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A  NEW  SERIES   OF  PLANT   SCIENCE  BOOKS 

edited  by  Frans  Verdoorn 

Volume  IX 


THE  CARNIVOROUS  PLANTS 


Francis  Ernest  Lloyd  u/as  born  in  1868  0}  Welsh 
parentage  in  Manchester,  England,  coming  to  the  United 
States  in  1882.  After  graduation  at  Princeton  in  i8gi,  he 
taught  at  Pacific  University  in  Oregon  for  five  years  and 
was  then  appointed  Associate  Professor  of  Biology  at 
Teachers  College,  Columbia  University.  During  this  period 
of  ten  years  he  studied  with  Goebel  {Munich)  and  Stras- 
BURGER  {Bonn).  In  IQ06  he  became  Investigator,  ap- 
pointed by  the  Carnegie  Institution  of  Washington  to  work 
at  the  Desert  Laboratory  at  Tucson,  Ariz.  Research  here 
resulted  in  The  Physiology  of  Stomata  {Cam.  hist.  Publ. 
no.  S3).  He  then  entered  into  a  contract  with  the  Con- 
tinental-Mexican Rubber  Company  of  New  York  to  study 
the  biology  of  guayule  {Parlhenium  argentatum)  in  the 
state  of  Zacatecas,  Mexico,  and  in  igii  the  book  on  Gua- 
yule, a  Rubber  Plant  of  the  Chihuahuan  Desert  ap- 
peared {Carnegie  Institution  Publication  no.  ijg;  reissued 
in  IP42).  After  four  years  as  Professor  of  Botany  in  the 
Alabama  Polytechnic  Institute,  where  he  studied  boll-shedding 
in  cotton  (Environmental  Changes  and  their  Effect  on 
Boll-Shedding  in  Cotton,  Gossj^iium  herbaceum,  Ann. 
N.  Y.  Acad.  Sci.  zg:  1-131,  ig2o)  he  was  appointed  Mac- 
donald  Professor  of  Botany  in  McGill  University,  and 
Emeritus  in  igjs.  Was  chairman  of  Sect.  G.,  A.A.A.S.,  in 
ig2j;  President  of  the  American  Society  of  Plant  Physiolo- 
gists in  ig2y;  of  the  Royal  Society  of  Canada  in  igjj  atid  of 
the  Botanical  Section  of  the  British  Association  in  igj4. 
He  is  a  Barnes  Life  Member  of  the  American  Society  of 
Plant  Physiologists,  Honorary  British  Fellow  of  the  Botani- 
cal Society  of  Edinburgh,  and  has  received  the  D.Sc.  honoris 
causa, /row  the  University  of  Wales  and  from  Masaryk  Uni- 
versity. —  In  igoj  he  7narried  Mary  Elizabeth  Hart, 
formerly  Professor  of  Biology  in  The  Western  College  for 
Women,  Oxford,  Ohio. 


The 

CARNIVOROUS 

PLANTS 


BY 


Francis  Ernest  Lloyd 

D.  Sc.  L  c.  (  Wales);  F.  R.  S.  C,  F.  L.  S. 
Emeritus  Professor  of  Botany,  McGill  University 


h-^:^ 


1942 


WALTHAM.  MASS.,  U.S.A. 

PuLlisLeJ  ty  tlie  Clironica  Botanica  Company 


First  published  MCMXLII 

By  the  Chronica  Botanica  Company 

of  Waltham,  Mass.,  U.  S.  A. 


All  rights  reserved 


New  York,  N.  Y.:    G.  E.  Stechert  and  Co., 
31  East  loth  Street. 

San  Francisco,  Cal.:   J.  W.  Stacey,  Inc., 
236-238  Flood  Building. 

Toronto  2:    Wm.  Dawson  Subscription  Service,  Ltd., 
70  King  Street,  East. 

Mexico,  D.  F.:    Livrarla  Cervantes, 
Calle  de  57  No.   i,  Despacho  3;    Ap.  2302. 

Rio  de  Janeiro:    Livraria  Kosmos, 
Caixa  Postal  3481. 

Buenos  Aires:    Acme  Agency, 
Bartolome  Mitre  552. 

Santiago  de  Chile:    Livraria  Zamorano  y  Caperan, 

Casilla  362.. 

London,  W.  1:    Wm.  Dawson  and  Sons,  Ltd., 
43  Weymouth  Street. 

Moscow:    Mezhdunarodnaja  Kniga, 
Kouznetski  Most  18. 

Calcutta:    Macmillan  and  Co.,  Ltd., 
294  Bow  Bazar  Street. 

Johannesburg:   Juta  and  Co.,  Ltd., 
43  Pritchard  Street. 

Sydney:    Angus  and  Robertson,  Ltd., 
89  Castlereagh  Street. 


Made  and  printed  in  the  U.S.A. 


V\    1 


PREFACE 

The  experience  which  has  led  to  the  writing  of  this  book  began  in  ig2g 
when,  examining  a  species  related  to  Utricularia  gibba,  /  made  an  observation 
of  some  importance  in  understanding  the  mechanism  of  the  trap.  This  begot 
a  desire  to  study  as  many  other  species  of  the  genus  as  I  could  obtain  for  com- 
parison, primarily  to  determine  the  validity  of  my  conclusions.  My  feeling 
that  research  in  this  field  was  promising  was  strengthened  by  the  discovery  that 
the  pertinent  literature  was  singularly  barren  of  the  information  most  needed, 
that  is  to  say,  precise  accounts  of  the  structure  of  the  entrance  mechanisms  of 
the  traps.  And  an  examination  of  much  herbarium  material,  because  of  the 
meagreness  of  the  underground  parts  of  the  terrestrial  types  resulting  from 
indifferent  methods  of  collection,  forced  the  conclusion  that,  even  had  other 
difficulties  inherent  in  studying  dried  material  not  intervened,  it  would  be 
necessary  to  obtain  adequately  preserved  specimens.  This  meant  a  wide  corre- 
spondence and,  if  possible,  extensive  travel.  The  uncertainty  of  achieving  the 
latter  made  the  former  imperative. 

The  responses  to  my  requests  for  help  were  numerous  and  generous  from 
all  parts  of  the  world,  with  the  result  that  there  came  to  me  from  many  sources 
well  preserved  material  which  fairly  represented  the  genus,  for  it  brought  to  me 
some  100  of  the  total  of  2jo  or  more  species.  The  most  lavish  single  contribu- 
tion was  put  at  my  disposal  by  my  teacher  and  friend,  Karl  von  Goebel, 
who  gave  me  a  collection  of  Utricularia  collected  by  him  in  the  tropics  of  the  Old 
and  New  Worlds,  and  in  temperate  Australia.  Many  others,  while  they  may 
have  contributed  less  in  amount,  could  have  been  no  less  generous,  for  the  work 
of  collecting,  preserving,  packing  and  posting  specimens  is  by  no  means  an 
easy  job. 

Travels  included  two  journeys,  one  to  Africa  and  one  to  Africa  and  Aus- 
tralia, the  latter  made  possible  by  a  parting  gift  from  my  colleagues  of  McGill 
University  on  my  retirement  from  the  Macdonald  Chair  of  Botany  in  igjj. 
At  the  university  centres  visited  I  was  afforded  all  kinds  of  help:  laboratory 
space,  guidance  to  promising  localities  and  means  of  transportation.  Several 
summers  were  spent  also  at  the  Botanical  Institute  of  the  University  of  Munich 
on  the  original  invitation  of  Professor  Goebel,  seconded,  after  his  death,  by 
Professor  F.  von  Wettstein  and  his  successor  Dr.  F.  C.  von  Faber. 

During  my  preoccupation  with  Utricularia  /  had  to  prepare  two  presi- 
dential addresses,  and  I  was  thus  led,  as  has  many  another  in  like  circum- 
stances, to  give  an  account  of  the  whole  field  of  plant  carnivory.  My  interests 
were  widened  in  this  way,  and  soon  I  became  imbued  with  the  idea  of  bringing 
together,  and  perhaps  of  adding  to,  our  knowledge  of  this  fascinating  group  of 
plants.  This  extended  my  list  of  desiderata.  On  my  requests  sent  to  various 
correspondents  I  received  material  of  every  group,  some  living,  some  preserved, 
e.g.,  living  material  of  Heliamphora  nutans  from  the  Edinburgh  Botanical 
Garden,  where  also  I  saw  and  studied  Cephalotus. 

On  the  study  of  the  material  received  from  many  sources,  therefore,  the  ac- 
counts in  this  book  rest,  and  not,  in  the  first  instance,  on  the  published  papers 


Francis  E.  Lloyd  —  viii  —  Carnivorous  Plants 

of  the  many  excellent  workers  who  have  busied  themselves  in  this  field,  excepting, 
however,  the  studies  oj  fungi,  of  digestion  and,  in  some  forms,  of  motility. 

In  view  of  so  much  help  I  cannot  forbear  from  making  some,  if  inadequate, 
acknowledgement:  — 

First  of  all  I  should  acknowledge  the  hospitality  of  the  botanical  stafifs  of  the  Uni- 
versities visited  and  made  use  of  as  centers  of  activity  during  my  travels.  At  the  Edin- 
burgh Botanical  Garden,  Sir  William  Wright  Smith,  Mr.  M.  Y.  Orr  and  Dr.  J.  M. 
Cowan  (who  helped  me  by  raising  seedhngs  of  Utricularia);  at  the  Royal  College  of 
Surgeons,  my  friend  Dr.  J.  Beattie;  at  the  University  of  Capetown,  Miss  E.  L.  Stephens 
who  has  been  a  constant  help  for  some  years.  My  stay  there  was  made  profitable  by 
the  practical  assistance  in  transportation  and  guidance  afforded  by  Mrs.  Frank  Bolus, 
Professor  R.  H.  Compton,  Mrs.  M.  R.  Levyns  and  Mr.  A.  J.  M.  Middlemost;  at  Bris- 
bane University,  Professor  D.  A.  Herbert  and  Mr.  C.  T.  White;  at  the  University  of 
New  South  Wales,  Sydney,  Professor  John  McLuckie,  Dr.  Pat  Brough,  Professor  I.  V. 
Newman  (now  of  the  University  at  Wellington,  N.  Z.)  and  other  members  of  the  staff; 
at  the  University  in  Melbourne,  the  late  Professor  A.  J.  Ewart  and  Miss  Ethel  I.  Mc- 
Lennan; at  the  Melbourne  Herbarium,  the  late  Director  Mr.  F.  J.  Rae  and  Mr.  P.  F. 
Morris;  at  the  University  of  Adelaide,  Dr.  A.  E.  V.  Richardson  (of  the  Australian 
National  Research  Council)  and  Professor  J.  G.  Wood;  and  at  Perth,  Professor  J.  C. 
Armstrong  and  Miss  Alison  Baird;  at  the  Western  Australian  State  Herbarium,  Dr. 
C.  A.  Gardner.  Without  their  knowledge  of  local  conditions  and  immediate  assistance, 
always  put  promptly  at  my  disposal,  my  work  would  have  been  much  delayed  and  always 
less  fruitful. 

To  those  who  as  individuals  have  given  me  various  forms  of  help,  often   involving 
much  effort,  I  offer  these  mere  thanks  into  which  I  ask^them  to  read  my  highest  appre- 
ciation.   Dr.  J.  W.  Adams,  Morris  Arboretum;    Dr.  A.  Akerman,  Svalov;    Miss  E.  Bea- 
trice Ashcroft,  Auckland  University  College;   Dr.  Joji  Ashida,  Ky6t6;   Professor  L.  G. 
M.  Baas  Becking,  Leiden  and  Buitenzorg;    the  late  Professor  Edward  Barnes,  Madras 
Christian   College,   India;     Mr.    Charles    Barrett,    Editor,    The    Victorian    Naturalist, 
Melbourne;    the  late   Mr.   H.   Blatter,   Panchgani,   India;    Professor    Y.    Bh.\radwaja, 
Benares  Hindu  University;    Dr.  K.  Biswas,  Botanic  Gardens,  Sibpur  near  Calcutta;    the 
late  Dr.  H.  R.  Briton-Jones,  Trinidad;    Mr.  J.  H.  Buzacott,  Maringa,  N.  Queensland; 
Mr.   E.  J.  H.   Corner,   Botanic  Gardens,   Singapore;    Miss  Lucy  M.   Cranwell,  The 
Museum,  Auckland,  N.  Z.;   Dr.  J.  M.  Curry,  Health  Department,  Panama  (Canal  Zone); 
Mr.  F.  C.  Deighton,  Department  of  Agriculture,  Sierra  Leone;    Professor  H.  H.  Dixon, 
Trinity  College,  Dublin;   Mr.  Wm.  Dunstan,  Manager,  The  Herald,  Melbourne;   Dr.  J.  H. 
Ehlers,  University  of  Michigan,  Ann  Arbor,  Mich.;    Miss   Katherine  Esau,  University 
of  CaUfornia,  Davis,  Calif.;    Professor  M.  L.  Fernald,  The  Gray  Herbarium,  Harvard 
University;    Mr.  M.  Free,  Brooklyn  Botanic  Garden;    Mr.  A.  V.  Giblin,  Hobart,  Tas- 
mania;   the  late  Prof.  H.  Gluck,  Heidelberg;    Professor  T.  H.  Goodspeed,  University  of 
California;    Professor  John  E.  Holloway,  The  University,  Dunedin,  N.  Z.;    Mr.  R.  E. 
Holttum,  Botanic  Gardens,  Singapore;    Dr.  F.  C.  Hoehne,  Sao  Paulo,  Brazil;    Dr.  M. 
Homes,  The  University,   Brussels;    Mr.   F.   W.  Jane,  University  College,  London;    Dr. 
W.  Karstens,  Leiden;    Dr.  S.  B.  Kausik,  Central  College,  Bangalore,  India;    Professor 
L.  P.  Khanna,  Rangoon,  Burma;    Professor  W.   Kupper,  Botanical  Institute,  Munich; 
Mrs.  M.  H.  Lea,  Fairhope,  Ala.;    Frere  Leon,  Cuba;    Dr.  Gunnar  Lohamm.\r,  Uppsala; 
Mr.  Allan  McIntyre,  Hobart,  Tasmania;    Mr.  C.  Macnamara,  Arn  Prior,  Ont.;    Dr. 
E.   B.   Martyn,  now  of  Jamaica;    Mr.   O.   Mellingen,   Hanau,   Germany;    Dr.   E.   M. 
Merl,  Munich;    the  late  Professor  G.  E.  Nichols,  Yale  University,  New  Haven,  Conn.; 
Mr.  C.  E.  Parkinson,  Forest  Research  Institute,  Dehra  Dun,  India;    Dr.  D.  Y.  Padma- 
peruma.  Royal  College,  Colombo,  Ceylon;  the  late  Mrs.  Emily  H.  Pelloe,  Perth,  W.  A.;  Dr. 
A.  Quint ANiLHA,  The  University,  Coimbra,  Portugal,  later  of  Paris;   Mrs.  Lester  Rown- 
TREE,  Carmel,  Calif.;    Mr.  E.  O.  G.  Scott,  Launceston,  Tasmania;    Professor  em.  Geo. 
H.  Shull,  Princeton  Unversity,  Princeton,  N.  J.;   Mr.  N.  D.  Simpson,  Botanical  Garden, 
Peradeniya,  Ceylon;   Dr.  C.  M.  Smith,  De  Land,  Fla.;   Mr.  J.  H.  Smith,  Atherton,  Queens- 
land;   Mr.  H.  Steedman,  Perth,  W.  Australia;    Mr.  E.  J.  Steer,  Capetown,  S.  Africa; 
Mr.  D.  R.  Stewart,  Albany,  W.  Australia;    Dr.  G.  H.  H.  Tate,  American  Museum  of 
Natural  History,  New  York,  N.  Y.;    Professor  R.  B.  Thomson,  The  University,  Toronto, 
Ont.;    Dr.  J.  C.  Th.  Uphof,  Orlando,  Fla.;    Dr.   C.  A.  Weatherby,  Gray  Herbarium, 
and  Professor  Wm.  H.   Weston,  both  of  Harvard  University;    Dr.   Fr.  v.   Wettstein, 


Carnivorous   Plants  — -  ix  —  Preface 

K.  Wilhelm  Institut  f.  Biologic,  Dahlem;  Professor  Edgar  J.  Wherry,  University  of 
Pennsylvania,  Philadelphia,  Pa.;  Mr.  J.  Wyer,  N.  Queensland  Natural  History  Club, 
Cairns,  N.  Queensland. 

Finally  my  thanks  are  due  to  the  Carnegie  Institution  of  Washington,  at  Stanford 
University,  for  technical  help. 


From  time  to  time  during  the  last  50  or  60  years  there  have  appeared  in  various 
popular  magazines  and  newspapers  accounts  giving  more  or  less  detailed  descriptions  of 
fabulous  man-eating  trees.  The  earliest  of  these,  apparently,  is  one  which  was  written 
by  Dr.  Carle  Liche,  quoted  at  length  by  Chase  S.  Osborn  in  his  book  Madagascar, 
the  land  of  the  mafi-eating  tree.  This  lurid  title  was  used  avowedly  to  "enmesh  the  interest 
of  possible  readers",  not  to  propagate  the  faith.  A  summary  of  this  and  of  a  number  of 
other  yarns  has  been  provided  by  Sophia  Prior  in  a  bulletin  issued  by  the  Field  Museum 
of  Natural  History  in  1939.  If  the  reader  cares  to  inform  himself  concerning  this  lore, 
these  two  sources  will  set  him  on  his  way.  Miss  Prior's  paper  is  documented,  and  in- 
cludes reproduction  of  some  of  the  illustrations  which  constitute  part  of  the  original  but 
unconvincing  evidence  offered  in  the  various  accounts  reviewed  by  her.  Extensive  use 
has  been  made  of  the  Field  Museum  bulletin  by  Dr.  Abilio  Fernandes  in  an  article 
entitled  Morphologia  e  biologia  das  plantas  carnivoras  (see  under  Drosophyllum). 

An  amusing,  perhaps  also  tragic,  circumstance  is  to  be  found  described  in  Liche's 
account,  in  which  a  highly  imaginative  illustration  shows  that,  instead  of  a  native  maiden 
being  sacrificed  by  her  tribe  by  yielding  her  up  to  the  man-eating  tree  (possibly  a  ficti- 
tious kind  of  cycad),  a  beautiful  magazine  cover  blonde  was  the  Iamb  brought  to  the 
slaughter  .  .  . 

A  certain  carnivorous-plant-mindedness  shown  by  the  general  public  has  been  due 
also  to  occasional  cartoons  in  papers  and  magazines.  In  these  it  is  usually  the  flowers 
which  are  incorrectly  if  amusingly  represented  as  the  traps.  Such  contributions  to  the 
more  evanescent  literature  are  happily  intended  less  for  instruction  than  for  titillation. 
The  misconceptions  which  arise  in  this  way,  while  doing  little  harm,  awaken  curiosity, 
the  mother  of  knowledge. 

All  the  illustrations  in  this  book  are  originals,  prepared  by  the  author, 
unless  specifically  noted  otherwise.  The  names  of  authorities  in  many  cases 
are  not  accompanied  by  dates.  In  such  cases  only  a  single  publication,  to  be 
found  in  the  literature  lists,  can  be  referred  to.  Passages  in  languages  other 
than  English  have  been  translated. 

The  arrangement  of  chapters  may  appear  illogical.  The  principle  under- 
lying it  is  the  increasing  complexity  of  the  traps.  But  for  this,  the  fungi  may 
be  thought  to  appear  in  a  strange  setting. 


Finally  I  wish  to  acknowledge  assistance,  in  the  reading  of  proofs,  of  Professor  C.  B, 
VAN  NiEL,  of  Stanford  University;  of  Dr.  Mary  Mitchell  Moore  (Mrs.  A.  R.  Moore). 
and  Mrs.  F.  Verdoorn,  who  also  prepared  the  indices.  Dr.  Michael  Doudoroff, 
University  of  California,  and  the  editors  of  Chronica  Botanica  have  kindly  helped  me  in 
checking  a  number  of  references  to  the  literature. 


Caroli  Goebelii 

Praeceptoris  Illustrissimi 
Amici  Fidelis 
MEMORIAE 


CONTENTS 


INTRODUCTION 


Number  of  species,  genera i 

Geographic  distribution      i 

Kinds  of  traps  tabulated 2 


Analogs      3 

Origin,  evolution      7 

Literature      ° 


Chapter  I:  HELIAMPHORA 


Heliamphora  mdans 9 

Discovery      9 

Habitat      9 

Appearance 9 

The  pitcher 10 

Abnormal  leaves 11 

Other  species ^  ^ 

Habitat      " 


The  pitcher 12 

Drainage  slit 12 

Histology ^3 

Trichomes ^3 

Glands ^4 

Prey  and  its  fate      ^^ 

Literature      ^° 


Chapter  II:  SARRACENIA 


Original  description i7 

Known  species      .    .    .    ._ i? 

Geographical  distribution 17 

Sarracetiia  purpurea 18 

History i^ 

Pitcher 1° 

Early  ideas 18 

Distribution      

Pitcher-leaf 

Form      

Structure 

Outer  surface 

Inner  surface 20 

Leaves,  juvenile 22 

Histology 

Glands 

Trichomes 

Sarracetiia  psittacina 

Form      


19 
19 
19 
19 
20 


22 
22 
22 
23 
23 


Habitat      23 

Pitcher 24 

Development 24 

Interior  surface 25 

Sarracetiia  Conrtii 26 

Sarracetiia  ttiinor      . 26 

Sarracetiia  Druttittiotdii  .  _ 27 

Precarious  footing  for  flies      ....  29 

Sarracetiia  flava 29 

Sarracetiia  Jonesii 3° 

Leaf 30 

Morphology 3° 

Digestion 32 

Absorption 32 

Animal  inhabitants      35 

Literature      3^ 


Chapter  III:  DARLINGTONIA   CALIFORNICA 


Distribution      4° 

Habitat      4© 

Habit 40 

Leaves 4° 

Juvenile 4° 

Adult      42 

Form      42 

Color 43 

Fenestrations 43 

Entrance 43 

Structure 43 

Wing 43 

Fishtail 43 


Trichomes 44 

Glands 44 

Absorption 45 

Locus  of 45 

Pitcher  leaf 46 

Development 4" 

Digestion 4° 

Absorption 48 

Pitcher  fluid      48 

Wetting  power 48 

EnzjTnes 49 

Bacteria 49 

Literature      49 


56852 


Francis  E.  Lloyd 


Xll 


Carnivorous  Plants 


Chapter  IV: 

Geographical  distribution 51 

Habitat      Si 

General  characters 51 

Seedling S3 

Morphology S3 

Form  of  leaves      Si 

Adventitious  shoots S4 

Leaves S4 

Pitcher 55 

Form      SS 

Color      S5 

Mouth  and  lid      56 

Spur S7 

Peristome 57 

Anatomy 57 

Form,  variety  of 57 

Morphology 59 

Histology 63 

Peristome 63 

Glands 64 

Wall 65 

Anatomy 65 

Vascular  system 66 

Interior  surface 66 

Waxy  zone 66 

Digestive  zone 68 


NEPENTHES 

Digestion 69 

Pitcher  fluid 69 

Hooker 69 

Tate 70 

Rees  and  Will 70 

Gorup-Besanez 70 

Vines 70 

Dubois 71 

TiSCHUTKIN 71 

Goebel     71 

couvreur 71 

Wallace 72 

Grimm 72 

MoHNiKE 72 

Clautriau 73 

Fenner 73 

Hepburn  et  al 74 

Stern  and  Stern 74 

De  Kramer      76 

Pitcher  liquor 76 

Antisepsis      76 

Animal  life  of 77 

Folk  lore 78 

Uses 78 

Literature      79 


Chapter  V:   CEPHALOTUS  FOLLICULARIS 


Distribution 
Habit     .    . 
Habitat      . 
Leaf    .    .    . 

Foliage  . 

Pitcher  . 


81 

81 
81 
81 
81 
82 


Development 82 

Morphology 82 


Anatomy 85 

External  surface 85 

Internal  surface 85 

Glands 86 

Glandular  patches 87 

Digestion 88 

Literature      89 


Chapter  VI:  GENLISEA 


Discovery      90 

Distribution      90 

Early  studies 90 

Warming 90 

Goebel     90 

Flower 90 

Leaves 90 


Trap 91 

Prop  cells 91 

Size 92 

Form      93 

Anatomy 93 

Histology 93 

Glands 94 


Fohage 90      Literature 


94 


Chapter  VII:  BYBLIS 


Species 95 

Occurrence 95 

Appearance 95 

Systematic  position 95 

Habitat      95 

Habit 95 

Leaf 96 

Form      96 


Structure 96 

Glands 96 

Structure 96 

Functions 97 

Digestion 97 

Absorption 97 

Literature      98 


Carnivorous  Plants 


xm 


Contents 


Chapter  VIII:  DROSOPHYLLUM  LUSITANICUM 


Occurrence  .  . 
Habitat  .  .  . 
Appearance  .  . 
Habit  .  .  .  , 
Leaf 

Form      .    .    . 

CircinatioD    . 

Marcescence 


99 
99 
99 
99 
99 
99 
99 
99 


Glands loo 

Structure loo 

Secretion loi 

Digestion 102 

Cytology 103 

Recent  work 103 

QUINTANILHA I04 

Literature      105 


Chapter  IX:  PINGUICULA 

Geographical  distribution 106 

Appearance 106 

Habitat      106 

Leaves 107 

Glands 107 

Structure 107 


Darwin's  studies 107 

Movements 108 

Secretion;  Digestion 109 

Uses  of  leaves 112 

Literature      114 


Chapter  X:  DROSERA 


Species iiS 

Number 115 

Distribution      115 

Habitat 115 

Form,  habit 116 

Leaf-roots      117 

Leaf 

Unfolding  movements 117 

Form      117 

Anatomy 118 

Starch  content      119 

Tentacles 120 

Glands  of 121 

Development  of 123 

Function  of  parts 124 

Sessile  glands 125 

Function  of 126 

Absorption,  Locus  of 127 

Reproduction 129 

Seed 129 

Tubers 130 

Gemmae 131 

Leaf  buds 131 

Condition  for  incidence 133 

Polarity 134 

Carnivory      13S 

Early  observation 13S 


Mucilage 136 

Locus  of  secretion 137 

Movements  :- 

Tentacles 138 

Leaf-blade 138 

Direction  of  bending 139 

Duration  of  response 139 

Leaf -blade  and  stimulus 140 

Stimulus 

Path  of 140 

Intensity  of  (Darwin) 140 

Nature  of  stimulant 141 

Tentacles 142 

Mechanism  of  movement 142 

Specificity  of  reaction      143 

Aggregation:  Darwin,  C 145 

i5arwin,  F.,  Gardiner 146 

De  Vries 147 

Akerman 148 

coelingh     149 

Janson 151 

Homes 152 

Cytoplasm  and  nucleus 156 

Digestion,  enzymes      158 

Carnivory,  significance  of 162 

Literature 165 


Chapter  XI:   CARNIVOROUS   FUNGI 


Zoophagy  (Cordyceps) 169 

Earliest  discovery  by  Zopf 169 

Loop  snares  :- 

Swelling 170 

Adhesive 171 

Eel-bob  snare  :- 

Zoophagus,  Sommerstorffia 171 

Gicklhorn's  studies 172 


Capture  of  rhizopods  by:- 

Adhesive  alone 173 

Adhesive  organs 173 

Literature      175 


Francis  E.  Lloyd 


XIV 


Carnivorous  Plants 


Chapter  Xlla:  DIONAEA 


General  description      i77 

Discovery  by  DoBBS ■    ■    •  178 

Original  description  by  Ellis    ....  179 

Diderot 179 

Later  work 180 

Curtis,  Oudemans,  Canby  ....  180 

C.  Darwin,  Goebel 180 

Seed,  seedling 181 

Leaf 182 

Trap 182 

Cma 182 

Lobes,  posture  of 183 

Trichomes  (steUate) 183 

Glands  (digestive,  alluring)    ....  183 

Closure  of  trap 184 


Sensitive  hairs 184 

Internal  structure  of  trap 185 

Physiology 186 

Stimulus 186 

Perception,  localisation  of 187 

Mechanism  of  closure      188 

ZlEGENSPECK,  C.  DaRWIN       .     .     .  l88 

MuNK,  Batalin 189 

Brown,  Macfarlane 190 

Von  Guttenberg 191 

Ashida 192 

Haberlandt 193 

Digestion;  absorption 194 

Literature      210 


Chapter  Xllb:  ALDROVANDA 


General  description      194 

Discovery      195 

Distribution      195 

Leaf 19s 

Seed,  seedling 19S 

Mature  leaf 196 

Bristles 196 

Petiole 196 

Trap,  posture  of 197 

Development 197 

Terminology  (Ashida) 197 

Structure 197 

Trichomes,  glands 199 

Sensitive  hairs 200 

Mechanics  of  trap  movement    .    .    .  201 

Locus  of  bending      201 

Dionaea,  comparison  with  ....  202 


Recapitulation      204 

Stimuli,  responses  to 205 

Electrical 205 

Temperature  effects  on 206 

Chemical 206 

Sugar,  glycerin 206 

Neutral  salts,  acids,  alkalis    .    .    .  207 

Other  organic  substances    ....  208 

Formalin,  ether,  ethyl  alcohol    .    .  208 

Chloroform 208 

Ethyl  alcohol,  chloroform  ....  208 

Digestion;  absorption 208 

Vesicles,  interpretations  of 209 

Culture 209 

Literature      210 


Chapter  XIII:  UTRICULARIA,   BIOVULARIA   and 
POLYPOMPHOLYX 


Form  of  plant 213 

Traps,  variety  of      214 

Prey 214 

Flowers      214 

Distribution      215 

Embryology      216 

Seed 216 

Embryo 217 

Germination      217 

Ulriciilaria  capensis,  etc 217 

Uiricularia  vulgaris,  etc 218 

Utricidaria  purpurea 219 

Types  of  Utricidaria 219 

Utricidaria  vulgaris  type 219 

Freely  floating      220 

Floats 221 

Rhizoids 221 

Foliar  dimorphism 222 

Dwarf  shoots 222 

Branching;  inflorescence    ....  222 


Anchored  forms 224 

Terrestrial  forms      226 

Epiphj'tic  forms 226 

Biovularia  type. 227 

Utricidaria  purpurea  type 228 

Utricidaria  dichotoma  type 229 

Freely  floating      229 

Anchored 230 

Other  types,  according  to  trap  struc- 
ture :- 

Utricidaria  cornuta 231 

Utricidaria  caeridea      231 

Utricidaria  rosea,  Warhurgii  ....  231 

Utricidaria  orbiculata,  etc 232 

Utricidaria  simplex,  etc 232 

Utricidaria  globulariaefolia      ....  232 

Utricidaria  Kirkii 232 

Utricidaria  nana 232 

Utricidaria  Lloydii 232 

Literature 267 


Carnivorous  Plants 


XV  — 


Contents 


Chapter  XIV:  The   UTRICULARIA  TRAP 


General  description      233 

Terminology 233 

Early  ideas 234 

Benjamin  to  Cohn,  Darwin    .    .    .  234 

Later  advances 237 

Brocher,      Ekambaram,      Withy- 
combe    236 

Merl,  Czaja 238 

Hegner 240 

Watertightness  of  trap 242 

The  two  valves 242 

Anatomjf  and 

Histology 242 

Walls      243 

Glands 244 

Path  of  fluid  through  walls    ....  244 

Cytology 245 

Entrance 245 

Development 246 

Threshold      246 

Pavement      247 

Velum,  origin  of 247 


Door 248 

Histology 249 

Contact  with  threshold 250 

Relation  of  velum 251 

Sucking  in  of  prey 251 

Velum 253 

GoEBEL 254 

Roger  Fry 254 

Mechanical  types  of  trap  as  to  posture 

of  door  and  depth  of  entrance .    .  254 

Utricularia  vulgaris      254 

Utriciilaria  capensis 255 

Utricularia  monanthos 256 

Polypompholyx 257 

Varieties  of  traps  :- 

With  short  tubular  entrance      ...  257 

With  long  tubular  entrance    ....  258 

Digestion 263 

Prey  and  its  fate      265 

Appendix:  models  of  the  trap  ....  266 

Literature      267 


The  earliest  known  illustration  or  Nepenthes  (Nepenthes  mirabUis  (Lour.)  Merr.)  prom  RmiPHHJS 
Herbarium  Amboinense  5:  59  (published  in  1747,  but  drawn  in  the  second  part  o^  ™f  J7TH 
century).     The  plant  at  the  right  is  Flagellaria  indica.  -  The  vignette  on  p.  xv  ha^  been  re 
PRODUCED  prom  Clusius'  Rariorum  Plantakum  Historia(c/.  p.  ^^Y^^Z^iZ^^ll^^Z 
OE  A  Sarracenia.    The  Drosera  vignette  on  p.  271  has,  by  courtesy  of  Prof.  Baas  Decking,  been  re 

PRODUCED  from  A  PRINT,  MADE  DIRECTLY  FROM  A  i6TH  CENTURY  BLOCK  USED  FOR  DODONAEUS    HERBALS. 


INTRODUCTION 


The  purpose  of  this  book  is  to  give  an  historical  review  and  sum- 
mary of  our  present  knowledge  about  the  carnivorous  or  insectivorous 
plants,  the  former  being  the  better  term.  Of  these  there  are  about  450 
or  more  species,  representing  15  genera,  belonging,  aside  from  the 
fungi,  to  six  families,  indicated  in  the  present  table  (Table  i),  to- 
gether with  their  geographic  distribution. 


Table  i 


Family  and  genus 


No.  OF 

SPECIES 


Geographic  distribution 


S 
9 


6S 


90 


Sarraceniaceae 
Heliamphora 
Sarracenia 

Darlingtonia 

{Chrysamphora) 
Nepenthaceae 

Nepentfies 
Droseraceae 

Dionaea 

Aldrovanda 

Drosophyllum 

Drosera 
ByUidaceae 

Byhlis 
Cephalotaceae 

Cephalolus 
Lentibulariaceae 

Pingidcula 

Utricularia 

Biovularia 

Polypompholyx 

Genlisea 
Fungi  (various  genera 
with    trapping    mech- 
anisms) 

Roridula,  formerly  regarded  as  carnivorous,  has  now  been  shown 
by  me  not  to  be  so,  and  is  excluded  from  the  above  list.  The  ''man- 
eating  tree  of  Madagascar"  must  at  present  also  be  excluded,  since  the 
evidence  of  its  existence  is  elusive. 

The  table  shows  that  the  carnivorous  plants  are  divisible  into  two 
groups,  one  lot  {Sarraceniaceae  to  Cephalotaceae)  belonging  to  the  Chori- 
petalae,  the  rest  to  the  Sympetalae,  with  personate  flowers.  This  wide 
separation  is  a  remarkable  indication  that  the  carnivorous  habit  has 
arisen  among  the  higher  plants  at  two  points  at  the  fewest,  (as  well  as 
among  the  fungi),  in  the  course  of  evolution.  The  methods  of  captur- 
ing prey  are  in  some  measure  common  to  the  two  lots,  the  greatest 
height  of  specialization  having  been  reached  by  Dionaea  and  Aldro- 


30 
275 

2  (4) 
10 

20  or  more. 


British  Guiana;   Venezuela. 

Eastern   N.   America:    Labrador   to   S.  E.   United 

States  of  America. 
N.  California  and  S.  Oregon. 

Eastern  Tropics  to  Ceylon  and  Madagascar. 

North    Carolina    and    northern    South    Carolina, 

U.  S.  A. 
Europe,    India,    Japan,    Africa    and    Queensland, 

Australia. 
S.  Portugal,  S.  VV.  Spain,  Morocco. 
Ubiquitous. 

Australia,  from  N.  W.  to  S.  W. 

Australia,  extreme  S.  W. 

N.  hemisphere  in  Old  and  New  Worlds. 

Ubiquitous. 

Cuba;    eastern  S.  America. 

S.  and  S.  W.  Australia. 

W.  African  and  E.  South  American  tropics. 

Ubiquitous. 


Francis  E.  Lloyd  —  2  —  Carnivorous  Plants 

vanda  among  the  Choripetalae  and  by  Utricularia  among  the  Sympetalae. 
For  this  reason  the  arrangement  (Table  2)  which  has  been  followed  is 
that  which  groups  the  plants  according  to  the  character  of  their  trap- 
ping mechanisms,  named  for  their  obvious  analogs  among  human 
devices.  By  'active  traps'  is  meant  those  which  display  special  move- 
ments necessary  or  contributory  to  the  capture  of  prey. 


Table  2 

Kind  ( 

3F  TRAP 

Genus 

Pitfalls  (passive  traps),  the 

pitcher  plants 

Heliampkora 
Sarracenia 

Darlingtonia 

Cephalotus 

Nepenthes 

Lobster  pot  (passive 

trap) 

Genlisea 

Snares  (noose,  some 

active; 

sticky  discs,  etc.,  passive) 

Certain  Fungi 

Bird  lime  or  fly-paper  traps 
Passive 

Byblis 
Drosophyllum 

Active 

Pinguicula 
Drosera 

Steel-trap  (active) 

Dionaea 
Aldrovanda 

Mousetrap 

Utricularia 

Biovularia 

Polypompholyx 

The  above  table  mentions  merely  the  form  of  the  trap.  There  are, 
however,  other  characters  which  contribute  in  some  way  to  the  effi- 
ciency of  action.  These  include  methods  of  attracting  the  prey  by 
means  of  lures:  the  odor  of  violets  in  Sarracenia,  of  honey  in  Droso- 
phyllum, of  fungus  in  Pinguicula;  the  secretion  of  nectar  by  glands 
either  on  the  traps  or  on  parts  leading  to  them  as  in  Nepenthes,  etc. ;  the 
exhibition  of  attractive  colors  and  of  bright  fenestrations  in  Sarracenia, 
Darlingtonia,  Cephalotus;  of  brilliant  points  of  light  reflected  from 
drops  of  mucilage  in  Pinguicula,  Drosera,  etc. ;  the  secretion  of  mucilage 
in  Drosera,  etc.,  movements  of  various  degrees  of  rapidity,  as  in  Pin- 
guicula, Dactylella,  Drosera,  Dionaea  and  Utricularia.  There  are  also, 
with  few  exceptions,  means  for  digesting  the  prey  when  caught:  en- 
zymes and  acids  are  excreted.  When  these,  together  with  the  captured 
prey,  are  accumulated  in  some  sort  of  a  receptacle,  something  much 
like  the  animal  stomach  results.  Involved  in  all  this  there  are  special 
structures:  hairs,  glands,  specialized  stomata  {Cephalotus,  Nepenthes), 
waxy  excretions  (Nepenthes),  emergencies  (tentacles  of  Drosera). 

From  the  purely  physiological  point  of  view  the  carnivorous  plants 
are  concerned  in  a  somewhat  special  way  in  the  acquisition  of  nutrient 
substances  containing  protein,  possibly  vitamins  and  perhaps  the  salts 
of  potassium  and  phosphorus,  and  even  others.  In  this  way  they  re- 
ceive some  profit,  though  what  they  receive  is  no  sine  qua  non,  as  it  is 
with  many  other  plants.  As  Pfeffer  pointed  out,  many  fungi  are 
wholly  carnivorous,  as  in  the  cases  of  Cordyceps,  Empusa,  etc.  Among 
the  higher  plants  are  some  which  get  all  their  food  materials  indirectly 


Intro-  —3— duction 

through  agencies  such  as  mycorrhizal  fungi.    Our  so-called  carnivorous 
plants  are  therefore  not  peculiar  in  this  habit. 

What  then  distinguishes  the  carnivorous  plants  from  the  rest  of  the 
plant  world?  Why  should  we  still  share  the  feelings  of  the  naturalists 
of  the  1 8th  century  who  regarded  them  as  miracula  naturae?  We  do  so, 
I  think,  because  a  carnivorous  plant  in  the  sense  here  meant  is  one 
possessing  a  trap  which,  though  merely  a  constellation  of  structures  and 
functions,  many  of  them  conmion  enough  elsewhere  among  plants,  is  a 
special  organ  for  the  capture  and  digestion  of  animal  prey,  thus  turning 
the  tables  on  animals,  which  directly  or  indirectly  are  herbivorous. 

But  may  these  traps  as  such  be  regarded  as  something  unique?  The 
answer  to  this  question  must  be  sought  in  such  analogs  as  we  may  find 
among  plants  in  general. 

Pitfalls  in  the  form  of  pitchers  are  of  rather  widespread  occurrence. 
In  some  flowers  the  corolla  is  tubular  and  the  inner  surface  is  supplied 
with  downward  pointing  hairs,  and  there  is  emitted  a  luring,  if  not  al- 
luring, smell.  Flies  are  attracted  and  caught,  but  after  effecting  polli- 
nation, and  the  hairs  having  withered,  are  released  (Aristolochia).  In 
other  flowers  one  or  more  members  of  the  perianth  are  tubular  and  se- 
crete and  hold  nectar  {Aquilegia,  Marcgravia,  Delphinium).  Perhaps 
the  closest  parallel  is  found  in  the  pitcher  leaves  of  some  species  of 
Dischidia,  a  tropical  genus  of  the  old  world.  They  are  invaded  by 
adventitious  roots  from  nearby  stems  of  their  own  plant,  and  are  often 
occupied  by  ants  who  use  them  as  shelters.  Probably  in  their  native 
habitats  they  often  contain  moisture  available  for  their  invading  roots. 
An  inturned  marginal  rim  surrounding  the  narrow  mouth  reminds  one 
of  the  rim  of  the  carnivorous  pitcher,  but  it  seems  to  have  no  well 
marked  special  function.  In  some  species  of  Dischidia  the  pitchers  are 
represented  merely  by  dished  leaves  facing  each  other.  At  the  other 
extreme  Dischidia  pectinoides  has  a  double  pitcher,  one  inside  the  other, 
according  to  Goebel.  Lathraea  squamaria,  a  root  parasite  of  Europe, 
has  hollow  leaves,  the  hollow  lined  with  glands.  Goebel  regards  them 
as  reservoirs  for  reserve  stuffs.  The  upper  leaf  lobes  of  Azolla  are  also 
hollow,  but  these  are  inhabited  by  Anabaena  azollae  in  symbiotic  re- 
lationship. Among  the  liverworts  are  species  in  which  the  leaves  are 
partly  converted  into  "water  sacs"  (Goebel),  notably  Frullania 
cornigera  of  New  Zealand,  though  our  own  species  offer  sufficiently 
good  examples.  Lejeunea  behaves  similarly,  but  the  sacs  are  simpler. 
Most  impressive  are  Colura  and  Physiotum.  In  P.  majus^  occur  nearly 
closed  sacs  the  mouths  of  which  are  guarded  by  two  lips  closed  to- 
gether like  the  lips  of  a  mussel  shell  (Goebel).  Moreover  one  of  the  lips 
is  moveable,  being  provided  with  a  hinge  region,  thus  serving  as  a  valve. 
Precisely  how  this  valve  works  is  not  clear.  Goebel,  to  whose  account 
I  am  indebted,  points  out  that  such  an  arrangement  is  known  only  in 
Utricularia,  but  it  must  be  remembered  that  this  comparison  loses  some  of 
its  cogency  for  the  reason  that  Goebel  thought  the  valve  of  the  Utric- 
ularia trap  to  be  a  simple  check  valve.  There  is  no  evidence  that  these 
arrangements  in  the  liverworts  indicate  a  carnivorous  habit,  though 
they  are  inhabited,  like  any  liverwort  or  moss,  by  protozoa,  nematodes, 
etc.    That  they  are  water  holders  is  evident. 

The  common  teasel  {Dipsacus  sylvestris)  has  been  regarded  in   all 


Francis  E.  Lloyd  —  4  —  Carnivorous  Plants 

probability  to  be  a  carnivorous  plant  by  Miller  Christy  (1923). 
This  biennial  herb  is  well  known  for  its  water  catching  reservoirs  formed 
by  the  connation  of  the  opposed  leaves  at  their  bases.  A  large  plant 
attains  a  height  of  6  feet.  Eight  plants,  with  an  average  height  of  5  feet 
8  inches,  were  found  by  Christy  to  retain  an  average  of  a  half  pint  of 
water.  It  is  of  interest  to  know  that  the  teasel  for  this  reason  claimed 
the  attention  of  Turner  (1551),  who  remarked  the  catching  of  "rayne" 
and  ''dew"  (Herball,  o.iiij,  1551)  and  Gerard  (Herball,  p.  1005,  1597) 
wrote  quaintly,  as  it  now  appears  to  us,  "The  leaves  growe  foorth  of  the 
iointes  by  couples,  not  onely  opposite  or  set  one  against  an  other,  but 
also  compassing  the  stalke  about,  and  fastened  togither,  and  so  fas- 
tened that  they  hold  deaw  and  raine  water  in  manner  of  a  little  bason." 

Christy  rejects  the  ideas  that  the  primary  object  of  the  collection 
of  water  is  the  succour  of  the  plant  in  times  of  drought,  and  the  pro- 
tection of  its  nectar  from  predatory  insects.  The  presence  of  dead  in- 
sects, rendering  the  water  filthy,  seems  to  point  to  these  as  a  source  of 
nutriment.  "The  cups  undoubtedly  form  most  efficient  traps,"  Fran- 
cis Darwin  had  said.  Christy  suspected  the  water  to  have  some 
narcotizing  or  intoxicating  substance  (F.  Darwin  had  noticed  that 
beetles  drown  in  it  more  rapidly  than  in  pure  water),  and  he  further 
expressed  the  conviction  that  "the  plant  does  profit  by  the  insects 
caught  in  the  cups".  In  view  of  the  general  evidence  Christy  draws 
the  conclusion  that  the  teasel  is  a  carnivorous  plant,  but  without  ad- 
vancing any  definite  experimental  proof. 

The  lobster-pot  of  Genlisea,  though  an  exceedingly  specialized 
structure,  is  fundamentally  nothing  more  than  a  narrow  pitcher  with  its 
interior  armed  with  downward  pointing  hairs.  Even  the  curious 
method  of  holding  the  lips  of  the  narrow  slit-like  mouth  in  rigid  rela- 
tion to  each  other  by  an  adhesion  of  cells  finds  its  parallel  in  other 
situations  such  as  the  adhesions  of  algal  cells  and  those  of  mycelia. 
In  form,  the  'prop-cells'  responsible  find  a  loose  analog  in  the  cystidia 
of  Coprinus.  But,  after  all,  their  structure  and  method  of  function  is 
unique. 

The  snares  found  among  the  carnivorous  fungi  —  those  having  def- 
inite traps  —  are  more  obscure  in  their  analogies,  and,  it  would  appear, 
have  originated  within  the  group.  Apparently  unique  is  the  noose  of 
Arthrobotrys,  etc.  The  adhesive  disc  is  found  among  the  orchids,  in 
which  it  is  the  mechanism  for  attaching  the  pollinia  to  visiting  insects. 
Obviously  the  orchids  did  not  invent  this  originally  —  the  fungi  prob- 
ably did  so.  The  loop  of  the  pollinia  of  Asclepias  is  a  sort  of  noose 
snare  (Carry). 

The  snare  of  Zoophagus  is  a  variant  of  the  adhesive  disc,  but  is  re- 
markable as  a  device  resembling  in  its  manner  of  working  a  common 
fish-line  and  hook,  or  perhaps  better  an  'eel-bob.' 

The  plants  which  catch  their  prey  by  means  of  a  viscid  secretion 
are  only  a  few  of  a  multitude  of  others  that  excrete  sticky  substances 
by  which  small  insects  are  caught.  These  substances  are  in  general  of 
three  kinds:  oily  (often  aromatic),  resinous  and  mucilaginous.  Among 
the  carnivorous  plants,  only  the  last  is  found,  as  a  watery  medium  is 
the  only  one  that  can  carry  an  enzyme,  as  in  Drosera.  Adhesive  (mu- 
cilaginous or  resinous)  glands  are  very  common,  and  often  small  insects 


Intro-  —5— tiuction 

are  captured,  as,  e.g.  in  the  case  of  the  catch-fly  {Silene).  Suspecting 
that  many  such  plants  might  turn  out  to  be  carnivorous  Darwin 
investigated  the  behavior  of  some  of  them:  Saxifraga  umbrosa,  S. 
rotundijolia  (?),  Primula  sinensis,  Pelargonium  zonale,  Erica  tetralix, 
Mirabilis  longifolia  and  Nicotiana  tabacum.  But  while  he  thought  to 
have  proved  that  the  hairs  of  these  plants  can  in  some  instances  absorb 
organic  nutrients,  he  regretted  that  he  did  not  try  if  they  could  "digest 
or  render  soluble  animal  substances."  Fermi  and  Buscaglione  in  1899 
tried  some  of  these  and  still  others  {Martynia,  Hydrolea,  Sparmannia) 
for  digestion  with  negative  results,  whereas  those  of  the  recognized 
carnivorous  plants  which  they  tried  were  positive.  This  brings  into 
relief  the  fact  that  there  are  many  plants  which  resemble  our  carniv- 
orous plants  so  closely  that  we  can  decide  about  them  only  through 
experiment. 

Though  the  glands  involved  are  in  structure  similar  in  some  cases 
{Byhlis,  Pinguicula)  to  those  found  among  other  plants,  those  of  Dro- 
sophyllum  and  Drosera,  fundamentally  the  same  in  structure  in  both, 
are  unique  as  entireties.  Those  of  Drosera  are  raised  on  emergencies 
which  display  motility  in  no  respect  different,  except  perhaps  in  speed, 
from  that  of  ordinary  growth.  The  histological  elements  of  the  glands 
are  common  enough;    again  it  is  the  constellation  of  characters  which 

stands  out. 

The  most  complete  analog  to  a  carnivorous  plant  of  this  type  is  one 
which  was  until  recently  regarded  as  one  itself.  This  is  the  Roridula, 
of  which  there  are  two  species,  in  South  Africa.  I  myself  included  it 
among  the  carnivores  in  an  account  pubhshed  in  1933.  Since  that 
time,  on  receiving  material  preserved  in  formalin  from  Munich,  it  was 
at  once  apparent  that  the  secretion  which  appears  as  glistening  drop- 
lets in  the  living  plant,  was  intact  and  still  adherent  to  the  glands,  and 
could  therefore  not  be  a  mucilage.  Had  the  preservative  been  alcohol 
this  might  have  escaped  attention.  The  leaves  bear  many  tentacles 
superficially  similar  to  those  of  Drosera.  Examination  showed  them  to 
be  anatomically  quite  different,  and  that  they  exude  a  resinous  secre- 
tion. There  are  no  other  glands,  so  that  on  this  evidence  the  carniv- 
orous habit  seems  to  be  quite  excluded  (Lloyd,  1934)-  These  two 
species,  relatives  of  Drosera,  are,  like  them  and  Byblis,  used  by  certain 
insects  (certain  bugs  and  crab  spiders)  as  habitual  feeding  grounds. 
When  insects  are  freshly  caught,  they  are  attacked  for  their  body  juices. 
How  these  commensal  forms  avoid  capture  is  another  matter,  but  an 
interesting  one. 

The  trap  of  Dionaea  and  Aldrovanda,  with  its  close  resemblance  to 
a  steel-trap,  has  been,  and  still  is  regarded  by  some  as  "perhaps  the 
most  marvellous  in  the  world,"  to  quote  Morren  (1875)  who,  in  say- 
ing this,  was  only  repeating  what  Darwin  had  already  said.  It  appears 
to  be  quite  unique  when  regarded  as  a  total  mechanism.  But  an  analog, 
in  some  measure  at  any  rate,  was  suggested  by  Delpino,  quoted  by 
Hooker  in  his  Presidential  Address  at  the  meeting  of  the  British 
Association  for  the  Advancement  of  Science  in  1874.  Hooker  had 
already  described  a  plant  from  Tierra  del  Fuego  under  the  name  Caliha 
dioneaefolia  "which,"  Delpino  in  effect  remarked,  "is  so  analogous  in 
the  structure  of  its  leaves  to  Dionaea,  that  it  is  difficult  to  resist  the 


Francis  E.  Lloyd  —  6  —  Carnivorous  Plants 

conviction  that  its  structure  also  is  adapted  for  the  capture  of  small 
insects". 

Contributory  structural  features  of  these  traps  are  the  glands,  phys- 
iologically of  two  kinds,  but  of  identical  {Dionaea)  or  different  (Aldro- 
vanda)  structure,  and  the  sensitive  hairs,  which  are  local  points  of 
greater  sensitivity.  The  latter  only  are  unique  in  structure.  There  is 
also  motile  tissue  which,  startling  in  rapidity  though  its  movements 
are,  appears  to  work  in  much  the  same  way  as  that  of  tissues  exhibit- 
ing geotropic  responses,  according  to  Brown.  But  should  Caltha 
dioneaefolia,  as  Delpino  suggested,  turn  out  to  be  quite  parallel  to 
Dionaea,  it  would  only  add  another  member  to  a  very  small  unique 
group. 

A  curious  case  of  an  insect-catching  grass,  Molinia  coerulea,  briefly 
described  by  F.  Ludwig  in  1881,  may  here  be  indicated  as  an  analog, 
albeit  a  very  loose  one,  to  the  trap  of  Dionaea.  It  appears  that  this 
grass  can  catch  small  insects  between  its  paleae,  which  act  as  the  jaws 
of  a  spring  trap,  after  the  fashion  of  a  5-cent  spring  mousetrap.  It  is 
well  known  that,  during  flowering,  the  paleae  are  forcibly  separated 
by  the  swelling  lodicules,  and  are  held  there  for  the  space  of  anthesis. 
The  lodicules  then  shrink  and  allow  the  paleae  to  close.  If  now,  during 
the  period,  an  insect,  attracted  by  the  shining,  sappy  and  turgid  masses, 
attacks  them  by  biting  or  puncturing,  the  resulting  reduction  of  turgor 
is  sufficient  to  allow  the  outer  palea  to  close,  which  it  does  "with  sur- 
prising swiftness"  (Hildebrand,  fide  Ludwig)  thereby  trapping  the 
offending  insect.  This  action,  Ludwig  points  out,  disadvantages  the 
plant  in  curtailing  the  time  during  which  the  flower  would  normally 
remain  open.    No  compensating  benefit  seems  to  accrue. 

The  trap  of  Utricularia,  minute  though  it  is,  is  compared  in  the 
present  account  to  a  mousetrap.  There  are  mousetraps  and  mouse- 
traps however,  from  simple  to  complex  in  structure,  from  a  5  cent 
dead-fall  to  an  elaborate,  automatic  self-setting  one,  which  catches 
them  as  fast  as  they  come.  If  to  this  should  be  added  a  disposal  plant 
(Prof.  Tracy  I.  Storer  informs  me  that  such  a  mousetrap  has  been 
invented)  so  that  nothing  is  left  at  last  but  hair  and  bones,  the  com- 
parison would  be  fairly  complete,  especially  if  the  trap  should  work  in 
any  position  and  at  the  same  time  under  water.  These  are  constructed 
of  rigid  parts,  while  that  of  Utricularia  is  composed  of  soft,  yielding 
parts.  Previous  to  191 1,  the  Utricularia  trap  was  thought  to  be  rela- 
tively simple:  a  soft  "pitcher"  or  vesicle  guarded  by  a  simple  check- 
valve;  now  it  is  known  to  have  two  valves,  a  tripping  mechanism,  a 
spring  which  opens  the  door  (one  of  the  valves)  which  then  automati- 
cally closes,  barely  to  indicate  the  complexity  of  the  mechanism,  the 
complexity  and  perfection  of  which  are  extraordinary.  In  1891  Goebel 
said  that  the  Utricularias  are  "among  the  most  interesting  of  plant 
forms,  whether  we  view  them  from  the  point  of  view  of  their  morphol- 
ogy, anatomy  or  biology."  If  this  was  true  at  that  date,  it  is,  because 
of  the  added  knowledge  about  the  complexity  of  the  trap,  much  more 
true  now,  as  indeed  Goebel  personally  admitted  to  me  in  conversation. 

For  my  own  edification  I  have  attempted  to  indicate  the  structure 
of  a  mousetrap  which,  as  closely  as  may  be,  duplicates  the  trap  of 
Utricularia  without,  however,  hoping  for  the  reward  for  him  who  invents 


Intro-  —  7  —  duction 

a  mousetrap,  promised,  I  believe,  by  Emerson.  In  this  I  am  yielding 
to  the  importunities  of  many  of  my  friends,  whose  urgings  I  must  as- 
sume to  be  disinterested.  I  have,  somewhat  apologetically,  relegated 
the  drawings  and  description  (very  necessary  I  fear)  to  an  appendix 
to  the  chapter  on  Utricularia. 

For  such  a  mechanism  we  cannot  find  an  analog  among  other 
plants.  Though  it  has  moving  parts,  the  property  of  irritability  is  not 
used.  Particularly,  after  the  door  opens,  which  it  does  only  passively, 
it  instantly  recovers  its  original  position  all  in  1/33  second.  Though  its 
movements  are  made  possible  by  its  turgidity,  there  is  no  change  of 
turgor  —  hence  the  instant  reversibility  of  movement.  But  this  again 
depends  on  a  structure  which  finds  some  analogy  in  the  walls  of  anthers, 
but  only  a  partial  one.  Without  further  amplification  we  may  regard 
Utricularia  as  unique. 

It  is  not  without  interest  to  note  that  among  the  Lentihulariaceae 
we  find  examples  of  the  simplest  traps  (Pinguicula),  the  most  complex 
of  the  pitfall  type,  (in  the  lobster  pot  of  Genlisea),  and  the  incomparable 
trap  of  Utricularia,  whose  only  rival  is  that  of  Dionaea.  Which  of  the 
two  is  the  more  "wonderful"  (I  refer  now  to  Darwin's  statement  that 
he  thought  Dionaea  the  "  most  wonderful  plant  in  the  world  ")  will 
perhaps  be  a  matter  of  opinion,  but  the  evidence  seems  to  favor  Utricu- 
laria. 

How  all  these  traps  work  and  how  we  came  to  know  about  them, 
it  is  the  purpose  of  this  book  to  tell.  But  I  have  not  confined  myself 
to  the  traps,  for  it  seemed  necessary  to  present  an  adequate  picture  of 
the  plants  as  a  whole.  This  was  especially  true  of  Utricularia,  as,  in 
spite  of  many  studies,  a  survey  of  the  entire  genus  (and  those  of  Poly- 
pompholyx  and  Biovularia)  has  not  been  made  since  the  1891  publica- 
tion of  GoEBEL.  No  genus  more  fully  substantiates  the  saying  of 
Caruel  "La  pianta  cresce  ciascuna  alia  sua  idiosincrasia",  for  which 
allusion  I  am  indebted  to  Professor  Goebel.  The  survey  presented 
seems  to  indicate  with  some  fairness  the  extraordinary  variety  of  form 
and  behavior  of  these  plants,  but  necessarily  as  briefly  as  possible  in 
the  interest  of  space  saving. 

About  the  origin  and  evolution  of  the  carnivorous  plants,  however 
much  these  questions  may  intrigue  the  mind,  little  can  be  said,  nor 
have  I  attempted  to  discuss  them.  The  evidence  from  fossils  is  meagre, 
for  these  plants,  even  the  most  prolific  of  them,  have  seldom  been  pre- 
served. A  Utricularia  {U.  Berendii  Keilhack)  is  recorded  from  the  old- 
diluvial  of  Oberohe  (Engler  and  Prantl).  No  others,  so  far  as  I 
know,  have  been  recorded.  The  water  lilies  are  recorded  for  the  Ter- 
tiary, and  it  is  probable  that  Utricularia  was  contemporary.  The  fact 
that  they  have  originated  at  two  or  more  distinct  points  in  the  phylo- 
genetic  tree  is  of  major  importance.  How  the  highly  specialized  organs 
of  capture  could  have  evolved  seems  to  defy  our  present  knowledge. 

J.  G.  Peirce  (1926)  remarks  that  the  wide  distribution  of  the  car- 
nivorous plants  and  the  permanence  of  their  peculiar  morphological 
and  physiological  characters  mark  them  as  descendants  of  ancient 
forms,  but  we  have  to  add  that  only  some  of  them  are  widely  dis- 
tributed {Drosera,  Pinguicula,  Aldrovanda  (Old  World  only)  and  Utric- 
ularia) while  others,  though  related  in  one  taxonomic  group  or   the 


Francis  E.  Lloyd  —  8  —  Carnivorous  Plants 

other,  are  of  restricted,  sometimes  very  restricted,  distribution.  The 
two  categories  exist  side  by  side  in  that  ancient  continent,  Australia. 
Are  the  latter  young  scions  derived  from  the  more  ancient  stocks?  And 
may  we  regard  the  Australian  types  of  Utricularia  as  ancient  t3^es  and 
in  some  measure  as  analogs  of  ancient  animal  forms  of  that  continent? 
Since  we  cannot  answer  these  questions,  it  is  perhaps  as  well  to  say  no 
more. 

Literature  Cited: 

Carry,  T.  H.,  On  the  structure  and  development  of  the  g3mostegium  and  the  mode  of 

fertilization  in  ^iic/e^/a^  CorM7</j  Decaisne.    Trans.  Linn.   Soc.  London,   II,   2:173-208, 

1881-1887. 
Christy,  M.,  The  common  teasel  as  a  carnivorous  plant.    Journ.  Bot.  61:33-45,  1923. 
Cramer,   C,  tJber  die  insectenfressenden  Pflanzen.     A  lecture.     Ziirich,    14   Dec.    1876. 

Seen.     No  more  expHcit  data  given. 
Darwin,  F.,  On  the  protoplasmic  filaments  from  the  glandular  hairs  on  the  leaves  of  the 

common  teasel  {Dipsacus  sylveslris).    Quart.  Journ.  Micros.  Sci.  n.  s.  25:245-272,  1877. 
Drude,  O.,  Die  insectenfressenden  Pflanzen.     Schenk's  Handbuch  der  Botanik,  Breslau, 

1881,  1:113-146. 
Fermi  and  Buscaglione  (see  under  Utricularia). 
Franca,  C,  La  question  des  plantes  carnivores  dans  le  passe  et  dans  le  present.    Bol.  Soc. 

Brot.  1:38-57,  1922. 
Goebel,  K.,  Organographie  der  Pflanzen,  3.  Auflage,  Jena,  1928-33. 
Hooker,  J.  D.,  Address  to  the  Department  of  Zoology  and  Botany,   1874.     B.  A.  A.  S., 

Report  of  the  Forty-fourth  Meeting,  1874:102-116,  1875. 
Jones,  F.  M.,  The  most  wonderful  plant  in  the  world,  with  some  unpublished  correspon- 
dence of  Charles  Darwin.    Nat.  Hist.  23:589-596,  1923. 
Lloyd  F.  E.,  Is  Roridula  a  carnivorous  plant?    Can.  Journ.  Res.    10:780-786,  1934. 
LuDWiG,  F.,  Molinia  coerulea  als  Fliegenfangerin.     Bot.  Centralbl.  8:87,  1881. 
Morren,  Ed.,  La  theorie  des  plantes  carnivores  et  irritables.     Bull,  de  I'Acad.  Roy.  Belg. 

II,  40:1040  seq.  (seconde  edition  revue  et  amelioree  dans  Bull.  Fed.  Soc.  Hort.  1875). 
OsBORN,  C.  S.,  The  land  of  the  man-eating  tree.     Pp.  442,  New  York,  1924. 
Peirce,  J.  G.,  The  physiology  of  plants.     New  York,  1926. 
Pfeffer,  W.,  tJber  die  fleischifressenden  Pflanzen  und  iiber  die  Ernahrung  durch  Aufnahme 

der  organischen  Stoffe  iiberhaupt.  Landw.  Jahrb.  6:969-998,  1877. 
Planchon,  J.-E.,  Las  plantes  carnivores.     Rev.  des  deux  mondes,    13:231-259,   1876. 


Chapter  I 
HELIAMPHORA 

Discovery.  —  Appearance  of  H.  nutans.  —  Discovery  of  other  species.  —  Habitat.  — 
Leaf  structure.  —  Leaf  forms.  —  Comparison  of  species. 

The  genus  Heliampliora  is  based  on  a  plant,  H.  nutans,  collected  by 
ScHOMBURGK  who  found  it  growing  "in  a  marshy  savannah,  at  an  ele- 
vation of  about  6000  ft.  above  the  level  of  the  sea  on  the  mountain  of 
Roraima,"  "the  fruitful  mother  of  streams,"  on  the  borders  of  British 
Guiana.  (Bentham  1840;  Schomburgk  1841).  Im  Thurn  (1887)  de- 
scribed its  habitat  and  appearance.     " the  most  remarkable 

plant  of  the  swamp is  the  South  American  pitcher  plant,  Hel- 

ianiphora  nutans  Benth.,  which  grows  in  wide-spreading,  very  dense 
tufts  in  the  wettest  places,  but  where  the  grass  happens  not  to  be  long. 
Its  red-veined  pitcher-leaves,  its  delicate  white  flowers  raised  high  on 
red  tinted  stems,  its  sturdy  habit  of  growth,  make  it  a  pretty  little  pic- 
ture wherever  it  grows it  attains  its  full  size  and  best  de- 
velopment   up  on  the  ledges  of  the  cliff  of  Roraima  and  even 

on  the  top."     (Im  Thurn  1887). 

For  many  years  only  the  one  species,  H.  nutans  Bentham  {i  —  i),  was 
known.  The  meagre  hterature  deals  almost  solely  with  this  plant. 
Four  other  species  are  now  known.  Three  of  these  were  discovered  on 
Mt.  Duida,  Venezuela,  by  Dr.  G.  H.  H.  Tate  just  previous  to  1931, 
and  were  described  by  Dr.  H.  A.  Gleason  in  1931.  An  examination 
of  the  herbarium  material  (all  t3^e  specimens  in  the  herbarium  of  the 
New  York  Botanical  Garden)  was  made  possible  for  me  through  the 
kindness  of  Dr.  Gleason,  and  my  notes  on  these  species  have  been 
published  (1933).  A  fourth  species,  also  discovered  by  Dr.  Tate  in 
1937-8  in  the  same  general  region,  is  H.  minor  (Text  fig.  i).  The 
three  Mt.  Duida  species,  H.  Macdonaldae  (i — -2),  H.  Tyleri  and  H. 
Tatei,  are  closely  related  and  furnish  a  striking  example  of  closely 
related  species  arising  within  a  restricted  region  (Lloyd  1905).  Fur- 
ther exploration  may  show  the  genus  Heliaynphora  to  be  as  prolific 
of  species  as  the  North  American  Sarracenia,  or  even  more  so. 

Heliamphora  grows  in  a  region  of  vast  rainfall,  under  extremely  wet 
conditions  of  soil  and  air.  It  is  cultivated  only  with  difficulty,  but 
successfully  at  the  Edinburgh  Botanical  Garden,  and  I  am  indebted  to 
Sir  William  Wright  Smith  for  both  preserved  and  living  material  of 
the  species  H.  nutans,  on  which  the  present  account  is  based.  The 
name   Heliamphora  means  swamp-pitcher. 

The  accounts  of  H.  nutans  given  us  by  Zipperer  (1885),  Mac- 
farlane  (1889,  1893),  GoEBEL  (1891),  and  by  one  of  his  students, 
Krafft  (1896),  leave  Httle  to  be  added.  The  plant  consists  of  a  rosette 
of  basal  leaves  arising  from  a  strong  rootstock.  It  produces  a  simple 
racemose  inflorescence  of  white  or  pale  rose  colored  apetalous  flowers. 
The  4-6  sepals  are  ovate-acuminate  in  form,  with  numerous  stamens 
and  a  trilocular  ovary  with  a  single  style.     The  normal  mature  leaves 


Francis  E.  Lloyd  ^10  —  Carnivorous  Plants 

may  attain  a  length  of  30  cm.;  in  cultivation,  they  are  rarely  longer 
than  15  cm.  On  side  shoots  of  the  rhizome  arise  depauperate  branches 
bearing  leaves  in  various  stages  of  arrested  development  (2  —  2-4), 
which  have  been  duly  described  by  the  above  authors. 

Structure  of  the  leaf.  —  The  normal  pitcher  leaf  is  an  insect  trap  of 
the  pitfall  type.  Its  form  is  that  of  a  gracefully  curved  funnel,  widen- 
ing above  the  base  to  contract  somewhat  just  below  a  leafy  expansion, 
the  bell  (2  —  i;  Text  fig.  i).  The  apex  of  the  bell  normally  ends  in  a 
spoon-shaped,  thick- walled  structure  resembling  superficially  the  lid  of 
Nepenthes,  which  stands  upright  as  represented  by  Bentham,  and  not 
bent  forward  as  Goebel  suggested  as  a  protection  of  the  nectar  se- 
creted against  rain.  The  spoon  is  lacking  in  some  of  the  leaves  on 
plants  which  I  have  seen  growing  in  greenhouses,  where  many  of  the 
leaves  are  small  and  lacking  in  vigor,  but  seems  to  be  normally  present 
and  upright  in  position  in  wild  plants,  judging  from  a  photograph 
made  by  Tate  (Lloyd  1933). 

Mrs.  Arber  (1941)  regards  the  spoon  ("hood"  she  calls  it)  as  the 
continuation  of  the  rudimentary  curve-over  of  the  pitcher-lip.  The 
indications  of  this  curve-over  are  stated  to  be  "very  slight".  My  ma- 
terial, derived  from  the  same  source  as  hers,  shows  no  such  indication. 
To  be  sure,  the  sides  of  the  spoon  are  the  incurled  margins  of  the  leaf 
apex,  but  these  have  no  relation,  it  seems  to  me,  to  anything  corre- 
sponding to  a  putative  "outward  roll-over". 

The  flaring  bell  is  oval  in  form,  the  margins  sweeping  forward  to 
meet  at  once  or  to  run  parallel  for  a  short  distance  before  joining.  At 
this  point  they  continue  into  two  narrow  wings  running  down  the  mid- 
ventral  surface  of  the  pitcher,  toward  the  base  of  which  they  enlarge 
and  spread  to  form  a  wide  membranous  spreading  and  clasping  base. 
Above  the  wings  are  closely  approximated,  and  in  this  respect  Heliam- 
phora,  according  to  Macfarlane,  occupies  an  intermediate  position  be- 
tween Nepenthes,  with  widely  removed  wings  and  Sarracenia  and 
Darlingtonia  with  a  single  keel  (representing  fused  wings).  The  outer 
surface  of  the  pitcher  bears  numerous  twin  unicellular  trichomes  which 
have  inverted  V-shaped  spreading  arms  quite  unique  and  peculiar  to 
this  plant  (2  —  6  and  Text  fig.  i),  stomata,  and  many  minute  glands 
which  probably  secrete  nectar  (2  —  10).  These  are  numerous  on  the 
wings,  and  are  probably  part  of  a  general  lure  for  insects.  The  inner 
surface  can  be  divided  for  the  purpose  of  description  into  four  zones. 
Zone  I  (2  —  i)  is  the  spoon,  which  is  quite  smooth  on  its  concave  sur- 
face, but  here  bears  a  number  of  glands  which  are  larger  than  else- 
where, and  some  of  them  very  large,  usually  three  or  four  on  each 
flank.  These  are  nectar  glands.  Zone  2  begins  just  below  the  spoon 
and  is  indicated  by  a  dense  clothing  of  downward  pointing,  delicate 
hairs  in  great  numbers  covering  the  whole  of  the  surface  of  the  bell 
(which  occasionally  is  smooth),  and  the  upper  constricted  portion  of 
the  tubular  part  of  the  pitcher.  They  are  found  in  reduced  numbers 
for  a  short  space  just  below  the  constriction,  and  here  they  are  very 
long  and  straight.  Below  a  certain  point,  however,  the  hairiness  sud- 
denly ceases,  and  gives  way  to  the  next  zone  (3)  in  which  the  epidermis 
is  glistening  smooth.  While  in  zone  2  there  are  very  numerous  nectar 
glands,  interspersed  between  the  bases  of  the  hairs,  here  in  zone  3  there 


Chapter  I  — 11  —  Heliamphora 

are  none  at  all.  Below  the  lower  limit  of  the  smooth  area  there  be- 
gins zone  4,  which  again  is  clothed,  but  more  sparsely  than  the  bell, 
with  downwardly  directed  hairs.  These  are  very  stout  and  claw-like 
{2  —  5),  while  those  of  the  bell  are  longer  and  flexible.  Both  kinds 
are  longitudinally  ridged  with  delicate  folds  of  cuticle,  the  hairs  of  the 
bell  especially  so.  The  difference  of  stature  and  rigidity  is  related  to 
their  functions.  The  hairs  of  the  bell  afford  an  unstable  footing  for 
insects  which  are  trying  to  get  at  the  nectar  on  the  surface  between 
them,  and  their  flexibility  adds  to  the  instabihty..  while  those  in  the 
depths  of  the  pitcher  have  the  role  of  retention,  and  for  this  purpose 
the  stronger  they  are  the  better.  There  are  no  glands  in  zone  4. 
There  are  no  digestive  glands  present  in  this  trap. 

The  abnormal  leaves  on  the  reduced  side  shoots  are  of  various  forms 
{2  —  2-4).  The  base  of  the  shoot  is  enveloped  in  scale  leaves.  Fol- 
lowing these  there  may  be  underdeveloped  leaves,  described  by  Krafft, 
in  which  the  tube  is  very  slender  and  would  have  a  very  limited  func- 
tion as  a  trap,  and  acts  simply  as  a  petiole.  The  bell  is  relatively  large 
so  that  the  whole  behaves  as  nothing  more  than  a  photosynthetic  organ. 
A  spoon  is  not  developed.  The  inner  surface  of  the  blade  (bell)  is  free 
of  hairs,  but  carries  nectar  glands.  At  the  lower  limits  of  the  bell 
there  is  a  trapping  zone  of  hairs,  but  the  rest  of  the  tube  is  quite 
smooth.  It  is  to  be  noticed  that  the  "tube"  is  not  truly  such,  since  its 
edges  are  not  fused.  This  I  judge  from  Krafft's  drawing,  though  he 
does  not  state  so  specifically.  Goebel  described  a  sort  of  juvenile  leaf 
at  the  base  of  normal  shoots  consisting  of  a  closed  tube,  winged  with 
two  wings  as  in  the  normal,  but  with  a  much  reduced  bell  with  out- 
turned  edges  and  no  spoon.  Krafft  added  some  details,  pointing  out 
that  the  whole  of  the  inner  surface,  save  a  small  zone  at  the  base,  is 
lined  with  downward  pointing  hairs.  The  bell,  with  the  exception  of 
the  outturned  edges,  is  also  hairy,  but  the  spoon  —  this  is  not  evi- 
dently such,  nor  did  Goebel  recognize  it  —  is  without  hairs  or  glands. 
Goebel  described  a  still  simpler  and  more  elementary  condition  in 
leaves  seen  on  much  reduced  side  shoots.  These  were  small,  with  an 
undeveloped  bell,  and  the  tube  was  open,  though  appearing  closed  by 
the  juxtaposition  of  the  edges  of  the  leaf  margins,  or  perhaps  some- 
times closed  by  the  concrescence  or  adhesion  of  these  edges,  a  mode  of 
development  which  he  argues  is  different  from  that  of  the  normal  leaf 
which  arises  as  a  peltate  structure.  This  idea  has  been  elaborated  by 
Troll  who  generally  supports  Goebel's  thesis  that  the  tube  of  the 
pitcher  of  Sarracenia  and  Heliamphora  is  fundamentally  a  peltate  leaf. 
The  condition  of  concrescence  or  adhesion  of  the  leaf  margins  is  ac- 
tually realized  in  the  case  of  H.  Tyleri  in  its  fully  developed  normal 
leaves,    as   we    shall   see. 

The  latest  described  species,  H.  minor  Gleason  was  found  by  Dr. 
G.  H.  H.  Tate  on  Mt.  Auyan-Tepui,  Venezuela  in  December,  1937  at 
an  altitude  of  2,200  meters.  Generally  similar  to  H.  nutans,  it  differs 
in  the  more  sturdy  and  less  graceful  leaves,  10  to  12  cm.  long.  The 
spoon  is  larger  and  deeper,  and  orbicular  in  form.  The  bell  is  densely 
hairy  only  along  the  marginal  zone,  with  a  few  scattered  small  down- 
ward directed  hairs  on  the  general  surface,  with  many  nectar  glands. 
The  slight  constriction   at   the   base   of   the   bell  is  hairy,  with  slen- 


Francis  E.  Lloyd  —  12— Carnivorous  Plants 

der  hairs,  and  very  glandular.    The  twin  hairs  on  the  outer  surface  are 
finely   tuberculate    (Text   fig.    i). 

The  other  recently  described  species  H.  Tatei,  H.  Tyleri  and  H. 
Macdonaldae  (Gleason  1931)  are  tall  shrubby  plants  (4  feet),  but 
otherwise  present  only  a  few  differences  which  concern  us  here._  The 
leaf  is  in  all  three  much  elongated,  the  major  elongation  being  in  the 
bell  which  becomes  tubular,  expanding  only  at  the  top  where  it  is  sur- 
mounted by  a  rather  large  and  massive  overhanging  lip-Hke  appendage, 
which,  hke  the  spoon  in  //.  nutans,  carries  large  nectar  glands.  The 
most  divergent  of  the  three  is  H.  Macdonaldae,  in  which  the  inner  sur- 
face of  the  bell  is  quite  smooth  except  along  the  free  margin  and  for  a 
narrow  zone  at  the  lower  hmit  of  the  neck  about  2  cm.  wide.  The 
distribution  of  small  glands  on  the  outer  surface  is  much  the  same  as 
in  H.  nutans  except  that  they  do  not  occur  on  the  outer  faces  of  the 
extensive   stipular  wings. 

Glands  are  absent  from  the  interior  surface  of  the  bell  where  the 
surface  is  smooth,  while  even  when  in  H.  nutans  the  surface  of  the  bell 
is  smooth,  as  it  sometimes  is,  glands  occur  nevertheless. 

An  adaptive  feature  of  very  great  interest  is  one  reported  by  Tate  :— 

"The  question  arose as  to  how  the  pitchers,  closely  packed 

and  unable  to  bend  over  as  they  were,  maintained  a  constant  water 
level  and  succeeded  in  getting  rid  of  the  excess  water  poured  into  them 
during  the  frequent  heavy  rains.  Upon  examination  it  was  found  that 
each  leaf  had  a  small  pore  in  the  seam  (opposite  the  midrib)  placed 
just  at  the  juncture  of  the  basal  water  containing  part  of  the  pitcher 
and  the  terminal  portion,  through  which  the  excess  fluid_  might  run 
out.  This  observation  was  made  on  H.  Macdonaldae,  but  in  all  prob- 
abihty  holds  for  other  species   as  well. "  (Tate,   quoted  by   Gleason, 

1931). 

I  have  examined  the  material  collected  by  Dr.  Tate  with  much 
care  and  interest,  so  far  as  it  was  permitted,  and  I  have  found  that 
the  condition  described  above  is  to  be  found  in  its  most  pronounced 
form  in  H.  Tatei.  To  understand  the  morphology  involved  _  let  us 
compare  the  structure  of  the  leaf  with  that  of  H.  nutans,  in  which  the 
closed  tubular  portion  ends  abruptly  in  a  bell,  sht  for  a  short  dis- 
tance along  the  ventral  border,  the  margins  running  downward  as  the 
ventral  wings  as  above  described,  to  be  continued  as  the  stipular 
wings.  In  H.  Tatei  the  leaves  are  from  40  to  50  cm.  long,  and  the 
stipules,  in  accordance  with  the  shrubby  habit  of  the  plant,  are  very 
long,  clasping  the  bearing  stem  and  adjacent  leaf  bases.  The  ventral 
wings  are  short  and  fohose,  while  the  bell  is  very  long,  being  slit 
down  the  ventral  side  for  some  distance.  The  edges  of  the  trumpet 
are  here  also  confluent  with  the  ventral  wings,  but  above  the  morpho- 
logical limit  of  the  slit  they  are  concrescent  except  for  a  space  of  about 
one  centimeter  at  its  lowest  limit.  Here  the  edges  of  the  bell  remain 
free,  forming  a  short  elongated-oval  slit,  which  we  may  call  the  drain- 
slit  or  pore  (Text  fig.  i).  The  head  of  water  released  by  flowing 
through  the  slit  amounts  to  5  cm.  in  some  leaves,  or  possibly  more, 
often  less.  This  would  have  the  effect  of  lowering  the  center  of  gravity 
of  the  water  loaded  leaf  very  considerably.  In  //.  Macdonaldae,  in  a 
leaf  of  nearly  the  same  length  (37  cm.),  the  region  of  fused  edges  was 


Chapter  I 


13 


Heliamphora 


much  shorter  in  the  only  leaf  I  could  examine,  while  in  H.  Tyler i  (of 
which  I  examined  two  leaves)  there  is  but  a  shght  commissure  above 
the  drain  slit,  or  it  may  be  quite  open,  as  it  is  in  H.  nutans.  The 
length  of  the  slit  is  about  i  cm.  more  or  less,  and  has  cihated  margins, 
since  it  lies  within  the  hairy  zone  of  the  bell  near  its  lower  limit. 
Owing  to  the  fact  that  the  specimens  were  dried  and  pressed  "types", 
I  was  limited  in  my  examination.  Where  the  slit  of  the  bell  in  H. 
Macdonaldae  seemed  to  be  open,  this  may  have  been  due  to  the  sepa- 
ration of  the  fused  margins  in  drying  (Lloyd  1933). 


Fig.  I.  —  I,  Heliamphora  Tatei;  2,  H.  Macdonaldae;  3,  H.  minor,  the  zonation  of  the 
interior  surface  is  indicated  by  the  numbers  1-4;  4,  H.  minor;  5,  H.  nutans;  6,  retrorse 
hair  of  H.  minor;   7,  twin  hairs  of  H.  minor. 

It  is  quite  evident  that  the  presence  of  the  drain  slit  discovered 
by  Tate  would  render  tall  plants,  which  grow  to  the  height  of  four 
feet  and  inhabit  a  very  rainy  habitat,  far  less  top-heavy.  The  up- 
right position  of  the  leaves  is  further  assured  by  the  ample,  tightly 
clasping,  stipular  wings.  At  the  same  time  it  is  to  be  observed  that 
the  adaptation  is  not  equally  expressed  in  all  three  species,  being  least 
so  in  H.  Tyleri,  in  which  the  slit  may  not  be  present  at  all,  the  bell 
being  slit  all  the  way  down  to  the  limit  of  the  hairy  zone.  So  far  as 
the  effect  is  concerned,  this  amounts  to  the  same  thing,  since  the 
water  is  drained  off  to  the  lowest  open  point  of  the  bell  in  any  case. 

Trichomes.  —  There  are  two  kinds  of  hairs  to  be  found  on  the  inner 
surface  of  the  pitcher,  those  of  the  bell  and  adjacent  tube,  that  is  of 
the  conducting  surface  of  Hooker,  and  those  of  the  basal  portion  of 
the  tube.     They  are  of  identical  morphology,  but  differ  in  important 


Francis  E.  Lloyd  —  14  —  Carnivorous  Plants 

details  of  structure.  They  are  unicellular  hairs  with  the  bases  embed- 
ded in  a  raised  mass  of  epidermis  and  underlying  parenchyma.  They 
taper  from  the  base  gradually  to  the  sharp  tip,  and  the  cuticle  is 
raised  to  form  folds  or  ridges,  beginning  at  or  near  the  base  and  con- 
verging on  the  apex,  where  they  gradually  fade  away.  These  ridges 
are  more  pronounced  on  the  hairs  of  the  conductive  surface,  and  are 
much  weaker  to  scarcely  distinct  on  the  hairs  of  the  detentive  surface. 
The  former  are  relatively  longer,  more  slender  and  distinctly  flexible, 
the  more  so  in  the  lower  parts  of  the  conductive  surface.  Krafft 
suggested  that  these  ridges  have  use  as  strengthening  elements,  but 
the  effect  is  not  to  make  the  hairs  rigid.  They  may  make  it  more 
difficult  for  flies  to  use  their  foot  organs.  Their  chief  eflficiency  lies, 
I  imagine,  in  their  number  and  flexibility,  so  that  an  insect  cannot 
place  its  feet  on  the  bell  surface,  but  can  only  hook  onto  the  hairs 
which  by  their  flexibility  give  way  and  permit  the  insect  to  slip  into 
the  pitcher.  The  hairs  of  the  detentive  surface  on  the  other  hand 
are  short,  very  thick  walled  and  rigid,  thereby  making  escape  difficult. 
Bentham  (1840)  said  of  these  that  ''they  have  all  the  appearance  of 
ordinary  secreting  hairs,"  but  this  was  a  mistake.  They  are  cer- 
tainly not  secretory. 

The  structure  of  the  nectar  gland  of  the  pitcher  in  Heliampkora 
has  been  described,  though  not  quite  correctly,  by  Krafft  (1896). 
There  are,  for  purposes  of  description,  two  kinds:  (a)  those  which 
are  relatively  small  and  have  few  cells,  about  12  in  number  (2  —  10). 
These  are  found  scattered  over  the  whole  of  the  bell,  and  on  the  outer 
surfaces,  including  the  wings,  and  are  regarded  as  nectar  glands 
by  GoEBEL,  who  detected  a  sweetness  in  the  excreted  fluid;  and 
(b)  large  glands  found  only  on  the  inner  surface  of  the  spoon  (2  —  7). 
Krafft  spoke  of  three  kinds  of  glands,  distinguishing  those  on  the 
inner  from  those  on  the  outer  surfaces.  But  they  are  all  quite  the 
same  in  structure,  differing  somewhat  in  size,  those  on  the  outer  sur- 
faces being  shallower,  the  glandular  cells  of  a  gland  having  little  more 
depth  than  that  of  the  surrounding  epidermis. 

The  structure  of  the  smaller  glands  is  as  follows:  They  appear  in 
surface  view  to  consist  of  six  cells,  four  in  a  single  course  in  the  level 
of  the  epidermis,  covered  partially  by  two  cells,  the  "cover  cells"  of 
GoEBEL.  The  area  of  the  exposed  surface  of  the  gland  is  about  equal 
to  that  of  a  stoma.  It  is  difficult  to  resist  the  theory  that  the  glands 
are  derived  phylogenetically  from  stomata,  but  there  is  no  support 
for  this  beyond  the  suggestive  appearance  of  the  two  cover  cells. 
Beneath  the  course  of  four  cells,  there  is  a  second  inner  course  of  cells 
which  appeared  to  Krafft  to  be  four  in  number.  One  usually  can 
count  at  least  six  cells,  two  cells  lying  beneath  the  two  cover  cells. 
But  the  glands  are  of  irregular  structure,  and  one  cannot  say  definitely 
that  there  are  only  so  many  cells.  These  constitute  the  gland  proper, 
and  are  all  derived  from  the  epidermis.  They  are  surrounded  by  a 
cuticularized  membrane,  except  at  the  base,  which,  though  being 
partially  covered  with  this  membrane,  is  not  entirely  so,  there  being 
left  a  "window"  (Krafft  used  this  word),  so  that  the  active  gland 
cells  lie  in  direct  contact  with  usually  two,  sometimes  one,  or  three 
to  four,  parenchyma  cells  below. 


Chapter  I  — 15  —  HeUamphora 

The  walls  of  these  cells  which  lie  in  contact  with  those  of  the 
gland  immediately  above  (if  we  assume  an  orientation  of  up  and 
down,  the  cover  cells  being  up)  are  always  strengthened  by  curved 
thickenings  like  those  of  xylem  vessels.  Krafft  seems  to  have  re- 
garded these  cells  also  to  be  cuticularized,  and  the  wall  thickenings 
to  be  on  the  lateral  walls  in  contact  with  surrounding  parenchyma 
cells.  On  both  these  points  he  was  mistaken.  The  wall  thickenings 
are  found  on  the  walls  only  where  the  cells  impinge  on  the  gland  cells, 
and  are  not  cuticularized  in  any  part.  This  arrangement  is  found  also 
in  the  glands  of  Sarracenia,  as  Goebel  showed,  to  be  described  be- 
yond. The  function  of  these  parenchyma  cells  is  not  known,  but  it 
serves  to  call  them  transmitting  cells.  But  whether  they  do  more 
than  permit  movement  of  substances  from  the  leaf  tissues  to  the 
gland,  is  not  known.  There  is  no  reason  to  particularize  as  to  the 
distinction  between  the  glands  of  the  inner  and  outer  surfaces,  be- 
yond the  fact  that  where  the  outer  surface  glands  impinge  on  the 
underlying  parenchyma,  the  parenchyma  cells  in  immediate  contact 
are  sometimes  so  large  that  it  is  very  easy  to  recognize  the  fact  that 
the  wall  thickenings  occur  only  where  the  gland  cells  are  in  contact 
with  the  parenchyma  cells.  In  cases  where  the  section  has  run  through 
the  gland  at  right  angles  to  the  common  axis  of  the  contingent  pa- 
renchyma walls  beneath  the  gland,  it  becomes  apparent  why  cell 
walls  carrying  the  thickenings  appear  to  be  other  than  those  exactly 
in  contact  with  the  glands,  namely,  because  of  the  oblique  position. 
In  making  a  drawing  one  is  usually  forced  to  show  them  as  if  they 
were  anticHnal,  instead  of  periclinal  walls.  For  this  reason  one  can 
understand  how  Krafft  may  have  been  misled.  Viewing  the  gland 
from  beneath,  possible  in  tangential  sections,  leaves  no  doubt  about 

the  facts. 

The  glandular  cells  and  the  contingent  parenchyma  cells  were 
regarded  together  as  constituting  the  gland  by  Krafft,  and  the 
whole  was  attributed  by  him  to  an  epidermal  origin.  But  the  pa- 
renchyma cells  are  certainly  not  of  glandular  nature,  judging  by  their 
meagre  protoplasmic  contents,  and  are  of  equal  certainty  not  of  epider- 
mal origin.  One  hardly  needs  to  see  developmental  stages  to  draw 
this  conclusion.  Tenner's  account  of  the  origin  of  the  Sarracenia 
nectar  gland,  which  is  of  the  same  structure  as  that  of  HeUamphora, 
also  includes  the  parenchyma  cells. 

The  large  glands  are  found  only  on  the  inner  surface  of  the  spoon. 
Krafft  correctly  traces  this  type  of  gland  to  an  epidermal  origin, 
but  does  not  show  that  in  this  gland  also  there  are  to  be  found  the 
xylem-Hke  parenchyma  cells.  He  attributes  to  the  gland  an  identity 
with  the  large  glands  found  in  Cephalotus  which,  as  we  shall  see  when 
we  discuss  the  latter,  is  not  justified.  These  glands  occur  to  the 
number  of  about  20,  larger  and  smaller  in  size,  the  larger  ones  being 
in  a  more  lateral  position.  And  these  are  very  large.  In  surface 
view  they  consist  of  a  number  of  cover  cells  and  first  course  cells, 
underlain  by  about  four  courses  of  thick  walled  cells  beneath  which 
lies  the  mass  of  glandular  cells  proper.  The  periphery  of  this  mass 
is  irregular,  as  if  there  was  a  tendency  of  the  glandular  mass  to  branch 
or  lobe.     The   contingent   parenchyma   by   the   same   token   intrudes 


Francis  E,  Lloyd  —  16  —  Carnivorous  Plants 

cells  between  the  lobes.  So  large  are  these  glands  that  they  must 
contain  about  looo  cells.  There  are  only  a  half-dozen  such  large 
glands,  the  rest  within  the  spoon  being  of  various  sizes,  but  all  smaller 
and  showing  a  structure  more  obviously  like  that  of  the  rest  of  the 
glands  of  the  inner  and  outer  surfaces.  One  of  the  smallest  I  show 
in  Plate  2  —  7,  in  which  it  is  seen  that  some  of  the  parenchyma  cells 
in  contact  with  the  gland  have  spirally  and  reticulately  thickened  walls. 
One  finds  them  in  the  large  glands,  but  only  occasionally;  they  are 
very  difficult  to  find,  however.  In  any  event  the  wall  thickenings 
seem  to  be  less  pronounced  and  distinct.  The  large  gland  is  often 
in  close  contact  with  the  vascular  tissue. 

The  cuticularization,  as  in  the  small  glands  of  the  general  surfaces, 
extends  around  the  gland,  with,  however,  areas  furnishing  contact 
with  the  surrounding  parenchyma. 

GoEBEL  leaned  towards  the  opinion  that  the  glands  above  de- 
scribed are  different  in  structure  from  those  of  Sarracenia,  but  the 
evidence  to  be  later  deduced  will,  I  think,  show  otherwise.  Mac- 
FARLANE  described  the  glands  as  being  depressed  and  surrounded 
by  thick  walled  neighbor  cells,  "the  upper  part  of  which  may  over- 
hang" the  gland.  He  did  not  study  the  gland  structure  further, 
as  Krafft  did  later,  and  suggested  that  the  glands  of  Heliamphora 
stand  in  an  intermediate  position  between  those  of  Sarracenia  and 
those  of  Nepenthes.     This  idea  seems  lacking  in  justification. 

Prey  and  its  fate.  —  That  insects  are  caught  by  the  pitchers  of 
Heliamphora  was  not  known  to  Bentham,  who  handled  the  first  ma- 
terial to  reach  London.  I  found  insect  remains  in  the  pitchers  of 
H.  Tyleri  and  Krafft  did  so  in  the  pitchers  of  H.  nutans  sent  to  him 
from  England  by  Veitch  and  Sons.  The  odor  accompanying  decay 
of  insect  bodies  was  noticed  by  Krafft.  As  there  are  no  digestive 
glands  to  be  found,  we  must  conclude  that  the  proteins  of  animal 
bodies  are  made  available  to  the  plant  only  by  means  of  bacterial 
digestion.  That  no  work  has  been  done  on  this  plant  can  be  ex- 
plained by  the  rarity  of  the  material,  due  to  the  difficulties  of  cul- 
tivation. 

Literature  Cited: 

Arber  {see  under  Cephalotiis). 

Bentham,  G.,  Heliamphora  nutans,  a  new  pitcher  plant  from  British  Guiana.  Transact. 
Linn.  Soc.  18,  1840. 

Fenner,  C.  a.,  Beitrage  zur  Kenntnis  der  Anatomie,  Entwicklungsgeschichte  und  Biologic 
der  Laubblatter  und  Driisen  einiger  Insektivoren.     Flora  93:335-434,  1904. 

Gleason,  H.  a.  and  E.  F.  Killep,  Botanical  results  of  the  Tyler-Duida  Expedition.  Bull. 
Torr.  Bot.  Club  58:277-586,  1931. 

Gleason,  H.  A.,  Brittonia  3:164,  1939  (Description  of  Heliamphora  minor). 

GoEBEL,  K.,  Pflanzenbiologische  Schilderungen.     Marburg,  1891. 

Im  Thurn,  E.  F.  and  D.  Oliver,  The  botany  of  the  Roraima  Expedition  of  1884.  Trans. 
Linn.  Soc.  London  II,  2:249-300,  1887. 

Kraeft,  S.,  Beitrage  zur  Kenntnis  der  Sarraceniaceen-Gattung  Heliamphora.  Diss.  Mu- 
nich, 1896. 

Lloyd,  F.  E.,  Isolation  and  the  origin  of  species.     Science,  N.  S.  22:710-712,  1905. 

Lloyd,  F.  E.,  The  carnivorous  plants.     Trans.  R.  S.  C.  27:3-67,  1933. 

Macfarlane,  J.  M.,  Observations  on  some  pitchered  insectivorous  plants,  I.  Ann.  Bot. 
3:253-266,  1889;    11.  Ann.  Bot.  7:403-458,  1893. 

ScHOMBURGK,  R.  H.,  Reisen  im  Guiana  .  .  .  Leipzig  1841. 

Troll,  W.,  Morphologic  der  schildformigen  Blatter.     Planta  17:153-314,  1932. 

ZrppERER,  Paul,  Beitrag  zur  Kenntnis  der  Sarraceniaceen.     Diss.  Erlangen,  1885. 


Chapter  II 
SARRACENIA 

Discovery.  —  Known  species.  —  Descriptions  of:  5.  purpurea.  —  S.  psiUacina.  —  S. 
Courtii.  —  S.  minor.  —  S.  Drumtnondii.  —  S.  flava.  —  S.  Jonesii.  —  Morphology  of  the  leaf. 
—  Digestion  and  absorption.  —  Animal  life  of  the  pitchers. 

The  genus  Sarracenia  is  based  on  Tournefort's  original  description 
(1700)  of  a  plant  sent  to  him  by  Dr.  M.  S.  Sarrazin  from  Quebec, 
Canada.  The  name  was  adopted  by  Linnaeus  (1737).  The  earliest 
known  illustration  of  Sarracenia  is  to  be  found  in  de  l'Obel's  Nova 
Stirpium  Adversaria,  evidently  of  a  leaf  of  5.  minor,  probably  re- 
ceived from  some  Spanish  explorer  in  Florida  (p.  430,  1576  ed.).  Ac- 
cording to  Uphof  (Engler  and  Prantl,  2  ed.)  there  are  nine  species. 
Wherry  (1933)  distinguishes  between  the  northern  form  of  S.  pur- 
purea and  a  southern  form,  namely,  the  subspecies  S.  purpurea  gih- 
bosa  and  5.  purpurea  venosa,  respectively.  All  species  are  distinguished 
by  the  possession  of  pitcher  leaves  either  upright  or  decumbent,  of  con- 
siderable variety  of  form,  to  be  detailed  later.  The  following  is  a 
list  of  the  species  and  their  geographic  distribution,  according  to 
Wherry  (1935). 

Species  with  upright  tubular  pitcher  leaves:  — 

S.  oreophila  (Kearney)  Wherry.  Green  pitcher  plant.  Of  very 
hmited  distribution:  Taylor  Co.,  Georgia,  and  in  the  Appalachian 
Mountains  of  Alabama  (Cherokee,  DeKald,  and  Marshall  Cos.). 

S.  Sledgei  Macfarlane.  Pale  pitcher  plant.  S.  Alabama,  Missis- 
sippi, Louisiana  and  E.  Texas.  One  or  two  colonies  are  reported 
to  survive  in  the  Cumberland  Plateau  of  Tennessee,  presumably  in 
its  ancestral  home  before  the  rise  of  the  peneplain  of  the  Cretaceous. 

S.  flava  L.  Yellow  pitcher  plant  (1  —  7).  N.  and  S.  Carolina, 
Georgia,  extreme  N.   Florida  and  S.  Alabama,   in  the  coastal  plain. 

S.  Jonesii  Wherry.  Red  pitcher  plant.  There  is  a  singular  and 
striking  survival  of  this  plant  in  an  isolated  spot  in  Buncombe  and 
Henderson  Cos.,  N.  Carolina.  Otherwise  it  is  found  chiefly  in  S. 
Alabama  and  in  restricted  regions  nearby  in  Florida  and  Mississippi. 

S.  Drummondii  Croom.  (7 — 6).  White-top  pitcher  plant.  Chiefly 
S.  Alabama,  with  slight  extensions  into  Mississippi,  Georgia,  and  N. 
Florida.  It  forms  two  isolated  colonies  in  Georgia  (Sumter  Co.)  and 
in  Florida  (Madison  Co.). 

S.  rubra  Walter.  Sweet  pitcher  plant.  North  Carolina  (from 
Moore  Co.  southward)  through  S.  Carohna  into  Georgia,  away  from 
the  coast  except  in  N.  Carolina. 

S.minorW&W.  {1  —  9).  Hooded  pitcher  plant.  " Fly-traps "  (Mel- 
LiCHAMp).  Eastern  half  of  the  peninsula  of  Florida,  in  the  north  of 
that  state,  southern  Georgia,  western  S.  CaroUna  and  slightly  into 
N.    Carolina. 

Species  with  decumbent  leaves:  — • 

5.    psittacina   Michaux    (/ — 8).     Parrot   pitcher  plant.      From   a 


Francis  E.  Lloyd  —18— Carnivorous  Plants 

short  distance  E.  of  New  Orleans,  Mississippi,  through  S.  Alabama, 
S.    Georgia  to  the   coast  and  in  N.   Florida. 

S.  purpurea  venosa  (Rafinesque)  Wherry.  Southern  pitcher  plant. 
This  species  has  an  interrupted  distribution  from  southern  New  Jersey 
to  S.  Mississippi.  Only  small  isolated  colonies  are  to  be  found  be- 
tween N.  Carolina,  where  it  is  widespread,  and  a  similarly  wide- 
spread area  in  S.  E.  Georgia,  extreme  N.  E.  Florida,  S.  Alabama, 
from  which  a  narrow  tongue  extends  to  near  the  Mississippi  River 
N.    of   New   Orleans. 

S.  purpurea  gibbosa  (Rafinesque)  Wherry.  (i—SS)-  Northern 
pitcher  plant.  Found  throughout  a  vast  area,  beginning  with  a  nar- 
row strip  embracing  the  coastal  regions  of  Maryland,  Delaware  and 
New  Jersey,  it  spread  westerly  through  N.  Pennsylvania,  N.  Ohio, 
N.  IlHnois,  Wisconsin,  through  the  whole  region  north  and  east  to 
the  Atlantic  coast,  and  N.  W.  through  the  region  of  Winnipeg  into 
uncharted   regions.     The   northern   limits   are   not  known. 

Sarracenia  purpurea  Linn,  has  had  a  long  history,  and  we  are  in- 
debted to  Hooker  (1875)  for  digging  out  the  facts.  From_  an  early 
sketch  by  an  unknown  author,  which  found  its  way  to  Lisbon  and 
thence  to  Paris,  Clusius  (Rariorum  pi.  historia,  1601,  p.  boodj) 
published  a  figure,  which  thirty  years  later  was  copied  by  Johnson 
in  his  edition  of  Gerard's  Herbal,  in  the  hope  that  someone  would 
find  the  plant.  The  hope  was  reahzed  when  John  Tradescant, 
whose  name  is  perpetuated  in  the  genus  Tradescantia,  ^  found  it  in 
Virginia  and  succeeded  in  bringing  it  ahve  to  England  in  1640.  In 
1700  Tournefort  described  the  plant,  naming  it  Sarracenia  (or  Sar- 
racena)  in  honor  of  Dr.  M.  S.  Sarrazin,  who  had  sent  it  to  him  from 
Quebec.  The  name  was  adopted  by  Linnaeus  in  his  Hortus  Clif- 
fortianus,  1737.  The  plant  in  question  is  then  called  Sarracenia 
purpurea  L.,  and  is  the  best  known  of  all  the  species  chiefly  by  reason 
of  its  above  mentioned  wide  distribution. 

Quite  naturally  the  structural  features  of  these  peculiar  plants 
were  the  first  to  attract  attention.  The  terminal  lobe  or  flap  not 
only  looked  like  a  Hd,  but  was  believed  by  Morison  (Plantarum 
Historiae,  1699,  3:533)  to  be  hinged  and  capable  of  movement,  as 
many  non-botanists  believe  today.  Linnaeus  and  others  adopted 
this  idea,  thinking  this  behaviour  to  conserve  the  water  within.  Bur- 
nett (1829)  seemed  very  sure  of  this.  "In  many  instances  the  ap- 
paratus is  fitted  with  a  lip  or  Hd,  by  which  the  mouth  may  be  shut  or 
opened;  the  machinery  of  which  limb  is  so  contrived  that,  when  the 
cavity  within  is  well  supphed,  it  closes  to  prevent  evaporation;  and 
when  the  stock  is  diminished  or  consumed,  the  lip  is  raised,  so  that  the 
mouth  is  again  raised  to  receive  the  falhng  rain  or  rising  dew." 
Catesby  (Nat.  Hist,  of  CaroHna  2:69,  1743)  had  the  idea  that  the 
hollow  leaves  were  a  refuge  for  insects  from  the  animals  (frogs,  etc.) 
which  might  devour  them.  William,  son  of  Charles  Bartram,  in 
his  Travels  in  N.  and  S.  Carolina,  Georgia  and  Florida  (1791)  re- 
corded the  objection  suggested  earlier  by  Collinson  (see  Smith, 
182 1)  that  many  insects,  on  the  contrary,  are  caught  and  destroyed 
in   the   pitchers. 

Later  more  meticulous  observations  on  S.  adunca  led  Macbride 


Chapter  II  —  19  —  Sarracenia 

(1817)  to  find  that  the  tube  of  the  pitcher  leaf  is  lined  with  down- 
wardly pointed  hairs,  which  he  could  "plainly  see  at  the  bottom  of 
the  tube,"  and  he  saw  also  that  there  is  about  the  mouth  of  the  tube 
a  viscid  substance  which  attracts  flies. 

Then  Mellichamp,  a  physician  like  Macbride,  resident  of  the 
same  region  and  a  contemporary  of  Hooker,  did  the  first  real  ex- 
perimentation on  this  plant  and  compared  the  rate  at  which  fresh  veni- 
son showed  disintegration  in  the  pitcher  fluid  and  in  distilled  water, 
concluding  that  bacterial  action  was  at  work.  He  found  also  that 
the  pitcher  fluid  did  not  allow  the  escape  of  flies  when  they  fell  into 
it  as  water  does,  indicating  that  there  is  an  "anaesthetic  action." 
There  is  also,  he  saw,  a  nectar  baited  pathway  up  the  outside  of  the 
pitcher  to  its  mouth.  Thus  Mellichamp's  work  opened  up  the  field 
of  physiological  research  to  which  reference  will  be  made  later. 

Since  then  there  have  been  numerous  descriptions  of  the  structure 
of  the  various  plants  of  the  genus,  not  always  of  unimpeachable  ac- 
curacy.    We  now  consider  this  aspect  of  the  matter  in  what  follows. 

Sarracenia  purpurea  is  the  most  widely  distributed,  and  longest 
and  best  known,  species,  ranging  from  Labrador  to  Florida  along  the 
Atlantic  seacoast  of  N.  America,  and  westward  to  Wisconsin  and 
Minnesota,  successfully  withstanding  the  rigors  of  the  northern  win- 
ters. It  has  been  successfully  introduced  in  Switzerland.  With  S. 
psiUacina  Michx.  it  is  associated  in  the  section  Decumbentes  Uphof, 
both  being  characterized  by  having  their  leaves  more  or  less  spread- 
ing as  a  rosette.  It  is  to  be  found  in  bogs,  usually  in  company  with 
much  Sphagnum,  anchored  therein  by  its  strong  ascending  rhizomes 
clothed  with  the  remnants  of  dead  leaf  bases  and  sending  out  thick 
fibrous  roots.  It  may  often  be  found  in  company  with  other  plants, 
making  large  floating  or  semi-floating  masses  of  vegetation  about  the 
edges  of  ponds,  as  described  by  Macfarlane  and  Steckbeck  for 
Davenport  Lake,  near  Toms  River,  N.  J.,  U.  S.  A.  (1933).  In  com- 
mon with  carnivorous  plants  in  general  the  roots  are  devoid  of  mycor- 
rhiza  (MacDougal  1899). 

It  is  a  beautiful  plant  (/  —  3).  Its  leaves,  which  have  a  very  grace- 
ful form,  are  clustered  into  a  rosette  and  are  deep  green  with  rich 
crimson  markings  along  the  venation  of  the  "flap"  and  more  or  less 
uniform  similar  coloration  in  the  upper  portion  of  the  body  of  the 
leaf,  depending  on  the  exposure  to  fight. 

Form  and  structure  of  the  leaf.  —  The  pitcher  leaf  of  Sarracenia 
has  many  times  been  the  subject  of  description  from  the  anatomical 
point  of  view  by  Vogl  (1864),  Macbride  (181 7),  Mellichamp  (1875), 
Hooker  (1875),  Zipperer  (1885),  Goebel  (1891),  Macfarlane 
(1889,    1893). 

Aside  from  the  cotyledons,  which  present  no  especially  peculiar 
features,  there  are  two  forms  of  the  pitcher  leaf,  a  juvenile  and  a  ma- 
ture, both  mentioned  by  Troll  (1932).  The  mature  form  may  be 
likened  to  an  elegant  cornucopia  curving  however  only  in  one  plane. 
Arising  from  a  winged  base,  the  wings  embracing  the  bearing  stem,  it 
becomes  cylindrical  for  a  shorter  or  longer  distance  according  to  cir- 
cumstances. The  lower  part  of  this  is  soHd;  in  its  upper  part  may 
be  found  the  deepest  portion  of  the  hollow  interior  of  the  pitcher. 


Francis  E.  Lloyd  —  20  —  Carnivorous  Plants 

Along  the  upper  (ventral)  surface  of  the  cylindrical  petiolar  portion  arises 
very  gradually  a  single  ridge,  the  ala  ventralis,  which  attains  consider- 
able depth  further  up  the  leaf  (/ — 4;  2  —  12).  At  the  same  time 
the  leaf  becomes  expanded  into  a  curved  conical  hollow  vessel,  ex- 
tending to  the  mouth.  As  this  point  is  approached  the  ventral  wing 
begins  to  show  evidence  of  a  double  character  in  that  its  edge  is  longi- 
tudinally fissured  to  form  two  parallel  ridges  which  are  continuous 
with  the  edges  (nectar  roll)  of  the  bell,  which  in  this  species  has  a  very 
peculiar  form.  The  abaxial  two-thirds  are  expanded  into  a  cordate 
"flap,"  the  sides  of  which  where  they  meet  the  adaxial  part  of  the 
bell  become  helicoidal.  The  edge  of  the  helix  can  be  seen  to  continue 
as  the  edge  of  a  convolute  margin  of  the  pitcher  —  the  adaxial  part 
just  mentioned  which  I  have  called  the  nectar  roll,  and  which  is  noth- 
ing more  or  less  than  the  adaxial  part  of  the  bell.  Troll's  (1932) 
description  says  that  the  abaxial  part  of  the  pitcher  is  lengthened  as 
the  lid.  This  is  true  enough  as  far  as  it  goes,  but  this  and  all  other 
descriptions,  as  far  as  I  am  aware,  neglect  to  point  out  the  nature  of 
the  curious  rolled  margin  around  the  adaxial  limb  of  the  opening. 
At  the  midpoint  of  this  rolled  margin  there  is  on  the  surface  no  sign 
of  its  nature.  Examination  by  means  of  sections,  however,  shows  that 
the  two  ridges  of  the  ventral  wing  spread  to  right  and  left  to  continue 
as  its  involuted  margins.  One  is  reminded  of  the  volutes  of  the 
capital  of  an  Ionic  column.  To  sura  up  in  a  word,  the  flap  and  nectar 
roll  are  to  be  taken  together  as  the  edge  of  the  pitcher,  wide  and 
leaf-life  abaxially  and  tightly  rolled  outwardly  adaxially. 

But  this  comes  out  quite  clearly  in  the  juvenile  form  of  pitcher, 
found  on  seedlings  and  delicate  shoots.  These  are  slender,  the  tubular 
portion  being  narrow  and  only  very  gradually  widening  toward  the 
mouth  (2  —  13).  This  is  surmounted  by  an  overhanging  hood-like 
expansion,  the  margins  of  which  do  not  become  rolled  along  the  ab- 
axial reach  of  the  mouth,  but  run  obliquely,  meeting  to  form  the 
ventral  wing.  According  to  this  description  the  ventral  wing  is  a 
single  structure  below  and  double  above,  so  far  as  external  evidence 

goes. 

Mrs.  Arber  (1941)  has  recently  argued  that  the  lid  in  Sarracenia 
"is  merely  a  localized  development  of  the  collar".  This  may  be 
questioned  on  the  evidence  above  stated,  that  the  collar  (nectar  roll)  is 
not  present  in  juvenile  leaves. 

The  whole  of  the  outer  surface  of  the  mature  pitcher  is  supplied 
with  scattered  nectar  glands  (2  —  15,  16).  It  is  also  somewhat  rough 
and  hairy  with  scattered  trichomes  (j  —  2)  with  peculiar  thicken- 
ings in  the  form  of  waves  of  surface  expansion  rather  than  continuous 
ridges,  such  as  occur  on  the  trichomes  of  the  interior.  The  external 
glands  may  be  regarded,  as  Macfarlane  suggested,  as  alluring  in 
function,   leading  creeping  prey  to   the   mouth. 

The  internal  surface  shows,  as  Hooker  pointed  out,  distinct  zo- 
nation.  He  recognized  four  zones  and  described  them  as  follows. 
Zone  I  (2  —  12)  embraces  the  cordate  emarginate  flap.  The  epider- 
mis carries  stomata,  glands  and  strong  downwardly  directed  hairs. 
The  lower  limit  of  this  zonation  is  clearly  marked  by  an  irregular  line 
where  the  character  of  the  epidermis  cells  abruptly  changes.     In  zone 


Chapter  II  —  21  —  Sarracenia 

2,  the  epidermis  cells  have  very  thick  outer  walls  each  ending  in  an 
umbo,  and  more  or  less  imbricated  with  its  neighbors  below  (2  —  14). 
There  are  numerous  glands  here.  The  appearance  to  the  eye  is  vel- 
vety, the  surface  being  broken  up  by  the  imbrication  and  by  the  very 
numerous,  fine,  downwardly  directed  ridges  concentering  on  each  outer 
cell  wall  on  the  umbo.  This  zone  forms  a  collar  about  i  cm.  in  width. 
While  zone  i  is  highly  colored  with  red  along  the  venations,  green  be- 
tween, zone  2  is  less  colored,  though  the  red  still  follows  the  main 
veins.     There  are  no  stomata  here. 

Zone  3  is  smooth  and  glassy  and  reflects  the  light  strongly.  The 
epidermal  cells  have  wavy  thick  walls,  and  except  for  a  narrow  strip 
just  below  zone  2,  there  are  throughout  numerous  glands  (I  count 
15-20  per  mm  2),  but  no  stomata.  This  zone  occupies  about  one- 
half  the  whole  interior.  Below  it  is  zone  4,  which  is  devoid  of  cuticle 
(Batalin  1880)  except  for  a  small  space  surrounding  the  base  of  each 
hair.  These  are  numerous,  downwardly  pointed,  long,  slender  and 
glassy,  and  are  effective  in  the  detention  of  prey.  The  lack  of  cuticle 
can  be  very  easily  demonstrated  by  exposing  the  interior  surface  of  a 
leaf  to  a  weak  solution  of  methylene  blue  (or  other  suitable  dye)  or 
potassium  permanganate.  It  shows  some  discoloration,  being  brown- 
ish as  compared  with  the  rest  of  the  surface.  At  the  lower  limit  of 
zone  3  the  sinuous  walled  epidermis  abruptly  changes  to  an  epidermis 
with  plain  walls,  and  the  cells  appear  strictly  isodiametric.  There  are 
neither  glands  nor  stomata. 

For  the  above  zones  we  may  adopt  Hooker's  descriptive  terms, 
which,  for  zone  i,  is  attractive,  zone  2,  conducting,  zone  3,  glandular, 
and  zone  4,  detentive,  even  though  these  terms  are  incomplete  in  sig- 
nificance. Zone  I  is  not  only  attractive  but  is  also  a  place  of  very 
insecure  foothold,  because  of  the  form  and  direction  of  the  hairs. 
Zone  2  is  also  both  attractive  because  of  the  nectar  secreted,  as  in 
zone  I,  and  affords  a  precarious  foothold.  Zone  3  has  a  hard,  glassy 
surface,  extending  the  glacis  of  zone  2,  all  three  zones  forming  a.  facilis 
descensus  Averno.  Zone  4  is  probably  not  only  detentive,  but  also 
absorptive. 

And  to  these  should  be  added  a  fifth  zone.  This  is  a  relatively 
narrow  zone  below  zone  4,  in  which  the  cuticle  is  permanent,  and 
which  is  hairy  only  in  its  upper  part,  the  lower  being  completely 
smooth.  There  are  no  glands,  and  the  epidermal  cells  are  quite  like 
those  of  zone  4.  Fenner  (1904)  calls  this  zone  (but  he  was  describing 
S.  flava)  an  absorption  zone,  but  I  think  without  good  reason.  It  is 
true  that  these  cells  do  not  completely  resist  the  entrance  of  methyl- 
ene blue,  but  this  enters  them  much  less  easily  than  into  the  cells  of 
zone  4,  though  evidently  more  easily  than  into  those  of  zone  3,  which 
are   completely   resistant. 

MacDougal  recognized  the  zones  as  I  have  described  them. 
When  subjected  to  total  darkness,  the  petiolar  region  of  the  leaf  elon- 
gates greatly,  while  the  upper  zones  become  shorter,  zones  i  and  2 
showing  the  greatest  reduction  in  size.  Fully  etiolated  leaves  are 
twice  the  length  of  normal  ones,  but  the  petiolar  region,  including 
the  basal  part  of  the  pitcher,  is  five  times  the  normal  length.  The 
ventral  wing  does  not  develop,  the  leaf  being  wedge-shaped  in  trans- 


Francis  E.  Lloyd  —  22  —  Carnivorous  Plants 

verse  section.  The  ascidium  is  present.  Corresponding  dimensional 
changes  take  place  in  the  component  cells,  but  there  is  also,  according 
to  MacDougal,  an  actual  increase  in  the  number  of  cells  in  the 
elongated  portion  of  the  detentive  region  (which  partakes  in  elonga- 
tion with  the  petiole)  and  an  actual  decrease  in  the  number  of  cells 
of  the  conductive  surfaces  (zones  i  and  2).  Thus  the  pitcher  of  Sar- 
racenia  behaves,  in  relation  to  light,  as  if  it  were  a  leaf  blade  (zones 
I,  2  and  the  upper  part  of  3)  and  the  rest  as  if  it  were  petiolar  (1903, 
pp.  173-6).  Iris,  when  grown  in  the  dark,  grew  only  slightly  in  excess 
of  the  normal.  We  recall  that  Goebel  compares  the  Sarracenia  leaf 
with  that  of  Iris. 

The  juvenile  leaves,  which  are  also  pitcher  leaves,  differ  in  some 
details  from  the  mature.  While  they  display  the  same  zonation,  the 
characters  as  they  have  been  described  for  the  mature  leaves  overlap. 
They  can   be   described   as  follows: 

Zone  I  is  the  same  as  in  the  mature  leaves.  The  margin  of  the  flap 
is  ciliated  with  more  or  less  curved  blunt  hairs.  The  epidermal  cells 
are  sinuous  walled,  the  glands  present  but  few.  Stomata  are  present 
and  the  hairs  stout  and  curved. 

Zone  2.  The  epidermis  of  zone  i  changes  abruptly  in  that  all  the 
cells  become  trichomatous,  but  very  short  and  produce  the  effect  of 
imbrication,  as  described  above.  Glands  are  large  and  numerous, 
more  so  towards  the  lower  limit  of  the  zone,  where  the  epidermis 
again  changes. 

Zone  3.  The  epidermal  cells  are  again  sinuous  walled  but,  unhke 
the  mature  leaf,  there  are  numerous  trichomes.  Glands  are  here  also 
present,  but  no  stomata. 

Zone  4.  The  epidermal  cells  become  straight,  the  cells  isodiametric, 
with  numerous  very  slender  hairs,  and  no  glands,  and  no  cuticle. 

Zone  5  has  the  same  sort  of  epidermis  as  zone  4,  but  is  devoid  of 
hairs. 

As  we  shall  see,  the,  juvenile  leaf  of  S.  purpurea  resembles  in  struc- 
ture that  of  5.  psittacina. 

We  come  to  the  details  of  the  glands  and  trichomes.  The  glands 
(j — i)  are  all  of  one  type  (the  ''Sarracenia  type,"  Goebel,  1891). 
Viewed  as  part  of  the  general  surface,  each  gland  exposes  normally 
six  cells  to  view,  four  in  a  rough  circle  and  two,  the  cover  cells  (Goe- 
bel) in  the  middle  (2  —  15).  The  cover  cells  overlap  the  four  bor- 
dering cells  to  a  greater  or  less  extent.  Those  on  the  outer  surface 
have  relatively  large  cover  cells,  which  jut  out  further  beyond  the 
general  level  of  the  surface.  Those  of  the  glands  of  zone  2  are  rela- 
tively much  smaller. 

The  outer  surface  glands  (2  —  15,  16)  are  the  smallest  and  simplest 
in  structure,  derived  from  a  single  epidermal  cell,  according  to  Zip- 
perer  and  to  Fenner.  Undoubtedly  the  gland  is  of  epidermal  ori- 
gin, and  the  idea  is  not  precluded  that  it  may  represent  originally  a 
stomatal  apparatus,  the  cover  cells  arising  originally  as  guard  cells. 
But  this  is  admittedly  speculation.  The  four  peripheral  cells  lie  in 
the  general  level  of  the  surrounding  epidermal  cells,  while  the  two 
cover  cells  are  conical  and  are  wedged  in  between  the  peripheral  cells. 
Against  the  interior  faces  of  the  peripheral  cells  there  is  usually  one, 


Chapter  II 


23  —  Sarracenia 


sometimes  two  cells,  the  adjunct  cells,  which  appear  to  be  derived 
from  the  parenchyma.  The  walls  of  the  adjunct  cell,  or  cells  in  con- 
tact with  the  gland  cells,  are  variously  thickened,  reticulately  and 
circularly,  as  represented  by  Goebel  (1891).  Fenner  thought  that 
the  adjunct  cells  are  also  derived  from  the  epidermis  (Fenner  called 
them  "Durchlasszellen"),  but  their  denser  protoplasmic  content  in- 
dicates that  they  have  more  than  a  passive  role.  The  outer  walls 
of  the  cover  and  peripheral  cells  are  all  cuticularized,  staining  with 
fat  stains  (Congo  Red,  etc.)  except  a  part  of  those  making  the  contact 
with  the  adjunct  cell  or  cells.  These  walls  resist  sulfuric  acid  along 
with  the  outer  walls  of  the  surrounding  epidermal  cells.  But  meth- 
ylene blue  easily  permeates  these  glands  in  the  living  leaf. 

The  interior  glands  (j— i)  are  of  similar  structure,  but  are  of 
two  courses,  evidently,  as  Fenner  indicates,  derived  from  originally 
four  peripheral  cells.  The  gland,  aside  from  the  adjunct  cells,  there- 
fore consists  of  normally  10-12  cells,  the  outer  course  having  four  periph- 
eral and  two  cover  cells,  the  inner  course  usually  four  to  six  cells.  The 
cover  cells  are  slenderly  conical,  are  wedged  in  the  middle  of  the  outer 
peripheral  cells,  extending  inwardly  till  more  or  less  in  contact  with 
the  inner  course.  Their  walls  are  considerably  thickened  and  cuti- 
cularized throughout.  The  base  of  the  gland  is  in  contact  with  two 
to  four  or  five  adjunct  cells  with  reticulate,  circularly  or  spirally 
thickened  walls  of  contact  which  give  a  positive  reaction  with  phloro- 
glucin  and  HCl.  Here,  however,  there  is  no  suberization  of  the  gland 
cells  so  that  there  is  left  a  "window"  (Fenner's  term)  allowing 
communication  by  ready  diffusion  between  the  adjunct  and  gland 
cells  proper.  The  glands  of  the  nectar  roll,  while  identical  in  struc- 
ture with  those  elsewhere,  show  a  certain  distortion  consequent  on  the 
growth  movement  resulting  from  torsion  during  the  development. 

The  structure  of  the  glands  in  whatever  zone  they  occur  is  the 
same,  though  they  function  differently.  On  the  outer  surface  of  the 
pitcher  and  on  the  inner  in  zones  i  and  2,  they  secrete  nectar.  Though 
Hooker  was  in  doubt  on  this  point,  I  am  sure  of  it  from  my  own 
observation.  I  have  also,  on  a  warm,  sunshiny  day  watched  flies  in 
numbers  busily  sucking  the  nectar  and  some  of  them  getting  trapped 
by  slipping  down  the  surface  of  zones  i  and  2.  The  glands  of  zone 
3,  however,  probably  secrete  digestive  ferments,  judging  from  the 
results  of  Hepburn  et  al.  (1927),  to  be  discussed  later. 

Sarracenia  psittacina  Michx.  —  This  species  (i  —  8)  is  associated 
with  5.  purpurea  in  the  Decumhentes  by  Uphof,  because  of  the  posi- 
tion of  the  leaves  which  lie  more  or  less  parallel  with  the  ground.  The 
leaf  considered  as  a  trap,  is,  however,  quite  different  in  this  species, 
and  is  much  more  efficient  mechanically  —  or  at  least  it  appears  so. 
No  account  I  know  of  quite  brings  this  point  out.  The  leaf  which 
Goebel  described  as  the  "first  pitcher  leaf"  is  a  juvenile  form  (3  —  5). 

Its  habitat  is  low,  wet,  sandy  meadows  subject  to  inundations 
by   the   acid  waters   of  nearby   swamps   (Wherry). 

It  is  regarded  taxonomically  as  associated  with  S.  purpurea,  but 
it  is  as  much  or  more  like  Darlingtonia.  The  pitcher  consists  of  a 
narrow,  tapering  curved  tube  (j  — 4),  somewhat  flattened  dorsiven- 
trally,  with  a  wide  ventral  wing,   and  with  the  top  of  the  pitcher 


Francis  E.  Lloyd  —  24  —  Carnivorous  Plants 

curved  over  to  form  a  hood,  with  an  entrance  of  narrow  caliber  facing 
horizontally,  instead  of  downwards  as  in  Darlingtonia.  It  is  deep 
red  in  color,  mottled  by  angular  white  fenestrations  which  allow 
diffused  light  to  enter  the  tube  on  all  sides,  more  especially  on  the 
ventral  aspect  of  the  tube  which,  because  of  the  decumbent  position 
of  the  leaf,  hes  uppermost.  In  some  other  species,  the  fenestrations 
occur  on  the  dorsal  aspect  of  the  tube.  The  pitchers  are  rigid,  and 
are  of  striking  shape,  suggesting  the  specific  and  common  name.  The 
above  mentioned  fenestrations  have  a  more  opaque  look  than  those 
of  Darlingtonia,  and  on  examination  they  were  found  to  have  extensive 
intercellular  spaces,  the  effect  of  which  is  to  diffuse  the  Hght,  thus 
producing  a  snowy  whiteness. 

The  form  and  structure  of  a  pitcher  can  be  best  seen  in  one  cut 
sagittally  (j  — 4).  The  upper  part  of  the  tube  is  strongly  curved,  so 
as  to  direct  the  opening  toward  the  leaf  base.  The  end  of  the  mid- 
vein  is  indicated  by  a  low  umbo,  the  organic  apex  of  the  pitcher.  Be- 
yond this  point  the  hood  is  closed  by  the  forwardly  curved  lobes  of 
the  "flap,"  the  margins  of  which  are  closely  apposed,  sometimes  even 
to  mutual  adherence,  though  sections  show  their  histological  inde- 
pendence (j  —  6).  The  more  ventral  reaches  of  these  lobes  are  en- 
larged and  bend  inwards  to  form  the  entrance  tube.  Inspection  of 
this  shows  that  it  is  formed  partly  by  the  upper  short  stretch  of  the 
ventral  pitcher  wall  and  the  proximate  parts  of  the  lobes,  a  condition 
dupHcated  in  the  aberrant  juvenile  leaf  of  Darlingtonia  (5  —  3).  Thus 
is  formed  a  short  cylindrical  entrance  tube  (j  —  6),  making  the  trap 
of  the  lobster-pot  type.  The  inner  free  edge  of  the  entrance  tube  is 
stiffened  not  only  by  the  strong  epidermis,  but  by  a  weal  running 
parallel  to  the  free  edge  {3  —  4).  This  weal  is  continuous  with  the 
exact  edge  of  the  lobes  above  the  entrance  tube,  and  must  be  re- 
garded as  the  morphological  margin.  The  edging  beyond  this  forms 
a  shelf  bearing  numerous  nectar  glands,  and  is  clothed  on  both  sides 
with  tessellated  epidermis  of  umbonate,  striated  cells,  characteristic 
of  the  inner  general  surface  of  the  entrance  tube,  where  also  glands 
are  found. 

This  shelf  corresponds  exactly  with  the  inwardly  curved  nectar 
roll  of  Darlingtonia  (5  —  10),  from  the  pitcher  of  which  that  of  S. 
psittacina  differs  in  the  fact  that  the  organic  apex  of  the  tube  lies 
within  the  periphery  of  the  hood,  while  in  Darlingtonia  it  lies  beyond. 
The  two  lobes  of  the  fishtail  appendage  of  Darlingtonia  correspond 
to  the  two  lobes  of  S.  psittacina.  Macfarlane  regarded  this  species 
as  the  most  aberrant  of  all  the  species  of  Sarracenia,  and  its  similar- 
ity to  Darlingtonia  supports  this  view.  It  is  on  the  whole  more 
similar  to  Darlingtonia  than  to  5.  purpurea. 

The  earlier  stages  in  the  development  of  the  leaf  are  practically 
indistinguishable  from  that  of  other  species  examined.  The  feature 
peculiar  to  this  species,  however,  the  infolded  edge  of  the  flap,  is  a 
character  which  appears  quite  late  in  the  course  of  development.  In 
a  leaf  which,  though  embryonic  in  form,  was  large  enough  to  be  ex- 
posed to  the  Hght,  the  hood  measured  about  0.75  mm.  and  in  this 
the  fold  has  just  commenced  to  develop  (5—  11).  In  one  with  the  hood 
2  mm.  long  the  ingrowth  was  marked,  but  far  from  fully  developed. 


Chapter  II      —25—    Sarracenia 

In  this  early  stage  the  structure  resembles  that  of  Darlingtonia,  save 
for  the  forward  developing  fishtail  appendage,  which   here    does   not 

appear   at   all. 

The  interior  surface  of  the  pitcher  presents  a  zonation  which  cor- 
responds roughly  with  that  in  S.  purpurea,  but  is  by  no  means  as 
distinct  as  in  that  species.  This  lack  of  distinction  arises  from  the 
overlapping  of  the  zones  3  and  4,  and  the  restriction  of  zone  2  to  the 
inner  surface  of  the  entrance  tube,  the  ventral  portion  of  which  is  part 
of  the  pitcher  tube  proper.  This  point  must  be  appreciated  as  other- 
wise it  would  be  difficult  to  recognize  zone  2  at  all. 

Zone  I  (j  —  4)  is  the  whole  of  the  inner  surface  of  the  hood  ex- 
cepting the  inturned  edge  of  the  re-entrant  tube.  The  epidermis  is 
of  wavy-walled  cells  with  stomata  and  many  nectar  glands,  and  scat- 
tered, relatively  few  downwardly  directed,  curved  weak  hairs,  as  com- 
pared with  the  flap  of  5.  purpurea,  or  Heliamphora.  Since  the  chief 
mechanism  for  the  capture  of  insects  is  the  re-entrant  tube,  these  hairs 
are  of  little  importance.  This  is  compensated  for  by  the  presence  of 
very  many  stiff  hairs  in  the  dorsal  aspect  of  the  dome,  to  which  zone 
3  reaches. 

Zone  2  corresponds  to  this  zone  in  S.  purpurea  in  function,  though 
it  is  not  a  complete  zone  geometrically  speaking.  It  embraces  a  short 
reach  of  the  ventral  wall  of  the  pitcher  with  the  contiguous  sides  of 
the  re-entrant  tube,  including  the  shelf,  which  is  within  the  morpholog- 
ical edge  of  the  lobe.  The  shelf  and  the  inner  surface  of  the  tube 
sides  are  clothed  with  an  epidermis  of  tessellated  straight  walled  cells 
each  with  a  low  striated  umbo,  pointing  inward  and  downward,  as  in 
zone  2  of  S.  purpurea.  Glands  are  present,  in  greater  number  proxi- 
mally  than  distally.  They  are  absent  under  the  shelf,  but  the  shelf 
itself  bears  a  great  many.  This  is  the  principal  lure  evidently,  but  the 
insect  which  advances  into  the  re-entrant  tube  to  sip  the  nectar  is 
invited  to  enter  further  by  the  shining  white  fenestrations,  mullioned 
in  red,  of  the  pitcher  wall.  The  outer  surface  bears  many  small  glands 
also,  which,  with  those  of  the  general  outer  pitcher  surface,  constitute 
a  general  lure. 

Zone  3.  Like  zone  3  of  5.  purpurea  this  carries  some  stomata  and 
many  glands,  but,  unlike  that  species,  the  whole  surface  is  clothed 
with  a  dense  felt  of  downwardly  pointed,  slender  stiff  hairs,  continuous 
with  those  of  zone  4.  It  may  be  described  as  an  advance  of  zone  4 
to  overlap  zone  3.  The  parallelism  between  this  species  and  S.  pur- 
purea is  seen  in  the  many  glands  of  this  zone.  These  are  possibly 
peptic  glands,  though  the  evidence  is  at  present  not  conclusive  {see 
p.  34).  The  epidermis  is  of  a  mixture  of  wavy- walled  cells,  and  smaller 
straight  walled  cells,  these  becoming  more  numerous  as  the  next  zone 
4  is  approached.  It  is  underlain  by  a  course  of  wavy-walled  cells,  the 
walls  of  which  are  thick  and  afford  stiffening  to  the  pitcher  wall._ 

Zone  4  is  devoid  of  glands,  but  has  a  dense  clothing  of  trapping 
hairs  down  to  the  very  end  of  the  pitcher  tube,  where  they  are  shorter, 
fitting  better  the  reduced  bore  of  the  tube,  and  leaving  a  lumen. 
Macfarlane  described  the  whole  of  zones  3  and  4,  as  above  delimited, 
as  the  detentive  zone,  but  having  glands  in  the  upper  one-third.  In 
S.  purpurea  zone  3  is  secretive,  and  has  a  glissade  surface,  while  in 
S.  psittacina  the  surface  is  hairy. 


Francis  E.  Lloyd  —  26  —  Carnivorous  Plants 

The  structure  of  the  glands  is  like  that  in  S.  purpurea  (3  —  3). 

GoEBEL  described  the  seedling  leaves  which  appear  directly  fol- 
lowing the  cotyledons.  In  form  they  resemble  closely  the  juvenile 
leaves  of  S.  purpurea.  The  leaves  of  the  two  species  in  the  juvenile 
state  are  regarded  by  W.  P.  Wilson  (1888)  as  indistinguishable,  and 
he  regarded  them  as  closely  related.  The  presence  of  the  umbo,  how- 
ever (5  —  5),  clearly  separates  S.  psittacina  from  S.  purpurea.  The 
forward  margin  of  the  mouth  is  simple,  and  the  inturning  valvular 
nectar  roll  with  its  marginal  thickening  is  absent.  Absent  also  are 
the  two  lateral  lobes.  The  interior  surface  is  divided  into  four  zones: 
(i)  the  under  surface  of  the  hood,  with  scattered  retrorse  hairs  with 
interspersed  glands;  (2)  the  ghding  zone  with  a  Hning  of  imbricated 
cells  with  downward  directed  points;  (j)  a  wide  zone  with  many  long 
downward  pointed  hairs  with  glands  between;  and  {4)  the  bottom 
zone  with  smooth  epidermis.  Goebel's  zone  (2)  corresponds  to  zones 
2  and  3  in  my  description  of  the  adult  form  of  leaf  above. 

Sarracenia  Courtii.  —  This  is  a  hybrid  between  S.  purpurea  and 
S.  psittacina,  and  in  its  structure  reflects  the  characters  of  both  in  the 
zonation  of  the  pitcher  leaf.  As  in  S.  purpurea,  the  conductive  zone, 
zone  2,  is  broader  than  in  6*.  psittacina,  and  occupies  a  transverse  band 
around  the  interior  of  the  leaf,  narrowing  dorsally,  thus  separating 
zones  I  and  3  almost  completely.  Zone  3  is  much  less  hairy  than  this 
zone  in  S.  psittacina,  but  is  glandular,  as  in  that  species.  The  general 
aspect  of  5.  Courtii  resembles  that  of  5.  psittacina,  but  the  plant  is 
larger. 

Sarracenia  minor.  —  In  this  species  the  leaf  stands  in  a  vertical 
position,  and  the  opening  is  overhung  by  a  wide,  domed  lid  (i  —  9; 
3 —  7-9)-  The  wall  of  the  pitcher  opposite  the  opening,  and  for  some 
distance  up  and  down,  is  fenestrated  with  white  patches  as  in  Darling- 
tonia.  These  are  slightly  thinner  areas  of  the  wall,  devoid  of  chloro- 
phyll, and  there  is  no  palisade  tissue  anywhere.  These  white  spots 
may  be  regarded  as  a  visual  lure  for  insects.  The  lower  edge  of  the 
mouth  is  thickened  by  an  outwardly  reflexed  edge  of  the  wall,  as  in 
5.  purpurea,  to  form  the  nectar  roll.  The  body  of  the  pitcher  is  a 
tapering  tube  slightly  curved,  and  carrying  a  wing  in  front  —  the 
ala  ventralis  —  which,  has  a  double  edge  above,  the  edges  flowing 
right  and  left  into  the  edge  of  the  hd,  but  a  single  one  below,  and  is 
not  confluent  with  the  stipular  wings  of  the  leaf  base.  The  ventral 
wing  starts  at  the  top  of  the  tube  and  attains  its  greatest  width  about 
half  way  down. 

The  outer  surface  is  sparsely  hairy  with  short,  curved  hairs  with 
finely  tuberculated  walls.  There  are  numerous  glands  scattered  all 
over  the  outer  surface,  and  these  are  especially  active  in  secretion  along 
the  upper  part  of  the  edge  of  the  wing,  where  drops  of  nectar  which 
have  been  excreted  by  them  may  be  seen  (5  —  9).  I  have  not  seen 
nectar  collecting  visibly  elsewhere  on  the  outer  surface.  The  interior 
surface  presents  a  zonation  visible  to  the  eye  but  somewhat  dif- 
ferent from  that  of  5.  purpurea  and  more  like  that  of  6".  psittacina. 
Mellichamp  (1875)  recognized  three  "belts"  or  zones:  (/)  embracing 
the  internal  honey  secreting  portion;  (2)  a  belt  hned  with  soft  and 
velvety  pubescence   affording  no  foothold  for   most  insects;   and   (j) 


Chapter  II  —  27  —  Sarracenia 

that  of  coarse  straw-colored  hairs  extending  to  the  bottom  of  the  tube 
where  a  watery  fluid  is  secreted.  Essentially  correct,  this  description 
does  not  specify  closely  enough  the  distinction  which  actually  exists. 
Though  the  zonation  does  not  stand  out  so  clearly  as  in  S.  purpurea, 
we  can  nevertheless  recognize  four  zones. 

Zone  I,  that  of  the  under  surface  of  the  lid  which  ends  in  an  obhque 
line  extending  obliquely  upwards  from  the  lower  margin  of  the  mouth. 
This  is  covered  rather  densely  with  curved  hairs  downwardly  directed. 
Interspersed  are  numerous  nectar  glands  which  are  evidently  active, 
for  one  can  see  minute  drops  of  nectar  studding  the  surface.  At  the 
line  of  demarkation  the  epidermis  abruptly  changes  to  a  smooth,  con- 
tinuous surface  of  tessellated  cells,  each  of  which  is  downwardly  sharply 
umbonate  (j — lo).  Interspersed  are  very  numerous  glands  which 
are  very  active.  In  the  upper  part  stand  large  drops  which  run  to- 
gether to  form  a  flood  of  nectar.  This  is  continuous  along  the  lower 
lip  of  the  mouth  and  for  a  centimeter  down  from  there  and  elsewhere 
around  the  tube.  This  I  call  zone  2.  At  its  lower  limit  the  umbonate 
cells  give  way  gradually  to  cells  of  identical  structure,  but  having 
the  umbo  lengthened  into  a  longer  slender  spike,  still  with  many 
glands  scattered  between.  This  zone  measures  about  3  to  4  cm.  in 
depth.  It  is  evidently  glaucous,  with  a  white  sheen.  This  is  zone  3. 
Below  begins  zone  4,  recognizable  to  the  eye  by  the  pale  green,  non- 
glaucous  appearance.  It  soon  becomes  brownish  in  color  and  bears 
numerous  scattered  long  slender  hairs  with  a  detentive  function  (j  — 
11),  with  more  or  less  straight  walled  cells  between.  In  the  upper 
part  of  this  zone  there  are  a  few  glands,  but  none  much  below  a 
depth  of  I  cm.  Below  the  epidermis  in  zones  2,  3  and  4,  the  pitcher 
wall  is  conspicuously  strengthened  by  a  hypodermis  of  wavy  walled 
cells  with  walls  rather  thin  above,  but  in  the  general  region  of  zone  4 
very  thick  and  underlain  by  a  second  course  of  wavy  walled  cells  with 
thinner  walls.  It  is  obvious  that  these  cells  add  materially  to  the 
rigidity  of  the  tubular  wall.  The  epidermal  walls  themselves  are 
straight  or  only  very  slightly  wavy.  The  edges  of  the  lid  are  con- 
tinuous with  the  true  edge  of  the  lower  reach  of  the  mouth  border. 
The  nectar  roll,  as  in  5.  purpurea,  is  covered  with  tightly  imbricated 
umbonate  cells  with  numerous  nectar  glands  (j  —  10,  12).  On  the 
whole,  the  pitcher  hning  is  similar  to  that  of  the  juvenile  pitchers 
of  that  species,  in  which,  however,  zone  3  is  much  shallower  than  in 
S.  minor.  In  general  form  this  species  resembles  S.  purpurea  with  its 
bell  turned  forward  so  as  to  shade  the  opening,  but  as  far  as  the 
epidermal  lining  is  concerned  is  more  like  either  the  juvenile  leaves 
of  S.  purpurea,  or  the  mature  leaves  of  5.  psittacina.  In  the  course 
of  evolution  it  is  possible  that  S.  purpurea  has  been  derived  from  a 
plant  resembling  S.  minor  simply  by  a  change  in  the  posture  of  the 
leaves  from  vertical  to  spreading,  and  by  an  extension  of  one  zone 
at  the  expense  of  another.  A  change  from  5".  minor  to  S.  psittacina 
could  have  been  accomplished  by  an  additional  elaboration  of  the 
region  surrounding  the  mouth  by  extending  the  dimensions  of  the 
nectar  roll,  and  reversing  it,  curling  it  to  the  inside  instead  of  to 
the  outside.     This  is  speculating,  of  course. 

Sarracenia   Drummondii.  —  This    is    a    tall    species,    the    trumpet- 


Francis  E.  Lloyd  —  28  —  Carnivorous  Plants 

shaped  leaves  attaining  a  length  of  2-3  ft.  and  standing  in  a  strictly- 
erect  posture  (/  —  6).  The  tapering  tube  gradually  widens  to  the 
top,  but  contracts  somewhat  just  below  the  opening,  the  bulge  being 
scarcely  wider  than  the  opening,  which  is  oblique.  About  two-thirds 
of  the  margin  is  occupied  by  a  nectar  roll,  the  free  edges  of  which 
are  continuous  with  the  two  edges  of  the  ventral  wing,  as  in  other 
species  already  described.  The  abaxial  third  of  the  edge  of  the  open- 
ing is  extended  into  a  spreading,  over-hanging  lid  supported  by  its 
broad  stalk.  The  posture  changes  somewhat  with  age,  passing  from 
a  more  horizontal  to  a  more  oblique  position,  and,  according  to  Goebel 
and  others,  serves  to  divert  rain  water  from  the  interior  of  the  tube. 
The  lid  and  upper  portion  of  the  tube  are  highly  colored  in  a  motley 
of  white  and  red,  with  green  except  in  the  white  fenestrations,  which 
occur  here  as  in  S.  minor  and  Darlingtonia. 

The  external  surface  is  supplied  with  small  nectar  glands  and  is 
roughly  hairy  on  the  upper  part  of  the  tube.  The  hairs,  which  are 
like  those  in  S.  purpurea,  point  in  various  directions,  and  not  uni- 
formly in  one  direction. 

The  internal  surface  is  clearly  divisible  into  zones.  Zone  i  is  the 
inner  surface  of  the  lid  as  far  as  a  distinct  line  crossing  the  isthmus 
supporting  it.  There  are  many  glands  and  stomata,  and  the  surface 
is  studded  with  curved,  downwardly  pointed  hairs  of  slender  form 
and  bending  under  the  pull  of  a  fly's  foot.  Zone  2  starts  at  the  line 
across  the  stalk  of  the  hd,  and,  including  the  nectar  roll,  extends  down- 
ward inside  the  tube  a  distance  of  18  cm.  in  a  leaf  60  cm.  tall.  The 
surface  is  clothed  with  oval  cells  which  form  short  sharp  hairs,  retrorse 
as  elsewhere.  There  are  large  nectar  glands  on  the  nectar  roll  and 
in  the  upper  one-half  of  the  zone,  but  none  below.  There  are  no 
stomata  (Zipperer).  This  is  the  conducting  zone  (Macfarlane). 
Zones  3  and  4  are  not  separable  to  the  eye  except  for  the  fact  that, 
in  the  upper  region  of  the  combined  zones,  which  are  detentive,  there 
are  a  few  glands  in  a  narrow  belt  just  below  the  lower  limit  of  zone  2. 
Though  to  the  eye  the  line  of  demarkation  between  zones  2  and  3  is 
distinct,  the  transition  under  the  microscope  is  not  a  very  sudden  one, 
since  the  change  from  very  short  hairs  (zone  2)  to  the  very  long  ones 
of  zone  3  is  gradual.  In  zone  2,  every  epidermal  cell  is  a  trichome 
(except  of  course  where  glands  occur);  in  the  zone  below  this  is  true 
only  of  relatively  few  epidermal  cells.  In  the  upper  part  of  zone  3,  the 
epidermal  cells  have  more  or  less  sinuous  walls,  giving  way  soon  to 
cells  with  oval  outline,  and  this  region  we  may  recognize  as  zone  4. 
The  bottom  of  the  tube  is  quite  smooth  for  nearly  five  cm.  From  the 
whole  of  zones  3  and  4  the  cuticle  is  absent.  The  tube  throughout  its 
length  is  greatly  strengthened  mechanically  by  the  presence  of  a  wavy 
thick  walled  second  layer. 

Macfarlane  denied  the  presence  of  glands  in  the  upper  part  of 
the  detentive  zone,  saying  that  there  are  stomata  surrounded  by 
groups  of  cells.  I  think  he  was  mistaken  in  this.  The  glands,  which 
are  few  in  number,  are  somewhat  distorted,  owing  to  the  character 
of  the  epidermis  of  many  imbricated  hairs,  but  are  nevertheless  clearly 
glands.     There  are  no  stomata  (Zipperer). 

In  addition  to  the  normal  pitcher  leaves  there  are  others  in  which 


Chapter  II  —29— Sarracenia 

the  tube  is  not  developed.  The  leaf  then  consists  of  a  cylindrical 
stalk  with  a  wide  ventral  wing.  At  the  apex  there  is  more  or  less 
of  a  depression.  Such  leaves  are  photosynthetic  only,  and  have  been 
compared  by  Goebel  to  the  unifacial  leaf  of  Iris.  These  leaves  de- 
velop later  in  the  growing  season  (Goebel). 

Having  favorable  material  at  Munich,  I  arranged  the  upper  part 
of  a  leaf  under  a  bell  jar  and  put  a  blue  bottle  fly  inside.  The  leaf 
stood  vertically  in  shallow  water  in  a  vial.  The  fly  was  soon  attracted 
by  the  nectar  secreted  by  the  glands  of  the  external  surface  and  gradu- 
ally worked  his  way  by  an  erratic  path  to  the  rim.  Mounting  this 
he  began  to  sip  the  nectar,  either  on  the  under  surface  of  the  lid  as 
far  as  he  could  reach  without  letting  go  his  hold  with  his  hind  legs 
on  the  edge  of  the  lid,  or  of  the  rim.  Swinging  about  he  explored 
the  surface  inside  the  rim,  always  hanging  on  by  his  hind  legs;  and 
it  was  evident  that  he  was  aware  of  the  precarious  foothold,  for  he  was 
loth  to  free  his  hind  foot  or  feet.  But  on  getting  what  seemed  to  be 
a  foothold  and  reaching  as  far  as  possible  for  the  nectar,  he  would 
let  go  and  then  invariably  fall  plump  into  the  abyss.  A  bit  of  the 
tube  was  cut  away  above  the  water  level  so  that  he  could  escape, 
and  in  consequence  he  performed  for  me  again  and  again.  His  actions 
were  repeated  a  dozen  times  without  failure  of  being  trapped.  If 
he  ventured  on  the  under  side  of  the  lid,  as  he  sometimes  did,  he 
could  remain  there  as  long  as  he  grasped  the  edge  with  one  foot,  seiz- 
ing the  hairs  with  the  other;  but  the  moment  he  let  go  of  the  edge, 
down  he  fell  into  the  tube.  There  is  therefore  no  question  but  that 
the  surface  of  zones  i  and  2  is  one  which  gives  no  foothold  to  such 
flies  and,  to  infer  from  the  variety  of  prey  found  in  the  pitchers,  to 
most  other  insects  as  well. 

Sarracenia  flava.  —  This  species  resembles  S.  Drummondii  in  many 
respects,  but  is  stouter  and  coarser,  and  its  prevailing  color  is  greenish- 
yellow,  with  the  latter  color  quite  dominant.  The  tube  tapers  gradu- 
ally from  the  mouth  down,  being  widest  at  this  point.  The  lid  is 
more  erect  and  has  a  narrower  and  stouter  neck,  and  is  backwardly 
recurved  at  the  edges.  The  apex,  instead  of  being  emarginate  as  in 
some  species,  is  acute  (7 — 7).  A  leaf  24  cm.  long,  examined  at  Munich, 
shows  zonation  as  follows. 

Zone  I  is  the  under  surface  of  the  lid  and  carries  many  short, 
stout,  downwardly  pointed  hairs  and  many  nectar  glands.  The  lower 
limit  of  this  zone  is  very  irregular,  the  hairiness  following  the  promi- 
nent veins,  the  spaces  between  being  smooth  and  glaucous  and  con- 
tinuous with  zone  2,  which  is  lined  with  an  epidermis  of  imbricated 
pointed  cells  with  many  glands  scattered  over  the  surface.  This  zone 
extends  about  2  cm.  downwards,  and  includes  most  of  the  neck,  the 
nectar  roll  and  a  narrow  zone  below  it,  as  in  5.  minor.  This  is  deep 
yellow,  glaucous  and  the  imbricated  cells  of  the  epidermis  are  short 
pointed.  There  are  glands  present  in  great  numbers,  and,  quite  as  in 
other  species  described,  this  is  a  dominant  place  of  lure.  The  lower 
limit  of  this  zone  is  not  defined  but  fades  into  zone  3  (8  cm.  deep), 
in  which  the  imbricated  cells  have  longer  retrorse  points.  The  num- 
ber of  glands  is  reduced  so  that  in  the  lower  regions  there  are  none 
to  be  found.     The  whole  area  is  glaucous.     The  lower  limit  of  zone  3 


Francis  E.  Lloyd  —  30  —  Carnivorous  Plants 

is  very  irregular,  but  readily  distinguished  by  the  eye  by  the  change 
in  color,  due  to  absence  of  cuticle  in  zone  4.  Under  the  microscope 
there  is  a  sudden  transition  from  imbricated  apiculate  hairs  to  scat- 
tered, very  long,  curved  ones,  characteristic  of  zone  4.  Underlying 
both  zones  there  is  a  hypodermis  of  wavy,  thick  walled  cells.  The 
lowest  portion  of  zone  4  is  quite  smooth,  is  lined  with  a  small,  straight 
walled  epidermis,  and  is  6  cm.  in  depth. 

Sarracenia  Jonesii.  —  Living  material  from  Flat  Rock,  North 
Carolina,  collected  by  Dr.  L.  E.  Anderson  through  the  courtesy  of 
Professor  F.  A.  Wolf,  was  examined  and  showed  quite  the  same  char- 
acters of  the  epidermis  and  of  zonation  as  have  been  described  for  S. 
Drummondii  and  S.  flava.  Such  differences  as  occur  are  those  of  the 
shape  of  the  hd,  which  is  smaller  and  ovate,  similar  to  that  of  S. 
minor  save  that  it  is  more  erect  and  apiculate.  The  color  is  green, 
veined  with  red,  with  no  fenestrations.  There  are  no  glands  in  the 
lower  part  of  zone  3,  or  in  zone  4. 

Morphology  of  the  leaf.  —  Troll  (1932)  has  summarized  our  knowl- 
edge on  this  subject,  adding  his  own  views. 

Baillon  (1870)  compared  the  leaf  of  Sarracenia  with  that  of 
Nelumbo,  expressing  the  opinion  that  "the  wide  but  shallow  cone 
of  the  (peltate)  leaf  of  Nelumbo  becomes  in  Sarracenia  deeper  and 
narrower  in  such  a  manner  as  to  produce  definitively  the  form  of  a 
long,  obconical  trumpet,"  thus  recognizing  the  relation  between  the 
epiascidiate  pitcher  of  Sarracenia  with  peltate  leaves. 

As  we  have  already  seen,  the  pitcher  consists  of  a  spreading  bi- 
facial leaf  base  surmounted  by  a  tubular,  gradually  widening  pitcher 
bearing  a  strong  ventral  wing  and  the  foliaceous  flap  continued  in 
front  as  the  nectar  roll.  When  the  ascidium  fails  of  development,  as 
it  sometimes  does  (as  in  S.  flava,  etc.),  the  leaf  presents  a  certain 
likeness  to  that  of  Iris  and  the  phyllodia  of  Acacia  sp.  Asa  Gray 
(1895-7)  designated  the  ventral  wing  or  keel  as  a  "phyllodial  wing." 
Various  earlier  authors  (Lindley  1832,  Saint-Hilaire  1840,  Morren 
1838,  Duchartre  1867)  regarded  the  pitcher  as  a  leaf  blade  with  the 
margins  fused,  some  of  them  thinking  the  tube  to  be  the  winged 
petiolar  region  and  the  flap  the  leaf  blade.  Gray  accepted  this  view, 
saying,  "they  are  evidently  phyllodia."  Of  them,  however,  Morren 
believed  the  flap  to  be  only  the  apical  portion  of  the  leaf  blade,  the 
most  of  which  is  involved  in  the  tube.  Macfarlane  (1889-90)  was 
firmly  of  this  opinion.  He  regarded  the  keel  as  compound  of  the 
fused  leaf  edges,  comparing  the  condition  with  that  in  the  leaf  of 
Iris  as  he  interpreted  the  anatomy  of  this.  The  single  keel  of  Sar- 
racenia is  equivalent  to  the  pair  of  apposed  wings  of  Heliamphora 
and  the  more  widely  separated  ones  in  Nepenthes,  according  to  the 
nature  of  the  fusion.  The  flap  of  Sarracenia  is  to  be  regarded  as 
compound  of  two  pinnae,  as  is  the  lid  of  Nepenthes  (1893).  Troll 
regards  this  view  as  false,  based  on  a  misconception  of  the  mor- 
phology of  the  Iris  leaf,  which  he  insists  is  congenitally  a  strictly  uni- 
facial  leaf.  He  accepts  Goebel's  intrepretation  that  the  Sarracenia 
pitcher  is  a  unifacial  leaf  in  the  form  of  a  tube  and  turns  to  the  de- 
velopment of  it  for  support.  He  recalls  that  in  plants  with  sword- 
shaped  leaves  the  leaf  blade  (Oberblatt)  arises  as  an  outgrowth  of  the 


Chapter  II  —  31  —  Sarracenia 

back  mass  (abaxial  side)  of  the  leaf  base  (Goebel  i88i),  which 
then  enlarges  its  own  apex  behind  and  above  the  "primary  leaf  apex," 
that  of  the  leaf  base  proper. 

The  development  of  the  embryo  leaf  follows  the  same  course  except 
that  the  upper  side  of  the  primordium  of  the  lamina  is  not  completely 
suppressed  but  is  limited  to  a  minute  depression  between  the  leaf 
base  and  the  apex  of  the  leaf  blade  (Oberblatt).  This  is  limited 
below  by  an  as  yet  extremely  narrow  transverse  zone,  which  cor- 
responds to  the  transverse  zone  of  a  peltate  leaf,  and  at  the  same 
time  may  be  taken  as  an  indication  of  a  unifacial  petiole  primordium, 
one,  however,  which  experiences  no  further  development.  It  is  im- 
portant to  note  that  the  leaf  blade  apex  does  not  rise  much  above 
that  of  the  leaf  base  and  that  therefore  the  leaf  blade  stands  nearly 
normal  to  the  base.  This,  however,  soon  changes.  The  apex  now 
grows  rapidly  and  the  primordium  widens,  flattening  dorsiventrally, 
and  changes  in  curvatures  ensue  to  produce  the  helmet-shaped  form 
of  the  lid.  Meanwhile  the  adaxial  side  elongates  and  the  keel  appears, 
below  which  the  transverse  weal  of  the  leaf-base  runs;  otherwise  said, 
the  edges  of  the  leaf  base  are  not  concurrent  with  the  keel.  The 
similarity  to  the  Iris  leaf  is  unmistakable,  only  allowing  that  the  leaf 
blade  is  hollow.  Thus  the  unifacial  character  of  the  leaf  blade  comes 
into  expression,  not  as  a  shallow  saucer  but  as  a  narrow  furrow.  The 
upper  side  of  the  lamina  primordium  is  at  first  confined  to  the  adaxial 
side  of  the  leaf  blade.  Growth  progresses  less  by  spreading  than  by 
upward  growth  of  the  margins  to  form  the  tubular  leaf.  The  petiole 
is  not  developed,  but  instead  the  blade  greatly  lengthens,  in  S.  flava 
to  the  extent  of  i  meter.  The  terminal  portion,  whose  edges  are 
free,  becomes  the  lid. 

I  have  examined  the  development  of  the  leaf  of  5.  minor  and  can 
generally  agree  with  Troll.  In  this  species,  however,  the  primordia 
stand  out  perhaps  more  clearly  because  of  the  greater  tendency  to 
grow  in  length,  as  compared  with  S.  purpurea.  In  this,  however,  all 
leaves  do  not  act  ahke,  for  there  is  sometimes  a  greater  lengthening 
of  the  petiolar  region,  so  that  even  in  this  species  the  petiole  is  not 
absent,  though  normally  much  reduced  (2  —  12). 

In  S.  minor  the  earliest  stage  of  development  available  was  a  leaf 
only  0.1  mm.  in  height  in  the  form  of  a  low  cone,  its  base  reniform, 
about  0.4  mm.  in  greatest  diameter,  its  convex  edge  adaxial  (3 —  13). 
The  extremities  of  this  edge  had  a  talus-like  slope,  the  cone  melting 
into  the  overhanging  front  of  the  body  of  the  leaf.  This  rose  to  a 
very  low  apex,  evidently  a  growing  point,  scarcely  evident  as  a 
distinct  boss.  There  could  be  seen  a  very  shallow  groove  from  the 
top  down  the  adaxial  face  of  the  overhanging  mass.  In  this  very 
early  and  undifferentiated  condition  there  is  recognizable  a  leaf  base 
with  very  thick  edges,  a  groove,  a  sign  of  the  coming  invagination, 
and  a  very  low  boss.  It  is  not,  however,  possible  to  locahze  a  definite 
growing  point  for  the  leaf  base,  while  even  at  this  young  stage,  the 
apex  of  growth  of  the  leaf  blade  is  just  visible. 

In  a  leaf  0.3  mm.  (j —  14,  15)  in  height  the  apex  stands  out  well, 
and  below  it  adaxially  one  now  sees  a  short  groove,  the  leaf  base 
margins   distinctly  passing   transversely   across,   some   distance   below 


Francis  E.  Lloyd  —  32  —  Carnivorous  Plants 

the  groove.  But  there  is  no  conclusive  evidence  that  the  only  apex 
ever  seen,  the  leaf-apex,  is  secondary,  as  in  the  case  of  Iris,  though  I 
hesitate  to  deny  the  parallel  accepted  by  Troll. 

In  a  leaf  0.8  mm.  long  (j — 16)  the  initial  groove  is  surrounded 
by  a  Hp  which  is  evidently  the  rim  of  the  pitcher,  surrounding  the 
mouth.  With  further  growth  this  is  raised  upward  on  a  laterally 
compressed  stalk  on  the  adaxial  side  of  which  the  wing  now  appears 
as  a  solid  longitudinal  outgrowth.  In  these  later  stages  it  is  quite 
evident  that  the  margins  of  the  leaf  base  meet  transversely,  and  that 
the  wing  arises  quite  independently  of  it.  The  zone  between  the  lower 
end  of  the  wing  and  the  upper  end  of  the  leaf  base  must,  I  think,  be 
regarded  as  petiolar.  It  is  solid,  and  has  unifacial  structure.  In  the 
mature  leaf  one  can  see  that  the  wing  is,  near  the  mouth,  slightly 
doubled  (j —  17,  18). 

Digestion  and  absorption.  —  It  was  once  thought  that  the  tubular 
leaves  were  a  device  for  holding  water.    Collinson  wrote  to  Linnaeus, 

"the  leaves are  open  tubes,  contrived  to  collect  rains  and  dews, 

to  nourish  the  plant  in  dry  weather."  This  prompted  Linnaeus 
to  regard  Sarracenia  leaves  as  derived  morphologically  from  those 
of  Nymphaea,  but  adapted  to  holding  water  for  its  needs,  thus  enabHng 
it  to  occupy  drier  situations,  incidentally  providing  water  for  thirsty 
birds.  But  as  Goebel,  from  whom  we  have  drawn  these  notes,  re- 
marks, Sarracenia  lives  in  swamps,  a  fact  with  which  William  Bar- 
tram  was  familiar,  but  who  yet  thought  that  the  water  caught  by  the 
hollow  leaves  was  for  the   "  refreshment  "   of  the  plant. 

Goebel,  however,  showed  that  it  is  easy  enough  to  demonstrate 
that  the  pitchers  can  and  do  absorb  a  not  inconsiderable  amount  of 
water:  6.8  cc.  out  of  20  cc,  and  2  cc.  out  of  10  cc.  in  two  cases.  Fibrin 
which  he  introduced  remained  unaffected,  and  meat  extract,  neutral- 
ized with  sodium  carbonate,  was  attacked  by  bacteria.  These  and 
other  similar  experiments  led  Goebel  to  the  conviction  that  while 
absorption  can  take  place,  there  is  no  digestion  beyond  that  attribut- 
able to  bacteria,  and  there  is  no  antiseptic  action.  Previous  to 
Goebel  several  authors  had  expressed  suggestions,  opinions,  even 
convictions  about  the  matter.  Sometimes  the  remarks  made  did 
little  more  than  show  that  a  question  had  arisen  in  the  mind,  as  in 
the  case  of  Macbride  (1817).  Hooker  (1875)  merely  recognized  a 
possibility  that  digestion  occurs.  Mellichamp  (1875)  was  the  first 
to  do  some  experiments  which,  though  crude,  led  him  to  conclude  that 
the  fluid  of  the  pitchers  hastens  the  decomposition  of  insects,  without 
at  all  evaluating  the  role  of  bacteria.  Batalin  (1880)  interpreted  the 
exfoliation  of  the  cuticle  in  the  deeper  zone  of  the  pitcher  as  evidence 
that  in  the  absence  of  glands,  which  he  incorrectly  stated  to  be  absent 
from  Sarracenia,  digestive  stuffs  (Losungsmittel)  for  the  solution  of 
proteins  were  released.  No  experiments  to  prove  the  occurrence  of 
digestion  were  done.  Schimper  (1882)  showed  that  changes,  due  to 
the  absorption  of  food  materials,  occur  in  the  epidermal  cells  similar 
to  the  changes  called  aggregation  by  Darwin,  but  he  could  not  find, 
from  experiments,  that  there  is  evidence  of  digestion  aside  from  bac- 
terial action.  That  nitrogenous  compounds  are  absorbed  was  shown 
by  HiGLEY  (1885).    Zipperer  (1885),  concerned  chiefly  with  anatomy, 


Chapter  II  —  33  —  Sarracenia 

did  only  two  superficial  experiments,  one  proving  to  his  mind  that 
diastase,  and  a  second  that  a  pepsin  is  present. 

Following  GoEBEL,  Lambert  (1902)  showed  absorption  to  take 
place  in  certain  regions,  by  following  the  entrance  of  methylene  blue 
or  fuchsin.  That  digestion  occurs  was  no  more  than  a  conviction 
without  proof.  Fenner  (1904)  like  Schimper  observed  that  absorp- 
tion takes  place  and  is  followed  by  cytological  changes  in  the  epider- 
mal cells.  He  observed  quantitatively  considerable  amounts  of  fluids 
absorbed.  As  to  digestion  he  expressed  the  opinion  that  Sarracenia 
flava  is  an  insectivorous  plant  with  a  digestive  enzyme.  Robinson 
(1908)  found  evidence  that  sucrose  and  starch  can  be  digested  to, 
presumably,  simple  sugars  by  the  pitcher  fluid,  confirming  Zipperer 
as  to  starch,  but  none  that  there  is  either  fat  or  protein  digestion. 

Thus  stood  the  evidence  when  in  1918  Hepburn,  St.  John  and 
Jones  started  their  exhaustive  studies  on  these  physiological  questions 
presented  by  Sarracenia  (and  Darlinglonia,  mentioned  elsewhere). 
These  authors  did  an  immense  lot  of  work  and  travelled  extensively 
for  the  purpose  of  doing  field  experiments.  To  their  results  we  now 
turn. 

For  the  purpose  of  learning  about  the  presence  or  absence  of 
digestion,  they  examined  5.  flava,  Drummondii,  Sledgei,  rubra,  minor, 
psittacina  and  purpurea.  Tests  were  made  on  the  fluid  from  both 
unopened  and  opened  pitchers,  with  and  without  the  addition  of  weak 
acid  (HCl)  and  alkali  (sodium  carbonate),  and  always  in  the  presence 
of  trikresol  as  a  bactericide.  Carmine  fibrin  was  used  as  a  substrate 
in  the  field,  and  this,  edestin,  casein  and  coagulated  egg  albumin  in 
the  laboratory.  The  evidence  was  strengthened  by  duplication,  trip- 
lication, or  even  quadruplication  of  the  tests.  Generally  composite 
samples  of  fluid  drawn  from  a  number  of  pitchers  were  used.  All 
experiments  were  done  quantitatively,  even  to  measuring  the  amount 
of  substrate,  a  matter  of  importance  often  disregarded. 

In  S.  flava  a  protease  was  shown  to  act  on  fibrin  in  both  closed 
(that  is,  still  unopened)  and  open  pitchers.  It  is  more  active  in  weak 
acid  (0.2%),  than  in  weak  alkali,  but  there  was  no  action  in  their 
absence.  Edestin  was  digested  in  1.5  to  2  hours.  The  fluid  from  closed 
pitchers  was  vigorous,  acting  completely  in  30  min.  at  37.5°  C.  and 
almost  so  at  room  temperature.  Casein  was  partially  digested  in  2 
hours.     With  coagulated  egg-white  negative  results  only  were  obtained. 

S.  Drummondii  and  S.  Sledgei.  —  When  the  fluid  of  closed  pitchers 
was  acidified  and  then  tested  the  results  were  purely  negative.  With 
that  of  open  pitchers,  six  experiments  of  eight  were  negative,  but 
partial  or  complete  digestion  occurred  in  two  on  sustained  exposure 
(49-57  days).  When  neither  acid  or  alkali  were  added  the  fluid  of 
closed  pitchers  failed  to  act  even  after  50-55  days  in  four  experiments; 
in  two  others  digestion  occurred  in  7  and  21  days  respectively  for  S. 
Drummondii.  For  5.  Sledgei  one  experiment  was  negative,  while 
others  acted  slowly  but  completely  in  37  to  49  days.  The  results 
stand  in  marked  contrast  with  those  in  which  the  fluid  was  modified 
by  alkali,  showing  that  digestion  occurred  in  1.5  to  18  days  in  20  ex- 
periments, while  in  two  others  it  required  32-36  days,  the  slowness 
being   due   to   a   reduced   concentration   of   sodium   carbonate,   which 


Francis  E.  Lloyd  —  34  —  Carnivorous  Plants 

was  probably  neutralized  by  the  acid  proper  to  the  fluid  which  had 
been  shown  to  be  present.  There  was  no  marked  difference  between 
the  fluid  of  open  and  of  closed  pitchers.  It  was  concluded  that  a 
protease  was  present  which,  however,  acted  best  in  an  alkaline  medium. 

Edestin  was  slightly  attacked  by  the  fluid  of  open  pitchers.  Casein 
was  digested  completely  in  2-8  hours  at  37.5°  C,  and  coagulated 
egg-white,  in  the  absence  of  acid  or  alkali,  was  not  attacked,  nor  was 
it  in  the  presence  of  acid,  but,  on  the  addition  of  alkah,  "incipient 
digestion  was  noted  in  24  hours,  marked  digestion  in  48  and  144 
hours  and  advanced  digestion  in  168  and  216  hours  respectively"  for 
two  experiments. 

S.  rubra.  —  Only  a  single  sample  of  fluid  was  available,  but  this 
on  division  showed  that  in  the  presence  of  alkali  digestion  proceeded 
rapidly,  o.oi  gram  of  fibrin  being  completely  digested  in  1.3  cc.  of 
fluid  in  2  hours.  In  the  part  with  acid  added  "partial  solution  was 
noted  at  the  end  of  9  days,  complete  solution  at  the  end  of  50  days." 

S.  minor.  —  Experiments  were  done  in  the  field.  No  digestion  oc- 
curred in  30  days  (trikresol  present)  in  the  absence  of  acid  or  alkali, 
but  it  did  occur  when  either  acid  or  alkali  was  added  to  the  fluid, 
but  less  vigorously  in  the  alkaline,  than  in  the  acid  medium.  This 
species   therefore    stands   in    contrast    to    the    others    aforementioned. 

S.  psittacina.  —  Field  observation  showed  that  fluid  was  being  se- 
creted in  the  pitchers,  but  in  such  small  amounts  that  it  had  to  be 
collected  by  dilution  with  water  (0.5  cc.  in  each  of  50  pitchers  free 
of  insects).  The  results  were  inconclusive,  but  indicated  that  a  pro- 
tease is  present  which  is  active  in  the  presence  of  acid. 

Sarracenia  purpurea.  —  The  secretion  in  this  species  is  very  small 
in  amount,  being  found  as  beads  of  moisture  on  the  walls.  Experi- 
ments were  done  by  flushing  the  pitchers,  emptying,  and  adding  10 
to  15  cc.  of  water  to  each  pitcher.  After  some  days  this  was  removed 
and  tested.  The  fluid  thus  obtained  showed  an  ability  when  alka- 
line to  digest  fibrin  to  a  marked  extent  in  8,  24,  72,  and  87  hours 
(4  samples),  and  completely  in  42,  48,  120,  and  135  hours,  respectively. 
Three  other  experiments  gave  positive  results  in  42  and  87  hours. 
In  acid,  the  results  were  equivocal. 

The  general  conclusions  reached  by  Hepburn  and  his  colleagues 
are  that  a  protease  is  present  in  all  the  Sarraceniae,  but  that  in  most 
cases  it  acts  best  in  an  alkaline  medium.  In  some  cases,  however,  it 
acts  in  an  acid  medium. 

It  was  shown  experimentally  that  pitcher  fluid  retains  its  power 
of  digestion  after  being  kept  at  room  temperature  for  as  long  as  370 
days,  either  with  or  without  a  bactericide;  and  that  this  is  also  re- 
tained on  dilution,  which  is  of  importance  in  view  of  the  fact  that 
dilution  by  rain  may  always  be  expected  in  the  habitat.  In  contrast 
with  Nepenthes,  neither  mechanical  nor  food  stimulation  was  found 
to  have  any  effect. 

In  the  fluid  of  closed  pitchers  there  is  evidence  that  there  are  both 
invertase  and  lipase,  while  maltase,  emulsin,  diastase,  urease,  and 
esterase  were  present.  It  will  be  recalled  that  Zipperer  claimed  the 
digestion  of  starch  and  Robinson  that  of  sucrose  and  starch. 

It  is  generafly  understood  that  the  water  of  swamps  and  sandy 


Chapter  II  —  35  —  Sarracenia 

soils  is  acid,  though  not  always.  Wherry  found  bog  water  to  be 
sometimes  alkahne,  though  the  sphagnum  hummocks  would  contain 
acid  water.  Generally  he  found  that  when  growing  in  acid  water, 
the  pitcher  fluid  was  acid,  but  not  always  in  the  same  degree.  But 
occasionally  the  fluid  would  be  alkaline  or  neutral.  On  the  same 
plant  the  fluid  of  a  young  pitcher  might  be  alkaline,  and  of  old  pitchers 
acid  —  this  for  Sarracenia  purpurea.  Hepburn  et  al.  found  for  some 
southern  species  acidity  and  alkalinity  about  equally  distributed  for  S. 
Drummondii  and  S.  Sledgei.    Five  pitchers  of  S.  flava  all  held  acid  fluid. 

Hepburn  and  St.  John  examined  the  bacterial  content  of  closed 
and  open  pitchers.  Closed  pitchers  were  always  sterile.  The  fluid 
of  open  pitchers  which  had  captured  prey  always  contained  bacteria, 
as  is  to  be  expected,  and  these  always  digested  several  different  sub- 
stances. The  interesting  fact  is  pointed  out,  however,  that  these 
"bacteria  digested  the  proteins  so  slowly  that  their  part  in  the  di- 
gestion of  prey  must  be  a  minor  one  in  the  genus  Sarracenia,  the 
protease  of  the  pitcher  liquor  playing  the  leading  role."  "The  bac- 
teria apparently  live  in  symbiosis  with  the  Sarracenias,  drawing  their 
nutriment  from  the  digested  insects,  and  aiding,  to  a  certain  extent, 
in  the  digestion  of  the  prey."  An  exception  must  be  made  for  Dar- 
lingtonia  where  there  is  no  digestion  by  the  pitcher  fluid  proper  (see 
beyond).  Reference  is  made  to  the  odors  of  putridity  and  of  am- 
monia and  amines  noticed  when  such  bacteria  are  active. 

The  earHer  observations  of  others  that  water  is  absorbed  was 
verified,  and  it  was  further  found  that,  when  nitrogenous  substances 
in  solution  were  used,  the  absorption  of  the  solutes  proceeded  more 
rapidly  than  that  of  the  water.  In  the  presence  of  a  phosphate  buffer, 
the  nitrogenous  compound  would  be  absorbed  while  the  total  amount 
of  water  increased.  When  a  neutral  phosphate  solution  was  used, 
the  absorption  of  the  phosphate  was  less  rapid  than  that  of  the  water. 
The  percentage  of  compound  absorbed  usually  increased  with  the 
length  of  the  period  of  absorption.  The  actual  entrance  of  substances 
into  the  tissues  was  demonstrated  by  the  presence  of  the  lithium  ion, 
after  introducing  lithium  citrate  into  the  pitcher  fluid.  It  is  thus 
indicated  that  the  products  of  proteolysis  and  phosphates  are  ab- 
sorbed by  the  walls  of  the  pitcher  and  utilized  by  the  plant.  Data 
on  the  chemical  composition  of  the  tissues  are  also  furnished,  but 
are  of  only  secondary  interest  here. 

This  brief  summary  of  the  work  of  Hepburn  and  his  colleagues, 
it  is  gratifying  to  record,  has  furnished  a  comprehensive  view  of  the 
physiology  of  the  pitchers  of  Sarracenia  in  its  relation  to  digestion, 
which  might  have  remained  unwritten  but  for  their  evident  enthusiasm 
and  dihgence. 

Animals  which  live  in  the  pitchers  of  Sarracenia  and  Darlingtonia.  — 
It  is  a  matter  of  common  observation  that  the  pitcher  plants  attract 
a  horde  of  insects  of  all  kinds:  "ants,  wasps,  bees,  butterflies  and 
moths"  by  their  nectar,  and  other  forms  (beetles,  spiders)  for  other 
reasons.  Spiders  frequent  the  opening  of  the  pitcher  in  the  not  vain 
hope  of  visits  of  small  insects  which  may  be  caught  by  them.  Ed- 
wards observed  this  in  Darlingtonia.  They  occur  on  Drosera,  Byblis, 
Nepenthes  and  probably  others  for  the  same  reasons.     Minute  wasp- 


Francis  E.  Lloyd  —  36  —  Carnivorous  Plants 

like  creatures  parasitize  pitcher  inhabitants.  The  caterpillars  of  a 
moth  live  in  burrows  formed  by  feeding  on  the  tissues  of  the  rhizome, 
and  form  characteristic,  more  or  less  upright,  above-ground  tubes 
of  the  debris.  This  is  Papaipema  appassionata,  the  moth  being  maroon 
and  yellow  in  color.  Of  especial  interest  here  are  those  which  habitu- 
ally use  the  pitchers  as  their  homes,  and  live  in  them  and  nowhere 
else.  They  fijid  their  food  either  in  the  tissues  of  the  pitcher  walls, 
or  in  the  mass  of  dead  insects  caught  by  the  trap,  or  merely  live  in 
the  water  from  which,  however,  they  must  derive  their  food.  Animals 
other  than  insects  include  a  small  tree-toad  and  a  small  chameleon 
lizard,  whose  bones  are  sometimes  found  in  the  inclosed  debris.  The 
toad  rests  just  inside  the  mouth  of  the  pitcher,  doubtless  awaiting 
the  chance  of  capturing  prey.  But  to  come  to  the  obligate  inhabit- 
ants : 

A  small  mosquito  {Wyeomyia  Smithii)  lays  its  eggs  in  the  pitchers 
of  Sarracenia  purpurea.  In  the  pitcher  fluid  (always  diluted  by 
rains)  the  larvae  grow  to  maturity,  hibernating  frozen  in  ice  during 
the  winter.  It  is  harmless  to  man.  It  is  said  not  to  breed  elsewhere, 
and  is  found  well  beyond  the  Canadian  border,  though  it  is  tropical 
in  its  affinities. 

Similarly  the  larvae  of  a  minute  gnat,  Metriocnemus  Knabi,  breeds 
in  the  same  manner.  A  closely  related  species,  M.  Edwardsii,  de- 
scribed by  Jones  (191 6),  was  discovered  to  occur  in  the  pitchers  of 
Darlingtonia  californica  by  Mrs.  Austin  about  the  year  1875.  The 
larvae  are  minute  thread-Uke  "worms"  circulating  in  the  decaying 
insect  debris,  which  appears  as  writhing  masses,  so  numerous  are  the 
larvae.  According  to  Hepburn  and  Jones  (1919),  such  forms  pre- 
serve themselves  against  the  digestive  action  of  the  surrounding  fluid 
by  means  of  antienzymes.  In  this  connection  it  may  be  mentioned 
that,  in  discussing  the  anthelmintic  action  of  papain  (in  the  crystal- 
line form),  Berger  and  Asenjo  (1940)  tested  the  effect  of  this  enzyme 
on  Ascaris  lumhricoides  (from  pig  intestine)  and  found  that  these 
organisms  were  attacked,  that  is,  ulcerations  were  formed  on  them 
inside  of  16  hours  in  a  0.02%  solution  in  a  phosphate  buffer  of  pH  5, 
and  the  animals  were  completely  digested  in  16  hours  in  a  0.11%  solu- 
tion. The  same  authors  showed  that  the  bromelin  of  fresh  pineapple 
juice  acts  similarly.  Evidently  Ascaris  has  no  sufficient  protection 
against  this  enzyme  in  the  concentrations  used,  though  presumably  it 
has  an  antienzyme  which  protects  it  within  its  normal  environment. 

The  most  intriguing  of  all  the  animal  associates  are  three  closely 
related  species  of  a  small  moth  of  the  genus  Exyra,  because  of  the 
striking  adaptations  which  they  display  to  a  special  environment 
(Jones  192 i).  These  moths  lay  their  eggs  singly  or  in  groups  in  the 
mouth  of  the  pitcher.  When  laid  singly,  the  hatched  larva  enters 
the  tube  and  feeds  on  the  superficial  tissues  of  its  wall.  This  is  true  of 
the  species  Ridingsii  and  semicrocea.  If  more  than  one  larva  happens 
to  occupy  a  pitcher,  one  of  them  ruthlessly  drives  out  or  kills  its 
neighbors.  The  third  species,  Rolandiana,  lays  a  group  of  eggs  in  a 
pitcher  of  a  single  plant  (of  S.  purpurea),  and  when  hatched  the 
larvae  spread  to  various  closely  placed  pitchers,  readily  possible  in 
this  species  because   of  the   dense   massing  of   the  pitchers   (z — 3). 


Chapter  II  —  37  —  Sarracenia 

Eventually  only  a  single  larva  occupies  a  pitcher.  The  wide  separa- 
tion of  pitchers  of  5.  jlava,  rubra,  Drummondii,  Sledgei  and  minor  are 
a  practical  hindrance  to  such  movements  of  very  young  larvae  from 
one  pitcher  to  the  other,  and  it  is  in  these  that  the  other  species  of 
£^>'m  lay  their  eggs  singly.  "Thus,"  says  F.  M.  Jones,  "the  habit 
of  growth  of  the  food  plant  determines  the  egg-laying  habit  of  the 
associated  insect"  (1921). 

The  newly  hatched  larva  is  very  small  (2.6  mm.),  and  being  trans- 
lucent and  half  buried  in  the  tissues  on  which  it  feeds  and  partly 
covered  by  debris  enclosed  within  the  tube,  seems  pretty  well  pro- 
tected without  further  ado.  E.  Ridingsii  on  hatching  retires  to  the 
grooves  in  the  hd-stalk  of  S.  flava,  and  there  forms  for  itself  a  small 
tent  of  silk  and  frass,  on  the  floor  of  which  it  continues  feeding.  The 
older  larvae  of  all  three  species  make  use  of  a  method  of  isolating 
themselves  from  the  outside  world  as  follows.  They  spin  a  diaphragm 
of  silk  webbing  across  the  mouth  of  the  tube,  either  transversely  or 
more  or  less  obliquely  according  to  the  position  of  the  hd,  and  in 
5*.  psittacina,  across  the  mouth  of  the  entrance  tube.  Any  accidental 
openings  are  closed  by  webbing,  and  thus  they  immure  themselves 
in  a  food  chamber  from  which  rain  is  prevented  entrance.  Larvae 
of  a  spring  brood,  when  they  find  themselves  in  young  tender  pitchers, 
use  another  quite  extraordinary  method  of  insuring  for  themselves  a 
safe  retreat.  The  young  larva  then  eats  away  a  ringing  groove  near 
the  top  of  the  pitcher.  Above  this  the  pitcher  wall  dies,  dries,  and 
becomes  indurated,  sagging  over  and  barring  the  entrance.  In  the 
chamber  thus  formed  the  larva  feeds  and  hibernates.  In  the  pitchers 
of  S.  flava,  which  die  down  during  the  winter,  the  larva  retires  to  the 
lower  regions  of  the  pitcher,  and  there  ensconces  itself  in  a  chamber 
plugged  by  webbing  and  frass,  where  it  awaits  the  spring.  A  curious 
variant  of  this  habit  is  displayed  by  the  caterpillar  of  Exyra  Ridingsii, 
which  before  pupation  prepares  for  the  future  by  cutting  an  emergence 
hole  above  its  point  of  pupation,  so  that  the  moth  may  easily  escape, 
and  below  a  small  hole  for  the  drainage  of  water,  so  that  its  pupation 
chamber  may  not  be  flooded.  It  then  forms  its  chamber  by  webbing 
spun  loosely  so  as  to  allow  water  to  pass,  and  then  spins  its  cocoon 
of  webbing  and  frass.  Exyra  semicrocea,  when  it  pupates  in  the  pitchers 
of  S.  psittacina,  handles  its  situation  somewhat  similarly,  but  with 
special  attention  to  the  peculiarities  of  the  host  plant.  Usually  when 
the  larva  intends  to  pupate  it  passes  into  an  uninjured  pitcher.  Since 
that  of  5".  psittacina  has  a  lobster-trap  entrance,  out  of  which  escape 
would  be  difficult  — not  because  of  the  size  of  the  opening,  but  be- 
cause of  its  re-entrant  character  —  the  larva  first  cuts  an  escape  hole 
in  the  roof  region  of  the  hood. 

After  hibernation  the  larvae  (the  third  instar),  are  voracious,  and, 
emerging  in  the  spring,  attack  not  only  the  pitcher,  but  the  flowers 
and  young  fruit  which  they  devour.  When  ready  to  pupate  the  larva 
cuts  a  hole  in  a  young  growing  leaf  still  unopen,  ascends  the  tube, 
and  feeds  on  the  inner  tissues.  This  causes  the  tops  of  the  pitchers 
to  wither  and  the  dead  portion  to  topple  over.  E.  Rolandiana  does 
the  same  in  S.  purpurea.  The  larvae  of  these  moths  have  lateral 
tubercles  or  "lappets"  which,  according  to  Jones,  prevent  them  from 


Francis  E.  Lloyd  —  38  —  Carnivorous  Plants 

entering  and  so  getting  pinched  in  too  narrow  spaces.  The  species 
{E.  Rolandiana)  pecuhar  to  S.  purpurea,  with  its  wide,  amply  spacious 
pitcher,  does  not  possess  the  lappets.  These  in  the  very  young  larvae 
are  scarcely  more  than  bristles,  but  with  successive  instars  the  tubercle 
becomes  larger,  and  armed  with  a  prominent  bristle. 

A  solitary  wasp,  Chlorion  Harrisi,  habitually  makes  use  of  Sar- 
racenia  pitchers  for  its  nest  of  several  stories  which  are  supplied  with 
food  and  each  an  egg.  Dr.  Jones  informs  me,  however,  that  this 
insect  is  not  confined  to  Sarracenia.  He  found  it  in  1939  nesting  in 
abandoned  beetle-burrows  on  Martha's  Vineyard,  Vineyard  Island, 
where  Sarracenia  does  not  occur. 

A  fly,  Sarcophaga,  produces  large  white  maggots  which  feed  upon 
the  remains  of  insects  in  the  pitchers.  The  protective  enzyme  studied 
by  Hepburn  and  Jones  was  extracted  from  Sarcophaga  larvae.  Sev- 
eral species  of  this  genus,  peculiar  to  Sarracenia,  were  described  by 
Riley. 

There  is  a  minute  fly  (2-3  mm.),  Dorniphora  venusta,  which  is  found 
in  the  pitchers  of  6*.  flava  late  in  the  season  when  they  are  relatively 
dry  and  have  lost  their  trapping  abilities,  as  they  apparently  do 
(Jones,  191 8).     The  larva  feeds  upon  the  captured  insects. 

Another  small  fly,  3-3.8  mm.  in  length,  described  under  the  name 
Neosciara  Macfarlanei  by  F.  M.  Jones  (1920)  has  similar  habits,  and 
is  found  in  the  vertical  tubed  Sarracenias.  Its  presence  is  betrayed 
by  a  frothy  looking  product  of  the  larvae  about  to  pupate,  which 
fills  the  pitcher  tube  just  above  the  mass  of  dead  insects  on  which 
they  have  fed.  Both  these  flies,  as  well  as  the  Sarcophagids  above 
mentioned,  appear  to  be  confined  to  Sarracenia,  but  some  doubt 
remains  as  to  this. 

The  purpose  of  the  above  brief  account  is  merely  to  point  out 
the  more  general  facts  about  the  constant  insect  associates  of  Sar- 
racenia and  Darlingtonia.  To  exhaust  the  present  knowledge  of  all 
the  insects  which  attack  and  feed  upon  and  pollinate  these  plants 
would  go  beyond  our  purpose.  A  general  summary  of  this  knowledge 
is  supplied  by  Jones  in  Walcott's  book  of  illustrations  of  the  Sar- 
racenias, in  which  a  bibliography  is  to  be  found.  It  is  upon  this 
author  that  I  have  depended  for  these  notes.  It  may  be  added  as  a 
matter  of  speculation  that  further  investigation  would  certainly  dis- 
cover many  other  associates,  including  Crustacea,  protozoa  and  pro- 
tophyta,  some  of  which  might  turn  out  to  be  obligate  inhabitants, 
as  in  the  case  of  Nepenthes. 

Literature  Cited: 

Arber  {see  under  Cephalotus). 

Baillon,  H.,  Sur  le  developpement  des  feuilles  des  Sarracenia.  C.  r.  Acad.  Sci.  Paris 
71:630,  1870.     Also  in  Adansonia  9:331,  1868-1870  {through  Troll). 

Bartram,  Wm.,  Travels  in  N.  and  S.  Carolina,  Georgia  and  Florida.      Philadelphia  1791. 

Batalin,  a.,  tJber  die  Function  der  Epidermis  in  den  Schlauchen  von  Sarracenia  und 
Darlingtonia.    Acta  Hort.  Petropol.     7:345-359,  1880. 

Berger,  J.  &  C.  F.  Asenjo,  Anthelmintic  activity  of  crystalline  papain.  Science  II,  91: 
387-388,  1940. 

Burnett,  G.  T.,  On  the  functions  and  structure  of  plants,  with  reference  to  the  adumbra- 
tions of  a  stomach  in  vegetals.  Quart.  Journ.  Sci.  Lit.  and  Art,  Vol.  for  Jy.-Dec, 
1829:279-292. 


Chapter  II  —  39  —  Sarracenia 

Canby,  W.  M.,  Darlingtonia  calif ornica,  an  insectivorous  plant.     Proc.  A.  A.  A.  S.   1875, 

6:64-72. 
Catesby,  Nat.  Hist,  of  Car.,  Vol.  2,  p.  69,  1743  {through  Hooker). 
CoLLiNsoN,  (see  Smith  1765). 
Darwin,  (see  under  Drosera). 

DucHARTRE,  P.  E.,  Elemcns  de  botanique.     Paris  1867  (through  Troll). 
Fenner  (see  under  Nepenthes).  . 

GoEBEL,  K.,  Blattentwickelung  von  Iris  (under  the  heading  of  "Litteratur").    Bot.  Zeitung 

39:95-101,  1881. 
GoEBEL,  K.  (see  also  under  Nepenthes). 

Gray,  Asa,  Sarraceniaceae.  Synoptical  Flora  of  North  America  1:79,  1895-7,  New  York. 
Hegner,  R.  W.,  The  protozoa  of  the  pitcher  plant  (Sarracenia  purpurea).    Biol.  Bull.  50: 

271-276,  1926.  .  J    II-  J 

Hepburn,  J.  S.,  F.  M.  Jones,  &  Eliz.  Q.  St.  John,  The  absorption  of  nutrients  and  allied 

phenomena  in  the  pitchers  of  the  5(Z?-raceH/aceae.    Journ.  Franklin  Inst.  189:147-184,  1920. 
Hepburn,  Jones  &  St.  John,  The  biochemistry  of  the  American  pitcher  plants  (Secondary 

title:    Biochemical   Studies  of  the  North  American  Sarraceniaceae).     Trans.   Wagner 

Free  Inst,  of  Science  11:1-95,  1927-     Full  bibhography. 
Higley,  Bull.  Chic.  Acad.  Sci.  1:41-55,  1885  (through  Hepburn). 
Hooker,  J.  D.,  Address  to  the  Department  of  Botany  and  Zoology.    Rep.  44th  Meeting 

Brit.  As.  Adv.  Sci.  Belfast  1874:102-116,  1875. 
Jones,  F.  M.,  Pitcher-plant  insects.     Ent.  News  15:14-17,  1893. 
Jones,  F.  M.,  Pitcher-plant  insects,  II.     Ibid.     18:413-420,  1907. 
Jones,  F.  M.,  Pitcher-plant  insects.  III.     Ibid.     19:150-156,  1908. 
Jones,  F.  M.,  Two  insect  associates  of  the  California  pitcher-plant,  Darlingtonia  califor- 

nica.    Ibid.  27:385-392,  191 6. 
Jones,  F.  M.,  Domiphora  venusta  Coq.  in  Sarracenia  flava.     Ibid.  29:299-302,  igis. 
Jones,  F.  M.,  Another  pitcher-plant  insect.     Ibid.  31:91-94,  1920. 
Jones,  F.  M.,  Pitcher  plants  and  their  moths.     Nat.  Hist.  21:296-316,  1921. 
Jones,  F.  M.,  Pitcher  plants  and  their  insect  associates.     In  Walcott,  1935,  pp.   25-34- 
Krafft  (see  under  Heliamphora). 

Lambert,  Ann.  de  Hygiene  et  de  Med.  col.  Paris  1902,  5:652-662  (through  Hepburn). 
Lindley,  J.,  Introduction  to  Botany.     London,  1832. 
Macbride,  James,  Trans.  Linn.  Soc.  London  12:48-52,  1817. 
MacDougal,  D.  T.,  Symbiotic  saprophytism.     Ann.  Bot.  13:1-47,  1899. 
MacDougal,  D.  T.,  The  influence  of  light  and  darkness  upon  growth  and  development. 

Mem.  N.  Y.  Bot.  Gard.  2,  319  pp..  New  York  1903. 
Macfarlane,  J.  M.,  &  D.  W.  Steckbeck,  Sarracenia  purpurea  var.  stolonifera,  A  note- 
worthy morphological  and  ecological  type.    Bull.  Misc.  Inform.  Kew,  No.  4, 1933:161-169. 
Macfarlane  (see  also  under  Nepenthes). 
Mellichamp,  J.  H.,  Notes  on  Sarracenia  variolaris.    Proc.  .\m.  Ass.  Adv.  Sci.  23  meeting. 

MoRREN,'  Ch.,   Morphologic   des   ascidies.      Bull.   Acad.   R.   Belg.   Bruxelles   5:430,    1838 

(through  Troll).  ■  ,      /  j 

Riley,  C.  V.,  On  the  insects  more  particularly  associated  with  Sarracema  varwlus  (spotted 

trumpet-leaf).     Proc.  A.  A.  A.  S.  1875,  6:18-25. 
Robinson,  Winifred  J.,  A  study  of  the  digestive  power  of  Sarracema  purpurea,     lorreya 

8:181-194,  1908. 
Saint-Hilaire,  a.  DE,  Legons  de  botanique  etc.     Paris  1840  (n.v.). 
ScHiMPER,  A.  F.  W.,  Notizen  uber  insectenfressenden  Pflanzen.     Bot.  Zeitung  40:225-234; 

241-248,  1882. 
Smith,    Correspondence   of   Linneaus.     Vol.    i,   p.   69,    1821.      Reference   to   Collinson 

(through  Hooker,  1875). 
Troll,  W.,  Morphologic  der  schildformigen  Blatter.     Planta  17:153-314,  i932- 
Uphof,  J.  C.  Th.,  Sarraceniaceae.     Die  naturlichen  Pflanzenfamilien,   2.  Aufl.,  Vol.   17b: 

1-24,  1936.  .  . . 

Vogl,   a.,   Phytohistologische   Beitrage,   II.     Die   Blatter  der  Sarracenia  purpurea  l>mn. 

Sitzungsber.  Wien.  Akad.  Wiss.  Math.-Wiss.  Kl.  50:281-301,  1864. 
Walcott,  Mary  V.,  Illustrations  of  North  American  pitcher  plants.     Smith.  Inst.  Wash. 

1935  (containing  contributions  by  Wherry  and  by  Jones). 
Wherry,  E.  T.,  Acidity  relations  of  the  Sarracenias.  Journ.  Wash.  Acad.  Sci.  19:379-39°,  1929- 
Wherry,   E.   T.,   The   geographic   relations   of   Sarracenia   purpurea.     Bartoma   No.    15, 

Wherry,  E.  T.,  Exploring  for  plants  in  the  southeastern  states.  Sci.  Mo.  38:80-85,  1934- 
Wherry,  E.  T.,  Distribution  of  the  North  American  pitcher  plants.  Walcott,  1935,  Pp.  1-23. 
Wilson,  W.  P.,  On  the  relation  of  Sarracenia  purpurea  to  S.  variolaris.     Proc.  Acad.  Nat. 

Sci.  Phila.  1888:10-11.  ivt     •  u 

Zipperer,  Paul,  Beitrag  zur  Kenntnis  der  Sarraceniaceen.     Diss.  Univ.  Erlangen.     Munich 

1885,  Pp.  34- 


Chapter    III 
DARLINGTONIA   CALIFORNICA 

Discovery.  —  Distribution.  —  Habit.  —  Leaves :  kinds.  —  Structure.  —  Place  of  absorp- 
tion. —  Development  of  leaf.  —  Digestion  and  absorption. 

The  genus  name  Darlingtonia  is  used  here  because  of  its  wide 
familiarity  and  use  in  horticultural  literature.  Under  the  International 
Rules  of  Botanical  Nomenclature  this  name  is  invalid  because  of  being 
a  later  homonym,  and  is  to  be  replaced  by  Chrysamphora  Greene. 

This  highly  localized  pitcher  plant  of  Oregon  and  California  called 
locally  the  ''cobra  plant''  was  discovered  in  October  1841  by  Mr.  J.  D. 
Brackenridge,  Assistant  Botanist  of  the  U.  S.  Exploring  Expedition, 
under  Captain  Wilkes,  on  a  journey  from  Oregon  to  San  Francisco. 
It  was  found  in  a  marsh  bordering  a  small  tributary  of  the  Upper 
Sacramento  River  a  few  miles  south  of  Mt.  Shasta.  In  the  opinion  of 
John  Torrey,  who  described  it  in  1853,  it  was  sufficiently  different  from 
Sarracenia  to  warrant  the  new  generic  name  which  he  gave  it,  dedi- 
cating it  to  his  "esteemed  friend"  Dr.  Willl^.m  Darlington,  of  West 
Chester,  Pa.,  "whose  valuable  works  have  contributed  so  largely  to  the 
scientific  reputation  of  our  country."  The  range  of  this  species  is  now 
known  to  extend  into  the  Siskiyou  Mountains  of  S.  Oregon,  down  to 
sea-level  along  the  coast  (I  found  it  6  miles  north  of  the  town  of 
Florence)  and  in  the  contiguous  region  of  California.  As  an  example 
of  a  restricted  geographical  distribution,  this  is  comparable  to  that  of 
Cephalotus  follicularis  in  S.  W.  Australia. 

Darlingtonia  has  the  same  general  habit  of  growth  as  that  of  the 
other  Sarraceniaceae,  a  strong  perennial  rootstock,  bearing  a  sort  of 
rosette  of  leaves  and  clothed  with  the  dead  remains  of  older  leaves. 
The  larger  leaves  attain  a  length  of  2-3  feet  ("3  ft.  6  in.",  Edwards) 
and  present  a  unique  appearance,  owing  to  the  torsion  of  their  tubes 
and  the  large  motley  domes  with  their  fishtail-shaped  appendages. 
"The  leaves  are  most  beautiful  and  singular,  having  a  fanciful  re- 
semblance to  a  number  of  hooded  yellow  snakes  with  heads  erect 
in  the  act  of  making  a  final  spring,  suggesting  the  name  'caput  ser- 
pentis',"  wrote  Edwards  in  1876.  He  states  that  the  leaves  all  twist 
in  the  same  direction,  which  is  not  the  case   (Kurtz)   {4  —  1-5). 

There  are  two  kinds  of  leaves,  juvenile,  produced  by  seedlings 
and  by  small  shoots,  and  the  leaves  of  maturity.  The  juvenile  leaves 
(5  —  1-4,  6;  6 — 17),  which  have  been  described  by  Goebel,  follow 
directly  on  the  very  simple  lanceolate  cotyledons,  and  on  small  lateral 
shoots  of  restricted  growth  on  rhizomes.  They  are  tubular,  tapering 
downwardly,  with  a  clasping  base.  The  opening  is  oblique,  the  leaf 
being  drawn  out  on  the  abaxial  side  into  a  tapering  acute  or  bifid 
apex.  The  edges  of  the  opening  are  simple,  that  is,  are  not  curved 
in-  or  outwardly.  On  the  adaxial  aspect  the  opening  is  bayed  or 
sometimes  slit  downwards.  The  whole  outer  surface  of  the  leaf  is 
studded  with  somewhat  raised  stomata  and  many  nectar  glands  which 


Chapter  III  —  41  —  Darlingtonia 

scarcely  exceed  the  stomata  in  size.  These  glands  are  found  even 
on  the  outer  surface  of  the  overhanging  apex.  The  inner  surface  can 
be  roughly  divided  into  three  zones.  The  uppermost  embraces  the 
whole  of  the  apex  and  some  distance  into  the  interior  from  the  open- 
ing. The  inside  surface  of  this  portion  is  furrowed  longitudinally  from 
the  extreme  apex  to  a  point  well  within  the  tube.  The  floor  of  this 
furrow  is  lined  with  smooth  epidermis  which  for  some  distance  forms 
a  low  swelling  on  each  side  of  the  furrow.  Among  these  cells  are  a 
very  few  groups  which  have  distinctly  the  structure  of  a  nectar  gland, 
but  I  have  not  been  able  to  determine  positively  that  nectar  is  se- 
creted. They  seem  not  to  be  quite  so  highly  speciaHzed  in  form  at 
least  as  the  glands  of  a  mature  or  adult  type  of  pitcher.  The  epider- 
mis in  general  of  this  zone  is  of  the  "fishscale"  type,  that  is  the  cells 
are  imbricated  and  are  downwardly  sharply  pointed,  the  more  sharply 
the  more  deeply  placed  in  the  pitcher.  As  zone  2  is  reached,  fewer 
of  the  cells  are  trichomes,  which  are  now  much  longer,  the  remaining 
cells  being  quadratic  and  elongated  to  some  extent.  In  the  depths 
of  the  pitcher,  hairiness  ceases,  and  the  epidermis,  in  zone  3,  is  quite 
smooth.  Like  the  senile  leaves,  the  juvenile  tube  leaf  is  twisted 
through  180  degrees  from  base  to  apex,  so  that  the  opening  comes 
to  face  downwards,  more  or  less.  In  size  they  may  be  as  small  as  i 
cm.   and  up  to   10  cm. 

Occasional  juvenile  leaves  display  aberrancies  from  the  normal 
course  of  development.  Rather  frequently  one  finds  a  leaf  with  the 
apex  forked,  and  having  no  median  vein,  clearly  corresponding  to 
the  fishtail  appendage  of  the  adult  leaf.  Accompanying  this  con- 
dition there  may  or  may  not  be  developed  an  ala  ventralis.  In  most 
cases  the  rim  of  the  mouth  remains  simple,  but  in  one  leaf  I  found 
that  a  distinct  nectar  roll  had  been  developed  along  both  sides,  but 
not  meeting  anteriorly,  as  in  the  adult  leaf,  to  fuse  {5  —  3)-  This 
indicates  pretty  clearly  that  the  place  where  the  two  sides  of  the 
nectar  roll  meet  is  a  site  of  concrescence  in  the  fully  elaborated  leaf. 
As  in  all  these  forms  of  juvenile  leaves  there  are  nectar  glands,  which 
are  confined  to  a  broad  band  along  the  inside  of  the  hood  and  apex 
but  not  elsewhere  on  the  inner  surface  ((5— 18).  The  epidermis  is 
all  of  tesselated  umbonate  cells  above,  becoming  longer  pointed  further 
down.  The  glands  are  not  quite  so  elaborate  here  as  in  the  adult 
leaf.     Those  on  the  outer  surface  are  typical  in  appearance. 

A  single  juvenile  leaf  was  found  in  which  there  was  a  closure  of 
the  mouth  for  only  a  short  distance  above  the  base.  What  might 
have  been  the  tube  was  laid  quite  open,  and  formed  no  trap  at  all. 
Glands  were  present  on  the  apical  appendage  and  along  a  midband, 
as  usual.  The  epidermis  was  tesselated.  That  is,  the  leaf  was  a  nor- 
mal juvenile  leaf  in  all  respects  except  that  the  edges  remained  free 

(5-6). 

Cases  of  this  kind  might  be  used  as  evidence  that  the  pitcher 
arises  by  fusion  of  the  leaf  margins  (Macfarlane)  but  can  as  well 
be  explained  as  resulting  from  disharmony  of  growth.  On  various 
grounds   another  explanation   is  to   be  preferred.      (See  beyond). 

It  may  be  noted  in  the  juvenile  leaves  that  the  margins  of  the 
"total  stipule"  (Troll)  run  far  up  the  petiolar  region.     In  a  juvenile 


Francis  E.  Lloyd  —  42  —  Carnivorous  Plants 

leaf  about  30  mm.  long,  the  ends  of  the  stipular  margins  were  encoun- 
tered about  half  the  way  up  (ca.  15  mm.).  This  very  gradual  running 
out  of  the  stipular  margins  conveys  the  impression  that  the  edge  of 
the  wing  is  doubled  throughout  its  length,  and  inasmuch  as  in  the 
adult  leaf  the  edge  of  the  wing  in  its  upper  reaches  is,  as  a  matter  of 
fact,  also  double,  this  doubhng  seems  continuous  with  that  of  the 
stipular  wings.  We  shall,  however,  see  elsewhere  that  the  one  had 
nothing  to  do  with  the  other.  In  the  juvenile  leaf,  however,  the  wing 
is  single  above  so  that  the  end  of  the  stipulation  is  clear.  This  in- 
volves the  study  of  transverse  sections  (5  —  4). 

At  the  same  time  it  can  be  seen  that  the  outgrowth  to  form  the 
wing  had  already  started  its  growth  beneath  the  stipular  margins. 
A  study  of  the  development  of  the  leaf  shows  why  this  takes  place. 

The  adult  leaves  have  been  described  a  number  of  times,  by  Tor- 
REY,  Hooker,  Macfarlane,  Kurtz,  Goebel  and  others,  but  despite 
this,  the  precise  morphological  relations  of  the  parts  about  the  mouth 
of  the  pitchers  remain  only  vaguely  comprehended. 

Adult  leaves  are  produced  both  on  short  shoots,  when  they  may 
be  quite  small  (1.5  cm.  to  10  cm.)  and  on  large  vigorous  rhizomes  when 
they  attain  a  stature  of  a  meter  more  or  less.  When  seen  in  its  native 
habitat,  growing  thickly  in  large  clumps,  with  its  tall  leaves  standing 
straight  up,  it  affords  a  spectacular  sight.  The  picture  which  is  seen 
reproduced  {4  —  i)  was  taken  in  an  open  glade  on  a  steepish  wet 
hillside  in  the  mountains  east  of  Crescent  City,  Calif,  in  August  1938, 
when  many  of  the  leaves  were  just  approaching  maturity.  The  seeds 
were  already  fully  ripe,  since  the  flowers  (4  —  2,  3)  are  produced  in 
early  spring,  before  the  leaves  start  to  grow. 

The  pitcher  arises  from  a  clasping  base,  the  wings  of  which  appear 
concurrent  with  the  ventral  wing,  the  edge  of  which  is  doubled  as  in 
Sarracenia  ((5  — 15).  The  tube  is  tapering,  widening  upward.  At 
the  top  the  tube  spreads  suddenly  and  at  the  same  time  is  bent  sharply 
forward  to  form  a  dome,  bringing  the  mouth  into  a  horizontal  posi- 
tion underneath.  From  the  front  of  the  mouth  a  prominent  forked 
appendage,  of  ''swallow-tail"  (Lemmon)  or  fishtail  form,  hangs 
down  with  a  forward  curve.  In  the  largest  leaves  the  dome  rnay  be 
10  cm.  long,  6  broad  and  5  deep,  while  in  a  very  small,  but  still  per- 
fectly formed  pitcher  1.5  cm.  long,  the  dome  measures  only  2.5  mm.  in 
length.  A  feature  peculiar  to  Darlingtonia  is  the  twisting  of  the  tube 
either  to  the  right  or  left  so  that  the  helmet-shaped  dome  is  turned 
about  180  degrees  from  the  axis  of  the  plant.  All  the  leaves  then 
are  turned  outwardly,  a  position  conceivably  of  advantage  in  attract- 
ing prey.  The  small  leaves  often  lie  more  or  less  prostrate  and  the 
fishtail  appendage  lies  on  the  surface  of  the  ground  forming  a  ramp 
leading  small  creeping  things  to  the  opening  {6  —  14). 

When  the  leaf  is  yet  immature,  but  of  full  extent,  the  tissues  of 
the  dome  are  still  soft,  and  the  two  sides  lie  against  one  another.  In 
attaining  their  final  shape  the  sides  expand,  the  dome  is  inflated,  and 
then  becomes  indurated,  so  that,  supported  by  the  sclerotic  cell  walls 
and  other  mechanical  tissues,  the  dome  attains  a  marked  firmness, 
like  a  hard  hat.  The  wings  of  the  appendage  spread  to  form  a  plat- 
form leading  to  the  opening,  its  ventral  surface  secreting  much  nectar 


Chapter  III  —  43  —  Darlingtonia 

as  a  lure.  Light  green  at  first,  the  color  gradually  deepens  and  at 
last  becomes  splashed  with  red.  The  roof  of  the  dome  and  the  back 
of  the  upper  part  of  the  tube  are  mottled  with  numerous  white  flecks, 
devoid  of  chlorophyll,  glands  and  hairs,  and,  to  an  insect  at  the 
mouth,  form  a  visual  lure  {4  —  4,  5).  Such  fenestrations  or  areolae 
are  found  in  Sarracenia  minor,  S.  psittacina,  and  S.  Drummondii  and 
perhaps  some  others.  The  transparency  of  an  areole  is  traceable  to 
the  entire  absence  of  chlorophyll-bearing  tissues  and  of  intercellular 
spaces.  Each  areole  lies  in  a  mesh  of  the  vascular  tissue  surrounded 
by  an  irregular  edging  of  chlorophyllous  tissue  with,  inside,  stomata, 
glands  and  blunt  curved  downward  pointing  hairs,  the  latter  encroach- 
ing a  little  more  on  the  clear  tissue,  which  is  composed  of  wavy  walled 
epidermis  on  both  surfaces,  with  three  or  four  courses  of  thick-walled, 
perfectly  clear  cells.  There  is  no  pigment  of  any  kind,  except  in  old 
leaves,  when  a  yellow  tinge  may  be  detected.  So  complete  is  the  ab- 
sence of  air-spaces  and  pigment,  that  the  areole  is  quite  glassy.  A 
few  coarse  starch  grains  occur  especially  toward  the  margins. 

We  will  now  consider  the  structures  about  the  mouth.  We  note 
in  the  first  place  that  the  ventral  wing  just  below  the  mouth  as  in 
all  the  Sarraceniae  has  a  doubled  edge,  less  conspicuous  in  some  species 
(S.  purpurea)  than  in  others  (S.  minor).  This  is  most  conspicuous  in 
Darlingtonia,  in  which  the  double  margin  may  be  traced  down  a  long 
way  and  appears,  as  it  did  to  Torre y  and  to  Kurtz,  to  be  continuous 
with  the  edges  of  the  basal  stipular  wings.  The  embryology  shows, 
however,  that  this  is  not  the  case  {See  beyond).  If  it  were  not  so, 
then  we  should  have  to  explain  a  condition  in  Darlingtonia  which  is 
not  common  to  the  Sarraceniae.  As  the  evidence  indicates,  the  ven- 
tral wing  or  keel  originates  in  the  same  way  in  both  these  genera. 
The  condition  in  Heliamphora,  which  has  a  pair  of  independent  wings, 
cannot  in  the  absence  of  embryological  evidence  be  brought  into 
comparison,  as  Troll  also  remarked. 

Now  these  two  admittedly  shallow  free  edges  of  the  keel  mark 
the  margins  of  the  mouth.  In  Darlingtonia  they  may  be  traced  along 
the  nectar  roll  and  marking  its  outer  limb.  The  wing  edges  are  ac- 
companied by  the  major  wing  veins,  and  these  run  forward  to  the 
base  of  the  fishtail,  and  enter  it,  one  on  each  side,  where  they  branch. 
The  appendage  receives  the  end  of  the  midvein  also,  but  this 
immediately  branches.  The  fishtail  is  evidently  due  to  deep  emargi- 
nation,  as  Goebel  maintained,  and  is  not  a  pair  of  pinnae,  as  Mac- 
FARLANE  believed.  The  condition  in  Darlingtonia  is  not  parallel  to 
that  in  S.  psittacina,  in  which  the  inrolled  edges  of  the  flap  lobes 
form  valves  with  a  weal  along  the  edge  of  each  representing  the  nectar 
roll,  but  not  of  the  same  form.  This  receives  only  a  minor  branch  of 
the  keel  veins,  which  continues  along  the  margins  of  the  flap  lobes. 
In  Darlingtonia  the  nectar  roll  results  from  hypertrophy  of  the  leaf 
edge  in  a  lateral  direction.  The  strong  venation  is  correlated  with 
the  supply  necessary  to  the  fishtail  with  its  large  number  of  active 
glands  and  its  large  size.  As  already  remarked,  the  veins  running 
along  the  outer  Hmb  of  the  nectar  roll  (5  —  7-10)  pass  forward  to 
enter  the  fishtail  near  its  outer  margins,  there  branch  and  furnish 
the  main  supply  lines.     One   readily  infers  that  the  outer  marginal 


Francis  E.  Lloyd  —  44  —  Carnivorous  Plants 

zone  of  each  lobe  of  the  fishtail  is  a  continuation  of  the  nectar  roll 
on  its  own  side.  Its  position  and  topographical  relations  in  the  defini- 
tive pitcher  leaf  show  that  it  gets  these  as  a  result  of  torsion  and  con- 
traction of  the  tissues  at  its  base.  I  have  been  prompted  to  make 
a  guess  as  to  what  a  primitive  condition  of  the  Darlingtonia  leaf  might 
have  been.  Plate  6  —  13  represents  such  a  hypothetical  condition. 
In  order  to  get  B,  which  with  a  little  more  forward  curvature  would 
represent  the  modern  pitcher,  all  that  need  occur  is  the  transverse 
contraction  of  the  base  of  the  flap  accompanied  by  bending  forward. 
It  should  be  noted  that  there  is  no  fusion  of  the  two  sides  of  the  nec- 
tar roll  in  front,  so  that  the  inner  superficies  of  the  hood  are  con- 
tinuous through  the  gap  between  the  forward  ends  of  the  two  sides 
of  the  nectar  roll  with  the  ventral  (upper)  surface  of  the  fishtail.  That 
a  change  of  this  nature  has  occurred  in  the  process  of  evolution  is 
indicated  by  the  case  above  mentioned  of  a  juvenile  leaf  with  a  nectar 
roll  and  an  emarginate  apex,  but  not  contracted  transversely  at  its 
base  (5  —  3).  In  this  case  the  edge  of  the  nectar  roll  is  clearly  con- 
tinuous with  the  edge  of  the  apical  appendage.  This  is  an  objective 
example  of  the  hypothetical  primitive  condition  presented  in  6  —  11. 

The  fishtail  appendage  on  its  outer  (dorsal)  surface  has  stomata 
and  simple  glands  in  great  numbers.  The  inner  or  ventral  surface  has 
no  stomata,  but  there  are  numerous  glands,  and  a  good  many  stiff, 
thick,  blunt  hairs  turned  morphologically  downwards,  but,  because  of 
the  upsidedownness  of  the  hanging  appendage,  point  upward  and 
furnish  a  rough  surface  which  assists,  rather  than  impedes,  a  climbing 
insect,  lured  by  the  abundant  nectar.  To  the  presence  of  this  there 
is  abundant  evidence  in  the  living  plant.  The  converging  folds  of 
the  appendage,  as  an  insect  crawls  upward,  {4  —  5;  5  —  9),  guide  it 
toward  the  entrance  into  the  hood,  where  it  meets  the  inturned  nectar 
roll.  Once  inside,  the  insect  has  to  face  the  dangers  of  the  inner 
surface.  It  is  not  to  be  supposed  that  insects  will  insist  on  using  the 
appendage.  Nectar  glands  occur  everywhere  on  the  outer  surface. 
The  ventral  wing,  as  well  as  the  appendage,  may  act  as  a  wing-fence 
to  guide  them  to  the  opening.  Meeting  the  heavy  exudation  of  nectar 
on  the  nectar  roll  is  an  added  spur  to  entrance,  however  they  may 
have  been  attracted  thus  far. 

To  turn  to  the  conditions  found  in  the  interior  of  the  pitcher.  The 
forward  (upper)  portion,  the  dome,  is  lined  with  many  stiff,  coarse 
hairs  so  directed  as  to  urge  insects  toward  the  depths  of  the  tube.  These 
are  largely  absent  from  the  areolae,  though  small  ones  may  occur. 
They  are  most  plentiful  on  the  floor,  where  there  are  no  areolae.  In- 
termingled with  the  hairs  are  many  nectar  glands,  so  that  the  whole 
forward  portion  of  the  floor  of  the  dome  serves  as  a  feeding  ground, 
from  which  also  insects  can  feed  with  great  convenience  on  the  nectar 
roll,  as  from  a  table.  The  rear  of  the  dome,  however,  the  surface  of 
which  extends  down  into  the  tube,  has  no  glands,  but  the  imbricated 
epidermal  cells  are  elongated,  each  into  a  sharp  downwardly  pointed 
hair,  which  offers  no  foothold.  This  continues  far  into  the  tube,  as 
far  as  a  point  where  there  are  no  more  fenestrations  in  the  wall.  Here 
the  character  of  the  hairs  gradually  changes,  and  they  become  fewer 
and  longer.     In  the  extreme  depth  of  the  tube  the  hairs  are  absent. 


Chapter  III  —  45  —  Darlingtonia 

and  there  are  no  glands.  If  the  absence  of  glands  indicates  anything 
it  is  that  in  Darlingtonia  the  only  digestion  which  may  occur  is  that 
induced  by  bacteria,  and  that  this  at  least  takes  place  has  been  testi- 
fied by  J.  G.  Lemmon  in  a  letter  to  Canby  who  mentions  the  obser- 
vation in  a  paper  in  1875.  Lemmon  remarked  that  he  detected  a 
strong  smell  of  decay  at  some  distance,  as  did  Jones  and  others  later. 

The  structure  of  the  nectar  glands  is  quite  unique,  though  they 
evidently  may  be  regarded  as  conforming  to  the  Sanacenia  type. 
On  the  surface  a  gland  appears  as  one  of  the  epidermal  cells,  or  if 
compound  from  two  to  five  or  six  such  cells  {6 —  18,  19,  22).  It  ap- 
pears filled  with  cytoplasm  and  a  nucleus  is  always  distinctly  visible, 
sometimes  two  or  three  (in  the  thin  superimposed  cells).  Focussing 
more  deeply  the  gland  cells  become  larger  and  rounded  in  outhne. 
The  reason  for  this  is  understood  when  a  section  is  examined  {6  —  20, 
21,  23).  It  is  then  seen  that  the  diameter  of  the  glands  increases 
with  depth  and  is  composed  of  a  row  of  flat  cells,  evidently  derived 
by  periclinal  division  of  an  original  epidermal  cell.  Underlying  each 
gland  (if  simple)  is  usually  a  single  parenchyma  cell,  which  in  the 
glands  of  the  outer  surface  is  quite  deep,  suggesting  to  Macfarlane 
the  adjective  "globoid"  {6  —  20,  21). 

When  the  gland  is  compound  there  will  be  seen  in  section  two 
(rarely  more  because  of  the  unfavorable  chances  of  such  a  section) 
tiers  of  flat  cells.  These  glands  are  not  only  compound  but  are  much 
larger  than  those  on  the  outer  surface,  where  they  are  invariably  small 
(about  the  size  of  the  stomata)  and  simple.  Compound  glands  occur 
in  great  numbers  on  the  nectar  roll,  and,  to  a  less  extent,  on  the  for- 
ward interior  face  of  the  dome. 

When  a  pitcher  is  allowed  to  lie  in  a  weak  solution  of  methylene 
blue,  the  glands  of  the  outer  surface  become  stained  throughout, 
though  the  surrounding  epidermal  cells  remain  colorless.  There  is 
evidently  ease  of  diffusion  through  the  external  cells.  Macfarlane 
explained  this  by  the  absence  of  cuticle  from  the  outer  gland  cell,  say- 
ing that  he  could  observe  the  torn  edges  of  the  cuticle  in  a  surface 
view,  but  I  have  been  unable  to  verify  this.  By  the  evidence  of  ex- 
posure to  methylene  blue  it  also  appears  that  the  wafls  of  the  gland 
are  cutinized  (Goebel)  except  at  the  base,  as  is  the  case  with  the 
glands  of  other  genera  of  the  Sarraceniaceae. 

In  the  absence  of  digestive  glands,  but  on  the  presumptive  nutri- 
tion of  the  plant  from  the  decaying  insects  which  are  caught  in  great 
numbers  (Edwards  counted  33  spp.),  the  question  as  to  what  part,  if 
any,  of  the  interior  surface  of  the  tube  can  absorb  the  products  of  such 
decay,  is  pertinent.  We  have  seen  that  zone  4  in  S.  purpurea  is  devoid 
of  cuticle.  In  Darlingtonia  it  is  surprising  to  note  that  the  whole  of 
the  surface  from  the  lower  limit  of  zone  i,  that  is,  below  about  two- 
thirds  of  the  dome,  is  capable  of  absorption.  When  a  leaf  is  plunged 
into  a  weak  methylene  blue  solution  for  20  hours  the  tissues,  as  far 
as  and  including  the  outer  part  of  the  third  layer  of  parenchyma,  become 
dyed,  while  no  dye  enters  through  the  outer  surface  epidermis,  except 
through  the  nectar  glands.  There  can  hardly  be  any  question,  there- 
fore, that  the  inner  surface  of  the  pitcher  is  capable  of  absorbing  so- 
lutes which  result  from  the  decay  of  insects  within  it.     This  is  due, 


Francis  E.  Lloyd  —  46  —  Carnivorous  Plants 

probably  in  a  large  part,  to  the  absence  of  cuticle  from  the  whole  area 
occupied  by  the  long  detentive  hairs,  according  to  Batalin  (1880) 
who  observed  the  loosening  of  the  cuticle  from  the  free  surface  of  the 
cells  by  the  formation  of  blisters  (in  Sarracenia  flava).  Batalin  even 
suggests  that  this  non-cuticularized  epidermis  takes  over  in  the  ab- 
sence of  glands,  their  function,  not  only  of  absorption  but  also  of  di- 
gestion, since  throwing  off  the  cuticle  seems  to  be  indicative  of  the 
excretion  of  some  substance,  possibly  digestive.  The  condition  in 
Darlingtonia  does  not  seem  to  be  wholly  parallel  to  that  described 
by  Batalin  for  Sarracenia.  I  placed  a  pitcher  in  methylene  blue  over- 
night and  found  the  whole  inner  surface  stained  deeply  in  the  morn- 
ing. On  sectioning,  the  whole  inner  epidermis  was  found  deeply 
colored.  On  staining  with  Sudan  III  there  was  distinct  evidence  of 
cuticularization,  especially  in  the  radial  walls.  The  outer  walls  were 
thinly  stained,  sometimes  not  at  all,  while  the  cuticle  of  the  outer 
epidermis  was  obviously  thick  and  richly  stained.  I  could  not,  how- 
ever, find  clear  evidence  that  the  matter  stands  as  Batalin  describes 

it. 

Development  of  the  leaf.  —  Material  for  the  study  of  the  development 
of  the  leaf  in  Darlingtonia  was  obtained  on  May  22,  1938,  growing  in  a 
sphagnum  swamp  6  miles  N.  of  Florence,  on  the  coast  of  Oregon  at  a 
few  feet  above  sea  level.  At  that  time  the  plant  was  in  full  flower,  and 
in  some  plants  very  young  leaves  were  beginning  to  make  their  ap- 
pearance. New  leafage  would  be  achieved  in  the  course  of  a  month, 
the  present  leaves  having  persisted  since  the  previous  season.  In  the 
depths  of  the  pitchers  were  to  be  found  merely  the  chitinous  remains 
of  insects  long  since  caught,  and  no  odor,  such  as  has  been  detected 
by  others  during  the  active  season,  was  noticed. 

The  morphology  of  the  leaf  is  easily  the  most  complicated  of  all 
the  pitcher  plants  of  the  Sarracenia  type.  This  is  because  of  the 
torsion  of  tissues  which  occurs  at  the  outer  (distal)  extremities  of  the 
two  sides  of  the  nectar  roll,  and  the  edges  of  the  fishtail  flap.  The 
nectar  roll  appears  to  be  extended  as  an  infold  of  the  outer  edges  of 
the  fishtail  flap,  which  hangs  down  from  the  distal  sector  of  the  open- 
ing, its  ventral  face  being  that  one  which  faces  the  tube  of  the  pitcher. 
We  may  follow  the  development  of  the  leaf  in  examining  the  follow- 
ing series  of  stages,  chosen  conveniently. 

Case  I.  A  very  early  stage  of  development  (<5  —  i)  in  which  the 
whole  leaf  consists  of  a  flat  cone  0.3  mm.  high.  This  may  be  regarded 
as  identical  with  the  corresponding  early  stage  of  Sarracenia  purpurea 
as  represented  by  Troll  (1932)  and  earlier  by  Goebel  (1891),  though 
in  Goebel's  figure  the  mouth  of  the  beginning  pitcher  is  too  wide, 
and  the  leaf -base  is  not  shown.  The  mouth  is  not  set  so  nearly  hori- 
zontal as  in  Sarracenia.  The  margins  of  the  leaf-base  wings  are  con- 
tinuous transversely  from  one  side  to  the  other.  A  small  stretch  of 
tissue  separates  this  from  the  edges  of  the  mouth,  already  well  marked. 
The  rim  of  the  mouth  is  continuous  all  around,  making  peltation  com- 
plete. 

Case  2.  Leaf  0.7  mm.  tall  {6  —  2).  The  mouth  and  its  continuous 
rim  form  a  definite  papilla,  the  upper  margin  taking  the  lead  in  up- 
ward growth.     The  tissues  between  the  lower  transverse  rim  of  the 


Chapter  III  —  47  —  Darlingtonia 

mouth  are  somewhat  raised  to  form  a  low  ridge.    The  twisting,  charac- 
teristic of  the  Darlingtonia  leaf,  has  already  begun. 

Case  3.  A  leaf  1.5  mm.  long  {6  —  3).  The  leaf  base  has  elongated, 
carrying  the  margins  of  its  wings  up  some  distance.  Above,  the  rim 
of  the  mouth  has  been  extended  down  as  a  low  double  ridge  and  the 
lateral  reaches  of  the  rim  now  begin  to  form  the  two  sides  of  the  ter- 
minal fishtail  of  the  mature  leaf  {6  —  6).  The  ascidium  reaches  well 
down  into  the  leaf  base. 

Case  4.  Leaf  2.6  mm.  long  {6  —  7).  The  wings  of  the  leaf  base 
have  now  developed  so  that  the  distinction  between  this  and  the  leaf- 
blade  is  sharp.  The  double  ridge,  continuous  with  the  two  sides  of 
the  mouth  is  longer  and  is  raised  up  on  the  edge  of  the  ala  ventralis. 
The  close  apposition  of  this  with  the  apex  of  the  leaf-base  wings  shown 
by  Troll  for  Sarracenia  does  not  occur  here.  It  has  now  become 
clear  that  the  double  character  of  the  edge  of  the  ala  ventralis  is  de- 
rived from  the  rim  of  the  mouth.  If  not  so  extended  in  Sarracenia, 
yet  the  origin  of  the  double  edge  is  the  same.  In  this  case  the  twist 
of  the  leaf  is  to  the  right. 

Case  5.  A  trifle  older  than  case  2,  not  so  old  as  case  3,  in  sagittal 
section  {6  —  4).  Here  can  be  clearly  seen  the  identity  of  the  side  lip 
of  the  mouth  and  the  edge  of  the  keel.  The  pore  of  the  mouth  is  still 
small.  The  section  being  truly  sagittal,  the  other  keel  edge  is  not  seen. 
No  indication  of  the  nectar  roll  is  yet  visible.  Advance  beyond  this 
stage  consists  of  the  enlargement  of  the  lateral  reaches  of  the  lips  of 
the  mouth  concomitant  with  the  laying  down  of  the  nectar  roll  and 
its  continuation  along  the  outer  margins  of  the  fishtail. 

Cases  d,  7  and  8  {6  —  5,  6,  10).  Successive  stages  following  on 
case  5,  showing  the  development  of  the  fishtail  from  the  sides  of  the 
mouth,  the  apex  being  now  arrested  and  of  slower  growth.  In  cases 
7  and  8,  the  outer  marginal  roll  of  the  one  side  of  the  fishtail  is  seen, 
and  that  it  is  continuous  with  the  nectar  roll  which  has  also  appeared. 
The  fold  between  the  distal  ends  of  the  nectar  roll  has  begun  develop- 
ment. 

Case  g  {6  —  16).  Surface  view  of  a  somewhat  later  stage,  about 
like  that  shown  by  Goebel.    The  difficulty  of  interpretation  is  obvious. 

Case  10  {6  —  8).  The  dome  has  begun  development  and  the  tube 
is  twisted  through  90  degrees.  The  distinction  between  the  edges  of 
the  wings  of  the  leaf  base  has  become  obscure,  except  in  transverse 
sections  (5  —  5).  Seen  in  sagittal  section  the  dome  is  represented  in 
6  —  9.  The  fold  {6  —  10)  has  now  come  into  a  vertical  position  as  the 
dome  has  enlarged  fore  and  aft,  and  the  outer  marginal  roll  of  the  one 
side  of  the  fishtail  is  seen  continuous  with  the  nectar  roll,  which  has 
pushed  forward.  The  ventral  surface  of  the  fishtail  is  continuous  with 
the  inside  surface  of  the  dome. 

In  a  word,  all  parts  are  now  clearly  defined,  and  the  glands  have 
appeared.  The  final  condition  may  be  seen  in  various  figures  illustrat- 
ing the  mature  leaf.  At  the  time  growth  is  complete,  the  leaf  has 
twisted  through  an  angle  of  180  degrees,  though  it  may  be  as  small  as 
90  degrees  or  as  large  as  270  degrees.  The  torsion  does  not  involve  the 
dome.  It  is  either  to  the  right  or  left  in  any  given  plant  (antidromy 
of  McClosky). 


Francis  E.  Lloyd  —  48  —  Carnivorous  Plants 

Digestion  and  Absorption.  —  Edwards  (1876)  and  Goebel  were  of 
the  opinion  that  true  digestion,  that  is,  by  means  of  a  secreted  enz3mie, 
does  not  take  place  in  Darlingtonia.  More  recently  Hepburn  and 
his  collaborators  St.  John  and  Jones  (1920,  1927)  examined  the  fluid 
of  unopened,  cotton-plugged  and  open  pitchers  with  regard  to  its 
effect  chiefly  on  carmine  fibrin  and  fibrin  in  the  presence  of  a  bacteri- 
cide (0.2%  trikresol).  Of  a  total  of  57  experiments  in  the  laboratory 
and  field,  none  gave  a  definitely  positive  result,  occasional,  very  slight 
aberrancies  being  due  probably  to  the  presence  of  bacterial  ferments. 
On  anatomical  grounds  this  is  to  be  expected,  though  as  above  noted, 
Batalin  made  a  suggestion  that  the  non-cuticularized  cells  of  the 
depths  of  the  pitcher  might  take  over  the  function  of  the  glands.  But 
that  the  function  of  the  secretion  of  a  protease  could  be  one  seems, 
in  view  of  the  above  cited  results,  to  be  out  of  the  question.  That 
insects  are  disintegrated  by  bacteria  is  obvious,  and  that  their  products 
are  available  as  nutriment  to  the  plant  is  indicated  by  the  fact  that 
absorption  of  various  substances  can  and  does  take  place  as  shown 
also  by  Hepburn  and  his  colleagues,  and  as  would  appear  to  be  the 
case  in  view  of  the  non-cutinized  tissues  of  the  pitcher  through  which 
methylene  blue  readily  passes.  Hepburn,  St.  John  and  Jones  showed 
that  water  is  absorbed,  and  dissolved  lithium  was  found  to  have  been 
taken  up  by  the  tissues.  When  various  nitrogenous  substances  were 
introduced,  both  these  and  the  solvent  were  absorbed,  but  in  the 
presence  of  a  phosphate  buffer  the  water  might  increase  though  the 
compounds  were  absorbed.  Mrs.  Austin  had  found  (1876)  that  when 
stimulated  by  the  introduction  of  bits  of  meat,  the  amount  of  fluid 
increased  in  the  pitchers.  Her  results  were  quoted  by  Asa  Gray 
(1876).  Though  the  experiments  were  done  in  the  field,  there  is  as- 
surance of  the  exclusion  of  rain  which,  if  any  fell,  which  is  quite  un- 
likely, could  gain  no  entrance  into  the  hooded  pitchers.  Hepburn 
et  al.  investigated  this  point,  also  in  the  field  (Plumas  Co.,  Calif.)  and 
found  that  when  milk  was  introduced  into  the  pitchers,  there  was  in- 
variably an  increase  in  the  amount  of  fluid  ranging  from  20  to  1242 
per  cent  in  periods  of  1-7  days.  They  studied  77  pitchers,  and  the 
amount  of  increase  of  volume  varied  independently  of  the  time,  so 
that  some  pitchers  were  much  more  active  than  others.  When  beef 
broth  was  used,  there  was  an  increase  of  from  302  to  387  per  cent  in 
fluid  content  in  five  days.  When  bits  of  meat  were  used  the  results 
depended  on  whether  the  meat  was  cooked  or  raw.  If  cooked  there  was 
little  if  any  increase,  because  only  small  patches  of  the  surface  were 
affected.  If  raw,  an  increase  of  volume  of  from  48  to  157  per  cent 
was  observed.  No  results  were  obtained  with  raw  or  coagulated  egg- 
white,  nor  with  cheese,  casein  or  fibrin  "possibly  for  the  same  reason 
as  with  meat."  When  acids  and  alkalis  in  very  dilute  solutions  were 
introduced,  there  was  no  very  "marked  tendency"  for  the  volume  of 
fluid  to  "increase  or  decrease",  but  it  was  noted  that,  as  in  the  human 
stomach,  the  fluid  returned  to  neutrality  whatever  the  nature  of  the 
introduced  reagent. 

Has  the  fluid  of  pitchers  the  power  of  wetting  insects,  when  im- 
mersed, more  than  pure  water?  While  positive  evidence  was  ob- 
tained for  other  species  of  Sarraceniaceae,  that  from  Darlingtonia, 
from  experiments  done  in  the  field,  was  purely  negative. 


Chapter  III  —  49  —  Darlingtonia 

Experiments  done  by  the  same  authors  to  determine  if  other 
enzymes  than  protease  might  be  detected  in  Darlingtonia  gave  nega- 
tive results  except  for  diastase,  of  which,  however,  only  a  trace  could 
be  detected.  Maltase,  invertase,  emulsin  and  urease  were  absent. 
It  seems,  therefore,  indisputable  that  this  plant  depends  solely  upon 
the  activity  of  bacteria  to  provide  the  absorbable  protein  and  other 
nutrients,  if  any,  through  the  pitcher  walls.  Edwards'  opinion,  ex- 
pressed in  1876,  turned  out  to  be  correct. 

The  presence  of  bacteria  and  their  activities  were  observed  by 
Hepburn  ct  al.  A  chemical  study  of  the  pitcher  fluid  was  made  by 
these  authors  who  found  that  in  closed,  plugged  and  open  pitchers,  a 
small  amount  of  nitrogen  could  be  recovered,  viz.  0.027%  from  closed 
pitchers,  0.015  %  to  0.009%  from  plugged  pitchers  and  0.034  f;  to  0.049  % 
from  open  pitchers.  The  fluid  studied  has  a  specific  gravity  of  1.003 
at  15  degrees  C.  and  contained  0.213%  solids,  0.104%  ash,  and  0.046% 
calcium  oxide  (lime)  forming  44.23  %  of  the  ash.  Chlorides  were  present. 
No  reducing  sugars  could  be  found,  though  it  is  quite  probable  that 
such  may  sometimes  be  present  by  contamination  with  the  nectar 
found  elsewhere  on  the  walls  of  the  pitcher. 

Literature  Cited: 

Ames,  Mary  E.  P.,  Calif.  Horticulturalist  and  Floral  Magazine  10:225-229,  1880.    Quotes 

a  letter  from  Mrs.  Austin  re  increase  of  fluid  in  pitchers  of  Darlingtonia. 
Arbee  {see  under  Cephalotus). 
Austin,  R.  M.  L.,  Brief  an  Dr.  K.  Keck,  iiber  Darlingtonia.    Oester.  Bot.  Zeitschr.    1876: 

1 70-171. 
Barnhart,  J.  H.,  Brackenridge  and  his  book  on  Ferns.  Journ.  N.  Y.  Bot.  Card.  23:117- 

124,   1919.  . 

Batalin,  a.,  tjber  die  Function  der  Epidermis  in  den  Schlauchen  von  Sarracema  und  Dar- 
lingtonia.    Acta  Hort.  Petropolitani  7:346-359.  1880. 

Braun,    a.,    Uber    Darlingtonia    californica    Torrey.      Sitzungsber.  d.    Gesellsch.    naturf. 

Freunde,  Berlin  1873:73-75-  ,  ^  *     a    a     c  • 

Canbv,  Wm.  M.,  Darlingtonia  californica,  an  msectivorous  plant.  Proc.  A.  A.  A.  bci. 
1874:64-72,  Salem,  Mass.  1878.     Reprinted  in  Oester.  Bot.  Zeitschr.  1875:287-293. 

D.ARWiN,  C,  Insectivorous  Plants.     London  1875. 

Edv.'ards,  Henry,  Darlingtonia  californica  Torrey.  Proc.  Calif.  Acad.  Sci.  6:161-166,  1875 
(published  in  1876). 

GoEBEL,  K.,  Pflanzenbiologische  Schilderungen.     Part  2,  V.  Insectivoren.     Marburg,  1891. 

Gray,  Asa,  (Description  of  the  seed  of  Darlingtonia).  Amer.  Journ.  of  Science  and  Arts, 
2  ser.  35:136-7,  1863. 

Gray,  Asa,  Darwiniana.  Appleton,  New  York  1876,  330  pp.  (Cites  Austin's  Observa- 
tions on  fluid  in  pitchers  of  Darlingtonia). 

Hepburn,  J.  S.,  F.  M.  Jones  &  Eliz.  Q.  St.  John,  Biochemical  studies  of  North  Ameri- 
can Sarraceniaceae.  Trans.  Wagner  Free  Inst.  Phila.  11:1-95.  1927-  A  very  full  bib- 
liography. 

Hooker,  J.  D.,  On  the  carnivorous  habits  of  some  of  our  brother  organisms  —  plants. 
Rep.  Brit.  Assoc.  Adv.  Sci.,  Belfast  1874.  . 

Kurtz,  F.,  Zur  Kenntnis  der  Darlingtonia  californica  Torrey.  Verhandl.  Bot.  Vereins 
Brandenburg,  meeting  June  2,  1878,  24  pp. 

Lemmon,  J.  G.,  Brief  an  Dr.  K.  Keck  iiber  Darlingtonia.    Oester.  Bot.  Zeitschr.  1876: 35. 

Macbride,  J.,  On  the  power  of  Sarracenia  adnnca  to  entrap  insects.  Trans.  Linn.  Soc. 
London  12:48-52,  1817  (read  in  1815). 

Macfarlane,  J.  M.,  Observations  on  the  pitchered  insectivorous  plants,  I.  Ann.  Bot. 
3:253-266,  1889,  1890. 

Macfarlane,  J.  M.,  Observations  on  the  pitchered  insectivorous  plants,  II.  Ann.  Bot. 
7^.03-458,  1893. 

Mellichamp,  J.  H.,  Letter  to  Dr.  Hooker  on  the  CaUfornia  pitcher  plant.     Gard.  Chron. 

1871:46. 
Mellichamp,  J.  H.,  Notes  on  Sarracenia  variolaris.     Proc.  A.  A.  A.  S.   23   meeting,   1874. 
1875:113-133.      An  earlier  communication  appeared  in  Gard.   Chron.   1874:818-819, 
earlier  published  in  the  N.  Y.  Tribune  by  Asa  Gray. 


Francis  E.  Lloyd  —  50  —  Carnivorous  Plants 

ToRREY,  John,  On  Darlingtonia  californica,  a  new  pitcher  plant  from  Northern  California. 

Smithsonian   Contrib.   to  Knowledge  5:1,   1853.     (Year  of  discovery  given   as  1842. 

According  to  Barnhart,  1919,  the  year  must  have  been  1841). 
Troll,  W.,  Morphologie  der  schildformigen  Blatter.     Planta  17:153-314,  1932. 
VoGL,  A.,  Die  Blatter  der  Sarracenia  purpurea.    Sitzungsber.     Wien.  Akad.  Wiss.  50,  Oct. 

1864. 


Chapter  IV 
NEPENTHES 

Geographical  distribution.  —  Habitat.  —  General  character.  —  Morphology  of  the  leaf 
and  the  seedUng.  —  Development  of  the  leaf  and  adventive  shoots.  —  The  pitcher  (Mor- 
phology; Variety  of  form,  color  etc.;  The  mouth;  The  lid;  Spur;  Special  anatomy). — 
The  rim  or  peristome.  —  Histology  of  the  peristome.  —  The  glands:  their  histology. _ — 
Anatomy  of  the  pitcher-wall  (Vascular  system;  The  interior  surface;  Wax  zone;  Digestive 
zone;  Rim).  —  Digestion.  —  The  animal  life  of  the  pitchers.  —  Folklore,  uses.  —  Antisepsis 
of  pitcher  fluid. 

The  species  of  Nepenthes  are  found  scattered  throughout  the  tropics 
of  the  Old  World  with  the  center  of  distribution  in  the  region  of 
Borneo,  being  found  as  far  East  as  N.  Austraha  and  New  Guinea, 
and  to  the  West  in  Ceylon  and  in  Madagascar,  its  extreme  outpost 
(Danser).  Madagascar,  indeed,  was  the  scene  of  its  first  discovery  by 
the  Governor,  Flacourt,  in  the  middle  of  the  17th  century,  and  it  was 
reported  from  Ceylon  a  little  later  by  Paul  Hermann,  a  physician, 
who  sent  the  specimens  to  Commelin  in  Amsterdam.     (Wunschmann 

1872). 

They  grow  with  rare  exceptions  only  in  moist  or  very  moist  situa- 
tions, and  they  are  successfully  cultivated  in  greenhouses  only  if  the 
relative  humidity  is  kept  very  high;  in  particular,  a  slightly  reduced 
humidity  inhibits  the  development  of  pitchers.  In  their  vertical  dis- 
tribution they  occur  from  near  sea-level  to  9000  ft.  altitude  {Nepenthes 
Rajah  and  villosa,  on  Kina  Balu,  Borneo).  They  are  chiefly  jungle 
plants,  though  one  species  at  least  {N.  destillatoria  in  Ceylon)  grows 
in  wet  savannahs  where  it  climbs  on  scattered  shrubs.  A^.  gracilis  was 
found  by  Korthals  (1839)  in  "dry  sandy,  stony  ground"  though  it 
was  found  to  prosper  better  in  other,  moister  situations.  The  de- 
mands of  the  plant  are  for  wet  soil  and  hot  to  cool  temperatures  ac- 
companied by  a  high  humidity  of  the  air. 

It  is  most  rarely  that  they  can  be  successfully  cultivated  outdoors 
in  temperate  regions  but  it  was  reported  some  years  ago  at  a  meeting 
of  the  Naturalists  Club  of  Sydney,  N.  S.  W.  that  two  unidentified 
species  were  grown  out  of  doors  on  a  trellis,  at  Parramatta,  not  far 
from  Sydney.  This  is  a  region  where  staghom  ferns  are  grown  out  of 
doors  by  everybody,  and  the  Nepenthes  species  above  mentioned  may 
be  especially  hardy. 

In  general  appearance  the  species  of  this  genus  are  pretty  uniform, 
the  more  striking  differences  being  found  in  the  size  and  shape  of  the 
pitchers.  The  plant  consists  of  a  creeping  rhizome  from  which  spring 
coarse,  clambering  vines  with  thick,  glossy  leaves  of  frequently  con- 
siderable length  (i  meter)  arranged  in  a  "^5  phyllotaxy,  though  one 
species  (A.  Veitchii)  is  wholly  distichous  (Troll  1939).  The  leaf  con- 
sists of  a  spreading  winged  base  narrowing  into  a  short  isthmus 
beyond  which  it  spreads  into  a  hgulate  to  orbicular  blade  beyond  which 
extends  a  short  or  long  tendril  which  can  twine  about  a  support  and 
ending  in  a  pitcher  with  a  lid  overhanging  the  mouth,  behind  which 


Francis  E.  Lloyd  —  52— Carnivorous  Plants 

is  a  small  or  larger  spur.  The  pitcher  is  always  held  in  an  upright 
position.  When  young  the  various  parts  are  clothed  with  a  tight  rusty 
pubescence  of  curiously  branched  hairs.  In  cKmbing,  often  to  the 
crowns  of  tall  trees  (i6  to  20  meters:  N.  bicalcarata,  Rafflesiana,  etc. 
according  to  Macfarlane),  the  plant  supports  itself  by  means  of  the 
stout  tendrils.  It  sometimes  grows  epiphytically,  as  in  the  case  of 
N.  Veitchii  (Burbidge,  1880).  Such  species  may  have  cHmbing  stems 
3  cm.  in  diameter.  Troll  (1932)  has  given  us  an  excellent^  word 
picture  of  the  appearance  of  N.  ampullaria  {4  —  9)  in  its  habitat. 

"I  came  across  N.  ampullaria  among  the  massive  vegetations  of  a 
swamp-forest  on  the  island  of  Siburut,  off  the  west  coast  of  Sumatra. 
It  was  a  fabulous,  unforgettable  sight.  Everywhere,  through  the 
network  of  lianas  the  peculiarly  formed  pitchers  of  this  species  gleamed 
forth,  often  in  tight  clusters;  and,  most  remarkably,  the  muddy,  moss 
overgrown  soil  was  spotted  with  the  pitchers  of  this  plant,  so  that  one 
got  the  impression  of  a  carpet.  How  is  this  pecuUar  behavior  to  be 
explained? 

"iV.  ampullaria  develops  a  rhizome  which  creeps  in  the  earth  or 
between  clumps  of  moss.  This  sends  out  one  or  more  hana-like  shoots 
which  cHmb  high  into  the  trees,  and  at  their  ends,  where  they  can  en- 
joy bright  illumination,  they  become  leafy.  The  leaves  of  these  long 
shoots  are  of  the  usual  type  —  they  possess  a  well  developed  lamina 
and  a  functional  tendril.  Elsewhere  the  Manas  are  bare  or  have  re- 
mains of  dead  leaves  clinging  to  them. 

"Of  quite  a  different  appearance  are  the  pitcher  leaves  which  are 
found  on  the  ground.  True,  the  pitchers  are  well  developed,  but  the 
tendrils  are  always  short  and  serve  only  to  hold  them  in  an  upright 
position. 

"If  one  searches  for  the  attachments  of  these  simplified  leaves, 
they  will  be  found  to  occur  on  short  branches,  just  as  Goebel  de- 
scribed them.  It  has  been  overlooked,  however,  that  they  are  not  con- 
fined to  the  main  rhizome  but  spring  also  from  numerous  prostrate 
stems  which  attain  a  considerable  thickness.  Such  branches  may  be 
followed  for  a  distance  of  several  meters  along  the  soil  surface  quite 
easily  because  of  the  numerous  dense  clusters  of  pitchers  which  are 
strung  along  them."     {Translated). 

Earlier  observers  in  some  cases  thought  that  the  lid  of  the  pitcher 
is  capable  of  motion,  and  so  to  close  and  open  its  mouth.  Loureiro 
is  mentioned  by  Sims  (1826)  to  have  held  this  view.  But  this  of 
course  is  not  the  case  —  the  Hd  attains  a  quite  fixed  posture,  usually 
overhanging  the  mouth  of  the  pitcher,  but  sometimes  turned  quite  back. 

The  morphology  of  the  very  highly  specialized  leaf  of  Nepenthes 
can  best  be  considered  by  a  comparison  of  the  mature  condition  with 
that  met  with  in  the  leaves  of  seedUngs  and  of  adventitious  shoots 
on  cuttings.  The  former  have  been  studied  by  Dickson,  J.  D.  Hooker, 
Goebel,  Macfarlane  and  Stern.  In  spite  of  a  general  uniform- 
ity of  evidence,  with  exceptions  to  be  noted,  there  is  a  wide  divergence 
of  opinion  as  to  the  homology  of  the  parts,  Macfarlane  regarding 
the  leaf  as  a  p'nnate  structure  and  Goebel  as  a  simple  leaf  with  a 
highly  specialized  region  forming  the  ascidium  or  pitcher.  These  and 
other  interpretations  will  be  considered. 


Chapter  IV  —  53  —  Nepenthes 

Seedlings.  —  The  primary  leaves  of  the  seedling  (first  described  by 
BiscHOFF  in  1834),  the  cotyledons,  are  elongate  oval  and  present  no 
noteworthy  features.  The  following  leaves,  which  will  for  convenience 
be  called  primary,  consist  of  a  short  spreading  and  clasping  base, 
narrowing  briefly  to  expand  at  once  into  a  pitcher  (Korthals)  with  the 
edges  of  the  leaf  base  extending  up  its  ventral  (adaxial)  face  as  two 
wings  which  either  meet  transversely  somewhat  beneath  the  rim  of  the 
pitcher  mouth  (Hooker,  1859,  Dickson,  Macfarlane),  or  end 
abruptly  without  meeting  (Goebel).  Stern,  restudying  Goebel's 
material,  verified  this  but  pointed  out  that  he  found  a  row  of  gland- 
like tentacles  (7  —  5)  and  these  might  indicate  a  transverse  connection. 
Troll  strongly  favored  the  view  that  there  occurs  actually  or  funda- 
mentally a  union  of  the  wings  below  the  rim  to  express  '"total  stipula- 
tion." The  edge  of  the  mouth  of  the  pitcher  is  armed  with  a  transverse 
rim  usually  well  developed,  and  occupies  about  one-half  to  two-thirds 
of  the  peripher>^  the  rest  being  taken  up  by  the  base  of  a  lid,  that  is, 
in  the  primary  leaves  the  lid  base  is  very  broad  (7  —  7,  9)  while  in 
the  adult  leaf  type  it  is  narrow,  with  the  consequence  that  the  veins 
are  spread  apart  in  the  former  and  crowded  together  in  the  latter. 
The  venation  of  the  lid  appears  quite  evidently  to  be  an  extension  of 
the  plan  of  that  of  the  pitcher,  and  not  secondary  as  is  that  of  the  rim, 
if  we  may  lean  on  juvenile  leaf  forms  arising  on  small  forced  shoots. 
The  lid  bears  a  number  of  tentacle-hke  emergencies  at  its  edges  and 
upper  surface,  and  behind  it  extends  an  appendage  which  is  properly 
regarded  as  the  organic  apex  of  the  leaf,  the  "spur."  With  the  advance 
of  age,  the  region  betw^een  the  leaf  base  and  the  pitcher  elongates,  so 
that  a  blade  now  intervenes,  with  its  margins  continuous  with  the  wings 
of  the  pitcher.  The  intercalation  of  a  tendril  at  this  region  is  indicated 
in  the  narrowing  of  the  blade  (7  —  7,  11),  and  in  the  more  mature 
condition  a  tendril  is  realized.  The  leaf  then  consists  of  an  expanded 
base,  a  blade,  generally  of  some  length,  a  tendril  which  becomes 
functional  as  such,  supporting  at  its  end  the  pitcher  which  is  always 
winged,  though  less  obviously,  it  may  be,  than  in  the  seedling  {4  —  7, 
8).  In  some  species  the  pitchers  on  the  higher  parts  of  the  plant  have 
the  wings  reduced  to  mere  ridges. 

The  early  development  of  the  pitcher  leaf  has  been  described  by 
J.  D.  Hooker  (1859),  Bower,  Stern,  who,  as  to  the  facts,  agree. 
In  the  very  early  condition,  there  is  to  be  observed  a  depression  just 
below  the  apex  of  the  yet  merely  low  conical  structure  (7  —  i).  The 
lid  develops  as  a  transverse  ridge  at  the  distal  limb  of  the  depression 
and  is  independent  of  the  true  apex  (7  —  2).  The  lid  is  therefore  not 
the  tip  of  the  leaf,  but  an  outgrowth  on  the  ventral  face  of  the  leaf 
near  its  apex  (Hooker).  It  grows  downward  over  the  opening,  which 
in  the  meantime  becomes  deeper  to  form  the  acidium.  It  has  the 
appearance  of  a  two  lobed  affair  (7  —  4),  and  that  it  is  really  such 
has  been  thought  by  Bower  and  by  Macfarlane  who  cite  in  support 
of  their  view  the  fact  that  the  lid  in  the  mature  leaf  is  often  emargi- 
nate.  The  conical  apex  continues  its  development  into  an  expanded 
leaf  tip  which  may  at  length  bear  one  to  several  expanded  lobes 
{N.  ampullaria),  "pinnae"  as  they  have  been  called,  and  Macfarlane 
regards  them  as  supporting  evidence  of  his  theory  that  the  whole  leaf 


Francis  E.  Lloyd  —  54  —  Carnivorous  Plants 

is  a  pinnate  structure  obscured  by  secondary  changes.  They  are  more 
or  less  conspicuous  on  mature  leaves  in  some  species  {N.  ampullaria) 
while  on  others  the  spur,  as  it  is  called,  is  a  tapering  simple  conical 
projection  often  much  displaced  by  the  secondary  growth  of  the  tissues 
beneath  it  so  that  the  lid  is  moved  forward  to  occupy  an  apparently 
terminal  position  (4—10;  7  —  23).  Meanwhile  the  leaf  blade  de- 
velops more  or  less  in  front,  i.e.  on  the  ventral  surface,  of  the  enlarging 
ascidium  in  two  usually  deep  ridges,  the  margins  of  which  are  con- 
tinuous to  the  base.  From  their  position  it  appears  clear  that  the 
ascidium  is  formed  by  the  expansion  chiefly  of  the  lower  moiety  of 
the  midrib,  so  that  at  full  growth  the  leaf  margins  mark  the  limits  of 
the  upper  surface  of  the  midrib. 

In  adventitious  shoots  produced  by  forcing  cuttings,  good  material 
of  which  I  obtained  at  Munich,  various  embryonic  conditions  of  the 
leaf  are  preserved  in  the  mature  condition,  which  are  always  small 
and  embryonic  ("juvenile")  in  appearance  as  in  fact.  This  is  to  be 
referred  to  the  failure  locally  of  the  incidences  of  growth  which  would 
mold  the  leaf  into  the  mature  form,  such  as  the  failure  of  the  leaf  to 
elongate  in  the  region  giving  rise  to  the  tendril;  or  the  continuation  of 
growth  where  it  is  normally  suppressed,  such  as  in  the  narrowing  of 
the  blade  at  the  base  of  the  ascidium.  The  former  is  shown  in  Fig. 
7  —  II  which  is  nearly  mature,  the  leaf  blade  being  here  narrowed  in 
the  region  which  in  a  completely  developed  leaf  would  have  become 
the  tendril.  The  second  condition  is  shown  in  Fig.  7  —  13  in  which 
it  is  seen  that  the  leaf  blade  has  expanded,  beginning  to  do  so  at  the 
middle  point  of  the  ascidium  instead  of  below  the  base.  In  both  these, 
as  in  other  early  stages  of  development,  the  apparent  "two-lobed" 
condition  of  the  lid,  seen  by  Bower  and  others,  stands  out.  That  this 
is  more  than  appearance  may  be  doubted.  It  may  be  contended  that 
the  lobing  may  be  an  appearance  due  merely  to  the  infolding  of  the 
middle  longitudinal  zone,  the  marginal  zones  resting  on  the  rim  of  the 
pitcher,  which  during  the  earlier  stages  of  development  is  laterally 
compressed  so  that  the  sides  of  the  mouth,  that  is  of  the  rim,  are 
close  together  and  parallel  (7  —  24;  8—  19).  The  presence  of  emargi- 
nation  is  not  by  any  means  general,  and  at  best,  as  Goebel  points  out, 
its  presence  is  not  an  indication  of  lobation.  In  any  event  emargina- 
tion  may  easily  occur  when  it  does,  from  the  manner  of  longitudinal 
folding  by  mutual  pressure  of  the  rim  and  Hd  apex. 

The  spur  (we  continue  to  treat  of  juvenile  leaves  of  short  shoots) 
is  usually  broad  and  lobed,  and,  being  the  organic  leaf  apex  (Hooker) 
receives  the  terminal  part  of  the  mid  vein,  which  does  not  pass  into 
the  lid,  so  that  this  is  devoid  of  a  midvein  (7  —  7-10).  Below  the  base 
of  the  spur,  however,  the  midvein  of  the  pitcher  may  send  anastomoses 
joining  it  with  lateral  veins.  The  venation  of  the  spur  is  made  up 
almost  wholly  of  lateral  veins  derived  from  far  down  at  the  base  of  the 
pitcher,  swerving  around  from  back  to  front,  and  then  back  again 
below  the  rim.  In  specimens  resembling  the  more  adult  type  of 
pitcher,  veins  appear  in  the  lid  which,  though  suggesting  a  midvein,  are 
really  branches  and  anastomoses  between  the  laterals  and  the  midvein 
(7  —  9;   Text  fig.  2,  p.  63). 

The  mature  leaf  may  in  some  species  attain  a  length  of  one  to 


Chapter  IV  —  55  —  Nepenthes 

three  feet.  It  consists  of  an  expanded  base,  sometimes  connate  about 
the  supporting  stem,  and  expands  above  into  an  elongate  blade  cor- 
responding morphologically  to  the  narrowed  portion  of  the  seedHng 
leaf.  At  the  apex  it  may  sometimes  be  found  to  be  peltate  {N.  clip- 
eata),  and  this,  as  above  said,  is  compared  by  Macfarlane  to  the 
peltation  observed  by  him  of  the  two  ventral  ridges  just  below  the 
mouth  of  the  pitcher.  Beyond  this  there  occurs  a  tendril  which  is 
short  and  non-functional  as  such  in  soil  rosettes  {e.g.  N.  ampullaria), 
but  which  in  the  climbing  forms  becomes  long,  stout  and  twining. 
Sachs  (1896,  through  Goebel)  held  that  the  tendril  activity  (the 
actual  winding)  acts  as  a  stimulant  to  the  growth  of  the  pitcher,  but 
the  evidence  is  not  convincing,  for  it  is  quite  usual  to  find  well  de- 
veloped pitchers  when  no  winding  has  intervened  (4  —  7,  8).  Though 
the  tendrils  wind  about  supports,  they  may  wind  even  when  supports 
are  not  available;  but  it  is  not  true,  as  Oudemans  thought,  that  this 
winding  is  a  means  of  bringing  the  pitchers  into  the  proper  position. 
The  sensitive  tissues  which  are  responsible  for  this  occur  at  the  base 
of  the  pitcher  and  neighboring  portion  of  the  tendril  (Stern). 

The  Pitcher.  —  It  is  with  the  structure  and  behavior  of  the  mature 
pitcher  that  we  are  chiefly  concerned.  It  shows  a  considerable  variety 
of  form,  from  that  of  a  cylinder  (7\^.  phyllamphora,  N.  gracilis),  a 
cylinder  modified  by  a  basal  globular  expansion  {N.  ventricosa,  N. 
Lowii),  an  open  funnel,  narrowest  at  the  base  {N.  inermis,  N.  dubia), 
to  an  oval  sac  slightly  compressed  laterally  (N.  ampullaria).  All  of 
these  forms  have  been  illustrated  by  Danser  (1928).  In  most  species, 
and  this  is  especially  noticeable  in  the  approximately  cylindrical  ones, 
the  upper  one-third,  more  or  less,  is  somewhat  constricted,  correspond- 
ing in  extent  to  the  waxy  zone  within  (to  be  described  beyond).  From 
some  species  this  is  absent  {N.  ventricosa,  N.  bicalcarata,  N.  ampul- 
laria) or  may  be  very  narrow  {N.  intermedia).  It  is  said  to  be  ex- 
ceptionally present  in  forms  from  which  it  is  normally  absent.  The 
size  of  the  pitcher  may  reach  in  some  species  the  length  of  a  foot, 
with  a  capacity  great  enough  to  accomodate  small  mammals,  birds, 
etc.,  e.g.  N.  rajah  25-30  cm.  by  12  cm.  (Hooker).  The  majority  of 
species  have  pitchers  which  range  from  5  to  15  cm.  in  length. 

The  pitchers  produced  even  in  a  single  individual,  this  being  a 
character  of  the  species,  may  be  of  two  or  even  three  different  forms, 
that  is,  they  may  be  mono-,  di-,  or  tri-morphic  (Macfarlane).  When 
this  occurs,  the  rosette  leaves  in  contact  with  the  soil  differ  from  the 
cauline,  the  uppermost  of  these  being  again  different  from  those  mid- 
way of  the  plant.  Thus  N.  ampullaria  has  rosette  leaves  with  goblet 
shaped  pitchers,  the  cauHne  ones  being  cylindrical;  while  in  N.  Bosch- 
iana,  N.  maxima  and  A^.  Vieillardii,  the  lowermost  pitchers  are  globose, 
the  lower  cauline  tubular  and  the  uppermost  infundibuHform  or  cornu- 
copioid.  So  different  are  they  that  different  pieces  of  the  same  species 
have  been  described  as  different  species.  In  some  cases  the  internal 
structure  differs,  there  being  a  wax  zone  in  some  pitchers  and  not  in 
others.  In  color  the  pitchers  are  usually  green  with  more  or  less 
splotchings  of  red,  and  when  this  occurs  in  the  rim  the  color  lies  in 
very  definitely  regular  transverse  stripes,  obviously  connected  with  the 
regular,  straight-rowed  arrangement  of  the  cells.     Some  species  have, 


Francis  E.  Lloyd  —  56  ^ —  Carnivorous  Plants 

according  to  Macfarlane,  ''porcellaneous  white"  pitchers  marked 
with  "deep  crimson  splotches"  {N.  Raffiesiana  var.  nivea,  N.  Bur- 
bidgei).  Others  have  uniform  deep  red  color,  even  when  growing  in 
the  shade,  or  covered  with  a  growth  of  moss,  while  the  pitchers  ex- 
posed to  greater  illumination  are  less  deeply  colored,  (N.  Rajah,  N. 
Edwardsiana) .  These  relations,  in  perhaps  less  striking  fashion, 
are  shown  by  N.  ampullaria  in  which  the  soil  pitchers  are  splotched 
with  red  while  the  cauline  pitchers  are  almost  or  entirely  free  of  color. 
Some  species  have  pale  green  pitchers  with  no  markings  at  all  (N. 
ventricosa)  {4  —  7).  On  account  of  the  frequently  brilliant  coloring,  be- 
lieved by  Troll  to  be,  in  addition  to  the  nectar,  attractive  to  insects, 
the  pitchers  are  regarded  by  Malayans  as  "bungabunga"  (flowers) 
(Troll  1939).  The  glossy  rim  may  be  entirely  red  or  trans- 
versely striped  with  red,  or  devoid  of  color  other  than  green.  The 
outer  surface  of  the  pitcher  is  usually  clothed  with  a  rough  pubescence 
of  many  branched  hairs,  each  rising  from  a  unicellular  stalk  with  thin 
walls,  those  of  the  rest  of  the  cells  forming  the  branching  complex 
being  very  thick  {S  —  4).  There  are  also  low  sessile  stellate  hairs 
which  in  some  species  {N .  intermedia)  stand  in  a  pit  {8 — 1-3)- 
The  four  arms  forming  the  star  are  each  two-celled,  but  the  whole 
may  be  composed  of  eight  to  sixteen  cells.  They  are  regarded  as 
hydathodes  by  Stern  (191 6).  These  trichomes  are  by  no  means  con- 
fined to  the  pitchers,  however,  the  whole  plant  showing  a  marked  de- 
gree of  the  rough  hairiness,  especially  along  the  tendrils  and  the  backs 
of  the   "phyllode." 

Borne  on  a  tendril,  often  hanging,  the  pitcher  in  order  to  function 
must  stand  upright.  This  is  accomphshed  by  tropisms  resident  in 
the  region  between  the  pitcher  base  and  the  end  of  the  tendril.  Since 
the  tendril  is  positively  geotropic,  and  the  pitcher  "  geotropically  con- 
ditioned," though  not  simply  negatively  geotropic  (Stern),  the  usual 
position  is  a  sharply  upturned  pitcher  on  the  end  of  the  vertically 
hanging  tendril. 

In  one  species  at  least  {N .  hicalcarata)  the  portion  of  the  tendril 
near  the  pitcher  is  swollen  and  hollow  to  form  a  formicary,  but  the 
space  is  separated  from  that  of  the  pitcher  by  a  partition  and  it  re- 
mains filled  with  air.  Ants  usually  eat  away  an  entrance  into  the  in- 
terior, as  they  do  e.g.  into  the  stems  of  Cecropia  and  the  thorns  of 
Acacia  sp.  etc.,  and  use  the  hollow  as  a  nest. 

The  mouth  of  the  pitcher  is  always  more  or  less  oblique,  and  dur- 
ing development  is  hermetically  sealed  by  the  lid,  which  opens  only 
when  the  definitive  size  and  shape  of  the  pitcher  is  almost  attained. 
It  is  well  known  that,  until  this  happens,  the  contained  fluid,  of  which 
there  is  a  considerable  amount,  is  kept  in  a  bacteria-sterile  condition. 
The  method  by  which  the  edge  of  the  lid  is  kept  hermetically  sealed 
during  development  is  both  interesting  and  unique.  There  is,  it  must 
be  observed,  no  concrescence  or  fusion  of  tissues  (7  —  24;  8  —  19). 
What  happens  is  that  the  edge  of  the  hd  is  in  the  first  place  tightly 
applied.  Then,  whatever  chink  there  may  be  left  is  tightly  sealed  by 
a  dense  growth  of  branching  hairs  which  clothe  the  outer  face  of  the 
pitcher  mouth  and  the  edge  of  the  Hd  (Macfarlane  1908).  These 
interweave  so  as  to  produce  a  firm  wad  of  cottony  stuff.     As  long  as 


Chapter  IV     —57—    Nepenthes 

the  growth  of  the  two  parts  is  synchronous  the  sealing  remains  effec- 
tive. During  the  last  phase  of  development  differences  in  growth  cause 
the  Hd  and  pitcher  mouth  to  separate  and  the  former,  as  the  result  of  the 
growth  of  the  isthmus  of  tissue  between  the  hd  and  pitcher  edge,  is 
hfted  in  many  cases  a  considerable  height  above  the  mouth  (7—  22,  23). 
In  its  final  position  the  lid  may  overhang  the  mouth,  becoming  a 
more  or  less  effective  bar  to  the  entrance  of  rain,  especially  in  such 
forms  as  N.  Rajah  Hook,  in  which  the  lid  continues  to  grow  and  attains 
a  sufficiently  large  size  to  overshade  the  opening  entirely.  In  other 
species  it  remains  small  and  narrow  and  turns  completely  back,  fully 
exposing  the  mouth  of  the  pitcher  (.V.  ampidlaria  Jack,  .V.  dubia 
Dans.)  (4  —  9),  and  though  overhanging  the  mouth,  is  obviously 
quite  ineffective  as  a  roof  (A',  incrmis  Dans.).  When  the  lid  is  large 
and  overhanging  in  position,  it  is  thin,  more  or  less  emarginate,  in- 
dicating to  Bower  and  to  Macfaelane  that  the  two  halves  of  the  lid 
represent  paired  pinnae.  In  some  species  there  is  a  median  ridge  on 
the  inner  surface  bearing  numerous  nectar  glands  (7  —  25),  and  in 
other  species  there  is  a  shallow  invagination  near  the  apex,  the  function 
of  which,  if  it  has  one,  is  not  clear;  or,  as  in  .V.  Ladenhurgii,  there  is  a 
short  clavate  projection.  In  .V.  Tivcyi  (and,  says  Macfarlane,  in  N. 
maxima)  there  is  a  short,  thick,  glandular  crest  or  ridge  near  the  base 
and  near  the  apex  a  sharp  thorn-like  projection,  hollow  on  its  forward 
surface  (7  —  25). 

The  under  surface  of  the  Hd  is  the  seat  of  numerous  nectar  glands 
except  in  a  few  species  {N .  ampidlaria,  N.  inermis  probably).  In 
N.  Lowii  Hook.,  it  is  suppKed  with  many  small  appendages  or  bristles, 
as  Danser  calls  them,  with  nectar  glands  on  the  general  surface  be- 
tween their  bases. 

At  or  below  the  base  of  the  hd  on  the  outside  of  the  pitcher  stands 
the  spur.  This,  as  may  readily  be  ascertained  by  examining  the  young 
pitcher  during  development,  is  the  apical  portion  of  the  leaf  (Hooker) 
and  it  appears  that  the  Hd  is  an  outgrowth  over  the  upper  surface. 
The  spur  is  very  small  in  some  species  and  stands  just  at  the  base  of 
the  lid  {N.  inermis).  In  N.  bicalcarata,  e.g.,  it  becomes  considerably 
displaced  downwardly,  and  stands  out,  quite  suggesting  a  spur,  from  a 
neck  of  tissue  which  raises  the  lid  far  above  the  opening  {N.  bical- 
carata) (7  —  23).  Sometimes  the  spur  is  compound  and  bears  pinnae- 
Uke  laterals,  suggesting  lateral  leaflets  (Macfarlane)  {N.  ampidlaria, 
N.  phyllamphora) . 

Special  anatomy.  —  The  edge  of  the  mouth  of  the  pitcher  is  of  dis- 
tinctly pecuhar  structure.  It  appears  to  be  a  parapet  standing  on  the 
edge,  sloping  inwardly  on  the  whole,  but  with  the  outer  margin  some- 
times turned  more  or  less  down.  In  a  section  of  it  made  transversely, 
it  is  T-shaped  with  the  arms  of  the  T  of  various  lengths,  according  to 
the  species.  In  the  majority  both  arms  are  of  some  length,  so  that  the 
parapet  in  such  cases  overhangs  as  much  on  the  outside  as  on  the  in- 
side, and  with  a  general  slope  as  much  away  as  toward  the  opening  of 
the  pitcher.  N.  ventricosa  may  be  cited  as  an  example  of  this  con- 
dition (7  —  16).  In  others  (7  —  15,  17)  the  inner  arm  is  short, 
the  outer  long,  while  in  .V.  inermis  (7  —  20)  both  are  very  short,  the 
outer  a  trifle  longer  than  the  inner.     In  N.  Veitchii  the  width  of  the 


Francis  E.  Lloyd  —  58  —  Carnivorous  Plants 

rim  towards  the  lid  is  so  great  (up  to  60  mm,  says  Danser)  as  to  bear 
a  likeness  to  a  "Marie  Stuart  collar"  (de  Ruiter  1935).  The  greatest 
reduction  of  the  inner  arm  is  found  in  N.  Lowii  (7  —  18),  which  has 
been  described  as  without  a  peristome  (Danser).  There  is,  however,  a 
row  of  glands  embedded  in  tissues  which  project  to  form  a  slight, 
interrupted  shelf  while  the  outer  arm  is  of  some  width  relatively.  At 
the  other  end  of  the  series  stand  such  forms  as  N.  hicalcarata,  N . 
intermedia  and  A^.  ampullaria  (7  —  19),  in  which  the  outer  arm  is  very 
short  and  tightly  reflexed  and  the  inner  very  long;  in  these  species  the 
peristome  has  a  very  pronounced  funnel  shape.  In  N.  ampullaria, 
which  forms  rosettes  of  pitchered  leaves  on  the  forest  floor,  the  pitchers 
partly  buried  on  the  humus,  the  whole  constitutes  a  group  of  pitfalls, 
each  with  a  broad  overhanging  edge  which  would  prevent  escape  quite 
effectively  in  many  cases. 

Of  the  two  arms  of  the  T,  one,  the  outer,  represents  the  true 
pitcher  mouth  edge,  outwardly  reflexed.  The  inner  arm  is  an  out- 
growth from  the  inner  wall  near  the  edge.  This  is  easily  seen  to  be 
the  case  in  young  pitchers  during  their  development  (Heide,  19 10) 
{8 —  19).  In  any  case  it  can  be  seen  that  the  vascular  tissues  of  the 
inner  arm  are  derived  by  sharp  branching  from  the  main  trunks  which 
extend  to  and  along  the  edge  proper. 

But  although  the  peristome  is  composed  as  it  were  of  two  flanges, 
an  outer,  the  edge  of  the  pitcher  mouth,  and  an  inner,  growing  out  as 
a  ridge  from  the  inner  wall,  the  whole  during  late  development  is  so 
moulded  that  the  two  flanges  are  amalgamated  to  constitute  a  single 
organ,  the  inner  surface  of  the  edging  flange  and  the  outer  surface  of 
the  side  flange  becoming  a  continuous  uninterrupted  surface.  The 
whole  is  mechanically  very  rigid,  for  it  is  strengthened  by  a  very  thick 
cuticle  and  the  surface  is  broken  up  into  minute  striae  and  coarser 
corrugations  (4  — 11).  The  latter  give  the  peristome  their  ribbed 
appearance,  and  their  most  pronounced  expression  is  reached  in  N. 
villosa  Hook.  On  the  inner  edge  of  the  peristome  the  corrugations 
end  in  minute  teeth,  and  between  each  pair  of  teeth  (7  —  21)  there  is 
an  opening,  the  mouth  of  a  large  nectar  gland  which  lies  buried  in  the 
tissues.  The  nectar  oozes  in  a  drop  held  between  a  pair  of  teeth,  of 
access  to  insects  standing  on  the  rim  and  reaching  down.  This  ar- 
rangement together  with  the  nectar  glands  on  the  under  side  of  the 
lid  constitute  a  lure,  the  ''attractive  zone"  of  Hooker.  The  hard, 
glossy  surface  of  the  peristome  is  not,  as  it  may  seem  to  the  eye,  a 
smooth,  slippery  one,  for  as  a  matter  of  observation,  small  insects 
(ants,  etc.)  can  walk  freely  on  it,  using  their  footpads.  When  the 
tissues  below  the  base  of  the  lid  are  considerably  extended,  as  they 
are  in  A^.  hicalcarata  and  N.  intermedia  (7  —  22,  23),  the  peristome  is 
extended  likewise,  and  in  these  two  cases,  but  only  in  these,  there  is,  at 
its  extreme  upper  ends  which  are  separated  by  the  base  of  the  lid,  a 
very  strong  development  of  the  last  dozen  or  so  corrugations  to  form 
two  long  sharp  thorns,  resembling  the  canine  teeth  of  a  cat.  In 
A^^.  hicalcarata,  these  are  long,  solid,  curved,  very  sharp  and  distinctly 
canine  in  appearance.  A  rather  fanciful  explanation  of  the  use  of  these 
was  advanced  by  Burbidge  (1880)  who  pointed  out  that  the  Tarsius 
spectrum,    a   small,    insectivorous,    monkey-like   mammal,    "visits   the 


Chapter  IV  —  59  —  Nepenthes 

pitchers  of  N.  Rafflesiana"  (which  is  similar  to  N.  hicalcarata  in  all 
respects  except  that  it  lacks  the  canine-like  thorns),  "and  empties 
them  of  their  prey,  but  not  those  of  A^.  hicalcarata,  in  which  the  very 
sharp  spurs  are  so  arranged  that  the  tarsius  is  certainly  held  and 
pierced  when  he  inserts  his  head  to  see  what  there  is  in  the  pitcher." 
GoEBEL  remarks  of  this  idea  that  more  study  of  the  matter  in  the 
habitat  is  required.  In  N.  intermedia  the  spurs  are  interesting  because 
they  are  broad,  and  are  quite  obviously  made  up  of  a  group  of  corru- 
gations; they  are  not  sharp  and  tooth-Hke,  and  could  not  act  in  the 
manner  described  by  Burbidge  for  N.  hicalcarata.  Yet  so  far  as  we 
know,  the  latter  shows  no  superiority  over  the  former  or  over  N. 
Rafflesiana  in  the  struggle  for  existence.  /V.  intermedia  is  a  hybrid  of 
horneensis  and  Rafflesiana  (the  former  parent  is  uncertain,  Mac- 
farlane).  If  this  occurred  in  nature  it  would  be  doubtful  if  the 
specialized  tooth-Hke  portion  of  the  peristome  could  act  adaptively  as  a 
beginning  for  the  condition  seen  in  N.  hicalcarata. 

The  several  interpretations  of  the  morphology  of  the  Nepenthes 
leaf,  as  resumed  in  part  by  Troll  (1932,  1939),  are  the  following: 

1.  The  Hd  is  the  lamina  of  the  leaf,  the  rest  is  the  petiole  with 
highly  specialized  regions,  phyllodial  at  the  base.  This  view  is  trace- 
able to  A.  P.  DE  Candolle  (1827).  Among  others  Goebel  took  this 
position  in  his  earlier  writings  (1884).  The  recognition  by  Hooker 
that  the  spur  is  the  true  organic  apex  of  the  leaf  threw  this  out  of 
court.  According  to  Bower,  Goebel  regarded  the  lid  as  only  a  part 
of  the  lamina,  the  rest  appearing  in  modified  form  as  the  pitcher, 
tendril,  etc. 

2.  Instead  of  regarding  the  laminar  portion  of  the  leaf  as  petiolar, 
WuNSCHMANN  (1872)  preferred  to  see  in  it  the  "lower  part  of  the  leaf 
blade",  and  therefore  that  the  leaf  is  non-petiolate.  The  evidence 
from  development  denies  this. 

J.  The  pitcher  has  arisen  phylogenetically  as  an  apical  gland, 
which  through  enlargement  and  specialization  became  the  complex  of 
organs  which  we  now  know.  This,  Hooker's  interpretation,  was 
based  in  part  on  embryological  observations  and  by  comparison  with 
such  leaves  as  that  of  Flagellaria,  Gloriosa  which  have  a  cirrhus,  a 
terminal  tenuous  apex  serving  as  a  tendril.  Faivre  held  a  somewhat 
similar  view  that  the  pitcher  arises  in  the  elongated  midrib.  But  the 
spur  is,  as  said  above,  the  organic  apex  of  the  leaf  (Hooker). 

4.  The  leaf  arises  as  a  peltate  one.  According  to  this  view  the 
pitcher  is  a  peltate  leaf  in  which  the  margin  is  contracted  so  that  the 
upper  surface  lines  a  hollow  organ,  the  pitcher.  Its  outer  surface  is 
the  lower  leaf  surface.  Dickson,  receiving  his  impulse  from  Baillon's 
examination  of  the  embryology  of  the  Sarracenia  leaf,  and  impressed 
by  the  analogy  supplied  by  the  interrupted  leaf  of  Codiaeum  sp.,  wrote 
"it  seems  highly  probable  that  in  Nepenthes  we  have  to  deal  with  a 
leaf,  the  lamina  of  which  is  interrupted  in  the  middle  of  its  course  by 
becoming  reduced  to  a  midrib  and  that,  while  the  proximal  portion  of 
the  lamina  retains  its  typical  form  of  a  flat  expansion,  the  distal  por- 
tion becomes  peltately  expanded  into  a  funnel  or  pitcher. "  But 
Troll,  though  conceding  the  outward  resemblance,  one  which  strikes 
anyone  who  has  made  the  comparison,  even  to  the  peltation  of  the 


Francis  E.  Lloyd —60— Carnivorous  Plants 

lower  moiety  of  the  blade  with  a  similar  condition  found  in  N.^  clipeata 
Dans.,  points  out  that  the  resemblance  is  but  superficial,  since  the 
Codiaeum  leaf  is  petioled  while  the  ''blade"  of  Nepenthes  is  more 
probably  an  expansion  of  the  leaf  base  (Blattgrund)  to  be  compared 
with  the  primary  leaf  of  Pothos.  Goebel  also  held  the  view  that  the 
pitcher  is  a  peltate  leaf  developed  into  a  tubiform  one,  and  compared 
the  pitcher  of  Nepenthes  with  that  of  Utricularia,  which  is  also  ter- 
minal either  to  a  single  "leaf"  {Polypompholyx,  Utricularia  Menziesii, 
etc.),  and  has  a  lid  (door)  which  springs  laterally  from  the  true  apex  of 
the  trap  visible  as  such  in  some  species,  e.g.  U.  Welwitschii,  or  to  a  leaf 

segment. 

5.  The  leaf  of  Nepenthes  is  not  simple  but  compound.  According 
to  Bower  the  lid  arises  as  a  double  organ,  the  two  congenitally  fused 
(^_  4)  ^  and  represents  two  leaflets.  This  was  based  on  embryological 
observations.  Macfarlane  went  still  further  and  claimed  to  be  able 
to  analyze  the  whole  leaf  into  "3  to  4  or  5  pair  of  leaflets",  the  basal 
lamina,  the  wings  on  the  ventral  surface  of  the  pitcher,  the  lobes  of  the 
Kd  (Bower),  and  one  or  two  pairs  of  lateral  appendages  sometimes 
occurring  on  the  spur,  which  itself  terminates  the  leaf.  This  idea  goes 
back  to  Ch.  Morren  (1838)  (Goebel  1891)  who  regarded  the  leaf  as 
having  fused  foholes  and  the  lid  as  a  terminal  leaflet.  Goebel  (1923) 
remarked  that  this  view  might  have  been  entertained  if,  in  the  circle  of 
relationship,  plants  with  compound  leaves  were  known. 

6.  Troll  put  forward  the  theory  that  the  Nepenthes  leaf  is  a  com- 
plete parallel  to  the  ordinary  foliage  leaf  consisting  of  a  basal  zone 
(Blattgrund),  a  petiole,  and  blade  which  is  the  pitcher  (Oberblatt) 
disturbed,  however,  by  a  modification  of  the  petiole  whereby  it  is  at- 
tended by  a  displacement  upwards  of  the  edges  of  the  leaf  base  to 
become  the  wings  of  the  pitcher.  Such  a  displacement  occurs  in  Syn- 
gonium  podophyllum,  and  I  have  shown  (1914)  that  it  occurs  in  Gos- 
sypium  in  which  the  flower  peduncle  normally  suffers  displacement  up 
the  internode  above,  bringing  the  flower  into  an  unusual  position. 
More  specifically,  Troll  sets  forth  that  (7)  the  leaf  base  consists  of  a 
clasping  bottom  leaf  zone  which  is  contracted  briefly  to  reexpand  to 
form  the  conspicuous  lamina,  and  which  in  some  species  extends  at  its 
apex  across  the  base  of  the  tendril  in  total  stipulation  {N.  clipeata, 
and  others).  (2)  The  blade  is  differentiated  into  the  petiole  and  true 
leaf  blade.  The  former  takes  the  form  of  a  tendril,  the  latter  the 
pitcher,  the  blade  in  peltate  form.  But  here  the  relation  between  the 
petiolar  structure  and  the  peltation  does  not  behave  so  simply  as  in 
simple  peltate  leaves,  (j)  The  spur  is  unifacial  (as  in  Pothos).  Arber 
(1941)  questions  this  view.  At  its  base,  the  edge  of  the  blade  grows 
to  form  a  transverse  connection  from  which  the  lid  arises.  This  again 
is  total  stipulation. 

The  supporting  evidence  is  now  briefly  stated.  (/)  In  the  first 
place  the  tendril  is  of  bifacial  structure  (Troll)  {8  —  20),  and  not,  as 
C.  P.  de  Candolle  (1898)  thought,  unifacial.  The  arrangement  of  the 
fibrovascular  bundles  is  not  concentric  with  respect  to  phloem  and 
xylem,  since  the  wood  faces  ventrally  in  the  ventral  moiety  of  the 
organ.  I  can  confirm  this.  (2)  Reexamining  the  embryology  of  the 
leaf,  it  is  clear  that  in  the  primary  leaf  (in  seedlings)  the  thinned  out 


Chapter  IV  —  61  —  Nepenthes 

basal  part  is  composed  of  two  halves  which  separate  above  and  now 
appear  as  the  wings  on  the  adaxial  pitcher  wall  to  form  a  transverse 
membrane  below  the  rim  (Hooker,  Dickson,  Macfarlane).  When 
the  transverse  connection  is  absent  (which  Goebel  held  to  be  the  case), 
there  is  often  an  indication  of  it  in  the  presence  of  a  row  of  gland-like 
emergencies  indicating  such  a  connection  (Stern  observed  such). 
Macfarlane  said  that  a  transverse  strand  of  the  venation  also  is  to  be 
taken  as  an  indication,  but  I  cannot  substantiate  this  (7  —  7,  9). 
Hooker's  view  that  the  pitcher  is  "the  hollowed  out  upper  half  of  the 
petiole"  is  discarded,  and  Dickson's  theory  of  contracted  peltate  leaf 
blade  accepted.  The  earlier  embryological  condition  is  now  examined. 
In  an  early  stage,  when  the  leaf  appears  as  a  low  conical  structure, 
there  is  a  pit  just  below  the  apex  on  the  adaxial  side.  Just  below  it  is  a 
transverse  weal,  the  transverse  connection  of  the  edges  of  the  leaf  base. 
The  leaf  blade,  it  is  important  to  note,  arises  on  the  abaxial  side  of 
the  leaf  base,  the  latter,  as  in  Iris,  presenting  total  stipulation.  The 
blade  cannot  therefore  be  an  extension  of  the  apex  of  the  stipule,  but 
though  near  it  must  arise  below,  abaxially.  If  without  further  differ- 
entiation this  embryonic  stage  passes  into  permanent  form,  a  primary 
leaf  results,  in  which  the  pitcher  stands  in  a  dorsal  position.  What 
authors  have  designated  the  blade  is  therefore  only  the  leaf  base 
showing  total  stipulation,  of  which  the  transverse  sector,  as  already 
said,  may  be  suppressed.  In  support  of  this  I  may  point  out  that  the 
extent  of  the  pitcher  wings  is  not  commensurate  with  that  of  the 
veins  beneath  them,  the  wings  often  extending  beyond  the  venation, 
which  swerves  away  to  pass  around  the  mouth  of  the  pitcher.  This 
in  the  adult  leaf.  In  intermediate  forms,  the  development  of  the 
rudiments  proceeds  further,  especially  the  tendril,  by  contraction  be- 
low the  pitcher.  Nevertheless  the  wings  of  the  pitcher  pass  down 
along  the  edges  of  the  tendril.  In  purely  adult  forms  the  tendril  be- 
comes entirely  wingless.  Troll  now  asks:  (7)  May  the  tendril  be  re- 
garded as  the  petiole  of  the  leaf  between  the  pitcher  as  blade  and 
the  leaf  base?  (2)  How  are  the  wings  of  the  pitcher  to  be  understood? 
To  answer  these  he  analyzes  the  embryonic  condition.  In  this  a  peti- 
ole is  not  recognizable  as  such,  but  assuming  that  it  must  be  there,  he 
postulates  a  zone  of  tissue,  broad  abaxially  and  narrow  or  absent 
adaxially,  the  narrow  adaxial  edge  of  this  wedge  of  tissue  impinging 
on  the  leaf  base  at  its  transverse  weal  (Wulst).  The  elongation  of 
this  petiolar  zone  meets,  however,  an  impediment  in  the  leaf  base  tis- 
sues, which  converge  below  the  mouth  depression.  In  consequence,  the 
leaf  base  is  dragged  out  along  with  the  petiole  and  adaxial  side  of  the 
pitcher  up  to  the  edge  of  the  mouth  (but  not  quite,  it  may  be  added). 
The  whole  adaxial  side  of  the  young  leaf  from  the  leaf  base  to  the 
mouth  (I  should  say  not  quite)  belongs  to  the  leaf  base  and  one  may 
come  to  the  view  that  the  tendril  is  an  extension  of  the  leaf  base  as 
Goebel  showed  to  be  the  case  for  the  fan-palms.  Nevertheless  Troll 
insists  that  the  tendril  is  a  petiole,  though  it  may  in  some  instances 
(such  as  ;V.  clipeata)  have  an  unifacial  structure  in  the  lower  portion. 
But  the  leaf  base  is  never  unifacial,  always  bifacial.  But  where  the 
tendril  is  bifacial  it  should  be  regarded  not  as  entirely  independent 
indeed,  but  concrescent  with  the  leaf  base. 


Francis  E.  Lloyd  —  62  —  Carnivorous  Plants 

As  to  the  pitcher  wings,  which  show  a  wide  variety  of  definitive 
development,  they  may  be  considered  as  secondary  outgrowths,  like 
those  of  Cephalotus  or,  as  Goebel  held,  hke  the  keel  of  Sarracenia. 
Others  have  held  them  to  be  leaf  margins.  Troll  comes  to  the  con- 
clusion that  they  are  the  edges  of  the  leaf  base  dragged  out  (ver- 
schleppte),  while  growing  themselves,  by  the  growing  petiole  and  leaf 
beneath.  Concerning  the  lid,  its  interpretation,  before  Hooker  rec- 
ognized the  spur  as  the  true  apex  of  the  pitcher  leaf,  was  easy,  as 
being  the  true  apex.  Stern  's  suggestion  that  it  arises  by  a  longitudinal 
splitting  of  the  apical  meristem  is  untenable  in  view  of  the  anatomical 
facts.  The  views  of  Bower,  Macfarlane  and  Goebel  are  also  dis- 
carded. The  key  to  the  problem,  says  Troll,  is  to  be  found  in  the 
structure  of  the  spur,  which  is  unifacial,  from  which  it  follows  that 
the  edges  of  the  leaf  blade  at  its  base  run  together  and  unite  (total 
stipulation).  Important  here  is  a  fact,  pointed  out  by  Heide  (1910) 
that  the  inner  (lower)  face  of  the  lid  is  anatomically  identical  with  that 
of  the  interior  of  the  pitcher,  and  the  upper  (outer)  with  that  of  the 
outer  pitcher  surface.  The  lid  cannot  therefore  be  an  "outgrowth  of 
the  upper  surface"  as  Goebel  held.  It  should  here  be  noted  that 
Dickson  stated  (and  truly)  that  the  base  of  the  lid  in  primary  leaves 
(as  also  in  other  juvenile  leaves)  is  very  broad,  extending  "around 
fully  one  half  of  the  orifice  of  the  pitcher"  (7  —  7).  Troll's  view  as 
just  stated  is  certainly  supported  by  an  examination  of  the  venation  of 
even  old  adult  pitchers  in  which  the  isthmus  between  the  orifice  and 
the  lid  is  very  narrow.  A  macerated  preparation  of  A^.  formosa  demon- 
strates this,  by  which  it  is  seen  that,  as  already  indicated  in  discussing 
primary  leaves,  the  venation  is  but  that  of  a  totally  stipulate  leaf 
blade,  sharply  constricted  below  the  apex.  The  apical  portion,  the  lid, 
may  in  adult  leaves  be  supplied  with  a  midvein  which  is  secondary 
since  in  primary  leaves  such  a  midvein  does  not  exist.  And  when  pres- 
ent, as  it  is  in  adult  leaves,  it  is  evidently  smaller  and  is  dominated 
by  the  lateral  veins. 

A  novel  interpretation  of  the  rim,  lid  and  spur  has  been  advanced 
by  Mrs.  Arber  (1941).  In  doing  this  she  rejects  all  earlier  views,  that 
of  Troll  included,  which  hold  that  the  lid  is  a  transversal  pinna.  If 
Troll  is  right,  she  says,  the  veins  of  the  fid  should  have  their  wood 
upwards,  not  downwards.  She  questions  also  the  statement  of  Troll 
that  the  spur  is  unifacial,  though  admitting  that  the  veins  of  the  spur 
"tend  toward  a  radial  arrangement."  Had  Troll  selected  A'^.  intermedia 
and/or  A^.  hicalcarata  for  study,  his  evidence  would  have  been  still 
more  convincing.  Having  disposed  of  the  spur  as  the  leaf  apex,  Mrs. 
Arber  argues  that  "both  the  lid  and  the  median  point  are  merely 
localized  expressions  of  collar-forming  activity,  which  is  responsible  for 
the  double  curve-over  of  the  aperture  edge  ....  the  lid,  which  is 
turned  down  in  youth,  corresponding  to  the  inner  curve-over,  and  the 
median  point  to  the  outer  curve-over." 

"The  relative  hypertrophy  of  the  lid  and  median  point  may  be 
correlated  with  the  special  character  of  the  venation  ....  of  the 
parallel  type  as  in  other  pitchers.  The  midrib  passes  directly  to  the 
junction  of  the  hd  and  median  point,  while  the  veins  of  the  adaxial 
part  of  the  pitcher  also  show  a  strong  tendency  to  converge  upon  the 


Chapter  IV 


63 


Nepenthes 


apical  region.  The  median  point  and  the  Hd  can  thus  draw  upon  a 
richer  vascular  supply  than  the  rest  of  the  collar,  which  is  entered 
only  by  minor  lateral  veins,  and  thus  overgrowth  of  the  median  region 
may  be  stimulated." 

It  may  be  answered  (/)  that  the  midrib  vein  enters  and  traverses 
the  spur  to  its  tip  (7  —  9,  10;  Text  fig.  2).  (2)  The  Kd  cannot  be 
regarded  as  the  inner  "curve-over"  since  the  surface  of  the  rim  would 
then  be  a  part  of  the  outer  pitcher  surface,  which  the  histology  of  the 
rim  denies.  The  "inner  curve-over"  would  then  have  to  be  sought  as 
an  outgrowth  of  the  under  surface  of  the  lid,  and  that  does  not  exist, 
(j)  The  vascular  system  of  the  lid,  assuming  its  origin  as  a  transverse 
weal,  along  the  pitcher  edge  (Troll),  is  as  it  should  be.  {4)  The 
anatomy  of  the  spur  shows  it  to  be  the    organic    apex   of   the    leaf 


Fig.  2.  —  Nepenthes  (various  species).  —  i,  Venation  of  lid  and  spur  of  a  pitcher 
I  cm  long;  2,  of  a  pitcher  2  cm  long;  3,  of  a  pitcher  2.5  cm  long;  4,  of  a  full  sized  pitcher; 
the  veins  (dotted  lines)  lie  at  a  different  level  and  more  ventral  to  the  rest  (solid  lines); 
5,  Section  of  pitcher  wall  just  below  the  insertion  of  the  spur  in  N.  intermedia;  6,  Section 
through  the  spur  of  N.  bicalcarata. 

(Hooker),  this  being  supported  by  additional  evidence  here  from 
N.  intermedia  and  N.  bicalcarata  (Text  fig.  2).  (5)  The  wide  dis- 
placement of  Hd  and  spur  in  these  and  other  species  is  not  accounted 
for. 

Histology  of  the  peristome  or  rim.  — •  If  we  examine  into  the  minute 
anatomy  of  the  hard,  glossy  surface  tissue  of  the  peristome  we  find 
that  it  is  composed  of  straight  rows  of  cells,  running  across  following 
the  transverse  curve.  In  each  row  the  cells  overlap  very  much,  in  one 
direction,  the  tapering  tail  of  one  cell  overlapping  the  next  and  forming 
a  sharp  ridge  along  it  {8  —  7).  The  rows  being  straight,  the  cells 
not  imbricated  as  in  the  other  pitcher  plants,  the  ridges  of  successive 
cells  overlap  the  one  over  the  other,  to  form  a  single  sharp  ridge, 
about  0.017  mm.  from  its  parallel  neighbor.  The  general  surface  is  also 
formed  into  sulci  separated  by  sharp  secondary  ridges  about  0.17  mm. 


Francis  E.  Lloyd  —64—  Carnivorous  Plants 

apart,  there  being  about  10-12  rows  of  cells  to  each  sulcus  (N.  am- 
pullaria)  {8—17).  Whether  the  very  large  ridges  that  occur  in  TV. 
villosa  are  secondary,  or  of  the  third  order  I  cannot  say,  as  I  have 
had  no  opportunity  of  examining  the  plant.  The  pubhshed  drawing  of 
Hooker  (1859)  suggests  the  former. 

The  epidermis  seen  in  a  transverse  section  is  complicated  and  re- 
quires elucidation.  One  may  see  a  row  of  cells  equal  in  size  or  larger 
cells  separated  by  a  pair  of  smaller  ones  (8 —  18).  The  latter  are  the 
backward  extensions  of  two  cells  which  straddle  the  large  one  between 
them.  Two  small  cells,  one  on  each  side  of  the  larger  one,  are  therefore 
really  the  backward  extensions  of  a  single  cell.  Atop  each  large  cell 
there  is  a  central  projection  of  various  dimensions.  This  is  the  over- 
lapping point  of  another  neighbor  cell,  and  appears  as  a  solid  mass  of 
cellulose,  or  with  a  lumen,  according  to  the  position  of  the  section. 
It  is  evident  that  the  ridge  is  composed  of  the  continuity  of  overlaps 
(Heide  1910).  N.  Lowii  presents  a  different  appearance  {8  —  12).  The 
overlapping  spur  is  not  lengthened  so  that  no  sharp  ridge  can  be  seen  in 
transverse  sections.  Only  where  the  secondary  ridges  occur  do  the  cells 
give  indication  of  striae;  these  not  as  well  marked  as  in  N.  ampullaria. 
With  regard  to  these  details  Macfarlane's  account  (1908)  is  inadequate. 

The  ridges  of  the  second  order  of  magnitude,  those  readily  seen 
by  the  naked  eye,  end  at  the  inner  edge  of  the  peristome  in  more  or  less 
prominent  teeth.  When  these  are  definite  and  prominent  there  can 
be  seen  between  them  re-entrant  bays  marking  the  marginal  pits,  at 
the  bottom  of  which  lie  the  flask-shaped  glands  first  observed  by  Hunt 
(1874),  further  studied  by  Dickson  (1883)  and  called  by  him  "mar- 
ginal glands."  The  conformation  of  the  bays  is  such  as  to  afford  a 
seat  for  sustaining  a  large  drop  of  nectar  in  position  to  attract  insects 
to  the  peril  of  falling  into  the  pitcher. 

The  secondary  ridges  of  N.  Lowii  are  very  low  and  not  conspicuous 
enough  to  catch  the  unaided  eye  except  where,  at  their  inner  extrem- 
ities, they  become  more  elevated  and  end  in  a  tooth  beneath  which 
rests  the  large  nectar  gland.  In  N.  ijiermis  a  few  low  ridges  converging 
on  the  broad  tooth  overhanging  the  gland  may  be  seen.  That  it  is 
true  that  the  general  surface  of  the  peristome  affords  a  precarious  foot- 
hold for  insects,  ants  at  least,  is  as  I  have  already  said,  doubtful. 
Knoll  found  that  they  can  use  their  footpads,  for  which,  in  spite  of 
the  minute  ridges,  the  surface  is  sufficiently  smooth. 

Histology  of  the  glaitds.  —  Brongniart  (1824)  was  the  first  to  notice 
the  glandular  character  of  the  inner  surface  of  the  Nepenthes  pitcher. 
Treviranus,  Meyen  (1837)  and  Korthals  (1839)  recognized  the  glands 
but  thought  that  they  were  subepidermal,  an  error  corrected  by 
Oudemans  (1864). 

The  pitchers  of  Nepenthes  are  conspicuously  supplied  with  glands, 
those  which  serve  to  attract  prey,  the  alluring  glands,  and  those  which 
secrete  the  fluid  of  the  pitcher,  which  is  digestive.  The  alluring  glands 
are  to  be  found  on  the  under  surface  of  the  lid  {8  —  8)  and 
between  the  teeth  of  the  inner  edge  of  the  peristome  {8 — 13).  The 
former  are  usually  dished,  biscuit-shaped,  sessile  glands  resting  in  deep- 
ish  depressions.  Some  of  these  glands,  in  shallower  depressions,  are 
to  be  found  in  the  invagination  near  the  apex  of  the  hd  in  N.  Tiveyi, 


Chapter  IV  —  65  —  Nepenthes 

suggesting  that  the  pocket  may  serve  to  hold  a  drop  of  nectar  when 
the  pitcher  is  in  active  condition.  In  this  species  also,  and  in  others 
perhaps,  in  which  a  strong  ridge  stands  on  the  median  line  on  the 
under  surface  of  the  lid,  there  occur  on  this  ridge  a  number  of  nectar 
glands,  deeply  enough  sunken  so  that  the  surrounding  rim  makes  a 
distinct  duct  (8  —  i6).  The  gland  tissues  are  limited  by  a  course  of  cells 
with  suberized  radial  walls.  The  most  strikingly  developed  alluring  glands 
are  to  be  found,  as  Macfarlane  showed,  distributed  here  and  there 
on  the  other  leaf  parts  (midrib,  tendril)  serving  to  attract  a  wander- 
ing population  of  ants  which  sooner  or  later  find  their  way  to  the 
pitcher.  These  glands  are  among  the  most  highly  developed  struc- 
turally in  the  plant  kingdom,  notably  because  of  the  deep  duct  {8  — 15). 

Digestive  glands  occur  on  the  inner  surface  of  the  pitcher  wall  in 
great  numbers  —  as  many  as  6000  per  cm.  in  A^.  stenophylla,  as  few  as 
100  in  N.  gracillinia  (Danser). 

Both  nectar  and  digestive  glands  have  the  same  structure.  They 
consist  of  a  single  course  of  deep  columnar  cells  resting  on  two  courses 
of  rounded  cells,  these  lying  in  turn  on  a  single  course  of  cells  having 
their  radial  walls  suberized,  called  by  Macfarlane  the  "Hmiting" 
layer,  and  being  in  strict  continuity  with  the  surrounding  epidermis. 
This  indicates  their  origin  which,  according  to  Oudemans,  Macfarlane 
and  Stern,  is  wholly  epidermal,  though  Fenner  has  asserted  that  they 
involve  also  the  underlying  parenchyma.  His  drawing  is  not  convinc- 
ing. As  to  the  origin  of  the  marginal  nectar  glands,  these  too  have 
been  regarded  by  Macfarlane  as  of  epidermal  origin,  but  Stern  has 
maintained  that  they  have  two  centers  of  origin,  the  deeper  portion 
of  the  gland  being  of  mesophyll,  and  only  the  upper  portion  of  epider- 
mal origin.  I  have  examined  N.  ampullaria  {8 —  13),  the  species  that 
Stern  worked  with,  and  the  evidence  favors  a  doctrine  of  uniformity, 
that  they  are  of  wholly  epidermal  origin.  The  presence  of  the  limiting 
layer  seems  to  be  decisive  evidence. 

Anatomy  of  the  pitcher  wall.  —  The  wall  of  the  pitcher  is  thin  but 
of  great  strength,  attributable  chiefly  to  the  thick- walled  epidermis 
both  within  and  without,  supported  by  the  veins  which  have  a  gen- 
erous supply  of  sclerenchyma.  The  most  interesting  feature  of  the 
wall  anatomy  is  the  occurrence  of  large  idioblasts  with  spirally  thick- 
ened walls  first  seen  by  Unger  in  Nepenthes  (according  to  Man- 
gust  1882).  These  are  very  large  spindle-  or  rod-shaped  cells  with 
clear  contents,  apparently  merely  sap,  and  multispiral  wall  thicken- 
ings. These,  when  the  tissues  are  cut  or  torn,  are  drawn  out  as  long 
cottony  conspicuous  thread.  The  natural  expectation  that  these  pe- 
culiar cells  are  connected  with  the  vascular  tissue  system  is  not  real- 
ized (GiLBURT  1 881)  as  they  do  not  stand  in  any  relation  to,  and  are 
not  at  any  point  in  contact  with  it. 

Similar  cells  occur  in  some  if  not  all  species  of  Crinum  (Mangin); 
also  in  some  orchids  {Pleurothallus,  Bulbophyllufn)  (Trecul,  through 
Mangin);  and  in  Salicornia  (Duval-Jouve  1868).  Mangin  con- 
sidered them  as  organs  of  support;  and  it  is  quite  possible  that  they 
contribute  to  the  walls  of  the  pitcher  a  considerable  degree  of  mechani- 
cal strength  which  they  certainly  display.  In  Dischidia  the  walls  of  the 
pitchers  have  in  analogous   situations   sclerenchyma   fibers.     Duval- 


Francis  E.  Lloyd —66— Carnivorous  Plants 

JouvE  thought  them  to  be  organs  of  aeration,  and  that  they  were  al- 
ways in  contact  with  sub-stomatal  cavities,  which  is  surely  not  the 
case.  I  have  satisfied  myself  that  they  are  quite  independent  of  all 
other  cells  than  those  of  the  parenchyma  in  which  they  lie.  They 
occur  elsewhere  than  in  the  pitchers.  It  is  probable  that  they  are  more 
properly  to  be  regarded  as  water-reservoirs   (Kny  and  Zimmermann 

1885). 

The  vascular  system.  —  The  course  of  the  vascular  strands  is  such  as 
to  indicate  that  the  pitcher  is  produced  by  the  expansion  chiefly  of  the 
abaxial  moiety  of  the  leaf,  and  this  is  also  indicated  by  the  mutual 
approximation  of  the  wings  along  the  edges  of  the  ventral  surface  (Mac- 
farlane).  The  finer  endings  of  the  vascular  tissue  often  but  not 
always  (Macfarlane)  abut  on  the  under  side  of  the  surface 
glands  found  on  the  interior  surface  of  the  pitcher  and  of  the  lid.  The 
fact  that  unopened  pitchers  which  have  been  removed  from  the  plant 
soon  lose  their  juice  (invariably  found  in  young  pitchers  before  open- 
ing) observed  by  de  Zeeuw  (1934)  seems  to  be  related  to  this  fact. 

Surface  anatomy.  —  By  this  we  mean  the  anatomy  of  the  epidermis, 
that  of  the  interior  surface  of  the  pitcher  being  of  primary  interest  to 
us.  Examination  of  the  interior  of  the  pitcher  {4  —  6)  will  show  that, 
with  some  exceptions  (A^.  ampullaria,  hicalcarata,  ventricosa,  inermis) 
there  is  a  broad  zone,  beginning  just  beneath  the  rim,  having  a  glau- 
cous, opalescent  appearance  caused  by  an  ample  waxy  secretion  with 
a  pebbly  surface.  The  epidermal  cells  here  are  simply  polygonal  with 
the  exception  of  a  large  number  of  slightly  projecting  lunate  ones,  so 
placed  that  their  concave  edges  are  turned  downwards  {8  —  5).  They 
have  the  appearance,  at  once  perceived,  of  half  stomata,  each  in  itself 
looking  like  a  guard  cell.  Oudemans  (1864)  thought  them  to  be  wax- 
secreting  glands.  WuNSCHMANN  would  have  none  of  this  (1872)  and 
pronounced  them  to  be  squat  hairs,  broader  than  long.  Dickson 
(1883)  was  the  first  to  arrive  at  the  correct  interpretation:  "I  have 
here  to  note  that  each  crescentic  ledge  consists  of  a  semilunar  cell 
which  overlaps  a  lower  and  smaller  one.  Occasionally  these  two  cells 
puzzlingly  resemble  deformed  stomata,"  he  wrote.  His  sometime 
associate  Macfarlane  confirmed  this,  as  did  Haberlandt,  independ- 
ently, and  later  Bobisut  (1910)  showed  that  they  are  completely  non- 
functional stomata,  having  no  pore,  though  Macfarlane  had  thought 
otherwise.  Macfarlane  thought,  too,  that  they  exude  water;  and 
Goebel  that  they  might  serve  for  gas  exchange  (1891),  neither  of 
which  can  be  true  in  the  absence  of  a  pore.  I  (19336)  have  confirmed 
Bobisut's  observations.  The  lunate  cell  is  one  guard  cell,  projecting 
somewhat  above  the  general  level  of  the  surface,  hiding  beneath  itself 
the  second  guard  cell  {8  —  6) ,  the  whole  having  been  rotated  on  the 
longer  axis.  The  whole  waxy  zone  is  a  "conductive"  (Hooker)  or 
slippery  surface  (Gleitzone,  Goebel)  on  which  insects  such  as  ants 
can  find  no  foothold. 

It  is  interesting  to  note  in  this  connection  that  Macbrlde,  in  181 7, 
made  the  suggestion  that  the  inabiUty  of  insects  to  cling  to  the  surface 
of  the  pitcher  of  Sarracenia  adunca  might  be  due  to  the  presence  of 
an  impalpable  powder,  or  to  the  breaking  away  of  fine  hairs.  To  this 
question  in  relation  to  Nepenthes  Knoll  (1914)  has  directed  some 
painstaking  experimentation. 


Chapter  IV  —  67  —  Nepenthes 

Knoll  found  that  if  he  placed  an  ant  on  a  cleaned  surface  of  an 
iris  leaf  {Iris  pallida),  the  waxy  secretion  thus  being  locally  removed, 
and  then  placed  the  leaf  in  a  vertical  position,  the  ant  could  not  get 
away  from  the  smooth,  clean  part.  It  seems  that  the  ant  clings  to 
smooth  surfaces  by  means  of  its  foot-pads,  not  by  its  claws,  since  there 
is  no  roughness  available.  It  cannot  cling  to  the  glaucous  surface  of 
the  Iris  leaf,  however,  because  the  waxy  secretion  is  loose  and  pulls  off, 
cumbering  the  foot-pads  so  that  the  ant  must  stop  to  clean  them  be- 
fore they  are  again  useful.  This  Knoll  proved  experimentally  by 
seeing  if  an  ant  can  walk  on  a  smooth  surface  as  of  glass  when  it  has 
been  coated  with  a  thin  layer  of  a  powder  such  as  talc  or  carbon  and 
found  that  it  cannot  do  so.  Since  the  ant  can  walk  on  clean  glass  or 
a  smooth  wax  surface  (beeswax  melted  onto  a  glass  plate)  it  is  quite 
evident  that  the  difficulty  for  the  ant  lies  in  the  particles  which  come 
off  on  his  pads  and  prevent  him  from  clinging.  Experiments  with  the 
loose  waxy  covering  of  the  iris  leaf  first  removing  it  and  then  applying 
it  again,  showed  the  same  result.  Coming  to  the  waxy  zone  of  most 
Nepenthes  pitchers,  Bobisut  had  already  experimented  and  believed 
to  have  found  that  ants  could  not  climb  the  surface  when  in  the  verti- 
cal position;  even  after  he  had  (as  he  thought)  removed  the  waxy 
surface.  Believing  that  he  had  failed  to  remove  the  waxy  covering 
perfectly,  Knoll  continued  his  experiments  in  the  same  sense  as  be- 
fore with  Iris,  etc.  He  removed  the  wax  thoroughly  with  chloroform, 
rubbing  downwards  to  avoid  breaking  the  lunate  cells  and  produced  a 
smooth  green  surface  showing  clearly  the  red  markings,  and  upon  this 
he  found  that  the  insects  could  climb  and  run  in  any  direction.  When 
now  he  scattered  talc  powder  or  wax  powder  obtained  from  the  pitchers 
themselves,  they  failed,  showing  that  their  ability  to  climb  on  the 
smooth  surface  was  due  to  the  absence  of  a  deterrent  to  the  use  of  their 
pads.  He  observed,  however,  that  ants  could  readily  negotiate  the 
gliding  zone  of  older  pitchers  in  greenhouses,  and  thought  that  this  is 
due  to  the  removal  of  the  wax  by  the  vigorous  sprinkling  with  water 
which  the  plants  usually  receive,  just  as  rain  is  known  to  remove  the 
waxy  covering  from  plants  like  Cotyledon,  etc.  Knoll's  observations 
on  the  walking  behavior  of  ants  and  the  effectiveness  of  the  waxy 
zone  as  a  precipitating  mechanism  have  been  repeated  by  my  friend 
Prof.  W.  KuppER  and  myself.  The  plant  was  a  vigorously  growing 
one  of  N.  gracillima  (aff.?),  one  which  is  evidently  very  attractive  to 
ants  as  they  are  always  to  be  seen  in  numbers  rapidly  walking  hither 
and  yon  especially  about  the  tops  of  the  pitchers.  We  observed  that 
they  persistently  visit  the  lid  and  the  rim.  They  run  no  risk  of  capture 
on  the  lid.  On  the  rim,  however,  it  is  supposed  that  they  do.  As  a 
matter  of  fact,  however,  they  do  not,  for  they  can  walk  on  it  in  any 
direction  with  rapidity,  and  they  frequently  stop  to  take  the  nectar 
from  the  marginal  glands.  They  even  passed  underneath  the  rim  and 
back  several  times  in  one  excursion  without  danger.  If,  however,  they 
venture  on  to  the  waxy  zone  they  at  once  display  a  quite  different 
behavior.  They  cannot  then  by  any  chance  move  rapidly  forward. 
If  they  progress  at  all,  it  is  very  slowly  and  with  much  groping  with 
the  legs  as  if  searching  for  a  hold.  Usually  this  ends  in  a  complete 
loss  of  foothold,  and  the  ant  falls  into  the  abyss.    One  pitcher  I  ex- 


Francis  E.  Lloyd  —  68  —  Carnivorous  Plants 

amined  held  a  collection  of  ants  which  must  have  run  into  the  thou- 
sands. With  regard  to  the  ability  of  flies  (houseflies  and  blue-bottles) 
to  retain  a  foothold  on  the  rim,  my  friend  Professor  A.  H.  Reginald 
BuLLER  repeatedly  observed  many  years  ago  that,  in  trying  to 
straddle  the  rim,  they  promptly  fell  into  the  pitcher,  in  N.  Master- 
si  ana. 

BoBisuT  further  thought  that  the  curious  deformed  stomata  could 
furnish  a  foothold  for  the  claws  of  the  ants,  etc.  but  Knoll  showed 
that  the  conformation,  position  and  size  of  the  ant's  claws  and  of  the 
apparently  available  points  for  grasping  with  claws  make  them  un- 
available. From  the  ant's  point  of  view  the  projecting  guard  cells 
should  have  been  turned  the  other  way.  Haberlandt  thought  that 
they  helped  an  insect  to  crawl  downward  but  not  upward,  since  they 
afforded  no  foothold  for  the  claws,  but  since  the  claws  are  not  used, 
but  the  pads  only  (Knoll),  and  since  ants  cannot  climb  downwards 
any  better  than  upwards  on  the  surface,  Knoll,  not  being  able  to 
avoid  the  impression  that  the  stomata  are  in  some  way  connected 
with  trapping  of  insects,  has  advanced  the  following  suggestion,  namely, 
that  the  numerous  projecting  guard  cells  serve,  when  the  waxy  surface 
has  more  or  less  been  removed  by  various  means  (rain,  much  traffic  of 
insects),  as  a  means  of  joggling  the  body  of  the  ant  by  the  slipping  of 
a  foot  over  them,  somewhat  as  when,  on  climbing  on  a  steep,  precarious 
rocky  surface,  a  hand  should  slip  from  its  hold  of  a  ledge  and  slap  the 
rock  surface  just  below.  "  Riitteleinrichtungen "  Knoll  calls  the 
projecting  half-moon  shaped  cells,  and  regards  them,  briefly,  as  an 
arrangement  for  hindering  the  climbing  of  the  walls  of  the  slipping 
zone  (Hooker's  conducting  zone).  It  must  be  remembered  that  an 
ant  uses  its  footpads  and  not  the  claws  in  trying  to  climb  a  smooth 
surface.  The  frequent  irregularities  in  form  of  the  surface  make  it  the 
more  perilous,  according  to  Knoll.  The  theory  is  ingenious  and  may 
very  well  represent  the  facts,  which  to  Knoll  are  such  in  view  of  his 
observations. 

Below  the  slide  or  conducting  zone,  when  present,  the  whole  of  the 
remaining  surface  constitutes  the  detentive  or  digestive  zone  {4  —  6) . 
It  is  a  glossy  green  or  red  (A^.  ventricosa)  in  color,  and  stands  out  in 
sharp  contrast  with  the  glaucous  color  of  the  waxy  zone  above.  The 
surface  is  richly  supplied  with  glands.  Each  gland  stands  in  a  slight 
depression,  the  upper  edge  of  which  projects  and  overhangs  the  gland  like 
an  eave,  sometimes  slightly,  more  often  covering  at  least  half  the  gland 
{8  —  10,  11),  or  in  the  case  of  N.  Pervillei  (7  —  14)  forming  a  deep  pit. 
In  the  depths  of  the  pitcher,  the  glands  often  become  more  or  less  ir- 
regular in  shape  and  are  devoid  of  any  overhang  (Macfarlane,  Stern). 

There  seems  to  be  every  reason  to  regard  these  glands  as  both  diges- 
tive (or  peptic  as  Macfarlane  called  them)  and  absorptive.  Their  ac- 
tivity becomes  evident  long  before  the  pitcher  reaches  its  maturity, 
young  unopened  pitchers  always  having  the  cavity  half-filled  with 
fluid.  Later  a  plentiful  additional  secretion  occurs  when  organic,  but 
not  so  plentiful  if  inorganic  materials  are  placed  in  the  pitcher 
(Hooker).  That  they  are  capable  of  reabsorbing  the  fluid  is  evident 
in  the  fact  that  in  a  rather  short  time  (24  hours  or  so)  the  fluid  may 
entirely  disappear  from  unopened  pitchers  (de  Zeeuw),  and  Goebel 


Chapter  IV  —  69  —  Nepenthes 

showed  that  nitrogen,  as  ammonia  and  peptone,  is  rapidly  reabsorbed 
(1891). 

Concerning  the  overhanging  eave-like  coverings  of  the  glands, 
Knoll  argued  that  they  serve  to  prevent  the  use  of  the  gland  for  foot- 
hold by  insects,  but  incidentally  prevent  also  damage  by  their  claws  to 
the  glands  themselves. 

Digestion.  —  The  students  of  digestion  in  Nepenthes  (as  in  other 
insectivorous  plants)  have  been  divided  into  two  camps  {a)  of  those 
who  argued  that  it  is  a  function  of  the  plant  itself  carried  out  by  the 
secretion  of  an  appropriate  enzyme  and  {b)  of  those  who  have  believed 
it  to  be  the  result  of  bacterial  action  (decay  or  rotting,  Dubois).  If 
the  latter  only  takes  place  (as  seems  to  be  true  in  Darlingtonia,  Hel- 
iamphora,  and  perhaps  some  spp.  of  Sarracenia)  this  fact  does  not 
disqualify  these  as  carnivorous;  bacterial  action  is  an  invariable  ac- 
companiment of  some  animal  digestion  {e.g.  of  cellulose  in  herbivores). 
Bacterial  action  is  often  unavoidable  in  open  pitchers  and  it  has  not  always 
been  possible  to  separate  the  different  digestive  processes.  Nepenthes 
offers  a  special  condition  in  that  the  pitchers  secrete  a  quantity  of  fluid 
before  they  open.  The  nature  of  this  fluid  was  investigated  by  Voel- 
KER  (1849).  He  described  it  as  hmpid  and  colorless,  with  a  slight 
agreeable  odor  and  taste,  and  containing  a  non-volatile  acid.  The 
total  solids  in  percentage  of  the  fluid  ranged  from  0.27  to  0.92  of 
which  63.94%  to  74.14%  was  non-volatile  substances.  Potassium, 
sodium,  magnesium,  calcium,  chlorine  (as  hydrochloric  acid)  and 
organic  acids  were  found,  chiefly  malic,  with  a  little  citric.  Tait 
found  that  pitcher  fluid  from  unopened  pitchers  was  sometimes  acid, 
but  frequently  not.  When  flies  had  found  their  way  into  open  pitchers 
the  fluid  became  much  more  acid  as  well  as  more  viscid.  According 
to  VON  GoRUP  and  Will  (1876)  the  fluid  is  colorless,  clear  or  slightly 
opalescent,  odorless,  tasteless  and  of  various  consistency.  After  stimu- 
lation the  fluid  changes  from  being  neutral  or  only  slightly  acid,  to 
decidedly  acid.  "Miss  R.  Bok  found  that  carefully  washed  beakers 
of  Nepenthes  filled  with  distilled  water  did  not  show  any  acid  pro- 
duction while  the  addition  of  2o/mgr./liter  NH4CI  would  cause  prompt 
acid  production.  The  pH  went  down  to  about  3.0  in  24  hours". 
(Baas  Becking,  in  ep.). 

It  is  an  important  and  well  attested  fact  that  the  fluid  of  unopened 
pitchers  is  above  all  free  of  bacteria,  owing  in  part  to  the  tight  sealing 
around  the  edge  of  the  lid  by  interwoven  branching  hairs,  a  precursor 
in  Nature  of  the  cotton  plug  used  in  bacteriological  technique. 

The  pioneer  work,  constituting  a  prime  stimulus  to  the  investiga- 
tion of  digestion  in  carnivorous  plants,  was  done  by  J.  D.  Hooker, 
announced  in  his  address  before  the  Biological  Section  of  the  British 
Association  for  the  Advancement  of  Science  in  August  1874.  Hooker 
was  in  touch  with  Charles  Darwin,  and  his  interest  was  a  natural 
outcome  of  this  contact;  for  Darwin  was  finishing  his  book  on  car- 
nivorous plants  at  the  time.  Hooker  found  that  bits  of  egg-white, 
meat,  fibrin  and  cartilage,  when  placed  in  the  pitchers,  showed  un- 
mistakable evidence  in  24  hours  of  disintegration,  but  that  this  action 
was  by  no  means  so  pronounced  in  fluid  placed  in  test  tubes.  From 
this  Hooker  inferred  that  the  digestion  depends  not  on  the  first  fluid 


Francis  E.  Lloyd        —70— Carnivorous  Plants 

secreted  by  the  glands,  but  that  there  is  a  direct  response  to  the 
presence  of  the  material  to  be  digested.  He  saw  evidence  also  of 
antiseptic  action  in  that  odor  was  not  developed  so  rapidly  in  the 
pitcher  fluid  as  in  water.    His  general  conclusion  may  be  stated  in  his 

own  words:  " it  would  appear  probable  that  a  substance  acting 

as  a  pepsine  does  is  given  off  from  the  inner  wall  of  the  pitcher,  but 

chiefly  after  placing  the  animal  matter  in  the  acid  fluid; "    In 

the  following  year  (1875)  Lawson  Tate  announced  that  he  had  suc- 
ceeded in  separating  a  substance  "closely  resembling  pepsin"  from 
the  secretion  of  Drosera  dichotoma  and  a  little  later  he  obtained  a  sim- 
ilar substance  from  the  fluid  taken  from  the  pitchers  of  several  species 
of  Nepenthes,  but  did  not  subject  these  extracts  to  the  appropriate 
tests.  The  preparations  seem  to  have  been  glycerin  extracts,  in  which 
both  were  soluble.  At  the  same  time  Rees  and  Will  of  Erlangen 
(1875)  made  preparations  of  Drosera,  drying  the  leaves  with  absolute 
alcohol  and  extracting  the  ground  material  with  glycerin.  Such  ex- 
tracts, but  only  when  slightly  acidified  with  HCl  (.2%),  caused  the 
disappearance  of  swollen  fibrin  at  40  degrees  in  18  hours,  peptones 
being  produced,  thus  confirming  the  work  of  Darwin  on  Drosera.  At 
about  the  same  time  von  Gorup-Besanez  (1874)  studied  the  fluid  of 
Nepenthes  pitchers,  and  found  that  when  he  subjected  shreds  of  fibrin 
to  the  naturally  acid  secretion,  they  were  nearly  digested  in  an  hour  at 
40  degrees,  peptones  then  being  present.  Additional  acid  as  above 
accelerated  the  action. 

Von  Gorup  and  Will  (1876)  investigated  further.  They  compared 
the  behavior  of  the  fluid  from  stimulated  pitchers  (to  which  insects 
had  had  access)  with  that  from  unstimulated  pitchers.  The  former 
was  filtered  and  tested  with  acidulated  fibrin,  raw  meat,  coagulated 
egg-white,  legumin  and  gelatin,  obtaining  positive  evidence  in  all  cases 
with  the  Biuret  reaction,  the  gelatin  excepted.  This  yielded  a  non- 
jelHng  gelatin-peptone.  The  fluid  of  unstimulated  pitchers  was  found 
to  fail  to  act  unless  acidified,  but  responded  in  the  presence  of  HCl, 
formic,  malic,  citric,  acetic  and  propionic  acids.  The  efficiency  of  these 
was  various,  formic  acid  being  very  active  ("fast  momentan"),  followed 
by  malic,  citric,  acetic  and  propionic  in  the  order  named.  The  length 
of  time  in  which  positive  results  were  obtained,  as  indicated  by  the 
Biuret  reaction,  varied  from  10  minutes  to  three  hours  or  more  accord- 
ing to  the  activity  of  the  acid  and  the  temperature. 

Vines  was  busy  at  the  same  time.  Following  the  method  of  Rees 
and  Will,  he  (1877)  alcohol-dried  pitcher  walls  bearing  the  glands  of 
Nepenthes  and  ground  and  extracted  them  with  glycerin.  In  testing 
his  extracts  he  used  the  following  method.  In  each  of  three  test  tubes 
he  placed  (i)  extract  acidified;  (2)  extract  only  and  (3)  acid  only,  and 
added  a  bit  of  swollen  fibrin  and  kept  the  tubes  at  40  degrees.  Only 
the  first  of  the  preparations  gave  a  positive  result  and  a  peptone  reac- 
tion could  be  detected;  the  other  two  were  negative.  Vines  noticed 
that  the  pitcher  fluid  in  von  Gorup-Besanez'  experiments  appeared  to 
be  more  active  than  his  own  extracts.  Following  the  lead  of  Ebstein 
and  Gruetzner  and  of  Haidenhain  (through  Vlnes),  who  had  ob- 
tained more  active  extracts  of  animal  glands  by  previous  treat- 
ment with  acid.  Vines  then  treated  the  pitcher  wafls  bearing  glands 


Chapter  IV  —  71  —  Nepenthes 

with  1%  acetic  acid  for  24  hours,  before  extracting  with  glycerin,  and 
found  that  this  extract  was  more  powerful  than  that  of  the  control 
prepared  without  previous  acid  treatment.  This  indicated  that,  as  in 
the  case  of  animal  glands  (Haidenhain)  ,  the  ferment  exists  in  the 
glands  as  a  zymogen,  a  basic  substance  from  which  the  ferment  is 
derived  by  acidification.  The  facts  seemed  to  bring  the  whole  phe- 
nomenon of  plant  digestion  into  line  with  that  in  animals.  This  was 
the  beginning  of  a  sustained  investigation  on  the  part  of  Vines  on  this 
subject.  Dubois  and  Tischutkin  held  that  there  is  no  digestion 
proper  to  the  Nepenthes  pitcher,  and  that  such  digestion  as  takes  place 
is  bacterial.  Goebel's  examination  of  the  matter,  however,  afforded 
experimental  evidence  in  agreement  with  that  of  Vines  (1877),  who 
now,  however,  repeated  and  extended  his  earlier  work  and  drew  the 
conclusion  that  settled  the  matter  to  all  appearances.  For  instance, 
he  showed  that  digestion  goes  on  in  the  fluid  of  (unopened)  pitchers 
in  the  presence  of  poisons  deadly  to  bacteria  (HCN,  thymol,  KCN, 
chloroform);  but  as  opened  pitchers  were  used  the  possibility  is  not 
excluded  that  a  bacterial  ferment  had  already  accumulated.  Vines 
concluded  that  the  ferment  present  in  the  pitchers  is  secreted  by  the 
pitcher  glands,  is  not  a  product  of  bacteria,  but  is  tryptic  in  na- 
ture, like  that  of  certain  seeds  (Green  1899)  not  producing  pep- 
tones, or  if  it  does,  these  are  broken  down  at  once  into  other  bodies 
(leucine,  etc.).  It  is  remarkably  stable  and  has  an  antiseptic  action. 
The  pitcher  liquid  is  usually  distinctly  acid,  contrary  to  the  prevaihng 
views,  the  acidity  therefore  not  depending  on  the  supposed  stimula- 
tion by  foreign  bodies.  In  his  third  paper  (1898)  Vines  showed  more 
in  detail  that  the  enzyme  is  unusually  stable  towards  heat  and  alkalis, 
for  while  exposure  to  these  agencies  does  reduce  its  activity,  "it  re- 
tains a  sort  of  residual  digestive  power  which  asserts  itself  in  a  very 
slow  and  prolonged  digestion,  and  which  can  only  be  destroyed  by 
very  strong  measures."  The  enzyme  exists  in  the  tissues  as  a  zymo- 
gen, is  essentially  tryptic  in  character,  and  among  its  products  of  di- 
gestion true  peptones  are  present.  In  his  last  paper  published  in  1901, 
Vines  proposed  the  name  "nepenthin"  for  the  proteolytic  ferment 
which  he  had  previously  studied  and  made  further  tests  of  the  action 
of  the  pitcher  fluid  on  fibrin  and  on  Witte  peptone,  exposing  them  to 
action  for  several  days  at  38.5  degrees  C.  with  the  addition  of  HCl 
or  citric  acid.  The  results  showed  the  presence  of  tryptophane,  char- 
acteristic of  tryptic  digestion. 

The  detail  of  Vines'  general  conclusions,  that  the  digestion  is 
rather  of  the  tryptic  kind,  was  later  called  in  question  by  Abderhalden 
and  Teruuchi  (1906).  From  data  obtained  by  experiments  in  which 
glycyl-1-tyrosin  was  used,  which  gave  negative  results,  they  concluded 
that  the  Nepenthes  protease  is  not  a  trypsin,  though  they  did  not  as- 
sert certainty  in  view  of  the  lack  of  sufficient  material  for  further  work 
{See  Stern  and  Stern,  beyond). 

Quite  opposite  conclusions  were  drawn  by  Tischutkin  (1891), 
Dubois  (1890)  and  Couvreur  (1900).  Tischutkin  placed  small  cubes 
of  egg-albumin  in  unopened  pitchers  by  passing  them  through  a  small 
window  cut  in  the  wall  under  sterile  conditions,  and  saw  no  digestion. 
When  the  test  material  was  placed  in  pitcher  fluid  in  vitro,  digestion 


Francis  E.  Lloyd —12— Carnivorous  Plants 

occurred   after   some   days   during   which   bacteria   had   accumulated. 
Dubois  (1890)  found  the  sterile  fluid  from  unopened  pitchers  without 
action,  but  that  from  recently  opened  pitchers,  while  still  clear,  acted 
vigorously  on   egg-albumin.     Dubois   voted   for   the   bacterial   action 
theory.     Couvreur  (1900)  argued  that  Vines'  results  were  due  to  the 
interaction   of   the  reagents   on   one   another.     This   totally   negative 
attitude  had  been  combatted  by  Goebel  (1893).     In  a  prehminary  ex- 
periment, he  took  a  pitcher  of  A^.  paradisiaca  (a  hybrid)  which  contains 
a  "clear,  odorless  and  tasteless  fluid"  and  in  it  placed  a  bit  of  flbrin, 
with  one  in  water  as  control.     In  six  days  the  fibrin  was  broken  up 
and  bacteria  were  plentiful,  and  the  fluid  showed  a  neutral  or  sHghtly 
alkaline  reaction.    A  yellow  reaction  was  obtained  in  the  water  but  not 
in  the  pitcher,  by  which  the  products  had  been  resorbed.    No  peptone 
had    been    produced.      Cultures    showed    the    presence    of    Bacterium 
fiiiorescens  liquejaciens.     This  result  admittedly  agreed  with  those  of 
Dubois  and  Tischutkin.    But  Goebel  pointed  out  that  the  plant  was 
not  normal.    When  he  took  a  strong,  wefl  grown  plant  he  found  other- 
wise.   It  had  three  pitchers,  an  old  one,  a  strong  vigorous  one  and  an 
unopened  one.    In  the  old  one,  a  wasp  was  attacked  and  digested.    In 
three  days  the  fluid  was  alkaline  and  bacteria  and  infusoria  were  plenti- 
ful.   In  the  open  but  vigorous  pitcher  a  fly  had  been  caught.    A  bit  of 
fibrin  was  introduced  and  was  attacked  in  one  hour.    In  3  hours  pep- 
tone was  demonstrable.    Another  bit  of  fibrin  together  with  0.2%  HCl 
were  introduced,  and  this  was  digested  in  40  minutes,  and  no  bacteria 
could  be  found.     The  fluid  of  the  unopened  pitcher  was  neutral.     In 
its  fluid  fibrin  accompanied  by   1%  formic  acid  was  digested  in   12 
hours,   and  no  bacteria  were   detected  after  8   days.     He   concluded 
therefore  that  a  peptone   forming  ferment  was  present  in   the   fully 
normal  pitchers.    He  further  showed  that  normal  pitchers,  when  stim- 
ulated by  the  presence  of  an  insect,  secrete  formic  acid.     By  way  of 
further  control  he  tried  to  see  if  fibrin  might  be  digested  by  the  secre- 
tions of  the  lid,  with  negative  results.    To  do  this  he  fastened  a  bit  of 
fibrin  on  the  under  side  of  the  lid  with   moist   filter  paper.     Thus 
Goebel  confirmed  Vines'  conclusions.     In  general  support  of  the  view 
that  the  bacteria  of  decay  have  nothing  to  do  with  the  digestion  of 
insects   in    normal    plants   in    their    native    habitats    Goebel    quoted 
Wallace  who  wrote  in  The  Malay  Archipelago  as  foflows:   "We  had 
been  told  that  we  should  find  water  at  Padangbatu,  but  we  looked  for 
it  in  vain,  as  we  were  exceedingly  thirsty.     At  last  we  turned  to  the 
pitcher  plants,  but  the  water  contained  in  the  pitchers  (about  half  a 
pint  in  each)  was  full  of  insects  and  otherwise  uninviting.     On  tasting 
it,  however,  we  found  it  very  palatable,  though  rather  warm,  and  we 
all  quenched  our  thirst  from  these  natural  jugs."     And  stiU  earlier 
Hermann  Nicolaus  Grimm  recorded  (in  1682)  the  discovery  of  "aqua 
dulcis,  limpida,  amabihs,  confortans  et  frigida"  in  the  pitchers,  and  the 
fluid  from  six  to  eight  of  them  was  sufficient  to  satisfy  a  thirsty  person. 
That  our  greenhouse  cultivated  plants,  because  of  their  compara- 
tively feeble  vitality  as  compared  with  plants  in  their  native  habitats, 
may    often    behave    abnormally,   is  indicated   by    the    observation    of 
MoHNiKE,  whom  Goebel  cites,  who  said  that  the  pitcher  almost  al- 
ways contains  a  mass  of  dead  insects  including  even   large   beetles. 


Chapter  IV —73— Nepenthes 

The  larvae  of  Apogonia  spherica  were  found  entire  but  quite  digested 
internally.  Insects  die  in  the  pitcher  fluid  much  more  quickly  than  in 
distilled  water.  In  48  hours  or  so,  insects  are  disintegrated,  only  their 
chitinous  skeletons  remaining.  Such  statements,  encountered  in  other 
writings,  indicate  a  very  vigorous  action.  Goebel  ventured  the  state- 
ment that  of  all  the  pitchered  carnivorous  plants  Nepenthes  is  the  most 
vigorous  in  these  matters. 

Clautriau  (i  899-1 900)  took  the  opportunity  of  studying  Nepen- 
thes in  its  habitat  in  Java.  His  results  fully  corroborate  in  general 
Goebel  and  Vines.    He  observes: 

While  the  fluid  in  unstimulated  pitchers  is  neutral,  it  becomes  acid 
on  the  introduction  of  foreign  bodies.  Even  shaking  has  this  effect, 
the  strongest  acidity  obtained  being  equal  to  that  of  a  Uter  of  water 
acidified  with  2  cc.  of  fuming  HCl.  In  the  fluid  there  is  a  thermolabile 
substance  which  acts  as  a  wetting  agent,  so  that  insects  are  quickly 
drowned  but  are  not  killed  by  any  poison.  Insects  are  digested  with- 
out any  putrefaction.  Antiseptics  such  as  formaldehyde,  chloroform, 
etc.  inhibit  both  the  secretion  of  acid  and  digestion,  and  the  pitchers 
presently  die.  On  the  introduction  of  egg-white,  both  digestion  and 
absorption  occurred.  If  a  small  quantity  was  used  absorption  equalled 
digestion  in  rate;  if  a  too  large  quantity  was  used,  the  products  re- 
mained in  quantity  sufficient  to  afford  a  culture  medium  for  bacteria. 
Quantitative  experiments  showed  that  5  cc.  of  egg-white  (10  cc.  to  90 
cc.  water)  is  completely  digested  in  vigorous  pitchers  in  2  days.  If  a 
pitcher  were  separated  from  the  plant,  digestion  was  inhibited,  and 
Clautriau  usually  found  that  in  vitro  experiments  gave  negative  re- 
sults. At  home  in  Brussels  he  showed  by  refined  methods  that  al- 
bumin is  completely  digested  to  peptone.  This  is  readily  absorbed  by 
the  pitcher  walls,  so  that  he  was  able  to  give  successive  doses  of  food 
(albumin)  and  see  that  they  were  digested  perfectly  by  the  pitchers  of 
N.  M aster siana. 

Clautriau  concluded  that  the  enzyme  is  a  true  pepsin  as  it  acts 
only  in  an  acid  medium  and  produces  true  peptone  as  an  end  result. 
No  other  products  could  be  found.  No  amylase  was  detected.  The 
evidence  indicated  that  an  ample  secretion  of  both  enzyme  and  acids 
required  stimulation,  and,  on  microchemical  evidence,  that  peptone  is 
absorbed  by  the  glands  and  stored  as  protein.  A  superabundance  of 
food  may  allow  the  play  of  bacteria,  and  the  products  of  their  activity 
(amino  acids  and  ammonia)  may  be  used  by  the  plant.  These  do  not 
necessarily  damage  the  pitcher  itself. 

Fenner  has  (1904)  advanced  an  interesting  presentation  of  what 
he  believes  goes  on  in  natural  conditions.  The  original  pitcher  fluid  is 
slightly  acid  (formic  acid,  Goebel).  If  a  few  gnats  are  introduced, 
they  float  on  top  of  the  fluid.  If  alive  they  endeavor  to  escape  by 
cKmbing  up  the  wall,  and  in  this  way  they  come  in  contact  with  the 
glands  below  their  overhanging  eaves,  which,  Haberlandt  has  sug- 
gested, serve  the  purpose  of  retaining  fluid  by  capillarity.  ^  The  body 
of  an  insect  wet  with  pitcher  fluid  thus  applied  serves  to  stimulate  the 
glands  to  action,  when  they  secrete  a  highly  viscid,  active  fluid  which 
attacks  the  insect  so  vigorously  that  it  is  digested  in  5-8  hours. 
Tenner  tested  this  view  experimentally  by  taking  an  opened  pitcher 


Francis  E.  Lloyd —74— Carnivorous  Plants 

and  placing  an  insect  (a  gnat)  on  an  area  of  the  wall  which  had  been 
dried.  A  slight  amount  of  secretion  then  occurs  which  is  insufficient  to 
act  and  readtly  dries  up.  But  if  an  insect  wet  with  pitcher  fluid  is  used, 
an  ample  secretion  from  the  gland  ensues  and  the  insect  is  digested  in 
the  time  indicated  above.  It  would  appear  according  to  Fenner's  in- 
terpretation that  the  pitcher  fluid  acts  as  a  stimulant  to  secretion.  In 
this  way  the  body  of  a  smaU  insect  comes  into  contact  with  a  more 
vigorous  secretion.  The  greater  activity,  therefore,  is  not  within  the 
depths  of  the  pitcher  fluid  but  in  the  films  of  fluid  by  which  the  bodies 
of  the  insect  adhere  to  the  glands.  Into  this  position  they  come  nat- 
urally enough  since  they  float  towards  the  walls,  and  the  fluid  level, 
by  shaking  (as  by  the  wind),  is  moved  so  that  insects  stick  on  the 

walls  above  it. 

The  collection  of  Nepenthes  accumulated  at  the  University  of 
Pennsylvania  by  Professor  Macfarlane,  furnished  an  abundant  amount 
of  material  for  the  study  of  proteolysis  by  Hepburn  (191 9),  who  car- 
ried out  his  experiments  with  unopened  pitchers,  and  opened  pitchers 
from  which  insects  were  excluded  by  means  of  cotton  wool  plugs.  Some 
of  these  were  stimulated  by  the  introduction  of  glass  beads  after  shak- 
ing. A  distinction  between  "stimulated"  and  "unstimulated"  pitchers 
became  evident:  Their  fluid  was  found  to  differ  in  its  activity.  Bac- 
teria were  carefully  excluded  by  means  of  active  bactericides,  and  all 
experiments  were  controlled.  With  various  substrates  (ovalbumin, 
fibrin,  ovomucoid,  Heyden's  nutrient  and  Witte  peptone)  and  by 
means  of  formol  titration  (Sorensen)  he  found  that  the  fluid  from 
stimulated  pitchers  digested  all  of  them;  but  not  that  of  unstimulated. 
In  the  presence  of  very  dilute  HCl  edestin  was  also  acted  upon  by 
fluid  of  stimulated  but  not  by  that  of  unstimulated  pitchers.  Carmine 
fibrin  in  the  presence  of  acid  was  digested  by  both,  but  not  by  that  of 
unstimulated  pitchers  in  the  absence  of  acid.  Protean  (from  the  globu- 
lin of  the  seed  of  castor  bean,  Ricinus  communis)  and  ricin  were 
attacked  by  the  fluid  of  both  stimulated  and  unstimulated  pitchers  if 
in  the  presence  of  very  dilute  acid.  With  sufficiently  long  exposure, 
glycyltryptophane  was  "apparently"  hydrolysed  by  the  fluid  of 
stimulated  pitchers.  It  appeared  that  the  fluid  of  stimulated  pitchers 
possessed  proteolytic  power  in  the  absence  of  acid  (as  weU  as  with 
acid)  while  that  of  unstimulated  pitchers  always  required  the  ad- 
dition of  acid.  It  is  not  clear  how  the  stimulation  acts:  whether  by  a 
change  of  acidity  creating  a  favorable  medium  for  an  enzyme  already 
present,  or  by  the  activation  of  a  zymogen  already  present  or  by  an 
increase  in  the  secretion  of  the  protease  of  the  glands. 

In  1932  Stern  and  Stern  reopened  the  question.  They  chose  a 
series  of  substrates  (gelatin,  casein,  edestin,  ovalbumin  and  serum 
protein),  and  tested  the  effect  of  the  pitcher  secretion  on  them  through- 
out the  whole  physiological  range  of  pH,  and  found  that  they  obtained 
two  maxima,  one  at  pH  4.7  and  7.0  for  gelatin,  pH  3  and  8  for  edes- 
tin, pH  4  and  8  for  ovalbumin.  Serum  protein  was  not  measurably 
attacked  between  pH  1.5  and  8.4.  The  behavior  of  casein  is  anoma- 
lous. The  curve  shows  two  maxima,  at  pH  3  and  5.5,  with  a  deep  dip 
between,  due  probably  to  the  flocking  of  the  protein  at  the  isoelectric 
point  and  the  binding  of  the  enzyme.     The  tryptic  optimum  was  not 


Chapter  IV —75— Nepenthes 

evident,  due  possibly  to  the  inhibiting  effect  of  the  glycerine  present. 
These  results  were  obtained  on  pitcher  secretion  preserved  with  50% 
glycerine,  from  N.  Hibherdii  and  N.  mixta.  The  secretion  from  open 
pitchers  containing  insects,  mostly  ants,  was  used.  In  order  to  exclude 
the  effect  of  microbes  and  the  enzymes  of  insect  bodies,  the  authors 
also  took  the  glandular  walls,  comminuted  and  extracted  them  with  acetic- 
glycerine.  The  extract  they  found  active  on  gelatine  at  pH  8,  and  on 
ovalbumin  only  in  the  region  of  pH  3-3.5,  thus  supplying  evidence  that 
a  tryptic  ferment  is  secreted  by  the  glands  of  the  Nepenthes  pitcher. 
In  order  to  compare  the  enzymes  of  Nepenthes  with  those  of  animals 
they  made  tests  of  the  effect  on  them  of  certain  activators,  known  to 
affect  other  proteinases,  \\ath  negative  results.  Neither  HCN,  H2S  or 
cystein  have  any  effect  on  the  proteinase,  nor  does  enterokinase  on  the 
tryptase;  the  latter  Stern  had  shown  for  the  proteinase  of  white 
blood  cells. 

The  conclusions  of  Stern  and  Stern,  that  there  are  two  enzymes 
present,  a  catheptic  and  a  tryptic,  and  that  the  latter  is  not  attribut- 
able to  the  presence  of  bacteria,  led  W.  de  Kramer  (1932)  in  Baas 
Becking's  laboratory  at  Leiden  to  re-examine  the  question.  He  came 
to  the  conclusion  that  the  opinion  that  the  tryptic  action  is  due  to 
bacteria  is  justified.  De  Zeeuw,  who  quotes  de  Kramer's  unpubhshed 
results,  attacked  this  question.  Both  catheptic  and  tr>T>tic  action  was 
found  by  them.  De  Zeeuw  experimented  with  unopened  pitchers 
which  were  allowed  to  open  under  sterile  conditions,  using  bromine 
water  and  sterile  cotton  for  insurance  against  bacterial  infection,  and 
with  unopened  ones,  which  were  always  found  sterile. 

The  fluid  of  unopened  pitchers  does  not  digest  fibrin  until  an  acid 
is  added,  an  enzyme  is  therefore  present.  It  becomes  active  within 
the  pH  range  of  3.4  to  4.4,  phosphoric,  malic  and  citric  acid  having 
been  used,  and  a  phosphate  buffer.  That  from  an  aseptically  opened 
pitcher  acted  at  pH  3.6  in  phosphoric  acid,  while  that  from  normally 
opened  pitchers  was  active  at  pH  3.2  with  phosphoric  acid  and  from 
7.2  and  8.6  with  phosphate  buffer.  The  last  named  was  not  sterile. 
Bacterium  fluorescens  liquefaciens,  B.  prodigiosum  and  two  others  were 
present,  and  all  of  these  were  found  to  exert  tryptic  action.  By  way  of 
control  the  fluid  of  a  pitcher,  opened  under  sterile  conditions,  of 
N.  Morganiana,  was  tested  and  found  to  digest  fibrin  at  pH  4.4  to  5.5, 
the  pH  increasing  steadily  during  15  days.  An  acetic  acid-glycerine 
extract  was  found  to  digest  fibrin  at  pH  2.3  to  4.2,  in  direct  contra- 
diction to  the  results  of  Stern  and  Stern  (1932)  who  also  believed 
their  extract  to  be  bacteria-free. 

Open  pitchers  display  a  wide  range  of  pH  (3.0-7.2),  S3%  reacting 
neutral  or  basic,  36  pitchers  being  examined.  When  completely  di- 
gested insect  cadavers  were  present,  the  fluid  was  neutral  or  weakly 
basic;  when  digestion  was  in  its  early  stages,  acid.  Into  a  pitcher 
which  showed  an  acid  reaction  (pH  3.0)  the  acid  was  neutralized  by 
means  of  hme  water,  and  a  pH  of  8.2  established.  Since  digestion  was 
proceeding,  the  next  morning  the  fluid  was  found  to  be  at  pH  3.0  again. 
Pitchers  after  being  washed  out  thoroughly  with  distilled  water  were 
then  supplied  with  distilled  water  (pH  7).  When  fibrin  was  added,  the 
pH  dropped  to  3.5,  as  also  when  egg-albumin  (such  as  used  by  Clautriau) 


Francis  E.  Lloyd —76— Carnivorous  Plants 

was  used.  This  is  interpreted  as  demonstrating  that  the  addition  of  a 
protein  to  the  fluid  stimulates  the  secretion  of  acid;  but  de  Zeeuw  was 
unable  to  bring  this  about  by  mechanical  stimulation,  the  contrary 
having  been  reported  by  Hepburn  {see  above).  The  secretion  of  un- 
opened pitchers  had  been  found  by  de  Kramer  to  be  always  neutral, 
and  this  was  re-examined  by  de  Zeeuw  who  found  the  pH  ranging 
from  4.2  to  7  (ave.  6.6  ±  1.2)  in  October  and  from  4.2  to  4.8  (ave. 
4.5  +  0.3)  in  November  and  December,  a  difference  possibly  attribut- 
able to  the  time  of  year,  with  a  lower  temperature  prevailing  (in  the 
greenhouse?).  The  fluid  of  pitchers  opened  under  sterile  conditions, 
therefore  without  chemical  stimulation,  always  reacted  acid  (pH  4.2  to 
5.8)  but  required  additional  acid  to  secure  digestion.  When  acidified  to 
pH  3.0  to  3.5  with  certain  acids  (phosphoric,  HCl,  formic,  malic, 
and  succinic  acid),  and  kept  sterile  with  toluene,  digestion  proceeded, 
but  not  with  the  others  tried,  which  probably  destroyed  the  enzyme. 
What  kind  of  acid  is  secreted  by  the  pitcher,  aside  from  the  fact  that  it 
is  not  a  volatile  one,  was  not  determined.  But  the  acid  reaction  of  the 
glands  indicated  that  these  are  responsible.  De  Zeeuw  therefore 
reached  the  conclusion  that  the  enzymes  present  are  catheptic  and 
tryptic,  but  that  the  former  only  is  present  in  sterile  pitcher  fluid,  the 
latter  occurring  only  in  opened  pitchers  to  which  bacteria  had  had 
access.  Acid  is  secreted  by  the  gland  when  stimulated  by  chemical 
but  not  by  mechanical  means. 

As  the  matter  stands  at  the  present,  therefore,  the  positive  evidence 
that  a  catheptic  proteinase  is  secreted  by  the  pitchers  of  Nepenthes  is 
conclusive.  That  tryptic  digestion  in  the  absence  of  bacteria  takes 
place  there  seems  little  doubt,  but  this  cannot  yet  be  said  to  be  com- 
pletely proven. 

Antisepsis  of  pitcher  fluid.  —  Reference  has  been  made  to  the  fact, 
usually  accepted  as  such,  that  the  pitcher  fluid  of  normal  actively  di- 
gesting pitchers  is  free  of  bacterial  action.    Wallace  has  already  been 
quoted  as  testifying  to  this  in  the  natural  habitat  in  Borneo.     Goebel 
atributed  this,  in  the  experiments  he  conducted,  to  the  presence  of  for- 
mic acid  secreted  by  the  pitcher  glands.     Robinson  (1908)  observed 
that  meat  extract  might  remain  in  the  pitchers  of  N.  destillatoria  for 
two  weeks  without  the  odor  of  foulness.    Although  they  confirmed  the 
generally  accepted  belief  that  the  fluid  of  unopened  pitchers  is  sterile, 
Hepburn   et   al.    (1919,    1927)    found   that    opened    pitchers,    whether 
containing  insects  or  not,  invariably  contained  bacteria  in  large  num- 
bers, whose  activity  in  digesting  proteins  they  found  was  low,  and  that 
they  play  only  a  secondary  role  in  the  digestion  of  insects,  the  leading 
role  being  played  by  the  protease  proper  to  the  pitcher  itself.     They 
argued  that  the  bacteria  five  in  symbiosis  with  the  plant,  assisting  some- 
what in  the  digestion  of  insects,  thereby  drawing  nutrition  therefrom. 
Since  the  plants  they  experimented  with  were  under  cultivation,  the 
argument   that   their   results   do   not   reflect   the   conditions   found   in 
nature,  as  indicated  by  such  experiences  as  Wallace,  seems  justified. 
Testimony  is,  however,  not  uniform  on  this  point.    Jensen  (1910)  speaks 
twice  of  the  horrible  stench  arising  from  pitchers  loaded  with  centi- 
pedes, cockroaches,  butterflies  and  a  huge  scorpion  found  in  pitchers 
near  Tjibodas,  Java.     This  may  mean  merely  that  the  pitchers  were 


Chapter  IV  —  77  —  Nepenthes 

overloaded  beyond  the  limits  at  which  the  antiseptic  effect  could  be 
expected  to  work.  On  the  basis  of  experiments,  Jensen  regards  it  as 
sure  that  certain  larvae  which  live  on  the  debris  in  pitchers  have  an 
antiferment  which  is  not  possessed  by  the  same  kind  of  larvae  when 
inhabiting  water  in  pools. 

Under  the  title,  ''The  animal  world  of  Nepenthes  pitchers",  August 
Thienemann  (1932)  brought  together  all  that  at  the  time  of  publi- 
cation was  known  about  the  fauna  to  be  found  in  the  pitchers  of 
Nepenthes.  Long  ago,  as  early  as  1747,  G.  E.  Rumphius,  the  renowned 
explorer,  remarked  in  his  Herbarium  Aniboinense   (pt.    5,   p.    122):  — 

"In  aperto  varii  repunt  vermicuK  et  insecta,  quae  in  hoc  moriuntur, 
excepta  parva  quadam  squilla  gibba,  quae  aliquando  in  hoc  reperitur 

et  vivit "     Since  that  time  innumerable  observations  have  been 

made  and  it  would  scarcely  be  profitable  to  detail  them. 

The  first  question  which  will  occur  to  one  interested  in  this  fact  is 
one  which  Jensen  (1910)  asked,  namely,  how  can  animals  live  in  the 
digestive  fluids  of  the  pitchers.  In  answer  he  said  that  he  beheved 
there  was  indicated  the  presence  of  an  antipepsin  formed  by  the 
animals  in  question.  Dover  (1928)  agreed  with  him,  but  did  not  go  so 
far  as  to  assert  the  presence  of  an  antipepsin,  though  he  beheved  that 
mosquito  larvae  do  possess  such,  and  suggested  that  the  "presence  of 
neutral  salts  in  the  tissues  of  the  larvae  might  possibly  retard  peptic 
digestion;"  Thienemann,  however,  maintained  that  there  is  no  bind- 
ing evidence  that  there  is  an  antipepsin  and  goes  further  in  saying  that 
he  sees  no  special  problem  to  be  involved.  The  numerous  internal 
parasites  of  the  animal  body  hve  in  body  fluids  rich  in  ferments. 
Dover,  himself,  observed  that  the  larvae  of  Megarhinus  acaudatus  can 
remain  alive  in  a  very  weak  iodine  and  in  a  strong  pepsin  solution  and 
in  the  latter  Kved  some  days,  pupated  and  hatched  out.  Are  we  then 
to  expect  if  an  antipepsin  is  present  that  there  is  also  an  antiiodine? 
We  may  recall  here  that  Hepburn  and  Jones  (191 9)  believe  that  they 
demonstrated  the  presence  of  antiproteases  in  the  larvae  of  Sarcophaga 
which  inhabit   the  pitchers  of  Sarracenia  flava. 

The  inhabitants  of  the  pitchers  are  divided  by  Thienemann  into 
three  classes,  (a)  those  which  are  occasionally  found,  but  which  belong 
properly  in  other  places  (nepenthexene) ;  {h)  those  which  occur,  find  in 
the  pitcher  suitable  conditions  and  can  pass  their  watery  fives  there 
but  which  are  not  confined  to  them  (nepenthephile)  and  thirdly  those 
which  five  only  in  the  pitchers  and  are  not  found  elsewhere  (nepen- 
thebionts).  Since  the  pitchers  are  commonly  only  partly  filled  with 
fluid,  namely,  ca.  up  to  the  waxy  zone,  there  is  a  "terrestrial  fauna" 
as  well  as  an  aquatic  fauna. 

Of  the  former,  aside  from  2  species  of  leaf  miners  (which,  however, 
have  been  claimed  to  behave  in  relation  to  the  water  level)  which  are 
questionably  peculiar  to  Nepenthes  pitchers,  there  are  four  spiders, 
three  of  which  are  claimed  to  be  nepenthebiont.  The  4  species  are 
Misumenops  nepenthicola,  M.  Thienemannii,  Thomisus  callidus  and  Th. 
nepenthephilus.  Th.  callidus  is  nepenthephile;  the  others  have  been 
found  up  tin  the  present  only  in  pitchers  of  Nepenthes,  but  are  not 
confined  to  any  one  species.  But  they  are  excluded  from  .V.  ampul- 
laria  because  there  is  no  w^axy  zone,  states  Thienemann;  they  should 


Francis  E.  Lloyd 


78  —  Carnivorous  Plants 


also  be  absent  from  N.  ventricosa.  Since  the  spiders  above  named  find 
their  food  in  insects  attracted  to  the  pitchers,  they  may  be  regarded 
as  commensal.  The  case  is  somewhat  if  not  quite  the  same  as  that  of 
the  spider-plant  combination  of  Roridula  (Lloyd,  1934)- 

The  "aquatic  fauna"  nepenthexene  forms  include  protozoa,  myx- 
ophyceae,  desmids  and  diatoms,  rotatoria,  Oligochaetes,  crustaceae 
and  also'  larvae  of  various  Diptera  and  a  very  occasional  tadpole. 
Such  forms  occur  relatively  infrequently,  but  are  most  abundant  in 
those  pitchers  of  N.  ampullaria  which  stand  half  buried  in  the  sub- 
stratum, as  would  be  expected.  The  nepenthephile  animals  occur  in 
only  very  small  numbers;  only  three  known  in  fact.  It  is  interesting 
to  know  that  of  these  one  is  represented  by  two  races,  one  of  which 
lives  in  hollows  of  bamboos.  The  nepenthebionts  include  the  remark- 
able number  of  26  species;  of  the  Phoridae  6,  Chironomidae  i,  and  of 
the  Culicidae  19.  All  these  are  Diptera,  19  of  which  are  mosquitos. 
It  is  admitted  that  further  research  may  reduce  or  enlarge  this  number 
somewhat,  but  it  can  hardly  alter  the  general  weight  of  the  evidence 
that  there  is  a  strikingly  large  number  of  animals  which  habitually  live 
in  the  pitchers  of  Nepenthes  and  nowhere  else.  They  feed  on  the  ani- 
mal detritus  found  there.  To  account  for  this  large  number  of  forms 
adapted  only  to  Nepenthes  as  commensals,  Thienemann  points  out 
that  Danser  refers  the  origin  of  the  genus  to  a  time  earlier  than 
the  beginning  of  the  Tertiary,  in  the  Chalk,  but  Danser  thinks  of  the 
genus  as  a  young  one. 

Folklore,  uses.  —  It  is  inevitable  that  such  an  unusual  and  curious 
plant  as  Nepenthes  should  figure  in  the  folklore  of  the  peoples  in  con- 
tact with  it.  In  this  connection  I  quote  an  interesting  passage  from 
RuMPHius  {Herbarium  Amboinense  5:123)  containing  notes  made 
about  1660  in  the  Far  East.  This  was  kindly  translated  for  me  by 
Prof.  Baas  Becking,  who  indeed  drew  my  attention  to  it. 

"Uses.  This  remarkable  plant  mostly  serves  as  a  curiosity,  to  keep  its  pitchers  amongst  other 
strange  objects  which  are  worth  keeping  to  show  the  nice  playfulness  of  nature.  To  this  end  open 
pitchers  are  preferred.  They  are  emptied  and  wind-dried,  filled  with  cotton  or  other  fine  material 
in  order  that  the  natural  form  may  be  preserved.  Or  the  dried  pitchers  are  placed  in  a  book  and 
pressed  flat.  However,  to  show  the  curiosity  more  completely,  one  should  have  the  leaf  still  at- 
tached. 

"The  natives  are  unwilling  to  bring  them  to  us  from  the  mountains,  because  of  an  old  super- 
stition according  to  which  if  one  cuts  off  the  pitchers  and  pours  out  the  water  one  will  meet  with  a 
heavy  rain  before  reaching  home.  As  this  happened  a  few  times  when  I  had  ordered  them  to  fetch 
me  the  largest  species  from  the  mountains  of  Mamalo,  they  were  strengthened  in  their  superstition, 
notwithstanding  the  fact  that  I  convinced  them  that  it  had  rained  on  the  two  days  previous  to  this 
expedition.  Others  go  to  the  mountains  when  the  rain  has  not  fallen  for  a  long  time,  and  empty 
all  pitchers  which  they  can  reach  with  a  stupid  zeal  as  they  want  to  bring  rain  to  the  land  in  this 
way;  but  the  converted  natives  do  not  dare  to  perform  such  tricks,  out  of  respect  to  our  and  to  the 
Mohammedan  priests. 

"Now  listen  to  the  contrary  effect.  If  children  often  wet  the  bed,  the  native  goes  to  the  moun- 
tains and  fetches  a  few  of  the  filled  and  still  unopened  {sic)  pitchers,  the  water  of  which  he  pours  over 
the  head  of  the  children  and  makes  them  drink  of  it,  as  they  also  do  to  adults  who  are  unable  to 
keep  their  water. 

"As  it  seems,  one  or  the  other  must  be  a  lie  or  a  great  miracle,  if  one  could  by  means  of  this 
little  pitcher  draw  the  water  from  the  heavens  and  also  keep  it  in  the  children's  bellies." 

At  a  guess,  the  virtue  attributed  by  the  natives  to  the  open  pitchers, 
out  of  which  water  can  be  poured,  and  the  unopened  pitcher,  lies  fun- 
damentally in  the  fact  that  the  latter  holds  its  water.  The  symboHsm 
appears  evident. 


Chapter  IV  —  79  —  Nepenthes 

B.  H.  Danser  (1927)  remarks  that  no  trace  of  these  superstitions 
is  to  be  found  nowadays,  but  that  the  Malayans  from  Malacca  and  the 
Riouw  Archipelago  use  the  fluid  from  the  unopened  pitchers  to  wash 
their  eyes  or  put  it  on  inflamed  skin  until  the  new  skin  is  formed. 

He  points  out  also  that  the  long  viney  stems  (lianas)  of  N.  ampul- 
laria  are  used  as  ropes  for  slinging  foot-bridges.  Possibly  other  species 
are  similarly  used. 

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Hepburn,  J.  S.,  E.  Q.  St.  John  &  F.  M.  Jones,  Biochemical  studies  of  insectivorous  plants. 

Contr.  Bot.  Lab.  U.  of  Penna.  4:419-463,  1919. — See  also  p.  39. 
Hooker,  J.  D.,  On  the  origin  and  development  of  the  pitcher  of  Nepenthes,  with  an  ac- 
count of  some  new  Bornean  plants  of  the  genus.    Trans.  Linn.  Soc.  22:415-424,  1859. 
Hooker,  J.  D.,  Address  to  the  Department  of  Zoology  and  Botany,  B.  A.  A.  S.  Report  of 

the  forty-fourth  meeting,  1874:102-116,  1875. 


Francis  E.  Lloyd  —  80  —  Carnivorous  Plants 

Hunt,  J.  Gibbons,  (A  minute  in)  Proc.  Acad.  Nat.  Sci.  Phila.  26:144,  1874. 

Jensen,  H.,  NepenlheS'TieTe,  II.     Biologische  Notizen.     Ann.  du  jard.   Buitenzorg,  Sup. 

Ill:    941-946,  1910. 
Knoll,  F.,  tJber  die  Ursache  des  Ausgleitens  der  Insektenbeine  an  Wachsbedeckten  Pflan- 

zentheilen.     Jahrb.  wiss.  Botan.  54:448-497,  1914. 
Kny,  L.  and  A.  Zimmermann,  Die  Bedeutung  der  Spiralzellen  von  Nepenthes.  Bet.  d.  d. 

bot.  Gesellsch.  3,  1885. 
KoRTHALS,  p.  W.,  Nepenthes,    in    Verb.    d.    nat.    Geschiedenis   der   Nederl.    Overzeesche 

Bezittingen  (Botanie),  Leiden,  1839/1842,  Ed.  by  C.  J.  Temminck. 
Lloyd,  F.  E.,  Abscission.    Ottawa  Naturalist  38:41-52;    61-75,  iQM- 
Lloyd,  1933&,  see  p.  269;    1934,  see  p.  8. 
Macbride,  J.  M.,  On  the  power  of  Sarracenia  adimca  to  entrap  insects.    (Read  in  1815) 

Trans.  Linn.  Soc.  London  12:48-52,  181 7. 
Macfarlane,  J.  M.,  Nature,  Dec.  25,  1884. 
Macfarlane,  J.  M.,  Observations  on  the  pitchered  insectivorous  plants,    I.    Ann.   Bot. 

3:253-266,  1889/90;    IL  7:403-458,  1893. 
Macfarlane,  J.  M.,  Nepenthaceae.     Das  Pflanzenreich,  Leipzig,  1908. 
Mangin,  L.,  Sur  le  developpement  des  cellules  spiralees.  Bull.  Soc.  bot.  France  29:14-17,  1882. 
Menzel,  R.,  Beitrage  zur  Kenntnis  der  Mikroflora  vom  Niederlandischen  Ost-Indien;  II. 

tJber  den  tierischen  Inhalt  der  Kannen  von  N.  melamphora  Reinw.  mit  bes.  Beriicksich- 

tigung  der   Nematoden.      Treubia   3:116-122    (Doubts  that  the  pitchers  are  a  mere 

"Luxus-Anpassung").    Harpacticiden als Bromeliaceen-Bewohner.   Ihid.  3:122-126, 1923. 
Meyen,  F.  J.  F.,  tJber  die  Sekretionsorganen  der  Pflanzen.    Berlin,  1837. 
Mohnike,  Blicke  auf  das  Pflanzen-  und  Thierleben  in  den   niederlandischen   Malaienlan- 

dern.     1883  (p.  148). 
Morren,  Ch.,  Morphologic  des  acidies.     Bull.  R.  Acad.  Brux.  5:430,  1838. 
Morren,  Ch.,  Criticism  of  Bower's  Review  of  above.     Ann.  Bot.  7:420,  1893. 
Oudemans,  C.  a.  J.  A.,  De  Bekerplanten.     Amsterdam  1864. 
Oye,  p.  van,  Zur  Biologic  der  Kanne  von  Nepenthes  melamphora.     Biol.   Zentralblatt  41: 

529-534,  1921- 
Rees,   M.  &  H.  Will,  Einige  Bemerkungen  iiber  "  fleischf ressende "  Pflanzen.  Bot.  Zeit. 

33:713-718,  1875  {also  see  Sitzungsber.  d.  phys.-med.  Soz.  Erlangen  8:13,  1875). 
Robinson,  W.  J.,  Torreya  8:181-194,  1908. 
RmxER,   C.   DE,  Op  zoek  naar  de  bekerplant  met  de   "Marie-Stuart  kraag",  Nepenthes 

Veitchil  Hook.  f.  De  Trop.  Natuur  24:195,  1935.     {through  Troll). 
ScHMiTZ,  P.  H.  S.  J.  &  J.  V.  DE  Janti,  Contribution  a  I'etude  de  la  faune  nepenthicole. 

Natuurhist.  Maanblad  I,  21  (9):ii6-ii7,  1932;   II,  21  (12),  1932;    III  (by  A.  Starke), 

22   (3):29-3i,   1933;    IV  (by  E.  O.  Engel,  Beitrag  zur  Morphologic  der  Larva  von 

Wilhelmina  nepenthicola  Villeneuve),  22  (4)  :46-48,  1933;  V  (by  Schmitz),  23  (3)  :26,  1934; 

VI  (by  S.  L.  Brug,  Culicidae  collected  from  iVe/>eM/Aej  in  Borneo),  23  (ii):i49-i5o,  1934- 
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53:  plate  2629,  1826. 
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252:81-96,  1932. 
Tate,  Lawson,  Nature  12:251-252,  1875. 
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1932.    Tropische  Binnengewasser  3:1-54. 
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{Digest  in  Bot.  Centralb.  50:304-305,  1892). 
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of  literature  citations.). 
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and  Mag.  Nat.  Hist.  II,  4:128-136,  1849. 
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Strassburg,  1877. 
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269:187-195,  1934. 


Chapter    V 
CEPHALOTUS   FOLLICULARIS 

Distribution.  —  Habit.  —  Habitat.  —  Foliage  leaf.  —  Pitcher  leaf.  —  Development  of 
pitcher  leaf.  —  Morphology.  —  Anatomy.  —  Digestion. 

The  West  Australian  Pitcher  Plant  is  a  unique  form  and,  though 
related  to  Sarracenia  and  Nepenthes,  diverges  from  them  in  many  de- 
tails of  form  and  structure.  It  occurs  in  a  lunate  area,  in  extreme 
S.  W.  Austraha,  one  horn  of  the  crescent  lying  about  150  miles  S.  of 
Perth,  the  other  at  the  Fitzgerald  River,  the  southern  rim  of  the  area 
passing  through  Albany.  Its  first  collector  was  probably  Archibald 
Menzies,  naturalist  of  the  Vancouver's  Expedition  of  1791.  Menzies 
"landed  at  King  George's  Sound  and  made  large  collections."  But  as 
these  were  not  studied  till  much  later  by  Robert  Brown,  the  plant, 
if  actually  found,  did  not  become  known.  In  the  following  year,  1792, 
came  the  expedition  under  d'Entrecasteau  ("  Voyage  a  la  recherche  de 
la  Perouse'').  The  naturahst  was  La  Billardiere.  He  landed  first  "on 
one  of  the  islands  of  Esperance  Bay  and  then  on  the  mainland"  (Gard- 
ner 1926).  Here  the  naturalist  of  the  expedition  found  the  plant 
which  he  later  (1806)  described  under  the  name  Cephalotus  follicularis. 

The  plant  is  of  rosette  habit,  the  rosette,  where  primary,  surmount- 
ing a  tap-root  (La  Billardiere).  and  in  older  plants  ending  branches  of 
a  freely  forking  rootstock.  These  branches  when  small  produce  for 
some  time  only  minute  leaves  and  pitchers;  more  massive  branches 
produce  at  once  larger  or  even  normal  sized  organs.  The  flowers,  in  a 
short  panicle,  and  borne  on  a  very  long  slender  scape,  triangular  at  its 
base,  are  small,  apetalous,  have  a  six-parted  calyx  and  twelve  stamens 

The  habitat  is  the  drier  parts  of  peaty  swamps.  The  leaves  are, 
as  has  been  known  since  the  publication  of  La  Billardiere's  descrip- 
tion, of  two  very  distinct  kinds:  the  fohage  leaves,  or  " non-ascidif orm " 
(Dickson  1878)  (9  —  6)  and  the  pitcher  or  ascidiform  leaves  {g  — 1-3). 

The  fohage  leaves  attain  a  length  of  about  13  or  14  cm.  when  of 
large  size.  The  blade  is  ovate  and  acute,  about  the  length  of  the  peti- 
ole, which,  as  Troll  has  shown,  is  of  unifacial  structure.  Two  of  the 
vascular  strands,  dorsal  and  ventral,  facing  each  other  wood  to  wood, 
enter  and  extend  up  into  the  blade,  thus  indicating,  according  to  Troll, 
the  peltate  structure  of  the  leaf.  The  ventral  strand  enters  and  sup- 
phes  vascular  tissues  to  the  hd  of  the  pitcher  when  this  develops  in 
place  of  a  flat  leaf.  The  blade  is  furthermore  inchned  to  transverse 
thickening  above  the  petiole  (9  —  6  at  left).  This  becomes  very  pro- 
nounced in  intergrade  forms  between  pitchers  and  foliage  leaves  which 
in  this  plant  occur  very  frequently,  and  will  be  described  below. 

The  leaf  is  thick,  coriaceous  and  supplied  with  nectar  glands,  and 
its  surface  smooth  and  glassy.  The  margins  are  ciliated  with  the 
pecuHar  hairs  mentioned  by  Dickson  (1878).     Their  pecuUarity  con- 


Francis  E.  Lloyd 


—  82  —  Carnivorous  Plants 


sists  in  the  secondary  filling  in  of  the  lumen  by  callus  (or  callus-like 
substance),  the  protoplast  withdrawing  toward  the  base.  A  central 
thread-like  core  of  protoplasmic  substance  with  more  or  less  con- 
tinuity can  be  traced  through  the  otherwise  soUd  mass  of  callus. 

FoHage  leaves  are  produced  in  seasonal  rhythm.  Of  this  A.  G. 
Hamilton  (1904)  wrote,  ''I  believe  that  the  ordinary  leaves  develop 
in  the  autumn,  reaching  their  full  maturity  in  the  spring,  and  then 
gradually  going  off,  while  the  pitchers  grow  in  winter  and  spring  and 
are  fully  formed  and  functional  in  summer  when  the  insects  which  they 
capture  are  most  plentiful."  This  seems  to  be  a  true  account.  I  can 
only  add  that  at  the  time  of  my  visit  to  the  classical  ground  of  Albany 
in  the  spring  (Oct.  1936),  the  pitchers  were  in  full  representation,  and 
foHage  leaves  much  less  conspicuous. 

The  pitchers  when  full  sized  measure  in  length  about  5  cm.  or 
slightly  more.  The  majority  measure  less,  say  about  3  cm.  in  length, 
and  about  2  cm.  in  transverse  measurement,  somewhat  compressed 
from  front  to  back.  The  orifice  is  oval  in  form,  wider  transversely 
than  from  back  to  front,  measuring  in  a  pitcher  5  cm.  long,  i  X  1.5  cm. 
(inside  measurement).  Hamilton  well  compares  the  form  of  the 
pitcher  with  that  of  a  loose  slipper,  with  the  heel  turned  over  to  form 
a  lid.  Its  stalk  (the  petiole)  stands  approximately  at  right  angles  with 
the  axis  of  the  pitcher,  and  in  this  at  once  we  see  a  marked  divergence 
from  the  morphology  of  Sarracenia  and  Nepenthes,  in  that  the  mouth 
of  the  pitcher  faces  the  base  of  the  petiole  in  Cephalotus,  while  the 
opposite  occurs  in  the  other  two  genera. 

This  is  best  understood  by  examining  the  development,  as  did 
EicHLER  (1881)  and  Goebel,  or  by  comparing  the  various  aberrant 
pitchers  which  in  this  species  are  rather  common  and  have  been  re- 
marked by  Dickson,  Goebel,  and  Hamilton.  The  true  orientation 
is  clearly  seen  in  a  pitcher  only  i  to  3  mm.  long.  Such  a  one  in  longi- 
tudinal section  is  seen  in  the  figure  {10  —  6),  in  which  it  is  evident 
that  the  Hd  does  not  terminate  the  leaf  (Dickson),  but  is  an  outgrowth 
from  the  upper  surface  of  the  petiole  below  the  pitcher  proper  while 
the  pitcher  has  been  produced  by  a  ventro-dorsal  invagination  of  the 
upper,  more  distal  region.  Abnormal  leaves,  which  occur  in  sizes  be- 
tween I  mm.  to  a  few  cm.,  bear  out  the  above  interpretation,  and  fur- 
ther show  that  the  hd  represents  the  transverse  extension  of  the  leaf 
margins  across  the  basal  zone  of  the  blade,  that  therefore  the  pitcher  is 
a  peltate  leaf  highly  differentiated  into  the  compHcated  apparatus  that 
it  is  {10  —  13-18).  The  orientation  and  course  of  the  vascular  bundles 
are  in  accord  with  this  interpretation,  though  Arber  argues  that  the 
absence  of  a  median  ventral  vein  in  the  petiole  does  not  agree  with 
Troll's  description,  and  that  this  raises  doubt  as  to  the  truly  peltate 
condition.     With  Arber,  I  find  no  median  ventral  bundle   [lo  —  2). 

The  mouth  of  the  pitcher  is  surrounded  by  a  corrugated  rim,  each 
corrugation  forming  a  claw-hke  tooth  extending  inward  and  downward, 
much  as  in  Nepenthes,  except  here  the  teeth  are  coarser  and  are  not 
provided  with  glands.  There  are  about  24  such  teeth,  the  numbers  on 
each  side  not  being  always  symmetrical.  I  counted  12  on  one  side  and 
II  on  the  other  in  a  particular  specimen.  They  are  largest  in  front 
(the  ventral  aspect  of  the  opening)  and  are  smaller  and  smaller  as  one 


Chapter  V  —  83  —  Cephalotus 

swings  around  the  curve  towards  the  lid,  and  are  longitudinally  ridged. 
The  largest  teeth,  however,  are  opposite  the  median  and  lateral  ridges 
{lo  —  2).     The  purse  of  the  pitcher  externally  has  three  strong  ridges, 
one  a  ventral  one,  T-shaped  in  transverse  section,  extending  along  the 
front  of  the  pitcher  along  its  whole  length,  along  and  below  the  midrib 
of  the  pouched  leaf,  the  other  two  lateral  and  obliquely  placed.    These, 
too,  are  T-shaped  though  less  obviously  so.     The  lateral  and  median 
wings  are  connected  by  a  low  ridge,  readily  discernible  only  in  strongly 
developed  pitchers.     From  each  lateral  wing  there  runs  a  similar  but 
more  vague   ridge  toward  the  petiole    {10  —  i,    11).     All  three   bear 
strong  cilia,  chiefly  on  the  edges  of  the  lateral  wings  {10  —  7).     These 
cilia  develop  early,  so  that  a  young  pitcher  looks,  as  Hamilton  put  it, 
like  a  "vegetable  hedgehog."     These  ridges  must  be  regarded  as  ena- 
tions  from  the  ventral  and  subventral  surfaces  of    the   leaf    (Goebel 
1 89 1,  Troll  1932).     In  addition  to  these  there  are  low  but  quite  evi- 
dent ridges  between  them,  especially  evident  near  the  toothed  rim,  and 
which  may  pass  for  mere  rugosities,  but  which  are  probably  more  than 
that.     The   rest  of  the  frontal   (appearing  ventral  but  really  dorsal) 
surface  presents  low  rugosities.    The  lid  overhangs  the  opening  more  or 
less  closely  according  to  age,  and  is  nicely  arched,  but  is  not,  as  once 
believed    (Woolls),    moveable.      It    is   traversed    radially   by   narrow 
patches  of  green  ciHated  tissue,  often  forking  once  or  twice  toward  the 
margin  of  the  lid;  and  lying  between  them  are  clear  patches  devoid  of 
chlorophyll,  which  present  window-like  areas  framed  in  green,  or  in 
nature  usually  bright  red  mullions.    Whatever  their  purpose  is,  they  are 
evidently  analogous  to  the  fenestrations   in   Sarracenia   and  Darling- 
tonia:    they  are  to  insects  apparently  open  spaces  and  the  insects  are 
thus  tempted  to  escape  through  them,  to  rebound  into  the  depths  of 
the  pitcher.     The  lid  is  emarginate,  a  feature  which  can  be  seen  in 
abnormal  intergrade  forms,  in  which  the  transverse  pad  at  the  base  of 
the  blade  betrays  itself  as  a  bilobed  structure  {10  —  11,  etc.).     In  the 
unopened  pitcher  the  apical  notch  of  the  Hd  lies  beneath  the  end  of  the 
median  enation  and  straddles  its  wing,  the  lid  margin  inclosing  the 
teeth.    The  edge  of  the  lid  is  ciHated,  the  hairs  becoming  reduced  and 
more  or  less  contorted  along  the  frontal  region.     It  is  devoid  of  a  mid- 
vein,  being  supplied  by  two  pairs  of  veins  from  the  ventral  moiety  of 
the  petiole  bundles  {10  —  4,  8).    The  veins  traverse  the  green  strips  of 
the  lid  between  the  white  patches.     From  each  of  the  angles  of  the  lid 
and  mouth  edge  runs  a  low  ridge  (scarcely  "wings"  as  Arber  puts  it) 
demarking,  according  to  Dickson,  the  ventral  aspect  of  the  pitcher 
(70  —  1,  11). 

Mrs.  Arber  (1941)  has  advanced  the  suggestion  that  "the  lid  ...  . 
may  be  interpreted  as  a  hypertrophy  of  the  collar  region",  that  it  is 
"essentially  of  the  same  nature  as  the  collar"  being  "indicated  by  the 
fact  that  the  cornice  continues  unaltered  below  both  the  collar  and  the 
lid.  It  is  possible  that  the  thickened  ribs  of  the  expanded  hd  are 
equivalent  to  the  hooks  of  the  collar".  To  this  it  may  be  replied  that 
the  teeth  of  the  rim  are  developed  from  the  margin  of  the  abaxial,  distal 
part  of  the  leaf  and  that  the  lid  is  the  whole  adaxial,  basal  part  of  the 
leaf  which,  as  the  teratological  evidence  shows  (/o —  13-18),  arises  as 
two  lobular  extensions  that  fuse  (concrescence),  the  indication  of  this 


Francis  E.  Lloyd 


84  —  Carnivorous  Plants 


fusion  being  found  in  the  emargination  of  the  lid,  and  in  its  ''dual" 
structure,  to  be  expected  in  peltate  leaves. 

The  whole  of  the  pitcher,  "slipper"  shaped  as  already  said,  has  a 
gentle  forwardly  concave  curvature.  The  under  side  is  the  thinnest 
region,  and  rests,  in  nature,  on  the  surface  of  the  soil,  in  such  a  manner 
that  the  pitcher  stands  more  or  less  obHquely  {9  —  1,  2). 

The  interior  of  the  pitcher  is  divisible  into  two  distinct  zones,  the 
upper  of  which  forms  a  collar  with,  at  its  lower  edge,  an  overhanging 
eave.  The  epidermis  of  this  collar  ("conducting  shelf",  Dickson) 
forms  a  surface  of  low  pointed  trichomes  which  are  downwardly  di- 
rected, supplying  a  smooth,  glistening,  chalk- white  face.  This  surface 
is  continuous  with  that  of  the  lid,  where  the  trichomes  point  in  the 
same  sense  but  here  they  are  very  low  and  appear  as  imbricated. 
Among  them  are  numerous  nectar  glands. 

The  jutting  eave  overhangs,  like  the  entrance  of  a  lobster  pot,  the 
far  interior  of  the  pitcher.  Here  the  surface  is  smooth,  and  the  epider- 
mal cells  are  wavy-walled,  the  radial  synclinal  walls  supported  by 
numerous  buttresses  from  the  angles  of  the  undulations.  There  are  in 
the  upper  region  (ca.  one  half  of  the  surface)  extending  further  down 
in  front  than  behind,  many  glands,  which  are  smaller  above,  becoming 
larger  below.  These  are,  it  may  be  fairly  argued,  digestive  in  function. 
In  the  lower  half  there  is  on  each  side  an  obliquely  placed  kidney- 
shaped  mass,  in  reaUty  a  thickened  bolster  of  tissue,  called  by  Dick- 
son the  "lateral  coloured  patch,"  since  it  is  usually  deeply  red  colored, 
and  which  Hamilton  preferred  to  call  the  "lateral  gland  mass."  The 
upper  zone  of  this  bolster  is  the  seat  of  a  number  of  very  large  glands 
though  they  are  not  wholly  confined  to  it  (9  —  4)-  Its  lower  half  has 
a  very  peculiar  feature  in  the  presence  of  numerous  immobile  stomata 
with  widely  open  mouths  first  observed  but  not  properly  understood 
by  Dickson  (/o  — 23).  The  function  of  the  glands  also  is  digestive, 
the  general  evidence  for  which  was  offered  by  Dakin  {see  below).  The 
lower  portion  of  the  general  surface  of  the  pitcher  interior  is  entirely  free 
of  glands.  Hamilton  thinks  that  normally  only  the  lower  portion  of 
the  pitcher  holds  fluid  and  the  obliquity  of  the  distribution  of  the 
glands  in  the  upper  zone  is  correlated  therewith,  since  the  pitchers 
usually  lie  somewhat  obliquely  on  the  ground.  My  own  observations 
lead  me  to  doubt  this  as  a  matter  of  fact;  particularly  it  is  difficult  to 
agree  that  the  quantity  of  fluid  is  so  definitely  restricted.  While  it  is  a 
curious  enough  fact  that  the  distribution  of  the  glands  is  as  described 
above,  there  may  very  well  be  another  explanation,  for  the  glands  of 
the  lateral  patches  in  any  event  would,  according  to  the  Hamllton 
view,  be  submersed. 

Slender  rhizomes  produce  very  small  pitchers,  having  a  slightly 
different  aspect  in  detail  from  that  of  the  normally  larger  pitchers. 
They  attain  a  size  in  general  of  about  i  cm.  in  length,  often  less,  with 
tissues  correspondingly  thinner  and  more  delicate.  A  major  difference 
is  in  the  development  of  the  teeth  surrounding  the  mouth:  there 
are  fewer  of  them  and  all  arise  from  an  external  low  ridge,  and  stand 
freely  independent  of  the  actual  edge  of  the  mouth  (70  —  9-12),  one 
opposite  each  of  the  three  wings,  and  two  further  back  on  each  side. 
A  further  important  difference  is  the  relatively  greater  width  of  the 


Chapter  V  —  85  —  Cephalotus 

collar,  as  will  be  clear  in  the  figures.  Correlated  with  size  are  the 
simpler  venation  and  small  number  of  glands.  Hamilton  drew  atten- 
tion to  this  condition  (1904).  In  the  large  pitchers  the  teeth  are 
concrescent  with  the  rim  and  overhang  it  inwardly.  Another  feature 
of  juvenile  pitchers  is  the  large  size  of  the  lid,  which  is  strongly  arched 
and  widely  overhangs  the  opening,  so  that  it  more  efifectually  pre- 
vents the  entrance  of  rain  water,  or  appears  to.  As  I  have  observed 
these  small  pitchers  are  efficient  in  catching  correspondingly  small 
insects. 

Transition  forms  between  the  large  and  small  pitchers  have  not 
been  observed.  When  a  relatively  large  pitcher  appears  after  a  number 
of  small  ones  have  been  produced,  the  passage  from  the  small  to  the 
large  form  is  made  at  once  in  a  jump. 

We  turn  to  the  anatomy  of  the  pitcher  {10  —  3,  6,  12).  The 
venation  is  derived  from  two  systems  of  bundles  in  the  petiole,  a  dorsal, 
of  three  veins,  and  a  ventral  of  two,  these  splitting  near  the  pitcher 
into  four,  then  six  and  branching  further  in  spreading.  Referring  to 
the  figures  in  which  the  veins  are  numbered,  we  see  that  of  the  ventral 
system,  Vi,  (median  ventral  pair)  passes  into  the  lid,  right  and  left 
of  the  midline;  V2  sends  veins  into  the  sides  of  the  hd  and  into  the 
collar;  V3  goes  entirely  to  the  upper  part  of  the  digestive  cavity, 
anastomosing  with  the  dorsal  veins.  It  seems  quite  doubtful  that 
Arber's  statement  about  "the  relatively  high  development  of  the 
ventral  system  of  the  pitcher's  venation"  corresponds  with  the  facts, 
since  one  third  of  it  is  not  connected  with  the  lid  at  all,  and  only  a 
small  part  of  it  with  the  collar.  Of  the  three  dorsal  veins  of  the 
petiole,  the  median  is  the  midvein  of  the  pitcher,  passing  entirely 
around  it,  and  ending,  not  in  the  point  of  the  median  ridge,  as  Dickson 
claimed,  who  therefore  regarded  it  as  the  leaf  apex,  but  in  the  collar, 
opposite  the  middle  tooth,  there  branching.  Of  the  laterals  (D2)  each 
runs  obliquely  down  the  side  of  the  pitcher  toward  the  upper  end  of 
the  glandular  patch,  having  just  before  reaching  it  sent  a  branch  into  a 
lateral  ridge,  whence  it  emerges  in  the  collar.  Traversing  the  glandular 
patch  obliquely  it  leaves  it  near  the  middle  point  and  then  runs  up  the 
wall  parallel  to  the  midvein,  and  ending  in  the  collar.  The  midvein 
(Di)  sends  branches  right  and  left  into  the  lower  part  of  the  pitcher. 
This  basic  arrangement  of  the  vascular  system  of  the  pitcher  can  be 
most  clearly  seen  in  a  very  young  one,  3  mm.  long  {10  —  5). 

The  external  surface  of  the  pitcher  is  covered  with  an  epidermis  of 
isodiametric  cells  with  thick  walls,  and  is  supplied  with  stomata  and 
nectar  glands.  On  the  lid  the  epidermis  of  the  green  patches  is  of 
more  or  less  wavy-walled  cells,  with  glands  and  stomata  interspersed, 
while  in  the  fenestrations  the  cells  are  isodiametric  and  straight  walled, 
with  glands  but  no  stomata. 

The  epidermis  of  the  interior  surface  of  the  lid  and  collar  has  been 
already  described  above.  That  of  the  far  interior  is  of  wavy- walled 
cells,  the  walls  thick  and  buttressed  at  the  angles.  Scattered  through- 
out the  surface,  except  along  a  narrow  strip  beneath  the  eave  of  the 
collar,  and  the  deeper  portion  of  the  pitcher  demarked  by  an  oblique 
fine  running  downward  and  forward  from  about  the  middle  point  of 
the  back  surface  across  the  top  of  the  glandular  bolster,  there  are 


Francis  E.  Lloyd  —  86  —  Carnivorous  Plants 

numerous  glands.  These  are  smaller  above  and  become  increasingly- 
larger  below.  In  the  bolster  itself  the  glands  attain  the  maximum  size, 
and  occupy  chiefly  the  upper  half  of  it,  though  not  entirely  excluded 
from  the  lower  half  {9  —  4).  This  latter  is  covered  with  a  wavy- 
walled  epidermis  supplied  with  extremely  numerous  stomata. 

The  small  glands  which  occur  on  the  outer  surface  and  on  the  inner 
surface  of  the  Hd,  have,  as  Goebel  (1891)  pointed  out,  essentially  the 
same  structure  as  those  of  Sarracenia,  but  are  directly  comparable 
rather  to  those  of  the  outer  surface  of  the  pitcher  in  that  genus.  In 
these  there  is  only  one  course  of  cells,  six  in  number,  surmounting  a 
single  parenchyma  cell  (2  —  16).  The  same  is  true  of  Cephalotus,  with 
the  difference  that,  while  in  Sarracenia  the  "cover"  cells  are  inwardly 
drawn  out  to  a  point,  those  in  the  Cephalotus  gland  reach  inwardly  as 
far  as  do  the  four  surrounding  cells  {10  —  21).  The  glands  are  very 
small,  indeed  no  bigger  in  transverse  section  than  the  stomata  with 
which  they  are  interspersed,  and  are  no  deeper  than  the  surrounding 
epidermal  cells.  The  outer  walls  are  all  suberized,  except  both  outer 
and  inner  walls  of  the  basal  cell,  derived  from  the  parenchyma.  The 
inner  wall  of  this  cell,  in  contact  with  the  six  other  cells,  is  not,  as  in 
Sarracenia,  reticulated.  Whether  more  than  one  cell  at  the  base  of  the 
gland  may  be  regarded  as  part  of  the  gland  is  questionable  but  possible. 
I  have  seen  some  indications  that  such  is  the  case,  as  Goebel  (1891) 
seems  to  have  thought.  As  he  did  not  afford  a  drawing  (nor  has  any- 
one else  since)  of  this  particular  gland,  it  is  difficult  to  decide  what 
precisely  was  Goebel's  meaning. 

These  glands  are  found  on  all  green  parts,  and  appear  to  have  the 
same  function  as  analogous  glands  in  Nepenthes,  Sarracenia.  Hamil- 
ton observed  insects  feeding  on  the  outer  surface  of  the  pitcher,  but 
could  not  satisfy  himself  that  nectar  was  present.  It  is  possible  as 
Goebel  suggested  that  they  secrete  something  else  attractive  to  in- 
sects. 

The  glands  of  the  inner  surface  of  the  lid  have  the  same  structure 
as  those  above  described. 

In  the  far  interior  of  the  pitcher  the  glands  are  of  various  sizes, 
smaller  above  and  increasingly  larger  the  deeper  they  are  placed  till 
the  maximum  size  is  reached  in  the  glandular  patches.  They  are  flask- 
shaped,  with  a  broad  neck  lying  in  the  plane  of  the  epidermis,  made 
up  of  a  greater  or  smaller  number  of  columnar  cells  (neck  cells)  whose 
outer  walls  are  very  much  thickened  and  pitted.  The  wafls  lying 
against  the  epidermis  around  the  neck  of  the  gland  are  also  thickened 
and  suberized,  and,  forming  an  investment  of  the  whole  gland  there  is 
a  single  layer  of  flatfish  cells  (similar  to  the  flat  cell  below  the  small 
gland  of  the  outer  pitcher  surface)  which  are  strongly  cuticularized  in 
their  radial  waUs  only,  not,  as  Goebel  thought,  wholly.  Each  of  these 
sheathing  ceUs  is  therefore  a  window,  or  better  a  double  cellulose 
window  framed  in  mullions  of  suberized  walls.  The  body  of  the  gland 
is  made  up  of  rounded  thin-walled  cells,  evidently  the  active  glandular 
secreting  cells,  as  indicated  by  the  richness  of  the  protoplasmic  con- 
tent {10  —  20). 

When  the  neck  ceUs  are  examined  as  part  of  the  epidermis  in  face 
view,  the  outer  walls,  in  the  case  of  the  smallest  glands,  are  arranged 


Chapter  V  —  87  —  Cephalotus 

in  the  typical  manner  —  two  cover  cells  surrounded  by  four  others.  In 
slightly  larger  glands  additional  cells  are  intercalated.  Their  outer 
walls  are  seen  now  to  be  thick  and  pitted.  The  surrounding  epidermal 
cells  overlap  the  shoulder  of  the  flask,  and  the  strong  buttress  thicken- 
ings of  their  radial  cell  walls  stand  out  {lo  —  20). 

The  largest  glands  are  to  be  found  in  the  areas  in  the  "colored 
patches"  as  Dickson  called  them,  on  account  of  their  deep  red  color- 
ing. They  differ  in  no  respect  beyond  that  of  size  from  the  others. 
They  are  spherical  in  form,  with  a  thick  neck  and  the  central  mass  of 
something  like  150  to  200  cells  is  surrounded  as  seen  above  by  a  single 
layer  of  flat  cells  with  their  radial  walls  suberized,  the  periclinal  walls 
being  of  cellulose,  thus  ensuring  a  path  of  diffusion  {10  —  19). 

The  colored  or  glandular  patches,  of  which  there  are  two,  one  on 
each  side  of  the  pitcher,  are  the  most  remarkable  feature  of  this  species. 
They  are  reniform,  thickened  regions  of  the  wall,  the  outline  being  sharp 
and  well  marked  below  and  more  or  less  crenate  along  the  upper 
edge  (p  —  4).  It  is  a  "bolster"  (Goebel)  of  tissue  in  which  the 
mesophyll  is  more  developed  than  otherwhere,  and  projecting  in- 
wardly, showing  no  sign  of  its  presence  on  the  outer  surface.  The 
glands  just  mentioned  are  more  numerous  on  the  upper  moiety,  but  are 
by  no  means  confined  to  it.  The  epidermis  between  the  glands  offers 
the  most  remarkable  appearance  of  all  in  that  it  is  supphed  with  in- 
numerable stomata.  Dickson  (1878)  described  them  as  small  oval 
bodies  surrounded  by  two  to  four  other  cells.  Hamilton  remarked 
that  they  are  "remarkably  Kke  stomates"  but  that  there  is  always  a 
wide  opening  between  the  guard  cells.  Dakin  (191 8),  at  that  time  a 
member  of  the  staff  of  the  University  of  Western  Australia,  visited 
Albany  and  there  obtained  material  for  study.  He  saw  clearly  that 
these  structures  are  stomata,  confirming  Goebel's  earlier  description 
(1891).  It  is  clear  that  the  guard  cells  are  immobile  and  that  these 
stomata  do  not  function  as  such.  Goebel  called  them  water  pores, 
pointing  out  that  the  pore  is  plugged  by  the  cellulose  membrane  of  a 
parenchyma  cell  underlying  it,  which  would  not,  of  course,  prevent  the 
excretion  of  water.  Dakin  found  that  the  membrane  closing  the  pore 
is  locally  thickened  to  form  a  "pad"  which  he  thought  acted  as  a 
torus  that,  with  changing  turgidity  of  the  cell,  would  open  and  close 
the  pore,  the  whole  acting  as  a  regulating  mechanism.  He  further 
thought  that  the  function  of  the  stomata  is  absorption  and  suggested 
that  the  glandular  patches  be  called  lateral  absorbing  areas  {10  —  12). 

I  found  (19336)  that  Dakin  is  correct  in  his  claim  that  the  wall  of 
the  underlying  parenchyma  cell  is  thickened  beneath  the  pore;  but 
that  the  thickening  is  so  definitely  torus-like  as  he  showed  in  his  figure 
(191 8,  Fig.  11),  and  especially  his  interpretations  are  certainly  to  be 
doubted.  There  is  some  evidence  that  the  plugging  membrane  is  the 
result  of  hydrolysis  of  the  occluding  wall  and  that  there  is  given  off  a 
mucilage-hice  secretion  (Lloyd  19336),  but  further  study  on  fresh  ma- 
terial obtained  at  Albany  does  not  strengthen  this  idea  of  the  matter. 
The  more  ready  staining  of  the  torus-like  thickening  is  due  to  the  fact 
that  it  is  not  cuticularized  as  are  the  guard  cells  and  the  epidermis  in 
general,  so  that  cellulose  stain  (such  as  methylene  blue)  attacks  the 
thickening   quickly.     That,   however,   these   structures  are   important 


Francis  E.  Lloyd  —  88  —  Carnivorous  Plants 

physiologically  is  hard  to  resist  in  view  of  their  number  and  general 
relations.  Goebel's  idea  that  they  are  water  pores  seems  the  most 
acceptable,  that  is,  that  they  pour  a  fluid  into  the  pitcher  cavity;  but 
this  fluid  may  contain  substances  in  solution,  more  Hkely  enzymes, 
possibly  one  or  more  enzymes  different  from  those  of  the  glands.  I 
did  a  simple  experiment  with  living  pitchers  to  test  Goebel's  idea. 
Halving  a  pitcher  longitudinally,  and  cleaning  it  out  thoroughly,  I 
placed  it  in  contact,  by  its  outer  surface,  with  water  in  a  closed  damp 
chamber.  In  the  course  of  some  hours  beads  of  moisture  appeared 
from  the  mouths  of  the  glands,  larger  ones  from  the  larger  glands  but 
none  from  the  stomata,  at  least  in  appreciable  quantities.  This  seems 
to  indicate  that  water  excretion  by  the  "water  pores"  plays  a  minor 
role,  if  any,  and  that  Dakin's  suggestion  that  their  function  is  that  of  ab- 
sorption cannot  be  dismissed  without  further  examination.  Any  in- 
terpretation of  the  activity  of  these  stomata  must  take  into  account 
the  constant  presence  of  a  large  amount  of  starch  in  large  grains  in  the 
mesophyll  of  the  glandular  patches. 

The  problem  of  digestion  by  the  pitchers  has  been  examined  in  any 
thoroughgoing  way  only  by  Daken  (191 8),  who  spent  a  vacation  at 
Albany,  W.  A.,  making  as  careful  a  study  as  he  could,  under  laboratory 
conditions.     To  be  sure,  Dickson  (1878)  had  reported  that  Lawson 
Tate  had  examined  into  the  matter  somewhat  and  had  found  that 
"fluid  taken  from  virgin  or  unopened  pitchers"  showed  "that  it  ex- 
erted a  similar  digestive  action  on  animal  substances  to  that  exhibited 
by  the  Nepenthes  pitcher,  etc."     Dakin  made  use  only  of  the  fluid 
from  opened  pitchers,  which  did  not  surprise  me  when  on  careful  ex- 
amination of  all  the  unopened  pitchers  which  I  could  come  by  on  my 
own  visit  to  Albany,  I  found  no  one  of  them  containing  any  sign  of 
fluid,  a  matter  of  disappointment  as  I  had  intended  to  conduct  experi- 
mentation on  such  fluid  if  it   could    be   found.     Dakin's   results   are 
as  follows:    He  found  that  the  pitchers  capture  many  insects,  notably 
ants,  as  others  had  found.     They  are  represented  usually  by  fragmen- 
tary remains  of  the  chitinous  parts.    Even  the  very  small  pitchers,  as  I 
have  previously  said,  catch  small  insects.    That  the  soft  parts  undergo 
dissolution  in  some  sort  is  at  once  evident.    But,  Dakin  asked,  is  this 
the  result  of  digestion  by  enzymes  secreted  by  the  pitcher  glands,  or  of 
bacterial  action,  or  of  both  ?     Fibrin  was  his  test  substrate.     The  ex- 
periments were  conducted  with  pitcher  fluid  with  an  antiseptic  (HCN) 
and   with    and    without    weak    acid    (HCl)    or    alkaK.      The    specific 
results  which  he   records  showed  that   pitcher   fluid    in   vitro  in   the 
presence  of  added  acid  does  digest  fibrin,  and  that  it  contains  a  di- 
gestive ferment  which  will  break  up  proteins  into  peptone-like  bodies 
in  the  presence  of  acid.    Since  non-acidulated  pitcher  fluid  does  not  act 
thus,  it  cannot  be  concluded  that  this  process  actually  takes  place  in 
the  pitchers  under  normal  circumstances.     Pitcher  fluid  alone  procures 
dissolution  of  fibrin  with  the  odor  of  putrefaction.     Dakin  admits  the 
possibility  that  digestion  by  pitcher  fluid  may,   however,   take  place 
very  slowly  in  the  pitchers. 

He  raises,  however,  the  question  of  the  usefulness  or  necessity  of 
this  to  the  plant.  He  kept  plants  under  his  eye  in  the  laboratory 
where  they  grew  thriftily  and  flowered  without  having  been  supplied 


Chapter  V  —  89  —  Cephalotus 

with  insects.  In  view  of  the  work  of  Busgen  (Utricularia)  and  of  F. 
Darwin  (Drosera)  he  does  not  exclude  a  "carnivorous  tendency." 
On  the  whole,  therefore,  at  the  present  moment,  the  evidence  favors 
the  view  that  both  the  secretions  of  the  pitcher  and  the  action  of 
bacteria  contribute  to  the  breaking  down  of  proteins  making  the 
products  available  to  the  plant.  Experiments  with  starch  showed  no 
evidence  of  the  presence  of  diastase. 

Literature    Cited: 

Arber,   Agnzs,   On   the   morphology   of   the   pitcher-leaves  in   Heliamphora,    Sarracenia, 

Cephalotus,  and  Nepenthes.  Ann.  Bot.  n.s.  5:563-578,  1941. 
Brown,    Robert,    General   remarks   on   the   botany   of   Terra   Australis.      Miscellaneous 

Botanical  Works  i  :76-78,  1866. 
Dakin,  W.  J.,  The  West  Australian  pitcher  plant  (Cephalotus  follicular  is),  and  its  physi- 
ology.   Journ.  Roy.  Soc.  W.  Austr.  4:37-53.  1917/1918. 
Dickson,  A.,  The  structure  of  the  pitcher  of  Cephalotus  follicularis.    Journ.  of  Bot.  16:1-5, 

1878. 
Dickson,  A.,  On  the  morphology  of  the  pitcher  of  Cephalotus  follicularis.    Trans,  and  Proc. 

Bot.  Soc.  Edin.  14:172-181,  1882. 
EiCHLER,  A.  W.,  tJber  die  Schlauchblatter  von  Cephalotus.    Jahrb.  des  Berliner  Bot.  Gart. 

1:193-197,  1881  {through  Engler  u.  Prantl). 
Gardner,  C.  A.,  The  history  of  botanical  investigation  in  Western  Australia.  Handbook 

for  B.  A.  A.  S.  i8th  meeting,  Perth,  W.  A.,  1926  (Pp.  40-52). 
GiLBURT,  W.  H.,  Notes  on  the  histology  of  pitcher  plants.     Quekett  Microscopic  Journal 

6:151-164,  1881. 
Goebel,  K.,  Pflanzenbiologische  Schilderungen,  Pt.    2.   Marburg    1891.     {Cephalotus:   pp. 

110-115;    170-173). 
Hamilton,  A.  G.,  Notes  on  the  West  AustraHan  pitcher  plant  {Cephalotus  follicularis  La 

Bill.).     Proc.  Linn.  Soc.  N.  S.  W.  29:36-53,  1904. 
Lloyd,  F.  E.,  The  carnivorous  plants  —  a  review  with  contributions  (Presidential  Address). 

Trans.  Roy.  Soc.  Can.  HI,  27:1-67,  1933. 
Maury,  Paul,  Note  sur  I'acidie  du  Cephalotus  follicularis  La  Bill.     Bull.  Soc.  Bot.  France 

34:164-168,  1887. 
Tate,  Lawson,  Phil.  Trans.  Birmingham  1878  {through  Hamilton). 
Troll  {see  under  Nepenthes). 
Woolls,  W.,  Lectures  on  the  vegetable  kingdom,  p.  icx)  {through  Hamilton). 


Chapter   VI 
GENLISEA 

Discovery.  —  Early  studies.  —  Two  kinds  of  leaves.  —  Anatomy  of  trap-leaf. 

The  specimens  on  which  the  genus  Genlisea  is  based  were  discovered 
by  AuGUSTE  DE  Saint-Hilaire  in  Brazil  in  1833.  Most  of  the  species 
are  found  in  the  New  World  in  Brazil,  the  Guianas  and  Cuba,  while 
two  are  known  from  west  tropical  Africa.  The  Cuban  species,  found 
many  years  ago  by  C.  Wright  at  the  time  he  found  Biovularia  olivacea, 
has  never  again  been  collected. 

For  our  information  about  these  plants  we  are  indebted  first  of  all 
to  Warming  (1874)  and  to  Goebel  (1891).  All  the  species  are  small 
plants  which  inhabit  swampy  places  and  apparently  live  mostly  sub- 
mersed in  shallow  water,  only  the  inflorescence,  as  in  Utricularia,  pro- 
jecting above  the  surface.  This  is  to  be  inferred  from  the  absence  of 
stomata  and  from  the  fact  that  colonies  of  algae  have  been  observed  by 
me  attached  to  the  surfaces  of  the  leaves.  Benjamin  in  the  Flora  Bra- 
siliensis  says  merely  "herbae  paludosae."  The  close  relationship  to 
Utricularia  is  shown  by  the  fact  that  the  structure  of  the  flower  is  the 
same  in  the  two  genera,  that  of  Genlisea  differing  in  having  a  five- 
parted  calyx  instead  of  the  two-parted  calyx  of  Utricularia.  All  are 
rosette  plants  with  two  kinds  of  leaves,  foliage  and  trapping,  arising 
from  a  vertical  or  sometimes  nearly  prostrate  rootstock.  Like  Utric- 
ularia, there  are  no  roots,  though  the  trap  leaves  look  superficially 
much  like  them  and  have  been  mistakenly  so  regarded  by  some  (p  —  7 ; 

The  first  thorough  description,  though  lacking  in  an  important  de- 
tail, was  published  by  Warming  in  1874.  This  work  was  known  to 
Darwin,  whose  son  Francis  repeated  Warming's  observations  and 
afforded  the  description  given  by  Darwin  in  his  Insectivorous 
Plants  (P.  360,  2nd  ed.  of  1875).  Goebel's  description  of  1891,  though 
incorrect  in  certain  details,  leaves  otherwise  little  to  be  desired.  The 
plant  which  these  authors  studied  was  Genlisea  ornata,  the  largest 
known  species.  The  present  account  is  based  on  herbarium  specimens 
(British  Museum  of  Natural  History  and  Kew)  but  more  particularly 
on  alcohol  material  kindly  sent  to  me  by  Dr.  F.  C.  Hoehne,  collected 
in  Butantan,  Brazil.  As  far  as  the  anatomy  is  concerned  the  genus  is 
very  homogeneous.  Darwin,  it  is  true,  described  G.  filifor?nis ^  as 
bearing  bladders  like  those  of  Utricularia  and  being  devoid  of  ''utricu- 
Hferous  leaves"  characteristic  of  the  other  species.  I  examined  all 
the  specimens  of  Genlisea  filiformis  at  Kew,  which  was  the  source  of 
Darwin's  material,  but  could  find  no  evidence  to  corroborate  him. 
It  seems  quite  certain  that  he  examined  a  plant  which  had  been  grow- 
ing with  a  Utricularia  whose  stolons  had  intermixed  with  the  Genlisea 
leaves.     Indeed,  I  saw  a  case  of  this. 

There  are  two  kinds  of  leaves,  true  foliage  leaves,  linear  or  spatulate 


Chapter  VI  —  91  —  Genlisea 

in  form,  and  trap  leaves,  all  arising  densely  crowded  and  without  trace- 
able order,  from  a  slender  rhizome,  very  much  as  the  leaves  and  stolons 
arise  from  the  radially  symmetrical  corm-like  stem  of  the  seedling  of 
Utricularia.  There  are  no  axillary  buds,  again  as  in  Utricularia, 
but  the  rhizome  produces  a  few  branches  toward  the  apex,  which  is 
the  widest  part.  The  trap  leaves  arise  like  the  stolons  of  Utricularia 
and  at  first  look  like  them.  At  first  cyHndrical  with  a  tapering  grow- 
ing point,  they  grow  out  for  some  distance  (i  cm.  or  more  or  less)  be- 
fore any  further  differentation  takes  place.  In  structure  this  portion 
consists  of  epidermis  inclosing  a  very  extensive  intercellular  air  space 
of  lysigenous  origin.  In  the  dorsal  sector  lies  a  cord  of  relatively  few 
parenchyma  cells  surrounding  the  vascular  tissue,  again  quite  hke  a 
Utricularia  stolon.  This  portion  may  be  called  the  foot  stalk,  but  not 
petiole  since  this  leaf  region  is  produced  by  intercalary  extension  be- 
tween the  leaf  base  and  the  apex,  while,  as  Goebel  pointed  out,  the 
base  at  the  foot  stalk  is  the  oldest  portion  of  the  trap  leaf,  which  ex- 
tends solely  by  apical  growth.  At  length  the  end  of  the  footstalk  be- 
gins to  widen  and  an  invagination  takes  place  just  behind  the  tip  and 
on  the  ventral  (upper)  side.  The  basal  portion  of  the  invagination  be- 
comes a  subspherical  hollow  bulb.  The  neck  of  this  bulb  extends  for 
some  distance  to  form  a  tube,  which  toward  the  mouth  gradually 
widens  to  right  and  left,  so  that  the  opening  becomes  a  transverse  slit, 
with  the  lips  dorsal  and  ventral,  the  latter  being  shorter,  and  the  for- 
mer being  more  or  less  arched  over  the  opening.  The  angles  of  the 
mouth  develop  into  two  long  arms  with  circinate  apices,  the  slit  being 
on  the  outer  curve  of  the  crook  (//  — 3,  4,  7).  During  elongation  and 
resulting  from  rotatory  growth,  the  arms  become  twisted,  the  one  on 
the  right,  clockwise,  the  other  counter  clockwise  {11  —  8,  10).  In 
consequence  one  lip  of  the  mouth  of  the  arm,  which  extends  through- 
out its  length,  becomes  longer  than  the  other,  so  that,  if  an  arm  be 
laid  open  it  takes  the  form  of  a  spiral  ribbon  {11  —  9).  The  arms  may 
be  likened  to  two  ribbons  folded  longitudinally  and  twisted  on  the  long 
axis  so  that  the  two  edges  form  spirals  roughly  parallel  to  each  other. 
One  edge  becomes  the  inner,  and  in  the  plant  is  the  shorter.  In  the 
actual  trap,  the  two  edges  are  anchored  to  each  other  at  short  inter- 
vals. This  is  accomplished  by  large  marginal  cells,  cystid-like  in  ap- 
pearance, which  during  growth  become  pressed  into,  and  adherent  to, 
the  tissue  of  the  apposed  edge.  These  large  cells  we  may  with  Goebel 
term  prop-cells.     They  were  first  described  by  Goebel  (1891)  but  not 

quite  correctly.     He  wrote  " the  funnel  shaped  entrances  are 

formed  by  the  occurrence  at  certain  distances  apart  of  two  large  clear 
cells  which  He  the  one  upon  the  other,  and  which  may  be  called  prop- 
cells.  They  are  merely  the  end  cells  of  the  rows  of  trapping  hairs  in 
which,  however,  the  hair  itself  is  merely  one-celled,  while  the  cell  be- 
neath is  swollen  to  a  giant  size."  By  making  a  paper  model  it  will  be 
seen,  continues  Goebel,  "that  in  order  that  the  two  prop-cells  shall 
really  meet  each  other  it  is  necessary  that  the  shorter  edge  of  the  arm 

shall  be  bent  outwardly.     One  can  see    the    two    prop-cells " 

This  passage  is  quoted  to  indicate  that  Goebel  thought  that  there  is 
a  row  of  prop-cells  along  each  margin  of  the  arm  entrance,  and  that 
during  development  these  meet  and  adhere  in  pairs,  the  one  prop-cell 


Francis  E.  Lloyd  —  92  —  Carnivorous  Plants 

to  the  other.  The  facts  are  otherwise.  There  is  a  row  of  prop-cells 
on  only  one  edge,  and  the  prop-cell  is  Only  the  middle  cell  of  a  three- 
celled  hypertrophied  trichome,  the  basal  cell  of  which  is  much  enlarged, 
while  above  it  the  middle  cell  is  enormously  large  and  ends  in  a  small 
knob-shaped  cell  terminating  the  trichome  (72^15).  In  structure 
they  are,  therefore,  not  at  all  different  from  the  neighboring  trapping 
hairs,  except  for  relative  sizes  of  the  component  cells.  The  size  of  the 
basal  and  middle  cells  is  so  large  that,  in  sections  which  are  bound  to 
be  pretty  complicated  to  the  eye,  they  appear  as  two  apposed  and  ad- 
herent cells.  GoEBEL  represented  them  thus  in  his  figures  (7a  and  76, 
plate  16,  1 891).  It  is  significant  that  Goebel  showed  a  terminal  cell 
on  only  one  of  each  pair  of  prop-cells,  as  he  regarded  them  to  be  (Figs. 
6  and  76).  In  this  detail  Goebel  was  correct.  What  he  took  for  the 
prop-cells  along  the  shorter  border  of  the  ribbon-like  arm  are  the  scar- 
like depressions,  optically  suggesting  raised  surfaces,  which  are  really 
dished  out  surfaces  against  which  the  prop-cells  of  the  longer  border 
lay  and  to  which  they  were  attached  {11  —  6).  When  the  two 
margins  of  the  arms  are  torn  apart  in  dissection,  it  happens  more 
frequently  than  otherwise  that  the  whole  of  the  prop-hair  is  torn  away 
from  its  moorings,  leaving  bare  the  depressed  surface  to  which  it  was 
attached.  The  depression  so  caused  is  spoon-shaped,  the  bottom  being 
formed  of  cells  which  have  been  more  or  less  distorted  by  the  pressure 
of  the  prop-cell  during  growth  {12  —  18).  On  the  other  hand,  the  prop- 
cell  is  sometimes  torn  away  from  its  basal  cell,  and  remains  on  the 
wrong  margin,  a  perfidious  witness  whose  evidence  is  hereby  impeached. 

A  striking  analog  of  the  prop-cells  is  to  be  found  in  the  cystidia  in 
CopHnus  atramentarius  in  which  they  serve  to  keep  the  slender  gills 
at  a  certain  distance  apart,  allowing  the  free  dispersal  of  spores,  as 
described  by  Buller  (1922),  in  his  Researches  on  Fungi,  where  he  in- 
troduces the  engineering  term  "distance  pieces"  for  the  cystids. 
Protruding  from  one  gill,  from  which  they  arise,  their  free  ends  are 
attached  to  the  surface  of  the  next  gill. 

The  size  of  the  trap  leaf  in  Genlisea  repens,  one  of  the  smallest 
species,  is  as  follows.  The  footstalk  is  about  i  cm.  in  length  support- 
ing the  bulb-shaped  flask  which  is  about  i  mm.  long  and  0.7  mm. 
broad.  The  surmounting  tube  is  about  i  cm.  long,  and  0.27  mm.  in 
outside  diameter.  The  arms  extend  i  cm.  beyond  the  transverse  mouth 
and  are  little  more  than  0.5  mm.  in  width.  In  a  large  African  species, 
the  traps  are  about  three  to  five  times  the  foregoing  dimensions,  the 
tube  being  relatively  shorter.  The  footstalk  may  be  5  cm.  long,  the 
tube  two  and  the  arms  3  to  5  cm.  long.  The  bulb  is  about  4  mm.  long 
and  2  mm.  in  diameter.  The  turns  of  the  arms  are  looser  and  make  a 
larger  angle  with  a  transverse  plane. 

The  outer  surface  of  the  plant  is  supplied  with  a  large  number  of 
sessile  globular,  glandular  trichomes,  similar  to  those  of  Utricularia, 
and  which  secrete  mucilage  {12  —  11).  The  trap,  whose  inner  surface 
is  most  complicated,  has  excited  the  wonder  of  all  who  have  busied 
themselves  with  this  object.  Darwin  referred  to  it  as  "a  contrivance 
resembling  an  eel-trap  though  more  complex."  Goebel  (1891)  re- 
marked of  it  that  "it  is  in  the  highest  degree  remarkable;  one  might  say 
of  it  that  it  is  constructed  with  over-weening  care  and  anxiety  so  as 


Chapter  VI  —  93  —  Genlisea 

to  allow  only  very  small  animals  to  enter  and  then  to  hold  them  ir- 
revocably".    This  remarkable   structure  is  as  follows. 

In  form,  the  bulb  and  tubular  neck  (the  tube)  may  be  compared  to 
a  chianti  flask.  Within  the  flask  there  are  two  ridges  (if  we  were 
speaking  of  an  ovary  they  would  be  called  placentae),  one  ventral  and 
one  dorsal,  extending  from  the  base  up  the  sides  about  two-thirds  the 
distance  to  the  neck  above  {12  —  10).  Within  the  tissue  of  the  ridges 
runs  in  each  a  branch  of  the  single  vascular  strand  arriving  from  the 
footstalk,  while  the  surface  bears  numerous  glands,  which  may  be  pre- 
sumed to  be  digestive  and  absorptive,  either  but  probably  both.  A 
few  additional  glands  are  to  be  found  on  the  rest  of  the  surface.  The 
two  vascular  strands,  each  of  a  single  spiral  vessel  accompanied  by  a 
thin  strand  of  phloem,  the  one  dorsal  and  the  other  ventral,  pass  up- 
ward from  the  bulb  into  the  walls  of  the  tube  without  change  of  di- 
rection. Near  the  mouth  of  the  tube  they  divide,  a  branch  from  each 
supplying  each  arm,  which  then  has  two  vascular  strands  quite  as  if  it 
were  a  closed  tube  branched  from  the  main  tube.  The  inner  surface 
of  the  tube  is  broken  up  into  a  series  of  some  forty  transverse  ridges 
each  formed  of  a  transverse  row  of  radially  thickened  cells,  each  of 
which  sends  downward  toward  the  flask  a  stiff  curved  trichome  {g  — 
8;  12  —  8,  9,  13).  Of  these  cells  there  are  about  50,  so  that  there  are 
that  number  of  slender  stiff  bristles  projecting  inward  and  downward 
from  each  ridge.  Each  section  of  the  tube  below  and  including  a 
transverse  ridge  is  therefore  of  the  form  of  the  entrance  to  an  eel  trap, 
or  lobster  pot,  if  you  will.  The  whole  tube,  0.13  to  0.42  mm.  inside 
diameter,  is  a  series  of  such  traps,  some  forty  to  fifty  in  number,  each 
with  its  funnel  extending  into  the  next  below.  In  addition  to  these 
downwardly  directed  hairs,  and  just  below  the  ridges  in  each  section 
there  are  one  or  two  transverse  rows  of  glandular  trichomes  {12  —  8, 
9,  16).  The  zone  where  these  occur  broadens  toward  the  outer  end 
of  the  tube  and  is  composed  of  wavy-walled  cells,  while  the  bristle 
bearing  cells  are  conspicuously  straight  and  narrow,  lengthwise  the 
tube. 

On  approaching  the  open  end,  the  tube  widens  somewhat,  and 
spreads  out  to  form  the  arms.  The  open  end  is  formed  of  the  upper 
and  lower  sides  to  form  two  lips,  the  upper  (ventral)  somewhat  shorter 
than  the  lower,  and  fixed  in  a  position  a  little  distance  apart  by  the 
ballooned  cells  above  mentioned  (prop-cells)  (77  —  1-4;  12  —  2,  3). 
These  are  closely  enough  placed  so  that  in  between,  alternating  with 
them,  a  series  of  funnels,  guarded  by  inward  pointing  hairs,  is  formed. 
This  is  repeated  along  the  open  slit  of  the  arm  (77  — ^11)  quite  to  the 
apex. 

In  passing  up  into  the  arms,  the  same  general  structure  described 
for  the  tube  is  repeated  {12  —  i,  4),  but  the  ridges  are  now  curved 
obhquely,  comformably  with  the  directions  and  amounts  of  growth 
(77  —  6,  9).  Along  the  edges  of  the  arm,  as  one  inspects  it  if  laid 
open,  the  ridges  run  almost  parallel  thereto,  each  ridge  beginning  in  a 
prop-cell.  Passing  obliquely  inward  and  forward  they  gradually  ap- 
proach the  other  edge  in  a  harmonic  curve.  When  past  the  middle  of 
the  arm  they  bend  rather  sharply  back  and  approach  a  direction  again 
parallel  to  the  other  edge  and  then  end  at  the  scar-like  depression 


Francis  E.  Lloyd  —  84  —  Carnivorous  Plants 

formed  by  its  prop-cell  at  the  other  end  {ii  —  6).  In  consequence  of 
this  development,  the  trapping  hairs  stand  approximately  at  right 
angles  to  the  edges  of  the  funnel  formed  by  the  prop-cells,  so  that  al- 
though oblique,  the  ridges  with  their  trapping  hairs  function  as  in  the 
straight  tube,  although  no  two  hairs  on  the  same  ridge  have  pre- 
cisely the  same  direction.  The  whole  structure  is  one  to  arouse  won- 
der in  the  observer. 

The  inner  surface,  except  that  occupied  by  the  bristle  ridges,  is 
made  up  of  wavy-walled  cells  with  scattered  glandular  hairs,  repeating 
again  the  structure  of  the  tube  (//  —  6).  The  funnel  shaped  mouths 
of  the  tube  and  arms  are  guarded,  outside  the  level  of  the  prop-cells, 
by  shorter  stiff er  hairs,  claw-like  in  shape  {12  —  12),  allowing  some 
room  for  the  entrance  of  prey,  but  nevertheless  inveigling  them  to- 
ward the  interior.  The  captures  consist  of  copepods,  and  the  like, 
small  water  spiders,  nematodes  and  plenty  of  other  forms,  many  of 
which  I  have  seen  in  the  Brazilian  material  studied. 

In  both  species  examined,  the  structure  is  the  same,  with  the  slight 
difference  that  the  large  African  species  structures  are  not  so  crowded 
and  in  consequence  are  easier  to  decipher. 

The  glands  are  all  of  the  same  type,  that  common  to  this  genus  and 
Utricularia,  consisting  of  a  basal  cell  anchored  in  the  epidermis,  a  short 
neck  cell,  and  the  capital  of  two  to  eight  cells.  It  is  wholly  a  matter 
of  speculation  as  to  the  function  of  these  glands.  They  may  supply 
only  mucilage  to  lubricate  the  interior  and  facilitate  the  movements  of 
prey  downwards  through  the  arms  and  neck,  or  they  may  secrete 
digestive  enzymes  or  both.  I  have  observed  that  prey  only  half  way 
down  the  tubular  neck  shows  signs  of  a  far  degree  of  disintegration, 
but,  as  bacterial  action  cannot  at  the  moment  be  excluded,  it  boots 
nothing  to  do  more  than  indicate  the  possibilities.  The  goal  of  prey  is 
the  flask  at  the  bottom  of  the  neck.  Here  one  finds  various  remnants 
of  the  animals,  copepods,  spiders,  nematodes,  together  with  algae. 

According  to  Goebel,  the  twisting  growth  of  the  arms  facilitates 
their  penetration  of  the  substrate  which,  being  filled  with  water,  is 
quite  loose.  This  explanation  does  not  help  for  the  trap  leaf  up  till  the 
time  when  the  arms  begin  to  form,  which  is  a  good  deal  more  than  half 
the  time  of  its  growth  activity.  If  teleological  interpretation  be  of  any 
use,  one  might  venture  that  the  twisted  form  of  the  arms  results  in  the 
presentation  in  all  direction  of  entrances  to  the  interior  so  that  prey 
find  openings  in  whatever  direction  they  may  approach. 

Literature  Cited: 

Benjamin,  L.,  Flora  Brasiliensis,  10:252,  1847. 

BuLLER,  A.  H.  Reginald,  Researches  on  Fungi,  Vol.  2,  1922. 

Darwin,  C,  Insectivorous  Plants.     2d.  ed.,  London  1875. 

Goebel,  K.,  Pflanzenbiologische  Schilderungen,  1891.     Zur  Biologic  von  Genlisea.     Flora 

77:208-212,  1893. 
St.  Hilaire,  A.  de,  Voyage  au  district  des  Diamans,  11:428,  1833. 
St.  Hilaire  &  F.  de  Girard,  Monographie  des  Primulacees  et  des  Lentibulariees  du  Bresil 

meridional  et  de  la  Republique  Argentine.     Mem.  Soc.  roy.  des  Sci.  etc.  d'Orleans  5, 

1840. 
TuTiN,  T.  G.,  New  Species  from  British  Guiana,  Cambridge  University  Expedition,  1933. 

Journ.  Bot.  1934:306-341. 
Warming,  Eug.,  Contribution  a  la  connaissance  des  Lentibulariaceae,  I.     Genlisea  ornata 

Mart.;    II.     Germination   des   graines   de   VUtricidaria   vulgaris.     Vidensk.    Medd.    f. 

Naturhist.  For.  Kj0benhavn  1874:33-58.     Resume  in  French  (appendi.x  8). 
Wright,  C,  in  Grisebach's  Catalogus  plantarum  Cubensium.     Leipzig,  1866. 


Chapter  VII 
BYBLIS 

Occurrence.  —  Appearance  and  systematic  position.  —  Habitat.  —  Structure.  —  Func- 
tions of  the  glands. 

Byhlis  is  a  genus  confined  to  western  Australia,  where  it  is  endemic. 
There  are  two  species,  B.  linifolia  Salisb.  and  B.  gigantea  Lindl.,  the 
latter  being  much  the  larger  plant,  one  about  50  cm.  tall.  It  is  a  half- 
shrub  in  habit,  consisting  of  a  woody  rhizome  bearing  in  any  one 
season  the  dying  parts  of  the  previous  and  the  growing  ones  of  the 
present  season  (zj  - — i).  These  consist  usually  of  a  single  chief  stem 
with  one  to  three  branches  from  near  the  base,  all  bearing  long  (1-2 
dm.)  linear  leaves,  clothed  with  numerous  stalked  mucilage  glands. 
The  color,  a  yellow-green,  is  characteristic,  and  the  surface  is  charged  with 
numerous  ghstening  mucilage  droplets.  The  flowers,  raised  on  axillary 
peduncles,  are  violet  or  rose  colored,  have  a  deeply  five  lobed  rotate 
corolla,  which  appears  superficially  as  pol}^etalous,  the  lobes  alter- 
nating with  five  oval  attenuate  sepals  and  with  the  five  stamens.  The 
systematic  position  of  this  plant  has  not  been  at  all  clear.  Planchon 
(1848)  and  Bentham  (Flora  australiensis  2:469)  believed  that  it  is  re- 
lated to  the  Pittosporaceae  rather  than  to  the  Droseraceae.  Later 
Lang,  stressing  too  much  its  sympetaly,  advanced  reasons  for  its  re- 
lation to  Pinguicula  and  its  inclusion  within  the  Lentibulariaceae,  while 
more  recently  Domin  (1922)  has  placed  it  in  a  new  family,  the  Bybli- 
daceae,  of  which  B.  linifolia  is  the  type. 

Byhlis  gigantea  was  found  growing  abundantly  in  sandy,  swampy 
places  in  the  Swan  River  district  not  far  from  Perth,  where  also  are 
to  be  found  very  characteristic  species  of  Polypompholyx,  (P.  tenella 
and  multifida)  and  the  peculiar  Australian  species  of  Utricularia,  U. 
Menziesii,  Hookeri,  etc.,  and  all,  except  Polypompholyx  tenella,  confined 
to  W.  Australia.  Byhlis  gigantea  is,  however,  to  be  found  in  drier  and 
better  drained  parts  of  such  swamps,  as  for  example  at  Cannington 
where  it  grows  around  the  base  of  a  low  hillock  on  which  stood  a  house, 
and  not,  as  Ross  suggests,  in  very  wet  places  on  the  banks  of  streams. 
The  substrate  was  a  coarse  quartz  sand  with  some  admixture  of  fine 
white  or  yellow  clay,  and  little  humus.  Specimens  of  Byhlis  linifolia 
were  received  from  N.  E.  Arnhem  Land  where  it  was  found  growing 
"around  rocky  pools  in  the  bed  of  a  river". 

The  stem  arises  from  a  slender  rhizome  with  triarch  (Lang)  or,  as 
I  have  observed,  diarch  roots  often  showing  a  considerable  degree  of 
secondary  thickening  with  a  thick  cortex  loaded  with  starch  and  tannin- 
emulsion-colloid  (Lloyd  191  i).  Both  of  these  may  be  regarded  as 
storage  material.  From  the  perennating  rootstock  arises  the  new  an- 
nual stem  with  its  appendages,  which  are  secondary  branches,  leaves 
and  long  peduncled  flowers.  All  these  parts  are  clothed  with  two  kinds 
of  glands,  sessile  and  stalked.  In  aU  parts  except  the  sepals,  the 
epidermis  is  composed  of  elongated  straight-walled  cells,  all  of  which 


Francis  E.  Lloyd —96— Carnivorous  Plants 

in  young  organs  lie  at  the  same  level.  With  maturity,  the  epidermis 
becomes  ribbed  with  sunken  furrows  between  the  ribs.  The  floor  of 
the  furrow  is  composed  of  a  double  row  of  shorter  cells,  each  pair 
bearing  a  sessile  gland  (74  —  10,  13).  In  scattered  positions  occur 
stalked  glands  which  secrete  abundant  mucilage.  In  the  sepals  the 
epidermal  cells  are  wavy-walled  on  both  surfaces,  less  so  on  the  outer 
(lower)  surface  toward  the  base.  On  the  outer,  dorsal  face  of  the  leaf 
occur  both  sessile  and  stalked  glands,  the  latter  very  numerous,  on  the 
inner  face  only  sessile  glands  occur  (p  — 9).  Stalked  glands  are  to  be 
found  even  on  the  ovary  wall.  Stomata  occur  on  both  faces  of  the 
sepals,  and  on  the  leaves  and  stem  they  are  to  be  found  interrupting 
the  rows  of  sessile  glands  {14  —  13).  They  are  somewhat  raised  and 
extend  considerably  above  the  ditch  bottom.  In  this  way  according  to 
Fenner  the  stomatal  pore  does  not  become  clogged  with  the  secretion 
of  the  sessile  glands,  which  probably  fills  that  reach  of  the  ditch  oc- 
cupied by  them. 

The  leaves  are  long,  slender  and  linear  in  form,  tapering  toward 
the  apex.  When  in  the  bud  they  display,  in  the  case  of  B.  gigantea, 
no  circination,  the  apices  showing  only  a  very  meagre  outward  curva- 
ture, if  any.  In  B.  Hnifolia,  however,  the  leaves  are  outwardly  cir- 
cinate,  as  in  Drosophyllum.  This  somewhat  surprising  fact  was  clearly 
seen  in  the  material  from  Arnhem  Land  sent  me  by  my  friend  Mr. 
Charles  Barrett,  and  figured  in  14  —7.  B.  gigantea  is  seen  in  14  — 
8.  Of  this  DiELS  (1930)  says  merely  that  the  leaves  are  spirally  in- 
rolled  at  the  tip. 

In  transverse  section  the  leaves  are  triangular  with  round  angles 
{14  —  11).  Toward  the  tip  they  become  nearly  cylindrical  and  the  tip 
itself  is  somewhat  enlarged  to  form  a  knob,  properly  interpreted  to  be 
a  hydathode  (Lang,  Fenner).  Its  interior  is  occupied  by  a  large 
mass  of  tracheidal  tissue  in  contact  with  and  ending  the  vascular 
strand  which  reaches  thereto.  One  or  two  protuberant  stomata  are  to 
be  found  at  the  apical  surface,  not  by  any  means  always  at  the  extreme 
apex,  together  with  both  stalked  and  sessile  glands.  The  rigidity  of 
the  leaf,  which  is  very  slender  for  its  length,  is  attained  by  the  very 
thick-walled  epidermis  and  the  strands  of  mechanical  tissue  accom- 
panying the  vascular  bundles.  Beneath  the  epidermis  on  all  sides 
there  is  a  thick  layer  of  chlorenchyma  in  which  there  is  no  sharp  de- 
markation  between  palisade  and  spongy  tissue.  All  of  the  cells  are 
oval  rather  than  columnar  and  lie  in  three  courses.  Beneath  the 
epidermis  the  palisade  cells  have  expanding  ends  in  contact  with  it 
{14  —  9,  10).  This,  Fenner  explains,  ensures  a  contact  for  lively 
diffusion  between  the  glands  and  the  vascular  system.  The  upper  leaf 
surface  is  rather  flat,  with  a  very  shallow  depression  along  the  middle. 
On  this  surface  there  are  very  few  stalked  glands,  which  on  the  lower 
surface  are  very  numerous.  Sessile  glands  are  as  numerous  here  as 
elsewhere  {g  —  9) . 

The  sessile  gland  {14  —  10,  13)  stands  upon  a  pair  of  epidermal 
cells,  and  consists  of  a  capital  of  eight  radially  disposed  cells,  supported 
on  a  single  very  short  stalk  cell,  this  resting  on  two  short  epidermal 
cells,  which  according  to  Fenner  originate  from  a  single  basal  cell  of 
the  very  young  trichome.    The  furrow  in  which  the  sessile  glands  stand 


Chapter  VII —97— Byblis 

is  sufficiently  deep  and  narrow  so  that  the  sides  of  the  glands  lean 
against  and  are  supported  by  the  sides  of  the  furrow. 

The  stalked  gland  (14  —  12-15)  has  a  capital  of  usually  32  cells 
radiating  from  the  centre  and  standing  out  like  an  umbrella  top.  These 
cells  all  abut  on  a  central  short  cell  resting  on  the  top  of  the  long  stalk 
cell.  This  in  turn  stands  on  a  group  of  basal  cells  which  may  be  as 
many  as  eight  in  number,  or  as  few  as  two  in  the  case  of  a  small 
stalked  gland.  The  latter  may  also  have  as  few  as  four  cells  in  the 
capital,  the  mature  glands  showing  no  great  degree  of  uniformity  in 
this  regard.  The  stalk  cells  of  the  larger  glands  have  strongly  striated 
thick  cellulose  walls,  the  striations  reaching  deeply,  as  far  as  the  cuticle. 
These  striations  run  obliquely  (as  in  the  cotton  fiber)  and  when  the 
gland  dries  (in  air  or  alcohol),  the  stalk  cells  twist,  as  noted  by  Dar- 
win {14  —  14).  Fenner  regards  this  arrangement  as  one  to  allow 
bending  of  the  trichome  without  collapse. 

While  the  gland  capitals  are  covered  with  a  thin  cuticle  there  is 
access  by  diffusion  through  pores,  mentioned  but  not  described  by 
Fenner.  I  found  them  (19336)  to  be  rather  large  oval  openings  ar- 
ranged in  a  circle  about  and  some  distance  away  from  the  centre  of  the 
capital.  They  become  evident  on  treatment  of  the  stalked  glands  with 
sulfuric  acid  {14  —  12).  Both  the  sessile  and  stalked  glands  are 
readily  penetrable  by  dyes  (methylene  blue). 

Our  earlier  knowledge  of  the  function  of  the  glands  bearing  on  the 
question  of  the  carnivorous  habit  of  the  plant  we  have  at  the  hands  of 
A.  NiNiAN  Bruce  (1905).  Her  work  is  clearly  indicative  of  this,  but 
the  question  needs  further  investigation,  which  in  this  type  of  plant  is 
not  easy.  Bruce  placed  minute  cubes  of  coagulated  egg-albumen  in 
contact  with  the  sessile  glands,  and  after  a  period  of  some  days  (two 
to  eight)  the  whiteness  has  completely  disappeared.  During  the 
progress  of  digestion  the  round  white  core  of  the  cube  of  albumen  could 
be  observed  to  suffer  gradual  reduction  in  size.  This  material  placed 
in  contact  with  the  heads  of  stalked  glands  failed  to  show  any  evi- 
dence of  digestion,  but  when  removed  and  placed  in  contact  with  the 
sessile  glands  promptly  did  so.  This  seems  to  indicate  that  bacterial 
action  does  not  supervene.  Some  observations  by  Fenner  justify 
Bruce's  results.  When  insects  are  caught,  he  says,  and  come  in  contact 
with  the  sessile  glands,  a  secretion  is  thrown  out  by  them  which  is 
much  less  viscous  than  that  of  the  stalked  glands.  After  four  to  six 
hours,  the  group  of  glands  affected  again  become  dry  and  an  examina- 
tion of  them  shows  that  the  contents  of  the  gland  cells  and  even  of 
the  stalk  cells  betray  evidence  of  absorption  in  the  presence  of  a  greater 
density  of  the  protoplasm  and  the  presence  of  large  rounded  dark 
masses.  These  changes  are  not  to  be  observed  in  the  stalked  glands, 
which  do  nothing  else  than  secrete  mucilage.  I  attempted  to  prove 
the  matter  for  myself  at  Perth,  W.  AustraHa.  Byblis  appeared  late  in 
the  season,  during  the  latter  part  of  my  visit,  so  that  I  had  only  lim- 
ited time  at  my  disposal.  My  method  consisted  in  placing  minute 
fragments  of  carmine  fibrin  in  contact  with  the  glands  of  the  living 
leaf,  on  the  plant,  and  in  a  small  vial  with  a  dozen  short  pieces  of  leaf 
with  and  without  a  little  added  water,  with  and  without  added  weak 
HCl,  and  with  and  without  ammonium  nitrate.     The  results  were  en- 


Francis  E.  Lloyd —98— Carnivorous  Plants 

tirely  negative,  even  after  two  weeks,  though  there  was  at  length  a  dis- 
tinct and  unpleasant  odor  emitted. 

I  first  learned  from  Mr.  A.  G.  Hamilton  that  Byblis  harbours  a 
small  insect  which  he  called  a  ''buttner".  In  Perth  I  received  the 
same  information  from  Mr.  H.  Stedman,  who  kindly  took  me  to  a 
locality  at  some  distance  north  of  Perth  where  we  found  a  lot 
of  plants  growing.  All  of  these  were  infested  with  a  small  wingless 
capsid  which  turns  out  to  be  a  new  genus  and  will  be  described  by 
Dr.  W.  R.  China  of  the  British  Museum  (Natural  History)  {13 — i). 
While  small  insects  in  general  are  caught  by  the  mucilage  secreted  by 
the  stalked  glands,  this  capsid  moves  about  freely  without  difficulty, 
just  as  do  similar  insects,  also  capsids,  over  the  surface  of  Drosera 
leaves  in  Australia,  and  of  the  African  genus  Roridula,  once  thought 
to  be  carnivorous.  How  the  insect  manages  this  is  a  bit  puzzling.  It 
is  noticeable  that  it  prefers  to  walk  on  the  upper  leaf  surface  where 
there  are  very  few  and  usually  smaller  glands  but  when  alarmed  it 
progresses  rapidly  in  any  direction  without  becoming  entangled  with 
the  mucilage.  Full  sized  insects  are  perhaps  too  big  to  be  readily  en- 
cumbered, but  the  smaller  ones  move  about  just  as  freely.  Their  food 
consists  of  freshly  captured  flies,  the  juices  of  which  they  suck,  the  re- 
lation of  insect  and  plant  affording  a  sort  of  commensalism,  but  this 
term  could  hardly  be  used  in  the  case  of  Roridula  (non-carnivorous) 
the  secretion  from  whose  glands  is  resinous  (Lloyd  1934). 

Literature  Cited: 

Bruce,  A.  Ninian,  On  the  activity  of  the  glands  of  Byblis  gigantea.     Notes  Roy.  Bot.  Gar- 
den Edin.  16:9-14,  1905,  also  17:83,  1907. 
DiELS,  L.,  Byblidaceae,  Nat.  Pfianzenfamilien.  i8a.  1930. 
DoMiN,  K.,  Byblidaceae,  a  new  archichlamydeous  family.     Contr.   to  the  Australian  flora, 

undated,  but  about  1920.     Extracted  from  MS.  and  published  separately  in  Acta  Bot. 

Bohem.  1:3-4,  1922. 
Fenner,  see  under  Nepenthes. 
Hamilton,  A.  G.,  Notes  on  Byblis  gigantea.     Proc.  Linn.   Soc.  New  South  Wales  28:680- 

684,  1903. 
Lang,  F.  X.,  Untersuchungen  iiber  Morphologie,  Anatomic  und  Samenentwickelung  von 

Polypompholyx  und  Bvblis  gigantea.     Flora  88:3-60,  1901. 
Llo\T),  F.  E.,  The  tannin-colloid  complexes  in  the  fruit  of  the  persimmon.  Biochem.  Journ. 

1:7-41  (pi.  1-3),  191 1. 
Lloyd,  1933  (see  under  E eliamphora) . 
Lloyd,  1934  {see  under  Introduction). 
Planchon,  J.  E.,  Sur  la  famille  des  Droseracees.    Ann.  sci.  nat.  bot.,  3  ser.,  9:79-99,  1848. 

(Contains  also  descriptions  of  Drosera  carpels  bearing  tentacles,  these  being  intergrades 

between  normal  leaves  and  carpels). 
Ross,  H.,  Byblis  gigantea.     Gartenflora  51 :337-339  (pl-  15°°),  1902. 


Chapter    VIII 

DROSOPHYLLUM  LUSITANICUM 

Drosophyllum  lusilanicum  Lk.  (jj  —  2)  is  a  plant  with  much  the  ap- 
pearance of  Byblis,  but  it  is  larger  and  shrubbier  (1-1.6  m.  tall)  and  is 
unusual,  for  the  carnivorous  plants,  in  growing  not  in  a  wet,  but  in  a 
very  dry  habitat  in  Morocco  and  nearby  Portugal  and  Spain.  Harsh- 
BERGER  visited  a  locahty  in  Sra.  de  Valongo  near  Oporto,  where  he 
found  Drosophyllum  growing  in  open  formations,  scattered  over  the 
quartz-rocky  soil.  He  observed  its  leaves  to  be  crowded  with  small 
gnats.  Its  flowers  are  bright  sulphur  yellow,  are  i-i>^  inches  in 
diameter,  and  have  convolute  aestivation.  It  is  called  locally  "herba 
piniera  orvalhada"  (dewy  pine)  in  allusion  to  its  bedewed  appearance 
due  to  the  numerous  glands  carrying  large  droplets  of  clear  mucilage. 
The  base  is  strongly  woody,  and  its  abundant  roots  penetrate  deeply 
into  the  dry  soil.  "Mr.  W.  C.  Tait  informs  me  that  it  grows  plenti- 
fully on  the  sides  of  dry  hills  near  Oporto,  and  that  vast  numbers  of 
flies  adhere  to  the  leaves.  The  latter  fact  is  well  known  to  the  vil- 
lagers, who  call  the  plant  the  'fly-catcher,'  and  hang  it  up  in  their 
cottages  for  this  purpose"  wrote  Darwin  (1875).  Inquiry  by  corre- 
spondence with  Dr.  QuiNTANiLHA  has  elicited  doubt  of  the  correctness 
of  Tait's  statement  as  to  the  use  by  the  paisanos  of  the  plant  as  a 
fly-catcher,  though  it  seems  reasonable  enough. 

The  leaf  is  linear  with  a  deep  furrow  along  the  upper  side.  It 
is  traversed  by  three  vascular  bundles,  a  median  and  two  lateral,  arising 
from  a  single  bundle  entering  at  the  base  {14  —  5). 

A  peculiar  feature  is  found  in  the  reverse  circination  (14  — 4)  the 
rolled  leaf-tip  facing  outwardly  while  in  Drosera  very  generally  the 
opposite  holds.  Although  in  Byblis  gigantea  the  leaves  are  nearly 
straight,  showing  no  evident  circination,  in  Byblis  linifolia  the  be- 
havior is  like  that  of  Drosophyllum.  Fenner  expresses  the  opinion 
that  this  arrangement  has  its  significance  in  permitting  the  free  de- 
velopment of  the  stalked  glands,  but  he  overlooks  the  fact  that  the 
circination  of  Drosera  is  in  the  opposite  sense  without  any  prejudice 
to  the  development  of  the  tentacles.  The  case  of  Byblis  linifolia  was 
not  known  to  him.  In  any  event,  in  the  tight  coils  the  dorsal  and 
ventral  leaf  surfaces  are  mutually  compressed;  and  assuming  that  the 
tentacles  (hairs  in  the  case  of  Byblis)  develop  after  uncoiling,  the  ven- 
tral (upper)  surface  is  freer  than  the  dorsal,  where  the  most  of  the 
tentacles   or  hairs  are   to   be   found. 

Another  characteristic  behavior  of  the  leaves  is  their  marcescence. 
Instead  of  falling  away  as  they  die,  they  remain  attached,  forming  a 
grass-skirt  about  the  stem.  Franca  (1922)  regarded  this  as  a  symptom 
of  a  condition  which  he  regarded  as  pathological,  due  to  overnutrition 
and  the  inability,  because  of  the  absence  of  an  excretory  apparatus,  to 
throw  off  waste.  Quintanilha,  however,  disagrees  with  this  and,  in 
our  opinion,  justly. 


Francis  E.  Lloyd  —  100  —  Carnivorous  Plants 

In  the  seedling,  the  cotyledons  withdraw  from  the  seed  during 
germination  and  develop  into  broadly  linear  tapering  members,  sup- 
plied with  glands  enabling  them  to  capture  prey  (Franca). 

The  leaf  bears  two  kinds  of  glands,  stalked  mucilage  glands  and 
sessile  digestive  glands  {14 —  i,  2,  6).  Their  position  is  determined  if 
at  all  only  to  a  sHght  extent  by  the  three  vascular  bundles,  from 
which,  however,  they  receive  branchlets  ending  at  the  bases  of  the 
glandular  tissues.  There  are  three  double  files  of  stalked  glands,  one 
along  each  leaf  margin,  roughly  speaking,  and  two  rows  along  the 
under  leaf  surface,  one  on  each  side  of  the  midvein.  The  sessile  glands 
are  more  scattered,  and  apparently  only  in  some  degree  determined  in 
position  by  the  vascular  tissues.  Sessile  glands  occur  on  both  upper 
and  under  leaf  surface,  stalked  glands  only  on  the  under  surface  and 
along  the  margins. 

Structure  of  the  glands.  —  Drosophyllum  differs  from  Byblis  in  that 
the  glands,  instead  of  being  trichomes,  are  emergences,  and,  as  Darwin 
pointed  out,  have  much  the  same  structure  as  those  of  Drosera,  with- 
out, however,  being  endowed  with  the  power  of  movement.  This 
refers  of  course  to  the  stalked  glands.  These  have  a  stout  stalk  sur- 
mounted by  a  large  nearly  hemispherical  capital,  and,  as  Darw^in  put 
it,  have  the   "appearance  of  miniature  mushrooms." 

The  capital  {14  —  2)  consists  of  three  courses  of  cells  running 
parallel  with  the  outer  surface.  The  outer  of  these,  the  epidermis,  is  of 
rather  thick,  wavy-walled  cells,  with  strong  buttress  thickenings,  stiffen- 
ing the  angles  of  the  radial  walls  {14  —  3).  The  dense  protoplasmic 
contents  and  prominent  nuclei  speak  for  their  glandular  activity. 
These  are  covered  with  a  cuticle,  which  according  to  Fenner  is  finely 
porous,  thus  permitting  the  exudation  of  the  mucilaginous  secretion. 
I  have  not  succeeded  in  convincing  myself  that  the  pores  are  optically 
demonstrable,  but  it  is  certain  that  the  cuticle  offers  no  impediment  to 
the  diffusion  of  methylene  blue,  for  less  than  a  minute's  exposure  to  a 
watery  solution  of  this  dye  results  in  the  deep  staining  of  the  whole 
capital  while  the  dye  does  not  penetrate  the  remaining  epidermis  at 
all.  Meyer  and  Dewevre  also  failed  to  see  the  pores  but  demon- 
strated on  kiUing  the  escape  through  the  cuticle  of  the  pigment  which 
renders  the  gland  conspicuous.  They  found  also  that  lithium  nitrate 
taken  up  through  the  roots  is  found  12  hours  later  in  the  mucilaginous 
secretion.  The  cells  of  the  second  course  underlying  the  epidermis  are 
somewhat  more  irregular  in  form,  but  are  likewise  provided  with  but- 
tress-thickenings in  the  radial  walls,  though  they  are  not  so  numerous 
and  prominent  as  in  the  epidermal  cells.  The  general  character  of 
these  two  courses  is  the  same;  they  were  called,  by  Penzig  (1877),  the 
secretion-layer.  Underlying  these  two  courses  is  a  third,  of  flat  cells, 
of  greater  size  in  the  transverse  direction  (with  reference  to  the  axis  of 
the  gland)  with  their  contiguous  radial  walls  strongly  cuticularized,  so 
that  in  a  cleared  preparation  when  suitably  stained,  as  with  congo  red, 
one  sees  a  strong  network  lying  within  the  capital.  Contrary  to  an 
earlier  view  (Solereder  1899,  p.  367)  not  the  entire  but  only  the 
radial  walls  are  cuticularized,  thus  (Goebel  1891)  leaving  a  free 
diffusion  passage.  This  feature  is  held  in  common  with  other  gland- 
ular structures  described  elsewhere. 


Chapter  VIII  —  101  —  DrosophyUum 

The  third  layer  (limiting  layer  of  Penzig)  caps  a  mass  of  short 
irregular  tracheids  constituting  the  expanded  end  of  a  strand  of  vas- 
cular tissue  extending  through  the  stalk  and  communicating  with  the 
vascular  tissues  of  the  leaf.  This  strand  consists  of  both  xylem  and 
phloem  elements  (Fenner  contra  Meyer  and  Dew-eyre)  affording, 
according  to  Fenner,  not  only  a  pathway  for  water  but,  in  the  case  of 
the  phloem,  for  the  transmission  of  stimuli  to  the  neighboring  sessile 
glands,  which  have  been  shown  to  show  secretory  activity  in  response 
to  such  stimulus  received  from  the  stalked  glands.  The  stalk  itself  is 
made  up  of  the  epidermis  and  an  underlying  course  of  parenchyma,  sur- 
rounding the  vascular  strand.  The  capping  secreting  cells  contain 
brilHant  red  coloring  matter,  interpreted  as  an  optical  lure  for  insects, 
and  when  the  capital  bears  its  shining  droplet  of  clear  mucilage,  which 
acts  as  a  Hght  collecting  lens,  the  glands  appear  as  brilUiant  red  dots. 
The  sessile  glands  have  no  such  coloring  matter.  These  {14  —6)  have 
the  same  structure  as  the  stalked  glands,  differing  only  in  the  absence 
of  the  stalk.  Occasionally  an  intergrading  condition  is  met  with; 
Goebel  found  one  such,  with  a  very  short  stalk.  The  sessile  glands 
are  usually  oval,  generally  smaller,  and  have  a  less  extensive  contact 
with  the  vascular  system.  Each  gland,  however,  is  underlaid  by  a 
group  of  cavernous  looking  tracheidal  cells,  with  no  protoplasmic  con- 
tent, evidently  an  important  part  of  the  gland  but  with  what  function 
we  do  not  know.  If  Fenner  saw  this  feature,  he  regarded  it  as  the 
end  of  the  tracheidal  system.  For  there  is  also  to  be  found  at  the  base 
of  each  gland  the  end  of  a  branch  of  the  vascular  system.  These 
glands  are  devoid  of  a  mucilaginous  secretion,  as  of  coloring  pigment 
and  even  of  chlorophyll,  for  they  appear  whitish. 

The  mucilage  secreted  by  the  stalked  glands  is  peculiar,  in  that  it 
is  not  readily  drawn  out  into  slender  viscous  threads,  but  is  easily 
pulled  off  the  gland  by  a  touch  of  even  a  needle  point  as  Darwin  ob- 
served. "From  this  peculiarity,  when  a  small  insect  alights  on  a  leaf 
of  DrosophyUum,  the  drops  adhere  to  its  wings,  feet  or  body,  and  are 
drawn  from  the  gland;  the  insect  then  crawls  onward  and  other  drops 
adhere  to  it;  so  that  at  last,  bathed  by  the  viscid  secretion  it  sinks 
down  and  dies,  resting  on  the  small  sessile  glands  with  which  the  sur- 
face of  the  leaf  is  thickly  covered"  (Darwin,  1875,  2nd  ed.,  p.  271). 
The  secretion  of  mucilage  continues  after  removal  and  Darwin 
found  that  when  a  plant  is  kept  under  a  bell  glass  to  prevent  evap- 
oration the  secretion  is  produced  in  such  quantities  as  to  run  down 
the  leaf  surface  in  droplets;  and  further  that  the  secretion  shows  an 
acid  reaction.  Goebel  found  that  among  the  possible  acids  pres- 
ent formic  acid  is  one,  and  believed  that  this  is  effective  in  pre- 
venting bacterial  action.  Emanating  from  these  glands,  probably,  is 
an  odor  which  Goebel  likened  to  that  of  honey,  which  would  be  at- 
tractive to  insects  and  thus  act  as  a  lure. 

In  the  case  of  many  carnivorous  plants  "overfeeding"  usually  re- 
sults in  the  damage  and  death  of  the  leaf  wholly  or  locally,  notably  in 
the  pitcher  plants.  This  has  not  been  observed  to  occur  in  Drosophyl- 
lum,  and  may  be  accounted  for  by  the  inhibition  of  bacterial  action  as 
just  indicated. 

The    sessile    glands    do    not   exude    a    secretion    unless   stimulated 


Francis  E.  Lloyd  —  102  —  Carnivorous  Plants 

(Darwin,  Goebel,  Fenner,  Quintanilha).  The  secretion  appears 
normally  when  the  mucilage  glands  are  stimulated  by  the  catching  of 
prey,  but  not  merely  mechanically,  as  by  placing  on  them  sand  grains, 
bits  of  paper,  etc.  Fenner  showed  in  considerable  detail  by  appropri- 
ate experiments  that  the  maximum  activity  of  the  sessile  glands  is  ob- 
tained when,  after  the  stalk  glands  nearby  have  received  prey,  both 
prey  and  mucilage  secretion  are  brought  into  contact  with  them.  But 
in  the  presence  of  mucilage  removed  from  the  stalked  glands  and  mixed 
with  the  juices  of  prey,  leaving  the  stalked  glands  unstimulated,  the 
sessile  glands  work  only  slightly  if  at  all.  Fenner  concluded  that  the 
maximum  activity  of  the  sessile  glands  is  called  forth  by  something 
passing  through  the  tissues  by  way  of  the  vascular  elements  (phloem). 
The  sessile  and  stalked  glands  must,  therefore,  be  considered  as  a  single 
mechanism  in  which  one  part  is  dependent  on  the  other. 

There  is  a  general  agreement  on  the  part  of  the  authors  mentioned 
that  Drosophyllum  exercises  its  own  proper  power  of  digestion,  and  that 
this  is  not  the  result  of  bacterial  activity.  As  mentioned  already, 
Goebel  regarded  digestion  as  too  rapid  for  bacterial  action,  and  that  the 
presence  of  formic  acid  excludes  such  activity,  and  though  he  was 
unable  to  state  the  concentration  of  acid  present,  he  supports  his  in- 
ference by  inoculating  nutrient  gelatine  plates  with  negative  results. 
The  activity  of  formic  acid  may  not,  however,  Goebel  adds,  be  con- 
fined to  that  of  an  antiseptic,  but  it  may  consist  in  an  initial  dis- 
solution of  the  proteins  of  the  body  of  the  prey,  with  the  escape  of 
materials  v/hich  then  affect  the  sessile  glands  and  stimulate  them  to 
greater  activity. 

Darwln  found  that  fragments  of  egg  albumen,  fibrin,  were  acted 
upon  rapidly  when  they  came  in  contact  with  the  sessile  glands.  If 
only  in  contact  with  the  stalked  glands,  they  were  not  attacked.  If 
then  placed  on  the  sessile  glands,  there  was  a  copious  secretion,  and 
the  albumen  was  completely  dissolved  in  7  to  22  hours.  "We  may 
therefore  conclude,  either  that  the  secretion  from  the  tall  glands  has 
Httle  power  of  digestion,  though  strongly  acid,  or  that  the  amount 
poured  forth  from  a  single  gland  is  insufficient  to  dissolve  a  particle  of 
albumen  which  within  the  same  time  would  have  been  dissolved  by  the 
secretion  from  several  of  the  sessile  glands."  Fibrin  likewise,  when 
placed  on  the  stalked  glands,  was  not  attacked,  though,  as  in  the  case 
of  albumen,  the  secretion  was  absorbed  (together  with  whatever  es- 
caped into  it  from  the  fibrin).  But  when  the  fibrin  was  slipped  onto 
the  sessile  glands,  digestion  proceeded  rapidly  (17  to  21  hours)  with  an 
abundant  exudation  of  fluid  from  the  glands.  Darwin  thought  the 
digestion  more  rapid  than  in  Drosera.  He  had  not  excluded  the  action 
of  bacteria,  which,  however,  as  above  said,  Goebel  did  by  suitable 
culture  experiments.  He  observed  a  more  rapid  action  than  did 
Darwin.  A  fibrin  flock  i  cm.  long  and  one-fourth  the  width  of  the 
leaf  was  noticeably  attacked  in  a  half-hour  on  a  warm  summer  day, 
and  in  an  hour  no  trace  could  be  seen,  though  the  spot  had  been  care- 
fuUy  marked  by  a  bit  of  paper.  With  a  lens  small  fragments  could 
still  be  seen.  A  true  digestion,  he  concluded,  is  therefore  present.  The 
enzyme  is  secreted  in  response  to  a  special  stimulus,  and  chiefly,  if  not 
exclusively,  by  the  sessile  glands.  The  stalked  glands  are  chiefly  a 
trapping  apparatus  (Goebel  1891). 


Chapter  VIII  —  103  —  Drosophyllum 

In  1894  came  Meyer  and  Dewevre.  They  managed  to  collect  1.6 
grams  of  mucilage  and  investigated  it.  It  was  stiff,  clear,  had  the  odor 
of  honey  and  was  strongly  acid.  It  contained  no  free  reducing  sugar, 
but  on  heating  with  HCl  it  reduced  Fehling,  and  gave  a  weak  red 
color  with  thymol  and  H2SO4  (indicating  polysaccharides).  The 
presence  of  a  sugar  was  indicated  by  a  yellow  coloration  with  chlor- 
zinc-iodide  as  also  its  precipitation  by  lead  acetate,  by  barium  hydrox- 
ide and  by  alcohol.  No  proteins  were  present.  It  was  poor  in  salts, 
only  Ca  being  present.  No  K,  phosphates  or  nitrates  were  found. 
The  acidity  was  due  to  a  non-volatile  acid,  and  not  to  formic  acid,  as 
Goebel  had  held.  These  authors  verified  Darwin's  observation  that 
the  sessile  glands  secrete  only  on  stimulus  by  a  protein.  Insects  are 
attracted  both  by  the  odor  and  by  the  gHstening  of  the  droplets  of 
mucilage.  They  recorded  observations  also  which  indicate  that  there 
are  two  periods  of  activity  in  the  plant,  (i)  From  the  beginning  of 
vegetative  activity  to  the  beginning  of  seed  ripening  (from  Jan.  15  to 
May  15,  in  the  greenhouse).  During  fruit  ripening  the  leaves  begin 
dying  from  apex  to  base  and  the  glands  do  not  secrete  vigorously.  The 
soil  must  be  kept  "dry"  during  this  period.  (2)  After  fruit  ripening  is 
complete  (Aug.  i  to  Oct.  15)  secretion  and  odor  are  both  strong,  es- 
pecially in  sunny  weather.  The  experience  of  Darwin  was  again  sub- 
stantiated in  finding  that  coagulated  egg  albumen,  meat  and  fibrin 
were  acted  upon,  especially  if  well  smeared  with  mucilage  and  placed 
on  the  sessile  glands.  The  time  necessary  for  complete  digestion  was 
about  the  same  as  in  Darwin's  experience.  Goebel's  figures  were 
criticised  as  being  too  low  but  an  error  of  proofreading  may  have 
crept  in,  rather  than,  as  is  suggested,  incorrect  observation.  It  was 
found  that  very  small  fragments  of  albumen  were  attacked  in  the 
mucilage  of  a  stalked  gland  and  completely  digested  in  7  days.  If  large 
bits  were  imposed,  they  absorbed  the  mucilage,  and  damage  might  re- 
sult to  the  gland  in  consequence.  No  diastase  was  found.  Bacteria 
were  never  found  and  it  was  clear  that  the  mucilage,  as  Goebel  said, 
is  antiseptic. 

Franca  (1925)  gave  a  general  account  of  the  plant,  and  studied 
especially  the  cytological  changes  which  he  observed  in  the  glands 
during  digestion  and  absorption,  using  both  Hving  material  viewed 
microscopically,  and  fixed  material  stained  with  iron  haematoxyhn  and 
fuchsine,  etc.  He  found  evidence  that  the  two  courses  of  the  glandular 
cells  (the  outer  and  second)  have  different  functions,  that  the  outer 
course  is  secretory  only,  the  inner  both  secretory  and  absorptive.  The 
sessile  glands  have  only  the  power  of  secretion.  This  evidence  con- 
sists in  the  cytological  appearances  observed  during  digestion  and  ab- 
sorption. Changes  of  the  bright  red  color  in  the  glands  to  a  deeper, 
much  darker  shade,  had  been  noted  by  Darwin.  When  such  glands 
are  examined,  the  cells  of  the  outer  layer  of  the  gland  are  seen  to  have 
remained  unchanged,  while  those  of  the  second  layer  are  now  charged 
with  large  black  granules.  These  rise  to  a  maximum  some  hours  after 
the  glands  have  been  suppKed  with  muscle  fiber.  Some  similar  granules 
are  found  also  in  the  more  distal  short  cells  of  the  stalk  of  the  gland 
and  finally  in  approximate  leaf  tissues.  Such  dark  granules  are  seen 
when  an  insect  has  been  captured,  but  only  in  the  deeper  gland  cells. 


Francis  E.  Lloyd  —  104  —  Carnivorous  Plants 

With  neutral  red  the  protoplasm  displays  a  great  number  of  small  red 
granules,  considered  to  be  granules  of  secretion.  On  the  other  hand 
the  deeper  cells  are  filled  with  voluminous  granulations  of  dark  red 
color.  In  this  way  it  is  supposed  that  the  power  of  absorption  is 
demonstrated,  for  when  prey  has  been  captured,  the  superficial  cells 
show  only  the  small  granules,  while  the  deeper  cells  and  the  distal 
stalk  cells  are  at  the  same  time  found  crowded  with  grey  or  black 
granules  in  addition  to  the  secretory  granules  seen  also  in  the  outer  cell 
layer.  The  recounted  facts  are  held  to  support  Fran^a's  conclusion 
that  the  outer  glandular  layer  of  cells  is  secretory  only  and  the  inner 
layer  both  secretory  and  absorptive.  Additional  and  supporting  evi- 
dence is  found  by  Franca  in  the  presence  of  canalicuh.  Some  occur 
"in  the  thickness"  of  the  membranes  between  the  cells  of  the  two 
layers  and  open  on  the  outside  of  the  gland  by  means  of  minute  oval 
mouths.  It  is  these  which  permit  the  entrance  of  absorbed  substances 
to  the  deeper  cell  layer.  Others  occur  in  "the  thickness"  of  the  but- 
tresses of  the  epidermal  cells  (between  which  fingers  of  the  protoplasm 
project,  as  described  by  Haberlandt  for  Drosera),  and  these  "without 
doubt"  permit  the  escape  of  secretion.  I  have  carefully  examined 
preparations  after  treatment  with  II2S04,  followed  by  Sudan  III  and 
have  been  unable  to  find  any  evidence  of  pores.  The  evidence  in  the 
form  of  a  drawing  in  his  plate  has  httle  convincing  effect. 

A  critical  study  of  Drosophyllum  was  undertaken  by  Quintanilha 
at  Coimbra.  His  results,  pubHshed  in  1926,  briefly  stated  are  as  fol- 
lows. Drosophyllum  is  indeed  a  carnivorous  plant,  acting  by  means  of 
a  proteolytic  ferment  of  the  type,  of  animal  pepsin.  A  mosquito  can 
be  completely  digested  in  24  hours.  Bacterial  digestion  does  not 
enter  into  the  picture  (in  this  agreeing  with  Goebel,  whose  experi- 
ments were  repeated  and  verified).  The  stalked  glands  are  essentially 
organs  of  capture  but  at  the  same  time  they  are  "signales  d'alarme"; 
that  is,  on  capture  of  an  insect,  they  send  a  stimulus  to  the  sessile 
glands  and  provoke  their  activity.  These  are  exclusively  organs  of  di- 
gestion and  absorption,  but  they  act  only  on  stimulation.  Experimen- 
tally and  under  favorable  conditions,  the  stalked  glands  may  digest 
very  small  amounts  of  albumen  without  the  intervention  of  the  sessile 
glands,  but  the  proteolytic  properties  of  the  mucilage  are  always  in- 
significant. Experimentally  it  was  shown  also  that  the  sessile  glands, 
when  previously  excited,  can  digest  and  absorb  albumen  without  the 
intervention  of  the  stalked  glands  which  had  been  removed  by  ampu- 
tation, and  in  this  condition  the  absorption  is  as  rapid,  or  even  more 
rapid,  than  it  would  be  in  collaboration  with  the  stalked  glands  be- 
cause of  dilution  of  the  secretion.  In  the  normal  state  the  stalked 
glands  act  as  traps  and  furnish  stimuli  to  the  sessile  glands. 

Excitation  of  the  sessile  glands  can  be  procured  directly  by  chemi- 
cal but  not  by  mechanical  means  and  indirectly  by  both  means.  Simple 
pressure  or  friction  of  the  stalked  glands  does  not  procure  excitation 
of  the  sessile.  However,  the  cutting  off  of  the  glands  from  the  stalks 
can  excite  indirectly  and  mechanically  the  sessile  glands.  The  ex- 
citation is  slow  of  transmission  and  is  limited  to  an  area  of  about  i  cm. 
from  the  tentacle  stimulated.  On  anatomical  grounds  Quintanilha 
inclines  to  believe  with  Fenner  that  the  phloem  of  the  vascular  system 


Chapter  VIII  —  105  —  Drosophyllum 

serves  to  transmit  the  stimulus.  The  digestive  capacity  of  the  plant 
is  reduced  after  fructification. 

The  same  author  studied  the  cytological  concomitants  of  the  di- 
gestive and  absorptive  activity,  and  his  findings  are  of  interest  in  con- 
nection with  those  of  Homes  and  others  on  aggregation  in  Drosera 
and  with  those  of  Franca  above  given.  He  found  that  the  state  of 
aggregation  can  be  procured  independently  of  digestion.  During 
digestion  there  occur  "black  concretions"  in  the  inner  course  of  cells 
of  the  stalked  glands.  These  are  not  the  "spherules  alimentaires "  of 
Franca,  but  intravacuolar  precipitation  of  anthocyanin  compounds. 
In  the  sessile  glands,  however,  concretions  appear  in  the  cells  derived 
from  the  absorption  of  albumins  impregnated  with  melanin.  The 
chondriome  of  the  glandular  cells  does  not  act  directly  in  the  elabora- 
tion of  proteolytic  enz3rmes  and  it  does  not  present  alterations  which 
allow  us  to  attribute  to  them  an  important  role  in  the  phenomenon  of 
digestion.  Only  in  the  internal  secretory  layer  of  the  sessile  gland 
the  elements  of  the  chondriome  are  considerably  reduced  in  volume 
during  intracellular  digestion.  The  number  of  the  chondrioconts  is  also 
reduced  and  that  of  the  mitochondria  is  increased  proportionally. 

On  the  other  hand,  the  vacuome  appears  to  be  the  seat  of  the 
elaboration  of  ferments  and  certainly  has  an  important  role  in  the 
processes   of    digestion    and    secretion. 

Pathological  conditions  in  the  plant  due  to  overfeeding  have  not 
been  observed.  It  is  clear  that  Drosophyllum  profits  by  food  materials 
supplied  by  animals,  and  that  this  compensates  for  an  insufficient 
mineral  nutrition,  Quintanilha  says  in  general  conclusion. 

Literature  Cited: 

Darwin,  C,  Insectivorous  Plants.     2d.  ed.,  London  1875.     1908  reprint. 

Fenner,  C.  a.,  Beitrage  zur  Kenntnis  der  Anatomic,  Entwickelungsgeschichte  und  Biologic 

der  Laubblatter  und  Driisen  einiger  Inscktivoren.     Flora  93:335-434,  i904- 
Fernandes,  Ab{lio,  Morphologia  e  biologia  das  plantas  carnlvoras.    Anuario  da  Sociedade 

Brotcriana  6:14-46,  1940;    7:16-52,  1941.     A  third  part  appeared  later  in  1941;    the 

whole  was  issued  as  a  brochure,  repaged,  in  1941.     Good  photographs  of  Drosophyllum 

and  of  its  habitat. 
FR-A-Nf  A,  C,  La  question  des  plantes  carnivores  dans  le  passe  at  dans  le  present.    Bol.  Soc. 

Broteriana  I  (2  ser.):38-57,  1922. 
FRANfA,  C,  Recherches  sur  le  "Drosophyllum  lusitanicum"  et  remarques  sur  les  plantes 

carnivores.    Arch,  portug.  d.  Sci.  biol.  1:1-30,  1925. 
GoEBEL,  K.,  Pfianzenbiologische  Schilderungen.     Marburg  1889-1891. 
Harshberger,  J.  W.,  Notes  on  the  Portuguese  insectivorous  plant,  Drosophyllum  lusitani- 

cum.     Proc.  Amer.   Philosoph.  Soc.   64:51-54,   1925. 
Meyer,   A.  &  A.  Dewevre,  tjber  Drosophyllum-  lusilanicum.     Bot.    Centralbl.   60:33-41, 

1894. 
Penzig,  O.,  Untersuchungen  iiber  Drosophyllum  lusitanicum.     Diss.  Breslau,  1877. 
Quintanilha,  A.,  O  problema  das  plantas  carnivoras.    Dissertation  Coimbra,  1926,  88  pp 

(Contains  a  very  full  bibliography  of  the  Uterature  pertinent  to  carnivorous  plants. 

French  resume).     Extr.  from  Bol.  Soc.  Brot.  4. 
Solereder  1899  {see  under  Dionaea). 


Chapter  IX 
PINGUICULA,   BUTTERWORT 

Distribution.  —  General  appearance.  —  Habitat.  —  The  leaves.  —  Two  kinds  of  glands 
(Points  of  structure.  Early  work  of  Darwin:  movements.  Secretion  and  digestion). — 
Popular  uses. 

The  genus  Pinguicula  consists  of  about  30  species  distributed 
throughout  the  northern  hemisphere  in  temperate  or  cool  temperate 
regions.  Although  making  use  of  a  far  different  mode  of  capture  of  prey, 
it  is  closely  related  to  Utricularia  and  Genlisea,  and  is  one  of  the  three 
lentibulariaceous  genera,  as  shown  by  the  flower  structure.  The 
personate  corolla  is  blue,  purple  or  yellow,  and  differs  from  that  of 
Utricularia  principally  in  the  five-parted  cal30c. 

All  the  species  are  of  very  uniform  character.  The  plant  consists 
of  a  short  vertical  stem  giving  rise  to  a  compact  rosette  of  leaves  which 
usually  lie  flat  on  the  ground,  or  in  some  species  {P.  gypsicola)  are 
directed  obHquely  upward  also.  They  exhale  a  distinct  fungus-like 
odor.  The  tissue  tensions  in  the  leaves  are  such  that  when  a  plant  is 
uprooted  from  the  soil  they  become  at  once  strongly  reflexed,  as 
Darwin  observed;  but  this  is  a  feature  common  to  rosette  plants. 
The  leaves  are  entire,  usually  ovate  {P.  vulgaris)  or  broadly  ovate  {P. 
cuneata),  with  upcurled  margins.  In  color  they  are  a  pale  faded  green, 
yellowish  in  bright  light  (Batalin),  deeper  green  in  the  shade,  in  P. 
vulgaris  pale  purple  due  to  the  presence  of  pigment  in  the  lower  epider- 
mis. They  are  very  soft  and  yielding,  easily  bruised  and  torn;  and, 
being  "greasy"  to  touch,  the  name,  derived  from  the  Latin  pinguis, 
fat,  was  suggested,  according  to  accounts.  The  dorsal  surface  is  quite 
smooth  and  shiny,  the  ventral  ghstening  with  myriads  of  minute 
mucilage  glands.  In  addition  to  their  glands,  both  surfaces  bear  num- 
erous stomata  peculiar  in  having  no  chlorophyfl,  though  there  is  pres- 
ent according  to  Batalin  a  pale  yellow  pigment.  The  flowers  are 
borne  singly  on  slender,  glandular,  pubescent  scapes,  have  a  five-parted 
corolla,  with  a  slender  spur,  so  large  and  showy  in  some  species  of  the 
genus  that  they  are  found  in  glasshouse  cultivation.  Although  the 
peduncles  also  have  glandular  hairs,  Darwin  thought  them  devoid 
of  digestive  function.  The  seedlings  have  a  short  taproot  possessed 
of  a  few  root  hairs,  but  this  does  not  persist  and  soon  gives  way  to 
adventitious  roots  arising  from  the  stem  above.  In  possessing  a  tap- 
root, even  though  fugacious,  this  genus  differs  from  the  others  of  the 
family,  in  which  there  is  none.  There  is  but  one  cotyledon,  which 
arises  as  a  semicircular  ridge  around  the  plumule,  and  when  fully 
developed  is  strongly  folded  lengthwise  and  may  in  longitudinal 
sections  be  easily  interpreted  as  two,  as  Goebel  pointed  out. 

Pinguicula  grows  in  wet  places,  with  mosses,  etc.,  in  chinks  of  wet, 
dripping  rocks,  on  hummocks  in  swamps  {ij  — 4)  and  similar  situa- 
tions, in  general  conformity  with  the  majority  of  carnivorous  plants. 
Towards  the  end  of  the  growing  season  the  plant  produces  very  com- 


Chapter  IX —107  — Pinguicula 

pact  buds  of  various  sizes  (brood-buds)  which  can  reproduce  the  plant 
in  the  following  growing  season  (Hovelacque). 

The  entire  leaves  and  peduncles  are  provided  with  two  kinds  of 
glands,   stalked   and   sessile    (jj  —  lo,    ii),   densely   scattered   on   the 
upper  surface,  with  a  much  smaller  number  of  sessile  glands  with  four- 
celled  capitals  on  the  lower  dorsal  surface  (75  —  2-4).    According  to 
Fenner   the   latter   are   hydathodic   in   character   for   he   observed   a 
minute  droplet  of  fluid  water,  presumably,  on  each  gland.     They  may 
safely  be  excluded  from  taking  part  in  the  capture  and  digestion  of 
prey.     Goebel  had  thought  their  secretion   to  be  mucilaginous  but 
this  seems  not  to  be  the  case.    All  these  glands  are  of  epidermal  origin 
(Gressner,   1877;  Fenner,   1904).     The  stalked  glands  of  the  upper 
surface  stand  on  an  epidermal  cell,  the  stalk  cell  displaying  a  marked 
entasis,  ending  in  a  single  short  domed  cell  supporting  the  capital  com- 
posed of   16  radiating  cells.     This  secretes  and  supports  a  globule  of 
stiff  mucilage  which  serves  to  entrap  and  smother  the  prey,   which 
must  be  small  —  only  small  insects  are  effectively  caught  —  such  as 
aphides,  minute  flies  of  various  kinds,  etc.     The  sessile  glands  have  a 
similar  structure,  but  the  stalk  cell  is  not  cut  off  from  the  foundation 
epidermis  cell,  and  there  is  no  elongation  of  it.    The  base  of  the  gland, 
therefore,  lies  flush  with  the  general  surface.     The  capital  has  only 
eight  cells.    The  sessile  glands  of  the  under  surface  have  capitals  with 
only  four  cells.     All  these  have  been  described  by  Fenner.     This  in- 
vestigator further  adds  that  some  four  rows  of  cells  along  the  very 
thin  leaf  margin  are  also  glandular,  and  that  these  secrete  mucilage. 
The  margin  is  of  only  three  cells  in  thickness,  a  single  course  of  cells 
being  embraced  between  the  two  epidermes   (75  —  5).     It  is  always 
curled  upwards  through  about  180  degrees,  and  this  has  been  inter- 
preted as  an  adaptation  for  conserving  the  digestive  fluids  which  escape 
from  the  glands  on  stimulation.     Fenner  believes  also  that  the  escape 
of  secretions  from  the  glands  is  made  possible  by  the  occurrence  of 
pores  in  the  cuticle.    I  have  not  been  able  to  see  them,  but  treatment 
with  methylene  blue  proves  the  easy  passage  of  solutes,  for  if  a  leaf  is 
plunged  into  a  solution  of  medium  strength  the  capitals  of  the  glands 
are  almost  immediately  and  deeply  stained.    The  capitals  of  the  stalked 
glands  are  also  stained  but  not  so  quickly  as  those  of  the  sessile  glands, 
perhaps  because  of  the  presence  of  mucilage.    With  regard  to  the  struc- 
ture of  the  cells  along  the  margin  of  the  upper  surface,  I  can  see  no 
cytological  evidence,  such  as  claimed  by  Fenner,  that  they  are  glandu- 
lar, nor  have  I  seen  a  band  of  mucilage  as  described  by  him.     J.  R. 
Green    (1899,   p.    214)    cites   Darwin   to   the   effect   that   Pinguicula 
secretes  a  digestive  fluid  on  the  edges  of  the  upper  surface  of  the  leaf 
which  folds  over  to  enclose  its  captive.    On  perusing  Darwin's  account 
I  am  unable  to  subscribe  to  Green's  statement.    True,  Darwin  does 
use  the  expression  ''placed  among  one  margin"  or  "on  one  margin"  but 
this  was  not  meant  to  indicate  that  when  secretion  occurred  it  was 
confined  to  the  margin,  but  that  the  nearby  stalked  glands  contributed. 
Drops  of  meat  infusions  could  not  be  confined  to  the  margin  without 
coming  into  contact  with  nearby  glands.     Darwin  in  his  first  set  of 
experiments  was  concerned  with  the  possibility  of  leaf  movement  which 
he  demonstrated  to  his  own  satisfaction.     In  his  experiment  on  di- 


Francis  E.  Lloyd  —108— Carnivorous  Plants 

gestion  he  invariably  placed  the  substrate  to  be  acted  on  "on  the 
leaf",  and  I  think  it  is  quite  evident  from  the  context  that  Darwin 
did  not  think  of  the  margin  of  the  leaf  as  having  a  localized  digestive 

action. 

Pmguicula  was  first  studied  and  shown  to  be  carnivorous  by  Dar- 
win. "I  was  led  to  investigate  the  habits  of  this  plant  by  being  told 
by  Mr.  W.  Marshall  that  on  the  mountains  of  Cumberland  many 
insects  adhere  to  the  leaves"  {Insectivorous  Plants,  p.  297).  He  noted 
the  presence  of  two  kinds  of  glands,  sessile  and  stalked,  later  studied 
carefully  by  Fenner.  Having  studied  Drosera  extensively  Darwin 
first  looked  for  and  discovered  movements  of  the  leaves.  In  a  se- 
ries of  17  experiments  small  flies,  or  portions  of  larger  flies,  smaller 
and  larger  fragments  of  meat,  meat  juice  stabilized  in  small  bits  of 
sponge,  even  fragments  of  glass  were  placed  in  various  positions  in 
rows  parallel  to  the  margin,  near  the  apex,  and  along  the  midrib,  and 
he  found  curvatures  of  the  leaf  margin  to  occur  within  periods  of  a  few 
(2-4)  hours,  to  increase  for  some  hours  and  finally  to  disappear.  The 
apex  of  the  leaf  never  shows  motion,  this  being  confined  to  the  margins. 
He  found  evidence  leading  him  to  believe  that  the  stimulus  could  be 
transmitted  to  a  distance  of  about  6  mm.  (his  exp.  13).  A  weak  so- 
lution of  ammonium  carbonate  caused  marked  incurvation  of  the  leaf 
margin  in  3.5  hrs.,  a  stronger  solution  (i  to  218  H2O)  causing  no  move- 
ment, probably  due  to  damage.  Mechanical  irritation  of  the  leaf 
surface  either  before  or  after  the  apphcation  of  meat  juice,  thus  im- 
itating the  actions  of  dying  prey,  did  not  hasten  or  increase  the  re- 
sponse. The  effect  produced  by  fragments  of  glass  was  as  rapid  as 
that  following  the  application  of  nitrogenous  substances,  but  the  de- 
gree of  curvature  was  less.  The  substances  used  other  than  glass  in- 
cited a  more  or  less  copious  flow  of  secretion. 

Darwin  commented  on  the  brevity  of  the  response  action,  there 
being  a  complete  restoration  of  form  within  24  hours.  He  was  thus 
prompted  to  doubt  the  usefulness  of  the  behavior,  but  ventured  the 
idea  that  the  infolded  margin  could  prevent  the  washing  away  of  prey, 
as  in  fact  was  observed  by  a  friend  of  Darwin  in  Wales.  If  the  prey 
is  large  the  infolding  leaf  margin  pushed  it  further  toward  the  middle 
of  the  midrib,  thus  bringing  it  into  contact  with  more  glands,  an  effect 
comparable  to  the  action  of  the  tentacles  in  Drosera.  The  margins  of 
the  leaf  are  always  curved  up,  and  this  Darwin  thought  to  help  to 
conserve  the  fluids  from  loss,  keeping  them  on  the  leaf  surface  to  be 
absorbed.  Goebel  could  not  substantiate  Darwin's  conclusions  about 
the  sensitivity  of  the  Pmguicula  leaf,  his  experimental  results  being 
mostly  negative.  On  the  other  hand,  Fenner,  one  of  Goebel's 
students,  did  find  sHght  movements  on  the  application  of  fragments 
of  glass,  followed  by  quick  recovery.  The  secretion  of  mucilage  is 
thereby  excited.  When  an  insect  falls  on  or  near  the  leaf  margin,  an 
abundant  secretion  foflows,  overwhelming  it.  This  escape  of  fluids 
from  the  leaf  alters  the  tensions  and  this  results  in  the  inrolhng  of 
the  leaf  margin  which  does  not  occur  in  older  mature  leaves.  When  the 
insects  sink  down  to  the  leaf  surface  and  come  into  contact  with  the 
sessile  glands  (75 —  11),  an  acid  secretion  of  greater  viscosity  and  con- 
taining a  digestive  enzyme  escapes   from  these.     Goebel  had  shown 


Chapter  IX  —109— Pinguicula 

that    the    abundant    mucilaginous    secretion    following    application    of 
granules  of  sugar  is  without  digestive  power. 

Having  cultivated  material  of  P.  vulgaris  collected  in  the  mountains 
of  California  east  of  Crescent  City,  I  repeated  such  experiments  as 
done  by  Darwin,  Goebel  and  Fenner  on  about  a  dozen  leaves,  with 
definitely  positive  results.  I  cite  only  one  as  typical,  this  being  il- 
lustrated in  15  —  I,  see  also  13  —  6.  The  total  activity  extended  over 
more  than  six  days.  Four  minute  flies  were  observed  caught  in  a  row 
parallel  to  one  margin  and  two  similarly  placed  with  respect  to  the 
other  margin.  Already  the  one  margin  was  slightly  curved  upwards 
on  Oct.  2,  the  other  showed  no  motion  until  the  night  of  Oct.  3-4.  On 
the  morning  of  Oct.  4  both  margins  were  well  curved,  enough  to  hide 
all  the  flies.  On  Oct.  6,  the  inward  rolHng  of  the  margins  was  well 
developed,  and  next  day  it  had  begun  to  recede,  again  exposing  the 
flies  to  one's  vision.  This  behavior  was  typical  of  the  whole  series  of 
cases.  This  and  a  number  of  other  cases  observed  seem  to  throw  doubt 
on  the  vaHdity  of  Darwin's  statement  that  the  time  leaves  remain 
incurved,  even  though  the  exciting  objects  remain  in  position,  is  but 
short,  i.e.,  not  more  than  twenty-four  hours.  It  is  further  well  known 
that  the  contact  of  an  insect  with  the  leaf  at  a  point  removed  from  the 
margin,  i.e.,  near  the  midrib,  results  in  the  dishing  of  the  leaf  below 
the  insect  (Darwin,  Batalin).  This,  as  Batalin  suggests,  is  the 
same  phenomenon  as  observed  in  Drosera,  and  must  be  attributed  to 
growth  and  not  to  injury  as  Darwin  supposed.  When  flies  are  ar- 
ranged along  and  more  or  less  parallel  to  the  leaf  margin  the  growth 
results  in  the  rolling  of  it.  There  is  Httle  doubt  of  the  correctness  of 
this  explanation;  and  moreover  it  agrees  with  our  knowledge  of  the 
procedure  in  Drosera  and  Dionaea. 

Movement  in  Pinguicula  is  then  an  undoubted  fact.  How  much  sig- 
nificance may  be  attached  to  it  is  a  question.  Goebel  attached  Kttle. 
Darwin  thought  that  the  rolling  of  the  leaf  margin  brings  more  glands 
into  contact  with  the  prey,  and  in  some  cases  pushes  it  into  new  posi- 
tions further  away  from  the  margin.  Darwin  probably  underesti- 
mated the  persistence  of  the  change  in  movement,  and  therefore  its 
importance.  The  upward  curved  leaf  margins  help  to  hold  the  se- 
cretion in  place.  This  is  probably  as  much  as  we  can  say  about  the 
matter. 

Darwin  then  turned  his  attention  to  the  question  of  secretion  and 
digestion.  He  found  that  when  he  placed  prey  (small  flies),  fragments 
of  meat,  cartilage,  fibrin,  albumen  (egg-white,  coagulated),  gluten  and 
gelatin,  etc.,  on  the  leaf  surface,  there  was  an  increase  of  secretion, 
often  copious,  and  that  this  was  acid.  Evidence  of  digestion  was 
clear:  insects  fell  apart  readily,  and  other  substances  showed  the  ex- 
pected signs  of  disintegration.  Objects  not  containing  soluble  nitrog- 
enous matter,  or  other  soluble  matter  do  not  excite  secretion.  Non- 
nitrogenous  fluids  can  cause  free  flow  of  the  secretion,  but  this  remains 
neutral  (non-acid).  Among  the  substances  or  objects  which  incite 
acid  secretion  were  small  leaves  {Erica  tetralix),  pollen  and  various 
seeds,  all  often  seen  to  adhere  to  leaves  in  the  open,  aU,  of  course,  con- 
taining nitrogen  from  which  Darwin  argued  that  these  objects  also,  as 
well  as  animal  prey,  help  to  nourish  the  plant.    Since  the  peduncles  are 


Francis  E.  Lloyd  —HO— Carnivorous  Plants 

equally  glandular  with  the  leaf,  and  since  the  life  of  a  peduncle  is  fully 
a  month  or  more,  whatever  benefit  may  be  derived  from  prey  caught 
by  leaves  may  also  be  said  to  accrue  from  that  caught  by  the  peduncles. 

Cytological  changes.  —  Darwin  examined  the  condition  of  the  glan- 
dular cells  after  being  in  contact  for  some  time  with  sources  of  matter 
which  was  plainly  absorbed,  and  found  evidence  of  change  in  structure 
and  appearance  of  the  protoplasm  and  its  content,  usually  in  the  ap- 
pearance of  granular  matter  colored  brownish,  or  in  the  cell  contents, 
at  first  limpid,  being  aggregated  into  slowly  moving  masses  of  proto- 
plasm. The  difficulties  of  observation  and  inference  are  obviously 
great,  a  great  deal  more  so  than  in  the  case  of  Drosera.  Darwin  re- 
ferred the  appearances  to  the  absorption  of  food  materials. 

NicoLOSi-RoNCATi  (1912)  endeavored  to  relate  cytoplasmic  changes 
observed  in  fixed  and  stained  material  to  secretive  activity,  in  P. 
hirtifiora.  In  actively  secreting  glands  (mucilage  glands  presumably), 
the  cytoplasm  is  vacuolated  and  contains  many  fuchsinophile  granules 
scattered  toward  the  periphery  of  the  cell  with  moniliform  bodies  in 
the  vicinity  of  the  nucleus.  The  nucleolus,  large  and  intensely  fuch- 
sinophile at  the  beginning  of  secretion,  diminishes  notably  in  volume 
and  in  capacity  for  staining  in  evidently  secreting  cells.  The  author 
concluded  that  the  first  impulse  to  secretion  comes  from  the  nucleolus, 
the  primary  granules  of  secretion  being  formed  by  the  chromatin. 
These  diffuse  throughout  the  body  of  the  cell  definitively  elaborating 
secretory  substance.  This  work,  while  affording  a  beginning,  does  not 
lead  us  very  definitely  forward,  as  at  this  time  we  are  unable  to  dis- 
tinguish the  kind  of  secretion  dealt  with,  whether  of  mucilage  or  en- 
zymes. 

TiscHUTKiN  (1889)  carried  out  experiments  similar  to  those  of 
Darwin,  and  worked  also  with  glycerin  extracts  of  leaves  and  mix- 
tures of  leaf  secretion,  withdrawn  by  means  of  a  pipette,  with  glycerin, 
acidified  variously  (HCl,  formic,  mahc  acids).  Both  glycerin  extracts 
and  mixtures  gave  only  negative  results.  Albumen,  gelatin  and 
fibrin  placed  on  the  leaves  gave  results  for  him  much  the  same  as  for 
Darwin.  Tischutkin  states  then  that  in  Pinguicula  insects  which 
are  caught  call  forth  a  secretion  of  acid  sap  which  can  procure  a  cer- 
tain alteration  of  their  substance.  Examining  the  work  of  Rees, 
Gorup  and  Will  (later  substantiated)  he  sees  in  its  deficiencies  ev- 
idence of  bacterial  action  and  he  comes  to  the  conviction  that  the  role 
of  the  plant  is  the  secretion  of  a  medium  which  is  suited  to  the  hfe 
and  activity  of  microorganisms  (bacteria),  and  concludes  without  fur- 
ther experimental  evidence  that  in  Pinguicula  we  are  deaHng  with 
bacterial  action,  in  this  agreeing  with  Morren  (1875). 

Somewhat  later  Goebel  also  attacked  the  problem  of  digestion  in 
Pinguicula.  When  he  put  particles  of  fibrin  on  the  leaves,  the  secre- 
tion was  intensified,  and  the  smallest  particles  digested  in  24  hours. 
The  secretion  was  weakly  acid.  When  insects  (those,  as  already  said, 
are  always  small,  for  Pinguicula  is  adapted  to  the  capture  and  di- 
gestion of  only  small  ones)  are  found  in  an  advanced  stage  of  digestion, 
the  glands  are  found  to  contain  droplets  of  fat.  Large  insects  or  fibrin 
fragments  are  overcome  by  decay.  By  ad  hoc  culture  experiments 
Goebel  showed  that  Tischutkin's  views  are  not  justified.    He  showed 


Chapter  IX  —  111  —  Pinguicula 

that  when  even  small  flies,  partly  digested,  were  transferred  to  nutrient 
gelatin  plates,  no  evidence  of  bacterial  activity  was  forthcoming.  He 
convinced  himself,  on  experimental  evidence,  that  Pinguicula  secretes 
an  antiseptic  substance  which  prevents  bacterial  action,  and,  while  his 
procedure  cannot  be  regarded  as  beyond  criticism,  yet  it  is  to  be 
noted  that  later  Loew  and  Aso  (1907)  claimed  to  have  found  benzoic 
acid  in  the  leaves.  Naturally  the  amount  present  is  not  sufficient  to 
meet  all  conditions,  since  in  nature  the  Pinguicula  catches  only  minute 
flies,  and  only  small  amounts  of  the  antiseptic  agent  are  called  for.  In 
Tischutkin's  experiments,  says  Goebel,  he  used  too  large  masses  of 
material  with  erroneous  results.  The  capacity  of  the  stomach  to  digest 
cheese,  he  added,  cannot  fairly  be  judged  by  feeding  a  kilo  of  cheese  at 
one  time. 

Goebel  made  an  experiment  which  seems  to  distinguish  between 
the  action  of  the  sessile  and  stalked  glands,  substantiating  Darwin's 
findings  that  "non-nitrogenous  fluids  if  dense  cause  the  glands  to  pour 
forth  a  large  supply  of  viscid  fluid,  but  this  is  not  in  the  least  acid. 
On  the  other  hand  the  secretion  from  glands  excited  by  contact  with  ni- 
trogenous soHds  and  fluids  is  invariably  acid ".    Tischutkin  had 

tried  to  extract  leaves  by  placing  them  in  glycerin,  with  negative  results. 
By  strewing  granular  cane  sugar  on  the  leaf  surface  of  some  70  plants, 
Goebel  collected  about  i  cc.  of  secretion  which  was  neutral  and  after 
the  addition  of  0.2%  formic  acid  a  particle  of  fibrin  remained  in  it 
undigested  at  35°  C.  From  this  it  appears  that  an  abundant  se- 
cretion (probably  from  the  stalked  glands)  is  not  necessarily  correlated 
with  digestive  activity.  On  the  other  hand  if  leaves  are  stimulated  by 
strewing  particles  of  fibrin,  smeared  with  meat  juice  and  finally  placed 
in  meat  juice,  with  1.5  Tc  formic  acid  added  and  allowed  to  stand  for 
18  hours,  a  fluid  was  obtained  which  digested  swollen  fibrin  in  25  hours. 
No  bacteria  were  present,  due  to  the  hindering  action  of  the  formic 
acid.     In  any  event,  the  amount  of  enzyme  obtainable  is  smafl. 

In  the  foregoing  it  will  be  seen  that  the  conclusion  that  Pinguicula 
is  a  true  carnivorous  plant  rests  on  the  evidence  that  fragments  of 
nitrogenous  matters  and  insects  are  disintegrated  by  the  secreted 
juices,  and  that  this  takes  place  in  the  absence  of  bacteria  (Goebel). 
Dernby  (191 7)  pushed  the  matter  further,  and  by  means  of  glycerin 
extracts  obtained  a  true  tryptase,  not  observed  elsewhere  among 
plants.  There  is  also  a  weak  and  incomplete  pepsidase  effect,  as  small 
amounts  of  amino-compounds  are  set  free  at  pH  8.  The  tryptase  at- 
tacked caseinogen  at  pH  8-9. 

But  this  has  not  gone  without  further  challenge. 

MiRiMANOFF  (1938)  found  that  the  gland  ceUs  of  both  stalked 
and  sessile  glands,  where  an  insect  was  attached,  showed  aggregation. 
His  description  of  this  agrees  with  that  of  Darwin  and  others.  He 
could  not  induce  it,  however,  with  other  substances  (egg-white,  cheese, 
meat  extract).  It  appeared  to  him  that  only  certain  products  of 
deamination  were  responsible  for  disturbing  the  osmotic  equihbrium 
of  the  cefl,  inducing  the  changes  leading  to  aggregation.  It  is  revers- 
ible, and  different  from  those  irreversible  changes  observed  on  the  ap- 
phcation  of  neutral  red,  though  by  some  observers  they  have  been 
regarded  as  similar  or  ahke.     Incidentally,  pointing  out  the  total  con- 


Francis  E.  Lloyd  —  112  —  Carnivorous  Plants 

tradiction  between  the  results  of  Tischutkin,  who  denied  the  role  of 
other  than  bacterial  digestion,  and  Colla,  who  argued  the  opposite, 
he  states  his  belief  that  digestion  by  the  leaf  is  extraordinarily  feeble, 
and  it  seemed  to  Mirimanoff  that  Pinguicula  would  better  be  re- 
garded as  a  "semi-carnivore".  Following  up  this  hint  Olivet  and 
Mirimanoff  (1940)  re-examined  the  matter  by  a  new  method.  They 
applied  {a)  a  sterilized  insect  (Drosophila)  to  a  bacteria-sterile  leaf, 
and  (b)  one  to  a  non-sterile  leaf;  and  (c)  a  non-sterile  insect  to  a  non- 
sterile  leaf.  In  the  first  case  there  was  no  evidence  of  digestion,  and 
none  of  aggregation  and  no  discoloration  of  the  glands.  In  the  second 
there  was  an  evident  discoloration  of  the  glands,  and  aggregation  was 
observed.  Tested,  the  fly  now  was  swarming  with  bacteria  among 
which  were  gelatin-liquifying  motile  forms.  In  the  last  case  digestion 
of  the  insect  proceeded  with  abundant  evidence  of  aggregation  and 
discoloration.  It  was  tried  to  obtain  the  putative  protease  by  diffusion 
into  gelatin-sugar  in  the  cold.  On  warming  at  ordinary  temperatures 
there  was  no  liquifaction.  They  concluded  that  the  digestion  of  insects 
on  Pinguicula  is  the  result  of  bacterial  activity,  and  while  the  authors 
do  not  deny  the  presence  of  a  protease  secreted  by  the  plant,  they  hold 
its  action  to  be  negligible. 

Thus  the  question  has  been  reopened,  and  demands  further  critical 
examination. 

Pinguicula  has  long  been  supposed  to  have  the  ability  to  curdle 
milk.  Linnaeus  (Flora  Lapponica,  p.  10)  tells  us  that  the  Lapps  used 
it  for  the  curdling  of  milk  and  that  the  peasants  of  the  Italian  Alps  use  it 
similarly  (Pfeffer,  through  Oppenheimer)  .  Francis  Darwin  also 
records  the  fact  that  the  same  use  was  made  of  it  by  the  farmers  of 
Wales  "for  the  past  30  years"  as  previous  to  1875.  This  probably 
means  a  very  much  longer  time  (F.  Darwin,  in  a  footnote  in  Darwin, 
1888). 

The  fact  that  some  plants  can  cause  coagulation  in  milk  (notably 
Galium  veruni)  was  known  to  the  ancients,  according  to  Czapek.  It 
is  not  clear  what  precisely  the  function  of  a  rennet  on  this  plant  would 
be,  but  it  seems  that  it  is  not  a  substance  per  se,  but  that  the  pro- 
teolytic enzymes  have  the  property  of  coagulation,  as  will  be  seen 
beyond.  In  relation  to  this  question,  the  following  quotations  were 
sent  me  by  Dr.  Oke  Gustafsson,  translated  and  transmitted  by 
Dr.  Jens  Clausen,  to  both  of  whom  I  owe  thanks:  — 

"This  'tatort'  {Pinguicula  vulgaris)  has  long  been  used  in  some  of  the  more  northern 
provinces  of  Sweden,  as  for  example  Jamtland  and  Dalarne.  It  has  been  mixed  with  fresh 
milk  by  smearing  either  the  milk-sieve  or  the  container  with  the  glutinous  leaves.  For 
a  long  time  it  has  been  a  common  view  that  the  milk  was  changed  to  ropy-  or  long-milk 
by  its  tough  and  viscid  slime  similar  to  cheese-lep  (The  milk  has  been  given  this  name  be- 
cause it  is  so  thick  and  tough  [viscid]  that  it  can  be  pulled  into  long  strands).  Through 
experiments  it  has  now  been  found  that  long-milk  cannot  always  be  produced  with  Pin- 
guicula (the  'tatort'),  if  ever,  but  that  on  the  contrary  such  milk  can  originate  without 
this  medium."     (Lindman). 

Properties  and  uses  in  Norway  and  Denmark.  — "When  the  leaves 
are  laid  in  milk  it  will  curdle,  although  without  separating  from  the 
whey,  and  this  milk,  in  Norway  called  'Ta^ttemaelk'  (ropy  milk)  will 
make  other  milk  curdle.  From  this  the  Norwegian  name  'Tsettegrses' 
(curdlegrass)    and    the    Faroe    name    'Undslaeva    Greas'    have    their 


Chapter  IX  —  113  —  Pinguicula 

origin.  Especially  the  milk  of  reindeer  is  supposed  to  curdle.  However, 
it  had  been  impossible  for  me  to  obtain  information  that  at  the  present 
time  this  plant  is  used  in  Norway  for  production  of  ropy  milk,  be- 
cause usually  the  left-overs  of  milk  curdled  in  this  manner  are  used  to 
thicken  fresh  milk  with. 

"Previously  this  plant  has  been  accused  of  producing  liver  sickness 
(rot)  in  sheep  but  we  now  know  that  this  is  an  effect  of  the  liver 
fluke,  Distotnum  hepaticum,  which  lives  in  wet  pastures  (Note  by 
J.  Clausen,  in  ep.).  The  bees  seek  this  plant,  but  stock  do  not  eat  it. 
It  is  told  that  it  will  stain  yellow.  It  is  an  indicator  of  moist,  so-called 
sour  soil.  In  places  it  is  used  mixed  with  linseed  oil  as  a  home-remedy 
against  wounds."     (Hornemann). 

Dernby  considered  this  whole  question  fully,  citing  the  popular 
belief  in  Scandinavia  that  both  Pinguicula  and  Drosera  procure  when 
in  contact  with  milk  a  "long",  that  is,  a  very  viscous  coagulum. 
Although  the  work  of  Troili-Petersson  and  Olsen-Sopp  (Centralb. 
f.  Bact.  II  T^T,:  191 2)  shows  that  these  plants  have  nothing  to  do  with 
"langmjolk",  yet  the  expressed  sap  of  Pinguicula  leaves  does  have 
a  definite  effect  on  sweet  milk,  that  is,  on  its  casein.  It  produces  a 
viscous  fluid  of  alkahne  reaction,  but  the  casein  is  not  coagulated,  but 
broken  down  into  simpler  bodies.  Dernby  states  the  foflowing  con- 
clusions from  experimental  evidence:  —  (7)  Dialysed  expressed  sap  of 
Pinguicula  cannot  make  milk  "thick";  (2)  On  the  other  hand  it  splits 
casein  of  milk,  but  only  partly,  in  a  weakly  alkaline  field,  just  as 
it  does  Witte-peptone  under  the  same  conditions;  (3)  The  enzyme  is  very 
similar  to  trypsin,  working  at  an  opt.  pH  of  ca.  8;  {4)  No  enzyme  of 
pepsin-erepsin  character  could  be  found. 

Therapeutic  effects.  —  P.  Geddes  pointed  out  that  all  alpine  peasan- 
try apply  the  leaves  to  the  sores  of  cattle,  and  its  healing  effect,  if  such 
there  is,  might  be  referred  to  the  antiseptic  properties.  More  recently 
there  have  been  more  exact  studies  made  of  this  property  (McLean, 
191 9)  indicating  the  truth  of  Geddes'  report. 

Summarizing,  we  may  conclude  that  Pinguicula  is  a  carnivorous 
plant  inasmuch  as  it  catches  small  insects  and  digests  them,  at  least 
in  part,  by  means  of  its  own  ferments.  The  possible  part  played  by  bac- 
teria is  not  excluded.  Its  leaves  are  very  sensitive  to  too  great  "por- 
tions" of  food  as  GoEBEL  truly  said.  Only  minute  insects  can  be 
captured  in  nature,  this  being  a  matter  of  common  observation.  Large 
insects  or  bits  of  fibrin,  unless  very  small,  cause  decay  beneath  with 
permanent  injury  to  the  tissues.  A  closer  understanding  of  the  chem- 
ical nature  of  the  digestive  ferments  has  been  attained  by  Dernby. 

As  to  the  power  of  the  leaf  to  move,  first  observed  by  Darwin, 
there  can  be  no  doubt  of  the  fact,  and  that  the  stimulus,  supplied 
by  the  application  of  various  kinds  of  substances,  organic  and  in- 
organic, is  transmitted  in  some  fashion,  but  only  slowly.  The  short- 
est time  in  which  Darwin  observed  movement  was  2  hours  17  minutes, 
the  stimulus  being  transmitted  over  a  very  short  distance,  a  matter 
probably  of  not  more  than  2  to  6  mm.  Movements  can  be  induced 
by  substances  which  do  not  cause  increased  secretion,  such  as  fine 
grains  of  sand,  as  I  have  also  observed.  Increased  secretion  follows 
the  application  of  sugar  and  proteins  among  others.    But  that  following 


Francis  E.  Lloyd  — 114  —  Carnivorous  Plants  I 

, — ■ i 

sugar  does  not  contain  ferments,  indicating  the  abeyance  of  activity  I 

on  the  part  of  the  sessile  glands  in  this  case.  i 

Literature  Cited: 

Batalin,  a.,  Mechanik  der  Bewegungen  der  insektenfressenden  Pflanzen.    Flora  60:33-39;  I 

54-58;   65-73;    105-111;    129-144;    145-154,  1877  (Pingiiicula,  pp.  150-154).  _  { 

CoLLA,   Silvia,   Sui  fermenti  secret!  da  Pingidcula  alpina  L.   Annuario  della   Chanousia 

3:144,  1937  (through  Mirimanoff). 
CzAPEK,  F.,  Biochemie  der  Pflanzen.  3  vols.  825  pp.  Jena,  1925. 
Darwin,  C,  Irritability  of  Pingidcula.     Gard.  Chron.  II,  2:15  and  19,  4  July,  1874. 
Darwin,  C,  Insectivorous  Plants.     2d  Ed.,  1875. 
Dernby,  K.  G.,  Die  proteolitischen  Enzyme  der  Pingidcula  vulgaris.    Bioch.  Zeitschr.  80:152- 

158,  1917. 
Fenner  (see  under  Nepenthes). 

Geddes,  p.,  Chapters  in  modern  Botany.     New  York  1893,  201  pp.  1 

Goebei.,  K.,  Pflanzenbiologische  Schilderungen,  TI.     1891.  I 

GoRUP,  (see  under  Nepenthes)  \ 

Green,  J.  R.,  (see  under  Nepenthes).  _  I 

Gressner,  H.,  Botanische  Untersuchungen,  i.      Beobachtungen   iiber  Pingidcula  vulgaris.  | 

Jahresber.  d.  evangel.  Fiirstl.  Bentheim'schen  Gymn.    Arnold,  z.    Burgsteinfurt.    Iser-  1 

lohn  1877.  ' 

Hornemann,  J.  W.,  Fors0g  til  en  dansk  oekonomisk  Plantelaere.      Kj0benhavn  1821,  pp.  < 

27-28.  I 

Hovelacque,  M.,  Sur  les  propagules  de  Pingidcula  vulgaris.     C.  R.  106:310,  Feb.  1888. 
Klein,  J.,  Pingidcula  alpina,  als  insektenfressende  Pflanze  und  in  anatomischer  Beziehung. 

Beitr.  z.  Biol.  d.  Pflanzen.  3:163-185,  1880. 
Lindman,  C.  a.  M.,  Bilder  ur  Nordens  flora,    p.  100.     Stockholm,  1922.  I 

LoEW,  O.  &  R.  Aso,  Benzoesaure  in  Pingidcula  vulgaris.     Bull.  Agri.  Coll.  Tokyo  Imp.  1 

Univ.  7:411-412,  1907. 
McLean,  R.  C,  The  anaerobic  treatment  of  wounds  in  life  and  its  maintenance.     New  1 

York,  1919.  _  _       _  ; 

Mirimanoff,  A.,   Aggregation  protoplasmique  et  contraction  vacuolaire  chez  Pingidcula 

vulgaris  L.  Bull.  Soc.  Bot.  de  Geneve  II,  29:1-15,  1938. 
MoRREN,  E.,  Observations  sur  les  precedes  insecticides  des  Pinguicula.     Bull.    Acad.  roy.  , 

d.  Sci.  etc.  Belg.,  2  ser.,  39:870,  1875. 
NicoLOSi-RoNCATi,  F.,  Contributo   alia  conoscenza  citofisiologica   delle   glandule   vegetali. 

Bull.  Soc.  Bot.  Ital.  1912:  186-193. 
Olivet,  R.  &  A.  Mirimanoff,  Pinguicula  vulgaris  L.  est-elle  une  plante  carnivore?     BuU.  j 

Soc.  Bot.  Geneve  II,  30:230-235,  1940. 
Oppenheimer,  C,  Die  Fermente  und  ihre  Wirkungen.  vol.  2,  pp.  1106-1111.     Leipzig,  1925. 
Rees,  (see  under  Nepenthes). 
TiscHUTKiN,  N.,  Die  RoUe  der  Bacterien  bei  der  Veriinderung  der  Eiweisstoffe  auf  den 

Blattern  von  Pinguicula.     Ber.  d.  d.  bot.  Ges.  7:346-355,  18S9. 
Will  (see  under  Nepenthes). 
VON  Willer,  Vital-Microscopische  Beobachtungen  an  Insektenfressenden  Pflanzen.    Trudy 

Inst.  Fiz.  Narkomprosa  (Trav.  Inst.  Rech.  Phys.  Moscou)  2:517-519,  1936.    Not  seen. 

Describes  a  method  of  observing  a  single  gland  of  Pinguicula  exclusively,  all  others 

being  left  intact,  to  be  stained  vitally  and  otherwise  experimented  on. 


Chapter  X 
DROSERA 

Number  of  species.  —  Geographical  distribution.  —  Habitat.  —  Form  and  habit  of  the 
plant.  —  Unfolding  movements  of  the  leaf.  —  The  leaf  (Form.  Anatomy.  Appendages. 
Tentacles.  Sessile  glands,  origin  and  structure,  function.  Locus  of  absorption.  Other 
glands).  —  Reproduction.  —  Carnivory,  early  observations.  —  Mucilage,  origin.  —  Move- 
ments of  the  tentacles  (Early  observations.  Nitschke  and  Darwin).  —  Direction  of  bend- 
ing. —  Duration  of  response.  —  Leaf  blade  not  receptive  to  stimulus.  —  Path  of  stimulus. 

—  Intensity  of  stimulus.  —  Mechanism  of  movement.  —  Behre's  studies.  —  Aggregation. 

—  Digestion.  —  Enzymes.  —  The  significance  of  carnivory  for  the  plant. 

The  genus  Drosera  contains  more  than  90  species  found  in  almost 
all  parts  of  the  world.  It  reaches  its  greatest  development  in  Australia 
and  is  well  represented  in  S.  Africa.  The  most  widely  known,  at  least 
historically,  is  the  common  sundew,  ros  solis,  D.  rotundifolia,  the  plant 
which  chiefly  formed  the  subject  of  Darwin's  extensive  studies.  This 
and  its  allies,  D.  anglica,  D.  intermedia  and  filiformis,  also  well  known 
in  the  North  Temperate  zone,  are  modest  representatives  of  the  genus 
as  compared  with  such  forms  as  D.  gigantea  of  Australia  or  D.  regia  of 
S.  Africa. 

Habitat.  —  It    is    very    generally    understood    that    Drosera    grows 
where  the  soil  is  poor  in  nutrient  substances.     Such  a  statement  ap- 
plies fully  enough  to  the   best  known   species  of  the  northern  hem- 
isphere, D.  rotundifolia,  intermedia,  filiformis,  etc.,  but  seems  not  to  be 
true  of  some  species  such  as  D.  Whittakeri  of  S.  Australia,  where  I 
saw  it  growing  on  wooded  slopes  with  a  general  vegetation.    Even  this, 
however,    though   probably   a   richer   soil   than   that   of   a   sphagnum 
swamp,  is  not  a  rich  soil.     One  commonly  linds  D.  rotundifolia  in  any 
swamp  where  Sphagnum  grows,  and  it  grows  plentifully  in  the  chinks 
of  partially  decayed  floating  or  stranded  logs,  a  favorite  place.    In  the 
Sequoia  National  Park,  California,  it  is  found  in  the  wet  open  mead- 
ows surrounded  by  Sequoia  gigantea,  growing  on  a  dense  floor  of  moss 
(not  Sphagnum).    A  more  accurate  picture  is  afforded  by  Weber  (1902) 
in  his  monograph  describing  the  great  swamps  of  Augustumal,  in  the 
delta  of  the  Memel  River.     There  is  in  this  swamp,  as  of  course  in 
swamps  elsewhere,  a  zonation  of  the  vegetation.    As  one  proceeds  from 
the  margin  to  the  middle,  one  finds  that  the  ash  content  of  the  soil 
and  soil  water  becomes  more  and  more  reduced.    It  is  only  in  the  more 
central  parts  that  D.  anglica  and  D.  rotundifolia  are  to  be  found,  and 
these  are  the  parts  which  are  most  lacking  in  salts.     The  vegetation 
here  consists  of  Spagnum  with  Cladonia  uncinalis,  Scirpus  caespitosus, 
Eriophorum    vaginatum,     Scheuchzeria    palustris,     Rhynchospora     alba, 
Vaccinium  oxy coccus,  and  Andromeda  polifolia  —  and  therefore  of  few 
species.    This  habitat  was  found  to  have  a  soil  with  the  following  com- 
position in  absolute  and  relative  terms.    In  quoting  these  data,  Schmld 

Augustumal       Diluvial  clay 


SWAMPS 

SOIL 

Potassium 

0.044     (1) 

1.06       (24) 

Phosphoric  acid 

0.075     (i) 

0.18       (    2.4) 

Calcium 

0.217     (i) 

2.86     (13.1) 

Magnesia 

0.138     (i) 

0.88     (  5.9) 

Francis  E.  Lloyd  —  116  ^  Carnivorous  Plants 

points  out  the  absence  of  data  on  the  nitrogen  content,  and  cites,  in 
order  to  fill  the  gap,  the  fact,  stated  by  Wollny  (1897),  that  the  soil 
(raw  humus)  of  a  pine  forest  as  compared  with  that  of  the  Drosera 
habitat,  contains  nitrogen  in  the  proportion  of  27:1.  Even  more  strik- 
ing than  the  fact  that  the  habitat  is  of  such  poor  quality  in  respect  to 
salt  content  is  the  further  observation  that  the  first  immigrants  onto 
the  newly  cut  turf  surfaces  after  the  removal  of  peats,  is  Drosera,  and 
this  remains  for  a  long  time  the  only  inhabitant  of  these  raw  peat 
surfaces.  We  may  recall  in  this  connection  that  Correns  (1896) 
showed  that  tap  water  at  a  high  temperature  (54.4°  C.)  does  not 
cause  movements  of  the  tentacles,  but  that  water  devoid  of  CaCOs 
and  CO2  called  forth  reactions  at  that  temperature.  In  this  way  he 
detected  a  toxic  effect  of  Ca  and  inferred  that  this  substance  in  the 
soil  (at  least  too  much  of  it)  might  be  toxic. 

Form  and  habit  of  the  plant.  —  The  commonest  type  of  Drosera 
consists  of  a  slender  stem  crowned  by  a  rosette  of  leaves  with  flowering 
scapes  growing  in  the  leaf  axils.  It  arises  from  a  seedling  (D.  rotundi- 
folia)  which  has  a  fugacious  taproot,  which,  however,  serves  for  the 
formation  of  the  earliest  rosette  of  leaves  (Nitschke,  i860).  Ac- 
cording to  Heinricher  (1902)  the  taproot  fails  to  elongate,  but  swells 
into  a  rounded  mass  covered  with  root  hairs.  The  cotyledons  are 
simple,  spatulate,  followed  by  leaves  of  the  mature  type,  though  small 
and  with  fewer  appendages  (tentacles)  than  the  latter.  As  the  plant 
grows  the  stem  dies  off  behind.  In  winter  the  rosette  is  reduced  to  a 
tight  compact  winter  bud  which  may  have  no  extending  stem  or  roots. 

Growing  as  it  {D.  rot^indifolia  e.g.)  does  in  mats  of  Sphagnum,  the 
differential  growth  rates  of  these  plants  brings  it  about  that  Sphagnum 
by  its  more  rapid  growth  during  the  cool  months,  overtops  the  Drosera 
and  in  the  warmer  months  the  latter  in  its  turn  overtops  the  Sphagnum. 
One  sees,  therefore,  in  a  Drosera  plant,  which  has  grown  in  this  way, 
successive  dead  rosettes  clinging  to  the  dead  stem,  ending  above  in  a 
living  rosette,  as  figured  by  Nitschke.  Such  are  our  familiar  species 
of  the  northern  hemisphere.  The  leaves  of  the  rosette  when  fully  ex- 
panded may  be  relatively  small,  as  in  D.  rotundifolia,  intermedia,  etc., 
or  very  large  and  ligulate,  as  in  a  remarkable  species,  D.  regina,  de- 
scribed by  Miss  E.  L.  Stephens  from  S.  Africa.  In  this  species  the 
leaves  are  2  cm.  broad  by  35  cm.  long.  Or  again  the  leaves  may  be 
large  and  fern-like  in  aspect,  with  strong  terete  petioles  with  a  once  to 
thrice  parted  leaf  blade  as  in  D.  binata,  D.  dichotoma  (S.  Africa,  Aus- 
tralia). These  make  showy  greenhouse  plants,  and  have  often  been 
cultivated  and  used  for  study,  to  be  reported  upon  in  some  detail 
beyond. 

Or  again  the  main  stem  may  be  elongated  upward,  only  slightly  in 
D.  capensis,  an  often  cultivated  form  from  S.  Africa,  with  hgulate  leaf 
blades  supported  on  rather  long  petioles  {13  —  5,7).  In  the  most  stately 
species  D.  gigantea  the  stem  may  be  a  meter  long  and  many  plants  together 
form  a  dense  half  shrubby  tangle  crowned  with  the  numerous  flowers 
in  panicles.  The  stems  climb  or  clamber,  partly  by  twisting  and  partly 
by  means  of  certain  long-petioled  leaves  in  which  the  leaf  blade  be- 
comes a  disc  of  attachment,  its  dense  secretion  forming  an  adhesive 
(GoEBEL  1923).  The  stems  are  wiry,  the  leaves  peltate  and  deeply 
cupped.     It  is  a  pronounced  sclerophyll,  according  to  Czaja. 


Chapter  X  —  117  —  Drosera 

Some  species,  after  the  seedling  stage  is  passed,  form  tubers  which 
perennate,  and  send  up  strong  stems  ending  in  a  rosette  or  whatever 
type  of  above-ground  parts  it  has.  From  the  stems  grow  axillary, 
positively  geotropic  shoots  (droppers),  at  the  ends  of  which  new  tubers 
arise  {See  beyond  for  details).  These  species  have  no  roots,  while  in 
general  the  roots  are  always  meagre  in  numbers  and  extent,  a  fact 
which  is  well  known  (Schmid).  The  root  hairs  are  numerous  in  some 
species  and  their  walls  are  suberized  and  persistent.  In  other  species 
the  root  hairs  are  sparse.  Marloth  has  reported  both  conditions  in 
S.  African  species.  In  some  species  the  roots  are  apparently  replaced 
by  rhizoids.  Diels  has  thus  described  for  D.  erythrorhiza  the  root-like 
productions  one  to  three  in  number  from  the  base  of  each  scale  leaf. 
These  have  no  root  cap,  but  are  provided  with  "root"  hairs  (Diels 
1906).  GoEBEL  comments  on  the  nature  of  these  structures,  called 
by  the  equivocal  name  of  leaf-roots  ("Blattwurzeln"),  pointing  out 
that  in  the  apex,  while  no  root  cap  is  present,  there  is  an  apical  mer- 
istem  just  behind  the  epidermis,  the  outer  walls  of  which  are  thick- 
ened, and  which  are  evidently  a  protective  mail  for  a  boring  apex, 
which  may  be  regarded  perhaps  as  a  reducing  or  reduced  root  end. 
Their  origin  according  to  Diels,  however,  is  exogenous,  and  he  called 
them  leaf  rhizoids,  but  leaves  details  of  their  origin  not  fully  under- 
stood.   I  have  verified  Diels'  observation. 

I  have  examined  the  "leaf roots"  of  D.  erythrorhiza  from  West 
Australia  and  am  able  to  confirm  Goebel's  observation  of  very  thick 
outer  cell  walls  of  the  apical  cells  (75  —  19).  There  is  a  meristem,  but 
this  does  not  lie  immediately  behind  the  epidermis,  but  just  back  of 
three  cell  layers  within.  The  apex  itself  is  composed  of  enlarged 
epidermal  cells  underlain  by  other  cells  of  similar  appearance  derived 
from  two  subepidermal  layers,  and  heavily  loaded  with  large  starch 
grains.  The  apical  cells  constitute  a  boring  organ  which  does  not 
slough  off  as  does  the  root  cap.  If  there  is  any  renewal  of  substance, 
this  would  be  in  new  secretion  of  cell  wall.  The  plant  grows,  however, 
in  very  loose  soil  where  friction  against  the  growing  tip  is  minimum  in 
amount.  At  all  events  I  have  examined  a  large  number  of  "leaf- 
roots"  and  have  not  found  any  evidence  of  renewal  of  epidermal  cells. 

In  the  axis  of  each  rhizoid-bearing  scale  small  tubers,  having  evi- 
dently the  function  of  reproduction,  can  be  produced   (Goebel   1933). 

Unfolding  movements  of  the  leaf.  —  In  many  of  the  species  of  Dro- 
sera {D.  rotundifolia,  D.  pygmaea),  the  petiole  is  bent  so  that  the 
upper  face  of  the  blade  becomes  applied  to  the  petiole  {16  —  17).  This 
is  brought  about  by  the  hyponasty  of  a  more  or  less  narrow  zone  of  the 
petiole  at  the  base  of  the  blade.  In  other  species,  however, 
those  in  which  the  leaf  blade  is  slender  and  filiform,  there  oc- 
curs true  circination,  as  in  D.  filiformis,  D.  regia  (with  slender 
ligulate  leaves  with  short  petioles),  D.  binata,  D.  dichotoma,  with 
the  volute  facing  the  stem,  and  due  again  to  hyponasty.  Just 
the  opposite  occurs  in  Drosophyllum  and  in  Byblis  linifolia.  These 
two  directly  opposite  behaviors  appear,  according  to  Fenner  (1904), 
to  be  related  to  the  need  for  protection  of  the  tentacles  since  they  are 
on  the  upper  surface  in  Drosera  and  on  the  lower  in  Drosophyllum, 
but,  it  is  to  be  noted,  along  the  margins  in  both,  with  the  result  that 


Francis  E.  Lloyd  —  118  —  Carnivorous  Plants 

in  the  volute  a  large  number  of  the  tentacles  are  exposed  and  cannot 
receive  protection  from  the  overlying  turn  of  the  volute.  I  have  ob- 
served this  and  can  confirm  Goebel  on  the  point.  On  the  other  hand, 
GoEBEL  proposes  a  causal  explanation  as  follows.  The  production  of 
a  great  extension  of  surface  by  the  growth  of  tentacles  can  act  to  in- 
hibit the  growth  rate  of  that  surface,  and  thus  permit  the  more  rapid 
growth  of  the  other  face  of  the  leaf,  the  lower  in  Drosera,  the  upper 
in  Drosophyllum  (Goebel,  1924).  In  Byhlis  gigantea  the  leaf  shows  no 
such  movements.  The  leaf  grows  in  a  basal  zone,  and  the  filiform  blade 
extends  always  straight  on.  In  this  the  glands  are  more  numerous  on 
the  lower  surface.  Here  the  distribution  of  the  very  numerous  glands 
either  has  no  inhibiting  effect,  or  has  an  equal  effect  on  all  sides  of  the 
leaf. 

Of  particular  interest  to  us  here  are  the  leaves,  which  are  the 
mechanism  for  catching  and  digesting  prey.  These  present  a  variety  of 
forms  from  a  simple  orbiculate  bifacial  leaf  of  small  size  {D.  rotundi- 
folia  I  cm.  diam.)  through  linear  {D.  filiformis)  to  broad  liguliform 
tapering  at  both  ends  {D.  regia).  Or  the  blade  may  be  once  to  twice 
forked  {D.  binata,  D.  dichotoma)  the  petioles  firm  and  cylindrical 
("rush-like"  as  Darwin  put  it).  Further,  the  leaf  may  be  peltate, 
either  obliquely  {D.  pygmaea)  or  centrally  {D.  gigantea,  D.  peltata, 
D.  subhirtella),  sometimes  with  two  basal  lobes  {D.  auriculata)  making 
the  leaf  base  angular,  a  condition  reaching  its  maximum  expression  in 
D.  lunata  (E.  Asia).  In  the  seedlings  of  the  peltate  leafed  species  the  pri- 
mary seedling  leaves  are  usually  non-peltate,  those  of  D.  peltata  re- 
sembling the  following  leaves  of  D.  rotundifolia  (Diels,   Goebel). 

The  leaf  is  conspicuous  because  of  its  glands  raised  on  elongated 
stalks,  each  bearing  a  drop  of  mucilage  which  is  extremely  viscid  and 
serves  to  entrap  small  insects.  Erasmus  Darwin  thought  that  "Dro- 
sera mucilage  prevents  small  insects  from  infesting  the  leaves"  (The 
Botanic  Garden,  vol.  2,  Canto  i,  p.  229). 

Anatomy  of  the  leaf  blade.  —  The  epidermis  is  composed  of  straight- 
walled  cells  in  D.  rotundifolia  and  D.  capensis,  but  in  D.  Whittakeri 
the  lower  epidermis  is  wavy-walled,  the  upper  straight-walled.  In 
these  species  the  cells  have  many  chloroplasts,  absent  from  the  lower 
epidermis  of  D.  rotundifolia  (Solereder). 

The  internal  parenchyma  has  no  palisade,  as  pointed  out  by 
NiTSCHKE,  the  whole  being  made  up  of  rounded  cells  in  rather  few 
courses,  more  in  some  species  {D.  Whittakeri)  than  in  others  {D.  ro- 
tundifolia). In  the  latter  species  there  are,  in  the  case  examined  by  me, 
3  to  5  courses  of  cells.  The  smallest  are  in  contact  with  the  upper 
epidermis.  Below  there  are  much  larger  cells,  the  third  course  in  con- 
tact with  the  lower  epidermis  unless  a  fourth  course  occurs,  when  the 
cells  are  somewhat  smaller,  but  still  larger  than  the  upper  course 
cells  (/J —  15).  All  the  cells,  usually  including  the  epidermis  (Solere- 
der), contain  chloroplasts.  Stomata  occur  on  both  surfaces.  The  in- 
tercellular spaces  are  large.  This  general  structure  is,  as  Schmid 
(191 2)  has  said,  rather  primitive,  a  quality  which  is  shared,  in  varying 
degree,  with  insectivorous  plants  in  general,  indicating  that  this  qual- 
ity stands  in  a  probable  relation  to  carnivory.  In  these  plants  the 
elaboration  of  starch  and  its  metabolism  and  withdrawal  are  all  slow 
processes. 


Chapter  X  —  119  —  Drosera 

It  was  observed  by  Schmid  that  during  the  absorption  of  materials 
from  the  bodies  of  prey,  the  starch  content  of  the  tissues  at  the  base 
of  the  tentacles  is  lost.  According  to  Spoehr  (1923)  the  amino  acids 
are  concerned  with  the  metabolism  of  starch.  From  this  Geessler 
(1928)  was  prompted  to  investigate  the  influence  of  salts  on  the  me- 
tabolism of  starch  in  the  leaf  of  Drosera  capensis.  He  found  that  in 
this  species,  when  the  leaf  is  fed  with  insects  or  with  various  salts, 
there  is  a  disappearance  of  starch  from  the  leaf.  The  leaves  of  D. 
capensis  are  in  summertime  heavily  loaded  with  starch.  The  starch 
content  is  not  lowered  even  when  the  plant  is  kept  in  the  dark.  Even 
after  45  days  in  the  dark  in  contact  with  distilled  water,  the  leaf  (at 
temp.  36-38°  C.)  showed  no  reduction  in  starch.  The  sugar  con- 
tent is  minute.  In  winter  the  leaves  are  starch-free,  but  there  is  as 
little  sugar  as  in  summer.  These  facts,  together  with  the  high  respira- 
tory intensity,  indicated  to  Giessler  that  the  physiology  of  Drosera 
resembles  rather  that  of  the  animal  than  of  the  plant,  in  that  there 
is  a  protein  respiration.  He  suggests  that  the  starch  is  used  in  the 
secretion  of  mucilage  and  in  supplying  the  energy  for  the  bending  of 
the  tentacles  and  leaf  blade  in  response  to  stimulation.  In  support  of 
his  thesis  he  points  out  the  abundant  occurrence  of  labile  albumin 
(LoEw)  in  many  carnivorous  plants  and  mentions  in  support  of  this 
the  work  of  Erna  Janson  on  aggregation,  to  which  reference  is  made 
elsewhere.  It  has  often  been  asked  if  the  carnivorous  plants  are  not 
animal-like  in  view  of  their  habits,  and  this  is  at  present  answered  as 
above. 

The  absence  of  a  palisade  tissue  in  Drosera,  already  mentioned,  is 
not  confined  to  this  genus,  but  is  generally  though  not  universally  true 
of  carnivorous  plants.  This  lack  stands,  according  to  Schmid,  in  re- 
lation to  insectivory,  the  latter  affording  compensation.  But  Kos- 
TYTSCHEW  questioned  this,  and  did  experiments  which  he  regarded  as 
proving  that  both  Drosera  and  Pinguicula  are  quite  as  active  as  the 
control  plants  which  he  used.  As  his  figures  are  the  only  ones  avail- 
able, I  give  them.  The  amount  of  CO2  assimilated  per  i  dm^  of  leaf 
surface:  Drosera  rotimdifolia,  4  cc,  Tussilago  farfara  (control)  3.8  cc, 
Pinguicula  vulgaris,  38.4  cc,  Aegopodium  podagraria  18. i  cc. 

"Thus  KosTYTSCHEw's  experiments  answered  the  question  whether  a  carnivorous  plant 
can  obtain  its  carbon  nutrition  through  photosynthesis  in  the  affirmative.  The  scant  ex- 
perimental data  show,  and  the  text  implies,  that  Drosera  and  Pinguicula  leaves,  which 
have  not  had  access  to  animal  nutrition  for  some  time,  carry  on  photosynthesis  at  a  normal 
rate.  The  observed  rates  are  in  good  agreement  with  those  estabhshed  by  Willstatter 
and  Stoll  for  a  wide  variety  of  green  plants.  Kostytschew's  comparisons  with  Aiiricu- 
laria  and  Lenina  also  bear  this  out. 

"From  his  data  on  photos>Tithesis  of  Drosera  it  appears,  however,  that  the  rate  of 
carbon  dioxide  assimilation  would  have  increased  materially  after  feeding  the  plants  with 
insects.  The  experimental  details  have  not  been  recorded  in  sufficient  detail  to  permit  of 
a  definitive  decision.  But  the  discovery  of  a  measurable  effect  of  the  ingestion  of  animal 
material  on  the  rate  of  photosynthesis  would  open  up  a  new  approach  to  a  study  of  the 
problem  of  photosynthesis  itself.  The  importance  of  such  a  possibiUty  made  it  an  easy 
matter  to  obtain  the  co-operation  of  Dr.  W.  Arnold  in  carrying  out  some  preliminary  ex- 
periments. 

"Drosera  and  Pinguicula  plants,  previously  not  animal  fed,  were  used  for  the  experi- 
ments. Single  leaves  were  placed  in  distilled  water  in  the  center-cups  of  Warburg  vessels. 
A  mixture  of  sodium  carbonate  and  bicarbonate  was  introduced  into  the  main  chamber 
in  order  to  insure  a  constant  carbon  dioxide  pressure  in  the  gas  phase.     Photosynthesis 


Francis  E.  Lloyd  —120— Carnivorous  Plants 

was  measured  manometrically  at  27°  C.  The  rate  was  constant  over  a  period  of  six  hours, 
at  the  end  of  which  one  leaf  was  fed  with  a  fly  and  some  egg  albumen,  while  another  was 
kept  as  a  control.  Repeated  measurements  over  a  period  of  some  20  hours  following  the 
feeding  showed  that  the  control  leaf  maintained  a  practically  constant  rate  of  both  pho- 
tosynthesis and  respiration.  The  rate  of  oxygen  production  of  the  experimental  leaf 
appeared  somewhat  depressed,  but  its  respiratory  rate  was  considerably  higher  than  that 
of  the  control.  By  correcting  the  photos3Ti thesis  measurements  for  respiration  in  the 
usual  way  it  was  found  that  the  corrected  values  do  not  differ  significantly  from  the  orig- 
inal ones.  The  increased  respiration  obviously  resulted  from  the  availabiUty  of  substrates 
for  oxidation  on  the  outside  of  the  leaf,  and  may  be  caused  by  the  plant  itself  or  by  con- 
taminating micro-organisms.  These  experiments  lend  no  support  whatever  to  the  idea  of 
an  influence  of  feeding  upon  the  rate  of  photosjm thesis  of  carnivorous  plants."  (C.  B.  van 
NiEL,  in  ep.). 

The  appendages  of  the  leaf.  —  There  are  several  kinds  of  appendages 
but  they  are  not  all  common  to  all  species  of  Drosera.  Some  are  im- 
portant physiologically  in  relation  to  the  carnivorous  habit,  others  not. 
To  the  former  belong  the  tentacles  and  sessile  glands,  common  to  all 
species;  to  the  latter  are  the  glandular  and  eglandular  trichomes  seen 
in  D.  rotundifolia  and  other  N.  hemisphere  species  and  the  glandular 
trichomes  found  in  such  species  as  D.  gigantea,  and  distributed  over 
the  whole  plant  body  (75 — 16).  We  may  add,  at  this  point,  that 
the  fringes  of  trichome-like  structures  were  regarded  collectively  as  a 
ligule  by  Nitschke.  It  is  a  fringed  membrane  formed  at  the  sides  and 
across  the  leaf  base  in  D.  rotundifolia  and  some  other  species  {16  —  18), 
but  is  absent  from  many  others  {D.  Whittakeri,  D.  peltata,  D.  gigantea, 
etc.)  It  has  been  regarded  as  stipular  and  is  so  called  in  the  taxonomic 
literature  (Diels)  though  Small  (1939)  takes  another  view,  that  the 
apparent  membrane  is  merely  a  linear  cluster  of  trichomes.  That 
similar  trichomes  are  found  abundantly  on  the  rest  of  the  petiole  sup- 
ports his  contention.  On  the  other  hand  it  is  difficult  not  to  see  in 
the  huge  ligulate  "stipule"  possessed  by  some  species  {D.  paleacea, 
D.  pygmaea)  {16  —  18)  in  Australia,  in  which  they  serve  to  protect 
the  bud  during  periods  of  drought  (Diels),  an  integration  of  a  fringe 
as  it  occurs  e.g.  in  D.  rotundifolia. 

Tentacles.  —  Of  these,  the  stalked  glands  or  tentacles  are  the  most 
conspicuous  and  have  most  frequently  been  described.  They  have  often 
called  forth  exclamatory  remarks  of  wonder  at  their  complex  structure. 
They  have  been  described,  but  not  always  correctly,  by  Gronland, 
Trecul,  Nitschke,  Warming,  Darwin,  Huie,  Fenner,  Homes  and 
probably  others.  The  tentacles  occur  on  the  margin  and  upper  surface 
of  the  leaf  blade  and  in  some  species  on  the  tapering  upper  region  of 
the  petiole,  excepting  those  species  which  are  strictly  peltate. 

The  "tentacle"  consists  of  a  tapering  stalk  topped  by  an  oval  gland. 
The  stalk  arises  from  the  leaf  surface,  as  a  mass  of  tissue  including  all 
the  elements  of  the  leaf  structure,  epidermis,  parenchyma  and  vascular 
tissue.  The  terms  "trichome"  and  "hair"  are  therefore  not  suitable, 
though  they  have  been  used. 

The  term  "tentacle"  is  not  a  strict  one;  it  has  been  equated  with 
"emergence"  and  serves  if  we  think  of  the  tentacle  as  an  extension 
of  the  leaf  adapted  to  certain  functions  which  makes'them  so  trichome- 
like  that  they  are  no  longer  distinguishable  from  trichomes  (Diels). 
Nitschke  and  others  regarded  the  tentacles  as  extensions  of  the  leaf, 
Warming  as  trichomes  and  Penzig  as  intergradients  between 
phyllome  and  trichome. 


Chapter  X  — 121  —  Drosera 

In  the  upper  reach  the  tentacle  consists  of  the  epidermis  and  one 
course  of  parenchyma  cells  surrounding  a  very  slender  vascular  strand 
which  extends  from  the  leaf  system  up  into  the  gland  (75  —  6).  This 
was  seen  by  Meyen  in  1837,  who  supposed  that  it  entered  the  gland. 
This  structure  led  Trecul  (1855)  to  compare  the  tentacle  with  the 
dicotyledonous  stem,  and  to  regard  the  adventitious  buds  described 
first  by  Naudin  as  metamorphosed  tentacles.  Gronland  called 
them  lobes,  and  Schacht,  projections  of  the  leaf.  On  the  surface 
as  part  of  the  epidermal  system  there  are  a  few  small  sessile  glands, 
these  being  found  also  on  the  general  leaf  surface.  They  formed  con- 
venient marks  by  which  H.  D.  Hooker  was  able  to  record  changes 
in  the  length  of  the  tentacles  during  movement.  The  widened  base 
of  the  tentacle  has,  naturally,  an  increasing  number  of  parenchyma 
cells  as  the  general  leaf  surface  is  approached.  Similarly  the  vascular 
system,  consisting  of  spiral  tracheids,  may  here  consist  of  two  or  more 
vessels,  but  above  there  is  usually  found  only  a  single  strand  except 
where  two  may  overlap.  Fenner  did  not  see  any  phloem,  and  I  can 
only  support  him  in  this  (ij  —  7).  The  single  vessel  sets  into  a  dense 
mass  of  thick  and  short  tracheids  occupying  the  middle  of  the  gland 
(75  —  6)  which,  oval  in  form  save  when  on  a  strictly  marginal  tentacle, 
sits  atop  the  narrow  neck  of  the  stalk.  Those  tentacles  arising  from 
the  leaf  margin  are  bilaterally  symmetrical,  the  stalk  being  extended 
under  the  glandular  structure  proper  in  the  form  of  a  spoon  holding 
the  gland  in  its  bowl  (ij  —  9,  n;  16  —  1-3).  Darw^in  records  finding 
intermediate  forms,  which  I  have  also  seen.  The  tentacles  spring- 
ing from  the  surface  are  increasingly  radially  symmetrical  as  the 
margin  of  the  leaf  is  left,  are  oval,  and  present  the  following  struc- 
ture. 

The  oval  head  of  the  tentacle  consists  of  four  layers  of  cells  (75  — 
6,  8).  The  innermost  of  these  is  a  roughly  oval  mass  of  tracheids  which 
is  connected  by  means  of  the  vascular  strand  of  spiral  vessels  in  the 
stalk  with  the  system  in  the  leaf.  Surrounding  this  xylem  mass, 
three  outermore  layers  cover  it  as  a  thimble,  the  flaring  mouth  of  it 
articulating  with  the  somewhat  expanded  tip  of  the  stalk.  The  layer 
of  cells  in  contact  with  the  xylem  mass  is  distinctly  bell-shaped,  and 
was  called  by  Fenner  the  parenchyma  bell.  The  flaring  wall  of  the 
bell  is  composed  of  a  single  layer  of  elongated,  curved  cells,  the  ex- 
posed ends  of  which  come  to  the  surface  of  the  gland,  and  whose  cuti- 
cle is  continuous  with  that  of  the  gland  above  and  the  stalk  below. 
The  inner  ends  articulate,  at  a  point  about  half-way  up  the  bell,  with 
shorter  cells,  forming  the  top  of  the  bell.  Both  the  transverse  and 
longitudinal  walls  of  all  cells  are  cuticularized  so  that  when  a  gland  has 
been  treated  with  sulfuric  acid,  these  walls  remain  as  a  network  (75  — 
12)  or,  as  it  were,  a  cage  formed  of  a  continuous  band  of  cuticularized 
cell  wall.  In  transverse  section  this  band  is  T-shaped,  the  cross  bar  of 
the  T  being  narrow  and  placed  towards  the  outside  with  respect  to  the 
gland  as  a  whole.  Huie  believed  that  only  the  outer  part  of  the  wall 
(approximately  one-half)  is  cuticularized,  and  abuts  at  the  middle  of 
the  wall  on  a  pit  connecting  adjacent  bell  cells,  the  inner  moiety  of  the 
wall  being  Hgnified.  Fenner  did  not  see  this,  and  I  have  been  unable 
to  verify  Huie's  description.     This  parenchyma  bell  appears  to  func- 


Francis  E.  Lloyd  —  122  —  Carnivorous  Plants 

tion  as  an  endodermis,  though  Fenner  questions  Goebel's  view  that 
water  may  pass  only  in  one  direction  (outwardly).  The  outer  ends  of 
these  cells  form  a  continuous  single  row  of  rounded  outHnes  like  a  string 
of  beads,  seen  in  an  entire  gland,  which  limits  the  gland  proper  from  the 
uppermost  transverse  course  of  stalk  cells.  These  cells  were  seen  by 
Warming,  whose  drawing  Darwin  reproduces.  But  Darwin  (1875 
2d.  ed.,  p.  5)  himself  failed  to  see  them,  nor,  said  he,  did  Nitschke, 
though  one  of  his  drawings  seems  to  indicate  that  he  did.  Neither 
did  Gronland  (1855)  or  Trecul  (1855)  see  them. 

Fitting  over  the  parenchyma  bell  are  the  two  layers  of  glandular 
cells.  The  outer  course  is  made  up  of  columnar  epidermal  cells, 
polygonal  en  face,  their  outer  ends  covered  by  a  cuticle  and  their 
radial,  and  sometimes  outer  walls  strengthened  by  cellulose  buttresses 
and  beams  (75  —  13),  as  shown  by  Fenner.  They  are  most  pro- 
nounced throughout  the  lateral  reaches  of  the  gland  and  diminish  in 
stature  toward  its  apex,  from  which  they  are  quite  absent  (Huie), 
though  Homes  thinks  they  occur  here,  but  are  smaller,  in  much  smaller 
numbers  and  far  apart  (1928).  Careful  examination  persuades  me  to 
agree  with  Huie.  They  are  obvious  in  the  apical  cells  of  the  glands 
of  D.  pygmaea.  Naturally  enough,  the  protoplasm  of  the  cell  fits  into 
the  bays  between  the  buttresses,  and  by  the  use  of  weak  H2SO4  for 
maceration,  the  protoplasts  may  be  isolated  and  are  then  seen  edged 
with  crenellations,  interpreted  by  Haberlandt  as  sensitive  papillae. 
If  this  is  a  correct  view,  we  must  think  that  the  glands  are  more  sensi- 
tive along  their  sides  than  on  the  apex,  for  which  we  have  no  evidence 
one  way  or  another. 

The  cuticle  covers  over  the  whole  of  the  gland  and  is  continuous 
with  that  of  the  stalk.  As  Huie  has  said,  it  is  quite  continuous  and  is 
not  penetrated  by  pores  (Gardiner)  nor  is  it  absent  from  the  apical 
cells  (Goebel).  Goebel's  statement  to  this  effect  appears  to  have 
been  due  to  the  observation  of  the  earlier  penetration  of  solutes  through 
these  cells,  but  I  have  satisfied  myself  that  methylene  blue  enters 
equally  rapidly  over  the  entire  surface  of  the  gland.  Prolonged  treat- 
ment with  sulphuric  acid  leaves  a  very  delicate  continuous  membrane 
covering  it.  Yet  as  Huie  says,  the  cuticle  is  readily  penetrated  by 
silver  nitrate,  just  as  by  methylene  blue.  Another  observation  of 
Huie's  I  can  confirm,  namely,  that  in  life  the  lateral  walls  of  the 
apical  cells  are  often  separated  from  each  other  by  fissures  tapering 
inwardly  between  them,  as  if  the  walls  had  separated  along  the  middle 
fine.  It  is  possible  that  this  is  what  Franca  saw  in  Drosophyllum, 
interpreted  by  him  as  canals  leading  to  the  inner  course  of  glandular 
cells.  The  nucleus  of  these  cells  lies  near  the  base  and  the  cytoplasm 
has  a  large  vacuole  in  the  outer  moiety  of  the  cell  (in  the  resting  con- 
dition—  see  beyond  under  aggregation). 

The  second  layer  of  glandular  cells  lies  between  the  epidermis  and 
the  parenchyma  bell,  and  is  composed  of  more  depressed  and  irregular 
cells,  overlooked  by  Nitschke,  but  seen  by  Darwin,  and  correctly 
described  by  Warming.  The  cells  are  irregular  in  shape  fitting  the 
irregular  bases  of  the  epidermal  cells  without  intercellular  spaces. 
The  functions  of  these  two  glandular  layers  differ  according  to  Homes 
as  we  shall  see. 


Chapter  X —123—  Drosera 

The  emplacement  of  the  glandular  tissues  is  different  in  the  marginal 
tentacles.  Here  the  end  of  the  tentacle  stalk  is  formed  into  a  spoon, 
in  the  bowl  of  which  lies  the  gland.  There  is,  as  it  were,  a  torsion  of 
the  upper  part  of  the  tentacle  so  as  to  bring  the  gland  on  the  upper 
ventral  surface.  The  complete  homology  of  the  two  types  is  seen  on 
examination  of  a  transverse  section  of  the  marginal  gland  {13  —  9,  n; 

zd  —  I,  2). 

To  be  included  as  a  specialized  portion  of  the  gland,  or  better  a 
portion  of  the  tentacle  acting  in  a  specialized  way  in  cooperation  with 
the  gland,  is,  according  to  Fenner  (1904),  the  uppermost  course  of 
epidermal  cells  of  the  stalk,  those,  namely,  which  are  in  direct  contact 
with  the  tissues  of  the  gland  at  its  base.     These  cells  are  short  and 
being  epidermal,  they  form  a  circle  of  8-10  cells  called  by  Fenner  the 
"Halskranz",  or  as  we  may  call    them,    the   neck    cells.      Sometimes 
there  are  two  rows  of  neck  cells  (Konopka),  and  this  I  note  may  be 
the  case  in  D.  Whittakeri.     The  neck  cells  surround  the  parenchyma 
cells  of  the  same  transverse  course  but  these  latter  are  not  included  in 
the  "Halskranz",  as  defined  by  Fenner,  who  describes  the  anatomi- 
cal relations  as  follows.     The  neck  cells  are  in  contact  above  with  the 
lower  ends  of  the  emergent  parenchyma  bell  cells,  and  with  the  outer 
zone  of  the  xylem  mass  of  the  gland.     Inwardly  they  lie  in  contact 
with  the  short  parenchyma  cells  of  the  stalk,  these  in  turn  lying  against 
the  inner  zone  of  xylem  tracheids  and  with  the  end  of  the  stalk  vascu- 
lar bundle.     Below,   the  neck   cells  impinge   on   the   stalk  epidermis. 
They  are,  as  one  may  say,  in  a  strategic  position  to  carry  on  a  special 
function,  if  Fenner  is  right  in  his  interpretation.     That  they  have  a 
function  he  beheves  is  evidenced  by  the  presence  of  numerous  pits  in 
their  walls  which  He  against  the  parenchyma  bell  cells  and  those  of  the 
xylem,  and  furthermore,  by  the  fact  that  their  cuticle  is  porous.     He 
gives  the  following  interpretation.     The  neck  cells  receive  water  from 
the  bell  cells  which  bring  water  from  the  upper  part  of  the  xylem  mass, 
and  from  the  lower  xylem  cells,  presumably  also  from  the  parenchyma 
transversely  within  the  neck  cells,  and  pass  it  outwardly  through  the 
pores  of  the  cuticle  supplying  fluid  to  dilute  the  viscid  mucilage  se- 
creted by  the  glandular  cells  above.     The  glistening  drop  of  mucilage 
supported   on   the   tentacle   head   is,   says   Fenner,   pear-shaped,    the 
broad  part  of  the  drop  being  around  the  neck  cells  because  the  fluid 
exudes  chiefly  from  them.     The  reasoning  here  appears  disingenuous. 
Nor  is  his  statement  that  the  cuticle  is  porous  acceptable  since  dyes 
(methylene  blue)  never  enter  the  outer  surface  of  the  neck  cells,  but 
pass  into  the  stalk  only  by  diffusion  through  the  gland,  as  I  have 
verified  repeatedly.     While  crediting  Fenner  with  imagination,  it  is 
still  permitted  to  doubt  the  correctness  of  his  interpretation  and  even 
the  supposed  facts  on  which  it  is  based.     Konopka  indeed  has  taken 
issue  with  Fenner,  and  his  view  is  stated  beyond. 

The  development  of  the  tentacle  has  been  worked  out  by  Homes, 
and  it  becomes  evident  that  the  outermost  layer  of  the  gland  is  purely 
epidermic  in  origin,  as  would  appear  on  the  face  of  it.  The  second 
layer,  which  might  be  interpreted  as  of  epidermic  origin,  is  shown  to 
be  of  parenchymatous  origin.  The  third  layer,  the  parenchyma  bell, 
is    partly    epidermic    and    partly    parenchymatous   (Fenner).     Those 


Francis  E.  Lloyd         —124— Carnivorous  Plants 

cells  which  come  to  the  surface  at  the  base  of  the  gland  are  epidermic. 
They  are  narrower  and  longer  than  the  others,  which  are  of  parenchy- 
matous origin.  The  inclosed  mass  of  reticulated,  and  annular  and 
spiral  vessels  are  obviously  an  extension  of  the  leaf  vascular  tissue 
(j^_4_6).  The  developmental  behavior  of  the  gland  in  Drosera  cor- 
responds point  for  point  with  that  of  Drosophyllum  (Fenner). 

Functions  of  gland  parts.  —  Such  a  complicated  gland  as  above  de- 
scribed can  scarcely  be  a  simple  matter  physiologically.  The  reception 
and  transmission  of  stimuli,  the  secretion  of  mucilage,  of  one  or  more 
ferments,  probably  of  an  odoriferous  principle,  water,  and  in  the  op- 
posed direction,  the  absorption  of  the  products  of  digestion  are  car- 
ried on.  Is  it  possible  to  assign  any  degree  of  specialization  to  the 
various  elements  of  structure?  Homes  (19296),  having  studied  with 
meticulous  care  the  behavior  of  the  cells  in  the  matter  of  aggregation, 
assigned  to  the  outer  layer,  the  epidermis,  the  function  of  "responding 
directly  to  the  necessities  of  secretion  by  the  variation  of  its  vacuome". 
Its  cells  elaborate  the  substance  secreted.  That  of  the  second  layer  is 
the  regulation  of  osmotic  pressure.  The  third  layer,  the  parenchyma 
bell,  takes  no  part  in  secretion  (Homes,  1929^),  p.  49).  It  may  be  as- 
sumed, of  course,  that  the  cells  of  the  bell  allow  the  rapid  transfer  of 
water  from  the  inclosed  xylem,  but  whether  the  movement  is  a  one- 
way one  only,  as  Goebel  suggested,  or  not,  is  difificult  to  say. 

Reference  has  been  made  above  to  Haberlandt's  view  that  the 
protoplasmic  processes  lying  between  the  buttresses  of  the  epidermal 
cells  are  sensitive  organs,  analogous  to  those  seen  by  him_  in  tendrils 
and  other  plant  parts.  Konopka  preferred  another  suggestion  in  1930, 
that  the  increased  surface  due  to  crenellation  may  be  important  also 
in  secretion  and  absorption,  as  a  secondary  advantage.  Goebel  has 
regarded  them  in  this  way. 

With  respect  to  other  parts  of  the  gland  Konopka  has  made  some 
further  suggestions.  The  xylem  bundle  mass  is,  he  says,  composed  of 
spiral  vessels  of  narrower  bore  in  the  central  part,  with  wider  lumened 
tracheids  surrounding  them,  and  the  more  central  vessels  widen 
in  contact  with  the  apical  portion  of  the  gland.  The  central  vessels 
are  indeed  often  narrower  than  the  outer,  but  other  details  it  is  diffi- 
cult to  accede.  Konopka  would  attribute  different  functions  to  the 
two  regions,  but  beyond  this  regards  the  whole  as  a  water  storage 
organ,  which  rather  obviously  it  seems  to  be.  He  has,  however,  ex- 
amined the  behavior  of  the  nuclei,  and  finds  that  during  digestion  and 
absorption  there  occur  changes  in  them  which  he  interprets  as  con- 
nected with  taking  up  and  transmitting  nutrients  from  the  outer  tis- 
sues of  the  gland  to  the  stalk  cells.  He  asserts  that  the  nuclei  of  the 
endodermis,  of  the  xylem  and  of  the  stalk  cells,  show  a  gradient  of  such 
changes,  the  nuclei  of  the  more  superficial  tissues  showing  greater 
changes  in  a  quantitative  sense  than  those  of  the  deeper  and  more 
removed  tissues.  To  the  endodermis  (parenchyma  bell)  he  attributes 
the  special  function  of  a  protective  filter.  It  must  be  questioned 
whether  Konopka  has  advanced  sufficient  evidence  to  support  this 
hypothesis.  Aside  from  the  nuclear  changes  claimed  to  occur  by 
Konopka,  there  is  no  other  change  such  as  characterizes  the  secretion 
cells,  namely  aggregation  (Homes),  during  periods  of  activity.     This 


Chapter  X  — 125  —  Drosera 

seems  to  indicate  that  whatever  the  function  of  the  endodermis,  it  is  a 
different  one  from  that  of  the  secretion  layer,  and  this  I  believe  is  as 
far  as  we  can  go  in  interpretation  beyond  admitting  that  substances 
are  transmitted,  but  not  differentially. 

KoNOPKA  also  questions  Fenner's  view  about  the  neck  cells.  He 
does  violence  to  Fenner's  definition  of  the  neck  cells  by  including  the 
uppermost  parenchyma  cells  which  lie  somewhat  (but  very  little)  above 
the  level  of  the  ring  or  circle  ("Kranz")  of  neck  cells.  The  neck  cells, 
as  he  uses  the  term,  have  membranes  which  resist  the  action  of 
concentrated  sulfuric  acid,  and  are  similar  in  this  respect  to  the  endo- 
dermis cells.  Discarding  Fenner's  idea  that  they  are  especially  con- 
cerned with  the  transmission  of  water  to  the  surface,  he  thinks  that, 
on  the  basis  of  his  observation  of  the  nuclear  changes,  which  are  sim- 
ilar to  those  seen  in  the  endodermal,  tracheid  and  stalk  cells,  they 
transmit  absorbed  materials  downwardly  to  the  stalk.  This  seems  to 
be  a  simple  and  natural  view  of  the  matter.  But  I  have  been  unable 
to  see  cuticularized  walls  in  these  cells,  and  Fenner  says  nothing  of 
this  (75 —  12).  Nor  have  others  (Huie,  Homes,  myself)  seen  nuclei  in 
the  xylem  of  the  mature  gland. 

We  may  summarize  what  has  been  said  in  the  few  preceding  para- 
graphs by  emphasizing  the  very  complex  functioning  of  the  tentacle 
gland,  that  it  is,  as  a  mechanism,  relatively  complex  as  compared  with 
many  other  known  plant  glands,  but  that  we  are  far  from  recognizing 
specific  correlations  between  structure  and  function.  It  would  seem 
that  the  complexity  of  function  is  much  greater  than  recognizable 
structural  differentiation. 

Sessile  glands.  — ■  In  addition  to  the  stalked  glands  or  tentacles 
there  are  very  numerous,  small  sessile  glands,  or,  as  Darwin  called 
them,  "papillae".  They  were  described  for  the  European  species  by 
Nitschke  and  others,  and  in  detail  by  Fenner,  who  traced  their 
development.  They  are  to  be  found  on  both  leaf  surfaces,  on  the 
stalks  of  the  tentacles,  and  elsewhere  (petioles,  scapes).  The  glands 
project  dome-shaped  from  the  leaf  surface,  are  little  larger  than  the 
stomata  in  area,  and  consist  of  a  capital  of  two  cells,  which  may  be 
rounded  and  compact,  or  more  or  less  elongated  into  obliquely  placed 
cylinders.  These  stand  on  a  short  stalk  of  compressed  cells  in  two 
courses,  each  course  of  two  cells.  The  basal  cells  have  cuticularized 
inner  walls.  These  in  turn  stand  on  two  epidermal  cells  (75 — -18). 
Fenner  describes  also  a  variant  of  the  fundamental  form.  It  occcurs 
on  the  petioles,  and  consists  of  a  more  or  less  elongated  stalk  with  a 
capital  of  about  four  cells. 

The  origin  of  the  sessile  glands  is  purely  epidermal  (Fenner). 
The  mother  cells  are  two  short  epidermal  ones  which  by  tangential 
division  give  rise  to  a  pair  of  capital  cells,  the  base  of  which  is  again 
cut  off  to  make  stalk  cells.  The  remaining  true  capital  cells  are  two 
in  number  and  may  remain  rounded,  or  elongate  more  or  less  into  two 
divergent  short  cylindrical  cells,  seen  on  the  base  of  the  tentacles  and 
on  the  petiole  (Nitschke).  In  D.  Whittakeri  these  glands  are  much 
larger  and  more  complicated  in  structure  and  consist  of  twelve  cells, 
eight  outer  surrounding  a  core  of  four  inner,  the  whole  being  supported 
on    a   very   short   biseriate    stalk   of   longitudinally   compressed    cells. 


Francis  E.  Lloyd  —  126  —  Carnivorous  Plants 

Other  glandular  trichomes  occur  in  D.  gigantea  (seen  by  Darwin)  and 
probably  in  other  species.  These  are  stalked,  bear  an  oval  gland,  and 
look  superficially  like  the  tentacles,  but  do  not  have  their  elaborate 
differentiation.  They  are  to  be  found  scattered  on  the  petioles  and 
stems;  on  the  latter  they  are  quite  numerous.  I  failed  to  observe  any 
secretion.  Though  the  gland  is  covered  with  cuticle,  they  absorb  dye 
readily.  Their  structure  is  indicated  in  i§  —  i6.  In  origin  they  are 
epidermal,  but  in  the  base  there  is  a  small  involvement  of  parenchyma 
as  it  is  rather  broad,  the  stalk  tapering  upward  into  a  uniseriate  por- 
tion just  beneath  the  gland.  What  function  these  can  serve,  if  any,  is 
not  known.     Small  flies  have  been  observed  sticking  to  them. 

Function  of  sessile  glands.  —  Darwin  observed  that  aggregation 
takes  place  in  the  sessile  glands  during  the  digestion  of  prey,  and 
thought  therefore  that  they  are  concerned  in  the  absorption  of  sub- 
stances derived  therefrom,  "but  this  cannot  be  the  case  with  the  pa- 
pillae on  the  backs  of  the  leaves  or  on  the  petiole."  It  is  not  clear  if 
he  meant  this  merely  because  of  unfavorable  position.  But  Fenner 
held  that  the  sessile  glands  of  the  concave  leaf  surface  are  alone  capable 
of  absorption,  pointing  out  that  those  of  the  dorsal  surface  are  small, 
and  usually  lose  the  capital  cells.  The  active  glands  display  cytoplas- 
mic changes  (Darwin's  aggregation  evidently)  during  the  absorption 
of  nutriment.  Because  nuclear  changes  also  intervene,  Rosenberg 
aligned  himself  with  these  authors.  To  all  this  Konopka  opposes  a 
contrary  opinion.  Nuclear  changes  such  as  Rosenberg  observed  are 
also  to  be  seen  in  other  glands,  certainly  not  concerned  in  the  absorp- 
tion of  substances;  and  the  "middle  layer"  (endodermis)  also  is  to  be 
found  in  nectaries,  hydathodes,  etc.  He  believes  the  sessile  glands  to 
be  hydathodes.  They  never,  he  continues,  show  such  far-reaching 
changes  in  nuclear  behavior  as  do  the  tentacle  cells,  and  there  never 
occur  the  "  Digestionsballen "  which  he  found  in  tentacle  gland  cells. 
Nor  have  the  glands  any  connection  with  the  vascular  tissues;  they 
develop  much  earlier  than  the  tentacles,  and  occur  on  both  leaf  faces. 
These  points  argue  that  the  sessile  glands  are  not  absorptive.  There 
is,  Konopka  believes,  much  greater  probabihty  that  they  serve  the 
purpose  of  water  secretion.  In  support  of  this  view  he  cites  as  facts 
(a)  the  "not  small"  vascular  system  of  the  roots;  (b)  the  rich  supply 
of  root  hairs;  (c)  the  wetness  of  the  substrate;  (d)  the  active  passage 
of  water  through  the  plant  and  (e)  the  high  relative  humidity  of  the 
habitat,  tending  to  reduce  transpiration.  And  Schmid,  he  says,  had 
found  that  there  is  only  a  slow  transfer  of  water  to  the  tentacle  glands 
following  the  experimental  removal  of  the  mucilage  drop,  while  on  the 
capture  of  prey  there  is  an  extraordinary  increase  of  fluid  supplied 
from  the  leaf  during  the  digestion  of  prey  (as  Darwin  and  others  have 
observed),  all  speaking  for  a  process  of  guttation.  Admitting  the 
above  as  facts  (though  Schmid 's  results  seem  to  question  some  of 
them)  Konopka  arrives  at  an  interesting  interpretation  of  the  whole 
situation:  the  sessile  glands  draw  off  water  from  the  leaf,  supplying  it 
for  the  process  of  digestion  and  thus  at  the  same  time  exert  suction  on 
the  tentacles,  thus  increasing  absorption  by  them.  These  glands,  he 
says,  may  be  roughly  compared  with  the  animal  kidney  which  with- 
draws water  from  the  body  thus  making  room  for  more  to  be  absorbed. 


Chapter  X  —  127  —  Drosera 

In  support  of  the  idea  he  recalls  the  case  of  the  trap  of  Utricularia, 
which  is  known  to  excrete  water  from  the  glands  on  its  outer  surface 
(glands  not  much  dissimilar  from  the  ones  in  question)  and  to  absorb 
nutrition  and  water  from  the  interior  by  means  of  the  bifid  and  quad- 
rifid  trichome  glands.  Since  these  two  sets  of  glands  in  Utricularia  are 
the  only  non-cuticularized  areas  of  the  inner  and  outer  surfaces  of  the 
trap  and  since  the  cuticle  elsewhere  is  impermeable  {e.g.  to  dyes)  we 
are  forced  to  recognize  its  pecuHar  glandular  action  as  involving  the 
two  sets  of  glands,  as  Czaja,  Merl  and  Nold  have  beHeved.  This 
view  would  harmonize  our  ideas  about  the  two  apparently  widely 
different  structures,  leaf  and  trap. 

The  free  flow  of  watery  secretion  observed  during  the  earlier  stages 
of  digestion  or  just  previous  thereto,  even  if  Konopk.a.'s  view  is  correct, 
does  not  preclude  the  possibility  that  the  sessile  glands  may  not  con- 
tribute to  the  efficiency  of  the  leaf  by  exercising  the  function  of  ab- 
sorption as  well.  We  may,  therefore,  direct  our  attention  briefly  to 
the  specific  question  of  locus  or  loci  of  absorption  of  the  leaf. 

The  locus  of  absorption.  —  Previous  to  the  studies  of  Oudman,  there 
had  always  been  a  vagueness  about  the  point  of  entrance  of  substances 
absorbed  by  the  leaf.  Three  possibilities  there  are:  (i)  that  they  enter 
through  the  tentacles;  or  (2)  through  the  papiUae;  and  (j)  through  the 
epidermis,  which  according  to  Nitschke,  has  no  cuticle.  The  last  may 
be  at  once  excluded  as  Nitschke's  statement  is  not  true.  Aside  from 
direct  proof  with  sulfuric  acid,  the  dift'usion  of  e.g.  caffeine  (Kok)  into 
the  leaf  takes  place  through  the  papillae,  and  not  through  nearby 
epidermal  cells. 

With  regard  to  the  tentacles  the  fact  of  aggregation  in  the  stalk 
cells  following  on  the  application  of  various  substances  (insects,  caffeine, 
etc.)  would  seem  to  indicate  at  once  that  absorption  can  and  does  take 
place  through  the  glands.  Darwin  indeed  regarded  aggregation  as 
proof  of  absorption.  Pfeffer,  however,  pointed  out  that  this  might 
be  the  result  of  the  stimulating  eft'ect  of  minimal  quantities  of  ma- 
terial with  no  quantitative  relations  indicating  absorption.  Some  such 
substance  has  been  thought  to  be  necessary  to  procure  aggregation, 
that  is,  a  specific  aggregation-stimulating  substance  formed  in  the 
gland  (Akerman,  191 7;  Coelingh,  1929).  Ali  Kok  determined  the 
rate  of  transport  of  caffeine  from  the  glands  into  the  tentacle  stalks. 
Changes  in  the  structure  of  the  cytoplasm  and  nucleus  (studies  by 
HuiE,  Rosenberg,  Konopka  and  Ziegenspeck,  and  Kruck  on  Utricu- 
laria), were  referred  by  them  to  the  activity  of  these  structures  (cyto- 
plasm and  nucleus)  in  response  to  the  absorption  of  various  foods. 
Taking  up  of  food  by  the  tentacles  has  been  generally  assumed,  as 
e.g.  by  GoEBEL,  Fenner,  Ruschmann.  Oudman  points  out,  however, 
that  there  is  little  positive  information  and  that  even  if  the  tentacles 
do  absorb,  their  role  may  be  small  and  of  secondary  significance. 

That  the  papillae,  small  sessile  glands  of  various  sizes,  smallest  on 
the  tentacle  stalks,  largest  on  the  leaf  blade,  where  they  occur  on  both 
surfaces,  are  concerned  in  absorption  has  been  expressed  by  Darv;in, 
and  by  Rosenberg,  both  of  whom  saw  the  ready  passage  of  sub- 
stances through  them  into  the  tissues.  Rosenberg  used  methylene 
blue   (as  I  have  repeatedly  done).     Fenner  and  Coelingh,  as  also 


Francis  E.  Lloyd  —128— Carnivorous  Plants 

Darwin  and  Rosenberg,  saw  that  aggregation  and  granulation  occur 
in  response  to  the  entrance  of  various  substances,  but  this  is  true  of 
the  tentacles,  also,  and  proves  as  much  and  as  little  in  both  cases. 
To  be  sure  it  was  thought  that  the  papillae  produce  no  secretion  ex- 
ternally escaping,  and  this  has  perhaps  influenced  the  judgment.  As 
OuDMAN  remarks,  here  also  as  in  the  case  of  tentacles  quantitative 
results  had  not  been  forthcoming.     He  therefore  endeavored  to  supply 

these. 

Having  first  assured  himself  that  the  N- content  of  the  leaves  (of 
Drosera  capensis)  under  the  circumstances  under  which  he  worked,  is 
nearly  constant,  Oudman  then  arranged  a  simple  experiment  (i)  so 
that  the  more  marginal  tentacles  were  surrounded  by  agar  (2%),  with 
asparagin  (1.5%),  and  (2)  so  that  the  mixture  was  poured  on  the  back 
of  the  leaf  taking  precautions  against  capillary  flow.  He  obtained 
these    results : 


Treatment  of  the  Leaf 


N   IN    %   OF        INCREASE   IN 
FRESH   WEIGHT         24   HOURS 


Control                                                                 2.07                        — 
Asparagin  on  the  marginal  tentacles               3.54                     1.47 
Asparagin  on  the  back  of  the  leaf                   3.31                      1.24 

A  second  experiment,  greater  precautions  against  capillary  flow:  — 

Control                                                                 2.01                        — 
Asparagin  on  the  bordering  tentacles              3.53                      1.52 
Asparagin  on  back  of  the  leaf                          3.38                     1.37 

From  these  figures  it  was  evident  that  asparagin  is  taken  up  both 
by  the  tentacles  and  by  the  back  of  the  leaf.  By  comparing  the  total 
area  of  the  tentacle  glands  with  that  of  the  back  of  the  leaf  he  found 
that  the  amount  of  asparagin  absorbed  by  the  tentacles  was  six  times 
that  absorbed  by  the  back  of  the  leaf.  Two  explanations  presented 
themselves,  namely,  either  that  the  tentacle  heads  (glands)  are  better 
adapted  to  this  purpose  than  the  leaf  epidermis  (which  would  be  ruled 
out  by  the  fact  that  the  epidermis  is  cuticularized,  as  above  said); 
or  that  the  absorption  by  the  leaf-back  takes  place  only  at  certain 
points,  that  is,  through  the  papillae,  through  which  it  has  been  ob- 
served that  entrance  can  take  place  (Darwin,  Rosenberg,  Kok). 
Oudman  adopted  the  latter  view,  and  inferred  that  in  nature  both  the 
tentacles  and  the  papillae  are  made  use  of  for  the  absorption  of  food, 
but  rather  the  papillae  of  the  upper  side  of  the  leaf  than  those  of  the 
lower.  Oudman  also  examined  into  the  question  of  the  influence  of 
various  factors  (temperature,  concentration  of  the  applied  materials, 
the  course  of  absorption  in  relation  to  time,  the  nature  of  the  ap- 
pHed  material,  the  influence  of  the  glands  and  narcosis). 

As  would  be  expected,  the  higher  the  temperature  within  physio- 
logical limits,  the  more  rapid  the  absorption.  But  whether  this  is 
due  to  the  greater  rapidity  of  transportation,  or  to  the  greater  uptake 
by  the  glands,  does  not  appear.  The  same  with  increasing  concentra- 
tions of  applied  substance  (asparagin).  In  the  course  of  absorption, 
the  rate  was  greater  after  the  first  period  (3-6  hrs.),  than  at  first,  and 
falls  off  again  after  9  hours.    This,  it  may  be  suggested,  may  be  due  to 


Chapter  X —129— Drosera 

the  dilution  of  the  applied  material  by  the  secretion  of  the  glands 
during  the  beginning  period,  and  to  equiHbrium  during  the  later  period. 

All  substances  are  not  absorbed  at  equal  rates.  Darwin  noted 
that  they  did  not  procure  aggregation  at  the  same  rate.  Oudman 
found  that  caffeine  is  much  more  rapidly  absorbed  than  asparagin, 
although  the  latter  has  the  smaller  molecule.  This  may  be  due  to  the 
path  taken.  Caffeine  enters  the  vacuole  and  is  there  precipitated,  and 
fresh  caffeine  must  traverse  the  zone  of  precipitation.  Asparagin 
probably  passes  along  the  path  provided  by  the  protoplasm.  By 
following  the  localization  of  fluorescence  it  was  shown  that  fluorescein 
does  this.  If  the  tentacles  are  removed,  leaving  the  stalks  open  at  the 
outer  end  (due  to  the  operation),  less  material  is  absorbed,  but  the 
difference  is  not  related  to  the  exposed  surface,  it  being  much  greater 
for  tentacles  with  the  glands  removed.  The  glands  therefore  offer 
some  hindrance,  perhaps  because  they  are  quite  complex  organs,  excreting 
at  the  same  time  as  absorbing.  The  presence  of  an  endodermis  (the 
parenchyma  bell,  Fenner)  may  have  some  regulatory  effect,  but  this 
is  not  known  to  be  the  case.  It  is  worthy  of  note  that  narcosis  (with 
ether)  inhibits  the  penetration  of  asparagin  more  than  caffeine,  the 
former  traversing  the  protoplasm,  the  latter  the  vacuole.  Caffeine  is 
known  to  penetrate  into  the  vacuole  with  great  rapidity  (Bokorny, 
Akerman,  Erna  Janson)  and  in  any  event  it  has  to  pass  only  a  thin 
layer  of  cytoplasm  while  asparagin  is  forced  to  pass  lengthwise  the 
cells  within  the  cytoplasm. 

In  a  later  paper  by  Arisz  and  Oudman  (1937),  making  use  of  an 
improved  method  of  applying  the  reagents  to  the  tentacles,  Oudman's 
figures  describing  the  rate  of  absorption  of  caffeine  and  of  asparagin 
were  confirmed.  Caffeine  is  absorbed  in  the  fashion  of  a  physical 
diffusion,  while  asparagin  shows  a  maximum  penetration  in  the  second 
period,  and  low  rates  in  the  first  and  third  periods.  Nevertheless  more 
asparagin  penetrated  into  the  leaf  blade  as  shown  by  tests  after  the 
removal  of  the  tentacles  before  analysis.  It  seems  obvious  that  the 
conclusion  that  the  paths  followed  by  these  substances  are  different  is 
justified,  namely  that  caffeine  travels  by  way  of  the  vacuoles  and 
asparagin  through  the  cytoplasm,  yet  in  spite  of  the  narrowness  of  the 
path  through  the  cytoplasm,  the  latter  moves  more  readily.  This  again 
seems  to  be  due  to  the  taking  up  of  the  caffeine  by  precipitation,  a 
subsequent  wave  of  diffusion  having  to  overstep  the  zone  of  pre- 
cipitation. 

An  attempt  was  made  by  Arisz  and  Oudman  to  determine  the  in- 
fluence of  aggregation  upon  the  transport  of  asparagin.  Aggregation 
was  first  induced  by  suitable  reagents  (sahcin  0.25%  and  KH2PO4 
0.1%  solutions)  with  a  "remarkable  result"  that  now  more  asparagin 
was  taken  up  during  the  first  period  (contrary  to  the  above  mentioned 
rates).  Since  asparagin  itself  causes  aggregation,  during  the  first 
period  aggregation  takes  place,  and  during  the  second  period,  ag- 
gregation now  having  taken  place,  penetration  goes  on  more  rapidly 
because  of  this  earlier  induced  aggregation.  This  behavior,  that  is, 
aggregation,  has  on  the  other  hand  no  effect  on  the  rate  of  transport 
of  caffeine. 

Reproduction  by  seeds  and  by  buds  {"regeneration'').  —  While  Dros- 


Francis  E.  Lloyd  —  130  —  Carnivorous  Plants 

era  reproduces  itself  through  seeds,  it  is,  on  the  other  hand,  extraor- 
dinarily prohfic  by  means  of  non-sexual  multipHcation  making  use  of 
brood  bodies  {D.  pygmaea,  Goebel)  and  tubers,  of  strong  axillary  buds 
and  especially  and  above  all  of  budding  from  the  leaves.  So  frequently 
and  vigorously  is  the  last  method  used  that  it  would  seem  to  rival 
that  by  seed  (Behre). 

The  seedlings  are  very  small,  the  cotyledons  either  escaping  from 
the  seed  coat  (Nitschke,  Lubbock,  Goebel)  or  remaining  perman- 
ently embedded  therein  {D.  peltata  and  D.  auriculata,  Vickery  1933). 
The  earlier  leaves  in  all  cases  are  rounded  (spatulate),  indicating  this 
to  be  the  primitive  form  for  this  genus  (Leavitt,  1903.  1909).  The 
leaf  blades  are  provided  with  a  few  glands,  both  marginal  (Nitschke) 
and  on  the  disc,  5  on  each  (D.  rotundifolia,  Leavitt).  The  radicle 
is  short,  provided  with  root  hairs  and  fugacious.  As  the  shoot  develops, 
adventitious  roots  put  out  from  the  stem,  and,  as  this  dies  away  with 
the  extension  of  growth,  new  adventitious  roots  are  produced  above. 
The  root  system  cannot  be  said  to  be  abundant  (Schmid). 

In  some  species,  e.g.  D.  rotundifolia  (Nitschke),  the  axillary  buds 
below  the  rosette  form  at  once  secondary  rosettes,  similar  to  the  chief 
rosette,  and  as  the  stem  decays  they  are  separated,  to  propagate  the 
plant.  In  one  group  (Ergaleium)  tubers  are  formed.  These  have  been 
described  in  their  static  condition  by  Diels  (1906)  and  Morrison 
(1905),  and  very  fully,  from  the  point  of  view  of  development, 
by  Vickery,  from  whose  paper  (1933)  the  present  account  is  taken. 
She  worked  with  the  two  species  D.  peltata  and  D.  auriculata  which  I 
saw  growing  about  Sydney,  N.  S.  W.  When  exhumed,  the  stem  below 
the  epigaeal  rosette  extends  downward  a  matter  of  a  few  centimeters, 
is  clothed  with  scale  leaves,  and  emerges  from  a  small  hard  rounded 
tuber  clothed  with  loose  membranous  envelopes,  which  when  peeled 
off  leave  a  smooth  white  tuber.  This  at  the  upwardly  directed  apex 
bears  an  "eye",  a  depressed  scaly  bud  which  can  develop  into  a  new 
plant  {16  ■ —  II,  12).  The  genesis  of  this  structure  is  seen  in  the  seed- 
ling as  an  axillary  shoot  bearing  normally  only  scales  and  growing 
downwards  {16  —  13).  This  is  a  "dropper".  Reaching  a  certain 
depth  the  end  bends  upward,  and  develops  into  a  corm.  While  this 
structure  normally  elongates  upward  to  form  a  rosette  at  the  surface 
of  the  ground,  if  more  or  less  exposed  to  light  it  may  produce  at  once  a 
partial  or  complete  rosette  of  normal  leaves.  Such  leaves  may  arise 
even  from  the  extending  dropper  instead  of  scale  leaves.  An  old  tuber, 
as  it  becomes  exhausted,  is  usually  replaced  by  another  produced 
laterally  on  the  end  of  the  dropper  axis  close  to  it.  In  Australia  es- 
pecially this  form  of  reproduction  is  of  common  occurrence. 

The  underground  tubers,  as  Goebel  has  pointed  out,  are  doubtless 
important  as  storage  reserves  of  food  and  water  which  can  tide  the 
plant  over  during  a  season  when  the  rosette  of  leaves  disappears.  Some 
of  the  Australian  species  have  strong  coloring  matter  in  their  tissues, 
as  is  evident  from  the  staining  of  herbarium  sheets  on  drying.  It  con- 
tains two  substances,  a  red  one  CuHsOs,  and  a  yellow  C11H8O4,  the 
latter  in  only  small  amounts.  Rennie  (1893)  had  shown  "that  the 
Os-compound  formed  a  triacetate  and  was  probably  a  trihydroxy- 
methylnaphthaquinone,  whereas    the    04-compound    gave    a    diacetate 


Chapter  X  —131— Drosera 

and  appeared  to  be  a  dihydroxymethylnaphthaquinone."  This  was 
confirmed  by  Macbeth,  Price  and  Winzor,  who  called  these  sub- 
stances hydroxydroserone  and  droserone  respectively,  determining  the 
constitution  of  the  hydroxydroserone. 

Reproduction  by  means  of  gemmae.  —  The  case  of  D.  pygmaea  de- 
scribed by  GoEBEL  (1908)  is  one  of  a  small  group  of  species  in  which  a 
very  highly  specialized  method  of  non-sexual  reproduction  takes  place, 
viz.,  by  means  of  gemmae.  D.  pygmaea  is  a  very  small  plant,  about 
1.5  cm.  in  diameter,  and  consists  of  a  tight  rosette  of  minute  acentri- 
cally  peltate  leaves  with  fleshy  petioles  which  appear  to  be  the  im- 
portant chlorophyllous  parts.  On  the  approach  of  the  resting  season 
there  are  formed  small  brood  bodies,  resembling  superficially  those  of 
Marchantia,  clustered  in  the  center  of  the  rosette.  The  gemma  itself 
is  a  small,  ovate,  hard  mass  of  tissue,  flattish  on  the  dorsal  surface,  with 
a  deep  depression  at  the  base  of  the  ventral  surface,  in  which  develops 
a  minute  bud  which  gives  rise  to  a  plant  {16  —  14-^17).  At  the  base  it 
is  attached  to  a  cylindrical  hyaline  stalk  of  some  length.  At  the  point 
of  attachment  to  the  brood  body  it  is  constricted,  and  is  here  fragile, 
so  that  the  brood  body  is  easily  detached.  The  stalk  is  marcescent, 
drying  up  iw  situ.  The  brood  bodies  measure  about  0.5  by  0.7  mm. 
and  contain  an  abundance  of  food  in  the  form  of  fat  and  starch. 

I  received  material  of  D.  pygmaea  collected  by  Dr.  Pat  Brough 
near  Sydney,  N.  S.  W.,  in  response  to  my  request,  on  two  occasions, 
viz.,  in  Nov.,  1939  and  in  April,  1940.  In  the  former  no  signs  of  gem- 
mae were  to  be  found;  in  the  latter  they  were  present  in  various  stages 
of  development.  In  none  of  the  specimens  could  brood  bodies  be  seen 
openly  exposed,  as  represented  in  Goebel's  drawing  (1908).  The  plants 
were  perhaps  still  too  young.  The  structure  of  the  gemmae  was  as  Goebel 
described  them.  He  suggested  their  homology  with  leaves,  but  it  is  to 
be  noticed  that  there  is  no  suggestion  of  stipules.  They  arise  in  a 
ring  about  a  dished  growing  point,  and  stand  in  several  ranks  around 
it  {16  —  17).  Around  them  young  leaves  have  already  begun  develop- 
ment, the  older  of  these  expanding.  The  gemmae  seem  therefore  to 
represent  the  culmination  of  a  growth  period,  and  they  would  be 
set  free  during  the  winter  season  in  the  natural  habitat.  Professor 
Buller  suggests  to  me  that  the  rosette,  with  its  gemmae  at  the  center, 
may  be  regarded  as  a  "splash  cup",  Hke  those  of  the  bird's  nest  fungi. 

Of  much  more  general  occurrence  is  another  method,  namely,  by 
budding  from  the  leaf.  This  is  by  no  means  of  recent  observation. 
First  seen  by  Naudin  in  1840,  it  has  been  described  by  numerous 
others,  at  least  thirteen  in  number.  The  historical  aspect  of  this  mat- 
ter has  been  well  summarized  by  Behre  (1929). 

Naudin  in  D.  intermedia  (1840)  and  Kirschleger  (1855)  in  D. 
longifolia  had  observed  the  fact  of  budding  from  the  leaf  surfaces,  and 
that  the  origin  was  "probably  endogenous"  (Naudin).  Nitschke's 
account  was  sufficiently  extended  and  exact  so  that  Behre  found  little 
to  correct,  so  far  as  general  morphology  was  involved.  The  earliest 
anatomical  study  was  made  by  Beijerinck  (1886),  estabUshing  the  exo- 
genous origin  of  the  leaf  buds.  Leavitt  (1899,  1903,  1909)  pointed 
out  that  the  earlier  leaves  of  the  leaf  buds  of  even  such  extreme  forms 
as  D.   binata,   have   rounded   leaves  characteristic  of  D.   rotundifolia, 


Francis  E.  Lloyd  —132— Carnivorous  Plants 

regarding  this  a  repetition  of  phylogeny.  Winkler  (1903)  observed  the 
lack  of  polarity  in  the  occurrence  of  leaf  buds  in  D.  capensis,  as  in 
Torenia  and  Begonia,  and  further  for  the  first  time  showed  clearly  that 
the  buds  arise  not  from  retained  embryonal  tissue,  but  by  redifferentia- 
tion  of  the  leaf  tissues. 

Exact  studies  of  the  mode  of  origin  of  the  adventitious  buds  of  the 
leaf  surface  have  been  made  by  Behre  (1929)  and  by  Vickery  (1933), 
the  latter  author  independently  confirming  the  former  in  all  essentials. 
Such  leaf  buds  arise  on  the  blade  always  from  the  bases  of  tentacles, 
usually  on  the  adaxial  surface,  but  occasionally  laterally  or  even  adax- 
ially  (Behre).  They  are  often  visible  in  a  few  days  if  during  that  time 
the  leaf  has  been  separated  from  the  plant  and  kept  under  moist  con- 
ditions. The  cells  involved  have  in  all  cases  arrived  at  maturity,  and 
there  is  no  sign  of  the  persistence  of  embryonic  tissue.  The  cells  there- 
fore undergo  a  true  rejuvenation  passing  from  an  adult,  vacuolated 
condition  into  one  of  high  protoplasmic  content  with  accompanying 
changes  in  the  nucleus.  They  then  undergo  cell  division  previous  to 
growth,  the  earliest  divisions,  in  general,  being  anticlinal,  followed  by 
perichnal  {16  —  7,  8).  Increase  in  size  now  overtakes  the  newly  active 
cells,  and  a  simple  outgrowth  emerges  exogenously,  this  gradually  in- 
volving the  whole  of  the  base  of  the  tentacle  (Vickery)  {16  —  9,  10). 
The  vegetation  point  having  been  defined  at  the  scene  of  the  earliest 
divisions,  this  is  now  raised  by  the  growth  activities  of  the  paren- 
chyma of  the  upper  moiety  of  the  mother  leaf  in  the  immediate  vicinity, 
carrying  up  the  tentacle  so  that  this  now  appears  to  arise  from  the  bud, 
rather  than  the  bud  from  it.  Whether  the  new  vascular  tissue,  that  of 
the  bud,  becomes  articulated  with  the  older,  that  of  the  leaf,  is  not 
clear.  Doubtless  this  occurs  if  the  leaf  does  not  decay,  as  observed  by 
Vickery.  If,  however,  the  leaf  does  decay,  this  may  be  questioned. 
Robinson  (1909)  asserts  that  no  connection  occurs.  The  vegetation 
point  having  been  established,  leaves  appear  on  the  bud  and  a  new 
plantlet  becomes  established,  roots  being  formed  secondarily.  The 
earlier  leaves  frequently  show  abnormalities,  as  I  have  observed, 
such  as  the  lateral  fusion  of  contiguous  leaf  primordia,  producing  more 
or  less  laterally  doubled  leaves.  Nepionic  leaves  occur.  Leavitt 
(1903)  was  able  to  produce  such  even  from  the  terminal  bud  by  cutting 
off  the  stem  below  it  and  removing  the  leaves  as  they  expanded.  D. 
intermedia,  which  bears  only  radially  symmetrical  tentacles  normally, 
under  such  condition  of  ''malnutrition  "  bears  on  nepionic  leaves 
spoon-shaped  lateral  tentacles  like  those  of  D.  rotundifolia.  The  fre- 
quency and  ease  with  which  all  this  occurs,  as  already  mentioned, 
makes  it  probable  that  this  method  of  reproduction  rivals,  in  its  re- 
sults, reproduction  by  seed.  I  have  at  my  hand  now  a  small  flower 
pot  which  a  few  months  ago  carried  three  small  plants  sent  to  me  from 
Ontario  by  my  friend  Professor  R.  B.  Thomson.  These  at  the  present 
writing  have  died  down  to  winter  buds,  and  I  count  at  least  a  dozen 
minute  plantlets  which  I  observed  to  have  arisen  from  old  and  at 
length  decaying  leaves. 

Behre  has  further  described  the  origin  of  plantlets  from  the  leaf 
stalk.  As  in  the  case  of  the  blade,  such  always  occur  on  the  upper 
surface,  with  the  exception  of  D.  capefisis  and  D.  binata,  in  which  they 


Chapter  X  — 133  —  Drosera 

may  occur  on  the  under  side.  Due  to  the  different  anatomical  struc- 
ture, the  origin  is  more  various,  for  the  epidermis  may  not  in  all  cases 
take  active  part  in  the  earlier  cell  divisions.  These  occur  usually  in 
the  vicinity  of  stomata  or  near  the  bases  of  trichomes  or  of  sessile 
glands,  but  can  arise  also  on  the  stalk  of  the  inflorescence  or  even  from 
the  latter  itself,  as  axillary  buds  however  (Robinson  1909).  Since  the 
flower  stalk  is  radial  in  structure,  the  buds  arise  on  all  sides,  and  on 
account  of  the  closed  cylinder  of  sclerenchyma,  they  never  articulate 
with  the  vascular  system  of  the  flower  stalk.  Adventitious  buds  may 
arise  from  roots  also,  in  which  case  they  are,  as  would  be  expected, 
endogenous  in  origin. 

In  the  case  of  D.  spathulata  Behre  found  regeneration  by  bud  for- 
mation to  take  place  indirectly  from  callus,  previously  formed  on  the 
cut  end  of  a  leaf  stalk. 

Miss  MouLAERT  (1937)  obtained  adventitious  buds  from  leaves, 
isolated  petioles,  hypocotyls,  stems,  scapes,  receptacles  and  sepals. 
Following  the  formation  of  epiphyllous  buds,  she  observed  the  develop- 
ment of  cushions  of  tissue  ("bourrelets")  extending  from  the  base  of 
the  plantlet  toward  the  petiole.  These  are  of  three  kinds,  those  which 
remain  as  mere  thickenings  in  the  parenchyma  above  the  veins,  and 
which  she  called  "undifferentiated";  those  which  act  as  a  liaison  be- 
tween the  plantlet  and  a  root  which  has  already  differentiated  ad- 
ventitiously nearby  and  in  which  a  vascular  connection  between  shoot 
and  root  becomes  established;  and  third,  a  kind  which  is  formed  near 
the  plantlet  which  does  connect  with  it,  an  example  of  "affolement 
cellulaire. " 

Another  observation  made  by  Moulaert  is  the  occurrence  of  ab- 
sorbing hairs,  structures  quite  like  root  hairs,  which  arise  from  the 
upper  surface  of  the  leaf  blade  or  from  the  basal  part  of  the  stem  of 
the  plantlet.  They  are  very  abundant  and  their  walls  are  brown  as 
in   the  case  of  root  hairs. 

Conditions  determining  the  incidence  of  leaf  buds.  —  It  has  gen- 
erally been  observed  that  the  production  of  adventitious  buds  takes 
place  only  under  conditions  of  high  humidity,  and  apparently  the 
higher  the  better.  In  order  to  obtain  them  the  practice  is  to  remove 
leaves  and  place  them  on  moist  moss,  or  float  them  on  water,  in  cov- 
ered vessels  (Graves  1897;  Grout  1898;  Ames  1899;  Robinson  1909; 
Leavitt  1903;  Salisbury  191 5;  Vickery  1933,  and  others).  But  the 
matter  seems  not  to  be  quite  so  straight-forward  as  this.  Dixon  (1901) 
found  that  such  buds  occur  on  plants  in  abundance  when  they  have 
been  allowed  to  dry  out  gradually  on  their  bed  of  Sphagnum  under  a 
bell-jar,  during  a  period  of  two  months.  Confirmatory  of  this  is 
Behre's  observation  that  leaves  which  had  been  removed  and  sus- 
pended in  a  moist  chamber,  but  not  so  moist  as  to  prevent  some  wilt- 
ing, will  produce  many  buds.  A  too  great  plenitude  of  moisture 
therefore  appears  to  mask  a  delicate  balance  of  affairs  between  the 
leaf  and  its  environment. 

As  to  temperatures,  Ames  (1899)  thought  that  low  temperatures 
were  favorable.  Vickery  found  a  wide  favorable  range.  My  own 
experience  favors  the  idea  that  D.  rotundifolia  at  any  rate  is  active  in 
this  way  at  prevailing  cool  temperatures. 


Francis  E.  Lloyd  —  134  —  Carnivorous  Plants 

Wounding,  necessary  in  such  plants  as  Begonia  (Goebel  1903),  in 
itself  is  of  no  influence  (Behre).  It  has  been  thought  that  the  removal 
of  the  chief  shoot  (particularly  the  growing  shoot)  is  a  stimulus,  that 
is  to  say,  the  disturbance  of  correlations  (Behre),  which  is  attained 
simply  by  the  removal  of  the  leaf.  The  weight  of  this  point  seems  not 
to  be  great  since  budding  occurs  in  abundance  on  leaves  still  attached, 
in  the  case  of  D.  peltata,  though  rather  more  slowly  than  when  the 
leaves  have  been  removed  (Vickery).  When  some  of  the  glands  have 
been  injured  or  removed,  the  leaf  will  still  produce  buds,  but  only  from 
the  bases  of  uninjured  glands  (Vickery),  indicating  that  the  gland  may 
contribute  something  in  the  form  of  a  growth  substance  (see  Coe- 
LiNGH   1929). 

Nevertheless  Behre  did  find  certain  correlations.  The  removal  of 
the  growing  point  always  increased  the  leaf  budding,  though  em- 
bedding it  in  gypsum  plaster  did  not.  If  the  removal  of  the  growing 
point  incited  the  development  of  an  axillary  bud,  this  itself  would 
inhibit  bud  formation,  though  if  at  the  same  time  the  vascular  tissue 
had  been  suitably  cut,  before  the  axillary  bud  was  put  into  activation, 
buds  were  formed.  Behre  further  did  this  experiment:  after  removal 
of  the  growing  point  the  leaves  were  cut  longitudinally  in  some  cases 
and  transversely,  but  not  sufhcient  for  amputation,  in  others.  Only 
on  the  outer  parts  of  transversely  cut  leaves  did  buds  arise,  while  on 
plants  similarly  treated  but  with  the  growing  point  not  removed,  the 
result  was  negative.  Yet  Behre  recorded  the  occurrence  of  an  ad- 
ventitious bud  on  a  leaf  on  a  plantlet,  itself  produced  adventitiously 
from  a  scape,  with  the  growing  point  active  (1929,  Fig.  i).  These  results 
with  D.  rotundifolia  could  not  be  obtained  with  D.  capensis.  But  the 
facts  as  they  stand  support  the  view  that  there  is  a  delicate  inter- 
relation between  the  growing  point  and  the  inclination  to  regeneration 
(Goebel)  as  observed  in  numerous  other  plants.  Thus  we  are  led  to 
consider  what  the  internal  conditions  in  the  plants  may  be  which  de- 
termine or  control  such  phenomena.  Here  the  food  materials  may 
play  a  role  or  hormones  may  act  as  regulators,  but  this  question  is  too 
far  away  from  our  present  purpose,  though  it  may  as  well  be  pointed 
out  that  Behre  did  experiments  in  which  he  reduced  leaves  to  a  con- 
dition of  pronounced  hunger  in  darkness  with  the  deprivation  of  CO2 
and  yet  obtained  regeneration,  from  which  he  concluded  that  "there 
is  no  doubt  that  regeneration  is  put  into  activity  by  some  other  stimu- 
lus than  a  surplus  of  nutrient  materials,"  thus  indicating  the  presence 
of  specific  substances,  hormones  perhaps,  which  could  procure  the 
results. 

Polarity.  —  The  fact  of  polarity  is  one  of  so  general  observation 
that  Behre  naturally  raised  the  question  in  regard  to  Drosera,  finding 
but  little  evidence  that  it  obtains,  except  to  a  slight  extent  in  the  case 
of  D.  capensis  and  D.  filiformis.  Adventitious  buds  are  not  related  in 
position  to  the  stronger  vascular  strands,  but  are  found  scattered  in- 
differently, arising  usually  from  the  abaxial  surfaces  of  tentacle  bases, 
though  they  may  be  found  on  the  side  or  on  the  adaxial  aspect.  If 
small  pieces  of  the  leaf  blade  are  made,  more  buds  arise  than  would 
otherwise,  and  even  on  the  leaf  margin  where  they  do  not  occur  except 
when  a  narrow  band  (i  mm.  broad)  is  made  by  a  cut  parallel  to  the 


Chapter  X  —  135  —  Drosera 

margin.  They  never  arise  on  the  lower  leaf  surface.  That  buds  arise 
on  other  parts  where  there  are  no  tentacles  indicated  that  if  it  were 
possible  to  obtain  leaf  pieces  large  enough  and  free  of  tentacles,  they 
would  arise  also  from  the  upper  leaf  surface  proper.  The  age  of  the 
leaf  makes  little  or  no  difference.  It  is  remarkable  in  this  connection 
that  even  young  leaves  when  removed  from  the  plant  will  continue 
their  development  under  suitable  conditions  of  light  and  moisture.  If 
the  entire  leaf,  blade  and  stalk  are  removed,  buds  occur  on  the  blade. 
If  the  blade  is  then  removed,  buds  occur  on  the  outer  end  of  the 
petiole  where  there  are  tentacles,  though  not  always  on  a  tentacle  base. 
If  the  tentacle  bearing  part  is  now  removed,  a  bud  may  arise  at  any 
point,  no  polarity  being  shown.  If  now  the  conditions  are  so  ar- 
ranged that  the  petiole  is  kept  moist  and  the  blade  relatively  dry,  the 
petiole  will  regenerate  instead  of  the  blade.  In  D.  capensis,  however, 
there  is  a  distinct  tendency  for  buds  to  appear  near  the  leaf  apex,  this 
species  having  long  leaves  with  narrow  blade  which  unrolls  during 
growth.  This  is  true  in  both  old  and  young  leaves,  and  is  regarded  by 
Behre  as  evidence  of  polarity.  This  polarity  may  be  easily  masked, 
however,  by  placing  a  leaf  with  its  petiole  in  moist  sand  and  the  blade 
in  the  air,  when  buds  now  appear  toward  the  basal  end.  Winkler 
(1913)  had  observed  a  similar  behavior  in  D.  filiformis,  which  has  long 
cylindrical  leaves.  It  is  curious  that  the  long  slender  leaves  of  such 
species  as  D.  binata  do  not  exhibit  the  same  tendency.  The  readier 
production  of  buds  near  the  leaf  apex  in  D.  capensis,  but  in  the  case  of 
young,  not  older  scapes,  is  conditioned  by  the  young  state  of  the 
tissues.  The  readiness  of  roots  to  produce  buds  is  well  known  and 
made  use  of  for  propagating  exotic  species,  but  here  also  they  may 
arise  quite  indifferently  in  position,  and  no  polarity  can  be  de- 
tected. 

Carnivory.  —  The  attention  of  botanists  was  first  attracted  to 
Drosera  as  an  insectivorous  plant  by  the  observation  that  the  tentacles 
are  capable  of  movement.  This  was  made  in  1779  (Hooker  1875), 
when  a  physician  of  Bremen,  Dr.  A.  W.  Roth,  noted  as  follows:  ''that 
many  leaves  were  folded  together  from  the  apex  toward  the  base,  and 
that  all  the  hairs  were  bent  like  a  bow,  but  that  there  was  no  apparent 
change  in  the  leaf  stalk."  When  he  opened  the  leaves  he  found  cap- 
tured insects,  and  was  driven  to  compare  Drosera  with  Dionaea,  think- 
ing that  it  had  the  same  power  of  motion  as  the  latter.  He  records  an 
experiment  which  he  did.  "With  a  pair  of  tweezers  I  placed  an  ant 
upon  the  middle  of  the  leaf  of  Drosera  rotundifolia  but  so  as  not  to 
disturb  the  plant.  The  ant  endeavored  to  escape,  but  was  held  fast 
by  the  clammy  juice  at  the  points  of  the  hairs,  which  was  drawn  out 
by  its  feet  into  fine  threads.  In  some  minutes  the  short  hairs  on  the 
disc  of  the  leaf  began  to  bend,  then  the  long  hairs,  and  laid  themselves 
on  the  insect.  After  a  while  the  leaf  began  to  bend,  and  in  some  hours 
the  end  of  the  leaf  was  so  bent  inwards  as  to  touch  the  base.  The  ant 
died  in  fifteen  minutes,  which  was  before  all  the  hairs  had  bent  them- 
selves" (fde  Hooker,  1875).  At  about  this  time  (1780)  similar  ob- 
servations were  made  independently  by  Dr.  Whately,  "an  eminent 
London  surgeon"  (E.  Darwin:  Botanic  Garden,  pt.  2,  p.  24)  as  re- 
ported by  his  friend  Mr.   Gardom,  a  Derbyshire  botanist.     "On   in- 


Francis  E.  Lloyd  —  136  —  Carnivorous  Plants 

specting  some  of  the  contracted  leaves  we  observed  a  small  insect  or 
fly  very  closely  imprisoned  therein,  which  occasioned  some  astonish- 
ment as  to  how  it  happened  to  get  into  so  confined  a  situation.  After- 
wards, on  Mr.  Whately's  centrically  pressing  with  a  pin  other  leaves 
which  were  yet  in  their  natural  and  expanded  form,  we  observed  a 
remarkable  sudden  and  elastic  spring  of  the  leaves,  so  as  to  be  inverted 
upwards  and,  as  it  were,  encircling  the  pin,  which  evidently  showed  the 
method  by  which  the  fly  came  into  its  embarrassing  position." 
(Withering  1796).  It  is  unfortunate  that  Dr.  Whately  did  not 
record  his  observations  himself  since  the  rate  of  movement  seems,  by  a 
trick  of  memory,  to  have  been  exaggerated  by  the  writer,  Mr.  Gardom. 
As  late  as  1855  the  facts  were  denied  by  Trecul,  but  in  i860  Nitschke 
made  a  thoroughgoing  study,  substantiating  the  earlier  observations, 
to  be  followed  by  Darwin,  who  had  been  heralded  both  by  Hooker 
and  by  Asa  Gray,  to  whom  Darwin  had  previously  communicated 
his  results.  Of  267  pages  of  Darwin's  book  on  Insectivorous  Plants 
230  are  devoted  to  an  extraordinarily  minute  examination  of  the  activ- 
ities of  Drosera,  attesting  to  his  immense  patience  and  determination 
to  uncover  every  secret  possible. 

Following  Darwin  various  trends  of  investigation  can  be  followed. 
His  observation  of  the  phenomenon  of  aggregation  was  the  beginning 
of  numerous  studies  of  the  cytological  changes  in  glandular  and  other 
cells,  summarized  by  Homes.  Other  trends  have  been  in  the  field  of 
anatomy,  already  discusssed,  of  digestion  and  nutrition  and  of  the 
nature  of  the  movements,  all  to  be  duly  considered. 

Mucilage.  —  While  the  papillae  have  not  been  observed  to  throw 
off  secretion,  unless  it  be  water  (Konopka),  the  glands  of  the  tentacles 
are  very  conspicuous  because  each  bears  a  drop  of  mucilage  of  high 
viscidity,  clear  and  ghstening,  secreted  by  and  supported  on  it  (ij — 9). 
The  glands  are  charged  with  red  pigment,  so  that  the  shining  drops  of 
mucilage  lend  to  the  leaf  a  brilliant  red  hue.  Since  these  persist  as 
well  during  the  sunshine  as  otherwhile,  we  have  the  name  "sundew" 
common  among  Europeans.  This  mucilage,  because  of  its  briUiance 
and  reflected  color,  may  be  interpreted  as  a  visible  lure;  it  is  at  all 
events  an  effective  means  of  capturing  prey  of  small  dimensions,  if  it 
ventures  to  alight  on  the  glands.  A  delicate  fungus-like  odor  which 
has  been  detected  by  various  observers  (Geddes)  may  be  an  additional 
factor  of  allure.  The  insect  caught  is  soon  (Nitschke:  15  min.)  wet 
all  over  and  smothered  by  the  secretion,  which  upon  stimulation  is  said 
to  flow  more  freely.  Darwin  investigated  the  secretion  activity  on 
the  application  of  various  kinds  of  substances  and  found  that  not  only 
does  the  secretion  increase  in  the  gland  directly  stimulated,  but  in 
nearby  glands  as  well,  as  the  result  of  transmitted  stimulus.  When 
the  stimulating  material  is  nitrogenous  the  secretion  becomes  acid,  sup- 
plying an  important  condition  for  digestion.  The  amount  of  secretion 
which  becomes  applied  to  the  captured  prey  is  increased  not  only  by  a 
more  ample  supply  of  secretion,  but  by  the  movement  of  the  tentacles 
which  bring  more  glands  than  originally  stimulated  into  contact  with 
the  prey.  The  secretion,  Darwin  showed,  is  possessed  of  antiseptic 
properties,  and  thus  inhibits  the  action  of  bacteria.  In  his  experiments 
he  found  that  bits  of  meat  and  of  albumen  placed  on  the  Drosera  leaf 


Chapter  X  — 137  —  Drosera 

underwent  changes,  shown  to  be  due  to  digestion,  and  were  found  to 
be  free  of  bacteria,  while  similar  pieces  of  material  placed  on  wet  moss 
"swarmed  with  infusoria." 

Chemically  the  mucilage  appears  to  be  a  sort  of  hydrocellulose,  but 
the  seat  of  its  secretion  is  not  known.  Like  other  cases  of  mucilage  it 
may  be  a  product  of  an  alteration  of  the  cell  wall,  or  it  may  be  an 
exudation  from  the  protoplast.  In  any  event  it  is  permeated  by  other 
substances  in  which  its  power  of  digestion  rests  —  enzyme,  acid,  some 
antiseptic  substances,  and  latterly  Weber  has  suspected  the  presence 
of  ascorbic  acid. 

Small  (1939)  has  advanced  the  notion  that  the  mucilage  is  se- 
creted only  by  the  lateral  cells  of  the  gland,  and  not  by  the  apical  cells. 
His  evidence  is  seen  in  internal  reflecting  surfaces,  stated  to  be  present 
at  the  apex  and  absent  from  the  lateral  cells,  between  them  and  the 
mucilage.  For  my  part  I  fail  to  find  such  reflecting  surfaces.  On  the 
other  hand,  if  a  piece  of  leaf  with  glands  which  have  been  thoroughly 
wiped  off  with  filter  paper  is  placed  in  parafhn  oil  and  carefully  ex- 
amined to  find  glands  on  which  no  trace  of  mucilage  is  visible,  these 
in  the  course  of  one  to  several  hours  will  show  numerous  droplets  of 
mucilage  oozing  away  from  the  surface  as  well  at  the  apex  as  on  the 
sides  of  the  gland  (75— 14).  Weber  (1938)  by  means  of  sodium 
oleate  has  demonstrated  to  his  own  satisfaction  rods  or  streams  of 
mucilage  radiating  from  the  gland  surface  at  every  point.  I  have  not 
been  able  to  confirm  this.  If  the  glands  are  watched  under  a  binocular 
dissecting  microscope,  in  the  course  of  a  short  time  it  will  be  noticed 
that  the  surface  of  an  opalescent  mucilage  drop  is  wrinkled  longi- 
tudinally, and  by  this  time  the  surface  of  the  drop  has  lost  its  glassy 
look.  It  is  evident  that  there  is  a  surface  concentration  of  some  sub- 
stance or  substances.  As  one  watches  steadily,  one  sees  an  occasional 
explosion  on  the  surface  as  if  some  minute  particle  or  droplet  had  on 
arriving  there  from  inside  immediately  spread  over  it.  As  the  wrink- 
ling progresses  the  drop  becomes  pear-shaped,  the  broad  end  above  the 
apex.  With  cessation  of  evaporation,  the  drop  will  assume  its  oval 
form.  The  mucilage  is  a  jelly-hke  mass.  If  two  glands  with  drops  are 
approached  so  that  they  touch  and  then  are  moved  apart,  the  drops 
will  largely  separate,  adhering  by  only  a  slender  thread.  If  a  drop  is 
touched  with  a  corner  of  filter  paper  at  its  basal  margin  and,  on  ad- 
hering, the  mucilage  is  pulled  away  upwards  toward  the  gland  apex,  it 
will  tear  away  and  extend  asymmetrically  from  the  gland  apex.  When 
a  drop  is  pulled  out,  it  at  first  refuses  to  leave  the  gland.  Only  when 
there  is  sufficient  adhesion  and  pull,  the  whole  mass,  after  a  certain 
amount  of  stretching,  will  pull  away  suddenly.  These  and  similar 
evidences  indicate  that  the  mucilage  has  a  sort  of  structure.  When 
dry,  it  shows  double  refraction,  but  not  when  wet  (Weber).  It  is  not 
so  stiff  a  jelly  as  that  of  Drosophyllum,  which  pulls  away  readily  in  a 
mass,  but  is  otherwise  similar. 

One  other  apparently  trifling  observation  which  I  have  made  may 
be  mentioned  here.  I  have  noticed  that,  over  the  apical  half  of  a 
gland  there  are  in  the  immediate  vicinity  of  the  gland  surface  minute 
plaques  of  clear  colorless  substance  not  soluble  in  sulfuric  acid,  rounded 
or  sometimes  angular  in  shape  {15 — 10).     Sulfuric  acid  dissolves  the 


Francis  E.  Lloyd  —  138  —  Carnivorous  Plants 

mucilage,  and  the  cuticle  remains  intact.  They  might  be  delicate 
flakes  of  cuticle  exfohated  from  the  remaining  cuticle,  but  of  this  there 
is  no  certainty. 

Movements  of  tentacles  and  leaf  blade.  — We  must  go  back  to  1782 
to  find  the  first  record  of  studies  of  the  modes  of  behavior  of  the  ten- 
tacles and  leaf  blade.  These  were  carried  on  by  the  above  mentioned 
Dr.  Roth,  botanist  as  well  as  physician.  He  was  stimulated  to  study 
Drosera  by  reading  Ellis'  letter  to  Linnaeus  in  1770  announcing  the 
discovery  of  Dionaea  muscipula;  and  in  his  essay  he  makes  cogent 
comparisons  between  these  two,  the  only  then  known  carnivorous  plants. 

According  to  Roth,  if  an  ant  be  placed  on  a  leaf,  the  glands  re- 
spond by  bending,  first  the  centrally  placed,  then,  but  much  more 
slowly,  the  glands  most  distant.  Finally  the  leaf  blade  bends  either 
transversely,  its  apex  approaching  its  base,  or  if  the  stimulus,  say  a 
small  fly,  has  been  placed  laterally,  the  side  may  bend  over.  The 
rates  of  movement  depend  on  external  conditions,  and  are  most  rapid 
in  warm  sultry  weather.  He  remarks  that  D.  longifolia  reacts  more 
readily  than  D.  rotundifolia,  and  that  rain  reduces  sensitivity. 

The  next  contribution  of  major  importance,  by  Nitschke,  did  not 
appear  till  i860,  eighty  years  later.  Meanwhile,  however,  several  bota- 
nists had  observed  and  discussed  the  matter.  Somewhat  previous  to 
1835  ^-  P-  °E  Candolle  had  observed  the  response  of  the  tentacles. 
Treviranus  (1838)  quoted  Roth  (1782)  but  said  that  he  failed  to  get 
the  results  described  by  him.  Hayne  (date  about  this  time,  see 
Nitschke  i860)  saw  the  response  of  the  tentacles  and  that,  at  length, 
the  leaf  blade  bent  and  became  spoon-shaped.  In  1837  Meyen  re- 
viewed previous  observations  and  while  he  could  confirm  the  fact  that 
the  tentacles  as  also  the  leaf  blade  were  bent,  he  maintained  the  idea 
that  it  was  due  not  to  irritability,  but  to  the  activity  of  a  struggUng  in- 
sect pulhng  over  the  tentacles  toward  itself.  Milde  (1852),  however, 
put  this  right  by  experiment.  He  placed  small  flies  on  the  leaf,  and  ob- 
served in  5  min.  the  outer  tentacles  bending  inwards.  Next  day 
the  whole  leaf  was  bent,  and  in  5  days  again  unrolled.  A  useful  skep- 
tic appeared  in  1855  in  the  person  of  Trecul,  who  thought  that  the 
insects  were  caught  by  young  leaves  which  then  retained  their  youth 
position.  Came  then  Nitschke  (i860),  who  was  the  first  to  attack  the 
problem  in  a  sustained  way  and  with  a  critical  attitude.  His  first 
argument  was  directed  against  Trecul,  and  he  established  the  general 
correctness  of  Roth's  observations.  He  believed  that  when  a  stimulus 
has  been  applied  at  some  point  by  the  apphcation  of  an  insect,  the 
surrounding  tentacles  bend  their  heads  directly  toward  this  point, 
whether  the  position  of  the  stimulating  object  is  central  or  lateral. 
The  marginal  tentacles  move,  he  says,  always  in  the  "most  direct" 
path  toward  the  point  of  stimulation.  On  this  point  the  reader  is  re- 
ferred to  the  work  of  Behre  beyond.  Nitschke  regarded  the  behavior 
as  an  expression  of  true  irritability,  and  that  Meyen's  view  that  the 
action  of  the  tentacles  is  purely  passive  is  wrong  for  a  number  of 
reasons,  especially  cogent  being  the  fact  that  young  leaves  do  not  se- 
crete mucilage,  and  that  neither  they  nor  aged  leaves  are  sensitive. 
First  when  the  leaves  are  widely  open  and  rich  in  secretion  is  this  the 
case;  even  dead  insects  procure  movements,  if  indeed  somewhat  less 


Chapter  X  —  139  —  Drosera 

vigorous  ones.  He  found,  however,  no  response  to  simple  mechanical 
stimulation,  but  this  was  found  later  to  be  wrong.  Equally  so  his  view 
that  a  stimulating  body  attached  to  the  back  of  a  leaf  induced  re- 
sponses whereby  the  tentacles  turned  backward  to  embrace  the  body 
quite  as  well  as  forward.  He  found  that  the  leaf  may  repeat  the  per- 
formance after  recovery  on  renewal  of  secretion,  and  further  that  the 
effect  of  a  given  stimulus  depends  on  the  distance  it  has  to  travel.  The 
movements  can  take  place  under  water  and  in  response  to  soHd  bodies 
and  acids  in  weak  solution.  The  rate  of  response  is  aflfected  by  tem- 
perature but  not  by  Hght.  It  is  then  chiefly  to  Nitschke  and  to  Dar- 
win that  we  owe  many  original  observations  which  furnish  a  picture  of 
the  direction  and  rapidity  of  the  movements  of  the  leaf  and  tentacles. 
The  general  facts  first  and  most  readily  observed  are  the  following. 
If  a  suitable  stimulus  is  received  by  any  group  of  leaf  tentacles,  say 
near  the  middle  of  the  leaf,  or  on  or  near  the  "disc"  in  the  case  of 
D.  rotundifolia,  in  the  course  of  a  few  minutes  a  bending  of  the  near- 
by tentacles  is  to  be  observed  until,  the  stimulus  evidently  travelling 
radially,  it  reaches  even  the  extreme  marginal  tentacles  which  then 
bend  over.  If  the  stimulus  is  sufficient  even  the  leaf  blade  responds 
in  like  manner.  Goebel  figures  a  leaf  of  D.  intermedia  which  had  com- 
pletely folded  over  to  embrace  the  body  of  a  large  fly  which  had  been 
caught.  D.  capensis  was  found  to  be  particularly  good  at  this.  I 
placed  a  single  Drosophila  flylet  on  a  leaf  and  in  the  course  of  time  the 
marginal  tentacles,  as  well  of  course  as  those  nearby,  had  responded. 
Finally  the  whole  apex  of  the  leaf  bent  over  (ij  —  8).  With  regard  to 
the  leaf  blade  not  all  the  species  of  Drosera  behave  in  this  way.  Goe- 
bel observed  that  D.  hinata  does  not,  nor  does  D.  dichotoma,  and 
probably  others.  From  such  observations  it  is  evident  that  the  stim- 
ulus received  by  a  tentacle  travels  to  its  base  and  radially  from  there 
to  neighboring  tentacles,  which  then  respond.  A  casual  glance  at  a 
leaf  displaying  these  responses,  one  in  which  the  tentacles  are  bent 
over  towards  the  middle  of  the  disc  (speaking  of  D.  rotundifolia)  sug- 
gests that  the  normal  movement  of  the  tentacles  is  along  radial  lines. 
The  dorsiventral  flatness  of  the  tentacles  would  seem  to  condition  them 
to  move  thus.  But  Nitschke  saw  that  the  matter  is  not  so  simple. 
He  said  that  the  tentacles  receiving  the  stimulus  bend  over  in  the  di- 
rection of  the  point  at  which  the  stimulus  was  received,  irrespective  of 
its  position,  so  that,  if  a  fly  is  caught  at  some  eccentric  point,  the 
tentacles  affected  bend  over  toward  this  point  and  not  toward  the 
center  of  the  disc.  Apparently  the  direction  of  movement  of  the  stim- 
ulus determined  the  appropriate  direction  of  movement  of  the  tentacle. 
There  is  an  apparent  exception  to  be  noted.  Darwin  found  that 
when  a  marginal  tentacle  is  stimulated,  it  bends  over,  but  no  response 
is  called  forth  in  the  neighboring  marginal  tentacles.  Only  when  the 
marginal  tentacle  originally  stimulated  brings  its  glands  with  its  stimu- 
lating material  into  contact  with  the  glands  of  the  disc,  is  a  stimulus 
provided  by  the  latter  which  now  calls  forth  a  response  of  the  mar- 
ginal tentacles  hitherto  not  affected. 

The  duration  of  the  response  depends  on  the  nature  of  the  stimu- 
lus. Here  I  quote  from  Darwin  (p.  19)  "The  central  glands  of  a  leaf 
were  irritated  with  a  small  camel's  hair  brush,   and  in   70  minutes 


Francis  E.  Lloyd  —  140  —  Carnivorous  Plants 

several  of  the  outer  tentacles  were  inflected;  in  5  hours  all  the  sub- 
marginal  tentacles  were  fully  inflected;  next  morning  after  an  interval  of 

22  hours  they  were  fully  expanded I  then  put  a  dead  fly  in  the 

center  of  (a)  leaf,  and  next  morning  it  was  closely  clasped;  five  days 
after  the  leaf  reexpanded  and  the  tentacles,  with  their  glands  sur- 
rounded by  secretion,  were  ready  to  act  again." 

A  given  stimulus  acting  somewhere  on  one  side  of  the  leaf  will  affect 
the  marginal  tentacles  on  that  side  sooner  than  those  of  the  other  side 
further  away;  or  indeed,  only  one  side  of  the  leaf  may  be  called  into 
action.  In  the  case  of  a  cup-shaped  peltate  leaf  {D.  gigantea)  I  have 
observed  that  the  total  result  of  such  movements  is  to  bring  the  prey 
into  the  depths  of  the  cup,  where,  in  the  course  of  time,  only  the  chitin- 
ous  remains  of  the  captured  insects  are  to  be  found.  This  result  is 
perhaps  contributed  to  by  the  surface  tension  of  the  drop  of  secretion 
which  more  or  less  fills  the  cup. 

It  was  thought  by  Nitschke  that  even  the  back  of  the  leaf  could 
accept  stimuli  and  transmit  them  to  the  tentacles,  but  Darwin  was 
unable  to  cause  any  response  by  stimulating  the  leaf  blade  proper,  on 
the  front  or  the  back.  In  order  to  locate  the  sensitive  or  sense  per- 
ceptive points,  Darwin  removed  the  gland  from  a  tentacle,  whereupon 
the  latter  made  a  brief  response  by  slightly  bending  but  soon  regained 
its  erstwhile  posture.  When  stimulus  was  applied  to  the  cut  tentacle, 
no  response  followed.  But  if  now  the  disc  tentacles  were  stimulated, 
the  amputated  tentacle  responded,  as  if  the  head  were  not  missing. 
The  stalk  of  a  tentacle,  no  more  than  the  leaf  or  petiole,  can  receive  a 
stimulus.  In  any  event,  the  marginal  tentacles  are  not  so  sensitive  as 
the  rest,  nor  are  they  affected  by  rain  drops.  Small  (1939)  denies 
this.  That  the  disc  tentacles  are  more  sensitive  may  appear  to  be  the 
case  because  the  stalks  of  these  are  very  short,  and  the  tentacles  are 
closer  together  so  that  a  given  stimulus  does  not  have  to  travel  so  far 
to  elicit  response.  And  although  the  stimulus  travels  radially  from  a 
point  of  stimulation,  Darwin  found  that  it  travels  more  readily  longi- 
tudinally than  transversely  across  the  leaf  blade.  The  stimulus  may 
travel  quite  across  the  blade  so  that  when  it  is  applied  to  the  tentacles 
on  one  margin,  those  of  the  opposite  may  respond;  but  in  spite  of 
repetition  of  the  stimulus,  the  opposite  tentacles  will  open  again,  from 
which  Darwin  argued  that  the  "motor  discharge  must  be  more  power- 
ful at  first  then  afterward."  It  was  asked  by  Darwin  whether  the 
motor  impulse  travels  through  the  vascular  tissue,  but  this  turned  out 
not  to  be  the  case,  certainly  "not  exclusively,"  for  the  tentacles  of  a 
group  surrounding  the  point  of  stimulus  will  respond  all  at  a  uniform 
rate  notwithstanding  the  fact  that  the  vascular  connections  are  very 
unequal  in  length;  indeed  the  course  of  the  vascular  tissues  in  the  leaf 
as  a  whole  does  not  permit  the  view  in  question  when  the  uniformity 
of  response  of  the  tentacles  is  considered. 

The  intensity  of  the  stimulus  necessary  to  procure  response  was  a 
matter  of  much  concern  to  Darwin.  He  endeavored  to  get  some 
measure  of  intensity  by  weighing  small  pieces  of  hair,  etc.,  which  would 
prove  efficient.     The  following  quotation  embodies  an  expression  of  his 

reflections  on  this  " it  is  an  extraordinary  fact  that  a  little  bit  of 

soft  thread  1/50  of  an  inch  in  length  and  weighing  1/8197  of  a  grain, 


Chapter  X  —  141  —  Drosera 

or  of  a  human  hair  8/1000  of  an  inch  in  length  and  weighing  only 
1/78740  of  a  grain  (.000822  milligram)  or  particles  of  precipitated 
chalk,  after  resting  for  a  short  time  on  a  gland,  should  induce  some 
change  in  its  cells,  exciting  them  to  transmit  a  motor  impulse  through- 
out the  whole  length  of  the  pedicel,  consisting  of  about  20  cells,  to 
near  its  base,  causing  this  part  to  bend,  and  the  tentacle  to  sweep 
through  an  angle  of  above  80  degrees". 

It  was  generally  conceded  by  both  Nitschke  and  Darwin  that 
dead  bodies  do  not  provoke  so  much  response  as  hving  and  therefore 
moving  bodies.  This  was  explained  by  Pfeffer  by  pointing  out  that 
mere  constant  contact  does  not  produce  response,  but  that  there  must 
be  both  direct  contact  with  the  gland  and  friction  on  its  surface.  The 
mucilaginous  drop  can  prevent  direct  contact  as  in  the  case  of  rain  or 
quicksilver  (which  Pfeffer  tried)  or  even  particles  suspended  in  it  un- 
less by  their  weight  they  fall  against  the  sensitive  surface.  That  the 
minute  particles  of  hair  used  by  Darwin  should  produce  the  results 
observed  may  be  understood  better  when,  as  Pfeffer  showed,  vibra- 
tion of  the  table  or  floor  causes  movements  of  such  particles  on  the 
surface  of  the  gland  sufficient  to  stimulate  it. 

In  addition  to  non-living  substances,  Darwin  tested  the  reactions 
of  the  tentacles  to  a  large  variety  of  organic  materials  with  the  purpose 
of  determining  what  digestive  juice  or  juices  are  secreted  by  the  leaves 
of  Drosera.  His  contribution  to  the  problem  of  digestion  will  more 
suitably  be  considered  under  the  appropriate  caption  beyond.  Here 
it  will  be  mentioned  that  he  seemed  to  regard  the  movements  of  the 
tentacles  and  the  length  of  time  they  remain  inflected  as  evidence  of 
the  nutritional  value  to  the  plant  of  the  material  exposed  to  them. 
But  he  himself  records  a  various  behavior  of  the  tentacles  in  this  re- 
gard. He  says  in  conclusion  "The  substances  which  are  digested  by 
Drosera  act  on  the  leaves  very  differently.  Some  cause  much  more 
energetic  and  rapid  inflection  of  the  tentacles  and  keep  them  inflected 
for  a  much  longer  time,  than  do  others.     We  are  thus  led  to  believe 

that  the  former  are   more    nutritious   than    the   latter "     This 

generalization  can  hardly  hold.  Robinson  found  that  pure  creatin  was 
digested  but  caused  no  bending  of  the  tentacles.  As  Schmid  points 
out,  Darwin's  work,  rightly  or  wrongly,  led  emphasis  to  be  too  strongly 
placed  on  the  Drosera  mechanism  being  an  adaptation  for  the  obtain- 
ing of  protein  nutrition.    While  it  is  true  that,  to  quote  Darwin  again, 

" inorganic  substances,  or  such  substances  as  are  not  attacked  by 

the  secretion,  act  much  less  quickly  and  efficiently  than  organic  sub- 
stances yielding  soluble  matter  which  is  absorbed"  it  is  also  true  that 
some  nitrogenous  bodies  equally  do  not,  and  therefore  it  is  impossible 
to  formulate  a  rule.  Darwin  himself  records  the  failure  of  urea  to 
procure  movements.  What  explanation  serves  when  HCl,  boric  acid, 
malic  acid  and  camphor  stimulate  to  movement  when  Ca,  Mg  and  K 
salts  generally  do  not?  And  ammonium  phosphate  was  found  more 
energetic  than  other  ammonium  salts  though  containing  less  nitrogen. 
But  because  potassium  phosphate  is  taken  up  Darwin  argued  a  need 
for  phosphorus.  Schmid,  considering  this  phase  of  the  insectivory 
problem,  himself  tested  the  action  of  pure  salts  and  concluded  that  the 
movements  of  tentacles  alone  cannot  lead  to  any  real  index  of  the 
value  of  insectivory  from  the  nutritional-ecological  point  of  view. 


Francis  E.  Lloyd 


—  142 


Carnivorous  Plants 


As  little  indeed  may  one  thus  argue  as  about  the  nutritional  value 
of  food  taken  by  man  from  the  action  of  the  salivary  glands,  adds 
ScHMED.  It  seems  proper  to  conclude  that  the  reactions  of  the  ten- 
tacles are  general  rather  than  specific.  The  length  of  time  they  remain 
inflected,  however,  seems,  in  the  absence  of  injury  (several  times  noted 
by  Darwin)  to  be  generally  correlated  with  their  opportunity  for  ab- 
sorption. 

Mechanism  of  tentacle  movement.  —  Nitschke  pointed  out  that  al- 
though the  tentacles  can  bend,  there  are  no  special  motile  organs,  such 
as  occur  e.g.  in  Mimosa.  What  then  is  the  nature  of  the  bending 
movements  of  the  tentacle?  Though  Darwin  obtained  no  hght  on  this 
question,  it  was  answered  by  Batalin  (1877).  He  made  spaced  marks 
on  the  sides  of  the  tentacle,  and  found  that  after  a  movement  was  com- 
pleted, the  distances  had  increased.  When  the  recovery  is  complete, 
these  distances  are  maintained,  showing  that  the  bending  is  a  growth 
phenomenon.  This  was  shown  true  also  of  the  leaf  blade.  H.  D. 
Hooker  (191 6)  investigated  the  matter  more  thoroughly.    In  making 


Fig.  3.  —  Drosera  rotundifolia.  —  A,  Side  views  of  a  tentacle  in  process_  of  bending, 
beginning  with  the  bottom  figure;  B,  same  in  process  of  unbending,  beginning  with  the 
top  figure;  C,  Side  views  of  the  same  tentacle  before  and  at  close  of  the  reaction  (after 
Hooker). 

his  measurements  of  the  tentacles  during  bending  he  made  use  of 
natural  marks  supplied  by  the  minute  sessile  glands  to  be  found  on  the 
surface  of  the  tentacle  stalk.  By  means  of  these  measurements  and  of 
camera  lucida  drawings,  he  got  a  detailed  record  of  changes  in  dimen- 
sions during  bending  and  recovery.  A  set  of  his  drawings  are  here  re- 
produced (Text  fig.  3).  Hooker  found,  as  did  Batalin,  that  the 
movement,  whether  bending  or  unbending,  is  a  growth  phenomenon. 
During  bending  acceleration  of  growth  begins  near  the  base  along  the 
back  (the  convex  surface)  of  the  tentacle,  and  moves  upward  during  the 
bending  phase,  so  that  the  tentacle  end  moves  through  an^  angle 
of  215  to  270  degrees,  beginning  the  movement  within  1.5  minutes, 
completing  it  in  a  few  hours,  or  sometimes  in  as  short  a  time  as  17 
min.  30  sec.  (Darwin).  The  unbending  movement  results  from  in- 
creased growth  on  the  now  concave  side,  and  takes  place  at  once  if  the 
stimulus  was  a  brief  one,  or  is  delayed  as  when  the  tentacles  have 
closed  over  prey.  Here  also  growth  begins  near  the  base  and  moves 
upward  toward  the  gland.     During  neither  phase  is  the  growth  neces- 


Chapter  X  —  143  —  Drosera 

sarily  limited  to  one  side,  but  the  difference  of  rate  is  obvious  and 
produces  the  same  result.  Since  the  movement  of  the  tentacle  is  a 
matter  of  growth,  and  since  there  is  a  limit  of  total  growth,  the  num- 
ber of  times  bending  may  be  repeated  is  limited.  Darwin  found  the 
number  is  three,  and  this  was  confirmed  by  Hooker.  Though  the  two 
movements  constitute  practically  a  continuous  reaction,  at  least  when 
a  single  brief  stimulus  is  originally  applied,  the  unbending  reaction  fol- 
lows a  stimulus  inherent  in  the  internal  conditions  (such  as  tissue  ten- 
sions) set  up  during  bending,  and  is  tropic  (autotropic,  autonomous, 
Behre)  in  nature.  Since  the  entire  armament  of  tentacles  may  not  be 
used  in  any  one  grasping  of  prey,  the  leaf  as  a  whole  may  react  more 
than  three  times,  even  though  a  single  tentacle  cannot.  The  short 
radially  structured  tentacles  of  the  disc  do  not  react  by  bending  to 
stimuli  applied  directly  to  the  glands,  but  only  to  stimuli  received 
through  the  glands  of  other  tentacles.  Hooker  regards  the  response  as 
tropic  while  the  original  response  of  the  lateral  tentacles  is  evidently 
nastic,  though  the  unbending  response  is  tropic.  Both  Darwin  and 
NiTSCHKE  recorded  their  behef  that  marginal  tentacles  when  stimu- 
lated indirectly  bend  toward  the  point  of  stimulation.  Hooker  takes 
exception  to  this,  saying  that  he  was  unable  to  get  evidence  of  it, 
and  thinks  that  they  normally  bend  toward  the  middle  of  the  disc,  that 
is,  nastically. 

Exceptions  to  this  he  thought  "to  be  purely  accidental."  None- 
theless, Hooker  was  sufficiently  impressed  with  his  observations 
to  state  that  "most  of  the  marginal  tentacles  which  reacted  to  the 
conducted  impulse"  from  the  discal  tentacles  "in  bending  toward  the 
center  of  the  leaf  bent  hkewise  in  the  direction  of  the  source  of  excite- 
ment."  The  bending  of  the  discal  tentacles  is,  however,  always  toward 
the  point  of  original  stimulation,  and  cannot  be  stimulated  directly. 
The  response  is  tropic,  but  "in  all  probability"  the  movements  "are 
likewise  the  result  of  differential  growth  on  opposite  sides"  of  the 
tentacle  base.  The  method  used  was  not  applicable  to  the  determina- 
tion of  this  fact. 

Behre  (1929)  admitted  that  Hooker's  conclusions  were  nearly 
right,  but  was  evidently  impressed  by  the  discrepancies  admitted 
by  him.  He,  therefore,  attacked  the  problem  at  this  point,  and  ana- 
lysed the  movement  of  the  tentacles  more  rigorously,  controlling  his  ob- 
servation by  means  of  a  horizontal  measuring  microscope  with  a  scale 
in  the  field.  He  recorded  accurately  the  movements  of  tentacles  rela- 
tive to  each  other  and  to  the  position  of  the  source  of  stimulation,  and 
made  them  available  to  the  reader  by  means  of  maps  showing  the 
paths  of  movements. 

In  the  case  of  D.  rotundifolia  he  found  that,  according  to  their  be- 
havior the  tentacles  can  be  divided  into  three  groups,  namely,  {a)  mar- 
ginal, the  outermost  standing  exactly  on,  or  very  near  to  the  leaf  mar- 
gin; {h)  an  outer  zone  of  discal  tentacles  of  one  to  three  rows,  called  by 
him  the  "surface  outer  tentacles";  and  (c)  the  discal  tentacles  within 
(&),  or  "central  tentacles".  With  some  sHght  differences  due  to  the 
posture  of  the  tentacles,  the  same  holds  for  other  species  investigated 
{D.  binata,  intermedia,  capensis,  spathulata).  His  observations  yielded 
the  following  results,  and  here  it  may  be  injected  that  he  used  in  most 


Francis  E.  Lloyd  —  144  —  Carnivorous  Plants 

cases  small  and  uniformly  sized  objects  for  stimulation,  viz.,  the  eggs 
of  the  wood-louse. 

The  responses  of  the  strictly  marginal  ("outer  marginal")  tentacles 
are  somewhat  slower  than  those  standing  just  within  the  margin  ("in- 
ner marginal")-  Their  reaction  to  a  direct  stimulus  (that  is,  one  ap- 
plied to  the  glands  of  these  tentacles)  is,  however,  always  strictly 
nastic;  their  function  is  to  bring  the  prey  into  contact  with  the  discal 
glands.  The  sensitivity  and  quickness  of  reaction  are  surprising.  The 
reaction  may  begin  in  lo  seconds,  and  was  seen  to  make  a  complete 
excursion  of  i8o  degrees  in  20  seconds,  the  movement  being  visible  to 
the  naked  eye.  This  was  a  maximum,  however.  It  must  be  clear  that 
the  direction  of  movement  is  in  a  single  plane  normal  to  the  leaf  mar- 
gin. Prompt  and  rapid  as  their  response  to  direct  stimulus  is,  they  re- 
spond to  indirect  stimulus,  derived  from  stimulated  discal  tentacles, 
only  slowly  and  weakly.  At  best,  a  reaction  may  be  detected  in  10 
minutes,  but  the  total  excursion  is  short.  Only  when  the  leaf  is  heavily 
fed,  especially  with  living  prey,  do  the  marginal  tentacles  indirectly  stim- 
ulated actually  reach  the  prey.  If  the  stimulus  is  derived  from  a  small 
insect,  the  excursions  of  the  marginal  tentacles  are  incomplete,  are  soon 
reversed  and  can  be  of  no  use  to  the  plant,  though,  since  complete 
bendings  can  occur  only  three  times  at  best,  the  meagreness  of  re- 
sponse may  be  regarded  as  an  economy  of  effort.  Full  expenditure  of 
effort  is  made  only  when  the  prey  falls  on  the  marginal  tentacles,  when 
by  bending  fully  they  bring  it  into  contact  with  the  inner  tentacles 
thus  exposing  it  to  much  greater  digestive  surface.  The  movements 
are  at  first  nastic.  Since  in  D.  rokmdifolia  the  orbicular  form  of  the 
leaf  results  in  nastic  and  tropistic  reactions  acting  in  the  same  direc- 
tion, the  observer  is  and  has  been  naturally  deceived.  Only  when  the 
reactions  are  observed  in  such  leaves  as  those  of  D.  intermedia  and  D. 
binata  is  it  seen  clearly  that,  while  the  reaction  of  the  marginal  ten- 
tacles to  direct  stimulation  is  at  first  nastic,  in  the  course  of  the  ex- 
cursion the  direction  of  movement  may  be  modified  by  tropistic  re- 
actions, especially  clear  in  D.  binata,  and  in  this  is  the  account  of 
Hooker  amplified. 

In  the  case  of  the  central  or  discal  tentacles,  there  is  no  response  to 
direct  stimulus,  that  is,  stimulating  material  placed  on  a  single  tentacle 
produces  no  movement  in  that  tentacle.  But  the  stimulus  is  quickly 
transmitted  to  nearby  tentacles  and  these  then  bend  toward  the  point 
of  stimulation,  that  is  tropistically.  The  rate  of  reaction  is  here  much 
more  dependent  on  temperature  —  from  an  hour  to  20  or  so,  according 
to  circumstances. 

Between  the  central  disc  tentacles  and  the  marginal  lies  a  narrow 
zone  of  outer  surface  tentacles,  in  size  grading  between  them,  being  in 
such  species  as  D.  binata  as  long  as  the  marginal  tentacles,  or  longer. 
Their  reactions  are  more  complicated  than  those  of  the  tentacles  of  the 
other  two  zones,  since  they  combine  properties  of  both.  They  react 
nastically  to  direct  stimulus  and  as  rapidly  as  the  marginal  tentacles, 
and  this  character  distinguishes  them  at  once  from  the  central  disc 
tentacles.  Toward  indirect  stimulus  their  reactions  are  both  nastic  and 
tropistic,  and  the  resulting  excursions  are  rapid  and  more  extended  than 
those  of  the  marginal  tentacles  to  indirect  stimulus,  and  result  in  bring- 


Chapter  X  —145— Drosera 

ing  the  glands  into  contact  with  the  prey.  The  tropistic  movement  is 
slower.  The  case  of  D.  hinata  well  illustrates  the  behavior,  because  of 
the  cylindrical  form  of  the  leaf.  A  small  fragment  of  meat  was  placed 
on  an  outer  surface  tentacle.  This  responded  at  first  quickly,  and  in 
the  course  of  five  hours  brought  the  prey  into  contact  with  the  discal 
tentacles.  In  two  hours  the  nearby  outer  surface  tentacles  began  their 
excursions  which  were  at  first  (for  four  and  a  half  hours)  nastic.  The 
next  morning  it  was  evident  that  tropistic  movements  had  set  in, 
since  by  then  all  the  glands  were  in  contact  with  the  prey.  When, 
however,  in  this  species  the  stimulus  is  applied  to  the  discal  tentacles, 
the  reactions  of  the  outer  surface  tentacles  are  entirely,  or  very  nearly 
entirely,  tropistic.  The  case  of  D.  capensis  was  of  peculiar  interest, 
since  in  this  species  stimulus  of  an  outer  tentacle  procured  tropistic 
reactions  of  its  neighbors  so  that  their  glands  would  have  travelled 
the  shortest  way  to  the  place  where  the  prey  was  deposited  on  the 
discal  tentacles  (the  completion  of  the  movement  was  not  observed  by 
Behre)  and  not  as  in  D.  hinata,  at  first  nastically  (carrying  the  glands 
away  from  a  direct  path)  and  later  tropistically,  correcting  the  error. 

Behre,  having  pointed  out  such  minor  differences  in  behavior  as 
between  different  species,  remarks  that,  since  the  nastic  and  tropic  re- 
sponses are  influenced  differently  by  different  temperatures,  as  when 
the  nastic  responses  are  arrested  by  a  high  temperature  while  the  tro- 
pistic are  stimulated,  such  differences  may  account  in  part  at  least  for 
various  behaviors.     By  and  large,  however,  the  various  species  act  in 

the  same  way. 

Aggregation.  —  Darwin  observed  that,  following  stimulation,  the 
contents  of  the  gland  cells  first  and  later  of  those  of  the  pedicel,  dis- 
play changes  in  appearance  due  to  a  rearrangement  of  the  protoplasm 
and  vacuole  which  he  termed  "aggregation."  The  total  effect  is  suf- 
ficient to  be  seen  by  the  naked  eye,  if  pigment  is  present,  in  the  change 
of  color  of  the  gland.  In  this  way  it  is  possible  to  follow  the  direction, 
if  not  the  extent  of  the  movement  of  a  stimulus.  While  Darwin's  de- 
scription of  these  changes  was  incorrect,  they  stimulated  a  great 
amount  of  work  directed  toward  their  elucidation.  Those  who  have 
seen  at  Down  House  the  tools  Darwin  worked  with  may  well  wonder 
at  the  extent  and  acuteness  of  observation  which  characterize  his  work 
in  this  particular.  Taken  with  the  general  state  of  the  knowledge  of 
the  cell  in  his  day,  the  observations  of  Darwin  are  the  more  sur- 
prising. 

Darwin  gives  his  observations  as  follows:  "If ....  .  tentacles  that 
have  never  been  excited  or  become  inflected  be  examined,  the  cells 
forming  the  pedicels  are  seen  to  be  filled  with  a  homogeneous  purple 

fluid.     The  walls  are  Hned  by  a  layer  of  protoplasm ".     "  If  a 

tentacle  is  examined  some  hours  after  a  gland  has  been  excited  by  re- 
peated touches,  or  by  an  organic  or  inorganic  particle  placed  on  it,  or 
by  the  absorption  of  certain  fluids,  it  presents  a  wholly  changed  ap- 
pearance. The  cells,  instead  of  being  filled  with  a  homogeneous  purple 
fluid,  now  contain  variously  shaped  masses  of  purple  matter  suspended 

in  a  colorless  fluid By  whatever   cause    the   process   may   have 

been  excited,  it  commences  with  the  glands,  and  then  travels  down  the 
tentacles The   Httle    masses    of    aggregated    matter    are    of    the 


Francis  E.  Lloyd  —  146  —  Carnivorous  Plants 

most  diversified  shapes,  often  spherical  or  oval,  sometimes  much 
elongated,  or  quite  irregular  with  thread-  or  necklace-like  or  club- 
formed  projections they  consist  of  thick,  apparently  viscid  mat- 
ter ...  .  "  "  ....  these  Httle  masses  incessantly  change  their  form 

resembling  the  movements  of  Amoebae,  or  white  blood  corpuscles." 
"  We  may  therefore  conclude  that  they  consist  of  protoplasm." 

Francis  Darwin  in  1876  concurred  with  his  father,  but  later  in 
1888  reversed  his  position,  pointing  out  that  Darwin  was  in  error  in 
thinking  that  the  aggregated  masses  consisted  merely  of  protoplasm, 
but  that  they  are  concentrations  or  precipitations  of  the  cell  sap,  and 
that  their  amoeboid  movements  are  the  result  of  streaming  protoplasm 
which  moulds  the  passive  masses  into  a  variety  of  forms"  (Darwin, 
2d.  ed.  1875,  note  by  Francis  Darwin,  p.  34)  in  agreement  with 
Pfeffer's  views  as  pointed  out  in  his  Osmotische  tlntersuchungen.  Fran- 
cis Darwin's  volte  face  resulted  from  the  pubHcation  of  views  by 
ScHiMPER,  by  Gardiner,  and  by  de  Vries.  These  we  presently  ex- 
amine. ScHiMPER  made  his  studies  while  in  the  U.  S.  A.  where  he  was 
evidently  impressed  with  his  opportunities.  He  examined  Sarracenia 
purpurea,  Drosera  intermedia  and  Utricularia  cornuta. 

Examining  the  epidermal  and  subepidermal  cells  of  the  tissues  of 
the  lower  part  of  the  pitcher  of  Sarracenia,  when  such  cells  had  been 
exposed  to  nutrient  substances,  he  observed  that  they  showed,  in  con- 
trast to  those  not  fed,  the  following  behavior.  The  single  vacuole 
containing  tannin  was  found  to  be  now  broken  up  into  two  or  more, 
becoming,  because  of  the  concentration  of  their  tannin  solution,  more 
highly  refringent.  These  vacuoles  were  found  not  to  be  suspended  in 
the  cell  sap,  but  themselves  represented  the  whole  of  the  sap,  and  were 
found  now  to  be  suspended  in  a  swollen  protoplasm.  "  That  under 
the  influence  of  certain  substances  the  protoplasm  attains  a  greater 
capacity  for  swelhng  seems  probably  to  be  of  direct  significance  for 
nutrition." 

Recalling  Darwin's  statement  that  the  aggregations  are  suspended 
in  the  cell  sap,  Schimper  examined  Drosera  intermedia  tentacles.  Here 
he  found,  as  in  Sarracenia,  that  the  protoplasm  is  swollen,  the  tannin 
bearing  vacuoles  contracted.  "  By  plasmolysis  (with  NaCl)  it  is  seen 
with  the  greatest  clearness  that  here  also  that  which  appears  to  be  the 
cell  sap  is  really  only  the  much  swollen  protoplasm.  After  extraction 
with  alcohol,  the  protoplasm  remains  as  a  beautiful  framework  of 
meshes." 

Gardiner  in  1886,  apparently  without  having  seen  Schimper's 
paper,  described  his  own  observations  thus.     "  The  chief  phenomena 

induced  in  the  stalk  cells" "  most  marked  when  stimulated  by 

food" "are  that  the  protoplasmic  utricle  swells  up  and  encroaches 

on  its  own  vacuole,  that  granules  appear  in  the  protoplasm  and  that 
the  movement  of  rotation  increases  in  vigor."  The  cell  becomes  less 
turgid.  "  The  protoplasm  in  swelling  abstracts  water  from  its  own 
vacuole  and  in  so  doing  leaves  the  sap  in  a  more  concentrated  con- 
dition." Going  on  to  describe  the  protoplasmic  activity  of  move- 
ment he  says  that  the  reduced  vacuole  becomes  fragmented,  the  re- 
sulting small  vacuoles  become  droplets,  pear-shaped  bodies  and  long 
string-like  processes  (77  —  i),  just  as  described  by  Darwin. 


Chapter  X  —  147  —  Drosera 

De  Vries'  studies  were  most  illuminating.  He  examined  cells  of  the 
tentacle  stalk.  He  says  that  the  whole  process  of  aggregation  falls  into 
two  periods.  In  the  earlier  period  there  is  a  pronounced  increase  in  the 
rate  of  cyclosis  of  the  protoplasm,  accompanied  by  growing  complexity 
of  the  currents  ("  differentiation").  Many  accounts  ignore  this, 
though  Gardiner  mentioned  it.  During  the  second  period  there  is  a 
breaking  up  of  the  vacuole  into  a  varying  number  of  smaller  ones,  the 
more  obvious  phase  usually  seen.  These  periods  are  not  sharply  de- 
fined, the  first  passing  over  gradually  into  the  second. 

The  rapidly  circulating  protoplasm,  with  its  breaking  up  into  new 
streams,  furnishes  a  mechanism  for  subdividing  the  originally  single 
vacuole  which  in  the  meantime  loses  some  of  its  sap.  This  escapes 
through  the  wall  of  the  vacuole  (the  "  tonoplast")  into  the  space  be- 
tween this  and  the  protoplasm.  This  escaped  sap  retains  its  osmotic 
pressure,  since  tentacles  in  aggregation  are  as  rigid  as  otherwise.  Left 
behind,  however,  are  the  pigment,  albuminoids  and  tannin  which  can 
be  precipitated  within  the  resulting  vacuoles.  The  vacuoles,  however, 
are  now  less  rigid  and  more  readily  broken  up  by  the  cutting  streams 
of  protoplasm.  There  result  eventually  many  lesser  vacuoles  as  drop- 
lets of  various  shapes,  especially  slender  tubular  ones,  constantly  stirred 
up  by  the  moving  protoplasm,  and  thus  constantly  changing  positions. 
De  Vries  attempts  an  interpretation  of  these  changes  by  suggesting 
that  the  heightened  circulation  of  protoplasm  may  serve  to  facilitate 
the  movements  of  nutritive  materials  absorbed  by  the  glands;  that 
the  contraction  of  the  vacuoles  is  connected  with  the  partition  of  sub- 
stances (acids,  enzymes). 

Here  it  should  be  pointed  out  that  the  process  of  aggregation, 
thought  to  be  observed  in  stimulated  tentacles,  is  quite  independent  of 
the  process  of  inflexion  of  the  tentacles,  as  Darwin  pointed  out.  I 
myself  have  observed  that  the  bending  of  the  tentacles  occurs  in  a 
region  where  no  aggregation  had  taken  place.  As  pointed  out  by  Jost 
(Benecke-Jost,  1924)  aggregation  takes  place  in  a  primarily  stimu- 
lated tentacle  downwards  from  cell  to  cell,  but  also  later  in  those 
tentacles  secondarily  stimulated,  but  does  not  in  these  precede  the 
bending  movement,  and  moreover  proceeds  not  from  the  base  upwards 
but  from  the  gland  downward.  Aggregation  can,  therefore,  have  no 
relation  to  the  transmission  of  stimulus,  likely  enough  as  it  first  seemed. 

I  have  mentioned  above  that,  on  the  escape  of  sap  from  the  vac- 
uoles, there  is  left  behind  a  variety  of  substances,  pigment,  tannin, 
albumin,  which  can  be  precipitated  by  various  chemical  agents  (al- 
kaloids, weak  bases)  and  then  appear  as  minute  droplets  or  granula- 
tions which  coalesce  into  larger  ones,  and  which  in  the  case  of  tannin 
and  albumin  can  become  brittle  masses.  Such  precipitation  was  con- 
fused by  Darwin  with  true  aggregation.  Gardiner  called  this  "  pas- 
sive aggregation,"  Goebel  "  granulation."  Glauer  (1S87)  {fide  F. 
Darwin  in  Darwin,  1875)  and  Bokorny  (1889)  extended  the  dis- 
tinction, the  latter  recognizing  other  kinds  of  aggregation  to  the  num- 
ber of  four,  viz.:  the  contraction  of  the  entire  protoplasmic  utricle, 
contraction  and  division  of  the  vacuoles  {''  true  aggregation"),  the 
precipitation  of  albumin  in  the  vacuoles  and  fourth,  in  the  protoplasm. 

The  albumin  in  question  has  been  called  "  active  albumin"  by  O. 


Francis  E.  Lloj'd  —  148  —  Carnivorous  Plants 

LoEW  and  Bokorny,  so  designated  by  them  because  of  its  imputed 
peculiar  properties  which  place  it  in  a  category  of  substances  which 
may  be  regarded  as  bridging  the  gap  between  the  non-living  and  the 
living  parts  of  the  cell.  These  peculiarities  were  recited  by  Erna 
Janson,  who,  working  in  Loew's  laboratory,  examined  aggregation 
from  the  point  of  view  thus  indicated.  Her  paper  (1920)  cannot  be 
said  to  indicate  a  full  apprehension  of  the  observations  of  those  workers 
(Gardiner,  de  Vries,  Akerman,  especially  the  last  two  named)  who 
had  described  in  much  detail  the  curious  and  complicated  happenings 
which  take  place  during  aggregation  in  the  Darwinian  sense.  Before 
resuming  Janson's  work,  it  would  profit  us  to  look  first  at  that  of 
Akerman,  who  while  differing  from  de  Vries  in  the  interpretation  of 
certain  details,  nevertheless  agrees  with  him  about  the  general  trend  of 
affairs.  Akerman  used  pepsin  as  the  stimulating  substance  which, 
when  applied  to  the  gland,  quickly  causes  movement  responses  and  ag- 
gregation.    The  course  of  events  he  described  as  follows: 

At  first  the  peripheral  protoplasm  is  thin,   and  displays  rotation 
(cyclosis).     This  movement,  as  threads  and  ultimately  plates  of  proto- 
plasm arise,  becomes  more  comphcated,  and  changes  into  a  true  circu- 
lation,  becoming  more   and  more   active.     Meanwhile  the  peripheral 
layer  of  protoplasm   thickens,   even   to   twice   the   original   thickness. 
Folds  of  protoplasm,  impinging  on  the  vacuole,  become  strands  which 
become  thicker  and  more  and  more  extensive   till  they  cut  into  the 
vacuole  and  ultimately  break  it  up  into  numerous  small  ones.     The 
change  in  volume  of  the  protoplasm  is  accompanied  by  a  reduction  in 
volume  of  the  vacuoles,  the  substances  in  solution  therein  (the  red  pig- 
ment, tannin,  etc.)  becoming  more  concentrated  till  the  specific  gravity 
of  the  two  are  reversed,  that  of  the  sap  increasing,  as  shown  by  cen- 
trifuging.     At  length  the  vacuoles  display  remarkable  activity.     They 
elongate,  become  vermiform  and  move,  creeping  about  each  other  in  a 
most  dramatic  fashion.    In  my  own  experience  it  has  been  found  diffi- 
cult to  make  drawings  of  them  as  the  movements,  apparently  slow,  are 
fast  enough  to  defy  adequate  representation  of  the  proceedings.    Aker- 
man affords  a  fair  idea  of  the  condition  regarded  for  the  moment  as 
static  in  his  Fig.  3,  but  even  this  does  not  do  the  matter  justice.     But 
the  photographic  reproduction  of  three  exposures  of  a  single  cell  two 
and    fifteen    minutes    apart    and    two   two    minutes    apart,   are    truly 
illuminating  (77  —  i).    We  may  here  recall  de  Vries'  own  figures,  not 
to  be  ignored.     Such  activity  can  be  sustained  for  hours,  even  days. 
At  last  a  reversal  of  changes  sets  in  and  proceeds  till  at  length  the 
primary    condition    is    attained.       During    the    forward    progression 
Schimper  thought  to  have  observed  the  formation  of  new  vacuoles, 
new  evidently  as  they  did  not  contain  red  pigment;    de  Vrees  also. 
These  Akerman  did  not  see.    He  also  supports  Gardiner,  Schimper, 
Goebel  in  his  view  that  there  is  no  separation  and  independence  of  the 
vacuole  walls   {"  tonoplast"  of  de  Vries)  from  the  peripheral  proto- 
plasm, and  no  accumulation  of  water  between  them.     Indeed,  he  goes 
so  far  as  to  state  it  as  his  considered  opinion  that  the  important  and 
characteristic  feature  of  aggregation  is  the  swelling  of  the  protoplasm, 
the  vacuolar  phenomena  being  resultant  and  secondary.     In  support 
of  this  view  Akerman  again  tested  a  long  series  of  substances  and 


Chapter  X  — 149  —  Drosera 

found  that  some  (albumin,  pepsin,  peptone,  phosphoric  acid,  ethyl 
alcohol)  cause  swelling  of  the  protoplasm  and  the  accompanying  ap- 
pearances of  aggregation,  while  others  (basic  substances  such  as  am- 
monia, carbonates  of  ammonia,  sodium  or  potassium,  alkaloids),  do  not 
cause  protoplasmic  swelling,  but  only  a  precipitation  in  the  vacuole 
with  unchanged  volume.  Further,  that  these  latter  substances  can  in- 
hibit the  action  of  the  former. 

The  difference  between  true  aggregation  and  "  granulation"  in 
which  merely  precipitation  occurs  within  the  vacuole,  is  emphasized  by 
the  results  of  plasmolytic  studies.  Akerman  found  that  during  ag- 
gregation there  is  an  increase  in  turgor  pressure  of  about  5  atm.  in  the 
cells  involved.  De  Vries,  it  is  true,  found  no  changes  while  G.^rdener 
beheved  that  they  "  lose  their  turgidity"  (he  made  no  experiments  to 
show  this).  As  Coelingh  points  out,  the  difference  in  the  use  of  the 
terms  turgidity  and  turgor  pressure  (dependent  on  the  concentration  of 
the  sap)  is  to  be  noted.  In  the  case  of  cells  in  which  precipitation  oc- 
curred, there  is  no  change. 

From  experiments  to  determine  if  there  is  an  influence  of  the  gland 
on  aggregation,  Akerm.a.n  found  that  in  pieces  of  tentacle  stalk  from 
which  (a)  the  gland  with  one-third  and  (b)  with  two-thirds  of  the  stalk 
removed,  no  aggregation  at  all  could  be  procured  in  the  remaining 
portion  of  the  tentacle.  If  only  the  gland  and  one-third  of  the  stalk 
had  been  removed,  a  weak  or  no  aggregation  occurred,  according  to  the 
test  substance  used.     Akerman  tried  eight  agents. 

That  injury  is  not  involved  is  shown  by  the  fact  that  aggregation 
intervenes  in  small  pieces  of  the  upper  region  of  the  tentacle  when  pep- 
sin or  meat  extract  are  applied. 

These  results  in  Akerman's  opinion  pointed  to  the  presence  of  a 
substance,  resident  or  formed  in  the  gland  and  in  the  more  apical  stalk 
cells,  which  can  on  suitable  stimulation  procure  aggregation.  It  looks 
therefore,  as  if  two  substances  are  required  to  cause  aggregation,  one 
inherent  and  one  which  must  be  supplied  from  the  outside  as  a  stimu- 
lant. As  Darwin  recorded,  however,  aggregation  occurs  when  the 
tentacles  are  stimulated  by  mechanical  means  only.  If  a  second  sub- 
stance is  required,  this  must  mean  that  the  second  substance  is  also 
formed  in  the  gland  when  so  stimulated  {see  beyond). 

Miss  Coelingh,  working  at  Utrecht,  where  the  study  of  growth 
substances  was  then  being  actively  prosecuted,  repeated  some  of  Aker- 
man's work,  supporting  his  conclusion  that  during  the  progress  of  ag- 
gregation there  is  an  increase  in  the  osmotic  value  of  the  sap,  but  that 
this  also  takes  place  when  the  tentacles  are  successfully  stimulated  by 
mechanical  means.  Having  also  verified  Akerman's  observation  on  the 
effect  of  the  gland  on  aggregation  in  the  stalk  (finding  shght  but 
not  significant  differences)  Coelingh  proceeded  to  test  the  value  of 
his  theory  of  an  aggregation-promoting  substance.  To  this  end  she 
made  extracts  of  glands  in  distilled  water.  Such  extracts  may  be 
preserved  dry,  and  can  then  withstand  heating  to  100°  C.  In 
order  to  determine  the  virtue  of  gland-extract,  Coelingh  proceeded 
to  obtain  "empty"  pieces  of  tentacle  stalk,  that  is,  such  as  would 
not  show  aggregation  when  a  "stimulating"  agent  (beef  extract)  was 
apphed.     Such  were  obtained  of  four  kinds:    (/)  small  strips  of  leaf 


Francis  E.  Lloyd  —  150  —  Carnivorous  Plants 

blade  with  mere  stumps  of  tentacles,  (2)  such  pieces,  or  short  pieces 
of  tentacle  stalk  placed  for  some  time  in  a  slightly  hypotonic  solu- 
tion of  cane  sugar,  remaining  a  few  days  to  allow  the  putative  sub- 
stance to  escape  by  diffusion;  (j)  young,  still  unfolded  leaf  tentacles, 
the  glands  being  removed  and  {4)  a  young  but  fully  unfolded  leaf 
plunged  into  ethyl  alcohol  (96%)  for  4-6  seconds.  The  alcohol  be- 
cause of  the  relative  penetrabihty  of  the  cuticles  could  not  penetrate 
into  the  leaf  beyond  the  glands  so  that  living  tentacles  with  dead 
glands  were  provided.  Various  difficulties  involved  need  not  be  re- 
cited here. 

On  testing  the  responses  of  thus  prepared  material  to  a  "  stimulat- 
ing" substance  in  the  presence  and  absence  of  gland-extract,  it  was 
found  that,  with  few  exceptions,  aggregation  did  not  occur  in  the 
presence  of  either  alone,  but  only  when  both  were  presented  together. 
As  control  the  author  used  extracts  of  Drosera  leafstalks,  with  negative 
results. 

CoELiNGH  also  suspected  that  the  aggregation-promoting  substance 
may  occur  also  in  the  capital  cells  of  other  glandular  structures  of 
Drosera  since  by  the  use  of  a  stimulant  (such  as  pepsin)  she  found  it 
possible  to  get  aggregation  in  stalk  cells  of  sessile  and  other  glandular 
trichomes  and  in  leaf  blade  cells,  even  on  the  lower  surface  opposite 
the  bases  of  tentacles.  On  the  other  hand  she  could  never  obtain  ag- 
gregation in  other  parts  of  the  plant  where  tentacles  do  not  occur: 
petals,  sepals,  ovary-wall,  adventitious  roots,  young  stipules. 

It  was  found  also  that  there  are  substances  (saliva,  diastase,  tryp- 
sin) which  act  as  the  theoretical  aggregation-promoting  substance, 
and  in  a  search  for  a  possible  clue  as  to  its  nature,  some  such  sub- 
stances were  tested  on  '^  empty"  tissues.  Saliva  added  to  pepsin  acts 
positively,  even  after  heating  to  exclude  enzymes,  but  saliva  also  acts 
alone,  as  I  have  found.  The  composition  of  saHva  being  known,  the 
various  components  were  tried  and  only  the  phosphates  were  active. 
For  example  a  0.1%  solution  of  Na2HP04  was  active  and  sahva  di- 
luted to  this  concentration  of  that  salt  was  also.  Aggregation  follows 
on  the  use  of  pepsin  plus  growth-substance  of  Indian  corn  on  "empty" 
pieces  of  tentacle,  while  pepsin  or  meat-extract  alone  have  no  effect. 
Among  organic  N-substances,  aspartic  acid,  asparagin  and  leucine  have 
the  greatest  action;  creatin,  alanine  and  urea  are  doubtful  or  negative; 
guanine  and  ethylurethane  no  effect  whatever.  Substances  which 
lower  surface  tension  (saponin,  amylalcohol)  have  no  effect.  The 
presence  of  oxygen,  as  Darwin  had  found,  is  necessary.  Since  the 
swelling  of  protoplasm  is  considered  characteristic  of  aggregation,  per- 
haps the  chief  one  (Schimper),  it  was  thought  that  the  pB.  of  the  ag- 
gregating agents  would  betray  an  influence,  but  on  experimentation 
only  negative  results  were  obtained. 

CoELiNGH  in  a  discussion  of  all  the  facts  observed  fully  agrees  with 
Akerman,  that  two  substances  are  needed  to  procure  aggregation: 
i)  one  with  property  A,  which  does  not  cause  aggregation,  but  which 
conditions  cells  to  aggregate;  and  2)  one  with  B,  which  provides  a 
stimulus  (pepsin,  etc.)  to  aggregation.  But  it  may  not  be  assumed  that 
all  substances  have  only  one  of  these  properties  A  and  B  but  not  both, 
for  some  may  have  both  in  various  degrees  of  efficiency.    This  is  indi- 


Chapter  X —161— Drosera 

cated  in  the  behavior  of  various  substances.  It  seems  sure,  however, 
that  some  substances  have  only  the  property  B,  such  as  meat  extract, 
pepsin,  peptone  Witte,  none  of  which  can  procure  aggregation  in  empty 
cells,  that  is  cells  devoid  of  A.  But  substances  having  A  only  seem 
not  to  occur.  On  the  other  hand  some  substances  can  cause  aggre- 
gation in  both  normal  and  ''empty"  cells,  e.g.,  saliva,  gland  extract, 
etc.,  and  these,  therefore,  seem  to  have  both  properties  A  and  B. 
If  this  were  true,  we  would  be  helped  in  understanding  why  aggrega- 
tion can  be  procured  by  merely  mechanical  stimulation  by  assuming 
that  a  substance  containing  AB  is  secreted  only  on  stimulation,  then 
to  diffuse  into  the  stalk  cells.  To  this  it  can  be  objected  that  the 
cells  of  tentacle  stalks  with  the  glands  removed  can  respond  to  pepsin 
alone,  indicating  that  B  is  already  present  in  the  stalk  cells. 

But  more,  for  it  appears  that  tentacles  are  to  be  found  in  a  state 
of  aggregation  when  they  have  never  been  stimulated  in  any  way  so 
far  as  this  can  be  ruled  out  by  conditions  of  culture,  as  Homes 
subsequently  showed.  The  hypothetical  substance  we  are  looking 
for  must  therefore  inhere  and  have  both  properties  A  and  B.  Since,  if 
this  is  to  be  assumed  to  be  the  case,  aggregation  may  not  be  present 
till  stimulation  occurs,  it  must  be  argued  that  stimulation  merely  ac- 
tivates B. 

Thus  Miss  CoELiNGH  brings  her  argument  into  a  purely  theoretical 
atmosphere  which  she,  herself,  finds  hard  to  breathe,  and  says  that 
speculation  without  further  experimentation  affords  no  sure  guidance. 
But  it  must  be  evident  that  the  problem  of  aggregation  is  most  in- 
triguing. 

To  the  previously  cited  results  of  Schimper,  Gardiner,  de  Vries, 
Akerman,  in  which  they  clearly  distinguished  between  true  aggregation 
and  Goebel's  granulation,  Erna  Janson  took  a  diametrically  opposite 
position,  stating  that  all  aggregation  is  due  to  the  precipitation  of  mate- 
rials in  solution  in  the  cell  sap.  Neither  the  tonoplast  (de  Vries)  nor  the 
swelHng  of  the  protoplasm  have  any  part  in  the  process.  It  does  not 
appear  in  her  paper,  however,  that  she  has  taken  sufficient  cognisance  of 
that  condition  called  by  de  Vries  "  true  "  aggregation.  Her  figures,  which 
are  very  crude,  give  no  hint  that  she  brought  this  into  her  field  of  con- 
sideration. She  showed,  what  Bokorny  also  had  shown  at  length, 
that  certain  reagents  (alkaloids,  other  weak  bases)  procure  precipita- 
tions in  the  vacuoles.  Beyond  this  she  failed  to  show  that  "true 
aggregation"  could  thus  be  achieved.  Nor  did  Bokorny's  figure  of 
aggregation  in  Drosera  show  more.  Considered  as  contributions  to 
the  nature  of  the  vacuolar  contents,  these  papers  have  value.  As 
furnishing  enlightenment  on  the  nature  of  that  kind  of  aggregation 
which  follows  on  mechanical  stimulation  and  on  feeding  with  pepsin, 
peptone,  etc.  (though  in  these  was  suspected  the  presence  of  ammonia), 
the  work  of  Janson  is  very  limited.  For  it  is  quite  certain,  and  I 
speak  now  from  my  own  observations,  that  during  true  aggregation 
there  is  no  slightest  evidence  of  precipitation  from  beginning  to  end. 

Following  the  studies  of  Darwin  and  Gardiner  on  aggregation  a 
new  phase  of  the  subject  was  entered  upon,  in  which  the  cytological 
changes  taking  place  within  the  cells  of  the  gland  especially  were  ex- 
amined.    Lily  Huie  examined  the  behavior  of  the  nucleus  during  se- 


Francis  E.  Lloyd         —152— Carnivorous  Plants 

cretion,  digestion  and  absorption  (1897-9).  Much  later  Kruck  (1931) 
did  the  same  for  the  gland  cells  within  the  traps  of  Utricularia  (to  be 
mentioned  elsewhere). 

QuiNTANiLHA  (1926)  (on  DrosopJiyllum),  Dufrenoy  and  Homes  ex- 
amined the  cells  as  a  whole  with  reference  to  the  comportment  of  the 
vacuome.  Homes  has  carried  on  most  meticulous  studies.  He  set 
himself  the  task  of  determining  first  of  all  what  happens  during  the 
development  of  the  cell  during  the  ontogeny  of  the  leaf  and  gland. 
The  next  step  was  to  determine  if  it  is  possible  to  describe  definitely 
the  conditions  of  the  glandular  cells  during  repose,  so  far  as  this  con- 
dition might  be  reaHzed.  To  this  end  he  depended  not  on  plants  col- 
lected in  the  field,  but  on  those  raised  under  control,  and  which  there- 
fore, though  secreting,  were  known  not  to  have  been  stimulated  by 
insects,  etc.,  but  only  by  light,  humidity,  temperature.  He  then 
studied  glands  during  "  digestion",  that  is  glands  which  were  actively 
secreting  enzymes  and  absorbing. 

The  development  of  the  vacuome  during  the  ontogeny  of  the  vari- 
ous tissues,  including  the  glands,  follows  a  general  course  beginning 
with  minute  droplets  of  material  in  solution  (primordia  or  metachro- 
mata).  These  enlarge,  remaining  spherical  or  more  or  less  elongating, 
and  then  give  rise  to  rods  or  fine  filaments  which  are  straight  or  curved, 
simple  or  branched,  giving  rise  to  thicker,  short,  large  and  massive 
rods,  turning  gradually  into  vacuoles  of  very  irregular  shape.  From 
these  by  confluence  arises  a  single  massive  vacuole  with  concentrated 
contents  from  which  may  arise  a  vacuome  with  a  fine,  becoming  a 
coarser,  even  large  and  massive  network  from  which  in  turn  a  defini- 
tive single  vacuole  with  "  diluted  contents"  arises.  Homes  then  re- 
marks that  these  observed  stages  are  not  strictly  common  to  all  tissues, 
e.g.,  parenchyma  cells  do  not  pass  through  a  network  stage,  which 
stage  in  any  event  is  very  transitory,  and  marks  tissues  or  cells  which 
are  very  active,  or  are  at  a  moment  of  particular  cell  activity.  There 
are,  he  continues,  the  following  two  essential  phases:  growth  by  the 
augmentation  of  vacuolar  substance,  followed  by  growth  by  simple  hy- 
dration. All  tissues  commence  with  a  vacuome  in  the  form  of  meta- 
chromata,  and  finish  (certain  tissues,  including  the  glands,  apart)  with  a 
single  vacuole  with  dilute  contents.  The  more,  however,  a  region 
preserves  the  capability  of  specialization,  the  slower  the  evolution  of 
the  vacuole.  The  glands,  therefore,  remain  in  a  relatively  juvenile 
condition,  and  consequently  more  capable  of  immediate  activity. 

In  his  second  paper  Homes  followed  the  behavior  of  glandular  cells 
in  order  to  find  out  what  happens  in  them  during  the  secretion  of  mu- 
cilage only,  so  as  to  be  able  to  distinguish  later  between  this  activity 
and  that  which  takes  place  during  digestion  and  absorption. 

He  found  first  of  all  that  under  natural  conditions  the  gland  cells 
presented  no  uniform  structural  condition.  But  since  in  nature,  that 
is  in  plants  studied  in  situ,  it  is  impossible  to  know  the  precise  history 
of  a  given  leaf,  since  it  may  have  been  digesting  and  recovered.  Homes 
raised  plants  from  winter  buds  under  control,  regulating  within  ap- 
preciable hmits  the  amount  of  illumination  and  humidity.  Much  to 
his  surprise,  the  glands  of  such  plants  were  as  Httle  uniform  in  cytolog- 
ical  features  as  those  in  situ.     That  is,  instead  of  finding  a  uniform 


Chapter  X  —153—  Drosera 

condition  in  the  gland  cells  supposedly  in  a  state  of  repose,  he  found 
all  possible  conditions.  It  should  be  here  noted  that  various  authors 
had  previously  described  the  resting  condition  in  various  ways.  Darwin, 
ScHiMPER,  DE  Vrees,  Bokorny,  Goebel,  Akerman  thought  that  in 
this  condition  the  gland  cells  have  a  single  large  vacuole.  Gardiner 
described  the  gland  cell  as  consisting  of  a  fine  meshwork  of  protoplasm 
holding  red  sap  in  the  interstices.  Dufrenoy  held  a  similar  view,  be- 
lieving that  there  are  many  small  vacuoles.  Quentanilha  found  a 
meshwork  of  threadlike  vacuoles.  Allowing  for  discrepancies  of  under- 
standing it  is  obvious  that  Homes'  findings  bring  these  various  views 
into  some  harmony,  since  no  one  condition  prevails  in  the  resting  gland 
cells. 

Having  compared  living  and  fixed  material  it  was  established  to 
Homes'  satisfaction  that  his  fixative  (osmic  acid,  2%,  i  part;  mercuric 
chloride  2.5%,  4  parts)  preserved  the  cell  structure  accurately.  Know- 
ing also  that  the  glands  in  the  middle  of  the  leaf  are  more  active  in 
secretion  than  those  standing  along  the  limb  (since  the  inhibiting 
action  of  the  environment  on  the  former  is  less  effective),  he  made  a 
statistical  study  of  the  gland  cells  as  to  the  form  of  the  vacuome.  But 
a  statistical  study  called  for  standard  conditions.  These  were  supplied 
by  growing  plants  under  three  sets  of  conditions,  inciting  minimum, 
medium  and  maximum  secretory  activity.  From  these  plants  Homes 
obtained  evidence  of  the  behavior  of  the  gland  cells  under  these  various 
conditions,  and  found  that,  though  all  states  of  activity  occurred  in  all 
cases,  there  was  a  preponderance  of  one  state  over  the  others  in  any 
one  experimental  set  of  conditions.  Relying  on  the  relative  abundance 
of  the  different  structural  states  of  activity,  four  ''  witness"  glands 
were  chosen  to  serve  as  criteria,  called  types  A,  B,  C,  and  D.  Briefly 
stated,  and  neglecting  details,  the  outer  glandular  cells  of  these  types 
have  vacuomes  of  the  following  character: 

T5T)e  A.  the  vacuome  consists  of  a  single  large  vacuole. 

Type  B.  —        —  —    —  numerous  small  droplets. 

T3T)e  C.  —        —  —    —  fewer,  larger  droplets. 

Type  D.  —        —  —    —  a  thicker  reticulum. 

It  was  then  found  that  glands  at  minimum,  medium  and  maximum 
secretory  activity  displayed  the  above  cytological  characters  in  the 
following  percentages: 


Glands  of 

A 

B 

C 

D 

Variants 

Minimum  activity 
Medium          " 
Maximum       " 

97% 
0 
0 

0 

30% 
15% 

0 

65% 

25% 

0 
0 

60% 

3% 
5% 
0 

showing  clearly  that  when  glands  are  at  minimum  activity,  the 
glandular  cells  are  in  the  state  in  which  they  have  a  single  large  vacu- 
ole, while  when  in  maximum  activity,  the  vacuome  is  a  thick  reticulum. 
Intermediate  conditions  characterize  glands  of  approximately  medium 
activity.  In  the  second  layer  there  is  a  similar  course  of  events,  but 
these  are  not  so  pronounced,  and  do  not  follow  the  changes  of  the  outer 
layer  promptly,  scarcely  ever  doing  more  than  fragmenting  the 
vacuole  into  two  or  three  parts.    The  cells  of  the  parenchyme  bell  (the 


Francis  E.  Lloyd  —  164  —  Carnivorous  Plants 

third  layer)  never  show  these  changes.  There  would,  therefore,  seem 
to  be  a  difference  of  function  of  these  layers,  the  innermost  taking  no 
part  in  secretion.  Under  severe  conditions  caUing  for  active  secretion, 
the  outer  layer  may  display  a  certain  degree  of  plasmolysis,  the  cells 
recovering  by  drawing  water  from  the  second  layer.  Homes  regards 
this  plasmolysis  as  a  normal  event,  and  attributes  it  to  the  concentra- 
tion of  the  mucilage  by  rapid  evaporation  so  that  it  becomes  hyper- 
tonic to  the  cell-sap.  Though  normal,  it  occurs  infrequently  in  plants 
under  usual  conditions.  Such  plasmolysis  can  cause  directly  the  frag- 
mentation of  the  vacuole,  as  shown  by  plasmolysis  studies  in  general. 

Summarizing,  it  seems  certain  that  the  rate  of  secretion  obeys 
changes  in  the  external  conditions,  quite  apart  from  any  responses  to 
irritability  to  chemical  substances  which  are  presented  at  and  during 
digestion.  The  changes  described  as  aggregation  under  which  these 
can  be  subsumed  are  therefore  not  alone  the  result  of  stimulation  in 
the  usual  sense  (mechanical,  chemical). 

The  purpose  of  Homes'  final  paper  was  to  determine  if  during  di- 
gestion there  is  a  specific  activity  of  the  glandular  cells  different  from 
that  during  secretion  of  mucilage.  The  same  methods  were  used  as 
previously  and  the  various  behaviors  of  gland  cells  fed  with  raw  egg 
albumin  compared  with  those  from  leaves  without  nourishment.  We 
recall  that  during  secretion,  according  to  its  intensity,  any  one  of  four 
types  of  condition  above  mentioned  may  be  found,  these  types  being 
a)  cells  with  one  large  vacuole,  h)  cells  with  many  small  round  drop- 
lets, c)  cells  with  irregular  droplets,  and  d)  cells  with  a  thick  reticulum. 

"If  now  the  glands  are  fed,  at  whatever  state  they  may  be  at  the  moment,  a  first 
rapid  change  will  occur  in  the  direction  from  A  to  D,  or  from  B  to  D,  but  if  they  are  al- 
ready in  the  state  D,  no  change  will  be  apparent.  Later,  after  the  reticulimi  stage  has 
been  reached,  a  gradual  concentration  of  the  vacuole  takes  place  till  a  single  concentrated 
vacuole  is  present  in  each  glandular  cell.  Then  this  single  vacuole  becomes  more  and 
more  hydrated  and  finally  a  large  diluted  vacuole  is  present  and  persists  till  the  end  of  the 
digestion.  Practically  any  type  of  vacuole  present  during  digestion  can  thus  be  found  in 
a  "resting"  tentacle,  and  it  is  consequently  impossible,  by  examining  a  single  tentacle,  to 
tell  if  it  is,  was  or  is  going  to  be  in  the  process  of  digestion. 

"But  the  vacuolar  changes  revealed  by  the  statistical  study  can  also  be  related  to  the 
intensity  of  the  secretory  process  or  even  more  generally  to  the  exchange  of  water  between 
the  gland  and  the  external  medium.  The  first  change  towards  the  reticulum  expresses 
the  increase  of  secretion  which  takes  place  immediately  after  feeding;  the  later  hydration 
of  the  single  vacuole  indicates  the  decrease  of  secretion  and  the  beginning  of  absorption. 

"Aggregation  is  thus  not  the  characteristic  result  of  'excitation'  in  a  carnivorous  plant, 
but  simply  the  expression  of  any  rapid  change  in  the  water  content,  as  can  happen  during 
secretion  or  absorption  of  a  liquid."     (Homes  in  ep.). 

Thus  stands  the  problem  at  the  present.  We  are  impressed  with 
what  appears  to  be  a  relatively  simple  cytological  behavior  of  the 
cytoplasm  (not  speaking  for  the  moment  of  the  nucleus)  and  by  the  phys- 
iological complexities  indicated  by  the  behavior  of  the  glands  and 
tentacles  during  the  process  of  digestion  during  which  there  must  be 
secretion  and  escape  of  enzyme  (even  though  they  may  be  al- 
ready present  in  the  mucilage),  acid  or  acids,  a  substance  inhibiting 
bacterial  action  (Goebel),  perhaps  an  odorous  principle,  and  a  more 
active  secretion  of  mucilage  which  ceases  at  the  end  of  digestion  and 
absorption.  Meanwhile,  absorption  takes  place.  Simple  as  the  cyto- 
logical behavior  may  be,  it  is,  I  feel,  not  yet  thoroughly  understood. 


Chapter  X  —  155  —  Drosera 

From  studies  during  the  past  three  summers  I  can  confirm  Homes  in 
his  claim  that  resting  glands,  that  is  glands  found  on  young  vigorous 
resting  leaves,  can  be  found  in  a  resting  condition,  meaning  with  cells 
having  a  single  grand  vacuole,  or  with  its  cells  in  a  condition  which  is 
distinctly  otherwise,  that  is,  with  an  appearance  which  may  be  in- 
terpreted as  a  mass  of  smaller  irregular  vacuoles,  or  as  a  network,  prob- 
ably fairly  represented  by  Homes'  fig.  60-63,  1932-  Guided  by  what 
we  have  seen  in  the  tentacle  cells,  in  which  it  seems  reasonably  certain 
that  the  vermiform  condition  can  give  rise  by  confluence  to  a  network, 
temporary  though  it  may  be,  we  may  agree  that  the  same  occurs  in 
the  gland  cells,  as  Homes  believes,  and  he  may  be  quite  right. 

I  have  seen  evidence,  however,  that,  during  the  period  after  feed- 
ing (with  raw  and  purified  egg  albumin,  pepsin,  peptone  Witte, 
saliva)  while  aggregation  follows  in  the  tentacle  cells,  meaning  specifi- 
cally the  breaking  up  of  the  grand  vacuole  into  smaller  ones,  these  be- 
coming numerous,  slender,  actively  agitated  vermiform  bodies  of  high 
refringence  (as  so  well  depicted  by  Akerman),  to  suffer  at  length  con- 
fluence and  total  reversion,  this  series  of  changes  is  not  followed  in  the 
cells  of  both  glandular  courses,  though  some  approach  to  it  may  be 
observed  in  the  lateral  epidermal  cells  seen  en  face,  and  in  the  apical 
cells  of  a  gland  which  were  distinctly  not  in  the  grand  vacuolar  state, 
having  instead  a  number  of  smaller  irregular  vacuoles,  in  appearance 
at  any  rate. 

Lateral  cells  viewed  en  face  present  a  crenated  outline  in  conformity 
with  the  buttresses  which  cut  up  the  periphery  of  the  cell  into  bays, 
seen  by  Franca  in  Drosophyllum.  I  observed  that  in  these  cells,  in 
saliva,  a  droplet  containing  pigment  would  be  formed  in  each  bay, 
there  being  as  many  droplets  as  bays.  Dufrenoy's  drawings  indicate 
that  he  saw  the  same  condition,  which  he  called  aggregation,  but  ap- 
parently did  not  connect  the  early  form  of  the  vacuole  with  the  cre- 
nated walls.  These  droplets  formed  in  the  bays  might  remain  as  such 
or  might  run  together  to  form  a  single  drop  containing  all  the  pigment 
of  the  cell,  depending  apparently  on  the  size  of  the  droplets  and  the 
vigor  of  the  process.  In  the  apical  cells,  also  in  saliva,  the  whole  mass 
of  vacuoles,  whatever  may  have  been  their  exact  state,  became  con- 
fluent and  there  was  formed  a  single  large  drop,  corresponding  to 
Homes'  condensed  vacuole.  Here  then  we  have  a  case  which  appears 
to  conform  with  Homes'  observations.  On  the  other  hand,  when  the 
gland  cells  are,  to  begin  with,  in  the  dilute  vacuolar  state,  each  having  a 
single  grand  vacuole  (Homes' "vacuole  diluee")  when  treated  with 
egg  albumin,  raw  or  purified,  the  first  sign  of  response  is  to  be  seen  in 
ten  minutes  in  the  cells  of  the  internal  course  in  the  lateral  region  of 
the  gland.  The  change  advances  toward  its  apex.  In  90  minutes  simi- 
lar droplets  appear  in  the  epidermis  lateral  cells  low  down  near  the 
base  of  the  gland,  again  advancing  toward  the  apex.  These  droplets 
do  not  apparently  appear  in  the  grand  vacuole  but  in  the  cytoplasm, 
but  this  is  a  point  very  difficult  to  make  out.  In  the  course  of  time 
the  confluence  of  droplets  yields  a  single  large  drop.  This  seems  to  be 
what  Darwin  saw:  "  In  15  min.  I  distinctly  saw  extremely  minute 
spheres  of  protoplasm  aggregating  themselves  in  the  purple  fluid;  these 
rapidly  increased  in  size,  both  within  the  cells  of  glands  and  of  the 


Francis  E.  Lloyd  —  156  —  Carnivorous  Plants 

upper  ends  of  the  pedicels."  In  my  preparations  aggregation,  in  the 
generally  understood  sense,  occurred  in  the  upper  end  of  the  tentacle 
stalk.  Similar  appearances  were  seen  in  glands  treated  with  pepsin, 
and  peptone  Witte  (each  i%  soln.),  in  that  the  first  thing  noted  is  the 
appearance  of  drops  and  there  is  no  breaking  up  of  the  grand  vacuole 
into  parts,  as  is  to  be  constantly  observed  in  the  tentacles.  In  KH2- 
PO4  (tried  by  Coelingh  as  a  component  of  sahva)  in  i  %  soln.  the 
gland  cells  behaved  so  far  differently  that  its  action  can  be  only  doubt- 
fully compared  with  that  of  saliva  since  vacuoles  without  pigment  are 
formed  which  push  aside  the  cell  contents,  producing  a  distinctly  path- 
ological effect.  Aggregation  occurred  in  the  tentacles,  but  this  also  oc- 
curs in  water.  In  order  to  check  on  my  observation,  I  took  a  piece  of 
leaf  which  had  lain  in  oil  for  48  hours,  and  which  showed  very  clearly 
that  there  was  no  aggregation  at  all  in  any  gland  cells.  After  removing 
the  oil,  which  does  not  adhere  to  the  glands  because  of  the  mucilage,  I 
treated  it  with  saliva.  In  15  min.  droplets  had  appeared  in  the  lateral 
cells  of  the  inner  course  of  gland  cells  (C-II),  the  epidermis  (C-I)  re- 
maining quite  clear.  At  the  end  of  50  min.  all  the  cells  of  C-II  had  each 
a  large  drop,  appearing  in  the  apical  cells  last.  All  the  lateral  cells  of 
C-I  had  drops  in  them,  a  few  small  droplets  in  some  apical  cells.  In 
an  hour's  time,  droplets  had  appeared  in  many  of  the  apical  cells  of 
C-I  and  they  were  evidently  enlarging. 

These  observations  seem  to  indicate  that  during  the  ordinary  course 
of  events  when  the  glands  are  secreting  mucilage  the  condition  of  the 
gland  cells  may  be  found  in  various  states  such  as  Homes  had  de- 
scribed. If  the  glands  are  fed  they  may  follow  one  of  two  courses. 
If  the  gland  cells  are  filled  with  smaller  vacuoles  (are  aggregated),  these 
become  confluent  to  form  a  single  large  drop,  the  condensed  vacuole  of 
Homes.  If  the  gland  cells  are  in  the  resting  condition,  that  is,  are  in 
the  grand  vacuolar  stage  with  no  sign  of  aggregation,  the  course  of 
events  on  feeding  consists  in  the  formation  of  small  droplets  in  the 
cells  of  the  inner  glandular  course  in  the  lateral  regions  of  the  gland. 
This  advances  till  the  apical  cells  of  this  course  have  all  formed  drop- 
lets. These  grow  until  by  their  size  they  form  an  optically  dense  layer. 
In  the  meantime,  droplets  have  appeared  in  the  epidermis,  in  the 
lateral  region.  This  also  progresses  toward  the  apex,  until  all  the  epi- 
dermal cells  are  involved.  The  drops  all  contain  pigment.  In  the 
course  of  change,  the  gland  becomes  denser  and  darker  in  color  as  Dar- 
win observed.  During  six  hours  aggregation  had  occurred  in  the  tenta- 
cles and  by  next  morning  it  had  progressed  quite  to  their  bases  and 
into  the  leaf  tissue  about  their  bases. 

Whatever  the  final  agreement  as  to  the  course  of  aggregation,  which 
appears  to  be  different  in  detail,  if  the  same  in  results,  in  gland  and 
tentacle,  the  whole  activity  is  most  extraordinary,  and  demands  much 
further  study  before  any  final  answer  can  be  given  as  to  the  relation  of 
aggregation  to  secretion  and  absorption. 

Studies  of  cytoplasm  and  nucleus.  —  The  studies  of  the  living  cell 
leading  to  our  knowledge  of  aggregation  led  to  a  desire  to  know  more 
of  those  details  of  behavior  of  the  cytoplasm  and  especially  of  the 
nucleus  which  cannot  be  discovered  by  the  methods  used  for  obser- 
vation of  the  li\'ing  material.    Accordingly  the  method  of  fixation  fol- 


Chapter  X     —157— Drosera 

lowed  by  sectioning  and  staining  came  into  use  first  by  Gardiner, 
followed  later  by  Lily  Huie,  Rosenberg  and  Konopka.  Homes' 
work  we  have  already  mentioned  as  especially  bearing  on  aggregation. 
Gardiner  believed  that  the  mucilage  of  the  glands  is  secreted  as  a 
"  formed  matter"  within  vacuoles  which  grow  after  stimulation,  the 
protoplasm  being  reduced  in  amount  to  be  later  restored  by  new 
growth  from  the  vicinity  of  the  nucleus.  He  observed  the  presence  of 
the  crystalloid  "  rhabdoids".  It  is  not  unfair  to  say  that  his  work  was 
rather  meagre  in  amount,  and  he  did  not  use  staining  reactions.  Huie 
on  the  other  hand  did  a  sustained  piece  of  work.  She  traced  rhythmic 
changes  in  cytoplasm,  nucleus  and  nucleolus,  attempting  to  interpret 
these  as  chemical  and  morphological  reactions  connected  with  and 
following  stimulation  by  food  materials  of  various  kinds,  which,  ac- 
cording to  their  nature,  were  followed  by  quantitatively  various  re- 
actions, though  quahtatively  similar.  We  may  leave  out  of  account 
the  reactions  to  non-organic  substances  which  produced  in  any  event 
only  very  fleeting  cytological  changes.  Following  feeding  there  is  a 
reduction  in  the  volume  of  the  basophile  cytoplasm  until  it  becomes 
scanty  in  amount  and  eosinophile  in  character  confirming  Gardiner's 
similar  observation.  Following  this  but  preceding  the  restoration  of  the 
cytoplasm  there  is  an  increase  in  the  volume  of  the  basophile  chromo- 
somes accompanied  by  a  reduced  amount  of  nucleolar  chromatin.  The 
beginning  of  restoration  of  the  cytoplasm  is  to  be  seen  in  an  accumula- 
tion of  neutrophile  dense  cytoplasm  surrounding  the  nucleus  correspond- 
ing chemically  (as  indicated  by  color  reaction)  and  morphologically 
(size  of  granules)  to  the  intranuclear  plasm.  At  completion  of 
cytoplasmic  restoration  the  nuclear  chromatin  is  reduced  in  amount, 
and  the  nucleolar  chromatin  increases.  What  is  left  of  the  chromoso- 
mal bodies  (chromatin)  is  finally  aggregated  into  definite  V-shaped 
bodies  of  a  constant  number  (eight)  characteristic  of  the  plant,  which 
"  proves"  that  this  is  a  mark  of  nuclear  activity  and  not  merely  a 
feature  of  mitosis.  Huie's  second  paper  (1899)  adds  nothing  to  the 
above  account  in  general,  but  she  concludes  that  the  nucleus  is  the 
seat  of  metaboHc  activity,  and  that  the  usefulness  of  a  food  can  be 
judged  by  the  condition  of  the  ''  nuclear  organs." 

Rosenberg  (1899)  supported  and  extended  Huie's  studies.  He 
saw  similar  changes,  but  in  lesser  degree,  in  the  endodermis,  tracheids 
and  stalk  cells.  He  diverged,  however,  from  her  interpretation  of  the 
masses  of  chromatin  as  chromosomal,  for  he  found  them  in  no  constant 
number,  nor  did  he  find  splitting  as  in  prophase,  but  on  the  contrary 
much  difference  in  form  and  size.  He  observed,  however,  certain 
bodies  lying  on  or  near  the  nuclear  membrane,  called  generally  "pseu- 
donucleoli",  which  he  termed  prochromosomes.  These  occur  in  a  con- 
stant number,  and  are  the  chromosomes. 

Konopka  and  Ziegenspeck  (1929)  studied  D.  rotimdifolia,  D. 
binata  and  D.  anglica.  After  the  glands  have  been  fed  24  hours  with 
various  proteins,  including  pollen,  droplets  appear  in  the  cytoplasm 
near  the  nucleus  (intermediate  food  products)  at  first  always  in  the 
inner  gland  cells  layer,  later  in  the  outer,  and  also  in  endodermis 
(parenchyme  bell)  tracheids,  stalk  cells  and  leaf  blade  cells.  They  in- 
crease in  number  and  size,  and  at  length  are  overtaken  by  a  sort  of 


Francis  E.  Lloyd  —  158  —  Carnivorous  Plants 

disruption,  show  hollows  and  cracks,  and  appear  to  be  in  some  vague 
but  perhaps  intimate  connection  with  the  nucleus,  indicating  that  they 
are  products  taken  up  by  it.  At  the  "  high  point"  of  feeding  the 
nucleus  has  enlarged  and  the  membrane  becomes  less  definite  and 
finally  disappears  so  that  the  chromosomes  and  nuclear  materials  ap- 
pear to  he  free  in  the  cytoplasm,  or  at  any  rate  in  a  nuclear  lymph. 
KoNOPKA  observed  in  the  resting  stage  the  bodies  which  Rosenberg 
called  prochromosomes,  but  could  not  confirm  his  belief  that  they  oc- 
cur in  a  constant  number,  regarding  them  rather  to  be  of  nucleolar 
nature.  After  feeding  the  nucleoli  become  reduced  in  size,  and  lie  in  a 
large  vacuole  ("  Hof")  from  which,  in  many  cases,  he  could  observe 
canals  leading  to  the  cytoplasm,  bringing  the  nucleus  into  more  inti- 
mate contact  with  the  cytoplasm.  Here  it  is  to  be  regretted  that  cost 
prevented  the  reproduction  of  his  photographs,  since  the  figures  are 
unsatisfactory  to  a  degree,  and  show  no  convincing  evidence  of  this. 
The  chromatin  on  the  other  hand  exhibits  increase  and  occurs  in  larger 
masses  of  various  form.  After  24  hours  they  become  very  evident  by 
their  clearness  and  size,  and  besides  granules  of  various  sizes  there  ap- 
pear rod-shaped  structures  ("  Rhabdoids"?)  lying  near  the  periphery 
(of  the  nucleus)  sometimes  paired  and  connected  by  fibers  with  the 
interior  of  the  nucleus,  but  in  no  constant  number.  The  nucleolus  has 
now  been  dissolved,  and  appears  as  a  pale,  rather  than,  according  to 
Rosenberg,  a  distinct  body.  The  chromatin  rods  now  unite  to  form 
threads  and  rings.  Among  them  the  granules,  which  Rosenberg 
thought  to  be  prochromosomes,  are  secondary  nucleoh,  indicating 
enhanced  nucleolar  activity.  They  always  he  in  vacuoles  ("  Hof") 
and  have  no  connection  with  the  nuclear  structure,  show  disinte- 
gration and  disappearance  at  the  high  point  of  the  reaction.  During 
long  periods  of  digestion  these  events  appear  not  to  progress  steadily, 
but  rather  to  pulsate  —  there  is  a  rhythm  in  behavior.  These  nucleolar 
structures  are  regarded  by  Konopka  as  supplying  materials  for  forming 
mucilage  and  for  digestion,  and  he  is  inchned  to  regard  the  central  and 
peripheral  nucleoh  as  having  different  functions.  The  whole  aspect  of 
the  changes  in  the  chromatin  and  nucleolus  indicates  that  these  changes 
are  connected  with  ferment  production.  With  the  escape  of  the  fer- 
ment the  chromatin  shrinks  in  ring  forms,  so  that  one  might  regard  the 
nucleus  now  as  being  in  a  spireme  stage,  leading  to  mitosis,  or  merely 
as  a  reformation  of  chromosomes  in  a  somatic  condition.  They  are  at 
all  events  true  chromosomes. 

It  has  been  attempted  to  summarize  the  above  work  with  not 
too  great  brevity,  so  that  the  reader  may  appreciate  the  difficul- 
ties of  interpretation.  It  is  not  too  much  to  say  that,  while  it  has 
been  shown  experimentally  that  changes  in  the  cell  do  indeed  occur 
during  digestion,  and  while  we  have  become  aware  to  some  extent 
what,  in  detail,  these  changes  are,  it  must  still  be  recognized  that  we 
are  yet  lacking  general  agreement  as  to  the  precise  nature  of  many  of 
these  details,  and  much  less  are  in  a  position  to  attribute  precise  func- 
tions to  the  various  structures  seen. 

Digestion;  enzymes. — Darwin  (1875)  proclaimed  the  digestive 
power  of  the  secretion  of  Drosera  tentacles.  He  fed  the  leaves  proteins, 
connective  tissue,  cartilage,  gelatin,  to  find  that  these  were  attacked. 


Chapter  X —169— Drosera 

The  presence  of  acid  being  a  condition  for  peptic  digestion,  he  observed 
that  the  inner  tentacles  of  the  disc  of  the  leaf  were  more  acid  than  the 
outer.  This  may  have  been  because  of  the  greater  number  of  tentacles 
per  unit  of  area.  Darwin  thought  that  the  acidity  of  the  secretion  of 
the  leaf  is  increased  on  the  absorption  of  nitrogenous  substances  de- 
rived from  the  captured  insect. 

Opposed  to  the  general  trend  of  opinion  was  that  of  Morren 
(1875),  Batalin  (1877),  TiscHUTKiN  (1889),  and  of  Dubois  (1899),  all 
of  whom  were  persuaded  that  the  digestion  of  insects  by  Drosera  is 
always  the  result  of  bacterial  action,  so  that  the  results  of  others,  to 
be  detailed  below,  were  not  without  opposition. 

Rees  and  Will  (1875)  made  a  glycerin  extract  of  the  leaves  and 
found  it  weakly  acid  and  to  contain  an  enzyme  which  in  the  presence 
of  weak  HCl  exercised  a  peptonizing  action.  Lawson  Tate  (1875) 
collected  the  secretion  from  the  tentacles,  sweeping  the  leaves  with  a 
feather  (he  used  Drosera  dichotoma),  mixed  it  with  water  and  pre- 
cipitated it  with  cholesterin.  The  precipitate  was  found  to  coagulate 
milk,  and  this  he  referred  to  the  action  of  a  ferment  which  he  named 
droserin.  In  191 1  Miss  J.  White  reinvestigated  the  matter;  leaves 
were  removed,  washed  with  previously  boiled  water  with  added  chloro- 
form and  chopped  with  a  sterile  knife.  The  bits  were  then  placed  in 
lukewarm  boiled  water  with  chloroform  as  antiseptic,  shaken  vigor- 
ously for  2  hours.  To  the  filtrate  was  added  an  equal  part  of  satu- 
rated ammonium  sulfate,  from  which  a  filtrate  was  obtained  which 
contained  a  principle  which  could  attack  fibrin  but  only  in  an  acid 
medium.  The  product  gave  the  biuret  reactions.  Abderhalden 
(1906)  had  found  that  in  its  presence  peptides  are  not  spHt. 

Dernby  in  191 7  obtained  a  glycerin  extract  of  the  leaves  from 
which  by  means  of  dialysis  he  obtained  an  enzyme  which  he  regarded 
as  a  pepsin.  This  worked  at  an  acidity  of  pR  5  as  optimum.  No 
tryptase  or  ereptase  was  found. 

Miss  Robinson  (1909)  tested  the  digestive  effect  of  Drosera  on 
"  purer  proteins"  then  available.  She  found  that  acid-albumin,  alkali 
albuminate  and  edestin  were  digested,  but  "  somewhat  less  readily" 
than  dry  egg-white,  fibrin,  tendo-mucoid  and  nucleoproteins.  Col- 
lagen and  elastin  proved  entirely  indigestible.  Though  creatin  did  not 
cause  a  bending  of  the  tentacles,  it  was  readily  dissolved,  meanwhile 
remaining  in  contact  with  the  leaf  for  three  days.  It  is  important,  in 
view  of  Darwin's  opposed  idea,  that  the  lack  of  movement  of  the 
tentacles  is  not  an  indication  of  the  non-nutritional  value  of  the  sub- 
stances applied;  nor  did  Darwin  find  that  the  positive  response  indi- 
cates the  contrary. 

Beginning  in  1930  Okahara  pubHshed  a  series  of  papers  deahng 
with  the  matter.  He  first  dealt  with  the  question  of  the  actual  oc- 
currence of  a  digestive  ferment  in  Drosera.  The  leaves  were  extracted 
with  glycerine  and  water  for  several  days  (with  toluene)  and  the  press 
juice  then  filtered  off.  The  mother  solution  thus  obtained  showed 
strong  acidity.  The  enzyme  was  separated  by  means  of  acetone  and 
redissolved  for  experimentation. 

He  concluded  that  there  exists  in  the  leaves  of  Drosera  a  powerful 
proteolytic  enzyme   which,   acting    on    proteins,    hydrolyses   them    to 


Francis  E.  Lloyd  —  160  —  Carnivorous  Plants 

proteoses  and  peptones,  with  an  optimum  activity  at  pB.  1.5,  an  acidity 
high  for  plant  enzymes  and  suggesting  a  resemblance  to  animal  pepsin. 
In  order  to  determine  to  what  extent  the  Drosera  pepsin  is  identical  in 
action  with  animal  pepsin,  Okahara  observed  the  influence  of  poisons 
(quinine  hydrochloride  and  atoxyl)  on  them.  He  failed  to  find  a  strict 
parallel,  since  the  enzyme  activity  under  certain  conditions  was  re- 
pressed in  the  one  and  accelerated  in  the  other. 

Okahara's  second  paper  (1930J)  is  of  a  more  general  nature,  deal- 
ing with  the  effect  of  toxic  substances  on  pepsin  with  a  view  to 
illuminating  his  earher  observations  cited  just  above.  Though  the  sub- 
ject may  be  regarded  as  controversial,  it  remains  true  that  there  is  a 
substance  capable  of  digestion  of  proteins  in  Drosera  leaves. 

In  a  third  paper  (1931)  Okahara  gave  the  results  of  inquiry  into 
the  optimum  acidities  of  various  acids  for  the  enzyme  activity.  He 
had  observed  the  occurrence  of  formic  acid  in  Drosera,  and  was 
prompted  to  investigate  the  comparative  effect  of  various  acids  on  the 
action  of  a  proteolytic  enzyme  on  edestin  and  found  that  the  optimum 
acidities  for  various  acids  differ,  and  that  the  decrease  from  the  op- 
timum acidity  parallels  the  decrease  of  the  electrical  dissociation  con- 
stant. 

While  Okahara's  second  and  third  papers  do  not  immediately 
concern  Drosera,  they  have  been  mentioned  in  this  connection  since 
their  bearing  will  doubtless  be  made  clear  by  further  studies.  His 
fourth  paper,  however,  bears  directly  on  the  controversial  question, 
do  bacteria  play  a  role  in  the  digestion  of  carnivorous  plants  and  in 
particular  of  Drosera?  Nepenthes  was  examined  also  in  this  connection. 
The  paper  was  published  in  1933.  The  author  isolated  from  the  plants 
studied  a  series  of  bacteria  and  moulds.  Experiments  with  these 
in  media  held  at  two  acidities,  />H  5-6  and  /?H  3.3,  afforded  the  following 
results.  Three  of  the  moulds  acted  on  Witte's  peptone  and  glycocoll 
at  ^H  3.3.  The  other  organisms  attacked  various  nitrogenous  com- 
pounds supplied  (Witte's  peptone,  glycylglycine,  glycocoll  and  alanine) 
falling  into  two  groups  which  cooperate  to  reduce  these  substances  to 
ammonia.  Okahara  concludes,  that,  while  the  plant  enzymes  may 
themselves  take  a  leading  part  in  the  breaking  down  of  proteins, 
such  organisms  as  were  isolated  from  the  plants  mentioned  ''may 
also  cooperate  in  the  completion  of  the  process."  Okahara  to  this 
extent  supports  the  views  of  Labbe  (1904)  and  of  Stutzer  (1926), 
the  former  for  Drosera  and  the  latter  for  Utricularia. 

Following  Okahara,  Linderstr0m-Lang  and  Holter  (1934)  again 
raised  the  question  whether  digestion  in  Drosera  rotundifolia  is  es- 
sentially different  from  that  in  other  plants  and  similar  to  that  in 
animals,  or  do  they  depend  on  resorption  of  the  products  of  bacterial 
action? 

Accordingly,  the  secretions  from  the  glands  and  from  the  leaf 
tissues  (from  the  blade,  that  is)  were  examined  separately,  in  order 
to  answer  specific  questions,  to  wit:  (i)  whether  proteinase  is  secreted 
by  the  glands;  (2)  what  position  among  the  proteolytic  enzymes 
it  takes;  (3)  in  what  quantities  it  occurs  and  how  these  quantities 
behave  in  relation  to  the  endoproteinase  to  be  expected  in  the  leaf 
tissues. 


Chapter  X —161— Drosera 

Their  method  of  obtaining  the  enzymes  was  as  follows.  The  se- 
cretion of  the  glands  was  taken  up  by  filter  paper  and  because  of  its 
viscosity  was  diluted.  That  of  the  leaf  tissues  was  extracted  with 
glycerin.     Both  were  tested  on  edestin. 

It  was  found  that  the  gland  secretion,  with  its  optimuni  at  pB. 
^.^,  was  far  more  active  than  that  of  the  leaf  blade,  with  its  opti- 
mum at  4.6,  or  even  of  the  secretion,  extracted  from  removed  glands 
with  maximum  activity  at  ^H  3.8.  It  is  admitted  that  the  last  may 
be  due  to  the  overlapping  of  the  action  of  the  two  enzymes  in  ques- 
tion. The  authors  concluded,  "We  have  to  do  with  a  quite  different 
distribution  of  two  enzymes,  of  which  the  one  occurring  in  the  se- 
cretion is  a  proteinase  for  the  purpose  of  digestion."  Further  it  was 
pointed  out  that  the  distinct  function  of  a  proteinase,  optimum  activity 
at  pB.  3.2,  does  not  harmonize  with  Dernby's  results  who  found 
the  maximum  activity  on  acid  albumin  at  ^H  5,  nor  with  Okahara's 
with  carmine  fibrin,  maximum  activity  at  pE.  1.4.  Dernby's  results 
may  have  come  about  because  he  used  masses  of  total  leaf,  but  those 
of  Okahara's  are  regarded  as  distinctly  antagonistic.  This  may  be 
due  to  the  possibiUty  that  the  Japanese  plant  may  differ  physiolog- 
ically from  the  European.  Merck's  pepsin  acted  on  edestin  at  pB. 
1.8;  therefore,  the  proteinase  of  Drosera  and  pepsin  are  not  iden- 
tical. ,         .       o  , 

Recent  and  still  unpublished  work  done  by  A.  Akerman  and 
L.  G.  M.  Baas  Becking  using  D.  capensis  yielded  definite  evidence 
that  peptic  fermentation  takes  place.  The  method  used  was  the  fol- 
lowing: A  single  tentacle  on  the  leaf  edge  was  plunged  into  distilled 
water  held  in  a  small  paraffin  cup.  Under  these  conditions  the  water 
retained  its  initial  pB.  of  5.8  for  at  least  24  hours.  When,  however, 
a  solution  of  NH4CI  (cone.  25  mgr/L)  was  used  the  ^H  fell  from  5.8 
to  2.0,  from  which  it  is  evident  that  this  salt  served  to  stimulate  the 
production  of  acid.  Equivalent  solutions  of  CaCl2,  NaCl  and  MgClz 
gave  no  action,  while  KCl  produced  only  a  very  slight  change  in 
pB.  When  egg  albumin  {pB  7.0)  was  placed  on  a  tentacle,  the  pB 
changed  to  3.0.  Carmine-fibrin  when  treated  with  a  leaf  extract  was 
digested  indicating  the  presence  of  a  peptic  enzyme,  effective  at  an 
optimum  pB  of  2-3.0  while  it  has  been  shown  by  J.  de  Zeeuw  that 
digestion  in  Nepenthes  takes  place  at  about  pB  4.0.  Since  the  leaf 
extract  was  not  bacteria  free.  Prof.  Baas  Becking  (Sept.  1935)  pointed 
out  that  the  proof  for  Drosera  is  not  absolute,  and  final  proof  will 
require  experiments  with  bacteria-free  plants.  It  is  further  noted 
that  Drosera  proteinase  takes  a  middle  position  between  pepsin  and 
papain  {in  ep.). 

Darwin  observed  that  milk  when  placed  on  Drosera  leaves  was 
soon  coagulated.  Green  mentions  this  under  the  heading  "Vegetable 
Rennet,"  presumably  because  of  the  more  obvious  inference  that  milk 
coagulation  is  brought  about  by  a  rennet,  as  perhaps  is  the  case 
when  Galium  verum  is  used  for  the  preparation  of  curds  for  cheese 
making,  also  mentioned  by  Green.  As  has  been  seen,  a  similar  ac- 
tion of  Pinguicula  in  coagulating  milk  is  not  attributed  to  the  pres- 
ence of  a  rennet  (Dernby  191 7),  and  if  so,  this  may  be  equally  true 
of  Drosera.     Darwin  does  not  speak  of  a  rennet,  but  does  remark 


Francis  E.  Lloyd 


—  162  —  Carnivorous  Plants 


on  the  digestive  effect  of  the  secretion  on  casein,  which  harmonizes 
with  Dernby's  view  that  a  trypsin  is  present  (in  Pinguicula). 

The  general  conclusion  may  be  drawn  from  the  foregoing  summaries 
of  work  done  on  digestion  in  Drosera  that  this  plant  does  indeed 
secrete  a  ferment  which  can  act  upon  proteins  and  reduce  them  to 
substances  which  can  be  and  are  absorbed  for  nutriment.  If  food 
materials  in  the  form  of  an  abundance  of  insects,  pollen,  etc.  (Darwin) 
are  present  so  that  the  antiseptic  effect  is  incomplete,  bacteria  may 
(particularly   according  to   Okahara)    assist  in   rendering  such  foods 

available  to  the  plant. 

The  abundance  of  fats  in  the  bodies  of  insects  would  suggest 
the  presence  of  a  lipase  in  Drosera,  but  such  has  not  been  found. 
Whether  lecithin  and  fatty  acids  might  be  absorbed  by  infiltration 
(as  lecithin  is  taken  in  by  the  human  intestine  according  to  Shocot- 
YOFF,  fide  ScHMiD,  1912)  is  a  matter  of  speculation,  though  Goebel 
thought  that  he  found  fats  to  be  absorbed  by  the  glands  of  Pingui- 
cula  and  Utricularia. 

Significance  of  carnivory  for  the  plant.  ~  Although.  Darwin  left 
no  room  for  doubt  that  Drosera  is  able  to  catch,  digest  and  absorb 
the  products  of  digestion,  it  remained  a  question  if  this  abihty  is 
of  advantage  to  the  plant  in  furthering  its  growth  and  development. 
It  was  natural  that  Francis  Darwin  (1878)  should  take  up  the  cud- 
gels in  his  father's  behalf.  He  grew  plants,  obtained  from  the  field, 
in  shallow  dishes  duly  protected  so  as  to  prevent  insects  from  reaching 
them.  These  he  divided  into  two  lots,  one  of  which  he  fed,  the  other 
remaining  unfed.  The  result  showed  the  indubitable  conclusion  that 
the  plants  which  were  fed  were  more  vigorous,  produced  more  and 
stronger  inflorescences  and  seed  than  the  unfed.  Similar  results  were 
obtained  by  Kellermann  and  v.  Raumer  (1878).  Busgen  (1883) 
then  pointed  out  that  plants  grown  from  winter  buds  show  a  wide 
range  of  development  to  begin  with,  so  that  an  experiment  with  these 
is  really  a  handicap  race.  To  avoid  this  he  used  plants  grown  from 
seed,  so  that  his  plants  started  out  from  scratch.  The  results  were 
even  more  striking  than  those  of  the  previous  workers.  In  the  table 
herewith  the  results  of  the  three  authors  are  compared  in  terms  of 
percentage,  the  quantities  for  the  unfed  plants  being  100:  — 

Fr.  Darwin  Kellermann  &  Busgen 

1878  V.  Raumer,  1878  1883 


Number  of  inflorescences  164.9 

Number  of  capsules  i94-4 

Total  weight  of  seed  379-7 


100  152:     100  300:     100 

100  174:     100  533:     100 

100       capsules  205:     100 


And  in  terms  of  dry  weight:  Solution  Spring 

nutrient  water 


Winter  buds,  i  Feb 173:     100 

Winter  buds,  3  Apr 213:     100 

Entire  plant,  end  of  2nd.  year 296:     100  174:     100 

Inflorescences 141.  i :     100 

Plants  minus  Inflorescences 12 1.5:     100 

{flde  Busgen) 

While  these  figures  speak  for  themselves,  I  venture  to  quote  briefly 
from  these  authors.     Kellermann  and  von  Raumer:    "The  general 


Chapter  X  —163— Drosera 

result  is  not  to  be  doubted,  that  in  all  essential  points  the  fed  plants 
forge  ahead  of  the  unfed";  Busgen:  "We  must  therefore  take  it 
as  proven  that  animal  stuflfs  are  transferred  to  the  plant  and  that 
they  are  of  great  significance  to  it  for  its  development,  namely,  for 
the  development  of  its  fruit,  etc.";  and  finally  Francis  Darwin 
said:  "These  results  show  clearly  that  insectivorous  plants  derive 
great  advantage  from  animal  food." 

Just    previously    to    the    publications    of    Kellermann    and    v. 
Raumer's  work  Pfeffer  (1877)  had  grown  Drosera  rotundifolia  plants 
from  winter  buds  under  cover  to  prevent  the  access  of  insects,  and 
observed  that  they  grew  vigorously,  evidently  leading  to  the  conclu- 
sion that  the  carnivory  is  not  always  a  necessity.     Regel  (1879)  went 
further  than  this,  claiming  that  the  carnivorous  habit  is  a  distinct  dis- 
advantage  because   he   observed   that   the   leaves    {Drosera  filiformis) 
were  often  injured  by  feeding,  and  that  fed  leaves  die  sooner  than 
unfed   ones.     It  is,   however,   well   known,   as   Goebel   pointed   out, 
that  overfeeding  often  causes  decay  of  the  leaf;    and  to  deplore  the 
earlier  passing  of  fed,   not  overfed,   leaves  is  to  ignore   the  possible 
good  which  may  have  accrued  to  the  plant  in  the  meantime.     And 
Haberlandt  was  of  the  opinion,  based  on  field  observations  in  Java, 
that  Nepenthes  pitchers  appeared  to  have  but  a  meagre  booty,  that 
insectivory  is  a  sort  of  semi-superfluous,  luxus  adaptation.     In  this 
Massart  {through  Haberlandt),  having  had  similar  field  experiences, 
agreed.    Nor  did  Goebel  regard  the  role  of  insectivory  in  the  struggle 
for  existence  very  seriously  —  it  is  useful,  he  said,  but  not  obligatory, 
and  the  plant  does  not  meet  much  competition  in  its  natural  habitat. 
Such  more  or  less  contrary  views  have  in  the  long  run  been  brought 
to  a  focus  in  the  idea  now  generally  accepted  that  carnivory  is  a  very 
striking  and  useful  adaptation,  which,  though  not  always  obHgatory, 
can   under   circumstances   better   the    condition    of    the    plant.      Ad- 
ditional   questions,    no   less   important,    however,    arose.      It    will    be 
noted  that  the  above  researches  were  overshadowed  by  the  sole  idea 
of  animal  food,  as  supplying  chiefly  proteids,  and  this  has  crept  into 
the  textbooks  as  the  dominant  thought.      Stahl,  in   1900,  published 
a   long   dissertation   on   the   significance  of  mycorrhizal  arrangements 
in  plants,   in  which  he  instituted  comparisons  between  those  plants 
with  the  carnivorous  plants,  all  of  which  grew  in  sterile  soils.     Sar- 
racenia  had  been  shown  by  MacDougal  (1899)  to  be  free  of  mycor- 
rhiza,  nor  had  it  been  found  otherwise  in  Pinguicula  (Schlicht,  1889, 
through  Stahl),  Drosera,  or  Nepenthes  (Janse,   1896,  through  Stahl) 
and  this  is  now  known  to  be  the  case  for  all  carnivores.     As  com- 
pared with  true  parasites,  mycorrhizal  plants  and  autotrophic  plants 
with  very  extensive  roots,  those  plants  which  avail  themselves  of  capil- 
lary water  and  in  which  many  forms  of  animal  life  perish  and  are 
entangled  in  the  foHage  {e.g.  mosses),  and  carnivores  have  poor  roots 
and  therefore  httle  means  for  obtaining  the  materials  of  the  soil^  no- 
tably lacking  in  salts,  especially  those  of  phosphorus  and  potassium, 
in  which  they  grow.    And  while  it  may  be  true  that  it  may  be  shown 
by    experiment    that    carnivores    may    obtain    all    their    requirements 
through  their  roots,  if  plentifully  supphed  to  the  substrate,  this  does 
not  show  that  in  a  state  of  nature  their  arrangements  for  obtaining 


Francis  E,  Lloyd     —164— Carnivorous  Plants 

these  materials  are  superfluous  or  useless,  since  they  live  in  nature 
and  not  under  experimental  conditions.  Stahl  indicated  the  low  ash 
content  of  the  leaves  of  carnivores,  and  advanced  this  additional  fact 
as  an  argument  for  the  significance  of  carnivory.  There  is  generally 
also  a  depression  of  transpiration  due  to  situation  in  the  habitat, 
and  where  transpiration  is  low,  some  other  means  of  obtaining  salts 
is  called  for.  The  leaves  of  Nepenthes,  when  exposed  to  situations 
where  transpiration  can  act  freely,  do  not  make  pitchers,  and  have 
a  higher  ash  content  than  those  low  down  and  exposed  to  higher 
humidity,  where  also,  as  in  the  case  of  seedlings  (Goebel),  pitchers 
are  immediately  produced  following  the  cotyledons.  Stahl  thus 
argues:  the  carnivory  has  been  dominated  by  the  idea  that  it  is 
an  adaptation  to  obtain  proteins;  but  the  soils  in  which  carnivorous 
plants  grow  are  notoriously  poor  ones,  and  therefore  the  question  of 
how  the  carnivorous  plants  obtain  substances  aside  from  nitrogen  is 
in  need  of  investigation.  This  in  1900.  Pfeffer  had  indicated 
this  problem  (1877),  thinking  particularly  of  phosphorus  compounds, 
and  his  and  Stahl's  suggestions  were  fruitful  ones.* 

In  191 2,  Weyland  and  Schmid  both  entertained  this  idea,  Wey- 
LAND  showing  that  there  was  Kttle  of  K  and  P  to  be  found  in  the 
meagre  roots  of  Drosera,  and  Schmid  finding  these  elements  present 
in  the  leaves  of  this  plant  after  insect  feeding,  whereas  before  this 
they  were  not  to  be  found  or  only  in  meagre  amounts  (Ruschmann, 
1914).  Oosterhuis  (1927)  pushed  investigation  further  along  in  this 
direction.  He  asked  the  question  whether  the  lack  of  any  particular 
mineral  in  the  soil  could  be  compensated  for  by  insect  feeding.  He 
summed  up  his  experiments  by  saying  that  (i)  mineral  nutrients  can 
be  taken  up  by  the  roots;  (2)  even  if  an  abundant  supply  of  nutrient 
salts  is  present,  the  plants  can  not  grow  as  well  as  if  insect-fed;  (3)  in 
view  of  the  fact  that  in  his  experiments  plants  grown  on  a  substrate 
poor  in  salts  but  insect-fed  prospered  beyond  plants  grown  on  salt- 
rich  medium  but  not  insect-fed,  he  argued  that  the  significance  of 
insectivory  Hes  in  the  uptake  of  the  cleavage-products  of  proteins 
out  of  insects  by  the  plant.  The  absorption  of  salts  from  the  in- 
sect is  not  excluded,  but  is  not  the  important  factor.  Summarily 
stated,  in  the  lack  of  nitrogen  in  the  soil,  the  plants  can  be  supphed 
this  by  insect  prey,  and  then  flourish  better  than  when  grown  in 
a  substrate  with  Knop's  solution  supplying  all  elements.  That  plants  fed 
with  insects  have  a  higher  nitrogen  content  than  those  grown  ap  seedlings 
on  turf  carrying  Knop's  solution  strengthened  him  in  this  view. 

Behre  (1929),  stimulated  by  an  expression  of  doubt  by  Diels 
(1906)  as  to  the  value  of  insectivory,  asserted  that  such  value  had 
not  been  proved,  and  instituted  experiments  of  his  own  to  test  the 
matter.  He  found  that  plants  grown  in  distilled  water  but  plenti- 
fully fed  with  flies  or  meat  throve  very  much  better  than  those  grown 
in  distilled  water,  or  even  in  a  v/eak  Knop  solution  (M  cone),  in 
both  cases  not  fed.  The  differences  noted  became  much  more  evident 
toward  the  end  of  the  second  summer.  He  concluded  that  insectivory 
is  indeed  of  great  moment  to  the  plant.  An  important  value,  it 
seemed  to  Behre,  hes  in  the  taking  up  of  inorganic  salts,  and  that 

*  Peyronel  (1932)  argues  that  if  mycorrhizal  fungi  are  parasitic,  they  should  be  found 
in  carnivorous  plants,  but  he  found  none  in  Drosera  or  Pinguicnla.  Mycorrhiza  occurs 
chiefly  when  soils  are  poor  in  nitrates  and  ammoniacal  salts,  but  rich  in  organic  matter. 


Chapter  X —165— TtTosera. 

the  lack  of  such  salts  in  the  natural  environment  is  compensated  for 

in  this  way. 

Came  Oudm.\n  in  1936  with  further  proofs.  The  virtue  of  his 
experiments  lies  in  the  fact  that  his  experimental  plants  {Drosera 
capensis)  were  grown  from  seed,  and  the  seedlings  carefully  chosen 
for  their  uniformity,  and  in  the  further  fact  that  the  plants  were 
grown  on  a  very  uniform  substrate  of  powdered  peat  which  had  pre- 
viously been  very  thoroughly  washed.  Several  sets  of  plants  with 
{a)  distilled  water,  (b)  nutrient  solution  without  N,  and  (c)  Knop's 
solution,  were  set  up  and  either  not  fed  at  aU,  or  fed  with  asparagin 
1.5%,  peptone  1.5%,  gelatin  2%  (against  dist.  water  alone),  gelatin 
plus  Knop  (against  dist.  water  only  in  the  substrate),  Knop  solution 
alone,  and  finally  with  insects.  He  found  that  plants  grown  on  salt- 
poor  substrate,  but  fed  insects,  were  quite  normal.  Plants  grown 
on  N-free  substrate  could  make  use  of  asparagin  and  peptone  as  well 
as  the  N-compounds  occurring  in  insects.  Plants  well  supplied  with 
nutrient  salts,  incl.  nitrogen  compounds,  can  grow  well  in  the  absence  of 
leaf-feeding  with  insects.  Drosera  can  obtain  nitrogen  if  this  is  not  pres- 
ent in  the  substrate,  through  its  leaves,  and  this  in  organic  form. 
It  can  also  take  up  through  its  leaves  not  only  N,  but  other  salts 
as  well.  Oudman's  conclusions  correspond  quite  fully  with  those  of 
OosTERHUis.  There  can,  therefore,  be  no  sort  of  doubt  that  the 
ability  to  absorb  substances  (mineral  salts  as  well  as  N)  is  of  sig- 
nificance to  the  plant.  It  should  be  added  that  gelatin  and  glutin, 
a  derivative  of  gelatin,  cause  degeneration  of  the  tentacles,  so  that 
in  time  they  entirely  disappear. 

The  presence  of  ascorbic  acid  in  D.  intermedia,  suspected  by  Weber 
(1938),  was  soon  after  demonstrated  in  the  leaves  of  this  plant  by 
Neubauer  (1939)  who  claims  to  have  found  a  content  nearly  as  high  as 
that  of  a  "well  known  paprika  preparation",  which  itself  contains 
20-fold  that  of  lemon  juice.  On  this  Weber  (1940)  again  examined 
the  leaves  of  the  same  species  after  having  been  fed  peptone  powder, 
and  obtained  evidence  of  a  heightening  of  cell  activity,  accompanied  by 
an  increase  in  vitamin-C  content.  This  being  a  non-nitrogenous  com- 
pound, the  significance  of  these  results  is  quite  problematical. 

Literature  Cited: 

Akermam,  a.,  Untersuchungen  iiber  die  Aggregation  in  den  Tentakeln  von  Drosera  rotun- 

difolia.     Bot.  Notiser  1917:145-192. 
Ames,  O.,  An  easy  method  of  propagating  Drosera  filiformis.     Rhodora  1:172,  1899. 
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Chapter  X  — 167  —  Drosera 

(b)  Further  studies  of  cytological  changes  produced  in  Drosera.     Q.  Journ.  Mic.  Sci. 
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Okahara,  K.,  Studies,  III.  The  effect  of  various  acids  on  the  digestion  of  protein  by  pep- 
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droserone.    Journ.  Chem.  Soc.  1935,  1:336-338. 
Withering,  W.,  Arrangement  of  British  Plants,  ed.  3,  London,  1796. 
WoLLNY,  Ew.,  Die  Zersetzung  der  organischen  Stoffe  und  die  Humusbildung.    Heidelberg, 

1897. 


Chapter  XI 
CARNIVOROUS  FUNGI 

Occurrence.  —  Habit.  —  Glands.  —  Secretion.  —  Digestion. 

Among  the  multifarious  activities  of  fungi,  that  of  zoophagy  has 
been  well  known  for  a  very  long  time.  Of  this  one  of  the  best  known 
examples  is  the  behavior  of  Cordyceps,  which  invades  the  bodies  of 
caterpillars  of  various  species  and  sizes.  After  displacing  the  substance 
of  the  body  of  the  larva  attacked,  preserving  its  form,  however,  in  the 
sclerotium  thus  formed,  the  fungus  then  sends  up  a  linear  stalk  bearing 
the  fruiting  bodies,  the  sclerotium  being  buried  in  the  soil  (since 
it  was  there  that  the  larva  was  destroyed),  and  the  fruiting  stalk 
rising  above  in  free  air.  The  study  of  this  kind  of  pathology  in  rela- 
tion to  lower  forms  (algae,  small  water  animals)  was  being  pursued 
by  the  botanist,  W.  Zopf,  in  Austria,  when  there  came  to  his  atten- 
tion just  previous  to  1888  a  fungus  which  attacked  eelworms  {Anguil- 
lulidae) . 

In  the  various  cultures  which  he  was  observing,  there  were  numer- 
ous living  eelworms  and  many  dead  ones  tangled  with  and  variously 
penetrated  by  the  hyphae  of  the  fungus.  The  question  then  arose 
in  his  mind  as  to  whether  the  fungus  is  purely  saprophytic,  pene- 
trating only  already  dead  worms,  or  does  the  fungus  attack  and  kill 
the  Kving  animal?  In  answering  this  question  experimentally,  Zopf 
made  the  first  discovery  of  a  fungus  which  traps  a  living  animal. 

The  fungus  was  Arthrohotrys  oligospora,  first  described  by  Fres- 
ENros  (1850-63).  It  is  found  in  all  kinds  of  more  or  less  decayed 
matter  —  mats  of  old  algae  for  example  —  and  makes  a  thin  veil  of 
mycelium  of  septate  hyphae  over  the  surface.  From  it  there 
extend  slender  septate  conidiophores  bearing  pear-shaped  two-celled 
spores.  The  peculiar  feature  is  the  occurrence  on  the  hyphae  of  many 
slings  or  loops  of  various  sizes,  formed  by  the  sharp  curving  of  a 
growing  branch  which  turns  upon  itself  and  fuses  by  its  end  with  its 
base.  From  one  loop  a  second  and  from  this  a  third  may  arise,  and 
thus  is  formed  a  tangle  of  loops  lying  in  all  positions,  as  Woronin 
had  already  observed.  It  was  Zopf,  however,  who  first  saw  that 
living  eel-worms  were  actually  caught  by  these  loops,  either  by  the 
tail  or  by  the  head.  The  fact  that  when  once  the  worm  has  by  chance 
inserted  one  end  or  the  other  into  a  loop,  it  cannot  free  itself  again, 
was  definitely  observed.  The  eelworm  he  used  was  Telenckus  scandens, 
which  infests  wheat.  One  observed,  on  being  caught,  struggled  vio- 
lently for  a  half-hour,  then  became  quieter  and  finally  died  in  2.5 
hours.  Why  the  eelworm  cannot  free  itself  when  once  trapped  he 
attempted  to  explain  by  analogy,  using  as  a  model  a  rubber  loop 
just  big  enough  to  allow  a  finger  to  enter.  When  one  attempts  to 
withdraw  the  finger,  the  rubber  band  clamps  on  the  surface  and  holds 
the  finger.     The  clamping  effect  is  due  to  springiness  of  the  loops,  he 


Francis  E.  Lloyd 


170  — 


Carnivorous  Plants 


thought.    After  the  animal  succumbs,  branches  from  the  loop  penetrate 
its  body,  and  withdraw  nutriment  (Text  fig.  4). 

What  happens  in  the  case  of  another  similar  organism,  Dactylella 
bembicoides  Drechsler,  was  explained  by  Couch  (1937).  In  this 
plant  the  loops  are  composed  of  a  short  branch  of  three  cells  turned 
upon  themselves.  Fusion  occurs  between  the  end  and  basal  cells, 
and  a  neat  ring  is  thus  formed.  By  growing  the  fungus  on  agar 
to  allow  of  clear  microscopic  observation,  he  saw  an  astonishing  thing, 
that  when  an  eelworm  pokes  his  head  or  tail  into  a  ring,  the  ring 
immediately  clamps  on  it  by  the  sudden  swelling  of  the  three  cells 
(Text  fig.  4,  d,  e,  i).  Couch  records  his  opinion  that  the  rings  are 
formed  most  abundantly  in  media  poor  in  "available  food  supply," 


Fig.  4.  —  A,  B,  Zoophagus  insidians  (after  Gicklhorn  1922);  C,  Dactylella  tylopaga 
attacking  Amoeba  (after  Drechsler  1935^);  D,  E,  F,  Dactylella  bembicoides  which  attacks 
nematodes  (after  Couch  1937);  G,  H,  Arthrobotrys  oligospora,  which  attacks  nematodes 
(after  Zopf  1888);   I,  Dactylella  betubicoides  (after  Couch). 

judging  from  experiments  which  he  did.  He  attempted  to  get  rings 
to  close  on  fine  glass  rods,  with  limited  success,  so  that  it  seemed 
unlikely  that  mechanical  stimulation  suffices.  He  did  find,  however, 
that  heat  (water,  at  t,3  to  75°  C.)  will  cause  the  rings  to  close, 
but  that  the  temperature  of  the  animal's  body  enters  in  as  a  factor 
in  nature  is  quite  unlikely.  Couch  therefore  fell  back  on  the  perhaps 
correct  explanation  that  the  fungus  responds  to  a  chemical  stimulus 
from  the  worm's  body.  A  1%  solution  of  lactic  acid  caused  a  slight 
swelling.  While  this  was  uncertain.  Couch  observed  that  in  every 
case  "when  a  nematode  thrusts  its  head  or  tail  into  one  of  the  rings 
it  closes  practically  instantaneously  by  the  simultaneous  swelHng  of 
the  three  cells  of  the  ring."  Later,  new  hyphal  branches  penetrate 
the  body  of  the  prey.  Among  these  predacious  species  are  included 
Trichothecium,  Arthrobotrys,  Dactylaria,  Monacrosporium  and  Dactylella, 
all  figured  by  Drechsler  (1934a).  Still  others  may  be  expected  to 
turn  up. 

But  not  all  the  ring  forming  fungi  act  in  the  same  way.    We  owe 


Chapter  XI  — 171  —  Carnivorous 


much  knowledge  about  these  to  Drechsler,  who  points  out  (1933c) 
that  some  species  have  loops  the  component  cells  of  which  do  not 
swell  to  constrict  the  loop,  and  that  these  catch  their  prey  by  means 
of  a  strong  adhesive  found  on  the  inner  surface  of  the  loop.  It  is 
not  unlikely  that  this  is  the  case  in  the  plant  studied  by  Zopf  who 
did  not  observe  constriction  of  the  loops.  One  species  has  the  loop 
borne  on  a  very  slender  stalk  which  may  be  broken  off  during  the 
struggles  of  the  worm,  but  this  does  not  obviate  death  and  destruc- 
tion, as  the  cells  of  the  loop  can  still  form  their  penetrating  hyphae 
(Drechsler,   1933^). 

Some  of  these  species,  e.g.  Dactylaria  Candida  (Nees)  Sacc,  have 
in  addition  to  the  loops  a  second  organ  for  the  catching  of  the  prey, 
called  "globular"  bodies.  These  are  round  knobs  on  short  hyphae. 
On  the  knob  is  secreted  a  patch  of  strong  adhesive,  by  which  the 
eelworm  is  caught.  In  the  course  of  a  short  time,  a  penetrating  haus- 
torium  grows  through  the  adhesive  pad  and  enters  the  animal's  body. 
In  these  and  the  other  cases  above  mentioned,  after  the  prey  is  per- 
meated with  haustorial  hyphae,  and  after  these  have  withdrawn  all  the 
available  nutriment,  the  fungal  protoplasm  withdraws,  leaving  an 
empty  shell  (Drechsler,  19336,  c;   1935c). 

A  similar  method  of  capture  is  used  by  a  species  in  which  the 
catching  organs  consist  merely  of  the  ends  of  hyphal  branches,  pro- 
vided, as  on  the  globose  organ,  with  an  adhesive.  The  penetrating 
haustorial  tube  swells  up  after  entrance,  and  from  the  sweUing  the 
haustorial  complex  of  hyphae  grows. 

A  similar,  very  striking  case  of  a  fungus  which  catches  armoured 
Rotatoria,  the  first  of  its  kind  known,  was  described  in  191 1,  follow- 
ing Zopf's  original  discovery  of  a  carnivorous  fungus  in  Arthrobotrys, 
by  SoMMERSTORPF  Under  the  name  Zoophagus  insidians  n.  gen.,  n.  sp. 
This  plant  grows  epiphytically  on  Cladophora,  and  consists  of  a  net- 
work of  septate  hyphae  which  bear  "short"  branches  scattered  at 
irregular  intervals  along  them.  These  short  branches  have  dense 
glistening  contents,  and  are  the  organs  of  capture.  Rotatoria  (of 
the  genera  Salpina,  Metopidia,  Colurus,  Monostyla),  feeding  among 
the  threads  of  the  algae  and  associated  fungus,  take  hold  of  the  ends 
of  the  short  branches,  and  remain  attached,  unable  to  break  loose. 
By  pulHng  ofT  a  newly  captured  animal  he  (Sommerstorff)  was  able 
to  determine  that  the  end  of  the  hypha  had  enlarged,  apparently  by 
the  swelling  of  the  membrane,  which  now  took  up  methylene  blue 
with  avidity.  Previous  to  having  captured  an  animal,  there  appears 
to  be  no  adhesive,  since  no  detritus  could  be  observed  sticking  to 
the  ends  of  the  short  branches,  nor  did  they  take  up  the  stain.  Som- 
merstorff concluded  that  the  swelling  takes  place  on  the  stimulation 
occurring  when  the  animal  takes  the  short  branch  into  its  mouth. 
Generally  the  prey  cannot  escape,  despite  his  size.  But  as  it  has 
no  other  organs  of  locomotion  save  the  cilia,  the  'tail'  only  is  avail- 
able for  struggling.  If  he  can  get  leverage  with  this  on  a  neighboring 
algal  filament,  he  may  and  sometimes  does  escape.  After  struggling 
ceases  and  death  is  intervening,  the  capturing  branch  grows  into  a 
penetrating  tube  which  then  sends  numerous  thin-walled  haustorial 
hyphae  to  withdraw  nutriment. 


Francis  E.  Lloyd  —  172  —  Carnivorous  Plants 

This  organism  was  studied  later  also  by  Mirande  and  by  Gickl- 
HORN.  The  former  generally  verified  Sommerstorff's  observations. 
He  observed,  also,  the  capture  of  Stylonychia  and  of  other  organisms 
than  armoured  Rotatoria,  which  have  the  same  manner  of  feeding. 
By  staining  he  thought  to  have  identified  a  substance  in  the  short 
h}phae  capable  of  quick  swelling. 

GiCKLHORN  however  paid  closer  attention  to  the  contents  of  the 
short  hyphae,  the  organs  of  capture.  By  means  of  staining  and  solu- 
bility tests  he  came  to  the  conclusion  that  an  oval  glistening  body, 
observable  in  the  short  hyphae,  is  a  discrete  body  of  callose  capable 
of  great  swelling.  It  is  always  present  in  organs  ready  for  capture 
as  a  definite  plug.  In  unstimulated  branchlets  it  is  always  on  the 
inside;  on  stimulated  ones  it  occurs  as  a  mucilaginous  cap.  Dead 
organs  are  always  free  of  the  mucilage  and  are  cut  off  from  the  bear- 
ing hypha  by  a  partition.  After  a  short  time  following  capture  (lo- 
30  minutes)  the  callus  plug  is  emptied  into  the  maw  of  the  prey  and 
spreads  out  entangling  the  whole  of  its  ciliary  mouth  apparatus. 
There  is  no  further  discharge  of  mucilage  after  the  expulsion  of  the 
one  shot.  These  results  were  indeed  foreshadowed  by  Sommerstorff, 
but  not  proven.  His  suggestion  that  the  mucilage  was  provided  by 
the  swelling  of  the  outer  membrane  Gicklhorn  could  not  verify. 
GiCKLHORN  on  the  other  hand  failed  to  show  how  the  callus  plug 
makes  its  escape,  since  no  pore  or  other  point  of  exudation  could  be 
observed  (Text  fig.  4A,  b). 

Gicklhorn  studied  the  mode  of  capture  and  its  sequelae,  confirm- 
ing and  amplifying  such  observations  as  had  been  made  by  Sommer- 
storff. He  observed  in  freshly  caught  animals  which  had  succeeded 
in  escaping  that  the  ciliary  apparatus  was  in  a  swollen  condition. 
He  asserts  that  only  certain  sorts  of  Rotatoria  are  caught  {Colurus, 
Distyla,  Metopidia,  Monostyla,  Salpina  and  Squalella  species)  and 
never  those  which  are  supplied  with  a  strong  ciliary  apparatus,  such 
as  Brachionus,  Noteus,  Anuria,  Rotifer  and  Philodina,  all  of  which 
were  subjected  to  experimental  observation.  He  was  unable  to  ob- 
serve that  infusoria  such  as  Stylonychia,  Stentor,  Paramaecium  and  the 
flagellates  Euglena  and  Paranema  were  ever  caught.  This  fact,  which 
he  held  to  be  such,  indicates  at  once  that  not  only  is  the  plant  a 
capturing  one  but  that  the  animal  must  be  capturable.  He  admits 
observing  some  infusoria  "caught",  but  they  were  stuck  to  the  catch- 
ing organs,  and  this  does  not  prove  that  they  were  properly  caught 
in  the  manner  of  Rotatoria.  He  concludes  that  instead  of  speaking 
of  the  animal  as  being  caught  one  should  say  that  it  gets  itself  caught, 
since  only  those  armoured  Rotatoria  which  are  able  to  swallow  the  bait 
can  be  caught.  In  a  culture  with  many  animals  the  process  was 
followed  and  this  account  is  given.  If  an  animal  hits  against  the 
main  hypha  or  against  a  short  hypha  sideways,  these  bend  a  little 
under  the  impact  and  then  recover.  The  animal,  on  hitting,  infolds 
its  ciliary  apparatus;  if,  however,  it  approaches  a  short  hypha,  the 
trapping  organ,  end  on,  so  that  it  enters  the  ciliary  apparatus,  the 
latter  immediately  clamps  down  on  it  and  draws  it  in.  This  is  done 
repeatedly  for  5-10  minutes  during  which  interval  repeated  attempts 
are  made  by  the  ciliary  apparatus  to  open,  only  to  clamp  down  again 


Chapter  XI  — 173  —  Carnivorous  Fungi 

in  response  to  the  mechanical  stimulus  provided  by  the  short  hypha. 
At  the  end  of  this  interval  it  can  now  be  shown  by  staining  methods 
that  the  callus  plug  has  been  emptied  and  that  it  has  swollen  and 
spread  out  to  involve  the  entire  ciliary  apparatus,  which  is  now  ren- 
dered useless.  In  this  condition  the  animal  finds  its  weak  foot  useless 
in  effecting  escape,  and  in  the  course  of  another  period  of  twenty 
minutes  it  ceases  to  struggle.  From  these  observations  Gicklhorn 
draws  the  following  conclusions.  In  the  first  stage  of  capture,  there 
is  no  adhesive  effect  on  stimulation  of  the  short  hypha,  as  Sommer- 
STORFF  thought,  but  repeated  mechanical  grasping  of  it  by  the  re- 
tractile ciliary  apparatus  of  the  animal.  Secondarily  there  follows 
the  excretion  of  the  mucilage.  This  is  an  active  process  on  the  part 
of  the  hving  short  hypha  on  stimulus,  and  is  not  a  simple  swelling 
of  the  membrane.  He  tried,  with  success,  to  stimulate  short  hyphae 
to  throw  off  their  mucilage  by  stroking  them  with  a  fine  hair.  The 
short  hypha  now  begins  to  send  out  haustoria  which  penetrate  through- 
out the  body  of  the  animal.  Even  at  the  end  of  digestion,  the  mucilage 
plug,  which  can  still  be  seen,  is  found  to  have  hardened  and  become 
yellow  in  color,  holding  the  shell  of  the  animal  in  position.  The 
growth  of  the  haustoria  proceeds  till  the  interior  of  the  body  is  a  mass 
of  hyphae  which  send  out  conidiophores  projecting  from  the  animal 
and  in  swarm-spores  produced  in  a  sac  which  escape  through  the 
mouth  end. 

A  plant  with  a  similar  method  of  capturing  its  prey  as  that  em- 
ployed by  Zoophagus  insidians  is  Sommerstorffia  spinosa,  described  by 
Arnaudow  (1923).  Both  of  these  species  have  been  collected  in 
Massachusetts  and  observed  by  Sparrow  (1929). 

An  extraordinary  group  of  fungi  which  prey  upon  species  of  Amoeba 
and  shelled  rhizopods  has  been  uncovered  and  studied  by  Drechsler. 
His  accounts  include  the  minutiae  of  taxonomic  interest  as  well  as 
the  mode  of  capture.  We  need  not  take  consideration  of  the  former 
here.  They  are  nearly  all  plants  with  septate  hyphae  producing 
conidia  of  various  forms,  and  in  some  cases  the  sexual  method  of 
reproduction  is  known.  The  method  of  capture  is  quite  similar  in 
all  cases.  The  species  of  Amoeba  appear  to  be  large.  Amoeba  ter- 
ricola  or  related  species  being  often  the  victim.  There  is  evidence 
that  certain  fungi  can  attack  only  one  kind  of  Amoeba  and  not  an- 
other. In  some  fungi  an  adhesive  has  been  observed,  in  others  not, 
leaving  it  for  conjecture  that  a  non-visible  adhesive  occurs.  There 
is  seldom  any  preformed  structure  with  the  function  of  capture,  but 
this  occurs  in  Dactylella  tylopaga  Drechsler.  In  this  "prolate  el- 
hpsoidal  protuberances"  are  provided  with  an  adhesive.  An  animal 
sticks  to  one  of  these,  which  then  sends  out  a  tube  of  penetration. 
This  grows  inside  the  animal  into  a  branching  mass  of  short  h>^hae 
which  absorb  the  body  of  the  animal. 

Pedilospora  dactylopaga  captures  shelled  Rhizopods  (Drechsler 
1934).  Eight  species  of  Acaulopage  have  been  described  by  Drechs- 
ler, all  of  which  capture  Amoebae  in  much  the  same  way  as  Dac- 
tylella tylopaga  except  that  there  is  no  special  organ  involved  in  capture. 
"An  Amoeba  after  capture  is  always  to  be  seen  attached  whether 
to  a  mycelial  element  or  as  is  often  the  case  in  some  species,  to  a 


Francis  E.  Lloyd  —  174  —  Carnivorous  Plants 

fallen  conidium  by  means  of  a  minute  mass  of  golden  yellow  adhesive 
material."     "From   the   mycehal   element  or  the   conidium   is   thrust 
forth  a  narrow  process  which  passes  through  the  deposit  of  adhesive 
material  and  perforates  the  animal's  pellicle  to  give  rise  inside  to  a 
more    or    less    characteristically    branched    haustorium    or    haustorial 
system.     When  the  protoplasmic  contents  of  the  Amoeba  are  nearly 
exhausted,    the    protoplasm    of    the    haustorium    begins    to    withdraw 
back  into  the  parent  mycelial  filament.     Eventually  the  haustorium 
is    completely   evacuated    and    thereupon,    like    the    collapsed   pellicle 
surrounding  it,  becomes  altogether  invisible;    so  that  an  instance  of 
capture  is  afterwards  found  recorded,   and  then  usually  only  rather 
dubiously,  in  an  inconspicuous  scar-hke  or  shghtly  protuberant  modi- 
fication of  the  contour  of  the  hypha  or  conidium"   (Text  fig.  4c), 
(Drechsler  1935&,  p.   183).     In  the  case    of    another   fungus,  Endo- 
cochlus  asteroides  Drechsler,  the  animal  is  attacked  by  conidia  picked  up 
in  its  wanderings.     Sticking  to  the  surface  of  the  pelhcle,  they  form  a 
small  bulbous  body,  serving  apparently  as  an  appressorium,  through 
which  a  slender  tube  punctures  the  pellicle  and  enters  the  animal,  pass- 
ing in  to  some  distance.    There  the  end  swells  up,  taking  in  the  proto- 
plasm of  the  conidium,  which  becomes  detached  and  is  usually  thrown 
off   by   the   animal.      Sometimes   the    conidium   is  ingested,  however. 
Owing  to  the  fact  that  the  animal  may  be  infected  a  number  of  times, 
because  of  the  numbers  of  fallen  spores,  it  may  have  a  corresponding 
number  of  bulbous  bodies,  each  derived  from  a  conidium.     After  the 
conidium  with  its  germ  tube  is  loosened  and  cast  off,  the  remaining 
globular  thallus  becomes  considerably  enlarged  and  turgid.    As  it  length- 
ens it  curves  and  with  elongation  becomes  a  helicoidal  mass.     In  the 
meantime,  the  animal  remains  alive  and  active,  so  that  we  are  con- 
templating here  a  case  of  parasitism.     The  briskness  of  action  per- 
sists for  some  time,  until  the  bulk  of  the  animal  becomes  reduced, 
and  it  finally  succumbs.     The  inclosed  fungus  then  sends  out  slender 
hyphae   which   penetrate    the   pellicle    to    the   exterior,    where    spores 
and   sexual   apparatus  are  produced,   to  produce   new  hyphae   which 
begin  the  cycle  again.     The  same  story  is  presented  by  Cochlonema 
verrucosum  Drechsler,   and  in    C.    dolichosporum,    but    in    these  it^  is 
started  by  conidia  which  are  first  ingested  by  the  animal,  one  having 
the  same  dimensions  as  Amoeba  sphaeronucleus.     In  Bdellospora  heli- 
coides  Drechsler  the  infection  takes  place  as  in  Endocochlus  asteroides. 
In  Zoopage  phanera  Drechsler   the   manner   of    capture    is    a   matter 
of   inference    rather   than   direct   observation.     The    animal    captured 
is  an  Amoeba  from  35-110  micra  in  diameter.     An  adhesive  is  in- 
dicated,  though   Drechsler   suggests   that   the   small   botryoidal   or- 
gans seen  in  a  captured  animal  could  be  taken  for  grappling  organs. 
At  all  events  they  are  very  distinctive  in  form  as  his  figure    shows. 
In  the  forms  above   described  it  is  evident  that  we   are   dealing 
with    organisms    that    stand    between    plants    which    have    elaborated 
organs  designed  —  if  we  may  use   the  word  —  for  first  trapping  an 
animal  before  disposing  of  it,  and  those  which  infect  an  animal  by  a 
process  which  must  be  repeated  in  a  very  many  cases,  as  for  instance 
that  of  Cordyceps  and  related  plants  already  mentioned.     Carnivorous 
the  latter  are,  but  they  can  hardly  be  regarded  as  "trapping"  plants. 


Chapter  XI  —  175  — Carnivorous  Fungi 

The  significance  of  carnivory  for  Zoophagus  (and  hence  by  implica- 
tion for  fungi  in  general)  has  been  indicated  experimentally  by  Gickl- 
HORN  (1922).  By  culturing  it  for  two  months  in  properly  prepared 
water,  free  of  animals,  he  found  that  it  could  persist  saprophytically, 
as  many  other  fungi  do.  Under  these  conditions,  however,  it  became  a 
"hunger  form",  with  the  "long  hyphae",  though  normal  as  to  branch- 
ing, weakly  developed,  and  with  depreciated  cellular  contents.  In  two 
days  after  the  addition  of  Rotatoria,  the  hyphae  became  appreciably 
stronger  and  were  well  filled  with  contents,  "After  such  evidence  one 
can  hardly  avoid  the  thought  that  the  capture  of  animals  by  Zoophagus 
supplied  an  important  source  of  nutrition  and  that  we  have  before  us  a 
highly  specialized  adaptation"  {I.e.  p.  217). 


Literature  Cited: 

Arnaudow,   N.,   Zur   Morphologic  und   Biologie   von   Zoophagus  insidians  Soramerstorff. 

Jahrb.  d.  Univ.  Sofia  15-16:1-32,  igiS-Cigai)  (Bulgarian  with  German  summary). 
Mnaudow,  N.,  Ein  neuer  Radertiere  (Rotatoria)  fangender  Pilz  (Sommerslorffia  spinosa 

nov.  gen.,  nov.  sp.).     Flora  116:109-113,  1923. 
Arnaudow,  N.,  Untersuchungen  iiber  Sommerstorffia  spinosa  nov.  gen.,  nov.  spec.    Jahrb. 

d.  Univ.  Sofia  Bd.  19,  H.  2,  Abt.  la,  1923. 
Arnaudow,  N.,  Untersuchung  iiber  den  Tiere  fangenden  Pilz  Zoophagus  insidians  Som. 

Flora  118-119:1-16,  1925. 
BuDDE,  E.,  tjber  die  in  Radertieren  lebenden  Parasiten.     Arch.  f.  Hydrob.  18:442-459. 
Couch,  J.  N.,  The  formation  and  operation  of  the  traps  in  the  nematode-catching  fungus, 

Dactvlella  bembicoides  Drechsler.    Jour.  Elisha  Mitchell  Sci.  Soc.  53:301-309,  ^937- 
Drechsler,   C,   Morphological  features  of  some  fungi  capturing  and  killing   Amoebae. 

J.  Wash.  Acad.  Sci.  23:200-202,  1933a. 
Drechsler,  C,  Morphological  diversity  among  fungi  capturing  and  destroying  nematodes. 

J.  Wash.  Acad.  Sci.  23(3):i38-i4i,  19336. 
Drechsler,  C,  Morphological  features  of  some  more  fungi  that  capture  and  kill  nema- 
todes.   J.  Wash.  Acad.  Sci.  23(5):267-27o,  1933c. 
Drechsler,  C,  Several  more  fungi  that  prey  on  nematodes.     J.   Wash.   Acad.  Sci.  23(7): 

355-357,  igssd. 
Drechsler,  C,  Organs  of  capture  in  some  fungi  preying  on  nematodes.     Mycol.  26:135- 

144,  1934a. 

Drechsler,  C,  Pedilospora  dactylopaga  n.  sp.,  a  fungus  capturing  and  consuming  testa- 
ceous rhizopods.     J.  Wash.  Acad.  Sci.  24:395-402,  19346- 

Drechsler,  C,  Some  conidial  Phycomycetes  destructive  to  terricolous  Amoebae.  Mycol. 
27:6-40,  1935a. 

Drechsler,  C,  Some  non-catenulate  conidial  Phycomycetes  preying  on  terricolous  Amoe- 
bae.    Mycol.  27:176-205,  19356. 

Drechsler,  C,  A  new  species  of  conidial  Phycomycete  preying  on  nematodes.  Mycol. 
27:206-215,  1935c.  ... 

Drechsler,  C,  A  new  Mucedinaceous  fungus  capturing  and  consuming  Amoeba  verrucosa. 
Mycol.  27:216-223,  i93S<f. 

Drechsler,  C,  A  new  species  of  Stylopage  preying  on  nematodes.  Mycol.  28:241-246, 
1936a. 

Drechsler,  C,  New  conidial  Phycomycetes  destructive  to  terricolous  Amoebae.    Mycol. 

28:363-389,  19366.  .  ^       ,  „  .  .  •      .    . 

Drechsler,  C,  A  Fusarium-like  species  of  Dactylella  capturing  and  consuming  testaceous 
rhizopods.     J.  Wash.  Acad.  Sci.  26:397-404,  1936c. 

Drechsler,  C,  New  Zoopagaceae  destructive  to  soil  rhizopods.     Mycol.  29:229-249,  1937a. 

Drechsler,  C,  Some  Hyphomycetes  that  prey  on  free-living  terricolous  nematodes.  My- 
col. 29:447-552,  19376.  _  .,    A        u         n*       1     • 

Drechsler,  C,  New  Zoopagaceae  capturing  and  consuming  soil  Amoebae.  Mycologia 
30:2:137-157,  1938. 

Drechsler,  C,  A  few  new  Zoopagaceae  destructive  to  large  soil  rhizopods.     Mycologia 

31:2:128-153,  1939. 

Drechsler,  C,  Five  new  Zoopagaceae  destructive  to  Rhizopods  and  Nematodes.  My- 
cologia 31 :4:388-4i5>  i939-  „      ,         r  /rj    -7       \ 

Fresenius,  Beitrage  zur  Mycologie.     Frankfurt,  1850-63,  p.  18,  pi.  3,  fags.  1-7  {fide  f^ovY). 

Geitler,  L.,  iiber  einen  Pilzparasiten  auf  Ajnoeba  proleus  und  uber  die  polare  Organisation 
des  Amoebenkorpers.     Biol.  Zentralbl.  57:166-175,  1939. 


Francis  E.  Lloyd  —176— Carnivorous  Plants 

GiCKLHORN,  J.,  Studien  an  Zoophagiis  insidians  Som.,  einem  Tiere  fangenden  Pilz.    "Glas- 

nik"  Kroat.  Nat.  Ges.  34(2):i99-288,  1922. 
GiCKLHORN,  J.,  Aphanomyces  ovidestruens  nov.  spec,  ein  Parasit  m  den  Eiern  von  Diap- 

tomus.    Lotos  71:143-156,  1923.  ,     ,     .    T^      .        ,       . 

KoNSULOFF,  St.,  Untersuchungen  liber  Rotatonenparasiten.    Arch.  f.  Protistenk.  30:353- 

MiRANDE,  R.,  Zoophagiis  insidians  Sonunerstorff,  capteur  de  Rotiferes  vivants.     Bull.  Soc. 

Myc.  Fr.  36:47-53,  1920. 
Rennerfelt,  E.,  Untersuchungen  iiber  die  Entwicklung  und  Biologic  des  Krebspestpilzes, 

Aphanomyces  astaci  Schikora.    Mitt.  Anst.  f.  Binnenfischerei  bei  Drottninghobn,  Stock- 

hohn.  No.  10,  21  pp.,  1936.  _         ,      ^     .„    .  j    •  • 

Scherffel,  a.,  Endophytische  Phycomyceten-Parasiten  der  Bacillanaceen  und  emige  neue 

Monadinen.     Archiv  Protistenk.  52:1-141,  1925.  _ 

Schikora,  F.,  Uber  die  Krebspest  und  ihren  Erreger,  Aphanomyces  Magnusi  Schikora. 

Verhandl.  Bot.  Verein  Prov.  Brandenburg  63:87-88,  1922. 
SOMMERSTORFF,  H.,  Ein  Ticrc  fangender  Pilz  {Zoophagiis  insidians  nov.  gen.,  nov.  sp.). 

Oest.  Bot.  Zeitschr.  61:361-373,  191 1. 
Sparrow,  F.  K.,  Jr.,  A  note  on  the  occurrence  of  two  rotifer-capturing  Phycomycetes. 

Mycol.  2i(2):90-96,  1929.  ,    ,  „      ,       t.-.  a     i.- 

Valkanov,  a.,  Uber  Morphologie  und  Systematik  der  rotatorienbefallenden  Pilze.    Archiv 

Protist.  74(0:5-17,  1931.  .      ,    ,  ,,     J      ^ 

Valkanov,  A.,  tjber  die  Morphologie  und  Systematik  der  Rotatonen  befallenden  Uomy- 

ceten  (bulgarisch).    Jahrb.  Univ.  Sofia,  27,  1931.  .     r-     -n      • 

Valkanov,  A.,  Nachtrag  zu  meiner  Arbeit  uber  rotatorienbefallende  Pilze.    Archiv  Protist. 

78(2)  :485-496,  1932. 
ZoPF,  W.,  Zur  Kenntniss  der  Infectionskrankheiten  niederer  Thieren  und  Pllanzen.    Nova 

Acta  d.  Leop.-Carol.  Akad.  d.  Naturf.  52:315-375.  1888. 


Chapter  XII 

DIONAEA    MUSCIPULA    AND    ALDROVANDA 

VESICULOSA 

Dionaea:  general  description.  —  Early  discovery.  —  Original  description  by  Ellis.  — 
Work  of  Curtis  (1834),  Oudemans  (1859),  Caxby  (1868),  Darwin,  Goebel.  —  Mor- 
phology (Seed  and  seedling.  Structure  of  mature  leaf:  trap.  Lobes,  glands,  sensitive  hairs. 
Internal  structure).  —  Physiology.  —  Aldrovanda:  general  description.  —  Discovery,  dis- 
tribution.—  Morphology  (Seed.  Germination.  Mature  leaf.  Posture  of  the  trap). — 
Physiology. 

These  two  monotypic  genera  are  members  of  the  family  Droser- 
aceae,  and  while  the  former,  Dionaea,  is  well  known,  it  being  widely 
grown  in  greenhouses,  Aldrovanda  is  well  known  chiefly  to  such  bot- 
anists as  have  a  special  interest  in  these  curious  plants.  Dionaea 
has  a  very  restricted  geographical  range,  Aldrovanda  a  very  wide 
one.  Though  the  method  of  trapping  animals  is  identical,  the  one 
is  a  land  plant,  and  Aldrovanda  a  submersed  water  plant.  We  con- 
sider these  separately. 

Dionaea  muscipula  Ellis,  Venus'  fly  trap:  —  This  is  a  small 
plant  (77 — 2),  consisting  of  a  rosette  of  leaves  three  to  six  inches 
across  arising  from  a  rootstock  growing  more  or  less  horizontally. 
The  rootstock  is  apparent  even  in  the  young  seedling  (Smith  193 i). 
Long  scapes  are  sent  up  bearing  several  flowers  in  a  short  cyme  with 
two  to  fourteen  flowers.  These  are  of  pentamerous  structure,  five 
small  elliptical  sepals  alternate  with  five  white  cuneate  and  somewhat 
oblique  petals,  usually  fifteen  stamens.  The  leaf  consists  of  two  re- 
gions, a  basal  "footstalk"  as  Darwin  called  it,  articulated  by  means 
of  a  short  cylindrical  portion  (midrib)  with  the  blade  which  is  a  trap. 
The  footstalk  is  a  more  or  less  expanded  leaf-like  structure,  either 
broadly  obcordate  to  narrowly  obcordate  in  form,  depending  on  ex- 
posure to  fight  and  the  presence  of  surrounding  vegetation.  The 
upper  part  of  the  leaf,  a  "striking  and  noteworthy"  trap,  to  quote 
Goebel,  consists  of  two  dished  lobes  of  trapezoidal  form.  The  outer 
margins  are  "ciliated,"  that  is,  are  provided  with  a  row  of  coarse 
projections,  prongs  or  teeth.  Ellis  (1770)  spoke  of  the  arrange- 
ment as  "a  miniature  form  of  a  rat-trap,"  and  Curtis  (1834)  com- 
pared it  to  "two  upper  eyefids  joined  at  their  bases."  Springing 
from  the  upper  surface  of  the  two  lobes  there  are  six  slender,  sensi- 
tive hairs,  three  on  each  side  placed  in  triangular  position  (in  ex- 
ceptional cases  a  smaller  or  larger  number  has  been  noted  {iS — i). 
The  rest  of  the  surface  is  covered  rather  densely  with  two  kinds  of 
sessile  glands,  most  of  which  under  usual  circumstances  are  colored 
with  brilliant  red  pigment,  giving  a  bright  red  tinge  to  the  surface. 
When  with  suitable  temperatures  the  sensitive  hairs  are  moved,  the 
two  lobes  swing  swiftly  on  their  common  axis,  and  the  finger-like 
cilia  intercross  to  form  a  barred  cage.  Darwin  interpreted  this  ini- 
tial posture  as  an  arrangement  to  allow  small  insects,  relatively  value- 


I'-. 


Francis  E.  Lloyd  —  178  —  Carnivorous  Plants 

less  on  account  of  their  size,  to  escape  before  final  closure,  a  view 
for  which  F.  M.  Jones  has  adduced  constructive  evidence.  Subse- 
quent movement  progressing  during  >^-i2±  hours  approximates  the 
lobes  more  closely  and  even  causes  them  to  become  flatter,  bringing 
the  inner  surfaces  into  closer  apposition. 

If  by  this  reaction  an  insect,  the  normal  agent  of  stimulation, 
has  been  caught,  the  body  may  be  more  or  less  compressed  between 
the  lobes  (17  —  3).  The  glands  then  secrete  a  digestive  fluid  and 
in  a  few  days  the  insect  body  disintegrates  and  the  products  are 
absorbed.  In  the  course  of  ten  days  the  lobes  open  again,  and  are 
ready  to  catch  other  prey.  This  may  be  repeated  two  or  three  times 
before  the  leaf  reaches  its  complete  maturity,  when  it  dies.  Of  this 
arrangement  Curtis  (1834)  remarked,  "if  it  were  a  problem  to  con- 
struct a  plant  with  reference  to  entrapping  insects,  I  cannot  con- 
ceive of  a  form  and  organization  better  adapted  to  secure  that  end 
than  are  found  in  Dionaea  muscipula." 

"  This  plant,  which  Linnaeus  called  miraculum  naturae,  appears 
to  have  first  been  discovered  by  Arthur  Dobbs,  Governor  of  North 
Carohna,  and  he  sent  the  following  account  of  it  to  Mr.  Collinson 
in  a  letter  dated  at  Brunswick,  Jan.  24,  1760.  After  describing  the 
Schrankia,  he  proceeds:—  'But  the  great  wonder  of  the  vegetable 
kingdom  is  a  very  curious  unknown  species  of  sensitive;  it  is  a  dwarf 
plant;  the  leaves  are  like  a  narrow  segment  of  a  sphere,  consisting 
of  two  parts,  like  the  cap  of  a  spring  purse,  the  concave  part  out- 
ward, each  of  which  falls  back  with  indented  edges  (like  an  iron 
spring  fox  trap);  upon  anything  touching  the  leaves,  or  falHng  be- 
tween them,  they  instantly  close  like  a  spring  trap,  and  confine  any 
insect  or  anything  that  falls  between  them;  it  bears  a  white  flower; 
to  this  surprising  plant  I  have  given  the  name  of  Fly  Trap  Sensitive.' 
Mr.  Collinson,  in  a  memorandum,  has  recorded  the  death  of  Gov- 
ernor Dobbs  in  1765"   (Dillwyn  1843). 

It  may  be  inferred  from  the  note  by  Governor  Dobbs,   written 

in  1760,  but  which  did  not  gain  publicity  till  the  appearance  of  the 

Hortus  Collinsonianus  in   1843,  that  the  Dionaea  was  well  known  in 

North  Carolina  when,  in  1763,  a  Mr.  Young,  "the  Queen's  botanist," 

had  his  attention  drawn  by  some  friends  to  a  "pecuhar  plant"  which 

he   subsequently   found   in   great   abundance   in   North    Carohna   and 

in  some  parts  of  South  Carohna.     Still  later  Young  brought  hving 

plants  to  England,  he  also  introduced  them  in   Kew   (Sims  1S04)  and 

from    these    Ellis,    a    London    merchant,    drew    his    description    and 

figure  sent  by  him  to  Linnaeus  in  1770  (Young  1783).     These  were 

published    in    a   small    volume    entitled.    Directions  for   Bringing   over 

Seeds  and  Plants  from  the  East  Indies  and  other  Distant  Countries  in  a 

State   of   Vegetation,    in    1770.      Ellis'    description    was   pubHshed    in 

Latin   at   a   subsequent   date   in   Nova  Acta  Soc.    Scient.    Upsaliensis 

1:98,  1773.     Though  Ellis'  description  was  based  on  living  material, 

he  had  just  previously  received  from  John  Bartram  of  Philadelphia, 

through  Mr.  Peter  Collinson,  an  herbarium  specimen  which  furnished 

material  which  enabled  Dr.  Solander  and  himself  to  determine  that 

they  had  before  them  a  new  genus  allied  to  Drosera  (Ellis  1770).    But 

Ellis,  who  from  the  dried  material  got  no  hint  of  the  motility  of  the 


Chapter  XII  — 179  —  Dionaea  and  Aldrovanda 

leaves,  did  so  when  he  examined  the  material  brought  to  England  by 
Young,  and  he  was  the  first  to  publish  a  definite  statement  of  the 
carnivorous  habits  of  the  plant.  It  is  this,  expressed  in  the  letter  to 
Linnaeus,  which  interests  us  here.  Having  recalled  that  Mimosa  is 
irritable,  but  shortly  recovers  from  its  position  of  response,  Ellis 
continues : 

''But  the  plant,  of  which  I  now  inclose  you  an  exact  figure,  with 
a  specimen  of  its  leaves  and  blossoms,  shews,  that  nature  may  have 
some  view  towards  nourishtnent,  in  forming  the  upper  joint  of  the 
leaf  like  a  machine  to  catch  food:  upon  the  middle  of  this  lies  the 
bait  for  the  unhappy  insect  that  becomes  its  prey.  Many  minute 
red  glands,  that  cover  its  inner  surface,  and  which  perhaps  discharge 
sweet  liquor,  tempt  the  poor  animal  to  taste  them;  and  the  instant 
these  tender  parts  are  irritated  by  its  feet,  the  two  lobes  rise  up, 
grasp  it  fast,  lock  the  rows  of  spines  together,  and  squeeze  it  to  death. 
And,  further,  lest  the  strong  efforts  for  life,  in  the  creature  thus  taken, 
should  serve  to  disengage  it,  three  small  erect  spines  are  fixed  near 
the  middle  of  each  lobe,  among  the  glands,  that  effectually  put  an 
end  to  all  its  struggles.  Nor  do  the  lobes  ever  open  again,  while 
the  dead  animal  continues  there.  But  it  is  nevertheless  certain  that 
the  plant  cannot  distinguish  an  animal,  from  a  vegetable  or  min- 
eral, substance;  for  if  we  introduce  a  straw  or  a  pin  between  the 
lobes,  it  will  grasp  it  full  as  fast  as  if  it  were  an  insect." 

The  above  paragraph,  quoted  also  by  Hooker  in  1875,  was  taken 
from  the  original,  a  copy  of  which  is  to  be  found  in  the  Library  of 
Congress,  Washington.  It  shows  us  clearly  what  Ellis  thought 
about  the  plant.  Linnaeus,  to  whom  was  sent  the  letter  contain- 
ing the  above  quotation,  did  not,  however,  fully  respond  to  Ellis' 
evident  enthusiasm,  and  merely  regarded  the  movement  as  a  special 
case  of  irritability  like  that  in  Mimosa,  and  believed  that  on  reopen- 
ing the  captured  insect  was  released  {Mantissa  plantaruni  altera, 
Holmiae  1771);  nor  did  he  see  eye  to  eye  with  Ellis  about  the  func- 
tion of  the  "three  small  erect  spines"  whether  from  sagacity,  as 
Hooker  suggests  (1875),  or  as  part  of  his  general  non-responsiveness 
to  Ellis'  interpretations,  it  is  hard  to  say.  It  happens,  of  course, 
that  Ellis  was  wrong;  the  idea  was  even  fantastic.  No  less  was 
that  of  Erasmus  Darwin  who  wrote:  "In  the  Dionaea  muscipula 
there  is  a  still  more  wonderful  contrivance  to  prevent  the  depreda- 
tions of  insects:  the  leaves  are  armed  with  long  teeth,  like  the  an- 
tennae of  insects,  and  lie  spread  upon  the  ground  around  the  stem, 
and  are  so  irritable,  that  when  an  insect  creeps  upon  them  they  fold  up 
and  crush  or  pierce  it  to  death."    {The  Botanic  Garden  2 :  canto  I,  p.  39). 

E.  MoRREN  (1875)  in  a  footnote  calls  attention  to  a  description 
by  the  French  encyclopaedist  Denis  Diderot  (1713-1784)  of  "Plante 
de  la  Caroline  appellee  Muscipula  Dionaea",  of  which  he  says,  at 
the  close  of  his  description  "Voila  une  plante  presque  carnivore". 
The  essay  from  which  this  is  quoted  is  said  to  be  dated  1 774-1 780, 
not  1762  as  M.  Catalan  told  Dr.  Morren.  It  is  of  interest  to 
record  Diderot's  speculation  "Je  ne  me  doute  point  que  la  Muscipula 
ne  donnat  a  I'analyse  de  I'alcali  volatil,  produit  caracteristique  du 
regne  animal." 


Francis  E.  Lloyd  —  180  —  Carnivorous  Plants 

In  1834  M.  A.  Curtis  (quoted  on  p.  177),  a  minister  resident  in  Wil- 
mington, N.  C,  published  his  observations,  which  led  him  to  think 
that  the  sensitiveness  resides  only  in  the  hair-like  processes,  and 
that  other  parts  of  the  leaf  may  be  touched  or  pressed  without  any 
response.  This  is  not  quite  true,  as  has  later  been  found.  Further, 
that  insects  captured  are  not  always  crushed  on  being  caught,  for 
if  the  trap  were  opened  again  they  might  escape;  but  that  in  time 
they  were  surrounded  by  a  mucilaginous  fluid  by  which  the  insects 
were  more  or  less  consumed.  The  fact  that  a  special  sensitivity 
resides  in  the  six  slender  hairs  of  the  upper  surface  of  the  trap  had 
been  noted  by  a  botanical  draughtsman,  Sydenham  Edwards,  em- 
ployed by  Dr.  John  Sims  in  illustrating  Curtis's  Botanical  Magazine. 
This  observation  was  recorded  by  Sims  (1804)  in  the  description  of  plate 
785  of  vol.  20  which  reads:  "These  small  spines  are  mentioned  and 
figured  by  Ellis  and  supposed  by  him  to  assist  in  destroying  the  en- 
trapped animal;  but  that  they  are  only  irritable  points,  and  that  any 
other  part  of  the  leaf  may  be  touched  with  impunity,  was  discovered 
by  our  draughtsman,  Mr.  Edwards,  several  years  ago,  when  taking  a 
sketch  of  a  plant  flowering  at  Mr.  Lipman's,  Mile  End,  and  has  since 
been  repeatedly  confirmed.  The  same  observation  was  made,  without 
knowing  it  had  previously  been  noticed,  by  our  friend  Mr.  Charles 
Konig"  (Hooker  1875). 

In  1859  OuDEMANS,  a  Dutch  botanist,  rediscovered  the  sensi- 
tivity of  the  trigger  hairs,  and  did  a  number  of  experiments  which 
afforded  results  which  anticipated  some  of  Darwin's.  He  found 
that  there  is  no  periodic  closure  of  the  trap,  as  Meyen  has  claimed, 
and  that  traps,  after  closure,  opened  again  during  the  night.  Meyen 
had  said  that  the  closure  was  too  slow  to  catch  insects,  to  which 
Oudemans  answered  that  at  sufficiently  high  temperatures  it  is  rapid, 
which  we  now  know  to  be  true.  He  recorded  that  the  trap  does 
not  open  after  catching  prey  until  several  days  after  its  death.  When 
the  trap  does,  the  prey  is  found  lying  in  a  slimy  liquid;  and  further 
that  the  trap  does  not  remain  closed  over  inanimate  objects  such  as 
paper,  reopening  in  36  hours  or  less.  Though  he  thought  that  the 
stimulus  was  transmitted  to  the  mid-vein,  he  attributed  closure  to 
alterations  of  strain  in  the  parenchyma. 

In  1868  Canby  thought  it  might  be  that  the  fluids  collecting 
in  the  closed  trap  might  escape  and,  flowing  down  the  petioles  of 
the  leaves,  might  enrich  the  soil  at  the  base  of  the  plant.  Experi- 
ments showed  him,  however,  that  this  is  not  the  case,  but  that,  on 
feeding  the  leaf,  the  insect  is  entirely  destroyed  and  absorbed,  thus 
confirming  Curtis,  thirty-four  years  his  predecessor.  He  concluded 
by  saying,  "so  that,  in  fine,  the  fluid  (secreted  by  the  leaves)  may 
well  be  said  to  be  analogous  to  the  gastric  juice  of  animals,^  dissolv- 
ing the  prey  and  rendering  it  fit  for  absorption  by  the  leaf." 

That,  however,  the  sensitive  hairs  are  the  only  sensitive  spots 
in  the  leaf  was  shown  by  Darwin  and  by  Goebel  (1891)  not  to  be 
true.  "It  is  sufiicient  to  rub  the  upper  or  lower  surface,  and  not 
too  strongly,  with  a  solid  object  to  procure  immediate  closure  of  the 
two  halves  of  the  trap"  (Goebel).  This,  as  will  be  seen,  has  later 
been  confirmed. 


Chapter  XII  — 181  —  Dionaea  and  Aldrovanda 

We  now  direct  our  attention  to  certain  of  the  more  intimate  de- 
tails of  the  life  history  and  structure  of  the  plant. 

The  seed  and  seedling  (Smith  i 931).  — The  seed  is  a  small  pear- 
shaped  mass  with  a  lid  at  the  micropylar  end.  The  embryo,  also 
pear-shaped,  Hes  with  its  two  broad  cotyledons  in  contact  with  an 
abundant  endosperm.  The  cotyledon-ends  remain  in  contact  with 
the  endosperm  for  an  extended  period,  while  their  bodies  enlarge, 
become  green,  and  eventually  spread  apart,  becoming  elongate  in 
form.  Meanwhile  the  primary  root  has  developed,  bears  a  niass  of 
root  hairs,  but  does  not  persist.  From  the  plumule  there  arises  at 
once  a  rhizome  bearing  small  leaves  which  are  similar  to  the  mature 
leaves  in  all  points,  except  that  they  are  small  (Goebel  1891,  Holm 
1891),  the  shape  of  the  trap  is  more  rectangular,  and  the  glands 
are  fewer  in  number.  This  story,  as  we  shall  see,  is  similar  to  that 
of  Aldrovanda. 

Although,  as  Miss  Smith  says,  the  juvenile  leaves  (those  of  seed- 
lings) are  similar  to  those  of  mature  plants,  there  are  differences 
worthy  of  note,  among  which  are  the  following:  Traps  2  nrni.  long 
have  poorly  developed  marginal  spines  of  rather  irregular  form  and 
little  rigidity,  and  may  arise  symmetrically,  so  that  those  of  the 
opposing  lobes  face  each  other  (/5  — 8);  or  there  may  be  a  conspic- 
uous lack  of  symmetry  and  a  disparity  of  number  (18  on  one  side 
and  13  on  the  other),  some  teeth  displaying  branching  to  some  ex- 
tent {i8~g).  Traps  of  larger  size  (4  mm.  along  the  midrib  and  7 
mm.  along  the  free  margins)  have  well  developed  spines  with  pos- 
ture and  rigidity  comparable  to  traps  on  mature  leaves.  The  number 
of  glands  in  juvenile  leaves  is  much  smaller,  while  the  size  of  the 
glands  approaches  that  of  maturity.  They  are  rather  widely  scattered. 
I  counted  about  70  in  the  2  mm.  trap  {i8~()).  There  is  a  wide 
zone  between  the  outer  limit  of  this  glandular  region  and  the  lobe 
margin;  and  in  the  outer  zone  of  allure,  a  narrow  zone  just  within 
the  margin,  the  nectar  (?)  glands  are  only  2  to  12  in  number,  con- 
fined to  the  outer  angles  of  the  lobes  in  the  2  mm.  traps  examined; 
while  as  many  as  50  were  found  in  the  4  mm.  trap.  As  would  be 
expected,  the  structure  of  the  lobes  is  of  much  greater  delicacy  as 
compared  with  that  of  mature  leaves.  In  the  2  mm.  trap  the  lobe 
was  found  0.5  mm.  thick  at  the  level  of  an  inner  sensitive  hair  {18  — 
17,  18).  The  inner  (upper)  epidermis  cells  were  somewhat  larger  than 
those  of  the  outer  in  the  ratio  of  1.4  to  i,  and  had  somewhat  thicker 
outer  walls.  The  number  of  parenchyma  cells  between  ranged  from 
two  to  four  courses  with  large  interspaces,  in  this  feature  again  re- 
sembling the  mature  leaves  of  Aldrovanda  much  more  than  do 
the  thicker  mature  leaves  of  Dionaea.  It  is  easier,  thus,  to  see  the 
parallelism  of  action  in  these  two  plants,  to  which  reference  is 
made  beyond.  The  sensitive  hairs  are  much  smaller  and  simpler 
in  construction  {18 —t,)-  They  are  about  0.6  mm.  long,  the  outer 
stiff  "lever"  being  somewhat  more  than  half  that.  The  basal  por- 
tion is  deeply  constricted,  and  the  bending  cells  are  relatively  large 
and  impinge  on  each  other  in  the  middle  of  the  hair,  there  being 
no  medullary  cells.  These  latter  seem,  therefore,  of  no  importance 
beyond  that  of  a  filler  in  the  large,  sensitive  hairs  of  the  mature  leaf. 


Francis  E.  Lloyd  —  182  —  Carnivorous  Plants 

In  young  plants  derived  from  leaf  cuttings  (seen  growing  in  Mu- 
nich) the  lobes  of  the  traps  were  usually  quite  oblique  in  form,  and 
the  cilia  were  very  irregular  and  often  very  small.  Both  kinds  of 
glands  were  present  in  small  numbers.  I  counted  six  alluring  glands 
clustered  near  each  of  the  outer  angles  of  the  lobe  in  one,  and  three 
in  another  trap.  The  digestive  glands  were  more  numerous,  but  still 
few  and  scattered.  The  sensitive  hairs  were  absent  in  one  case,  and 
from  one  to  two  occurred  in  several  others.  While  small,  they  showed 
all  the  normal  histological  details. 

During  development  the  blade  and  trap  both  display  circination. 
In  the  latter  the  two  lobes  are  rolled  inwardly  and  gradually  un- 
fold, the  cilia  being  the  last  to  unroll.  The  blade  lobes  are  inrolled 
longitudinally  at  first,  but  as  it  develops  the  axis  of  the  roll  grad- 
ually comes  to  lie  more  transversely,  the  last  portion  of  the  blade 
to  unroll  being  the  apex.  At  first  also  the  trap  is  bent  sharply  back 
on  the  blade,  but  lying  asymmetrically  on  its  right  lobe,  which  presses 
against  the  blade  surface.  With  further  growth  the  trap  swings 
forward  on  its  stalk,  and  now  comes  to  lie  more  or  less  on  its  left 
lobe,  or  otherwise  expressed,  the  trap  is  twisted  more  or  less  to  the 
left  (as  seen  from  above)  (iS  —  7).  This  posture  is  more  evident 
in  small  plants,  with  small  traps,  than  in  plants  large  enough  to 
produce  normal  sized  traps.  It  is,  however,  often  quite  evident  in 
the  latter,  as  I  have  myself  observed  in  plants  growing  under  my 
eye.  In  the  account  beyond  of  Aldrovanda,  it  will  be  seen  that  in 
this  plant  the  trap  always  lies  on  its  left  side,  a  position  which  offers 
distinct  advantages  in  the  trapping  of  prey.  Much  less  marked,  how- 
ever, is  the  posture  just  mentioned  for  Dionaea,  and  it  cannot  be 
said  to  be  of  any  significance.  I  have  never  seen  the  trap  bending 
to  the  right  (as  seen  from  above). 

Structure  of  the  mature  leaf.  —  The  structure  of  the  leaf  has  often 
been  the  subject  of  examination  (Oudemans,  1859;  Daewin,  1875; 
Kurtz,  1876;  de  Candolle,  1876;  Fraustadt,  1877;  Goebel,  1891; 
Haberlandt,  1901;  GuTTENBERG,  1925).  The  winged  form  of  the 
petiolar  region  traversed  by  a  single  vascular  bundle,  which  presents 
nothing  further  of  special  interest,  is  regarded  by  Goebel  as  a  physio- 
logical compensation  in  the  interest  of  photosynthesis,  such  compen- 
sations being  generally  found  among  the  carnivorous  plants.  In 
seedlings  the  petiole  is  relatively  much  larger. 

The  outer  part  of  the  leaf,  the  blade,  is  the  trap.  This  consists 
of  two  lobes,  trapezoidal  in  form,  united  along  the  middle  line  by  a 
thick  midrib,  which  has  often  been  considered  a  hinge,  but  which 
has  no  hinge  function  {i8 — i).  At  their  bases  the  lobes  have  their 
greatest  thickness,  thinning  off  gradually  as  the  margins  are  approached 
{18  —  4b).  Here,  however,  they  are  thickened  locally  by  the  enlarged 
bases  of  the  marginal  cilia.  These  are  prominent,  tapering,  finger-like 
processes,  evidently  emergencies  (Solereder),  which  are  so  placed 
that  when  the  lobes  are  approximated  they  interweave  like  the  fingers 
of  closed  hands.  The  cilia  have  been  thought  to  be  homologous  with 
the  tentacles  of  Drosera,  but,  as  Goebel  pointed  out,  the  comparison 
fails  in  that  the  ciha  show  no  trace  of  glandular  tissue,  and  have 
evidently  a  widely  different  function.     The  whole  trap  acts,  to  quote 


Chapter  XII  —  183  —  Dionaea  and  Aldrovanda 

LiNDLEY  (1848),  like  the  jaws  of  a  steel  trap.  The  simile  may  not 
be  appHed  too  rigorously  since  it  is  not  the  edges  of  the  lobes  which 
catch  the  prey. 

The  two  lobes,  when  the  leaf  is  widely  open,  stand  at  an  angle 
of  40-50  (Darwin:  ''80")  degrees  to  each  other,  published  drawings 
being  often  in  error  on  this  point  (iS  —  40).  They  are  clothed  with 
a  distinctly  firm  epidermis  of  straight  walled  cells,  elongated  parallel 
with  the  veins,  becoming  somewhat  wavy  on  approaching  the  margins, 
which  lends  a  surprising  stiffness  to  the  trap.  When  once  a  lobe  is 
cut,  as  in  making  sections,  it  becomes  evident  that  the  epidermis  is 
the  only  mechanical  tissue  present.  The  outer  surfaces  bear  scattered 
stellate  trichomes  {18 —  11)  which  are  found  also  in  the  bays  between 
the  ciha  of  seedhng  traps,  and  even  shghtly  invading  their  inner  sur- 
faces. The  inner  surfaces  are  supplied  with  very  numerous  glands, 
all  having  the  same  structure.  They  consist  of  two  basal  epidermal 
cells,  placed  parallel  with  the  midrib,  and  whose  walls  are  thickened 
by  cellulose  ridges,  producing  an  appearance  which  led  Macfarlane 
(1892)  to  take  them  to  be  ''intercellular  protoplasmic  connections." 
What  he  saw,  it  seems,  are  only  layers  of  cytoplasm  lying  between 
the  cellulose  ridges,  but  this  is  not  to  deny  that  such  protoplasmic 
connections  may  not  also  be  present.  Surmounting  the  two  basal 
cells  is  a  second  course  of  two  small  cells,  with  cutinized  diametrical 
wall,  constituting  the  stalk.  This  supports  a  large  capital  of  about 
32  cells  in  two  courses,  the  lower  capped  by  the  upper  to  form  a  bun- 
shaped  mass  (iS  —  12,  13).  There  are  two  physiological  kinds  of 
these  glands,  as  evidence  adduced  by  Frank  Morton  Jones  indicates 
(1923),  namely  digestive  (and  absorptive)  and  alluring.  The  former, 
thought  by  Ellis  "perhaps"  to  discharge  a  sweet  liquor,  occupy  the 
major  area  of  the  surface  and  are  so  numerous  that  they  often  crowd 
on  each  other  {18 — i).  The  alluring  glands  occupy  a  narrow  zone 
just  within  the  ciHated  margin.  Between  the  two  groups  of  glands 
there  is  a  narrow  zone  quite  free  of  glands  (Jones).  Though  identical 
in  structure,  the  digestive  and  alluring  glands  display  some  differences. 
The  digestive  glands  {18 — 12,  13)  are  rendered  conspicuous  by  their 
deep  red  color,  due  to  anthocyanin  present  in  the  sap  of  their  cells, 
and  are  responsible  for  the  deep  red  note  of  color  of  the  inner  surface 
of  the  trap.  The  alluring  glands  (in  the  traps  I  examined)  contain 
no  pigment.  These  are  imbedded  somewhat  in  the  epidermis  {18  — 
14),  while  the  digestive  glands  stand  out  prominently.  These  also 
are  larger  (0.096-0.1  mm.  in  diam.)  than  the  alluring  glands,  which 
measure  0.06-0.073  mm.  in  diameter.  That  the  alluring  glands  se- 
crete a  sugar  (or  something  attractive  to  insects)  is  supported  strongly 
by  Jones'  observations  already  alluded  to:  "...  these  little  ants 
were  observed  to  occupy  a  uniform  position  on  the  upper  surface, 
their  heads  close  to  the  bases  of  the  marginal  spikes.  As  they  moved 
slowly  across  this  belt  of  the  leaf  they  made  frequent  and  prolonged 
pauses,  during  which  their  mouth  parts  were  observed  under  the  lens 
to  be  in  motion  against  the  surface  of  the  leaf.  A  larger  and  winged 
hymenopteron  was  observed  to  be  engaged  in  the  same  performance. 
Obviously  they  were  feeding  upon  some  attractive  exudation  of  the 
leaf.     The  behavior  of  visiting  insects  is  entirely  convincing  to  the 


Francis  E.  Lloyd  —  184  —  Carnivorous  Plants 

observer  that  a  baited  area  extends  across  the  leaf  surface  just  within 
the  bases  of  the  marginal  spines.  This  baited  marginal  band  is  so 
situated  upon  the  leaf  surface  that  a  visiting  insect  in  length  too  small 
to  reach  from  the  halt  to  the  trigger  hairs,  usually  does  not  spring  the 
trap.  Whether  or  not  these  conditions  are  to  be  interpreted  as  ad- 
justments to  that  end,  the  effect  of  the  arrangement,  in  conjunction 
with  the  peculiarities  of  the  closing  movement  by  which  small  insects 
are  given  an  opportunity  to  escape,  is  to  limit  the  captures  of  the 
leaves  to  insects  approximating  one  quarter  of  an  inch  or  more  in 
length."  Jones  examined  the  captures  of  fifty  closed  traps  and  found 
that,  of  all  the  prey  "only  one  was  less  than  5  mm.  in  length  and 
only  seven  less  than  6  mm.;  they  were  10  mm.  or  more  in  length, 
with  a  maximum  of  30  mm."  (Jones  1923).  In  this  way  was  cor- 
roborated Darwin's  suspicion  that  the  posture  first  assumed  by  the 
trap  on  closure  in  which  the  marginal  spines  form  a  cage  is  one  which 
permits  small  insects  to  escape.  I  have  observed  larger  ones,  small 
centipedes,  doing  their  best  to  force  their  way  between  the  spines, 
but  without  success.  A  wood  louse  was  seen  to  free  itself  because 
its  position  was  such  that  its  carapace  held  the  lobe  margins  open 
just  enough  to  allow  escape,  which  was  evidently  facilitated  by  the 
fact  that  the  lateral  projections  of  the  carapace  allowed  leg  movement. 
Many  a  wood  louse  is  not  so  lucky. 

The  closure  of  the  trap,  a  seismonastic  movement,  normally  follows 
when  sensitive  or  trigger  hairs  are  disturbed  as  Curtis  recorded  in 
1834.  "Each  side  of  the  leaf  is  a  little  concave  on  the  inner  side 
where  are  placed  three  deHcate,  hair-hke  organs,  in  such  an  order, 
that  an  insect  can  hardly  traverse  it,  without  interfering  with  one 
of  them,  when  the  two  sides  suddenly  collapse  and  enclose  the  prey 
with  a  force  which  surpasses  the  insect's  efforts  to  escape."  Though 
usually  three  in  number  on  each  lobe,  there  may  on  occasion  be  more 
or  fewer.  When  three,  they  stand  at  the  angles  of  a  triangle 
placed  in  the  middle  of  the  lobe  with  its  base  nearer  and  parallel 
to  the  outer  cihated  margin.  If  we  examine  one  of  these  hairs  we 
find  that  it  is  multicellular  and  displays  two  distinct  regions.  The 
outer  of  these  is  a  slender  cone  {18 — 2)  in  form,  about  1.5  mm. 
in  length  and  0.15  mm.  thick  at  the  base.  It  is  composed  of  elon- 
gated, thick  walled  cells  and  constitutes  a  lever;  any  slight  move- 
ment causes  a  bending  in  the  basal  region,  to  which  Oudemans  (1859) 
attributed  a  special  sensitivity.  This  is  only  0.15  mm.  in  height 
and  is  conspicuous  on  account  of  a  deep  constriction  slightly  below 
the  base  of  the  lever,  first  described  by  Goebel  (1891).  This  con- 
striction, the  hinge  or  bending  place  (Goebel),  is  made  up  of  a  single 
transverse  ring  of  cells  of  which  their  outer  walls  are  deeply  indented 
{18 — 15,  16).  Their  lateral  walls  are  thick  and  collenchymatous  in 
character,  their  end  walls  thin.  Because  of  the  indentation,  the  outer 
wall  is  thinner  at  this  point.  Within  the  ring  of  indented  cells  there 
is  a  medullary  group  of  elongated  cells,  tracheidal  in  character 
(Goebel),  absent  from  the  small  trigger  hairs  of  seedling  leaves,  which 
measure  only  0.15  to  0.2  mm.  in  length,  of  which  the  lever  occupies 
well  over  a  half,  the  greatest  width  being  0.03  mm.  {18  —  3).  The 
indented  cells  are  surmounted  by  three  layers  of  flattish  cells  under- 


Chapter  XII  — 185  —  Dionaea  and  Aldrovanda 

lying  the  base  of  the  lever,  and  stand  upon  a  base  of  about  four  or 
five  courses  of  cells,  meeting  the  general  leaf  surface.  All  the  cells 
have  rather  thick  walls,  and  there  are  no  intercellular  spaces.  This 
whole  basal  region  is  the  podium.  Its  histological  character  just 
mentioned  is  such  as  to  permit  bending.  It  is,  however,  the  whole 
podium  which  bends,  and  not  merely  the  cells  under  the  constriction 
0/  ~  5)-  I  noted  while  cutting  hand  sections  that  the  podium  readily 
stretches  and  compresses,  bending  being  a  combination  of  these.  But 
although  the  whole  podium  bends  notably  when  the  lever  is  much 
displaced,  it  is  quite  clear  on  watching  with  the  microscope  that 
sHght  bending  is  evident  first  and  at  once  in  the  constricted  zone, 
as  GoEBEL  recorded. 

The  hinge  cells  were  thought  by  Macfarlane  (1892)  to  be  de- 
void of  a  cuticle,  or  to  have  a  very  thin  one.  Haberlandt,  however, 
denied  this.  The  cuticle  is  fairly  thick  and  displays  a  certain  amount 
of  wrinkling,  which  would  allow  freer  movement  of  the  coUench}^- 
matous  cell  walls  beneath.  It  further  appears  finely  punctate,  inter- 
preted by  Macfarlane  as  due  to  the  presence  of  pores.  Haberlandt 
regarded  this  to  be  due  rather  to  denticulations  of  the  inner  surface 
of  the  cuticle  which  prevent  loosening  of  the  cuticle  under  repeated 
bendings  by  anchoring  it  to  the  cellulose  wall.  It  is  easier  to  agree 
with  Haberlandt  that  the  points  seen  (of  which  there  is  no  doubt) 
are  not  pores,  than  that  they  are  extensions  of  the  cuticle  into  the 
cellulose  underneath.  Nevertheless,  it  is  possible  to  see  minute  ir- 
regularities on  the  inner  face  of  the  cuticle,  so  that  the  interface 
between  the  cuticle  and  cellulose  is  greater  than  it  would  be  other- 
wise. 

The  medullary  cells  show  some  peculiarities.  In  addition  to  a 
fime  porosity  (Goebel),  Haberlandt  records  the  presence  of  mi- 
nute granular  inclusions  of  high  refringency  in  the  middle  layer 
between  the  walls  and  between  these  and  the  hinge  cells.  He  de- 
scribes these  as  cutinized  granules.  Some  cutinization  certainly  oc- 
curs. 

There  is  no  vascular  connection  between  the  medullary  cells  of 
Goebel  and  the  leaf,  since  there  is  no  vein  in  the  hair. 

The  internal  structure  of  the  leaf  blade  or  trap  was  described  by 
MuNK  in  1876,  concerned  as  he  was  with  the  direction  of  movement 
of  electrical  currents,  in  much  detail  as  to  form  and  position  of  the 
component  cells.  We  recall  that  the  trap  has  a  massive  midrib  trav- 
ersed longitudinally  by  a  double  vascular  bundle  which  gives  ofif 
branches,  running  parallel  to  each  other,  towards  the  margins,  ap- 
proaching which  they  form  a  coarse  zig-zag  network.  All  the  remain- 
ing space  between  the  two  epiderms  is  occupied  by  a  thin-walled 
parenchyma,  of  large-sized  cells  inside  and  smaller  against  the  epi- 
derm,  those  against  the  inner  epidermis  being  larger  than  those  against 
the  outer,  where  they  are  much  smaller  and  more  numerous.  There 
are  more  smaller  cells  opposite  the  vascular  bundles  and  more  cells 
of  very  large  size  between  the  vascular  bundles  {18 — 10).  The 
walls  beneath  the  inner  epidermis  and  the  cells  of  the  first  parenchyma 
course  are  thickened  into  a  collenchyma  {18  —  5)  and  to  some  ex- 
tent also,  those  between  this  and  the  next  course.     This  mechanical 


Francis  E.  Lloyd  —186— Carnivorous  Plants 

element  is  absent  from  the  outer  epidermis  region.  There  is  a  total 
absence  of  palisade  tissue,  a  feature  common  to  many  carnivorous 
plants,  as  Schmid  showed.  The  parenchyma  cells  are  elongated  in 
different  degrees  according  to  position.  Below  the  chief  vascular 
strands  in  the  midrib  their  long  axes  run  lengthwise,  above  at  right 
angles  to  it  and  here  are  shorter.  Those  of  the  lateral  regions  run 
up  into  the  two  lobes,  and  here  they  attain  their  greater  longitu- 
dinal dimensions,  the  largest,  in  the  middle,  being  the  longest.  Ap- 
proaching the  margins,  they  become  shorter  and,  as  Munk  points 
out,  are  shortest,  though  not  round,  at  the  base  of  the  ciha,  length- 
ening again  in  the  cilia  themselves.  The  intercellular  spaces  are 
large  and  extensive,  and  while  the  protoplasm  is  very  tenuous,  chlor- 
oplasts  are  present  and  much  starch  may  occur,  as  Brown  pointed 

out. 

Physiology.  —  If  the  question  is  asked  how  the  structure  just  de- 
scribed is  related  to  the  movement  of  the  lobes,  the  answer  is  indicated 
by  comparing  it  with  that  of  the  lobes  of  very  small  traps  found 
in  seedUngs,  and  with  those  of  Aldrovanda.  They  all  show  the  same 
capacity  for  movement,  whether  the  parenchyma  consists  of  one 
course  of  cells  only  {Aldrovanda)  or  of  a  few,  as  in  seedlings  traps. 
The  evidence  indicates  that  the  seat  of  movement  resides  in  the 
epidermis  first  of  all.  Further  complication  of  structure  is  connected 
with  the  mechanical  strength  of  the  lobes  naturally  greater  in  the 
massive  leaves  of  adult  Dionaea  plants.  That  is,  the  machine  as 
such  is  stronger  (involving  parenchyma  cells)  and  can  exert  more 
energy  in  the  last,  without  any  difference  in  the  seat  or  directions 
of  movement.  All  movement  occurs  in  the  lobes  and,  as  Brown 
showed,  none  in  the  midrib,  which  is  therefore  not  a  hinge  in  any 
sense.  This  is  indicated  in  the  diagram,  borrowed  from  Ashida,  shown 
in  i8  —  4a,  though  this  does  not  indicate  the  extreme  possibilities 
of  closure,   better  shown  in   iS  —  46. 

The  stimulus  leading  to  action.  —  In  nature  the  walking  of  an  insect 
across  a  lobe  of  the  trap  almost  inevitably  results  in  the  disturbance  of 
the  sensitive  hairs,  ensuring  the  prompt  closure  of  the  trap.  This 
Curtis  (1834)  clearly  observed.  Ellis  (1770)  had  thought  the  move- 
ment as  following  irritation  of  the  glands  by  the  feet  of  the  prey,  and 
Broussonet  (1784)  believed  that  it  was  due  to  the  loss  of  turgidity 
caused  by  the  pricking  of  the  surface  by  insects.  But  from  the  time 
of  Curtis  it  was  supposed  that  it  was  necessary  only  to  touch  a  hair 
to  bring  about  closure,  until  the  work  of  Burdon-S Anderson  demon- 
strated the  fact  of  summation  of  stimuh.  Macfarlant:  found  inde- 
pendently that  under  usual  circumstances  (temperature  is  important) 
in  order  to  effect  closure  of  the  trap,  it  requires  two  stimuh,  either  by 
touching  the  same  trigger  hair  twice,  or  any  two  different  ones  with  an 
interval  of  time  neither  too  short  (about  0.75  sec.)  nor  too  long  (oyer 
20  sec).  This  was  in  1892.  Previous  observers,  with  the  exception 
above  noted,  had  failed  to  notice  this  behavior,  very  obvious  when 
once  seen.  For  example,  Darwin  says:  "It  is  sufficient  to  touch  any 
one  of  the  six  filaments  to  cause  both  lobes  to  close  .  .  . ,"  but  observed 
that  an  extremely  delicate  stimulus  might  be  inadequate.  Darwin 
does  remark,  however,  that  "  on  another  occasion  two  or  three  touches 


Chapter  XII  — 187  —  Dionaea  and  Aldrovanda 

of  the  same  kind  were  necessary  before  any  movement  ensued,"  but 
failed  to  indicate  a  general  rule. 

Following  in  the  trail  left  by  Burdon-S Anderson  and  Munk, 
the  method  of  electrical  stimulation  has  been  used  by  Brown  and 
Sharp  (1910)  to  study  time  and  intensity  relations.  They  found 
first  of  all  that  at  15  deg.  C.  two  stimuli  were  always  required,  and 
must  be  applied  within  an  interval  of  from  1.5  to  20  seconds.  But 
at  the  higher  temperature  of  35  deg.  C.  frequently  only  one  stimulus 
was  required,  while  at  40  deg.  C.  only  one  stimulus  was  required 
in  50%  of  the  instances.  In  order  to  elucidate  this  behavior,  Brown 
and  Sharp  tried  the  effect  of  electrical  shock  in  various  intensities 
and  found  that  the  number  of  shocks  required  varied  inversely  with 
their  intensity.  The  authors  then  proceeded  to  determine  the  number 
of  stimuli  (by  bending  the  sensitive  hairs)  required  when  applied  at 
various  intervals,  viz.,  20  seconds,  i,  2,  and  3  minutes,  and  found 
that  for  these  intervals,  2.0,  3.8,  6.2  and  8.7  stimuH  (averages  of 
several  tests)  were  required.  It  thus  appears  that  "the  number  of 
stimuU  necessary  for  complete  response  varies  almost  directly  with 
the  length  of  the  intervals.  It  would  seem,  therefore,  that  the  re- 
sponse follows  on  a  definite  amount  of  accumulated  efiect,  "possibly 
the  accumulation  of  some  chemical  substance  as  the  result  of  ex- 
citation." It  should  be  added  that  the  physiological  condition  of 
individual  leaves  has  a  modifying  effect  —  at  a  given  time  and  place 
all  leaves  are  not  equally  sensitive. 

In  1873,  stimulated  by  Darwin's  studies,  J.  Burdon-S  Anderson 
published  the  first  observations  on  the  electric  current  in  leaves  as 
indicating  physiological  disturbance,  using  those  of  Dionaea.  Having 
demonstrated  that  there  is  a  normal  current  from  base  to  apex  of 
the  trap  while  there  is  one  in  the  reverse  sense  in  the  petiole,  related 
quantitatively  so  that  if  the  petiole  were  cut  off  at  different  lengths, 
the  current  in  the  trap  was  increased,  he  then  studied  the  effect  of 
stimulating  the  sensitive  hairs  on  the  current.  Whenever  a  fly  was 
allowed  to  walk  into  the  trap  it  disturbed  the  hairs  and  at  once  there 
was  observed  a  deflection  of  a  galvanometer.  If  the  stimulus  were 
repeated,  the  galvanometer  indicator  came  to  rest  in  a  different  position 
(more  to  the  left)  each  time.  Disturbance  of  the  hairs  with  a  camel's 
hair  brush  had  the  same  effect.  Thus  the  fact  that  movements  of 
the  sensitive  hairs  constitute  a  stimulus  was  demonstrated  by  noting 
consequent  electrical  disturbance. 

Localization  of  perception.  —  It  had  been  generally  accepted  since 
OuDEMANs'  time,  in  spite  of  Meyen's  evidence  to  the  contrary,  that 
StimuH  leading  to  closure  could  be  received  only  by  the  sensitive 
hairs.  Oudemans  could  not  repeat  Meyen's  (1839)  result,  namely, 
causing  closure  by  scraping  the  midnerve.  Darwin,  however,  found 
both  the  area  within  the  triangle  formed  by  the  sensitive  hairs  and 
the  surface  along  the  midrib  to  be  sensitive,  so  that  when  scratched 
or  pricked  with  a  needle,  closure  followed.  Macfarlane  found  that 
this  occurred  on  pinching  the  blade  of  the  trap  with  steel  forceps, 
but  that  two  stimuli  were  required.  Brown  and  Sharp  confirmed 
Macfarlane's  observation,  only  quaUfying  the  numerical  expression 
since  they  found  that  one  only,  or  two  or  more  pinches  might  be  re- 


Francis  E.  Lloyd  —  188  —  Carnivorous  Plants 

quired  to  procure  reactions.  They  also  found  that  the  trap  may  be 
stimulated  to  close  by  the  apphcation  of  strong  electrical  stimuli  to 
the  petiole.  That  various  kinds  of  stimulating  agents  (cutting,  hot 
water  at  65  deg.  C,  various  chemicals,  electrical  stimuli)  can  effect 
response  has  been  abundantly  shown  by  Darwin,  Burdon-S Anderson, 
MuNK,  Macfarlane,  Brown  and  Sharp.  But  it  is  easier  to  stim- 
ulate by  cutting,  etc.  the  upper  face  of  the  leaf  than  the  lower.  If 
the  lower  face  is  cut,  it  must  be  cut  deeply  so  as  to  reach  the  upper 
face  tissues  (Munk).  Stimulation  is  not  procurable  by  cutting  the 
outer  marginal  zone  of  the  cilia  (Munk).  It  appears  therefore  that 
the  more  ventral  tissues  (Munk:  the  parenchyma)  are  sensitive,  not 
the  more  dorsal.  But  it  remains  the  central  fact  that  normally  the 
closure  of  the  trap  results  from  the  stimulation  of  the  sensitive  hairs, 
even  though  very  slow  closure  may  take  place  in  response  to  applied 
protein  (chemonasty),  after  the  power  to  react  seismically  has  been  lost. 
It  was  natural  for  earlier  observers,  from  Curtis  on,  to  suppose  the 
whole  of  the  hair  to  be  sensitive,  as  did  Darwin.  "These  filaments, 
from  their  tips  to  their  bases,  are  exquisitely  sensitive  to  a  momentary 
touch"  (1875).  Sixteen  years  previously,  however,  Oudemans  had 
succeeded  in  showing  experimentally  that  the  sensitivity  resides  in 
the  basal  region  of  the  hair,  to  which  Munk  (1876)  and  Batalin 
(1877)  agreed.  Darwin  appears  to  have  attached  importance  to  the 
flexible  base  in  allowing  the  hair  to  bend  rather  than  be  broken  by 
the  closing  lobes.  He  saw  that  there  is  a  constriction  about  the 
base,  merely  mentioning  it.  Goebel  (1891),  in  view  of  the  config- 
uration of  the  cells  of  the  constriction  (as  well  as  of  the  organ  in 
general),  believed  that  these  receive,  on  movement  of  the  "lever," 
a  "much  stronger  stimulus  than  any  other  leaf  cell."  The  stimulus 
is  hindered  from  moving  upward  by  suberized  cells  in  the  two  courses 
above  (in  which  I  find  very  little  if  any  suberization). 

The  cells  of  the  constricted  zone  were  regarded  by  Haberlandt 
(1901)  as  special  sense  organs.  The  cells  respond  to  compression, 
but  not  to  release  from  a  constrained  bent  position  (Brown  and 
Sharp),  and  if  the  hair  is  amputated,  pressure  on  the  remaining 
base  will  procure  closure  (Brown  and  Sharp  19 10). 

The  mechanism  of  closure.  —  The  first  effort  to  explain  the  mecha- 
nism of  closure  in  the  trap  of  Dionaea  was  made  by  Meyen,  in  1839. 
To  him  the  spiral  vessels  of  the  nerves,  because  of  their  spiral-spring- 
like structure,  seem  to  afford  a  suitable  mechanism.  If  the  idea  is 
naive,  it  still  indicates  the  early  desire  and  effort  to  answer  the  ques- 
tion. 

Ziegenspeck  much  later  (1925)  {through  von  Guttenberg)  at- 
tributed importance  to  a  hinge  mechanism,  saying  that  closure  is 
due  to  the  loss  of  turgor  by  the  cells  of  the  tissues  above  the  mid- 
vein.     Von  Guttenberg  (1925)  showed  this  to  be  incorrect. 

Darwin  described  the  closure  of  the  trap  as  passing  through  two 
phases.  There  is  first  a  sudden  response,  bringing  the  edges  of  the 
lobes  into  some  approximation,  enough  at  least  to  bring  the  ciHa  in 
position  so  as  to  make  a  sort  of  cage  preventing  the  escape  of  suf- 
ficiently large  prey,  and  allowing  small  ones  (ants  especially)  to  escape 
(Jones)    (//  —  6).      This    is    followed    by    a    slow   movement    during 


Chapter  XII  — 189  —  Dionaea  and  Aldrovanda 

which  the  lobes  are  closely  apposed,  pressing  together,  their  mar- 
ginal regions  being  curved  outwards.  Ashida  in  his  studies  of  Al- 
drovanda has  called  these  the  "shutting"  and  the  "narrowing"  phases 
of  closure.  We  are  now  to  consider  the  first  of  these,  to  which  more 
attention  has  been  paid  than  to  the  latter.  Darwin  investigated 
the  mechanism  of  closure  by  making  marks  on  the  upper  surface  of 
a  lobe  in  the  transverse  sense  before  stimulation,  viewing  the  same 
through  a  window  cut  in  the  opposite  lobe.  When  closure  had  been 
effected,  the  marks  were  found  to  be  closer  together  and  he  concluded 
from  this  that  closure  is  accompanied  by  a  transverse  contraction 
of  the  more  superficial  cells  of  the  whole  upper  surface  and  sub-surface. 
He  thought  also  that  the  tissues  above  the  midvein  took  part  with  a 
hinge-like  action. 

This  contraction  was  attributed  by  Munk  (1876)  to  the  loss  of 
turgor  by  more  sensitive  superficial  tissues  ("parenchyma")  lying 
beneath  the  upper  epidermis,  accompanied  by  the  active  expansion 
of  the  tissues  of  the  lower  layers  of  parenchyma  near  the  under  epi- 
dermis. De  Candolle,  from  anatomical  study,  seems  to  have  held 
essentially  the  same  view. 

Burdon-Sanderson,  seeking  for  a  "resistance"  which  has  to  be 
removed  in  responding  to  stimulation,  could  find  it  only  in  the  turgor 
of  the  leaf.  "In  the  case  of  cells  which  are  excitable  the  immediate 
effect  of  excitation  is  suddenly  to  diminish  the  power  (of  turgescence) 
and  thereby  produce  a  diminution  of  the  volume  of  the  cells  which 
is  equal  to  that  of  the  water  (probably  holding  diffusible  bodies  in 
solution)  which  is  discharged  into  the  intercellular  spaces."  It  was 
already  known  from  the  work  of  Bruecke,  cited  by  Munk,  that 
the  only  mechanism  of  the  actual  movements  of  the  sensitive  plant 
(Mimosa)  was  such  a  diminution  of  turgor  in  the  sensitive  region  of 
the  pulvinus. 

Batalin  (1877)  re-examined  the  matter  and,  confirming  Darwin's 
observations,  extended  the  account  to  include  subsequent  opening. 
Using  the  same  method  as  Darwin,  namely,  measurements  of  changes 
between  ink  marks  during  closure,  Batalin  came  to  agree  with  him 
that  there  is  a  real  contraction  of  the  upper  side  of  the  lobes  and  a 
concomitant  expansion  of  the  lower,  both  longitudinal  and  transverse. 
He  takes  issue  with  Darw^in  (and  Ziegenspeck,  1925),  however, 
holding  that  the  midvein  takes  no  part,  or  at  least  a  very  small  and 
unobservable  part.  When  the  trap  remains  closed,  as  it  does  for  a 
week  or  ten  days  (or  even  longer)  if  it  has  been  fed  a  Hving  insect, 
it  enters  at  once  into  a  second  phase  of  movement.  The  lobes  begin 
to  compress  together  mutually,  so  that  in  a  half-hour  (as  I  have 
observed)  much  of  their  inner  surfaces  are  in  actual  contact,  leaving 
however  a  space  above  the  midvein.  The  compression  is  such  that 
the  margins  of  the  lobes  are  turned  outwards  and  the  cilia  come  to 
lie  more  nearly  parallel  to  the  general  plane  of  the  lobes  (iS  —  4b). 
As  Batalin  observes,  the  pressure  exerted  is  enough  to  crush  a  soft- 
bodied  insect.  Darwin  thought  that  this  compression  is  owing  to 
the  absorption  of  animal  matter.  Batalin  said  that  it  is  caused  by 
the  reduction  of  the  expansion  of  the  lower  surface,  for  he  determined 
that  during  the  slow  compression  of  the  lobes  together  after  the  in- 


Francis  E.  Lloyd  —  190  —  Carnivorous  Plants 

itial  closure,  there  is  actual  and  measurable  shrinkage  of  that  sur- 
face, except  where  the  body  of  the  insect  propped  it  out.  AsnroA 
(1934),  we  remember,  compares  this  movement  with  the  slow  movement 
which  supervenes  on  "closure"  in  Aldrovanda,  caUing  it  the  "narrow- 
ing" movement. 

But  the  main  contention  of  Batalin,  in  which  he  was  in  agree- 
ment with  Darwin,  was  that  during  closure  there  is  an  actual  shrink- 
age of  the  upper  or  inner  surface,  accompanied  by  expansion  of  the 
lower.  This  amounts  to  saying  that  the  tissues  including  the  epidermis, 
contract  in  the  upper  region,  and  expand  in  the  lower.  This  was 
made  an  issue  by  Brown  (1916).  Using  again  the  same  method, 
he  found  extension  in  the  lower  surface  and  decreases  in  the  upper. 
But  the  latter  amounts  were  very  small,  amounting  to  only  1.5% 
of  the  original  distances,  while  for  the  lower  surface  the  differences 
of  dimension  range  between  :^.s  to  10,  or  an  average  of  6.7%.  Fur- 
thermore, and  this  is  of  prime  importance,  Brown  found  that  there 
is  an  error  of  observation  due  to  changed  surface  curvatures,  so  that 
the  actual  surface  retains  dimensions  which  it  only  seems  to  lose, 
since  what  one  measures  is  not  the  curved  surface,  but  the  chord 
of  its  arc.  Brown's  opinion,  based  on  the  measurement  of  a  model, 
was  that  "if  there  is  any  change  in  the  area  of  the  upper  surface 
during  closure  it  is  probably  in  the  direction  of  an  increase  rather 
than  in  that  of  a  decrease,"  in  this  squarely  contravening  previous 
opinions.  During  subsequent  opening,  however,  the  reverse  obtains. 
The  upper  surface  now  expands  (to  the  amount  of  9.4%  of  the  orig- 
inal measurements)  while  the  under  surface  maintains  its  enlargement 
merely.  True  there  is  a  small  apparent  expansion  which  is  attrib- 
uted by  Brown  to  the  same  sort  of  error  as  that  detected  in  the 
measurements  of  shrinkage  of  the  inner  surface.  It  was  shown  also 
that  as  the  result  of  stimulation  the  growth  of  the  lobes  of  the  trap 
was  greater  by  a  good  deal  than  their  growth  during  a  long  period 
when  there  was  no  stimulation,  from  which  it  appears  that  stimu- 
lation is  a  Hberator  of  growth  and  that,  accordingly,  the  responses 
to  stimulation  become  less  vigorous  if  the  stimulus  is  repeated  of- 
ten. This  recalls  Batalin's  experiments  which  showed  that  when 
a  trap  was  stimulated  seven  times  on  ten  successive  days,  the  abil- 
ity to  respond  was  not  lost,  but  was  progressively  very  materially 
weakened. 

What  then  takes  place  during  the  response  movement?  Macfar- 
LANE  allowed  that  the  contraction  observed  by  Darwin  would  be 
due  to  the  escape  of  water  through  pores  in  the  protoplasm,  and 
sought  for  some  visible  evidence  of  such.  He  ventured  to  suggest 
that  appearances  in  the  parenchyma  cells  of  the  motile  tissue,  con- 
sisting of  "rows  of  extremely  minute  globules  or  pores  in  the  proto- 
plasm," suggested  a  parallel  with  animal  voluntary  muscle,  and  that 
on  ultimate  analysis  the  activity  might  be  explained,  as  in  the  case  of 
plant  cells,  by  water  movements.  This  is  not  the  same  as  saying 
that  "Macfarlane  beheved  that  there  are  structures  in  the  leaves  .  .  . 
which  resemble  animal  muscles." 

Batalin,  not  being  able  to  detect  any  change  in  translucence  of 
the  tissues,   which  would  be  expected  if  there  were  any  effusion   of 


Chapter  XII  — 191  —  Dionaea  and  Aldrovanda 

sap  into  the  intercellular  spaces,  such  as  is  well  known  to  take  place 
in  the  pulvini  of  Mimosa  during  movement  response,  denied  that 
there  is  any  extrusion  of  water  by  the  cells  in  the  upper  moiety  of 
the  trap  lobe,  and  Brown  denying  the  contraction  of  the  upper  face 
sees  no  necessity  for  such  extrusion,  but  falls  back  on  the  expansion 
of  the  cells  of  the  lower  face.  This  makes  it  necessary  to  find  a  move- 
ment of  water  from  a  source  sufficient  for  this  expansion.  The  only 
source  considered  is  the  parenchyma  of  the  upper  face,  in  which,  since 
the  intercellular  spaces  are  not  flooded,  water  must  pass  from  cell 
to  cell;  the  movement  would  then  resemble  that  of  geotropism. 
An  acknowledged  difficulty  is  seen  in  the  rapidity  of  the  response 
which,  though  often  slow  enough,  is  at  times  and  normally  so  rapid 
that  complete  closure  is  reached  in  the  space  of  even  less  than  a 
half  second  (77  —  6).  This  difficulty  must  be  faced  as  also  that 
arising  from  the  attempt  to  account  for  the  loss  of  water  by  some 
cells  (those  of  the  upper  face)  by  changes  in  the  substances  present 
in  the  cells  to  less  osmotically  active  ones,  thus  permitting  the  water 
to  be  drawn  off  into  other  cells  (those  of  the  lower  face)  to  facili- 
tate their  expansion.  How  sufficient  water  can  thus  be  moved  to 
procure  the  recorded  amount  of  expansion  of  the  lower  face,  with- 
out causing  a  reduction  (contraction)  of  the  upper  face  in  even  greater 
amount  (since  the  latter  is  shorter,  if  only  slightly),  is  not  clear. 

This  rapidity  of  movement  seems  to  demand  that  there  be  a  con- 
dition of  unstable  equilibrium  resulting  from  growth  and  residing  in 
the  trap  lobes.  Batalin  advanced  this  idea  but  he  was,  it  is  recalled, 
committed  to  explain  a  shortening  of  the  upper  face.  That  tissue 
tensions  do  exist  may  be  taken  for  granted  (Darwin),  just  as  they 
exist  in  the  valves  of  the  fruit  of  Impatiens.  In  this  plant  the  ten- 
sions are  held  in  check  by  mechanical  conditions,  namely,  the  mu- 
tual adherence  of  the  valves.  This  disturbed,  the  valves  spring  away 
by  immediately  curving  in  the  same  sense  as  the  lobes  of  the  Dionaea 
trap.  In  the  latter  the  lobes  maintain  their  form,  unless  stimulated, 
by  the  opposition  of  the  two  epiderms  to  their  contiguous  tissues. 
When  stimulated,  the  balance  of  forces  is  upset  and  curvature  imme- 
diately follows.  That  is,  when  stimulation  takes  place  something 
happens  to  release  the  tensions.  What  this  something  is  we  do  not 
yet  know.  If  we  might  postulate  chemical  changes  in  the  cell 
contents  from  sugar  to  starch  in  the  upper  surface  of  the  trap  lobes, 
it  would  serve  us  with  a  mechanism  for  changing  the  tensions,  but 
sufficiently  rapid  changes  are  not  known.  Brown's  experiment  in 
which  he  substituted  xylene,  in  which  sugars  are  insoluble,  for  water, 
are  suggestive,  but  not  convincing  further  than  showing  that  ten- 
sions exist  which  might  be  released  by  such  a  mechanism.  This  is 
in  essence  the  theory  put  forth  by  voN  Guttenberg  (1925)  who  be- 
lieves that  the  movement  is  caused,  not  by  any  reduction  of  turgor 
in  any  tissues  whatever,  but  by  the  drag  of  the  parenchyma  on  the 
two  epiderms  (upper  and  lower),  the  upper  being  thicker  and  less 
extensible  than  the  lower  {iS  —  5,  6,  10),  as  Macfarlane  also  main- 
tained. That  this  drag  is  positive,  exerting  a  pull  on  the  epiderms, 
is  indicated  by  the  fact  that  if  the  tissues  of  the  upper  epidermis 
and   the    contiguous   parenchyma   are   partially   robbed   of   water   by 


Francis  E.  Lloyd  —  192  —  Carnivorous  Plants 

the  application  of  a  plasmolyte  to  the  upper  surface,  no  closure  can 
take  place  on  stimulation  (application  of  the  plasmolyte  to  the  base 
of  the  sensitive  hairs  was  avoided).  Indeed,  any  experiment  in  which 
the  parenchyma  is  robbed  of  its  turgor  renders  the  valves  incapable 
of  closure.  This  positive  drag  therefore,  present  before  closure, 
stretches  the  epiderms  as  much  as  it,  previous  to  excitation,  is  ca- 
pable. On  stimulation  this  capacity  is  increased,  the  epiderms  re- 
sponding by  expanding  differentially,  the  upper  scarcely  at  all,  the 
lower  6-7%,  in  accordance  also  with  measurements  by  Brov^n  and 
others.  Von  Guttenberg  then  faces  the  questions,  whence  the  water 
necessary  to  increase  the  volume  of  the  parenchyma  cells,  and  what 
conditions  allow  the  momentary  increase  of  water  uptake?  To  the 
former  he  suggests  that  the  water  comes  from  the  vascular  tissues; 
to  the  latter  that  it  may  be  due  to  the  sudden  changes  of  substances 
in  the  sap  from  a  large  molecular  to  a  small  molecular  condition. 
Von  Guttenberg  extends  this  theory  to  the  case  of  Aldrovanda, 
making  the  pertinent  observation  that,  in  view  of  the  fact  that  this 
trap  has  only  a  single  course  of  parenchyma  cells,  it  is  unthinkable 
that  there  exists  a  differential  action  in  the  tissues  between  the  epi- 
derms, of  which  more  beyond. 

Von  Guttenberg's  difficulties  may,  however,  on  theoretical  grounds 
be  avoided.  If  it  be  assumed  that  the  response  to  irritability  is  con- 
fined to  the  epidermis,  we  might  argue  that  this  response  consists 
only  in  the  reduction  of  turgor.  True,  as  von  Guttenberg  says, 
this  would  be  removing  one  factor  in  tissue  stretching,  but  as  turgor 
expands  the  cells  in  every  direction,  the  relative  amount  of  exten- 
sion depending  on  the  lengths  of  the  walls,  its  removal  would  allow 
the  application  of  the  energy  of  the  turgid  parenchyma  to  the  flaccid 
epidermal  cells,  the  longitudinal  walls  of  which  then  would  respond 
readily  to  the  stretching  effort,  the  amount  of  stretching  depending 
only  on  the  physical  properties  of  the  walls.  In  a  word,  the  system 
would  work  like  a  bimetalhc  strip  of  metals  of  different  indices  of 
expansion,  von  Guttenberg's  idea,  but  demanding  simply  loss  of  tur- 
gor in  the  epidermis  only,  and  this,  as  von  Guttenberg  observes  in 
regard  to  Ziegenspeck's  theory,  is  easier  physiologically  than  a  rise 
in  turgor  in  a  mass  of  tissue.  It  should  be  added  that  the  loss  of 
turgor  by  the  epidermis  need  not  advance  beyond  an  initial  stage 
of  relaxation,  just  sufficient  to  allow,  without  evident  effusion  of  water, 
the  stretching  of  the  longer  walls,  which  would  otherwise  be  pushed 
out  laterally  by  conditions  of  turgor.  Thus  the  theoretical  neces- 
sities are  reduced  to  a  minimum,  and  the  movement  of  Dionaea 
brought  into  fine  with  movements  in  general  in  sensitive  plants. 
As  to  the  bursting  of  fruits  such  as  Impatiens,  Sicyos,  etc.  we  have 
to  do  with  change  of  shape  of  parenchyma  cells  without  change  in 
turgor.     In  Impatiens  the  two  epiderms  are  of  unequal  extensibility. 

This  seems  to  be  the  view  advanced  by  Ashida  (1934)  which, 
prompted  by  his  study  of  Aldrovanda,  he  applies  "by  deduction  to 
the  case  of  Dionaea."  He  cites  Macfarlane's  observations  that 
the  lower  epidermis  has  a  thinner  cuticle  than  the  upper,  and  is  there- 
fore more  easily  distensible,  permitting  curvature  on  the  relaxation  of 
the  upper  epidermis  with  the  effect  of  closure. 


Chapter  XII  — 193  —  Dionaea  and  Aldrovanda 

What  is  the  nature  of  stimulation  is  certainly  not  known.  Haber- 
LANDT  regarded  the  constricted  cells  at  the  base  of  a  sensitive  hair 
as  sense  organs  which  are  activated  by  compression.  Brown  found 
that  the  sensitive  hairs  do  not  respond  to  decompression  procured 
by  two  successive  movements  of  a  hair  which  had  previously  been 
kept  in  an  extreme  bent  position.  Propagation  of  the  stimulus  cannot 
be  dependent  upon  the  vascular  tissues,  since  they  are  absent  from 
the  trigger  hairs;  and  in  Aldrovanda,  which  has  no  vascular  tissues 
except  the  single  strand  along  the  midvein,  it  is  even  more  obvious  that 
the  path  of  movement  must  be  found  in  the  parenchyma,  but  whether 
of  the  epidermis  alone  or  of  the  internal  tissues  also,  is  not  yet  known. 

That  response,  an  event  following  on  stimulation,  is  accompanied 
by  electrical  disturbances  Burdon-Sanderson  showed,  and  the  char- 
acter of  these  permitted  him  to  Hken  them  to  those  which  occur 
during  muscular  contraction,  though  this  is  not  the  same  as  iden- 
tifying the  contraction,  asserted  by  Darwin  and  Batalin,  of  the 
upper  surface  with  muscular  contraction  (F.  Darwin,  1875),  espe- 
cially when  now  such  contraction  has  been  questioned  (Broavn). 
The  molecular  transposition  measured  by  Burdon-Sanderson  might 
indeed  be  the  expression  of  sap  movements,  and  such  sap  movements 
need  not  be  great  quantitatively  to  upset  an  equilibrium  and  might 
constitute  a  trigger  action  to  start  the  mechanism  a-going. 

Whatever  the  tensions  in  the  open  trap  lobe  may  be,  they  must 
be  duplicated  in  the  similar  trap  of  Aldrovanda,  and  when  we  look 
at  this  beyond,  it  is  a  help  to  comprehend  what  happens  in  Dionaea 
when  such  tensions  are  reUeved. 

For  Dionaea  we  may  at  present  say:  — 

i)  During  the  open  condition  there  are  tensions  present  which 
are  so  distributed  that  they  maintain  the  trap  in  an  open  position, 
the  lobes  standing  at  an  angle  as  great  as  80  deg.  (Darwin). 

2)  When  stimulated  the  lobes  close,  the  ciHa  becoming  interlaced 
like  the  fingers  of  clasped  hands.  The  lobes  remain  concavo-convex, 
inclosing  a  wide  space  between  them.  During  this  closure  the  outer 
face  of  the  lobe  expands,  the  inner  remains  unaltered,  or  at  least 
it  does  not  contract.  If  the  stimulus  is  prolonged  by  chemical  stim- 
ulation (as  when  an  insect  has  been  introduced),  the  lobes  continue 
toward  a  greater  mutual  compression  and  thus  obliterate  to  some 
measure  the  inclosed  space  (the  "narrowing"  of  Ashida).  Batalin 
thought  that  this  is  due  to  a  subsequent  contraction  of  the  lower 
face  of  this  lobe.  It  might  be  due  to  a  passive  extension  of  the  upper 
face  resulting  from  rapid  exudation  of  secretion,  depleting  the  tissues 
of  water.  The  edges  of  the  lobes,  which  do  not  actively  participate 
in  the  movements,  become  bent  outwards  and  the  cilia  now  extend 
less  transversely,  so  that  the  two  sets  become  more  nearly  parallel. 

3)  With  the  cessation  of  secretion  and  absorption,  the  lobes  re- 
open, this  being  the  result  of  increased  growth  of  the  upper  faces, 
the  expansion  of  the  lower  faces  being  maintained. 

The  mechanically  stimulated  trap  closes,  and  reopens  without  nar- 
rowing in  about  24  hours,  when  it  will  respond  again.  But  repeated 
daily  responses  are  followed  by  decreasing  sensitivity,  probably  due  to 
the  completion  of  growth. 


Francis  E.  Lloyd  —  194  —  Carnivorous  Plants 

If  closure  follows  trapping  of  suitable  prey,  narrowing  (in  the 
sense  of  Ashida)  takes  place.  Reopening  follows  at  the  end  of  a 
period  of  days  (5-10  or  more)  when  there  is  evident  a  diminution  of 
sensitivity,  which  however  is  regained  in  the  course  of  time  (some 
days,  OuDEMANs). 

Digestion.  —  During  all  this  digestion  and  absorption  have  been 
taking  place.  Darwin  did  a  variety  of  experiments  with  various 
substances.  We  have  seen  that  the  upper  surface  of  the  lobes  is 
crowded  with  many  glands  capable  of  secretion  and  absorption,  as 
Darwin  stated.  These  glands  remain  passive  unless  some  suitable 
material  (insect,  meat,  etc.)  is  inclosed  between  the  lobes.  Then 
there  is  a  copious  secretion  of  a  fluid  which  has  the  power  of  diges- 
tion, and  which  causes  the  dissolution  of  the  substances  acted  upon. 
"It  is  so  copious  that  on  one  occasion,  when  a  leaf  was  cut  open, 
on  which  a  small  cube  of  albumen  had  been  placed  48  hours  before, 
drops  rolled  off  the  leaf"  (Darwin).  The  secretion  is  acid,  the  pres- 
ence of  formic  acid  (Balfour)  serving  also  for  the  inhibition  of  bac- 
teria, so  that,  unless  too  great  ''portions"  have  been  supplied,  there 
is  no  odor  of  decay.  Balfour  found  that  a  strip  of  meat  placed  partly 
within  the  closed  valves  and  partly  out,  showed  no  bacterial  action 
within,  but  did  so  without.  When  the  rotted  portion  was  placed  in 
a  fresh  leaf,  the  odor  of  decay  disappeared.  This  contravened  the 
opinion  of  Rees  and  Will,  whose  experiment  seems  to  have  been  done 
with  abnormal  plants  (Goebel).  There  seems  therefore  to  be  no 
doubt  of  the  digestive  power  of  the  secretion,  though  no  in  vitro 
experiments  have  been  done  with  Dionaea  secretion.  According  to 
Darwin  some  substances  are  not  digested  (fats,  iibro-elastic  cartilage). 

If  not  too  great  masses  of  material  have  been  fed,  when  the  trap 
begins  to  open  the  interior  is  found  to  be  dry,  and  the  fluid  has  been 
entirely  absorbed.  Experiments  to  show  the  usefulness  of  the  ab- 
sorption of  proteins,  such  as  those  carried  out  by  various  authors  on 
Drosera,  Utricularia,  have  not  been  done.  Our  opinion  on  that  must 
therefore  rest  on  evident  analogy. 

Fraustadt  thought  that  during  the  period  when  the  trap  is  closed 
over  an  insect  photosynthesis  stops.  But  Pfeffer  (1877)  suggested 
that  the  lowering  of  the  starch  content  observed  by  Fraustadt  may 
be  the  accompaniment  of  a  change  in  metabolism  while  at  the  same 
time  photosynthesis  may  be  proceeding.  The  work  of  Kostytschew, 
if  meagre,  seems  to  deny  Fraustadt' s  belief  (see  under  Drosera, 
p.  119). 

Aldrovanda  vesiculosa  L. :  —  Aldrovanda  is  a  small  fresh  water  plant 
{ly  —  5)  growing  in  quiet  waters,  floating  just  below  the  surface. 
It  is  quite  rootless,  and  consists  of  a  slender  stem,  clothed  with  whorls 
of  leaves  not  distantly  separated.  Each  whorl  has  eight  leaves  mu- 
tually attached  at  their  bases.  It  branches  infrequently,  so  that  usu- 
ally one  finds  only  a  single  stem.  The  whole  plant  reaches  a  length 
of  10  to  15  cm.  with  a  width  of  2  cm.  including  the  spread  leaves 
which  are  refiexed  in  age.  The  tip  of  the  shoot  is  especially  con- 
spicuous by  the  numerous  bristles  which  jut  beyond  the  general  leaf 
profile.     The   flowers   are   supported   on   short   stalks,   bringing   them 


Chapter  XII  — 195  —  Dionaea  and  Aldrovanda 

just  beyond  the  extent  of  the  bristles.  They  measure  about  8  mm. 
when  widely  open.  The  seeds  are  ovate,  clothed  with  a  hard  shell 
(KORZSCHINSKI   1886). 

This  unique  plant  was  first  seen  in  India  and  was  cited  in  1696 
by  Plukenet  as  '' Lenticula  palustris  Indica"  in  his  Almagestum 
Botanicum  or  Phytographia  (4:  211,  pi.  41,  fig.  6).  In  1747  Gaetano 
Monti  had  received  a  collection  of  it  made  by  an  Italian  physician,  Dr. 
Carlo  Amadei,  in  the  DulioH  Swamp,  east  from  Bologna.  It  was 
named  Aldrovandia  by  Monti  in  honor  of  the  Italian  naturalist, 
Ulisse  Aldrovandi,  who  died  in  1605.  This  plant  was  identified 
by  J.  J.  Dillon  with  the  Plukenet  one  from  India.  In  1751  it  was 
mentioned  in  a  dissertation  by  L.  J.  Chenon  (1751),  a  student  of 
Linnaeus,  as  Aldrovanda  (probably  a  mistake  in  copying,  thinks 
DuvAL-Jou\TE,  1861)  and  finally  published  byLiNN.\EUS  in  the  Species 
Plantarum  1753,  p.  281,  as  Aldrovanda  vesiculosa. 

Caspary  points  out  on  high  philological  authority  that  the  Lin- 
naean  name  is  ungrammatical.  The  name  Aldrovanda  is  now  generally 
accepted  in  accordance  with  the  International  Rules  of  Botanical 
Nomenclature.  Another  plant  from  India  was  described  as  the  species 
verticillata  by  Roxburgh  {Flora  Indica  1832,  2:  p.  113),  but  this 
was  shown  by  T.  Thomson  not  to  be  distinct,  but  has  been  regarded 
as  a  variety.  A  plant  from  Queensland,  Australia,  once  called  the 
var.  auslralis,  is  not  distinguishable  from  the  original  species,  though 
Darwin  found  some  difference  in  size,  together  with  other  minor  ones, 
such  as  the  number  of  serrations  on  the  bristles. 

Aldrovanda  vesiculosa  ranges  from  S.  France  to  Japan,  south  to 
Austraha,  and  in  Africa  to  the  southern  tropics  where  it  was  found 
by  Miss  E.  L.  Stephens  in  the  Chobe  Swamp,  ico  miles  west  of 
Victoria  Falls.  This  material,  together  with  living  plants,  has  been 
studied  by  me,  the  latter  having  been  obtained  in  Silesia  and  grown 
during  the  summer  of  1933  in  the  Garden  of  the  Botanical  Institute 
of  Munich.  Beautiful  herbarium  specimens  in  all  stages  of  fruiting 
and  flowering  from  Mizoro  Pond,  near  Kyoto,  were  sent  me  by  Dr. 

JOJI  ASHIDA. 

The  morphology  and  anatomy  of  the  vegetative  parts  of  the 
plant  were  first  described  by  Cohn  in  1850,  and  more  completely 
by  Caspary  in  1859  and  1862.  Further  reference  to  details  was 
made  by  Goebel   (1891),  Fenner   (1904),  and  Haberlandt  (1901). 

Like  the  leaves  of  Dionaea,  those  of  Aldrovanda  consist  of  a  flat- 
tened petiole  armed  at  its  apex.  This  appears  somewhat  truncated, 
with  four  to  six,  or  seldom  even  eight  parenchymatous  lobe-Hke  bris- 
tles, surmounted  by  a  nearly  circular  leaf  blade,  4  mm.  wide.  When 
mature  the  petiole  is  wedge-shaped,  broader  at  the  apex,  6  mm.  long 
and  4  mm.  wide.  The  bristles  extend  another  5  mm.  The  midrib 
of  the  petiole  with  its  vascular  tissue  continues  into  the  blade,  which 
has  the  form  of  a  steel  trap,  as  in  Dionaea. 

Seedling  {ig  —  1-5).  —  The  elliptical  seed  has  a  snout  at  one  end, 
plugged  with  a  cap,  under  which  lies  the  root  end  of  the  short  hypo- 
cotyl.  Surmounting  this  are  the  two  broadly  conical  cotyledons 
pressing  against  the  large  endosperm,  much  as  in  Dionaea  (Smith). 
In  early  germination   the   hypocotyl  protrudes,   pushing  off  the   cap 


Francis  E.  Lloyd  —196— Carnivorous  Plants 

and  carrying  it  forward  for  some  time,  till  indeed  the  hypocotyl  reaches 
its  fullness  of  development,  with  a  length  of  3  mm.  (79  —  1-3).  By 
this  time  the  petioles  of  the  cotyledons  have  emerged,  and,  just  above 
the  plumule,  expand  to  form  a  sack-like  expansion  surrounding  it. 
Above  this  they  are  suddenly  constricted,  the  isthmus  entering  the 
seed  and  connecting  with  the  expanded  ends  of  the  cotyledons  which 
form  a  haustorium.  The  developing  plumule  breaks  out  of  one 
side  of  the  surrounding  cotyledonary  envelope  and  progresses  toward 
forming  the  plant.  The  leaves  of  the  first  whorl  are  slender  ligulate 
and  taper  to  a  fine  point,  or  may  be  variously  laciniate  to  some  de- 
gree. There  are  usually  five  in  the  whorl.  The  next  whorl,  raised 
on  an  evident  internode,  shows  still  more  laciniations,  but  does  not 
yet  produce  traps  (79-5).  These,  however,  usually  appear  in  the 
fourth  whorl.  Subsequently  the  mature  condition  is  gradually  estab- 
lished. The  hypocotyl  ends  without  forming  a  root  cap,  and  initial 
cells  appear  never  to  be  established  after  the  primary  condition  has 
passed  {iq  —  4).  This,  Korzschinski,  who  described  the  course  of 
germination,  did  not  see,  and  this  lack  was  indicated  by  Goebel. 
The  structure  of  the  seed  and  seedHng  in  its  primary  condition  is 
quite  similar  to  that  of  Dionaea,  as  described  by  Smith  (193 i),  dif- 
fering however  in  a  few  details,  notably  in  the  greater  expansion  of 
the  cotyledonary  petioles  to  embrace  the  plumule,  and  in  the  failure 
of  root  growth. 

The  leaf  of  maturity.  —  This  consists  of  a  wedge-shaped  petiole 
(regarded  by  Nitschke  as  the  leaf  base  {fide  Troll,  1939)  and  the  nar- 
row isthmus  between  it  and  the  trap  as  the  petiole,  a  view  now  re- 
garded as  untenable),  somewhat  truncated  at  the  apex,  where  it  bears 
four  to  six,  occasionally  more  (eight,  Caspary)  serrate  bristles,  and  at 
its  middle  point  a  leaf  blade  in  the  form  of  a  trap. 

When  four  bristles  only  are  present  they  appear  to  stand  two 
on  each  side  of  the  trap,  but  the  inner  two,  as  revealed  during  de- 
velopment, stand  somewhat  behind  the  insertion  of  the  trap,  and 
overlap  it  {19  —  6).  If  a  fifth  occurs,  this  quite  evidently  stands 
behind  the  trap,  and  therefore  does  not,  as  Caspary  noted,  arise  from 
the  end  of  the  petiole,  but  from  its  dorsal  surface.  The  bristles  cannot 
therefore  be  regarded  as  lobes  of  the  leaf,  as  Cohn  thought,  nor 
as  stipular  appendages  (Nitschke,  1861),  but  rather  as  emergences. 

The  structure  of  the  petiole  {19  —  9)  in  general  is  that  of  water 
plants;  there  are  wide  intercellular  chambers  of  pentagonal,  hexagonal 
(along  the  midrib),  or  elongated  form  (along  the  margins),  separated 
by  partitions  one  cell  thick.  Fenner,  who  has  more  than  anyone 
else  described  the  minutiae  of  the  plant's  structures  and  their  de- 
velopment, errs  in  showing  large  hexagonal  chambers  over  the  midrib, 
and  in  fact  the  figure  of  his  transverse  section  does  not  consist  with 
that  of  the  leaf  en  face,  the  former  being  correct.  The  epidermis  is 
scantily  clothed  with  two-armed  trichomes  {19 — 16),  standing  on 
two  very  short  stalk  cells  with  cutinized  walls,  these  in  turn  on  two 
epidermal  basal  cells.  The  arms  of  these  hairs  may  be  short  or,  es- 
pecially along  the  margins,  twice  as  long.  The  bristles  taper  grad- 
ually from  their  broader  bases  and  are  serrated  irregularly  by 
projecting  unicellular  trichomes,  ending  in  a  similar  spinous  one. 


Chapter  XII  — 197  —  Dionaea  and  Aldrovanda 

The  trap  stands  at  the  apex  of  the  petiole,  the  midrib,  carrying 
a  single  annular  vessel  with  an  ample  phloem,  being  continuous  from 
one   to   the   other.     But   it   always   stands   asymmetrically,    resulting 
from  a  twist  in  the  stalk,  in  such  a  manner  that  the  mutually  appressed 
lobes  in  the  young  trap  are   turned  with  their  free  margins  to   the 
left   (as  viewed  from  above)   through  an  angle  of  about  90  degrees. 
In  addition  to  this  torsion,  the  trap  is  bent  backwards  (i.e.,  to  the 
right  as  seen  from  above)  through  an  angle  of  30  to  40  degrees  (77  — 
5).     Monti  evidently  refers  to  this  posture  when  he  said,  "In  bar- 
bularum   medio    folliculus   oblique    appenditur."      It    is   thus   brought 
about  that,  when  the  traps  are  open,  their  openings  face  outwardly 
away  from  the  stem,  instead  of  tangentially.     The  course  of  devel- 
opment of  the  leaf  is  here  worth  a  glance   {ig  —  6).     In  its  earliest 
stage,   the  whole   leaf   consists  of   a  mere   conical  protuberance   from 
the  stem  apex.    Soon  it  becomes  apparent  that  the  basal  half  is  broad- 
ening to  form  the  fiat  petiole,  while   the  now  more   cyhndrical  end 
is  to  become  the  trap.     Very  soon  this  begins  to  show  torsion  which 
progresses   until,    when    the    leaf   is    approaching   maturity,    the    trap 
comes  to  lie  in  its  definitive  position.     In  the  meantime  the  bristles 
have  developed,  first  the  outer  followed  by  the  inner.     At  an  early 
stage  it  can  be  clearly  seen,  as  it  was  by  Caspary,  that  the  trap  and 
inner  bristles  do  not  he  in  the  same  plane.     In  maturity,  the  bristles 
project  much  beyond  the  trap  and  so  produce  the  bristly  appearance 
of  the  plant. 

The  position  of  the  mature  traps  resulting  from  torsion  and  bend- 
ing may  be  regarded  as  a  distinct  adaptation,  since  their  mouths, 
when  open,  are  all  placed  so  as  to  avoid  obstruction  from  neighboring 
leaves,  which  in  view  of  their  numbers  and  crowding,  is  obviously 
advantageous  for  the  easy  approach  of  prey. 

In  describing  the  action  of  the  trap,  whose  pecuharities  of  posture, 
much  less  pronounced  but  present  in  Dionaea,  have  just  been  de- 
scribed, a  special  terminology  is  required,  proposed  by  Ashida.  It 
is  clear  that  if  the  trap  is  twisted  90  degrees  to  the  left  (in  the  sense 
above  indicated)  the  one  side  or  lobe  of  the  trap  must  come  to  lie 
against  the  bristles  {ig  —  5).  This  Ashida  calls  the  bristle-side  lobe. 
The  other  lobe  is  the  free-side  lobe.  The  importance  of  this  distinc- 
tion lies  in  the  fact  that  both  lobes  are  concavo-convex  and  lie  dished 
the  one  into  the  other  (ig  —  7).  That  is,  the  outer  surface  of  the 
bristle-side  lobe  and  the  inner  surface  of  the  free-side  lobe  are  convex, 
the  other  two  concave.  Since  this  has  been  brought  about  in  the 
course  of  development,  the  two  lobes  acquire  a  different  set,  the 
effect  of  which  will  be  clear  when  the  action  of  the  trap  is  described. 
The  trap  has  a  unique  structure,  which  we  shall  now  describe. 
Morphologically  it  is  a  leaf  blade,  each  half  being  nearly  semi-circular, 
the  circle  being  subjected  to  some  degree  of  skewing.  Each,  of  course,  is 
attached  to  the  midrib,  which  is  the  thickest  portion.  Fenner, 
CzAjA  and  others  have  called  the  midrib  the  "hinge,"  but  as  the 
proximal  parts  of  the  lobes  do  not  move  at  any  time,  this  is  a  mis- 
nomer. It  is  true  that  textbook  figures  taken  from  earlier  authors 
would  indicate  the  contrary,  but  they  are  certainly  wrong,  as  Ashida 
has  clearly  shown. 


Francis  E.  Lloyd  —  198  —  Carnivorous  Plants 

Each  lobe,  when  the  trap  is  mature  and  is  in  the  set  posture 
(ready  to  catch  prey),  is  concavo-convex  from  within  out.  But  the 
curvatures  are  not  simple  spherical  ones.  It  will  be  seen  by  the  fig- 
ures herewith  that  two  oval  zonal  regions,  one  on  either  side  of  the 
midrib,  are  fiat  (ig  —  8,  21-23)  and  are  subject  only  to  slight  cur- 
vatures under  stress  during  the  closure  of  the  trap.  From  this  flat 
middle  region,  the  lobes  spread  with  a  maximum  curvature  along  the 
transverse  middle  line.  Here  the  curvature  is  much  like  that  of  the 
ribs  of  a  vessel  amidships.  This  is  the  principal  region  of  motion 
during  closure  (2,  ig  —  22-23).  The  next  region  is  one  of  compara- 
tively Httle  inward  curvature  (5,  19  —  23)  as  far  as  the  margin,  which 
is  sharply  bent  back  inwardly  to  form  a  valve  edged  with  a  row  of 
sharp  teeth.  The  whole  looks  hke  a  widely  opened  clam  or  mussel 
(ig  —  21a).  This  is  what  one  sees  looking  merely  at  the  outer  form. 
When  the  thickness  of  the  lobes  is  examined,  the  following  is  found. 
The  inner  half,  along  the  midrib,  is  thick  and  relatively  rigid.  This 
half  (the  thick  region)  includes  the  place  of  greatest  curvature,  to- 
gether with  a  measure  beyond  (again  as  seen  in  a  transverse  section 
normal  to  the  midrib  at  its  middle  point)  (1-3,  ig  —  23).  Anatom- 
ically it  consists  of  three  courses  of  cells,  the  two  slender  celled  epi- 
derms  which  are  thin,  enclosing  a  single  course  of  very  large 
thin-walled  cells,  the  long  axes  of  which  run  transversely  the  leaf 
(ig — 10,  11).  This  structure  is  continued  around  the  sharp  bend 
of  the  motile  region,  which  is  somewhat  thinner  than  elsewhere,  into 
the  sides  of  the  trap  somewhat  less  than  half-way  to  the  free  mar- 
gin. At  this  point  the  lobe  suddenly  thins,  the  middle  course  of  large 
cells  ceasing.  The  lobe  then  consists  of  a  very  thin  membrane  con- 
sisting of  only  the  two  epiderms  juxtaposed,  and  so  it  continues 
quite  to  the  inturned  margin  which  forms  the  valve.  The  valve 
itself  is  thicker  again,  due  to  the  enlargement  of  the  epidermal  cells, 
giving  it  a  useful  firmness  to  make  it  eftective.  Since  only  the  mid- 
dle transverse  structure  as  seen  in  section  has  been  examined,  some 
details  concerning  the  curvature  of  the  lobe  margins  must  be  men-' 
tioned. 

The  stiff  region  of  the  trap  wall  along  the  midrib  does  not  extend 
its  full  length,  so  that,  beyond  certain  points,  the  proximal  and  distal 
parts  of  the  walls  are  thin  and,  when  the  trap  is  closed,  readily  ap- 
proach each  other  so  as  to  lie  juxtaposed.  As  the  marginal  valve 
does  not  reach  the  midrib  —  it  becomes  narrower  as  it  approaches 
it  and  quite  ceases  0.75  mm.  away  —  there  are  left  two  spaces,  one 
at  the  apex  and  one  at  the  base  of  the  blade,  which,  when  the  trap 
is  closed,  can  allow  the  escape  of  water,  while  elsewhere  the  valve 
acts  to  prevent  the  escape  of  prey  during  the  whole  course  of  closure 
of  the  trap.  This  escape  of  water  is  necessary  to  permit  the  two 
thin  regions  of  the  lobes  to  approach  and  to  become  mutually  ap- 
pressed.  This  is  possible  because  the  thin  region  of  the  free-side 
lobe  inclines  to  bend  when  pressed  against  the  bristle-side  lobe, 
due  to  its  set  acquired  during  development,  so  that  when  the 
trap  is  fully  closed,  the  thin  regions  of  the  two  lobes  dish  into  one 
another  as  during  development  {ig  —  21,  22),  crowding  the  prey,  if 
caught,  into  the  digestion  cavity.     Before  the  act  of  closure  is  looked 


Chapter  XII  — 199  —  Dionaea  and  Aldrovanda 

into  more  carefully,  further  details  of  anatomy  will  be  examined. 
The  thick  region,  as  above  said,  is  composed  of  three  cell  layers,  the 
two  thin  epiderms  sandwiching  a  middle  course  of  large  thin-walled 
cells  of  cyhndrical  form.  In  these  three  courses  the  cells  are  elon- 
gated at  right  angles  to  the  midrib,  and  have  straight  walls,  excepting 
that  the  outer  epidermis  beyond  the  motile  zone,  to  be  delimited 
later,  has  wavy-walled  cells.  In  passing  over  into  the  thin  region 
of  the  lobe,  the  middle  course  of  cells  ceases  entirely,  so  that  there 
remain  only  the  two  epiderms  juxtaposed  {ig — 19).  In  the  inner 
zone  of  this  region  the  cells  are  elongated  and  have  straight  walls, 
but  there  is  a  gradual  transition  to  irregularity,  when  the  walls  be- 
come wavy.  The  thinnest  part  of  the  valve  is  toward  the  outer 
edge,  where  it  is  reduced  to  0.5  mm.  and  is  here  only  one  cell  in 
thickness.  This  is  accounted  for  by  the  fact  that,  as  Cohn  and 
Caspary  observed,  the  cells  of  the  two  epiderms  become  mutually  in- 
tercalated, the  cells  of  the  inner  course  protruding  between  those  of  the 
outer  course  to  occupy  part  of  the  general  outer  surface  and  vice  versa 
{ig  —  12,  13,  17).  The  margin  of  the  thin  region  is  reflexed  to  form 
the  valve  and  has  a  greater  thickness,  namely  about  i  mm.  Along 
the  edge  of  the  valve  stands  a  row  of  sharp,  stiff,  unicellular  hairs 
which,  when  the  trap  is  closed,  intercross  to  prevent  any  escape 
of  prey  between  the  valves  (Cohn)  {ig  —  18),  recalling  the  analogous 
arrangement  in  Dionaea,  but  in  a  reverse  sense.  This  the  trichomes 
accomplish  more  by  numbers  than  by  strength,  which  is  indeed  not 
great,  as  Darwin  observed.  His  doubt  on  the  usefulness  of  the  de- 
vice is,  however,  scarcely  justified. 

The  cells  of  the  two  epiderms  of  the  thick  regions  differ  in  size. 
The  outer  epidermis  per  unit  of  measurement  is  composed  of  more 
and  therefore  more  slender  cells,  than  the  inner,  in  the  ratio  of  about 
7:5.  The  cells  of  the  middle  course  are  longest  near  but  not  next 
the  midrib.     The  structure  of  this  is  seen  in  ig  —  10,  11,  23. 

The  inner  and  outer  surfaces  of  the  trap  are  supplied  with  a  variety 
of  trichomes  with  various  functions.  On  the  outer  surface  there  are 
squat,  two-armed  hairs  {ig — 16)  similar  to  those  found  over  the 
general  plant  surface.  Their  capital  cells  are  devoid  of  cuticle,  and 
they  secrete  mucilage.  On  the  inner  face  of  the  lobes  are  to  be  found 
three  kinds  of  hairs.  On  the  surface  of  the  distal  zone  of  the  thin 
portion  there  are  four-armed  hairs  resembling  superficially  the  "quad- 
rifid  hairs"  (so  called  by  Darwin)  in  the  interior  of  the  traps  of  many 
species  of  Utricularia  {ig —  15).  Aside  from  having  four  arms,  which 
lie  prostrate  against  the  surface  of  the  leaf,  they  are  otherwise  of 
the  same  structure  as  the  two-armed  hairs,  and  like  them  are  devoid 
of  cuticle,  and  secrete  mucilage  (Goebel).  They  are  distributed  in 
a  broad  zone  lying  adjacent  to  the  valve  (ig — ^8).  The  innermore 
region  is  devoid  of  them.  On  the  inner  surface  of  the  thicker  region 
of  the  lobe  occur  bun-shaped  glands  which  may  be  regarded  as  di- 
gestive and  absorptive  in  function  {ig  —  14).  They  arise  from  two 
(Fenner)  epidermal  cells,  on  which  stands  a  short  stalk  of  four  cells 
which  expand  into  balloon  shaped  upper  ends,  clothed  with  a  dozen 
or  more  cells  to  form  the  capital.  They  too  lie  in  a  zone  of  much 
density  toward  the   outer  margin   of  the   thick   region,   and  are  few 


Francis  E.  Lloyd  —  200  —  Carnivorous  Plants 

and  more  scattered  nearer  the  midrib,  on  which,  however,  there  is  a 
dense  row  of  them.  Darwin  regarded  the  "quadrifid"  or  cruciform 
hairs  within  the  trap  as  absorptive,  but  Duval-Jouve  (1876),  because 
of  their  occurrence  on  the  outer  surfaces  of  the  petiole,  etc.,  considered 
them  as  of  identical  nature  with  the  latter. 

In  this  region,  to  which,  thought  Mori  (1876),  irritability  was  con- 
fined, there  are  also  about  40  (20  on  each  lobe)  long,  very  slender  hairs, 
described  by  Goebel,  Haberlandt  and  Fenner,  analogous  to  the 
normally  six  sensitive  bristles  which  occur  on  the  lobes  of  the  Dionaea 
trap.  In  Aldrovanda,  however,  they  are  of  a  much  simpler  though 
equally  effective  structure.  They  are  about  1.3  to  1.5  mm.  long  and 
0.05  mm.  thick  except  at  the  base,  where  they  are  a  bit  wider.  ^  They 
are  very  slender  shafts,  arising  from  a  four-celled  base  lying  in  the 
epiderm,  and  projecting  slightly  therefrom.  On  these  is  surmounted  a 
length  of  two  courses,  each  of  four  long,  slender  cells.  These  bear  the 
super-sensitive  cells,  four  in  number,  though  sometimes  there  appear  to 
be  only  two.  Haberlandt  does  not  state  the  number.  They  are 
short,  thin-walled  and  form  a  sort  of  joint  or  hinge  where  the  otherwise 
stiff  hair  can  bend  sharply,  thereby  compressing  the  cells  on  the  con- 
cave side  (Goebel,  1891).  Above  there  are  two  courses  of  slender  cells 
of  two  each,  gradually  tapering  to  a  sharp,  sometimes  forked,  end 
(ig  —  20).  They  are  arranged  and  postured  in  such  fashion  that, 
contrary  to  the  impression  given  by  some  authors,  they  are  not  bent  on 
the  closure  of  the  trap.  They  stand  upright  on  the  flat  region  of  the 
trap  on  either  side  of  the  midrib,  where  they  have  plenty  of  head-room 
when  the  trap  is  fully  closed,  but  obliquely  on  the  sides  so  that,  though 
long  enough  to  reach  beyond  the  fully  closed  digestion  chamber,  they 
lie  sandwiched  between  the  thin  regions  when  approximated  without 
being  bent.  Disturbing  these  hairs  results  in  the  closure  of  the  trap, 
one  touch  of  a  bristle  of  a  young  leaf  sufficing,  but  as  the  leaf  grows 
older  two  or  even  many  more  become  necessary.  Quite  old  leaves, 
appearing  at  first  to  be  beyond  response,  showed  action  when  a  lot  of 
the  sensitive  hairs  were  disturbed  by  a  sweeping  motion  of  a  needle  a 
considerable  number  of  times. 

But  though  I  did  300  experiments  I  found  it  diihcult  to  make  a 
very  definite  rule.  There  is  a  good  deal  of  difficulty,  of  course,  in 
getting  a  clear-cut  result  when  one  is  dealing  with  so  small  an  object 
as  the  Aldrovanda  trap  which  has  so  many  deHcate  bristles  close  to- 
gether. In  cases  where  the  results  were  quite  clear-cut,  the  data 
were  contradictory.  Thus  in  one  case  a  young  trap  responded  to 
one  touch  of  a  single  hair  while  another  one,  of  similar  age  and  ap- 
parently ready  for  action,  being  widely  open,  required  seven  stimuh 
appKed  to  a  single  bristle.  Another  required  even  more,  caused  by 
a  sweeping  of  a  number  of  hairs  after  six  single  stimuH.  In  some- 
what older  leaves,  two  stimuh  only  were  frequently  required  to  effect 
closure,  but  this  also  was  by  no  means  constant.  Older  traps  behaved 
often  in  a  singularly  refractive  fashion,  but  yet  were  found  to  respond 
at  last.  One  case  only:  a  single  inner  (on  the  fiat  region)  bristle 
was  bent  10  times;  a  second  was  bent  10  times;  several  bristles 
were  then  bent  by  a  sweeping  motion  10  times;  then  several  outer 
bristles  were  swept  ten  times,  and  finally  a  single  inner  bristle  was 


Chapter  XII  —  201  —  Dionaea  and  Aldrovanda 

bent  twice,  followed  by  the  closure  of  the  trap.  On  the  other  hand 
an  old  trap  closed  with  one  stimulus  only,  seen  by  Dr.  E.  Merl 
and  myself,  as  we  were  working  jointly  at  the  time.  Another  dis- 
tinctly old  trap  responded  to  the  eleventh  stimulus,  ten  on  one  hair, 
the  eleventh  on  another.  Many  did  not  respond  at  all.  Ashida 
made  quite  similar  observations.  De  Lassus  (i86i)  had  already 
observed  that  young  traps  are  somewhat  more  sensitive  than  older 
ones.  It  became  apparent  that  this  lack  of  uniformity,  while  a  fact, 
does  not  mean  lack  of  dependability  of  the  trap  in  nature,  since 
the  prey  which  ventures  into  an  open  trap  must  needs  stimulate 
many  hairs  many  times  if  it  moves  about.  If  the  trap  closes  par- 
tially (see  below)  so  that  the  prey  cannot  escape,  the  continued  move- 
ments insure  a  further  stimulation,   and  complete  closure  is  assured. 

The  mode  and  mechanics  of  closure  may  now  claim  our  attention. 
We  have  seen  that  each  lobe  displays  two  concentric  regions,  an  inner 
thicker,  and  an  outer  very  thin  and  pliable,  and  edged  with  a  valve. 
If  a  relatively  weak  stimulus  is  applied,  the  lobes  close  till  their 
free  edges  meet.  Unless  additional  stimulus  is  added,  in  the  course 
of  a  short  time  (20  to  30  min.)  the  lobes  begin  to  open,  and  shortly 
resume  their  original  postures,  at  some  45  or  50  degrees  from  each 
other.  If,  however,  a  sufificiently  strong  stimulus,  or  repeated  stimuli 
be  used,  the  lobes  continue  to  close  still  further.  This  is  possible 
because  the  free-side  lobe  flexes  under  pressure  against  the  bristle- 
side  lobe,  at  first  just  inside  the  valvular  edge,  the  flexure  extending 
until  most  of  the  two  regions  are  mutually  appressed  {ig — 21). 
The  two  marginal  valves  become  bent  under  this  mutual  pressure, 
the  teeth  intercrossing  so  as  to  prevent  prey  from  escaping  when 
the  lobes  are  first  closed.  Resulting  from  the  whole  movement,  the 
thick  regions  have  moved  together  and  a  space  has  been  inclosed  by 
the  meeting  of  their  outer  Hmits,  forming  a  smaller  but  more  ines- 
capable prison  {ig  —  22).  Here  the  digestive  glands  begin  their 
work  of  digestion,  and  in  the  course  of  time  the  prey  is  disintegrated 
and  the  products  absorbed.  If  a  plant  is  Hfted  out  of  the  water, 
the  water  films  stimulate  the  traps  to  closure,  and  in  closing,  air 
is  entrapped.  The  idea  that  the  traps  were  hollow,  closed  organs, 
held  by  Monti,  led  him  to  use  the  descriptive  name  ''vesiculosa.''' 
CoHN  (1850)  and  de  Lassus  (1861)  found  this  to  be  a  mistake. 

The  mechanism  of  movement.  —  The  sensitivity  of  the  trap  was 
first  observed  by  Auge  de  Lassus,  who  was  cognizant  of  the  facts 
regarding  Dionaea  and  Drosera  in  1861.  The  fact  was  rediscovered 
by  B.  Stein  in  1873  (mentioned  by  Cohn  in  1875)  who  found  that 
it  is  the  slender  hairs  which  are  capable  of  receiving  stimulus,  and 
recognized  the  analogy  in  this  detail  with  Dionaea.  Additional  con- 
firmation was  offered  by  Mori  (1876).  Goebel  showed  more  com- 
pletely this  analogy  by  demonstrating  the  hinge  of  the  sensitive 
hair.  Czaja  (1924)  studied  the  effect  of  various  kinds  of  stimula- 
tion. He  incorrectly  regarded  the  midvein  as  a  hinge  about  which 
the  valves  rotate  to  approach  each  other  in  closure. 

It  has  remained  for  Joji  Ashida  to  make  a  studious  attempt  to 
elucidate  the  mechanism  of  response,  following  that  of  Brown  and 
Sharp   for  Dionaea.     Ashida   first   made   clear   where   the   exact   re- 


Francis  E.  Lloyd  —  202  —  Carnivorous  Plants 

gion  of  active  bending  is.  To  determine  this,  he  devised  a  method 
of  imbedding  the  open  trap  in  agar  jelly,  transferring  it  from  warm 
water  to  still  fluid  agar  at  the  same  temperature,  low  enough  to  do 
no  harm.  On  setting,  the  agar  with  its  imbedded  trap  could  be  cut. 
It  was  noticed  that  on  cutting  the  leaf  it  would  react,  and  in  doing 
so,  it  would  withdraw  from  the  agar  on  the  outside,  so  indicating 
the  zone  of  maximum  bending.  This  was  found,  as  already  shown 
above,  to  be  in  the  flanks  of  the  thick  region,  between  the  flat  part 
next  the  midrib  and  the  outer  rib-like  region  (2,  ig  —  23).  How 
is  this  movement  accomplished?  In  a  complete  response  the  amount 
of  movement  is  sufficient  to  bring  the  edges  of  the  thick  regions 
in  mutual  apposition,  thus  inclosing  an  ellipsoidal  shut-off  space. 
Meanwhile,  as  already  said,  the  thin  regions  dish  the  one  into  the 
other  as  the  result  of  mutual  pressure  brought  about  by  the  thick 
regions. 

Precisely  what  happens  to  procure  the  bending  is  more  obscure. 
An  observation  made  by  Ashida  is,  if  substantiated,  of  prime  im- 
portance. It  is  that  the  outer  epidermis  of  the  motile  zone,  when 
in  the  state  of  open  rest,  is  undulated,  and  in  this  condition  not 
in  a  state  of  extension,  whereas  the  inner  epiderm  is,  if  not  fully  ex- 
tended, at  least  more  so  than  the  outer,  since  very  hght,  if  any,  un- 
dulation is  to  be  seen.  During  closure  the  undulations  disappear, 
due  to  stretching  of  the  tissues.  As  I  have  already  suggested  (1933), 
the  two  epiderms  act  after  the  fashion  of  a  bi-metallic  spring.  As- 
suming this  to  be  the  case,  two  questions  arise.  What  condition 
of  the  tissues  operates  to  keep  the  outer  epidermis  lax?  And  what 
happens  to  procure  the  changes  from  the  lax  to  the  taut  condition? 

In  addition  to  this  undulation  of  the  outer  epidermis,  the  motile 
region  is  thinner  than  the  non-motile  parts  of  the  thick  region.  And 
if  the  opposing  lobes  are  cut  away  so  as  to  exclude  their  mutual 
pressure  during  closure,  it  is  ascertained  that  the  lobes  can  curve 
far  more  than  they  do  otherwise,  as  is  the  case  in  Dionaea;  and  fur- 
ther, that  the  free-side  lobe  bends,  during  closure,  more  than  the 
bristle-side  lobe.  Ashida  has  also  demonstrated  to  his  own  satis- 
faction that  the  outer  epidermal  walls  are  the  more  easily  extensible, 
the  outer  subepidermal  walls  less  easily,  while  the  two  inner  walls 
are  least  extensible.  This  conclusion  is  regarded  as  flowing  from  the 
observation  that,  if  a  trap  is  plunged  in  acetone  or  alcohol,  under 
the  internal  pressures  induced  by  the  entrance  of  these  fluids  into 
the  cells,  vesicles  arise,  but  only  on  the  outer  face  of  the  motile  zone. 
The  vesiculation  is  caused  by  the  rising  of  the  cuticle  and  the  breaking 
of  the  radial  walls  of  the  epidermis.  Evidently  the  outer  epidermal 
walls  are  readily  extensible,  but,  since  they  do  not  retract  when  the 
vesicles  are  reduced,  they  are  thrown  into  folds.  Ashida  argues  that 
the  walls  are  plastically,  not  elastically,  extended.  That  the  motile 
zone  is  weaker  than  the  lobe  is  elsewhere  was  shown  by  a  tearing  test, 
the  result  being  that  the  lobes  always  tear  at  the  motile  zone.  Again, 
from  observing  the  movements  of  the  intercellular  air  on  the  en- 
trance of  alcohol,  the  inference  was  drawn  that  the  walls  in  the  motile 
region  are  more  readily  penetrated  than  elsewhere. 

Before  discussing  the  mode  of  operation  of  the  motile  mechanism 


Chapter  XII  —  203  —  Dionaea  and  Aldrovanda 

in  Aldrovanda,  for  the  purposes  of  comparing  it  with  that  of  Dionaea 
(there  is  a  definite  analogy  between  them),  Ashida  draws  the  following 
parallel  between  them.  The  motile  zone  of  Aldrovanda  is  but  three 
cells  in  thickness;  that  of  Dionaea  composed  of  several  to  many  cells 
in  thickness,  according  to  age  of  plant. 

Aldrovanda  Dionaea 

The  outer  epidermis 
The  outer  epidermis  The  mass  of  parenchyma  beneath 

(either  one  or  both) 

The  middle  course  of  parenchyma  The  parenchyma  as  a  whole 

The  inner  epidermis 
The  inner  epidermis  The  parenchyma  beneath 

(either  one  or  both) 

The  actual  leaf  movement  embraces  two  phases  of  motion  which 
Ashida  calls  (a)  the  shutting  movement,  to  the  "shut"  stage,  when 
the  rims  of  the  lobes  just  meet;  {19  — 21b)  and  (b)  the  narrowing 
movement  leading  to  the  "narrowed  stage"  {ig  —  2id,  22).  In  re- 
covery the  opening  passes  through  the  "rebulging  movement"  from 
the  narrowed  stage  to  the  merely  shut  stage  and  the  reopening  move- 
ment, completing  the  opening.     To  avoid  confusion  these  terms  will 

be  used. 

In  the  shutting  movement  the  margins  of  the  thick  region  ap- 
proach sufficiently  to  bring  the  margins  of  the  thin  regions  together. 
This  follows  on  the  application  of  a  weak  stimulus,  but  proceeds  no 
further.  In  time  reopening  occurs.  If,  however,  the  stimulus  is  suf- 
ficiently strong,  this  posture  is  passed  through,  the  edges  of  the  thick 
region  approach  mutually  still  further,  the  thin  regions  press  on  each 
other  mutually,  and  the  free-side  lobe  buckles,  dishing  itself  in  against 
the  more  rigid  bristle-side  lobe.  Ashida  maintains  that  these  two 
movements  are  not  simply  a  continuation  the  one  of  the  other,  as  will 
be  seen. 

The  rapid  shutting  movement  is  caused  by  the  loss  of  turgor  by 
the  inner  epidermis.  This  allows  the  other  two  layers  to  expand  and 
the  curvature  ensues  mechanically.  The  membranes  of  the  outer  epi- 
dermis are  stretched  irreversibly.  The  undulations  described  by 
Ashida  disappear,  having  previously  been  maintained  by  the  outward 
pressure  of  the  inner  epidermis.  The  posture  thus  attained  now 
changes  to  that  of  the  narrowed  posture  by  the  narrowing  movement. 
This  is  a  slow  movement,  accomplished  by  the  slow  elongation  of 
the  outer  epidermal  cells,  that  is,  by  growth.  Resulting  is  the  mutual 
appression  of  the  two  thin  regions,  during  which  water  must  escape 
from  the  inclosed  space.  Ashida  tried  to  determine  by  means  of 
colored  fluid  where  the  water  escapes  but  did  not  get  any  very  convinc- 
ing evidence.  It  has  been  suggested  above  that  the  escape  is  between 
the  non-valvular  parts  of  the  lips  at  the  forward  and  rear  ends  of 
the  margins.  Ashida,  by  means  of  ingenious  optical  apparatus,  was 
able  to  record  photographically  the  advance  of  the  whole  movement. 
The  shutting  movement  is  very  rapid,  occupying  about  one  fiftieth  of 
a  second,  following  on  a  latent  period  of  0.09  seconds.  This  rapid 
movement  involves  the  expulsion  from  the  trap  of  water,  the  pres- 


Francis  E.  Lloyd  —  204  —  Carnivorous  Plants 

sure  of  which  must  be  overcome.  As  in  the  case  of  Utricularia,  the 
energy  expended  is  sufficient  to  cause  a  trap  lying  free  in  the  water 
to  close  with  a  sudden  jerk,  displacing  it,  just  as  a  Peclen  swims. 
There  seems  to  be  a  slight  difference  in  the  behavior  of  the  two  lobes, 
the  free-side  lobe  moving  a  bit  more  rapidly  than  the  other.  The 
difference  is  very  httle,  however. 

Advance  from  the  shut  to  the  narrowed  posture  is  slower,  more 
irregular,  complicated  by  conditions.  The  slowness  depends  in  the 
first  place  on  the  slowness  of  the  mechanism  causing  it,  namely  the 
absorption  of  water  and  extension  by  growth  of  the  outer  epidermis. 
It  seems  not  unlikely,  however,  that  closure  is  impeded  by  the  pre- 
vention of  the  escape  of  water  by  the  mutually  appressed  valves  of 
the  lobe  margins  and  the  probably  tight  appression  of  the  non- valvular 
portions.  This,  of  course,  insures  in  nature  the  retention  of  prey. 
To  test  this  point,  Ashida  made  a  hole  in  the  bristle-side  lobe  to 
allow  the  free  escape  of  water,  when  the  record  indicated  that  the 
inclosed  water  in  an  uninjured  trap  does  indeed  offer  impedance  to 
narrowing.  The  free-side  lobe,  however,  due  to  its  measurable  rigidity 
offers  resistance  to  buckling  and  by  itself  produces  irregularities  in 
the  rate  of  narrowing,  which  commences  in  any  event,  if  the  stim- 
ulus is  sufficient,  in  about  30  min.  after  the  shut  stage  has 
been  reached.  The  narrowed  condition  in  the  case  of  strong  stimu- 
lation, but  in  the  absence  of  prey,  is  maintained  for  a  period  of  from 
6  to  12  hours. 

In  the  return  to  the  widely  open  condition,  the  trap  passes  through 
the  reverse  of  the  two  phases  of  movement  seen  during  shutting  and 
narrowing,  that  is,  during  a  first  period  the  rebulging  of  the  free-side 
lobe  takes  place,  followed  by  the  reopening  of  both  lobes  when  the 
trap  is  again  ready  to  react  if  stimulation  is  applied.  All  this  is 
ascribed  to  the  growth  of  the  inner  epidermis.  During  its  progress 
irregularities  of  rate  of  movement  can  be  ascribed  to  the  resistance 
to  the  inflow  of  water  into  the  narrowed  trap  and  the  elastic  action 
of  the  thin  regions  added  to  the  action  proper  to  the  thick  regions. 
It  is  not  known  just  how  the  water  enters,  but  it  may  again  be  sug- 
gested that  the  valve-free  parts  of  the  lips  of  the  thin  regions  may  be 
the  place  of  entrance,  as  well  as  of  exit. 

To  recapitulate.  —  The  rapid  shutting  movement  is  caused  by  the 
response  of  the  inner  epidermis  of  the  thick  region  in  loss  of  turgidity. 
The  slow  narrowing  movement  is  brought  about  by  the  growth  of  the 
outer  epidermis,  following  its  stretching  in  the  curving  of  the  lobe. 
The  movements  of  recovery  are  due  to  the  growth  of  the  inner  epi- 
dermis, following  the  restoration  of  turgidity.  The  shutting  move- 
ment is  facihtated  by  the  circumstance  that  the  walls  of  the  outer 
epidermis  are  at  open  rest,  not  stretched  to  their  full  capacity,  and 
that  these  walls  can  be  stretched  plastically.  A  feature  peculiar  to 
Aldrovanda  is  the  fact  that  the  loss  of  turgor  by  the  inner  epidermis 
causes  curvature  of  the  single  large  celled  middle  layer,  the  walls 
attached  to  the  inner  epidermis  shrinking  and  those  to  the  outer 
expanding.  In  a  more  anatomically  complex  organ,  such  as  the  trap 
of  Dionaea,  the  same  must  be  true  of  all  the  parenchyma,  but  the 
difference    of   extension    between    the    outer   and   inner   walls   of   any 


Chapter  XII  —  205  —  Dionaea  and  Aldrovanda 

individual  cell  must  be  less,  since  the  total  difference  as  between  the 
inner  and  outer  epidermis  is  distributed  throughout  the  tissue  of,  it 
may  be,  some  dozen  cells  in  thickness.  It  is  quite  possible,  therefore, 
to  extend  the  explanation  given  above  for  Aldrovanda  to  Dionaea,  at 
the  same  time  excluding  the  loss  of  turgidity  from  the  parenchyma,  and 
refer  the  whole  movement  to  the  action  of  the  epidermis  alone.  This, 
of  course,  does  not  square  with  Brown's  explanation,  but  it  neverthe- 
less deserves  consideration. 

Reference  has  already  been  made  to  the  fact  of  sensitivity,  its 
seat  and  the  varying  response  of  leaves  of  various  ages.  We  inquire 
now  more  particularly  into  the  responses  to  various  types  of  agents, 
whether  stimulatory  or  otherwise.  Under  conditions  of  nature,  within 
the  ordinary  limits  of  temperature  during  the  growing  season,  it  has 
been  found  that  stimulation  through  pushing  against  the  sensitive 
hairs  by  animals,  such  as  water  fleas,  spiders,  etc.  of  small  size,  pro- 
cures closure  (shutting  and  narrowing).  The  trap  then  usually  has 
caught  a  small  total  amount  of  food  material  which  is  digested.  In 
the  course  of  a  few  days  (5-6,  Czaja  1924)  the  traps  reopen  and  are 
ready  to  act  again.  This  may  be  repeated  by  the  same  trap  several 
times,  the  number  depending  on  the  size  of  the  prey  caught  and 
the  amount  of  undigested  remains.  The  possible  activity  in  repeated 
response  and  reopening  is  certainly  not  so  limited  as  thought  by 
Fenner. 

If,  however,  the  prey  is  large  and  fills  the  digestion  cavity  (Czaja 
used  for  experiment  pieces  of  flatworm),  the  trap  may  never  open 
again.  This  may  be  due  to  the  time  involved,  so  that  the  trap  passes 
through  its  growth  period  and  loses  its  sensitivity,  or  the  production 
and  accumulation  of  substances  having  a  poisonous  effect.  Too  much 
feeding  is  known  to  have  a  deleterious  effect  in  other  carnivorous 
plants.  This  argues  little  or  nothing  in  regard  to  the  total  value  of 
the  process,  since  one  long  feeding  may  be  of  as  much  use  to  the 
plant  as  several  short  ones. 

The  observation  of  Burdon-Sanderson  on  Dionaea,  that  response 
can  be  obtained  by  electrical  stimulation,  was  the  beginning  of  a  num- 
ber of  studies  of  interest  in  the  field  of  general  plant  and  animal 
physiology,  leading  to  the  examination  of  various  agents  on  the  ac- 
tivity of  the  trap.  By  means  of  the  electric  current  it  has  been  pos- 
sible to  analyze  the  response  into  time  phases.  Czaja  determined 
the  intensity  of  threshold  stimuli  to  be  0.91  •  lo"*^  Coulomb  for  an 
opening  shock,  and  0.24-10"^  for  a  closing  shock.  By  repeated  ap- 
plication of  smaller  shocks  he  found  that  there  is  a  summation  of 
stimuli.  AsHroA  used  this  method  for  further  analysis  of  the  response, 
and  found  that  for  fully  opened  leaves  the  direction  in  which  the 
current  engages  the  trap  has  its  effect,  which  is  greater  when  applied 
transversely  than  longitudinally,  from  which  it  is  inferred  that  the 
stimulus  is  more  effective  when  running  parallel  to  the  long  cells  of 
the  motile  zone,  than  across,  and  that  the  latter  is  more  sensitive  to 
this  stimulus  than  are  the  sensitive  hairs  themselves.  This  may  be 
related  to  the  various  resistances  offered  by  the  tissues  concerned  and 
the  direction  of  the  current  through  the  individual  cells.  The  possi- 
bility of  controlling  the  intensity  of  stimulation  by  means  of  the  elec- 


Francis  E.  Lloyd  —  206  —  Carnivorous  Plants 

trie  shock  has  further  permitted  the  examination  of  the  behaviour  of 
the  trap  under  special  conditions  of  temperature. 

Within  the  permissible  temperature  limits  (extreme  temperatures, 
it  goes  without  saying,  are  finally  damaging)  Czaja  found  that  sensi- 
tivity increased  with  higher  temperatures,  as  determined  by  observa- 
tion between  15  to  35  deg.  C.  Raising  the  temperature  gradually  to 
45  deg.  was  followed  by  spontaneous  closure  of  nearly  all  the  traps 
(that  is,  excepting  some  of  the  oldest).  Opening  again  on  reduction 
of  temperature  to  20  deg.  they  again  closed  on  gradual  lowering  to 
10  deg.,  the  older  traps  responding  in  this  way  on  reducing  the  temper- 
ature further  to  5  deg.,  all  due  to  the  reduction  of  sensitivity,  as  shown 
by  appropriate  trials  (Czaja  1924). 

AsHiDA  went  further,  and  found  that  sudden  changes  of  tempera- 
ture (he  used  changes  of  10  deg.  C.)  in  either  direction  would  cause 
closure.  From  his  data  the  curious  fact  emerges  that  sudden  reduc- 
tion of  temperature  beginning  with  any  workable  levels  from  10  to 
40  deg.  C,  is  more  effective  than  sudden  rise  in  temperature  at  these 
levels.  Further,  the  higher  the  initial  level  of  temperature  the  more 
sensitive  is  the  trap  to  rises,  and  the  less  sensitive  to  drops.  Exam- 
ples of  stimulation  to  both  rise  and  fall  of  temperature  are  not  lacking, 
e.g.  changes  in  the  growth  rate  of  coleop tiles  (Silberschmidt),  nastic 
movements  of  leaves  (Stern  and  Bunning),  the  curhng  of  tendrils 
(MacDougal),  cited  by  Ashida,  offer  some  analogy.  Protoplasmic 
movement  is  retarded  only  by  a  fall  in  temperature,  the  Aldrovanda 
trap  being  stimulated  by  both  rise  and  fall,  but  more  by  the  latter. 
Aldrovanda  appeared  therefore  to  Ashida  to  be  unique  in  the  quantita- 
tive aspects  of  behavior  in  this  regard.  Metzner  (1920)  had,  however, 
already  shown  that  bipolar-flagellated  Spirillum  sp.  show  a  reversal  of 
movement  due  to  thermotaxis  both  on  increase  and  decrease  of  tem- 
perature. But  such  rises  and  falls  of  temperature  as  can  be  experi- 
mentally imposed  can  scarcely  be  expected  in  nature  except  as  slow 
changes;  they  can  hardly  be  regarded  as  affecting  appreciably  the 
general  economy  of  the  plant. 

In  a  third  paper  Ashida  has  given  the  results  of  studies  of  response 
of  Aldrovanda  traps  of  different  ages  to  weak  and  strong  stimulation 
applied  in  the  form  of  constant  currents  of  30.6  and  70.1  volts.  With 
the  strong  current  all  traps  of  various  ages  and  at  different  temper- 
atures (10  to  40  deg.)  close  promptly  in  the  same  time  interval.  With 
the  weak  current,  however,  the  responses  were  scattered,  a  frequency 
polygon  expressing  the  results  having  its  highest  node  at  about  the 
same  position  as  in  the  case  of  the  strong  current  stimulation,  with 
secondary  nodes  scattered  to  the  right  of  gradually  lessening  height. 
The  explanation  of  the  delayed  responses  lies,  Ashida  beheves,  in 
the  distinct  and  different  sensibility  of  the  hairs  and  the  motile  zone, 
diverse  excitability  of  different  cells  and  other  possible  causes. 

Responses  to  chemical  stimuli.  —  Both  Czaja  and  Ashida  have 
studied  the  behavior  of  Aldrovanda  to  a  series  of  chemical  agents: 
narcotics,  electrolytes  (acids,  alkalis,  salts),  non-electrolytes  (sugar, 
glycerine). 

Sugar,  glycerine.  —  It  is  difficult  because  of  the  impenetrable  cu- 
ticle to  plasmolyze  the  cells  of  the  trap  unless  a  cut  is  made  to  allow 


Chapter  XII  —  207  —  Dionaea  and  Aldrovanda 

the  approach  of  the  plasmolyte,  as  Czaja  also  found  for  Utricularia. 
At  the  most,  the  cells  display  a  systrophic  contraction,  but  there  is 
no  quantitative  relation  to  the  concentration  of  the  plasmolyte 
(Ashida).  By  watching  the  creeping  in  of  the  plasmolyte  through 
the  cut  ends  of  cells,  Czaja  estimated  the  osmotic  equivalent  to  be 
about  m/3  KNO3. 

A  plasmolyte  has  the  effect  of  immobilizing  the  trap  by  the  with- 
drawal of  water.  For  sugar  (sucrose)  immobilization  occurs  in  from 
40  seconds  to  7.5  minutes  for  solutions  of  the  concentrations  0.50  M. 
to  0.1 1  M.  according  to  the  age  of  the  leaf,  the  younger  being  more 
easily  affected.  They  react  on  stimulation  till  immobilization  sets 
in.  On  immersion  in  the  solution  (0.2  M.  sucrose),  the  trap  opens 
a  little  beyond  the  normal,  due  perhaps  to  the  withdrawal  of  water 
weakening  the  bending  force  of  the  outer  epidermis  and  the  middle 
layer.  The  springiness  of  the  walls  is,  however,  retained  to  some 
extent,  and  they  will  spring  open  if  closed  by  force,  unless  too  far. 
When  left  for  some  hours  (six)  in  a  0.15  M.  glycerine  solution  the 
power  of  movement  is  recovered,  due  perhaps  to  the  penetration 
of  the  solute  into  the  cells.  Rapid  changes  of  concentration  in  either 
direction  can  stimulate,  causing  partial  closure,  but  it  is  evident 
that  the  immobilising  effect  and  that  of  stimulation  are  antagonis- 
tic.    Only  traps  which  are  not  completely  immobilized  can  react  at 

all. 

Neutral  salts.  —  Czaja  found  only  a  "narcotizing  effect."  Ashdda, 
however,  found  also  that  salts  in  solution  can  stimulate,  for,  though 
strong  solutions  may  quickly  immobilize,  their  first  effect  is  stim- 
ulation and  the  traps  close.  Even  in  a  saturated  solution  of  KCl 
the  traps  reacted  within  1.6  to  2.6  seconds  according  to  the  age  of 
the  trap,  the  younger  the  quicker.  Similar  behavior  was  found  for 
some  other  salts. 

Acids  and  alkalis.  —  When  Ashida  exposed  traps  to  low  concen- 
trations of  acetic  acid  and  of  HCl  (0.005  to  0.05  N.)  they  closed  after 
various  rather  irregular  periods  from  29  to  2  minutes,  respectively. 
Since  osmotic  pressure  is  regarded  as  not  entering  in,  Ashida  tried 
combining  an  acid  with  a  non-electrolyte  (acetic  acid  with  sucrose) 
and  found  that  the  reaction  time  was  reduced,  and  that  the  more 
sucrose  is  present,  the  shorter  the  reaction  time.  Two  possible  ex- 
planations present  themselves.  Sucrose,  even  much  below  the  concen- 
tration which  can  stimulate  osmotically,  may  help  the  stimulating 
effect  of  the  acid,  an  additive  effect;  or  the  permeability  of  the  proto- 
plast to  acid  may  be  increased  during  partial  plasmolysis.  Ashida 
favors  the  latter  alternative,  for  the  additive  effect  is  not  observed 
in  young  traps,  in  which  osmotic  and  chemical  stimulation  alone 
procure  quicker  responses.  The  second  alternative  also  receives  support 
from  the  observations  of  Scarth  (1927)  that  acid  dyes  penetrate 
Spirogyra  cells  more  readily  when  the  protoplast  is  changing  its  vol- 
ume during  plasmolysis. 

Where  now  is  the  stimulus  perceived?  From  applying  acid  to  the 
different  leaf  surfaces,  Ashida  found  that  when  it  was  put  on  the 
upper  surface  the  response  was  obtained  more  quickly,  indicating 
that  the  joint  cells  of  the  sensitive  hairs  are  the  points  of  perception, 


Francis  E.  Lloyd  —  208  —  Carnivorous  Plants 

though  the  difficulty  of  confining  the  acid  to  the  hairs  alone,  which  is 
obvious,  throws  some  doubt  on  the  conclusion. 

Other  organic  substances:  —  When  exposed  to  commercial  for- 
malin, the  trap  becomes  immobilized  in  35-45  seconds.  During 
this  period,  if  stimulated  mechanically  the  traps  will  close.  In  some 
cases  the  traps  close  on  direct  stimulation  by  the  reagent  about  15-30 
seconds  after  immersion.  Because  overtaken  by  immobilization,  the 
closure  is  never  complete.  In  dilute  formalin,  the  closure  may  be 
complete,  since  immobilization  does  not  overtake  the  traps  quickly 
enough.  This  is  explained  by  the  toxic  effect  overtaking  the  epi- 
dermis cells  before  the  reagent  can  enter  by  way  of  the  sensitive 
hairs.  Ashida  also  reports  the  recovery  of  sensibility  in  20  minutes 
after  immobilization  by  exposure  to  concentrated  formalin  for  45  sec- 
onds, indicating  that  the  injury  to  the  epidermal  cells  is  to  some 
extent  reversible.  Such  traps  may  close  and  narrow,  perhaps  as  an 
after  effect  of  adherent  formalin  for  i  minute,  hence  completely  im- 
mobilized traps  close  and  narrow  in  water  5-10  minutes  later  in  spite 
of  complete  immobilization.  If  entirely  killed  by  longer  exposure,  no 
movement  occurs. 

Such  experiments  are  puzzling,  but  indicate  at  least  that  the 
toxic  effects  are  realized  somewhat  slowly,  and  that  the  stages  of 
turgor  reduction  realized  in  the  meantime  are  such  as  to  allow  the 
working  of  the  mechanism  of  closure,  partially  or  completely.  The 
slow  penetration  must  be  due  to  the  resistance  of  the  cuticle.  Ashida 
recognizes  two  effects,  stimulation  and  immobilization,  on  the  rate  of 
the  latter  depending  the  ability  to  respond,  through  the  action  of  the 
sensitive  hairs,  into  the  hinge  cells  of  which  the  reagent  can  penetrate 
more  quickly. 

In  ethylalcohol  10-40  percent  by  volume,  traps  close  spontane- 
ously in  from  about  i  to  90  minutes,  according  to  age.  Curiously 
enough,  in  solutions  stronger  than  40%  closure  occurs  in  two  steps, 
both  sudden,  separated  by  a  pause. 

In  saturated  chloroform-water,  most  traps  close  within  i  minute, 
some  quickly,  some  slowly  and  some  irregularly.  Restoration  to  water 
procures  no  further  activity,  and  they  die.  Czaja  had  previously 
obtained  similar  results.  He  found  also  that,  after  treatment  with 
ethyl  ether  at  similar  concentrations,  return  to  water  restored  the 
normal  activity.  The  effect  of  narcotics,  he  says,  is  at  first  stimulative, 
then  destructive.  He  obtained  similar  results  with  methyl  and  ethyl 
alcohols. 

The  addition  of  peptone  or  egg-albumin  to  the  culture  medium 
causes  the  traps  to  close  and  narrow,  as  also  if  a  fragment  of  fish 
or  meat  is  fed  to  the  trap.  Closure  follows  then  from  mechanical 
stimulation,  and  narrowing  results  from  the  chemical  stimulation. 
Gelatin  and  coagulated  egg-albumin  do  not  stimulate  beyond  the 
shutting  stage,  since  they  do  not  stimulate  chemically  (Ashida). 

Digestion  and  absorption.  —  There  is  not  much  doubt  that  Aldro- 
vanda  digests  prey  and  absorbs  the  products  of  digestion.  All  ob- 
servers have  seen  that  the  bodies  of  prey,  except  the  hard  parts, 
disappear,  and  Darwin  did  a  few  experiments  which  convinced  him 
that  absorption  takes  place.     The  evidence  is,  however,  not  complete, 


Chapter  XII  —  209  —  Dionaea  and  Aldrovanda 

and  we  base  our  opinion  with  Darwin  on  the  obvious  analogy  with 
Dionaea.  The  closure  of  the  trap  into  the  narrowed  posture  reduces 
the  volume  of  fluid  containing  the  digestive  ferment,  if  present,  thus 
rendering  it  more  effective  (Darwin).  Fermi  and  Buscaglione 
(1899)  offered  some  evidence  that  Aldrovanda  is  capable  of  digestion 
by  placing  traps  on  sterilized  gelatin,  and  finding  that  it  was  rendered 
fluid. 

To  the  earliest  observers  the  traps  of  Aldrovanda  were  thought 
to  be  vesicles.  The  lifting  of  the  plant  from  the  water  released  the 
traps  so  that  air  was  inclosed,  as  in  the  case  of  Utricularia,  but,  as 
CoHN  pointed  out,  this  air  was  purely  accidental.  That  it  enabled 
the  plant  to  float  in  the  water,  or  at  least  assist  in  this  when  the 
plant  becomes  loaded  with  prey  (Fenner),  in  view  of  the  fact  that 
it  floats  whether  air  is  present  in  the  trap  or  not,  was  seen  to  be  a 
gratuitous  explanation.  More  recently  Fenner  advanced  the  idea 
that  gas  is  present  as  the  result  of  chemical  activity  (digestion  of 
one  kind  or  another).  But  this  also  has  been  questioned  (Czaja 
1924).  That  the  presence  of  an  air  bubble  assists  in  digestion 
by  reducing  the  water  content  of  the  digestion  cavity,  thus  procuring 
a  more  concentrated  solution  of  ferments,  that  the  water  is  absorbed 
by  the  epidermis  cells,  and  that  the  air  bubbles  assist  in  opening  by 
outward  pressure  (Fenner),  are  ideas  which  are  superfluous  in  view 
of  the  fact  that  adequate  observation  shows  that  the  inclusion  of 
air  is  accidental.  Fenner  reports  also  that  in  vigorous  leaves,  after 
the  capture  of  prey,  not  only  do  the  digestive  glands,  but  also  the 
valve  trichomes  and  the  quadrifid  hairs  show  signs  of  activity  by 
exhibiting  changes  in  their  contents.  This  requires  further  exami- 
nation. It  is  true  that  Darwin  had  made  similar  observations  indicat- 
ing, it  seemed  to  him,  that  the  valve  teeth  and  quadrifids  do  absorb, 
but  this  evidence  was  regarded  only  as  indicatory. 

When  small  prey  are  captured,  the  trap,  stimulated  by  the  vigorous 
movements  in  the  attempt  of  the  prey  to  escape,  remains  closed  for 
some  time  according  to  the  mass  of  the  substance  to  be  digested. 
If  the  trap  is  overfed,  as  when  supplied  with  large  pieces  of  a  flat- 
worm  (Czaja)  it  remains  permanently  closed,  possibly  because  poi- 
soned by  the  overplus  of  deleterious  products,  or  perhaps  because 
growth  had  ceased.  Reopening  may  be  repeated  several  times  under 
favorable  conditions  of  sufficiently  meagre  feeding.  As  already  said 
heavy  feeding  may,  however,  advantage  the  plant  as  much  as  several 
smaller  feedings. 

According  to  Schenk  (on  the  authority  of  Cramer,  1877)  Al- 
drovanda was  grown  by  him  for  two  years  in  an  inorganic  salt  solu- 
tion without,  apparently,  any  deleterious  effect.  Pfeffer  cites  this 
in  support  of  the  non-obhgate  character  of  carnivory  in  this  plant. 
This  experience  of  Schenk's  is  surprising  in  the  light  of  the  expe- 
riences of  AsHiDA,  who  found  it  very  difficult  to  grow  the  plant  ex- 
cept under  rather  special  conditions.  "No  inorganic  culture  medium 
could  be  found  which  would  keep  the  plant  in  the  normal  form  even 
for  a  week".  Aldrovanda  grows  in  shallow  water  between  the  stems 
of  Typha,  Zizania,  Phragmiles,  etc.,  which  Hausleutner  regarded  as 
merely  protection  against  sun  and  wind.     Asheda  took  a  hint  from 


Francis  E.  Lloyd  —  210  —  Carnivorous  Plants 

these  relations,  and  found  that  by  introducing  into  the  water  re- 
mains of  the  associated  plants  mentioned  above,  Aldrovanda  can  be 
made  to  grow  quite  satisfactorily  even  to  flowering  and  seeding. 

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Chapter  XII  —  211  —  Dionaea  and  Aldrovanda 

Knight  of  the  Polar  Star,  Physician  to  the  King  of  Sweden,  and  Member  of  most  of 

the  learned  societies  of  Europe,  from  John  Ellis,  Fellow  of  the  Royal  Societies  of 

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Francis  E.  Lloyd  —  212  —  Carnivorous  Plants 

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Stein,  B.,  1873.    Mentioned  by  Cohn,  1875,  p.  73. 
Stern,  K.  &  E.  Bunning,  Uber  die  tagesperiodischen  Bewegungen  der  Primarblatter  von 

Phaseolus  viultiflorus,  I.   Der  Einfluss  der  Temperatur  auf  die  Bewegung.      Ber.  d.  d. 

Bot.  Gesell.  47:565-584,  1929  {through  Ashida). 
Thomson,  T.  and  J.  D.  Hooker,  Praecursores  ad   Floram   Indicam.     Journ.    Proc.   Linn. 

Soc.  Bot.  London.  2 :83,  1858. 
Troll,  1939.    See  under  Nepenthes. 

Young,  Wm.,  Catalogue  des  Arbres,  etc.,  d'Amerique.     1783,  p.  34  (n.v.  through  Coker). 
Ziegenspeck,   H.,   tJber   Zwischenproducte   des   Aufbaues    von   Kohlenhydrat-zellwanden 

und  deren  mechanische  Eigenschaften.     Bot.  Arch.  9:297-376,   1925   {n.v.,  through  v. 

Guttenberg,  1926). 


Chapter  XIII 
UTRICULARIA,    BIOVULARIA   AND    POLYPOMPHOLYX 

Form,  habit  and  habitat.  —  Distribution.  —  Embryology.  —  The  various  types  ar- 
ranged according  to  the  character  of  their  traps.  — The  vulgaris  type  (Freely  floating 
forms.  Semi-submersed,  submersed  but  anchored  forms.  Terrestrial  and  epiphytic  forms). 
—  Biovularia,  a  floating  type.  —  The  purpurea  type,  a  floating  form.  —  The  dichotoma- 
monanthos  type  (Floating  form.  Terrestrial.  Polypompholyx:  annual,  monaxial). — The 
cornuta  type.  —  The  caerulea  type.  —  The  capensis  type.  —  The  orbiculata  type.  —  The 
longiciliata  type.  —  The  globulariaefolia  type.  —  The  nana  type.  —  The  Lloydii  type.  — 
The  Kirkii  type.  —  The  simplex  type. 

Of  the  Lentibulariaceae  there  are  recognized  by  Kamienski  five 
genera,  Pinguicula,  Genlisea,  Polypompholyx,  Utricularia  and  Bio- 
vularia. The  first  two,  Pinguicula  and  Genlisea  have  already  been 
considered.  It  now  remains  to  treat  Utricularia,  Polypompholyx  and 
Biovularia.  These  plants  are  freely  floating  or  anchored  aquatics,  or 
are  epiphytic,  in  wet  moss,  or  are  terrestrial  in  wet  to  moist  sandy 
soils.  The  largest  of  these  are  among  the  aquatic  and  epiphytic 
forms.  The  former  are  well  exemplified  by  U.  vulgaris,  among  the 
best  known,  which  is  a  lax  floating  plant  of  several  feet  in  extent, 
but  of  little  mass.  The  epiphytic  U.  reniformis  is  more  massive 
and  makes  a  brave  showing  as  a  greenhouse  plant,  frequently  found 
in  the  good  company  of  the  orchids  because  of  the  similar  habitat 
requirements  and  the  showiness  of  their  flowers.  It  is  indigenous  in 
Brazil.  One  species,  U.  nelumbifolia,  finds  its  home  habitually  in  the 
water-containing  leaf  rosettes  of  large  Tillandsias,  whence  it  sends 
out  runners  which  reach  into  the  urns  of  neighboring  rosettes 
(Gardner  1842,  Ule  1898).  Showy  species  are  U.  Humholdtii,  U. 
longifolia  (both  S.  America),  U.  Endresii  (Costa  Rica)  and  the  related 
U.  Dusenii  which,  though  small,  has  a  flower  of  the  same  type.  Other 
of  the  larger  species  are  the  tropical  American  terrestrial  U.  globu- 
lariaefolia and  amethystina  (Trinidad),  and  a  few  others  chiefly  no- 
ticeable because  of  their  tall  inflorescences.  But  among  the  aquatics 
are  found  also  the  smallest  species,  as  e.g.  U.  cymbantha  (Africa)  and 
a  related  unnamed  species  of  still  smaller  size,  the  flower  being  only 
2  mm.  long,  and  the  stolons  mere  threads,  collected  by  Miss  E.  L. 
Stephens  in  Portuguese  East  Africa.  As  small  are  the  two  species  re- 
ferred by  Kameenski  to  Biovularia,  B.  minima  and  B.  olivacea.  With 
a  few  exceptions  such  as  those  above  noted,  the  terrestrial  species 
are  smafl.  When  in  flower  and  in  numbers,  they  are  conspicuous 
enough,  but  if  not  in  flower  they  may  be  found  only  with  very  as- 
siduous hunting.  How  one  would  find  U.  simplex  (S.  W.  Australia) 
unless  in  flower  is  past  guessing,  so  minute  are  the  leaves. 

But  large  or  small,  massive  or  delicate,  perennial  or  evanescent 
annuals,  they  present  a  complex  and  puzzling  morphology.  They 
are  entirely  rootless,  even  in  the  embryonic  condition.  The  distinc- 
tion between  stem  and  leaf  is  vague.  Only  in  the  inflorescence  and 
in   certain   shoots   (air-shoots  of   U.  vulgaris  etc.)   is  the  morphology 


Francis  E.  Lloyd  —  214  —  Carnivorous  Plants 

easily  recognizable.  But  most  to  be  wondered  at  are  the  traps  which 
present  an  astounding  degree  of  mechanical  delicacy  depending  on 
a  fineness  of  structure  scarcely  equalled  elsewhere  in  the  plant  king- 
dom. Moreover  they  occur  in  an  unexpected  variety  of  form.  But 
withal  they  are  small,  the  largest  scarcely  exceeding  5  mm.  in  great- 
est extent,  the  smallest  0.3  mm.  The  prey  caught  by  these  traps 
are  small  —  water  fleas,  minute  larvae  often  of  mosquitos,  very  young 
fish  (Dean)  and  small  tadpoles,  fish  and  tadpoles,  however,  being 
ensnared  only  by  being  caught  by  the  tail  or  head  in  the  mouth 
of  the  trap  but  not  entirely  engulfed  as  is  smaller  prey  (Dean, 
Lloyd).  Larger  prey  may,  however,  be  finally  "entirely  absorbed" 
according  to  Matheson  (1930),  as  e.g.  in  the  case  of  the  larva  of 
Brachydeutera  argentata.  Matheson  sees  the  difficulty  of  explain- 
ing this,  since  the  greater  mass  of  the  animal's  body  is  outside  of 
the  trap.  An  explanation  is,  however,  at  hand  and  will  be  later  of- 
fered. 

The  observation  that  mosquito  larvae  are  often  caught  in  the 
traps  has  led  some  investigators  to  hope  that  the  floating  large  trapped 
species  of  Utricidaria  would  be  useful  in  aiding  to  control  those  pests 
(Matheson  1930).  It  is  well  enough  known  that  multitudes  of 
mosquito  larvae  are  in  fact  captured,  the  number  being  limited  only 
by  the  number  of  traps  available  (Franca). 

The  flowers  are  of  the  personate  type,  two-lipped,  the  throat 
usually  closed  by  a  palate,  and  the  lower  Hp  provided  with  a  spur 
of  various  shape,  except  in  a  few  species,  in  which  it  is  a  saccate 
enlargement,  as  in  Biovularia,  in  U.  cymbantha,  U.  Stephens ae  (Ms. 
name),  and  in  U.  minor,  a  fact  which  tends  to  invalidate  Kamienski's 
genus.  U.  purpurea  and  its  co-species  have  flowers  with  a  peculiarly 
laterally  saccate  lower  lip.  Most  extraordinary  are  the  two  species 
U.  capilliflora  F.v.M.,  and  U.  Dunstani  Lloyd  (Lloyd  1936^)  (Text 
FIG.  5).  The  former  has  the  upper  lip  drawn  out  into  two  very  long 
attenuate  lobes,  the  lower  lip  into  five  slender  finger-like  lobes.  In 
U.  Dunstani,  the  upper  lobe  is  rounded  and  entire  while  the  lower 
lip  is  five  lobed,  the  middle  adjoining  two  lobes  small,  and  the  two 
lateral  lobes  very  long  and  attenuate  and  to  the  casual  observer  iden- 
tical with  the  long  tips  of  the  upper  lip  in  U.  capilliflora.  The  flowers 
are  very  small;  had  they  been  large  they  would  have  excited  as  much 
admiration  as  the  flowers  of  some  orchids  or  that  of  an  Aristolochia 
with  long  appendages.  The  showy  flowers  of  some  S.  American  spe- 
cies have  been  mentioned.  These  are  large  and  are  rendered  conspicu- 
ous by  the  wide  lateral  lobes  of  the  lower  lip  particularly.  Yellow 
is  the  most  prevalent  color,  but  white  to  purple  flowers  are  also  fre- 
quent with  admixtures  in  the  form  of  yellow  or  reddish  markings 
on  white  or  blue  grounds;  or  red  on  yellow,  especially  on  the  palate, 
are  often  met  with.  Generally  the  pistil  has  a  unilocular,  globular 
ovary  with  a  two  lipped  stigma,  the  lower  being  considerably  larger 
than  the  upper.  The  seeds  are  usually  numerous  on  a  globular  ba- 
sifixed  placenta.  In  certain  species,  however,  two  to  three  seeds 
only  are  produced  on  a  rounded  placenta  {U.  cymbantha)  or  two  only, 
back  to  back,  in  Biovularia,  the  placenta  reduced.  The  release  of 
the  seeds  may  be  by  circumcissile  or  irregular  fracture,  by  a  trian- 


Chapter  XIII 


—  215  — 


Utricularia,  Biovularia 


gular  window  {U.  subulata),  or  by  a  longitudinal  slit  {U.  orhiculata). 
There  are  only  two  stamens  bending  upward  along  the  curve  of  the 
ovary  wall. 

The  sepals  are  usually  two  in  number,  upper  and  lower.  In  Poly- 
pompholyx  there  are  four,  hence  de  Candolle's  justification  of  his 
name  Tetralobus,  of  slightly  later  date  than  and  therefore  superceded 
by  Polypompholyx  Lehmann.  Polypompholyx  as  a  generic  name 
should,  according  to  Barnhart,  be  in  turn  superseded  by  Cosmiza 
Raf.  1838,  since  both  Polypompholyx  Lehmann  (Feb.  1844)  and  Telra- 
lohus  DC.  (Mar.  1844)  are  later  names.  Lehmann's  name  is  at  the 
moment  generally  used. 

U.  fimbriata   superficially   resembles  Polypompholyx  in   having  its 


Fig.  5.  —  Utricularia  capilliflora  (277)  and  U.  Dunsiani  (272);  up,  upper  corolla  lobe; 
us,  upper  sepal;  aus,  abnormal  upper  sepal.  The  two  figures  on  the  right  are  shadow 
prints  from  herbarium  specimens,  natural  size. 

two  fimbriate  sepals  backed  up  by  two  fimbriate  bracts,  and  has  been 
incorrectly  referred  to  Polypompholyx.  Barnhart  calls  it  Aranella 
fimbriata  (Barnhart  191 6). 

The  Utriculariae  are  of  world  wide  distribution.  Of  the  widest 
distribution  are  the  submersed  or  semi-submersed  plants  of  the  type 
of  U.  vulgaris.  They  are  found  occupying  a  circumboreal  zone  char- 
acterized by  certain  species  peculiar  to  it,  throughout  N.  America 
including  Greenland,  Europe  and  Asia.  Related  species  extend 
throughout  the  tropics  and  into  S.  America,  S.  Africa,  Australia  and 
New  Zealand.  The  submersed  floater  U.  purpurea  and  its  co-species 
are  purely  American,  extending  from  Maine,  possibly  Newfoundland, 
down  the  Atlantic  Coast,  west,  to  Indiana,  and  into  E.  South  Amer- 
ica. Another  submersed  form,  U.  tubulata,  which  is  related  to  quite 
another  group  peculiar  to  Australia  (the  U.  monanthos  type),  is  found 
in  N.  E.  Australia  (Queensland). 

The  terrestrial  forms  are  widely  distributed  in  the  tropics  of  the 


Francis  E.  Lloyd  —  216  —  Carnivorous  Plants 

Old  and  New  Worlds,  with  northward  extensions  along  the  Atlantic 
coast,  through  Central  America,  and  along  the  Pacific  Coast  of  Asia. 
These  include  a  considerable  number  of  distinct  types,  some  of  which 
are  pecuHar  to  America,  others  to  the  Old  World,  and  still  others 
common  to  both  (£/.  suhulata).  They  are  to  be  found  also  in  Aus- 
tralasia. 

So  far  as  is  known,  Utricularia  is  not  found  on  oceanic  islands. 

Embryology.  —  The  embryological  story  of  Utricularia  has  not  yet 
been  worked  out  in  its  fullness,  but  certain  striking  features  have 
been  observed  and  have  been  recorded  by  Lang,  Merl  (Genlisea), 
Merz,  and  Wylie  and  Yocom.  Merz  pointed  out  that  the  vascular 
tissues  supplying  the  large  placenta  end  there  and  do  not  enter  the 
funicles  of  the  ovules.  As  a  compensation  for  this,  it  would  appear, 
special  masses  of  nutritive  tissue  arise  in  the  chalaza  and  in  the  pla- 
centa {Utricularia  vulgaris,  etc.)  or  what  amounts  to  the  same  thing, 
in  a  "funicular  hump"  (to  quote  Wylie)  (Poly  pomp  holy  x  Lehm.). 
These  islands  of  food  materials  are  made  use  of  for  the  embryo  by 
the  penetration  into  them  of  peculiar  haustorial  extensions  of  the 
endosperm.  Transitory  starch  appears  in  these  haustoria.  These  nu- 
tritive masses  are  finally  cut  off  from  the  ovule,  as  the  embryo  ap- 
proaches maturity,  by  the  development  of  diaphragms  of  suberized 
cells.  Since  according  to  Merz  the  end  of  the  suspensor  extends 
into  the  placental  nutritive  tissue,  this  is  cut  ofT  at  the  same  time. 
Wylie  and  Yocom  do  not  support  this.  In  the  related  Genlisea, 
nutritive  islands  occur  entirely  within  the  ovule  (Merl). 

The  ovule  has  but  a  single  integument,  which  is  common  enough 
among  the  sympetalae,  from  the  outer  cell  course  of  which  a  thin 
testa  is  derived.  The  tegmen,  membranous  and  delicate,  may  repre- 
sent the  remaining  tissue  of  the  integument,  since  the  nucellus  is 
absorbed  (Merz).  The  mature  embryo  has  neither  root  nor  punctum 
vegetationis  (Merl,  Lloyd). 

Seed,  embryo  and  seedling.  —  The  seeds,  in  most  cases,  develop 
on  a  large  globular,  central  placenta,  and  are  crowded  suf^ciently 
in  some  species  so  that  by  mutual  compression,  they  become  angu- 
lar, approximately  hexagonal,  with  fiattish  outer  chalazal  and  inner 
micropylar  surfaces,  the  latter  the  smaller  (Warming,  Wylee).  The 
planes  of  the  sides  radiate  as  if  from  the  center  of  the  placenta  {U. 
vulgaris,  U.  resupinata),  or  the  ovules  overlap  and  become  winged 
with  circular  wings  {U.  oligosperma,  U.  exolcta)  the  whole  dished 
into  a  concavo-convex  lens  shape.  In  other  species,  chiefly  terres- 
trial, the  seeds  are  minute  (down  to  0.2  mm.  in  diam.)  and  globular 
or  oval,  occasionally  lobulate  {U.  reniformis,  U.  Dusenii,  U.  pur- 
purea) or  have  polar  clusters  of  trichomes  {U.  brachiata)  (Compton) 
or  scattered  glochidia  covering  one  end  {U.  orbiculata). 

The  testa  is  composed  of  an  epidermis  of  darkened  (reddish  or 
brown),  relatively  large  cells  with  their  inner  and  radial  walls  thick- 
ened, the  outer  thin  and  collapsed  in  maturity.  Their  shape  varies 
from  round  angular  to  elongate,  many  and  relatively  small  or  few 
and  relatively  large.  In  a  few  instances  they  become  mucilaginous 
when  wet,  in  species  which  grow  with  the  vegetative  parts  submersed 
and    attached    to   a   stony    substrate    in    running    water    {U.    rigida, 


Chapter  XIII  —  217  —  Utricularia,  Biovularia 

and  probably  U.  neottioides) .  In  a  very  few  instances  the  seed  has 
no  hard  testa,  but  simply  a  thin  lax  membrane  easily  torn,  and  the 
seed  seems  to  be  released  by  the  rotting  away  of  the  capsule  {Bio- 
vularia) . 

Embryo.  —  The  embryo  is  a  mass  of  scarcely  differentiated  cells 
containing  much  starch  and  oil,  and  is  either  bun  shaped  with  a 
depression  at  the  vegetative  pole  {U.  vulgaris)  (Warming)  (2/  —  6) 
or  flattened  by  lateral  compression,  with  the  growth  pole  on  its  edge 
{U.  emarginata  and  exoleta)  {21  —  7),  this  position  and  form  being  due, 
according  to  Merz,  to  rotation  of  the  embryo-sac  and  embryo  through 
90  deg.  following  the  abscission  of  the  egg-pole  endosperm;  or  again 
more  or  less  oval  or  spindle  shaped  (a  host  of  species,  e.g.  U.  bifida) 
(22  —  I,  18).  In  a  few  there  is  a  depression  at  the  root  pole  (Poly- 
pompholyx)  {22  —  26).  Its  structure  is  very  simple:  it  is  a  mass 
of  rounded  parenchyma  clothed  with  an  epidermis,  the  cells  of  which 
covering  the  growth  pole  are  small,  columnar  and  highly  protoplas- 
mic. The  primary  organs  usually  originate  at  this  pole,  but  may 
occasionally  appear  elsewhere  {U.  bifida)  {22  —  19-22).  There  is  an 
entire  absence  of  a  root.  Even  at  maturity  the  embryo  has  as  yet 
no  lateral  organs.  Goebel  reported  them  in  the  embryo  of  U .  or- 
biculata,  but  I  have  failed  to  find  them.  In  U.  reniformis  and  U. 
nelumbijolia  primary  leaves  have  been  seen,  and  these  species  may 
display  vivipary  (Merl). 

While  the  growth  pole  produces  lateral  organs,  two  in  many  cases 
(cotyledonoids)  or  various  numbers  in  others,  a  punctum  vcgetationis 
(the  primary  primordium  of  a  shoot)  is  never  present  in  the  embryo, 
nor  is  ever  developed.  Shoots  when  present  in  the  plant  are  always 
produced  as  lateral  organs. 

Germination  {22  —  1-28).  —  The  events  of  germination  show  that 
there  are  three  types  of  seedling:  (i)  a  simple,  in  which  there  are 
two  cotyledonoids  (since  one  of  these  is  a  stolon);  and  (2)  a  com- 
plex, in  which  there  are  6  to  13  (Warming,  Jane)  cotyledonoids, 
or  indeed  only  two;  and  (3)  a  type  in  which  there  are  no  cotyledonoids 
at  all,  with  three  primary  shoots  only.  The  simple  type  is  displayed 
by  all  the  terrestrial  species  (so  far  as  known),  such  as  U .  capensis,  U. 
bifida,  U.  monanthos,  Polypompholyx,  which  have  been  studied.  The 
complex  type  is  seen  in  U.  vulgaris  (with  many  cotyledonoids)  and  in 
U.  exoleta,  U.  emarginata  etc.  (with  two  cotyledonoids).  U.  capensis 
among  others  has  been  studied  by  myself  (19376).  The  seed  is  minute 
and  oval  in  shape.  From  the  growth  pole  emerges  at  first  a  leaf 
followed  shortly  by  a  stolon.  Between  them  in  the  expected  position 
there  is  no  punctum  vcgetationis.  The  leaf  extends  upwards,  the  stolon 
downwards.  The  first  evidence  of  further  growth  is  the  appearance 
of  a  trap,  on  the  base  of  the  stolon,  a  little  away  from  the  middle 
Kne  (22  —  14),  or  rarely,  as  in  U.  cleistogama,  asymmetrically  near  the 
leaf  base.  At  the  base  of  the  trap-stalk  a  bud  arises  which  pro- 
duces an  ascending  stolon  with  more  or  less  crowded  leaves.  This 
becomes  thicker  with  upward  growth,  finally  becoming  an  inverted 
cone,  a  protocorm  bearing  leaves,  traps  and  stolons.  Their  vascular 
tissues  form  within  the  protocorm  a  loose  stem-Hke  structure,  similar 
to  that  described  by  Warming  for  Genlisea  and  by  myself  for  Poly- 


Francis  E.  Lloyd  —  218  —  Carnivorous  Plants 

pompholyx.  At  its  top  is  formed  at  length  a  large  radially  sym- 
metrical bud,  which  becomes  the  inflorescence  {22  —  11,  25).  Of  the 
stolons,  some  are  anchoring  in  function  (rhizoids)  while  others  be- 
come runner  stolons,  bearing  leaves  along  the  upper  surface,  and 
facing  toward  the  corm,  in  the  adaxial  axils  of  which  other  scapes 
may  arise.  Thus  is  produced  a  spreading  plant.  Scapes  may  also 
arise  from  buds  adventive  on  the  leaves,  this  among  many  irregu- 
larities of  growth.  Sometimes  the  primary  leaf  may  produce  a  num- 
ber of  traps  in  the  adaxial  axils  of  which  buds  are  formed,  as  in  the 
case  of  the  axils  of  leaves  produced  on  stolons. 

This  course  of  events,  thus  briefly  stated,  is  followed  by  all  other 
species  studied:  U.  bifida,  U.  monanthos,  with  evidence  from  a  con- 
siderable number  of  others.  U.  bifida  was  also  studied  by  Goebel 
who  seems  to  have  thought  that  the  first  bud  was  between  the  cot- 
yledonoids,  and  suffered  later  displacement,  as  his  drawings  indi- 
cate. But  the  statements  of  both  Goebel  and  Merl  (U.  longifolia) 
admit  an  asymmetrical  position.  My  own  studies  of  U.  bifida  have 
revealed  a  strong  tendency  on  the  part  of  the  embryo  to  produce 
at  first  a  leaf  only,  raised  more  or  less  on  an  elongate  extension  of 
the  upper  part  of  the  embryo  body  (a  podium)  and  for  the  primary 
stolon  to  be  produced  at  its  base  from  a  distinct  bud  there  seen  {22  — 
i-ii). 

If  the  protocorm  produces  no  runners,  as  in  U.  capilliflora,  U. 
violacea,  U.  Hookeri,  Polypompholyx,  an  inflorescence  can  be  produced 
only  from  the  top  of  the  protocorm  (22  —  25,  26),  or  by  secondary 
branching  from  the  scape  itself.  This  development  is  called  abrupt. 
Such  plants  do  not  spread  by  runner  stolons.  The  behavior  of  U. 
capensis  etc.,  which  spreads  by  runners,  is  diffuse. 

In  all  these  forms,  especially  in  the  abrupt  kind  of  germination, 
the  primary  bud  arising  from  the  first  stolon  can  elongate  very  con- 
siderably to  form  a  naked  ascending  stolon  producing  leaves  only  at 
length.  The  curious  asymmetrical  relations  of  embryo  and  its  primary 
organs  than  becomes  quite  apparent.  I  have  seen  this  in  U.  violacea, 
U.  Hookeri  and  Polypompholyx,  in  which  the  events  of  germination 
are  preserved  in  the  mature  individual,  for  the  embryo  may  persist 
throughout  the  life  of  the  plant  {22  —  26). 

The  complex  kind  of  germination  is  displayed  by  a  lot  of  spe- 
cies represented  by  U.  vulgaris,  which  has  been  the  subject  of  much 
study  by  Warming,  Pringsheim,  Kamienski,  Goebel,  Jane  and 
Lloyd,  and  by  U.  oligosperma  (Goebel).  The  condition  found 
in  U.  exoleta  (Goebel)  and  U.  emarginata  though  simple  in  the  sense 
indicated  by  the  number  of  cotyledonoids,  is  merely  a  special  case 
evidently  related  to  the  vulgaris  condition. 

In  U.  vulgaris  the  embryo  is  a  prolate  spheroid.  From  a  low  dome 
arise  several  leaf  buds  in  an  outer  circle,  within  which  several  other 
primordia  stand,  with  no  apparent  order,  though  it  has  been  stated 
otherwise  (Goebel).  The  outer,  and  some  of  the  inner  primordia 
become  awl-shaped  leaves,  but  to  pick  out  two  of  these  as  cotyledons 
is  impossible  (Goebel).  Occasionally  one  of  them  ends  in  a  trap 
(Goebel;  Jane).  Of  the  inner  primordia,  some  become  leaves,  usually 
one  a  dorsiventral  shoot,  and  one  a  primary  trap.     Sometimes  leaves 


Chapter  XIII  —  219  —  Utricularia,  Biovularia 

are  produced  which  are  evidently  partly  shoot  in  structure,  the  dis- 
tinction between  leaf  and  shoot  being  here  vague.  The  apex  of  the 
dome  never  develops  {21  —  1-5)- 

In  U.  exoleta  and  U.  emarginata  the  embryo  is  laterally  compressed 
so  that  the  growth  pole  is  on  the  edge.  Here  two  leaves  are  produced. 
These  may  occasionally  become  shoots  {21  —  7D).  Near  their  bases, 
but  displaced  to  one  side  are  usually  two  buds,  sometimes  a  third. 
These  become  dorsiventral  shoots. 

Aberrancies  of  development  are  not  at  all  unusual.  For  example, 
one  embryo  of  U.  vulgaris  produced  only  two  leaves  and  two  shoots 
which  became  at  once  dorsiventral  "water  shoots." 

In  U.  nelmnbifolia,  otherwise  similar  to  U.  vulgaris,  the  primary 
leaves  are  widely  forked  (Merl)  and  those  of  U.  reniformis  are  broadly 
spatulate  (Goebel).  According  to  Goebel,  the  embryo  of  U.  mon- 
tana  has  no  primordia  before  germination,  and  on  it  there  are  pro- 
duced two  primordia  (the  cotyledonoids)  of  which  one  becomes  a 
spatulate  leaf,  the  other  a  trap,  on  the  side  of  the  "vegetation  point" 
which  grows  directly  into  a  radial  structure  from  which  stolons  etc. 
grow.  The  interpretation  here  is  to  be  questioned,  as  it  is  doubt- 
ful if  Goebel's  identification  of  the  vegetation  point  is  correct. 

The  third  type  of  germination  is  seen  in  U.  purpurea.  The  embryo 
is  ovate,  with  a  flattened  broad  end.  From  this  there  normally  arise, 
in  succession,  three  shoot  buds  standing  in  a  triangle  with  respect  to 
each  other.  The  first  is  dominant  in  growth;  the  second  to  appear 
may  form  at  first  a  close  second,  but  at  length  lags  behind  in  growth; 
while  the  third  may  not  do  more  than  put  in  an  appearance,  and  then 
fail  to  develop  (Text  fig.  6,  1-7).  In  one  case  a  fourth  shoot  bud 
appeared  early  (Text  fig.  6,  4  and  5),  but  its  subsequent  development 
showed  it  to  be  a  branch  at  the  base  of  the  first  bud,  and  in  other 
seedlings  it  appeared  later,  but  constantly.  The  development  of  the 
first  shoot  has  been  followed  until  it  produced  five  whorls  of  branches 
(leaves  in  the  taxonomic  texts).  The  earlier  two  whorls  have  but  two 
members  bearing  traps,  placed  symmetrically  attached  to  the  upper 
moiety  of  the  stem.  On  the  upper  surface  of  the  stem  as  a  member  of 
the  whorl  may  appear  a  bud  of  unlimited  growth,  destined  in  its  turn 
to  produce  whorls  of  secondary  members  (Text  fig.  6,  7).  In  the 
third  to  fifth  whorls,  two  additional  members,  placed  in  the  wide  dorsal 
space,  appear.  These,  however,  do  not  bear  traps.  In  the  fourth 
whorl,  in  one  case  observed,  one  of  the  ventral  pair  produced  a  branch 
which,  however,  bore  no  trap.  In  one  instance  a  seedling  was  found  in 
which  the  first  and  second  buds  were  fasciated  (Text  fig.  6,  6).  It  is 
evident  that  in  this  type  the  seedling  at  once  takes  on  the  morphologi- 
cal character  of  the  mature  form,  which,  however,  has  whorls  of  four 
{U.  elephas)  or  six  {U.  purpurea)  branched  members. 

It  would  be  most  interesting  to  know  the  course  of  germination  of 
U.  tubidata,  but  of  this  we  are  yet  ignorant. 

Types  of  Utricularia.  —  In  the  following  account,  the  various  spe- 
cies, so  far  as  they  are  here  included,  are  arranged  according  to  the 
character  of  their  traps. 

I .  The  Utricularia  vulgaris  type.  —  All  the  plants  of  this  type  have 
traps  which  are  closely  similar  in  the  mechanical  details  of  structure 


Francis  E.  Lloyd  —  220  —  Carnivorous  Plants 

to  those  of  U.  vulgaris,  differing  among  themselves  only  as  regards  non- 
essential, small  details.     A  description  of  the  trap  is  deferred  till  later. 

Freely  floating  forms.  —  U.  vulgaris  itself  is  the  best  known  and 
most  widely  distributed,  and  will  serve  well  as  the  type  of  numerous 
species,  world  wide  in  distribution. 

The  plant  consists  of  a  cylindrical  or  laterally  compressed  axis 
which  may  reach  a  length  of  300  cm.,  probably  more,  supporting 
two  lateral  rows  of  divided  "leaves,"  and  dying  off  behind  as  it  grows 
from  the  tip.  The  leaves  are  very  crowded  toward  the  growing  cir- 
cinate  end.  The  whole  plant  is  lax  and  lies  in  the  still  water  in  which 
it  grows  entangled,  one  plant  with  another,  forming  often  dense  mats. 
Toward  the  end  of  the  growing  season  the  more  terminal  internodes 
become  very  short  and  the  leaves  densely  packed  to  form  a  resting 
bud  (turion),  which  sinks  or  floats,  according  to  circumstances,  and 
may  be  frozen  in  the  ice.  In  spring  the  tips  of  the  leaves  or  the 
chief  axis  proliferate,  giving  rise  directly  to  new  plants  with  leaves  of 
simpler  structure  at  first. 

A  leaf  arises  from  a  single  lateral  outgrowth  from  the  prostrate 
stem,  remaining  single  in  U.  oligosperma,  or  forking  as  it  develops 
(Pringsheim,  Goebel)  to  form  two  lobes  {21  —  8),  at  whose  bases 
may  arise  secondary  outgrowths,  one  on  each  of  which  can  develop  into 
additional  lobes.  The  third  and  fourth  lobes  are  not  at  all  or  only 
weakly  developed  in  some  species  {U.  vulgaris)  but  are  strongly  de- 
veloped in  others,  e.g.  U.  Thonningii.  In  others  fifth  and  sixth  small 
lobes  are  formed  laterally  to  the  third  and  fourth,  and  are  known  as 
auricles.  In  U.  Thonningii  (Angola)  the  auricle  is  a  fan  shaped  pro- 
duction, with  many  rays  from  its  edge,  all  armed  with  stiff  bristles, 
occasionally  bearing  a  trap.  In  U.  stellaris  (Asia,  Africa)  and  flexuosa 
(Singapore)  the  auricles  are  deeply  subdivided,  the  divisions  more 
or  less  curved  and  crowded  upon  each  other.  Each  leaf  lobe  is  pin- 
natifid,  the  pinnae  being,  however,  alternate,  the  internodes  so 
placed  as  to  produce  a  zigzag  axis,  appearing  monopodial  {20  —  i). 
The  lateral  divisions  (pinnae)  have  the  same  disposition  of  parts. 
The  ends  of  the  divisions  are  usually  armed  with  stiff  bristles,  either 
singly  or  in  bundles,  and  these  afford  a  taxonomic  character. 

The  traps  are  borne  on  the  leaves  in  such  position  as  to  suggest 
that  each  represents  a  leaf  division  (Goebel,  Meierhofer).  The 
details  of  the  structure  of  the  trap  will  be  given  fully  beyond.  Here 
is  only  to  point  out  that  the  trap  is  always  placed  with  its  sagittal 
section  transverse  to  the  plane  of  the  leaf,  the  mouth  facing  the 
apex  of  the  shoot  {20  —  i).  The  interior  surface  of  the  trap  is  mor- 
phologically the  upper  surface  of  the  leaf  division  which  it  repre- 
sents (hypopeltate,  Goebel).  In  some  species  only  one  lobe  of  a 
leaf  produces  traps,  the  other  (upper)  half  being  wholly  photosynthetic 
in  function. 

In  certain  species  leaves  of  a  highly  speciahzed  kind  occur  on 
the  basal  part  of  the  flower  stalk.  In  these  the  midrib  is  much  in- 
flated by  the  enlargement  of  intercellular  spaces  while  the  lateral 
divisions  are  much  reduced.  These  are  disposed  in  a  whorl  ("false 
whorl")  and  act  as  floats  to  support  the  inflorescence  above  the 
water  surface    {U.   radiata,    U.   inflata,    U.   stellaris)    {20  — 12).     The 


Chapter  XIII 


221 


Utricularia,  Bioviilaria 


size  and  shape  of  these  floats  are  characteristic  of  different  species 
possessing  them.  In  U.  stellaris  they  are  short  and  of  relatively 
wide  diameter.     In   U.  injlata  they  are  long  (4-5  cm.)   and  clavate. 


Fig.  6.  —  1-7,  Utricularia  purpurea.  —  i,  Early  stages  of  germination  of  a  seed  {2>-2> 
mm  long)  from  which  only  one  growing  point  arose  (to  be  followed  by  others  later  in  all 
probability);  2,  Three  figures  in  a  row,  three  views  of  an  early  stage  of  germination,  a 
later  stage  of  which  is  shown  in  3,  in  which  two  young  growing  points  show  circination; 
4  and  5,  Two  following  stages  in  the  germination  of  a  seed  which  produced  three  growing 
pomts  all  of  nearly  the  same  age,  with  a  fourth,  secondary  to  the  middle  growing  point; 
6,  A  case  in  which  fasciation  occurred,  the  two  figures  on  the  right  show  an  early  stage 
of  germination,  a  much  later  stage  is  shown  on  the  left,  in  which  it  is  seen  that  one  of  the 
growing  points  had  divided,  an  abnormality;  7,  An  advanced  stage  in  germination  (15  mm 
long),  one  of  the  three  growing  points  still  quiescent;  five  whorls  of  branches  (the  maximum 
seen)  were  produced,  as  shown  on  the  longer  stolon  of  this  figure.  At  the  first  whorl  of  this, 
the  bud  of  a  branch  stolon  of  indefinite  growth  is  seen.  No  traps  are  produced  on  the  two 
dorsal  branches  of  the  third  and  fourth  whorls. 

8-10,  Utricularia  cleistogama.  —  8,  Early  stage  of  germination  showing  primary  stolon 
and  primary  leaf,  with  the  primary  trap  on  the  leaf  near  its  base;  9,  A  later  stage  in  detail 
showing  the  origin  of  the  trap  from  the  leaf  base;  10,  A  more  advanced  stage  of  the  seed- 
ling in  which  a  second  leaf  arose  in  the  place  of  a  primary  trap. 

Still  another  form  of  leaf  occurs  on  short  stolons  at  the  base  of 
the  scape  of  the  inflorescence  (Buchenau  1865),  the  so-called  rhi- 
zoids,  several  of  which  are  usually  present.  Their  leaves  are  much 
reduced  in  size  and  have  very  small  pinnae  which  are  curved  and 
crowded  into  claw-Hke  masses.  More  or  less  of  each  pinna  is  densely 
covered  with  mucilage  glands  quite  like  those  scattered  over  the 
whole  plant  surface  {U.  vulgaris,  etc.). 


Francis  E.  Lloyd  —  222  —  Carnivorous  Plants 

In  the  species  U.  oligosperma  there  is  a  pronounced  dimorphism 
of  leaves,  each  kind  occurring  on  separate  branches.  Those  of  one 
kind  bear  none,  or  very  few  poorly  developed  traps.  They  are  finely 
divided  with  very  long  terminal  divisions  in  the  form  of  fiat,  ensi- 
form  divisions,  and  are  very  crowded,  so  that  the  leafy  branches 
appear  as  dense  tufts  strongly  contrasted  with  those  which  bear  the 
second  kind  of  leaves  which  are  trap  bearing.  The  traps  are  very 
numerous  and  crowded,  and  the  leaves  which  bear  them  have  only 
a  single  lobe,  whose  divisions  all  He  in  the  plane  of  the  axis  which 
bears  them. 

The  leaves  in  this  and  similar  species  {e.g.  U.  mixta)  are  provided 
on  one  side  only  with  a  small  fohose  appendage  consisting  of  about 
four  radiating  accuminate  members  each  bearing  a  trap,  the  whole 
having  a  stipulate  appearance  (2j  —  3).  These  may  be  similar  to 
the  minute  axillary  shoots  mentioned  by  Pringsheim  in  U.  vulgaris 
{21  —  10),  different  only  in  position. 

A  pair  of  similar  appendages  (we  may  call  them  tentatively  dwarf 
shoots)  occurs  also  at  the  sides  of  the  base  of  the  air  shoot,  but  here 
they  often  have  more  divisions,  each  carrying  a  trap  (23  —  2,  6), 
They  are  found  also  in  U.  mixta.  To  the  unaided  eye  in  such  cases 
there  appears  at  the  base  of  the  air  shoot  a  tight  grape-like  cluster 
of  as  many  as  a  dozen,  or  as  few  as  two  to  four  traps.  Without 
careful  examination  it  would  seem  as  if  the  air  shoot  were  supplied 
with  stipules,  but  the  organs  in  question  arise  directly  from  the  axis. 
They,  however,  derive  their  vascular  strands  as  branches  from  the 
main  strand  entering  the  air  shoot,  though  exceptions  have  been 
noted.  So  far  as  I  am  aware  these  pecuHar  dwarf  leaves  are  to  be 
found  only  on  those  species  which  have  strap-shaped  stolons,  the 
greater  longitudinal  plane  being  vertical,  the  upper  edge  somewhat 
narrower  than  the  lower.  They  cannot  readily  be  homologized  with 
the  auricles  of  some  species  because  of  the  distinct  origin  from  the 
stolon. 

A  large  number  of  species  of  the  U.  vulgaris  type  {U.  exoleta, 
emarginata,  gibba,  cymbantha,  etc.),  plants  with  thread-Kke  stolons, 
have  leaves  which  may  be  no  more  than  a  single  fork,  two  slender 
segments  arising  from  the  base,  only  the  lower  one  bearing  a  single 
trap  (27  —  17,  18);  or  they  may  be  variously  more  complex,  but 
always  much  simpler  than  in  U.  vtdgaris. 

Branching;  origin  of  the  inflorescence.  —  It  was  quite  apparent  to 
the  earlier  observers  (Irmisch  1858;  Buchenau  1865)  that  branch- 
ing in  Utricularia  does  not  follow  a  pattern  common  to  the  flower- 
ing plants.  The  observations  of  these  students,  with  those  of 
Pringsheim  (1869)  and  Goebel  (1891),  afford  the  available  basis  for 
description  to  which  my  own  studies  have  been  added.  From  these 
there  emerges  in  fairly  clear  form  the  pattern  peculiar  to  these  very 
aberrant  organisms.  We  consider  U.  vulgaris  which  Pringsheim 
studied  developmentally,  in  contrast  with  Irmisch  and  Buchenau 
who  examined  only  the  mature  condition. 

U.  vulgaris.  —  The  growing  point  (2/  —  8)  of  the  horizontal  shoot 
shows  upward  circination  (Pringsheim,  Goebel)  and  that  (i)  a  row 
of  peculiar  branches  arises  in  a  line  on  the  upper  surface  of  the  stolon 


Chapter  XIII  —  223  —  Utricularia,  Biovularia 

in  no  relation  to  the  leaves  except  that  they  are  usually  nearer  the 
nodes  than  to  the  middle  of  the  internode,  and  either  in  front  or 
behind  them.  They  do  not  arise  in  a  leaf  axil.  These,  first  seen 
by  BucHENAU  and  thought  by  him  to  be  roots,  are  the  "tendrils"  of 
Prlngsheim  and  "air  shoots"  of  Goebel  (23 — i).  Gluck  ques- 
tions their  usefulness  as  air  shoots.  They  are  long  and  very  slender 
with  two  lateral  rows  of  "mussel-shaped"  leaves  with  stomata,  and 
are  circinate  forwards.  They  are  absent  from  many  species,  including 
all  of  the  U.  exoleta  type.  They  have  the  abihty  to  transform  them- 
selves by  apical  growth  into  ordinary  shoots  (Goebel,  Glxjck). 
(2)  Lateral  branches  (st2)  arise  near  the  upper  edge  of  the  oblique 
leaf  insertion,  but  not  in  the  leaf  axil.  They  are  of  occasional  oc- 
currence only  {21  —  8,  st2).  (3)  The  inflorescence  (sc)  arises  in  as- 
sociation with  a  third  stolon  branch  (sta)  in  the  axil  of  sta,  the  latter 
being  the  larger  at  first,  the  scape  arising  from  its  base.  As  Goebel 
observed  in  U.  flexuosa,  "Never  does  one  find  the  inflorescence  iso- 
lated, but  always  combined  with  a  leafy  branch  springing  from  its 
base."  The  question  which  of  the  two  is  primary  cannot  at  the  mo- 
ment be  settled.  (4)  In  some  leaf  axils  ("older  ones,"  Pringsheim) 
buds  may  arise,  which  do  not  center  on  the  middle  of  the  leaf  axil. 
Here  again  are  two,  one  arising  from  the  base  of  the  other,  and  they 
are  a  leafy  shoot  and  a  scape  (the  smaller)  just  as  when  an  st2  branch 
is  present,  but  now  in  a  leaf  axil,  not  in  the  branch  axil  {21  —  9). 
Pringsheim  calls  them  dwarf  or  aborted  shoots.  (5)  In  the  axil  of 
most  leaves  there  is  a  cluster  of  about  4  traps  arising  at  the  middle 
point.  Goebel  interpreted  Pringsheim's  observation  and  drawing  to 
mean  that  this  group  of  traps  arises  from  a  short  branch,  while 
Pringsheim  thought  that  the  branch  arises  from  a  trap  stalk.  Goebel 
is  probably  correct  {21  —  10). 

U.  stellaris,  U.  inflata  and  the  Hke  appear  to  conform  to  the  above 
description.  In  U.  oligosperma  and  U.  mixta  somewhat  more  special 
conditions  prevail.  Instead  of  one  branch  of  st2  rank,  there  are  two, 
coordinate  in  development,  one  opposite  the  single  leaf  (undivided  at 
the  base)  and  one  below  the  axil.  The  lower  of  these  {U.  oligosperma) 
bears  leaves  with  very  many  traps,  the  upper  is  almost  devoid  of 
traps.  Above  the  axil  of  the  upper  branch  arise  the  twin  branches, 
one  a  leafy  branch,  the  other  a  scape,  conjoined  at  the  base  {21 — 
11).  Thus  in  maturity  there  is  a  cluster  of  stolons  radiating  from 
the  base  of  an  inflorescence,  the  forward  and  backward  extensions 
of  the  chief  stolon,  and  three  leafy  branches.  In  both  species  the 
air  shoots  are  prominent  and  have  laterally  placed  at  their  bases 
clusters  of  traps  which  have  been  referred  to  already  as  dwarf  leaves. 
They  occur  also  at  the  leaf  bases,  either  axillary  or  at  one  side.  There 
is  evidence  that  these  are  dwarf  shoots  (Goebel)  bearing  traps  with 
broadened  stalks,  not  trap  stalks  bearing  shoots,  as  Pringsheim 
thought. 

V .  minor  {21  —  16,  17)  was  studied  by  Irmisch  and  by  Buchenau. 
It  is  a  smaller  and  more  slender  plant,  the  leaves,  in  lateral  rows,  be- 
ing placed  aslant,  facing  upward,  the  upper  edge  being  therefore  farther 
from  the  apex  than  the  lower.  The  branching  is  essentially  as  in 
U.  vulgaris,  with  the  difference  that  the  chief  branch  (st2)  arises  at 


Francis  E.  Lloyd  —  224  —  Carnivorous  Plants 

the  lower  edge  of  the  leaf,  and  is  circinate  upwards.  In  the  axil  of 
the  leaf  there  are  two  shoots,  a  leafy  one  (sta)  circinate  towards  st2 
and  a  scape  (sc)  circinate  towards  sca.  sca  and  sc  may,  however,  occur 
without  SC2  which  is  much  less  frequent  in  incidence.  In  the  normal 
condition  therefore  when  the  scape  is  developed  there  are  at  its  base 
two  stolons,  one  from  the  chief  axis  and  one  from  the  base  of  the 
scape.  An  additional  one,  apparently  seen  by  Buchenau,  may  arise 
from  the  scape  base.  My  material  came  from  Eire  through  Professor 
H.  H.  Dixon. 

In  U.  gibba  {21  —  12,  20),  on  the  other  hand,  the  first  branch 
arises  at  the  upper  edge  of  the  leaf  base.  A  pair  of  mutually  facing 
and  circinate  branches  then  arise,  as  in  U.  minor,  to  produce  a  second 
branch  and  scape.  Secondary  scapes  arise  in  close  apposition  to  the 
primary  as  branches  of  the  bearing  stolon.  A  plant  sent  me  by 
Dr.  F.  W.  Went  from  Pasadena  behaves  similarly  as  do  also  U. 
emarginata  and  U.  exoleta  {21  —  18,  19).  In  these  species  the  scape 
produces  near  its  base  numerous  branches,  not  in  any  leaf  axil, 
which  bear  much  reduced  and  very  glandular  leaves.  These  are  rhi- 
zoids  {2 J  —  8).  Secondary  scapes  may  also  arise  in  the  axils  of  these 
{21  —  20). 

It  is  apparent  that  in  the  vulgaris  type  of  Utricularia  the  branch- 
ing has  distinct  pecuHarities.  One  sort  of  branch,  the  air-shoot,  never 
arises  in  any  relation  to  a  leaf.  The  chief  stolon  branch  (st2)  arises 
near  one  edge  of  a  leaf  base,  more  or  less  overlapping  the  axil,  but 
never  centered  on  it.  At  its  base,  opposite  the  leaf  axil,  arise  two 
buds,  one  a  stolon  and  the  other,  on  or  near  its  base,  an  inflorescence. 
In  some  species  a  dwarf  shoot  bearing  only  traps  arises  in  the  leaf 
axil,  behind  the  scape  and  its  companion  shoot. 

The  rhizoids  are  absent  from  some  species.  They  are  regarded  as 
anchoring  in  function,  but  are  only  very  ineffectively  so  in  the  floating 
species  (Glijck).  They  are  much  better  developed  and  are  much  more 
numerous  in  the  exoleta  type. 

In  the  mature  condition  the  original  position  of  the  primordia  is 
usually  completely  obscured  by  the  enlargement  and  mutual  distor- 
tion of  the  adjacent  parts.  The  embryonic  condition  was  studied 
by  Pringsheim  and  by  Goebel,  both  of  whom  recognized  the  ori- 
gin of  the  ''tendrils"  or  "air-shoots"  and  of  the  chief  stolon  branch. 

The  immediately  above  mentioned  species  {U.  gibba,  exoleta,  etc.) 
are,  in  contrast  to  vulgaris,  very  slender  plants  with  thread-like  stolons 
and  simple  leaves,  once  or  twice  divided,  or  even  thrice  {U.  eniar- 
gitiata)  {20  —  2).  The  internodes  are  long.  Obviously  closely  related 
to  these  are  two  African  species,  U.  cymbantha  OHver  and  U.  Ste- 
phensae  (in  Ms.)  which  deserve  special  mention.  These  are  minute 
plants  with  single  flowered  scapes.  The  method  of  branching  is 
simple.  A  stolon  branch  (st2),  always  single,  and  without  axillary 
buds,  arises  near  the  upper  edge  of  a  leaf,  but  more  or  less  axillary, 
while  the  scape  arises  from  or  near  to  the  upper  surface  of  the  stolon, 
and  near  or  somewhat  distant  from  a  leaf  and  certainly  in  no  definite 
relation  to  it  {23 — 12,  13,  21,  22). 

Submersed,  semi-submersed  but  anchored  forms  of  the  vulgaris  type.  — ■ 
These  fall  into  two  groups:    those  which  grow  (i)  submersed  but  send 


Chapter  XIII  —  225  —  Utricularia,  Biovularia 

out  shoots  of  two  kinds,  one  chiefly  trap-bearing;  or  (2)  on 
the  surface  of  the  wet  substrate,  sending  out  branches  which  pene- 
trate the  substrate,  bearing  traps  and  reduced  leaves.  These  emerge 
eventually.  To  the  former  belong  such  species  as  U.  ochroleuca,  U. 
Bremii  (Europe)  and  U.  minor  (in  both  hemispheres).  To  the  latter 
belongs  U.  intermedia  (20  —  4;  21  —  13,  14).  According  to  Glijck 
they  exhibit  a  good  deal  of  polymorphism  in  response  to  environmental 
differences.  So  far  as  they  have  been  investigated  the  method  of  branch- 
ing shows  no  peculiarities.  For  full  accounts  the  reader  may  be  referred 
to  Glijck's  book. 

Here  may  be  mentioned  the  peculiar  U.  clandestina  Nutt.  (23  —  i). 
This  is  a  lax  floater  of  the  general  appearance  of  an  undernourished 
condition  of  U.  vulgaris.  It  is  provided  with  special  branches  with 
reduced  foliage  and  traps,  these  occurring  sparingly  if  at  all  on  the 
leaves  of  the  main  stolons.  The  scape  of  the  inflorescence  arises  in 
connection  with  a  branch  (the  latter  in  or  near  the  axil  of  a  leaf) 
and,  in  addition  to  the  normal  inflorescence  bearing  normal  flowers, 
bears  at  its  base  usually  two  flowers  in  the  axils  of  scales.  The  ped- 
icels of  these  flowers  nod  downwardly  and  produce  seed  abundantly 
by  close  pollination  (presumably).  Sometimes  these  cleistogamous 
flowers  (which  never  emerge  from  the  water)  are  produced  without  an 
accompanying  scape  bearing  proper  flowers.  The  presence  of  scale 
leaves  allows  no  doubt  that  the  spur  on  which  they  are  borne  rep- 
resents an  undeveloped  inflorescence.  Its  position  with  relation  to 
a  leaf  and  branch  are  the  same  as  above  described  for  a  normal  in- 
florescence. 

In  this  species  also  air  shoots  are  to  be  found,  usually  emerging 
from  the  upper  surface  of  the  chief  axis  rather  near  to  an  inflores- 
cence.    They  are  absent  from  others  of  this  group  above  cited. 

A  few  forms  are,  with  the  exception  of  their  inflorescences  of  course, 
not  only  completely  submersed,  but  their  chief  stolons  are  buried  in 
in  the  substrate  of  sand  or  mud,  and  their  leafy  branches  or  merely 
their  leaves  emerge  into  the  supernatant  water.  Among  these  may  be 
counted  U.  resupinata  (N.  America),  U.  biloha  (Australia)  and  U. 
paradoxa  (in  Ms.)  (Angola). 

U.  resupinata  {23  —  8,  9). — ^  The  body  of  the  plant  consists  of 
horizontal  stolons  bearing  terete,  tapering  leaves  on  the  upper  surface, 
with  branch  stolons  emerging  laterally,  a  pair  at  each  node.  This 
is  a  wide  departure  from  what  we  have  seen  above,  and  foreshadowing 
what  we  shall  see  in  the  terrestrial  forms.  The  leaves  are  circinate 
backwards,  that  is,  away  from  the  apex  of  the  bearing  stolon,  as 
first  observed  by  Goebel  in  U.  orbiculata.  The  inflorescence  arises 
as  a  bud  in  the  forward  leaf  axil,  flanked  usually  by  stolon  buds. 
From  the  base  of  the  scape  a  number  of  rhizoids  spring  out  and 
penetrate  the  substrate.  The  method  of  branching  is  the  same  in 
U.  hiloha  and  U.  paradoxa  {21  —  22),  the  differences  being  in  their 
leaves.  In  the  latter  they  are  much  as  in  U.  vulgaris  but  emerge 
from  the  substrate  and  appear  as  little  trees  in  the  water.  The 
traps  are  borne  chiefly  on  the  stolons.  In  U.  hiloha  the  leaves  are 
articulated,  segment  with  segment  {21  —  21).  Sometimes  a  seg- 
ment  becomes  a  stolon,  iUustrating  the  indeterminate  morphological 


Francis  E.  Lloyd  —  226  —  Carnivorous  Plants 

character  of  these  parts  often  referred  to  in  the  literature  (Goebel). 
The  traps  occur  on  secondary  stolons,  rarely  on  the  leaves. 

Utricularia  grows  generally,  when  submersed,  in  still  waters. 
There  are  two  very  striking  exceptions  to  this  in  U.  neottioides  and 
U.  rigida,  the  former  South  American,  the  latter  from  Africa,  both 
tropical.  They  grow  in  running  streams,  attached  to  the  rocky  bot- 
tom, recalling  the  Podostemonaceae.  Creeping  on  the  rock  surface  and 
tightly  clinging  to  it  are  numerous  fleshy,  coral-like  stolons.  From 
these  arise  branches  which  are  leafy,  bearing  traps  (Luetzelburg 
1910)  and  finally  flowers.  The  traps  diverge  from  the  vulgaris  trap  in 
being  streamlined  —  to  yield  to  the  vocabulary  of  the  moment  —  being 
spindle  shaped,  the  stalk  at  one  end  and  the  mouth  at  the  other.  Ac- 
cording to  O.  Staff  (1906),  U.  rigida,  which  closely  resembles  U. 
neottioides,  has  no  traps.  None  of  the  Kew  specimens  showed  any,  and 
though  the  herbarium  specimens  of  U.  neottioides  did  not  show  them, 
Luetzelburg  found  them.  The  material  I  examined  was  collected  by 
him,  and  preserved  in  Goebel's  collection. 

Terrestrial  and  epiphytic  forms  of  the  vulgaris  type.  —  Of  the 
strictly  terrestrial  species  are,  e.g.  U.  suhulata  L.  (W.  Africa,  Amer- 
ica) and  U.  Rendlei  Lloyd  (Victoria  Falls).  These  grow  in  a  wet  sub- 
strate of  sand  or  sandy  soil,  and  consist  of  very  delicate  thread-like 
stolons  sending  up  simple  spatulate  or  ligulate  leaves  of  very  small  size 
and  often  difJEicult  to  see  when  collecting,  and  having  dehcate  scapes 
with  yellow  flowers.  U.  suhulata  shows  a  cleistogamous  condition  in 
Nova  Scotia  (Fernald).  The  method  of  branching  is  the  same  as  that 
in  U.  resupinata.  The  traps  are  numerous  on  the  stolons,  in  lateral 
rows  and  one  row  along  the  upper  surface  and  along  the  leaf  margins. 
The  leaves  face  away  from  the  apex  of  the  bearing  stolon. 

The  epiphytic  species  are  usually  large  and  bear  showy  flowers, 
and  are  often  grown  as  greenhouse  plants  among  the  orchids  with 
which  some  of  them  vie  in  beauty.  Mentioned  here  may  be  U.  reni- 
formis,  U.  nelumbifolia,  U.  montana,  U.  Humboldtii,  U.  longifolia, 
U.  Endresii  and  the  small  but  often  large  flowered  species  growing 
in  the  soil  such  as  U.  Dusenii  and  U.  Campbelliana,  all  from  Central 
or  South  America.  Some  species  grow  in  the  water  held  by  the  leaf 
rosettes  of  Tillandsias,  e.g.  tj.  nelumbifolia  in  the  Organ  Mts.  of  Brazil 
(Gardner  1846),  and  U.  Humboldtii,  on  the  Kaieteur  Savannah, 
British  Guiana  (Im  Thurn  1887),  both  of  which  grow  in  the  axils 
of  the  leaves  of  bromeliads  (Brocchinia  spp.).  These,  and  especially 
the  forms  which  grow  in  wet  moss  {U.  reniformis),  are  conspicuous 
for  their  thick,  coral-like  stolons,  the  anatomy  of  which  has  been  de- 
scribed by  Hovelacque.  The  method  of  branching  differs  with  dif- 
ferent species. 

U.  reniformis  is  on  the  evidence  of  its  branching  related  to  the 
terrestrial  types,  e.g.  U.  suhulata.  From  the  6  mm.  thick  stolon 
the  leaves  arise  in  a  row  on  the  upper  surface.  These  are  circinate 
backward,  and  have  a  reniform  blade  15  cm.  in  diameter.  The  bud 
of  the  scape  arises  in  the  leaf  axil  on  the  proximal  side  but  not  al- 
ways in  the  middle  point  indicating  a  degree  of  obliquity  in  the 
position  of  the  leaf  (Goebel).  The  branch  stolons  arise  in  single 
lateral  rows  (21  —  15).     Though  the  plant  is  of  stately  proportions, 


Chapter  XIII  —  227  —  Utricularia,  Biovularia 

the  traps  are  small.  There  are  no  rhizoids  judging  from  Hoehne's 
figure. 

U.  montana  has  leaves  and  branch  stolons  alternating  irregularly 
in  lateral  rows,  all  lying  in  the  horizontal  plane  of  the  bearing  sto- 
lon. Their  axillary  buds,  however,  He  obliquely  (Goebel).  Branch 
stolons  may  also  arise  from  the  upper  chief  stolon  surface.  The 
condition  here  recalls  that  of  U.  cornuia,  a  small  terrestrial  species. 

In  U.  longifolia  leaves  may  occur  both  laterally  and  on  the  up- 
per stolon  surface  (Goebel).  U.  Dusenii  Sylv.  is  a  small  delicate 
plant  resembling  U.  reniformis  in  habit  and  flower  structure,  and 
has  the  same  disposition  of  lateral  organs.  Instead  of  a  leaf  with 
attendant  stolons,  the  node  may  bear  three  leaves.  Rhizoids  are  pres- 
ent. 

The  traps  of  all  the  previously  mentioned  plants  adhere  strictly 
to  the  kind  found  in  U.  vulgaris.  Some  slight  differences  occur,  but 
these  will  be  better  described  in  a  following  chapter  devoted  to  the 
structure  of  the  trap. 

2.  The  Biovularia  type.  —  In  the  only  two  known  species  of  Biovula- 
ria, the  general  morphology  aligns  itself  with  that  of  the  vulgaris  type 
while  that  of  the  trap  stands  closer  to  the  U.  purpurea  type.  The 
species  are  B.  olivacea  (Wright)  Kam.  and  B.  minima  (Warm.)  Kam. 

Utricularia  olivacea  was  described  by  C.  Wright  in  Grisebach's 
Plantarum  Cubensium  .  .  .  (1866)  and  was  regarded  by  him  as  closely 
related  to  U.  gibba,  which  it  is  not.  Kamienski,  who  also  related 
it  to  U.  gibba,  made  it  the  type  of  a  new  genus,  Biovularia,  based 
on  the  number  of  ovules  present  in  the  ovary,  namely,  two,  arising 
from  the  bottom  of  the  ovary  and  not  from  an  enlarged  central  pla- 
centa, as  in  Utricularia.    We  call  it  therefore  Biovularia  olivacea. 

The  plant  consists  of  extremely  delicate  axes  bearing  traps  on 
long  stalks  in  the  place  of  leaves  (23^14-18).  The  latter  are  ab- 
sent, but  Wright  described  the  plant  as  having  them.  To  quote 
him:  "utriculis  obovoideis  ad  segmenta  folii  capillaceo-divisa  spar- 
sis."  This  error  seems  to  have  arisen  either  from  admixture  with 
other  floating  species  or  from  the  fact  that  the  long  stalks  frequently 
shed  the  traps  at  the  outer  end,  and  thus  appear  as  leaves.  Still 
they  are  not  divided.  When  branching  occurs  one  or  two  branches 
may  arise  from  a  node.  In  herbarium  material  (Cotype,  Herb. 
Smithsonian  Institution)  I  could  get  no  evidence  bearing  on  the  se- 
quence of  development. 

The  inflorescence  arises  as  a  branch  near  the  axil  of  a  trap.  This 
branch  assumes  considerable  thickness,  and  dominates,  in  the  mat- 
ter of  size  (diameter),  the  mother  stolon.  From  its  base  arise  two 
branches,  with  a  120  degree  angle  of  divergence,  one  somewhat  higher 
up  than  the  other.  From  the  apex  of  this  short  thick  spur  springs 
a  flower  pedicel,  which  is  surrounded  at  its  base  by  an  enveloping, 
involucral  scale  leaf.  Just  within  this  may  arise  a  second  pedicel 
in  the  axil  of  a  second  enveloping  scale.  In  exceptional  cases  the 
second  pedicel  may  arise  from  a  point  on  the  first  formed  pedicel 
a  considerable  distance  above  the  base.  A  third  pedicel  may  arise 
from  the  second.  We  are  evidently  dealing  here  with  a  compound  in- 
florescence in  which  the  chief  axis  is  suppressed. 


Francis  E.  Lloyd  —  228  —  Carnivorous  Plants 

The  ovate  sepals  continue  development  during  the  growth  of  the 
capsule,  becoming  deeply  denticulate  along  their  margins,  and  form 
a  graceful  vase-like  involucre  about  the  ripened  clavate  capsule. 

Usually  only  one  seed  develops.  The  narrowly  ovate  embryo  (0,28 
X  0.15  mm.)  conforms  to  type,  there  being  no  organs  differentiated. 
It  is  invested  by  a  loose  and  papery  covering  which  probably  remains 
attached  to  the  capsule. 

Biovularia  minima  growing  in  Lagoa  Santa,  Brazil  was  sus- 
pected by  Kameenski  (E.  und  P.  VI,  Lentihulariaceae)  to  be  spe- 
cifically identical  with  B.  olivacea,  both  subsumed  by  him  under 
Biovularia.  With  the  courtesy  of  the  Botanical  Museum,  Copen- 
hagen, I  have  been  able  to  examine  the  original  Warming  type  mate- 
rial, and  am  now  in  a  position  to  say  that  the  two  plants  are  specifically 
distinct  on  evidence  of  flower  structure. 

3.  The  purpurea  type  {20  —  3).  —  To  this  type  belongs  a  small 
group  of  highly  distinctive  plants  found  only  in  the  New  World.  They 
are  so  far  as  known  freely  floating  plants,  and  have  no  terrestrial 
analogs. 

The  plant  body  consists  of  stolons  which  send  out  at  the  nodes 
6  or  7  cylindrical  branches  forming  very  regular  whorls.  The  whole 
displays  a  minor  degree  only  of  dorsiventrality  which,  however,  is 
more  evident  at  and  near  the  growing  apex,  where  the  stolon  apex 
is  upwardly  strongly  circinate,  and  the  branches  develop  at  une- 
qual rates,  faster  below,  slower  above.  The  cylindrical  branches  in 
turn  can  produce  branches  of  the  third  order,  more  below  near  their 
bases  (about  4),  fewer  above  (two),  also  in  whorls,  but  unevenly 
spaced.  These  branches  are  more  definitely  and  evidently  dorsiven- 
tral  than  the  chief  stolon,  and  are  of  limited  growth,  and  each  branch 
is  constricted  at  the  end  into  a  slender  stalk,  bearing  a  trap.  At 
the  base  of  each  branch  there  is  an  abscission  zone,  as  there  is  also 
at  the  base  of  each  branch  of  the  third  order  and  at  the  base  of  the 
trap. 

Barnhart  correctly  described  this  plant  as  having  no  leaves, 
these  being  represented  by  verticillate  branches.  Luetzelburg,  how- 
ever, regards  them  as  leaves.  He  studied  a  species  which  he  called 
U.  elephas,  which  differs  from  U.  purpurea  in  having  only  two  to 
four  branches  instead  of  6-7.  He  examined  the  growing  tip  and 
believed  that  he  could  see  that  the  pair  of  lateral  "leaves"  were 
united  in  the  early  stage  of  development.  Goebel  accepted  Luet- 
zelburg's  interpretation.  Had  Luetzelburg  examined  U.  purpurea 
in  the  same  way,  the  evidence  would  probably  have  given  him  pause, 
since  six  or  seven  "leaves"  would  have  to  have  been  accounted  for. 
I  have  studied  both  U.  purpurea  and  U.  elephas  in  the  same  way, 
and  can  find  no  evidence  that  any  of  the  branches  are  fused  at  first. 
This  is  borne  out  by  the  distribution  of  the  vascular  strands,  which 
radiate  separately  out  from  the  central  cylinder.  Add  to  this  the  ver- 
ticillate arrangement  of  the  branches  of  the  third  and  fourth  order, 
and  it  is  clear  that  we  have  to  do  not  with  leaves  (even  in  the  re- 
stricted sense  this  term  is  used  when  speaking  of  Utricularia)  but  with 
branches. 

In    U.    elephas   as   in    U.    purpurea  the  scape  occurs   in    the    axil 


Chapter  XIII  —  229  —  Utricularia,  Biovularia 

of  a  more  or  less  aborted  branch  arising  on  the  upper  surface  of  the 
chief  stolon.  This  branch  always  remains  delayed  in  development. 
The  scape  produces  no  rhizoids,  nor  any  scale  except  in  the  inflores- 
cence. 

4.  The  dichotoma-monanthos  type.  —  To  this  type  belongs  a  goodly 
number  of  species  which  are  purely  Australasian,  and  so  far  known 
only  from  Tasmania,  Australia  proper  and  New  Zealand.  This  type 
is  not  present  in  the  recent  Brass  collections  of  New  Guinea  plants 
at  the  Arnold  Arboretum  of  Harvard  University.  They  are  at  once 
recognizable  by  their  winged  traps. 

The  series  includes  one  freely  floating  form,  U.  tubtdala,  and  while 
the  terrestrial  forms  are  readily  divided  into  two  groups,  those  with 
runner  stolons  {U.  dichotoma,  U.  monanthos,  etc.)  and  those  which 
have  only  anchoring  stolons  {U.  Menziesii,  U.  violacea,  U.  volubilis, 
U.  Hookeri),  never  runners,  and  which  are  confined  to  the  extreme 
S.  W.  of  Western  Australia.  These  have  been  regarded  by  Goebel 
as  primitive  forms,  but  the  only  fact  to  which  this  view  can  be  tied 
is  the  absence  of  runner  stolons.  Allied  and  included  with  these  is 
the  genus  Polypompholyx,  with  2  (or  probably  4)  species. 

Freely  floating  species.  —  The  only  freely  floating  species  of  this 
group  known,  and  that  only  from  herbarium  specimens  in  the  Mel- 
bourne Herbarium  (paratypes  at  Kew  and  at  the  British  Museum  of 
Natural  History),  to  which  I  had  access,  is  U.  tuhulata.  It  was  col- 
lected in  1875  by  W.  E.  Armit  in  "mountain  swamps  near  Cash- 
mere, 40-50  mi.  west  of  Rockingham  Bay"  in  Queensland,  but  never 
since.  In  general  appearance  it  resembles  U.  purpurea,  but  only 
superficially  owing  to  the  whorled  position  of  the  leaves  (j(5 —  10,  11). 

The  "rather  long"  stolons  bear  leaves  and  traps  in  whorls,  in  each 
whorl  four  leaves  alternating  with  four  traps  on  long  stalks,  so  ori- 
entated that  usually  two  of  the  leaves  he  on  one  side  and  two  on 
the  other  side  of  the  stolon,  the  traps  being  then  one  dorsal,  one 
ventral,  and  one  on  each  side.  Occasional  departures  from  the  rule 
may  be  observed  when  two  traps  may  stand  side  by  side,  or  two 
leaves.  In  the  mature  condition  the  leaves  and  traps  are  joined 
at  their  bases  to  form  a  complete  ring  of  tissue  surrounding  the  node 
from  which  they  arise.  A  dissection  of  several  terminal  buds  showed 
clearly  that  the  primordia  of  the  lateral  organs  are  all  quite  distinct 
at  first,  so  that  the  ring  supporting  them  is  secondary.  The  primor- 
dia appear  at  first  as  low  mounds  of  tissue  in  transverse  series  of 
eight,  at  first  indistinguishable  from  each  other.  At  about  the  sixth 
node  the  leaves  elongate  somewhat,  overpassing  the  traps  in  growth. 
The  apex  of  the  axis  is  long,  naked  and  slightly  circinate.  The  pri- 
mordia are  not  at  all  crowded.  In  the  axil  of  a  leaf  a  bud  which 
develops  into  a  branch  stolon  may  arise.  Traps  with  their  stalks  and 
leaves  attain  a  length  of  2  cm.  The  leaves  are  flat,  hnear  and  apicu- 
late,  the  trap  stalk  foliose  (Lloyd  1936c). 

According  to  von  Mueller,  the  scape  is  terminal  on  a  chief 
shoot  and  such  evidence  as  I  was  able  to  obtain  bears  out  this  view. 
I  dissected  one  terminal  bud  to  find  that  it  was  indeed  an  inflores- 
cence with  a  lateral  vegetative  bud.  Slender  at  the  base,  it  swells 
considerably  at  or  above  the  middle  to  form  a  spar-buoy  float.     The 


Francis  E.  Lloyd  —  230— Carnivorous  Plants 

scales  are  basifixed.  Mueller's  description  of  the  flower  does  not 
help  us  much,  but  the  few  specimens  I  saw  in  Melbourne  indicate 
clearly  that  the  flower  with  a  widely  spreading  lower  lip  conforms 
to  that  of  U.  dichotoma.  Its  color  is  bluish  ("albida-caerulescente"). 
U.  iuhulata  as  a  floating  plant  appears  to  stand  alone  in  regard 
to  the  morphology  of  the  leaves  and  traps.  If  the  upper  and  lower 
traps  of  a  whorl  were  absent,  we  would  be  tempted  to  homologize 
the  two  lateral  leaves  with  the  trap  between  them  with  the  condition 
found  in  U.  gibba,  but  that  would  be  pressing  the  matter  too  far. 

U.    dichotoma;     U.    monanthos    (23—19,    20).  — These    and   other 
related   species   are   characterized   by   the   fact   that   the   stolons   dis- 
play well  marked  nodes  and  internodes,  the  latter  usually  quite  naked, 
though   in   some   cases    {e.g.    U.   dichotoma)    traps    (facing   backward) 
may  arise  from  the  upper  surface  of  the  internode.     At  the  node  a 
leaf,  its  upper  surface  facing  backward,   arises  from  the  upper  sur- 
face and  from  each  side  of  the  stolon  near  the  leaf  base  a  branch 
stolon  and  a  trap.     From  the  proximal  leaf  axil  two  traps  and  a  bud, 
which  becomes  a  second  leaf,  usually  spring,  and  from  this  axil  also 
a  scape  can  arise.     Thus  these  forms  align  themselves  with  the  ter- 
restrial forms  in  general,  but  are    striking   for  the   more  readily  ob- 
servable emplacement  of  their  parts.     The  traps  are  generally  long 
stalked,  and  in  U.  dichotoma  often  emerge  slightly  from  the  surface 
of  the  wet  but  firm   substrate,   covered  by  a  water  film  in  normal 
times.     Hundreds  of  traps  could  be  seen  dotting  the  ground  at  Nar- 
rabeen,  N.  S.  W.,  using  a  lens  of  course.     An  additional  feature  of 
interest  in  this  group  is  the  widely  lacunate  structure  of  the  stolons 
and  petioles,  which  consist  of  scarcely  more  than  the  epidermis  and 
the  vascular  strand  with  a  few  collapsed  parenchyma  cells  clinging 
to  it  (much  as  in  Genlisea).    In  U.  monanthos,  which  grows  in  shallow 
water,  both  stolons  and  petioles  are  much  puffed  up.     U.  dichotoma 
has  very  small  spatulate  leaves  and  a  tall  scape;    U.  monanthos  rela- 
tively large  leaves  and  a  short  scape.     The  scapes  produce  anchoring 
stolons,  leaves  and  traps  on  their  bases. 

Another  group  of  species  of  the  dichotoma  type  is  composed  of 
plants  devoid  of  runner  stolons  and  consisting  solely  of  a  corm-like, 
vertically  growing  axis  springing  directly  from  the  seedHng  (22  —  25, 
26).  The  corm  is  very  slender  at  the  bottom  where  it  emerges  from 
the  seedling,  widening  toward  the  top,  having  below  the  structure 
of  a  stolon,  becoming  more  and  more  stem-like  as  in  Genlisea  (Warm- 
ing). This  puts  out  anchoring  stolons,  traps  and  leaves,  and  ter- 
minates in  an  inflorescence.  They  are  either  annuals  of  small,  very 
deUcate  structure  {e.g.  U.  capilliflora,  U.  Dunstani,  U.  albiflora) 
which  grow  in  wet  places  during  the  rainy  season,  chiefly  in  N.  W. 
Australia;  or  much  more  sturdy  plants,  but  of  the  same  plan  of 
structure,  all  but  one  {Polypompholyx  tenella)  of  S.  W.  Australia. 
These  latter  may  be  annuals  found  in  wet  sandy  soil  {P.  latifolia, 
P.  tenella)  or  in  very  shallow  water  {U.  violacea,  U.  Hookeri);  or  peren- 
nials in  wet  clay-sandy  soil  {U.  Menziesii)  or  in  water  {U.  volubilis). 
All  these  with  the  exception  of  U.  volubilis  and  U.  Menziesii  con- 
form in  morphological  features  to  Polypompholyx,  and  are  sufficiently 
indicated  in  the  figure  of  this  genus  (22  —  25,  26).     General  descrip- 


Chapter  XIII  —  231  —  Utricularia,  Biovularia 

tions  have  been  given  by  Goebel  in  his  Organographie.  The  perennial 
species  U.  Menziesii  and  U.  volubilis  require  some  further  description. 

U.  Menziesii  {20  —  8,  9;  2j  —  23,  24)  was  seen  growing  near 
Perth,  W.  A.  The  plant  body  consists  of  a  minute  corm  which  grows 
upwards,  dying  off  below.  From  it  spring  hundreds  of  minute  long 
stalked  traps  penetrating  the  soil  in  all  directions,  those  growing  up- 
ward coming  close  to  the  surface.  The  latter  are  covered  by  a  ro- 
sette of  long  petioled  spatulate  leaves,  from  the  middle  of  which 
emerges  early  in  the  wet  season  the  scape  (one  or  two)  with  unique, 
conspicuously  brilliant  red,  large-spurred  flowers.  My  material  allows 
the  inference  that  the  plant  begins  its  course  by  forming  from  the 
seedling  primary  stolon  an  oval  tuber  penetrating  deeper  into  the 
substrate.  From  a  lateral  bud  on  this  a  small  corm  is  formed,  which 
again  produces  penetrating  tubers.  At  length  a  substantial  corm  is 
formed  which  produces  near  the  apex  only  laterally  borne  tubers, 
two  to  four  in  number,  regarded  by  Goebel  as  water  storage  organs, 
tiding  the  plants  over  the  dry  season,  which  they  undoubtedly  do. 
They  contain  some  starch.  The  scape  is  always  borne  laterally, 
and  is  not,  as  in  the  annual  species,  a  finial  of  the  corm. 

U.  volubilis  {2j  —  25).  — I  found  this  growing  near  Albany,  W.  A. 
among  the  fibrous  matting  of  a  wet  swamp.  The  young  stages  are 
not  known.  The  plant  body  is  a  stout  upright  corm,  which  grows 
at  the  top  and  dies  behind.  It  bears  numerous  fihform  leaves  about 
3  cm.  long  and  numerous  long  stalked  traps,  often  with  leaf-Hke 
stalks.  The  scape  is  terminal,  but  the  corm  is  continued  by  a  large 
lateral  bud  at  the  base  of  the  scape.  There  are  also  produced  long 
anchoring  stolons  of  strong  texture,  bearing  traps  in  groups  of  three. 
The   scapes   are   very   long,    and   twine    about    supporting   reeds. 

In  the  foregoing  pages  an  account  of  the  general  structure  of 
the  plant  body  has  been  presented,  which  practically  covers  all  the 
major  varieties  of  habit.  It  is  still  insufficient  for  our  present  pur- 
pose in  not  embracing  all  the  types  of  Utricularia  as  indicated  by 
their  kinds  of  traps.  Those  still  to  be  mentioned  include  the  spe- 
cies U.  cornuta,  caerulea,  capensis,  orbiculata,  longiciliata,  and  sim- 
plex, taken  as  typifying  large  or  small  groups  of  species  having  traps 
of  pecuUar  structure,  to  be  mentioned  beyond.  While  some  of  these 
grow  in  shallow  water,  most  of  them  grow  in  wet  sandy  soil,  and  all 
have  in  common  the  general  structure  above  indicated  for  U.  sub- 
ulata,  with  some  slight  exceptions,  most  of  which  need  not  here  be 
amphfied  upon. 

U.  cornuta  is  an  American  plant  and  was  described  by  Schimper. 
Its  leaves  and  branch  stolons  are  borne  laterally  on  the  runner  stolons, 
with  no  very  regular  alternation. 

U.  caerulea  represents  a  large  number  of  Asiatic  and  African 
species  with  leaves  bearing  numbers  of  traps  and  branch  stolons. 
Goebel  (1891)  has  studied  this  type.  I  refer  to  the  plant  studied 
by  Goebel.  There  is  doubt  about  its  proper  specific  name 
(Barnhart),  but  as  I  had  access  to  the  same  material  as  used  by 
Goebel,  I  continue  to  use  the  name  he  used. 

U.  capensis  is  a  good  representative  of  a  number  of  African  and 
Asiatic  species,  the  latter  including  U.  rosea  and  U.  Warburgii,  both 


Francis  E.  Lloyd  —232— Carnivorous  Plants 

studied  by  Goebel.  This  group  is  represented  in  the  New  World 
by  U.  peltata  which,  Hke  some  cognate  species  in  Africa,  has  peltate 
leaves,  their  petioles  bearing  traps. 

U.  orbiculata,  U.  striatula,  U.  brachiata,  U.  multicaulis  and  pos- 
sibly some  others  are  minute  Asiatic  and  African  species,  most  epi- 
phytic in  wet  moss  on  leaves,  tree-trunks  or  on  rocks.  It  was  on  U. 
orbiculata  that  Goebel  first  noted  the  peculiar  back-facing  position 
of  the  stolon  leaves  and  the  coordinate  position  of  the  axillary  buds 
(Goebel,  1891).  This  species  produces  a  number  of  minute  spherical 
pearl-like  tubers  strung  along  its  stolons,  probably  for  water  storage 
(Goebel).  U.  longiciliata  (America)  is  unique  so  far  as  the  structure 
of  the  trap  is  concerned.  It  is  a  typical  small  terrestrial  species  sim- 
ilar in  habit  to  U.  subulata. 

U.  simplex  (S.  W.  Australia)  exhibits  a  rare  peculiarity^  of  pro- 
ducing its  scape  directly  from  the  margin  of  a  leaf,  a  habit  which 
it  may  have  in  common  with  its  relatives  U.  lateriflora  (S.  E.  Aus- 
traha)  and  U.  calliphysa  (Borneo)  (Staff  19 14),  another  species 
still  undescribed  from  India,  and  one  from  Ceylon.  Of  over  a  hun- 
dred complete  plants  of  U.  simplex  {23  —  7)  exhumed  from  a  sandy 
substrate  not  far  from  Albany,  W.  A.  not  one  showed  a  different 
origin  of  the  scape,  though  specimens  of  U.  lateriflora,  from  near 
Sydney,  N.  S.  W.,  showed  the  primary  origin  to  be  from  the  seedHng 
in  the  usual  way,  as  in  U.  Barnesii  mihi  in  ms.  {22  —  27).  Their 
traps  are  minute,  of  similar  structure,  but  display  specific  difierences. 

U.  globidariaefolia  and  a  few  similar  species  are  American.  They 
are  terrestrial,  rather  large  and  become  perennial  by  their  stout, 
tough  stolons.  Aside  from  their  considerable  stature,  growing  as  they 
do  among  the  grasses  and  reeds  of  such  habitats  as  the  Aripo  Savannah 
of  Trinidad,  they  display  no  striking  pecuharities  beyond  the  pos- 
session of  distinctive  traps. 

U.  Kirkii  is  an  African  species  with  apparently  few  associates, 
if  any,  and  has  a  distinct  form  of  trap.     It  is  of  the  usual  terrestrial 

habit. 

U.  nana  and  U.  Lloydii,  small  terrestrial  species,  are  unique  as 
regards  the  character  of  the  traps.  Both  S.  American,  each  appears 
to  share  its  peculiarities  with  no  other  species  yet  known. 

It  will  be  the  purpose  of  a  succeeding  chapter  to  consider  the 
mechanism  of  the  trap  and  the  various  peculiarities  of  the  various 
kinds  of  traps  characteristic  of  the  above  mentioned  types. 

—  {References  on  p.  26 f)  — 


Chapter  XIV 
THE    UTRICULARIA    TRAP 

General  description  of  the  trap ;  terminology.  —  Historical  account.  —  Anatomy  and  physi- 
ology of  the  trap.  —  Two  mechanical  types  of  trap  as  regards  the  posture  of  the  door  (the 
vulgaris-biovularia-purpurea  type.  The  capensis-caerulea-cornuta  type.  The  monanthos- 
dichotoma-Polj'pompholyx  type).  —  The  variety  of  traps.  —  Digestion;   the  fate  of  prey. 

In  the  account  of  the  character  of  the  various  sorts  of  Utricu- 
laria  already  given,  their  arrangement  in  groups  or  types  was  based 
on  the  character  of  the  traps.  In  order  to  explain  the  workings  of 
all  of  them  we  shall  begin  by  a  detailed  examination  of  the  longest 
studied  and  best  known,  that  of  Utricularia  vulgaris  and  its  close 
relatives.  What  we  learn  of  this  we  may  then  use  as  a  basis  for  com- 
parison with  other  types. 

The  traps  have  been  called  urceoli,  ampullae,  vesiculae,  utriculae, 
pitchers,  bladders,  or  traps.  The  most  widely  accepted  term,  blad- 
der or  vesicle,  or  the  Latin,  vesiaila,  is  not  so  bad  as  it  seems,  since 
a  bladder  has  an  opening  guarded  by  a  valve  in  the  form  of  a  sphinc- 
ter muscle  which  keeps  it  closed  except  under  certain  physiologi- 
cal conditions  when  the  muscle  is  temporarily  relaxed.  It  was  called 
a  pitcher  by  analogy  with  other  carnivorous  plants  (Staff),  but 
this  suggests  a  passive  trap,  and  it  is  anything  but  that.  Utricle 
(utriculus),  a  small  bottle  with  yielding  sides  (of  skin  or  leather), 
presumes  a  stopper.  "Trap",  used  in  this  work,  precisely  fits,  be- 
cause the  mechanism  is  that  of  an  elaborate  trap  which  is  set  automat- 
ically and,  after  capturing  prey,  resets  itself  repeatedly,  by  observation 
as  many  as  fourteen  times,  and  this  is  certainly  not  the  limit. 

A  description,  in  general  terms,  of  the  trap.  Terminology.  —  The 
vulgaris  type  of  trap  is  a  small  flattened  pear-shaped  hollow  body 
attached  to  the  plant  by  means  of  a  stalk  placed  laterally,  and  trun- 
cated obliquely  across  the  narrow  end,  where  occurs  the  mouth  of 
entrance.  The  stalk  side  is  ventral;  the  opposite  dorsal.  The  edge 
of  the  mouth  carries  in  most  cases  a  pair  of  branched  antennae,  and 
the  sides  some  slender  elongated  bristles  (27  —  7).  These  form  a  sort 
of  funnel  leading  to  the  entrance,  acting  as  guides  for  prey.  In  some 
species  these  appendages  are  absent  or  much  reduced  in  size  {U.  oli- 
gosperma).  Because  of  the  flattened  shape  we  may  speak  of  the  sides 
and  the  edge  of  the  trap.  The  sides  may  be  convex  or  concave, 
as  first  clearly  recorded  by  Erocher,  according  to  physiological  cir- 
cumstances. When  the  trap  is  set,  they  are  concave;  after  action,  they 
are  less  so,  and  the  trap  has  now  a  more  rounded  form.  Scattered 
over  the  outer  surface  there  are  numerous  small  spherical  glands,  de- 
void of  cuticle,  which  give  off  mucilage.  These  glands  are  common  to 
the  whole  plant  surface. 

The  entrance  {26  —  i,  2)  is  guarded  by  two  valves,  a  larger, 
the  door,  and  a  smaller  membranous  one,  the  velum  (Lloyd  1929). 
The  door  is  attached  to  the  trap   along  a  semicircular  hne  on   the 


Francis  E.  Lloyd  —  234  —  Carnivorous  Plants 

dorsal  part  of  the  entrance,  its  free  edge  hanging  and  in  contact  with 
a  firm,  semicircular  collar  or  threshold,  against  which  the  door  edge 
rests.  The  convex  outer  surface  of  the  door  bears  a  lot  of  longer 
or  shorter  stalked  mucilage  glands,  throwing  off  mucilage  and  sugar 
(Luetzelburg),  which  have  been  said  to  be  attractive  to  small  animals 
(Cyprids,  Daphneae,  etc.)  and  so  to  act  as  a  lure.  In  addition  it 
bears  four  stiff,  tapering  bristles,  based  near  the  free,  lower  door 
edge.  These  are  the  tripping  mechanism.  The  surface  of  the  thres- 
hold, against  which  the  door  edge  rests,  is  covered  with  a  "pave- 
ment epithelium"  of  glandular  sessile  cells  secreting  mucilage.  Along 
the  outer  edge  of  this  pavement  there  is  attached  a  thin  but  firm 
transparent  membrane,  the  velum,  which  lies  against  the  lower  edge 
of  the  door,  filling  in  the  chink  between  this  and  the  threshold. 

The  internal  surface  of  the  trap  carries  many  glandular  hairs 
{26  —  9-13),  with  two  or  four  projections,  the  former  on  the  inside 
of  the  threshold,  the  latter  everywhere  else  {26  —  2).  Darwin  called 
them  bifids  and  quadrifids.  The  capital  cells  are  devoid  of  cuticle. 
The  rest  of  the  surfaces  except  at  these  points  is  cuticularized. 

In  size  the  traps,  at  their  largest,  are  usually  not  more  than  5 
mm.  long;  in  the  majority  of  species,  3  mm.  long  and  less.  Their 
small  size  has  militated  against  readily  understanding  them. 

An  ample,  partly  incorrect  description  of  the  trap  was  furnished 
by  Benjamin  in  1848.  He  recalled  the  more  important  earlier  ob- 
servations: Meyen  had  thought  the  traps  open  in  the  mature  plant, 
ScHLEiDEN  thought  the  entrance  was  merely  guarded  by  hairs. 
Treviranus  realized  that  the  tightly  closed  door  prevents  the  es- 
cape of  air  when  inclosed  within  the  trap.  De  Clair ville  said  that 
the  door  opens  outwardly,  but,  as  Benjamin  pointed  out,  he  failed 
to  see  that,  if  this  were  the  case,  air  could  escape,  but  nothing  could 
enter.  Benjamin  himself  clearly  demonstrated  that  the  door  opens 
inwardly  —  he  could  push  it  in  with  a  needle  —  but  not  outwardly 
—  for  if  you  push  a  needle  against  it  in  this  direction  it  is  torn.  The 
function  of  the  traps  —  he  called  them  bladders  —  he  thought  to  be 
connected  with  the  supply  of  air  to  the  plant.  They  were  to  him 
air  reservoirs,  getting  it  from  the  water  through  the  four-armed  hairs. 
De  Candolle  (1832)  and  van  Tieghem  (1868)  believed  that  they 
had  to  do  with  the  floating  and  sinking  of  the  plant  in  spring  and 
autumn.  As  pointed  out  by  Goebel,  the  plants  float  just  as  surely 
after  the  bladders  are  removed.  What  had  not  then  been  observed 
is  that  normally  the  traps  hold  no  air,  but  that  this  enters  when 
the  plant  is  raised  out  of  the  water.  As  Cohn  remarked,  the 
failure  to  understand  the  traps  arose  out  of  a  wrong  point  of  view. 
He  and  Darwin  adopted  another  only  in  turn  to  prove  wrong.  Cohn 
recorded  finding  various  forms  of  Daphnia  and  Cyclops  in  the  traps 
of  a  herbarium  specimen.  He  then  put  a  living  sprig  in  an  aquar- 
ium where  it  grew  rather  feebly  for  some  time.  There  was  no  prey 
in  the  traps  —  none  in  the  water.  He  then  added  some  Ostracods 
from  a  culture,  and  next  morning  many  of  them  had  been  caught 
in  the  traps.  But  Cohn's  observations  did  not  stand  alone;  the 
brothers  Crouan  (1858)  had  recorded  the  presence  of  small  beasts 
in  the  traps.    In  America,  in  1873  Mrs.  Mary  Treat  and  a  coworker 


Chapter  XIV 


235 


The  Utricularia  Trap 


found  entomostraca  in  the  traps  of  U.  deistogama.  Prompted  by 
this  she  made  a  careful  examination  to  see  if  she  could  observe  the 
method  of  capture.  She  thought  in  1875  that  the  animals  "open  the 
door  and  walk  in",  agreeing  with  Darwin  and  with  Cohn  that  prey 
push  in  the  door,  which  then  closes  and  prevents  escape.  In  her  1876 
account  she  re\ased  her  conclusions,  for  she  then  found,  in  U .  purpurea, 
that  prey  is  suddenly  engulfed,  as  if  drawn  into  a  "partial  vacuum". 
Not  seeing  that  the  trap  walls  change  their  posture,  she  was  ignorant 
as  to  how  the  vacuum  could  be  achieved;  yet  her  idea  foreshadowed 
the  discovery  to  be  made  in  191 1  by  Brocher.  Mrs.  Treat  learned 
through  Dr.  Asa  Gray,  in  correspondence  with  Charles  Darwin, 
that  the  latter  was  making  similar  studies;  so  that  it  is  of  interest  to 
see  that  Cohn,  Darwin  and  Mrs.  Treat,  whom  Darwin  later  quoted, 
were  arriving  at  similar  conclusions  at  the  same  time  independently. 
She  further  saw  evidence  that  larvae  were  digested  in  the  course  of 
48  hours.  '"'I  was  forced  to  the  conclusion  that  these  httle  bladders 
are  in  truth  like  so  many  stomachs,  digesting|and  assimilating  animal 
food",  she  remarked. 


Fig.  7.  —  Copies  of  the  original  drawings  of  Cohn  (left)  and  of  Brocher,  of  the  en- 
trance of  the  trap  of  Utricularia  vulgaris. 

Cohn's  and  Darwin's  conceptions  of  how  the  trap  works  were 
identical  as  is  shown  by  their  descriptions.  Cohn  said  that  "the 
valve  is  held  against  the  threshold  by  a  pressure  of  water  within  the 
trap,  but  that  it  is  easy  to  open  by  pushing  it  inwards.  This  ar- 
rangement makes  it  understandable  that  living  water  animals,  en- 
tering the  peristome,  lift  the  valve  and  without  difficulty  enter  into 
the  hollow  cavity  of  the  bladder,  whence  they  cannot  escape  since 
the  valve  opens  only  inwardly,  not  outwardly."  And  Darwin  spoke 
in  the  same  manner,  saying  that  "animals  enter  merely  by  forcing 
their  way  through  the  slit-Hke  orifice;  their  heads  serving  as  a  wedge." 
GoEBEL  accepted  this  explanation,  as  did  Meierhofer  and  Luet- 
ZELBURG.  An  impressive  drawing  by  Goebel  as  well  as  that  by 
Cohn  (Text  fig.  7),  though  incorrect,  are  still  used  as  illustrations. 
It  is  clear  that  up  to  this  time  the  trap  was  regarded  as  a  passive 
mechanism,  the  animal  caught  having  to  do  the  work  of  forcing  en- 
trance. We  must  add  however  that  it  was  thought  that  the  door 
was  either  forced  against  the  threshold  by  a  "m  a  tergo",  the  water 


Francis  E.  Lloyd  —  236  —  Carnivorous  Plants 


pressure  (Cohn),  or  by  its  own  property  of  elasticity,  the  latter  im- 
plicit in  all  Darwin's  statements.  It  remained  thus  till  191 1  when 
a  Swiss  entomologist,  Brocher,  became  interested  in  Utricularia. 
Pointing  out  that  the  view  just  above  expressed  is  but  an  hypothe- 
sis, since  no  one  had  actually  observed  what  happened,  Brocher 
tried  to  do  this. 

In  a  series  of  experiments  (Czaja  does  him  the  injustice  of  say- 
ing he  did  none)  Brocher  established  the  following  points,  to  his 
own  satisfaction.  When  an  animal  is  caught  it  always  disappears 
very  suddenly.  Darwin  and  Busgen  (1888)  had  all  seen  this 
and  recorded  their  observations,  but  had  drawn  no  correct  inference 
therefrom.  Further  that,  at  the  moment  of  this  disappearance,  the 
trap  gives  a  spasmodic  jump,  and  widens  a  little,  from  which  Brocher 
concluded  that  the  trap  sucks  in  the  prey  (57  —  4,  6,  9).  This  observa- 
tion was  of  fundamental  importance.  He  was  able  then  to  explain 
why,  when  a  leaf  is  raised  out  of  the  water,  the  traps  are  often  found 
to  contain  air  bubbles,  whereas  before  they  were  absent.  On  lifting 
a  plant  from  the  water  he  could  hear  a  "  crepidulation"  (an  observa- 
tion made  independently  by  others)  explained  by  the  swallowing  of 
air  by  reacting  traps.  He  saw  that  in  traps  which  had  not  reacted, 
the  sides  were  concave,  but  after  reaction  were  flattened  or  slightly 
convex.  Finally  he  found  that  he  could  cause  a  trap  to  react  by 
''titillating"  the  door  bristles  with  a  needle  point,  and  that  when 
this  was  accomplished  there  was  each  time  a  spasm  of  movement, 
and  a  change  in  profile.  These  observations  by  Brocher,  made  with 
exactitude,  furnished  a  point  of  view  which  finally  led  to  the  correct 
explanation  of  the  workings  of  the  trap. 

Passing  on  to  hypothesis,  he  supposed  that  the  collapsed  form 
of  the  trap  is  explained  by  the  principle  that  the  rate  of  develop- 
ment of  the  tissues,  being  quasi  superficial,  is  greater  than  the  rate  of 
expansion  of  the  volume.  To  the  extent  that  the  walls  are  depressed, 
the  tensions  of  their  tissues  are  augmented  and  thus  they  try  the 
more  to  take  a  normal  position,  that  is,  to  obliterate  their  re-entrant 
curvatures.  The  walls  are  therefore  in  a  position  of  unstable  equilib- 
rium, during  which  the  interior  is  in  a  state  of  "negative",  that  is, 
reduced  pressure.  The  proof  of  this  is  the  fact  that,  when  punc- 
tured, the  walls  take  up  the  normal  position,  dilating  to  a  maximum. 
This  could  not  be  possible  if  the  structure  of  the  trap  is  as  repre- 
sented in  the  textbooks,  he  remarked  at  this  point,  since  a  simple 
check  valve  could  not  preserve  the  reduced  pressure.  He  further 
supposed  that  the  door  is  strongly  curved,  especially  transversely, 
and  that,  because  of  the  curvatures  of  the  wall,  it  is  held  firmly  against 
the  lip,  and,  with  the  addition  of  mucilage,  is  thus  rendered  a  water- 
tight valve  (Text  fig.  7).  In  order  that  the  equihbrium  thus  pre- 
served may  be  upset,  Brocher  assumed  that  the  door  is  endowed  with 
a  certain  "sensibility"  and  "contractihty",  so  that,  on  touching  the 
bristles,  it  can  shrink  a  little,  and  thus  allow  the  water  pressure  to  exert 
its  force.  An  animal  doing  this  would  be  swallowed  with  the  inrushing 
water.  That  minute  fish  are  sometimes  caught  by  the  tail  shows  that 
it  is  not  because  they  try  to  get  in,  but  that  merely  by  the  flick  of  the 
tail,  they  have  stimulated  the  trap.    The  action  of  the  door  or  "oper- 


Chapter  XIV  —  237  —  The  Utricularia  Trap 

culum"  is  so  rapid,  Brocher  observed,  that  it  closes  before  the  walls 
can  more  than  partly  expand,  so  that  the  trap  may  act  again,  but 
this  remained  questionable.  It  was  admitted  that  the  contents  of 
the  vesicle  might  be  absorbed  by  the  "rhizoids"  (quadrifid  hairs), 
in  which  case  the  walls  would  again  be  drawn  in,  and  the  trap  re- 
sensitized.  But  Brocher,  not  being  a  botanist,  was  too  modest  to 
undertake  to  solve  this  part  of  the  problem. 

Ekambaram  (1916,  1918,  1926)  in  India  made  observations  on 
the  traps  of  U.  flexiwsa  (similar  to  U.  vulgaris),  which  substantiated 
those  of  Brocher  above  mentioned,  though  apparently  in  ignorance 
of  this  author's  work.  That  is,  Ekambaram  recognized  the  two  states 
of  the  trap,  one  with  concave  and  one  with  convex  sides,  and  that 
in  the  latter,  when  the  "irritable"  hairs  are  touched  by  a  prowling 
animalcule,  it  is  sucked  into  the  trap  with  the  inflowing  water.  It 
had  been  noticed  by  him  also  that  when  the  whole  plant  is  lifted 
from  the  water  there  can  be  heard  "light  crackling  sounds  like  the 
ticking  of  a  watch"  and  this  was  referred  to  the  action  of  the  traps 
when  released,  presumably  by  water  films.  When  pushed  in  by  the 
water,  the  door  becomes  inverted  and  boat  shaped,  with  the  "irrita- 
ble" hairs  folded  up  into  the  groove  {26  —  7).  The  movement  of  the 
door  he  considered  to  be  due  to  the  momentary  loss  of  turgidity,  as 
quickly  regained  leading  to  closure,  but  he  does  not  offer  any  evidence 
for  this.  The  irritable  hairs  he  mistakenly  thought  to  have  the  same 
structure  as  those  of  Aldrovanda. 

Ekambaram  was  able  to  reset  the  trap  by  carefully  pressing  out 
the  water  by  compressing  its  sides,  but  it  does  not  appear  that  he 
understood  that  the  trap  can  automatically  reset  itself.  The  escape 
from  the  walls  of  intercellular  air  during  this  operation  must  have 
been  accident,  and  can  have  no  bearing  on  the  matter.  Merl  found 
the  contrary. 

At  about  the  same  time  Withycombe,  a  British  student,  announced, 
in  1916,  "that  the  bladders  of  Utricularia  ...  2lXQ  not  passive  traps, 
but  that  they  capture  prey  by  active  movement  in  response  to  stim- 
ulation. A  bladder  becomes  sensitive  to  contact  after  its  walls  be- 
come concave  on  each  side.  Then,  on  touching  certain  short  hairs 
at  the  mouth  of  the  bladder,  the  lateral  walls  spring  outwards,  be- 
coming somewhat  convex,  and  so  drawing  a  current  of  water  into  the 
bladder  which  swept  with  it,  of  course,  any  body  sufficiently  hght  to 
be  sucked  in."  Again,  this  observation  was  made  quite  independently, 
as  Withycombe  learned  of  Brocher's  work  only  ca.  1922  through 
Merl.  Nor  did  he  yet  know  of  Ekambaram's  observations.  In  his 
paper  of  1924  Withycombe,  thinking  Brocher's  explanation  of  the 
working  of  the  trap  valve  inadequate,  agreeing,  however,  about  the 
matter  of  "negative"  pressure  and  its  results,  advanced  the  idea  that 
the  edge  of  the  valve  or  door,  instead  of  being  merely  pressed  against 
the  collar  or  threshold  (Brocher),  is  caught  in  a  groove  from  which 
it  can  be  released  only  by  an  upward  movement.  This  groove  stands 
in  front  of  the  zone  of  specialized  cells  (see  beyond)  and  is  as  deep 
as  these.  "A  certain  amount  of  mucilage  is  secreted  apparently  by 
the  middle  layer,  and  this  makes  a  complete  watertight  fitting  of  the 
valve."    Here  is  a  specific  attempt  to  account  for  the  hermetical  seal- 


Francis  E.  Lloyd  —  238  —  Carnivorous  Plants 

ing  of  the  door  mechanism,  and  though  as  it  will  appear  a  mistaken 
one,  the  idea  was  correct.  The  internal  water  is  absorbed  by  the  quad- 
rifid  hairs,  so  that  the  trap  can  be  reset  by  setting  up  anew  the 
strains  expressed  in  the  convexity  of  the  side  walls.  In  his  experience 
this  required  about  30  minutes.  The  action  of  the  door  is  due,  he 
says,  to  its  irritabihty,  and  the  slender  four  hairs  inserted  in  the  door 
are  the  only  organs  which  can  be  stimulated.  Irritability,  however,  was 
not  proven  to  exist. 

Merl's  work,  above  mentioned,  appeared  two  years  before 
Withycombe's  second  paper.  He  set  out  from  Brocher's  important 
observation  that  on  stimulation  the  walls  of  the  trap  expand,  drawing 
in  water  in  the  capture  of  prey,  but  further  showed  that  the  operation 
can  be  repeated  again  and  again.  During  three  days  he  observed  the 
trap  to  act  thirteen  times.  Merl  correctly  determined  also  that 
traps  which  contain  some  air  can  react,  contrary  to  Brocher's  view 
(but  this  could  happen  only  if  the  bubble  of  air  in  the  trap  is  not  too 
large!).  It  is  only  if,  owing  to  the  shape  of  the  trap,  the  bubble  can 
be  moved  or  distorted,  that  this  can  happen.  The  time  required  for 
resetting  in  U.  flexuosa  was  found  to  be  a  minimum  of  15  minutes, 
but  full  resetting  requires  about  30  minutes.  In  U.  purpurea  {jy  — i) 
it  takes  upwards  of  two  hours  (Lloyd  1933a).  It  was  shown  by  Merl 
that  the  full  expansion  of  the  trap  sides  takes  place  when  the  door  is 
forced  open  or  when  the  wall  is  punctured.  The  reverse  of  this,  the 
sucking  in  of  the  side  walls,  is  more  pronounced  the  longer  a  period 
of  non-stimulation,  until  of  course  the  cohesion  of  the  internal  water 
sets  a  limit.  Apropos  of  Brocher's  note  to  the  effect  that  on  removal 
of  a  plant  out  of  the  water  a  clicking  sound  was  noticed  due  to  the 
swallowing  of  air  by  the  traps,  Merl  was  able  to  do  this  without 
setting  off  all  the  traps.  Some  of  them  did  not  react  and  remained 
unaffected  under  a  bell  glass.  He  was  then  able  to  procure  the  re- 
action by  touching  the  bristles.  Aside  from  furnishing  him  an  argu- 
ment against  Brocher's  theory  that  the  compression  of  the  trap  walls 
is  due  to  "atmospheric  and  hydraulic"  pressure  (Merl's  statement 
concerning  this  view  seems  incorrect)  the  experiment  shows  that  it  is  on 
general  grounds  not  surprising  that  some  species  are  not  submersed, 
species  the  traps  of  which  normally  exist  and  act  in  moist  air,  sur- 
rounded by  wet  moss,  detritus  or  sandy  soil.  The  action  of  the  traps 
on  lifting  from  water  is  therefore  due,  it  is  suggested  by  Merl,  to  the 
action  of  water  films  on  the  bristles  of  the  door  and  not  to  the  mere  re- 
lease from  water  pressure. 

Merl  then  tried  to  determine  whether  the  reaction  of  the  trap, 
or  specifically  of  the  door,  is  an  irritable  response.  He  could  not 
procure  reaction  by  wounding  or  by  electrical  stimulation.  As  to  the 
temperature  relations  he  found  that  the  traps  reacted  as  long  as  they 
remained  alive,  and  that  by  chemical  means  no  condition  of  rever- 
sible inactivity  (rigor)  could  be  induced.  Incidentally  he  found  that 
the  trap  is  so  completely  sealed  by  the  door  that  there  is  no  entrance 
even  for  dyes,  such  as  eosin  and  methylene  blue,  so  long  as  the  dyes 
do  not  induce  death  of  the  trap.  Nevertheless  Merl  could  not  quite 
rid  himself  of  the  feehng  that  the  mechanism  is  irritable,  and  would 
have  adopted  this  view  if  so  much  evidence  "had  not  spoken  against 


Chapter  XIV  —  239  —  The  Utricularia  Trap 

it."  Among  this  evidence,  he  found  that  during  action  there  was  no 
disturbance  of  the  air  in  the  intercellular  spaces,  which  would  occur 
if  there  was  an  extrusion  of  water  into  them  such  as  occurs  in  irri- 
table tissues.  In  spite  of  inimical  evidence,  however,  Merl  inclined 
to  think  that  the  bristles  are  irritable  hairs  analogous  to  those  of 
Dionaea  and  Aldrovanda  (as  had  Ekambaram  and  Brocher).  He 
proposed,  however,  the  only  alternative  theory,  a  purely  mechanical 
one.  The  four-armed  hairs  withdraw  the  water  from  the  interior 
of  the  trap,  thereby  setting  up  a  tension,  the  walls  responding  to 
the  draft  by  cohesion  of  the  water.  The  highly  elastic  door,  the  free 
edge  of  which  rests  firmly  against  the  threshold,  opposes  this  draft 
and  comes  into  a  position  of  labile  equilibrium,  which  must  be  dis- 
turbed "by  the  slightest  movement  or  by  shrinkage"  of  the  (door) 
cells,  to  allow  the  walls  to  retract  into  their  relaxed  position.  Even 
now  he  could  not  quite  exclude  a  certain  irritabihty  as  a  capstone 
of  the  bridge.     This  view  was  to  be  championed  later  by  Kruck. 

Working  at  the  same  time,  independently  of  Merl,  Czaja  exam- 
ined the  problem  of  the  Utricularia  trap.  His  publication  was  but 
a  trifle  later  than  Merl's.  Proceeding  from  the  same  point  of  at- 
tack, Czaja  agreed  with  Merl  that  the  trap  could  repeat  its  action, 
and  could  reset  itself  in  a  short  period  of  15  to  30  minutes  and  that 
the  reaction  (on  suitable  stimulation)  takes  place  very  suddenly. 
The  concave  sides  then  became  much  less  so.  The  door  in  this  re- 
action opens  to  a  narrow  slit,  and  closes  as  suddenly  as  it  opens 
(neither  of  which,  however,  is  quite  true)  allowing  the  entrance  of  a 
stream  of  water.  The  process  is  released  by  touching  the  bristles. 
By  chemical  means  Czaja  could  not  decide  definitely  on  the  nature  of 
the  mechanism,  and  this  left  him  for  the  moment  at  the  same  point 
as  it  did  Merl.  With  respect  to  the  anatomy  of  the  trap,  he  exam- 
ined first  the  closure  of  the  trap  by  the  door,  in  order  to  settle  the 
question  of  the  path  of  the  internal  water  when  the  trap  is  exhausted 
as  it  must  be  when  the  walls  pass  from  the  less  to  the  more  concave 
posture.  He  determined  that  the  entrance  is  hermetically  sealed.  The 
proof  consisted  in  inserting  a  fine  hair  beneath  the  door  edge,  when 
the  trap  could  not  again  set  itself.  When  the  hair  was  withdrawn, 
again  the  trap  became  effective.  Further  proof  was  supplied  by  the 
fact  that  Congo  red  and  methylene  blue  never  entered  healthy,  but  only 
damaged,  traps.  All  this  he  beHeved  points  to  the  membrane,  or  rather 
the  wall  of  the  trap,  as  important. 

As  had  been  demonstrated  by  Cohn  in  1875,  the  walls  of  the  trap, 
if  set  free  to  act  by  removing  inhibiting  structures  (the  threshold  and 
contiguous  walls),  will  expand.  Because  of  their  structure  and  the  tur- 
gidity  of  their  cells  they  always  strive  to  take  an  outwardly  convex 
form.  Substances  which  can  reduce  their  turgor  (5%  KNO3)  put  the 
trap  out  of  commission.  On  the  other  hand  substances  which  cannot 
penetrate  but  which  withdraw  the  water  from  the  trap  (glycerine, 
cane  sugar)  can  up  to  a  certain  limit  of  concentration  reset  the  trap 
but  if  in  too  great  concentrations,  cause  its  total  collapse.  The  reset- 
ting of  the  trap  is  therefore  the  result  of  withdrawing  water  from  its 
lumen,  and  not  of  direct  participation  of  the  walls  which  would  in- 
volve turgor  changes. 


Francis  E.  Lloyd  —  240  —  Carnivorous  Plants 

This  is  made  possible  by  the  tight  application  of  the  door  edge 
to  the  threshold  (specifically,  to  the  layer  of  epithelium  on  the  top 
of  the  threshold)  enhanced  by  the  mucilage  which  has  an  added 
sealing  effect.  Since  the  cells  of  the  wall  are  not  plasmolysed  by 
glycerin  etc.,  water  is  not  withdrawn  from  these  cells  but  only  from 
the  lumen  without  changes  in  turgor.  This  is  what  happens  in  na- 
ture. The  setting  of  the  trap  results  from  the  withdrawal  of  water 
from  the  lumen.  The  only  agent  for  this  is  the  action  of  the  four- 
armed  hairs.  It  is  allowed  that  some  water  may  penetrate  through 
the  walls  inwardly  but  at  a  slower  rate  than  that  at  which  it  is  thrown 
off,  for  otherwise  it  would  lead  to  overtension,  and  this,  he  held, 
would  bring  the  trap  into  a  condition  unfavorable  for  prompt  action. 

CzAjA  holds  that  the  withdrawal  of  water  results  not  only  in  the 
change  in  position  of  the  walls,  but  that  this  results  in  turn  in  a 
cramping  effect  on  the  door,  forcing  it  against  the  threshold  more 
tightly  and  so  effectively  increasing  its  watertightness,  an  idea  held 
by  Brocher,  but  which  is  untenable  in  the  hght  of  the  structure  of 
the  walls,  which  are  thin,  acting  as  hinges  near  the  threshold  {26  — 
3).  When  the  trap  is  in  the  set  posture,  the  walls  concave,  and  the 
door  tightly  in  contact  with  the  threshold,  the  bristles  stick  out  at 
an  angle  in  such  position  that  on  touching  them  the  edge  of  the  door 
is  disturbed  and  a  narrow  opening  is  formed  between  the  door  edge 
and  the  threshold,  through  which  water  is  drawn  in  by  the  expanding 
walls.  The  action  is  mechanical.  In  support  of  this  Czaja  records 
that  it  is  easier  to  fire  the  trap  if  the  bristles  are  swept  from  above 
downwards  than  transversely  to  this  direction.  This  can  mean  only 
that  the  leverage  is  more  effective  in  disturbing  the  door  edge  when  the 
levers  are  moved  in  one  direction  than  another  and  rules  out  mere  irri- 
tability. Firing  the  trap  is  due  to  the  deformation  of  the  door  edge 
and  the  consequent  lifting  of  it  from  the  threshold  allowing  water 
pressure  to  act.  For  the  rest,  Czaja  did  much  experimentation  show- 
ing that  the  trap  is  surrounded  by  a  selectively  permeable  membrane 
but  Prat  (1923)  found  that  the  entire  plant  is  protected  by  this 
membrane. 

Czaja  was  the  first  to  take  a  definite  stand  that  the  trap  action 
is  mechanical,  aside  of  course  from  the  water-extruding  power  of  the 
walls,  and  the  general  condition  of  turgidity.  That  is,  the  springing 
of  the  trap  is  purely  mechanical.  This  was  opposed  to  the  views 
of  Brocher,  Ekambaram  and  Withycombe,  and  to  Merl  insofar 
as  he  allowed  the  question  to  hang  in  the  balance.  Hegner  (1926) 
(not  knowing  of  the  work  of  Brocher,  Merl  or  Czaja)  made  inde- 
pendently the  observations  as  to  the  method  of  catching  prey  re- 
corded by  Brocher,  noting  its  rapidity,  but  did  not  venture  into 
the  question  of  the  method  of  function  of  the  bristles.  Thus  Czaja 
was  left  the  sole  champion  of  the  view  that  the  whole  capturing 
action  of  the  trap  is  mechanical,  but  he  was  not  to  go  unchallenged; 
for  Miss  M.  Kruck  in  1931  undertook  to  prove  the  contrary,  but, 
to  state  it  abruptly,  she  quite  failed  (Lloyd  1932&).  In  the  first 
place  her  presentation  of  the  structure  of  the  trap  was  askew  and 
it  was  patent  from  her  figures  that  she  did  not  grasp  the  anatomical 
facts.     The  drawings  showed  initial  and  final  positions  of  the  door, 


Chapter  XIV  —  241  —  The  Utricularia  Trap 

after  stimulation  and  reaction,  which  simply  do  not  occur.  The 
physiological  evidence  consisted  in  the  observation  of  the  extent  and 
position  of  intercellular  spaces  in  the  tissue  of  the  door  before  and 
after  response.  To  meet  this  I  reproduced  photographic  evidence 
which  showed  clearly  that  such  changes  do  not  occur,  though  it  is 
evident  that  changes  in  the  mere  distribution  of  air  might  occur 
without  vitiating  my  evidence.  Again  Kruck  stated  that  the  cells 
of  the  door  change  their  shape,  but  this  was  found  equally  illusory. 
In  the  course  of  response  she  stated  that  the  bristles  lose  water, 
supplying  a  stimulus  to  the  neighboring  cells  of  the  door  which  re- 
spond in  like  manner,  with  the  result  that  the  shape  of  the  cells 
of  the  door  changes  through  loss  of  turgor,  but  evidence  for  this 
was  quite  absent.  She  further  allows  15  minutes  for  the  restitution 
of  irritabihty,  in  this  agreeing  with  Czaja  and  Merl,  both  of  whom 
allowed  this  as  the  time  necessary  for  the  withdrawal  of  sufficient 
water  to  set  the  mechanism.  If  Kruck  was  right,  it  is  not  clear 
why  the  restoration  of  irritabihty  should  not  proceed  when  a  trap 
is  punctured,  but  this  never  occurs.  Most  impressive  is  the  fact  shown 
first  by  Ekambaram,  repeated  by  myself,  that  by  careful  expulsion 
of  the  water  from  a  trap,  it  may  be  reset  repeatedly  without  allow- 
ing time  for  the  restoration  of  irritability,  unless,  to  be  sure,  an  im- 
mediate restoration  is  predicated.  The  claim  that  the  bristles  are 
irritable  was  shown  to  be  not  true  by  first  killing  them  with  iodine, 
after  which  they  could  procure  response  on  touching  (Lloyd  1932ft). 
It  should  here  be  recalled  that  Withycombe  observed  that  this  re- 
sponse could  take  place  even  in  traps  which  had  lain  for  a  half-hour 
in  Bouin's  picro-formal  solution.  It  seems  clear  that  Kruck  failed 
in  supporting  her  contention.  The  evidence  points  to  the  contrary, 
that  the  action  of  the  door  is  purely  mechanical,  always  granting 
the  turgidity  of  the  component  cells,  devoid  of  which  they  could  not 
give  to  the  door  the  necessary  properties. 

The  walls,  because  of  their  activity  in  excreting  water  from  the 
trap  lumen,  are  an  important  part  of  the  mechanism.  The  total 
amount  which  a  trap  throws  out  amounts  to  88  %  according  to  Hegner 
(1926),  much  less  according  to  Nold.  Such  figures  are  in  any  event 
not  important  since  the  total  amount  excreted  depends  on  the  type 
of  trap.  In  U.  purpurea  it  must  be  much  more  than  in  U.  vulgaris. 
That  they  do  excrete  water  is  all  we  need  to  know  to  explain  the 
action  of  the  trap,  and  this  was  first  demonstrated  by  Brocher, 
later  independently  by  others,  Ekambaram,  Withycombe,  Hegner, 
and  possibly  Hada  (but  who  had  seen  Hegner's  paper).  It  may  be 
emphasized,  however,  that  this  action  can  go  on  when,  as  a  result 
of  the  introduction  of  much  food  material,  including  salts,  in  the 
form  of  the  bodies  of  water  animalcules,  the  osmotic  pressure  of  the 
internal  fluid  reaches  a  considerable  but  never  measured  figure.  This 
cannot  be  overdone,  however,  for  if  glycerine  be  introduced  (Merl) 
water  is  then  drawn  into  the  lumen.  Experiments  show  that  the 
trap  works  within  wide  limits  in  nature.  Nevertheless  the  phys- 
iological properties  of  the  walls  remained  a  subject  of  inquiry,  and 
this  has  been  pursued  by  Czaja  and  by  Nold.  Czaja's  conclusion 
was   that   the   trap   is   surrounded   by   a   selectively-permeable   mem- 


Francis  E.  Lloyd  —  242  —  Carnivorous  Plants 

brane,  the  cuticle,  which  excludes  solutes.  The  four-armed  hairs  of 
the  internal  surface  absorb  water  more  rapidly  than  it  can  find  its 
way  in.  Nold  (1934)  had  advanced  the  theory  that  the  potential 
difference  existing  between  the  outer  and  inner  surfaces  of  the  traps 
accounts  for  the  movement  of  water  outwardly.  He  localized  this 
difference  in  the  only  parts  of  the  walls  free  of  cuticle,  namely  the 
outer  spherical  and  the  inner  four-armed  glandular  cells,  the  only 
ones  through  the  walls  of  which  the  water  can  pass.  That  this  shall 
pass  outwardly,  he  believed,  is  assured  by  the  difference  in  pH  at 
these  places.  At  the  inner  surface  this  is  6.2  and  for  the  outer  6.6, 
determined  by  the  Folin  colorimeter;  or  7.5  and  8.2  with  the  quin- 
hydrone  electrode,  differences  which  seem  non-significant  for  water 
movement.  Nold  seems  to  have  shown,  however,  that  the  loss  of 
water  from  the  trap  increases  inversely  with  the  pH.  of  the  outer 
medium,  the  normal  behavior  taking  place  at  ^H  5-7.  The  traps 
are  damaged  at  lower  and  higher  pH  values.  Yet  it  has  been  shown 
that  Utricularia  can  prosper  in  water  of  ^H  4  (Emil  Wehrle, 
1927)  and  U.  minor  in  "weakly  alkaline  water"  (Nold).  In  any 
event,  since  a  difference  of  potential  between  inner  and  outer  sur- 
faces is  known  to  cause  a  water  loss,  but  since  also  organs  are  known 
which  show  such  differences  without  water  movements,  it  is  scarcely 
possible  to  regard  Nold's  hypothesis  as  proven.  This  judgment  is  not 
weakened  by  inspection  of  the  evidence  advanced. 

There  is  a  further  point  in  the  mechanism  of  the  trap  about  which 
opinions  had  been  expressed  previous  to  1929,  without  the  provision 
of  proof.  I  refer  to  the  method  by  which  the  watertightness  of  the 
door  is  procured.  That  watertightness  is  a  necessary  condition  for 
the  successful  action  of  the  trap  was  first  recognized  by  Brocher, 
and  by  his  successors  in  investigation,  all  of  whom  placed  faith  in 
the  contention  that  it  is  due  to  the  tight  appHcation  of  the  door 
selvage  to  the  threshold,  aided  by  the  mucilage  present.  Withycombe 
realized  the  inadequacy  of  this  explanation,  and  supplemented  it  by 
arguing  that  the  door  edge  rests  against  the  outer  edge  of  the  "middle 
layer,"  the  pavement,  seeing  in  this  a  valvular  seat.  An  examination 
of  the  action  of  the  trap  and  certain  details  of  the  emplacement  of 
the  door  led  me  to  suspect  that  the  explanation  was  a  lame  one. 
This  led  to  the  discovery  that  the  entrance  of  the  trap  is  guarded, 
not  merely  by  one  valve,  the  door,  but  by  two,  the  door  and  a  second 
valve,  the  velum,  attached  to  the  threshold  and  finding  its  seat  against 
the  door  selvage,  thus  blocking  the  chink.  This  second  valve  has 
been  seen  in  some  75  species,  in  slightly  various  form  to  be  sure, 
but  always  present  {24,  25).  This  discovery  led  to  a  minute  examina- 
tion of  the  structure  of  the  trap  in  all  material  available  from  various 
parts  of  the  world.  The  results  of  this  survey,  made  on  many  living 
species  and  on  still  more  preserved  ones,  he  in  the  field  of  anatomy, 
which  in  the  presentation  thus  far  has  received  only  minor  mention. 
This  is  now  to  be  taken  up  in  the  following,  in  which  it  will  emerge 
that  Withycombe  was  quite  right  in  principle  if  wrong  in  his  under- 
standing of  the  mechanism.     I  myself  erred  similarly  in  1929. 

The  physiological  anatomy  and  histology  of  the  trap  of  Utricu- 
laria vulgaris  and  closely  related  forms  will  now  be  considered.    Within 


Chapter  XIV  —  243  —  The  Utricularia  Trap 

the  limits  here  imposed  it  will  be  practically  impossible  to  show  in 
detail  the  contributions  of  the  several  investigators  to  our  knowl- 
edge in  this  field,  and  it  must  suffice  to  indicate  critical  observa- 
tions. It  may  as  well  be  said  that  the  study  of  the  anatomy  of  the 
trap  is  by  no  means  easy,  if  we  desire  to  have  exact  knowledge  of 
the  emplacement  of  the  various  parts.  This  is  because  on  cutting 
the  trap,  the  tissue  tensions  are  disturbed  and  the  parts  (especially 
the  door)  disarranged;  and  it  is  necessary  to  know  the  exact  rela- 
tion between  the  valves  (door  and  velum)  and  the  threshold.  This 
cannot  be  finally  determined  by  the  study  of  the  traps  which  have 
been  cut,  though  useful  evidence  can  be  got  this  way,  but  only  by 
the  examination  of  the  entire,  healthy  organ.  An  accurate  descrip- 
tion must  be  based  on  living  turgid  material,  and  errors  have  been 
made  by  placing  faith  on  paraffin  sections.  Again,  the  presence  of 
mucilage  makes  the  trap  slippery,  and  the  knife,  which  must  be  very 
keen,  readily  slips,  so  that  to  make  a  true  sagittal  section  is  diffi- 
cult and  this  has  led  to  mistakes.  The  much  used  figure  first  pub- 
lished by  GoEBEL  in  his  1891  paper  is  wrong  for  this  reason,  and  the 
figure  used  in  a  recent  (German)  edition  of  the  Bonn  textbook  is 
equally  wrong. 

Accounts  dealing  with  our  knowledge  of  the  anatomy  of  the  trap 
(U.  vulgaris  and  closely  allied  forms)  are  those  of  Benjamin  (1848), 
CoHN    (1875),   Darwin   (1875),   Hovelacque    (1888),   Dean    (1890), 

GOEBEL  (1891),  MeIERHOFER  (1902),  LUETZELBURG  (1910),  EkAM- 
BARAM    (1916),    FRANfA    (1922),    MeRL    (1922),    CzAJA    (1922),    WlTHY- 

COMBE  (1924),  Lloyd  (1929),  Kruck  (1931)  and  Nold  (1934)-  Dur- 
ing the  prevalence  of  the  earlier  view  that  the  role  of  the  trap  was 
wholly  passive,  the  results  of  investigation  fell  far  short  of  adequacy 
in  the  presentation  of  details  of  structure  later  found  to  be  im- 
portant. This  period  ended  with  Luetzelburg  in  1910.  With 
Brocher's  discovery  in  191 1  attention  was  concerned  more  and  more 
with  these  details,  though  not  always  with  sufficiently  critical  ob- 
servation, and  sometimes  with  the  entire  lack  of  it.  This  appHes 
particularly  to  the  entrance  structures,  more  so  to  the  door,  of  which 
the  special  features  began  to  be  appreciated  only  with  Withycombe 
and  Merl. 

The  general  features  of  the  trap  have  already  been  described. 
Broadly  speaking  two  regions  are  to  be  considered  alone  and  in  re- 
lation with  each  other,  the  walls  and  the  entrance  mechanism.  The 
appendages  (antennae  etc.)  are  of  less  importance  and  will  be  de- 
scribed in  a  comparative  study  of  the  various  types  of  traps. 

The  walls.  — ■  In  the  species  before  us  the  walls  are  composed  of 
two  courses  of  cells,  the  outer  and  inner,  both  clothed  with  a  thin 
cuticle  on  their  exposed  surfaces.  In  general  the  outer  course  cells 
are  smaller  in  surface  extent  than  the  inner,  in  the  ratio  of  about 
three  to  two,  linear  dimensions.  The  relative  thickness  of  the  two 
courses  varies.  Along  the  profile  of  the  trap,  the  inner  cells  are  the 
deeper,  but  this  relation  is  reversed  on  the  sides  of  the  trap,  where 
the  outer  cells  are  deeper.  This  is  connected  with  the  movement 
of  the  walls  from  convex  to  concave,  the  outer  cells  suffering  increas- 
ing  compression   during   the   excretion    of   water.      Nor   is   the    total 


Francis  E.  Lloyd  —  244  —  Carnivorous  Plants 

thickness  of  the  wall  the  same  everywhere.  Under  the  entrance  the 
threshold,  a  part  of  the  wall,  has  a  thickness  at  the  top  of  four  or 
five  parenchyma  cells  plus  the  epidermis  on  either  side.  The  threshold 
extends  upward  on  both  sides  to  form  the  '' collar  "-Hke  thickening 
which  stands  out  from  the  wall  in  shelf-like  fashion.  Beneath  this 
shelf  the  side  wall  is  attached  to  the  threshold,  and  is  here  quite 
thin,  so  that  the  wall  swings  here  as  on  a  hinge,  thus  not  bringing 
any  torsion  on  the  threshold  and  door.  This  structure  excludes  the 
theory  advanced  by  Brocher,  that  the  walls  help  to  cramp  the  door  in 
position  {26  —  3). 

Chlorophyll  bodies  occur  in  both  courses,  perhaps  somewhat  fewer 
in  the  inner,  but  not  absent,  as  Nold  has  said.  Anthocyanin  often 
occurs  in  the  inner  course  cells,  but  is  absent  from  young  traps  and 
increases  with  age  after  once  appearing.  Interspersed  with  the  larger 
epidermal  cells  are  smaller  ones,  more  numerous  in  the  inner  epidermis, 
the  basal  cells.  These  bear  each  a  short  cutinized  cell,  the  "middle" 
cell,  bearing  two  to  four  glandular,  non-cutinized  cells  to  form  a  cap- 
ital. In  the  outer  course,  the  gland  is  spherical,  of  two  cells.  On  the 
inside  each  middle  cell  bears  two  or  four  elongated  cells.  Darwin 
called  these  hairs  the  bifids  and  quadrifids.  The  former  are  to  be 
found  only  on  the  inner  face  of  the  threshold;  the  quadrifids  else- 
where all  over  the  inner  surface.  In  U.  vulgaris  two  of  the  arms  are 
reflexed,  and  the  whole  is  tilted  towards  the  entrance  to  induce  inward 
movement  of  prey,  it  may  be  argued.  In  U.  gibba  and  allies  all  four 
arms  extend  radially,  but  two  are  shorter  (those  toward  the  entrance), 
and  with  more  spread.  These  quadrifids  are  also  tilted  toward  the 
entrance.  The  bifid  hairs,  forming  a  chevatix  de  frise  on  the  inner  face 
of  the  threshold,  appear  to  be  there  to  discourage  prey  from  working  its 
way  toward  the  door.  In  these  hairs  each  arm  is  a  cell  terminating 
proximally  in  a  slender  stalk.  The  two  or  four  stalks  are  united  to 
form  a  single  short  round  stalk  basing  on  the  middle  cell  {26  —  9-13). 
The  arms  are  not  cuticularized,  and  absorb  dyes  very  readily.  They 
are  generally  regarded  as  the  organs  of  absorption  which  take  up 
digested  food  materials,  and  at  the  same  time  secrete  ferments  and  acid 
to  accomplish  digestion.  The  function  of  the  spherical  glands  of  the 
outer  surface  is  more  in  question.  These  hairs  may  belong  to  the 
category  of  hydropotes  (proposed  by  Mayr  191 5),  the  function  of 
which  is  to  absorb  water  in  submersed  plants,  the  general  epidermis 
being  cuticularized.  In  the  case  of  the  Utricularia  trap  the  function  of 
water  excretion  seems  likely  a  reversal  of  function  which  may  be 
determined  by  the  greater  activity  of  the  quadrifids  in  absorption, 
these  presenting  much  more  surface  to  the  surrounding  medium. 
That  the  function  of  hydropotes  may  be  the  excretion  of  water  has  had 
some  support,  cited  by  Meyer  (1935).  In  one  form  or  another  both 
these  kinds  of  hairs  are  common  to  all  species  of  Utricularia.  In  1931 
Kruck  questioned  Czaja's  contention  that  the  water,  when  being 
excreted  by  the  trap,  escapes  through  the  cuticle  and  therefore  the 
whole  significance  of  his  results  from  examining  the  permeability 
relations  of  this  membrane.  On  her  part  she  held  that  the  internal 
water  is  absorbed  by  the  quadrifids,  and  excreted  by  the  spherical 
glands  of  the  outer  surface.     In  proof  of  this,  which  she  contends  is 


Chapter  XIV  —  245  —  The  Utricularia  Trap 

convincing,  she  claims  to  have  followed  the  path  of  dyes  from  the 
inside  of  the  trap,  which  she  saw  to  enter  through  the  quadrifids  and 
escape  from  the  outer  surface  glands,  and  made  the  observation,  in 
agreement  with  this  view,  that  the  quadrifids  take  up  the  dyes  more 
readily  than  the  outer  glands.  Her  method  of  experimentation  was 
(a)  to  lay  the  traps  in  the  solution,  and  (b)  to  fill  the  traps  with  the 
solution.  As  however  she  does  not  tell  us  in  detail  how  the  latter  was 
managed,  one  hesitates  to  accept  her  observation  without  reserve. 

That  the  quadrifids  are  active  during  digestion  was  observed  by 
Darwin  and  by  Goebel.  Darwin's  experiments  showed  that  sub- 
stances in  solution  (urea,  ammonium  carbonate,  infusions  of  raw  meat) 
are  absorbed  by  the  quadrifids,  but  not  by  these  alone  as  he  found  the 
spherical  hairs  of  the  outside  surface  to  do  the  same,  as  also  the 
mucilage  glands  about  the  entrance.  He  realized  and  admitted  that 
his  experiments  were  not  critical,  but  they  indicated  the  importance  of 
the  problem.  Goebel  detected  the  presence  of  fat  droplets  after 
feeding,  and  Schimper  noted,  in  U.  cornida,  appearances  in  the  ab- 
sorbant  hairs  (here  bifid)  which  had  been  absorbing  food  different  from 
those  in  traps  which  had  not  been  fed.  The  protoplast  showed  activity 
which  he  compared  with  Darwin's  aggregation,  saying  that  the  proto- 
plasm swells  and  the  vacuole  is  broken  up  more  or  less,  as  he  observed 
also  in  Drosera  and  Sarracenia.  Less  constant  in  occurrence  were 
yellow  granules  or  droplets. 

Later  Kruck,  in  the  paper  already  cited,  presented  her  results  of 
study  of  the  cytological  changes  which  are  to  be  seen  in  the  glands  in 
various  conditions  of  rest  and  feeding.  Her  observations  he  in  the 
field  of  cytology  and  are  open  to  various  interpretations.  At  any 
rate  they  need  not  concern  us  here. 

The  trap  wall  is  traversed  by  vascular  bundles  which  branch  from  a 
single  strand  which  enters  by  the  stalk.  On  reaching  the  trap  it 
divides  into  two  branches,  one  of  which  goes  forward  around  the 
longer  edge  to  the  entrance  where  it  ends  abruptly.  The  other  branch 
moves  toward  the  threshold,  on  reaching  which  it  branches,  each  arm 
following  beneath  the  threshold  and  ending  at  one  extremity.  Xylem 
is  present  but  is  very  meagre. 

Far  more  compHcated  in  structure  is  the  trap  about  the  entrance. 
The  opening  arises  in  the  very  young  trap  as  a  sUt  caused  by  the  in- 
vagination of  the  rounded  primordium.  The  lips  of  the  slit  turn 
inwards,  the  upper  becoming  the  door  and  the  lower  the  threshold 
(Meierhofer).  Two  conditions  are  found.  In  one  (as  in  U.  vulgaris) 
the  wall  of  the  trap  bends  abruptly  in  to  continue  as  the  door  {26  —  6). 
In  the  other  {e.g.  U.  gibba,  minor)  the  wall  extends  forward  to  form  an 
overhang,  the  door  springing  away  from  its  inner  under  surface  (26  — 
2).  In  any  case,  from  the  edge  of  the  fold  arise  the  antennae,  stout 
branching  emergencies  springing  from  the  upper  hmb  of  the  opening, 
right  and  left  {2/  —  8).  The  arrangement  of  these  together  with  their 
curvature  produces  a  pair  of  drift  fences  funnelling  toward  the  en- 
trance, thus  serving  to  guide  prey  to  their  doom.  This  condition  is 
found  in  U.  gibba  and  a  good  many  other  species,  in  all  of  which  the 
antennae  are  curved  forward  and  downward  in  front  of  the  entrance 
and   are   strong  prominent   appendages.     The   branches   of   the   main 


Francis  E.  Lloyd  —  246  —  Carnivorous  Plants 

trunk  of  the  appendage  are  long  uniseriate  hairs.  In  other  species 
{U.  vulgaris  americana,  U.  oligosperma)  the  antennae  are  much  smaller 
and  curve  upward,  away  from  the  entrance.  There  are  often  no 
antennae  in  these  species,  and  there  are  others  from  which  they  are 
always  absent  {U.  nana)  {28  —  5).  In  still  other  species,  as  will  be 
seen  later,  quite  other  arrangements  are  met  with.  In  the  water- 
dwelling  species,  while  they  can  evidently  be  regarded  as  elaboration 
of  the  trapping  mechanism,  it  must  be  said  that  their  absence  does  not 
seem  to  make  any  practical  difference  in  the  number  of  prey  cap- 
tured. In  the  mud  dwelling  species,  they  may  serve  to  keep  the 
entrance  free  from  detritus,  and  so  help  in  preserving  the  effectiveness 
of  the  trap.  In  the  wet  sandy  soils  and  in  wet  moss,  where  the  water- 
is  not  continuous,  such  arrangements  may  be  important  in  keeping 
capillary  water,  in  which  prey  may  move,  in  contact  with  the  entrance, 
so  that  when  the  trap  acts  it  does  not  draw  in  air.  The  capillary 
action  in  such  cases  is  helped  by  the  mucilage  secreted  by  glandular 
hairs  in  large  numbers  attached  to  the  door  itself,  and  to  the  sides  of 
the  entrance. 

After  the  two  Hps  are  laid  down  during  the  development  of  the 
trap,  the  sides  of  the  entrance  extend,  moving  the  lips  apart  so  as  to 
produce  a  funnel-shaped  approach.  These  sides,  called  by  Cohn  the 
cheeks,  are  continuous  with  the  overhang,  when  this  is  present,  to 
form  a  sort  of  hood  or  "vestibule"  around  the  opening  {2j  —  9). 

From  each  cheek,  and  from  the  edge  of  the  overhang,  springs  an 
oblique  row  of  long  uniseriate  hairs,  about  four  on  each  cheek,  and  two 
or  three  from  the  overhang  (27  —  7). 

It  is  only  in  the  front  of  the  opening  that  the  hps  are  drawn  apart. 
At  their  free  edges  they  remain  close,  and  in  the  final  stages  of  develop- 
ment are  in  mutual  contact.  At  their  lateral  extremities  they  are 
continuous,  though  their  anatomical  character  changes.  Another 
important  feature  is  alteration  in  the  form  of  the  lower  lip.  Though 
transverse  at  first,  it  becomes  finally  semicircular  in  shape  and  thick- 
ened by  the  growth  of  additional  layers  of  wall  cells  beneath  it  to  form 
a  massive  thickening  and  strengthening  of  the  wall  in  this  zone.  This 
structure  so  produced  was  called  the  collar  by  Darwin,  and  the  abut- 
ment by  GoEBEL.  In  this  account  it  is  called  the  threshold.  By  its 
form  and  strength  it  preserves  the  shape  of  the  opening,  and  resists  any 
cramping  effect  (said  to  occur  by  Brocher  and  Czaja)  of  the  dis- 
tortion of  the  walls  when  the  maximum  of  internal  water  has  been 
withdrawn.  Measurements  made  by  myself  did  not  reveal  any  differ- 
ence in  form  in  the  set  and  the  extremely  relaxed  condition  of  the  trap 
after  puncture.  In  fact,  the  walls  where  they  articulate  with  the 
threshold  are  thinner  than  elsewhere,  so  that  they  can  bend  without 
exerting  distortion  on  it  {26  —  3),  besides  which  is  the  fact  that  the 
inner  part  of  the  threshold  is  supported  free  of  the  wall,  so  that  this 
cannot  press  upon  it. 

The  structure  of  the  threshold  in  detail  is  best  understood  first  by 
an  examination  of  a  transverse  section  through  its  middle  point  (25  — 
I,  2,  5;  2g  —  4)  and  then  by  viewing  it  from  a  point  of  view  which 
embraces  the  whole  inner  surface,  flattened  out  for  convenience  of 
study  {25  —  9) .     In  the  transverse  section  the  threshold  is  roughly 


Chapter  XIV  —  247  —  The  Utricularia  Trap 

triangular,  the  base  forming  the  free  surface,  the  apex  continuous  with 
the  wall.  The  free  surface  is  sHghtly  convex,  with  broken  curves 
indicating  three  regions,  an  outer,  continuous  with  the  cheeks,  carrying 
scattered  stalked  glandular  hairs;  a  middle,  clothed  with  a  layer  of 
densely  crowded  glands,  called  the  pavement  epithelium  by  Goebel, 
and  an  inner  of  epidermal  cells,  forming  a  shelf  projecting  into  the 
interior  of  the  trap. 

The  outer  region  is  part  of  the  vestibule,  and  we  may  think  of  it  as 
a  doorstep.  The  inner  region  is  merely  a  part  of  the  inner  wall  sur- 
face, but  re-entrant.  The  middle  region  is  of  critical  importance.  We 
shall  use  Goebel's  name  for  it,  recognizing  however  that  the  surface  is 
not  epithelial  but  consists  of  closely  set  glandular  cells  which  arise  from 
the  epithelium  below.  It  is  a  pavement  of  packed  tiles,  each  tile  being 
the  capital  of  a  glandular  hair.  We  pause  here  to  recall  the  structure 
of  the  glandular  hairs  in  Utricularia.  Arising  from  a  basal  epidermal 
cell,  each  consists  of  a  middle  cell  (Goebel),  strongly  cuticularized, 
short  and  discoid  in  shape,  supporting  a  glandular  capital  of  one,  but 
more  usually  two  cells,  sometimes  four  (quadrifids),  uncuticularized 
(BiJSGEN  1888).  The  middle  cells  may  be  supported  on  a  shorter  or 
longer  tubular  extension  of  the  epidermis  cell  wall,  as  is  the  case  of  the 
hairs  surrounding  the  entrance.  Those  of  the  pavement  are  similar 
to  the  glandular  hairs  of  the  general  outer  plant  surface,  but  differ  in 
having  capitals  elongated,  at  right  angles  to  the  axis  of  the  entrance, 
so  that,  on  looking  down  on  the  threshold,  the  pavement  appears  to  be 
made  of  closely  packed  sausages.  The  capitals  may  be  one  or  two 
celled.  Each  gland  arises  from  a  laterally  compressed  epidermal  cell, 
so  narrow  that  the  middle  cell  lies  tightly  against  the  neighboring 
ones.  The  terminal  cells  are  similarly  tightly  packed,  forming  the 
visible  pavement  (Gislen  191 7)  (C/.  various  figures  on  25  to  zg). 

Like  the  glandular  hairs  in  general,  the  pavement  glands  loosen 
and  shed  their  cuticles,  but  most  curiously  in  a  single  piece,  except  in 
the  inner  zone  {2g  —  4).  To  describe  this  behavior  we  have  to  recog- 
nize three  zones  of  the  pavement  epithelium,  outer,  middle  and  inner. 
In  the  outer  zone,  the  cuticles  of  its  glands  enlarge  into  balloons,  but 
remain  attached  mutually  and  to  the  glands  which  bear  them.  In  the 
middle  zone,  broadest  at  the  ends,  the  cuticles  remain  mutually  at- 
tached, but  are  freed  from  the  capitals  which  produced  them,  and 
from  the  inner  zone  glands,  but  remain  attached  to  the  ballooned 
cuticles  of  the  outer  zone.  The  glands  of  the  inner  zone  behave 
individually,  their  cuticles  enlarging  and  bursting.  There  is  formed 
in  this  way  a  membrane,  which  I  call  the  velum,  consisting  of  two 
parts,  a  cushion  of  cuticular  balloons  running  from  one  end  of  the 
pavement  to  the  other  on  the  outer  zone,  and  attached  to  it  a  thin 
membrane,  bearing  the  markings  of  the  capitals  which  produced  it,  the 
two  together  forming  a  valve  which,  stretching  from  one  side  of  the 
pavement  to  the  other,  overlies  the  door  edge  (25  —  4-8).  The  inner 
zone  is  lenticular,  broadest  at  the  middle,  and  scarcely  reaching  the 
outer  ends  of  the  pavement.  Its  glands  are  larger  and  not  very 
tightly  packed.  The  middle  zone,  entirely  free  of  cuticles,  presents  a 
soft  yielding  surface  into  which  the  door  edge  can  sink  somewhat 
under  pressure. 


Francis  E.  Lloyd  —  248  —  Carnivorous  Plants 

We  consider  now  the  door  or  valve.  This  is  a  flap,  two  cell  courses 
in  thickness,  forming  the  upper  free  edge  of  the  entrance  opening,  and, 
in  nature,  bulges  outwardly  (2j  —  2,  5).  If  it  is  removed  by  cutting 
along  its  line  of  attachment  to  the  trap  wall  and  is  allowed  to  lie  in 
water,  it  retains  the  shape  it  has  in  situ  as  Bijsgen  observed  (1888). 
It  is,  if  we  disregard  minor  curvatures,  roughly  semicircular,  the 
shorter  side  being  the  free  edge.  For  the  sake  of  description  we  may 
flatten  the  door  and  then  map  out  certain  regions,  shown  in  the  dia- 
gram {2Q  —  13).  A  wide  zone  around  the  edge  of  attachment  is  the 
hinge  region,  where  strong  reverse  flexures  occur  when  the  door  is 
opened.  The  middle  region  of  this  zone  is  the  upper  hinge,  the  two 
lateral  the  lateral  hinges.  The  upper  hinge  is  characterised  by  marked 
flexures  when  the  door  is  at  rest.  The  hinge  area  surrounds  a  lentic- 
ular middle  area,  which  may  be  called  simply  the  middle  area.  At 
the  lower  part  of  this  a  small  circular  patch  of  the  door  is  quite  thin, 
and  this  is  the  central  hinge.  Out  from  just  below  this  project  four  to 
six  stout,  curved,  tapering  bristles.  That  part  of  the  door  below  the 
central  hinge  is  thick  and  strong.  This  is  the  middle  piece.  Towards 
the  flanks,  the  door  selvage  becomes  thinner.  With  this  terminology 
{26  —  i)  we  can  more  easily  describe  the  histology. 

As  above  said,  the  door  consists  of  two  cell  layers  {2j  —  2,  5;  2g  — 
I,  2),  an  outer,  and  an  inner.  The  two  are  very  different  in  structure, 
the  general  relation  between  them  being  that  existing  in  a  bimetallic 
strip,  one  of  the  metals  having  a  greater  index  of  expansion  than  the 
other;  the  former  under  changes  of  temperature  is  active,  the  latter 
relatively  passive.  The  cells  of  both  layers  are  equally  turgid,  but  the 
inner  is  capable  of  ready  expansion  and  contraction  of  its  inner  surface, 
the  outer  not.  This  is  ascribable  to  the  differences  of  structure.  The 
door  has  been  described  as  highly  flexible  and  elastic,  as  for  example 
by  Darwin.  Highly  flexible  it  is,  but  if  by  elasticity  we  mean  ex- 
tensibihty,  this  adjective  does  not  apply.  The  tissue  has  a  sort  of 
cartilaginous  quality,  bending  without  breaking  in  any  direction.  If 
the  door  is  freed  in  part  by  cutting  a  median  strip,  releasing  this  from 
the  pull  of  the  sides,  it  will  spring  outwardly  and  only  on  plasmolysis 
can  it  be  brought  back.  This  shows  that  the  door  as  a  whole  is  always 
normally  insistent  in  pushing  outward,  and  is  held  in  its  proper  position 
only  by  virtue  of  its  semicircular  attachment  to  the  trap  wall.  As 
Benjamin  showed,  it  can  be  pushed  in-  but  not  outwardly.  When 
fully  inwardly  inflexed,  it  is  folded  along  its  middle  line,  becomes  some- 
what concave,  and  the  tripping  bristles  then  lie  in  the  groove  of  the 
fold  {26  —  7),  as  Ekambaram  described  it. 

The  inner  reaches  of  this  attachment,  that  is,  the  lateral  hinges, 
coincide  with  the  inner  ends  of  the  threshold,  the  extreme  end  of  the 
free  door  edge  coinciding  with  the  inner  angle  of  the  threshold.  The 
outer  surface  of  the  lateral  hinge  therefore  lies  against  the  outer  reach 
of  the  threshold.  But  the  free  edge  of  the  door,  starting  from  the 
inner  angle  of  the  threshold,  passes  obliquely  across  it,  the  angle  be- 
tween the  face  of  the  door  gradually  changing  till,  in  the  middle  reach, 
it  stands  obhquely  on  edge  {26  —  2).  Only  the  middle  reach  of  the 
door  selvage  is  thickened  and  stiff;    the  outer  reaches  are  thin. 

The  rest  of  the  attachment  extends  along  the  wall  of  the  trap,  curving 


Chapter  XIV  —249— The  Utricularia  Trap 

around  from  one  end  of  the  threshold  to  the  other  in  a  semicircular 
sweep.  Here  the  door  curves  inwardly  at  first,  to  form  the  upper  hinge, 
below  this  outwardly  to  form  the  bulging  middle  area.  The  curves  of 
the  upper  hinge  are  most  pronounced  in  front,  and  are  reduced  at  the 
sides.  The  outward  spring  of  the  door  depends  on  the  physical  prop- 
erties of  the  upper  hinge  chiefly.  The  lateral  hinges  resist  this  pull, 
but  can  bend  passively. 

If  now  we  examine  the  histology  of  the  door  we  find  (29—1,  2), 
on   inspecting  a  section   in   any  direction,  that  in   general   the  outer 
course  of  cells  is  thin,  the  inner  thick,  in  the  ratio  of  about  one  to 
three,  differing  from  place  to  place.     In  the  central  hinge  they  are  of 
nearly  equal  thickness,  as  also  in  the  middle  piece.     The  cells  of  the 
outer  course  are  all  flat,  their  anticlinal  walls   zigzag    (Bijsgen)    and 
these  walls  are  strongly  supported  by  buttresses  at  their  angles.    These 
prevent  their  collapse  under  bending.     This  layer  must  put  up  with  as 
much  bending  as  the  outer,  but  passively.     Many  of  these  cells  bear 
glandular   hairs    {24—1;    26  —  2),    some    with   pyriform,    some   with 
spherical  capitals.    Those  with  pyriform  capitals  are  scattered  over  the 
upper  part  of  the   door  surface,  and  are  shorter  stalked  as  one  ap- 
proaches the  middle  point  of  the  door.     Near  the  door  edge,  arranged 
in  a  crescent  parallel  with  it,  is  a  row  of  glands  with  short  stalks  and 
globose  capitals,  a  quite  large  one  at  the  middle  point.     Just  above  the 
level  at  which  this  stands  there  are  hairs  of  different  structure.    These 
are  stiff,  tapering,  sharply  pointed  bristles,  four  in  number,  standing  at 
the  angles  of  a  trapezoid,  in  an  oblique  posture,  extending  upward, 
then  curving  delicately   (25  —  3,  5).     Each  is  composed  of  three  to 
five  cells,  the  basal   the   shortest,   the   terminal  the   longest.    Ekam- 
BARAM  described  short  hinge  cells,  like  those  in  the  sensitive  hairs  of 
Aldrovanda,  but  this  is  a  mistake.    They  anchor  in  the  outer  cell  layer, 
by  a  broad  base,  as  correctly  shown  by  Meierhofer,  without  any 
bulbous    insertion    as    Merl    showed    {26  —  4).      These    four    (or    in 
U.  flexuosa   six,    Ekambaram)    hairs    constitute    the    tripping   mecha- 
nism of  the  trap.     A  touch  of  these  in  any  direction  but,  according 
to  CzAjA,  best  from  above  down,  causes  some  distortion  of  the  middle 
piece  of  the  door  selvage.     This  distorts  the  door  edge  from  its  equal 
seat,    upsetting   the    dehcate   equilibrium,    and   permitting   the    water 
pressing  against  the  door  to  push  it   in,    assuming   the    trap   to   be 
properly  set.     As  we  shall  see,  the  tripping  mechanism  shows  a  wide 
variety  of  form  in  the  genus.    That  just  described  is  found  only  in  the 
vulgaris  type  and  in  Biovularia,  though  in  the  latter  the  door  has  a 
different  plan  of  structure. 

When  facing  the  door,  the  outer  course  of  cells  presents  a  plan  as 
follows.  In  the  region  of  the  upper  hinge,  the  cells  are  isodiametric, 
very  wavy  walled,  with  strong  buttresses  (Cohn  1875).  Their  walls 
lie  athwart  those  of  the  inner  course  cells.  The  same  is  true  of  the 
middle  area.  In  the  central  hinge  they  are  very  small,  corresponding 
in  size  to  the  cells  of  the  inner  course.  The  same  is  true  of  the  middle 
piece,  where  the  cells  are  very  small  and  their  walls  are  strongly 
fortified  with  broad  and  thick  buttresses.  These  cells,  however,  while 
small  when  seen  en  face,  are  deep,  and  equally  deep  with  those  of  the 
inner  course.     Along  the   selvage   to   the   outer  hmits  of  the   lateral 


Francis  E.  Lloyd  —  250  —  Carnivorous  Plants 

hinge,  the  cells  are  elongate,  and  have  numerous  very  small  but- 
tresses, difficultly  seen.  That  is  to  say,  the  cells  in  the  regions  of 
maximum  bending  have  zigzag  walls  with  many  buttresses.  Where 
the  door  is  stiffest,  i.e.,  in  the  middle  piece,  the  buttresses  are  at  a 
maximum  in  numbers  and  size.  In  these  cells  also  the  walls  are  thick, 
especially  the  outer. 

Looking  at  the  inner  face  of  the  door,  we  note  a  different  pattern. 
With  the  central  hinge  as  a  center,  the  inner  course  consists  of  elon- 
gated cells  radiating  from  this  center  to  this  circumference  {24  —  9). 
The  closer  to  the  center  the  shorter  the  ceUs  become,  so  that  at  the 
center  they  are  isodiametric  and  thickly  studded  with  buttresses. 
Below  the  center,  the  cells  of  the  inner  course  of  the  middle  piece 
are  also  isodiametric  and  match  the  outer  course  of  cells  in  the  degree 
of  buttressing.  From  here,  tending  toward  each  side  of  the  door,  the 
cells  become  longer  and  run  along  the  selvage  parallel  to  it.  This 
seems  at  first  glance  simple  enough,  and  it  seems  surprising  that  the 
cells  of  the  whole  inner  course  should  have  been  more  than  once 
described  as  isodiametric.  The  mistake  is  easily  explained,  for  when 
the  inner  surface  of  the  door  is  examined  without  flattening  it  out, 
to  do  which  it  must  be  fully  plasmolysed,  a  series  of  concentric  lines 
can  be  seen  {24  —  9;  2g  —  3).  Darwin  saw  them.  They  were  cor- 
rectly understood  first  by  Meeerhofer.  They  are  nothing  more  than 
an  optical  effect  arising  from  the  fact  that  the  inner  cells  are  constricted 
at  regular  intervals  (29  —  1-3)-  Wherever  the  constrictions  meet  the 
side  walls  of  the  ceUs,  these  are  here  buttressed  by  props.  In  sections 
the  spaces  between  the  constrictions  are  usually  taken  for  single  cells, 
a  mistake  which  I  made  myself  at  first.  Within  the  central  area 
these  lines,  indicating  the  constrictions,  run  with  great  regularity  from 
cell  to  cell.  In  the  region  of  the  outer  and  lateral  hinges  they  are 
equally  present,  but  are  less  regular.  In  the  central  hinge  and  in  the 
middle  piece  they  are  also  present,  but  are  here  quite  irregular  and 
numerous  and  are  only  with  difficulty  observable. 

The  effect  of  these  constrictions  is  to  render  the  outer  wall  of  the 
inner  course  of  cells  readily  compressible,  like  a  bellows,  without  injury 
to  the  cells.  Without  them  it  is  hard  to  see  how  so  great  flexibility  of 
the  door  tissues  combined  with  firmness  and  quick  reaction  could  be 
attained.  It  is  indeed,  as  Meierhofer  exclaimed,  a  "most  wonder- 
ful" arrangement.  In  the  upper  hinge  the  constrictions  are  not  so 
deep  as  in  the  middle  area  but  are  more  numerous,  which  may  be  a 
better  arrangement  for  the  maximum  bending  which  this  has  to  en- 
dure. 

It  may  be  pointed  out  that  these  cells  have  been  represented  (by 
Ekambaram  and  Meierhofer)  as  having  their  anticlinal  walls  con- 
stricted like  the  periclinal.  This  is  not  the  case.  It  is  true  that  if  a 
door  is  torn  from  its  moorings  and  laid  in  water  for  examination  the 
injured  cells  along  the  torn  edge  will  collapse  and  their  uninjured 
neighbors  will  swell  and  present  the  picture  recorded  by  these  authors 
{24  —  9).  But  this  cannot  occur  when  the  door  is  in  situ  and  un- 
injured. 

We  now  consider  (a)  the  way  in  which  the  door  edge  lies  in  con- 
tact with  the  threshold,  so  that  it  can  maintain  its  posture  in  spite  of 


Chapter  XIV  —  251  —  The  Utricularia  Trap 

the  water  pressure  it  must  sustain  when  the  trap  is  set,  and  (b)  how  the 
water  is  prevented  from  leaking  under  the  door  edge.  Recalhng  the 
structure  of  the  threshold  and  especially  that  of  the  pavement,  it  is 
necessary  to  point  out  that  the  latter  along  its  middle  reach  is  curved 
in  such  a  manner  that  it  slopes  somewhat,  so  as  to  face  the  interior  of 
the  trap.  At  the  bottom  of  the  slope,  where  the  inner  zone  begins, 
there  is  an  abrupt  change  in  the  direction  of  the  slope  so  that  a  slight 
depression  is  produced  (29  —  4).  Here  the  pavement  is  most  closely 
packed.  The  middle  reach  of  the  door  edge  is,  as  we  have  seen, 
strengthened  so  as  to  make  a  firm  edge,  which  rests  against  the  pave- 
ment just  in  or  beyond  the  depression,  its  outer  selvage  surface  resting 
more  or  less  against  the  pavement,  according  to  the  amount  of  strain 
produced  by  water  pressure.  When  the  water  pressure  is  greatest, 
that  is,  when  the  trap  is  fully  set,  the  position  of  the  door  edge  is 
more  nearly  normal  to  the  pavement  than  when  the  trap  has  just  been 
released.  This  can  be  inferred  from  the  measurements  of  photographs 
of  traps  before  and  just  after  "firing"  (Lloyd  1932&)  {29  —  11).  It  is 
indicated  also  by  the  position  of  the  bristles,  which  are  more  erect 
when  the  trap  is  in  the  set  condition.  It  may  be  added  here  that  the 
whole  shape  of  the  trap  is  altered  a  little  by  the  change  in  postures  of 
the  side  walls.  Since  the  ends  of  the  door  edge  coincide  with  the  inner 
angles  of  the  threshold,  it  follows  that  its  lateral  reaches  cannot  follow 
the  pavement  parallel  to  its  midline.  It  is  only  its  middle  reach  (the 
middle  piece)  which  impinges  edgewise  on  the  pavement.  The  lateral 
reaches  merely  lie  with  the  outer  surface  of  the  selvage  flat  against  the 
pavement,  thus  forming  a  re-entrant  sHt  through  which  the  water  must 
leak  under  pressure  unless  this  contingency  were  provided  against, 
which  is  the  case.  The  cuticular  membrane,  the  velum,  attached  to 
the  outer  zone  of  the  pavement,  is  slung  completely  across  from  end 
to  end  of  the  threshold  (25  —  5-8).  When  the  door  swings  outwardly 
after  springing  the  trap,  it  pushes  against  the  velum  which  folds 
against  the  door  {2j  —  4),  covering  the  re-entrant  shts  on  the  sides  and 
blocking  the  door  edge  in  the  middle.  When  the  door  is  in  position, 
the  velum  reaches  in  front  up  to  the  short  spherical  hairs  which  stand 
in  a  curved  row  just  below  the  level  of  the  tripping  hairs  (24  —  i ; 
2j  —  3-5)-  Experimental  proof  that  the  velum  thus  blocks  the 
entrance  by  its  valvular  action,  consisted  in  cutting  the  side  reach. 
This  was  accomplished  with  a  very  small  knife  several  times  and  the 
parts  carefully  examined  afterwards  for  assurance  that  no  other  damage 
had  been  done  (Lloyd  1932&).  In  no  case  after  the  velum  was  cut 
did  the  trap  reset  itself.  In  Czaja's  experiment  in  which  he  thrust  a 
hair  beneath  the  door  edge,  this  not  only  held  up  the  door  edge  but 
depressed  the  velum  also,  but  this  escaped  his  attention. 

As  CzAjA  found,  the  distortion  of  the  door  edge  (and  that  of  the 
velum  at  the  same  time)  when  it  rests  on  a  hair,  prevents  the  traps 
from  working.  This  does  not  seem  to  be  the  case  if  the  entrance  is 
filled  with  the  soft  body  of  a  large  capture,  sufficient  to  plug  it  {20  — 
11).  Matheson  (1930)  states  that  such  prey  may  eventually  be 
ingested,  indicating  that  the  trap,  plugged  by  the  animal's  body,  still 
evacuates  its  water.  In  the  meantime  the  prey  may  be  softened  and 
respond  to  the  sucking  action  when  re-established,  and  thus  eventually 


Francis  E.  Lloyd  —  252  —  Carnivorous  Plants 

be  drawn  in.  Mr.  J.  H.  Buzacott  writes  me  that  this  has  been  ob- 
served at  Meringa,  Queensland,  {20 —  11)  where  tadpoles  of  Bnfo  nia- 
ritius,  imported  to  control  insect  pests  in  sugar  cane,  have  been 
destroyed  in  numbers. 

On  the  sucking-in  of  prey:  —  The  fact  that  large  prey  (young 
tadpoles  and  fish  fry,  worms  etc.)  can  be  caught  by  some  part  of  the 
body,  usually  the  tail,  has  long  been  known.  After  a  tadpolette  has 
been  trapped  but  not  completely  engulfed,  it  has  been  stated  that  the 
body  is  later  sucked  in.  This  would  obviously  be  limited  by  the 
volume  of  the  trap.  The  question  has  been  raised  by  me,  does  this 
sucking-in  actually  occur  and  if  so  what  is  the  mechanical  procedure? 
I  have  recently  taken  pains  to  get  evidence  on  this  point.  I  employed 
Utriciilaria  aff.  gibba,  sent  me  from  Pasadena,  Calif.,  by  Dr.  F.  Went. 

In  a  series  of  experiments  young  mosquito  larvae  about  2  mm.  long 
were  used.  By  manipulation  it  was  possible  to  get  one  caught  by  the 
tail,  the  head  being  too  big  to  enter  the  trap.  When  this  occurred, 
one  half  of  the  body  was  instantaneously  engulfed,  leaving  four  or  five 
joints  behind  the  thorax  projecting  beyond  the  mouth  of  the  trap. 
The  joints  served  as  clear-cut  measures.  Several  cases  were  observed, 
and  all  followed  the  same  pattern.  One  example  will  suffice.  The 
larva  was  caught  by  the  tail,  the  door  clamping  down  between  the 
sixth  and  seventh  joints,  while  six  remained  protruding  (11:30  hrs.). 
At  18  hrs.  only  the  thorax  and  head  remained  protruding.  Next 
morning,  the  thorax  had  also  been  engulfed,  the  head  only,  too  big  to 
enter,  being  left  outside.  (Text  fig.  8,  A,  B).  Since  the  body  of  the 
larva  prevents  the  door  from  assuming  its  normal  set  posture,  and 
though  the  trap  walls  did  not  become  concave,  as  observed  from  time  to 
time,  it  must  be  inferred  that  nevertheless  the  entrance  was  sufficiently 
occluded  by  the  door  and  larva  so  that  the  exhaustion  of  the  water 
from  the  inside  of  the  trap  could  proceed,  creating  a  suction  on  the 
prey  from  time  to  time,  and  drawing  it  gradually  in.  As  I  did  not  see 
this  happening  during  a  prolonged  period  of  observation,  I  cast  about  for 
more  suitable  experimental  material.  This  I  found  in  fine  shreds  of 
albumin,  made  by  stirring  egg-white  in  boiHng  water.  These  were  soft 
and  of  fairly  even  caliber.  Of  a  goodly  number  of  experiments  I  choose 
the  following.  Case  i  (Text  fig.  8  C,  D).  A  shred  about  two  milli- 
meters long  was  presented  to  the  trap  by  touching  the  tripping  bristles 
with  its  end.  One  half  of  the  shred  was  swallowed;  the  rest  remained 
protruding.  On  this  some  bits  of  rust,  detached  from  the  needle  point, 
adhered,  serving  as  marks.  When  examined  18  minutes  later,  the  entire 
shred  had  been  taken  in.  In  the  meantime  the  experiment  was  re- 
peated (Case  2)  (Text  fig.  8  E-H)  and  kept  under  close  and  continuous 
observation.  Immediately  after  the  door  had  clamped  down  on  the 
partially  engulfed  shred,  the  latter  was  seen  to  sHde  slowly  in  for  two 
minutes,  when  it  stopped  (F).  This  movement  was  the  result  of 
residual  wall  action.  Nothing  further  happened  for  about  ten  minutes 
(during  which  time  a  partial  reduction  of  pressure  within  the  trap  took 
place)  when  the  door  opened  and  closed  rather  slowly  (the  movement 
was  quite  visible  to  the  eye)  and  another  portion  of  the  shred  entered 
(11  43  hrs.).  By  16:00  hrs.  the  shred  had  been  entiredly  swallowed  (H). 
The  walls  were  now  concave,  and  the  trap,  completely  reset,  reacted 


Chapter  XIV 


—  253  — 


The  Utricularia  Trap 


to  touch  on  the  tripping  bristles.  In  still  another  case,  a  very  slender 
bit  of  a  swallowed  shred  remained  protruding,  and  the  walls  of  the 
trap  had  become  concave.  The  delicacy  of  this  protruding  shred  had 
permitted  the  door  to  take  the  set  posture,  allowing  full  exhaustion  of 
the  internal  water.  On  stimulating  the  tripping  hairs,  this  shred  was 
swallowed. 

It  is  evident  from  these  experiments  that:  i.  When  the  prey  is 
soft  and  yielding,  but,  caught  part  way  in,  is  large  enough  to  prevent 
the  door  from  taking  the  set  posture,  this  still  may  clamp  down 
enough  to  enable  the  trap  walls  to  bring  about  a  sufficiently  low 
pressure  to  exert  suction  and  thus  draw  in  the  body  of  the  prey  and,  by 
repetition,  finally  engulf  it,  if  small  enough. 


E  F  G  H 

YiG.  8.  —  The  sucking  in  of  prey  by  the  trap  of  Utriciduria  gibba  or  a  related  species; 
A,  an  injured  mosquito  larva  was  presented  and  suddenly  but  only  partly  swallowed, 
May  21,  1941;  B,  the  same  three  days  later;  C,  a  shred  of  albumen  presented  and  partly 
swallowed  at  11:20;  D,  at  11:38,  the  shred  entirely  swallowed  (the  insert  figure  indicates 
the  edge  of  the  door  looped  over  the  soft  and  yielding  prey,  the  surface  of  the  threshold 
indicated  by  the  broken  line);  E,  a  shred  of  albumen  presented  at  11:35,  and  the  trap 
observed  continually;  F,  at  11:37,  part  of  the  shred  indicated  by  a  double  arrow  had  been 
slowly  sucked  in;  G,  at  11:43,  the  door  quickly  (but  not  very  suddenly)  opened  and 
another  portion  of  the  shred  (/)  swallowed;   later  (H)  the  remainder  was  engulfed. 

2.  If  the  prey  is  slender  and  yielding  enough,  the  door  may  assume 
a  sufficiently  exact  set  posture  to  insure  the  full  setting  of  the  trap, 
when  it  will  react  normally  but,  of  course,  only  in  response  to  move- 
ment of  the  tripping  bristles.  When  the  prey,  still  not  engulfed, 
dies,  it  may  not  be  swallowed  unless  the  tripping  bristles  are  touched 
by  some  other  agent.  If  a  stiff,  unyielding  object  such  as  a  hair  is 
used  (as  did  Czaja),  this  cannot  happen  because  of  inleakage  of  water 
at  the  side  of  the  hair. 

Traps  which  have  captured  mosquito  larvae  (the  head  remaining 
protruding)  do  not  survive,  dying  in  10  days  or  so,  evidently  from 
overfeeding. 

We  now  resume  our  discussion  of  the  structure  of  the  trap.  In 
addition  to  the  front  view  of  the  velum,  which  can  be  seen  in  the  living 
trap,  a  side  view  can  be  had  under  favorable  conditions,  when  it  is 
seen  that  the  velum  forms  a  bolster  in  front  of  the  door  edge  (25  —  3,4). 


Francis  E.  Lloyd  —  254  —  Carnivorous  Plants 

It  is  of  interest  and  mere  justice  to  record  that  the  velum  had  been 
seen  previously  by  two  observers,  both  in  1891.  Giesenhagen,  I  be- 
lieve it  was,  made  a  drawing  for  Goebel's  paper  of  1891  of  a  trans- 
verse section  of  the  threshold  of  U.  flexuosa.  In  this  drawing  the  velum 
was  shown  in  the  clearest  manner,  but  no  mention  of  it  was  made  in 
the  text.  And  in  1891,  at  Cambridge  (England)  R.  E.  Fry,  a  student 
who  was  later  to  become  an  eminent  art  critic  and  Professor  of  Art 
in  that  university,  and  who  is  better  and  more  widely  known  as 
"Roger  Fry,"  prepared  a  Ms.  which  was  never  pubhshed,  but  to 
which  I  fortunately  had  my  attention  drawn  when  attending  the 
International  Botanical  Congress  in  1930.  It  was  lying  on  the  shelves 
of  a  bookshop.  Roger  Fry  was  evidently  a  close  observer,  for  in  one 
of  his  drawings,  meticulously  executed  in  fine  pencil  and  color,  he 
showed  the  velum,  and  in  his  description  he  described  the  pavement 
epithelium  (he  used  Goebel's  1891  term),  saying  that  "the  whole  of 
this  secretes  mucilage,  the  cuticles  of  the  hairs  being  raised  in  a  mass;" 
but  he  did  not  examine  further  into  the  matter.  One  cannot  help 
wondering  why  others,  who  saw  other  minute  details,  failed  to  see  the 
velum.  Roger  Fry's  Ms.  has  now  been  deposited  by  me  in  the 
Library  of  the  School  of  Botany,  Cambridge  University. 

Two  mechanical  types  of  trap.  —  Having  described  in  some  detail 
the  structure  of  the  trap  of  Utricularia  vulgaris,  it  must  now  be  pointed 
out  that,  though  working  according  to  the  same  mechanical  principles 
and  being  of  the  same  morphological  type,  there  are  two  distinct  kinds 
of  traps  (Lloyd  1936c).  They  can  be  distinguished  readily  by  the 
posture  of  the  door  in  its  relation  to  the  threshold  (Text  fig.  9).  If  we 
consider  the  entrance  as  tubular,  in  one  kind  the  tube  is  short,  in  the 
other  long.  U.  vulgaris  has  a  trap  with  a  short  tube  entrance.  In  it 
the  door  stands  approximately  at  right  angles  to  the  axis  of  the  tube, 
or  at  any  rate  forming  a  wide  angle  with  it.  In  the  other  kind,  of 
which  U.  capensis  is  a  good  example,  the  entrance  is  tubular  (Ste- 
phens 1923),  and  the  door  stands  obhquely,  forming  a  narrow  angle 
with  the  axis.  Considered  as  a  valve,  this  is  the  less  efficient,  ceteris 
paribus,  but  its  inferiority  is  compensated  for  in  various  ways,  to  be 
noted.  Of  the  latter  kind  there  are  two  variants  represented  by  such 
species  as  U.  monanthos,  and  U.  dichotoma,  on  the  one  hand  and  Poly- 
pompholyx  on  the  other,  all  purely  Australasian  types,  with  differences 
demanding  separate  description. 

The  description  of  U.  vulgaris  above  given  will  serve  as  a  standard 
of  comparison.  Correlated  with  its  position  in  the  short  tubular 
entrance,  the  shape  of  the  door  is  such  that  its  sagittal  measurement 
is  less  than  its  transverse.  The  top  of  the  threshold  is  narrow.  In 
U.  capensis,  with  a  long  tubular  entrance,  the  door  has  reversed 
measurements:  it  is  longer  than  broad,  and  the  threshold  is  broad 
(29  —  12,  13).  The  door  stands  obhquely.  A  glance  at  the  diagram 
(Text  fig.  9)  will  reveal  these  differences.  It  is  seen  that,  considered 
as  a  check  valve,  the  long  door,  presenting  a  re-entrant  angle  with  the 
threshold,  and  with  no  opposing  seat,  is,  with  respect  to  the  direction 
of  the  water  pressure,  at  a  disadvantage.  In  our  blood  vessels  the 
valves,  which  are  also  obliquely  set  flaps,  are  in  the  reverse  position. 
But  from  the  point  of  view  of  the  efficacy  of  the  trap,  the  door  would 


Chapter  XIV 


265 


The  Utricularia  Trap 


be  useless  if  it  were  set  in  this  way.  In  the  trap  it  must  be  able  to 
resist  the  water  pressure  to  which  it  is  normally  subjected,  until  a 
trigger  action  is  applied,  when  it  must  then  be  weak  enough  to  fold 
up,  allowing  the  entrance  of  a  water  column.  And  it  must  of  course 
not  allow  the  leaking  in  of  water  when  the  trap  is  set.  How  these  de- 
mands are  met  may  be  understood  by  examining  the  structures  in- 
volved.   For  models  of  the  U.  vulgaris  trap,  see  p.  266. 

The  door  is  divided  into  a  relatively  thin  anterior  half,  and  a 
thick  posterior  half  {31  —  3  etc.).  The  former  includes  the  areas 
of  the  upper  hinge  and  the  middle  area.  The  two  cell  courses  of 
the  upper  hinge  have  the  structure  seen  before,  with  deeply  constricted 
walls  in  the  inner  course  {31  —  9).  Those  of  the  middle  area,  not  a 
region  of  sharp  bending,  have  about  equal  thickness,  with  no  con- 
strictions.    There  is  no  central  hinge  and  below  the  mid-point  of  the 


Fig.  9.  —  Diagrams  of  the  entrances  of  Utricularia  vulgaris  (i,  2)  and  U.  capensis  (3  riglit) 
or  caerulea  (3  left )  embodying  the  different  mechanical  conditions  in  these  two  types  of 
trap;  pd,  general  direction  of  thrust  of  the  door,  and,  pt,  of  the  threshold;  r,  relaxed  position 
of  the  door;  a,  point  of  impact  of  prey;  PH20,  pressure  of  water  against  the  door;  iz,  slope 
of  inner  zone  of  the  pavement  epithelium;  mz,  slope  of  middle  zone  of  same;  d,  thrust  of 
the  door;   Ih,  thrust  of  the  lateral  hinge;   c,  composition  of  these  thrusts. 

door  lie  the  middle  piece  and  the  lateral  hinges.  Their  total  thickness 
is  usually  greater  than  elsewhere,  and  in  the  lateral  hinges  the  outer 
course  cells  are  thin  and  the  inner  thick  and  are  constricted  with  many 
constrictions  {30  —  6-8).  As  these  merge  into  the  middle  piece  the 
two  cell  courses  become  nearly  equal  in  thickness  and  the  walls  are 
thick.  The  threshold  is  broad  and  semicylindrical  in  form  (jo  —  5-8). 
The  outer  third  as  seen  in  sagittal  section  (the  "doorstep")  bears 
glandular  hairs,  the  middle  third  of  pavement  cells  supplying  a  volu- 
minous velum  of  balloon  cells,  and  the  inner  third  being  dense  pave- 
ment {2j  —  2).  The  whole  is  surrounded  by  the  massive  trap  walls, 
giving  firm  support.  The  lower  part  of  the  door,  when  closed,  rests 
cramped  into  the  relatively  narrow  arc  of  the  threshold,  exerting  a 
firm  pressure  by  its  middle  piece  {30  —  8).  In  the  set  posture  the 
upper  part  of  the  door  assumes  a  convex  form,  thereby  increasing  the 
pressure  of  the  door  selvage  on  the  pavement,  widening  the  angle 
between  the  two  {30  —  3).  Just  after  release,  the  door,  now  in  the 
relaxed  posture,  has  its  upper  part  convex.  It  is  watertight  in  this 
condition.    As  water  is  withdrawn  the  upper  half  of  the  door  becomes 


Francis  E.  Lloyd  —  256  —  Carnivorous  Plants 

more  and  more  concave  till  the  set  posture  is  reached.  This  account 
has  been  substantiated  by  a  photographic  record  of  silhouette  of  living 
traps  in  the  set  and  relaxed  condition  of  two  related  species.  Seeds  of 
U.  Wehvitschii  collected  by  Young  in  Angola  were  grown  for  me  at 
the  Edinburgh  Royal  Botanical  Garden  in  1934  and  the  traps  studied 
there.  U.  capensis  was  studied  alive  at  Capetown  later,  and  the  results 
were  pubHshed  in  1936  {24  —  5)  (Lloyd  1936&). 

Another,  an  Australian  species,  U.  lateriflora,  typical  of  a  small 
group  of  species  distributed  in  S.  E.  Asia,  and  Australia,  having  very 
small  traps  less  than  i  mm.  long,  yielded  to  experimental  methods 
(1936c)  and  the  results  are  shown  in  33  —  9,  demonstrating  that  the 
behavior  is  quite  like  that  in  U.  capensis  and  U.  Welwitschii.  The 
living  material  was  available  at  Sydney,  N.  S.  W. 

The  same  behavior  is  displayed  by  U.  caerulea  (Asia)  {24  —  2)  and 
by  U.  cornuta  (N.  Amer.)  (jo  —  3)  in  both  of  which  the  living  trap 
was  studied. 

In  all  these,  when  the  trap  is  in  the  set  condition  the  outer  selvage 
of  the  door  rests  on  the  pavement,  held  there  firmly  by  the  thrust  of 
the  lateral  hinges.  The  wide  angle  between  door  and  threshold  is 
filled  by  the  massive  velum,  preventing  inleakage  of  water.  A  thrust 
on  the  tripping  mechanism,  the  kriss  hair  (p.  259)  in  U.  capensis  and  U. 
Welwitschii,  a  group  of  sessile  glands  in  U.  caerulea  and  U .  cornuta, 
disturbs  a  dehcate  balance  of  forces  in  unstable  equilibrium,  and  the 
trap  is  ''fired." 

Both  U.  monanthos  {24  —  3)  and  Polypompholyx  {24  —  8)  act  in 
the  same  way,  and  they  also  have  been  studied  in  the  living  condition. 
U.  monanthos  was  grown  for  me  in  Edinburgh  in  1934  (1936a)  and 
Polypompholyx  could  be  examined  in  1936  at  the  University  of  Western 
Australia  at  Perth  near  which  it  grows.  The  structures  involved  are, 
however,  to  be  considered  separately. 

U.  monanthos  {j4  —  1-5)-- — In  this  and  allied  species,  the  thresh- 
old is  very  broad,  front  to  back,  and  near  its  inner  limit  is  bent, 
curving  downwards.  Beyond  the  bend  lies  the  dense  pavement 
which  receives  the  middle  piece,  which  is  therefore  applied  on  the 
inside  of  the  bend.  This  looks  like  a  pretty  poor  arrangement,  yet 
it  works.  The  major  zone  in  front  of  the  bend  is  occupied  by  an 
ample  velum  which  arises  also  from  the  walls  projecting  in  front  of 
the  door.  Here  is  formed  a  complete  massive  ring  resting  against  the 
bulge  of  the  upper  part  of  the  door  when  in  the  relaxed  posture.  When 
in  the  set  posture,  the  inner  portion  of  the  velum  arising  from  the 
pavement  alone  continues  to  block  the  entrance  of  water.  The  door  is 
still  longer  than  in  U.  capensis  etc.,  but  the  middle  piece  is  relatively 
smaller,  and  the  middle  area  is  correspondingly  large,  occupying  about 
four-fifths  of  the  door  length.  When  in  the  set  posture,  the  whole  of 
this  large  area  is  concave,  so  that  the  sagittal  curve  is  now  continuous 
with  that  of  the  middle  piece,  which  by  virtue  of  the  thrust  of  the 
lateral  hinges  is  impressed  against  the  dense  pavement  just  inside  the 
bend  of  the  threshold.  The  trigger  consists  of  a  group  of  sessile  hairs 
just  above  the  bend  of  the  door.  The  action  when  the  trap  is  fired  is 
like  that  in  U.  capensis.  It  must  be  confessed  at  this  point  that  my 
earlier  account  of  door  action  (1932a)  based  on  preserved  material  of 


Chapter  XIV  —  257  —  The  Utricularia  Trap 

U.  Hookeri  was  wrong.     This  species  conforms  in  every  way  to   U. 
monanthos.     Living  material  was  examined  in  Sydney,  N.  S.  W. 

In  Polypojnpholyx  the  case  is  again  quite  special,  for  here  the  door 
is  as  broad  as  long,  but  works  as  in  U.  monanthos.  The  whole  trap 
to  be  described  (p.  262)  is  extremely  curious.  Because  of  the  thickness 
of  the  walls  and  other  parts  and  the  masses  of  glandular  hairs  on  the 
door  and  on  the  floor  of  the  antechamber,  it  was  difficult  to  study 
the  trap  in  action,  and  especially  to  photograph  it.  Nevertheless  the 
attempt  succeeded  {24  —  8).  When  the  trap  is  set,  the  door  shows  a 
simple  curve,  along  the  sagittal  line  from  the  upper  hinge,  which  is 
very  thick  and  does  little  bending,  to  the  edge  which  lies  just  within 
the  ridge  of  the  pavement.  When  relaxed,  just  after  discharge,  the 
lower  two-thirds  of  the  door  is  convex,  the  upper  hinge  showing  little 
movement  —  a  slight  bending  in  its  distal  zone  only.  It  is  evident 
that  the  very  deep  cells  of  the  outer  course  of  this  tissue  exert  a 
strong  tangential  pressure  on  the  lower  parts  of  the  door,  ensuring  a 
tight  apphcation  of  the  selvage  to  the  pavement  when  the  door  is 
relaxed  and  a  still  tighter  application  when  the  trap  is  set. 

The  variety  of  traps.  —  The  following  account,  necessarily  brief, 
will  give  some  idea  of  the  diversity  of  structure  and  form  displayed  by 
the  traps  of  Utricularia,  Biovularia  and  Polypompholyx.  We  may  con- 
veniently follow  the  grouping  into  those  having  short  and  long  tubular 
entrances. 

Traps  with  a  short  tubular  entrance.  —  These  are  found  in  the  U. 
vulgaris  type,  in  U.  Lloydii  Merl  and  U.  nana  St.  Hil.,  in  a  group  of 
few  species  represented  by  U.  globulariaefolia,  in  Biovularia  and  in  U. 
purpurea  and  associates. 

The  trap  of  U.  vulgaris  has  been  sufficiently  described  already. 
Those  of  such  species  as  U.  gibba,  and  of  the  terrestrial  U.  subulata, 
U.  biloba  [27  —  i)  and  a  number  of  others,  all  small  plants,  show 
only  slight  differences.  In  U.  neottioides  {zy — -9),  growing  in  running 
water,  the  traps  present  a  streamhne  contour  and  a  deep  overhang. 
In  those  species,  such  as  U.  reniformis,  which  live  more  or  less  epi- 
phytically in  wet  moss,  etc.,  the  antennae  are  broad  at  the  base,  un- 
branched,  and  appear  to  be  adapted  to  holding  water  in  the  entrance 
by  offering  support  for  surface  films.  Sometimes  the  entrance  is 
tilted  forward  (U.  longifolia)  involving  the  threshold  {26  —  4),  so  that 
the  pavement  also  faces  forward.  There  are  two  apparently  unique 
S.  American  species,  both  small  and  terrestrial,  U.  Lloydii  Merl  and 
U.  nana  St.  Hil.  The  former,  U.  Lloydii,  has  two  forms  of  trap,  one  on 
the  leaves,  the  other  on  the  stolons  {28 — 1-4).  They  difTer  in  the 
character  of  the  hairs,  and  notably  in  the  presence  on  the  door  of  a 
single  tripping  hair,  with  a  saddle  shaped  cell  next  its  base  apparently 
to  facihtate  hinge  movement,  on  the  leaf  trap,  which  has  also  slender 
backwardly  curved  antennae,  while  the  stolon  trap  has  short  forwardly 
directed  antennae  with  long  hairs,  but  no  tripping  bristle  on  the  door. 
Such  differences  are  difficult  to  explain.  In  U.  nana  the  trap  is  quite 
devoid  of  appendages,  but  is  otherwise  much  like  that  of  If.  Lloydii 
except  that  the  tripping  mechanism  consists  of  two  bristles  set  trans- 
versely {28  —  5,  6)  (Lloyd  1932a). 

U.  globulariaefolia  and  U.  amethystina  represent  a  group  of  Central 


Francis  E.  Lloyd  —  258  —  Carnivorous  Plants 

and  South  American  species  which  are  terrestrial.  Their  traps  {28  — 
7-9)  are  superficially  much  different  from  the  vulgaris  type,  yet  con- 
form in  having  a  short  tube  entrance,  though  this  has  a  long  funnel- 
shaped  approach,  lined  with  numerous  long-stalked  glandular  hairs. 
The  door,  while  lacking  in  well  demarked  mechanical  areas,  is  ex- 
tremely flexible  because  of  very  numerous  constrictions  in  the  inner 
course  cells  (Lloyd  193 i). 

Biovularia  has  a  door  in  which  the  middle  piece  is  half  its  depth 
(27  —  5,  6).  At  the  upper  edge  of  this  there  are  always  six  tripping 
bristles  arranged  transversely  and  radiating  outwardly  (Lloyd  1935a). 
In  U.  purpurea  and  its  allies  (27  —  2-4)  the  tripping  hairs  arise  in  a 
radiating  manner  from  a  tubercle  centrally  placed  on  the  door  which 
is  naked  of  other  glands.  Either  the  entrance  is  quite  simple  and 
unadorned  {U.  purpurea)  or  the  lower  lip  may  be  extended  into  a  long 
upturned  rostrum  carrying  a  few  unicellular  hairs,  with  a  tuft  of  these 
on  each  side  of,  but  somewhat  above,  the  middle  of  the  entrance 
{U.  elephas  Luetz.).  The  tripping  hair  consists  of  a  long  stalk  {zg  — 
7),  an  elongation  of  an  epidermal  cell  which  is  part  of  the  tubercle, 
expanded  at  the  top,  bearing  a  short  basal  cell,  and  a  large  mucilage 
cell  with  expanded  cuticle.  The  edge  of  the  door  is  thickened  by  a 
beading  which  rests  in  a  slight  depression  of  the  narrow  pavement 
(Lloyd  1933a,  1935a;  Luetzelburg) .  The  outer  surface  hairs  are 
sickle-shaped  mucilage  cells  and  sessile,  oil-bearing  ones  (29  —  6). 

The  mechanical  response  following  a  contact  of  prey  against  the 
tripping  hairs  cannot  of  course  be  seen,  but  may  be  fairly  guessed  at. 
Movement  of  the  hairs  causes  slight  rotation  of  the  knob  to  which  they 
are  attached.  This  results  in  slight  displacement  of  the  door  middle 
piece,  disturbing  the  even  contact  of  its  edge  on  the  threshold,  thus 
allowing  the  pressure  of  water  to  push  it  in.  In  a  diagram  {26  —  8) 
I  have  shown  the  action  (much  exaggerated)  as  in  the  up  and  down 
plane.  The  thinness  of  the  door  about  the  knob  allows  its  rotation 
(Lloyd  1933a). 

Traps  with  a  long  tubular  entrance.  — ■  The  species  belonging  to  this 
group  present  a  by  no  means  homogeneous  picture,  and  in  some  cases 
are  obviously  less  closely  related  to  each  other  than  those  in  the 
short-tube  entrance  group.  With  regard  to  the  mechanism  of  the 
entrance  they  fall  into  two  sub-groups:  (7)  That  in  which  the  door 
when  in  relaxed  posture  presents  along  the  sagittal  axis  a  single  con- 
tinuous curve;  and  (2)  that  in  which  the  door  shows  two  curves,  a 
strong  one  in  the  upper  hinge  region,  and  a  lesser  one  in  the  middle 
piece.  To  the  former  belong  U.  cornuta  (N.  America)  and  caerulea 
(Old  World),  the  latter  representing  a  large  number  of  allied  species. 

U.  cornuta  will  serve  as  an  example  (jo  — 1-8) .  The  trap  is 
wholly  devoid  of  appendages.  Just  below  the  entrance  there  is  a 
rounded  group  of  sessile  glands  (Schimper)  which  may  be  regarded 
as  a  lure  for  prey.  The  tripping  mechanism  consists  of  a  scattered 
group  of  sausage-shaped  glands  on  the  lower  half  of  the  upper  hinge. 
They  can  be  seen  when  one  looks  straight  into  the  entrance.  The  pos- 
ture of  the  door  in  the  living  trap  in  set  and  relaxed  condition  was 
studied,  and  recorded  photographically.  In  the  set  posture,  the  outer 
selvage  of  the  middle  piece  rests  on  the  middle  zone  of  the  pavement. 


Chapter  XIV  —  259  —  The  Utricularia  Trap 

From  that  point  as  seen  along  the  sagittal  line,  the  door  is  gently 
concave  throughout  its  whole  length.  The  whole  extent  of  the  middle 
piece  is  covered  by  the  velum  {24  —  6),  leaving  the  upper  region  with 
the  tripping  hairs  exposed.  A  touch  on  this  surface  discharges  the 
mechanism,  and  the  door  immediately  returns  to  the  closed  but  now 
relaxed  posture  in  which  the  whole  door  is  convex  outwardly.  In  the 
set  posture,  while  concave  along  its  middle  axial  line,  it  is  slightly 
convex  transversely,  that  is,  it  is  saddle-shaped.  It  was  possible  to 
make  transverse  sections  of  the  hving  trap,  and  these  disclosed  the 
door  posture  in  the  middle  piece  region,  from  which  it  was  clearly  seen 
that  the  close  application  of  its  selvage  to  the  pavement  is  procured  by 
the  thrust  of  the  thick  lateral  hinges.  The  release  from  this  posi- 
tion results  only  from  the  longitudinal  extension  of  the  shallow  fold 
already  present  in  the  set  posture  of  the  door. 

ScHiMPER  (1882)  was  the  only  previous  student  of  this  plant. 
Since  he  accepted  the  Cohn  and  Darwin  view,  he  was  not  aware  of 
any  special  significance  to  be  attached  to  the  structures  of  the  entrance 
mechanism. 

U.  caerulea  {31  —  i),  U.  ogtnospenna,  U.  equiseticaulis,  U.  bifida 
(Asia),  U.  cyanea  (Australia)  and  a  lot  more  species,  with  the  general 
features  of  the  trap  very  similar,  conform  to  U.  cornuta,  except  in 
relatively  unimportant  details.  They  are  usually  provided  with  two 
simple  antennae  and  a  small  overhang,  and  the  tripping  mechanism 
consists  of  a  group  of  short-stalked  glandular  hairs,  the  longer  nearer 
the  top  of  the  door,  and  the  shorter  as  the  middle  piece  is  approached. 
Goebel's  very  brief  account  of  the  trap  of  caertdea  shows  the  general 
position  of  the  door  correctly  though  sketchily.  U.  bifida  is  evidently 
of  this  group  (Goebel)  as  I  have  myself  determined,  confirming 
Goebel's  drawing  as  correct.  Only  bifid  hairs  are  present  in  the 
interior  of  the  trap,  as  Darwin  observed.  In  such  species,  however,  the 
glands  below  and  at  the  edge  of  the  threshold  have  a  single  capital. 

As  a  type  of  the  second  sub-group,  we  choose  U.  capensis,  and 
U.  Welwitschii.  A  number  of  other  species  pecuhar  to  S.  America, 
Central  and  South  Africa,  all  small  plants,  fully  conform  to  this  type. 
A  description  of  the  form  of  the  door  and  of  its  manner  of  operating 
has  already  been  given  above  (p.  255).  The  tripping  mechanism  (jz  — 
8,  9)  consists  of  a  curiously  formed  large  trichome,  the  capital  cell 
of  which  resembles  in  shape  a  Malay  kriss,  called  therefore  the  kriss 
trichome  (Lloyd  1931),  supplemented  by  a  group  of  curved  glandular 
hairs  on  the  upper  part  of  the  door.  In  some  species  the  kriss  trichome 
is  not  present,  its  place  taken  by  large  globular  sessile  glandular  cells 
{U.  pellata,  U.  Deightonii  Ms.)  {31  —  6,  7).  A  conspicuous  feature  of 
this  group  of  plants  is  the  development  of  a  funnel  shaped  approach 
to  the  entrance  by  spreading  of  the  cheeks,  and  the  lining  of  this 
funnel  with  about  ten  rows  of  stout  glandular  hairs  radiating  towards 
the  entrance.  In  U.  Welwitschii  these  are  reduced  to  mere  sessile 
glands  but  a  rostrum  bears  a  radiating  row  of  longer  glandular  hairs 
{31  —  4).  The  S.  American  U.  peltata,  so  like  U.  capensis  except  for 
the  globular  tripping  hairs,  has  in  common  with  some  African  species 
(£/.  Deightonii  in  Ms.)  minute  peltate  leaves  very  thickly  covered  with 
stiff  mucilage   (29  —  9,   10),  a  significant  fact  of  geographical  distri- 


Francis  E.  Lloyd  —  260  —  Carnivorous  Plants 

bution.  Some  Asian  species  {U.  rosea,  U.  Warhurgii)  (ji  —  lo,  ii) 
studied  by  Goebel  have  an  extension  of  the  funnel  to  form  a  long  pro- 
jecting beak  of  the  shape  of  a  knife  blade,  armed  with  gland  hairs. 
Apparently  some  degree  of  trap  dimorphism  occurs  in  U.  rosea,  affect- 
ing the  size  of  the  trap  and  the  form  of  the  beak  (Lloyd  1932a).  Species 
showing  these  pecuharities  are  found  also  in  Australia  and  New  Guinea. 
U.  Kirkii,  occurring  in  central  Africa,  is  apparently  unique  (jj  — 
I,  2).  Of  the  same  general  form  and  appearance  of  U.  capensis,  the 
threshold  retreats  into  the  interior,  and  has  no  step  leading  to  the 
pavement.  The  tripping  mechanism  consists  of  two  long  upwardly 
curved  bristles  based  at  the  juncture  of  the  hinge  and  the  blunt  edged 
middle  piece.  The  latter  is  fortified  by  two  large  tubercles  developed 
from  inner  course  cells,  each  semi-pyriform,  with  a  thin  line  of  tissue 
between,  along  which  the  middle  piece  can  fold  during  opening. 

U.  orhiculata  (32  —  1-4).  —  This,  representing  a  group  of  species  in 
Asia  and  Africa,  was  examined  by  Goebel,  who  did  not  observe  more 
than  the  stubby,  branched,  glandular  antennae.  The  entrance  mech- 
anism is  very  peculiar.  The  velum  is  supplemented  by  membranes 
arising  from  the  stalked  glands  of  the  step.  The  tripping  mechanism 
of  the  door  consists  of  three  glandular  hairs  set  in  a  triangle  on  the 
upper  half  of  the  door.  One  is  mallet-shaped,  placed  at  the  inwardly 
directed  apex  of  the  triangle.  The  other  two  are  at  first  large, 
globular,  nearly  sessile  glands  (32  —  6).  In  maturity,  the  capital,  con- 
taining a  large  mass  of  stiff  mucilage,  bursts  in  a  regular  fashion,  re- 
leasing a  long  sausage-like  mass  of  jelly  which  remains  attached  to  the 
hair.  Two  of  these  hang  down  in  front  of  the  entrance,  and  with  the 
mallet-shaped  hair  receive  the  impact  of  prey  which  trips  the  door 
(Lloyd  1932a).  A  Thibetan  species  (Brit.  Mus.:  L.S.  and  T.  802), 
similar  to  U.  muUicaulis,  has  a  broad  fan-shaped  rostrum  armed  with 
radiating  glands,  which  extend  forward  and  in  front  of  the  entrance. 
U.  hrachiata  is  also  like  this  (Compton)  (32  —  5,  7-9). 

U.  longiciliata  {jj  —  3,  4)  is  a  unique  terrestrial  species  of  S. 
America,  and  has  been  described  by  Merl  (191 5).  The  traps  are 
very  small  (0.3  mm.).  The  lower  lip  projects  as  a  strong  bifurcated 
rostrum,  the  arms  extending  laterally.  The  upper  lip  forms  a  short, 
slightly  upturned  beak.  The  middle  piece  of  the  door  is  exceptionally 
thick  and  bears  a  single  tripping  hair  (Merl).  This  consists  of  a  thin 
stalk  and  a  disc  shaped  basal  cell  and  a  capital  of  spindle  shape.  It  pro- 
jects straight  forward  (Lloyd  1932a).  The  internal  glands  are  few  in 
number  but  large. 

A  small  group  of  species  from  India,  East  Indies  and  Australia  in- 
cludes U.  lateriflora,  U.  simplex  (Australian),  U.  calliphysa  (Borneo) 
and  two  probably  unnamed  species  from  India  and  Ceylon,  all  terres- 
trial and  small  in  size  (jj  —  5-9).  The  minute  (0.3-0.5  mm.)  traps 
have  a  pronounced  upper  rostrum  and  a  row  of  short  glandular  hairs 
on  each  side  of  the  trap  leading  up  to  the  lower  angles  of  the  entrance. 
Sometimes  there  is  a  frieze  of  low  tubercles  on  each  side  above  the 
mouth  (Stapf).  The  tripping  hairs  (jj  —  8)  stand  in  a  prominent 
group,  marked  by  sessile,  transversely  long  capitals  on  the  upper  part 
of  the  door.     The  internal  glands  are  few  but  large. 

We  shall  now  speak  of  that  variety  of  traps  represented  in  the  fore- 


Chapter  XIV  —  261  —  The  Utricularia  Trap 

going  discussion  by  U.  monanthos  (p.  256)  or  alternatively  by  U. 
dichotoma  (they  are  much  alike).  The  structure  of  the  entrance 
mechanism  has  been  described.  Beyond  this  is  the  form  of  the  trap, 
with  its  appendages  and  glands. 

The  appendages,  when  a  full  complement  is  present,  consist  of  a 
rostrum,  upper  (dorsal)  wings  and  lower  (ventral)  wings  {34  —  i).  The 
rostrum  projects  forward  from  the  overhang;  the  upper  wings  arise 
one  from  each  side  of  the  trap  above  the  door,  and  the  lower  wings 
extend  each  from  a  point  near  the  insertion  of  the  stalk  up  to  the 
lower  angles  of  the  entrance.  In  the  various  species  one  pair  or  the 
other  of  the  wings  may  be  either  suppressed  or  greatly  enlarged  or 
extended,  with  great  differences  in  the  character  of  their  margins 
{34>  35)-  The  rostrum  is  always  present,  but  may  be  short  or  ex- 
tended, to  a  maximum  in  U.  tuhidata,  and  sometimes  once  branched 
{U.  volubilis)  (34  —  6).  It  will  suffice  to  refer  the  reader  to  the  figures, 
made  with  a  minimum  of  detail,  for  some  grasp  of  the  great  variety 
within  this  restricted  group  of  purely  Australian  plants. 

In  U.  volubilis,  which  grows  anchored  in  rather  deep  water,  there 
are  three  forms  of  traps  {34  —  6).     Its  runner  stolons  bear  traps  in 
groups  of  three,  and  these  have  wings  crenately  margined,  and  the 
rostrum    is    short.      The    shoots    bear   numerous    hgulate    leaves    and 
among  these,  exposed  directly  to  the  water,  are  two  kinds  of  trap, 
large,  reaching  a  length  of  five  mm.  (this  species  has  the  largest  trap) 
with  rather  short  cylindrical  stalks,  so  that  they  stand  near  the  surface 
of  the  substrate;    and  smaller  ones  (2  mm.  or  less)  on  very  long  leafy 
stalks,  and  these  stand  4-5  cm.  above  the  substrate.     The  distinction 
between  the  water  traps  is  not  a  sharp  one  for  there  are  gradations  of 
size  and  form,  but  they  are  on  the  whole  quite  recognizable.    The  traps 
in  the  substrate  are  similar  to  those  of  U.  monanthos  in  that  the  wings, 
of  which  there  are  two  pairs,  are  not  laciniate;    the  rostrum  is  short 
and    unbranched.      The    large    water    traps    have    a   long,    sometimes 
branched  rostrum,  and  the  edge  of  the  shallow  overhang  bears  addi- 
tional  fimbriae   more   or  less   branched,   while    the    wings   are   deeply 
laciniate.     The  abundance  of  fimbriae  seems  to  clutter  up   the   front 
end  of  the  trap.     In  the  long  stalked  kinds,  the  ventral  wings  are 
much  reduced  in  size  and  may  or  may  not  have  a  single  thread-like 
lobe.     The  dorsal  wings  are  single  slender  processes,   as  is  also  the 
rostrum,  which  may  be  once  branched.    This  trap  resembles  much  that 
of  U.  tuhulata,  which  is  a  submersed  floater.     Similar  behavior  is  seen 
in  U.  Hookeri,  also  an  anchored  submersed  plant  in  which  the  traps 
are  long  stalked  {ca.  i  cm.).    It  bears  traps  of  various  sizes,  the  largest 
4  mm.   long,  to  smaller  ones   1.5  mm.   long.     In  the  large  traps  the 
wings  are  slender  and  fimbriate,  but  prominent,  and  the  rostrum  single, 
rather  long  and  straight  or  curved  downwards.     In  the  small  traps  the 
ventral  wings  are  represented  by  low  ridges,  the  slender  dorsal  wings, 
and  the  single  rostrum,  all  very  long  (34  —  7). 

In  the  little  known  floating  species  U.  tuhulata,  (j5  —  8)  the  traps 
have  a  very  long  rostrum  and  filiform  dorsal  wings,  without  branches. 
The  ventral  wings  are  absent.  In  U.  Menziesii,  different  in  habit, 
being  totally  buried  in  wet  quartz  clay  with  only  the  leaf  blades  and 
flowers  showing,  there  is  complete  uniformity  of  trap  structure  (55  — 


Francis  E.  Lloyd  —  282  —  Carnivorous  Plants 

lo,  ii),  but  physiologically  the  traps  behave  differently,  there  being 
three  sets,  one  growing  downward,  one  growing  laterally  and  one  up- 
ward {20  —  9). 

There  are  still  other  varieties  of  traps  displaying  various  permu- 
tations of  size  and  shape  of  the  appendages.  So  far  as  known  these  are 
represented  in  plate  35. 

Lastly  the  genus  Polypompholyx  {36 — ■  1-9),  the  trap  of  which  was 
described  with  respect  to  the  entrance  mechanism  on  p.  257.  It  has  a 
very  special  form  in  this  genus  (there  is  little  variety),  in  which  the 
stalk  plays  a  special  part  of  the  approach  to  the  door. 

The  form  of  the  trap  and  a  number  of  anatomical  details  were 
described  by  F.  X.  Lang  in  1901  from  material  in  the  Goebel  collec- 
tion, which  I  examined  later. 

The  traps  are  of  various  sizes,  the  largest  measuring  4  mm.  in 
length.  For  the  most  part  they  are  smaller,  about  1.5-2  mm.  In  one 
species  (possibly  P.  latifolia,  though  Bentham  did  not  admit  this 
species)  the  traps  are  dimorphic  both  in  size  and  structure  {36  —  8,  9). 
In  all  the  species  (probably  four)  they  present  the  following  characters. 
Viewed  from  above,  the  body  of  the  trap  is  seen  to  be  roundly  trian- 
gular with  a  forked  rostrum  in  front  and  a  broad  wing  on  either  side. 
The  margins  are  entire  but  carry  stiff  hairs.  The  fork  of  the  rostrum 
is  seen  to  clasp  the  stalk,  over  which  the  whole  forward  part  of  the 
trap  is  incHned.  The  top  of  the  trap  body  is  almost  fiat  —  this  is  the 
upper  side  of  the  three  sided  body.  Seen  from  below  the  trap  body  evi- 
dently has  two.  lateral  faces,  from  the  upper  angles  of  which  the 
wings  extend.  The  stalk,  which  now  hides  the  rostrum,  gradually 
swells  on  its  approach  to  the  trap,  and  is  molded  into  two  low 
ridges,  one  on  each  side,  just  before  the  insertion  is  reached.  These 
ridges  are  strongly  ciliated,  forming  guiding  fences  directing  prey  to 
the  entrance  of  the  trap,  which  is  approached  only  laterally  because  of 
the  contact  of  the  rostrum  on  the  stalk.  The  wings  complete  two 
funnel  effects,  one  on  each  side.  Viewed  now  from  the  side  the  stalk 
is  seen  to  be  increasingly  massive  as  it  approaches  the  trap,  and  this  is 
due  to  a  large  intercellular  space  which  inflates  the  lower  moiety 
below  the  rostrum.  The  upper  half  is  expanded  into  a  ridge  which 
becomes  deeper  under  the  rostrum,  then  to  be  reduced.  The  loss  of 
height  is,  however,  compensated  for  by  a  comb  of  stiff  hairs  with  long, 
tapering  capitals,  and  their  ends  curiously  distorted  (Lang)  as  if  bent 
during  development  by  impinging  against  the  rostrum.  This  ridge 
being  tightly  pressed  against  the  rostrum  divides  the  approach  to  the 
door  into  two  lateral  vestibules,  so  that  the  prey  must  advance  under 
the  wings  from  behind,  to  be  diverted  by  the  combs  of  bristles  on  the 
sides  of  the  stalk  toward  a  space  beneath  the  rostrum.  This  space  has 
the  wall  of  the  trap  for  its  floor  and  the  rostrum  and  door  for  its 
roof,  and  is  an  antechamber  leading  to  the  entrance  proper.  Its  floor 
is  clothed  with  mucilaginous  hairs  with  long  whip-lash  capitals,  lying 
pointed  toward  the  entrance.  The  roof,  which  is  chiefly  the  door, 
bears  similar  hairs,  longer  toward  the  door  insertion,  shorter  toward 
its  free  edge.  The  entrance  is  a  small  semi-circular  hole  in  the  trap 
wall,  which  stands  at  a  steep  angle  with  the  floor  of  the  antechamber. 
The  semicircular  edge  of  the  entrance  is  clothed  with  pavement  epi- 


Chapter  XIV  —  263  —  The  Utricularia  Trap 

thelium,  the  middle  zone  of  which  lies  just  within  this  edge.  The 
outer  zone,  which  carries  the  velum,  faces  outwardly  {36  —  8,  9).  The 
inner  region  bears  glandular  hairs  of  various  forms,  at  first  with 
conical  capitals,  then  with  bifids.  Quadrifids  of  large  size  occupy  the 
interior  wall  surface.  The  door  lies  almost  at  right  angles  to  the  plane 
of  the  threshold,  result  of  the  forward  bending  of  the  rostrum.  The 
action  of  the  door  has  been  already  described  (p.  257).  Histologically 
the  door  presents  a  unique  feature  in  the  very  great  depth  of  the  inner 
course  cells  in  the  upper  hinge  region,  the  door  gradually  tapering  in 
thickness  toward  the  edge.  Of  this  we  may  say  that  these  thick  cells 
can  exert  a  strong  tangential  thrust  so  as  to  press  the  door  selvage 
firmly  against  the  pavement,  the  outer  zone  of  which  bears  the  velum, 
seen  in  living  material  at  Perth,  W.  Australia.  The  door  selvage  is  not 
thickened.  Its  cells  are  of  equal  thickness  in  both  courses,  and  there  is 
no  obvious  middle  piece.  This  means  that  the  door  selvage  must  bend 
over  the  pavement,  not  impinge  edgewise  on  it.  The  tripping  mechan- 
ism consists  of  short,  bent,  glandular  hairs,  30-40  in  number,  scattered 
on  the  surface  of  the  door  below  the  middle  point  {36  —  5). 

The  dimorphism  in  the  traps  of  P.  latifolia  has  been  indicated. 
There  are  two  sizes  of  traps.  In  the  larger,  the  threshold  behind  the 
pavement  bristles  with  a  dense  fringe  of  conical  glands  of  graduated 
sizes,  described  by  Lang.  Inside  this  pale  stand  some  bifid  glands. 
In  the  small  sized  trap  there  are  no  conical  glands.  In  their  place 
there  are  glands  with  single-celled  capitals  of  the  form  of  the  bifids  and 
quadrifids.    Inside  the  traps  are  bifids  {36  —  8,  9). 

The  walls  consist  of  four  courses  of  cells,  the  two  epiderms  and 
two  courses  of  parenchyma.  The  epiderms  vary  in  thickness.  The 
outer  is  thickest  in  the  middle  of  the  sides,  and  the  inner  thickest  at 
the  angles,  here  forming  a  hinge  structure. 

The  total  thickness  of  the  three  walls,  which  have  four  courses  of 
cells  throughout,  is  always  greatest  at  the  middle  of  their  faces,  pro- 
ducing a  hinge  effect  at  the  angles.  Further,  the  outer  epiderniis  is 
always  thin  at  the  angles  and  progressively  thicker  toward  the  middle 
of  the  faces,  while  the  inner  is  thick  at  the  angles  and  th  n  elsewhere, 
the  more  readily  allowing  compression  on  the  inside  of  the  angles  and 
on  the  outside  of  the  faces.  It  is  evident  from  mere  inspection  that 
these  massive  walls  must  exert  a  big  pull  when  the  trap  is  exhausted 

of  water  (3^  —  7)- 

In  closing  this  account  one  cannot  but  wonder  at  the  astonishing 
variety  of  trap  structure.  It  is  not  less  astonishing  that  there  is  no 
evidence  that  one  form  of  trap  is  superior  to  another  in  action.  The 
fact  of  variety  is  one  with  the  same  phenomenon  observed  when  we 
survey  attentively  some  other  unit  of  structure.  It  seems  as  though 
nature,  or  to  deify  her  fruitfulness,  Nature,  is  not  nor  ever  has  been 
content  to  make  some  one  thing,  however  satisfactory,  and  to  let  it  go  at 
that.  She  must  show  that  she  is  not  bound  to  the  details  of  a  pattern 
that,  in  this  case,  she  can  make  a  whole  shelf  full  of  different  kinds  of 
traps,  as  if  to  puzzle  you  to  pick  the  best. 

Digestion.  —  Goebel  remarked  the  great  difficulty,  because  of  their 
small  size,  of  studying  the  traps  ot  Utricularia  to  determine  the  pres- 
ence or  absence  of  digestive  activity.     It  had  of  course  been  quite 


Francis  E.  Lloyd  —  264  —  Carnivorous  Plants 

apparent  to  Darwin,  Cohn,  Mrs.  Treat  and  others  that  animals 
caught  in  the  traps  disintegrate,  but  the  natural  inference,  that  diges- 
tion was  effected  by  the  plant,  was  not  sustained  by  evidence,  for  a 
few  experiments  done  by  Darwin  in  which  he  introduced  minute 
fragments  of  meat,  albumen  and  cartilage  into  the  traps,  gave  only 
negative  results,  and  he  concluded  that  Utricularia  cannot  digest  its 
prey.  Bijsgen  fared  no  better  —  he  worked  with  an  acid  medium 
with  which  Luetzelburg  also  got  meagre  results. 

GoEBEL  regarded  Utricularia  as  capable  of  digestion  because  of  its 
close  relationship  to  Pinguicula,  but  confessed  that  no  evidence  had 
been  forthcoming.  Luetzelburg  (1910),  one  of  his  students,  obtained 
evidence  with  sap  expressed  from  large  numbers  of  traps  removed 
individually,  ground  up  with  clean  sand  and  glycerin,  and  perco- 
lated. The  extract  thus  obtained  showed  a  sHght  activity,  visible 
after  3  days,  in  an  acid  medium.  It  was,  however,  much  more  active 
in  an  alkaline  medium,  and  the  conclusion  that  a  trypsin  was  present 
was  arrived  at. 

During  prolonged  observation  of  the  experiments  it  was  noticed 
that  there  was  never  any  odor  of  putrefaction,  and  culture  tests 
showed  that  bacteria  did  not  grow  in  the  presence  of  the  expressed 
juices,  yet  these  could  liquify  gelatin  in  four  days.  The  presence  of  an 
agent  inhibiting  the  growth  of  bacteria  was  inferred  and  this  inference 
was  strengthened  by  experimental  evidence  that  bacteria  are  only 
feebly  produced  in  trap  fluid  put  on  a  gelatin  surface.  This  led  to  the 
discovery  of  benzoic  acid  in  the  trap  fluid,  this  substance  having  been 
found  also  in  the  leaves  and  glands  of  Pinguicula  by  Loew  and  Aso, 
and  in  the  pitchers  of  Cephalotus  by  Goebel. 

Adowa  (1924)  attacked  the  same  problem.  He  first  made  sahne 
and  acid  (HCl)  extracts  of  the  whole  plant,  and  tested  their  efficacy 
in  digesting  gelatin,  fibrin,  milk  casein  and  egg-albumin.  The  tissues 
of  the  whole  plant  contain,  he  found,  two  proteoclastic  ferments, 
alpha-  and  beta-protease,  the  latter  active  in  an  acid  medium.  The 
former  is  rendered  a  httle  more  active  with  the  addition  of  CaCl2  to 
it  in  a  neutral  medium.  He  then  made  extracts  of  three  lots  of  ma- 
terial (fl)  stems,  {h)  green  (young)  traps  and  (c)  red  and  blue  traps, 
and  tested  these  separately.  In  neutral  gelatin,  the  effects  of  these 
three  extracts  were  in  the  ratios  of  18.5  for  green  traps,  6.5  for  colored 
traps,  and  3.5  for  stems;  in  alkaline  gelatin  the  ratios  were  22,  23.5 
and  6.  In  acid  gelatin  the  effects  were  rapid  at  first  but  stopped  quickly, 
while  in  the  alkahne  and  neutral  media  the  action  was  continuous.  The 
conclusions  were  drawn  that  (/)  the  extract  of  the  traps  contained  more 
alpha-protease  than  that  of  the  stems;  (2)  that  of  green  traps  affects 
alkaline  gelatine  over  a  long  period  (24  days)  to  the  same  extent  as 
that  of  colored  traps;  (3)  the  extract  of  green  traps  acts  more  ener- 
getically on  neutral  gelatine  than  that  of  the  colored  traps;  {4)  the 
protease  content  of  branches  is  very  insignificant;  (5)  alkahne  gela- 
tin is  the  best  medium  for  digestion  by  undiluted  extracts,  neutral 
gelatin  for  diluted  extracts  (50%  and  less);  {6)  beta-protease  both 
from  the  branches  and  from  the  traps  shows  a  weaker  activity  than 
alpha-protease,  and  (7)  extracts  diluted  8-16  times  act  in  neutral  but 
not  in  alkahne  medium. 


Chapter  XIV  —  265  —  The  Utricularia  Trap 

It  seemed  evident  from  all  the  foregoing  that  digestive  ferments 
are  present,  but  principally  in  the  traps. 

KiESEL  (1924),  however,  took  the  opposite  view.  He  found  that 
fragments  of  fibrin  were  digested  in  the  traps,  but  if  acidified  with 
0.2%  HCl  were  not.  The  trap  fluid,  obtained  by  means  of  a  fine 
pipette  directly  from  the  traps  and  preserved  under  toluol  showed 
no  power  to  digest  fibrin,  gelatin  or  albumin.  He  concluded  that  the 
digestion  in  the  traps  of  Utricularia  is  the  work  of  microorganisms. 
What  these  might  be  was  investigated  by  Stutzer  (1926).  Traps 
washed  in  sterile  physiological  solution  were  minced  and  the  contents 
thus  obtained  were  sown  on  agar  plates.  He  found  bacteria  of  the 
Bacterium  coli  group  to  be  dominant  and  suggested  that  they  play  the 
important  role  of  digestion.  Other  bacteria  play  a  secondary  role. 
Those  of  the  kind  found  in  the  digestive  tracts  of  insects  etc.,  are  also 
to  be  met  with,  but  these  he  thought  play  the  same  role  in  the  traps 
as  there,  namely,  to  conserve  the  nutrient  mass  during  digestion  and 
hinder  the  development  of  putrefactive  bacteria.  It  is  possible,  in  ad- 
dition, that  Bacillus  aquatilis  communis,  one  of  the  soil  bacteria,  takes 
some  part  in  digestion,  since  it  can  digest  albumin. 

And  there  the  matter  stands  at  the  moment.  On  the  one  hand, 
it  is  held  that  the  presence  of  benzoic  acid  inhibits  bacterial  action, 
and  that  any  digestive  action  is  the  work  of  the  ferments  secreted  by 
the  trap  itself;  on  the  other  the  digestion  is  referred  to  the  activity  of 
bacteria.     Hada    (1930)    takes   a   middle   ground,   holding   that   "the 

animals  captured are  decomposed  not  only  by  the  enzyme  secreted 

by  the  plant,  but  also  by  the  bacteria  which  increase  rapidly  after  the 
death  of  the  animals."  Since  his  paper  is  in  Japanese,  I  do  not  know 
what  evidence  he  puts  forward. 

Prey  and  their  fate.  —  The  presence  of  sugar  as  well  as  mucilage 
in  the  glandular  hairs  at  the  entrance  of  U.  vulgaris,  shown  by  Luetzel- 
BURG,  was  thought  by  him  to  indicate  that  these  hairs  form  a  lure  to 
attract  animals.  The  presence  of  special  groups  of  glands  near  the 
entrance  in  some  species  {e.g.  U.  cornuta)  seems  to  support  this  view. 

While  it  is  true  enough  that  animal  prey  captured  by  the  traps  of 
Utricularia  sooner  or  later  succumb  and  are  digested,  there  are  ex- 
ceptions in  organisms  which  are  able  to  live  and  multiply  in  the  re- 
stricted space  of  the  interior  of  the  trap,  notably  Euglena,  Heteronema, 
Phacus  (Hegner)  and  probably  others,  including  diatoms  and  desmids, 
often  seen.  There  is  at  present  no  evidence  of  obligate  relations; 
these  forms  seem  to  be  caught  probably  accidentally,  and  can  live 
inside  the  trap  indefinitely,  though  Hegner  states  that  when  plants 
are  kept  a  long  time  in  an  aquarium,  the  Euglena  runs  out.  Protozoa 
when  captured  generally  succumb,  but  some  remain  alive  for  a  long 
time,  a  fact  noted  long  ago.  The  presence  of  decaying  Paramaecia  in 
the  trap  does  not  affect  the  Euglenae. 

That  Paramaecium  is  sometimes  quickly  killed  and  at  others  re- 
mains alive  for  a  long  time  (75  min.  to  17  days)  (Hegner)  seems  to 
indicate  that  the  physiological  conditions  in  the  traps  are  not  always 
uniform.  Luetzglburg  thought  he  detected  a  paralysing  effect  of 
the  extract  which  he  used  for  digestion  experiments  on  small  crusta- 
ceans,  but   that   it   must   be   weak.     Hada   advanced   the   idea   that 


Francis  E.  Lloyd 


—  266  — 


Carnivorous  Plants 


animals  are  killed  by  being  compressed  by  the  walls  in  becoming 
convex.  This  can  hardly  be  the  case  as  animals  have  been  seen  to  Hve, 
meanwhile  freely  moving,  for  days. 

Appendix:  — 

Here  in  a  position  of  obscurity  I  ask  leave  to  present  two  models, 
in  the  form  of  mouse  traps,  designed  ad  hoc,  to  illustrate  the  way  in 
which  the  trap  of  Ultricularia  has  been  and  at  present  is  thought  to 
work. 

Two  models  are  offered.  One,  Fig.  id,  represents  the  mechanism  of 
the  trap  as  conceived  by  Cohn,  Darwin  and  others.  In  this  the  door 
is  a  passive  check  valve,  easily  pushed  inwards,  but  not  outwards. 
In  the  model  a  small  hole  in  the  bottom  of  the  door  allows  the  mouse 
to  see  the  bait  thus  enhancing  the  effect  of  the  lure  by  adding  sight 
to  smell.  This  model  is  an  improvement  on  the  Utricularia  trap  in 
having  the  bait  on  the  inside.  Its  extreme  simplicity  is  in  contrast  to 
that  of  the  second  model,  Fig.  ii,  which  affords  an  analog  in  which  the 


Fig.  io.  —  A  mouse  trap  designed  to  embody  the  idea  held  by  Cohn  and  by  Darwin 
and  others  for  fifteen  years  after  them. 

complexity  of  the  Utricularia  trap  as  now  understood  is  suggested  with- 
out exaggeration. 

A  description  of  this  model  is  presently  given.  A  box  is  provided 
with  a  door  having  two  hinges  (hi,  h2).  Below  h2  the  part  d2  swings 
independently  from  that  above,  di.  Pressure  applied  at  the  arrow  pr 
cannot  push  in  the  door;  but  rotation  of  d2  on  h2,  so  that  its  edge 
clears  the  stop  {sp),  allowing  inward  swing.  Outward  swing  is  pre- 
vented by  a  backstay  st4.  A  handle  tr  on  d2,  actuated  by  a  mouse, 
accomplishes  inward  opening  by  pulling  on  the  string  sts,  whereby  the 
doodad  {d)  is  pulled  away  from  the  top  of  the  plunger  pi,  allowing  play 
to  the  spring  ^2.  This  spring  then  pulls  on  the  string  sh  actuating  the 
double  pulley  p  'X  2,  one  element  smaller  than  the  other  in  the  ratio  M. 
The  outer  pulley  pulls  on  sh,  swiftly  opening  the  door.  To  this  is 
attached  a  device  called  a  booster,  B,  the  purpose  of  which,  hke  the 
sudden  inward  gush  of  water  in  nature,  ensures  the  entrance  of  the 
mouse  into  the  trap.  This  is  now  momentarily  open,  and  of  course 
would  remain  so  unless  power  were  available  to  close  it  again.  This  is 
supplied  by  an  electric  motor  m  which  starts  to  rotate  when  an  electri- 
cal circuit  is  closed  by  a  contact  point  on  the  plunger  coming  into 
contact  with  e.  The  motor  continues  to  rotate  till  the  plunger,  push- 
ing the  spring  ^2  into  its  set  posture,  the  door  being  pushed  back  into 
position  by  its  spring  Si.     When  this  is  completed,  the  contact  point 


Chapter  XIV 


267  — 


The  Utricularia  Trap 


on  the  plunger  comes  into  contact  with  the  contact  point  e,  below, 
and  the  relay  r  then  stops  the  motor.  The  power  from  the  motor 
is  applied  to  the  plunger  through  the  gear  p2  etc.,  ending  in  a  cani  c, 
the  whole  being  adjusted  so  that  the  cam  comes  into  a  position  which 
allows  the  lever  /  to  swing  downwards  when  the  door  is  actuated 
again  by,  it  is  confidently  hoped,  a  second  mouse.  In  the  meantime, 
the  mouse  first  caught  can  employ  his  time  admiring  the  interior 
effect,  and  possibly  suggest  improvements.  A  digestion  chamber  could 
of  course  be  provided. 


Fig.  II.  — a  mouse  trap  intended  as  a  model  embodying  present  ideas  of  the  Utric- 
ularia trap  as  a  mechanism  (with  apologies  to  Heath  Robinson). 

A  captious  reader  may  find  difficulty  in  accepting  the  analogy  as 
complete.  I  can  say  only  that  he  would  be  right;  but  at  least  a  pur- 
pose is  served,  to  indicate  that  the  Utricularia  is  a  pretty  complex  bit 
of  mechanism. 

Literature  Cited: 
Adowa,  a.  N.,  Zur  Frage  nach  den  Fermenten  von  Utricularia  vulgaris  L.,  I.   Bioch.  Z. 

150:101-107,    1924;     II.     153:506-509,    1924.  XT    ^^     TJ    .     /-      ^     A 

Barnhart,  J.  H.,  Segregation  of  genera  m  Lenhbulariaceae.    Mem.  N.  Y.  Bot.  Lrard.  6:39- 

Bath,  \v.,  liber  Kaulquappen  in  den  Fangblasen  von  U.  vulgaris.      Sitzungsber.  d.  Ges. 

Naturforsch.  Freunde  Berlin  1905:153-155-  „  .  . 

Benjamin,  L.,  Uber  den  Bau  und  die  Physiologie  der  Utriculanen.    Botan.  Zeitung  6:1-5; 

17-23;    45-50;    57-61;    81-86,  1848. 
Brocher,  Frank,  Le  probleme  de  I'Utriculaire.     Ann.  de  Biol,  lacustre  5:33-46,  19"- 
Brocher,  F.,  a  propos  de  la  capture  d'anopheles  par  les  Utriculaires.     Ann.  Parasitol.  5: 

Brumpt,  E.,  Capture  des  larves  de  Culicidees  par  les  plantes  du  genre  Utricularia.    Ann.  de 

Parasit.  humaine  et  compar.  3:403-411,  1925- 
Buchenau,  Franz,  Morphologische  Studien  an  deutschen  Lentibularieen.     Botan.  Zeitung 

23:61-66;. .69-71;      77-80;      85-91;     93-99.    1865.  ^    .     rr.    ■      ,       ■  1         •       T        13 

BtJSGEN,  M.,  Uber  die  Art  und  Bedeutung  des  Tierfangs  bei   Utricularia  vulgaris  L.   Ber. 

d.  deutsch.  bot.  Gesellsch.  6:55-63,  1888. 
Candolle,  a.  p.  DE,  Physiologie  vegetale  11:528,  1832. 

Chandler,  Bertha,  Utricularia  emarginata  Benj.  Ann.  Bot.  24:549-555,  19 10. 
Clarke,  W.  G.  and  R.  Gurney,  Notes  on  the  genus  Utricularia  and  its  distribution  in 

Norfolk.     Trans.  Norfolk  and  Norwich  Nat.  Soc.  11:128-161,  1920-1921. 
Cohn,  Ferd.,  tJber  die  Funktion  der  Blasen  von  Aldrovanda  und  Utricularia.     Cohns  Bei- 

trage  zur  Biologie  der  Pllanzen  i(3):7i-92,  1875. 
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Phytologist  8:117-130,   1909.  . 

Crouan   Freres,   Observations  sur   un   mode  particulier  de  propagation   des   Utricularia. 

Bull,  de  la  Soc.  bot.  de  France  5:27-29,  1858. 
Curry,   Dalferes   P.,   Breeding   of   Anopheles   mosquitoes  among  aquatic  vegetation   of 

Gatun  Lake,  accompanied  by  periodic  long  flights  of  A.  albimanus  Wied.  Southern 

Med.  Journ.  27:644-651,  1934.  _    .  ,,      ^  r,        j    j     .    u 

Czaja,  a.  Th.,  Ein  allseitig  geschlossenes,  selektivpermeables  System.     Ber.  d.  deutscn. 

bot.  Gesellsch.  40:381-385,  1923. 


Francis  E.  Lloyd  —  268— Carnivorous  Plants 

CzAjA,  A.  Th.,  Die  Fangvorrichtung  der  Utriculanah\a.se.     Zeitschr.  f.  Bot.   14:705-729, 

IQ22. 

CzAjA,  A.  Th.,  Physikalisch-chemische  Eigenschaften  der  Membran  der  Utriculariah\a.se. 

Pfiugers  Arch.  f.  d.  Ges.  Physiol.  206:554-613,  1924. 
Darwin,  Charles,  Insectivorous  Plants.    New  York  1875. 
Dean,  B.,  Report  on  the  supposed  fish-eating  plant.     Commissioners  of  Fisheries  of  the 

State' of  New  York,  Report  18:183-197,  1890. 
Drude,  O.,  Die  insektenfressenden  Pflanzen.     Schenk's  Handbuch  der  Botanik  1:113-146 

{Utricidaria,  pp.   133-135),  Breslau  1881. 
Ekambaram,  T.,  Irritability  of  the  bladders  in  Utrictilarm.    Agric.  Journ.  India  11:72-79, 

Ekambaram,  T.,  Uiriadaria  flexuosa  Vahl.  Bot.  Bull,  of  the  Presidency  College  Madras, 
Sept.,  1918:1-21. 

Ekambaram,  T.,  A  note  on  the  mechanism  of  the  bladders  of  Utricularta.  Journ.  Indian 
Bot.  Soc.  4:73-74,   1926. 

Fermi,  C.  &  Buscaglione,  Die  proteolytischen  Enz3Tne  im  Pfianzenreiche.  Lentralbl.  t. 
Bakt.,  Parasit.  u.  Pfianzenkr.     II,  5:24-33;    63-66;    91-9S;    125-134;    145-158,  1899. 

Fernald,  M.  L.,  Expedition  to  Nova  Scotia.     Rhodora  23:89-111,  1921. 

Fernald,  M.  L.,  Specific  segregations  and  identities  in  some  floras  of  eastern  North  Amer- 
ica.    Rhodora  33:25-63,  i93i-  .  xt     77.  •    7     ■         7      •        u  1     c 

FRANfA,   C,   Recherches  sur  les  plantes  carnivores,   II.    Utricidana  vulgaris.     Bol.   boo. 

Brot.  I,  ser.  2:11-37,  1922. 
Gardner,  G.,  Travels  in  the  interior  of  Brazil  1836-1841.     London  1846. 
Gates,  F.  C,  Heat  and  the  flowering  of   Utricularta  resupinata.     Ecology   io(3):353-354, 

1929. 
Geddes,  Patrick,  Chapters  in  Modern  Botany.     New  York  1893. 
GiBBS,  R.  D.,  The  trap  of  Utricidaria.    Torreya  29:85-94,  1929. 
Gislen,  T.,   Beitrage  zur  Anatomic  der   Gattung   Utricularia.     Arkiv  for  Bot.    15:1-17, 

GLtJCK,  H.,  Biologische  und  morphologische  Untersuchungen  uber  Wasser-  und  Sumpfge- 
wachse.     Jena  1906.  ,     tt     j 

Goebel,  K.,  Vergleichende  Entwicklungsgeschichte  der  Pflanzenorgane.  Schenk  s  Hand- 
buch der  Botanik  111:99-431,  1884.     (re  Utricularia  etc.,  pp.  236-241.) 

Goebel,  K.,  IJber  die  Jugendzustande  der  Pflanzen.     Flora  72:1-45,  1889. 

Goebel,  K.,  Der  Aufbau  von  Utricularia.     Flora  72:291-297,  1889. 

Goebel,  K.,  Morphologische  und  biologische  Studien,  V.  Utricularia.  Ann.  Jard.  Bot. 
Buit.  9:41-119,   1891. 

Goebel,  K.,  Pflanzenbiologische  Schilderungen,  II.     Marburg  1891. 

GuRNEY,  Robert,  Utricularia  in  Norfolk:  the  effects  of  drought  and  temperature.  Trans. 
Norfolk  and  Norwich  Nat.  Soc.  11:260-266,  1921/22. 

Hada,  Y.,  The  feeding  habits  of  Utricularia  (with  English  abstract).    Trans.  Sapporo  Nat. 

Hist.  Soc.  11:175-183,  1930.  r    TT,  ■    1     ■        Tj-  1 

Hegner,   R.   W.,  The  interrelations  of  protozoa  and  the  utricles  of    UtriaUaria.     tJiol. 

Bull.  50:239-270,  1926.  . 

HoEHNE,  F.  C,  &  KuHLMANN,  J.  G.,  Utricularias  do  Rio  de  Janeiro  e  seus  arredores.    Mem. 

Inst.  Butantan  1:1-26,  1918.  ,       -r.-         ■     .        ou- 

HovELACQUE,  MAURICE,  Rechcrches  sur  I'appareil  vegetative  des  Bignomacees,  Rmnan- 
thacees,  Orobanchees  et  Utriculariees.  765  pp..  Lib.  Acad.  Med.  Pans,  1888  {Utricu- 
laria,   pp.    635-745).  T         ^  QQ 

Im  Thurn,  E.  F.,  Among  the  Indians  of  Guyana.    London  1883.  _         ,     00        t- 

Im  Thurn,  E.  F.  &  D.  Oliver,  The  botany  of  the  Roraima  Expedition  of  1884.  irans. 
Linn.  Soc.  Lond.  ser.  II,  2  (bot.),  1881-1888;    Part  13:249-300,  1887. 

Irmisch,  Thilo,  Botanische  Mitteilung,  I.   tjber  Utricularia  minor.    Flora  41:33-37,  1858. 

Jane,  F.  W.  &  Wells,  B.  R.,  Observations  on  the  seeds  and  seedhngs  of  Utricidaria  vul- 
garis L.  Trans.  Norfolk  and  Norwich  Naturalists  Soc.  14:31-54,  1935. 

Kamienski,  Fr.,  Vergleichende  Untersuchungen  uber  die  Entwicklungsgeschichte  der  Utri- 
cularien.     Botan.  Zeitung  35:761-775,  1877.  ^,         ,       o  o 

Kamienski,  Fr.,  Lentihulariaceae.     Naturliche  Pflanzenfamilien  4,  Abt.  36:108-123,  i»95. 

KiESEL,  A.,  Etudes  sur  la  nutrition  de  VUtricidaria  vulgaris.     Ann.  Inst.  Pasteur  38:879- 

Kruck,'m.,  p'hysiologische  und  zytologische  Studien  uber  die  Utriculariah\a.se.    Bot.  Arch. 

33:257-309,  1931- 

Lang,  F.  X.,  Untersuchungen  liber  Morphologic,  Anatomic  und  Samenentwicklung  von 
Pohpompholvx  and  Byblis.     Flora  88:149-206,  1901. 

Lloyd,  F.  E.,  The  mechanism  of  the  watertight  door  of  the  Utricularia  trap.  Plant  Phys- 
iol.   4:87-102,     1929.  ....  r    TT,     ■       J        • 

Lloyd,  F.  E.,  The  range  of  structural  and  functional  variation  in  the  traps  of  Utricularia. 

Flora  125:260-276,  1931.  .       ,  c   TT,  ■     1     ■ 

Lloyd,  F.  E.,  The  range  of  structural  and  functional  variety  in  the  traps  of  Utricularta 
and  Polypompholyx.     Flora  126:303-328,   1932a. 


Chapter  XIV 


269  —  The  Utricularia  Trap 


Lloyd,  F.  E.,  Is  the  door  of  Utriadaria  an  irritable  mechanism?     Canadian  Journ.  Res. 

7:386-425,     19326.  /-.  J-  T  TJ 

Lloyd,  F.  E.,  The  structure  and  behaviour  of  Utricularia  purpurea.    Canadian  Journ.  Kes. 

8:234-252,  1933a.  _,      .,      •  I    »  jj 

Lloyd,  F.  E.,  Carnivorous  plants  —  a  review  with  contributions.     Presidential  Address, 

Trans.  Roy.  Soc.  of  Canada,  Ser.  Ill,  27:35-101,  1933^-  ....,•/•,  j- 

Lloyd    F.  E.,  The  types  of  entrance  mechanisms  of  the  traps  of  Utricularia  (including 

Poly  pom  pholyx).      Presidential    Address,    Section    K-Botany,    B.  A.  A.  S.,    Leicester, 

Sept.  1933c,  pp.  183-218.  /-       J-        T  1? 

Lloyd,   F.   E.,  Additional  observations  on  some   Utricidariaceae.     Canadian  Journ.   Kes. 

10:557-562,  1934-  ^.  ,    ^     . 

Lloyd,  F.  E.,  Utricularia.    Biol.  Reviews  10:72-110,  1935a-  .   ^,    .     ,     .        „  ., 

Lloyd,  F.  E.,  Struktur  und  Funktion  des  Eintrittsmechanismus  bei  UlnciUaria.     Beih.  z. 

Bot.  Centralbl.  A,  54:292-320,  19356.  c     f  . 

Lloyd,  F.  E.,  The  traps  of  Utricidaria.    Proc.  Sixth  Intern.  Botan.  Congress,  Sept.   1935, 

Lloyd,  F.  e'.,  The  trap  of  Utricularia  capensis,  how  it  works.    Journ.  S.  Afr.  Bot.,  2:75-94, 

Lloyd,^F.  E.,  Notes  on  Utricularia,  with  special  reference  to  Australia,  mth  descriptions  of 

four  new  species.    Victorian  Naturalist  53:91-112,  1936c.  _  _ 

Lloyd,  F.  E.,  Further  notes  on  Australian  Utricularia  with  a  correction.     Victonan  JNat- 

uralist  53:  163-166,  1937a-  ^  ,  ,      ^  c     at      u^f       ...r- 

Lloyd,  F.  E.,  Utricularia:    its  development  from  the  seed.     Journ.    b.  Air.    Hot.   3.155- 

164,   19376.  .        „, 

Lxjetzelburg,  p.  v.,  Beitrage  zur  Kenntnis  der  Utricularia.     flora  100:145-212    1910. 
Matheson,  Robert,  The  utihzation  of  aquatic  plants  as  aids  in  mosquito  control.    Amer. 

Nat.  64:56-86,  1930.  ., 

Mayr,  F.  X.,  Hydropoten  an  Wasser-  und  Sumpfpflanzen.  Diss.  Erlangen,  1914-     Bein. 

Bot.  Centralbl.  I,  32:278-371,  1915-  .         ,  ^       .  ,    ,  u-  u.    j 

Meierhofer,  Hans,  Beitrage  zur  Kenntnis  der  Anatomic  und  Entwickelungsgeschichte  der 

Utricularia-BlsLsen.    Flora  90:84-113,  1902. 
Merl,  E.  M.,  Beitrage  zur  Kenntnis  der  Utricularien  und  Genliseen.     flora  108:127-200, 

1915. 
Merl,  E.  M.,  Biologische  Studien  iiber  die  Utricidariahl^ise.    Flora  115:59-74.  1922. 
Merl,   E.   M.,   Beitrage  zur  Kenntnis  der  brasilianischen   Utricularien.     Flora   118-119: 

Merl,  E.  M.,  A  new  Brazilian  species  of  the  genus  Utricularia.     Bull.  Torr.  Bot.  Club 

Merz,  M.,  Untersuchungen  iiber  die  Samenentwickelung  der  Utricularien.    Flora  84:69-87, 

1897. 
Meyen,  F.  J.  F.,  Neues  System  der  Pflanzenphysiologie.     Berlin  1837. 
Meyer,  F.  J.,  Zur  Frage  der  Funktion  der  Hydropoten.    Ber.  d.  D.  Bot.  Gesellsch.  53:542- 

Morren,  Ed.,  La  theorie  des  plantes  carnivores  et  irritables.     Bull,  de  TAcad.  Roy.  Belg. 

II,  60:1-60  (repaged?),  1875. 
MosELY,  H.  N.,  Bull.  U.  S.  Fish  Commission  4:259,  1884/5. 
NoLD,  R.  H.,  Die  Funktion  der  Blase  von  Utricularia  vulgaris  (Ein  Beitrag  zur  Llektro- 

p'hysiologie  der  Drusenfunktion).     Beihefte  Bot.  Centralb.  52:415-448,  i934- 
Oliver,  Daniel,  The  Indian  species  of  Utricularia.    Journ.  Linnean  Soc,  Bot.,  3:169-176, 

Oppenheimer,  C,  Die  Fermente  und  ihre  Wirkungen.     5.  Aufl.,  2:1106-1108,  1925- 
PORSILD,  M.  P.,  Stray  contributions  to  the  flora  of  Greenland,  VI-XII.    Medd.  om  Gr0n- 
land,  Komm.  f.  Videnskab.  Unders^g.  i  Gr^nland  93:i-94,  i93S  {Ulriadana,  pp.  25- 

34)- 
Prat,  S.,  Plasmolyse  und  Permeabilitat.  Ber.  d.  D.  Bot.  Gesellsch.  41:225-227,  1923.    _ 
Pringsheim,  N.,  Uber  die  Bildungsvorgange  am  Vegetationskegel  von  Utricularia  vulgaris. 

Monatsbericht  k.  Akad.  d.  Wiss.  1869:92-116.  ^ 

Ridley,  H.  N.,  On  the  foliar  organs  of  a  new  species  of  Utricularia  from  St.  Thomas, 

West  Africa.     Ann.  Bot.  2:305-308,  1888. 
RossBACH,  G.  B.,  Aquatic  Utricularias.     Rhodora  41:113-128,  1939. 
St.  Hilaire,  A.  de.  Voyages  dans  les  provinces  du  Rio  de  Janeiro  et  du  Minas  Geraes. 

Paris  1830.  ,    .      r       •  u 

SCHENCK,  H.,  Beitrage  zur  Kenntnis  der  Utricularien.     Pnngsheim  s  Jahrb.  f.  wissensch. 

Bot.  18:218-235,  1887. 
ScHiMPER,  A.  F.  W.,  Notizen  uber  insectenfressenden  Pflanzen.     Botan.  Zeitung  40:225- 

234;  241-248,  1882. 
Schwartz,  O.,  Plantae  novae  vel  minus  cognitae  Australiae  tropicae,  Rep.  spec.  nov.  reg. 

veg.  24:80-109,  1927.  ^^; 

SIMMS,  G.  E.  Bull.  U.  S.  Fish  Commission  4:257,  1884/5.  ,     ,  ,<  \ 

SIMMS,  G.  E.  &  H.  N.  MosELY,  Naturforscher  17:276,   1884.    Ref.  in  Centralbl.  f.   Agn- 

culturchemie  14:69,  1885. 


Francis  E.  Lloyd                          —  270  —                      Carnivorous  Plants  ! 

Skutch,  a.  F.,  The  capture  of  prey  by  the  bladderwort,  A  review  of  the  physiology  of  the  ) 

bladders.     New  Phytologist  27:261-297,  1928.   _  i 
Stapf,  O.,  Lentibulariaceae,  in  Flora  of  Tropical  Africa.    London,  1906. 

Staff,  O.,  Lentibulariaceae  (of  Borneo).    Journ.  Linn.  Soc,  Bot.,  42:115,  1914.  ' 

Stephens,  Edith  L.,  Carnivorous  plants  of  the  Cape  Peninsula.     Journ.  Bot.  Soc.  South  j 

'Africa,  Part  IX:2o-24,  1923.  I 

Stutzer,  M.  J.,  Zur  Biologic  der  Utricularia  vulgaris.    Arch.  Hydrobiol.  i7  730~735>  1926.  j 

Thompson,  G.  M.,  On  the  fertilization  of  flowering  plants  (Lentibulariaceae) .    Trans,  and  : 

Proc.  N.  Zealand  Inst.  13:278-281,  1881.                                     _  1 

Tieghem,  Ph.  van,  Anatomic  dc  I'utriculaire  commune.    Ann.  Sci.  Nat.  Bot.  V,  10:54-58,  j 

1869;    C.  R.  Acad.  Sci.  Paris  67:1063-1066,  1868.  I 

Topp,  C.  A.,  Notes  on  the  genus  Utricularia.    Victorian  Naturalist  1:71-74,  1884.  ; 

Topp,  C.  A.,  Note  on  Utricularia  dichotoma.     Victorian  Naturalist  3:74-75.  1886.  ; 

Treat,  Mary,  Plants  that  eat  animals.     N.  Y.  Daily  Tribune,  i  Feb.  1875.     Reprinted  ' 

without  illustrations  in  Gardeners'  Chronicle,  March  6,  1875:  303-304.  , 
Treat,  Mary,  Is  the  valve  of  Utricularia  sensitive?    Harper's  New  Monthly  Mag.  52:382- 

387,  1876. 
Treviranus,  C.  L.,  Noch  etwas  iiber  die  Schlauche  der  Utricularien.    Bot.  Zeit.  6:444-448, 

1848.  ; 

Ule,  E.,  liber  Standortsanpassungen  emiger  Utricularien  in  BraziUen.     Ber.  deutsch.  bot.  ' 

Ges.  16:308-314,  1898. 

Uphof,  J.  C.  Th.,  Einiges  zur  Biologic  der  terrestrischen  Utricularien.    Oest.  bot.  Zeit.  82:  j 

207-212,  1933.  I 

Warming,   E.,   Bidrag  til  Kundskaben  om  Lentibulariaceae.     Vidensk.   Medd.   nat.   For.  | 

Copenhagen,  Nos.  3-7:33-58,  1874.                                                                  ,   ^    .  j  ,  ; 
Wehrle,  Emil,  Studien  iiber  Wasserstoflionenkonzentrationsverhaltmsse  und  Besiedelung 

an  Algenstandorten  in  der  Umgebung  von   Freiburg  im   Breisgau.  Zeitschr.   f.   Bot. 

19:    209-287,  1927.  I 
Withycombe,  C.  L.,  Observations  on  the  bladderwort.     Knowledge  39:238-241,  1916.  _ 

Withycombe,  C.  L.,  On  the  function  of  the  bladders  in  Utricularia  vulgaris.     Journ.  Lin  | 

nean  Soc,  Bot.,  46:401-413,  1922-1924.    Paper  published  in  1923.  ; 

Wylie,  R.  B.  &  YocoM,  A.  E.,  The  endosperm  of  Utricularia.    Univ.  of_Iowa_Studies  Nat.  ', 

Hist.  10:3-181,  My.,  1923. 


PLAT  E  S 


—  Plate  I.  — 

Fig.  I.  —  Heliamphora  nutans  (grown  at  the  Edinburgh  Botanical  Gar- 
den). 

Fig.  2.  —  H.  Macdonaldae  (Photograph  by  Dr.  G.  H.  H.  Tate  taken  on 
Mt.  Duida,  Venezuela). 

Fig.  3.  —  Sarracenia  purpurea  (Photograph  by  Charles  Macnamara, 
Ontario). 

Fig.  4.  —  S.  purpurea:   a  leaf  cut  lengthwise. 

Fig.  5.  —  S.  purpurea:   view  facing  the  opening. 

Fig.  6.  —  5.  Drummondii. 

Fig.  7.  —  5.  flava. 

Fig.  8.  —  S.  psittacina. 

Fig.  9.  —  S.  minor  (Photograph  by  Professor  J.  C.  Th.  Uphof). 


—  Plate  2.  -— 

Fig.  I.  —  Heliamphora  nutans.  Front  view,  spoon  enlarged  and  longitu- 
dinal view  of  pitcher  cut  near  the  sagittal  plane,  in  which  the  sections 
i""2,  3-4  and  5-6  are  indicated  by  corresponding  numbers. 

Fig.  2.  —  Juvenile  leaf  (after  Krafft  1896). 

Fig.  3.  —  Assimilating  leaf  (after  Krafft  1896). 

Fig.  4.  —  Abnormal  juvenile  leaf  (after  Goebel  1891). 

Fig.  5.  —  Hair  from  zone  2,  fig.  i,  above.  Below,  detentive  hair  from  zone 
A- 

Fig.  6.  —  V-shaped  twin  hairs,  from  outer  surface  of  pitcher. 

Fig.  7.  —  Nectar  gland  from  spoon,  in  longitudinal  section. 

Fig.  8.  —  Nectar  gland  from  outer  surface  of  pitcher. 

Fig.  9.  —  Surface  view  of  same. 

Fig.  10.  —  Nectar  gland  from  inner  surface  of  pitcher. 

Fig.  II.  —  Transverse  section  of  spoon  indicating  size  and  distribution  of 
nectar  glands. 

Fig.  12.  —  Sarracenia  purpurea.  Upper  two-thirds  of  pitcher,  seen  whole; 
view  of  interior  of  an  entire  pitcher:  the  zones  are  indicated  by  num- 
bers; front  view  of  bell;  petiole  in  longitudinal  section  of  a  pitcher  in 
which  this  was  abnormally  long. 

Fig.  13.  —  Juvenile  leaf,  shown  in  the  same  way  as  the  pitcher  in  fig.  12. 

Fig.  14.  —  Surface  and  longitudinal  views  of  the  tesselated  cells  of  zone  2. 

Fig.  15.  —  Surface  view  of  a  nectar  gland  from  outer  surface  of  pitcher. 

Fig.   16.  —  Longitudinal  section  of  same. 


—  Plate  J.  — 

Figs,  i  and  2.  —  Sarracenia  purpurea. 

Figs.   3-6.  -^  S.  psiltacina. 

Figs.  7-12.  —  S.  minor. 

Figs.  13-18.  —  S.  Jonesii. 

Fig.  I.  —  Nectar  gland  from  surface  of  the  nectar  roll. 

Fig.  2.  —  Hair  from  outer  surface  of  pitcher. 

Fig.  3.  —  Nectar  gland  from  interior  surface  of  the  pitcher. 

Fig.  4.  —  Pitcher,  cut  lengthwise  to  show  interior  surface;   a-h,  transverse 

section  of  nectar  ridge,  its  position  indicated  in  the  larger  figure. 
Fig.  5.  —  Juvenile  leaf  (after  Goebel  1891). 

Fig.  6.  —  View  looking  into  the  entrance  of  leaf,  such  as  in  fig.  4. 
Fig.  7.  —  Pitcher  of  S.  minor. 
Fig.   8.  —  Front  view  of  same.     Nectar  droplets  are  indicated,   as   also 

in  next  figure. 
jTjg   g  _  The  lateral  view  of  same,  with  section  of  the  nectar  roll  and  of 

the  wing  where  indicated. 
Fig.  10.  —  Surface  view  of  nectar  gland  with  a  few  adjacent  imbricated 

cells. 
Fig.  II.  —  Detentive  hair,  from  zone  4. 
Fig.  12.  —  Nectar  gland  surface  of  nectar  roll,  S.  minor. 
Figs.  13-18.  —  Developmental  series,  pitcher  of  S.  Jonesii. 
Fig.  13.  —  The  mouth  begins  to  be  seen. 
Fig.  14.  —  Lips  of  mouth  are  seen.     The  lateral  and  basal  views  of  this 

stage  are  seen  in  fig.  15. 
jTjc    i5  _  The  lower  edge  of  the  mouth  begins  to  extend,  as  the  apex 

elongates. 
Figs.  17  and  18.  —  The  lower  edge  of  the  mouth  has  been  extended  as  a 
ridge,  the  ala  ventralis. 


—  Plate  4.  — 

Fig.  I.  —  Darlingtonia  calif ornica,  as  seen  growing  25  miles  east  of  Cres- 
cent City,  Calif. 

Fig.  2.  —  The  same,  in  flower  in  early  spring  (Photograph  by  Dr.  Frank 
Morton  Jones,  taken  in  Plumas  Co.,  Calif.,  1920). 

Fig.  3.  —  The  same,  flowers  (near  Florence,  Oregon). 

Fig.  4.  —  The  same.    View  looking  up  into  the  dome  of  the  leaf. 

Fig.  5.  —  The  same.    A  leaf  split  lengthwise. 

Fig.  6.  —  Nepenthes  Mastersiana.    A  pitcher  split  lengthwise,  showing  the 
waxy  zone  above  and  the  glandular  zone  below. 

Fig.  7.  —  N.  ventricosa. 

Fig.  8.  —  N.  Balfouriana  (N.  mixta  x  Mastersiana). 

Fig.  9.  — •  N.  ampidlaria. 

Fig.  10.  —  N.  bicalcarata. 

Fig.  II.  —  N.  ampullar ia,  looking  into  a  pitcher. 


—  Plate  5.  — 

Figs.   i-io.  —  Darlingtonia  calif jniica. 

Figs.  1-3.  —  Various  juvenile  leaves. 

Fig.  4.  —  A  series  of  sections  through  a  juvenile  leaf  at  levels  indicated  in 
the  drawings  (in  mm.,  the  7  mm.  section  being  proximal). 

Fig.  5.  —  Sections  through  the  wings  of  a  mature  pitcher  at  various  levels 
(indicated  in  mim.);  at  10  n  m.  the  edges  of  the  basal  wings  are  evi- 
dent, at  65  n  m.  the  edges  of  the  mouth. 

Fig.  6.  —  Juvenile  leaf  which  had  failed  to  become  ascidiate,  except 
slightly  in  the  petiolar  region. 

Fig.  7.  —  Interior  view  of  the  lower  half  of  a  large  mature  pitcher  dome; 
ii,  T2,  veins  of  the  tube  which  fuse  to  enter  the  fishtail. 

Fig.  8.  —  Lateral  view  of  the  interior  of  the  dome.  The  hairs  and  fenes- 
trations are  only  partially  indicated. 

Fig.  g.  —  Interior  of  dome  looking  forward  (distally),  showing  the  articu- 
lation of  the  nectar  roll  with  the  edges  of  the  fishtail. 

Fig.  10.  —  Interior  view  of  dome  looking  backward,  showing  relation  of 
the  ala  vzntralis  with  the  nectar  roll. 

Fig.  II. — Sarracenia  psittacina.  —  A  young  leaf  showing  the  early  stage 
of  the  infold  to  form  the  entrance  tube. 


( 


J' 


—  Plate  6.  — 

Figs.    1-23.  —  Darlingtonia   calijornica. 

Figs.  i-io.  —  Various  stages  of  the  development  of  the  leaf  showing  espe- 
cially the  development  of  the  da  ventralis  as  part  of  the  lateral  lips  of 
the  mouth  and  quite  apart  from  the  stipular  wings. 

Figs.  4-6  and  10  show  the  development  of  the  fishtail. 

Fig.  9.  —  Longitudinal  interior  view  of  a  leaf  of  the  dimensions  of  fig.  8; 
nr,  nectar  roll;  tnr,  marginal  roll  of  the  fishtail;  /,  upward  fold  of  the 
wall  of  the  dome. 

Fig.  II.  —  Diagrams  idealizing  the  development  of  the  nectar  roll  and  its 
continuation  to  form  the  marginal  roll  of  the  fishtail;  a,  a  theoretical 
condition  corresponding  to  the  condition  actually  recorded  in  plate 
5-y,  b,  a  theoretical  condition  further  advanced  than  a,  in  which  the 
'fold'  {see  fig.  9)  has  not  fused  and  the  edge  of  the  nectar  roll  is  still 
evidently  confluent  with  the  edge  of  the  marginal  roll  of  the  fishtail. 

Figs.  12  and  13.  —  Supposed  appearance  of  pitchers  on  the  conditions  in- 
dicated theoretically  in  figs,   iia  and  b. 

Fig.  14.  —  A  mature  pitcher  on  a  small  plant  (the  figure  is  larger  than 
natural  size)  showing  the  posture  taken  in  relation  to  the  soil  surface, 
in  which  the  fishtail  serves  as  a  ramp  leading  to  the  entrance  of  the 
dome. 

Fig.  15.  —  Appearance  of  mature  pitchers  of  upright  posture,  front  and 
side  view. 

Fig.  16.  —  External  view  of  the  dome  of  a  young  pitcher  somewhat  ad- 
vanced beyond  that  of  fig.  10.     (Goebel  published  a  similar  figure). 

Fig.  17.  —  Seedling,  with  juvenile  leaves  only  and,  as  it  happens,  with 
three  cotyledons. 

Fig.  18.  —  Surface  view  of  nectar  gland  in  a  juvenile  leaf. 

Fig.  19.  —  Surface  view  of  a  nectar  gland  such  as  seen  in  fig.  23. 

Fig.  20.  —  Nectar  gland  from  outer  surface  of  pitcher. 

Fig.  21.  —  Nectar  gland  from  inner  surface. 

Fig.  22.  —  Surface  view  of  same. 

Fig.  23.  —  Lateral  sectional  view  of  nectar  gland  with  at  least  two  tiers  of 
cells. 


—  Plate  7.  — 

Figs.  1-25.  —  Nepenthes. 

Figs.  1-6.  —  Developmental  series  of  the  pitcher  leaf. 

Fig.  I.  —  Very  young  stage  (after  Hooker  1859). 

Fig.  2.  —  Somewhat  later  stage,  the  lid  having  appeared  (after  Hooker). 

Fig.  3.  —  Longitudinal  section  of  a  still  later  stage  showing  lid  appressed 
to  the  rim  (after  Hooker). 

Fig.  4.  —  The  origin  of  the  lip  as  a  two  lobed  structure  (after  Bower). 

Fig.  5.  —  Definitive  form  of  the  first  seedling  leaf  (after  Stern).  The 
transverse  stipular  juncture  is  represented  by  emergencies. 

Fig.  6.  —  A  similar  stage  of  development  (after  Macfarlane),  in  which 
the  transverse  stipular  membrane  is  evident. 

Fig.  7.  — •  Front  and  side  view  of  a  pitcher  produced  on  a  forced  sprout 
showing  venation  as  broken  lines.  The  small  number  and  the  dis- 
tribution of  digestive  glands  are  indicated. 

Figs.  8  and  9.  —  Lateral  and  front  view  of  a  pitcher  on  a  forced  shoot, 
showing  the  spur  is  a  flat  structure,  and  the  distribution  of  veins. 

Figs.  10-13.  —  Other  pitchers  produced  on  short  shoots  in  which  various 
relations  of  the  petiolar  '  blade '  to  the  wings  of  the  pitcher  are  noted. 

Fig.  14.  —  The  digestive  gland  in  N.  Pervillei,  covered  by  a  deep  pocket. 

Figs.  15-20.  —  Transverse  section  of  the  rim  of  several  species.  The  arm 
of  the  inner  ridge  bears  a  nectar  gland. 

Fig.  15.  —  N.  sp.  aff.  Balfouriana. 

Fig.   16.  —  N.  venlricosa. 

Fig.  17.  —  N.  gracilis. 

Fig.  18.  —  iV.  Lowii. 

Fig.  19.  —  N.  ampuUaria. 

Fig.  20. — -N.  inermis  Danser,  "peristome  almost  none".  A,  transverse 
section  through  peristome;   B,  looking  into  a  nectar  gland  pit. 

Fig.  21.  —  Front  and  side  view  of  the  nectar  gland  in  its  pit,  N.  ampul- 
lar ia. 

Fig.  22.  —  A^.  intermedia,  showing  the  two  strongly  developed  groups  of 
peristome  teeth  at  the  base  of  the  lid. 

Fig.  23.  —  N.  bicalcarata,  divided  lengthwise,  showing  therefore  only  one 
of  the  well  developed,  claw-like  projections  at  the  base  of  the  lid. 

Fig.  24.  —  Transverse  section  through  the  lid  and  mouth  of  a  very  young 
pitcher  of  N.  anipidlaria.  The  glandular  inner  limb  of  the  peristome  is 
seen  to  be  an  emergence  from  the  inner  surface  of  the  pitcher  wall. 

Fig.  25.  —  N.  Tiveyi.  Under  surface  of  the  lid,  bearing  a  prominent  me- 
dian ridge  with  prominent  processes. 


—  Plate  8.  — 

Figs.  1-20.  —  Nepenthes.  1 

Figs.  1-3.  —  Stellate  hairs,  sometimes  emergent,  sometimes  in  pits. 

Fig.  4.  —  Tufted  hair,  producing  the  rusty  pubescence  of  Nepenthes. 
There  are  several  varieties  of  form. 

Figs.  5  and  6.  —  Front  and  lateral  views  of  the  peculiar  stomata  on  the  ' 

waxy  zone  of  the  interior  of  the  pitcher.  ' 

Fig.  7.  —  Front  and  lateral  views  of  the  epidermis  clothing  the  peristome;  , 

a-b  and  c-d  correspond  in  position.    N.  ampuUaria  {of.  figs.  17  and 
18). 

Fig.  8.  —  Nectar  gland  from  inner  surface  of  the  lid. 

Figs.  9  and  10.  —  Digestive  glands  from  two  species,  in  section;  cut. 
suberized  course  of  cells. 

Fig.  II.  —  Front  view  of  a  digestive  gland,  standing  in  its  pocket.  , 

Fig.  12.  —  Epidermal  cells  of  the  peristome  of  N.  Lowii. 

Fig.  13.  —  Nectar  gland  of  the  peristome  edge,  N.  ampuUaria.  The 
outermost  course  of  cells  is  suberized. 

Fig.  14.  —  Digestive  gland  in  young,  thin-walled  condition  of  N.  ampul- 
lar ia. 

Fig.  15.  —  External  alluring  (nectar)  gland  from  the  midrib  of  the  blade. 
S,  suberized  layer. 

Fig.  16.  —  Nectar  gland  from  the  ridge  beneath  the  lid,  of  N.  Tiveyi.  S, 
suberized  course  of  cells. 

Fig.  17.  —  Transverse  section  of  epidermis  of  the  peristome  of  A'.  am- 
puUaria.    The  cells  appear  ridged. 

Fig.  18.  ^  The  ridges  are  seen  to  be  due  to  the  overlying  of  next  cells 
(see  also  fig.  7). 

Fig.  19.  —  Quite  young  stage  of  development  of  a  pitcher  and  lid  in  sec- 
tion, showing  folding  of  the  lid  and  origin  of  the  inner  peristome  ridge 
as  an  outgrowth  of  the  wall. 

Fig.  20.  —  Transverse  section  of  the  petiole  showing  it  to  be  bifacial. 


—  Plate  g.  — 

Figs.  i-6.  —  Cephalotus  follicular  is. 

Fig.  I.  — ^  A  clump  of  plants  photographed  at  Albany,  Western  Australia. 

Fig.  2.  —  A  plant,  grown  at  the  Edinburgh  Botanical  Garden. 

Fig.  3.  —  Pitcher  split  lengthwise. 

Fig.  4.  —  A  shadow  picture  of  a  glandular  patch. 

Fig.  5.  —  An  entire  plant  in  flower.  Inset:  flower  enlarged.  From  a 
large  clump  of  plants  sent  bj-  me  from  Austraha  to  the  Botanical  Insti- 
tute, Munich  (Photograph  by  Dr.  Th.  P.  Haas). 

Fig.  6.  —  View  looking  down  on  the  same  culture,  to  show  the  two  kinds 
of  leaves,  pitcher  and  photosynthetic,  the  latter  in  full  development; 
an  aberrant  one  may  be  seen  at  the  left  of  the  picture  (Photograph 
by  Dr.  Haas). 

Fig.  7.  —  Genlisea  re  pens  (from  Sao  Paulo,  Brazil). 

Fig.  8.  —  The  same.  Tubular  portion  of  the  trap  showing  the  lobster- 
pot  structure. 

Fig.  9.  —  Byhlis  gigantea  (Western  Australia).  Various  aspects  of  the 
leaf  to  show  the  distribution  of  glands.  The  sessile  glands  are  dis- 
cernible as  white  dots  on  the  leaf  surface. 


'f  ■■:■-■ -u*^ 


i-mm 


—  Plate  10.  — 

Figs.   1-24.  —  Cephalotus  Jollicularis. 

Figs,  i  and  2.  —  Lateral  and  front  views  of  a  mature,  full  sized  pitcher, 

4.5  cm.  long. 
Fig.  3.  —  View  of  interior  of  pitcher.     Distribution  of  veins  shown:   Vi,  Vi 

and  Vi,  one  of  each  of  the  median  and  following  lateral  veins  of  the  ven- 
tral group,  v;  di,  d-i,  veins  of  the  dorsal  group  {d),  the  former  a  single 

median  vein. 
Fig.  4.  —  Sections  through  the  base   (lowermost),   middle  and  top  of  a 

pitcher  stalk,  showing  distribution  of  veins:     v,  ventral;    i,  2  and  3, 

the  three  pairs  of  ventral  veins. 
Fig.   5.  —  Lateral   view   of   a   young  pitcher   3   mm.   long.     For  section 

through  a-b,  see  fig.  7. 
Fig.  6.  —  Interior  view  of  a  similar  pitcher,  showing  the  distribution  of 

veins  at  this  age.    These  can  be  identified  with  those  seen  in  fig.  3. 
Fig.  7.  —  Section  through  young  pitcher  through  a-b  of  fig.  5. 
Fig.  8.  —  Section  through  base  (lowermost),  middle  and  through  base  of 

blade  of  a  mature  foliage  leaf;    v,  ventral. 
Fig.  9.  —  Section  through  rim  of  a  juvenile  pitcher  (figs.  10-12)  showing 

tooth  and  distal  end  of  the  median  dorsal  vein. 
Figs.  10,  11.  —  Frontal  and  lateral  views  of  a  juvenile  pitcher  8  mm.  long. 
Fig.  12.  —  Interior  view  of  same,  showing  deep  collar  and  distribution  of 

veins.     Compare  with  fig.  3.    See  also  fig.  24. 
Figs.  13-18.  —  Various  intergradient  forms  of  leaves  between  the  foliage 

leaf  and  pitcher.    For  normal  foliage  leaf,  see  figs.  2  and  6,  plate  9. 
Fig.   19.  —  Diagram  of  section  of  a  medium  sized  digestive  gland  from 

glandular  patch. 
Fig.  20.  —  Diagram  of  section  of  a  small  digestive  gland  (above)  and  sur- 
face view  of  same  (below). 
Fig.  21.  —  Diagram  of  section  of  a  gland  from  external  surface  of  pitcher 

and  elsewhere. 
Fig.  22.  —  Surface  view  of  same. 

Fig.  23.  —  Two  stomata  from  surface  of  a  glandular  patch. 
Fig.  24.  —  Longitudinal  section  of  a  trap  1.25  mm.  long;   v,  ventral;    d, 

dorsal. 


—  Plate  II.  — 

Figs.  i-ii.  —  Genlisea. 

Figs.  1-4,  7,  8  and  10.  —  Series  showing  the  development  of  the  trap. 

Fig.  5.  —  A  single  plant  (from  Brazil)  X  2;  inf.,  inflorescence  stalk;  /., 
trap. 

Fig.  6.  —  Portion  of  an  arm  laid  open  of  G.  ornata.  In  this  species  the 
number  of  rows  of  detentive  hairs  is  small.  The  position  of  the 
glands  and  the  shape  of  the  inner  epidermal  cells  (on  a  larger  scale) 
are  indicated. 

Fig.  7.  ^ — ^  A  trap  in  which  the  arms  are  beginning  to  develop;  vent.,  ventral 
view;   lat.,  lateral  view. 

Fig.  8.  —  Distal  end  of  a  young  trap  showing  the  arms  in  a  stage  of 
growth  later  than  that  seen  in  fig.  4.  Dotted  hnes  indicate  veins,  as 
in  fig.  7. 

Fig.  9.  —  Mature  trap,  one  arm  having  been  laid  open  and  shown  in  its 
posture  thereafter.  A  portion  of  the  laid-open  arm  at  a  is  shown 
above  and  to  the  right;  below  this,  the  sections  along  a-b  and  c-d 
are  shown. 

Fig.  10.  —  A  mature  trap.  The  numbered  lines  indicate  the  positions  of 
the  sections  shown  in  plate  12. 

Fig.  II.  —  A  portion  of  the  oral  termination  of  the  tube,  with  the  ad- 
jacent portion  of  an  arm,  diagrammed  in  perspective.  Note  prey 
caught,  seen  through  the  window  cut  in  the  wall,  on  the  right. 


—  Plate  12.  — 

Figs.  i-i8.  —  Genlisea. 

Fig.  1.  — Transverse  section  through  the  mouth  of  a  twisted  arm,  being  I 

an  amplified  figure  of  part  of  fig.  4  {cf.  11  —  10,  at  j).  i 

Fig.  2.  —  Section  through  the  mouth  at  the  top  of  the  neck  {11  —  10  at  5) 

showing  the  rows  of  detentive  hairs. 
Fig.  3.  —  Section  through  the  mouth  at  the  top  of  the  neck  (//  —  10  at 

5)  showing  particularly  the  giant  articulating  hair  ("distance  piece"). 
Fig.  4.  —  Section  across  arm  (//  —  10  at  j).     The  obliquity  of  the  rows 

of  detentive  hairs  is  to  be  noted.  1 

Fig.  5.  —  Transverse  section  through  neck  {11  —  10   at   i),  at  the  level  j 

of  the  row  of  glands,  indicated  by  is,  fig.  9,  which  is  a  longitudinal  ^ 

section  in  the  same  region.  ! 

Fig.  6.  —  Transverse  section  through  neck  at  2  (11  — 10),  through  the  | 

basal  cells  of  the  detentive  hairs.  ' 

Fig.   7.  —  Transverse  section  through  a  ridge  in   the  belly  of  the  flask 

(7/  —  10  at  4). 
Fig.  8.  —  Longitudinal  section  with  perspective  at  2  (// —  10).     Inter- 
cellular spaces  are  hatched.  I 
Fig.  9.  —  Longitudinal  section  at  /   (//  —  10)  and  approximately  in  the 

plane  in  which  one  of  the  vascular  strands  lies.  ^  1 

Fig.  10.  —  Longitudinal  dorsi-ventral  section  showing  also  the  interior  of 

the  belly  of  the  flask. 
Fig.  II.  —  Mucilage  gland  from  external  surface  lies. 
Fig.  12.  —  Short  detentive  hair  from  edge  of  arm. 
Fig.  13.  —  Detentive  hair  from  interior  of  arm  or  neck. 
Fig.  14.  —  Glandular  hairs  (presumably  digestive)  from  belly  of  flask. 
Fig.  15.  —  Articulating  hair  ("distance  piece")  from  edge  of  arm. 
Fig.  16.  —  Glandular  hair  from  interior  of  upper  part  of  neck  and  of  the 

arms. 
Fig.  17.  —  Digestive  hairs  with  four  celled  capital.     Otherwise  as  in  fig. 

14- 
Fig.  18.  —  View  of  the  depression  into  which  the  large  giant  cell  of  a  dis- 
tance piece  fits. 


I 

i 

—  Plate  I  J.  — 

Fig.   I.  —  Byblis  gigantea  (W.  Australia).   Inset:    commensal  (true)  bug, 

as  yet  undescribed. 
Fig.  2.  —  Drosophyllum  lusitanicum,  in  culture  (Munich).     Right,  a  piece 

of  a  leaf  with  captured  prey. 
Fig.  3.  —  The  same  (Photograph  by  Dr.  A.  Quint.^nilha). 
Fig.  4.  —  Pinguicida  vulgaris  (Alberta,  Canada).  X '2. 
Fig.  5.  —  At  left  of  numeral,  a  piece  of  a  leaf  of  Byblis;   at  right  of  nu-  j 

meral  a  part  of  a  leaf  of  Drosera  capensis.  ! 

Fig.   6.  —  Pinguicida  vulgaris.     Two  views  of  the  same  plant  taken   24 

hours  apart   to   show   leaf  movements.      Collected     20    mi.    east    of  j 

Crescent  City,  Calif.  J 

Fig.  7.  —  Drosera  capensis.      X  V^.  \ 

Fig.  8.  —  Time-lapse  motion  pictures  of  D.  capensis,  showing  leaf  move-  ,1 

ments.    Total  period  about  one  and  one  half  hours. 
Fig.  9.  —  D.  rotundifolia,  a  leaf  with  captured  prey. 
Fig.  10.  —  Pinguicula  vulgaris,  a  small  area  of  leaf  surface  with  the  muci-  1 

lage  glands  in  the  focal  plane  of  the  camera  lens. 
Fig    II.  —  The  same,  with  the  focal  plane  of  the  lens  at  the  level  of  the 

digestive  glands.    A  captured  insect  is  seen. 


—  Plate  14.  — 

Figs.  1-6.  —  Drosophyllum  lusitanicum. 

Fig.  I.  —  A  bit  of  a  leaf  showing  the  distribution  of  stalked  and  sessile 

glands  on  the  under  face. 
Fig.  2.  —  A  stalked  gland  in  longitudinal  section. 
Fig.  3.  —  Surface  view  of  epidermal  cells  of  the  capital  of  a  stalked  gland, 

to  show  the  buttresses. 
Fig.  4.  —  A  bud  showing  three  leaves  in  outward  circination. 
Fig.  5.  —  Transverse  section  of  leaf  showing  the  three  vascular  bundles 

and  distribution  of  the  glands. 
Fig.  6.  —  Sessile  gland  in  section. 
Figs.  7-15.  —  Byblis. 

Fig.  7.  —  Bud  of  Byblis  linifolia  showing  leaves  with  outward  circination. 
Fig.  8.  —  Bud  of  Byblis  gigantea  showing  absence  of  circination. 
Fig.   9.  —  Section  across  a  longitudinal  depression  of   the  leaf  showing 

glandular  hair,  intermediate  in  form  between  a  mucilage  hair  (fig.  12) 

and  a  true  digestive  hair  (fig.  10). 
Fig.  10.  —  Digestive  hair,  one  of  a  row  as  seen  in  fig.  13. 
Fig.  II.  —  Transverse  section  through  a  leaf,  showing  distribution  of  ad- 
hesive  glands,   vascular   bundles  and    the    outer    extensive    palisade 

zone. 
Fig.  12.  —  An  adhesive  gland,  the  right  hand  figure  showing  the  pores. 
Fig.  13.  —  Surface  view  of  leaf  showing  row  of  digestive  glands. 
Fig.  14.  —  Adhesive  gland  showing  the  curled  state  of  the  stalk  when  dry. 
Fig.   15.  —  Other  adhesive  glands  from  flower  stalk. 


—  Plate  ij.  — 

Figs.  1-5  — Pinguicula. 

Fig.  I.  —  Series  showing  a  leaf  on  different  days  after  capture  of  prey, 
Oct.  2,  3,  4,  6,  and  7.,  1939.  The  maximum  amount  of  inrolling  of  the 
margin  observed  is  indicated.    P.  vulgaris  (of  California). 

Fig.  2.  —  Digestive  glands  from  the  upper  leaf  surface. 

Fig.  3.  —  Adhesive  gland. 

Fig.  4.  —  Glands  from  scape. 

Fig.  5.  —  Section  through  margin  of  leaf,  showing  the  large  terminal 
tracheid. 

Figs.  6-24.  —  Drosera. 

Fig.  6.  —  Longitudinal  section  through  the  glandular  capital  of  a  tentacle. 

Fig.  7.  —  Transverse  section  through  a  tentacle  stalk  at  the  narrow  region. 

Fig.  8.  —  Transverse  section  through  the  gland  of  tentacle. 

Fig.  9.  —  Transverse  section  through  the  gland  of  a  marginal  tentacle  of 
D.  rotiindifolia  {see  fig.  ii). 

Fig.  10.  —  Apex  of  a  tentacle  gland  showing  exfoliated  scale-like  par- 
ticles, seen  lying  in  the  mucilage  secreted. 

Fig.  II.  —  Longitudinal  section  through  the  gland  of  a  marginal  tentacle 
of  D.  rotiindifolia. 

Fig.  12.  —  Gland  of  tentacle  after  thorough  treatment  with  sulfuric  acid. 
Only  cuticular  membranes  left. 

Fig.  13.  —  Surface  view  of  the  outer  epidermal  cells  of  a  tentacle  gland 
to  show  the  buttresses. 

Fig.  14.  —  Living  tentacle  gland.  The  mucilage  was  entirely  removed, 
the  gland  was  then  placed  in  mineral  oil.  Droplets  of  mucilage  ap- 
peared. 

Fig.  15  ,— Section  of  leaf:   absence  of  palisade. 

Fig.  16.  —  Glandular  trichome  from  petiole  {D.  gigantea). 

Fig.  17.  —  Apical  view  of  gland  shown  in  fig.  22. 

Fig.  18.  —  Small  gland  from  tentacle  stalk. 

Fig.  19.  —  Longitudinal  section  of  the  apex  of  a  leaf  rhizoid  of  D.  ery- 
throrhiza. 

Fig.  20.  —  A  young  leaf  of  D.  pygmaea,  showing  the  immense  stipules. 

Figs.  21  and  22.  —  Sessile  glands  of  D.  Whittakeri. 

Fig.  23.  —  Sessile  gland  of  D.  capensis. 

Fig.  24.  —  Scarious  trichomes  from  petiole  of  D.  rotuniifolia. 


—  Plate  i6.— 

Figs.  i-i8.  —  Drosera. 

Figs,  i,  2,  3.  —  D.  pygmaea.  i,  ventral,  2,  lateral  views  of  a  marginal 
tentacle  gland;   3,  sectional  view  of  leaf  blade  gland. 

Figs.  4-6.  —  Stages  in  the  development  of  the  gland  in  D.  rotundifolia 
(after  Homes). 

Fig.  7,  earlier,  and  Fig.  8,  later  stage  in  the  development  of  a  leaf  bud  at 
the  base  of  a  tentacle  in  D.  rotundifolia  (after  Behre). 

Figs.  9,  10.  —  Still  later  stages  of  same  in  D.  peltata.  In  fig.  10  the  ten- 
tacle is  completely  displaced  (after  Vickery).  The  broken  line  in- 
dicates one  face  of  the  thick  section. 

Fig.  II.  —  End  of  a  dropper  while  extending. 

Fig.  12.  —  Same,  on  beginning  to  round  up  to  form  a  bulb  in  D.  peltata 
(after  Vickery). 

Fig.  13.  —  Young  and  older  seedling.  A  dropper  is  developing  on  the 
older  seedling  in  D.  peltata  (after  Vickery). 

Fig.  14.  —  Ventral,  lateral  and  basal  views  of  a  gemma  of  D.  pygmaea. 

Fig.  15.  —  Same  after  Goebel.    The  right  hand  one  is  germinating. 

Fig.  16.  —  D.  pygmaea  (or  a  related  sp.),  showing  mature  gemmae  (after 
Goebel). 

Pic  17. —  Diagram  of  mid-sectional  view  of  the  true  D.  pygmaea  (col- 
lected by  Dr.  Pat  Brough  near  Sydney,  N.  S.  W.). 

Fig.  18.  —  Young  leaf  from  same,  dorsal  view. 


—  Plate  17.  — 

Fig.  I.  —  Aggregation  in  the  stalk  cells  of  Drosera  rotitndifolia.  These 
photographs  were  provided  by  Dr.  A.  Akerman.  A  and  B,  successive 
photographs  of  the  same  field  taken  2  minutes  apart;  B  and  C,  taken 
15  minutes  apart. 

Fig.  2.  —  Dionaea  muscipula  (Photograph  by  Dr.  Cornelia  M.  Smith). 

Fig.  3.  —  Dionaea  leaf  which  has  captured  a  Harvest-man  or  Harvest- 
spider  {Phalangiiim  sp). 

Fig.  4.  —  Drosera  gigantea.  This  species  grows  to  a  height  of  four  feet 
(Western  Australia). 

Fig.  5.  —  Aldrovanda  vesiculosa  (Silesia).  On  the  right  of  the  numeral  5, 
half  a  whorl  of  eight  leaves,  axial  view. 

Fig.  6.  —  Dionaea.  Moving  pictures  taken  at  one-sixteenth  of  a  second 
intervals.     The  last  one  was  taken  half  an  hour  later. 


E 


J 


—  Plate  iS.— 

Figs.  i-i8.  —  Dionaea  muscipida. 

Fig.  I.  —  Inner  surface  of  a  trap  lobe,  showing  the  distribution  of  veins, 
of  the  digestive  glands  and,  along  the  scalloped  margin,  the  alluring 
glands.     The  three  trigger  hairs  are  seen. 

Fig.  2.  —  A  trigger  hair  from  a  fully  developed  large  leaf. 

Fig.  3.  —  A  trigger  hair  from  a  minute  seedling  leaf. 

Fig.  4.  —  a,  diagram  to  indicate  postures  of  the  trap  lobes  in  (/)  open, 
(2)  closed  and  (j)  "narrowed"  states  (after  Ashida);  b,  trap  nar- 
rowed to  the  extreme. 

Fig.  5.  —  Section  of  the  upper  epidermis  and  adjacent  parenchyma  of  a 
mature  large  trap. 

Fig.  6.  —  Lower  epidermis  of  same. 

Fig.  7.  —  Young  leaf:  growth  movement  involved  in  the  unfolding  of  the 
trap. 

Fig.  8.  —  A  trap  about  2  mm.  long  showing  the  twisted  stalk  and  the 
symmetry  of  the  cilia. 

Fig.  9.  —  Upper  surface  of  the  left  lobe  of  a  trap  2  mm.  long,  taken  from 
a  seedling. 

Fig.  10.  —  Sections  of  a  mature  leaf,  drawn  to  scale,  to  show  the  relative 
sizes  of  the  epidermal  and  parenchyma  cells. 

Fig.  II.  —  A  stellate  hair  from  exterior  surface  of  trap  (and  elsewhere). 

Fig.  12.  —  A  digestive  gland.  The  section  on  the  left  is  cut  trans- 
versely to  the  leaf  lobe.    At  right,  apical  view  of  gland. 

Fig.  13.  —  Base  of  digestive  gland,  the  section  cut  at  right  angles  to 
that  of  FIG.  12. 

Fig.  14.  —  xAlluring  gland  in  section. 

Fig.  15.  —  Longitudinal  section  through  base  of  trigger  hair  to  show  the 
sensitive  cells  (arrow  point). 

Fig.   16.  —  Transverse  section  through  the  sensitive  cells  of  trigger  hair. 

Fig.  17.  —  Transverse  section  of  lobe  of  a  minute  (2  mm.  long)  trap. 

Fig.  18.  —  Longitudinal  section  of  same. 


—  Plate  19.  — 

Figs.  1-23.  —  Aldrovanda  vesiculosa. 
Figs,  i,  2  and  3.  — Stages  of  germination. 
Fig.  4.  —  Apex  of  root  cap  showing  its  obsolescence. 

Pjc    5.  —  a  series  of  juvenile  leaves  such  as  at  first  formed  on  the  plu- 
mule;  the  perfect,  mature  form  on  the  right. 
Fjg.  6. —  The  development  of  the  leaf  showing  the  early  occurrence  of 
twisting  which  brings  the  trap  into  its  definitive  posture.    E,  F  and  H, 
dorsal  views;    G,  ventral  view. 
jTjg    7  _  Immature  trap,  as  in  riG.  5,  showing  the  curvatures  which,  be- 
coming fixed,  determine  the  behavior  of  the  trap  during  narrowing. 
Fig.  8.  —  Interior  (upper)  face  of  a  trap  lobe.     Distribution  of  cruciform 
and  digestive  glands  shown,  as  also  the  sensitive   hairs   and  reflexed 
lobe  margin,  with  its  teeth. 
Fig.  9.  —  Transverse  section  through  a  footstalk  (petiole),  showing  vast 

intercellular  spaces. 
Fig.  10.  —  Section  through  the  midrib  of  a  trap. 
Fig.   II.  — Transverse  section  through  the  wall  of  a  trap  in  the  region 

marked  2,  fig.  23. 
Fig.  12.  — Three  sections  through  the  reflexed  margin  of  the  trap.     Note 

the  irregularity  of  structure. 
Fig.  13.  —  The  reflexed  margin  of  trap  with  tooth. 
Pjq    j4  —  Digestive  gland  viewed  from  above  and  laterally;    a  and  b  are 

are  normal  to  each  other. 
Fig.  15.  —  A  cruciform  gland. 

Pjg.  16.  —  A  mucilage  gland  from  the  outer  surface  of  the  trap  and  else- 
where. 
Pic    17. —  Surface  view  of  the  reflexed  lobe  margin,  showing  the  cells  of 
one  surface  intruding  between  those  of  the  other.    The  arrowpoints 
indicate  inward  or  outward  intrusion. 
Fig.  18.  —  Crossing  of  marginal  spines  to  close  the  trap  against  the  escape 
of  prey.    The  posture  of  the  teeth  in  this  figure  is  exaggerated  in  rela- 
tion  to   the  borders,   but  represents  what   does   occur  during  early 
approach  of  the  edges. 
Fig.   19.  —  Transverse  section  of  the  wall  of  the  trap  in  the  region  be- 
tween 3  and  4,  fig.  23  of  this  plate.     The  component  cells  are  cut 
longitudinally. 
Fig.  20.  —  A  trigger  hair  (above  and  to  the  right  of  the  numeral). 
Fig.   21.- Diagrams  showing   (a)  open,   (b)   closed,   (c)    early   narrowing 
and  {d)  completely  narrowed  stages  of  action.    After  Ashida,  checked 
by  my  own  observations. 
Fig.  22.  —  Diagram  to  show  zone  of  major  movement  during  closing  and 

narrowing.  ^  ,  •  1        j 

Pjc.  23.  —  Diagram  of  transverse  section  of  a  trap  to  show  the  thick  and 
thin  regions,  the  distribution  of  digestive  and  cruciform  glands,  and 
of  the  trigger  hairs. 


—  Plate  20.  — 

Fig.  I.  —  Utricular ia  vulgaris.    Leaf  with  traps. 

Fig.  2.  —  Utricularia  aff.  emarginata,  showing  water  stolons,  and  those  en- 
tering the  muddy  substrate. 

Fig.  3.  —  U.  purpurea. 

Fig.  4.  — •  U.  intermedia. 

Fig.  5.  —  U.  lateriflora  (x  J^). 

Fig.  6.  —  U.  capensis.    The  leaves  (x  2). 

Fig.  7.  —  U.  volubilis. 

Fig.  8.  —  U.  Menziesii. 

Fig.  9. —  The  same,  a  young  plant,  showing  better  the  distribution  in 
space  of  the  traps.     One  tuber  is  seen. 

Fig.  10.  —  Polypompholyx  tenella,  an  entire  plant,  the  scape  in  bud.  En- 
larged about  6  times.    Two  forms  of  traps. 

Fig.  II.  — Photograph  (x  8)  of  a  tadpole  (Biifo  marinus),  4  days  old, 
captured  by  the  head  by  a  trap  of  U.  flexuosa  at  Gordonvale,  Queens- 
land (transmitted  by  Mr.  J.  H.  Buzacott,  Feb.  10,  1936)- 

Fig.  12.  —  Floats  at  the  base  of  a  young  inflorescence  of  U.  stellaris  (Sin- 
gapore). 


I 


—  Plate  21.  — 

Sh,  chief  stolon;   5/v,  secondary  stolon;   5/3,  stolon  of  the  third  order;   /,  leaf;   rhi,  rhizoid; 
as,  air  shoot;   ic,  scape;   tr,  trap. 

Figs.  1-6.  —  Jjlricidaria  vi.lgan's. 

Fig.  I.  —  Early  germination  of  seeds. 

Fig.  2.  —  Emergence  of  primary  leaves. 

Fig.  3.  —  Aberrant  seedling. 

Figs.  4  and  5.  —  Seedlings  in  advanced  stages. 

Fig.  6.  —  Longitudinal  section  of  seed  (after  van  Tieghem). 

Fig.  7.  —  Germiination  of  U.  emarginata.  A,  embryo,  above,  its  apex  en- 
larged; D,  embryo  with  one  cotyledonoid  a  shoot;  B,  early  germina- 
tion;   C,  one  primary  shoot;    E,  two  primary  shoots. 

Fig.  8.  —  Growing  point,  U.  vulgaris. 

Figs.  9  and  10.  —  Branching,  U.  vulgaris.    Note  dwarf  branch  in  leaf  axil. 

Fig.  II. —  U.  oligosperma. 

Fig.  12.  —  U.  gilha. 

Fig.  13.  ■ —  U.  intermedia. 

Fig.  14.  —  The  same,  with  scape. 

Fig.  15.  —  U .  reniformis. 

Figs.  16  and  17.  —  U .  n.inor. 

Figs.  18  and  19. —  U.  exoleta  aS. 

Fig.  20.  — U.  gibba. 

Fig.  21.  —  U.  bitoba,  a  leaf-branch. 

Fig.  22.  —  U.  paradoxa  (Ms.  name);    s,  level  of  mud,  with  water  above. 

Fig.   23.  — The  same.     Stiff  hair  clothing  the  plant,  bifid  and  quadrifid 
hairs  and  a  trap  (material:   Young  1421,  in  Brit.  Mus.). 


—  Plate  22.  — 

1,  /2,  primary  and  secondary  leaves;   st,  with  sub-numerals,  stolons;    Ir,  trap;  pod,  podium; 
e,  embryo. 

Figs,  i-ii  and  28.  —  U.  monanthos. 

Figs.  1-3.  —  Early  germination,  during  which  the  primary  leaf  develops 
precociously. 

Fig.  4.  —  A  primary  trap  develops  in  the  place  of  a  primary  stolon. 

Figs.  5  and  6.  —  Normal  germination. 

Fig.  7.  —  The  upper  moiety  of  the  embryo  has  developed  into  a  very  long 
podium. 

Figs.  8  and  9.  —  Two  aspects  of  the  same  embryo.  Partial  concrescence 
of  the  primary  trap  with  its  axillary  bud,  and  of  the  whole  with  the 
primary  leaf. 

Fig.  10.  —  Seedling  with  a  well-developed  podium. 

Fig.  II.  —  The  bud  which  produces  the  scape  is  far  advanced. 

Fig.  12.  —  U.  orbiculata. 

Figs.  13  and  14.  —  U .  capensis.  Fig.  13,  primary  leaf  bearing  adventive 
traps  each  with  an  axillary  bud  in  adaxial  position. 

Figs.  15  and  16.  —  U.  rosea. 

Figs.  17-22.  —  U .  bifida.  Fig.  18,  precocious  development  of  primary  leaf; 
later  emergence  of  primary  stolon  from  podium  (3d,  4th,  5th  and  6th 
drawings  of  the  series  to  left  of  numeral  18);  fig.  19,  lateral  origin, 
near  base  of  embryo,  of  primary  leaf;  fig.  20,  concrescence  of  pri- 
mary leaf  and  stolon;  fig.  21,  the  primary  vegetation  point  has  pro- 
duced only  a  leaf,  while  an  adventitious  growing  point  has  emerged 
laterally,  bearing  otherwise  normal  leaf  and  stolon;  fig.  22,  primary 
stolon  apparently  from  primary  leaf. 

Figs.  23-26.  —  Polypompholyx  tenella. 

Fig.  27.  —  U.  Barnesii  (Ms.  name). 

Fig.  28.  —  U .  nionanthos.  A  stage  of  development  following  that  shown 
in  FIG.  3. 


—  Plate  2 J.  — 

Lettering  as  in  plate  21. 
Fig.  I .  —  Utricidaria  clandestina. 
Figs.  2-6.  —  U.  oligosperma. 
Fig.  7.  —  U.  simplex. 
Figs.  8-11.  —  U.  resupinata. 

Figs.  12  and  13.  —  U.  Stephensae  (Ms.  name)  aff.  U.  cymbantha  Oliver. 
Figs.  14-18.  —  Utricularia  {Biovidaria)  olivacea. 
Figs.  19  and  20.  —  U.  monanthos. 
Figs.  21  and  22. — -  U.  cymbantha. 
Figs.  23  and  24.  —  f/.  Menziesii. 
Fig.  25.  —  f/.  volubilis. 


—  Plate  24.  — 

Fig.  I.  —  Utricularia  gibba.     View  looking  into  the  entrance  showing  the  I 

velum.     X  50.  ^ 

Fig.  2.  —  U.  caeridea.    Trap  before  {left)  and  after  actuation.     Note  the  / 

changed  door  profile.  | 

Fig.  3.  —  U.  monanthos,  trap  before  {left)  and  after  actuation.  1 

Fig.  4.  —  View  looking  into  the  entrance  of  U.  dichotoma,  showing  the  \ 

circular  outer  velum.     Ca.  40  x. 

Fig.  5.  —  U.  capensis.     Trap  before  {left)  and  after  actuation.  \ 

Fig.  6.  —  Transverse  section  of  the  threshold  of  U.  cornuta,  showing  the  'i 

velum.  ' 
Fig.  7.  —  U.  Welwitschii.    The  tripping  hair. 
Fig.    8. —  Polypompholyx  miiUifida.      Trap    entrance   before    {above)    and 

after  actuation.  j 

Fig.  9.  —  Inner  surface  of  the  door  of   U.  gibba,  showing  the  concentric  1 

sulci.     Note  that  in  the  upper  part  of  this  illustration  the  anticlinal  i| 

walls  appear  constricted,  this  being  artifact.  t 

) 
I 

I 

J 
I 


I 


i 


—  Plate  25.  — 

Fig.  I. —  Utricularia  Deightonii  (Ms.  name)  aff.  peltata.     Sagittal  section  ) 

of  trap.  ■•  j 

Fig.  2.  —  Sagittal  section  of  entrance  to  trap  of  U.  peltata.  | 

Fig.  3.  —  The  same,  of  trap  of  U.  gibha  showing  very  approximately  the  j 

normal  (but  not  set)  posture  of  the  door  and  velum.  I 

Fig.  4.  —  Profile  of  the  door  and  velum  in  the  set  posture,  in  an  entirely 
whole  trap  of  U.  emarginata.  The  lens  has,  of  necessity,  to  penetrate 
a  considerable  thickness  of  tissues,  and  hence  a  sharp  picture  is  unob- 
tainable. The  velum  is  seen  as  a  bulbous  mass  just  above  the  thresh- 
old and  in  front  of  the  lower  door  edge. 

Fig.  5.  —  Sagittal  section  of  door  and  velum,  U.  gibha  —  the  same  as  in  j 

fig.  3,  but  at  higher  magnification  to  show  details  of  structure.  < 

Fig.  6.  —  View  as  from  the  inside  of  the  trap  of  the  middle  reach  of  the  ; 

velum  in  U.  vulgaris. 

Fig.  7.  —  U.  gibba.    Transverse  section  of  the  threshold  with  the  velum,  j 

from  which  its  origin  can  be  discerned.  . 

Fig.  8.  —  The  same.     View  of  the  velum  as  one  looks  into  the  entrance. 

Fig.  9.  —  U.  intermedia  (or  U.  vulgaris).  View  looking  down  on  the  pave-  , 

ment,  showing,  however,  only  a  narrow  middle  fore  and  aft  strip. 
The  velum  is  at  the  lower  edge  of  the  picture.  The  outer,  middle  and 
inner  zones  are  discernible. 


—  Plate  26.  — 

Fig.  I.  —  Diagram  of  a  sagittal  section  of  entrance  of  the  trap  of  Utricu- 
lar ia  gibba,  with  terminology. 
Fig.  2.  —  Entrance  of  U.  gibba,  exoleta  etc.  in  sagittal  section.  The 
arrows  (3,  4)  indicate  the  general  direction  of  the  movements  of  prey 
in  approach.  The  structure  of  the  pavement  is  seen  through  the  door 
as  if  transparent. 

Fig.  3.  —  U.  gibba.  View  of  threshold  and  door  edge,  as  seen  from  the 
viewpoint  indicated  by  the  arrow  i  in  fig.  2.  Arrow  i  indicates  the 
direction  of  thrust  of  the  side  of  the  door  on  the  lateral  reaches  of 
the  threshold;  arrow  2,  thrust  of  the  door  lateral  hinges  on  the  middle 
piece,  and  of  this  against  the  pavement  in  its  middle  reach. 

Fig.  4.  —  Sagittal  section  of  entrance  of  U.  longifolia. 

Fig.  5.  —  U.  purpurea.  The  knob  at  the  middle  of  the  door.  See  fig. 
2-4,  PLATE  27. 

Fig.  6.  —  U.  vulgaris. 

Fig.  7.  —  The  same,  the  door  swung  widely  open. 

Fig.  8.  —  Diagram  of  the  sagittal  section  of  the  door  of  U.  purpurea  to 
show  that  movement  of  the  knob  up  or  down  lifts  the  door  edge;  c, 
center  of  rotation;  d,  b,  displacements  of  point  a  when  the  trigger 
hairs  are  touched  downwardly  or  upwardly,  respectively. 

Fig.  9.  —  Quadrifid  hair  of  U.  gibba,  quite  young. 

Fig.  10.  —  Reflexed  quadrifid  hair  of  U.  neottioides. 

Fig.  II.  — Quadrifid  hair  of  Poly  pom  pholyx. 

Fig.  12.  —  The  same,  side  view. 

Fig.  13.  —  The  same,  diagram  of  the  shape  of  a  single  one  of  the  four  cells 
of  the  capital. 


H 


—  Plate  2y.  — 

Fig.  I.  —  Trap  of  Utricitlaria  biloba.    Only  a  few  of  the  bifid  and  quadri- 

fid  hairs  are  shown. 
Fig.  2.  —  Entrance  of  U .  purpurea,  sagittal  section.    The  door  is  regarded 

as  transparent. 
Fig.  3.  —  The  same,  the  door  in  open  and  closed  postures. 
Fig.  4.  —  Trap  of  U.  elephas  Luetz. 
Fig.  5.  —  Trap  of  Utricularia  (Biovularia)  olivacea. 
Fig.  6.  —  Front  view  of  door  of  same  to  show  the  six  tripping  bristles.  [ 

Fig.  7.  —  Traps  of  U.  resupinata  displaying  dimorphism. 
Fig.  8.  —  Trap  of  U.  exoleta  (Queenlad). 
Fig.  9.  —  Trap  of  U.  neoUioides. 


J 
1 


Plate  28.  — 


Figs.  1-4.  —  Utricularia  Lloydii  Merl,  an  example  of  dimorphism. 

Fig.  I.  —  The  kind  of  trap  found  only  on  the  leaves. 

Fig.  2.  —  Trap  found  only  on  the  stolons. 

Fig.  3.  —  Door  with  single  tripping  bristle,  from  leaf  trap. 

Fig.  4.  —  Door  of  stolon  trap,  devoid  of  tripping  bristle. 

Fig.  5.  —  U.  nana. 

Fig.  6.  —  Entrance  of  same,  showing  the  two  tripping  bristles. 

Figs.  7-9.  —  U.  globulariaefolia. 

Fig.  7.  —  Entrance. 

Figs.  8  and  9.  —  Two  forms  of  trap  (dimorphism). 


—  Plate  2g.  — 

Figs.  1-13.  —  Utricidaria. 

Fig.    I.  —  Diagrammatic    representation    of    the   histology   of   the    door. 
Above,  view  en  face  of  the  door  seen   from  the  inside   of   the   trap; 
below,  section  through  a-b. 
Fig.  2.  —  Sagittal  section  of  the  door:    7,  upper  hinge;    2,  middle  area; 

5,  central  hinge;    4,  middle  piece;    cut,  cuticle;    eel,  cellulose. 
Fig.  3.  —  Cells  of  the  inner  course  of  a  portion  of  the  door,  the  central 
hinge  approximately  in  the  middle;    the  bases  of  the  tripping  bristles 
shown  in  dotted  lines.     Numerous  props. 
Fig.  4.  —  Transverse  section  of  the  threshold  at  the  middle  point,  showing 

the  velum.    The- posture  of  the  door  edge  in  broken  lines. 
Fig.   5.  —  Section   through   the  lateral  reach,   near  its  outer  end,   of  the 
threshold  in  U.  purpurea.     The  posture  of  the  door  thrusting  against 
the  pavement   indicated   by   the   oblique   arrows.     The   direction   of 
water  pressure   against   the   door  and   velum   shown   by  the   arrows 
below. 
Fig.  6.  —  Surface  hairs  of  U.  purpurea;    a,  sickle-shaped,  glandular  (muci- 
lage) hairs;    6,  c,  young  stage  of  oil-bearing  hairs;    d-g,  mature  stage 
of  same,  showing  oil  deposit  held  by  the  raised  cuticle. 
Fig.  7.  —  Glandular  hairs  of  the  central  boss  of  the  door  of  U.  purpurea, 

shown  in  developmental  stages,  numbered  serially. 
Fig.   8.  —  Diagram  of  wall  structure,  showing  the  inner  quadrifid   {left) 
and   the   outer  spherical  glands.     Vascular   tissue   between   the   two 
cell  courses. 
Fig.  9.  —  Peltate  leaves  of  U.  sp.  aff.  peltata  (from  Angola).    They  bear  a 

deep  coating  of  mucilage  on  their  upper  surfaces. 
Fig.  10.  —  Mucilage  glands  of  the  same  with  their  heavy  loads  of  stiff  mu- 
cilage   {b)\    c,    scheme    of   branching:     a,    leaf,    with    three    branches 
(stolons   of    second   order)    emerging   from    the   primary   stolon   seen 
axially. 
Fig.  II.  —  U.  gibba,  schematized  to  show  relation  of  door  and  threshold 
in  the  wide-angle  type  of  entrance  (cf.  30  —  3).     The  angular  rela- 
tion of  the  door  posture  {p-d)  to  the  general  level  of  the  threshold  {p- 
t)  is  ca.  90  ;    r,  relaxed  posture  of  door;    s,  set  posture;    pr,  various 
possible  directions  of  impact  of  prey  on  the  tripping    bristles;     uh, 
upper  hinge;    ch,  central  hinge;    Ih,  lateral  hinge;    <j,   middle  piece. 
Fig.    12.  —  Narrow   angle   door:    its   shape   and   areas    {cj.   jo  —  4)   and, 
below,  the  areas  of  the  threshold,  of  U.  capensis;    uh,  upper,  and  Ih, 
lateral  hinge;    ma,  middle  area;    mp.  middle  piece;    oz,  outer  zone  of 
pavement;    tnz,  middle  zone;    and  iz,  inner  zone,  of  same. 
Fig.  13.  —  Wide  angle  door  {U.  gibba  or  vulgaris  etc.);    ch,  central  hinge. 


I 

I 


—  Plate  JO.  — 

Figs.  i-8.  —  Utricularia  cornuta. 

Fig.  1.  —  The  trap  in  lateral  and  frontal  views. 

Fig.  2.  — Entrance,  with  alluring  glands  below,  from  in  front. 

Fig.  3.  —  Sagittal  section  of  entrance.  The  door  {di)  is  shown  in  the  set 
posture;  d-i  its  open  posture;  dz  normal  relaxed  posture  and  di,  totally 
relaxed  posture,  as  when  the  trap  is  punctured;  dt,  direction  of 
thrust  of  lateral  hinge;  0/,  longitudinal  thrust  of  door;  c,  compo- 
nent of  the  two  thrusts;   dh,  inner  angle  of  threshold,  as  also  in  fig.  5. 

Fig.  4.  —  The  door  seen  from  in  front.  Inner  course  cells  in  double  out- 
line.   Lettering  as  above. 

PiQ  ^  —  View  of  pavement  from  above  as  from  point  d,  fig.  3;  oz,  mz, 
iz,  outer,  middle  and  inner  zones  of  pavement;   de,  position  of  door 

edge. 
Fjg    6  _  Section  through  door  and  threshold  taken  as  between  c  and  d, 

FIG.  3;    I,  set,  and  2  relaxed  posture  of  door,  approximately. 
fjG   7.  _  Section  of  same  through  d,  fig.  3.    Broken  lines  indicate  opening 

flexures. 
Fig.  8. —  Section  of  same  through  c,  fig.  3;    mp,  middle  piece;    /,  rear 
part  of  middle  zone  of  pavement  indicated  in  outline;   d,  dotted  line 
indicating  the  thrust  of  the  door  edge  into  the  soft  pavement  cells 
(arrows  indicate  the  thrust  of  the  lateral  hinges). 


—  Plate  31.—  ^  ^ 

Fig.  I.  —  Entrance  of  Utricular ia  caeriilea. 

Fig.  2.  —  Trap  of  U.  Gibbseae.  ^ 

Fig.  3.  —  Trap  of  U.  capensis. 

Fig.  4.  —  Entrance  of  U .  Welwitschii. 

Fig.  5.  —  View  from  below  of  trap  of  U.  rosea  aff.  (N.  Queensland). 

Fig.  6.  —  Entrance  of  U.  Deightonii  (Ms.  name). 

Fig.  7.  —  Front  view  of  entrance  of  same. 

Fig.  8.  —  Door  of  U.  Welmtschii,  showing  the  kriss  tripping  hair  {see  also 

24  —  7). 
Fig.  9.  —  Entrance  of  U.  capensis.  ( 

Fig.  10.  —  U.  rosea,  entrance,  small  trap.  ^ 

Fig.  II.  ^ — The  two  forms  of  the  trap  of  U.  rosea.  ^ 


—  Plate  J2.  — 

Fig.  I.  —  Utricular ia  orhiculata.     Entrance. 

Fig.  2.  —  Front  view  of  the  door,  U.  striatida. 

Fig.  3.  —  U.  striatida.    Entrance. 

Fig.  4.  —  Transverse  section  through    the    entrance,    showing    the    front 

view  of  the  tripping  hairs  with  their  mucilaginous  masses. 
Fig.  5.  —  U.  midticaulis,  trap. 
Fig.  6.  —  Development  of  the  peculiar  tripping  glands  of  U.  orhicidata, 

numbered  in  series,  1-8.     In  8  the  mucilage  mass  has  fallen  away. 
Fig.  7.  —  Utricidaria  sp.  (Thibet,  Ludlow,  Sherreff  and  Taylor,  No. 

5264,  Brit.  Mus.)  to  display  the  form  of  the  forked  rostrum. 
Fig.   S.  —  Utricidaria  sp.   (Thibet,  L.,   S.  and  T.   5802),  door  and  single 

rostrum  with  long  radiating  fingers.  i 

Fig.  9.  —  Rostrum  of  U.  midticaulis  (Fig.  5)  from  below.  | 

1 


—  Plate  33.  — 

Fig.  I.  —  Utricularia  Kirkii.    Entrance. 

Fig.  2.  - —  Transverse  sections  of  entrance  of  U.  Kirkii  through  a,  b,  c, 
and  d,  fig.  i. 

Fig.  3.  —  U.  longiciliata,  trap,  side  and  front  views. 

Fig.  4.  — •  The  same,  entrance,  showing  single  glandular  tripping  bristle. 

Fig.  5.  —  U.  lateriflora. 

Fig.  6.  —  Utricularia  sp.  (Ceylon,  Simpson  No.  9482)  related,  if  not  iden- 
tical, with  U .  calUphysa  Stapf. 

Fig.  7.  —  The  same,  in  sagittal  section. 

Fig.  8.  —  U.  Barnesii  (Ms.  name).  Trap  and  views,  from  beneath,  of 
the  lower  and  upper  lateral  combes. 

Fig.  9.  —  U.  lateriflora:  set  and  relaxed  postures  of  the  door,  traced  from 
photographs. 


—  Plate  J4.  — 

Fig.  I.-  Ulricularia  monanlhos,  trap,  studded  with  glands. 

Fig.  2.  —  Entrance  of  same,  sagittal  section. 

Fig.  3.  —  Same,  in  diagram  to  show  set  {di),  relaxed  (^2)  and  quite  open 
{dz)  posture  of  the  door.  Arrows  indicate  water  pressure  on  the  door; 
nip,  middle  piece,  the  arrow  4  indicating  the  direction  of  the  thrust  of 
the  lateral  hinges  on  it;  pmp,  arrow  indicates  the  direct  thrust  of 
middle  piece  itself;  ov,  iv,  outer  and  inner  velum;  pe,  pavement;  uh, 
upper  hinge;  2,  inner  angle  of  the  threshold,  th;  j,  line  of  attach- 
ment of  door  to  wall. 

Fig.  4.  —  Section  of  trap  so  made  as  to  allow  one  to  look  down  through 
the  door  (regarded  as  transparent)  so  as  to  see  the  opening  guarded 
by  the  outer  velum.  The  two  groups  of  glands  on  the  door's  outer 
surface  are  shown.  The  abrupt  bend  in  the  threshold  is  indicated  by 
the  transverse,  curved  dotted  line.  The  other  two  dotted  lines  indicate 
the  limits  of  the  lateral  hinge.    Lettering  as  in  previous  figure. 

Fig.  5.  —  Section  across  the  entrance  showing  the  deeply  curved  concave 
threshold  (th)  and  the  door  fitting  into  it,  held  by  the  thrust  of  the 
lateral  hinges  (long  arrow)  on  the  middle  piece  {mp,  short  arrow). 
The  dotted  lines  indicate  flexures  of  the  door  edge  on  opening. 

Fig.  6.  —  The  various  kinds  of  traps  of  U.  volubilis.  A,  short  stalked,  basal 
trap;  B,  long  stalked  trap,  with  foliaceous  stalk;  C,  rostrum  of  A; 
D,  E,  dorsal  and  lateral  views  of  stolon  trap. 

Fig.  7.  —  Variants  of  the  trap  of  U.  Hooker i.  A,  large  trap  with  deeply 
laciniate  wings;  B,  its  rostrum  and  wings  seen  from  above;  C, 
medium  sized  trap  with  broader  wings;  D,  small  trap  with  ventral 
wings  suppressed,  the  dorsal  wings  and  rostrum  very  slender. 


—  Plate  55.  — 
Traps  of  Utricularia  species  (all  of  the  U.  monanthos  type) : 


Fig.  I.  —  Utricularia  Singeriana  F.  Muell. 

Fig.  2.  —  U.  Wallichiana  Wight. 

Fig.  3.  — ■  U.  Hamittonii  F.  E.  Lloyd. 

Fig.  4.  —  U.  Dimstani  F.  E.  Lloyd. 

Fig.  5.  —  U.  lasiocaidis  F.  Muell. 

Fig.  6.  —  Looking  into  the  entrance  of  any  of  these  species,   the  outer, 

circular  velum,  through  the  opening  of  which  are  seen  the  glands  on 

the  door  surface. 
Fig.  7.  —  U.  Moorei  F.  E.  Lloyd. 
Fig.  8.  —  U.  tubulata  F.  Muell. 

Fig.  9.  —  U.  Holzii  F.  Muell.  and  U.  albiflora  R.  Br. 
Fig.  10.  —  U.  Menziesii  R.  Br.,  seen  from  beneath. 
Fig.  II. —  U.  Menziesii,  lateral  view. 


I 
f 


I 


1 


—  Plate  36.  — 

Figs.  1-9,  Polypompholyx;    Figs,  io-ii,  U.  tiihulata. 

Fig.  I.  —  Trap  (side  view)  of  P.  mnUifida  F.  Muell. 

Fig.  2.  ^ — Same,  sagittal  section:   c,  antechamber;   </,  door;   /c,  large  inter- 
cellular space  in  the  stalk;    r',  ridge  along   ventral   surface   of    the  | 
stalk;   s,  a  zone  of  hairs  seen  in  fig.  i.  ' 

Fig.   3.  —  Transverse  section,  embracing  part  indicated  by  the  parallel 

broken  hnes  in  fig.   i,  looking  inwardly;     s,  space  above  door;    d,  ; 

door;     c,  back  wall  of  antechamber;    r,  n,  ridge  along  the  stalk;    ic, 
intercellular  space  in  the  stalk. 

Fig.  4.  —  Trap,  view  from  above.    Arrows  indicate  directions  of  approach  j 

of  prey,  as  also  in  fig.  i.  | 

Fig.  5.  —  Entrance,  showing  the  door  in  the  relaxed  posture.    The  broken  *     j 

lines  indicate  the  set  posture  (c/.  24  —  8).  I 

Fig.  6.  —  Trap  of  P.  tenella,  from  below.  ' 

Fig.  7.  —  Transverse  section  through  body  of  trap  of  P.  niuUifida,  show- 
ing the  occurrence  of  deep  compression  cells. 

Fig.  8.  —  Transverse  section  of  the  threshold  of  the  large  traps  of  P. 
latifolia. 

Fig.  9.  —  Same,  of  the  small  traps.  i 

Fig.  10.  —  Growing  point  of  Ulricularia  tubulata. 

Fig.  II.  —  A  whorl  of  very  young  leaves  and  traps  alternating  at  the  same 
level.  Lateral  view  with  growth  apex  above  the  numeral,  axial  view 
below.  ' 


I 


—  Plate  37.  —  ^ 

Moving  pictures  showing  the  action  of  the  trap  of  Utrkularia,  and  of  the  sensitive  hairs 

of  Dionaea  (all  frames  are  1/16  sec.  apart,  except  in  fig.  2,  in  which  they  are  1/160  sec.  ; 

apart,  and  in  fig.  lA,  which  is  time  lapse);  — 

Fig.    ik.  — Utrkularia   purpurea.     Trap  showing  the  exhaustion  of  the 

contained  water  and  the  consequent  collapse  of  the  walls,  indicated  ^ 

by   the   distortion   of   a   contained   bubble   of   air.      Moving  picture:  , 

time  lapse  spread  over  about  2  hours.  J 

Fig.  iB.  — The  same,  viewed  edgewise,  before  and  after  action.  i 

Fig.  2.  —  U.  vulgaris.     View  looking  into  the  entrance  showing  the  open-  , 

ing  of  the  door  (in  1/160  sec.)  and  the  subsequent  closing  in  4/160  \ 

sec.     The  open  door  is  seen  in  the  third  frame  from  top.     The  round  1 

object  in  front  of  the  door  is  the  knob  of  a  glass  probe.  ; 

Fig.  3.  —  t^.  vulgaris.    The  capture  of  a  copepod.    The  trap  was  set  in  a 

shallow  glass  tank  with  walls  to  guide  the  copepod  to  the  mouth  of  1 

the  trap.  ' 
Fig.  4.  —  The  same.    The  lateral  profile  of  a  trap  before  and  after  {below) 

actuation. 
Fig.  5.  —  Dionaea  muscipula.     Bending  and  straightening  of  a  sensitive 

hair. 
Fig   6  _The  "Darwin  experiment,"  referred  to  in  the  text:    the  sudden 

disappearance  of  colored  particles  (here  particles  of  carbon)  resting  on  I 

the  door,  on  its  actuation  by  a  needle  point  slowly  moved  across  the  '■ 

entrance. 
Fig.  7.  —  U.  gibba,  capturing  a  larva. 

Fig.  8.  —  U.  purpurea.     A  trap  swallowing  a  bubble.  _  = 

Fig.  9.  —  U.  vulgaris.     Trap  swallowing  a  glass  bead  and,  in  doing  so, 

jumping  at  the  probe.    The  trap  had  been  removed  from  the  plant. 


—  Plate  jS:— 

Animation  of  the  trap  of  U.  gibba,  by  Mr.  Harold  Peberdy,  illustrating 
its  action  in  the  capture  of  prey  (Courtesy  of  the  Associated_Screen 
News,  Montreal). 


—  »*. 


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V 


INDEX    of  PLANT   and  ANIMAL   NAMES 


ACACLA,    30,   56 

Acaulopage,  173 

Aegopodium  podagraria,  119 

Aldrovanda,  i,  2,  5,  6,  7,  177,  181, 
182,  186,  i8g,  190,  ig2,  193,  194, 
195,  200,  203,  204,  205,  206,  208, 
2og,  210,  211,  237,  239,  249,  267 

• verticillata,  195 

vesiculosa,   177,  194,  195,  210, 

pi.  17,  19 

var.  australis,  195 

Aldrovandia,  195.  210,  211 

vesiculosa,  21c,  211 

Amoeba,  170*,  173,  174,  175 
proteus,  17s 

sphaeronucleus,  174 

terricola,  173 

verrucosa,  17s 

Anabaena  azoUae,  3 
Andromeda  polifolia,  115 
Anguillulidae,  169 
Anopheles,  267 

albimanus,  267 

Anuria,   172 
Aphanomyces  astaci,  176 

Magnusi,  176 

ovidestruens,  176 

Apogonia  spherica,  73 
Aquilegia,  3 
Aranella  fimbriata,  215 
Aristolochia,  3,  214 
Arthrobotrys,  4,  170,  171 

oligospora,  169,  17c* 

Ascaris,  36 

lumbricoides,  36 

Asclepias,  4 

Cornuti,  8 

Auricularia,  119 
AzoUa,  3 

Bacillus  aquaticus  communis,  265 

Bacterium  coli,  265 

fluorescens  liquefaciens,  72,  75 

prodigiosum,  75 

Bdellospora  helicoides,  174 
Begonia,  132,  134 

Biovularia,  i,  2,  7,  213,  214,  217, 
227,  228,  249,  257,  258 

minima,  213,  227,  228 

olivacea,  90,  213,  227,  228,  pi. 

23,  27 
Brachionus,  172 
Brachydeutera  argentata,  214 
Brocchinia,  226 
Bufo  marinus,  252,  pi.  20 
Bulbophyllum,  65 
Byblidaceae,  i,  95,  98 
Byblis,  I,  2,  5,  35,  95,  97,  98,  99, 

100,  268,  pi.  13,  14 

gigantea,  95,  96,  98,  99,   118, 

pi.  Q,  13,  14 

linifolia,  95,  g6,  99,  117,  pi.  14 

Caltha  dioneaefolia,  5,  6 
Cecropia,  56 
Cephalotaceae,  i 

Cephalotus,  i,  2,  15,  16,  38,  49,  62, 
79,  82,  86,  89,  264 

follicularis,  40,  81,  89,  pi.  g,  10 

Chironomidae,  78 
Chlorion  Harrisi,  38 
Chrysamphora  (see  Darlingtonia),  i, 

Cladonia  uncinalis,  115 

Cladophora,  171 

Cochlonema  dolichosporum,  174 

verrucosum,  174 

Codiaeum,  59,  60 
Colura,  3 

Colurus,  171,  172 

Coprinus,  4 

atramentarius,  92 


Cordyceps,  2,  169,  174 
Cosmiza,  215 
Cotyledon,  67 
Crinum,  65 
Culicidae,  78,  267 
Cyclops,  234 

Dactylaria,  170 

Candida,  171 

Dactylella,  2,  170,  175 

bembicoides,  170*,  175 

• tylopaga,  170*,  173 

Daphneae,  234 

Daphnia,  234 

Darlingtonia  =  Chrysamphora,  i, 
2,  10,  23,  24,  25,  26,  28,  i^,  35, 
38,  40,  42,  43,  44,  45,  46,  47.  48, 
49,  69,  83 

californica,  36,  39,  40,  49,  50, 

pi.  4,  5,  6 

Delphinium,  3 

Diaptomus,  176 

Dionaea,  i,  2,  5,  6,  7,  105,  109,  135, 
165,  177,  178,  181,  182,  186,  187, 
188,  191,  192,  193,  194,  195,  196, 

197,    199,    200,    2CI,    202,    203,   204, 

205,  209,  210,  211,  239,  pi.  17,  37 

muscipula,  138.  177,  178,  179, 

210,  211,  pi.  17,  18,  37 
Dipsacus  sylvestris,  3,  8 
Dischidia,  3,  65 

pectinoides,  3 

Distomum  hepaticum,  113 

Distyla,  172 

Dorniphora  venusta,  38,  39 

Drosera,  1,  2,  4,  5,  7,  35,  39,  7°,  89, 
98,  99,  100,  102,  104,  105,  108, 
109,  no,  113,  115,  116,  117,  118, 
119,  120,  124,  129,  134,  135,  136, 

138,  139,  141,  150,  151.  158,  159, 
160,  161,  162,  163,  164,  165,  166, 
167,  168,  178,  182,  194,  2CI,  210, 

211,  245,  pi.  IS,  16 
anglica,  115,  157 

auriculata,  118,  130,  168 

binata,  116,  117,  118,  131,  132, 

135,  139,  143,  144,  145,  157,  167 

capensis,   116,   118,   119,   128, 

132,  134,  135,  139,  143,  145,  161, 
165,  168,  pi.  13,  IS 

■ dichotoma,  70,  116,  117,  118, 

139,  159,  166 

erythrorhiza,  117,  pi.  IS 

filiformis,   115,   117,   118,   134, 

13s,  163,  165 

gigantea,   115,   116,   118,   120, 

126,  139,  pi.  IS,  17  t 

intermedia,  115,  116,  131,  132, 

139,  143,  144,  146,  165,  166,  167 

longifoha,  131,  138,  166,  168 

lunata,  118 

paleacea,  120 

peltata,  118,  120,  130,  134,  168, 

pi.  16 

■ pygmaea,   117,   118,   120,   122, 

130,  131,  166,  pi.  IS,  16 

regia,   115,   116,  117,  118,  168 

rotundifolia,  115,  116,  117,  118, 

119,  120,  130,  131,  132,  133,  134, 
13s,  J38,  139,  142*,  143,  144,  157, 
160,  163,  165,  166,  167,  168,  pi. 
13,  IS,  16,  17 

spathulata,  133,  I43 

subhirtella,  118 

VVhittakeri,  115,  118,  120,  123, 

125,  165,  167,  168,  pi.  /i 

Droseraceae,  i,  95,  166,  177,  210 

Drosophila,  112,  139 

Drosophyllum,  i,  2,  5,  96,  99,  100, 
loi,  102,  104,  105,  117,  118,  122, 
124,  137,  152,  155,  166,  168 

lusitanicum,  99,  105,  pi.  13,  14 


Empusa,  2 

Endocochlus  asteroides,  174 
Erica  tetraU.x,  5,  109 
Eriophorum  vaginatum,  115 
Euglena,  172,  265 
Exyra,  36,  37 

■ Ridingsii,  36,  37 

■ Rolandiana,  36,  37,  38 

semicrocea,  36,  37 

Flagellarla,  59 
Frullania  cornigera,  3 

Galium  verum,  112,  161 
GenUsea,  i,  2,  4,  7,  go,  94,  106,  213, 
216,  217,  230,  pi.  II,  12 

filiformis,  90 

ornata,  90,  94,  pi.  IJ 

repens,  92,  pi.  9 

Gloriosa,  59 
Gossypium,  60 

Heliamphora,  I,  2,  g,  10,  11,  14, 
IS.  16,  25,  30,  39,  43,  69,  89,  98, 
211 

• Macdonaldae,  9,  12,  13*,  pi.  I 

minor,  9,  11,  12,  13*,  16 

nutans,  9,  11,  12,  13*,  16,  pi. 

I,  2 

Tatei,  9,  12,  13* 

■ Tyleri,  11,  12,  13,  16 

Heteronema,  265 
Hydrolea,  5 

Impatiens,  igi,  192 

Iris,  22,  2g,  30,  31,  32,  39,  61,  67 

pallida,  67 

Lathraea  squamaria,  3 

Lejeunea,  3 
Lemna,  119 

Lentibulariaceae,  i,  7,  94,  95.  213, 
228,  267,  268,  270 

Marcgravl-^,  3 
Marchantia,  131 
Martynia,  5 

Megarhinus  acaudatus,  77 
Metopidia,  171,  172 
Metriocnemus  Edwardsii,  36 

Knabi,  36 

Mimosa,  142,  179,  189,  igi 
Mirabilis  longifolia,  5 
Misumenops  nepenthicola,  77 

Thienemannii,  77 

Molinia  coerulea,  6,  8 
Monacrosporium,  170 
Monostyla,  171,  172 

Nelumbo,  30 

Neosciara  Macfarlanei,  38 

Nepenthaceae,  i.  79,  80 

Nepenthes,  i,  2,  10,  16,  30,  31,  35, 
38,  39,  SI,  52,  59,  60,  63*  64,  65, 
66,  67,  69,  70,  71.  73,  74,  75.  76, 
77,  78,  79,  80,  81,  82,  86,  88,  8g, 
98,  114,  160,  161,  163,  164,  166, 
168,  211,  212,  pi.  7,  S 

ampullaria,  52,  53,  54.  55.  56, 

57,  58,  64,  65.  66,  77,  78,  79,  pl- 
4,7,8 

Balfouriana,  pl.  4,  7 

bicalcarata,  52,  55,  56,  57,  58, 

59,  62,  63*,  66,  pl.  4,  7 

borneensis,  59 

Boschiana,  55 

Burbidgei,  56 

clipeata,  55,  60,  61 

destillatoria,  51,  76,  79 

dubia,  55,  57 

Edwardsiana,  56 

formosa,  62 


Francis  E.  Lloyd 


—  349  — 


Carnivorous  Plants 


gracilis,  51,  55,  pL  7 

gracillima,  65,  67 

Hibberdii,  75 

• inermis,  55.  57.  64.  66,  pi.  7 

intermedia,  55,  S6.  58,  59.  62, 

63*,  pi.  7 

Ladenburgii,  57 

Lowii,  55,  57.  58.  64,  pi.  7.  * 

Mastersiana,  68,  73,  pi.  4 

maxima,  55,  57 

melamphora,  80 

mixta,  75,  pi.  4 

Morganiana,  75 

paradii^iaca,  72 

Pervillei,  68,  pi.  7 

phyllamphora,  S5,  57.  80 

Rafflesiana,  52,  5g 

■ var.  nivea,  56 

Rajah,  51,  56,  57 

stenophylla,  65 

• Tiveyi,  57,  64,  pl-  7,  ^ 

Veitchii,  51,  52.  57,  80 

ventricosa,  55.  56.  57.  66,  68, 

78,  pl.  4,  7 

Vieillardii,  55 

villosa,  51,  64 

Nicotiana  tabacum,  s 
Noteus,  172 
Nymphaea,  32 

Papaipema  appassionata,  36 

Paramaecium,  172,  265 

Paranema,  172 

Pecten,  204 

Pedilospora   dactylopaga,    173.    i75 

Pelargonium  zonale,  5 

Phacus,  265 

Phalangium,  pl.  17 

Phaseolus  multiflorus,  212 

Philodina,  172 

Phoridae,  78 

Phragmites,  209 

Physiotum,  3 

majus,  3 

Pinguicula,  i,  2,  5,  7,  95.  106,  io7. 

108,  109,  no.  III,  112,  113,   114. 

119,  161,  162,  163,  164,  165,  166, 

168,  213,  264,  pl.  IS 

alpina,  114 

cuneata,  106 

gypsicola,  105.  106 

hirtiflora,  no 

vulgaris,    106,    109,    112,    114, 

119,  pl.  13,  IS 

Pittosporaceae,  95 

Pleurothallus,  65 

Podostemonaceae,  226 

Polypompholyx,  i,  2,  7,  60,  95,  98, 
213,  215,  216,  217,  218,  229,  230, 
254,  256,  257,  262,  268,  269,  pl. 
26,  36 

latifolia,  230,  262,  263,  pl.  36 

multifida,  95,  pl.  24,  36 

tenella,  95,  230,  pl.  20,  22,  36 

Pothos,  60 

Primula  sinensis,  s 


purpurea,  17,  18,  19,  22,  23,  24, 

25,  26,  27,  28,  31,  33.  34.  35.  36. 
37.  38,  39.  43,  45.  46.  5°.  146,  pl- 
I,  2,  3 

gibbosa,  17,  18 

var.  stolonifera.  39 

venosa,  17,  i? 


RhYNCHOSPORA  alba,    IIS 

Ricinus  communis,  74 
Roridula,  i,  5,  8,  78,  98 
Rotatoria,  171,  172,  175,  176 
Rotifer,  172 

Salicornia,  65,  79 

Salpina,  171,  172 

Sarcophaga,  38,  77 

Sarracena,  18 

Sarracenia,  i,  2,  9,  10,  11,  15,  16, 
17,  18,  19,  20,  22,  24,  30,  32,  33, 
34,  35.  38,  40,  43,  45,  46,  47,  49, 
S9,  62,  69,  81,  82,  83,  86,  89,  146, 
163,  245 

adunca,  18,  49,  66,  80 

Courtii,  17,  26 

Drummondii,    17,   27,   29,   30, 

33,  35,  37,  43.  pl-  I 
flava,  17,  21,  29,  30,  31,  33,  35, 

37.  38.  39,  46.  77,  pl-  I 

■ Jonesii,  17,  30,  pl.  3 

■ minor,  17,  26,  27,  28,  29,  31, 

33,  34,  37,  43,  pl-  ',  3 

oreophila,  17 

psittacina,  17,  19,  22,  23,  24, 

25.  26,  27,  is,  34,  37,  43,  pl.  I,  3,  S 


rubra,  17,  33,  34.  37 

Sledgei,  17,  33,  35,  37 

variolaris,  39,  49 

Sarraceniaceae,  i,  39,  40.  45.  48 
Saxifraga  rotundifolla,  5 

umbrosa,  5 

Scheuchzeria  palustris,  115 

Schrankia,  178 

Scirpus  caespitosus,  115 

Sequoia  gigantea,  115 

Sicyos,  192 

Silene,  s 

SommerstorfBa  spinosa,  173,  i75 

Sparmannia,  s 

Sphagnum,  19,  115,  116,  133 

Spirillum,  206 

Spirogyra,  207,  211 

Squalella,  172 

Stentor,  172 

Stylonychia,  172 

Stylopage,  175 

Syngonium  podophyllum,  60 

Tarsius  spectrum,  58 
Telenchus  scandens,  169 
Tetralobus,  215 
Thomisus  callidus,  77 

nepenthephilus,  77 

Tillandsia,  213,  226 
T-orenia,  132 
Tradescantia,  18 
Trichothecium.  170 
Tussilago  farfara,  119 
Typha,  209 

Utricularia,  I,  2,  3,  6,  7,  8,  60,  89, 
go,  gi,  92,  94,  95,  106,  127,  152, 
160,  162,  167,  168,  194,  199,  204, 
207,  2og,  210,  211,  213,  214,  216, 
2ig,  222,  226,  227,  228,  231,  236, 
237,  23g,  242,  244.  247.  257,  263, 
264,  265,  266,  267,  268,  269,  270, 
pl.  2Q,  32,  33,  35,  37 

albiflora,  230,  pl.  33 

amethystina,  21^.  257 

Barnesii,  232,  pl.  22,  33 

Berendii,  7 

bifida,  217,  218,  259,  pl.  22 

biloba,  225,  257,  pl.  21,  27 

brachiata,  216,  232,  260,  267 

Bremii,  225 

caerulea,  231,  255*,  256,  258, 

259,  pl-  24,  31 

calliphysa,  232,  260,  pl.  33 

Campbelliana,  226 

capensis,   217,   218,   231,   254, 

255*.  256,  259,   260,   269,  pl.  20, 

22,  24,  2Q,  31 

capilliflora,  214,  215*,  218,  230 

clandestina  225,  pl.  23 

— ,-  cleistogama,  217,  221*,  235 

■ cornuta,    146,    227,    231,    245, 

256,  258,  259,  265,  pl.  24,  30 

cyanea,  259 

cymbantha,  213,  214,  222,  224, 

f'-  ^-'     ,        .. 

Deightonr,  259,  pl.  25,  31 

dichotoma,  229,  230,  254,  261, 

270,  pl.  24 

Dunstani,  214,   215*,   230,  pl. 

35 

Dusenii,  213,  216,  226,  227 

elephas,  219,  228,  258,  pl.  27 

emarginata,  217,  218,  219,  222, 

224,  267,  pl.  20.  21,  2S 

Endresii,  213,  226 

equiseticaulis,  259 

exoleta,  216,  217,  218,  219,  222, 

223,  224,  pl-  21,  26,  27 

fimbriata,  215 

tlexuosa,    220,    223,    237,    238 

249,  254,  268,  pl.  20 

gibba,  222,  224,  227,  230,  244, 

245,  252,  253*.  257,  pl.  21,  24,  2S, 
26,  2Q,  37,  3S 

Gibbseae,  pl.  31 


globulariaefolia,  213,  232,  257, 

pl.  28 

■ Hamiltonii,  pl.  35 

Holzii,  pl.  35 

■ Hookeri,  95,  218,  229,  230,  257, 

261,  pl.  34 

Humboldtii,  213,  226 

intlata,  2:0,  221,  223 

intermedia,  225,  pl.  20,  21,  25 

Kirkii,  232,  260,  pl.  33 

lasiocaulis,  pl.  35 

lateriflora,  232,  256,  260,  pl.  20, 

Lloydii,  232,  257,  pl.  28 

longiciliata,  231,  232,  260,  pl. 

33 
■ longifolia,  213,  218,  226,  227, 

257,  pl-  26 
Menziesii,  60,  95,  229,  230,  231, 

261,  pl.  20,  23,  35 
minor,  214,  223,  224,  225,  242, 

245,  268,  pl.  21 

mixta,  222,  223 

monanthos,  215,  217,  218,  229, 

230,  254,  256,  257,  261,  pl.  22,  23, 

24,  34,  35 

montana,  219,  226,  227 

Moorei,  pl.  35 

multi  aulis,  232,  260,  pl.  32 

nana,  232,  246,  257,  pl.  28 

■  nelumbifolia,    213,     217,     219, 

226 

neottioides,  217,  226,  257,  pl- 

26.  27 

ochroleuca,  225 

ogmosperma,  259 

• oligosperma,  216,  218,  220,  222, 

223,  233,  246,  pl.  21,  23 
olivacea.  227 

orbiculata,  215,  216,  217,  225, 

231,  232,  260,  pl.  22,  32 
paradoxa,  225,  pl.  21 

peltata,  232,  259,  pl.  25,  29 

■ purpurea,   214,  215,  216,  219, 

221*,   227,    228,   229,235,238,241, 

257,  258,  269,  pl.  20,26,27,  29,  37 

radiata,  220 

Rendlei,  226 

reniformis,  213,  216,  217,  219, 

226,  227,  257,  pl.  21 

resupinala,  216,  225,  226,  268, 

pl.  23,  27 

■ rigida,  216,  226 

■ rosea,  231,  260,  pl.  22,  31 

simnlex,   213,    231,    232,   260, 

pl-  23 

Singeriana,  pl.  35 

stellaris,  220,  221,  223,  pl.  20 

Stephensae,  214,  224,  pl.  23 

striatula,  232,  pl.  32 

subulata,  215,   216,   226,   231, 

232,  257 

Thonningii,  220 

tubulata,   215,   2ig,   229,   230, 

261,  pl.  33,  36 

violacea,  218,  229,  230 

volubilis,   229,   230,   231,   261, 

pl.  20,  23,  34 

vulgaris,  94,  213,  215,  216,  217, 

218,  2ig,  220,  221,  222,  223,  224, 
22s,  226,  227,  233,  235*,  237.  241. 
242,  243,  244,  245,  249,  254.  255  . 
257,  26s,  267,  268,  269,  270,  pl. 
20,  21,  23,  26,  2g,  37 

americana,  246 

Wallichiana,  pl.  35 

Warburgii,  231,  260 

Welwitschii,  60,  256,  259,  pl. 

24,  31 
Utriculariaceae,  269 
Utriculariae,  215 

VaCCINIUM  OXYCOCCUS,   IIS 
WllHELMINA  NEPENTHICOLA,  83 

Wyeomyia  Smithii,  36 

Zizanta,  2og 
Zoopagaceae,  175 
Zoopage  phanera,  174 
Zoophagus,  4.  175 

■ insidians,  17c*,  171,  i73,  i75. 

176 


AUTHOR    INDEX 


Abderhalden,  71,  7g,  159 

Adowa,  A.  N.,  264,  267 

Akerman,    A.,    127,    129,    148,    149, 

150,  151,  153,  155,  i6i,  165,  pi.  17 
Aldrovandi,  U.,  195 
Amadei,  C,  195 
Ames,  M.  E.  P.,  49 
Ames,  O.,  133,  165 
Anderson,  L.  E.,  30 
Arber,  A.,  id,  16,  23,  38,  49,  6o,  62, 

79,  82,  83,  85,  89 
Arisz,  W.  H.,  129,  165 
Armit,  W.  E.,  229 
Arnaudow,  N.,  173,  175 
Arnold,  W.,  119 
Asenjo,  C.  F.,  36,  38 
Ashida,  Joji,  186,  189,  19^1,  192,  193, 

194,  195,  197,  201,  202,  203,  204, 

205,  206,  207,  208,  209,  210,  211, 

212,  pi.  18,  IQ 
Aso,  R.,  HI,  114,  264 
Austin,  R.  M.  L.,  36,  48,  49 

Baas  Becking,  L.  G.  M.,  69,  75, 

78,  161 

Baillon,  H.,  30,  38,  59 
Balfour,  T.  A.  G.,  194,  210 
Barnhart,  J.  H.,  49,   53,   215,   228, 

231,  267 
Barrett,  C,  96 
Bartram,  Ch.,  18 
Bartram,  J.,  178 
Bartram,  Wm.,  18,  32,  38 
Batalin,  A.,  21,  32,  38,  46,  48,  49, 

106,  log,  114,  142,  159,  165,  188, 

189,  19:1,  191,  193,  210 
Bath,  W.,  267 
Beck,  A.  B.,  165,  167 
Behre,  K.,  130,  131,  132,  133,  134, 

138,  14.3.  145,  164,  165,  pl.  16 
Beijerinck,  M.  VV.,  131,  165 
Benecke,  W.,  147,  165,  167 
Benjamin,  L.,  90,  94,  234,  243,  248, 

267 
Bennett,  A.  W.,  165 
Bentham,  G.,  9,  10,  14,  16,  95,  262 
Berger,  J.,  36,  38 
Bischoflt,  G.  W.,  53,  79 
Bobisut,  O.,  66,  67,  68,  79 
Bok,  R.,  69 
Bokorny,    T.,    129,    147,    148,    151, 

153,  166 
Bower,  F.  O.,  53,  54,  57,  59,  60,  62, 

79,  80,  */.  7 
Brackenridge,  J.  D.,  40,  49 
Brass,  L.  J.,  229 

Braun,  A.,  49 

Brocher,  F.,  233,  235,  236,  237,  238, 

239,  240,  241,  242,  243,  244,  246, 

267 
Brongniart,  A.  T.,  64,  79 
Brough,  P.,  131,  pl.  16 
Broussonet,  P.  M.  A.,  186,  210 
Brown,  R.,  81,  89 
Brown,  W.  H.,  6,  186,  187,  188,  190, 

191,  192,  193,  201,  205,  210 
Bruce,  A.  N.,  97,  98 
Bruecke,  189 
Brug,  S.  L.,  80 
Brumpt,  E.,  267 
Buchenau,   F.,   221,    222,   223,   224, 

267 
Budde,  E.,  175 
Bunning,  E.,  206,  212 
Biisgen,  M.,  89,  162,  163,  166,  236, 

247,  248,  249,  264,  267 
Buller,  A.  H.  R.,  68,  92,  94,  131 
Burbidge,  F.  W.  T.,  52,  58,  59,  79 
Burdon-Sanderson,  J.,  186,  187,  188, 

189,  19^,  205,  210,  211 
Burnett,  G.  T.,  18,  38 
Buscaglione,  5,  8,  209,  211,  268 
Buzacott,  J.  H.,  252,  pl.  20 

Canby,  W.  M.,  38,  45,  49,  177,  180, 
210,  211 


CandoUe,  A.  P.  de,  59,  79,  138,  166, 

215,  234,  267 
Candolle,  C.  P.  de,  60,  79,  182,  189, 

210 
Carry,  T.  H.,  4,  8 
Caruel,  T.,  7 
Caspary,    R.,    195,    196,    197,    199, 

210 
Catalan,  M.,  179 
Catesby,  M.,  18,  39 
Chandler,  B.,  267 
Chenon,  L.  J.,  195 
China,  W.  R.,  98 
Christy,  M.,  4,  8 
Clairville,  J.  P.  de,  234 
Clarke,  W.  G.,  267 
Clausen,  J.,  112,  113 
Clautriau,  G.,  73,  75,  79 
Clusius,  C,  18 
Coelingh,  W.  M.,  127,  134,  149,  150, 

151,  156,  166 
Cohn,  F.,   19s,   196,  199,  201,  209, 

210,  21-',  234,  235,  236,  239,  243, 

246,  249,  259,  264,  266,  267 
Coker,  W.  C,  210,  212 
CoUa,  S.,  112,  114 
Collinson,  P.,  18,  32,  39,  178,  210 
Commelin,  J.,  51 
Compton,  R.  H.,  216,  260,  267 
Correns,  C,  116,  166 
Couch,  J.  N.,  170,  175 
Couvreur,  71,  72,  79 
Cramer,  C.,  8,  209,  210,  211 
Crouan,  234,  267 
Curry,  D.  P.,  267 
Curtis,  M.  A.,  177,  178,    180,    184, 

186,  188,  210 
Curtis.  W..  79,  180,  210 

Czaja,  A.  T.,  116,  127,  166,  197, 
201,  205,  206,  207,  208,  209,  210, 
236,  239,  240,  241,  243,  244,  246, 
249,  251,  253,  267.  268 

Czapek,  F.,  79,  112,  114 

Dakin,  W.  J.,  84,  87,  88,  89 

Danser,  B.  H.,  51,  55,  57,  58,  65, 
78,  79 

Darlington,  W.,  40 

Darwin,  C,  5,  7,  8,  32,  39,  49,  69, 
70,  90,  92,  94,  97,  99,  100,  lOI, 
102,  103,  105,  106,  107,  108,  109, 
110,  III,  112,  113,  114,  115,  118. 

120,    121,    122,    125,    126,    127,    128, 

129,  136,  139,  140,  141,  142,  143, 
145,  146,  147,  148,  149,  ISO,  ISI. 
153,  155.  156,  158,  159,  161,  162. 
166,  177,  180,  1S2,  183,   1S4,  186, 

187,  188,  i8g,  190,  191,  193,  194, 
195,  199,  200,  208,  209,  210,  211, 
234,  235,  236,  243,  244,  245,  246, 
248,  250,   259,  264,   266,   268 

Darwin,  E.,  118,  135.  166,  168,  179, 

180,  210 
Darwin,  F.,  4,  8,  Sg,  90,  112,   146, 

147,  162,  163,  166,  193,  210 
Dean,  B.,  214,  243,  268 
Delpino,  F.,  5,  6 
Dernby,  K.  G.,  iii,  113,  114,  159, 

161,  162,  166 
Dewevre,  A.,  100,  loi,  103,  105 
Dickson,  A.,  52,  53,  59,  61,  62,  64, 

66,  79,  81,  82,  83,  84,  85,  87,  88, 

89 
Diderot,  D,,  179,  210 
Diels,  L.,  96,  98,  117,  n8,  120,  130, 

164,  166,  210 
Dillon,  J.  J.,  195 
Dillwyn,  L.  W.,  178,  210 
Dixon,  H.  H.,  133,  166,  224 
Dobbs,  A.,  178 
Domin,  K.,  95,  98 
Dover,  C,  77,  79 
Drechsler,   C,    170,    171,    173,    174, 

175 
Drude,  O.,  8,  166,  268 
Dubois,  R.,  71,  72,  79,  159,  166 


Duchartre,  P.  E.,  30,  39 
Dufrenoy,  J.,  152,  153,  155,  166 
Duval-Jouve,  J.,  65,   79,   195,   200, 
21C 

Ebstein,  70 

Edwards,  H.,  35,  40,  45,  48,  49 

Edwards,  S.,  180 

Eichler,  A.  W.,  82,  89 

Ekambaram,  T.,  237,  238,  240,  241, 

243,  248,  249,  250,  268 
Ellis,   J.,    138.    177,    178,    179,    183, 

186,  210,  211 
Emerson,  7 
Engel,  E.  O.,  So 
Engler,  A.,  7,  8g 
d'Entrecasteau,  81 

Faivre,  E.,  59,  79 
Fenner,   C.  A.,   15,   16,   21,   22,   23, 
33,  39,  65,  73,  74,  79,  96,  97,  98, 

99,  loi,  102,  104,  105,  107,  108, 
109,  114,  117,  120,  121,  122,  123, 
124,  125,  126,  127,  129,  166,  195, 
196,  197,  199,  200,  205,  209,  211 

Fermi,  C,  5,  8,  209,  211,  268 

Fernald,  M.  L.,  226,  268 

Fernandes.  A.,  105 

Flacourt,  E.  de,  51 

Franca,  C,  8,  99,  100,  103,  104,  105, 

122,  155,  166,  214,  243,  268 
Frankland,  166 
Fraustadt,  A.,  182,  194,  211 
Fresenius,  169.  175 
Fry,  R.  E.,  254 

Gardiner,  W.,  122,  146,  147,  148, 
149,  151,  153.  157,  i66.  211 

Gardner,  C.  A.,  81,  89 

Gardner,  G.,  213,  226,  268 

Gardom,  135,  136 

Gates,  F.  C,  268 

Geddes,  P.,  113,  114,  136,  166,  268 

Geitler,  L.,  175 

Gerard,  J.,  4,  18 

Gibbs,  R.  D.,  268 

Gicklhorn,  J.,  170,  172,  173,  175,  176 

Giesenhagen,  254 

Giessler,  A.,  119,  166 

Gilburt,  W.  H.,  65,  79,  89 

Girard,  F.  de,  94 

Gislen,  T.,  247,  26S 

Glauer,  147,  166 

Gleason,  H.  A.,  9,  12,  13,  16 

Gluck,  H.,  223,  224,  225,  268 

Goebel,  K.,  3,  6,  7,  8,  9,  to,  11,  14, 
15,  16,  19,  22,  23,  26,  29,  30,  31, 
32,  il,  39,  40,  42,  43,  45,  46,  47, 
48,  49,  52,  53,  54,  55.  59,  60,  61, 
62,  66,  68,  71,  72,  73,  76,  79,  80, 
82,83,86,  87,88,89,90,91,92,94, 

100,  loi,  102,  103,  105,  106,  107, 
108,  109,  110,  III,  113,  114,  116, 
117,  118,  122,  124,  127,  130,  131, 
134,  139,  147,  148,  151,  153,  154, 
162,  163,  164,  166,  177,  180,  181, 
182,  184,  185,  188,  194,  195,  196, 
199,  200,  201,  211,  217,  218,  219, 
220,  222,  223,  224,  225,  226,  227, 
228,  231,  232,  234,  235,  243,  245, 
246,  247,  254,  259,  260,  262,  263, 
264,  268,  pl.  2,  J,  6,  16 

Gorup-Besanez,  E.  von,  69,  70,  79, 

HO,  114 
Graves,  J.  A.,  133,  166 
Gray,  A.,  30,  39,  48,  49,  136,  235 
Green,  J.  R,,  71,  79,  107,  114,  161, 

166 
Gressner,  H.,  107,  114 
Grimm,  H,  N.,  72,  79 
Grisebach,  H.  R.  A.,  94,  227 
Gronland,  J.,  120,  121,  122,  166 
Grout,  A.  J.,  133,  166 
Gruetzner,  70 
Guenther,  79 
Gurney,  R.,  267,  268 


Francis  E.  Lloyd 


—  351  — 


Carnivorous  Plants 


Gustafsson,  0.,  112 

Guttenberg,  H.  von,  182,  188,  igi, 

192,  211,  212 

Haas,  Th.  P.,  pi.  g 
Haberlandt,  G.,  66,  68,  73,  79,  io4, 
122,  124,  163,  166,  182,  185,  188, 

193,  I95i  200,  211 
Hada,  Y.,  241,  265,  268 
Haidenhain,  70,  71 

Hamilton,  A.  G.,  82,  83,  84,  85,  86, 

87.  89,  98 
Harshberger,  J.  W.,  99.  lOS 
Hausleutner,  209,  211 
Hayne,  F.  G.,  138,  166 
Hegner,  R.  W.,  39,   24°.   241,   265, 

268 
Heide,  F.,  58,  62,  64,  79 
Heinricher,  E.,  79,  116,  166,  211 
Hepburn,  J.  S.,  23,  ^t,,  34,  35,  36, 

38,  39,  48,  49,  74.  76,  77,  79 
Hermann,  P.,  51 
Higley,  32,  39 
Hildebrand,  6 
Hoehne,  F.  C,  90,  227,  268 
Holm,  T.,  181,  211 
Holier,  H.,  160,  167 
Homes,  M.  V.  L.,  105,  120,  122,  123, 

124,  125,  136,  151,  152,  153,  154, 

155.  157.  166,  p\.  16 
Hooker,  H.  D.,  Jr.,  121,  142,   143. 

144,  166 
Hooker,  J.  D.,  5,  8,  13,  18,  19,  20, 

21,  23,  32,  39,  42,  49,  52,  S3,  54, 

55.  57,  58,  59.  61,  62,  63,  64,  66, 

68,  69,  79,  13s,  136,  166,  179.  211. 

212,  pi.  7 
Hornemann,  J.  W..  113,  114 
Hovelacque,  M.,  107,  114,  226,  243, 

268 
Huie,  L.  M.,  120,  121,  122,  125,  127, 

151,  157,  166 
Hunt,  J.  G.,  64,  80 

Im  Thurn,  E.  F.,  9,  16,  226,  268 
Irmisch,  T.,  222,  223,  268 

Jane,  F.  W.,  217,  218,  268 

Janse,  163,  167 

Janson,  E.,  119,  129,  148,  151,  167 

Janti,  J.  V.  de,  8o 

Jensen,  H.,  76,  77,  80 

Johnson,  Th.,  18 

Jones,  F.  M.,  8,  a,  36,  37,  38,  39, 

45,  48,  49,  77,  79,  178,  183,  184, 

188,  211,  pi.  4 
Jost,  L.,  147,  165,  167 

Kamienski,  F.,  213,  214,  218,  227, 

228,  268 
Keck,  K.,  49 

Kellermann,  C,  162,  163,  167 
Kiesel,  A.,  265,  268 
Killip.  E.  F.,  16 
Kirschleger,  M.,  131,  167 
Klein.  J.,  114 

Knoll,  F.,  66,  67,  68,  69,  80 
Kny,  L.,  66,  80 
Kok,  A.  C.  A.,  127,  128,  167 
Konig,  C,  180 
Konopka,   K.,    123,   124,    125,    126, 

127,  136,  157,  158,  167 
KonsuloS,  S.,  176 
Korthals,  P.  W.,  51,  53,  64,  80 
Korzschinski,  S.,  195,  196,  211 
Kostytschew,  S.,  119,  167,  194,  211 
Krafft,  S.,  9,  II,  14,  15,  16,  39,  pi.  2 
Kramer,  W.  de,  75,  76 
Kruck,  M.,  127,  152,  167,  239,  240, 
_  241,  243,  244,  24s,  268 
Kuhlmann,  J.  G.,  268 
Kupper,  W.,  67 
Kurtz,  F.,  40,  42,  43,  49,  182,  211 

Labbe,  E.,  160,  167 

La  Billardiere,  J.  J.  Houton  de,  81 

Lambert,  G.,  33,  39 

Lang,  F.  X.,  95,  96,  98,  216,  262, 

263,  268 
Lassus,  A.  de,  201,  211 
Leavitt,  R.  G.,  130,  131,  132,  133, 

167 
Lehmann,  215 
Lemmon,  J.  G.,  42,  45,  49 


Linderstr0m-Lang,  160,  167 

Lindley,  J.,  30,  39,  183,  211 

Lindman,  C.  A.  M.,  112,  114 

Linnaeus,  C.,  17,  18,  32,  39,  112, 
1,58.  178,  179,  19s,  210,  211 

Lipman,  180 

Lloyd,  F.  E.,  s.  8,  9.  10,  13.  16,  78, 
80,  87,  89,  95,  98,  211,  214,  216, 
218,  229,  233,  238,  240,  241,  243, 
251,  254,  256,  257,  258,  259,  260, 
268,  269 

rObel,  M.  de,  17 

Loew,  O.,  Ill,  114,  119,  148,  264 

Loureiro,  J.,  52 

Lubbock,  J.,  130,  167 

Ludlow,  pi.  32 

Ludwig,  F.,  6,  8 

Luetzelburg,  P.  von,  226,  228,  234, 
235,  243,  258,  264,  265,  269 

Macbeth,  A.  K.,  Jr.,  131,  165,  167 

Macbride,  J.,  18,  19,  32,  39,  49,  66, 
80 

McClosky,  47 

MacDougal,  D.  T.,  19,  21,  22,  39, 
163,  167,  206,  211 

Macfarlane,  J.  M.,  9,  10,  16,  19,  20, 
24,  25,  28,  30,  39,  41,  42.  43.  45, 
49,  52,  53,  55.  56.  57,  59,  60,  61 
62,  64,  65,  66,  68,  74,  79,  80,  183, 
185,  186,  187,  188,  190,  191,  192, 
211,  pi.  7 

McGee,  J.  M.,  168 

McLean,  R.  C,  113,  114 

Macnamara,  C,  pi.  i 

Mangin,  L.,  65,  80 

Marloth,  R.,  117,  167 

Marshall,  W.,  108 

Massart,  J.,  163,  167 

Matheson,  R.,  214,  251,  269 

Maury,  P.,  89 

Mayr,  F.  X.,  244,  269 

Meehan,  210 

Meierhofer,  H.,  220,  235,  243,  245, 
249,  250,  269 

Mellichamp,  J.  H.,   17,   19,  26,  32, 

39,  49 
Menzel,  R.,  80 
Menzies,  A.,  81 
Merl,  E.,   127,   201,   216,  217,   218, 

219,  237,  238,  239,  240,  241,  243, 

249,  260,  269 
Merz,  M.,  216,  217,  269 
Metzner,  P.,  206,  211 
Meyen,  F.  J.  F.,  64,  80,   121,   138, 

167,  180,  187,  188,  211,  234,  269 
Meyer,  A.,  100,  loi,  103,  105 
Meyer,  F.  J.,  244,  269 
Milde,  J.,  138,  167 
Mirande,  R.,  172,  176 
MirimanoEf,  A.,   iii,   112,  114,  167 
Mohnike,  72,  80 
Monti,  G.,  19s,  197,  201,  211 
Mori,  A.,  200,  201,  211 
Morison,  R.,  18 
Morren,  Ch.,  30,  39,  60,  80 
Morren,  E.,  5,   no,   114,   159,   167, 

179,  210,  269 
Morrison,  A.,  130,  167 
Mosely,  H.  N..  269 
Moulaert,  B.,  133,  167 
von  Mueller,  229,  230 
Munk,  H.,  185,  186,  187,  188,  189, 

211 

Naudin,  M.,  121,  131,  167 

Neubauer,  M.,  165,  167 

Nicolosi-Roncati,  F.,  no,  114 

Niel,  C.  B.  van,  120 

Nitschke,  T.,  115,  116,  118,  120,  122, 
125,  127,  130,  131,  136,  138,  139, 
140,  141,  142,  167,  196,  211 

Nold,  R.  H.,  127,  241,  242,  243,  244, 
269 

Dels.  W..  167 

Okahara,   K.,   159,   160,    161,    162, 

167,  168 
Oliver,  D.,  16,  268,  269 
Olivet,  R.,  112,  114 
Olsen-Sopp,  113 
Gosterhuis,  J.,  164,  165,  16S 
Oppenheimer,  C.,  112,  114,  269 
Osborn,  C.  S.,  8 


Oudemans,  C.  A.  J.  A.,  55,  64,  65, 
66,  80,  177,  180,  182,  184,  187, 
194,  211 

Oudman,  J.,  127,  128,  129,  165,  168 

Oye,  P.  van,  80 

Page,  210 

Peberdy,  H.,  pi.  38 

Peirce,  J.  G.,  7,  8 

Penzig,  O.,  100,  loi,  105,  120 

Peyronel.  B.,  164.  168 

Pfeffer,  W.,  2,  8,  112,  127,  141,  146, 

163.  164,  168,  194,  209,  211 
Planchon,  J.-E.,  8,  95,  98 
Plukenet,  L.,  196,  211 
Porsild.  M.  P..  269 
Prantl,  H.,  7,  89 
Prat,  S.,  240,  269 
Price,  J.  R.,  131,  167 
Pringsheim,  N.,  218,  220,  222,  223, 

224,  269 

QUINTANILHA,  A.,  99,  102,  IO4,  10$, 
152,   153,   168,  pi.   13 

Raumer,  E.  von,  162,  163,  167 
Rees,  M.,  70,  80,  no,  114,  159,  168, 

194,  211 
Regel,  E.,  163,  168 
Rennerfelt,  E.,  176 
Rennie,  E.  D.,  130,  168 
Ridley,  H.  N.,  269 
Riley,  C.  v.,  38,  39 
Robinson,  Heath,  267 
Robinson,  \V.  J.,  a,  34,  39,  76,  80, 

132,  133.  141,  159.  168 
Roeper,  J.,  166 
Rosenberg,  O.,   126,   127,   128,   157, 

158,  168 
Ross,  H.,  9=;.  gS 
Rossbach,  G.  B.,  269 
Roth,  A.  \V.,  135,  138,  168 
Roxburgh,  195 
Ruiter,  C.  de,  58,  80 
Rumphius,  G.  E.,  77,  78 
Ruschmann,  G.,  127,  164,  168 

S.\CHS,  J.,  55 

Saint-Hilaire,  A.  de,  30,  39,  90,  94, 

269 
St.  John,  E.  Q.,  33,  35.  39.  48,  49. 

79 
Salisbur>',  133 
Sarrazin,  M.  S.,  17,  18 
Scarth,  G.  W.,  207,  211 
Schacht,  121 
Schenck,  H.,  269 
Schenk,  A.,  8,  166,  209,  211,  268 
Scherffel,  A.,  176 
Schikora,  F.,  176 
Schimper,  A.  F.  W.,  32,  33,  39,  146, 

148,  150,  151,  153,  168,  231,  245, 

258,  259,  269 
Schleiden,  M.  J.,  234 
Schhcht,  163,  168 
Schmid,  G.,  117,  118,  119,  126,  130, 

141,  142.  162,  164,  168,  186 
Schmitz,  P.  H.  S.  J.,  80 
de  Schoenfelt,  210 
Schomburgk,  R.,  9,  16 
Schwartz,  O.,  269 
Sharp,  L.  W.,  187,  188,  201,  210 
Sherreff,  pi.  32 
Shocotyoff,  162 
Silberschmidt,  K.,  206,  211 
Simms,  G.  E..  269 
Simpson,  pi.  33 
Sims,  J.,  52,  80,  178,  180,  211 
Skutch,  A.  F.,  270 
Small,  J.,  120,  137,  140,  168 
Smith,  18,  39 
Smith,  C.  M.,   177.   181,   195,   196, 

211,  pi.  17 
Smith,  W.  \V.,  9 
Sorensen,  74 
Solander,  D.,  178 
Solereder,    H.,    99.    105,    118,    168, 

182,  212 
SommerstorEf,    H.,    171,    172,    173, 

176 
Sparrow,  F.  K.,  173,  176 
Spoehr,  H.  A.,  119,  168 
Starke,  A.,  80 
Stahl,  E.,  163,  164,  167,  168 


Index  of 


—  352 


Personal  Names 


Stapf,  O.,  226,  232,  233,  260,  270 

Steckbeck,  D.  W.,  19,  39 

Stedman,  H.,  98 

Stein,  B.,  201,  212 

Stephens,  E.  L.,  116,  168,  195,  213, 

254,  270 
Stern,  52,  53,  55,  56,  61,  62,  65,  68, 

71,  74.  75,  80,  206,  212,  pi.  7 
Storer,  T.  I.,  6 
Stutzer,  M.  J.,  160,  168,  265,  270 


9,  10,  II,   12,   13, 


Tait,  W.  C,  99 
Tate,  G.  H.  H., 

pi.  I 

Tate,  L,,  70,  8c,  88,  89,  159,  168 
Taylor,  pi.  32 
Temminck,  C.  J.,  80 
Teruuchi,  71,  79 
Thienemann,  A.,  77,  78,  80 
Thompson,  G.  M.,  270 
Thomson,  R.  B.,  132 
Thomson,  T.,  195.  212 
Tieghem,  Th.  van,  234,  270,  pi.  21 
Tischutkin,  N.,  71,  72,  80,  no,  in, 

112,  114,  159,  168 
Topp,  C.  A.,  270 
Torrey,  J.,  40,  42,  43,  3° 
Tournefort,  17,  18 
Tradescant,  J.,  18 
Treat,  M.,  168,  234,  235,  264,  270 
Trecul,   A.,   65,   80,   120,   121,    122, 

136,  138,  168 
Treviranus,  C.  L.,  64,  80,  138,  16S, 

234,  270 


Troili-Petersson,  113 

Troll,  W.,  II,  16,  19,  20,  30,  31,  32, 
38,  39,  41,  43,  46,  47,  50,  51,  52, 
53,  56,  59,  60,  61,  62,  63,  79,  80, 
81,  83,  89,  168,  196,  212 

Turner,  W.,  4 

Tutin.  T.  G.,  94 

Ule,  E.,  213,  270 
linger,  F.,  65 

Uphof,  J.  C.  Th.,  17,  23,  39,  270, 
pi.  I 

Valkonov,  A.,  176 

Vickery,  J.  W.,  130,  132,  133,  134, 

168,  pi.  16 
Vines,  S.  H.,  70,  71,  72,  73,  80 
Voelker,  A.,  69,  80 
Vogl,  A.,  19,  39,  so 
Vouk,  v.,  80 
Vries,  H.  de,  146,  147,  148,  149,  151, 

153,  168 

Walcott,  M.  v.,  38,  39 

Wallace,  A.  R.,  72,  76 

Warming,  E.,  90,  94,  120,  122,  168, 

216,  217,  218,  228,  230,  270 
Weber,  Fr.,  137,  165,  168 
Wehrle,  E.,  242.  270 
Wells,  B.  R.,  268 
Went,  F.  W.,  224,  252 
Weyland,  H.,  164,  168 
Whately,  135,  136.  168 
Wherry,  E.  T.,  17,  23,  35,  39 


White,  J.,  IS9,  168 

Wilkes,  40 

Will,  H.,  69,  70,  79,  80,  no,  114, 

159,  168,  194,  211 
von  Wilier,  114 
Wilson,  V\'.  P.,  26,  39 
Wilstatter,  119 
Winkler,  H.,  132,  135,  168 
Winzor,  F.  L.,  131,  165,  167,  168 
Withering.   136 
Withycombe,  C.  L.,  237,  238,  240, 

241,  242,  243,  270 
Wolf,  F.  A.,  30 
WoUny,  E.,  116.  168 
Woolls,  W.,  83,  89 
Woronin,  169 
Wright,  C,  90,  9+,  227 
Wunschmann,   E.,   51,   59,   66,    79, 

80 
Wylie,  R.  B.,  216,  270 

YocoM,  A.  E.,  216,  270 
Young,  R.  G.  N.,  256,  pi.  21 
Young,  W.,  178,  179,  212 

Zacharias,  E.,  80 

Zeeuw,  J.  de,  66,  68,  75,  76,  80,  161 

Ziegenspeck,  H.,  127,  157,  167,  188, 

189,  192,  212 
Zimmermann,  A.,  66,  80 
Zipperer,  P.,  9,   16,  19,  22,  28,  32, 

a,  34,  39 
Zopf,  W.,  169,  171,  17s,  176