356. 
Lacerta,  372,  409. 

eggs,  382. 

skull,  377. 
Lacertilia,  407. 
Lachesis,  415. 
Lack,  D.,  503,  524. 
Lagomorpha,  660. 
Lagopas,  518. 
Lagostomus,  661. 
Lama,  751. 
Lambdotherium,  730. 
Lampetra,  83,  119. 
Land  bridges,  573. 
Land,  colonization  of,  296,  355,    381, 

429. 
Land  vertebrates,  succession,  429,  775. 
Lanius,  470,  485,  522. 
Lanthanotus,  410. 
Lapwing,  519. 


Lariosaurus,  399. 

Lark,  463,  521. 

Lams,  519. 

Larva,  amphibia,  334,  358,  361,  364. 

amphioxus,  43. 

Cephalodiscus,  58. 

dipnoi,  279. 

Lampetra,  114. 

Larvacea,  70. 

polyzoa,  58. 

tornaria,  56. 

tunicates,  67. 
Larynx,  amphibia,  334. 

birds,  471. 

reptiles,  379. 
Lateral  line,  actinopterygii,  218. 

amphibia,  326. 

bones,  195,  230. 

cephalaspids,  127. 

elasmobranchs,  172,  218. 

functions,  218,  230. 

Lampetra,  108. 

palaeoniscids,  230. 

placoderms,  187. 

pteraspida,  129. 
Lateral  plate  musculature,  155. 
Latimeria,  268,  771. 
Laagia,  246. 
Learning,  actinopterygii,  210,  225. 

amphibia,  354. 

elephants,  713. 

horses,  735. 
Lebistes,  258,  266. 
Leiopelma,  307,  360,  365. 
Lemmas,  661. 
Lemur,  609. 
Leopard,  690. 
Lepadogaster,  251. 
Lepidosauria,  401. 
Lepidosiren,  262,  268,  275. 
Lepidotes,  236. 
Lepidotrichia,  200. 
Lepisosteus,  233,  235,  244,  262. 
Lepomis,  245,  250. 
Lepospondyli,  296,  361. 
Leptictoidea,  584. 
Leptocephalus  larvae,  243. 
Leptodactylus,  312. 
Leptolepis,  236. 
Leuciscus,  191,  237. 
Leucocytes,  actinopterygii,  202. 

amphibia,  338. 

birds,  471. 

lampreys,  93. 
Life,  definition  of,  2. 
Limbs,  aardvark,  704. 

amphibia,  304,  309. 

artiodactyls,  696,  742,  758. 

bats,  586. 


INDEX 


809 


Limbs  (cont.) 

birds,  440,  512. 

camels,  751. 

carnivora,  682. 

chalicotheres,  731. 

chelonia,  394. 

crocodiles,  419. 

dinosaurs,  423. 

direction  of  movements,  299. 

edentata,  594,  600. 

elephants,  712. 

eutherians,  576. 

horses,  732. 

hyrax,  708. 

ichthyosaurs,  401. 

insectivores,  582. 

man,  616,  628,  635. 

marsupials,  559,  566. 

moles,  565,  583,  778. 

monotremes,  551. 

origin  of,  307. 

perissodactyls,  696,  722. 

plesiosaurs,  399. 

primates,  605,  616,  618,  629,  633. 

pterodactyls,  427. 

reptiles,  373,  394,  411,  417,  4*9,  423, 
428. 

rodents,  657. 

sea  cows,  720. 

seals,  691. 

snakes,  411. 

synapsids,  540,  542. 

ungulates,  696. 

whales,  667. 
Limb  Muscles,  amphibia,  308. 

birds,  418. 

fishes,  308. 

reptiles,  375. 
Limnopithecus,  632. 
Limnoscelis,  389. 
Ling,  265. 
Lion,  690. 
Lipase,  amphioxus,  34. 

Ciona,  62. 
Lipotyphla,  584. 
Litopterna,  703. 
Liver,  amphibia,  343. 

amphioxus,  32. 

elasmobranchs,  139. 

lamprey,  90. 
Llama,  751. 
Loach,  265. 
Locomotion,  actinopterygii,  133,  191, 

235.  244- 
amphibia;  303,  308,  317,  357. 
amphioxus,  26. 
Balanoglossus ,  51. 
birds,  440. 
crocodiles,  419. 


dinosaurs,  423. 

earliest  chordates,  766. 

elasmobranchs,  131. 

fishes,  133. 

giraffe,  757. 

Lampetra,  85. 

primates,  605,  616,  618,  629,  633. 

pterodactyls,  428. 

reptiles,  373,  411,  417,  419,  423,  428. 

sea  cows,  720. 

seals,  691. 

snakes,  41 1. 

tunicates,  64,  69. 

ungulates,  696. 

whales,  666. 
Loon,  516. 
Lophius,  214,  223,  237,  248,  253,  257, 

262. 
Lophophore,  58,  78. 
Lorenzini,  ampullae,  172. 
Lorts,  609. 
Lotka,  A.  J.,  769. 
Loxodonta,  709. 
Luminescence,  actinopterygii,  254. 

Pyrosoma,  72. 
Lunaspis,  186. 
Lungs,  see  Respiration. 

lung-fishes,  268. 
Luscinia,  522. 
Lutra,  686. 
Lymphatics,  actinopterygii,  202. 

amphibia,  338. 

birds,  471. 

dipnoi,  278. 

lamprey,  93. 
Lyriocephalus ,  407. 
Lysorophus,  361. 

Macaca,  624. 
Mackerel,  134,  246,  256. 
Macraachenia,  703. 
Macroclemmys,  398. 
Macropetalichthyida,  186. 
Macropus,  565. 
Macroscelides,  584. 
Magpie,  437. 
Maigre,  218. 
Malapterurus,  254. 

Mammals,   characteristics,   534,    574, 
767. 

classification,  532,  576. 

mesozoic,  536,  569. 

origin,  536,  569. 
Mammonteas,  716. 
Mamtnut,  716. 
Mammuthus,  716. 
Man,  633. 
Manatus,  720. 
Mandrilhis,  624. 


Sio 


INDEX 


Montis,  60 1. 

Mantipus,  302. 

Marmoset,  621. 

Marmota,  657. 

Marsupials,  538,  557,  563. 

Mauthner  cell,  101. 

Megaladapis,  610. 

Megalobatrachus,  358,  364. 

Megalohyrax,  709. 

Megapodes,  518. 

Megatherium,  596. 

Melanin,  255. 

Melanophores,  see  Chromatophores. 

Colour  change. 
Meleagris,  518. 
Meles,  686. 
Meniscotherium,  701. 
Menotyphla,  584. 
Menstruation,     607,     616,     620,     623, 

630. 
Mephitis,  686. 
Merops,  521. 
Merychippus,  736. 
Merycoidodon,  748. 
Mesichthyes,  237. 
Mesoderm,  see  Coelom. 
Mesohippus,  736. 
Mesolithic  culture,  648. 
Mesonephros,  see  Excretion. 
Mesonyx,  683. 
Mesopithecus,  626. 
Metacheiromys,  594. 
Metamerism,  see  Segmentation. 
Metamorphosis,  amphibia,  342. 

amphioxus,  44. 

Balanoglossus,  57. 

Lampetra,  118. 

tunicates,  69. 
Metapleural  folds,  28. 
Miacidae,  684. 
Microbrachis,  361. 
Microdon,  236. 
Micropodiformes,  520. 
Microsauria,  361. 
Microtus,  660. 

Migration,    actinopterygii,    205,    221, 
226. 

amphibia,  354. 

birds,  493. 

eels,  226. 

lamprey,  1 12. 

trout,  205. 
Milk,  birds,  469. 

marsupials,  561. 

monotremes,  551. 

whales,  673. 
Milk-fish,  281. 
Milvus,  459. 
Minnow,  252. 


Miobatrachus,  361. 
Mioclaenus,  700. 
Michippus,  736. 
Moa,  514. 
Mobula,  182. 
Mocking-bird,  525. 
Moeritherium,  713. 
Mola,  246. 
Mole,  565,  583,  778. 
Molgida,  62. 
Mongoose,  689. 
Monitor  lizard,  409. 
Monodon,  674. 
Monotremes,  538,  546. 
Moorhen,  518. 
Mordacia,  121. 
Mormyridae,  217,  254. 
Moropus,  731. 
Mosasaurs,  409. 
Moschops,  541. 
Moschus,  755. 
Motacilla,  521. 
Moulting,  amphibia,  298. 

birds,  434. 

mouse,  659. 
Mouse-deer,  754. 
Mouth,  actinopterygii,  193. 

agnatha,  127,  129. 

amphioxus,  30. 

Balanoglossus,  52. 

gnathostomata,  142. 

insect-eaters,  778. 

Lampetra,  88. 

origin,  142. 

tunicates,  61,  70. 
Moy-Thomas,  J.  A.,  188. 
Muco-cartilage,  86. 
Mud-skipper,  250. 
Mugil,  237. 
Muller's  fibres,  100. 
Muller's  organ,  31,  45. 
Multituberculata,  537,  547. 
Muraenosaurus,  399. 
Muridae,  659. 
Muscicapa,  523. 
Muscles,  amphibia,  302,  318. 

amphioxus,  26. 

ascidian  tadpole,  68. 

birds,  439. 

elasmobranchs,  132. 

fishes,  133,  178,  200. 

lamprey,  85. 

nomenclature  of,  319. 

reptiles,  375. 
Musk-deer,  713. 
Mustela,  686. 
Mustelus,       137,       152,       164,       170, 

181. 
Mutica,  666. 


INDEX 


811 


Myliobatis,  170,  182,  250. 
Myocomma,  amphioxus,  27. 

Lampetra,  85. 
Myogale,  584. 
Myomorpha,  656. 
Myotis,  588. 
Myotome,  actinopterygii,  200. 

amphibia,  302. 

amphioxus,  26,  28. 

ascidian  tadpole,  68. 

function  in  fishes,  133. 

Lampetra,  85,  94. 

pro-otic,  149. 
Myrmecobius,  565. 
Myrmecophaga,  596. 
Mystriosuchus,  418. 
Myxine,  109,  122. 

Nannippus,  737. 

Narzvhal,  674. 

Native  cats,  565. 

Natrix,  413. 

Neanderthal  man,  647. 

Necrolemur,  617. 

Nectophrynoid.es,  361,  366. 

Necturus,  358,  364. 

Neoceratodas,   199,  262,  268,  275,  322, 

771. 
Neognathae,  516. 
Neolithic  culture,  641. 
Neomylodon,  597. 
Neophron,  517. 

Neoteny,  see  Paedomorphosis. 
Nephridia,  35. 
Nephrotome,  94. 
Nerve  cord,  see  Spinal  cord. 
Nerve  fibres,  amphioxus,  37. 

Lampetra,  98. 

See  Conduction  velocity. 
Nerve  roots,  amphioxus,  37. 

Balanoglossus,  55. 

cephalaspida,  127. 

cranial  segmentation,  148. 

hag-fishes,  124. 

Lampetra,  97. 
Nerves,  cranial,  see  Cranial  Nerves. 
Nervous  system,  amphioxus,  36. 

Balanoglossus,  54. 

Lampetra,  97. 

polyzoa,  59. 

tunicates,  64,  69. 

See  Brain,  Spinal  cord. 
Nesomimus,  525. 
Nest-building,  112,  505,  555. 
Neural  gland,  65. 
Neuropil,  amphibia,  345. 

Lampetra,  98. 
Neuropore,  amphioxus,  39. 
Neurosecretion,  40,  208. 


Newts,  303,  364. 
Nightingale,  522. 
Nightjar,  520. 
Niobium,  62. 
Nitrate,  in  sea,  286. 
Nodosaurus,  426. 
Nose,  see  Olfactory  organ. 
Notharctus,  614. 
Nothosaurs,  399. 
Notidanoidea,  180. 
Notochord,  amphibia,  303. 

amphioxus,  27,  42. 

Balanoglossus,  51. 

Cephalodtscus,  58. 

dipnoi,  275. 

elasmobranchs,  132,  176. 

Jamoytius,  128. 

Lampetra,  86. 

La  timer  ia,  272. 

tunicates,  68. 
Notomys,  660. 
Notoryctes,  565,  778. 
Notostylops,  701. 
Nototrema,  366. 
Notoungulata,  701. 
Nucleic  acids,  8. 
Numbers,  amphibia,  297. 

birds,  432. 

fishes,  191. 

fluctuations,  663. 

horses,  739. 

man,  641. 

rodents,  663. 

species,  769. 
Numenius,  519. 
Numida,  518. 
Nycticebns,  613. 

Odobenus,  692. 

Odontognathae,  513. 

Oikopleura,  73. 

Okapi,  757. 

Olfactory  organ,  actinopterygii,  220. 

agnatha,  125,  129. 

amphibia,  333,  350. 

amphioxus,  40. 

birds,  490. 

crossopterygii,  270. 

dipnoi,  276. 

elasmobranchs,  167,  170. 

hag-fishes,  123. 

Lampetra,  108. 

mammals,  615. 

primates,  615. 

reptiles,  385. 
Oligokyphus,  544. 
Omphalosaurns,  401. 
Operculum,  184,  193,  327. 
Ophidia,  411. 


8l2 


INDEX 


Opisthocomus,  518. 

Opisthonephros,  162. 

Opossum,  563. 

Orang-utan,  626. 

Orcinus,  667. 

Oreodonta,  748,  750. 

Oreopithecus,  632. 

Organization,  evolution  of,  765,  780. 

earliest  chordates,  765. 

mammals,  767. 

vertebrates,  81. 
Ornithischia,  424. 
Ornitholestes,  423. 
Ornithomimus ,  423 . 
Ornithorhynchus,  549. 
Orogenesis,  13. 
Orohippns,  736. 
Orycteropus,  701,  704. 
Osborn,  H.  F.,  709. 
Osmoregulation,  actinopterygii,  202, 
208. 

amphibia,  340. 

birds,  474. 

earliest  chordates,  124. 

elasmobranchs,  162. 

hag-fishes,  124. 

Lampetra,  93. 

reptiles,  378,  380. 

tunicates,  63. 
Ostariophysi,  216,  237. 
Osteolepis,  268,  326. 
Osteostraci,  81,  125. 
Ostracion,  246,  249,  252,  258. 
Otter,  686. 
Ovary,  see  Reproduction,  Eggs,  Sex 

hormones. 
Ovis,  764. 
Owl,  482,  489. 
Oxen,  761. 
Oxyaena,  684. 

Pachycortnus,  236. 
Packard,  A.,  218. 
Paedomorphosis,  23,  46,  77. 

amphibia,  332,  364. 

dipnoi,  279. 

Lampetra,  120. 

man,  640,  651. 

origin  of  chordates,  77. 

tunicates,  73. 
Paenungulata,  706. 
Palaeanodonta,  594. 
Palaeodonta,  748. 
Palaeognathae,  514. 
Palaeogyrinus,  326. 
Palaeolithic  men,  648. 
Palaeomastodon,  715. 
Palaeomeryx,  755. 
Palaeoniscoidea,  228. 


Palaeospondylus,  186. 

Palaeostylops,  701. 

Palaeotherium,  732. 

Palaeotragus,  758. 

Palate,  see  Skull. 

Pan,  626. 

Pancreas,  actinopterygii,  201. 

amphibia,  343. 

elasmobranchs,  159,  167. 

lamprey,  90. 
Panda,  686. 
Pangolin,  601. 
Pantodonta,  716. 
Pantolambda,  718. 
Pantotheria,  548. 
Papio,  624. 
Parachordals,  144. 
Paracirrhites,  250. 
Paradise,  birds  of,  500. 
Parahippus,  736. 

Parallel  evolution,  see  Evolution. 
Paranthropus,  643. 
Parapithecus,  625,  632. 
Parapsida,  391,  399. 
Parasympathetic  system,  see  Auto- 
nomic nerves. 
Parathyroid,    208. 
Pareiasaurs,  390. 
Parker,  G.  H.,  41,  259. 
Parotoid  glands,  302. 
Parr,  205. 
Parrot,  477. 
Parrot  fish,  252. 
Partridge,  492,  518. 
Parns,  521. 
Passer,  521. 
Passeriformes,  521. 
Patagium,  426,  585,  592,  657. 
Pathogens,  effect  on  evolution,  784. 
Pavo,  518. 
Peacock,  500,  518. 
Pearls,  artificial,  243. 
Peccary,  749. 
Pecking  order,  493. 
Pecora,  755. 
Pecten,  484. 

Pectoral  girdle,  see  Fins,  Limbs. 
Pelecaniformes,  517. 
Pelvic  girdle,  see  Fins,  Limbs. 
Pelycosauria,  540. 
Penguins,  441,  493,  514. 
Penis,  see  Fertilization. 
Perameles,  560. 
Perch,  191,  237,  247,  252. 
Perching,  447. 
Perdix,  518. 

Pericardio-peritoneal  canal,  161. 
Pericardium,  Ciona,  63. 

elasmobranchs,  161. 


INDEX 


813 


Pericardium  (cont.) 

Lampetra,  91. 
Periophthalmus,  250. 
Periptychidae,  701. 
Perissodactyla,  722. 
Perodicticus,  613. 
Petaurista,  657. 
Petaurns,  567. 
Peters,  J.  L.,  516. 
Petrel,  517. 
Petromyzon,  121. 
Pliacochoerus,  749. 
Phalacrocorax,  517. 
Phalangers,  567. 
Pharynx,  amphioxus,  30. 

Balanoglossus ,  52. 

Cephalodiscus,  58. 

Ciona,  61. 

elasmobranchs,  145,  157. 

evolution  of,  75. 

hag-fishes,  123. 

Lampetra,  89,  1 17. 
Phascolarctos,  567. 
Pheasant,  501,  518. 
Phenacodus,  700. 
Phillipson,  A.  T.,  743. 
Phiomia,  715. 

Phobotaxis,  amphioxus,  41. 
Phoca,  691. 
Phocaena,  673. 
Phoenicopterus,  517. 
Pholidophorus,  236. 
Pholidota,  601. 
Phoronis,  49,  58,  75. 
Phororhacos,  518. 
Phosphate,  in  sea,  286. 
Photocorynus,  265. 
Photomechanical    changes,    Lampetra, 

103. 
Photoreceptors,  see  Eyes. 
Phototropism,  amphioxus,  40. 

tunicates,  64,  69. 
Phoxinus,  210,  221. 
Phrynosoma,  409. 
Phyllospondyli,  296,  361. 
Physeter,  674. 
Phytosauria,  417. 
Picus,  521. 
Pigeon,  see  Columba. 
Pigeons,  homing,  493. 
Pigments,  blood,  amphibia,  339. 

birds,  436,  470. 

Lampetra,  92. 

mammals,  604,  618. 

tunicates,  62. 
Pigs,  748. 

Pike,  237,  247,  251. 
Pilosa,  597. 
Pinaroloxias,  527. 


Pineal,  actinopterygii,  209. 

amphibia,  332,  349. 

elasmobranchs,  167. 

Lampetra,  103. 

ostracodcrms,  125,  127,  129. 

reptiles,  384,  402. 
Pinnipedia,  691. 
Pipa,  354,  360,  365. 
Pipe-fish,  237,  249,  257,  266. 
Pipistrellus,  566. 
Pipit,  521. 
Pit  vipers,  415. 
Pithecanthropus,  645. 
Pituitary,  actinopterygii,  206,  260. 

amphibia,  301,  341,  349. 

amphioxus,  40. 

birds,  469. 

elasmobranchs,  164. 

Lampetra,  96,  105. 

Latimeria,  272. 

reptiles,  410. 

tunicates,  65. 
Placenta,  aardvark,  704. 

artiodactyls,  745. 

bats,  591. 

carnivores,  683,  692. 

edentates,  596,  601. 

elephants,  713. 

fishes,  164,  266. 

hyrax,  708. 

insectivores,  582. 

marsupials,  560. 

perissodactyls,  723. 

primates,  606,  616,  620,  624,  630. 

rodents,  657. 

sea  cows,  721. 

whales,  673. 
Placentals,  origin  of,  574. 
Placodermi,  186,  772. 
Placodus,  400. 
Plaice,  237,  251. 
Planetarium,  birds  in,  494. 
Plankton,  cycles  of,  285. 
Platanista,  673. 
Platax,  257. 
Platelets,  see  Blood. 
Plateosaurus,  423. 
Platichthys,  256. 
Platynota,  409. 
Platypus,  549. 
Platyrrhina,  620. 
Platysomidae,  231. 
Plautus,  519. 
Play,  birds',  492. 
Plecotus,  589. 
Plesiadapts,  613. 
Plesianthrepus,  629. 
Plcsiosauria,  399. 
Plethodon,  299,  365. 


,i4 


INDEX 


Pleur  acanthus,  179. 
Pleurodira,  398. 
Pleuronectes,  237,  251. 
Pleurotremata,  180. 
Pliohippus,  737. 
Pliopithecus,  632. 
Plover,  519. 
Podiceps,  499. 
Poebr  other  ium,  753. 
Pogonias,  218. 
Pogonophora,  49,  60. 
Poison,  actinopterygii,  252. 

amphibia,  299,  302. 

ophidia,  412. 

reptiles,  378,  410,  583. 
Polynemus,  250. 
Polyodon,  234,  778. 
Polypedates,  360,  366. 
Polyprotodonts,  563. 
Polypterus,  39,  229,  233,  262. 
Polyzoa,  49,  58,  75. 
Pomatomus,  251. 
Pongidae,  626. 
Pongo,  626. 
Population,  birds,  431. 

bovidae,  761. 

evolution  of,  8,  782. 

fishes,  280. 

fluctuations,  663. 

horses,  739. 

man,  641. 
Porcupine,  661. 
Porcupine  fish,  252. 
Porpoise,  673. 
Portheus,  237. 
Potamochoerus,  749. 
Potamogale,  583. 
Potto,  613. 
Prairie  dog,  657. 

Predators,  influence  on  evolution,  783. 
Prepollex,  317. 
Presbytis,  625. 
Primates,  602. 
Pristiophorus,  182. 
Pristis,  162,  182. 
Proboscidea,  709. 
Procamelus,  753. 
Procavia,  708. 
Procellariiformes,  517. 
Proconsul,  632. 
Procyon,  685. 
Prolacerta,  402. 
Prolactin,  469. 
Pronation,  definition,  299. 
Pronephros,  elasmobranchs,  163. 

hag-fishes,  124. 

Lampetra,  94. 
Prong-buck,  760. 
Pro-otic  somites,  149. 


Propliopithecus,  632. 
Proprioceptors,  amphibia,  304. 

elasmobranchs,  172. 

eye-muscles,  157. 

fishes,  136. 

lamprey,  97. 
Prosimians,  608. 
Protease,  amphioxus,  32. 

elasmobranchs,  59. 

lamprey,  90. 

tunicates,  62. 
Protection,  fishes,  252. 
Proteus,  352,  358,  365. 
Protobatrachus,  361. 
Protopterus,  262,  268,  275,  308. 
Protorosaurs,  399. 
Protoselachii,  180. 
Protosiren,  721. 
Protosuchus,  421. 
Prototheria,  549. 
Protoungulata,  700. 
Protylopus,  753. 
Prunella,  522. 
Psephurus,  234. 
Pseudobranch,  260. 
Pseudoloris,  617. 
Pseudosuchia,  417. 
Pseudoteeth,  331. 
Psittaciformes,  520. 
Pteranodon,  428. 
Pteraspida,  see  Heterostraci. 
Pteraspis,  125. 
Pterichthyomorphi,  186. 
Pterobranchia,  50,  58. 
Pterois,  250. 
Pterophyllum,  248. 
Pteropus,  592. 
Pterosauria,  426. 
Ptychodera,  50. 
Ptycholepis,  234. 
Ptychozoon,  407. 
Puffinus,  493. 

PUMPHREY,  R.  J.,  482. 

Pupil,  see  Eyes. 

Pyrosoma,  72. 
Pyrotherium,  718. 

Quelea,  506. 

Rabbit,  660. 
Raccoon,  685. 
Radials,  132,  200. 
Raja,  172,  182. 
Ramapithecus ,  632. 
Rana,  298,  360,  366. 
Raphus,  519. 
Rat,  659. 
Ratites,  514. 
Rattle-snakes,  415. 


INDEX 


815 


Rays,  182. 
Redd,  205. 
Reeve,  E.  C,  598. 
Regidus,  470. 
Reissner's  fibre,  40. 
Releasers,  birds,  481,  501. 

fishes,  225. 
Rennin  in  fishes,  208. 
Reproduction,     actinopterygii,     204, 
208. 

amphibia,  341. 

amphioxus,  41. 

artiodactyls,  745. 

Balanoglossus,  56. 

bats,  591. 

birds,  472,  496. 

chelonia,  397. 

dipnoi,  278. 

earliest  chordates,  766. 

elasmobranchs,       163,       167,       180, 
181. 

elephants,  713. 

hag-fishes,  124. 

hyrax,  708. 

ichthyosaurs,  401. 

insectivores,  582. 

lampreys,  95,  112. 

man,  641. 

marsupials,  559. 

monotremes,  553. 

perissodactyls,  723. 

primates,  606,  616,  620,  623,  630. 

pterobranchs,  58. 

rate,  713,  782. 

reptiles,  380. 

rodents,  657. 

seals,  692. 

sea  cows,  721. 

trout,  204. 

tunicates,  66. 

ungulates,  697. 

whales,  673. 
Reptilia,  369,  39',  533- 
Respiration,  actinopterygii,  196. 

amphibia,  332. 

amphioxus,  34. 

Balanoglossus,  54. 

birds,  471. 

chelonia,  397. 

crocodiles,  420. 

elasmobranchs,  157,  184. 

hag-fishes,  123. 

lampreys,  89. 

reptiles,  378,  412,  420. 

seals,  692. 

snakes,  412. 

tunicates,  63. 

whales,  669. 
Rete  mirabile,  264,  670. 


Rhabdopleura,  50,  58. 
Rhachitomi,  359. 
Rhamplwrhynchns,  428. 
Rhea,  514. 
Rhineodon,  18  r. 
Rhinobatis,  180,  182. 
Rhinoceros,  728. 
Rhinolophus,  588. 
Rhipidistia,  268. 
Rhodeus,  266. 
Rhynchocephalia,  402. 
Rhynchosaurs,  404. 
Rhytina,  720. 
Ribs,  actinopterygii,  199. 

amphibia,  307. 

birds,  441. 

crocodiles,  419. 

elasmobranchs,  132. 

monotremes,  552. 

reptiles,  374,  394,  419. 

synapsids,  542. 
Rituals,  birds,  500. 
Roach,  237. 
Robertson,  J.  D.,  124. 
Robin,  437,  482,  522. 
Rodents,  652. 
Roe  deer,  715. 
Rohon-Beard  cells,  97. 
Romer,  A.  R.,  18,  341. 
Romeria,  326. 
Rook,  437,  492,  521. 
Rudd,  247. 
Ruff,  497,  502. 
Rumen,  743. 
Ruminants,  753. 

Sabre-tooths,  566,  589. 
Saccobranchas,  261. 
Saccoglossus,  50. 
Saccus  vasculosus,  39,  169. 
Sacrum,  amphibia,  307,  313. 

birds,  438. 
Salamandra,  302,  334,  358,  364. 
Salivary  glands,  amphibia,  342. 

anteaters,  593,  601. 

elasmobranchs,  158. 

lamprey,  89. 

reptiles,  378. 
Salmo,  191,  204,  237,  247,  250. 
Sal  pa,  70. 
Saltoposnchus,  417. 
Sand,  A.,  218. 
Sandpiper,  519. 
Sarcophilas,  564. 
Sauripterus,  268,  774. 
Saurischia,  422. 
Sauropoda,  423. 
Sauropsida,  371. 
Sauropterygia,  399. 


8i6 


INDEX 


Saw-fishes,  182. 
Scales,  acanthodii,  187. 

amphibia,  298,  366. 

anaspida,  127. 

birds,  432. 

cosmoid,  269. 

crocodiles,  419. 

crossopterygii,  256. 

ctenoid,  252. 

cycloid,  192,  252. 

dipnoi,  273. 

elasmobranchs,  176. 

osteolepids,  269. 

palaeoniscoid,  229. 

placoid,  129,  141,  158,  188,  252. 

pteraspida,  129. 

reptiles,  373,  411,  419. 
Scarus,  252. 
.Scent,  amphibia,  299. 
Schizocoele,  48. 

SCHOENHEIMER,  R.,  3. 

Sciaena,  218. 
Scincomorpha,  409. 
Sciuromorpha,  656. 
Scturus,  657. 
Scleromyotome,  94. 
Scolopax,  519. 
Scomber,  246,  256. 
Scorpion-fish,  250. 
Scyliorhinns,  130,  181,  250. 
:Scymnog?iathns,  542. 
Sea,  changes  in,  238. 

-cows,  720. 

-horses,  237,  246,  249,  256,  266. 

-level,  changes  of,  n. 

-lion,  692. 

-squirts,  60. 
Seal,  691. 

Segmentation,  head,  148,  155. 
Seining,  282. 
Selachii,  175. 

Semicircular    canals,    cephalaspftia, 
125. 

fishes,  216. 

hag-fishes,  109,  124. 

Lampetra,  109. 

pteraspida,  129. 
Semnopithecus,  625. 
Serranidae,  265. 
Serridentinas,  716. 
Sex  hormones,  actinopterygii,  266. 

amphibia,  341. 

birds,  476. 

elasmobranchs,  167. 

lampreys,  96,  120. 
Sex  reversal,  birds,  476 
Sexual  reproduction,  see  Reproduc- 
tion, Fertilization. 
Sexual  selection,  birds,  502. 


Seymouria,  3  09,  359,  386,  539,  774. 

Sharks,  180. 

Shearwater,  493,  495. 

Sheep,  764. 

Shell,  tortoise,  373,  393. 

Sherrington,  C.  S.,  157. 

Shoaling,  fishes,  227,  281. 

Shrews,  583. 

Shrike,  470,  485,  522. 

Sicklebill,  530. 

Sign  stimuli,  480,  501. 

Silurus,  218,  237. 

Simia,  626. 

Simpson,  G.  G.,  546. 

Sinanthropus,  645. 

Sinopa,  684. 

Siren,  358,  365. 

Sirenia,  720. 

Sivatherium,  758. 

Size,  artiodactyls,  741. 

elephants,  709. 

eutherians,  576. 

horses,  737. 

reptiles,  421. 

whales,  666. 
Skates,  182. 
Skeleton,  amphioxus,  29. 

Balanoglossus,  51. 

Lampetra,  85. 

See  Vertebrae,  Skull,  Limbs. 
Skin,  actinopterygii,  192. 

amphibia,  298,  349,  352. 

amphioxus,  29. 

Balanoglossus,  51. 

birds,  432. 

elasmobranchs,  141. 

lamprey,  84. 

primates,  624. 

reptiles,  373. 

rhinoceros,  728. 

sexual,  624. 

tunicates,  60. 

whales,  667. 
Skull,  acanthodii,  187. 

actinopterygii,  193. 

amphibia,  325,  332. 

ant-eaters,  597. 

Archaeopteryx,  513. 

artiodactyls,  741. 

bird,  464. 

carnivora,  682. 

chelonia,  394. 

crocodiles,  419. 

development,  144. 

dipnoi,  272. 

edentata,  597. 

elasmobranchs,  142. 

elephant,  709. 

eosuchia,  402. 


INDEX 


817 


Skull  (cotit.) 

frog,  328. 

horse,  695. 

insectivores,  582. 

kinesis,  272,  377,  412. 

lamprey,  87. 

Latimeria,  272. 

man,  637,  650. 

marsupials,  557. 

monotremes,  551. 

morphology,  142,  195,  230. 

ophidia,  411. 

osteolepis,  269,  325. 

palaeoniscoidea,  230. 

primates,  605,  618,  637. 

ratites,  514. 

reptiles,  375,  391,  402,  411,  417. 

rhinoceros,  728. 

rodents,  657. 

Sphenodon,  402. 

squamata,  405. 

stegocephalia,  325. 

sturgeon,  234. 

synapsida,  539. 

tapir,  727. 

whales,  668. 
Skunk,  686. 
Sloth,  599. 
Smilodon,  688. 
Sminthopsis,  565. 
Snipe,  519. 
Social  behaviour,  artiodactyls,  745. 

birds,  492. 

carnivores,  681. 

cervidae,  757. 

elephants,  713. 

fishes,  227. 

man,  613. 

primates,  610,  616,  621,  624,  630. 

rodents,  657. 

snakes,  401. 

ungulates,  697. 

whales,  672. 
Solar  radiation,  variations  of,  15. 
Solea,  237,  251. 
Solenodon,  583. 
Song,  birds',  497. 
Sorex,  584. 

Sound  production,  see  Voice. 
Sparidae,  265. 
Sparrow,  521. 
Species,  definition,  122. 
Species  formation,  birds,  524. 

Lampetra,  119. 
Sperm,  whale,  674. 
Spheniscus,  514. 
Sphenodon,  380,  384,  402,  772. 
Sphyraena,  251. 
Spider  monkey,  620. 


Spinal  cord,  amphibia,  344. 

amphioxus,  37. 

Balanoglossns ,  54. 

function  in  fishes,  136. 

Lampetra,  97. 

tunicates,  69,  74. 
Spinal  nerves,  amphibia,  345. 

amphioxus,  37. 

cyclostomes,  97. 

elasmobranchs,  148,  173. 
Spinax,  254. 
Spiralia,  48. 
Spleen,  see  Blood. 
Spurway,  H.,  783. 
Squaloidea,  182. 
Squalus,  182. 
Squamata,  404. 
Squatina,  182. 
Squirrel,  657. 

Star-gazer,  see  Uranoscopus. 
Star  navigation,  494. 
Starling,  437,  470,  492,  521. 
Statoreceptors,  see  Ear. 
Steatornis,  489. 
Stegocephalia,  296,  356. 
Stegosaurus,  425. 
Stegodon,  716. 
Stegolophodon,  716. 
Stegomastodon,  716. 
Stegoselachii,  186. 
Stensio,  E.,  127. 
Stereospondyli,  359. 
Sterna,  493. 
Sternum,  birds,  438. 
Stickleback,  225,  251. 
Stoat,  686. 
Stomach,  actinopterygii,  201,  223. 

amphibia,  342. 

artiodactyls,  743. 

birds,  468. 

camel,  743. 

edentata,  600. 

elasmobranchs,  158. 

kangaroos,  567. 

origin  of,  159. 

rabbit,  662. 

rodents,  657. 

ruminants,  699,  743. 

ungulates,  699. 

whales,  669. 
Stomochordata,  50. 
Stork,  471,  494. 
Strigiformes,  520. 
Struthio.  514. 
Struthiomimus,  423. 
Sturgeon,  234,  262. 
Sturnus,  521. 
Subholostei,  234. 
Subneural  gland,  65. 


8i8 


INDEX 


Subspecies,  birds,  524. 

Sula,  517. 

Sunfish,  246,  250. 

Sunspots,  14. 

Suprarenal,  see  Adrenal. 

Sus,  749. 

Swallow,  485,  491,  522. 

Swan,  517. 

Swift,  520. 

Swimming,  of  fishes,  133,  see  Loco- 
motion. 

Sword-fish,  249. 

Sylvia,  503,  522. 

Symbolic  actions,  birds,  501. 

Symmetrodonta,  548. 

Synapsida,  533,  539. 

Synaptosauria,  399. 

Syndactyly,  562. 

Syngnathus,  237,  249. 

Sympathetic  System,  see  Autonon- 
mic  nerves. 

Syrinx,  472. 

Tachyglossus,  549. 
Tachytely,  771. 

Tadpole,  amphibia,  298,  342,  358, 
361. 

tunicates,  67. 
Tail,  actinopterygii,  192,  233. 

amphioxus,  28. 

birds,  435,  440,  512. 

elasmobranchs,  135. 

heterocercal,  136,  234. 

homocercal,  192. 

hypocercal,  127. 

Lampetra,  84. 

Ostracoderms,  125. 

tunicates,  66. 
Talpa,  584,  778. 
Tamandua,  596. 
Tanystropheus,  399. 
Tapir,  727. 
Tarpon,  250. 
Tarrassius,  233. 
Tar  sins,  614. 

Tarsus,  314,  see  Limbs. 
Tasmanian  wolf,  564. 
Taste,  actinopterygii,  211,  220. 

amphibia,  342,  350. 

birds,  490. 

elasmobranchs,  170. 
Taurotragns ,  762. 
Teeth,  aardvark,  704. 

acanthodii,  187. 

actinopterygii,  196. 

amphibia,  327,  342. 

artiodactyls,  697,  743. 

brachydont,  698. 

brontotheres,  730. 


bunodont,  698. 

carnivores,  681,  691. 

crossopterygians,  270. 

cusp  pattern,  548. 

dinosaurs,  424. 

dipnoi,  273. 

edentata,  594. 

elasmobranchs,  142,  158,  176,  180. 

elephants,  710. 

eutherians,  575. 

horses,  732. 

hypsodont,  698. 

hyrax,  708. 

insectivores,  582. 

kangaroos,  542. 

lamprey,  89. 

Latimeria,  272. 

lophodont,  698. 

mammalia,  548. 

man,  638. 

marsupials,  558,  566. 

perissodactyls,  697,  722. 

pinnepedes,  691. 

platypus,  549. 

primates,  606,  611,  618,  623,  629,  638. 

pseudoteeth,  331. 

replacement,  158. 

reptiles,  378,  408,  417,  424. 

rodents,  655. 

sea-cows,  721. 

snakes,  412. 

synapsids,  540,  542. 

tapir,  727. 

ungulates,  697. 

whales,  674. 
Teleostei,  225. 

Temperature  receptors,  172,  415. 
Temperature  regulation,   amphibia, 
299. 

bats,  587. 

birds,  431,  471. 

edentates,  594. 

mammals,  534. 

monotremes,  553. 

reptiles,  372,  430,  540. 

whales,  669. 
Tench,  256. 
Tenrec,  583. 
Tern,  arctic,  493,  495. 
Territory,  birds,  503. 
Tertiary,  divisions  of,  571. 
Testis,  see  Fertilization,  Reproduc- 
tion. 
Testndo,  380,  393,  396. 
Tetraclaenodon,  701. 
Thaliacea,  70. 
Thecodontia,  418. 
Thelodonta,  129. 
Therapsida,  541. 


INDEX 


819 


Theriodontia,  541. 

Theromorpha,  540. 

Theropoda,  423. 

Theropsida,  371. 

Thoatherium,  703,  781. 

Thread-fish,  250. 

Thrush,  437,  466,  522. 

Thylacinas,  564. 

Thylacoleo,  568. 

Thylacosmilus,  566. 

Thynnus,  250. 

Thyroid  gland,  actinopterygii,  207. 

elasmobranchs,  164. 

hag-fishes,  124. 

Lampetra,  117. 
Tiger,  690. 
Tilapia,  287. 
Time,  16. 
Tinamu,  514. 

TlNBERGEN,  N.,  480. 

Tits,  522. 
Titanotheres,  730. 
Tomistorna,  421. 
Tornaria  larva,  56. 
Torpedo,  182,  254,  258. 
Tortoiseshell,  373,  393. 
Toucan,  467. 
Tongue,  actinopterygii,  193. 

amphibia,  342. 

artiodactyls,  744. 

birds,  490. 

elasmobranchs,  158. 

lamprey,  89. 

reptiles,  378,  405,  409. 

ruminants,  743. 

squamata,  405. 
Touch,  amphibia,  350. 

bats,  589. 

birds,  435. 

fishes,  172,  212,  222. 
Toxodon,  702. 
Trabecula,  87,  144. 
Trachinus,  252,  258. 
Trachodonts,  424. 
Tragulus,  754. 
Trawling,  282. 
Tree-creeper,  521. 
Tree-shrews,  584. 
Triassochelys,  390,  395,  398. 
Tricentes,  683. 
Triceratops,  426. 
Trichosurus,  567. 
Triconodonta,  546. 
Trigger-fish,  253,  258. 
Trigla,  211,  237,  250. 
Trilophodon,  715. 
Trionyx,  395,  396. 
Trituberculata,  548. 
Triturus,  303,  358,  365. 


Tritylodon,  544. 

Trochilus,  520. 

Trochophore  larva,  49. 

Troglodytes,  497,  522. 

Trophonemata,  164. 

Trout,  191. 

Trunk  fishes,  246,  249,  252,  258. 

Trygon,  162,  164,  182. 

Tuatara,  402. 

Tubulidentata,  704. 

Tunicata,  60. 

Tunicin,  60. 

Tunny,  250. 

Tupaia,  584. 

Turacou,  colour,  436. 

Turbot,  265. 

Turdus,  437,  466,  522. 

Turkey,  501,  518. 

Tursiops,  672. 

Turtles,  392. 

Tylopoda,  751. 

Tylosaurus,  409. 

Tylotriton,  332. 

Typhlomolge,  358,  365. 

Typhlonectes,  366. 

Typhlops,  413. 

Tyrannosaurus,  423. 

Tyto,  520. 

Uintatherium,  718. 
Ultimobranchial  gland,  208. 
Undina,  268. 
Ungulata,  694. 

Uranoscopus,  zit,,  222,  249,  253. 
Urea,  in  blood,  162,  341. 
Uria,  519. 

Uric  acid,  birds,  474. 
Urinogenital  system,  actinopterygii, 
202. 

amphibia,  340. 

birds,  474. 

chelonia,  397. 

dipnoi,  278. 

elasmobranchs,  162. 

hag-fishes,  124. 

lamprey,  93. 

marsupials,  559. 

monotremes,  553. 

reptiles,  380. 
Urochordata,  24,  69. 
Urodela,  361,  364. 
Urohypophysis,  208. 
Uromastix,  407. 
Uropygial  gland,  432. 
Ursus,  685. 
Uterus,  see  Placenta. 

Vagina,    see    Reproduction,    Urino- 
genital system,  Fertilization. 


820 


INDEX 


Vagus  nerve,  154. 

Vampires,  588. 

Vanadium,  in  Tunicates,  62. 

Vanellus,  519. 

Varanosaurus,  540. 

V or  anus,  409. 

Veins,  see  Circulation. 

Velum,  amphioxus,  31. 

dona,  61. 

Lampetra,  89,  117. 

Pteraspis,  129. 
Vertebrae,  actinopterygii,  199. 

amphibia,  303,  357,  359. 

artiodactyls,  697,  742. 

birds,  438,  512. 

carnivores,  682. 

crocodiles,  419. 

dinosaurs,  424. 

dipnoi,  275. 

edentata,  594. 

elasmobranchs,  132. 

elephant,  712. 

giraffe,  758. 

graviportal,  697,  728,  742. 

ichthyosaurs,  401. 

lamprey,  87. 

marsupials,  558. 

monotremes,  55. 

perissodactyls,  697,  722. 

primates,  634. 

reptiles,  374,  401,  411,  424,  540. 

rhinoceros,  728. 

sea-cows,  720. 

snakes,  411. 

whales,  667. 
Vertebrata,  classification,  24,  79. 

earliest,  124,  128. 

general  features,  81. 

organization  of,  132,  765. 

origin  of,  74,  124. 
Vespertilio,  592. 
Vestibular  organs,  see  Ear. 
Vipera,  372,  382,  415. 
Visceral  arches,  see  Branchial  skele- 
ton. 
Viverridae,  689. 
Vivipary,  actinopterygii,  266. 

amphibia,  365,  366. 

elasmobranchs,  164,  167,  180,  181. 

ichthyosaurs,  401. 

marsupials,  560. 

reptiles,  382,  401,  413,  415. 

snakes,  413,  415. 
Vizcacha,  661. 
Voice,  amphibia,  334. 

birds,  472. 

fishes,  218. 


primates,  621,  633. 

reptiles,  379,  407. 

seals,  692. 

whales,  672. 
Vombatus,  568. 
Vomero-nasal  organ,  see  Jacobson's 

organ. 
Vulpavus,  684. 
Vulture,  456,  517. 

Wagtail,  521. 

Walrus,  692. 

Warbler,  494,  503,  522. 

Wart-hog,  749. 

Water,  succession  of  forms  in,  775. 

Water  balance,  see  Osmoregulation. 

Water  receptors,  354. 

Water,  return  to,  775. 

amphibia,  359. 

crocodiles,  418. 

reptiles,  409,  417,  429. 
Watson,  D.  M.  S.,  364,  709. 
Weasel,  686. 
Weaver  bird,  506. 
Weberian  ossicles,  216,  237,  265. 
Weever,  252,  258. 
Whales,  666. 
White,  E.  I.,  128. 
Whiting,  220,  237. 
Wind  tunnel,  experiments,  137,  450. 
Wing,  see  Limbs. 
Wolf,  685. 
Wombat,  568. 
Woodcock,  519. 
Woodpecker,  435,  521. 
Woodpecker  finch,  467. 
Wrasse,  251. 
Wren,  497,  522. 
Wright,  S.,  530. 

Xenarthra,  594. 

Xenopus,  313,  341,  354,  360,  365. 

Xiphias,  249. 

Yak,  763. 
Yaleosaurus,  423. 
Youngina,  402. 

Zaglossus,  550. 
Zalambdalestes,  584. 
Zebra,  774. 
Zeiiglodon,  675. 
Zeus,  237,  248. 
Zinjanthropus,  645. 
Zoarces,  266. 

Zoogeographical  regions,  572. 
Zygolophodon,  716.