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READINGS  IN 
MAMMALOGY 


J.  Knox  Jones,  Jr. 
Sydney  Anderson 


Museum  of  Natural  History 

The  University  of  Kansas 

19  70 


HARVARD    UNIVERSITY 

Library  of  the 

Museum  of 

Comparative  Zoology 

Gift  of  E.   E.   Williams 


Readings  In  Mammalogy 


Selected  from  the  original  literature 
and  introduced  with  comments  by 


J.  Knox  Jones,  Jr. 

The  University  of  Kansas,  Lawrence 


AND 


Sydney  Anderson 

The  American  Museum  of  Natural  History,  New  York  City 


/SCi  Z.  .-  Ke  '      .\oa 


Qt. 


:-v 


'  1  ('  nus  I  ■\' 


Monograph  No.  2 

Museum  of  Natural  History 

The  University  of  Kansas 

1970 


Monograph  No.  2 

Museum  of  Natural  History,  The  University  of  Kansas 

ix-{-586  pp.,  1970 


Lawrence  •   Kansas 


MUS.  COMP.  ZOOL" 
LIBRARY 

MAR  12 1980 

HARVARD     , 
UNIVERSITY      ' 


PRINTED  BY 
THE  XJNIVERSITY  OF  KANSAS  PRINTING  SERVICE 


PREFACE 

This  anthology  is  intended  as  an  introduction  to  the  study  of  mammals, 
principally  for  those  who  already  have  some  biological  background  and  who 
want  to  know  the  general  scope  of  the  field  of  mammalogy.  The  subdisciplines 
or  specialties  of  mammalog>%  its  relationship  to  other  biological  fields,  and 
specific  examples  of  the  type  of  work  done  by  mammalogists  are  here  intro- 
duced by  means  of  a  selection  of  complete  papers  in  their  original  form.  We 
hope  that  these  will  help  college  students  looking  forward  to  graduate  work  in 
biology  obtain  a  realistic  general  view  of  mammalogy  as  a  possible  specialty. 
Also,  beginning  graduate  students  in  related  disciplines  such  as  ornithology, 
mammahan  physiology,  or  ecology,  or  undergraduate  majors  in  wildlife  man- 
agement, may  find  their  perspectives  broadened  by  perusal  of  the  present 
selection  of  papers  and  the  introductory  commentaries. 

The  published  literature  on  the  scientific  study  of  mammals,  which,  broadly 
speaking,  comprises  the  field  of  mammalogy,  includes  about  90,000  separate 
papers,  and  new  papers  are  now  being  published  at  the  rate  of  5000  to  6000 
each  year,  the  actual  number  depending  on  where  one  draws  the  borders  of 
the  discipline.  Precise  borders  do  not  exist.  Mammalogy,  like  other  scientific 
fields,  draws  from  and  contributes  to  various  areas  of  human  knowledge.  Our 
selection  of  the  64  papers  here  reproduced  was  influenced  by :  ( 1 )  our  con- 
cept of  the  scope  of  mammalogy  and  of  a  reasonable  and  representative  bal- 
ance of  its  parts  at  this  time;  (2)  our  desire  to  illustrate  various  ways  in  which 
a  wide  variety  of  information  can  be  presented  in  published  form;  and  (3) 
our  awareness  that  most  of  our  readers  will  be  English-speaking  Americans, 
which  led  us  to  use  articles  published  in  English  and  selected  predominantly 
from  American  sources.  Nevertheless,  we  judge  that  the  broad  sweep  of 
concepts  and  methods  portrayed  is  relevant  to  students  of  mammalogy  in  all 
parts  of  the  world.  We  have  selected  short  papers,  in  general  less  than  20  pages 
in  length,  in  preference  to  either  longer  papers  or  excerpts  therefrom — chiefly 
because  of  space,  but  also  because  we  want  the  serious  student,  who  may  later 
contribute  to  the  literature  himself,  to  see  each  published  work  in  its  entirety 
as  one  tangible  contribution  to  knowledge.  He  can  then  grasp  its  concept,  its 
methodology,  its  organization,  its  presentation,  its  conclusions,  and  perhaps 
even  its  limitations.  On  the  latter  score  we  would  note  that,  although  we  think 
the  papers  selected  are  worthy  contributions  and  make  the  points  we  wish  to 
emphasize,  we  do  not  pretend  to  have  selected  the  finest  papers  ever  published. 
We  could  have  used  a  somewhat  different  selection  to  serve  much  the  same 
purpose,  and  we  are  sure  someone  else  would  use  a  different  selection  to 
represent  his  views  of  mammalogy. 

Although  many  college  and  university  libraries  have  some  or  most  of  the 
journals  and  other  sources  from  which  papers  were  selected,  we  decided  an 
anthology  was  warranted  for  those  who  want  an  overview  of  the  field,  who 
may  not  know  where  to  find  the  relevant  literature,  or  who  want  the  conve- 
nience of  a  collection  of  separate  papers.  Many  undergraduate  students  are 
largely  unaware  of  the  existence  of,  or  the  nature  of,  the  technical  literature 
of  science,  although  their  textbooks  are  replete  with  terminal  citations.   Hope- 


Monograph  No.  2 

Museum  of  Natural  History,  The  University  of  Kansas 

ix-\-586  pp.,  1970 


Lawrence  •  Kansas 


MUS.  COMP.  ZOOU 
LIBRARY 

MAR  12  1980 

HARVARD 
UNIVERSITY      ' 


PRINTED  BY 
THE  tJNIVERSITY  OF  KANSAS  PRINTING  SERVICE 


PREFACE 

This  anthology  is  intended  as  an  introduction  to  the  study  of  mammals, 
principally  for  those  who  already  have  some  biological  background  and  who 
want  to  know  the  general  scope  of  the  field  of  mammalogy.  The  subdisciplines 
or  specialties  of  mammalogy^  its  relationship  to  other  biological  fields,  and 
specific  examples  of  the  type  of  work  done  by  mammalogists  are  here  intro- 
duced by  means  of  a  selection  of  complete  papers  in  their  original  form.  We 
hope  that  these  will  help  college  students  looking  forward  to  graduate  work  in 
biology  obtain  a  realistic  general  view  of  mammalogy  as  a  possible  specialty. 
Also,  beginning  graduate  students  in  related  disciplines  such  as  ornithology, 
mammalian  physiology,  or  ecology,  or  undergraduate  majors  in  wildlife  man- 
agement, may  find  their  perspectives  broadened  by  perusal  of  the  present 
selection  of  papers  and  the  introductory  commentaries. 

The  published  literature  on  the  scientific  study  of  mammals,  which,  broadly 
speaking,  comprises  the  field  of  mammalogy,  includes  about  90,000  separate 
papers,  and  new  papers  are  now  being  published  at  the  rate  of  5000  to  6000 
each  year,  the  actual  number  depending  on  where  one  draws  the  borders  of 
the  discipline.  Precise  borders  do  not  exist.  Mammalogy,  like  other  scientific 
fields,  draws  from  and  contributes  to  various  areas  of  human  knowledge.  Our 
selection  of  the  64  papers  here  reproduced  was  influenced  by:  (1)  our  con- 
cept of  the  scope  of  mammalogy  and  of  a  reasonable  and  representative  bal- 
ance of  its  parts  at  this  time;  (2)  our  desire  to  illustrate  various  ways  in  which 
a  wide  variety  of  information  can  be  presented  in  published  form;  and  (3) 
our  awareness  that  most  of  our  readers  will  be  English-speaking  Americans, 
which  led  us  to  use  articles  published  in  English  and  selected  predominantly 
from  American  sources.  Nevertheless,  we  judge  that  the  broad  sweep  of 
concepts  and  methods  portrayed  is  relevant  to  students  of  mammalogy  in  all 
parts  of  the  world.  We  have  selected  short  papers,  in  general  less  than  20  pages 
in  length,  in  preference  to  either  longer  papers  or  excerpts  therefrom — chiefly 
because  of  space,  but  also  because  we  want  the  serious  student,  who  may  later 
contribute  to  the  literature  himself,  to  see  each  published  work  in  its  entirety 
as  one  tangible  contribution  to  knowledge.  He  can  then  grasp  its  concept,  its 
methodology,  its  organization,  its  presentation,  its  conclusions,  and  perhaps 
even  its  limitations.  On  the  latter  score  we  would  note  that,  although  we  think 
the  papers  selected  are  worthy  contributions  and  make  the  points  we  wish  to 
emphasize,  we  do  not  pretend  to  have  selected  the  finest  papers  ever  published. 
We  could  have  used  a  somewhat  different  selection  to  serve  much  the  same 
pmpose,  and  we  are  sure  someone  else  would  use  a  different  selection  to 
represent  his  views  of  mammalogy. 

Although  many  college  and  university  libraries  have  some  or  most  of  the 
journals  and  other  sources  from  which  papers  were  selected,  we  decided  an 
anthology  was  warranted  for  those  who  want  an  overview  of  the  field,  who 
may  not  know  where  to  find  the  relevant  literature,  or  who  want  the  conve- 
nience of  a  collection  of  separate  papers.  Many  undergraduate  students  are 
largely  unaware  of  the  existence  of,  or  the  nature  of,  the  technical  literature 
of  science,  although  their  textbooks  are  replete  with  terminal  citations.  Hope- 


fully,  many  of  our  readers  will  be  provoked  to  go  to  the  library  to  seek  out 
additional  information  on  mammals,  once  they  learn  the  interest  and  value  of 
subjects  treated  in  the  pages  of  the  Journal  of  Mammalogy  and  other  scien- 
tific sources. 

We  have  formulated  our  ideas  for  this  anthology  over  the  past  three  years 
and  we  are  grateful  for  suggestions  received  from  many  persons  in  that  time. 
We  are  grateful  also  to  editors,  publishers,  and  living  authors  for  permission 
to  include  their  works  in  Readings  in  Mammalogy. 

J.  Knox  Jones,  Jr. 
Sydney  Anderson 


IV 


CONTENTS 

Introduction  __ — -.      3 

Section  1 — Systematics 

Grinnell,  J. 

The  museum  conscience.    Museum  Work,  4:62-63,  1922  9 

Thomas,  O. 

Suggestions  for  the  nomenclature  of  the  cranial  length 

measurements  and  of  the  cheek-teeth  of  mammals.  Proc. 

Biol.  Soc.  Washington,  18:191-196,  1905  11 

Hall,  E.  R. 

Criteria  for  vertebrate  subspecies,  species  and  genera:   the 

mammals.   Ann.  New  York  Acad.  Sci.,  44:141-144,  1943  17 

LiDiCKER,  W.  Z.,  Jr. 

The  nature  of  subspecies  boundaries  in  a  desert  rodent  and  its 
implications  for  subspecies  taxonomy.   Syst.  Zool.,  11:160-171,  1962  _. .     21 

Hershkovitz,  p. 

Generic  names  of  the  four-eyed  pouch  opossum  and  the  woolly 

opossum  (Didelphidae).  Proc.  Biol.  Soc.  Washington, 

62: 11-12,  1949  33 

Allen,  J,  A. 

Two  important  papers  on  North-American  mammals.  Amer. 

Nat.,  35:221-224,  1901  35 

Merriam,  C.  H. 

Descriptions  of  two  new  species  and  one  new  subspecies  of 

grasshopper  mouse,  with  a  diagnosis  of  the  genus  Onychomys, 

and  a  synopsis  of  the  species  and  subspecies.  N.  Amer. 

Fauna,  2:1-5,  pi.  1,  1889  __.__.. 39 

Handley,  C.  O.,  Jr. 

Descriptions  of  new  bats  {Choeroniscus  and  Rhinophylla)  from 
Colombia.   Proc.  Biol.  Soc.  Washington,  79:83-88,  1966 46 

Benson,  S.  B. 

The  status  of  Reithrodontomys  montanus  (Baird).  Jour. 

Mamm.,  16:139-142,  1935  52 

Hoffmeister,  D.  F.,  and  L.  de  la  Torre 

A  revision  of  the  woodrat  Neotoma  stephensi.  Jour.  Mamm., 

41 :476-491,  1960  56 

Lawrence,  B.,  and  W.  H.  Bossert 

Multiple  character  analysis  of  Canis  lupus,  latrans,  and 

familiaris,  with  a  discussion  of  the  relationships  of 

Canis  niger.   Amer.  Zool.,  7:223-232,  1967  72 

Patton,  J.  L.,  and  R.  E.  Dingman 

Chromosome  studies  of  pocket  gophers,  genus  Thomomys. 

I.  The  specific  status  of  Thomomys  umbrinus  (Richardson) 

in  Arizona.    Jour.  Mamm.,  49:1-13,  1968  82 


Nadler,  C.  F.,  and  C.  E,  Hughes 

Serum  protein  electrophoresis  in  the  taxonomy  of  some 
species  of  the  ground  squirrel  subgenus  Spermophilus. 
Comp.  Biochem.  Physiol,  18:639-651,  1966 95 

Machado- Allison,  C.  E. 

The  systematic  position  of  the  bats  Desmodus  and 

Chilonycteris,  based  on  host-parasite  relationships 

(Mammalia;  Chiroptera).  Proc.  Biol.  Soc.  Washington, 

80 :  223-226,  1967  108 


Section  2 — Anatomy  and  Physiology 

Hill,  J.  E. 

The  homology  of  the  presemimembranosus  muscle  in  some 

rodents.  Anat.  Rec,  59:311-314,  1934 115 

Hooper,  E.  T. 

The  glans  penis  in  Sigmodon,  Sigmomys,  and  Reithrodon 

(Rodentia,  Cricetinae).  Occas.  Papers  Mus.  Zool., 

Univ.  Michigan,  625:1-11,  1962  119 

Hughes,  R.  L. 

Comparative  morphology  of  spermatozoa  from  five  marsupial 

families.   Australian  Jour.  Zool.,  13:533-543,  pi.  1,  1965  130 

MOSSMAN,  H.  W. 

The  genital  system  and  the  fetal  membranes  as  criteria  for  mammalian 
phylogeny  and  taxonomy.  Jour.  Mamm.,  34:289-298,  1953 142 

NOBACK,  C.  R. 

Morphology  and  phylogeny  of  hair.  Ann.  New  York  Acad.  Sci., 
53:476-492,  1951  152 

Vaughan,  T.  a. 

Morphology  and  flight  characteristics  of  molossid  bats. 

Jour.  Mamm.,  47:249-260,  1966  169 

Rabb,  G.  B. 

Toxic  salivary  glands  in  the  primitive  insectivore  Solenodon. 

Nat.  Hist.  Misc.,  Chicago  Acad.  Sci.,  170:1-3,  1959 181 

Forbes,  R.  B. 

Some  aspects  of  the  water  economics  of  two  species  of 

chipmunks.    Jour.  Mamm.,  48:466-468,  1967  184 

Pearson,  O.  P. 

The  oxygen  consumption  and  bioenergetics  of  harvest 

mice.  Physiol.  Zool.,  33:152-160,  1960 187 

Bartholomew,  G.  A.,  and  R.  E.  MacMillen 

Oxygen  consumption,  estivation,  and  hibernation  in  the  kangaroo 

mouse,  Microdipodops  pallidus.   Physiol.  Zool.,  34:177-183,  1961  196 

Scholander,  p.  F.,  and  W.  E.  Schevill 

Counter-current  vascular  heat  exchange  in  the  fins  of 

whales.    Jour.  Applied  Physiol.,  8:279-282,  1955  203 


Section  3 — Reproduction  and  Development 

Hamilton,  W.  J.,  Jr. 

The  reproductive  rates  of  some  small  mammals.  Jour. 

Mamm.,  30:257-260,  1949  209 

Spencer,  A.  W.,  and  H.  W.  Steinhoff 

An  explanation  of  geographic  variation  in  litter  size. 

Jour.  Mamm.,  49:281-286,   1968 --- 213 

Sharmax,  G.  B. 

The  effects  of  suckling  on  normal  and  delayed  cycles  of  reproduc- 
tion in  the  red  kangaroo.  Z.  Siiugetierk.,  30:10-20,  1965 219 

Wright,  P.  L.,  and  M.  W.  Coulter 

Reproduction  and  growth  in  Maine  fishers.  Jour.  Wildlife 

Mgt.,  31:70-87,   1967 230 

Jones,  C. 

Growth,  development,  and  wing  loading  in  the  evening  bat, 

Nycticeiiis  liwneralis  (Rafinesque).  Jour.  Mamm., 

48: 1-19,  1967  248 

Butter  worth,  B.  B. 

A  comparative  study  of  growth  and  development  of  the 

kangaroo  rats,  Dipodomys  deserti  Stephens  and  Dipodomys 

merriami  Mearns.  Growth,  25:127-138,  1961 267 

Allen,  J.  A. 

Cranial  variations  in  Neotoma  micropus  due  to  growth  and 

individual  differentiation.  Bull.  Amer.  Mus.  Nat.  Hist., 

6:233-246,  pi.  4,  1894 279 

LiNZEY,  D.  W.,  and  A.  V.  Linzey 

Maturational  and  seasonal  molts  in  the  golden  mouse, 

Ochrotomys  nuttalli.    Jour.  Mamm.,  48:236-241,  1967  294 


Section  4 — Ecology  and  Behavior 

Caughley,  G. 

Mortality  patterns  in  mammals.    Ecology,  47:906-918,  1966  303 

Frank,  F. 

The  causality  of  microtine  cycles  in  Germany.  Jour. 

Wildlife  Mgt.,  21:113-121,  1957  316 

Burt,  W.  H. 

Territoriality  and  home  range  concepts  as  applied  to 

mammals.  Jour.  Mamm.,  24:346-352,  1943 325 

Miller,  G.  S.,  Jr. 

Migration  of  bats  on  Cape  Cod,  Massachusetts.  Science, 

5:541-543,  1897  -..- 332 

Brown,  L.  N. 

Ecological  distribution  of  six  species  of  shrews  and 

comparison  of  sampling  methods  in  the  central  Rocky 

Mountains.  Jour.  Mamm.,  48:617-623,  1967 335 

Davis,  D.  E.,  and  J.  J.  Christian 

Changes  in  Norway  rat  populations  induced  by  introduction 

of  rats.  Jour.  Wildlife  Mgt.,  20:378-383,  1956  342 


Pearson,  O.  P. 

A  traffic  survey  of  Microtus-Reithrodontomys  runways. 

Jour.  Mamm.,  40:169-180,  1959 ..-' 348 

EsTES,  R.  D.,  and  J.  Goddard 

Prey  selection  and  hunting  behavior  of  the  African  wild 

dog.   Jour.  Wildlife  Mgt.,  31:52-70,  1967  360 

Layne,  J.  N. 

Homing  behavior  of  chipmunks  in  central  New  York.  Jour. 

Mamm.,  38:519-520,  1957 379 

SUTHERS,  R.  A. 

Comparative  echolocation  by  fishing  bats.  Jour.  Mamm., 

48:79-87,  1967  381 

ElSENBERG,  J.  F. 

The  intraspecific  social  behavior  of  some  cricetine  rodents  of  the 

genus  Peromyscus.  Amer.  Midland  Nat.,  69:240-246,  1963 390 

McCarley,  H. 

Ethological  isolation  in  the  cenospecies  Peromyscus 

leucopus.    Evolution,  18:331-332,  1964  397 

Lyman,  C.  P. 

Activity,  food  consumption  and  hoarding  in  hibernators. 

Jour.  Mamm.,  35:545-552,  1954  399 

Real,  R.  O. 

Radio  transmitter-collars  for  squirrels.  Jour.  Wildlife 

Mgt.,  31:373-374,  1967  407 


Section  5 — Paleontology  and  Evolution 

Reed,  C.  A. 

The  generic  allocation  of  the  hominid  species  hahilis  as  a  problem  in 
systematics.   South  African  Jour.  Sci.,  63:3-5,  1967  411 

HiBBARD,  C.  W. 

Microtus  pennsylvanicus  (Ord)  from  the  Hav  Springs  local  fauna 

of  Nebraska.   Jour.  Paleont.,  30:1263-1266,  1956  414 

Wilson,  R.  W. 

Tvpe  localities  of  Cope's  Cretaceous  mammals.  Proc.  South 

Dakota  Acad.  Sci.,  44:88-90,  1965  418 

Radinsky,  L.  B. 

The  adaptive  radiation  of  the  phenacodontid  condylarths  and  the 

origin  of  the  Perissodactyla.  Evolution,  20:408-417,  1966 421 

Miller,  G.  S.,  Jr.,  and  J.  W.  Gidley 

Synopsis  of  the  supergeneric  groups  of  rodents.  Jour. 

Washington  Acad.  Sci.,  8:431-448,  1918  431 

Wood,  A.  E. 

Grades  and  clades  among  rodents.   Evolution,  19:115-130,  1965  449 

Durrant,  S.  D.,  and  R.  M.  Hansen 

Distribution  patterns  and  phvlogeny  of  some  western  ground 

squirrels.   Syst.  Zool.,  3:82-85,  1954 465 


Guthrie,  R.  D. 

Variability  in  characters  undergoing  rapid  evolution,  an  analysis 

of  Microtus  molars.   Evolution,  19:214-233,  1965  469 

Jansky,  L. 

Evolutionarv  adaptations  of  temperature  regulation  in 

mammals.  Z.  Saugetierk.,  32:167-172,  1967 - -- 489 


Section  6 — Zoogeography  and  Faunal  Studies 

Dice,  L.  R. 

The  Canadian  Biotic  Province  with  special  reference  to 

the  mammals.  Ecology,  19:503-514,  1938 497 

GUILDAY,  J.  E. 

Pleistocene  zoogeography  of  the  lemming,  Dicrostonyx. 

Evolution,  17:194-197,  1963 509 

KooPMAN,  K.  F.,  and  P.  S.  Martin 

Subfossil  mammals  from  the  Gomez  Farias  region  and  the  tropical 
gradient  of  eastern  Mexico.  Jour.  Mamm.,  40:1-12,  1959  513 

FiNDLEY,  J.  S.,  and  S.  Anderson 

Zoogeography  of  the  montane  mammals  of  Colorado.  Jour. 

Mamm.,  37:80-82,  1956 525 

Jones,  J.  K.,  Jr.,  and  T.  E.  Lawlor 

Mammals  from  Isla  Cozumel,  Mexico,  with  description  of 

a  new  species  of  harvest  mouse.  Univ.  Kansas  Publ., 

Mus.  Nat.  Hist.,  16:411-419,  1965  528 

Davis,  W.  B. 

Relation  of  size  of  pocket  gophers  to  soil  and  altitude. 

Jour.  Mamm.,  19:338-342,  1938 537 

Davies,  J.  L. 

The  Pinnipedia:   an  essav  in  zoogeography.  Geographical 

Rev.,  48:474-493,  1958  .' 542 

Hagmeier,  E.  M. 

A  numerical  analysis  of  the  distributional  patterns  of 

North  American  mammals.  II.  Re-evaluation  of  the  provinces. 

Syst.  Zool.,  15:279-299,  1966 562 


Literature  Cited  583 


READINGS  IN 
MAMMALOGY 


INTRODUCTION 

The  overall  unity  of  the  different  fields  of  science  and  of  other  aspects  of 
human  experience,  or  at  least  their  interdependence,  is  evident  in  both  theory 
and  practice.  Nevertheless,  this  is  an  age  of  specialization.  The  sheer  volume 
of  information,  the  current  rate  of  increase  in  knowledge,  the  changing  and 
often  elaborate  techniques  that  must  be  learned,  and  human  limitations  all 
have  contributed  to  the  production  of  specialties. 

A  definition  of  the  specialty  of  mammalogy  as  "all  scientific  study  of  mam- 
mals" is  too  broad,  for  that  definition  encompasses,  for  example,  all  parts  of 
animal  physiology  in  which  any  mammal,  such  as  a  white  rat  in  the  laboratory, 
may  happen  to  be  used.  It  also  would  include  much  of  medical  practice, 
because  humans  are  mammals.  Generally  speaking,  those  scientists  who  call 
themselves  mammalogists  are  interested  in  the  mammal  as  an  animal — as  an 
organism — not  just  as  a  specific  case  of  some  more  general  phenomenon,  be  it 
the  nature  of  life  or  the  nature  of  the  nerve  impulse.  For  example,  a  physiolo- 
gist who  is  interested  in  comparative  studies  between  different  mammals  or  in 
the  function  of  a  physiological  process  as  an  adaptive  mechanism  may  regard 
himself  as  a  mammalologist.  A  physiologist  who  studies  one  kind  of  laboratory 
animal  and  is  interested  in  explaining  a  process  in  terms  of  progressively  sim- 
pler mechanisms  rarely  will  regard  himself  as  a  mammalogist.  Both  types  of 
study,  of  course,  contribute  to  biological  knowledge. 

Life  is  best  comprehended  in  terms  of  four  basic  concepts:  first,  that 
biology,  as  all  of  science,  is  monistic,  assuming  one  universe  in  which  the  same 
natural  laws  apply  to  living  and  non-living  things;  second,  that  life  is  a  dynamic 
and  self-perpetuating  process;  third,  that  the  patterns  of  life  change  with  time; 
finally,  that  these  factors  together  have  resulted  in  a  diversity  of  living  forms. 

Different  branches  of  biology  tend  to  focus  or  concentrate  on  different 
concepts.  Thus,  the  above  four  concepts  are  focal  points,  respectively,  of  ( 1 ) 
physiology  and  biochemistry,  (2)  ecology,  (3)  evolutionary  biology,  and  (4) 
systematic  biology.  Mammalogy  is  the  study  of  one  systematic  group  or  taxon, 
the  Class  Mammalia.  Studies  emphasizing  different  aspects  of  mammalian 
biology  are  evident  in  our  section  headings  and  in  the  specific  papers  repro- 
duced. Biology  as  a  whole  and  mammalogy  specifically  may  be  best  likened 
to  a  woven  fabric  rather  than  to  a  series  of  compartments. 

We  feel  that  a  unifying  conceptual  scheme  for  "mammalogy"  lies  in  the 
realm  of  "systematic  mammalogy."  This  scheme  is  unifying  because  it  includes 
the  basis  for  subsequent  study  and  the  only  meaningful  framework  for  the 
synthesis  of  existing  knowledge  of  mammals.  On  this  point,  George  Gaylord 
Simpson,  in  introducing  his  classic  The  Principles  of  Classification  and  a  Classi- 
fication of  Mammals  (1945)  wrote  (Simpson  at  that  time  used  the  term 
"taxonomy"  as  we  use  "systematics" ) : 

"Taxonomy  is  at  the  same  time  the  most  elementary  and  the  most 
inclusive  part  of  zoology,  most  elementary  because  animals  cannot  be 
discussed  or  treated  in  a  scientific  way  until  some  taxonomy  has  been 
achieved,  and  most  inclusive  because  taxonomy  in  its  various  guises  and 


branches  eventually  gathers  together,  utilizes,  summarizes,  and  imple- 
ments everything  that  is  known  about  animals,  whether  morphological, 
physiological,  psychological,  or  ecological." 

Knowledge  of  the  identity  of  any  animal  studied  is  essential  so  that  the 
results  may  be  compared  with  other  knowledge  about  the  same  kind  of  animal 
and  with  the  same  kind  of  knowledge  about  different  animals. 

We  originally  had  hoped  to  develop  the  history  of  mammalogy  along  with 
our  other  objectives,  but  when  the  hard  fact  of  page  limitation  was  faced, 
some  selections  whose  chief  justification  was  historical  were  sacrificed.  In  the 
comments  beginning  each  section,  some  historical  information  helps  place  the 
selections  in  an  understandable  framework.  To  attain  variety  we  have 
included  papers  both  of  restricted  and  of  general  scope;  for  example,  papers 
pertaining  to  local  faunas  and  continental  faunas,  to  higher  classification  and 
infraspecific  variation,  and  to  contemporary  serum  proteins  and  millions  of 
years  of  evolution. 

Every  serious  student  of  mammalogy,  whether  amateur  or  professional, 
researcher  or  compiler,  writer  or  reviewer,  artist  or  teacher,  must  learn  to  use 
the  literature.  One  does  not  learn  all  about  mammals  because  that  is  impossi- 
ble. One  learns  what  one  can,  where  to  look  for  further  information,  and, 
more  important,  how  to  evaluate  what  one  finds. 

Most  of  the  literature  on  mammals  is  in  technical  journals,  a  few  of  which 
are  devoted  exclusively  to  mammalogy:  Journal  of  Mammalogy  (USA), 
Mammallv  (France),  Zeitschrift  fur  Saugetierkunde  (Germany),  Sauge- 
TiERKLrxDLiCHE  MiTTEiLUNGEN  (Germany),  LuTRA  (Benelux  countries).  Lynx 
(Czechoslovakia),  Acta  Theriologica  (Poland),  The  Journal  of  the  Mam- 

MALOGICAL   SOCIETY   OF   JaPAN,    AuSTR.\LLVN    MaMMAL    SOCIETY    BULLETIN,    and 

Bulletin  of  the  British  Mammal  Society.  Also  there  are  the  specialized 
Folia  Primatologica,  an  international  journal  of  primatology,  founded  in 
1963,  and  a  number  of  serial  publications  such  as  Journal  of  Wildlife  Man- 
agement, Bulletin  of  the  Wildlife  Disease  Association,  and  journals  issued 
by  various  game  departments  and  conservation  agencies  that  may  deal  in  large 
part,  but  not  exclusively,  with  mammals.  However,  much  of  the  published 
information  on  mammals,  as  on  most  aspects  of  biology,  is  widely  scattered. 
About  40  journals  include  50  per  cent  of  the  current  Hterature,  but  to  cover  70 
per  cent,  at  least  150  journals  must  be  consulted.  Articles  in  the  Journal  of 
Mammalogy  (now  more  than  800  pages  each  year)  comprise  only  about 
three  per  cent  of  all  current  titles  on  mammals,  for  example. 

Some  categories  of  literature  other  than  journals  are  books,  symposia, 
transactions  of  various  meetings  or  groups  such  as  the  Transactions  of  the 
North  American  WildHfe  and  Natural  Resources  Conference  (the  34th  was 
issued  in  1969),  yearbooks  such  as  the  International  Zoo  Yearbook  (the  tenth 
was  published  in  1970),  newsletters  such  as  the  Laboratory  Primate  Newslet- 
ter, Carnivore  Genetics  Newsletter,  or  Bat  Research  News,  major  revisions  or 
compilations  of  special  subjects,  bibHographies,  and  abstracts.  The  chief 
bibliographic  sources  for  mammalogists  are  the  Journal  of  Mammalogy, 
through  its  lists  of  Recent  Literature,  Saugetierkut>jdliche  Mitteilungen, 
through  its  "Schriftenschau"  section,  the  Zoological  Record,  published  by  the 


Zoological  Society  of  London,  Biological  Abstracts  (quite  incomplete  for 
some  branches  of  mammalogy),  and  the  quarterly  Wildlife  Review  that  is 
issued  by  the  U.S.  Fish  and  WildUfe  Service  (along  with  the  three  collections 
of  Wildlife  Abstracts — a  misnomer  because  only  citations  are  included — 
compiled  therefrom  and  published  in  1954,  1957,  and  1964);  one  especially 
useful  bibliography  to  older  papers  on  North  American  mammals  is  that  com- 
piled by  Gill  and  Coues  (in  Coues  and  Allen,  1877).  Some  individuals  and 
institutions  maintain  records  in  the  form  of  card  files,  or  collections  of  sepa- 
rates, or  both,  over  many  years  for  special  subjects,  special  geographic  areas, 
or  other  more  general  purposes.  It  is  important  for  the  student  to  remember 
that  large-scale  faunal  reports,  catalogues,  revisionary  works,  and  the  like 
often  are  valuable  as  bibliographic  sources  as  well  as  sources  of  other  informa- 
tion. Some  of  these  reports  are  mentioned  in  the  introductory  remarks  to 
several  sections. 

An  individual  who  delves  into  the  literature  on  a  particular  subject  usually 
begins  with  one  or  more  pertinent  recent  works  and  proceeds  backward  in 
time  by  looking  up  publications  cited  in  the  later  works  or  found  in  other 
bibliographic  sources. 

An  amazing  amount  of  published  information  on  a  given  subject  frequently 
is  available  to  the  person  willing  to  look  for  it.  However,  paradoxically,  there 
is  often  no  pubhshed  record  for  what  one  might  suppose  to  be  nearly  common 
knowledge.  The  questioning  mind  must  return  to  nature  when  the  Hterature 
holds  no  answer,  exactly  what  the  authors  of  papers  reproduced  in  this  anthol- 
ogy have  done. 

A  few  decades  ago  only  a  small  number  of  American  colleges  and  universi- 
ties offered  a  formal  course  in  mammalogy,  and  only  since  about  1950  have 
such  courses  been  widely  offered.  It  is  not  surprising,  therefore,  that  only 
two  textbooks,  Cockrum's  Introduction  to  Mammalogy  (1962)  and  Principles 
in  Mammalogy  by  Davis  and  Golley  (1963)  have  been  published  in  EngHsh. 
The  formCT  has  a  systematic  orientation  and  the  latter  is  predominantly  eco- 
logical. Some  instructors  use  general  works  like  Recent  Mammals  of  the 
World,  A  Synopsis  of  Families  (edited  by  Anderson  and  Jones,  1967),  Mam- 
mals of  the  World,  a  three- volume  work  by  Walker  et  al.  ( 1964),  or  Hamilton's 
( 1939)  American  Mammals  as  texts  or  as  references  along  with  other  suggested 
readings.  Accounts  of  the  mammals  of  certain  states  or  regions  also  may  be 
used  as  texts  by  persons  in  those  places.  Other  general  works  of  reference 
value  are  Bourhere's  Natural  History  of  Mammals  ( 1954),  Young's  The  Life  of 
Mammals  (1957),  Crandall's  Management  of  Wild  Mammals  in  Captivity 
(1964),  and  the  fascicles  on  mammals  in  the  Traite  de  Zoologie  (edited  by 
Grasse,  1955  and  later).  Two  classic  general  works  less  readily  available  are 
An  Introduction  to  the  Study  of  Mammals,  Living  and  Extinct  by  Flower  and 
Lydekker  (1891)  and  Mammalia  by  Beddard  (1902)  in  the  Cambridge  Natu- 
ral History  series. 

Compact  field  guides  to  the  mammals  of  a  few  parts  of  the  world  are  avail- 
able, such  as  those  of  Burt  and  Grossenheider  ( 1964 ) ,  Palmer  ( 1954 ) ,  and 
Anthony  (1928)  for  parts  of  North  America,  and  Van  den  Brink  (1967)  for 
Europe. 


The  dates  in  the  tvvo  preceding  paragraphs  suggest  the  recent  expansion  in 
the  volume  of  work  in  mammalog)'.  Another  such  measure  is  membership  in 
The  American  Society-  of  Mammalogists,  which  grew  from  252  in  1919  to  more 
than  3200  in  1969,  and  half  of  the  growth  occurred  after  1957.  Persons  inter- 
ested in  mammalog)'  are  in\ited  to  appl>-  for  membership  in  this  society',  mem- 
bers of  which  receive  the  Journal  of  Mammalogy. 

Human  medicine,  veterinary-  medicine,  animal  husbandry,  and  animal 
physiology  (including  much  work  with  a  comparatiNcly  few  species  of  mam- 
mals in  the  laboratory),  all  preceded  mammalogy  as  separate  disciplines  deal- 
ing with  mammals.  Many  of  the  first  mammalogists  (as  defined  here)  trained 
themselves  in  one  of  these  disciplines  and  some  also  practiced  in  fields  other 
than  mammalogy.  C.  Hart  Merriam,  who  founded  the  U.S.  Biological  Survey, 
studied  medicine,  as  did  E.  A.  Mearns,  who  N\Tote  on  mammals  of  the  Mexican 
boundary  (1907).  Harrison  Allen  %\Tote  much  of  his  first  review  of  North 
American  bats  ( 1864 )  while  on  furloughs  from  duty  as  a  surgeon  in  the  Union 
army  in  the  Ci\il  War.  Mammalogy  continues  to  interact  %\ith  the  above- 
mentioned  fields  to  their  mutual  benefit. 

Another  largely  separate  but  partly  overlapping  field  that  flowered  slightly 
later  than  mammalogy  is  genetics.  We  have  included  no  papers  on  mammalian 
genetics  as  such,  although  the  rele\ance  of  genetics  is  evident  in  some  of  our 
selections.  A  recent  book  on  Comparative  Genetics  of  Coat  Color  in  Mammals 
by  Searle  (1968)  contains  about  800  references,  including  some  fascinating 
works  on  species  other  than  the  oft-studied  mouse  (Mus  musculus). 

Our  six  groupings  of  papers  are  somewhat  arbitrary.  Ecology  is  as  closely 
allied  to  physiology  or  zoogeography  as  to  behaxior,  and  anatomy  could  as  well 
have  been  placed  with  development  as  with  physiology.  The  present  arrange- 
ment as  to  the  sequence  of  sections  and  the  contents  of  sections  seems  to  be 
about  as  convenient  and  useful  as  any  other,  and  that  is  the  extent  of  our  expec- 
tations. We  imply  no  hierarchy  of  subdisciplines. 

In  selecting  works  to  be  included  here,  we  have,  in  addition  to  the  consider- 
ations already  noted,  sought  papers  in  which  different  kinds  of  mammals  were 
compared,  and  in  which  different  approaches,  styles,  and  methods  of  presenta- 
tion were  used.  Individual  papers  often  pertain  to  more  than  one  area  of  study. 
In  fact,  we  favored  papers  that  illustrated  the  rele\ance  of  different  disciplines 
and  methods  of  study  to  each  other.  Perhaps  the  reader  will  be  able  to  ap- 
preciate our  moments  of  anguish  as  the  final  selections  w-ere  made  for  this 
anthology. 

Our  introduction  for  each  section  is  brief.  We  hope  that  our  comments  aid 
the  reader  in  considering  ( 1 )  some  historical  aspects  that  make  the  papers 
more  meaningful,  (2)  the  major  areas  of  study  and  some  major  concepts  that 
the  papers  illustrate,  (3)  the  existence  of  related  Hterature,  to  which  we  can 
only  call  attention  by  citing  a  few  examples,  and  (4)  the  continuous  transfer 
of  ideas,  methods,  and  results  from  one  worker  to  another,  from  one  field  of 
science  to  another,  and  between  science  and  other  fields  of  human  endeavor. 


SECTION  1— SYSTEMATICS 

A  sound  classification  provides  the  necessary  framework  upon  which  other 
knowledge  about  mammals  can  be  built.  In  order  to  classify  organisms,  it 
first  is  necessary  to  know  their  similarities  and  differences;  in  other  words, 
structures  and  their  functions  need  to  be  observed,  described,  and  compared, 
and  taxa  need  to  be  recognized  and  named  before  a  useful  and  meaningful 
classification  can  be  constructed.  The  field  of  study  relating  to  classification 
frequently  is  called  "taxonomy,"  although  the  broader  term  "systematics"  is 
also  widely  used  and  is  preferred  by  us. 

Prior  to  the  first  decade  or  so  of  the  20th  century,  the  practice  of  mamma- 
Han  taxonomy  generally  was  based  on  a  "hit-or-miss"  typological  approach, 
which,  although  it  fostered  considerable  advancement  in  cataloguing  the 
faunas  of  the  world,  was  limited  in  perspective  and  potential.  The  develop- 
ment of  evolutionary  thought  and  the  spectacular  growth  of  genetics  have  led 
to  the  "new  systematics,"  the  biological  species  concept  of  today,  as  discussed 
in  detail  in  such  syntheses  as  Huxley  (1943),  Mayr  et  al.  (1953),  Simpson 
(1961),  and  Mayr  (1963  and  1969),  among  others.  Blackwelder's  (1967) 
recent  text  in  taxonomy  also  is  deserving  of  mention  here. 

Technological  advances  in  the  means  of  collecting,  preparing,  and  storing 
specimens  resulted  in  the  accumulation  of  series  of  individuals  of  the  same 
species  (the  invention  of  the  break-back  mouse  trap  might  be  mentioned  here 
along  with  the  relatively  recent  widespread  use  of  mist  nets  for  capturing  bats ) 
and  thus  in  turn  allowed  for  assessment  of  variations  within  and  between 
populations.  Sophisticated  studies  of  intergradation,  hybridization,  and  the 
cenospecies  concept  in  the  past  few  decades  are  examples  of  results  from  tech- 
nological and  conceptual  advances  in  this  area. 

To  imply  that  all  early  taxonomic  treatments  of  mammals  were  either 
inconsequential  or  poorly  conceived  would  be  a  gross  error.  Pallas'  (1778) 
revision  of  rodents,  for  example,  was  a  monumental  work  far  advanced  for  its 
day,  as  were  many  other  outstanding  contributions  by  18th  and  19th  century 
mammalogists  that  could  be  mentioned.  Nevertheless,  one  has  only  to  compare 
the  descriptions  and  accounts  of  Pallas  with  those  found  in  papers  reprinted 
here  by  Merriam,  Handley,  and  Hoffmeister  and  de  la  Torre  to  appreciate  the 
tremendous  revolution  in  systematic  practice.  It  is  of  interest  to  note  that  the 
80-year-old  paper  by  Merriam  still  is  valid  with  reference  to  the  specific  status 
of  grasshopper  mice.  The  short  contribution  by  J.  A.  Allen  not  only  provides 
an  example  of  a  review,  but  deals  in  some  detail  with  two  substantial  revision- 
ary  works  published  at  the  turn  of  the  century.  Among  the  larger  modern 
revisionary  studies  that  might  be  recommended  to  the  student  are  those  of 
Osgood  (1909),  Jackson  (1928),  Hooper  (1952),  Pearson  (1958),  Lidicker 
(1960),  and  Packard  (1960).  Ellerman's  (1940,  1941,  1948)  well  organized 
review  of  living  rodents  and  Hill's  ( 1953  and  subsequent  volumes )  somewhat 
more  rambling  and  less  critical  coverage  of  the  primates  are  also  noteworthy 
as  attempts  to  summarize  selected  bodies  of  knowledge  of  important  groups  of 
mammals. 


The  goal  of  scientific  nomenclature  is  to  assure  that  each  kind  of  organism 
has  a  unique  name,  and  only  one  name.  The  International  Code  of  Zoological 
Nomenclature  ( latest  edition,  1961 )  forms  the  legalistic  framework  for  dealing 
with  nomenclature,  both  past  and  present.  The  presently  reprinted  paper  by 
Hershkovitz  points  up  some  of  the  kinds  of  nomenclatorial  problems  faced  by 
the  systematist.  The  Code  is  administered  by  the  International  Commission 
on  Zoological  Nomenclature  but,  as  Blair  (1968)  pointed  out,  the  Commission 
"has  no  way  of  enforcing  its  decisions,  and  the  burden  of  holding  names  to 
conformity  with  the  [Code]  falls  on  the  individual  worker  and  on  editors  of 
scientific  pubHcations." 

The  emphasis  in  this  section  is  mostly  at  the  level  of  species  and  subspecies 
( for  example,  the  papers  by  Benson  and  by  Lidicker ) .  Higher  categories  are 
dealt  with  primarily  in  Section  5.  Attempts  over  the  years  by  taxonomists  to 
standardize  techniques  and  definitions  are  illustrated  by  the  papers  of  Thomas 
and  Hall.  The  short  essay  by  Grinnell  also  bears  on  this  point. 

The  final  four  selections  illustrate  the  application  of  new  techniques  and 
concepts  to  specific  taxonomic  problems,  all  of  which  were  clarified  in  ways 
that  might  have  been  impossible  otherwise.  The  treatment  by  Lawrence  and 
Bossert  of  the  problem  of  the  relationships  of  the  red  wolf  uses  standard 
cranial  measurements  but  analyzes  them  by  discriminant  analysis,  a  concep- 
tually simple  but  computationally  difficult  statistical  technique  that  has  become 
generally  applicable  only  with  the  development  of  digital  computers.  The 
karyological  studies  reported  by  Patton  and  Dingman  treat  some  taxonomically 
interesting  and  previously  confusing  gophers  in  Arizona  and  enabled  the 
authors  to  extend  and  refine  the  tentative  conclusions  based  on  other  evidence; 
this  paper  also  provides  a  good  example  of  the  careful  integration  of  a  new 
systematic  approach  with  ecological  and  distributional  considerations.  Sero- 
logical methods  have  been  employed  in  taxonomic  studies  for  many  years,  but 
new  methods  such  as  the  serum  protein  electrophoresis  used  by  Nadler  and 
Hughes  are  increasing  the  useful  means  of  approaching  systematic  problems 
at  the  biochemical  or  molecular  level.  Machado-AlHson's  contribution  on  host- 
parasite  relationships  illustrates  the  relevance  of  taxonomic  data  from  one 
group,  in  this  case  ectoparasites,  to  the  taxonomy  of  a  different  (host)  group, 

bats. 

Many  papers  in  other  sections  of  this  anthology  touch  on  systematics  in 
one  way  or  another,  and  the  usefulness  to  the  taxonomist  of  information  from 
a  variety  of  sources  will  be  immediately  evident  to  the  reader.  Two  journals 
devoted  to  the  concepts  and  practices  of  systematics  and  in  which  contributions 
in  mammalogy  regularly  appear  are  Systematic  Zoology  and  Zeitschrift  fur 

ZOOLOGISCHE  SySTEMATIK. 


The  Museum  Conscience 


THE  scientific  museum,  the  kind 
of  museum  with  which  my  re- 
marks here  have  chiefly  to  do, 
is  a  storehouse  of  facts,  arranged  acces- 
sibly and  supported  by  the  written 
records  and  labeled  specimens  to  which 
they  pertain.  The  purpose  of  a  scien- 
tific museum  is  realized  whenever  some 
group  of  its  contained  facts  is  drawn 
upon  for  studies  leading  to  publication. 
The  investment  of  human  energy  in  the 
formation  and  maintenance  of  a  re- 
search museum  is  justified  only  in 
proportion  to  the  amount  of  real 
knowledge  which  is  derived  from  its 
materials  and  given  to  the  world. 

All  this  may  seem  to  be  innocuous 
platitude — but  it  is  genuine  gospel, 
never-the-!ess,  worth  pondering  from 
time  to  time  by  each  and  every  museum 
administrator.  It  serves  now  as  a 
background  for  my  further  comments. 

For  worthy  investigation  based  upon 
museum  materials  it  is  absolutely  es- 
sential that  such  materials  have  been 
handled  with  careful  regard  for  ac- 
curacy and  order.  To  secure  accuracy 
and  order  must,  then,  once  the  mere 
safe  preservation  of  the  collections 
of  which  he  is  in  charge  have  been 
attended  to,  be  the  immediate  aim  of 
the   curator. 

Order  is  the  key  both  to  the  accessi- 
bility of  materials  and  to  the  apprecia- 
tion of  such  facts  and  inferences  as 
these    materials    afford.      An    arrange- 


ment according  to  some  definite  plan 
of  grouping  has  to  do  with  whole  col- 
lections, with  categories  of  specimens 
within  each  collection,  with  specimens 
within  each  general  category,  with  the 
card  indexes,  and  even  with  the  place- 
ment of  the  data  on  the  label  attached 
to  each  specimen.  Simplicity  and 
clearness  are  fundamental  to  any 
scheme  of  arrangement  adopted.  Noth- 
ing can  be  more  disheartening  to  a 
research  student,  except  absolute  chaos, 
than  a  complicated  "system,"  in  the 
invidious  sense  of  the  word,  carried 
out  to  the  absurd  limits  reo  nmended 
by  some  so-called  "efiiciency  expert." 
However,  error  in  this  direction  is  rare 
compared  with  the  opposite  extreme, 
namely,  little  or  no  order  at  all. 

To  secure  a  really  practicable  scheme 
of  arrangement  takes  the  best  thought 
and  much  experimentation  on  the  part 
of  the  keenest  museum  curator.  Once 
he  has  selected  or  devised  his  scheme, 
his  work  is  not  done,  moreover,  until 
this  scheme  is  in  operation  throughout 
all  the  materials  in  his  charge.  Any 
fact,  specimen,  or  record  left  out  of 
order  is  lost.  It  had,  perhaps,  better 
not  exist,  for  it  is  taking  space  some- 
where; and  space  is  the  chief  cost 
initially  and  currently  in  any  museum. 

The  second  essential  in  the  care  of 
scientific  materials  is  accuracy.  Every 
item  on  the  label  of  each  specimen, 
every    item    of    the    general    record    in 


The     Ml'seum     Conscience 


the  accession  catalog,  must  be  precise 
as  to  fact.  Many  errors  in  published 
literature,  now  practically  impossible 
to  "head  off,"  are  traceable  to  mistakes 
on  labels.  Label-writing  having  to  do 
with  scientific  materials  is  not  a  chore 
to  be  handed  over  casually  to  a  "25- 
cent-an-hour"  girl,  or  even  to  the 
ordinary  clerk.  To  do  this  essential 
work  correctly  requires  an  exceptional 
genius  plus  training.  The  important 
habit  of  reading  every  item  back  to 
copy  is  a  thing  that  has  to  be  acquired 
through  diligent  attention  to  this 
very  point.  By  no  means  any  person 
that  happens  to  be  around  is  capable 
of  doing  such  work  with  reliable 
results. 

Now  it  happens  that  there  is  scarcely 
an  institution  in  the  country  bearing 
the  name  museum,  even  though  its 
main  purpose  be  the  quite  distinct  func- 
tion of  exhibition  and  popular  educa- 
tion, that  does  not  lay  more  or  less 
claim  to  housing  "scientific  collections." 
Yet  such  a  claim  is  false,  unless  an 
adequate  effort  has  been  expended  both 
to  label  accurately  and  to  arrange 
systematically  all  of  the  collections 
housed.  Only  when  this  has  been  done 
can  the  collections  be  called  in  truth 
scientific. 

My  appeal  is,  then,  to  every  museum 
director  and  to  every  curator  responsi- 
ble for  the  proper  use  as  well  as  the 
safe  preservation  of  natural  history 
specimens.  Many  species  of  vertebrate 
animals  are  disappearing;  some  are 
gone  already.  All  that  the  investigator 
of  the  future  will  have,  to  indicate  the 


nature  of  such  then  extinct  species, 
will  be  the  remains  of  these  species 
preserved  more  or  less  faithfully,  along 
with  the  data  accompanying  them,  in 
the  museums  of  the  country. 

I  have  definite  grounds  for  present- 
ing this  appeal  at  this  time  and  in  this 
place.  My  visits  to  the  various  larger 
museums  have  left  me  with  the  un- 
pleasant and  very  distinct  conviction 
that  a  large  portion  of  the  vertebrate 
collections  in  this  country,  perhaps  90 
per  cent  of  them,  are  in  far  from  satis- 
factory condition  with  respect  to  the 
matters  here  emphasized.  It  is  ad- 
mittedly somewhat  difficult  for  the 
older  museums  to  modify  systems  of 
installation  adopted  at  an  early  period. 
But  this  is  no  valid  argument  against 
necessary  modification,  which  should 
begin  at  once  with  all  the  means  avail- 
able— the  need  for  which  should,  in- 
deed, be  emphasized  above  the  making 
of  new  collections  or  the  undertaking 
of  new  expeditions.  The  older  materials 
are  immensely  valuable  historically, 
often  irreplaceable.  Scientific  interests 
at  large  demand  special  attention  to 
these  materials. 

The  urgent  need,  right  now,  in  every 
museum,  is  for  that  special  type  of  cura- 
tor who  has  ingrained  within  him  the 
instinct  to  devise  and  put  into  opera- 
tion the  best  arrangement  of  his 
materials — who  will  be  alert  to  see  and 
to  hunt  out  errors  and  instantly  make 
corrections — who  has  the  museum  con- 
science. 

March  29,  1921. 


10 


Vol.  XVIII,  pp.  191-196  September  2,  1905 

PROCEEDINGS 


OF  THE 


BIOLOGICAL  SOCIETY  OF  WASHINGTON 


SUGGESTIONS    FOR    THE    NOMENCLATURE    OF   THE 

CRANIAL  LENGTH  INIEASUREMENTS  AND  OF 

THE  CHEEK-TEETH  OF  MAMMALS. 

BY  OLDFIELD  THOMAS. 


Although  various  reasons  prevent  the  general  success  of  such 
a  wholesale  revolution  in  scientific  terms  as  is  described  in 
Wilder  and  Gage's  Anatomical  Technology  (1882),  where  the 
many  arguments  in  favor  of  accurate  nomenclature  are  admira- 
bly put  forth,  yet  in  various  corners  of  science  improvements 
can  be  suggested  which,  if  the  workers  are  willing  and  in  touch 
with  each  other,  may  be  a  real  help  in  reducing  the  inconvenience 
of  the  loose  or  clumsy  terminology  commonly  in  vogue. 

Two  such  suggestions,  due  largely  to  the  instigation  of  Mr. 
Gerrit  S.  Miller,  Jr.,  form  the  subject  of  the  present  paper. 

I.  Length  Measurements  of  the  Skull  and  Palate. 

In  giving  the  length  measurement  of  the  skull,  not  only  do 
different  authors  at  present  use  different  measurements  in  de- 
scribing the  skulls  of  similar  or  related  animals,  but  in  doing  so 
they  designate  these  measurements  by  terms  of  which  it  is  often 
difficult  or  impossible  to  make  out  the  exact  meaning.  Such  a 
name  as  ' '  basal  length  ' '  has  I  believe  been  used  by  one  person 
or  another  for  almost  every  one  of  the  measurements  to  be  here- 

34— Proc.  Biol.  Soc.  Wash.,  Vol.  XVIII,  1905.  (191) 


11 


192 


Thomas — Nomenclature  of  Measurements. 


after  defined,  and  readers  are  expi'cted  to  know  by  heart  every- 
thing that  the  user  has  ever  written  on  the  sul)ject,  footnotes 
and  all,  in  order  to  understand  what  is  meant  by  the  particular 
term  employed.  Such  a  state  of  things  has  many  inconveniences, 
and  it  is  hoped  the  present  communication,  if  it  meets  with  the 
approval  of  other  workers  on  the  subject,  may  do  a  little  toward 
putting  an  end  to  the  existing  confusion. 

As  long  ago  as  1894,*  Ijy  agreeing  with  Dr.  Nehring  for  the 
definition  of  the  terms  ])asal  and  basilar  in  our  own  future  writ- 


ings, I  made  a  first  step  in  this  direction,  and  the  present  is 
an  amplification  of  the  principle  then  adopted. 

All  the  difficulty  has  arisen  from  the  fact  that  both  at  the 
anterior  and  the  posterior  ends  of  the  skull  there  are  two  meas- 
urement points,  so  that  there  are  four  different  ways  in  which 
the  l)asal  length  of  the  skull  may  l)e  taken,  and  under  that 
name  some  authors  have  adopted  nearly  every  one  of  them. 

It  is  clear  that  if  a  definite  name  be  given  to  each  one  of  the 
four  measurements,  authors,  by  using  these  names,  will  be  en- 
abled to  give  the  measurements  they  fancy  without  causing  con- 
fusion in  the  minds  of  their  readers  as  to  their  exact  meaning. 

*Ann.  &  Mag.  Nat.  Hist.,  Ser.  6,  XIII,  p.  203. 


12 


Thomas — Nomenclature  of  Measurements.  193 

The  different  points  are: 

Anteriorly :     1 .  Tiik  Gnatiiion,  the  most  anterior  point  of  the 

premaxilke,  on  or  near  the  middle  line. 
2.  The  Henselion,  the  back  of  the  alveolus  of 

either  of  the  median  incisors,  the  point  used 

and  defined  by  Prof.  ITensel  in  his  cranio- 

logical  work. 
Posteriorly:    3.  The  Basiox,  a  point  in  the  middle  line  of  the 

hinder  edge  of  the  basioccipital  margin  of 

the  foramen  magnum. 
4.  The  Condylion,  the  most  posterior  point  of 

the  articular  surface  of  either  condyle. 

A  fifth  measuring  point  to  })e  referred  to  below  is  the  Pala- 
TioN,  the  most  anti'rior  point  of  the  hinder  edge  of  the  bony 
palate,  whether  in  the  middle  line  or  on  either  side  of  a  median 
spine. 

Now  using  these  words  for. the  purposes  of  definition,  I  would 
propose>,  as  shown  in  the  diagram,  the  following  names  for  the 
four  measurements  that  may  be  taken  between  the  points  above 
defined : — 

1.  Basal  length,  tlie  distance  from  Basion  to  Gnathion. 

2.  Basilar  len(;th,  the  distance  from  Basion  to  Henselion. 

3.  Condylo-basal  lenoth,  the    distance  from  Condylion  to 

Gnathion. 

4.  Condylo-basilar  length,  the  distance  from  Condylion  to 

Henselion. 
In  addition  there  may  be: 

5.  Gre.\test  len(;th,  to  be  taken  not  further  divergent  from 

the  middle  line  than  either  condylion.  A  long  diagonal 
to  a  projecting  bulla  or  paroccipital  process  would  thus 
be  barred .  If  however  the  words  ' '  between  uprights  ' ' 
be  added  the  measurement  would  be  between  two  ver- 
tical planes  pressed  respectively  against  the  anterior 
and  posterior  ends  of  the  skull  at  right  angles  to  its 
middle  line. 

6.  Upper  length,  from  tip  of  nasals  to  hinder  edge  of  occipi- 

tal ridge  in  middle  line. 

The  difference  between  the  words  basal  and  basilar,  which  at 
first  seemed  trivial  and  indistinctive,  is  founded  on  the  use  of 


13 


194  Thomas — Nomenrlnture  of  Measurements. 

the  Englisli  word  ])asal  by  the  older  writers,  such  as  Flower  and 
others,  who  used  tlie  lueasurenient  from  tlie  gnatliion;  wliile 
basilai'  is  an  adaptation  of  tlie  German  of  Hensel  and  liis  school, 
who  used  the  ^' ha.^ilar-lcinge'"  from  the  henselion.  These 
names  again,  coml)ined  with  condylo-,  readily  express  the  points 
which  are  used  hy  those  who  like  to  adopt  tlie  condylion  as  a 
posterior  measuring  point. 

But  further,  the  association  of  the  ending  "  al  "  with  a  meas- 
urement from  the  gnathion,  and  "  ilar  "  with  one  from  the 
henselion,  if  once  defined  and  fixed,  may  l)e  utilized  in  a  second 
case  of  similar  character. 

The  length  of  tlie  l)ony  palate  is  a  measurement  given  hy  all 
careful  descrihers,  hut  tlu.'  anterior  measuring  point  used  is  again 
either  the  gnathion  or  henselion,  doubt  as  to  which  is  l)eing 
used  often  nullifying  the  valu(^  of  the  measurement  altogether.* 
To  avoid  this  doubt  T  would  suggest,  exactly  as  in  the  other 
case,  that  the  name  of  the  measurement  from  the  gnathion 
should  end  in  "  al  "  and  tliat  from  the  henselion  in  "ilar." 
We  should  then  liave: 

Palatal  LE\(/rn,  the  distance  from  gnathion  to  palation. 

Palatilar  LEX(iTii,  the  distance  from  henselion  to  palation. 

The  indeterminate  "  palate  length  "  would  then  be  dropped 
altogether. 

II.  The  Names  of  the  Cheek-teeth  of  Mammals. 

Although  the  cheek-teeth  of  mammals,  the  molars  and  pre- 
molars, have  l)een  studied  and  written  about  ever  since  the  birth 
of  zoology,  no  uniform  system  of  naming  them  has  been  evolved 
and  there  is  the  greatest  divergence  between  the  usage  of  differ- 
ent workers  on  the  subject.  In  old  days  all  were  called  molars 
or  grinders;  tluMi  the  premolars  were  distinguished  from  the 
true  molars  (although  French  zoologists,  Winge  in  Denmark, 
and  Ameghino  in  Argentina,  continued  to  use  a  continuous 
notation  for  the  two  sets  of  teeth  combined)  and  the  usual  habit 
among  zoologists  in  general  was  to  speak  of  them  individually 
as  "  second  premolar,"  "  third  molar,"  and  soon.  Even  here, 
however,  an  important  difference  cropped  up  owing  to  Hensel 

*  I  may  explain  that  in  my  own  descriptions  the  palate  of  any  given  animal  has  al- 
ways been  measnred  from  tlie  same  anterior  point,  gnathion  or  henselion,  as  the  skull 
itself,  this  latter  being  indicated  by  the  use  of  the  words  basal  or  basilar. 


14 


Thomas — Nomenclature  of  Measurements.  195 

and  his  school  in  lu'rnuiny  numbering  the  premolars  from  be- 
hind forwards,  while  naturalists  of  other  nations  counted  from 
before  backwards,  as  with  the  incisors  and  molars,  a  difference 
often  productive  of  fatal  confusion. 

Of  late  years,  however,  partly  owing  to  an  increasing  concensus 
of  opinion  that  the  seven  cheek-teeth  of  Placentals,  four  pre- 
molars and  three  molars,  are  serially  and  individually  homolo- 
gous with  the  seven  of  Marsupials,  formerly  reckoned  as  three 
premolars  and  four  molars,  many  naturalists  have  again  begun 
to  think  that  a  continuous  numeration  might  be  the  best  one. 

But  the  difficulties  in  the  way  of  its  adoption  are  very  great, 
largely  owing  to  the  a])sence  of  any  convenient  and  suitable  word 
in  English  less  clumsy  than  "  cheek-tooth,"  to  express  a  tooth 
of  the  combined  premolar  and  molar  series.  To  speak  of  the 
"  first  cheek-tooth  "  or  of  the  "  predecessor  to  the  fourth  cheek- 
tooth "  would  l)e  so  retrogressive  a  step  that  I  am  sure  no 
one  would  adopt  it.  But  if  instead  of  trying  to  find  a  word 
for  the  series  combined  with  a  numeral  to  show  the  position, 
we  were  to  have  a  name  for  each  tooth,  we  should  get  some- 
thing of  the  immense  convenience  we  have  all  realized  in  having 
definite  names  for  the  canine  and  the  carnassial  teeth,  the  latter 
name  being  found  of  value  in  spite  of  the  fact  that  the  upper 
and  lower  carnassials  are  not  homologous  with  each  other.  Such 
names  might  be  made  from  the  positions  of  the  teeth  if  their 
meanings  were  not  so  obtrusive  as  to  confuse  the  minds  of  per- 
sons who  do  not  readily  understand  how  a  tooth  should  be  called 
' '  the  second  "  or  "  secundus  ' '  when  it  is  actually  the  most  an- 
terior of  the  series. 

Now  it  fortunately  happens  that  while  the  Latin  terms  ' '  pri- 
mus, "  "  secundus, ' '  etc, ,  express  the  serial  positions  too  clearly 
for  the  convenience  of  weak  minds.  Latinized  Greek  terms  have 
just  about  the  right  amount  of  unfamiliarity  which  would  enable 
them  to  be  used  as  names  without  their  serial  origin  being  too 
much  insisted  on,  IVIoreover,  their  construction  is  similar  to 
the  process  we  all  use  in  making  generic  names,  and  so  far  as  I 
know  they  have  never  been  previously  utilized  in  zoology. 

Then,  after  Latinizing  the  Greek  ordinal  terms  -ptoru^^  etc. 
for  the  cheek-teeth  of  the  upper  jaw,  the  same  modification  as 
is  already  used  in  cusp  nomenclature  might  be  adopted  for  those 
of  the  mandible. 


15 


196 


Thomas — Nomenclature  of  Measurements. 


We  should  thus  have,  counting  from  before  backwards: 


UPPER  JAW. 

LOWER  JAW 

Cheek-tooth  1 

Protus 

Protid 

2 

Deuterus 

Deuterid 

3 

Tritus 

Tritid 

4 

Tetartus 

Tetartid 

5 

Pemptus 

Pemptid 

6 

Hectus 

Hectid 

7 

Hebdonius 

Heljdoniid 

To  avoid  any  doubt,  I  would  expressly  allocate  these  names 
to  the  permanent  teeth  of  placentals,  leaving  the  names  of  the 
marsupial  teeth  to  be  settled  in  accordance  with  their  placental 
homologies. 

For  the  milk  teeth  a  further  modification  would  l;)e  available 
by  prefixing  the  syllable  Pro-  to  the  names  of  the  respective 
permanent  teeth.  We  could  thus  for  example  in  the  case  of  a 
third  lower  milk  premolar  call  it  tlie  protritid,  and  so  use  one 
word  instead  of  foui'. 

Of  course  I  have  no  supposition  that  this  system  would  ever  be 
frequently  or  generally  used,  l)ut  I  am  convinced  that  in  many 
special  cases,  and  particularly  in  such  descriptions  and  cata- 
logues of  isolated  teeth  as  paleontologists  often  liave  to  give,  it 
might  result  in  considerable  convenience  and  saving  of  space. 


16 


CRITERIA  FOR  VERTEBRATE  SUBSPECIES, 
SPECIES  AND  GENERA:  THE  MAMMALS 

By 

E.  Raymond  Hall 

University  of  California,  Berkeley,  California 

Mr.  Chairman,  members  of  the  American  Society  of  Ichthyologists  and 
Herpetologists,  members  of  the  American  Society  of  Mammalogists,  and 
guests:  We  had  expected  as  a  speaker  at  this  time  one  of  the  senior 
mammalogists  who  now  is  unable  to  attend.  I  am  glad  to  appear  as  a 
substitute  because  the  subject  under  discussion  is  one  in  which  I  am 
especially  interested.  In  these  extemporaneous  remarks  I  propose:  (1) 
to  indicate  some  steps  which  I  think  useful  to  take  in  classifying  mam- 
malian .specimens  as  to  subspecies;  (2)  to  express  my  personal  views 
as  to  criteria  for  subspecies,  species,  and  genera  of  mammals;  (3)  to 
illustrate  how  some  of  these  criteria  for  subspecies  and  species  may  be 
applied  to  closely  related  insular  kinds  of  mammals;  and  (4)  to  suggest 
a  way  in  which  subspecies  may  disappear  without  becoming  extinct. 

When  I  undertake  to  classify  mammalian  specimens  as  to  subspecies 
or  species,  or  when  I  present  a  series  to  a  beginning  student  for  classifica- 
tion, I  like  to  observe  the  following  steps:  (a)  select  for  initial,  intensive 
study  a  large  series,  30  or  more  individuals,  from  one  restricted  locality; 
(b)  segregate  these  by  sex;  (c)  arrange  specimens  of  each  sex  from  oldest 
to  youngest;  (d)  divide  these  into  age-groups  and  within  a  given  group, 
of  one  sex,  from  one  locality,  of  what  is  judged  to  be  one  species,  measure 
the  amount  of  so-called  individual  variation;  (e)  with  this  measurement 
as  a  "yardstick,"  compare  individuals,  and  if  possible  series,  comparable 
as  to  sex  and  age  (and  seasons  where  characteristics  of  the  pelage  are 
involved)  from  this  and  other  localities.  The  differences  found  are 
usually  properly  designated  as  geographic  variations  and  form  the  basis 
for  recognition  of  subspecies,  which  in  turn  comprise  one  of  the  tools  used 
by  some  students  of  geographic  variation. 

As  to  criteria  for  the  recognition  of  genera,  species  and  subspecies  of 
mammals,  it  seems  to  me  that  if  crossbreeding  occurs  freely  in  nature 
where  the  geographic  ranges  of  two  kinds  of  mammals  meet,  the  two 
kinds  should  be  treated  as  subspecies  of  one  species.  If  at  this  and  all 
other  places  where  the  ranges  of  the  two  kinds  meet  or  overlap,  no  cross- 
breeding occurs,  then  the  two  kinds  are  to  be  regarded  as  two  distinct, 
full  species.     The  concept  of  a  species,  therefore,  is  relatively  clear-cut 

(141) 


17 


142  ANNALS  NEW  YORK  ACADEMY  OF  SCIENCES 

and  precise;  the  species  is  a  definite  entity.  Furthermore,  if  a  zoologist 
knows  the  morphological  characteristics  diagnostic  of  the  species,  he  has 
no  difficulty  in  identifying  a  particular  individual  as  of  one  species  or 
another.  In  identification  of  subspecies,  difficulty  is  frequently  en- 
countered, especially  with  individuals  which  originate  in  an  area  of 
intergradation. 

The  category  next  higher  than  the  species,  namely,  the  genus,  is  less 
definite  and  more  subjective  as  regards  its  limits  than  is  the  species.  As 
the  species  is  the  definite,  clear-cut  starting  point  for  defining  subspecies, 
the  species  is  likewise  the  starting  point  for  consideration  of  genera. 
Degree  of  difference  is  the  criterion  for  a  genus.  The  genus  lies  about 
midway  between  the  species  and  the  family.  Because  the  limits  of  the 
family,  like  those  of  the  genus,  are  subjective,  it  follows  that  the  criterion 
for  recognition  of  genera,  although  precise  enough  at  the  lower  point  of 
beginning,  the  species,  is  elastic  at  the  upper  end — namely,  at  the  level 
of  the  family. 

In  summary,  the  criterion  for  subspecies  is  intergradation,  that  for 
species  is  lack  of  intergradation,  and  that  for  genera  is  degree  of  difference. 
These  ideas  agree  in  general  with  the  ideas  expressed  by  the  previous 
speakers. 

One  of  the  situations  in  which  it  is  difficult,  or  impossible,  to  apply 
these  criteria  to  conditions  actually  existing  in  nature  is  comprised  in 
some  insular  populations.  Frequently  the  populations  on  two  islands 
near  each  other  differ  enough  to  warrant  subspecific  or  possibly  specific 
distinction.  A  means  of  deciding  on  specific  versus  subspecific  status  for 
these  populations  is  to  find  on  the  adjacent  mainland  a  continuously  dis- 
tributed, related  kind  of  mammal  which  there  breaks  up  into  subspecies. 
Ascertain  the  degree  of  difference  between  each  pair  of  mainland  sub- 
species which  intergrade  directly.  If  the  maximum  degree  of  difference 
between  the  insular  kinds  is  greater  than  the  difference  between  the  two 
subspecies  on  the  mainland,  which  intergrade  directly,  and  greater  than 
that  between  either  insular  kind  and  the  related  population  on  the  nearby 
mainland,  the  two  insular  kinds  may  properly  be  treated  as  full  species. 
If  the  maximum  degree  of  difference  between  the  insular  kinds  is  no 
greater  than,  or  less  than,  the  difference  found  on  the  mainland  between 
pairs  of  subspecies  which  intergrade  directly,  the  insular  kinds  may 
properly  be  treated  as  subspecies  of  one  species.  In  fine,  the  criterion  is 
degree  of  difference  with  the  limitation  of  geographic  adjacency,  rather 
than  intergradation  or  lack  of  it. 

Now  to  my  fourth  point,  namely  the  suggestion  that  many  subspecies 
disappear  without  becoming  extinct.     Permit  me  first  to  observe  that 


18 


HALL:  CRITERIA  FOR  MAMMALS  143 

although  species  and  subspecies  seem  to  have  the  same  kinds  of  dis- 
tinguishing characters,  which  appear  to  be  inherited  by  means  of  essen- 
tially the  same  kinds  of  mechanisms  in  the  germ  plasm,  there  are  two 
noteworthy  differences  between  species  and  subspecies.  One  already 
implied  is  that,  in  a  species  which  is  continually  distributee!  over  a  given 
area,  its  characters  at  the  boundaries  of  its  range  are  sharp,  definite,  and 
precise.  Some  of  its  characters  comprised  in  size,  shape  and  color,  at 
any  one  place  are  either  those  of  one  species  or  instead  unequivocally 
those  of  some  other,  whereas  the  characters  of  a  subspecies,  particularly 
at  or  near  the  place  where  two  subspecies  meet,  more  often  than  not  are 
various  combinations  of  those  of  the  two  subspecies  and  in  many  indi- 
vidual characters  there  is  blending. 

Second,  through  a  given  epoch  of  geological  time  while  a  species  is  in 
existence,  one  or  more  of  its  subspecies  may  disappear  and  one  or  several 
new  subspecies  may  be  formed.  Subspecies,  therefore,  on  the  average 
are  shorter-lived  than  species. 

Now  the  disappearance  of  subspecies  is  to  be  expected  on  a  priori 
grounds  if  we  suppose  that  new  subspecies  are  formed  in  every  geological 
epoch.  There  is  reason  to  believe  that  in  the  Pleistocene,  the  epoch  of 
time  immediately  preceding  the  Recent,  there  were  even  more  species  of 
mammals  than  there  are  now.  In  each  of  several  successively  corre- 
sponding periods  of  Tertiary  time  before  the  Pleistocene,  probably  there 
were  as  many  species  as  now.  Probably  too,  these  species  then  were 
about  as  productive  of  subspecies  as  species  are  now.  Had  even  half  of 
these  subspecies  persisted,  either  as  subspecies  unchanged  or  in  con- 
siderable part  by  becoming  full  species,  there  would  now  be  an  array  of 
species  and  subspecies  many  times  as  numerous  as  actually  does  exist. 
It  is  obvious  therefore  that  many  disappeared. 

In  accounting  for  this  adjustment  of  numbers  of  kinds  of  mammals,  I 
have  spoken  of  the  disappearance  of  subspecies  rather  than  of  their  ex- 
tinction because  I  can  imagine  how  a  species,  say,  the  pocket  gopher 
Thomomys  townsendii,  in  the  middle  Pleistocene  with  three  subspecies 
(geographic  races)  could  have  come  down  to  the  present  by  means  of 
each  of  the  three  subspecies  having  gradually  changed  its  characters  into 
those  of  one  of  the  three  subspecies  existing  today  in  the  area  of  northern 
Nevada  that  I  have  in  mind.  In  this  way,  disappearance  of  subspecies 
living  in  the  Pleistocene  has  been  accomplished,  without  their  having 
become  extinct  in  the  sense  that  the  subspecies  left  no  living  descendants. 
Of  course  this  has  to  be  true  for  some  of  the  subspecies  of  each  successively 
preceding  epoch  if  any  animals  at  all  persist,  but  what  I  wish  to  empha- 
size is  the  strong  probability  that  many,  perhaps  more  than  50  per  cent, 


19 


144  ANNALS  NEW  YORK  ACADEMY  OF  SCIENCES 

disappeared  thus  without  actually  becoming  extinct,  when,  for  example, 
two  successive  stages  of  the  Pleistocene,  south  of  the  ice  sheet,  are  con- 
sidered. In  this  regard  it  is  pertinent  to  recall  that  each  of  three 
Pleistocene  kinds  of  pocket  gophers,  Thomomys  (probably  species  tal- 
poides)  gidleyi,  Thomomys  (probably  species  townsendii)  vetus,  and 
Thomomys  (probably  species  hottae)  scudderi,  from  a  short  distance  over 
the  northern  boundary  of  Nevada,  differs  from  living  representatives  cor- 
responding to  it  (several  subspecies  of  one  species)  in  greater  width  la- 
bially  of  the  individual  cheek  teeth  of  the  lower  jaw.  Significant  for  the 
thesis  being  defended  is  the  point  that  each  and  all  of  these  Thomomys  in 
the  Pleistocene  differed,  at  least  as  regards  the  shape  of  the  teeth,  in  the 
same  way  from  the  three  living  species  which  I  feel  confident  are  their 
descendants. 

Let  us  suppose  that  three  hypothetical  subspecies  of  Thomomys 
townsendii  in  middle  Pleistocene  time  each  gradually  changed  into  three 
different  subspecies  inhabiting  about  the  same  areas  in  upper  Pleistocene 
time,  and  that  these  in  turn  were  the  ancestors  of  the  three  subspecies 
living  in  those  same  general  areas  today.  A  total  of  nine  kinds  is  thus 
accounted  for.  At  any  one  time  there  was  geographical  intergradation, 
which  has  reference  to  horizontal  direction.  Also  there  was  intergrada- 
tion up  through  time,  which  has  reference  for  present  purposes  to  a 
vertical  direction.  If  I  had  before  me  all  the  material  necessary  to  sub- 
stantiate this  or  a  similar  case,  I  would  be  inclined  to  recognize  nine  sub- 
species of  one  species.  This  hypothetical  case  emphasizes  the  import- 
ance of  intergradation,  the  criterion  for  subspecies. 

In  review :  I  have  mentioned  some  preliminary  steps  useful  for  a  person 
to  take  when  he  aims  to  analyze  variation  in  mammals  and  to  establish 
species  and  subspecies  thereon;  intergradation  is  the  criterion  for  sub- 
species and  degree  of  difference  is  the  criterion  for  genera;  degree  of 
difference  with  the  limitation  of  geographic  adjacency  may  be  used  as 
the  criterion  for  insular  populations  (the  classification  of  which  is  doubt- 
ful as  between  subspecies  and  species);  and,  finally,  I  have  sought  to 
stress  the  importance  of  intergradation  as  a  criterion  for  subspecies  by 
showing  how  subspecies  may  disappear  without  becommg  extinct. 


20 


The  Nature  of  Subspecies  Boundaries 
in  a  Desert  Rodent  and  its  Implications 
for  Subspecies  Taxonomy 


WILLIAM  Z.  LIDIGKER,  JR. 


IT  SEEMS  to  me  that  the  wide  diversity 
of  opinion  which  exists  concerning  the 
usefulness  of  trinomial  nomenclature  re- 
volves in  large  measure  on  the  more  basic 
issue  of  whether  or  not  it  is  possible  to 
recognize  infraspecific  categories  which 
reflect  genetic  relationships.  As  recently 
pointed  out  by  Sneath  (1961),  taxonomic 
categories  which  are  not  based  on  rela- 
tionships are  thereby  rankless  and  cannot 
logically  be  included  in  a  taxonomic 
hierarchy.  Thus  if  the  subspecies  cate- 
gory is  used  merely  as  an  instrument  for 
describing  geographic  variation  in  a  few 
characters  or  as  a  device  for  cataloging 
geographic  variants  (as  is  done  by  many 
taxonomists),  artificial  classifications  of 
convenience  are  characteristically  pro- 
duced. Such  convenience  classifications 
usually  contain  rankless  groups  (the 
"false  taxa"  of  Sneath)  which  cannot  be 
allocated  in  the  taxonomic  hierarchy.  This 
is  simply  because  categories  based  on  a 
few  arbitrary  characters  are  themselves 
arbitrary,  and  lead  to  the  objection  of 
Brown  and  Wilson  (1954)  and  others  that 
trinomials  based  on  one  group  of  char- 
acters need  not  bear  any  relation  to  those 
based  on  different  traits.  Many  of  the 
same  philosophical  difficulties  apply  to 
systems  such  as  that  recently  proposed 
by  Edwards  (1954)  and  Pimentel  (1959) 
in  which  the  subspecies  would  become  a 
measure  of  isolation,  by  restricting  its  use 
to  completely  isolated  and  "obviously  dif- 
ferent" populations. 

If  on  the  other  hand  studies  of  infra- 
specific  populations  are  focused  on  dis- 
covering evolutionary  diversity  or  degrees 
of  relationship  between  the  various  popu- 


lations, I  see  no  philosophical  objection 
to  the  use  of  the  trinomen.  The  question 
then  reduces  to  one  of  the  feasibility  and/ 
or  desirability  of  searching  for  such  rela- 
tionships, and  of  deciding  what  level  of 
dissimilarity  if  any  justifies  use  of  the 
formal  trinomen.  It  is  primarily  these 
two  subsidiary  questions  which  are  ex- 
amined in  this  paper,  with  the  frank  hope 
that  the  subspecies  can  be  rescued  from 
the  rankless  limbo  of  the  morph,  ecotype, 
and  form.  If  this  rescue  operation  should 
prove  successful,  attention  can  then  be 
directed  to  other  problems  of  greater  bio- 
logical interest,  such  as  whether  or  not 
determinations  of  genetic  relationships 
within  a  species,  which  are  based  on 
phenotj^es,  can  serve  as  a  basis  for  specu- 
lations on  phylogeny.  Obviously  geogra- 
phic relations  would  have  to  be  con- 
sidered at  this  level,  but,  assuming  that 
such  information  is  taken  into  account,  it 
would  be  highly  informative  to  contrast 
phenetic  and  phylogenetic  subspecies 
classifications.  In  any  case,  analyses  of 
infraspecific  relationships  would  very 
likely  provide  valuable  clues  concerning 
the  environmental  forces  which  have  in- 
fluenced the  development  of  the  existing 
evolutionary  diversity. 

In  a  previous  paper  (1960)  I  attempted 
to  determine  the  genetic  relationships 
among  populations  within  a  species  of 
kangaroo  rat  (Dipodomys  merriami 
Mearns,  1890)  by  a  careful  analysis  of  20 
morphological  features.  I  concluded  at 
that  time  that  at  least  in  well-known  ter- 
restrial species  an  attempt  to  recognize 
relative  relationships  within  a  species  was 
at  least  possible.  And,  at  the  same  time  it 


21 


SUBSPECIES  BOUNDARIES 


161 


was  apparent  that  (besides  the  philosophi- 
cal objections  already  pointed  out)  the 
subspecies  category  by  itself  was  com- 
pletely inadequate  for  describing  the 
complex  geographic  variation  occurring 
in  that  species.  It  is  the  raw  data  from 
this  former  investigation  that  I  have  used 
here  to  test  further  the  reliability  of  those 
tentative  conclusions. 

The  search  for  relationships  among 
populations  of  the  same  species  implies  a 
search  for  total  genetic  differentiation  (or 
at  least  its  phenotypic  manifestations), 
and  hence  of  lineages  with  partially  in- 
dependent evolutionary  origins  such  that 
they  have  some  internal  homogeneity  and 
their  own  adaptive  tendencies.  To  detect 
this  kind  of  differentiation  it  seems  impor- 
tant to  analyze,  among  other  things,  the 
populations  occurring  at  the  boundaries 
between  differentiating  groups,  just  as  in 
the  analysis  of  species  relationships  it  is 
the  boundaries  between  them,  or  areas  of 
sympatry,  where  the  most  significant  in- 
formation on  relationships  is  to  be  found. 
This  is  not  to  say  that  information  con- 
cerning the  regions  of  greatest  divergence 
or  adaptive  peaks  (in  this  case  peaklets) 
of  infraspecific  populations  is  not  impor- 
tant, but  only  that  such  data  should  not 
be  the  only  source  material  for  taxonomic 
judgments.  Thus  it  is  the  intent  of  this 
paper  to  focus  attention  on  the  previously 
all  but  ignored  subspecies  boundaries, 
and  to  examine  the  nature  of  these  areas 
in  Dipodomys  merriami  as  I  had  pre- 
viously and  without  the  benefit  of  this 
analysis  defined  them  (Lidicker,  1960). 
Because  the  determination  of  these  intra- 
specific  units  was  guided  in  this  case  by 
a  desire  to  find  populations  of  comparable 
evolutionary  relationship,  careful  scrutiny 
of  the  intergrading  zones  between  them 
and  surrounding  areas  should  be  of  par- 
ticular interest.  Comparisons  will  also 
be  made  with  levels  of  differentiation  in 
areas  in  which  no  subspecies  boundary 
was  recognized,  as  well  as  with  one  re- 
gion in  which  species  level  differentiation 
was  postulated  to  have  been  reached  by 
an  island  isolate. 


The  second  and  related  purpose  of  the 
paper  is  to  describe  a  method  which  helps 
to  accomplish  the  first  objective  by  meas- 
uring total  differentiation,  or  lack  of 
similarity,  in  many  diverse  characters, 
and  hence  is  proposed  as  a  criterion  of 
relationship.  But  at  the  same  time  the 
technique  does  not  require  the  hard 
working  taxonomist  to  have  either  access 
to  a  digital  computer  or  facility  with 
matrix  algebra. 

The  Method 

Most  quantitative  techniques  available 
to  the  systematist,  which  concern  them- 
selves with  determining  relationships, 
and  hence  with  similarities  as  well  as  dif- 
ferences, either  involve  the  analysis  of 
qualitative  or  discontinuous  characters 
and  thus  are  most  useful  at  the  species  or 
genus  level  (e.g.,  Michener  and  Sokal, 
1957;  Lysenko  and  Sneath,  1959),  or  in- 
volve calculations  sufficiently  complex 
(e.g.,  Williams  and  Lance,  1958)  that  they 
are  avoided  by  most  practicing  systema- 
tists.  What  seems  to  be  needed  is  an  ad- 
ditional technique  which  is  sufficiently 
adaptable  to  handle  continuously  variable, 
as  well  as  discontinuous,  characters  of 
diverse  types  (and  so  is  useful  in  infra- 
specific  studies),  and  which  at  the  same 
time  is  sufficiently  practical  that  it  will  be 
widely  useful.  To  this  end  the  following 
proposed  method  is  dedicated.  It  is  not 
intended  as  a  substitute  for  discriminant 
function  analysis  (Fisher,  1936;  Jolicoeur, 
1959)  and  related  methods  which  attempt 
to  discriminate  between  previously  con- 
ceptualized populations  by  using  combina- 
tions of  variables. 

An  analysis  of  relationship  should 
ideally  compare  relative  similarities  and 
not  differences.  However,  since  the  num- 
ber of  similarities  between  populations 
within  a  species  is  very  large,  it  is  much 
easier  to  measure  their  differences  and 
consider  that  the  reciprocal  of  the  amount 
of  difference  represents  a  measure  of 
similarity.  Thus  as  the  amount  of  differ- 
ence approaches  zero,  the  reciprocal  ap- 


22 


162 


SYSTEMATIC  ZOOLOGY 


preaches  infinity.    The  problem  then  be- 
comes  one   of   summing   the  amount   of 
difference  in  many  diverse  characters.  To 
do  this  we  must  be  able  to  express  the 
differentiation  for  each  trait  by  a  pure 
number   (no  units).    Cain  and  Harrison 
(1958),    for   example,    accomplished   this 
by   dividing  the  differences  which  they 
observed  between  means  by  the  maxi- 
mum value  recorded  for  each  character. 
The  resulting  ratios,  which  they  called 
"reduced  values,"  express  the  observed 
differences  in  terms  of  a  fraction  of  the 
maximum    size    of    each    character.     Al- 
though  this   permits  the  comparison  of 
diversity  among  traits  of  different  abso- 
lute size,  it  does  not  take  into  account 
either  the  possibility  that  various  char- 
acters  may   have   different  variabilities, 
or  the  statistical  significance  of  the  ob- 
served  mean    differences.    Furthermore, 
maximum  size  would  seem  to  be  a  statistic 
of  dubious  biological  importance  in  con- 
tinuously   varying    characters.     On    the 
other  hand,  all  of  these  important  vari- 
ables, the  variance  of  each  trait,  character 
magnitude,  as  well  as  a  consideration  of 
whether  or  not  mean  differences  have  a 
high  probability  of  representing  real  dif- 
ferences, are  taken  into  account  by  ex- 
pressing  differentiation  as  a   proportion 
between  the  observed  differences  between 
samples  and  the  maximum  amount  of  dif- 
ference expected  on  the  basis  of  chance 
sampling   variation.     Only    mean    differ- 
ences greater  than   that  amount  which 
may  be  due  to  chance  would  then  be  con- 
sidered as  real  differences.    For  our  pur- 
poses the  maximum  chance  variation  ex- 
pected in  any  comparison  can  be  equated 
to  the  minimum  difference  required  for 
statistical  significance  (at  any  given  con- 
fidence level).   This  minimum  significant 
difference   (msd)  can  be  calculated  in  a 
number  of  ways.    One   possibility   is   to 
determine  the  standard  error  of  the  mean 
for  each  character  for  each  sample.  Then 
in  comparing  two  samples  for  this  char- 
acter, 2  SEj  +2SF,^_^  =  msd.  This  provides 
a  conservative  estimate  of  msd  with  con- 
fidence limits  usuallv  well   in  excess  of 


95%.  For  large  studies,  however,  these 
calculations  would  be  extremely  laborious, 
as  well  as  perhaps  overly  conservative, 
and  a  short-cut  is  suggested. 

If  we  can  assume  that  each  quantitative 
character  in  a  given  species  exhibits  a 
characteristic  variability   throughout  its 
range,    then   calculations   would   be   tre- 
mendously reduced  if  we  were  able  to  de- 
termine the  expected  or  pooled  standard 
deviation    (5,,)   and  standard  error   (Sp_) 
of  samples  for  which  say  r2>20.    Very 
small  samples  would  have  to  be  grouped 
with  adjacent  samples  whenever  possible, 
or  if  necessary   either  ignored   or  have 
separate  msd-values  calculated  for  them. 
Under  these  conditions  4sp_represents  our 
best  estimate  of  Tusd.  Unfortunately  con- 
fidence limits  cannot  be  calculated  for  its 
reliability,  although  again  it  is  generally 
a  conservative  estimate.    The  statistic  Sp 
can  be  conveniently  determined  by  averag- 
ing the  weighted  variances  for  several 
samples    of   adequate   size    (Hald,    1952: 
395).  Note  that  as  the  estimate  of  s^  im- 
proves it  approaches  the  population  stand- 
ard deviation  (a),  and  hence  is  applicable 
to  a  wider  range  of  sample  sizes.    Better 
estimates  of  Sp  require  knowledge  of  the 
total  number  of  individuals  in  each  of  the 
populations  sampled  (see  Cochran,  1959: 
72),  an  obvious  impossibility  in  this  type 
of  problem.  In  the  examples  given  in  this 
paper  45  p.  was  estimated  by  using  the 
standard  deviation  of  one  large  sample 
collected  near  the  center  of  the  species' 
range,  and  by  assuming  n  =  20.    This  ex- 
pediency seemed  justified  because  of  the 
close  similarity  in  values  of  s  calculated 
for  a  given  trait  among  several  samples, 
and  because  of  the  likelihood  that  s  ap- 
proaches a  under  these  circumstances. 

Still  another  method  of  deriving  the 
statistic  msd,  but  one  not  used  in  this  re- 
port, involves  a  more  laborious,  but  sta- 
tistically more  precise,  procedure.  The 
confidence  limits  for  the  difference  be- 
tween any  pair  of  means  can  be  calcu- 
lated (see  Dixon  and  Massey,  1957:128) 
whether  or  not  we  assume  that  we  know 


23 


SUBSPECIES  BOUNDARIES 


163 


the  variance  characteristic  of  each  trait 
(s^)  or  use  only  the  pertinent  sample 
variances  (sj  and  s|).  For  a  large  study, 
the  calculations  are  very  much  reduced  if 
one  can  estimate  Sp  (see  above),  and  per- 
haps even  use  only  samples  in  which 
n>20.  If  these  simplifications  are  pos- 
sible, a  pair  of  confidence  limits  can  be 
computed  which  will  be  characteristic  for 
each  trait  studied.  In  either  case,  one  con- 
fidence limit  gives  us  our  msd,  since  mean 
differences  greater  than  this  can  with  a 
known  probability  be  considered  real.  We 
need  not  be  concerned  with  the  possibility 
that  the  mean  differences  are  even  larger 
than  those  observed. 

Consider  then  only  those  characters  in 
which  the  differences  in  the  mean  values 
(Xi— X2)  for  a  given  pair  of  locations 
(samples)  are  greater  than  the  minimum 
significant  differences.  Now,  divide  these 
significant  differences  in  mean  values  by 
the  minimum  significant  difference  char- 
acteristic for  that  trait  (or  for  that  pair 
of  samples).  This  procedure  gives  us  our 
pure  number  which  can  be  designated  as 

di,  d.,, dn  for  successive  characters, 

each  representing  a  measure  of  differen- 
tiation in  one  character  between  one  pair 
of  samples.  Having  defined  the  amount 
of  differentiation  in  each  character 
in  terms  of  a  pure  number,  we  can 
now  add  these  to  arrive  at  an  esti- 
mate of  total  differentiation  in  the  char- 
acters studied  (2c?i).  In  interpreting  this 
statistic  in  any  real  situation,  however,  it 
seems  apparent  that  the  distance  between 
the  two  samples  compared  should  be 
taken  into  account.  Obviously  an  amount 
of  total  differentiation  exhibited  between 
two  samples  which  are  close  together  geo- 
graphically would  be  more  significant 
than  the  same  amount  of  differentiation 
between  samples  geographically  distant. 
To  compensate  for  this  effect  of  distance, 
I  have  divided  the  total  differentiation 
by  the  distance  (in  miles)  between  the 
two  samples.  The  resulting  figure,  which 
I  have  called  D  or  the  Index  of  Differen- 


tiation,^  represents  the  proportion  of  sig- 
nificant change  that  occurs  between  the 
two  locations  per  mile.  Then  the  re- 
ciprocal of  D  easily  gives  us  our  measure 
of  similarity  between  populations.  D  need 
now  only  be  further  divided  by  the  total 
number  of  characters  studied,  including 
those  of  course  in  which  no  differentia- 
tion occurred,  to  arrive  at  the  mean  char- 
acter differentiation  per  mile  {MCD/mi.). 

The  importance  of  considering  distance 
between  samples  will  depend  in  large 
measure  on  the  specific  problem  under  in- 
vestigation. Obviously  air-line  distance 
between  samples  does  not  always  accu- 
rately reflect  the  real  magnitude  of  the 
distance  or  barriers  between  them.  I  feel 
that  this  is  not  a  serious  difficulty,  how- 
ever, since  we  are  concerned  with  the 
abruptness  of  differentiation  between  ad- 
jacent populations  and  not  with  barriers 
per  se.  Moreover,  in  some  ways  D  acts  as 
a  measure  of  restriction  on  gene  flow,  be- 
cause, if  distance  is  kept  constant,  D  will 
tend  to  increase  as  gene  flow  is  reduced. 
Another  potential  difficulty  with  the  dis- 
tance calculation  is  that  it  carries  the 
assumption  that  if  the  two  localities  be- 
ing compared  were  actually  closer  to- 
gether, the  amount  of  total  differentiation 
shown  would  be  less.  This  is  not  always 
true  because  not  only  are  there  sometimes 
large  areas  which  exhibit  very  little  geo- 
graphic variation,  but  also  there  exist  un- 
avoidable gaps  in  specimen  collections. 
For  these  reasons  I  felt  that  in  the  pres- 
ent analysis  of  D.  merriami  it  was  neces- 
sary to  consider  both  2c?i  and  B  in  assess- 
ing differentiation. 

One  further  complication  seems  worth 
considering.  This  concerns  variation  in 
the  direction  of  change  between  different 
characters.  It  seemed  to  me  more  signifi- 
cant if  one  or  two  characters  were  found 
to  change  significantly  in  a  direction  op- 
posite to  that  of  the  other  characters, 
than  if  they  all  changed  in  the  same  di- 


1  Note  that  this  is  in  no  way  similar  to  the 
"differentiation  index"  of  Kurten  (1958) 
which  compares  growth  gradients. 


24 


1G4 


SYSTEMATIC  ZOOLOGY 


rection.  Thus  for  each  such  direction 
change,  I  arbitrarily  added  one  half  the 
(Z-value  for  that  specific  character  to  2d. 
This  also  serves  to  oppose  any  tendency 
to  give  too  much  weight  to  characters 
which  may  not  be  entirely  independent  in 
their  variation,  or  to  those  varying  allo- 
metrically.  Otherwise  no  allowance  has 
been  made  for  differentially  weighting 
characters  which  might  be  considered  to 
have  greater  phylogenetic  importance. 
Presumably  this  could  be  readily  done,  if 
there  were  some  sound  basis  for  making 
such  judgments.  Sneath  ( 1961 ) ,  however, 
points  out  some  of  the  dangers  inherent 
in  attempts  to  do  this,  and  argues  for 
considering  each  character  equally. 

Table  1  summarizes  the  calculations 
for  2<i,  D,  and  MCD/mi.  for  one  pair  of 
localities  in  southeastern  Arizona.  Note 
that  a  value  of  3.476  has  been  included  in 
2d  for  color  changes.  Ordinarily  color 
characters  should  be  quantified  so  that 
they  can  easily  be  added  into  this  scheme. 
Unfortunately  in  my  study,  I  did  not 
quantify  in  numerical  terms  the  six  color 
features  analyzed.  This  necessitated  my 
determining  when  significant  changes 
had  occurred  by  reference  to  the  color 
descriptions  of  each  sample.  Whenever 
important  color  changes  were  found  be- 


tween samples,  I  included  in  2d  for  each 
such  change  a  figure  which  represented 
the  average  d-value  for  all  pairs  of  locali- 
ties in  the  boundary  region  under  study 
which  exhibited  the  same  number  of  color 
changes  as  the  sample  pair  being  calcu- 
lated. For  example,  if  two  samples  dif- 
fered in  three  color  features  and  if  the 
average  d  for  all  pairs  of  samples  in  that 
region  which  also  differed  by  three  color 
features  was  1.50,  then  4.5  (3  x  1.50) 
would  represent  the  combined  value  of  d 
for  the  three  color  traits.  Although  this 
represents  an  unfortunate  complication, 
it  should  not  detract  from  the  validity  of 
the  overall  method  being  proposed. 

Figures  1,  2,  and  3  show  the  differentia- 
tion observed  in  20  characters  in  D.  mer- 
riami  in  selected  portions  of  its  large 
range.  It  is  important  to  emphasize  that 
these  20  characters  were  chosen  in  the 
original  investigation  (Lidicker,  1960) 
independently  of  the  conclusions  of  other 
authors  concerning  what  they  considered 
important  characters  in  distinguishing 
subspecies.  The  list  thus  includes  not 
only  most  of  the  "taxonomically  impor- 
tant" characters  of  other  authors  but 
numerous  additional  features  as  well.  I 
chose  for  illustration  regions  which  dem- 
onstrate various  levels  of  differentiation 


Table  1 — Calculations  for  Total  Differentlation,  the  Index  of  Differentiation,  and  the 
Mean  Character  Differentiation  per  Mile  in  Dipodomys  merriami  for  a  Pair  or 
Localities  in  Southeastern  Arizona  (Vicinities  of  the  Huachuca  and  Santa  Rita 
Mountains  54  Miles  Apart). 


character  * 

Xi- 

-Xa(mm.) 

msd 

d. 

hind  foot  length 

ear  length 

basal  length  of  the  skull 

cranial  length 

rostral  width 

1  direction  change  (ear) 

2  color  changes 

1.40 

0.62 

0.54 

0.78 

0.19 

(ids) 
(2Xd  for  those  pairs  of 
localities  with  two  color 
changes) 

0.68 
0.52 
0.52 
0.48 
0.06 

2di 
D 

MCD/mi. 

2.059 
1.192 
1.039 
1.625 
3.167 
0.596 

3.476 

=  13.154 
=    0.244 
=    0.012** 

*  See  Lidicker  (1960)  for  a  description  of  these  characters. 
*♦  Total  of  20  characters  studied. 


25 


SUBSPECIES  BOUNDARIES 


165 


>.40(>20) 

>.35(>l5)or>40«20) 
>.25{>IO)or>.35«l5) 
>.20(>IO)or>.25(<IC) 
>.l5{>IO)or>.20{<IO) 
>.IO(>IO)or).l5  (<I0) 
>.05(>5)or>.IO(<IO) 
<.05  or  >.05«5) 
.00  (0) 


Fig.  1.  Observed  diflferentiation  of  Dipodomys  merriami  in  southeastern  Arizona  and 
adjacent  Mexico  and  New  Mexico.  Numbers  on  the  lines  connecting  the  various  sample 
localities  represent  the  calculated  values  for  D  and  in  parenthesis  Sd,.  The  key  to  the 
intensity  of  stippling  is  based  on  these  same  statistics.  The  scale  associated  with  each  map  rep- 
resents a  distance  of  25  miles.  See  also  the  text  for  a  more  complete  explanation  of  the  figures. 


26 


!6G 


SYSTEMATIC  ZOOLOGY 


"^S  %_oo'.oQ^' 


Las  Vegas 


\   Aguongo 


Fallon  X 

Fig.  2.  Observed  differentiation  of  D.  merriann  in  a)  northern  Nevada,  b)  southern 
Nevada  and  adjacent  Mojave  desert  of  California,  and  c)  small  area  in  extreme  southern 
California.  For  a  more  complete  explanation  of  the  figures  and  a  key  to  stippling  intensity, 
see  the  text  and  Figure  1. 


ranging  from  essentially  none  to  that 
judged  to  be  at  the  species  level.  Figure 
1  shows  the  boundary  region  between  D. 
merriami  merriami  and  D.  m.  olivaceus 
(nomenclature  based  on  Lidicker,  1960) 
in  southeastern  Arizona  and  adjacent 
Mexico  and  New  Mexico.  Figure  2  illus- 
trates areas  in  northern  Nevada  (a), 
southern  Nevada  and  the  adjacent  eastern 
Mojave  desert  of  California  (b),  and  fi- 
nally a  small  area  in  southern  California 
at  the  boundary  of  D.  m.  collinus  and  D. 
m.  arenivagus  (c).  Figure  3  represents 
the  southern  tip  of  the  Baja  California 
peninsula  (a),  and  southern  Sonora 
where  the  boundary  between  D.  vi.  mer- 
riami and  D.  m.  mayensis  is  found  (b). 


The  first  of  these  (3a)  is  of  particular  in- 
terest as  it  shows  the  entire  range  of  D. 
m.  melanurus  and  the  adjacent  island 
populations  of  D.  m.  margaritae  and  the 
presumed  allopatric  species  D.  insularis. 
Notice  that  the  key  takes  into  account 
both  D  and  2<i  (but  gives  greatest  weight 
to  D)  and  is  arranged  so  that  increased 
intensity  of  stippling  represents  increased 
differentiation.  Heavy  dashed  lines  repre- 
sent the  locations  of  previously  estab- 
lished subspecies  boundaries,  and  double 
dashed  lines  previously  established  spe- 
cies boundaries  (see  Lidicker,  1960). 
Each  drawing  also  indicates  the  location 
of  one  prominent  town  so  that  each  chart 
can  be  placed  geographically;  all  are  ori- 
ented with  north  upward. 


27 


SUBSPECIES  BOUNDARIES 


167 


Fig.  3.  Observed  differentiation  of  D.  merriami  in  a)  southern  Baja  California,  and 
b)  southern  Sonora.  For  a  more  complete  explanation  of  the  figures  and  a  key  to  stippling 
intensity,  see  the  text  and  Figure  1. 


Discussion  of  the  Method 

The  method  described  and  its  pictorial 
representation  as  shown  in  the  figures 
gives  us  a  geographically  oriented  sum- 
mary of  statistically  significant  differen- 
tiation in  the  characters  studied.  Its  most 
important  feature  is  that  it  takes  into  ac- 
count the  variability  of  each  character  as 
well  as  its  magnitude,  and  concerns  itself 
only  with  diversity  which  has  a  high 
probability  of  being  real.  Clearly,  the 
more  characters  examined  by  the  investi- 
gator, the  greater  will  be  his  chance  of 


discovering  all  of  the  existing  differences 
between  populations,  and  the  better  will 
be  his  estimate  of  genetic  diversity.  In 
the  present  case  there  is  a  remarkable 
correlation  between  the  subspecies  and 
species  boundaries  as  previously  de- 
scribed by  the  author  and  the  bands  of 
rapid  character  changes  as  defined  by  the 
Index  of  Differentiation.-  It  is  clear  that 
in  this  case  subspecies  boundaries  uni- 


2  No  particular  correlation  is  evident,  how- 
ever, with  many  of  the  taxonomic  conclusions 
of  previous  authors. 


28 


168 


SYSTEMATIC  ZOOLOGY 


formly  appear  as  relatively  narrow  zones 
of  high  levels  of  differentiation  or  low 
levels  of  similarity,  and,  although  it  can- 
not be  determined  from  the  figures,  these 
are  usually,  but  not  always,  in  areas  of 
partial  or  complete  isolation  between  pop- 
ulations. If  the  Index  method  truly  de- 
scribes genetic  diversity,  then  our  con- 
fidence is  bolstered  in  the  possibility  of 
using  the  subspecies  category  for  char- 
acterizing infraspecific  lineages. 

Besides  the  degree  of  differentiation, 
other  suggested  criteria  for  the  recogni- 
tion of  such  lineages  include  the  following 
considerations:  1)  the  continuity  of  the 
zone  of  differentiation;  2)  diversity  of  the 
two  postulated  adaptive  peaks;  3)  differ- 
ences in  the  environments  to  which  the 
adjacent  populations  are  adapted,  or  con- 
sideration of  the  possibility  that  the  two 
populations  are  adapted  to  the  same  en- 
vironment in  a  different  way;  4)  geologic 
or  paleontologic  evidence  of  separate  evo- 
lution. Moreover,  it  would  seem  to  be  a 
simple  matter  to  devise  modifications  of 
the  Index  of  Differentiation  so  as  to  in- 
corporate discontinuous  and  qualitative 
characters.  This  would  extend  the  useful- 
ness of  the  method,  not  only  to  infraspe- 
cific populations  which  differ  by  such 
characters,  but  also  to  the  species  level. 
However,  above  the  infraspecific  level  the 
problems  of  convergence,  giving  different 
weight  to  different  characters  (that  is 
identifying  primitive  or  generalized  char- 
acters), and  correlated  characters  (see 
especially  discussions  by  Cain  and  Harri- 
son, 1960)  are  aggravated.  It  might  be 
added  in  passing,  however,  that  these 
sources  of  error  are  not  so  great  a  prob- 
lem as  might  be  expected,  because  the 
proposed  method  emphasizes  large  num- 
bers of  characters  and  overall  similarities. 
Under  these  circumstances  a  few  con- 
vergent or  pleiotropic  traits  would  alter 
the  results  very  little.  Moreover,  the 
problem  of  differentially  weighting  char- 
acters often  leads  into  circular  arguments 
as  pointed  out  by  Sneath  (1961). 

Although  the  proposed  method  incor- 
porates a  number  of  compromises  with 


mathematical  sophistication,  I  think  that 
it  is  sufficiently  accurate  to  be  of  consid- 
erable utility  to  the  practicing  taxono- 
mist.  Furthermore,  several  modifications 
are  suggested  for  improving  precision  if 
this  seems  appropriate.  The  method  will 
not  of  course  make  any  decisions  for  the 
investigator,  as  it  should  not,  but  it  will 
give  him  additional  objective  criteria  on 
which  to  base  his  decisions.  The  fact  that 
the  conclusions  suggested  by  the  calcula- 
tions and  analysis  of  D's  are  similar  if  not 
identical  to  those  proposed  without  the 
benefit  of  the  method  suggests  that  the 
method  does  not  produce  unreasonable 
results,  and  therefore  must  not  suffer  un- 
duly from  its  lack  of  statistical  elegance. 

Discussion  of  Results 

An  obvious,  but  important,  conclusion 
derived  from  a  study  of  the  figures  is  that 
statistically  significant  differences  can  be 
found  between  the  vast  majority  of  the 
population  pairs.  This  serves  to  empha- 
size what  is  really  intuitively  obvious, 
namely  that  the  ability  to  prove  that  two 
populations  are  statistically  different  in 
one  or  several  characters  is  only  a  meas- 
ure of  the  persistence  and  patience  of  the 
systematist.  To  base  formal  subspecific 
descriptions  on  this  kind  of  evidence 
seems  to  me  to  be  almost  meaningless  as 
well  as  a  contribution  to  the  degradation 
of  the  subspecies  category  to  the  extent 
of  losing  it  as  a  legitimate  member  of  the 
taxonomic  hierarchy.  Furthermore,  this 
is  precisely  the  philosophy  which  usually 
seems  to  nurture  the  widespread  empha- 
sis on  naming  with  its  often  accompany- 
ing neglect  of  relationships,  which  has 
stimulated  so  much  critical  comment  (see 
for  example  Wilson  and  Brown,  1953,  and 
Gosline,  1954). 

The  description  of  differentiation  pro- 
vided in  the  figures  carries  the  further  im- 
plication that  all  levels  of  differentiation 
are  found  in  D.  merriami,  and  no  obvious 
dividing  line  between  subspecies  and  non- 
subspecies,  and  species  for  that  matter,  is 
thereby  indicated.  The  method  thus  gives 


29 


SUBSPECIES  BOUNDARIES 


169 


US  information  regarding  how  different 
(or  similar)  populations  are,  but  does  not 
tell  us  which  ones  we  should  call  subspe- 
cies. This  finding  is  consistent  with  cur- 
rent concepts  of  intraspecific  variation, 
and  permits  the  systematist  to  decide 
what  degree  of  relationship  has  phylo- 
genetic  significance  for  the  particular  or- 
ganism involved,  and  finally  what  level, 
if  any,  he  wants  to  recognize  with  formal 
subspecies  descriptions.  In  the  present 
example  subspecific  boundaries  are  found 
to  be  usually  associated  with  continuous 
bands  of  differentiation  characterized  by 
D-values  greater  than  0.15. 

The  fact  that  this  study  has  failed  to 
reveal  some  biologically  meaningful  divi- 
sion marking  the  subspecies  level  does 
not  mean  of  course  that  some  such  divi- 
sion will  not  be  possible  in  the  future. 
However,  such  a  line  of  demarcation  is 
obviously  not  a  prerequisite  to  the  success 
of  the  proposed  method,  which  only  con- 
cerns recognition  of  degrees  of  evolution. 
Nevertheless,  one  possible  criterion  for 
such  a  division  which  occurs  to  me  is  the 
relationship  between  the  observed  gene 
flow  between  two  adjacent  populations 
and  that  amount  expected  on  the  basis  of 
the  extent  of  physical  contact  existing 
between  them.  If  the  observed  gene  flow 
turned  out  to  be  less  than  that  expected, 
or  discriminating  in  terms  of  what  genes 
were  allowed  to  flow,  this  would  serve  as 
an  indication  that  partially  independent 
lineages  were  involved.  This  idea  would 
not  diminish  in  any  way  the  obvious  im- 
portance of  geographical  barriers  in  in- 
hibiting gene  flow,  but  merely  suggests 
that  some  day  it  may  be  possible  to  ask 
the  question — would  a  high  level  of  differ- 
entiation persist  between  two  geograph- 
ically partially  isolated  populations  if  the 
barrier  were  reduced  or  eliminated?  Or 
to  put  it  in  another  way,  how  much  re- 
duction in  the  physical  barrier  between 
them  can  these  two  populations  resist  be- 
fore gene  flow  becomes  free  flowing?  This 
genetic  concept  of  a  subspecies  argues 
that  there  are  numerous  infraspecific  pop- 
ulations which  by  virtue  of  their  past  iso- 


lation (not  necessarily  complete)  show 
some  inhibition  of  gene  flow  between 
them  and  their  neighbors,  which  would 
tend  to  slow  down  the  dedifferentiation 
process.  If  the  geographic  isolation  is 
current,  the  argument  must  be  stated  that 
such  a  reduction  in  gene  flow  would  occur 
if  they  were  not  so  isolated.  This  reason- 
ing is  merely  a  corollary  of  the  fact  that 
not  all  attempts  by  a  species  for  isolation 
and  differentiation  result  in  species  for- 
mation. There  are  a  number  of  reasons 
why  gene  flow  might  be  inhibited  in  such 
cases,  and  one  of  these  is  interdeme  ge- 
netic homeostasis  (Lerner,  1954).  Other 
factors  might  be  partial  ecological  or  be- 
havioral barriers  to  free  interbreeding. 
Although  this  suggestion  for  a  biologi- 
cally meaningful  subspecies  criterion  is 
mainly  speculative,  it  seems  to  me  to  be 
one  possible  direction  that  future  develop- 
ments in  intraspecific  analysis  might 
take.  The  following  definition  of  a  sub- 
species is  thus  perhaps  premature,  but 
is  offered  because  it  is  only  a  slight 
modification  of  widely  used  current 
definitions,  but  yet  incorporates  the  con- 
cept outlined  above;  at  the  same  time  it 
does  not  commit  one  to  any  specific  cri- 
teria for  the  recognition  of  subspecies.  A 
subspecies  is  a  relatively  homogeneous 
and  genetically  distinct  portion  of  a  spe- 
cies which  represents  a  separately  evolv- 
ing, or  recently  evolved,  lineage  with  its 
own  evolutionary  tendencies,  inhabits  a 
definite  geographical  area,  is  usually  at 
least  partially  isolated,  and  may  intergrade 
gradually,  although  over  a  fairly  narrow 
zone,  with  adjacent  subspecies.  This  does 
not  say  that  subspecies  are  "incipient  spe- 
cies." It  does  say  that  subspecies  are 
populations  which  have  made  initial  steps 
in  the  direction  of  species  formation,  such 
that  they  might  form  species  if  suitable 
isolating  conditions  should  develop,  or 
they  may  be  populations  which  have  not 
reached  the  species  level  and  are  dedif- 
ferentiating. Obviously  most  subspecies 
will  not  become  species,  and  likewise  the 
process  of  dedifferentiation  may  become 
relatively  stabilized  through  diverse  selec- 


30 


170 


SYSTEMATIC  ZOOLOGY 


live  pressures  on  either  side  of  the  inter- 
grade  zone. 

It  seems  to  me  then  that  the  Index  of 
Differentiation  or  some  similar  device  can 
give  us  an  often  needed  additional  cri- 
terion for  judging  relationship  between 
populations.  And  it  is  these  relative 
relationships  that  are  of  primary  interest; 
and  if  used  as  guide  lines  to  the  recogni- 
tion of  subspecies  will  permit  the  legiti- 
mate retention  of  this  category  in  the 
taxonomic  hierarchy.  Such  an  evolution- 
ary philosophy  applied  to  infraspecific 
analysis  has  a  number  of  important  ad- 
vantages, not  least  of  which  is  that  it 
focuses  attention  on  the  speciation  proc- 
ess and  not  on  geographic  variation  per 
se,  and  thus  emphasizes  that  the  steps 
which  can  lead  to  species  divergence  must 
be  initiated  long  before  the  process  is 
actually  completed.  Other  advantages  not 
already  alluded  to  include  a  consistency 
in  applying  the  concept  of  relationship  to 
all  taxa  and  hence  justifying  to  some  ex- 
tent the  nomenclatorial  equivalence  of 
species  and  subspecies,  provision  of  a 
more  uniform  goal  for  infraspecific  sys- 
tematists,  and  greater  usefulness  of  sub- 
species to  non-taxonomists  because  of  the 
greater  nomenclatorial  stability  and  more 
reliable  predictability  of  genetic  differ- 
ences in  unstudied  trails  that  would 
result. 

There  is  little  doubt  that  this  approach 
will  be  considered  impractical  in  some 
groups  of  organisms,  but  this  seems  of 
relatively  little  importance  to  the  present 
discussion.  Whereas  a  technique  must  be 
usable,  no  limits  should  be  placed  on  the 
conceptualization  of  direction  and  signifi- 
cance of  inquiry.  I  have  confidence  that 
systematists  are  not  so  unimaginative 
that  appropriate  procedures  will  not  rap- 
idly follow  perception  of  important  and 
necessary  goals,  as  they  have  already 
done  to  some  extent.  Present  day  taxon- 
omy is  fraught  with  practicality,  but  is 
nevertheless  shaken  by  criticism  as  to 
where  it  is  all  leading. 


Summary 

A   growing  dissatisfaction  with  much 
of  what  is  now  subspecies  taxonomy  and 
the  associated  indiscriminant  use  of  the 
trinomen  has  caused  many  taxonomists  to 
re-examine  the  basic  tenets  of  intraspe- 
cific  analysis.    This  "soul  searching"  has 
raised  the  important  questions  of  whether 
or  not  it  is  possible  or  even  desirable  to 
use  the  subspecies  category  as  a  rankable 
taxon  below  the  species  level  in  the  taxo- 
nomic hierarchy  and  at  what  level  of  dis- 
similarity,  if   any,   formal  trinomial   no- 
menclature  becomes    appropriate.    It   is 
argued  here  that  if  the  subspecies  is  to  be 
preserved  from  degradation  to  the  level  of 
the  rankless  morphs,  ecotypes,  and  forms, 
it  must  be  based  on  degrees  of  relation- 
ship or  evolutionary  divergence.    More- 
over, the  determinations  of  relative  ge- 
netic relationships  implies  an  emphasis 
on  similarities  between  the  various  sub- 
populations  comprising  a  species,  as  well 
as  careful  scrutiny  of  events  occurring  in 
the    boundary    regions    between    them. 
This  paper  is  therefore  concerned  with 
characterizing  some  of  these  postulated 
boundary  areas,  as  well  as  some  areas  of 
lesser  and  greater  amounts  of  differentia- 
tion, in  the  kangaroo  rat  Dipodomys  mer- 
riami. 

To  accomplish  this,  a  method  is  out- 
lined which  serves  to  sum  the  observed 
statistically  significant  differentiation  in 
many  diverse  characters  between  adja- 
cent populations.  In  doing  this,  the 
method  takes  into  account  the  variability 
and  magnitude  of  each  character.  The 
estimate  of  total  differentiation  thus  ob- 
tained can  then  be  divided  by  the  distance 
between  the  samples  being  compared  to 
give  the  Index  of  Differentiation  (D).  The 
reciprocal  of  this  statistic  can  also  be 
taken  as  a  measure  of  similarity.  The 
Index  of  Differentiation  can  be  further 
divided  by  the  number  of  characters 
studied  to  give  the  mean  character  dif- 
ferentiation per  mile  (MCD/mi.).  The 
system  involves  no  complicated  mathe- 
matical procedures,  and  yet  contains  only 


31 


SUBSPECIES  BOUNDARIES 


171 


minor  compromises  with  statistical  so- 
phistication. Furthermore  it  is  readily 
adapted  to  visual  portrayal  and  analysis. 

The  results  of  this  analysis  demonstrate 
a  very  close  agreement  between  levels  of 
differentiation  as  determined  by  the  In- 
dex of  Differentiation  and  the  taxonomic 
conclusions  previously  arrived  at,  when 
an  attempt  was  made  to  base  subspecies 
on  the  relative  relationships  among  infra- 
specific  populations.  Under  these  condi- 
tions subspecies  boundaries  are  uniformly 
characterized  by  a  high  level  of  differen- 
tiation which  occurs  over  a  relatively  nar- 
row zone,  and  is  usually  but  not  always 
associated  with  partial  or  complete  isola- 
tion between  populations.  Moreover  the 
analysis  has  emphasized  the  nearly  ubi- 
quitous occurrence  of  statistically  signifi- 
cant differences  between  populations,  and 
hence  of  the  futility  of  basing  formal  sub- 
species on  this  kind  of  evidence.  And 
finally  a  continuum  of  levels  of  differen- 
tiation was  found,  ranging  from  none  at 
all  to  the  species  level. 

It  is  concluded  from  this  evidence  that 
it  is  indeed  possible  to  gather  evidence 
on  the  relative  relationships  of  the  vari- 
ous portions  of  a  species,  and  it  is  sug- 
gested that  data  of  this  sort  should  form 
the  foundation  for  subspecific  diagnosis. 
This  approach  tends  to  focus  attention  on 
the  speciation  process  itself  instead  of  on 
geographic  variation  'per  se.  Various  other 
advantages  of  this  system  are  pointed  out, 
and  speculation  is  presented  concerning 
the  possible  determination  of  a  biologi- 
cally meaningful  division  between  sub- 
species and  lesser  categories. 

Acknoivledyments 

1  am  greatly  indebted  to  the  following 
individuals  who  have  critically  read  this 
manuscript,  but  who  do  not  necessarily 
share  the  views  which  I  have  expressed: 
S.  B.  Benson,  N.  K.  Johnson,  0.  P.  Pear- 
son, F.  J.  Sonleitner,  and  C.  S.  Thaeler. 
The  figures  were  prepared  by  G.  M. 
Christman  nf  the  Museum  of  Vertebrate 
Zoolog}'. 


REFERENCES 

Brown,  W.  L.,  Jr.,  and  E.  0.  Wilson.  1954. 
The  case  against  the  trinomen.  System. 
Zool.,  3:174-176. 

Cain,  A.  J.,  and  G.  A.  Harrison.  1958.  An  anal- 
ysis of  the  taxonomist's  judgment  of  affin- 
ity.   Proc.  Zool.  Soc.  London,  131:85-98. 
1960.    Phyletic  weighting.    Proc.  Zool.  Soc. 
London,   135:1-31. 

Cochran,  W.  G.  1959.  Sampling  techniques. 
John  Wiley,  New  York. 

Dixon,  W.  J.,  and  F.  J.  Massey,  Jr.  1957.  In- 
troduction to  statistical  analysis.  McGraw- 
Hill,  New  York. 

Edwards,  J.  G.  1954.  A  new  approach  to  infra- 
specific  categories.    System.  Zool.,  3:1-20. 

Fisher,  R.  A.  1936.  The  use  of  multiple  meas- 
urements in  taxonomic  problems.  Ann.  Eu- 
genics, 7:179-188. 

GosLiNE,  W.  A.  1954.  Further  thoughts  on 
subspecies  and  trinomials.  System.  Zool., 
3:92-94. 

Hald,  a.  1952.  Statistical  theory  with  engi- 
neering applications.  John  Wiley,  New 
York. 

Jolicoeur,  p.  1959.  Multivariate  geographical 
variation  in  the  wolf,  Canis  lupus  L.  Evolu- 
tion, 13:283-299. 

Kurten,  B.  1958.  A  differentiation  index,  and 
a  new  measure  of  evolutionary  rates.  Evo- 
lution, 12:146-157. 

Lerner,  L  M.  1954.  Genetic  homeostasis. 
Oliver  and  Boyd,  London. 

Lidicker,  W.  Z.,  Jr.  1960.  An  analysis  of  in- 
traspecific  variation  in  the  kangaroo  rat 
Dipodomys  merriami.  Univ.  California 
Pubis.  Zool.,  67:125-218. 

Lysenko,  O.,  and  P.  H.  A.  Sneath.  1959.  The 
use  of  models  in  bacterial  classification. 
Jour.  Gen.  Microbiol.,  20:284-290. 

Mearns,  E.  a.  1890.  Description  of  supposed 
new  species  and  subspecies  of  mammals, 
from  Arizona.  Bull.  Amer.  Mus.  Natur. 
Hist.,  2:277-307. 

Michener,  C.  D.,  and  R.  R.  Sokal.  1957.  A 
quantitative  approach  to  a  problem  in  classi- 
fication.   Evolution,  11:130-162. 

Pimentel,  R.  a.  1959.  Mendelian  infraspecific 
divergence  levels  and  their  analysis.    Sys- 
tem. Zool.,  8:139-159. 
Sneath,  P.  H.  A.    1961.   Recent  developments 
in  theoretical  and  quantitative  taxonomy. 
System.  Zool.,  10:118-139. 
Williams,   W.   T.,   and   G.    N.   Lance.    1958. 
Automatic  subdivision  of  associated  popu- 
lations.  Nature,  182:1755. 
Wilson,  E.  O.,  and  W.  L.  Brown,  Jr.    1953. 
The  subspecies  concept  and  its  taxonomic 
application.   System.  Zool.,  2:97-111. 

WILLIAM  Z.  LIDICKER,  JR.  is  Assistant 
Curator  of  Mammals  at  the  Museum  of  Verte- 
brate Zoology  and  Assistant  Professor  in  the 
Department  of  Zoology  at  the  University  of 
California,  Berkeley. 


32 


Vol  62,  pp.  11-12  March  17,  1949 

PROCEEDiNCS 

OF  THE 

BIOLOGICAL  SOCIETY  OF  WASHINGTON 

GENERIC  NAMES  OP  THE  FOUR-EYED  POUCH 
OPOSSUM  AND  THE  WOOLLY  OPOSSUM  (Didelphidae) 

By  Philip  Hershkovitz 


Published  opinions  on  the  status  of  Philander  Tiedemann 
(Zoologie,  vol.  1,  p.  426,  1808)  are  not  convincing  for  lack  of 
evidence  that  the  work  cited  had  been  carefully  studied  or 
even  consulted.  Tiedemann 's  system  of  classification  is  Lin- 
naean  with  names  for  all  hierarchies  recognized  (orders, 
families,  genera,  species)  properly  proposed  and,  for  his  time, 
adequately  diagnosed.  The  following  abstract  from  the  "Zoo- 
logie"  exposes  the  nature  of  the  name  Philander. 

p.  426]  Geschlecht  1. 

Opossum.   Philander  (Didelphys  L.) 

(Sarigue) 

[Generic  description  follows] 

p.  427]  [Description    continued] 

Es  gibt  gegen  10  bekannten  Arten: 

1)  Das  Virginische  Opossum.   P.  virginianus  (Did.  opossum  L.) 
(le  sarique  Buff.  T.  X.  p.  279.) 

Korper    rothlich    braun.     Ueber    jedem    Auge    ein    gelblieh 

weiser  Flecken.    Sehwanz  so  lang  als  der  Leib. 

1  Fuss  und  3  Zoll  lang  ohne  den  Sehwanz. 

In  Virginien,  Mexico,  Peru  u.  s.  w. 

Schreb.  tab.  146,  A.  B. 

Edw.  Tyson  Carigueya  seu  marsupiale  Americanum  or  tho 

anatomy  of  an  opossum.    Philos.  Transact.  V.  1698.  p.  105, 

V.  1704,  p.  1576. 

William  Cowper  an  account  of  the  anatomy  of  those  parti 

of  a  male  opossum  that  differ  from  the  female.    Ibid.  V. 

1704.  p.  1576. 

2)  Das  mausartige  Opossum  P.  murinus  (Did.  murina  L.)  (la 
marmose  Buff.  T.  X.  p.  335.) 

p.  428]  [Specific  description  follows] 

3)  Das  kurzgeschwanzte  Opossum.  P.  brachyurus  (Did. 
brachyuros  Penn.)  (le  touan  Cuvier  Tabl.  Element,  d'hiat. 
nat.  p.  125.) 

[Specific  description  follows] 

The  above  three  species  are  all  that  were  included  in  the  genua 
PMlander.  It  is  perfectly  clear  from  the  description  and  the  references 
to  Buffon,  Linnaeus  and  Schreber,  that  the  first  species  P.  virginianus 
is  merely  a  new  name  for  the  four-eyed  pouch  opossum,  Didelphis 
opossum  Linnaeus.  The  second  species  is  a  Marmosa,  the  third  a  Mono- 
delphis.    As  P.  virginianvs  is  virtually  tautonymic,  it  is  here  designated 

5— Proo.    Biol.   Soc.   Wash.,   Vou   62,    1949  (U) 


33 


12    Proceedings  of  the  Biological  Society  of  Washington 

genotype  of  Philander  Tiedemann,  Designation  of  the  woolly  opossum, 
Didelphis  philander  Linnaeus,  as  genotype  by  Thomas  (Catalogue  of  the 
Marsupialia  and  Monotremata  in  the  collection  of  the  British  Museum, 
p.  336,  1888)  is  untenable.  In  reality,  the  Philander  of  Thomas  and  sub- 
sequent authors  is  the  homonym  Philander  Burmeister  1856,  with  type 
Didelphis  philander  Linnaeus. 

Arguments  presented  by  Allen  (Bull.  Amer.  Mus.  Nat.  Hist.,  vol  .13, 
pp.  188-189,  1900)  against  usage  of  Philander  Tiedemann  stem  from  a 
misunderstanding  of  the  original  composition  of  the  genus  and  are  not 
relevant.  Nevertheless,  Allen's  substitution  of  his  own  Cahiromys  {D. 
philander  Linnaeus  type)  for  Philander  authors  (not  Tiedemann),  is 
accidentally  valid.  Tate's  (Ibid.,  vol.  76,  p.  164,  1939)  rejection  of 
Philander  Tiedemann  is  based  primarily  on  the  misidentification  of  P. 
virginianus  as  a  Didelphis,  and  secondarily  on  the  "homonymity"  with 
Philander  Brisson,  1762.  This  last  in  spite  of  the  fact  that  Tate  (op.  cit. 
p.  161)  listed  Philander  Brisson  as  an  unavailable  synonym  of  Meta- 
chirops  Matschie!  With  all  due  respect  for  Tate's  doubtful  endorsement, 
Brisson 's  system  of  classification  is  non-Linnaean  and  merits  no  con- 
sideration. Furthermore,  it  already  has  been  shown  by  Hopwood  (Proc. 
Zool.  Soc.  London,  vol.  117,  p.  533,  1947),  that  Brisson 's  generic  names 
are  pre-Linnaean  and  unavailable  in  any  case.  Hopwood  (op.  cit.  p. 
635)  erred,  however,  in  naming  " Didelphys  philander  Linnaeus"  the 
genotype  of  Philander  Tiedemann.  In  addition,  he  disinterred  Philander 
Gronovius,  1763,  with  the  same  genotype  designated.  Names  by  Grono- 
vius  are  no  better  than  those  of  Brisson  and  need  not  be  revived  at 
this  late  date  (c/.  Opinion  89,  International  Commission  on  Zoological 
Nomenclature). 

To  avoid  the  possibility  of  future  confusion,  disposition  must  be  made 
of  two  other  and  unused  generic  names  each  with  several  species  includ- 
ing those  under  discussion.  Genotype  of  Gamba  Liais  (Climats,  geol. 
faune  et  geogr.  bot.  Bresil,  p.  329,  1872)  is  hero  designated  Gamba 
palmata  Liais  (=  Chironectes  minimus  Zimmermann)  ;  genotype  of 
Cuica  Liais  (loc.  cit.)  is  here  designated  Cuica  murina  Liais  (=  Mar- 
mosa  murina  Linnaeus). 

Pertinent  data  presented  are  summarized  in  the  following  synonymies. 
Genus   Philander   Tiedemann    (Four-eyed    pouch    opossums). 

Philander  Tiedemann,  Zoologie,  vol.  1,  p.  426,  1808  (genotype, 
P[hilander]  virginianus  Tiedemann  =  Didelphis  opossum  Linnaeus). 

Metachirops  Matschie,  Sitz-ber.  Gessellseh.  naturforsch.  Fr.  Berlin, 
p.  268,  1916   (genotype,  Didelphis  opossum  Linnaeus). 

Eolothylax  Cabrera,  Genera  Mammalium,  (Monotremata,  Marsu- 
pialia), Mus.  Nac.  Cien.  Nat.,  Madrid,  p.  47,  1919  (genotype,  Didelphis 
opossum  Linnaeus). 

Genus  Caluromys  Allen   (Woolly  opossums). 

Philander  Burmeister,  Erliiuterungen  Fauna  Brasiliens,  p.  74,  Berlin 
1856  (genotype,  Philander  cayopollin  Burmeister  —  Didelphis  philander 
Linnaeus;  homonym  of  Philander  Tiedemann,  1808). 

Caluromys  Allen,  Bull.  Amer.  Mus.  Nat.  Hist.,  vol.  13,  p.  189,  1900 
(genotype,  Didelphis  philander  Linnaeus). 

Micoureus  Matschie,  Sitz-ber.  Gesellsch.  naturforsch.  Fr.  Berlin,  pp. 
259,  269  (genotype,  Didelphis  laniger  Desmarest  =  D.  lanata  Olfers; 
homonym  of  Micoureus  Lesson,  1842). 

Mallodelphys  Thomas,  Ann,  Mag.  Nat.  Hist.,  ser.  9,  vol.  5,  p.  195,  1920 
(substitutp  name  for  Micoureu.t  Matschie). 


34 


REVIEWS    OF    RECENT    LITERATURE. 

ZOOLOGY. 

Two  Important  Papers   on   North-American   Mammals.  —  The 

literature  relating  to  recent  work  on  North-American  mammals  is  so 
scattered,  and  the  results  have  been  the  outcome  of  investigations 
by  such  a  number  of  different  workers,  and  based  on  such  varying 
amounts  of  material,  that  it  is  a  great  gain  when  a  competent  author- 
ity on  any  given  group  can  go  over  it  and  coordinate  the  efforts  of 
his  predecessors  in  the  light  of,  practically,  all  of  their  material, 
combined  with  a  vast  amount  in  addition.  In  other  words,  the 
monographic  revision  of  any  of  the  larger  genera  of  North-American 
mammals  by  an  expert  is  a  distinct  advance,  for  which  all  mammalo- 
gists  may  well  feel  grateful.  It  is  with  pleasure,  therefore,  that  we 
call  attention  to  two  recent  contributions  of  this  character  —  Mr. 
Vernon  Bailey's  "  Revision  of  American  Voles  of  the  Genus  JNIicro- 
tus,"  and  Mr.  W.  H.  Osgood's  "  Revision  of  the  Pocket  Mice  of  the 
Genus  Perognathus." 

Mr.  Bailey's  revision  ^  of  the  American  voles,  or  meadow  mice,  is 
"  based  on  a  study  of  between  five  thousand  and  six  thousand  speci- 
mens from  more  than  eight  hundred  localities,  including  types  or 
topotypes  of  every  recognized  species  with  a  known  type  locality, 
and  also  types  or  topotypes  of  most  of  the  species  placed  in  syn- 
onymy." With  such  material  at  command,  and  with  a  wide  experi- 
ence with  the  animals  in  life,  and  personal  knowledge  of  the  actual 
conditions  of  environment  over  a  large  part  of  the  range  of  the  group, 
Mr.  Bailey  has  had  peculiar  advantages  for  his  work,  and  his  results 
are  subject  to  revision  only  at  points  where  material  is  still  deficient, 
or  from  some  other  point  of  view.  This  revision,  while  obviously 
not  final,  presents  a  new  starting  point  for  future  workers,  and  is 
likely  to  be  a  standard  for  many  long  years  to  come. 

The  little  animals   here   treated   are    the   short-tailed    field   mice, 

1  Revision  of  American  Voles  of  the  Genus  Microtus.  By  Vernon  Bailey, 
Chief  Field  Naturalist,  Division  of  Biological  Survey,  U.  S.  Department  of  Agri- 
culture. Prepared  under  the  direction  of  Dr.  C.  Hart  Merriam,  Chief  of  the 
Division.  North  Americafz  Fauna,  No.  17,  pp.  I-8S,  with  5  plates  and  17  text- 
figures.     Issued  June  6,  1900. 

221 


35 


2  22  THE   AMERICAN  NATURALIST.         [Vol.  XXXV. 

familiarly  typified  by  our  common  "  meadow  mice  "  of  the  Eastern 
States.  The  group  is  divisible  into  several  well-marked  subgenera, 
formerly  generally  known  under  the  generic  term  "  Arvicola,"  which 
has  had  to  give  way  to  the  less  known  but  older  term  "Microtus." 
The  group  is  especially  distinctive  of  the  northern  hemisphere  north 
of  the  tropics,  and  is  found  throughout  North  America  from  the 
mountains  of  Guatemala  and  southern  Mexico  northward,  increasing 
numerically,  both  in  species  and  individuals,  from  the  south  north- 
ward till  it  reaches  its  greatest  abundance  in  the  middle  and  colder 
temperate  zones,  again  declining  thence  northward  to  the  Arctic 
coast.  They  are  vegetable  feeders,  and  often  do  considerable  dam- 
age to  trees  and  crops  ;  they  are  active  in  the  winter,  forming  long 
burrows  or  tunnels  under  the  snow  ;  they  are  also  very  prolific,  breed- 
ing several  times  a  year,  young  being  found  throughout  the  warmer 
months. 

The  seventy  species  and  subspecies  recognized  by  Mr.  Bailey  are 
arranged  in  nine  subgenera  ;  between  the  extreme  forms  the  differ- 
ences are  strongly  marked,  but  the  intermediate  forms  present  grad- 
ual stages  of  intergradation.  The  subgenus  Neofiber,  of  Florida, 
embracing  the  round-tailed  muskrat,  and  the  subgenus  Lagurus,  of 
the  semi-arid  districts  of  the  northwestern  United  States,  present  the 
most  striking  contrast,  not  only  in  size  but  in  many  other  features. 
The  former  is  perhaps  the  largest  known  vole,  while  the  latter  group 
includes  the  smallest. 

Mr.  Bailey's  paper,  being  a  synopsis  rather  than  a  monograph, 
leaves  much  to  be  desired  in  point  of  detail,  but  is  admirable  in  its 
way,  and  covers  the  ground  with  as  much  fullness  as  his  prescribed 
limits  would  permit.  Of  the  twenty-six  synonyms  cited,  it  is  notice- 
able that  thirteen  relate  to  our  common  eastern  meadow  mouse,  and 
date  from  the  early  authors,  while  two  other  eastern  species  furnish 
three  others,  also  of  early  date.  Only  six  of  the  remaining  ten  are 
of  recent  date,  showing  that  of  some  fifty-five  forms  described  within 
the  last  ten  years,  by  nine  different  authors,  forty-eight  meet  with 
Mr.  Bailey's  approval.  Four  of  the  remaining  seven  are  identified 
with  earlier  names  which  for  many  years  have  been  considered 
indeterminable,  but  which  Mr.  Bailey  claims  to  have  established  on 
the  basis  of  topotypes. 

While  he  may  be  correct  in  these  determinations,  it  would  have 
been  of  interest  to  his  fellow-specialists  if  he  had  stated  the  basis  of 
his  determination  of  certain  type  localities,  notably  those  of  Richard- 
son's species,  described  as  from  the  "  Rocky  Mountains,"  or  similarly 


36 


No.  41 1 -J       REVIEWS   OF  RECENT  LITERATURE.  223 

vague  localities.  If  he  has  some  "  inside  history  "  to  fall  back  upon, 
it  is  only  fair  that  the  secret  should  be  made  public. 

It  may  be  said  further,  in  the  way  of  gentle  criticism,  that  it  is 
hardly  fair  wholly  to  ignore  such  knotty  points  as  the  allocation  of  a 
few  names  which  he  omits,  since  they  form  part  of  the  literature 
of  the  subject,  as,  for  example,  Hypudiziis  ochrogaster  Wagner,  Arvi- 
cola  noveboracensis  Richardson,  and  some  of  Rafinesque's  names. 
Mr.   Bailey  describes  as  new  two  species  and  one  subspecies. 

Mr.  Osgood's  "  Revision  of  the  Pocket  Mice  "  ^  is  an  equally  wel- 
come contribution,  and  has  been  prepared  upon  much  the  same  lines, 
with  equal  advantages  in  the  way  of  material  and  field  experience. 
The  pocket  mice  of  the  genus  Perognathus  are  confined  to  a  limited 
portion  of  North  America,  being  found  only  west  of  the  Mississippi, 
and  ranging  from  the  southern  border  of  British  Columbia  south  to 
the  valley  of  Mexico.  They  are  strictly  nocturnal  and  live  in  bur- 
rows, are  partial  to  arid  regions  and  seem  to  thrive  even  in  the  most 
barren  deserts.  Their  habits  are  hence  not  well  known,  as  they  are 
very  shy  and  even  difficult  to  trap.  They  are  mouse-like  in  form,  but 
only  distantly  related  to  the  true  rats  and  mice.  Their  most  obvious 
character  is  the  possession  of  cheek  pouches  which  open  externally. 

The  pocket  mice  vary  greatly  in  size,  form,  and  in  the  nature  of 
their  pelage,  which  may  be  either  soft  or  hispid  ;  but  between  the 
wide  extremes  there  are  so  many  closely  connecting  links  that  it  is 
difficult  to  find  any  sharp  lines  of  division,  although  two  subgenera 
are  fairly  recognizable.  The  whole  number  of  forms  here  recognized 
is  52  — 31  species  and  21  additional  subspecies,  about  equally  divided 
between  the  subgenera  Perognathus  and  Chaetodipus.  Of  these, 
thirteen  are  here  for  the  first  time  described.  Out  of  a  total  of  61 
specific  and  subspecific  names  applied  to  forms  of  this  group,  9 
are  relegated  to  synonymy.  Of  these  6r  names,  it  is  interesting  to 
note  that  52  date  from  1889  or  later,  and  that  of  these,  eight  prove 
to  be  synonyms,  three  of  them  having  become  so  through  the  identi- 
fication of  older  names  thought  ten  years  ago  to  be  indeterminable, 
but  since  reestablished  on  the  basis  of  topotypes. 

A  previous  revision  of  this  group  was  made  in  1889  by  Dr.  C. 
Hart  Merriam,  on  the  basis  of  less  than  two  hundred  specimens  — 

1  Revision  of  the  Pocket  Mice  of  the  Genus  Perognathus.  By  Wilfred  H. 
Osgood,  Assistant  Biologist,  Biological  Survey,  U.  S.  Department  of  Agriculture. 
Prepared  under  the  direction  of  Dr.  C.  Hart  Merriam,  Chief  of  Division  of  Bio- 
logical Survey.  North  American  Fauna,  No.  18,  pp.  1-72,  Pis.  I-IV,  and  15  text- 
cuts.     Issued  Sept.  20,  1900. 


37 


2  24  ^-^^   ^  M ERICA  N  NA  TURA  LIS T.         [  V ol.  X X  X  \' . 

all  of  the  material  then  available  —  when  the  number  of  currently 
recognized  forms  was  raised  from  six  to  twenty-one.  Dr.  Merriam's 
work,  however,  cleared  the  way  for  a  better  conception  of  the  group, 
rectifying  important  errors  of  nomenclature  and  making  known  many 
new  forms.  Mr.  Osgood,  with  fifteen  times  this  amount  of  material, 
seems  to  have  settled  all  of  the  remaining  doubts  regarding  the  appli- 
cation of  certain  early  names,  and,  besides  coordinating  the  work 
of  his  predecessors,  has  immensely  extended  our  knowledge  of  the 
group.  The  paper  is  admirable  from  every  point  of  view  and  does 
great  credit  to  its  author.  t_  p^   ^ 


38 


No.  2.  NORTH  AMERICAN  FAUNA.  October,  1889. 


DESCRIPTIONS  OF  TWO  NEW  SPECIES  AND  ONE  NEW  SUBSPECIES  OF 

GRASSHOPPER  MOUSE, 

WITH  A  DIAGNOSIS    OF    THE   GENUS   ONYCHOMYS,  AND   A    SYNOPSIS   OF   THE   SPECIES 

AND   SUBSPECIES. 


By  C.  Haet  Merriam,  M.  D. 


A.  DESCRIPTIONS  OF  NEW  SPECIES  AND  SUBSPECIES. 

ONYCHOMYS  LONGIPES  sp.  uov. 

(Texas  Grasshopper  Mouse.) 

Type  f|5|   9   ad.    Merriam  Collection.     Concho  County,  Texas,  March  11,  1887. 
Collected  by  William  Lloyd. 

Measurements  (taken  in  the  flesh  by  collector).— Total  length,  190°"°; 
tail,  48  [this  measurement  seems  to  be  too  short]  ;  hind  foot,  25;  ear 
from  crown,  13  (measured  from  dry  skin). 

General  characters. — Size  larger  than  that  of  the  other  known  repre- 
sentatives of  the  genus,  with  larger  and  broader  ears,  and  much  longer 
hind  feet.  Ears  less  hairy  than  in  0.  leucogaster,  with  the  lanuginous 
tuft  at  base  less  apparent ;  tail  longer  and  more  slender. 

Color. — Above,  mouse  graj-,  sparingly  mixed  with  black-tipped  hairs, 
and  with  a  narrow  fulvous  stripe  along  each  side  between  the  gray  of 
the  back  and  white  of  the  belly,  extending  from  the  fore-legs  to  the  root 
of  the  tail;  under  parts  white. 

Cranial  characters. — Skull  longer  and  narrower  than  that  of  0.  leuco- 
gaster (particularly  the  rostral  portion),  with  much  longer  nasals,  aud  a 
distinct  supraorbital  "  bead"  running  the  full  length  of  the  frontals  and 
there  terminating  abruptly.  The  nasals  overreach  the  nasal  branch  of 
the  premaxillaries  about  as  far  as  in  leucogaster.  The  iucisive  foram. 
ina,  as  in  0.  leucogaster,  barely  reach  the  anterior  cusp  of  the  first 
molar.  The  roof  of  the  palate  extends  further  behind  the  last  molar 
than  in  leucogaster,  and  gives  off  a  median  blunt  spine  projecting  into 
the  pterygoid  fossa.  The  palatal  bones  end  anteriorly  exactly  on  a  line 
2541— No.  2 1  1 


39 


2  NORTH    AMERICAN    FAUNA.  [No.  2. 

with  the  interspace  between  the  first  and  second  molars.  The  presphe- 
noid  is  excavated  laterally  to  such  a  degree  that  the  middle  portion  is 
reduced  to  a  narrow  bar  less  than  one-third  the  width  of  its  base.  The 
condylar  ramus  is  lower  and  more  nearly  horizontal  than  in  leucogaster, 
and  the  angular  notch  is  deeper.  The  coronoid  process  resembles  that 
of  leucogaster. 

ONYCHOMYS  L0:NGICAUDUS  sp.  nov. 

(Long-tailed  Gkasshoppeu  Mouse.) 

Type^sISi  ^  a<l-     St.  George,  Utah,  January  4,  1889.  Collected  by  Vernon  Bailey. 

Measurements  (taken  in  the  flesh  by  the  collector). — Total  length,  145  j 
tail,  5/) ;  hind  foot,  20 ;  ear  from  crown,  10  (measured  from  dry  skin). 

General  characters. — Similar  to  0.  leucogaster,  but  smaller,  with  longer 
and  slenderer  tail.  Pelage  longer,  but  not  so  dense.  General  color 
above,  cinnamon-fawn,  well  mixed  with  black-tipped  hairs. 

Cranial  characters. — Skull  smaller  and  narrower  than  that  of  0.  leuco- 
gaster; zygomatic  arches  less  spreading ;  nasais  less  projecting  behind 
nasal  branch  of  premaxillaries.  The  coronoid  and  condylar  processes 
of  the  mandible  are  shorter,  and  the  coronoid  notch  is  not  so  deep  as 
in  leucogaster.  The  presphenoid  shows  little  or  no  lateral  excavation. 
The  incisive  foramina  do  not  quite  reach  the  plane  of  the  anterior  cusp 
of  the  first  molar.  The  shelf  of  the  palate  projects  posteriorly  consid- 
erably beyond  the  molars,  and  terminates  in  a  nearly  straight  line  with- 
out trace  of  a  median  spine. 

ONYCHOMYS  LEUCOGASTER  MELANOPHRYS  subsp.  nov. 

(Black-eyed  Grasshopper  Mouse.) 

Type,  lilf  (?  ad.    Kanab,  Utah,  December  22, 1888.     Collected  by  Vernon  Bailey. 

3Ieasure7nents  {tnken  in  the  flesh  by  collector). — Total  length,  154; 
tail,  41 ;  hind  foot,  21.     Ear  from  crown  10  (measured  from  the  dry  skin). 

Size  of  0.  leucogaster.  Ear  a  little  smaller.  Hind  foot  densely  furred 
to  base  of  toes.  Color  above,  rich  tawny  cinnamon,  well  mixed  with 
black-tipped  hairs  on  the  back,  and  brightest  on  the  sides;  a  distinct 
black  ring  round  the  eye,  broadest  above.  This  ring  is  considerably 
broader  and  more  conspicuous  than  the  very  narrow  ring  of  leucogaster. 

Cranial  characters. — Skull  large  and  broad ;  very  similar  to  0.  leuco- 
gaster in  size  and  proportions,  but  with  zygomatic  arches  less  spread- 
ing posteriorly,  interparietal  narrower,  nasals  not  reaching  quite  so  far 
beyond  the  nasal  branch  of  premaxillaries,  and  antorbital  slit  narrower. 
Presphenoid  moderately  excavated,  as  in  leucogaster.  The  incisive  fo- 
ramina reach  past  the  plane  of  the  first  cusp  of  the  anterior  molar.  The 
condylar  ramus  is  longer  and  directed  more  obliquely  upward  than  in 
leucogaster,  with  the  coronoid  and  infra-condylar  notches  deeper. 

Note. — In  order  to  render  the  preceding  diagnoses  of  new  forms 
more  useful,  the  following  brief  descriptions  of  the  skulls  of  the  two 


40 


Oct.,  1889.1  REVISION    OF    THE    GENUS    ONYCHOMYS.  3 

rdvioas  ly  knowu  species  are  appended  for  coinparisou,  together  with 
figures  of  the  skull  of  the  type  of  the  genus  {0.  leucogaster): 

Onychomys  leucogaster  Max. — Skull  large  and  broad,  with  zygomatic  arches  spread- 
inf  posteriorly.     Antorbital  slit  larger  than  in   the  other  known   species.     Palate 
hort,  ending  posteriorly  in  a  short  median  spine  (see  figure). 

Onychomys  torridus  Coues. — SkuU  small ,  narrow,  with  zygomatic  arches  not  spread- 
ing, and  vault  of  cranium  more  rounded  than  in  any  other  member  of  the  genus.  In- 
terparietal relatively  large.  Nasals  projecting  far  beyond  nasal  branch  of  premaxil- 
lary.  Incisive  foramina  very  long,  extending  back  to  second  cusp  of  first  molar. 
Shelf  of  palate  produced  posteriorly  nearly  as  far  as  in  longicaudus,  and  truncated. 
Presphenoid  slightly  excavated  laterally.  Mandible  much  as  in  longicaudus,  but 
with  coroaoid    process  more  depressed  and  condylar  ramus  more  slender. 

B.  DIAGNOSIS  OF  THE  GENUS  ONYCHOMYS. 

The  striking  external  differences  which  distinguish  the  Missouri 
Grasshopper  Mouse  from  the  other  White-footed  Mice  of  America 
(Hesperomys  auct.)  led  its  discoverer,  Maximilian,  to  place  it  in  the 
genus  Hypiidceus  [=Evotomys^  Coues),  and  led  Baird  to  erect  for  its  re- 
ception a  separate  section  or  subgenus,  which  he  named  Onychomys. 
Coues,  the  only  recent  monographer  of  the  American  Mice,  treats  Ony- 
chomys as  a  subgenus,  and  gives  a  lengthy  description  of  its  characters. 
Since,  however,  some  of  the  statements  contained  in  this  description 
are  erroneous,  and  the  conclusions  absurd,*  and  since  the  most  impor- 
tant taxonomic  characters  are  overlooked,  it  becomes  necessary  to  re- 
define the  type.  A  somewhat  critical  study  of  the  cranial  and  dental 
characters  of  Onychomys  in  comparison  with  the  other  North  American 
White-footed  Mice  has  compelled  me  to  raise  it  to  full  generic  rank. 
It  may  be  known  by  the  following  diagnosis  : 

Genus  ONYCHOMYS  Baird,  1857. 

Baird,  Mammals  of  North  America,  1857,  p.  457  (subgenus). 

Type,  HypudoBus  leucogaster,  Max.  Wied,  Reise  in  das  innere  Nord  Amerika,  ii, 

1841,  99-101  (from  Fort  Clark,  Dakota). 
Hesperomys  auct. 

First  and  second  upper  molars  large  and  broad ;  third  less  than  half 
the  size  of  the  second.  First  upper  molar  with  two  internal  and  three 
external  cusps,  the  anterior  cusp  a  trefoil  when  young,  narrow,  and  on  a 
line  with  the  outside  of  the  tooth,  leaving  a  distinct  step  on  the  inside. 
Second  upper  molar  with  two  internal  and  two  external  cusps,  and  a 
narrow  antero  external  fold.  Last  upper  molar  subcircular  in  outline, 
smaller  than  in  Hesperomys^  and  less  indented  by  the  lateral  notches. 

*  Coues  says :  "  Although  unmistakably  a  true  Murine,  as  shown  by  the  cranial  and 
other  fundamental  characters,  it  nevertheless  deviates  much  from  Mus  and  Hesper- 
omys, and  approaches  the  Arvicolines.  Its  affinities  with  Evotomys  are  really  close." 
(Monographs  of  North  American  Rodentia,  1877,  p.  106.)  As  a  matter  of  fact,  Ony- 
chomys has  no  alhnities  whatever  with  Evotomys,  or  any  other  member  of  the  Arvico- 
line  series,  its  departure  from  Hesperomys  being  in  a  widely  different  direction. 


41 


4  NORTH    AMERICAN    FAUNA.  [No.  2. 

Lower  molar  series  much  broader  than  iu  Hesperomys,  First  lower 
molar  with  an  anterior,  two  internal,  and  two  external  cusps,  and  a 
postero-internal  loop.  In  Hesperomys  the  anterior  cusp  is  divided,  so 
that  there  are  three  distinct  cusps  on  each  side.  Second  lower  molar 
with  two  internal  and  two  external  cusps,  an  antero-external  and  a  pos- 
terointernal  fold.  Third  lower  molar  scarcely  longer  than  broad,  sub- 
circular  in  outline,  with  the  large  posterior  lobe  of  Hesperomys  reduced 
to  a  slight  fold  of  enamel,  which  disappears  with  wear. 

Coronoid  process  of  mandible  well  developed,  rising  high  above  the 
condylar  ramus  and  directed  backward  in  the  form  of  a  large  hook 
(see  accompanying  cut).  Nasals  wedge-shaped,  terminating  posteri- 
orly considerably  behind  the  end  of  the  nasal  branch  of  the  premaxil- 
laries. 


Fig.  1.  Fig.  2. 

1.  Lower  jaw  of  Onj/cAomy*  Zewco^asJer.  2.  Lower  jaw  of  fl'esperojni/a  Zewcopw8. 

Body  much  stouter  and  heavier  than  in  Hesperomys.  Tail  short, 
thick,  and  tapering  to  an  obtuse  point. 

Fore  feet  larger  than  in  Hesperomys ;  five  tuberculate,  as  usual  in  the 
Murine  series.  Hind  feet  four-tuberculate,  and  densely  furred  from 
heel  to  tubercles.  Tubercles  phalangeal,  corresponding  to  the  four  an- 
terior tubercles  of  Hesperomys^  that  is  to  say,  the  first  is  situated  at 
the  base  of  the  first  digit,  the  second  at  the  base  of  the  second  digit? 
the  third  over  the  bases  of  the  third  and  fourth  digits  together,  the 
fourth  at  the  base  of  the  fifth  digit.  The  fifth  and  sixth  (or  metatarsal) 
tubercles  of  Hesperomys  are  altogether  wanting. 

C.  SYNOPSIS  OP  SPECIES  AND  SUBSPECIES. 

(1)  By  External  Characters. 

Length,  about  ISC'"™  ;  tail,  about  40 ;  hind  foot,  about  21 ;  ear  from  crown,  10.  Color 
above,  mouse-gray ;  black  ring  around  eye  inconspicuous 0.  leucogaster. 

Size  of  0.  leucogaster.  Color  above,  rich  tawny  cinnamon,  brightest  on  the  sides; 
black  ring  round  eye  conspicuous 0.  leucogaster  melanophrya. 

Length,  about  145™™  ;  tail,  about  55;  hind  foot,  20;  ear  from  crown,  10.  Color  above, 
cinnamon  fawn 0.  longicaudus. 

Length,  about  190™"';  tail,  about  50;  hind  foot,  25;  ear  from  crown,  13.  Color 
above,  mouse-gray,  with  a  narrow  fulvous  stripe  along  the  sides 0.  longipes. 

Length,  about  135™™;  tail,  about  45;  hind  foot,  20;  ear  from  crown,  10.  Color 
above,  uniform  dull  tawny  cinnamon;  no  black  ring  around  the  eye.  Tail  thick 
with  a  dark  stripe  above  reaching  three-fourths  its  length  ;  rest  of  tail  white. 

0.  torridiiJi. 


42 


Oct.,  1889.] 


Palate  ending 
posteriorly 


REVISION    OF    THE    GENUS    ONYCHOMYS.  5 

(2)  By  Cranial  Characteks. 

th  a  blunt  me- S  ^  'i'stinct  supraorbital  bead longipea. 

no  distinct  supraorbital  bead leucogaster. 


th  a  blunt  nie-S 
dian  spine        y 


<>  (  skull  large  and  broad melanophrys. 

with  straiirht  or  ..      .  .       ~  •      i        i  i     i 

Ifrl  tl  '      n       }  I  J  nosive  foramina  barely  reach  plane 

8  ig      y  CO  -     "^  skull  smaller  I       of  first  molar longicaudus. 

and  nar-     <; 
L       rower        I  incisive  foramina  reach  second  cusp 
I      of  til 


vex  edge 

L       rower        |  inci 

'  tirst  molar torridus. 

Cranial  measurements  of  the  known  forma  of  the  genua  Onychomys 


Basilar  length  of  Hensel  (from  foramen  magnum  to  incisor) 

Zygomatic  breadth  

Greatest  parietal  breadth 

Interorbital  constriction 

Length  of  nasals 

Incisor  to  post-palatal  notch 

Foramen  magnum  to  incisive  foramina  

Foramen  magnum  to  palate  

Length  of  upper  molar  series  (on  alveolte) 

Length  of  incisive  foramina 

Length  of  mandible  

Height  of  coronoid  process  from  angle  

Katios  to  basilar  length: 

Zygomatio  breadth 

Parietal  breadth 

Nasals 

Molar  series  (on  alveolae) 

Incisive  foramina 

Foramen  magnum  to  incisive  foramen    

Foramen  magnum  to  palate 


O.  leucogaster,  ;    vfplanonhrvo 
Fort  Buford,       -S^^rte"' 


Dakota. 


Kanab,  Utah. 


4418$ 

4419d" 

5393  cT 

5894  cT 

22 

22 

22.3 

21.6 

15 

15.2 

15.4 

1.^5 

12.9 

12.7 

12.8 

12.5 

4.5 

4.5 

5.2 

4.8 

10.8 

11.6 

10.7 

10.7 

12 

12 

11.7 

11.5 

14.7 

14.6 

15 

14.5 

9.7 

10 

10.2 

9.9 

4.5 

4.2 

4.6 

4.8 

5 

5.7 

5 

5 

15.5 

15.8 

15.7 

15.3 

6.5 

7.3 

6.8 

6.8 

68,1 

69 

69 

71.7 

58.9 

57.7 

57.3 

57 

49 

52.7 

47.9 

49.5 

20.4 

ISJ 

20.6 

22 

22.7 

25.9 

22.4 

23.1 

66 

66.3 

67.3 

67 

44 

45.4 

45.7 

45.8 

Longipes, 
Concho 
County, 
Texas, 


23.3 
15.5 
12.2 

4.4 
12.5 
12.4 
15.7 
10.6 

4.4 

5.3 
16 

7.2 

66.6 

52 

52.3 

20 

22.7 

67.3 

45.4 


Basilar  length  of  Hensel  (from  foramen  magnnm  to  incisor) 

Zygomatic  breadth    

Greatest  parietal  breadth 

Interorbital  constriction 

Length  of  nasals 

Incisor  to  post-palatal  notch 

Foramen  magnum  to  incisive  foramina 

Foramen  magnum  to  palate 

Length  of  upper  molar  series  (on  alveolae) 

Length  of  incisive  foramina 

Length  of  mandible 

Height  of  coronoid  process  from  angle  

Batios  to  basilar  length : 

Zygomatic  breadth 

Parietal  breadth 

Nasals 

Molar  series  (on  alveolae) 

Incisive  foramina      

Foramen  magnum  to  incisive  foramen ., 

Foramen  magnum  to  palate. 


Longicaudus. 
St.  George,  Utah. 


Torridus, 

Grant 

County, 

N.  Mex. 


5895? 


19.3 

13 

11.2 
4.7 

10 

10.5 

13.5 
8.8 
3.8 
4.3 

13.4 
6.2 

67.3 

58 

51.8 

19.6 

22.2 

68.3 

45.5 


5896,/      5897  cf 


2839  cT 


19.3 

19.4 

13 

18.1 

11.5 

11.2 

4.7 

4.8 

9.5 

9.7 

10.5 

10.4 

13.4 

13.3 

8.7 

8.7 

3.8 

3.8 

4,3 

4  4 

13.5 

13.2 

6.3 

6.2 

67.3 

68 

59.5 

57.7 

49.2 

50 

19.6 

19.5 

22.2 

22.6 

69.4 

68.5 

45 

44.8 

18.5 
12.5 
11.4 
4.2 
9.6 
10 

12.5 
8.5 
3.5 
5 

13.2 
5.8 

67.5 

61.6 

51.8 

18.9 

27 

67.5 

45.8 


43 


PLATE  I. 

Figs.  1, 2, 3, 4,  and  5,  Onychomys  leucogaater,  $  young.     (Skull  No.  4422. )    Fort  Baford, 
Dakota. 

1.  Skull  from  above,  and  left  under  jaw  from  outside  (X  2). 

2.  Crowns  of  left  upper  molars  from  below  (x  10). 

3.  Crowns  of  left  lower  molars  from  above  ( X  10). 

4.  Crowns  of  right  upper  molfirs  from  the  side  (  X  10). 

5.  Crowns  of  right  lower  molars  from  the  side  (X  10). 

Figs.  6  and  7,  Onychomys  leucogaster,  $  ad.     (No.  5012).    Valentine,  Nebraska. 

6.  Crowns  of  left  upper  molars  from  below  (  X  10). 

7.  Crowns  of  left  lower  molars  from  above  (X  10). 

Figs.  8  and  9,  Onychomys  longicaudus,  $  ad.     (No.  5896).     St.  George,  Utah. 

8.  Crowns  of  left  upper  molars  from  below  (X  10). 

9.  Crowns  of  left  lower  molars  from  above  ( X  10). 

38 


44 


North  American  Fauna,  No.  2. 


Plate  I. 


1-5.  Onychomys  leucogaster,  d  j'oung. 
6,7.  Onychomys  leucogaster,  $  adult. 
8, 9.  Onychomys  longicaudus,  d  axlult. 


45 


Vol.  79,  pp.  83-88  23  May  1966 

PROCEEDINGS 
OF  THE 

BIOLOGICAL  SOCIETY  OF  WASHINGTON 


DESCRIPTIONS  OF  NEW  BATS    {CHOERONISCUS 
AND  RHINOPHYLLA)   FROM  COLOMBIA 

By  Charles  O.  Handley,  Jr. 
U.  S.  National  Museum,  Washington,  D.  C. 

An  imperfectly  known  endemic  mammalian  fauna  is  found 
on  the  Pacific  coast  and  Andean  foothills  of  northwestern 
Ecuador  and  Colombia  and  northward  into  Panama,  where  it 
crosses  to  the  Caribbean  slope  and  continues  into  Costa  Rica 
and  Nicaragua  and  in  some  instances  even  into  Mexico.  The 
relatives  of  its  endemic  species  are  mostly  South  American, 
but  some  are  Mexican.  Species  characteristic  of  this  fauna, 
snch  as  Carollia  castanea,  Vampyressa  nymphaea,  Heteromys 
australis,  Oryzomys  bombycinus,  and  Hoplomys  gymnurus, 
were  among  the  mammals  collected  in  the  course  of  virological 
studies  of  the  Rockefeller  Foundation  on  the  Pacific  coast  of 
Colombia  in  1962  and  1963.  In  addition  there  were  striking 
new  species  of  Choeroniscus  and  Rhinophylla. 

1  am  grateful  to  Wilmot  A.  Thornton,  Center  for  Zoonoses  Research, 
University  of  Illinois,  Urbana  (formerly  at  Universidad  del  Valle,  Cali, 
Colombia)  for  the  opportunity  to  study  the  Colombian  material  here 
reported.  Richard  G.  Van  Gelder,  American  Museum  of  Natural  History 
(AMNH);  Philip  Hershkovitz  and  J.  C.  Moore,  Chicago  Natural  History 
Museum  ( CNHM ) ;  Bernardo  Villa-R,  Instituto  de  Biologia,  Mexico  ( IB ) ; 
Barbara  Lawrence,  Museum  of  Comparative  Zoology,  Harvard  University 
(MCZ);  J.  Knox  Jones,  Jr.,  Museum  of  Natural  History,  University  of 
Kansas  (KU);  William  H.  Burt,  Museum  of  Zoology,  University  of 
Michigan  (UMMZ);  A.  Musso,  Sociedad  de  Ciencias  Naturales  La  Salle 
(LS);  and  Juhani  Ojasti,  Universidad  Central  de  Venezuela  (UCV) 
kindly  permitted  me  to  study  comparative  material.  Specimens  in  the 
U.  S.  National  Museum  are  designated  by  the  abbreviation  (USNM). 
Studies  which  led  to  the  following  descriptions  were  supported  in  part 
by  National  Science  Foundation  Grant  G-19415. 

All  measurements  are  in  millimeters.  For  definition  of  cranial  mea- 
surements see  Handley  (1959:  98-99).  Capitalized  color  terms  are 
From  Ridgway  (1912). 

11— Proc.  Biol.  Soc.  Wash.,  Vol.  79,  1966  (83) 


46 


84     Proceedings  of  the  Biological  Society  of  Washington 

Choeroniscus 

There  are  few  specimens  of  the  poorly  known  glossophagine  genus 
Choeroniscus  in  collections.  The  limits  of  variation  in  the  genus  are 
incompletely  known  (Sanborn,  1954),  and  until  now  its  separation  from 
Choeronycteris  has  been  questionable.  A  specimen  of  a  new  species  of 
Choeroniscus  from  the  west  coast  of  Colombia  greatly  extends  knowledge 
of  the  genus  and  strengthens  its  stature  as  a  genus  distinct  from  Choero- 
nycteris. 

Choeroniscus  periosus,  new  species 

Holotype:  USNM  no.  344918,  adult  female,  alcoholic  and  skull, 
collected  1  February  1963,  by  Wilmot  A.  Thornton,  at  the  Rio  Raposo, 
near  sea  level,  27  km  south  of  Buenaventura,  Departamento  de  Valle, 
Colombia,  original  niunber  592. 

Etymology:     Greek  periosus,  immense. 

Distribution:     Known  only  from  the  type-locality. 

Description:  Body  size  large  (forearm  41.2;  greatest  length  of  skull 
30.3).  Dorsal  mass  effect  coloration  (after  three  month's  submersion  in 
formalin)  rich  blackish-brown;  basal  three-fourths  orange-brown  in  dorsal 
hairs;  underparts  but  slightly  paler  than  dorsum.  Vibrissae  abundant 
and  conspicuous  on  snout  and  chin.  Ears,  chin,  noseleaf,  hps,  membranes, 
legs,  feet,  and  fingers  blackish.  Lancet  of  noseleaf  relatively  narrow,  with 
three  notches  on  each  side  near  tip,  and  with  prominent  vertical  median 
ridge  on  anterior  face.  Membranous  "tongue-channel"  on  chin  im- 
usually  well  developed,  protruding  1.5  mm  forward  and  2.0  mm  up 
from  lower  lip;  dorsal  and  anterior  edges  scalloped.  Ear  short,  tip 
rounded,  antitragus  well  defined;  tragus  spatulate,  3.8  mm  long,  with 
margins  entire  ( except  for  prominent  posterior  notch  opposite  anterior 
base),  and  with  anterior  edge  and  posterior  basal  lobe  thickened.  Inter- 
femoral  membrane  broad,  naked.  Hind  legs  naked.  Calcar  shorter  than 
foot,  not  lobed. 

Rostrum  longer  than  braincase;  cranium  little  elevated  from  basi- 
cranial  plane;  profiles  of  rostrum  and  cranium  evenly  tapered,  without 
sharp  angle  in  between;  no  orbital  ridges  or  processes;  zygoma  absent; 
lambdoidal  crest  low;  sagittal  crest  absent;  maxillary  toothrows  sub- 
parallel;  palate  relatively  broad  anteriorly  and  narrow  posteriorly; 
posterolateral  margin  of  palate  not  notched;  postpalatal  extension 
parallel-sided,  tubular,  reaching  posterior  to  level  of  mandibular  fossae; 
mesopterygoid  fossa  reduced  to  a  straight-sided,  V-shaped  notch;  hamular 
processes  greatly  inflated  and  approaching,  but  not  quite  touching, 
auditory  bullae;  basial  pits  prominent,  separated  by  broad  median  ridge. 

2    12    3 
Dentition    weak.     Dental    formula  -,-,—,  —  —  30.     Upper  incisors 

small,  vmicuspid;  inner  upper  incisors  (P)  separated  by  a  space  three  to 
four  times  the  width  of  the  teeth;  larger,  outer  upper  incisor  (P)  sep- 
arated by  somewhat  less  than  its  own  width  from  P  and  from  canine. 


47 


New  Bats  from  Colombia  85 

Upper  canine  with  small  posterobasal  cusp.  Upper  premolars  very  nar- 
row; median  cusp,  particularly  of  anterior  premolar,  very  little  higher 
than  weU-defined  anterior  and  posterior  cusps.  Upper  molars  with  cusps 
greatly  reduced;  M^  and  M-  similar  in  size  and  shape,  M^  slightly 
shorter  and  broader.  Upper  premolars  widely  spaced;  molars  closer 
together,  but  not  touching.  Lower  premolars  narrow,  with  well-defined, 
subequal  anterior,  posterior,  and  median  cusps.  Metaconid  cusps  of 
lower  molars  enlarged  and  protoconid  cusps  reduced;  paraconid  cusps  in 
line  with  protoconids,  not  inflected.  Anterior  lo\\"er  premolar  close 
behind,  but  not  touching,  canine;  spaces  between  premolars  great,  but 
spaces  between  P^  and  Mi  and  between  other  molars,  much  less. 

Measurements  (All  external  dimensions  taken  from  specimen  in  alco- 
hol): Total  length  62,  tail  vertebrae  10,  hind  foot  12,  ear  from  notch 
15,  forearm  41.2,  tibia  13.3,  calcar  7.9. 

Greatest  length  of  skull  30.3.  zygomatic  breadth  11.0,  postorbital 
breadth  4.7,  braincase  breadth  9.9,  braincase  depth  7.4,  maxillary  tooth 
row  length  10.8,  postpalatal  length  7.0,  palatal  breadth  at  \P  5.2,  pal- 
atal breadth  at  canines  4.6. 

Comparisons:  C.  periosus  can  be  distinguished  from  all  other  species 
of  Choeroniscus  by  its  longer  (longer  than  braincase),  more  robust 
rostrum;  more  inflated  hamular  process;  and  larger  size  {e.g.,  forearm 
41.2  vs.  32.4-36.9;  greatest  length  of  skull  30.3  vs.  19.3-24.4;  maxillary 
tooth  row  10.8  vs.  6.5-9.2).  It  is  allied  with  the  Amazonian  species  C. 
minor,  C.  intermedius,  and  C.  inca,  and  distinguished  from  the  Central 
American  and  northern  South  American  C.  godmani,  in  having  the 
posterolateral  margin  of  the  palate  unnotched  and  the  craniiun  not  so 
markedly  elevated  from  the  basicranial  plane. 

Remarks:  With  the  addition  of  C.  periosus,  the  genus  Choeroniscus 
includes  five  nominal  species.  C.  periosus  is  much  the  largest  species; 
C.  inca  Thomas,  C.  intermedius  Allen  and  Chapman,  and  C.  minor 
Peters  are  intermediate  in  size;  and  C.  godmani  Thomas  is  smallest. 

Choeroniscus  is  the  most  specialized  of  a  group  of  nominal  glossopha- 
gine  genera  which  may  be  characterized  briefly  as  follows: 

Teeth  nearly  normal  pterygoids  normal  Lichonycteris 

Teeth  shghtly  reduced         pterygoids?  Scleronycteris 

Teeth  reduced;  PM  high     pterygoids  shghtly  Hylonycteris 

specialized 

Teeth  reduced;  PM  high     pterygoids  specialized  Choeronycteris 

Teeth  greatly  reduced;       pterygoids  greatly  speciahzed  Choeroniscus 

PM  low 

Lichonycteris  has  26  teeth  and  the  other  genera  have  30. 

As  here  understood,  the  genus  Choeronycteris  includes  Musonycteris 
harrisoni  Schaldach  and  McLaughlin,  which  is  distinguished  from 
Choeronycteris  mexicana  Tschudi  principally  by  its  strikingly  elongated 
rostrum  and  associated  modifications  in  proportions.    The  disparity  in 


48 


86     Proceedings  of  tJie  Biological  Society  of  Washington 

rostral  proportions  is  much  greater,  however,  between  Choeroniscus 
godmani  and  Choeroniscus  periosus  than  between  Choeronycteris  mexi- 
cana  and  Choeronycteris  harrisoni.  Thus,  to  distinguish  C.  harrisoni  as 
representative  of  a  separate  genus  tends  to  obscure  relationships  in  this 
segment  of  the  Glossophaginae.  Muson-ycteris  should  be  regarded  as  a 
synonym  of  Choeronycteris. 

Specimens  examined:  Choeroniscus  godmani.  COLOMBIA:  Meta: 
Restrepo,  1  (MCZ).  COSTA  RICA:  Vicinity  of  San  Jose,  3000  ft,  5 
(AMNH).  HONDURAS:  Cantoral,  1  (AMNH);  La  Flor  Archaga,  2 
(AMNH).  MEXICO:  Chiapas:  Pijijiapan,  50  m,  1  (UMMZ);  Guer- 
rero: 1  mi.  SE  San  Andres  de  la  Cruz,  700  m,  1  (UMMZ);  Oaxaca: 
16  km  ENE  Piedra  Blanca,  1  (IB);  Sinaloa:  San  Ignacio,  700  ft,  1 
(KU).  NICARAGUA:  El  Realejo,  1  (KU),  2  (USNM).  VENEZUELA: 
Boli\'.\r:  38  km  S  El  Dorado,  1  (UCV);  Distrtto  Federal:  Caracas 
(Santa  Monica),  900  m,  1  (LS);  Chichiriviche,  1  (UCV).  Choeroniscus  inca. 
BRITISH  GUIANA:  Kamakusa,  1  (AMNH);  Kartabo,  1  (AMNH). 
ECUADOR:  Los  Pozos,  2  (AMNH).  VENEZUELA:  Bolivar:  Chi- 
manta-tepui,  1300  ft,  9  (CNHM).  Choeroniscus  intermedins:  TRINI- 
DAD: Irois  Forest,  1  (AMNH);  Maracas,  1  (AMNH),  Princesto\\Ti,  1 
(holotype  of  C.  intermedius,  AMNH);  Sangre  Grande,  1  (AMNH). 
Choeroniscus  minor.  BR.\ZIL:  P.ara:  Belem,  3  (USNM).  PERU: 
Pasco,  San  Juan,  900  ft,  1  (USNM);  Puerto  Melendez,  above  Maranon, 
1  (AMNH).  Choeroniscus  periosus.  COLOMBIA:  Valle:  Rio  Raposo, 
1  (holotype  of  C.  periosus,  USNM).  Also,  numerous  specimens  of 
Lichonycteris,  Hylonycteris,  and  Choeronycteris  (including  C.  harrisoni). 

Rhisophylla 

The  carolliinine  genus  Rhinophylla  has  until  now  been  kno\Mi  only 
from  the  basin  of  the  Rio  Amazonas  and  the  lowlands  of  northeastern 
South  America  (Husson,  1962:  152-153).  The  sole  representative  of 
the  genus,  R.  pumilio  Peters,  has  been  regarded  as  closely  related  to, 
but  more  speciahzed  than,  the  species  of  the  abundant  and  widespread 
genus  Carollia  (Miller,  1907:  147).  It  is  thus  rather  surprising  to  find 
in  the  collection  of  W.  A.  Thornton  from  the  west  coast  of  Colombia  a 
number  of  specimens  of  a  striking  new  species  of  Rhinophylla  that  is 
even  more  strongly  differentiated  from  Carollia  than  is  R.  pumilio. 

Rhinophylla  alethina,  new  species 

Holotype:  USNM  no.  324988,  adult  male,  skin  and  skull,  collected  13 
July  1962,  by  Wilmot  A.  Thornton,  at  the  Rio  Raposo,  near  sea  level,  27 
km  south  of  Buenaventura,  Departamento  de  \'alle,  Colombia,  original 
number  172. 

Etymology:     Greek,  alethinos,  genuine. 

Distribution:     Known  only  from  the  t>3)e-locality. 

Description:  Size  large  for  genus  (forearm  34.9-37.2  mm).  Col- 
oration blackish,  darkest  anteriorly,  paler  posteriorly.  In  holotype,  head 
and  nape  black,  shading  to  Fuscous-Black  on  rump;  underparts  varying 


49 


New  Bats  from  Colombia  87 

from  black  on  chin  to  Fuscous-Black  on  chest  and  to  Natal  Brown  on 
abdomen.  Another  specimen  (Univ.  del  Valle  220)  slightly  paler:  Fus- 
cous-Black anteriorly  and  Natal  Brown  posteriorly  on  dorsum,  and 
correspondingly  paler  on  underparts.  Hairs  of  dorsum  and  abdomen 
sharply  tricolor:  at  mid-dorsum  Slate-Black  basally,  with  broad  Benzo 
Brown  median  band;  on  sides,  neck,  and  shoulders  median  band  pales 
almost  to  Ecru-Drab  and  shows  through  to  surface  rather  prominently. 
Noseleaf,  lips,  ears,  tragis,  fingers,  forearms,  legs,  feet,  and  all  mem- 
branes blackish.  Fur  soft,  woolly;  legs,  feet,  interfemoral  membranes,  and 
basal  two-thirds  of  forearm  hairy;  interfemoral  membrane  fringed.  Inter- 
femoral membrane  narrow  ( about  5  mm  at  base ) ;  calcar  short  ( less  than 
length  of  metatarsals);  tibia  and  forearm  stout;  pinna  with  anterior 
margin  convex,  posterior  margin  concave,  tip  blunt,  antitragus  triangular; 
tragus  usually  blunt,  with  upper  posterior  margin  entire  or  notched; 
lancet  of  noseleaf  longer  than  broad,  upper  margins  slightly  concave; 
horseshoe  of  noseleaf  with  median  half  of  base  bound  to  lip;  chin  orna- 
ment composed  of  four  parts — a  central  triangular  element  ( apex  down ) , 
a  pair  of  narrow,  elongated  lateral  elements  converging  ventrally  but 
not  meeting  (their  outer  margin  more  or  less  scalloped),  and  a  small, 
circular  median  ventral  element. 

Skull  like  that  of  Rhinophylla  pumilio  but  rostrum  shghtly  heavier 
( broader  and  deeper  anteriorly ) ,  and  a  distinct  low  sagittal  crest  present. 

Dentition,  with  the  exception  of  inner  incisors,  extremely  weak  and 

2     12     3 
reduced;    formula -=32.     Inner   upper    incisor    (P)    large, 

adz-shaped,  with  cutting  edge  entire;  outer  upper  incisor  (P)  small, 
featureless.  Canine  simple,  without  cingulum  or  subsidiary  cusps.  Ante- 
rior upper  premolar  (P^)  small  and  featureless;  posterior  upper  premolar 
( P* )  almost  rectangular,  longer  than  broad,  with  large  median  cusp  and 
tiny  posterior  cusp.  NP  short  and  M"  shorter,  almost  triangular  in  occlusal 
shape,  each  with  a  single  prominent  internal  cusp  (the  metacone); 
protocone  obliterated;  paracone  barely  indicated  in  M\  obliterated  in  M^; 
parastyle  and  metastyle,  particularly  the  latter,  low  and  weakly  devel- 
oped; M^  reduced  to  a  tiny  featureless  spicule. 

Inner  lower  incisors  (Ii)  large,  trilobed  (occasionally  bilobed);  I2 
small,  unicuspid.  Canine  simple,  without  accessory  cusps.  Premolars 
simple,  unicuspid;  anterior  premolar  wider  than  any  succeeding  tooth. 
Molars  very  narrow,  tricuspid;  anterior  and  posterior  cusps  low  on  Mi 
and  M2  and  more  or  less  obliterated  on  Ms. 

Measurements  (Extremes  in  parentheses,  preceded  by  means  and 
followed  by  number  of  individuals  ( only  adults  included ) .  Measurements 
of  the  total  length,  ear,  and  weight  were  made  by  the  collector  in  the 
field.  All  other  measurements  were  made  by  me  in  the  laboratory. ) :  Total 
length  $  55,  58;  hind  foot  $11  (11-11)  4,  $  11  (10-11)  6;  ear  from 
notch  S  15,  16;  forearm  $  36.4  (35.5-37.2)  4,  $  35.7  (34.9-36.6)  4; 
tibia  9  12.3  (11.2-12.9)  4,  $  12.0  (11.5-12.5)  4;  calcar  2  3.1  (3.0- 
3.5)  4,  $  3.4  (3.3-3.5)  5.   Weight  $  12  gm,  16  gm. 


50 


88     Proceedings  of  the  Biological  Society  of  Washington 

Cranial  measurements  of  male  holotype:  Greatest  length  of  skull  19.5, 
zygomatic  breadth  10.7+ ;  postorbital  breadth  5.3,  braincase  breadth  8.9, 
braincase  depth  7.5,  maxillary  tooth  row  length  4.9,  postpalatal  length  7.2, 
palatal  breadth  at  M"  6.4,  palatal  breadth  at  canines  5.1. 

Comparisons:  Specimens  of  R.  alethina  are  slightly  larger  than  speci- 
mens of  R.  pumilio  from  the  valley  of  the  Rio  Amazonas;  have  the  inter- 
femoral  membrane  narrower;  calcar  shorter;  hind  legs  stouter;  legs,  feet, 
and  interfemoral  membrane  ( including  posterior  margin )  more  hairy; 
fur  more  woolly  in  texture;  and  coloration,  including  that  of  lips,  ears, 
and  membranes,  darker,  more  blackish.  As  noted  in  the  description,  the 
skulls  of  the  two  species  are  very  similar.  However,  except  for  the  inner 
incisors,  the  teeth  of  R.  alethina  are  smaller  and  weaker,  and  the  tooth 
rows  are  shorter  than  in  R.  pumilio.  R.  alethina  has  cutting  edges  of  V 
and  I2  entire  rather  than  notched;  P*  shorter;  cusps  of  upper  molars  more 
reduced;  and  I2,  P\  M^,  and  lower  molars  notably  smaller. 

Aside  from  its  relative  R.  pumilio,  R.  alethina  is  likely  to  be  confused 
only  with  the  Glossophaginae  and  with  Carollia  castanea.  Its  non-exten- 
sible tongue  and  lack  of  rostral  elongation  are  sufficient  to  distinguish 
it  from  the  Glossophaginae.  From  Carollia  castanea  it  can  be  distin- 
guished easily  by  its  blacker  coloration,  narrow,  fringed  interfemoral 
membrane,  hairy  legs,  simple  chin  ornament,  and  smaller,  simplified  teeth. 
In  most  of  these  characteristics  R.  alethina  differs  more  from  the  species 
of  Carollia  than  R.  pumilio  does. 

Specimens  examined:  Rhinophxjlla  alethina.  COLOMBIA:  Valle 
Rio  Raposo,  11  (including  the  holotype,  USNM),  1  (Univ.  del  Valle). 
Rhinophylla  pumilio.  BRAZIL:  ParA:  Belem,  52  (USNM).  ECUADOR: 
Boca  de  Rio  Curaray,  2  (USNM).  PERU:  Pasco:  San  Juan,  900  ft, 
4  (USNM). 

Literature  Cited 

Handley,  C.  O.,  Jr.  1959.  A  revision  of  American  bats  of  the  genera 
Euderma  and  Plecotus.  Proc.  U.S.  Nat.  Mus.,  110:  95-246, 
27  figs. 

HussoN,  A.  M.  1962.  The  bats  of  Suriname.  Zoologische  Vemhande- 
lingen,  Rijksmus.  Nat.  Hist.,  Leiden,  58:  1-282,  30  pis.,  39 
figs. 

Miller,  G.  S.,  Jr.  1907.  The  families  and  genera  of  bats.  U.S.  Nat. 
Mus.  Bull.  57,  xvii  +  282  pp.,  14  pis.,  49  figs. 

RiDGWAY,  R.  1912.  Color  standards  and  color  nomenclature,  iv  +  44  pp., 
53  pis. 

Sanborn,  C.  C.  1954.  Bats  from  Chimanta-tepui,  Venezuela,  with  re- 
marks on  Choeroniscus.     Fieldiana- Zoology,  34:   289-293. 


51 


BENSON — STATUS   OF   REITHKODONTOMYS   MONTANUS  139 

THE  STATUS  OF  REITHKODONTOMYS  MONTANUS  (BAIRD) 

By  Seth  B.  Benson 

The  status  and  relationships  of  Reithrodontomys  montanus  have  been  uncer- 
tain ever  since  this  harvest  mouse  was  named  and  described  by  Baird  in  1855. 
Study  of  the  type  specimen,  and  of  specimens  collected  in  the  type  locality 
of  R.  montanus,  has  revealed  that  all  the  specimens,  except  the  type  itself,  are 
examples  of  the  species  Reithrodontomys  megalotis  (Baird).  Confusion  has 
arisen  because  these  specimens  have  been  mistakenly  referred  to  R.  montanus. 

The  nomenclatural  history  is  as  follows.  Baird  (1855,  p.  355)  described 
Reithrodon  montanus  on  the  basis  of  a  single  specimen  collected  by  a  Mr. 
Kreutzfeldt  [  =  J.  Creutzfeldt,  botanist  of  Gunnison's  expedition]  at  "Rocky 
Mountains,  Lat.  38°."  Later,  Baird  (1857,  p.  450)  gave  the  locality  as 
"Rocky  Mountains,  39°."  Coues  (1874,  p.  186)  listed  Ochetodon  montanus 
as  a  questionable  species.  This  he  also  did  later  (1877,  p.  130),  stating 
"The  single  specimen  is  too  imperfect  to  permit  of  final  characterization,  or 
to  enable  us  to  come  to  any  positive  conclusion;  but  if  the  size  and  coloration 
it  presents  are  really  permanent,  we  should  judge  it  entitled  to  recognition 
as  a  vahd  species.  At  present,  however,  we  regard  it  with  suspicion  and  are 
unwilhng  to  endorse  its  validity." 

This  remained  the  status  of  the  name  until  Allen  (1893,  p.  80),  after  exam- 
ining the  type  specimen,  stated  "I  have  therefore  no  hesitation  in  recognizing 
Reithrodontomys  montanus  (Baird)  as  a  well-marked,  valid  species,  which  will 
probably  be  found  to  range  from  the  eastern  base  of  the  Rocky  Mountains 
eastward  to  middle  Kansas." 

WTien  Allen  (1895)  revised  the  harvest  mice  the  type  of  montanus  was  still 
unique.  In  his  treatment  of  the  species  (pp.  123-125)  he  determined  the  type 
locality  to  be  the  upper  part  of  the  San  Luis  Valley  in  Colorado.  He  stated 
that  "Until  this  region  has  been  thoroughly  explored  for  'topotypes'  of  R. 
montanus,  it  would  be  obviously  improper  to  reject  this  species  as  unidentifi- 
able or  to  give  the  name  precedence  over  R.  megalotis  for  the  form  here  recog- 
nized under  that  name." 

At  this  time  the  species  currently  recognized  as  albescens  was  not  known, 
although  Allen  actually  had  specimens  which  he  confused  with  the  form  now 
known  as  R.  megalotis  dychei  (see  Howell,  1914,  p.  31).  Subsequently  Cary 
(1903,  p.  53)  described  Reithrodontomys  albescens  from  Nebraska,  stating 
that  the  species  required  "no  close  comparison  with  any  described  Reithro- 
dontomys." Bailey  (1905,  p.  106)  described  Reithrodontomys  griseus  from 
Texas,  and  remarked  that  it  probably  graded  into  albescens. 

In  1907  Cary  visited  Medano  Springs  Ranch  in  search  of  topotypes  of  R. 
montanus.  He  collected  twenty  specimens,  most  of  them  immature,  which 
he  identified  as  montanus.  Cary  (1911,  pp.  108-110),  following  a  manuscript 
of  A.  H.  Howell,  regarded  R.  montanus  as  a  species  related  to  R.  albescens  and 
R.  griseus.    He  placed  albescens  as  a  subspecies  of  montanus. 


&2 


140 


JOURNAL   OF   MAMMALOGY 


When  Howell  (1914)  revised  the  harvest  mice,  the  specimens  from  the  type 
locality  of  montanus  consisted  of  the  type  specimen  and  the  specimens  col- 
lected by  Gary  at  Medano  Springs  Ranch.  In  this  revision  Howell  altered 
his  earlier  opinions  concerning  the  relationships  of  montanus.  He  wrote 
(p.  26)  "The  species,  although  combining  in  a  remarkable  degree  the  char- 
acters of  the  megalotis  and  albescens  groups,  seems  not  to  be  directly  connected 
with  either  of  them.  It  is  perhaps  best  placed  in  the  megalotis  group,  but 
seems  not  to  intergrade  with  any  member  of  it."  He  pointed  out  that  the 
relationships  of  the  species  were  yet  not  clear,  since  the  type  specimen  did  not 
agree  with  any  of  the  "topotypes"  collected  by  Gary,  but  instead  resembled 
specimens  of  R.  a.  griseus  from  Texas.  Because  the  color  of  the  "topotypes" 
agreed  with  the  original  description  of  montanus,  he  decided  to  "consider  the 
tj-pe  skull  aberrant,  and  to  continue  to  use  the  name  for  the  form  represented 


Fig.  1.  Drawings  Made  from  Photographs  of  Skulls  of  Harvest  Mice.    Natural 

Size 

a.  Reithrodontomys  megalotis  subsp.,  no.  61120,  Mus.  Vert.  Zool.,  from  Medano  Ranch, 
15  miles  northeast  of  Mosca,  Alamosa  County,  Colorado. 

b.  Reithrodontomys  montanus  montanus,  type  specimen,  no.  1036/441,  U.  S.  Nat.  Mus., 
from  upper  end  of  San  Luis  Valley,  Colorado. 

c.  Reithrodontomys  montanus  griseus,  no.  58737,  Mus.  Vert.  Zool.,  from  3  miles  north 
of  Socorro,  Socorro  County,  New  Mexico. 

by  the  modern  series."     It  might  be  mentioned  here  that  no  specimens  of  the 
albescens  group  have  as  yet  been  taken  near  the  type  locality  of  montanus. 

In  1933,  Miss  Annie  M.  Alexander  and  Miss  Louise  Kellogg  collected 
harvest  mice  from  several  localities  in  Golorado  and  New  Mexico  including 
the  type  localities  of  R.  megalotis  aztecus  and  R.  montanus.  Two  of  the  three 
specimens  from  the  Medano  Ranch,  15  miles  northeast  of  jMosca,  Alamosa 
Gounty,  Golorado,  were  adults  similar  to  adult  topotypes  of  aztecus.  The 
third,  a  young  individual,  was  so  much  smaller  that  at  first  I  judged  it  was  of  a 
different  species.  I  suspected  then  that  Howell's  treatment  of  montanus  was 
the  result  of  confusing  two  distinct  species,  one  a  small  form  like  albescens,  the 
other  a  larger  one  hke  megalotis.  The  occurrence  of  two  species  at  this 
locality  seemed  possible,  since  albescens  occurs  with  dychei  in  Nebraska, 
griseus  is  known  to  occur  with  dychei  in  Kansas,  and  in  1933  I  collected  mega- 
lotis and  griseus  together  in  the  bottom-land  of  the  Rio  Grande,  three  miles 


53 


BENSON — STATUS   OF   REITHRODONTOMYS   MONTANUS  141 

north  of  Socorro,  New  Mexico,  which  is  in  the  same  drainage  system  as  San 
Luis  Valley. 

At  my  request  the  Bureau  of  Biological  Survey  loaned  me  16  of  the  speci- 
mens collected  by  Gary  at  Medano  Ranch.  Only  one  of  these  was  fully 
adult  (the  one  whose  skull  is  figured  as  montanus  in  Howell's  revision) .  Among 
the  younger  specimens  were  some  which  matched  the  smallest  of  the  three 
specimens  collected  by  Miss  Alexander  and  Miss  Kellogg,  and  the  rest  formed 
a  series  approaching  the  largest  specimens.  The  adult  specimen  collected  by 
Gary  is  smaller  than  the  other  two  adults,  yet  is  similar  to  them  in  most 
characters.  It  was  obvious  that  all  belonged  to  a  single  species.  I  concluded 
that  all  the  Medano  Ranch  specimens  I  had  examined  were  of  the  species 
currently  known  as  megalotis.  It  was  also  obvious  that  if  the  type  of  montanus 
were  conspecific  with  the  other  San  Luis  Valley  specimens,  megalotis  would 
become  a  synonym  of  montanus,  since  montanus  has  priority. 

Through  the  courtesy  of  Dr.  Remington  Kellogg  and  others  in  charge  of  the 
collection  of  mammals  in  the  United  States  National  Museum,  I  was  granted 
the  loan  of  the  type  specimens  of  R.  megalotis  and  R.  montanus.  After  study- 
ing these  specimens  I  reached  the  following  conclusions:  (1)  The  Medano 
Ranch  specimens  are  conspecific  with  the  type  of  megalotis;  (2)  the  type 
specimen  of  montanus  is  specifically  distinct  from  megalotis,  and  is  conspecific 
with  albescens  and  griseus.  Some  characters  in  which  the  type  of  montanus 
and  specimens  of  griseus  (MVZ  no.  41192,  from  Hemphill  Go.,  Texas;  no. 
56220,  from  44  miles  northwest  of  Roswell,  N.  M.;  and  no.  58737,  from  3  miles 
north  of  Socorro,  N.  M.)  differ  from  megalotis  are:  smaller  size;  shorter,  more 
depressed  rostrum;  narrower  interorbital  space;  relatively  shorter  brain  case. 

As  a  result,  megalotis  is  not  a  synonym  of  montanus,  and  montanus  becomes 
the  specific  name  for  the  species  currently  known  as  albescens.     Until  addi- 
tional specimens  of  montanus  from  San  Luis  Valley  are  available  to  allow  a 
more  thorough  appraisal  of  its  characters,  it  seems  best  to  regard  albescens  and 
griseus  as  valid  races  of  montanus,  although  it  is  quite  likely  that  griseus  may 
become  a  synonym  of  montanus.     The  three  races  here  recognized  are : 
Reithrodontomys  montanus  montanus  (Baird) 
Reithrodontomys  montanus  albescens  Gary 
Reithrodontomys  montanus  griseus  Bailey. 

It  may  be  well  to  remark  here  that  all  the  available  information  indicates 
that  the  species  R.  montanus  is  rarely  abundant  and  that  it  prefers  more  arid, 
sandier  ground  than  does  its  relative  R.  megalotis,  although  both  species  may 
be  found  together. 

The  racial  identity  of  the  San  Luis  Valley  megalotis  has  also  presented  some 
problems.  At  first  I  referred  them  to  the  race  aztecus  because  some  of  them 
fell  within  the  range  of  variation  present  in  specimens  from  within  the 
distributional  area  assigned  to  aztecus  in  Howell's  revision.  In  addition, 
there  was  so  much  variation  in  size  in  the  few  adults  available  to  me  that  I 


54 


142  JOURNAL   OF    MAMMALOGY 

felt  it  was  possible  they  did  not  truly  represent  the  population,  and  so  could 
not  serve  as  a  satisfactory  basis  for  the  description  of  a  new  race.  However, 
Mr.  Howell,  who  has  restudied  the  problem  with  the  aid  of  a  greater  amount 
of  material  than  was  available  to  me,  has  concluded  that  the  San  Luis  Valley 
megalotis  represent  an  unnamed  race.  He  will  describe  this  race  in  another 
article. 

LITERATURE  CITED 

Allen,  J.  A.  1893.  List  of  mammals  collected  by  Mr.  Charles  P.  Rowley  in  the  San 
Juan  Region  of  Colorado,  New  Mexico  and  Utah,  with  descriptions  of  new  spe- 
cies.    Bull.  Amer.  Mus.  Nat.  Hist.,  vol.  5,  pp.  69-84.     April  28,  1893. 

1895.     On  the  species  of  the  genus  Reilhrodontomys.     Bull.  Amer.  Mus.  Nat. 

Hist.,  vol.  7,  pp.  107-143.     May  21,  1895. 

Bailey,  V.  1905.  Biological  Survey  of  Texas.  U.  S.  Dept.  Agric,  North  Amer. 
Faima  no.  25,  222  pp.,  16  pis.,  24  figs.     October  24,  1905. 

Baird,  S.  F.  1855.  Characteristics  of  some  new  species  of  North  American  Mammalia, 
collected  chiefly  in  connection  with  U.  S.  Surveys  of  a  Railroad  route  to  the 
Pacific.     Proc.  Acad.  Nat.  Sci.  Philadelphia,  vol.  7,  April,  1855,  pp.  333-336. 

1857.     General  report  upon  the  mammals  of  the  several  Pacific  Railroad 

routes.     U.  S.  Pac.  R.  R.  Expl.  and  Surv.,  vol.  8,  pt.  1,  xxxiv  +  764  pp.,  60  pis. 

Gary,  M.  1903.  A  new  Reithrodontomys  from  western  Nebraska.  Proc.  Biol.  Soc. 
Washington,  vol.  16,  pp.  53-54.     May  6,  1903. 

1911.     A  biological  survey  of  Colorado.     U.  S.  Dept.  Agric,  North  Amer. 

Fauna  no.  33,  256  pp.,  12  pis.,  39  figs.     August  17,  1911. 

CouES,  E.  1874.  Synopsis  of  the  Muridae  of  North  America.  Proc.  Acad.  Nat.  Sci. 
Philadelphia,  1874,  pp.  173-196. 

1877.     No.  I. — Muridae,  in  Coues  and  Allen,  Monog.  North  Amer.  Rodentia 

(=  U.  S.  Geol.  Surv.  Terr.  [Hayden],  vol.  9),  pp.  481-542. 

Howell,  A.  H.  1914.  Revision  of  the  American  harvest  mice.  U.  S.  Dept.  Agric, 
North  Amer.  Fauna  no.  36,  97  pp.,  7  pis.,  6  figs.     June  5,  1914. 

Museum  of  Vertebrate  Zoology,  University  of  California,  Berkeley,  California. 


55 


A  REVISION  OF  THE  WOOD  RAT  NEOTOMA  STEPHENSl 
By  Donald  F.  Hoffmeister  and  Luis  de  la  Torre 

Within  the  last  few  years,  some  field  guides  to  mammals  of  the  United 
States  have  appeared  which  do  not  include  the  wood  rat  Neotoma  stephensi. 
The  imphcation  is  that  Neotoma  stephensi  is  not  a  valid  species.  Some  spe- 
cific characters  of  Neotoma  stephensi  were  enumerated  in  the  original  descrip- 
tion by  Goldman  in  1905,  and  its  specific  distinctness  (from  Neotoma  lepida) 
was  reaffirmed  by  Goldman  in  1932.  Because  of  the  previous  confusion  of 
Neotoma  stephensi  with  Neotoma  lepida,  and  even  the  subsequent  confusion 
of  the  two  species  following  Goldman's  review  (Jour.  Mamm.,  13:  59-67, 
1932),  it  is  somewhat  understandable  that  some  authors  might  question  the 
validity  of  stephensi.  Even  the  recently  pubhshed  work  by  Hall  and  Kelson 
(The  Mammals  of  North  America,  2:  690,  1959)  fails  to  show  the  coexistence 
of  N.  lepida  and  N.  stephensi  in  parts  of  their  range,  a  fact  which  lends  addi- 
tional evidence  for  the  distinctness  of  the  two  species.  With  more  adequate 
material,  and  using  Goldman's  work  as  a  starting  point,  we  have  attempted 
to  define  more  clearly  the  species  N.  stephensi. 

Many  persons  have  made  available,  for  study,  specimens  of  Neotoma 
stephensi  in  their  collections.  We  should  especially  like  to  thank  Richard  G. 
Van  Gelder,  Stanley  P.  Young,  Viola  Schantz,  Laurence  Huey,  Seth  B.  Benson, 
William  Z.  Lidicker,  and  William  H.  Burt.  Specimens  from  the  following 
collections  have  been  examined  (the  abbreviations  in  parentheses  are  used 
under  Specimens  examined):  American  Museum  of  Natiural  History  (AM); 
United  States  Biological  Survey  (BS);  Grand  Canyon  National  Park  Museum 
(GC);  San  Diego  Society  of  Natural  History  (SD);  University  of  California, 
Museum  of  Vertebrate  Zoology  (UC);  University  of  Illinois,  Museum  of 
Natural  History  (UI);  University  of  Michigan,  Museum  of  Zoology  (UM). 
Capitalized  color  terms  are  from  Ridgway  ( Color  Standards  and  Color  Nomen- 
clature, 1912).  All  measurements  are  in  millimeters.  Under  Additional  records 
we  have  included  localities  from  which  the  species  is  known  but  from  which 
we  have  not  examined  specimens.  The  Graduate  College  of  the  University 
of  Illinois  has  financially  aided  us  in  this  study.  Illustrations  were  prepared 
by  Alice  A.  Boatright  and  Harry  C.  Henriksen  of  the  University  of  Illinois. 

GENERAL  CHARACTERS  OF  THE  SPECIES 

Obvious  characters  of  Neotoma  stephensi,  which  in  part  are  diagnostic,  are 
the  presence  of  a  semi-bushy  tail  ( bushier  than  in  all  species  except  N.  cinerea ) 
in  a  medium-  to  small-sized  Neotoma;  dusky  coloration  extending  down  the 
top  of  the  foot  one-fourth  to  one-third  the  distance  below  the  ankle;  skull 
resembling  IV.  lepida.  A  closer  study  indicates  the  following  characters  are 
diagnostic: 

Baculum. — Exclamation-mark-shaped  or  wedge-shaped  (Fig.  1);  small,  being 
one-fifth  or  less  than  the  length  of  the  baculum  in  N.  lepida;  smaller  than  in 


56 


Nov.,  1960  HOFFMEISTER  AND  DE  LA  TORRE— NEOTOMA  477 

any  species  of  Neotoma  found  in  the  United  States;  similar  in  size  and  shape 
to  that  of  Neotoma  phenax,  except  not  indented  along  sides  and  thus  not 
"violin-shaped."  When  everted  from  the  prepuce,  the  distinctively  small  size 
of  the  baculum  in  N.  stephensi  is  clearly  noticeable,  and  in  contrast  to  the 
condition  in  Neotoma  lepida,  N.  albigula,  and  N.  mexicana.  In  one  specimen 
of  N.  s.  relicta,  the  baculum  is  identical  to  that  in  N.  s.  stephensi. 

Skull. — Teeth:  The  pattern  of  M^  together  with  features  of  M^  serves  to 
distinguish  N.  stephensi  in  most  cases.  In  M^,  the  antero-medial  fold  is  usually 
absent  or,  if  present,  is  shallow,  approaching  albigula,  never  deeply  re-entrant 
as  in  mexicana.  In  M',  the  postero-labial  fold  (Fig.  1)  is  directed  postero- 
mediaUy  and  "terminates"  posterior  to  the  lingual  fold.  In  N.  lepida,  the 
postero-labial  fold  (Fig.  1)  is  directed  medially  and  less  posteriorly,  nearly 
meeting  the  lingual  fold.  In  M^  of  stephensi,  the  second  loph  is  usually  long 
and  narrow,  extending  diagonally  across  the  tooth  (Fig.  1).  In  this  regard, 
it  is  similar  to  N.  mexicana  and  N.  albigula,  but  differs  from  N.  lepida  in 
which  the  second  loph  is  usually  broad  labially  and  nearly  at  right  angles  to 
the  long  axis  of  the  toothrow  (Fig.  2). 

In  N.  stephensi,  the  lingual  fold  of  M3  is  as  deep  as  or  deeper  than  the 
labial  fold  (Fig.  2),  whereas  in  N.  lepida  and  N.  albigula,  the  lingual  fold  is 
shorter  than  the  labial  fold.   In  N.  mexicana,  both  conditions  seem  to  occur. 

Rostrum:  The  rostrum  is  narrower  than  in  any  other  species  within  the 
range  of  N.  stephensi  ( Fig.  3 ) .  Generally,  the  nasals  in  stephensi  are  truncate 
posteriorly,  rarely  sharply  pointed  as  is  common  in  lepida  and  albigula 
(Fig.  3).  The  posterior  extensions  of  the  premaxillaries  seldom  expand  pos- 
teriorly as  in  albigula,  but  are  more  as  in  mexicana  except  that  they  are  longer. 

Interorbital,  region:  The  region  between  the  orbits  is  broader  and  less 
depressed  than  in  either  lepida,  albigula,  or  mexicana.  In  some  instances,  it 
is  difficult  to  distinguish  between  stephensi  and  lepida  on  the  basis  of  this 
character.  The  supraorbital  ridges  in  stephensi  tend  to  remain  lateral  as  they 
continue  forward  toward  the  rostrum,  whereas  in  the  other  species  these 
ridges  approach  the  midUne,  ending  almost  in  line  with  the  posterior  exten- 
sions of  the  premaxillaries  (Fig.  3). 


second  loph  ^      »  .    ^      . 

stephensi 


postero-labial  fold 


stephensi  iepida  lepida 

Fig.  1. — Third  upper  molar   (x6.5)   and  baculum  (x2.4)   of  Neotoma  stephensi  and 
Neotoma  lepida. 


57 


478 


JOURNAL  OF  MAMMALOGY 


Vol.  41,  No.  4 


Of  perhaps  lesser  diagnostic  significance  when  compared  with  N.  lepida 
are  the  following  skull  characters:  upper  incisors  strongly  recurved;  tubercle  on 
outer  face  of  mandible  at  base  of  lower  incisor  hardly  noticeable,  whereas 
more  nearly  knoblike  in  lepida. 

External  features. — The  bushiness  of  the  tail,  particularly  the  terminal  third, 
approaches  that  of  Neotoma  cinerea.  The  tail  is  far  more  bushy  than  in  any 
other  species  within  the  range  of  stephensi,  and  probably  exceeds  that  of 
any  wood  rat  except  cinerea.  In  young  stephensi,  only  a  few  weeks  old,  the 
tail  already  is  bushy,  and  specific  recognition  is  possible  on  this  character. 

On  the  hind  foot,  a  wedge  of  dusky-colored  hair  may  extend  onto  the  dorsal 
surface  as  much  as  one-third  the  distance  to  the  base  of  the  toes.  In  most 
specimens  of  N.  lepida,  particularly  in  those  races  which  are  not  melanistic, 
the  dorsal  surface  of  the  foot  is  whitish,  with  the  dusky  color  stopping  at  the 
tarsal  region. 

The  underparts  are  suffused  with  an  ochraceous  or  buffy  wash  in  nearly 
all  specimens.  In  N.  stephensi  stephensi  the  throat  region  also  shows  this  same 
wash,  but  the  region  between  the  forelegs  is  whitish.  In  JV.  stephensi  relicta, 
the  wash  does  not  extend  onto  the  throat  and  thus  it  is  usually  white.  The 
coloration  of  the  underparts  in  N.  s.  stephensi  is  similar  to  that  in  most  speci- 
mens of  the  dark  races  of  IV.  lepida,  such  as  monstrabilis  and  harteri,  and  is 
thus  noticeably  different  than  in  the  light-colored  races  of  the  latter  species. 
Where  N.  lepida  occurs  within  the  range  of  N.  stephensi,  nearly  all  specimens 
of  lepida  have  light-colored  underparts  and  thus  this  character  aids  in  dis- 
tinguishing the  two. 


upper  molars 


lower  molars 


£mi 


stephensi 


lepida 


albigula 


stephensi 


lepida 


Fig.  2. — Occlusal  view  of  right  upper  molars  of  Neotoma  stephensi,  N.  lepida,  N.  albigula, 
and  left  lower  molars  of  N.  stephensi  and  N.  lepida  (  x6.5). 


58 


Not;.,  1960 


HOFFMEISTER  AND  DE  LA  TORRE— NEOTOMA 


479 


Stephens' 


tepida 


albigufa 


mexicona 


Fig.  3. — Dorsal  view  of  anterior  part  of  skull  of  Neotoma  stephensi,  N.  lepida,  N. 
albigula,  and  N.  mexicana  (  X 1 ) . 

VABIATION 

Age. — In  N.  stephensi,  we  can  recognize  four  groups  which  include  young 
animals,  old  animals,  and  two  categories  between  these  extremes.  These 
groups  are  based  on  the  degree  of  eruption  and  wear  of  the  upper  molar  teeth. 
We  attempted  to  corroborate  this  grouping  by  the  use  of  other  characters, 
such  as  closure  of  sutures,  size  and  proportion  of  various  parts  of  the  skull, 
and  molt,  but  these  proved  to  be  of  httle  help.  Further  discussion  of  the 
younger  groups  is  given  under  Growth  and  Reproduction. 

Group  1.  Immatures;  M^  not  erupted  or  in  the  process  of  erupting  and 
occlusal  surface  of  posterior  loph  isolated  from  that  of  more  anterior  lophs. 

Group  2.  Young  adults;  females,  at  least,  sexually  mature.  Folds  of  M^, 
as  seen  laterally,  continuing  down  below  alveolus;  M^  fully  erupted  and  oc- 
clusal pattern  usually  complete  with  posterior  loph  rarely  isolated. 

Group  3.  Adults;  folds  of  M^  not  extending  to  alveolus,  but  to  or  below 
an  arbitrary  midpoint  between  alveolus  and  occlusal  surface. 

Group  4.  Old  adults;  folds  of  M^  very  short  and  not  reaching  midpoint 
between  occlusal  surface  and  alveolus.    Folds  may  be  entirely  absent. 

Sexual. — Although  there  is  a  size  difference  between  males  and  females, 
it  is  less  marked  in  certain  age  groups.  From  our  sample,  we  find  that  in 
Groups  1  and  2,  the  sexual  difference  is  slight.  In  Group  3,  males  usually 
average  larger  than  females  in  most  measurements.  For  example,  in  specimens 
from  the  Hualpai  Mountains  (65  5,  109  9  ),  the  Grand  Canyon  (45  5,  49  2  ), 
and  Wupatki  (455,  499),  the  males  are  larger  than  the  females  by  per- 
centages ranging  from  1  to  13  in  most  measurements.  In  all  three  localities, 
however,  the  females  average  larger  than  the  males  in  length  of  maxiUary 
toothrow  as  follows:  Hualpai  Mountains,  2.3;  Grand  Canyon,  1.2;  Wupatki, 
1.2  per  cent.  The  larger  average  size  of  the  toothrow  in  females  is  also  indi- 
cated in  specimens  from  other  localities.  Group  4  is  represented  by  too  few 
individuals  to  determine  sexual  differences.  Aside  from  the  quantitative  dif- 
ferences pointed  out,  the  skull  of  adult  females  is  characteristically  short  and 
broad,  in  contrast  to  the  long  and  narrower  skull  of  the  males. 


59 


480  JOURNAL  OF  MAMMALOGY  Vol.  41,  No.  4 

No  sexual  difference  in  color  was  apparent. 

Color. — The  color  of  an  "average"  specimen  consists  of  a  light  buff  wash 
extending  from  the  chest  to  the  inguinal  region.  The  chest  is  white,  with 
the  throat  a  buffy  color  with  the  hair  plumbeous  basally  and  buffy-tipped. 
The  white  of  the  chest  may  extend  anteriorly  to  the  chin  as  a  median  narrow 
stripe.    The  inguinal  area  is  whitish. 

The  coloration  of  the  underparts,  including  the  buffy  wash,  throat,  and 
chest  color,  in  any  one  population,  may  be  highly  variable.  For  example, 
near  Montezuma  Well,  Yavapai  County,  Arizona,  one  specimen  has  98  per 
cent  of  the  underparts  heavily  washed  with  a  dark  buff,  one  has  little  or  no 
buff,  and  one  has  no  white  on  the  chest  and  throat.  Still  other  specimens 
from  here  show  varying  stages  of  intermediacy.  In  other  populations,  indi- 
viduals can  be  found  that  have  the  throat  entirely  white,  with  the  basal 
portions  of  the  hairs  not  plumbeous  or  gray-colored.  The  whitish  throat  is 
"typical"  of  another,  unrelated  species — albigula.  Such  occurrences  of  "white- 
throatedness"  are  widely  scattered  throughout  the  range  of  the  species,  being 
found  in  populations  from  the  Hualpai  Mountains  in  the  northwest  to  the 
Burro  Mountains  in  the  southeast. 

The  extreme  of  this  white-throatedness  is  found  in  N.  stephensi  relicta.  In 
this  race,  nearly  all  individuals,  and  probably  every  adult,  have  white  throats. 
Within  the  race  stephensi,  certain  populations  have  most  of  the  adults  with 
white  throats.  This  is  true  for  the  populations  at  Hilltop,  west  end  of  Grand 
Canyon  National  Park,  but  is  not  true  for  other  populations  within  the  Park 
or  for  most  specimens  from  the  Hualpais.  The  population  from  the  Burro 
Mountains,  New  Mexico,  has  all  of  the  specimens  white-throated.  In  general, 
specimens  with  the  entire  throat  region  white  have  the  buffy  wash  over  the 
abdominal  region  greatly  reduced  or  entirely  lacking.  Thus  most  specimens 
of  relicta  and  specimens  of  stephensi  from  Hilltop  and  the  Burro  Mountains 
lack  the  buffy  wash. 

Variation  of  the  dorsal  coloration  within  a  population  is  less  easily  observed. 
The  geographical  variation  of  this  color,  within  subspecies,  is  discussed  beyond 
and  illustrated  in  Plate  I. 

GROWTH   AND   REPRODUCTIGN 

In  the  absence  of  growth  data  for  IV.  stephensi,  we  have  been  guided  by 
previous  work  in  other  species  of  Neotoma,  especially  in  N.  albigula  from 
Arizona  (Richardson,  Jour.  Mamm.,  24:  134,  1943).  Although  two  species 
may  well  differ  markedly  in  their  rate  of  growth  and  reproductive  patterns 
due  to  different  heredity  and  different  environmental  conditions,  we  have 
used  the  N.  albigula  information  to  put  forth  tentative  conclusions,  leaving  it 
to  future  work  to  prove  or  disprove  the  validity  of  our  interpretations.  We 
have,  thus,  assumed  that  the  progress  of  growth  is  essentially  the  same  in 
N.  albigula  from  Arizona  as  it  is  in  IV.  stephensi  from  that  area,  and  that  the 
gestation  period  in  N.  stephensi  is,  as  in  other  species,  approximately  30  days 


60 


Nov.,  1960 


HOFFMEISTER  AND  DE  LA  TORRE— NEOTOMA 


481 


in  length.  From  the  growth  curve  of  head  and  body  size  in  N.  albigula  ( Rich- 
ardson, op.  cit.),  approximate  ages  and  thus  dates  of  birth  were  calculated  for 
our  sample  of  immature  specimens  ( Group  1 )  of  N.  stephensi.  Table  1  indi- 
cates the  chronological  distribution  of  Group  1  and  Group  2  specimens  studied, 
and  the  dates  of  capture  of  pregnant  and  lactating  females. 

The  near  disappearance  of  Group  1  individuals  following  the  middle  of 
August,  and  the  clear  increase  of  Group  2  animals  from  this  time  on,  strongly 
suggest  that  Group  2  is  a  composite  group.  Group  2  specimens  taken  in  June, 
July  and  August  most  likely  are  young  born  late  in  the  preceding  year,  that  is, 
in  August,  September  and  October.  Specimens  taken  in  September  and 
October,  however,  probably  represent  young  of  the  year,  born  in  the  early 
months  following  the  earliest  breeding  period. 


ian«tK-iXfiiiHi''Wu*'M3SiaMM:A~'-^  %^M* 


PLATE  I 

Variation   in   the   intensity  of  the  over-all  color   in    'Scotoma   stephensi.    The   darkest- 
colored  populations  are  represented  by  the  darkest  area;  the  lightest,  by  the  lightest  area. 


61 


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Vol.  41,  No.  4 


Table    L — Bimonthly   distribution   of   Group    1    and   Group   2   individuals,   ivith   dates   of 
capture  and  age  of  pregnant  and  lactaiing  females 


Date  of 
Capture 


Group  1 


Group  2 


Pregnant  ?  ? 


Lactating  ?  9 


April 

16-30 

May 

1-15 

1 

1 

16-31 

1 

June 

1-15 

3 

16-30 

5 

1 

July 

1-15 

6 

8 

16-31 

6 

1 

Aug. 

1-15 

6 

5 

16-30 

3 

Sept. 

1-15 

1 

4 

16-30 

1 

11 

Oct. 

1-15 

11 

Apr.  30   (Group  4) 


June  18   (Group  3) 
July  13   (Group  2) 


Late  Sept. 


June  26   ( Group  3 ) 
July  15   (Group  2) 


Aug.  22   (Group  4) 


Using  the  growth  rate  of  IV.  albigula  as  a  guide,  the  dates  of  birth  of  Group 
1  individuals  begin  in  early  March,  and  thus  mating  must  begin  early  in  Feb- 
ruary. The  dates  of  birth  appear  to  form  two  groups — one  including  March 
and  April,  and  the  other  from  the  middle  of  May  to  the  middle  of  July.  This 
suggests  two  litters  but,  if  a  litter  can  follow  another  in  a  period  of  15  days,  as 
has  been  reported  for  N.  albigula,  it  is  quite  possible  that  IV.  stephensi  may 
have  more  than  two  litters.  The  usual  litter  seems  to  consist  of  two  young,  as 
indicated  by  four  cases  of  pregnant  females  containing  two  embryos  each.  It 
is  of  interest  that  one  of  the  pregnant  animals  taken  on  13  July,  and  a  lactating 
female  taken  15  July,  were  clearly  of  Group  2.  The  date  of  capture,  in  addition 
to  the  age  group  of  these  animals,  certainly  seems  to  indicate  that  females 
reach  sexual  maturity  the  second  season  after  birth.  These  females  must  have 
been  born  in  the  spring  or  summer  of  the  preceding  year. 

HABITAT 

Neotoma  stephensi  occupies  an  ecological  niche  quite  distinctive  from  that 
of  Neotoma  lepida.  In  our  collecting  experience,  IV.  stephensi  is  found  in 
rocky  situations,  usually  where  the  rocks  are  in  piles,  and  usually  where  there 
are  piiions  and  junipers.  Neotoma  stephensi  is  not  a  cliff  dweller,  although 
it  may  be  found  in  the  general  vicinity  of  cliffs,  but  is  found  where  the  rocks 
have  rolled  down  and  become  stacked.  However,  even  though  suitable  rocks 
may  be  present,  N.  stephensi  most  likely  will  not  be  found  if  piiions  and 
junipers  are  absent.  This  wood  rat  is  frequently  found  associated  with  the 
piiion  mouse,  Peromyscus  truei,  the  brush  mouse,  Peromyscus  boylii,  or  the 
cactus  mouse,  Peromyscus  eremicus. 

Within  Grand  Canyon  National  Park,  Neotoma  stephensi  is  to  be  found  in 
several  ecological  situations.  In  the  majority  of  places,  N.  stephensi  was  found 
in  rocky  situations  where  there  were  piiion,  juniper,  scrub  oak  and  cliffrose. 
In  these  situations,  it  was  usually  associated  with  Neotoma  mexicana,  but  in 


62 


Nov.,  1960  HOFFMEISTER  AND  DE  LA  TORRE— NEOTOMA  483 

a  few  cases,  with  IV.  alhigula.  In  Long  Jim  Canyon,  N.  stephensi  was  in  a 
rocky  place  within  the  yellow  pine  forest.  At  Cedar  Mountain,  the  species 
was  at  the  lowest  edge  of  the  pinon-juniper  belt.  Here,  on  the  rocky,  desert 
slopes,  there  were  many  cacti  and  agave  plants  and  only  a  few  straggling 
piiions  or  junipers.  N.  stephensi  widely  overlapped  the  range  of  N.  albigula 
here.  At  Hilltop,  near  the  western  boundary  of  the  Park,  N.  stephensi  was 
in  rocky  places  decidedly  below  the  piiion-juniper  zone  and  in  an  area 
where  there  were  sagebrush,  Indian  paintbrush  and  grasses.  Here,  Perog- 
nathus  intermedins,  Neotoma  albigula,  Eutamias  dorsalis,  and  even  Pero- 
myscus  truei  and  P.  hoylii  were  present. 

In  the  vicinity  of  Rimrock  and  Montezuma  Well  in  eastern  Yavapai  County, 
Arizona,  N.  stephensi  was  found  along  the  fractured  limestone  outcrop 
extending  horizontally  near  the  top  of  the  low  mesas.  This  outcrop  was  5  to 
8  feet  in  height  and  was  fractured  along  its  length  into  large  blocks.  N. 
stephensi  occurred  in  the  crevices  among  these  blocks,  along  with  many 
Peromyscus  eremicus.  Rat  houses  and  piles  of  droppings  were  evident  all 
through  the  outcrop.  About  40  feet  below  the  limestone  stratum  there  oc- 
curred a  short  dark  lava  outcrop  which  was  much  more  finely  fractmred. 
Neotoma  albigula  was  found  here  as  well  as  on  the  valley  floor  where  it 
lived  among  the  cacti.  No  N.  albigula  was  taken  among  the  blocks  of  lime- 
stone where  N.  stephensi  occurred.  These  field  observations  made  by  John  S. 
Hall  suggest  an  important  difference  in  the  habitat  preference  of  N.  stephensi 
and  N.  albigula,  even  in  areas  where  these  two  species  are  very  near  to 
each  other. 

At  the  western  edge  of  the  range  of  Neotoma  stephensi,  in  the  Hualpai 
Moimtains,  it  may  also  occur  above  the  pinon-juniper  zone  in  the  scrub  oak 
and  yellow  pine.  However,  it  was  taken  in  rocky  situations  and  in  association 
with  Peromyscus  boylii. 

Occasionally,  N.  stephensi  will  desert  its  preferred  rocky  habitat  and  move 
into  or  under  man-made  structures.  At  Pasture  Wash,  a  female  with  half- 
grown  young  was  living  among  bales  of  hay  in  the  loft  of  an  unused  bam. 
Near  McMillen  Mine,  individuals  had  homes  under  large  sheets  of  building 
material  which  had  been  on  the  ground  for  a  long  period  of  time. 

In  New  Mexico,  according  to  Bailey  (N.  Amer.  Faima  53:  188,  1931), 
N.  stephensi  in  the  Burro  Mountains  live  in  "stick  nests  placed  about  logs  or 
brush,  and  in  places  their  burrows  entered  the  ground  about  the  bases  of 
rocks  with  many  sticks  piled  about  the  entrances."  Bailey  stated  that  they 
occupy  the  juniper-piiion  plateau  region,  frequenting  rocky  places  and  even 
cliffs. 

Neotoma  stephensi  Goldman 

Range. — Central  Arizona,  from  Hualpai  Mountains  on  the  west  to  western 
New  Mexico  on  the  east,  and  from  McMillenville  on  the  south  to  extreme 
south-central  Utah  (Navajo  Mountain)  on  the  north  (Fig.  4). 


63 


484 


JOURNAL  OF  MAMMALOGY 


Vol.  41,  No.  4 


Diagnosis. — A  medium-sized  species  of  Neotoma  with  a  bushy  tail  (bushier 
than  in  any  other  species  except  IV.  cinerea);  dusky  coloration  on  dorsal  sur- 
face of  foot  extending  from  ankle  nearly  one-third  distance  to  base  of  toes; 
small  baculum,  exclamation-mark-shaped  (Fig.  1);  upper  molariform  teeth 
with  following  combination  of  characters:  M^  with  antero-medial  fold  absent 
or  poorly  developed,  and  M^  with  postero-labial  fold  and  second  loph  directed 
obliquely  (Figs.  1,  2);  last  lower  molar  with  deep  lingual  fold  as  deep  or 
deeper  than  labial  fold  (Fig.  2);  skull  broad  and  flat  interorbitally;  rostrum 
narrow;  nasals  truncate  posteriorly  (Fig.  3). 

Neotoma  stephensi  stephensi  Goldman 

Neotoma  stephensi  Goldman,  1905,  Proc.  Biol.  Soc.  Wash.,  18:  32,  2  Feb. 
Neotoma  lepida  stephensi,  Goldman,  1910,  N.  Amer.  Fauna  31:  80,  19  Oct. 
Neotoma  stephensi  stephensi,  Goldman,  1932,  Jour.  Mamm.,  13:  66,  9  Feb. 


Fig.  4. — Distribution  of  the  subspecies  of  Neotoma  stephensi. 


64 


Nov.,  1960  HOFFMEISTER  AND  DE  LA  TORRE— NEOTOMA  485 

Type.— Adult  female,  U.S.  National  Museum  (Biol.  Surv.),  No.  117466, 
from  Hualpai  Mountains,  6,300  ft.,  actually  at  Horse  Tank  (see  Remarks), 
Mohave  County,  Arizona,  collected  on  1  July  1902  by  Frank  Stephens;  original 
no.  4192. 

Range. — From  the  Hualpai,  Chemehuevis,  and  Harquahala  mountains  in 
western  Arizona  east  along  the  MogoUon  Plateau  to  the  Burro  and  Gallinas 
mountains  in  southwestern  New  Mexico  (see  map,  Fig.  4). 

Diagnosis. — A  race  showing  considerable  variation  throughout  its  range 
but  possessing  the  following  characteristics:  color  of  dorsum  dark,  being 
darkest  in  central  Arizona  and  southwestern  New  Mexico  (Plate  I);  sides 
above  lateral  line  with  narrow  fulvous  band  near  Pinkish  Buff;  nose,  fore- 
head and  cheeks  grayish  or  plumbeous;  hair  of  throat  usually  plumbeous 
basally;  top  of  tail  appears  dark,  almost  black,  because  more  black  hairs  and 
few  or  no  white  hairs  interspersed  or  show  through;  size  large,  as  indicated 
by  weight  in  adult  males  of  usually  more  than  180  grams;  skull  large,  usually 
averaging  more  in  greatest  length  than  41.2  mm.  in  adult  males;  upper  tooth- 
row  long,  usually  8.4  mm.  or  more;  skull  with  supraorbital  ridges  frequently 
beaded  and  heavy. 

Comparisons. — Since  there  is  considerable  variation  within  the  subspecies 
stephensi,  groups  of  populations  of  this  race  have  been  compared  with  the 
relatively  homogeneous  "population"  of  relicta. 

From  relicta,  the  race  stephensi  from  the  Hualpai  Mountains,  Hackberry, 
Harquahala  Mountains,  and  Grand  Canyon  National  Park  differs  as  follows: 
darker  coloration  (but  less  different  than  in  other  populations  of  stephensi); 
more  grayish  nose,  forehead  and  cheeks;  not  "white-throated"  except  for 
specimens  from  HiUtop;  markedly  heavier  in  weight;  broader  skull,  both 
actually  and  relatively  to  its  length  (especially  marked  in  specimens  from 
the  Hualpai  Mountains);  longer  toothrow  and  broader  interorbitally  (es- 
pecially in  specimens  from  the  Hualpais). 

Central  Arizona  populations  (for  discussion,  see  under  Remarks)  differ 
from  N.  s.  relicta  as  follows:  color  markedly  darker,  both  on  the  dorsum  and 
sides;  dorsal  tail  stripe  more  blackish,  less  gray;  body-weight,  length  of  tooth- 
row,  and  interorbital  width  greater,  but  not  so  pronounced  as  in  topotypes  of 
stephensi  from  the  Hualpai  Mountains;  differ  from  relicta  in  other  features 
the  same  way  as  do  topotypes  of  stephensi. 

Populations  from  eastern  Arizona  and  southwestern  New  Mexico  differ 
from  N.  s.  relicta  as  follows  (for  discussion,  see  under  Remarks) :  color  darker, 
including  facial  region,  sides  and  tail;  throat  tending  to  be  partially  or  entirely 
white  (in  the  latter  case  showing  similarity  to  relicta);  externally  larger  and 
heavier;  skull  with  nasals  broad,  tending  to  be  bell-shaped  anteriorly,  but 
constricted  posteriorly;  ascending  arms  of  premaxillaries  broader;  differ  from 
relicta  in  other  features  as  do  topotypes  of  stephensi. 

Measurements. — See  Tables  2  and  3. 

Remarks. — As  mentioned  under  Comparisons,  there  is  considerable  varia- 


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JOURNAL  OF  MAMMALOGY 


Vol  41,  No.  4 


Table  2. — External  and  cranial  measurements  of  "Group  3"  male  specimens  of  Neotoma 
stephensi  stephensi.  Grouped  localities  are  as  follows:  Western  Arizona  (Hackberry, 
Hualpai  Mts.,  Lucky  Star  Mine);  Northern  Arizona  (Grand  Canyon);  Central  Arizona 
(Red  Lake,  Wupatki  area);  Southeastern  Arizona  (McMillenville  area,  Nantanes  Plateau, 
Black  River);  Western  New  Mexico  (Burley,  Burro  Mts.,  Glenwood) 


Western 

Northern 

Central 

Southeastern 

Western 

Arizona 

Arizona 

Arizona 

Arizona 

New  Mexico 

Number   

8 

4 

6 

3 

4 

Total   length   

301.2 

311.2 

314.0* 

308.3 

298.3* 

283.0-334.0 

305.0-320.0 

303.0-320.0 

302.0-313.0 

290.0-310.0 

Head  and  body  

173.6 

175.8 

183.2* 

174.0 

169.5" 

161.0-201.0 

172.0-178.0 

171.0-203.0 

165.0-182.0 

165.0-177.0 

TaU    

127.6 

135.0 

132.7* 

134.3 

127.3" 

120.0-135.0 

127.0-144.0 

125.0-138.0 

131.0-137.0 

120.0-133.0 

Hind    foot    .— 

32.3 

31.5 

32.7 

31.7 

31.6 

31.0-34.0 

29.0-34.0 

32.0-34.0 

31.0-32.0 

30.0-33.0 

Condylobasal  length. 

39.5' 

39.7 

40.0 

38.6 

37.3 

37.6-41.5 

39.3-40.1 

37.7-42.5 

37.7-39.3 

36.5-39.2 

Zygomatic  breadth ... 

22.r 

21.2 

21.3" 

20.4" 

21.0-23.0 

20.6-21.8 

20.6-21.9 

21.0^ 

20.^-20.8 

Interorbital  

5.7 

5.4 

5.5 

5.5 

5.3 

5.6-6.0 

5.1-5.7 

5.3-6.0 

5.4-5.6 

5.0-5.6 

Breadth  of  rostnmi  . 

6.5 

6.4 

6.1 

6.5 

6.1 

5.9-6.9 

6.3-6.5 

5.9-6.4 

6.2-7.0 

5.6-6.5 

Depth  of  rostrum  ... 

6.8 

6.9 

6.8 

6.7 

6.3 

6.5-7.0 

6.8-7.1 

6.5-7.1 

6.4-7.1 

6.1-6.5 

Nasal    

15.5 

16.0 

16.3 

16.0 

15.1 

15.0-16.2 

15.4-16.8 

15.7-17.5 

15.8-16.3 

14.1-16.8 

Incisive  foramen  

9.1 

9.0 

9.5 

8.7 

8.4 

8.8-9.5 

8.8-9.4 

9.0-10.2 

8.2-9.2 

8.0-9.0 

Palatal  bridge 

7.6 

7.5 

7.5 

8.1 

7,7 

7.4-7.9 

7.3-7.6 

7.0-7.7 

7.9-8.4 

7.5-7.9 

Maxillary  toothrow  . 

8.7 

8.3 

8.5 

8.9 

8.6 

8.3-9.3 

8.1-8.6 

7.9-9.0 

8.7-9.2 

8.4-8.8 

tion  within  the  subspecies  N.  s.  stephensi  as  here  delimited.  This  variation 
can  be  discussed  by  grouping  the  populations  into  three  segments,  from  (1) 
the  Hualpai  Mountains,  including  others  from  western  Arizona  and  the  Grand 
Canyon  region,  (2)  central  Arizona,  and  (3)  eastern  Arizona  and  western 
New  Mexico.  We  prefer  to  describe  these  three  "variants"  but  not  to  give 
them  names. 

The  first  group  of  populations  in  western  Arizona  possesses  the  following 
characteristics:  hght  color  (see  Plate  I);  long  toothrow,  broad  across  zygo- 
matic arches,  broad  interorbitally,  yet  skull  is  only  of  average  length;  large 
foot,  average  length  of  body,  and  short  tail.  Within  this  group  of  populations, 
those  specimens  from  the  type  locahty  (Hualpai  Mountains)  have  certain 
unique  features  such  as  relatively  short  but  broad  skulls,  long  toothrows,  broad 
interorbital  regions,  greater  weight,  and  slightly  paler  than  "average"  colora- 
tion for  the  subspecies.  If  only  topotypes  are  used  for  comparison  with  other 


66 


Nov.,  1960 


HOFFMEISTER  AND  DE  LA  TORRE— NEOTOMA 


487 


populations  of  N.  stephensi,  the  impression  may  be  gained  that  the  population 
is  quite  distinct.  However,  when  the  range  of  variation  in  all  characters  from 
throughout  the  geographic  range  of  stephensi  is  taken  into  consideration, 
the  differences  are  less  impressive  and  not  as  significant.  In  many  features, 
topotypes  of  stephensi  are  not  "typical"  or  "average"  for  the  race. 

In  central  Arizona,  there  is  a  series  of  populations  of  N.  stephensi  which 
possesses  characteristics  of  an  average  difference  distinguishing  it  from  neigh- 
boring populations.  This  series,  depicted  by  the  dark  area  in  Plate  I,  com- 
prises populations  from  Black  Tank  to  the  north,  south  through  Deadman's 
Flat,  Wupatki  Monument,  Winona,  Walnut,  Verde  Valley,  and  west  to  Red 
Lake  and  Fort  Whipple.  Specimens  from  as  far  south  as  McMillenville  and 
the  Natanes  Plateau  in  Gila  County  are  not  included.  This  complex  of  popula- 
tions possesses  the  following  features,  many  of  which  are  of  an  average  sort: 
color  dark;  dorsal  tail  stripe  often  black;  sides  with  the  ochraceous  color  along 
the  lateral  line  greatly  restricted;  body  long,  as  long  or  longer,  on  the  average, 
than  in  any  population;  body  weight  intermediate  between  that  of  relicta  and 


Table  3. — External  aand  cranial  measurements  of  "Group  3"  female  specimens  of  Neotoma 
stephensi  stephensi.  Grouped  localities  are  as  in  Table  2 


Western 

Northern 

Central 

Southeastern 

Arizona 

Arizona 

Arizona 

Arizona 

Number         

12 

5 

5 

3 

Total  length  

274.2 

298.3'^ 

309.8^ 

264.0-329.0 

279.0-323.0 

293.0-322.0 

304.0^ 

Head  and  body  

170.1 

168.3" 

175.0* 

148.0-195.0 

160.0-180.0 

173.0-179.0 

164.0^ 

Tail    

129.0 

130.0" 

134.8^ 

106.0-141.0 

119.0-143.0 

118.0-148.0 

140.0^ 

Hind  foot  

32.0 

31.3« 

33.3* 

30.0-34.0 

30.0-32.0 

33.0-34.0 

32.5^ 

Condylobasal  length  -. 

38.8" 

36.6 

38.6 

38.8^ 

36.8-40.7 

35.9-37.5 

38.0-39.7 

38.2,39.3 

Zygomatic  breadth  .... 

21.8' 

20.7 

20.7 

21.6 

21.1-23.2 

20.4-20.9 

20.5-20.9 

21.2-22.0 

Interorbital  

5.4 

5.4 

5.4 

5.7 

4.7-5.8 

5.2-5.7 

5.0-5.7 

5.3-6.0 

Rostrum  breadth  _ 

6.3 

5.9 

6.3 

6.4^ 

6.0-6.6 

5.6-6.0 

6.1-6.5 

6.3,6.5 

Rostrum  depth  

6.6 

6.1 

6.5 

6.7^ 

6.2-7.0 

5.5-6.2 

6.4-6.7 

6.5,6.8 

Nasal 

15.3 

14.3 

15.7 

15.5= 

13.9-16.6 

13.7-14.6 

15.3-16.3 

14.9,16.1 

Incisive  foramen  

8.5 
7.9-8.8 

8.4 
8.1-8.8 

9.1 
8.5-9.5 

8.7= 

8.5,8.9 

Palatal  bridge  

7.6 

7.2 

7.2 

7.8 

6.9-8.5 

6.9-7.9 

6.5-7.5 

7.5-8.5 

Maxillary  toothrow   ... 

8.9 

8.4 

8.6 

9.0 

8.4-9.5 

8.1-8.8 

8.5-8.8 

8.6-9.3 

67 


488  JOURNAL  OF  MAMMALOGY  Vol.  41,  No.  4 

Specimens  from  the  Hualpai  Mountains;  skull  long  and  narrow,  with  the  per- 
centage of  zygomatic  breadth  to  greatest  length  in  adult  males  being  between 
48.4  and  50.4;  for  the  Hualpais,  51.7  to  53.6;  for  the  Grand  Canyon,  49.7  to 
51.4;  similar  percentages  for  adult  females  from  the  respective  localities  are 
between  49.2  and  53.8;  50.8  to  54.8;  51.6  to  53.5.  The  length  of  the  upper 
toothrow  and  width  of  the  interorbital  region  are  intermediate  between 
relicta  and  specimens  from  the  Hualpai  Mountains. 

Although  this  complex  of  populations  may  possess  some  average  differences 
of  color  and  size,  we  feel  that  it  has  not  reached  the  subspecific  stage  of 
differentiation. 

In  western  New  Mexico  and  eastern  Arizona,  there  is  a  group  of  populations 
that  has  certain  characters  in  common,  and  differs  in  an  average  way  from 
N.  s.  stephensi  in  western  Arizona.  This  group  includes  localities  from  25  mi. 
N  Springerville  and  from  Springerville  in  Arizona  southeast  to  the  Burro 
Mountains,  New  Mexico,  and  northeast  to  Grants.  Some  features  of  this 
group,  many  of  which  are  not  diagnostic,  include:  nasals  broad,  almost  bell- 
shaped  anteriorly;  posterior  arms  (ascending  branches)  of  premaxillae  on 
dorsum  of  skull  broad;  nasals,  posteriorly,  constricted  more  by  premaxillae 
than  in  most  other  populations;  color  dark,  as  dark  as  that  in  central  Arizona 
populations  except  for  specimens  from  Burley.  For  remarks  about  the  white- 
throatedness  of  specimens  from  the  Burro  Mountains,  see  page  480.  One 
specimen  from  Grants,  Catron  County,  New  Mexico,  in  many  ways  exemplifies 
the  extreme  of  these  characters  listed:  nasals  bell-shaped  anteriorly,  con- 
stricted posteriorly;  posterior,  ascending  arms  of  premaxillae  broad;  inter- 
orbital region  broad;  color  dark,  with  the  addition  of  a  heavy,  rich  fulvous 
wash  over  the  entire  underparts.  This  specimen  lacks  90  per  cent  of  the  tail, 
and  our  first  reaction  was  that  this  specimen  was  not  a  bushy-tailed  Neotoma 
stephensi.  The  heavy  wash  of  fulvous  on  the  underparts  is  duplicated  in  one 
of  three  specimens  of  Neotoma  mexicana  from  5  mi.  SE  Grants.  However, 
careful  analysis,  particularly  of  cranial  features,  indicates  that  the  specimen 
is  N.  stephensi,  not  N.  mexicana.  This  individual  is  either  aberrant  or  reflects 
the  extreme  characters  of  this  group  of  populations  we  have  described  above. 
We  prefer  the  latter  interpretation.  The  fulvous  wash  on  the  underparts  may 
reflect  the  "influence"  of  the  black  lava  near  Grants.  We  do  not  think  this 
fulvous  wash  represents  a  "dichromatic  condition"  that  Goldman  (N.  Amer. 
Fauna  31:  81,  1910)  alluded  to,  although  more  specimens  may  indicate  that 
such  is  the  case.  A  specimen  from  4  mi.  W  McCartys,  which  is  near  Grants,  is 
a  very  young  animal  and  shows  none  of  the  features  of  the  Grants'  specimen. 

According  to  Laurence  Huey,  the  type  locality  should  be  regarded  as  Horse 
Tank  at  the  southern  end  of  the  Hualpai  Mountains.  Mr.  Huey  informs  us 
that  Frank  Stephens  provided  him  with  this  information. 

Specimens  examined. — Total  number,  163,  from  the  following  localities:  Arizona — 
Mohave  County:  Hackberry,  7  (BS);  Democrat  Mine,  13  mi.  ESE  Kingman,  Hualpai  Mts., 
1  (UI);  Hualpai  Mtn.  Park,  Hualpai  Mts.,  1  (UI);  1  mi.  N  Hualpai  Peak,  Hualpai  Mtn. 


68 


Not;.,  1960  HOFFMEISTER  AND  DE  LA  TORRE— NEOTOMA  489 

Park,  7,000  ft.,  1  (UI);  Pine  Lake,  Hualpai  Mtn.  Park,  6,000  ft,  1  (UI);  Hualpai  Mts., 
5,600  ft.,  7,000  ft.,  6  (BS),  1  (UI);  Horse  Tank,  5  (SD);  Lucky  Star  Mine,  Chemehuevis 
Mts.,  3  (SD);  Yuma  County:  Harquahala  Mts.,  5,000  ft.,  3  (BS);  Coconino  County:  Hilltop, 
S  side  GCNP  [=  Grand  Canyon  Nat.  Park],  4  (UI);  Lower  end  Prospect  Valley,  5,200  ft., 
2  (BS);  Pasture  Wash  Ranger  Station,  6,300  ft.,  GCNP,  3  (UI);  Pasture  Wash,  Jet.  rds. 
W9A  &  W9,  GCNP,  1  (UI);  8  mi.  N  Pine  Spg.,  Hualpai  Indian  Reservation,  3  (BS); 
E  side  Cedar  Mt..  6,400  ft.,  GCNP,  2  (UI);  Yaki  Bum,  S  rim  Grand  Canyon,  2  (GC); 
Yavapai  Point  Station,  S  rim  Grand  Canyon,  3  ( GC ) ;  Grand  Canyon  Village,  S  rim  Grand 
Canyon,  1  (GC);  S  rim  Grand  Canyon,  1  (GC);  S  boundary  GCNP,  nr.  Rowes  Well, 
GCNP,  1  (UI);  School  athletic  grounds.  Village,  GCNP,  7  (UI);  Shoshone  Point,  GCNP, 

2  (UI);  Wayside  Museum,  S  rim  Grand  Canyon,  1  (GC);  1  mi.  E,  V2  mi.  S  Desert  View 
Pt,  GCNP,  1  (UI);  Grandview  Pt.,  GCNP,  1  (UI);  Long  Jim  Canyon,  3  (UI);  W  side 
Zuni  Pt.,  7,200  ft.,  GCNP,  6  (UI);  Rt.  64,  SE  Boundary  GCNP,  1  (UI);  Cataract  Canyon, 
12  mi.  WSW  Anita,  2  (BS);  Red  Butte,  2  (BS);  Black  Tank  Lava  Beds,  6,100  ft,  3  (UC); 
Lava  Field,  12  mi.  N  Deadman's  Flat,  NE  San  Francisco  Mt.,  1  (UC);  2.6  mi.  W  Wupatki 
Ruins,  8  (UC);  Wupatki  Indian  Ruins,  35  mi.  NE  Flagstaff,  5,100  ft,  1  (BS),  6  (UC); 
Deadman's  Flat,  NE  San  Francisco  Mt.,  6,400  ft.,  2  (UC);  4  mi.  NE  Deadman  Ranger 
Station,  San  Francisco  Mt,  6,600  ft.,  1  (BS);  Red  Lake,  5  (BS);  3  mi.  NW  Winona, 
6,200  ft.,  6,400  ft,  2  (BS);  Aztec  Tank,  5,800  ft.,  2  (BS);  Winona,  6,400  ft,  2  (UC); 
Wahiut,  1  (BS);  Wabut  Canyon,  5  mi.  S  Mt.  Elden,  6,500  ft.,  1  (BS);  Anderson  Mesa, 
Anderson  Canyon,  30  mi.  SE  Flagstaff,  6,500  ft.,  1  (BS);  Yavapai  County:  Pine  Flat, 
Jumper  Mts.,  20  mi.  NW  Simmons,  3  (BS);  5  mi.  S,  1  mi.  W  Sedona,  1  (UI);  2  mi.  N 
Montezimia  WeU,  3  (UI);  2  mi.  N  Rimrock,  1  (UI);  Montezuma  WeU,  3,500  ft.,  2  (BS); 

3  mi.  N  Ft  Whipple,  1  (BS);  6  mi.  NW  Camp  Verde,  1  (UI);  Mayer,  1  (BS);  Gila 
County:  7  mi.  N  Payson,  4,500  ft.,  1  (BS);  Black  River,  5  mi.  above  mouth  White  River, 
4,600  ft.,  1  (BS);  nr.  sawmill,  25  mi.  NE  Rice  [nov/  San  Carlos],  Natanes  Plateau,  5,800  ft., 
3  (BS);  McMillen  Mine,  5  mi.  E,  12y2  mi.  N  Globe,  4  (UI);  Cazador  Spring,  S  base 
Natanes  Plateau,  San  Carlos  Indian  Reservation,  4,000  ft.,  1  (BS);  McMillenville,  4,300  ft., 
3  (BS);  Apache  County:  Zuni  River,  3  (BS);  8  mi.  S  St  Johns,  5,800  ft,  4  (BS);  25  mi. 
N  Springerville,  2  (BS);  Springerville,  7,000  ft.,  1  (BS);  Greenlee  County:  3  mi.  W  Gosper 
Ranch,  6,000  ft,  1  (BS);  Gosper  Ranch,  Blue  River,  5,000  ft,  2  (BS);  New  Mexico— 
Valencia  County:  Grants,  1  (BS);  4  mi.  W  McCartys,  1  (UM);  Socorro  County:  Burley 
[22  mi.  N  Augustine],  3  (BS);  Catron  County:  Largo  Canyon,  1  (UC);  Whitewater 
Canyon,  5  mi.  NE  Glenwood,  5,450  ft.,  1  (AM);  Glenwood,  San  Francisco  Valley,  5,000 
ft,  1  (BS);  Grant  County:    Burro  Mts.,  8  (BS). 

Additional  records. — Arizona — Coconino  County:  S  side  Bass  Camp,  8  mi.  NW  Grand 
Canyon  (BS);  1  mi.  N  Bass  Camp,  5,200  ft,  (BS);  3  mi.  S  Bass  Camp,  5,400  ft,  (BS); 
Bass  Camp  (BS);  nr.  Bright  Angel  Trail,  Grand  Canyon,  (BS);  S  Yaki  Point,  in  yellow 
pine,  Grand  Canyon  (BS);  top  of  rim  nr.  Village,  Grand  Canyon,  6,800  ft.,  (BS);  Grand 
View  Point,  Grand  Canyon,  (BS);  Trash  Tank,  S  rim  Grand  Canyon,  (GC);  Trash  Wash, 
S  rim  Grand  Canyon,  ( GC ) ;  N  Red  Butte,  Main  Road,  Grand  Canyon,  ( BS ) ;  Red  Butte, 
Museum  of  Northern  Arizona;  Wupatki  Nat'l  Monument,  5,100  ft.,  Museum  of  Northern 
Arizona;  Wupatki  Indian  Ruins,  35  mi.  NE  Flagstaff,  5,100  ft,  (BS);  Yavapai  County: 
Fools  Gulch,  Weaver  Mts.,  (BS). 

Neotoma  stephensi  relicta  Goldman 
Neotoma  stephensi  relicta  Goldman,  1932,  Jour.  Mamm.,  13:  66,  9  Feb. 

Type.— Adult  female,  U.S.  National  Museum  (Biol.  Surv.),  No.  67780,  from 
Keams  Canyon,  Navajo  County,  Arizona,  collected  on  22  July  1894  by  A.  K. 
Fisher;  original  no.  1649. 


69 


490 


JOURNAL  OF  MAMMALOGY 


Vol.  41,  No.  4 


Table  4. — External  and  cranial  measurements  of  "Group  3"  specimens  of  Neotoma 
stephensi  relicta.  Localities  represented  are  as  follows:  Utah — Navajo  Mt.,  Rainbow 
Bridge;  Arizona — Rainbow  Lodge,  Cedar  Ridge,  Keams  Canyon;  New  Mexico — Wingate 

area,  Long  Canyon,  Blanco 


Females 


Males 


Number 

Total  length 

Head  and  body 

Tail  

Hind  foot 

Condylobasal  length 

Zygomatic  breadth  ... 

Interorbital 

Breadth  of  rostrum  . 

Depth  of  rostrum  . 

Nasal 


Incisive  foramen  

Palatal  bridge   

Maxillary  toothrow  


10 

296.7' 
273.O-320.0 

163.0" 
153.0-175.0 

133.7" 
120.0-145.0 

30.4" 
28.0-33.5 

36.3« 
33.7-38.0 
20.0« 
18.4-20.2 

5.2 
4.8-5.7 
5.9 
5.5-6.3 
6.2 
5.8-6.5 
14.7' 
13.5-15.8 

8.4 

7.8-9.0 

7.2 

6.7-7.8 

8.1 

7.7-8.3 


10 
304.7" 
283.0-333.0 

172.0" 
159.0-187.0 

130.9 
123.0-144.0 
31.2 
29.0-33.0 
37.8« 
36.8-38.6 
20.5" 
20.0-21.1 
5.3" 
5.2-5.4 
6.0" 
5.5-eA 
6.6 
6.4-7.0 
15.4 
14.9-16.0 
8.8 
8.5-9.4 
7.4 
7.1-7.9 
8.2 
7.9-8.4 


Range. — East  of  the  Colorado  River,  from  Navajo  Mountain  in  extreme 
south-central  Utah,  south  to  the  Little  Colorado  River,  and  eastward  in  New 
Mexico  to  the  San  Juan  Basin  at  the  north  and  the  Zimi  Mountains  at  the 
south  (see  map,  Fig.  4). 

Diagnosis. — A  race  of  Neotoma  stephensi  characterized  by  markedly  pale 
buffy  color,  with  much  less  blackish  and  brownish  than  in  other  populations 
of  species;  sides,  above  lateral  line,  with  large  extent  of  buffy  color,  which 
varies  between  Pinkish  Buff  and  Light  Ochraceous-Salmon;  nose,  forehead 
and  cheeks  buffy,  less  plumbeous  tiian  other  subspecies;  hairs  on  throat 
usually  white  throughout  (base  not  plumbeous);  top  of  tail  appears  grayish 
because  few  dark  hairs  present;  underparts  usually  without  fulvous  wash; 
size  small,  being  best  indicated  by  Hght  weight  (adult  males  less  than  117 
gms.);  skull  small,  greatest  length  averaging  less  than  41.2  mm.  in  adult  males; 
upper  toothrow  short,  usually  less  than  8.4  mm.;  skull  narrow,  with  interorbital 
width  usually  5.3  mm.  or  less  and  narrow  across  zygomata,  with  males  usually 


70 


Nov.,  1960  HOFFMEISTER  AND  DE  LA  TORRE— NEOTOMA  491 

averaging  less  than  21.0  mm.;  skull  delicate  for  the  species,  with  supraorbital 
ridges  not  heavily  beaded. 

Comparisons. — For  a  comparison  with  N.  stephensi  stephensi,  and  the  geo- 
graphic variants  within  that  subspecies,  see  the  account  of  N.  s.  stephensi. 

Measurements. — See  Table  4. 

Remarks. — N.  s.  relicta  is  a  pale  race  inhabiting  the  mountainous  areas  of 
the  elevated,  short  grass  region  of  northeastern  Arizona.  The  race  does  extend 
into  New  Mexico  and  Utah,  but  its  principal  center  of  distribution  is  in 
Arizona. 

N.  s.  relicta  is  quite  distinctive  from  many  populations  of  N.  s.  stephensi 
adjacent  to  its  range.  It  is  less  distinctive  from  some  other  populations  farther 
removed.  However,  with  a  combination  of  characters  (principally  on  the 
basis  of  color),  relicta  and  stephensi  can  be  distinguished.  As  here  delimited, 
relicta  shows  less  morphological  variation  geographically  than  does  stephensi. 
Specimens  from  the  eastern  part  of  Grand  Canyon  National  Park,  referred  to 
stephensi,  show  considerable  approach  toward  specimens  from  Cedar  Ridge, 
referred  to  relicta.  These  two  localities  are  less  than  45  miles  apart.  The 
intermediacy  is  in  color  and,  to  some  extent,  size  of  the  skull.  Specimens 
from  Wingate  and  Gallup  are  of  a  color  intermediate  between  that  of  relicta 
and  stephensi,  but  the  skulls  of  the  adult  specimens  seem  more  as  in  relicta, 
to  which  subspecies  they  are  referred. 

Specimens  examined. — Total  number,  62,  from  the  following  localities:  Utah — San 
Juan  County:  Rainbow  Bridge,  4,000  ft.,  1  (UC);  nr.  War  God  Spring,  8,500  ft.,  Navajo 
Mt,  1  (AM);  Navajo  Mt.  Trading  Post,  SE  side  Navajo  Mt.,  1  (UC);  Arizona — Coconino 
County:  Rainbow  Lodge,  Navajo  Mts.,  6,400  ft.,  2  (BS);  5  mi.  S  simmiit,  Navajo  Mt.,  1 
(UC);  Cedar  Ridge,  30  mi.  N  Tuba,  3  (BS);  Cedar  Ridge,  6,000  ft.,  10  (UC);  Tuba, 
1  (BS);  Navajo  County:  Long  Canyon,  6,450  ft.,  1  (AM);  Keams  Canyon,  80  mi.  N 
Holbrook,  20  (BS);  Keams  Canyon,  6,200  ft.,  6  (UC);  Apache  County:  Ganado,  6,500  ft., 
5  (BS);  St.  Michaels,  7,000  ft.,  2  (BS);  New  Mexico— Sen  Juan  County:  Blanco,  1  (BS); 
McKinley  County:  Gallup,  1  (BS);  Wingate,  2  (BS);  Fort  Wingate,  3  (BS);  12  mi.  S 
Gallup,  1   (BS). 

Museum  of  Natural  History,  Univ.  of  Illinois,  Urbana.    Received  18  August  1959. 


71 


Am.  Zoologist,  7:223-232(1967). 

Multiple  Character  Analysis  of  Canis  lupus,  latrans,  and  familiaris, 
With  a  Discussion  of  the  Relationships  of  Canis  niger 

Barbara  Lawrence,  Museum  of  Comparative  Zoology,  Harvard  University, 

and 
William  H.  Bossert,  Department  of  Biology,  Harvard  University, 

Cambridge,  Mass. 

Synopsis.  A  multiple  character  analysis  was  undertaken  of  a  broadly  representative  sample 
of  three  species:  Canis  lupus  (wolf),  C.  latrans  (coyote),  and  C.  familiaris  (dog).  These  species 
are  clearly  and  significantly  distinguished  by  the  technique  of  linear  discrimination.  The  analy- 
sis provides  a  basis  for  the  identification  of  skulls  not  obviously  distinguishable  by  size  or  other 
diagnostic  charactei^s. 

Early  populations  of  Canis  n.  niger  and  C.  n.  gregoryi  (red  wolf)  are  compared  with  the  three 
species  above  and  are  found  to  form  a  cluster  with  lupus  and  to  be  sharply  distinct  from  the 
other  two  species.  Additional  comparisons  show  that  while  lupus  lycaon  and  niger  both  overlap 
with  lupus,  they  are  distinct  from  each  other.  This  entire  cluster  is  quite  distinct  from  latrans, 
with  niger  being  the  farthest  removed.  A  sample  population  of  C.  ?!.  gregoryi,  from  the  edge  of 
the  extending  range  of  C.  latrans,  was  examined  and  found  to  show  too  great  a  range  of  vari- 
ation to  be  attributed  to  a  single  species. 

With  the  advent  of  white  man  in  North  a  unit.  When  a  particular  subspecies  is  re- 
America  and  his  consequent  modification  ferred  to,  a  trinomial  is  used,  as  Canis  lu- 
of  the  environment  by  lumbering  and  pus  lycaon.  Canis  niger,  the  red  wolf,  is 
clearing  for  farming,  coyotes  have  been  ex-  usually  considered  to  include  three  sub- 
tending their  range  (Young  and  Jackson,  species.  Their  status  is  uncertain,  and  Ca- 
1951).  As  they  have  extended  their  range,  7us  niger  as  used  in  the  present  work  refers 
on  the  fringes  of  their  newly  acquired  ter-  to  the  typical  form,  C.  n.  niger,  and  to  those 
ritories,  animals  which  are  difficult  to  iden-  southeastern  populations,  presently  called 
tify  have  frequently  been  captured.  In  the  C.  n.  gregoryi,  which  show  no  evidence  of 
South,  as  often  as  not,  these  are  called  red  hybridization  and  which  were  collected 
wolves,  in  the  Northeast,  coydogs.  In  both  from  well  outside  the  range  of  latrans.  Ca- 
parts  of  the  country  these  animals  occur  nis  familiaris,  the  dog,  presents  no  prob- 
where  coyotes  have  moved  into  areas  that  lem  because,  in  spite  of  its  variability,  it  is 
formerly  were  inhabited  by  small  races  of  monotypic. 

wolf.    Coincident  also  with  these  shifts  in  The   present  study  was  undertaken   be- 

distribution  has  been  an  upward  revision  cause    attempts    to    identify   skulls    of   the 

in  the  reported  weights  for  coyotes.   Young  northeastern   population    of   rather   large- 

and  Jackson  (1951),  eliminating  a  few  out-  sized  members  of  the  genus  Canis  bogged 

sized    individuals,    give    a    range    of    18-30  down  in  a  mass  of  overlapping  characters, 

pounds  for  typical  western  coyotes,  while  It  was  then  decided  that  before  such  fringe 

Burt   (1946)  gives  a  range  of  23-50  pounds  populations  could  be  identified  we  needed 

for  Michigan  coyotes.    The  latter  overlaps  to    know    what,    if    any,    combinations    of 

with  weights  of  a  long  series  of  wolves  from  characters  reliably  separated  known  Canis 

Algonquin   Provincial   Park    (unpublished  lupus,  latrans,  and  familiaris,  particularly 

data    from    the    Ontario    Department    of  if  size  were  eliminated  as  a  character.   This 

Lands  and  Forests)   and,  as  a  result,   size  part  of  the  work  will  be  described  in  detail 

alone  becomes  a  less  useful  criterion  in  dis-  in  section  I. 
tinguishing  between  wolves  and  coyotes.  While  these  three  species  are  unquestion- 

In  the  following  discussion,  since  Canis  ably  distinct,  the  red  wolf,  currently  called 

lupus,  the  wolf,  and  Canis  latrans,  the  coy-  Canis  niger,  is  a  more  problematical  entity 

ote,  are  both  composite  species,  these  names  and  will  be  discussed  in  section  II  in  the 

as  used  in  the  text  refer  to  each  species  as  light  of  our  findings  in  section  I. 

(223) 


72 


224 


Barbara  Lawrence  and  William  H.  Bossert 


SECTION  I 

The  purpose  of  this  part  of  the  study 
was  to  determine  what,  if  any,  combina- 
tions of  characters  separate  the  three  spe- 
cies, C.  lupus,  C.  latrans,  and  C.  familiaris, 
and  how  widely  they  are  separated.  To  do 
this,  we  have  used  a  biased  random  selec- 
tion of  20  adult  members,  including  males 
and  females,  of  each  species.  In  latrans, 
wide  geographic  distribution  within  the 
original  range  of  the  species  was  an  impor- 
tant factor  in  choice  of  specimens.  In  lu- 
pus, only  North  American  races  were  used 
and  large  individuals  were  avoided.  In  fa- 
miliaris,  the  selection  was  deliberately  bi- 
ased to  include  the  most  wolf-like  and  coy- 
<ote-like  animals. 

Characters  to  be  used  were  not  randomly 
selected  but  chosen  because  of  their  known 
value  in  distinguishing  the  species  in- 
volved. Forty-two  different  measurements 
(see  appendix)  were  taken  on  as  many  as 
225  skulls.  The  measurements  of  125  of 
these  were  then  variously  plotted  to  esti- 
mate regression  lines.  Based  on  these,  24 
possibly  significant  characters  were  selected, 
13  dealing  with  skull  shape  and  11  with 
tooth  form,  to  test  for  diagnostic  value. 
Since  we  wished  to  ascertain  whether  or 
not,  regardless  of  size,  skulls  of  each  of  the 
species  had  certain  unique  characters  or 
combinations  of  characters,  size  was  elimi- 
nated as  a  factor  by  relating  all  measure- 
ments to  total  length  of  skull.  The  mean 
and  standard  deviation  of  these  24  charac- 
ters, as  a  fraction  of  total  length,  were  com- 
puted for  each  of  the  selected  series. 
The  value  of  each  character  in  distin- 
guishing a  pair  of  species  was  tested  by 
computing  single  character  distances  for 
the  pair,  dividing  the  difference  in  means 
for  the  two  populations  by  the  average 
standard  deviation. 

From  this  analysis,  nine  cranial  and  six 
tooth  measurements  were  found  to  be  most 
diagnostic,  although  no  single  character 
was  found  without  overlap  between  a  pair 
of  species.  These  were  the  measurements 
used  in  our  linear  discrimination. 

In  the  following  non-numerical  descrip- 
tion of  differences  between  the  species  con- 
sidered, the  numbers  of  the  measurements, 


which  are  expressions  of  these  differences, 
and  which  were  used  in  our  linear  discrimi- 
nation, are  given  in  parentheses.  For  de- 
scriptions of  the  measurements  see  Appen- 
dix A. 

When  lupus  and  latrans  are  compared, 
it  is  found  that  the  most  significant  differ- 
ences are  in  the  relative  development  of 
the  rostrum  and  of  the  brain  case.  W^olves 
have  a  relatively  small  brain  case  and  mas- 
sive rostrum.  The  latter  is  presumably  a 
reflection  of  the  large  size  of  the  animals 
on  which  they  prey.  Breadth  of  palate  (7, 
19),  large  teeth  (11,  12,  13,  15,  20),  and 
heavy  maxilla  (8),  all  contribute  to  the 
formation  of  powerful  jaws.  The  position 
of  the  anterior  root  to  the  zygomatic  arch 
and  its  massiveness  help  to  buttress  the 
teeth  and  strengthen  the  crushing  action 
of  the  jaws.  In  the  intermediate  region  of 
the  skull,  the  strength  of  the  masticatory 
apparatus  shows  in  the  depth  of  the  jugal 
bone  (18)  and  in  the  size  of  the  temporal 
fossa.  The  one  provides  attachment  for  the 
masseter  muscle,  the  other  space  for  the 
temporal  muscle.  This  space  is  difficult  to 
measure,  but  the  relation  between  the 
broadly  spreading  zygomatic  arches  (4)  and 
the  narrow  brain  case  (6)  expresses  it  well. 
Size  of  the  temporal  muscle  is  also  shown 
by  the  development  of  a  large  sagittal  crest. 

Coyotes,  preying  as  they  do  on  small  spe- 
cies, have  opposite  skull  proportions  and 
small,  narrow  teeth.  Compared  with  the 
brain  case,  the  rostrum  is  slender,  the  max- 
illa and  the  anterior  root  of  the  zygomatic 
arch  less  massive,  the  temporal  fossa  small- 
er, and  the  jugal  narrower.  All  of  this  gives 
the  skull  a  rather  long  slender  appearance 
as  compared  with  that  of  a  wolf.  This  over- 
all distinction  is  a  good  one  and  has  often 
been  used  as  diagnostic  in  separating  wolf 
and  coyote  skulls,  but  it  can  be  confusing. 
Ratios  of  total  length  to  zygomatic 
breadth  in  long,  narrow,  wolf  skulls  may 
overlap  with  these  ratios  for  short,  broad, 
coyote  skulls.  If  width  of  the  brain  case, 
width  across  molars,  and  width  between 
premolars  anteriorly  are  also  taken  into  ac- 
count, the  characteristic,  relatively-small 
brain  case  of  a  typical  wolf  skull  is  imme- 
diately apparent. 


73 


Multiple  Character  Analysis  of  Cayiis 


225 


Dogs  present  a  different  problem.  Essen- 
tially they  are  small  wolves,  distinguishable 
from  coyotes  by  many  of  the  wolf-like  pro- 
portions of  rostrum  and  brain  case.  How- 
ever, their  great  variability  means  that  no 
single  set  of  characters  is  equally  diagnos- 
tic for  all  kinds.  Key  characters  for  sepa- 
rating lupus  and  latrans  are  based  on  a  cer- 
tain intraspecific  homogeneity  which  is  not 
too  difficult  to  describe  or  to  see.  C.  famili- 
aris  lacks  this  homogeneity  and  often  super- 
ficially resembles  either  of  the  other  two 
more  than  it  does  other  familiaris.  This 
means  that  the  best  combinations  of  char- 
acters to  be  used  for  purposes  of  identifica- 
tion vary  depending  on  whether  the  animal 
in  question  is  large  and  wolf-like  or  small- 
er and  coyote-like.  Certain  of  the  highly 
modified  breeds  are,  of  course,  easily  iden- 
tified by  the  disproportionate  development 
of  brain  case  or  rostrum.  Other  less  modi- 
fied forms  may  be  distinguished  by  the  in- 
flation of  the  frontal  sinuses  and  resultant 
steep  angle  of  the  forehead.  They  may  also 
be  recognized  by  a  bend  in  the  mid-region 
of  the  skull  so  that  rostrum  and  brain  case 
meet  at  more  of  an  angle  than  is  usual  in 
wild  canids. 

Turning  to  the  less  modified  kinds,  and 
these  include  many  mongrels,  the  large 
dogs  differ  from  wolves  in  having  relatively 
small  teeth,  and  having  the  skull  elongated 
in  the  interorbital  region  so  that  the  dis- 
tance between  the  tooth  row  and  the  bulla 
(2)  is  long  compared  with  the  length  of  the 
tooth  row  (10) .  The  palate  also  is  elon- 
gated so  that  its  posterior  margin  lies  well 

posterior  to  m-.  The  brain  case  often  looks 
atypically  heavily  ossified.  The  sagittal 
crest  is  usually  drawn  out  less  far  beyond 
the  occiput;  when  it  is  strongly  developed 
and  projecting,  the  dorsal  margin  usually 
curves  strongly  down  at  the  tip.  Briefly, 
big  dogs  look  rather  as  if  they  had  out- 
grown themselves  and  were  never  meant  to 
be  that  size. 

For  the  most  part,  wolf-like  proportions 
of  brain  case  and  rostrum  distinguish  most 
dogs  from  coyotes.  Long,  narrow-skulled 
dogs  may  approach  coyotes  in  some  of  their 
length-breadth  proportions,  but  not  in  all 


of  them,  and  a  coyote-like  elongation  of  the 
tooth  row  is  not  usually  accompanied  by 
coyote-like  proportions  of  the  teeth. 

Disparate  proportions  of  the  teeth  which 
show  as  differences  in  certain  of  them  also 
help  to  distinguish  dogs  and  coyotes.  The 
relatively  greater  size  of  the  canine  (13)  in 
dogs  may  be  a  reflection  of  their  relation- 
ship with  wolves.  The  greater  width  across 
the  incisors  (15)  is  partly  an  expression  of 
larger  tooth  size;  however,  it  also  expresses 
the  greater  premaxillary  width  of  dogs.  In 
contrast,  the  last  upper  molar  is  small  (14). 
This  tooth,  as  frequently  happens  with  the 
anteriormost  or  posteriormost  of  the  cheek 
teeth,  is  the  most  variable  tooth  in  the  up- 
per jaw.  Nevertheless,  its  average  smaller 
size  in  dogs  than  in  wolves  and  coyotes  is  a 
good  diagnostic  feature  and  may  be  one  of 
the  results  of  domestication.  The  last  char- 
acter to  be  considered  is  characteristic  of 
most  coyotes  and  is  one  of  the  best  expres- 
sions of  the  general  narrowing  of  the  pre- 
molars and  carnassials  in  this  form.  The 
posterior  part  of  pj  (22)  is  relatively  long 
compared  both  to  the  length  of  the  tooth 
(20)  and  to  its  maximum  width.  Because  of 
this  lengthening,  a  second  accessory  cusp 
behind  the  main  cusp  is  usually  present  in 
coyotes  and  has  often  been  used  as  diagnos- 
tic (Gidley,  1913). 

We  have  applied  the  technique  of  linear 
discrimination  as  described  by  Kendall 
(1946).  Jolicoeur  (1959),  who  has  used  line- 
ar discrimination  to  somewhat  different 
ends,  gives  an  excellent  graphical  explana- 
tion of  the  technique.  The  computations 
were  done  on  an  IBM  7094  computer  using 
the  BIMD  05  program  developed  by  the 
University  of  California  at  Los  Angeles 
Medical  School.  In  short,  the  technique 
finds  the  weighted  sum  of  a  number  of 
characters  which  is  most  different  for  two 
populations,  that  is,  the  weighted  sum  of 
characters  which  best  separates  the  popula- 
tions. The  sum  itself  is  called  the  discrimi- 
nant function,  and  the  weights,  determined 
by  the  computations,  are  called  the  dis- 
criminant coefficients.  The  mean  value  of 
the  discriminant  function  for  each  of  the 
populations  can  be  obtained  by  multiply- 


74 


226 


Barbara  Lawrence  and  William  H.  Bossert 


ing  the  mean  value  of  each  character  over 
the  population  by  the  discriminant  coeffi- 
cient for  the  character  and  then  summing. 
If  an  individual  is  known  to  belong  to  one 
of  a  pair  of  populations,  he  can  be  identi- 
fied by  evaluating  the  discriminant  func- 
tion separating  the  pair  for  his  values  of 
the  characters  (that  is,  summing  the 
weighted  measurements  for  the  specimen) 
and  assigning  him  to  the  population  hav- 
ing the  closest  mean  value  of  the  function. 
The  accuracy  of  the  identification  will  de- 
pend, of  course,  on  the  degree  to  which  the 
populations  are  separated  by  the  discrimi- 
nant function.  A  useful  measure  of  the 
multiple  character  difference  between  two 
populations  is  the  D-  statistic  of  Mahalo- 
nobis  (see  Rao,  1952) .  This  is  a  general 
extension  of  the  distance  comparisons  for 
single  characters  mentioned  earlier. 

For  this  study  the  discriminant  coeffi- 
cients and  the  D-  statistic  for  each  pair  of 
the  selected  populations  of  C.  latrans,  lu- 
pus, and  familiaris  were  computed  using 
the  fifteen  characters  discussed  above.  The 
discriminant  coefficients  are  given  in  Table 
1   along  with  the  mean  values  of  the  dis- 

TABLE   1.    Results   of  pairwisc  discriminant  analysis 
for  C.  latrans,  lupus,  and  familiaris. 


Discriminant  coefficient 

lupus  vs. 

latrans  vs. 

lupus  vs. 

Measurements* 

latrans 

familiaris 

familiaris 

2 

3.389 

—  16.876 

—  6.900 

4 

—  7.107 

14.670 

8.494 

6 

14.971 

—  11.182 

—  6.760 

7 

—  0.495 

—  11.246 

—  5.124 

8 

—  7.313 

—33.699 

—  7.849 

10 

9.889 

—24.989 

—  10.108 

11 

14.984 

66.749 

26.784 

12 

—  12.510 

—25.968 

—   1.089 

13 

—24.891 

—77.655 

—  4.088 

20 

-32.167 

5.155 

22.738 

22 

87.360 

35.272 

—33.076 

14 

3.652 

63.729 

0.606 

15 

—  8.932 

—28.702 

—  3.531 

18 

3.299 

31.510 

0.784 

19 

1.230 

—  15.404 

—  10.638 

Average  discrimi 

- 

nant  function 

value  for  latrans      4.79 

—  14.6 

for  lupus 

3.10 

—  4.73 

for  familiaris 

—  17.8 

—  5.44 

D^(D) 

64.1  (8.0) 

119.9(10.9) 

27.2(5.2) 

criminant  functions  for  the  populations,  D^ 
and  D.  The  last  value  is  roughly  the  dif- 
ference in  standard  deviations  between  the 
mean  values  of  the  function  for  the  two 
populations.  We  see  that  latrans  differs  by 
eight  and  nearly  II  standard  deviations 
from  lupus  and  familiaris,  respectively, 
while  lupus  and  familiaris  differ  by  only  a 
little  more  than  five. 

A  clear  view  of  the  degree  of  separation 
of    the    populations    achieved   by    the    dis- 
criminant functions  results  from  the  a  pos- 
teriori identification  of  the  original   indi- 
vidual specimens  using  the  functions.    For 
each   of   the   pairwise   discriminations    the 
specimens  were  assigned  to  one  species  ten- 
tatively.   A    final    identification    was    then 
made   by   assigning   the   specimen   to   that 
species  for  which  two  tentative  assignments 
had  been  made.    For  example,  if  between 
latrans    and    lupus    the   specimen   was    as- 
signed  to   lupus,  between   latrans  and  fa- 
miliaris to  latrans,  and  between  lupus  and 
familiaris  to  lupus,  then  the  specimen  was 
identified  as  lupus.   In  this  way  all  sixty  of 
the    specimens    were    unambiguously    and 
correctly  identified;   there  was  no  overlap 
in  the  values  of  the  various  discriminant 
functions    for    the    populations    on    which 
they  were  based.    Figure  1  gives  a  plot  of 
the  populations  using  the  latrans-lupus  and 
latrans-familiaris  discriminant  functions  as 


5  - 


J. 


J. 


*  Measurements  are  numbered  as  in  Appendix. 
Each  must  be  divided  by  total  length  of  skull, 
measurement  1. 


--14  -15  ^16  -17  -18  ' 

FIG.  1.  Linear  discrimination  of  C.  latrans  (C), 
C.  lupus  (W),  and  C.  familiaris  (D).  The  contours 
indicate  the  extreme  range  of  individuals  in  the 
populations  used.  The  latrans-familiaris  discrimi- 
nant function  is  used  as  the  abscissa  and  the  lat- 
rans-lupus discriminant  function  is  used  as  ordi- 
nate. 


75 


Multiple  Character  Analysis  of  Canis 


227 


coordinate  axes.  This  figure  shows  the  rela- 
tive separations  of  the  populations  as  well 
as  the  lack  of  overlap. 

SECTION    II 

As  stated  earlier,  in  North  America,  in 
addition  to  C.  lupus  and  C.  latrans,  a  third 
species  of  wild  Canis,  C.  niger,  the  red 
wolf,  is  currently  recognized.  Young  and 
Goldman  (1944)  describe  it  as  a  wolf  which 
is  somewhat  intermediate  between  lupus 
and  latrayis,  with  a  distribution  limited  to 
the  south-eastern  part  of  the  United  States. 
This  is  a  unique  situation  since  all  other 
wolves  in  both  Eurasia  (Pocock,  1935)  and 
North  America  are  races  of  C.  lupus. 
Ranges  as  plotted  for  lupus  and  niger  by 
Young  and  Goldman  (1944)  show  an  over- 
lapping of  lupus  with  niger  in  the  south- 
eastern part  of  the  former's  range.  Even 
more  surprising  is  the  overlapping  of  all 
three  species  of  Canis  at  the  western  edge 
of  the  range  of  niger  and  the  eastern  edge 
of  that  of  latrans  (Young  and  Jackson, 
1951;  Young  and  Goldman.  1944).  Such  an 
occurrence  together  of  three  closely  related 
members  of  the  genus  Canis  is  without 
parallel  elsewhere  in  the  world.  The  situ- 
ation is  obviously  peculiar,  and  various  au- 
thors have  attempted  to  explain  it.  It  is 
not  pertinent  here  to  review  these  discus- 
sions; suffice  it  to  say  that  for  the  most  part 
they  have  concentrated  on  the  relationship 
between  niger  and  latrans.  The  most  re- 
cent effort  to  unravel  the  problem  is  a 
paper  by  McCarley  which  includes  an  in- 
teresting discussion  of  the  possibility  of  hy- 
bridization and  population  replacement 
(1962)  where  latrans  is  encroaching  on  the 
range  of  niger. 

Implicit  in  McCarley's  interpretation  of 
his  data,  though  not  explicitly  stated,  is  the 
fact  that,  while  closely  related  species  usu- 
ally differ  most  from  each  other  where  their 
ranges  meet  or  overlap,  the  opposite  is  true 
of  these  forms  in  the  south-central  states. 
Here,  at  the  western  edge  of  the  range  of 
niger,  the  small  C.  n.  rufus  Audubon  and 
Bachman  1851  is  often  difficult  to  tell  from 
C.  latrans  frustror  Woodhouse  1851,  while 
at  the  eastern  end  of  its  range,  the  larger  C. 
n.  niger  Bartram  1791  is  said  to  resemble  C. 


lupus  lycaon  Schreber  1775  (Young  and 
Goldman,  1944).  Essentially,  as  presently 
defined,  niger  appears  as  a  population  in- 
termediate in  characters  between  a  large 
western  latrans  and  a  small  eastern  lupus. 
Efforts  to  determine  the  true  status  of 
niger  will  be  helped  if  we  first  understand 
some  of  its  taxonomic  history.  Because  of 
the  complications  of  priority,  Canis  rufus 
from  Texas  with  three  subspecies  of  in- 
creasing size  from  west  to  east  now  figures 
in  the  literature  as  Canis  niger  of  Florida 
with  three  subspecies  of  decreasing  size 
from  east  to  west.  The  three  related  forms 
are  the  same  in  each  case,  but  depending 
on  which  end  of  the  range  one  starts  from, 
the  reasons  for  the  primary  distinction  of 
the  species  are  different.  Canis  rufus  as  a 
Texas  phenomenon  had  a  quite  different 
reason  for  being  set  apart  than  did  Canis 
niger  as  a  Florida  phenomenon.  The  ear- 
liest descriptions  of  a  small  wolf  in  the 
south-central  states  are  based  on  the  occur- 
rence of  a  medium-sized  non-coyote  in  east- 
ern Texas.  Animals  were  found  which  re- 
sembled coyotes  in  size  but  not  in  cranial 
characters,  and  the  difference  in  size  be- 
tween these  animals  and  the  big  plains 
wolves  was  so  gieat  that  the  two  were 
scarcely  compared.  Typical  coyotes  were 
also  found  to  occur  in  the  same  area.  The 
fact  that  two  distinct  kinds  of  Canis  were 
recognized  is  more  important  than  the  rea- 
sons why  the  name  rufus  was  selected  for 
the  one  and  frustror  for  the  other  (Young 
and  Goldman,  1944;  Young  and  Jackson, 
1951).  Once  rufus  was  set  apart  as  a  dis- 
tinct species  of  wolf,  efforts  were  made  to 
determine  the  eastern  limits  of  its  range.  A 
reasonable  number  of  specimens  was  avail- 
able from  Louisiana,  but  progressing  to- 
wards Florida  the  number  of  available 
specimens  diminishes  rapidly.  There  are 
very  few  from  that  part  of  the  range  where 
nigei-  and  lupus  lycaon  supposedly  meet. 
Since,  in  addition  to  this,  there  are  almost 
no  extant  specimens  of  C.  lupus  lycaon 
from  the  southeastern  states,  it  is  easy  to 
see  why  the  relationship  between  the  east- 
ern red  wolf,  C.  n.  niger,  and  C.  lupus  ly- 
caon has  not  been  more  thoroughly  ana- 
lyzed. 


76 


228 


Barbara  Lawrence  and  William  H.  Bossert 


If  the  study  of  the  small  wolves  in  the 
southern  states  had  begun  with  niger  in 
Florida  and  been  based  on  adequate  series, 
it  is  highly  unlikely  that  niger  ever  would 
have  been  separated  as  a  species  from  lupus. 
The  biologically  difficult  problem  of  re- 
concilino;  the  existence  of  two  similarly- 
sized  forms  of  wolf  in  one  continuous  habi- 
tat would  never  have  arisen  and  the  area 
of  systematic  uncertainty  would  have  been 
more  properly  limited  to  the  eastern  edge 
of  the  coyote's  extending  range. 

The  purpose  of  this  part  of  the  present 
work  has  been  to  establish  whether  or  not 
two  distinct  species  of  wolf  occur  in  the 
southeastern  United  States.  The  following 
discussion  presents  our  evidence  for  con- 
sidering that  the  wolves  of  this  area  all  be- 
long to  the  species  lupus  and  that  niger  is 
not  a  distinct  species.  Unequivocal  estab- 
lishment of  the  status  of  niger  has  seemed 
a  necessary  preliminary  to  understanding 
and  identifying  the  widely  varying  popula- 
tions from  west  of  the  Mississippi  presently 
identified  as  n.  gregoryi  Goldman  1937  and 
n.  rufus. 

In  order  to  be  as  certain  as  possible  that 
we  were  excluding  latrans  from  our  sample 
population,  the  series  selected  for  a  linear 
discrimination  was  limited  to  all  available 
specimens  of  C.  n.  niger  and  C.  n.  gregoryi 
collected  before  1920  from  Louisiana,  Ala- 
bama, and  Florida;  in  addition,  a  Florida 
skull  previously  identified  as  C.  lupus  lyca- 
on  was  included.  In  the  following  discus- 
sion this  series  is  referred  to  as  C.  niger. 
The  type  of  floridanus  Miller  1912  (^=  ni- 
ger), though  it  could  not  be  included  be- 
cause the  skull  is  too  broken,  falls  within 
the  range  of  variation  of  the  rest  of  the 
series. 

In  our  linear  discrimination,  comparison 
was  made  with  the  broadly  representative 
series  of  the  three  species,  lupus,  latrans, 
and  familiaris,  used  in  the  first  section.  It 
was  also  made  with  a  series  of  ten  males 
and  ten  females,  all  adult,  of  Canis  lupus 
lycaon,  the  race  whose  range  has  been  pre- 
sumed to  overlap  with  that  of  niger  in  the 
Southeast.  The  individuals  were  randomly 
selected  from  71  specimens  from  Algonquin 
Provincial   Park   in    Canada   and   weighed 


from  48-81  pounds  (average  58).  It  was  nec- 
essary to  use  a  northern  population  be- 
cause adequate  series  from  farther  south 
were  not  preserved  before  wolves  were  ex- 
terminated. 

To  the  eye,  the  specimens  of  niger  stud- 
ied appear  /upu5-like  and  this  is  borne  out 
by  the  numerical  analysis.  As  a  first  step 
in  the  analysis,  all  of  the  individual  speci- 
mens in  the  niger  and  lycaon  populations 
were  identified  using  the  discriminant  func- 
tions presented  in  the  previous  section.  All 
were  assigned  to  the  lupus  category;  they 
were  on  the  whole  both  less  coyote-like  and 
less  dog-like  than  the  original  lupus  popu- 
lation. In  itself  this  provides  little  infor- 
mation about  the  relationships  of  lupus  to 
these  populations,  of  course,  since  the  iden- 
tification tacitly  assumes  the  individuals  to 
be  from  the  latrans,  lupus,  or  familiaris 
groups.  The  study  was  continued,  there- 
fore, by  computing  the  discriminant  func- 
tion coefficients  and  D^  values  for  all  pairs 
of  the  five  populations.  The  values  of  D^ 
are  given  in  Table  2.   Using  these  with  the 

TABLE  2.    The  generalized  distance,  D*,  between  pop- 
ulatiojis  described  in  the  text. 

C. latrans 
C.lupus  64.1    C. lupus 

C.  familiaris  119.9        27.2    C. familiaris     r  i^jjus 

C.  lupus  lycaon      69.5        10.0 


C.  niger 


116.0       20.3 


66.6 
87.6 


lycaon 
56.0 


cluster  grouping  technique  discussed  by 
Rao  (1952),  the  lycaon  and  niger  popula- 
tions form  a  cluster  with  the  selected  lupus 
population.  The  average  D^  within  this 
cluster  is  28.8,  while  the  average  D^  of  its 
members  to  populations  outside  the  cluster 
is  71.8.  Although  the  lycaon  and  niger 
populations  are  fairly  distinct,  they  are 
even  more  distant  from  the  latrans  and  ja- 
miliaris  species  groups,  and  have  a  common 
similarity  to  the  lupus  population.  These 
relationships  are  shown  fairly  well  in  Fig- 
ure 2,  the  plot  of  the  populations  using  the 
latrans-lycaon  and  lycaon-niger  discrimi- 
nant functions  as  coordinate  axes.  The  lat- 
ter axis  provides  maximum  separation  of 
the  wolf  populations.    Notice  that  the  lu- 


ll 


Multiple  Character  Analysis  of  Canis 


229 


3r 


N 


_L 


_L 


I 


N 


II  12  13  14  15 

FIG.  2.  Linear  discrimination  of  C.  latrans  (C),  C. 
lupus  (\V),  C.  lupiis  lycaon  (A),  and  C.  n/ger  (N). 
The  lycaon-niger  discriminant  function  is  used  as 
the  abscissa  and  the  latrans-lycaon  discriminant 
function  is  used  as  ordinate. 

pus  population  falls  intermediate  to,  and 
completely  bridges,  the  gap  between  lycaon 
and  niser. 

Although  we  did  not  include  recently 
collected  specimens  of  red  wolf  from  Lou- 
isiana in  our  linear  discrimination,  the 
relative  position  of  each  individual  speci- 
men was  computed  and,  while  found  to  be 
clearly  wolf,  the  specimens  were  spread 
somewhat  o\er  the  range  from  niger  to  ly- 
caon. 

It  now  appears  that  the  early  populations 
described  as  Canis  niger  and  n.  gregoryi 
from  the  southeastern  wooded  regions,  east 
of  the  range  of  Canis  latrans,  are  a  local 
form  of  Canis  lupus,  not  a  distinct  species 
of  wolf.  The  situation  in  the  areas  where 
these  small  wohes  and  the  large  coyote, 
C.  /.  frustror,  meet  is  much  more  confused. 
The  present  study  has  not  attempted  to  go 
beyond  McCarley's  conclusions  (1962).  We 
have,  however,  tested  our  methods  on  a 
small  series  from  Fallsville,  Newton  Coun- 
ty, Arkansas.  The  specimens,  collected  in 
1921  and  identified  as  Canis  niger  gregoryi 
(Young  and  Goldman,  1944),  span  the 
whole  range  of  variation  from  coyote  to 
wolf.  Figure  3  shows  this  variation  of  the 
individuals  using  the  latrans-lycaon  and 
lycaon-niger  discriminant  function  as  co- 
ordinate axes,  as  in  Figure  2. 

DISCUSSION 

To  date  most  efforts  to  measure  differ- 
ences between  wolf,  coyote,  and  dog  skulls 


11  12  13  14  15 

FIG.  3.  Evaluation  of  discriminant  functions  for 
the  series  of  C.  niger  gregoryi  from  Fallsville,  Ar- 
kansas. The  coordinate  axes  are  identical  to  those 
of  Figure  2. 

have  used  a  few  specific  measurements  such 
as  width  between  the  premolar  teeth  ante- 
riorly, or  have  relied  on  standard  length- 
breadth  comparisons  of  the  whole  skull  as, 
for  instance,  relation  of  zygomatic  width  to 
total  length.  Such  data  are  useful  but  show 
too  much  overlap  to  separate  reliably  the 
species  involved.  They  are  also  inadequate 
as  an  expression  of  the  basic  differences  be- 
tween the  skulls.  These  basic  differences 
center  around  the  differential  development 
of  different  segments  of  the  skull  which,  in 
their  extreme  form,  are  easily  seen.  Brain 
case,  rostral,  and  interorbital  shape  of  a 
t^pical  coyote  are  quite  different  from 
those  of  a  typical  wolf.  The  significance  of 
cranial  measurements  in  expressing  these 
differences  in  proportion  depends  on  the 
multiple  relationships  of  each  measure- 
ment with  a  number  of  others,  when  size 
has  been  eliminated  as  a  factor.  The  tech- 
nique of  linear  discrimination  has  allowed 
us  to  make  use  of  these  multiple  relation- 
ships in  comparing  skulls.  The  results  of 
these  comparisons  showed  that  all  three 
species  are  sharply  distinct,  with  lupus  and 
familiaris  resembling  each  other  more  than 
either  does  latrans. 

Since  size  has  been  eliminated  as  a  char- 
acter, the  numerical  values  of  the  discrimi- 
nant function  may  show  two  skulls  to  be 
most  closely  related  which  on  the  basis  of 
size  alone  would  be  easy  to  tell  apart.  The 
same  may  be  true  of  other  unmeasurable 
but  diagnostic  characters. 

Often,  of  course,  there  is  little  difficulty 
in  distinguishing  between  the  three  species 


78 


230 


Barbara  Lawrence  and  William  H.  Bossert 


without  resort  to  the  kind  of  analysis  de- 
scribed above.    In   addition   to  differences 
already  discussed  in  the  text,  certain  spot 
differences  are  often  highly  diagnostic:  flat- 
tened, rugose  bullae  characterize  dogs.  Coy- 
otes have   the   dorso-posterior  part  of   the 
brain  case  well  inflated,  with  the  maximum 
width  of  brain  case  in  the  region  of  the 
parietotemporal  suture,  the  frontal  shield 
not  tilted  up,  and  the  postorbital  constric- 
tion close  to  the  postorbital  processes.    In 
wolves  and  dogs,   the  maximum  width  of 
the  brain  case  is  usually  at  the  roots  of  the 
zygoma;  the  frontal  shield  tilts  up,  and  the 
postorbital  region  is  elongated,  so  that  the 
constriction    at    the    anterior    part    of    the 
brain  case  and  that  behind  the  postorbital 
processes  are  well  separated  and  the  area 
between  inflated.   Further  accentuating  the 
different  appearance  of  this  region  is  the 
fact  that  the  dorsal  surface  of  the  brain  case 
in  wolves  and  dogs  is  lower  relative  to  the 
postorbital  processes  than  in  coyotes.    The 
orbit   in    coyotes    tends    to   be    large;    this 
shows  both  in  vertical  dimensions  and  in 
its  length  as  compared  to  that  of  the  zygo- 
matic arch.   In  coyotes  also,  as  distinct  from 
dogs  and  wolves,  there  is  a  round  protuber- 
ance of  the  occiput,  often  thin-walled,  over 
the  vermis  of  the  cerebellum;   certain  dif- 
ferences in  the  teeth,  though  not  precisely 
measurable,     are    also    rather    diagnostic. 
These    are    well    reviewed    in    Young   and 
Jackson    (1951)  and  will  not  be  repeated 
here.   In  addition,  the  present  authors  have 

found  useful  the  fact  that  in  coyotes  M- 
measured  lateromedially  has  the  distance 
from  the  outer  border  of  the  tooth  to  the 
base  of  the  paracone  less  than  the  distance 
from  this  point  to  the  inner  margin  of  the 
tooth,  while  the  reverse  is  true  in  wolves 
and  dogs.  Wear  makes  this  a  difficult  meas- 
urement to  take  precisely,  but  the  differ- 
ence, expressing  as  it  does  the  plumper 
para-  and  metacones  of  wolves  and  dogs,  is 
a  significant  one.  None  of  these  characters 
is  completely  reliable,  just  as  is  none  of 
those  described  earlier.  Used  in  combina- 
tion, and  with  total  size  included,  they  are 
adequate  to  identify  most  canids. 

The  significance  of  the  present  study  lies 
in  the  fact  that  linear  discrimination,  based 


on    characters    tested    for    their   diagnostic 
value,  can  separate  similarly-sized  individ- 
uals of  each  of  the  three  species  considered. 
A  corollary  of  this  is  the  fact  that  a  small 
wolf  does  not  assume  the  characters  of  a 
large  coyote,  nor  is  the  reverse  true.    Cri- 
teria have  been  observed  and  tested  which 
distinguish  the  two  species  and  these  may 
be  used  to  separate  individuals  which  ap- 
proach each  other  in  size.    This  has  made 
possible    a    re-examination   of   the   specific 
status  of  the  red  wolf,  long  a  biologically- 
puzzling  phenomenon.    From  the  evidence 
at  hand,  it  appears  that  from  central  Lou- 
isiana east  to  Florida  the  large  canids  hith- 
erto called  C.  niger  and  niger  gregoryi  are 
no  more  than  subspecifically  distinct  from 
Canis  lupus.    Preliminary  study  of  a  small 
sample  from  the  western  part  of  the  red 
wolf's  range  shows  typical  lupus  and  typical 
latrans  both  present,  with  the  possibility  of 
hybridization   as   McCarley   has   suggested. 
In  investigating  this  possibility,  we  can  now 
assume  that  w^e  are  considering  only  two 
species  of  wild  canid,  not  three  as  has  been 
previously  supposed,  and  that  we  have  over- 
lapping and  possible  hybridization  of  these 
two   distinct   species,   not  an    intergrading 
from   coyote   to  wolf  across   the   southern 
states   as   has   sometimes    been    postulated. 
Our  test  analysis  of  the  Fallsville  specimens 
has  also  confirmed  what  has  been  apparent 
for  a  long  time,  that  cranial  variation  in 
localized   series   currently   called   C.   niger 
gregoryi  or  C.  niger  rufus  is  atypically  wide 
for  a  race  of  North  American  Canis.    Not 
only  is  it  greater  than  the  range  for  a  local 
population  of  a  given  subspecies  of  either 
lupus  or  latrans,  but  it  is  also  wider  than 
the    range    for   either   species    taken    as    a 
whole.    Either  this  means  sympatry  of  lo- 
cally similar  forms  which   have   the  same 
chromosome  number  and  essentially  similar 
karyograms     (Benirschke    and   Low,    1965; 
Hungerford  and  Snyder,  1966) ,  or  it  means 
hybridization.    Before  this  can  be  decided, 
both  the  morphological  and  the  behavioral 
characteristics  of  these  populations  need  to 
be  studied  in  more  detail. 

appendix  a 
Following  are  listed  the  42  measurements 


79 


Multiple  Character  Analysis  of  Canis 


231 


taken  on  the  entire  series.  In  the  first  para- 
graph are  given  the  24  tested  for  diagnos- 
tic value.  The  16  of  these  used  in  our  line- 
ar discrimination  are  italicized.  In  the  sec- 
ond paragraph  is  a  briefer  listing  of  the  re- 
maining 18  characters,  which  were  found  to 
be  not  taxonomically  reliable. 

Skull.  1.  Total  length  from  sagittal  crest 
to  alveoli  of  I—;  2.  Minimum  distance  from 
alveolus  of  M-  to  depression  in  front  oj 
bulla  at  base  of  styloid  process;  3.  Mini- 
mum length  of  rostrum  from  orbital  mar- 
gin to  alveolus  of  I-;  4.  Zygomatic  width; 
5.  Breadth  across  postorbital  processes;  6. 
Maximum  breadth  of  brain  case  at  parieto- 
temporal suture;  7.  Maximum  crown  width 
across  upper  cheek  teeth;  8.  Minimum  dis- 
tance taken  at  right  angles  from  alveolar 
margin  of  molars  to  orbit;  9.  Maximum  di- 
ameter of  orbit,  parallel  to  medial  edge  and 
starting  at  most  ventral  point;   10.  Crown 

length  of  upper  cheek  teeth  from  C  -  M-; 
1 1.  Crown  length  of  P-  externally;  12.  Mini- 
mum crown  width  of  P-  taken  between 
roots;  13.  Maximum  antero-posterior  width 
of  upper  canine  taken  at  base  of  enamel; 

14.  Crown  width  of  M-;  15.  Crown  width 
across  upper  incisors;  16.  Height  of  brain 
case  vertical  to  basi-sphenoid  and  not  in- 
cluding sagittal  crest;  17.  Maximum  width 
across  occipital  condyles;  18.  Minimum 
height  of  jugal  at  right  angles  to  axis  of 
bone;  19.  Minimum  width  between  alveoli 

of  P-.  Lower  jaw.  20.  Crown  length  of  P-; 
21.    Maximum    crown    width    of    P--;    22. 

4 

Length  of  posterior  cusps  of  P-,  along  line 
parallel  to  base  from  back  of  tooth  to  point 
below  notch  posterior  to  main  cusp;  23. 
Crown  length  of  M-  parallel  to  main  axis; 
24.  Maximum  crown  width  of  M-  at  right 
angles  to  main  axis. 

Skull.  Condylo-basal  length;  palatal 
length;  length  of  brain  case;  interorbital 
width;  width  of  rostrum;  width  of  nasals; 
height  of  nasal  aperture;  alveolar  length  of 
upper  cheek  teeth;  alveolar  length  of  P-; 
maximum  width  of  P-  anteriorly;   antero- 


posterior  diameter  of  I-;  height  of  bullae; 
height  of  posterior  bony  nares.  Lower  jaw. 
Total  length;  distance  from  back  of  tooth 
row   to  condyle;    alveolar   length   P-  -  M-; 

alveolar  length  C  -  M-;   crown   length   C  - 


M-. 

3 


ACKNOWLEDGMENTS 


The  authors  are  indebted  to  Mr.  John  L.  Para- 
diso  of  the  United  States  National  Museum,  Dr. 
George  B.  Kolenosky  of  the  Ontario  Department 
of  Lands  and  Forests,  Dr.  Douglas  H.  Pimlott  of 
the  University  of  Toronto,  and  Dr.  Claude  Minguy 
of  the  Department  of  Fish  and  Game  of  the  Prov- 
ince of  Quebec  for  making  available  much  impor- 
tant material. 

This  work  has  been  supported  by  National  Sci- 
ence Foundation  Grant  GB-1265.  Computer  time 
was  supported  by  National  Science  Foundation 
Grant  GP-2723. 


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Burt,  W.  H.  1946.  The  mammals  of  Michigan. 
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ation in  the  wolf  Canis  lupus  L.  Evolution  13: 
283-299. 

Kendall,  M.  G.  1951.  The  advanced  theory  of  sta- 
tistics, Vol.  II.  Hafner  House,  New  York.  521  p. 

McCarley,  H.  1962.  The  taxonomic  status  of  wild 
Canis  (Canidae)  in  the  South  Central  United 
States.  The  Southwestern  Naturalist  7:227-235. 

Pocock,  R.  I.  1935.  The  races  of  Canis  lupus.  Proc. 
Zool.  Soc.  London,  part  3:647-686,  2  pis. 


80 


232  Barbara  Lawrence  and  William  H.  Bossert 

Rao,   C.   R.   1952.   Advanced  statistical   methods  in  tute,  xx  -f  636  p.,  illustr. 

biometric  research.  John   Wiley,  New   York.   390  Young,   S.   P.,   and   H.   H.   T.   Jackson.    1951.   The 

p.  clever    coyote.    The    Stackpole    Co.,    Harrisburg, 

Young,  S.  P.,  and  E.  A.  Goldman.  1944.  The  wolves  Pa.,    and    The    Wildlife    Management    Institute, 

of  North  America.  The  American  Wildlife  Insti-  Washington,  D.  C.  xv  -\-  411  p.,  illustr. 


81 


CHROMOSOME  STUDIES  OF  POCKET  GOPHERS, 

GENUS  THOMOMYS.     I.     THE  SPECIFIC  STATUS  OF 

THOMOMYS  UMBRINUS  (RICHARDSON)  IN  ARIZONA 

James  L.  Patton  and  Ross  E.  Dingman 

Abstract. — The  complexities  of  morphology  and,  hence,  taxonomy  of  pocket 
gophers  (genus  Thomomtjs)  in  southern  Arizona  are  reflected  by  extreme 
interpopulation  chromosomal  variation  in  both  T.  hottae  ( 2n  =  76 )  and  T. 
umhrinus  (2n  =  78).  The  variation  consists  of  differing  numbers  of  morpho- 
logical types  of  chromosomes  for  nearly  each  population  karyotype.  The  known 
range  of  variation  in  either  species  is  less  than  the  amount  of  difference  between 
the  two.  A  somewhat  strict  ecological  separation  exists  between  T.  hottae  and 
T.  umbrinus  in  areas  of  sympatry  or  near  sympatry,  with  the  former  preferring 
the  more  friable  soils  of  the  valley  floors  and  mountain  tops  and  the  latter 
confined  to  the  indurate  soils  of  the  oak  zones  at  intermediate  elevations. 
Chromosomal  and  ecological  concordance  support  the  interpretation  that  T. 
hottae  and  T.  umhrinus  are  distinct  species.  Limited  hybridization  between  the 
two  species  at  one  locality  of  sympatric  contact,  however,   is  known. 

The  taxonomy  of  Thomomys  umbrinus  (Richardson)  has  been  the  subject 
of  considerable  confusion  in  recent  years.  This  problem  centers  primarily 
around  isolated  gopher  populations  inhabiting  montane  woodlands  in  south- 
eastern Arizona.  These  gophers  have  been  allocated  to  three  subspecies  of 
T.  umbrinus  by  Goldman  ( 1947 )  and  to  two  subspecies  by  Cockrum  ( 1960 ) . 
Lange  ( 1959 )  also  recognized  only  two  subspecies  but  used  a  different 
combination  of  names  than  did  Cockrum  ( 1960 ) .  We  follow  this  latter 
interpretation  and  recognize  T.  u.  intermedins  Mearns  as  occurring  in  the 
Santa  Rita,  Patagonia,  and  Huachuca  mountains,  and  T.  u.  quercinus  Burt 
and  Campbell  as  occurring  in  the  Pajarito  Mountains. 

Hoffmeister  and  Goodpaster  (1954:95)  felt  that  ".  .  .  perhaps  in  all  of 
southern  Arizona,  gophers  regarded  as  T.  umbrinus  by  Goldman  ( 1947 )  are 
best  referred  to  T.  bottae."  This  was  finalized  with  their  arrangement  of  T. 
burti  proximus  Burt  and  Campbell  ( =  T.  umbrinus  proximus  auct. )  as  a 
synonym  of  T.  bottae  hueyi  Goldman.  On  the  basis  of  this  interpretation,  Hall 
and  Kelson  (1959)  regarded  all  populations  of  T.  umbrinus  and  T.  bottae 
as  conspecific.  Subsequently,  Lange  ( 1959 )  and  Anderson  ( 1966 )  have 
recorded  sympatry  or  near  sympatry  for  some  populations  of  T.  bottae  and 
T.  umbrinus,  and  Hoffmeister  ( 1963 )  has  revised  his  opinion  of  1954  and 
implied  that  the  populations   of  T.    umbrinus  in   the   Huachuca,   Patagonia, 


82 


2  JOURNAL  OP^  MAMMALOGY  Vol.  49,  No.  1 

and  Pajarito  mountains  of  southern  Arizona  are  not  conspecific  with  T.  bottae. 

As  recognized  here,  T.  umbrinus  {sensu  stricto)  is  essentially  limited  to 
the  Mexican  Plateau  (see  Anderson,  1966)  whereas  T.  bottae  has  a  more 
northern  and  western  distribution  including  most  of  the  southwestern  United 
States  and  northwestern  Mexico.  The  two  species  are  sympatric,  or  nearly  so, 
in  at  least  six  localities,  all  in  the  extreme  northwestern  part  of  the  range  of 
T.  umbrinus  (i.e.,  the  Pajarito,  Patagonia,  Santa  Rita,  and  Huachuca  mountains 
of  Arizona,  the  Animas  Mountains  of  New  Mexico,  and  the  Sierra  de  la 
Breiia  of  northwestern  Chihuahua).  In  the  first  five  of  these  areas,  T. 
umbrinus  occurs  as  "insular"  populations,  surrounded  by  intervening  popula- 
tions of  T.  bottae. 

The  systematic  status  of  the  Arizona  populations  has  been  a  difficult 
problem  to  approach  by  use  of  conventional  characters,  and  it  still  remains 
the  subject  of  considerable  debate.  Many  authors  (Baker,  1953;  Hoffmeister 
and  Goodpaster,  1954;  Lange,  1957;  and  Anderson,  1966)  have  pointed  out 
the  lack  of  a  single,  definable  character  that  can  be  used  consistently  to 
separate  T.  umbrinus  from  T.  bottae  throughout  the  areas  of  sympatry  or 
near  sympatry.  The  karyotypic  analysis  reported  herein  may  supply  such  a 
"diagnostic  character,"  for  in  studies  thus  far  conducted  consistent  differences 
exist  between  T.  umbrinus  and  T.  bottae  in  Arizona. 

Chromosomal  characters  in  the  future  will  aid  in  the  "purification"  of 
samples  so  that  other  characters,  including  standard  morphological  ones, 
may  be  better  evaluated,  and  the  ecologic,  geographic,  and  genetic  limits 
of  gopher  populations  more  clearly  ascertained.  At  present,  and  until  such 
"purified"  collections  are  available,  analysis   of  this  type  is   difficult. 

Materials  and  Methods 

The  animals  studied  (N  =  65)  were  trapped  alive  using  traps  designed  by  Howard 
(1952).  Specimens  were  initially  assigned  to  species  on  the  basis  of  pelage  characters 
(see  Goldman,  1947;  Lange,  1957;  Hoffmeister  and  Goodpaster,  1954).  Such  initial 
identification  was  later  substantiated  by  the  karotypes.  Allocations  of  specimens  to 
subspecies  were  based  primarily  on  geography  and  gross  morphology  (Goldman,  1947; 
Hall  and  Kelson,  1959;  Cockrum,  I960;  Lane,  1965).  Conventional  museum  skins  and 
skulls  were  saved  of  all  animals  examined  and  these  are  deposited  in  the  collection  of 
mammals  of  the  Department  of  Biological  Sciences  (Zoology),  University  of  Arizona, 
Tucson.  See  the  list  of  specimens  examined  below  for  museum  catalogue  numbers  and 
localities. 

Karyotype  anulysis. — Metaphase  chromosomes  of  bone  marrow  cells  were  analyzed 
using  the  in  vivo  colchicine-hypotonic  citrate  sequence  described  elsewhere  (Patton,  1967). 
For  the  present  analysis,  the  preparation  of  karyotypes  from  photomicrographs  was  based 
on  the  number  of  biarmed  (metacentric,  submetacentric,  and  subtelocentric )  and  uniarmed 
(acrocentric  or  telocentric)  autosomes  present  in  the  complement,  and  on  the  morphology 
of  the  X-chromosome. 

Sampling  procedure. — Interpopulation  variation  was  analyzed  by  comparing  16  popula- 
tions of  gophers  in  Arizona,  13  of  T.  bottae  and  three  of  T.  umbrinus  (see  Fig.  1). 
Intrapopulation  variation  was  assessed  by  examining  at  least  two  individuals  from  all 
but  one  population  sampled.    The  largest  samples  from  a  single  population  of  both  species 


83 


February  1968     PATTON  AND  DINGMAN— CHROMOSOMES  OF  THOMOMYS 


\i)    Affs. 


10 


20    MILES 


Nogoles 


Fig.   1. — Map   of   southeastern    Arizona    showing   locaHties    of    gophers    analyzed    (soHd 
circles  =  T.   hottae;   solid   triangles  =  T.    iiinhrinus);    5000-ft   contour   line    shown. 


were  16  T.  iimbrinus  and  11  T.  hottae,  both  from  the  Patagonia  Mountains.  These 
represent  the  most  critical  samples  in  the  present  analysis.  Although  the  samples  are 
relatively  small,  they  do  indicate  no  chromosomal  variation  within  any  single  population. 

Results 

Extensive  variation  in  the  chromosomal  complements  between  populations 
of  T.  hottae  {i.e.,  subspecies  or  demes)  and  slight  variation  between  popula- 
tions of  T.  umhrinus  was  found.  No  intrapopulation  variation  was  found  in 
either  species. 


(} 


X  X 


}i  Si  i-i  A*  h^ 

Fig.   2. — Karyotype   of   Thonwrmjs  hottae   modicus   Goldman    ($,    UA    14992).     Yerba 
Buena  Ranch,  Santa  Cruz  Co.,  Arizona. 


84 


JOURNAL  OF  MAMMALOGY 


Vol.  49,  No.  1 


Table    L — Siininuiry    of    kdnjottjpic    variation    in    i)oi)ulation.s    of    Thomomys    bottae    in 

.wuihcrn  Arizona. 


Subspecies 


d 


Locality 


Number  of 
acrocentrics 


Morphology 

of  X-chromo- 

some* 


V. 

b. 

alicnus 

- 

1 

St.   David,  San   Pedro 
River,   Cochise   County 

9 

pairs 

ST** 

T. 

h. 

coll  inns 

2 

4 

Turkey   Creek   and    Rucker 
tanyons,    Chiricahua    Mts., 
Cochise   Countv 

8 

pairs 

M 

T. 

h. 

collinus 

1 

1 

Rustlers    Park,    Chiricahua 
Mts.,   Cochise   County 

6 

pairs 

M** 

T. 

b. 

ixtciitiatii.i 

1 

1 

Sulfur    Springs    Valley, 
Cochise   County 

8 

pairs 

M 

T. 

b. 

proxinitis 

1 

3 

C'arr   Canyon,    Huachuca 
Mts.,   Cochise   County 

4 

pairs 

SM** 

r. 

b. 

cdtdlinac 

2 

3 

Mt.    Lemnion,    Santa 
Catalina   Mts.   Pima   County 

1 

pair 

SM 

r. 

b. 

iiioclictis 

3 

2 

vie.    Tucson,    Pima    County 

o 

pairs 

ST 

r. 

b. 

niodicus 

4 

7 

Patagonia     Mts.,     Santa 
Cruz   County 

0 

pairs 

SM 

r. 

b. 

inisillus 

1 

1 

Kit   Peak,   Quinlan   Mts., 
Pima  County 

0 

pairs 

SM** 

*    M  =  metacentric;      SM  =  submetacentric;      ST  =  subtelocentric. 
**Indicates  probable  designation   of   X-chromosomes. 

Thomomys  bottae. — Although  all  T.  bottae  studied  to  date  have  a  diploid 
number  of  76  and  a  low  number  of  acrocentric  autosomes,  seven  different 
population  karyotypes  have  been  discovered.  These  populations  differ  in 
the  number  of  acrocentric  chromosomes  and  in  the  morphology  of  the 
X-chromosome  (see  Table  1).  Samples  of  T.  bottae  modicus  Goldman  (Fig. 
2),  with  no  acrocentric  elements  present,  and  of  T.  bottae  aliemis  Goldman 
(Fig.  3),  with  nine  pairs  of  acrocentrics,  represent  the  extremes  of  inter- 
population  chromosomal  variation  known  for  the  species.  This  great  varia- 
tion contrasts  to  chromosomal  variation  known  for  other  mammals,  but  it 
does  parallel  (and  perhaps  correlates  with)  the  great  variation  in  other 
morphological  characters  of  this  species  (see  Goldman,  1947;  Durrant,  1946; 
Hall  and  Davis,  1935).  Indeed,  the  populations  sampled  represent  seven 
different  subspecies  to  some  workers  (see  Hall  and  Kelson,  1959). 

Thomomys  umbrinus. — Populations  of  only  one  of  the  two  subspecies 
recognized  in  Arizona  by  Lange  (1959)  have  been  sampled.   This  subspecies. 

Table    2. — Summary    of    kanjotijpic    variation    in    population-    of    Thomomys    umbrimis 
intermedins  from  the  Santa  Rita  and  Patagonia  mountains,  Arizotm. 


Minute 

Morphology 

of 

Populatior 

1 
Canyon, 

? 

c^ 

M  and  SM* 

ST* 

A* 

chromosomes 

X-chromosome 

\ I adera 

Santa 

Rita  Mts. 

1 

.3 

10 

12 

.54 

6 

ST 

Gardner 

Canyon, 

Santa 

Rita  Mts. 

2 

- 

s 

12 

56 

6 

ST 

Svcamorc  and 

Italiar 

1  canyons, 

6 

10 

10 

10 

56 

6 

ST 

Patagonia  Mts. 

M  =  metacentric;      SM  =  submetacentric;      ST  =  subtelocentric;      A  =  acrocentric. 


85 


February  1968     PATTON  AND  DINCMAN— CHROMOSOMES  OF  THOMOMYS  5 

ii(i  XH  KV)  ^i*« 

Rfi  U  Af)  ftn  XA^MKKis    Hl^ 

?SR  ft?*  Aft  1^^  Mr\  4A  A'^  /»^     x  x 
/\(\  n<\  /^O  00  n(K  f\Q  AO 

Fig.  3. — Karyotype  of  Tlioniomys  bottae  alienus  Goldman  (9,  UA  14989).  About 
4.5  mi  S  St.  David,  San  Pedro  River  Vallev,  Cochise  Co.,  Arizona. 

T.  u.  intermedins  Mearns,  is  represented  by  three  sampled  populations  that 
are  characterized  by  a  diploid  number  of  78,  a  high  number  of  acrocentrics 
in  the  autosomal  complement,  and  the  presence  of  three  pairs  of  minute 
acrocentrics  (these  latter  elements  are  absent  in  all  karyotypes  of  T.  bottae). 
Slightly  different  karyotypes  were  found  for  each  of  these  samples  (see 
Table  2  and  Figs.  4,  5,  and  6).  Again,  the  samples  differ  in  the  number  of 
acrocentrics  and  in  the  relative  number  of  each  type  of  biarmed  chromosomes. 
Unlike  T.  bottae,  the  X-chromosomes  of  all  T.  urnbrinus  are  subtelocentric 
and  do  not  vary  in  morphology. 

The  various  population  karyotypes  of  T.  bottae  have  little  similarity  with 
those  of  T.  urnbrinus.  These  two  species  differ  noticeably  in  the  number 
of  biarmed  and  uniarmed  chromosomes  present  in  their  respective  comple- 
ments (see  Table  3).  From  Table  3  it  is  also  apparent  that  the  total  known 
range  of  variation  within  each  species  is  less  than  the  difference  between 
them. 

T.  bottae  x  T.  urnbrinus  hybrids. — The  number  of  differences  between 
the  karyotypes  of  the  two  species  facilitates  the  determination  of  any  gene 
flow  between  them,  since  hybrids  can  be  readily  detected  by  the  number 
of  acrocentric  chromosomes  present  in  their  complements.  In  the  sample 
of  both  species  from  the  sympatric  locality  in  the  Patagonia   Mountains,   a 

Table  3. — Chromosome  features  of  populations  of  Thomomys  bottae  and  Thomomys 
urnbrinus  in  southern  Arizona,  induding  total  known  range  of  variation  for  each  species. 


Feature  T.   bottae  T.   urnbrinus 


Diploid  number  76  78 

Number  of  metacentrics  and 

submetacentrics  22-32  8-10 

Number  of   subtelocentrics  32-46  10-12 

Number  of  acrocentrics  0-18  54-56 

Number  of  minute  chromosomes  0  6 


86 


JOURNAL  OF  MAMMALOGY 


Vol.  49,  No.  1 


Table  4. — Summary  of  chromosome  features  between  sampled  populations  of  Thomomys 

bottae  niodicus  and  T.  umbrinus  intennedius  from  the  Patagonia  MountainSy  Santa  Cruz 

Co.,  Arizona,  and  of  the  four  proposed  hybrids. 


r.  bottae 

Fi  hybrids 
(UA15158) 

Backcross   hybrids 

Feature 

UA14991 

UA15424 

UA15935 

T.   umbrinus 

Diploid    nunihcr 

76 

77 

76 

76 

77 

78 

Number  of 

metacentrics  and 

32 

21 

31 

33 

16 

10 

submetacentrics 

Number  of 

subtelocentrics 

42 

26 

40 

40 

13 

10 

Number  of 

acrocentrics 

0 

28 

3 

1 

48 

56 

Number  of  minute 

chromosomes 

0 

3 

0 

0 

4 

6 

Morphology  of 

X-chromosome* 

SM 

SM/ST 

? 

p 

? 

ST 

*   SM  =  submetacentric;      ST  =  subtelocentric. 

single  individual  examined  (UA  15158)  possessed  a  diploid  number  of  77, 
and  in  all  aspects  of  the  karyotype  it  was  intermediate  between  the  two 
species  (see  Fig.  7  and  Table  4).  Such  total  intermediacy  when  compared 
to  both  species  karyotypes  from  this  locality  (see  Figs.  2,  6,  and  7)  leaves 
little  doubt  but  that  the  specimen  represents  a  first  generation  hybrid 
between  T.  bottae  and  T.  umbrinus.  The  animal  was  a  pregnant  adult  female 
with  three  nearly  full-term  and  apparently  normal  embryos.  The  hybrid  is 
thus  judged  to  be  fertile,  and  backcrossing  to  either  parental  species  pre- 
sumably occurs,  at  least  to  a  limited  degree. 

«  n  u  «K 

nh  j)j&  a  u  Ah »» (' 

X  Y 

fiA  OA  Oo  on  00  Oft  ocv 

nrt  ftn  nn  no  ao  on  na 

|lf\    An     tx€\     fyi\    H/^    1^^    ^^ 

^(1      4\  ^       Af>      /t^      .#.-        •«'> 

Fig.    4. — Karyotype    of    Thomomys    umbrinus    intermedins    Mearns    {S,    UA    14987). 
Gardner  Canyon,  Santa  Rita  Mts.,  Santa  Cruz  Co.,  Arizona. 


87 


February  1968     PATTON  AND  DINGMAN— CHROMOSOMES  OF  THOMOMYS  7 

X  X 

^^  Aft  Aft  ftO  ^^  ^^ 
^^   HA  A^  Ail  o^  A^ 

'"'ft  ll#\  A^  -^^  ll<l  #v*-» 
AM  A^  A^  ^-^  -*••  «^* 

Fig.    5. — Karyotype    of    Thomomys    umbrinus    intermedins    Mearns    (9,    UA    15343). 
Madera  Canyon,   Santa   Rita  Mts.,   Santa   Cruz   Co.,   Arizona. 


Three  additional  specimens  examined  from  this  population  are  judged 
to  be  backcross  hybrids  on  the  basis  of  the  number  of  acrocentric  elements 
in  their  respective  karyotypes  (Table  4).  Two  of  these  (UA  14991,  9,  and 
UA  15424,  S  )  are  the  probable  results  of  backcrossing  to  parental  T.  hottae, 
and  one  ( UA  15935,  9  )  the  result  of  backcrossing  to  parental  T.  umbrinus. 
A  more  detailed  analysis  of  this  hybridization  is  presently  under  investigation 
and  will  be  presented  in  the  future. 

Discussion 

Ecological  considerations. — Correlated  with  the  karyotypic  distinctness  of 
the  two  species  of  Thomomys  is  a  somewhat  marked  ecological  separation  in 
areas  where  the  two  are  found  in  sympatry  or  near  sympatry.  Thomomys 
umbrinus  was  found  only  in  the  oak  woodland  through  oak-pine  woodland 
in  the  intermediate  elevations  of  the  Santa  Rita  and  Patagonia  mountains. 
These  are  two  of  the  four  mountain  ranges  in  Arizona  where  presumed 
specimens  of  T.  umbrinus  were  reported  by  Cockrum  (1960).  The  other 
two  populations  allocated  to  T.  umbrinus  inhabit  equivalent  habitats  in  the 
Pajarito  and  Huachuca  mountains.  We  have  not  yet  sampled  these  popula- 
tions for  karyotypic  analyses,  but  have  examined  specimens  from  these  areas. 

In  the  Huachuca  Mountains,  specimens  obtained  from  what  could  be 
considered  typical  habitat  for  T.  umbrinus  {i.e.,  oak  woodland)  in  Carr 
Canyon  were  found  to  be  T.  bottae,  referable  to  the  subspecies  T.  b.  proximus 
Burt  and  Campbell.  These  specimens  lack  the  somewhat  distinctive  dark, 
purplish-hued  dorsum  characteristic  of  T.  umbrinus,  and  even  without  karyo- 
types they  would  not  be  confused  with  that  species.  Hoffmeister  and  Good- 
paster  ( 1954 )  correctly  allocated  all  of  the  specimens  they  examined  from 


88 


8  JOURNAL  OF  MAMMALOGY  Vol.  49,  No.  1 


nt 


mumux.   K 


X    Y 


u^th  (^H  A6  ftfi  on  An 

Afi  AA  t\f\   00  r\tk  AA  A/> 

Al*    Aft    ^SifN    An     ti  ft     A/4<»«* 


Fig.  6. — Karyotype  of  Thomomys  timbrimis  intermedins  Mearns  (6,  UA  14990). 
Sycamore  Canyon,  Patagonia  Mts.,  Santa  Cruz  Co.,  Arizona. 

the  Huachuca  Mountains  to  T.  hottae.  However,  they  incorrectly  identified 
the  material  from  Carr  Peak  as  T.  umhrinus  intermedius  Mearns,  and  on  this 
basis,  in  part,  assumed  that  only  T.  hottae  occurred  in  the  mountain  range. 
Lange  (1959)  examined  the  type  of  T.  u.  intermedius  and  considered  this 
name  as  valid  and  specifically  distinct  from  the  Carr  Peak  material  examined 
by  Hoffmeister  and  Goodpaster.  Moreover,  both  Lange  ( 1959 )  and  Cockrum 
(1960)  consider  specimens  from  Brown  Canyon  and  the  vicinity  of  Panama 
Mine  (near  the  west  gate  of  Fort  Huachuca)  as  T.  umhrinus.  Specimens 
examined  by  one  of  us  (JLP)  through  the  courtesy  of  Dr.  Seth  B.  Benson 
from  the  Peterson  Ranch,  Sunnyside  Canyon,  definitely  are  referable  to 
this  species.  Thomomys  umhrinus  is  unquestionably  present  in  the  Huachuca 
Mountains,  therefore,  but  additional  specimens  must  be  collected  and  karyo- 
typed to  enable  assessment  of  their  ecological  as  well  as  genetical  relation- 
ships to  T.  hottae  in  this  same  mountain  range. 

Thomomys  hottae  is  not  known  from  the  higher  elevations  of  the  Patagonia 
and  Santa  Rita  mountains,  although  the  latter  supports  well-developed  pine 
forests  similar  to  those  occupied  by  T.  hottae  on  more  northern  mountains 
in  Arizona  as  well  as  the  adjacent  Huachuca  Mountains. 

Gophers  occurring  in  oak  woodland  habitats  in  other  mountain  ranges  in 
southern  Arizona,  namely  the  Santa  Catalina,  Quinlan,  and  Chiricahua 
mountains,  have  karyotypes  identical  or  similar  to  those  of  nearby  popula- 
tions of  T.  hottae.  These  animals  have  been  considered  to  be  T.  hottae  and 
not  T.  umhrinus  by  most  authors. 

The  ecological  separation  of  the  two  species  is  quite  apparent  in  Sycamore 
and  Italian  canyons  of  the  Patagonia  Mountains.  Generally,  samples  of  T. 
hottae  were  obtained  only  at  lower  elevations  in  desert  grassland  or  riparian 


89 


February  1968     PATTON  AND  DINGMAN— CHROMOSOMES  OF  THOMOMYS 

kit*'  «**•••«• 


Fig.  7. — Karyotype  of  Fi  hybrid  between  T.  bottae  modicus  and  T.  umbrinus  inter- 
medius  (9,  UA  15158).  The  proposed  parental  genomes  are  separated,  with  that 
of  r.  bottae  on  the  left  and  that  of  T.  umbrinus  on  the  right. 

habitats  (3600^800  ft),  while  T.  umbrinus  was  found  in  open  oak  or  juniper- 
oak  woodlands  (4500-6000  ft).  Unlike  the  spatial  separation  of  T.  bottae 
and  T.  umbrinus  at  two  localities  in  northwestern  Chihuahua  (Anderson, 
1966),  the  two  species  are  sympatric  along  a  narrow  zone  in  the  flat  ground 
bordering  the  stream  beds  of  Sycamore  and  Italian  canyons  {ca.  4400-4850 
ft;  see  Fig.  8).  The  floors  of  the  canyons  in  this  area  consist  of  a  mesquite- 
desert  willow-grassland  association  with  a  few  riparian  elements  {e.g.,  cotton- 
woods  and  sycamores)  in  Sycamore  Canyon  and  a  narrow  desert  riparian 
woodland  community  in  Italian  Canyon.  Although  both  species  were  trapped 
on  the  canyon  floors  in  such  communities,  T.  umbrinus  appears  more  limited 
to  the  open,  rockier  hillsides  where  Emory  and  Mexican  blue  oaks  {Quercus 
emoryi  and  Q.  oblongifoUa)  predominate. 

Hijbridization. — At  present,  little  more  than  speculative  remarks  can  be 
made  concerning  the  natural  hybridization  between  T.  bottae  and  T.  umbrinus 
in  Sycamore  and  Italian  canyons  of  the  Patagonia  Mountains.  The  single  Fi 
hybrid  and  the  three  individuals  considered  by  their  karyotypes  to  be  back- 
cross  hybrids  all  were  trapped  within  the  narrow  zone  of  sympatry  (see  Fig. 
8,  note  localities  of  hybrids),  an  indication  that  the  main  populations  of  both 
species  are  not  affected  to  a  great  extent  by  the  hybridization.  Although  the 
Fi  hybrid  was  fertile  and  backcrossing  to  both  parental  species  is,  therefore, 
judged  to  occur,  lack  of  extensive  introgression  coupled  with  the  narrowness 
of  the  hybrid  zone  indicates  restricted  gene  flow  between  T.  bottae  and 
T.  umbrinus  at  this  single  locality. 

Historical  considerations. — The  present  distributions  of  many  species  in 
the  inland  Southwest  have  been  explained  in  part  by  the  shifting  climatic 
and  vegetational  events  of  the  late  Pleistocene  (summarized  by  Martin  and 
Mehringer,  1965).  Some  populations  that  were  continuous  during  late  glacial 
to  post-glacial  times  became  disjunct,  and  interconnections  were  formed 
between  other  previously  disjunct  populations.    This  is  apparent  in  the  cases 


90 


10 


JOURNAL  OF  MAMMALOGY 


Vol.  49,  No.  1 


Miles 


Fig.  8. — Map  of  Sycamore  and  Italian  canyons,  Patagonia  Mountains,  Santa  Cruz  Co., 
Arizona,  showing  area  of  sympatric  contact  between  T.  hottae  and  T.  umbrinus  (shaded 
area)  and  locahties  where  gophers  were  trapped  in  relation  to  zone  of  contact.  SoHd  circles 
=  T.  hottae;  solid  triangles  =  T.  umbrinus;  solid  square  =  Fi  hybrid;  half-filled  circles  = 
hybrids  backcrossed  to  T.  bottae;  half-filled  triangle  =  hybrid  backcrossed  to  T.  umbrinus. 
(Additional  specir^ens  of  T.  bottae  were  trapped  from  outside  the  area  indicated  on  map.) 

of  T.  bottae  and  T.  umbrinus.  Their  present  distributional  pattern  with 
"islands"  of  T.  umbrinus  in  a  "sea"  of  T.  bottae,  and  the  increased  contact 
between  the  two  species  in  Recent  times,  have  been  accompanied  by  repro- 
ductive isolating  mechanisms  that  were  inadequate  to  prevent  limited  hybrid- 
ization between  the  two  species  in  the  restricted  area  of  the  Patagonia 
Mountains.  Presumably  this  occurred  as  the  two  species  came  into  contact 
following  changes  in  the  vegetation  in  the  present  area  of  sympatry.  Present 
hybridization  between  other  groups  of  vertebrates  (for  example,  Cnemi- 
dophorus — Zweifel,  1962;  Lowe  and  Wright,  1966)  and  plants  (for  example, 
oaks — Tucker,  1963)  in  the  same  general  area  has  been  attributed  to  these 
factors  also. 

Much  of  the  current  vegetation  between  the  Santa  Rita,  Huachuca,  and 
Patagonia  mountains  is  desert  grassland  with  scattered  oaks  and  mesquites. 
A  more  well-developed  oak  woodland  is  present  between  the  Patagonia  and 
Pajarito  mountains,  following  elevational  contours  into  and  out  of  Sonora. 
If  the  oak  woodland  were  lowered  400  m  during  the  late  Pleistocene  ( Wiscon- 
sin glaciation),  as  suggested  by  Martin  and  Mehringer  (1965),  all  of  these 
ranges  would  have  been  connected  by  well-developed  oak  woodland.  Such 
habitats  appear  ideal  for  T.  umbrinus  in  these  mountain  ranges  today. 


91 


February  1968     PATTON  AND  DIXGMAX— CHROMOSOMES  OF  THOMOMYS         11 

Thomomys  umbrinus  is  presently  widespread  on  the  Mexican  Plateau, 
and  was  once  undoubtedh'  more  widely  spread  in  southern  Arizona.  The 
area  that  T.  umbrinus  now  inhabits  is  known  to  contain  the  greatest  degree 
of  Mexican  floral  influence  anywhere  in  Arizona  ( Marshall,  1957;  Martin, 
1963;  Lowe,  1964);  this  applies  especially  to  the  vegetation  at  the  lower  and 
intermediate  elevations.  The  two  main  factors  contributing  to  the  presently 
isolated  state  of  T.  umbrinus  populations  in  Arizona  were,  then,  the  withdrawal 
of  the  extensive  woodlands  of  the  late  glacial  period  to  their  present  positions 
during  the  past  10,000  years  (Martin  and  Mehringer,  1965),  and  the  spread 
of  r.  bottae  through  the  lower  elevations  in  recently  invaded  desert  scrub 
and  desert  grassland  communities. 

In  areas  where  T.  bottae  is  present  in  the  higher  pine  forests  and  the  lower 
valley  floors  (for  example,  in  the  Huachuca  Mountains).  T.  umbrinus,  so  far 
as  is  known,  is  restricted  to  the  intermediate  elevations  in  the  oak  zones. 
However,  in  mountain  ranges  where  no  T.  bottae  are  found  in  upper  eleva- 
tions (for  example,  in  the  Santa  Rita  Mountains),  T.  umbrinus  inhabits  both 
the  oak  woodland  and  the  pine  forests.  It  is  apparent,  therefore,  that  the 
present  restriction  of  T.  umbrinus  to  the  oak  zone  is  due  in  part  to  dis- 
placement through  inability  to  compete  with  T.  bottae.  In  all  cases  where 
T.  bottae  and  T.  umbrinus  approach  or  meet  in  Arizona,  the  former  occupies 
the  more  friable  soils  of  the  valley  floors  and  mountain  tops,  whereas  T. 
umbrinus  is  restricted  more  to  the  harder  soils  of  the  somewhat  steeply 
inclined  middle  elevations.  Thomomys  bottae  probably  does  not  compete 
with  T.  umbrinus  for  these  somewhat  marginal  habitats,  for  even  in  mountain 
ranges  where  T.  umbrinus  is  absent,  T.  bottae  populations  are  scarce  in  the 
indurate  soils  of  the  oak  zones.  The  ability  of  T.  umbrinus  to  survive  in 
these  habitats  appears  to  have  resulted  in  the  present  spatial  and  ecological 
relationships  of  the  two  species  of  gophers  in  southern  Arizona. 

Taxonomic  conclusions. — A  basic  problem  to  systematics  has  arisen  from 
the  above  discussion — that  is,  whether  to  consider  T.  bottae  and  T.  umbrinus 
in  Arizona  as  distinct  species  that  infrequently  hybridize,  or  to  consider  them 
subspecies  that  intergrade.  At  the  present  time,  it  would  appear  more  im- 
portant not  to  overshadow  the  biological  findings  with  nomenclatorial 
problems.  In  this  respect,  we  judge  that  consideration  of  the  two  forms  as 
distinct  species  is  in  greater  accord  with  the  biological  inferences.  This 
interpretation  allows  for  a  greater  appreciation  and  understanding  of  the 
past  historical  events,  present  distributional  and  ecological  discordance,  and 
great  chromosomal  distinction  between  T.  bottae  and  T.  umbrinus. 

Acknowledgments 

We  are  considerably  grateful  to  Drs.  Sydney  Anderson,  ^^'illiam  B.  Heed,  T.  C.  Hsu, 
and  John  W.  Wright  for  critically  evaluating  the  manuscript.  Special  appreciation  is 
due  Dr.  Wright  for  his  sound  biological  advice  and  for  aid  in  the  field,  to  Dr.  Anderson 
for  clarifying  the  confusion  of  names  apphed  to  the  gophers  of  the  Huachuca  Mountains, 
and  to  Dr.  E.   L.   Cockrvim  for  providing  equipment  and  encouragement   throughout  this 


92 


12  JOURNAL  OF  MAMMALOGY  Vol.  49,  No.  1 

study.    The  field  assistance  of  Robert  J.   Baker,  Charles  Drabek,  and  Oscar  H.   Soule  is 
also  ackno\%ledged. 

Specimens  Examined 

Specimens  prefixed  by  UA  refer  to  those  catalogued  in  the  mammal  collection,  Depart- 
ment of  Biological  Sciences  (Zoology),  University  of  Arizona,  Tucson.  Other  numbers 
refer  to  the  personal  field  catalogue  of  one  of  us   (JLP). 

Thomomys  bottae  catalinae  {2$,  3  9  )• — Arizona.  Pima  Co.:  Snow  Bowl,  Mt.  Lemmon, 
Santa  Catalina  Mts.    (JLP  737);   Bear  Wallow,  Santa  Catalina  Mts.    ( UA   15411-14). 

Thomomys  bottae  modicus  (8$,  9  9). — Arizona.  Pima  Co.:  Tucson  (UA  1.5149-50, 
JLP  688);  Molino  Basin,  Santa  Catalina  Mts.  ( UA  1.5415-16).  Santa  Cruz  Co.:  1.1  mi 
E  Amado  ( UA  15410);  Verba  Buena  Ranch  ( UA  14992,  UA  15144,  UA  15154);  mouth 
of  Italian  Canyon,  Patagonia  Mts.  ( UA  14988,  UA  15409,  UA  15943-44);  Chamberlain 
Tank,  Patagonia  Mts.  (UA  14993,  UA  14906-07);  Sycamore  Canyon,  Patagonia  Mts., 
9.3  mi  E  Jet  Arizona  82  and  Washington  Camp  Road  (UA  15942). 

Thomomys  bottae  extenuatus  (l  $ ,  19). — Arizona.  Cochise  Co.:  0.2  mi  E  Jet 
Arizona  181  and  Turkey  Creek  Canyon  Road,  Sulfur  Springs  Valley  ( UA  15145);  3.9  mi 
E  Jet  Arizona  181  and  Turkey  Creek  Canyon  Road,  Sulfur  Springs  Valley   (UA  15151). 

Thomomys  bottae  collinus  {Z$,  5  9). — Arizona.  Cochise  Co.:  El  Coronado  Ranch, 
West  Turkey  Creek  Canyon,  Chiricahua  Mts.  (UA  15154,  UA  15147);  1.7  mi  E  El 
Coronado  Ranch,  West  Turkey  Creek  Canyon,  Chiricahua  Mts.  (UA  15152,  UA  15148); 
Rucker  Canyon,  Chiricahua  Mts.,  ca.  5600  ft  (UA  15146,  UA  15153);  1  mi  below  Rustlers 
Park,  Chiricahua  Mts.    (UA  15406-07). 

Thomomys  bottae  proximus  (1$,  3  9). — Arizona.  Cochise  Co.:  Carr  Canyon  Ranch, 
Huachuca  Mts.  (UA  15404-05);  0.5  mi  N  Clark  Spring,  Carr  Canyon,  Huachuca  Mts. 
(UA  1.5417-18). 

Thomomys  bottae  alienus  (19). — Arizona.  Cochise  Co.:  ca.  4.5  mi  S  St.  David  on 
US  80  (UA  14989). 

Thomomys  bottae  pusillus  (1$,  19)- — Arizona.  Pima  Co.:  ca.  1.5  mi  below  Kit 
Peak  National  Observatory,   Quinlan   Mts.    (UA   15419-20). 

Thomomys  umbrinus  intermedius  {\0 i  ,  12  9). — Arizona.  Santa  Cruz  Co.:  Madera 
Canyon,  Santa  Rita  Mts.  ( UA  15343,  UA  15163,  UA  15403,  UA  15001);  Gardner  Canyon, 
Santa  Rita  Mts.  (UA  14986-87);  Sycamore  Canyon,  Patagonia  Mts.,  ca.  9.9  mi  E  Jet 
Arizona  82  and  Washington  Camp  Road  ( UA  14985 )  and  ca.  9.3  mi  E  Jet  Arizona  82 
and  Washington  Camp  Road  (UA  15937-41);  ca.  1.2  mi  E  Crescent  Spring  (UA  15156, 
UA  15012);  ca.  0.4  mi  E  Crescent  Spring  (UA  15160);  ca.  0.6  mi  E  Crescent  Spring 
(UA  14990);  Crescent  Spring  (UA  15159);  ca.  8.7  mi  E  Jet  Arizona  82  and  Washington 
Camp  Road  (UA  15408);  mouth  of  Italian  Canyon,  Patagonia  Mts.  (UA  15157,  UA  14983); 
Italian  Canyon,  Patagonia  Mts.  (UA  14984,  UA  15936). 

Thomomys  bottae  x  Thomom,ys  umbrinus  hybrids  (15,  3  9). — Arizona.  Santa  Cruz 
Co.:  Italian  Canyon,  Patagonia  Mts.  (UA  15158,  UA  15424);  Sycamore  Canyon,  Patagonia 
Mts.,  ca.  8.7  mi  E  Jet  Arizona  82  and  Washington  Camp  Road  (UA  14991)  and  ca.  9.3 
mi  E  Jet  Arizona  82  and  Washington  Camp  Road  (UA  15935). 

Literature  Cited 

Antjerson,  S.     1966.     Taxonomy  of  gophers,  especially  Thomomys,  in  Chihuahua,  Mexico. 

Syst.  Zool.,  15:   189-198. 
Baker,    R.    H.     1953.     The    pocket    gophers    ( genus    Thomomys )    of    Coahuila,    Mexico. 

Univ.  Kansas  Publ.,  Mus.  Nat.  Hist.,  5:  499-514. 
CocKRUM,  E.  L.     1960.     The  Recent  mammals  of  Arizona.    Univ.  Arizona  Press,  Tucson, 

vii  -^-  276  pp. 


93 


February  1968     PATTON  AND  DINGMAN— CHROMOSOMES  OF  THOMOMYS         13 

DuRRANT,  S.  D.     1946.     The  pocket  gophers  (genus  Thomomys)  of  Utah.    Univ.  Kansas 

Publ,  Mus.  Nat.  Hist.,  1:   1-82. 
Goldman,  E.  A.     1947.     The  pocket  gophers  (genus  Thomomys)  of  Arizona.    N.  Anier. 

Fauna,  59:    1-39. 
Hall,  E.  R.,  and  W.  B.  Davis.     1935.     Geographic  distribution  of  pocket  gophers  (genus 

Thomomys)   in  Nevada.    Univ.  Cahfornia  Publ.  Zool.,  40:    387-402. 
Hall,  E.  R.,  and  K.  R.  Kelson.     1959.     The  mammals  of  North  America.    Ronald  Press, 

New  York,  1:  xxx  +  546  +  79. 
HoFFMEisTER,    D.    F.     1963.     The  yellow-nosed   cotton    rat,    Sigmodon    ochrognathus,    in 

Arizona.    Amer.  Midland  Nat.,  70:  429-441. 
HoFFMEiSTER,  D.  F.,  AND  W.  W.  GooDPASTER.     1954.     The  mammals  of  the  Huachuca 

Mountains,  southeastern  Arizona.    iHinois  Biol.  Monogr.,  24:    v   -f    1-152. 
Howard,  W.  E.     1952.     A  live  trap  for  pocket  gophers.    J.  Mamm.,  33:   61-65. 
Lane,  J.  D.     1965.     Taxonomy  of  the  pocket  gopher,  Thomomys  haileyi.    Ph.D.  disserta- 
tion, Univ.  Arizona,  Tucson.  80  pp. 
Lange,  K.  I.     1957.     Taxonomy  and  distribution  of  pocket  gophers    (genus  Thomomys) 

in  southeastern  Arizona.    M.S.  thesis,  Univ.  Arizona,  Tucson.    68  pp. 
.     1959.     Taxonomy  and  nomenclature  of  some  pocket   gophers  from  southeastern 

Arizona.    Proc.   Biol.  Soc.  Washington,  72:    127-132. 
Lowe,   C.   H.      1964.     The  vertebrates   of  Arizona.     Univ.    Arizona   Press,   Tucson,   vii    + 

259  pp. 
Lowe,    C.    H.,    and    J.    W.    Wright.     1966.     Evolution    of    parthenogenetic    species    of 

Cnemidophorus  (whiptail  lizards)  in  western  North  America.    J.  Arizona  Acad. 

Sci.,  4:   81-87. 
Marshall,  J.  T.,  Jr.     1957.     Birds  of  the  pine-oak  woodland   in  southern   Arizona  and 

adjacent  Mexico.    Pacific  Coast  Avifauna,   32:    1-125. 
Martin,  P.   S.     1963.       The  last   10,000  years,   a   fossil  pollen   record   of  the   American 

Southwest.    Univ.  Arizona  Press,  Tucson,  87  pp. 
Martin,  P.   S.,   and  P.  J.   Mehringer,   Jr.     1965.     Pleistocene   pollen   analysis   and   bio- 
geography  of  the  Southwest.    Pp.  433-451,  in  The  Quaternary  of  the  United 

States    (H.   E.  Wright  and  D.   G.    Frey,   eds.).    Princeton   Univ.    Press,    New 

Jersey. 
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(Rodentia:   Heteromyidae ) .    J.   Mamm.,  48:    27-37. 
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Department  of  Biological  Sciences,  University  of  Arizona,  Tucson,  85721,  and  Depart- 
ment of  Biology,  University  of  San  Diego,  San  Diego,  California  92110.  Accepted  30 
October  1967. 


94 


Comp.  Biochem.  Physiol.,  1966,  Vol.  18,  pp.  639  to  651.  Pergamon  Press  Ltd.  Printed  in  Great  Britain 

SERUM  PROTEIN  ELECTROPHORESIS  IN  THE 

TAXONOMY  OF  SOME  SPECIES  OF  THE  GROUND 

SQUIRREL  SUBGENUS  SPERMOPHILUS* 

CHARLES  F.  NADLER  and  CHARLES  E.  HUGHES 

Department  of  Medicine,  Northwestern  University  Medical  School, 

Chicago,  Illinois 

{Received  IS  January  1966) 

Abstract — 1.  Serum  protein  patterns  of  Spermophilus  undulatus,  Spermophilus 
columbianiis  and  Spermophilus  beldingi  were  analyzed  by  two-dimensional 
starch-gel  electrophoresis. 

2.  The  patterns,  although  generally  similar,  exhibited  variation  in  nine 
fractions  or  groups  of  fractions  and  these  fractions  had  taxonomic  significance 
at  the  level  of  population,  subspecies  or  species.  Intraspecific  variability  of  two 
unidentified  protein  fractions  was  observed  in  S.  undulatus  kennicotti  and  S. 
beldingi  and  a  third  protein  polymorphism  involving  transferrin  was  also 
observed  in  S.  undulatus  kennicotti.  Intraspecific  divergence  between  Arctic 
and  sub-Arctic  subspecies  of  S.  undulatus  was  found  and  proteins  from  the 
latter  show  a  closer  resemblance  to  S.  columbianus . 

3.  The  protein  characters  support  present  taxonomic  concepts  of  the  species 
of  Spermophilus  that  indicate  a  close  relationship  between  all  three  species  and  a 
closer  relationship  between  S.  undulatus  and  S.  columbianus. 

4.  Protein  characters,  as  observed  in  the  genus  Spermophilus,  appear  to 
offer  great  promise  as  a  method  for  systematic  investigation  at  intraspecific 
levels  where  gross  morphologic  characters  are  least  definitive. 

INTRODUCTION 
The  concept  that  protein  synthesis  is  dependent  on  rigid  genetic  control  and  is 
therefore  a  reflection  of  the  genotype  has  provided  a  sound  theoretical  basis  for 
utilizing  physico-chemical  characteristics  of  proteins  in  taxonomic  studies.  Among 
the  simpler  and  more  reliable  techniques  for  study  of  serum  protein  fractions  are 
paper  electrophoresis  and  starch-gel  electrophoresis.  The  more  recent  use  of 
starch-gel  electrophoresis  provides  an  increased  resolving  power  that  results  in 
patterns  containing  as  many  as  thirty  protein  fractions  in  some  human  sera 
(Smithies,  1959),  in  comparison  to  the  usual  five  fractions  observed  with  paper 
electrophoresis. 

Many  different  vertebrates  including  primates  (Goodman,  1963)  and  Rodentia 
(Blumberg  et  al.,  1960)  of  the  class  Mammalia,  Reptilia  and  Amphibia  (Dessauer 
et  al.,  1962)  and  fishes  (Sanders,  1964)  have  been  investigated  with  electrophoretic 
techniques  and  the  data  applied  to  the  taxonomy  of  groups  within  the  respective 

*  This  investigation  was  supported  by  National  Science  Foundation  Grant  GB-3251. 

639 


95 


640  Charles  F.  Nadler  and  Charles  E.  Hughes 

classes.  In  their  excellent  review,  Dessauer  and  Fox  (1964)  concluded  that  starch- 
gel  electrophoresis  showed  greatest  taxonomic  promise  at  infraspecific  and  specific 
levels  where  the  probability  was  high  that  proteins  of  identical  mobility  had 
identical  structure.  Certain  proteins  have  been  demonstrated  to  be  polymorphic 
within  a  species  and  under  genetic  control.  In  the  case  of  transferrin,  which  binds 
serum  iron,  gene  frequencies  can  be  calculated  and  successfully  used  to  evaluate 
species  and  population  relationships  (Goodman  et  al.,  1965). 

In  the  present  investigation  the  serum  proteins  of  Spermophilus  undulatus, 
Spermophilus  columbianus  and  Spermophilus  beldingi  were  analyzed  by  two- 
dimensional  starch-gel  electrophoresis  (Poulik  &  Smithies,  1958).  These  species 
constitute  three  of  the  eight  species  presently  classified  in  the  ground  squirrel 
subgenus  Spermophilus  (Hall  &  Kelson,  1959)  and  they  are  of  taxonomic  interest  for 
several  reasons.  First,  Spermophilus  is  considered  the  most  specialized  of  the 
ground  squirrel  subgenera  (Bryant,  1945)  and  most  recently  evolved  (Black,  1963) 
yet  there  is  a  paucity  of  gross  morphological  characters  for  convincing  definition 
of  interspecific  relationships.  Second,  other  lines  of  evidence  have  been  applied 
to  the  latter  problems  that  have  yielded  differing  conclusions;  zoogeographic 
evidence  (Rand,  1954;  MacPherson,  1965)  and  host-parasite  observations  (Holland, 
1958)  indicate  a  close  affinity  between  S.  undulatus  and  S.  columbianus  whereas 
chromosomal  evidence  (Nadler,  1963,  1966)  suggests  an  equal  degree  of  divergence 
between  S.  undulatus,  S.  columbianus  and  S.  beldingi.  Because  introducing  evidence 
from  additional  characters  might  resolve  these  interspecific  problems,  the  present 
study  was  undertaken  with  the  following  aims: 

(1)  to  determine  whether  the  number  and  mobilities  of  fractions  comprising 
the  total  serum  protein  pattern  can  be  analyzed  to  yield  reliable  taxonomic  charac- 
ters; (2)  to  determine  the  appropriate  taxonomic  level  at  which  the  protein 
characters  are  applicable;  and  (3)  to  test  the  validity  of  these  characters  by  correlat- 
ing and  comparing  them  with  known  systematic  data  of  Spermophilus. 

MATERIALS  AND  METHODS 

Serum  was  obtained  from  the  following  animals : 

Spermophilus  undulatus  kennicotti  (Ross).  Alaska:  30  miles  E.  of  Anaktuvuk 
Pass,  9  males  and  5  females;  6  miles  E.  of  Anaktuvuk  Pass,  15  males  and  7  females. 

Spermophilus  undulatus  kodiacensis  (Allen).  Alaska:  Kodiak  Island,  1  male  and 
2  females. 

Spermophilus  beldingi  crebrus  (Hall).  Idaho:  Twin  Falls  Co.;  10  miles  N.W.  of 
Buhl,  3  males  and  3  females. 

Spermophilus  beldingi  oregonus  (Merriam).  Oregon:  Harney  Co.;  Malheur 
Valley,  2  males  and  1  female ;  Burns,  6  males  and  4  females. 

Spermophilus  columbianus  columbianus  (Ord).  Idaho:  Adams  Co.;  Brundage 
Mountain,  4  males  and  10  females. 

Blood  was  drawn  from  the  heart  using  sterile  equipment  and  the  serum  was 
stored  at  4°C.  Serum  proteins  were  analyzed  using  a  technique  for  horizontal,  two- 
dimensional,  starch-gel  electrophoresis  (Poulik  &  Smithies,  1958)  combined  with  a 


96 


SERUM  PROTEIN  PATTERNS  OF  THE  GROUND  SQUIRREL  641 

tris-discontinuous  buffer  system  (Poulik,  1957).  The  procedure  was  modified  as 
reported  by  Goodman  (1963).  Starch  blocks  were  bisected,  stained  with  Nigrosin 
for  2-5  min  (1  g  Nigrosin,  30  cc  acetic  acid,  135  cc  methyl  alcohol  and  135  cc 
distilled  water)  and  decolorized  for  24  hr  using  the  same  solution  without  the  dye. 
Two  to  three  separations  of  each  serum  specimen  were  performed  on  different  days 
and  all  runs  were  carefully  compared  before  recording  the  protein  pattern  of  an 
individual  animal  as  a  scale  indian  ink  drawing.  Fractions  with  staining  density 
equal  to  albumin  or  transferrin  were  recorded  in  black,  those  with  faint  staining 
reaction  were  drawn  with  open  lines  and  fractions  of  intermediate  intensity  were 
stippled.  When  question  arose  regarding  the  presence  or  absence  of  a  given 
fraction,  additional  runs  were  made  to  clarify  the  problem. 

The  densely  staining  fraction  with  fastest  mobility  on  paper  and  starch  is 
tentatively  labeled  albumin  and  the  fraction  with  slowest  migration  rate  is  labeled 
gamma  globulin.  Transferrins  {Tf)  were  identified  in  several  animals  of  each 
species  by  Fe^^  radioautography  (Smithies,  1959).  Transferrin  was  investigated 
at  the  interspecific  level  by  simultaneously  running  serum  samples  from  each 
species  in  one-dimensional  starch-gel  separations. 

RESULTS 

The  serum  protein  patterns  of  S.  undulatus,  S.  columbianus  and  S.  beldingi  show 

an  overall  similarity  in  the  number  of  protein  fractions  and  their  respective 

mobilities  (Figs.  2-8).  However,  a  careful  comparison  shows  nine  major  differences, 

illustrated  in  Fig.  1,  that  are  exhibited  in  one  or  more  species  or  populations  and 

Alb 

<£-3    *""    A 


Fig.  1.  A  hypothetical  separation  of  ground  squirrel  serum  proteins  illustrating 
fractions  with  taxonomic  significance.  The  inital  separation  on  paper  results  in  a 
horizontal  separation  from  left  to  right,  followed  by  starch-gel  electrophoresis 
which  produces  a  vertical  separation.  The  labeled  fractions  correspond  with  the 
following  characters:  Albumin  (Character  I),  Fraction  Group  A  (II),  Fraction 
B  (IV),  Fraction  C  (V),  Transferrin  or  T/(III),  Fraction  D  (VI),  Fraction  E  (VII) 
and  Fraction  F  (VIII).  The  number  of  arc-like  fractions  constitute  Character  IX. 
Gamma  globulin,  y,  has  the  slowest  mobility  on  both  paper  and  starch. 


22 


97 


642  Charles  F.  Nadler  and  Charles  E.  Hughes 

they  may  be  evaluated  as  possible  taxonomic  characters.  Other  differences  in  the 
protein  patterns  were  observed  in  some  of  the  figures,  but  were  inconsistent  or 
difficult  to  evaluate  because  of  faint  staining  properties.  Because  fractions  other 
than  transferrin  were  not  characterized  with  regard  to  chemical  structure  or 
function,  they  are  given  a  letter  designation  from  A  through  F.  It  is  recognized 
that  similarity  in  mobility  and  configuration,  as  determined  by  a  single  technique, 
does  not  necessarily  indicate  identical  chemical  structure  and  it  should  be  emphas- 
ized that  no  individual  studied  contained  all  nine  characters. 


*is:i 


Fig.  2.  A  protein  pattern  from  S.  undulatus  kemiicotti  (30  mile  population).  The 
albumin  is  homogeneous.  Fraction  Group  A  contains  four  fractions;  Fractions  B 
and  C  are  both  present;  two  transferrins  are  present;  Fractions  D  and  E  are 
absent;  and  Fraction  Group  F  is  not  separated.    One  arc  fraction  is  observed. 

For  clarity,  the  nine  protein  characters  observed  in  S.  undulatus,  S.  columbianus 
and  S.  heldingi  will  be  described  individually  and  later  comparisons  made  between 
taxa.    The  same  data  are  presented  in  tabular  form  for  each  species  in  Table  1. 

Character  I.  This  character  consists  of  the  presence  or  absence  of  a  homogene- 
ous serum  albumin  fraction.  S.  undulatus  (Figs.  2-6)  and  S.  beldingi  (Fig.  8)  have  a 
homogeneous  serum  albumin  while  S.  columbianus  (Fig.  7)  showed  an  indication  of 
two  fractions  migrating  with  nearly  identical  mobilities  on  starch. 

Character  II.  This  character,  designated  Fraction  Group  A,  is  composed  of 
three  to  four  fractions  that  migrate  slightly  slower  than  albumin  (Fig.  1).  Both 
populations  of  S.  undulatus  kennicotti  are  characterized  by  Fraction  A  containing 
four  individual  fractions  having  an  identical  group  configuration  (Figs.  2,  3,  4,  5). 
In  contrast,  S.  undulatus  kodiacensis  has  only  three  fractions  and  these  assumed  a 
different  configuration  (Fig.  6).  This  pattern  seen  in  S.  undulatus  kodiacensis  is 
found  to  be  identical  to  Fraction  Group  A  in  S.  columbianus  (Fig.  7).  Fraction 
Group  A  of  S.  beldingi  (Fig.  8)  contains  three  fractions  that  exhibit  a  configuration 
different  from  the  other  taxa.  Therefore,  Character  II  shows  both  interspecific 
and  intraspecific  variability  without  individual  variation. 


98 


SERUM  PROTEIN  PATTERNS  OF  THE  GROUND  SQUIRREL 


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Charles  F.  Nadler  and  Charles  E.  Hughes 


Character  ///consists  of  the  number  of  transferrin  fractions  and  their  mobilities 
(Fig.  1).  The  population  of  S.  undulatus  kennicotti  from  30  miles  E.  of  Anaktuvuk 
Pass  is  polymorphic  with  respect  to  transferrin  because  8  of  14  animals  have  two 
darkly  staining  bands  with  nearly  identical  mobility  (Figs.  2,  3),  both  of  which 


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^ 


Fig.  3.  A  protein  pattern  from  S.  undulatus  kennicotti  (30  mile  population).   This 
animal  differs  from  the  animal  in  Fig.  2  by  an  absence  of  Fractions  B  and  C.  Two 
transferrins  are  present.   Fraction  Group  F  is  continuous. 


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Fig.  4.  A  protein  pattern  from  S.  undulatus  kennicotti  (30  mile  population).   This 

specimen  lacks  Fraction  B,  but  Fraction  C  is  present  and  only  one  transferrin  {Tf) 

is  observed.    Note  the  absence  of  a  separation  within  Fraction  Group  F. 

bind  Fe^^.  At  present,  the  slower  fraction  is  designated  as  a  second  molecular 
form  of  transferrin.  The  population  of  S.  undulatus  kennicotti  from  6  miles  E.  of 
Anaktuvuk  Pass  is  homogeneous  with  respect  to  transferrin,  and  only  one  fraction, 
migrating  with  a  mobihty  identical  to  the  faster  fraction  from  the  30  mile  population, 


100 


SERUM  PROTEIN  PATTERNS  OF  THE  GROUND  SQUIRREL 


645 


is  observed  in  each  of  the  22  animals  (Fig.  5).  On  the  basis  of  the  transferrin 
polymorphism  it  is  possible,  when  the  populations  are  considered  as  a  whole,  to 
differentiate  the  two  by  this  character. 


Fig.  5.  A  protein  pattern  from  S.  undulatus  kennicotti  (6  mile  population).  Fraction 

B  is  absent  which  is  characteristic  of  all  specimens  from  the  6  mile  population.  A 

single  transferrin  {Tf)  is  present.     Fraction  F  is  continuous. 


O 


Fig.  6.  A  protein  pattern  from  S.  undulatus  kodiacensis.  Fraction  Group  A 
contains  three  fractions  with  a  configuration  similar  to  S.  columbianus  (Fig.  7).  Frac- 
tions B  and  C  are  present  and  a  single  transferrin  (77)  with  a  mobility  identical  to 
the  faster  fraction  of  5.  undulatus  kennicotti  is  observed.  A  darkly  staining  Fraction 
D  is  present  whereas  Fraction  E  is  absent.    The  two  fractions  comprising  F  are 

separated. 

All  3  specimens  of  S.  undulatus  kodiacensis  (Fig.  6)  have  a  single  transferrin 
fraction  that  migrates  at  the  same  rate  as  the  faster  transferrin  of  both  population 
samples  of  S.  undulatus  kennicotti,  which  suggests  a  common  relationship  between 
the  three  populations  studied. 


101 


646  Charles  F.  Nadler  and  Charles  E.  Hughes 

S.  columbianus  (Fig.  7)  and  S.  beldingi  (Fig,  8)  each  have  a  single  transferrin 
fraction  and  the  transferrins  of  both  species  have  an  identical  mobility  that  is  faster 
than  the  mobility  of  S.  undulatus  transferrin. 

Character  IV  consists  of  a  single  fraction  that  migrates  slightly  more  slowly, 
on  both  paper  and  starch-gel,  than  the  fastest  arc-like  fraction,  and  it  is  designated 
Fraction  B  (Fig.  1).  It  stains  with  moderate  or  strong  intensity.  Fraction  B  was 
present  in  4  of  the  14  specimens  of  S.  undulatus  kennicotti  (Fig.  2)  from  the  30  mile 
population  and  absent  in  all  animals  from  the  6  mile  population  (Fig.  5). 

Fraction  B  was  present  in  all  3  specimens  of  S.  undulatus  kodiacensis  (Fig.  6), 
8  of  19  specimens  of  S.  beldingi  (Fig.  8)  and  all  10  specimens  of  S.  columbianus 
(Fig.  7). 


Fig.  7.  A  protein  pattern  from  S.  columbianus  columbianus.  The  albumin  is 
notched,  indicating  a  heterogeneous  fraction.  Three  fractions  comprise  Fraction 
Group  A  and  their  configuration  resembles  .S.  undulatus  kodiacensis  (Fig.  6).  Both 
Fractions  B  and  C  are  present  and  a  single  transferrin  {Tf)  migrates  more  rapidly 
than  Fraction  C  and  the  Tf  of  S.  undulatus  (Figs.  2-6).  Fractions  D  and  E  are 
present  and  Fraction  Group  F  is  separated.    Three  arc  fractions  are  observed,  a 

characteristic  feature  of  the  species. 

Character  V.  Fraction  C  constitutes  Character  V,  It  migrates  faster  than 
transferrin,  slower  than  Fraction  B  and  is  located  diagonally  between  the  two 
fractions  on  the  two-dimensional  separation  (Fig.  1).  Staining  intensity  varies 
between  individual  specimens  from  moderate  to  strong. 

Among  specimens  of  S.  undulatus  kennicotti,  from  the  30  mile  population 
Fraction  C  was  observed  in  8  of  14  specimens  (Fig.  2,  4)  and  15  of  22  specimens 
from  the  6  mile  population  (Fig.  5).  All  specimens  of  S.  undulatus  kodiacensis 
(Fig.  6),  S.  columbianus  (Fig.  7)  and  S.  beldingi  (Fig.  8)  had  patterns  containing 
Fraction  C,  and  no  geographic  variation  was  seen. 

Character  VI  is  a  strongly  staining  fraction,  designated  Fraction  D,  that 
migrates  faster  than  gamma  globulin  on  paper  but  slower  in  starch  (Fig.  1).  Frac- 
tion D  is  absent  in  both  populations  of  S.  undulatus  kennicotti  (Figs.  2,  3,  4  and  5) 


102 


SERUM  PROTEIN  PATTERNS  OF  THE  GROUND  SQUIRREL  647 

and  present  in  5.  undulatus  kodiacensis  (Fig.  6),  S.  coliimbianus  (Fig.  7)  and  S. 
beldingi  (Fig.  8).  There  is  no  intrapopulational  variation. 

Character  VII  consists  of  a  small  lightly  or  moderately  staining  fraction, 
Fraction  E,  that  migrates  slightly  faster  than  Fraction  D  on  both  paper  and 
starch-gel  (Fig.  1).  Fraction  D  is  absent  in  both  populations  of  S.  undulatus 
kennicotti  (Figs.  2-5)  and  in  S.  undulatus  kodiacensis  (Fig.  6).  It  is  present  in  S. 
columbianus  (Fig.  7)  and  S.  beldingi  (Fig.  8). 


Fig.  8.  A  protein  pattern  from  5.  beldingi  crebriis.  Fraction  Group  A  contains 
three  fractions  with  different  configuration  from  S.  undulatus  and  S.  columbianus. 
Fractions  B,  C,  D  and  E  are  present.  A  single  transferrin  {Tf)  with  mobility 
more  rapid  than  Fraction  C  and  similar  to  Tf  oi  S.  columbianus  is  present.   Fraction 

Group  F  is  separated. 

Character  VIII  consists  of  two  fractions  that  migrate  more  slowly  than  Fraction 
E  on  starch  but  at  the  same  or  faster  rate  on  paper,  and  they  are  designated  Fraction 
Group  F  (Fig.  1).  The  two  fractions  are  separated  by  a  gap  in  S.  undulatus  kodia- 
censis (Fig.  6),  S.  columbianus  (Fig.  7)  and  S.  beldingi  (Fig.  8)  that  is  produced  by 
more  rapid  migration  of  one  fraction  during  the  initial  paper  run.  Conversely, 
Fraction  Group  F  is  not  separated  by  a  gap  in  either  population  of  S.  undulatus 
kennicotti  (Figs.  2,  3,  4,  5). 

Character  IX.  The  number  of  arc-like  fractions  observed  in  the  protein  pattern 
varies.  S.  undulatus  kennicotti,  S.  undulatus  kodiacensis  and  S.  beldingi  patterns  are 
characterized  by  one  arc  fraction  whereas  S.  columbianus  patterns  (Fig.  7)  contain 
three  arc  fractions. 

DISCUSSION 
The  present  study  demonstrates  that  serum  protein  patterns  from  three  related 
ground  squirrel  species  can  be  analyzed  to  provide  nine  potential  taxonomic 
characters.  The  theoretical  basis  for  the  valid  use  of  proteins  as  characters  rests 
upon  the  assumption  that  they  are  under  genetic  control  and  differences  in  genotype 
will  be  reflected  by  an  alteration  in  chemical  structure  and  behavior.    However, 


103 


648  Charles  F.  Nadler  and  Charles  E.  Hughes 

before  accepting  these  characters  as  rehable  indicators  of  taxonomic  relationships, 
it  is  important  to  attempt  to  exclude  protein  differences  influenced  by  the  stage  of 
development  or  physiologic  state  of  the  animal  (Dessauer  &  Fox,  1964).  In  this 
study,  no  juvenile  or  pregnant  animals  were  studied  and  no  differences  in  pattern 
could  be  attributed  to  the  sex  of  the  animal.  With  respect  to  seasonal  influences, 
S.  undulatus  kodiacensis  specimens  were  obtained  in  late  April  1965,  S.  beldingi 
specimens  were  collected  from  27  May-25  June  1965,  and  S.  columbianus  specimens 
were  collected  on  19  August  1965.  The  two  populations  of  S.  undulatus  kennicotti 
that  showed  the  greatest  intraspecific  variation  in  proteins  were  collected  between 
20-30  August  1965.  Animals  were  not  examined  just  before  or  after  hibernation. 
These  observations,  we  believe,  indicate  that  the  proposed  protein  characters  are 
not  due  to  non-genetic  variation. 

Protein  characters  appear  definitive  at  the  species  level  where  Characters  I,  II, 
III,  VI,  VII,  VIII  and  IX  may  be  used  alone  or  in  combination  (Table  1)  to 
distinguish  individual  species,  and  these  characters  appear  fully  as  diagnostic  as 
such  gross  morphological  characters  as  pelage  color,  size,  etc.  (Howell,  1938). 
Two  taxonomic  conclusions  at  the  species  level  are  suggested  by  the  protein 
characters  derived  from  this  investigation.  First,  S.  undulatus,  S.  beldingi  and  S. 
columbianus  all  show  a  certain  general  similarity  in  their  protein  patterns  that 
suggests  a  common  ancestral  relationship,  although  each  exhibits  a  number  of 
characteristic  features.  5.  beldingi  is  unique  in  its  manifestation  of  Character  II, 
by  a  combination  of  Characters  I  and  IX  it  can  be  distinguished  from  S.  columbian- 
us, and  utilizing  Characters  III  and  VII  it  can  be  distinguished  from  S.  undulatus. 
S.  columbianus  has  two  unique  characters,  I  and  IX,  yet  it  exhibits  a  similarity  and 
presumably  close  relationship  to  S.  beldingi  with  respect  to  Characters  III,  VI,  VII 
and  VIII. 

Second,  it  is  pertinent  that  S.  undulatus  kennicotti  and  S.  undulatus  kodiacensis, 
which  share  a  number  of  characters  that  distinguish  them  from  the  other  species 
(Table  I),  also  differ  with  respect  to  Characters  II,  VI  and  VIII.  In  fact,  these 
latter  characters  suggest  a  close  relationship  between  S.  undulatus  kodiacensis  and 
S.  columbianus  whereas  S.  undulatus  kennicotti  might  be  considered  more  divergent. 
The  validity  of  these  seemingly  paradoxical  observations  receives  support  from 
zoogeographic  and  ectoparasite  studies.  Rand  (1954)  suggests  that  S.  undulatus 
and  S.  columbianus  originated  from  the  same  stock  which  became  separated  by 
continental  glaciation.  One  part  survived  in  the  Beringia  refugium  during  the 
Wisconsin  phase  of  the  Pleistocene  and  differentiated  during  the  separation  to 
become  undulatus  and  the  other  survived  in  a  refugium  south  of  the  ice  and  became 
what  is  now  columbianus.  Holland  (1958)  compared  samples  of  fleas  from  S. 
undulatus  of  Western  Alaska  and  Northern  British  Columbia  with  samples  from  S. 
columbianus  and  regarded  the  fleas  only  weakly  differentiated  at  the  subspecies 
level.  These  observations  suggested  the  ranges  of  the  two  ground  squirrels  were 
at  one  time  contiguous  (Holland,  1963)  and  the  possibility  that  they  evolved  from 
a  single  ancestral  stock  is  also  strongly  suggested  by  protein  data  from  the  present 
study.    MacPherson  (1965)  also  accepts  the  thesis  offered  by  Rand  (1954)  and 


104 


SERUM  PROTEIN  PATTERNS  OF  THE  GROUND  SQUIRREL  649 

supported  by  Holland  (1958).  Therefore,  among  the  three  species  we  have 
examined,  the  kodiacensis  population  of  S.  iindulatus  exhibits  a  closer  degree  of 
relationship  to  5.  columbiamis  than  that  found  between  any  other  two  species. 

Analysis  of  mitotic  chromosomes  from  species  of  the  genus  Spermophilus  has 
provided  evidence  for  an  equal  degree  of  kar^otypic  divergence  between  5. 
beldingi  with  diploid  number  {In)  of  30,  S.  columbianus  2n  =  32  and  S.  undulatus 
with  2n  =  34  (Nadler,  1966).  Comparison  of  their  chromosomes  did  not  suggest 
a  particularly  close  relationship  between  5.  undulatus  and  S.  columbianus  because 
several  relatively  uncommon  types  of  rearrangements  had  to  be  postulated  as  the 
mechanisms  responsible  for  their  kar^'otypic  divergence.  The  chromosome  data 
might  be  interpreted  to  indicate  that  the  two  species  diverged  less  recently  than 
other  lines  of  evidence  suggest,  but  it  is  generally  recognized  that  no  one  line  of  evi- 
dence invariably  provides  unequivocal  evidence  for  satisfying  taxonomic  decisions. 

The  subspecific  divergence  between  S.  undulatus  kennicotti  and  S.  undulatus 
kodiacensis,  which  is  suggested  by  protein  Characters  II,  VI  and  VIII,  correlates 
with  Holland's  (1958,  1963)  observations  that  Arctic  and  sub-Arctic  populations  of 
S.  undulatus  are  parasitized  by  different  species  of  fleas.  He  postulated  a  possible 
intraspecific  divergence  within  these  ground  squirrels,  although  it  was  recognized 
that  the  differences  could  be  explained  by  a  dependence  of  the  fleas  upon  ecologic 
factors  other  than  the  host.  Perhaps  these  three  lines  of  evidence,  mammalian 
morpholog}',  Siphonapteran  morphology  and  protein  analysis,  may  be  interpreted 
as  indicating  differing  rates  of  evolutionary  divergence  from  what  must  have  once 
been  a  common  ancestral  gene  pool.  The  Arctic  subspecies  of  S.  undulatus  may 
have  diverged  farther  from  the  ancestral  genotype  than  sub-Arctic  subspecies 
which  appear  to  share  a  greater  number  of  common  characteristics  w^ith  S. 
columbianus.  It  should,  of  course,  be  emphasized  that  the  several  evidences  of 
divergence  manifested  by  S.  undulatus  are  of  a  low  degree  of  magnitude  and  do  not 
imply  achievement  of  species  status,  although  they  do  suggest  the  probability  of 
incipient  speciation  within  S.  undulatus. 

The  two  subspecies  of  5.  beldingi  that  were  studied  could  not  be  differentiated 
by  trenchant  protein  characters.  However,  the  frequency  of  Fraction  B  in  two 
populations  of  S.  beldingi  oregonus  was  1/10  and  1/3  and  in  S.  beldingi  crebrus,  it  was 
6/6.  This  fraction,  constituting  Character  IV,  appears  to  be  a  genetically  controlled 
protein  that  exists  in  a  polymorphic  state  similar  to,  but  distinct  from,  transferrin 
and  haptoglobin.  As  such,  its  gene  frequency  might  be  determined  in  larger  samples 
from  additional  populations  and  thereby  serve  as  a  means  for  distinguishing  these 
tw'o  subspecies  of  S.  beldingi. 

Differences  in  protein  pattern  between  populations  of  S.  undulatus  kennicotti 
are  quite  striking  and  they  involve  two  apparently  unrelated  fractions  (Table  1). 
First,  8  of  14  specimens  of  kennicotti  from  the  30  mile  population  exhibit  two 
transferrin  fractions  as  judged  by  the  ability  of  both  to  bind  Fe^^.  In  contrast, 
sera  from  the  22  animals  obtained  6  miles  from  Anaktuvuk  Pass  contain  only  one 
transferrin.  Thus,  the  two  populations  can  be  differentiated  on  the  basis  of  the 
frequency  of  one  versus  two  transferrins ;  similar  observations  have  been  reported 


105 


650  Charles  F.  Nadler  and  Charles  E.  Hughes 

in  primates  (Goodman  et  ai,  1965)  and  reptiles  (Dessauer  et  ai,  1962).  A  second 
population  difference  consists  of  the  presence  of  a  low  frequency  of  Fraction  B 
(4/14)  in  the  30  mile  kennicotti  population  and  a  complete  absence  in  the  6  mile 
population  (0/22).  The  chemical  identity  and  function  of  this  fraction  are  not 
known:  it  exists  in  a  polymorphic  state  in  both  S.  undidatus  kennicotti  and  S. 
beldingi,  whereas  it  is  present  in  all  samples  of  ^S.  undulatus  kodiacensis  and  S. 
columbianus.  As  mentioned  in  the  discussion  of  this  fraction  in  S.  beldingi,  calcula- 
tion of  its  frequency  in  larger  population  samples  might  provide  an  additional 
reliable  indicator  of  population  composition  that  could  be  employed  with  transferrin 
in  the  study  of  kennicotti  populations.  A  third  protein,  Fraction  C,  exhibits  a 
nearly  equal  degree  of  variation  in  the  two  kennicotti  populations  and  therefore  this 
fraction  does  not  aid  in  their  differentiation,  although  the  fact  that  all  three  speci- 
mens of  5.  undulatus  kodiacensis  manifested  this  fraction  suggests  that  Character  V 
might  be  applicable  at  the  subspecies  level  if  larger  samples  were  studied. 

Because  of  the  differences  shown  to  exist  between  the  proteins  of  ground 
squirrels  from  the  30  and  6  mile  localities,  it  is  necessary  here  to  consider  the 
taxonomic  status  of  specimens  from  the  Anaktuvuk  Pass  region  and  the  geographic 
distribtuion  of  animals  examined  in  the  present  study.  Concerning  taxonomic 
status,  Bee  &  Hall  (1956)  examined  a  large  sample  of  S.  undulatus  from  the  entire 
Arctic  slope  of  Alaska,  including  specimens  from  Anaktuvuk  Pass  and  Tulugak 
Lake  located  12  miles  N.  of  Anaktuvuk  Pass,  and  concluded  that  all  were  referable 
to  a  single  subspecies,  kennicotti.  Specimens  analyzed  in  the  present  study  were 
taken  from  a  locality  on  the  Anaktuvuk  River  (Arctic  slope  Brooks  Range)  6  miles  E. 
of  Anaktuvuk  Pass  and  are  probably  also  referable  to  kennicotti.  The  second 
population  we  studied,  however,  was  taken  30  miles  E.  of  Anaktuvuk  Pass  on 
Ernie  Creek,  which  is  a  tributary  of  the  Koyukuk-Yukon  River  Drainage  (south 
slope  Brooks  Range).  Since  animals  from  the  south  slope  of  the  Brooks  Range 
have  not  yet  been  studied  in  detail,  our  sample  from  the  30  mile  population  can  be 
only  tentatively  regarded  as  kennicotti  and  the  possibility  that  they  are  referable  to  a 
different  subspecies,  perhaps  osgoodi,  is  open  to  consideration. 

There  are  no  obvious  physical  barriers  at  the  divide  that  might  separate  the  two 
populations  of  S.  undulatus  we  studied,  although  we  did  observe  that  the  terrain 
even  in  mid-August  was  wet  and  poorly  drained  for  about  2  miles  on  either  side 
and  that  area  may  be  unsuitable  for  burrow  construction.  Future  studies  might  be 
profitably  directed  toward  analysis  of  proteins  from  larger  samples  and  examination 
of  additional  north  and  south  slope  colonies  in  an  attempt  to  further  characterize 
and  explain  the  mechanisms  responsible  for  the  divergence  we  observed  within 
S.  undulatus  kennicotti. 

Acknoiuledgements — We  thank  Doctor  Robert  L.  Rausch  and  Russell  Pengelly  for 
generously  providing  some  of  the  specimens  studied.  Nancy  W.  Nadler,  Bob  Ahgook  and 
Johnny  Rulland  rendered  invaluable  service  to  the  senior  author  during  field  work  in  Alaska. 
Doctors  Joseph  Curtis  Moore  and  Roy  Patterson  offered  valuable  suggestions  and  reviewed 
the  manuscript.  Doctor  Morris  Goodman  offered  encouragement  and  advice  concerning 
methodology. 


106 


SERUM  PROTEIN  PATTERNS  OF  THE  GROUND  SQUIRREL  651 

REFERENCES 

Bee  J.  W.  &  Hall  E.  R.  (1956)  Mammals  of  northern  Alaska  on  the  Arctic  slope.    Univ. 

Kans.  Pubis  Mus.  nat.  Hist.  8,  1-309. 
Black  C.  C.  (1963)  A  review  of  the  North  American  Tertiary  Sciuridae.  Bull.  Mus.  comp. 

Zool.  Harv.  130,  109-248. 
Blumberg  B.  S.,  Allison  A.  C.  &  Garry  B.  (1960)  The  haptoglobins   hemoglobins  and 

serum  proteins  of  the  Alaskan  fur  seal,  ground  squirrel  and  marmot.   J.  cell.  comp. 

Physiol.  55,  61-71. 
Bryant  M.  D.  (1945)  Phylogeny  of  Nearcac  Sciuridae.  Am.  Midi.  Nat.  33,  257-390. 
Dessauer  H.   C.  &  Fox  W.   (1964)   Electrophoresis  in  taxonomic  studies  illustrated  by 

analyses  of  blood  proteins.    In  Taxonomic  Biochemistry  and  Serology  (Edited  by  Leone 

C.  A.),  pp.  625-647.   Ronald  Press,  New  York. 
Dessauer  H.  C,  Fox  W.  &  Hartwig  Q.  L.  (1962)  Comparative  study  of  transferrins  of 

Amphibia  and  Reptilia  using  starch-gel  electrophoresis  and  autoradiography.    Comp. 

Biochem.  Physiol.  5,  17-29. 
Goodman  M.  (1963)  Serological  analysis  of  the  systematics  of  recent  Hominoids.   Human 

Biol.  35,  377^36. 
Goodman  M.,  Kulkarni  A.,  Poulik  E.  &  Reklys  E.  (1965)  Species  and  geographic  differ- 
ences in  the  transferrin  polymorphism  of  macaques.   Science,  N.Y  147,  884-886. 
Hall  E.  R.  &  Kelson  K.  R.  (1959)  The  Mammals  of  North  America,  Vol.  1,  pp.  1-546. 

Ronald  Press,  New  York. 
Holland  G.  P.  (1958)  Distribution  patterns  of  northern  fleas  (Siphonaptera).    Proc.  \Oth 

int.  Congr.  Ent.  1,  645-658. 
Holland  G.  P.  (1963)  Faunal  affinities  of  the  fleas  (Siphonaptera)  of  Alaska:  With  an 

annotated  list  of  species.    In  Pacific  Basin  Biogeography  (Edited  by  Gressitt  J.  L.), 

pp.  45-63.   Bishop  Museum  Press,  Honolulu. 
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l-25o. 
MacPherson  a.  H.  (1965)  The  origin  of  diversity  in  mammals  of  the  Canadian  arctic 

tundra.    Systematic  Zool.  14,  153-173. 
Nadler  C.  F.  (1963)  The  application  of  chromosomal  analysis  to  taxonomy  of  some  North 

American  Sciuridae.    Proc. XVI  int.  Congr.  Zool.  4,  111-115. 
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Spermophilus.  To  be  published. 
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Nature,  Lond.  180,  1477-1479. 
Poulik  M.  D.  &  Smithies  O.  (1958)  Comparison  and  combination  of  the  starch-gel  and 

filter-paper  electrophoretic  methods  applied  to  human  sera:  two-dimensional  electro- 
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Rand  A.  L.  (1954)  The  ice  age  and  mammal  speciation  in  North  America.  Arctic  7,  31-35. 
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proteins  of  normal  human  adults.   Biochem.  J.  61,  629-641. 
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107 


\'oL  SO,  pp.  22-3-226  1  December  1967 

PROCEEDINGS 
OF  THE 

BIOLOGICAL  SOCIETY   OF  WASHINGTON 

THE  SYSTEMATIC  POSITION'  OF  THE  BATS  DESMODUS 

AND  CHILOXYCTERIS.  BASED  OX  HOST-PAK\SITE 

RELATIONSHIPS  (MAMMALIA:  CHIROPTEIL\)i 

By  C.  E.  Machado-Allisox 

Instituto  de  Zoologia  Tropical,  Universidad 

Central  de  Venezuela 

Patterson  (IGSe^i  has  pointed  out  that  the  fossils  and  ecto- 
parasites of  bats  pro\ide  ver\-  Little  e\idence  which  can  be 
used  in  clarif>"ing  the  problems  of  phylogem'  in  the  order 
Chiroptera.  Indeed,  chiropteran  fossils  are  scarce,  and  the 
majorit}-  of  chiropteran  ectoparasites  belong  to  groups  that, 
ha\ing  a  Hfe  histon-  stage  off  the  body  of  the  host  do  not 
show  notable  specificit>".  Another  factor  detracting  from  the 
use  of  ectoparasites  is  the  intimate  ecological  association 
existing  betvveen  bats  of  different  groups,  particularly  those 
found  in  caves,  holes  in  trees,  etc.,  where,  occasionally,  several 
species  roost  together.  This  beha\'ior  favors,  without  doubt, 
polyhaematophag>",  and  there  are  striking  cases  of  this  such 
as  the  presence  of  fleas  of  the  family  IschnopsylHdae  on  bats 
of  the  distantly  related  famHies  Molossidae  (Tadarida  Raf- 
inesque)  and  Xoctihonidae  {ycctilio  Linnaeus).  However, 
host-parasite  relationships  may  yet  prove  to  be  of  value  in 
shedding  new  hght  on  phylogenetic  problems  in  Chiroptera. 
It  must  be  realized  that  we  still  know  httle  about  such  relation- 
ships in  the  majorit>-  of  bats  and  that  only  in  the  last  few 
years  have  careful  well-documented  collections  of  the  ecto- 
parasites been  made. 

In  \iew  of  these  facts,  it  becomes  particularly  important 
to  study  a  group  of  ectoparasites,  such  as  the  Spintumicidae 
(Acarina.  Mesostigmata)  which  apparently  show  great  host 


-A     eor-tribntion     of     the     S~/.:':.-.   -;in     Venezuelan     Project,     supported     by     a 
•     -        DA-49-193-MD-27SS,      of     the     Medical     Research     and     Development 

_     ---r.  i,   Office  cf  the  Siirgeon  General,   U.   S.  Army. 

35— Pp.oc.  Biol.  Soc.  W.\sh.,  Vol.  SO,  1967  (223) 


108 


224  Proceedings  of  the  Biological  Society  of  Washington 

specif icit\'  (Rudnick,  1960;  Macbado-Alli'soD.  1965a),  and  also 
show  peculiar  modifications  in  their  life  c\'cle  (Baer,  1952; 
Rudnick,  op.  cit.),  for  instance,  ovo\i\~iparit>-  and  reduction 
in  number  of  n)Tnphal  stages. 

In  the  past  few  years  I  have  been  stud>ing  the  taxonomy 
of  the  Neotropical  Spintumicidae,  especially  of  the  genus 
Perighschrus  Kolenati  ( Machado-.Allison,  1965b),  which  is 
intimately  related  to  the  bats  of  the  familv  PhvUostomidae. 
Comparing  the  arrangement  of  the  genera  and  subfamilies  of 
Phyllostomidae,  based  on  the  work  of  Miller  (1907)  and 
Simpson  (1945),  now  acc-epted  by  most  mammalogists,  with 
certain  data  offered  by  the  relationships  of  Spintumicidae  and 
the  bats,  I  find  some  significant  disagreements  which  I  want 
to  point  out. 

According  to  Simpson  (op.  cit.^,  the  superfamily  Phyl- 
lostomoidea  includes  the  families  Phyllostomidae  and  Des- 
modidae.  Simpson  di\ided  the  family  Phyllostomidae  into 
seven  subfamilies:  Chilonycterinae,  PhyUostominae,  Glos- 
sophaginae,  CaroUiinae,  Stumirinae,  Stenodermatinae,  and 
PhyUonycterinae.  Among  these  subfamilies,  only  one,  Phyl- 
lon\cterinae,  is  not  known  to  be  parasitized  by  the  Spin- 
tumicidae (there  are  no  pubhshed  data  on  the  CaroUiinae, 
but  I  have  recently  found  a  new  spintumicid  on  Rhinophylla 
pumilio  Peters), 

The  Chilon>"cterinae  occupy  a  special  position  in  the  Phyl- 
lostomidae. The  absence  of  a  noseleaf  and  the  lack  of  articula- 
tion of  the  trochiter  with  the  scapula  clearly  differentiate  these 
bats  from  those  of  the  other  subfanulies.  These  features  led 
Winge  (1923)  to  associate  the  Chilonycterinae  \^-ith  the 
Noctihonidae  in  a  section  of  the  Phyllostomidae  that  he  called 
"Mormopini."  Xo\ick  (1963)  found  the  orientation  sounds 
and  associated  anatomical  features  of  the  Chilonycterinae  to 
differ  sharply  from  those  of  other  phyUostomids. 

Spintumicidae  have  not  been  found  on  the  Xoctilionidae. 
and  the  only  South  .American  form  that  I  have  found  on 
ChiJonycterls  Gray  presents  morphological  characteristics  so 
peculiar  that  I  have  considered  it  to  belong  to  a  genus  Camer- 
onieta  Machado- Allison,  distinct  from  Periglischrus  (Machado- 
-AlHson.  1965a).    The  other  subfamilies  of  PhvUostomidae  are 


109 


Host-Parasite  Relationships  of  Bats 


225 


Table  1.     Host-parasite  relationships  of  Phyllostomidae  with 

Spinturnicidae. 


Spintumicid 
species 

Chiropteran 
genera 

Present  subfamilial 
assignment 

Cameronieta  ihomasi 

Chilonycteris 

Chilonycterinae 

Periglischrus  acutisternus 
Periglischrus  torrealbai 
Periglischrus  parvus 

Phyllostomus 
Phyllostomus 
Microntjcteris 

Phyllostominae 

Periglischrus  setosus 
Periglischrus  squamosus 
Periglischrus  hopkinsi 

Glossophaga 

Anoura 

Lionycteris 

Glossophaginae 

Periglischrus  ojastii 

Sturnira 

Stumirinae 

Periglischrus  iheringi 

Artiheus, 

Vampyrops,  etc. 

Stenodennatinae 

Periglischrus  sp. 

Rhinophylla 

Carolliinae 

Periglischrus  herrerai 

Desmodus 

Desmodidae 

parasited  by  species  of  Periglischrus  (three  species  on  Glos- 
sophaginae, three  on  Phyllostominae,  one  on  Carolliinae,  one 
on  Stumirinae,  and  one  on  Stenodermatinae;  see  Table  1). 

Desmodus  rotundus  E.  Geoffrey,  family  Desmodidae,  is  the 
host  of  the  species  Periglischrus  herrerai  Machado-AlHson, 
which  clearly  belongs  to  the  genus  Periglischrus.  In  orienta- 
tion behavior  Desmodus  resembles  phyllostomid  genera 
( Novick,  op.  cit. ) . 

The  evidence  presented  here  indicates  that  a  reappraisal 
of  the  familial  relationships  of  the  Chilonycterinae  and  the 
Desmodidae  is  in  order.  I  would  suggest  that  rather  than 
being  a  subfamily  of  the  Phyllostomidae,  the  chilonycterines 
may  form  a  distinct  family.  The  desmodids,  on  the  other  hand, 
may  be  no  more  than  a  subfamily  of  the  Phyllostomidae. 

Literature  Cited 

Baer,  J.  1952.  Ecology  of  Animal  Parasites.  The  University  of 
Illinois  Press,  Urbana,  223  pp. 

Machado- Allison,  C.  E.  1965a.  Notas  Sobre  Mesostigmata  Neo- 
tropicales  III.  Cameronieta  Thomasi:  Nuevo  Genero  y 
Nueva  Especie  Parasita  de  Chiroptera  (Acarina,  Spin- 
turnicidae).   Acta   Biol.   Ven.,   4(10):     243-258,    15   Figs. 


110 


226  Proceedings  of  the  Biological  Society  of  Washington 

.    1965b.     Las  Especies  Venezolanas  del  Genero  Periglischrus 

Kolenati,  1857,  (Acarina,  Mesostigmata,  Spintumicidae ) . 
Acta  Biol.  Ven.,  4(11):    259-348,  46  Figs. 

Miller,  G.  S.  1907.  The  Families  and  Genera  of  Bats.  Smithsonian 
Inst.,  U.  S.  Nat.  Mus.,  Bull.  no.  57,  282  pp.,  14  pis. 

Nov^CK,  A.  1963.  Orientation  in  Neotropical  bats.  II  Phyllostomatidae 
and  Desmodontidae.    Journ.  Mamm.,  44:    44-56. 

Patterson,  B.  1956.  Mammalian  Phylogeny.  ler.  Symp.  Specif. 
Parasit.,  Neufchatel,  pp.  15-49. 

RuDNiCK,  A.  1960.  A  Revision  of  the  Mites  of  the  Family  Spin- 
tumicidae (Acarina).  Univ.  Calif.  Publ.  Entomol.,  17(2): 
157-284,  pis.  18-48. 

Simpson,  G.  G.  1945.  The  principles  of  classification  and  a  classifica- 
tion of  mammals.  Bull.  Amer.  Mus.  Nat.  Hist.,  vol.  85, 
350  pp. 

Wince,  H.  1923.  Pattedyr-Slaegter.  Kjobenhavn,  H.  Hagerups  F. 
vol.  1,  360  pp. 


Ill 


SECTION  2— ANATOMY  AND  PHYSIOLOGY 

Form  and  function  are  intimately  related.  It  is  difficult  to  consider  one  for 
long  or  at  all  thoroughly  without  considering  the  other. 

In  comments  elsewhere  we  apply  a  concept  of  organizational  levels.  In 
taxonomy,  classification  begins  with  individuals  and  proceeds  through  local 
aggregates  or  populations,  geographic  variants,  subspecies,  and  species,  and 
on  to  groupings  at  the  level  of  higher  categories.  In  ecology,  the  individual 
organism  is  the  basic  unit,  then  progressively  more  inclusive  and  more  com- 
plex levels  are  local  populations  of  single  species,  local  communities  of  many 
species,  larger  ecosystems,  and  finally  the  entire  biosphere  of  life-supporting 
parts  of  the  surface  of  the  Earth.  Similarly  in  anatomy  and  physiology  there 
are  organizational  levels.  However,  in  these  fields  the  individual  is  the  largest 
unit  instead  of  the  smallest,  except  as  we  may  speak  of  the  anatomical  charac- 
ters of  a  species  or  other  taxon.  Form  or  function  may  be  studied  at  the  bio- 
chemical or  molecular  level,  or  at  progressively  higher  levels  through  more 
complex  molecules,  mixtures  and  solutions,  organelles,  cells,  tissues,  organs, 
systems,  and  finally  to  the  organism  in  its  entirety. 

The  study  of  anatomy  began  at  the  gross  level  and  only  after  the  invention 
of  the  microscope  and  development  of  special  techniques  of  preparing  mate- 
rials did  histological  and  cytological  studies  become  possible.  The  recent 
development  of  the  electron  microscope  has  added  several  orders  of  magnitude 
to  the  possibilities  of  studying  fine  structure.  Physiology  developed  later  than 
gross  anatomy  and  in  many  ways  paralleled  chemistry  and  physics. 

Our  selection  of  examples  is  a  modest  one,  drawn  from  a  rich  field,  and  we 
will  have  to  be  content  with  the  above  mention  of  the  broad  scope  of  anatomy 
and  physiology,  inasmuch  as  none  of  our  selections  has  electron  photomicro- 
graphs or  histochemical  analyses.  The  selections  do,  nevertheless,  serve  to 
illustrate  some  fundamental  biological  concepts. 

The  concept  of  homeostasis  was  conceived  and  broadly  applied  in  physiol- 
ogy. The  concept  is  relevant,  at  least  by  analogy,  in  ecology  under  the  guise  of 
the  "balance  of  nature,"  recently  expanded  to  include  a  sizable  vocabulary  of 
terms  such  as  "feedback  regulatory  mechanism"  and  "damped  cycles."  We 
judge  that  homeostasis  or  the  tendency  of  an  organism  to  maintain  internal 
conditions  at  a  dynamic  equilibrium  is  the  most  general  concept  of  physiology, 
and  that  homology  is  the  most  general  concept  of  anatomy. 

The  short  paper  by  Hill  that  begins  this  section  presents  one  simple  ana- 
tomical problem,  and  at  the  same  time  presents  the  concept  of  homology  and 
the  problems  of  interpreting  it. 

The  subsequent  contributions  by  Hooper,  Hughes,  and  Mossman  are  com- 
parative studies  within  one  family  ( Cricetidae ) ,  one  order  (Marsupialia),  and 
one  class  (Mammalia),  respectively.  Each  author  studied  a  different  part  of 
the  animals  concerned  and  attempted  to  relate  his  observations  to  existing 
knowledge  within  the  systematic  framework. 

The  next  paper,  by  Noback,  treats  hair,  one  of  the  unique  features  of  the 
Class  Mammalia,  and  theorizes  about  its  adaptive  and  phylogenetic  impHca- 


113 


tions.   This  article  is  from  a  symposium  that  contains  other  interesting  papers 
on  hair. 

The  two  reprinted  papers  by  Vaughan  and  Rabb  treat  form  and  function 
together,  the  former  at  the  level  of  a  taxonomic  family,  the  latter  in  terms  of 
one  set  of  glands  in  one  species. 

Among  the  classic  works  in  mammalian  anatomy  is  Weber's  Die  Sdugetiere 
(1927,  1928).  English  mammalogists  dating  back  to  Richard  Owen  and  earlier 
have  published  many  comparative  papers  on  mammalian  anatomy  (see  for 
example  Pocock's  The  External  Characters  of  the  Pangolins,  1924 ) .  One  of  the 
most  productive  American  mammalian  anatomists  was  A.  B.  Howell,  whose 
Anatomy  of  the  Wood  Rat  (1926)  and  Aquatic  Mammals  (1930)  both  have 
much  to  offer.  Four  good  recent  works  of  a  comparative  nature  are  Rinker's 
( 1954 )  study  of  four  cricetine  genera,  Vaughan's  ( 1959 )  paper  on  three  kinds 
of  bats,  Klingener's  (1964)  treatment  of  dipodoid  rodents,  and  D.  Dwight 
Davis'  major  work  (1964)  on  the  greater  panda.  Hildebrand's  (1959)  paper 
on  locomotion  in  the  cheetah  and  the  horse  should  be  consulted  by  any  student 
interested  in  functional  anatomy  or  locomotion.  The  Anatomical  Record  and 
Journal  of  Morphology  are  two  of  the  more  important  serial  pubHcations 
containing  papers  on  anatomy. 

Among  the  environmental  influences  that  are  important  to  organisms,  and 
whose  effects  within  the  organism  must  be  mitigated,  are  water,  oxygen  and 
other  gases,  energy  sources  (food),  ions,  temperature,  and  radiation.  Most  of 
these  factors  are  touched  upon  in  one  or  more  of  the  last  four  papers  in  this 
selection  in  ways  that  help  clarify  the  adaptive  nature  of  internal,  behavioral, 
and  ecological  responses.  In  addition  to  these  aspects  of  physiology,  some 
areas  of  special  mammalogical  interest  are  hibernation,  estivation,  thermo- 
regulation, and  sensory  physiology.  Examples  appear  in  Section  4  (Ecology 
and  Behavior )  as  well  as  in  this  section. 

A  recent  paper  by  Brown  ( 1968 ) ,  too  long  to  include  among  our  selections, 
is  an  excellent  example  of  how  physiological  adaptations,  related  in  this  case 
to  environmental  temperature,  can  be  studied  comparatively.  Other  important 
contributions  in  mammalian  physiology  can  be  found  in  such  journals  as  Com- 
parative Biochemistry  and  Physiology,  Journal  of  Applied  Physiology, 
Journal  of  Cell  and  Comparative  Physiology,  and  Physiological  Zoology. 


114 


THE  HOMOLOGY  OF  THE  PRESEMIMEMBRANOSUS 
MUSCLE  IN  SOME  RODENTS 

JOHN  ERIC  HILL 
Museum  of  Vertebrate  Zoology,  University  of  California 

ONE  FIGXTBE 

Appleton  ('28)  has  distinguished  between  the  caudofemo- 
ralis  muscle  and  the  presemimembranosus  muscle  (of  Leche, 
1883)  on  the  basis  of  their  respective  relations  to  the  'nerve 
to  the  hamstring  muscles.'  At  the  same  time  he  has  empha- 
sized the  importance  of  considering  topographical  relations 
in  any  discussion  of  the  homologies  of  muscles.  The  caudo- 
femoralis,  according  to  this  author,  crosses  over  the  nerve  to 
the  hamstring  muscles,  dorsal  and  lateral  to  this,  while  the 
presemimembranosus  is  medial  to  the  nerve. 

In  many  rodents  (Parsons,  1894,  1896)  the  caudofemoralis 
arises  from  the  caudal  vertebrae  and  inserts  on  the  medial 
epicondyle  of  the  femur  and  the  caudal  surface  of  this  bone. 
This  is  the  condition  in  the  white  rat  (Rattus  norvegicus) 
where  I  found  the  muscle  dorsal  to  the  nerve.  In  this  rodent, 
and  in  the  others  mentioned  below,  the  caudofemoralis  is  sup- 
plied by  the  most  cephalic  branch  of  the  nerve  to  the  ham- 
string muscles.  In  the  pocket  gophers  (Thomomys  bulbivorus 
and  Geomys  bursarius),  in  the  kangaroo  rat  (Dipodomys 
spectabilis),  and  in  a  specimen  of  the  wood  rat  (Neotoma 
fuscipes),  I  found  that  the  caudofemoralis  arises  from  the 
ischial  tuberosity  and  inserts  on  the  medial  epicondyle. 
Howell  ('26)  found  that,  in  some  specimens  of  the  wood  rat, 
the  muscle  originates  from  the  caudal  vertebrae,  and  in  all 
these  cases  the  caudofemoralis  is  dorsal  (that  is  superficial) 
to  the  nerve  to  the  hamstring  muscles;  so  there  is  no  doubt 
of  its  identity.  In  Dipodomys  a  few  fibers  of  the  muscle  were 
medial  to  the  nerve. 

311 

THE   ANATOMICAL  RECORD,   VOL.    59,    NO.    3 


115 


312 


JOHN    ERIC    HILL 


However,  in  two  specimens  of  a  ground  squirrel  (Citellus 
richardsonii)  and  in  a  mountain  beaver  (Aplodontia  rufa)  I 
found  a  muscle  which  originated  from  the  ischium  medial 
(that  is  deep)  to  the  nerve  to  the  hamstrings,  but  which  other- 
wise presented  the  same  topographical  relations  as  the  caudo- 
femoralis  in  the  other  rodents.  Like  the  latter  muscle  in 
these  other  forms,  it  was  supplied  by  the  most  cephalic  branch 


dorsal  hjscia 
gluteus  maximus  (cut) 
aluleus  medius 


iensc fasciae  lahe 


uashis  lalefalis 


qtuheus  maximus 
'  (cuO 

Quadfatus  femon's 


femorvcoccf^g  e  us 
(cut) 


Fascia    la  la- 


ienuissimua   (cut) 
piriforinis 

nefi/e  {o  hamsifing  mascJts 
■femo''ococcu<^eiAS   (cut) 
N.  ^udendus 

Nfernoralis  cuhneus posiethr 
I'endon  of caudo^emofal/s 
caudal  head  of seniilendinasus 
c  audofemorali  s 
-ischial  head  of  semiiendinosus 

adduclor  ma^nus 

-N  ischiadicus 
biceps  femon's 
somimambrano  Sus 
gracilis 
M  Surae  lateralis 

ienuissimus  fculj 

vV  peroneus  communis 

biceps  femoris  Icuti 

fascia  lafa 


Fig.  1     The  muscles  of  the  thigh  of  Sciurus  griseus  showing  the  relations  of 
the  caudofemoralis    (presemimembranosus). 

of  the  nerve  to  the  hamstrings.  According  to  the  views  of 
Appleton  ('28)  and  Leche  (1883),  however,  this  muscle  would 
be  a  presemimembranosus  and  not  a  caudofemoralis. 

The  condition  of  this  muscle  in  the  gray  squirrel  (Sciurus 
griseus)  suggests  a  solution  to  the  problem  of  its  homology, 
in  rodents  at  least.  In  the  specimen  dissected,  the  muscle 
arose  by  tendinous  and  fleshy  fibers  from  the  ischial  bone 
and,  by  a  slender  tendon  (fig.  1),  from  the  transverse  process 


116 


HOMOLOGY    OF    PRESEMIMEMBRANOSUS    MUSCLE  313 

of  the  first  caudal  vertebra.  The  tendon  crossed  superficial  to 
the  nerve  to  the  hamstring  muscles,  while  the  part  of  the 
muscle  arising  from  the  ischium  lay  medial  and  deep  to  the 
nerve.  Alezais  ( '00)  described  the  muscle  in  Sciurus  vulgaris 
as  the  'ischio-condylien.'  In  this  animal  it  is  apparently 
identical  with  the  muscle  described  above  in  Sciurus  griseus, 
but  that  author  did  not  perceive  the  significance  of  the  peculiar 
relation  between  the  muscle  and  the  nerve  to  the  hamstrings. 
This  relation  may  be  considered  a  stage  intermediate  between 
the  typical  position  of  the  caudofemoralis  and  that  of  the  so- 
called  presemimembranosus. 

It  may  be  concluded  that  muscles  do,  in  rare  instances, 
change  their  topographical  relations  to  nerves;  and  that  the 
caudofemoralis  and  the  presemimembranosus  are  homologous 
muscles.  Consequently,  when  the  muscle  in  question  is  con- 
tinuous with  the  semimembranosus,  the  condition  should  not 
be  considered  primitive  or  undifferentiated,  but  rather  as  a 
secondary  fusion  of  the  caudofemoralis  and  the  semimem- 
branosus. Also,  since  it  is  generally  accepted  by  workers  in 
comparative  myology  (Alezias,  '00;  Parsons,  1892;  Leche,  '00) 
that  the  presimimembranosus  forms  part  of  the  great  ad- 
ductor in  man,  the  identification  of  the  former  muscle  as  a 
modified  caudofemoralis  seems  to  fill  a  gap  between  the  known 
morphological  history  of  the  sciatic  part  of  the  adductor 
magnus  and  the  phylogeny  of  the  caudofemoralis  as  traced 
by  Appleton  ('28).  ' 


117 


314  JOHN    EEIC    HILL 

LITERATURE  CITED 

Alezais,  H.     1900     Contribution  a  la  myologie  des  rongeurs.     Theses  presentees 

a  la  faculte  des  sciences  de  Paris. 
Appleton,  a.  B.     1928     The  muscles  and  nerves  of  the  post-axial  region  of  the 

tetrapod  thigh.     J.  Anat.,  vol.  62,  pp.  364-438. 
Howell,  A.  B.     1926     Anatomy  of  the  wood  rat.    Baltimore :  Williams  &  Wilkins 

Company. 
Leche,   W.     1883     Zur    Anatomie    der    Beckenregion    bei    Insectivora.      Kongl. 

Svensk.  Vetensk.-Akad.  Handl.,  vol.  20,  pp.  1-112. 

1900     Muskulatur.     Saugethiere:      Mammalia.     In  Bronn:    Klassen 

und  Ordnungen  des  Thier-Reichs,  Bd.  6 :  5 :  1 :  2,  S  649-919. 

Parsons,  F.   G.     1892     Some  points  in  the  myology  of  rodents.     J.  Anat.  and 
Physiol.,  vol.  26,  Proc  Anat.  Soc.  Gt.  Britain  and  Ireland. 

1894     On  the  myology  of  the  sciuromorphine  and  hystricomorphine 

rodents.     Proc.  Zool.  Soc.  London,  pp.  251-296. 

■ 1896     Myology  of  rodents.     Part  II.  An  account  of  the  myology  of 

the   Myomorpha,   together   with   a   comparison   of   the   muscles   of   the 
various  suborders  of  rodents.     Proc.  Zool.  Soc.  London,  pp.  159-192. 


118 


Number  625  May  10,  1962 

OCCASIONAL  PAPERS  OF  THE  MUSEUM  OF 

ZOOLOGY 
UNIVERSITY  OF  MICHIGAN 

Ann  Arbor,  Michigan 

THE  GLANS  PENIS  IN  SIGMODON,  SIGMOMYS,  AND 
REITHRODON   (RODENTIA,  CRICETINAE) 

By  Emmet  T.  Hooper 

Cotton  rats  {Sigmodon  and  Sigmomys),  marsh  rats,  (Holochilus), 
coney  rats  (Reithrodon),  and  red-nosed  rats  (Neotomys)  compose  an 
assemblage  which  Hershkovitz  (1955)  considers  to  be  natural  and 
which  he  designates  as  the  "sigmodont  group."  This  group  contrasts 
with  or)zomyine,  ichthyomyine,  phyllotine,  akodont,  and  other 
supraspecific  assemblages  which  various  authors  (e.g.,  Thomas,  1917; 
Gyldenstolpe,  1932;  Hershkovitz,  1944,  1948,  1955,  1960;  and  Voront- 
sov,  1959)  have  recognized  in  analyzing  the  large  cricetine  fauna  of 
South  America.  While  all  of  these  groups  are  tentative,  at  least  in 
regard  to  total  complement  of  species  in  each,  nevertheless  some  are 
strongly  characterized  and  probably  natural;  and  all,  whether  natural 
or  not,  are  useful  in  that  they  constitute  conveniently  assessable  seg- 
ments of  an  unwieldly  large  South  American  cricetine  fauna,  now 
disposed  in  approximately  40  nominal  genera.  New  information  re- 
garding three  of  those  genera  is  provided  below.  It  is  derived  from 
fluid-preserved  and  partially  cleared  glandes  (procedures  described  by 
Hooper,  1959)  as  follows: 

Reithrodon  ciiniculoides:  Argentina,  Tierra  del  Fuego,  1  adult. 
Sigmodon  alleni:  Michoacan,  Dos  Aguas,  3  adults.  5.  hispidus: 
Arizona,  Pima  Co.,  1  subadult.  Florida,  Alachua  and  Osceola  coun- 
ties, 3  adults.  Michoacan,  Lombardia,  2  adults.  5.  minimus:  New 
Mexico,  Hidalgo  Co.,  1  juvenile.  5.  ochrognathus:  Texas,  Brewster 
Co.,  1  subadult.  Sigjnomys  alstoni:  Venezuela,  Aragua,  1  subadult. 

I  am  indebted  to  Elio  Massoia  for  the  specimen  of  Reithrodon  and 
to  Charles  O.  Handley,  Jr.,  for  the  example  of  Sigmomys.  Figures  1 
and  2  were  rendered  by  Suzanne  Runyan,  staff  artist  of  the  Museum  of 
Zoology.  The  National  Science  Foundation  provided  financial  aid. 

Listed  below  in  sequence  are  representative  measurements  (in  mm.) 

1 


119 


2  Emmet  T.  Hooper  Occ.  Papers 

of  Sigmodon  hispidus  (averages  of  five  adults),  Sigmomys  ahtoni  (one 
subadult),  and  Reithrodon  cuniculoides  (one  adult).  Length  of  hind 
foot:  34,  30,  33;  greatest  lengths  of  glans,  7.6,  6.6,  7.8;  greatest  diam- 
eter of  glans,  6.2,  4.0,  5.0;  length  of  main  bone  of  baculum,  5.5,  4.9, 
4.1;  length  of  medial  distal  segment  of  baculum,  2.8,  2.0,  2.7;  total 
length  of  baculum,  8.3,  6.9,  6.8. 

DESCRIPTION  OF  GLANDES 

Sigmodon  hispidus.— In  Sigmodon  hispidus  the  glans  is  a  spinous, 
stubby,  contorted  cylinder  (Fig.  1),  its  length  one-fourth  to  one-fifth 
that  of  the  hind  foot  and  its  greatest  diameter  approximately  three- 
fourths  its  length  (see  measurements).  The  spines  which  densely  stud 
almost  all  of  the  epidemiis,  except  tJiat  of  the  terminal  crater,  are 
short  and  thick-set;  each  is  recessed  in  a  rhombic  or  hexagonal  pit.  The 
glans  is  somewhat  swayback  and  potbellied,  yet  in  its  basal  one-half 
or  tAvo-thirds  it  is  essentially  plain  and  cylindrical,  without  lobes  or 
folds  other  than  a  short  midventral  frenum  which,  as  an  indistinct 
raphe,  continues  distad  to  the  rim  of  the  crater.  The  distal  third  or 
half  of  the  glans  is  conspicuously  hexalobate,  the  six  lobes  separated 
from  each  other  by  longitudinal  troughs  or  grooves  which  increase  in 
depth  distad.  The  lobes  are  unequal  in  size  and  shape;  the  ventral 
pair  is  largest  and  the  least  convex,  the  lateral  pair  smallest,  and  the 
dorsal  pair  the  most  convex;  the  latter  is  a  key  item  in  the  swayback 
appearance  of  the  glans.  These  lobes  converge  distally,  and  tJieir 
crescentic  lips  form  the  scalloped,  overhanging  rim  of  the  terminal 
crater. 

The  largest  structure  in  the  crater  is  the  mound  which  houses  the 
medial  distal  segment  of  the  baculum.  Nestled  between  the  lips  of  the 
ventral  lobes,  it  projects  outside  the  crater  approximately  to  the  limits 
of  the  dorsal  lobes.  The  two  smaller  lateral  mounds,  housing  the 
lateral  processes  of  the  baculum,  are  closely  appressed  to  the  medial 
mound,  and  the  tip  of  each  is  distinctly  pointed,  rather  than  gently 
rounded  like  the  medial  mound.  Immediately  ventral  to  the  medial 
mound  is  the  meatus  urinarius  which  is  guarded  ventrally  by  a  ure- 
thral process.  This  process  consists  of  a  pair  of  rather  thick  arms  each 
of  which  is  out-curved  and  tapers  to  an  obtuse  tip  (Fig.  1);  in  one 
specimen  the  ventral  face  of  the  process  is  studded  with  spines.  Dorsal 
to  the  medial  mound  is  the  dorsal  papilla,  which  is  a  single  distensible 
cone  of  soft  tissue  dotted  with  spines  both  dorsally  and  laterally.  Two 
additional  pairs  of  crater  conules,  here  termed  "dorsolateral  and 
lateral  papillae,"  are  particularly  noteworthy  because,  insofar  as  known 


120 


No.  625 


Glans  Penis  in  Sigmodont  Rodents 


3 


I  I 


foot  glans  bac.  bone 


Fig.  1.  Views  of  glans  penis  of  Sigmodon  hispidus:  a,  dorsal;  b,  lateral;  c,  incised 
midventrally  exposing  urethra;  d,  epidermal  spines,  enlarged;  e,  urethral  process, 
enlarged,  ventral  aspect;  UMMZ  97270,  Florida. 


121 


4  Emmet  T.  Hooper  Occ.  Papers 

in  the  New  World  cricetids  studied  to  date,  they  are  peculiar  to 
Sigmodon  and  Sigmomys.  All  four  of  these  are  spine-studded,  stubby, 
and  smoothly  rounded  terminally.  Each  dorsolateral  papilla  is  situated 
just  below  the  crater  rim  at  the  junction  of  the  dorsal  and  lateral 
lobes.  Each  lateral  papilla  is  partly  recessed  in  a  pocket  on  the  lower 
flank  of  the  crater  wall  alongside  a  lateral  bacular  mound. 

There  is  no  ventral  shield  (a  large  mass  of  tissue  between  the 
urethral  process  and  the  ventral  lip  of  the  crater)  as  seen  in  most 
microtines,  and  the  bacular  mounds  are  relatively  free  within  the 
crater,  there  being  no  partitions  connecting  the  lateral  mounds  with 
the  crater  walls;  the  urethra  empties  onto  the  crater  floor,  not  into  a 
partition-encircled  secondary  crater  within  the  larger  crater,  an 
arrangement  seen  in  some  rodent  species. 

Below  the  crater  floor  is  a  right  and  left  pair  of  bilobed  sacs  (Fig. 
1),  each  ovoid  ventral  lobe  about  1.5  mm.  in  length,  and  each  atten- 
uate dorsal  lobe  approximately  a  millimeter  longer,  its  tip  extending 
distad  almost  to  the  limits  of  the  main  bone  of  the  baculum.  These 
sacs  or  sinuses  emerge  from  tissues  situated  beside  the  corpora 
cavernosa  penis  and  they  extend  alongside  the  baculum  and  the  corpus 
cavernosum  urethra,  but  they  apparently  are  not  parts  of  either  of 
those  structures.  Composed  entirely  of  soft  tissues  and  engorged  with 
blood  in  some  specimens,  they  appear  to  be  continuous  with  the  deep 
dorsal  vein  and,  thus,  they  seem  to  be  part  of  the  vascular  system. 
Similar  sacs,  as  illustrated  in  Phyllotis  by  Pearson  (1958:424)  for  ex- 
ample, occur  in  all  of  those  New  World  cricetids  studied  to  date  that 
have  a  four-part  baculum;  they  have  not  been  observed  in  Peromyscus, 
Neotoma,  or  other  cricetid  groups  which  are  characterized  by  a  simple 
baculum  and  glans. 

The  four-part  baculum  is  at  least  as  long  as  the  glans  and  is  one- 
fourth  the  hind  foot  in  length  (see  measurements).  The  main  bone, 
one-sixth  the  length  of  the  hind  foot,  is  angular  and  gross.  The  dorsal 
face  of  its  wide  and  angular  base  is  deeply  concave  between  prominent 
lateral  and  proximal  condyles  to  which  the  corpora  cavernosa  attach, 
while  the  ventral  surface  is  almost  flat  except  for  a  midventral  keel  of 
either  cartilage  or  bone  which,  spanning  approximately  four-fifths  the 
length  of  the  bone,  terminates  at  the  cartilage  of  the  digital  junction. 
The  shaft  is  oval  in  cross-section,  the  dorsoventral  diameter  exceeding 
the  transverse  one;  as  viewed  laterally  it  is  slightly  bent  and  is  con- 
stricted terminally,  while  in  ventral  view  it  is  gently  tapered  distad 
before  expanding  to  form  a  distinct  terminal  head. 

The  three  distal  segments  of  the  baculum  are  subequal  in  length. 


122 


No.  625  Glans  Penis  in  Sigmodont  Rodents  5 

the  lateral  pair  slightly  shorter  than  the  medial  one.  They  differ  con- 
siderably in  shape  and  amount  of  ossification.  In  one  breeding  adult 
they  are  entirely  cartilaginous,  while  in  four  other  adults  they  con- 
tain various  amounts  of  osseous  tissue  in  addition  to  cartilage;  proba- 
bly in  very  old  animals  they  are  entirely  osseous.  The  medial  segment, 
attached  to  the  ventral  sector  of  the  main  bone,  projects  distad  and 
slightly  ventrad,  then  it  bends  abruptly  dorsad  before  terminating  in 
a  rounded  tip.  It  is  approximately  oval  in  cross  section  in  its  distal 
three-fourths,  but  in  its  proximal  fourth  it  is  much  wider  than  deep 
and  is  keeled  ventrally;  moreover,  at  the  digital  junction  it  bears  a 
pair  of  lateral  processes  and  a  medial  flange,  the  continuation  of  the 
midventral  keel,  w'hich  extends  over  the  ventral  face  of  the  head  of 
the  main  bone.  In  all  specimens  at  hand  these  three  processes  are 
cartilaginous;  furthennore,  the  osseous  tissue  of  the  three  distal  seg- 
ments is  restricted  to,  or  concentrated  in,  the  distal  parts  of  each  seg- 
ment, indicating  that  ossification  apparently  proceeds  from  the  tip 
proximad  in  S.  hispidus. 

The  lateral  segments,  situated  dorsolateral  to  the  medial  unit, 
attach  onto  the  dorsal  and  lateral  parts  of  the  head  of  the  main  bone- 
dorsal  to  the  flanges  of  the  medial  segment.  Each  is  pointed  and  blade- 
shaped,  the  dorsoventral  diameter  exceeding  the  transverse  one;  and 
as  viewed  ventrally  each  curves  gently  distad  and  slightly  laterad. 
Whether  cartilaginous  or  osseous,  they  are  situated  in  the  lateral  parts 
of  each  bacular  mound,  while  the  medial  and  distalmost  parts  of  each 
mound  consist  entirely  of  soft  tissue,  a  large  part  of  which  is  vascular 
and  appears  to  be  instrumental  in  distention  of  the  mounds.  In  some 
examples,  the  basal  parts  of  the  three  distal  segments  of  the  baculum 
are  more  or  less  coalesced;  this  is  particularly  true  of  the  two  lateral 
units,  and  the  two  have  been  interpreted  as  a  single  horn-shaped 
structure  (Hamilton,  1946).  However,  as  indicated  by  Burt  (1960)  they 
are  separate  units  (Fig.  1);  their  individual  limits  are  clear  in  speci- 
mens at  hand. 

Sigmodon  minimus,  S.  ochrognathus,  and  5.  alleni.—l  recognize  no 
interspecific  differences  in  the  specimens  of  minimus  and  ochrognathus, 
both  examples  of  which  are  young  and  rather  unsatisfactory.  Each 
closely  resembles  specimens  of  hispidus  of  like  age  in  external  size  and 
shape,  and  in  conformation  of  the  six  exterior  lobes,  dorsal  papilla, 
dorsolateral  papillae,  lateral  papillae,  urethral  process,  crater  mounds, 
and  baculum.  If  there  are  interspecific  differences,  they  are  not  clearly 
evident  in  the  materal  at  hand. 

The  three  adults  from  Dos  Aguas,  Michoacan,  which  are  labeled  S. 


123 


6  Emmet  T.  Hooper  Occ.  Papers 

alleni,  are  also  like  adults  of  hispidus.  The  two  series  differ  slightly 
in  regard  to  size  of  glans  and  shape  of  baculum,  but  these  are  small 
differences  and  doubtfully  interspecific. 

A  few  remarks  regarding  the  identification  of  the  specimens  from 
Dos  Aguas  are  needed.  Until  variation  in  Sigmodon  is  better  under- 
stood, .S.  alleni  seems  to  be  the  most  appropriate  name  to  apply  to 
these  specimens  and,  as  well,  to  others  like  them  from  the  vicinity  of 
Autlan,  Jalisco,  and  Angahuan  and  Uruapan,  Michoacan.  Cranially 
and  externally  distinguishable  from  specimens  of  5.  hispidus  and  S. 
mclanotis  from  nearby  localities  in  the  same  states,  they  appear  to 
represent  a  species  other  than  either  hispidus  or  melanotis.  They 
agree  well  with  the  description  of  alleni,  but  they  have  not  been  com- 
pared directly  with  the  type  specimen  of  that  form. 

Sig7nomys  alstoni.—The  specimen  of  Sigmomys  alstoni  resembles 
examples  of  Sigmodon  of  comparable  age  in  length  (relative  to  hind 
foot),  in  external  configuration  (hexalobate,  swaybacked  and  pot- 
bellied in  lateral  view,  and  covered  with  proximally  directed,  thickset, 
sharp,  entrenched  spines),  shape  of  dorsal  papilla  (single,  spine-stud- 
ded cone),  appearance  of  urethral  process  (two  outcurved  arms  with  a 
longitudinal  row  of  spines  on  the  ventral  face  of  each),  shape  of  the 
bacular  mounds  (the  medial  one  large  and  rounded,  each  lateral  one 
smaller  and  rounded  laterally  but  acute  medially),  position  of  digits 
of  baculum  with  respect  to  the  main  bone,  presence  of  ventral  keel 
and  lateral  arms  on  the  medial  digit,  and  occurrence  of  a  midventral 
keel  on  the  main  bone.  The  specimen  differs  from  examples  of 
Sigmodon  in  characters  as  follows:  glans  smaller  in  diameter  (diam- 
eter-length ratio  approximately  60  per  cent,  compared  with  70-88  per 
cent  in  Sigmodon);  the  six  external  lobes,  particularly  the  dorsal  pair, 
less  prominent;  dorsolateral  papillae  smaller,  scarcely  more  than  the 
spine-studded  infolding  of  the  dorsal  and  lateral  lobes;  crater  more 
extensively  spinous  (spines  studding  most  of  inner  wall  of  each  lateral 
lobe);  medial  digit  of  baculum  projecting  principally  distad,  its  tip 
not  sharply  flexed  dorsad;  and  the  osseous  proximal  segment  flatter 
and  wider  for  a  larger  fraction  of  its  length. 

The  lateral  papillae  and  baculum  warrant  additional  comment.  It 
is  uncertain  whether  lateral  papillae  are  present  in  the  specimen.  Two 
papillose  vascular  cores  occur  at  sites  where  papillae  are  to  be  ex- 
pected, but  in  the  present  damaged  specimen  the  overlying  crater 
floor  is  not  correspondingly  papillose,  although  it  is  strongly  spinous; 
the  spiny  area  occupies  most  of  the  inner  face  of  the  lateral  lobe  and 
of  the  adjoining  crater  floor.  On  the  left  side  of  the  specimen  this 


124 


No.  625  Glans  Penis  in  Sigmodont  Rodents  7 

roughly  circular  spiny  area  is  plate-like,  while  on  the  right  side  it  is 
buckled  distad  and,  thus,  resembles  a  large  papilla.  If,  in  undamaged 
specimens,  these  areas  are  papillose,  then  the  lateral  papillae  in  5. 
alstoni  are  relatively  larger  than  any  yet  seen  in  Sigmodon. 

In  ventral  view,  the  main  bone  of  the  baculum  is  shaped  roughly 
like  an  isosceles  triangle— wide  basally  and  tapered  rather  evenly  dis- 
tad (without  pronounced  incurve)  almost  to  the  slight  constriction 
which  subtends  the  small,  round,  terminal  head.  Its  wide  basal  part 
is  concave  dorsally  (between  low  lateral  condyles)  and  almost  fiat 
ventrally;  but  farther  distad  the  bone  is  deeper  than  wide  and,  some- 
what triangular  in  cross  section,  it  bears  a  slight  midventral  ridge  to 
which  a  cartilaginous  keel  is  attached.  The  distal  segments  are  entirely 
cartilaginous.  The  medial  one  is  deeper  than  wide  in  its  distal  half 
and  blunt  terminally;  basally  it  bears  a  medial  process  and  two  lateral 
flanges.  Each  lateral  segment,  also  deeper  than  wide  and  blunt  termin- 
allv,  is  situated  dorsolateral  to  the  medial  unit. 

Reithrodon  cimiculoides— The  glans  of  R.  cuniciiloides  (Fig.  2)  is 
stubby  (diameter-length  ratio  64  per  cent),  subcylindrical,  and  indis- 
tinctly lobate,  the  lobes  defined  by  four,  shallow,  longitudinal  troughs. 
Two  of  these  depressions,  one  situated  middorsally  and  the  other 
mid\entrally,  extend  approximately  the  full  length  of  the  glans  and 
thereby  divide  the  surface  of  the  glans  into  right  and  left  halves;  the 
distal  limit  of  each  is  a  notch  in  the  crater  rim.  The  shorter  third  pair 
of  troughs  is  situated  dorsolaterally  in  the  distal  half  of  the  glans,  but 
each  tenninates  short  of  the  rim.  All  of  the  epidermis  as  far  distad  as 
the  crenate,  membranous,  overhanging  rim  of  the  crater  is  densely 
studded  with  small,  conical,  recessed  tubercles. 

The  three  bacular  mounds,  together  with  the  underlying  baculum, 
resemble  a  fieur-de-lis  in  ventral  aspect  (Fig.  2);  the  erect  medial  part 
extends  beyond  the  crater,  while  each  of  the  truncate  lateral  pair 
sends  off  an  attenuate  lateral  segment  which  curves  laterad  and  then 
distad  before  terminating  in  an  acute  tip.  These  lateral  processes  con- 
tain no  cartilage  or  bone;  they  consist  entirely  of  soft  tissues,  a  large 
part  of  which  is  vascular  and  apparently  erectile.  The  spine-tipped 
dorsal  papilla  is  unusually  small  and  slender;  it  is  a  single  cone,  but  a 
slight  cleft  near  its  tip  suggests  that  the  papilla  may  consist  of  two 
conules  in  other  specimens.  The  urethral  process  is  a  bilobed  flap 
with  two  attenuate  and  erect  (not  outcurved)  arms;  it  bears  two  longi- 
tudinal rows,  each  of  eight  tubercles,  on  its  ventral  face.  There  are  no 
lateral  or  dorsolateral  papillae,  and  the  crater  walls  and  floor  are 
smooth  and  non-spinous. 


125 


Emmet  T.  Hooper 


Occ.  Papers 


I    I     I 

foot  glans  bac.  bone 


Fig.  2.  Views  of  glans  penis  of  Reithrodon  cuniculoides;  UMMZ  109233,  Argen- 
tina. For  explanation  see  Fig.  1  and  text. 


126 


No.  625  Glans  Penis  in  Siemodont  Rodents 


Q' 


The  baculum  is  shorter  than  the  glans  (see  measurements).  Its  prox- 
imal, osseous  segment  consists  of  a  wide  basal  part  and  a  slender  shaft. 
The  basal  part,  which  bears  large,  proximally  directed  condyles  (these 
separated  medially  by  a  deep  notch),  is  broadly  concave  ventrally  and 
narrowly  and  shallowly  concave  dorsally.  The  relatively  straight  shaft 
is  slightly  deeper  (dorsoventrally)  than  wide  and  it  bears  a  slight 
ventral  keel;  its  terminal  portion  is  slightly  expanded  laterad  and 
slightly  constricted  dorsoventrally  (Fig.  2).  The  three  distal  segments 
are  cartilaginous.  The  long  medial  one  (its  length  two-thirds  that  of 
the  bone)  is  rod-like  for  much  of  its  length,  but  it  is  enlarged  basally 
and  is  tapered  distally  to  a  pointed  tip.  The  lateral  units  are  disc- 
shaped in  cross  section,  the  dorsoventral  diameter  of  each  much  great- 
er than  the  transverse  one.  From  its  attachment  on  the  head  of  the 
bone  (the  attachment  dorsal  and  lateral  to  that  of  the  medial  unit) 
each  lateral  segment  curves  gently  laterad  and  distad  before  it  termin- 
ates at  the  base  of  the  laterally  projecting  process  of  its  lateral  mound. 

DISCUSSION 

To  judge  from  specimens  at  hand,  the  glandes  of  Sigmodon  alleni, 
S.  hispidus,  S.  minimus,  and  5.  ochrognathus  are  fundamentally  alike, 
although  they  may  differ  interspecifically  in  details  which  can  not  be 
appraised  in  present  samples.  In  each  species  the  stubby,  swayback, 
tubercle-invested  glans  bears  six  prominent  exterior  lobes  which  sur- 
round the  terminal  crater  and  divide  its  rim  into  six  corresponding 
parts.  Within  the  crater  there  are  five  spine-studded  papillae  consist- 
ing of  dorsolateral  and  lateral  pairs  in  addition  to  a  single  cone  mid- 
dorsally.  The  urethral  process  bears  two  attenuate,  outcurved  arms. 
The  bacular  mounds  are  truncate  except  for  a  small,  acute  medial 
crest  on  each  lateral  mound,  and  the  medial  distal  segment  of  the 
four-part  baculum  bears  a  medial  keel  and  a  pair  of  lateral  processes 
on  its  base,  while  its  tip  is  flexed  sharply  dorsad.  These  characters, 
together  with  others,  distinguish  Sigmodon  from  the  other  New  World 
cricetid  genera  which  have  been  studied  to  date,  with  the  possible 
exception  of  Sigmomys.  Sigmomys  alstoni,  the  only  species  of  Sig- 
momys  about  which  there  is  information  on  the  glans,  appears  to  be 
closely  similar  to  species  of  Sigmodon,  but  its  characters  are  not  yet 
adequately  known. 

In  contrast  to  the  phalli  of  Sigmodon  and  Sigtnomys,  the  glans  of 
Reithrodon  cuniculoides  is  comparatively  slim  and  simple.  There  are 
only  four  exterior  lobes,  and  these  are  less  prominent  than  the  lobes 
of  Sigmodon  or  Sigmomys.  The  membranous,  crenate,  and  non-spiny 


127 


10  Emmet  T.  Hooper  Occ.  Papers 

crater  rim  is  not  divided  into  six  distinct  lobes.  The  crater,  also 
smooth  and  spineless,  has  no  dorsolateral  or  lateral  papillae.  The 
slender  dorsal  papilla  bears  spines  only  at  its  tip.  Each  lateral  mound 
has  an  attenuate  lateral  process,  and  the  entire  configuration  of  the 
three  crater  mounds  as  well  as  of  the  underlying  baculum  is  distinc- 
tive. The  three,  long,  erect  distal  segments  of  the  baculum,  all  car- 
tilaginous insofar  as  known,  are  essentially  rod-like  in  form,  without 
prominent  keels  or  processes.  These  and  other  contrasting  characters 
indicate  that  the  glans  of  R.  cuniculoides  is  morphologically  quite 
different  from  that  seen  in  Sigmodon  and  Sigmomys.  Preliminary 
comparisons  suggest  that  it  may  be  more  similar  to  glandes  of  phyllo- 
tine  or  other  species  which  are  not  now  included  in  the  sigmodont 
group  of  rodents. 


128 


No.  625  Glans  Penis  in  Sigmodont  Rodents  11 

LITERATURE  CITED 

Burt,  William  H. 

1960  Bacula  of  North  American  mammals.  Miscl.  Publ.  Mus.  Zool.  Univ.  Mich., 
113:1-76,25  pis. 

Gyldenstolpe,  Nils 

1932  A  manual  of  Neotropical  sigmodont  rodents.  Kungl.  Svenska  Veten. 
Hand.,  Ser.  3,  no.  3:  1-164,  18  pis. 

Hamilton,  William  J.,  Jr. 

1946  A  study  of  the  baculum  in  some  North  American  Microtinae.  Jour. 
Mamm.,  27:378-87,  1  pi.,  3  figs. 

Hershkovttz^  Philip 

1944  A  systematic  review  of  the  neotropical  water  rats  of  the  genus  Nectornys 
(Cricctinae).  Miscl.  Publ.  Mus.  Zool.  Univ.  Mich.,  58:1-88,  4  pis.,  5  figs. 

1948  Mammals  of  northern  Colombia,  preliminary  report  No.  3:  water  rats 
(genus  Nectornys),  with  supplemental  notes  on  related  forms.  Proc.  U.S. 
Natl.  Mus.,  98:49-56. 

1955  South  American  marsh  rats,  genus  Holochilus,  with  a  summary  of  sig- 
modont rodents.  Fieldiana:  Zoology,  37:639-73,  13  pis.,  6  figs. 

1960  Mammals  of  northern  Colombia,  preliminary  report  No.  8:  arboreal  rice 
rats,  a  systematic  revision  of  the  subgenus  Oecomys,  genus  Oryzomys. 
Proc.  U.S.  Natl.  Mus.,  110:513-68,  12  pis.,  6  figs. 

Hooper,  Emmet  T. 

1959  The  glans  penis  in  five  genera  of  cricetid  rodents.  Occ.  Pap.  Mus.  Zool. 
Univ.  Mich.,  613:1-10,  5  pis. 

Pearson,  Oliver  P. 

1958  A  taxonomic  revision  of  the  rodent  genus  Phyllotis.  Univ.  Calif.  Publ. 
Zool.,  56:391-496,  8  pis.,  21  figs. 

Thomas,  Oldfield 

1917  On  the  arrangement  of  the  South  American  rats  allied  to  Oryzomys  and 
Rhipidomys.  Ann.  Mag.  Nat.  Hist.,  ser.  8,  20:192-8. 

Vorontsov,  N.  N. 

1959  The  system  of  hamster  (Cricetinae)  in  the  sphere  of  the  world  fauna 
and  their  phylogenetic  relations.  Bull.  Mosk.  Obsh.  Ispyt.  Prirody,  Biol. 
Sec.    (Bull.  Moscow  Soc.  Naturalists),  64:134-7. 

Accepted  for  publication  February  5,  1962 


129 


COMPARATIVE  MORPHOLOGY  OF  SPERMATOZOA  FROM  FIVE 

MARSUPIAL  FAMILIES 

By  R.  L.  Hughes* 

[Manuscript  received  April  8,  1965] 
Summary 

The  spermatozoa  of  18  marsupial  species  derived  from  five  families  have  been 
examined  and  of  these  only  the  spermatozoon  of  the  bandicoot  Perameles  nasuta 
has  previously  been  described  adequately. 

The  spermatozoon  morphology  within  the  families  Macropodidae,  Dasyuridae, 
Phascolarctidae,  and  Peramelidae  was  relatively  homogeneous.  A  distinctive 
morphology  occured  between  these  families.  Within  the  family  Phalangeridae 
spermatozoa  were  morphologically  diverse,  however,  as  a  group  they  were  relatively 
separate  from  those  of  the  other  families  studied. 

The  spermatozoa  of  the  Phascolarctidae  (koala,  Phascolarctos  cinereus,  and 
wombat,  Phascolomis  mitchelli)  have  a  unique,  somewhat  rat-like  morphology  which 
clearly  separates  them  from  those  of  the  other  marsupial  sperm  studied.  This  finding 
is  of  considerable  taxonomic  interest  as  most  authorities  consider  the  koala  to  be  more 
closely  related  to  the  phalangerid  marsupials  than  to  the  wombat. 

I.  Introduction 

Previous  descriptions  of  marsupial  spermatozoon  morphology  cover  six  of  the 
major  marsupial  groups.  A  considerable  proportion  of  these  accounts  is  devoted  to 
a  study  of  the  spermatozoon  morphology  of  three  species,  each  belonging  to  separate 
marsupial  families.  (1)  Family  Didelphidae:  Didelphis  [Selenka  (1887),  Fiirst  (1887), 
Waldeyer  (1902),  KorflF  (1902),  Retzius  (1909),  Jordan  (1911),  Duesberg  (1920), 
Wilson  (1928),  McCrady  (1938),  Biggers  and  Creed  (1962)];  (2)  family  Phalangeridae: 
Phalangista  vulpina  (  =  Trichosurus  vulpecula)  [Korff  (1902),  Benda  (1897,  1906), 
Retzius  (1906),  Bishop  and  Walton  (I960)];  (3)  family  Peramehdae:  Perameles  nasuta 
[Benda  (1906),  Cleland  (1955,  1956,  1964),  Cleland  and  Rothschild  (1959),  Bishop  and 
Austin  (1957),  Bishop  and  Walton  (I960)]. 

The  spermatozoon  morphology  of  two  Dasyuridae,  Phascogale  albipes  (  =  Smin- 
thopsis  murina)  and  Dasyurops  maculatus,  was  studied  by  Fiirst  (1887),  Bishop  and 
Austin  (1957),  and  Bishop  and  Walton  (1960). 

Benda's  (1906)  description  of  an  epididymal  sperm  from  the  koala,  Phascolarctos 
(family  Phascolarctidae),  is,  as  he  admits,  inadequate. 

Spermatozoon  morphology  studies  on  members  of  the  family  Macropodidae 
include  those  of  an  unknown  Macropus  sp.  (Benda  1906),  Macropus  billardierii 
(  =  Thylogale  billardierii),  Petrogale  penicillata,  Onychogale  limata  (  =  Onychogalea 
lunata),  Bettongia  cimiculus  (Retzius  1906),  Macropus  giganteus  (  =  Macropus  canguru) 
(Binder  1927),  and  Potorous  tridactylus  (Hughes  1964). 

*  Division  of  Wildlife  Research,  CSIRO,  Canberra. 

Aust.  J.  ZooL,  1965,  13,  533-43 


130 


534  R.   L.    HUGHES 

The  spermatozoa  examined  in  the  present  study  were  obtained  from  members 
of  the  five  Australasian  marsupial  families:  Phalangeridae,  Peramelidae,  Dasyuridae, 
Phascolarctidae,  and  Macropodidae.  The  present  series  of  observations  has  been 
viewed  with  reference  to  those  of  earlier  workers  and  this  has  permitted  at  least  an 
elementary  discussion  of  the  comparative  aspects  of  spermatozoon  morphology 
between  the  marsupial  families  examined. 

II.  Material  and  Methods 

The  testes  together  with  the  attached  epididymis  were  removed  from  the  scrotum 
soon  after  death  and  fixed  in  10%  neutral  formalin  or,  more  rarely,  Bouin's  fluid  or 
Carnoy  fixative. 

(i)  Method  for  Adhering  Spermatozoa  to  Microscope  Slides 

The  slides  were  labelled  at  one  end  with  a  diamond  pencil  and  a  15-mm  square 
was  marked  out  at  the  opposite  end.  The  entire  surface  of  the  slide  was  liberally 
smeared  with  Mayer's  albumen.  A  small  piece  of  epididymal  tissue  was  placed  in  a 
drop  of  10%  neutral  buifered  formalin  within  the  marked  square  and  extensively 
teased  with  dissecting  needles.  Filter  paper  circles  of  5-5  cm  diam.  were  saturated 
with  10%  formalin,  drained,  and  placed  over  the  specimen  by  a  rolling  action.  Air 
bubbles  were  punctured  with  a  needle.  The  filter  paper  was  kept  moist  with  10% 
formalin  for  at  least  30  min  and  then  permitted  to  dry  until  free  fluid  between  the 
slide  and  the  filter  paper  had  disappeared.  The  filter  paper  was  then  removed  by  a 
rolling  action,  excess  tissue  was  removed  with  fine  forceps,  and  the  preparations  rinsed 
and  stored  in  water  for  staining. 

(ii)  Staining  of  Spermatozoa 

(1)  Heidenhains  Iron  Haematoxylin. — Slides  containing  adhering  spermatozoa 
were  transferred  from  water  to  a  5  %  solution  of  iron  alum  and  kept  in  a  warm  place 
for  2-3  days.  They  were  then  stained  with  Heidenhain's  haematoxylin  for  a  similar 
period.  The  area  not  containing  the  specimen  was  thoroughly  cleaned  with  paper 
tissues  during  a  10-15  min  rinsing  period  in  running  tap  water.  The  preparations  were 
then  diff'erentiated  in  5%  iron  alum  under  a  staining  microscope  at  30  sec  intervals. 
The  preparation  was  washed  in  water  and  re-examined  after  each  differentiation  inter- 
val. Difl'erentiation  times  of  between  30  sec  and  5  min  proved  satisfactory  to  show  the 
desired  range  of  structures.  The  preparations  were  upgraded  to  absolute  ethyl  alcohol, 
placed  in  two  changes  of  xylol,  and  mounted  in  euparal. 

(2)  Periodic  Acid-Schijf  {with  saliva  controls). — Slides  containing  the  mounted 
spermatozoa  were  removed  from  water  and  placed  horizontally  in  two  groups  on  a 
flat  tray.  One  group  was  flooded  with  water  and  the  other  with  saliva  for  1  hr  at  a 
temperature  of  37°C.  The  slides  were  then  thoroughly  rinsed  in  distilled  water  and 
stained  by  a  method  described  by  Carleton  and  Drury  (1957,  p.  143).  The  SchiflF's 
reagent  used  was  de  Tomasi  (for  preparation  see  Pearse  1961,  p.  822).  The  prepara- 
tions were  mounted  in  euparal. 

(3)  Feulgen  (with  and  without  fast  green  counterstain). — Slides  containing  the 
adhering  spermatozoa  were  removed  from  water  and  stained  by  a  method  described 


131 


MORPHOLOGY  OF  SPERMATOZOA  535 

by  Pearse  (1961,  p.  823).  The  Schiff' s  solution  used  was  de  Tomasi.  Half  the  Feulgen 
preparations  were  stained  with  fast  green  counterstain  (0-5%  solution  in  70%  ethyl 
alcohol)  for  15-20  min.  Both  Feulgen  and  Feulgen-fast  green  preparations  were 
quickly  passed  through  three  changes  of  90%  alcohol  (dips  only)  to  absolute  ethyl 
alcohol  and  then  cleared  in  xylol  and  mounted  in  euparal. 

Slides  were  stored  until  dry  in  an  oven  at  a  temperature  of  37°C  after  mounting 
in  euparal.  Preparations  were  not  permitted  to  dry  out  during  any  of  the  earlier  stages 
in  preparation. 

The  drawings  of  spermatozoa  shown  in  Figure  1  are  based  on  camera  lucida 
outlines  using  a  Xl2  eyepiece  in  conjunction  with  a  x  100  oil-immersion  objective. 

The  spermatozoon  dimensions  shown  in  Table  1  are  means  of  25  observations 
and  were  obtained  with  a  special  Leitz  x  12  -5  screw  micrometer  eyepiece  and  a  X  100 
oil-immersion  objective.  The  preparations  used  were  fixed  in  10%  neutral  formalin 
or,  more  rarely,  Bouin's  fluid  or  Carnoy  and  were  stained  with  Heidenhain's  iron 
haematoxylin. 

During  the  course  of  the  observations  on  sperm  it  became  apparent  that  the 
efferent  ducts  connecting  the  testis  and  epididymis  were  either  multiple  or  single 
within  each  marsupial  family.  This  was  investigated  further  from  frozen  transverse 
sections  stained  with  haematoxylin  and  eosin.  The  sections  were  prepared  from  the 
efferent  duct  or  ducts  at  the  point  of  their  emergence  from  the  testis  and  also  approxim- 
ately midway  between  the  testis  and  epididymis. 

The  author  follows  Cleland  and  Rothschild  (1959)  in  considering  for  the  purpose 
of  description  that  the  flagellum  is  inserted  into  the  ventral  surface  of  the  sperm  head 
and  the  opposite  surface  is  taken  as  dorsal. 

in.  Results 

The  mature  epididymal  spermatozoa  of  1 8  marsupial  species  have  been  examined. 
The  dimensions  of  13  of  these  spermatozoa  are  shown  in  Table  1.  The  gross  morphol- 
ogy of  14  of  the  spermatozoa  is  shown  in  Figure  1. 

Spermatozoa  of  each  of  the  five  marsupial  families  studied  (Macropodidae, 
Phalangeridae,  Dasyuridae,  Peramelidae,  Phascolarctidae*)  exhibited  sufficient 
homogeneity  in  morphology  and  dimensions  of  the  head,  flagellum,  and  fine  structure 
to  be  of  taxonomic  value. 

The  heads  of  all  marsupial  spermatozoa  examined  showed  some  dorsoventral 
flattening.  This  was  most  marked  in  the  Dasyuridae  and  Peramelidae.  It  was  least 
evident  in  the  Phascolarctidae  and  the  genus  Pseudocheirus  of  the  Phalangeridae. 
Macropod  and  the  other  phalangerid  spermatozoa  exhibited  an  intermediate  con- 
dition. The  distal  extremity  of  the  head  of  all  species  when  viewed  dorsally  was 
relatively  rounded  while  the  shape  of  the  lateral  margins  and  proximal  tip  varied 
considerably.  In  the  Dasyuridae  the  spermatozoon  heads  of  up  to  12-7  /a  in  length 
in  Dasyuroides  byrnei  are  among  the  longest  known  for  mammals  (Table  1).    The 

*  The  author  follows  Sonntag  (1923)  in  grouping  the  wombat  and  koala  in  the  family 
Phascolarctidae. 


132 


536 


R.    L.    HUGHES 


lateral  head  margins  of  dasyurid  sperm  are  slightly  convex  in  dorsal  view  and  taper 
gradually  to  a  proximal  point.  Macropod  sperm  heads  are  considerably  shorter  than 
those  of  the  Dasyuridae  and  in  dorsal  outline  are  elongated  ovoids  bluntly  pointed 
proximally.  The  sperm  head  of  the  macropod  Megaleia  rufa  (Figs.  1^  and  1/?)  is 
rapidly  tapering,  a  condition  typically  found  in  the  Phalangeridae.  Phalangerid 
sperm,  when  viewed  dorsally,  exhibit  considerable  variability  in  the  convexity  of  the 
lateral  head  margins.  The  proximal  region  of  the  head  is  typically  semicircular, 
although  sometimes  bluntly  pointed  as  in  Pseudocheirus  cupreus  (Figs.   \n  and  \o). 

Table  1 
marsupial  spermatozoon  dimensions 


Mean  ±SD  (/a) 

Family  and  Species 

Head 

Middle 

-piece 

Flagellum 

Length 

Width 

Length 

Diameter 

Length 

Macropodidae 

Macropus  canguru 

7-3±016 

2-2  +  011 

10-7±0-24 

1-5±014 

111-6+  3-60 

Megaleia  rufa* 

5-l±0-2I 

2-4±009 

7-9±0-25 

l-4i:012 

1040±  4-74 

Protemnodon  rufogrisea 

8-5±0-22 

2-3±018 

Il-7±0-34 

l-6±0-14 

115-4±  8-85 

Protemnodon  agilis] 

7-l±0-38 

1-8±012 

110±0-28 

1-4±013 

—           — 

Thylogale  stiginatica* 

7-2±009 

2-2±0Il 

10-9±0-22 

1-5±012 

1031±  4-43 

Dasyuridae 

Dasyuroides  byrnei 

12-7±0-41 

2-5±015 

40-7  il -26 

3- 1+0- 19 

242- 1±  6-77 

Sarcophilus  harrisii 

llliO-45 

2-2±0-I7 

34-4:rO-84 

2-6±013 

207-4±1202 

Phalangeridae 

Petaurus  brevicepsX 

5-9±019 

2-5±018 

8-3  :L0-27 

1-4±011 

101-3±  4-96 

Pseudocheirus  cupreus% 

5-4±016 

2-6±011 

6-2^016 

1-5±017 

84-7±  2-47 

Pseudocheirus  peregrinus 

5-9iO-38 

3-8±018 

6-9±0-21 

21±0-22 

106-9±  5-31 

Phascolarctidae 

Phascolomis  mitchelli 

5-7±0-33 

l-7x009 

180±l-56 

0-9±010 

87-9±  8-23 

Peramelidae 

Perameles  nasuta 

5-7±015 

30±013 

140±0-32 

20±011 

1941±  5-25 

Isoodon  macrourus 

60±013 

3-3±018 

10-7±0-19 

1-8±014 

1651±  3-64 

*  Fixed  in  Bouin's  fluid;  t  Carnoy  fixative;  %  from  New  Guinea. 

Peramelid  spermatozoon  heads  have  concave  lateral  margins  when  seen  in  dorsal 
view  and  are  relatively  square  proximally  with  a  median  cap.  In  phascolarctid  sperm 
the  proximal  portion  of  the  spermatozoon  head  of  both  the  wombat  Phascolomis 
mitchelli,  and  the  koala,  Phascolarctos  cinereus,  bears  a  strongly  recurved  hook. 

In  all  sperm,  a  positive  Feulgen  reaction  for  nuclear  material  (DNA)  was  given 
by  almost  the  entire  head  mass.  The  DNA-negative  areas  that  took  up  a  fast  green 
counterstain  in  Feulgen  preparations  were  the  acrosome  (Fig.  1 ;  AC)  and  basal 
granule  complex  which  is  located  at  the  proximal  tip  of  the  flagellum.  The  acrosome 


133 


MORPHOLOGY  OF  SPERMATOZOA 


537 


20; 


Fig.  1. — Marsupial  epididymal  spermatozoa:  the  drawings  are  all  at  the  same  scale  and  are  based 
on  camera  lucida  outlines  of  formalin-fixed  Heidenhain's  iron  haematoxylin  preparations.  A  xl2 
eyepiece  was  used  in  conjunction  with  a  x  100  oil-immersion  lens.  Fam.  Phascolarctidae:  Phascolomis 
mitchelli,  {a)  lateral  view;  Phascolarctos  cinereus,  (b)  lateral  view  of  spermatozoon  head  with  flagellum 
outline.  Fam.  Macropodidae:  /'ro/f/?;Aio^o/7r///o^m£'fl,  (c)  ventral  view,  (^) lateral  view;  Protemnodon 
agilis*,  (e)  lateral  view,  (/)  ventral  view;  Megaleia  rufaj,  (g)  lateral  view,  (/;)  ventral  view;  Macropus 
canguru,  (/)  lateral  view;  Thyiogale  stiginaiica't,  (/)  lateral  view;  (A)  ventral  view.  Fam.  Dasyurinae: 
Dasyuroides  byrnei,  (I)  dorsolateral  view;  Sarcophilius  harrisii,  (m)  ventral  view.  Fam.  Phalangeridae: 
Pseudocheirus  cupreus,  (n)  dorsal  view,  io)  lateral  view;  Pseudocheirus  peregrinus,  (p)  lateral  view, 
(q)  dorsal  view;  Petaurus  breviceps,  (r)  ventral  view.  Fam.  Peramelidae:  Isoodon  macrourus,  {s) 
ventral  view;  Peranieles  nasuta,  (t)  ventral  view.  Key:  AC,  acrosome;  AF,  axial  filament;  CD, 
cytoplasmic  droplet  (middle-piece  bead) ;  CM,  cortical  helix  of  main-piece  sheath ;  MH,  mitochondrial 
helix  of  middle-piece;  A'G,  neck  granule;  i?C,  ringcentriole;  FG,  ventral  groove. 
*  Fixed  in  Carnoy  fixative,   t  Fixed  in  Bouin's  fluid. 


134 


538  R.   L.    HUGHES 

was  also  variably  positive  to  periodic  acid-Schiff  (P.A.S.)  between  species  and  the  basal 
granule  complex  was  invariably  strongly  P.A.S. -positive.  Neither  acrosome  nor  basal 
granule  complex  exhibited  any  reduction  in  P.A.S.  activity  in  saliva  controls.  A  faint 
tinge  of  green  over  the  entire  head  surface  in  Feulgen-fast  green  preparations  pre- 
sumably represents  a  limiting  membrane. 

A  "nuclear  rarefaction"  of  vacuole-like  appearance  results  from  a  minute 
superficial  nuclear  indentation.  The  nuclear  rarefaction  was  most  conspicuous  in  the 
Dasyuridae  and  Peramelidac  and  least  evident  in  the  Macropodidae.  This  structure 
is  located  on  the  mid-median  aspect  of  the  ventral  nuclear  surface  of  all  sperm  with 
the  exception  of  those  of  the  Phascolarctidae,  where  its  occurrence  is  also  ventral  and 
median  but  distal. 

In  most  of  the  marsupial  sperm  examined  acrosomal  material  (Fig.  1 ;  AC)  was 
apparently  confined  to  a  relatively  small  surface  area  of  the  head.  In  the  Macropodidae 
the  acrosome  is  relatively  small  and  is  a  discrete  ovoid  structure  embedded  super- 
ficially in  the  extreme  proximal  portion  of  the  dorsal  head  surface.  In  some  of  the 
Phalangeridae  it  has  a  definite  structure  as  in  Pseudocheinis  (Figs,  \n-\q)  where 
it  occupies  all  but  a  marginal  annular  zone  of  the  dorsal  head  surface  and  is  rather 
deeply  embedded.  In  other  phalangerids,  such  as  Petaurus  breviceps  (Fig.  \r),  the 
dorsal  head  surface  in  Feulgen-fast  green  preparations  gives  a  diffuse  acrosomal 
reaction  and  bears  a  shallow  depression  which  extends  to  all  but  the  margins.  A 
similar  diffuse  acrosomal  reaction  of  at  least  the  proximal  half  of  the  dorsal  head 
surface  occurred  in  the  Dasyuridae.  The  proximal  dorsal  tip  of  the  dasyurid  sperm 
has  a  concentration  of  acrosomal  material  situated  in  a  minute  groove.  The  acrosomal 
material  in  the  Peramelidae  was  found  in  a  small  distally  flanged  proximal  cap  which 
covered  a  minute  nuclear  protuberance.  In  the  Phascolarctidae  the  acrosome  is  a 
small  "comma-shaped"  structure.  The  body  of  the  acrosomal  "comma"  is  embedded 
superficially  in  about  the  middle  of  the  dorsal  head  surface  and  the  tail  of  the  comma 
extends  throughout  the  greater  portion  of  the  inner  curvature  of  the  head  hook. 

In  marsupial  sperm  the  ventral  surface  of  the  head  (by  convention  that  bearing 
the  flagellum)  is  typically  grooved  (Fig.  1 ;  VG)  or  bears  a  shallow  distal  notch  as  in 
the  case  of  the  Phascolarctidae.  At  the  distal  extremity  of  the  head  the  groove  is  broad 
and  deep  so  that  the  head  is  here  relatively  broad  and  has  the  form  of  an  extremely 
thin  curved  plate.  The  groove  becomes  shallow  and  narrow  towards  its  proximal 
extremity;  in  the  Macropodidae  and  Phalangeridae  it  terminates  at  about  the  mid- 
median  portion  of  the  ventral  head  surface.  The  groove  is  most  extensive  in  the 
Peramelidae  involving  the  whole  of  the  ventral  aspect  of  the  nucleus,  only  the  proximal 
acrosomal  head  cap  is  excepted.  In  the  Dasyuridae  it  extends  throughout  the  distal 
four-fifths  of  the  head. 

Spermatozoa  are  immature  when  they  enter  the  head  of  the  epididymis  and 
were  characterized  by  the  orientation  of  the  long  axis  of  the  head  at  90°  to  the 
flagellum  which  was  directed  towards  the  nuclear  rarefaction.  The  ventral  surface  of 
the  spermatozoon  head  was  supported  by  a  somewhat  cone-shaped  cytoplasmic 
droplet  (Fig.  1 ;  CD)  of  characteristic  morphology  for  each  species.  Phascolarctid 
sperm  from  the  head  region  of  the  epididymis  differed  from  the  other  marsupial 


135 


MORPHOLOGY  OF  SPERMATOZOA  539 

species  examined  in  that  tiie  flagellum  was  most  frequently  observed  not  to  meet  the 
head  at  right  angles  and  cytoplasmic  droplets  were  small  and  often  absent.  On 
entering  the  epididymis  the  head  hook  of  the  phascolarctid  spermatozoa  were  only 
slightly  recurved  or  of  an  irregular  spiral  configuration.  During  the  passage  of 
spermatozoa  through  the  epididymis  the  head  hook  became  simple  (vv'ithout  spiral) 
and  more  tightly  recurved. 

Maturation  of  spermatozoa  is  completed  during  their  passage  through  the 
epididymis  and  is  accompanied  by  shedding  of  the  cytoplasmic  droplet  and  rotation 
of  the  long  axis  of  the  head  parallel  to  that  of  the  flagellum.  The  neck  of  the 
flagellum  of  mature  epididymal  sperm  in  all  species  was  inserted  in  the  vicinity  of  the 
nuclear  rarefaction.  In  the  Dasyuridae  the  neck  was  inserted  rather  deeply  into  the 
proximal  margin  of  the  nuclear  rarefaction.  In  the  Peramelidae  the  proximal  tip  of 
the  flagellum  was  also  deeply  inserted  and  extended  from  the  proximal  margin  of  the 
nuclear  rarefaction  to  a  point  about  midway  between  the  anterior  rim  of  the  nuclear 
rarefaction  and  the  most  proximal  extremity  of  the  nucleus. 

The  flagellum  is  traversed  throughout  its  entirety  by  an  axial  filament  (Fig.  3; 
AF).  The  size  of  the  flagellum  varies  from  species  to  species.  The  smallest  flagellum 
was  that  of  Pliascolomis  mitchelli  with  a  maximum  diameter  of  0-9  /^  and  a  minimum 
length  of  87-9^  (Table  1).  The  giant  flagella  of  dasyurid  sperm  are  among  the 
largest  known  for  mammals.  Dasyiiroides  byrnei  has  a  minimum  flagellum  length 
of  242  •  1  /Li  and  a  maximum  flagellum  thickness  of  3  •  1  /x.  In  an  old  museum  specimen 
of  the  testes  of  the  now  possibly  extinct  dasyurid  Thylacinus  cynocephalus  (Tasmanian 
wolf  or  tiger)  the  flagellum  of  epididymal  sperm  in  wax  sections  had  a  maximum 
diameter  of  3  0/x  and  comparable  morphology  to  that  of  other  dasyurids;  the 
sperm  heads,  although  degenerate,  were  in  the  form  of  a  long  narrow  plate,  dorso- 
ventrally  flattened  and  with  the  flagellum  inserted  at  about  the  mid-median  ventral 
aspect.  Peramelid  sperm  flagellae  were  also  relatively  large,  having  a  maximum 
diameter  of  as  much  as  2  ;li  and  a  minimum  length  of  up  to  about  200  ^  (Table  1). 
Macropod  and  phalangerid  sperm  flagellae  were  of  intermediate  dimensions  rarely 
varying  from  a  maximum  diameter  of  1  -5  /m  and  a  minimum  length  of  a  little  over 
100 /x. 

The  basal  granule  complex  located  at  the  proximal  end  of  the  flagellum  consists 
of  at  least  fused  proximal  and  distal  components  in  the  Dasyuridae  and  Peramelidae. 

The  neck  region  of  the  flagellum  is  a  slender  proximally  pointed  cone  with  a 
smooth  contour,  and  a  small  neck  granule  (Fig.  1 ;  NG)  is  situated  at  approximately 
half  its  length.  It  was  only  possible  to  identify  the  neck  granule  with  certainty  in  the 
Peramelidae,  Dasyuridae,  and  Macropodidae.  In  the  Peramelidae  and  Dasyuridae 
it  seemed  to  be  a  more  deeply  stained,  modified  portion  of  the  ground  substance  of 
the  neck  rather  than  the  discrete  granule  found  in  the  Macropodidae.  The  sperm  of 
the  dasyurids  Dasyuroides  byrnei,  Sarcophilus  harrisii,  and  Thylacinus  cynocephalus 
had  a  neck  length  of  about  3-5 /j.  in  comparison  with  2-7  fi  for  the  peramelids 
Isoodon  macrourus  and  Perameles  nasuta.  Macropod  sperm  necks  ranged  in  length 
from  1  •  8  /x  in  Thylogale  stigmatica  to  2  •  6  /x  in  Protemnodon  rufogrisea.  The  neck 
lengthsof  the  Phalangeridae  and  Phascolarctidae  were  somewhat  reduced  in  compari- 
son to  those  of  other  marsupial  families. 


136 


540  R.    L.    HUGHES 

The  proximal  portion  of  the  middle-piece  in  all  species  examined  tapered  gradu- 
ally to  the  diameter  of  the  neck  and  was  particularly  firmly  clasped  by  the  lateral 
margins  of  the  sperm  head  in  the  Peramelidae  and  Dasyuridae.  The  remainder  of 
the  middle-piece  was  relatively  cylindrical.  A  mitochondrial  helix  (Fig.  1 ;  MH)  of 
spiral  configuration  gave  the  entire  surface  of  the  middle-piece  sheath  a  slightly 
uneven  contour.  The  mitochondrial  helix  is  a  relatively  fine  structure  in  the  Dasyuridae 
and  Peramelidae,  of  moderate  thickness  in  the  Macropodidae  and  Phascolarctidae 
and  Petaiirus  breviceps  of  the  Phalangeridae.  It  was  quite  thick  and  granular  with 
relatively  few  gyres  in  the  genus  Pseudocheirus  of  the  Phalangeridae.  The  middle- 
piece  is  terminated  distally  by  a  ring  centriole  (Fig.  1 ;   RC). 

The  flagellum  undergoes  an  abrupt  reduction  in  diameter  on  the  main-piece 
side  of  the  ring  centriole  in  both  the  Pseudocheirus  species  and  to  a  moderate  degree 
in  Petaurus  breviceps  and  the  Macropodidae,  but  not  to  any  appreciable  extent  in  the 
Dasyuridae,  Peramelidae,  and  Phascolarctidae. 

The  main-piece  of  the  flagellum  tapers  distally  and  in  twisted  specimens  appears 
not  to  be  circular  in  cross  section  in  Pseudocheirus peregrinus,  Peramelidae,  Dasyuridae, 
and  Macropodidae.  Striations  of  the  sheath  of  the  main  piece  in  all  sperm  indicate 
the  presence  of  a  fine  spiral  cortical  helix  (Fig.  1 ;  CH).  The  tail  sheath  also  gave  a 
strong  impression  of  two  lateral  thickenings  in  transverse  axis  in  Macropus  canguru, 
Protemnodon  rufogrisea,  Pseudocheirus  peregrinus,  Perameles  nasuta,  and  Isoodon 
macrourus. 

The  axial  filament  protruded  beyond  the  terminal  portion  of  the  sheath  of  the 
main-piece  in  apparently  complete  sperm  of  all  species  but  this  cannot  be  positively 
taken  to  represent  a  true  end-piece  for  in  all  preparations  terminal  breakage  of  the 
main-piece  was  prevalent. 

IV.  Discussion 

Spermatozoa  from  three  other  Peramelidae,  Perameles  gunnii,  Isoodon  obesulus, 
and  Echymipera  rufescens  have  also  been  exam.ined  superficially  and  it  can  be  stated 
that  they  are  comparable  in  morphology  to  other  peramelid  sperm.  The  spermatozoa 
of  marsupial  mice,  Antechinus  flavipes  flavipes,  A.  f.  leucogaster,  A.  swainsonii,  A. 
stuartii,  and  Sminthopsis  crassicaudata,  have  a  morphology  typical  of  other  dasyurids 
(Woolley,  personal  communication).  This  similarity  in  morphology  also  extends  to 
two  other  dasyurids,  Phascogale  albipes  (  =  Sminthopsis  murina)  (Fiirst  1887)  and 
Dasyurops  maculatus  (Bishop  and  Austin  1957;  Bishop  and  Walton  1960).  The 
spermatozoon  morphology  of  the  macropod  species  examined  in  the  present  study 
varies  in  only  minor  details  from  that  of  six  other  macropods  previously  described 
by  Benda  (1906),  Retzius  (1906),  and  Hughes  (1964). 

The  phenomenon  of  conjugate  spermatozoa  (pairing  of  relatively  numerous 
epididymal  spermatozoa)  redescribed  and  reviewed  by  Biggers  and  Creed  (1962)  for 
the  American  opossum,  Didelphis,  has  not  been  observed  in  any  of  the  sperm  pre- 
parations from  Australian  marsupials;  however,  fresh  unfixed  material  has  been 
examined  only  for  Potorous  tridactylus  (Hughes   1964)  and  Phascolomis  mitchelli. 


137 


MORPHOLOGY   OF   SPERMATOZOA  541 

Another  feature  worth  mentioning  is  that  the  head  of  the  epididymis  was  not 
fused  with  the  testis  in  any  marsupial  examined,  including  Thylacinus  cynocephalus 
and  Dendrolagus  lumholtzi.  In  the  Dasyuridae  and  Peramelidae  a  relatively  long 
single  efferent  duct  together  with  associated  blood  vessels  links  the  epididymis  to 
one  pole  of  the  testis  long  axis  by  way  of  an  extensive  membrane,  the  mesorchium. 
A  tract  of  relatively  long  multiple  efferent  ducts  serves  the  same  function  in  the 
Phalangeridae,  Phascolarctidae,  and  Macropodidae.  A  ligament  was  inserted  by 
way  of  the  mesorchium  into  the  opposite  pole  of  the  testis. 

In  both  the  wombat  and  the  koala  the  morphology  of  the  sperm,  particularly 
the  head,  differs  strikingly  from  that  of  any  marsupial  sperm  previously  described. 
In  both  species  the  proximal  portion  of  the  spermatozoon  head  bears  a  strongly 
recurved  hook  not  described  for  other  marsupial  sperm,  and  the  flagellum  is  inserted 
into  a  notch  on  one  side  of  the  distal  portion  of  the  head  (Plate  1,  Fig.  1 ;  and  Figs.  \a 
and  \b).  These  features,  although  somewhat  resembling  those  of  certain  murid 
sperm,  are  not  strictly  comparable  (Plate  1,  Fig.  2)  (Friend  1936).  The  hook  in  the 
wombat  sperm  resembles  that  of  Microtus  hirtus,  Lemmus  lemmus,  and  several  other 
members  of  the  murid  subfamily  Microtinae  in  that  the  hook  contains  no  supporting 
"rod"  and  its  tip  like  that  of  Lemmus  lemmus  is  typically  extremely  reflected  so  that 
it  lies  against  the  distal  portion  of  the  head  (Friend  1936).  The  position  of  the  hook 
in  Phascolomis  is  not  an  artefact  of  fixation  for  it  was  observed  in  living  spermatozoa 
from  the  epididymis  of  several  specimens.  In  sperm  from  the  head  of  the  epididymis 
the  curvature  of  the  hook  frequently  approximated  to  that  of  rats  and  mice.  It  can 
be  seen  from  Plate  1,  Figure  1,  and  Figures  \a  and  \b  that  the  insertion  notch  of 
the  flagellum  of  the  wombat  and  koala  sperm  is  located  on  the  opposite  side  of  the 
head  to  the  hook,  whereas  in  the  hooked  types  of  murid  sperm  both  structures  occur 
on  the  same  side  of  the  head  (Plate  1,  Fig.  2).  A  head  hook  is  absent  in  at  least  the 
murine,  Micromys  mmutus  and  in  the  microtine  Ondatra  zibethica  (Friend  1936). 
In  Heidenhain's  iron  haematoxylin  preparations  the  head  length  of  the  wombat  sperm 
measured  from  the  distal  extremity  to  the  most  proximal  point  of  the  curvature  of 
the  hook  (i.e.  excluding  the  recurved  portion  of  the  hook)  is  about  5-7  /x  in  contrast 
to  8-0 /x  and  11-7/x  for  mouse  and  rat,  respectively  (Friend  1936).  Feulgen  pre- 
parations (with  or  without  fast  green  counterstain)  of  wombat  and  koala  sperm  have 
shown  that  nuclear  material  (DNA)  extends  to  the  tip  of  the  hook  and  occupies  all 
but  a  small  comma-shaped  acrosomal  portion  of  the  head.  Herein  lies  the  greatest 
departure  of  wombat  sperm  from  the  hooked  varieties  of  murid  sperm.  In  several 
microtine  species  the  hook  is  formed  entirely  from  a  proximal  extension  of  the  nuclear 
cap  (acrosome).  In  murine  sperm  a  hooked  portion  of  the  nucleus  bearing  a  rod 
extends  into  the  hooked  nuclear  cap  and  follows  its  contour  almost  to  its  proximal 
extremity  (Friend  1936). 

On  the  basis  of  skeletal  and  dental  structure  most  workers  consider  the  koala 
to  be  more  closely  related  to  the  ringtail  possums  of  the  genus  Pseudocheirus  than  the 
wombat  (Wood  Jones  1924;  Simpson  1945).  Comparisons  of  sperm  morphology  on 
which  selection  pressure  would  presumably  be  lower  than  that  for  external  characters 
of  an  animal  such  as  skeletal  or  dental  characters,  is  therefore  of  considerable  interest 
as  a  possible  basis  for  taxonomic  classification. 


138 


542  R.    L.    HUGHES 

Tt  can  be  seen  from  the  previous  descriptions  that  the  spermatozoon  oi  Pseudo- 
cheirus  peregrinus  is  not  intermediate  in  structure  between  the  more  typical  marsupial 
types  (Macropodidae  and  Dasyuridae)  and  those  of  the  highly  divergent  wombat  and 
koala.  On  the  contrary,  it  deviates  in  quite  a  difTerent  manner  from  the  typical 
marsupial  patterns.  The  head  is  broad  (3-8/x)  in  comparison  to  its  length  (5-9/^), 
the  anterior  end  lacks  a  hook  and  is  semi-circular  in  dorsal  view  (Plate  1,  Figs.  3  and  4). 
Other  distinguishing  features  are  the  shape  and  position  of  the  acrosome  previously 
mentioned  and  a  relatively  short  middle-piece  (6-9 /x).  The  view  that  the  koala  is 
more  closely  related  to  the  ringtail  possum  than  the  wombat  is  not  supported  by 
comparisons  of  sperm  morphology.  On  the  contrary,  the  findings  reported  here 
support  the  observations  of  Sonntag  (1923)  and  Troughton  (1957)  who  considered 
that  the  koala  shares  sufficient  characters  with  the  wombat  for  its  classification  along 
with  the  phalangers  to  be  rejected. 

V.  Acknowledgments 

The  author  wishes  to  express  his  sincere  thanks  to  Dr.  E.  H.  Hipsley,  Director, 
Institute  of  Anatomy,  Canberra;  to  J.  T.  Woods,  Queensland  Museum;  to  J.  A. 
Thomson,  Zoology  Department,  University  of  Melbourne;  to  Dr.  M.  E.  GriflSths, 
W.  E.  Poole,  K.  Keith,  M.  G.  Ridpath,  Division  of  Wildlife  Research,  CSIRO,  for 
material;  to  J.  Sangiau  and  L.  S.  Hall  for  technical  assistance;  to  E.  Slater  for 
photography;  and  to  Professor  K.  W.  Cleland  and  Dr.  A.  W.  H.  Braden  who  offered 
helpful  criticism. 

VI.  References 

Benda,  C.  (1897). — Neuere  Mittheilungen  iiber  die  Histiogenese  der  Saugethierspermatozoen.    Verh. 

berl.  physiol.  Ges.  1897.    [In  Arch.  Anat.  Physiol.  (Physiol.  Abt.)  1897:  406-14.) 
Benda,  C.  (1906). — Die  Spermiogenese  der  Marsupialier.  Denkschr.  med.-naturw.  Ges.  Jena6:  441-58. 
BiGGERS,  J.  D.,  and  Creed,  R.  F.  S.  (1962). — Conjugate  spermatozoa  of  the  North  American  opossum. 

Nature,  Lond.  196:  1112-3. 
Binder,  S.  (1927). — Spermatogenese  von  Macropus  giganteus.  Z.  Zellforsch.  5:  293-346. 
Bishop,  M.  W.  H.,  and  Austin,  C.  R.  (1957). — Mammalian  spermatozoa.   Endeavour  16:  137-50. 
Bishop,  M.  W.  H.,  and  Walton,  A;  (1960). — Spermatogenesis  and  the  structure  of  mammalian 

spermatozoa.    In  "Marshall's  Physiology  of  Reproduction".    (Ed.  A.  S.  Parkes.)  3rd  Ed. 

Vol.  1,  Pt.  2,  pp.  1-129.   (Longmans,  Green  and  Co.:  London.) 
Carleton,  H.,  and  Drury,  R.  A.  B.  (1957). — "Histological  Technique."  (Oxford  University  Press.) 
Cleland,  K.  W.  (1955). — Structure  of  bandicoot  sperm  tail.  Aust.  J.  Sci.  18:  96-7. 
Cleland,  K.  W.  (1956). — Acrosome  formation  in  bandicoot  spermiogenesis.    Nature,  Lond.  Ill: 

387-8. 
Cleland,  K.  W.  (1964). — History  of  the  centrioles  in  bandicoot  (Perameles)  spermiogenesis.  J.  Anat. 

98:487. 
Cleland,  K.  W.,  and  Lord  Rothschild  (1959). — The  bandicoot  spermatozoon:    an  electron 

microscope  study  of  the  tail.   Proc.  R.  Soc.  B  150:  24-42. 
Duesberg,  J.  (1920). — Cytoplasmic  structures  in  the  seminal  epithelium  of  the  opossum.   Carnegie 

Institute  Contributions  to  Embryology.  Vol.  9,  pp.  47-84. 
Friend,  G.  F.  (1936).— The  sperms  of  the  British  Muridae.   Quart.  J.  Micr.  Sci.  78:  419-43. 
Furst,  C.  M.  (1887). — Ueber  die  Entwicklung  der  Samenkorperchen  bei  den  Beutelthieren.    Arch. 

mikrosk.  Anat.  EntwMech.  30:  336-65. 
Hughes,  R.  L.  (1964). — Sexual  development  and  spermatozoon  morphology  in  the  male  macropod 

marsupial  Potorous  tridactylus  (Kerr).   Aust.  J.  Zool.  12:  42-51. 


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Jordan,  H.  E.  (1911). — The  spermatogenesis  of  the  opossum  {Didelphis  virginiana)  with  special 

reference  to  the  accessory  chromosome  and  the  chondriosomes.    Arch.  Zellforsch.  7:  41-86. 
KoRFF,  K.  VON  (1902). — Zur  Histogenese  der  Spermien  von  Phalangista  vulpina.    Arch,  mikrosk. 

Anat.  EntwMech.  60:  233-60. 
McCrady,  E.  (1938). — The  embryology  of  the  opossum.  Am.  Anat.  Mem.  16:  1-233. 
Pearse,  a.  G.  E.  (1961).— "Histochemistry."  (J.  &  A.  Churchill:   London.) 
Retzius,  G.  (1906). — Die  Spermien  der  Marsupialier.  Biol.  Unlers.  (N.  F.)  13:  77-86. 
Retzius,  G.  (1909).— Die  Spermien  von  Didelphis.   Biol.  Unfers.  (N.  F.)  14:  123-6. 
Selenka,  E.  (1887). — Studien  ijber  Entwickelungsgeschichte  der  Thiere.  Das  Opossum  (Didelphis 

virginiana).    Wiesbaden  1887,  pp.  101-72. 
Simpson,  G.  G.  (1945). — Principles  of  classification  and  a  classification  of  mammals.    Bull.  Am. 

Mas.  Nat.  Hist.  S5:  1-350. 
Sonntag,  C.  F.  (1923). — On  the  myology  and  classification  of  the  wombat,  koala  and  phalangers. 

Proc.  Zool.  Soc.  Lond.  1922:  683-895. 
Troughton,  E.  (1957). — "Furred  Animals  of  Australia."  6th  Ed.  (Angus  and  Robertson:   Sydney.) 
Waldeyer,  W.  (1902). — Die  Geschlechtszellen.  In  "Handbuch  der  vergleichend  und  experimentellen 

Entwickelungsgeschichte  der  Wirbelthiere".   Vol.  1,  Pt.  1,  pp.  86-476. 
Wilson,  E.  B.  (1928). — "The  Cell  in  Development  and  Heredity."   (Macmillan:   New  York.) 
Wood  Jones,  F.  (1924). — "The  Mammals  of  South  Australia."    Pt.  II.  (Govt.  Printer:    Adelaide.) 


Explanation  of  Plate  1 

Figures  1  and  2  are  photographs  of  Heidenhain's  iron-haematoxylin  preparations  from  formalin-fixed 

epididymal  material 

Fig.  1. — Phascolomis  mitchelli,  mature  epididymal  spermatozoon,  lateral  view. 

Fig.  2. — Rattus  norvegicus,  mature  epididymal  spermatozoon,  lateral  view. 

Fig.  3. — Pseudocheirus  peregrinus,  spermatozoon  head,   showing  centrally  placed  acrosomal  pit, 

dorsal  view. 
Fig.  4. — Pseudocheirus  peregrinus,  epididymal  spermatozoon,  lateral  view. 


140 


Hughes 


MORPHOLOGY  OF  SPERMATOZOA 


A 


Aust.  J.  ZooL,  1965,  13,  533-43 


Plate  1 


s 


141 


THE  GENITAL  SYSTEM  AND  THE  FETAL  MEMBRANES 
AS  CRITERIA  FOR  MAMMALIAN  PHYLOGENY  AND 

TAXONOMY 

By  H.  W.  Mobsman 

All  systems  of  classification  of  natural  phenomena  are  admittedly  imperfect 
because  these  phenomena  differ  from  one  another  in  such  infinitely  variable  de- 
grees that  it  is  impossible  to  divide  them  into  a  system  of  groupings  which  do 
not  frequently  overlap  or  intergrade.  It  is  also  absolutely  impossible  consistently 
to  select  morphological  criteria  for  a  scheme  of  classification  that  will  lend  them- 
selves to  the  assignment  of  a  series  of  ranks  such  as  species,  genera,  and  famiUes, 
in  one  group  that  ^vill  be  of  parallel  value  to  a  similar  series  assigned  to  another 
related  group.  Yet  in  spite  of  these  obviously  insurmountable  barriers  to  perfec- 
tion, convenience  and  orderliness  in  science  demand  that  classifications  be  made, 
and  that  their  categories  be  of  as  nearly  parallel  value  as  possible. 

Most  biologists  believe  that  the  best  basis  for  classification  is  phylogeny,  that 
is,  the  evolutionary  or  genetic  relationships  within  and  of  the  group.  This  is  so 
widely  accepted  that  practically  all  other  forms  of  classification  are  considered 
"artificial."  Although  artificial  classification  is  often  temporarily  necessary,  as 
in  tentatively  fitting  a  poorly  understood  entity  into  a  general  scheme,  still  a 
natural  or  phylogenetic  classification  should  always  be  the  ultimate  aim. 

Criteria  for  classification  of  any  group  should  therefore  be  characters  of 
phylogenetic  significance.  Furthermore  there  should  be  some  way  to  evaluate 
the  relative  significance  of  one  set  of  criteria  in  relation  to  another  set;  for  in- 
stance, dentition  as  compared  to  skull  proportions;  or  pelage  as  compared  to 
baculum.  There  should  also  be  some  method  for  determining  whether  a  given  set 
of  characters  is  suitable  for  separating  the  lower  categories  such  as  species  and 
genera,  or  the  higher  categories  such  as  famihes  and  orders. 

The  more  conservative  characters  obviously  will  be  of  greater  value  in  char- 
acterizing the  higher  categories,  while  the  less  conservative  will  only  be  of  use 
in  the  lower  categories.  The  presence  of  the  fetal  membranes  (amnion,  chorion, 
yolk  sac,  and  allantois)  is  a  highly  conservative  character  appearing  in  all  Am- 
niota.  Yet  certain  aspects  of  the  finer  morphology  of  the  placenta,  such  as 
whether  it  is  villous,  trabecular,  or  labyrinthine,  are  of  use  only  in  characterizing 
the  families  within  a  suborder,  for  example  the  Anthropoidea.  This  is  true  be- 

289 


142 


290  JOURNAL  OF  MAMMALOGY  Vol.  34,  No.  S 

cause  parallel  transitions  in  placental  morphology  are  known  to  occur  inde- 
pendently in  other  orders  not  closely  related  to  the  Anthropoidea  or  to  one 
another.  These  same  aspects  of  finer  morphology  are,  however,  too  conservative 
to  be  of  much  use  in  separating  genera  or  species,  there  being  very  slight  or  no 
differences  in  this  character  within  single  families  or  genera. 

The  relative  conservatism  of  biological  characters  is  based  on  two  entirely 
distinct  and  independent  thhigs.  The  first  is  the  human  factor,  or  simply  the 
question  of  generality  versus  particularity  of  concept.  The  greater  the  breadth 
or  inclusiveness  of  a  character  concept  the  more  conservative  it  is  within  its 
particular  field.  For  example,  the  character  "bony  skeleton"  is  much  broader 
and  therefore  much  more  conservative  than  the  character  "cranium",  w'hile 
the  latter  is  in  turn  much  broader  and  more  conservative  than  "zygoma."  We 
can  and  do  quite  properly  select  the  generalized  and  broader  characters  as 
criteria  for  separating  the  higher  categories,  and  the  more  narrow  and  particular 
ones  for  the  lower  subdivisions. 

Superimposed  on  this,  much  more  complex,  and  equally  as  important,  is  the 
second  or  biological  factor  in  determining  conservatism.  This  may  be  expressed 
as  the  degree  to  which  a  character  has  been  subjected  to  natural  selection. 

Assuming  equal,  intrinsic  genetic  factors,  it  is  certainly  true  that  the  more 
intimately  a  character  is  related  to  the  environment  the  more  rapid  and  exten- 
sive will  be  its  environmental  adaptations  during  the  course  of  evolution.  The 
main  thesis  of  this  discussion  rests  on  this  assumption.  It  is  maintained  that 
the  structural  characters  of  the  reproductive  tracts  and  fetal  membranes  of 
mammals,  because  they  have  been  largely  independent  of  environmental  selec- 
tion, show  relatively  little  evolutionary  divergence  as  compared  to  most  other 
organ  systems.  This  is  not  the  place  to  discuss,  statistically,  results  to  be  ex- 
pected in  the  evolution  of  a  genetically  variable  system  subjected  to  environ- 
mental selection  in  contrast  to  one  subjected  to  very  little  and  indirect  en- 
vironmental action.  However,  it  can  be  readily  understood  that  without  the 
selective  effects  of  differing  environments,  variations  would  tend  to  be  submerged 
because  of  continuous  selection  for  one  constant  set  of  environmental  conditions. 
A  race  under  these  conditions  would  become  more  and  more  stabilized  and 
specialized,  but  no  new  divergent  races  would  arise  from  it.  But  this  is  not  the 
situation  in  regard  to  a  genetically  variable  system,  such  as  the  fetal  membranes 
that  are  practically  isolated  from  any  direct  selective  effects  of  external  environ- 
ment. In  such  a  system,  in  this  case  the  fetal  membranes,  evolution  is  free  to 
proceed  along  almost  any  line  so  long  as  it  meets  certain  vital  requirements: 
(1)  the  supplying  of  a  means  of  maintaining  an  embryo  within  the  mother's 
uterus  until  mature  enough  to  be  bom;  (2)  structural  conditions  which  will 
allow  the  uterus  to  resume  a  normal  nonpregnant  state  after  delivery,  so  that 
another  pregnancy  may  ensue. 

Certainly  these  fundamental  requirements  are  far  from  simple  in  either  a 
structural  or  physiological  sense;  they  involve  extremely  complex  mechanisms. 
But  the  point  is  that  not  only  is  the  intrauterine  en\'ironment  relatively  con- 
stant in  mammals  generally,  but  so  are  the  requirements  for  maintenance  of  an 


143 


Aug.,  195S  MOBSMAN— TAXONOMIC  CRITERIA  291 

embryo  and  for  restorability  of  the  uterus  to  the  condition  for  beginning  another 
pregnancy. 

What  then  should  one  expect  of  the  evolution  of  an  organ  system,  such  as  the 
fetal  membranes,  largely  isolated  from  the  external  environment  and  charged 
with  a  highly  complex  job  to  do,  but  one  which  is  fundamentally  the  same  in  all 
members  of  the  group,  in  this  case  the  Subclass  Eutheria?  It  seems  that,  regard- 
less of  rate  of  genetic  variation  of  the  system,  divergence  would  be  relatively 
slow  and  narrow,  and  that  intergradation  would  be  the  rule,  there  being  slight 
environmental  selection,  and  little  race  isolation  due  directly  to  adaptive  varia- 
tions in  this  system  itself.  But  while  this  type  of  evolution  would  be  taking 
place  in  an  environmentally  independent  organ  system,  the  group  of  organisms 
in  which  the  organ  system  existed  could  nevertheless  be  undergoing  the  usual 
evolutionary  course  in  its  other  organ  systems:  diverging  widely  in  adaptation 
to  environmental  niches  old  or  new;  losing  species  or  whole  major  groups  by 
extinction;  in  short,  becoming  the  widely  divergent,  often  aberrant  or  isolated 
groups  that  are  characteristic  of  mammals  at  the  present  time. 

Such  an  environmentally  isolated  system  must  then  be  very  conservative  in 
its  characters  as  compared  to  those  organ  systems  related  closely  to  the  environ- 
ment and  therefore  subject  to  intense,  adaptive  evolution.  The  characteristics  of 
such  a  system  should  vary  relatively  little  between  major  groups,  and  almost 
none  between  closely  related  minor  categories.  This  lack  of  divergence  should 
make  it  possible  to  detect  common  characteristics  among  groups  widely  sepa- 
rated from  one  another  in  other  characteristics,  whether  this  be  due  to  adapta- 
tions to  divergent  environments,  or  to  extinction  of  intergrading  groups.  Con- 
versely, dissimilarity  in  characters  of  a  conservative  organ  system  should  be  good 
evidence  of  lack  of  close  phylogenetic  relationship. 

It  is  generally  conceded  that  similarity  of  more  conservative  characters  be- 
tween two  forms  is  better  evidence  of  close  relationship  than  similarity  of  less 
conservative  characters.  Whether  lack  of  conservatism  is  due  to  more  intensive 
environmental  selection  or  to  a  combination  of  this  with  such  things  as  more 
intensive  sexual  selection,  or  greater  innate  potential  of  genetic  variability,  there 
is  more  chance  that  similarities  in  less  conservative  characteristics  are  due  to 
evolutionary  parallelism  or  convergence.  In  estimating  phylogenetic  relation- 
ship it  is  therefore  extremely  important  to  know  which  are  the  more  conserva- 
tive organ  systems  and  to  give  their  characters  the  greater  weight.  It  is  also  im- 
portant to  evaluate  the  various  characters  of  such  an  organ  system  to  determine 
which  are  the  more  conservative  within  the  system.  The  more  conservative  will 
serve  to  characterize  the  higher  categories,  the  less  only  the  lower  ones. 

The  foregoing  discussion  largely  reiterates  generally  recognized  principles 
which  have  been  used  for  years  by  students  of  evolution  and  taxonomy.  How- 
ever it  seemed  best  to  restate  them  here  since  the  chief  purpose  of  this  paper  is 
to  point  out  that  the  reproductive  tracts  and  fetal  membranes  of  mammals  are 
conservative  systems  which  have  never  been  adequately  used  in  phylogenetic 
and  taxonomic  studies  of  this  group.  It  will  be  shown  that  the  relative  conserva- 
tism of  the  various  features  of  these  organ  systems  can  be  estimated  and  the 


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characters  used  as  criteria  in  proper  relation  to  their  significance.  It  is  now  best 
to  proceed  to  specific  examples.  The  first  concerns  the  male  genital  tract  of  the 
Sciuridae. 

In  1923,  Pocock  pointed  out  the  marked  difference  between  the  male  external 
genitalia  of  Tamiasciurus  and  Sciurus  and  separated  the  two  genera  on  this 
basis.  In  1932,  Mossman,  Lawlah,  and  Bradley  published  a  more  detailed  study 
of  the  tracts  of  Sciurus  carolinensis,  S.  niger,  Tamias  striatus,  Citellus  tridecem- 
lineatus,  Glaucomys  volans,  and  Tamiasciurus  hudsonicus.  They  showed  that  the 
typical  sciurid  male  tract  as  seen  in  all  these  genera  (except  Tamiasciurus),  and 
as  also  described  by  KroUing  (1921)  in  Sciurus  vulgaris,  is  characterized  by  a 
unique  arrangement  of  the  ducts  of  the  bulbo-urethral  glands.  Tullberg  (1899) 
gave  enough  information  on  several  other  genera  to  indicate  the  probability 
that  they  also  have  this  same  character,  and  Oudemans  (1892)  made  it  fairly 
clear  that  Petaurista  petaurista  is  essentially  like  Sciurus.  So,  with  the  exception 
of  Tamiasciurus,  other  sciurids  so  far  as  known  have  a  pair  of  large  bulbo- 
urethral glands  drained  by  a  pair  of  voluminous  ducts  which,  upon  entering  the 
sheath  of  the  corpus  cavernosum  urethrae  in  the  bulb  region,  become  highly 
modified  to  form  another  accessory  organ,  the  bulbar  gland.  This  whole  com- 
plex is  then  drained  by  a  single  long  glandular  duct,  the  penile  duct,  w^hich  lies 
ventral  to  the  urethra  throughout  almost  the  entire  length  of  the  corpus  cav- 
ernosum urethrae,  finally  entering  the  urethra  at  approximately  the  base  of  the 
glans.  The  author  has  examined  some  other  genera,  including  Marmota  and 
Heliosciurus  and  has  found  them  also  fundamentally  like  this. 

At  the  same  time  we  showed  that  Tamiasciurus,  the  red  squirrel  or  chickaree, 
possesses  an  entirely  different  type  of  bulbo-urethral  gland  and  duct.  It  has  no 
bulbar  gland  and  no  penile  duct.  It  does  have  a  urethral  sinus  in  the  bulb  much 
like  that  of  some  Muridae.  Later  it  was  shown  that  the  female  tract  of  the 
chickarees  is  also  unique,  the  vagina  being  extremely  long  and  coiled  while  that 
of  all  other  Sciuridae  studied  is  short  and  broad  (Mossman,  1940).  Other  peculiar 
features  of  the  male  tract  of  the  chickarees,  such  as  the  long  filiform  penis  and 
the  absence  of  a  baculum,  were  also  pointed  out  at  that  time.  (Layne  (1952)  has 
shown  that  Tamiasciurus  does  possess  a  minute  baculum  averaging  only  .26  mm, 
in  length  in  adults.  Pocock  and  the  author  both  failed  to  note  this  structure.) 

A  recent,  and  as  yet  unpublished  manuscript  by  Mr.  M.  R.  N.  Prasad  of 
Central  College,  Bangalore,  India  entitled,  "Male  genital  tract  of  two  genera  of 
Indian  squirrels,"  presents  excellent  descriptions  of  the  palm  squirrel,  Funam- 
bulus  palmarum  palmarum  Linn.,  and  of  the  giant  Malabar  squirrel,  Ratufa 
indica  maxima  Schreb.  Ratufa  has  the  typical  sciurid  tract,  but  F.  palmarum 
is  hke  Tamiasciurus  in  having  minute  Cowper's  glands  and  no  bulbar  gland  or 
penile  duct.  Obviously  this  indicates  close  relationship  between  this  species  and 
the  Tamiasciurinae,  and  poses  a  number  of  interesting  questions  in  regard  to 
sciurid  phylogeny  and  geographic  distribution,  to  say  nothing  of  the  doubt  it 
throws  on  the  present  taxonomy  of  the  whole  group. 

Although  the  nature  of  the  reproductive  tracts  of  most  of  the  genera  of  squir- 
rels is  still  unknown,  enough  knowledge  is  available  to  make  it  seem  very  prob- 


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Aug.,  195S  MOBSMAN— TAXONOMIC  CRITERIA  293 

able  that  instead  of  a  wide  range  of  types  within  the  family,  there  are  at  least 
two  fundamentally  different  types.  This  seems  probable  as  it  is  definitely  known 
that  at  least  one  genus  of  three  of  the  six  tribes  that  Simpson  (1945)  includes 
under  the  subfamily  Sciurinae  has  the  typical  male  sciurid  tract;  and  that  two 
genera  of  his  second  subfamily,  Petauristinae,  also  are  typical.  One  can  raise 
the  question  then  as  to  the  logic  in  placing  the  chickarees  and  Funambulini  as 
tribes  of  the  subfamily  Sciurinae  when  the  reproductive  tracts  of  Tamiasciurus 
and  F.  p.  palmarum  are  so  different  from  others  of  this  group.  Also,  in  view  of 
Prasad's  work,  F.  p.  palmarum  and  Ratufa  should  not  be  in  the  same  tribe  with 
one  another.  Furthermore,  it  is  illogical  to  place  the  chickarees  and  Funambulus 
in  these  subgroups  and  at  the  same  time  to  put  Petaurista  and  Glaucomys  in  a 
separate  subfamily,  although  their  genital  tracts  are  almost  identical  to  that 
of  Sciurus.  Obviously  the  flying  squirrels  (Petauristinae)  have  been  separated 
on  the  basis  of  petagial  characters;  but  these  must  be  highly  subject  to  environ- 
mental selection,  hence  nonconservative.  Very  similar  petagial  characters  have 
been  developed  in  certain  marsupials  (Acrohates  and  Petaurus),  and  in  other 
Eutheria,  namely  in  the  Dermoptera,  and  in  the  Anomaluroidea  among  the  ro- 
dents. Of  course  one  could  ask  if  similar  reproductive  tract  characters  may  not 
also  have  developed  in  widely  unrelated  groups.  There  is  no  evidence  that  this 
is  true,  but  it  must  be  admitted  that  the  data  are  insufficient.  This  in  itself  should 
be  a  challenge,  to  those  who  ask  the  question,  to  make  an  effort  to  gather  the 
information. 

There  may  be  those  who  will  still  fall  back  on  the  fundamental  question  of 
whether  the  genital  tract  characters  are  more  conservative  than  others  in  the 
Sciuridae.  If  they  will  allow  the  ruling  out  of  the  genus  Tamiasciurus  and  the 
species  Funambulus  p.  palmarum  as  members  of  the  family,  then  one  can  cite 
the  fact  that  the  genital  tracts  of  Sciurus,  Tamias,  Citellus,  Marmota,  Ratufa, 
and  Glaucomys  are  the  same  in  fundamentals,  and  indeed  very  similar  even  in 
details,  while  there  is  great  divergence  between  these  various  genera  in  body 
form,  pelage,  feet,  ears,  skeleton,  skull,  and  teeth.  If  one  is  not  willing  to  allow 
the  ruling  out  of  the  chickaree  group,  and  F.  p.  palmarum,  then  in  the  face  of 
the  apparent  aberrance  of  these  he  is  bound  to  withhold  judgment  until  someone 
can  show  whether  or  not  there  are  intergrading  forms,  so  far  as  male  genitals 
are  concerned,  between  them  and  the  typical  sciurids.  If  there  are,  then  perhaps 
the  genitals  are  not  as  conservative  as  they  now  seem. 

There  are  a  few  minor  characters  of  male  genital  tracts  that  are  variable 
enough  in  some  groups  to  be  of  use  in  separating  species  of  a  single  genus.  Howell 
(1938)  pubhshed  a  plate  showing  the  bacula  of  several  species  each  from  the 
genera  Eutamias,  Citellus,  and  Sciurus.  There  are  fairly  obvious  intrageneric 
differences  between  these  bones  within  each  of  the  three  genera,  although  oc- 
casionally in  two  species  they  are  practically  identical  (Sciurus  carolinensis  and 
niger).  It  is  probable  that  there  are  other  features  of  the  male  genitals  which 
would  show  intrageneric  differences:  certainly  differences  in  the  glans  penis  cor- 
related with  those  of  the  bacula  would  be  expected.  However,  appreciable  intra- 
generic, species  differences  in  the  internal  genitaha  of  either  the  male  or  female 


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294  JOURNAL  OF  MAMMALOGY  Vol.  S4,  No.  S 

have  never  been  noted  by  the  author  in  the  sciurids  or  other  groups,  but  inter- 
generic  differences  are  the  rule,  and  are  often  rather  extensive;  for  example 
between  Tamias,  Citellus,  and  Sdurus  (Mossman,  Lawlah  and  Bradley,  1932). 

To  the  author's  knowledge,  no  attempt  has  ever  been  made  to  compare  the 
reproductive  tract  at  the  level  of  the  higher  categories.  It  seems  doubtful  that 
such  clearcut  indications  of  relationship  would  be  found  as  occur  in  the  case  of 
the  fetal  membranes,  where,  for  example,  considerable  affinity  is  shown  be- 
tween the  Artiodactyla,  Perissodactyla,  and  Cetacea;  and  between  the  Fis- 
sipedia  and  Pinnipedia.  Before  such  a  study  would  be  sound,  a  thorough  investi- 
gation of  the  various  genera  and  families  of  several  well-defined  orders  should  be 
made,  in  order  to  evaluate  the  conservativeness  of  the  various  genital  tract 
features. 

The  female  genital  tract  characters  are  probably  about  as  equally  conserva- 
tive as  those  of  the  male,  but  those  of  the  female  are  in  general  more  difficult  to 
observe  and  define.  A  good  example  of  this  is  the  os  clitoridis  or  baculum,  which 
in  recent  years  has  been  demonstrated  in  females  of  several  species,  leading  one 
to  expect  that,  where  present  in  the  male,  it  probably  also  occurs  in  the  female. 
This  female  element  may  show  intrageneric  differences  like  its  male  homolog, 
but  the  fact  that  it  is  usually  so  small  and  so  obviously  rudimentary  argues 
against  its  value  as  a  character  for  taxonomic  purposes.  The  other  characters  of 
the  female  external  genitalia  are  also  relatively  indefinite  and  difficult  to  ob- 
serve. Female  internal  genitalia  show  a  few  very  definite  features  which  could 
be  of  considerable  use,  but  they  are  almost  always  too  conservative  for  intra- 
generic taxonomy,  in  fact  in  most  cases  they  are  of  use  only  in  separating  groups 
higher  than  genera.  For  instance,  the  form  of  the  uterus,  oviduct,  and  ovary  is 
almost  identical  in  the  Cervidae  and  Bovidae.  The  Mustelidae,  Procyonidae, 
and  Ursidae  have  a  peculiar  configuration  of  the  oviduct  in  relation  to  the 
ovary  and  ovarian  bursa  that  is  highly  characteristic  and  differs  very  little  be- 
tween the  three  families.  The  Heteromyidae  and  Geomjddae  likewise  have  a 
characteristic  oviduct  pattern  which  is  practically  identical  in  the  two  groups. 
By  and  large  then,  it  may  be  said  that  the  characters  of  the  female  internal 
genitalia  are  very  conservative,  but  usually  rather  obscure  and  difficult  to 
observe. 

Comparative  studies  of  the  microscopic  anatomy  of  the  ovaries  have  revealed 
no  case  where  obvious  intrageneric  differences  exist,  except  those  due  to  differ- 
ences in  body  size  of  the  species.  However  some  intergeneric  differences  in 
microscopic  structure  do  occur:  for  example;  ovaries  of  mature  females  of  Syl- 
vilagus  and  Lepus  are  rather  easily  distinguished  from  one  another,  but  those  of 
Lepus  and  Oryctolagus  would  be  difficult;  Citellus  and  Sdurus  are  separable, 
but  Sdurus  and  Tamias  are  alike,  except  for  size.  When  one  reaches  the  higher 
categories  such  as  families  and  orders,  then  microscopic  features  become  char- 
acteristic for  each  group.  All  the  mustelids  examined  have  a  very  similar  and 
tjrpical  interstitial  cell  pattern:  this  includes  Maries  americana,  Taxidea  taxus, 
Mephitis  mephitis,  Spilogale  interrupta,  and  Mustela  vison,  dcognani,  frenata,  and 
putorius.  There  are  even  examples  of  striking  similarity  in  microscopic  structure 


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Aug.,  1953  MOBSMAN— TAXONOMIC  CRITERIA  295 

between  related  families,  at  least  so  far  as  the  few  genera  of  each  studied  are  an 
indication.  Examples  of  this  are  Ursidae  and  Procyonidae,  Cervidae  and  Bovidae, 
and  Erethizontidae  and  Dasyproctidae. 

Let  us  now  turn  our  attention  briefly  to  the  fetal  membrane  characters  of  the 
Sciuridae  (Mossman,  1937;  Mossman  and  Weisfeldt,  1939).  It  is  not  necessary 
to  enter  into  a  detailed  description  of  the  sciurid  membranes  and  placentation, 
as  the  main  point  to  be  made  is  that  these  are  even  more  conservative  characters 
than  the  male  genital  system  of  the  group.  So  it  is  not  surprising  that  in  all  the 
genera  studied,  including  Tamiasciurus,  the  fetal  membranes  are  practically  the 
same,  differing  only  in  minor  details.  These  include  all  the  genera  mentioned  in 
connection  with  the  male  genitals,  except  Heliosciurus  and  Petaurisia,  and  two 
others  in  addition,  Cynomys,  Xerus  (Rau,  1925).  In  fact  the  membranes  and 
placenta  of  Aplodontia  are  distinctly  sciuroid,  although  the  male  genitals  lack 
the  bulbar  gland  and  penile  duct. 

It  appears  then  that  the  criteria  of  the  male  and  female  reproductive  tracts 
and  the  fetal  membranes  could  be  applied  to  advantage  in  determining  the 
phylogenetic  relations  of  the  Sciuridae,  and  consequently  in  estabhshing  a  more 
logical  taxonomy  of  this  group.  The  fetal  membrane  characters  are  even 
more  conservative  criteria  than  those  of  the  male  or  female  genital  tracts. 

The  application  of  the  genital  tract  and  fetal  membrane  criteria  in  the  phy- 
togeny and  taxonomy  of  the  Sciuridae  has  been  discussed  first,  since  it  is  the 
only  group  in  which  the  author  has  made  reasonably  comprehensive  studies  of 
both  systems.  Little  has  been  said  thus  far  of  the  evaluation  of  specific  criteria, 
as  the  studies  of  the  male  tract  in  such  a  small  group  do  not  lend  themselves  to 
adequate  analysis.  The  author  has  however  made  extensive  comparative  studies 
of  mammalian  fetal  membranes  and  believes,  that  for  them,  the  basis  is  broad 
enough  to  enable  clearly  reliable  estimates  to  be  made  of  the  relative  value  of 
the  different  characters  involved.  Since  this  subject  was  presented  fully  in  his 
1937  monograph,  it  is  not  necessary  to  repeat  the  details  here.  Suffice  it  to  point 
out  that  all  the  descriptions  of  the  fetal  membranes  of  specific  species  which 
have  appeared  in  the  literature  since  then,  and  all  of  the  numerous  additional 
observations  of  the  author,  bear  out  the  thesis  proposed  at  that  time.  The  facts 
derived  from  these  studies  can  be  stated  very  simply. 

1.  In  every  group  of  mammals,  high  or  low  in  category,  in  which  the  members 
can  be  clearly  related  to  one  another  on  the  basis  of  total  anatomical  similarity, 
their  fetal  membranes  are  fundamentally  similar,  showing  far  less  divergence 
than  do  other  characters.  These  groups  are  perhaps  best  illustrated  by  the  orders 
Lagomorpha,  Rodentia,  Carnivora,  and  Artiodactyla;  by  the  suborders  Micro- 
chiroptera,  Lemuroidea,  and  Anthropoidea;  by  the  families  Tenrecidae,  Sorici- 
dae,  Talpidae,  Cebidae,  Cercopithecidae,  Pongidae,  Das5T)odidae,  Sciuridae, 
Heteromyidae,  Geomyidae,  Muridae,  Canidae,  Mustelidae,  Felidae,  Cervidae, 
and  Bovidae;  and  by  numerous  genera  in  these  and  some  other  families.  All 
these  groups  consist  of  anatomically  closely  related  forms  and  all  have  even 
closer  fetal-membrane  affinities.  They  are  used  as  illustrations  because  enough 
is  known  about  the  fetal  membranes  of  enough  members  of  each  group  to  make 


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296  JOURNAL  OF  MAM^IALOGY  Vol.  S4,  No.  S 

it  reasonably  certain  that  the  above  statement  is  true.  There  are  other  ana- 
tomically homogeneous  groups  such  as  the  Megachiroptera,  Cetacea,  and  Peris- 
sodactyla  where  the  limited  data  available  points  in  the  same  direction.  This  is 
particularly  true  of  the  data  on  the  species  of  numerous  genera  of  the  groups 
already  mentioned. 

2.  In  many  groups  of  mammals  made  up  of  subgroups  widely  divergent  or  of 
uncertain  affinities  there  are  fundamental  differences  in  the  fetal  membranes. 
This  is  true  of  the  Insectivora;  the  Chiroptera,  where  there  is  wide  divergence 
between  the  membranes  of  the  two  suborders  (Microchiroptera  and  Mega- 
chiroptera); the  Primates,  where  the  membranes  of  Lemuroidea  and  Tarsoidea 
differ  widely  from  one  another  and  from  the  Anthropoidea;  and  the  Edentata, 
where  the  Bradipodidae  and  Myrmecophagidae  are  probably  much  alike,  but 
differ  markedly  from  the  Dasypodidae.  The  Pholidota,  often  included  in  the 
order  Edentata,  differ  fundamentally  from  all  others  of  this  order. 

3.  The  membranes  of  certain  groups  commonly  separated  on  anatomical 
grounds,  but  known  to  be  somewhat  related,  are  often  so  similar  that  the  wide- 
ness  of  separation  does  not  seem  justified.  This  is  true  of  the  Pongidae  and 
Hominidae,  the  Lagomorpha  and  Rodentia,  and  of  the  Perissodactyla  and 
Artiodactyla. 

4.  There  are  fundamental  similarities  between  certain  aberrant  groups  and 
other  groups  to  which  they  have  not  been  supposed  to  be  clearly  related.  Strik- 
ing examples  of  this  are  the  strong  resemblances  between  the  membranes  of  the 
Brady podidae  and  the  Anthropoidea;  between  the  Lemuroidea,  Pholidota,  Ceta- 
cea, and  Sirenia  and  those  of  the  Perissodactyla  and  Artiodactyla;  and  between 
the  Dasypodidae,  Rodentia,  Microchiroptera  and  Soricoidea. 

More  data  than  are  at  present  available  are  certainly  necessary  to  warrant 
drawing  more  than  very  tentative  conclusions  as  to  the  significance  or  non- 
significance  of  these  facts,  but  it  is  interesting  to  note  that  there  are  many 
points  of  anatomical  resemblance  between  lemurs  and  the  hoofed  animals,  and 
between  the  sloths  and  anthropoids.  Certainly  taxonomists  should  not  close 
their  minds  to  the  possibility  that  lemurs  are  an  arboreal  line  derived  from  stock 
ancestral  to  the  hoofed  animals,  and  that  their  relatively  slight  resemblance  to 
anthropoids  is  due  to  retention  of  primitive  characters  in  both  lines,  and  to 
convergence  and  parallelism  effected  by  adaptation  of  both  to  an  arboreal 
habitat.  Nor  should  one  close  his  mind  to  the  possibility  that  the  sloths  repre- 
sent highly  specialized  edentulous  forms  derived  from  the  same  ancestral  stock 
as  the  anthropoids. 

Now  that  the  general  method  of  application  of  the  reproductive  tract  and 
fetal  membrane  criteria  to  the  taxonomy  and  phylogeny  of  mammals  has  been 
described  and  illustrated,  one  must  clear  up  the  important  point  of  the  evalua- 
tion of  the  criteria  used.  The  basis  for  this  is  the  observation  described  as  number 
1  above ;  namely,  that  in  every  group  of  mammals  in  which  the  members  can  be 
clearly  related  to  one  another  on  the  basis  of  total  anatomical  similarity  their 
fetal  membranes  are  fundamentally  similar,  showing  far  less  divergence  than 
do  other  characters.  This  makes  it  possible  to  compare  the  variability  of  differ- 


149 


Aug.,  19BS  MOSSMAN— TAXONOMIC  CRITERIA  297 

ent  features  of  the  membranes  within  the  group  as  a  whole  and  within  its  various 
lesser  taxonomic  categories,  as  was  done  by  the  author  some  years  ago  (Moss- 
man,  1937).  Those  characters  which  are  consistently  constant  throughout  all 
the  subgroups  of  a  major  category  certainly  are  the  more  conservative  ones  of 
that  group.  If  the  same  characters  are  also  constant,  but  not  necessarily  alike, 
throughout  several  well  established  orders,  then  they  are  certainly  characters 
conservative  enough  to  be  used  for  establishing  phylogenetic  relationships  be- 
tween orders.  If  they  are  constant  within  single  families,  but  vary  between  differ- 
ent families  of  an  order,  then  they  are  only  conservative  enough  to  establish 
relationship  between  families.  This  general  principle  can  be  applied  to  all  cate- 
gories. Obviously  one  must  choose  test  groups  in  which  the  taxonomy  is  quite 
clear  and  definite,  and  must  compare  parallel,  major  groups  in  which  the  minor 
categories  are  also  reasonably  parallel  in  value.  This  is  obviously  arguing  in  a 
circle,  and  thus  a  dangerous  practice  if  not  tempered  with  good  judgment  and  a 
reasonable  scientific  conservatism  on  the  part  of  the  person  using  it.  However 
it  is  the  best  method  available,  and  far  superior  to  making  no  attempt  at  evalua- 
tion. 

One  further  argument  in  favor  of  the  fetal  membranes  as  criteria  for  phy- 
logeny  must  be  stated.  This  point  seems  even  more  important  than  that  of  their 
conservatism.  In  fact,  coupled  with  their  conservatism,  it  makes  them  the  most 
ideal  of  all  anatomical  criteria  for  recent  forms.  This  is  the  fact  that  the  history 
of  the  development  of  the  fetal  membranes  of  a  species  is  the  history  of  a  com- 
plete, complex,  and,  structurally,  highly  independent  organ  system,  from  its 
inception  during  cleavage  to  its  complete  functional  maturity,  old  age,  and  death 
at  the  time  of  birth  of  the  young.  We  are  therefore  dealing  with  the  complete 
life  history  of  an  organ  system  carried  out  in  the  relatively  constant  environment 
of  the  uterus,  thus  almost  completely  isolated  from  adaptational  demands  of 
the  varying  external  environment.  Other  criteria  conmionly  used  do  not  offer 
this  overall  picture  of  the  individual.  The  fetal  membranes  and  their  develop- 
ment are  comphcated,  but  far  less  so  than  the  total  history  of  all  the  organ  sys- 
tems ordinarily  used  as  criteria.  Their  conservatism,  and  the  total  develop- 
mental picture  that  they  give,  render  them  the  most  ideal  of  all  organ  systems 
for  phylogenetic  and  taxonomic  studies  of  recent  mammals, 

SUMMARY 

When  compared  with  the  organ  systems  ordinarily  employed  as  criteria  for 
taxonomic  and  phylogenetic  studies  of  manmials,  the  characters  of  the  male 
and  the  female  reproductive  systems  and  of  the  fetal  membranes  are  the  more 
conservative.  This  is  apparently  due  to  the  relatively  minor  role  that  adaptation 
to  external  environment  has  played  in  the  evolution  of  these  systems. 

Little  effort  has  ever  been  made  to  apply  male  and  female  genital  tract  char- 
acters to  such  studies  of  mammals,  but  a  limited  consideration  of  them  by  the 
author  indicates  that  they  are  less  conservative  than  the  fetal  membranes.  They 
furnish  characters  that  are  of  use  in  the  study  of  the  interrelationships  of  genera 
and  families,  and,  in  some  cases,  even  of  species.  Whether  or  not  they  would  be 


150 


298  JOURNAL  OF  MAMMALOGY  Vol.  S4,  No.  S 

reliable  in  showing  affinities  between  higher  categories,  such  as  orders  and  sub- 
orders, is  unknown. 

On  the  contrary,  the  fetal  membranes  are  so  conservative  that  clear-cut  inter- 
specific or  even  intergeneric  differences  seldom  exist.  Furthermore  interorder 
and  interfamily  fetal-membrane  similarities  often  demonstrate  relationships 
between  these  major  groups.  This  conservatism,  plus  the  fact  that  the  complete 
life  cycle  of  the  fetal  membranes  takes  place  during  embryonic  development 
and  is  therefore  much  more  easily  studied  than  that  of  any  other  organ-system 
ontogeny,  makes  this  system  the  most  ideal  of  all  criteria  for  the  study  of  phy- 
logenetic  interrelationships  of  recent  mammals. 

Acknowledgement. — This  study  was  aided  by  grants  from  the  Wisconsin  Alumni 
Research  Foundation. 

LITERATURE  CITED 

Howell,  A.  H.  1938.  Revision  of  the  North  American  ground  squirrels  with  a  classifica- 
tion of  the  North  American  Sciuridae.  U.  S.  D.  A.,  N.  Amer.  Fauna,  No.  56: 
1-256. 

Kbolling,  O.  1921.  Die  akzessorischen  Geschlechtsdriisen  und  mannlichen  Kopula- 
tionsorgane  von  Sciurus  vulgaris.  Zeitschr.  f.  Anat.  u.  Entwick.,  61:  402-438. 

Layne,  J.  N.  1952.  The  os  genitale  of  the  red  squirrel,  Tamiasciurus.  Jour.  Manam., 
33:  457-459. 

Mobsman,  H.  W.  1937.  Comparative  morphogenesis  of  the  fetal  membranes  and  ac- 
cessory uterine  structures.  Contribs.  Embry.,  158;  Publ.  479,  Carnegie  Inst, 
Washington,    129-246. 

1940.    What  is  the  red  squirrel?  Trans.  Wis.  Acad.  Sci.,  Arts  &  Letters,  32: 

123-134. 

Mobsman,  H.  W.,  J.  W.  Lawlah,  and  J.  A.  Bradley.  1932.  The  male  reproductive  tract 
of  the  Sciuridae.  Amer.  Jour.  Anat.,  51:  89-155. 

MossMAN,  H.  W.,  AND  L.  A.  Weisfeldt.  1939.  The  fetal  membranes  of  a  primitive  ro- 
dent, the  thirteen-striped  ground  squirrel.  Amer.  Jour.  Anat.,  64:  59-109. 

Oudemans,  J.  T.  1892.  Die  accessorischen  Geschlechtsdriisen  der  Saugetiere.  Natuurkun- 
dije  Verhandelingen  van  de  Hollandsche  Maatschappij  der  Wetenschappen. 
3de  Verz.,  Deel  5,  2de  Stuk.,  1887-1892. 

PococK,  R.  I.  1923.  The  classification  of  the  Sciuridae.  Proc.  Zool.  Soc.  Lond.,  1:  209- 
246. 

Rau,  a.  S.  1925.  Contributions  to  our  knowledge  of  the  structure  of  the  placenta  of 
Mustelidae,  Ursidae,  and  Sciuridae.  Proc.  Zool.  Soc.  London,  1925:  1027-1070. 

Simpson,  G.  G.  1945.  The  principles  of  classification  and  a  classification  of  mammals. 
Bui.  Amer.  Mus.  Nat.  Hist.,  85:  350  p. 

Tullberg,  T.  1899.  Ueber  das  System  der  Nagetiere.  Nova  Acta  Reg.  Soc.  Upsala,  ser. 
3,  18:  1-514. 

Department  of  Anatomy,  University  of  Wisconsin,  Madison.  Received  December  26,  1952. 


151 


MORPHOLOGY  AND  PHYLOGENY  OF  HAIR 

By  Charles  R.  Noback* 

Department  of  Anatomy,  College  of  Physicians  and  Surgeons,  Columbia  University, 

New  York 

Hair  is  a  structure  found  exclusively  in  mammals.  With  this  in  mind, 
Oken  named  the  Mammalia,  Trichozoa  (hair  animals),  and  Bonnet  (1892) 
named  them  Pilifera  (hair  bearers). 

Of  the  many  aspects  of  morphology  and  phylogeny  of  hair,  only  four  will 
be  discussed.  These  include  (1)  the  principle  of  the  arrangement  of  hairs  in 
group  patterns,  (2)  the  types  of  hair  and  their  relation  to  the  principle  of 
the  group  pattern,  (3)  a  brief  analysis  of  the  structural  elements  of  hair  and 
their  relation  to  the  types  of  hair,  and  (4)  the  phylogeny  of  hair,  with  some 
remarks  on  (a)  the  relation  of  hair  to  the  epidermal  derivatives  of  other 
vertebrate  classes  and  (b)  aspects  of  the  phylogeny  of  the  hair  and  wool  of 
sheep  to  illustrate  that  marked  dififerences  in  hair  coats  exist  between  closely 
related  animals. 

Hair  is  the  subject  of  a  voluminous  literature.  Toldt  (1910,  1912,  1914, 
and  1935),  Danforth  (1925a),  Pinkus  (1927),  Pax  and  Arndt  (1929-1938), 
Trotter  (1932),  Lochte  (1938),  Smith  and  Glaister  (1939),  and  Stoves 
(1943a)  discuss  the  problem  of  mammalian  hair  in  general.  Wildman 
(1940),  von  Bergen  and  Krause  (1942),  and  the  American  Society  for 
Testing  Materials  (1948)  discuss  the  problem  of  fiber  identification  as 
applied  to  textiles. 

Principle  of  the  Group  Pattern  of  Hairs 

In  the  only  extensive  survey  of  the  grouping  of  hair  in  mammals,  DeMei- 
jere  (1894)  documented  the  concept  of  the  group  pattern  of  hair  (figures 
1-6).  Unfortunately,  the  few  studies  on  this  phase  of  the  problem  since 
that  time  have  not  fully  exploited  the  implications  of  this  concept.  DeMei- 
jere  concluded  that  hairs  are  mainly  arranged  in  groups  with  the  pattern  of  3 
hairs — with  the  largest  hair  in  the  middle — as  the  basic  pattern.  The 
concept  of  the  basic  trio  as  the  primitive  condition  is  accepted  as  an  ade- 
quate working  hypothesis  by  Wildman  (1932),  Galpin  (1935),  Hofer  (1914), 
Gibbs  (1938),  Hardy  (1946),  and  others.  DeMeijere  described  8  patterns: 
(1)  3  or  less  hairs  behind  each  scale  of  the  tail  (as  in  the  opossum,  Didelphis 
marsupialis),  (2)  more  than  3  hairs  behind  each  scale  of  the  tail  (as  in  the 
rodent,  Loncheres  [Echimys]  cristata),  (3)  3  hairs  (as  in  the  back  of  the 
marmoset,  Midas  rosalia),  (4)  more  than  3  hairs  arranged  in  a  regular 
pattern  with  some  of  greater  diameter  than  others  (as  in  the  back  hairs  of 
Loncheres  [Echimys]  cristata  in  figure  3),  (5)  several  hairs  composed  of  a 
number  of  fine  hairs  and  one  coarse  hair  (as  in  the  back  of  the  dog,  Canis 
familiaris,  in  figure  5D),  (6)  several  hairs  composed  of  a  number  of  fine 
hairs  and  one  isolated  coarse  hair  (as  in  the  back  hairs  of  the  mouse,  Mus 
decumanus,  in  figure  6D),  (7)  scatterings  of  fine  hairs  with  no  apparent 

*  The  author  wishes  to  thank  Dr.  Margaret  Hardy,  Division  of  Animal  Health  and  Production,  Sydney, 
Australia,  for  her  valuable  suggestions. 

476 


152 


Noback:  Morpholog}^  and  Phylogeny  477 

arrangement  and  a  few  intermingled  coarse  hairs  (as  in  the  back  hairs 
of  the  cat,  Felis  domesticus  in  figure  4D),  and  (8)  hairs  in  irregularly 
scattered  groups  (as  in  the  back  hair  of  the  raccoon,  Procyon  cancrivorus) . 

Dawson  (1930)  does  not  completely  agree  with  DeMeijere's  pattern  in 
the  guinea  pig.  She  found  variations  in  the  pattern  and  no  correlation  be- 
tween the  size  of  hair  and  the  arrangement  of  the  hairs  in  each  group. 
Histological  study  frequently  shows  follicle  grouping  which  was  not  appar- 
ent to  DeMeijere  when  he  was  examining  only  the  skin  surface,  e.g.,  in 
Felis  domesticus  (see  Hofer,  1914).  This  indicates  that  analyses  of  the 
group  pattern  of  hairs  are  needed  in  both  common  laboratory  mammals  and 
mammals  in  general. 

In  addition,  DeMeijere  analyzed  the  formation  of  the  patterns  by  ex- 
amining the  skins  of  animals  during  their  development  (figures  4-6). 
This  phase  of  the  problem  has  been  extended  to  include  a  study  of  the  ontog- 
eny of  the  arrangement  of  hair  follicles  in  sheep  (Wildman,  1932,  Galpin, 
1935,  and  Duerden,  1939),  in  the  cat  (Hofer,  1914),  in  marsupials  (Gibbs, 
1938,  Stoves,  1944b,  and  Hardy,  1946),  in  the  mouse  (Calef,  1900,  Dry, 
1926,  and  Gibbs,  1941)  in  the  rat  (Frazer,  1928),  and  in  a  number  of  mam- 
mals (Duerden,  1939).  The  terminology  used  by  these  authors  in  this 
problem  is  summarized  in  table  1  (adapted  from  Wildman  and  Carter, 
1939  and  Carter,  1943). 

UtiHzing  the  terminology  of  Wildman  and  Carter,  1939,  the  following  is  a 
brief  statement  of  the  relation  of  the  fiber  generations.  The  first  follicles 
to  differentiate  are  the  central  trio  follicles  (figure  7).  If  these  follicles 
appear  at  two  different  times  as  in  the  opossum  (Gibbs,  1938),  then  the 
follicles  are  called  "primary  X"  and  "primary  Y."  The  essential  point  is 
that  each  of  these  primary  follicles  will  be  the  central  follicle  of  different  hair 
groups.  Later  in  development,  other  follicles  of  the  hair  group  differentiate 
in  relation  to  these  central  trio  follicles.  The  trio  is  formed  when  two 
follicles  are  differentiated  lateral  to  the  primary  follicles  (figure  8).  The 
lateral  follicles  associated  with  primary  X  and  primary  Y  are  called  re- 
spectively "primary  x"  and  "primary  y."  If  only  one  lateral  follicle  is 
formed  adjacent  to  a  primary  follicle  (X  or  Y),  then  a  couplet  follicle 
is  formed.  If  no  lateral  follicles  differentiate,  a  primary  follicle  (X  or  Y)  is 
called  a  "solitary  follicle."  Later,  another  generation  of  follicles  is  differ- 
entiated— the  secondary  follicles.  In  the  opossum  (figure  9),  these 
secondary  follicles  are  located  between  the  central  trio  follicle  and  the  lateral 
trio  follicles.  The  ontogenetic  studies  of  follicle  arrangement  have  added 
confirmatory  evidence  to  DeMeijere's  basic  concept  that  in  mammals  there 
is  a  universal  and  regular  grouping  of  hair  follicles  (Hardy,  1946). 

In  general,  the  early  differentiating  follicles  (central  trio  follicles)  form 
the  coarse  overhair,  while  the  late  differentiating  follicles  (lateral  trio 
follicles  and  secondary  follicles)  form  the  fine  underhair.  Lateral  trio 
follicles  sometimes  at  least  produce  overhair  like  that  of  the  central  fol- 
licles {e.g.  in  sheep)  or  intermediate  types  such  as  awns,  which  are  classified 
by  Danforth  (1925a)  as  overhair.  In  Ornithorhynchus  analinus  (Spencer 
and  Sweet,  1899)  and  many  marsupials  (Gibbs,  1938,  Bolliger  and  Hardy, 


153 


478 


Annals  New  York  Academy  of  Sciences 


1945,  Hardy,  1946),  however,  the  lateral  trio  fibers  are  indistinguishable 
from  those  of  secondary  follicles,  so  it  is  difficult  to  place  them  in  either  the 
"overhair"  or  the  "underhair"  category. 


Figures  1-9  {see  facing  page). 


Spencer  and  Sweet  (1899)  claimed  that,  in  monotremes,  each  group  of 
follicles  was  differentiated  by  budding  from  the  central  follicle.  This  has 
not  been  described  in  marsupials  or  in  eutherians,  in  which  the  follicles 
arise  independently  as  epidermal  downgrowths.     Monotremes  and  mar- 


154 


Noback:  Morphology  and  Phylogeny  479 

supials  have  in  common  the  fact  that  a  follicle  group  typically  contains  a 
large  central  follicle  with  a  sudoriferous  gland,  and  two  or  more  clusters  of 
smaller  lateral  follicles  (Spencer  and  Sweet,  1899,  Gibbs,  1938,  Hardy,  1946). 
This  arrangement  is  also  found  in  some  eutherians,  such  as  the  cat  (Hofer, 
1914)  and  dog  (Claushen,  1933).  In  the  cat  and  a  few  other  eutherians,  the 
first-formed  lateral  follicles  (primary  x  and  y  of  the  classification  of  Wild- 
man  and  Carter,  1939)  produce  hairs  intermediate  in  type  between  those  of 
the  central  and  the  other  lateral  follicles.  There  are  other  eutherians  in 
which  the  lateral  primary  x  and  y  fibers  are  still  more  like  the  central  pri- 
mary X  and  Y  fibers,  as  in  the  pig  (Hofliger,  1931)  and  the  sheep  (Carter, 
1943).  Except  in  the  rodents,  there  is  always  a  sudoriferous  gland  opening 
into  the  central  primary  X  or  Y  follicle  (Hardy,  unpublished  data).  Many 
animals,  such  as  the  pig  and  sheep,  also  have  a  sudoriferous  gland  opening 
into  each  primary  x  and  y  follicle,  but  others  do  not  (Duerden,  1939). 
Some  of  the  eutherians  have  only  primary  follicles  in  their  skin,  each  with 
a  sudoriferous  gland.  Findlay  and  Yang  (1948)  showed  that  this  is  the 
arrangement  in  cattle,  and  the  same  is  probably  true  in  horses  and  in 
human  head  hair  (Hardy,  unpublished  observations). 

Types  of  Hair 

DeMeijere's  analysis  leads  to  the  classification  of  hair  types  by  Toldt 
(1910  and  1935)  and  by  Danforth  (1925a).  Many  details  of  the  hair  types 
in  many  species  of  animals  and  the  variations  of  the  structure  of  these  types 
are  described,  illustrated,  and  bibliographically  annotated  by  Toldt  (1935) 
and  Lochte  (1938). 

Types  of  Mammalian  Hair 
(after  Danforth,  1925a) 
1.  Hairs  with  specialized  folhcles  containing  erectile  tissue.     Large,  stiff  hairs  that  are 
preeminently  sensory.     They  have  been  variously  designated  as  feelers,  whiskers, 


FiGDRES  1-9  (see  opposite  page) . 

Figure  1.  The  trio  hair  group  pattern  on  the  back  and  tail  of  the  marmoset,  Midas  rosalia  (after  DeMei- 
jere,  1896).     .Ml  hairs  have  similar  diameters. 

Figure  2.  The  hair  group  pattern  of  more  than  3  hairs  with  some  fibers  of  greater  diameter  than  other 
fibers  on  the  back  of  the  paca,  Coelogenys  paca  (after  DeMeijere,  1896). 

Figure  3.  The  hair  group  pattern  of  more  than  3  hairs  with  some  fibers  of  greater  diameter  than  other 
fibers  on  the  back  of  the  rodent,  Loncheres  (Echimys)  cristata  (after  DeMeijere,  1896). 

Figure  4.  Ontogeny  of  a  hair  group  on  the  back  of  the  cat,  Felis  domesticus.  A,  from  a  newborn  animal; 
B  and  C,  from  an  older  animal;  and  D,  from  an  adult  animal  (after  DeMeijere,  1896). 

Figure  5.  Ontogeny  of  a  hair  group  on  the  back  of  the  dog,  Canis  Jamiliaris.  A,  from  an  embryo  dog;  B, 
from  a  newborn  animal;  C,  from  a  young  dog;  and  D,  from  an  adult  animal  (after  DeMeijere,  1896). 

Figure  6.  Ontogeny  of  a  hair  group  on  the  back  of  the  mouse,  Mus  decumanus.  A,  from  a  7  cm.  long  ani- 
mal; B,  from  a  9  cm.  long  animal;  C,  from  a  12.5  cm.  long  animal;  and  D,  from  an  adult  animal. 

(Figures  4,  5,  and  6  illustrate  that  the  follicle  of  the  first  hair  to  erupt  (A)  will  be  the  follicle  of  the  coars- 
est hair  of  the  hair  group  in  the  adult.  The  type  of  hair  group  pattern  in  the  adult  (D)  in  each  figure  is  noted 
in  the  text.    The  X  in  the  diagrams  marks  the  location  of  erupting  follicles.) 

Figure  7.  The  primary  follicles  X  (the  more  differentiated  follicles)  and  the  primary  follicles  Y  (the  less 
differentiated  follicles)  in  the  transverse  section  of  skin  of  a  12.5  cm.  Australian  opossum  embryo  [Tricliosurus 
vulpecula).     Follicles  are  scattered  irregularly.     (After  Gibbs,  1938.) 

Figure  8.  Two  new  follicles  (primary  x  or  primary  y)  have  become  grouped  with  each  previously  differen- 
tiated follicle  (primary  X  or  primary  Y)  to  form  the  typical  trio  arrangement.  The  trio  would  be  either 
primary  x,  primary  X,  primary  x  or  primary  y,  primary  Y,  primary  y.  Transverse  section  of  skin  of  a  15.0 
cm.  Australian  opossum  embryo  (Trichosurus  vulpecula).     (After  Gibbs,  1938.) 

Figure  9.  Two  secondary  follicles  have  added  to  each  ffio  group  to  form  a  5  follicle  group.  The  secondary 
follicles  differentiate  between  the  primary  X  (or  Y)  follicle  and  the  primary  x  (or  y)  follicles.  The  five  group 
would  be  either  primary  x,  secondary  follicle,  primary  X,  secondary  follicle,  primary  x  or  primary  y,  second- 
ary follicle,  primary  Y,  secondary  follicle,  primary  y.  Transverse  section  of  skin  from  20.0  cm.  Australian 
opossum  emciryo  (Trichosurus  vulpecula).  Note  presence  of  a  dermal  capsule  surrounding  each  5  follicle 
group.     (After  Gibbs,  1938.) 

(In  figures  7,  8,  and  9,  the  terminology  of  Wildman  and  Carter  (1939),  noted  in  the  text,  is  used.) 


155 


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Annals  New  York  Academy  of  Sciences 


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156 


Noback:  Morphology  and  Phylogeny  481 

sensory  hairs,  sinus  hairs,  tactile  hairs,  vibrissae,  etc.     They  occur  in  all  mammals 
except  man,  and  are  grouped  by  Botezat  (1914)  (Pocock,  1914)  essentially  as  follows: 

(1).  Active  tactile  hairs — under  voluntary  control. 

(2)  Passive  tactile  hairs — not  under  voluntary  control. 

(a)  Follicles  characterized  by  a  circular  sinus. 

(b)  Follicles  without   a   circular   sinus. 

2.  Hairs  with  follicles  not  containing  erectile  tissue.    The  remaining  types  of  hair,  most 
of  which  are  more  or  less  defensive  or  protective  in  function.     In  many  cases,  the 
follicles  have  a  good  nerve  supply,  endowing  the  hair  with  a  passive  sensory  function 
as  well.     These  hairs  are  grouped  here  according  to  their  size  and  rigidity. 
(1).  Coarser,  more  or  less  stiffened  "overhair,"  guard  hair,  top  hair. 

(a)  Spines.     Greatly  enlarged  and  often  modified  defensive  hairs,  quills. 

(b)  Bristles.  Firm,  usually  subulate,  deeply  pigmented,  and  generally 
scattered  hairs.  "Transitional  hairs"  (Botezat,  1914),  "Leithaare" 
(Toldt,  1910),  "protective  hair,"  "primary  hair,"  "overhair."  This 
group  also  includes  mane  hairs. 

(c)  Awns.  Hairs  with  a  firm,  generally  mucronate  lip  but  weaker  and 
softer  near  the  base.  "Grannenhaare"  (Toldt,  1910),  "overhair,"  "pro- 
tective hair." 

(2).  Fine,  uniformly  soft  "underhair,"  "ground  hair,"  "underwool." 

(a)  Wool.     Long,  soft,  usually  curly  hair. 

(b)  Fur.     Thick,  fine,  relatively  short  hair — "underhair,"  "wool  hair." 

(c)  Vellus.  Finest  and  shortest  hair — "down,"  "wool,"  "fuzz,"  "lanugo." 
(Danforth,  1939). 

The  following  comments  supplement  the  above  classification.  The  guard 
hairs  are  listed  in  a  series  from  greater  to  lesser  rigidity  (in  order:  spines, 
bristles,  and  awns).  There  are  many  intergrade  hairs  between  the  typical 
bristle  and  the  typical  awn  and  between  the  typical  awn  and  the  typical 
fur  hair  (figures  10,  11,  and  12). 

The  tactile  hairs  have  a  rich  nerv^e  supply,  while  the  roots  of  some  are 
encircled  by  large  circular  sinuses  containing  erectile  tissue.  When  the 
pressure  in  the  circular  sinus  is  increased  the  hair  becomes  a  more  efficient 
pressure  receptor.  The  overhairs  have  a  definite  nerve  supply,  while  the 
underhairs  have  no  direct  nerve  supply.  As  a  general  but  not  absolute 
rule,  the  coarser  hairs  appear  ontogenetically  earlier  than  the  finer  hairs 
(Gibbs,  1938,  Danforth,  1925a,  Duerden,  1937  (reported  by  Wildman, 
1937),  Hofer,  1914,  and  Spencer  and  Sweet,  1899). 

The  contour,  diameter,  and  shape  of  a  hair  fiber  changes  from  its  root  to 
its  tip  (Note  awns,  figures  16-18).  The  cross-sectional  outline  of  hairs 
may  vary  from  the  thick  rounded  porcupine  quill  to  the  eccentric  flattened 
hairs  of  seals.  The  former  serves  a  protective  function,  while  the  latter  is 
adapted  to  hug  to  the  skin  so  as  not  to  hinder  aquatic  locomotion.  Many 
details  of  the  anatomy  of  hair  form  are  noted  by  Stoves  (1942  and  1944a), 
Toldt  (1935),  and  Lochte  (1938). 

It  is  possible  for  a  hair  follicle  to  differentiate  one  type  of  hair  at  one  stage 
and  another  type  at  another  stage.  The  follicle  of  a  bristle  (kemp)  of  the 
Merino  lamb  may  become  the  follicle  of  wool  in  the  adult  sheep  (Duerden, 
1937,  reported  by  Wildman,  1937).  A  fine  lanugo  hair  of  the  human 
fetus  is  associated  with  a  follicle  which  will  later  be  the  follicle  of  a  coarser 
hair. 

The  theories  of  hair  curling  are  reviewed  by  Herre  and  Wigger  (1939). 
The  curling  of  hair  in  primitive  sheep  is  independent  of  the  arrangement  of 
hair,  existence  of  hair  whorls,  or  the  cross  section  of  the  hair  (Pfeifer,  1929). 


157 


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Annals  New  York  Academy  of  Sciences 


Wildman  (1932)  suggests  that  the  shape  of  the  foUicle,  especially  the  curve 
in  its  basal  portion,  is  a  possible  factor  in  hair  curling.  Reversal  of  the 
spiral  in  some  wool  fibers  may  be  explained  according  to  Wildman  as  due  to 
a  shift  in  the  growing  point  of  the  follicle  and  inner  root  sheath.  Spiral 
reversal  occurs  in  human  hair  (Danforth,  1926).  Pfeifer  (1929)  doubts 
that  curHng  is  determined  by  a  curve  of  the  follicle  alone  and  suggests  that 
Tiinzer's  (1926)  contention  that  the  follicle  must  be  saber-shaped  is  im- 


12 


14 


s. 


"D. 


c.T=is.ne 


Figures  10-15. 


Figure  10.  The  hair  of  the  fox,  Canis  vulpes  (after  Toldt,  1935),  illustrating  intergrade  hairs.  From  the 
left  to  the  right,  Toldt  named  the  fibers  Leithaar  (bristles),  Leit-Grannenhaar,  thick  Grannenhaar  (awns), 
thin  Grannenhaar,  Grannen-WoUhaar,  and  WoUhaar  (fur). 

Figure  11.  The  hair  of  the  chinchilla.  Chinchilla  laniger  (after  Toldt,  1935)  illustrating  an  animal  hair 
coat  with  hairs  of  appro.ximately  the  same  length.  The  2  hairs  on  the  left  are  awns,  and  the  rest,  either 
intergrade  hairs  or  fur  hairs. 

Figure  12.  The  hair  of  the  wild  pig,  Sus  scrofa  (after  Toldt,  1935)  illustrating  bristles  on  the  left  and 
underhair  on  the  right  with  some  intergrade  hairs  between  them.  Note  the  brushlike  distal  ends  of  the 
bristles. 

P'igure  13.  The  scale  index  (S.  I.),  according  to  Hausman  (1930),  is  equal  to  the  ratio  of  the  free  proximo- 
distal  length  of  a  scale  (F)  to  the  diameter  of  the  hair  shaft  (E)). 

Figure  14.  The  thickness  of  the  cuticle  (C.  T.),  according  to  Rudall  (1941),  is  equal  to  the  length  of  a 
cuticular  scale  (1)  times  the  sine  of  angle  (sin  9)  the  scale  makes  with  the  cortex  (X). 

Figure  15.  Cross  sections  of  several  regions  of  a  fur  hair  (left)  and  an  awn  (right)  of  the  rabbit  (after 
Toldt,  1935).  The  sections,  at  the  top  of  the  figure,  are  from  the  base  of  the  hair  and,  at  the  bottom  of  the 
figure,  from  the  tip  of  the  hair.  Illustrates  general  uniformity  of  the  diameters  of  the  fur  haii  and  differences 
in  diameters  and  contour  of  awn  hairs  throughout  their  lengths. 

portant.  Waving  of  all  compact  wools  is  due  at  least  in  part  to  the  flat- 
tening of  the  primary  spiral  and  to  the  unequal  lateral  growth  of  the  fiber 
(Duerden,  1927).  The  curling  of  hair  in  karakul  sheep  fetuses  may  be 
associated  with  the  differences  in  the  rates  of  growth  in  the  various  skin 
layers  (Herre  and  Wigger,  1939). 

The  factors  responsible  for  curling  and  crimping  of  hair  are  as  yet  not 
completely  known. 


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Noback :  Morphology  and  Phylogeny  483 

Structural  Components  of  Hair 

The  cuticle,  cortex,  and  medulla  are  the  three  structural  components  in 
hair.     They  will  be  discussed  in  order. 

Cuticle.  The  cuticle  consists  of  thin,  unpigmented,  transparent  over- 
lapping scales,  whose  free  margins  are  oriented  toward  the  tip  of  the  hair 


20 


Figures  16-21. 

KiGi'FE  16.  Diagram  of  the  fiber  components  of  coat  of  a  generalized  non-wooled  animal  fafter  Duerden, 
1929).  Note  presence  of  bristles  (coarse  fibers),  awns  (fibers  with  fine  basal  segments  and  coarse  distal 
segments)  and  fur  fibers  (fine  fibers). 

Figure  17.  Diagram  of  the  fibers  of  the  wild  sheep  (after  Duerden,  1929).  Note  the  presence  of  bristles 
(kemp),  awns  (heterotypes),  and  wool. 

Figure  18.  Diagram  of  the  fibers  of  British  mountain  breeds  (after  Duerden,  1929\  The  fibers  are 
mainly  awns  and  wool.     Few  bristles  are  present. 

Figure  19.  Diagram  of  the  fibers  of  the  British  luster  breeds  (after  Duerden,  1929).  F'ibers  on  the  left 
are  wool  fibers  which  are  coarser  than  the  wool  fibers  of  wild  sheep.  The  fibers  on  the  right  are  modified 
awns  with  fine  pro.ximal  segments  and  slightly  coarse  distal  segments.     All  fibers  are  elongated  and  spiraled. 

Figure  20.  Diagram  of  fibers  of  adult  Merino  sheep  (after  Duerden,  1929).  All  fibers  are  wool.  Note 
uniformity  of  all  fibers  as  to  size,  length,  and  waviness.  These  wool  fibers  are  coarser  than  wool  fibers  from 
wild  sheep.  Unlike  the  fibers  of  other  breeds,  the  fibers  of  the  adult  Merino  sheep  grow  from  persistent  germs 
and  do  not  shed. 

Figure  21.  Diagram  of  the  fibers  of  the  Merino  lamb.  Note  the  presence  of  bristles  (kemp),  awns  (hetero- 
types), and  wool.  During  later  development,  the  bristles  are  shed  and  the  distal  coarse  segments  of  the 
awns  are  lost.  The  adult  coat  is  formed  by  the  persistent  growth  of  the  wool  fibers  of  the  lamb,  by  the  re- 
placement of  wool  in  the  follicles  of  the  shed  kemp,  and  by  the  persistence  of  the  growth  of  the  proximal  seg- 
ments of  the  awns. 

(figure  22).  Within  the  follicle,  the  free  margins  of  the  hair  cuticular 
scales  interlock  with  the  inner  root  sheath  cuticular  scales,  which  are  oriented 
in  the  opposite  direction  toward  the  papilla.  This  interlocking  of  scales 
helps  to  secure  the  hair  in  place  (Danforth,  1925a).  The  cuticle  functions 
as  a  capsule  containing  the  longitudinally  splitable  corte.x  (Rudall,  1941). 
This  explains  why  the  cortex  of  a  hair  frays  at  its  severed  end.  In  addition, 
the  cuticle,  with  its  oily  layer,  prevents  the  transfer  of  water  (Rudallj  1041). 


159 


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Annals  New  York  Academy  of  Sciences 


The  cuticular  scales  vary  in  thickness  from  0.5  to  3  micra  (Frolich,  Spotel, 
and  Tanzer,  1929).  Since  the  scales  overlap,  the  number  of  overlapping 
scales  at  any  point  on  the  hair  surface  determines  the  thickness  of  the 
cuticle.  The  cuticular  thickness  may  be  expressed  as  being  equal  to  the 
length  of  the  scales  times  the  sine  of  the  angle  the  scale  makes  with  the 
cortical  surface  (figure  14,  Rudall,  1941). 

The  cuticular  scales  may  be  classified  into  two  types:  coronal  scales  and 
imbricate  scales  (Hausman,  1930).  A  coronal  scale  completely  encircles 
the  hair  shaft.  They  are  subdivided  according  to  the  contour  of  the  free 
margins  as:  simple,  serrate,  or  dentate  (figure  23).  Mliller  (1939)  con- 
tends that  a  coronal  scale  is  in  reality  several  scales  whose  lateral  edges  are 


HAIR  SHAFT  IN  MICR0N5 


;oronal  I 


ICORONAl   I  ACUMINATE 

EL0N6ATE  OVATE 


CRENATE        1 

FLATTENED 


Figure  22.  Graph  illustrating  the  relation  of  the  diameter  of  the  hair  to  the  tjmes  of  cuticular  scales. 
The  finest  hairs  (with  small  diameters)  have  a  high-scale  index  and  coronal  scales.  The  coarsest  hairs  (with 
large  diameters)  have  a  low-scale  index  and  flattened  scales.  Diameters  of  hair  shafts  are  plotted  on  the 
ordinate.  General  regions  of  the  occurrence  of  scale  forms  are  shown  along  the  abscissa,  the  average  scale 
indices  along  the  curve.  The  figures  of  the  scale  types  beneath  the  graph  are  not  drawn  to  scale.  (After 
Hausman,  1930.) 

fused.  For  example,  a  dentate  coronal  scale  with  5  processes  in  its  free 
border  is  the  fused  product  of  5  elongated  pointed  scales. 

An  imbricate  scale  does  not  completely  surround  the  hair  shaft.  They 
are  classified  as  ovate,  acuminate,  elongate,  crenate,  and  flattened  (figure 
22,  Hausman,  1930). 

Hausman  (1930)  devised  a  scale  index  to  express  the  relation  between  the 
diameter  of  the  hair  shaft  and  the  free  proximo-distal  dimension  of  the 
scales  (figure  13).  The  free  proximo-distal  dimension  is  actually  a  means 
of  expressing  the  type  of  scale.  For  example,  coronal  scales  have  a  large 
proximo-distal  dimension,  while  crenate  scales  have  a  small  dimension 
(figure  22).  An  analysis  of  the  scale  indices  indicates  that  a  relation  exists 
between  the  types  of  scales  and  the  shaft  diameters.     In  general,  the  finest 


160 


Noback:  Morphology  and  Phylogeny 


485 


hairs  have  large  scale  indices  and  coronal  scales,  while  the  coarsest  hairs 
have  small  scale  indices  and  crenate  or  flattened  scales.  On  the  basis  of 
the  above,  it  is  concluded  that  the  types  of  cuticular  scales  present  on  hair 
are  related  not  to  the  taxonomic  status  of  the  animal  possessing  the  hair 
but  rather  to  the  diameter  of  the  hair  shaft  (Hausman,  1930).  In  hairs 
with  both  thick  and  thin  segments,  the  thick  segments  have  the  scale  types 
of  large  diameter  hairs  while  the  thin  segments  have  the  scale  types  of  small 
diameter  hairs. 

A  coarse  guard  hair  has  scales  with  free  lips  that  are  closely  applied  to  the 
cortex  and  are  scarcely  raised.  As  a  result,  these  hairs  have  a  high  luster 
(due  to  unbroken  reflection  of  light  from  the  hair  surface)  and  do  not  inter- 
lock with  other  hairs.  A  fine  underhair  has  scales  with  lips  that  have  raised 
margins.  As  a  result,  these  hairs  are  dull  (due  to  broken  reflection  of  light) 
and  interlock  with  other  fine  hairs.  Thus,  mohair  has  a  high  luster  but 
makes  poor  felt,  while  wool  is  dull  but  makes  good  textiles. 


C. 


Figure  23.  Figures  illustrating  the  types  of  coronal  cuticular  scales.  A.  simple  scales,  B.  serrate  scales, 
C.  dentate  scales,  (after  Hausman,  1930).    Note  raised  nurgins  on  the  free  lips  of  scales. 

Many  details  of  the  cuticle,  in  many  species  of  animals  are  presented  and 
illustrated  by  Lochte  (1938). 

Cortex.  The  cortex  usually  forms  the  main  bulk  of  a  hair.  It  is  a  column 
of  fusiform  keratinized  cells  which  are  coalesced  into  a  rigid,  almost  homoge- 
neous, hyaline  mass  (Hausman,  1932).  Damaged  hairs  tend  to  split  length- 
wise because  the  elongated  cortical  cells  are  oriented  longitudinally.  The 
cortex  has  such  a  low  refractive  index — due  to  the  degree  of  cornification^ 
that,  in  the  absence  of  pigment,  it  is  translucent.  Since  cortical  scales  have 
not  been  analyzed  in  such  detail  as  cuticular  scales,  no  statement  can  be 
made  of  a  relation  between  cortical  scale  morphology  and  hair  size.  The 
form  and  distribution  of  the  pigment  in  the  cortex  and  the  medulla  is  noted 
by  Lochte  (1938),  Toldt  (1935),  and  Hausman  (1930). 

Hausman  (1932  and  1944)  analyzed  the  cortical  air  spaces  known  as 
cortical  fusi — cortical  in  location  and  fusiform  in  shape — air  vacuoles,  air 
chambers,  air  vesicles,  or  vacuoles.  As  the  irregular-shaped  cortical  cells 
located  in  the  bulb  rise  to  the  follicular  mouth,  they  carry  between  them 
cavities  filled  with  tissue  fluid.     As  the  hair  shaft  dries  out,  the  cavities  lose 


161 


486  Annals  New  York  Academy  of  Sciences 

the  fluid,  and  air  may  fill  the  resulting  spaces — the  fusi.  The  shape  of  the 
fusi  vary.  They  are  largest,  most  numerous,  and  most  prominent  near 
the  base  of  the  hair,  and  they  are  fihform  and  thin  or  lost  in  the  distal  seg- 
ments of  the  hair.  Seldom  do  they  persist  to  the  tip  of  a  hair.  As  a  rule, 
they  are  visible  only  under  a  microscope.  Hausman  implies  that  there  is 
a  relation  between  fusi  and  hair  size.  Presumably,  the  coarser  a  hair  seg- 
ment is,  the  more  numerous  the  fusi. 

Ringed  hair  results  when  the  fusi  appear  in  masses  at  regular  intervals  in 
the  shaft.  Fractured  fusi  result  when  hairs  are  damaged  sufficiently  to 
separate  the  cortical  cells  enough  to  allow  air  to  collect  between  them. 
Fusi  can  be  distinguished  from  pigment  granules,  for  they  are  fusiform, 
whereas  pigment  granules  have  blunt  ends. 

The  presence  of  a  thin  membrane  located  between  the  cuticle  and  the 
cortex  has  been  assumed  by  Lehmann  (1944).  Observations  of  pigment 
granules,  cell  nuclei,  and  submicroscopic  fibrils  are  presented  by  Mercer 
(1942),  Hausman  (1930),  and  others. 

Medulla.  The  medulla  (pith),  when  present,  is  composed  of  shrunken  and 
variably  shaped  cornified  remnants  of  epithelial  cells  connected  by  a  fila- 
mentous network.  In  contrast  to  the  cortex,  the  medulla  is  less  dense  and 
has  fewer  and  larger  cells,  which  are  more  loosely  held  together.  In  the 
medulla  are  air  cells  or  chambers,  which  are  filled  by  a  gas,  probably  air. 
These  air  cells  may  be  intracellular  (deer)  or  intercellular  (dog,  weasel, 
and  rat)  (Lochte,  1938).  The  intercellular  air  cells  are  classifiable  accord- 
ing to  their  coarseness  and  arrangement  (Lochte,  1934  and  1938). 

Medullas  are  classified  by  Hausman  (1930)  as  follows:  absence  of  medulla, 
discontinuous  medulla  (air  cells  separate),  intermediate  medulla  (several 
separate  air  cells  of  the  discontinuous  type  arranged  into  regular  groups), 
continuous  medulla  (air  cells  arranged  to  form  a  column),  and  fragmental 
medulla  (air  cells  arranged  into  irregular  groups).  These  types  are  illus- 
trated in  FIGURE  24  and  are  arranged  in  the  order  of  the  sizes  of  hairs  in 
which  they  are  located.  In  the  finest  hairs  (underfur),  the  medulla  is  either 
absent  or  of  the  discontinuous  type.  In  the  coarsest  hairs,  the  medulla  is 
either  of  the  continuous  or  the  fragmental  type  (figure  24).  If  a  hair 
varies  in  thickness,  its  medulla  will  vary.  For  example,  in  the  awns  of 
sheep,  the  distal  thickened  segment  has  a  medulla,  while  the  fine  proximal 
segment  may  have  no  medulla.  The  arrangement  of  the  medullary  air 
cells  is  related  not  to  the  taxonomic  group  of  the  animal  possessing  the  hair 
nor  the  age  of  the  hair,  but  rather  to  the  diameter  of  the  hair  shaft  (figure 
24)  (Hausman,  1930;  Wynkoop,  1929;  and  Smith,  1933).  The  sheens 
and  colors  of  hairs  are  largely  determined  by  the  light  reflected  from  the 
medulla  (Hausman,  1944). 

Although  the  cortex  forms  the  bulk  of  the  shaft  in  most  hairs,  the  medulla 
assumes  large  proportions  in  some  hairs.  In  rabbit  hair  (figure  15),  the 
medulla  is  composed  of  large  air  cells  separated  by  little  more  than  a  frame- 
work of  cortex  (Stoves,  1944c). 

The  significance  of  the  cuticle,  cortex,  and  medulla  in  the  commercial 
aspects  of  fur  is  presented  by  Bachrach  (1946).     Although  many  of  the 


162 


Noback :  Morphology  and  Phylogeny 


487 


details  of  the  structural  elements  of  hair  cannot  be  detinitely  utilized  to 
identify  an  animal  species  (Hausman,  1944),  it  is  possible  that  some  morpho- 
logical features  of  hair  can  be  used  (Williams,  1938). 

Some  chemical  and  physical  aspects  of  the  morphological  elements  of 
hair  have  been  analyzed.  Not  only  do  the  cuticle,  cortex,  and  medulla 
exhibit  different  chemical  and  physical  properties,  but  various  segments  of 
these  structural  elements  may  have  different  chemical  and  physical  proper- 


FiGURE  24.  Graph  illustrating  the  relation  of  the  diameter  of  the  hair  to  the  types  of  medullas.  The 
finest  hairs  have  no  medulla,  and  the  coarsest  hairs  have  a  fragmental  medulla.  Diameters  in  micra  of  the 
hair  shafts  are  plotted  on  the  ordinate.  The  figures  of  the  types  of  medullas  beneath  the  graph  are  not  drawn 
to  scale.     (After  Hausman,  1930.) 

ties  (Rudall,  1944;  Stoves,  19436,  1945;  Lustig,  Kondritzer,  and  Moore, 
1945;  Leblond,  1951;  and  Giroud  and  Leblond,  1951). 

Some  Phylogenelic  Aspects  of  Hair 

The  relation  of  hair  to  the  epidermal  structures  in  non-mammalian  ani- 
mals has  been  discussed  by  many  authors  and  has  been  summarized  by 


163 


488  Annals  New  York  Academy  of  Sciences 

Botezat  (1913  and  1914),  Danforth  (1925b),  and  Matkeiev  (1932).  No 
direct  relation  between  hair  and  non-mammalian  epidermal  elements  has 
been  established.  Hair  is  most  probably  an  analog  to  these  structures. 
Danforth  (1925b)  and  others  conclude  that  hair  is  probably  a  de  novo  morpho- 
logical entity  in  mammals. 

Broili  (1927)  reports  that  he  identified  hair  and  hair  follicles  in  a  fossil 
aquatic  reptile,  Rhamphorynchus.  This  animal  is  a  specialized  reptile, 
removed  from  those  reptiles  in  the  evolutionary  line  to  mammals.  If 
established,  this  observation  would  alter  the  concept  that  only  mammals 
produce  hair. 

The  phylogeny  of  hair  in  related  groups  of  animals  has  not  been  analyzed 
extensively.  Because  of  the  economic  importance  of  wool,  several  studies 
of  the  hair  types  in  the  coat  of  a  number  of  breeds  of  sheep  have  been  made. 
One  significant  aspect  of  these  studies  is  that  they  illustrate  how  the  hair 
coat  may  vary  in  closely  related  forms. 

This  statement  is  adapted  primarily  from  Duerden  (1927  and  1929). 
The  generalized  wild  animal  hair  coat  consists  of  an  overcoat  of  bristles  and 
awns  and  an  undercoat  of  fur  (figure  16).  In  the  wild  sheep  and  the 
black-headed  Persian  sheep,  the  hair  coat  is  similar  to  that  of  the  wild 
animal.  These  sheep  have  an  overcoat  of  bristles  (called  kemp)  and  awns 
(called  heterotypes)  and  an  undercoat  of  wool  (figure  17).  The  British 
mountain  breeds  have  a  hair  coat  consisting  of  awns  and  wool  (figure 
18).  In  these  breeds,  kemp  formation  is  negligible.  The  coat  of  the 
British  luster  breeds  have  evolved  in  another  direction.  The  awns  retain 
their  fine  proximal  segments.  Their  distal  segments  are  still  thicker  than 
the  proximal  segments,  but  are  thinner  than  the  distal  segments  of  the  awns 
of  primitive  sheep.  The  wool  undercoat  fibers  have  thickened.  Both  fiber 
types  are  elongated  and  spiraled  (figure  19).  The  adult  Merino  sheep, 
the  most  efficient  wool-producing  sheep,  has  a  coat  consisting  of  elongated, 
regularly  crimped  fibers  of  uniform  diameters  and  lengths  (figure  20). 
An  analysis  of  the  coat  of  the  Merino  lamb  is  essential  for  the  identification 
of  the  types  of  fibers  that  form  the  coat  of  the  adult  sheep.  The  Merino 
lamb  coat  has  bristle,  awn,  and  wool  fibers  (figure  21).  During  ontogeny, 
the  bristles  are  shed  and  then  replaced  by  wool  fibers.  The  awn  fibers 
lose  their  distal  thickened  segments,  but  the  thin  proximal  segments  persist. 
The  wool  fibers  are  retained,  but  are  coarser  than  the  wool  of  primitive 
sheep.  Hence,  the  adult  Merino  sheep  coat  consists  of  wool  fibers  differ- 
entiating from  follicles  which  produced  kemp  in  the  lamb,  of  awns  deprived 
of  their  distal  segments,  and  of  wool  fibers  differentiating  from  follicles 
which  produced  wool  in  the  lamb.  A  major  difference  between  the  Merino 
sheep  and  other  sheep  is  in  the  nature  of  the  hair  follicles.  Whereas  the 
coat  of  other  breeds  is  shed  periodically  and  then  new  hairs  differentiate 
from  the  follicles,  the  fibers  of  the  adult  Merino  sheep  grow  from  persistent 
germs  and  are  not  shed. 

In  the  evolution  of  the  sheep  coat  from  primitive  wild  sheep  to  the  various 
domestic  breeds,  several  changes  have  occurred.  As  summarized  by  Duer- 
den (1927),  the  domestic  wooled  sheep  has  evolved  in  the  direction  of  the 


164 


Noback :  Morphology-  and  Phylogeny  489 

loss  of  the  protective  coat  both  of  bristles  (kemp)  and  awns  (heterotypes), 
the  increase  in  length,  density,  and  uniformity  of  the  fibers,  and  the  tend- 
ency of  the  retained  bristles  to  become  finer  but  still  capable  of  being  shed. 
In  addition,  the  Merino  sheep  has  developed  persistently  growing  hair 
follicles. 

Important  implications  of  the  evolution  of  the  sheep  coat  are  that  the 
types  of  hair  in  the  hair  coat  may  differ  (1)  in  closely  related  animals  and 
(2)  at  various  stages  of  ontogeny  with  the  same  animal.  Hence,  data 
derived  from  a  study  of  the  coat  of  one  animal  species  may  not  always  apply 
to  another  animal  species. 

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Discussion  of  the  Paper 

Doctor  M.  H.  H.jirdy  {McM aster  Laboratory,  Glebe,  X.  S.  W.,  Austra- 
lia): I  am  glad  Dr.  Noback  mentioned  sheep,  because  the  study  of  the  ar- 
rangement of  folUcles  in  groups  on  these  animals  has  disclosed  some  im- 
portant principles.  Terentjeva,^  Duerden,'  and  Carter^  showed  that  de 
Meijere's  trio  group  is  the  basic  unit  in  the  follicle  population  of  sheep. 
The  trio  (primary)  follicles  develop  first  and  have  accessory  structures 
(sudoriferous  gland,  arrector  pili  muscle)  which  are  absent  from  the  later 
developing  (secondary)  follicles  of  the  group.''  In  the  young  lamb,  it  is  the 
primary  follicles  which  produce  the  coarse,  and  frequently  meduUated, 
kemp  fibers  and  the  secondary  follicles  which  produce  the  fine  and  usually 
non-meduUated  wool  fibers.  These  correspond  respectively  to  the  'over- 
hair'  and  'underhair'  in  Danforth's  classification.  The  primary  follicles 
may  produce  kemp  in  the  lamb  and  wool  in  the  adult  sheep,  as  Dr.  Xoback 
has  mentioned. 

The  size  of  the  follicle  groups,  i.e.,  the  number  of  secondary  follicles  to 
each  trio  of  primary  follicles,  varies  greatly  between  breeds*  and  individuals^ 
and  also  between  body  regions.®  The  breeds  and,  to  some  extent,  indi- 
viduals with  the  largest  group  size  have  also  the  greatest  number  of  fibers 
to  the  square  inch  and  the  greatest  uniformity  of  fiber  thickness  and  length.^ 
In  the  midside  region,  at  least,  the  potential  group  size  (including  second- 
ary follicle  rudiments  in  the  young  lamb)  is  strongly  inherited,  but  the 
actual  group  size  (number  of  active  follicles)  in  the  mature  animal  varies 


167 


492  Annals  New  York  Academy  of  Sciences 

according  to  the  food  intake  in  the  first  year  of  lifeJ  Thus,  it  is  possible 
to  alter  the  group  size  experimentally.  Varying  the  food  intake  in  the 
second  and  third  year  of  life  had  no  marked  effect  on  group  size.^'^ 

It  seems  that  many  properties  of  the  coat  of  the  sheep  depend  on  the 
inherited  follicle  group  pattern  and  the  modifications  of  this  superimposed 
by  the  environment.     Perhaps  the  same  principles  apply  to  other  mammals. 

1.  Terentjeva,  a.  a.     1939.     Pre-natal  development  of  the  coat  of  some  fine-wooled 

breeds  of  sheep.     C.  R.  Acad.  Sci.  U.R.S.S.  (N.S.)  25:  557. 

2.  DuERDEN,  J.  E.     1939.     The  arrangement  of  fibre  follicles  in  some  mammals,  with 

special  reference  to  the  Ovidae.     Trans.  Roy.  Soc.  Edin.  59:  763. 

3.  Carter,  H.  B.     1943.     Studies  in  the  biology  of  the  skin  and  fleece  of  sheep.     1. 

The  development  and  general  histologv  of  the  follicle  group  in  the  skin  of  the  Merino. 
Coun.  Sci.  Ind.  Res.  (Aust.)  Bull.  164:  7. 

4.  Carter,  H.  B.  &  P.  Davidson.     Unpublished  data. 

5.  Carter,  H.  B.     1942.     "Density"  and  some  related  characters  of  the  fleece  in  the 

Australian  Merino.     J.  Coun.  Sci.  Ind.  Res.  (Aust.)  15:  217. 

6.  Carter,  H.  B.  &  M.  H.  Hardy.     1947.     Studies  in  the  biology  of  the  skin  and  fleece 

of  sheep.     4.  The  hair  follicle  group  and  its  topographical  variations  in  the  skin 
of  the  Merino  foetus.     Coun.  Sci.  Ind.  Res.  (Aust.)  Bull.  215:  5. 

7.  Carter,  H.  B.,  H.  R.  Marston,  &  A.  W.  Peirce.     Unpublished  data. 

8.  Ferguson,K.  A.,  H.B.  Carter  &  M.H.Hardy.     1949.     Studies  of  comparative  fleece 

growth  in  sheep.     Aust.  J.  Sci.  Res.  B  2:  42. 

9.  Ferguson,  K.  A.,  H.  B.  Carter,  M.  H.  Hardy,  &  H.  N.  Turner.     Unpublished 

data. 


168 


MORPHOLOGY  AND  FLIGHT  CHARACTERISTICS  OF 

MOLOSSID  BATS 

By  Terry  A.  Vaughan 

Abstract:  Selected  aspects  of  the  morphology  of  bats  of  the  family  Molossidae 
are  described  and  the  functional  significance  of  these  features  are  discussed.  The 
structure  and  proportions  of  the  ears  and  the  wings  are  considered  to  reflect 
primarily  the  rapid  enduring  fUght  typical  of  molossids.  Comparisons  of  some 
characteristics  of  the  wings  of  three  molossids  and  of  four  bats  of  the  family 
Vespertilionidae  were  made,  and  several  aerodynamic  relationships  were  applied 
to  a  consideration  of  the  styles  and  speeds  of  flight  of  these  bats.  Molossid  bats  in 
general  seem  adapted  to  fast  flight  in  open  areas,  whereas  the  vespertihonids 
studied  are  apparently  suited  to  slower  flight  fairly  low  to  the  ground,  near  vege- 
tation and  other  obstacles. 

Bats  of  the  family  Molossidae  form  a  distinctive  and  anatomically  peripheral 
group,  and  their  flight  probably  surpasses  that  of  all  other  bats  in  speed  and 
endurance.  Repeated  mention  in  the  literature  has  been  made  of  the  mode  of 
flight  of  these  bats  (H.  W.  Grinnell,  1918;  A.  B.  Howell,  1920;  Orr,  1954; 
Vaughan,  1959;  Hall  and  Dalquest,  1963);  and  Miller  (1907),  Vaughan  (1959) 
and  Struhsaker  ( 1961 )  have  described  selected  aspects  of  the  postcranial 
morphology  of  molossids. 

MATERIALS  AND  METHODS 

Specimens  in  alcohol  representing  the  following  species  and  famiUes  were  examined  for 
this  study:  Macrotus  californicus  ( Phyllostomidae ) ;  Myotis  lucifugus,  M.  yumanensis,  M. 
velifer,  M.  evotis,  Lasiurus  horealis,  L.  cinereus,  Plecotus  townsendii,  Antrozous  pallidus 
( Vespertilioiiidae ) ;  Tadarida  hrasiliensis,  T.  molossa,  Eumops  perotis  (Molossidae).  The 
specimens  are  in  the  collection  of  the  author. 

Measurements  of  areas  and  proportions  of  wings  were  made  from  tracings  of  wing 
outhnes.  Although  care  was  taken  to  pin  each  wing  in  the  same  fuUy  spread  position,  the 
wing  measurements  of  preserved  specimens  probably  differ  from  those  of  fresh  animals. 


169 


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Vol.  47,  No.  2 


,,.^L^'^.^t^ 


Fig.  L — Front  and  side  views  of  the  heads  of  Eumops  perotis  (above)  and  Tadanda 
molossa  (below).  In  tlie  front  view  of  Eumops  the  anterior  part  of  the  left  ear  is  removed 
to  show  the  structure  of  the  ear. 

All  wing  measurements  were  taken  as  follows  from  fully  outstretched  wings:  the  length 
of  the  distal  segment  of  the  wing  ( chiropatagium )  was  measured  from  the  base  of  the 
thumb  to  the  wing  tip;  the  length  of  the  proximal  segment  of  the  wing  ( plagiopatagiimi ) 
was  measured  from  the  middle  of  the  base  of  the  wing  where  it  joins  the  body  to  the 
middle  of  the  fifth  digit;  the  width  of  the  wing  was  measured  across  the  flattened  airfoil 
from  the  base  of  the  thumb  to  the  tip  of  the  fifth  digit;  the  length  of  the  wing  was 
measured  from  the  center  of  the  base  of  the  wing  to  the  vdng  tip.  Wing  areas  were 
measured  as  if  the  wings  were  continuous  through  the  interf emoral  membrane  ( uropatagium ) 
and  the  body.  Ear  lengths  were  measured  from  the  crown,  and  ear  widths  were  measured 
across  the  base  of  the  pinna  where  it  joins  the  head,  or,  as  in  the  case  of  molossids,  from 
the  posterior  base  of  the  pinna  to  where  the  anterior  base  joins  the  fold  of  tissue  connecting 
the  anterior  edges  of  the  pinnae. 

RESULTS  AND  DISCUSSION 

Head. — The  heads  of  all  molossid  bats  are  similar  in  basic  design:  the 
braincase  and  rostrum  are  broad  and  the  muzzle  is  truncate;  the  lips  are 
thick  and  frequently  wrinkled;  the  ears  are  usually  broader  than  long,  have 
thickened  and  reinforced  borders,  and  face  more  nearly  downward  or  to  the 
side  than  forward  (Fig.  1).  The  design  and  position  of  the  ears  is  of  con- 
siderable aerodynamic  importance  in  a  bat  with  rapid,  sustained  flight,  and 
with  this  in  mind  the  ears  of  molossid  bats  merit  close  attention. 

The  shape  and  proportions  of  the  ears  of  molossids  are  distinctive  and  fairly 
uniform.  The  ears  are  characteristically  very  broad,  relative  to  their  length, 
and  have  squared-off  tips.  In  Eumops  perotis  and  Tadarida  molossa  the  ears 
are  1.6  times  as  wide  as  high.  The  corresponding  figure  for  T.  brasiliensis  is 
1.2.  The  ears  of  most  vespertilionid  bats,  in  contrast,  are  longer  than  wide. 
In  the  vespertilionid  bats  listed  in  Table  1,  for  example,  the  ratio  of  ear  width 
to  ear  length  is  from  0.39  to  0.70. 

In  molossid  bats  the  anterior  and  ventral  borders  of  the  pinnae  are  generally 


170 


May  1966    VAUGHAN— MORPHOLOGY  AND  FLIGHT  OF  MOLOSSIDS 


251 


Table  1. — Sizes  of  heads  of  bats  and  birds  and  proportions  of  the  ears  of  bats.    All  figures 
are  averages;  the  numbers  of  specimens  measured  are  given  in  parentheses 


Weight  of  head 

Ear  width 

Species 

Total  weight 

Ear  length 

Sturnus  vulgaris 

(9) 

0.11 

— 

Turdus  migratorius 

(13) 

0.11 

- 

Mijotis  yumanensis 

(10) 

0.15 

0.58 

M.  velifer 

(10) 

0.17 

0.70 

Plccotus  townsendii 

(10) 

0.16 

0.39 

Tadarida  brasiliensis 

(10) 

0.16 

1.15 

T.  molossa 

(3) 

0.20 

1.56 

Eumops  perotis 

(5) 

0.23 

1.61 

strongly  braced  by  connective  tissue.  Viewed  from  the  side,  the  pinna  arches 
dorsad  and  resembles  a  crude  airfoil  of  high  camber  (Fig.  1).  The  base  of 
the  leading  edge  of  the  pinna  is  almost  directly  anterior  to  the  base  of  the 
trailing  edge,  thus  furthering  the  resemblance  of  the  ears  to  short,  broad  wings. 
During  flight  the  thickened  ventral  borders  of  the  ears  lie  against  the  side  of 
the  head  and  cover  the  eyes  in  some  molossids.  Short,  broad  ears  which  lie 
against  the  head  and  do  not  directly  face  the  airstream  during  flight  are  found 
also  in  Lasiurus.  Here,  as  in  the  molossids,  this  type  of  ear  is  associated  with 
rapid  flight. 

In  both  birds  and  bats  there  has  been  a  trend  toward  the  concentration  of 
weight  near  the  center  of  gravity.  The  heads  of  most  birds  are  light;  they 
carry  no  teeth  and  generally  have  only  light  jaw  musculature.  In  a  series  of  13 
robins  {Turdus  migratorius)  and  9  starlings  (Sturnus  vulgaris)  from  Colorado 
the  head  comprised  on  the  average  10.9%  and  11.2%  of  the  total  weight,  re- 
spectively. Relative  to  total  body  weight,  bats  have  heavier  heads  than  those 
of  birds.  In  the  bats  studied  the  weight  of  the  head  comprised  from  approxi- 
mately 15  to  23%  of  the  total  weight  (Table  1).  The  heads  of  two  of  the 
molossid  bats  are  relatively  considerably  heavier  than  the  heads  of  the  ves- 
pertilionid  bats.  When  in  flight  most  bats  carry  the  occipital  portion  of  the 
head  against  the  interscapular  depression,  thus  compensating  for  the  weight 
of  the  head  by  bringing  it  fairly  close  to  the  center  of  gravity. 

The  unique  design  of  the  ears  of  molossid  bats  probably  developed  in  re- 
sponse to  fast,  sustained  flight,  and  serves  to  minimize  drag  and  to  brace  the 
ears  against  the  force  of  the  airstream.  In  addition,  the  ears  probably  develop 
some  lift  during  flight,  allowing  the  heavy  head  to  be  supported  as  least  in 
part  by  the  airstream.  During  long  flights  this  could  result  in  an  important 
conservation  of  energy  which  would  otherwise  be  expended  in  supporting 

the  head. 

A  further  characteristic  of  the  molossid  head  which  has  probably  been  de- 
veloped in  response  to  rapid  flight  is  the  loose  or  wrinkled  lips.  It  remains 
for  high-speed  photography  to  demonstrate  the  operation  of  the  lips  in  catching 
insects,  but  it  seems  probable  that  when  the  mouth  is  wide  open  during  flight 


171 


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Vol.  47,  No.  2 


r""Coraco-cutaneus 


•  occipito-pollicalis 

■•humeropatagialis 


Fig.  2. — The  wings  of  Eumops  perotis  (top),  Lasiurus  borealis  (middle),  and  Myotis 
evotis  (bottom),  showing  the  muscles  and  networks  of  elastic  fibers  that  tighten  and  brace 
the  wing  membranes. 

the  lips  spread  outward,  away  from  the  teeth,  thus  increasing  the  area  of  the 
mouth.  The  wrinkled  or  loose  lips  of  molossids  seem  functionally  homologous 
to  the  rictal  bristles  around  the  bills  of  caprimulgiform  birds;  in  both  groups 
the  increase  in  the  effective  area  of  the  mouth  may  partially  compensate  for 
the  sacrifice  of  maneuverability  attending  rapid  flight. 


172 


May  1966    VAUGHAN— MORPHOLOGY  AND  FLIGHT  OF  MOLOSSIDS  253 

Wings. — Molossids  possess  many  advanced  chiropteran  characteristics  as- 
sociated with  efficient  flight,  such  as  the  well-developed  humeroscapular  lock- 
ing device  (Vaughan,  1959:  54);  but  in  addition  they  are  obviously  highly 
specialized  for  fast  flight,  with  a  resulting  sacrifice  in  maneuverability  and 
lifting  power.  Davis  and  Cockrum  ( 1964 )  have  shown  by  experimentally 
attaching  weights  to  bats  that,  although  the  animals  are  roughly  equal  in 
weight,  Macrotus  calif ornicus  ( Phyllostomidae )  can  take  flight  with  approxi- 
mately five  times  the  additional  load  lifted  by  Tadarida  brasiliensis  (Molossi- 
dae).  Differences  in  the  ability  to  take  off  with  extra  loads  reflect,  in  part, 
differences  in  wing  design. 

The  long,  narrow  wings  of  molossid  bats  are  unique  in  several  ways.  The 
fifth  digit  is  unusually  short,  making  the  plagiopatagium  narrow.  The  first 
phalanges  of  the  third  and  fourth  digits  flex  posteriorly  instead  of  ventrally 
as  in  most  other  bats.  This  allows  the  long  part  of  the  wing  distal  to  the  third 
and  fourth  metacarpals  to  be  folded  compactly  against  the  posterior  surfaces 
of  these  bones  when  the  wing  is  at  rest  or  is  used  in  terrestrial  locomotion.  In 
molossid  bats  the  third  metacarpal,  the  longest  bone  in  the  hand,  is  almost 
exactly  the  same  length  as  the  radius.  Consequently,  because  of  the  pattern  of 
flexion  of  the  third  and  fourth  digits,  the  long  chiropatagium  folds  into  a  bundle 
no  longer  than  the  radius. 

In  considering  the  form  and  function  of  wings,  the  amount  of  camber  (an- 
teroposterior curvatiu-e)  is  of  basic  importance.  The  amount  of  camber  is  a 
major  factor  in  determining  the  ability  of  a  wing  to  develop  lift.  Airfoils  with 
high  camber  develop  high  lift  at  low  speeds,  but  create  considerable  drag. 
Relative  to  airfoils  of  high  camber,  those  of  low  camber  are  effective  at  pro- 
ducing lift  at  higher  speeds  and  produce  little  drag.  The  airfoils  of  most  bats 
are  of  high  camber,  whereas  those  of  molossids  are  of  relatively  low  camber. 
In  terms  of  function,  the  latter  design  creates  relatively  little  drag  but  forces 
molossid  bats  to  fly  fairly  rapidly  to  enable  the  airfoils  to  produce  sufficient 
lift  to  maintain  flight.  An  aerodynamic  refinement  occurring  in  bats  but  not 
in  birds  is  the  ability  to  vary  the  camber  of  the  wing.  Flexion  of  the  phalanges 
of  the  fifth  digit  and  lowering  the  hind  limbs  increases  the  camber  of  the  wing 
by  curving  the  trailing  edge  of  the  plagiopatagium  downward  and  causing  it 
to  function  like  a  flap  on  an  airplane.  Such  a  flap  enables  either  bats  or  air- 
craft to  increase  the  camber  of  an  airfoil  for  higher  Hft  at  low  speeds  and  to 
flatten  the  airfoil  and  reduce  the  drag  at  higher  speeds.  Thus,  a  wing  with 
flaps  can  operate  effectively  under  a  greater  range  of  speeds  than  that  within 
which  the  same  wing  could  function  if  it  had  a  fixed  airfoil.  The  ability  to 
change  the  amount  of  camber  of  the  wings  is  probably  important  in  enabling 
small,  broad-winged  bats  such  as  Myotis  evotis  and  Plecotus  townsendii  to  fly 
at  a  great  variety  of  speeds.  The  camber  of  the  narrow  molossid  wing  seems 
less  variable  than  that  of  broad-winged  vesperitilionids. 

The  flight  membranes  of  molossids  are  leathery  and  elastic  and  seem  much 
stronger  than  those  of  other  bats.  In  molossids  the  wing  membranes  are  braced 


173 


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JOURNAL  OF  MAMMALOGY 


Vol.  47,  No.  2 


•biceps  brachii 


acromiodeltoideus 

clavodeltoideus 

■  occipito-pollicalis 

■  omocervicalis 

V  i^vi$^^' pectoralis 


Fig.  3. — Front  view  of  the  right  shoulder  of  Eumops  perotis  showing  the  attachment  of 
the  occipito-poUicahs  muscle  to  the  pectorahs  muscle. 


by  cartilaginous  extensions  of  the  distal  ends  of  the  third,  fourth  and  fifth 
phalanges  and  by  complex  meshworks  of  connective  tissue  in  the  plagiopa- 
tagium  and  in  the  interdigital  membranes  ( Fig.  2 ) .  The  elasticity  of  the  wing 
membranes  may  be  of  considerable  aerodynamic  importance.  When  the  wings 
are  partially  flexed,  as  they  are  during  dives  or  in  rapid  level  flight,  the  tension 
on  the  plagiopatagium  is  partially  relaxed  and  this  membrane  narrows  sharply, 
reducing  its  area  and  the  drag  it  creates.  This  narrowing  is  probably  caused  by 
both  the  elastic  network  and  by  the  humeropatagialis  muscle.  The  high-speed 
dives  made  by  Eumops  perotis,  and  sometimes  made  by  Tadarida  brasiliensis, 
when  approaching  a  roosting  place  in  a  cliff  (see  Vaughan,  1959:  20)  may  be 
made  possible  partly  by  the  narrowing  of  the  plagiopatagium  when  the  wing 
is  partly  flexed. 

In  all  bats  the  wing  membranes  are  strengthened  by  muscles  not  present  in 
other  mammals,  but  in  molossids  there  has  been  a  greater  development  of  these 
muscles  than  in  any  other  group  of  bats.  The  occipito-pollicalis  muscle  in 
most  bats  originates  on  the  lambdoidal  crest,  extends  along  the  leading  edge 
of  the  propatagium  ( the  membrane  anterior  to  the  humerus  and  radius ) ,  and 
inserts  along  the  anterior  surface  of  the  second  metacarpal.  This  muscle  keeps 
the  propatagium  taut  during  flight,  pulls  this  membrane  slightly  ventrad,  and 
thereby  helps  give  camber  to  the  plagiopatagium.  This  improves  the  effective- 
ness of  this  segment  of  the  wing  as  an  airfoil.  This  narrow  muscle  is  attached 
by  fascia  to  the  front  of  the  shoulder  in  most  bats.  In  molossids,  however,  the 
muscle  is  relatively  large  and  is  more  complex:  it  is  divided  into  a  proximal 
and  a  distal  part,  and  the  junction  of  these  parts  is  attached  strongly  by  a 
tendon-like  fascial  bundle  to  the  pectoralis  muscle  (Fig.  3).  The  coraco-cutane- 
ous  muscle,  which  occurs  in  all  bats,  originates  on  the  humerus  and  passes 
into  the  proximal  part  of  the  plagiopatagium.  This  muscle  helps  maintain  the 
tautness  of  the  axillary  portion  of  the  plagiopatagium.  Two  additional  muscles, 
serving  to  tense  the  plagiopatagium,  are  present  only  in  molossid  bats  and  are 


174 


May  1966    VAUGHAN— MORPHOLOGY  AND  FLIGHT  OF  MOLOSSIDS  255 

probably  adaptations  to  fast  flight.  The  first,  the  tensor  plagiopatagii,  origi- 
nates on  the  tibia  and  tarsus  and  inserts  into  the  part  of  the  plagiopatagium 
adjoining  the  shank  and  into  the  connective  tissue  tliat  reinforces  the  trailing 
edge  of  the  plagiopatagium.  This  muscle  not  only  tenses  this  part  of  the  wing 
but  is  of  importance  in  strengthening  the  attachment  of  the  plagiopatagium 
to  the  shank  and  tarsus.  The  second  muscle,  the  humeropatagialis,  originates 
on  the  distal  end  of  the  humerus  and  inserts  into  the  elastic  fibers  in  the  distal 
part  of  the  plagiopatagium  (Fig.  2).  The  most  important  function  of  the 
muscles  and  connective  tissue  which  reinforce  and  tense  the  plagiopatagium 
is  to  maintain  this  proximal  segment  of  the  wing  as  an  efficient  airfoil  during 
flight  and  to  keep  the  membrane  from  being  distorted  by  the  force  of  the  air- 
stream.  In  fast-flying  bats  considerable  distortion  could  occur  and  this  would 
reduce  sharply  the  effectiveness  of  the  plagiopatagium  as  a  lifting  surface.  Be- 
cause the  plagiopatagium  supplies  the  major  share  of  lift  during  flight,  this 
is  of  critical  importance.  An  additional  function  of  the  plagiopatagialis  may 
be  to  narrow  the  plagiopatagium  during  dives  or  when  the  wings  are  partially 
flexed  during  rapid  flight. 

The  morphology  of  the  scapula  varies  considerably  within  the  order  Chirop- 
tera  and  reflects,  in  part,  degrees  of  specialization  for  various  modes  of  flight. 
One  variable  structure  is  the  long  coracoid  process,  which,  because  it  extends 
ventral  to  the  plane  of  the  scapula,  allows  the  biceps  brachii  and  coraco- 
brachialis  muscles  to  serve  as  adductors  of  the  wing.  In  most  bats  the  coracoid 
curves  laterad  (toward  the  wing),  whereas  in  all  molossids  the  coracoid  is  di- 
rected sharply  mediad  (Fig.  4).  This  "molossid"  type  of  coracoid  is  found  also  in 
Miniopterus  (Miller,  1907),  and  to  a  lesser  degree  in  Lasiurus.  Attending  this 
difference  are  differences  between  the  brachial  musculature  of  molossid  bats 
and  most  other  bats.  In  the  latter  the  coracobrachialis  and  the  biceps  brachii 
muscles  are  the  important  members  of  the  flexor  group  of  the  arm.  The 
glenoid  head  of  the  biceps  originates  on  the  lateral  base  of  the  coracoid  process 
and  is  the  larger  division  of  the  biceps.  The  smaller  coracoid  head  originates 
along  the  distal  part  of  the  coracoid  process.  Both  divisions  insert  into  a  slit 
in  the  anteromedial  surface  of  the  radius  just  distal  to  its  head.  Molossids,  in 
contrast,  have  lost  the  coracobrachialis  muscle;  and  the  coracoid  head  of  the 
biceps,  rather  than  the  glenoid  head,  is  the  largest  division  of  this  muscle 
(Fig.  4).  Because  of  the  medial  curvature  of  the  coracoid  process  in  molossids, 
during  the  lower  part  of  the  downstroke  of  the  wing  the  coracoid  head  of  the 
biceps  can  act  as  a  far  more  effective  adductor  than  can  this  muscle  in  most 
nonmolossid  bats  (Vaughan,  1959:  90).  In  molossids,  due  partly  to  the  modi- 
fications of  the  scapula  and  biceps  mentioned  above,  occurs  the  most  perfect 
development  of  the  basic  chiropteran  trend  toward  dividing  the  labor  of  the 
downstroke  of  the  wing  between  a  number  of  muscles.  This  division  of  labor 
was  probably  developed  in  response  to  the  demands  of  the  enduring  flight 
typical  of  most  molossids. 

The  shapes  and  aerodynamic  characteristics  of  the  wings  considered  in  this 


175 


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Vol.  47,  No.  2 


••humerus 


acromion  process 


coracoid  process 


>■• biceps  brachii 
(glenoid  head) 


•biceps  brachii  (coracoid  head) 


Fig.  4. — Front  views  of  the  right  shoulders  of  Antrozous  pallidus  (above),  showing  the 
lateral  curvature  of  the  coracoid  process  of  the  scapula  typical  of  most  vespertilionid  bats, 
and  of  Eumops  perotis  (below),  showing  the  medial  curvature  of  the  coracoid  process 
typical  of  molossid  bats. 

study  differed  widely  (Fig.  2,  Table  2),  but  certain  differences  between  the 
molossid  and  vespertilionid  wings  are  readily  apparent  and  are  indicative  of 
functional  contrasts.  The  ratios  based  on  wing  proportions  illustrate  that,  com- 
pared to  the  vespertilionid  wing,  the  molossid  wing  is  narrow,  has  a  long  distal 
segment,  a  high  aspect  ratio  (the  ratio  of  length  to  width  of  a  wing;  for  ir- 
regularly shaped  wings  it  is  considered  to  be  the  ratio  of  the  wing  span^/wing 
area),  and  a  high  wing  loading  (weight  in  pounds/wing  area  in  feet^). 

For  the  molossid  bats  considered  here  the  length  of  the  chiropatagium 
averaged  154.1%  of  the  length  of  the  plagiopatagium,  and  the  width  of  the 
wings  averaged  36.8%  of  the  length.  In  the  vespertilionids  measured  the  cor- 
responding figures  were  138.5%  and  48.7%.  The  aspect  ratios  reflect  these 
differences  and  are  higher  for  the  molossids  (8.60-9.98)  than  for  the  ves- 
pertilionids (5.99-6.74).  In  general,  the  higher  the  aspect  ratio  the  more  ef- 
ficient the  wing  because  of  the  reduction  of  drag  at  the  wing  tip.   The  wing 


176 


May  1966    VAUGHAN— MORPHOLOGY  AND  FLIGHT  OF  MOLOSSIDS 


257 


Table  2. — Proportions  of  wings  of  bats.   All  figures  are  averages;  the  numbers  of 
specimens  measured  are  given  in  parentheses 


Species 

Area  of 
chiropatagium 

Area  of 
phigiopatagium 

Length  of 
chiropatagium 

Length  of 
plagiopatagium 

Greatest  width 
of  wing 
Length 
of  wing 

Aspect  ratio: 
Wing  span^ 

Area  of  wings 

Myotis  yumanensis 

(5) 

0.95 

L32 

0.47 

6.74 

M.  evotis 

(5) 

0.80 

L35 

0.51 

6.48 

M.  lucifugus 

(5) 

0.69 

L41 

0.48 

6.47 

Plecotus  townsendii 

(5) 

0.86 

L46 

0.50 

5.99 

Tadarida  brasUiensis 

(5) 

0.93 

1.58 

0.38 

8.60 

T.  molossa 

(3) 

0.86 

L47 

0.36 

9.71 

Eumops  perotis 

(5) 

0.83 

1.58 

0.36 

9.98 

loadings  of  the  molossid  bats  (0.325-0.546)  are  considerably  higher  than  those 
of  the  vespertilionids  (0.157-0.202).  As  a  rule,  the  higher  the  wing  loading 
the  greater  the  speed  necessary  to  produce  adequate  lift  for  sustained  flight. 
Usually  the  smaller  the  bat  the  lower  the  wing  loading  because  in  small  bats 
the  ratio  of  mass  to  surface  is  small  ( the  volume  and  mass  vary  as  the  cube 
of  the  linear  dimensions  whereas  the  surface  area  varies  as  the  square). 

Instructive  comparisons  can  be  made  between  habitat  and  wing  form  in 
both  bats  and  birds  and  between  the  characteristics  of  the  wings  of  certain 
bats  and  those  of  the  wings  of  birds  with  well-known  modes  of  flight.  The 
plan  form  of  the  wing  of  Myotis  evotis  ( Fig.  2 )  is  similar  to  that  of  many  small 
passerine  birds.  This  roughly  elliptical  wing  is  fairly  efficient  for  low  speed 
flight,  and  occurs  in  birds  adapted  to  flight  through  brush  or  woods,  or  where 
numerous  obstacles  make  long  wings  unmanageable  (Savile,  1957).  The 
short,  broad  wing  of  Myotis  evotis  is  seemingly  well  suited  to  flight  near  the 
ground  in  the  wooded  or  brushy  areas  the  bat  inhabits.  A  markedly  different 
adaptation  is  Illustrated  by  the  wings  of  molossid  bats  which  are  similar  to 
the  "high-speed"  wings  of  many  birds  known  to  be  strong  enduring  fliers  or 
to  feed  on  the  wing  ( falcons,  plovers,  sandpipers,  swifts  and  swallows ) .  Such 
birds  characteristically  fly  in  open  places  with  few  obstructions,  a  situation 
"allowing"  the  development  of  long,  aerodynamically  efficient  wings.  The 
wings  of  these  birds  have  the  following  characteristics  according  to  Savile 
( 1957 ) :  low  camber;  high  aspect  ratio;  taper  to  a  slender,  elliptical  tip;  pro- 
nounced sweepback  of  the  leading  edge;  and  wing  root  fairing.  These  same 
features  describe  well  the  molossid  wing.  Thus,  in  wing  design  and  foraging 
habits  the  molossids  appear  to  be  chiropteran  counterparts  of  the  swdfts  and 
swallows,  whereas  the  smaller  vespertilionids  seem  to  most  nearly  resemble  the 
smaller  flycatchers  in  wing  design,  but  differ  from  the  latter  in  flying  con- 
tinuously while  feeding. 


177 


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Vol.  47,  No.  2 


Table   3. — Sizes,   aerodynamic   characteristics   and   computed   minimum   flight   speeds  of 
seven  species  of  bats.    All  figures  are  averages;  the  numbers  of  specimens  measured  are 

given  in  parentheses 


Species 


Weight 

(g) 


Wing  span 
( cm ) 


Wing  area 
(cm2) 


Wing  loading 


lbs/ft2 


g/cm2 


Minimum 
flight 
speed 
(mph) 


Myotis  yumanensis 

(5) 

5.2 

20.26 

60.95 

0.173 

0.084 

8.3 

M.  evotis 

(5) 

6.2 

22.80 

80.20 

0.157 

0.077 

7.9 

M.  lucifugus 

(5) 

8.1 

23.30 

83.41 

0.202 

0.099 

8.8 

Plecotus  townsendii 

(5) 

9.1 

24.52 

100.41 

0.184 

0.090 

8.5 

Tadarida  hrasiliensis 

(5) 

12.2 

25.08 

73.14 

0.339 

0.165 

11.6 

T.  molossa 

(3) 

16.2 

31.33 

101.12 

0.325 

0.159 

11.7 

F.umops  perotis 

(5) 

53.5 

44.58 

199.22 

0.546 

0.266 

14.7 

From  the  weight  of  a  bat  and  the  area  of  its  wing  surfaces  the  speed  it  must 
fly  to  sustain  level  flight  can  be  approximated  by  the  equation 

(von  Mises,  1945)  where  V  is  velocity  (in  feet  per  second);  2  gc  is  a  unit- 
conversion  constant;  W  is  the  total  weight;  A  is  the  area  of  the  wings;  C^  is 
the  coefficient  of  lift;  and  V  is  the  density  of  air  in  pounds  per  cubic  foot. 
The  coefficient  of  lift  is  derived  from  the  size,  camber,  aspect  ratio,  angle  of 
attack  and  other  characteristics  of  the  wing,  and  for  the  present  study  was 
assumed  to  be  1.0,  which  probably  approximates  the  actual  values  closely 
enough  to  cause  little  error.  These  calculations  are  based  on  the  further  as- 
sumption that  each  bat  has  its  wings  fully  and  rigidly  outstretched.  Although 
the  calculated  speeds  may  not  correspond  closely  to  the  actual  flight  speeds 
of  the  bats,  they  probably  reflect  accurately  the  relative  flight  speeds.  Except 
for  the  molossids,  flight  speeds  arrived  at  by  the  above  equation  (Table  3) 
are  fairly  close  to  those  found  experimentally  by  Hayward  and  Davis  ( 1964 ) . 
As  these  authors  mention,  the  speeds  shown  for  the  molossids  in  their  study 
are  probably  too  low  because  the  bats  could  not  fly  normally  under  their 
experimental  conditions. 

The  speeds  calculated  on  the  basis  of  the  figures  for  total  weight  and  wing 
area  shown  in  Table  3  suggest  that  in  order  to  maintain  level  flight  the 
molossids  must  fly  faster  than  do  the  vespertilionids.  The  speed  for  Myotis 
evotis  (7.9  mph),  for  example,  is  roughly  half  that  of  Eumops  perotis  (14.7 
mph).  The  calculated  speeds  probably  approximate  the  relative  speeds  of 
the  bats  under  study  in  level  flight,  but  all  of  these  bats  seem  to  be  capable 
of  a  wide  range  of  flight  speeds.  Judging  from  my  own  observations,  M.  evotis 
can  hover  briefly  and  can  fly  at  very  low  speeds;  at  the  other  extreme,  some 
molossids  are  capable  of  rapid  dives  and  of  level  flights  at  speeds  far  greater 
than  those  listed  here.  A  complicating  factor,  but  one  of  critical  importance 
when  considering  the  flight  capabilities  of  a  bat,  is  the  animal's  ability  to 


178 


May  1966    VAUGHAN— MORPHOLOGY  AND  FLIGHT  OF  MOLOSSIDS  259 

vary  the  camber,  angle  of  attack  and  the  areas  of  the  membranes.  A  fm-ther 
complexit>'  is  the  fact  that  the  wings  are  in  nearly  constant  movement  dur- 
ing flight,  and  supply  both  the  lift  and  the  thrust  necessary  for  flight. 

Various  aerodynamic  relationships  are  pertinent  to  the  problem  of  relative 
flight  speeds  and  differences  in  morphology  in  bats.  For  example,  because 
drag  increases  in  proportion  to  surface  area  and  as  the  square  of  the  speed, 
E.  perotis  is  probably  subject  to  about  three  times  the  drag  faced  by  M.  evotis. 
This  explains  why  features  which  tend  to  minimize  drag,  such  as  low  camber 
of  the  wing  and  short  ears  which  present  their  most  streamlined  aspect  to 
the  airstream,  are  of  vastly  greater  importance  in  the  large  E.  perotis,  and  in 
most  molossid  bats,  than  in  smaller,  relatively  slow-flying  bats.  Even  the 
short,  velvety  fur  of  molossids  may  be  an  adaptation  to  reduce  drag  caused 
by  the  body  during  flight. 

Miscellaneous  considerations. — The  family  Molossidae  is  unique  in  having 
developed  the  most  rapid,  enduring  flight  occurring  in  bats  while  retaining 
(or  developing)  the  most  accomplished  terrestrial  locomotion.  Consequently, 
molossids  offer  many  trenchant  examples  of  a  single  morphological  character 
serving  diverse  functional  ends. 

One  such  character  is  the  posterior  flexion  of  the  first  phalanges  of  digits 
three  and  four.  Because  of  this  modification  the  long  tip  of  the  narrow  wing  is 
manageable  when  the  bats  are  not  flying,  an  important  feature  in  a  group 
including  many  species  which  take  daytime  refuge  in  narrow  crevices.  This 
unusual  pattern  of  flexion  may  have  developed  prior  to  the  lengthening  of 
the  wing  tip  and  may  have  "allowed"  the  evolution  of  this  typically  molossid 
character.  The  part  of  the  wing  distal  to  the  carpus  folds  into  a  bundle  no 
longer  than  the  radius,  facilitating  a  lateral  action  of  the  forelimb  during 
quadripedal  locomotion  which  enables  molossids  to  move  remarkably  rapidly 
and  easily  within  the  confines  of  narrow  crevices.  Thus,  the  pattern  of 
phalangeal  flexion  in  molossids  has  probably  played  a  role  in  both  terrestrial 
and  aerial  locomotion. 

The  small  uropatagium  of  these  bats  slips  forward  along  the  tail  freeing 
the  hind  limbs  to  move  in  a  wide  arc  when  the  animals  run.  Also,  the  re- 
duced drag  during  flight  resulting  from  the  small  size  of  the  uropatagium  is 
probably  aerodynamically  important  in  furthering  the  cause  of  fast  flight. 
The  well-braced  flight  membranes  of  molossids  may  also  serve  two  ends, 
for  in  addition  to  resisting  effectively  the  force  of  the  airstream  during  rapid 
flight,  they  are  better  able  than  are  the  delicate  membranes  of  most  bats  to 
withstand  the  occasional  rough  treatment  resulting  from  crawling  between  the 
irregular  and  abrasive  surfaces  of  rock  crevices. 

Perhaps  the  strong  adductors  and  flexors  of  the  hind  limbs  represent  the 
best  example  of  a  dual-puipose  molossid  character.  These  limbs  are  re- 
markably robust  and  strongly  muscled  and  account  in  large  part  for  the  ac- 
complished terrestrial  locomotion  typical  of  the  group.  Of  equal  importance, 
however,  is  their  function  in  serving  as  a  rigid  anchor  for  the  posterior  portion 


179 


260  JOURNAL  OF  MAMMALOGY  Vol.  47,  No.  2 

of  the  plagiopatagium.  This  function  requires  strong  flexors  and  adductors 
of  the  shank  to  resist  the  powerful  lateral  and  dorsal  pull  exerted  by  the  flight 
membranes  during  the  downstroke  of  the  wing,  and  is  of  basic  importance 
in  maintaining  the  proper  angle  of  attack  and  camber  of  the  plagiopatagium. 

Considering  the  evolution  of  the  family  Molossidae,  the  sturdiness  of  the 
hind  limb  and  the  complete  fibula  suggest  that  the  basal  molossid  stock 
may  have  diverged  early  from  the  rest  of  the  Chiroptera,  before  the  hind 
limbs  had  been  greatly  modified  from  their  primitive  structure  and  propor- 
tions. By  contrast,  in  many  members  of  the  family  Phyllostomidae  the  hind 
limbs  have  become  so  highly  specialized  that  they  no  longer  function  effec- 
tively in  quadripedal  locomotion.  But  in  molossids,  probably  because  the 
primitive  hind  limbs  suited  the  demands  of  both  terrestrial  and  aerial  locomo- 
tion, the  hind  limbs  have  remained  basically  primitive  through  a  period  of 
time  that  saw  the  evolution  of  the  highly  specialized  molossid  wing  of  today. 

Some  vespertilionid  bats  and  one  rhinolophid  bat  have  been  shown  to  use 
the  flight  membranes  in  capturing  insects  (Webster  and  Griffin,  1962),  In 
these  species  most  modifications  tending  to  reduce  the  dexterity  of  the 
phalanges  were  probably  disadvantageous,  and  the  evolution  of  the  hand 
was  probably  influenced  by  its  use  in  capturing  insects,  as  well  as  by  the  de- 
mands of  aerial  and  terrestrial  locomotion. 

ACKNOWLEDGMENTS 

This  study  was  supported  in  part  by  a  grant  from  The  Society  of  Sigma  Xi  and  RESA 
Research  Fund.  For  critically  reading  the  manuscript  and  for  helpful  discussions  of 
aerodynamics  I  am  grateful  to  Dr.  P.  H.  Baldwin  and  Dr.  R.  D.  Haberstroh. 

LITERATURE  CITED 
Davis,  R.  and  E.  L.  Cockrum.     1964.     Experimentally  determined  weight  lifting  capacity 

in  individuals  of  five  species  of  western  bats.    J.  Mamm.,  45:  643-644. 
Grinnell,  H.  W.     1918.     A  synopsis  of  the  bats  of  CaHfomia.    Univ.   California  Publ. 

Zool.,  17:  223-404. 
Hall,  E.  R.  and  W.  W.  Dalquest.     1963.     The  mammals  of  Veracruz.    Univ.   Kansas 

Publ.,  Mus.  Nat.  Hist.,  14:   165-362. 
Hayward,  B.  and  R.  Davis.     1964.     Fhght  speeds  in  western  bats.  J.  Mamm.,  45:  236-242. 
Howell,  A.  B.     1920.     Contribution  to  the  hfe  history  of  the  California  mastiff  bat.    J. 

Mamm.,  1:  111-117. 
Miller,   G.    S.     1907.     The  famihes   and   genera  of   bats.     U.    S.    Nat.    Mus.    Bull.,    57: 

xvii  -I-  282  pp. 
Orr,  R.  T.     1954.     Natural  history  of  the  pallid  bat,  Antrozous  pallidus.    Proc.  CaUfomia 

Acad.  Sci.,  28:  165-246. 
Savtle,  D.  B.  O.     1957.     Adaptive  evolution  in  the  avian  wing.    Evolution,  11:  212-224. 
Struhsaker,  T.   T.     1961.     Morphological  factors   regulating  flight  in  bats.    J.   Mamm., 

42:  152^159. 
Vaughan,  T.  a.     1959.     Functional  morphology  of  three  bats:    Eumops,  Myotis,  Macrotus. 

Univ.  Kansas  Publ,  Mus.  Nat.  Hist.,  12:  1-153. 
von  Mises,  R.     1945.     Theory  of  flight.    McGraw-Hill  Book  Co.,  New  York.    629  pp. 
Webster,  F.  A.  and  D.  R.  Griffin.     1962.     The  role  of  the  flight  membranes  in  insect 

capture  by  bats.    Animal  Behavior,  10:  332-340. 

Colorado  Agricultural  Experiment  Station,  Colorado  State  University,  Fort  Collins. 
Accepted  23  September  1965. 


180 


NATURAL  HISTORY  MISCELLANEA 

Published  by 

The     Chicago     Academy     of     Sciences 

Lincoln  Park  -  2001  N.  Clark  St.,  Chicago  14,  Illinois 

No.  170  October  30,  1959 


Toxic  Salivary  Glands  in  the  Primitive  Insectivore  Solenodon 

George  B.  Rabb* 

In  1942  0.  P.  Pearson  demonstrated  the  toxic  property  of  the  saliva 
of  Blarina  brevkauda,  a  common  shrew  of  the  eastern  United  States, 
and  identified  its  principal  source  as  the  submaxillary  gland.  Compara- 
tive studies  at  that  time  and  subsequently  revealed  that  similar  poison- 
ous factors  were  not  present  in  the  salivary  glands  of  other  soricid  and 
talpid  insectivores  (Pearson,  1942,  1950,  1956).  I  had  an  unexpected 
opportunity  to  make  a  crude  check  on  the  salivary  glands  of  Solenodon 
paradoxus,  a  remote  relative  of  the  shrews,  when  three  of  these  animals 
died  at  the  Chicago  Zoological  Park  within  two  months  after  their 
arrival  in  1958  from  the  Dominican  Republic. 

Parts  of  the  submaxillary  and  parotid  glands  of  one  animal  that 
had  died  one  to  two  hours  beforehand  were  ground  separately  with 
sand,  diluted  to  10  per  cent  by  weight  solutions  with  0.9  per  cent  XaCl 
solution,  and  filtered,  following  the  procedure  of  Pearson  (1942).  These 
solutions  were  injected  into  a  small  series  of  male  white  mice  that 
ranged  in  weight  from  29  to  44  grams. 

All  of  the  mice  injected  with  extract  from  submaxillary  gland 
showed  some  reaction  —  at  least  urination  and  irregular  or  rapid 
breathing  for  several  minutes.  Five  that  received  intravenous  doses  of 
extract  of  .09  to  .38  mg.  submaxillary  gland  per  gram  of  body  weight 
did  little  more  than  this  and  recovered  within  30  minutes.  Five  that 
received  intravenous  doses  of  .38  to  .55  mg.  per  gram  additionally  ex- 
hibited protruding  eyes,  gasping,  and  convulsions  before  dying  within 
two  to  six  minutes.  Two  animals  that  had  intraperitoneal  injections  of 
extract  of  .56  and  .66  mg.  per  gram  died  in  about  12  hours,  and  one 
injected  at  the  level  of  1.02  mg.  per  gram  died  in  13  minutes.  Urination, 
cyanosis,  and  depression  were  observed  in  these  animals.  Three  "con- 
trol" mice  injected  intravenously  with  extract  of  1.02,  1.68,  and  1.87 


♦Chicago  Zoological  Park,  Brookfield,  Illinois 


181 


No.   170  The  Chicago  Academy  of  Sciences,  Natural  History   Miscellanea 

mg.  of  parotid  gland  per  gram  of  body  weight  showed  no  distress  except 
for  initially  very  rapid  breathing  in  the  last  case. 

In  general  these  results  are  very  like  those  described  for  Blarina 
extracts.  It  may  be  noted  that  the  twentyfold  lesser  potency  evident 
here  of  Solenodon  extract  as  compared  to  that  of  Blarina  may  be  due 
to  postmortem  inactivation  of  the  toxic  principle  as  reported  by  EiLs 
and  Krayer  (1955)  for  fresh  Blarina  material.  Further  tests  with  tne 
refined  techniques  of  these  authors  using  acetone  treated  glands  will 
be  necessary  for  a  fairer  assessment  of  the  potency  of  Solenodon  toxin. 

Sections  were  made  of  the  submaxillary  glands  and  stained  w-th 
hematoxylin  and  eosin  and  also  with  a  modification  of  Mallory's  triple 
stain.  These  sections  showed  some  large  cells  with  coarse  acidophilic 
granules  and  small  nuclei  in  the  secretory  ducts.  Pearson  (1950)  sus- 
pected that  such  cells  in  Blarina  might  be  concerned  in  the  production 
of  the  saliva's  toxic  principle,  although  somewhat  similar  cells  are 
found  in  other  soricids. 

The  submaxillary  glands  of  Solenodon  are  rather  enormous  and  con- 
spicuous structures  (see  fig.  47  in  Mohr,  1938).  Each  gland  weighs 
three  to  four  grams  in  adult  animals.  According  to  Allen  (1910),  the 
duct  of  the  submaxillary  gland  ends  at  the  base  of  the  large  deeply 
channeled  second  incisor  tooth  of  the  lower  jaw  (see  fig.  19D  in  Mc- 
Dowell, 1958).  Presumably  toxic  saliva  would  be  conducted  thereby 
into  a  wound.  I  could  not  induce  Solenodon  to  bite  live  mice  and  there- 
fore have  no  direct  evidence  on  this  point.  However,  in  1877  Gundlach 
reported  inflammatory  effects  of  bites  by  Cuban  Solenodon  to  himself 
and  a  mountaineer  (although  he  dismissed  the  possibility  of  venomous 
action  on  the  basis  of  authority!).  Of  his  hand  bite  he  said:  "...  I 
was  bitten  by  the  tame  individual,  which  gave  me  four  wounds  cor- 
responding to  the  [large]  incisors:  those  from  the  two  upper  incisors 
healed  well,  but  those  from  the  lower  ones  inflamed." 

Moreover,  there  are  indications  that  Solenodon  is  not  immune  to  its 
own  venom.  Autopsy  of  the  third  animal  disclosed  multiple  bite  wounds 
on  the  feet  and  no  obvious  internal  evidence  of  other  causes  of  death. 
Sections  of  the  liver  show  considerable  congestion  in  that  organ.  The 
snout,  lips,  limbs,  and  tail  were  very  pale  the  afternoon  preceding  death. 
Mohr  (1937,  1938)  gave  accounts  of  several  cases  in  which  death  was 
the  outcome  of  fighting  with  cage  mates  although  only  slight  foot 
wounds  were  inflicted.  Pearson  (1950)  reported  that  Blarina  was  rela- 
tively immune  to  its  own  venom,  although  the  single  test  animal  died 
and  the  interpretation  was  problematical.   The  utility  of  the  venom  for 


182 


Rabb:  Toxic  Salivary  Glands  of  Solenodon  1959 

Solenodon  in  its  natural  environment  is  unknown  and  is  certainly  not 
indicated  by  its  insectivorous  habits.  The  explanation  may  be  phylo- 
genetic  and  historical  rather  than  one  of  present-day  function. 

I  wish  to  acknowledge  the  help  of  the  park's  veterinarian,  W.  M. 
Williamson,  and  medical  technician,  Ruth  M.  Getty. 

Literature  Cited 

Allen,  Glover  M. 

1910.         Solenodon  paradoxus.  Mem.  Mus.  Comp.  Zool.,  40:  1-54. 
Ellis,  Sydney  and  Otto  Krayer 

1955.  Properties  of  a  toxin  from  the  salivary  gland  of  the 
shrew,  Blarina  brevicauda.  Jour.  Pharmacol,  and  Exptl. 
Therap.,  114:   127-37. 

Gundlach,  Juan 

1877.         Contribucion    a    la    mamalogia    Cubana.     Havana,    G. 
Monteil,  53  pp. 
McDowell,  Samuel  B.,  Jr. 

1958.  The  Greater  Antillean  insectivores.  Bull.  American  Mus. 
Nat.  Hist.,  115(3):  113-214. 

Mohr,  Erna 

1937.  Biologische  beobachtungen  an  Solenodon  paradoxus 
Brandt  in  Gefangenschaft.  HI.  Zool.  Anz.,  117:  233-41. 

1938.  Biologische  beobachtungen  an  Solenodon  paradoxus 
Brandt  in  Gefangenschaft.  IV.  Ibid.,  122:   132-43. 

Pearson,  Oliver  P. 

1942.         On  the  cause  and  nature  of  a  poisonous  action  produced 

by   the   bite   of   a   shrew    {Blarina    brevicauda).   Jour. 

Mamm.,  23:   159-66. 
1950.         The  submaxillary  glands  of  shrews.   Anat.  Record,  107; 

161-69. 

1956.  A  toxic  substance  from  the  salivary  glands  of  a  mammal 
(short-tailed  shrew),  pp.  55-58  in  Venoms,  ed.  E.  E. 
Buckley  and  N.  Porges,  American  Assoc.  Adv.  Science 
Publ.  No.  44,  xii  +  467  pp. 


183 


466  JOURNAL  OF  MAMMALOGY  Vol.  48,  No.  3 

SOME  ASPECTS  OF  THE  WATER  ECONOMICS  OF  TWO  SPECIES  OF  CHIPMUNKS 

The  water  economics  of  chipmunks  have  not  received  much  attention  from  physiological 
ecologists.  Allen  (New  York  State  Mus.  Bull.,  314:  1-122,  1938)  wrote  of  Tamias  striatus: 
"Unlike  many  of  the  western  ground  squirrels,  the  Eastern  chipmunk  requires  a  great  deal 
of  water  to  drink."  Panuska  and  Wade  (J.  Mamm.,  38:  192-196,  1957)  found  that  water 
consumption  of  captive  T.  striatus  decreased  from  33.4  ml  per  day  just  after  capture  to 
29.2  ml  per  day  after  the  animals  had  been  confined  for  a  time.  Davis  ( Murrelet,  15:  20-22, 
1934)  wrote  that  water  was  not  a  factor  in  determining  the  distribution  of  the  cliff  chip- 
munk, Eutamias  dorsalis,  in  Nevada.  Seton  (Lives  of  game  animals,  4:  184-215,  1929) 
observed  that  west  and  south  of  Manitoba  the  least  chipmunk,  E.  minimus,  is  found  in 
desert  environments  far  from  permanent  water.  ManviUe  (Misc.  Publ.  Mus.  Zool.,  Univ. 
Michigan,  73:  1-83,  1949)  thought  water  to  be  of  httle  importance  in  the  distribution  of 
E.  minimus  in  the  Huron  Mountains  of  Michigan. 

In  the  Itasca  region  of  Minnesota  the  ranges  of  the  gray  eastern  chipmunk,  T.  striatus 
griseus,  and  the  least  chipmunk,  E.  minimus  neglectus,  overlap.  Since  striatus  and  minimus 
apparently  have  markedly  different  water  economics  in  the  extremes  of  their  ranges,  I 
wondered  if  the  two  species,  in  the  mesic,  forested  Itascan  habitats,  would  differ  from  each 
other  in  their  gross  and  weight-relative  water  consumption  and  in  their  responses  to  water 
deprivation. 

These  studies  were  conducted  in  August  and  September  1963.  Chipmunks  of  both  species 
were  captured  in  National  Live  Traps,  5^/4  X  5^2  X  16  inches,  set  within  3  miles  of  Itasca 
State  Park,  Hubbard  and  Clearwater  counties,  Minnesota.  The  chipmunks  were  transferred 
to  an  animal  room  in  the  zoology  building  at  the  University  of  Minnesota,  Minneapohs. 
There  were  no  provisions  for  regulating  light,  temperature,  or  humiclit;    in   the  room. 

Nine  striatus  and  nine  minimus  were  confined  individually  in  cages  18  X  18  X  12  inches 
with  wood  shavings  provided  for  htter,  and  were  fed  only  sunflower  seeds.  The  seeds 
contained  water  amounting  to  about  12%  of  their  weight.  Tap  water  was  provided  ad 
libidum  in  30  cc  or  100  cc  graduated  drinking  tubes.  One  tube  of  each  size,  hung  on  the 
rack  of  cages,  permitted  assessment  of  evaporative  water  loss  from  the  tubes.  For  36  days, 
daily  records  were  kept  of  the  change  of  water  level  in  each  tube.  On  18  days,  at  least 
one  of  the  striatus  spilled  water,  indicated  by  wet  litter  below  the  tube.  Least  chipmunks 
were  not  known  to  spiU  water.  Records  of  water  consumption  for  the  18  days  on  which  no 
spillage  was  noted  were  used  to  calculate  each  animal's  gross  water  consumption.  Each 
animal's  mean  daily  water  consumption  was  calculated  by  dividing  gross  water  consump- 
tion by  18.  Each  animal's  water  consumption  per  g  of  body  weight  was  estimated  by 
dividing  gross  water  consumption  by  the  mean  value  of  the  animal's  body  weight  as 
recorded  on  the  first  and  thirty-sixth  days.  The  arithmetic  mean,  standard  deviation, 
standard  error  of  the  mean,  and  coefficient  of  variation  ( V )  were  computed  for  each  of  the 
foregoing  variables  for  each  species. 

Following  the  studies  of  water  consumption,  seven  individuals  of  each  species  were 
deprived  of  water  for  five  consecutive  days.  Two  individuals  of  each  species  served  as 
controls  and  were  allowed  unrestricted  access  to  drinking  water.  The  chipmunks  were 
weighed  daily  during  the  five  days  of  water  deprivation  and  for  seven  days  after  ad 
libidum  access  to  water  was  restored.  Each  animal's  daily  weight  was  recorded  as  a 
percentage  of  its  body  weight  at  tlie  outset  of  the  experiment.  Mean  daily  percentages  were 
calculated  for  each  species. 

Statistical  procedures  followed  were  those  of  Simpson,  Roe,  and  Lewontin  (Quantitative 
zoology,  1960).   The  level  of  significance  used  for  tests  of  hypotheses  was  95%. 

Data  on  water  consumption  are  summarized  in  Table  1.  Although  the  gross  water 
requirement  of  minimus  was  about  one-third  that  of  striatus,  there  was  no  significant 
difference  in  the  weight-relative  water  consuimptions  of  the  two  species.    The  coefficients 


184 


August  1967 


GENERAL  NOTES 


467 


Table  1. — Summary  of  data  on  water  constimption  of  confined  chipmunks. 


1'.  striatus 

E.  minimus 

Variable 

Mean 
Range 

SE 

V 

Mean 

Range                   se 

V 

Weights  of 
animals   (g) 

Total  HaO 
consumed   ( ml ) 

Mean  HaO  consumed 
per  day  (ml) 

Mean  H2O  consumed 
per  g  body  weight 


115.0 
102.8-132.8 

296.1 
208-471 

16.4 
11.6-26.2 

2.52 
1.98-<3.60 


3.4  8.9 
26.5  26.8 

1.5        

0.18  20.8 


46.2 


42.0-50.2 


97.8 


76-150 

5.4 
4.2-8.3 

2.16 
1.62r-2.96 


0.8 
7.6 
0.4 
0.17 


5.1 
23.2 


23.6 


of  variation  show  that  individual  variation  in  water  consumption  was  very  large.  There  are 
individual  and  specific  differences  in  the  adjustments  of  the  animals  to  captivity.  As  a 
group,  eastern  chipmunks  were  more  sedentary  in  their  cages  than  were  least  chipmunks,  but 
activity  among  individual  striatus  was  quite  variable. 

The  two  species  did  not  differ  significantly  from  each  other  in  their  abilities  to  resist 
weight  loss  during  water  deprivation  or  to  regain  weight  once  access  to  water  was  restored 
(Table  2).  When  experimental  animals  were  deprived  of  water,  they  first  became  more 
active  than  usual.  Their  activity  decreased  markedly  during  the  last  three  days  of  water 
deprivation.  Normally,  a  lively  chase  ensued  before  an  animal  could  be  caught  by  hand 
for  weighing,  but  by  the  fifth  day  of  water  deprivation  one  could  easily  pick  up  a 
dehydrated  chipmunk  from  its  cage.  Control  animals  remained  quick  and  alert.  Their 
weights  varied  only  a  few  grams  on  either  side  of  their  pre-experimental  weights  during  this 
study.  The  mean  weights  of  rehydrating  striatus  are  distorted  by  the  weights  of  one 
individual  that  continued  to  lose  weight  even  after  access  to  water  was  restored.   Ultimately, 


Table   2. — Percentages   of   pre-experimental   weights   of   experimental   chipmunks   during 

dehydration  and  rehydration. 


Day 

n 

T.  striatus 
Range                   Mean 

SD 

E.  minimus 

number 

n 

Range 

Mean 

SD 

1 

7 

89.9-95.5 

93.0 

1.8 

7 

89.5-95.4 

93.4 

1.8 

2 

7 

85.5-91.6 

88.2 

2.2 

7 

85.6-91.6 

88.6 

1.9 

3 

7 

80.0-86.7 

83.6 

2.6 

7 

79.2-S5.2 

82.9 

2.2 

4 

7 

74.6-82.5 

78.6 

3.4 

7 

74.8-83.7 

78.8 

3.1 

5 

7 

70.4-79.4 

75.7 
Access 

4.0 
to  water 

7 
restored 

69.4-79.2 

74.9 

3.7 

6 

7 

76.6-85.4 

82.5 

2.9 

7 

80.7-92.0 

84.7 

4.5 

7 

6* 

67.8-85.5 

81.1 

6.6 

7 

77.3-95.0 

84.9 

6.2 

8 

6 

63.6-92.8 

83.3 

10.1 

6* 

79.1-96.5 

88.1 

6.3 

9 

6 

62.8-94.3 

85.7 

11.6 

6 

80.7-100.0 

89.1 

7.0 

10 

6 

59.4-97.4 

87.0 

14.1 

6 

79.9-100.0 

89.1 

7.1 

12 

6 

57.9-100.0 

89.1 

16.3 

6 

82.7-100.0 

90.6 

6.0 

*  One  experimental  animal  found  dead. 


185 


468  JOURNAL  OF  MAMMALOGY  Vol.  48,  No.  3 

this  animal  lost  half  of  its  pre-experimental  weight,  but  the  pre-experimental  weight  was 
eventually  regained  and  siupassed. 

The  literature  suggests  that  striatus  is  somewhat  more  dependent  upon  a  plentiful  supply 
of  drinking  water  than  are  minimus  and  its  relatives.  The  present  experimental  evidence 
suggests  that  this  is  so.  The  gross  water  requirements  of  minimus  are  small.  With  some 
insects  and  fruit  of  high  water  content,  and  a  morning  supply  of  dew,  Itascan  minimus  can 
probably  keep  themselves  in  good  condition  with  no  permanent  source  of  drinking  water. 
When  raspberries  ( Rubus  minnesotanus )  are  in  fruit  at  Itasca,  minimus  is  found  in  greatest 
abundance  around  raspberry  thickets.  Often,  several  chipmunks  at  a  time  can  be  seen 
eating  the  fruit,  the  seeds  of  which  the  animals  carry  away  in  their  cheek  pouches.  While 
such  a  diet  would  supplement  a  marginal  water  supply,  I  think  the  chipmunks  take  the  fruit 
as  much  for  the  seeds  as  for  the  moist,  pulpy  parts. 

It  was  surprising  to  me  that  m,inimus — a  small,  active  species  with  high  metabolic  and 
breathing  rates — did  not  require  more  water  per  g  of  body  weight  than  did  the  larger, 
seemingly  less  active  striatus  whose  metabohc  and  breathing  rates  are  lower.  Nor  did 
comparison  of  rates  of  dehydration  and  rehydration  suggest  any  significant  difference 
between  the  water  economics  of  the  two  species.  At  Itasca,  as  in  other  parts  of  its  range, 
minimus  is  most  common  in  exposed  habitats  such  as  the  margins  of  slash  piles  and  gravel 
pits.  Exposure  to  wind  and  solar  radiation  is  maximal  in  such  situations;  daytime  tempera- 
tures, consequently,  are  often  high  and  relative  humidity  is  often  low.  In  contrast,  striatus 
remains  beneath  tree  and  shrub  cover  where,  since  insolation  and  wind  are  reduced,  daytime 
temperatures  are  lower  and  relative  humidity  is  higher  than  in  open  habitats.  In  view  of 
the  morphologic,  physiologic,  and  behavioral  differences  between  the  two  species,  the 
similarities  found  in  their  water  economics  may  represent  the  existence  of  physiologic 
adaptations  in  minimus  to  its  somewhat  more  xeric  Itascan  microhabitats. 

A  thorough  analysis  of  the  water  economics  of  these  and  other  chipmunks  could,  in 
addition  to  testing  these  results,  provide  information  relevant  to  habitat  preferences  among 
the  many  species  of  Eutamias.  In  addition,  Nadler  (Amer.  Midland  Nat.,  72:  298-312, 
1964)  has  suggested  that  physiologic  and  ecologic  study  may  shed  light  on  phylogenetic 
problems  involving  Eutamias.  I  have  found  chipmunks  to  be  difficult  subjects  for  experi- 
ments of  this  sort.  They  are  active  and  often  hard  to  catch  for  weighing.  Some  individuals 
invariably  shake  water  out  of  their  drinking  tubes;  others  are  inclined  to  pack  Htter  into  the 
tubes,  but  use  of  cedar  tow  as  litter  reduces  this.  Control  of  temperature,  light,  and  hu- 
midity, and  selection  of  experimental  animals  of  about  the  same  size  and  age,  should  reduce 
the  variability  in  performance. 

Part  of  this  work  was  done  while  I  held  an  NSF  Summer  Fellowship  for  Teaching 
Assistants,  awarded  through  the  University  of  Minnesota. — Richard  B.  Forbes,  Department 
of  Biology,  Portland  State  College,  Portland,  Oregon  97207.   Accepted  30  January  1967. 


186 


THE  OXYGEN  CONSUMPTION  AND  BIOENER- 
GETICS  OF  HARVEST  MICE 

OLIVER  P.  PEARSON 
Museum  of  Vertebrate  Zoology,  University  of  California,  Berkeley 


R\TES  of  metabolism  or  of  oxygen 
consumption  have  been  reported 
k,  for  many  species  of  small  mam- 
mals, but  little  effort  has  been  made  to 
relate  such  measurements  to  the  energy 
economy  of  small  mammals  in  the  wild. 
Such  efifort  has  been  avoided  because  the 
rate  of  metabolism  varies  so  much  with 
changes  of  the  ambient  temperature  and 
with  activity  of  the  animal.  I  believe, 
however,  that  these  variables  can  be 
handled  with  sufficient  accuracy  so  that 
one  can  make  meaningful  estimates  of 
the  24-hour  metabolic  budget  of  free-liv- 
ing mice  in  the  wild.  In  this  study  I  have 
measured  the  oxygen  consumption  of 
captive  harvest  mice  under  different  con- 
ditions, and  from  these  measurements  I 
have  estimated  the  daily  metabolic  ex- 
change of  wild  harvest  mice  living  in 
Orinda,  Contra  Costa  County,  Califor- 
nia. 

The  harvest  mice  used  in  the  study 
{Reithrodontomys  megalotis)  are  noctur- 
nal, seed-eating  rodents  living  in  grassy, 
weedy,  and  brushy  places  in  the  western 
half  of  the  United  States  and  in  Mexico. 
In  Orinda  they  encounter  cool  wet  win- 
ters (nighttime  temperatures  frequently 
slightly  below  0°  C.)  and  warm  dry  sum- 
mers (daytime  temperatures  sometimes 
above  35°  C,  but  nights  always  cool). 
They  do  nothibernate. 

MATERIAL  AND  METHODS 

Five  adult  harvest  mice  were  caught 
on  January  29  and  30,  1959,  and  were 
kept  in  two  cages  in  an  unheated  room 
with  open  windows  so  that  the  air  tem- 


perature would  remain  close  to  that  out- 
side the  building.  They  were  fed  a  mix- 
ture of  seeds  known  as  "wild  bird  seed." 
Metabolic  rates  were  tested  between  Jan- 
uary 29  and  April  1  in  a  closed-circuit 
oxygen  consumption  apparatus  similar  to 
the  one  described  by  Morrison  (1947)  but 
without  the  automatic  recording  and  re- 
filling features.  All  tests  except  the  24- 
hour  runs  were  made  during  the  daytime 
and  without  food.  Since  harvest  mice  are 
strongly  nocturnal,  several  hours  had 
usually  elapsed  between  their  last  meal 
and  the  measuring  of  their  oxygen  con- 
sumption. When  placed  in  the  apparatus, 
the  mice  usually  explored  the  metabolic 
chamber  and  groomed  their  fur  for  about 
half  an  hour  and  then  went  to  sleep  on 
the  wire  mesh  floor  of  the  chamber.  One 
hour  or  more  was  allowed  for  the  animals 
to  become  quiet  and  for  the  system  to 
come  to  temperature  equilibrium.  The 
animals  usually  were  left  in  the  chamber 
until  from  five  to  ten  determinations  of 
oxygen  consumption  had  been  made, 
during  which  they  had  remained  asleep 
or  at  least  had  made  no  gross  movements. 
Each  determination  lasted  between  9  and 
24  minutes.  The  mice  were  weighed  when 
they  were  removed  from  the  apparatus. 
Oxygen  consumptions  are  reported  as 
volume  of  dry  gas  at  0°  C.  per  gram  of 
mouse. 

RESULTS 
SIZE  X  RATE  OF  METABOLISM 

Adult  harvest  mice  weigh  between  7 
and  14  grams.  Larger  individuals  con- 
sume oxygen  at  a  lower  rate  per  gram  of 


152 


187 


A'lETABOLISM  OF  HARVEST  MICK  153 

body  weight  (I'ig.  1).  I'or  example,  at  with  restful  surroundings,  as  in  a  nest, 
12°  (\  a  12-gram  mouse  would  use  only  the  animals  probably  relaxed  their  tcm- 
1.17  times  as  much  oxygen  per  hour  as  an  perature  control  temporarily.  This  ex- 
8-gram  mouse,  although  it  is  1.5  times  as  planation  seems  plausible  in  view  of  the 
heavy.  The  various  points  in  the  regres-  known  lability  of  the  body  temperature 
sion  of  body  weight  against  rate  of  oxy-  of  some  rodents  such  as  Peromyscus 
gen  consumption  can  be  fitted  ade-  (Morrison  and  Ryser,  1959),  Dipodomys 
quately  with  a  straight  line,  and  from  the  (Dawson,  1955),  and  Perognathus  (Bar- 
slopes  of  such  lines  illustrating  the  re-  tholomew  and  Cade,  1957)  under  similar 
gression  at  different  ambient  tempera-  circumstances.  Birds  permit  their  body 
tures  it  may  be  seen  (Fig.  1)  that  at  cold  temperature  to  drop  about  2°  C.  when 
temperatures  a  variation  of  1  gram  in  they  sleep  at  night,  and  this  is  accom- 
body  weight  causes  a  greater  change  in  panied  by  a  drop  of  as  much  as  27  per 
metabolic  rate  than  at  30°  C.  At  1°,  12°,  cent  in  rate  of  metabolism  (De  Bont, 
and  24°  a  change  of  1  gram  in  weight  is  1945).  The  40  per  cent  drop  shown  by 
associated  with  a  change  in  oxygen  con-  some  of  the  mice  may  have  been  accom- 
sumption  of  0.98,  0.48,  and  0.35  cc/g/hr,  panied  by  a  drop  in  body  temperature  of 
respectively.  several  degrees. 

At  warm  and  moderate  temperatures 
there  was  little  variation  in  the  measure-  resting  met.^bolism  at  different 
ments  of  each  mouse  during  any  one  run  temperatures 
(Fig.  1),  but  at  1°  C.  the  variation  was  Since  the  weights  of  adult  harvest  mice 
sometimes  enormous.  Since  each  meas-  vary  so  much,  it  is  desirable  to  eliminate 
urement  was  made  over  a  period  while  the  the  size  variable  by  adjusting  all  rates  of 
mouse  was  inactive,  the  variation  must  metabolism  to  a  single  average  size  (9 
stem  from  a  real  difference  in  the  resting  grams) .  This  has  been  done  by  using  the 
metabolism  of  each  mouse  at  different  series  of  regression  lines  in  Figure  1. 
times.  I  believe  that  lability  of  body  tem-  Where  each  of  these  lines  crosses  the  9- 
perature  is  the  cause.  Harvest  mice  ex-  gram  ordinate,  that  value  is  taken  as  the 
posed  to  cold  and  hunger  in  box  traps  appropriate  rate  for  a  "standard"  9-gram 
sometimes  are  found  to  be  torpid  and  harvest  mouse  and  is  used  in  Figure  2. 
with  a  cold  body  temperature.  If  they  The  middle  curve  in  Figure  2  shows 
are  tagged  and  released,  they  can  be  re-  that  the  minimum  rate  of  oxygen  con- 
captured  in  good  health  at  subsequent  sumption  of  harvest  mice  (2.5  cc/g/hr 
trappings,  demonstrating  that  harvest  ^or  a  9-gram  mouse)  is  reached  at  the 
mice  have  a  labile  body  temperature  and  relatively  high  ambient  temperature  of 
can  recover  trom  profound  hypothermia.  ^^°  or  34°  C.  and  that  there  is  almost  no 
During  the  metaboUc  tests  at  1°  C,  espe-  zone  of  thermal  neutrality.  Rate  of  me- 
cially  those  with  the  mouse  in  a  nest,  tabolism  almost  certainly  begins  to  in- 
there  was  a  tendency  for  most  of  the  crease  before  36°  C.  is  reached  so  that  the 
measurements  to  lie  at  one  level;  but  zone  of  minimum  metabolism  could  not 
there  would  be  a  few  very  low  readings  include  more  than  3°.  The  critical  tem- 
and  a  few  intermediate  readings,  pre-  perature  (33-34°)  is  remarkably  close  to 
sumably  as  the  animal  entered  and  the  upper  lethal  temperature.  The  single 
emerged  from  the  low-metaboUc  condi-  animal  tested  at  37°  died  after  two  hours 
tion  (best  shown  by  the  U^-gram  mouse  at  this  temperature  but  provided  several 
in  Fig.  1).  In  response  to  cold  coupled  good  measurements  before  entering  the 


188 


12 

II 
^  10 

(T 

I 

o 
B  8 

z 
9  7 

I- 

Q. 

2   6 

3 

in 

§5 
o 

z  4 

UJ 

o 

^  3 

o 


\ 


^"^'f^ONEST 


•NONESr 


8 


9  10 

WEIGHT  IN   GRAMS 


II 


12 


Fig.  1.— The  relation  beUveen  body  weight  and  rale  of  oxygen  consumption  under  different  conditions, 
showing  also  the  variation  in  individual  measurements.  Each  cluster  or  vertical  array  of  points  represents 
a  series  of  values  obtained  from  a  single  individual. 


189 


METABOLISM  OF  HARVEST  MICE 


155 


final  coma.  Because  of  the  large  exposed 
surface  of  calcium  chloride  and  soda  lime 
in  the  metabolic  chamber,  relative  hu- 
midity was  probably  low;  heat  death 
would  probably  occur  at  an  even  lower 
temperature  under  humid  conditions  in 
which  cooling  by  evaporation  would  be 
limited. 


ercd  body  temperature.  Inclusion  of 
these  low  values  causes  the  apparent  de- 
crease of  the  slope  of  the  two  curves  be- 
tween 12°  and  1°.  No  body  temperatures, 
however,  dropped  to  the  torpid  level. 
Rcithrodontomys  megalotis  is  able  to  main- 
tain its  temperature  well  above  the  tor- 
pid level  even  when  sleeping  in  cold  sur- 


I    I    I    I    I 


T— r 


10 


_9 

O  ' 

z6 

o 

Q.  ^ 

z 


THREE  MICE 
HUDDLED 


uj  ^ 

>• 

X 

o 


r     I 


I     I     I     I 
-  NOT 
HUDDLED 


r 


p 


•XX 


• 


Xf 


'■■■'■■'■ 


■    ■    '    ■ 


X 


I    I    I 


BODY 
TEMR^< 
■'''''■■*' 


8  12  16  20  24 

TEMPERATURE    °C 


28 


32 


36 


Fig.  2. — The  rate  of  oxygen  consumption  of  resting  harvest  mice  at  different  temperatures  in  a  nest, 
without  nest,  and  without  fur.  All  three  curves  have  been  adjusted,  on  the  basis  of  the  regression  Hnes  shown 
in  Fig.  1,  to  represent  a  9-gram  mouse.  Triangles  indicate  rate  of  oxygen  consumption  of  three  mice  huddled 
together  without  a  nest  compared  with  the  expected  rate  for  the  same  three  mice  singly  (average  weight 
8.5  grams).  I  am  grateful  to  Martin  Murie  for  supplying  the  value  for  deej)  body  temperature,  which  was 
the  average  of  manj^  determinations  made  during  the  day  and  night  at  ambient  temperatures  between 
14°  and  27°  C. 


The  increase  in  rate  of  metabolism  at 
cool  temperatures  is  almost  linear  be- 
tween ?>i°  and  12°;  each  drop  of  1°  C. 
causes  an  increase  in  the  rate  of  oxygen 
consumption  of  0.27  cc/g/hr.  This  rate  of 
change,  possibly  because  of  the  small  size 
of  harvest  mice,  is  greater  than  that  of 
any  of  the  rodents  listed  by  Morrison  and 
Ryser  (1951)  and  by  Dawson  (1955).  The 
averages  used  for  the  two  points  at  1°  C. 
include  several  low  values  obtained  while 
the  animals  probably  had  a  slightly  low- 


roundings.  In  this  respect  it  differs  from 
the  pocket  mouse  {Perognathus  longi- 
membris),  a  mouse  with  which  it  should 
be  compared  because  of  its  similarly 
small  size.  When  pocket  mice  are  caged 
at  cold  temperatures  with  adequate 
food,  they  either  drop  into  torpor  or  are 
continually  awake  and  active.  They  may 
even  be  unable  to  maintain  a  high  body 
temperature  during  a  prolonged  period 
of  sleep  at  cool  temperatures  (Bartholo- 
mew and  Cade,  1957). 


190 


156 


OLRER  P.  PEARSON 


The  only  other  report  on  the  rate  of 
oxygen  consumption  of  harvest  mice  lists 
a  rate  of  3.8  cc/g/  hr  at  24°  C.  for  mice 
with  an  average  weight  of  9.6  grams 
(Pearson,  1948a).  This  rate  is  almost  10 
per  cent  lower  than  the  comparable  rate 
obtained  from  I'lgure  1  and  is  below  the 
range  of  variation  obtained  at  this  tem- 
perature. The  difference  may  be  ac- 
counted for  by  the  fact  that  the  mice 
used  in  the  earlier  study  were  acclimated 
to  a  warmer  temperature  (for  discussion 
of  the  effect  of  acclimatization  on  me- 
tabolism see  Hart,  1957). 

INSl'LATING  EFFECTIVENESS  OF  FL'R 

Figure  2  shows  also  the  metabolic  ef- 
fect of  removing  all  the  fur  (277  mg.  in 


cent  at  intermediate  temperatures  and  24 
per  cent  at  1°  C.  (lowest  curve  in  Fig.  2). 
To  obtain  these  measurements,  individ- 
ual mice  placed  in  the  metabolic  chamber 
were  provided  with  a  harvest  mouse  nest 
collected  from  the  wild  (shredded  grass 
and  down  from  Compositae),  and  this 
the  mouse  ciuickly  rebuilt  into  an  almost- 
complete  hollow  sphere  about  tliree 
inches  in  diameter.  Metabolic  rates  were 
counted  only  when  a  mouse  was  resting 
Cjuietly  deep  in  the  nest. 

THERMAL  ECONOMY  OF  IIIDDLINC, 

The  metabolic  economy  of  huddling 
was  measured  on  one  occasion  with  three 
mice  at  an  environmental  temperature  of 
1°  C.  without  nesting  material.  The  rate 


10 


o 

o 

7 

eh 


/\r~. 


\j 


-VA..AA J  V  ^V,__  _^  /-v.A/.-/\/v.7 


v^- 


\/ 


\/"^v 


12       I        2       3       4       5        6       7       e       9       10      II       12       I        2        3       4       5       6       7       8       9       10      II       12 

PM  AM 

Fig.  3. — Rale  of  oxygen  consumption  of  a  9-gram  harvest  mouse  for  24  hours  at  12°  C. 


the  single  8.8-gram  specimen  used)  with 
an  electric  clipper.  When  calculating  the 
points  for  the  curve  in  Figure  2,  0.28 
grams  was  added  to  the  naked  weight 
and  then  this  rate  was  adjusted  to  that 
for  a  9-gram  animal  on  the  basis  of  the 
regression  lines  shown  in  I'lguie  1.  The 
rate  of  metabolism  of  the  naked  mouse 
was  about  35  per  cent  higher  at  each  of 
the  temperatures  used,  and  the  rate  in- 
creased 0.38  cc/g/hr  for  each  1°  C.  drop 
in  air  temperature. 

INSULATING  EFFECTIVENESS  OF  NESTS 

When  normal,  fully  furred  mice  were 
given  an  opportunity  to  increase  their  in- 
sulation by  constructing  nests,  their  met- 
abolic rates  were  lowered  about  17  per 


of  metabolism  per  gram  of  huddled  mice 
was  28  per  cent  less  than  it  would  have 
been  for  a  single  one  of  the  mice  (Fig.  2). 
The  metabolic  saving  would  probably  be 
greater  when  more  mice  were  huddled  to- 
gether and  less  when  only  two  mice  were 
huddled,  as  is  true  for  feral  Mus  (Pear- 
son, 1947)  and  laboratory  mice  (Prychod- 
ko,  1958). 

24-HOUR  OXYGEN  CONSUMPTION  IN  CAPTIVITY 

Figure  3  illustrates  the  rate  of  oxygen 
consumption  of  a  mouse  kept  in  the  ap- 
paratus at  12°  C.  without  nesting  mate- 
rial but  with  food  and  water  for  24  hours. 
The  mouse  consumed  1,831  cc.  of  oxygen 
to  give  an  average  rate  of  8.48  cc/g/hr. 
This  is  equal  to  a  heat  production  of 


191 


METABOLISM  OF  HARVEST  MICE 


157 


about  8.8  Calories  per  day.  In  agreement  sumed  during  rest  and  during  activity  is 
with  the  fact  that  activity  of  harvest  proportionately  great  at  warm  tempera- 
mice  in  the  wild  is  greatest  shortly  after  tures  and  small  at  cold  temperatures, 
dusk  (Pearson,  1960),  the  oxygen  con- 
sumption was  greatest  at  that  time.  The  ^^^^^'^  °^-  activity  on  metabolfsm 
prolonged  low  i)eriod  lasting  from  aljout  An  athlete  is  able,  for  short  periods,  to 
8:30  to  10:0:)  p.m.  was  unexpected  in  raise  his  rate  of  metabolism  to  a  level  15 
this  nocturnal  animal.  to  20  times  his  basal  rate,  but  small 
Pearson  (1947)  used  as  an  indicator  of  mammals  do  not  match  this  effort.  The 
the  noctuvnality  of  different  species  the  peak  metabolic  effort  of  mice  running  in 
ratio  of  the  total  amount  of  oxygen  con-  ^  wheel  is  only  6  to  8  times  their  basal 
sumed  at  ni.uht  (6:00  p.m.  to  6:00  A.m.)  rate  (Hart,  1950).  At  (f  C.  lemmings  run- 
to  that  consumed  in  the  daytime.  I'or  the  ning  in  a  wheel  at  a  speed  of  15  cm/sec 
harvest  mouse  described  in  Mgure  3,  the  increase  their  o.xygen  consum[)tion  less 
ratio  is  low- -1.02-  but  it  should  be  than  35  per  cent  above  the  level  of  rest- 
pointed  out  that  the  record  was  made  at  ing  lemmings  (Hart  and  Heroux,  1955). 
12°  C,  which  is  colder  than  the  tempera-  At  cool  ambient  temperatures,  such  as 
ture  used  for  the  species  in  the  earlier  re-  this,  small  mammals  ex[-)end  so  much 
port.  Temperature  affects  the  night/day  energy  at  rest  that  a  considerable  amount 
ratio  of  oxygen  consumption  because  the  of  activity  causes  only  a  proi)ortionately 
ditterence    in    amount    of    oxygen    con-  small  increase  in  oxygen  consumption ; 

T.VHLK  1 

'rill';  24  iiouK  ()XV(;i;\  coxsu.nu' rnix  fix  ((  .)  of  a  9-(;r.\m  harv  i:si' 

Mousi'.  nuKixc;  DkckmuI'R  axi)  Junjc  at  (:)KIX|)A,  Camiokxia 


Willi 

Wilh 

Willi- 

Undcr- 

With- 

Undct- 

out 

.1,'iounci 

out 

{^round 

Xc^l 

Xest 

Xesl 

Xest 

Noclur- 

nal 

haljit 

4  hr.  above  grouiul 
at  l°C.* 

367 

367 

4  hr.  above  ground 
at  12°C.t 

297 

297 

20  hr.  under  ground 

1,548 

1,296 

20  hr.  under  ground 

1,152 

954 

at  ]0°C.t 

at  18°C.§ 

Activity  correction |! 

+  119 
2,034 

+  119 
1,782  cc. 

Activity  correction | 

+  119 
1,568 

+  119 

1  ,370  cc. 

(8.55  Ca].)# 

(6.58  Cal.),f 

i^iunial 

lialiit 

20  hr.  under  ground 
at  10°C.| 

1,.548 

1,296 

20  hr.  under  grounel 
at  18°C.§ 

1,152 

954 

4   lir.   above   ground 

M3 

3M 

4  hr.   above  ground 

155 

155 

at6°C.** 

at  25°  C. ft 

Activity  correctionjl 

+  119 
2,000 

+  119 

Activit}'  correction] 

+  119 
1,426 

+  119 

1 ,  748  cc. 

1,228  cc. 

(8.39  Cal.)# 

(5.89  Cal.)# 

*  ^fcaii  tcniiicrature  in  runways  at  time  of  passage  of  harvest  mite  in  December. 

t  Mean  temperature  in  runways  at  time  of  passage  of  harvest  mice  in  June. 

X  Underground  temperature  in  December. 

§  Underground  temperature  in  June. 

II  Add  40  per  rent  of  the  oxygen  consumption  on  the  surface  at  a  temperature  of  12°  C 

//  Assunii-d  4..S  (  al.  per  liler  of  oxygen. 

*'■  .Mean  half-hourly  temperature  in  runways  l>etwcen  6  a.m.  and  6  P.M.  in  DeLtmbcr. 

tt  Mean  half-hoiiily  temperature  in  runways  between  6  a.m.  and  6  p.m.  in  June. 


192 


158                                                   OLIVER  P.  PEARSON 

and  at  cold  temperatures  the  metabolic  24-hour  metabolism  in  the  field 
cost  of  keeping  warm  may  be  so  high  as  The  preceding  observations  indicate 
to  leave  little  or  no  capacity  tor  exercise  that  ambient  temperature  is  a  much 
(Hart,  1953).  During  measurement  of  the  more  important  variable  than  activity  in 
resting  metabolism  of  harvest  mice,  nu-  the  24-hour  energy  budget  of  harvest 
meious  measuring  periods  had  to  be  dis-  mice  in  the  wild.  By  use  of  automatic  de- 
carded  because  the  mouse  was  moving  vices  that  record  the  temperature  in 
around  in  the  metabolism  chamber.  Such  mouse  runway?  whenever  a  mouse  passes 
activity  rarely  raised  the  oxygen  con-  by,  the  temperature  encountered  by  har- 
sumption  more  than  40  per  cent  above  vest  mice  during  their  nightly  periods  of 
the  level  of  a  resting  animal  at  the  same  activity  are  known  (Pearson,  1960).  I 
temperature.  During  the  24-hour  run  at  have  also  recorded  throughout  the  year 
12°  C,  the  highest  metabolic  rate  oc-  the  temperature  five  inches  below  the 
curred  during  an  11-minute  period  when  surface  of  the  ground.  This  gives  an  ap- 
the  average  oxygen  consumption  was  proximation  of  the  temperature  encoun- 
10.36  cc/g/hr.  This  is  only  40  per  cent  tered  by  the  mice  while  they  are  in  their 
greater  than  the  lowest  rate  recorded  for  retreats  during  the  daytime.  Some  of 
that  mouse  during  any  one  measuring  these  surface  and  underground  tempera- 
period.  The  maximum  metabolic  effort  ture  measurements  have  been  used  m  the 
recorded  for  any  harvest  mouse  was  that  calculations  summarized  m  Table  L 
of  an  8.6-gram  mouse  at  1°  C.  This  ani-  ^  To  complete  the  calculations  m  Table 
,  •  ^  1  •  •  1  •  J  1,  it  has  been  necessary  to  estimate  how 
mal  persisted  in  gnawing,  exploring,  and  ,  ,  ,  ^/^,  , 
.  ,  ,  ,  ,  r  many  hours  of  each  24  the  mouse  spends 
trying  to  escape  from  the  chamber  tor  /,           .          r  .lu               i        i  u 

•^    ^,             V          T^     •             1^     •  ori  the  surface  of  the  ground  and  how 

more  than  two  hours.  During  one  lO-mm-  ^^^^  ^^^^^  ^^^  ^^^^^^^   ^^  ^^^^  ^^^^ 

ute  period  its  oxygen  consumption  aver-  ^^^^^^  ^^  j  ^^^^  ^^^^  ^^  estimate  based 
aged  15.8  cc/g/hr,  which  is  50  per  cent  ^^  ^^^  behavior  of  captive  animals  and 
higher  than  the  rate  of  a  resting  mouse  at  ^^  automatic  recordings  made  at  the  exit 
the  same  air  temperature  and  six  times  of  ^n  underground  nest  box  being  used  by 
the  minimum  value  for  the  species  at  ^ild  harvest  mice.  Admittedly  this  esti- 
thermal  neutrahty.  This  is  probably  not  mate  (4  hours  on  the  surface  each  night) 
far  from  the  peak  metabolic  effort  of  the  could  be  wrong  by  50  per  cent  or  more, 
species.  but  it  should  be  noted  that  an  error  of 
On  several  occasions  I  have  watched  two  hours  in  this  estimate  would  only 
undisturbed  harvest  mice  carrying  on  alter  the  answer  (the  total  24-hour  me- 
their  normal  activities  in  the  wild,  and  I  tabolism)  by  about  25  per  cent.  Assum- 
have  been  impressed  by  their  leisurely  ing  that  the  rate  of  oxygen  consumption 
approach  to  life.  Hard  physical  labor  and  during  above-ground  activity  is  40  per 
strenuous  exercise  must  occur  quite  in-  cent  higher  than  the  rate  of  a  mouse  rest- 
frequently.  Most  normal  activities  of  ing  at  12°  C.  (see  above),  the  activity 
harvest  mice  are  probably  accomplished  correction  used  in  Table  1  can  be  calcu- 
without  a  rise  in  metabolic  rate  more  lated. 

than  50  per  cent  above  what  it  would  be  In  24  hours  in  December  a  harvest 

in  a  resting  animal  at  the  same  air  tem-  mouse  uses  8.55  Calories,  and  in  June, 

perature.  6.58  Calories  (Table  1),  assuming  that 


193 


METABOLISM  OF  HARVEST  MICE 


159 


the  mouse  has  the  benefit  of  a  nest.  A 
nest  reduces  his  daily  energy  budget  by 
about  12  per  cent.  These  estimates  of 
daily  metabolic  demands  seem  reason- 
able when  compared  with  the  values  ac- 
tually obtained  by  measuring  the  24-hour 
oxygen  consumption  of  captive  animals, 
as  reported  above.  The  average  metabol- 
ic impact,  or  daily  degradation  of  en- 
ergy, by  a  single  harvest  mouse  should  be 
somewhere  between  that  in  December 
and  that  in  June,  perhaps  7.6  Calories. 
This  is  about  the  same  as  that  of  a  hum- 
mingbird in  the  wild  (Pearson,  1954)— 
less  than  half  that  of  a  much  heavier 
English  sparrow  (Davis,  1955). 

BIOENERGETICS 

In  seasons  when  harvest  mice  are  abun- 
dant, there  may  be  twelve  of  them  per 
acre  (Brant,  1953).  At  that  population 
density,  the  species  would  be  dissipating 
at  the  rate  of  91  Calories  per  acre  per  day 
the  solar  energy  captured  by  photosyn- 
thesis, or  something  like  ^  of  1  per  cent 
of  the  energy  stored  each  day  by  the 
plants  in  good  harvest-mouse  habitat  in 
the  Orinda  area.  This  percentage  was  cal- 
culated using  a  net  productivity  of 
20,000  Cal/acre/day,  which  was  esti- 
mated by  assuming  4  Calories  per  gram 
of  dry  vegetation  (based  on  data  in  Brody, 
1945,  pp.  35,  788)  and  an  annual  crop 
of  1,800  kg.  of  dry  vegetation  per  acre 
(based  on  Bentley  and  Talbot,  1951). 
The  harvest  mice  on  this  hypothetical 
acre  are  causing  about  the  same  caloric 
drain  on  the  environment  as  all  the  small 
mammals  in  the  acre  of  forest  described 
by  Pearson  (19486). 

By  using  caloric  units,  direct  compari- 
son can  be  made  of  the  metabolic  impact 
of  different  species,  as  in  the  example 
above.  Similarly,  the  metabolic  cost  of 
different  activities  and  different  habits 
can  be  compared  (Pearson,  1954).  For 


example,  harvest  mice  are  strongly  noc- 
turnal (Pearson,  1960),  in  spite  of  the 
fact  that  air  temperatures  are  much 
colder  at  night  and  force  mice  to  con- 
sume more  oxygen  and  more  food  than  if 
they  were  diurnal.  Since  evolution  has 
permitted  nocturnahty  to  persist,  it 
seems  logical  to  assume  that  the  value  of 
nocturnality  to  harvest  mice  is  greater 
than  the  metabolic  cost.  I  estimate  that 
during  a  24-hour  period  in  December  a 
9-gram  harvest  mouse  uses  0.16  more 
Calories  by  being  nocturnal  than  it 
would  if  it  were  diurnal  (Table  1).  In 
summer,  the  difference  is  even  greater, 
0.69  Calories.  The  average  is  0.42  Cal- 
ories, or  about  3|  grains  of  wheat.  This  is 
a  rough  estimate  of  the  price  each  har- 
vest mouse  pays  for  nocturnality.  Some 
environmental  pressure  makes  harvest 
mice  remain  nocturnal,  and  this  pressure 
must  be  more  than  0.42  Calories  per 
mouse  per  day.  If  harvest-mouse  noc- 
turnality evolved  for  one  reason  only— to 
avoid  predation  by  hawks — -then  we 
would  have  discovered  a  minimum  esti- 
mate of  the  predation  pressure  of  hawks 
on  harvest  mice.  Surely  the  situation  is 
not  this  simple;  nevertheless,  it  is  inter- 
esting to  measure  the  pressure  that 
makes  harvest  mice  nocturnal  even  if  the 
cause  of  the  pressure  is  not  known. 

SUMMARY 

Oxygen  consumption  of  harvest  mice 
reaches  a  minimum  of  2.5  cc/g/hr  at  an 
ambient  temperature  of  33°  C,  and  the 
zone  of  thermal  neutrality  is  not  more 
than  3°.  Each  drop  of  1°  in  ambient  tem- 
perature causes  an  increase  in  the  rate  of 
metabolism  of  0.27  cc/g/hr.  Removing 
the  fur  raises  the  rate  of  metabolism 
about  35  per  cent,  and  use  of  a  nest 
lowers  it  17  to  24  per  cent.  Huddling  by 
three  mice  at  1°  reduces  the  rate  28  per 
cent. 


194 


160 


OLIVER  P.  PEARSON 


Jvxcrcise  at  cool  tcm{)eraturcs  causes  a 
relatively  small  increase  in  the  rate  o£ 
metabolism,  whereas  change  of  ambient 
temperature  has  a  great  effect!  Making 
use  of  the  temperatures  that  harvest  mice 
are  known  to  encounter  in  the  wild,  the 
24-hour  oxygen  consumption  of  a  wild 
harvest  mouse  was  calculated  to  be  1,782 
cc.  in  December  and  1,370  cc.  in  June. 
The  average  (1,576  cc.)  is  equivalent  to 


about  7.6  Calories  per  day.  A  dense  p(Jp- 
ulation  of  harvest  mice  would  dissipate 
about  91  Calories  per  day  per  acre,  which 
is  about  ^  of  1  per  cent  of  the  energy 
stored  by  the  plants  each  day. 

By  being  nocturnal,  harvest  mice  en- 
counter cooler  temperatures,  and  this 
habit  increases  the  daily  energy  budget 
of  each  mouse  by  0.42  Calories,  or  about 
3|  grains  of  wheat. 


LITERATURE  CITED 


Bartholomew,  G.  A.,  and  C.a.de,  T.  J.  1957.  Tem- 
])erature  regulation,  hibernation,  and  aestivation 
in  the  little  pocket  mouse,  Perognatlnts  longintem- 
bris.  Jour.  Mammal.,  38:60-72. 

Bentley,  J.  R.,  and  T.^lbot,  M.  W.  195L  Efficient 
use  of  annual  plants  on  cattle  ranges  in  the 
California  foothills.  U.S.  Dept.  .Agriculture,  Cir- 
cular No.  870,  52  pp. 

Brant,  D.  H.  1953.  Small  mammal  populations  near 
Berkeley,  California:  Reithrodontomys,  Peromys- 
cus,  Microtus.  Doctoral  thesis,  University  of  Cali- 
fornia, Berkeley. 

Brody,  S.  B.  1945.  Bioenergetics  and  growth.  New- 
York:  Reinhold  Publishing  Corp. 

D.xvis,  E.  A.,  Jr.  1955.  Seasonal  changes  in  the 
energy  balance  of  the  English  Sparrow.  Auk, 
72:385-411. 

Dawson,  VV.  R.  1955.  The  relation  of  oxygen  con- 
sumption to  temperature  in  desert  rodents.  Jour. 
Mammal.,  36:543-53. 

De  Bont,  A.-F.  1945.  Metabolisme  de  repos  de 
quelques  es])eces  d'oiseaux.  .Ann.  Soc.  Roy.  Zool. 
Belgique,  75  (1944)  :75-80. 

Hart,  J.  S.  1950.  Interrelations  of  daily  metabolic 
cycle,  activity,  and  environmental  temperature 
of  mice.  Canadian  Jour.  Research,  D,  28:293- 
307. 

.  1953.  The  influence  of  thermal  acclimation 

on  limitation  of  running  activity  by  cold  in 
deer  mice.  Canadian  Jour.  Zool.,  31:117-20. 


.   1957.   Climatic  and   temperature  induced 

changes  in  the  energetics  of  homeotherms.  Revue 
Canadienne  de  biol.,  16:133-74. 

Hart,  J.  S.,  and  Heroux,  O.  1955.  Exercise  and 
temperature  regulation  in  lemmings  and  rabbits. 
Canadian  Jour.  Biochem.  &  Physiol.,  33:428-35. 

Morrison,  P.  R.  1947.  An  automatic  api)aratus 
for  the  determination  of  oxygen  consumption. 
Jour.  Biol.  Chem.,  169:667-79. 

Morrison,  P.  R.,  and  Ryser,  F.  .\.  1951.  Tempera- 
ture and  metabolism  in  some  Wisconsin  mam- 
mals. Federation  Proc,  10:93-94. 

.  1959.  Body  temperature  in  the  white-footed 

mouse,  Peromyscus  leiicopus  noveboracensis.  Phvs- 
iol.  Zool.,  32:90-103. 

Pearson,  0.  P.  1947.  The  rate  of  metabolism  of  some 
small  mammals.  Ecology,  28:127-45. 

.  1948a.  Metabolism  of  small  mammals,  with 

remarks  on  the  lower  limit  of  mammalian  size. 
Science,  108:44. 

.  19486.  Metabolism  and  bioenergetics.  Sci- 


entific Monthly,  66:131-34. 

.    1954.    The   daily   energy   requirements   of 

a  wild  Anna  Hummingbird.  Condor,  56:317-22. 
1960.  Habits  of  harvest  mice  revealed  by 


automatic  photographic  recorders.  Jour.  Mam- 
mal, (in  press). 
Prychodko,  W.  1958.  Effect  of  aggregation  of  labo- 
ratory mice  {Mus  musculus)  on  food  intake  at 
different  temperatures.  Ecology,  39:500-503. 


Reprinted  for  private  circulation  from 
PHYSIOLOGICAL  ZOOLOGY 

Vol.  XXXIII,  No.  2,  April  1960 

Copyright  1960  by  the  University  of  Chicago 


195 


OXYGEN  CONSUMPTION,  ESTIVATION,  AND  HIBERNATION  IN 
THE  KANGAROO  MOUSE,  MICRODIPODOPS  PALLIDUS^ 

GEORGE  A.  BARTHOLOMEW  AND  RICHARD  E.  MacMILLEN 

Departments  of  Zoology,  University  of  California,  Los  Angeles, 
and  Pomona  College,  Claremont,  California 

THE  pallid  kangaroo  mouse  occurs  material  and  methods 
only  in  the  desert  parts  of  western  Experimental  animals— The  twenty- 
Nevada  and  extreme  eastern  Call-  ^^iree  kangaroo  mice  used  were  trapped 
fornia.  Its  habitat  is  restricted  to  areas  of  ^^  ^^^^  ^^^^^  f^^^  rniles  south  of  Arle- 
fine  sand  which  support  some  plant  ^^^^  Ranch,  Esmeralda  County,  Neva- 
growth.  Like  its  relatives,  the  kangaroo  ^^^  j^^  ^pj.-^^  ^959^  ^nd  May,  1960.  They 
rats  (Dipodomys)  and  the  pocket  mice  ^^^^  housed  individually  in  small  ter- 
{Perognathus) ,  it  is  nocturnal,  fossorial,  ^^^^^  p^^^^y  ^^g^j  ^ith  ftne  sand,  kept  in  a 
and  gramnivorous  and  can  under  some  ^indowless  room  on  a  photoperiod  of  12 
circumstances  live  indefinitely  on  a  dry  j^^^j.^^  ^^^  f^^  ^^  ^  ^i^^  of  j^ixed  bird 
diet  without  drinking  water.  The  genera]  ^^^^  supplemented  occasionally  with 
life  history  (Hall  and  Linsdale,  1929)  of  ^^^-^^  p^g^g^  ^f  cabbage.  Survival  was 
this  kangaroo  mouse  and  the  details  of  excellent,  and  some  of  the  animals  were 
its  distribution  (Hall,  1946)  are  known,  ^^^^  f^j.  ^^gj.  ^g^^  months, 
but  virtually  no  quantitative  data  on  its  ^^^y  temperatures— AW  temperatures 
physiology  are  available.  ^g^g  measured  with  30-gauge  copper- 
The  present  study  was  undertaken  to  gonstantan  thermocouples  connected  to 
compare  the  thermoregulation  of  Micro-  ^  recording  potentiometer.  All  body  tem- 
dipodops  with  that  of  the  better-known  pg^atures  were  taken  orally  by  inserting 
genera,  Dipodomys  and  Perognathus.  ^  thermocouple  to  a  depth  of  at  least 
These  three  genera  belong  to  the  family  2  cm 

Heteromyidae,  which  has  been  more  sue-  Ambient  temperatures— The  ambient 

cessful  in  occupying  the  and  parts  of  tgn^pg^atures  were  monitored  with  ther- 

Tof'of  mTmrnalT''''^  ^^^"^  ^""^  *'^^''     "^«^«^P^^^  ^^^  controlled  by  insulated 
^      P  ^  ■  chambers  equipped  with  automatic  heat- 

1  This  study  was  aided  in  part  by  a  contract  be-      ing     and     cooling     units,     blowers,     and 
tween  the  Office  of  Naval  Research,  Department  of      Uahts 
the  Navy,  and  the  University  of  California  (Nonr         °        '  •  r\ 

266[3ll).  Oxygen    consumption. — Oxygen    con- 

177 


196 


178 


GEORGE  A.  BARTHOLOMEW  AND  RICHARD  E.  MacMILLEN 


sumption  was  measured  by  placing  a 
mouse  in  an  air-tight  500-cc.  glass  con- 
tainer equipped  with  a  thermocouple  and 
ports  for  the  introduction  and  removal 
of  air.  The  bottom  of  the  container  was 
covered  to  a  depth  of  about  1  cm.  with 
fine  dry  sand.  The  glass  container  with 
animal  inside  was  placed  in  a  tempera- 
ture-control chamber,  and  dry  air  was 
metered  through  the  container  at  a  rate 


the  response  of  body  temperature  {Tb) 
to  moderately  low  ambient  temperatures 
{Ta),  kangaroo  mice  were  placed  at  Ta 
of  7°-9°  C.  for  five  days  starting  May  11, 
1959,  with  food  available  in  excess; 
measurements  of  Tb  were  made  at  24- 
hour  intervals.  There  were  no  apparent 
changes  in  Tb  during  the  test  period,  nor 
was  the  mean  Tb  significantly  different 
from  that  of  animals  maintained  at  room 


42 
o 

o 

q:  40 
iij 


i  38 

ffi 


36 


o 

o 
I 


o 

o 

I 
^. 

OJ 
CO 


B 


o 

o 

in 

in" 

to 

I 

If) 

^" 
ro 


D 


o 

o 
lO 

d 

I 
m 

ro 


42 


40 


38 


36 


Fig.  1. — Body  temperatures  of  M.  pallidus  at  various  ambient  temperatures.  A,  47  measurements  on 
twelve  animals;  B,  38  measurements  on  thirteen  animals;  C,  7  measurements  on  four  animals;  D,  9  measure- 
ments on  four  animals  (three  other  animals  tested  at  this  temperature  died).  The  horizontal  lines  indicate 
the  means  {M).  The  rectangles  inclose  M  ±  a^-  The  vertical  lines  indicate  the  range. 


of  250  cc/min  and  then  delivered  to  a 
Beckman  paramagnetic  oxygen  analyzer 
which,  used  in  conjunction  with  a  re- 
cording potentiometer,  gave  a  continu- 
ous record  of  oxygen  consumption.  All 
data  used  were  from  post-absorptive 
animals. 

RESULTS 

Body  temperature  during  normal  ac- 
tivity.— Normally  active  animals  kept  at 
room  temperature  (22.4°-25.4°  C.)  had 
body  temperatures  ranging  from  slightly 
less  than  37°  to  as  high  as  41°  C,  with 
a  mean  of  38.8°  C.  (Fig.  1).  To  determine 


temperature.  The  animals  appeared  nor- 
mally active  and  unaffected  by  the 
change  in  environmental  temperature. 

Animals  were  maintained  at  Ta  of 
37.5°-40.5°  C.  for  24  hours  to  test  their 
response  to  moderately  high  environ- 
mental temperatures.  They  showed  a 
conspicuous  elevation  in  Tb  with  a  mean 
almost  2°  C.  higher  than  that  of  animals 
at  room  temperature.  Animals  main- 
tained at  Ta  close  to  35°  C.  also  became 
hyperthermic  and  showed  a  mean  Tb  in- 
termediate between  that  of  animals  held 
at  room  temperatures  and  those  held  at 
39°  C.  There  was  no  mortality  in  animals 


197 


THERMOREGULATION  IN  THE  KANGAROO  MOUSE 


179 


held  at  35°  C,  but  exposure  to  39°  C.  for 
more  than  a  few  hours  killed  three  out  of 
the  seven  animals  tested.  At  a  high  Ta 
the  kangaroo  mice  did  not  salivate  or 
pant;  they  merely  sprawled  out  fiat  on 
the  sand  with  legs  extended  and  lower 
jaw  and  neck  prone  on  the  substrate. 
This  prone  posture  alternated  with  brief 
bursts  of  intense  activity  characterized 
by  repeated  shifts  in  position  and  much 
digging  and  moving  of  sand. 


gm.)  is  1.8  cc  02/gm/hr  when  the  for- 
mula M  =  3.811^-''  "  jg  ygg(j  (^ggg  Brody, 

1945,  and  Morrison,  Ryser,  and  Dawe, 
1959).  The  observed  basal  metabolism 
of  our  kangaroo  mice  (mean,  1.3  ±  0.2 
cc  02/gm/hr)  was  about  three-fourths 
of  the  predicted  value.  This  relatively 
low  figure  is  consistent  with  the  obser- 
vation on  some  other  heteromyids  (Daw- 
son, 1955). 

The  only  comparative  data  on    the 


a: 

X 


o 
o 


-|4 


•• 


•  • 


•  •     • 

•      •  • 

•  •    • 


10 


20 


30 


40 


Fig.  2. — The  relation  of  oxygen  consumption  to  ambient  temperature.  Data  obtained  from  ten  animals. 
Each  point  represents  the  minimum  level  of  oxygen  consumption  maintained  by  an  animal  for  half  an  hour. 
Oxygen  volumes  are  corrected  to  0°  C.  and  760  mm.  (Hg.)  pressure. 


Oxygen  consumption. — The  relation  of 
oxygen  consumption  to  Ta  is  summarized 
in  Figure  2.  There  is  no  clearly  defined 
zone  of  thermal  neutrality,  but  oxygen 
consumption  is  minimal  at  about  35°  C. 
The  increase  in  oxygen  consumption  at 
temperatures  above  35°  C.  is  relatively 
more  rapid  than  is  the  increase  below 
this  point  of  thermal  neutrality.  No  dif- 
ferences in  oxygen  consumption  were  ap- 
parent between  males  and  females. 

The  calculated  metabolism  of  Micro- 
dipodops  paUidus    (mean   weight,    15.2 


energy  metabolism  of  Microdipodops  is 
that  of  Pearson  (1948)  on  M.  megacepha- 
lus.  Pearson's  data,  obtained  at  tempera- 
tures near  24°  C.  from  animals  that  were 
not  post-absorptive,  gave  oxygen  con- 
sumptions of  3.4-3.7  cc  02/gm/hr.  Pear- 
son's measurements,  as  might  be  expect- 
ed from  the  fact  that  he  was  not  using 
post-absorptive  animals,  are  higher  than 
our  determinations  of  2.7  cc  02/gm/hr 
at  25°  C. 

Hibernation  and  estivation. — No  infor- 


198 


180 


GEORGE  A.  BARTHOLOMEW  AND  RICHARD  E.  MacMILLEN 


mation  on  hibernation  or  estivation  is 
available  for  Microdipodops.  Hall  (1946, 
p.  386)  pointed  out  that  kangaroo  mice 
are  often  active  above  ground  in  temper- 
atures many  degrees  below  freezing,  and 
Ingles  (1954,  p.  214)  suggested  that 
kangaroo  mice  probably  do  not  hiber- 
nate. 

Under  laboratory  conditions  we  found 
that  kangaroo  mice   at  any  time  of  year 


40  r 


there  are  no  conspicuous  physiological 
differences  between  arousal  from  spon- 
taneous dormancy  and  that  from  induced 
dormancy. 

Animals  dormant  at  room  tempera- 
tures (estivating)  started  to  arouse  im- 
mediately upon  being  handled.  The  rate 
of  increase  in  Tb  varied  but  usually  fell 
between  0.5°  and  0.8°  C.  per  minute. 
Usually  within  20  minutes  of  the  onset 


-.40 


10  20  30  40  50 

MINUTES     FROM     START     OF    AROUSAL 

Fig.  3. — Increases  in  oral  temperatures  in  nine  kangaroo  mice  during  arousal  from  torpor.  All  arousals 
took  place  in  ambient  temperatures  between  23°  and  26°  C.  Temperatures  taken  manually  with  thermo- 
couples. The  five  upper  animals  were  dormant  at  room  temperature  (22°-25°  C);  the  four  lower  animals 
were  dormant  at  5°-8°  C. 


will  spontaneously  become  dormant  at 
ambient  temperatures  ranging  at  least 
from  5°  to  26°  C.  and  can  readily  be  in- 
duced to  hibernate  (or  estivate)  over  this 
range  of  temperatures  by  reduction  of 
food  for  24  hours  or  less. 

Body  temperature  and  behavior  dur- 
ing entry  into  torpor  were  not  recorded, 
but  the  animals  apparently  entered  tor- 
por in  the  crouching  posture  normally 
used  in  sleeping.  Dormant  animals  had 
body  temperatures  l°-2°  C.  above  am- 
bient. Judging  from  the  course  of  body 
temperature  during  arousal  from  torpor, 


of  arousal  the  animals  attained  their  nor- 
mal operating  temperature,  and  within 
as  little  as  12-15  minutes  from  the  start 
of  arousal  they  appeared  to  behave  nor- 
mally, even  though  Tb  approximated 
30°  C.  Arousal  from  low  temperatures 
was  essentially  the  same  as  arousal  from 
high  temperatures  (Fig.  3).  However, 
animals  arousing  from  low  temperatures 
attained  maximal  body  temperatures 
about  1°  C.  higher  than  did  those  arous- 
ing from  room  temperature. 

Incidental  to  the  measurement  of  Tb 
the  relations  of  various  types  of  behavior 


199 


THERMOREGULATION  IN  THE  KANGAROO  MOUSE                       181 

to  body  temperature  were  noted  during  mals  the  ability  to  become  dormant  and 

nine  arousals.   Mice  unsuccessfully  at-  to  decrease  body  temperature  and  meta- 

tempted  to  right  themselves  when  turned  bolic  activity  may  be  more  useful  in  the 

over  at  Tb  between  16.1°  and  18.2°  C.  summer  than  in  the  winter,  and  it  may 

and  successfully  righted  themselves  at  be  as  important  for  water  conservation 

Tb  between  19.0°  and  22.0°  C.  The  first  as  for  energy  conservation, 

vocalizations  were  given  at  Tb  between  Kangaroo    mice    are    unique    among 

24.7°  and  28.6°  C.  Grain  was  available  heteromyids  in  having  conspicuous  de- 

to  the  animals  during  arousal,  and  seven  posits  of  adipose  tissue  in  the  proximal 

of  the  nine  animals  ate  during  arousal,  third  of  the  tail,  which  is  considerably 

The  lowest  Tb  for  eating  was  25.5°  C,  larger  than  either  its  base  or  its  distal 

and  three  animals  ate  at  temperatures  half.  Hall  (1946,  p.  379)  suggests  that  the 

between  25°  and  29.4°  C.  The  mean  Tb  fleshiness  of  the  tail  permits  it  to  func- 

for  onset  of  visible  shivering  for  seven  tion  in  balancing.  However,  since  these 

animals  was  25.5°  C.  Two  of  the  nine  mice  hibernate  but  do  not  show  conspicu- 

animals  observed  did  not  visibly  shiver  ous  seasonal  deposits  of  subcutaneous  fat 

during  arousal.  Shivering  usually  stopped  over  the  body  as  a  whole,  it  seems  reason- 

at  a  Tb  of  34°-35°  C .  able  to  suggest  that  the  fat  tail  serves  as 

a  reserve  of  energy  for  use  during  periods 

DISCUSSION  q£  torpor.  In  the  laboratory  with  food 

The  general  features  of  thermoregula-  available  in  excess,  many  of  the  kangaroo 

tionin Microdipodops pallidus dirtsirmlzr  mice  showed  a  marked  increase  in  tail 

to  those  of  the  related  genus  Perognathus  diameter. 

in  that  both  show  well-developed  pat-  Our  data  (Fig.  1)  show  almost  no  in- 
terns of  hibernation  and  estivation,  es-  dication  of  a  discrete  zone  of  thermal 
sentially  normal  behavior  at  Tb  below  neutrality  for  the  kangaroo  mouse.  Its 
35°  C,  obligate  hyperthermia  at  Ta  critical  temperature  is  unusually  high  for 
above  35°  C,  and  no  apparent  salivary  an  animal  living  in  an  area  characterized 
response  to  elevated  body  temperature,  by  cold  winters.  For  months  on  end  kan- 
Microdipodops  differs  from  the  related  garoo  mice  can  be  active  only  at  tempera- 
genus  Dipodomys  in  that  the  latter  does  tures  below  thermal  neutrality.  Presum- 
not  readily  become  dormant  at  either  ably,  their  energetic  and  thermal  prob- 
high  or  low  temperatures  and  does  use  lems  are  reduced  in  cold  weather  by  pe- 
salivation  as  an  emergency  thermoregu-  riodic  episodes  of  torpor.  It  is  of  interest 
latory  response  (Schmidt-Nielsen  and  that  we  captured  our  animals  on  nights 
Schmidt-Nielsen,  1952).  when  environmental  temperatures  went 

In  kangaroo  mice,  as  in  Perognathus  below  —10°  C,  and  Hall  (1946,  p.  396) 

longimemhris  (Bartholomew  and  Cade,  reports  that  these  animals  are  often  "ac- 

1957)  and  Citellus  mohavensis  (Bartholo-  tive  on  nights  when  the  temperature  is  so 

mew  and  Hudson,  I960-),  there  appears  to  low  as  to  freeze  to  a  state  of  stiffness  the 

be  no  sharp  physiological  differentiation  bodies  of  mice  caught  in  traps."  Thus,  al- 

between  hibernation  and  estivation.  This  though    they  can   hibernate,    they   are 

underscores  the  point  that  the  faculta-  also  commonly  active  during  subfreezing 

tive  hypothermia    shown  by  mammals  weather. 

should  not  be  thought  of  only  as  an  adap-  This  species  has  remarkably  shallow 

tive  response  to  low  environmental  tem-  burrows,  often  no  deeper  than  4  inches 

peratures;  at  least  for  small  desert  mam-  (Hall,  1946,  p.  396).  Consequently,  when 


200 


182  GEORGE  A.  BARTHOLOMEW  AND  RICHARD  E.  MacMILLEN 

high  daytime  temperatures  occur,  at  in  Microdipodops  correlates  nicely  with 
least  some  members  of  the  population  its  strong  tendency  toward  hyperthermia 
may  be  exposed  to  temperatures  near  at  high  ambient  temperatures.  For  ani- 
35°  C.  It  is  possible,  therefore,  that  the  mals  living  in  a  desert  environment 
high  point  of  thermal  neutrality  of  this  where  water  is  usually  in  short  supply, 
species  allows  a  significant  metabolic  hyperthermia  is  a  more  advantageous  re- 
economy  and  a  significant  reduction  in  sponse  to  heat  than  is  evaporative  cool- 
pulmocutaneous  water  loss  during  the  ing. 
severely  hot  desert  summers.  summary 

Extrapolation  of  the  plot  of  metabo-  Microdipodops  pallidus  occurs  only  on 
lism  against  ambient  temperature  below  gp^^g^iy  vegetated  sand  dunes  in  the 
thermal  neutrality  does  not  intersect  the  ^^^^^^   ^^^^^   ^^   western    Nevada   and 
abscissa  within  the  usual  range  of  body  ^^^^^^^   California.    In   the   absence  of 
temperature    (38°-39°C.)    of    kangaroo  ^-gj^pei-ature   stress   body   temperature, 
mice  (Fig.  2).  This  means  that,  unlike  j^  averages  38.8°C.  There  is  no  diminu- 
some  of  the  species  considered  by  Scho-  ^j^^  ^^  j.^  ^^-^^^  decreasing  ambient  tem- 
lander   et   al.    (1950),    and    unlike    the  perature,  T^,  at  least  to  8°  C.  However, 
masked  shrew,  Sorex  cinereus  (Morrison,  hyperthermia  is  apparent   at  a   Ta  of 
Ryser,  and  Dawe,  1959),  the  kangaroo  350  ^  ^^^  ^^  390  ^  j^^  averages  40.5°  C. 
mouse  does  not  follow  Newton's  empiri-  E^pos^re  for  more  than  a  few  hours  to 
cal  law  of  cooling  in  a  simple  and  direct  390  ^    j^  ^^^^^  lethal.  At  high  ambient 
manner.  The  failure  to  follow  the  pattern  temperatures    kangaroo    mice    neither 
predicted  by  Newton's  law  of  cooling  p^^^  ^^^  ^^^^^  ^j^^y  ^^^^  no  clearly  de- 
may  be  related  to  the  fact  that  kangaroo  ^^^^  ^^^^  ^f  thermal  neutrality;  oxygen 
mice  start  to  become  hyperthermic  as  consumption  is  minimal  at  35°  C.  and  in- 
they  approach  their  critical  temperature  ^^^^^^^   ^lore   rapidly   at   temperatures 
(Fig.  1),  and  it  suggests  that  the  relation  ^^^^^  ^^^^  ^^-^^^  ^^^^  ^^i^^  it.  Basal 
between  skin  and  ambient  temperature  ^letabolism  is  25  per  cent  less  than  that 
in  this  species  differs  from  the  usual  pat-  pj-g^i^ted  on  the  basis  of  body  size.  Kan- 
tern.  It  is  of  interest  that  Pearson's  data  ^^^^^  ^^^^  ^^^  capable  of  both  estivation 
(1960)  for  Reithrodontomys  show  a  situa-  ^^^  hibernation.  In  the  laboratory  they 
tion  similar  to  that  reported  here  for  ^^^^^  become  dormant  at  ambient  tem- 
Microc^z>(^o^5,  that  is,  almost  no  zone  of  pg^atures  ranging  at  least  from  5°  to 
thermal  neutrality,  a  high  critical  tem-  25°  c.  The  rate  of  temperature  increase 
perature,  and  a  failure  of  the  curve  of  ^^^j^^g  arousal  at  room  temperature  is 
metabolism  against  ambient  temperature  0  5o__0.8°C.  per  minute.  Terminal  body 
to  intersect  the  abscissa  at  the  usual  body  temperatures  after  arousal  from  low  tem- 
temperature.  Although  Pearson  does  not  pej-^tures  averaged  about   1°  C.  higher 
comment  on  this  point,  it  appears  that  in  ^^iQ^n  after  arousal  from  room  tempera- 
Reithrodontomys  as  in  Microdipodops  the  ^^^.g  gy  ^^g  time  the  Tb  of  arousing  ani- 
curve   of   metabolism   against   ambient  ^lals  reaches  30°  C,  their  behavior  ap- 
temperature  intersects  the  abscissa  at  a  pears  normal.  The  thermoregulatory  re- 
point  above  the  lethal  temperature  for  sponses  of  kangaroo  mice  are  compared 
the  species.  with  those  of  other  desert  heteromyids. 
The  apparent  absence  of  a  marked  in-  and  the  ecological  significance  of  their 
crease  in  salivation  at  high  temperatures  physiological  capacities  is  discussed. 


201 


THERMOREGULATION  IN  THE  KANGAROO  MOUSE 


183 


LITERATURE  CITED 


Bartholomew,  G.  A.,  and  Cade,  T.  J.  1957.  Tem- 
perature regulation,  hibernation,  and  aestivation 
in  the  Uttle  pocket  mouse,  Perognatlms  longimem- 
bris.  Jour.  Mamm.,  38:60-72. 

Bartholomew,  G.  A.,  and  Hudson,  J.  W.  1960. 
Aestivation  in  the  Mohave  ground  squirrel,  Citel- 
lus  mohavensis.  Bull.  Mus.  Comp.  Zool.,  124:193- 
208. 

Brody,  S.  1945.  Bioenergetics  and  growth.  New 
York:  Reinhold  Publishing  Co. 

Dawson,  W.  R.  1955.  The  relation  of  oxygen  con- 
sumption to  temperature  in  desert  rodents.  Jour. 
Mamm.,  36:543-53. 

Ingles,  L.  G.  1954.  Mammals  of  California  and  its 
coastal  waters.  Stanford,  Calif.:  Stanford  Univer- 
sity Press. 

Hall,  E.  R.  1946.  Mammals  of  Nevada.  Berkeley: 
University  California  Press. 

Hall,  E.  R.,  and  Linsdale,  J.  M.  1929.  Notes  on 
the  life  history  of  the  kangaroo  mouse  {Microdi- 


podops).  Jour.  Mamm.,  10:298-305. 

Lyman,  C.  P.,  and  Chatfield,  P.  0.  1955.  Physiol- 
ogy of  hibernation  in  mammals.  Physiol.  Rev., 
35:403-25. 

Morrison,  P.,  Ryser,  F.  A.,  and  Dawe,  A.  R.  1959. 
Studies  on  the  physiology  of  the  masked  shrew 
Sorex  cinereus.  Physiol.  Zool.,  32:256-71. 

Pearson,  0.  P.  1948.  Metabolism  of  small  mam- 
mals, with  remarks  on  the  lower  limit  of  mam- 
malian size.  Science,  108:44. 

.  1960.  The  oxygen  consumption  and  bio- 
energetics of  harvest  mice.  Physiol.  Zool.,  33: 
152-60. 

Schmidt-Nielsen,  K.,  and  Schmidt-Nielsen,  B. 
1952.  Water  metabolism  of  desert  mammals. 
Physiol.  Rev.,  32:135-66. 

Scholander,  p.  F.,  Hock,  R.,  Walters,  V.,  John- 
son, F.,  and  Irving,  L.  1950.  Heat  regulation  in 
some  arctic  and  tropical  mammals  and  birds. 
Biol.  Bull.,  99:237-58. 


Reprinted  for  private  circulation  from 
PHYSIOLOGICAL  ZOOLOGY 

Vol.  XXXIV,  No.  3,  July  1961 
Copyright  1961  by  the  University  of  Chicago 

PRINTED   IN   U.S.A. 


202 


Counter-Current  Vascular  Heat  Exchange  in  the  Fins  of  Whales^ 


p.  F.  SCHOLANDER  and  WILLIAM   E.  SCHEVILL.  From  the  Woods  Hole 
Oceanographic  Instilution,  Woods  Hole,  Afassaclmsetts 


IT  MAY  BE  a  source  of  wonder  that  whales 
swimming  about  in  the  icy  waters  of  the 
polar  seas  can  maintain  a  normal  mam- 
malian body  temperature.  What  prevents 
them  from  being  chilled  to  death  from  heat  loss 
through  their  large  thin  fins?-  These  are  well 
enough  vascularized  to  justify  the  question 
(fig.  i).  One  may  conjecture  that  a  whale  may 
be  so  well  insulated  by  its  blubber  that  it  needs 
such  large  surfaces  to  dissipate  its  heat.  On  the 
other  hand,  if  heat  conservation  is  at  a  pre- 
mium, there  must  be  some  mechanism  whereby 
the  fins  can  be  circulated  without  losing  much 
heat  to  the  water.  One  may  point  to  two 
circulatory  factors  which  would  reduce  the  heat 
loss  from  the  fin:  a)  slow  rate  of  blood  flow 
and,  6)  precooling  of  the  arterial  blood  by  veins 
before  it  enters  the  fin. 

Bazett  and  his  coworkers  (i)  found  that  in 
man  the  brachial  artery  could  lose  as  much  as 
3°C/decimeter  to  the  two  venae  comitantes. 
This  simple  counter-current  exchange  system 
is  a  mere  rudiment  compared  to  the  multi- 
channelled  arteriovenous  blood  vascular  bun- 
dles which  we  find  at  the  base  of  the  extremities 
in  a  variety  of  aquatic  and  terrestrial  mammals 
and  birds.  These  long  recognized  structures 
have  most  recently  been  studied  by  Wislocki 
(2),  Wislocki  and  Straus  (3)  and  Fawcett  (4). 

The  function  of  these  bundles  has  long  been 
a  mystery.  No  matter  what  else  they  do,  they 
must  exchange  heat  between  the  arteries  and 
veins,  and  it  has  been  pointed  out  that  they 
very  likely  play  an  important  role  in  the  pres- 
ervation and  regulation  of  the  body  heat  of 
many  mammals  and  birds  (5). 

In  the  present  study  we  describe  a  conspic- 
uous arteriovenous  counter-current  system  in 
the  fins  and  flukes  of  whales,  which  we  interpret 
as  organs  for  heat  preservation. 

Received  for  publication  July  21,  1955. 

'  Contribution  Number  807  from  the  Woods  Hole 
Oceanographic  Institution. 

^  In  'fin'  we  include  the  structures  more  specifically 
called  flippers  (pectoral  fins),  flukes  (caudal  fins)  and 
dorsal  fin. 


MATERIAL 

Two  species  of  porpoises  have  been  studied :  Lageno- 
rliynclius  aculits:  dorsal  fin,  tail-fluke,  and  flipper  of 
an  adult  female  collected  50  miles  east  of  Cape  Cod; 
Tursiops  tnmcatus:  dorsal  fin  and  tail-fluke  of  a  4- 
month-old  calf  from  Florida,  supplied  through  the 
courtesy  of  the  Marineland  Research  Laboratory. 

Lagenorhynchiis  is  a  genus  of  fairly  high  latitudes, 
the  southern  limit  of  L.  acutns  being  about  latitude 
4i°N.  on  the  New  England  coast  and  about  55°N.  in 
the  British  Isles.  It  has  been  caught  at  least  as  far 
north  as  latitude  64°N.  in  west  Greenland  and  Nor- 
wegian waters.  Tursiops  is  found  in  lower  latitudes, 
T.  truncalus  overlapping  slightly  with  L.  aciihts  and 
occurring  south  into  the  tropics. 

DESCRIPTION 

Figure  2  illustrates  the  vascular  supply  at 
the  base  of  the  dorsal,  pectoral  and  caudal  fins. 
It  may  be  seen  that  all  major  arteries  are 
located  centrally  within  a  trabeculate  venous 
channel.  This  results  in  two  concentric  con- 
duits, with  the  warm  one  inside.  In  addition 
to  the  circumarterial  venous  channels  there  are 
separate  superficial  veins,  as  seen  in  figure  2. 
The  circumarterial  venous  channels  are  con- 
spicuously thin  walled  compared  to  the  simple 
veins,  as  may  be  seen  in  figure  3.  When  an 
artery  was  perfused  with  saline,  the  solution 
returned  through  both  of  these  venous  systems. 

INTERPRETATION 

Based  on  the  anatomical  findings  and  on  the 
perfusion  experiments,  we  interpret  the  artery- 
within-vein  arrangement  as  a  heat-conserving 
counter-current  system,  as  schematically  pre- 
sented in  fig.  4.  In  such  an  arrangement  the 
warm  arterial  blood  is  cooled  by  the  venous 
blood  which  has  been  chilled  in  the  fin.  The 
result  is  a  steep  proximodistal  temperature 
drop  from  the  body  into  the  appendage.  The 
heat  of  the  arterial  blood  does  not  reach  the 
fin,  but  is  short-circuited  back  into  the  body  in 
the  venous  system.  Body  heat  is  therefore 
conserved  at  the  expense  of  keeping  the  appen- 
dage cold.  There  is  reason  to  believe  that  the 
analogous  blood  vascular  bundle  in  the  proxi- 


279 


203 


28o 


p.  F.  SCHOLANDER  AND  WILLIAM  E.  SCHEVILL 


Volume  S 


Fig.  I.  Arterial  supply  to  the  flukes  in  the  common 
porpoise  {Plincoena  phocnena),  drawn  from  an  x-ray 
l^icture  by  Braun  (6). 

mal  part  of  the  extremities  of  sloths  serves  a 
similar  function,  inasmuch  as  these  animals 
can  barely  keep  warm  even  in  their  warm 
environment  (5).  Cold  extremities  have  been 
described  in  many  arctic  mammals  and  birds 
as  important  factors  for  conservation  of  body 
heat  (7),  but  to  what  extent  arteriovenous 
counter-current  structures  are  present  in  these 
animals  is  not  known. 

The  efficiency  of  heat  exchange  in  a  system 
like  that  diagrammed  in  figure  4  is  related  to 
the  blood  flow.  The  slower  the  flow,  the  more 
nearly  identical  will  be  the  arterial  and  venous 
temperatures  along  the  system,  and  the  more 
efficient  will  be  the  heat  conservation.  At  high 
rates  of  flow,  warm  blood  will  reach  the  periph- 


ery and  cool  venous  blood  will  penetrate  into 
the  body.'' 

It  was  shown  by  perfusion  experiments  on 
the  detached  fins  that  the  arterial  blood  may 
return  via  the  concentric  veins,  and/or  through 
the  separate  superficial  veins.  As  pointed  out 
above,  the  concentric  vein  channels  are  very 
thin  walled  and  weak  compared  to  the  thick- 
walled  superficial  veins  (fig.  3).  One  may  inter- 
pret these  anatomical  facts  in  the  following 
way.  If  the  animal  needs  maximal  heat  con- 
servation, blood  circulation  through  the  fins 
should  be  slow,  and  the  venous  return  should 
preferentially  take  place  through  the  counter- 
current  veins.  But  a  slow  rate  of  blood  flow 
would  need  only  weak  venous  walls,  as  actually 
found.  If,  on  the  other  hand,  the  animal  needed 
maximal  cooling,  as  during  exercise  in  rela- 
tively warm  water,  this  would  be  most  effec- 
tively accomplished  by  a  high  rate  of  blood 
flow  through  the  fins,  with  venous  return 
through  the  superficial  veins  and  the  least 
possible  flow  through  the  concentric  veins. 
This  would  require  the  strong  and  thick  walls 
of  the  superficial  veins.  One  may  even  see  the 
likelihood  of  a  semiautomatic  regulatory  func- 
tion in  the  concentric  system,  for  when  the 
artery  is  swelled  by  increased  blood  flow,  the 
concentric  veins  will  be  more  or  less  obliterated, 


^  The  theory  for  a  multichannel  counter-current 
system  has  been  elaborated  in  connection  with  the 
swimbladder  in  deep  sea  fishes  (8). 


L.  CAUDAL 

„I1„„IIU.  .1  iv  II,,..  |i»i 


DORSAL 


r— 1 >— I 1 1 

O    CEMTIMETERS  .S 


TUR5I0P5     TRUhCflTUS 


L.PECTORflL 


mmumasssiiiiMsamm 


LAGEMORHYMCHU^    AOUTUS 


Fig.  2.  Sections  near  base  of 
fins  and  flukes  of  two  species  of 
jiorpoises.  Each  artery  is  sur- 
rounded by  a  multiple  venous 
channel.  Simple  veins  are  near  the 
skin  (only  the  larger  ones  are  indi- 
cated). 


204 


COUNTER-CURRENT  HEAT  EXCHANGE  IN  W  HAEE  FINS 


281 


Fig.  3.  Sections  from  Tursiops  Inincatus.  (Courtesy  of  the  Department  of  Anatomy.  Harvard  Medical  School.) 
A.  From  tail-fluke.  Upper:  artery  surrounded  by  thin-walled  venous  channels.  Lower:  superficial  single  thick- 
walled  vein  in  the  hypodermis.  (X  9)  B.  From  dorsal  fin.  Artery  surrounded  hy  thin-walled  venous  channels  (X  12) 


but  will  remain  open  when  the  diameter  of  the 
artery  is  reduced  during  decreased  blood  flow. 
Thus  the  anatomical  findings  fit  logically  into 
the  simplest  possible  scheme  of  heat  regulation 
in  the  fins. 

There  are  a  few  observations  available  in- 
dicative of  heat  regulation  in  the  fins  of  por- 
poises. Tomilin  (g)  made  some  observations 
on  an  east  Siberian  'white-sided  dolphin'  on 
deck,  and  found  that  the  fins  could  vary  be- 
tween 25°  and  33. 5°C,  while  the  body  varied 
only  0.5°.  Schevill  observ^ed  that  the  flukes  in 
a  Florida  Tursiops  out  of  water  became  about 
10°  warmer  than  the  body  surface  itself.  In 
both  of  these  cases  the  animals  were  probably 
resisting  overheating.  On  the  other  hand, 
Scholander  (5)  has  recorded  cold  flippers  in 
water-borne  common  porpoises  (Phocoena). 

The  concentric  counter-current  system  of 
an  artery  within  a  vein  appears  to  be  a  pecu- 
liarly cetacean  arrangement,  and  we  have  seen 
it  only  in  the  fins,  flippers  and  flukes  of  these 
animals."*  This  is  an  impressive  example  of 
bioengineering,    which,    together    with    other 


TRUNK 


29" 


39° 


h;^////>//,',7/]///////////^/////////^;//7777. 
ARTERY-«4-iO°  20°  30°  40°    -- 


■*  The  present  material  is  from  odontocetes,  Ijut 
these  structures  have  also  been  noted  by  Scholander 
in  the  tail  flukes  of  a  mysticete  (fin  whale). 


>:::^  TRUNK 


Fig.  4.  Schematic  diagram  of  hj^iothetical  tempera- 
ture gradients  in  a  concentric  counter-current  system. 

factors,  adapts  these  homeotherms  for  a  suc- 
cessful existence  in  a  heat-hungry  environment. 

SUMM.'^RY 

The  vascular  supply  to  the  fins  and  flukes 
of  two  species  of  porpoises,  Lagenorhynchus 
aciitus  and  Tursiops  truncalus,  is  described. 
All  major  arteries  entering  the  fins  and  flukes 


205 


282 


1'.  F.  SCHOLANDER  AND  WILLIAM  E.  SCHEVILL 


Volintie  8 


are  surrounded  by  a  trabeculate  venous  chan- 
nel. The  arteries  drain  into  these,  but  also  into 
superlicial  simple  veins.  The  artery  within  the 
venous  channel  is  interpreted  as  a  heat-con- 
serving counter-current  exchange  system.  The 
heat  regulatory  aspects  of  the  two  venous 
systems  are  discussed. 

We  wish  to  express  our  appreciation  to  Dr.  F.  G. 
Wood,  Jr.,  and  the  Marineland  Research  Laboratory, 
Marineland,  Fla.,  for  providing  the  material  of  Tur- 
siops  tnmcatus,  and  to  Dr.  G.  B.  Wislocki  of  the  Dept. 
of  Anatomy,  Harvard  Medical  School,  Boston,  Mass., 
for  providing  the  histological  sections  and  photographs. 


REFERENCES 

1.  B.\ZETT,  H.  C,  L.  Love,  M.  Newton,  L.  Eisen- 
BERG,  R.  Day  and  R.  Forster  II.  J.  Appl. 
Pliysiol.  1 :  3,  1948. 

2.  Wislocki,  G.  B.  /.  Morpliol.  46:  317,  1928. 

3.  Wislocki,  G.  B.  and  W.  L.  Straus,  Jr.  Ball.  Mus. 
Comp.  Zool.  Harvard  74:  i,  1933. 

4.  Fawcett,  D.  W.  J  Morphol.  71:  105,  1942. 

5.  ScHOLANDER,  P.  F.  Evolution  9:  15,  1955. 

6.  Braun,  M.  Zool.  Anz.  29:  145-149,  1905. 

7.  Irving,  L.  and  J.  Krog.  J.  Appl.  Pliysiol.  7:  355, 

1955- 

8.  Scholander,  p.  F.  Biol.  Bull.  107:  260,  1954. 

9.  ToMiLiN,  A.  G.  Rybnoe  Khozaistvo  26:  50,  1950.  (In 

Russian.) 


206 


SECTION  3— REPRODUCTION  AND  DEVELOPMENT 

Just  as  animal  structures  must  be  adaptive,  so  must  reproductive  and  devel- 
opmental patterns.  In  other  words,  the  organism  must  be  a  functioning  unit  in 
its  particular  environment  at  all  times.  In  our  selections,  Spencer  and  Steinhoff 
discuss  the  possible  functional  significance  of  geographic  variation  in  litter 
size,  and  Sharman  points  out  the  adaptive  value  of  some  peculiarities  of  kan- 
garoo reproduction.  The  interrelationships  of  reproductive  and  developmental 
patterns  in  the  fisher  are  evident  in  the  account  by  Wright  and  Coulter.  Super- 
fetation  ( or  the  fertilization  of  new  ova  during  gestation,  known  in  kangaroos, 
rabbits,  and  some  rodents),  delayed  implantation  (which  occurs  in  some 
mustelids),  and  delayed  fertilization  (through  sperm  storage,  known  in  some 
bats)  all  are  interesting  variations  of  the  reproductive  theme,  and  all  are 
adaptive  in  certain  circumstances.  A  recent  study  of  reproductive  adaptations 
of  the  red  tree  mouse  by  Hamilton  ( 1962,  not  reprinted  here )  related  small 
litters,  long  gestation,  delayed  implantation  during  lactation,  and  slow  develop- 
ment of  young  with  the  limited  amount  of  energy  available  in  the  food  sources 
of  the  mice.  The  study  here  reproduced  by  Jones  on  the  evening  bat  relates 
development  to  function,  in  this  case  flight,  and  also  nicely  illustrates  some 
quantitative  refinements  that  adequate  data  provide. 

The  student  of  any  field  is  well  advised  to  learn  what  compilations,  summa- 
ries, or  collected  works  are  available.  Sometimes  a  summary  is  short,  as  is  the 
paper  by  Hamilton  included  herein  on  reproductive  rates  of  some  small  mam- 
mals. In  the  field  of  mammalian  reproduction,  the  classic  summary  by  Asdell 
(as  revised  in  1964),  and  recent  collections  of  contributions  edited  by  Enders 
( 1963)  on  delayed  implantation  and  by  Rowlands  ( 1966)  on  comparative  biol- 
ogy of  mammalian  reproduction  will  repay  study. 

Two  classic  books  in  the  field  of  development  in  which  relative  growth 
rates  were  considered  at  length  are  On  Growth  and  Form  by  D'Arcy  Went- 
worth  Thompson  (1942)  and  Problems  of  Relative  Growth  by  Julian  Huxley 
( 1932 ) .  A  comparative  study  of  two  related  species  ( Butterworth  on  Dipod- 
omys)  is  included  here.  A  recent  and  detailed  account  (too  long  to  include 
here)  of  one  species  in  terms  of  relative  growth  and  in  comparison  to  several 
other  species  is  the  study  by  Lyne  and  Verhagen  ( 1957 )  on  Trichosurus  vul- 
pecula,  an  Australian  brush-tailed  possum. 

A  number  of  studies  of  single  species  may  be  found  in  the  literature.  Allen's 
paper  (reprinted  here)  is  of  interest  because  it  is  one  of  the  earliest  to  give 
serious  consideration  to  variation  as  such  and  to  possible  relevance  of  variation 
to  systematic  and  other  problems.  Hall  (1926)  described  at  greater  length 
than  could  be  included  here  and  in  detail  uncommon  at  that  time  the  changes 
during  growth  of  the  skull  in  the  CaHfornia  ground  squirrel.  Two  among  the 
many  good  recent  studies  of  development  of  single  species  are  by  Layne  ( 1960, 
1966)  on  Ochrotomys  nuttalli  and  Peromyscus  floridanus. 

Although  we  have  not  included  examples  of  methods  of  determining  age 
other  than  the  report  of  Wright  and  Coulter  on  the  fisher,  we  must  comment 
that  age  determination  is  important  in  many  practical  problems  of  wildlife 
management  as  well  as  in  studies  of  population  composition  or  of  growth  as 


207 


such.  Managers  of  deer  herds,  for  example,  can  examine  the  teeth  of  hunter- 
killed  animals  using  standards  developed  by  Severinghaus  (1949)  and  later 
workers.  The  formation  of  annuli  in  dental  cement  in  various  kinds  of  mam- 
mals provides  another  method  for  determining  age — see  Adams  and  Watkins 
(1967)  on  its  application  to  ground  squirrels.  Epiphyseal  growth  as  observed 
in  X-ray  photographs  and  the  use  of  lens  weights  are  other  means  ( see  Wight 
and  Conaway,  1962,  on  aging  cottontails ) . 

A  short  paper  on  maturational  and  seasonal  molt  in  the  golden  mouse  con- 
cludes our  selection  for  this  section.  Studies  of  molt  in  furbearers  are,  of 
course,  of  special  economic  import,  and  knowledge  of  pelage  differences  related 
to  age,  sex,  or  season  are  of  obvious  use  in  most  studies  of  mammalian  popula- 
tions. 


208 


THE    REPRODUCTIVE    RATES    OF    SOME    SMALL    MAMMALS 

By  W.  J.  Hamilton,  Jr. 

Students  of  cyclic  mammal  populations  realize  the  necessity  of  properly  evaluat- 
ing the  breeding  rate.  A  proper  assessment  of  the  reproductive  rate  is  frequently 
essential  for  a  correct  interpretation  of  population  levels.  Without  a  satisfactory' 
estimate  of  breeding  rate,  conclusions  regarding  cyclic  populations  may  be  in- 
valid. Unfortunately,  it  is  difl&cult  to  secure  accurate  data  on  the  breeding  rate 
in  feral  species;  analogous  observations  on  captive  species  may  not  give  a  true 
picture  of  the  breeding  behavior  in  wild  species.  Many  field  investigators  be- 
lieve that  small  mammals  have  successive  litters,  one  following  another  in  rapid 
succession  during  the  height  of  the  breeding  season.  On  the  other  hand,  there 
are  those  who  argue  that  a  post-partus  oestrus  in  wild  species  seldom  occurs. 
They  insist  that  mating  during  the  lactation  period  is  rare  under  natural  condi- 
tions; captive  individuals  alone  exhibit  this  phenomenon  due  to  crowding  or  other 
factors  imposed  by  laboratory  conditions.  Since  the  subject  is  an  important  one 
in  population  studies,  I  present  such  data  as  are  available  to  demonstrate  that 
certain  shrews,  mice,  and  other  small  mammals  are  not  only  capable,  but  do  mate 
successfully  following  partus.  Actively  lactating  species  are  upon  occasion 
gravid. 


209 


258  JOURNAL  OF  MAMMALOGY  Vol.  SO,  No.  S 

In  an  important  paper  on  discontinuous  development  in  mammals,  Hamlett 
(1935)  remarks  that  in  a  fairly  extensive  series  of  mice  of  various  kinds,  including 
free  living  house  mice,  Norway  rats,  and  wild  species  of  deer  mice  and  field  mice, 
pregnant  suckling  females  were  never  found.  He  concludes  that  copulation  im- 
mediately after  parturition  in  mice  is  a  response  to  domestication,  and  is  rare  or 
lacking  in  free  living  races.  Pearson  (1944)  examined  early  pregnant  females  of 
Blarina  in  which  placental  scars  were  visible  and  the  manmiary  glands  greatly 
developed,  indicating  that  these  individuals  had  been  nursing  young  recently. 
He  suggests  the  possibility  that  the  young  may  have  been  lost  or  destroyed  a 
short  time  before,  and  that  mating  took  place  after  the  loss  of  the  young.  Pear- 
son believes  that  shrews  with  advanced  mammary  development  merely  indicate 
that  it  is  possible  for  Blarina  to  produce  more  than  one  litter,  but  his  data  do  not 
prove  that  there  is  a  true  post-partum  oestrus.  He  concludes  that  true  post- 
partum mating  and  pregnancy  during  lactation  rarely,  if  ever,  occur  in  Blarina; 
remating  depends  upon  the  loss  of  a  litter. 

Several  investigators  have  demonstrated  a  post-partum  oestrus  in  captive 
cricetid  rodents.  Bailey  (1924)  observed  that  captive  meadow  voles,  Microtus  p. 
pennsylvanicus,  mated  immediately  following  parturition,  one  female  producing 
seventeen  litters  in  a  year.  The  gestation  of  this  species  is  twenty-one  days; 
lactation  does  not  lengthen  the  period.  Svihla  (1932)  reports  several  species  of 
captive  Pcromyscus  mating  shortly  after  parturition.  Practically  all  females  of 
the  European  wild  rabbit  (Oryctolagus  cuniculus)  under  natural  conditions  become 
pregnant  again  at  each  post-partum  oestrus  during  the  height  of  the  breeding 
season  (Brambell,  1943).  Elsewhere  (Hamilton,  1940),  I  have  shown  that  the 
cottontail,  Sylvilagus  floridanus  mearnsii,  presumably  has  a  post-partus  oestrus, 
for  actively  nursing  females  have  contained  embryos,  suggesting  that  mating 
occurs  shortly  following  parturition.  Vorhies  and  Taylor  (1940),  in  their  study 
of  the  white-throated  wood  rat,  Neotoma  albigula,  suggest  that  it  is  highly  prob- 
able that  this  species  produces  successive  litters  with  only  very  short  intervals. 
In  one  den  they  found  a  female  with  two  newly  bom  young  hanging  to  the  teats, 
with  three  half-grown  young  in  the  same  den.  This  presumptive  evidence  of 
rapid  succession  in  litters  is  nevertheless  suggestive. 

Obviously  with  the  species  discussed  above  there  is  a  post-partum  oestrus  at 
which  time  the  female  is  receptive  to  the  male.  It  appears  unlikely  that  the  im- 
position of  captivity  would  modify  the  reproductive  cycle  in  a  short  time.  The 
absolute  proof  of  such  should  be  studied  under  natural  conditions,  though  posi- 
tive data  are  rather  difficult  to  secure. 

A  feral  Norway  rat  will  cease  lactating  within  forty-eight  hours  after  the  loss  of 
a  litter.  Gentle  traction  on  the  teats  fails  to  produce  milk  following  this  period. 
Meadow  voles  usually  cease  to  lactate  a  day  after  the  young  are  removed.  The 
short-tailed  shrew,  Blarina  hrevicavda,  will  not  produce  a  flow  of  milk  in  a  similar 
length  of  time  if  the  nursing  young  be  destroyed.  Since  such  is  known  of  these 
three  species,  we  may  adduce  the  probability  of  pregnant  females  nursing  a  litter 
if  a  flow  of  milk  is  possible.  The  mammary  glands  and  teats  swell  noticeably  in 
many  mammals  shortly  before  parturition.     Interpretation  of  data  may  be  faulty 


210 


Aug.,  1949  HAMILTON— REPRODUCTIVE  RATES  259 

if  such  evidence  is  not  considered  with  care.  A  colustral  flow  is  evident  in  sev- 
eral cricetid  rodents  and  some  insectivores  shortly  before  parturition.  Inexperi- 
enced observers  may  mistake  this  secretion  for  milk  and  draw  faulty  conclusions. 
The  following  data  lend  support  to  the  assumption  that  some  small  mammals, 
under  natural  conditions,  successfully  mate  shortly  after  parturition  and  produce 
successive  litters  in  rapid  succession  during  part  of  the  breeding  season.  Unless 
otherwise  stated,  the  observations  below  relate  to  those  of  small  mammals  under 
conditions  in  the  vicinity  of  Ithaca,  New  York. 

Blarlna  brevicauda.  Short-tailed  shrew. — On  July  23,  1947,  E.  W.  Jameson,  Jr.  collected 
a  nursing  shrew.  Under  gentle  pressure,  milk  could  be  drawn  from  the  posterior  teats. 
This  shrew  had  four  embryos,  the  uterine  swellings  measured  10  mm.  in  greatest  width,  sug- 
gestive of  at  least  half-time  pregnancy.  A  week  later  I  trapped  a  nursing  Blarina  with  five 
11-mm.  embrj'os.  The  teats,  on  traction,  produced  milk.  A  Blarina  with  six  9-nim.  em- 
bryos was  taken  on  August  10,  1948.  The  teats  were  drawn  out  and  produced  milk  under 
gentle  traction.  In  my  field  notes  from  1926  to  1941  I  have  recorded  data  on  many  hundreds 
of  these  shrews,  and  noted  on  numerous  occasions  the  occurrence  of  lactating  gravid  females. 
I  have  always  considered  this  condition  a  perfectly  natural  one  in  shrews. 

Sorex  f.  fumeus.  Smoky  shrew. — Mating  may  follow  parturition  in  this  species  (Hamil- 
tion,  1940).  Actively  nursing  females  have  been  taken  which  contained  well-developed  em- 
bryos. Specimens  of  pregnant  Sorex  cinereus  have  likewise  been  collected  with  prominent 
mammary  glands  containing  an  abundance  of  milk. 

Peromyscus  leucopus  noveboracensls.  White-footed  mouse. — Many  hundreds  of  adult 
females  have  been  examined  during  the  breeding  season  over  a  twenty-year  period.  Many 
of  these  were  actively  nursing  and  contained  embryos  of  various  sizes.  Pregnant  nursing 
individuals  appear  more  frequently  in  May  and  June  collections.  It  is  possible  that  more 
lactating  individuals  were  gravid  than  my  notes  indicate,  since  early  pregnancy  cannot  be 
determined  by  macroscopic  examination. 

Oryzomys  palustrls.  Rice  rat. — This  is  a  prolific  species.  Field  data  obtained  in  Vir- 
ginia demonstrates  that  actively  nursing  females  are  occasionally  pregnant ;  there  is  evidence 
that  a  high  fertility,  resulting  in  vigorous  females  actually  producing  nine  litters  in  a  breed- 
ing season,  is  quite  possible.    The  females  are  capable  of  breeding  when  seven  weeks  old. 

Clethrionomys  gapperi.  Red-backed  vole. — On  October  10, 1941, 1  took  a  35-gram  nursing 
female  with  four  3-mm.  embryos  and  recent  placental  scars.  The  mammary  glands,  when 
dissected  out,  weighed  2.5  grams.  On  May  29,  1940,  a  nursing  individual  contained  five 
6-mm.  embryos.  Such  data  are  admittedly  fragmentary,  but  do  suggest  the  rapidity  of 
breeding  in  this  species.  Apparently  many  parous  animals  of  the  bank  vole,  Clethrionomys 
glareolus,  are  pregnant  and  lactating  simultaneously.  In  such,  pregnancies  are  prolonged 
by  lactation  causing  a  delay  in  implantation.  This  delay  results  in  the  blastocysts  remaining 
in  a  resting  state  in  the  uterine  lumen  for  a  considerable  period  (Brambell  and  Rowlands, 
1936). 

Microtus  pennsylvanlcus.  Meadow  vole. — The  reproductive  behavior  of  this  species  in 
the  wild  is  similar  to  that  of  captives.  Adult  females  give  birth  to  one  litter  after  another  in 
rapid  succession.  Data  on  this  high  fecundity  are  readily  obtainable  by  live  trapping. 
Females  approaching  full  term  are  readily  recognized ;  repeated  captures  of  specific  individ- 
uals indicate  that  in  some  instances  young  are  produced  at  three-week  intervals  over  a  period 
of  several  successive  months.  The  capture  of  numerous  wild  pregnant  females  with  nest- 
young  is  indubitable  proof  that  post-parous  mating  occurs  normally  from  early  spring  to  fall. 
I  have  obtained  many  records  of  such. 

Ondatra  zibethica.  Muskrat. — Arthur  C.  Cook  of  the  New  York  Conservation  Depart- 
ment informs  me  (personal  letter)  that  on  June  20,  1941,  he  dug  out  a  muskrat  den  at  How- 
lands'  Island,  Cayuga  County,  New  York.     From  the  den  he  recovered  a  pregnant  muskrat 


211 


260  JOURNAL  OF  MAMMALOGY  Vol.  SO,  No.  3 

with  two  litters  of  different  size.     In  captivity,  this  gravid  female  suckled  the  smaller  litter. 
This  is  presumptive  evidence  that  the  muskrat  may  mate  following  partus. 

Some  polyoestrous  rodents,  in  which  two  Htters  a  year  are  the  rule,  have  the 
Htters  widely  spaced.  Mating  normally  occurs  in  the  late  winter  and  midsum- 
mer. No  post-partum  oestrus  occurs.  Deanesly  and  Parkes  (1933)  indicate 
that  there  is  no  oestrus  immediately  after  parturition  or  during  lactation  in  the 
gray  squirrel,  Sciurus  caroUnensis.  A  similar  condition  obtains  with  Tamiasdu- 
rus,  Tamias,  and  Eutamias. 

Where  populations  of  small  mammals  are  sufficiently  large,  it  appears  prob- 
able that  fruitful  matings  often  occur  following  partus,  at  least  during  the  height 
of  the  breeding  season.  If  such  a  condition  be  generally  true,  it  enables  one  to 
compute,  in  a  measure,  the  probable  reproductive  rate.  One  may  thus  visualize 
the  annual  natural  increment  in  a  population  during  the  breeding  season.  Such 
data  are  most  useful  to  students  of  populations  and  animal  behavior. 

LITERATURE  CITED 

Bailey,  Vernon.     1924.     Breeding,  feeding,  and  other  life  habits  of  meadow  mice  (Micro- 

tus).    Journ.  Agr.  Research,  27:  523-536. 
Bbambell,  F.  W.  Rogers.     1943.    The  reproduction  of  the  wild  rabbit  Oryctolagua  cuni- 

culu8  (L.).     Proc.  Zool.  Soc.  London,  114:  1-45. 
Brambell,  F.  W.  R.,  and  I.  W.  Rowlands.     1936.     Reproduction  in  the  bank  vole  (Evo- 

tomys  glareolus  Schreber).     I.  The  oestrous  cycle  of  the  female.    Phil.  Trans. 

Royal  Soc.  London,  Series  B.,  No.  531,  226:  71-97. 
Deanesly,  Ruth,  and   A.  S.  Parkes.     1933.    3.  The  reproductive  process  of  certain 

mammals.     Part  4.  The  oestrous  cycle  of  the  grey  squirrel  {Sciurus  caroUnensis) 

Phil.  Trans.  Royal  Soc.  London,  B.  222:  47-78. 
Hamilton,  W.  J.,  Jr.     1940.     The  biology  of  the  smoky  shrew  {Sorex  Jumeus  fumeuiMiWQr) . 

Zoologica,  25(4) :  473-492. 
1940.     Breeding  habits  of  the  cottontail  rabbit  in  New  York  State.     Jour. 

Mamm.,  21:  8-11. 
Hamlett,  G.  W.  D.     1935.     Delayed  implantation  and  discontinuous  development  in  the 

mammals.     Quart.  Rev.  Biol.,  10:  432-447. 
Pearson,  Oliver  P.     1944.     Reproduction  in  the  shrew  (Blarina  brevicauda  Say).     Amer. 

Jour.     Anat.,  75:  39-93. 
SviHLA,  Arthur.     1932.     A  comparative  life  history  study  of  the  mice  of  the  genus  Pero- 

myscus.    Misc.  Publ.  Mus.  Zool.  Univ.  Michigan,  24:  1-39. 
VoRHiES,  Charles  T.,  and  Walter  P.  Taylor.     1940.     Life  history  and  ecology  of  the 

white-throated  wood  rat,  Neotoma  albigula  albigula  Hartley,  in  relation  to 

grazing  in  Arizona.     Univ.  Ariz.  Agr.  Exp.  Sta.  Tech.  Bull.,  86:  456-629. 

Cornell  University,  Ithaca,  New  York.    Received  October  4,  1948. 


212 


AN  EXPLANATION  OF  GEOGRAPHIC  VARIATION  IN  LITTER  SIZE 
Albekt  W.  SpexNCeh  and  Harold  W.  Steinhoff 

Absthact. — Our  explanation  of  the  latitudinal  and  altitudinal  variation  in  litter 
sizes  of  small  nianinials  invokes  the  effect  of  length  of  season  and  parental  mor- 
tality related  to  reproduction.  It  may  be  assumed  that  a  portion  of  the  maternal 
mortality  rate  varies  directly  as  the  size  of  litter  produced.  Short  seasons  limit 
the  maximum  number  of  times  a  female  can  reproduce  in  her  lifetime  and  give  an 
advantage  to  phenof\pes  producing  large  litters.  Long  seasons  favor  producers  of 
small  litters.  The  contribution  to  the  total  rate  of  increase  of  the  litters  produced 
in  the  additional  time  afforded  by  long  seasons  is  greater  for  producers  of  small 
litters  because  a  larger  proportion  of  parents  of  small  litters  survive  to  produce 
throughout  the  periods.  The  increment  provided  is  sufficient  to  overcome  the 
initial  advantage  of  parents  producing  large  numbers  of  young  in  their  first  litters. 

Variation  in  mean  litter  size  related  to  latitude  and  altitude  has  been  re- 
ported for  several  species  of  small  mammals.  Lord  (1960)  analyzed  data  on 
several  species  and  concluded  there  was  a  regression  of  litter  size  on  latitude 
in  small  nonhibernating  prey  species.  Dunmire  ( 1960 )  added  the  dimension 
of  altitude  when  he  reported  an  increase  with  elevation  of  mean  litter  sizes 
of  deer  mice  from  the  White  Mountains  in  California.  Mean  litter  sizes  in 
all  cases  were  larger  at  northern  locations  and  high  elevations  than  at  more 
southern  or  lower  localities. 

Several  explanations  have  been  proposed  to  account  for  the  observed  varia- 
tion. Lord  ( 1960 )  reviewed  and  rejected  several  hypotheses  before  proposing 
his  own  theory  that  higher  mortality  rates  during  northern  winters  required 
an  increase  in  reproductive  rate.  We  cannot  accept  this  explanation  because 
it  contradicts  established  principles  of  population  dynamics. 

The  problem  is  part  of  the  larger  question  of  regulation  of  fecundity  in  all 
animals.  Lack  ( 1948,  1954 )  has  explained  the  regulation  of  clutch  size  and 
litter  size  in  terms  of  natural  selection.  The  modal  number  in  his  view  repre- 
sents the  most  consistently  successful  clutch  or  litter.  Williams  ( 1967 )  has 
presented  a  mathematical  refinement  of  Lack's  Principle.  According  to  his 
concept,  an  allocation  of  parental  energy  between  present  and  residual  re- 
productive values  that  will  maximize  the  total  reproductive  value  is  selectively 
advantageous.  The  cost  of  rearing  a  large  or  better  nourished  brood  now  is 
reduction  of  future  reproduction.  The  litter  size  prevalent  in  a  particular 
population  represents  the  best  investment  possible  for  the  particular  situation 
of  the  population. 

Although  Williams  did  not  specifically  consider  intraspecific  latitudinal 
variation  in  litter  size,  our  own  explanation,  developed  independently,  sub- 
stantially parallels  his  general  treatment.  We  believe  the  shorter  seasons  of 
more  northern  latitudes  or  higher  altitudes  limit  the  number  of  times  an 
animal  resident  in  those  areas  is  able  to  reproduce  in  its  lifetime  compared 
to  its  relatives  in  lower  or  more  southern  regions.    It  therefore  becomes  ad- 

281 


213 


282  JOURNAL  OF  MAMMALOGY  Vol.  49,  No.  2 

vantageous  for  an  animal  to  invest  its  energies  in  a  few,  large,  early  litters 
even  though  doing  so  reduces  its  life  expectancy  and  total  reproductive  con- 
tribution below  the  maximum  achievable  by  many  small  litters.  This  is  so 
because  short  seasons  make  it  impossible  for  the  animal  to  realize  the  returns 
from  the  conservative  approach  within  its  life-span.  The  most  productive 
strategy  is  the  production  of  large  litters.  This  idea  is  developed  and  illus- 
trated below. 

Results  and  Discussion 

Our  interest  in  the  problem  began  with  the  observations  recorded  in  Table 
1.  Feromyscus  maniculatus  had  been  collected  at  several  sites  in  Colorado 
along  a  transect  extending  from  the  plains  of  central  Weld  County  to  timber- 
line  in  western  Larimer  County.  The  increase  in  mean  potential  litter  size 
parallels  the  experience  of  Dunmire  ( 1960 )  in  the  White  Mountains  of  Cali- 
fornia. The  regression  of  mean  litter  size  on  elevation  is  of  the  same  order 
of  magnitude  as  that  on  latitude  as  determined  by  Lord  (1960).  The  data 
thus  illustrate  the  general  nature  of  the  variation. 

The  major  factors  influencing  the  potential  rate  of  increase  of  a  species  are 
the  number  of  female  young  per  female  per  parturition  and  the  length  of  the 
period  from  birth  to  first  reproduction.  However  in  realistically  appraising 
the  number  of  young  per  female  per  litter  it  is  necessary  to  consider  the 
actual  contribution  to  the  next  generation  represented  by  that  litter  (Lack, 
1948,  1954).  If  survival  to  maturity  were  a  linear  function  of  litter  size  and 
decreased  10%  for  each  additional  young,  then  only  2.5  (1.25  females)  in  a 
litter  of  five  and  only  2.4  ( 1.2  females )  in  a  litter  of  six  would  effectively  be 
contributed  on  the  average  to  the  next  generation.  If  these  were  the  only 
factors  influencing  the  rate  of  increase  and  time  to  maturation  were  uniform 
in  the  species,  then  a  phenotype  producing  the  greatest  effective  number  (5) 
would  have  the  highest  potential  rate  of  increase  and  thus  the  selective  ad- 
vantage. 

Reproductive  longevity  and  subsequent  reproduction,  however,  also  play 
a  role  in  determining  the  rate  of  increase.  Each  successive  litter  contributes 
an  increment  to  the  total  reproductive  value.  The  value  of  each  increment 
declines  the  later  its  production  occurs  in  life,  but  the  collective  importance 
of  the  increments  in  influencing  the  rate  of  increase  grows  as  the  margin  of 
difference  between  the  effective  numbers  of  different  litter  sizes  diminish 
and  as  the  length  of  the  maturational  period  lengthens  (Fisher,  1930;  Birch, 
1948).  This  portion  of  the  reproductive  value  is  the  major  element  involved 
in  the  phenomenon  of  latitudinal  and  altitudinal  variations  in  litter  size. 

The  magnitude  of  the  contribution  to  the  rate  of  increase  by  successive 
litters  depends  in  part  on  the  survival  of  the  parents  (Birch,  1948).  Bearing 
and  rearing  young  constitutes  a  risk  for  the  parent.  The  presence  of  the 
young  reduces  concealment  of  parents  from,  and  adds  to  their  vulnerability 
to,  predators.  Increased  foraging  activity  also  exposes  the  parents  to  greater 
dangers  of  predation.    Physiological  stresses  such  as  nutritional  deficiencies 


214 


May  1968 


SPENCER  AND  STEINHOFF"— LITTER  SIZE 


283 


Table    1. — Fieciticncy    distribution    of    embryo    counts    in    Pcroinysciis    nianiculatus    from 

different  elevations. 


Number 

Mean 

Mean 

of 

litter 

bod\' 

Site 

females 

1 

2 

3 

4 

•■D 

6 

7 

8 

9 

size 

length 

Plains  (5100-5300  ft) 
Coal  Creek  10 

Pierce  17 

Cobb  Lake  29 


Subtotal 


56 


5  3  1 
2  9  4 
2     17       9 


1 


9     29     14       1 


4.0 


95.5  -0.7 


Foothills  ( 5500-6500  ft ) 
Rist  Canyon  22 

Siiltzcr  Culch  15 


Subtotal 


37 


2 
2 


S 
10 


6 
2 


18 


4.1 


95.9  -0,9 


Mountains  (8000-11,000  ft; 


Buckhorn  R.  S. 

7 

1 

3 

1 

I 

1 

Pennock  Creek 

4 

1 

3 

Cirques 

3 

1 

1 

1 

5.0 

94.2 

Subtotal 

14 

2 

6 

1 

2 

1 

2 

-2.2 

Pingree  Park 

33 

1 

1 

6 

6 

11 

5 

2 

1 

5.6 

Mountain 

subtotal 

47 

1 

O 

12 

7 

13 

6 

4 

1 

5.4 

and  post  partum  diificulties  impair  the  survival  of  the  parents  and  damage 
their  capabilities  for  reproduction  in  the  future.  It  is  reasonable  to  assume 
that  the  effects  are  proportional  to  the  number  of  young  produced  ( Lack, 
1954,  1948).  Such  risk  is  incurred  at  each  successive  reproductive  event.  The 
greater  the  risk  and  the  more  times  repeated,  the  more  the  survival  rate  is 
lowered  and  reproduction  in  later  life  is  curtailed.  Less  drastic  effects  than 
actual  death  of  the  parents  are  probable  and  perhaps  even  more  important. 
However  the  end  result  is  the  same  and  we  feel  justified  in  regarding  these 
lesser  effects  as  a  form  of  mortalitv. 

The  natural  longevity  (maximum  physical  reproductive  longevity)  of  the 
organism  and  extrinsic  factors  such  as  climate  impose  an  upper  limit  on  the 
maximum  number  of  opportunities  for  reproduction  (hereafter  designated 
MOR).  For  example  if  the  season  permitted  four  litters  annually  and  the 
maximum  reproductive  longevity  of  the  species  were  2  years  the  MOR  would 
be  eight.  Only  a  fraction  of  any  age  class  would  attain  the  maximum  limit 
MOR.  The  actual  proportion  of  the  population  that  achieved  the  maximum 
would  depend  upon  the  mortality  rates  discussed  above,  and  would  be  in- 
versely proportional  to  litter  size.  It  follows,  then,  that  any  reduction  in  the 
MOR  would  have  a  relatively  greater  effect  on  the  rate  of  increase  of  pheno- 
types  producing  smaller  number  of  young  per  litter  and  having  higher  sur- 
vival rate  than  on  phenotypes  producing  large  litters. 


215 


284  JOURNAL  iW  MAMMALOGY  Vol.  49,  No.  2 

This  is  the  Hne  of  reasoning  that  led  to  our  conception  of  the  connection 
between  length  of  season  and  variation  in  litter  size.  Thus  far  we  have  ap- 
proached the  problem  strictly  from  the  theoretical  aspect  by  constructing 
models  of  the  growth  of  idealized  populations.  We  then  studied  the  conse- 
quences for  the  potential  intrinsic  rate  of  increase  of  reducing  the  MOR  and 
changing  the  length  of  the  period  of  maturation.  For  simplicity,  the  relation- 
ships of  survival  of  the  young  to  maturity  and  survival  of  parents  was  as- 
sumed to  be  an  inverse  linear  function  of  litter  size.  Consideration  of  avail- 
able data  on  guinea  pigs  (Lack,  1948),  Peromysctis  (McCabe  and  Blanchard, 
1950)  and  birds  and  lizards  (Lack,  1954)  indicated  that  these  may  be  accept- 
able approximations.  All  effects  of  fecundity  on  future  parental  reproduction 
were  combined  under  the  heading  of  parental  mortality.  All  mortality  not 
related  to  litter  size  was  ignored.  Litter  size  was  assumed  to  be  a  constant 
characteristic  throughout  the  population  and  independent  of  age.  Only  female 
births  were  considered.  The  unit  of  time  was  taken  to  be  the  minimum  in- 
terval between  successive  parturitions  and  each  mature  female  was  assumed 
to  reproduce  at  each  interval.  Net  reproductive  ratios  and  rates  of  increase 
were  evaluated  by  a  combination  of  numerical  integration  and  graphic  methods. 
Lotka  (1925),  Fisher  (1930),  and  particularly  Birch  (1948)  were  the  main 
sources  of  inspiration  and  methods  used  in  the  computations. 

Fig.  1  summarizes  the  findings  of  our  study.  Observe  that  the  size  of  the 
litter  with  the  greatest  potential  rate  of  increase  declines  as  the  MOR  in- 
creases. The  shift  reflects  the  relatively  greater  increase  in  the  total  repro- 
ductive value  of  producers  of  small  litters  as  the  number  of  late  reproductions 
is  allowed  to  increase.  Note  also  that  the  shift  is  rather  abrupt  and  little 
affected  by  further  increase  in  MOR.  The  range  of  the  shift  increases  as  the 
period  of  maturation  lengthens.  Changes  in  the  parameters  of  survival  of 
parents  and  young  also  affect  the  locus  and  magnitude  of  the  shift  but  these 
effects  have  not  yet  been  thoroughly  explored.  Approximations  of  the  varia- 
tion shown  in  Table  1  were  achieved  by  substitution  into  the  calculations  for 
curve  C  (Fig.  1)  of  the  following  coefficients.  The  coefficient  of  regression 
for  survival  of  young  to  maturity  on  litter  size  used  was  -.10  and  of  survival 
of  parents  on  litter  size  was  -.016.  It  of  course  would  be  possible  to  obtain 
the  same  approximation  by  an  almost  limitless  number  of  combinations,  but 
the  important  point  is  that  the  magnitude  of  the  coefficients  required  is  of 
plausible  order. 

The  analysis  offers  an  explanation  of  the  observed  distribution  of  latitudinal 
variation  in  litter  size  among  mammals  considered  by  Lord  ( 1960 ) .  The 
fossorial  and  hibernating  species  investigated  (Spermophilus  and  Thomomys) 
usually  have  one  litter  annually.  Their  period  of  development  from  birth  to 
first  reproduction  is  about  1  year  or  6  months  when  two  litters  are  produced 
(Asdell,  1964).  The  effect  of  shortening  the  annual  season  would  thus  have 
little  effect  on  the  reproductive  opportunities  of  these  organisms.  Their  pat- 
terns of  reproduction  are  approximated  by  that  shown  in  curve  A  in  Fig.  1. 


216 


May  1968  SPENCER  AND  STEINHOFF— LITTER  SIZE  285 


6- 


B 

3 

z  4 


Maturity     at    one    reproductive     interval 


Maturity    at     two     reproductive      intervals 


Maturity    at    ttiree    reproductive    intervals 

P ►€ 


2  4  8  16 

Maiimum    number   of   opportunities     for    reproduction 

Fig.  1. — Change  in  the  fitness  of  Htter  sizes  as  the  maximum  number  of  opportunities  fur 
reproduction  is  increased.  The  Hnes  connect  the  htter  sizes  liaving  the  greatest  potential 
rate  of  increase  under  the  hmitations  imposed. 


Only  drastic  differences  in  length  of  season  would  produce  noticeable  effects. 
Even  then  the  magnitude  of  variation  would  be  relatively  small.  On  the  other 
hand,  the  species  of  mice  and  shrews  that  display  latitudinal  variation  can 
produce  several  (up  to  12)  litters  annually  and  yet  have  a  period  of  develop- 
ment from  birth  to  first  reproduction  equal  to  several  reproductive  intervals. 
Many  shrews  begin  reproducing  at  the  age  of  1  year.  The  reproductive  pat- 
terns of  these  animals  correspond  to  curve  C.  Effects  of  significant  magnitude 
could  be  produced  with  relatively  small  changes  in  the  length  of  the  season. 
In  the  Colorado  data,  for  example,  the  growing  seasons  on  the  plains  (5000 
ft)  and  in  subalpine  areas  (8000-10,000  ft)  differ  by  almost  a  factor  of  two. 
An  interesting  aspect  of  the  analysis  is  that  the  relative  superiority  of  the 
favored  phenotype  is  reduced  directly  as  the  MOR.  Therefore,  the  genetic 
variance  in  the  population  would  be  correspondingly  reduced.  Attainment  of 
maximum  fitness  in  the  population  should  be  a  long  process;  in  two  popula- 
tions, the  one  occupying  the  environment  with  the  shorter  season  should 
have  the  greater  variability  in  litter  size  after  a  given  period.    This  would  be 


217 


286  JOURNAL,  OF  MAMMALOGY  Vol.  49,  No.  2 

particularly  true  if  gene  flow  between  them  were  occurring.    This  condition 
is  seen  in  Table  1. 

Intraspecific  variation  may  originate  in  many  ways.  There  is,  however, 
only  one  agency,  natural  selection,  regularly  producing  the  directed  sort  of 
variation  we  are  considering.  Lord  (1960)  has  suggested  that  the  increased 
size  of  litters  may  be  a  compensating  response  to  mortality  among  the  small 
mammals  during  winter.  However,  if  a  population  of  a  species  were  able  to 
increase  its  reproductive  potential  in  this  manner,  the  ability  would  be  just 
as  adaptive  in  any  environment.  Variation  would  quickly  disappear.  If  the 
variation  is  to  be  described  in  terms  of  fitness  then  the  particular  phenotypes 
characteristic  of  each  locality  must  have  the  greatest  fitness  in  that  situation. 
Our  explanation  offers  an  hypothesis  explaining  how  the  differential  in  fitness 
may  originate. 

Literature  Cited 

AsDELL,  S.  A.      1964.     Patterns  of  mammalian  reproduction.    Cornell  Univ.  Pre.ss,   Ithaca, 

2ncl  ed.,  viii  +  670  pp. 
Bn^CH,  L.  C.      1948.     The  intrinsic  rate  of  increase  of  an  insect  population.    J.  Anim.  Ecol., 

17:    15-26. 
DuxMiRE,  W.   W.      1960.     An  altitudinal  survey  of  reproduction   in   Pcronnj.scus   niaiiictt- 

latus.  Ecology,  41:    174-182. 
Fisher,  R.  A.      1930.     The  genetical  theory  of  natural  selection.    Clarendon  Press,  O.xford, 

272  pp. 
Lack,  D.      1948.     The  significance  of  litter-size.    J.  Anim.  Ecol.,   17:   45-50. 
.      1954.     The    natural    regulation    of    animal    numbers.     Clarendon    Press,    Oxford, 

viii  +  .34.3  pp. 
Lord,   R.   D.,   Jr.      1960.     Litter  size   and   latitude   in   North    American   mannnals.     Amer. 

Midland  Nat.,  64:   488^99. 
LoTKA,  A.  J.      1925.     Elements  of  physical  biology.    Williams  and  Wilkins,  Baltimore. 
McCabe,    T.    T.,    and   B.    D.    Blaxchard.      1950.     Three    species    of    Peromyscus.     Rood 

Associates,  Santa  Barbara,  California,  v  -|-   136  pp. 
Williams,   G.  C.      1967.     Natural  selection,  the  costs  of   reproduction,   and   a   refinement 

of  Lack's  principle.    Amer.  Nat.,   100:   687-690. 

Division  of  Biological  Science,  Fort  Lewis  College,  Durango,  Colorado  81301,  and 
Departmetit  of  Fishery  and  Wildlife  Biology,  Colorado  State  University,  Fort  Collins,  80521. 
Accepted  2  January  1968. 


218 


Sonderdruck  aus  Z.  f.  Saugetierkunde  Bd.  30  (1965),  H.  1,  S.  10—20 

A!le    Rechte,    audi    die    der   Cbersetzung,    des    Nadidrudts    und    der    photomedianischen    Wiedergabe,    vorbehalten. 
VERLAG    PAUL    PAREY    ■    HAMBURG  1    •    SPITALERSTRASSE  12 

The  effects  of  suckling  on  normal  and  delayed  cycles  of 
reproduction  in  the  Red  Kangaroo 

By  G.  B.  Sharman 

Eingang  des  Ms.  23.  12.  1963 

Introduction 

In  non-lactating  female  marsupials  the  occurrence  of  fertilization,  followed  by  imme- 
diate gestation  of  the  embryo,  does  not  delay  the  onset  of  the  following  oestrus.  In 
those  marsupials  in  which  the  gestation  period  is  considerably  shorter  than  the  length 
of  one  oestrous  cycle,  such  as  Didelphis  virginiana  (Hartman,  1923)  and  Trichosurus 
vulpecula  (Pilton  and  Sharman,  1962),  oestrus  recurs  at  the  expected  time  if  the  young 
are  removed  at  birth.  In  several  species  of  Macropodidae,  sudi  as  Setonix  brachyurus 
(Sharman,  1955),  Potorous  tridactylus  (Hughes,  1962)  and  the  Red  Kangaroo  (Shar- 
man and  Calaby,  1964),  the  gestation  period  occupies  almost  the  length  of  one  oestrous 
cycle  and  oestrus  is  imminent  at  the  time  of  parturition.  Oestrus  thus  recurs  just  after 
the  young  reach  the  pouch  (post-partum  oestrus)  presumably  because  pro-oestrus  chan- 
ges are  initiated  before  the  onset  of  the  suckling  stimulus.  In  all  marsupials  suckling 
of  young  in  the  pouch  is  accompanied  by  a  lengthy  period  during  which  oestrus  does 
not  occur.  This  period  is  called  the  quiescent  phase  of  lactation  or,  simply,  the  quies- 
cent phase.  It  differs  from  seasonal  anoestrus  in  that  the  ovaries  and  other  reproduc- 
tive organs  respond  to  the  removal  of  the  suckling  stimulus  by  resuming  cyclic  func- 
tions. Those  marsupials  in  which  post-partum  oestrus  occurs  exhibit  discontinuous 
embryonic  development  analogous  to  the  delayed  implantation  which  occurs  in  some 
eutherian  mammals.  If  fertilization  takes  place  at  post-partum  oestrus  the  resulting 
embryo  assumes  a  dormant  phase,  at  the  blastocyst  stage,  and  is  retained  as  a  dormant 
blastocyst  during  the  quiescent  phase.  In  these  marsupials  pregnancy  (the  interval 
between  copulation  at  post-partum  oestrus  and  parturition)  is  long  and  gestation  of 
the  embryo  is  interrupted  by  the  dormant  phase. 

In  the  Red  Kangaroo,  Megaleia  rufa  (Desm.),  the  oestrous  cycle  averages  34  to  35 
days  and  the  gestation  period  is  33  days  in  length  (Sharman  and  Calaby,  1964).  Post- 
partum oestrus  occurs,  usually  less  than  2  days  afler  the  newborn  young  reaches  the 
pouch,  and  a  dormant  blastocyst  is  found  in  the  uterus  of  females,  fertilized  at  post- 
partum oestrus,  which  are  suckling  young  less  than  200  days  old  in  the  pouch  (Shar- 
man, 1963).  If  the  young  is  removed  from  the  pouch  suckling  ceases  and  the  dormant 
blastocyst  resumes  development:  the  young  derived  from  it  being  born  about  32  days 
after  removal  of  the  pouch  young  (RPY).  This  birth  is  followed  by  another  post- 
partum oestrus  or,  if  the  female  was  not  carrying  a  blastocyst,  by  a  normal  oestrus. 
Oestrus  recurs  at  the  same  number  of  days  after  RPY  irrespective  of  whether  a  de- 
layed blastocyst  was  carried  or  not.  The  sequence  of  events  from  RPY  to  the  next 
oestrus  is  called  the  delayed  cycle  of  reproduction^  to  distinguish  it  from  the  normal 
reproductive  cycle  which  follows  oestrus.  The  delayed  reproductive  cycle  may  be 
divided  into  delayed  gestation  and  delayed  oestrus  cycle  according  to  whether  a  dor- 


1  The  term  "delayed  cycle  of  reproduction"  or  "delayed  (reproductive)  cycle",  was  introduced 
by  Tyndale-Biscoe  (1963)  to  describe  the  resumption  of  ovarian  activity,  and  the  features 
associated  with  it,  following  removal  of  pouch  young  (RPY). 


219 


Normal  and  delayed  cycles  of  reproduction  in  the  Red  Kangaroo  11 

niant  blastocyst  does  or  does  not  complete  development.  If  the  young  is  retained  in 
the  pouch  until  it  leaves  in  the  normal  course  of  events  the  delayed  reproductive 
cycle  occurs  coincident  with  the  latter  stages  of  pouch  life.  The  dormant  phase  of 
the  blastocyst  gives  way  to  renewed  development  when  the  pouch  young  is  a  little 
over  200  days  old  and  subsequent  vacation  of  the  pouch,  at  an  average  age  of  235  days, 
is  immediately  followed  by  birth  of  another  young  (Sharman  and  Calaby,  1964). 
The  young  is  suckled  for  another  130  days,  that  is  until  it  is  about  a  year  old,  after 
it  leaves  the  pouch.  During  this  period  the  normal  reproductive  cycle  occurs  if  the 
pouch  is  not  occupied.  It  is  thus  evident  that,  although  the  delayed  reproductive  cycle 
occurs  after  RPY  and  cessation  af  lactation,  some  factor  other  than  the  actual  pro- 
duction of  milk  must  be  implicated  for  both  delayed  and  normal  cycles  may  also 
occur  during  lactation. 

The  aim  of  the  experiments  reported  below  was  to  determine  the  effect  of  the 
suckling  stimulus  on  both  normal  and  delayed  reproductive  cycles.  Additional  suck- 
ling stimulus  was  provided  by  fostering  an  extra  young  on  to  females  already  suck- 
ling a  young-at-foot.  The  experimental  approach  was  suggested  by  chance  obser- 
vations on  a  female  Red  Kangaroo  which,  while  suckling  her  own  young-at-foot, 
alternately  fed  the  young  of  another  female  kept  in  the  same  enclosure.  There  are 
four  teats  in  the  pouch  but  the  teat  to  which  the  young  attaches  after  birth  alone 
produces  milk  and  its  underlying  mammary  gland  produces  all  the  milk  for  the 
young  from  birth  to  weaning.  The  female's  own  young  and  the  foster-young  thus 
shared  the  products  of  a  single  mammary  gland  and  used  the  same  teat  alternately. 
Some  initial  results,  in  so  far  as  they  were  relevant  to  the  theme  of  delayed  implanta- 
tion, were  reported  earlier  in  a  review  of  that  subject  (Sharman,  1963). 


Methods 

The  results  presented  consist  of  observations  on  a  minimum  of  five  reproductive  cyc- 
les in  the  female  Red  Kangaroo  in  each  of  the  following  categories: 

1.  Normal  cycle  of  reproduction,  suckling  one  young-at-foot. 

2.  Normal  cycle  of  reproduction,  suckling  two  young-at-foot. 

3.  Delayed  cycle  of  reproduction,  suckling  one  young-at-foot. 

4.  Delayed  cycle  of  reproduction,  suckling  two  young-at-foot. 

The  results  are  compared  with  data  on  the  normal  and  delayed  cycles  of  reproduc- 
tion in  non-lactating  females  most  of  which  have  been  published  elsewhere  (Sharman, 
1963;  Sharman  and  Calaby,  1964;  Sharman  and  Pilton,  1964).  In  most  cases  the 
experimental  females  were  pregnant  or  carrying  dormant  blastocysts  so  that  cycles 
of  normal  or  delayed  gestation  with  subsequent  post-partum  oestrus  were  studied. 
The  gestation  periods  and  cycles  were  regarded  as  having  been  significantly  lengthened 
when  they  occupied  a  time  greater  by  the  length  of  two,  or  more,  standard  deviations 
than  similar  cycles  in  control,  non-lactating,  females 

Some  difficulty  was  experienced  in  getting  females  to  accept  foster-young  and  only 
six  females  readily  did  so.  The  experiments  were  therefore  done  serially  one  female 
being  used  in  two  and  two  females  in  three  experiments. 

The  animals  were  watched  from  a  hide  overlooking  the  enclosures  and  observed 
with  binoculars.  An  initial  watch  was  always  done  to  find  whether  females  accepted 
their  potential  foster-young.  Thereafter  prolonged  watches  were  kept  on  some  females 
to  determine  the  amount  of  time  spent  suckling  the  young-at-foot. 

Vaginal  smears  for  the  detection  of  oestrus  and  copulation  were  taken  as  reported 
previously  (Sharman  and  Calaby,  1964). 


220 


12  G.  B.  Sharman 

Results 

Effects  of  suckling  on  the  normal  cycle  of  reproduction 

In  thirteen  non-lactating  female  Red  Kangaroos  forty-two  intervals  from  oestrus  to 
the  succeeding  oestrus  averaged  34.64  days  with  a  standard  deviation  of  2.22  days 
(34.64  ±  2.22  days).  Twenty  gestation  periods  in  fourteen  females  lasted  33.00  ±  0.32 
days  (Fig.  lA).  In  five  females,  each  observed  for  a  single  reproductive  cycle  while 
suckling  one  young-at-foot,  the  intervals  between  two  successive  oestrous  periods  were 
not  different  from  those  in  non-lactating  females  (Fig.  IB).  In  another  female  (K32a) 


A     42  cycles 


K60 

K53a 

Kic 

K30c 

K12c 

K32q 

K3lQ 

K31b 

K36c 

K30a 

Kdd 

K4e 

K35c 


12 


16 


20        24        28        32 


36 


40        44 


48 


Intervals  between  successive  oestrous  periods 


Fig.  1.  Intervals  between  successive  oestrous  periods  in  nonlactating  (control)  female  Red 
Kangaroos  (A),  females  sudiling  one  young-at-foot  (B)  and  females  suckling  two  young-at- 
foot  (C).  Black  lines  —  continuous  embryonic  development,  broken  lines  —  approximate 
periods  of  dormant  phase  in  embryo  induced  and  maintained  by  suckling  young-at-foot,  open 
lines  —  no  embryos  present,  bars  inserted  in  A  —  standard  deviations  either  side  of  mean. 

the  gestation  period  was  not  significantly  different  from  that  of  control  females  but 
oestrus  did  not  occur  until  5  days  post-partum.  This  was  the  longest  interval  between 
parturition  and  post-partum  oestrus  recorded  but  it  is  not  regarded  as  significant.  Two 
cycles  in  female  K31,  one  lasting  41  days  and  one  47  days,  were  abnormally  long.  The 
41-day  cycle  is  of  special  significance  since  the  interval  between  copulation  and  birth 
was  40  days.  This  differs  so  much  from  the  gestation  period  in  the  control,  non-lacta- 
ting, females  that  it  must  be  assumed  that  suckling  of  the  single  young-at-foot  induced 
a  short  quiescent  phase  in  the  uterus  accompanied  by  a  dormant  phase  of  about  7  days 
in  the  embryo.  The  47-day  cycle  was  over  12  days  longer  than  the  mean  normal  cycle 
length  and  7  days  longer  than  the  maximum  cycle  length.  The  female  copulated  at 
oestrus  but  did  not  give  birth  so  it  is  presumed  that  fertilization  did  not  occur. 

In  three  females  already  suckling  one  young-at-foot,  which  had  another  young-at- 
foot  fostered  on  to  them  at  about  the  time  of  fertilization,  the  lengths  of  the  repro- 
ductive cycles  were  not  significantly  different  from  those  in  control  females.  Two 
females  had  significantly  longer  cycles  than  in  control  females.  One  of  these  (K36)  was 
used  in  three  successive  experiments  while  suckling  the  same  two  young-at-foot.  In  the 
first  of  these  (K36a)  the  extra  suckling  stimulus  had  no  significant  effect  on  the  length 
of  the  reproductive  cycle.  The  second  experiment  concerned  the  delayed  reproductive 
cycle  and  is  reported  below.  During  the  third  experiment  (K36c)  the  young  were  being 
weaned  but  a  highly  significant  result  was  obtained.  The  interval  from  copulation  to 


221 


Normal  and  delayed  cycles  of  reproduction  in  the  Red  Kangaroo 


13 


birth  showed  conclusively  that  a  dormant  phase  had  been  induced  and  maintained  in 
the  embryo  for  about  14  days  of  the  47-day  pregnancy.  In  the  other  female  in  which 
the  cycle  was  prolonged  (K4e)  the  embryo  presumably  had  a  dormant  phase  of  about 
6  days. 

Effects  of  suckling  on  the  delayed  cycle  of  reproduction 

In  ten  non-lactating  females  thirteen  intervals  from  RPY  to  the  succeeding  oestrus 
were  34.46  ±  1.92  days.  In  seven  of  these  females  the  delayed  gestation  period  was 
31.64  ±  0.65  days  (Fig.  2A).  There  was  no  evidence  that  suckling  one  young-at-foot 
had  any  effect  on  the  length  of  the  delayed  reproductive  cycle  (Fig.  2B).  In  one  female 
(K12a)  the  interval  from  RPY  to  the  following  oestrus  was  38  days  but  this  falls  short 
of  the  minimum  interval  accepted  as  significantly  different. 

All  six  females  suckling  two  young-at-foot  (Fig.  2C)  were  carrying  a  dormant 
blastocyst  in  the  uterus  when  the  pouch  young  were  removed.  In  five  of  these  the 
Interval  RPY  to  birth  was  significantly  longer  than  in  control  females  (Fig.  2C).  The 
interval  RPY  to  the  next  oestrus  was  longer  than  the  mean  for  control  non-lactating 
females  in  all  six  experimental  females  and  in  three  of  them  (K4b,  K30b,  K36b)  the 
difference  from  controls  was  highly  significant.  It  must  be  concluded  that  the  blasto- 
cysts of  five  of  the  above  experimental  females  remained  in  the  dormant  phase  for 
between  3  and  22  days  longer  afler  RPY  than  did  those  of  control  non-lactating 
females  and  females  suckling  one  young-at-foot. 


A     13  cycles 


B 


Kio 

K15 

K38b 

K12b 

K12a 

K38a 
K63b 
K32b 
K36b 
K30b 
K4b 


12 


16         20 


24 


28 


32        36 


40 


44        48        52        56 


Intervals   between   RPY  and    oestrus 


Fig.  2.  Intervals  between  removal  of  pouch  young  (RPY)  and  the  next  oestrus  in  non-lactating 
(control)  female  Red  Kangaroos  (A),  females  suckling  one  young-at-foot  (B)  and  females 
suckling  two  young-at-foot  (C).  Black  lines  —  continuous  embryonic  development,  broken 
lines  —  approximate  periods  of  continued  dormant  phase  of  embryo  maintained  by  suckling 
young-at-foot,  bars  inserted  in  A  —  standard  deviations  either  side  of  mean. 


The  amount  suckling  in  relation  to  occurrence  of  parturition  and  return  to  oestrus 

Observations  on  the  habits  of  the  pouch  young  suggested  that  the  stimulus  causing 
withholding  of  the  mother's  reproductive  cycles  might  be  tactile  and  received  via  the 
teat.  The  young  during  the  early  stages  of  pouch  life,  when  reproductive  cycles  were 
withheld,  were  suckled  continuously  and  could  not  regain  the  teat  if  removed  before 
the  age  of  6  weeks.  Later  young  were  able  to  take  the  teat  back  into  their  mouths  but 
were  seldom  found  free  of  the  teat  before  the  age  of  about  5  months.  On  the  other 


222 


14 


G.  B.  Sharman 


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hand  the  pouch  young 
present  when  the  delayed 
reproductive  cycle  occur- 
red apparently  frequently 
released  the  teat  as  they 
were  seen  protruding  their 
heads  from  the  pouch  to 
feed  from  the  ground  or 
leaving  the  pouch  entirely 
(Sharman  and  Calaby, 
1964). 

Theoretically  it  was  to 
be  expected  that  if  repro- 
ductive cycles  resumed  in 
response  to  a  lowered 
suckling  stimulus,  as  they 
did  during  the  terminal 
stages  of  pouch  feeding, 
then  the  cycles  which 
occurred  as  soon  as  the 
young  left  the  pouch 
should  have  been  of  nor- 
mal length.  Six  of  the  eight 
cycles  shown  m  Fig.  1 B 
were  the  first  which  oc- 
curred after  termination 
of  pouch  feeding.  Four 
were  of  normal  length  but 
two  cycles  in  one  female 
(K  31a,  b)  were  lengthe- 
ned by  a  significant 
amount.  Observations  on 
the  habits  of  the  young,  just 
after  they  left  the  pouch 
permanently,  showed  that 
they  frequently  attempted 
to  regain  the  pouch  but 
were  restrained  from 
doing  so  by  their  mothers 
(Sharman  and  Calaby, 
1964).  In  these  cases  they 
spent  long  periods  with 
their  heads  in  the  pouch 
during  which  time  they 
may  have  grasped  the 
teat.  It  is  also  possible 
that  the  young,  subjected 
permanently  for  the  first 
time  to  the  cooler  environ- 
ment outside  the  pouch, 
fed  more  frequently  than 
they  did  during  the  ter- 


223 


Normal  and  delayed  cycles  of  reproduction  in  the  Red  Kangaroo  15 

minal  stages  of  pouch  life.  This  would  result  in  a  greater  suckling  stimulus  being 
exerted:  at  least  during  the  initial  stages  of  life  outside  the  pouch. 

A  number  of  females  suckling  one  or  two  young-at-foot  were  watdied  continuously 
for  varying  periods  and  the  amounts  of  time  spent  suckling  were  recorded  (Table  1). 
It  was  at  once  apparent  that  females  feeding  two  young-at-foot  spent  nearly  twice  as 
much  time  suckling  as  did  females  with  a  single  young-at-foot.  The  relationship  bet- 
ween amount  of  suckling  and  interruption  or  resumption  of  the  reproductive  cycle  is, 
however,  not  so  obvious.  Thus,  in  female  K31,  48  and  51  minutes  of  suckling  per  day 
were  associated  with  lengthening  of  the  interval  between  successive  oestrous  periods 
and  48  minutes  per  day  with  inducing  and  maintaining  a  short  dormant  phase  in  the 
embryo.  In  two  other  females  (K60,  K30c)  a  greater  amount  of  suckling  apparently 
had  no  effect  on  the  length  of  the  cycle  or  on  pregnancy.  However,  although  the 
watches  were  done  during  the  relevant  cycles,  they  were  not  necessarily  done  at  the 
critical  period  of  the  cycle  when  the  suckling  stimulus  exerted  its  effect.  This  period 
could  not  be  ascertained  since  no  evidence  of  its  occurrence  was  available  until  the 
females  gave  birth  or  returned  to  oestrus.  The  figures  in  Table  1  are  thus  to  be  regar- 
ded as  no  more  than  a  guide  to  the  amount  of  suckling  whidi  occurred  at  the  critical 
period. 

The  most  conclusive  evidence  about  the  effect  of  the  suckling  stimulus  on  the  re- 
productive cycle  came  from  the  females  from  which  pouch  young  were  removed 
while  they  were  suckling  two  young-at-foot  (Fig.  2C).  In  one  of  these  females  (K38a) 
the  suckling  of  two  young-at-foot  was  without  effect  on  the  delayed  reproductive 
cycle;  in  three  (K32b,  K36b,  K63b)  the  delayed  cycle  began  while  two  young  were 
being  sudcled  but  in  two  others  (K4b,  K30b)  the  delayed  cycle  was  only  initiated 
when  one  of  the  suckling  young-at-foot  was  removed.  The  interval  from  removal  of 
the  young-at-foot  to  completion  of  the  delayed  cycle  was  approximately  the  same 
(31—32  days)  as  from  RPY  to  the  completion  of  the  cycle  in  the  control  females. 

The  two  intervals  between  successive  oestrous  periods  with  intervening  pregnan- 
cies which  were  observed  in  the  same  female  (K36a,  c)  while  suckling  the  same  two 
young-at-foot  call  for  some  comment.  Parturition  and  return  to  oestrus  occurred 
when  expected  in  the  first  cycle  but  were  delayed  significantly  in  a  subsequent  cycle 
when  the  young  were  much  older  and  were  being  weaned  (Fig.  IC).  During  this, 
latter,  cycle  one  of  the  young  frequently  grasped  the  teat  for  periods  of  10  minutes 
or  more  but  when  the  female's  pouch  was  examined  it  was  found  that  no  milk  could 
be  expressed  from  the  teat  and  that  the  mammary  gland  was  regressing.  This  was  in 
contrast  to  the  condition  in  other  females  suckling  young-at-foot  in  which  milk  could 
usually  be  readily  expressed.  No  watdi  was  done  to  observe  the  amount  of  time  the 
young  spent  sucking  the  dry  teat  as  the  significance  of  the  observation  was  only 
realised  after  completion  of  the  cycle.  This  cycle  is,  however,  of  particular  significance 
because  it  appears  likely  that  the  suckling  stimulus,  in  the  absence  of  lactation,  in- 
duced a  quiescent  phase  in  the  uterus  lasting  some  14  days  and  a  corresponding  period 
of  dormancy  in  the  blastocyst. 

Discussion 

Delayed  implantation  in  the  Red  Kangaroo  is  of  the  type  usually  referred  to  as  lacta- 
tion controlled  delayed  implantation.  This  description  is  adequate  in  so  far  as  the 
delayed  cycle  of  reproduction  is  initiated  following  removal  of  the  pouch  young  and 
cessation  of  lactation.  However,  the  delayed  cycle  also  occurs  during  the  seventh  and 
eighth  months  of  the  12-month  lactation  period.  It  therefore  follows  that,  in  these 
cases,  the  delayed  cycle  does  not  begin  in  response  to  the  cessation  of  lactation  or 
to  the  imminent  cessation  of  lactation.  The  quiescent  phase  of  lactation  with  asso- 


224 


1^  G.  B.  Sharman 

ciated  arrested  development  of  the  embryo  is  initiated  during  the  early  part  of  lac- 
tation while  a  sm.all  young  is  suckled  continuously  in  the  pouch  but  the  normal  re- 
productive cycle  may,  as  has  been  shown  above,  occur  during  the  latter  part  of  lac- 
tation. It  is  thus  much  more  likely  that  the  amount  of  suckling  stimulus  which  the 
female  receives  at  various  phases  of  the  lactation  period  is  of  paramount  importance 
in  determining  whether  the  normal  reproductive  cycle  shall  be  interrupted  or  whether 
the  delayed  cycle  shall  be  initiated.  The  experiments  reported  above  have  shown  that 
in  some  females  the  normal  cycle  is  interrupted  and  a  quiescent  phase  of  lactation, 
with  associated  dormant  phase  of  the  embryo  is  induced  by  increasing  the  suckling 
stimulus.  It  has  also  been  shown  that  the  stimulus  of  suckling  of  young,  outside  the 
pouch,  is  capable  of  prolonging  the  quiescent  phase  of  lactation  and  dormant  phase 
of  the  embryo. 

Two  other  factors  could  be  of  importance  in  determining  the  time  of  onset  of  the 
delayed  cycle  of  reproduction:  1.  Temporary  or  permanent  vacation  of  the  poudi. 
2.  Fall  in  milk  yield.  Temporary  emergence  from  the  pouch  first  occurs  when  the 
young  are  less  than  190  days  old  and  permanent  emergence  at  the  average  age  of 
235  days  —  that  is  a  few  days  before  the  completion  of  the  delayed  cycle  (Sharman 
and  Calaby,  1964)  but  the  delayed  cycle  apparently  begins  when  the  young  are  a 
little  over  200  days  old.  Precise  data  on  this  point  are  difficult  to  obtain  but  assu- 
ming that  the  delayed  cycle,  once  initiated,  proceeds  at  the  same  rate  in  lactating 
females  as  it  does  in  females  from  which  the  poudi  young  are  removed  then  it  must 
begin  about  30  days  before  the  young  leaves  the  pouch.  This  is  in  agreement  with  the 
massive  amount  of  data  obtained  from  Red  Kangaroos  taken  in  the  field.  The  onset 
of  the  delayed  cycle  can  hardly  occur  in  response  to  a  fall  in  milk  yield  since  it  takes 
place  when  the  young  is  actively  growing  and  when  it  is  increasing  rapidly  in  weight. 
From  the  age  of  200  days  to  the  age  of  220  days,  during  which  period  the  delayed 
cycle  is  resumed,  the  pouch  young  increase  from  about  2.5  to  3.5  kg  in  weight  which 
is  not  the  expected  result  of  a  fall  in  milk  yield.  Furthermore  removal  of  young  from 
the  pouches  of  females  whidi  were  suckling  two  young-at-foot  must  have  been  ac- 
companied by  a  fall  in  milk  yield  yet  under  these  circumstances  the  quiescent  phase 
of  lactation  with  associated  dormant  blastocyst  continued  in  five  of  six  females 
(Fig.  2C). 

The  importance  of  the  suckling  stimulus  in  marsupial  reproduction  was  demon- 
strated by  Sharman  (1962)  and  Sharman  and  Calaby  (1964)  who  transferred  new- 
born young  Trichosurus  vulpecula  and  Megaleia  rufa  to  the  pouches  or  teats  of  non- 
lactating,  non-mated  or  virgin  females  of  each  of  these  species  at  the  appropriate 
number  of  days  after  oestrus.  The  suckling  stimulus  exerted  by  the  young  induced 
the  onset  of  lactation  without  the  prior  occurrence  of  pregnancy  and  oestrous  cycles 
were  withheld  while  the  foster-young  were  suckled  in  the  pouch.  Sharman  and  Ca- 
laby (1964)  were  unable  to  demonstrate  any  behavioural  differences  between  preg- 
nant and  non-mated  female  Red  Kangaroos  at  the  same  number  of  days  after  oestrus 
except  that  pregnant  females  repeatedly  cleaned  their  pouches  just  before  giving  birth. 
Other  authors  (Hill  and  O'Donoghue,  1913;  Hartman,  1923;  Sharman,  1955;  Pil- 
TON  and  Sharman,  1962)  have  drawn  attention  to  the  remarkable  resemblances  of 
post-oestrous  dianges  in  pregnant  females  to  those  of  non-mated  females  in  various 
species  of  marsupials.  It  is  apparent,  that  whereas  in  polyoestrous  eutherian  mammals 
hormones  produced  by  the  embryonic  membranes  modify  the  reproductive  cycle  and 
prevent  the  recurrence  of  oestrus  during  pregnancy,  no  such  mechanism  has  yet  been 
demonstrated  in  any  marsupial.  In  those  marsupials  which  do  not  have  a  seasonal 
anoestrous  period,  such  as  the  Red  Kangaroo,  the  reproductive  cycle  is  continuous 
except  when  interrupted  by  the  quiescent  phase  of  lactation. 

Owen  (1839—47)  determined  the  gestation  period  (interval  from  mating  to  birth) 


225 


Normal  and  delayed  cycles  of  reproduction  in  the  Red  Kangaroo  17 

of  a  lactating  female  Great  Grey  Kangaroo  as  38—39  days.  Hediger  (1958)  stated 
that  K.  H.  WiNKELSTRATER  and  E.  Cristen  in  Zurich  Zoo  found  gestation  periods 
of  30  and  46  days  in  the  same  species  and  later,  in  the  same  paper,  stated  that  a 
young  was  born  on  the  forty-sixth  day  after  mating  in  a  lactating  female  Great  Grey 
Kangaroo.  However  the  dates  quoted  by  Hediger  show  that  the  „gestation  period" 
was  actually  57  days.  In  non-lactating  Great  Grey  Kangaroos  Miss  Phyllis  Pilton 
(pers.  comm.)  found  the  gestation  period  was  about  30  days  and  in  the  C.S.I.R.O. 
Division  of  Wildlife  Research  four  gestation  periods  in  three  non-lactating  females 
were  33  days  6  hours  to  34  days  6  hours,  33  days  18  hours  to  34  days  10  hours, 
34  days  to  34  days  17  hours  and  34  days  to  34  days  20  hours.  It  is  apparent  that, 
although  the  Great  Grey  Kangaroo  does  not  have  the  same  type  of  lactation  con- 
trolled delayed  implantation  as  occurs  in  the  Red  Kangaroo  and  other  marsupials 
(Sharman,  1963),  intervals  between  mating  and  birth  in  lactating  females  may  be  an 
unreliable  guide  to  the  gestation  period.  Hediger  (1958)  stated  that  exact  gestation 
periods  in  kangaroos  and  other  marsupials  are  difficult  to  determine  because  ovulation 
occurs  several  days  after  mating  and  spermatozoa  can  remain  active  in  the  oviduct 
for  long  periods.  This  may  be  true  of  the  marsupial  Dasyurus  viverrinus,  but  Hill 
and  O'Donoghue's  (1913)  work  on  this  species  has  not  been  repeated  and  confirmed. 
Delayed  ovulation  and  storage  of  spermatozoa  do  not  occur  in  Didelphis  (Hartman, 
1923),  Setonix  (Sharman,  1955)  or  Trichosurus  (Pilton  and  Sharman,  1962)  and 
gestation  periods  in  non-lactating  females  of  these  species  can  be  determined  with 
considerable  accuracy.  In  the  Red  Kangaroo  the  intervals  between  mating  and  birth 
in  some  lactating  females  (Table  2)  are  not  true  gestation  periods  since  they  include 


Table  2 

Intervals  from  mating  to  birth  and  intervals  from  removal  of  pouch  young  (RPY)  to  birth 
in  seven  female  Red  Kangaroos  subjected  to  different  levels  of  sudcling  stimulus 


No.  of  female 

K4 

K30             K31               K32              K36 
Intervals  from  mating  to  birth 

K38 

K63 

Non-sudiling 

33 

—             —             33             — 

— 

33 

Sudcling  1  young 

34 

33             40             33             — 

— 

33 

Suckling  2  young 

34,39 

33             —             —             32,47 
Intervals  from  RPY  to  birth 

Non-suckling 

32 

2,2             —             —             — 

32 

— 

Suckling  1  young 

31 

—             —             —             — 

31 

— 

Suckling  2  young 

54 

43             —             35             38 

32 

35 

a  period  of  arrested  development  of  the  embryo.  Plowever,  in  thirteen  non-lactating 
female  Red  Kangaroos  one  gestation  period  was  32  days,  one  was  34  days  and 
eighteen  were  33  days  in  length  (Sharman  and  Calaby,  1964).  The  true  gestation 
period,  as  in  the  species  above,  can  therefore  be  determined  with  precision. 

Perhaps  failure  to  recognise  the  importance  of  the  suckling  stimulus  accounts  for 
the  inaccuracy  of  some  of  the  marsupial  gestation  periods  given  in  International  Zoo 
Year  Book  Vol.  1  (Jarvis  and  Morris,  1959).  The  list  is  incomplete  and  at  least  half 
of  the  figures  given  are  wrong. 


226 


18  G.  B.  Sharman 

The  occurrence  of  lactation  controlled  delayed  implantation  in  marsupials  was  re- 
ported in  1954  (Sharman,  1954)  and  numerous  papers  have  since  appeared  indicating 
that  it  is  of  widespread  occurrence  among  kangaroo-like  marsupials.  Records  of  birth 
in  captive  female  marsupials  after  long  isolation  from  males,  such  as  those  reported  by 
Carson  (1912)  in  the  Red  Kangaroo  and,  recently,  by  Hediger  (1958)  in  Bennett's 
Wallaby,  are  readily  explained  in  terms  of  the  occurrence  of  delayed  implantation. 

I  am  indebted  to  Miss  Pat  Berger,  Mr.  John  Libke  and  Mr.  James  Merchant 
who  helped  with  animal  maintenance,  handling  and  watching.  The  interest,  assistance 
and  advice  on  the  manuscript  given  by  my  colleague  Mr.  J.  H.  Calaby  is  gratefully 
adtnowledged. 

Summary 

In  non-Iactating  female  Red  Kangaroos  the  oestrous  cycle  lasted  about  35  days  and  the 
gestation  period  was  about  33  days.  Gestation  did  not  interrupt  the  oestrous  cycle.  Postpartum 
oestrus,  at  which  copulation  and  fertilization  took  place  if  the  female  was  with  a  male, 
occurred  just  after  parturition.  Recurring  reproductive  cycles  were  replaced  by  the  quiescent 
phase  of  lactation  for  up  to  about  200  days  while  the  young  were  suckled  in  the  pouch.  If 
fertilization  occurred  at  postpartum  oestrus  a  dormant  blastocyst  was  carried  in  the  uterus 
during  the  quiescent  phase  of  lactation.  The  delayed  cycle  of  reproduction  during  whidi  the 
hitherto  dormant  blastocyst,  if  present,  completed  development  occurred  following  removal 
of  young  less  than  200  days  old  from  the  poudi.  If  the  young  were  retained  in  the  pouch 
until  they  emerged  in  the  normal  course  of  events  the  delayed  cycle  of  reproduction  occurred 
coincident  with  the  last  month  of  pouch  life  and  was  completed  a  day  or  two  after  the  young 
permanently  left  the  pouch.  Suckling  of  the  young  occupied  one  year:  they  were  suckled  for 
about  235  days  in  the  pouch  and  for  a  further  130  days  after  leaving  the  pouch.  The  delayed 
cycle  of  reproduction  could  thus  occur  during,  and  long  before  the  cessation  of,  lactation. 
Normal  cycles  of  reproduction  occurred  during  lactation  if  the  pouch  was  not  occupied. 

The  lengths  of  normal  and  delayed  cycles  of  reproduction  In  females  suckling  one  and  two 
young-at-foot  were  compared  with  those  In  control,  non-lactating,  females.  The  results  were 
as  follows: 

Normal  cycle  of  reproduction 

Females  suckling  one  young-at-foot.  Six  cycles  not  significantly  different  from  those  of 
controls;  two  cycles  significantly  longer  than  in  controls  in  one  of  which  a  dormant  phase  of 
about  7  days  occurred  In  the  embryo.  Total:  8  cycles. 

Females  suckling  two  young-at-foot.  Three  cycles  not  significantly  different  from  those  of 
control  females:  two  cycles  significantly  longer  than  In  control  females  which  Included  dor- 
mant periods  of  6  and  14  days  In  the  embryos.  Total:  5  cycles. 

Delayed  cycle  of  reproduction 

Females  suckling  one  young-at-foot.  No  effect  of  suckling.  Total:  5  cycles. 

Females  suckling  two  young-at-foot.  One  cycle  not  significantly  different  from  those  of 
control  females.  Five  cycles  longer  than  those  of  control  females  In  which  the  dormant  periods 
of  the  blastocysts  were  extended  by  3,  3,  6,  11  and  22  days.  In  the  two  latter  cycles  resumption 
of  development  of  the  dormant  blastocysts  did  not  occur  until  removal  of  one  of  the  suckling 
young-at-foot.  Total:  6  cycles. 

Observations  showed  that  females  with  two  young-at-foot  suckled  their  young  for  about 
twice  the  length  of  time  that  females  suckled  a  single  young-at-foot.  It  was  concluded  that 
the  suckling  stimulus  exerted  by  one  or  two  young-at-foot  could  Induce  and  maintain  the 
quiescent  phase  of  lactation  and  the  associated  dormant  phase  in  the  embryo.  Available 
evidence  suggested  that  the  stimulus  causing  onset  of  the  quiescent  phase  was  tactile  and 
received  via  the  teat  and  that  the  delayed  cycle  of  reproduction  occurred,  or  the  Interrupted 
normal  cycle  was  resumed,  when  the  suckling  stimulus  was  lessened. 

It  is  suggested  that  some  published  gestation  periods  of  marsupials  owe  their  error  to  the 
failure  of  observers  to  appreciate  the  significance  of  concurrent  suckling.  Reported  cases  of 
female  marsupials  giving  birth  after  long  isolation  from  males  can  readily  be  explained  as 
due  to  the  occurrence  of  the  delayed  cycle  of  reproduction. 


227 


Normal  and  delayed  cycles  of  reproduction  in  the  Red  Kangaroo  19 

Zusammenfassung 

Bel  nichtsaugenden  9$  ^^^  Roten  RIesenkanguruhs  dauert  der  Oestrus-Cyclus  rund 
35  Tage,  die  Triichtigkeit  rund  33  Tage.  Trachtigkeit  unterbricht  den  Cyclus  nicht.  Postpartum- 
Oestrus,  bei  dem  Begattung  und  Befruchtung  stattfanden,  erfolgten  unmittelbar  nach  der 
Geburt.  Wiederkehr  des  Oestrus  wurde  durch  eine  Latenz  wiihrend  der  Laktation  bis  zu  200 
Tagen  verhlndert,  wahrend  welcher  das  Junge  im  Beutel  gesaugt  wurde.  Wenn  beim  Postpar- 
tum-Oestrus  Befruchtung  erfolgt  war,  enthalt  der  Uterus  wahrend  dieser  Latenzperiode  eine 
ruhende  Blastocyste.  Der  verzogerte  Cyclus  der  Fortpflanzung,  wahrend  der  die  bisher  ruhende 
Blastocyste  (wenn  sie  vorhanden  ist)  ihre  Entwicklung  vollendet,  tritt  auf,  wenn  das  Junge 
friiher  als  200  Tage  nach  der  Geburt  aus  dem  Beutel  entfernt  wird.  Wenn  die  Jungen  jedoch 
so  lange  im  Beutel  bleiben,  bis  sie  ihn  normalerweise  verlassen  hatten,  fallt  der  verzogerte 
Cyclus  der  Fortpflanzung  mit  dem  letzten  Monat  des  Beutellebens  zusammen  und  ist  vollendet 
ein  oder  zwei  Tage  nachdem  die  Jungen  den  Beutel  endgiiltig  verlassen  haben.  Das  Saugen 
dauert  ein  voiles  Jahr:  die  Jungen  werden  rund  235  Tage  lang  im  Beutel  und  noch  weitere 
130  Tage  bei  Ful^  gesaugt. 

Der  verzogerte  Cyclus  der  Fortpflanzung  kann  also  wahrend  und  auch  lange  vor  Beendi- 
gung  der  Laktation  auftreten.  Normaler  Cyclus  der  Fortpflanzung  tritt  auf,  wenn  kein  Junges 
im  Beutel  ist.  Die  Lange  von  normalen  und  verzogerten  Cyclen  der  Fortpflanzung  bei  saugen- 
den  $9  rn'*^  einem  bzw.  zwei  Jungen  bei  Fuft  wurde  mit  solchen  bei  nicht  saugenden  KontroU- 
5$  verglichen.  Die  Ergebnisse  waren: 

Normaler  Cyclus  der  Fortpflanzung 

bei  9?)  ciis  1  Junges  bei  Fufi  saugten:  6  Cyclen  waren  nicht  besonders  verschieden  von  den 
Kontroll-$9-  Zwei  Cyclen  waren  bedeutend  langer;  bei  einem  davon  machte  der  Embryo  eine 
Ruhepause  von  etwa  7  Tagen  durch.  Im  ganzen  8  Cyclen. 

Bei  9$)  die  2  Junge  bei  Fufi  saugten:  3  Cyclen  nicht  besonders  verschieden  von  den  Kon- 
troll-99;  2  Cyclen  bedeutend  langer  als  bei  den  Kontroll-99  "^'^  Ruheperioden  des  Embryos 
von  6  und  14  Tagen.  Im  ganzen  5  Cyclen. 

Verzogerter  Cyclus  der  Fortpflanzung 

bei99>  die  ein  Junges  bei  Fufi  saugten,  ergab  sich  keinEinfluft  des  Saugens.  Im  ganzen  5  Cyclen. 

Bei  99>  <ii^  2  Junge  bei  Fufi  saugten,  war  1  Cyclus  nicht  sehr  verschieden  von  den  Kontroll- 
99-  5  Cyclen  waren  langer  als  bei  den  Kontroll-99>  bei  denen  die  Ruhezeit  der  Blastocyste 
resp.  3,  3,  6,  11  und  22  Tage  betrug.  In  letzteren  beiden  setzte  die  Weiterentwicklung  nicht  ein, 
bevor  nicht  eines  der  Jungen  weggenommen  wurde.  Im  ganzen  6  Cyclen. 

Die  Beobachtungen  zeigten,  dafi  9?  ^^^  2  Jungen  bei  Fufi  ihre  Jungen  doppelt  so  lange 
saugen,  wie  sie  ein  einziges  gesaugt  haben  wiirden.  Daraus  wurde  geschlossen,  dafi  der  Sauge- 
Stimulus,  von  einem  oder  zwei  Jungen  bei  Fui5  ausgelost,  sowohl  die  Ruhephase  wahrend  der 
Laktation,  als  auch  die  damit  gleichlaufende  Ruhephase  des  Embryos  einleitet  und  erhalt.  Die 
bisherige  Erfahrung  laEt  annehmen,  dafi  der  Stimulus,  der  den  Beginn  der  Ruhephase  bewirkt, 
tactil  ist  und  iiber  die  Zitze  empfangen  wird,  und  dafi  der  verzogerte  Cyclus  der  Fortpflanzung 
auftritt,  oder  der  unterbrochene  normale  Cyclus  wieder  aufgenommen  wird,  wenn  der  Sauge- 
reiz  sich  vermindert. 

Einige  von  anderer  Seite  veroffentlichte  Daten  iiber  Trachtigkeitsdauern  von  Beuteltieren 
enthalten  offenbar  Fehler,  da  die  betreffenden  Autoren  die  Bedeutung  gleichlaufenden  Saugens 
nicht  beachteten.  Mitgeteilte  Falle,  daf^  9  Beuteltiere  auch  nach  langer  Isolierung  vom  S  war- 
fen,  kann  ohne  weiteres  durch  das  Auftreten  des  verzogerten  Fortpflanzungs-Cyclus  erklart 
werden. 

Literature 

Carson,  R.  D.  (1912):  Retarded  development  in  a  red  kangaroo;  Proc.  zool.  Soc.  Lond.  1912, 
234-235.  —  Hartman,  C.  G.  (1923):  The  oestrous  cycle  in  the  opossum;  Am.  J.  Anat.  32, 
353-421.  —  FiEDiGER,  H.  (1958):  Verhalten  der  Beuteltiere  (Marsupialia);  Handbuch  Zool.  8, 
18  Lief  10(9),  1-28.  —  FiiLL,  J.  P.,  and  O'Donoghue,  C.  H.  (1913):  The  reproductive  cycle 
in  the  marsupial  Dasyurus  viverrinus.  Quart.  J.  micr.  Sci.  59,  133-174.  —  Hughes,  R.  L. 
(1962):  Reproduction  in  the  macropod  marsupial  Potorous  tridactylus  (Kerr);  Aust.  J.  Zool. 
10,  193-224.  —  Morris,  D.,  and  Jarvis,  C.  (Eds.)  (1959):  The  International  Zoo  Year  Book, 
Vol.  1;  London.  —  Owen,  R.  (1839-47):  Marsupialia;  In:  The  Cyclopaedia  of  Anatomy  and 
Physiology,  Vol.  3  (ed.  R.  B.  Todd),  London.  —  Pilton,  P.  E.,  and  Sharman,  G.  B.  (1962): 
Reproduction  in  the  marsupial  Trichosurus  vulpecula.  J.  Endocrin.  25,  119-136.  —  Sharman, 
G.  B.  (1954):  Reproduction  in  marsupials;  Nature,  Lond.  173,  302-303.  —  Sharman, 
G.  B.  (1955):  Studies  on  marsupial  reproduction.  3.  Normal  and  delayed  pregnancy  in  Setonix 
brachyurus;  Aust.  J.  Zool.  3,  56-70.  —  Sharman,  G.  B.  (1962):  The  initiation  and  maintenance 


228 


20  G.  B.  Sharman 

of  lactation  in  the  marsupial  Trichosurus  vulpecula;  J.  Endocrin.  25,  375-385.  —  Sharman, 
G.  B.  (1963):  Delayed  implantation  in  marsupials;  In:  Delayed  implantation  (ed.  A.  C.  En- 
ders),  Chicago.  —  Sharman,  G.  B.,  and  Calaby,  J.  H.  (1964):  Reproductive  behaviour  in 
the  red  kangaroo  in  captivity;  C.  S.  I.  R.  O.  Wildl.  Res.  9  (in  press).  —  Sharman,  G.  B.,  and 
PiLTON,  P.  E.  (1964):  The  life  history  and  reproduction  of  the  red  kangaroo  {Megaleia  rufa). 
Proc.  zool.  Soc.  Lond.  142  (in  press).  —  Tyndale-Biscoe,  C.  H.  (1963):  The  rule  of  the  corpus 
luteum  in  the  delayed  implantation  of  marsupials;  In:  Delayed  implantation  (ed.  A.  C.  Enders), 
Chicago. 

Author's  address:  Dr.  G.  B.  Sharman,  C.  S.  I.  R.  O.  Division  of  Wildlife  Research,  Canberra, 
A.  C.  T.,  Australia 


229 


REPRODUCTION  AND  GROWTH  IN  AAAINE  FISHERS' 

PHILIP   L.    WRIGHT,   Montana    Cooperafive   Wildlife    Research    Unit    and    Departnnent    of    Zoology,    University    of    Montana, 

Missoula 
MALCOLM  W.   COULTER,  Maine  Cooperative  Wildlife   Research   Unit,   University  of  Maine,   Orono 

Abstract:  New  data  concerning  reproduction,  aging  techniques,  and  growth  of  fishers  (Martes  pennanti) 
were  obtained  from  204  specimens  taken  from  October  to  April  during  1950-64.  All  female  fishers  more 
than  1  year  old  were  pregnant.  The  immature  class  consisted  of  juveniles  in  their  first  year.  The  period 
of  delayed  implantation  lasted  from  early  spring  until  mid-  or  late  winter.  Nine  adult  females  taken  in 
January,  February,  or  March  showed  implanted  embryos.  Fishers  in  active  pregnancy  had  corpora  lutea 
7  times  the  volume  of  those  in  the  period  of  delay.  Most  litters  are  bom  in  March,  but  some  as  early 
as  late  February  and  some  in  early  April.  Counts  of  corpora  lutea  of  54  animals  taken  during  the  period 
of  delay  and  during  active  pregnancy  averaged  3.35  per  female.  The  number  of  embryos,  either  un- 
implanted  or  implanted,  corresponded  exactly  with  the  number  of  corpora  lutea  in  18  of  21  animals. 
Two  recently  impregnated  1-year-old  females,  recognizable  from  cranial  characters,  had  tubal  morulae, 
confirming  that  females  breed  for  the  first  time  when  1  year  old.  Also  confirmed  are  previous  findings 
of  Eadie  and  Hamilton  that  juvenile  females  can  be  distinguished  from  adults  by  open  sutures  in  the 
skull  throughout  their  first  year.  Juvenile  males  can  be  recognized  in  early  fall  by  open  sutures  in  the 
skull,  absence  of  sagittal  crest,  immature  appearance  and  lighter  weight  of  bacula,  unfused  epiphyses 
in  the  long  bones,  and  small  body  size.  The  sagittal  crest  begins  to  develop  in  December  and  often 
is  well  developed  by  March.  The  baculum  grows  slowly  during  the  early  winter,  but  by  February  there 
was  some  overlap  with  weights  of  adult  bacula.  Male  fishers  showed  active  spermatogenesis  at  1  year. 
Open  sutures  were  found  in  juvenile  male  skulls  throughout  the  first  year.  Pelvic  girdles  of  juveniles 
were  distinguished  by  an  open  pubo-ischiac  symphysis;  adults  of  both  sexes  showed  the  two  innominates 
fused  into  a  single  bone  resulting  from  at  least  a  partial  obliteration  of  the  symphysis.  Mean  body  weights 
of  animals  weighed  whole  in  the  laboratory  were  as  follows:  adult  males,  10  lb  12  oz;  juvenile  males,  8 
lb  TV2  oz;  adult  females  5  lb  8  oz;  juvenile  females,  4  lb  11  oz. 


After  reaching  an  all-time  low  during  the 
early  part  of  the  century,  the  fisher  has 
made  a  remarkable  recovery  during  the 
past  25  or  30  years  in  Maine  (Coulter  1960) 
and  in  New  York  State  (Hamilton  and  Cook 
1955).    The  increase  in  abundance  of  this 


high  quality  furbearer  in  New  York  to  the 
point  that  it  could  be  legally  trapped  al- 
lowed Hamilton  and  Cook  ( 1955 )  and  later 
Eadie  and  Hamilton  ( 1958 )  to  discover  sig- 
nificant facts  from  studying  carcasses  ob- 
tained from  trappers. 


^  This  study  is  a  contribution  from  the  Maine 
and  the  Montana  Cooperative  Wildlife  Research 
Units,  the  University  of  Maine,  the  Maine  De- 
partment of  Inland  Fisheries  and  Game,  the  Uni- 
versity of  Montana,  the  Montana  Fish  and  Game 


Department,  the  U.  S.  Bureau  of  Sport  Fisheries 
and  Wildlife,  and  the  Wildlife  Management  In- 
stitute cooperating.  The  study  was  supported  by 
Grant  GB-3780  from  the  National  Science  Foun- 
dation. 


230 


Maine  Fishers  •  Wright  and  Coulter        71 


In  Maine,  the  season  was  reopened  in 
1950,  pennitting  collection  of  data  and  ma- 
terial from  fishers  trapped  there.  The  pur- 
pose of  the  present  paper  is  to  present  new 
information  about  reproduction,  age  de- 
termination, and  growth  of  fishers,  derived 
from  study  of  Maine  animals  obtained  be- 
tween 1950  and  1964. 

More  than  a  dozen  biologists  and  many 
wardens  of  the  Maine  Department  of  In- 
land Fisheries  and  Game  collected  material 
from  trappers.  Special  thanks  are  due  to 
Myron  Smart,  Biology  Aide,  who  assisted  in 
numerous  ways  throughout  the  entire  study, 
and  to  Maynard  Marsh,  Chief  Warden,  who 
made  arrangements  for  confiscated  speci- 
mens to  be  processed  at  the  Maine  Unit. 
Numerous  graduate  assistants  at  the  Maine 
Unit  helped  with  processing  carcasses  and 
the  preparation  of  skulls  and  bacula.  We 
are  indebted  to  Howard  L.  Mendall  for  edi- 
torial assistance  and  to  Virginia  Vincent 
and  Alden  Wright  who  made  the  statistical 
calculations.  Margaret  H.  Wright  did  the 
microtechnique  work.  Elsie  H.  Froeschner 
made  the  drawings.  Some  of  these  findings 
were  summarized  in  an  unpublished  Ph.D. 
dissertation  presented  by  Coulter  at  the 
State  University  College  of  Forestry  at 
Syracuse  University. 

FINDINGS  OF  PREVIOUS  WORKERS 

Hall  (1942:147)  pubHshed  data  from  fur 
farmers  in  British  Columbia  showing  that 
the  gestation  period  in  captive  fishers 
ranges  from  338  to  358  days  and  that  copu- 
lation normally  takes  place  about  a  week 
after  the  young  are  born.  Enders  and  Pear- 
son (1943)  described  the  blastocyst  of  the 
fisher  from  sectioned  uteri  of  trapper-caught 
animals  and  showed  that  the  long  gestation 
period  is  due  to  delayed  implantation.  It 
was  assumed  that  the  blastocysts  remain  in- 
active from  spring  until  sometime  during 
winter.    De  Vos  ( 1952 )   studied  fishers  in 


Ontario  and  made  preliminary  attempts  to 
establish  an  aging  method  based  upon  skulls 
of  males  and  females  and  the  bacula  of 
males.  Hamilton  and  Cook  ( 1955 )  pub- 
lished information  about  the  current  status 
of  fishers  in  New  York  State  and  described 
a  technique  for  recovering  the  unimplanted 
blastocysts  from  fresh  reproductive  tracts 
by  flushing  them  out  with  a  syringe.  Eadie 
and  Hamilton  (1958)  provided  additional 
data  on  the  numbers  of  blastocysts  in  preg- 
nant tracts  and  described  cranial  differ- 
ences between  adult  and  immature  females. 

MATERIALS  AND  METHODS 

Coulter  collected  material  in  Maine  from 
trapped  fishers,  starting  in  1950  when  the 
season  was  first  reopened.  The  intensity  of 
the  collection  varied  over  the  years  depend- 
ing upon  the  legal  regulations  in  effect. 
Data  are  available  from  204  animals. 

In  addition  to  animals  legally  taken  dur- 
ing the  trapping  season,  Coulter  obtained 
a  number  of  animals  both  before  and  after 
the  season,  taken  by  trappers  who  were 
trapping  other  species,  primarily  bears  and 
bobcats.  Trappers  who  caught  fishers  ac- 
cidentally were  required  to  turn  them  over 
to  the  Department  of  Inland  Fisheries  and 
Game  which  in  turn  brought  or  sent  them 
to  the  Maine  Unit  at  Orono  where  they 
were  autopsied  by  Coulter.  Unskinned  fish- 
ers as  well  as  skinned  carcasses  were  sub- 
mitted to  the  laboratory.  Whenever  possi- 
ble, weights  were  taken  immediately  before 
and  after  skinning  to  obtain  an  index  for 
converting  the  weights  of  carcasses  re- 
ceived from  trappers  to  whole  weights. 
During  the  trapping  season  carcasses  were 
collected  at  trappers'  homes.  Usually  the 
material  was  submitted  in  fresh  condition; 
often  it  was  frozen  or  thoroughly  chilled 
when  received  at  the  laboratory.  Because 
of  the  interest  of  the  cooperators,  most  of 
the  material  was  accompanied  by  collection 


231 


72        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


dates,  method  of  capture,  locality,  and  other 
notes.  These  data  together  with  measure- 
ments, weights,  observations  about  the  con- 
dition and  completeness  of  the  specimens, 
and  a  record  of  material  saved  for  future 
study  were  entered  on  individual  cards  for 
each  animal. 

A  special  effort  was  made  from  the  fall 
of  1955  to  the  spring  of  1958  to  obtain  com- 
plete skeletons,  and  59  such  specimens  were 
obtained.  Coulter  trapped  a  series  of  espe- 
cially needed  animals  in  late  March  and 
early  April,  1957.  Because  of  excellent  co- 
operation by  State  Game  Wardens  and  Re- 
gional Biologists,  a  good  sample  of  speci- 
mens was  available  for  study  over  a  6- 
month  period  from  October  to  April. 

This  series  of  fishers  is  an  unusually  valu- 
able one  for  discerning  important  aspects 
of  the  growth  and  the  reproductive  cycle  of 
this  mustelid.  For  example,  nine  females  in 
active  pregnancy  were  obtained,  as  well  as 
several  adult  males  in  full  spermatogenesis. 
Furthermore,  the  juvenile  fishers  were  grow- 
ing and  maturing  rapidly  during  the  col- 
lecting period,  and  this  fairly  large  collec- 
tion has  allowed  us  to  reach  significant  con- 
clusions concerning  the  onset  of  sexual  ma- 
turity and  the  distinction  between  the  age 
classes  with  more  assurance  than  de  Vos 
( 1952 )  was  able  to  do  with  more  limited 
material. 

The  reproductive  tracts  of  female  fishers 
were  removed  in  the  laboratory  and  pre- 
served in  10-percent  formalin,  in  AFA,  or 
in  special  cases,  Bouin's  fluid.  The  bacula 
of  all  the  males  were  air-dried,  as  were  the 
skulls  of  both  sexes.  Testes  from  a  few  rep- 
resentative males  were  fixed  in  formalin 
also.  Coulter  solicited  the  cooperation  of 
Wright  in  1955  and  all  of  the  material  then 
available  was  shipped  to  him  for  further 
analysis  and  for  histological  work.  Most  of 
the  skeletal  material  was  cleaned  by  der- 
mestid  beetles  in  Montana. 


This  study  was  carried  out  without  the 
aid  of  known-age  specimens.  Since  the 
study  was  completed,  three  known-age  ani- 
mals have  become  available:  an  18-month- 
old  female  in  Maine  which  was  in  captivity 
for  1  year,  and  two  females  captured  in 
central  British  Columbia,  released  in  west- 
ern Montana,  and  recaptured  6  years  later. 
Study  of  these  three  animals  in  no  way  af- 
fects the  findings  presented  in  this  paper. 
Evidence  is  presented  to  indicate  that 
young-of-the-year  animals  can  be  distin- 
guished from  adults  by  studying  either 
their  skulls  and  skeletons  or  their  reproduc- 
tive tracts.  Animals  judged  by  these  criteria 
to  be  less  than  1  year  old  are,  for  conve- 
nience, referred  to  as  juveniles  even  though 
in  a  few  cases  they  may  be  almost  1  year 
old.  Except  for  one  criterion  for  distinguish- 
ing yearUng  females  from  older  adult  fe- 
males, described  by  Eadie  and  Hamilton 
(1958:79-81)  and  confirmed  here,  no  method 
of  determining  the  relative  ages  of  adults 
was  discovered. 

Wherever  appropriate,  standard  devia- 
tions and  standard  errors  have  been  calcu- 
lated, but  generally  such  figures  are  not 
presented  here.  Wlien  it  is  stated  that  a 
significant  or  highly  significant  difference 
exists,  it  is  based  upon  the  use  of  the  t  test. 

FINDINGS 

Female  Reproductive  Tracts 

The  reproductive  tract  of  the  female  fisher 
is  similar  to  that  of  other  mustelids.  The 
ovaries  are  completely  encapsulated  with 
only  a  small  ostium  through  which  a  small 
portion  of  the  fimbria  extends.  The  ovary 
must  be  cut  free  from  the  bursa  under  a 
dissecting  scope  with  a  pair  of  fine  scissors. 
The  oviduct  encircles  the  ovary  as  in  other 
mustelids.  The  oviducts  were  not  highly 
enlarged  in  any  animals  studied,  since  no 
estrous  stages  were  seen.  The  uterus  has  a 
common  corpus  uteri  which  allows  embryos 


232 


Maine  Fishers  •  Wright  and  Coulter       73 


developing  in  one  horn  to  migrate  to  the 
other  horn.  The  uterine  horns  are  40-60  mm 
long  in  adult  females  in  inactive  pregnancy, 
and  2y2-4  mm  in  diameter.  Immature  fish- 
ers show  smaller  uteri  with  horns  about  30- 
40  mm  long  and  IV2-2V2  mm  in  diameter. 
No  search  was  made  for  an  os  clitoridis. 

The  ovaries  from  each  preserved  tract 
were  dissected  from  the  fixed  reproductive 
tract,  blotted,  and  weighed.  Each  ovary 
from  animals  taken  in  fall  or  early  winter 
was  sliced  macroscopically  and  the  number 
of  corpora  lutea  present  determined  by  the 
use  of  a  dissecting  microscope.  Of  the  77 
tracts  handled  in  this  way,  44  animals 
showed  corpora  and  were  thus  judged  to  be 
adults.  Thirty-three  animals  were  without 
corpora  and  were  judged  to  be  immature. 
The  average  combined  weights  of  the 
ovaries  was  134.4  mg  for  adults  and  76.5 
mg  for  immatures.  The  average  weight  of 
the  left  ovaries  ( I — 40.3  mg,  A— 70.0  mg ) 
was  greater  than  that  of  the  right  ovaries 
(1—36.2  mg,  A— 64.4  mg)  in  both  im- 
matures and  adults,  but  no  special  signifi- 
cance is  ascribed  to  this  matter.  The  aver- 
age number  of  corpora  lutea  from  this  series 
of  44  adult  females  was  1.68  in  the  right 
ovaries  and  1.60  in  the  left;  the  average  was 
3.28  per  adult  female.  Eadie  and  Hamilton 
(1958)  reported  that  the  mean  number  of 
corpora  lutea  in  23  adult  New  York  fishers 
was  2.72.  The  difference  in  the  average 
number  of  corpora  lutea  between  the  Maine 
and  New  York  samples  is  highly  significant. 
The  distribution  of  the  corpora  lutea  from 
all  of  the  Maine,  pregnant  animals  is  shown 
in  Table  1. 

To  determine  the  relationship  between 
the  number  of  corpora  lutea  in  the  ovaries 
and  the  number  of  blastocysts  in  the  uteri, 
11  tracts  of  adult  females  were  studied  in 
detail.  After  the  ovaries  were  removed  and 
sectioned  by  hand,  uteri  were  selected  that 
appeared  to  be  the  best  preserved.    These 


Table    1.      Distribution    of   corpora    lutea    in    ovaries    of    preg- 
nant Maine   fishers. 


No.  OF  Cor- 

No. OF 

pora  IN 

Corpora  in 

No.  OF 

Both  Ova- 

No. of 

Single 

Cases 

ries  of 

Females 

Ovaries 

Individual 
Females 

4 
3 
2 
1 
0 


2 
14 

42 

43 

8 

Total  109* 


5 
4 
3 
2 


1 
21 
30 

2 

54 


*  One  case  in  which  only  one  ovary  available. 

entire  uteri  were  dehydrated  and  cleared 
in  wintergreen  oil.  Study  of  the  entire 
cleared  tract  under  a  dissecting  scope  using 
transmitted  light  often  revealed  the  loca- 
tion of  blastocysts.  Serial  sections  of  each 
of  these  tracts  were  made  to  locate  the 
blastocysts.  As  soon  as  all  of  the  expected 
blastocysts  were  found,  no  further  section- 
ing of  that  tract  was  done.  In  some  cases 
the  entire  uterus  was  sectioned  before  all 
the  blastocysts  could  be  located,  and  in  2 
of  the  11  tracts,  1  potential  blastocyst  was 
not  found.  This  represents  a  loss  of  only  6 
percent,  as  there  were  35  corpora  in  the 
ovaries  of  the  11  animals  and  33  blastocysts 
were  located.  The  technique  of  Hamilton 
and  Cook  (1955:30-31)  of  flushing  the 
uteri  for  the  blastocysts  was  not  followed 
here  since  the  tracts  had  been  fixed  in  for- 
malin. 

The  sectioned  blastocysts  were  similar  to 
those  described  by  Enders  and  Pearson 
(1943:286).  The  extremely  thick  zona  pel- 
lucida,  14.4  /a  according  to  these  authors, 
makes  it  possible  to  find  the  blastocysts  in 
very  poorly  preserved  material.  None  of 
the  blastocysts  studied  was  in  better  condi- 
tion than  those  seen  by  Enders  and  Pearson, 
and  the  relative  numbers  of  nuclei  in  the 
trophoblast  and  the  inner  cell  mass  for  this 
species  is  still  not  known.    In  order  to  ob- 


233 


January,  1965 
February  2,  1961 

118 

77 

3 

1 

February  7,  1956 
February  21,  1964 
Late  February,  1959 
March  3,  1959 

182 

110 

98 

179 

98 

73 

108 

138 

3 

2 

1 
3 

0 

1 
3 

1 

March  11,  1965 

2 

1 

March  13,  1956 
March  20,  1957 

92 
121 

92 
137 

2 
1 

1 

2 

74        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


Table  2.     Findings  in   nine  reproductive  tracts  of  female  fishers   in   active   pregnancy. 

Weight  of  Distribution  of 

Date  Ovaries  (mg)         Corpora  Lutea  State  of 

Killed Uterus 

Right  Left  Right     Left 

3  embryos,   18   mm   CR    (Crown-Rump) 

4  embryos,  2R,  2L,  17-mm  swelhngs,  em- 
bryo 8  mm  CR 

3  embryos,  IR,  2L,  embryo  13  mm  CR 

3  embryos,  2R,  IL,  embryo  18  mm  CR 

4  embryos,  2R,  2L,  embryo  8  mm  CR 
4  fetuses,    2R,    2L,    2    males,    2    females, 

fetuses  53,  54,  55,  57  mm  CR 
3  fetuses,  2R,  IL,  3  males,  fetuses  69,  71, 

74  mm  CR 
3  early  embryos,  2R,  IL,  7-mm  swellings 
3  fetuses,  2R,   IL,  3  females,  fetuses  74, 

80,  83  mm  CR 

tain  such  material,  adult  tracts  would  have  young  before  the  end  of  February.  Two  re- 

to  be  preserved  in  a  matter  of  minutes  after  cently  captured  females  produced  litters  on 

the  animal  was  killed.  March  2  and  on  March  20  at  the  Maine 

Tracts  of  nine  adult  fishers  in  which  Unit.  The  evidence  indicates  that  the  ma- 
there  were  implanted  embryos  were  studied  jority  of  Maine  fishers  produce  their  litters 
(Table  2).  Studies  of  the  marten  and  a  during  the  month  of  March,  but  some  do  so 
weasel  are  of  some  value  in  estimating  the  as  early  as  mid-February,  and  some  as  late 
times  of  parturition  in  these  tracts.   Jonkel  as  early  April. 

and    Weckwerth     (1963:96-97)     made    a  The  ovaries  of  female  fishers  with  im- 

series  of  laparotomies  on  late-winter  adult  planted  embiyos  were  all  serially  sectioned, 

female  marten  ( Martes  americana )  and  de-  The  ovaries  are  much  larger  than  those  in 

termined  that  the  interval  between  implan-  inactive  pregnancy,  the  average  combined 

tation  and  parturition  was  less  than  28  days,  weight  being  231.9  mg  as  compared  with 

In  the  long-tailed  weasel  (Mustela  frenata),  134.4    mg    for    the    inactive    group.     The 

Wright  (1948)  showed  that  the  postimplan-  corpora    lutea    are    markedly    enlarged    in 

tation  period  lasted  about  23  or  24  days,  active  pregnancy  as  is  generally  known  in 

In  estimating  the  parturition  dates  from  the  mustelids  with  long  periods  of  delayed  im- 

pregnant  fisher  tracts  it  is  assumed  that  the  plantation  (Wright  1963:87).   The  corpora 

period  of  active  pregnancy  is  about  30  days,  of  three  of  these  animals  averaged  2,380, 

This  seems  reasonable  on  the  basis  of  the  2,917,   and  3,057   /x  in   diameter,   whereas 

larger  size  of  the  fisher  in  comparison  with  corpora  from  two  animals  with  unimplanted 

the  marten  and  the  weasel.  blastocysts  averaged  1,387  and  1,219  /x.  Al- 

The  female  fisher  with  the  largest  fetuses,  though  these  corpora  in  animals  with  im- 

taken  on  March  20,  would  probably  have  planted  embryos  are  more  than  seven  times 

borne  young  before  April  1.   The  one  with  the  volume  of  those  with  unimplanted  em- 

the  earliest  stages  was  taken  on  March  13,  bryos,  the  increased  size  of  the  ovaries  is 

and  it  is  estimated  that  her  litter  would  not  not  due  solely  to  the  increase  in  corpus  size, 

have  been  born  until  after  April  1.  The  one  In  no  case  is  the  histological  preservation 

with  the   13-mm    ( crown-rump )    embryos,  of  high  quality,  but  the  corpora  lutea  were 

taken  on  February  7,  would  have  borne  her  readily   seen   and   counted   in   all  ovaries. 


234 


Maine  Fishers  •  Wright  and  Coulter        75 


There  is  a  great  deal  of  interstitial  tissue  in  11  tracts  which  were  preserved  during  in- 
all  of  these  ovaries,  and  in  this  they  differ  active  pregnancy  and  which  were  sectioned 
from  weasel  ovaries  (Deanesly  1935:484)  in  to  locate  all  of  the  blastocysts, 
which  the  interstitial  tissue  is  most  active  On  a  few  occasions  at  the  time  of  au- 
in  late  summer  but  by  implantation  time  topsy,  Coulter  observed  darkened  areas  in 
shows  considerable  degeneration.  There  the  uteri  which  were  apparently  placental 
are  also  numerous  small  and  medium-sized  scars.  After  being  fixed  and  cleared,  most 
follicles  in  these  fisher  ovaries.  In  all  cases  of  these  areas  were  no  longer  visible, 
the  cells  of  the  corpora  lutea  are  highly  Wright  (1966:29)  found  that  in  the  badger 
vacuolated.  Vacuolated  cells  in  corpora  are  ( Taxidea  taxus )  placental  scars  can  readily 
common  in  many  mustelids  during  the  be  found  in  cleared  tracts  of  parous  fe- 
period  of  inactive  pregnancy.  Eadie  and  males,  provided  the  uteri  were  preserved  at 
Hamilton  (1958:78)  noted  that  their  fisher  once  after  death.  Placental  scars  are  diffi- 
corpora  in  ovaries  in  inactive  pregnancy  were  cult  to  find,  even  in  lactating  badgers,  in 
highly  vacuolated.  Wright  and  Rausch  material  that  is  not  freshly  preserved.  It 
(1955:348-350)  describe  vacuolated  corpora  seems  likely  that  the  general  level  of  preser- 
in  the  wolverine  {Gido  gulo)  in  inactive  preg-  vation  in  these  fisher  tracts  was  not  good 
nancy,  but  during  active  pregnancy  the  enough  to  preserve  placental  scars, 
vacuolation  had  disappeared.  It  appears 
then  that  vacuolated  corpora  lutea  during  Breeding  Season 

active  pregnancy  is  a  condition  not  com-  Earlier  workers,  Hall  (1942:147),  for 
monly  seen  in  this  group.  We  suppose  that  example,  indicate  that  the  female  fisher 
the  corpora  lutea  of  active  pregnancy  are  breeds  soon  after  her  litter  is  born;  thus 
secreting  progesterone,  whereas  during  the  the  gestation  period  may  be  as  long  as  51 
inactive  period  there  may  be  no  active  weeks.  Since  no  recently  postparturient 
secretion  of  progesterone.  This  is  suggested  tracts  were  available  for  study,  this  particu 
by  the  urine  analysis  conducted  in  various  lar  point  could  not  be  confirmed  from  wild- 
stages  of  pregnancy  by  Ruffie  et  al.  ( 1961 )  caught  animals.  However,  among  speci- 
on  the  European  badger  {Meles  meles)  mens  collected  in  late  March  and  early 
which  has  a  similar  reproductive  cycle.  April,  1957,  two  recently  bred  nulliparous 

The  number  of  embryos   or  fetuses   in  females  were  obtained  and  the  tracts  pre- 

these  eight  animals  averaged  3.38  and  in  served  fresh.  These  two  tracts  are  the  bes*- 

each  case  the  number  of  corpora  lutea  cor-  preserved  in  the  entire   series,   and  tuba 

responded  to  the  number  of  embryos;  that  embryos  were  found  in  each  by  serially  sec- 

is,  there  was  seen  here  no  loss  of  potential  tioning    the    oviducts.     Each    animal    had 

embryos  that  may  have   occurred   during  three  corpora  lutea,  2  R,  and  1  L,  and  3 

either  the  preimplantation   period   or  the  morulae  were  found  in  one  and  2  in  the 

postimplantation  period.  other.   In  the  one  taken  on  March  28,  one 

There  was  evidence  of  migration  of  em-  morula  had  about  228  nuclei  (Fig.  lA);  the 

bryos  from  one  uterine  horn  to  the  other  in  other  embr\'os  were  of  comparable  devel- 

five  of  the  eight  animals.  Migration  of  em-  opment,  but  it  was  not  possible  to  count 

bryos  is  well  known  in  other  mustelids.    It  the  nuclei. 

apparently  occurs  largely  during  the  process  The  animal  taken  on  April  4  showed  2 

of  spacing  just  before  implantation.    Only  morulae  with  12  and  20  nuclei  (Fig.  IB). 

one  example  of  migration  was  seen  in  all  No   evidence  was  found   of  the   expected 


235 


76        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


-^ 


m 


\h 


'■f 


:<V' 


Fig.  1.  Photomicrographs  of  tubal  morulae  from  recently  impregnated  female  fishers.  (Left)  Embryo  of  about  225  nuclei, 
from  1 -year-old  female  taken  on  March  28.  (Right)  Embryo  of  about  12  nuclei  from  oviduct  of  1 -year-old  female  taken 
on  April  4. 


third  embryo.  The  only  musteUd  possess- 
ing a  long  period  of  delay  in  implantation 
in  which  the  rate  of  cleavage  is  known  is 
the  long-tailed  weasel  (Wright  1948).  If 
the  fisher  has  a  comparable  slow  rate  of 
cleavage,  the  March  28  animal  was  impreg- 
nated about  March  18,  and  the  April  4 
specimen  was  impregnated  about  March 
27.  This  is  probably  about  the  same  time 
as  recently  parturient  females  would  be  im- 
pregnated. The  young  developing  from 
these  tubal  embryos  would  normally  have 
been  bom  about  1  year  later. 

The  ovaries  of  these  nulliparous  animals 
were  largely  masses  of  interstitial  tissue, 
apparently  of  cortical  origin.  There  were 
no  graafian  follicles  of  medium  or  large 
size.  The  small,  almost  fully  formed  corpora 
lutea  with  organized  connective  tissue  cen- 
ters also  suggested  that  ovulation  had  oc- 


curred some  8  or  10  days  earlier.  The  luteal 
cells  were  not  vacuolated.  The  medulla  of 
these  ovaries  was  discernible  only  as  a 
small  area  adjacent  to  the  mesovarium. 

Both  of  these  recently  bred  females,  even 
though  nulliparous,  showed  slight  mam- 
mary development.  In  weasels,  Wright  (Un- 
published data)  has  never  seen  mammary 
development  associated  with  the  summer 
breeding  season.  The  nipples  become  con- 
spicuous for  the  first  time  about  the  time 
of  implantation. 

Both  of  the  fishers  in  question  were 
judged  to  be  1  year  old,  on  the  basis  of  the 
development  of  both  their  skulls  and  skele- 
tons. Another  nulliparous  female  taken  at 
the  same  time,  March  27,  was  also  judged 
to  be  1  year  old,  but  showed  no  sign  of 
reaching  estrus.  This  animal  might  have 
attained  estrus  within  2  or  3  weeks. 


236 


Maine  Fishers  •  Wright  and  Coulter        77 


Table   3.      Findings    in    tracts   of   male   fishers    taken    in    late   winter  and  early  spring. 


Weight 

OK  Com- 

Paireu 

Status 

bined 

Paibed 

Epi- 

Status of 

OF 

Baculum 

Esti- 

Date 

Testes 

Testis 

didymis 

Sperm  in 

Sperm 

Weight 

mated 

Body 

(1957) 

AND  Epi- 

Weight 

Weight 

Testes 

IN  Epi- 

(mg) 

Age  of 

Weight 

didymides 

(G) 

(G) 

(G) 

didymides 

Animal 

January  5 

2.7 

1.8 

0.4 

None 

None 

1262 

Juv. 

7  lb     3 

oz 

February  26 

7.4 

5.6 

1.4 

Active 
spermato- 
genesis 

None 

? 

? 

? 

February  or 

early  March 

6.3 

4.8 

1.1 

None 

None 

1725 

Juv. 

10  lb     7 

oz 

March  1 

6.3 

4.8 

1.0 

Active 

spermato- 
genesis 

Few 

1252 

Juv. 

8  lb     5 

oz 

March  1 

8.6 

6.9 

1.3 

Abundant 

Abundant 

1550 

Juv. 

9  lb  12 

oz 

March  1-15 

10.3 

7.6 

1.9 

Abundant 

Abundant 

1562 

Adult 

March  17 

11.3 

8.6 

1.9 

Abundant 

Abundant 

1522 

Adult 

11  lb     5 

oz 

March  27 

7.4 

5.8 

1.2 

Abundant 

Abundant 

1921 

Adult 

8  lb     3 

oz 

March  27 

13.0 

9.8 

2.2 

Abundant 

Abundant 

2053 

Adult 

14  lb     6 

oz 

April  4 

9.0 

7.0 

1.7 

Abundant 

Abundant 

1800 

Adult 

9  lb     5 

oz 

Coulter  has  often  noticed  a  definite 
change  in  travel  pattern  beginning  in  March 
and  suspects  that  it  is  associated  with  breed- 
ing activities.  Earlier,  the  animals  are  fairly 
solitary  and  travel  in  long  routes  in  more 
or  less  direct  fashion.  But  during  March 
there  are  numerous  cases  of  animals  travel- 
ing together.  The  incidence  of  scent  posts 
is  much  higher  than  in  early  or  midwinter. 
At  this  season,  reports  are  received  of 
"dozens  of  fisher"  in  a  given  locality.  Closer 
study  shows  that  only  two  or  three  animals 
may  be  responsible  for  an  unbelievable 
maze  of  tracks  in  a  small  area. 

In  the  European  badger,  which  may  also 
have  a  gestation  period  of  almost  a  full 
year,  both  Neal  and  Harrison  (1958:115- 
116)  and  Canivenc  and  Bonnin-Laffargue 
(1963:121-122)  present  evidence  for  sterile 
matings  occurring  outside  of  the  usual 
breeding  season  and  ovulation  in  animals 
already  in  inactive  pregnancy.  Although  no 
fishers  were  obtained  during  the  period  ex- 
tending from  early  April  until  October,  it  is 
clear  from  the  material  at  hand  that  ovula- 
tion occurs  only  during  the  breeding  sea- 


son,  and  there  is  no   evidence   of   sterile 
matings. 

Male  Tracts 

Since  testes  were  generally  inactive  dur- 
ing the  trapping  season,  they  were  not 
routinely  saved  from  trapper-caught  speci- 
mens. With  a  breeding  season  in  March 
and  April,  it  was  obvious  that  late-winter 
animals  would  show  transitional  stages  from 
the  inactive  early-winter  condition  to  the 
active  state  in  the  breeding  season.  An  ef- 
fort was  made,  therefore,  in  the  late  winter 
of  1957  to  preserve  testes  from  available 
males.  The  results  of  the  observations  are 
included  in  Table  3. 

The  weights  of  the  combined  testes  and 
epididymides  were  obtained  after  first 
stripping  free  the  tunica  vaginalis.  Then 
the  testes  were  further  separated  from  the 
epididymides  and  both  were  weighed  again. 
Thus,  the  total  of  the  separated  weights 
does  not  equal  the  combined  weights  be- 
cause additional  connective  tissue  and  fat 
had  been  removed.  Representative  sections 
of  testes  from  each  animal  and  from  the 


237 


78        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


Fig.  2.  Dorsal  and  ventral  views  of  adult  and  juvenile  fisher  pelvic  girdles.  (A)  Dorsal  view  of  adult  $  showing  complete 
disappearance  of  the  symphysis  in  a  portion  of  the  anterior  half  of  pubo-ischioc  junction.  (B)  Ventral  view  of  adult  $ 
showing  almost  complete  disappearance  of  pubo-ischiac  symphysis.  There  are  conspicuous  rugosities  projecting  from  each 
side  of  the  symphyseal  line.  (C)  Dorsal  view  of  juvenile  9  showing  complete  separation  of  the  innominates  by  symphyseal 
cartilage.  (D)  Ventral  view  of  juvenile  $  in  which  the  two  innominates  are  completely  separated  by  a  substantial  symphys- 
eal cartilage. 


tail  of  the  epididymis  were  prepared  and 
stained. 

The  juvenile  male  taken  on  January  5 
was  aspermatic.  By  late  February  and  early 
March  three  juveniles  showed  somewhat 
enlarged  testes,  but  only  one  of  these  ani- 
mals was  in  breeding  condition.  All  of  the 
adults  taken  from  early  March  into  early 
April  were  fully  developed  with  abundant 
sperm  in  the  tails  of  the  epididymides.  It 
would  have  been  desirable  to  have  tracts 
from  additional  males  taken  earlier  in  the 
winter.  The  results  indicate,  however,  that 
adult  males  are  fully  active  sexually  during 
the  breeding  season;  and  the  young  males, 
now  just  1  year  old,  are  also  apparently  in 
breeding  condition. 

Skeletal  Development 

The  series  of  59  skeletons  was  studied 
with  respect  to  the  fusion  of  the  epiphyses 
in  each  of  the  long  bones  and  representa- 
tive vertebrae.    Sixteen  specific  sites  were 


studied  in  addition  to  the  status  of  fusion 
of  the  pubo-ischiac  symphysis  and  certain 
sutures  in  the  skulls. 

Examination  of  the  November  and  De- 
cember skeletons  showed  striking  differ- 
ences between  two  groups,  apparently  ju- 
veniles and  adults,  in  both  sexes.  All  of  the 
sutures  studied  were  open  in  November  and 
December  males  judged  to  be  juveniles;  and 
most  of  the  sutures  were  only  partly  closed 
in  comparable  females  thought  to  be  ju- 
veniles. The  obviously  juvenile  animals 
were  smaller  and  showed  many  open  sutures 
in  the  skulls.  The  bacula  of  the  males  in 
this  group  were  small  and  weighed  less  than 
1,000  mg,  compared  to  an  average  of  more 
than  2,000  mg  for  those  with  closed  sutures. 
The  ovaries  of  females  regarded  by  skeletal 
criteria  as  juveniles  were  all  without  corpora 
lutea;  the  ovaries  of  all  those  classed  as 
adults  possessed  corpora  lutea. 

The  pubo-ischiac  symphysis  clearly  re- 
mains open  longer  than  most  of  the  sutures. 


238 


Maine  Fishers  •  Wright  and  Coulter        79 


It  was  completely  open  in  all  animals  that 
were  regarded  as  less  than  1  year  old  taken 
throughout  the  fall,  winter,  and  early 
spring.  It  was  at  least  partially  obliterated, 
when  \iewed  either  dorsallv  or  ventrallv, 
in  all  animals  regarded  as  more  than  1  year 
of  age  (Fig.  2).  The  findings  of  striking 
differences  in  the  fusion  of  this  symphysis 
parallel  those  of  Taber  (1956),  who  de- 
scribed differences  in  this  symphysis  ex- 
tending over  several  years  in  deer  (Odo- 
coileus  herniontis  and  O.  virginianus) .  The 
pubo-ischiac  symphysis  should  be  studied 
in  other  mammals  in  which  aging  criteria 
are  needed. 

Baculum 

Weights  of  bacula  are  shown  in  Fig.  3, 
and  drawings  of  representative  types  are 
shown  in  Fig.  4.  The  bacula  of  adults  are 
more  than  100  mm  long,  and  they  com- 
monly weigh  2,000  mg  or  more.  The  fully 
mature  baculum  shows  an  elevated  ridge 
near  the  proximal  end  that  completely  en- 
circles the  bone  in  a  diagonal  line  when 
viewed  from  the  side.  The  bacula  of  ju- 
veniles taken  in  the  fall  and  early  winter 
are  much  smaller.  Although  they  show  the 
typical  splayed  tip  at  the  distal  end,  which 
is  universally  perforated  by  a  small,  round, 
or  oval  foramen,  they  do  not  show  the  en- 
larged proximal  end  typical  of  the  adults. 
The  series  of  bacula  in  Fig.  3  shows  that 
those  of  the  juveniles  are  growing  rapidly 
during  the  winter  months.  By  February 
some  of  them  weigh  as  much  as  1,600  mg 
(one  2,099  mg)  and  thus  overlap  the  weight 
of  those  of  adults.  Two  such  bacula  are 
shown  in  Fig.  4,  F  and  G.  Since  the  testes 
of  juveniles  in  February  were  becoming 
active,  it  seems  reasonable  to  assume  that 
such  animals  were  secreting  androgen  at 
high  levels. 

The  fully  adult  baculum  undoubtedly 
develops  under  the  influence  of  androgen. 


3000 


2800 


2600- 


2400- 


e>  2200- 


■  2000- 


UJ 

1600- 


1400 


1200- 


1000- 


800 


600- 


400 


•         • 


•      •         t 

o* 


o 


••  ^- 


•     • 


o 
o 
o 

o       o 
o 


OCT 


NOV 


T 


DEC 


JAN 


TT^rr 


MAR 


T 


APR 


Fig.  3.  Baculum  weights.  Adults  are  shown  in  solid  dots, 
juveniles  with  open  circles.  The  continued  growth  of  the 
juvenile  baculum  during  the  winter  months  is  clearly  shown 
as  is  the  overlap  in  weights  of  February,  March,  and  April 
juveniles  and  adults. 

as  it  probably  does  in  all  mustelids.  This 
was  demonstrated  (Wright  1950)  to  be  the 
case  in  the  long-tailed  weasel.  Probably  the 
fully  adult  type  of  baculum  would  develop 
by  late  spring  in  these  year-old  males,  since 
Deanesly  (1935:469)  concluded  that  the 
adult  baculum  of  the  European  stoat 
{Mustela  erminea)  develops  to  adult  type 
within  1  month  after  the  testes  become 
active  for  the  first  time.  Although  Elder 
(1951:44)  showed  that  bacula  may  continue 
to  develop  in  succeeding  years  in  sexually 
mature  mink  (Mustela  vison),  the  lack  of 
known-age  fishers  in  this  series  does  not 
make  such  conclusions  possible  here.  The 
tentative  conclusion  reached  by  de  Vos 
(1952),  that  bacula  were  not  of  value  in 
distinguishing  adult  from  juvenile  fishers, 
resulted  from  failure  to  recognize  changes 


239 


80        Journal  of  Wildlife  Managemeni,  Vol.  31,  No.  1,  January  1967 


240 


Maine  Fishers  •  Wright  and  Coulter        81 


in  the  rapidly  maturing  skulls  of  juvenile 
male  fishers  during  the  late  winter.  This 
will  be  discussed  further  in  a  later  section. 

Skulls 

The  specimens  were  placed  in  four 
groups  (adult  males,  juvenile  males,  adult 
females,  and  juvenile  females)  on  the  basis 
of  reproductive  condition  and  skeletal 
analysis,  and  12  measurements  were  taken 
of  each  skull  (see  Wright  1953:78-79). 
Means,  standard  errors,  and  coefficients  of 
variation  were  calculated  for  each  group. 
It  is  clear  from  study  of  these  statistics  that 
the  skulls  of  tlie  juvenile  animals  in  both 
sexes  have  not  reached  maximum  growth. 
In  many  cases  the  differences  between  the 
means  is  statistically  significant,  but,  be- 
cause of  overlap  between  the  measure- 
ments in  adults  and  juveniles,  it  is  not  pos- 
sible to  develop  aging  criteria  based  on 
measurement  of  a  single  skull  parameter, 
with  one  exception  to  be  discussed  later. 

The  differences  between  the  means  of 
these  measurements  was  generally  much 
greater  among  males  than  among  females. 
For  example,  the  mean  weight  of  adult 
male  skulls  was  70.6  g,  whereas  in  juvenile 
males  it  was  53.9  g,  a  difference  of  some 
20  percent.  In  female  skulls,  however,  the 
adults  average  32.1  g  and  the  juveniles  31.1 
g,  a  difference  of  only  3  percent. 

The  postorbital  constriction  becomes 
somewhat  smaller  with  increased  age  in 
both  sexes  of  fishers,  as  it  does  in  other 
mustehds.    Another  striking  difference  be- 


tween adult  and  juvenile  skulls  was  seen  in 
males  where  the  zygomatic  breadth  averages 
77.4  mm  in  adults  and  only  64.8  mm  in 
juveniles.  In  spite  of  this  18  percent  smaller 
measurement  in  juveniles,  there  is  overlap. 
It  is  not  possible  to  classify  a  male  fisher  as 
juvenile  or  adult  solely  on  the  basis  of  this 
measurement.  Tire  difference  in  zygomatic 
breadth  would,  in  most  cases,  produce  a 
broader  appearing  face  on  adult  males  than 
on  juvenile  males. 

The  sutures  in  the  skulls  of  fishers,  like 
those  of  all  other  mustelids,  tend  to  dis- 
appear at  a  relatively  young  age  (Marshall 
1951:278,  Greer  1957:322^23)  as  com- 
pared to  the  Ursidae,  for  example,  where 
they  persist  for  many  years  (Rausch  1961: 
86,  Marks  and  Erickson  1966:398).  Juvenile 
male  fishers  taken  in  early  fall  (Fig.  5A) 
show  almost  all  of  the  sutures  unfused,  but 
on  specimens  during  March  or  April  (Fig. 
5C)  almost  all  have  completely  disappeared. 
Eadie  and  Hamilton  (1958:77)  showed,  in 
New  York  fishers  from  which  they  had  re- 
productive tracts,  that  "All  breeding  fe- 
males showed  at  least  partial  fusion  of  the 
temporal  ridges  ...  to  form  a  sagittal  crest, 
and  [that]  the  maxillary-palatine  sutures 
were  completely  fused.  Non-breeding  fe- 
males showed  the  temporal  ridges  in  various 
degrees  of  separation  and  had  the  maxillary- 
palatine  sutures  at  least  partly  open.  It  is 
concluded  that  female  fisher  normally 
breed  at  the  age  of  one  year  in  the  wild, 
and  that  these  criteria  will  separate  young- 
of-the-year  from  adults." 


Fig.  4.  (A)  Lateral  view  of  skull  of  winter  juvenile  male,  February,  showing  well  developed  sagittal  crest  and  open  zygo- 
matic-maxillary  suture.  (B)  Lateral  view  of  skull  of  fully  adult  male  showing  typical  tremendously  developed  sagittal  crest 
and  disappearance  of  zygomatic-temporal  suture.  The  heavily  worn  teeth  shown  ore  not  necessorily  characteristic  of  adult 
fishers.  (C  to  J)  Bacula  of  male  fishers  showing  progressive  changes  with  age,  distal  end  to  the  top,  the  youngest  to  the 
left  and  oldest  to  the  right.  C,  D,  and  E  ore  from  juveniles,  C  taken  October  12,  D  taken  December  3,  E  taken  January  5. 
F  and  G  are  from  late  winter  juveniles  showing  progressive  changes  toward  the  adult  type  with  increased  deposition  of  bone 
at  the  basal  end.  Both  F  and  G  were  taken  in  February  or  early  March.  H,  I,  and  J  ore  selected  adult  bacula  showing  the 
characteristic  oblique  ridge  near  the  basal  end  and  generally  more  massive  appearance.  H  is  from  a  smaller-than-average 
male  (body  weight,  9  lb,  5  oz),  I  and  J  from  iarger-than-overoge  males  (I,  carcass  weight  10  lb;  J,  body  weight,  14  lb 
6  oz). 


241 


82        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


242 


Maine  Fishers  •  Wright  and  Coulter        83 


Our  findings  from  study  of  66  female 
fishers  from  Maine,  from  which  comparable 
data  were  available,  confirm  in  detail  the 
findings  of  Eadie  and  Hamilton  ( 1958 ) .  It 
is  also  clear  that  the  maxillary-palatine  su- 
ture is  among  the  last,  if  not  the  last,  to 
disappear. 

These  authors  also  describe  a  frequency 
distribution  in  the  length  of  the  sagittal 
crests  in  adult  females,  and  reference  to 
their  Fig.  3  shows  that  there  are  two  peaks 
of  sagittal  crest  lengths  which  they  tenta- 
tively regarded  as  representing  a  group  of 
iy2-year-old  females  and  another  group  of 
older  females.  When  we  plotted  our  data 
in  comparable  fashion,  the  line  exactly 
paralleled  theirs;  and  there  is  thus  further 
evidence  that  such  separation  into  young 
adults  and  older  adults  is  possible.  The 
distribution  of  the  lengths  of  the  sagittal 
crests  of  the  adult  Maine  female  fishers, 
plotted  in  the  same  fashion  as  did  Eadie 
and  Hamilton,  is  as  follows:  0-10,  1;  11-20, 
11;  21-30,  3;  31-40,  8;  41-50,  19;  51-60,  1. 

The  findings  in  the  skulls  and  skeletons 
of  the  two  recently  bred  nulliparous  fe- 
males, whose  reproductive  tracts  were  des- 
cribed in  an  earlier  section,  also  provide 
significant  evidence  that  the  onset  of  breed- 
ing in  female  fishers  occurs  when  they  are 
1  year  old.  In  each  case  there  was  no 
sagittal  crest,  and  the  maxillary-palatine 
suture  was  partially  open.  Eadie  and  Ham- 
ilton (1958:79)  found  this  suture  closed 
in  all  New  York  fishers  judged  to  be  adults. 
In  their  collection,  adult  fishers,  taken  en- 


tirely in  fall  and  winter,  would  have  been 
at  least  20  months  old,  whereas  our  two 
animals  were  almost  exactly  1  year  of  age. 
One  of  these  animals  shows  the  pubo- 
ischiac  symphysis  still  open;  the  other 
shows  it  partly  closed.  Further,  the  fact 
that  during  the  fall  and  winter  there  is  only 
one  type  of  skull  to  be  found  in  fishers  that 
have  not  bred  makes  it  virtually  certain 
that  wild  Maine  fishers  are  regularly  im- 
pregnated at  the  age  of  1  year  and  thus 
produce  their  first  litters  at  the  age  of  2 
years. 

The  sagittal  crests  of  adult  male  fishers 
are  extremely  well  developed  as  was  men- 
tioned by  Coues  (1877:65),  and  the  degree 
of  sexual  dimorphism  in  skulls  of  fishers  is 
greater  than  in  any  other  American  muste- 
lid.  All  adult  females  develop  sagittal 
crests,  but  even  the  most  highly  developed 
crests  in  females  are  almost  vestigial  com- 
pared with  those  of  adult  males.  It  is  natu- 
ral to  suspect  that  with  this  tremendous 
development  in  mature  males  the  crest 
might  begin  to  develop  earlier  in  juvenile 
males  than  in  females.  This  is  exactly  the 
case,  and  sagittal  crests  were  first  seen  in 
one  of  two  juvenile  males  taken  in  Decem- 
ber (Fig.  5B).  By  February,  March,  and 
April  the  crests  of  the  juvenile  class,  now 
almost  1  year  old,  are  well  developed  ( Fig. 
5C),  as  much  so  as  they  ever  become  in 
adult  females. 

In  the  female  fishers  it  is  clear  that  the 
sagittal  crest  develops  first  at  the  posterior 
end  of  the  skull  and  grows  progressively 


Fig.  5.  Dorsal  view  of  male  fisher  skulls  showing  characteristic  changes  associated  with  development.  (A)  Juvenile  mole, 
October  12,  showing  narrow  zygomatic  breadth,  all  sutures  in  nasal  region  clearly  open;  the  frontoparietal  sutures  are 
partly  fused.  The  poorly  developed  temporal  lines  are  wide  apart  and  thus  there  is  no  sagittal  crest.  (B)  Juvenile  male, 
December  3,  showing  disappearance  of  fronto-parietal  suture,  less  conspicuous  sutures  in  nasal  region,  and  characteristic  early 
development  of  sagittal  crest  running  throughout  the  middle  and  posterior  portions  of  the  cranium.  (C)  Juvenile  male  in  late 
winter,  February,  in  which  these  naso-maxillary  and  maxillary-frontal  sutures  are  barely  visible,  but  the  zygomatic-temporal 
sutures  are  still  very  distinct  and  the  sagittal  crest  is  better  developed.  (Same  skull  as  shown  in  Fig.  4A).  (D)  Skull  of  adult 
male  in  which  the  entire  dorsal  skull  is  ankylosed  into  a  single  unit;  no  suture  visible  except  for  faint  remains  of  posterior 
internasal  suture.  The  characteristic  highly  developed  keel-like  sagittal  crest  of  all  adult  males  is  clearly  shown.  (Same 
skull  as  shown  in  Fig.  4B). 


243 


84        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


forward  over  a  period  of  months  or  prob-  as  well  as  his  "juvenile"  class,  and  that  only 

ably  years.  In  the  male  fisher  the  temporal  the  animals   he   called   "old   adults"   were 

lines  move  rapidly  together  during  the  win-  adult  males  over  1  year  of  age. 

ter  months;   and  as   soon   as   the   crest  is  It  is   concluded,   therefore,   that   during 

formed,  it  mns  essentially  the  entire  length  the  early  winter,  adult  males  can  be  sepa- 

of  the  dorsal  region  from  the  postorbital  rated  from  juvenile  males   by   the  occur- 

constriction  to  the  inion,  a  distance  of  50-  rence  of  a  well  developed  sagittal  crest  on 

60   mm.     The    sagittal    crest    continues    to  adults;  but  by  mid-  or  late  winter  only  those 

develop  in  adult  males,  and  they  have  the  males  with  all  of  the  skull  sutures  closed 

crest  developed  to  the  extent  of  forming  a  are  adults, 
"thin,  laminar  ridge"  (Coues  1877:65).    It 

is  difficult  to  measure  the  extent  of  this  Body  Weights 

ridge    objectively;    but    since    it    extends  Both  de  Vos  (1952)  and  Hamilton  and 

posteriorly  in  fully  adult  males,  one  can  use  Cook  ( 1955 )  have  provided  body  weights 

the  method  employed  by  Wright  and  Rausch  of   wild-caught   fishers,    and   both   studies 

( 1955 )  on  wolverines  to  subtract  the  con-  show  that  males  often  weigh  twice  as  much 

dylobasal  length  from  the  greatest  length  as  females.   The  latter  indicate  an  average 

of  the  sk-ull.    This  is  one  accurate  method  weight  for  males  of  3,707  g  (8  lb  3  oz)  and 

of  showing  the  posterior  extension  of  this  2,057  g  (4  lb  9  oz)  for  females.    De  Vos's 

crest.  This  indirect  measurement  shows  no  figures  are  roughly  comparable.    In  both 

overlap   whatever   between   males    classed  studies  many  of  the  body  weights  were  esti- 

as  adults  and   those   classed   as  juveniles,  mated  from  carcass  weights  by  applying  a 

The  mean  for  the  former  group  is  11.9  mm  correction  factor  to  skinned  carcasses.  (Most 

and  for  the  latter,  3.9  mm  (see  Fig.  4,  A  fisher  specimens  coming  to  biologists  are 

and  B).   Thus  in  male  skulls  if  the  differ-  likely  to  be  carcasses  skinned  by  trappers.) 

ence  between   the  greatest  length  of  the  Hamilton    and    Cook    (1955:21-22)    state 

skull  and  the  condylobasal  length  is  6  or  that  the  fresh  carcasses  average  80  percent 

more  mm   (may  be  as  much  as  15  mm),  of  the  unskinned  weight.    In  the  present 

the  animal  is  an  adult;  if  it  is  less  than  6  study  many  fishers  were  confiscated  and 

mm,  the  animal  is  a  juvenile.  were  available  intact.    Thus,   it  was  pos- 

Another  reason  for  assuming  that  skulls  sible  to  obtain  a  sample  of  weights  taken 

of  males  with  immature  bacula,  but  with  directly  from  the  entire  unskinned  carcasses, 

sagittal  crests,  are  still  in  their  first  year  of  allowing   consideration   of   differences   be- 

life  is  provided  by  data  on  the  closure  of  tween  adult  and  juvenile  classes  in  both 

sutures  in  the  skull.    The  last  sutures  to  sexes. 

close  in  males  are  the  zygomatic-temporal,  Data  obtained  from  those  fishers  which 

the  naso-maxillary,  the  internasal,  and  the  were  weighed  entire  in  the  laboratory  are 

naso-frontal.   In  all  of  the  skulls  classed  as  shown  in  Table  4.  The  differences  between 

adult,  all  of  these  sutures  were  closed,  but  the  juveniles  and  adults  in  both  sexes  is 

in  every  male  skull  classed  as  juvenile,  all  highly   significant  although  there  is   some 

four  of  these  sutures  were  still  open  ( Figs,  overlap  in  each  case.  Furthermore,  juvenile 

4  and  5 ) .  males    are    significantly   heavier   than   the 

On  the  basis  of  this  evidence,  it  seems  adult  females.  The  available  mean  weights 

clear  to  us  that  males  classed  by  de  Vos  of  adults   are   probably  more   satisfactory 

(1952)  as  "adults"  were  in  effect  juveniles  than  those  of  the  juveniles.    Presumably, 


244 


Maine  Fishers  •  Wright  and  Coulter        85 


tlie  adults  were  no  longer  growing,  but 
the  ]u\eniles  were  growing  throughout  the 
collection  period  from  October  to  April. 
The  sample  is  not  large  enough  to  allow  a 
breakdown  \\ithin  the  juvenile  classes  b\" 
month,  but  the  smallest  juveniles  were 
taken  in  the  fall. 

The  fact  that  weights  of  the  juvenile 
males  are  21  percent  less  than  those  of  the 
adult  males,  while  the  weights  of  juvenile 
females  are  onh"  15  percent  less  than  those 
of  the  adult  females,  further  indicates  that 
juvenile  female  fishers  are  more  nearly  full 
grown  during  the  first  winter  of  life  than 
are  the  juvenile  males. 

In  man\-  cases,  the  fishers  that  were 
weighed  whole  were  also  weighed  after 
skinning.  This  allowed  detennination  of 
a  correction  factor.  Thirty-nine  animals 
were  weighed  both  before  and  after  skin- 
ning: 14  adult  males,  5  juvenile  males, 
8  adult  females,  and  12  juvenile  females. 
The  carcasses  averaged  81.9  percent  of 
the  whole  weight;  or,  stated  conversely, 
one  could  multiply  the  carcass  weight  by 
1.22  to  obtain  an  estimate  of  the  entire 
adult  weight.  This  latter  conversion  factor 
was  applied  to  those  animals  that  were 
weighed  only  after  being  skinned.  Esti- 
mated entire  body  weights  obtained  in 
this  fashion  were  comparable  for  both  adult 
and  juvenile  males,  but  weights  of  females 
were  significantly  below  the  weights  of 
those  females  weighed  entire.  For  this 
reason,  it  was  obvious  that  in  the  interval 
between  skinning  and  weighing,  many  of 
the  female  carcasses  had  lost  significant 
weight.  It  was  therefore  necessary  to  aban- 
don any  attempt  to  use  the  more  numerous 
carcass  weights  for  interpretation  of  pos- 
sible growth  rates  in  the  juveniles  or  other 
weight  changes  that  might  exist  between 
months. 


Table  4.     Body  weights  of  Maine  fishers  weighed  whole. 


-No.  Mean  Body  sf. 

Class  ok  Weight  in  Max.         Min. 

Ani-  (0UNt:ES)  oz 

MALS 


Adult  S        23         172.1         ±6.30     14-  6     7-4 

(10  lb  12  oz) 
Juv.  6  10         135.5         ±7.08     10-  8     6-8 

(8-71/2) 
Adult  9        13  88.2         ±3.61       7-11     4-  8 

(5-8) 
Juv.  9  17  75.0         ±2.35       6-  8     3-13 

(4-11) 

DISCUSSION 

Tliis  study  indicates  that  in  the  fisher  the 
adult  class  consists  of  all  animals  more  than 
1  year  of  age  and  that  all  animals  of  both 
sexes  less  than  1  year  are  sexually  imma- 
ture. Females  older  than  1  year  normally  are 
carrying  unimplanted  blastocysts  through- 
out the  year  except  during  active  preg- 
nancy in  late  winter.  The  fisher,  then, 
differs  from  all  other  American  mustelids 
studied  in  this  regard  except  the  wolverine. 
The  weasels,  Mustela  erminea  and  M. 
frenata,  are  similar  in  that  the  males  reach 
sexual  maturity  in  1  year;  but  the  females 
breed  during  their  first  summer  and  thus 
produce  young  at  the  age  of  1  year 
(Wright  1963:83-84).  In  the  marten,  males 
also  apparently  reach  sexual  maturity  in  1 
year,  but  females  may  not  breed  until  they 
are  2  years  old,  and  thus  two  year-classes 
of  immature  females  may  be  found  in  wild 
populations  (Jonkel  and  Weckwerth  1963: 
95-96).  This  has  made  further  refinement 
of  Marshall's  ( 1951 )  original  study  of 
marten  quite  difficult. 

In  the  female  otter  it  appears  that  sexual 
maturity  is  delayed  another  year  beyond 
that  in  the  fisher  and  that  there  are  two 
age-classes  of  immature  otters  (Hamilton 
and  Eadie  1964:245).  In  the  badger  the 
same  type  of  situation  prevails  as  in  the 
fisher  except  that  some  females  breed  pre- 
cociously  during   their   first   summer   and 


245 


86       Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


such  females  would  produce  litters  at  the 
age  of  1  year,  whereas  most  badgers  pro- 
duce their  first  litters  at  the  age  of  2  years 
(Wright  1966:42).  Only  in  the  wolverine 
{Gulo  gulo)  does  it  appear  that  a  repro- 
ductive cycle  like  that  of  the  fisher  is 
found;  but  owing  to  a  small  sample  of  ani- 
mals of  the  former  species,  the  matter  of 
age  at  sexual  maturity  is  somewhat  in 
doubt. 

The  recovery  of  the  marten  in  Maine  has 
been  much  slower  than  in  the  fisher 
(Coulter  1959)  although  both  species  orig- 
inally occurred  sympatrically  in  much  the 
same  habitat.  The  present  study  indicates 
that  the  potential  rate  of  reproduction  in 
the  fisher  is  higher  than  in  the  marten.  A 
large  sample  of  winter-caught  marten  is  not 
available  from  Maine,  but  such  material 
was  obtained  from  Montana.  Wright  ( 1963: 
79)  indicates  that  corpora  lutea  counts 
averaged  3.02  in  a  sample  of  44  trapper- 
caught  marten.  The  present  study  showed 
3.28  for  the  fisher.  Perhaps  of  greater  sig- 
nificance, though,  is  the  fact  that  some 
female  martens  (in  Glacier  National  Park) 
(Jonkel  and  Weckwerth  1963)  do  not 
produce  litters  for  the  first  time  until  they 
are  3  years  old. 

LITERATURE  CITED 

Canivenc,  R.,  and  M.  Bonnin-Laffargue.  1963. 
Inventory  of  problems  raised  by  the  delayed 
ova  implantation  in  the  European  badger 
{Meles  meles  L.).  Pp.  115-125.  In  A.  C. 
Enders  (Editor),  Delayed  implantation.  Uni- 
versity of  Chicago  Press,  Chicago,  Illinois. 
309pp. 

CouES,  E.  1877.  Fur-bearing  animals:  a  mono- 
graph of  North  American  mustelidae.  Dept. 
Interior,  Misc.  Pub.  8,  Washington,  D.  C. 
348pp. 

Coulter,  M.  W.  1959.  Some  recent  records  of 
martens  in  Maine.  Maine  Field  Naturahst 
15(2):50-53. 

.      1960.      The    status    and    distribution    of 

fisher  in  Maine.    J.  Mammal.  41(l):l-9. 

Deanesly,  Ruth.  1935.  The  reproductive  proc- 
esses of  certain  mammals.    Part  IX:   Growth 


and     reproduction     in     the     stoat     {Mustela 
erminea).    Philos.   Trans.   Roy.    Soc.   London 

225 (528): 459-492. 

de  Vos,  a.  1952.  Ecology  and  management  of 
fisher  and  marten  in  Ontario.  Ontario  Dept. 
Lands  and  Forests  Tech.  Bull.    90pp. 

Eadie,  W.  R.,  and  W.  J.  Hamilton,  Jr.  1958. 
Reproduction  in  the  fisher  in  New  York.  New 
York  Fish  and  Game  J.  5(l):77-83. 

Elder,  W.  H.  1951.  The  baculum  as  an  age 
criterion  in  mink.    J.  Mammal.  32(l):43-50. 

Enders,  R.  K.,  and  O.  P.  Pearson.  1943.  The 
blastocyst  of  the  fisher.  Anat.  Rec.  85(3): 
285-287. 

Greer,  K.  R.  1957.  Some  osteological  charac- 
ters of  known-age  ranch  minks.  J.  Mammal. 
38(3):319-330. 

Hall,  E.  R.  1942.  Gestation  period  in  the  fisher 
with  recommendations  for  the  animal's  pro- 
tection in  California.  California  Fish  and 
Game  28(3)  :143-147. 

Hamilton,  W.  J.,  Jr.,  and  A.  H.  Cook.     1955. 
The  biology  and  management  of  the  fisher  in 
New   York.     New    York    Fish    and    Game    J. 
2(l):13-35. 
-,  and  W.  R.  Eadie.     1964.     Reproduction 


in  the  otter  {Lutra  canadensis).  J.  Mammal. 
45(2):242-252. 

Jonkel,  C.  J.,  and  R.  P.  Weckwerth.  1963. 
Sexual  maturity  and  implantation  of  blasto- 
cysts in  the  wild  pine  marten.  J.  Wildl.  Mgmt. 
27(l):93-98. 

Marks,  S.  A.,  and  A.  W.  Erickson.  1966.  Age 
determination  in  the  black  bear.  J.  Wildl. 
Mgmt.  30(2):389-410. 

Marshall,  W.  H.  1951.  An  age  determination 
method  for  the  pine  marten.  J.  Wildl.  Mgmt. 
15(3):276-283. 

Neal,  E.  G.,  and  R.  J.  Harrison.  1958.  Re- 
production in  the  European  badger  {Meles 
meles  L.).  Trans.  Zool.  Soc.  London  29(2): 
67-130. 

Rausch,  R.  L.  1961.  Notes  on  the  black  bear, 
Ursus  americanus  Pallas,  in  Alaska,  with  par- 
ticular reference  to  dentition  and  growth, 
Z.  Saugetier.  26(2):77-107. 

RuFFiE,  A.,  M.  Bonnin-Laffargue,  and  R. 
Canivenc.  1961.  Les  taux  du  pregnandiol 
urinaire  au  cours  de  la  grossesse  chez  le 
Blaireau  europeen.  Meles  meles  L.  Comptes 
rendus  des  seances  de  la  Societe  de  Biologie 
155(4):759-761. 

Taber,  R.  D.  1956.  Characteristics  of  the  pelvic 
girdle  in  relation  to  sex  in  black-tailed  and 
white-tailed  deer.  California  Fish  and  Game 
42(1):15-21. 


246 


Maine  Fishers  •  Wright  and  Coulter        87 


Wright,  P.  L.  1948.  Preimplantation  stages  in 
the  long-tailed  weasel  ( Mustela  frenata ) . 
Anat.   Rec.   100(4):593-607. 

— .     1950.     Development  of  the  baculum  of 

the  long-tailed  weasel.  Proc.  Soc.  Expt.  Biol, 
and  Med.  75:820-822. 

.      1953.      Intergradation    between    Martes 

americana  and  Martes  caurina  in  western 
Montana.    J.  Mammal.  34(l):74-86. 

.     1963.     Variations  in  reproductive  cycles 

in  North  American  mustelids.  Pp.  77-97.  In 
A.  C.  Enders  (Editor),  Delayed  implantation. 


University  of  Chicago  Press,  Chicago,  Illinois. 
309pp. 

.     1966.     Observations  on  the  reproductive 

cycle  of  the  American  badger  {Taxidea  taxus). 
Pp.  27^5.  In  I.  W.  Rowlands,  Editor,  Com- 
parative biology  of  reproduction  in  mammals. 
Symposia  Zool.  Soc.  London,  No.  15.  Aca- 
demic Press,  London.    527pp. 

,  AND  R.  Rausch.     1955.     Reproduction  in 

the  wolverine,  Gulo  gulo.  J.  Mammal.  36(3): 
346-355. 

Received  for  publication  August  22,  1966. 


247 


GROWTH,  DEVELOPMENT,  AND  WING  LOADING 
IN  THE  EVENING  BAT,  NYCTICEIUS  HUMERALIS  (RAFINESQUE) 

Clyde  Jones 

Abstract. — Selected  aspects  of  growth  and  development  of  young  evening  bats 
are  presented  and  summarized.  In  addition,  information  on  wing  loading  and  de- 
velopment of  flight  in  known-age  animals  is  given.  Data  regarding  growth,  de- 
velopment, and  wing  loading  of  Nycticeius  humeralis  and  information  that  is 
available  for  some  other  species  of  bats  are  compared  and  discussed. 

Few  observations  have  been  made  previously  on  growth  and  development 
of  bats,  and  such  information  has  been  frequently  incidental  to  other  studies 
of  natural  history  or  reproduction.  Ryberg  (1947),  while  presenting  data  on 
parasites  and  natural  history  of  bats,  made  some  mention  of  growth  and  de- 
velopment of  young.  Considerable  information  on  growth  and  development 
of  two  North  American  bats  has  been  contributed  by  Pearson  et  al.  ( 1952 ) 
and  Orr  ( 1954 ) .  Some  observations  of  young  and  early  growth  and  develop- 
ment of  Nycticeius  humeralis  were  noted  by  Gates  (1941).  In  general,  re- 
production of  bats  has  been  summarized  by  Cockrum  ( 1955 )  and  Asdell 
(1964). 

To  my  knowledge,  no  information  has  been  made  available  with  regard  to 
wing  loading  of  Nycticeius  humeralis.  Vaughan  ( 1959 ) ,  while  presenting  data 
on  aerodynamic  considerations  of  three  species  of  bats,  provided  a  survey  of 
important  earlier  works.  More  recently,  limited  information  on  flight  of  some 
North  American  bats  has  been  contributed  by  Struh&aker  (1961),  Davis  and 
Cockrum  (1964),  Hayward  and  Davis  (1964),  Vaughan  (1966),  and  others. 

The  purpose  of  this  report  is  to  present  information  on  growth  and  develop- 
ment and  to  discuss  briefly  some  aspects  of  wing  loading  of  Nycticeius 
humeralis. 

Materials  and  Methods 

This  report  is  based  upon  observations  of  28  young  of  14  litters  born  in  captivity  to 
females  netted  at  Clear  Springs,  Homochitta  State  Park,  Franklin  County,  Mississippi. 
The  adults  were  captured  between  11:30  pm  and  4:30  am  on  9  and  10  May  1965. 

Pregnant  bats  were  weighed  periodically  prior  to  parturition;  following  birth  of  the 
young,  weights  and  measurements  of  all  bats  were  taken  regularly.  The  growth  and 
development  of  three  litters  were  followed  in  detail  and  the  animals  were  measured  daily. 
The  remaining  animals  were  measured  each  3-  or  5-day  period.  Because  the  bats  were 
not  anesthetized,  it  was  not  always  possible  to  obtain  relaxed  individuals  for  measuring. 

1 


248 


2  JOURNAL  OF  MAMMALOGY  Vol.  48,  No.  1 

As  a  result  of  these  methods,  some  discrepancies  in  the  measurements  of  individuals  from 
one  date  to  another  are  evident  in  the  data.  Measurements  that  were  taken  include  total 
length,  length  of  tail,  length  of  foot,  length  of  ear  from  notch,  length  of  forearm,  and 
length  of  fifth  finger.    All  measurements  were  taken  with  a  Vernier  caliper. 

At  regular  intervals  of  age  of  the  animals,  wings  were  outlined  for  the  analysis  of  surface 
areas  utilized  in  flight.  For  the  purposes  of  measuring  wing  loading,  I  have  followed 
the  assumption  of  Vaughan  (1959)  that  the  wings  extend  through  the  body  and  I 
have  computed  the  wing  loadings  in  lb  per  sq  ft. 

Pregnant  females  and  females  with  young  were  housed  in  one-quart  cardboard  cans 
with  screen  tops.  Following  the  weaning  of  the  young,  each  female  and  her  offspring 
were  housed  in  one-half  gallon  cardboard  cans  with  screen  tops.  Cardboard  cans  containing 
bats  were  stored  on  the  sides.  The  animals  were  maintained  at  room  temperatures  and 
provided  a  daily  diet  of  larvae  of  Tenebrio  molitor  and  water  with  Theragran  (Squibb 
Therapeutic  Formula  Vitamin)  added.  Feeding,  watering,  and  handling  of  the  bats  were 
started  at  about  the  same  time  every  day,  usually  between  3:30  and  5:30  pm. 

For  purposes  of  identification,  adult  bats  were  banded.  Young  animals  were  toe  clipped 
soon  after  birth,  but  were  banded  when  adult  size  was  attained. 

Some  animals  were  sacrificed  at  various  stages  of  development  and  then  cleared  and 
stained  or  were  preserved  either  in  fluid  or  as  dried  specimens. 

Results 

Birth  of  young. — The  females  gave  birth  to  the  young  within  15  to  26  days 
after  capture.  The  births  recorded  herein  occurred  on  25  May  (two  Htters), 
26  May  (one  Htter),  29  May  (two  Htters),  30  May  (five  htters),  31  May  (two 
htters),  2  June  (one  Htter),  and  4  June  (one  Htter).  Fourteen  adult  females 
gave  birth  to  12  females  and  16  males.  This  ratio  of  sexes  (0.75  to  1.00)  was 
similar  to  the  ratio  (0.736  to  1.00)  reported  by  Hooper  (1939).  AsdeH  (1964) 
reported  two  young  as  the  usual  number  per  litter  and  stated  that  birth  oc- 
curred in  late  May. 

All  births  observed  were  by  breech  presentation  and  the  times  recorded 
for  births  were  from  3  to  114  minutes.  With  the  exception  of  two  litters  that 
were  bom  at  about  9:00  and  10:45  am,  all  litters  were  dropped  between  1:00 
and  4:00  pm. 

During  parturition  all  females  moved  to  the  bottoms  of  the  containers. 
Females  ate  the  placentae  and  umbiHcal  cords  and  licked  the  young  very 
soon  after  birth.  Placentae  were  eaten  first,  then  umbilical  cords  were  eaten 
to  within  2  or  3  mm  of  the  naval  area.  Some  of  the  females  hung  head  up 
on  the  screening  of  the  containers  while  eating  the  placental  materials,  but 
then  turned  head  down  and  licked  the  young  thoroughly.  Placentae  and 
umbilical  cords  were  eaten  and  the  young  were  licked  usually  within  35  to 
70  minutes  after  delivery. 

In  every  case  observed,  the  young  found  and  grasped  the  nipples  of  the 
adult  within  a  short  time,  usually  5  to  8  min  following  birth.  The  young  were 
aided  often  by  the  adult  in  climbing  to  the  mammary  glands.  The  young 
were  oriented  in  the  same  direction  as  the  adult.  The  plagiopatagium  and 
uropatagium  of  the  female  enveloped  the  young.  The  young  bats  held  firmly 
to  the  nipples  of  the  females  and  had  to  be  removed  forcibly  for  measuring. 


249 


February  1967 

100      -1 


E 
E 


c 
o 


o 


90 


80 


70      - 


60 


■S       50 


40      - 


30 


20 


JONES— EVENING  BAT 


(' 


\\. 


1 1 1 1 1 1 1 1 1 1 

0   10   20   30  40   50  60  70  80  90   100 

Days 

Fig.  1. — Total  lengths   of  young   Nycticeius  humeralis.     Dots   represent   the   arithmetic 
means  and  lines  represent  the  ranges  of  measurements. 


250 


JOURNAL  OF  MAMMALOGY 


Vol.  48.  No.  1 


E 
E 


o 
o 


-I 


42 


38 


34 


30 


o   26 


22 


18   - 


14 


10 


(  ■ 
■  . 

lip 

1 

— I 1 1 1 1 1 \ \ 1 1 

0   10  20  30  40  50  60  70  80  90  100 

Days 

Fig.  2. — Tail  lengths  of  young  evening  bats.    Dots  represent  the  arithmetic  means  and 
lines  represent  the  ranges  of  measurements. 


251 


February  1967 


JONES— EVENING  BAT 


Table   1. — Correlation  of  age  and  various  aspects  of  growth   and  development 

of  young  evening  bats. 


<U    u. 

_>, 

Cfl 

*J 

1 

g 

5  -o 

O     >" 

.S   E 

c 
o 

0; 

a! 

"a 

_4; 

"H  '^ 

"a 

"gs 

1  •« 

c  1 

c 

5 

.5* 
'c 

S 

1^ 

o 

o 

1 

«  S 
II 

^   a 

1° 

1^ 

E  ii 

C 

Age  in 

a  * 
.So 

>> 

"0 

C 

2  2 

-1 

C3     O 

2  S 

4~>   ^ 

0 

weeks 

< 

£  o 

o 
n 

ol 

it'  "- 

^  % 

«   0 

1 

X 

X 

2 

X 

X 

X 

X 

3 

X 

X 

X 

X 

X 

X 

X 

4 

X 

X 

X 

5 

X 

6 

X 

X 

7 

X 

X 

8 

X 

9 

X 

In  addition,  the  feet  and  first  fingers  were  utilized  for  clinging  to  the  fur  of 
the  adults. 

'^kin  and  pelage. — Young  bats  examined  within  1  hr  after  birth  were  pink 
with  smooth,  soft  skin.  Vicera  were  seen  through  the  skin  of  the  abdomen. 
There  was  slight  dark  pigmentation  on  the  feet,  membranes,  tips  of  the  pinnae, 
and  lips.  Only  a  few  hairs  were  present  on  the  feet  and  on  the  dorsum  of  the 
head  and  shoulders.  Some  vibrissae  were  evident  on  the  swollen  glandular 
areas  of  the  lips. 

When  about  6  hr  old,  the  young  had  more  pigmentation  on  the  dorsal 
sides  of  the  back  and  head  than  at  birth.  Pigmentation  became  evident  on  the 
venter  at  approximately  18  hr  of  age.  Within  24  hr  the  dorsum  was  pigmented 
heavily  and  the  venter  was  pigmented  except  for  a  small  abdominal  area 
that  appeared  rather  opaque.  The  skin  was  very  wrinkled  and  had  the 
appearance  of  being  hard  and  dry,  but  was  soft  and  pliable  to  the  touch. 

In  the  2-day-old  young,  a  few  hairs  appeared  on  the  dorsum  at  the 
base  of  the  uropatagium.  The  hairs  and  vibrissae  on  the  feet  and  lips  were 
noticeably  stiffened. 

At  3  days  of  age  a  small  patch  of  hair  became  noticeable  on  the  dorsum  over 
the  scapulae. 

By  the  4th  day,  pelage  was  seen  on  the  dorsum  over  the  scapulae,  on  the 
rump,  and  along  the  flanks.  At  this  age,  fur  was  first  apparent  on  the  venter 
at  the  base  of  the  uropatagium  and  in  the  pectoral  region. 

At  5  days  of  age,  fur  was  present  on  the  dorsum  across  the  scapular  region 
to  the  flanks  and  extended  onto  the  rump.  At  this  time  the  fur  was  short, 
soft,  and  gray  in  color. 


252 


6 


JOURNAL  OF  MAMMALOGY 


Vol.  48,  No.  1 


E 

o 


a» 


42   1 


38   - 


34  - 


E 

E   30 


26   - 


^   22 


18   - 


14  - 


10 


_  1 


"T- 

10 


— T" 
20 


30 


T 


40 
Days 


50 


— 1 1 1 1 1 

60  70  80  90  100 


Fig.  3. — Forearm  lengths  of  young  Nycticeius  humeralis.    Dots  represent  the  arithmetic 
means  and  Hnes  represent  the  ranges  of  measurements. 


253 


February  1967  JONES— EVENING  BAT  7 

On  the  6th  day,  soft  gray  hairs  covered  most  of  the  dorsum,  and,  except 
for  a  bare  abdominal  region,  much  of  the  venter.   The  feet  were  well  furred. 

At  7  days  of  age,  the  hairs  on  the  dorsum,  in  the  scapular  region,  appeared 
longer  and  darker  than  the  rest  of  the  general  pelage. 

At  8  to  9  days  of  age,  the  young  were  furred  completely  with  grayish  black 
hairs  on  the  dorsum  with  long,  dark  fur  over  the  scapulae.  In  contrast  to  the 
dorsum,  the  venter  was  grayish  white  in  color. 

The  aforementioned  general  appearance  of  the  pelage  remained  until  the 
young  were  approximately  30  days  of  age.  At  this  time  the  hair  became 
burnished  slightly  with  brown  at  the  tips,  perhaps  due  to  wearing  of  the  ends 
of  the  hairs.  Young  bats  were  not  observed  to  undergo  molt  during  the  course 
of  this  study.  At  the  time  the  young  bats  reached  about  80  to  95  days  of  age, 
the  parent  females  molted;  the  pelages  of  young  and  adults  were  similar  in 
appearance. 

Eyes,  ears,  and  vocalization. — At  birth  the  lids  of  the  eyes  were  sealed,  but 
the  line  of  fusion  was  very  evident.  At  18  to  24  hr  following  birth,  the  eyes 
opened.  At  this  age,  the  young  would  jump  and  scamper  about  in  response 
to  the  flash  of  light  from  a  photographic  strobe. 

Young  examined  soon  after  birth  had  pinnae  that  were  folded  over.  When 
the  young  were  24  to  36  hr  old,  the  pinnae  were  unfolded  and  held  erect. 

The  young  bats  were  vocal  almost  immediately  after  birth.  The  utterances 
of  weak  "squeaks"  or  "chirps"  seemingly  were  continuous  for  about  10  days. 
After  this  time,  bats  made  vocal  sounds  only  when  disturbed  or  handled. 

Dentition. — The  complete  number  of  deciduous  teeth  in  young  Nijcticeiiis 
humeralis  is  expressed  by  the  formula  i  2/3,  c  1/1,  p  2/2  =  22.  Examination  of 
newly-born  young  revealed  that  all  of  the  deciduous  teeth  were  erupted  at 
birth.  The  deciduous  teeth  have  two  accessory  cusps,  one  on  either  side  of  the 
main  central  cusp.  In  general,  each  cusp  is  in  the  shape  of  a  hook  and  is 
curved  backward  and  inward  toward  the  mouth.  The  highest  degree  of 
development  of  curved,  hook-shaped  cusps  is  on  the  incisors.  The  cusps 
of  the  canines  are  hooked  noticeably,  but  some  premolars  have  relatively 
poorly  developed  accessory  cusps  that  appear  as  small  bumps  rather  than 
hooks.  Hooked  cusps  are  more  highly  developed  in  2-  and  7-day  old  young 
than  in  young  1  day  of  age. 

The  complete  number  of  permanent  teeth  is  expressed  by  the  formula 
i  1/3,  c  1/1,  p  1/2,  m  3/3  =  30.  In  specimens  of  young  2  days  old  that  were 
cleared  and  stained,  the  crowns  of  the  permanent  teeth  are  clearly  visible  in 
a  position  internal  to  the  deciduous  teeth.  In  specimens  of  young  7  days  old, 
the  permanent  canines  have  penetrated  through  the  gums  and  crowns  of  the 
other  teeth  are  seen  at  the  gum  line  just  beneath  the  surface.  In  the  order 
of  appearance  of  permanent  dentition,  the  canines  become  apparent  first,  fol- 
lowed in  eruption  by  the  incisors,  premolars,  and  molars.  At  4  weeks  of  age, 
the  permanent  teeth  are  generally  in  place;  the  third  molars  may  not  be  in 
place  fully,  but  the  crowns  are  apparent  well  above  the  gum  lines. 


254 


8 


JOURNAL  OF  MAMMALOGY 


Vol.  48,  No.  1 


42       -1 


38 


34     - 


30      - 


S     26 


^    22 

c 

-I 


8      - 


4      - 


O       O      00   o 


o 

°o      OcPo° 


o  °  o    o      oo  o 

o       °  o 

o  o 


o  o  •       *     •        _*' 

o  o        °  .••    •.•^*    •••^ 

o  •     ,         •         • 

o  •  •  • 

•    • 

o  -•  •• 


•         «•*••       .  ••         ^ 


o  o^ 


1 1 1 1 1 1 1 1 1 f 

0   10   20  30  40  50   60  70  80  90  100 


Days 

Fig.  4. — Forearm  lengths  of  known-age  evening  bats.  The  open  circles  represent  the 
arithmetic  means  of  measurements  for  females;  the  dots  represent  the  arithmetic  means  of 
measurements  for  males. 


255 


February  1967  JONES— EVENING  BAT  9 

Digits. — The  digits  of  the  hind  limb  were  separated  at  birth  and  the  claws 
were  well  developed  and  pigmented.  Young  bats  at  birth  had  feet  nearly 
equal  in  size  to  the  feet  of  adults. 

The  first  finger  of  the  forelimb  was  developed  very  well  at  birth  and  thumbs 
of  young  were  similar  in  size  to  thumbs  of  adults.  Measurements  of  the  length 
of  the  first  finger  of  young  and  adults  were  5.5  to  6.2  mm. 

The  remaining  digits  of  the  forelimb  were  developed  to  a  lesser  degree 
in  young  than  in  adults.  In  the  young  less  than  15  days  of  age,  the  distal 
portion  of  the  forelimb  was  less  developed  than  the  proximal  part  of  the 
wing;  digits  two  to  five  were  shorter  in  length  than  the  forearm.  In  adults, 
the  lengths  of  digits  two  to  five  were  18  to  61%  greater  than  the  length  of 
the  forearm. 

Flight  of  young. — In  an  attempt  to  determine  the  exact  age  when  the  young 
bats  could  fly,  four  young  were  thrown  into  the  air  each  day  when  the  adults 
were  fed;  four  young  and  adults  were  housed  in  containers  placed  on  a  shelf 
4.6  ft  from  the  floor  and  the  tops  of  the  containers  were  taken  off  at  feeding 
time;  the  remaining  young  and  adults  were  cared  for  in  the  manner  mentioned 
previously.  When  the  young  bats  10  to  14  days  of  age  were  thrown  into  the 
air,  the  wings  were  extended  and  fluttered,  but  the  animals  simply  fell  to 
the  floor,  sometimes  without  righting  themselves.  When  the  bats  were  15 
days  of  age,  the  fifth  fingers  were  flexed  and  the  bats  would  right  themselves 
and  then  glide  or  "parachute"  to  the  floor.  At  18  days  of  age,  bats  thrown  into 
the  air  flew  10  to  12  ft,  but  would  hit  a  wall  or  the  ceiling  and  flutter  down 
to  a  flat  surface  such  as  the  floor  or  a  desk  or  would  hang  head  up  on  a  wall. 
At  19  days  of  age,  one  young  bat  housed  on  the  aforementioned  shelf  emerged 
and  flew  across  the  room.  When  the  young  were  20  to  21  days  old,  they  were 
observed  to  negotiate  turns,  land,  and  hang  head  down  from  walls  and  ceilings 
of  the  room.  All  of  the  young  animals,  including  those  with  no  practice 
previously,  could  fly  short  distances  ( 10  to  12  ft)  at  21  days  of  age,  and  all  could 
fly  well,  turn,  and  land  head  down  on  the  walls  or  ceilings  at  23  days  of  age. 

All  observations  of  flight  were  made  in  a  room  that  measured  18  by  15  ft 
with  a  partial  comer  partition  separating  an  area  about  8  by  8  ft.  The  young 
bats  could  fly  and  avoid  obstacles  well  in  these  spaces. 

Behavior  of  young  and  adults. — The  young  evening  bats  seemed  weak  and 
uncoordinated  at  birth.  Although  the  babies  attached  themselves  firmly  to 
the  parent,  young  1  day  of  age  seemed  rather  helpless  when  separated  from 
the  adult.  At  1  day  of  age,  the  young  could  crawl  about  only  feebly  and 
were  unable  to  right  themselves  when  placed  on  the  dorsum  on  a  flat  surface. 

By  3  days  of  age  the  young  could  crawl  about  very  well  and  could  right 
themselves  quickly.  In  part,  these  abilities  may  be  a  reflection  of  the  afore- 
mentioned unfolding  of  the  pinnae  at  this  time. 

For  nearly  the  first  2  weeks  of  age  the  young  were  attached  to  the  nipples 
of  the  adults  almost  constantly  and  remained  enveloped  by  the  membranes  of 
the  adults.    With  the  exception  of  a  few  occasions  when  a  young  bat  was 


256 


10 


JOURNAL  OF  MAMMALOGY 


Vol.  48,  No.  1 


E 
E 


c 


42   n 


38   - 


34   - 


30 


26 


H-   22   - 


18   - 


14   - 


10 


\ 1 1 1 1 1 1 1 1 1 

0   10  20  30  40   50  60  70  80  90  100 

Days 

Fig.  5. — Fifth-finger  lengths  of  young  Nycticeius  humeralis.    Dots  represent  the  arith- 
metic means  and  hnes  represent  the  ranges  of  measurements. 


257 


February  1967 
42 


E 
E 


E 
E 


c 


o» 

o» 

c 

c 

0> 

a> 

_l 

-I 

II 

II 

o 

X 

38 


34 


E      ;;: 

k. 

a 

o       .ti 

^      ^      26 


14 


JONES— EVENING  BAT 


11 


E        30       - 


XX 


^x"**   X   X 


X  X 

XX      X 


,X    X 


xx 


v»        X    X 


X 

X        X 
X        X 


«    "X  0    ^°  0,  0   00    0     0    0 

X       °      °     0  <: 

X  .  0   00   0 


Cb%cPo%°<?o°%.o„° 

5    nr.    ^      O     r>  _  O    0       0-, 

00    0  ^0 


00      0 


X      0 


22      - 


8      - 


0    o°o°o 

O^x 
0 

0 

X 

0 


o 


x\ 


,t 


X 

ox 

IX 


1 1 1 1 1 1 1 1 1 1 

0   10   20  30  40  50  60  70  80  90  100 

Days 

Fig.  6. — Relationships  of  forearm  lengths  and  fifth-finger  lengths  of  Nycticeius  humeralis. 
Open  circles  represent  arithmetic  means  of  measurements  of  forearm  lengths;  crosses 
represent  arithmetic  means  of  measurements  of  fifth-finger  lengths. 

observed  uncovered,  the  young  did  not  leave  the  close  association  with  the 
parent  and  move  about  in  the  containers  until  about  3  weeks  of  age.  After 
this  time,  young  scampered  frequently  about  the  cages,  but  hung  adjacent 
to  the  female  when  at  rest. 


258 


12 


JOURNAL  OF  MAMMALOGY 


Vol.  48,  No.  1 


10     n 


9      - 


8      - 


6      - 


E 

o 

o> 
c     5 


4      - 


3      - 


2      - 


— I 1 1 1 1 \ 1 1 1 r 

0       10     20     30     40     50     60     70     80     90     100 

Days 

Fig.  7. — Weights  of  young  bats.    Dots  represent  the  arithmetic  means  and  lines  represent 
the  ranges  of  weights. 


259 


February  1967  JONES— EVENING  BAT  13 

Table  2. — The  relationships  of  wing  loading,  proportions  of  the  forearm  and  fifth  finger, 
and  total  body  weight  of  known-age  Nycticeius  humeralis. 


Age  in 

Weight 

Wing  loading 

Length  of  forearm/ 

Size  of 

days 

in  g 

in   Ib/sq  ft 

length  of  fifth  finger 

sample 

1 

2.0 

0.5365 

1.00 

11 

2 

2.2 

0.4067 

0.99 

11 

4 

2.6 

0.4523 

1.02 

7 

5 

2.8 

0.3765 

1.02 

8 

8 

3.0 

0.3300 

1.04 

11 

12 

3.4 

0.2500 

1.02 

19 

15 

3.8 

0.2500 

0.99 

23 

18 

4.2 

0.2433 

0.97 

23 

35 

5.2 

0.2375 

0.93 

23 

43 

5.6 

0.2220 

0.85 

22 

60 

6.2 

0.2079 

0.85 

19 

73 

7.1 

0.1921 

0.85 

19 

97 

8.4 

0.2261 

0.83 

5 

As  mentioned  previously,  the  young  were  highly  vocal  for  the  first  10  days 
following  birth,  but  then  made  vocal  sounds  only  when  disturbed  or  handled. 
During  these  observations,  the  adults  emitted  sounds  only  when  disturbed, 
handled,  or  sometimes  when  offered  food. 

Some  definite  specificities  of  adults  for  their  young  were  noted.  As  long 
as  the  young  bats  were  returned  to  the  same  nipples  from  which  they  were 
taken,  no  female  refused  to  accept  the  young  after  they  had  been  removed 
from  the  mother  and  measured  or  handled  otherwise.  On  several  occasions 
attempts  were  made  to  get  adult  females  to  accept  nursing  young  from  other 
females;  all  such  efforts  failed.  The  adults  would  bite  and  move  away  from 
the  strange  young.  One  young  bat  that  was  allowed  to  become  attached  to 
the  nipple  of  a  restrained  female  was  attacked  and  thrown  from  her  when 
the  adult  was  released.  This  same  adult  accepted  her  own  young  a  few 
minutes  later.  Litters  and  females  could  not  be  mixed  successfully  until  nursing 
ceased.  The  refusal  of  adult  females  to  accept  other  young  may  be  a  reflection 
of  the  manner  in  which  the  animals  were  maintained  in  relative  isolation 
from  other  young  and  adults.  Gates  ( 1941 )  reported  that  he  detected  no 
specificity  with  regard  to  nursing  young  and  adult  females  when  the  young 
and  adults  no  longer  remained  together  during  periods  of  feeding. 

The  young  first  showed  an  interest  in  food  and  water  at  approximately 
3  weeks  of  age,  when  they  appeared  to  smell  and  lick  items  of  food  ( portions 
of  mealworm  larvae)  held  before  them.  Early  interests  of  young  in  water 
included  considerable  licking  of  the  end  of  a  water-filled  dropper.  At  the 
age  of  4  weeks,  young  bats  were  taking  water  from  a  dropper  and  eating 
small  mealworms  that  were  presented  with  forceps. 

Throughout  the  course  of  this  study,  the  adults  were  given  mealworms 
from  forceps  and  water  was  administered  from  a  dropper.   In  only  two  cases 


260 


14 


JOURNAL  OF  MAMMALOGY 


Vol.  48,  No.  1 


14    -, 


12     - 


10    - 


i  8 


• 


6     - 


4    - 


2     - 


••  V*^* 


•  •• 


•v.\\.. 


•Art-^" 


•  % 


-• 


>v 


/ 


T 


T 


T 


T 


T 


T 


T 


— \ r 1 n 

20     10       0      10      20     30     40    50     60     70     80     90    100 

Days 

Fig.  8. — Weights  of  Nycticeius  humeralis.    Open  circles  represent  arithmetic  means  of 
weights  of  adults  and  dots  represent  the  arithmetic  means  of  weights  of  young. 

did  individuals  become  accustomed  to  picking  up  and  eating  mealworms 
that  were  not  presented  by  hand.  In  general,  the  bats  made  little  effort  to  fly 
or  move  about  while  being  fed  and  it  was  possible  to  feed  four  to  six  animals 
at  one  time.  One  adult  crawled  about  almost  continually  while  being  fed. 
The  young  reared  by  this  female  behaved  in  similar  fashion  during  the  periods 
of  feeding. 

Some  animals  began  eating  immediately  when  food  was  offered;  others 
simply  held  a  food  item  in  the  mouth  for  a  short  time.   During  this  time  the 


261 


February  1967 


JONES— EVENING  BAT 


15 


Flight 


Fig.  9. — Actual  outlines  of  a  wing  of  a  young  Nycticeius  htimeralis  of  known  age.  Wing 
outlines  were  made  when  the  bat  was  1,  2,  4,  5,  8,  12,  15,  18,  35,  43,  60,  73,  and  97 
days  of  age. 


animals  exhibited  considerable  shivering,  presumably  while  the  body  tem- 
perature was  increased. 

Growth. — Information  relating  to  growth  and  development  of  young  Nyc- 
ticeius humeralis  given  herein  is  based  upon  bats  bom  and  reared  in  captivity. 
No  malformations  of  any  kind  were  noted  and  all  animals  seemed  normal, 
but  it  is  possible  that  under  laboratory  conditions  the  rate  of  growth  and 
development  may  not  have  been  normal. 

Data  regarding  growth  and  development  of  young  bats  are  presented  in 
Tables  1  and  2  and  Figs.  1-9.  Because  the  length  of  the  first  finger  and 
length  of  foot  of  newborn  bats  were  noted  to  increase  little  between  birth 
and  adulthood,  those  measurements  are  not  depicted  graphically. 

At  45  to  50  days  of  age,  total  length,  length  of  tail,  and  length  of  fifth 
finger  of  young  bats  were  of  adult  proportions  and  little  growth  occurred 
thereafter  (Figs.  1,  2,  and  5).  Length  of  forearm,  on  the  other  hand,  was 
of  adult  proportions  when  the  bats  were  about  30  days  of  age  (Figs.  3  and  4) 
and  little  growth  occurred  at  later  ages.  Some  sexual  dimorphism  of  the 
length  of  the  forearm  was  noted  (Fig.  4).    The  smaller  size  of  the  forearm 


262 


16  JOURNAL  OF  MAMMALOGY  Vol.  48,  No.  1 

of  males  became  apparent  when  the  animals  were  about  20  days  of  age. 
Pearson,  Koford,  and  Pearson  ( 1952 )  found  a  similar  situation  in  their  studies 
of  growth  of  Plecofus  townsendii.  In  young  bats,  the  proportional  relation- 
ships of  the  length  of  the  forearm  and  the  length  of  the  fifth  finger  (Table  2 
and  Fig.  6)  are  correlated  with  flight  and  are  discussed  later  with  regard  to 
flight. 

\\'eights  of  young  bats  were  noted  to  increase  rather  constantly  throughout 
the  period  of  study  (Figs.  7  and  8).  Some  activities  of  the  bats,  such  as  the 
development  of  the  ability  for  flight  and  the  acceptance  of  mealworms  and 
water  are  reflected  in  the  weights  of  the  young.  The  gradual  cessation  of 
nursing  and  lactation  seemingly  is  reflected  more  vividly  in  the  weights  of 
the  adults  ( Fig.  8 )  than  in  the  weights  of  young  during  the  same  period  of  time. 

Growth,  de\elopment,  and  relative  surface  area  of  the  wings  of  bats  of 
known  ages  are  depicted  in  Fig.  9.  The  data  presented  indicate  a  gradual 
increase  in  surface  area  of  the  wing  with  the  development  of  a  wing  of  adult 
proportions  at  the  age  of  60  to  97  days;  surface  area  is  stabilized  with  the 
cessation  of  growth. 

At  the  age  when  young  bats  first  began  to  fly,  several  changes  in  the  wings 
were  apparent  for  the  first  time.  The  length  of  the  fifth  finger  was  greater 
than  the  length  of  the  forearm  (Table  2  and  Fig.  6)  and  the  distal  portion 
of  the  wing,  that  area  from  the  apex  of  the  wing  to  the  first  and  fifth  fingers, 
was  nearly  equal  in  surface  area  to  the  proximal  portion  of  the  wing,  that  region 
between  the  body  and  the  first  and  fifth  fingers  (Fig.  9).  In  addition,  there 
was  a  change  in  the  ratio  of  body  weight  to  surface  area  of  the  wing  ( Table  2 ) . 

Discussion 

Data  on  various  aspects  of  growth  and  development  of  some  species  of 
North  American  vespertilionids  have  been  presented  by  Pearson  et  al.  ( 1952 ) , 
Orr  (1954),  and  others.  The  availibility  of  these  data  permits  a  general  com- 
parison of  the  rates  of  growth  and  development  of  Nycticeius  humeralis  with 
those  of  Flecotus  townsendii  and  Antrozous  pallidus. 

The  development  of  fur  over  the  entire  body  of  young  evening  bats  was 
completed  by  8  to  9  days  of  age.  Short  gray  hair  covered  the  bodies  of  Plecotus 
4  days  old  and  scanty  fur  was  evident  on  the  bodies  of  Antrozous  at  10  days 
of  age. 

The  eyes  of  young  Nycticeius  were  opened  at  the  age  of  18  to  24  hr,  but 
eyes  of  young  Plecotus  and  Antrozous  were  not  opened  until  the  age  of  7  to 
10  days.  Pinnae  of  young  Nycticeius  were  erected  after  2  to  3  days  of  age; 
pinnae  of  the  two  other  species  were  erected  after  7  days  of  age.  Vocalization 
was  noted  almost  immediately  following  birth  of  Nycticeius  and  was  evident 
within  a  few  hours  after  birth  of  Plecotus. 

The  complete  set  of  deciduous  teeth  of  Nycticeius  was  present  at  birth 
and  these  teeth  were  grown  out  fully  by  7  days  of  age.  Orr  ( 1954 )  found 
the  deciduous  premolars  lacking  in  newborn  Antrozous,  but  noted  that  the 


263 


February  1967  JONES— EVENING  BAT  17 

deciduous  teeth  were  grown  out  fully  by  the  second  week  of  age.  In  Nycticeius, 
all  of  the  permanent  teeth  were  erupted  at  an  age  of  4  weeks,  and  in  Antrozous, 
permanent  teeth  were  erupted  at  an  age  of  5  weeks. 

The  forearm  in  young  Nycticeius  was  of  adult  proportions  at  30  days  of 
age,  but  the  forearm  in  young  Plecotus  reached  adult  size  at  21  days  of  age. 

Comparisons  of  the  rates  of  growth  and  development  of  the  young  of 
Nycticeius  humeralis,  Plecotus  townsendii,  and  Antrozous  pallidus,  indicate 
that  young  Nycticeius  exhibit  more  rapid  growth  and  development  and  are 
perhaps  more  precocious  than  young  of  the  other  species. 

On  the  basis  of  the  data  presented  in  this  report,  it  seems  that  young  Nyc- 
ticeius humeralis,  prior  to  18  days  of  age,  simply  lack  adequate  surface  areas 
of  wing  membranes  to  support  the  weight  of  the  body  in  flight.  For  informa- 
tion with  regard  to  surface  areas  of  flight  membranes  and  body  weights  of 
bats,  see  Vaughan  (1959  and  1966)  and  Struhsaker  (1961).  In  addition  to 
the  relationships  of  surface  areas  and  weights,  other  factors  of  growth  and 
development  must  have  considerable  bearing  on  the  abilities  of  young  bats 
to  fly.  For  example,  both  lift  and  power  for  flight  of  young  bats  must  be 
highly  dependent  upon  the  development  of  the  ventral  thoracic  flight  muscles 
as  well  as  development  of  the  musculature  of  the  entire  forehmb.  For  a 
discussion  of  surface  areas  of  flight  membranes  and  volumes  of  fhght  muscles 
in  relation  to  total  volumes  of  the  body,  see  Struhsaker  (1961),  and  for 
descriptions  and  discussions  of  flight  muscles,  see  Vaughan  (1959  and  1966). 
It  was  noted  that  after  the  forearm  of  the  bats  observed  during  this  study 
reached  maximum  length  ( at  about  30  days )  there  was  an  increase  in  diameter 
of  this  portion  of  the  forelimb.  This  increase  in  diameter  of  the  forearm 
was  noticed  especially  at  the  proximal  portion  and  was  due  apparently  to 
growth  and  development  of  the  muscles  that  are  located  in  this  region. 

Sexual  dimorphism  in  the  surface  area  of  wings  was  not  detected,  but  some 
dimorphism  in  the  length  of  the  forearm  was  noted  (Fig.  4).  The  slightly 
greater  length  of  the  forearm  in  females  implies  that  perhaps  females  may 
be  capable  of  supporting  a  slightly  greater  load  in  flight  than  males. 

At  18  to  21  days  of  age  when  young  bats  were  capable  of  flight  for  the 
first  time,  the  relationships  of  the  surface  areas  of  the  wings  to  the  total 
weights  of  the  animals  ( Table  2 )  perhaps  were  indicative  of  the  optimal  wing 
loading  for  flight  in  the  species  of  bat  considered  herein.  If  this  were  true, 
an  indication  of  maximum  weight-carrying  capacity  of  these  bats  could  be 
obtained  by  comparing  the  wing  loadings  of  bats  capable  of  first  flight 
with  wing  loadings  of  mature  animals.  It  is  of  interest  that  none  of  the  young 
bats  were  capable  of  flight  unless  the  wing  loading  was  less  than  0.250  lb 
per  sq  ft  (Table  2).  Young  bats  may  be  capable  of  flight  with  the  optimal 
wing  loading  for  the  species,  but  probably  would  lack  the  coordinations 
and  skills  of  flight  that  were  developed  in  the  adults,  thus  more  mature 
bats  probably  have  the  ability  to  carry  extra  weight  at  least  for  brief  periods 
of  time.    The  achievement  of  the  relationship  of  surface  area  versus  weight 


264 


18  JOURNAL  OF  MAMMALOGY  Vol.  48,  No.  1 

was  correlated  closely  with  the  relative  growth  rate  of  the  forearm  and  fifth 
finger  (Table  2  and  Fig.  6).  Wing  loading  of  adult  animals  (73  and  97  days 
of  age)  varied  from  0.1921  to  0.2261  lb  per  sq  ft.  On  the  basis  of  these  afore- 
mentioned data,  it  can  be  suggested  that,  allowing  for  reasonable  amounts 
of  variation,  adult  animals  with  a  weight  of  9  to  11  g  would  have  a  wing 
loading  not  far  removed  from  the  postulated  maximum  of  about  0.2500  lb  per 
sq  ft. 

According  to  Gates  (1941),  weight  of  two  females  prior  to  parturition  was 
11.6  g  each.  Some  of  the  females  observed  in  this  study  weighed  as  much 
as  14  g  (the  average  was  slightly  more  than  12  g)  prior  to  parturition,  but 
these  animals  were  kept  in  confined  situations.  At  the  time  of  capture,  20 
days  before  parturition,  average  weight  of  females  was  slightly  more  than  10  g 
(Fig.  8).  Because  weights  of  newborn  bats  recorded  during  this  study 
were  greater  than  weights  of  young  bats  given  by  Gates  (1941),  it  is  suggested 
that  the  young  and  females  kept  in  captivity  may  have  weighed  more,  due 
to  overfeeding,  than  animals  living  in  natural  conditions. 

Bats  have  been  reported  to  carry  various  weight  loads  in  addition  to  the 
normal  weight  of  the  body  (Davis  and  Cockrum,  1964).  The  weight  carrying 
capacity  of  individuals  of  any  given  species  of  bats  undoubtedly  is  important 
with  regard  to  the  relationships  between  adult  females  and  the  young,  and 
may  be  reflected  in  the  behavior  of  adults  prior  to  and  following  parturition. 
As  noted  earlier  in  this  report  ( Table  1 ) ,  young  Nycticeius  humeralis  remained 
associated  closely  with  the  parents  for  nearly  3  weeks.  This  relationship  may 
be  a  reflection  of  the  methods  of  housing  the  animals  during  these  observa- 
tions. Gates  ( 1941 )  suggested  that  the  young  remained  with  the  adult  for  less 
than  10  days  and  he  implied  that  this  is  a  reflection  of  the  weight  carrying 
capacity  of  the  adults.  Hamilton  (1943)  mentioned  that  nursing  female 
Nycticeius  probably  do  not  carry  the  young  while  foraging  for  food.  The  re- 
lationships of  weights,  surface  areas  of  flight  membranes,  and  related  abilities 
of  flight  of  the  animals  may  be  reflected  in  the  selection  of  sites  for  roosting 
by  adults  both  prior  to  and  following  birth  of  the  young. 

Acknowledgments 

Sincere  thanks  are  clue  Dan  Walton  and  Dr.  Francis  Rose  for  help  in  collecting  the 
original  material,  Dr.  Clyde  Barbour  for  the  preparation  of  photographs,  and  Glenn 
Clemmer  for  help  in  caring  for  the  animals.  This  study  could  not  have  been  conducted 
without  the  countless  hours  of  help  in  feeding  and  caring  for  the  animals  that  were  con- 
tributed by  Dr.  Francis  Rose  and  Charlene  Jones.  Dr.  Andrew  Arata  photographed  bats 
and  made  many  helpful  suggestions  throughout  this  study.  The  study  was  supported  in 
part  by  an  American  Cancer  Society  Grant  to  Tulane  University   (IN-24-G). 

Literature  Cited 

AsDELL,  S.     1964.     Patterns  of  mammalian  reproduction.    Comstock  Publishing  Associates, 

New  York,  2nd  ed.,  670  pp. 
Cockrum,   E.     1955.     Reproduction  in  North  American  bats.    Trans.   Kansas  Acad.   Sci., 

58:  487-511. 


265 


February  1967  JONES— EVENING  BAT  19 

Davis,  R.,  and  E.   Cockrum.      1964.     Experimentally  determined   weight   lifting   capacity 

in  individuals  of  five  species  of  western  bats.    J.  Mamm.,  45:   643-644. 
Gates,  W.      1941.     A  few  notes  on  the  evening  bat,  Nycticeius  humeralis   ( Raf inesque ) . 

J.  Mamm.,  22:  53-56. 
Hamilton,    W.     1943.     The   mammals    of   eastern    United    States.     Comstock    Publishing 

Company,  Inc.,  Ithaca,  New  York,  432  pp. 
Hayward,    B.,    and   R.    Davis.      1964.     Flight   speeds    in    western    bats.     J.    Mamm.,    45: 

236-242. 
Hooper,  E.     1939.     Notes  on  the  sex  ratio  in  Nycticeius  humeralis.    J.  Mamm.,  20:   369- 

370. 
Orr,   R.      1954.     Natural  history  of  the  pallid  bat,  Antrozous  pallidus    (LeConte).     Proc. 

California  Acad.  Sci.,  28:    165-246. 
Pearson,  O.,  M.  Koford,  and  A.  Pearson.     1952.     Reproduction  of  the  lump-nosed  bat 

(Corynorhinus  rafinesquei)    in  California.    J.   Mamm.,  33:   273-320. 
Ryberg,  O.     1947.     Studies  on  bats  and  bat  parasites.    Svensk  Natur,  Stockholm,  319  pp. 
Struhsaker,   T.     1961.     Morphological  factors  regulating   flight  in   bats.    J.   Mamm.,   42: 

152-159. 
Vaughan,  T.     1959.     Functional  morphology  of  three  bats:     Eumops,  Myotis,  Macrotus. 

Univ.  Kansas  Publ,  Mus.  Nat.  Hist.,  12:    1-153. 
.      1966.     Morphology    and    flight    characteristics    of    molossid    bats.     J.     Mamm., 

47:  249-260. 

Department  of  Biology,   Tulane  University,  New  Orleans,  Louisiana.    Accepted  28  No- 
vember 1966. 


266 


Growth,   1961,  25,   127-139. 

A  COMPARATIVE  STUDY  OF  GROWTH  AND  DEVELOPMENT 
OF  THE  KANGAROO  RATS,  DIPODOMYS  DESERTI 
STEPHENS  AND  DIPODOMYS  MERRIAMI  MEARNS 


Bernard  B.  Butterworth 


Department   of  Biology,   University   of   Wichita,   Wichita  8,  Kansas 


During  a  recent  study  of  sexual  behavior  and  reproduction  of  the 
kangaroo  rats,  Dipodomys  deserti  and  Dipodomys  merriami,  a  com- 
parison of  growth  and  development  of  closely  related  sympatric  species 
reared  under  identical  laboratory  conditions  was  possible.  Litters 
born  in  the  laboratory  were  carefully  examined  and  measured  from 
birth  to  maturity. 

Although  growth  in  other  genera  of  mammals  has  been  carefully 
studied,  few  instances  of  breeding  in  the  genus  Dipodomys  have  been 
recorded  and  limited  growth  data  are  available.  The  solitary  nature  of 
the  animals  prevents  laboratory  breeding  under  ordinary  conditions. 
Animals  confined  in  restricted  space  engage  in  fighting  which  usually 
results  in  the  death  of  one  or  both  of  them.  Chew  and  Butterworth  (3) 
published  an  analysis  of  growth  and  development  of  Merriam's  kanga- 
roo rat,  D.  merriami  in  which  the  senior  author  was  successful  in 
laboratory  breedings  of  this  species.  The  scattered  literature  on  growth 
and  development  in  the  genus  Dipodomys  is  summarized  in  their  paper. 

Materials  and  Methods 

A  total  of  32  laboratory  animals  representing  8  D.  deserti  litters  and 
4  D.  merriami  litters  that  were  the  direct  progeny  of  wild  parents  were 
used  in  this  study.  Seven  of  the  8  litters  of  D.  deserti  were  the  products 
of  laboratory  breedings,  the  first  recorded  instances  for  this  particular 
species.  The  other  litters  were  from  pregnant  females  captured  in  the 
field  and  brought  back  to  the  laboratory  for  observation  and  which 
subsequently  produced  young. 

The  parent  animals  were  all  obtained  from  one  locality  at  the 
western  edge  of  the  Mojave  Desert  near  the  base  of  Alpine  Butte 
located  approximately  16  miles  northeast  of  Palmdale  in  Los  Angeles 

127 


267 


128  GROWTH   AND    DEVELOPMENT    OF    KANGAROO   RATS 

County,  California.  The  altitude  of  the  collecting  area  was  approxi- 
mately 1000  meters  (3261  feet). 

The  captive  animals  were  placed  in  two  large  breeding  cages 
measuring  3  by  4  meters  at  the  University  of  Southern  California.  A 
partition  separated  the  two  cages  and  sand  and  desert  soil  up  to  several 
inches  in  depth  was  spread  on  the  floor.  Animals  were  allowed  to 
run  in  these  cages  without  restriction.  Nesting  sites  consisting  of  glass 
bottles,  empty  cardboard  mailing  tubes  and  cardboard  boxes  were  pro- 
vided. One  pair  of  each  species  was  placed  in  each  cage.  Instances 
of  breeding  in  D.  dcscrti  occurred  in  these  cages.  Animals  were  fed 
rolled  oats  and  sunflower  seeds.  Lettuce  was  provided  and  water  was 
also  made  available.  An  excess  amount  of  food  material  was  always 
available. 

All  animals  were  measured  from  birth  and  the  measurements  were 
continued  daily  or  at  frequent  intervals  until  adult  sizes  were  attained. 
Standard  measurements  of  total  length,  tail  length,  hind  foot  length, 
ear  (from  the  notch)  length,  and  body  weight  were  taken.  Measure- 
ments were  analyzed  as  in  Brody  (  2 )  and  values  were  plotted  on  a 
semilogarithmic  scale  against  age  on  the  arithmetic  scale.  Linear  seg- 
ments of  such  a  plot  indicate  periods  when  growth  increments  are 
constant  percentages  of  previous  sizes.  From  these  linear  sections 
instantaneous  growth  rates  were  calculated  as: 

T^         In  m_>  —  In  mi 
K  =  

The  value  of  K  is  the  instantaneous  percentage  rate  of  growth  for  the 
unit  of  time  in  which  tj  and  ti  are  expressed.  Ln  m^  and  In  mi  are 
natural  logarithms  of  the  measurements  made  at  ti  and  t2. 

Observations  and  Discussion 

General  Development.  The  general  pattern  of  development  in  D. 
deserti  is  similar  to  that  described  by  Chew  and  Butterworth  (3)  for 
D.  merriami.  The  desert  kangaroo  rat  is  born  hairless  and  has  a  thin, 
pink,  wrinkled,  transparent  integument.  Viscera  are  apparent  through 
the  skin  of  the  venter  and  sutures  and  blood  vessels  on  the  skull  are 
visible.  The  snout  area  containing  the  vibrissa  sheaths  appear  to  be 
swollen  and  are  richly  vascular.  The  yellowish-brown  vibrissae  are 
about  6  millimeters  long  at  birth,  but  lengthen  to  13  mm.  in  5  days  and 


268 


BERNARD  B.  BUTTERWORTH  129 

23  mm.  by  15  days.  The  adult  length  of  72  mm.  is  attained  by  90 
days. 

Black  pigmentation  appears  about  5  days  after  birth.  The  pigmenta- 
tion begins  on  the  dorsum  and  top  of  the  head.  A  faint  dorsal  tail 
stripe  is  present.  The  end  of  the  tail  is  unpigmented  for  10  mm.  and 
then  a  black  ring  circles  the  entire  tail  for  about  7  mm.  The  black 
area  extends  on  the  dorsal  side  of  the  tail  for  about  30  mm.  and  shades 
out  to  a  pale  gray  color.  The  entire  ventral  surface  of  the  tail  is  white 
except  for  the  small  black  area  near  the  tip.  The  feet  and  venter  are 
white.  The  site  of  the  dermal  gland  shows  as  a  light  depression  just 
posterior  to  the  scapulae.  It  darkens  by  15  days,  begins  to  lighten  by 
19  days  and  is  covered  with  hair  by  21  days.  The  head  is  sufficiently 
pigmented  by  7  days  so  that  the  dorsal  cranial  sutures  and  blood 
vessels  are  no  longer  visible.  By  21  days  the  mammae  have  become 
very  distinct.  The  insides  of  the  thighs  and  the  venter,  in  general,  are 
sparsely  haired  until  about  15  days.  By  21  days  the  animal  is  fully 
furred  and  the  color  pattern  of  the  young  is  now  similar  to  that  of  the 
adult.    The  young  appear  darker  than  the  parents,  however. 

The  pelage  of  D.  merriami  is  a  darker  yellowish-buff  than  that  of 
D.  deserti,  the  white  tail  stripe  is  wider  than  the  dark  tail  stripe,  and 
the  terminal  tuft  is  brown.  Dark  whisker  patches  are  distinct  in  D. 
merriami  but  are  absent  in  D.  deserti.  Juvenile  D.  merriami  are  com- 
pletely furred  by  15  days.  Developmental  stages  are  shown  in  Figures 
1  to  6. 

The  pinnae  of  the  ears,  closed  at  birth,  and  only  two  mm.  in  length 
gradually  open  from  9  to  15  days.  The  length  of  time  until  opening 
varies  with  different  litters.  The  ears  are  fully  opened  by  15  days  in 
D.  deserti  and  by  10  days  in  D.  merriami. 

The  nails  are  soft  at  birth  and  gradually  become  hard  by  15  days  in 
both  species. 

The  incisor  teeth  appear  later  in  D.  deserti  than  in  D.  merriami. 
They  break  through  the  gums  at  about  2  days  in  the  latter  ( Chew  and 
Butterworth,  3 )  while  they  do  not  appear  until  about  9  days  in  the 
former.  Teeth  are  white  at  first  but  gradually  darken  to  yellow.  By 
25  days  the  teeth  of  D.  deserti  are  strong  enough  to  pierce  the  skin  of 
man. 

Eye  development  is  summarized  in  Figure  7  for  various  species  of 
kangaroo  rats.  In  my  laboratory,  individuals  of  D.  deserti  had  their 
eyes  open  as  follows:  3  on  the  15th  day;  3  on  the  16th  day  and  6  on 


269 


130 


GROWTH   AND   DEVELOPMENT    OF    KANGAROO    RATS 


FIGURE   1 

Dipodomys   deserti,  3   days   old.    Note   absence   of   hair   and   the   relative   sizes   of   the 
feet.    Both  eves  and  ears  are  tightly  closed. 

FIGURE  2 
Dipodoiuvs   uien-iaini,   a    mother   nursins   her   voung. 
FIGURE  3 
Dipodomys  deserti,   10  days   old.   A   litter   of   5.    Note   the   white   tail   tip,   one   of   the 
distinguishing  features  of  this  species. 

FIGURE  4 

Dipodonivs  uierriami,  11  davs  old.    A  litter  of  3. 

FIGURE  5 

Dipodomvs  deserti,   16  davs  old.    From  the  same  litter  as  pictured  in  Figure  3. 

FIGURE  6 
Dipodomys  merriami,  16  days  old 


270 


BERNARD   B.    BUTTERWORTH 


131 


the  17th  day.   D.  merriami  had  their  eyes  open  between  the  11th  and 
15th  days. 


Davs  after  birth 

Species 

that  e\es  open 

Reference 

Dipodomvs  deserti 

15-17 

Butterworth 

D.  deserti 

16 

Rush   (8) 

D.  merriami 

11 

Butterworth 

D.  merriami 

11-15 

Chew  and   Butterworth    (3) 

D.  merriami 

21 

Do  ran   (5) 

D.  merriami 

by   third  week 

Reynolds   (7) 

D.  heermanni 

12-15 

Fitch   (6) 

D    heermanni 

14-16 

Tappe   (9) 

D.  nit  rat  aides 

13-14 

Culbertson   (4) 

D.  spectabilis 

14 

Bailey   (1) 

FIGURE  7 
Eye  development   in   various  species  of  kangaroo   rats. 

A  comparison  of  general  development  in  the  two  species  in  this 
study  is  shown  in  Figure  8. 


Eyes  open 

Ears  open 

Incisor  teeth  erupt 

Solid   food   eaten 

Solid  feces  first  noted 

Nails  harden 

Sand  used  for  cleaning  pelage 

Well  haired 

Weaned 

Mammae  first  visible 

Drumming  with  feet  first  noted 


Days 

after 

birth 

D.  deserti 

[ 

D. 

merriarni 

11-17 

11-15 

9-15 

8-10 

7-10 

2-8 

15 

13 

15 

17 

12-15 

12-15 

17 

13-15 

11-15 

14 

15-25 

17-22 

21 

11 

35 



FIGURE  8 
Comparison  of  sequences  of  general  development  of  Dipodomys  deserti  and  Dipodomys 
merriami.    Selected  features  based  on  8  Utters  of  D.  deserti  and  4  litters  of  D.  merriami. 

Growth  Analyses:  A  comparison  of  weight  increases  in  D.  deserti  and 
D.  merriami  is  shown  in  Figures  9  and  10.  Weights  become  constant 
at  adult  levels  of  approximately  145  grams  in  D.  deserti  and  40  grams 
in  D.  merriami.  An  analysis  indicates  that  early  growth  is  rapid  in 
D.  merriami  and  continues  more  slowly  toward  the  maximum  weight. 
At  10  days  D.  deserti  had  reached  16  per  cent  of  its  total  adult  weight 
while  D.  merriami  had  attained  26  per  cent  of  its  adult  weight.  At  30 
days  the  two  species  had  reached  approximately  half  their  maximum 
weight,  47  per  cent  in  D.  deserti  and  53  per  cent  in  D.  merriami.   At 


271 


132  GROWTH   AND   DEVELOPMENT    OF    KANGAROO   RATS 


15 

days 

20 

days 

30  days 

50 

days 

90 

days 

D.d. 

D.m. 

D.d. 

D.m. 

D.d.   D.m. 

D.d. 

D.m. 

D.d. 

D.m. 

Total  length 

47 

54 

55 

70 

72     80 

83 

95 

97 

99 

Tail  length 

39 

47 

50 

61 

73     81 

91 

97 

93 

99 

Foot  length 

70 

82 

80 

87 

82     95 

96 

99 

100 

100 

Ear  length 

63 

63 

67 

82 

78     90 

81 

95 

88 

99 

Weight 

27 

35 

33 

43 

47     53 

75 

64 

91 

78 

FIGURE  9 

Percentages  of  growth  toward  maturity  completed  at  indicated  intervals  in  D.  deserti 
nd  D.  merriami. 


50  days  D.  deserti  had  reached  75  per  cent  of  its  adult  weight  while 
D.  merriami  had  only  attained  64  per  cent.  At  this  point  D.  merriami 
lagged  behind  and  then  very  slowly  approached  the  maximum  weight. 
At  90  days  D.  deserti  had  attained  91  per  cent  of  its  weight  while  in 
D.  merriami  only  78  per  cent  had  been  reached.  In  the  later  phases 
of  growth  D.  merriami  gained  weight  more  slowly  than  D.  deserti. 
Both  attained  full  adult  average  weights  by  150  to  180  days. 

In  total  length  (  Figures  9  and  1 1 )  Z>.  merriami  grew  more  rapidly 
than  D.  deserti  throughout  the  growth  period.  Maximum  adult  lengths 
are  difficult  to  measure  but  approximate  adult  dimensions  are  attained 
by  90  days. 

The  tail  of  D.  merriami  (Figures  9  and  11)  grew  faster  than  that 
of  D.  deserti  during  the  developmental  period.  After  90  days  D. 
merriami  had  little  tail  growth  while  D.  deserti  continued  to  increase 
its  tail  length  by  7  per  cent. 

The  foot  (Figures  9  and  12),  which  was  already  well  developed  at 
birth,  grew  fastest  of  all.  At  15  days  D.  deserti  had  a  foot  70  per  cent 
of  adult  size  while  D.  merriami  had  attained  82  per  cent  of  the  adult 
foot  size.  Both  species  attained  maximum  foot  size  between  50  and 
90  days. 

The  ear  (Figures  9  and  12)  grew  rapidly  in  both  species,  that  of 
D.  merriami  faster  than  that  of  D.  deserti.  The  ear  was  approximately 
fully  grown  by  90  days  in  D.  merriami  but  continued  to  grow  slowly 
in  D.  deserti. 

Size  of  the  litter  (Figure  13)  made  little  difference  on  increases 
in  weight  of  D.  deserti.  Litters  containing  2,  3,  4,  and  5  individuals 
were  compared  and  showed  very  little  variation  in  weight  changes. 
Apparently  all  individuals  in  the  respective  litters  received  sufficient 
food  both  by  nursing  and  individually  after  weaning.  Litters  of 
D.  merriami  were  not  numerous  enough  to  permit  these  observations. 


272 


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134 


GROWTH   AND   DEVELOPMENT    OF    KANGAROO   RATS 


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J I I L 


1_J L_± 


0        6       12       18      24     30     36      42     48     54     60      66     72      78    84 

AGE  IN    DAYS 

FIGURE  11 
A   composite   graph   showing   increase   in   linear   dimensions   of   total   length    and   tail 
length  in  D.  deserli  and  D.  merriami,  semilogarithmic  plot. 


274 


BERNARD  B.   BUTTERWORTH 


135 


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20- 


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5- 
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3- 


2- 


FOOT    - 


K'. 00150 
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EAR     - 


INCREASE     IN     LINEAR 
DIMENSIONS 

y     p.  DESERTI 
o     D.  MERRIAMI 


J_ 


_L 


_L 


_L 


_L 


_L 


0   6   12   18   24   30  36   42   48  54   60  66  72   78  84 

AGE  IN  DAYS 

FIGURE  12 
A  composite  graph  showing  increase  in  linear  dimensions  of  foot  length  and  ear  length 
of  D.  deserti  and  D.  merriami,  semilogarithmic  plot. 


275 


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276 


BERNARD  B.   BUTTERWORTH  137 

The  differential  rates  of  growth  during  development  in  the  two 
species  of  kangaroo  rats  is  significant.  The  smaller  D.  merriami 
matures  more  rapidly  than  the  larger  D.  deserti.  The  development  of 
various  body  parts  in  growing  juveniles  of  D.  merriami  demonstrates 
more  rapid  growth  and  an  earlier  maturity  than  D.  deserti.  The 
precocious  growth,  especially  during  early  development,  brings  D. 
merriami  to  an  earlier  seasonal  reproductive  potential  than  D.  deserti 
and  may  allow  for  an  earlier  dispersion.  Rapid  development  may  be 
one  contributing  factor  for  the  larger  geographical  range  of  Merriam's 
kangaroo  rat. 

Summary  and  Conclusions 

The  growth  and  development  of  two  sympatric  species  of  kangaroo 
rats  is  discussed,  utilizing  data  from  8  litters  of  D.  deserti  and  4  litters 
of  D.  merriami  reared  under  identical  laboratory  conditions.  General 
development  and  sequences  of  hair  acquisition  are  described.  Animals 
of  both  species  were  completely  furred  by  15  days.  Their  pelages  were 
darker  than  those  of  their  parents. 

The  ears,  which  were  closed  at  birth,  opened  in  15  days  in  D.  deserti 
and  in  10  days  in  D.  merriami.  The  nails  hardened  by  15  days  in  both 
species  and  the  teeth  erupted  after  5  days  in  D.  merriami  and  in  8  days 
in  D.  deserti.  The  teeth  were  white  at  first  but  gradually  darkened  to 
a  shade  of  yellow.  Eyes  opened  at  about  16  days  in  D.  deserti  and 
from  11  to  15  days  in  D.  merriami. 

Instantaneous  growth  rates  were  calculated  for  various  measure- 
ments, such  as  weight,  total  length,  tail  length,  foot  length,  and  ear 
length.  Both  species  of  kangaroo  rats  attained  average  adult  weights 
from  150  to  180  days.  Each  species  reached  approximately  one-half 
of  its  adult  weight  by  30  days.  Early  growth  was  rapid  in  D.  merriami 
but  continued  more  slowly  toward  maximum  weight.  D.  deserti  at- 
tained maximum  adult  weight  at  a  slightly  earlier  age  than  D.  merriami. 
In  total  length,  D.  merriami  grew  more  rapidly  than  D.  deserti  through- 
out the  growth  period.  Both  grew  to  approximately  adult  lengths  by 
90  days.  The  tail  of  D.  merriami  grew  faster  than  that  of  D.  deserti 
during  development.  After  90  days  D.  merriami  had  little  tail  growth 
while  the  tail  of  D.  deserti  continued  to  increase  slowly  in  length.  The 
foot  showed  the  fastest  development.  By  15  days  D.  deserti  had  70 
per  cent  of  its  adult  size  while  D.  merriami  had  attained  82  per  cent 
of  its  adult  size.   Both  species  attained  maximum  size  between  50  and 


277 


138  GROWTH    AND    DEVELOPMENT    OF    KANGAROO    RATS 

90  days.  The  ear  of  D.  merriami  grew  slightly  faster  than  that  of 
D.  deserti.  Ears  were  almost  completely  grown  to  adult  size  in  D. 
merriami  by  90  days.  They  continued  to  grow  slowly  in  D.  deserti. 
Size  of  litter  made  no  appreciable  difference  in  growth  rates. 

The  precocious  early  development  of  D.  merriami  may  partly  explain 
its  larger  geographical  range. 

Acknowledgments 

Special  appreciation  is  extended  to  the  University  of  Southern 
California  Graduate  School  which  readily  furnished  equipment  and 
facilities  for  carrying  on  the  necessary  laboratory  work  connected 
with  this  research  and  to  the  Committee  for  Research  in  Problems  of 
Sex,  National  Academy  of  Sciences — National  Research  Council, 
which  provided,  in  part,  the  financial  help  needed  to  complete  the 
study. 

References 

1.  Bailey,  V.     1931.     Mammals  of  New  Mexico.    North  American  Fauna,  53,  412  pp. 

2.  Brody,  S.     1945.     Time  relations  of  growth  of  individuals  and  populations.    Chapter 

16:487-574  in   Bioenergetics  and   growth.    New  York:    Reinhold.    1023    pp. 

3.  Chew,    R.    M.,    &    Butterworth,     B.     B.     1959.     Growth    and    development     of 

Merriam's  kangaroo    rat,   Dipodomys   merriami.    Growth,   23,    75-95. 

4.  CuLBERTSON,    A.    E.     1946.     Observations    on    the    natural    history    of    the    Fresno 

kangaroo   rat.    Jour.  Mamm.,  27,   189-203. 

5.  DoRAN,   D.   J.     1952,     Observations    on    the   young   of   the    Merriam    kangaroo    rat. 

Jour.  Mamm.,  33,  494-495. 

6.  Fitch,    H.    S.     1948.     Habits   and    economic    relationships    of    the    Tulare    kangaroo 

rat.    Jour.  Mamm.,  29,  5-35. 

7.  Reynolds,   H.   G.     1956.     The   ecology   of   the   Merriam   kangaroo   rat    {Dipodomys 

merriami  Mearns)   on  the  grazing  lands  of  Southern  Arizona.    Ecol.  Monographs, 
28,  111-127. 

8.  Rush,  W.  M.     1945.     Beau  Brummel  of  the  wild.    Nat.  Hist.,  New  York,  54,  40-41. 

9.  Tappe,  D.  T.     1941.     Natural  history   of   the   Tulare   kangaroo   rat.    Jour.  Mamm., 

22,  117-148. 


278 


Article  IX.— CRANIAL  VARIATIONS  IN  NEOTOMA 
MICROPUS  DUE  TO  GROWTH  AND  INDIVIDUAL 
DIFFERENTIATION. 

By  J.  A.  Allen. 
Plate  IV. 

In  view  of  the  stress  naturally,  and  very  properly,  laid  upon 
the  importance  of  cranial  characters  in  the  discrimination  of 
species  in  groups  of  closely-allied  forms,  it  seems  desirable  to 
ascertain  the  character  and  amount  of  change  in  not  only  the 
general  form  of  the  skull  but  in  the  form  of  its  separate  bones 
due  to  growth,  and  also  to  determine  the  amount  and  kind  of 
individual  variation  that  may  be  expected  to  occur  in  skulls 
unquestionably  of  the  same  species.  Having  of  late  had  occasion 
to  examine  a  large  amount  of  material  relating  to  the  genus 
Neotoma^  the  subject  has  been  forcibly  brought  to  my  attention, 
and  some  of  the  results  of  a  careful  examination  of  a  large  series 
of  skulls  pertaining  to  several  species  of  this  genus  are  here 
presented.  No  attempt  is  made  to  treat  the  subject  exhaustively, 
only  a  few  special  points  being  here  presented. 

As  is  well  known  to  all  experienced  workers  in  mammalogy, 
tlie  general  contour  of  the  brain-case,  the  relative  size  and  form 
of  individual  bones,  notably  the  interparietal,  and  the  condition 
of  the  sujjraorbital  and  other  ridges  for  muscular  attachment, 
alter  materially  after  the  animal  reaches  sexual  maturity ;  the 
deposition  of  osseus  matter,  the  closing  of  sutures,  the  building 
out  of  crests  and  rugosities  continuing  throughout  life,  so  that  a 
skull  (){  a  very  old  animal  may  differ  notably  from  that  of  an  indi- 
vidual of  the  same  species  in  middle  life,  and  this  latter  from  one 
just  reaching  sexual  maturity. 

The  Museum  has  at  present  a  large  series  of  specimens  of 
Neoionia  niicropus  Baird,  including  ages  ranging  from  nursling 
young  to  very  old  adults.  They  are  mainly  from  three  localities 
in  the  eastern  coast  district  of  Texas,  namely,  Brownsville,  Cor[)us 
Christi,  and  Rockport.     In  order  to  avoid  any  complications  that 

[233] 


279 


2,34      Bulletin  American  Museum  of  Natural  History.     [Vol.  VI, 

might  arise  through  geographic  variation,  only  the  specimens  from 
Rockjjort  and  Corpus  Christi — localities  less  than  twenty-five 
miles  apart,  and  similar  in  physical  conditions — are  here  consid- 
ered. There  is  not  the  slightest  reason  for  questioning  their  con- 
specific  relationshi|).  The  series  selected  to  illustrate  variations 
due  to  age  are,  with  one  exception,  from  Rockport  ;  those  figured 
to  show  individual  variation  are  all  from  Corpus  Christi. 

Variations  due  to  Age. 

General  Contour. — The  variation  in  the  general  form  of  the 
skull  resulting  from  growth  is  due  mainly  to  the  lengthening  of 
the  several  skull  segments  without  a  corresponding  relative  in- 
crease in  the  breadth  of  the  skull.  Hence  in  the  young  skull,  in 
comparison  with  an  adult  skull  of  the  same  species,  the  brain- 
case  is  disproportionately  large  in  comparison  with  the  anteor- 
bital  and  basal  portions  of  the  skull.  This  is  well  shown  in 
Plate  IV,  and  in  the  subjoined  table  of  measurements  of  three 

Measurements  and    Ratios  showing   Cranial  Variations  due  to  Age 

IN  Neotoma  tnicropus. 


Occipito-nasal  length 

Length  of  nasals 

Length  of  frontais 

Length  of  parietals  on  median  line.    .  . . 

(Ireatest  length  of  parietals 

Length  of  interparietal 

Length  of  brain-case 

(Ireatest  rostral  breadth    

Least  interorbital  breadth .  .  , 

Breadth  of  brain-case    

Breadth  of  interparietal 

Greatest  zygomatic  breadth 

Depth  of  skull  at  middle  of  palate 

Depth  of  skull  at  front  of  basisphenoid. 
Length  of  tooth-row  (crown  surface). .  .  . 

Length  of  incisive  foramina 

Width  of  incisive  foramina 

Length  of  palatal  floor   


No. 

5834, 
9    JUV. 

1 

Ratioi 

No. 
4480, 
.',   juv. 

31 

100 

41 

10 

32.3 

14.5 

13 

42 

15 

5 

19.4 

6 

12 

39 

15 

4.5 

14.5 

5.5 

14 

45.2 

17 

5.5 

17.7 

6.3 

6 

1 ;» .  4 

6 

16 

51.  H 

19.5 

11 

35.5 

10 

20? 

ti4.B 

23 

8 

2rt 

11 

11 

35.5 

12 

8- 

26.8 

8 

6 

19.3 

8.5 

3 

9.7 

3 

5 

16.1 

7 

No. 

Ratio" 

4478, 

,'  very 

old. 

100 

53 

35.4 

22 

36.6 

18 

14.6 

8 

36.6 

16 

13.4 

7 

41.5 

21 

15.4 

6.5 

14.6 

6 

45 

20 

24.4 

7.5 

56.1 

30 

26 
29 . 3 
19.5 

20.7 
7.3 
17 


15 

14 

9 
11. 

3. 

7 


Ratioi 


100 
41.5 
34 
15 

30.2 
13.2 
39. 
12. 
11 
38 

14.2 
56.6 
28.5 
26.4 
17 

21.7 

6.6 

13.2 


.6 
.3 
.3 


'  Ratio  to  occipito-nasal  length. 

2  From  No.  448?,  9   juv.,  in  which  the  last  molar  has  Just  come  into  use. 


280 


1 894-]        Allen,  Cranial  Variations  in  JVeo/oma  micropus.  235 


specimens  of  A',  micropus  from  Rockport,  Texas.  No.  5834, 
$  juv.,  is  a  nursling  so  young  that  the  last  molar  is  still  wholly 
enclosed  in  the  jaw  ;'  No.  4480,  ^,  jnv.,  though  not  (]uite  full- 
grown,  would  pass  as  a  'young  adult';  No.  4478,  r?  ad.,  is  a  very 
old  male,  with  the  teeth  well  worn  down,  and  the  fangs  visible 
at  the  alveolar  border.  Other  specimens  in  the  series  furnish  a 
complete  series  of  gradations  between  the  two  extremes  (Nos. 
5834  and  447^)- 

In  general  contour  (Figs,  i-ii,  PI.  IV),  the  young  skull,  in 
comparison  with  adults,  is  much  more  convex  in  dorsal  outline,' 
very  broad  posteriorly,  and  very  narrow  anteriorly.  In  compar- 
ing the  relative  length  of  the  several  skull  segments  the  occipito- 
nasal  length  is  taken  as  the  basis,  and  the  skulls  will  be  referred 
to  as  A  (  =  No.  5834),  B  (  =  No.  4480),  and  C(  =  No.  4478). 

Rostral  Segment. — In  A  the  ratio  of  the  rostral  segment  to  the 
total  length  is  32.3  per  cent.  ;  in  B,  35.4;  in  C,  41.5 — giving  a 
rapid  increase  in  the  ratio  with  age. 

Frontal  Segment. — In  A  the  ratio  of  the  frontal  segment — /.  e., 
the  distance  between  the  naso-frontal  and  fronto-parietal  sutures 
— to  the  total  length  is  42  per  cent.  ;  in  B,  36.6  ;  in  C,  34 — a 
considerable  decrease  in  the  ratio  with  age. 

Parietal  Segment.  —  In  A  the  ratio  of  the  parietal  segment — 
/.  (?.,  the  distance  from  the  latero-anteri<jr  angle  of  the  parietal 
bone  on  either  side  to  the  occipito-parietal  suture — to  the  total 
length  is  39  per  cent.;  in  ^,  36.6;  in  C\  30.2 — again  a  rapid 
decrease  in  the  ratio. 

Brain-case. — The  length  of  the  brain-case  in  A  is  5  1.6  per  cent, 
of  the  total  length  of  the  skull  ;  in  B,  45  ;  in  C,  t,?>. 

In  each  case  the  change  in  ratio  is  due  to  the  disproportionate 
growth  of  the  rostral  portion  of  the  skull.  Thus  in  A  the  nasals 
have  a  length  of  only  10  mm.  ;  in  B  they  have  increased  to  14.5 
mm.,  and  in  C  to  22  mm.,  while  the  total  occipito-nasal  length  of 

'  The  length  of  the  tooth-row  given  in  the  table  is  taken  from  an  older  specimen  (No.  4482, 
^  juv.),  in  which  the  last  molar  has  reached  the  level  of  the  others  and  is  just  beginning  to 
show  traces  of  wear. 

'•^  In  Figs.  10  and  11  it  should  be  noted  that  the  greater  flatness  of  the  skull  interorbitally, 
as  compared  with  Fig.  6,  is  masked  by  the  raised  supraorbital  borders  in  the  older  skulls  wiien 
viewed  in  profile. 


281 


236      Bulletin  American  Museum  of  Natural  History.     [Vol.  VI, 

the  skull  has  increased  only  from  31  mm.  in  A  to  53  mm.  in  C. 
In  other  words,  the  nasal  bones  have  increased  in  length  120  per 
cent.,  while  the  total  length  has  increased  only  77  per  cent. 

Transverse  Breadth. — In  respect  to  the  breadth  of  the  skull 
the  variations  with  growth  are  much  less  than  in  its  length. 
Thus  tlie  greatest  diameter  of  the  rostrum  varies  only  from  5.5 
mm.  in  A  to  6.5  in  C — an  increase  of  about  20  per  cent,  in  the 
breadth  of  the  rostrum,  against  an  increase  of  120  per  cent,  in 
its  length.  The  interorbital  breadth  remains  nearly  constant, 
being  6  mm.  in  all  three  of  the  skulls  here  compared.  The  width 
of  the  brain-case  shows  an  increase  of  25  per  cent,  against  an 
increase  in  the  total  length  of  the  skull  of  77  per  cent.  The 
zygomatic  breadth  shows  an  increase  of  about  50  per  cent.,  due 
almost  wholly  to  the  thickening  and  increased  convexity  of  the 
zygomatic  arches. 

Vertical  Depth. — In  respect  to  the  depth  of  the  skull,  the  vari- 
ations with  age  prove  especially  interesting,  although  only  such 
as  would  be  expected  from  the  facts  already  given.  For  present 
purposes  the  depth  of  the  skull  is  taken  at  two  points,  namely, 
{a)  at  the  middle  of  the  palatal  region,  and  {b)  at  the  posterior 
border  of  the  basisphenoid  (basisphenoid-basioccipital  suture). 
The  palatal  depth  increases  markedly  with  age,  correlalively  with 
the  growth  of  the  rostrum  ;  the  basisphenoidal  depth  changes  but 
slightly  after  the  molars  have  attained  to  functional  development. 
Thus  in  A  the  basisphenoidal  depth  is  11  mm.  ;  in  /^,  12  mm.  ; 
in  C,  14  mm. — an  increase  of  about  28  per  cent.  The  palatal 
depth  in  ^4  is  8  mm.  ;  in  B,  11  mm.  ;  in  C\  15  mm. — an  increase 
of  nearly  88  per  cent. 

Tooth-row. — The  length  of  the  upper  tooth-row  varies  about  12 
per  cent.,  due  almost  wholly  to  the  wearing  down  of  the  teeth, 
the  length  of  the  crown  surface  being  much  less,  in  slightly 
worn  teeth,  than  the  length  taken  at  the  alveolar  border. 

Interparietal. — The  interparietal  shows  sur[jrising  modilication 
with  age,  both  as  to  size  and  form,  but  especially  in  respect  to 
the  latter.  At  early  stages,  as  in  ^,  this  bone  is  more  or  less 
crescentic  in  shape,  with  the  transverse  diameter  more  than  twice 


282 


1894-]       Allen,  Cranial  Variations  in  Neoto7na  micropus.  237 


the  antero-posterior  diameter.  Thus  in  A  the  two  diameters  are 
respectively  11  and  4.5  mm.  ;  in  B,  10  and  5.5  mm.  ;  in  6\  7.5 
and  7  mm.  In  other  words,  the  short,  broad,  convex  sub-cres- 
centic  interparietal  in  A  becomes  transformed  in  C  into  a 
squarish,  flat  bone  in  which  the  two  diameters  are  nearly  equal, 
instead  of  the  transverse  being  twice  as  great  as  the  antero- 
posterior, as  in  A.  This  would  be  almost  incredible  were  not 
the  proof  so  abundantly  furnished  by  the  material  in  hand,  where 
every  stage  of  transition  is  shown.  (Figs.  i-S,  PI.  IV.)  This 
change  is  coincident  with  the  development  of  the  raised  supra- 
orbital borders  and  their  prolongation  backward  as  ridges  to  the 
parieto-occipital  suture,  and  the  flattening  of  the  whole  dorsal 
aspect  of  the  post-rostral  portion  of  the  skull.  In  old  age  these 
ridges  become  confluent  with  the  lateral  edges  of  the  interparietal 
which  has  now  lost  its  postero-lateral  moieties,  partly  apparently 
by  absorption  and  partly  by  their  being  overgrown  by  the  mediad 
posterior  angle  of  the  parietals.  A  sharp  thin  ridge  for  muscular 
attachment  also  extends  back  from  the  posterior  base  of  the 
zygomatic  arch.  The  interparietal  at  the  same  time  develops  a 
more  or  less  prominent  median  angular  projection  at  its  posterior 
border,  confluent  with  the  median  ridge  of  the  supraoccipital. 
The  contrast  between  these  conditions,  obtaining  only  in  very 
old  skulls,  and  their  almost  entire  absence  in  skulls  which  have 
iust  reached  sexual  maturity,  is  strikingly  great. 

Supraoccipital. — The  supraoccipital  changes  from  a  posteriorly 
convex,  thin  lamina  of  bone,  in  early  life,  to  a  thick,  nearly  ver- 
tical plate,  with  a  strongly-developed  median  ridge  produced  into 
an  angular  spine  at  its  superior  border,  and  with  a  lateral  ridge 
on  either  side  about  midway  between  the  median  line  and  its 
lateral  borders  ;  these  lateral  ridges  also  each  develop  an  angular 
rugosity  or  process  about  midway  their  length.  The  superior 
border  is  also  produced  into  an  incipient  occipital  crest. 

Basioccipital. — The  basioccipital  becomes  greatly  altered  by 
growth,  as  in  fact  is  the  case  with  the  whole  postpalatal  region. 
In  comparing  stages  A  and  C  it  is  found  that  the  distance  across 
the  occipital  condyles  increases  only  about  15  per  cent.,  while 
the  breadth  of  the  anterior  border  increases  100  per  cent,  and 
the  length  about  50  per  cent.     (Figs.  12-14,  P^-  ^^ ■) 


283 


230     Bulletin  American  Museum  of  Natural  History.     [Vol.  VI, 

Basisphenoid. — The  basisphenoid  doubles  in  length,  and  its 
anterior  third  becomes  differentiated  into  a  narrow  projecting 
neck.  The  presphenoid  at  stage  A  is  nearly  hidden  by  the 
palatal  floor.     (Figs.  12-14,  PI.  IV.) 

Postpalatal  Region  as  a  whole. — This  doubles  its  length  with  an 
increase  in  breadth  of  only  about  50  per  cent.  At  stage  A  the 
postpalatal  border  terminates  slightly  behind  the  posterior  edge 
of  M.2  ;  in  stage  3  it  holds  very  nearly  the  same  position.  The 
distance  between  the  postpalatal  border  and  the  front  border  of 
the  auditory  bullae,  compared  with  the  total  length  of  the  skull, 
is  as  I  to  9  in  ^,  and  as  i  to  5  in  C.  In  A  the  pterygoid  hamuli 
reach  the  second  fourth  of  the  bullae  ;  in  C  they  terminate 
slightly  in  advance  of  the  bullae.  The  bullae  themselves  in  A  are 
more  obliquely  placed  than  in  C,  in  relation  to  the  axis  of  the 
skull,  and  are  quite  differently  shaped.  Also  the  form  of  the 
foramen  magnum  has  undergone  much  change.  These  points 
are  all  well  shown  in  Figs.  12-14  of  ^l^e  accompanying  plate. 

Incisive  Foramina. — Consequent  upon  the  growth  of  the 
rostral  portion  of  the  skull,  the  incisive  foramina  undergo  marked 
change  in  form,  and  somewhat  in  position,  as  regards  both  their 
anterior  and  posterior  borders.  In  the  stage  designated  as  A 
they  are  short  and  broad,  and  extend  relatively  further  both 
anteriorly  and  posteriorly  than  in  stage  B  or  C,  their  anterior 
border  being  nearer  the  base  of  the  incisors,  and  their  posterior 
border  being  carried  back  to  or  slightly  behind  the  front  border 
of  the  first  molar.  Thus  in  A  the  length  of  the  incisive  foramina 
is  6  mm.,  with  a  maximum  breadth  of  3  mm.,  while  in  C  the 
dimensions  are  respectively  11.5  and  3.5  mm. — a  great  increase 
in  length  with  only  slight  increase  in  breadth.  At  the  same 
time  the  anterior  border  is  considerably  further  from  the  base  of 
the  incisors,  and  the  posterior  border  is  slightly  in  advance, 
instead  of  slightly  behind,  the  front  border  of  the  molars. 

Sphe7io-palatine  Vacuities.  — Va  adults  of  N'eotoma  micropus^  as  in 
other  species  of  the  '  round-tailed  '  section  of  the  genus,  there  is 
a  long,  broad  vacuity  on  each  side  of  the  presphenoid  and  ante- 
rior third  of  the  basisphenoid,  which  Dr.  Merriam  has  recently 


284 


1 894-]        Allen,  Cranial  Vai'iations  in  Neotoma  micropus.  239 


named'  the  ^  spheno-palatine  vacuilies,'  and  he  has  also  called  atten- 
tion to  the  fact  that  they  are  not  present  in  some  forms  of  the 
*  bushy-tailed '  section  of  the  genus.  It  is  therefore  of  interest 
in  the  present  connection  to  note  that  these  vacuities  are  absent 
at  stage  A,  and  are  only  partially  developed  at  later  stages  (Figs. 
12-14,  PI.  IV).  My  attention  was  called  to  the  matter  by  finding 
several  nearly  fully-grown  skulls  from  Texas  and  northeastern 
Mexico  with  these  vacuities  either  quite  absent  or  represented  by 
an  exceedingly  narrow  slit,  while  I  could  find  no  differences  in 
the  skins  or  in  other  cranial  characters  that  gave  the  slightest 
hint  that  the  animals  were  not  referable  to  JV.  micropus.  Further 
examination  of  young  skulls  of  undoubted  JV.  micropus  from 
Rockport  and  Corpus  Christi,  Texas,  showed  that  the  closed 
condition  was  in  this  species  a  feature  of  juvenility.  It  is  thus  of 
interest  to  find  that  a  feature  which  proves  to  be  merely  a  char- 
acter of  immaturity  (and  quite  inconstant  as  well)  in  IV.  micropus 
is  a   permanent  condition  in  N.  cinerea  occidentalis: 

In  the  development  of  these  vacuities  it  appears  that  as  the 
presphenoid  increases  in  length  it  becomes  reduced  in  width  ; 
at  the  same  time,  as  the  skull  broadens,  the  edges  of  the  ascend- 
ing wings  of  the  palatine  bones  become  slightly  incised.  There 
is,  however,  much  individual  variation  in  this  respect,  as  will  be 
shown  later. 

Molars. — When  the  molars  first  cut  the  gum  they  have  nearly 
the  entire  crown-surface  capped  with  enamel.  Very  soon,  even 
before  the  tooth  has  attained  its  full  height,  the  enamel  begins  to 
disappear  from  the  centers  of  the  enamel  loops,  the  capping  re- 
maining longer  over  the  narrower  loops  than  over  the  broader 
ones  ;  it  quickly  disappears  from  all  as  soon  as  the  crown-surface 
becomes  subject  to  wear.  In  stage  ^,  in  which  only  M.i  and 
M.2  have  appeared,  and  are  less  than  one-third  grown,  the 
enamel  walls  of  the  loops  nearly  meet  over  the  dentinal  areas — 
quite  meeting  over  the  narrower  portions,  especially  in  the  case  of 
the  middle  transverse  loop  of  each  tooth.  Some  time  before  the 
age  represented  by  B  is  reached,  the  crown-surface  is  worn  to  an 

1  Proc.  Biol.  Soc.  Wash.,  VII I,  p.  112,  July,  1893. 

2  Unfortunately  the  outline  figures  here  given  (Figs.  12-15,  PI-  IV, )  fail  to  show  clearly  the 
points  at  issue. 


285 


240      Bulletin  American  Museum  of  Natural  History.     [Vol.  VI, 


even  plane  ;  the  tooth  has  reached  its  normal  length,  but  the 
fluting  of  the  sides  still  extends  to  the  alveolar  border.  As 
attrition  goes  on,  with  the  advance  of  the  animal  in  age,  the 
crown-surface  wears  down,  and  the  neck  of  the  tooth  appears 
above  the  alveolar  border,  till,  especially  in  the  upper  molars,  the 
fluted  terminal  and  the  smooth  basal  portions  are  of  nearly  equal 
extent ;  but  in  old  age  (as  in  C)  the  smooth  basal  portion  is  the 
longer  and  the  division  of  the  root  into  fangs  is  clearly  shown. 
With  this  wearing  down  the  tooth  increases  somewhat  in  both 
width  and  length,  but  the  pattern  of  the  enamel  folds  undergoes 
but  slight  change  until  nearly  the  whole  crown  is  worn  away, 
exce|:)t  that  the  angles  become  gradually  more  rounded. 

Resume.  —  As  already  stated  the  change  with  age  in  the  general 
form  of  the  skull  is  due  to  the  relatively  disproportionate  increase 
in  length  of  the  pre-  over  the  post-orbital  region,  and  the  same 
disproportionate  increase  of  the  basal  region  as  compared  with 
the  frontoparietal  elements.  In  the  first  case  the  rostrum  be- 
comes relatively  greatly  produced  ;  in  the  second  the  basiocci- 
pital  and  adjoining  parts  become  so  greatly  enlarged  as  to  change 
the  entire  aspect  of  the  basal  region  of  the  skull.  Thus  the 
occipital  condyles,  which  in  A  terminate  slightly  in  advance  of 
the  most  convex  portion  of  the  supraoccipital,  and  are  crowded 
u])  very  close  to  the  bullae,  form  in  C  the  most  posterior  part  of 
the  skull,  with  a  considerable  interval  between  them  and  the 
bulla;.     (Figs.  12-14,  PI-  IV.) 

Individual    Variation. 

In  comparing  a  large  series  of  skulls  of  the  same  species  it 
quickly  becomes  apparent  that  no  element  of  even  the  adult 
skull  is  constant,  either  as  to  form  or  relative  size.  There  is  also 
much  variation  in  the  size  of  skulls  of  the  same  sex  and  approxi- 
mately the  same  age. 

Variation  in  .5'/sr.— Thus  in  Neotoma  micropiis,  from  the  same 
locality,  there  are  dwarfs  and  giants.  While  the  females  average 
smaller  than  the  males,  size  is  by  no  means  a  safe  criterion  of 
sex.  Thus  two  old  females,  not  appreciably  different  in  age, 
from   Corpus  Christi,   Texas,  vary  as  follows  :    No.    2948,   total 


286 


1 894-]       Alleti,  Crania/  Variations  in  Ncotoma  micropus.  24 1 


length  51  mm.,  zygomatic  breadth  26  mm.  ;  the  corresponding 
dimensions  in  No.  2955  are  45  mm.  and  24  mm.  These  are 
merely  the  extremes  of  a  series  of  six  specimens  ;  with  a  much 
larger  series  doubtless  the  difference  would  be  considerably 
increased.  A  series  of  six  old  males,  from  the  same  locality  and 
indistinguishable  as  to  age,  vary  as  follows:  No.  2952,  total 
length  50.5  mm.,  zygomatic  breadth  27  mm.  ;  the  corresponding 
dimensions  in  No.  2956  are  45  mm.  and  25  mm. 

Nasals  and  ascending  branches  of  the  Premaxillce. — Ordinarily 
in  N.  micropus  the  nasals  terminate  in  a  gradually  narrowed 
evenly  rounded  point,  a  little  less  than  2  mm.  in  front  of  the 
posterior  termination  of  the  ascending  branches  of  the  premaxills. 
The  distance  between  the  points  of  termination  of  the  nasals  and 
premaxillse,  however,  frequently  varies  between  1.5  and  2.5  mm.  ; 
more  rarely  from  i  to  3  mm.  These  extremes  each  occur  in  the 
ratio  of  about  10  per  cent,  of  the  whole,  while  probably  60  per 
cent,  would  not  vary  much  from  the  normal  average  of  about 
2  mm.     (See  Figs.  1-8  and  t6,  17,  PI.  IV.) 

The  nasals,  as  already  said,  usually  terminate  in  an  evenly 
rounded  point,  but  in  several  of  the  50  skulls  of  N.  micropus 
before  me  their  posterior  border  forms  a  double  point,  each  nasal 
terminating  in  a  distinctly  rounded  point  ;  in  one  or  two  the 
posterior  border  is  squarely  truncate ;  in  others  it  is  irregularly 
uneven.  The  ascending  branches  of  the  premaxillae  usually 
terminate  in  an  obtusely  V-shaped  point,  with  a  uniformly  even 
outline,  their  breadth,  however,  being  subject  to  variation  ;  in 
some  specimens  they  terminate  in  a  brush  of  irregular  spiculae. 
(Figs.  1-8  and  16,  17,  PI.  IV.) 

Frontals. — The  posterior  border  of  the  frontals  is  subject  to 
great  irregularity,  varying  from  a  nearly  transverse  line  (rounded 
slightly  at  the  outer  corners)  to  a  gentle,  rather  even  convexity, 
and  thence  to  an  acute  angle,  involving  the  whole  posterior 
border.  It  is  difficult  to  decide  what  outline  is  the  most  frequent, 
though  the  tendency  seems  to  be  greatest  toward  a  well-pro- 
nounced rather  even  convexity.  Figures  1-8  and  18,  19,  Plate  V, 
well  show  the  variation  in  the  position  and  direction  of  the 
fronto-parietal  suture. 

\_Scptenibcr ,  /Sq/.] 


287 


242      Bulletin  American  Museum  of  Natural  History.     [Vol.  Vl, 

Parietals. — The  anterior  outline  of  the  parietals  of  course  con- 
forms to  the  posterior  outline  of  the  frontals,  and  must  be  equally 
variable.  It  hence  follows  that  their  length  on  the  median  line 
is  also  variable.  Their  posterior  border  is  also  subject  to  much 
variation  in  consequence  of  the  great  diversity  in  the  form  of  the 
interparietal. 

Intej'parietal. — In  middle-aged  specimens  the  interparietal  tends 
strongly  to  a  quadrate  form,  varying  from  quadrate  to  diamond 
shape,  through  a  more  or  less  marked  median  angular  extension 
of  both  its  anterior  and  posterior  borders,  and  occasionally  of  its 
lateral  borders  as  well.  Often  it  forms  a  quadrate  figure,  in  which 
each  of  its  four  sides  is  slightly  convex  ;  again  the  corners  are  so 
much  rounded,  and  the  lateral  breadth  so  much  in  excess  of  the 
antero-posterior,  as  to  give  a  lozenge-shaped  figure.  In  other 
cases  it  is  distinctly  shield-shaped  ;  in  others  it  is  hexagonal.  In 
size  the  variation  is  fully  50  per  cent,  of  what  may  be  regarded 
as  the  average  dimensions.  These  remarks  have  strict  reference 
to  fully  adult  specimens,  and  as  nearly  as  can  be  judged  these 
variations  are  not  at  all  due  to  differences  of  age,  which,  as 
already  shown,  has  so  great  an  influence  upon  the  size  and  form 
of  this  exceedingly  variable  element  of  the  skull.'  (Figs.  20-23, 
PI.  IV.     Compare  also  the  interparietal,  as  shown  in  Figs.  1-8.) 

Ventral  aspect. — The  ventral  aspect  of  the  skull  presents 
numerous  points  of  variability,  only  a  few  of  which  will  be  here 
mentioned.  The  palate  varies  more  or  less  in  breadth,  and 
especially  in  the  development  of  the  anterior  palatal  spine,  which 
is  sometimes  slight,  and  sometimes  so  strongly  produced  anteri- 
orly as  to  touch  the  vomer.  The  postpalatal  border  may  be 
evenly  concave,  or  present  a  slight  median  process.  The  pre- 
sphenoid  is  very  variable  in  size,  being  often  an  exceedingly 
slender  rod  of  bone,  and  at  other  times  very  stout,  the  variation 
in  thickness  being  nearly  or  quite  100  per  cent.  The  anterior 
third  of  the  basisphenoid  shares  in  the  same  variability.     As  the 

'  As  regards  variation  with  age  in  the  form  of  the  interparietal,  Neotoma  jnicropus  is  only 
an  example  of  what  doubtless  prevails  throughout  the  genus,  and  even  in  many  other  genera  as 
well.  Yet  in  adult  animals  the  form  of  this  bone  seems,  as  a  rule,  to  be  sufficiently  constant  to 
be  of  more  or  less  taxonomic  value.  Thus  in  the  A'^.  cinerea  group  it  may  be  said  to  be  nor- 
mally quadrate  ;  in  the  N .fuscipes  group  it  is  quite  constantly  shield-shaped.  In  N.  floridana., 
however,  and  in  the  N.  mexicana  group,  it  seems  to  be  nearly  or  quite  as  variable  as  in  N. 
jiiicropus,  both  as  to  size  and  shape. 


288 


1 894-]        Allen,  Cranial  Variations  in  Neotoma  ?nicropus.  243 

ascending  borders  of  the  palatals  are  also  variable  in  respect  to 
the  extent  of  their  development,  it  follows  that  there  is,  even 
among  adults,  a  wide  range  of  variation  in  the  size  of  the  spheno- 
palatine vacuities. 

Teeth. — Aside  from  differences  due  to  age  and  attrition,  the 
teeth  vary  in  size  to  a  considerable  extent  among  individuals 
strictly  comparable  as  to  sex  and  age,  some  having  a  much 
heavier  dental  armature  than  others.  But  more  particularly  note- 
worthy in  this  connection  is  the  variation  in  the  color  of  the 
teeth,  which  seems  strongly  a  matter  of  individuality.  Although 
Dr.  Merriam  has  recently  placed  JV.  micropus  in  his  "  Neotoma 
leucodon  group,'"  which  has,  among  other  alleged  characters, 
"  color  of  teeth  white  or  nearly  white,"  the  teeth  in  N.  micropus 
average  blacker  than  in  any  other  species  of  the  genus  known  to 
me.  Were  this  all  it  might  be  considered  that  N.  micropus  was 
erroneously  referred  to  X^^t'  leucodon  group';  but  unfortunately 
the  range  of  individual  variation  in  the  color  of  the  teeth  in  the 
large  series  at  hand  covers  also  the  whole  range  of  variation  for 
the  genus.  Thus  in  some  instances  the  molar  teeth  are  intensely 
black  from  base  to  crown,  while  the  crown-surface  itself  is 
strongly  blackish,  even  the  enamel  loops,  as  well  as  the  enclosed 
dentine  being  tinged  with  blackish  ;  in  other  cases  the  teeth 
are  merely  slightly  tinged  with  brownish  near  the  base  and  at  the 
bottom  of  the  sulci.  These  extremes  are  connected  by  a  series 
of  very  gradual  intergradations.  In  other  words,  among  hun- 
dreds of  skulls  of  Neotoma,  those  with  the  blackest  teeth  occur 
in  N.  micropus,  as  well  as  those  in  which  the  teeth  are  practically 
white. 

In  the  suckling  young  the  teeth  are  pure  white  ;  before  M.3 
has  come  to  wear,  M.i  and  M.2  have  become  more  or  less 
blackened  ;  in  young  adults,  and  in  middle  aged  specimens,  the 
teeth  are  often  intensely  black  ;  in  old  specimens,  with  the  teeth 
much  worn,  the  teeth  average  lighter  than  in  the  younger  indi- 
viduals. There  is,  however,  a  wide  range  of  variation  in  the 
color  of  the  teeth  in  specimens  of  corresponding  age,  whether 
old  or  young.     The  black  coloring  consists  to  a  large  extent  of  a 


»  Proc.  Biol.  Soc.  Wash.,  IX,  p.  ii8,  July  2,  1894. 


289 


244      Bulletin  American  Museum  of  Natural  History.     [Vol.  VI, 

superficial  incrustation  which  tends  to  scale  off  in  flakes  in  the 
prepared  skull,  and  its  absence  apparently  may  be  due  sometimes 
to  removal  in  the  process  of  cleaning  the  skull  for  the  cabinet. 
In  other  words,  the  blackness  is  to  some  extent  an  accidental  or 
pathological  condition,  due  probably  more  or  less  to  the  particu- 
lar character  of  the  food   or  to   the  health  of  the  animal. 

General  Remarks. 

The  bearing  of  what  has  been  stated  above  respecting  varia- 
tions in  the  form  of  the  skull  and  of  its  principal  elements  due 
to  age  is  of  course  obvious,  the  inference  being  that  in  animals 
which  have  reached  sexual  maturity  variations  due  wholly  to 
growth,  in  passing  through  adolescence  to  senility,  may  readily 
be  mistaken,  when  working  with  very  small  series  or  with  single 
specimens,  for  differences  of  subspecific  or  even  specific  import- 
ance. Not  only  do  the  individual  bones  vary  in  their  outlines 
and  proportions  and  in  relative  size,  but  the  skull  varies  as  a 
whole  in  its  relative  dimensions,  including  depth  as  well  as  length 
and  breadth.  There  is  beside  this  a  wide  range  of  purely  indi- 
vidual variation,  affecting  every  character  that  can  be  used  in  a 
diagnostic  sense.  Thus  in  a  series  of  fifty  skulls  of  Neotoma 
micropus  it  would  be  easy  to  select  extremes,  of  even  individual 
variation,  that  depart  so  widely  from  the  average,  in  one  or  more 
characters,  as  to  deceive  even  an  expert,  on  considering  these 
alone,  into  the  belief  that  they  must  represent  very  distinct 
species  ;  yet  in  the  present  instance  the  proof  that  such  is  not 
the  case  is  overwhelming.  In  N.  micropus  the  coloration  is  re- 
markably constant,  for  a  member  of  this  genus,  at  all  seasons 
and  ages,  so  that  the  case  is  less  complicated  than  it  would  be  in 
many  other  species  of  the  group,  where  the  color  of  the  pelage 
varies  radically  with  season  and  age. 

Personal  criticism  is  not  the  purpose  of  the  present  paper,  and 
it  was  not  my  intention  at  the  outset  to  refer  specifically  to  the 
work  of  any  of  my  confreres.  Since  its  preparation  was  begun, 
however,  its  raison  d'etre  has  perhaps  been  emphasized  by  the  pub- 
lication of  two  brochures  of  '  preliminary  descriptions  '  of  species 
and  subspecies  of  the  genus  Neotoma.^  numbering  altogether  lo 
species  and  8  subspecies,  which  added  to  the  22  species  and  sub- 


290 


1 894-]         Allen,  Cranial  Variations  in  Neotonia  nilcropus.  245 


species  previously  standing  practically  unchallenged,  makes,  at  the 
present  writing,  a  total  of  40  forms  of  the  genus  Neotoma.  Of 
these  no  less  than  26  have  been  described  within  the  last  nine 
months.'  Without  the  material  before  me  used  by  the  original 
describers  of  these  forms  it  would  be  presumptive  to  give  an 
opinion  respecting  the  merits  of  many  of  them.  While  the  greater 
part  may  have  some  real  basis,  it  is  evident  that  others  are  almost 
unquestionably  synonyms  of  previously-described  forms,  judging 
by  '  topotypes  '  in  this  Museum,  the  brief  diagnoses  accompanying 
the  names  affording  in  these  cases  no  characters  that  are  in  the 
least  degree  distinctive. 

The  genus  Neotoma  was  chosen  for  treatment  in  this  connec- 
tion in  preference  to  some  other  almost  solely  by  chance,  as  the 
facts  of  variation  above  presented  are  not  at  all  exceptional.  In 
fact  the  common  muskrat  {Fiber  zlbethlcus)  would  have  shown  a 
still  more  striking  case  of  variability,  as  would  also  various  species 
of  many  other  genera.  Yet  describers  of  new  species  are  con- 
stantly laying  stress  upon  cranial  differences  that  have  not  neces- 
sarily the  slightest  s])ecific  or  even  subspecific  importance  ;  and, 
so  far  as  can  be  judged  from  their  descriptions,  they  are  entirely 
unconscious  that  such  can  be  the  case. 

On  the  other  hand,  it  is  equally  certain  that  such  alleged 
characters  may  have  the  value  assigned  them  ;  since  it  is  now  a 
well  known  fact  that  the  extremes  of  purely  individual  variation 
in  any  character,  external  or  internal,  may  exceed  in  amount  the 
average  difTerences  that  serve  to  satisfactorily  distinguish  not 
only  well-marked  subspecies,  but  even  forms  that  are  unques- 
tionably specifically  distinct.  Hence  it  must  often  happen  that 
the  determination  of  the  status  of  a  species  or  subspecies  origin- 
ally described  from  one  or  two  specimens,  in  groups  especially 
susceptible  to  variation,  must  depend  upon  the  subsequent  exam- 
ination of  a  large  amount  of  material  bearing  upon  this  and  its 
closely-related  forms. 


'  For  a  list  of  the  species  and    subspecies   of  Neotovta   described    prior   to   July  6,  1894,  see 
Abstr.  Free.  Linn.  Soc.  New  York,  No.  6,  pp.  34,  35,  July,  1894. 


291 


246     Bulletin  American  Museum  of  Natural  History.    [Vol.  VI,] 


EXPLANATION  OF  PLATE  IV. 

Figures  all  Natural  size. 

Neotoma  micropus  Baird.  Showing  cranial  variations  due  to  age  and 
individualism.  (Unless  otherwise  stated,  the  specimens  are  from  Rockport, 
Texas.) 

Figs.  1-8.  Dorsal  aspect  of  skull,  showing  gradual  change  in  form  with  age, 
and  especially  in  the  form  and  relative  size  of  the  interparietal.  Fig.  i.  No. 
5834,  S  juv.  (suckling).  Fig.  2,  No.  2975,  $  juv.  (nearly  sexually  adult). 
Corpus  Christi,  Texas.  Fig.  3,  No.  5841,  ?  ad.  Fig.  4,  No.  4480,  f,  ad. 
Fig.  5,  No.  2958,  c?  ad^.,  Corpus  Christi.  Fig.  6,  No.  4479,  c5  ad.  Fig.  7, 
No.  4477,    ?  ad.     Fig.  8,  No.  4478,    6   ad. 

Figs.  9-1 1.     vSkuU  in  profile,  to  show  change  of  form  with  growth.     Fig.  9, 
No.    5834,    S    juv.    (nursling).      Fig.    10,    No.    44S0,    _<;    ad.    (rather   young). 
Fig.  II,  No.  4478,  (5  ad.  (very  old). 

Figs.  12-15.  Ventral  aspect,  showing  variations  in  postpalatal  region  due 
to  age.  Fig.  12,  No.  5834,  ?  juv.  (nursling).  Fig.  13,  No.  5841,  ?  ad.  (young- 
adult).  Y\g.  14,  No.  2958,  Corpus  Christi,  (5  ad.  (very  old).  Fig.  15,  No. 
1456,  Neotoma  cinerea  occidentalis,  (?ad..  Ducks,  B.  C.  (for  comparison  with 
N.  iincroptis). 

Figs.  16,  17.  To  show  extremes  of  individual  variation  in  relative  posterior 
extension  of  nasals  and  ascending  branches  of  premaxillie.  Locality,  Corpus 
Christi.  Texas.     Fig.  16,  No.  2958,  ,^  ad.     Fig.  17,  No.  2948,    $  ad. 

Figs.  18,  19.  To  show  extremes  of  individual  variation  in  posterior  border 
of  frontals.  Locality,  Corpus  Christi,  Texas.  Fig.  18,  No.  2949,  ,5  ad.  Fig. 
19,  No.  2951,   .^  ad. 

Figs.  20-23.  To  show  individual  variation  in  the  size  and  form  of  the  inter- 
parietal. Specimens  all  from  Corpus  Christi,  Texas.  Fig.  20,  No.  2949,  f,  ad. 
Fig.  21,  No.  2948,  $  ad.     Fig.  22,  No.  2952,  .5  ad.     Fig.  23,  No.  2945,  S  ad. 

Note. — If  the  Brownsville,  Texas,  series  of  specimens  had  also  been  included, 
the  range  of  individual  variation  would  have  been  considerably  increased. 


292 


HiLi..  A.  M.  X.  H. 


Vol..  VI.,  Pl.  IV. 


Neotoma  micropus. 

Fiarures  nat.  size. 


293 


MATURATIONAL  AND  SEASONAL  MOLTS  IN  THE 
GOLDEN  MOUSE,  OCHROTOMYS  NUTTALLI 

Donald  W.  Linzey  and  Alicia  V.  Linzey 

Abstract. — The  adult  pelage  of  the  golden  mouse  {Ochrotomys  mittalli)  is 
attained  by  a  single  maturational  molt.  Data  on  the  post-juvenile  molt  were 
obtained  from  96  young  golden  mice.  This  molt  began  on  the  ventral  surface  and 
spread  dorsally,  meeting  in  the  dorsal  midline.  It  then  proceeded  anteriorly  and 
posteriorly.  The  average  age  at  which  male  golden  mice  began  molting  was  36 
days,  whereas  that  of  females  was  38  days.  The  average  duration  of  molt  for  the 
sexes  was  29  days  and  25  days,  respectively.  Golden  mice  undergo  two  seasonal 
molts — spring  and  fall.  Data  were  obtained  from  36  mice.  Tlie  winter  pelage 
was  generally  much  darker  than  the  summer  pelage.  Both  spring  and  fall  molts 
were  more  irregular  than  the  post-juvenile  molt,  and  the  spring  molt  tended  to  be 
more  irregular  than  the  fall  molt.  Young  golden  mice  born  after  1  October  and 
8  April  appeared  to  combine  the  post-juvenile  and  seasonal  molt.  Hair  replace- 
ment was  more  irregular  than  during  the  normal  post-juvenile  molt. 

During  the  course  of  a  study  on  the  ecology  and  Hfe  history  of  the  golden 
mouse,  Ochrotomys  mittalli  nuttaUi,  in  the  Great  Smoky  Mountains  National 
Park  (Linzey,  1966),  considerable  data  were  obtained  on  pelage  changes. 
The  limited  data  presented  by  Layne  (1960)  have  been  the  only  published 
infomiation  concerning  molt  in  this  species. 

Maturational  Molt 

The  adult  pelage  of  the  golden  mouse  is  attained  after  a  single  matura- 
tional molt.  Data  on  the  post-juvenile  molt  were  obtained  from  96  young 
golden  mice.  Eighty-four  of  these  mice  were  raised  in  captivity.  Data  from 
the  remaining  12  individuals  were  obtained  from  field  observations. 

The  molt  from  the  golden-brown  juvenile  pelage  to  the  golden-orange  adult 
pelage,  although  varying  in  details,  followed  a  definite  pattern  ( Fig.  1 ) .  The 
first  indication  of  the  beginning  of  the  dorsal  molt  was  the  appearance  of 
new  golden  fur  along  the  line  separating  the  golden-brown  dorsal  fur  from 
the  white  fur  of  the  ventral  surface.  The  replacement  of  the  juvenile  pelage 
progressed  dorsally  on  both  sides  and  met  on  the  dorsal  midline  forming  a 
continuous  band  of  new  fur.  The  molt  then  proceeded  anteriorly  between  the 
ears  and  onto  the  head,  while  posteriorly,  it  joined  the  molt  proceeding 
dorsally  near  the  thighs.  By  this  time,  new  fur  had  appeared  on  the  sides 
of  the  face  and  just  anterior  to  the  ears.  The  molt  along  the  sides  of  the  body 
had  nearly  been  completed  by  this  time.  The  last  two  areas  in  which  the  fur 
was  replaced  were  the  top  of  the  head  and  the  base  of  the  tail.  In  some 
individuals,  the  new  fur  first  appeared  just  in  back  of  the  front  leg.  It  pro- 
ceeded both  posteriorly  and  dorsally  and  formed  a  band  of  new  fur  just 
behind  the  ears.  The  molt  proceeding  posteriorly  then  covered  the  remainder 
of  the  body. 

This  pattern  of  molt  generally  agrees  with  that  described  for  Peromyscus 

236 


294 


May  1967  LINZEY  AND  LINZEY— MOLT  OF  GOLDEN  MOUSE 


237 


^^^^.iirf^J^ 


Fig.   L — Sequence  of  post-juvenile  molt  on  the  dorsum  in  Ochrotomys  nuttalli.    Shaded 
portions  represent  areas  of  active  hair  replacement.    Stippled  areas  represent  adult  pelage. 


295 


238  JOURNAL  OF  MAMMALOCiY  Vol.  48,  No.  2 

Taule   1. — Duration   of  post-juvenile   molt  and  average  age  at  beginning  and  ending  of 
molt  in  34  captive  golden  mice  (Range  of  values  in  parentheses). 

Males  (15)  Females  (19) 

Duration  29  days   (14-45)  25  days   (12-49) 

Beginning  36  days   (33-42)  38  days   (31-47) 

Ending  64  days   (51-87)  63  days   (51-84) 

tmei  ( Hoffmeister,  1944),  Feromyscus  gossypinus  (Pournelle,  1952)  and 
Peromysctis  boy  lei  (Brown,  1963).  It  differs  from  that  reported  for  Pero- 
myscus  leucopiis  noveboracensis  (Gottschang,  1956). 

Data  on  the  begmning,  ending,  and  duration  of  the  post-juvenile  molt  on 
the  dorsum  in  male  and  female  golden  mice  are  compared  in  Table  1.  The 
average  duration  of  molt  for  males  was  slightly  longer  than  for  females.  The 
shortest  time  recorded  was  between  12  and  14  days,  whereas  the  maximum 
time  required  was  about  49  days.  Approximately  3.5  weeks  are  required  for 
most  Peromysciis  leucopus  noveboracensis  to  attain  their  full  adult  coat 
according  to  Gottschang  ( 1956 ) .  He  recorded  a  minimum  duration  of  12  days 
for  captive  individuals  and  10  days  for  one  wild  mouse  to  undergo  the  com- 
plete molt;  the  maximum  number  of  days  required  was  about  36. 

In  the  field,  animals  undergoing  various  stages  of  maturational  molt  were 
recorded  in  June  (1),  July  (1),  August  (2),  and  December  (8).  These  mice 
were  between  150  mm  and  164  mm  in  total  length  (mean,  156  mm).  In  the 
captive  population,  male  golden  mice  began  molting  when  their  total  length 
was  149  mm,  whereas  females  averaged  146  mm.  At  the  completion  of  molt, 
their  measurements  averaged  163  mm  and  160  mm,  respectively.  From  these 
data,  it  appears  that  both  wild  and  captive  individuals  molted  at  approxi- 
mately the  same  body  size,  although  it  is  not  known  whether  they  were  the 
same  age. 

The  youngest  individuals  in  captivity  to  begin  molting  during  the  current 
study  were  31  days  of  age.  Layne  (1960)  recorded  one  young  Ochrotomys 
molting  at  31  days  of  age  with  the  molt  apparently  being  complete  10  days 
later.  Molting  was  in  progress  in  one  four  week  old  mouse,  while  in  another 
of  the  same  age,  it  had  not  yet  begun  (Layne,  1960).  Collins  (1918)  reported 
that  the  transition  from  juvenile  to  post-juvenile  pelage  in  Peromyscus  usually 
began  at  6  weeks  and  was  completed  about  8  weeks  later.  The  earliest  age 
at  which  Peromyscus  leucopus  noveboracensis  began  molting  was  38  days 
(Gottschang,  1956).  These  were  all  males.  The  youngest  female  to  begin 
molting  was  40  days  of  age.  Ninety-five  per  cent  of  his  mice  of  both  sexes 
started  the  pelage  change  between  the  ages  of  40  and  50  days.  Young  Pero- 
myscus gossypinus  began  molting  when  they  were  between  34  and  40  days 
of  age  (Pournelle,  1952). 

Gottschang  ( 1956 )  found  that,  in  general,  mice  of  the  same  sex  in  a  single 
litter  started  molting  simultaneously.  However,  in  every  case  where  a  dif- 
ference did  occur,  he  found  that  the  males  started  to  molt  first.   In  the  current 


296 


May  1967  LINZEY  AND  LINZEV— MOLT  OF  C;OLDE.\   MOUSE  239 

study,  the  males  in  13  out  of  21  litters  containing  mice  of  both  sexes  began 
molting  before  the  females,  whereas  the  females  began  molting  first  in  three 
litters.  The  initiation  of  molt  was  simultaneous  in  the  remaining  five  litters. 
The  progression  of  the  ventral  molt  was  studied  in  seven  individuals  (four 
males,  three  females).  The  white  belly  fur  was  dyed  purple  by  the  stain 
Nyanzol  A  (20  g  per  liter  of  water-hydrogen  peroxide  mixture  in  ratio  of 
two  to  one)  and  replacement  by  new  hairs  was  followed.  The  ventral  molt 
began  approximately  2-4  days  before  the  dorsal  molt.  Hair  replacement 
occurred  first  in  the  center  of  the  belly  and  continued  laterally,  and  then 
dorsally  into  the  golden  fur.  Simultaneously,  new  hair  appeared  over  the 
entire  chest  and  abdomen.  The  last  areas  to  acquire  new  pelage  were  the 
throat  and  the  ventral  bases  of  the  hind  limbs.  The  ventral  molt  was  complete 
at  about  the  time  that  the  dorsal  molt  covered  the  entire  back  ( Fig.  1 ) , 

Seasonal  Molt 

Mice  of  the  genus  Peromyscus  are  generally  considered  to  undergo  one 
annul  adult  molt  in  autumn  (Collins,  1923).  However,  Osgood  (1909)  and 
Brown  ( 1963 )  recorded  two  annual  molts  in  Peromyscus  melanotis  and  Pero- 
myscus boylei,  respectively. 

Golden  mice  in  the  Great  Smoky  Mountains  National  Park  apparently  un- 
dergo two  annual  molts.  These  take  place  during  the  spring  (April-June)  and 
fall  ( October-December ) .  The  difference  between  summer  and  winter  pelage 
was  clearly  distinguishable  with  the  unaided  eye.  The  winter  pelage  was 
much  darker  than  the  usual  summer  pelage,  especially  on  the  mid-dorsum. 
Osgood  (1909)  noted  that  winter  specimens  of  Peromyscus  melanotis  pos- 
sessed a  paler  colored  pelage,  whereas  summer  specimens  were  in  a  dark 
pelage.  The  fall  molt  of  P.  boylei  was  characterized  by  the  replacement  of  a 
bright  cinnamon-brown  pelage  by  a  more  drab,  brown  winter  pelage  (Brown, 
1963). 

Nineteen  of  21  adult  golden  mice  in  captivity  underwent  a  fall  molt 
between  October  20  and  December  24.  A  total  of  10  adult  golden  mice  were 
observed  in  the  wild  between  December  12-17.  Six  of  these  were  molting; 
four  already  had  the  winter  pelage.  The  fall  molt  appeared  to  be  more 
irregular  than  the  post-juvenile  molt.  In  several  animals,  it  began  near  the 
hind  leg,  covered  the  rump  and  then  progressed  anteriorly  to  the  head. 
Replacement  of  the  hair  was  completed  first  over  the  posterior  half  of  the 
body.  This  separated  the  two  remaining  areas  of  molt — the  base  of  the  tail 
and  the  head.  The  replacement  of  fur  at  the  base  of  the  tail  was  completed 
shortly  thereafter.  The  final  area  of  molt  was  on  the  head  between  the  ears, 
and  this  sometimes  required  several  weeks  for  completion.  This  is  in  contrast 
to  the  post-juvenile  molt,  where  the  last  area  of  molt  in  all  of  the  animals 
was  at  the  base  of  the  tail. 

The  spring  molt  must  have  occurred  between  1  April  and  15  June.  All  wild 
individuals  observed  between  26  March  and  1  April  1964  still  retained  their 


297 


240  JOURNAL  OF  MAMMALOGY  Vol.  48,  No.  2 

winter  pelage.  By  15  June,  all  adult  golden  mice  had  either  already  com- 
pleted their  spring  molt  or  were  very  near  completion.  Seventy-four  per  cent 
(23)  of  the  adult  individuals  in  the  captive  population  molted  during  the 
spring.  Of  those  molting,  83%  (19)  did  so  between  15  May  and  30  June. 
As  in  the  fall  molt,  the  pattern  was  irregular.  Hair  replacement  occurred  in 
patches  along  the  sides  and  across  the  shoulders,  and  a  simultaneous  molt 
of  the  entire  dorsum  took  place  in  only  five  of  31  individuals  ( 16% ) .  In  the 
cases  where  this  molt  was  complete,  it  followed  a  more  regular  pattern,  with 
hair  replacement  occurring  last  on  the  nape  of  the  neck. 

Gottschang  ( 1956 )  noted  no  difference  in  the  onset,  progress  or  length  of 
time  required  for  the  pelage  change  between  spring-,  summer-,  or  fall-born 
litters  of  Pcromyscus  leiicopus.  During  the  current  study,  however,  golden 
mice  born  after  1  October  and  8  April  appeared  to  combine  the  post-juvenile 
molt  and  seasonal  molt.  The  process  of  hair  replacement  was  more  irregular 
than  during  the  normal  post-juvenile  molt.  The  molt  began  at  a  point  just 
behind  the  front  legs,  as  in  the  regular  post-juvenile  molt.  It  then  proceeded 
dorsally  and  posteriorly  at  approximately  equal  rates.  During  the  combined 
fall  molt  (post- juvenile  plus  fall  molt),  the  replacement  of  hair  at  the  base  of 
the  tail  was  completed  prior  to  the  completion  of  molt  on  the  head  in  all  cases. 
In  this  respect,  this  combined  molt  was  more  similar  to  the  regular  seasonal 
molt  than  to  the  regular  post-juvenile  molt.  Upon  completion  of  this  molt, 
the  mice  had  acquired  the  typical  dark  winter  pelage.  However,  during  the 
combined  spring  molt  (post-juvenile  plus  spring  molt),  hair  replacement  was 
completed  last  at  either  the  tail  or  head  regions. 

On  the  average,  those  animals  born  after  1  October  began  molt  at  a  later 
age  than  did  those  animals  bom  earlier  in  the  breeding  season.  Males  in  this 
group  began  molting  at  an  average  age  of  37  days,  whereas  spring  and 
summer-born  males  began  at  35  days  of  age.  Females  born  after  1  October 
began  molting  at  an  average  age  of  43  days,  while  females  bom  earlier  in 
the  season  began  molting  at  an  average  age  of  37  days. 

Acknowledgments 

We  thank  Dr.  W.  Robert  Eadie  of  Cornell  University  for  his  advice  and  criticism  of  the 
manuscript.  We  gratefully  acknowledge  the  financial  assistance  provided  by  The  Society 
of  the  Sigma  Xi  and  the  cooperation  of  the  National  Park  Service. 

Literature  Cited 

Brown,    L.    N.     1963.     NLaturational    and   seasonal   molts    in    Peromyscus   boylei.     Amer. 

Midland  Nat.,  70:   466-469. 
Collins,   H.   H.      1918.     Studies   of  normal  molt  and  of  artificially  induced  regeneration 

of  pelage  in  Peromyscus.    J.  Exp.  Zool.,  27:  73-99. 
.      1923.     Studies  of  the  pelage  phases   and  nature  of  color  variations  in  mice  of 

the  genus  Peromyscus.    J.  Exp.  Zool.,  38:   45-107. 
Gottschang,    J.    L.     1956.     Juvenile    molt    in    Peromyscus    leucopus   noveboracensis.     J. 

Mamm.,  37:   516-520. 
HoFFMEiSTER,   D.   F.      1944.     Phylogeny  of  the   Nearctic   cricetine   rodents,   with   especial 


298 


May  1967  LINZEY  AND  LINZEY— MOLT  OF  GOLDEN  MOUSE  241 

attention    to    variation    in    Peromtjscus   truei.     Ph.D.    thesis,    Univ.    Cahfornia, 

406  pp. 
Layne,  J.   N.      1960.     Tlu>  growth  and  development  of  younp  golden   mice,   Ochrotomijs 

mittalU.    Quart.  J.  Fla.  Acad.  Sci.,  23:   36-58. 
LI^fZEY,    D.    W.      1966.     The    life    history,    ecology    and    behavior    of    the    golden    mouse, 

Ochrotomijs  n.  nuttalli,  in   the  Great   Smoky  Mountains   National   Park.   Ph.D. 

thesis,  Cornell  Univ.,   170  pp. 
Osgood,  W.  H.      1909.     Revision  of  the  mice  of  the  American  genus  Peromyscus.    N.  Amer. 

Fauna,  28:    1-285. 
PouRNELLE,  G.   H.      1952.     Reproduction  and  early  post-natal  development  of  the  cotton 

mouse,  Peromyscus  gossypinus  gossypinus.     J.   Mamm.,  33:    1-20. 

Division   of   Biological   Sciences,   Cornell   University,   Ithaca,   New   York.    Accepted   16 
January  1967. 


299 


SECTION  4— ECOLOGY  AND  BEHAVIOR 

Ecology  and  behavior  comprise  amazingly  varied,  active,  and  expanding 
fields.  Probably  most  current  mammalogical  publications  relate  to  one  or  both 
of  these  disciplines.  Ecology  particularly  is  of  special  importance  to  man  owing 
to  his  increasing  awareness  of,  and  concern  for,  his  own  environment  and  such 
problems  as  the  need  to  regulate  human  populations  and  to  reduce  pollution  of 
air  and  water.  The  papers  selected  here  can  suggest  to  the  perspective  reader 
some  basic  ecological  principles  that  apply  to  man  himself. 

A  host  of  topics  other  than  those  we  were  able  to  include  in  our  selection 
come  to  mind  when  the  ecological  literature  is  contemplated — topics  such  as 
food  habits  as  learned  from  stomach  contents  or  droppings,  or  small  mammal 
populations  as  censused  by  various  methods  (one  such  method  is  the  study  of 
bones  in  pellets  regurgitated  by  owls,  which  are  very  eflBcient  "mouse  traps" ) . 
Long  term  cycles  in  populations  and  daily  cycles  in  activity  have  had  their 
share  of  ecological  work  also,  but  lack  of  space  precludes  further  discussion 
of  these  topics. 

A  large  and  well-documented  textbook  on  animal  ecology  is  that  by  Allee 
et  al.  ( 1949 ) .  Three  books  relating  to  animal  populations  and  factors  that  may 
regulate  them  are  by  Lack  (1954),  Andrewartha  and  Birch  (1954),  and 
Wynne-Edwards  (1962).  Their  views  differ  and  are  interesting;  their  exam- 
ples, however,  are  largely  non-mammalian. 

The  older  term  "natural  history"  is  perhaps  a  broader  concept  than  ecology, 
but  the  older  naturalists  were  deeply  committed  to  the  types  of  studies  that 
have  come  to  be  called  ecological,  as  well  as  ethological  (a  word  currently 
used  for  studies  of  behavior ) .  In  the  latter  context,  Ewer's  ( 1968 )  recent  book 
entitled  Ethology  of  Mammals  is  of  note  to  the  student  interested  in  a  general 
coverage  of  the  field,  and  Maternal  Behavior  in  Mammals  (Rheingold,  1963) 
also  is  useful. 

Papers  reproduced  here  illustrate  concepts  such  as  territoriality  and  home 
range  (applied  to  mammals  in  the  paper  by  Burt),  relatively  larger  studies 
( note  the  numbers  of  specimens  mentioned  in  Frank's  paper  for  example )  that 
provided  a  firm  statistical  base  and  sound  quantitative  results,  and  the  applica- 
tion of  experimental  procedures  (as  in  the  manipulation  of  rats  in  city  blocks 
reported  by  Davis  and  Christian  or  the  tests  run  by  McCarley  in  compart- 
mented  cages).  The  application  of  newer  techniques  such  as  Pearson's  traflBc 
counter  for  mouse  runways,  the  squirrel  radio  described  by  Beal,  and  auto- 
matic recording  equipment  of  various  types,  all  have  contributed  to  advances 
in  ecology  and  ethology.  The  recent  study  by  Estes  and  Goddard  of  the 
African  wild  dog  will  serve  to  remind  the  reader  that  careful  observational 
methods  such  as  were  used  so  effectively  by  older  field  naturalists  certainly 
have  not  been  supplanted,  but  only  expanded  and  supplemented. 

Recent  field  studies  dealing  with  primates  have  relied  heavily  on  good 
observational  techniques.  Schaller's  (1963)  book  on  the  gorilla  is  a  good 
example.  Other  recent  workers  have  studied  baboons,  chimpanzees,  langurs, 
and  other  primates  in  similar  ways.   A  report  by  Struhsaker  (1967),  not  here 


301 


reproduced,  on  vervet  monkeys  is  a  good  example  of  a  shorter  paper  on  primate 
behavior  in  the  field. 

The  short  paper,  here  included,  by  Miller,  written  more  than  60  years  ago, 
was  based  on  limited  data,  but  reflects  a  thoughtful  and  somehow  modern  way 
of  looking  at  the  problem  of  bat  migration,  about  which,  incidentally,  little  is 
known  even  today. 

Ecological  problems  may  be  approached  at  different  levels  of  inclusiveness. 
For  example,  the  relationships  of  all  species  of  plants  and  animals  in  an  entire 
community  may  be  studied.  Such  a  broad  approach  to  entire  ecosystems 
merges  imperceptibly  with  problems  concerning  factors  that  limit  distribu- 
tions, hence  to  ranges  of  species  and  faunal  and  zoogeographic  problems.  A 
short  paper  by  L.  R.  Dice  (1931),  not  included  here,  on  the  relation  of  mam- 
mahan  distribution  to  vegetation  types  is  a  classic,  for  here  he  adopted  the 
term  "Biotic  Province"  for  a  major  concept  that  he  and  others  expanded  in 
later  American  zoogeographic  studies.  Even  an  analysis  of  a  few  species  such 
as  Brown's  study  of  six  species  of  shrews  has  obvious  zoogeographic  relevance. 
At  a  less  inclusive  level  the  ecological  relationships  of  a  single  species  may  be 
studied.  This  approach  is  called  autecology  as  opposed  to  community  or  syn- 
ecological  studies.  If  we  restrict  ourselves  further  to  the  environmental  rela- 
tionships of  individual  animals,  we  find  our  studies,  again  by  gradual  stages, 
merge  with  those  that  are  primarily  physiological  and  behavioral.  Physiologi- 
cal techniques  also  enter  directly  into  the  study  of  ecosystems  when  energy 
flow  is  considered,  as  often  is  the  case  in  recent  studies.  Lyman's  paper,  repro- 
duced here,  on  hibernators  relates  to  energy,  its  sources,  and  its  dissipation. 
Two  noteworthy  contributions  to  the  study  of  hibernation  are  by  Lyman  and 
Dawe  (1960)  and  Kayser  (1961);  these  and  other  studies  are  summarized  and 
cited  in  the  textbook  by  Davis  and  Golley  ( 1963 ) . 

Some  of  the  more  important  journals  that  regularly  publish  contributions 
relating  to  ecology  and  behavior,  and  of  which  the  serious  student  should  be 
aware,  are  Animal  Behavior,  Behavior,  Ecological  Monographs,  Ecology, 
Journal  of  Animal  Ecology,  and  Zeitschrift  fur  Tierpsychologie. 


302 


MORTALITY  PATTERNS  IN  MAMMALS 

Graeme  Caugiiley 

Forest  Research  Instilute,  New  Zealand  Forest  Service,  Rotorua,  and  Zoology  Department, 

Canterbury  University,  New  Zealand 

(Accepted  for  publication  December  8,  1965) 

Abstract.  Methods  of  obtaining  life  table  data  are  outlined  and  the  assumptions  implicit 
in  such  treatment  are  defined.  Most  treatments  assume  a  stationary  age  distribution,  but 
published  methods  of  testing  the  stationary  nature  of  a  single  distribution  are  invalid.  Samples 
from  natural  populations  tend  to  be  biased  in  the  young  age  classes  and  therefore,  because 
it  is  least  affected  by  bias,  the  mortality  rate  curve  (q^)  is  the  most  efficient  life  table  series 
for  comparing  the  pattern  of  mortality  with  age  in  different  populations. 

A  life  table  and  fecundity  table  are  presented  for  females  of  the  ungulate  Heniitragiis 
jcmlahiens,  based  on  a  population  sample  that  was  first  tested  for  bias.  They  give  estimates 
of  mean  generation  length  as  S.4  yr,  annual  mortality  rate  as  0.25,  and  mean  life  expectancy 
at  birth  as  3.5  yr. 

The  life  table  for  Hemitragus  is  compared  with  those  of  Ovis  aries,  O.  dalli,  man,  Rattus 
norvegiciis,  Microtns  agrestis,  and  M.  orcadensis  to  show  that  despite  taxonomic  and  ecological 
differences  the  life  tables  have  common  characteristics.  This  suggests  the  hypotheses  that 
most  mammalian  species  have  life  tables  of  a  common  form,  and  that  the  pattern  of  age- 
specific  mortality  within  species  assumes  an  approximately  constant  form  irrespective  of  the 
proximate  causes  of  mortality. 


Introduction 

Most  studies  in  population  ecology  include  an 
attemin  to  determine  mortality  rates,  and  in  many 
cases  rates  are  given  for  each  age  class.  This  is 
no  accident.  Age-specific  mortality  rates  are 
usually  necessary  for  calculating  reproductive 
values  for  each  age  class,  the  ages  most  susceptible 
to  natural  selection,  the  population's  rate  of  in- 
crease, mean  life  expectancy  at  birth,  mean  gen- 
eration length,  and  the  percentage  of  the  popula- 
tion that  dies  each  year.     The  importance  of  these 


statistics  in  the  fields  of  game  management,  basic 
and  applied  ecology,  and  population  genetics  re- 
quires no  elaboration. 

The  pattern  of  changing  mortality  rates  with 
age  is  best  expressed  in  the  form  of  a  life  table. 
These  tables  usually  present  the  same  information 
in  a  variety  of  ways : 

1 )  Survivorship  (/x)  :  this  series  gives  the  prob- 
ability at  birth  of  an  individual  surviving  to  any 
age,  X  (/x  as  used  here  is  identical  with  P^  of 
Leslie,  Venables  and  Venables  1952).     The  ages 


303 


Autumn  1966 


MORTALITY    PATTERNS    IN    MAMMALS 


907 


are  most  conveniently  spaced  at  regular  intervals 
such  that  the  values  refer  to  survivorship  at  ages 
0,  1,  2  etc.  yr,  months,  or  some  other  convenient 
interval.  The  probability  at  birth  of  living  to  birth 
is  obviously  unity,  but  this  initial  value  in  the 
series  need  not  necessarily  be  set  at  1  ;  it  is  often 
convenient  to  multiply  it  by  1,000  and  to  increase 
proportionately  the  other  values  in  the  series.  If 
this  is  done,  survivorship  can  be  redefined  as  the 
number  of  animals  in  a  cohort  of  1,000  (or  any 
other  number  to  which  the  initial  value  is  raised ) 
that  survived  to  each  age  x.  In  this  way  a  ^/^ 
series  is  produced,  where  k  is  the  constant  by  which 
all  h  values  in  the  series  are  multiplied. 

2)  Mortality  (c/x)  :  the  fraction  of  a  cohort  that 
dies  during  the  age  interval  x,  x  +  1  is  designated 
dx-  It  can  be  defined  in  terms  of  the  individual  as 
the  probability  at  birth  of  dying  during  the  interval 
X,  X  +  1.  As  a  means  of  eliminating  decimal 
points  the  values  are  sometimes  multiplied  by  a 
constant  such  that  the  sum  of  the  d^  values  equals 
1,000.  The  values  can  be  calculated  from  the  h 
series  by 

c'x  =  'x  —  'x  +  l 

3)  Mortality  rate  {q-s.)  '■  the  mortality  rate  q 
for  the  age  interval  x,  x  +  1  is  termed  ^x-  It  is 
calculated  as  the  number  of  animals  in  the  cohort 
that  died  during  the  interval  x,  x  -f  1.  divided  by 
the  number  of  animals  alive  at  age  x.  This  value 
is  usually  expressed  as  l,000(7x,  the  number  of 
animals  out  of  1,000  alive  at  age  x  which  died 
before  x  -f-  1- 

These  are  three  ways  of  presenting  age-specific 
mortality.  Several  other  methods  are  available — 
e.g.  survival  rate  {px),  life  expectancy  (tx)  and 
probability  of  death  (Qx) — but  these  devices  only 
present  in  a  different  way  the  information  already 
contained  in  each  of  the  three  series  previously 
defined.  In  this  paper  only  the  Ix,  dx  and  qx  series 
will  be  considered. 

Methods  of  Obtaining  Mortality  Data 

Life  tables  may  be  constructed  from  data  col- 
lected in  several  ways.     Direct  methods  : 

1 )  Recording  the  ages  at  death  of  a  large  num- 
ber of  animals  born  at  the  same  time.  The  fre- 
quencies of  ages  at  death  form  a  kdx  series. 

2)  Recording  the  number  of  animals  in  the 
original  cohort  still  alive  at  various  ages.  The 
frequencies  from  a  klx  series. 


Approximate  methods : 

3)  Recording  the  ages  at  death  of  animals 
marked  at  birth  but  whose  births  were  not  coeval. 
The  frequencies  form  a  kdx  series. 


4)  Recording  ages  at  death  of  a  representative 
sample  by  ageing  carcasses  from  a  population  that 
has  assumed  a  stationary  age  distribution.  Small 
fluctuations  in  density  will  not  greatly  affect  the 
results  if  these  fluctuations  have  an  average  wave 
length  considerably  shorter  than  the  period  over 
which  the  carcasses  accumulated.  The  frequencies 
form  a  kdx  series. 

5 )  Recording  a  sample  of  ages  at  death  from 
a  population  with  a  stationary  age  distribution, 
where  the  specimens  were  killed  by  a  catastrophic 
event  (avalanche,  flood,  etc.)  that  removed  and 
fixed  an  unbiased  sample  of  ages  in  a  living  popu- 
lation. In  some  circumstances  (outlined  later)  the 
age  frequencies  can  be  treated  as  a  klx  series. 

6)  The  census  of  ages  in  a  living  population, 
or  a  sample  of  it,  where  the  population  has  assumed 
a  stationary  age  distribution.  Whether  the  speci- 
mens are  obtained  alive  by  trapping  or  are  killed 
by  unselective  shooting,  the  resultant  frequencies 
are  a  sample  of  ages  in  a  living  population  and 
form  a  klx  series  in  certain  circumstances. 

Methods  1  to  3  are  generally  used  in  studies  of 
small  mammals  while  methods  4  to  6  are  more 
commonly  used  for  large  mammals. 

Tests  for  Stationary  Age  Distribution 

Five  methods  have  been  suggested  for  deter- 
mining whether  the  age  structure  of  a  sample  is 
consistent  with  its  having  been  drawn  from  a 
stationary  age  distribution : 

a)  Comparison  of  the  "mean  mortality  rate," 
calculated  from  the  age  distribution  of  the  sample, 
with  the  proportion  represented  by  the  first  age 
class  (Kurten  1953,  p.  51). 

b)  Comparison  of  the  annual  female  fecundity 
of  a  female  sample  with  the  sample  number  multi- 
plied by  the  life  expectancy  at  birth,  the  latter 
statistic  being  estimated  from  the  age  structure 
(Quick  1963,  p.  210). 

c)  Calculation  of  instantaneous  birth  rates  and 
death  rates,  respectively,  from  a  sample  of  the 
population's  age  distribution  and  a  sample  of  ages 
at  death  (Hughes  1965). 

d )  Comparison  of  the  age  distribution  with  a 
prejudged  notion  of  what  a  stationary  age  distri- 
bution should  be  like  (Breakey  1963). 

e)  Examination  of  the  "/x"  and  "dx"  series, 
calculated  from  the  sampled  age  distribution,  for 
evidence  of  a  common  trend  (Quick  1963,  p.  204). 

Methods  a  to  c  are  tautological  because  they 
assume  the  sampled  age  distribution  is  either  a  klx 
or  kdx  series  ;  method  d  assumes  the  form  of  the 
life  table,  and  e  makes  use  of  both  assumptions. 

These  ways  of  judging  the  stationary  nature  of 


304 


908 

a  population  are  invalid.  But  I  intend  something 
more  general  than  the  simple  statement  that  these 
five  methods  do  not  test  what  they  are  supposed 
to  test.  Given  no  information  other  than  a  single 
age  distribution,  it  is  theoretically  impossible  to 
prove  that  the  distribution  is  from  a  stationary 
population  unless  one  begins  from  the  assumption 
that  the  population's  survival  curve  is  of  a  par- 
ticular form.  If  such  an  assumption  is  made,  the 
life  table  constructed  from  the  age  frequencies 
provides  no  more  information  than  was  contained 
in  the  original  premise. 

Mortality  Samples  and  Age  Structure 
Samples 

Methods  4  to  6  for  compiling  life  tables  are 
valid  only  when  the  data  are  drawn  from  a  sta- 
tionary age  distribution.  This  distribution  results 
when  a  population  does  not  change  in  size  and 
where  the  age  structure  of  the  population  is  con- 
stant with  time.  The  concept  has  developed  from 
demographic  research  on  man  and  is  useful  for 
species  which,  like  man,  have  no  seasonally  re- 
stricted period  of  births. 

Populations  that  have  a  restricted  season  of 
births  present  difficulties  of  treatment,  some  of 
which  have  been  discussed  by  Leslie  and  Ranson 
(1940).  Very  few  mammals  breed  at  the  same 
rate  throughout  the  year,  and  the  stationary  age 
distribution  must  be  redefined  if  it  is  to  include 
seasonal  breeders.  For  species  with  one  restricted 
breeding  season  each  year,  a  stationary  population 
can  be  defined  as  one  that  does  not  vary  either  in 
numbers  or  age  structure  at  successive  points  in 
time  spaced  at  intervals  of  1  yr.  The  stationary 
age  distribution  can  then  be  defined  for  such  popu- 
lations as  the  distribution  of  ages  at  a  given  time 
of  the  year.  Thus  there  will  be  an  infinite  num- 
ber of  different  age  distributions  according  to  the 
time  of  census,  other  than  in  the  exceptional  case 
of  a  population  having  a  constant  rate  of  mor- 
tality throughout  life. 

The  distribution  of  ages  in  a  stationary  popula- 
tion forms  a  kl^;  series  only  when  all  births  for  the 
year  occur  at  an  instant  of  time  and  the  sample  is 
taken  at  that  instant.  This  is  obviously  impossible, 
but  the  situation  is  approximated  when  births 
occur  over  a  small  fraction  of  the  year.  If  a  popu- 
lation has  a  restricted  season  of  births,  the  age 
structure  can  be  sampled  over  this  period  and  at 
the  same  time  the  number  of  live  births  produced 
by  a  hypothetical  cohort  can  be  calculated  from 
the  number  of  females  either  pregnant  or  suckling 
young.  In  this  way  a  set  of  data  closely  approxi- 
mating a  kl^  series  can  be  obtained. 


GRAEME  CAUGHLEY 


Ecology,  Vol.  47,  No.  6 


If  an  age  distribution  is  sampled  halfway  be- 
tween breeding  seasons,  it  cannot  be  presented  as 
a  A;/x  series  with  x  represented  as  integral  ages  in 
years.  With  such  a  sample  (making  the  usual 
assumptions  of  stability  and  lack  of  bias)  neither 
/x  nor  dx  can  be  established,  but  Qx  values  can  be 
calculated  for  each  age  interval  x  -(-  3^,  x  +  l^^. 
The  age  frequencies  from  a  population  with  a  con- 
tinuous rate  of  breeding  are  exactly  analogous ; 
they  do  not  form  a  kl^  series  but  can  be  treated  as 
a  series  of  the  form 

^(/x  +  /x  +  l)/2 

This  series  does  not  allow  calculation  of  l^  values 
from  birth  unless  the  mortality  rate  between  birth 
and  the  midpoint  of  the  first  age  interval  is  known. 

Because  a  sample  consists  of  dead  animals,  its 
age  frequencies  do  not  necessarily  form  a  mor- 
tality series.  The  kdx  series  is  obtained  only  when 
the  sample  represents  the  frequencies  of  ages  at 
death  in  a  stationary  population.  Many  published 
samples  treated  as  if  they  formed  a  kdx  series  are 
not  appropriate  to  this  form  of  analysis.  For 
instance,  if  the  animals  were  obtained  by  shooting 
which  was  unselective  with  respect  to  age,  the 
sample  gives  the  age  striicture  of  the  living  popu- 
lation at  that  time ;  that  the  animals  were  killed  to 
get  these  data  is  irrelevant.  Hence  unbiased 
shooting  samples  survivorship,  not  mortality,  and 
an  age  structure  so  obtained  can  be  treated  as  a 
klx  series  if  all  other  necessary  assumptions  obtain. 
Similarly,  groups  of  animals  killed  by  avalanches, 
fires,  or  floods — catastrophic  events  that  preserve 
a  sample  of  the  age  frequencies  of  animals  during 
life — do  not  provide  information  amenable  to  kdx 
treatment. 

A  sample  may  include  both  Ix  and  dx  compo- 
nents. For  instance,  it  could  consist  of  a  number 
of  dead  animals,  some  of  which  have  been  unselec- 
tively  shot,  whereas  the  deaths  of  others  are  at- 
tributable to  "natural"  mortality.  Or  it  could  be 
formed  by  a  herd  of  animals  killed  by  an  avalanche 
in  an  area  where  carcasses  of  animals  that  died 
"naturally"  were  also  present.  In  both  these  cases 
dx  and  /x  data  are  confounded  and  these  hetero- 
geneous samples  of  ages  at  death  can  be  treated 
neither  as  kdx  nor  klx  series. 

Even  if  a  sample  of  ages  at  death  wc/e  not 
heterogeneous  in  this  sense,  it  might  still  give  mis- 
leading information.  If,  for  instance,  carcasses 
attributable  to  "natural"  mortality  were  collected 
only  on  the  winter  range  of  a  population,  the  age 
frequencies  of  this  sample  would  provide  ages  at 
death  which  reflected  the  mortality  pattern  during 
only  part  of  the  year.  But  the  dx  series  gives  the 
proportion  of  deaths  over  contiguous  periods  of 


305 


Autumn  1966 


MORTALITY   PATTERNS  IN    MAMMALS 


909 


the  life  span  and  must  reflect  all  mortality  during 
each  of  these  periods. 

It  has  been  stressed  that  the  frequencies  of  ages 
in  life  or  of  ages  at  death  provide  Ufe-table  in- 
formation only  when  they  are  drawn  from  a  popu- 
lation with  a  stationary  age  distribution.  This  age 
distribution  should  not  be  confused  with  the  stable 
distribution.  When  a  population  increases  at  a 
constant  rate  and  where  survivorship  and  fecun- 
dity rates  are  constant,  the  age  distribution  even- 
tually assumes  a  stable  form  (Lotka  1907  a,  b; 
Sharpe  and  Lotka  1911 ).  Slobodkin  (1962,  p.  49) 
gives  a  simple  explanation  as  to  why  this  is  so.  A 
stable  age  distribution  does  not  form  a  kl^,  series 
except  when  the  rate  of  increase  is  zero,  the  season 
of  births  is  restricted,  and  the  sample  is  taken  at 
this  time.  Hence  the  stationary  age  distribution 
is  a  special  case  of  the  stable  age  distribution. 

The  Relative  Usefulness  of  the 
/x,  dx  and  gx  series 

Most  published  life  tables  for  wild  mammals 
have  been  constructed  either  from  age  frequencies 
obtained  by  shooting  to  give  a  ^/x  series,  or  by  de- 
termining the  ages  at  death  of  animals  found  dead, 
thereby  producing  a  kd^  series.  Unfortunately, 
both  these  methods  are  almost  invariably  subject 
to  bias  in  that  the  frequency  of  the  first-year  class 
is  not  representative.  Dead  immature  animals, 
especially  those  dying  soon  after  birth,  tend  to 
decay  faster  than  the  adults,  so  that  they  are  under- 
represented  in  the  count  of  carcasses.  The  ratio 
of  juveniles  to  adults  in  a  shot  sample  is  usually 
biased  because  the  two  age  classes  have  different 
susceptibilities  to  hunting.  With  such  a  bias  estab- 
lished or  suspected,  the  life  table  is  best  presented 
in  a  form  that  minimizes  this  bias.  An  error  in 
the  frequency  of  the  first  age  class  results  in  dis- 
tortions of  each  Ix  and  dx  value  below  it  in  the 
series,  but  q^  values  are  independent  of  frequencies 
in  younger  age  classes.  By  definition,  q  is  the  ratio 
of  those  dying  during  an  age  interval  to  those 
alive  at  the  beginning  of  the  interval.  At  age  y  the 
value  of  q  is  given  by 

Qy  =  dy/ly 


but 


dy    ty  I- 


y  +  1 


therefore 

Qy  ^  (^y  —  ^y  +  i)/^y   • 

Thus  the  value  of  ^y  is  not  directly  dependent  on 
absolute  values  of  /^  but  on  the  differences  between 
successive  values.  If  the  Ix  series  is  calculated 
from  age  frequencies  in  which  the  initial  frequency 


is  inaccurate,  each  Ix  value  will  be  distorted.  How- 
ever, the  difference  between  any  two,  divided  by 
the  first,  will  remain  constant  irrespective  of  the 
magnitude  of  error  above  them  in  the  series.  Thus 
a  qx  value  is  independent  of  all  but  two  survivor- 
ship age  frequencies  and  can  be  calculated  directly 
from  these  frequencies  (fx)  by 

qx  =  {fx  —  fx  +  i)/ix 

if  the  previously  discussed  conditions  are  met. 

The  calculation  of  q  from  frequencies  of  ages 
at  death  is  slightly  more  complex  : 

by  definition  qy  =  dy/U- 


but 


therefore 


00         y-i 
ly  =  2dx  —  SOx 

x=o        x=o 

00        y-1 
qy  =  dy/{i:dx  —  Zdx) 

x=o        x=o 


=  dy/Xdx: 

x=y 

but  the  frequencies  of  ages  at  death  (fx)  are  them- 

00 

selves  a  kdx  series  and  so  Q'y=/'y/2/  x  ■ 

x  =  y 

Thus  the  value  of  q  at  any  age  is  independent  of 
frequencies  of  the  younger  age  classes.  Although 
the  calculated  value  of  q  for  the  first  age  class  may 
be  wrong,  this  error  does  not  affect  the  qx  values 
for  the  older  age  classes. 

The  qx  series  has  other  advantages  over  the  Ix 
and  dx  series  for  presenting  the  pattern  of  mor- 
tality with  age.  It  shows  rates  of  mortality  di- 
rectly, whereas  this  rate  is  illustrated  in  a  graph 
of  the  Ix  series  (the  series  most  often  used  when 
comparing  species)  only  by  the  slope  of  the  curve. 

A  Life  Table  for  the  Thar, 

Hemitragus  jemlahicus 
The  Himalayan  thar  is  a  hollow-horned  ungu- 
late introduced  into  New  Zealand  in  1904  (Donne 
1924)  and  which  now  occupies  2,000  miles^  of 
mountainous  country  in  the  South  Island.  Thar 
were  liberated  at  Mount  Cook  and  have  since 
spread  mostly  north  and  south  along  the  Southern 
Alps.  They  are  still  spreading  at  a  rate  of  about 
1.1  miles  a  year  (Caughley  1%3)  and  so  the  popu- 
lations farthest  from  the  point  of  liberation  have 
been  established  only  recently  and  have  not  yet 
had  time  to  increase  greatly  in  numbers.  Closer 
to  the  site  of  liberation  the  density  is  higher  (cor- 
related with  the  greater  length  of  time  that  animals 
have  been  established  ther^),  and  around  the  point 
of  liberation  itself  there  is  evidence  that  the  popu- 
lation has  decreased  (Anderson  and  Henderson 
1961). 


306 


910 


GRAEME  CAUGHLEY 


Ecology,  Vol.  47,  No.  6 


The  growth  rings  on  its  horns  are  laid  down 
in  each  winter  of  life  other  than  the  first  (Caugh- 
ley  1965),  thereby  allowing  the  accurate  ageing  of 
specimens.  An  age  structure  was  calculated  from 
a  sample  of  623  females  older  than  1  yr  shot  in 
the  Godley  and  Macaulay  Valleys  between  Novem- 
ber 1963  and  February  1964.  Preliminary  work 
on  behavior  indicates  that  there  is  very  little  dis- 
persal of  females  into  or  out  of  this  region,  both 
because  the  females  have  distinct  home  ranges  and 
because  there  are  few  ice-free  passes  linking  the 
valley  heads. 

As  these  data  illustrate  problems  presented  by 
most  mammals,  and  because  the  life  table  has  not 
been  published  previously,  the  methods  of  treat- 
ment will  be  outlined  in  some  detail. 

Is  the  population  stationary  f 

Although  it  is  impossible  to  determine  the  sta- 
tionary nature  of  a  population  by  examining  the 
age  structure  of  a  single  sample,  even  when  rates 
of  fecundity  are  known,  in  some  circumstances  a 
series  of  age  structures  will  give  the  required  in- 
formation. This  fact  is  here  utilized  to  investigate 
the  stability  of  this  population. 

The  sample  was  taken  about  halfway  between 
the  point  of  liberation  and  the  edge  of  the  range. 
It  is  this  region  between  increasing  and  decreasing 
populations  where  one  would  expect  to  find  a 
stationary'  population.  The  animals  came  into  the 
Godley  Valley  from  the  southwest  and  presumably 
colonized  this  side  of  the  valley  before  crossing  the 
2  miles  of  river  bed  to  the  northeast  side.  This 
pattern  of  establishment  is  deduced  from  that  in 
the  Rakaia  Valley,  at  the  present  edge  of  the 
breeding  range,  where  thar  bred  for  at  least  5  yr 
on  the  south  side  of  the  valley  before  colonizing 
the  north  side.  Having  colonized  the  northeast 
side  of  the  Godley  Valley,  the  thar  would  then 
cross  the  Sibald  Range  to  enter  the  Macaulay 
Valley,  which  is  a  further  6  miles  northeast.  The 
sample  can  therefore  be  divided  into  three  sub- 
samples  corresponding  to  the  different  periods  of 
time  that  the  animals  have  been  present  in  the 
three  areas.  A  10  X  3  contingency  test  for  differ- 
ences between  the  three  age  distributions  of  fe- 
males 1  yr  of  age  or  older  gave  no  indication  'that 
the  three  subpopulations  differed  in  age  structure 
(X=^  =  22.34;  P  =  0.2). 

This  information  can  be  interpreted  in  two 
ways :  either  the  three  subpopulations  are  neither 
increasing  nor  decreasing  and  hence  are  likely  to 
have  stationary  age  distributions,  or  the  subpopu- 
lations could  be  increasing  at  the  same  rate,  in 
which  case  they  could  have  identical  stable  age 
distributions.      The    second   alternative   carries   a 


Table  I.     Relative  densities  of  thar 

in  three 

zones 

Zone 

Number 

females 

autopsied 

Mean 
density 
inde.x" 

Standard 
error 

Godley  Valley  south 

Godley  Valley  north 

Macaulay  Valley. 

258 
240 
115 

2.19 
1.67 
2.66 

0.56 
0.53 
0  69 

F2.56  for  densities  between  valleys  ==  1.74,  not  significant 

'Density  indices  were  calculated  as  the  number  of  females  other  than  kids 

recorded  a,s  autopsied  in  a  zone  each  day.  divided  by  the  number  of  shooters 

hunting  in  the  zone  on  that  day. 

corollary  that  the  subpopulations  would  have  dif- 
ferent densities  because  they  have  been  increasing 
for  differing  periods  of  time.  But  an  analysis  of 
the  three  densities  gives  no  indication  that  they 
differ  (Table  I).  This  result  necessitates  the 
rejection  of  the  second  alternative. 

The  above  evidence  suggesting  that  the  sample 
was  drawn  from  a  stationary  age  distribution  is 
supported  to  some  extent  by  observation.  When 
I  first  passed  through  the  area  in  1957,  I  saw 
about  as  many  thar  per  day  as  in  1963-64.  J.  A. 
Anderson,  a  man  who  has  taken  an  interest  in  the 
thar  of  this  region,  writes  that  the  numbers  of 
thar  in  1956  were  about  the  same  as  in  1%4 
(Anderson,  pers.  comm.).  These  are  subjective 
evaluations  and  for  that  reason  cannot  by  them- 
selves be  given  much  weight,  but  they  support  in- 
dependent evidence  that  the  population  is  station- 
ary or  nearly  so. 

Is  the  sample  biased? 

A  sample  of  the  age  structure  of  a  population 
can  be  biased  in  several  ways.  The  most  obvious 
source  of  bias  is  behavioral  or  range  differences 
between  males  and  females.  For  instance,  should 
males  tend  to  occupy  terrain  which  is  more  diffi- 
cult to  hunt  over  than  that  used  by  females,  they 
would  be  underrepresented  in  a  sample  obtained 
by  hunting.  During  the  summer  thar  range  in 
three  main  kinds  of  groups :  one  consists  of  fe- 
males, juveniles  and  kids,  a  second  consists  of 
young  males  and  the  third  of  mature  males.  The 
task  of  sampling  these  three  groupings  in  the  same 
proportions  as  they  occur  throughout  the  area  is 
complicated  by  their  preferences  for  terrain  that 
differs  in  slope,  altitude  and  exposure.  Conse- 
quently the  attempt  to  take  an  unbiased  sample 
of  both  males  and  females  was  abandoned  and  the 
hunting  was  directed  towards  sampling  only  the 
nanny-kid  herds  in  an  attempt  to  take  a  repre- 
sentative sample  of  females.  The  following  analy- 
sis is  restricted  to  females. 

Although  bias  attributable  to  differences  in  be- 
havior between  sexes  can  be  eliminated  by  the 
simple  contrivance  of  ignoring  one  sex,  some  age 


307 


Autumn  1966 


MORTALITY   PATTERNS   IN    MAMMALS 


911 


classes  of  females  may  be  more  susceptible  than  no  bias  could  be  detected  from  a  sample  of  this 
others  to  shooting.  To  test  for  such  a  difference,  size, 
females  other  than  kids  were  divided  into  two 
groups :  those  from  herds  in  which  some  mem- 
bers were  aware  of  the  presence  of  the  shooter 
before  he  fired,  and  those  from  herds  which  were 
undisturbed  before  shooting  commenced.  If  any 
age  group  is  particularly  wary  its  members  should 
occur  more  often  in  the  "disturbed"  category  than 
is  the  case  for  other  age  groups.  But  a  x"  test 
(X^  =  7.28,  df  =  9,  P  =  0.6)  revealed  no  signifi- 
cant difference  between  the  age  structures  of  the 
two  categories. 

The  sample  was  next  divided  into  those  females 
shot  at  ranges  less  than  200  yards  and  those  shot 
out  of  this  range.  If  animals  in  a  given  age  class 
are  more  easily  stalked  than  the  others,  they  will 
tend  to  be  shot  at  closer  ranges.  Alternatively, 
animals  which  present  small  targets  may  be  under- 
represented  in  the  sample  of  those  shot  at  ranges 
over  200  yards.  This  is  certainly  true  of  kids, 
which  are  difficult  to  see,  let  alone  to  shoot,  at 
ranges  in  excess  of  200  yards.  The  kids  have 
therefore  not  been  included  in  the  analysis  be- 
cause their  underrepresentation  in  the  sample  is 
an  acknowledged  fact,  but  for  older  females  there 
is  no  difference  between  the  age  structures  of  the 
two  groups  divided  by  range  which  is  not  ex- 
plainable as  sampling  variation  (x"  =  9.68,  df  :=  9. 
P^O.4).  This  is  not  to  imply  that  no  bias 
exists — the  yearling  class  for  instance  could  well 
be  underrepresented  beyond  200  yards — but  that 


The  taking  of  a  completely  representative  sam- 
ple from  a  natural  population  of  mammals  is  prob- 
ably a  practical  impossibility,  and  I  make  no  claim 
that  this  sample  of  thar  is  free  of  bias,  but  as  bias 
cannot  be  detected  from  the  data,  I  assume  it  is 
slight. 

Construction  of  the  life  table 

The  shooting  yielded  623  females  1  yr  old  or 
older,  aged  by  growth  rings  on  the  horns.  As 
the  sampling  period  spanned  the  season  of  births, 
a  frequency  for  age  0  cannot  be  calculated  directly 
from  the  number  of  kids  shot  because  early  in  the 
period  the  majority  had  not  been  born.  In  any 
case,  the  percentage  of  kids  in  the  sample  is  biased. 

The  numbers  of  females  at  each  age  are  shown 
in  Table  II,  column  2.  Although  the  ages  are 
given  only  to  integral  years  each  class  contains 
animals  between  ages  x  yr  —  "/^  month  and  x  yr 
4"  2j^  months.  Variance  owing  to  the  spread  of 
the  kidding  season  is  not  included  in  this  range, 
but  the  season  has  a  standard  deviation  of  only  15 
days  (Caughley  1965). 

Up  to  an  age  of  12  yr  (beyond  this  age  the 
values  dropped  below  5  and  were  not  treated) 
the  frequencies  were  smoothed  according  to  the 
formula 

log  y  =  1.9673  -f  0.0246x  —  0.01036  x^, 

where  y  is  the  frequency  and  x  the  age.     The 
linear  and  quadratic  terms   significantly  reduced 


Table  II.     Life  table  and  fecundity  table  for  the  thar  Hemitragus  jemlahicus  (females  only) 


1 

Age  in  years 

X 

2 

Frequency 
in  sample 

3 

Adjusted 
frequency 

4 

No.  female 

live  births 

per  female 

at  age  x 

nil 

5 
1,000?. 

6 
1,000  d. 

7 
l,000gi 

0 

1 

94 
97 
107 
68 
70 
47 
37 
35 
24 
16 

11 
6 

3 
4 
3 
0 

1 

205" 
95.83 
94.43 
88.69 
79.41 
67.81 
55.20 
42.85 
31.71 
22.37 
15,04 

9.64 
5.90 

0.000 
0.005 
0.135 
0.440 
0.420 
0.465 
0.425 
0.460 
0.485 
0.500 
0.500 

1 

^0.470 

J 

0.350 

1,000 
467 
461 
433 
387 
331 
269 
209 
155 
109 
73 

47 
29 

533 
6 
28 
46 
56 
62 
60 
54 
46 
36 
26 

18 

533 
13 

2 

61 

3 

106 

4 

145 

5 

187 

6 

223 

7 

258 

8 

297 

9 

330 

10 

356 

11 

382 

12 

13 

14 

15 

16 

17 

■Calculated  from  adjusted  frequencies  of  females  other  than  kids  (column  3)  and  mx  values  (column  4). 


308 


Q12 


GRAEME  CAUGHLEY 


Ecology,  Vol.  47,  No.  6 


AGE    IN  YEARS 


Fig.  1.  Age  frequencies,  plotted  on  a  logarithmic  scale, 
of  a  sample  of  female  thar,  with  a  curve  fitted  to  the  values 
from  ages  1  to  12  yr,  and  the  mortality  rate  per  1,000  for 
each  age  interval  of  1  yr  (IfiOOq^^)  plotted  against  the 
start  of  the  interval. 

variance  around  the  regression,  but  reduction  by 
the  addition  of  a  cubic  term  was  not  significant 
at  the  0.05  level.  There  are  biological  reasons 
for  suspecting  that  the  cubic  term  would  have 
given  a  significant  reduction  of  variance  had  the 
sample  been  larger,  but  for  the  purposes  of  this 
study  its  inclusion  in  the  equation  would  add  very 
little.  The  improved  fit  brought  about  by  the 
quadratic  term  indicates  that  the  rate  of  mortality 
increases  with  age.  Whether  the  rate  of  this  rate 
also  increases,  is  left  open.  The  computed  curve 
closely  fitted  the  observed  data  ( Fig.  1 )  and  should 
greatly  reduce  the  noise  resulting  from  sampling 
variation,  the  differential  effect  on  mortality  of 
different  seasons,  and  the  minor  heterogeneities 
which,  although  not  detectable,  are  almost  certain 
to  be  present.  The  equation  is  used  to  give  ad- 
justed frequencies  in  Table  II,  column  3. 

The  frequency  of  births  can  now  be  estimated 
from  the  observed  mean  number  of  female  kids 
produced  per  female  at  each  age.  These  are  shown 
in  column  4.  They  were  calculated  as  the  number 
of  females  at  each  age  either  carrying  a  foetus"  or 
lactating,  divided  by  the  number  of  females  of  that 
age  which  were  shot.  These  values  were  then 
halved  because  the  sex  ratio  of  late  foetuses  and 
kids  did  not  differ  significantly  from  1:1  (93  S  S  : 
97  9  9  ) .  The  method  is  open  to  a  number  of 
objections :  it  assumes  that  all  kids  were  born 
alive,  that  all  females  neither  pregnant  nor  lac- 
tating were  barren  for  that  season,  and  that  twin- 
ning did  not  occur.  The  first  assumption,  if  false, 
would  give  rise  to  a  positive  bias,  and  the  second 


and  third  to  a  negative  bias.  However,  the  ratio 
of  females  older  than  2  yr  that  were  either  preg- 
nant or  lactating  to  those  neither  pregnant  nor 
lactating  did  not  differ  significantly  between  the 
periods  November  to  December  and  January  to 
February  (x' =  0.79,  P  =  OA),  suggesting  that 
still  births  and  mortality  immediately  after  birth 
were  not  common  enough  to  bias  the  calculation 
seriously.  Errors  are  unlikely  to  be  introduced 
by  temporarily  barren  females  suckling  yearlings, 
because  no  female  shot  in  November  that  was 
either  barren  (as  judged  by  the  state  of  the  uterus) 
or  pregnant  was  lactating.  Errors  resulting  from 
the  production  of  twins  will  be  very  small ;  we 
found  no  evidence  of  twinning  in  this  area. 

The  products  of  each  pair  of  values  in  columns 
3  and  4  (Table  II)  were  summed  to  give  an  esti- 
mate of  the  potential  number  of  female  kids  pro- 
duced by  the  females  in  the  sample.  This  value 
of  205  is  entered  at  the  head  of  column  3.  The 
adjusted  age  frequencies  in  column  3  were  each 
multiplied  by  4.878  to  give  the  1,000/x  survivor- 
ship values  in  column  5.  The  mortality  series 
(column  6)  and  mortality-rate  series  (column  7) 
were  calculated  from  these. 

Conclusions 

Figure  1  shows  the  mortality  rate  of  females  in 
this  thar  population  up  to  an  age  of  12  yr.  Had 
the  sample  been  larger  the  graph  could  have  been 
extended  to  an  age  of  17  yr  or  more,  but  this 
would  have  little  practical  value  for  the  calcula- 
tion of  population  statistics  because  less  than  3% 
of  females  in  the  population  were  older  than  12  yr. 

The  pattern  of  mortality  with  age  can  be  di- 
vided into  two  parts — a  juvenile  phase  charac- 
terized by  a  high  rate  of  mortality,  followed  by  a 
postjuvenile  phase  in  which  the  rate  of  mortality 
is  initially  low  but  rises  at  an  approximately  con- 
stant rate  with  age. 

Table  II  gives  both  the  k  and  m^  series,  and 
these  two  sets  of  values  provide  most  of  the  in- 
formation needed  to  describe  the  dynamics  of  the 
population.  Assuming  that  these  two  series  are 
accurate,  the  following  statistics  can  be  derived : 
generation  length  (i.e.  mean  lapse  of  time  between 
a  female's  date  of  birth  and  the  mean  date  of  birth 
of  her  offspring),  T: 

^'^'"^^-^5.4yr; 


r  = 


S/xWs 


mean  rate  of  mortality  for  all  age  groups,  g^: 

'q^  —  l/S/x  =  0.25  per  female  per  annum; 

life  expectancy  at  birth,  eo : 

^0  =  2  /x  —  >^  =  3.5  yr. 


309 


Autumn  1966 


MORTALITY  PATTERNS  IN   MAMMALS 


913 


The  last  two  statistics  can  also  be  expressed 
conveniently  in  terms  of  the  mortality  series  by 

^,=  l/S(x+l)(f. 


and 


eo 


S  (2x+l)  d. 


The  relationship  of  the  two  is  given  by 

^,  =  2/(2^0+1). 

Life  Tables  for  Other  Mammals 

The  difficulty  of  comparing  the  mortality  pat- 
terns of  animals  that  differ  greatly  in  life  span  can 
be  readily  appreciated.  To  solve  this  problem, 
Deevey  (1947)  proposed  the  percentage  deviation 
from  mean  length  of  life  as  an  appropriate  scale, 
thereby  allowing  direct  comparison  of  the  life  tables 
of,  say,  a  mammal  and  an  invertebrate.  For  such 
comparisons  this  scale  is  obviously  useful,  but  for 
mammals  where  the  greatest  difference  in  mor- 
tality rates  may  be  at  the  juvenile  stage  the  scale 
often  obscures  similarities. 

By  way  of  illustration,  Figure  2  shows  l.OOOgx 
curves  for  two  model  populations  which  differ 
only  in  the  mortality  rate  of  the  first  age  class. 
When  the  values  are  graphed  on  a  scale  of  per- 
centage deviation  from  mean  length  of  life  the 
close  similarity  of  the  two  sets  of  data  is  no  longer 
apparent.      Thus   the    use   of   Deevey's   scale   for 

•/.  DEVIATION  FROM  MEAN  LENGTH  OF  LIFE 


eoo  - 


X 
O 


100 

-50                     0 

.50 

•100 

♦15 

T      ■                     1 

» 

1 
1 

^ 

P 

- 

/ 
/ 

1 

1 

/                 / 
1                 / 

- 

} 

/ 

p 

- 

\ 

\'.                 *'      P 

p 

- 

s. 

1               1               1 

1 

f 

1 

AGE    IN    ^'-A^'; 

Fig.  2.  The  mortality  rate  per  1,000  for  each  year  of 
life  for  two  model  populations  that  differ  only  in  the  de- 
gree of  first-year  mortality.  These  l.OOOq^  values  are 
each  graphed  on  two  time  scales :  absolute  age  in  years 
(continuous  lines)  and  percentage  deviation  from  mean 
life  expectancy   (broken  lines). 


comparing  mortality  patterns  in  mammals  might 
result  in  a  loss  rather  than  a  gain  of  information. 
In  this  paper,  absolute  age  has  been  retained  as 
a  scale  in  comparing  life  tables  of  different  species, 
although  this  scale  has  its  own  limitations. 

Domestic  sheep,  Ovis  aries. — Between  1954  and 
1959,  Hickey  (19(30)  recorded  the  ages  at  death 
of  83,113  females  on  selected  farms  in  the  North 
Island  of  New  Zealand.  He  constructed  a  ^x 
table  from  age  IJ^  yr  by  "dividing  the  number  of 
deaths  which  have  occurred  in  each  year  of  age 
by  the  number  'exposed  to  risk'  [of  death]  at  the 
same  age."  An  age  interval  of  1  yr  was  chosen 
and  the  age  series  V/z,  2]^,  3>4  etc.  was  used  in 
preference  to  integral  ages. 

The  qx  series  conformed  very  closely  to  the 
regression  :  log  g^  ^  0.1 56x  -f  0.24,  enabling  him 
in  a  subsequent  paper  (Hickey  1963)  to  present 
the  interpolated  q^  values  at  integral  ages.  He 
also  calculated  q  for  the  first  year  of  life  from  a 
knowledge  of  the  number  of  lambs  dying  before  1 
yr  of  age  out  of  85,309  (sexes  pooled)  born  alive. 

These  data  probably  provide  the  most  accurate 
life  table  for  any  mammal.  The  1,000^^  curve 
is  graphed  in  Figure  3. 


800 

- 

I 

1 

T    ■ 

I 

■   y  ■  ■ 

? 

600 

- 

/ 

■ 

400 

- 

^ 

■ 

200 

\ 

1 

- 

0 

0 

2 

4 

6 

8 

10 

12 

AGE  IN  YEARS 

Fig.  3.  Domestic  sheep :  mortaHty  rate  per  1,000  for 
each  age  interval  of  1  yr  (l,000qj,  plotted  against  the 
start  of  the  interval.     Data  from  Hickey   (1963). 

Dall  sheep,  Ovis  dalli. — During  his  study  on  the 
wolves  of  Mount  McKinley  National  Park,  Murie 
(1944)  aged  carcasses  of  dall  sheep  he  found 
dead,  their  ages  at  death  being  established  from 
the  growth  rings  on  the  horns.  This  sample  can 
be  divided  into  those  that  died  before  1937  and 
those  that  died  between  1937  and  1941.  The 
former  sample  was  used  by  Deevey  (1947)  to 
construct  the  life  table  presented  in  his  classic 
paper  on  mortality  in  natural  populations.  Kur- 
ten  (1953)  constructed  a  life  table  from  the  same 


310 


914 


GRAEME  CAUGHLEY 


Ecology,  Vol.  47,  Mo.  6 


data,  but  corrected  the  iinderrepresentation  of 
first-year  animals  resulting  from  the  relatively 
greater  perishability  of  their  skulls  by  assuming 
that  adult  females  produce  1  lamb  per  annum  from 
about  their  second  birthday.  Taber  and  Dasmann 
(1957)  constructed  life  tables  for  both  males  and 
females  from  the  sample  of  animals  dying  between 
1937  and  1941,  and  adjusted  both  the  0  to  1-  and 
1  to  2-year  age  frequencies  on  the  assumption  that 
a  female  produces  her  first  lamb  at  about  her  third 
birthday  and  another  lamb  each  year  thereafter, 
that  the  sex  ratio  at  birth  is  unity  and  that  the 
loss  of  yearlings  is  not  more  than  10%. 


1000 

1  ■              ■      I                       I                       I 

1 

■ 

aoo 

-■ 

/ 

/ 

eoo 

- 

// 

/. 

400 

A                            ??  - 

/    / 

- 

200 

^="=5=^=0- — "^       ,               1 

i<S 

- 

AGE  IN  YEARS 

Fig.  4.  Dall  sheep :  mortality  rate  per  1,000  for  each 
age  interval  of  1  yr  (1,000(7,^),  plotted  against  the  start 
of  the  interval.    Data  from  Murie  (1944). 

Figure  4  shows  a  version  of  this  table  con- 
structed from  the  pre- 1937  sample.  The  mortality 
of  the  first  year  class  has  been  adjusted  by  assum- 
ing that  the  sex  ratio  at  birth  is  unity,  that  50% 
of  females  produce  their  first  kids  at  their  second 
birthday  and  that  thereafter  90%  produce  kids 
each  year.  The  figure  of  50%  fecundity  at  age 
2  is  borrowed  from  \\'oodgerd's  (1964)  study  on 
the  closely  related  Ov'xs  canadensis,  and  the  sub- 
sequent 90%  fecundity  is  based  on  Murie's  (1944) 
statement  that  twins  are  extremely  rare.  To 
allow  for  temporarily  or  permanently  barren  ani- 
mals, 10%  is  subtracted  from  the  potential  fecun- 
dity. 

This  life  table  must  be  taken  as  an  approxima- 
tion. As  Deevey  (1947)  has  pointed  out,  the 
pre-1937  and  1937^1  samples  dififer  significantly 
in  age  structure.  The  obvious  conclusion  is  that 
the  mortality  rate  by  age  was  changing  before  and 
during  the  period  of  study.  Consequently  the  age 
structure  of  the  sample  is  likely  to  be  only  an 
approximation   of  the   kdj,   series.      Furthermore, 


the  qx  values  for  age  1  yr  are  likely  to  have  been 
biased  by  differential  perishability  of  skulls,  but 
no  arbitrary  adjustment  has  been  made. 

Man. — Most  of  the  life  tables  available  for  man 
show  that  males  have  a  higher  rate  of  mortality 
than  females.  However,  Macdonell's  (1913) 
tables  for  ancient  Rome,  Hispania  and  Lusitania 
suggest  that  this  might  not  always  have  been  so 
and  that  in  some  circumstance  the  reverse  can  be 
true. 

A  l,OOO^x  curve  for  Caucasian  males  and  fe- 
males in  the  United  States  between  1939  and 
1941  is  shown  in  Figure  5.  The  values  are  taken 
from  Dublin,  Lotka,  and  Spiegelman  (1949). 

Rat,  Rattus  norvegicus. — Wiesner  and  Sheard 
(1935)  gave  the  ages  at  death  of  1,456  females  of 
the  albino  rat  (Wistar  strain)  in  a  laboratory 
population.  Their  table  begins  at  an  age  of  31 
days,  but  Leslie  et  al.  (1952)  calculate  from  Wies- 
ner and  Sheard's  data  that  the  probability  of 
dying  between  birth  and  31  days  was  0.316.  Fig- 
ure 6  gives  a  ^x  curve  constructed  from  these  data. 

Short-tailed  vole,  Microtus  agrestis. — The  ages 
at  death  of  85  males  and  34  females  were  reported 
by  Leslie  and  Ranson  (1940)  from  a  laboratory 
population  of  voles  kept -at  the  Bureau  of  Animal 
Population,  Oxford.  Frequencies  for  both  sexes 
were  pooled  and  the  data  were  smoothed  by  the 
formula  fx  =  fo  e"'"'"  where  /  is  the  frequency  of 
animals  alive  age  x,  and  ^  is  a  constant.  The  com- 
puted curve  closely  fitted  the  data  (P  =  0.5  to 
0.7).  Figure  6  shows  the  1,000^^  curve  derived 
from  the  authors'  sixth  table. 


250 


200 


150  - 


o 
o 
o 


100  - 


AGE  IN  YEARS 

Fig.   5.     Man   in    U.S. :    mortality    rate    per    1,000   per 
year  of  age   (1,000^^).     Data  from  Dublin  et  al.   (1949). 


311 


Autumn  1966 


MORTALITY   PATTERNS   IN    MAMMALS 


915 


VOLE  0 


RAT 


16 


20 


AGE  UNITS 

Fig.  6.  Short-tailed  voles  and  rats :  mortality  rate  per 
1,000  for  each  age  interval  (1,000(7^),  plotted  against  the 
start  of  the  interval.  Age  interval  is  56  days  for  voles 
and  50  days  for  rats.  Rat  data  from  Wiesner  and  Sheard 
(1935)  ;  vole  data  from  Leslie  and  Ranson  (1940). 

The  pooling  of  mortality  data  from  both  sexes 
is  strictly  valid  only  when  the  two  qx  series  are 
not  significantly  different.  Studies  on  differential 
mortality  between  sexes  are  few,  but  those  avail- 
able for  man  (Dublin  et  al.  1949,  and  other  au- 
thors), dall  sheep  (Taber  and  Dasmann  1957,  and 
this  paper),  the  pocket  gopher  (Howard  and 
Childs  1959)  and  Orkney  vole  (Leslie  et  al.  1955) 
suggest  that  although  mortality  rates  certainly 
■differ  between  sexes,  the  trends  of  these  age- 
specific  rates  tend  to  be  parallel.  Consequently, 
this  life  table  for  voles,  although  based  on  pre- 
sumably heterogeneous  data,  is  probably  quite 
adequate  for  revealing  the  gross  pattern  of  mor- 
tality with  age. 

Orkney  vole,  Microtus  orcadensis. — Leslie  et  al. 
(1955)  gave  a  life  table  for  both  males  and  females 
in  captivity  from  a  base  age  of  9  weeks.  In  addi- 
tion they  gave  the  probability  at  birth  of  surviving 
to  ages  3,  6,  and  9  weeks,  but  did  not  differentiate 
sexes  over  this  period.  The  (/x  curve  given  here 
(Fig.  7)  was  constructed  by  calculating  survivor- 
ship series  for  both  males  and  females  from  these 
data,  drawing  trend  lines  through  the  points,  and 
interpolating  values  at  intervals  of  8  weeks. 

Proposed  life  tables  not  accepted 
In  the  Discussion  section  of  this  paper  the  life 
tables  discussed  previously  are  examined  in  an 


ACE  UNITS 

Fig.  7.  Orkney  vole:  mortality  rate  per  1,000  for  each 
age  interval  of  56  days  (l,000g^),  plotted  against  the 
start  of  the  interval.     Data  from  Leslie  et  al.   (1955). 

attempt  to  generalize  their  form.  Only  a  small 
proportion  of  published  life  tables  are  dealt  with, 
and  any  generalization  from  these  could  be  inter- 
preted as  an  artefact  resulting  from  selection  of 
evidence. 

To  provide  the  reader  with  the  information 
necessary  for  reaching  an  independent  conclusion, 
the  published  life  tables  not  selected  for  compari- 
son are  listed  below  with  the  reason  for  their 
rejection.  Only  those  including  all  juvenile  age 
classes  are  cited.  These  tables  are  rejected  only 
for  present  purposes  because  comparison  of  mor- 
tality patterns  between  species  demands  a  fairly 
high  level  of  accuracy  for  individual  tables.  The 
inclusion  of  a  table  in  this  section  does  not  neces- 
sarily imply  that  it  is  completely  inaccurate  and  of 
no  practical  value. 

Tables   based   on   inadequate   data    (i.e.   less 

than  50  ages  at  death  or  150  ages  of  living 

animals)  :   Odocoileus  hemionus   (Taber  and 

Dasmann    1957),    OzHs    canadensis    (Wood- 

gerd  1964)  ; 

Probable   sampling   bias :    Lepus   americanus 

(Green  and  Evans   1940),  Rupicapra  rupi- 

capra    (Kurten    1953),    fossil    accumulations 

(Kurten    1953,    1958;    Van    Valen    1964), 

Balaenoptera  physalus  (Laws  1962)  ; 

Age  structure  analyzed  as  a  kdx  series :  Syl- 

vilagus  floridanus   (Lord   1961),   Odocoileus 

virginianus  and  Capreolus  capreolus  (Quick 

1963); 

Death  and  emigration  confounded :  Peromys- 

cus  maniculatus   (Howard   1949),  Capreolus 

capreolus  (Taber  and  Dasmann  1957,  Quick 

1963); 


312 


916 


GRAEME  CAUGHLEY 


Ecology,  Vol.  47,  No.  6 


Sample    taken     between    breeding    seasons : 
Odocoileus  znrginianns   (Quick   1963)  ; 
Form  of  life  table,  or  significant  portion  of  it, 
based    largely    on    assumption :    Callorhinus 
iirsinus  (Kenyon  and  Scheffer  1954),  M\otis 
mysta^inus  (Sluiter,  van  Heerdt,  and  Bezem 
1956),  Cennis  elaphus  (Taber  and  Dasmann 
1957),     Rhinolophus     hipposideros,     Myotis 
emarginatus,  and  Myotis  daubentonii  (Bezem, 
Sluiter,  and  van  Heerdt  1960),  Halichoerus 
grypiis  (Hewer  1963,  1964)  ; 
Sample    from    a    nonstationary    population : 
Syhnlagus  floridaniis  (Lord  1961); 
Inadequate  aging:   Gorgon  tanrinns   (Talbot 
and  Talbot  1963)  ; 

Confounding  of  /^  and  d-s,  data :  Rangifer  arc- 
ticus  (Banfield  1955). 

Discussion 

The  most  striking  feature  of  the  g^  curves  of 
species  accepted  for  comparison  is  their  similarity. 
Each  curve  can  be  divided  into  two  components : 
a  juvenile  phase  where  the  rate  of  mortality  is 
initially  high  but  rapidly  decreases,  followed  by 
a  post  juvenile  phase  characterized  by  an  initially 
low  but  steadily  increasing  rate  of  mortality.  The 
seven  species  compared  in  this  paper  all  produced 
9x  curves  of  this  "U"  or  fish-hook  shape,  suggest- 
ing that  most  mammals  share  a  relationship  of  this 
form  between  mortality  rate  and  age.  This  con- 
clusion, if  false,  can  be  invalidated  by  a  few  more 
life  tables  from  other  species.  It  can  be  tested 
most  critically  by  reexamining  some  of  the  species 
for  which  life  tables,  although  published,  were  not 
accepted  in  this  paper.  Those  most  suitable  are 
species  that  can  be  adequately  sampled,  and  accu- 
rately aged  by  growth  rings  on  the  horns  or  growth 
layers  in  the  teeth  (chamois.  Rocky  Mountain 
sheep,  and  several  species  of  deer),  or  those  small 
mammals  that  can  be  marked  at  birth  and  subse- 
quently recaptured. 

High  juvenile  mortality,  characterizing  the  first 
phase  of  the  g.^  curve,  has  been  reported  also  for 
several  mammals  for  which  complete  life  tables 
have  not  yet  been  calculated  (e.g.  for  Oryctolagus 
cuniculus  (Tyndale-Biscoe  and  Williams  1955, 
Stodart  and  Myers  1964),  Gorgon  taurinns  (Tal- 
bot and  Talbot  1963),  Cervus  elaphus  (Riney 
1956)  and  Oreamnos  americanns  (Brandborg 
1955).  Kurten  (1953,  p.  88)  generalized  this 
phenomenon  by  stating  that  "the  initial  dip  [in  the 
survivorship  curve]  is  a  constitutional  character 
in  sexually  reproducing  forms  at  least  .  .  .".  This 
phase  of  mortality  is  highly  variable  in  degree  but 
not  in  form.  Taber  and  Dasmann  (1957)  and 
Bourliere  (1959)  have  emphasized  the  danger  of 


considering  a  life  table  of  a  population  in  given 
circumstances  as  a  typical  of  all  populations  of 
that  species.  Different  conditions  of  life  tend  to 
affect  life  tables,  and  the  greatest  differences  be- 
tween populations  of  a  species  are  likely  to  be 
found  at  the  juvenile  stage.  For  example,  the  rate 
of  juvenile  mortality  in  red  deer  (Riney  1956) 
and  in  man  differ  greatly  between  populations  of 
the  same  species. 

The  second  phase — the  increase  in  the  rate  of 
mortality  throughout  life — is  common  also  to  the 
seven  species  compared  in  this  paper.  However, 
although  the  increase  itself  is  common  to  them, 
the  pattern  of  this  increase  is  not.  Mortality  rates 
have  a  logarithmic  relationship  to  age  in  domestic 
sheep  and  to  a  less  marked  extent  in  the  rat,  the 
Orkney  vole,  and  the  dall  sheep,  whereas  the  re- 
lationship for  the  thar  and  the  short-tailed  vole 
appears  to  be  approximately  arithmetic.  How- 
ever, this  difference  may  prove  to  be  only  an  arte- 
fact resulting  from  the  smoothing  carried  out  on 
the  data  from  these  two  species. 

Despite  these  differences,  the  characteristics 
common  to  the  various  q^  curves  dominate  any 
comparison  made  between  them.  The  similarities 
are  all  the  more  striking  when  measured  against 
the  ecological  and  taxonomic  differences  between 
species.  Taxonomically,  the  seven  species  repre- 
sent three  separate  orders  (Primates,  Rodentia, 
and  Artiodactyla),  and  ecologically  they  comprise 
laboratory  populations  (rats  and  voles),  natural 
populations  (thar,  dall  sheep  and  man)  and  an 
artificial  population  (domestic  sheep).  The  agents 
of  mortality  which  acted  on  these  populations  must 
have  been  quite  diverse.  Murie  (1944)  reported 
that  most  of  the  dall  sheep  in  the  sample  had  been 
killed  by  wolves ;  most  mortality  in  the  thar  popu- 
lation is  considered  to  result  from  starvation  and 
exposure  in  the  winter ;  mortality  of  domestic 
sheep  seems  to  be  largely  a  result  of  disease,  physi- 
ological degeneration,  and  possibly  iodine  defi- 
ciency in  the  lambs  (Hickey  1963)  ;  whereas  the 
deaths  in  the  laboratory  populations  of  voles  and 
rats  may  be  due  to  inadequate  parental  care  and 
cannibalism  of  the  juveniles,  and  perhaps  disease 
and  physiological  degeneration  in  the  adults. 
These  differences  suggest  that  the  ^x  curve  of  a 
population  may  assume  the  same  form  under  the 
influence  of  various  mortality  agents,  even  though 
the  absolute  rate  of  mortality  of  a  given  age  class 
is  not  the  same  in  all  circumstances.  This  hy- 
pothesis is  worth  testing  because  it  implies  that 
the  susceptibility  to  mortality  of  an  age  class,  rela- 
tive to  that  of  other  age  classes,  is  not  strongly 
specific  to  any  particular  agent  of  mortality.  A 
critical  test  would  be  to  compare  the  life  tables  of 


313 


Autumn  1966 


MORTALITY   PATTERNS  IN   MAMMALS 


917 


two  stationary  populations  of  the  same  species, 
wliere  only  one  population  is  subjected  to  preda- 
tion. 

Although  no  attempt  is  made  here  to  explain  the 
observed  mortality  pattern  in  terms  of  evolutionary 
processes,  an  investigation  of  this  sort  could  be 
informative.  A  promising  line  of  attack,  for  in- 
stance, would  be  an  investigation  of  what  appears 
to  be  a  high  inverse  correlation  between  the  mor- 
tality rate  at  a  given  age  and  the  contribution  of 
an  animal  of  this  age  to  the  gene  pool  of  the  next 
generation.  Fisher  (1930)  gives  a  formula  for 
the  latter  statistic. 

Bodenheimer  (1958)  divided  expectation  of  life 
into  "physiological  longevity"  ("that  life  duration 
which  a  healthy  individual  may  expect  to  live 
under  optimum  environment  conditions  until  dying 
of  senescence")  and  "ecological  longevity"  (the 
duration  of  life  under  natural  conditions).  This 
study  suggests  that  such  a  division  is  inexpedient 
because  no  clear  distinction  can  be  made  between 
the  effect  on  mortality  rates  of  physiological  de- 
generation and  of  ecological  influences. 

It  is  customary  to  classify  life  tables  according 
to  the  three  hypothetical  patterns  of  mortality  given 
by  Pearl  and  Miner  (1935).  These  patterns  can 
be  characterized  as :  1  )  a  constant  rate  of  mor- 
tality throughout  life,  2)  low  mortality  through- 
out most  of  the  life  span,  the  rate  rising  abruptly 
at  old  age.  and  3 )  initial  high  mortality  followed 
by  a  low  rate  of  mortality.  Pearl  (1940)  empha- 
sizes that  the  three  patterns  are  conceptual  models 
having  no  necessary  empirical  reality,  but  a  few 
subsequent  writers  have  treated  them  as  laws 
which  all  populations  must  obey.  None  of  these 
models  fit  the  mortality  patterns  of  the  seven  spe- 
cies discussed  in  this  paper  although  Pearl's 
(1940)  later  modification  of  the  system  provides 
two  additional  models  (high-low-high  mortality 
rate  and  low-high-low  mortality  rate),  the  first 
of  which  is  an  adequate  approximation  to  these 
data.  For  mammals  at  least,  the  simple  three- 
fold classification  of  mortality  patterns  is  both  con- 
fusing and  misleading.  The  five-fold  classification 
allows  greater  scope ;  but  do  we  yet  know  enough 
about  mortality  patterns  in  mammals  to  justify 
the  construction  of  any  system  of  classification? 

Acknowledgments 

This  pajier  has  greatly  benefited  from  criticism  of  pre- 
vious drafts  by  M.  A.  Bateman,  CSIRO  ;  P.  H.  Leslie, 
Bureau  of  Animal  Population ;  M.  Marsh,  School  of 
Biological  Sciences,  University  of  Sydney ;  J.  Monro, 
Joint  FAO/IAEA  Div.  of  Atomic  Energy;  G.  R.  Wil- 
liams, Lincoln  College,  and  B.  Stonehouse,  Canterbury 
University,  New  Zealand ;  and  B.  B.  Jones  and  W.  G. 
Warren  of  this  Institute.  The  equation  for  smoothing 
age  frequencies  of  thar  was  kindly  calculated  by  W.  G. 


Warren.  For  assisting  in  the  shooting  and  autopsy  of 
specimens,  I  am  grateful  to  Chris  Challies,  Gary  Chis- 
hojm.  Lin  Hamilton,  Ian  Rogers  and  Bill  Risk. 

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315 


THE  CAUSALITY  OF  MICROTINE  CYCLES  IN   GERMANY 

(Second  Preliminary  Research  Report) 


Fritz  Frank 

Institut    fiir    Griinlandfragen   der   Biologischen    Bundesanstalt   fiir   Land- 

Philosophenweg  16,  Oldenburg   (Oldb),  Germany 


und   Forstwirtschaft, 


Hitherto  the  phenomenon  of  cycles  has  not 
been  a  subject  of  detailed  research  in  central 
Europe,  so  one  could  have  the  impression 
that  cycles  of  extreme  degree  do  not  exist  in 
the  temperate  zones  of  this  continent  ( and 
this  is  often  asserted,  indeed);  but  this  is  not 
the  case.  The  central  European  rodents  not 
only  exhibit  irregular  population  fluctua- 
tions, but  some  of  them  also  show  regular 
cycles  of  an  intensity  and  a  strict  periodicity 
not  inferior  to  those  of  the  cyclic  animals  in 
the  arctic  zone.  Primarily,  there  are  large 
plague  districts  of  Microtus  arvalis  Pallas 
in  Germany  and  her  neighbouring  countries 
which  can  be  followed  back  at  least  to  the 
fifteenth  century.  Recently,  these  plague 
districts  have  increased  because  of  cultiva- 
tion measures,  especially  the  drainage  of 
moist  lowlands  and  fens,  which  create  opti- 
mal biotopes  for  the  voles  (Frank,  1953c, 
1955, 1956b ) .  Besides,  particularly  since  the 
end  of  the  last  war,  Microtus  agrestis  L. 
caused  heavy  damage  in  the  forest  planta- 
tions, as  it  did  in  Great  Britain,  and  it  did 
so  in  a  decidedly  cyclic  manner  (Frank, 
1952 ) .  Systematic  research  on  the  causality 
of  these  cycles  was  started  by  the  author  in 
1951  at  first  with  main  emphasis  on  M.  ar- 
valis.  Besides  detailed  publications,  a  first 
preliminary  report  was  given  in  1954  (Frank, 
1954b ) .  In  the  meantime,  many  new  results 
have  been  collected — in  laboratory  popula- 
tions of  more  than  10,000  animals  and  in 
outdoor-cage  populations,  as  well  as  in  wild 
populations  involving  1,150  individually 
marked  animals.  This  paper  summarizes  the 
present  state  of  the  work,  including  as-yet- 
unpubhshed  material.  I  am  much  indebted 
to  Frances  Hamerstrom,  Plainfield  (Wis.), 
and  to  Robert  Rausch,  Anchorage  ( Alaska ) 
for  critically  revising  my  English  rough  copy, 
and  also  for  inducing  me  to  adjust  my  eco- 


logical terms   to  American  usage   and  to 
formulate  some  passages  more  precisely. 

The  main  emphasis  on  cyclic  work  for- 
merly was  mostly  placed  on  the  attempt  to 
get  to  the  bottom  of  the  causality  of  cycles 
by  analysing  and  explaining  the  periodicity 
from  phenological  data,  often  with  specula- 
tion on  cosmic  causalities  before  having  ex- 
plored all  terrestrial  events  and  influences. 
In  contrast,  the  German  researches  were 
concentrated  on  the  observation  and  analysis 
of  the  internal  events  occurring  in  cyclic 
populations  and  on  the  environmental  fac- 
tors influencing  them.  Naturally,  we  are 
not  able  to  solve  all  problems  connected 
with  microtine  cycles  in  so  short  a  time, 
but  I  dare  say  many  partial  solutions  have 
now  been  attained.  When  assembled,  they 
already  show  a  rough  picture  of  the  cyclic 
structure  established  on  a  foundation  of 
facts  containing  few  elements  of  a  specula- 
tive or  hypothetical  nature.  In  this  way  the 
cyclic  phenomenon  presents  itself — as  do 
other  biological  problems — as  an  interaction 
between  biological  events  and  environmen- 
tal factors  of  a  particularly  complicated 
structure,  depending  on  several  factor- 
groups  and  many  individual  factors. 

Population  Increase 

First,  population  increase  results  from 
three  factor-groups — the  "reproductive  po- 
tential" of  the  cyclic  species,  the  "carrying 
capacity"  of  the  environment,  and  that  which 
I  call  in  German  "Verdichtungspotential" 
(Frank,  1954b),  in  English  "condensation 
potential"  of  the  cyclic  species. 

Reproductive  Potential 

This  first  factor-group  is  based  on  age  at 
maturity,  litter  size,  litter  succession,  and 
length  of  the  reproductive  season.  Working 


113 


316 


114 


Journal  of  Wildlife  Management,  Vol.  21,  No.  2,  April  1957 


with  a  captive  population  of  more  than 
10,000  laboratory-reared  animals  (Frank, 
1956a )  and  individually  marked  wild  popu- 
lations of  M.  arvaJis  (yet  unpublished),  my 
findings  concerning  this  point  had  most  re- 
markable results.  M.  arvalis  distinguishes 
itself  by  having  a  pronounced  suckling-ma- 
turity. The  young  females,  which  suckle  un- 
til the  seventeenth  day,  already  show  a  per- 
forated vagina  from  the  eleventh  day  on 
and  are  mated  by  old  males  from  the  thir- 
teenth day  on.  Correspondingly,  the  earliest 
litters  were  dropped  by  a  wild  female  33 
days  old  and  by  a  captive  female  34  days  old 
(pregnancy  lasts  19-21  days,  on  an  average 
20  days ) .  Indeed  under  natural  conditions, 
a  high  proportion  of  the  young  females 
mate  in  the  maternal  home  range  before 
being  weaned  or  immediately  after  being 
weaned.^  But  this  happens  only  in  the  spring 
and  summer;  the  females  born  during  and 
after  September  for  the  most  part  do  not 
reach  sexual  maturity  in  the  same  year.  In 
the  autumn  the  young  generally  show  a  slow- 
er growth  rate  than  in  the  spring  and  sum- 
mer, when  an  astonishing  growth  rate  is  evi- 
dent. At  the  age  of  about  40  days  a  pregnant 
female  can  weigh  up  to  34g.,  and  the  males 
of  this  age  also  may  be  as  heavy  as  very  old 
animals.  Every  analysis  of  vole  populations 
for  age  classification  based  on  weight  classi- 
fication, therefore,  must  lead  to  serious 
errors,  and  conclusions  based  on  them  are 
subject  to  question  ( Frank  and  Zimmerman, 
1957). 

Besides  age  at  maturity,  reproductive  po- 
tential is  based  on  litter  size  and  litter  suc- 
cession. Litter  size  depends  upon  inherit- 
ance, upon  age  and  size  of  the  female,  and 
upon  season  ( Frank,  1956a ) ,  and  is  modified 
by  several  environmental  influences;  in  par- 
ticular, quality  and  quantity  of  food  are  of 
decisive  importance.  In  M.  arvalis  maximum 
litter  size  is  12;  in  one  case  Reichstein  (1957) 
found  13  embryos.  Under  optimal  condi- 
tions postpartum  mating  is  usual,  so  that  one 
litter  follows  another  every  20  days.  The 
maximum  number  of  litters  produced  by 


'Early  maturity  of  females  seems  to  be  a  general 
feature  of  the  genus  Microtus  because  I  found 
mating  females  20  days  old  also  in  M.  oeconomus 
(Frank  and  Zimmermann,  1956).  As  far  as  I  know 
suckling-maturity  among  other  mammals  has  hither- 
to been  established  only  for  Mustela  erminea  L. 
(Miiller,  1954). 


one  female  in  my  laboratory-reared  popula- 
tion of  more  than  10,000  animals  has  been 
33,  with  127  young  and  an  average  litter 
size  of  3.85.  Under  optimal  food  and  cli- 
matic conditions  in  spring  and  summer,  the 
average  litter  size  in  wild  populations  can 
amount  to  7  young.  Concerning  reproduc- 
tive efficiency,  M.  arvalis  represents  a  maxi- 
mum among  all  mammals  hitherto  investi- 
gated. In  captive  females  the  Htter  weight 
amounts  to  53.2  per  cent  of  the  mother's 
weight  (both  measured  immediately  after 
birth ),  while  in  other  mammals,  for  instance 
some  other  rodents  and  pygmy  dogs,  it  is 
only  one-third  (Frank,  1956a). 

Length  of  the  reproductive  season,  a  fur- 
ther factor  influencing  reproductive  poten- 
tial, continues  from  February  or  March  to 
October  or  November,  but  under  favourable 
conditions,  for  example  in  cornricks,  repro- 
duction goes  on  through  the  winter  ( Stein, 
1953a;  Frank,  1954b).  On  the  whole, 
M.  arvalis,  and  probably  M.  agrestis,  both 
showing  pronounced  cycles,  possess  an  un- 
common reproductive  potential  attainable 
under  the  optimal  environmental  conditions 
presented  in  the  plague  districts. 

Carrying  Capacity  of  Environment 

Whether  or  not  this  high  reproductive  po- 
tential causes  a  violent  population  increase 
depends  on  the  second  factor-group,  the 
carrying  capacity  of  the  environment.  In 
other  words,  it  depends  on  whether  or  not 
the  environment  can  support  a  high  popula- 
tion. The  individual  factors  influencing  this 
are  especially  food,  cover,  sunlight,  good 
overwintering  places,  and  ground-water 
level  (but  in  the  case  of  M.  arvalis  not  the 
nature  and  humidity  of  the  soil ) .  Also  it  is 
striking  that  all  plague  districts  of  M .  arvalis, 
although  they  lie  in  very  different  geological 
formations  (lowlands,  marshes,  fens,  loam 
steppes,  lower  mountain  regions,  etc. ),  show 
very  similar  characteristics  in  the  structure 
of  their  landscape.  They  always  represent 
large,  open,  monotonous,  and  uniform  bio- 
topes  with  extremely  scant  cover  of  trees 
and  bushes,  which  we  call  "cultivation 
steppes"  caused  by  human  activity  in  the 
once-wooded  or  marshy  central  European 
country.  Extremely  severe  and  regular 
plagues  of  M.  arvalis  occur  only  in  such 
biotopes,  evidently  representing  the  eco- 
logical optimum  for  this  species;  in  districts 
miscellaneously  covered  by  varied  biotopes 


317 


Causality  of  Microtine  Cycles  in  Germany — Frank 


115 


and  higher  proportions  of  woods,  trees,  and 
bushes,  only  moderate  fluctuations  are  visi- 
ble. Doubtless  these  circumstances  repre- 
sent certain  parallels  to  the  opinion  of 
Dymond  (1947),  that  the  uniformity  of  the 
arctic  biotopes  favours  the  amplitude  of 
cycles.  This  further  shows  that  not  only 
the  climate  but  also  the  structure  of  environ- 
ment is  important  for  the  origin  of  regular 
cycles,  which  indeed  are  observable  in  the 
temperate  zones  where  there  are  correspond- 
ing environmental  conditions.  The  abun- 
dance and  the  cycles  of  M.  arvalis  are  also 
influenced  by  the  economic  use  of  the  coun- 
try. Extensive  agricultural  use  favours 
plagues,  intensive  use  prevents  plagues.  On 
grazing  land  a  low  stock  of  cattle  and  an 
extensive  pasturing  favours  plagues,  while 
high  stocks  of  cattle  and  intensive  pasturing 
prevent  plagues  ( Frank,  1956b ) . 

Thus,  in  central  Europe,  the  cycles  of 
M.  arvalis  are  "released"  by  human  cultiva- 
tion. This  enables  us  to  stop  the  develop- 
ment of  plagues  by  an  ecological  and  eco- 
nomic reorganisation  of  the  plague  districts. 
Based  on  this  example  the  author  has  postu- 
lated the  introduction  of  the  more  effective 
"ecological  plague  control"  for  crop  protec- 
tion, rather  than  the  usual  chemical  pest 
control  by  poisons  and  biological  control  by 
encouragement  of  enemies  and  parasites 
(Frank,  1956b).  In  principle,  the  same  is 
valid  for  M.  agrestis,  which  shows  regular 
fluctuations  only  in  former  woodland  where 
the  trees  have  been  felled  or  new  plantations 
of  trees  are  laid  out,  and  tlie  bare  plains  are 
covered  with  large  grass  jungles,  evidently 
representing  the  ecological  optimum  for  this 
species  (Frank,  1952,  1954b).  In  any  case 
true  cycles  appear  only  under  optimal  en- 
vironmental conditions  permitting  both  the 
realization  of  the  high  reproductive  potential 
and  the  establishment  of  the  descendants 
produced  by  this  potential:  in  other  words, 
where  a  high  carrying  capacity  is  present. 
On  this  point  our  conclusions  probably  come 
near  to  some  of  the  ideas  expressed  by  Paul 
Errington. 

Condensation  Potential 

The  degree  of  the  population  increase 
depends  decisively  on  the  third  factor-group: 
the  condensation  potential,  which  consists 
of  certain  behaviour  mechanisms  that  en- 
able many  cyclic  species  to  live  at  an  un- 
commonly high  population  density.   Before 


describing  these  behaviour  mechanisms  I 
must  explain  the  new  term  "condensation 
potential"  (Frank,  1954b).  It  is  based  on 
all  intraspecific  and  especially  social  be- 
haviour that  favours  the  increase  of  density. 
Normally  the  condensation  potential  is 
limited  by  intrinsic  behaviour,  especially  by 
territoriality,  to  a  "saturation  point"  which 
is  approximately  adapted  to  the  carrying 
capacity  of  the  environment.  It  seems  to 
be  a  feature  of  many  cyclic  species  that  they 
show  particular  social  behaviour  that  abol- 
ishes the  normal  limits,  and  enables  them, 
under  optimal  environmental  conditions,  to 
exceed  the  saturation  point  so  far  that  the 
carrying  capacity  of  the  environment  is 
greatly  exceeded,  and  simultaneously  popu- 
lation regulation  by  crash,  mass  emigration, 
or  other  drastic  mechanisms  becomes  neces- 
sary and  inevitable.  In  M.  arvalis  the  con- 
densation potential  concerns:  reduction  of 
the  home  ranges,  social  communities  of  the 
females,  and  diminution  or  elimination  of 
males.  These  points  seem  worth  stressing 
as  aspects  of  cycle  research  that  further  the 
understanding  of  this  phenomenon  and  of 
population  dynamics  in  general  (Frank, 
1954b,  1956a). 

Fundamentally  the  European  microtines 
are  territorial  animals;  this  we  have  demon- 
strated in  the  laboratory  (Frank,  1953a, 
1956a)  as  well  as  in  individually  marked 
wild  populations.  Females  occupy  a  range 
around  their  burrows  where  they  tolerate  no 
stranger  of  their  species.  Females  tolerate 
a  strange  male  in  their  home  ranges  only 
when  they  are  in  heat  and  even  then  the  male 
must  fight  to  approach.  With  the  exception 
of  the  short  period  of  heat,  all  strangers  of 
either  sex  are  driven  away.  This  home  range 
has  a  diameter  of  10-20  meters  during  the 
reproductive  season.  Males  inhabit  an  ir- 
regular larger  range,  wandering  from  female 
to  female  to  mate  those  that  are  in  heat. 
They  are  only  intolerant  of  strange  males  of 
mature  age.  Recently  we  found  that  in 
spring  and  summer  the  young  males  with- 
out exception  disappear  from  their  mother's 
territory  and  its  surroundings  after  becoming 
mature,  and  the  old  males  mating  the  resi- 
dent females  are  all  strangers,  having  im- 
migrated from  other  places.  This  would 
tend  to  prevent  inbreeding.  In  contrast,  the 
young  females  settle  in  the  immediate  vicin- 
ity of  their  mother's  home  range,  or  some- 
times within  it.  When  space  becomes  scarce, 


318 


116 


Journal  of  Wildlife  Management,  Vol.  21,  No.  2,  April  1957 


the  size  of  the  home  ranges  can  be  reduced. 
This  also  gives  the  voles  a  considerable  con- 
densation potential  (Frank,  1953a). 

In  contrast  to  the  territorial  behaviour 
that  causes  intraspecific  demarcation  and 
guarantees  the  individual  space  and  food 
needed  for  life  and  reproduction,  the  follow- 
ing mechanisms  favour  life  in  social  com- 
munities and  also  high  density.  In  the  first 
place  we  have  die  "mother-family,"  con- 
sisting of  the  female  and  her  suckling  young, 
sometimes  also  her  unmated  subadult  off- 
spring. But  this  is  not  typical  of  spring  and 
summer  when,  for  the  most  part,  the  weaned 
young,  particularly  the  males,  leave  the 
maternal  home  range.  "Great  families"  arise 
every  autumn,  for  the  last  two  to  three  litters 
of  the  year  remain  in  the  maternal  home 
range  (because  the  female  does  not  drive 
them  out ) ,  and  constitute  the  overwintering 
community  (Frank,  1954a).  This  lightens 
existence  in  the  cold  season  when  stress  is 
great;  all  live  together  in  a  single,  thickly 
lined  nest,  the  many  small  individuals  form 
a  greater  thermal  unit,  and  the  loss  of  heat 
and  energy  is  significantly  reduced.  Freez- 
ing weather  and  heavy  precipitation  reduce 
the  activity  of  the  voles,  which  remain  in 
their  nests  and  eat  the  food  stores  they 
have  brought  in  during  autumn.  Neverthe- 
less, the  size  of  the  home  ranges  and  the 
radius  of  activity  of  the  voles  is  importantly 
enlarged  during  winter  (about  four  or  five 
times  larger  than  the  summer  home  range ) , 
probably  because  of  both  the  greater 
number  of  the  inhabitants  (overwintering 
community  instead  of  the  female  and  her 
last  litter  in  summer),  and  because  of  the 
shortage  of  available  food  requiring  a  larger 
feeding  area  for  these  herbivorous  animals. 
In  the  peak  years  the  impossibility  of  such 
an  enlargement  of  activity  radius,  caused 
by  population  density,  might  contribute 
much  to  intensify  competition  for  food  and 
to  bring  on  a  crash  situation.  In  spring  the 
overwintering  communities  dissolve  by 
scattering. 

Furthermore,  a  behaviour  mechanism  of 
highest  importance  is  involved  in  the  nest 
communities  of  the  females  ( Frank,  1953a ) , 
Increasingly  with  population  condensation, 
the  young  females  remain  together,  occupy 
a  common  territory,  and  bring  up  their 
litters  in  a  single  nest  by  means  of  social 
breeding  care.  Generally  they  remain  to- 
gether for  the  rest  of  their  lives,  and  if  they 


change  their  home  range  because  of  distur- 
bance, etc.,  they  move  as  a  community,  often 
with  their  young  also.  The  nest  community 
can  consist  of  2-4  (perhaps  5)  sisters,  and 
sometimes  of  their  mother  too.  The  decisive 
influence  of  this  behaviour  upon  the  popu- 
lation dynamic  is  that  it  enables  these  pri- 
marily territorial  animals  to  Hve  in  an  ab- 
normally high  density.  In  this  way  not  only 
more  females  can  live  in  the  same  space, 
but  also  a  correspondingly  greater  number 
of  young  can  be  produced  and  brought  up. 
Doubtless  this  particular  social  behaviour  of 
M.  arvolis  explains  the  uncommon  popula- 
tion density  and  the  outright  explosive  popu- 
lation increase  in  plague  centres,  i.e.,  those 
parts  of  the  plague  districts  ecologically  most 
favourable  and  first  occupied  by  the  voles. 

In  contrast  to  the  females,  the  mature 
males  cannot  draw  so  near  to  one  another 
because  they  generally  display  rivalry  (ex- 
cept as  members  of  a  family  or  of  an  over- 
wintering community).  During  population 
increase  in  a  given  space,  the  number  of 
old  males  remains  the  same,  while  that  of 
the  mature  females  rapidly  increases.  Pro- 
gressing with  population  condensation,  a 
considerable  elimination  of  mature  males 
occurs  (Frank,  1953a,  1954a,  1954b;  Stein, 
1953b).  This  reduction  is  also  evident  from 
the  pellets  of  owls  ( Becker,  1954 ) ,  and  thus 
not  caused  by  selective  predation  (on  the 
males),  but  by  intraspecific  competition 
( among  the  males ) .  In  spring  and  summer 
the  weaned  young  males,  without  exception, 
leave  their  birthplaces,  probably  because  of 
an  innate  drive  after  maturing.  They  must 
look  for  a  new  home  range  and  come  up 
against  all  other  males  they  meet.  Whether 
their  number  diminishes  by  killing  each 
other  or  merely  by  driving  each  other  away 
requires  further  observations.  A  large  num- 
ber of  the  wild  males  show  injuries,  espe- 
cially bites  in  the  region  of  the  hindquarters, 
and  lost  tails,  caused  by  intraspecific  fight- 
ing; however,  these  injuries  might  have  been 
acquired  from  resident  females  as  well  as 
from  other  males. 

Thus  we  see  that  the  intraspecific,  es- 
pecially social,  behaviour  of  the  animals  is 
of  great  importance  to  all  population-dy- 
namic events.  Further  research  is  needed 
on  this  point,  especially  in  other  cyclic 
species,  to  find  out  whether  similar  or  other 
condensation  mechanisms  are  prevalent. 


319 


Causality  of  Microtine  Cycles  in  Germany — Frank  117 

Population  Decline  curs  among  them  during  spring.   They  do 

not  mount  in  weight  and  can  hardly  bring 
What  causes  the  population  decline  of  up  their  young,  which  therefore  show  heavy 
M.  arvalis?  The  life  span  of  the  little  micro-  mortality.  This  has  already  been  pointed  out 
tines  is  naturally  short.  Periods  of  crises  and  by  Chitty  ( 1952,  1955 )  and  in  every  way 
losses  seem  to  be:  ( 1 )  becoming  acquainted  confirmed  also  by  my  own  researches  in 
with  the  maternal  home  range  first,  in  which  outdoor  cages  ( Frank,  1954a )  as  well  as  by 
there  is  danger  if  strange  neighbours  are  research  on  wild  populations  of  M.  arvalis 
encountered;  (2)  the  period  of  spreading  and  M.  agres^is  (as  yet  unpublished).  There- 
after weaning,  which  involves  heavier  losses  fore,  vole  populations  always  have  a  diffi- 
in  the  males  than  in  the  females;  and  (3)  cult  and  slow  start  toward  recovery  after 
the  winter  season,  which  normally  dimin-  severe  winters  and  after  crashes.  Predation 
ishes  the  population  up  to  50  per  cent  or  plays  only  a  very  small  part,  because  preda- 
more  (Frank,  1954b).  The  animals  of  my  tors  are  not  at  all  numerous  in  the  plague 
marked  wild  populations  never  survived  districts,  having  been  kept  down  both  by 
two  winters,  and  the  markedly  old  individ-  the  unfavourable,  monotonous  and  coverless 
uals  almost  all  succumb  to  the  stresses  of  the  biotope  and  by  human  persecution  ( Frank, 
first  winter  months.  Not  only  those  individ-  1954b,  1955,  1956b). 

uals  that  have  survived  a  winter  die,  but  In  the  peak  years  characterized  by  over- 
also  those  born  in  spring  and  summer  that  crowding,  the  regulation  of  microtine  popu- 
had  reproduced  suffer  mortality.  Their  body  lation  density  by  no  means  shows  itself  as 
weight  gradually  diminishes  throughout  the  mass    emigration    as    with    the    lemmings 
autumn,  and  their  body  reserves  are  nearly  (Lemmus   lemmus   L. ),   for  we   observed 
consumed  by  then.   In  contrast,  the  young  movement  of  individuals  only,  more  com- 
animals  born   in   the  autumn   increase  in  monly  in  the  males  than  in  the  females.  As 
weight  and  lose  only  a  little  in  the  begin-  previously  stated,  the  latter  are  generally  in- 
ning of  winter;  then  their  weight  is  main-  dined  to  settle  in  the  neighbourhood  of  their 
tained  during  the  winter  months   (mostly  birthplaces  as  long  as  they  are  able  to  find 
about  12- 18g.)  and  mounts  again  quickly  in  places  unoccupied  by  other  females.    But 
early  spring.  While  the  period  of  spreading  space  finally  becomes  scarce  ( in  spite  of  and 
causes  heavier  losses  among  males,  winter  after  reduction   of  the  size   of  the  home 
mortality  strikes  more  females  because  they  ranges )  and  competition  among  females  in- 
are  mostly  somewhat  smaller  and  weaker  creases.   Reproduction  is  then  gradually  re- 
( Frank,    i954b).     Nevertheless,    mortality  stricted  (Frank,  1953a,  1954a).  The  degree 
effects  a  real  selection  by  eliminating  the  of   embryonal   resorptions,   infertility,   and 
less  fit  individuals.  After  the  winter  period,  mortality  of  young  all  mount  quickly,  but 
the  surviving  population  consists  nearly  ex-  population  density  can  no  longer  be  regu- 
clusively  of  autumn-born  animals  that  had  lated  by  these;  the  carrying  capacity  of  the 
remained  sexually  immature  until  spring,  environment  has  already  been  greatly  ex- 
The  older  voles,  already  having  participated  ceeded.  For  this  reason  regulation  must  be 
in  reproduction  during  the  last  year,  have  performed  by  a  more  effective  mechanism: 
vanished  with  only  few  exceptions.  the  crash.  Our  investigations  could  not  pro- 
Winter  mortality  can  be  so  great,  partic-  d^ce  any  evidence  for  the  hypothesis  that 
ularly  in  extremely  severe  winters,  that  the  epizootic   diseases   or  parasites   cause   the 
population  declines  to  a  minimum  level  by  crash,  although  our  material  was  examined 
a  gradual  die-off  of  most  individuals;  but  by  many  specialists  (Frank,  1953b).  An  ex- 
this  happens  only  when  population  density  planation  was  only  possible  on  the  basis  of 
is  not  high  enough  to  produce  a  regular  Christian's  (1950)  important  idea  that  the 
crash.  However,  the  physiological  mechan-  "shock  disease"  of  the  varying  hare  ( Lepus 
ism  of  this  gradual  die-off  seems  to  be  similar  americanus  Erx. ) ,  discovered  by  Green  and 
to  that  of  the  regular  crash,  and  to  be  based  Larson  ( 1938 ),  seems  to  be  an  appearance  of 
on  the  endocrine  system  also  (see  below),  the  general  adaptation  syndrome  of  Selye 
In  this  way,  the  stress  of  such  a  severe  winter  ( 1946 ) . 

can  injure  the  survivors  of  the  gradual  die-  First  I  must  say  that  the  crash  symptoms 

off  (and  also  of  a  regular  crash)  so  much  in  M.  arvalis  are  the  same  as  in  L.  amer- 

that  a  remarkable  subsequent  mortality  oc-  icanus:    lethargy,  convulsions,  liver  degen- 


320 


118 


Journal  of  Wildlife  Management,  Vol.  21,  No.  2,  April  1957 


oration,  enlargement  of  the  adrenals  and 
hypoglycemia,  and  moreover  (not  mentioned 
by  Green  and  Larson)  marked  decline  in 
body  temperature  long  before  death,  and 
behavioural  changes  such  as  crowding  and 
cannibalism.  The  last  represents  an  impor- 
tant chance  for  survival  of  the  fitter  individ- 
uals by  making  use  of  the  carcasses  of  their 
dead  companions  as  food  reserves  during  the 
period  of  general  deficiency  or  shortage  of 
vegetable  food  already  used  up  by  the  over- 
crowded population  (Frank,  1953b).  Not 
only  have  we  found  these  symptoms  experi- 
mentally in  outdoor  cages  where  vole  popu- 
lations were  kept  overcrowded  and  showed 
drastic  crashes,  but  we  were  also  able  to 
produce  crash  symptoms  by  artificial  hypo- 
glycemia induced  by  insulin  injections;  con- 
versely, the  symptoms  could  be  suspended, 
temporarily  at  least,  by  injection  of  grape 
sugar  (Frank,  1953b). 

We  get  the  impression  that  condensation 
and  crowding  favour  competition  and  cause 
a  state  of  psychological  excitement  being 
transformed  by  the  pituitary-adrenocortical 
system  into  a  physical  stress.  This,  acutely 
combined  with  the  stress  of  food  shortage, 
produces  a  "readiness"  for  crash,  whether 
the  real  releasing  of  the  crash  is  caused  by 
an  increase  in  the  force  of  these  stresses,  or, 
in  nature,  largely  by  additional  meteorologi- 
cal stresses,  such  as  periods  of  cold  or  pre- 
cipitation. On  the  whole,  a  situation  with 
several  stress-producing  components  ulti- 
mately produces  the  resulting  "crash"  either 
when  all  stress  factors  jointly  reach  a  critical 
point  or  value,  or  when  a  new  stress  is  super- 
imposed on  the  already  stressed  adreno- 
pituitary  system. 

In  my  opinion,  our  results  confirm  the 
basic  trends  of  ideas  presented  by  Christian's 
( op.  cit. )  important  working  hypothesis,  but 
my  results  differ  in  one  essential  point. 
Christian  supposes  that  the  crash,  the  readi- 
ness for  which  is  brought  about  by  several 
stresses,  is  ultimately  caused  and  released 
by  the  additional  stress  of  the  activation  of 
gonads  happening  in  the  early  spring.  But 
I  never  found  any  enlargement  of  testes  and 
uteri  in  crashing  wild  populations.  Also  in 
my  experimentally  induced  crashes  of  out- 
door-cage populations,  activation  of  gonads 
was  certainly  not  in  play.  I  am  therefore 
convinced  that  gonadotrophic  demands  are 
not  involved  in  the  crash  phenomenon,  in 
Microtus  at  least.    In  my  conception  the 


ultimate  trigger,  producing  the  crash  of  vole 
populations,  is  an  additional  stress  of  mete- 
orological events,  particularly  frost  periods. 
I  believe  that  this  conception  explains  better 
than  Christian's  the  sudden  advent  of  a 
crash  within  a  few  days.  The  stress  of 
gonadotrophic  demands  would  be  extended 
over  longer  time  and  would  operate  in  very 
different  moments  upon  the  single  animal. 
In  contrast,  the  meteorological  stress  caused 
by  the  intrusion  of  frost  periods  acts  equally 
and  suddenly  upon  all  individuals  and  makes 
more  easily  understandable  the  suddenness 
of  the  crash. 

Nevertheless,  gonadotrophic  activation 
might  play  an  essential  role,  indeed,  in  the 
subsequent  mortality  occurring  in  spring 
among  the  survivors  from  crashes  and  grad- 
ual winter  die-offs,  which  was  discovered  by 
Chitty  ( op.  cit. )  and  also  found  in  the  vole 
populations  investigated  by  the  author  ( see 
above).  In  this  case,  gonadotrophic  activa- 
tion presents  a  true  additional  stress  upon 
the  endocrinological  system,  as  Christian  has 
supposed. 

I  must  emphasize  that  this  conception  is 
based  on  investigations  in  vole  populations 
only.  In  any  event,  it  now  seems  to  be  cer- 
tain that  the  adreno-pituitary  system  has  de- 
cisive importance  in  intraspecific  regulatory 
events  occurring  in  vertebrate  populations. 
Further  research  is  needed  to  complete  and 
deepen  our  knowledge  of  this  important 
point,  and  to  find  out  in  what  manner  and 
with  which  different  effects  this  psycho- 
physiological mechanism  is  operating  and 
which  environmental  factors  are  acting  up- 
on them,  in  voles  as  well  as  in  other  rodents 
and  vertebrates  generally. 

The  Periodicity  of  Cycles 

Many  workers  on  the  periodicity  of  cycles 
(recently  again  Siivonen  and  Koskimies, 
1955 )  attempt  to  connect  this  problem  with 
cosmic  factors  before  having  explored  all 
terrestrial  environmental  factors  possibly 
influencing  it.  But  nearly  all  such  work  on 
this  subject  generally  seems  to  suffer  from 
the  fact  that  the  phenological  data,  particu- 
larly the  meteorological  conditions,  are  not 
brought  into  relationship  as  the  most  im- 
portant environmental  factors  acting  upon 
cyclic  populations.  Favoured  by  the  ex- 
tremely equalized  temperate  climate  in  the 
Gulf  Stream  neighbourhood  of  northwestern 
Germany,  Maercks  ( 1954 )  has  been  able  to 


321 


Causality  of  Microtine  Cycles  in  Germany — Frank 


119 


evaluate  the  interaction  between  the  cycles 
of  M.  arvalis  and  meteorological  events  over 
a  period  of  39  years,  based  on  the  five-day 
median  values  of  temperature,  quantity  and 
frequency  of  precipitation,  and  duration  of 
sunshine.  Therefore  the  cyclic  events  take 
place  in  a  rather  "pure  culture"  generally 
little  influenced  by  extreme  changes  in 
weather  conditions,  which — if  they  occurred 
— could  easily  be  analysed  regarding  their 
effects  on  the  cyclic  events.  Maercks  found 
a  clear  and  strict  microtine-cycle  periodicity 
of  three  years  from  peak  to  peak,  obviously 
caused  by  the  reproductive  and  condensa- 
tion potential  of  the  species  and  the  carrying 
capacity  of  its  environment.  Under  optimal 
environmental  conditions  M.  arvalis  is  able 
to  replenish  a  plague  district  within  three 
years  so  completely  that  the  carrying  capa- 
city is  exceeded  and  natural  regulation  by 
crash  must  occur.  Every  population  has  its 
own  autonomous  periodicity,  and  in  other 
spheres  ( other  species  or  other  environment, 
or  both)  there  will  be  other  frequencies  of 
the  periodicity  (Frank,  1954b).  Dymond 
( 1947 )  has  already  suggested  that  animals 
with  a  high  and  constant  reproductive  po- 
tential may  be  able  to  populate  deficiently 
buffered^  biotopes  of  optimal  and  constant 
ecological  conditions  at  regularly  occurring 
intervals  to  an  unbearable  density. 

As  to  the  influence  of  meteorological  con- 
ditions, Maercks  (ibid.)  found  frequent 
quantitative  oscillations  in  the  degree  of  the 
peak  population  density  and  plague  damage, 
but  few  temporal  mutations  of  the  periodi- 
city itself.  The  former  are  caused  by  changes 
of  rainfall  and  duration  of  sunshine,  for  ex- 
ample, while  the  latter  are  all  reducible 
to  uncommon  and  extreme  deviations  in 
weather  conditions,  especially  in  winter.  In 
the  39  years  investigated  by  Maercks,  the 
three-year  periodicity  has  undergone  three 
mutations,  which  led  to  the  following  con- 
clusions: (1)  A  particularly  mild  winter 
prolongs  the  plague  over  a  two-year  period, 
and  therefore  the  cyclic  interval  extends  to 
four  years,  because  the  expected  crash  does 
not  happen  but  comes  a  year  later;  ( 2 )  an 
extremely  long  and  severe  winter  cuts  off 
the  population  increase  by  causing  a  gradual 


*These  are  biotopes  with  a  scarcity  of  natural 
counterpowers  to  the  species  in  question,  as  enemies, 
competition  by  other  species,  limit  of  food  and  habi- 
tats, or  other  unfavourable  ecological  conditions. 


die-off  or  a  precocious  crash  and  forcing  a 
new  start  of  population  increase. 

In  both  cases  the  cycle  periodicity  suffers 
a  shifting  of  phase  by  one  year  (or  more 
perhaps  in  other  cases).  This  shiJFting,  in- 
deed, is  a  point  in  the  cycle  phenomenon 
that  has  caused  considerable  difficulty  to 
cycle  workers,  who  have  almost  established 
a  periodicity  of  3  1/3  years.  But  this  was 
unsatisfactory  because  the  cyclic  periodicity 
is  based  ( in  my  opinion  at  least )  on  the  re- 
productive season's  being  fixed  by  the  astro- 
nomical year.  Every  biological  periodicity 
extended  over  several  years  might  also  pre- 
sent whole  numbers  corresponding  to  the 
whole  numbers  of  years.  This  difficulty  is 
removed  by  the  shifting  of  phase  caused  by 
meteorological  deviations  that  occur  in  every 
climate;  the  phase  shift  easily  explains  the 
fact  that  animal  cycles  never  show  a  sym- 
metrical periodicity  over  a  long  period  of 
time  but  always  show  a  few  exceptions  or 
deviations  from  the  prevailing  equal  pe- 
riodicity ( three  years  in  the  case  of  Microtus 
arvalis ) . 

Also  the  striking  conformity  in  the  peri- 
odicity of  different  cyclic  populations  and 
plague  districts,  independent  of  and  isolated 
from  each  other,  is  produced  by  meteoro- 
logical conditions  prevailing  equally  over  a 
large  region  ( Frank,  1954b ) .  For  example, 
an  uncommon  and  extremely  severe  winter 
will  simultaneously  throw  back  all  popula- 
tions influenced  by  it  ( each  having  its  own 
autonomous  periodicity  previously),  to  a 
new  (and  common)  starting  point.  Never- 
theless, some  populations  exposed  to  special 
environmental  conditions  can  show  a  dif- 
ferent periodicity,  most  commonly  because 
favourable  overwintering  conditions  have 
counterbalanced  unfavourable  meteorologi- 
cal conditions. 

Summary 

The  results  of  recent  work  on  microtine 
cycles  occurring  in  Germany  enable  us  to 
understand  this  phenomenon  as  an  inter- 
action between  biotic  and  environmental 
factors  only,  and  without  aid  of  any  hypo- 
thetical explanation  by  extraterrestrial  "cos- 
mic" factors.  It  may  be  supposed  that  the 
causality  of  other  animal  cycles  will  find 
a  similarly  "natural"  explanation  after  being 
explored  as  intensively  as  the  cycles  of  Mi- 
crotus arvalis  in  Germany.   Although  these 


322 


120 


Journal  of  Wildlife  Management,  Vol.  21,  No.  2,  April  1957 


are  indeed  "released"  by  human  cultivation 
measures,  which  have  produced  optimal  bio- 
topes  and  thus  the  ecological  base  of  cycles, 
the  biotic  causalities  and  laws  of  these  cycles 
must  be  the  same  as  those  prevailing  in 
cycles  occurring  in  natural  districts  not  in- 
fluenced by  man. 

Concerning  M.  arvalis  the  population  in- 
crease is  based  on:  ( 1 )  a  high  reproductive 
potential  based  on  ( a )  extremely  early  ma- 
turity and  mating  (in  females  often  before 
being  weaned),  (b)  high  reproductive  ef- 
ficiency (litter  weights  to  53.2  per  cent  of 
the  mother's  weight),  (c)  large  litter  size 
(maximum  12-13,  average  in  wild  popula- 
tions about  7  young),  (d)  rapid  litter  suc- 
cession (pregnancy  about  20  days,  post- 
partum mating  normal),  and  (e)  extended 
season  of  reproduction  ( sometimes  through- 
out winter);  (2)  a  high  carrying  capacity 
of  the  environment  under  the  optimal  eco- 
logical conditions  of  the  plague  districts, 
based  on  food,  cover,  ground-water  level, 
sunlight,  overwintering  places,  and  last  but 
not  least  on  the  uniform  structure  of  the 
landscape;  and  (3)  a  high  "condensation 
potential"  based  on  behaviour,  particularly 
social  mechanisms  concerning  ( a )  reducible 
home-range  size  during  population  increase, 
formation  of  (b)  "great  families"  and  (c) 
overwintering  communities,  (d)  communal 
nesting  of  females,  and  (e)  elimination  of 
males.  On  the  whole,  these  factors  suffi- 
ciently explain  the  outright  explosive  in- 
crease and  the  uncommon  density  of  micro- 
tine  populations  in  German  plague  districts. 

Because  this  rapid  population  increase 
cannot  be  regulated  by  normal  mortality 
and  dispersal,  more  efficient  regulatory 
mechanisms  are  called  into  play.  When  the 
supportable  density  of  population  is  ap- 
proached, restriction  of  reproduction  and 
accelerated  individual  emigration  take 
place,  but  these  are  not  enough  to  keep  the 
population  within  the  limits  set  by  the  car- 
rying capacity  of  the  environment.  When 
supportable  density  is  exceeded,  crash, 
caused  by  shock  disease,  occurs  in  the  fol- 
lowing winter.  Psychological  stresses  ( such 
as  crowding  and  competition )  and  physical 
stresses  (such  as  food  shortage)  produce  a 
"readiness"  for  crash,  but  the  real  trigger 
is  largely  the  additional  meteorological  stress 
of  winter.  Three  years  are  ordinarily  re- 
quired to  reach  this  point,  hence  an  auto- 
nomous and  strict  3-year  periodicity  exists. 


The  seldom-occurring  deviations  ("shifting 
of  phase")  are  caused  only  by  uncommon 
meteorological  conditions.  Unusually  severe 
winters  synchronize  the  periodicity  of  iso- 
lated populations  over  large  districts. 

On  the  whole,  cycles  take  place  where  the 
high  biotic  potential  of  the  species  is  fully 
realizable  in  the  optimal  biotopes  of  plague 
or  other  cyclic  districts.  It  seems  remarka- 
ble that  this  disproportion  is  not  balanced 
by  selection.  Cycles  have  undoubtedly  gone 
on  from  time  immemorial,  and  the  quick 
succession  of  generations  of  voles  should 
have  favoured  such  an  adaption  in  a  rela- 
tively short  time. 

Literature  Cited 

Becker,  K.  1954.  Beitrage  zur  Geschlechtsbestim- 
mung  von  Mausen  (Muridae)  nach  Skelettresten 
aiis  Eulengewollen.  Zool.  Jahrb.  ( Systematik ) , 
82:463-472. 

Chitty,  D.  1952.  Mortality  among  voles  ( Microf us 
agrestis)  at  Lake  Vyrnwy,  Montgomeryshire, 
in  1936-39.  Phil.  Trans.  Roy.  Soc.  London, 
Ser.  B,  236:505-552. 

.  1955.  Adverse  effects  of  population  den- 
sity upon  the  viability  of  later  generations. 
Pp.  57-67  in:  "The  numbers  of  man  and  ani- 
mals," edited  by  J.  B.  Cragg  and  N.  W.  Pirie. 
Oliver  and  Boyd,  Edinburgh.    152pp. 

Christian,  J.  J.  1950.  The  adreno-pituitary  system 
and  population  cycles  in  mammals.  J.  Mamm., 
31:247-259. 

Dymond,  J.  R.  1947.  Fluctuations  in  animal  popu- 
lations with  special  reference  to  those  of 
Canada.  Trans.  Roy.  Soc.  Canada,  Ser.  Ill, 
16:1-34. 

Frank,  F.  1952.  Umfang,  Ursachen  und  Bekampf- 
ungsmoglichkeiten  der  Mausefrassschaden  in 
Forstkulturen.  Nachrichtenbl.  Deutsch.  Pflan- 
zenschutzdienst  (Braunschweig),  4:183-189. 

.   1953a.  Zur  Entstehung  iibemormaler  Pop- 

ulationsdichten  im  Massenwechsel  der  Feld- 
maus,  Microtus  arvalis  (  Pallas  ) .  Zool.  Jahrb. 
(Systematik),  81:610-624. 

.    1953b.   Untersuchungen  iiber  den  Zusam- 

menbruch  von  Feldmausplagen  (Microtus  ar- 
valis Pallas).  Zool.  Jahrb.  (Systematik), 
82:95-136. 

.    1953c.    Zur  Entstehung  neuer  Feldmaus- 

plagegebiete  durch  Moorkultivierung  und 
Melioration.  Wasser  und  Boden  (Hannover), 
5:342-345. 

.    1954a.    Beitrage  zur  Biologic  der  Feld- 

maus,  Microtus  arvalis  (Pallas).  Teil  I: 
Gehegeversuche.  Zool.  Jahrb.  (Systematik), 
82:354-404. 

.   1954b.  Die  KausaUtat  der  Nagetier-Zyklen 

im  Lichte  neuer  populationsdynamischer  Un- 


323 


Causality  of  Microtine  Cycles  in  Germany — Frank 


121 


tersuchungen  an  deutschen  Microtinen.    Zeit- 
schr.  f.  Morphol.  u.  Oekol.,  43:321-356. 

— .  1955.  Naturschutz  und  Mauseplagen. 
Natur  und  Landschaft  (Liineburg),  30:109- 
112. 

— .  1956a.  Beitrage  zur  Biologic  der  Feld- 
maus,  Microtus  arvalis  (Pallas).  Teil  II: 
Laboratoriumsergebnisse.  Zool.  Jahrb.  (Sys- 
tematik),  84:32-74. 

— .  1956b.  Grundlagen,  Moglichkeiten  und 
Methoden  der  Sanierung  von  Feldmausplage- 
gebieten.  Nachrichtenbl.  Deutsch.  Pflanzen- 
schutzdienst  (Braunschweig),  8:147-158. 

—  AND  K.  ZiMMERMANN.  1956.  Zur  Biologic 
der  Nordischcn  Wiihlmaus  (Microtus  oecono- 
mus  stimmingi  Nehring).  Zeitschr.  f.  Sau- 
getierkundc,  21:58-83. 

1957.    Die  Verwendbarkeit  morphologis- 


cher  Merkmale  als  Alterskritericn  bei  der 
Fcldmaus,  Microtus  arvalis  (Pallas).  Zool. 
Jahrb.  (Systcmatik),  85:  in  press. 

Green,  R.  G.  and  C.  L.  Larson.  1938.  A  descrip- 
tion of  shock  disease  in  the  snowshoe  hare. 
Amer.  J.  Hyg.,  28:190-212. 

Maercks,  H.   1954.   Uber  den  Einfluss  der  Witter- 


ung  auf  den  Massenwechsel  der  Feldmaus 
( Microtus  arvalis  Pallas  )  in  der  Wesermarsch. 
Nachrichtenbl.  Deutsch.  Pflanzenschutzdienst 
(Braunschweig),  6:101-108. 

MiJLLER,  H.  1954.  Zur  Fortpflanzungsbiologie  des 
Hermelins  (Mustela  erminea  L. ).  Rev.  Suisse 
Zool.,  61:451-453. 

Reichstein,  H.  1957.  Feldmaus,  Microtus  arvalis 
(Pallas  1779),  mit  13  Embryonen.  Saugetier- 
kundliche  Mitt.,  5:  in  press. 

Selye,  H.  1946.  The  general  adaptation  syndrome 
and  the  diseases  of  adaptation.  J.  Clin.  Endo- 
crinol., 6:117-230. 

SiivoNEN,  L.  AND  J.  KosKiMiES.  1955.  Population 
fluctuations  and  the  lunar  cycle.  Papers  on 
Game  Research  (Helsinki),  14:1-22. 

Stein,  G.  H.  W.  1953a.  Uber  Umweltabhangig- 
keiten  bei  der  Vermehrung  der  Feldmaus, 
Microtus  arvalis.  Zool.  Jahrb.  ( Systematik ) , 
81:527-547. 

.     1953b.     tJber   das   Zahlenverhaltnis    der 

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Received  for  publication  October  9,  1956. 


324 


TERRITORIALITY  AND   HOME   RANGE   CONCEPTS   AS  APPLIED 

TO  MAMMALS 

By  William  Henry  Burt 

territoriality 

The  behavioristic  trait  manifested  by  a  display  of  property  ownership — a 
defense  of  certain  positions  or  things — reaches  its  highest  development  in  the 
human  species.  Man  considers  it  his  inherent  right  to  own  property  either  as 
an  individual  or  as  a  member  of  a  society  or  both.  Further,  he  is  ever  ready 
to  protect  that  property  against  aggressors,  even  to  the  extent  at  times  of 
sacrificing  his  own  life  if  necessary.  That  this  behavioristic  pattern  is  not 
peculiar  to  man,  but  is  a  fundamental  characteristic  of  animals  in  general,  has 
been  shown  for  diverse  animal  groups.  (For  an  excellent  historical  account 
and  summary  on  territoriality,  with  fairly  complete  bibliography,  the  reader  is 
referred  to  a  paper  by  Mrs.  Nice,  1941).  It  does  not  necessarily  follow  that 
this  trait  is  found  in  all  animals,  nor  that  it  is  developed  to  the  same  degree  in 
those  that  are  known  to  possess  it,  but  its  wide  distribution  among  the  verte- 
brates (see  Evans,  L.  T.,  1938,  for  reptiles),  and  even  in  some  of  the  invertebrates, 
lends  support  to  the  theory  that  it  is  a  basic  characteristic  of  animals  and  that 
the  potentialities  are  there  whether  the  particular  animal  in  question  displays 
the  characteristic.     Heape  (1931,  p.  74)  went  so  far  as  to  say: 

"Thus,  although  the  matter  is  often  an  intricate  one,  and  the  rights  of  terri- 
tory somewhat  involved,  there  can,  I  think;  be  no  question  that  territorial 
rights  are  established  rights  amongst  the  majority  of  species  of  animals.  There 
can  be  no  doubt  that  the  desire  for  acquisition  of  a  definite  territorial  area,  the 
determination  to  hold  it  by  fighting  if  necessary,  and  the  recognition  of  individual 
as  well  as  tribal  territorial  rights  by  others,  are  dominant  characteristics  in 
all  animals.  In  fact,  it  may  be  held  that  the  recognition  of  territorial  rights, 
one  of  the  most  significant  attributes  of  civilization,  was  not  evolved  by  man, 
but  has  ever  been  an  inherent  factor  in  the  life  history  of  all  animals." 

Undoubtedly  significant  is  the  fact  that  the  more  we  study  the  detailed  be- 
havior of  animals,  the  larger  is  the  list  of  kinds  knowoi  to  display  some  sort  of 
territoriality.  There  have  been  many  definitions  to  describe  the  territory  of 
different  animals  under  varying  circumstances.  The  best  and  simplest  of  these, 
in  my  mind,  is  by  Noble  (1939);  "territory  is  any  defended  area."  Noble's 
definition  may  be  modified  to  fit  any  special  case,  yet  it  is  all-inclusive  and  to 
the  point.  Territory  should  not  be  confused  with  "home  range" — an  entirely 
different  concept  that  will  be  treated  more  fully  later. 

The  territoriality  concept  is  not  a  new  one  (see  Nice,  1941).  It  has  been  only 
in  the  last  twenty  years,  however,  that  it  has  been  developed  and  brought 
to  the  front  as  an  important  biological  phenomenon  in  the  lower  animals. 
Howard's  book  "Territory  in  Bird  Life"  (1920)  stimulated  a  large  group  of 
W'Orkers,  chiefly  in  the  field  of  ornithology,  and  there  has  hardly  been  a  bird 
life-history  study  since  that  has  not  touched  on  this  phase  of  their  behavior. 


325 


BURT — TERRITORIALITY  AND  HOME  RANGE 


347 


In  the  field  of  mammals,  much  less  critical  work  has  been  done,  but  many  of  the 
older  naturalists  certainly  were  aware  of  this  behavior  pattern  even  though 
they  did  not  speak  of  it  in  modern  terms.  Hearne  (1795)  apparently  was 
thinking  of  property  rights  (territoriality)  when  he  wrote  about  the  beaver  as 


/                 V                               ^-^  /'             ^  1 

/  o              V                      /^"^  /     o        o  , 

/       -'""^^X            jC^^^         ®      ' 

/   y        \    x^^^^    o  ^ ; 

/           '        o        ^'       o        ^^^                      V 

o    'n         z;^^!      •  o^^              r 

^^^"1^'^     o     /^T^X^  j 

V    o  ^,=<^^^  v_^-^-:>^      XV 

\   T^^^^^dL^ 

.^^       -^  ^  ^^^■^^^^^^$^^$S^S^S^:^^$^^^^^^^ 

J, —       ^y          \\^o^$5oc^:SovN^?^^ 

(          ^              ^$$^^^^ 

\    {        o     ^^^ 

^^^^^^                ""^N       ^ 

XV                  ^         \ 

;$$^      /                              \ 

X      ^  M'    •     // 

X^^^^O  /\_ .     ^■~- '■'^       ^v 

'"~°^^^^     )  °      ""  ) 

O              f^^^^^^V^               \                  ^^/""^ 

•  O       i  ^"--— >^                     V-^ ' 

y               y 

HOME    RANGE    BOUNDARY     1^^:^^    NEUTRAL   AREA 

TERRITORIAL   BOUNDARY      •  NESTING    SITE 

BLANK— UNOCCUPIED   SPACE  O  REFUGE    SITE 

Fig.  1.  Theoretical  quadrat  with  six  occupants  of  the  same  species  and  sex,  showing 
territory  and  home  range  concepts  as  presented  in  text. 

follows:  "I  have  seen  a  large  beaver  house  built  in  a  small  island,  that  had  near 
a  dozen  houses  under  one  roof;  and,  two  or  three  of  these  only  excepted,  none 
of  them  had  any  communication  with  each  other  but  by  water.  As  there  were 
beavers  enough  to  inhabit  each  apartment,  it  is  more  than  probable  that  each 
famOy  knew  its  own,  and  always  entered  at  their  own  door  without  having  any 


326 


348  JOURNAL   OF   1VL\MMAL0GY 

further  connection  with  their  neighbors  than  a  friendly  intercourse"  (in  Morgan, 
1868,  pp.  308-309).  Morgan  (op.  cit.,  pp.  134-135),  also  writing  of  the  beaver, 
made  the  following  observation;  "a  beaver  family  consists  of  a  male  and  female, 
and  their  offspring  of  the  first  and  second  years,  or,  more  properly,  under  two 
years  old.  .  .  .  When  the  first  litter  attains  the  age  of  two  years,  and  in  the 
third  summer  after  their  birth,  they  are  sent  out  from  the  parent  lodge."  Mor- 
gan's observation  was  later  confirmed  by  Bradt  (1938).  The  works  of  Seton 
are  replete  wath  instances  in  the  lives  of  different  animals  that  indicate  territorial 
behavior.  In  the  introduction  to  his  "Lives"  Seton  (1909)  states  "In  the  idea 
of  a  home  region  is  the  germ  of  territorial  rights."  Heape  (1931)  devotes  an 
entire  chapter  to  "territory."  Although  he  uses  the  term  more  loosely  than 
I  propose  to,  (he  includes  home  ranges  of  individuals  and  feeding  ranges  of 
tribes  or  colonies  of  animals),  he  carries  through  his  work  the  idea  of  defense  of 
an  area  either  by  an  individual  or  a  group  of  individuals.  Not  only  this,  but 
he  draws  heavily  on  the  literature  in  various  fields  to  support  his  thesis.  Al- 
though the  evidence  set  forth  by  Seton,  Heape,  and  other  early  naturalists  is 
of  a  general  nature,  mostly  garnered  from  reports  by  others,  it  cannot  be  brushed 
aside  in  a  casual  manner.  The  old  time  naturalists  were  good  observers,  and, 
even  though  their  techniques  were  not  as  refined  as  those  of  present  day  biolo- 
gists, there  is  much  truth  in  what  they  wrote. 

A  few  fairly  recent  published  observations  on  specific  mammals  serve  to 
strengthen  many  of  the  general  statements  made  by  earlier  workers.  In  speak- 
ing of  the  red  squirrel  (Tamiasciurus),  Klugh  (1927,  p.  28)  writes;  "The  sense 
of  ownership  seems  to  be  well  developed.  Both  of  the  squirrels  which  have 
made  the  maple  in  my  garden  their  headquarters  apparently  regarded  this  tree 
as  their  private  property,  and  drove  away  other  squirrels  which  came  into  it. 
It  is  quite  likely  that  in  this  case  it  was  not  the  tree,  but  the  stores  that  were 
arranged  about  it,  which  they  were  defending."  Clarke  (1939)  made  similar 
observations  on  the  same  species.  In  raising  wild  mice  of  the  genus  Peromyscus 
in  the  laboratory,  Dice  (1929,  p.  124)  found  that  "when  mice  are  placed  together 
for  mating  or  to  conserve  cage  space  it  sometimes  happens  that  fighting  takes 
place,  especially  at  first,  and  sometimes  a  mouse  is  killed.  .  .  .  Nearly  always 
the  mouse  at  home  in  the  cage  will  attack  the  presumed  intruder."  Further 
on  he  states,  "However,  when  the  young  are  first  born,  the  male,  or  any  other 
female  in  the  same  cage,  is  driven  out  of  the  nest  by  the  mother,  who  fiercely 
protects  her  young."  Similarly,  Grange  (1932,  pp.  4-5)  noted  that  snowshoe 
hares  (Lepus  americanus)- in  captivity  "showed  a  definite  partiality  for  certain 
spots  and  corners  to  which  they  became  accustomed"  and  that  "the  female 
would  not  allow  the  male  in  her  territory  (cage)  during  late  pregnancy  and  the 
males  themselves  were  quarrelsome  during  the  breeding  season." 

Errington  (1939)  has  found  what  he  terms  "intraspecific  strife"  in  wild  musk- 
rats  (Ondatra).  Much  fighting  takes  place  when  marshes  become  overcrowded, 
especially  in  fall  and  winter  during  readjustment  of  populations.  "But  when 
invader  meets  resident  in  the  tunnel  system  of  one  of  [the]  last  lodges  to  be  used 
in  a  dry  marsh,  confhct  may  be  indeed  savage."     Gordon  (1936)  observed  def- 


327 


BURT TERRITORIALITY   AND   HOME   RANGE  349 

inite  territories  in  the  western  red   squirrels  (Tamiasciurus  fremonti  and    T. 
douglasii)  during  their  food  gathering  activities.     He  also  performed  a  neat 
experiment  with  marked  golden  mantled  squirrels  {Citellus  lateralis  chysodeirus) 
by  placing  an  abundance  of  food  at  the  home  of  a  female.     This  food  supply- 
attracted  others  of  the  same  species.     To  quote  Gordon:  "she  did  her  best  to 
drive  away  the  others.     Some  of  her  sallies  were  only  short,  but  others  were 
long  and  tortuous.     There  were  rather  definite  limits,  usually  not  more  than 
100  feet  from  the  pile,  beyond  which  she  would  not  extend  her  pursuit.     In 
spite  of  the  vigor  and  the  number  of  her  chases  (one  day  she  made  nearly  60 
in  about  6  hours)  she  never  succeeded  in  keeping  the  other  animals  away." 
This   individual   was  overpowered   by  numbers,   but,  nevertheless,   she  was 
using  all  her  strength  to  defend  her  own  log  pile.     To  my  knowledge,  this 
is  the  best  observation  to  have  been   published  on  territorial  behavior  in 
mammals.     I  have  observed  a  similar  situation  (Burt,  1940,  p.  45)  in  the  east- 
ern chipmunk  (Tamias).     An  old  female  was  watched  fairly  closely  during 
two  summers.     Having  marked  her,  I  was  certain  of  her  identity.     "Although 
other  chipmunks  often  invaded  her  territory,  she  invariably  drove  them  away 
[if  she  happened  to  be  present  at  the  time].     Her  protected  area  was  about 
fifty  yards  in  radius ;  beyond  this  fifty-yard  limit  around  her  nesting  site  she 
was  not  concerned.     Her  foraging  range  (i.e.,  home  range)  was  considerably 
greater  than  the  protected  area  (territory)  and  occasionally  extended    100  or 
more  yards  from  her  nest  site."     From  live  trapping  experiments,   plotting 
the  positions  of  capture  of  individuals  on  a  map  of  the  area  covered,  I  in- 
terpreted (op.  cit.,  p.  28)  the  results  to  mean  that  there  was  territorial  be- 
havior in  the  white-footed  mouse  (Peromyscus  leucopus),  a  nocturnal  form. 
When  the  ranges  of  the  various  individuals  were  plotted  on  a  map,  I  found 
that  "the  area  of  each  of  the  breeding  females  is  separate — that  although 
areas  sometimes  adjoin  one  another,  they  seldom  overlap."     Carpenter  (1942) 
writes  thus:  "The  organized  groups  of  every  type  of  monkey  or  ape  which  has 
been  adequately  observed  in  its  native  habitat,  have  been  found  to  possess 
territories  and  to  defend  these  ranges  from  all  other  groups  of  the  same  species." 
In  reporting  on  his  work  on  the  meadow  vole  {Microtus  pennsylvanicus) ,  Blair 
(1940,  pp.  154-155)  made  the  statement  "It  seems  evident  that  there  is  some 
factor  that  tends  to  make  the  females  occupy  ranges  that  are  in  part  exclusive ; 
....  Possibly  there  is  an  antagonism  between  the  females,  particularly  during 
the  breeding  season,  but  the  available  evidence  does  not  indicate  to  me  that 
they  have  definite  territories  which  they  defend  against  all  trespassers.     It 
seems  highly  probable  that  most  mammalian  females  attempt  to  drive  away 
intruders  from  the  close  vicinity  of  their  nests  containing  young,  hut  this  does 
not  constitute  territoriality  in  the  sense  that  the  term  has  been  used  by  Howard 
(1920),  Nice  (1937),  and  others  m  reference  to  the  breeding  territories  of  birds." 
(Ital.  mme.)     To  quote  Howard  (1920,  pp.  192-193):  "But  the  Guillemot  is 
generally  surrounded  by  other  Guillemots,  and  the  birds  are  often  so  densely 
packed  along  the  ledges  that  there  is  scarcely  standing  room,  so  it  seems,  for 
all  of  them.     Nevertheless  the  isolation  of  the  individual  is,  in  a  sense,  just  as 


328 


350  JOURNAL   OF   MAMMALOGY 

complete  as  that  of  the  individual  Bunting,  for  each  one  is  just  as  vigilant  in 
resisting  intrusion  upon  its  few  square  feet  as  the  Bunting  is  in  guarding  its 
many  square  yards,  so  that  the  evidence  seems  to  show  that  that  part  of  the 
inherited  nature  which  is  the  basis  of  the  territory  is  much  the  same  in  both 
species."  Blair,  in  a  later  paper  (1942,  p.  31),  writing  of  Peromyscus  manicu- 
latus  gracilis,  states:  "The  calculated  home  ranges  of  all  sex  and  age  classes 
broadly  overlapped  one  another.  Thus  there  was  no  occupation  of  exclusive 
home  ranges  by  breeding  females.  .  .  .  That  individual  woodland  deer-mice 
are  highly  tolerant  of  one  another  is  indicated  by  the  foregoing  discussion  of 
overlapping  home  ranges  of  all  sex  and  age  classes."  Reporting  on  an  extensive 
field  study  of  the  opossum,  Lay  (1942,  p.  149)  states  that  "The  ranges  of  indi- 
vidual opossums  overlapped  so  frequently  that  no  discernible  tendency  towards 
establishment  of  individual  territories  could  be  detected.  On  the  contrary, 
tracks  rarely  showed  that  two  or  more  opossums  traveled  together."  It  seems 
quite  evident  that  both  Blair  and  Lay  are  considering  the  home  range  as  syno- 
nymous with  the  territory  when  in  fact  they  are  two  quite  distinct  concepts. 
Further,  there  is  no  concrete  evidence  in  either  of  the  above  papers  for  or  against 
territoriality  in  the  species  they  studied.  It  is  to  be  expected  that  the  territory 
of  each  and  every  individual  will  be  trespassed  sooner  or  later  regardless  of  how 
vigilant  the  occupant  of  that  territory  might  be. 

It  is  not  intended  here  to  give  a  complete  list  of  works  on  territorial  behavior. 
The  bibliographies  in  the  works  cited  above  lead  to  a  great  mass  of  literature 
on  the  subject.  The  point  I  wish  to  emphasice  is  that  nearly  all  who  have 
critically  studied  the  behavior  of  w^ild  mammals  have  found  this  behavioristic 
trait  inherent  in  the  species  with  which  they  worked.  Also,  it  should  be  stressed, 
there  are  two  fundamental  types  of  territoriality  hi  mammals — one  concerns 
breeding  and  rearing  of  young,  the  other  food  and  shelter.  These  tw^o  may  be 
further  subdivided  to  fit  special  cases.  Mrs.  Nice  (1941)  gives  six  major  types 
of  territories  for  birds.  Our  knowledge  of  territoriality  in  mammals  is  yet  too 
limited,  it  seems  to  me,  to  build  an  elaborate  classification  of  types.  Some  day 
we  may  catch  up  with  the  ornithologists. 

HOME    RANGE 

The  home  range  concept  is,  in  my  opinion,  entirely  different  from,  although 
associated  with,  the  territoriality  concept.  The  two  terms  have  been  used  so 
loosely,  as  synonyms  in  many  instances,  that  I  propose  to  dwell  briefly  on  them 
here.  My  latest  Webster's  dictionary  (published  in  1938),  although  satisfac- 
tory in  most  respects,  does  not  list  "home  range,"  so  I  find  no  help  there.  Seton 
(1909)  used  the  term  extensively  in  his  "Lives"  where  he  explains  it  as  follows: 
"No  wild  animal  roams  at  random  over  the  country:  each  has  a  home  region, 
even  if  it  has  not  an  actual  home.  The  size  of  this  home  region  corresponds 
somewhat  with  the  size  of  the  animal.  Flesh-eaters  as  a  class  have  a  larger 
home  region  than  herb-eaters."  I  believe  Seton  was  thinking  of  the  adult 
animal  when  he  wrote  the  above.  We  know  that  young  adolescent  animals 
often  do  a  bit  of  wandering  in  search  of  a  home  region.  During  this  time  they 
do  not  have  a  home,  nor,  as  I  consider  it,  a  home  range.     It  is  only  after  they 


329 


BURT TERRITORIALITY  AND  HOME  RANGE  351 

establish  themselves,  normally  for  the  remainder  of  their  lives,  unless  disturbed,, 
that  one  can  rightfully  speak  of  the  home  range.  Even  then  I  would  restrict 
the  home  range  to  that  area  traversed  by  the  individual  in  its  normal  activities 
of  food  gathering,  mating,  and  caring  for  young.  Occasional  sallies  outside  the 
area,  perhaps  exploratory  in  nature,  should  not  be  considered  as  in  part  of  the 
home  range.  The  home  range  need  not  cover  the  same  area  during  the  life 
of  the  individual.  Often  animals  will  move  from  one  area  to  another,  thereby 
abandoning  the  old  home  range  and  setting  up  a  new  one.  Migratory  animals 
have  different  home  ranges  in  summer  and  winter — the  migratory  route  is  not 
considered  part  of  the  home  range  of  the  animal.  The  size  of  the  home  range 
may  vary  with  sex,  possibly  age,  and  season.  Population  density  also  may 
influence  the  size  of  the  home  range  and  cause  it  to  coincide  more  closely  with 
the  size  of  the  territory.  Home  ranges  of  different  individuals  may,  and  do, 
overlap.  This  area  of  overlap  is  neutral  range  and  does  not  constitute  part  of 
the  more  restricted  territory  of  animals  possessing  this  attribute.  Home  ranges 
are  rarely,  if  ever,  in  convenient  geometric  designs.  Many  home  ranges  prob- 
ably are  somewhat  ameboid  in  outline,  and  to  connect  the  outlying  points  gives 
a  false  impression  of  the  actual  area  covered.  Not  only  that,  it  may  indicate  a 
larger  range  than  really  exists.  A  calculated  home  range  based  on  trapping 
records,  therefore,  is  no  more  than  a  convenient  index  to  size.  Overlapping  of 
home  ranges,  based  on  these  calculated  areas,  thus  may  at  times  be  exaggerated. 
From  trapping  records  alone,  territory  may  be  indicated,  if  concentrations  of 
points  of  capture  segregate  out,  but  it  cannot  be  demonstrated  without  question. 
If  the  occupant  of  an  area  is  in  a  trap,  it  is  not  in  a  position  to  defend  that  area. 
It  is  only  by  direct  observation  that  one  can  be  absolutely  certain  of  terri- 
toriality. 

Home  range  then  is  the  area,  usually  around  a  home  site,  over  which  the 
animal  normally  travels  in  search  of  food.  Territory  is  the  protected  part  of 
the  home  range,  be  it  the  entire  home  range  or  only  the  nest.  Every  kind  of 
mammal  may  be  said  to  have  a  home  range,  stationary  or  shifting.  Only  those 
that  protect  some  part  of  the  home  range,  by  fighting  or  agressive  gestures,  from 
others  of  their  kind,  during  some  phase  of  their  lives,  may  be  said  to  have 
territories. 

SIGNIFICANCE    OF   BEHAVIORISTIC    STUDIES 

I  think  it  will  be  evident  that  more  critical  studies  in  the  behavior  of  wild  ani- 
mals are  needed.  We  are  now  spending  thousands  of  dollars  each  year  in  an 
attempt  to  manage  some  of  our  wild  creatures,  especially  game  species.  How 
can  we  manage  any  species  until  we  know  its  fundamental  behavior  pattern? 
What  good  is  there  in  releasing  a  thousand  animals  in  an  area  large  enough  to 
support  but  fifty?  Each  animal  must  have  so  much  living  room  in  addition  to 
other  essentials  of  life.  The  amount  of  living  room  may  vary  somewhat,  but 
for  a  given  species  it  probably  is  within  certain  definable  limits.  This  has  all 
been  said  before  by  eminent  students  of  wildlife,  but  many  of  us  learn  only  by 
repetition.     May  this  serve  to  drive  the  point  home  once  more. 


330 


352  JOURNAL   OF   MAMMALOGY 

LITERATURE  CITED 

Blair,  W.  F.  1940.  Home  ranges  and  populations  of  the  meadow  vole  in  southern  Michi- 
gan.    Jour.  Wildlife  Management,  vol.  4,  pp.  149-161,  1  fig. 

1942.  Size  of  home  range  and  notes  on  the  life  history  of  the  woodland  deer- 
mouse  and  eastern  chipmunk  in  northern  Michigan.  Jour.  Mamm.,  vol.  23, 
pp.  27-36,  1  fig. 

Bradt,  G.  W.     1938.     A  study  of  beaver  colonies  in  Michigan.    Jour.  Mamm.,  vol.  19, 

pp.  139-162. 
Burt,  W.  H.     1940.     Territorial  behavior  and  populations  of  some  small  mammals  in 

southern  Michigan.     Miscl.  Publ.  Mus.  Zool.  Univ.  Michigan,  no.  45,  pp.  1-58, 

2  pis.,  8  figs.,  2  maps. 
Carpenter,  C.  R.     1942.    Societies  of  monkeys  and  apes.     Biological  Symposia,  Lan- 
caster: The  Jaques  Cattell  Press,  vol.  8,  pp.  177-204. 
Clarke,  C.  H.  D.     1939.     Some  notes  on  hoarding  and  territorial  behavior  of  the  red 

squirrel  Sciurus  hudsonicus  (Erxleben).     Canadian  Field  Nat.,  vol.  53,  no.  3, 

pp.  42-43. 
Dice,  L.  R.     1929.     A  new  laboratory  cage  for  small  mammals,  with  notes  on  methods  of 

rearing  Peromyscus.     Jour.  Mamm.,  vol.  10,  pp.  116-124,  2  figs. 
Errington,  p.  L.     1939.     Reactions  of  muskrat  populations  to   drought.     Ecology,  vol. 

20,  pp.  168-186. 
Evans,  L.  T.     1938.     Cuban  field  studies  on  territoriality  of  the  lizard,  Anolis  sagrei. 

Jour.  Comp.  Psych.,  vol.  25,  pp.  97-125,  10  figs. 
Gordon,  K.     1936.     Territorial  behavior  and  social  dominance  among  Sciuridae.     Jour. 

Mamm.,  vol.  17,  pp.  171-172. 
Grange,  W.  B.     1932.     Observations  on  the  snowshoe  hare,  Lepus  americanus  phaeonotus 

Allen.     Jour.  Mamm.,  vol.  13,  pp.  1-19,  2  pis. 
Heape,  W.     1931.     Emigration,  migration  and  nomadism.     Cambridge:  W.  Heffer  and 

Son  Ltd.,  pp.  xii  +  369. 
Hearne,  S.     1795.     A  journey  from  Prince  of  Wale's  fort  in  Hudson's  Bay,  to  the  Northern 

Ocean.     London:  A.  Strahan  and  T.  Cadell,  pp.  xliv  +  458,  illustr. 
Howard,  H.E.     1920.     Territory  in  bird  life.     London:  John  Murray,  pp.  xii  +  308,  illustr. 
Klugh,  a.  B.     1927.     Ecology  of  the  red  squirrel.     Jour.  Mamm.,  vol.  8,  pp.  1-32,  5  pis. 
Lay,  D.  W.     1942.     Ecology  of  the  opossum  in  eastern  Texas.     Jour.  Mamm.,  vol.  23,  pp. 

147-159,  3  figs. 
Morgan,  L.  H.     1868.     The  American  beaver  and  his  works.     Philadelphia:  J.  B.  Lippin- 

cott  and  Co.,  pp.  xv  +  330,  illustr. 
Nice,  M.  M.     1941.     The  role  of  territory  in  bird  life.     Amer.  Midi.  Nat.,  vol.  26,  pp. 

441-487. 
Noble,  G.  K.     1939.    The  role  of  dominance  in  the  life  of  birds.     Auk,  vol.  56,  pp.  263-273. 
Seton,  E.  T.     1909.     Life-histories  of  northern  animals.     An  account  of  the  mammals  of 

Manitoba.     New  York  City:  Charles  Scribner's  Sons,  vol.  1,  pp.  xxx  +  673, 

illustr.,  vol.  2,  pp.  xii  +  677-1267,  illustr. 

1929.    Lives  of  game  animals,  Doubleday,  Doran  and  Co.,  Inc.,  4  vols.,  illustr. 

Museum  of  Zoology,  Ann  Arbor,  Michigan. 


331 


[Rejninted  from  SCIENCE,  N.  S.,  Vol.  V.,  No.  118, 
Pages  541-543,  April  2,  i597.] 


MIGRATION  OF  BATS  ON  CAPE  COD,  MASSA- 
CHUSETTS. 

Bat  migration  has  received  little  atten- 
tion. Various  writers  have  made  vague 
reference  to  the  fact  that  certain  bats  are 
found  in  winter  at  localities  where  they  are 
not  known  to  breed,  but  no  detailed  ac- 
count of  the  migratory  movements  of  any 
species  has  yet  been  published.  The  only 
special  paper  on  the  subject  that  I  have 
seen  is  by  Dr.  C.  Hart  Merriam,*  who 
clearly  establishes  the  fact  that  two  North 
American  bats  migrate.  The  data  on 
which  this  conclusion,  rests  are  as  follows  : 
The  hoary  bat,  one  of  the  migratory  species, 
is  not  known  to  breed  south  of  the  Cana- 
dian fauna.  In  the  Adirondack  region  it 
appears  about  the  middle  of  M'ay  and  dis- 
appears early  in  October.  During  the 
autumn  and  winter  it  has  been  taken  in  South 
Carolina  (Georgetown,  January  19th), 
Georgia  (Savannah,  February  6th),  and  on 
the  Bermudasf  ('  autumn  ').  As  the  writer 
remarks,  these  facts  may  be  fairly  regarded 
as  conclusive  evidence  of  migration.  The 
evidence  of  the  migratory  habits  of  the 
silver-haired  bat  rests  chiefly  on  the  ani- 
mal's periodical  appearance  in  spring  aud 
fall  at  the  lighthouse  on  Mount  Desert 
Rock,  thirty  miles  off  the  coast  of  Maine. 
This  species  has  also  been  observed  on  the 
Bermudas. 

In  August  and  September,  1890  ajid  1891, 
I  had  the  opportunity  to  watch  the  appear- 

*Trans.  Royal  Soc.  Canada  V  (1887),  Section  V,  p. 
85,  1888. 

1 1  may  add  that  I  have  a  bat  of  this  species,  killed 
at  Brownsville,  Texas,  on  October  22d. 


ance  aud  disappearance  of  three  species  of 
bats  at  a  locality  where  none  could  be  found 
during   the    breeding    season.      Highland 
Light,   the  place   where   my   observations 
were  made,  is  situated  near  the  edge  of  one 
of  the  highest  points  in  the  series  of  steep 
blufts   of  glacial    deposit   which    form   the 
outer  side  of  Cape  Cod,  Massachusetts.  The 
lidit,  which  is  less  than  ten  miles  from  the 
northern  extremity  of  the  cape,  is  separated 
from  the   mainland   toward  the   east   and 
northeast  by  from  twenty- five  to  fifty  miles 
of  water.     The   bluff  on  which  it   stands 
rises  abruptly  from  the  beach  to  a  height  of 
one  hundred  and   fifty   feet.     I  found  the 
bats  for  the  most  part  flying  along  the  face 
of  this  bluff,  where  they  fed  on  the  myriads 
of  insects   blown   there  by    the   prevailing 
southwest  winds.     They  chiefly  frequented 
the  middle  and  upper  heights  and  seldom 
flew  over  the  beach  at  the  foot  of  the  bluff 
or   over  the  level  ground  about  the  light- 
house.    I  do  not  know  where  the  animals 
spent  the   day,   as   careful   search   in  old 
buildings,  under   the  overhanging  edge  of 
the  bluff,    and   in   deserted   bank  swallow 
holes,  failed  to  reveal  their  hiding  places. 
It  is  possible  that  they  found  shelter  in  the 
dense,  stunted,  oak  scrub  with  which  the 
bluff  is  in  many  places  crowned,  but  of  this 
I  have  no  evidence.     I  hope  that  the  ob- 
servations given  below  may  again  call  the 
attention  of  field  naturalists   to   a  subject 
which  presents  many  difficult  and  interest- 
ing problems. 

Atalapha  noveboracensis*  (red  bat)  . 
Augtist  21,  1890.  The  first  bats  of  the  sea- 
son were   seen  this  evening.     There  were 

*With  bat  nomenclature  in  its  present  unsettled 
state  it  is  well  to  use  the  names    adopted   by    Dr. 


332 


only  two,  and  I  could  not  positively  identify 
them,  but  the}'^  were  probablj-  red  bats. 

August  25,  1890.  An  adult  male  taken. 

August  28,  1890.  Two  seen. 

August  29,  1890.  The  evening  was  too 
chilly  for  many  bats  to  be  on  the  wing.  A 
few  A.  noveboracends  seen  and  two  taken. 

Aiigust  SO,  1890.  Six  or  eight  A.  novehora- 
censis  seen  and  three  taken.  The  evening 
was  warm  and  bats  flew  much  more  freely 
than  on  the  29th. 

Aiigust  31,  1890.  A  chill}'  evening  again, 
and  onl}'  two  bats  seen ,  both  A.  noveboracen- 

September  2,  1800.  A  few  red  bats  seen 
and  two  taken. 

September  5,  1890.  I  was  not  at  Highland 
Light  this  evening,  but  Mr.  W.  M.  Small  re- 
ported a  heavy  flight  of  bats.  He  shot  five, 
all  A.  noveboracensis. 

September  8,  1890.  Heavy  fog,  so  that  no 
bats  could  be  seen,  if  any  were  moving  along 
the  face  of  the  bluff.  Three  or  four  red 
bats  flew  about  the  light  house  tower  dur- 
ing the  first  half  of  the  night,  feeding 
on  insects  attracted  by  the  light.  They 
flew  mostly  below  the  level  of  the  deck 
which  encircles  the  tower  about  six  feet  be- 
low the  lantern  and  never  approached  the 
light  itself. 

September  12,  1890.  A  single  red  bat  shot 
this  evening. 

After  this  date  I  watched  for  bats  on  sev- 
eral consecutive  evenings.  As  I  saw  no 
more  I  concluded  that  the  migration  had 
ended. 

August  25,  1891.  Fourteen  Atalapha  nove- 
boracensis, the  first  bats  of  the  season,  seen 

Harrison  Allen  in  his  latest  Monograph  of  the  Bats 
of  North  America  (1893),  although  many  of  these 
will  require  revision. 


this  evening.  They  were  flying  both  north 
and  south. 

Augiist  26,  1891.  Evening  very  foggy.  A 
red  bat  which  flew  about  the  lighthouse 
was  the  only  one  seen. 

August  27,  1891.  Half  a  dozen  red  bats 
seen  and  one  taken. 

August  28,  1891.  Four  red  bats  seen.  All 
flew  toward  the  south. 

August  SO,  1891.  A  red  bat  caught  in  a 
house  near  the  edge  of  the  bluff. 

September  2,  1891.  Eight  or  ten  seen  and 
three  taken.  The  movement  this  evening 
was  mostly,  though  not  wholly,  from  north 
to  south. 

September  S,  1891.  Six  seen  and  three 
tak^n. 

September  5,  1891.  Evening  cold  and 
misty.     No  bats  moving. 

September  7  and  8,  1891.  A  few  bats  seen 
each  evening,  but  none  taken.  All  ap- 
peared to  be  this  species. 

September  10,  1891.  One  red  bat  shot. 

September  11,  1891.  One  seen. 

September  12,  1891.  One  killed.  About  a 
dozen  bats  seen,  but  how  many  were  of  this 
species,  and  how  manj^  Lasionycteris  nodiva- 
gans  T  could  not  determine. 

September  IS,  1891.  About  a  dozen  bats 
seen.  Two  of  these  were  certainly  red 
bats. 

After  this  date  I  watched  for  bats  on  con- 
secutive evenings  for  more  than  a  week.  As 
I  saw  none  I  finally  gave  up  the  search. 

ATALAPHA    CINEREA    (HOARYBAT). 

August  26,  1890.  One  Atalapha  cinerea, 
the  only  bat  seen,  shot  this  evening. 

August  28,  1890.  Two  hoary  bats  taken, 
and  at  least  two,  and  probably  four,  others 
seen. 


333 


August  30,  1890.  Two  taken  and  two 
others  seen. 

September  2,  1890.  Only  two  seen.  Both 
taken. 

No  more  hoary  bats  seen  during  1890. 

Augttst  25, 1891.  A  single  Atalapha  cinerea 
seen  fljnng  south  along  the  face  of  the  bluff 
this  evening. 

September  2,  1891.  One  seen  flying  north. 

September  12,  1891.  An  adult  male  shot — 
the  last  of  the  season. 

At  Highland  Light  I  found  the  hoary  bat 
less  active  and  irregular  in  its  movements 
than  the  red  bat.  Its  large  and  compara- 
tively stead}^  flight  made  it  easier  to  shoot 
than  either  of  the  two  smaller  species  with 
which  it  was  associated.  It  began  to  fly 
immediately  after  sunset.  In  the  Adiron- 
dacks  Dr.  C.  Hart  Merriam  found  the  hoary 
bat  a  late  flyer,  and  an  exceeding  difficult 
animal  to  kill  on  account  of  its  swift,  ir- 
regular motions.*  It  is  possible  that  while 
on  Cape  Cod  the  animal  modifies  its  habits 
on  account  of  the  unusual  surroundings  in 
which  it  finds  itself.     The  fatigue  of  a  long 

*  Trans.  Linn.  Soc   New  York,  II,  p.  78-83.    1884. 


migration  might  also  have  an  appreciable 
effect  on  a  bat's  activity. 


lasionycteris  noctivagans  (silver-haired 

bat). 

September  1,  1890.  One  silver-haired  bat 
taken. 

September  2,  1890.  Four  taken  and  per- 
haps a  dozen  others  seen. 

The  silver-haired  bat  was  not  seen  again 
during  1890. 

September  10,  1891.  Three  shot  and  prob- 
ably half  a  dozen  others  seen.  They  were 
mostly  flying  north. 

September  11,  1891.  Two  shot  and  four  or 
five  more  seen. 

September  12,  1891.  About  a  dozen  bats 
seen.  Some  were  without  doubt  this  species, 
but  just  what  proportion  I  could  not  tell. 

While  September  12th  is'  the  latest  date 

at  which  I  have  seen  Lasionycteris  nodivagans 

at  Highland  Light,  I  have  a  specimen  killed 

there  by  Mr.  W.  M.  Small  on  October  28, 

1889. 

Gerrit  S.  Miller,  Jr. 


334 


ECOLOGICAL  DISTRIBUTION  OF  SIX  SPECIES  OF  SHREWS  AND 
COMPARISON  OF  SAMPLING   METHODS   IN  THE   CENTRAL 

ROCKY  MOUNTAINS 

Larry  N.  Brown 

Abstract. — The  ecological  distribution  of  six  species  of  shrews  was  studied 
using  sunken  cans  in  14  montane  and  intermontane  habitats  in  southern  Wyoming. 
The  vagrant  shrew  ( Sorex  vagrans )  and  masked  shrew  ( Sorex  cinereiis )  were  cos- 
mopolitan in  distribution.  Sorex  cinereus  was  slightly  more  abundant  in  moist  plant 
communities,  whereas  Sorex  vagrans  predominated  in  slightly  drier  communities. 
Merriam's  shrew  ( Sore.t  merriami)  occurred  only  in  arid  portions  of  the  plains  and 
foothills,  and  in  short-grass  prairie  was  the  only  shrew  taken.  The  water  shrew 
(Sorex  palustris)  occurred  only  along  or  near  cold  mountain  streams  and  ponds. 
The  dwarf  shrew  (Sorex  iwmis)  and  pigmy  shrew  (Microsorex  hotji)  occupied  re- 
stricted mountain  habitats.  The  dwarf  shrew  was  abundant  in  rocky  locations  in 
both  alpine  and  subalpine  plant  communities;  the  pigmy  shrew  was  taken  only  in 
peat-moss  bogs  in  the  spruce-fir  zone.  A  comparison  of  snap  traps  and  sunken 
cans  as  methods  of  collecting  shrews  revealed  that  snap  traps  failed  to  demonstrate 
the  presence  of  Sorex  nanus  and  Microsorex  hoyi  in  areas  where  they  were  abun- 
dant. Also,  densities  of  Sorex  vagrans  and  Sorex  cinereus  indicated  by  snap  traps 
were  considerably  below  those  indicated  by  sunken  cans. 

The  habitat  preferences  and  ecological  distribution  of  the  six  species  of 
shrews  found  in  the  Central  Rocky  Mountains  have  not  been  extensively  stud- 
ied. Only  scattered  references  to  the  ecological  distribution  of  shrews  in  the 
Rocky  Mountains  occur  in  the  literature  (Gary,  1911;  Warren,  1942;  Negas  and 
Findley,  1959;  and  Spencer  and  Pettus,  1966).  No  thorough  study  dealing  with 
Wyoming  shrews  has  been  reported. 

The  species  studied  were  the  masked  shrew  (Sorex  cinereus),  the  vagrant 
shrew  (Sorex  vagrans),  the  dwarf  shrew  (Sorex  nanus),  the  Merriam's  shrew 
(Sorex  merriami),  the  water  shrew  (Sorex  palustris),  and  the  pigmy  shrew 
(Microsorex  hoyi).  Information  was  collected  on  the  ecological  distribution 
of  these  species  in  southern  Wyoming  in  terms  of  type  of  plant  cover  and  prox- 
imity of  water.  Data  on  the  indicated  abundance  of  shrews  using  two  different 
trapping  methods  were  also  compiled. 

Materials  and  Methods 

The  Medicine  Bow  Mountains  and  Laramie  Basin  area  of  southern  Wyoming  have  a  wide 
range  of  plant  communities,  which  occur  at  altitudes  of  from  7000  to  12,000  ft.  The  eight 
montane  and  intermontane  plant  communities  selected  for  sampling  were  cottonwood-wil- 
low,  short-grass  prairie,  sagebrush,  mountain  mahogany,  aspen,  lodgepole  pine,  spruce-fir 
and  alpine  tundra.  Brief  descriptions  of  the  sampled  areas  in  Albany  County,  Wyoming, 
are  as  follows: 

1.  Cottonwood-willotc. — 7160  ft;  10  miles  SW  Laramie,  along  Big  Laramie  River.  Dom- 
inants: Populus  angustifolia,  Salix  sp.  Several  grasses  (Poa,  Agropijron,  Carex)  present  in 
understory. 

617 


335 


618  JOURNAL  OF  MAMMALOGY  Vol.  48,  No.  4 

2.  Short-firass  prairie. — 7180  ft;  V2  mile  E  Laramie.  Dominants:  Boiiteloiia  gracilis, 
Buchloe  dactijloides.    Numerous  forbs  {Eriogoniim,  Gaitra,  Phlox)  also  represented. 

3.  Sagebrush. — 7220  ft;  20  miles  N  Laramie.  Dominants:  Artemisia  Iridentata,  Purshia 
tridentaia.  Several  grasses  ( Poa,  Koeleria,  and  Agropijrorx )  abundant  in  open  spaces  be- 
tween shrubs. 

4.  Mountain  mahogany. — 7250  ft;  1  mile  E  Laramie.  Dominant:  Cercocarpus  montanus. 
Present:    Symphoricarpos,  Artemisia,  Amelanchier,  as  well  as  several  grasses  and  forbs. 

5.  Aspen. — 8205  ft;  %  mile  NW  Centennial.  Dominant:  Populus  tremuloides.  A  dense 
understory  of  grasses  (Poa,  Agropyron)  and  scattered  shrubs  {Acer,  Rosa,  and  Berberis). 

6.  Lodgepole  pine. — 9300  ft;  5  miles  VV  Centennial.  Dominant:  Pinus  contorta.  Under- 
story of  scattered  forbs  (Lupinus,  Antennaria,  etc.)  and  small  trees  (Abies,  Juniperus,  and 
Picea ) . 

7.  Spruce-fir. — 9630  ft;  7  miles  W  Centennial.  Dominants:  Picea  engelmanni,  Abies 
lasiocarpa.    Several  shrubs  (Ribes,  Rosa,  Vaccinium,  Berberis)  common  in  understory. 

8.  Alpine  tundra. — 10,470  ft;  5  miles  W  University  of  Wyoming  Science  Camp.  Domi- 
nants:   Artemisia  scopulorum,  Silene  acaulis,  Poa  alpina,  Trifolium  sp.,  Salix  sp. 

A  more  detailed  description  of  most  communities  in  the  Front  Range  of  the  Rocky  Moun- 
tains is  found  in  Marr  (1961). 

Moist  bogs  or  marshes  interrupted  the  uniformity  of  four  of  the  above  plant  communities, 
specifically  the  aspen,  lodgepole  pine,  spruce-fir,  and  alpine  tundra.  Therefore,  to  compare 
shrew  populations  in  adjacent  wet  and  dry  situations,  a  bog  or  marsh  near  each  original 
sampling  station  was  trapped  (sampling  sites  were  500-1000  ft  apart).  Brief  descriptions 
of  these  wet  plant  communities  are  as  follows: 

1.  Bog  in  alpine  tundra. — 10,460  ft;  5  miles  W  University  of  Wyoming  Summer  Science 
Camp.  Dominants:  sedges  (Carex  .sp.),  dwarfed  willows  (Salix  sp.)  around  small,  shallow 
pond. 

2.  Bog  in  spruce-fir. — 9620  ft;  7  miles  W  Centennial.  Dominants:  sedges  (Carex  sp.), 
horsetails  (Equisetum  sp.),  willows   (Salix  sp.),  sphagnum  moss   (Sphagnum  sp. ). 

3.  Bog  in  lodgepole  pine. — 9295  ft;  5  miles  W  Centennial.  Dominants:  willow  (Salix 
sp.),  alder  (Alnus  tenuifolia),  sedges  (Carex  sp. ).    Small  pond  of  open  water  at  edge  of  bog. 

4.  Bog  in  aspen. — 8200  ft;  %  mile  W  Centennial.  Dominants:  willow  (Salix  sp. ),  alder 
(Alnus  tenuifolia),  aspen  (Populus  tremuloides) ,  sedges  (Carex  sp.),  horsetails  (Equisetum 
sp.).    Two  beaver  ponds  adjacent  to  the  area. 

To  check  the  preference  of  certain  shrews  for  rocky  areas,  two  e.xtensive  rockslides  were 
sampled  at  different  elevations.  One  of  these  was  a  subalpine  rockslide  at  8480  ft  elevation 
(3  miles  NW  Centennial)  in  an  ecotone  area  of  lodgepole  pine,  aspen,  and  sagebrush.  The 
other  trapping  station  was  in  a  vast  alpine  rockslide  above  tree  line  at  10,600  ft  elevation. 
Thus,  14  locations  were  sampled. 

Shrews  were  trapped  in  pit-fall  traps  made  of  one-gallon  tin  cans.  These  were  buried  in 
the  ground  with  the  mouth  of  each  can  just  below  the  ground's  surface.  A  grid  with  an 
interval  of  30  ft  was  used  in  placing  these  traps.  Each  sampling  plot  consisted  of  25  cans 
arranged  in  five  rows  having  five  cans  each. 

In  areas  with  a  high  water  table,  it  was  necessary  to  punch  holes  in  the  bottom  or  sides 
of  each  can.  This  allowed  water  to  enter  the  can  to  equalize  pressure  and  prevent  the  can 
from  lieing  forced  up  out  of  the  ground.  To  catch  shrews  in  such  localities,  it  was  desirable 
that  the  top  of  the  water  table  ])e  at  least'  an  inch  or  so  below  ground  surface.  High  water 
tables  in  several  bogs  required  that  cans  be  placed  on  a  slight  elevation  or  hummock  nearest 
each  grid  intersect. 

The  sinking  of  cans  in  rockslides  was  accomplished  by  removing  rocks  by  hand  until  a 
pit  into  the  interior  of  the  slide  was  created.  Wedged  rocks  and  large  lioulders  usually 
limited  the  depth  of  each  excavation  to  three  to  five  feet.  Each  can  was  then  placed  at  the 
deepest  point  and  fist-sized  rocks  were  used  to  rebuild  the  sulistrate  almost  up  to  the  lip  of 


336 


November  1967     BROWN— ECOLOGICAL  DISTRIBUTION  OF  SHREWS 


619 


Fig.  1. — Diagrammatic  representation  of  placement  of  pitfall  traps  (gallon  cans)  in  study 
of  rockslide  habitats  in  mountain  locations. 

the  can.  Then  gravel  was  used  to  build  a  pavement  to  the  lip  of  the  can  (Fig.  1).  If  only 
larger,  fist-sized  rocks  were  placed  around  each  can,  sufficient  spaces  remained  adjacent  to 
the  mouth  to  constitute  a  barrier  for  access  by  the  shrews. 

Between  .30  May  and  .3  June  1966,  350  can  traps  were  set  out  at  the  14  locations.  Cans 
were  checked  on  alternate  days  for  slightly  more  than  3  months.  The  total  number  of  shrews 
by  .species  taken  per  habitat  was  determined  for  the  total  sampling  period. 

In  September  1966,  a  direct  comparison  of  two  methods  of  collecting  shrews  was  made 
involving  standard  mouse-sized  snap  traps  and  the  sunken  cans.  A  snap  trap  was  baited 
and  set  adjacent  to  each  can  in  the  sampling  grid  of  the  subalpine  rockslide  and  the  spruce- 
fir  bog.  Both  sets  of  traps  were  checked  once  daily  for  12  days.  The  bait  for  the  snap  traps 
consisted  of  a  mi.xture  of  peanut  butter,  bacon  grease,  rolled  oats,  and  chopped  raisins. 

Results  and  Discussion 

Following  the  placement  of  cans  in  various  plant  communities  no  shrews 
were  captured  in  any  plot  for  a  period  of  10  to  14  days.  After  this  period, 
shrews  appeared  in  the  cans  with  regularity  throughout  the  remainder  of  the 
summer;  this  suggested  that  all  shrews  avoided  the  areas  where  cans  were 
placed  until  they  became  accustomed  to  the  change. 

Table  1  summarizes  the  relative  abundance  of  five  species  of  shrews  at  the 
various  sampling  stations.  The  masked  shrew  (Sorex  cinereus)  and  vagrant 
shrew  (Sorex  va^rans)  were  the  most  cosmopolitan  in  distribution,  being  rep- 
resented in  all  the  habitats  sampled  except  short-grass  prairie.  These  species 
were  always  taken  together,  but  in  varying  densities  that  appeared  to  correlate 
with  moisture  conditions.  Sorex  cinereus  was  generally  more  abundant  than  S. 
va^rans  in  the  moist  bog  localities  regardless  of  altitude.    Sorex  va^ran.s  had 


337 


620 


JOURNAL  OF  MAMMALOGY 


Vol.  4H,  No.  4 


Tahle  L — Ecological  cllstrihuiion  and  relative  abundance  of  five  species  of  shrews  in  rela- 
tion to  varions  habitats  in  the  Medicine  Bow  Mountains  and  Laramie  Basin  of  Wyoming, 

summer  1966. 


Micro- 

Sorcx 

Sorcx 

Sorcx 

Sorcx 

sorex 

Total 

Habitat   and  ele\ 

ition 

cincrciis 

vagrans 

nanus 

mcrriami 

hoyi 

collected 

Cottoiiwood-willow 

(7160) 

2 

14 

0 

0 

0 

16 

Short-grass  prairie 

(7180) 

0 

0 

0 

3 

0 

3 

Sagel:)nish 

( 7220 ) 

4 

11 

0 

3 

0 

18 

Mountain  mahogany 

( 7250 ) 

2 

6 

0 

2 

0 

10 

Aspen 

( 8205 ) 

5 

16 

0 

0 

0 

21 

Bog  in  aspen 

( 8200 ) 

28 

12 

0 

0 

0 

40 

Snbalpine  rockshde 

(8480) 

11 

20 

25 

0 

0 

56 

Lodgepole  pine 

( 9300 ) 

6 

16 

0 

0 

0 

22 

Bog  in  lodgepole 

( 9295 ) 

29 

11 

0 

0 

0 

40 

Spruce-fir 

( 9630 ) 

8 

18 

0 

0 

0 

26 

Bog  in  spruce-fir 

( 9620 ) 

32 

15 

0 

0 

6 

53 

Alpine  tundra 

(10,470) 

4 

8 

2 

0 

0 

14 

Alpine  willow  bog 

(10,460) 

9 

5 

0 

0 

0 

14 

Alpine  rockslide 

(10,600) 

3 

9 

21 

0 

0 

33 

higher  population  densities  in  the  mesic  communities  that  were  paired  with 
the  bogs  (aspen,  lodgepole  pine,  spruce-fir,  and  alpine  tundra).  The  vagrant 
shrew  was  likewise  slightly  more  abundant  than  S.  cinereus  in  the  other  mesic 
situations  sampled  such  as  rockslides,  sagebrush,  mountain  mahogany,  and  cot- 
tonwood-willow  communities.  These  findings  are  in  disagreement  with  those 
of  Clothier  (1955),  who  reported  that  S.  vafirans  was  always  more  numerous 
in  Montana  than  S.  cinereus  regardless  of  habitat.  My  results  confirm  the  find- 
ings of  Getz  (1961)  that  S.  cinereus  is  abundant  in  moist  or  standing-water 
situations,  and  the  findings  of  Hoffmann  and  Taber  (1960)  that  S.  vagrans  is 
present  at  high  altitudes  as  well  as  low. 

The  dwarf  shrew,  which  is  generally  considered  by  mammalogists  to  be  rare, 
was  abundant  in  two  restricted  habitats  and  was  present  at  a  third.  It  was 
more  numerous  than  S.  vagrans  by  a  slight  margin  (25  S.  nanus  as  compared 
to  20  S.  vagrans)  in  the  subalpine  rockslide  and  was  by  far  the  predominant 
shrew  in  the  alpine  rockslide  (21  animals  out  of  33).  Sorcx  nanus  was  also  rep- 
resented in  the  alpine  tundra  plot  by  two  animals  taken  near  a  rock  outcrop. 
This  represents  an  altitudinal  range  extending  from  8480  to  10,600  ft  and  in- 
cluding several  types  of  montane  plant  communities.  Since  rockslides  extend 
continuously  from  10,600  to  12,000  ft  in  the  Medicine  Bow  Range,  there  is  little 
doubt  the  species  reaches  that  altitude  in  this  habitat.  All  dwarf  shrews  were 
captured  at  considerable  distances  from  water,  suggesting  they  may  be  some- 
what adapted  to  dry  situations. 

The  preference  of  S.  nanus  for  rocky  areas  in  the  mountains  was  first  sug- 
gested by  Hoffmann  and  Taber  (1960),  who  collected  several  in  polygonal  rock 
fields  on  the  Beartooth  Plateau.  They  have  been  recorded  in  a  variety  of  other 


338 


Novetnber  1967     BROWN— ECOLOCIICAL  DISTRIBUTION  OF  SHREWS  621 

montane  habitats  by  Schellbach  (1948),  Clothier  (1957),  and  Bradshaw  (1961). 
Spencer  and  Pettus  (1966)  reported  S.  nanus  was  abundant  in  an  open  clear- 
cut  area  of  spruce-fir  forest.  They  did  not  mention  the  presence  or  absence  of 
rocks. 

Sorcx  merriami  was  trapped  in  three  plant  communities  that  were  repre- 
sented only  at  lower  elevations  in  southern  Wyoming.  These  habitats  were 
short-grass  prairie,  sagebrush,  and  mountain  mahogany.  None  of  these  habi- 
tats occurred  higher  than  the  mountain  foothills  ( 7500  ft ) .  These  three  plots 
produced  onl\  eight  Merriam's  shrews  for  the  whole  summer,  indicating  that 
population  levels  in  the  areas  sampled  were  not  high.  In  the  short-grass  prairie 
plot,  S.  merriami  was  the  only  species  of  shrew  present;  in  the  low  foothills, 
where  sagebrush  and  mountain  mahogany  communities  were  sampled,  they 
were  present  in  low  numbers  with  S.  vagrans  and  S.  cinercus.  The  only  Mer- 
riam's shrew  previously  taken  in  southeastern  Wyoming  was  reported  by 
Mickey  and  Steele  (1947),  from  short-grass  prairie  near  Laramie.  In  W^ash- 
ington,  Johnson  and  Clanton  ( 1954 )  found  that  this  species  preferred  the  sage- 
brush-bunch grass  community,  where  individuals  were  taken  in  the  tunnels  of 
the  sagebrush  vole  (Laounis  curtatus).  Hoffmann  (1955)  likewise  collected 
S.  merriami  in  sagebrush  in  California.  One  of  the  few  records  of  occurrence 
of  the  species  in  mountain  mahogany  was  that  of  Hoffmeister  ( 1956 )  in  Owl 
Creek  Canyon  in  northeastern  Colorado,  about  40  miles  south  of  the  present 
study  area. 

In  southeastern  Wyoming,  S.  merriami  occurred  in  the  driest  habitats  and 
generally  at  lower  elevations  than  did  other  species.  Merriam's  shrew  was 
taken  with  Lagurus  curtatus  in  the  sagebrush  and  short-grass  prairie  area,  but 
this  vole  was  absent  from  the  mountain  mahogany  community. 

The  pigmy  shrew  (Microsorex  hoiji)  was  not  known  to  occur  in  Wyoming 
until  it  was  taken  in  1963  in  the  Medicine  Bow  Range  ( Brown,  1966 ) .  A  dis- 
junct population  occurs  in  southern  Wyoming  and  adjacent  northern  Colorado 
and  is  more  than  500  miles  south  of  the  nearest  locality  in  Montana  where  the 
species  has  been  reported  (Hall  and  Kelson,  1959).  In  the  course  of  the  pres- 
ent study,  pigmy  shrews  were  captured  at  one  sampling  station,  in  the  spruce- 
fir  bog  at  9620  ft  elevation.  Here  Microsorex  was  encountered  only  around  the 
periphery  of  the  bog  in  an  area  dominated  by  a  deep,  spongy  mat  of  sphagnum 
moss.  In  the  strip  of  sphagnum,  they  were  taken  in  equal  numbers  with  S. 
cinereiis  and  in  greater  numbers  than  S.  vagrans.  Spencer  and  Pettus  (1966), 
in  their  study  of  a  single  bog  area  west  of  Fort  Collins,  Colorado,  reported  that 
the  pigmy  shrew  was  most  abundant  in  the  transition  area  between  the  bog 
and  the  surrounding  spruce-fir  forest.   This  is  in  agreement  with  my  findings. 

The  habitat  preferences  of  Microsorex  in  the  other  parts  of  its  range  seem  to 
be  rather  broad,  including  heavy  woods,  clearings,  and  pastures  in  both  wet 
and  dry  situations  (Burt,  1957).  However,  Jackson  (1961)  and  Buchner  (1966) 
noted  that  in  Wisconsin  and  Canada  the  species  occasionally  is  found  in  cold 
sphagnum  or  tamarack  bogs.   In  the  MacDonald  Range  of  northwestern  Mon- 


339 


(y22  journal  of  MAMMALOGY  Vol.  48,  No.  4 

Taisle  2. — Comparison  of  trap])ii\<^  results  for  .shrews  ii.sinfi  .snap  traps  and  .sunken  cans  for 
12  days  at  two  location.s  in  the  Medicine  Bow  Mountains,  Wtjoniin^. 

Subalpine  rockslide  Spruce-fir  bog 


Species 

Snap  tr 

aps 

Sunken 

cans 

Snap  traps 

Sunken  cans 

Horex  vapran.s 

2 

4 

2 

3 

Sorex  cinereu.s 

1 

2 

4 

9 

Sorcx  nanus 

0 

6 

0 

0 

Microsorex  hoiji 

0 

0 

0 

2 

Totals 

3 

12 

6 

14 

tana,  Conaway  (personal  communication)  captured  Microsorex  in  dry  areas  of 
clearcut  forest  having  a  dense  ground  cover.  The  relict  population  located  in 
the  central  Rockies  may  have  a  broader  habitat  specificity  than  indicated  by 
the  present  study. 

The  water  shrew  {Sorcx  palustris)  is  too  large  to  be  retained  in  gallon  cans 
unless  there  is  some  water  present.  Water  shrews  were  taken  in  partially 
flooded  cans  in  habitats  ranging  from  the  alpine  willow  bog  at  10,470  ft  eleva- 
tion down  to  the  willow-alder  bog  in  the  aspen  community  at  8200  ft  elevation. 
The  species  was  never  trapped  at  a  distance  greater  than  100  ft  from  a  moun- 
tain stream  or  pond. 

The  total  samples  of  shrews  at  each  location  were  compared,  and  two  types 
of  habitats  were  found  to  support  especially  high  densities  of  shrews.  The  most 
productive  habitats  were  rockslide  areas  and  marshy  or  boggy  areas,  both  of 
which  have  high  invertebrate  populations  that  can  serve  as  a  readily  available 
food  supply.  The  least  productive  trapping  plot  for  shrews  was  located  in  short- 
grass  prairie.  This  may  have  been  due  to  the  scarcity  of  suitable  cover  or  to 
a  relative  scarcity  of  invertebrates. 

A  comparison  of  the  number  and  species  of  shrews  collected  utilizing  equal 
numbers  of  snap  traps  and  cans  is  presented  in  Table  2.  In  300  trap-nights  us- 
ing snap  traps,  three  shrews  of  two  species  were  collected  at  the  subalpine  rock 
slide.  The  sunken  cans  produced  four  times  as  many  shrews  during  the  same 
period  and  three  species  were  represented.  Six  S.  tmnus  were  taken  in  cans 
while  none  appeared  in  adjacent  snap  traps,  suggesting  that  the  species  readily 
avoids  traps  and  therefore  gives  the  appearance  of  being  rare. 

Twenty-five  sunken  cans  produced  slightly  more  than  twice  as  many  shrews 
( 14  animals)  than  did  25  snap  traps  (six  animals)  in  the  bog  in  the  spruce-fir 
community  during  the  12-day  period.  Again,  S.  vagrans  and  S.  cinereus  were 
taken  in  both  snap  traps  and  cans,  but  Microsorex  was  captured  only  in  cans. 
Even  for  the  two  "common"  species,  higher  numbers  were  recorded  for  the 
can  traps. 

These  and  other  trapping  results  indicate  that  S.  nanus,  S.  merriami,  and 
Microsorex  hoiji  are  seldom  captured  in  snap  traps  even  when  all  are  abun- 
dant. Sorex  vagrans,  S.  cinereus,  and  S.  palustris  were  readily  captured  in  snap 
traps,  but  data  provided  by  pitfall  traps  suggest  that  densities  calculated  for 


340 


Xoinnhcr   /.967     BHOWN— ECOI  .OCICAL   DISTRIBl'TION   OK  SUKEWS  62:3 

tlit'se  species  on  the  basis  ot  snap-trap  catches  ma\  l)e  consistently  too  low. 
MacLeod  and  Lethiecq  (1963)  presented  similar  data  when  comparing  these 
trapping  methods  for  S.  cinereus  in  Newfoundland. 

ACKNOWLEDCMENTS 

I  wisli  to  thank  tlie  following  students  who  helped  with  colleetiiiK  the  shrews:  James 
Bradley,  Robert  CiiKj-Mars,  Ronald  Lynde,  Paul  Lussow,  Mar\in  Maxell,  and  Richard  Mc- 
(luire. 

Literature  Cited 

Bradshaw,  C.  \.  R.      1961.     New  Arizona  localit\  for  the  dwarf  shrew.   J.  Manini.,  42:  96. 

Rhown.  L.  X.  1966.  First  record  of  the  pigmy  shrew  in  Wyoming  and  description  of  a 
new  subspecies  (Mammalia:  InsectiNora ).  Proc.  Biol.  Soc.  Washington,  79: 
49-51. 

BucKNEH,  C.  H.  1966.  Populations  and  ecological  relationship.s  of  shrews  in  tamarack 
Iiogs  of  southeastern  Manitoba.    J.  Mamm.,  47:    181-194. 

BiHi,  W.  11.  1957.  Mammals  of  the  Clreat  Lakes  Region.  Uni\.  Michigan  Press,  .Ann 
.Arbor,  \\  +  246  pp. 

Gary,  .M.      1911.     A  biological  surve\  of  Colorado.    \.  Amer.  P'auna,  33:    1-256. 

Clothieh,  R.  R.  1955.  Contribution  to  the  life  history  of  So/c.r  vagrans  in  Montana.  J. 
Mamm.,  36:   214-221. 

.      1957.     .\  second  dwarf  shrew  from  \ew  Mexico.    J.  Mamm.,  38:  256. 

C.ETZ,  L.  L.  1961.  Factors  influencing  the  local  distribution  of  shrews.  Amer.  Midland 
Nat.,  65:   67-88. 

Hall,  E.  R.,  and  K.  R.  Kelson.  1959.  The  mammals  of  North  America.  The  Ronald 
Press,  New  York,  1:  xxx  +  546  +  79. 

Hoffmann,  R.  S.      1955.     Merriam  shrew  in  California,    j.  Mamm.,  36:  561. 

Hoffmann,  R.  S.,  and  R.  D.  Taueh.  1960.  Notes  on  Suicx  in  the  Northern  RocIcn  Moun- 
tain alpine  zone.   J.  Mamm.,  41:  230-234. 

HoFFMEisTER,  D.  F.  1956.  A  record  of  ^orex  merriami  from  northeastern  Colorado.  J. 
Mamm.,  37:   276. 

Jackson,  H.  H.  T.  1961.  Mammals  of  Wisconsin.  Uni\-.  Wisconsin  Press,  Madison,  xii 
+  504  pp. 

Johnson,  M.  L.,  and  C.  W.  Clanton.  1954.  Natural  history  of  Sorex  merriami  in  Wash- 
ington State.    Murrelet,  35:   1—1. 

MacLeod,  C.  F.,  and  J.  L.  Lethiecq.  1963.  A  comparison  of  two  trapping  procedures 
for  Sorex  cinereus.    J.  Mamm.,  44:  277-278. 

NLahk,  J.  1961.  Ecosystems  of  the  east  slope  of  the  Front  Range  in  Colorado.  L'niv.  Colo- 
rado Stud.  Biol.,  8:   1-134. 

Mickey,  A.  B.,  and  C.  N.  Steele,  Jh.  1947.  A  record  of  Sorex  merriami  merriami  for 
.southeastern  Wyoming.   J.  Mamm.,  28:  293. 

Negus,  iX.  C,  and  J.  S.  Flndley.  1959.  Mammals  of  Jackson  Hole,  Wyoming.  J.  Mamm., 
40:   .371-381. 

ScHELLB.\CH,  L.,  HI.  1948.  A  record  of  the  shrew  Sorex  luiiius  for  Arizona.  J.  Mamm., 
29:   295. 

Spenceh,  A.  W.,  AND  D.  Pettus.  1966.  Habitat  preferences  of  fi\e  sympatric  species  of 
long-tailed  shrews.    Ecology,  47:   677-683. 

Warhen,  E.  R.  1942.  The  mammals  of  Colorado.  .  .  .  l'ni\ .  Oklahoma  Press,  x\  iii  + 
330  pp. 

Department  of  Zoology  and  Physiology,  University  of  Wyoming,  Laramie  {present  ad- 
dress: Department  of  Zoology,  University  of  Sonthern  Florida.  Tampa).  Accepted  1  Sep- 
tember 1967. 


341 


378 


Journal  of  Wildlife  Management,  Vol.  20,  No.  4,  October  1956 


CHANGES  IN  NORWAY  RAT  POPULATIONS  INDUCED 
BY  INTRODUCTION  OF  RATS 

David  E.  Davis  and  John  J.  Christian 

Division  of  Vertebrate  Ecology,  Johns  Hopkins  School  of  Hygiene  and  Pubhc  Health,  Baltimore  5;  Naval 

Medical  Research  Institute,  Bethesda,  Maryland 


The  introduction  of  aliens  into  an  existing 
population  of  mammals  may  be  followed 
by  unexpected  effects  that  relate  to  social 
structure  and  population  composition.  These 
effects  were  studied  by  introducing  alien 
rats  into  stationary  and  increasing  popula- 
tions of  rats  in  city  blocks.  This  work  is  part 
of  a  continuing  study  of  the  mechanisms  of 
change  in  vertebrate  populations  using  Nor- 
way rats  ( Rattus  norvegicus )  in  residential 
areas  in  Baltimore  as  experimental  animals 
(Davis,  1953).  These  rats  inhabit  back  yards, 
basements,  and  garages  and  feed  on  garbage. 
The  human  sanitary  conditions  in  general 
are  poor  and  remain  unchanged  for  months 
at  a  time,  so  that  the  food  supply  of  the  rats 
has  only  slight  seasonal  variations.  Other 
environmental  conditions  are  similarly  sub- 
ject to  little  change  for  many  months  at  a 
time.  The  constancy  of  these  factors  permits 


Methods  and  Procedures 

The  procedures  followed  to  study  the  ef- 
fects of  introducing  strange  rats  into  a  popu- 
lation consisted  of  taking  some  rats  from  a 
stationary  or  increasing  population  in  one 
block  and  introducing  them  into  a  compara- 
ble population  in  another  block  and  observ- 
ing the  resulting  changes  in  the  second  pop- 
ulation. The  status  (stationary  or  increasing) 
of  the  population  was  determined  by  esti- 
mates at  bimonthly  intervals  for  more  than 
a  year.  Blocks  that  appeared  to  be  either 
stationary  or  increasing  were  selected  in 
October  and  monthly  estimates  made.  From 
this  group  4  stationary  and  4  increasing  pop- 
ulations were  chosen.  To  get  a  base  line  for 
adrenal  weights,  six  rats  of  one  sex,  weighing 
over  200  grams  each,  were  removed  from 
each  block  during  the  first  experimental 
week  ( week  1 ) .  Alien  rats  were  then  intro- 


experiments  on  populations  in  a  relatively  duced  into  each  block  during  the  third  week, 

stable  environment.  Finally,  the  population  and  at  the  same  time  native  rats  were  re- 

of  rats  in  each  block  is  essentially  discrete  moved  from  the  increasing  populations.  The 

and  isolated,  as  rats  rarely  travel  from  one  details  of  these  removals  and  introductions 

block  to  another  ( see  Davis,  1953,  for  refer-  are  contained  in  tables  2  and  3.   Estimates 

ences).  were  made   during  the   sixth   and   eighth 

342 


' 


Changes  in  Rat  Populations — Davis  and  Christian 


379 


weeks,  each  followed  by  the  removal  of  a 
small  sample  of  rats  for  adrenal  weights. 
The  adrenal  weights  were  expressed  for  each 
sample  as  the  mean  per  cent  of  standard 
reference  values  (Christian  and  Davis,  1955). 
The  rats  to  be  introduced  into  a  population 
were  indi\'idually  marked  by  toe-clipping 
prior  to  introduction,  whereas  the  native  rats 
were  not  marked.  The  details  of  the  history 
of  each  population  were  complicated  by  the 
impossibility  of  introducing  exactly  the  same 
number  of  rats  into  each  block  on  exactly 
the  same  days,  and  the  numerical  popula- 
tion size  also  differed  in  each  block. 

A  discussion  of  the  likelihood  of  error  is 
desirable  when  it  is  claimed  that  two  popu- 
lations differ  in  number,  since  the  detection 
of  changes  is  fundamental  to  the  conclusions 
derived  from  these  introductions.  Some  as- 
pects of  the  census  method  were  discussed 
by  Brown,  et  al.  ( 1955 ) .  However,  the  basic 
problem  is  that,  even  witli  trapping,  the  true 
number  of  rats  in  a  block  is  not  known. 
Nevertheless,  a  check  on  the  validity  of  esti- 
mation can  be  made  by  comparing  estimates 
before  and  after  a  trapping  program.  Sup- 
pose that  an  estimate  of  Nj  rats  is  first  ob- 
tained, subsequently  T  rats  are  removed 
and  a  second  estimate  of  No  rats  is  made. 
Obviously  N^  should  equal  T  +  No.  A 
figure  for  percentage  of  error  can  be  given  as 
Ni-(T  +  N,). 


Table  1.  - 

-  Distribution 

OF  Differences  Among 

Estimates 

r" 

Blocks 

Per  cent  Erro 

Positive 

Negative 

Total 

0-9 

13 

6 

19 

10-19 

6 

11 

17 

20-29 

4 

4 

8 

30-39 

2 

3 

5 

40-49 

1 

0 

1 

Totals 

26 

24 

50 

»  Ni  - 

(T  + 

No) 

N, 


For  example,  if  the  estimate 


for  a  block  is  151  rats  and  then  81  are  re- 
moved by  trapping  and  an  estimate  of  63 

is  made,  then ^ti —  4.6  per 

cent.  Other  procedures  could  be  used  such  as 

^-(^j-N')  or  N-  -^y_-/-  The  first 

procedure  is  preferred  because  it  bases  the 
calculations  on  N^,  which  is  the  estimate  that 
was  used  to  determine  the  status  of  the 
block.  A  total  of  50  populations  was  avail- 
able to  determine  the  extent  of  error.  Each 
had  been  trapped  during  the  past  6  years, 
and  an  estimate  had  been  made  before  trap- 
ping and  another  within  a  month  after  ces- 
sation of  trapping.  Naturally,  some  changes 
can  occur  during  the  intervening  month,  but 
for  practical  reasons  it  is  usually  not  possible 
to  make  an  estimate  promptly  after  the  ces- 
sation of  trapping.  These  blocks  contained 
3,707  rats  by  the  estimates  (NJ  and  1,502 
were  trapped.  The  number  of  rats  per  block 


Ni 


varied  from  15  to  182.  The  distribution  of 
errors  is  given  in  Table  1.  The  percentage 
of  error  was  independent  of  the  number  of 
rats  in  the  population.  From  these  differ- 
ences the  standard  error  of  the  difference 
can  be  calculated  to  be  10.7  per  cent.  This 
value  can  be  used  as  an  indication  of  the 
errors  to  be  expected  in  estimates  of  popula- 
tion changes  in  blocks.  For  example,  from 
Table  2  it  is  seen  that  the  estimate  (block 
150128)  before  introduction  was  116  and 
after  was  89.  The  percentage  difference  is 
23.3  which  when  divided  by  10.7  gives  a 
ratio  of  2.2.  This  difference  appears  to  be 
statistically  significant. 

Results  and  Discussion 

The  histories  of  the  populations  are  given 
by  blocks  in  tables  2  and  3  and  figures  1,  2, 
and  3.  The  terms  "replacement"  and  "sup- 
plement" require  clarification  for  this  dis- 
cussion. We  mean  by  replacement  that  ap- 
proximately the  same  number  of  rats  was 
introduced  as  was  removed.  Supplement 
means  that  many  more  alien  rats  were  intro- 
duced than  were  removed.  A  quantitative 
percentage  might  have  been  used  to  dis- 
tinguish these  two  terms,  but  it  would  have 
been  rather  meaningless  because  ( 1 )  the 
size  of  the  individual  rats  varies  consider- 
ably, and  (2)  immediate  mortality  is  prob- 
ably high.  Therefore,  we  really  do  not  know 
the  actual  number  of  rats  that  produced  the 
results.  Another  factor  is  that  births  and 
deaths  are  normally  high  in  any  population 
of  rats.  The  average  monthly  death  rate  is 
about  20  per  cent  for  stationary  rat  popula- 
tions; therefore,  their  birth  rate  is  also  about 
20  per  cent.  Comparable  mortality  and  birth 
rates  for  increasing  populations  are  prob- 


343 


380  Journal  of  Wildlife  Management,  Vol.  20,  No.  4,  October  1956 

Table  2.  —  Results  of  Introduction  of  Rats  into  Stationary  Populations 


Block  number 

Zero  week  is 

140338 
Dec.    16 

140344 
Dec.   16 

140118 
Feb.   9 

150128 
Feb.  9 

Week 

Rats 

w 

R 

w 

R 

w 

R 

Population 

-20 

62 

-20 

30 

-19 

105 

-18 

122 

Population 

-13 

42 

-13 

32 

-11 

98 

-10 

118 

Population 

-  5 

40 

-  5 

38 

-  6 

87 

-  6 

120 

Population 

0 

49 

0 

35 

0 

100 

0 

116 

Rats  removed 

1 

6M 

1 

6F 

1 

6F 

1 

6M 

Rats  introduced 

3 

lOM 

3 

8F 

2-6 

23F 

2-6 

27M 

Rats  removed 

— 

— 

— 

— 

— 

— 

— 

— 

Population 

6 

45 

6 

44 

6 

76 

7 

89 

Rats  removed 

6 

6M 

6 

6F 

6 

6F 

7 

6M 

Population 

8 

56 

8 

23 

11 

63 

10 

86 

Rats  removed 

8 

22 

8 

12 

11 

27 

10 

36 

Week 

Indexi 

w 

I 

w 

1 

w 

1 

1 

83.0 

1 

91.8 

1 

93.4 

1 

79.2 

Adrenal  size 

6 

84.1 

6 

85.3 

6 

90.4 

7 

71.4 

8 

88.0 

8 

102.4 

11 

68.4 

10 

73.6 

1  Mean  of  the  individual 

per  cent  of  appropriate  reference  value  for  the  sex 

and  size 

of  the  rat. 

ablv  about  15  per  c 

ent  and  25 

per  cent  ] 

Der 

STATIONARY 

month  respectively.  It  is  unwise,  under  these 
circumstances,  to  attempt  a  precise  measure- 
ment of  numerical  differences  in  the  num- 
bers of  rats  used. 

The  population  estimates  (Table  2)  in 
the  two  replacement  blocks  6  weeks  after 
the  introduction  of  rats  showed  ( Fig.  1 )  that 
block  140338  was  not  significantly  different 
from  the  previous  estimate,  while  block 
140344  had  apparently  increased  ( P  is  about 
.04).  While  the  apparent  difference  in  re- 
sults in  these  2  blocks  might  be  due  to  sex 
( the  females  less  disturbing )  or  to  numbers 
(fewer  introduced  into  140344),  no  inter- 
pretation will  be  attempted  for  the  reasons 
cited  above.  The  two  supplemented  blocks 
declined  significantly  (P  is  about  .04  for 
each)  (Fig.  1). 

We  recognize  that  the  replacement  pair  of 
populations  was  done  in  December  1953, 
and  the  supplemented  pair  in  February  1954, 
and  that  differences  might  be  due  to  some 
seasonal  aspect.  However,  the  only  known 
seasonal  change,  an  increase  in  breeding 
from  December  to  February,  would  produce 
the  opposite  result. 

Population  growth  ceased  in  all  four  in- 
creasing populations  following  the  replace- 
ment of  native  with  alien  rats  (figs.  2,  3,). 
In  no  block  was  the  difference  statistically 
significant.  It  apparently  made  no  differ- 
ence whether  the  sex  of  the  introduced  rats 


Fig.  1.  The  changes  in  four  stationary  populations 
for  20  weeks  before  introduction  of  rats  ( at  0  time ) 
and  about  10  weeks  after.  The  number  added  is 
indicated  by  a  plus  sign,  the  number  removed  by 
a  minus  sign. 


344 


Changes  in  Rat  Populations — Davis  and  Christian 
Table  3.  —  Results  of  Introduction  of  Rats  into  Increasing  Populations 


381 


1            Block  number 

140111 

140134 

140201 

140222 

Zero  week  is 

.  .                 Dec 

16 

Dec 

.  16 

Feb 

9 

Feb 

9 

Week 

Rats 

W 

R 

W 

R 

w 

R 

Population 

-20 

110 

-20 

80 

-25 

86 

-20 

57 

Population 

-13 

118 

-13 

88 

-16 

100 

-14 

62 

Population 

-  5 

133 

-  4 

115 

-  8 

105 

-  5 

95 

Population 

0 

150 

0 

140 

0 

135 

0 

90 

Rats  removed 

1 

6F 

1 

6F 

1 

6M 

1 

6M 

Rats  introduced 

3 

22F 

3 

28F 

3 

18M 

3 

20M 

Rats  removed 

3 

28F 

3 

22F 

3 

20M 

3 

ISM 

Population 

6 

167 

6 

130 

6 

130 

6 

85 

Rats  removed 

7 

6F 

7 

6F 

7 

6M 

7 

6M 

Population 

10 

152 

10 

130 

10 

130 

10 

70 

Rats  removed 

10 

48 

10 

73 

10 

57 

10 

24 

Week 

Indexi 

W 

I 

w 

I 

w 

I 

1 

92.1 

1 

91.5 

1 

104.4 

1 

93.8 

Adrenal  size 

7 

93.8 

102.8 

7 

85.3 

7 

99.1 

10 

101.5 

10 

90.4 

10 

91.1 

10 

84.6 

1  Mean  of  the  individual  per  cent  of  appropriate  reference  value  for  the  sex  and  size  of  the  rat. 


was  male  or  female.  The  population  from 
block  140222  (Fig.  2)  may  have  become 
stationary  just  prior  to  the  introduction  of 
aliens,  but  the  high  rate  of  reproduction  ( 4/6 
mature  females  were  pregnant)  suggests  that 
the  population  was  increasing.  The  popula- 
tion in  block  140111  increased  numerically 
after  the  introduction,  but  the  difference  be- 
tween the  two  estimates  is  within  the  error 
of  estimate  and  does  not  indicate  a  change 
in  population.  It  appears  that  introducing  a 
number  of  alien  rats  may  halt  the  growth  of 
increasing  populations. 

The  reader  may  have  noticed  that  the  total 
number  of  rats  removed  from  the  four  in- 
creasing blocks  was  about  5  per  cent  greater 
than  the  number  introduced,  so  that  the  rats 
in  these  populations  were  not  replaced  in  the 
strict  arithmetic  sense  of  the  word.  However, 
considering  the  previously  mentioned  birth 
and  mortality  factors,  it  is  not  desirable  to 
be  more  precise.  All  aspects  considered,  it 
is  likely  that  the  four  increasing  populations 
were  somewhat  reduced  following  replace- 
ment procedures.  The  four  blocks  (taken 
together)  increased  by  173  rats  in  the  20 
weeks  preceding  replacement,  so  that  they 
might  have  been  expected  to  have  had  600 
rats  10  weeks  after  replacement  instead  of 
the  observed  482,  although  the  rate  of  in- 
crease would  decline  as  the  population  in- 
creased. 

On  several  occasions  episodes  have  been 
noted  that  appear  to  be  explainable  on  the 


Q. 
O 
Q. 


< 

tr. 


150 


125 


100- 


75 


50 


25 


0 


MALES 


_L 


-30 


•20 


-t — • 


-10 
WEEKS 


10 


Fig.  2.  The  changes  in  two  increasing  blocks  before 

and  after  the  introduction  of  males  (symbols  as  in 

Fig.  1.) 

basis  of  introduction  or  actual  immigration. 
In  January  1946,  about  60  rats  were  released 
in  a  block  in  one  night  as  part  of  an  experi- 


345 


382 


Journal  of  Wildlife  Management,  Vol.  20,  No.  4,  October  1956 


I75r 


150 


125 


100 

z 
o 

!5 

^75 

Q. 

o 

Ql 


< 

DC 


50 


25 


-6 


+22 

-28  /  \ 
/        \ 

/  \ 


+  28 
22 


FEMALES 


^x ^X 


-30 


-20 


-10 
WEEKS 


10 


Fig.  3.  The  changes  in  two  increasing  blocks  before 

and  after  the  introduction  of  females  ( symbols  as  in 

Fig.  1.) 

ment  on  "homing"  ability  in  rats.  The  block 
originally  contained  about  100  rats  but  with- 
in 3  weeks  there  were  so  few  rats  left  in  the 
block  that  the  project  was  stopped.  Calhoun 
( 1948 )  noticed  the  same  result  when  he  in- 
troduced rats  into  blocks.  These  episodes, 
as  well  as  miscellaneous  observations,  stim- 
ulated a  test  in  1947  of  the  idea  that  the  in- 
troduction of  rats  into  a  population  would 
result  in  its  decline.  Accordingly,  rats  were 
introduced  over  a  period  of  4  months  into 
two  populations  that  had  just  reached  a  level 
judged  to  be  stationary  (Davis,  1949).  The 
introduction  of  90  rats  in  one  block  and  101 
in  the  other  was  accompanied  by  declines  of 
about  25  per  cent  and  of  40  per  cent  respec- 
tively. The  populations  increased  after  the 
introductions  ended. 

The  present  experiments  suggest  that  the 
introduction  of  large  numbers  of  rats  into 
a  population  disrupts  the  population  mech- 


anisms in  some  way  that  causes  the  popula- 
tions either  to  decline  in  numbers  or  stop 
growing. 

The  decrease  is  due  in  part  to  a  decline  in 
reproduction.  Data  are  not  available  for  the 
period  immediately  after  introduction,  as  it  is 
not  feasible  to  follow  the  population  changes 
and  simultaneously  to  collect  a  number  of 
rats  for  reproductive  data.  However,  the 
large  sample  of  rats  collected  from  the  blocks 
8  to  11  weeks  after  introduction  had  a  high 
reproductive  rate  ( Table  4 )  and  a  low  lacta- 
tion rate.  One  would  conclude  from  these 
data  that  the  number  of  pregnancies  was 
low  immediately  after  the  introduction.  Only 
about  25  per  cent  of  the  females  were  lacta- 
ting  at  10  weeks,  whereas  normally  about 
40  per  cent  of  the  females  of  these  rats  are 
lactating  (Davis,  1953).  The  high  preva- 
lence of  pregnancy  presumably  resulted 
from  their  more  or  less  simultaneous  re- 
covery from  the  effects  of  introduction.  The 
decreases  in  rat  populations  obviously  may 
have  been  due  largely  to  mortality  and  move- 
ment, but  data  on  this  aspect  are  impossible 
to  obtain  under  these  conditions. 

Table  4.  —  Reproductive  Records  of  Local  Rats 
Captured  8-11   Weeks  after  Artificial  Immi- 
gration of  Rats  into  Blocks 


Number  Mean 

Population  Mature       Per  cent  Number  Per  cent 

status  Females      Pregnant         Embryos        Lactating 


Increasing 
Stationary 


85 
66 


33.0 

31.8 


10.38 
9.63 


20.0 
28.8 


Previous  experiments  have  shown  that  the 
weight  of  the  adrenal  glands  in  rats  responds 
to  changes  in  population.  An  increase  in 
adrenal  weight  parallels  increases  in  popu- 
lation; the  artificial  reduction  of  a  popula- 
tion also  results  in  a  decrease  in  adrenal 
weight  (Christian,  1954;  Christian  and  Davis, 
1955).  The  adrenal  responses  of  the  two 
sexes  are  parallel  ( ibid. ) .  Experiments  have 
indicated  that  changes  in  adrenal  weight  in 
response  to  changes  in  population  result 
primarily  from  changes  in  cortical  mass 
( Christian,  1955a,  1955b,  1956 ) .  To  examine 
these  problems,  the  adrenals  of  the  rats  from 
each  block  were  removed  and  weighed.  The 
observed  adrenal  weight  for  each  rat  was 
compared  with  a  standard  reference  weight 
for  the  appropriate  sex  and  size  (length  of 
head  and  body )  of  rat  ( Christian  and  Davis, 


346 


Changes  in  Rat  Populations — Davis  and  Christian 


383 


1955),  and  expressed  as  a  per  cent  of  the 
reference  value.  These  percentages  for  the 
rats  from  each  sample  were  averaged  and 
the  means  are  recorded  at  the  bottom  of 
tables  2  and  3.  We  have  used  the  mean  value 
of  a  given  sample  as  the  unit  of  measurement 
for  comparing  adrenal  weight  with  popula- 
tion size  (Christian,  1954;  Christian  and 
Davis,  1955). 

The  results  indicate  that,  in  the  replace- 
ment stationary  blocks  (140338  and  140344), 
there  was  a  small  increase  in  adrenal  weight 
after  8  weeks,  while  the  populations  appar- 
ently remained  practically  unchanged  (ta- 
bles 2  and  3,  Fig.  1 ) . 

A  mean  decline  in  population  size,  par- 
alleled by  a  decrease  in  adrenal  weight  in 
at  least  one  of  the  two  blocks,  followed  the 
addition  of  a  large  number  of  alien  rats  to 
stationary  populations  (blocks  140118  and 
150128 ) .  The  adrenal  weights  probably  re- 
flect largely  the  final  results  of  population 
manipulation  rather  than  the  immediate  ef- 
fects, as  the  adrenal  samples  were  obtained 
several  weeks  after  the  introductions  or  esti- 
mates. Therefore,  the  changes  in  adrenal 
weight  probably  reflect  overall  population 
changes  rather  than  any  immediate  social 
strife  resulting  from  the  introductions.  An 
experiment  to  collect  samples  a  few  days 
after  the  introductions  is  in  progress  and 
may  show  an  increase  in  adrenal  weight. 

The  adrenal  glands  of  rats  from  the  in- 
creasing blocks  showed  no  consistent  change, 
although  population  growth  terminated  ( Ta- 
ble 3,  figures  2  and  3 ) .  The  replacement  of 
rats  in  increasing  populations  had  little  ef- 
fect on  the  adrenal  weights  of  rats  examined 
10  weeks  later. 

The  results  reported  here  may  be  applica- 
ble to  certain  stocking  programs.  A  routine 
part  of  many  game-management  programs 
has  been  the  introduction  of  a  number  of 
animals  into  an  area  with  the  expressed  hope 
of  increasing  the  population  either  directly 
or  eventually  by  reproduction.  Indeed,  such 
stocking  has  often  been  considered  a  pana- 
cea for  all  hunting  problems.  The  present 
results,  using  rats  as  experimental  animals, 
show  that  the  disruption  of  a  population 
following  an  introduction  may  actually  pro- 
duce a  decline  under  certain  conditions.  Evi- 
dently the  introduction  of  a  number  of  ani- 
mals may  have  disastrous  results  when  a 
population  is  above  the  halfway  point  on  a 
growth  curve. 


Summary 

Wild  Norway  rats  {Rattus  norvegicus) 
were  introduced  from  one  city  block  to  an- 
other to  simulate  immigration.  The  pop- 
ulation changes  were  determined  by  fre- 
quent estimates  for  about  20  weeks  before 
introduction  and  8  to  11  weeks  thereafter. 
From  two  blocks  with  stationary  rat  popula- 
tions, some  rats  were  removed  and  then 
replaced  by  aliens.  The  populations  re- 
mained stationary.  In  two  blocks  about  four 
times  as  many  rats  were  introduced  as  were 
removed.  The  populations  declined  about 
25  per  cent.  In  four  blocks  with  increasing 
populations  about  one-fourth  of  each  pop- 
ulation was  removed  and  replaced  by  alien 
rats  from  other  blocks.  The  increase  halted. 

The  reproductive  rate  8  to  11  weeks  after 
the  introduction  was  normal  for  an  increas- 
ing population,  but  the  lactation  rate  was 
low,  indicating  that  the  decline  in  popula- 
tion growth  was  due  in  part  to  a  decreased 
reproductive  rate,  and  that  the  population 
was  back  to  normal  pregnancy  rate  in  two 
months.  The  adrenal  weights  were  also  es- 
sentially normal  for  the  population  level 
two  months  after  introduction. 

References 

Brown,  R.  Z.,  W.  Sallow,  David  E.  Davis,  and 
W.  G.  Cochran.  1955.  The  rat  population  of 
Baltimore  1952.  Amer.  J.  Hyg.,  61(  1 ) :  89-102. 

Calhoun,  J.  B.  1948.  Mortality  and  movement  of 
brown  rats  {Rattus  norvegicus)  in  artificially 
super-saturated  populations.  J.  Wildl.  Mgmt., 
12(2):167-172. 

Christl^n,  J.  J.  1954.  The  relation  of  adrenal  size 
to  population  numbers  of  house  mice.  Sc.  D. 
dissertation,  Johns  Hopkins  Univ.,  Baltimore. 

.  1955a.  Effect  of  population  size  on  the  adre- 
nal glands  and  reproduction  organs  of  male 
mice  in  populations  of  fixed  size.  Amer.  J. 
Physiol.,  182(2):292-300. 

.     1955b.     Effect   of   population   size   on   the 

weights  of  the  reproductive  organs  of  white 
mice.  Amer.  J.  Physiol.,  181(3)  :477-480. 

.   1956.   Adrenal  and  reproductive  responses  to 

population  size  in  mice  from  freely  growing 
populations.    Ecology,  37(2):258-273. 

AND  D.  E.  Davis,  1955.   Reduction  of  adrenal 

weight  in  rodents  by  reducing  population  size. 
Trans.  N.  Amer.  Wildl.  Conf.,  20:177-189. 

Davis,  D.  E.  1949.  The  role  of  intraspecific  compe- 
tition in  game  management.  Trans.  N.  Amer. 
Wildl.  Conf.,  14:225-231. 

.    1953.   The  characteristics  of  rat  populations. 

Quart.  Rev.  Biol,  28(4):373-401. 

Received  for  publication  October  24,  1955. 


347 


A  TRAFFIC  SURVEY  OF  MICROTUS-REITHRODONTOMYS  RUNWAYS 

By  Oliver  P.  Pearson 

Patient  observation  of  the  comings  and  goings  of  individual  birds  has  long 
been  one  of  the  most  rewarding  activities  of  ornithologists.  The  development 
in  recent  years  of  inexpensive  electronic  flash  photographic  equipment  has 
made  it  possible  and  practical  for  mammalogists  to  make  similar  studies 
on  this  aspect  of  the  natural  history  of  secretive  small  mammals.  The  report 
that  follows  is  based  on  photographic  recordings  of  the  vertebrate  traffic  in 
mouse  runways  over  a  period  of  19  months.  Species,  direction  of  travel,  time, 
temperature  and  relative  humidity  were  recorded  for  each  passage.  In  addi- 
tion, many  animals  in  the  area  were  live-trapped  and  marked  to  make  it  possible 
to  recognize  individuals  using  the  runways. 

THE  APPARATUS 

Two  recorders  were  used.  Each  consisted  of  an  instrument  shelter  and  a 
camera  shelter.  Each  instrument  shelter  was  a  glass-fronted,  white  box  con- 
taining an  electric  clock  with  a  sweep  second  hand,  a  ruler  for  measuring  the 
size  of  photographed  individuals,  a  dial  thermometer  and  a  Serdex  membrane 
hygrometer.  The  ends  of  the  box  were  louvered  to  provide  circulation  of  air 
as  in  a  standard  weather  station.  This  box  was  placed  along  one  side  of  the 
runway,  across  from  the  camera  shelter,  so  that  the  instruments  were  visible 
in  each  photograph  ( Plate  I ) .  The  camera  shelter  was  a  glass-fronted,  weather- 
proof box  containing  a  16-mm.  motion  picture  camera  synchronized  to  an 
electronic  flash  unit.  In  one  of  the  recorders  the  camera  was  actuated  by  a 
counterweighted  treadle  placed  in  the  mouse  runway  immediately  in  front 
of  the  instrument  shelter  (Plate  I,  bottom).  An  animal  passing  along  the 
runway  depressed  the  treadle,  thereby  closing  an  electrical  circuit  through  a 
mercury-dip  switch.  This  activated  a  solenoid  that  pulled  a  shutter-release 
pin  so  arranged  that  the  camera  made  a  single  exposure.  The  electronic 
flash  fired  while  the  shutter  was  open.  This  synchronization  was  easily  ac- 
complished by  having  the  film-advance  claw  close  the  flash  contact.  The 
camera  would  repeat  exposures  as  rapidly  as  the  treadle  could  be  depressed, 
but  at  night  about  three  seconds  were  required  for  the  flash  unit  to  recharge 
sufficiently  to  give  adequate  light  for  the  next  exposure. 

169 


348 


170  JOURNAL  OF  MAMMALOGY  Vol.40,No.2 

The  other  recorder  was  actuated  by  a  photoelectric  cell  instead  of  by  a 
treadle.  A  beam  of  deep  red  light  shone  from  the  camera  shelter  across  the 
runway  and  was  reflected  back  from  a  small  mirror  in  the  instrument  shelter 
to  a  photoelectric  unit  in  the  camera  shelter.  When  an  animal  interrupted  the 
light  beam,  the  photoelectric  unit  activated  a  solenoid  that  caused  the  camera 
to  make  a  single  exposure,  as  in  the  other  recorder. 

To  avoid  the  possibility  of  frightening  the  animals  it  would  be  desirable 
to  use  infra-red-sensitive  film  and  infra-red  light,  but  standard  electronic  flash 
tubes  emit  so  little  energy  in  the  infra-red  that  this  is  not  practical.  Instead, 
I  used  18  layers  of  red  cellophane  over  the  flash  tube  and  reflector  to  give 
a  deep  red  flash  of  light.  Wild  mice,  like  many  laboratory  rodents,  are  probably 
insensitive  to  deep  red  light.  I  found  no  evidence  that  the  flash,  which  lasts 
for  only  1/lOOOth  of  a  second,  frightened  the  mice.  A  muffled  clunk  made  by 
the  mechanism  also  seemed  not  to  alarm  the  mice  unduly. 

When  the  camera  diaphragm  was  set  to  give  the  proper  exposure  at  night, 
daytime  pictures  were  overexposed,  since  the  shutter  speed  was  considerably 
slower  than  l/30th  of  a  second.  To  reduce  the  daytime  exposure,  a  red  filter 
was  put  on  the  camera  lens.  The  filter  did  not  affect  night  exposures  because 
red  light  from  the  flash  passed  the  red  filter  with  little  loss.  In  addition,  on 
one  of  the  cameras  the  opening  in  the  rotary  shutter  was  reduced  to  give  a 
shorter  exposure. 

Both  recorders  function  on  110- volt  alternating  current.  The  treadle-actuated 
one  could  be  adapted  to  operate  from  batteries.  The  units  continue  to  record 
until  the  motion  picture  camera  runs  down  or  runs  out  of  film.  One  winding 
serves  for  several  hundred  pictures.  The  film  record  can  be  studied  directly 
by  projecting  the  film  strip  without  making  prints. 

The  camera  shelter  and  instrument  shelter  had  overhanging  eaves  to  prevent 
condensation  of  frost  and  dew  on  the  windows.  A  small  blackened  light  bulb 
was  also  kept  burning  in  the  camera  shelter  to  raise  the  temperature  enough 
to  retard  fogging  on  the  glass.  Animals  were  encouraged  to  stay  in  their  usual 
runway  by  a  picket  fence  made  of  twigs  or  slender  wires.   No  bait  was  used. 

A  few  individual  animals  could  be  recognized  in  the  pictures  by  scars  or 
molt  patterns,  but  most  had  to  be  live-trapped  and  marked.  Using  eartags  and 
fur-clipping  I  was  able  to  mark  distinctively  (Plate  I,  bottom)  all  of  the  mice 
captured  at  any  one  station.  The  clipping  remained  visible  for  days  or  months 
depending  upon  the  time  of  the  next  molt. 

The  apparatus  produces  photographic  records  such  as  those  shown  in  the 
lower  pictures  in  Plate  I.   These  can  be  transposed  into  some  form  as  Fig.  2. 

THE  STUDY  AREA 

The  study  centered  around  a  grassy-weedy  patch  surrounding  a  brush  pile 
in  Orinda,  Contra  Costa  County,  California  (Plate  I).  The  runways  wound 
through  a  20  X  20-foot  patch  of  tall  weeds  ( Artemisia  vulgaris,  Hemizonia  sp. 
and  Rumex  crispus)  and  under  the  brush  pile.   The  weeds  were  surrounded 


349 


May,  1959  PEARSON— TRAFFIC  SURVEY  171 

by  and  somewhat  intermixed  with  annual  grasses.    Oaks  and  other  trees,  as 
well  as  a  house  and  planting,  were  50  feet  away. 

Summer  climate  in  this  region  is  warm  and  sunny  with  official  mean  daily 
maximum  temperatures  rising  above  80  °F.  in  late  summer.  Official  temper- 
atures occasionally  reach  100°,  and  temperatures  in  the  small  instrument  shelters 
used  in  this  study  sometimes  exceeded  this.  Nights  in  summer  are  usually  clear 
and  with  the  mean  daily  minimum  temperature  below  52°  in  each  month. 
About  27  inches  of  rain  fall  in  the  winter  and  there  is  frost  on  most  clear 
nights.  The  mean  daily  maximum  temperature  in  January,  the  coldest  month, 
is  54°,  and  the  mean  daily  minimum  31°. 

PROCEDURE 

I  placed  the  first  recorder  in  operation  on  January  29,  1956,  and  the  second 
on  October  19,  1956.  Except  for  occasional  periods  of  malfunction  and  a  few 
periods  when  I  was  away  they  continued  to  record  until  the  end  of  the  study 
on  September  10,  1957.  Approximately  778  recorder-days  or  111  recorder- 
weeks  of  information  were  thus  obtained.  The  monthly  distribution  of  records 
was  as  follows:  January,  54  days;  February,  70;  March,  90;  April,  80;  May,  84; 
June,  67;  July,  52;  August,  88;  September,  48;  October,  33;  November,  52;  and 
December,  60. 

The  recorders  were  placed  at  what  appeared  to  be  frequently  used  Microtus 
runways,  usually  situated  on  opposite  sides  of  the  weedy  patch  20  to  30  feet 
apart.  For  one  period  of  four  months  one  of  the  recorders  was  placed  at  a 
similar  weedy  patch  70  yards  away.  Early  in  the  study  it  was  discovered  that 
a  neighbor's  Siamese  cat  sometimes  crouched  on  the  camera  shelter  waiting 
for  mice  to  pass  along  the  exposed  runway  in  front  of  the  instrument  shelter. 
Consequently,  a  2iA-foot  fence  of  2-inch-mesh  wire  netting  was  set  up  enclosing 
most  of  the  weedy  patch.  This  prevented  further  predation  by  cats  at  the  center 
of  the  study  area,  although  cats  continued  to  hunt  outside  of  the  fence  a  few 
yards  away  from  the  recorders.  The  only  other  tampering  with  predation  was 
the  removal  of  two  garter  snakes  on  April  11,  1957. 

RESULTS 

Traffic  in  individual  runways. — The  recorders  were  operated  at  eighteen 
different  stations.  At  seven  of  these  apparently  busy  runways  a  traffic  volume 
higher  than  a  few  passages  per  day  never  developed,  and  so  the  recorders 
were  moved  within  two  weeks.  Perhaps  the  mice  originally  using  these  runways 
had  abandoned  them  or  had  been  killed  shortly  before  a  recorder  was  moved 
to  their  runway,  or  perhaps  the  disturbance  of  placing  a  recorder  caused  the 
mice  to  divert  their  activities  to  other  runways.  At  the  other  eleven  stations 
a  satisfactory  volume  of  traffic  was  maintained  for  three  to  more  than  twenty 
weeks.  A  station  was  abandoned  and  the  recorder  moved  when  the  traffic 
had  decreased  to  a  few  passages  per  day.  Subsequently,  I  found  that  even  this 
little  activity  does  not  indicate  that  the  mice  are  going  to  abandon  the  runway, 


350 


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Vol.  40,  No.  2 


for  on  several  occasions  traffic  in  a  runway  dropped  this  low  and  then  climbed 
again  to  high  levels.  At  one  recorder  the  total  number  of  passages  in  consecutive 
weeks  was  183,  84,  26,  75  and  203.  The  runway  represented  in  Fig.  1  was  one 
of  those  used  most  consistently,  but  even  it  shows  marked  daily  and  weekly 
fluctuations.  It  is  probable  that  after  a  few  weeks  of  disuse  during  the  season 
when  grass  and  weeds  are  growing  rapidly,  a  runway  would  not  be  reopened, 
but  during  the  rest  of  the  year  an  abandoned  runway  remains  more  or  less 
passable  and  probably  more  attractive  to  mice  than  the  surrounding  terrain. 

Figure  1  summarizes  the  traffic  in  one  of  the  busiest  runways.  On  the  first 
night  there  were  an  unusual  number  of  records  of  harvest  mice  whose  curiosity 
may  have  been  aroused  by  the  apparatus.  Obviously  they  were  not  frightened 
away.  After  a  short  time  traffic  increased  to  a  high  level  and  remained  high 
until  the  middle  of  November,  when  passages  by  Microtus  decreased  sharply. 
During  the  week  before  the  decrease,  seven  marked  individuals  provided  most 
of  the  Microtus  traffic.  One  of  these  individuals,  an  infrequent  passerby,  dis- 
appeared at  the  time  of  the  decrease,  but  the  other  six  remained  nearby  for 
at  least  another  week  and  continued  to  pass  occasionally.  Those  Microtus  that 
disappeared  later  were  replaced  by  others  so  that  even  the  infrequent  passages 
in  late  November  and  early  December  were  being  provided  by  seven  marked 
individuals.  The  decrease  of  Microtus  traffic  was  caused,  therefore,  not  by 
deaths  but  by  a  change  in  runway  preference.  Several  of  these  same  individuals 
were  using  another  runway  20  feet  away  in  mid-January,  February  and  March. 

Three  to  six  marked  Reithrodontomys,  depending  upon  the  date,  were  pro- 
viding most  of  the  harvest-mouse  traffic  in  the  runway  represented  in  Fig.  1. 
The  average  number  of  passages  per  day  of  animals  of  all  kinds  was  eighteen. 
In  the  ten  other  most  successful  runways,  the  average  number  of  passages 
per  day  ranged  from  two  to  nineteen. 

Figure  2  gives  a  detailed  accounting  of  the  traffic  at  a  single  recording  station 
for  six  days.  One  can  judge  from  this  figure  the  kind  of  information  (excluding 


n  'OTHER 

^  =  MEADOW  MICE 

f{  ■HARVEST  MICE 


OCTOBER 


NOVEMBER 


DECEMBER 


Fig.  1. — Traffic  volume  along  one  runway  for  16  weeks.  Meaning  of  symbols  under 
the  base  line:  T=  live-trapping  carried  out  for  part  of  this  day;  0=  full  moon;  £=  total 
eclipse  of  the  moon;  R=  rain.  Columns  surmounted  by  a  vertical  line  represent  days  for 
which  the  recording  was  incomplete;  the  heights  of  the  various  segments  of  these  columns 
should  be  considered  minimum  values. 


351 


May,  1959 


PEARSON— TRAFFIC  SURVEY 


173 


temperatures  and  humidities)  obtained  with  the  recorders  and  can  at  the 
same  time  catch  a  reveahng  ghmpse  of  an  aspect  of  the  biology  of  small 
mammals  that  has  heretofore  been  revealed  inadequately  by  trapping  and  other 
techniques.  It  may  be  seen  that  the  mouse  traffic  was  provided  by  one  female 
and  two  male  harvest  mice  and  by  three  male,  three  female,  and  one  or  more 
unidentified  meadow  mice;  together  they  gave  between  15  and  24  passages 
each  day.  No  individual  passed  more  than  eight  times  in  one  day.  One  hai-vest 
mouse  ( R2 )  seemed  to  spend  the  day  to  the  left  and  to  make  a  single  excursion 


^:^:M^k^- 


PLATE  I 
Top:    Camera  shelter  (foreground)  and  instrument  shelter  in  position  at  a  mouse  runway 
on  the  study  area.   Bottom:   The  kind  of  records  obtained  with  the  recorder;  left — a  meadow 
mouse  marked  by  cHpping  two  strips  of  fur  on  the  hips;  riglit — a  marked  harvest  mouse 
crossing  the  treadle. 


352 


174                                            JOURNAL  OF  MAMMALOGY  Vol.  40,  No.  2 

to  the  light  each  night.  Harvest  mice  first  appeared  in  the  evening  between 
6:37  and  7:22  and  none  passed  after  6:26  in  the  morning.  Five  or  six  Microtus 
passed  within  a  few  hours  (February  24),  and  there  was  nightly  near-coinci- 
dence of  Reithrodontomijs  and  Microtus. 

Traffic  in  all  runways  combined. — During  the  111  recorder-weeks,  the  follow- 
ing passages  of  animals  were  photographed: 

Meadow  mouse,  Microtus  calif ornicus  6,077 

Harvest  mouse,  Rcithrodontomys  megalotis  1,753 

Bird  (see  following  account)  382 

Brush  rabbit,  Sylvilagus  hachmani  94 

Shrew,  Sorex  ornatus  56 

Peromyscus  (see  following  account)  39 

Fence  lizard,  Sceloporus  occidentalis  33 

Garter  snake,  Thamnophis  sp.  17 

Salamander  (see  following  account)  11 

Alligator  lizard,  Gerrhonotus  sp.  10 

House  cat,  Felis  domesticus  6 

Newt,  Taricha  sp.  5 

Pocket  gopher,  Thomomys  hottae  3 

Gopher  snake,  Pituophis  catenifer  3 

Mole  cricket,  Stenopelniatus  sp.  2 

Ground  squirrel,  Citellus  beecheyi  1 

Weasel,  Mustela  frenata  1 

King  snake,  Lampropeltis  getulus  1 

Racer,  Coluber  constrictor  1 


Total  8,495 

On  the  basis  of  trapping  results  in  this  and  in  similar  habitat  nearby,  large 
numbers  of  meadow  mice  and  harvest  mice  were  expected.  The  recording  of 
at  least  26  other  species  in  the  runways  came  as  a  pleasant  surprise.  Whereas 
all  of  these  species  would  be  expected  to  record  their  presence  eventually, 
some  of  them  are  rarely  seen  or  trapped  near  this  location.  After  living  five 
years  on  the  study  area,  after  doing  considerable  field  work  nearby,  and  after 
checking  the  recorders  twice  each  day  during  the  study,  I  have  not  yet  seen 
a  weasel  or  a  ground  squirrel  within  at  least  a  mile  of  the  study  area.  Weasels 
could  easily  escape  detection,  but  large,  diurnal  ground  squirrels  must  be 
very  rare.  The  single  individual  recorded  on  August  31  may  have  been  a 
young  squirrel  emigrating  from  some  distant  colony.  Noteworthy  absences 
were  those  of  wood  rats  (Neotoma  fuscipes),  moles  {Scapanus  latimanus), 
and  probably  California  mice  (Peromyscus  calif  ornicus) ,  all  of  which  were 
common  within  100  feet  of  the  recorders.  An  opossum  (Didelphis  marsupicilis) 
was  seen  a  few  feet  from  one  of  the  recorders  but  did  not  appear  on  the  films. 
No  house  mice  [Mtis  musculus)  were  detected  in  the  photographs,  although 


353 


May,  1959  PEARSON— TRAFFIC  SURVEY  175 

it  is  possible  that  some  passages  of  Mtis  were  listed  as  of  Reithrodontomys. 
House  mice  were  caught  occasionally  in  houses  nearby  and  in  a  field  near 
a  poultry  house  200  yards  away,  but  none  was  caught  during  frequent  live- 
trapping  near  the  recorders. 

The  total  of  8,495  passages  of  animals  gives  an  average  of  11  passages  per 
day  in  each  runway.  A  patient,  non-selective  predator  waiting  for  a  single 
catch  at  runways  such  as  these  could  expect,  theoretically,  a  reward  each  2.2 
hours.  The  mean  weight  of  animal  per  passage  was  about  31  grams,  which 
would  yield  approximately  40  calories  of  food.  This  much  each  2.2  hours 
would  be  more  than  enough  to  support  an  active  mammal  the  size  of  a  fox. 

Meadow  mouse. — The  6,077  Microtus  passages  were  distributed  throughout 
the  day  and  night  as  shown  in  Fig.  3  (above).  The  hours  of  above-ground 
activity,  however,  were  quite  different  in  winter  than  in  summer,  so  Fig.  3 
is  only  a  year-around  average  somewhat  biased  by  the  fact  that  more  Microtus 
were  recorded  in  the  spring  than  in  the  other  seasons.  A  more  detailed  analysis 
of  the  Microtus  data  will  be  given  in  a  later  report.  By  marking  as  many  of 
the  mice  as  possible,  it  was  found  that  usually  four  or  more  individual  Microtus 
were  using  each  runway  but  rarely  more  than  ten.  On  some  occasions  more 
than  60  Microtus  passages  were  recorded  at  a  single  point  in  24  hours. 

Harvest  mouse. — Harvest  mice  were  almost  entirely  nocturnal  (Fig.  3, 
center).  They  not  only  used  the  Microtus  runways,  but  their  passages  were 
frequently  intermixed  with  those  of  Microtus  ( Fig.  2 ) .  On  fourteen  occasions 
the  two  species  passed  within  60  seconds  of  each  other,  and  on  one  occasion 


-■ r-i ' 1 ' — I • — ^1 — 1 ■ r— 1 1 ni- 

o  MB  M       M  MM  M     MM     MM       R  M  M  MM  MM     MM  RMRR 

2  566  55  765BJ59  '' ^  %l     ^  K  IIV, 

9  a        i    a  (J(J  9cJc;9(J<J<J  9<J(J9  9iJ  Jddcf 


FEB.     , , . *J „ 1 1_] ,111 

25  -  26  I  I 


■n — ' ■— ' — I    '    '  ' — 1—; —I — I 

RMR         MMR  MMMMMRRM  M  RM  H 

373         57      4  8  6   6     5.  ^      .    5  7  3  5 

(39(J        <J9(f  9  <J(J(J(J(J(J  9  iJ  d 


FES.      JJ , ,_IJ 1_,_^ _LJ ,J-rl_ 

^^       ^'    RM  B  RRM      R  RMM       of    M  MMMM 

36  2274388  7  57 

dcJ  999  (5(599  9*9 


FEB. 
27-28 


-H 1 1—1 1 1 '-'-' ' I ""I  I  'I 

e        M            M     M                                                                     M                                R                  RRM                                             RMM           MRMMM  M  MM 

6           5     8                                                               5                              2                345                                         3                5                   6           7258  5  6 

(J(J9                                        (f                   9tf(JiJ                          6          i            <S       99i39  i  (f 


FEB  28- 


, M^ /—' rV r-^-V ' ■ ■    I  '      I    " V- 

"*'''^"   '  B  BBS  RM     M       MRMM  M    M    MMM      M  M  MMMMMR  MM 

2577  35  5  57118  5  857752  7  5 

9(J  9    9(S(J(J         (J  9  999  tf        9  (59    9(J9         9(5 


MARCH 


-r'-' H IT-' 1 '-'— 1 rn- 


'-2       MR  BB  B  M  RRM  MM        MR  R  M  MM    M  MMM  MRH         R 

73  5  335577347  77  8  5772  52 

9^  cr  (5(5(5       i59     9(5(5      9         9     9  9^9      99(5     9 

6  7  8  9  10  II        NOON         I  23456789  10  II        NIOHT       1  2  3  4  5  6 

Fig.  2. — A  sample  record  of  the  total  traffic  in  a  single  runway  over  a  period  of  six  days. 
Marks  above  the  base  Hnes  indicate  passages  from  right  to  left,  and  marks  below  the  base 
line  passages  from  left  to  right.  R  represents  Reithrodontomtjs;  M,  Microtus;  B,  bird  ( includes 
brown  towhee,  wren-tit,  and  song  sparrow);  and  RAB,  brush  rabbit.  Most  of  the  mice  are 
further  identified  by  number  and  sex. 


354 


176 


JOURNAL  OF  MAMMALOGY 


Vol.  40,  No.  2 


a  4-month-old  male  Microtus  and  a  5-month-old  male  Reithrodontomys  ap- 
peared in  the  same  photograph. 

The  history  of  one  runway  indicates  that  traffic  by  Reithrodontomys  alone 
does  not  keep  a  Microtus  runway  open.  One  or  more  Microtus  passed  almost 
daily  along  this  runway  during  February.  At  the  end  of  the  month  the 
Microtus  disappeared  and  two  Reithrodontomys  became  active  in  the  same 
runway.  Despite  an  average  of  3.3  passages  per  day  by  Reithrodontomys 
throughout  March  and  up  to  mid-April,  grass  and  weed  seedlings  grew  up 


3,0 

>- 
O 

z 

UJ 

§5 

- 

MEADOW    MICE 
ALL   MONTHS 
N  =  6077 

- 

UJ 

U. 

6     7     8     9     10    II     12     I 
NOON 


234567     89    lO    II     12    I      23456 

NIGHT 


Sic 

>- 
o 

z 

UJ 

cr 

u. 


HARVEST    MICE 

ALL    MONTHS 

N  =  1753 


6     7     8    9      10    II     12     I      2     3     4     5     6     7     8     9     10    II     12     I 
NOON  NIGHT 


2     3     4     5     6 


20 


> 
o 

I  10 
o 

or 


BRUSH    RABBIT 
N=  94 


m 


6     7     8     9     10    II     12     I      2     3     4     5     6     7     8     9     10    II     12     I 
NOON  NIGHT 


2     3     4     5     6 


Fig.  3. — Distribution  by  hours  of  6,077  passages  of  meadow  mice  (above);  1,753  passages 
of  harvest  mice  (center);  and  94  passages  of  brush  rabbits  (below). 


355 


May,  1959 


PEARSON— TRAFFIC  SURVEY 


177 


in  the  runway  and  it  began  to  look  unused.  By  the  end  of  April  almost  all 
traffic  had  ceased. 

The  Reithrodontomys  data  will  be  analyzed  in  a  later  report. 

Birds. — Of  the  382  bird  records,  at  least  255  were  of  sparrows  ( at  least  122 
song  sparrow;  the  remainder  mostly  fox  sparrow,  white-crowned  sparrow  and 
■golden-crowned  sparrow ) .  Other  birds  recognized  were  wren-tit,  wren,  brown 
towhee  and  thrush.  On  several  occasions  birds,  especially  song  sparrows,  battled 
their  reflections  in  the  window  of  the  instrument  shelter.  This  caused  long 
series  of  exposures.  Each  series  was  counted  as  a  single  passage.  If  the  bird 
stopped  for  a  minute  or  more  and  then  returned  to  the  battle,  this  was  counted 
as  another  passage.    All  bird  records  were  during  daylight  hours. 

On  three  occasions  a  sparrow  and  an  adult  Microtus  appeared  in  the  same 
photograph.  On  one  of  these  occurrences  a  song  sparrow  was  battling  its 
reflection  when  an  adult,  lactating  Microtus  came  along  the  runway.  The 
sparrow  retreated  about  12  inches  toward  the  camera  shelter  and,  as  soon 
as  the  mouse  had  passed,  returned  to  the  runway. 

Brush  rabbit. — All  except  four  of  the  records  of  brush  rabbits  were  in  June 
and  July  of  1957,  a  season  when  these  animals,  especially  young  ones,  were 
abundant.  Figure  3  (below)  shows  that  they  were  most  active  in  the  early 
morning. 


-^20- 


o 

^    10 

■=> 
a 
tu 


CL 


jh 


30 


>20 
o 

z 

UJ 

3 

S  10 
cr 


6     8     10   12    2    4     6 
NOON 


8     10    12    2     4 

NIGHT 


JFMAMJJASOND 


Fig.  4. — Distribution  by  hours  of  56  passages  of  shrews  (left)  and  distribution  by  months 
of  56  passages  of  shrews  (right). 

Shrew. — The  dry,  weedy  habitat  chosen  was  not  favorable  for  shrews,  and 
they  were  near  the  minimum  weight  necessary  to  depress  the  treadle  of  one  of 
the  recorders,  so  that  some  may  have  passed  along  the  runway  without  making 
a  record.  The  shrews  were  highly  nocturnal  (Fig.  4,  left)  and  avoided  the 
surface  runways  during  the  dry  summer  months  (Fig.  4,  right).  Since  captive 
specimens  of  Sorex  are  rarely  inactive  for  more  than  one  hour  ( Morrison,  Amer. 
Midi.  Nat.,  57:  493,  1957),  the  scarcity  of  records  in  the  daytime  probably 
means  only  that  the  shrews  were  not  moving  above  ground  at  this  time.  They 
may  have  been  foraging  along  gopher,  mole  and  Microtus  tunnels  during  the 
daytime. 


356 


178 


JOURNAL  OF  MAMMALOGY 


Vol.  40,  No.  2 


A  shrew  was  marked  on  March  4,  a  few  inches  from  one  of  the  recorders. 
It  was  captured  15  feet  away  on  May  30  and  5  feet  farther  away  on  June  23. 
It  passed  along  the  study  runway  five  times  in  the  16-week  interval  between 
first  and  last  capture:  on  March  13,  27,  31,  and  April  17,  and  possibly  on 
April  10  (markings  obscured).  Another  shrew  was  recorded  on  March  27. 
Unless  baited  traps  attract  shrews  from  a  considerable  distance,  or  the  recorder 
repels  them,  a  trapper  setting  traps  in  this  runway  for  a  few  nights  would  have 
had  small  chance  of  recording  the  presence  of  this  individual  which  apparently 
was  nearby  for  at  least  16  weeks. 

Not  a  single  shrew  was  recorded  during  the  dry  summer  months  of  June, 
July  and  August.  Nevertheless,  on  July  8  when  I  was  checking  the  photo- 
electric recorder  at  5:55  am,  a  shrew  emerged  completely  from  a  small  hole  in 


100 


90 


80 


70 


60 


1    50 

Q 

i 

X 


UJ    40 
> 


UJ 

a: 


30 


20 


10 


•   :  SHREWS 
O   =   LIZARDS 


50  60 

TEMPERATURE 


CF) 


Fig.  5. — A  comparison  of  the  temperatures  and  humidities  encountered  by  shrews  and 
fence  Hzards  in  tlie  runways.  The  larger  circles  show  the  position  of  the  mean  for  each 
species.  The  large  polygon  encloses  the  range  of  temperatures  and  humidities  available 
to  the  animals  during  the  study. 


357 


May,  1959  PEARSON— TRAFFIC  SURVEY  179 

the  ground  a  few  inches  from  the  instrument  shelter,  twitched  his  nose  rapidly 
for  a  few  seconds,  and  retreated  down  the  same  hole.  The  air  temperature  was 
54°  and  the  relative  humidity  78  per  cent — normal  for  this  season.  Obviously 
shrews  were  present  on  the  study  area  during  some  or  all  of  the  summer  months 
but  were  not  frequenting  the  surface  runways. 

Figure  5  shows  the  temperatures  and  relative  humidities  encountered  above 
ground  by  the  shrews  on  the  study  area  compared  with  the  total  range  of 
temperatures  and  humidities  recorded  throughout  the  study.  By  their  nocturnal, 
winter-time  activity  shrews  encountered  the  coldest,  most  humid  conditions 
available  in  the  region.  In  contrast,  the  similarly  small,  insectivorous  fence 
lizards  existing  in  the  same  habitat  managed  by  their  own  behavioral  patterns 
to  encounter  a  totally  different  climate  (Fig.  5).  The  mean  of  the  temperatures 
recorded  at  the  times  of  lizard  passages  was  39°  warmer  than  that  recorded 
for  shrew  passages,  and  relative  humidity  was  36  per  cent  lower. 

This  activity  pattern  of  shrews  differs  from  that  reported  by  Clothier  (Jour. 
Mamm.,  36:  214-226,  1955)  for  Sorex  vagrans  in  Montana.  He  found  shrews 
there  to  be  active  "both  day  and  night  and  throughout  the  year,  even  during 
extremely  bad  weather."  It  is  important  to  understand,  however,  that  he 
collected  in  damp  areas  near  water,  where  the  shrews  may  not  have  had  to 
modify  their  activity  to  avoid  desiccation.  Extremely  bad  weather,  for  a 
shrew,  is  hot  dry  weather. 

Peromyscus. — Peromyscus  truei  was  abundant  in  brushy  places  and  in  houses 
nearby;  P.  maniculatus  was  scarce.  Some  of  the  Peromyscus  records  were 
clearly  of  truei  and  some  may  have  been  of  maniculatus,  but  many  could  not 
be  identified  with  certainty.  No  adult  P.  californicus  was  recognized  although 
a  few  young  ones  may  have  passed  and  been  listed  as  truei.  All  passages  of 
Peromyscus  were  at  night. 

Salamander. — The  record  includes  passages  by  both  Etisatirui  escholtzii  and 
Aneides  luguhris.  They  were  recorded  in  October,  November,  March  and  April. 
By  being  nocturnal  and  by  avoiding  the  dry  season,  they  encountered  in  these 
autumn  and  spring  months  about  the  same  microclimate  as  shrews,  but  were 
recorded  neither  in  the  winter  months  nor  at  temperatures  below  39°.  A  third 
species,  Batrachoccps  attenuatus,  was  common  in  the  study  area  but  is  so  small 
that  it  could  not  be  expected  to  actuate  either  of  the  recorders.  One 
Batrachoccps  electrocuted  itself  underneath  the  treadle  but  has  not  been 
included  in  the  records. 

Comparison  of  traps  and  recorders. — The  combination  of  live-trapping  and 
photographing  revealed  a  failure  of  small  mammals  to  move  between  runways 
only  a  few  feet  apart.  On  several  occasions  meadow  mice  and  harvest  mice 
were  live-trapped  a  few  feet  from  one  of  the  recorders,  were  released  at  the 
same  place,  and  were  recaptured  a  week  or  more  later  not  more  than  a  few 
feet  away,  yet  during  the  intervening  time  they  failed  to  pass  the  recorder. 
Conversely,  some  individual  mice  repeatedly  recorded  themselves  on  the  films 
yet  could  never  be  induced  to  enter  any  of  a  large  number  of  live  traps  placed 


358 


180  JOURNAL  OF  MAMMALOGY  Vol.  40,  No.  2 

in  the  same  runway  and  in  nearby  runways.  It  is  obvious  that  all  mice  present 
do  not  use  all  of  the  active  runways  close  to  their  home,  and  it  is  also  obvious 
that  neither  the  recorders  nor  traps  give  a  complete  accounting  of  the  mice 
present. 

SUMMARY 

A  motion-picture  camera  synchronized  to  an  electronic  flash  unit  was  used  to  record  the 
passage  of  animals  along  meadow-mouse  runways  and  to  record  the  temperature,  relative 
humidity  and  time  at  which  they  passed.  More  than  26  species  used  the  runways  during 
111  weeks  of  recording.  Meadow  mice,  harvest  mice,  sparrows,  brush  rabbits  and  shrews 
passed  most  frequently.  The  average  traffic  per  day  in  each  runway  was  11  passages;  on 
some  days  there  were  more  than  60  passages.  Rarely  more  than  ten  meadow  mice  or 
six  harvest  mice  used  a  runway  in  any  one  period.  Meadow  mice  and  harvest  mice  used 
the  same  runways  simultaneously.  Traffic  by  harvest  mice  alone  did  not  keep  the  run- 
ways open. 

Meadow  mice  were  active  during  the  day  and  night;  harvest  mice  were  strongly  nocturnal. 
Brush  rabbits  were  active  primarily  early  in  the  morning.  Almost  all  shrews  were  recorded 
at  night  and  in  the  winter  months.  Consequently,  they  encountered  the  coldest,  most 
humid  conditions  available  to  them.  In  contrast,  the  similarly  small,  insectivorous  fence 
lizards  encountered  a  microclimate  that  was  39°  warmer  and  36  per  cent  less  humid. 

Neither  traps  nor  recorders  accounted  for  all  the  individuals  living  nearby. 

Museum  of  Vertebrate  Zoology,  Berkeley,  California.    Received  October  29,  1957. 


359 


PREY  SELECTION  AND  HUNTING  BEHAVIOR 
OF  THE  AFRICAN  WILD  DOG' 

RICHARD   D.    ESTES,   Division   of  Biological   Sciences,   Cornell    University,    Ithaca,    Nevv  York 
JOHN   GODDARD,   Game   Biologist,   Ngorongoro   Conservation   Area,   Tanzania 

Abstract:  African  wild  dog  (Lijcaon  picttis)  predation  was  observed  in  Ngorongoro  Crater,  Tanzania, 
between  September,  1964,  and  July,  1965,  when  packs  were  in  residence.  The  original  pack  of  21  dogs 
remained  only  4  months,  but  7  and  then  6  members  of  the  group  reappeared  in  the  Crater  at  irregular 
intervals.  The  ratio  of  males: females  was  disproportionately  high,  and  the  single  bitch  in  the  small  pack 
had  a  litter  of  9  in  which  there  was  only  one  female.  The  pack  functions  primarily  as  a  hunting  unit, 
cooperating  closely  in  kilhng  and  mutual  defense,  subordinating  individual  to  group  activity,  with  strong 
discipline  during  the  chase  and  unusually  amicable  relations  between  members.  A  regular  leader  se- 
lected and  ran  down  the  prey,  but  there  was  no  other  sign  of  a  rank  hierarchy.  Fights  are  very  rare.  A 
Greeting  ceremony  based  on  infantile  begging  functions  to  promote  pack  harmony,  and  appeasement 
behavior  substitutes  for  aggression  when  dogs  are  competing  over  meat.  Wild  dogs  hunt  primarily  by 
sight  and  by  daylight.  The  pack  often  approaches  herds  of  prey  within  several  hundred  yards,  but  the 
particular  quarry  is  selected  only  after  the  chase  begins.  They  do  not  run  in  relays  as  commonly  sup- 
posed. The  leader  can  overtake  the  fleetest  game  usually  within  2  miles.  While  the  others  lag  behind, 
one  or  two  dogs  maintain  intervals  of  100  yards  or  more  behind  the  leader,  in  positions  to  intercept  the 
quarry  if  it  circles  or  begins  to  dodge.  As  soon  as  small  prey  is  caught,  the  pack  pulls  it  apart;  large 
game  is  worried  from  the  rear  until  it  falls  from  exhaustion  and  shock.  Of  50  kills  observed,  Thomson's 
gazelles  (Gazella  thomsonii)  made  up  54  percent,  newborn  and  juvenile  wildebeest  {Connochaetes 
taiirmus)  36  percent.  Grant's  gazelles  (Gazella  granti)  8  percent,  and  kongoni  (Alcelaphus  buselaphus 
cokei)  2  percent.  The  dogs  hunted  regularly  in  early  morning  and  late  afternoon,  with  a  success  rate 
per  chase  of  over  85  percent  and  a  mean  time  of  only  25  minutes  between  starting  an  activity  cycle  to 
capturing  prey.  Both  large  and  small  packs  generally  killed  in  each  hunting  cycle,  so  large  packs  make 
more  efficient  use  of  their  prey  resource.  Reactions  of  prey  species  depend  on  the  behavior  of  the  wild 
dogs,  and  disturbance  to  game  was  far  less  than  has  been  represented.  Adult  wildebeest  and  zebra 
(Equus  burchelli)  showed  little  fear  of  the  dogs.  Territorial  male  Thomson's  gazelles,  which  made  up 
67  percent  of  the  kills  of  this  species,  and  females  with  concealed  fawns,  were  most  vulnerable.  The 
spotted  hyena  (Crocuta  crocuta)  is  a  serious  competitor  capable  of  driving  small  packs  from  their  kills. 
A  minimum  of  4-6  dogs  is  needed  to  function  effectively  as  a  pack.  It  is  concluded  that  the  wild  dog 
is  not  the  most  wantonly  destructive  and  disruptive  African  predator,  that  it  is  an  interesting,  valuable 
species  now  possibly  endangered,  and  should  be  strictly  protected,  particularly  where  the  small  and 
medium-sized  antelopes  have  increased  at  an  alarming  rate. 


The  habits  of  the  African  wild  dog  or 
Cape  hunting  dog  (Lijcaon  pictus)  have 
been  described,  sometimes  luridly,  in  most 
books  about  African  wildlife.  Accounts  by 
such  famous  hunters  and  naturalists  as 
Selous  (1881),  Vaughan-Kirby  (1899),  and 
Percival  (1924),  repeated  and  embellished 
by  other  authors,  have  created  the  popular 
image  of  a  wanton  killer,  more  destructive 
and  disruptive  to  game  than  any  other 
African  predator. 

^  Field  work  supported  by  the  National  Geo- 
graphic Society;  also  by  grants  from  the  New  York 
Explorers  Club  and  the  Tanzania  Ministry  of 
Agriculture,  Forests  and  Wild  Life. 

52 


Because  of  its  bad  reputation,  the  wild 
dog  was  relentlessly  destroyed  in  African 
parks  and  game  reserves  for  many  years. 
In  Kruger  National  Park,  for  instance,  it 
was  shot  on  sight  from  early  in  the  present 
century  up  until  1930  as  part  of  an  overall 
policy  to  keep  predators  down.  In  Rhode- 
sia's Wankie  National  Park  some  300  wild 
dogs  were  killed  by  gun  and  poison  be- 
tween 1930  and  1958. 

Acceptance  of  modem  concepts  of  wild- 
life management  has  finally  brought  an 
end  to  the  indiscriminate  destruction  of 
wild  dogs  and  other  predators  in  most,  if 
not  all,  African  national  parks.  There  is  now 


360 


The  African  Wild  Dog  •  Estes  and  Goddard        53 


a  general  awareness  among  game  wardens  in  sanctuaries,  paid  very  little  attention  to 

of  the  predator's  role  in  regulating  popula-  cars   and   could   be   watched   undisturbed 

tions,  which  perhaps  began  with  Stevenson-  from  within  30  yards  or  less.    It  was  also 

Hamilton  ( 1947 ) ,  Warden  of  Kruger  Park  feasible  to  keep  pace  with  the  pack  during 

for  almost  30  years,  who  related  the  alarm-  chases  over  the  central  Crater  floor,  either 

ing    increase    of    impala    {Aepijceros    me-  driving  parallel  to  the  leader  at  a  distance 

lampus)  to  the  disappearance  of  the  park's  of  100-200  yards  or  following  behind  and 

formerly  large  wild  dog  packs.  to  one  side  so  as  not  to  get  in  the  way  of 

While  the  wild  dog  has  benefited  from  other  pack  members.    To  locate  the  pack 

more  enlightened  concepts  of  game  man-  initially,  we  often  drove  to  an  observation 

agement,  its  reputation,  still  based  on  pop-  point  on  a  hill  and  scanned  the  Crater  with 

ular  writings  and  myth,  remains  unchanged,  binoculars  and  a  20-power  binocular  tele- 

I       But  recent  scientific  investigations  indicate  scope.  When  the  pack  was  moving  it  could 

that  a  new  and  less-prejudiced  evaluation  often  be  spotted  at  a  distance  of  over  5 

of  this   species   is   long   overdue.     Kiihme  miles,  and  a  number  of  chases  and  kills 

( 1965 )  has  studied  the  social  behavior  and  were    clearly    observed    from     a    hilltop 

family  life  at  the  den  of  a  pack  with  young  through  the  telescope. 

whelps  on  the  Serengeti  Plains,  Tanzania. 

We  have  observed  prey  selection  and  hunt-  RESULTS 

ing   behavior   in    a   free-ranging   pack   of  _     ,     _ 

J  ,^        J  .  1      •  V     XT  Pack  Composition 

adults  and  juveniles  m  nearby  Ngorongoro  ^ 

Crater,  a  caldera  with  a  floor  area  of  104         The  pack  that  first  entered  Ngorongoro 

square  miles  that  supports  a  resident  pop-  Crater  in   September,   1964,   contained  21 

ulation   of  around  25,000  common   plains  animals,  including  8  adult  males,  4  adult 

herbivores.  The  two  studies  together  throw  females,  and  9  juveniles.    They  remained 

quite  a  different  light  on  the  habits,  char-  more  or  less  continually  in  residence  through 

acter,   and   predator-prey  relationships   of  December,  then  disappeared  and  were  pre- 

this  highly  interesting  species.  sumed  to  have  left  the  Crater.  One  juvenile 

We  are  indebted  to  Dr.  B.  Foster  of  the  female  had  died  of  unknown  causes.   Dur- 

Royal    College,    Nairobi,    and    to    G.    C.  ing  January,  1965,  seven  members  of  the 

Roberts  of  the  Crater  Lodge  for  reporting  same  pack,  4  males,  1  female,  and  2  juvenile 

four  kills   and   one  kill  respectively,   that  males,    reappeared;    after    a    lapse    of    5 

they  witnessed  in  the  Crater;  also  to  Pro-  months,  apparently  the  same  animals,  minus 

fessors  W.  C.  Dilger,  O.  H.  Hewitt,  and  one   male,   again   took   up   residence,   and 

H.  E.  Evans  of  Cornell  University  for  criti-  have  been  observed  off  and  on  up  to  the 

cal  readings  of  the  manuscript.   Nomencla-  present  writing.  In  March,  1966,  the  female 

ture  follows  Haltenorth   (1963)   for  artio-  whelped  but  died  5  weeks  later,  leaving 

dactyls,  and  Mackworth-Praed  and  Grant  8   male   and   1   female   pups.    They  were 

(1957)  for  birds.  brought  up  by  the  5  males,  who  fed  them 

by  regurgitation  until  they  were  old  enough 

MtTHODS  j-Q  j.yj^  \Ni\h  the  pack.   However,  the  female 

Most   observations   were   made   from    a  and  4  male  pups  died,  leaving  an  all-male 

vehicle;  we  each  had  a  Land  Rover  and  pack  of  9  in  August,  1966. 
usually  operated  independently.    The  wild         While  an  all-male  pack  must  be  excep- 

dogs,   like   many   other  African   predators  tional,  there  is  other  evidence  to  suggest 


361 


54        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


that  a  high  proportion  of  males  may  be  observed  sexual  behavior  on  only  two  oc- 
common  in  this  species.  The  pack  Kiihme  casions,  when  one  male  mounted  another 
studied  consisted  of  6  adult  males  and  2  repeatedly  as  the  latter  was  feeding  at  a 
adult  females,  which  had  11  and  4  pups  kill.  Kiihme  also  saw  very  little  sexual  be- 
respectively,  sex  unreported.  During  2-3  havior.  When  two  animals  were  competing 
years  of  shooting  in  Kruger  National  Park,  for  the  same  piece  of  meat,  each  would  try 
the  ratio  of  males  was  6  :  4,  despite  an  to  burrow  beneath  the  other,  its  forequarters 
attempt  to  select  females  (Stevenson-Hamil-  and  head  flat  to  the  ground  and  hind- 
ton  1947).  We  have  no  explanation  to  offer  quarters  raised,  tail  arched  and  sometimes 
for  the  discrepancy,  but  if  it  is  real  and  wagging.  The  ears  were  flattened  to  the 
not  normal,  it  might  help  explain  the  head  and  the  lips  drawn  back  in  a  "grin," 
reported  decline  of  wild  dogs  during  recent  while  each  gave  excited  twittering  calls.  As 
years  in  many  parts  of  Africa.  Kiihme  observed  (p.  516),  the  dogs  "tried 

to  outdo  each  other  in  submissiveness." 

Social  Organization  In  this  way  juveniles  and  even  subadults 

Leadership  and  Rank  Hierarchy. — In  the  manage  to  monopolize  kills  in  competition 
full  pack  of  21  and  in  the  pack  of  7,  the  with  adults.  The  young  thus  enjoy  a  priv- 
same  adult  male  was  consistently  the  ileged  position  in  the  pack.  Pups  at  the 
leader;  he  usually  led  the  pack  on  the  hunt,  den  successfully  solicit  any  adult  to  regur- 
selected  the  prey,  and  ran  it  down.  In  the  gitate  food  by  poking  their  noses  into  the 
pack  of  6,  from  which  the  above  male  was  corner  of  the  adult's  mouth,  sometimes  lick- 
absent,  the  adult  female  was  the  leader,  ing  and  even  biting  at  the  lips.  Since  all 
One  of  the  males  filled  the  position  after  pack  members  contribute  to  feeding  and 
her  death.  protection  of  the  young,  the  mother  is  not 

Apart  from  the  position  of  leader,  we  saw  essential  to  their  survival  after  the  first  few 

no  indication  of  a  rank  order.   Kiihme  con-  weeks. 

eluded  there  was  no  hierarchy  in  the  pack  Greeting  Ceremony. — Whenever  the  pack 
he  observed,  nor  even  a  leader.  The  equality  became  active  after  a  rest  period,  and 
of  pack  members  may  partly  explain  the  particularly  if  two  parts  of  the  pack  were 
singularly  amicable  relations  typical  of  the  reunited  after  being  separated,  the  mem- 
species.  On  the  other  hand,  competition  for  bers  engaged  in  a  Greeting  ceremony  ( Fig. 
food  and  females  could  easily  lead  to  ag-  1),  in  which  face-licking  and  poking  the 
gression;  yet  neither  Kiihme  nor  we  ever  nose  into  the  corner  of  the  mouth  played  a 
saw  a  fight.  prominent  part.    The   ceremony  thus   ap- 

Food  Solicitation  and  Appeasement  Be-  f)ears  to  be  ritualized  food  solicitation;  the 

havior. — Overt  aggression  and  fighting  are  fact  that  Kiihme  actually  saw  regurgitation 

minimized  through  ritualized  appeasement  elicited  by  begging  adults  supports  this   in- 

behavior  derived  from  infantile  food  beg-  terpretation.    The   Greeting   ceremony   in 

ging.   Begging  and  appeasement  appear  in  the  wolf  (Canis  lupus),  in  which  one  takes 

almost  every  contact  between  individuals,  another's  face  in  its  jaws,  may  have  the 

and  particularly  in  situations  where  aggres-  same  derivation. 

sion  would  be  most  likely  to  occur — for  As  a  prelude  to  greeting,  dogs  typically 

instance,  when  animals  are  competing  over  adopted  the  Stalking  attitude  (Fig.  2),  with 

a  kill.    However,  we  cannot  comment  on  the  head  and  neck  held  horizontally,  shoul- 

sexual  competition,  having  seen  none;  we  ders  and  back  hunched,  and  the  tail  usually 


362 


The  African  Wild  Dog  •  Estes  and  Goddard        55 


Fig.    1.     Greeting  ceremony. 

hanging.  Kiihme  (p.  512)  interprets  this 
posture  as  inhibited  aggression;  the  same 
attitude  is  adopted  when  approaching  po- 
tential prey  and  competitors  of  other 
species.  The  Stalking  posture  changed  to 
greeting  when  dogs  got  close.  In  greeting- 
solicitation,  as  they  licked  each  other's  lips 
and  poked  the  nose  into  the  corner  of  the 
mouth,  one  or  both  crouched  low,  with 
head,  rump,  and  tail  raised  stiffly  ( Fig.  1 ) . 
Except  for  the  raised  head,  this  resembles 
the  submissive  posture  displayed  when  two 
dogs  are  competing  over  food.  The  Greet- 
ing ceremony  was  also  frequently  per- 
formed while  two  dogs  trotted  or  ran  side 
by  side. 

Vocal  Communication. — Although  Perci- 
val  (1924),  Stevenson-Hamilton  (1947),  Ma- 
berly  (1962),  Kiihme  (1965),  and  others 
have  given  good  descriptions  of  wild  dog 
calls,  the  function  of  the  calls  has  often 
been  misinterpreted.  This  applies  partic- 
ularly to  two  of  the  three  most  frequently 
heard  calls  (Nos.  1  and  3): 

1.  Contact  call — a  repeated,  bell-like 
"hoo."  Often  called  the  Hunting  call,  it  has 
nothing  to  do  with  hunting  as  such,  but  is 
given  only  when  members  of  a  pack  are 
separated.  Though  a  soft  and  musical 
sound,  it  carries  well  for  2  or  more  miles. 
When  members  of  the  Ngorongoro  pack- 
were  missing,  an  imitation  of  the  Contact 
call  would  bring  the  rest  to  their  feet, 
whereas  there  was  at  best  onlv  a  mild  reac- 


Fig.   2.     The   Stalking   attitude,    here   displayed   by   the   pack 
leader  while  approaching  a  herd  of  gazelles. 

tion  to  imitations  when  the  full  pack  was 
assembled. 

2.  Alarm  hark — a  deep,  gruff  bark,  often 
combined  with  growling,  given  when  star- 
tled or  frightened.  A  good  imitation  near 
a  resting  pack  elicited  an  immediate  star- 
tled reaction. 

3.  Twittering — a  high-pitched,  birdlike 
twitter  or  chatter.  The  most  characteristic 
and  unusual  vocalization,  it  expresses  a 
high  level  of  excitement.  It  is  given  in  the 
prelude  to  the  hunt,  while  making  a  kill,  in 
mobbing  hyenas  or  a  pack  member,  and  by 
dogs  competing  over  food.  Its  primary 
function  is  evidently  to  stimulate  and  con- 
cert pack  action.  Kiihme  described  this 
call  (Schnattern)  only  in  the  context  of  the 
Greeting  ceremony  (p.  513). 

Besides  these  vocalizations,  whining  may 
be  heard  during  appeasement  behavior  and 
when  pups  are  begging,  and  members  of 
the  pack  sometimes  yelp  like  hounds  when 
close  on  the  heels  of  their  prey.  Kiihme 
(p.  500)  further  distinguishes  an  Enticing 
call  (Locken)  given  by  adults  calling  the 
young  out  of  the  den,  and  a  Lamenting  call 
(Klage)  given  by  pups  when  deserted. 

Olfactory  and  Visual  Communication. — 
Wild  dogs  hunt  primarily  by  sight  and  by 
daylight.  We  never  saw  them  track  prey  by 
scent.  Though  they  evidently  have  a  good 
nose  and  may  well  use  it  for  tracking  in 
bush  country,  olfaction  in  this  species  seems 
to  have  a  primarily  intraspecific  significance. 


363 


^cn 


56        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


\^  regular  hunting  cycle  is   the  likeUest  ex- 

planation; it  was  more  usual,  however,  for 
the  pack  then  to  wait  until  the  following 
regular  period.  Wild  dogs  will  also  hunt  on 
moonlight  nights,  as  Stevenson-Hamilton 
noted.  When  the  Crater  dogs  had  not  killed 
before  dusk,  the  hunt  was  sometimes  pro- 
longed. The  latest  kill  we  recorded  was  at 
7:32  PM,  when  it  was  fully  dark. 

Since  they  are  capable  of  functioning  as 
a  pack  and  of  hunting  successfully  after 
dark,  the  fact  that  wild  dogs  are  so  strongly 
diurnal  may  seem  puzzling.   But  it  may  be 
Fig.  3.    Time  distribution  of  50  wild  dog  kills.  explained  by  the  fact  that  they  hunt  mainly 


1 

1          CO 

CO 

_j 

1 

1       ^ 

_i 

U- 

o 

L 

o 

1 

■    .0. 

1    I  ■ 

Ji 

J 

6 

li- 

7'8 

'  12  '   1  '  2  '  3  '  4 

5 

PM^ 

TIME 

by  sight;  it  would  be  much  more  difficult 

Wild  dogs  are  renowned  for  their  peculiarly  to  locate  prey  and  single  out  a  quarry  at 

strong,   and  to   many  humans   disgusting,  night.   As  to  the  regularity  and  brevity  of 

odor,  which  may  emanate  from  anal  glands  their  hunting  cycles  in  early  morning  and 

but  seems  to  come  from  the  whole  body,  late  afternoon,  this  is  partly  a  measure  of 

Sniffing  under  the  tail,  responsive  urination  their  hunting  efficiency,  discussed  below, 

and  defecation  are  socially  important  activ-  Also,  of  course,  these  are  the  times  in  the 

ities.   But  the  main  role  of  the  strong  body  day    when    diurnal    animals,    particularly 

odor  may  be  to  permit  high-speed  tracking  herbivores,  are  most  active  and  most  ap- 

of  the   pack  by   members   that  have  lost  proachable. 

visual  contact.  Lagging  members  seen  run-  Apart  from  a  certain  amount  of  play  and 

ning  on  the  track  taken  by  the  rest  of  the  other  social  activities  shortly  before  starting 

pack  sometimes  appeared  to  be  using  their  to    hunt    and    immediately    after    feeding, 

noses.  Similarly,  the  white  tail  tip  probably  pack   members   were   usually    active   only 

helps  maintain  visual  contact  in  bush  coun-  while  actually  hunting.  At  other  times  they 

try,  high  grass,  and  under  crepuscular  con-  could  often  be  found  resting  near  or  in  the 

ditions;  in  a  species  notable  for  every  pos-  same  place  where  they  had  settled  after  the 

sible  color  variation,  a  white-tipped  tail  is  morning   or   evening   kill.    When   resting, 

the  most  constant  and  conspicuous  mark.  pack  members  customarily  lay  touching  in 

close  groups  (Fig.  4).   Generally  speaking, 

Daily  Activity  Pattern  ^^xe  pack  became  active  between  5:30  and 

The  Ngorongoro  pack  had  two  well-de-  6:15   pm,   and   in   the   morning  within   Mj 

fined  hunting  periods  each  day  (Fig.  3).  hour   of  dawn,   remaining   active   for   1-2 

That  this  periodicity  is  characteristic  of  the  hoiu-s.    But  where   game   is   less   plentiful 

species  may  be  inferred  from  Kiihme's  ob-  than  it  is  in  Ngorongoro,  and  a  pack  must 

servations   (p.  511),  and  from  Stevenson-  range   more  widely    (Stevenson-Hamilton 

Hamilton's   (1947)   observations  in  Kruger  gives  a  range  of  at  least  1,500  square  miles 

National  Park.   In  nine  recorded  instances,  for   a   Transvaal   pack   whose   movements 

though,  the  Ngorongoro  dogs  killed  between  were  reported  over  a  period  of  years ) ,  a 

8:30  AM  and  3:30  pm,  well  outside  the  nor-  good   deal   of   time   between   and   during 

mal   periods.     Failure   to   kill   during   the  hunts  must  be  spent  in  travel. 


364 


The  African  Wild  Dog  •  Estes  and  Goddard        57 


Fig.  4.     Part  of  a  resting  pack,  lying  typically  close  together. 

Hunting   Behavior 

Prelude  to  the  Hunt. — Periods  of  activity 
were  initiated  by  the  actions  of  one  or  a 
few  dogs  apparently  more  restless  than  the 
others;  rarely  did  the  whole  pack  arise 
spontaneously  at  the  start  of  an  activity- 
cycle.  Typically,  one  dog  would  get  up 
and  run  to  a  nearby  group,  nose  the  others 
and  tumble  among  them  until  they  re- 
sponded. Within  a  few  minutes  the  whole 
pack  would  usually  become  active.  But  if, 
as  sometimes  happened,  the  majority  failed 
to  respond  to  the  urging  of  a  few,  then  all 
would  settle  down  to  rest  again.  Sometimes, 
after  a  brief  bout  of  general  activity,  the 
whole  pack  would  lie  down  once  more, 
even  if  it  was  past  the  usual  time  of  hunt- 
ing. 

During  the  first  5  or  10  minutes  after 
rousing,  the  pack  members  sniffed,  urinated, 
defecated,  greeted,  and  romped  together. 
Play  and  chasing  tended  to  become  pro- 
gressively wilder  and  reached  a  climax 
when  the  whole  pack  milled  together  in  a 
circle  and  gave  the  twittering  call  in  unison. 
As  soon  as  this  melee  broke  up,  the  pack 
usually  set  off  on  the  hunt.  Kiihme  (p.  522) 
interprets  this  performance  (specifically 
the  Greeting  ceremony)  as  "a  daily  re- 
peated final  rehearsal  for  the  behavior  at 
the  kill,"  wherein  mutual  dependence  and 
friendliness  are  reinforced  by  symbolic  beg- 
ging, thus  enabling  the  dogs  to  share  the 
kill  amicably,  ^^'hile  this  may  be  one  func- 
tion, the  progressive  buildup  of  excitement 
before  hunting  looked  to  us  like  nothing  so 


much  as  a  "pep  rally,"  that  served  to  bring 
the  whole  pack  to  hunting  pitch.  The  be- 
havior of  domestic  dogs  urging  one  another 
to  set  off  on  a  chase  is  somewhat  similar. 

The  Mobbing  Response. — During  the  mill- 
ing preparatory  to  hunting,  we  sometimes 
saw  what  appeared  to  be  incipient  mob- 
bing action  toward  a  pack  member,  when 
up  to  half  a  dozen  dogs  would  gang  up  on 
one,  tumble  and  roll  it  but  without  actually 
biting  it.  Intensive  play  between  two  or 
three  animals  usually  preceded  and  seemed 
to  trigger  a  mobbing  reaction  in  other  mem- 
bers, who  signaled  their  intentions  by  ap- 
proaching in  the  Stalking  posture.  Percival 
(1924:48)  reports  seeing  a  pack  mob  and 
kill  a  wild  dog  he  had  wounded.  The  oc- 
currence of  "play"  mobbing  suggests  that 
it  could  indeed  become  serious  when  an 
animal  is  maimed.  On  the  other  hand,  sick 
and  crippled  pack  members  are  often  not 
molested:  one  very  sick-looking  old  male  in 
the  large  pack  trailed  behind  the  others 
for  over  a  month  before  recovering,  and 
though  he  kept  usually  a  little  apart,  was 
tolerated  at  kills. 

It  is  significant  that  basically  the  same 
mobbing  behavior,  at  high  intensity,  is  dis- 
played when  wild  dogs  kill  large  prey  and 
when  they  harass  spotted  hyenas,  their 
most  serious  competitor.  It  seems  very 
likely,  in  fact,  that  mobbing  is  an  innate  re- 
sponse which  governs  pack  action  in  hunt- 
ing, killing,  and  mutual  defense.  It  is  per- 
haps the  key  to  pack  behavior  in  all  animals 
that  display  it.    That  mobbing  appears  in 


365 


58        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


play  and  can  be  released  by  a  conspecific  more   than   300   yards   was    generally   not 

which  is  wounded  or  otherwise  transformed  pursued.   As  far  as  we  could  tell,  the  prey 

from  its  normal  self,  supports  the  hypothesis  animal  was  never  singled  out  until  after 

that  it  is  an  innate  response.  It  is  also  note-  the  pack,  or  at  any  rate  the  leader(s),  had 

worthy  that  a  wild  dog  removed  from  its  broken  into  a  run. 

pack  apparently  makes  little  effort  to  defend  In  the  pack  of  21,  juveniles  and  some 
itself  against  attack.  Selous  ( in  Bryden  adults  usually  lagged  far  behind,  and  often 
1936:24)  reported  that  a  wild  dog  caught  caught  up  5-10  minutes  after  the  kill  was 
by  a  pack  of  hounds  shammed  death  and  made.  In  the  small  pack,  however,  corn- 
then  escaped  when  he  was  about  to  skin  it.  monly  all  kept  together  and  spread  out  on 

Hunting  Technique. — Sometimes  the  pack  a  front  during  the  stalking  phase.  When  all 

would  set  off  on  the  hunt  at  a  run  and  started  running  on  a  front,  sometimes  more 

chase    the    first    suitable    prey    that    was  than  one  dog  picked  out  a  quarry  from  the 

sighted.    More  often,  there  was  an  inter-  fleeing  herd,  whereupon  the  pack  might 

val  of  10-20  minutes  during  which  the  dogs  split,    some   following   one    dog,    the   rest 

trotted  along,  played  together,  and  engaged  another.    Kiihme  ( p.  527 )   considered  this 

in  individual  exploratory  activity,  stopping  the  normal  pattern  and  noted  that  often 

to  sniff  at  a  hole  or  a  tuft  of  grass,  then  each  animal  acted  for  itself  in  selecting  a 

running  to  catch  up  with  the  rest.   At  this  quarry  before  all  combined  on  a  common 

stage,  when  the  hunt  had  started  but  before  goal.    In  this  way  the  slowest  prey  tended 

any    common    objective    had    been    deter-  to  be  selected.    Selection  by  this  method 

mined,  individuals  might  forage  for  them-  was  exceptional  for  the  Ngorongoro  pack, 

selves.  The  observer  would  suddenly  notice  which  had  a  definite  leader;  as  a  rule  the 

that  a  dog  was  carrying  part  of  a  gazelle  lead  dog  made  the  choice  and  the  rest  of 

fawn  or  a  young  hare   (Lepus  capensis),  the  pack  fell  in  behind  him.    Nor  did  it 

that  must  have  been  simply  grabbed  as  it  appear  that  any  effort  was  made  to  single 

lay  in  concealment.    Once  during  a  moon-  out  the  slowest  prey,  although  that  would 

light  hunt  by  a  small  pack  that  visited  the  be  difficult  to  observe  clearly. 

Crater  in  1963,  individual  dogs  were  seen  Again  as  a  general  rule,  no  attempt  was 

to  pick  up  at  least  two  gazelle  fawns  and  made  to  carry  out  a  concealed  stalk,  which 

one     springhare     {Pedetes    surdaster),    a  would  in  any  case  be  practically  impossible 

strictly  nocturnal  rodent,  within   V2   hour,  by  daylight  on  the  short-grass  steppe.    But 

Concealed  small  game  such  as  this  is  ap-  on  one  occasion  the  pack  of  six  made  use 

parently  not  hunted  by  the  pack  in  concert,  of  a  tall  stand  of  grass  to  get  near  a  group 

Preparatory  to  the  chase,  there  was  fre-  of  Thomson's  gazelles.  On  another  hunt  the 

quently  a  preliminary  stalking  phase  dur-  pack  apparently  took  advantage  of  a  slight 

ing  which  the  pack  approached  herds  of  elevation  in  the  expectation  of  surprising 

game  at  a  deliberate  walk,  in  the  Stalking  any  game  that  might  be  out  of  sight  on  the 

attitude  (Fig.  2).  The  dogs  appeared  to  be  far  side.    They  moved  deliberately  up  the 

attempting  to  get  as  close  as  possible  with-  slope,  then  broke  into  a  run  and  swept  at 

out  alarming  the  game,  and  certainly  the  full  speed  over  the  crest  on  a  broad  front 

flight  distances  were  much  less  than  when  —but  without  finding  any  quarry  that  time, 

the  pack  appeared  running.  The  chase  was  When  the  leader  had  selected  one  of  a 

launched  the  moment  the  game  broke  into  fleeing  herd,  he  immediately  set  out  to  run 

flight.    But   game  that  began  running  at  it  down,  usually  backed  up  by  one  or  two 


366 


The  African  Wild  Dog  •  Estes  and  Goddard        59 


other  adults  who  maintained  intervals  of 
100  yards  or  more  behind  him,  but  might 
be  left  much  further  behind  in  a  long  chase. 
The  rest  of  the  pack  lagged  up  to  a  mile  in 
the  rear.  Discipline  during  the  chase  was 
so  remarkable  among  all  pack  members 
that  even  gazelles  which  bounded  right  be- 
tween them  and  the  quarry  were  generally 
ignored.  The  average  chase  lasted  3-5 
minutes  and  covered  1-2  miles.  At  top 
speed  a  wild  dog  can  perhaps  exceed  35 
mph,  and  can  sustain  a  pace  of  about  30 
mph  for  several  miles.  Once  when  a  chase 
had  begun  but  no  single  quarry  had  yet 
been  selected,  a  male  in  the  pack  of  21 
broke  away  and  proceeded  to  make  a  5- 
mile  circular  sweep  quite  by  itself,  turning 
on  bursts  of  speed  when  gazelles  bounded 
off  before  him,  but  without  ever  singling 
one  out.  His  average  speed,  as  determined 
by  pacing  him  in  a  vehicle,  was  approxi- 
mately 20  mph. 

In  descriptions  of  wild  dog  hunting 
methods,  much  has  been  made  of  their 
intelligent  cooperation  in  "cutting  comers" 
on  their  prey,  and  particularly  of  their  relay 
running,  with  fresh  dogs  taking  the  place 
of  tired  leaders.  We  concur  that  there  is  a 
basis  for  the  first  idea,  but  we  saw  no  evi- 
dence whatever  to  support  the  contention 
that  wild  dogs  run  in  relays.  The  truth  is 
that  wild  dogs  have  no  need  to  hunt  in 
relays.  The  lead  dog  has  ample  endurance, 
if  not  the  speed,  to  overtake  probably  any 
antelope,  of  which  gazelles  are  among 
the  fleetest.  The  fact  that  other  members 
of  the  pack  are  able  to  cut  comers  on  the 
prey  is  at  least  partly  accounted  for  by  the 
prey's  tendency  to  circle  instead  of  fleeing 
in  a  straight  line.  As  explained  later,  some 
prey  animals  have  a  greater  tendency  than 
others  of  their  species  to  do  this.  Of  course, 
once  overtaken,  even  a  quarry  that  has 
been  running  straight  is  forced  to  start 
dodging   if   it   is    to    avoid   being   caught 


straightaway.  Thus  a  dog  running  not  too 
far  behind  the  leader  is  well  placed  to  cut 
corners  when  the  quarry  changes  course, 
and  it  frequently  happened  that  one  of  the 
followers  made  the  capture.  Most  game, 
after  a  hard  chase  of  a  mile  or  two,  was 
too  exhausted  by  the  time  it  began  dodging 
to  have  any  real  chance  of  evading  its 
pursuers. 

Killing  and  Eating. — Wild  dogs  killed 
small  game  hke  Thomson's  gazelles  with 
amazing  dispatch.  Once  overtaken,  a 
gazelle  was  either  thrown  to  the  ground  or 
simply  bowled  over,  whereupon  all  nearby 
dogs  fell  on  it  instantly.  Grabbing  it  from 
all  sides  and  pulling  against  one  another 
so  strongly  that  the  body  was  suspended 
between  them,  they  then  literally  tore  it 
apart  ( Fig.  5 ) .  It  happened  so  quickly  that 
it  was  never  possible  to  come  up  to  a  kill 
before  the  prey  had  been  dismembered.  If 
it  didn't  go  down  at  once,  dogs  began  tear- 
ing out  chunks  while  it  was  still  struggling 
on  its  feet.  We  once  saw  a  three-quarter 
term  fetus  torn  from  a  Thomson's  gazelle 
within  seconds  of  the  time  it  was  overtaken 
and  before  it  went  down.  As  Kiihme  ob- 
served, there  is  no  specific  killing  bite  as 
in  felids  (Leyhausen  1965).  When  dealing 
with  larger  prey  such  as  juvenile  wildebeest 
and  notably  a  female  kongoni,  the  dogs 
slashed  and  tore  at  the  hind  legs,  flanks, 
and  belly — always  from  the  rear  and  never 
from  in  front — until  the  animal  fell  from 
sheer  exhaustion  and  shock.  They  then 
very  often  began  eating  it  ahve  while  it  was 
still  sitting  up  (Fig.  6).  Self-defense  on 
the  part  of  a  prey  was  never  once  observed; 
the  kongoni,  for  example,  did  little  more 
than  stand  with  head  high  while  the  dogs 
cut  it  to  ribbons,  looking  less  the  victim 
than  the  witness  of  its  own  execution. 

In  eating,  the  dogs  began  in  the  stomach 
cavity,  after  first  opening  up  the  belly,  and 
proceeded  from  inside  out.    Entrance  was 


367 


60 


Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


Fig.  5. 


The  pack  tearing  apart  a  young  gnu  calf. 


also  effected  through  the  anus  by  animals 
unable  to  win  a  place  in  the  stomach  cavity. 
While  several  dogs  forced  their  heads  in- 
side and  ripped  out  the  internal  organs, 
others  quickly  enlarged  the  opening  in 
struggling  for  position.  This  resulted  in 
skinning  out  the  carcass,  leaving  the  skin 
still  attached  to  the  head,  which  was  sel- 
dom touched.  Apart  from  these,  the  back- 
bone and  the  leg  bones,  very  little  of  a 
Thomson's  gazelle  would  remain  at  the 
end  of  10  minutes.  In  the  pack  of  21,  if 
only  part  had  managed  to  eat  their  fill, 
sometimes  the  rest  went  off  to  hunt  again 
before  the  carcass  was  cleaned.  They  pro- 
ceeded to  chase  and  pull  down  another 
gazelle  within  as  little  as  5  minutes  from 
the  time  of  the  previous  kill,  to  be  joined 
shortly  by  the  other  dogs.  As  each  animal 
became  satisfied  it  withdrew  a  little  from 
the  kill  and  joined  others  to  rest,  play,  or 
gnaw  at  a  bone  it  had  taken  along.  Some- 
times the  pack  stayed  at  the  scene  until  the 
next  hunting  period;  more  often  it  with- 
drew to  a  nearby  stream  or  waterhole  and 
settled  down  there.  Kiihme  never  saw  wild 
dogs  drink.  The  Ngorongoro  pack  drank, 
though  irregularly,  before  hunting  and  after 
eating. 


Selection  of  Prey  and  Frequency  of  Kills 

Table  1  summarizes  prey  selection  by 
species,  sex,  and  age  in  50  recorded  kills. 
The  11  wildebeest  calves  were  all  taken  in 
January  during  the  peak  calving  season, 
when  the  pack  of  seven  dogs  apparently 
specialized  on  them;  only  kills  of  calves 
were  seen  by  us  or  reported  by  Crater  visi- 
tors in  this  month.  Thus  the  percentage  of 
calves  in  the  total  gives  a  biased  picture  of 
prey  selection  during  the  rest  of  the  year. 
With  new  calves  excluded,  the  adjusted 
percentages,  based  on  39  kills,  are  as  fol- 
lows: 

Thomson's  gazelles  69  percent 

Juvenile  wildebeest  18  percent 

Grant's  gazelles  10  percent 

Kongoni  one  kill 

Wright  (1960:9)  records  a  similar  pre- 
ponderance  of   Thomson's    gazelles   in    10 


Fig.   6.     Dogs   begin   eating   a  yearling-class  gnu   while   it  is 
still  alive,  but  evidently  in  a  state  of  deep  shock. 


368 


The  African  Wild  Dog  •  Estes  and  Goddard        61 


Table  1.     Prey  selection  by  species,  sex,  and  age  in  50  kills  of  the  African  wild  dog. 


Prey 
Species 


Total 
No. 


Adult 
Males 


Adclt 
Females 


JUVENILE- 
SUBADULT 


Young* 


Percent  of 
Total  Kills 


Thomson's  gazelle 

27 

18 

6 

2 

1 

54 

Wildebeest 

18 

0 

0 

7 

11 

36 

Grant's  gazelle 

4 

1 

1 

2 

0 

8 

Kongoni 

1 

0 

1 

0 

0 

2 

*  Less  than   6   months   old. 


kills  on  the  Serengeti  Plains  (7  Thomson's 
gazelles,  1  wildebeest,  1  impala,  and  1  reed- 
buck  [Redunca  redwica]),  and  notes  that 
it  is  the  staple  diet  of  wild  dogs  in  the 
Serengeti.  Kiihme  also  observed  that  wild 
dogs  prey  mainly  on  Gazella  thomsonii  and 
G.  granti,  and  young  wildebeest  in  the 
Serengeti. 

In  terms  of  actual  preference,  informa- 
tion from  the  Serengeti,  where  the  Thom- 
son's gazelle  is  by  far  the  most  numerous 
herbivore,  is  far  less  revealing  than  the  fig- 
ures from  the  Crater,  where  this  species  oc- 
curs in  relatively  small  numbers.  The  status 
of  the  principal  ungulates  in  Ngorongoro, 
based  on  an  aerial  count  by  Turner  and 
Watson  ( 1964 ) ,  on  two  ground  counts  of 
the  gazelles  by  the  authors  in  collaboration 
with  the  Mweka  College  of  Wildlife  Man- 
agement, and  on  our  ground  counts  of  the 
less  numerous  species,  is  as  follows: 


Wildebeest 

14,000 

Zebra 

5,000 

Thomson's  gazelle 

3,500 

Grant's  gazelle 

1,500 

Eland   {Taurotragus  oryx) 

350 

Waterbuck  {Kobus  defassa) 

150 

Kongoni 

100 

Reedbuck 

100 

(?) 

The  evidence  suggests,  then,  that  Thom- 
son's gazelle  is  the  preferred  prey  of  the 
wild  dog  in  East  African  steppe-savanna. 
In  the  miambo  woodland  (Brown  1965) 
that  extends  from  mid-Tanzania  into  South 
Africa,  where  gazelles  are  not  found,  the 
main  prey  may  be  impala,  followed  by 
other  medium-  to  small-sized  antelopes  and 
the  young  of  large  antelopes.    In  Kruger 


Park,  for  example,  of  88  identified  wild  dog 
kills,  85  percent  were  impala  (Bourliere 
1963).  Stevenson-Hamilton  Hsted  other  prey 
as  reedbuck,  bushbuck  ( Tragelaphus  scrip- 
tiis),  duiker  (Sijlvicapra  grimmia  and  Cephal- 
ophus  spp.),  and  steinbok  (Raphicerus 
campestris),  also  female  waterbuck  and 
kudu  {Tragelaphus  strepsiceros)  when 
pressed  by  hunger.  In  Wankie  Park,  war- 
dens' reports  indicate  a  considerable  toll  of 
young  kudu,  eland,  sable  (Hippotragus 
niger),  and  tsessebe  (Damaliscus  lunatus). 
Instances  where  adult  female  and  even 
adult  male  kudu  were  pulled  down  by  wild 
dogs  are  also  cited. 

Bourliere  states  (1963:21)  that  "Carnivores 
actually  only  prey  upon  herbivores  of  about 
the  same  size  and  weight."  While  this  gen- 
eralization is  open  to  dispute,  it  applies  well 
enough  to  East  African  wild  dogs  preying 
on  Thomson's  gazelles.  Where  the  main 
prey  is  impala,  reedbuck,  etc.  that  weigh  in 
the  100-150  lb  class,  weight  and  size  may 
be  double  or  triple  that  of  the  wild  dog. 
But  the  wild  dogs  of  the  East  African 
steppe-savanna  are  smaller  (also  darker, 
with  more  black  and  less  tan  and  white) 
than  their  counterparts  in  Central  and 
South  African  woodland  (Fig.  7).  The 
average  weight  of  the  animals  we  have  seen 
in  East  Africa  would  not  exceed  40  lb;  the 
members  of  a  pack  seen  in  Wankie  Park,  by 
comparison,  looked  to  be  a  good  3  inches 
taller  and  20  lb  heavier.  This  consistent 
geographic  size  variation  may  be  adapted 
to  size  of  the  principal  prey  species;  specifi- 


369 


62        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


Fig.  7.     Two  specimens  of  the  larger,  lighter-colored  wild  dog  of  southern  Africa,   photographed   in   Wankie   National    Park. 


cally,  wild  dogs  of  the  East  African  plains 
may  be  smaller  as  the  result  of  specializa- 
tion on  Thomson's  gazelle. 

Kill  Frequency. — Because  of  the  difficulty 
of  locating  and  relocating  a  free-ranging 
pack,  our  data  for  consecutive  hunting 
periods  are  inadequate  for  defining  the  aver- 
age kill  frequency  and  average  food  intake 
per  animal  per  day.  Even  when  the  pack 
was  observed  during  the  two  daily  hunting 
periods,  it  was  rarely  certain  that  it  had 
not  killed  before,  after,  or  between  these 
periods.  Nonetheless,  because  this  type  of 
information  is  badly  needed,  data  covering 
consecutive  hunting  periods  are  presented 
in  Table  2  as  a  rough  average  of  kill  fre- 
quency and  meat  available  per  animal  per 
day. 

The  average  frequency  of  two  kills  per 
day  derived  from  the  data  for  consecutive 
hunting  periods  agrees  with  our  general  ob- 
servation that  the  pack  usually  killed  dur- 
ing each  period.  To  demonstrate  this,  on 
28  hunts  the  pack  performed  as  follows: 


Chases 

29 


Kills 
25 


Failures 

4 


Did  not   chase 

5 


This  indicates  a  success  rate  per  chase  of 
over  85  percent.  As  a  further  indication  of 
efficiency   in   locating   and   running   down 


prey  where  game  is  plentiful,  on  eight  oc- 
casions when  the  dogs  were  watched  from 
the  moment  they  left  their  resting  place  to 
the  moment  they  killed,  the  mean  time  was 
only  25  minutes,  with  a  range  of  15-45  min- 
utes. On  five  other  occasions  the  pack 
failed  to  hunt  seriously  during  the  normal 
period;  this  was  offset  in  the  above  figures 
by  five  periods  during  which  the  dogs 
chased  and  killed  twice.  The  possibility 
that  hunting  activity  and  success  might  be 
reduced  after  having  killed  larger  or  more 
than  one  of  the  usual  prey  is  not  borne  out 
by  the  six  instances  when  the  pack  was  ob- 
served during  the  next  hunting  period:  in 
four  cases  the  pack  killed  again.  There  are 
some  grounds  for  asserting,  then,  that  wild 
dogs  kill  twice  daily  regardless  of  what 
their  prey  may  be.  Certainly  they  do  not 
feed  more  than  once  from  the  same  kill,  at 
least  not  in  Ngorongoro  Crater,  where  the 
numerous  scavengers  dispose  of  all  left- 
overs in  very  short  order. 

Meat  Available  per  Animal  per  Day. — 
The  amount  of  meat  available  per  wild  dog 
per  day  works  out  at  roughly  6  lb,  assuming 
that  40  percent  of  the  prey  animal  consists 
of  inedible  or  unpalatable  bone,  skin,  and 
stomach  contents.  Wright's  ( 1960 )  calcula- 
tion of  0.15  lb  of  food  per  day  per  pound 


370 


The  African  Wild  Dog  •  Estes  and  Goddard        63 


Table  2.     Kill  frequency  and  meat  available  per  dog  per  day,  based  on  observations  of  consecutive  hunting  cycles. 


Avail- 

Est. Wt. 

No.   IN 

able* 

Meat/ 

Date 

Prey 

(LB) 

Pack 

Meat/ 
Dog 

Dog/Day 

1964 
Sept.  30 
Oct.   1 

Nov.  11 

Nov.  12 

Nov.  27 

Nov.  28 

Dec.  5   (pm) 

to 
Dec.  7   (aai) 

1965 

Jan.  17   (pm) 

to 
Jan.  19   (am) 
July  16 


Juvenile  wildebeest 
Thomson's  gazelle   (adult  M) 
M  .,        (adult  F) 

Thomson's  gazelle   (adult  F,  including  fetus) 
2  Thomson's  gazelles   (adult  F) 
Thomson's  gazelle   (adult  M) 
Kongoni  (adult  F) 
2  Thomson's  gazelles   ( adult  M ) 
Thomson's  gazelle   (subadult  M) 
Grant's  gazelle   (subadult  F) 
Thomson's  gazelle  ( adult  M ) 
2  Thomson's  gazelles   ( adult  M ) 

Thomson's  gazelle   (juv.  M) 
4  wildebeest  calves 


2  Thomson's  gazelles   ( adult  M ) 


125 

21 

3.6 

60 

21 

1.7 

40 

21 

1.1 

50 

21 

1.4 

80 

21 

2.2 

60 

21 

1.7 

250 

21 

7.4 

120 

21 

3.4 

50 

21 

1.4 

90 

21 

2.6 

60 

21 

1.7 

120 

12 

6.0 

40 


180 


120 


21 


6 


1.1 


15.5 


12.0 


3.6 


2.8 


3.6 


9.1 


4.8 


4.3 


3.5 


7.8 


12.0 


Kill  frequency  =  2  kills/day. 

Meat  available  per  dog  per  day:    combined  average  =  6  lb;  for  pack  of  21  =  4.5  lb;  for  pack  of  7-6 


9  lb 


*  A\ailable  meat  is  based  on  60  percent  of  carcass  weight. 

of  dog  also  works  out  to  6  lb  per  day  if  the 
average  weight  of  a  dog  is  taken  as  40  lb, 
but  his  figures  are  based  on  the  total 
weight  of  the  prey.  In  either  case,  two  to 
three  times  as  much  food  per  day  is  avail- 
able to  wild  dogs  as  is  given  to  domesti- 
cated dogs  of  the  same  size.  However,  the 
number  of  dogs  in  the  pack  is  an  important 
factor.  When  there  were  21  dogs,  the 
amount  of  meat  available  per  day  was  less 
than  5  lb  per  animal;  in  the  pack  of  7  and 
6,  each  animal  had  approximately  twice  as 
much  available  meat.  Since  the  small  packs 
killed  at  the  same  rate,  large  packs  are  un- 
doubtedly less  wasteful. 

Reactions  of  Prey  Species 

The  reactions  of  game  depended  on  the 
behavior  of  the  wild  dog  pack.  When  the 
pack  was  at  rest,  all  game  would  graze  un- 
concernedly within  150  yards.    When  the 


dogs  were  walking  or  trotting,  potential 
prey  would  stand  until  approached  within 
350-250  yards,  or  less  if  the  pack  was  not 
headed  directly  toward  them.  When  stalked, 
gazelles  often  stood  watching  until  the  pack 
came  within  3(X)-2(X)  yards.  But  when  the 
pack  was  running,  gazelles,  and  wildebeest 
herds  containing  young,  often  acted  alarmed 
at  a  distance  of  500  yards,  although  again, 
individual  animals  not  directly  in  the  ap- 
proach line  might  let  the  pack  go  by  as 
close  as  150  yards. 

Gazelles. — The  moment  a  running  wild 
dog  pack  appeared  on  the  plain,  both  ga- 
zelle species  immediately  reacted  by  per- 
forming the  stiff-legged  bounding  display, 
with  tail  raised  and  white  rump  patch  flash- 
ing, called  Stotting  or  Pronking.  Un- 
doubtedly a  warning  signal,  it  spread  wave- 
like in  advance  of  the  pack.  Apparently  in 
response  to  the  Stotting,  practically  every 


371 


64        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


gazelle  in  sight  fled  the  immediate  vicinity,  cially  territorial  bulls,  show  little  fear  of 

Adaptive   as   the   warning   display   may  wild  dogs,  which  is  a  good  indication  that 

seem,   it  nonetheless   appears   to   have  its  they  have  little  reason  to  fear  them  under 

drawbacks;  for  even  after  being  singled  out  normal  circumstances  (Fig.  8).  While  even 

by  the  pack,  every  gazelle  began  the  run  territorial  males  will  get  out  of  the  way  of 

for  its  life  by  Stotting,  and  appeared  to  lose  a    running   pack,    they   rarely   leave    their 

precious  ground  in  the  process.  Many  have  grounds,  but  merely  trot  to  one  side  and 

argued  that  the  Stotting  gait  is  nearly  or  turn  to  stare  as  the  pack  goes  by.  Bulls  not 

quite  as  fast  as  a  gallop,  at  any  rate  decep-  infrequentiy  act  aggressively  toward  walk- 

tively  slow.    But  time  and  again  we  have  ing  or  trotting  dogs,  and  may  even  make  a 

watched  the  lead  dog  closing  the  gap  until  short  charge  if  the  dogs  give  ground.    In 

the  quarry  settled  to  its  full  running  gait,  Rhodesia  we  have  seen  a  pack  of  the  larger 

when  it  was  capable  of  making  slightly  bet-  variety  of  wild  dogs  chased  by  females  and 

ter  speed  than  its  pursuer  for  the  first  half  yearlings    of   the   blue    wildebeest    (C.    t. 

mile  or  so.    It  is  therefore  hard  to  see  any  taurinus)  which  is  also  larger  and  perhaps 

advantage  to  the  individual  in  Stotting  when  generally  more  aggressive  than  the  Western 

chased,  since  individuals  that  made  no  dis-  wliite-bearded    gnu.     But   like    zebras,   all 

play  at  all  might  be  thought  to  have  a  bet-  wildebeest  will  on  occasion  follow  behind 

ter  chance  of  surviving  and  reproducing,  walking  or  trotting  dogs,  apparently  moti- 

On  theoretical  grounds,  then,  it  has  to  be  vated  by  curiosity,  just  as  they  will  gather 

assumed  that  the  Stotting  display  offers  an  to  stare  at  and  follow  lions  ( Panthera  leo ) . 

individual  selective  advantage  which  simply  In  hunting  wildebeest,  wild  dogs  are  ob- 

remains  to  be  determined.   Nor  is  this  type  viously  highly  selective.   Having  walked  in 

of  display  confined  to  the  gazelles:  during  the  Stalking  attitude  to  within  several  hun- 

the  aforementioned  kongoni  chase,  all  six  dred  yards  or  less  and  then  run  into  the 

members  of  the  herd  began  Stotting  when  midst  of  a  large  concentration,  the  pack 

the  wild  dog  pack  first  headed  in  their  di-  sphts  up  and  works  through  it,  approaching 

rection,  and  the  victim  continued  to  Stot  for  one  gnu  after  another  only  to  turn  away  if 

some  time  after  being  singled  out.  it  proves  adult.    Meanwhile  the  wildebeest 

Table  1   shows  that  67  percent  of  the  mill  and  run  in  all  directions,  without  ever 

Thomson's  gazelles  killed  were  adult  males,  making  any  effort  to  form  a  defensive  ring 

This  is  evidently  the  result  of  territorial  be-  — even  when  young  calves  are  present.   A 

havior.   Because  of  attachment  to  territory,  defensive  ring  has  been  reported  in  some 

probably    coupled    with    inhibition    about  of  the  wild  dog  literature.  Kiihme  (p.  528) 

trespassing  on  the  grounds  of  neighboring  observed   something   of   the    sort   in   large 

rivals,  territorial  males  tend  to  be  the  last  Serengeti  concentrations,  though  they  did 

to  flee  from  danger.    Moreover  they  show  not    form    any    regular    ring    but    simply 

a  greater  tendency  to  circle  back  toward  crowded  together  in  a  milling  mass.    Indi- 

home,  and  these  two  traits  together  make  vidual  females,  on  the  other  hand,  defend 

them  more  vulnerable  to  wild  dog  preda-  their  calves  after  being  overtaken  in  flight, 

tion  than  other  members  of  the  population.  Against  a  pack,  however,  one  wildebeest 

The  same  tendencies  are  displayed  by  fe-  cannot  put  up  any  effective  defense;  while 

males  with  young,  concealed  fawns,  making  it  confronts  one  or  two,  the  rest  go  around 

them  also  more  vulnerable.  and  seize  the  calf. 

Wildebeest. — Adult  wildebeest,  espe-  Zebra. — The  only  other  herbivore  whose 


372 


The  African  Wild  Dog  •  Estes  and  Goddard 


65 


Fig.  8.     Adults,  and  even  a  yearling  gnu   (4th  from  left)   show  little  fear  of  running  wild  dogs,   though   they  ran  out  of  the 
way   immediately  after  the   picture  was  taken.     The   quarry   is  a  young  calf,  visible  as  a  light  spot  in  the  upper  left. 


reactions  to  wild  dogs  we  observed  in  de- 
j  tail,  zebras  are  the  least  concerned  about 
them,  and  do  not  hesitate  to  attack  dogs 
that  come  too  close.  Wild  dogs  on  their 
part  rarely  stand  up  to  them.  Since  the 
members  of  a  harem  would  probably  co- 
operate with  the  herd  stallion  to  defend  the 
foals,  it  would  appear  that  wild-dog  preda- 
tion  on  zebra  is  quite  rare. 

Relations  with  Other  Predators  and 
Scavengers 

Vultures. — Since  wild  dogs  customarily 
kill  in  early  morning  and  late  afternoon,  the 
larger  vultures,  the  white-backed  (Pseu- 
dogyps  africanus) ,  Riippells  griffon  (Gyps 
riippelJi),  and  lappet-faced  (Torgos  trache- 
liotus),  whose  activities  are  largely  regu- 
lated by  the  presence  or  absence  of  thermal 
updrafts,  benefit  rather  little  from  their  pre- 
dation.  Large  vultures  were  more  likely  to 
appear  at  afternoon  than  morning  kills.  But 
the  two  smallest  species,  the  hooded  and 


Egyptian  vultures  (Necrosyrtes  motwchus 
and  Neophron  perenopterus) ,  were  regu- 
larly to  be  found  at  wild-dog  kills,  a  good 
hour  before  other  scavengers  were  even  air- 
borne. In  addition  to  these  vultures,  other 
regularly  encountered  scavengers  included 
the  tawny  eagle  (Aquila  rapax)  and  the 
kite  [MUxjus  migrans),  while  the  uncom- 
mon white-headed  vulture  (Trigonoceps 
occipitalis),  the  bateleur  eagle  (Terathopius 
ecaudatus),  and  Cape  rook  (Corvus  capen- 
sis)  showed  up  infrequently. 

On  several  occasions  hooded  vultures 
were  seen  following  a  chase  and  landing 
before  the  prey  had  even  been  pulled  down, 
shortly  after  full  daylight.  Aside  from  glean- 
ing bits  and  pieces  around  the  kill,  vultures 
had  to  wait  until  the  dogs  left  before  they 
could  feed  on  the  carcass.  But  the  kite  suc- 
cessfully stole  small  pieces  from  the  dogs 
by  swooping,  grabbing,  and  mounting  again 
to  eat  on  the  wing.  Although  young  ani- 
mals sometimes  stalked  and  ran  at  vultures 


373 


66        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


that  approached  close  to  the  kill,  the  dogs  stools  they  found,  and  coming  dangerously 

were  generally  tolerant  toward  avian  scav-  close,  to  stand  staring  with  their  short  tails 

engers.  twitching — a  sign  of  nervousness.    Kiihme 

Jackals. — The  Asiatic  jackal  (Canis  (p.  534)  reports  an  instance  in  which  a 
aureus)  was  seen  more  frequently  at  kills  hyena  even  touched  a  resting  wild  dog's 
than  the  black-backed  jackal  (C.  meso-  face,  meanwhile  "whining  friendly."  Such 
melas).  Since  the  latter  seemed  to  predomi-  boldness,  particularly  near  the  time  when 
nate  at  nocturnal  kills  by  lions  or  hyenas,  the  pack  was  becoming  active,  often  trig- 
it  may  be  that  one  is  more  nocturnal  and  gered  the  Mobbing  response, 
one  more  diurnal  in  its  habits.  Also,  the  Hyenas,  which  weigh  up  to  150  lb,  would 
Asiatic  jackal  tended  to  behave  more  boldly  be  more  than  a  match  for  wild  dogs  if  they 
and  aggressively  at  kills.  It  would  move  had  the  same  pack  (mobbing)  instinct, 
closer  to  a  feeding  pack  of  dogs  and  take  Lacking  it,  they  are  nearly  defenseless 
advantage  of  any  opportunity  to  steal  meat,  against  a  wild  dog  pack.  With  three  to  a 
When  threatened  by  a  dog,  a  little  15-lb  dozen  dogs  worrying  its  hindquarters,  the 
jackal,  coat  fluffed,  head  down,  and  snarl-  best  a  hyena  can  do  is  to  squat  down  and 
ing,  would  stand  its  ground  and  snap  fero-  snap  ineffectively  over  its  shoulder,  while 
ciously  if  the  dog  continued  to  advance,  voicing  loud  roars  and  growls.  On  rare  oc- 
Although  it  was  pure  bluff  that  quickly  casions  a  hard-pressed  one  would  simply  lie 
ended  in  flight  if  a  dog  attacked  in  earnest,  down  and  give  up;  a  hyena  we  once  saw 
it  proved  a  surprisingly  effective  intimida-  crowded  by  a  persistently  curious  group  of 
tion  display  in  most  encounters.  But  on  the  juvenile  wildebeest  did  the  same  thing.  The 
whole,  wild  dogs  behaved  almost  as  toler-  spotted  hyena  seems  on  the  whole  to  be 
antly  toward  jackals  as  toward  vultures.  notably  timid  by  nature,  as  may  be  judged 

Spotted  Hyenas. — Spotted  hyenas,  on  the  from  the  fact  that  mothers  will  often  not 

other   hand,    seriously    compete    with    the  even  defend  their  offspring.    Yet  they  are 

dogs  for  their  kills,  attempting  to  play  a  driven  by  hunger  to  take  incredible  and 

commensal  role   against   active  resistance,  sometimes  fatal  risks. 

In  a  place  like  the  Crater,  with  an  excep-  Often,  as  under  the  above  circumstances, 
tionally  large  hyena  population  for  such  a  they  provoked  attack  by  their  own  rash- 
small  area,  numbering  some  420  adults  ness.  But  in  other  cases  the  dogs  seemed 
(Kruuk  1966:1258),  it  is  probably  safe  to  to  go  out  of  their  way  to  harry  hyenas  en- 
say  that  wild  dogs  hunting  singly  or  in  twos  countered  during  the  early  stages  of  a  hunt, 
and  threes  would  very  frequently  lose  their  Those  unwary  enough  to  let  the  pack  get 
kills  to  hyenas,  since  this  happened  oc-  close  could  still  usually  get  off  entirely  by 
casionally  even  to  the  pack  of  21.  cowering  down  and  lying  still.    But  those 

Hyenas  actually  stayed  near  the  resting  that  stayed  until  the  pack  was  close  and 

pack  for  hours  at  a  time,  evidently  waiting  then  ran  away  were  inviting  pursuit  and  a 

for  a  hunt  to  begin.   It  was  not  unusual  to  good  mauling.    At  the  same  time,  hyenas 

see  one  or  more  of  them  slowly  approach  a  following  behind  the  pack  were  generally 

group  of  dogs,  then  crawl  to  within  a  few  ignored.  On  one  notable  occasion,  the  pack 

yards  and  lie  gazing  at  them  intently,  as  of  21  took  it  in  turns  to  mob  the  hyenas  it 

though  urging  them  to  get  started.    Often  happened  upon  in  a  denning  area  inhabited 

several    would    wander    between    resting  by  more  than  30  adults  and  cubs,  many 

groups,  sniffing  the  ground,  consuming  any  of  which  were  foregathered  as  usual  prior 


374 


The  African  Wild  Dog  •  Estes  and  Goddard        67 


to  the  evening  foraging.  What  was  most 
surprising  was  that  none,  on  this  or  any 
other  occasion,  attempted  to  take  refuge 
underground.  When  hard-pressed,  even 
half-grown  pups  bolted  into  nearby  dense 
streamside  vegetation,  where  the  dogs  did 
not  follow.  But  presumably  young  pups 
were  hidden  in  the  dens,  since  one  lactating 
female  was  reluctant  to  quit  the  immediate 
vicinity.  She  was  repeatedly  mobbed.  Set 
upon  by  five  or  six  dogs  at  a  time,  she 
would  maintain  a  squatting  defense  as  long 
as  she  could  bear  it,  then  break  free  to  race 
for  the  nearest  hole.  Instead  of  going  down 
it  or  backing  into  it,  she  threw  herself  into 
cup-shaped  depressions  next  to  the  holes, 
which  may  or  may  not  have  been  excavated 
by  the  hyenas  themselves  ( territorial  wilde- 
beest also  dig  these  depressions  by  pawing 
and  horning  the  earth ) .  In  these  she  lay  flat 
and  tried  to  defend  herself  from  the  dogs, 
to  whom  only  her  back  and  head  were  ex- 
posed, while  keeping  up  a  steady  volume 
of  roars,  growls,  and  staccato  chuckles. 
Eventually  she  also  took  refuge  in  the 
bushes.  Neither  this  hyena  nor  the  next, 
which  the  dogs  turned  on  its  back  and 
mauled  for  2  minutes,  bore  any  visible 
wounds.  In  fact,  we  have  never  known  the 
dogs  to  kill  or  even  seriously  injure  one. 
Either  hyenas  have  exceedingly  tough  hides 
or  else  wild  dogs  are  less  in  earnest  about 
mobbing  them  than  might  appear. 

Yet  the  degree  to  which  hyenas  are  able 
to  capitalize  on  wild-dog  predation  for  their 
own  benefit  would  justify  a  deep  antago- 
nism. They  frequently  drive  away  the  last 
dogs  on  a  kill  unless  the  rest  of  the  pack 
remains  close  by,  and  are  quite  capable  of 
taking  meat  away  from  one  or  two  dogs  only 
a  few  yards  removed  from  a  kill  where  the 
rest  are  feeding.  A  more  extraordinary 
example  of  this  exploitation  is  the  way 
hyenas  take  advantage  of  the  wild  dog's 
hunting  technique:  in  the  final  moments  of 


Fig.  9.  Hyenas  appropriate  a  wild  dog  prey  and  begin  eat- 
ing it  alive,  while  one  of  two  dogs  that  caught  it  looks  on, 
panting  heavily  from  the  chase.  Hyena  in  foreground  is 
half-grown.  As  shown  in  Fig.  6,  the  dogs  reclaimed  their 
prey  when  the  rest  of  the  pack  arrived. 


a  chase,  when  only  one  or  a  few  dogs  are 
close  to  the  quarry,  hyenas  have  an  oppor- 
tunity to  appropriate  it  before  the  rest  of 
the  pack  arrives  (Fig.  9).  They  attempted 
this  with  considerable  regularity  in  the 
Crater,  and  we  succeeded  in  recording  one 
instance  on  film.  In  some  cases  it  was  a 
matter  of  chance  that  hyenas  were  near 
enough  the  scene  of  the  capture  to  dash  in 
at  the  decisive  moment;  in  others  up  to 
three  or  four  actually  took  part  in  the  chase 
from  the  beginning.  Tliough  not  as  fast  as 
the  dogs,  they  were  able  to  be  in  a  position 
to  intercept  the  quarry  if  it  doubled  back, 
or  to  grab  it  away  from  the  dog(s)  as  soon 
as  it  was  caught.  When  only  two  or  three 
of  them  were  on  hand,  the  dogs  hesitated 
to  launch  an  immediate  counterattack,  par- 
ticularly if  more  than  one  hyena  was  in- 
volved. But  usually  other  pack  members 
quickly  appeared,  joined  together  to  mob 
the  hyenas,  and  forced  them  to  surrender 
the  kill. 

But  sometimes  the  dogs  were  defeated 
by  sheer  numbers.  Once  when  the  leader 
of  the  pack  of  21  had  pulled  down  a  juve- 
nile wildebeest  in  a  hyena  denning  area, 


375 


68        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


some  40  hyenas  closed  in  on  the  kill  before  5.    The  provision  of  food  for  infants  at 

the  others  could  gather.  Apparently  intimi-  the  den  and  the  adults  that  remain  with 

dated  by  so  many  competitors,  the  dogs  re-  them  when  the  pack  is  hunting,  and  for 

venged  themselves  by  mobbing  stragglers,  juveniles  and  sick  or  old  adults  unable  to 

punishing  them  savagely.    Twenty  minutes  kill  for  themselves, 
later,   while   they    were   ranging   for   new 

prey,  the  hyenas  pulled  down  an  adult  fe-  Effective  Pack  Size 

male  wildebeest  on  their  own,  quite  near  We  have  presented  evidence,  though  ad- 

the  first  kill.    Their  clamor  drew  the  dogs  mittedly  tentative,  that  large  packs  utilize 

back  to  the  scene.    But  they  did  nothing  prey  resources  more  efficiently  than  small 

this  time  but  look  on — there  were  now  60  packs,  with  less  waste.    Competition  from 

hyenas!  hyenas,   where   they   are   numerous,   must 

exert  a  strong  selective  pressure  in  favor  of 

CONCLUSIONS  large  packs  as  well  as  for  close  cooperation 

n     ,    n       X-  at  kills.    While  the  observed  tendency  for 

Pack  Function  „         ,          ,           ,                  i        .      i 

small  packs  to  keep  closer  together  m  the 

Hunting  is  undoubtedly  the  primary  func-  ^j^^^^  ^^^  ^^  ^^^^  ^^^j^  ^^^^  ^^  compen- 

tion  of  the  free-ranging  pack.  Wild-dog  be-  ^^^^  somewhat  for  low  numbers,  there  must 
havior  is  highly  specialized  and  adapted  for  ^^  ^  minimum  below  which  competition 
pack  life  by  dint  of  the  equal  and  excep-  f^.^^  j^y^^^^^  ^^^  reduced  hunting  and  kill- 
tionally  friendly  relations  between  individ-  .^^  capability,  would  become  a  serious 
uals,  subordination  of  individual  to  group  i.^^dicap.  From  our  observations  of  both 
activity,  disciphne  during  the  chase,  and  j^^.^^  ^^^  ^^^jj  p^^j,^^  ^^^^  ^^  ^-^  ^^^1^ 
close  cooperation  in  killing  prey  and  mutual  ^^^^  ^j^^^  ^^  ^^^  minimum  effective  unit, 
defense.  It  may,  in  fact,  be  seriously  ques-  ^^  helieve  that  wherever  wild  dogs  are 
tioned  whether  a  single  wild  dog  could  sur-  ^^^^^^^  ^o  such  small  packs,  their  ability 
Vive  for  long  on  its  own.  As  demonstrated  ^^  ^^^^.^^  ^^^  reproduce  may  be  endan- 
by  the  successful  rearing  of  a  litter  after  the  ^^^^^  j^.^  -^  ^^^  ^^^-^^  -^^^  account  the 
mother  died,  feeding  and  protection  of  the  possibility  of  a  differential  birth  or  mor- 
young  is  another  important  pack  function.  ^^^^^  ^^^^  ^^at  results  in  a  low  ratio  of  fe- 
The  main  selective  advantages  of  the  pack  ^^^^j^^  j^  -^  represents  a  pathological  con- 
hunting  unit  may  be  summarized  as  follows:  ^i^i^^^    ^bis    alone    could    mean    that    the 

1.  Increased  probability  of  success  species  is  in  serious  trouble;  a  prompt  in- 
through  cooperation,  hence  better  oppor-  vestigation  of  reproduction  and  neonatal 
tunity  to  eat  regularly  at  less  cost  in  indi-  mortality  is  called  for  to  find  out  to  what 
vidual  effort  extent  an  abnormally  low  percentage  of  fe- 

2.  More  efficient  utilization  of  food  re-  males  may  be  responsible  for  the  apparent 
sources  decline   of  the   species  in   many  parts   of 

3.  Less  disturbance  of  prey  populations  Africa, 
than  would  result  if  each  animal  hunted 
individually  ^'^V  Relations 

4.  Mutual  protection  against  competitors  It  seems  clear  that  wild  dogs  are  highly 
( spotted  hyenas )  and  possible  predators  selective  in  the  species  they  prey  upon,  spe- 
( hyena,  leopard  [Panthera  pardus],  and  ciahzing  in  East  African  steppe-savanna  on 
hon)  Thomson's    gazelles,    and    on    wildebeest 


376 


The  African  Wild  Dog  •  Estes  and  Goddard        69 


calves  during  the  gnu  calving  season.  Con- 
sidering their  selectivity,  their  rate  of  killing, 
and  the  observed  reactions  of  herbivores  to 
them,  it  can  only  be  concluded  that  wild 
dogs  are  by  no  means  so  wantonly  destruc- 
tive or  disruptive  to  game  as  is  commonly 
supposed.  Kiihme  reached  the  same  con- 
clusion (p.  528).  Indeed,  until  one  comes 
to  realize  that  plains  game  simply  has  no 
place  to  hide  and  no  sanctuary  where 
predators  cannot  follow,  it  is  a  recurrent 
surprise  to  note  how  short-lived  and  local- 
ized are  disturbances  due  to  predation. 

In  a  prey  population  as  small  as  that  of 
Thomson's  gazelles  in  Ngorongoro,  if  one 
assumes  an  average  annual  recruitment 
rate  of  roughly  10  percent,  predation  at  the 
rate  of  only  one  a  day  obviously  would  re- 
duce the  population  if  maintained  over  a 
long  period.  There  was,  however,  no  evi- 
dence that  the  Thomson's  gazelle  popula- 
tion declined  after  wild  dogs  became  resi- 
dent in  the  Crater;  our  gazelle  censuses  in 
October,  1964,  and  May,  1965,  showed  no 
reduction  that  could  not  be  accounted  for 
by  simple  counting  errors.  Even  an  actual 
reduction  would  have  no  relevance  to  the 
overall  situation,  as  Thomson's  gazelles  are 
the  most  numerous  herbivores  in  their  cen- 
ters of  distribution  (the  steppe-savanna 
from  central  Kenya  to  north-central  Tan- 
zania). On  the  Serengeti  Plains,  where  the 
gazelle  population  is  estimated  at  800,000 
and  there  are  probably  fewer  than  500  wild 
dogs,  predation  by  this  species  could  have 
no  appreciable  effect.  Indeed  wild  dogs  are 
only  one  of  nine  predators  on  the  Thom- 
son's gazelle  (Wright  1960),  and  not  the 
most  important  one  at  that;  jackals,  which 
are  numerous  and  specialize  in  catching 
new  fawns,  are  probably  the  main  predators. 

Since  wild  dogs  are  nowhere  numerous 
and  everywhere  apparently  specialize  on 
the  most  abundant  small  to  medium-sized 
antelopes,  it  can  be  argued  that  more,  not 


fewer,  of  them  are  needed.  The  population 
explosion  of  impala  in  Kruger  National 
Park  and  many  other  places  where  wild 
dog  numbers  have  declined  offers  convinc- 
ing evidence.  The  high  percentage  of  ter- 
ritorial males  in  wild  dog  kills  of  Thomson's 
gazelles  offers  a  more  subtle  example  of 
how  predation  may  benefit  a  prey  species: 
in  "probably  every  gregarious,  territorial 
antelope  species,  there  is  always  a  surplus 
of  fit,  adult  and  young-adult  males  which 
cannot  reproduce  for  want  of  enough  suit- 
able territories,  so  that  the  removal  of  ter- 
ritorial males  by  predation  is  of  perhaps 
major  importance  in  opening  up  territories 
for  younger  and  sexually  more  vigorous 
males. 

In  our  judgment,  the  wild  dog  is  an  in- 
teresting, valuable  predator  whose  con- 
tinued survival  may  be  endangered.  We 
feel  it  should  be  strictly  protected  by  law 
in  all  African  states  where  it  occurs,  and 
that  it  should  be  actively  encouraged,  if 
this  is  possible,  in  every  park  and  game  re- 
serve. 

LITERATURE  CITED 

BouRLiERE,  C.  F.     1963.     Specific  feeding  habits 

of  African  carnivores.    African  Wild!.  17(1): 

21-27. 
Brown,  L.     1965.    Africa,  a  natural  history.   Ran- 
dom House,  New  York.    299pp. 
Bryden,  H.  a.     1936.     Wild  life  in  South  Africa. 

George  G.  Harrap  Co.  Ltd.,  London.    282pp. 
Haltenorth,  T.     1963.     Klassifikation  der  Sauge- 

tiere:    Artiodactyla.     Handbuch   Zool.    Bd.    8. 

167pp. 
Kruuk,  H.     1966.    Clan-system  and  feeding  habits 

of  spotted  hvaenas  {Crocuta  crocttta  Erxleben). 

Nature  209  ( 5029) :  1257-1258. 
KiJHME,  W.     1965.     Freilandstudien  ziir  Soziologie 

des   Hyanenhundes.    Zeit.   Tierpsych.   22(5): 

495-541. 
Leyhausen,  p.     1965.     tjber  die  Funktion  der  rela- 

tiven    Stimmungshierarchie.     Zeit.    Tierpsych. 

22(4):395-^12. 
Maberly,  C.  T.  Astley.     1962.     Animals  of  East 

Africa.  Howard  Timmins,  Cape  Town.  221pp. 
Mackworth-Praed,  C.  W.,  and  C.  H.  B.  Grant. 

1957.      Birds    of    eastern    and    north    eastern 

Africa.     Series   I,    Vol.    I.     African   handbook 


377 


70        Journal  of  Wildlife  Management,  Vol.  31,  No.  1,  January  1967 


of  birds.    Longmans,  Green  and  Co.,  London.  of  game   in   Ngorongoro  Crater.    E.   African 

806[+40]pp.  Wildl.  J.  2:165-168. 

Percival,  a.   B.      1924.     A  game  ranger's  note-  Vaughan-Kirby,  F.     1899.     The  hunting  dog.  Pp. 

book.    Nisbet  &  Co.,  London.    374pp.  602-606.    In  H.   A.   Bryden    (Editor),  Great 

Selous,  F.  C.     1881.     A  hunter's  wanderings  in  and   small   game   of   Africa.     R.    Ward   Ltd., 

Africa.    R.  Bentley  &  Son,  London.    455pp.  London.    612pp. 

Stevenson-Hamilton,    J.      1947.      Wild    life    in  Wright,  B.  S.     1960.     Predation  on  big  game  in 

South  Africa.    Cassell  &  Co.,   Ltd.,   London.  East  Africa.    J.  Wildl.  Mgmt.  24(1):1-15. 

343pp. 

Turner,  M.,  and  M.  Watson.     1964.     A  census  Received  for  publication  March  21,  1966. 


378 


Novejnber,  1957  GENERAL  NOTES  519 


HOMING  BEHAVIOR  OF  CHIPMUNKS  IN  CENTRAL  NEW  YORK 

Homing  movements  ranging  from  about  150  to  700  yards  have  been  recorded  for  Tamias 
by  Seton  (life  histories  of  northern  animals,  vol.  1:  341,  1909),  Allen  (BuU.  N.  Y. 
State  Mus.,  314:  87,  1938),  Burt  (Misc.  Publ.  Mus.  Zool.  Univ.  Midi.,  45:  45,  1940),  and 
Hamilton  (  American  mammals,  p.  283,  1939 ) .  While  engaged  in  other  studies  during  the 
summer  of  1952,  I  had  the  opportunity  of  making  additional  observations  on  the  homing 
behavior  of  the  eastern  chipmunk,  Tamias  striatus  lysieri  (Richardson),  on  the  campus  of 
Cornell  University  at  Ithaca,  Tompkins  County,  New  York. 

Live-trapping  was  conducted  from  July  26  to  August  3  in  a  tract  of  approximately  3  acres 
of  hemlock  and  mixed  hardwood  forest  bordering  a  small  artificial  lake.  A  maximum  of  12 
traps  was  employed.  The  chipmunks  taken  were  sexed,  aged  (subadult  or  adult),  marked 
by  cUpping  patches  of  fur  on  various  parts  of  the  body,  and  transported  in  a  cloth  bag  to  one 
of  six  release  points.  The  latter  were  situated  in  similar  continuous  habitat  or  in  an  area 
of  campus  buildings,  lawns,  shrubbery,  and  widely  spaced  trees  adjacent  to  the  woodland. 
An  individual  was  considered  as  having  homed  when  it  was  retaken  within  115  feet  of  the 
original  point  of  capture.  Those  chipmunks  that  returned  and  were  recaptured  were  im- 
mediately released  again  in  a  different  direction  and  usually  at  a  greater  distance.  First 
releases  averaged  675  feet  (310-1,160)  and  second  ones,  1,015  feet  (500-1,570).  Two 
animals  that  returned  after  second  removals  were  liberated  for  a  third  time  at  distances  of 
1,130  and  2,180  feet.  All  distances  given  are  calculated  from  the  station  where  the  animal 
was  originally  trapped.  Since  the  mean  home  range  size  of  chipmunks  in  this  vicinity  has 
been  calculated  as  about  .28  acre  (Yerger,  Jour.  Mamm.,  34:  448-458,  1953),  it  is  assumed 


379 


520  JOURNAL  OF  MAMMALOGY  Vol.  38,  No.  4 

that  in  most,  if  not  all,  instances  the  removal  distances  involved  were  great  enough  to  place 
the  animal  in  unfamiliar  territory  beyond  the  boundaries  of  its  normal  range  of  movements. 

A  total  of  18  individuals,  consisting  of  five  adult  males,  four  adult  females,  two  subadult 
males  and  seven  subadult  females,  were  marked  and  released  a  total  of  29  times  through 
July  30.  Aniinals  handled  after  tliis  date  are  not  included  in  tlie  treatment  of  the  data,  since 
it  is  felt  that  there  was  insufficient  opportunity  for  them  to  be  retaken  following  their  release. 
Seven  of  the  chipmunks  returned  to  the  vicinity  of  original  capture  a  total  of  ten  times  over 
distances  varying  from  430  to  1,200  and  averaging  650  feet.  In  six  of  the  ten  returns  the 
animals  were  retaken  in  the  same  trap  in  which  they  were  initially  caught.  In  two  instances 
individuals  were  retrapped  at  stations  20  and  40  feet  removed  from  the  one  where  first 
taken,  and  in  two  others  tlie  individuals  were  recovered  at  a  distance  of  115  feet  from  the 
original  site  of  captuie. 

Two  adult  males  returned  from  490  and  540  feet  in  two  and  three  days,  respectively,  but 
were  not  recovered  after  second  removals  to  1,060  and  1,150  feet.  Two  other  mature  males 
trapped  following  their  release  at  310  and  750  feet  had  moved  in  a  direction  other  tlian  that 
of  their  original  capture.  An  adult  female  was  found  in  a  trap  a  day  after  having  been 
released  at  775  feet.  She  returned  a  second  time  from  600  feet  in  two  days.  Anodier  adult 
female  was  retrapped  at  the  original  trap  station  seven  days  following  her  release  only  430 
feet  away.  A  single  subadult  male  was  recaptured  in  his  original  location  tiie  next  day  after 
his  initial  removal  to  750  feet  and  tv/o  days  after  a  second  liberation  at  1,200  feet.  He  was  not 
retrapped  subsequent  to  a  third  relocation  2,180  feeL  distant.  Another  young  male  was 
captured  at  a  point  380  feet  closer  to  its  home  area  six  days  after  being  released  940  feet  away. 
Three  subadult  females  homed  successfully.  One  returned  [rom  580  feet  the  day  aiter  release, 
another  from  650  feet  in  two  days'  time,  and  the  third  from  490  feet  after  an  interval  of  five 
days.  None  were  retaken  foliowing  second  liberations  ranging  from  940  to  1,570  feet.  Two 
other  subadult  females  were  captured  100  and  120  feet  closer  to  their  original  capture  sites 
the  day  after  having  been  released  at  460  and  450  feet,  respectively. 

These  limited  data  suggest  that  homing  ability  was  restricted  to  rather  short  distances, 
only  one  individual  being  known  to  have  returned  from  a  point  more  than  775  feet  away. 
The  extent  of  these  movements  may  be  somewhat  less  than  several  reported  by  authors  pre- 
viously mentioned.  However,  because  of  tlie  smaller  home  range  size  of  chipmunks  in  this 
area  as  compared  to  odier  habitats  in  which  the  animals  homed  from  more  distant  points,  the 
actual  distances  mov^;.t  over  strange  territory  may  be  fairly  comparable.  The  present  results 
indicate  no  obvious  differences  in  the  proportion  of  adults  and  subaduits  homing  nor  in  the 
average  distance  over  which  individuals  in  each  of  tliese  age  classes  returned.  The  intervals  of 
one  to  seven  days  between  releases  and  recoveries,  the  relatively  short  distances  involved,  and 
the  rather  low  proportion  of  returns  ( 38.8  per  cent)  suggest  that  the  animals  may  have  returned 
to  their  home  areas  through  random  movements  until  familiar  terrain  was  encountered.  It 
should  be  mentioned,  however,  that  tlie  small  number  of  traps  employed  might  have  been 
a  factor  in  the  low  rate  of  recovery,  since  a  chipmunk  returning  to  its  home  region  had  a 
lower  probabihty  of  being  recaptured  than  would  have  been  the  case  had  more  traps  been 
present.  This  might  also  have  tended  to  increase  the  apparent  time  taken  to  reach  the  home 
area  following  release.  On  tlie  otlier  hand,  the  use  of  a  limited  number  of  traps  may  have 
been  advantageous  in  that  there  was  less  interference  by  traps  with  the  normal  activities  and 
movements  of  the  animals. — James  N.  Layne,  Dept.  of  Biology,  Univ.  of  Florida,  Gainesville. 
Received  December  1,  1956. 


380 


COMPARATIVE  ECHOLOCATIOX  BY  FISHING  BATS 

RODEHICK    A.    SUTHERS 

Abstract. — The  acoustic  orientation  of  two  species  of  fish-catching  hats  was 
studied  as  they  negotiated  a  row  of  strings  or  fine  wires  extending  across  their 
fhght  path.  Orientation  sounds  of  Pizomjx  vivesi  consisted  of  a  steep  descending 
FM  sweep  lasting  about  3  msec.  Noctilio  leporimis  used  8  to  10  msec  pulses 
composed  of  an  initial  nearly  constant  frequency  portion  followed  by  a  descending 
frequency  modulation.  The  echolocation  of  small  wires  by  N.  leporimis  differed 
from  that  of  surface  fish  in  that  during  wire  avoidance  no  nearly  constant  fre- 
quency or  entirely  FM  pulses  were  emitted,  nor  was  the  pulse  duration  markedly 
shortened  as  the  barrier  was  approached.  There  was  extensive  temporal  overlap 
at  the  animal's  ear  of  returning  echoes  with  the  emitted  cries  when  the  bat  was 
near  the  barrier — a  strong  contrast  to  the  apparent  careful  minimization  of  such 
overlap  during  feeding  maneuvers.  Soctiliu  increased  its  average  pulse  duration 
about  2  msec  when  confronted  with  a  barrier  of  0.21  mm,  as  opposed  to  0.51 
mm,  diameter  wires.  Fizonijx  detected  these  wires  well  before  pulse-echo  overlap 
began,  but  at  a  shorter  range  than  did  N.  leporimis,  suggesting  the  latter  species 
may  have  a  longer  effective  range  of  echolocation. 

At  least  two  species  of  Neotropical  bats  have  independently  evolved  an 
ability  to  capture  marine  or  aquatic  organisms.  A  comparison  of  the  acoustic 
orientation  of  these  animals  is  of  particular  interest  in  view  of  their  convergent 
feeding  habits  yet  strikingly  different  orientation  sounds.  Noctilio  leporimis 
Linnaeus  ( Noctilionidae )  catches  fish  by  occasionally  dipping  its  dispro- 
portionately large  feet  into  the  water  as  it  flies  low  over  the  surface.  Very 
small  surface  disturbances  can  be  echolocated  and  play  an  important  role  in 
determining  the  locations  of  the  dips  (Suthers,  1965).  Fi.sh  caught  in  this  way 
are  transferred  to  the  mouth  and  eaten.  Pizomjx  vivesi  Menegaux  (Vesper- 
tilionidae)  also  possesses  disproportionately  large  feet.  Much  less  is  known 
concerning  the  feeding  behavior  of  this  species,  though  it  is  reasonable  to 
assume  that  it  uses  its  feet  in  a  manner  similar  to  N.  leporimis  (but  see  Reeder 
and  Norris,  1954).  Extensive  attempts  to  induce  captive  P.  vivesi  to  catch 
pieces  of  shrimp  from  the  surface  of  a  large  pool  were  unsuccessful.  The  fol- 
lowing comparison  is  therefore  based  on  the  ability  of  these  bats  to  detect 
small  obstacles. 

Methods 

The  experimental  animals  consisted  of  two  P.  vicesi,  selected  as  the  l)est  flyers  of 
several  collected  in  the  Gulf  of  California,  and  one  N.  leporimis  captured  in  Trinidad. 
The  research  was  conducted  at  the  William  Beebe  Memorial  Tropical  Research  Station 
of  the  New  York  Zoological  Society  in  Trinidad. 

The  bats  were  flown  in  a  4  X  15  m  outdoor  cage  described  elsewhere  (Suthers,  1965). 
The  test  obstacles  consisted  of  a  row  of  strings  or  wires  2.5  m  long  which  were  hung  at 
55  cm  intervals  across  the  middle  of  the  cage.  Four  sets  of  obstacles  were  used:  2  mm 
diameter  strings,  0.51  mm,  0.21  mm,  and  0.10  nun  diameter  wires,  respectively.  The 
bats  were  forced  to  pass  through  this  barrier  in  order  to  fl\'  the  length  of  the  cage.    Each 

79 


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80  JOURNAL  OF  MAMMALOGY  Vol.  48,  No.  1 

ihght  was  scored  as  a  hit  or  a  miss  according  to  whether  any  part  of  the  animal  touched 
the  test  obstacles.  Movement  of  the  larger  wires  was  easily  visible  following  even  gentle 
contact,  but  lateral  illumination  of  the  barrier  was  necessary  in  order  to  score  flights 
through  the  row  of  0.10  nun  wires.  The  wires  were  occasionally  shifted  laterally  about 
20  cm  across  the  width  of  the  cage  in  order  to  reduce  the  possibility  that  the  bats  might 
learn   their  location. 

An  attempt  was  made  to  test  each  animal  on  two  or  more  sets  of  obstacles  per  night, 
though  this  was  not  always  possible.  Cases  in  which  the  bat  was  making  unusually 
frequent  landings  or  was  particularly  reluctant  to  fly  are  omitted.  Also  excluded  are  flights 
on  which  the  barrier  was  approached  very  near  the  upper  ends  of  the  wires,  along  either 
wall  of  the  cage,  or  at  an  angle  to  the  row  of  obstacles  which  was  decidedly  smaller  than 
90°.  Experiments  with  P.  vivesi  no.  1  were  terminated  by  its  sudden  death,  which  oc- 
curred before  the  0.10  mm  diameter  wire  was  available.  Tests  with  this  size  wire  were 
therefore  performed  with  a  second  healthy  Pizonyx. 

A  series  of  flights  through  the  0.51  mm  and  0.21  mm  diameter  wires  was  photographed 
with  a  16  mm  sound  motion  picture  camera,  while  simultaneous  two-channel  tape  re- 
cordings of  the  orientation  sounds  were  obtained  from  microphones  placed  on  opposite 
sides  of  the  barrier.  The  position  of  the  flying  bat  relative  to  the  barrier  was  calculated 
by  comparing  the  arrival  time  of  each  orientation  sound  at  either  microphone  and  also 
by  matching  the  image  of  the  bat  in  each  frame  of  the  film  with  rectified  orientation  sounds 
on  the  optical  sound  track.  Details  of  these  methods  and  the  instrumentation  are  de- 
scribed elsewhere  ( Suthers,  1965).  The  overall  frequency  response  of  the  recording  sys- 
tem was  approximately  uniform  between  15  and  100  kc/sec. 

A  total  of  45  flights  by  P.  vivesi  and  N.  leporinns  was  tape  recorded  and  photographed. 
Sixteen  of  these  were  discarded  for  reasons  listed  above,  or  because  the  bat  did  not  fly 
on  a  straight  path  between  the  microphones,  or  because  of  a  poor  signal-to-noise  ratio 
on  one  of  the  channels.  The  remaining  29  flights  were  analyzed  and  pulse  intervals  ( the 
silent  period  from  the  end  of  one  pulse  to  the  beginning  of  the  next)  were  plotted  against 
the  distance  of  the  bat  from  the  barrier  (see  Fig.  2).  The  animal's  position  was  deter- 
mined to  within  an  accuracy  of  about  ±  10-15  cm  at  a  distance  of  two  meters  from 
the  wires  and  ±  5-10  cm  in  the  immediate  region  of  the  wires. 

Results  and  Conclusions 

Obstacle  avoidance  scores  are  given  in  Table  1.  The  greater  success  of  P. 
vivesi  in  avoiding  0.10  mm  wires  may  reflect  its  shorter  maximum  wingspan 
of  40  cm,  compared  to  50  cm  for  N.  leporinus.  Audio  monitoring  of  the  recti- 
fied orientation  sounds  emitted  by  these  species  during  their  flights  indicated 

Table   1. — Percent  of  flights  through   harrier  on  which   hat  missed  obstacles  spaced  at 

55  cm  intervals.    Total  number  of  flights  in  parentheses.    Maximum  wingspan  of  P.  vivesi 

is  about  40  cm;  that  of  N.  leporinus   is  about  50  cm. 


OBSTACLE 

DIAMETER  (MM) 

Bat 

2 

0.51 

0.21 

0.10 

Pizxmijx  vivesi  (1) 

94% 

83% 

51% 

(163) 

(416) 

(232) 

Pizonyx  vivesi   (2) 

71% 
(151) 

37% 
(74) 

Noctilio  leporinus 

91% 

76%> 

60% 

20% 

(207) 

(203) 

(217) 

(55) 

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TIME  (MSEC) 

Fig.  1. — Sound  spectrographs  of  orientation  sounds  emitted  by  Pizonyx  vivesi  (a) 
and  Noctilio  leporinus  (b)  when  approaching  wire  obstacles.  A  pair  of  consecutive 
pulses,  reproduced  at  two  different  filter  settings  of  the  sound  spectrograph,  is  shown  for 
each  species.  The  narrow  band  filter  setting  (top)  best  indicates  the  frequency  spectrum 
of  the  cries,  whereas  pulse  duration  and  temporal  relationships  are  more  accurately  shown 
using  a  wide  band  filter  (bottom). 


that  approaches  to  the  three  larger  diameter  obstacles  were  accompanied  by 
increases  in  the  pulse  repetition  rate,  whereas  no  such  increase  was  noted 
during  approaches  to  the  0.10  mm  wires.  This  suggests  that  these  latter  wires 
were  too  small  to  be  detected  at  an  appreciable  distance  and  that  tests  using 
them  may  indicate  chance  scores. 

Tape  recordings  of  flights  between  0.51  and  0.21  mm  diameter  wires  showed 
that  these  two  species  used  distinctly  different  kinds  of  orientation  sounds 
in  detecting  the  obstacles  ( Fig.  1 ) .  When  approaching  the  barrier  at  a  dis- 
tance of  about  2  m,  P.  vivesi  emitted  ultrasonic  pulses  with  a  duration  of  about 
3  msec  at  a  mean  repetition  rate  of  10  to  20  per  sec.  Each  of  these  was  frequency 
modulated  ( FM ) ,  sweeping  downward  from  about  45  kc/sec  to  20  kc/sec  and 
accompanied  by  a  second  harmonic.  The  shghtly  lower  starting  frequency 
( 36  kc/sec )  reported  by  Griffin  ( 1958 )  may  be  due  to  the  lower  sensitivity 
to  high  frequencies  of  microphones  available  at  that  time.  At  a  similar  distance 
from  the  barrier  N.  leporinus  produced  pulses  with  a  duration  of  about  8  to 
10  msec  at  comparable  repetition  rates.  These  sounds,  however,  were  composed 
of  an  initial  portion  at  a  nearly  constant  frequency  of  about  60  kc/sec  followed 
by  an  FM  sweep  down  to  30  kc/sec.  Neither  species  made  any  pronounced 
change  in  the  frequency  structure  of  its  pulses  as  it  approached  and  negotiated 


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Vol.  48,  No.  1 


2  10  2  1 

DISTANCE  FROM  WIRES  (METERS) 

Fig.  2. — Examples  of  changes  in  orientation  pulse  intervals  during  flights  by  fishing 
bats  through  a  barrier  of  fine  wires  spaced  at  55  cm  intervals  across  their  flight  path. 
Each  dot  represents  one  orientation  sound:  (a)  Noctilio  leporinus  flying  between  0.51 
mm  diameter  wires;  (b)  Pizonyx  vivesi  flying  between  0.51  mm  diameter  wires;  (c)  N. 
leporinus  flying  between  0.21  mm  diameter  wires;  (d)  P.  vivesi  flying  between  0.21  mm 
diameter  wires.  On  flights  a,  b,  and  d,  the  bat  did  not  touch  the  wires.  On  the  flight 
shown  in  c  the  wires  were  hit  by  the  bat.  Vertical  dashed  line  indicates  position  of 
the  wires. 

the  barrier.  The  pulse  repetition  rate  was  increased,  however,  to  about  30  or 
35  per  sec.  The  use  of  a  single  pulse  type  by  IV.  leporinus  contrasts  with  its 
echolocation  during  normal  cruising  and  feeding  when  constant  frequency 
and  entirely  FM  pulses  are  also  employed  (Suthers,  1965). 

Fig.  2  gives  examples  of  alterations  in  pulse  intervals  during  one  flight  by 
each  species  through  a  barrier  of  0.51  mm  and  of  0.21  mm  diameter  wires.  The 
possible  significance  of  the  tendency  to  alternate  long  and  short  pulse  intervals 
during  the  approach  to  the  barrier'is  not  known.  It  was  not  possible  to  reliably 
distinguish  hits  from  misses  on  the  basis  of  these  graphs. 

The  minimum  average  distance  of  detection  was  estimated  by  calculating  the 
point  at  which  the  bat  began  to  shorten  the  pulse  intervals.  Pizonyx  vivesi 
and  N.  leporinus  must  have  detected  the  0.51  mm  wires  at  an  average  distance 
from  the  barrier  of  at  least  110  and  150  cm,  respectively,  and  the  0.21  mm 


384 


February   1961 


SUTHERS— FISHINC;  BATS 


83 


CO 


^    100- 


GO 


CO 


CO 


DISTANCE  FROM  WIRES  (METERS) 

Fig.  3. — Mean  pulse  intervals  (solid  line)  and  mean  pulse  duration  (broken  line) 
of  Noctilio  leporinus  (a)  and  Pizomjx  vivesi  (b)  during  approaches  to  the  0.51  mm 
diameter  wires  spaced  across  the  flight  path  at  55  cm  intervals.  The  bat  is  flying  from 
left  to  right.  Vertical  dashed  line  indicates  the  position  of  the  v/ires.  Arrows  indicate 
estimated  minimum  mean  distance  of  detection  as  judged  by  progressive  shortening  of  the 
pulse  intervals.  Dotted  diagonal  line  shows  the  distance  at  which  pulse-echo  overlap 
will  first  occur  for  any  given  pulse  duration.  Echoes  from  the  wires  of  pulses  whose 
mean  duration  lies  above  this  line  will  overlap  with  the  emitted  pulse  by  an  average 
amount  equal  to  their  vertical  distance  above  the  line.  Each  point  represents  tlie  mean 
interval  or  duration  of  pulses  emitted  in  the  adjacent  ±  10  cm.  Intervals  for  N.  leporinus 
are  averages  of  five  flights:  P.  vivesi  intervals,  of  seven  flights.  All  pulse  durations  are 
averages  of  three  flights. 


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Vol.  48,  No.  1 


lOOh 
80 
60 
40 
20 


CO 


^    100 


CO 


80 


60 


40 


20- 


10 
8 
6 
4 
2 


CO 


II 


CO 


2  1  0 

DISTANCE  PROM   WIRES   (METERS) 

Fig.  4. — Mean  pulse  intervals  (solid  line)  and  mean  pulse  duration  (broken  line)  of 
Noctilio  leporinus  (a)  and  Pizonyx  vivesi  (b)  during  approaches  to  the  0.21  mm  diameter 
wires  spaced  across  the  flight  path  at  55  cm  intervals.  For  explanation  see  legend  of 
Fig.  3.  Possible  alternate  interpretations  of  the  point  at  which  a  progressive  decrease  in 
pulse  intervals  first  appears  are  indicated  by  small  arrows.  The  more  conservative  estimates 
denoted  by  the  large  arrows  have  been  used  in  the  text.  Pulse  durations  and  intervals  of 
N.  leporinus  are  averages  of  10  flights;  those  of  P.  vivesi  are  averages  of  seven  flights. 


386 


February  1967  SUTHERS— FISHING  BATS  85 

wires  at  an  average  of  at  least  70  and  130  cm,  respectively  (Figs.  3  and  4). 
Pulse  durations  did  not  markedly  shorten  as  the  barrier  was  approached. 
Thus  at  close  ranges  the  echoes  returning  from  the  wires  must  have  overlapped 
extensively  with  the  emitted  pulse.  In  the  case  of  N.  leporinus  this  overlap 
may  have  begun  on  the  average  when  the  bat  was  still  130  and  170  cm  from 
the  0.51  and  0.21  mm  wires,  respectively  (Figs.  3  and  4). 

The  data  do  not  exclude  the  possibility  that  the  start  of  pulse-echo  overlap 
and  the  start  of  a  progressive  reduction  in  the  pulse  intervals  by  N.  leporinus 
may  occur  simultaneously  or  be  closely  synchronized.  The  pulses  of  P.  vivesi 
must  have  overlapped  with  their  echoes  during  the  last  40  and  50  cm  of  the 
approach  to  the  0.5]  and  0.21  mm  wires,  respectively  (Figs.  3  and  4).  It 
seems  clear  that  P.  vivesi  began  to  decrease  its  pulse  intervals  well  before 
the  first  pulse-echo  overlap  occurred. 

Noctilio  leporinus  regularly  emitted  longer  pulses  when  approaching  the 
0.21  mm  wires  than  when  approaching  the  0.51  mm  wires.  The  significance 
of  this  difference  is  not  known,  although  it  is  possible  that  the  earlier  initiation 
of  pulse-echo  overlap,  or  the  increased  duration  of  overlap  at  a  given  dis- 
tance, when  longer  pulses  are  used,  in  some  way  facilitated  detection  of  the 
finer  wires.  If  this  is  true,  however,  why  is  overlap  minimized  with  such 
apparent  care  during  the  detection  of  small  cubes  of  fish  muscle  tissue  pro- 
jecting above  the  water  surface  (see  below)?  Since  the  difference  in  pulse 
duration  as  a  function  of  wire  diameter  was  already  present  when  the  bat 
was  two  meters  from  the  barrier,  either  leporinus  must  have  determined  some- 
thing about  the  wire  diameter  at  a  distance  of  more  than  two  meters,  or  it 
must  have  remembered  what  kind  of  wires  it  had  to  detect  and  adopted  a 
suitable  pulse  duration  prior  to  their  detection. 

Details  of  the  echolocation  of  P.  vivesi  during  feeding  are  not  known.  Pulse- 
echo  overlap  during  wire  avoidance  by  N.  leporinus,  however,  contrasts  strongly 
with  its  apparent  careful  avoidance  during  catches  of  stationary  1  cm-  cubes  of 
fish  muscle  tissue  projecting  above  the  surface  of  the  water.  Pulse  lengths 
under  these  conditions  were  progressively  shortened  as  if  to  avoid  pulse-echo 
overlap  until  the  bat  was  30  cm  or  less  from  the  food  (Suthers,  1965).  Thus 
in  the  case  of  N.  leporinus,  at  least,  information  concerning  the  position  and 
nature  of  small  wire  obstacles  is  probably  received  in  the  presence  of  overlap, 
whereas  most  of  this  information  regarding  potential  food  must  be  obtained 
without  such  overlap.  It  has  yet  to  be  determined  whether  or  not  pulse-echo 
overlap  is  actually  utilized  by  the  bat. 

It  has  been  suggested  (Pye,  I960;  Kay,  1961)  that  possible  nonlinearities 
in  the  ear  may  allow  bats  to  utilize  beat  notes  arising  from  pulse-echo  overlap 
as  a  means  of  determining  distance.  Three  species  of  chilonycterine  bats  have 
subsequently  been  found  to  maintain  an  overlap  during  the  pursuit  and  catch- 
ing of  Drosophila  (Novick,  1963,  1965;  Novick  and  Vaisnys,  1964).  Myotis 
lucifugus  (Cahlander  et  al.,  1964)  and  N.  leporinus,  on  the  other  hand,  appear 
to  minimize  overlap  when  catching  tossed  mealworms  or  fish,  respectively. 


387 


86  JOURNAL  OF  MAMMALOGY  Vol.  48,  No.  1 

Should  pulse-echo  overlap  be  utilized  by  N.  leporinus  in  determining  its  dis- 
tance from  the  wires,  then  some  basically  different  method,  such  as  the 
temporal  delay  of  the  returning  echo  (Hartridge,  1945),  must  be  employed 
in  determining  the  range  of  potential  food. 

Since  the  constant  frequency  portion  of  the  Doppler-shifted  echo  would  at 
first  overlap  with  the  FM  portion  of  the  call,  and  later  with  part  of  both  the 
constant  frequency  and  FM  portions  of  the  call,  any  resulting  beat  note  would 
have  a  complexly  varying  frequency  structure  from  which  it  would  be  difficult 
for  the  bat  to  determine  its  distance  from  the  barrier. 

One  would  like  to  know  if  there  is  a  significant  difference  in  the  range 
of  echolocation  for  these  fishing  bats.  Noctilio  leporinus  emits  very  loud  pulses 
with  a  peak-to-peak  sound  pressure  of  up  to  60  dynes/cm-  at  a  distance  of 
50  cm  from  the  mouth  (Griffin  and  Novick,  1955).  The  intensity  of  sounds 
emitted  by  P.  vivesi  has  not  been  measured,  although  the  shorter  range  at 
which  they  can  be  detected  on  an  ultrasonic  receiver  suggests  they  are  less 
intense  than  those  of  Noctilio.  M.  hicifugus,  a  vespertihonid  closely  related 
to  Pizonyx,  can  detect  0.46  mm  diameter  wires  at  120  cm  and  0.18  mm  wires  at 
90  cm  (Grinnell  and  Griffin,  1958),  thus  comparing  favorably  with  fishing 
bats  in  this  respect.  Peak-to-peak  sound  pressures  of  this  species  have  been 
measured  at  12  dynes/cm-  at  50  cm  (Griffin,  1950).  Sound  intensity  of  the 
emitted  pulse,  however,  is  but  one  of  a  number  of  physical  and  physiological 
factors  which  must  play  important  roles  in  determining  the  range  of  such  a 
system  for  acoustic  orientation. 

Acknowledgments 

I  wish  to  thank  Prof.  Donald  R.  Griffin,  Drs.  H.  Markl,  N.  Suga,  and  D.  Dunning 
for  helpful  criticism  and  assistance.  Drs.  R.  E.  Carpenter,  G.  W.  Cox,  and  A.  Starrett 
gave  valuable  assistance  in  obtaining  live  P.  vivesi.  Appreciation  is  also  expressed  to  the 
San  Diego  Society  of  Natural  History  for  use  of  the  Vermillion  Sea  Station  at  Bahia 
de  los  Angeles,  Baja  California,  and  to  the  New  York  Zoological  Society  for  the  use 
of  the  William  Beebe  Memorial  Tropical  Research  Station  in  Trinidad.  The  coopera- 
tion of  the  Mexican,  Trinidadian,  and  United  States  governments  in  the  transit  of  bats 
is  gratefully  acknowledged.  This  work  was  supported  by  grants  from  N.LH.,  The  Society 
of  the  Sigma  Xi  Research  Fund,  and  the  Milton  Fund  of  Harvard  University. 

Literature  Cited 

Ghiffix,   D.    R.     1950.     Measurements   of   the   ultrasonic   cries   of  bats.    J.    Acoust.    Soc. 

Amer.,  22:   247-255. 

.      1958.     Listening  in  the  dark.    Yale  Univ.  Press,  New  Haven,  413  pp. 

Griffin,    D.    R.,    and    A.    Novick.      1955.     Acoustic    orientation    of    neotropical    bats.     J. 

Exp.  Zool.,  1.30:  251-300. 
Grinnell,   A.   D.,   and   D.   R.   Griffin.      1958.     The   .sensitivity   of   echolocation    in   bats. 

Biol.   Bull.,   114:    10-22. 
Hartridge,   H.      1945.     Acoustic  control  in  the  flight  of  bats.    Nature,   156:   490-494. 
Kay,  L.      1961.     Perception  of  distance  in  animal  echolocation.    Nature,   190:   361-.362. 
Novick,  A.      1963.     Pulse  duration  in  the  echolocation  of  insects  by  the  bat,  Pteronotus. 

Ergebnisse  Biol,  26:   21-26. 


388 


Fehruary  1967  SUTHERS— FISHING  BATS  87 

.      1965.     Echolocation   of   flying   insects   by    the   Ixit,    Chilonijcteris   psilotis.     Biol. 

Bvill.,  128:   297-314. 
NoviCK,    A.,    AND    J.    R.    V.\isNYs.      1964.     Echolocation    of    flying    insects    by    the    bat, 

Chilonijcteris  parnelli.    Biol.   Bull.,   127:   478-488. 
Pye,  J.  D.     1960.     A  theory  of  echolocation  by  bats.   J.  Laryng.    Otol.,  74;   718-729. 
Reeder,   W.    G.,    -AND    K.    S.    NoRRis.     1954.     Distribution,    habits,    and    type    locality    of 

the  fish-eating  bat,  Pizonyx  vivesi.    J.  Mamm.,  35:   81-87. 
SuTHEBs,  R.  a.      1965.     Acoustic  orientation  by  fishing  bats.    J.  E.xp.  Zool,  158:   319-348. 

The  Biological  Laboratories,  Harvard  University,  Cambridge,  Massachusetts  (present 
address:  Department  of  Aimtomy  and  Phijsiology,  Indiana  University,  Bloomington, 
Indiana  47401).    Accepted  11  November  1966. 


389 


The  Intraspecific  Social  Behavior  of  Some  Cricetine 
Rodents  of  the  Genus  Peromyscus 

JOHN  F.  EISENBERG 

Department  of  Zoology,  University  of  California,  Berkeley 

Abstract:  A  three-compartment  territorial  cage  was  employed  in 
studying  the  intraspecific  social  behavior  of  Perorjiyscus  californicus,  P. 
erernicus,  P.  crinitus,  and  P.  maniculatus.  Two  pairs  of  mice  of  the  same 
species  were  allowed  to  interact  for  one  week  following  a  period  of  separa- 
tion from  each  other  in  the  end  compartments.  All  species  showed  similar 
forms  of  agonistic  behavior  patterns.  The  closely  related  P.  erernicus  and 
P.  californicus  employed  a  modified  fighting  technique  involving  an 
attack  leap,  scuffle,  and  avoidance  leap.  The  females  of  P.  crinitus  and 
P.  californicus  showed  a  pronounced  nest  site  attachment  and  defense. 
Agonistic  behavior  with  the  exception  of  nest  defense  was  confined  almost 
entirely  to  the  males.  The  aggressivity  of  P.  erernicus  was  the  least  pro- 
nounced. Peromyscus  crinitus  males  showed  the  most  agonistic  behavior, 
and  P.  californicus  and  P.  maniculatus  were  intermediate.  Pair  associa- 
tions in  the  territorial  boxes  were  prolonged  for  P.  californicus  and,  to  a 
lesser  extent,  for  P.  crinitus.  The  other  two  species  showed  a  weak  pair 
bonding. 

Introduction 

In  a  previous  paper  (Eisenberg,  1962),  the  social  behavior  of 
Peromyscus  californicus  parasiticus  and  P.  maniculatus  gambelii  was 
described  and  contrasted.  In  the  present  study  the  methods  used  were 
extended  to  P.  crinitus  stephensi  and  P.  eremicus  eremicus.  Enough 
data  now  exist  to  present  a  comparison  of  all  four  species. 

Peromyscus  californicus  and  P.  eremicus  are  closely  related 
(Hooper,  1958)  and  are  included  in  the  Eremicus  division  of  the 
genus  Peromyscus.  Peromyscus  crinitus  is  considered  by  Hooper  to  be 
intermediate  between  P.  boylei  and  P.  maniculatus,  all  of  which  are 
included  within  the  Maniculatus  division. 

The  individuals  of  P.  californicus  and  P.  maniculatus  used  in  this 
study  were  trapped  in  the  vicinity  of  Berkeley,  Alameda  Co.,  Califor- 
nia. They  inhabit  <:ympatrically  the  chaparral  areas  in  west  central 
California,  and  their  ecology  has  been  intensively  studied  by  McCabe 
and  Blanchard   (1950).        ' 

Peromyscus  eremicus  and  P.  crinitus  inhabit  the  arid  Sonoran  life 
zones  of  western  North  America.  In  general,  P.  crinitus  occupies  the 
Upper  Sonoran  high  deserts  while  P.  eremicus  ranges  in  the  Lower 
Sonoran  zone.  The  individuals  of  P.  crinitus  used  in  this  study  were 
trapped  in  the  vicinity  of  Cottonwood  Springs,  San  Bernardino  Co., 
California.  The  individiials  of  P.  eremicus  were  all  collected  around 
15  miles  west  of  Borrego  Springs  in  San  Diego  Co..  California.  These 
two  species  are  sympatric  over  part  of  their  ranges.  In  general,  P. 
crinitus  is  a  rock  dweller  while  P.  erernicus  inhabits  the  brushy,  flat 
areas  of  the  desert  floor.  Both  P.  californicus  and  P.  eremicus  have 
smaller  litters  when  compared  with  P.  maniculatus,  while  P.  crinitus 

240 


390 


1963  Eisenberg:  Social  Behavior  of  Cricetines  241 

has  an  intermediate  average  litter  size.  McCabe  and  Blanchard  report 
average  litter  sizes  of  1.91  and  5  for  P.  calijornicus  and  P.  maniculatus 
^ambelii,  respectively.  Hall  gives  an  average  litter  size  of  4  for  P. 
crinitus,  while  Asdell  records  an  average  litter  size  of  3.7  for  P. 
eremicus.  The  maturation  and  growth  of  P.  calijornicus  and  P.  mani- 
culatus (^ambelii  are  analyzed  in  detail  by  McCabe  and  Blanchard 
(1950). 

Acknowledgments. — I  wish  to  express  my  gratitude  to  Drs.  Peter  Marler  and 
Seth  B.  Benson  for  their  valuable  criticism  of  this  work.  Part  of  the  research  was 
conducted  during  the  tenure  of  a  National  Science  Foundation  Prc-doctoral 
Fellowship. 

Methods 

Alter  the  individual  behavior  patterns  had  been  described  for  the 
various  species,  a  series  of  encounters  between  two  individuals  of  the 
sames  species  was  run  in  order  to  obtain  descriptions  of  the  various 
postures  and  activities  employed  in  the  .social  context.  Following  these 
preliminary  experiments  a  series  of  territorial  encounters  was  arranged 
using  two  pairs  of  mice  of  the  same  species  for  each  encounter.  The 
territorial  boxes  were  9  x  26  x  75  inches  in  size  with  glass  tops,  sides, 
and  fronts;  the  back  was  of  quarter-inch  hardware  cloth,  and  the 
bottom  of  wood.  Each  box  was  divided  into  three  equal  compartments 
by  wood  partitions.  A  small  opening,  2  x  1  inches,  cut  in  each  partition 
served  as  a  door,  and  was  closed  with  screen  except  at  the  time  of 
experimentation.  A  pair  of  animals  was  placed  in  each  end  compart- 
ment with  food,  water,  and  cotton  nesting  material,  and  left  for  two 
weeks.  The  doors  between  the  compartments  were  then  opened  and 
the  subsequent  behavior  of  the  four  individuals  was  noted  for  one 
hour.  These  observations  were  made  at  night  using  a  red  light  for 
illumination.  The  doors  were  then  left  open  for  one  week  and  daily 
observations  at  set  intervals  allowed  me  to  ascertain  in  which  compart- 
ment and  with  whom  the  animals  were  dwelling.  The  specimens  were 
liH-clipped  for  identification.  These  experiments  were  run  for  all 
species  during  the  spring,  summer,  and  fall.  Five  experiments  were 
run  with  P.  maniculatus  and  P.  crinitus,  and  six  with  P.  calijornicus 
and  P.  eremicus.  Each  experiment  was  run  with  a  difTerent  pair  of 
animals. 

Agonistic  Behavior   Patterns 

A  complete  description  of  the  adult  behaxior  patterns  for  P.  calijor- 
nicus and  P.  maniculatus  is  included  in  a  previous  publication  (Eisen- 
berg, 1962).  The  adult  behavior  of  P.  eremicus  and  P.  crinitus  is  very 
similar.  In  the  present  paper  only  the  agonistic  patterns  which  ap- 
peared in  the  encounters  will  be  discussed. 

Fightini>. — Two  animals  approach  and  one  or  both  rush.  The 
animals  lock  together  with  their  ventral  surfaces  in  contact  and  roll 
about,  gripping  one  another  very  lightly  with  their  fore  and  hind  feet. 
This  is  called  the  locked  fii^htino  posture.  It  generally  ends  either  by 
breaking   apart    followed    by    a    chase-flight    sequence,    or    when    one 


391 


242  The  American  Midland  Naturalist  69(1) 

Table  I. — Bouts  f)f  the  different  ftirnis  of  agonistic  beha\i()r 
during  six  territorial  encounters   (P.  californicus) 

Type  of  Fighting  NVst  Average;' 

eiKoiiMlrr  Modified     Locked         Clia>e        Upright        defense  ^  Encounter 


Male  to  Male 

4 

17 

38 

9 

0 

68 

11.3 

Male  to  Female 

1 

0 

4 

0 

0 

5 

.8 

Female  to  Male 

0 

I 

5 

3 

10 

19 

3.2 

Female  to  Female 

0 

0 

1 

1 

0 

2 

.3 

V 

5 

18 

48 

13 

10 

94 

15.6 

animal  is  forced  on  its  back  in  a  defeat  posture.  Peromyscus  califor- 
nicus and  P.  erernicus  often  employ  a  modified  fightiriii  technique 
where  the  animals  spring  at  one  another,  scuffle  briefly,  and  then 
jump  away   (cf.  Jumping  avoidance  technique,  Eisenberg,    1962). 

Chasitii^. — This  is  usually  confined  to  the  floor  of  the  cage,  but 
small  leaps  may  be  employed.  Durin"  chasing  the  pursuing  animal 
may  bite  at  the  rump  or  tail  of  the  subordinate. 

Upright  posturing. — Upright  posturing  was  scored  when  an  animal 
neither  attacked  nor  fled,  but  raised  its  forepaws  off  the  ground  and 
with  its  body  at  about  45-90  degrees  off  the  ground  either  darted  its 
head  at  or  e.xtended  its  forepaws  toward  the  aggressor.  This  posture 
can  be  broken  down  into  several  sub-patterns. 

Nt'st  defense. — The  animal  assumes  a  crouched  upright  in  the  nest 
and  by  wardin":  with  the  forepaws  or  darting  the  head  repulses  the 
intruder.  In  P.  maniculatus  and  P.  californicus  this  movement  is  often 
accompanied  by  an  explosive  squeak  or  ''chit.''  Peromyscus  crinitus 
has  a  slightly  different  nest  defense  sound  in  that  chits  are  uttered 
in  bursts  of  2  to  20  at  a  rate  of  5-6  per  second. 

Species  Comparisons 

Tables  I  through  IV  summarize  the  number  of  bouts  of  the  five 
major  agonistic  patterns  for  each  class  of  interaction  (male  to  male; 
male  to  female;  female  to  male;  and  female  to  female)  for  all  four 
species.    In   general,   after   the   doors   were   opened    the   males   would 


Table  II. — Bouts  of  the  different  forms  of  agonistic  behavior 
during  six  territorial  encounters  (P.  eremicus) 

Type  of  Fighting  Nest  Average/ 

encounter  Modified      Locked        Chase      Upright    defense  2  Encounter 


Male  to  Male 

12 

2 

31 

1 

0 

46 

7.7 

Male  to  Female 

1 

0 

9 

0 

0 

10 

1.7 

Female  to  Male 

1 

0 

4 

2 

1 

8 

1.3 

Female  to  Female 

2 
16 

1 
3 

4 
48 

0 
3 

0 

1 

7 
71 

1.2 

2 

11.9 

392 


1963  Eisenbf.ro:  Social  Behamor  of  Cricetines  243 

Table  III.  —  Bouts  of  the  different  forms  of  agonistic  behavior 
during  fi\  e  territorial  encounters  (P.  maniculatus) 

Type  of  Fighting  Nest  Average 

encounter  Modified     Locked        Chase  L'pright      defense         2i  Encounter 


Male  to  Male 

0 

20 

24 

11 

2 

57 

11.4 

Male  to  Female 

0 

1 

6 

3 

0 

10 

2.0 

Female  to  Male 

0 

n 

0 

3 

2 

5 

1.0 

Female  to  Female 

n 

0 

1 

22 

0 

30 

0 
17 

0 
4 

1 
73 

.2 

V 

14.6 

encounter  one  another  and  fit^ht.  After  a  variable  number  of  fights 
the  superior  male  would  invade  the  nest  chamber  of  the  subordinate 
pair.  The  females  were  less  prone  to  become  involved  in  fighting, 
but  females  of  P.  calijornicus  and  P.  crinitus  engaged  in  a  significant 
amount  of  nest  defense.  To  a  marked  extent,  males  of  P.  calijornicus 
and  P.  eremicus  employed  the  modified  fighting  technique  of  an 
attack  leap,  scuffle,  and  jumping  away.  Pfroniyscus  eremicus  males 
employed  this  [pattern  almost  exclusively.  Perornyscus  eremicus  showed 
the  lowest  number  of  male-male  aggressive  bouts  per  encounter  [1 .1  \  : 
P.  calijornicus  and  P.  maniculatus  were  intermediate  with  11.3  and 
11.4  bouts  per  male-male  encounter,  respectively.  Perornyscus  crinitus 
was  the  highest  with  an  average  of  17.0  bouts  per  encountei.  In  all 
sjjecies.  bouts  of  chasing  comprised  the  greatest  percentage  of  agonistic 
behavior.  Agonistic  behavior  involving  females  was  low  except  for 
P.  crinitus  and  P.  calijornicus  where  nest  defense  was  shown. 

By  taking  notes  on  the  distribution  of  the  animals  in  the  encounter 
cages  on  the  week  following  the  opening  of  the  doors,  it  was  possible 
to  determine  how  long  a  pair  remained  together  and  separate  from 
tfie  other  pair.  Peromyscus  calijornicus'  has  a  strong  tendency  to  re- 
main paired  and  separate.  PcrotJiyscus  crinitus  exhibits  this  to  a  lesser 
extent  and  the  other  two  species  show  a  weak  pair  association.  It 
appears  that  the  pair  association  results  in  part  from  the  strong  nest 
defense  tendencies  by  the  females  ot  P.  crinitus  and  P.  calijornicus. 
The  male,  whether  the  winner  or  loser  of  the  first  night's  battles,  is 
able  to  remain  with  his  female  while  her  nest  defense  mitigates  against 


Table  I\'. — Bouts  of  the  different  forms  of  agonistic  behavior 
during  five  territorial  encounters  (P.  crinitus) 

Type  of  Fighting  .Nest  Average 

encounter  Modified  ^ocked  Chase         Upright     defense  ^'  Encounter 

Male  to  Male 
Male  to  Female 
Female  to  Male 
Female  to  Female 

2  2  30  70  11  40  153  30.6 


2 

27 

50 

5 

1 

85 

17.0 

0 

3 

18 

0 

1 

22 

4.4 

0 

1 

6 

36 

43 

8.6 

0 

-■ 

1 

0 

2 

3 

.6 

393 


244  The  American  Midland  Naturalist  69(1 ) 

Table  V. — Length  of  time  the  pairs  remained  together  and  separate 
from  the  other  mice  in  the  territorial  experiments 


Number 

of  ex- 

Average  number 

Species 

periments 

of  days* 

P. 

californicus 

6 

5.5 

p. 

eremicus 

6 

1.0 

p. 

crinitus 

5 

4.4 

p. 

maniculatus 

5 

.8 

*  Maximum  possible  number  of  days —  7. 


the  integration  of  the  group.  In  the  experiments  with  P.  eremicus  and 
P.  maniculatus,  the  winning  male  and  both  females  generally  nested 
together  on  the  following  day.  The  losing  male  was  gradually  assim- 
ilated after  two  or  three  days. 

Table  VI  portrays  the  average  number  of  days  a  pair  or  a  single 
individual  remained  in  its  original  nest  during  the  week  following  the 
opening  of  the  doors.  Peromyscus  californicus  is  again  appreciably 
higher.  Peromyscus  crinitus  does  not  demonstrate  the  same  trend 
even  though  this  species  tend.s  to  preserve  its  pair  structure.  This  is 
probably  caused  by  the  extreme  aggressiveness  of  the  superior  male 
who  displaces  the  inferior  male  and  his  mate.  That  P.  californicus 
can  maintain  its  original  nest  site  may  be  in  part  a  result  of  its  ability 
to  control  the  expression  of  aggressive  behavior  (Eisenberg,  1962). 
Although  the  male  P.  californicus  fight  readily,  they  do  not  persist 
with  overt  as;?ression  but  soon  settle  down  to  a  dominance  situation 
in  the  cage.  The  males  never  wound  each  other  seriously  by  tail  and 
rump  bites,  and  P.  californicus  employs  a  special  mewing  cry  to 
inhibit  aggressive  rushes  by  a  conspecific.  The  other  species  seem 
not  to  be  able  to  control  their  agonistic  behavior  so  well.  Since  P. 
eremicus  males  fight  so  little,  wounding  during  the  subsequent  week 
was  minimal.  In  only  one  experiment  did  a  male  lose  his  tail  from 
tail  biting.  However,  P.  maniculatus  and  P.  crinitus  males  persisted 
throughout  the  week  in  their  aggressive  chasing  and  rump  and  tail 
biting.    In   three   experiments   with  P.    crinitus   and   two   experiments 


Table  VI. — Consecutive  days  that  a  separate  or  paired  animal 
remained  in  its  original  compartment 


Number 

of  ex- 

Average  number 

Species 

periments 

of  days* 

P. 

californicus 

6 

5.5 

p. 

eremicus 

6 

1.3 

p. 

crinitus 

5 

2.8 

p. 

maniculatus 

5 

2.0 

Maximum  possible  number  of  days  —  7. 


394 


1963  Eisenberg:  Social  Behavior  of  Cricetines  245 

with  P.  maniculatus,  the  inferior  males  lost  up  to  one-half  their  tails 
from  persistent  biting. 

In  the  breeding  cages  where  fajnilies  of  these  mice  were  allowed 
to  reproduce  and  live  together,  one  could  see  a  reflection  of  these 
aggressive  trends.  Peromyscus  crinitus  is  quarrelsome  and  the  females 
are  intolerant  during  parturition.  Serious  wounds  on  the  rumps  or  ta:ils 
were  of  common  occurrence  with  tfiis  species.  Peromyscus  maniculatus 
females  are  more  tolerant  during  parturition  and  may  allow  the  male 
to  remain  with  them.  However,  male-male  fights  in  the  breeding 
cages  often  resulted  in  serious  rump  and  tail  wounds.  Peromyscus 
eremicus  females  are  tolerant  and  the  males  fight  little  among  them- 
selves, but  at  high  densities  in  the  breeding  cages  rump  and  tail 
wounds  occasionally  resulted  from  male-male  and  male-female  antag- 
onism. 

Although  P.  calijornicus  males  will  fight  and  the  females  defend 
their  nests  vig^orouslv,  the  anim.als  in  the  breeding  cashes  formed  stable 
adult  groups  with  a  minimum  of  wounding.  A  female  would  readily 
permit  the  male  and  mature  litters  to  remain  with  her  during  par- 
turition. 

Discussion 

The  four  species  seem  to  exemplify  three  types  of  social  organ- 
ization. Peromyscus  crinitus  seems  to  be  a  form  having  a  dispersed 
social  organization  with  a  high  male-male  antagonism  and  with 
separate  nesting  by  females  with  young.  Adult  social  groupings  are 
probablv  confined  to  brief  pairings  by  males  and  females  during  the 
breeding  season.  This  seems  quite  comparable  to  the  situation  e.x- 
emplified  by  P.  leucopus  described  by  Nicholson  (1941).  Peromyscus 
eremicus  and  P.  maniculatus  gambelii  seem  to  have  a  loose  type  of 
.social  structure.  Pairing  appears  to  be  transient,  but  males,  females, 
and  litters  may  remain  associated  in  nature  for  longer  periods.  This 
may  be  comparable  to  the  situation  described  by  Howard  (1948) 
for  P.  maniculatus  bairdii. 

Peromyscus  californicus  with  its  low  reproductive  potential  builds 
and  defends  a  complex  nest  and  occupies  a  given  area  for  rather 
prolonged  periods  of  time  (McCabe  and  Blanchard,  1950).  This 
species  may  have  a  prolonged  pair  bond  and  if  the  male  and  female 
do  not  actually  nest  together  through  parturition,  a  male  remains  in 
the  vicinity  of  a  given  female  and  the  litter  for  several  months.  This 
species  appears  to  be  developing  a  social  system  based  on  small  semi- 
permanent family  groups.  The  ecology  of  P.  eremicus  and  P.  crinitus 
is  too  little  known  to  attempt  a  correlation  between  the  mode  of 
environmental  exploitation  and  the  form  of  their  social  organization. 
Peromyscus  californicus  has  probably  evolved  its  tolerance  abilities 
and  family  fonnation  as  a  concomitant  of  its  lower  reproductive 
potential  and  its  rather  restricted  mode  of  habitat  exploitation. 


395 


246  The  American  Midland  Naturalist  69(1 ) 

References 

AsDELL,  S.  A.  1946.  Patterns  of  mammalian  reproduction.  Comstock  Publ. 
Co.,  Ithaca,   x  -}-  437  p. 

EisENBERG,  J.  F.  1962.  Studies  on  the  behavior  of  Peromyscus  maniculatus 
gambelii  and  Peromyscus  calif  ornicus  parasiticus.  Behaviour,  19: 
177-207. 

Hall,  E.  R.  1946.  Mammals  of  Nevada.  Univ.  of  Calif.  Press,  Berkeley. 
xi  +  710  p. 

Hooper,  E.  T.  1958.  The  male  phallus  in  mice  of  the  genus  Peromyscus.  Misc. 
Pub.  Mus.  Zool.  Univ.  Mich.,  99: 1-59. 

Howard,  W.  E.  1948.  Dispersal,  amount  of  inbreeding,  and  longevity  in  a  local 
population  of  prairie  deer  mice  on  the  George  Reserve,  southern  Mich- 
igan.   Cont.  Lab.  Vertebr.  Biol.  Univ.  Mich.,  43:1-50. 

McCabe,  T.  T.  and  B.  D.  Blanchard.  1950.  Three  species  of  Peromyscus. 
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Nicholson,  A.  J.  1941.  The  homes  and  social  habits  of  the  woodmouse  Pero- 
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25:196-223. 


396 


ETHOLOGICAL  ISOLATION  IN  THE  CENOSPECIES  PEROMYSCUS  LEUCOPUS 

Howard  McCarley 
Department  of  Biology,  Austin  College,  Sherman,  Texas 

Accepted  December  30,  1964 


Peromyscus  leucopus  and  P.  gossypinus,  con- 
stituting the  cenospecies  Peromyscus  leucopus, 
have  diverged  genetically  .so  that  they  have  differ- 
ent morphological  and  adaptive  norms.  Genetic 
isolation,  however,  is  apparently  not  complete 
hecau.se  interspecific  hybridization  may  occur 
(Dice,  19,17;  McCarley,  1954a).  The  present 
paper  is  a  report  of  an  ethological  mechanism 
that  helps  maintain  the  genetic  distinctness  of  the 
two   species. 

Previous  studies  by  Dice  (1940),  Calhoun 
(1941),  and  McCarley  (19.54b,  1963)  showed  that 
leucopus  and  gossypinus  were  generally  ecologically 
separated  in  areas  of  sympatric  distribution: 
leucopus  in  upland  woods  and  gossypinus  in 
lowland  woods.  Overlapping  frequently  occurs, 
however,  during  the  winter  and  spring  reproduc- 
tive sea.sons  (McCarley,  1963).  Consequently, 
ecological  separation  alone  would  not  be  adequate 
to  account  for  the  few  recorded  examples  of 
natural  interspecific  hybrids  in  this  cenospecies 
(Howell,   1921;   McCarley,   1954a). 

Work  done  by  McCarley  (1953)  and  Bradshaw 
(1957)  using  the  procedures  of  Blair  and  Howard 
(1944)  suggested  that  continued  species  separa- 
tion of  leucopus  and  gossypinus  may,  in  part, 
depend  on  ethological,  or  species  discrimination 
mechanisms.  Experiments  were  begun  in  1959 
using  techniques  modified  from  the  procedures  of 
Blair  and  Howard  (1944).  These  tests  utilized 
three  individuals,  one  male  and  two  females  or 
one  female  and  two  males.  If  males  were  to  be 
tested,  a  male  was  placed  in  one  of  the  two 
middle  compartments  of  a  four-compartmented 
cage  and  was  free  to  move  between  these  two 
compartments.  A  leucopus  female  was  confined 
to  one  end  compartment  and  a  gossypinus  female 
to    the    other    end    compartment.     A    reciprocal 


arrangement  of  mice  was  used  when  females 
were  tested.  Each  combination  of  three  mice 
was  observed  daily,  usually  early  in  the  morning, 
for  not  less  than  5  nor  more  than  1 1  days.  Ob- 
servations were  discontinued  randomly.  If  the 
mouse  being  tested  was  observed  nesting  next  to 
the  mouse  of  its  own  .species,  it  was  recorded  as 
a  positive  observation,  otherwise  as  a  negative 
observation.  Only  mice  in  breeding  condition 
were  used.  Sympatric  mice  were  from  Leon 
County,  Texas.  Allopatric  leucopus  were  from 
Bryan  and  Tillman  counties,  Oklahoma;  allo- 
patric gossypinus  were  from  Nacogdoches  County, 
Texas. 

The  results  of  these  association  experiments  arc 
summarized  in  table  1.  Sympatric  leucopus  fe- 
males and  gossypinus  males  and  females  demon- 
strated a  significant  positive  association  with 
members  of  their  own  species  of  the  opposite 
sex.  Sympatric  leucopus  males  associated  with 
females  of  their  own  species  more  frequently 
than  with  gossypinus  females  but  the  deviation 
from  the  expected  was  insufficient  to  produce  a 
significant  x-  value.  Table  1  also  presents  the 
results  of  tests  utilizing  allopatric  stocks  of  leuco- 
pus and  gossypinus.  Allopatric  mice,  in  this 
instance,  did  not  associate  with  members  of  their 
own  species  significantly  more  often  than  with 
members  of  the  other  species.  (In  the  case  of 
allopatric  leucopus  females,  five  of  the  six  tested 
showed  a  preference  for  individuals  of  the  op- 
posite species.)  This  suggests  that  existing  iso- 
lating mechanisms  are  being  reinforced  (Koopman, 
1950)    in  sympatric  areas. 

McCarley  (1963)  pointed  out  that  in  areas 
where  leucopus  and  gossypinus  are  sympatric, 
the  general  restriction  of  leucopus  to  upland 
habitats  (as  opposed  to  the  situation  in  allopatric 


Table  1.     Results  of  discrimination  tests  using  three  mice  in  a  four-compartmented  cage 


No.   of 
tests 


No.  of 

individuals 

tested 


Positive 
observations 


Negative 
ob.senations 


X- 
values 


Sympatric 
Sympatric 
Sympatric 
Sympatric 
Allopatric 
Allopatric 
Allopatric 
Allopatric 


leucopus  males 
leucopus  females 
gossypinus  males 
gossypinus  females 
leucopus  males 
leucopus  females 
gossypinus  males 
gossypinus  females 


36 

19 

113 

78 

3.010 

34 

16 

330 

65 

88.000 

54 

18 

233 

126 

15.605 

20 

12 

126 

46 

18.604 

14 

7 

69 

36 

4.8,W 

9 

6 

25 

69 

10.297 

20 

10 

81 

52 

2.925 

12 

S 

54 

64 

0.423 

331 


397 


332 


NOTES  AND  COMMENTS 


areas  where  leucopus  occupies  both  uplands  and 
lowlands)  was  the  result  of  the  presence  of 
gossypinus  in  lowlands.  The  presence  of  an 
ethological  mechanism  in  the  form  of  species 
discrimination  would  support   this  hypothesis. 

This  study  was  supported  by  Grants  No.  G- 
8019  and  G-19387  from  the  National  Science 
Foundation.  In  addition  to  Austin  College,  facili- 
ties at  the  University  of  Oklahoma  Biological 
Station  and  Southeastern  Oklahoma  State  College 
were  provided  while  I  was  in  residence  at  these 
institutions. 

Literature  Cited 

Blair,  \V.  F.,  .and  W.  E.  Howard.  1944.  Ex- 
perimental evidence  of  sexual  isolation  between 
three  forms  of  mice  of  the  cenospecies 
Peromyscus  maniculatus .  Contrib.  Lab.  Vert. 
Biol.,  ijniv.  Michigan,  No.  26:    1-19. 

Bradshaw,  VV.  N.  1957.  Reproductive  isolation 
in  the  Peromyscus  leucopus  group  of  mice. 
M.A.  Thesis,  Univ.  of  Texas,  Austin. 

Calhoun,  J.  B.  1941.  Distribution  and  food 
habits  of  mammals  in  the  vicinity  of  the 
Reelfoot  Lake  Biological  Station.  Proc.  Tenn. 
Acad.  Sci.,  6:    207-225. 


Dice,  Lee  R.  1937.  Fertility  relations  in  the 
Peromyscus  leucopus  group  of  mice.  Contrib. 
Lab.  Vert.  Gen.,  Univ.  Michigan,  No.  4:    1-3. 

.     1940.     Relations  between  the  wood  mouse 

and  the  cotton-mouse  in  eastern  Virginia. 
J.  Mammal.,  21:     14-23. 

Howell,  A.  H.  1921.  A  biological  survey  of 
Alabama.  U.  S.  Dept.  of  Agric.  Bur.  Biol. 
Surv.,  North  Amer.  Fauna,  No.  45. 

KooPMAN,  K.  F.  1950.  Natural  selection  for 
reproductive  isolation  between  Drosophila 
pseudoobscura  and  Drosophila  persimilis. 
Evolution,  4:    135-148. 

McCarley,  Howard.  1953.  Biological  relation- 
ships of  the  Peromyscus  leucopus  species  group 
of  mice.     Ph.D.  Thesis,  Univ.  of  Texas,  Austin. 

.     1954a.     Natural      hybridization      in      the 

Peromyscus  leucopus  species  group  of  mice. 
Evolution,  8:    314-323. 

.     1954b.     The  ecological  distribution  of  the 

Peromyscus  leucopus  species  group  in  eastern 
Texas.     Ecology,    35:     375-379. 

.     1963.     The   distributional   relationships   of 

sympatric  populations  of  Peromyscus  leucopus 
and  P.  gossypinus.     Ecology,  44:     784-788. 


398 


ACTIVITY,  FOOD  CONSUMPTION  AND  HOARDING  IN 

HIBERNATORS 

By  Charles  P.  Lyman 

In  previous  papers  it  has  been  emphasized  that  the  phenomenon  of  hiberna- 
tion is  not  precisely  the  same  among  all  mammals  and  differs  even  among 
various  famihes  of  rodents.  For  example,  the  electroencephalograms  of  "le  sper- 
mophile"  (probably  Citellus  citellus)  and  the  woodchuck  (Marmota  monax) 
differ  markedly  in  hibernation  and  during  the  process  of  arousal  from  that  of  the 
golden  hamster  (Mesocricetus  auraius)  (Kayser,  Rohmer  and  Hiebel,  1951; 
Chatfield,  Lyman  and  Purpura,  1951;  Lyman  and  Chatfield,  1953).  The  rela- 
tively active  electroencephalograms  of  the  deeply  hibernating  ground  squirrel 
and  woodchuck  reflect  the  behavior  of  these  species,  for  they  respond  to  strong 
stimuli  with  uncoordinated  muscular  movements.  The  deeply  hibernating  ham- 
ster, on  the  other  hand,  is  totally  inert  until  the  process  of  arousal  is  well  under 
way. 

Another  important  difference  concerns  the  nutritional  requirements  during 
the  hibernating  period.  Most  rodents  that  hibernate,  including  the  woodchuck 
and  the  ground  squirrel,  become  extremely  fat  before  the  period  of  dormancy 
and  apparently  Uve  on  this  fat  during  hibernation  (Kayser,  1950).  In  contrast, 
the  golden  hamster,  at  least  in  the  laboratory,  loses  weight  when  exposed  to  cold 
and  actually  enters  hibernation  when  quite  lean  (Lyman,  1948).  Although  Citellus 


399 


546  JOURNAL  OF  MAMMALOGY  Vol.  S5  No.  4 

tridecemlineatus  (Howell,  1938)  and  many  other  hibernators  store  some  food, 
storage  appears  to  be  of  paramount  importance  in  the  hamster,  for  it  eats  during 
its  periodic  arousals  from  the  hibernating  state  and  apparently  cannot  live 
throughout  the  hibernating  period  if  there  is  no  food  available  (Lyman  and 
Leduc,  1953). 

The  experiments  described  below  were  designed  to  clarify  these  differences. 
The  food  and  water  intake  and  the  activity  of  a  series  of  hamsters  and  ground 
squirrels  were  measured  when  the  animals  were  kept  in  a  warm  environment  and 
compared  with  the  same  measurements  when  the  animals  were  exposed  to  cold 
and  when  they  hibernated. 

During  the  course  of  the  experiments  it  became  apparent  that  hamsters  which 
were  denied  food  for  storage  did  not  hibernate  as  soon  as  control  animals.  There- 
fore, a  second  experiment  was  designed  to  elucidate  this  point. 

MATERIALS   AND   METHODS 

Experiment  1 . — A  series  of  nine  male  hamsters  (Mesocricetus  auratus)  between 
15  and  20  weeks  of  age  was  housed  in  activity  cages  equipped  with  exercise 
wheels.  The  rotating  wheel  of  each  cage  was  36  cm.  in  diameter  and  11.5  cm.  wide, 
and  the  resting  cage  measured  38  cm.  long  by  23  cm.  deep  by  23  cm.  high.  The 
animals  were  fed  ground  Purina  chow  from  non-spillable  food  cups,  and  water 
was  supplied  from  non-spillable  water  containers.  Food  and  water  intake  and 
the  number  of  revolutions  of  the  activity  wheel  were  usually  measured  each 
day.  If  very  small  amounts  of  water  were  consumed  daily,  allowance  was  made 
for  evaporation  from  the  water  container. 

The  animals  were  maintained  under  these  conditions  for  five  to  nine  weeks  in 
the  fall  of  the  year  in  an  animal  stock  room.  The  environmental  temperature  was 
24  ±  2°C.  and  the  animals  were  exposed  to  between  eight  and  nine  hours  of  hght 
daily.  At  the  end  of  this  period  the  hamsters  were  moved  into  a  cold  room  main- 
tained at  5°  ±  2°C.,  which  was  illuminated  daily  for  eight  hours.  The  measure- 
ments were  continued  under  these  conditions. 

A  second  series  of  two  female  hamsters  of  15  weeks  of  age  and  two  female 
ground  squirrels  (Citellus  tridecemlineatus)  over  three  years  of  age  was  housed 
in  individual  cages  of  the  same  size  as  the  previous  experiment.  The  cages  were 
suspended  from  springs,  and  balanced  from  below  by  a  tambour  at  each  corner. 
Any  major  movement  of  the  animal  in  the  cage  depressed  one  or  more  of  the 
tambours.  This  was  recorded  pneumatically  by  means  of  a  tambour  and  a  stylus 
on  a  slowly  revolving  smoked  chart.  Food  and  water  intake  were  measured  as 
in  the  first  experiment,  and  the  animals  were  exposed  to  the  same  environmental 
conditions.  In  all  experiments,  when  an  animal  was  observed  to  be  hibernating, 
a  small  amount  of  fine  shavings  was  placed  on  its  back  so  that,  if  it  moved 
enough  to  displace  the  shavings,  this  could  be  noted  at  the  next  observation. 

Experiment  2. — In  order  to  test  the  effect  of  hoarding  on  hibernation  a  series 
of  six  male  and  six  female  hamsters,  15  weeks  old,  was  housed  in  individual 
cages  supplied  with  ample  shavings  in  the  cold  room  (5°  ±  2°C.).  They  were  fed 
water  ad  libitum  and  ground  Purina  Chow  in  non-spillable  food  containers. 


400 


Nov.,  1954  LYMAN— ACTIVITY  AND  FOOD  IN  HIBERNATORS  547 

Under  these  conditions  the  animals  were  unable  to  store  food,  as  is  their  in- 
variable custom  if  supplied  with  pellets  of  compressed  food.  These  animals  were 
observed  daily  and  the  day  on  w^hich  they  first  hiberated  was  noted. 

To  provide  a  controlled  comparison  with  the  experimental  animals,  the  rec- 
ords of  373  animals  that  had  been  obser\^ed  during  the  last  few  years  in  this 
laboratory  w^ere  used.  The  use  of  this  large  number  of  animals  was  Employed 
because  it  sheds  some  light  on  the  variations  encountered  in  a  large  group  of 
animals.  These  hamsters  were  housed  under  conditions  identical  with  the  ex- 
perimental animals  in  the  cold  except  that  they  were  fed  Purina  laboratory 
chow  checkers  and  hence  could  store  their  food. 

RESULTS 

The  nine  hamsters  in  the  wheel-type  activity  cages  consumed,  in  the  warm 
room,  an  average  of  7.8  gms.  (Standard  Deviation  1.7)  of  Purina  Chow  each 
day.  Omitting  one  animal  that  spilled  water  in  spite  of  all  precautions,  the 
water  consumption  averaged  11.1  cc.  (S.D.  1.2)  per  day.  The  animals  averaged 
7335  revolutions  (S.D.  1834)  of  the  wheel  each  24  hours.  It  was  apparent  that 
most  of  the  activity  took  place  at  night,  whether  the  animals  had  an  exercise 
wheel  or  whether  the  motion  of  the  cage  was  recorded.  There  was  no  clear  evi- 
dence of  regular  periodic  activity  other  than  the  diurnal  cycle. 

When  moved  to  the  cold  room,  the  food  intake  of  the  hamsters  invariably 
rose  and  averaged  12.9  gms.  (S.D.  2.3).  This  rise  is  statistically  highly  significant 
according  to  the  "t"  test,  for  P  is  less  than  .01.  The  water  intake  rose  to  16.3 
cc.  (S.D.  4.7)  per  day.  This  rise  is  also  highly  significant  in  spite  of  the  fact  that 
one  animal  showed  a  slight  decrease  in  water  intake  (from  11.3  to  10.5  cc./day). 
The  hamsters  were  no  more  active  in  the  cold  than  in  the  warm  room  as  meas- 
ured by  the  activity  w^heels,  averaging  7141  revolutions  (S.D.  3029)  per  day. 
Furthermore,  there  was  no  evidence  in  the  tambour  records  that  the  animals 
moved  about  in  their  cages  to  a  greater  extent  when  exposed  to  cold. 

Although  most  of  the  hamsters  provided  with  activity  wheels  were  kept  in  the 
cold  room  for  over  a  year,  only  one  animal  hibernated  on  and  off  for  54  days  after 
being  in  the  cold  for  44  days.  During  this  period  it  was  observed  to  be  awake  on 
21  different  days  and  the  longest  period  of  continuous  hibernation  was  three 
days.  In  contrast,  the  average  period  of  hibernation,  punctuated  by  brief  waking 
periods,  for  19  typical  controls  was  95.1  days  (S.D.  21.7).  Furthermore,  most 
hamsters  remain  continually  in  the  hibernating  state  for  protracted  periods, 
the  longest  recorded  in  this  laboratory  being  21  days. 

There  was  no  diminution  of  exercise  or  food  and  water  intake  in  the  days  just 
prior  to  entering  the  hibernating  state.  On  each  awakening  the  animal  ate,  drank 
and  ran  on  the  exercise  wheel.  Considering  only  the  21  days  that  the  animal  was 
awake,  it  averaged  4207  revolutions  of  the  wheel,  12.7  gms.  of  food,  and  25  cc. 
of  water  per  day.  This  animal  averaged  11,646  revolutions  of  the  wheel,  14.8 
gms.  of  food  and  21.9  cc.  of  water  per  day  in  the  cold  room  before  entering  hiber- 
nation. 

One  of  the  hamsters  maintained  in  the  tambour-recording  cages  hibernated 


401 


548  JOURNAL  OF  MAMMALOGY  Vol.  35,  No.  4 

after  only  11  days  exposure  to  cold,  but  the  total  hibernating  period  lasted  only 
18  days  during  ten  days  of  which  the  animal  was  observed  to  be  awake.  The 
period  in  the  cold  room  before  hibernation  took  place  was  too  short  to  give  a 
reliable  figure,  but  the  food  intake  increased  and  the  water  intake  decreased 
during  the  11  days.  There  was  no  evidence  that  food  and  water  intake  or  exercise 
decreased  in  the  last  few  days  just  prior  to  hibernation.  In  the  ten  days  the 
animal  was  awake  during  the  hibernating  period  it  averaged  8.4  gms.  of  food 
and  10  cc.  of  water  per  day.  This  compares  with  8.1  gms.  of  food  and  5.1  cc.  of 
water  per  day  in  the  eleven  days  before  hibernation. 

The  hamster  in  the  other  tambour-recording  cage  adopted  a  peculiar  storing 
habit  which  spoiled  the  records  of  food  intake  and  caused  the  abandonment  of 
records  on  this  animal,  but  also  led  to  Experiment  2  of  this  series.  This  hamster 
was  able  to  obtain  food  from  the  unspillable  food  cup  by  forcing  its  muzzle  into 
the  ground  dog  chow.  Upon  lifting  its  head  from  the  food  cup,  it  removed  the 
crumbs  clinging  to  its  vibrissae  with  its  fore  paws  and  transferred  them  to  its 
cheek  pouches.  After  it  had  obtained  a  satisfactory  amount  of  food  in  this  way, 
it  carried  it  to  a  far  corner  of  the  cage  and  stored  it  in  the  manner  observed  in 
hamsters  fed  sohd  pellets  of  food.  This  animal  hibernated  on  the  72nd  day 
after  exposure  to  cold. 

Ground  Squirrels. — In  the  62  days  of  observation  prior  to  exposure  to  cold, 
ground  squirrel  no.  1  averaged  7.0  gms.  of  food  per  day  and  12.2  cc.  of  water. 
During  this  period  its  weight  dropped  from  266  gms.  to  237  gms.  Ground  squirrel 
no.  2  averaged  10.9  gms.  of  food  per  day  and  22.5  cc.  of  water,  and  its  weight 
dropped  only  from  275  to  267  gms.  Both  animals  were  very  fat  at  the  start  of  the 
experiment. 

In  sharp  contrast  to  the  hamsters,  the  two  ground  squirrels  hibernated  within 
24  hours  after  being  exposed  to  cold.  Ground  squirrel  no.  1  hibernated  over  a 
period  of  62  days,  at  the  end  of  which  time  the  animal  was  moved  to  the  warm 
room  because  of  its  emaciated  condition.  Of  the  62  days,  it  was  observed  to  have 
moved  enough  to  displace  the  shavings  on  its  back  on  14  days  and  was  active 
enough  to  cause  movement  of  the  cage  for  a  total  period  of  171  hours,  or  12  per 
cent  of  the  time.  During  the  time  it  was  awake  it  ate  a  total  of  16  gms.  of  food 
and  drank  87  cc.  of  water.  It  lost  111  gms.  body  weight  during  the  62  days  of  the 
sojourn  in  the  cold. 

Ground  squirrel  no.  2  hibernated  over  a  period  of  120  days  after  which  it  was 
moved  to  the  warm  room.  During  this  period  it  was  observed  to  have  lost  the 
shavings  from  its  back  on  23  days  and  was  active  enough  to  move  the  cage  for  a 
total  of  225  hours  or  8  per  cent  of  the  time.  During  the  time  it  was  awake  it  ate  a 
total  of  6  gms.  of  food  and  drank  no  water.  It  lost  130  gms.  body  weight  during 
the  120  days. 

Storing  Experiment. — The  twelve  hamsters  that  were  moved  to  the  cold  room 
but  not  allowed  to  store  food  hibernated  after  an  average  period  of  97.6  days 
(S.D.  20.4).  The  earliest  hibernation  occurred  on  the  54th  day  and  the  latest  on 
the  114th  day.  The  average  time  before  entering  hibernation  was  approximately 
the  same  for  both  sexes.  Once  in  the  hibernating  state,  the  animals  remained 


402 


Nov.,  1954  LY^^IAN— ACTIVITY  AND  FOOD  IN  HIBERNATORS  549 

in  this  condition,  with  the  usual  periodic  awakening,  for  a  period  of  about  three 
months.  Thus  the  length  of  the  hibernating  period,  once  started,  was  not  cur- 
tailed. 

Of  the  252  control  animals  that  entered  hibernation  the  average  time  before 
the  hibernating  state  occurred  was  56.6  days  (S.D.  33.2).  The  shortest  period 
before  hibernation  occurred  after  moving  to  the  cold  room  was  three  days  and 
the  longest  was  218  days.  On  the  other  hand,  121  animals  of  the  control  groups 
died  before  entering  the  hibernating  state.  The  average  time  when  death  oc- 
curred after  moving  to  the  cold  room  was  71.5  days  (S.D.  67.2). 

In  a  statistical  comparison  between  the  time  of  onset  of  hibernation  in  the  12 
hamsters  deprived  of  storing  and  the  252  controls  that  hibernated,  P  is  less  than 
.01.  This  highly  significant  difference  shows  that  the  abihty  to  store  food  has  a 
profound  effect  on  the  occurrence  of  hibernation.  On  the  other  hand,  the  data  on 
the  other  121  control  animals  show^  that  in  a  large  population  of  hamsters  in  the 
laboratory,  some  animals  will  Uve  in  the  cold  and  eventually  die  T\athout  enter- 
ing hibernation.  Therefore  it  may  be  more  accurate  to  include  the  animals  that 
died  in  the  cold  with  the  other  control  animals.  If  the  total  span  of  life  in  the 
cold  of  these  animals  is  averaged  with  the  total  time  in  the  cold  before  hiberna- 
tion in  other  controls,  one  obtains  a  figure  of  61.4  days  (S.D.  47.4).  When  this 
figure  is  compared  with  the  97.6  days  for  the  experimental  animals  the  difference 
between  the  two  figures  is  still  found  to  be  highly  significant  according  to  the 
Fisher  "t"  test  (P  <.01).  In  other  w^ords,  the  possibility  that  the  marked  delay 
in  the  onset  of  hibernation  in  the  non-storing  hamsters  is  due  to  chance  is  less 
than  one  in  100. 

DISCUSSION 

The  increased  food  and  water  intake  of  hamsters  when  exposed  to  cold  is 
tj''pical  of  mammals  that  do  not  hibernate,  and  is  to  be  expected  mth  the  in- 
crease of  metabolic  rate.  That  the  metabolic  rate  does  increase  in  hamsters 
when  exposed  to  cold  can  be  seen  by  comparing  the  figure  1014  cc.  02/K/hr. 
for  golden  hamsters  at  29.6°  (Kayser,  1940)  or  930  cc.  Os/K/hr.  at  30-34°C. 
(Adolph  and  Lawrow,  1951)  with  2877  cc.  02/K/hr.  at  5°C.  (Lyman,  1948). 
These  reactions  are  in  sharp  contrast  to  the  almost  immediate  hibernation  and 
cessation  of  eating  and  drinking  that  took  place  w^hen  the  two  ground  squirrels 
were  exposed  to  cold.  Although  ground  squirrels  do  not  invariably  hibernate 
within  24  hours  after  exposure  to  cold,  as  Johnson  (1930)  has  amply  demon- 
strated, still  the  onset  of  hibernation  is  usualty  quite  rapid.  On  the  other  hand, 
of  the  more  than  1000  hamsters  exposed  to  cold  in  this  laboratory,  the  shortest 
recorded  time  before  hibernation  occurred  was  three  days,  with  most  animals 
far  exceeding  this  figure. 

The  hibernating  phase  of  the  two  hamsters  recorded  here  cannot  be  regarded 
as  typical,  because  the  period  was  curtailed  and  the  animals  awoke  more  often 
than  is  normal.  However  all  indications  are  that  golden  hamsters  keep  up  high 
food  and  water  intake  and  remain  active  up  to  the  time  they  hibernate.  Further- 
more, the  data  emphasize  that  the  hamsters  will  consume  considerable  nourish- 


403 


550  JOURNAL  OF  MAMMALOGY  Vol.  35,  No.  4 

ment  each  time  they  wake  from  hibernation.  Although  observations  in  the  wil'd 
on  the  golden  hamster  are  lacking,  the  European  hamster  is  known  to  be  an 
inveterate  hoarder  of  food,  so  much  so  that  the  German  word  "hamster"  means 
to  hoard  or  store  in  anticipation  of  need.  It  is  highly  probable  that  hamsters 
do  not  have  access  to  water  when  they  are  holed  up  for  the  winter,  and  it  is 
reasonable  to  suspect  that  metabolic  water  and  water  from  the  stored  food  are 
their  only  sources.  The  data  indicate,  however,  that  the  animals  will  drink  a 
considerable  quantity  if  water  is  available. 

The  second  experiment  demonstrates  clearly  that  the  ability  to  store  food  has 
a  profound  effect  on  the  time  of  onset  of  hibernation.  Waddell  (1951)  has  shown 
that  noxious  conditions  such  as  illuminating  the  food  bin  will  increase  the  stor- 
age of  food  by  hamsters,  and  McCleary  and  Morgan  (1946)  have  demonstrated 
similar  reactions  in  the  rat  when  it  is  exposed  to  cold.  The  denial  of  the  ability 
to  hoard  when  stimulated  to  do  so  by  cold  must  upset  the  behavioral  pattern 
of  the  animal  so  that  the  onset  of  hibernation  is  delayed,  or,  in  the  case  of  one 
animal  in  the  cage  on  tambours,  the  period  of  hibernation  abnormally  shortened. 
This  takes  place  in  spite  of  the  fact  that  there  is  obviously  ample  food  obtainable 
at  all  times  from  the  food  containers. 

Again  in  contrast  to  the  hamsters,  the  ground  squirrels  hardly  touched  food 
or  water  while  they  were  exposed  to  cold  and  the  fast  is  reflected  in  the  great 
loss  of  body  weight.  This  loss  of  weight  bears  out  the  recent  work  of  Kayser 
(1952)  with  the  European  ground  squirrel  (Citellus  citellus).  He  was  able  to  show 
that  the  large  weight  losses  observed  in  animals  during  the  hibernating  period 
were  not  due  to  loss  of  weight  during  hibernation,  but  were  directly  correlated 
with  the  amount  of  time  the  animals  were  awake  during  that  period,  for  the 
process  of  arousal  and  the  awake  condition  consumed  a  great  deal  of  energy. 
Thus  in  ground  squirrel  no.  1,  which  was  awake  a  much  larger  proportion  of  the 
time,  the  weight  loss  was  much  faster  (1.8  gms./day)  than  in  ground  squirrel 
no.  2  (1.1  gms./day). 

Although  laboratory  experiments  can  not  completely  clarify  the  conditions 
that  occur  in  the  wild,  it  seems  justifiable  to  draw  from  these  results  a  sharp 
distinction  l^etween  the  preparation  for  hibernation  in  animals  such  as  the 
ground  squirrel  on  the  one  hand,  and  the  hamster  on  the  other.  Under  stimuli 
which  have  yet  to  be  elucidated,  the  former  animals  grow  extremely  fat  in  the 
period  previous  to  hibernation.  Exposure  to  cold  is  then  apt  to  cause  almost 
immediate  hiberation.  If  hibernation  does  not  occur  at  once,  denial  of  food  will 
hasten  it  (Johnson,  1930,  confirmed  in  these  laboratories).  Although  the  ground 
squirrel  stores  food  (Howell,  1938),  it  is  apparent  that  it  can  survive  repeated 
awakenings  with  practically  no  nourishment  by  utilizing  its  stored  fat.  From  all 
indications  the  woodchuck  (Marmota  monax)  is  very  similar  to  the  ground  squir- 
rel, for  it  becomes  extremely  obese  by  fall,  and  does  not  even  store  food  in  its 
burrow  (Merriam,  1884). 

The  hamster,  on  the  other  hand,  apparently  makes  no  physiological  prepara- 
tion for  hibernation  until  actually  exposed  to  cold.  Under  the  stimulus  of  cold 
exposure,  it  stores  food  and  loses  weight.  If  food  storage  is  denied,  hibernation 


404 


Nov.,  1954  LYMAN— ACTIVITY  AND  FOOD  IN  HIBERNATORS  551 

is  delayed.  Food  storage  is  essential  for  the  maintenance  of  the  hamster  during 
the  hibernating  period,  for  the  energy  necessary  for  the  periodic  awakening  is 
soon  exhausted  if  the  stored  food  is  removed  and  the  animal  cannot  eat  during 
the  periods  of  activity  (Lyman  and  Leduc,  1953).  Unpubhshed  experiments  in 
these  laboratories  have  conclusively  shown  that,  in  contrast  to  the  ground 
squirrel,  denial  of  food  or  water  will  never  cause  hibernation  in  the  hamster, 
which  is  precisely  what  might  be  expected  in  view  of  the  importance  of  stored 
food.  Thus  the  golden  hamster  is  provided  with  a  check  against  hibernation 
before  food  has  been  stored,  which,  under  natural  conditions,  must  protect  the 
animal  against  starvation  during  the  hibernating  period. 

How  the  lack  of  food  hoarding  can  delay  hibernation  is  a  problem  in  itself. 
Indications  are  that  it  is  not  the  only  psychic  factor  which  can  influence  the 
onset  of  hibernation,  for  of  the  nine  animals  with  activity  wheels  only  one  hiber- 
nated for  a  very  short  period,  though  all  were  exposed  to  cold  for  over  a  year. 
Possibly  exercise  on  activity  wheels  itself  may  halve  an  effect  on  the  onset  of 
hibernation.  In  any  event,  it  is  evident  that  a  behavior  pattern  such  as  storing 
can  have  a  profound  effect  on  the  onset  of  hibernation  in  the  hamster.  That 
behavior  must  be  considered  along  with  all  the  physiological  factors  when  at- 
tempting to  resolve  the  cause  of  hibernation  certainly  compounds  the  com- 
plexity of  the  problem. 

SUMMARY 

In  a  series  of  experiments  with  golden  hamsters  (Mesocricetus  auratus)  and 
thirteen-lined  ground  squirrels  {Citellus  tridecemlineatus)  it  was  found  that  the 
former  animals  did  not  hibernate  at  once,  but  increased  their  food  and  water 
intake  when  moved  to  a  cold  environment,  while  the  amount  of  exercise  taken 
remained  unchanged.  In  the  two  hamsters  that  eventually  hibernated  there  was 
no  decrease  of  eating,  drinking  or  exercise  up  to  the  time  of  hibernation.  The 
hamsters  ate  and  drank  considerable  quantities  and  exercised  to  some  extent 
on  each  awakening  from  hibernation.  Hamsters  that  were  prevented  from  hoard- 
ing food  showed  a  marked  delay  in  entering  hibernation. 

In  contrast,  the  ground  squirrels  hibernated  within  24  hours  after  exposure  to 
cold.  In  their  periodic  wakenings  the  ground  squirrels  ate  and  drank  almost 
nothing  and  in  consequence  lost  much  of  their  stored  fat. 

It  is  concluded  that  the  ground  squirrel  is  stimulated  in  some  unknown  way 
to  prepare  for  hibernation  by  becoming  extremely  obese.  Exposure  to  cold  brings 
on  hibernation  quickly  and  the  animal  lives  almost  exclusively  on  his  stored 
fat  during  the  hibernating  period.  The  golden  hamster,  on  the  other  hand,  does 
not  fatten  prior  to  hibernation,  but  is  stimulated  by  cold  to  store  food.  This  food 
is  used  during  the  periodic  arousals  in  the  hibernating  period,  and  without  the 
store  the  animal  would  perish.  Denial  of  the  ability  to  hoard  causes  a  delay  in 
the  onset  of  hibernation  and  thus  must  provide  the  animal  with  a  check  against 
premature  hibernation  that  would  result  in  starvation. 

Acknowledgement. — This  research  was  supported  by  a  grant  under  U.  S.  Air 
Force  Contract  AF  33  (038)-18133. 


405 


552  JOURNAL  OF  MAMMALOGY  Vol.  35,  No.  4 

LITERATURE  CITED 

Adolph,  E.  F.  and  J.  W.  Lawrow.  1951.  Acclimatization  to  cold  air;  hypothermia  and 
heat  production  in  the  golden  hamster.  Am.  Jour.  Physiol.,  166:  62-74. 

Chatfield,  p.  O.,  C.  p.  Lyman,  and  D.  P.  Purpura.  1951.  The  effects  of  temperature 
on  the  spontaneous  and  induced  electrical  activity  in  the  cerebral  cortex  of  the 
golden  hamster.  Electroencephalography  and  Clinical  Neurophysiol.,  3:  225- 
230. 

Howell,  A.  H.  1938.  Revision  of  the  North  American  ground  squirrels.  N.  A.  Fauna 
No.  56. 

Johnson,  G.  E.  1930.  Hibernation  of  the  thirteen-lined  ground  squirrel  Citellus  tri- 
decemlineatus  (Mitchill).  V.  Food,  light,  confined  air,  precooling,  castration 
and  fatness  in  relation  to  production  of  hibernation.  Biol.  Bui.,  59:  114-127. 

Kayser,  C.  1940.  Les  ^changes  respiratoires  des  hibernants.  Theses,  Fac.  d.  sci.  d. 
rUniversit^  de  Strasbourg,  1-364.  Also  in  Annales  de  Physiol,  et  Physicochimie 
biologique,  15  and  16,  1939,  1940. 

.     1950.     Le  sommeil  hibernal.  Biol.  Rev.,  25:  255-282. 

.    1952.     La  d^pense  d'^nergie  des  mammif^res  hibernants  pendant  toute  la  dur^e 

de  I'hibernation.  Arch.  d.  Sci.  Physiol.,  6:  193-212. 

Kayser,  C,  F.  Rohmer  and  G.  Hiebel.  1951.  L'E.E.G.  de  I'hibernant.  L6thargie  et 
r^viel  spontan^  du  spermophile.  Essai  de  reproduction  de  I'E.E.G.  chez  le  sper- 
mophile  r^veill6  et  le  rat  blanc.  Rev.  Neurologique,  84:  570-578. 

Lyman,  C.  P.  1948.  The  oxygen  consumption  and  temperature  regulation  of  hibernating 
hamsters.  Jour.  Exp.  Zool.,  109:  55-78. 

Lyman,  C.  P.,  and  P.  O.  Chatfield.  1953.  Hibernation  and  cortical  electrical  activity 
in  the  woodchuck  {Marmota  monax).  Science,  117:  533-534. 

Lyman,  C.  P.  and  E.  H.  Leduc.  1953.  Changes  in  blood  sugar  and  tissue  glycogen  in 
the  hamster  during  arousal  from  hibernation.  Jour.  Cell,  and  Comp.  Physiol., 
41 :  471-492. 

McCleary,  R.  a.  and  C.  T.  Morgan.  1946.  Food  hoarding  in  rats  as  a  function  of  en- 
vironmental temperature.  Jour.  Comp.  Psychol.,  39:  371-378. 

Merriam,  C.  H.  1884.  The  vertebrates  of  the  Adirondack  Region.  Trans.  Linn.  Soc. 
N.  Y.,  2:9-214. 

Waddell,  D.  1951.  Hoarding  behavior  in  the  golden  hamster.  Jour,  of  Comp.  and  Phys- 
iol. Psychol.,  44:383-388. 

Department  of  Anatomy,  Harvard  Medical  School  and  Museum  of  Comparative  Zoology, 
Harvard  University.  Received  December  IS,  1953. 


406 


RADIO  TRANSMITTER-COLLARS  FOR  SQUIRRELS' 

ROGER  O.   BEAL,  Waterloo  Wildlife  Experiment  Station,  Ohio  Division  of  Wildlife,   New  Marshfield 


Abstract:  An  adjustable  plastic  transmitter-collar  suitable  for  the  gray  squirrel  {Sciurus  carolinensis) 
and  fox  squirrel  {Sciurus  niger)  was  developed.  It  can  be  attached  at  the  trap  site  within  5  min. 
Placed  on  23  squirrels,  the  transmitter-collar  permitted  35-45  days  of  radio-tracking  data  to  be  ob- 
tained from  each  squirrel. 


Transmitter-collars  have  been  used  suc- 
cessfully on  rabbits,  hares,  and  raccoons 
( Mech  et  al.  1965 ) .  This  paper  describes  a 
transmitter-collar  which  was  found  satis- 
factory for  use  on  the  gray  squirrel  and  fox 
squirrel.  The  author  believes  that  this  same 
type  of  apparatus  can  be  attached  to  other 
mammals. 

The  electronic  components  for  a  squirrel 
transmitter-collar  were  mounted  on  a  self- 
locking,  11-inch  adjustable  plastic  hospital 
ID  bracelet  (purchased  from  Aloe,  1831 
Olive  St.,  St.  Louis,  Missouri).  The  com- 
ponents were  then  waterproofed  with  syn- 
thetic latex  rubber  and  wrapped  with  a 
layer  of  plastic  tape  ( Fig.  1 ) . 

The  antenna  loop  was  made  the  same 
size  on  each  transmitter-collar;  its  circum- 
ference was  measured  for  a  snug  fit  over 
the  head  of  the  largest  anticipated  squirrel. 
The  plastic  bracelet,  not  the  antenna  loop, 
is  the  adjustable  component  of  the' collar 

(Fig.  1). 

Average  weight  of  the  completed  trans- 
mitter-collars was  0.75  oz.  The  transmitter 
battery  life  averaged  35-45  days,  with  a 

^  A  contribution  from  Ohio  P.-R.  Project  W- 
105-R. 


range  of  %  to  VA  miles,  as  determined  by 
the  Drake  2-B  receiver  and  two  Hy-Gain 
5-element  beams. 

The  behavior  of  a  penned  gray  squirrel 
with  a  transmitter-collar  attached  during  a 
2-month  observation  period  appeared  nor- 
mal. The  squirrel  ate  regularly  and  moved 
without  hindrance.  At  the  end  of  the  test 
period,  the  squirrel  was  in  good  physical 
condition  and  the  neck  hair  was  not  worn. 

In  the  wild,  squirrels  were  livetrapped 
in  a  wooden  box  trap,  and  removed  from 
the  trap  with  heavy  leather  gloves.  The 
activated  transmitter-collar  was  slipped 
over  the  head  of  the  squirrel,  adjusted  to 
the  correct  fitting,  permanently  snap-locked, 
and  the  loose  end  of  the  collar  cut  off.  The 
squirrel  was  ear-tagged  and  then  released. 
This  entire  procedure  was  performed  at  the 
trap  site  by  two  workers,  and  required  5 
minutes  or  less. 

Between  February,  1964,  and  August, 
1966,  transmitter-collars  were  attached  to 
23  squirrels  (6  adult  gray  males,  11  adult 
gray  females,  4  adult  fox  males,  1  adult 
fox  female,  and  1  juvenile  fox  male).  In 
15  cases  squirrels  were  recovered  with  the 
transmitter-collar  attached.    In  all  but  one 


407 


374        Journal  of  Wildlife  Management,  Vol.  31,  No.  2,  April  1967 


Fig.   1.     Construction   sequence  of   transmitter  on   adjustable 
plastic   hospital    ID   bracelet. 


adult  male  fox  squirrel  which  was  re- 
trapped  after  1  month  of  radio-tracking. 
Its  neck  had  a  deep  cut,  possibly  caused 
by  the  edge  of  the  collar.  The  transmitter- 
collar  was  removed  and  the  squirrel  re- 
leased. The  animal  was  retrapped  4 
months  later  and  a  transmitter-collar  was 
attached  after  examination  showed  that  the 
neck  had  completely  healed. 

There  is  evidence  that  the  plastic  brace- 
let will  break  and  free  the  transmitter  after 
the  duration  of  batter>'  life.  A  gray  squirrel 
was  trapped  in  May,  1965,  tagged  and  re- 
leased. In  August,  1965,  this  animal  was 
retrapped  without  the  transmitter-collar. 
Examination  of  several  recovered  collars 
showed  that  they  were  brittle  after  being 
worn  for  a  month  or  more. 

In  three  instances  collars  were  chewed, 
presumably  by  another  squirrel.  However, 
this  did  not  appear  to  be  a  serious  problem. 

The  transmitter-collar  described  meets 
the  requirements  for  continued  study  by 
radio  telemetry  of  squirrel  behavior  in 
southeastern  Ohio  forests. 

LITERATURE  CITED 

Mech,  L.  D.,  V.  B.  KuECHLE,  D.  W.  Warner, 
AND  J.  R.  Tester.  1965.  A  coUar  for  at- 
taching radio  transmitters  to  rabbits,  hares, 
and  raccoons.  J.  Wildl.  Mgmt.  29(4) :898- 
902. 


case,  the  squirrels  appeared  in  good  physi- 
cal condition.    The  one  exception  was  an      Received  for  publication  September  14,  1966. 


408 


SECTION  5— PALEONTOLOGY  AND  EVOLUTION 

If  there  be  one  unifying  principle  that  pervades  all  of  biology,  it  is  that  of 
evolution.  Not  only  is  this  evident  in  consideration  of  the  papers  here  repro- 
duced (which  range  from  one  that  deals  in  part  with  intrapopulational  varia- 
tion up  to  those  concerned  with  higher  taxonomic  categories),  but  it  also  is 
evident  in  the  contents  of  virtually  all  other  papers  chosen  for  inclusion  in  this 
antholog)'.  The  few  selections  in  this  section,  then,  provide  but  a  glance  at 
some  aspects  of  mammalian  evolution. 

Linked  inseparably  with  the  e\olutionary  process  is  the  fossil  record,  which 
is  unusually  good  for  some  groups  of  mammals  and  provides  much  of  the  raw 
data  for  phylogenetic  considerations.  For  papers  relating  to  paleontolog}%  we 
have  chosen  one  on  a  local  fauna  ( Hibbard ) ,  one  ( Wilson )  that  alludes  to  the 
importance  of  sound  geographic  and  stratigraphic  data  and  that  ties  in  with 
the  historic  record,  one  (Radinsky)  that  deals  with  evolution  and  early  radia- 
tion of  perissodact>'ls,  and  two  on  rodents,  one  a  classic  early  paper  by  Miller 
and  Gidle>^  in  which  the  major  groups  of  that  extremely  complex  order  are 
outlined,  and  the  other  a  modern  treatment  of  the  same  problem  by  Wood  ( see 
also  Wood,  1959).  The  study  by  Guthrie  compares  evolutionary  change  in  mo- 
lar teeth,  using  both  fossil  and  Recent  species  oi'Microtiis,  and  thus  stresses  the 
on-going  evolutionary  process.  The  short  paper  by  Reed  clearly  presents  an 
interesting  problem  arising  from  attempts  to  classify  some  early  relatives  of 
man. 

The  essay  by  Durrant  and  Hansen  places  biogeography  in  the  evolutionary 
framework.  Some  of  the  species  of  ground  squirrels  mentioned  by  them  are 
treated  also  in  the  serum  protein  analysis  of  Nadler  and  Hughes  included  in 
Section  1.  The  paper  by  Jansky  is  interesting  because  it  provides  an  excellent 
example  of  evolutionary  trends  in  features  other  than  those  directly  related  to 
"hard  anatomy." 

The  literature  of  mammalian  evolutionary  and  paleontological  studies  is 
wddely  scattered.  Aside  from  the  journals  and  bibliographic  sources  mentioned 
in  the  Introduction,  the  interested  student  should  consult  Evolution,  a  quar- 
terly journal  published  by  the  Society  for  the  Study  of  Evolution,  and  the 
Journal  of  Paleontology.  He  should  also  be  aware  of  the  Bibliography  of 
Fossil  Vertebrates,  1959-1963,  compiled  by  Camp  et  at.  (as  well  as  earlier  vol- 
umes in  the  same  series)  and  the  News  Bulletin  of  the  Societ>'  of  Vertebrate 
Paleontolog}'. 

Romer's  textbook,  Vertebrate  Paleontology  (1966)  and  Simpson's  (1945) 
The  Principles  of  Classification  and  a  Classification  of  Mammals  are  especially 
recommended  as  sources  of  considerable  information  on  the  fossil  history  and 
evolution  of  mammals,  and  we  would  be  remiss  not  to  mention  also  Zittel's 
1891-93)  classic  Handbuch  der  Palaeontologie  (volume  4,  Mammalia).  Three 
substantial  longer  papers  on  systematics  and  evolution  of  special  groups  are 
Shotwell's  (1958)  study  of  aplodontid  and  mylagaulid  rodents,  Dawson's 
(1958)  review  of  Tertiary  leporids,  and  Black's  (1963)  report  on  the  Tertiary 
sciurids  of  North  America.    Extensive  paleofaunal  studies  of  note  are  many; 


409 


those  by  Hibbard  (1950)  on  the  Rexroad  Formation  from  Kansas  and  by 
Wilson  (1960)  on  Miocene  mammals  from  northeastern  Colorado  serve  as 
excellent  examples. 


410 


South  African  Journal  of  Science 
Suid-Afrikaanse  Tydsl<rif  vir  Wetenskap 

The  Association,  as  a  body,  is  not  responsible  for  the  statements  and  opinions  advanced  in  its  publications. 
Die   Vereniging    is    nie,    as    'n    liggaam,    verontwoordel  ik  vir   die  verklanngs   en   opmies   wat   in   sy   tydsknfte 

voorkom  nie. 


Vol./Deel  63 


JANUARY         1967        JANUARIE 


No.  1 


THE  GENERIC  ALLOCATION  OF  THE  HOMINID  SPECIES 
HABILIS  AS  A  PROBLEM  IN  SYSTEMATICS 

CHARLES  A.  REED 


'T'HE  recent  controversial  discussion,  in 
Current  Anthropology  (Oct.  1965)  and 
elsewhere,  concerning  the  correct  generic 
placement  of  the  Lower  Pleistocene  hominid 
species  liahilis  (Leakey,  Tobias,  and  Napier, 
1964),  depends  for  its  solution  upon  which 
one  of  two  kinds  of  philosophy  of  systematics 
is  followed.  None  of  the  participants  in  the 
discussion  have  emphasized  this  particular 
aspect  of  the  issues,  but  an  understanding  of 
these  concepts  is  basic  to  both  argument  and 
solution. 

If  one  is  impressed  with  the  phylogenetic 
approach  to  the  study  of  fossils,  stressing 
the  implications  of  those  evolutionary  inno- 
vations found  in  them  which  place  a  parti- 
cular group  at  the  beginning  of  a  new 
evolutionary  line,  leading  in  time  to  new 
adaptive  possibilities,  then  the  classification 
will  be  vertical  ('classification  by  clade'). 
Utilizing  this  approach  to  zoological  syste- 
matics the  investigator  will  emphasize  the 
importance  of  the  new  evolutionary  direction 
(the  new  adaptive  plateau  being  approached), 
by  placing  his  fossils  in  the  taxon  with  the 
advanced  forms  derived  from  them.  Leakey, 
Tobias,  and  Napier  did  exactly  this  when 
they  placed  the  population  habilis,  from 
Bed  I  of  Olduvai  Gorge,  Tanzania,  in  the 
genus  Homo  (Fig.  1). 

The  alternate  approach  to  systematics  is 
"classification  by  grade,"  wherein  the  investi- 
gator emphasizes  in  his  taxonomic  system. 


as  he  emphasizes  in  his  own  thinking  about 
the  material,  the  greater  or  lesser  degree  of 
morphological  likenesses  between  two  popu- 
lations which  have  essentially  reached,  at  the 
generic  or  specific  levels,  a  considerable 
similarity.  Obviously,  the  individuals  of 
habilis  are  anatomically  more  similar  to 
individuals  of  Australopithecus  africanus 
that  they  are  to  ourselves  as  Homo  sapiens, 
or  even  to  individuals  of  the  mid-Pleistocene 
taxon  H.  erectus.  Robinson  (1965a,  b)  and 
separately  Howell  (1965),  seeing  clearly  this 
essential  anatomical  similarity  between 
africanus  and  habilis,  wish  to  emphasize 
what  to  them  is  a  clear  closeness  of  biological 
relationship  by  placing  the  two  populations 
together  in  the  same  genus,  Australopithecus 
in  this  instance.* 

The  issues  involved  have  roots  deep  in  the 
history  of  post-Darwinian  systematics,  parti- 
cularly as  practised  by  palaeontologists. 
Simpson  ( 1 96 1 )  has  summarized  the  problems 
with  a  suggestion  for  a  solution  which 
attempts    (although    in    my    opinion    not 

•  The  mentioning  of  two  genera,  but  only  two,  as  comprising  ttie 
known  Quaternary  hominids  is  done  on  the  basis  of  the  general 
usage  of  the  authors  involved  in  the  controversy  presently  being 
considered,  and  with  the  view  that  Paranthropus  is  probably  best 
considered  as  a  sub-genus  of  Ausiralopiihecus.  We  must  not 
forget,  however,  that  Mayr  (1950)  advocated  that  all  Quaternary 
hommids  be  included  in  Homo,  a  practice  followed  only  inter- 
mittently thereafter  but  espoused  in  at  least  two  recent  textbooks 
(Brace  and  Montagu.  1965;  Buetlner-Janusch,  1966).  There  is 
also  another  possible  point  of  view,  the  one  that  habilis  be  included 
within  Homo  erecius,  probably  as  a  subspecies,  although  Tobias 
(1965b)  has  indicated  that  on  the  basis  of  present  evidence  this  is 
a  conclusion  with  which  he  could  not  agree. 


South  African  Journal  of  Science 


January,  1967 


411 


Fig.  1 :  Phylogeny  and  classification  of  the 
Family  Hominidae,  as  presently  understood 
(after  Tobias,  1%5a).  The  dotted  line  represents 
the  boundary  in  time  and  between  the  taxa 
Homo  and  Australopithecus  as  conceived  on  the 
basis  of  classification  by  clade;  the  dashed  line 
represents  the  same  concepts  on  the  basis  of 
classification   by  grade. 


successfully)  to  combine  the  two  approaches. 
An  earlier  paper  by  myself  (Reed  1960),  as 
based  on  publications  listed  in  its  biblio- 
graphy, states  these  particular  issues  in  a 
shorter  article  and  also  points  out  the 
logical  consequences  of  accepting  either 
system,  that  "by  clades"  or  the  contrasting 
one,  "by  grades." 

Neither  system  is  necessarily  correct,  nor 
either  wrong;  they  simply  are  based  on  two 
different,  and  in  my  opinion  mutually 
exclusive,  approaches  to  the  systematic 
organization  of  biological  populations  in  a 
time-continuum.  For  this  reason,  systematics 
remains  an  art  and  is  not  a  science,  depending 
upon  the  opinion  of  trained  investigators  for 
decisions  which  eventually  are  or  are  not 
followed  by  larger  numbers  of  people  who 
are  interested  in  the  fossils  and  the  phylogeny, 
but  have  neither  the  time  nor  training  to 
study  the  materials  in  detail. 


Our  problems  with  the  systematics  emerg; 
irrevocably  from  the  pattern  of  a  continuous 
flow  of  genes,  generation  by  generation,  and 
from  the  occasional  divisions  of  a  popu- 
lation's gene  pool  into  separate  evolutionary 
streams. 

The  vertical  type  of  classification  based  on 
clades  is  possible  only  if  a  population  has 
proved  its  survival  value  by  becoming  the 
ancestral  type  of  a  new  lineage,  and  if  we 
have  found  a  good  record  of  these  happen- 
ings. Thus  if  the  population  habilis  had 
become  extinct  during  the  period  of  the 
formation  of  Bed  I  at  Olduvai  Gorge,  its 
evolutionary  potential  would  be  unrecog- 
nizable and  its  remains  would  most  certainly 
be  classified  with  Australopithecus  by  what- 
ever subsequent  intelligent  being  was  doing 
the  paleontology.  The  Homo-ness  of  habilis 
lies  in  those  characters  which  we  can  recog- 
nize as  being  important  in  initiating  the 
lineage  Homo  only  because  we  have  a 
record  of  that  lineage.  Until,  however,  we 
had  as  complete  a  record  of  that  hneage  as 
we  finally  now  have,  systematics  by  clade 
was  not  possible. 

A  bit  of  an  analogy,  involving  non- 
hominid  lineages  with  which  we  are  not 
personally  involved,  may  help  to  clarify  the 
principles.  Thus  the  phylogenies  of  two 
super-families,  those  of  the  horses  (Equoidea) 
and  of  the  tapirs  (Tapiroidea),  diverged 
early  in  the  Eocene.  The  first-known  indi- 
vidual fossils  of  each  of  these  two  super- 
families  are  extremely  similar,  but  each— to 
the  eye  of  the  expert  — indicates  its  affinities 
to  its  known  descendants  by  what  might 
appear  to  be,  but  is  not,  a  trifle  of  dental 
pattern  (Radinsky,  1963).  Where  the  fossil 
record  is  as  complete  as  with  these  perisso- 
dactyls,  the  solution  of  the  systematic 
problems  has  typically  been  to  include  in 
different  clades  (families  or  super-famihes) 
different  populations  which  on  the  basis  of 
similarity  of  anatomical  form  would  be 
grouped  at  the  grade  level  as  closely  related 
genera  or  as  species  in  the  same  genus.  If, 
at  this  Eocene  level  of  evolution,  one  of 
these  ancestral  groups,  such  as  Hyracotherium 
(ancestral  to  all  later  "horses"  sensu  lato), 


Januarie  1967 


Suid-Afrikaanse  Tydskrif  vir  Wetenskap 


412 


had  become  extinci,  no  palaeontologist 
would  be  capable  of  recognizing  its  potential 
"horse-ness"  and  Hyracolherium  would 
today  be  classified  as  a  primitive  tapir. 
Conversely,  if  Homogalax,  the  earliest  of  the 
tapiroid  line,  had  become  extinct  without 
issue,  undoubtedly  it  would  today  be  classi- 
fied as  an  Eocene  equid. 

In  general,  as  the  gaps  in  the  fossil  record 
of  any  lineage  have  been  filled,  the  tendency 
has  been,  often  without  any  realization  of 
the  philosophy  of  the  systematics  involved, 
to  shift  from  a  horizontal  (grade)  type  of 
classification  to  the  vertical  (clade)  type,  and 
the  recent  flurry  of  published  opinions  as  to 
the  formal  position  of  the  species  habilis 
illustrated  a  repetition  of  this  historical 
pattern.  Tobias  (1965c)  has  stated  that  there 
is  general  agreement  as  to  the  meaning  of 
the  morphological  data  and  the  validity  of 
the  evolutionary  position  of  the  fossils 
included  in  the  population  habilis  from 
Bed  I  at  Olduvai  Gorge;  if  precedent  has 
any  value  as  a  guide,  we  may  safely  assume 
that  habilis  will  remain  in  Homo. 

In  general,  the  Primates  have  been  classi- 
fied on  the  principle  of  grades,  typical  of 
groups  with  an  incomplete  fossil  record  and 
thus  lacking  well-defined  lineages.  As  more 
fossils  are  found  and  the  phyletic  pattern 
becomes  clearer,  various  parts  of  the  sub- 
order (grade)  Prosimii  will  become  con- 
tinuous with  at  least  two  lineages  (platyrrhine 
and  catarrhine)  of  the  suborder  (grade) 
Anthropoidea.  and  slowly  the  present  pattern 
of  the  systematics  will  change. 

Exactly  this  sort  of  change,  to  the  surprise 
of  some,  is  what  is  occurring  in  the  Homini- 
dae.  due  to  the  filling  of  the  gaps  priorly 
existing  between  the  groups  called  Australo- 
pithecinae  and  Homininae.  We  should 
realize  also  that,  as  now  defined,  the  names 
applied  to  extinct  populations  of  Homo 
remain  as  grade  concepts,  as  has  already 
been  stated  clearly  by  Tobias  and  von 
Koenigswald  (1964).  Thus,  if  and  when 
human  fossils  are  found  to  fill  the  near-void 
now  existing  between  the  latest  erectus  and 
the  earliest  acknowledged  neandertals,  the 


whole  present  taxonomic  scheme  will  neces- 
sarily be  changed  from  the  horizontal  to 
the  vertical.  Perhaps  that  agonizing  re- 
appraisal will  be  easier  then  — as  indeed 
I  hope  it  will  be  now  at  the  habiUs  level  — 
if  we  realize  that  it  is  inevitable. 


REFERENCES   CITED 

Brace,  C.  L.  and  M.  F.  Ashley  Montagu  (1965): 
Man's  evolution:  An  introduction  to  physical 
anthropology.  New  York,  The  Macmillan  Com- 
pany. 

Buettner-Janusch,  John  (1966):  Origins  of  Man: 
Physical  Anthropology.  John  Wiley  and  Sons,  Inc. 
New  York. 

Howell,  F.  Clark  (1965):  Early  man.  New  York: 
Life  Nature  Library,  Time  Incorporated. 

Leakey,  L.  S.  B.,  Tobias,  P.  V,  and  Napier,  J.  R. 
(1964):  A  new  species  of  genus  Homo  from 
Olduvai  Gorge.  Nature  202:7-9.  (Reprinted  1965 
in  Current  .Anthropology.  6:424-27). 

Mayr.  Ernst  (1950):  Taxonomic  categories  in  fossil 
hominids.  Cold  Spring  Harbor  Symposia  in  Quanti- 
tative Biology  15:109-18. 

Radinsky.  Leonard  (1963):  Origin  and  evolution  of 
North  American  Tapiroidea.  Peabody  Museum 
of  Natural  History,  Yale  University,  Bulletin  17, 
1-106. 

Reed,  Charles  A.  (1960):  Polyphyletic  or  mono- 
phyletic  ancestry  of  mammals,  or:  What  is  a 
class?   Evolution  14,  314-22. 

Robinson,  J.  T.  (1965a):  Homo  'habilis'  and  the 
australopithecines.    Nature  205.  121-24. 

(1965b):    Comment   on    "New  discoveries  in 

Tanganyika :  Their  bearing  on  hominid  evolution," 
by  Phillip  V.  Tobias.  Current  Anthropology  6. 
403-6. 

Simpson,  George  Gay  lord  (1961 ):  Principles  of  animal 
taxonomy.  New  York:  Columbia  University  Press. 

Tobias,  Phillip  V.  (1965a):  Early  man  in  East  Africa. 
Science.  1949.  22-33. 

—  (1965b):    Homo  habilis.  Science  149.  918. 

(1965c):     New    discoveries    in    Tanganyika: 

Their  bearing  on  hominid  evolution.  Current 
Anthropology  6.  391-99. 

Tobias,  P.  V.  and  Von  Koenigswald.  G.  H.  R.  (1964): 
A  comparison  between  the  Olduvai  hominines  and 
those  of  Java  and  some  implications  for  hominid 
phylogeny.  Nature  204.  515-18.  (Reprinted  1965 
in  Current  Anthropology  6.  427-31). 

Departments  of  Anthropology  and 

Biological  Sciences, 
University  of  Illinois  at  Chicago  Circle, 
Chicago, 
Illinois, 
U.S.A. 


South  African  Journal  of  Science 


January.  1967 


413 


MICROTUS  PENNSYLVANICUS  (ORD)  FROM  THE  HAY 
SPRINGS  LOCAL  FAUNA  OF  NEBRASKA 

CLAUDE  W.  HIBBARD 
Department  of  Geology,  University  of  Michigan 


Abstract — Microtus  pennsylvanicus  (Ord),  the  meadow  vole,  a  member  of  the 
present  fauna  of  Nebraska,  is  known  from  fossil  remains  in  the  American  Museum 
of  Natural  History,  which  were  taken  with  the  Hay  Springs  local  fauna  of  Sheridan 
County,  Nebraska.  On  the  basis  of  known  Pleistocene  faunas,  the  Hay  Springs 
mammals  are  post-Pearlette  ash  in  age.  The  fauna  appears  to  be  equivalent  to  those 
that  lived  during  the  late  Illiuoian  and  Sangamon. 


The  occurrence  of  Microtus  in  the  Hay 
Springs  local  fauna  of  Nebraska  has  long 
been  known  (Matthew.  1918,  p.  227;  Hay, 
1924,  p.  305;  Osborn,  1942,  p.  1010).  In  the 
spring  of  1944  while  studying  the  holotypes 
of  Ondatra  nebracensis  (Hollister)  and  Ca- 
promeryx  furcifer  Matthew,  I  examined  a 
lower  jaw  of  Microtus  from  the  Hay  Springs 
fauna  which  led  to  my  statement  (Colbert, 
etal.,  1948,  p.  625)  regarding  the  occurrence 
of  this  vole  in  that  fauna.  Through  the 
courtesy  of  Dr.  G.  G.  Simpson  I  have  been 
given  permission  to  study  and  figure  these 
specimens. 


In  the  American  Museum  of  Natural 
History  collection  there  are  parts  of  three 
lower  jaws  and  two  left  upper  incisors  from 
the  Hay  Springs,  Nebraska  locality,  col- 
lected by  the  American  Museum  Expedition 
of  1897. 

Specimen  AMNH  2711  is  part  of  a  left 
lower  jaw  with  the  incisor,  Mi  and  Mj.  Mi 
consists  of  a  posterior  loop,  six  alternating 
triangles  and  an  anterior  loop.  The  sixth 
alternating  triangle  opens  into  the  anterior 
loop  (Text-fig.  IB).  Mjconsistsof  a  posterior 
loop  and  four  closed  alternating  triangles. 
Enamel  is  lacking  on  the  anterior  face  of 


414 


1264 


PALEONTOLOGICAL  NOTES 


Ml,  the  labial  and  lingual  sides  of  the  poste- 
rior loop  of  Ml  and  the  anterior  face  of  M2. 
The  posterior  loop  of  M2  has  an  interrupted 
enamel  pattern.  A  narrow  dentine  tract  on 
the  labial  and  lingual  sides  of  the  loop  ex- 
tends from  the  occlusal  surface  to  the  base 
of  the  tooth.  The  anteroposterior  length  of 
the  occlusal  surface  of  Mi  and  M2  is  5.3  mm. 

A  fragmentary  right  lower  jaw,  AMNH 
2712,  contains  part  of  the  incisor,  Mi  and 
M2.  The  occlusal  dental  pattern  is  similar 
to  that  of  the  previous  specimen,  except  that 
the  sixth  alternating  triangle  opens  more 
widely  into  the  anterior  loop  (Text-fig.  IC). 
The  anteroposterior  occlusal  length  of  Mi- 
Miis  5.0  mm. 

Specimen  AMNH  2713  is  a  right  lower 
jaw  with  an  incisor  and  M1-M3.  The  occlusal 
pattern  is  like  that  of  the  other  two  speci- 
mens. M3  consists  of  a  posterior  loop  with 
the  first  and  second  alternating  triangles 
broadly  confluent.  The  third  is  closed  ofT 
from  the  fourth  triangle  (Text-fig.  ID).  The 
anteroposterior  occlusal  length  of  Mi  and 
M2  is  4.75  mm.;  that  of  M1-M3  is  6.5  mm. 
Dentine  occurs  in  the  reentrant  angles  of  the 
teeth  and  is  as  well  developed  as  in  recent 


specimens.  A  deep  pit  occurs  between  M3 
and  the  ascending  ramus  as  in  Recent  speci- 
mens of  Microtus  pennsylvanicus.  The  gen- 
eral shape  of  the  lower  jaw  is  like  that  of 
other  fossil  and  Recent  specimens  of  this  spe- 
cies. 

The  two  left  upper  incisors,  AMNH  2714, 
are  the  size  and  shape  of  those  of  the  Recent 
species. 

The  original  American  Museum  label  car- 
ries the  name  Arvicola  fagrestis  but  on  the 
back  of  the  label  is  written,  "A  note  from 
O.  P.  Hay  says:  Not  A.  agrestis — an  Euro- 
pean species.  Probably  Microtus  pennsylva- 
nicus. O.  P.  H."  At  what  time  O.  P.  Hay 
made  this  identification  is  unknown  but  it 
must  have  been  after  the  publication  of  his 
1924  paper. 

The  number  of  closed  alternating  tri- 
angles of  Ml  vary  (5  to  6)  in  both  Recent 
and  fossil  specimens.  Text-fig.  IE  is  an  oc- 
clusal view  from  a  specimen,  Univ.  Michigan 
31773,  taken  with  the  Berends  local  fauna  of 
Oklahoma.  Text-fig.  IF  is  an  occlusal  view  of 
a  specimen,  Univ.  Michigan  29333,  from  the 
Jinglebob  local  fauna.  Both  of  these  spec- 
mens  have  an  Mi  with  six  closed  alternating 


F         G 


Text-fig.  1 — Microtus  pennsylvanicus  (Ord),  occlusal  views  of  lower  dentitions.  All  XlO.  Drawings 
by  Michael  O.  Woodburne.  A,  UMMZ  30048,  left  Mj-M,,  Recent  specimen.  B,  AMNH  2711.  left 
Ml  and  M2,  Hay  Springs  local  fauna.  C,  AMNH  2712,  right  Mi  and  M2,  Hay  Springs  local 
fauna.  D,  AMNH  2713,  right  Mj-Mj,  Hay  Springs  local  fauna.  E,  UMMP  31773,  left  M1-M2, 
Berends  local  fauna.  F,  UMMP  29333,  left  Mi-Mj,  Jinglebob  local  fauna.  G,  UMMZ  30013.  left 
M1-M3,  Recent  specimen. 


415 


PALEONTOLOGICAL  NOTES 


1265 


triangles  posterior  to  the  anterior  loop.  The 
two  Text-figs.  lA  and  IG  of  Recent  speci- 
mens in  the  Museum  of  Zoology,  University 
of  Michigan,  are  given  for  comparison  with 
the  fossil  occlusal  patterns. 

Age  of  the  Hay  Springs  local  fauna. — A 
stratigraphic  control  is  lacking  on  this  fauna 
since  it  appears  that  the  exact  location  of  the 
quarry  or  quarries  is  unknown.  Matthew 
(1902,  p.  317)  gives  the  location  as  a  bone- 
bed  near  the  Niobrara  River,  not  far  from 
Hay  Springs. 

O.  P.  Hay  (1924,  p.  304)  makes  the  follow- 
ing statement  regarding  the  location: 

Many  species  of  fossil  vertebrates  have  been 
taken  on  Niobrara  River,  near  a  place  now 
known  as  Old  Grayson,  not  far  from  the  present 
town  of  Grayson,  from  excavations  known  in 
the  literature  as  the  "Hay  Springs  quarry."  The 
locality  is  said  to  be  along  a  ravine  about  a  mile 
away  from  the  Niobrara  River,  and  south  of  it. 

Schultz  &  Stout  (1948,  p.  564)  make  the 

following  remark  regarding  this  early  local 

ity: 

The  American  Museum  of  Natural  History  ex- 
peditions of  1893,  1897,  and  1916  conducted 
minor  quarry  operations  south  of  Hay  Springs, 
but  the  exact  locations  of  these  quarries  cannot 
now  be  determined. 

A  succession  of  Pleistocene  faunas,  for 
which  there  is  a  stratigraphic  control,  is 
known  from  Meade  County,  Kansas  and 
Beaver  County,  Oklahoma  (Hibbard,  1956, 
p.  146.  fig.  1). 

The  earliest  remains  of  Microtus  in  the 
Plains  region  are  known  from  the  Crooked 
Creek  formation  (Hibbard,  1949).  This  for- 
mation is  tentatively  considered  as  having 
been  deposited  during  Kansan  and  Yar- 
mouth time.  The  basal  part  of  this  formation 
consists  of  sand  and  gravel  (Stump  Arroyo 
member)  which  rests  unconformably  upon 
the  Meade  formation.  The  following  fossils 
have  been  taken  from  the  Stump  Arroyo 
member  (Hibbard,  1951)  in  Clark  and 
Meade  counties:  Megalonyx  sp.,  Stegomas- 
todon  sp.,  Stegomastodon  mirijicus  (Leidy), 
Nannippus  phlegon  Hay  and  Plesippus  cf. 
P.  simplicidens  (Cope).  So  far  Equus  s.s. 
and  Mammiithus  have  never  been  taken  from 
this  sand  and  gravel.  They  are  known  from 
later  deposits  of  this  region  (Hibbard,  1953). 
Above  this  sand  and  gravel  member  occurs 
sandy  silt,  silt,  clay,  Pearlette  ash,  clay,  silt 


and  sandy  silt  which  is  overlain  by  massive 
caliche.  Two  faunas  are  known  from  these 
deposits.  The  older,  the  Cudahy  fauna,  oc- 
curs in  the  base  of  the  Pearlette  ash  and  the 
underlying  silts,  and  is  considered  as  latest 
Kansan  in  age.  Frye,  Swineford,  &  Leonard 
(1948)  and  Frye  &  Leonard  (1952)  have 
shown  that  the  Cudahy  molluscan  fauna 
from  the  base  and  just  below  the  Pearlette 
ash  is  the  same  in  Nebraska  and  Kansas.  It 
is  therefore  evident  that  the  mammalian 
fauna  should  be  the  same  in  Kansas  as  in 
Nebraska  except  for  a  few  more  northern 
forms  that  may  occur  in  the  fauna  in  Ne- 
braska. It  is  in  this  fauna  that  the  remains 
of  Microtus  and  other  microtines  are  found. 
The  species  of  Microtus  that  have  been  taken 
in  this  fauna  are  extinct.  The  small  muskrat 
{Ondatra  kansasensis  Hibbard)  occurring  in 
this  fauna  is  not  as  advanced  or  as  large  as 
Ondatra  nebracensis  (Hollister)  from  the 
Hay  Springs  fauna.  The  Hay  Springs  musk- 
rat  is  also  more  advanced  than  the  small 
Ondatra  hiatidens  (Cope)  from  the  Port 
Kennedy  Cave  fauna  of  Pennsyhania 
(Hibbard,  1955). 

The  younger  Borchers  fauna  occurring  in 
the  Crooked  Creek  formation  is  found  above 
the  Pearlette  ash  and  is  tentatively  consid- 
ered as  Yarmouth  in  age.  The  two  micro- 
tines  known  from  this  fauna  are  Synapto- 
mys  landesi  Hibbard,  and  a  small  muskrat- 
like  vole,  not  as  advanced  as  the  older 
Ondatra  kansasensis. 

The  earliest  occurrence  of  Microtus  penn- 
sylvanicus  in  the  Plains  region  south  of 
Nebraska  is  in  the  Illinoian  Berends  local 
fauna  of  Oklahoma  and  the  Sangamon 
Jinglebob  fauna  of  Kansas.  It  is  well  known 
from  Wisconsin  faunas.  It  should  be  noted 
that  this  vole  which  is  now  a  common  mem- 
ber of  our  northern  North  American  fauna 
is  unknown  from  the  Port  Kennedy  Cave 
and  Cumberland  Cave  local  faunas  of  north- 
eastern United  States.  All  evidence  at  the 
present  time  points  to  a  rather  late  arrival 
of  this  form  in  our  North  American  fauna. 

In  Kansas  the  remains  of  Microtus  penn- 
sylvanicus,  Paramylodon  har la ni  (Owen)  (see 
Stock,  1925,  p.  120);  Mammuthus  imperator 
(Leidy),  Capromeryx  furcifer  Matthew,  and 
Equus  niobrarensis  Hay  are  known  only  from 
deposits  that  are  post-Pearlctte  ash  in  age. 
Rinker   (1949)    commented   on   the   resem- 


416 


1266 


PALEONTOLOGICAL  NOTES 


blance  of  the  Hay  Springs  fauna  to  the  Cra- 
gin  Quarry  fauna  and  its  equivalents  in 
Kansas. 

The  Hay  Springs  local  fauna  of  Matthew 
(1918)  and  Hay  (1924)  is  post-Pearlette  ash 
in  age  (late  Kansan).  All  faunal  evidence 
points  to  a  late  lUinoian  and  Sangamon  age. 
In  this  paper  the  assignment  of  Pleistocene 
subages  to  the  faunas  and  deposits  in  the 
nonglaciated  Plains  region  is  tentative. 

REFERENCES 

Colbert,  K.  H.,  et  al.,  1948,  Pleistocene  of  the 
Great  Plains:  Geo!.  Soc.  Am.  Bull.,  vol.  59,  p. 
541-630,  1  p!.,  11  fig. 

Frye,  J.  C,  &  Leonard,  .\.  B.,  1952.  Pleistocene 
geologv  of  Kansas:  Kans.  Geol.  Survey,  Bull. 
99,  p.  i-230,  19  pi.,  17  fig. 

,  SwiNEFORD,  .\d.\,  &  Leonard,  A.  B.,  1948, 

Correlation  of  Pleistocene  deposits  of  the 
Central  Great  Plains  with  the  glacial  section: 
Jour.  Geol.,  vol.  56,  no.  6,  p.  501-525,  2  pi.,  .? 
fig.,  1  table. 

Hay,  O.  p.,  1924,  The  Pleistocene  ol  the  Middle 
Region  of  North  America  and  its  vertebrated 
animals:  Carnegie  Inst.  Washington  Piibl., 
no.  322  A,  385  p.,  5  fig.,  29  maps. 

Hibbard,  C.  W.,  1949,  Pleistocene  stratigraphy 
and  paleontology  of  Meade  County  Kansas: 
Univ.  Michigan,  Contrib.  Mus.  Paleo.,  vol. 
7,  no.  4,  p.  63-90,  1  pi,  2  fig.,  3  maps 

,  1951,  \'ertebrate  fossils  from  the  Pleisto- 
cene Slump  Arroyo  member,  Meade  County, 


Kansas:     Univ.     Michigan,     Contrib.     Mus. 

Paleo.,  vol.  9,  no.  7,  p.  227-245,  6  pi.,  1  fig. 
,  1953,  l-'.quus  (.Asinus)  calobatus  Troxelland 

associated  vertebrates  from  the  Pleistocene  of 

Kansas:  Kansas  .\cad.  Sci.,  Trans.,  vol.  56,  no. 

1,  p.  111-126,  3  fig. 
,  1955,  Notes  on  the  mirrotine  rodents  from 

the  Port  Kennedv  Cave  deposit :  .Acad.  Nat. 

Sci.  Philadelphia,  Proc,  vol.  107,  p.  87-97,  2 

fij:- 
,  1956,  \'ertebratc  fossils  from  the   Meade 

formation  of  southwestern  Kansas:  Michigan 

.\cad.  Sci.,  Papers,  .Arts  and  Letters,  \-ol.  41, 

p.  145-203,  2  pi.,  16  fig. 

Matthew,  W.  D.,  1902,  List  of  the  Pleistocene 
fauna  from  Hav  Springs,  Nebraska:  .Am.  Mus. 
Nat.  Hist.,  Bull.,  vol.  16,  art.  24,  p.  317-322. 

,  1918.    Contribution    to   the   Snake   Creek 

fauna  with  notes  upon  the  Pleistocene  of  west- 
ern Nebraska:  Am.  Mus.  Nat.  Hist.,  Bull., 
vol.  38,  art.  7,  p.  183-229,  7  pi.,  20  fig. 

OsBORX,  H.  P.,  1942,  Proboscidea:  vol.  2,  p. 
805-1675,  18  pi.,  564  fig.,  Am.  Mus.  Press. 

RiNKER,  G.  C,  1949,  Tremarctotherium  from  the 
I^leistoccne  of  ^Meade  County,  Kansas:  Univ. 
Michigan,  Contrib.  Mus.  Paleo.,  vol.  7,  no.  6, 
p.  107-112,  1  pi. 

ScHiJi.TZ,  C.  B.,  &  Stout,  T._  M.,  1948,  Pleisto- 
cene mammals  and  terraces  in  the  Great  Plains: 
Geol.  Soc.  Am.,  Bull.,  vol.  59.  p.  553-588,  1  pi., 
4  fig.,  2  tables. 

Stock,  C,  1925,  Cenozoic  gravigrade  edentates 
of  western  North  .America:  Carnegie  Inst. 
Washington  Publ.,  no.  331,  p.  1-206,  47  pi., 
120  fig.' 

MvxrscRirr  ufckivi'd  May  7,  1956 


417 


88  PROC.  S.  D.  ACAD.  SCI.  XLIV  (1965) 

TYPE  LOCALITIES  OF  COPE'S 
CRETACEOUS  MAMMALS 

Robert  W.  Wilson 

Museum  of  Geology 

South  Dakota  School  of  Mines  and  Technology,  Rapid  City 

ABSTRACT 

It  is  generally  stated  in  paleontological  literature  that  J.  L.  Wortman 
found  the  types  of  two  species  of  Late  Cretaceous  mammals  in  unknown 
parts  of  South  Dakota.  These  species,  subsequently  described  and  named  by 
E.  D.  Cope,  are  Meniscoessus  conquistus  (probably  the  first  Cretaceous  mam- 
mal to  be  found  and  described),  and  Thalaeodon  padanicus.  They  are  the 
only  Cretaceous  mammals  of  published  record  from  the  state. 

Review  of  some  neglected  sources  of  information  leads  to  the  conclu- 
sion that:  (1)  the  type  of  Meniscoessus  conquistus  came  from  Dakota  Terri- 
tory, but  not  necessarily  from  South  Dakota,  and  (2)  E.  D.  Cope,  rather  than 
Wortman,  found  the  type  of  Thlaeodon  padanicus,  and  this  specimen  came 
from  Hell  Creek  beds  along  the  Grand  River  approximately  four  miles  south- 
east of  Black  Horse. 

E.  D.  Cope  named  and  described  two  genera  of  Cretaceous  mam- 
mals: these  were  the  multituberculate  Meniscoessus  in  1882,  and  the 
marsupial  Thlaeodon  in  1892,  with  type  species  M.  conquistus  and 
T.  padanicus  respectively.  Cope  credited  J.  L.  Wortman  with  the 
discovery  of  Meniscoessus  conquistus,  but  said  nothing  about  the 
type  locality.  In  his  description  of  Thlaeodon  padanicus,  he  said 
nothing  about  either  the  discoverer  or  the  place  of  discovery,  except 
to  state  that  the  upper  and  lower  jaws  were  found  about  one  hun- 
dred feet  apart,  but  probably  pertained  to  a  single  individual.  At  a 
considerably  later  time,  G.  G.  Simpson  (1929)  and  others  have  stated 
that  the  type  specimens  of  both  M.  conquistus  and  T.  padanicus  were 
found  by  Wortman  in  the  "Laramie"  [Lancel  of  South  Dakota,  but 
that  no  other  locality  data  were  available. 

The  Museum  of  Geology  of  the  South  Dakota  School  of  Mines 
and  Technology  has  been  exploring  the  Hell  Creek  (Late  Cretaceous) 
of  South  Dakota  for  mammals.'  In  an  attempt  to  gain  clues  as  to 
where  Wortman  might  have  found  his  specimens,  I  searched  such 
literature  as  was  available  to  me  with  care.  As  a  result,  I  have 
reached  tentative  conclusions  at  variance  with  those  of  Simpson. 

In  respect  to  Meniscoessus  conquistus  not  much  can  be  said  with 
assurance.  A  note  by  Wortman  (1885,  p.  296)  states  that  Hill  (Rus- 
sell?) and  Wortman  found  the  type  in  the  summer  of  1883  {sic,  but 


'  Work  supported  by  National  Science  Foundation  grant  G23646 


418 


PROC.  S.  D.  ACAD.  SCI.  XLIV  (1965)  89 


surely  1882)  in  Dakota.  Because  the  division  of  the  Territory  into 
the  present  states  of  North  and  South  Dakota  did  not  take  place 
until  1889,  the  question  arises  as  to  how  it  is  known  that  the  locality 
was  in  what  is  now  South  Dakota  if  nothing  is  known  about  the  de- 
tails of  the  locality.  The  only  slight  clue  I  can  uncover  is  that  a  year 
after  Wortman's  finding  of  Meniscoessus,  Cope,  himself,  was  explor- 
ing the  Cretaceous  of  the  Dakota  Territory.  In  a  letter  to  his  wife 
dated  August  28,  1883  (Osborn,  p.  306),  and  written  at  what  is  seem- 
ingly now  Medora,  North  Dakota,  he  says  in  describing  local  out- 
crops: "This  is  the  formation  from  which  Wortman  got  the  Menis- 
coessus."  This  sentence  can  be  taken  literally  as  simply  that  the 
specimen  came  from  Cope's  Laramie  Formation,  or  with  more  license 
that  he  meant  these  are  the  outcrops  from  which  the  specimen 
came.  In  the  same  letter,  he  wrote  that  he  planned  to  go  30  miles 
south  where  the  "badlands  are  said  to  be  exceptionally  bad."  If  he 
were  following  Wortman's  footsteps  at  this  point,  he  would  have 
been  approximately  45  miles  north  of  the  state  line.  After  proceed- 
ing this  far  south  along  the  Little  Missouri,  Cope  went  southeast- 
ward to  White  Buttes  before  turning  back  to  Medora.  White  Buttes 
was  his  closest  approach  to  South  Dakota  on  this  trip  of  several 
days,  and  he  was  then  still  about  30  miles  from  South  Dakota.  It 
may  be  that  in  the  general  area  bounded  by  Medora,  Marmath,  and 
Bowman,  North  Dakota,  Wortman  found  the  type  of  Meniscoessus, 
but  even  if  he  did  not,  it  is  highly  uncertain  that  the  discovery  was 
made  in  the  South  Dakota  of  today.  As  a  matter  of  fact,  most  of  the 
outcrops  south  of  the  state  line  for  some  miles  may  be  somewhat  too 
high  in  the  geologic  section  for  Meniscoessus. 

In  respect  to  the  type  locality  of  Thlaeodon  padanicus,  there  are 
several  bits  of  evidence  suggesting  (1)  that  Cope  rather  than  Wort- 
man found  the  specimen,  and  (2)  that  it  was  in  fact  found  in  South 
Dakota  along  the  south  bank  of  the  Grand  River  southeast  of  Black 
Horse.  These  lines  of  evidence  are  itemized  below. 

1.  Nowhere  in  the  account  published  in  1892  in  the  American 
Naturalist  does  Cope  credit  Wortman  with  discovery  of 
Thlaeodon  padanicus. 

2.  The  Indian  name  for  the  Grand  River  is  Padani,  and  hence 
the  specific  name  T.  padanicus  is  a  broad  hint  as  to  locality. 

3.  In  the  year  of  its  discovery.  Cope  prospected  along  the  Grand 
River.  Wortman  was  also  in  South  Dakota,  but  was  occupied 
by  collecting  in  the  Big  Badlands  to  the  south,  and  such  Cre- 
taceous collections  as  he  made  seemed  to  have  been  in  the 
Lance  Creek  area  of  Wyoming.  In  any  case,  even  before  the 
summer  of  1892,  he  had  left  the  employ  of  Cope,  and  was 
working  for  the  American  Museum  of  Natural  History. 


419 


90  PROC.  S.  D.  ACAD.  SCI.  XLIV  (1965) 


4.  In  a  letter  to  his  wife  dated  July  17,  1892  (Osborn,  p.  431), 
Cope  says,  "We  made  noon  camp  on  the  bank  of  Grand  R.  and 
then  climbed  the  bluffs  on  the  S.  side  leaving  the  Rock  Creek 
and  this  subagency  to  the  N.  We  followed  this  high  land, 
driving  through  the  Grass,  sometimes  with,  sometimes  with- 
out trail.  We  had  great  distance  views,  fine  air,  and  plenty 
of  flowers.  During  the  afternoon  we  crossed  Five  (sic,  for 
Fire)  Steel  Creek,  which  comes  in  from  the  South.  As  evening 
approached  thunderclouds  arose  in  the  W.  and  I  began  to 
think  of  camp.  Oscar  however  drove  on,  and  the  Sioux  boy 
kept  ahead.  As  it  grew  late  we  turned  down  a  low  hill  to  the 
left  and  climbed  a  low  bench  at  the  foot  of  an  opposite  hill. 
I  saw  a  low  bare  bank  and  lying  around  white  objects.  I  told 
Oscar  to  let  me  get  out,  as  I  thought  I  saw  bones.  Sure  enough 
the  ground  was  covered  with  fragments  of  Dinosaurs,  small 
and  large,  soon  we  found  water  and  stopped  for  camp." 
ingly  thought;  see  1931,  p.  415). 

5.  In  the  letter  above-mentioned  (Osborn,  p.  443),  Cope  states 
his  results  as,  "In  the  3  days  I  collected  I  got  21  species  of 
vertebrates,  of  which  3  are  fishes,  and  all  the  rest  reptiles 
except  one  mammal.  This  is  a  fine  thing,  the  most  valuable 
I  procured,  and  new  as  to  species  at  least;  and  it  throws  im- 
portant light  on  systematic  questions."  This  mammalian 
specimen  is  not  otherwise  accounted  for  in  collections  if  it  is 
not  the  type  specimen  of  T.  padanicus  (as  H.  F.  Osborn  seem- 

Reference  to  a  geological  map  (Firesteel  Creek  Quadrangle, 
South  Dakota  State  Geological  Survey)  shows  that  the  closest  ex- 
posures from  whence  these  bones  could  come  after  the  Firesteel 
crossing  is  in  the  vicinity  of  section  25,  T.  20N,  R.  22E,  or  sections  29 
and  30,  T.  20N,  R.  23E.  A  good  skeleton  of  Anatosaurus  in  the  Mu- 
seum of  Geology  collections  is  from  the  southwest  corner  of  the 
SW14  of  section  25,  T.  20N,  R.  21E.  The  type  of  Thlaeodon  padanicus 
surely  came  from  somewhere  in  the  area  of  these  localities. 

LITERATURE  CITED 

Cope,  E.  D.,  1882,  Mammalia  in  the  Laramie  Formation.    Amer.  Nat.,  v.  16, 

pp.  830-831. 
,  1892,    On  a  New  Genus  of  Mammalia    from  the  Laramie 

Formation.   Amer.  Nat.,  v.  26,  pp.  758-762,  pi.  xxii. 

Osborn,  H.  F.,  1931,  Cope:    Master  Naturalist.    Princeton  Univ.  Press,    xvi 
plus  740  pp.,  30  figs.   Princeton. 

Simpson,  G.  G.,  1929,    American  Mesozoic  Mammals.    Mem.  Peabody  Mus. 
Yale  Univ.,  v.  3,  pt.  1,  xv  plus  235  pp.,  62  text-figs.,  32  pis. 

Wortman,  J.  L.,  1885,  Cope's  Tertiary  Vertebrata.   Amer.  Jour.  Sci.  (3),  v.  30, 
pp.  295-299. 


420 


THE  ADAPTIVE  RADIATION  OF  THE  PHENACODONTID 

CONDYLARTHS  AND  THE  ORIGIN  OF  THE 

PERISSODACTYLA^ 

Leonard  B.  Radinsky 
Department  of  Biology,  Brooklyn  College,  Brooklyn,  New  York 

Accepted  March  28,  1966 

The  mammalian  order  Condylarthra  in-  still   unspecialized   enough   to   have   given 

eludes    a    heterogeneous    assemblage     of  rise  to  Hyracotherium.     (The  occurrence 

small-  to  medium-sized  archaic  omnivores  of  incipient  mesostyles  in  a  small  number 

and    herbivores.     Most    families    in    the  of     Tetraclaenodon    specimens    does    not 

order    flourished    in    the    Paleocene    and  preclude    this   possibility;    the   alternative 

became  extinct  early  in  the  Eocene.  A  few  hypothesis,   that  proto-perissodactyls   and 

lineages,  however,  developed  crucial  adap-  Tetraclaenodon    were    independently    de- 

tations   which  led   to   their   emergence   as  rived  from  a  still  more  primitive  common 

new    orders    of    mammals,    one    of    which  ancestor,    requires    an    additional    compli- 

was  the  Perissodactyla.    The  origin  of  the  eating  factor — an  independent  acquisition 

Perissodactyla  is  better  documented  than  of  molar  hypocones  by  perissodactyls  and 

that  of  any  other  order  of  mammals  and  phenacodontids.)    Thus,  in  the  absence  of 

provides  an  excellent  opportunity  to  study  evidence  to  the  contrary,   Tetraclaenodon 

the  emergence  of  a  major  taxon.  may   be   considered   directly    ancestral    to 

Dental  evidence  indicates  that  perisso-  perissodactyls.  The  major  morphological 
dactyls  were  derived  from  the  condylarth  changes  involved  in  the  evolution  of  the 
family  Phenacodontidae.  To  view  in  Tetraclaenodon  stock  into  Phenacodus, 
proper  perspective  the  evolutionary  Ectocion,  and  Hyracotherium,  fall  into 
changes  which  led  to  the  origin  of  the  two  functional  categories,  one  concerned 
Perissodactyla,  it  will  be  necessary  to  with  mastication  and  the  other  with  loco- 
survey  the  adaptive  radiation  of  the  Phe-  motion, 
nacodontidae.  Mastication 

The  oldest  true  phenacodontid  condy-  Dentition 
larth,  Tetraclaenodon,  first  appears  in  ^he  main  changes  involved  in  the  evo- 
faunas  of  middle  Paleocene  age,  and  by  i^tjo^  of  the  phenacodontid  dentition  oc- 
the  begmning  of  the  late  Paleocene  ap-  ^ur  in  the  molar  teeth.  The  molars  of 
pears  to  have  radiated  mto  three  mam  Tetraclaenodon  (see  Fig.  1)  are  low- 
groups,  represented  respectively  by  Phe-  crowned,  with  low,  obtuse  cusps.  The 
«acorf«5,  £c/od(7«,  and  an  33  yet  unknown  ^-^^^  ^^^  ^^^^^^  ^pp^^  ^^1^^^  ^^^  ^^. 
proto-penssodactyl.  Forms  transitional  be-  ^^^^^^  ^^^^  ^^^  primitive  tritubercular 
tween     Tetraclaenodon     and     Phenacodus  ^^1^^     ^^^^^^  ^     ^^^  ^^^.^.^^  ^^  ^  ^^^^^^ 

(primitive    species    of    Phenacodus),    and  .                xi.     i                    rr^ 

,  ^,             ^  .      7         ,             ^      T^  \     •  main  cusp,  the  hypocone.    There  are  two 

between     Tetraclaenodon     and     Ectocion  ,  ,.    ,     ,          .  \          ■,. 

,.,                 /--ji     •     \          1              u  i  relatively  large  intermediate  cuspules,  the 

(the  genus  Gtdleytna)  are  known,  but  no  ,          ,                   ,           ,    ,        , 

intermediates  between  Tetraclaenodon  and  P^-^toconule    and    metaconule,    and    broad 

the   most   primitive   known    perissodactyl,  ^"t^"^'"  ^"^  P°^t^"°^  ^^"g"^^-    '^^^  ^^^^^ 

the    early    Eocene    genus    Hyracotherium,  "PP^^   "^°^^^   ^^   ^"^^"^^   than   the   second 

have  vet  been  found.   However,  Tetraclae-  ^"^    ^^""^^    ^    hypocone.     In    the    lower 

nodon  is  the  most  advanced  form  which  is  "^^^^'^   ^^^  paraconid   has  been   reduced, 

leaving  two  main  anterior  cusps,  the  pro- 

^This  work  was  supported  in  part  by  National  ^^^onid  and  metaconid,  and  a  prominent 

Science  Foundation  Grant  GB-2386.  anterior  ridge,  the  paralophid.    There  are 

Evolution  20:  408-417.     September,  1966  408 


421 


ORIGIN  OF  PERISSODACTYLS 


409 


Fig.  1.  Second  and  third  molars  of  A.  Ectocion,  B.  Hyracotherium,  C.  Tetraclaenodon,  and  D. 
Phenacodus.  Lower  molars  of  Ectocion  and  Phenaodiis  have  the  same  basic  cusp  pattern  as  is  seen  in 
Tetraclaenodon  and  are  therefore  omitted.  All  about  X  3.  Abbreviations:  HY,  hypocone;  HCLD, 
hypoconulid;  MCL,  metaconule;  MES,  mesostyle;  MLH,  metaloph. 


three  posterior  cusps,  a  large  hypoconid 
and  slightly  smaller  entoconid  and  hypo- 
conulid. The  third  lower  molar  is  nar- 
rower posteriorly  than  the  second.  The 
wear  facets  on  the  molars  of  Tetraclaeno- 
don suggest  that  both  crushing  and  shear- 
ing occurred  in  mastication,  with  the  em- 
phasis apparently  on  crushing. 

The  teeth  of  Phenacodus  are  very  sim- 
ilar to  those  of  Tetraclaenodon,  having 
low,  obtuse  cusps  and  ridges.    The  main 


differences  are  the  development  of  a  small 
mesostyle  on  the  upper  molars  and  the 
enlargement  of  the  posterior  cingulum  into 
a  hypocone  on  the  third  upper  molar.  The 
upper  molars  are  relatively  long  (antero- 
posteriorly)  and  narrow.  As  in  Tetraclae- 
nodon, the  broad  low  cusps  are  more 
adapted  for  crushing  than  shearing.  The 
addition  of  a  hypocone  on  the  third  upper 
molar  increases  the  surface  area  available 
for  chewing.    The  mesostyle  is  not  large 


422 


410  LEONARD  B.  RADINSKY 

enough  to  add  significantly   to   the  ecto-  great  enlargement  of  the  hypoconulid.    (In 

loph  area.  the    first    and    second    lower    molars    the 

In   molars   of   Ectocion   the   cusps   are  hypoconulid  is  reduced.)    However,  even 

relatively  higher  and  more  acute  and  the  excluding    the    enlarged    hypoconulid,    the 

ridges  connecting  cusps  are  more  promi-  third  lower  molar  is  still  as  large  as  the 

nent  than  in  Tetraclaenodon  or  Phenaco-  second.      Finally,     the    lower    molars    of 

dus.   The  ectoloph  is  higher  relative  to  the  Hyracotherium   are    narrower    relative    to 

lingual  cusps  and  is  folded  into  a  prom-  the  uppers  than  is  the  case  in   the  phe- 

inent    mesostyle.     The    upper    molars    are  nacodontids. 

relatively  short  and  wide.    The  third  up-  The  changes  in  cusp  pattern  and  tooth 

per  molar  does  not  develop  a  hypocone.  proportions   in   evolution    from    Tetraclae- 

On  the  lower  molars  the  paraconid  is  lost  nodon  to  Hyracotherium  indicate  an  in- 

and  the  paralophid  no  longer  extends  to  crease  in  the  amount  of  shearing    (espe- 

the  metaconid  (as  it  does  in  Phenacodus) .  cially  along  transverse  crests)  and  a  cor- 

The  high,  narrow  cusps  and  ridges  provide  responding    decrease    in    the    amount    of 

steep    occlusal    surfaces,    indicating    rela-  crushing  in   mastication.    A   shift   toward 

tively  more  shear  and  less  crushing  than  increased  shearing  also  occurred  in  Ecto- 

occurred   in    Tetraclaenodon   or   Phenaco-  cion,  but  in  that  genus  the  emphasis  was 

dus.    The   prominent   mesostyle    increases  on  vertical  ectoloph   shear.    The  enlarge- 

the  length  of  ectoloph  available   for  ver-  ment  of  the  third  molars  in  Hyracotherium 

tical    shear    against    the    labial    sides    of  provided  greater  occlusal  surface  and  could 

ridges  on  the  lower  molars.  have    been    brought    about    simply    by    a 

The     molars     of    Hyracotherium,    like  slight  posterior  shift  of   the   molarization 

those  af  Ectocion,  have  relatively  higher  field.  The  greatly  enlarged  hypoconulid  of 

and  more  acute  cusps  and  ridges  than  do  the  third  lower  molar  served  the  function 

those   of    Tetraclaenodon   or   Phenacodus.  in  occlusion  of  a  paralophid  and  presum- 

However,    Hyracotherium    is    even    more  ably    developed    in    correlation    with    the 

advanced  in  this  respect  than  is  Ectocion,  molarization    (and    enlargement)    of    the 

for  the  crests  connecting  cusps  are  better  posterior  half  of  the  upper  third  molar, 

developed.    An  important  modification  in  The  relatively   narrower   lower  molars   of 

cusp  pattern  has  been  brought  about  by  Hyracotherium  required  a  greater  degree 

the  loss  of  the  protcone-metaconule  con-  of  transverse  jaw  movement  for  complete 

nection,    an    anterior    shift    of    the    meta-  occlusion  with  the  uppers  than  was  neces- 

conule  and   the  development  of  a  hypo-  sary  in  Tetraclaenodon. 


Jaw  Musculature 


cone-metaconule  crest.  These  changes  re- 
sult in  a  cusp  pattern  with  two  oblique 
tranverse  crests  (an  anterior  protoloph  The  structure  of  the  lower  jaw,  known 
and  posterior  metaloph)  separated  by  a  for  Phenacodus,  Ectocion,  and  Hyracothe- 
lingually  open  valley.  Correlated  with  the  rium  (see  Fig.  2),  provides  information  on 
changes  in  upper  molar  pattern,  in  the  the  relative  proportions  of  the  main  com- 
lower  molars  the  hypoconulid  has  been  ponents  of  the  jaw  musculature.  In  man- 
posteriorly  displaced,  leaving  the  posterior  dibles  of  Hyracotherium  the  coronoid 
sides  of  the  hypoconid  and  equally  large  process  is  relatively  smaller  and  the  angle 
entoconid  clear  for  shear  against  the  ante-  relatively  larger  than  in  Phenacodus  or 
rior  side  of  the  metaloph  above.  Another  Ectocion.  In  addition,  the  posterior  bor- 
new  feature  in  the  dentition  of  Hyracothe-  der  of  the  angle  is  thicker  and  more  heav- 
rium  is  the  enlargement  of  the  third  ily  scarred  (from  insertions  of  the  ex- 
molars.  In  Hyracotherium  the  upper  third  ternal  masseter  and  internal  pterygoid 
molar  has  a  hypocone  and  is  as  large  as  muscles)  in  Hyracotherium.  These  differ- 
the  second  molar.  The  third  lower  molar  ences  suggest  that  the  masseter  and  in- 
is  larger  than   the  second,  owing   to  the  ternal   pterygoid    muscles   were    relatively 


423 


ORIGIN  OF  PERISSODACTYLS 


411 


Fig.  2.  Lower  jaws  of  A.  Hyracotherium 
(after  Simpson,  1952),  X  %;  B.  Ectocion  (Yale 
Peabody  Mus.  no.  21211),  X  %;  C.  Phenacodus 
(Princeton  Univ.  no.  14864),  X  %■  AH  in  lat- 
eral view. 

larger,  and  the  temporalis,  which  inserts 
on  the  coronoid  process,  relatively  smaller 
in  Hyracotherium  than  in  the  phenaco- 
dontids. 

In  living  ungulate  herbivores  the  mas- 
seter-pterygoid  complex  is  larger  than  the 
temporalis,  while  in  carnivores  the  oppo- 
site is  true  (Becht,  1953,  p.  522;  Schu- 
macher, 1961,  pp.  143,  180).  In  carni- 
vores, jaw  movement  is  almost  entirely 
confined  to  adduction,  for  which  the 
temporalis  is  well  suited,  but  in  ungulates 
and  many  other  herbivores  transverse 
movement  is  important  in  mastication, 
and  for  transverse  movement  the  deep 
part  of  the  masseter  and  the  internal 
pterygoid  are  more  efficient  than  the 
temporalis  (Smith  and  Savage,  1959,  p. 
297).  Thus  the  relatively  larger  masseter 
and  internal  pterygoid  musculature  indi- 
cated by  the  jaw  structure  of  Hyracothe- 


rium suggests  increased  specialization  for 
lateral  jaw  movement  in  mastication.  This 
specialization  of  the  jaw  musculature  cor- 
relates with  the  narrower  lower  molars 
and  predominance  of  transverse  shear  in- 
dicated by  the  molar  cusp  patterns  of 
Hyracotherium. 

Locomotion 

Much  of  the  postcranial  skeleton  is 
known  for  Hyracotherium,  Phenacodus 
and,  to  a  lesser  degree,  Tetraclaenodon,  but 
that  of  Ectocion  is  largely  unknown. 
Therefore  the  following  discussion  of  loco- 
motory  adaptions  will  deal  mainly  with 
the  first  three  genera. 

Vertebral  Column 

Slijper  (1946,  p.  103)  pointed  out  that 
with  decreasing  mobility  of  the  vertebral 
column  in  ungulates  the  longissimus  dorsi 
shifts  its  insertion  posteriorly  from  lum- 
bar to  sacral  vertebrae  and  consequently 
the  neural  spines  of  the  lumbar  vertebrae 
become  less  cranially,  and  even  caudally, 
inclined.  In  Phenacodus  copei  (Amer. 
Mus.  Nat.  Hist.  no.  4378)  the  lumbar 
neural  spines  are  inclined  cranially  about 
15  degrees  from  vertical.  Kitts  (1956,  p. 
2 1 )  states  that  the  neural  spine  of  the 
last  lumbar  vertebra  of  Hyracotherium  is 
less  cranialy  inclined  than  that  of  Phe- 
nacodus. No  specimen  of  Hyracotherium 
available  to  me  preserves  lumbar  neural 
spines,  but  in  Heptodon  posticus,  an  early 
Eocene  tapiroid  similar  in  morphology  to 
Hyracotherium,  the  neural  spine  of  the 
last  lumbar  vertebrae  (Mus.  Comp.  Zool. 
no.  17670)  is  inclined  cranially  about  five 
degrees  from  vertical.  This  difference 
from  the  condition  in  Phenacodus  sug- 
gests that  the  vertebral  column  in  early 
perissodactyls  was  somewhat  less  flexible 
than  that  of  Phenacodus. 

Kitts  (1956,  p.  20)  states  that  the 
zygapophyses  of  the  lumbar  vertebrae  of 
Hyracotherium  are  embracing,  but  his  il- 
lustration {loc.  cit.,  fig.  3)  shows  what 
appears  to  be  a  relatively  flat  prezyga- 
pophysis,  similar  to  the  condition  in  Phe- 
nacodus. 


424 


412 


LEONARD  B.  RADINSKY 


Fig.  3.  Front  feet  of  A.  Hyracotherium  (composite  from  Kitts,  1957,  and  Osborn,  1929,  fig.  700), 
X  %;  B.  Tetraclaenodon  (composite  from  AMNH  nos.  2468  and  2S47a),  X  1 ;  C.  Phenacodus  (AMNH 
no.  2961),   X   Vs. 


Forelimb 

In  Tetraclaenodon  the  humerus  has  a 
prominent  deltoid  crest,  with  the  deltoid 
tubercle  located  on  the  distal  half  of  the 
shaft,  and  a  large  medial  epicondyle,  with 
an  entepicondylar  foramen.  The  proximal 
end  of  the  radius  is  about  twice  as  wide 
as  it  is  deep  (anteroposteriorly)  and  artic- 
ulates with  the  ulna  along  a  wide  flat 
facet,  indicating  loss  of  the  ability  to 
supinate.  The  carpus  (see  Fig.  3)  is  rela- 
tively low  and  wide,  and  has  been  called 
"alternating";  that  is,  in  dorsal  view  the 
scaphoid  rests  partly  on  the  magnum  and 
the  lunar  partly  on  the  unciform.  The 
amount  of  overlap,  however,  is  slight. 
Facets  on  the  distal  row  of  carpals  indi- 
cate that  there  were  five  digits;  except  for 
the  proximal  head  of  the  third  metacarpal, 
the  metacarpus  is  unkno\\Ti. 

The  humerus,  radius,  and  ulna  of  Phe- 
nacodus are  similar  to  those  of  Tetraclae- 
nodon, except  that  the  deltoid  crest  of  the 


humerus  is  slightly  weaker  and  the  deltoid 
tubercle  is  higher  on  the  shaft.  The  car- 
pus of  Phenacodus  has  been  described  as 
being  of  the  serial  t^pe,  i.e.,  with  the 
scaphoid  resting  solely  on  the  trapezoid 
and  trapezium,  and  the  lunar  only  on  the 
magnum.  This  arrangement  occurs  in  the 
large  species  of  Phenacodus,  P.  priniaevus, 
but  in  the  small  species  P.  copei  (AMNH 
no.  16125),  the  lunar  overlaps  the  unci- 
form to  about  the  same  degree  (which  is 
very  little)  as  in  Tetraclaenodon. 

The  less  prominent  deltoid  crest  and 
higher  deltoid  tubercle  suggest  that  the 
forelimb  of  Phenacodus  was  relatively  less 
powerful  but  perhaps  capable  of  more 
rapid  movement  than  that  of  Tetraclaeno- 
don. The  small  medial  displacement  of 
the  lunar  and  scaphoid,  resulting  in  loss 
of  the  lunar-unciform  and  scaphoid-mag- 
num articulations  in  large  species  of  Phe- 
nacodus, suggests  a  slight  increase  in 
importance  of  the  ulna  in  weight  support. 


425 


ORIGIN  OF  PERISSODACTYLS 


413 


The  forelimb  of  Hyracotherium  differs 
from  that  of  Tetraclaenodon  in  the  follow- 
ing features:  humerus  with  shorter  and 
less  prominent  deltoid  crest  and  more 
proximally  located  deltoid  tubercle,  greatly 
reduced  medial  epicondyle  (with  conse- 
quent loss  of  the  entepicondylar  foramen), 
and  sharper  intercondyloid  ridge  ( =  capit- 
ulum);  radiohumeral  index  of  about  1.0 
compared  to  0.8  in  Tetraclaenodon  and 
Phenacodus,  ulna  with  narrower,  less  mas- 
sive, more  symmetrical  olecranon;  carpus 
relatively  higher  and  narrower,  with  more 
extensive  articulations  between  elements; 
cuneiform  smaller  and  scaphoid  displaced 
laterally  to  extensively  overlap  unciform 
and  magnum,  respectively;  unciform,  mag- 
num, and  scaphoid  with  larger  posterior 
tuberosities;  first  digit  lost  and  trapezium 
reduced  to  a  tiny  nubbin;  remaining  meta- 
carpals relatively  longer  and  thinner  (the 
ratio  of  the  length  of  the  third  metacarpal 
to  the  humerus  is  1 :  2  compared  to  about 
1:3  in  Phenacodus  and  probably  also 
Tetraclaenodon);  fifth  metacarpal  rela- 
tively smaller. 

All  of  these  differences  indicate  in- 
creased specialization  for  running  in  Hy- 
racotherium. The  elongation  of  distal 
limb  segments  (radius  and  metacarpals) 
and  reduction  of  lateral  digits  increases 
the  length  of  stride  and  makes  the  limb  a 
more  effective  lever.  The  reduction  of 
the  medial  epicondyle  probably  correlates 
with  the  decreased  importance  of  the  pro- 
nator teres  (which  originates  on  that  epi- 
condyle), for  the  manus  is  fixed  in  a  per- 
manently pronated  position,  and  may  also 
correlate  with  the  decrease  in  importance 
of  the  ulna  as  a  weight-bearing  element 
of  the  forearm.  The  latter  change  is  indi- 
cated by  the  reduction  in  size  of  the 
cuneiform  and  lateral  displacement  of  the 
lunar  and  scaphoid,  which  increases  the 
relative  size  of  the  area  of  manus  under 
the  radius.  The  alternating  arrangement 
of  the  carpals  and  more  compact  carpus 
make  the  wrist  less  flexible  but  better  for 
resisting  stresses.  The  larger  posterior  tu- 
berosities on  several  of  the  carpals  indicate 
more   powerful    flexor    musculature.     The 


sharper  intercondyloid  ridge  on  the  hu- 
merus restricts  lateral  movement  at  the 
elbow  joint.  The  weaker  deltoid  crest, 
higher  deltoid  tubercle,  and  narrower  and 
less  asymmetrical  olecranon  are  features 
associated  with  increased  cursoriality. 
Thus,  in  a  complex  of  features,  the  fore- 
limb  of  Hyracotherium  is  more  specialized 
for  running  than  is  that  of  Tetraclaenodon 
or  Phenacodus. 

Hind  Limb 

In  Tetraclaenodon  the  greater  trochan- 
ter of  the  femur  is  only  slightly  higher 
than  the  head,  the  lesser  trochanter  is 
very  weak,  and  the  third  trochanter  is 
large  and  located  about  two-fifth's  of  the 
way  down  the  shaft.  The  cnemial  crest  of 
the  tibia  is  relatively  large  and  extends 
about  halfway  down  the  shaft,  the  grooves 
for  the  astragalus  are  broad  and  very 
shallow,  and  the  medial  malleolus  and 
distal  end  of  the  fibula  (lateral  malleolus) 
are  large  and  massive.  The  astragalus  has 
a  relatively  flat,  low,  and  wide  trochlea 
with  a  foramen,  a  relatively  long  neck, 
and  a  dorsoventrally  flattened,  convex 
head.  The  posterior  astragalocalcaneal  ar- 
ticulation is  only  slightly  rounded.  The 
calcaneum  has  a  large  peroneal  tubercle 
and  the  ectocuneiform  a  large  plantar 
process.  The  pes  is  pentadactyl,  with  the 
lateral  toes  slightly  reduced  (see  Fig.  4). 

The  hind  limb  of  Phenacodus  is  similar 
to  that  of  Tetraclaenodon,  differing  in  the 
following  features:  femur  with  larger 
lesser  trochanter;  tibia  with  weaker  cne- 
mial crest,  smaller  medial  malleolus,  and 
slightly  deeper  grooves  for  astragalus; 
fibula  relatively  slimmer,  with  smaller  dis- 
tal end;  astragalus  with  a  slightly  rela- 
tively higher,  narrower,  and  more  deeply 
grooved  trochlea,  a  slightly  more  curved 
posterior  astragalocalcaneal  facet,  no  as- 
tragalar  foramen,  and  a  deeper  (dorso- 
plantarly)  head;  first  and  fifth  metatar- 
sals slightly  more  reduced. 

The  enlarged  lesser  trochanter  of  the 
femur  suggests  a  stronger  iliopsoas,  an 
adductor  of  the  femur.  The  reduction  of 
the  cnemial  crest  suggests  reduced  power 


426 


414 


LEONARD  B.  RADINSKY 


Fig.  4.    Hind  feet  of  A.  Hyracotheriutn  (from  Kitts,  1956),  X  V2;  B.    Tetraclaenodon  (from  Mat- 
thew, 1897),  X  ¥2;  C.  Phenacodus  (AMNH  no.  293),  X  Vs. 


but  increased  speed  in  the  hind  limb.  The 
more  deeply  grooved  astragalar  trochlea 
helps  restrict  lateral  movement  at  the 
upper  ankle  joint  and  reduces  the  necessity 
for  large  lateral  and  medial  malleoli.  The 
loss  of  the  astragalar  foramen  allows  a 
slightly  greater  arc  of  rotation  of  the 
astragalus  on  the  tibia.  The  more  curved 
posterior  astragalocalcaneal  facet  and 
deeper  astragalar  head  may  be  related  to 
a  more  digitigrade  posture,  which  is  sug- 
gested by  the  reduction  of  the  lateral  toes. 
In  all  of  these  features  the  hind  limb  of 
Phenacodus  is  slightly  more  specialized 
for  running  than  is  that  of  Tetraclaenodon. 
The  hind  limb  of  Ectocion  is  known 
only  from  an  astragalus  and  part  of  a  cal- 
caneum  (AMNH  no.  16127).   The  astrag- 


alus (see  Fig.  5)  differs  from  that  of 
Tetraclaenodon  in  having  a  slightly  higher 
and  narrower  tibial  trochlea  with  a  slightly 
deeper  groove  and  no  astragalar  foramen, 
a  more  anteriorly  directed  posterior  cal- 
caneal facet,  a  wider  neck  with  a  high 
anteroposteriorly  oriented  ridge  at  the 
dorsolateral  corner,  and  a  slightly  flatter 
and  deeper  navicular  facet.  The  high 
dorsolateral  ridge  probably  marks  the  at- 
tachment of  a  strong  lateral  astragalocal- 
caneal ligament,  which  suggests  restriction 
of  rotation  between  astragalus  and  calca- 
neum.  This  interpretation  is  supported  by 
the  less  oblique  posterior  calcaneal  facet 
and  the  flatter  head  (the  latter  indicates 
less  movement  between  astragalus  and 
navicular).  These  features  suggest  a  slight 


427 


ORIGIN  OF  PERISSODACTYLS 


415 


Fig.  S.  Astragali  of  A.  Ectocion  (AMNH  no. 
16127),  B.  Hyracotherium,  C.  Phenacodus,  D. 
Tetraclaenodon.    Not  to  scale. 


loss  of  freedom  for  lateral  movement  in 
the  tarsus  of  Ectocion  compared  with  the 
condition  in  Tetraclaenodon.  The  anterior 
end  of  the  calcaneum  is  as  wide  in  Ecto- 
cion as  in  Tetraclaenodon,  suggesting  that 
the  pes  of  Ectocion  was  pentadactyl. 

The  hind  limb  of  Hyracotherium  differs 
from  that  of  Tetraclaenodon  in  the  same 
features  mentioned  for  Phenacodus,  but  to 
a  greater  degree  and  with  additional  mod- 
ifications. The  latter  include:  femur  with 
higher  greater  trochanter  and  more  proxi- 
mally  located  third  trochanter;  cnemial 
crest  of  tibia  does  not  extend  as  far  dis- 
tally;  first  and  fifth  digits  lost  and  re- 
maining metatarsals  relatively  longer 
(length  of  third  metatarsal/femur  =  0.50 
in  Hyracotherium  compared  to  0.35  in  the 
phenacodontids) ;  tarsus  relatively  nar- 
rower and  more  compact,  and  astragalus, 
calcaneum,  and  navicular  modified  to 
eliminate  the  possibility  of  lateral  move- 
ment of  the  foot. 

The  higher  greater  trochanter  (which 
provides  better  leverage  for  the  gluteal 
muscles,  important  abductors  of  the  fe- 
mur), more  proximally  located  third  tro- 
chanter, shorter  cnemial  crest,  and  longer 
metatarsals,  plus  the  modifications  noted 
in  Phenacodus,  are  cursorial  specializa- 
tions of  Hyracotherium  which  occur  also 
in  other  running  mammals.  The  loss  of 
the    first   and    fifth    toes    and    the    great 


elongation  of  the  remaining  metatarsals 
are  not  unusual  cursorial  adaptations  in 
later  forms  but  are  extremely  progressive 
features  for  an  early  Eocene  mammal. 
They  require  a  compact,  relatively  rigid 
tarsus  and  it  is  in  modifications  of  the 
tarsus  to  provide  a  stable  ankle  joint  that 
Hyracotherium  was  unique. 

The  interpretation  of  tarsal  mechanics 
in  extinct  animals  is  necessarily  limited  by 
lack  of  knowledge  of  the  tarsal  ligaments, 
for  the  ligaments  may  be  as  important  as 
the  bone  articulations  in  restricting  move- 
ment. Thus  the  degree  of  tarsal  movement 
inferred  from  the  bones  alone  represents 
the  maximum  amount  possible  and  in  life 
the  actual  amount  of  movement  may  have 
been  considerably  less. 

The  configurations  of  the  tarsal  articu- 
lations in  Tetraclaenodon  suggest  that 
lateral  movements  of  the  foot  (eversion 
and  inversion)  were  possible,  resulting 
from  a  combination  of  rotation  at  the 
lower  ankle  joint  (between  astragalus  and 
calcaneum)  and  transverse  tarsal  joint 
(between  astragalus  and  navicular).  The 
posterior  astragalocalcaneal  articulation 
is  only  gently  curved  and  the  astragalo- 
navicular  articulation  resembles  a  shallow 
ball-and-socket  joint.  In  Hyracotherium 
the  posterior  astragalocalcaneal  articula- 
tion is  bent  into  a  right  angle  and  is  more 
vertically  oriented,  restricting  rotation  at 
the  lower  ankle  joint,  and  the  astragalo- 
navicular  articulation  is  saddle-shaped 
(with  the  distal  end  of  the  astragalus 
concave  mediolaterally),  allowing  a  small 
amount  of  dorsoplantar  rotation  but  no 
lateral  movement.  The  saddle-shaped  as- 
tragalonavicular  articulation  is  unique  to 
the  Perissodactyla  and  a  diagnostic  fea- 
ture of  the  order. 

The  redistribution  of  weight  necessi- 
tated by  the  loss  of  the  lateral  toes  and 
relative  enlargement  of  the  middle  digit 
in  Hyracotherium  is  reflected  in  the  nar- 
rower, more  compact  tarsus,  in  which  the 
cuboid  and  calcaneum  are  narrower  (the 
peroneal  tubercle  of  the  calcaneum  is 
lost),  the  neck  of  the  astragalus  shorter, 
wider,   and    deeper,   and    the   head    more 


428 


416 


LEONARD  B.  RADINSKY 


closely  appressed  to  the  calcaneum,  and 
the  entocuneiform  reoriented  so  that  the 
vestigial  first  metatarsal  is  located  behind 
the  ectocuneiform  and  third  metatarsal 
where  it  serves  as  attachment  for  deep 
flexor  muscles  and  as  a  brace  for  the 
tarsus  (Radinsky,  1963).  The  plantar 
process  of  the  ectocuneiform  is  lost,  its 
function  apparently  having  been  usurped 
by  the  reoriented  vestige  of  the  first  meta- 
tarsal. Thus  virtually  the  whole  tarsus  of 
Hyracotherium  was  remodeled  to  provide 
the  stability  required  by  the  loss  of  lateral 
toes  and  great  elongation  of  the  metatar- 
sus. Versatility  was  sacrificed  for  in- 
creased efficiency  in  running. 

Discussion 

Absolute  dating  of  the  early  Tertiary 
(Evernden  et  al.,  1964)  indicates  that 
evolution  from  Tetraclaenodon  to  Hyraco- 
therium took  place  in  less  than  five  mil- 
lion years.  Considering  the  magnitude  of 
the  morphological  changes  involved,  the 
speed  of  that  transition  indicates  a  con- 
siderably higher  rate  of  evolution  in  late 
Paleocene  proto-perissodactyls  than  oc- 
curred during  most  of  the  subsequent  55 
million  years  of  perissodactyl  evolution. 
This  fact,  coupled  with  the  evidence  of  a 
major  adaptive  radiation  of  perissodactyls 
at  the  beginning  of  the  Eocene,  suggests 
that  the  origin  of  the  Perissodactyla  coin- 
cided with  a  shift  to  a  new  adaptive  level. 

The  two  major  areas  of  specialization 
of  the  earliest  perissodactyls,  as  far  as  the 
paleontological  evidence  indicates,  are  in 
mastication  and  locomotion,  and  there  is 
evidence  of  experimentation  among  the 
condylarths  in  both  of  these  fields.  The 
dentition  of  Phenacodus  is  essentially  a 
conservative  continuation  of  the  basic 
Tetraclaenodon  pattern,  while  that  of  Ec- 
tocion  is  specialized  for  vertical  shear. 
The  molars  of  Ectocion  are  more  special- 
ized for  vertical  shear  than  are  those  of 
Hyracotherium,  but  are  less  specialized 
for  transverse  shear.  In  the  closely  re- 
lated meniscotheriid  condylarths,  Menisco- 
therium  has  teeth  which  are  more  special- 
ized for  vertical  shear  than  those  of  Hy- 


racotherium and  at  least  as  specialized, 
although  in  a  somewhat  different  way,  for 
transverse  shear.  The  specialization  for 
transverse  shear  is  also  reflected  in  the 
mandible  of  Meniscotherium,  which  has  a 
relatively  large  angular  process  and  small 
coronoid  process.  This  experimentation  in 
dentition  among  condylarths  suggests  that 
a  variety  of  ecological  niches  for  medium- 
sized  browsers  was  open  at  the  beginning 
of  the  late  Paleocene. 

Phenacodus,  Ectocion,  and  Meniscothe- 
rium appear  to  have  been  only  slightly 
more  specialized  for  running  than  was 
Tetraclaenodon,  although  the  astragalus 
of  Ectocion  suggests  that  lateral  move- 
ment at  the  ankle  joint  may  have  been 
restricted  by  ligaments.  In  Hyracothe- 
rium, however,  a  radical  and  unique  re- 
modeling of  the  ankle  joint  prevented  lat- 
eral movement  and  made  possible  a  pre- 
cocious elongation  of  the  metatarsals  and 
reduction  of  the  lateral  digits.  Other  spe- 
cializations for  running  are  evident  in  the 
forelimb  of  Hyracotherium. 

During  the  early  Eocene  perissodactyls 
underwent  an  extensive  radiation  while 
phenacodontid  and  meniscotheriid  condyl- 
arths became  extinct.  Since  the  menisco- 
theriid dentition  was  at  least  as  specialized 
for  shear  as  was  that  of  Hyracotherium  it 
would  seem  that  the  masticatory  special- 
ization was  less  important  for  the  success 
of  the  Perissodactyla  than  the  adaptations 
for  running.  The  early  perissodactyls  were 
considerably  more  specialized  for  running 
than  were  the  contemporary  predators, 
while  the  condylarths  were  not.  It  is 
surely  no  coincidence  that  the  other  ma- 
jor order  of  medium-sized  to  large  herbi- 
vores, the  Artiodactyla,  appeared  at  the 
same  time  as  the  Perissodactyla,  with  their 
main  adaptive  feature  a  cursorial  modifi- 
cation of  the  ankle  joint  (see  Schaeffer, 
1947).  Thus  it  would  seem  that  predator 
pressure,  resulting  in  a  major  cursorial 
specialization,  was  the  critical  selective 
force  involved  in  the  origin  of  the  Perisso- 
dactyla. Unfortunately  there  is  no  direct 
evidence  of  the  ecological  factors  involved, 
for  the  faunas  in  which  the  condylarth- 


429 


ORIGIN  OF  PERISSODACTYLS 


417 


perissodactyl  transition  took  place  have 
not  yet  been  discovered.  The  absence  of 
perissodactyls  in  known  late  Paleocene 
faunas  and  their  sudden  appearance  in 
abundance  at  the  beginning  of  the  Eocene 
suggests  migration  from  an  unknown  area. 
Thus  early  perissodactyls  may  have  origi- 
nated isolated  from,  and  perhaps  under 
different  selective  pressures  than,  other 
descendant  lineages  of  the  middle  Paleo- 
cene Tetraclaenodon  stock. 

Summary 

The  middle  Paleocene  phenacodontid 
condylarth  genus  Tetraclaenodon  gave  rise 
to  three  late  Paleocene  groups,  represented 
by  Phenacodus,  Ectocion,  and  an  as  yet 
unknown  proto-perissodactyl.  The  main 
morphological  changes  indicated  by  the 
fossil  evidence  of  this  evolutionary  radia- 
tion are  specializations  for  mastication 
and  locomotion.  Molars  of  Phenacodus 
are  very  similar  to  those  of  Tetraclaeno- 
don, with  low  broad  cusps  apparently 
mainly  adapted  for  crushing.  Teeth  of 
Ectocion  have  prominent  W-shaped  ecto- 
lophs,  an  adaptation  for  vertical  shear, 
while  molars  of  Hyracotherium,  the  most 
primitive  known  perissodactyl,  are  spe- 
cialized for  both  vertical  and  transverse 
shear.  Phenacodus  and  Ectocion  show 
little  specialization  for  running  over  the 
primitive  ambulatory  condition  of  Tetra- 
claenodon, but  the  limbs  of  Hyracotherium 
display  major  cursorial  modifications,  in- 
cluding a  unique  remodeling  of  the  ankle 


which  prevented  lateral  movement  at  that 
joint  and  made  possible  a  precocious 
elongation  and  narrowing  of  the  meta- 
tarsus. 

Literature  Cited 

Becht,  G.  1953.  Comparative  biologic-ana- 
tomical researches  on  mastication  in  some 
mammals.  Proc.  Kon.  Nederl.  Akad.  We- 
tensch.,   (C)   56:   508-527. 

EvERNDEN,  J.  F.,  D.  E.  Savage,  G.  H.  Curtis, 
AND  G.  T.  James.  1964.  Potassium-argon 
dates  and  the  Cenozoic  mammalian  chronol- 
ogy of  North  America.  Amer.  Jour.  Sci., 
262:   145-198. 

KiTTS,  D.  1956.  American  Hyracotherium  (Pe- 
rissodactyla,  Equidae).  Bull.  Amer.  Mus. 
Nat.  Hist.,  110  (1):   5-60. 

Matthew,  VV.  D.  1897.  A  revision  of  the 
Puerco  fauna.  Amer.  Mus.  Nat.  Hist.  Bull., 
9  (22):   259-323. 

OsBORN,  H.  F.  1929.  Titanotheres  of  ancient 
Wyoming,  Dakota,  and  Nebraska.  U.S.  Geol. 
Surv.  Monograph  55   (2  vols.):   1-953. 

Radinsky,  L.  B.  1963.  The  perissodactyl  hal- 
lux.  Amer.  Mus.  Novit.,  2145:  1-8. 

ScHAEFFER,  B.  1947.  Notcs  On  the  origin  and 
function  of  the  artiodactyl  tarsus.  Amer. 
Mus.  Novit.,  1356:    1-24. 

Schumacher,  G.  H.  1961.  Funktionalle  Mor- 
phologic der  Kaumuskulatur.  G.  Fischer, 
Jena,  262  pp. 

Simpson,  G.  G.  1952.  Notes  on  British  hyra- 
cotheres.    J.  Linn.  Soc.  Zool.,  42:   195-206. 

Slijper,  E.  J.  1946.  Comparative  biologic-an- 
atomical investigations  on  the  vertebral  col- 
umn and  spinal  musculature  of  mammals. 
Verb.  Konink.  Nederl.  Akad.  Wetensch.  afd. 
Natuurk.,   (2)  42:   1-128. 

Smith,  J.  M.,  and  R.  J.  G.  Savage.  1959.  The 
mechanics  of  mammalian  jaws.  School  Sci. 
Rev.,  141:  289-301. 


430 


MILLER  AND  GIDLEY:  SUPERGENERIC  GROUPS  OF  RODENTS      431 


ZOOLOGY. — Synopsis  of  the  supergeneric  groups  of  Rodents.^ 
Gerrit  S.  Miller,  Jr.,  and  James  W.  Gidley,  U.  S. 
National  ]\Iuseum. 

Work  on  the  taxonomy  of  the  Rodents,  Uving  and  extinct,  has 
occupied  much  of  our  time  during  the  past  four  years.  This 
paper  contains  a  brief  synopsis  of  the  results. 

The  classification  which  we  have  adopted  is  based  on  the  fol- 
lowing conception  of  the  evolutionary  course  followed  by  the 
order  during  its  development.  This  course  has  been  mainly 
conditioned  by  the  mechanical  problem  of  strengthening  a  chew- 
ing apparatus  in  which  the  unusually  important  cutting  func- 
tion of  the  incisors  is  strongly  contrasted  with  the  grinding  func- 
tion of  the  cheekteeth;  the  highest  degree  of  efficiency  to  be 
given  always  to  the  incisors  and  in  most  instances  to  the  cheek- 
teeth as  well.  The  problem  has  been  solved  by  five  sequences  of 
correlated  changes  in  the  masseter  muscle  and  the  bones  to 
which  this  muscle  is  attached.  All  of  these  sequences  could 
originate  from  the  structures  present  in  a  generalized  mammal, 
but  there  is  no  evidence  that  any  rodent  during  its  development 
has  passed  from  one  to  another.  The  groups  characterized  by 
the  various  sequences  are  therefore  natural.  We  have  treated 
them  as  superfamilies :  the  Sciuroidae,  Myoidae,  Dipodoidae, 
Bathyergoidae,  and  Hystricoidae.  Of  the  secondary  problems  the 
most  conspicuous  has  been  the  strengthening  of  the  cheekteeth. 
These  teeth,  however  unUke  their  structure  in  extreme  in- 
stances may  appear,  have  all  been  developed  from  some  primi- 
tive, low-cro\sTied,  tritubercular  type  not  essentially  different 

^  Published  by  permission  of  the  Secretary  of  the  Smithsonian  Institution. 


431 


432     MILLER  AND  gidley:  supergeneric  groups  of  rodents 

from  that  present  in  the  Eocene  Paramyidae  and  in  living  species 
of  Sciurus.  During  the  adjustment  of  the  cheekteeth  to  increas- 
ingly heavy  fore-and-aft  grinding  motion,  a  process  which  has 
taken  place  in  most  members  of  the  order,  the  crown  height  has 
been  augmented,  while  the  original  tubercles  and  lophs  have  been 
made  more  efficient  by  (a)  increase  in  complexity,  and  (b)  con- 
version into  transverse  ridges  and  specialized  enamel  plates,  usu- 
ally with  redaction  in  the  number  of  elements  present.  In  each 
superfamily  the  characteristic  modifications  in  the  muscles  and 
skull  were  begun  in  connection  with  the  development  of  the  in- 
cisors. Mechanical  improvement  of  the  cheekteeth  came  later. 
All  rodent  teeth  have  been  developed  from  an  essentially  uniform 
original  type  under  the  influence  of  practically  identical  mechani- 
cal forces.  Parallelism  in  highly  specialized  dental  structures 
between  genera  and  species  which  are  not  closely  related  is 
therefore  frequent  enough  to  be  one  of  the  noticeable  peculiari- 
ties of  the  order.  The  history  of  development  extends  so  far  into 
the  past  that  the  essential  features  of  structure  are  modernized 
in  the  oldest  known  Eocene  rodents.  No  extinct  member  of 
the  order  has  yet  been  found  which  can  be  regarded  as  ancestral 
to  any  considerable  number  of  subsequent  forms. 

The  order  Rodentia  may  be  defined  as  follows:  Terrestrial  and 
fossorial  (occasionally  arboreal  or  semiaquatic)  placental  mammals 
with  both  brain  and  placentation  generalized  in  type;  feet  unguiculate; 
elbow  joint  always  permitting  free  rotary  motion  of  forearm;  fibula 
never  articulating  with  calcaneum;  masseter  muscle  highly  specialized, 
divided  into  three  or  more  distinct  portions  having  slightly  different 
functions;  cecum  without  spiral  fold;  dental  formula  not  known  to 
exceed  i  |,  c  ^  pm  f ,  m  f  =  22  permanent  teeth;  incisors  scalpriform, 
growing  from  persistent  pulp,  the  enamel  of  the  upper  tooth  not  ex- 
tending to  posterior  surface;  distance  between  mandibular  and  maxil- 
lary toothrows  approximately  equal,  both  pairs  of  rows  capable  of  par- 
tial or  complete  opposition  at  the  same  time,  the  primary  motion  of  the 
lower  jaw  in  mastication  longitudinal  or  oblique. 

Superfamily  SCIUROIDAE 

Masseter  lateralis  superficialis  with  anterior  head  distinct,  this  por- 
tion of  the  muscle  not  attached  to  any  part  of  the  zygoma  except  occa- 
sionally to  a  point  at  extreme  base  of  zygomatic  plate;  zygomatic  plate 


432 


MILLER  AND  GIDLEY:  SUPERGENERIC  GROUPS  OF  RODENTS      433 

tilted  upward,  usually  broad,  with  its  superior  border  always  above 
lower  margin  of  infraorbital  foramen.  Infraorbital  foramen  inferior, 
transmittng  nerve  only;  masseter  lateralis  passing  obliquely  upward  to 
superior  border  of  rostrum,  always  to  exclusion  of  masseter  medialis. 

THBEE-CUSPED   SERIES 

Teeth  becoming  hypsodont  on  the  basis  of  a  tritubercular  structure. 

Family  Sciuridae 

Skull  never  truly  fossorial;  infraorbital  foramen  with  outer  wall 
usuall}'  though  not  always  forming  a  distinct  canal,  its  orifice  protected 
from  muscular  action  by  the  presence,  at  or  near  its  lower  border,  of  an 
outgrowth  for  attachment  of  masseter  lateralis  superficialis;  frontal 
with  decurved  postorbital  process;  cheekteeth  brachydont  or  uni- 
laterally hypsodont,  the  fundamental  tritubercular  plan  usually  (prob- 
ably alwaj's)  evident  in  functional  adult  teeth  that  have  not  under- 
gone considerable  wear;  external  form  suited  to  arboreal  or  terrestrial 
life. 

The  Sciuridae  of  authors. 

Subfamily  Sciurinae. — Orbital  region  normal,  the  middle  of  orbit  in 
front  of  middle  of  skull  (except  in  genera  with  greatly  elongated 
rostrum),  the  lachrymal  bone  above  or  in  front  of  anterior  extremity  of 
toothrow,  the  zygomatic  plate  not  especially  emarginate  below,  the 
postorbital  process  indicating  an  evident  boundary  between  orbit  and 
temporal  fossa;  no  parachute  membrane. 

The  entire  family  except  the  members  of  the  two  following  groups; 
Oligocene  to  Recent;  Northern  Hemisphere,  South  America,  conti- 
nental Africa. 

Subfamily  N  anno  sciurinae. — -Like  the  Sciurinae  but  orbital  region 
abnormal,  the  middle  of  orbit  behind  middle  of  skull  (rostrum  short) , 
the  lachrymal  bone  above  middle  of  toothrow,  the  zygomatic  plate 
conspicuously  emarginate  below,  the  postorbital  process  not  indicating 
an  evident  boundary  between  large  orbit  and  much  reduced  temporal 
fossa. 

Nannosciurus  of  the  Malay  region,  Myosciurus  of  West  Africa,  and 
Sciurillus  of  South  America  (the  last  not  seen);  Recent. 

Subfamily  Pteromyinae. — Like  the  Sciurinae  but  with  a  well  de- 
veloped parachute  membrane  present. 

The  Flying-squirrels;  Middle  Miocene  to  Recent;  Northern  Hemis- 
phere. 

Family  Geomyidae 

Skull  fossorial;  zygoma  robust;  infraorbital  foramen  always  at  end  of 
a  long  canal,  its  orifice  protected  from  muscle  pressure  by  counter- 


433 


434      MILLER  AND  GIDLEYI  SUPERGENERIC  GROUPS  OF  RODENTS 

sinking  in  an  oblique  sulcus;  frontal  without  postorbital  process;  cheek- 
teeth evenly  hypsodont  or  in  their  extreme  development  ever-growing, 
the  fundamental  tritubercular  plan  lost  in  functional  adult  teeth,  the 
first  and  second  molars  of  adult  consisting  of  either  one  or  two  simple 
loops.  External  form  in  living  members  of  the  group  highly  modified 
for  underground  life. 

Subfamily  Entopty chinas. — Angular  portion  of  mandible  mostly 
below  alveolar  level;  cheekteeth  rooted,  the  enamel  pattern  of  first  and 
second  molars  consisting  of  two  simple  loops  joined  at  protomere.^ 

Entoptychus;  North  American  Ohgocene. 

Subfamily  Geomyinae. — ^Angular  portion  of  mandible  mostly  above 
alveolar  level;  cheekteeth  ever-growing,  the  first  and  second  adult 
molar  consisting  each  of  a  simple  prism,  with  an  enamel  plate  always 
present  on  anterior  surface  in  upper  teeth  and  on  posterior  surface  of 
lower  teeth. 

North  American  pocket  gophers;  Miocene  to  Recent. 

Family  Heteromyidae 

Essential  characters  as  in  the  Geomyidae  but  skull  not  fossorial; 
zygoma  slender;  orifice  of  infraorbital  canal  protected  from  muscle 
pressure  by  countersinking  in  a  vacuity  which  extends  transversely 
through  rostrum;  external  form  murine  or  saltatorial. 

North  American  pocket-mice  and  kangaroo-rats;  Middle  Oligocene 
{Heliscomys)  to  Recent. 

FOUR-CUSPED   SERIES 

Teeth  becoming  hypsodont  on  the  basis  of  a  quadritubercular 
structure. 

Family  Adjidaumidae 

Zygomasseteric  structure^  and  infraorbital  canal  as  in  the  Sciur- 
idae;  cheekteeth  |,  slightly  hypsodont,  the  enamel  pattern  unmodified 
heptamerous." 

Adjidaumo;  North  American  Middle  Oligocene. 

^  Protomere  =  inner  side  of  maxillary  cheekteeth  and  outer  side  of  mandibular 
cheekteeth. 

Paramere  =  outer  side  of  maxillary  cheekteeth  and  inner  side  of  mandibular 
cheekteeth. 

'  Zygomasseteric  structure  =  the  combined  and  correlated  structures  of  the 
masseter  muscle  and  of  the  skull  in  the  region  at  which  the  muscle  takes  its  origin. 

*  Heptamerous  pattern  =  the  enamel  pattern  of  a  flat-crowned  cheektooth  in 
which  each  of  seven  original  tubercles  is  represented  by  a  loop  (two  on  the  proto- 
mere, five  on  the  paramere). 


434 


MILLER  AND  GIDLEY :  SUPERGENERIC  GROUPS  OF  RODENTS      435 

Family  Eutypomyidae 

Like  the  Adjidaumidae  but  with  cheekteeth  somewhat  more  hypso- 
dont  and  the  heptamerous  enamel  pattern  complicated  by  the  devel- 
opment of  a  considerable  number  of  secondary  closed  loops  which  ap- 
pear in  partially  worn  teeth  as  an  aggregation  of  minute  enamel  lakes 
covering  nearly  entire  surface  of  crown. 

Eutypomys;  North  American  Middle  Oligocene. 

Family  Chalicomyidae 

Like  the  Adjidaumidae  but  cheekteeth  strongly  hypsodont  and 
enamel  pattern  reduced-heptamerous  (sometimes  paralleling  that  of 
the  Hystricidae)  becoming  rapidly  simplified  as  the  crowns  wear  away; 
skull  occasionally  fossorial;  no  postorbital  process  on  frontal;  no  pit- 
like depression  in  basioccipital  region. 

Chalicomys  (=  Steneofiber)  and  related  genera,  European  Miocene 
and  Pliocene;  Trogontherium,  European  Pliocene  and  Pleistocene; 
Palaeocastor,  Eucastor  and  related  genera,  North  American  Upper 
Oligocene  and  Lower  Pliocene. 

Family  Castoridae 

Skull  with  rostrum  broadened  and  deepened  and  braincase  narrowed ; 
basioccipital  region  with  conspicuous  pit-like  depression ;  cheekteeth  not 
ever-growing  but  so  excessively  hypsodont  that  the  slightly  reduced- 
heptamerous  pattern  (parallel:  Myocastor)  changes  little  with  age  and 
rarely  if  ever  wears  out;  external  form  highy  modified  for  aquatic  hfe; 
caudal  vertebrae  flattened. 

Castor;  Lower  Pliocene  to  Recent;  Northern  Hemisphere. 

Family  Castoroididae 

Zygomasseteric  structure  modified  by  the  passage  of  the  shaft  of 
the  incisor  below  the  infraorbital  foramen  instead  of  above  it,  the  ridge 
formed  by  the  tooth  dividing  the  area  of  masseteric  origin  on  side  of 
rostrum  into  two  planes;  posterior  nares  divided  horizontally  by  the 
median  fusing  of  palatine  bones  over  roots  of  cheekteeth;  teeth  ever- 
growing, the  enamel  pattern  a  series  of  5-7  parallel  transversa  ridges 
(parallel:  Dinomyidae) . 

Castor  aides;  North  American  Pleistocene. 

Superfamily  MUROIDAE 

Zygomasseteric  structure  as  in  the  Sciuroidae  except:  Infraorbital 
foramen  superior  in  whole  or  in  part,  entered  or  traversed  by  muscle 
as  well  as  nerve;  masseter  lateralis  seldom  reaching  superior  border  of 
rostrum,  and  never  doing  this  to  exclusion  of  masseter  medialis. 

THREE-CUSPED   SERIES 

Modifications  of  teeth  based  on  an  underlying  tritubercular  structure. 


435 


436     MILLER  AND  gidley:  supergeneric  groups  of  rodents 

Family  Muscardinidae 

Skull  with  no  striking  modifications  of  general  form;  zygomatic  root, 
much  as  in  the  Sciuridae  except  that  its  anterior  face  is  nearly  vertical 
instead  of  strongly  oblique,  and  the  infraorbital  foramen  extends  above 
median  level  of  orbit,  receiving  or  transmitting  a  strand  of  muscle  as 
well  as  the  nerve;  no  postorbital  processes;  auditory  bullae  large,  globu- 
lar, rounded  in  front;  cheekteeth  |,  brachydont  (in  Leithia  subhypso- 
dont),  the  enamel  pattern  reduced-hexamerous  in  forms  with  basin- 
shaped  crowns,  passing  to  a  system  of  parellel  transverse  ridges  in 
those  with  flat  crowns  (parallel :  Graphiuridae) ;  external  form  showing 
a  combination  of  murine  and  sciurine  features. 

Eliomys,  Dyromys,  Glis,  Muscardinus,  Leithia:  Old  World  Middle 
Miocene  to  Recent. 

FOUR-CUSPED    SERIES 

Modifications  of  teeth  based  on  an  underlying  quadritubercular 
structure. 

Family  Ischyromyidae 

General  characters  of  the  skull  as  in  the  Muscardinidae;  teeth  |, 
moderately  hypsodont,  rooted,  the  fundamental  structure  quadri- 
tubercular, the  enamel  pattern  in  worn  teeth  reduced-heptamerous. 

Ischyromys;  North  American  Middle  Oligocene. 

Family  Cricetidae 

Fundamental  zygomasseteric  structure  as  in  the  Muscardinidae  and 
Ischyromyidae,  but  infraorbital  foramen  usually  enlarged  and  special- 
ized, consistioig  of  a  rounded  upper  portion  for  transmission  of  muscle 
and  a  narrow  lower  portion  for  transmission  of  nerve,  the  zygomatic 
root  developed  into  a  broad,  obhque  plate;  skull  varying  excessively  in 
form,  but  always  without  postorbital  process  on  the  frontal;  check- 
teeth  f ,  the  crown  structure  showing  all  stages  from  brachydont  to 
ever-growing,  the  fundamental  structure  quadritubercular,  the  enamel 
pattern  varying  from  simple  heptamerismto  excessive  speciahzation,  the 
tubercles  in  the  maxillary  teeth  always  presenting  a  longitudinally  bi- 
serial  arrangement  and  never  developing  a  functional  third  series  on 
lingual  side  of  crown;  external  form  murine  or  fossorial. 

Subfamily  Cricetinae. — Skull  without  special  modification,  the  zygo- 
masseteric structure  as  usual  in  the  family,  the  squamosal  not  devel- 
oping a  postorbital  ridge  or  process;  molars  rooted,  their  crowns  vary- 
ing gradually  from  tubercular  and  brachydont  to  flat-crowned  and 
strongly  hypsodont,  when  in  the  latter  condition  the  prisms  not  oppo- 
site (compare  Gerbillinae)  and  the  posterior  termination  of  m^  and  m^ 
not  angular  (compare  Microtinae). 

The  Cricetinae,  Sigmodontinae,  Neotominae,  and  Nesomyinae  of  authors; 
Oligocene  to  Recent;  continental  region  of  the  world;  Madagascar. 


436 


MILLER  AND  GIDLEY:  SUPERGENERIC  GROUPS  OF  RODENTS      437 

Subfamily  Gerbillinae. — Auditory  bullae  and  entire  posterior  portion 
of  skull  enlarged;  teeth  subhypsodont  or  hypsodont,  fiat-crowned  in 
adults,  with  opposite  prisms,  these  tending  to  form  transverse  ridges 
joined  at  median  Une,  or,  in  their  extreme  development,  to  separate 
into  plates;  external  form  saltatorial. 

The  Gerbillinae  of  authors;  Recent  only,  unless  Trilophomy shorn  the 
Pliocene  of  France  is  a  member  of  the  group;  Asia  and  Africa. 

Subfamily  Microtinae. — Like  the  more  hypsodont  members  of  the 
subfamily  Cricetinae  but  cheekteeth  often  growing  from  a  persistent 
pulp,  the  enamel  pattern  always  consisting  of  (at  least  partially)  alter- 
nating triangles,  the  posterior  termination  of  m^  and  m^  never  rounded; 
squamosal  with  distinct  postorbital  ridge  or  process. 

The  Microtinae  of  authors;  Miocene  to  Recent;  Northern  Hemisphere. 

Subfamily  Lophiomyinae. — Like  the  Cricetinae  with  tubercular, 
slightly  hypsodont  teeth,  but  skull  with  temporal  fossa  bridged  by  a 
plate  formed  of  laminae  arising  from  the  jugal,  frontal,  and  parietal, 
a  structure  not  known  to  occur  elsewhere  among  rodents. 

Lophiomys;  Recent;  Africa. 

Family  Platacanthomyidae 

Like  the  Cricetidae  but  zygomasseteric  structure  unusual,  the  infra- 
orbital foramen  of  normal  cricetine  form,  but  zygomatic  plate  much 
narrowed,  and  masseter  laterahs  profundus  extending  its  hne  of  at- 
tachment along  upper  zygomatic  border  to  side  of  rostrum  above  fora- 
men; cheekteeth  subhypsodont,  the  enamel  pattern  a  modified  hep- 
tamerous  with  tendency  to  form  parallel  obhque  cross-ridges  (parallel: 
Muscat  dinidae) . 

Platacanthomys  and  Typhlomys;  Recent;  Southern  Asia. 

Family  Rhizomyidae 

Like  the  Cricetidae  but  zygomasseteric  structure  imusual,  the  infra- 
orbital foramen  with  neural  portion  reduced  or  obhterated  by  partial 
or  entire  fusion  of  zygomatic  plate  with  side  of  rostrum;  skull  and 
external  form  fossorial. 

Subfamily  Tachyoryctinae. — Infraorbital  foramen  with  neural  por- 
tion reduced  to  an  inconspicuous  notch  by  fusion  of  the  broad  zygomatic 
plate  with  side  of  rostrum  (outline  of  plate  below  foramen  usually  vis- 
ible) ;  skull  strongly  fossorial ;  cheekteeth  closed  at  base  but  extremely 
hypsodont,  the  enamel  pattern  not  changing  in  character  during  adult 
life;  enamel  pattern  in  adult  consisting  of  2-3  parallel  curved  cross- 
ridges  (the  conqave  surface  directed  backward  and  outward  in  upper 
teeth,  forward  and  inward  in  lower  teeth;  parallel:  Protechimys); 
reduced-heptamerism  evident  in  unworn  enamel  cap;  external  form 
modified,  though  not  excessively,  for  underground  life. 

Tachyorydes;  Recent;  Africa. 


437 


438      MILLER  AND  GIDLEYI  SUPERGENERIC  GROUPS  OF  RODENTS 

Subfamily  Rhizomyinae. — -Like  the  Tachyorydinae  but  peculiarities  of 
infraorbital  region  carried  farther,  the  neural  notch  being  obliterated 
and  the  foramen  appearing  as  a  small  orifice  confined  to  upper  surface 
of  zygomatic  root;  teeth  moderately  hypsodont,  the  enamel  pattern 
obviously  heptamerous  or  reduced-heptamerous  and  changing  rapidly 
during  adult  life. 

Rhizomys  and  related  genera;  Pliocene  to  Recent;  southern  Asia. 

Subfamily  Braminae. — Like  the  Rhizomyinae  but  cheekteeth  with 
definitely  prismatic  structure. 

Bramus;  Pleistocene;  northern  Africa  (not  seen). 

Family  Spalacidae 

Like  the  Cricetidae  but  zygomasseteric  structure  unusual,  the  zygo- 
matic plate  narrowed  and  turned  downward  to  a  nearly  horizontal  posi- 
tion, thus  doing  away  with  the  separate  neural  portion  of  the  opening 
by  a  process  the  exact  opposite  to  that  bringing  about  a  similar  result 
in  some  of  the  Rhizormjidae;  skull  excessively  fossorial,  the  lambdoid 
crest  carried  forward  to  level  of  zygomatic  root. 

Subfamiy  Myospalacinae. — Mandible  scarcely  movable  at  symphysis, 
a  large  post-symphyseal  buttress  early  developed;  cheekteeth  growing 
from  persistent  pulps,  the  crowns  elongated,  the  enamel  pattern  con- 
sisting of  alternating  triangles,  the  posterior  termination  of  m^  and 
m'-  rounded. 

Myosp.alax;  Recent;  Asia. 

Subfamily  Spalacinae. — Mandible  movable  at  symphysis  through- 
out life;  cheekteeth  moderately  hypsodont,  rooted,  subterete,  the  pat- 
tern reduced-heptamerous,  changing  rapidly  with  wear;  skull  with  the 
characters  of  the  family  carried  to  such  an  extreme  as  to  make  it  the 
most  fossorial  type  known  among  rodents. 

Spalax,  Recent,  Prospalax,  Upper  Pliocene,  and  an  undescribed  genus 
from  the  upper  Oligocene;  eastern  Mediterranean  Region,  and  southern 
Europe. 

Family  Muridae 

Skull  as  in  the  typical  Cricetidae;  cheekteeth  |,  the  upper  teeth  with 
a  functional  row  of  tubercles  on  lingual  side  of  crown  internal  to  the 
protocone  and  hypocone,  these  tubercles  entering  conspicuously  into  the 
plan  of  modification  of  the  crowns. 

Subfamily  Dendromyinae. — Upper  cheekteeth  with  triserial  arrange- 
ment not  fully  developed;  manus  with  only  3  functional  digits. 
The  Dewdromymae  of  authors;  Recent;  Africa. 

Subfamily  Murinae. — Upper  cheekteeth  with  fully  developed  tri- 
serial arrangement  of  tubercles  always  evident,  though  frequently  vary- 


438 


MILLER  AND  GIDLEY:  SUPERGENERIC  GROUPS  OF  RODENTS      439 

ing  from  the  symmetrical  plan;  crowns  brachydont  or  slightly  hyp- 
sodont;  manus  normal. 

Tlie  Murinae  of  authors;  Upper  Miocene  to  Recent;  Old  World, 
except  Madagascar. 

Subfamily  Phloeomyinae. — Upper  cheekteeth  with  triserial  arrange- 
ment of  elements  obscured  by  flattening  out  of  each  trio  of  tubercles  to 
form  a  simple,  detached,  transverse  lamina  (parallel:  Diplomys); 
crowns  moderately  hypsodont ;  braincase  relatively  small  and  auditory 
bullae  reduced;  external  form  heavy,  arboreal. 

Phloeomys;  Recent;  Philippine  Islands. 

Subfamily  Otomyinae. — Upper  cheekteeth  with  same  modification  as 
in  the  Phloeomyinae,  but  m'  tending  to  become  the  dominant  tooth  in  the 
series,  its  size  always  greater  than  that  of  m^,  and  its  elements  usually 
reduplicated;  external  form  heavy,  terrestrial. 

Otomys;  Recent;  Africa. 

Subfamily  Hydromyinae. — Upper  cheekteeth  with  triserial  arrange- 
ment obscured  by  suppression  of  tubercles  of  outer  series;  m'  vestigial. 
The //ydromi/mae  of  authors;  Recent;  Australian  Region. 

Superfamily  DIPODOIDAE 

Masseter  lateralis  superficialis  with  anterior  head  not  distinct,  this 
portion  of  the  muscle  attaching  along  a  considerable  area  on  anterior 
border  of  zygoma;  zygomatic  plate  nearly  horizontal,  always  narrow 
and  completely  beneath  infraorbital  foramen.  Angular  portion  of 
mandible  not  distorted  outward  at  base  to  permit  free  passage  of  a 
branch  of  the  masseter  lateralis,  its  general  direction  not  parallel  with 
zygoma. 

THREE-CUSPED    SERIES 

Modifications  of  teeth  based  on  an  underlying  tritubercular  structure, 
the  hypocone  when  present  not  entering  into  the  essential  mechanical 
scheme  of  the  crown. 

A. — Skull  with  no  special  pecularities  except  that  the  auditory  bullae 
appear  to  be  imperfect  or  absent  (perhaps  merely  reduced  as  in  Phloeomys) ; 
infraorbital  foramen  not  transmitting  muscle;  cheekteeth  brachydont  or 
subhyposodont,  their  structure  essentially  as  in  the  less  modified  Sciuridae. 

Family  Paramyidae 

Rostrum  and  braincase  approximately  equal  in  width,  infraorbital 
foramen  very  small,  not  visible  in  lateral  view  of  the  skull;  cheekteeth 
I,  the  upper  molars  obviously  and  simply  tritubercular  in  general  plan, 
the  hypocone,  when  present,  appearing  as  a  supplement  to  the  original 
structure  of  the  tooth. 


439 


440      MILLER  AND  GIDLEYI  SUPERGENERIC  GROUPS  OF  RODENTS 

Paramys,  My  sops,  Prosciurus,  and  related  genera;  North  American 
Lower  Eocene  to  Middle  Oligocene. 

B. — Skull  and  teeth  as  in  the  Paramyids  except  that  the  auditory  bullae 
are  well  developed,  the  infraorbital  foramen  is  enlarged  to  transmit  a  small 
strand  of  muscle,  and  the  cheekteeth  are  flattened. 

Family  Graphiuridae 

Cheekteeth  |,  brachydont,  crowns  wider  than  long,  basin-shaped 
with  small  tubercles  and  low  ridges  (parallel:  Muscardinidae);  skull 
with  no  special  peculiarities,  the  braincase  much  wider  than  rostrum; 
auditory  bullae  globular;  external  form  muscardinine. 

Graphiurus;  Recent;   Africa. 

C. — Skull  fossorial  (except  perhaps  in  the  Allomyidae);  infraorbital 
foramen  not  transmitting  muscle;  auditory  bullae  well-developed;  cheek- 
teeth brachydont,  hypsodont,  or  ever-growing;  modification  of  crownsbased  on 
a  structure  including  well  developed  protoconule  and  metaconule,  and  con- 
spicuously trenchant  outer  commissures. 

Family  Allomyidae 

Cheekteeth  |,  brachydont  or  moderately  hypsodont,  the  trituber- 
cular  structure  of  upper  teeth  evident  in  unworn  crowns;  protoconule 
and  metaconule  large;  functional  cusps  in  m^  and  m^;  mesostyle  appear- 
ing in  hypsodont  forms  as  a  conspicuous  median  rib  on  outer  surface  of 
crown  (parallel:  Pseudosciuridae). 

Allomys,  Haplomys,^  Meniscomys,  Mylagaulodon;  North  American 
Upper  Oligocene  and  Miocene. 

Family  Aplodontiidae 

Like  the  Allomyidae  but  the  skull  greatly  widened  posteriorly,  the 
auditory  bullae  flask-shaped  with  neck  directed  horizontally  outward ; 
cheekteeth  growing  from  persistent  pulp,  the  unworn  caps  showing 
evident  pattern  of  the  Allomys-type,  this  soon  wearing  away  and  leaving 
a  simple  enamel  ring;  paramere  with  conspicuous  vertical  ridge. 

Aplodontia;  Pleistocene  and  Recent;  Liodontia,^  Miocene;  western 
North  America. 

Family  Cylindrodontidae 

Skull  fossorial  with  braincase  slightly  wider  than  rostrum;  cheek- 
teeth I,  subterete,  excessively  hypsodont  but  not  growing  from  persist- 
ent pulp,  the  enamel  pattern  in  considerably  worn  upper  teeth  consist- 
ing of  an  outer  ring  and  a  central  lake. 

Cylindrodon;  North  American  Lower  Ohgocene.  Position  of  group 
doubtful. 

*  New  genus,  type  Meniscomys  liolophus  Cope. 

*  New  genus,  type  Aplodontia  alexandrae  Furlong. 


440 


MILLER  AND  GIDLEY:  SUPERGENERIC  GROUPS  OF  RODENTS      441 


FOUR-CUSPED    SERIES 


Modifications  of  teeth  based  on  an  underlying  quadritubercular 
structure,  the  hypocone  always  entering  into  the  essential  mechanical 
scheme  of  the  crown. 

A. — Skull  not  specially  modified;  upper  molars  with  large  proioconule 
and  metaconulc,  and  conspicuously  trenchant  outer  commissures,  their 
structure  paralleling  that  of  the  Allomyidae  in  the  three-cusped  series. 

Family  Pseudosciuridae 

Skull  essentially  as  in  the  Sciuravidae  but  with  larger  infraorbital 
foramen  which  may  have  transmitted  a  strand  of  muscle. 
Pseudosciurus;  European  Oligocene. 

B. — Skull  excessively  fossorial;  occipital  region  obliquely  truncate,  with 
lambdoid  crest  moved  forward  nearly  to  level  of  zygomatic  root;  frontal  with 
short  postorbital  process;  bony  horn-cores  present  on  rostrum  in  two  genera, 
absent  in  a  third;  cheekteeth  highly  modified  from  a  normal  heptamerous 
structure,  the  grinding  function  of  toothrow  in  adult  almost  completely 
taken  over  by  the  greatly  enlarged  fourth  premolar. 

Family  Mylagaulidae 

General  structure  of  skull  much  as  in  the  Aplodontiidae;  cheekteeth 
f  or  I;  a  reduced-heptamerous  pattern  evident  in  slightly  worn  crowns, 
but  this  giving  place  with  wear  to  a  system  of  narrow  longitudinal  and 
oblique  lakes;  molars  relatively  small,  soon  crowded  out  by  the  pre- 
molar, an  excessively  hypsodont,  laterally  compressed  tooth,  closed  at 
the  base,  and  rapidly  increasing  in  crown  length  from  the  unworn  surface 
downward.     Skeleton  highly  modified  for  underground  life. 

Mylagaulus,  Ceratogaulus,  and  Epigaulus;  North  American  Miocene 
and  Pliocene. 

C. — Skull  without  special  peculiarities;  infraorbital  foramen  moderate 
or  very  large,  transmitting  both  muscle  and  Jierve;  cheekteeth  subhypsodont  or 
brachydont,  their  modifications  based  on  a  heptamerous  structure  in  which 
the  ridges  are  narrow  and  the  reentrant  spaces  wide  {parallels:  Funisciu- 
rus,  Erethizontidae) ;  external  form  glirine  or  pteromyine;  under  side  of 
tail  with  scaly  outgrowths  near  base. 

Family  Anomaluridae 

Skull  with  moderate  infraorbital  foramen;  lower  zygomatic  root  at 
level  immediately  in  front  of  anterior  cheektooth;  anterior  point  of 
masseteric  insertion  on  mandible  beneath  hinder  part  of  mi;  no  dis- 
crepancy between  size  of  incisors  and  molars;  cheekteeth  subhypso- 
dont, their  crowns  flat,  longer  than  wide;  external  form  pteromyine. 

Anomalurus;  Recent;  Africa. 


441 


442      MILLER  AND  GIDLEY:  SUPERGENEEIC  GROUPS  OF  RODENTS 

Family  Idiuridae 

Like  the  Anomaluridae  but  skull  with  infraorbital  foramen  greatly 
enlarged,  the  lower  zygomatic  root  nearer  to  incisor  than  to  anterior 
cheektooth ;  anterior  point  of  masseteric  insertion  on  mandible  in  front  of 
pm^;  incisors  excessively  heavy;  cheekteeth  weak,  extremely  brachydont, 
their  crowns  flat,  wider  than  long. 

Subfamily  Idiurinae. — Flying  membrane  present;  cheekteeth  with 
two  complete  median  transverse  ridges. 
Idiurus;  Recent;  Africa. 

Subfamily  Zcnkerellinae — Flying-membrane  absent;  cheekteeth  with 
one  complete  median  transverse  ridge. 
Zenkerella;  Recent;  Africa. 

D. — Skull  without  striking  peculiarities  other  than  a  tendency  to  assume 
a  form  characterized  by  broad  braincase,  large  auditory  parts,  and  weak 
rostruin  {parallels;  GerbilUnae,  Octodontinae) ;  infraorbital  foramen  trans- 
mitting muscle  in  all  members  of  the  group  in  which  the  skull  is  known 
except  probably  Sciuravus;  cheekteeth  varying  from  brachydont  to  ever- 
growing, their  modifications  based  on  a  heptamerous  structure  in  which  the 
ridges  are  wide  and  the  reentrant  spaces  narrow. 

Family  Sciuravidae 

Infraorbital  foramen  small,  but  visible  in  lateral  view  of  skull,  prob- 
ably transmitting  nerve  only;  cheekteeth  f ,  brachydont;  the  structure 
of  the  upper  molars  obviously  and  simply  quadritubercular. 

Sciuravus;  North  American  Middle  Eocene. 

Family  Zapodidae 

Infraorbital  foramen  large,  transmitting  muscle  as  well  as  nerve; 
cheekteeth  varying  in  number  from  f  in  the  earlier  members  of  the  group 
to  I  in  the  most  advanced ;  the  quadritubercular  crown  structure  usually 
though  not  always  much  modified;  metatarsals  not  reduced  or  fused. 

Subfamily  Theridomyinae. — The  earlier,  less  modified  members  of  the 
family:  pm*  a  large,  functional  tooth;  crowns  of  cheekteeth  varying 
from  brachydont  and  simply  quadritubercular  (Sciuroides)  to  hypsodont 
and  much  reduced  heptamerous  (Issiodoromys;  parallel:  Eocardia). 

The  Theridomyidae  of  authors;  European  Lower  Eocene  to  Miocene. 

Subfamily  Sicistinae. — Cheekteeth  brachydont,  |,  distinctly  quadri- 
tuberculate,  the  enamel  of  moderately  worn  upper  molars  with  a  simple 
heptamerous  pattern ;  external  form  murine,  the  hind  legs  and  feet  not 
lengthened. 

Sicista,  Recent,  Eurasia;  f  Eomys,  European  Upper  Eocene. 


442 


MILLER  AND  GIDLEY :  SUPERGENERIC  GROUPS  OF  RODENTS      443 

Subfamily  Zapodinae. — Cheekteeth  subhypsodont,|  or  |,  flat  crowned, 
the  enamel  pattern  of  the  upper  molars  heptamerous,  slightly  or  con- 
siderably modified;  external  form  saltatorial,  the  hind  legs  and  feet 
lengthened. 

Eozapus,  Recent,  China;  Zapus,  Napaeozapus,  Pleistocene  and 
Recent,  North  America. 

Family  Dipodidae 

Like  the  Zapodidae  but  with  the  inner  and  outer  metatarsals  reduced 
or  absent  and  the  three  median  fused  to  form  a  canon  bone;  cheekteeth 
hypsodont,  the  heptamerous  enamel  pattern  undergoing  modifications 
most  of  which  are  parallel  to  those  taking  place  in  the  teeth  of  the 
Cricetidae  and  in  the  hystricine  families. 

Subfamily  Protoptychinae. — Upper  cheekteeth  4,  moderately  hypso- 
dont; pm*  a  large,  functiorial  tooth;  skull  with  relatively  broad  rostrum 
and  narrow  braincase. 

Protoptychus;''  North  American  Upper  Eocene. 

Subfamily Dzpof/mae. — Cheekteeth  f  or  |,  strongly  hj^psodont;  pm< 
vestigial;  skull  with  relatively  narrow  rostrum  and  broad  braincase. 

The  Dipodidae  of  authors  who  recognize  the  Zapodidae  as  a  distinct 
family;  Pleistocene  and  Recent;   Eurasia  and  northern  Africa, 

Family  Ctenodactylidae 

Cheekteeth  growing  from  a  persistent  pulp,  the  adult  pattern  re- 
duced to  a  simple  ring  infolded  on  one  or  both  sides  (parallel:  Odo- 
dontinae);  external  form  fossorial. 

Ctenodactylus  and  related  genera  from  the  Mediterranean  region; 
Pliocene  to  Recent. 

Family  Pedetidae 

Cheekteeth  subterete,  growing  from  a  persistent  pulp;  all  trace  of 
the  original  crown  structure  lost,  the  unworn  enamel  cap  transversely 
cleft,  the  adult  pattern  consisting  of  a  narrow  median  infold  from  the 
paramere  extending  nearly  across  to  opposite  side;  external  form  con- 
spicuously saltatorial,  but  median  metatarsals  showing  no  tendency  to 
become  reduced  or  fused. 

Pedetes;  Recent;  Africa. 

Superfamily  BATHYERGOIDAE 

Zygomasseteric  structure  as  in  the  Dipodoidae  except:  Angular  por- 
tion of  mandible  distorted  outward  to  allow  passage  of  a  speciaHzed  and 

^  While  Protoptychus  is  a  true  dipodid  with  few  primitive  characters  its  exact 
position  is  not  clear.  It  may  prove  to  be  a  member  of  the  Theridomyinae;  but 
for  the  present  we  prefer  to  place  it  in  the  Dipodidae  on  account  of  its  resemblance 
to  the  recent  genus  Euchoreutes. 


443 


444    MILLER  AND  gidley:  supergeneric  groups  of  rodents 

enlarged  distal  anterior  limb  of  the  masseter  lateralis  superficialis,  its 
general  direction  parallel  with  zygoma.  Masseter  medialis  arising  from 
upper  margin  of  orbit  and  not  passing  through  small  infraorbital 
foramen. 

Family  Bathyergidae 

Skull  and  external  form  with  conspicuous  fossorial  adaptations. 
Cheekteeth  extremely  hypsodont,  though  not  ever-growing;  enamel 
pattern  in  adult  a  ring  with  or  without  a  reentrant  fold  on  one  or  each 
side  (parallel :  Octodontinae) ;  number  of  cheekteeth  ranging  from  |  to 
f .  (In  the  genus,  Heliophobius,  with  the  greatest  number  of  teeth  there 
are  never  more  than  |  functional  at  one  time;  the  apparent  addition  of 
one  tooth  in  the  upper  jaw  and  two  in  the  lower  jaw  to  the  maximum 
rodent  formula  is  probably  due  to  a  specialized  condition  of  the  milk 
dentition.) 

The  Bathyergidae  oi&Viihors;  Recent;  Africa. 

Superfamily  HYSTRICOIDAE 

Zygomasseteric  structure  as  in  the  Bathyergoidae  except:  Masseter 
medialis  arising  from  side  of  rostrum  and  passing  through  large  infra- 
orbital foramen. 

LATERALIS   SERIES 

Masseter  lateralis  the  chief  agent  in  modifying  form  of  outer  side  of 
mandible;  an  obhque  ridge  extending  forward  from  lower  border  of 
angular  process  usually  present  for  attachment  of  this  mascle. 

A. — Lachrymal  bone  small,  forming  no  important  part  of  zygomatic 
root,  its  lower  portion  confined  within  orbit;  lachyrmal  canal  closed  in  front 
of  orbit. 

Family  Hystricidae 

Skull  with  no  special  pecuharities  other  than  a  tendency  (most  pro- 
nounced in  the  genus  Hystrix)  to  inflation  of  the  rostral  and  frontal 
regions;  mandibular  rami  rather  freely  movable  at  symphysis;  angular 
process  deep,  neither  produced  backward  conspicuously  behind  articular 
level  nor  folded  inward  along  lower  margin;  cheekteeth  |,  their  enamel 
pattern  slightly  removed  from  the  simple  heptamerous  type,  the  re- 
entrant folds  narrow  and  not  angular. 

Old  World  porcupines;  Upper  Miocene  to  Recent. 

Subfamily  Hystricinae. — Base  of  upper  zygomatic  root  over  a  point 
decidedly  behind  the  anterior  extremity  of  toothrow;  cheekteeth 
strongly  hypsodont,  closed  at  base  but  without  definite  roots;  sacral 
vertebrae  4. 

Hystrix,  Acanthion,  Thecurus;  Africa,  southern  Asia,  and  Malay 
region. 


444 


MILLER  AND  GIDLEYI  SUPERGENERIC  GROUPS  OF  RODENTS      445 

Subfamily  Atherurinae. — ^Base  of  upper  zygomatic  root  over  anterior 
extremity  of  toothrow;  cheekteeth  subhypsodont,  with  well  developed 
roots;  sacral  vertebrae  3. 

Atherurus,  Trichys;  Recent;  Malay  region. 

Family  ERETHIZONTIDAE 

Like  the  Hystricidae  but:  Mandibular  rami  with  conspicuous  post- 
symphyseal  buttresses  which  prevent  movement  at  the  symphysis; 
lower  border  of  angular  process  folded  inward;  cheekteeth  subhypso- 
dont,  flat  crowned,  with  reduced-heptamerous  enamel  pattern  char- 
acterized by  narrow  ridges  and  wide  reentrant  spaces,  the  spaces  on  the 
paramere  tending  to  become  transformed  into  pits  (parallels:  Funis- 
ciurus,  Anomaluridae) .  Upper  zygomatic  root  over  anterior  part  of 
toothrow;  feet  noticeably  modified  for  arboreal  life. 

New  World  porcupines  except  Chaetomys:  Oligocene  to  Recent. 
Oligocene  of  Egypt?^  Extinct  South  American  genera:  Asteromys, 
Eosteiromys,  Parasteiromys,  Steiromys. 

Family  ECHIMYIDAE 

Like  the  Erethizontidae  but  lower  border  of  angular  process  usually 
with  no  evident  infolding,  feet  usually  not  modified  for  arboreal  life,  and 
adult  cheekteeth  with  narrow  reentrant  folds;  cheekteeth  varying  from 
brachydont  to  ever-growing,  the  structure  when  hypsodont  not  multi- 
laminar. 

Subfamily  Echimyinae. — Fos'sorial  specialization  usually  absent; 
skull  and  cheekteeth  showing  great  variety  of  form ;  enamel  pattern  not 
simplified  to  a  ring  with  an  infold  on  one  or  each  side. 

Tropical  America;  Miocene  to  Recent.  Spiny-rats  (provisionally 
including  Chaetomys) ,  Hutias  (Capromys,  Plagiodontia),  etc.;  also  many 
extinct  genera,  among  them  Acaremys,  Boromys,  Brotomys,  Colpostemma, 
Eocardia  (parallel:  Issiodoromys),  Eoctodon,  Graphvmys,  Gyrignophus, 
Haplostropha,  Heteropsomys,  Homopsomys,  Isolobodon,  Prospaniomys, 
Protadelphomys,  Protacaremys,  Sciamys,  Scleromys,  Spaniomys,  Sticho- 
mys,  Strophostephanus,  Trihodon.  It  is  probable  that  this  group  needs 
subdividing. 

Subfamily  Ododontinae. — Fofesorial  specialization  usually  present; 
cheekteeth,  except  in  earliest  known  genera,  with  enamel  pattern  com- 
pletely simplified  to  a  ring  with  an  infold  on  one  or  each  side  (parallel : 
Ctenodactylidae) . 

South  America;  Oligocene  to  Recent.  Recent  genera:  Ctenomys, 
Octodon,  Ododontomys,  Spalacopus.  Among  the  fossil  genera  are:  Ceph- 
alomys,  Dicoelophorus,  Eucoelophorus,  Litodontomys,  Neophanomys, 
Palaeododon,  Phtoramys,  Pithanotomys,  Plataeomys,  Scotomys. 

*  The  genera  Phiomys  and  Metaphiomys,  based  on  lower  jaws  and  teeth,  have 
no  characters  by  which  they  can  at  present  be  referred  to  any  other  family. 


445 


446      MILLER  AND  GIDLEY!  SUPERGENERIC  GROUPS  OF  RODENTS 

Family  Petromyidae 

In  general  resembling  the  Octodontinae  but  crown  of  each  cheektooth 
margined  by  two  elevations  on  the  protomere,  these  elevations  probably 
resulting  from  the  unusual  obliquity  at  which  the  teeth  appear  to  be  set. 
The  teeth  are  rooted,  strongly  hypsodont;  the  enamel  pattern  consists 
of  two  transverse  lobes  united  by  a  median  isthmus,  the  outer  edges  of 
the  lobes  becoming  joined  in  the  upper  teeth  when  worn.  No  speci- 
mens examined.^  Recognized  as  a  family  by  Tullberg,  partly  on  whose 
authority  we  continue  to  treat  it  as  distinct.  The  characters  of  the  teeth 
indicate  important  mechanical  peculiarities  of  the  chewing  apparatus. 
The  enamel  pattern  appears  to  be  of  a  type  which  could  be  directly  de- 
rived from  that  present  in  the  relatively  low-crowned  molars  of  Erethizon 
and  the  Oligocene  African  Phiomys. 

Petromys,  South  Africa:  Recent. 

Family  Myocastoridae 

In  general  like  the  Erethizontidae  but  upper  zygomatic  root  over 
middle  of  toothrow,  and  cheekteeth  with  structure  paralleling  that  pres- 
ent in  Castor;  lateral  process  of  paroccipital  large,  projecting  freely 
above  base  of  greatly  elongated  paroccipital  process;  in  living  species 
external  form  modified  for  aquatic  life. 

Myocastor  and  related  fossil  genera;  South  America;  Miocene  to 
Recent. 

Family  Thryonomyidae 

Like  the  Myocastoridae  but  cheekteeth  with  structure  paralleling 
that  present  in  some  of  the  Echimyinae,  and  lateral  process  of  paroc- 
cipital small,  closely  applied  to  base  of  moderately  large  paroccipital 
process;  external  form  not  modified  for  aquatic  life. 

Thryonomys;  Africa;  Recent. 

Family  Dinomyidae 

Like  the  Echimyidae  but  cheekteeth  combining  a  multilaminar 
structure  with  excessive  hyposodonty  (parallel :  Castoroides) ;  so  far  as 
known  the  external  form  is  robust,  terrestrial. 

South  America  and  the  Greater  Antilles;  Miocene  to  Recent.  In- 
cludes the  living  Dinomys  and  the  extinct  genera  Amblyrhiza,  Briar omys, 
Discolomys,  Elasmodontomys,  Gyriabrus,  Megamys,  Neoepiblema,  Olen- 
opsis,  Potamarchus,  Tetrastylus. 

Family  Cuniculidae 

Not  essentially  different  from  the  Dinomyidae;  but  the  jugal  and  part 
of  the  maxillary  are  expanded  to  form  a  conspicuous  cheekplate,  the 
surface  of  this  becoming  excessively  rugose  in  adult ;  cheekteeth  strongly 

»  Mr.  Oldfield  Thomas  has  kindly  sent  us  photographs  of  a  skull  in  the  British 
Museum  (No.  4.2.3.98). 


446 


MILLER  AND  GIDLEY:  SUPERGENERIC  GROUPS  OF  RODENTS      447 

hj^psodont,  but  enamel  structure  not  completely  multilaminar;  exter- 
nal form  robust,  terrestrial. 

Cuniculus  {  =  "Coeloge7iys");  Tropical  America;  Pleistocene  and 
Recent. 

Family  Heptaxodontidae 

First  tooth  of  maxillary  series  mechanically  dominant,  cheekteeth 
apparently  reduced  to  |,  conditions  not  known  elsewhere  in  the  Hystri- 
coidae,  and  indicating  zygomasseteric  development  along  a  line  different 
from  that  followed  elsewhere  in  the  group;  enamel  structure  multi- 
laminar  with  reduplication  in  the  anterior  tooth;  diagnostic  cranial 
characters  unknown. 

Heptaxodon;  Porto  Rico;  Pleistocene?  The  genus  Morenia  from  the 
South  American  Miocene  may  be  a  second  member  of  the  family;  it  is 
at  present  known  from  isolated  teeth  only. 

B. — Lachrymal  bone  large,  usually  forming  an  important  part  of  zygo- 
matic root,  its  lower  portion  extending  forward  out  of  orbit  to  a  level  in  front 
of  anterior  margin  of  infraorbital  foramen;  some  part  of  lachrymal  canal 
open  on  side  of  rostrum  in  front  of  orbit. 

Family  Dasyproctidae 

Skull  generalized  in  structure,  closely  resembling  that  of  the  less 
specialized  Hystricidae;  cheekteeth  hypsodont  but  with  a  nearly  unmod- 
ified heptamerous  structure,  paralleling  that  in  the  Hystricidae;  ex- 
ternal form  cursorial,  the  legs  lengthened,  the  digits  5-3.^" 

The  Dasyproctidae  of  authors  with  Cuniculus  removed  and  Neo- 
reomys  added;  South  and  Middle  America;  Miocene  to  Recent. 

Family  Chinchillidae 

Cheekteeth  with  heptamerous  structure  excessively  modified,  the 
enamel  pattern  consisting  of  parallel  transverse  laminae  (parallel: 
Diyiomyidae) ;  mandible  with  no  sharply  defined  ridge  for  attachment  of 
masseter  lateralis;  external  form  saltatorial. 

South  America;  Miocene  to  Recent.  Living  genera:  Chinchilla,  La- 
gostomus,  Viscaccia.  Extinct  genera:  Euphilus,  Perimys,  Pliolagosto- 
mus,  Prolagostomus,  Scotaeumys,  Sphaeromys. 

Family  Abrocomidae 

Like  the  Chinchillidae  but  cheekteeth  with  deep  reentrant  angles  on 
both  sides,  and  mandible  with  sharply  defined  ridge  for  attachment  of 
masseter  lateralis;  external  form  not  saltatorial. 

Abrocoma;  South  America;  Phocene  to  Recent. 

1°  The  feet  of  Neoreomys  are  imperfectly  known,  but  there  appears  to  be  notTi- 
ing  in  the  structure  of  the  parts  which  have  been  described  that  indicates  the 
presence  of  more  than  three  digits  in  the  hind  foot. 


447 


448    MILLER  AND  gidley:  supergeneric  groups  of  rodents 

MEDIALIS   SERIES 

Masseter  medialis  the  chief  agent  in  modifying  form  of  outer  side  of 
mandible;  a  conspicuous  horizontal  ridge  for  the  attachment  of  this 
muscle  present  on  side  of  mandible  slightly  below  alveolar  level. 

Family  Caviidae 

Posterior  cheektooth  both  above  and  below  without  reduplication  of 
elements,  the  general  character  of  the  toothrow  normal. 

The  Caviidae  of  authors  with  Hydrochoerus  and  its  alUes  removed; 
South  America;  Miocene  to  Recent.  Extinct  genera:  Anchimys,  Neo- 
procavia,  Orthomyctera,  Palaeocavia,  Phugatherium,  Procardiotherium. 

Family  Hydrochoeridae 

Posterior  cheektooth  both  above  and  below  with  conspicuous  redupli- 
cation of  elements,  the  general  character  of  the  toothrow  thus  rendered 
abnormal. 

Hydrochoerus  and  its  extinct  alhes  Plexochoerus,  Prohydrochoerus 
and  Protohydrochoerus;  perhaps  Cardiomys,  Caviodon  ( =  Diocartherium) 
and  Cardiotherium  also;  South  America,  Miocene  to  Recent;  south- 
eastern United  States,  Pleistocene. 


448 


GRADES  AND  CLADES  AMONG  RODENTS 

Albert  E.  Wood 
Biology  Department,  Amherst  College,  Amherst,  Massachusetts 

Accepted  September  30,  1964 

As  has  been  pointed  out  many  times,  the  that  is  an  advance  over  the  primitive  ro- 

rodents  are  the  most  abundant  and  sue-  dent  grade.    The  classic  suborders  repre- 

cessful  mammalian  order.    Their  evolution  sent  alternative  expressions  of  an  advanced 

has  been  channeled  into  a  single  major  di-  rodent    grade,    and    may    well    have    been 

rection  by  the  development,  as  an  initial  achieved     approximately     simultaneously, 

modification,  of  ever-growing,  gnawing  in-  The  various   clades  within   the  order   are 

cisors,  with  associated  changes  in  skull  and  still    not   clearly   recognizable,   and   much 

jaw  muscles.   Subsequent  evolution  has  in-  work   remains    to   be   done   before   rodent 

volved  a  great  deal  of  parallelism  within  cladal  classification  is  stabilized  to  every- 

the  order,  making  it  very  difficult  to  dis-  one's     satisfaction,     though     considerable 

entangle  the  convergent  and  parallel  changes  progress  is  being  made, 
from   those    that    are    truly    indicative   of  There  is  no  direct  evidence  as  to  the 

phyletic    relationship.     The    similarity    in  type  of  jaw  muscles  in  the  still  unknown 

complexity  of  the  evolutionary  pathways  ancestral    rodents    that    lived    during    the 

among  rodents  to  those  among  actinopteryg-  Paleocene.     However,    Edgeworth    (1935, 

ians,    and    particularly    teleosts,    has    also  pp.    73-75),    in    discussing    the    primitive 

been  pointed  out.  mammalian     jaw     musculature,     indicates 

Work  by  various  authors  has  indicated  that  a  major  part  of  it  consists  of  an  em- 

that  the  evolution  of  the  actinopterygians  bryological   single   muscle   mass,    divisible 

consists  of  the  sequential  attainment  of  a  into  the  Temporalis,  Zygomaticomandibiil- 

series  of  morphological  stages,   or   grades  aris,  and  Masseter.  The  Zygomaticomandi- 

(as  in  Huxley,   1958),  each  of  which  has  bularis  is  usually  divided  into  anterior  and 

been  derived  from  the  preceding  one  sev-  posterior  portions  by  the  masseteric  nerve, 

eral  independent  times  by  a  series  of  paral-  The  masseter  may  be  single  or  be  divisible 

lei  trends.    The  classification  of  actinopts  into  two  or  more  layers,  with  no  clear  in- 

at  the  supraordinal  level  involves  a  series  dications  as  to  which  is  the  primitive  con- 

of  taxa  that  are  currently  agreed  to  rep-  dition. 

resent  such  polyphyletic  grades  rather  than  Among  students  of  rodent  anatomy  there 

monophyletic   units   or   clades    (Schaeffer,  have  been  many  varying  interpretations  of 

1956,  p.  202).  the  jaw  musculature.    Usually,  the  Zygo- 

The    rodents    were,    classically,    divided  maticomandibularis  has  been  considered  to 

into  three  suborders  on  the  basis  of  the  be  part  of  the  masseter  {Masseter  medialis 

structure  of  the  jaw  musculature  and  as-  of   Tullberg,    1899,   pp.    61-62;    Masseter 

sociated  osteological  differences — the  Sciur-  profundus  of  Howell,  1932,  pp.  410-411), 

omorpha,      Myomorpha,     and     Hystrico-  but  sometimes  it  is  treated  as  a  separate 

morpha  (Simpson,  1945).  All  recently  pro-  muscle   (Lubosch,   1938,  p.   1068;   Miiller, 

posed  classifications  of  the  order  (Lavocat,  1933,  pp.   14-24).    The  two  parts  of  the 

1956;  Schaub,  1958,  p.  691-694;  Simpson,  masseter  of  Edgeworth  are   the  Masseter 

1959;  and  Wood,  1955a  and  1959),  adopt  lateralis  super jicialis  and  Masseter  lateralis 

the  multiplicity  of  major  groups  postulated  profundus   of   Tullberg,    or    the   Masseter 

by  Miller  and   Gidley    (1918)    or   Winge  superficialis  and  Massetermajor  oiUoweW. 

(1924),  and  agree  that  the  three  classic  Lubosch  (1938,  fig.  930)  and  Muller  (pp. 

suborders  are  not  monophyletic  clades,  but  19-20)    also    consider    the    anterointernal 

rather,  taken  as  a  whole,  represent  a  grade  portion  of  what  is  usually  called  the  mas- 

EvoLUTiON  19:  115-130.    March,  1965  115 


449 


116 


ALBERT  E.  WOOD 


seter  to  be  a  distinct  muscle,  the  Maxillo- 
mandibularis . 

In  the  following  discussion,  the  masseter 
is  considered  to  consist  of  three  parts — 
the  Masseter  super jicialis,  arising  from  the 
anterior  end  of  the  zygoma  or  the  side  of 
the  snout  and  inserting  on  the  ventral 
border  of  the  angle  ( =  Masseter  lateralis 
super jicialis);  the  Masseter  lateralis,  aris- 
ing from  most  of  the  length  of  the  lateral 
surface  of  the  zygoma  and  inserting  on 
the  ventral  part  of  the  angular  process  (  = 
Masseter  lateralis  profundus;  Masseter 
major) ;  and  the  Masseter  medialis,  arising 
from  the  medial  side  of  the  zygoma,  whence 
it  has  sometimes  spread  to  the  medial  wall 
of  the  orbit  or  forward  through  the  infra- 
orbital foramen,  and  inserting  on  the  dor- 
sal portion  of  the  masseteric  fossa  of  the 
jaw  {=  Masseter  profundus;  Zygomatico- 
mandibularis;  Maxillomandibularis) .  These 
are  illustrated  in  Figs.  1-4. 

The  separation  of  evolutionary  grades 
among  the  rodents  can  best  be  done  on 
the  basis  of:  (1)  the  incisor  pattern  and 
structure;  (2)  the  structure  of  the  jaw 
muscles  and  the  associated  areas  of  the 
skull  and  jaws;  and  (3)  the  general  pat- 
tern and  height  of  crown  of  the  cheek 
teeth.  These  can  be  used  as  general  clues 
to  evolutionary  grades  throughout  the 
order.  The  discussion  below  will  largely  be 
limited  to  these  sets  of  criteria.  On  the 
other  hand,  the  separation  and  identifica- 
tion of  the  clades  must  involve  the  use  of 
all  available  data,  and  must  not  select  one 
set  of  structures  as  the  most  critical  one, 
with  other  criteria  neglected. 

Grade  One — Protrogomorph  Radiation 

The  initial  recorded  rodent  radiation, 
known  from  the  Eocene  but  presumably 
having  gotten  well  started  in  the  later 
Paleocene,  involved  animals  that  had  al- 
ready acquired  the  basic  gnawing  adapta- 
tions. 

The  incisors  were  ever-growing,  with  the 
enamel  limited  to  an  anterior  band,  giving 
the  perpetual  chisel-edge  that  characterizes 
the  Rodentia.    The  upper  incisor  was  re- 


curved, the  worn  surface  being  nearly  ver- 
tical, and  the  lower  incisor  acted  against  it 
by  moving  upward  and  forward.  The 
enamel  cap  had  extended  around  the  edges 
of  the  incisor,  on  both  medial  and  lateral 
faces,  to  brace  it  better  against  the  stresses 
of  gnawing.  The  incisor  enamel  is  of  con- 
stant distribution  on  the  incisor  cross  sec- 
tion, once  the  animal  reached  its  adult  size. 
Histologically,  the  incisor  enamel  in  the 
Eocene  members  of  the  group  is  of  the 
type  called  pauciserial  by  Korvenkontio 
(1934,  p.  97,  and  fig.  1),  in  which  the 
enamel  is  made  up  of  irregular  bands,  rang- 
ing from  a  single  row  of  enamel  prisms,  to 
as  many  as  three  or  four  rows  of  prisms. 
A  change  to  the  uniserial  type  of  enamel 
{op.  cit.,  p.  130)  has  taken  place  in  mem- 
bers of  this  radiation  by  the  Oligocene. 

As  in  all  known  rodents,  there  were  no 
pre-  or  postglenoid  processes,  the  glenoid 
fossa  being  elongate  and  slightly  inclined 
from  rear  to  front,  so  that  the  jaw  could 
be  moved  backward  bringing  the  cheek 
teeth  into  occlusion,  or  forward  bringing 
the  incisors  together  and  separating  the 
cheek  teeth,  vertically. 

The  dental  formula  had  been  reduced  to 
the  most  primitive  that  is  still  found  in  liv- 
ing rodents,  namely  I^,  0°,  Pf,  M-^.  The 
cheek  teeth  were  low-crowned  and  cuspi- 
date in  the  earliest  family  (Paramyidae) 
or  higher  crowned  and  crested  in  derived 
families  (Ischyromyidae,  Sciuravidae), 
but  were  always  based  on  a  pattern  of  no 
more  than  four  transverse  crests.  Occa- 
sional Eocene  forms  plus  most  later  ones 
had  hypsodont  or  even  ever-growing  cheek 
teeth  (Cylindrodontidae,  Aplodontoidea). 
Locomotion  was  largely  scampering  (or 
arboreal  scampering),  though  some  deriva- 
tives of  this  group  had  developed  burrow- 
ing locomotion  (Cylindrodontidae,  Myla- 
gualidae),  and  some  may  have  been  salta- 
torial  (Protoptychidae). 

The  angle  of  the  lower  jaw  was  essen- 
tially in  the  same  vertical  plane  as  the 
rest  of  the  jaw,  as  is  usual  among  mam- 
mals. Specifically,  it  is  usually  in  the 
plane  of  the  incisive  alveolus   (sciurogna- 


450 


RODEiNT  GRADES 


117 


Fig.  1.  Skull  of  the  Eocene  protrogomorph  Ischyrotomus,  with  the  jaw  musculature  restored,  X 
1.  Abbreviations:  M.  LAT. — Masseter  lateralis,  dashed  portions  lying  beneath  Masseter  super jicialis; 
M.  PROF. — dashed  lines  indicating  the  course  of  the  Masseter  profundus;  M.  SUP. — Masseter  super- 
jicialis;  PT.  E. — dashed  line  indicating  course  of  Pterygoideus  externus;  TEMP. — Temporalis. 


thous),  though  occasionally  {Reithropara- 
mys — Wood,  1962,  fig.  41E)  it  has  shifted 
to  a  position  just  laterad  of  the  alveolus 
(incipiently  hystricognathous) . 

The  chief  components  of  the  jaw  mus- 
culature were  the  temporal,  the  pterygoid, 
and  the  masseter.  All  showed  a  certain 
amount  of  differentiation  (Fig.  1).  In  a 
form  such  as  Ischyrotomus,  the  temporal 
was  a  large,  fan-shaped  muscle,  arising  in 
a  semicircle  from  the  frontal  and  parietal, 
and  inserting  on  the  coronoid  process.  Al- 
though the  anterior  fibers  had  a  forward 
component  and  the  posterior  ones  a  back- 
ward component,  its  primary  function  was 
to  raise  the  jaw,  which  pivoted  about  the 
condyle.  The  internal  pterygoid,  arising 
on  the  inner  side  of  the  pterygoid  fossa 
and  inserting  on  the  inner  surface  of  the 
angle  (Wood,  1962,  fig.  69B),  pulled  the 
jaw  toward  the  midline  as  well  as  closing 
it.  The  external  pterygoid  (Fig.  1  PTE) 
arose  on  the  external  pterygoid  process 
and  inserted  on  the  medial  surface  of  the 
condyle.  It  helped  to  pull  the  jaw  mesiad, 
but  very  largely  served  to  slide  the  condyle 
forward  and  ventrad,  along  the  glenoid 
cavity,  to  disengage  the  cheek  teeth  and 
bring  the  incisor  tips  into  contact.  The 
jaw  was  moved  back  again  by  the  com- 


bined action  of  the  temporal  and  the  digas- 
tric. 

In  Ischyrotomus  the  areas  of  origin  and 
insertion  of  the  Masseter  super  jicialis,  M. 
lateralis,  and  M.  medialis  are  readily  sep- 
arable (Fig.  1).  The  Masseter  medialis 
arose  from  the  medial  surface  of  the  zy- 
goma and  inserted  on  the  dorsal  surface 
of  the  masseteric  fossa  of  the  lower  jaw. 
It  pulled  the  jaw  nearly  straight  upward. 
There  was  the  beginning  of  a  differentia- 
tion of  this  muscle  into  two  portions,  the 
anterior  inserting  on  the  masseteric  tuberos- 
ity by  a  separate  tendon.  It  seems  prob- 
able that  these  parts  were  separated  by 
the  masseteric  nerve.  The  Masseter  later- 
alis arose  from  a  fossa  extending  most  of 
the  length  of  the  zygoma,  and  occupying 
the  ventral  third  of  the  arch.  It  inserted 
over  much  of  the  lateral  surface  of  the 
angle,  and  pulled  the  lower  jaw  laterally, 
upward,  and  slightly  forward.  The  most 
superficial  of  the  three  divisions  of  the 
masseter  was  the  Masseter  super  jicialis, 
which  arose  from  the  masseteric  fossa  on 
the  base  of  the  maxillary  portion  of  the 
zygoma,  immediately  laterad  of  the  upper 
premolars,  and  inserted  along  the  ventral 
margin  of  the  jaw  all  the  way  to  the  angle. 


451 


118 


ALBERT  E.  WOOD 


M.  S  U  P. 
Fu;.  2.     Skull  ul   Ihc  sciuromoiphous  sciurid  Mannota,  X  1-    Abbreviations  as  for  Fig.  1. 


It  was  the  major  element  in  [Hilling  the 
lower  jaw  forward,  and  hence  in  gnawing. 

The  functional  activity  of  the  jaws  was 
composed  of  three  parts  (Becht,  1953,  p. 
515).  A  vertical  or  transverse  movement, 
with  the  condyle  toward  the  posterior  end 
of  the  glenoid  cavity,  was  used  in  the  chew- 
ing activities  of  the  cheek  teeth.  This 
would  have  involved  the  use  of  the  main 
[)art  of  the  temporal,  the  two  inner  parts 
of  the  masseter,  and  the  internal  pterygoid, 
and  is  the  usual  mammalian  chewing  ac- 
tivity. If  the  condyle  were  moved  forward 
to  the  anterior  end  of  the  sloping  glenoid 
cavity,  the  cheek  teeth  would  be  disen- 
gaged, and  the  same  combination  of  mus- 
cles plus  the  Masseter  super jicialis  would 
provide  the  motion  of  the  lower  incisor 
against  the  upper,  resulting  in  gnawing. 
The  third  component,  the  shift  from  the 
first  position  to  the  second,  would  be 
brought  about  by  the  anterior  portion  of 
the  temporal,  the  external  pterygoid,  and 
the  Messeter  super  jicialis;  the  reverse  by 
the  posterior  portion  of  the  temporal  and 
the  digastric. 

The  members  of  this  grade  include 
nearly  all  of  the  pre-OIigocene  rodents  of 
North  America  and  Asia  and  some  of 
those  of  Europe  (none  being  known  from 
the  rest  of  the  world).  Several  lines  sur- 
vive into  the  Oligocene  or  early  Miocene, 
and  the  Aplodontoidea  occur  from  the 
Oligocene  to  the  present,  mostly  in  North 


America,  although  some  aplodontids  are 
present  in  Palaearctica.  This  grade  seems 
to  include  forms  so  related  that  they  may 
be  considered  to  be  a  clade,  the  Suborder 
Protrogomorpha. 

Grade  Two — Second  Radiation 

Gnawing  in  the  method  outlined  above 
was  effective  and  presumably  more  effi- 
cient than  that  of  the  multituberculates  or 
any  of  the  other  gnawing  groups  that  were 
competing  with  the  rodents  in  the  Eocene. 
But  the  gradual  filling  of  the  available 
niches  resulted  in  greater  intra-ordinal 
competition  and  increased  selective  value 
for  more  efficient  use  of  the  incisors, 
which  was  brought  about  by  a  series  of 
changes  involving  the  muscles  of  mastica- 
tion, the  skull  structure,  the  incisors,  and 
the  cheek  teeth. 

The  modifications  of  the  masseter  mus- 
cle and  the  concomitant  skull  changes 
were  the  most  prominent  alterations  lead- 
ing to  Grade  Two.  These  changes  involved 
either  the  Masseter  lateralis  or  the  Mas- 
seter medialis  or  both,  the  Masseter  super- 
jicialis  remaining  essentially  unchanged. 

The  Masseter  lateralis  may  shift  forward 
and  upward,  behind  and  median  to  the 
origin  of  the  Masseter  super  jicialis,  onto 
the  front  of  the  zygomatic  arch  (Fig.  2). 
The  shift  was  beginning  in  the  ischyromy- 
ids  Titanothcriomys  (Wood,  1937,  pp. 
194-195,  pi.  27,  fig.  1,  la,  lb)  and  Ischy- 


452 


RODENT  GRADES 


119 


Fig.  3.     Skull  of  the  hystricomorphous  caviomorph  Myocastor,   X  1-    Abbreviations  as  lor  Fig.   1. 
Ventral  part  of  M .  profundus  dotted. 


romys  troxelli  {op.  cit.,  p.  191;  Burt  and 
Wood,  1960,  p.  958),  where  the  muscle 
was  below,  instead  of  lateral  to,  the  infra- 
orbital foramen.  This  process  continued, 
with  the  muscle  origin  moving  forward  and 
upward  along  the  anterior  face  of  the 
zygoma,  passing  lateral  and  dorsal  to  the 
infraorbital  foramen,  eventually  reaching 
almost  to  the  top  of  the  snout  and  forward 
onto  the  premaxillary.  This  pattern  char- 
acterizes the  sciuromorphous  rodents — the 
Sciuridae,  Castoroidea,  and  Geomyoidea. 
This  shift  of  origin  has  changed  the  direc- 
tion of  pull  of  the  anterior  part  of  the 
Masseter  lateralis  by  30  to  60°,  so  that 
it  essentially  parallels  the  Masseter  super- 
jicialis,  greatly  strengthening  the  forward 
component  of  masseteric  action  (Fig.  2). 

In  other  rodents,  the  anterior  part  of 
the  Masseter  medialis  has  spread  from  the 
inner  surface  of  the  zygoma  (or,  perhaps, 
from  the  medial  margin  of  the  orbit)  for- 
ward through  the  enlarged  infraorbital  fora- 
men onto  the  snout  (Fig.  3).  In  extreme 
cases,  its  origin  extends  as  far  forward  as 
the  premaxilla,  almost  reaching  the  pos- 
terior end  of  the  external  nares  (Hydro- 
choerus,  Pedetes,  Thryonomys).  This  gives 
an  almost  horizontal  resultant  to  the  con- 
traction of  this  muscle,  and  strongly  aug- 


ments the  horizontal  action  of  the  Mas- 
seter superjicialis.  This  pattern  charac- 
terizes the  hystricomorphous  rodents — the 
Caviomorpha;  the  Dipodoidea.  Theridom- 
yoidea,  and  Thryonomyoidea;  and  the 
Anomaluridae,  Ctenodactylidae,  Hystrici- 
dae,  and  Pedetidae. 

The  Bathyergidae  have  developed  per- 
haps the  most  massive  masseters  of  any  of 
the  rodents,  although  there  seems  to  have 
been  very  little  shifting  of  the  muscles 
(TuUberg,  1899,  p.  78).  The  Masseter 
medialis  has  a  broad  expanse  on  the  me- 
dian side  of  the  orbit  (perhaps  associated 
with  the  reduction  of  the  eyes)  and  is  con- 
fluent with  the  anterior  end  of  the  Tem- 
poralis (Tullberg,  op.  cit.,  p.  75,  and  pi.  2, 
figs.  8-10,  17-18).  In  most  members  of 
the  family,  no  part  of  the  Masseter  medi- 
alis passes  through  the  small  infraorbital 
foramen,  but  in  Cryptomys  {— Georychus 
coecutiens,  Tullberg,  1899.  p.  79)  a  small 
portion  just  edges  through  the  foramen 
{op.  cit..  pi.  2,  fig.  17).  Landry  (1957, 
pp.  66-67)  has  argued  that  the  small  size 
of  the  infraorbital  foramen  and  the  limited 
forward  extent  of  the  Masseter  medialis 
are  secondary  modifications  of  a  hystrico- 
morphous pattern,  and  that,  in  spite  of 
their  differences,  this  familv  is  relativelv 


453 


120 


ALBERT  E.  WOOD 


Fig.  4.     Skull  of  the  myomorphous  cricetid  Ondatra,   X  1-5. 
part  of  M .  profundus  dotted. 


Abbreviations  as  for  Fig.   1.    Ventral 


closely  related  to  the  Hystricidae.  Most 
authors  would  not  accept  this  conclusion. 
Since  the  earliest  known  bathyergids,  from 
the  Miocene  of  Kenya,  were  essentially 
identical  in  masseteric  structure  to  living 
forms  (Lavocat,  1962,  p.  292),  it  is  im- 
possible to  be  certain  of  the  direction  of 
evolutionary  change  in  this  group.  How- 
ever, the  Masseter  lateralis  seems  to  be  in 
the  process  of  spreading  forward  and  up- 
ward onto  the  anterior  side  of  the  snout. 
This,  together  with  the  enlarged  expanse 
of  the  Masseter  medialis  on  the  mesial  side 
of  the  orbit,  seem  to  be  jaw  muscle  migra- 
tions sufficient  to  place  these  forms  in 
Grade  Two. 

The  expansion  of  the  Masseter  medialis 
onto  the  medial  as  well  as  lateral  side  of 
the  orbit  in  bathyergids  (TuUberg,  1899, 
pi.  2)  and  in  Castor  {op.  cit.,  pi.  22,  fig. 
9),  putting  it  in  an  ideal  position  to  ex- 
pand through  the  infraorbital  foramen  if 
that  opening  were  large  enough,  was  prob- 
ably a  structural  antecedent  of  the  hys- 
tricomorphous  pattern.  Whether  or  not  it 
indicates  any  close  relationship  between 
these  forms  and  any  histricomorphous  ro- 
dents is  arguable. 

Finally,  in  the  myomorphous  rodents, 
both  the  Masseter  lateralis  and  the  Mas- 


seter medialis  have  migrated,  combining 
the  features  of  the  sciuromorphous  and 
hystricomorphous  groups  (Fig.  4).  This 
pattern  characterizes  the  Muroidea,  Spala- 
coidea,  and  Gliroidea.  Such  a  type  of  mas- 
seter gives  the  greatest  anteroposterior 
component  of  any  of  the  types  of  rodent 
jaw  musculature,  with  the  possible  excep- 
tion of  the  paca  {Cunicidus).  It  is  perhaps 
not  a  coincidence  that  this  pattern  is  found 
in  the  Muroidea,  the  most  successful  and 
cosmopolitan  of  all  rodents. 

At  the  same  time  that  these  changes  in 
the  masseter  were  occurring,  the  temporal 
muscle  withdrew  in  most  forms  from  the 
anterior  area  where  it  originated  in  Ischy- 
rotomus,  and  is  restricted  in  its  origin  to 
areas  behind  the  tip  of  the  coronoid  proc- 
ess. In  such  forms  it  serves  to  raise  the 
lower  jaw  and  close  the  mouth  or  joins 
with  the  digastric  and  part  of  the  Masseter 
medialis  to  move  the  jaw  backward.  How- 
ever, the  temporal  keeps  its  anterior  area 
of  origin  in  the  Bathyergidae  and  in  some 
of  the  Rhizomyidae.  Whether  the  condi- 
tions in  these  two  families  are  primitive 
or  secondary  is  unknown.  The  reduction 
of  the  temporal  muscle  continued  in  many 
rodents,  especially  those  with  enlarged 
auditory  bullae  (Howell,  1932,  p.  411),  so 


454 


RODENT  GRADES 


12 


that  in  some  it  eventually  became  reduced 
to  an  exceedingly  minute  slip  (Tullberg, 
1899,  pi.  9,  figs.  8-9,  Ctenodactylus;  pi. 
10,  figs.  8-9,  Pedetes;  pi.  12,  Dipus  and 
Alactaga;  and  pi.  23,  figs.  18-20,  Dipod- 
oniys). 

All  of  the  sciuromorphous  and  myo- 
morphous  rodents  and  a  number  of  the 
hystricomorphous  ones  (Theridomyoidea, 
Anomaluridae,  Ctenodactylidae,  and  Pede- 
tidae)  have  an  angular  process  of  the 
sciurognathous  type,  with  the  angle  in  the 
plane  of  the  incisive  alveolus.  This  is  un- 
doubtedly the  primitive  condition.  In  the 
other  hystricomorphous  rodents,  the  angle 
has  shifted  until  it  arises  quite  markedly 
laterad  of  the  incisor.  This  would  make 
the  Masseter  lateralis  and  M.  superjicialis 
more  nearly  vertical.  This  hystricogna- 
thous  arrangement  is  fully  developed  in  the 
earliest  known  (early  Oligocene)  members 
of  the  South  American  subordinal  clade 
Caviomorpha  (Wood  and  Patterson,  1959, 
p.  289)  and  of  the  African  clade  Thryono- 
myoidea  (Wood,  ms.  1),  as  well  as  in  the 
Hystricidae,  apparently  of  south  Asiatic 
origin  (Lavocat,  1962,  pp.  292-293),  and 
in  the  Bathyergidae. 

Associated  with  these  changes  in  the  jaw 
muscles,  but  not  necessarily  occurring  at 
precisely  the  same  time,  nor  necessarily 
functionally  correlated,  there  have  been 
changes  in  the  incisors,  involving  both  their 
angulation  and  their  histology.  The  lower 
incisors  have  usually  become  arcs  of  larger 
circles,  so  that  they  are  more  nearly  hori- 
zontal, with  the  tips  moving  anteroposte- 
riorly  against  the  upper  incisors.  The  upper 
incisors  have  tended  to  become  either 
larger  or  smaller  arcs,  so  that  the  tips  tend 
to  point  either  forward  (true  usually  of 
burrowing  forms),  or  slightly  backward  as 
is  true  of  most  living  rodents.  The  former 
of  these  adjustments  increases  the  ability 
to  use  the  incisors  as  digging  implements, 
with  a  corresponding  increase  in  the  rate 
of  growth  of  the  incisors,  which  reaches 
almost  0.5  cm  per  week  in  the  lower  in- 
cisors of  geomyids  (Manaro,  1959).  The 
second  change  brings  the  enamel  blades  of 


the  up|)er  and  lower  incisors  more  nearly 
into  direct  opposition  than  was  true  in 
Grade  One. 

Changes  also  took  place  in  the  histology 
of  the  incisor  enamel.  The  pauciserial  type 
has  been  modified,  in  members  of  Grade 
Two,  in  two  different  directions.  In  the 
uniserial  type  (Korvenkontio,  1934,  p. 
227),  the  lamellae  are  regular,  and  made 
up  of  one  row  of  prisms  each,  with  the 
prisms  oriented  in  opposite  directions  in 
successive  lamellae.  This  pattern  is  found 
in  the  Sciuridae,  Castoridae,  Geomyoidea, 
Gliridae,  Muroidea,  Spalacidae,  Dipodoid- 
ea,  and  Anomaluridae  among  members  of 
Grade  Two,  and  in  Aplodontia,  Menisco- 
mys,  and  Ischyromys  among  the  members 
of  Grade  One  (Korvenkotio,  1934,  table 
on  pp.  116-123). 

The  situation  among  the  Theridomy- 
oidea is  most  instructive.  In  the  middle 
Eocene  to  Oligocene  Pseudosciuridae, 
which  are  fully  hystricomorphous  in  the 
infraorbital  structure,  the  incisors  are  still 
pauciserial.  The  same  is  true  of  the  more 
primitive  members  of  the  Theridomyidae, 
such  as  Thcridomys.  In  more  advanced 
theridomyids,  there  is  a  complete  transi- 
tion to  the  uniserial  type  of  enamel.  In 
Issiodoromys  \  =  Nesokerodon]  minor, 
Korvenkontio  describes  the  enamel  as 
"pauci-uniserial"  (op.  cit.,  p.  116).  He 
further  describes  that  of  Protechimys  gra- 
cilis as  pauciserial,  and  that  of  Archacomys 
laurillardi  as  uniserial.  These  two  forms 
are  currently  recognized  as  being  two  spe- 
cies of  Archacomys  (Schaub,  1958,  figs. 
48-49).  So  in  the  Theridomyoidea,  the 
transition  from  Grade  One  to  Grade  Two 
has  occurred  later  in  the  incisor  enamel 
than  it  did  in  the  jaw  musculature,  the  two 
apparently  being  completely  independent. 

A  different  type  of  enamel  modification 
occurs  in  what  Korvenkontio  {op.  cit.,  p. 
130)  calls  the  multiserial  type.  Here  each 
lamella  is  formed  of  four  to  seven  identi- 
cally oriented  rows  of  prisms,  the  lamellae 
lying  at  an  angle  of  about  45°  to  the  sur- 
face of  the  enamel.  Successive  lamellae 
have  the  prisms  oriented  in  opposite  direc- 


455 


122 


ALBERT  E.  WOOD 


tions  (Korvenkontio,  1934,  pi.  8,  figs.  3, 
5,  7).  This  occurs  in  the  Caviomorpha, 
and  the  Bathyergidae,  Ctenodactylidae, 
Hystricidae,  and  Pedetidae. 

Finally,  there  are  likely  to  be  differences 
in  cheek-tooth  formula  or  pattern  associ- 
ated with  the  change  to  Grade  Two  from 
Grade  One.  Primitively,  the  rodent  cheek- 
tooth formula  was  Pf  and  M^,  although 
some  members  of  Grade  One  have  lost  P'^. 
This  tooth  has  been  preserved  today  only 
in  Aplodontia  and  among  the  Sciuridae.  In 
many  rodents  (most  Caviomorpha,  Anom- 
aluridae,  Castoroidea,  Ctenodactylidae, 
Geomyoidea,  Gliroidea,  Hystricidae,  and 
probably  Pedetidae),  V\  have  been  re- 
tained. In  such  caviomorphs  as  the 
Echimyidae  (Friant,  1936)  and  Capromy- 
idae  (Wood  and  Patterson,  1959,  p.  324) 
and  in  the  living  African  Thryonomyoidea 
(Wood,  1962,  p.  316-317),  the  permanent 
premolars  have  been  suppressed  and  the 
deciduous  premolars  are  retained  through- 
out life.  This  may  also  be  true  for  the 
Pedetidae  (Wood,  ms.  2).  According  to 
Schaub  (1958,  p.  678),  the  reverse  of  this 
process  occurs,  with  the  elimination  of  the 
deciduous  tooth  in  many  hystricomorphous 
forms.  Finally,  the  Muroidea  and  Spalacoi- 
dea  have  lost  all  the  premolars  and  the 
Dipodoidea  have  almost  reached  this  stage. 

In  summary,  in  Grade  Two,  there  is  a 
tendency  to  reduce  the  length  of  the  tooth 
row,  probably  an  adaptation  permitting 
greater  contrast  between  the  gnawing  and 
chewing  activities,  and  therefore  greater 
specialization  in  each.  Usually,  the  loss 
of  these  teeth  occurred  at  times  when  there 
are  still  gaps  in  the  paleontological  history 
of  the  groups.  However,  the  loss  of  P^  oc- 
curs within  the  known  history  of  the 
Eomyidae  (Wood,  19S5b)  and  Gliridae 
(Schaub,  1958,  figs.  201,  203),  and  the 
presence  of  P^  is  variable  in  living  mem- 
bers of  the  Dipodidae  (Schaub,  1958,  p. 
792). 

Although  the  loss  of  cheek  teeth  brought 
about  greater  specialization  of  gnawing  and 
chewing  activities,  it  may  have  interfered 
with  the  functional  activities  of  chewing, 


since  in  almost  all  members  of  Grade  Two 
there  has  been  a  tendency  secondarily  to 
elongate  the  cheek  teeth  by  developing  an 
additional  transverse  crest  (mesoloph  or 
mesolophid)  in  the  middle  of  the  teeth, 
making  them  five-crested  in  contrast  to 
the  four-crested  pattern  found  in  Grade 
One.  This  five-crested  stage  seems  cer- 
tainly to  have  developed  independently  in 
many  lines,  and  therefore  is  no  better  than 
any  other  single  criterion  in  determining 
the  phylogenetic  relationships  (clades) 
among  the  rodents. 

The  changes  in  the  jaw  musculature  look 
as  though  they  are  indicative  of  genetic  re- 
lationships (i.e.,  clades),  and  were  so  used 
by  most  authors  as  far  back  as  Brandt 
(1855)  or  even  earlier,  until  fairly  recent- 
ly, giving  three  suborders  of  rodents,  the 
Sciuromorpha,  Hystricomorpha,  and  Myo- 
morpha  (see  Simpson,  1945). 

However,  the  use  of  other  criteria  for 
rodent  classification  complicated  this  ap- 
parently simple  pattern.  Tullberg  (1899), 
for  example,  showed  that  rodents  could  be 
divided  into  two  groups  on  the  basis  of 
the  way  in  which  the  angle  of  the  lower 
jaw  originated — the  Sciuragnathi,  in  which 
the  angle  arises  in  the  plane  of  the  alveolus 
of  the  lower  incisor,  and  the  Hystricogna- 
thi,  in  which  it  arises  lateral  to  this  plane. 
The  hystricognathous  forms  include  only 
those  that  are  more  or  less  hystricomor- 
phous, whereas  the  sciurognathous  ones 
may  be  sciuromorphous,  myomorphous  or 
hystricomorphous. 

With  an  increase  in  the  detailed  studies 
of  rodent  paleontology  since  1920,  the 
chance  that  any  of  the  three  Brandtian 
suborders  represents  a  clade  has  become 
progressively  smaller,  and  students  of 
fossil  rodents  have  universally  abandoned 
them  at  present. 

The  Sciuromorpha  may  be  considered 
to  be  typical.  The  sciuromorphous  condi- 
tion was  achieved  by  the  squirrels  (Sciur- 
idae) in  a  transition,  which  is  as  yet  not 
completely  documented  but  that  seems 
very  probable,  from  a  mid-Eocene  para- 
myid  such  as  Uriscus  (Wood,  1962,  p.  247; 


456 


RODENT  GRADES 


123 


Black,  1963,  p.  229).  A  similar  trend,  not 
carried  so  far,  is  seen  in  the  Oliuocene 
ischyromyids,  Titanotheriomys  (Wood, 
1937,  pp.  194-195)  and  some  species  of 
Ischyromys  (Burt  and  Wood,  1960,  p. 
958).  These  forms  could  not  be  in  the 
ancestry  of  the  squirrels,  as  their  cheek- 
tooth pattern  is  much  more  advanced  than 
is  that  of  the  squirrels. 

The  sciuromorphous  Geomyoidea  (in- 
cluding the  e.xtinct  Eomyidae  as  well  as  the 
Geomyidae  and  Heteromyidae)  seem  to 
have  many  fundamental  similarities  espe- 
cially in  the  basicranium  (Wilson,  1949, 
pp.  42-48;  Galbreath,  1961,  pp.  226-230), 
to  the  myomorphous  IMuroidea  (Muridae, 
Cricetidae),  and  have  probably  come  from 
a  common  source.  Whether  this  source  was 
a  sciuromorphous  form,  among  some  of 
whose  descendants  the  Masseter  medialis 
shifted  forward,  or  whether  it  was  a  pro- 
trogomorphous  form,  and  one  group  of 
descendants  shifted  the  Masseter  lateralis 
alone  and  the  other  shifted  both  branches 
of  the  muscle  simultaneously,  is  completely 
unknown.  It  seems  rather  probable,  how- 
ever, that  the  Geomyoidea  and  the  Muro- 
idea  are  descended  from  some  member  of 
Grade  One  that  would  be  included  among 
the  Sciuravidae.  The  jaw  mechanism  of 
the  beavers  (Castoridae)  and  their  Oligo- 
cene  to  Miocene  relatives,  the  Eutypomy- 
idae,  is  almost  identical  to  that  of  the 
squirrels,  except  for  the  expansion  of  the 
Masseter  medialis  onto  the  median  side  of 
the  orbit.  At  present  there  is  no  evidence 
as  to  the  pre-beaver  ancestry  of  this  group. 
The  tooth  structure  of  the  Castoroidea  is 
completely  different  from  that  of  any  of 
the  other  sciuromorphous  rodents,  which 
has  led  Schaub  to  include  them,  with  the 
Theridomyoidea  and  Hystricoidea,  in  his 
Infraorder  Palaeotrogomorpha  (1958,  p. 
694).  This  association  seems  unnatural. 
It  is  possible  that  there  is  a  special  rela- 
tionship of  the  beavers  with  either  the 
ischyromyids  or  the  sciurids,  although  the 
presence  of  five-crested  teeth  in  both  upper 
and  lower  jaws  of  the  beavers  makes  this 
seem  very  unlikely. 


The  evidence  that  masseteric  structure 
represents  a  grade  is  equally  clear  among 
the  hystricomorphous  rodents.  These  in- 
clude the  Old  World  porcupines  (Hystri- 
cidae) ;  the  African  Oligocene  to  Recent 
Thryonomyoidea  (Cane  Rats,  Rock  Rats, 
and  Phiomyidae);  the  isolated  African 
families  Anomaluridae,  Bathyergidae,  Cten- 
odactylidae,  and  Pedetidae;  the  European 
Eocene  to  Oligocene  Theridomyoidea;  the 
South  American  Caviomorpha;  and,  as  al- 
ready indicated,  the  Dipodoidea.  The  lines 
of  descent  of  most  of  these  groups  are 
either  not  clear  or  are  unknown.  The  South 
American  forms  are  a  natural  unit,  the 
Suborder  Caviomorpha  of  Wood  and  Pat- 
terson (1959,  p.  289)  or  the  Infraorder 
Nototrogomorpha  of  Schaub  (1958,  p. 
720).  It  seems  certain  that  these  rodents 
have  evolved  in  isolation  in  South  America 
since  the  late  Eocene  or  early  Oligocene, 
when  at  least  some  members  of  the  group 
were  fully  hystricomorphous  and  all  were 
hystricognathous,  and  that  they  have  had 
no  connections  with  any  other  hystrico- 
morphous forms  during  that  period.  On 
the  basis  of  the  available  evidence,  the 
most  reasonable  explanation  for  them  is 
that  they  represent  derivatives  of  a  North 
American  Grade  One  stock,  that  managed 
to  reach  South  America  by  island  hopping 
during  the  late  Eocene,  either  via  Middle 
America  (Simpson,  1950,  p.  375;  Wood, 
1962,  p.  248;  Wood  and  Patterson,  1959, 
p.  401-406),  or  via  the  West  Indies  (Lan- 
dry, 1957,  p.  91,  who  believed  that  these 
were  hystricomorphs  from  the  Old  World; 
Wood,  1949,  p.  47).  The  African  Thryon- 
omyoidea are  clearly  derived  from  the 
Oligocene  to  Miocene  Phiomyidae  (Lavo- 
cat,  1962,  p.  289),  whose  Oligocene  mem- 
bers (W^ood,  MS.  1)  show  no  signs  of  rela- 
tionship with  any  other  group  of  hystrico- 
morphous rodents,  and  can  only  (at  pres- 
ent) be  considered  as  an  independent  line 
derived  from  unknown  protrogomorphs. 
The  Hystricidae  (all  that  seems  to  be  left 
of  the  old  Hystricomorpha)  seem  to  have 
had  a  south  Asiatic  origin  and  differentia- 
tion, whence  the}'  spread,  in  the  late  Mio- 


457 


124 


ALBERT  E.  WOOD 


cene  or  early  Pliocene,  to  Europe  and 
Africa.  The  Bathyergoidea  are,  unfortu- 
nately, very  poorly  known  as  fossils, 
though  they  occur  in  the  African  Miocene 
(Lavocat,  1962,  p.  290).  Certain  Mon- 
golian Oligocene  fossils  that  have  some- 
times been  referred  to  this  family  (Mat- 
thew and  Granger,  1923,  p.  2-5;  Landry, 
1957,  pp.  72-73)  have  generally  been 
agreed  probably  to  be  late  members  of 
the  Grade  One  Cylindrodontidae. 

The  other  hystricomorphous  groups  are 
all  sciurognathous.  The  Dipodoidea  (Dip- 
odidae,  Zapodidae)  are  extremely  close  to 
the  cricetids  in  tooth  pattern — so  close,  in 
fact,  that  many  Miocene  and  Pliocene 
zapodids  were  originally  referred  to  the 
Cricetidae  (Schaub,  1930,  pp.  616-617, 
627-629;  Wood,  1935b,  Schaubeumys; 
Hall,  1930,  Macrognathomys) .  The  skel- 
etal and  myological  differences  between 
the  Muroidea  and  Dipodoidea  also  seem 
to  be  relatively  minor,  and  the  Dipodoidea 
almost  certainly  belong  to  the  same  clade 
as  do  the  Muroidea  and  Geomyoidea. 
which  may  be  called  the  suborder  Myo- 
morpha. 

The  Theridomyoidea  are  an  Eocene- 
Oligocene  group,  not  known  outside  of 
Europe.  The  earliest  members  of  the  super- 
family  are  close  to  the  Paramyidae  in 
cheek-tooth  structure  (Wood,  1962,  p. 
170)  and  in  enamel  histology  (Korven- 
kontio,  1934,  pp.  96-97),  but  are  already 
fully  hystricomorphous.  It  was  long  cus- 
tomary to  consider  them  ancestral  to  the 
Caviomorpha,  with  the  descendants,  among 
other  things,  becoming  hystricognathous. 
This  interpretation  is  easily  read  into 
Schaub's  classification,  although  he  spe- 
cifically states  that  current  knowledge  is 
not  adequate  to  demonstrate  such  a  rela- 
tionship (1958,  p.  693).  But  the  closest 
resemblances  to  the  theridomyoid  tooth 
pattern  are  not  found  in  the  earliest  cavio- 
morphs  as  should  be  the  case  if  they  were 
genetically  related  (Wood  and  Patterson, 
1959,  pp.  400-401).  Current  work  makes 
it  equally  improbable  that  there  is  a 
theridomyoid-thryonomyoid       relationship 


(Wood,  MS.  1).  The  earliest  known  Anom- 
aluridae  are  from  the  Miocene  of  Africa. 
There  is  no  good  evidence  indicating  rela- 
tionship between  them  and  any  other  group 
of  rodents.  It  is  conceivable  that  they  are 
related  to  the  Theridomyoidea,  but  there 
is  no  real  evidence  for  such  a  relationship. 
The  Ctenodactylidae,  now  exclusively  Af- 
rican, have  been  shown  by  Bohlin  (1946, 
pp.  75-146)  to  be  abundant  in  the  Oligo- 
cene of  central  Asia,  and  are  known  from 
Africa  only  since  the  late  Miocene  (Lavo- 
cat, 1962,  p.  289).  Work  in  progress 
(Dawson,  1964)  rather  strongly  suggests 
an  independent  derivation  of  this  family 
within  central  Asia  from  members  of  Grade 
One,  though  the  jaw  muscle  transitions 
have  not  been  worked  out. 

Finally,  the  Pedetidae  are  in  many  ways 
the  most  isolated  of  all  rodents.  They 
have  lived  in  Africa  since  the  Miocene 
(Stromer,  1926,  pp.  128-134;  Maclnnes, 
1957),  and  have  a  tooth  pattern  which  is 
only  very  slightly  reminiscent  of  that  of 
any  other  rodents.  They  probably  (with 
no  evidence)  represent  an  independent 
derivation  from  members  of  Grade  One 
(Wood,  MS.  2). 

Schaub  (various  sources,  especially 
1958)  completely  abandoned  the  use  of 
the  zygomasseteric  structure  or  that  of  the 
angle,  in  the  subordinal  classification  of 
rodents,  and  relied  only  on  the  cheek- 
tooth pattern.  He  argued  extensively 
(1958,  p.  684,  691-694)  that  either  the 
five-crested  pattern  ("plan  Theridomys") 
originated  only  once,  in  the  Theridomyo- 
idea, and  that  all  other  five-crested  forms 
are  descended  from  them,  or  that  his  sub- 
order Pentalophodonta,  including  these 
forms,  is  a  natural  group  (clade)  in  that 
it  contains  those  forms,  and  only  those 
forms,  that  have  achieved  a  five-crested 
pattern  as  a  result  of  parallelism.  As  he 
stated  (op.  cit.,  p.  693),  our  current  knowl- 
edge of  the  detailed  phylogeny  of  the  ro- 
dents is  still  inadequate  to  permit  us  to 
make  positive  statements  of  the  exact  an- 
cestry of  most  of  the  families  of  what  are 
here  included  in  Grade  Two.    Schaub  fur- 


458 


RODENT  GRADES 


125 


ther  stated:  "II  me  parait  aussi  evident  que 
I'idee  de  ce  plan  fondamental  qui  nous 
permet  de  reveler  sinon  tous,  mais  presque 
tous  les  parallelismes,  peut  servir  comme 
base  utilisable  de  la  classification,  tandis 
qu'on  ne  peut  pas  placer  la  nieme  confiance 
dans  celles  qui  s'appuie  sur  les  structures 
zygo-masseteriques  et  la  configuration  de 
Tangle  niandibulaire"  {op.  cit.,  p.  693). 

The  current  conclusion  of  most  students 
of  fossil  rodents  is  that  there  is  no  simple 
key  to  separating  clades  from  grades  within 
this  complex  order,  and  that  no  one  set 
of  criteria  (tooth  patterns,  zygomasseteric 
structure,  type  of  angle,  fusion  of  ear 
ossicles,  incisor  histology,  etc.)  may  be  re- 
lied upon.  Parallelisms  and  convergences 
are  so  abundant  that  only  an  analysis  of 
all  possible  criteria  can  give  reliable  evi- 
dences of  cladal  unity  (Lavocat,  1962,  p. 
288). 

From  the  analysis  of  the  features  that 
are  used  to  separate  members  of  Grade 
Two  from  those  of  Grade  One  (jaw  mus- 
culature; angle  of  the  jaw;  incisor  posi- 
tion; incisor  histology;  cheek-tooth  for- 
mula and  pattern),  it  seems  quite  clear 
that  these  features  evolved  independently 
of  each  other.  Hystricomorphous  forms 
can  be  either  hystricognathous  or  sciur- 
ognathous;  any  clade  of  Grade  Two  can 
include  forms  with  high-crowned,  as  well 
as  low-crowned,  cheek  teeth;  and  the 
changes  in  incisor  histology  seem  to  have 
taken  place  independently  of  all  the  others. 
This  situation  is  not  surprising  and  should 
not  cause  insurmountable  difficulties  in 
classification.  It  merely  emphasizes  that 
the  grades  must  not  be  interpreted  as 
clades,  and  that  a  key,  based  on  grade 
characters,  may  be  useful  but  is  still  only 
a  key. 

Grade  Three — Hypsodonty 
AND  Pattern  Modification 

The  third  grade  in  rodent  evolution  is 
not  as  clear-cut  as  are  the  first  two.  It 
is  represented  by  those  members  of  Grades 
One  or  Two  that  have  developed  extremely 
hypsodont    or    ever-growing    cheek    teeth. 


These  have  developed  independently  many 
times,  in  almost  all  clades  of  rodents,  as 
adaptations  to  grazing  or  burrowing  modes 
of  living.  Among  protrogomorphs,  the  bur- 
rowing cylindrodonts,  the  perhaps  steppe- 
living  protoptychids,  the  aplodontids  and 
the  mylagaulids  all  become  very  hypso- 
dont. There  is  a  definite  trend  toward 
hypsodonty  in  burrowing  squirrels  {Cyno- 
mys)  and  in  some  of  the  Old  World  ground 
squirrels.  The  burrowing  geomyids  and 
the  desert-living  saltatorial  heteromyids 
have  ever-growing  cheek  teeth.  Extremely 
high  crowns  also  characterize  most  of  the 
Caviomorpha  except  for  the  New  World 
porcupines  (Erethizontidae) ;  the  Thryono- 
myoidea,  the  Bathyergidae,  Ctenodactyli- 
dac,  and  Pedetidae  in  Africa;  the  Spalaci- 
dae  and  Rhizomyidae;  the  Castoridae;  and 
the  iNIicrotinae  among  the  Cricetidae. 

Perhaps  the  suppression  of  the  premolars 
and  retention  of  the  deciduous  teeth,  dis- 
cussed above,  are  also  features  of  this 
grade.  On  theoretical  grounds,  it  would 
seem  that  a  good  explanation  might  be 
that  the  wear  of  the  cheek  teeth  was  so 
rapid  that  selection  for  increase  of  height 
of  dP;|  was  very  strong,  resulting  in  teeth 
that  would  last,  proportionately,  as  long 
as  in  low-crowned  ancestral  forms.  A 
long-growing  tooth  of  this  sort  would  be 
capable  of  increasing  its  horizontal  dimen- 
sions, thus  eliminating  the  primary  adap- 
tive reason  for  the  replacement  of  decidu- 
ous teeth  by  permanent  ones — the  fact 
that  the  baby  jaws  were  not  big  enough 
for  adult-sized  teeth.  However,  in  the 
only  case  where  the  details  of  the  suppres- 
sion of  V\  by  retained  dP;^  are  known 
(Phiomyidae,  Wood,  ms.  1),  this  change 
is  taking  place  in  animals  some  of  which 
are  still  low-crowned  while  others  are,  at 
most,  mesodont. 

Two  types  of  ever-growing  teeth  have 
developed  among  rodents.  Usually,  there 
has  been  growth  of  the  pattern-bearing 
portion  of  the  crown,  so  that  the  pattern  is 
preserved  with  wear — at  least  in  consider- 
able part.  This  has  resulted  in  cheek  teeth 
that  lose  the  details  of  cusp  arrangement 


459 


126 


ALBERT  E.  WOOD 


early  in  life,  but  in  which  a  characteristic 
pattern  is  quickly  achieved,  and  retained 
for  the  rest  of  the  animal's  lifetime.  Such 
patterns  are  found  in  most  caviomorphs, 
the  Thryonomyoidea,  the  Theridomyidae, 
Bathyergidae,  Ctenodactylidae,  Pedetidae, 
Rhizomyidae,  Castoridae,  Spalacidae,  and 
Microtinae. 

In  some  rodents,  however,  there  is  little 
or  no  growth  of  the  pattern-bearing  portion 
of  the  crown,  but  rather  a  strong  unilateral 
hypsodonty  of  the  basal  part  of  the  crown. 
This  arrangement  usually  results  in  the  re- 
duction of  the  enamel  to  one  or  a  few  trans- 
\  erse  plates  on  each  tooth,  alternating  with 
dentine  (or  occasionally  cement)  prisms. 
Such  pattern  developments  are  most  char- 
acteristically developed  in  the  Geomyidae 
(Merriam,  1895;  Wood,  1936)  and  Heter- 
omyidae  (Wood,  1935a).  Similar  develop- 
ments are  present  in  Mongolian  Oligocene 
cylindrodonts  (Schaub,  1958,  fig.  156),  in 
several  cases  among  caviomorphs  (Wood 
and  Patterson,  1959,  p.  333  et  seq.\  figs. 
9A,  14C,  16B,  23A),  and  in  advanced  the- 
ridomyids  (Schaub,  1958,  figs.  45,  49,  51, 
and  55). 

The  tendency  to  elongate  the  cheek 
teeth,  discussed  above  under  Grade  Two, 
has  been  continued  in  a  considerable  num- 
ber of  forms  by  developments  at  the  front 
end  of  the  anterior  cheek  teeth  (the  antero- 
cone  and  anteroconid),  or  by  additions  at 
the  rear  of  the  last  tooth.  The  former  is 
especially  characteristic  of  the  Microtinae, 
the  latter  of  the  Hydrochoeridae. 

There  can  be  no  possible  doubt  that 
these  high-crowned  or  ever-growing  cheek 
teeth  have  been  acquired  independently  in 
the  various  clades  that  are  involved. 

Grade  Zero — The  Basic  Level 

The  evidence  suggests  that  the  Paleocene 
rodent  differentiation  was  based  on  a  dis- 
tinctly more  primitive  level  of  gnawing 
ability  than  that  seen  in  later  forms.  This 
radiation,  while  essentially  hypothetical, 
can  be  fairly  well  characterized,  and  is 
here  called  Grade  Zero. 

Among  middle  Eocene  and  later  rodents. 


the  incisors  universally  have  an  enamel 
cap  that  covers  the  entire  front  face,  and 
that  curves  around  onto  the  buccal  and 
lingual  sides  of  the  tooth  for  a  short  dis- 
tance, serving  to  lock  the  enamel  firmly 
onto  the  dentine.  Among  some  of  the  ear- 
liest rodents  of  the  Family  Paramyidae, 
however,  the  locked-on  pattern  of  enamel 
had  not  been  achieved  and  the  enamel 
merely  forms  a  strip  extending  across  most 
(but  not  all)  of  the  width  of  the  front 
edge  of  the  tooth.  As  a  result,  there  would 
have  been  danger  of  chipping  or  breaking 
off  pieces  of  the  enamel  strip.  This  pat- 
tern shows  up  well  in  the  late  Paleocene 
Paramys  atavus  (Wood,  1962,  fig.  21  B, 
C),  and  is  also  suggested  in  many  individ- 
ual specimens  of  several  early  Eocene 
paramyids,  which  seem  to  represent  the 
last  remnants  of  this  Paleocene  radiation. 
The  early  development  of  the  Leptotoniiis 
incisor  pattern,  with  the  enamel  extending 
over  a  very  large  part  of  the  tooth,  may 
also  be  derived  from  such  a  basic  condi- 
tion. 

While  there  is  no  evidence  one  way  or 
the  other,  it  would  seem  entirely  possible 
that  the  rodents  of  Grade  Zero  had  a  com- 
plete enamel  cap  on  the  unworn  incisors, 
as  did  the  multituberculates,  and  had 
merely  achieved  extreme  unilateral  hypso- 
donty. \\.  some  unknown  time  during  the 
Paleocene,  the  rodents  achieved  a  level 
where  the  incisors,  including  the  enamel 
strip,  became  ever  growing.  Since  the  few 
known  late  Paleocene  rodent  incisors  are 
all  fragments,  it  cannot  be  determined 
when  this  condition  was  reached,  though 
these  incisor  fragments  seem  to  belong  to 
ever-growing  teeth  similar  (in  this  respect) 
to  those  of  Grade  One.  This  suggests  that 
this  type  of  tooth  began  to  be  acquired 
not  later  than  middle  Paleocene. 

In  the  early  rodents  or  their  immediate 
precursors  there  was  a  reduction  from  the 
primitive  placental  formula  of  I:';  C]  P|  Mi; 
to  that  characteristic  of  the  early  Eocene 
Paramyidae,  l\  C*/,  Pj  Mi;.  This  almost  cer- 
tainly had  taken  place  well  before  the  end 
of  the  Paleocene,  and  presumably  had  bc- 


460 


RODENT  GRADES 


127 


gun  before  the  enlargement  of  the  incisors 
was  completed. 

The  difference  between  the  jaw  mus- 
culature of  Grade  One  (Fig.  1)  and  that 
of  primitive  mammals  was  presumably  not 
ver\^  great,  if  Edgeworth's  figures  (1935, 
fig.  692a,  b,  p.  459)  of  the  musculature  of 
Dasyurus  are  any  criterion.  Here  the  Mas- 
setcr  superjicialis  has  the  same  anteropos- 
terior alignment  as  in  Ischyrotomus,  and 
the  Massctcr  lateralis  and  Massetcr  mcdi- 
alis  (Masseter  profundus  and  Zygomatic  o- 
mandibularis  of  Edgeworth)  have  an  al- 
most vertical  alignment.  Thus,  the  Dasyu- 
rus pattern  of  jaw  musculature  seems  pre- 
adaptive  for  the  beginnings  of  gnawing  ro- 
dents, and  therefore  probably  is  essentially 
what  was  found  in  Grade  Zero. 

The  skull  structure  of  Paleocene  rodents 
is  completely  unknown.  But  it  seems  prob- 
able that  the  development  of  free  antero- 
posterior movement  of  the  condyle  of  the 
lower  jaw  occurred  pari  passu  with  the  de- 
velopment of  extremely  hypsodont  to 
ever-growing  incisors  and  the  reduction  of 
the  dental  formula  discussed  above,  and 
that  the  structure  of  the  condyle  and 
glenoid  fossa,  of  the  incisors,  of  the  cheek 
teeth  and  of  the  jaw  muscles  evolved  as 
a  unit  complex. 

Discussion 

The  analysis  of  rodent  morphological 
evolution,  given  above,  involves  the  inter- 
pretation of  the  classical  suborders,  the 
Sciuromorpha,  Myomorpha,  and  Hystrico- 
morpha,  as  representing  alternative  expres- 
sions of  a  major  and  a  secondary  adaptive 
level  in  the  order,  here  called  Grade  Two 
and  Grade  Three.  In  all  cases,  they  seem 
clearly  not  to  be  clades.  The  Protrogo- 
morpha,  as  defined  by  Wood  (1959,  p. 
170)  are  a  closer  approach  to  being  both 
a  clade  and  a  grade.  This  suborder  does 
not  quite  coincide  with  a  grade  because 
some  members,  while  not  having  achieved 
any  of  the  specializations  of  Grade  Two, 
have  reached  a  level  of  dental  complexity 
that  is  here  considered  indicative  of  Grade 
Three.    Whether   the   Protrogomorpha,  as 


here  delimited,  can  be  considered  to  rep- 
resent a  clade,  is  perhaps  arguable.  Cer- 
tainly the  Ischyromyoidea  are  a  clade. 
Certainly  the  Aplodontoidea  are  derived 
from  them,  but  most  authors  consider  that 
the  same  is  true  of  all  the  other  rodents  as 
well.  However,  the  Protrogomorpha,  as 
here  defined,  are  related  forms  that  have 
structural  features  in  common,  permitting 
the  group  to  be  satisfactorily  defined. 

Black  has  recently  (1963,  pp.  126-128) 
argued  that  the  Sciuridae,  because  of  their 
primitive  dentition,  should  be  returned  to 
the  Protrogomorpha,  where  Wood  once  in- 
cluded them  (1955a).  The  suborder  could 
then  be  defined  as  members  of  Grade  One 
plus  certain  groups  that  had  not  gone  very 
far  in  evolving  into  Grades  Two  or  Three. 
It  seems  better,  however,  for  the  present 
to  use  the  break  between  Grade  One  and 
Grade  Two  as  a  fundamental  division  in 
rodent  classification,  and  hence  to  elim- 
inate the  Sciuridae  from  the  Protrogo- 
morpha. A  major  reason  why  Black  con- 
siders that  the  squirrels  can  no  longer  be 
separated  from  the  members  of  Grade  One 
is  that  Miosciurus  and  Protosciurus,  from 
the  early  Miocene,  have  zygomasseteric 
structures  that  have  not  fully  achieved  the 
sciuromorphous  pattern.  However,  his  de- 
scription (1963,  pp.  136,  140)  and  figures 
[op.  cit.,  pis.  3,  6)  show  that  the  masseter 
had  already  begun  its  migration  in  these 
forms,  so  that,  technically,  they  belong  to 
what  is  here  called  Grade  Two.  Naturally, 
there  had  to  have  been  a  transition  from 
Grade  One  to  Grade  Two,  and  the  transi- 
tional forms  would  be  hard  to  place  with 
exactitude,  but  it  seems  best  to  consider 
all  the  known  Sciuridae  as  members  of 
Grade  Two. 

The  rest  of  the  cladal  classification  of 
rodents  must  still  remain  largely  as  in- 
dicated by  Simpson  (1959)  and  Wood 
(1959,  p.  172).  The  main  changes  that 
are  required  at  the  present  time  involve 
certain  African  rodents.  The  Phiomyidae 
are  clearly  not  Protrogomorpha,  but  are 
hystricomorphous  forms  ancestral  to  the 
Thryonomyoidea,     to    which    superfaniily 


461 


128 


ALBERT  E.  WOOD 


they  should  be  referred.  There  seems  to 
be  even  less  justification  than  formerly 
(Wood,  1955a)  for  placing  the  Hystricidae 
close  to  any  other  known  families. 

All  the  available  evidence  suggests  that 
the  level  of  Grade  Two  has  been  achieved 
many  times  independently.  Instead  of  the 
three  suborders  that  were  formerly  rec- 
ognized, it  seems  better  to  recognize  at 
least  eleven  clades  that  have  independently 
passed  from  Grade  One  to  Grade  Two. 
Which  of  these  should  be  considered  sub- 
orders and  which  merely  families  or  super- 
families  is,  for  the  moment,  largely  a  mat- 
ter of  convenience  (Simpson,  1959;  Wood, 
1959). 

A  cladal  classification  of  rodents,  based 
on  current  knowledge,  is  as  follows: 

Order  Rodentia 

Suborder  Protrogomorpha 
Superfamily  Ischyromyoidea 

Paramyidae,  Sciuravidae,   Cylindrodonti- 

dae,  Protoptychidae,  and  Ischyromyidae 
Superfamily  Aplodontoidea 

Mylagaulidae  and  .Aplodontidae 
Suborder  Caviomorpha 
Superfamily  Octodontoidea 

Octodontidae,  Echimyidae,  Ctenomyidae, 

Abrocomidae,  and  Capromyidae 
Superfamily  Chinchilloidea 

Chinchillidae,    Dasyproctidae     (incl.    Ce- 

phalomyidae),  Cuniculidae,  Heptaxodon- 

tidae,  and  Dinomyidae 
Superfamily   Cavioidea 

Eocardiidae,  Caviidae,  and  Hydrochoeri- 

dae 
Superfamily  Erethizontoidea 

Erethizontidae 
Suborder  Myomorpha 
Superfamily  Muroidea 

Cricetidae  (incl.  Melissiodontidae  Schaub) 

and    Muridae    (incl.    Gerbillidae    Stehlin 

and  Schaub) 
Superfamily  Geomyoidea 

Geomyidae,   Heteromyidae,   and   Eomyi- 

dae 
Superfamily  Dipodoidea 

Dipodidae  and  Zapodidae 
Superfamily  Spalacoidea 

Spalacidae  and  Rhizomyidae 
Superfamily  Gliroidea 

Gliridae  and  Seleveniidae 
Clades  not  in  suborders: 

Family  Sciuridae   (incl.  Eupetauridae  Schaub 

and  lomyidae  Schaub) 
Superfamily  Castoroidea 


Castoridae  and  Eutypomyidae 
Superfamily  Theridomyoidea 

Pscudosciuridae  and  Theridomyidae 
Family   Ctenodactylidae    (incl.   Tataromyidae 

BohHn) 
Family  Anomaluridae 
Family  Pedetidae 
Family  Hystricidae 
Superfamily  Thryonomyoidea 

Phiomyidae  (incl.  Diamantomyidae  Schaub), 

Thryonomyidae,  and  Petromuridae 
Family  Bathyergidae 

The  Family  Pellegriniidae  of  Schaub  is 
based  on  a  single  species  of  completely  un- 
known affinities,  which  should  not  be  con- 
sidered a  family  until  more  is  known  about 
it. 

Summary 

Rodent  evolution  can  be  envisioned  as 
involving  three  relatively  clear-cut  evolu- 
tionary levels,  here  called  Grades  One, 
Two,  and  Three.  The  first  involves  well- 
developed  gnawing  animals,  with  a  primi- 
tive mammalian  jaw  musculature.  Grade 
Two  includes  those  animals  that  have  mod- 
ified the  jaw  musculature  in  one  of  sev- 
eral ways  that  formerly  were  used  as  the 
basis  for  rodent  subordinal  classification. 
There  were  also  changes  in  the  dentition, 
especially  in  the  development  of  cheek 
teeth  with  five  transverse  crests,  rather 
than  ones  with  no  more  than  four  crests  as 
in  Grade  One.  Changes  occurred  in  nu- 
merous other  parts  of  the  skeleton  and 
dentition,  although  these  were  probably 
not  correlated  with  each  other.  Grade 
Three  includes  those  rodents  with  very 
high-crowned  or  even  ever-growing  cheek 
teeth,  in  which  there  is  sometimes  the  same 
type  of  limitation  of  the  enamel  that  oc- 
curred during  the  Paleocene  on  the  in- 
cisors. Grade  Three  also  includes  forms 
in  which  there  has  been  a  marked  second- 
ary increase  in  the  length  of  the  cheek 
teeth.  A  hypothetical  Grade  Zero  is  imag- 
ined for  the  rodents  of  the  second  half  of 
the  Paleocene. 

Only  Grade  One  comes  close  to  approxi- 
mating a  clade.  The  Protrogomorpha,  as 
here  defined,  include  the  members  of 
Grade    One    and    some    forms    that    have 


462 


RODENT  GRADES 


129 


reached  Grade  Three  without  going  through 
Grade  Two.  The  cladal  classification  of 
the  rodents  still  requires  the  recognition 
of  numerous  independent  lines,  showing  no 
evidence  of  interrelationship  later  than  in 
members  of  Grade  One.  Only  two  or  pos- 
sibly three  clades  can  be  recognized  that 
require  units  larger  than  the  superfamily — 
the  Protrogomorpha.  the  Caviomorpha,  and 
perhaps  the  Myomorpha.  The  other  ro- 
dents fall  into  nine  familial  or  superfamilial 
clades. 

Acknowledgments 

A  discussion  of  the  similarities  and  dif- 
ferences between  rodent  and  teleost  evolu- 
tion prompted  Schaeffer  to  make  the  oral 
suggestion  that  an  analysis  of  evolutionary 
grades  and  clades  among  rodents  would  be 
very  useful  to  students  of  the  evolution  of 
other  groups.  This  has  led  to  the  prepara- 
tion of  the  present  review.  This  study  was 
assisted  by  grants  from  the  National  Sci- 
ence Foundation  and  from  the  Marsh  Fund 
of  the  National  Academy  of  Sciences. 

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464 


Distribution  Patterns  and  Phylogeny 
of  Some  Western  Ground  Squirrels 


STEPHEN  D.  DURRANT  and  RICHARD  M.  HANSEN 


IT  IS  well  known  that  many  kinds  of 
mammals  attain  their  distributional 
limits  in  the  intermontane  West.  In  Utah 
in  particular  many  species  reach  their 
limits,  and  along  the  margins  of  the 
ranges,  many  small  populations  have  de- 
veloped under  semi-isolation  into  recog- 
nizable subspecies  in  relatively  short  peri- 
ods of  time.  We  have  been  making  a 
detailed  study  of  ground  squirrels  of  the 
subgenus  Citellus  (Oken)  for  the  past 
several  years.  The  study  of  taxonomy  and 
speciation  has  to  date  been  largely  re- 
stricted to  data  concerning  the  morpho- 
logical features  of  the  animals.  While  plot- 
ting the  ranges  of  these  species,  and 
studying  competition  between  different 
species  at  the  interphases  of  their  ranges, 
we  have  made  many  observations  which 
lead  us  to  believe  that  a  significant  supple- 
ment to  the  morphological  data  may  be 
obtained  by  field  studies  of  the  distribu- 
tion and  ecology  of  related  species  under 
intense  competition.  Within  the  given 
genus,  what  are  the  relationships  as  indi- 
cated between  degrees  of  allopatry  and 
sympatry?  What  does  competition  indi- 
cate about  the  rate  of  differentiation  and 
selection? 

The  ground  squirrels  of  North  America 
belong  to  the  genus  Citellus  and  are  di- 
vided into  eight  subgenera.  The  group 
here  reported  upon  is  that  of  the  short- 
tailed  ground  squirrels  of  the  subgenus 
Citellus  (Oken).  We  are  not  concerned  at 
present  with  all  the  species  of  this  sub- 
genus, but  only  with  the  following:  C. 
armatus,  C.  beldingi,  C.  richardsoni,  C.  co- 
lumbianus,  and  C.  townsendii  and  its 
allies.  Generally  speaking  C.  armatus  is  a 
northern  species  that  attains  its  southern 
limits  in  Utah;  C.  beldingi  is  a  northwest- 


ern species  that  attains  its  southeastern 
limits  in  Utah,  in  the  extreme  northwest- 
ern part  of  the  state;  C.  richardsoni  is  a 
northern  and  eastern  species  that  has  its 
southern  limits  in  Colorado  and  Utah  and 
its  western  limits  in  Nevada;  C.  columbi- 
anus  is  also  a  northern  species  that  ex- 
tends as  far  south  as  southcentral  Idaho; 
and  C.  townsendii  and  its  allies  are  west- 
ern and  northern  animals  that  extend  as 
far  east  as  central  Utah  (Fig.  1). 

Students  of  these  shorttailed  ground 
squirrels  are  familiar  with  the  fact  that 
within  their  ranges  they  occupy  several 
types  of  habitats  ranging  from  dry  hill- 
sides to  lush,  moist  meadows.  Members 
of  all  of  the  aforementioned  species  appar- 
ently prefer  moist,  lush  meadows  when 
they  are  available.  Within  the  ranges  of 
the  several  species  of  this  subgenus,  mem- 
bers of  each  species  always  occupy  a  wider 
variety  of  habitats  if  that  species  is  the 
only  representative  of  the  subgenus 
present. 

Intraspecific  competition  appears  to  be 
of  lesser  degree  than  does  interspecific 
competition.  We  have  noted  that  where 
the  ranges  of  C.  richardsoni  and  C.  arma- 
tus come  into  contact  in  Rich  and  Daggett 
counties,  Utah,  each  species  occupies  a 
narrower  variety  of  habitats  than  it  would 
if  it  occurred  there  alone.  At  these  local- 
ities, where  the  ranges  of  the  two  come 
into  contact,  colonies  of  C.  richardsoni  oc- 
cupy the  dry,  open  areas  between  stands 
of  sagebrush  and  greasewood,  while  those 
of  C.  armatus  occupy  the  grassy  meadows. 
It  is  noteworthy  that  at  this  zone  of  con- 
tact between  the  ranges  of  these  two  spe- 
cies, the  competition  is  extreme;  the  bur- 
rows and  feeding  areas  of  the  animals  of 
one  species  being  in  some  instances  but  a 


465 


DISTRIBUTION  AND  PHYLOGENY   IN  WESTERN  GROUND  SQUIRRELS 


83 


Fig.  1.    Distribution  of  the  species  of  the  subgenus  Citellus  (Oken)  in  the  intermontane 
region  of  western  U.  S. 


466 


84 


SYSTEMATIC  ZOOLOGY 


few  feet  from  those  of  the  other.  Back 
from  the  zone  of  contact  between  the 
ranges  of  these  two  species,  we  noted  that 
where  animals  of  only  one  of  the  two 
species  occurred,  they  lived  in  both  the 
wet  and  dry  situations,  indicating  that 
they  could  live  successfully  in  either  wet 
meadows  or  dry,  barren  ground  as  long  as 
members  of  the  competing  species  were 
not  present. 

In  Colorado,  Warren  (1942,  p.  124)  re- 
ported colonies  of  C.  richardsoni  as  occur- 
ring in  high  mountains,  and  that  in  some 
instances  they  had  crossed  over  passes  at 
11,000  feet  to  become  established  in  the 
heads  of  drainages  on  the  other  side  of  the 
mountains.  Since  members  of  a  competi- 
tive species  do  not  occur  in  these  moun- 
tains in  Colorado,  colonies  of  C.  richard- 
soni were  able  to  establish  themselves 
there.  In  the  western  part  of  the  Bridger 
Basin  the  ranges  of  C.  armatus  and  C. 
richardsoni  overlap.  Where  both  are 
found  together  here,  they  are  ecologically 
displaced  as  previously  noted.  Each  lives, 
however,  in  wet,  moist  areas  and  also  in 
dry,  semiarid  areas  in  the  Bridger  Basin, 
except  where  colonies  of  the  two  co-exist. 
In  Idaho,  Davis  (1939,  pp.  171-180)  re- 
ported the  same  relative  ecological  distri- 
bution for  colonies  of  C.  armatus  and  C. 
richardsoni  as  we  have  noted,  and  com- 
mented that  they  both  occupy  the  same 
types  of  habitats;  but  he  did  not  indicate 
whether  or  not  the  animals  of  the  two  spe- 
cies are  ecologically  displaced  when  they 
occur  together.  We  suspect  that  they  are. 
Apparently  ground  squirrels  belonging  to 
C.  richardsoni  are  better  adapted  to  dry 
soils  than  are  those  of  C.  armatus,  but 
since  both  are  known  to  survive  in  the 
same  range  of  ecological  habitats,  it  is 
competition  that  limits  their  ranges  where 
they  meet.  In  the  Grouse  Creek  area  of 
northwestern  Utah,  where  colonies  of  C. 
armatus  and  C.  beldingi  come  into  con- 
tact with  each  other,  we  noted  that  the 
animals  of  C.  armatus  occupied  the  dry 
localities,  while  those  belonging  to  C.  bel- 
dingi occupied  the  wet  meadows.  In  Idaho, 


Davis  (1939,  pp.  169-172)  reported  that 
animals  of  these  two  species  occupy  the 
same  habitats,  and  that  the  ranges  of  the 
two  species  overlapped  there,  but  he  did 
not  note  whether  or  not  they  were  ecologi- 
cally displaced,  although  he  found  them  in 
separate  colonies  in  the  same  field.  He 
did  state  that  animals  of  both  species  pre- 
fer moist  meadows,  although  both  will 
live  in  dry  areas,  and  this  is  in  agreement 
with  our  findings  in  Utah.  Apparently 
animals  of  C.  armatus  are  better  adapted 
to  dry  situations  than  are  those  of  C. 
beldingi. 

In  Utah,  we  have  not  found  colonies  of 
C.  townsendi  in  close  proximity  to  those 
of  C.  armatus  and  C.  beldingi,  but  we  have 
found  them  about  a  mile  apart.  Our  obser- 
vations indicate  that  in  these  localities, 
ground  squirrels  of  the  species  C.  town- 
sendii  lived  in  extremely  dry  habitats, 
drier  than  any  found  for  the  other  two 
aforementioned  species.  In  Idaho,  how- 
ever, north  of  the  Snake  River  in  Jerome 
County,  we  did  find  animals  of  C.  townsen- 
dii  living  on  the  dry  soils  while  the  adja- 
cent meadow  was  occupied  by  animals  of 
C.  beldingi.  We  noted  animals  of  C.  bel- 
dingi also  on  dry  soils,  but  only  in  the  ab- 
sence of  C.  townsendii.  It  is  evident  that 
animals  belonging  to  the  species  C.  town- 
sendii are  remarkably  well  adapted  to  life 
in  extremely  dry  areas. 

Hall  (1946,  p.  290)  reported  that  wher- 
ever C.  beldingi  and  C.  townsendii  were 
found  together  in  Nevada,  the  Belding 
ground  squirrel  occupied  the  meadow- 
land,  and  colonies  of  C.  townsendii  lived 
on  the  sagebrush-covered  benches.  He 
further  commented  on  the  fact  that  both 
of  these  kinds  of  ground  squirrels  prefer 
moist  situations,  but  he  did  not  comment 
on  what  happens  where  the  ranges  of  C. 
richardsoni  and  C.  townsendii  overlap. 

To  date,  the  Belding  ground  squirrel 
has  not  been  taken  north  of  the  Snake 
River  in  Idaho.  We  found  both  the  Co- 
lumbian and  Belding  ground  squirrels 
north  of  the  river.  In  this  region,  they 
both  occurred  in  the  moist  meadows.  We 


467 


DISTRIBUTION  AND  PHYLOGENY  IN  WESTERN  GROUND  SQUIRRELS 


85 


did  not  have  an  opportunity  to  observe 
them  in  the  same  locality,  but  we  are  of 
the  opinion  that  where  their  ranges  over- 
lap, the  Belding  ground  squirrel  will  be 
found  to  occupy  the  moist  habitats,  while 
the  Columbian  will  be  found  in  the  drier 
situations. 

Phylogenetic  Interpretation 

Since  all  members  of  this  subgenus  are 
of  generally  northern  occurrence,  attain- 
ing their  southern  limits  in  the  western 
states,  and  since  all  prefer  moist  habitats 
where  available,  it  would  seem  that  the 
adaptational  feature  essential  to  increas- 
ing the  range  to  the  southward  would  be 
the  ability  to  take  over  more  xerophytic 
situations.  From  our  observations  on  com- 
petition between  the  several  species,  we 
align  them  with  reference  to  this  adapta- 
tion in  the  following  order:  first,  C.  town- 
sendii  is  able  to  outcompete  any  other  for 
arid  places;  next  is  C.  richardsoni,  followed 
by  C.  armatus,  then  C.  columbianus,  and 
finally  by  C.  beldingi  which  is  the  least 
adapted  to  dry  conditions.  These  observa- 
tions are  somewhat  borne  out  by  studies 
on  the  areas  of  occurrence.  It  is  axiomatic 
in  the  study  of  mammals  that  the  subspe- 
cies of  a  species  are  all  allopatric.  There- 
fore, within  limits,  it  would  appear  within 
a  genus  or  subgenus,  that  the  greater  the 
amount  of  allopatry  between  the  full  spe- 
cies the  younger  the  genus.  Moreover,  the 
greater  the  amount  of  sympatry  between 
species  of  the  genus,  the  greater  the  di- 
vergence between  the  species,  hence  the 
older  the  genus.  The  subgenus  in  question 
has  some  sympatry,  but  in  general  is 
markedly  polymorphic  and  allopatric. 
Some  species  are  totally  allopatric  with 
reference  to  other  species;  some  have  only 
a  minor  degree  of  overlap  of  ranges  and 
in  only  one  case  are  the  ranges  markedly 
sympatric.  The  ranges  of  C.  townsendii 
and  C.  beldingi  are  sympatric  to  a  large 
extent,  and  the  animals  are  markedly  dis- 
tinct in  both  morphological  and  ecological 


characteristics.  The  ranges  of  C.  beldingi 
and  C.  armatus  are  practically  allopatric 
and  the  animals  are  quite  similar  in  both 
morphology  and  ecological  tolerances. 
With  the  exception  of  the  subspecies  C.  r. 
nevadensis,  the  ranges  of  the  species  C. 
beldingi  and  C.  richardsoni  are  totally  allo- 
patric. The  subspecies  C.  r.  nevadensis  is 
a  relict  and  is  on  the  way  out.  Its  range 
is  sympatric  with  both  C.  beldingi  and  C. 
townsendii.  The  former  outcompetes  it 
for  the  wet  situations  while  the  latter  does 
the  same  with  reference  to  the  dry  ecologi- 
cal situations.  In  comparing  the  ranges 
of  each  species  with  all  others,  it  is  appar- 
ent that  there  is  a  correlation  between  the 
degree  of  overlap  of  the  ranges,  the  mor- 
phological relationships  and  the  ecological 
tolerances  of  the  animals  of  the  species 
in  question. 

From  the  above  data  on  interspecific 
competition,  and  from  our  study  of  the 
degree  of  sympatry  and  allopatry  of  the 
ranges  of  these  species,  we  would  formu- 
late a  phylogeny  of  the  members  reported 
upon  in  this  subgenus  in  the  following 
manner:  C.  townsendii  is  the  most  diver- 
gent, next  C.  richardsoni,  then  C.  armatus, 
with  C.  columbianus  and  C.  beldingi  being 
more  conservative  and  closer  to  the  ances- 
tral type.  Furthermore,  these  conclusions 
are  in  keeping  with  the  known  history  of 
animals  of  this  region  with  reference  to 
the  happenings  of  Pleistocene  and  post- 
Pleistocene  time. 

REFERENCES 

Davis,  W.  B.  1939.  The  Recent  mammals  of 
Idaho.  Caxton  Printers,  Caldwell,  Idaho. 

Hall,  E.  R.  1946.  Mammals  of  Nevada.  Univ. 
of  California  Press,  Berkeley. 

Warren,  E.  R.  1942.  The  mammals  of  Colo- 
rado.  Univ.  of  Oklahoma  Press,  Norman. 


STEPHEN  D.  DURRANT  is  Professor  of 
Vertebrate  Zoology  at  the  University  of  Utah. 
RICHARD  M.  HANSEN  is  a  U.S.  Public  Health 
Service  Fellow  at  the  Microbiological  Insti- 
tute, University  of  Utah. 


468 


VARIABILITY   IN   CHARACTERS   UNDERGOING    RAPID    EVOLUTION, 
AN  ANALYSIS  OF  MICROTUS  MOLARS 

R.  D.  Guthrie 
University  of  Alaska,  College,  Alaska 

Accepted  October  31,  1964 

Information  amassed  by  animal  breeders  nation  of  genetic  variance  does  have  mean- 
has  aided  considerably  the  understanding  of  ing  at  its  intermediate  stages.  It  is  the  as- 
the  genetic  changes  that  accompany  pheno-  sumption  of  many  evolutionary  thinkers 
typic  population  changes  through  time.  In  that  as  the  population  responds  to  the  pres- 
spite  of  genetic  inferences  from  these  artifi-  sures  of  directional  selection  the  genetic 
cial  selection  experiments,  there  are  few  and  phenotypic  variation  immediately  de- 
studies  of  genetic  and  phenotypic  changes  creases,  discouraging  further  evolutionary 
in  characters  evolving  under  natural  con-  changes  proportionally.  The  findings  of 
ditions.  Because  of  the  scarcity  of  statisti-  this  study  lead  me  to  take  issue  with  this 
cally  adequate  series  of  fossils  and  the  in-  assumption. 

completeness  of  knowledge  of  phylogenetic  Empirical    documentation   supporting   a 

patterns,  the  contributions  of  paleontology  reduction  of  phenotypic  variation  in  evolv- 

to  the  understanding  of  evolutionary  dy-  ing  populations  has  been  discussed  by  Simp- 

namics  have  been  far  below  its  potential,  son  (1953)  and  Bader  (1955),  although,  in 

However,    as    phylogenies    become    better  their  material,  the  decreases  in  phenotypic 

known  and  series   are   emphasized   rather  variation  were  slight.    Since   evolutionary 

than  types,  it  is  increasingly  possible  to  change  in  both  cases  was  taking  place  at 

study   the   detailed    behavior    of    evolving  only  a  moderate  pace,  an  examination  of  a 

characters.    Findings  of  these  studies,  in  more  rapidly  evolving  group  would  theoreti- 

turn,  permit  a  more  critical  evaluation  of  cally  provide  greater  clarification  as  the  in- 

our  theoretical  models.  terrelationships  would  be  accentuated  by 

One  of  the  critical  areas  of  evolutionary  the  more  intense  selection  pressures  exerted 
research  is  the  behavior  of  the  intrapopula-  over  a  shorter  period  of  time.  This  study 
tional  variation  of  a  character  when  it  is  is  an  examination  of  such  a  rapidly  evolv- 
undergoing  change.  An  understanding  of  ing  group.  The  variation  of  a  suite  of 
the  changes  in  genetic  variation  as  the  pop-  evolving  characters  has  been  compared  to 
ulation  moves  from  one  mean  to  another  is  the  variation  of  their  more  stable  homo- 
central  to  any  investigation  involving  evo-  logues. 

lutionary  mechanics.   Lerner  (1955)  listed  One  of  the  best  examples  of  rapid  evolu- 

as    one    of    the    significant    landmarks    of  tion  documented  in  the  mammalian  record 

population   genetics   the   discovery   of   the  has  been  chosen  for  this  investigation.  The 

great  genetic  reserves  in   natural  popula-  setting  for  this  rapid  radiation  is  the  late 

tions,  yet  this  high  potential  genetic  vari-  Pliocene  and  Pleistocene,  a  time  of  major 

ation  is  usually  associated  with  relatively  ecological  upsets,  rapid  introduction  of  new 

low  phenotypic  variation.  According  to  our  habitats,  periodic  invasions  of  new  terri- 

present  concepts,  sustained  intensive  direc-  tory,  and  novel  associations  of  faunas.  The 

tional  selection  would  decrease  and  even-  microtine  rodents  changed  so  rapidly  dur- 

tually  exhaust  this  residual  store  of  genetic  ing  this  time  that  they  are  used  as  one 

variance.    In  reality  the  situation  is  never  of   the  better   markers   for   correlation   of 

brought   to   this   extreme   since   evolution,  the    Pleistocene   stages    (Hibbard,    1959). 

even  at  its  most  rapid  pace,  is  slow  com-  Microtines  are  well  represented  in  the  fossil 

pared  to  changes  produced  by  artificial  se-  record,  and  as  a  result  of  their  generally 

lection.  However,  the  problem  of  the  elimi-  high  population  densities,   where  present, 

Evolution  19:  214-233.     June,  1965  214 


469 


VARIABILITY  IN  MICROTUS  MOLARS 


215 


fossils  are  usually  abundant.  The  micro- 
tines  have  undergone  a  major  adaptive  shift 
from  the  seed-fruit  diet  of  the  typical  crice- 
tine  to  a  bark-grass  diet.  This  change  has 
been  accompanied  by  a  characteristic  in- 
crease in  the  complexity  of  the  dentition, 
which  is  the  most  durable  portion  of  a  mam- 
mal and  also  the  part  most  frequently  pre- 
served. The  microtines  have  developed  in 
this  short  period  of  time  a  tooth  complexity 
comparable  to  that  which  the  Equidae 
achieved  throughout  the  entire  Tertiary. 
Bader  (1955)  suggested  about  two  million 
years  as  the  average  duration  of  a  species 
of  oreodont.  This  length  of  time  would  be 
too  conservative  for  genera  of  microtines. 

Preliminary  studies  indicated  that  the 
teeth  and  the  areas  of  the  particular  teeth 
which  are  undergoing  phylogenetic  change 
(more  variable  interspecifically  and  inter- 
generically)  are  also  those  which  are  more 
variable  intraspecifically  and  intrapopula- 
tionally.  Two  abundant  species  of  Microtus 
that  represent  two  minor  grades  of  tooth 
complexity  were  selected,  the  extinct  M. 
paroperarius  from  the  Kansan  glaciation 
and  the  recent  species  M.  pennsylv aniens, 
first  known  from  the  Illinoian. 

It  should  be  emphasized  that,  unlike 
studies  of  fossil  material  which  compared 
the  variation  between  rapidly  and  slowly 
evolving  lines  for  a  variety  of  characters, 
this  study  was  a  comparison  of  characters 
within  populations.  The  variation  of  tooth 
characters  that  are  undergoing  rapid  evolu- 
tion was  compared  with  the  variation  of 
their  serial  homologues  which  are  main- 
taining a  fundamentally  stable  morphology. 
The  hypothesis  examined  was  that  highly 
variable  characters  are  not  ipso  facto  ves- 
tigial. Quite  the  contrary,  some  of  these 
characters  have  recently  been,  or  are  yet 
being,  subjected  to  directional  positive  se- 
lection. Stated  in  another  way,  characters 
undergoing  directional  selection  do  not  ex- 
hibit the  expected  phenotypic  trend  toward 
homogeneity;  rather,  they  retain  the  same 
magnitude  of  variation  or  even  increase 
that  magnitude.  A  correlate  of  this  state- 
ment is  that  those  characters  which  are 


more  variable  between  groups  at  a  lower 
taxonomic  level  are  also  more  variable 
within  these  groups. 

As  it  is  difficult  to  speak  of  selection  in- 
tensity in  wild  populations,  a  phylogenetic 
unidirectional  change  in  a  mean  will  be 
equated  in  the  ensuing  discussions  with  se- 
lection response.  This  implied  association 
does  not  necessarily  follow  since  migration, 
inbreeding,  and  distortion  of  the  gene  pool 
due  to  random  fluctuations  alone  may  also 
cause  a  movement  of  the  population  mean. 
In  the  case  of  the  microtine  tooth  varia- 
tions, these  exceptions  to  the  assumption 
are  probably  not  involved.  The  tooth  evo- 
lution follows  a  syndrome  of  related  adap- 
tive changes  of  which  increased  tooth  com- 
plexity is  but  one  facet.  According  to  our 
present  knowledge,  only  selection  can  be 
held  responsible  for  directional  change  of 
this  type  and  magnitude. 

Evolution  of  Microtine  Molars 

Most  of  the  radiations  involving  grazing 
mammals  began  in  the  Miocene  with  the 
formation  of  the  temperate  and  boreal 
grasslands.  For  some  unknown  reason  the 
microtine  radiation,  involving  a  dietary 
shift  from  the  fruiting  part  of  the  plant  to 
the  vegetative  part,  lagged  until  the  late 
Pliocene.  As  in  many  other  radiations  in- 
volving the  exploitation  of  a  coarser  diet, 
the  low-crowned  tuberculate  teeth  changed 
into  complex  high-crowned  prismatic  teeth 
to  compensate  for  the  increased  rate  of  at- 
trition. 

The  microtine  molar  crown  consists  of  a 
wide  enamel  loop  at  one  end  with  alter- 
nating left  and  right  triangles  following. 
These  triangle-like  extensions  are  termed 
salient  angles  and  the  troughs  between  are 
the  re-entrant  angles  (Fig.  1).  The  crown 
pattern  of  the  upper  molars  is  oriented 
posteriorly  (the  loop  on  the  anterior  part 
of  the  tooth)  while  the  crown  pattern  of 
the  lower  molars  is  just  the  reverse.  Except 
for  this  reversal  the  tooth  pattern  of  the 
uppers  and  lowers  is  fundamentally  the 
same  so  that  M^  has  approximately  the 
same  shape  as  M2  except  that  the  loop  of 


470 


216 


R.  D.  GUTHRIE 


UPPERS 


LOWERS 


Fig.  1.  A  pictorial  representation  of  the  42  mea- 
surements taken  on  the  upper  and  lower  teeth  in 
two  species  of  Microtus.  Width  measurements  are 
numbered  serially  from  the  loop.  Anterior  and 
posterior  lengths  of  each  tooth  are  designated  by 
(a)  and  (p)  respectively,  and  the  entire  length  of 
each  tooth  by  (L). 

the  former  is  anterior  and  that  of  the  latter 
posterior.  In  the  upper  molars  the  enamel 
border  of  the  salient  angles  is  convex  on  the 
anterior  edge  and  concave  on  the  posterior: 
in  the  lower  teeth  the  pattern  is  reversed. 
Moving  the  teeth  anterior-posteriorly  pro- 
duces a  self-sharpening  system  of  opposed 
shearing  blades. 

Microtine  molars  have  become  more  com- 
plex by  the  addition  of  salient  angles  and 
in  the  more  advanced  forms  the  teeth  are 
quite  elaborate.  Phylogenetically  the  up- 
pers add  on  to  the  posterior  margins  of  the 
teeth  and  the  lowers  to  the  anterior.  As  a 
consequence,  the  posterior  margin  of  M^ 
and  the  anterior  margin  of  Mj  are  the  most 
variable  between  taxa.  There  have  been 
numerous  changes  in  all  of  the  molar  crowns 
although  JVP,  M2,  and  M3  are  more  con- 


stant than  any  of  the  other  teeth.  M3  does 
vary  in  form  intergenerically ;  perhaps  this 
is  a  result  of  the  position  of  the  incisor  root 
as  it  arcs  past  M3.  In  some  genera  the  in- 
cisor passes  between  M^  and  the  two  an- 
terior molars  and  in  other  genera  it  does 
not.  The  addition  of  triangles  is  accom- 
plished in  M^  and  Mi,  as  illustrated  in 
Fig.  2,  by  an  increased  penetration  of  the 
re-entrant  angles  in  the  trefoil  or  the  pri- 
mordium  at  the  variable  end  of  the  tooth. 
In  the  other  molars  the  addition  of  tri- 
angles is  accomplished  by  a  lateral  pinching 
off,  phylogenetically  speaking,  of  a  bud 
from  the  last  triangle  (see  M-  in  Fig.  2). 
M^  and  Mi  maintain  a  labile  primordium 
at  the  changing  end,  whereas  this  analo- 
gous area  in  the  other  molars  abuts  against 
the  stable  loop  of  the  following  tooth  and 
cannot  maintain  such  a  variable  structure, 
but  has  to  resort  to  the  use  of  the  last 
salient  angle  if  new  angles  are  to  be  added. 

The  addition  of  salient  angles  has  taken 
place  throughout  the  late  Pliocene  and 
Pleistocene,  but  it  would  be  naive  to  con- 
sider the  whole  subfamily  as  being  con- 
stantly driven  unidirectionally  by  a  bom- 
bardment of  selection  pressures  toward  a 
new  adaptive  peak.  Some  groups  within  the 
subfamily  have  become  stabilized  inter- 
mediates between  the  two  adaptive  ex- 
tremes. There  is  almost  a  whole  generic 
continuum,  even  in  the  living  forms,  from 
the  simple  crushing  bunodont  dentition  to  a 
complex  continuously  growing  hypsodont 
type.  Within  the  various  lines  of  descent 
there  have  been  irregular  increases  in  the 
rate  of  acquiring  tooth  complexity.  Also 
there  has  been  a  varied  differential  between 
lines  in  the  attainment  of  complex  hypso- 
dont molars.  Microtine  evolution  is  com- 
parable to  the  evolution  of  horse  cheek 
teeth  through  the  Tertiary,  where  the  more 
progressive  grazers  were  often  flanked  by 
browsing  groups  with  dentition  of  an  an- 
cestral pattern. 

It  is  not  intended  to  be  implied  that  the 
teeth  are  the  only  or  even  the  major  char- 
acters undergoing  change.  Emphasis  has 
been  put  on  dentition  in  this  treatment  as 


471 


VARIABILITY  IN  MICROTUS  MOLARS 


217 


Ml 


h' 


M^ 


($ 


m  ^ 


A 


B 


Fig.  2.  A  semischematic  illustration  of  the  extent  of  tooth  crown  variations  found  in 
the  two  species  of  Microtns:  (A)  M.  paroperarius,  (B)  M.  pennsylvanicus.  The  relatively 
stable  areas  are  marked  with  parallel  lines,  and  the  variable  areas  are  cross-hatched  (see 
Fig.  1  for  orientation). 


it  is  one  of  the  few  characters  which  is  con- 
sistently preserved  in  the  fossil  record.  Al- 
though character  choice  in  the  fossil  micro- 
tines  is  limited  by  default,  it  would  have 
been  difficult  to  have  found  a  more  suitable 
index  of  adaptive  change. 

Methods,  Materials,  and 
Measurements 

Samples  of  multiple  series  were  used  in 
this  study  to  investigate  the  horizontal  (in- 
traspecific)    and    vertical     (phylogenetic) 


species  uniformity  of  the  differential  tooth 
variations.  The  main  comparison  is  of  in- 
dividual variation  within  each  series  and 
not  between  series.  The  material  is  treated 
as  four  samples.  The  first  sample  repre- 
sents the  extinct  M.  paroperarius,  which 
occurs  only  as  a  fossil.  Samples  two,  three, 
and  four  are  of  the  Recent  meadow  vole, 
M.  pennsylvanicus.  Sample  two  is  one 
series  with  the  sexes  combined  and  the  last 
two  samples  are  another  series  with  the 
sexes  treated  separately.  These  two  species 


472 


218 


R.  D.  GUTHRIE 


probably  represent  one  evolutionary  line; 
at  least  AI.  pennsyivanicus  had  to  pass 
through  the  morphological  stage  repre- 
sented by  M.  paropcrarius. 

The  series  of  M.  paropcrarius  was  ob- 
tained from  the  collections  of  the  University 
of  Kansas  Museum  of  Natural  History. 
This  species  was  first  described  by  Hibbard 
(1944)  and  was  considered  in  more  detail, 
including  a  qualitative  analysis  of  the  intra- 
populational  variation,  by  Paulson  (1961). 
The  sample  was  collected  by  Hibbard  from 
several  localities  in  Meade  County,  Kansas. 
These  localities  all  belong  to  the  Cudahy 
Fauna,  which  lies  just  below  the  Pearlette 
ash,  a  petrographically  distinct  volcanic  ash. 
The  Pearlette  ash  is  a  widespread  Pleisto- 
cene marker  of  the  non-glaciated  areas  in 
central  and  western  North  America  and 
serves  to  delineate  a  contemporaneous 
fauna  over  a  considerable  territory.  Hib- 
bard (1944)  considers  the  Cudahy  Fauna 
to  be  late  Kansan  in  age. 

It  was  necessary  to  use  teeth  from  several 
localities  in  order  that  a  statistically  ade- 
quate sample  could  be  acquired.  The  series 
of  M.  paropcrarius  was  taken  as  a  not-too- 
serious  deviation  from  an  approximated 
population  sample  since  the  localities  were 
all  within  one  county  and  stratigraphically 
contemporaneous. 

M.  paropcrarius  is  represented  by  single 
teeth,  although  a  few  remained  attached  to 
mandible  fragments.  The  majority  of  the 
teeth  came  from  K.  U.  localities  10  and  17, 
but  a  small  number  were  from  Locality 
No.  20.  The  individual  tooth  morphology 
was  so  characteristic  that  the  individual 
molars  could  be  easily  identified  as  to  up- 
per or  lower  first,  second,  or  third  molars 
and  separated  as  to  left  or  right.  The  sexes 
were  not  distinguishable.  The  measure- 
ments of  the  left  and  right  teeth  were  com- 
bined to  increase  the  sample  size.  There 
was  a  positive  correlation  between  the  fre- 
quency of  the  teeth  in  the  collection  and 
their  size.  M3  was  the  smallest  and  most 
fragile  tooth  and  Mi  was  the  largest.  There 
were  fewer  Ms's  than  any  other  tooth  in 
the  sample    (31)    and   the  Mi's  were   the 


most  numerous  (58).  This  numerical  dis- 
parity could  have  been  due  either  to  the 
fact  that  a  more  robust  structure  would 
better  survive  preservation  or  that,  as  fos- 
sils, a  larger  individual  fragment  would  be 
more  likely  to  be  detected  than  a  smaller 
one. 

The  second  sample,  of  the  Recent  M. 
pennsyivanicus,  was  obtained  from  the  Car- 
negie Museum  collections  through  the  Chi- 
cago Museum  of  Natural  History.  This 
sample  was  originally  collected  from  the 
Pymatuning  Swamp,  Crawford  County, 
Pennsylvania,  an  area  15  miles  long  by  three 
miles  wide.  Coin  ( 1943)  included  a  qualita- 
tive review  of  the  M'^  variations  of  this  sam- 
ple and  discussed  the  locality  in  more  detail. 
Fifty  individuals  were  used,  25  males  and 
25  females.  The  sexes  in  sample  two  were 
combined  as  in  the  first  sample  {M.  paro- 
pcrarius). The  teeth  in  the  second  sample, 
unlike  those  of  M.  paropcrarius,  were  all 
in  place  in  the  jaws. 

Samples  three  and  four  are,  respectively, 
males  and  females  of  M.  pennsyivanicus. 
There  were  40  males  and  42  females.  This 
series  was  borrowed  from  the  University 
of  Michigan  Museum  of  Zoology  and  was 
originally  collected  near  the  city  of  Lynd- 
hurst,  Ohio.  The  sexes  were  treated  sepa- 
rately to  eliminate  the  variable  of  sexual 
dimorphism  and  to  see  what  changes  this 
dimorphism  brought  about  in  the  patterns 
of  tooth  variations. 

In  this  study  I  treated  the  teeth  as 
prismatic  structures  with  no  ontogenetic 
variation.  This  assumption  is  true  for  all 
practical  purposes  once  the  individual  has 
passed  the  early  juvenile  age.  Juveniles  can 
be  culled  from  Microtus  samples  by  the 
criteria  of  overall  small  skull  size,  lack  of 
suture  closure,  and  lack  of  parallel-sided 
molars.  The  molars  continue  to  grow 
throughout  the  life  of  the  adult  individual, 
maintaining  an  almost  constant  crown  pat- 
tern. 

I  treated  the  tooth  crown  as  if  it  were  a 
two-dimensional  surface.  This  procedure 
is  also  not  precisely  correct.  The  upper 
tooth-row  surface  wears  to  a  slight  convex 


473 


VARIABILITY  IN  MICROTUS  MOLARS 


219 


profile  and  the  lower  conforms  to  this  with 
a  concave  profile  of  the  same  magnitude. 
The  mean  of  the  greatest  distance  that  the 
arc  deviates  from  a  straight  line,  intersecting 
the  terminal  ends  of  the  arc,  is  0.25  mm  or 
0.041  of  the  distance  of  the  straight  line. 
From  the  lateral  view  the  teeth  are  also 
curved;  the  M^'s  have  their  concave  sides 
anterior  and  M.^'s  posterior.  The  M|;'s  have 
only  a  slight  curvature.  In  most  of  the 
teeth  there  is  a  dorsoventral  twist,  so  Micro- 
tus  molars  may  be  considered  in  form  as 
segments  of  a  broad  helix. 

The  teeth  of  this  genus  are  quite  small, 
the  whole  tooth-row  being  only  about  6  mm 
long  in  M.  pennsylvanicus.  To  cope  with 
the  problem  of  measuring  teeth  of  this  size 
in  detail,  photographs  of  the  tooth  crown  of 
the  individual  teeth  in  M.  paroperarins, 
and  of  the  whole  tooth-row  in  M.  pennsyl- 
vanicus, were  taken  through  a  dissecting 
microscope.  The  crown  was  first  oriented 
at  right  angles  to  the  ocular,  then  the 
camera  was  mounted  and  brought  into 
focus.  All  pictures  were  taken  through  the 
same  ocular  at  the  same  magnification. 
These  were  then  enlarged  and  developed 
under  the  same  conditions,  including  film, 
paper,  and  enlarger  magnification.  A  note 
on  the  technique  (Guthrie,  in  preparation) 
includes  approximations  of  the  errors  in 
the  technique  at  the  various  steps. 

The  measurements  were  then  taken  from 
the  pictures  with  a  dial  micrometer  reading 
to  the  nearest  0.1  mm.  With  the  picture 
enlargement  of  31.8X,  this  resulted  in  mea- 
surements to  the  nearest  ?>.?>  microns.  The 
measurements  were  quite  repeatable.  The 
exterior  edge  of  the  enamel  was  used  in  all 
measurements.  Pictures  of  both  left  and 
right  sides  were  taken  of  M.  pennsylvanicus. 
The  side  with  the  picture  of  highest  con- 
trast was  used,  and,  if  there  was  any  ques- 
tion, measurements  were  taken  on  both 
sides.  Rarely  was  there  a  break  or  crack 
on  both  sides  so  that  no  measurement  could 
be  taken. 

Measurements  were  made  as  illustrated 
in  Fig.  1.  The  measurements  on  the  whole 
were  well  defined.    The  only  possible  ex- 


ceptions were  the  anterior  part  of  Mi  and 
the  posterior  part  of  M^.  However,  this  is 
a  function  of  their  variability  in  form. 
Several  measurements  were  used  on  the 
anterior  part  of  Mi  and  posterior  part  of  M'', 
but  no  one  expresses  adequately  the  vari- 
ation in  shape. 

The  width  measurements  for  each  tooth 
are  numbered  serially  from  the  loop.  Con- 
sequently, the  uppers  are  numbered  from 
anterior  to  posterior  and  the  lowers  from 
posterior  to  anterior.  The  total  length  is 
designated  by  L  and  the  anterior  and  pos- 
terior lengths  by  a  and  p,  respectively. 
Forty-two  measurements  were  taken  on 
each  individual,  20  measurements  on  the 
uppers  and  22  on  the  lowers. 

Discussion  of  Molar  Variations 

The  variation  in  Mi,  M-,  and  M^*  is 
represented  in  Fig.  2.  The  teeth  viewed 
from  left  to  right  depict  the  nature  and  ex- 
tent of  the  shape  variations  present  in  these 
samples.  In  reality,  this  variation  does  not 
fall  into  discrete  classes  as  portrayed  in 
Fig.  2;  rather,  each  tooth  in  the  figure 
represents  a  point  along  the  variation  con- 
tinuum. The  most  variable  portions  are 
cross-hatched  to  facilitate  the  comparisons. 
Notice  that  in  Mi  the  rounded  primordium 
on  the  lower  part,  actually  the  anterior  part 
of  the  tooth,  is  utilized  to  construct  new- 
salient  angles  by  the  penetration  of  re- 
entrant angles  into  its  lateral  margins. 

In  the  M-  a  new  salient  angle  is  formed 
by  the  budding  off  of  the  extreme  posterior 
part  of  the  crown,  and  varies  in  these  sam- 
ples all  the  way  from  absence  to  almost  the 
size  of  the  other  salient  angles.  M.  paro- 
perarius  has  only  a  slight  suggestion  of  this 
bud  in  some  individuals,  with  most  not 
having  it  at  all.  In  M.  pennsylvanicus  this 
rudimentary  stage  is  present  only  at  a  low 
frequency,  most  of  the  individuals  having 
a  well-developed  salient  angle. 

The  cross-hatched  area  in  the  posterior 
portion  of  the  M-^  behaves  differently  than 
the  cross-hatched  area  in  the  Mi.  M''  in- 
creases its  number  of  salient  angles  phylo- 
genetically  by  dropping  a  bud  posteriorly 


474 


220 


R.  D.  GUTHRIE 


c.v. 


12     3  12     3  12     3    4b 


P  dp  dp 


L     L     L 


C.V. 


12     3  12     3  I     2     3     4     S 


a     p  a     p  a     p 


L      L     L 


C.V. 


12     3  12     3  12      3     4     5 


a     p  a     p  d     p 


L      L      L 


C.V. 


2      3  12     3  12      3     4b 


a     p  a     p  a     p 


L     L    L 


Fig.  3.  Coefficients  of  variation  (C.V.)  of  the  upper  molars  of  M.  paroperarius  (sample  1) 
and  M.  pennsylvanicus  (samples  2-4)  ;  samples  are  identified  in  text.  The  tongue  inserts  are 
equal  to  two  standard  errors  in  each  direction.  The  measurements  at  the  base  of  each  histo- 
gram correspond  to  those  in  Fig.  1. 


475 


VARIABILITY  IN  MICROTUS  MOLARS 


221 


c.v. 


1     2     3     4     S    6     ?  12     3  12     3 


a     p  a     p  3     p 


L      L     L 


12 

11 

. 

10 

■ 

J 

■ 

M,         1 

C.V.    ' 

■ 

- 

J_l       ll 

1 

nWJ 

1 

UH 

1 

■1 

23.29 


Sample        2 


12     3     4     5     6     7  12     3  12     3 


C.V. 


12     3     4      5     6     7  12     3  12      3 


1,2,3 


a     p  J     p  a     p 


L      L      L 


Sample       4 


C.V. 


M 

1^1  2  3 

iAA 


12     3     4     5     6     7  12     3  12     3 


a     p  a     p  a      p 


Fig.  4.  Coefficients  of  variation  (C.V.)  of  the  lower  molars  of  M.  paroperarms  (sample  1) 
and  M.  pennsylvanicus  (samples  2-4)  ;  samples  are  identified  in  text.  The  tongue  inserts  are 
equal  to  two  standard  errors  in  each  direction.  The  measurements  at  the  base  of  each  histo- 
gram correspond  to  those  in  Fig.  \. 


476 


222  R-  D.  GUTHRIE 

and  enlarging  it  lingually.  However,  on  the  of  variation  than  any  of  the  other  width 

labial  side,  the  penetration  of  the  re-entrant  measurements  of  either  M^  or  M^.   This  is 

angles  and   the  outgrowth   of   the  salient  the  incipient  angle  which  is  predominantly 

angles  act  in  a  manner  much  the  same  as  present  in  M.  pcnnsylvanicus  and  expressed 

in  the  Mi.  There  is  very  little  difference  in  in  some  individuals  of  M.  paroperarius  as  a 

principle  in  the  mode  of  addition  of  salient  rudimentary  bump. 

angles  in  any  of  these  teeth,  only  slight  In  every  case  in  the  upper  molars  the 

variations  in  detail.  anterior  length   is   less   variable   than   the 

These  cross-hatched  areas  are  the  ones  posterior  length.  Fig.  3,  (a)  and  (p)  re- 
that  vary  most  between  species.  For  exam-  spectively.  In  the  case  of  M^  in  samples 
pie,  the  M^  tooth  pattern  at  the  extreme  three  and  four,  which  represent  males  and 
right  in  Fig.  2  is  present  in  only  one  indi-  females  from  one  series,  the  difference  be- 
vidual  in  the  samples  of  M.  pennsylvanicus,  tween  (a)  and  (p)  is  not  outstanding.  The 
but  is  the  most  common  tooth  pattern  in  difference  between  the  coefficients  of  vari- 
M.  chrotorrhinus.  Komarek  (1932)  reports  ation  of  the  anterior  and  posterior  length  is 
a  specimen  of  M.  chrotorrhinus  which  has  greatest  in  M'',  which  has  no  overlap  at  two 
one  less  angle  in  the  M^  than  usual.  This  standard  errors  in  either  direction.  The  en- 
specimen  would  correspond  to  the  most  tire  length  measurements  (L)  of  M^  and 
common  M.  pennsylvanicus  pattern.  In  ad-  M-  appear  to  have  about  the  same  magni- 
dition  to  M.  pennsylvanicus,  several  other  tude  of  variation.  The  length  measurement 
species  of  Microtus  have  hints  of  the  pos-  of  M^  has  a  larger  variation  in  all  cases 
teriolingual  bud  on  the  M-,  and  in  M.  cali-  than  either  M^  or  M^.  It  will  be  remem- 
jornicus  it  is  of  creditable  magnitude  bered  that  the  upper  molars  add  to  the 
(Hooper  and  Hart,  1962).  A  further  dis-  tooth  complexity  from  the  posterior  mar- 
cussion  of  the  intrageneric  variations  in  gins.  From  the  findings  here  it  may  also 
Microtus  is  given  by  Hooper  and  Hart  in  be  stated  that  these  phylogenetically  varia- 
the  preceding  reference.  ble  posterior  areas  of  the  uppers  have  the 

There  is  some  overlap  in  shape  between  greater  intrapopulational  variability, 

the  fossil  M.  paroperarius  and  the  recent  The    uniformity    of    the    four    samples 

M.  pennsylvanicus.   Referring  to  Fig.  2,  in  would  seem  to  increase  with  the  order  in 

Ml  the  third  pattern  from  the  left,  in  M-  which  they  are  listed,  as  there  are  progres- 

the  second,  and  in  M^  the  fourth  are  com-  sively  fewer  collecting  restrictions  imposed, 

mon  to  both  species.   However,  it  must  be  The    fossil    M.    paroperarius    sample    was 

kept   in   mind   that   the   discrete   patterns  taken  from  several  localities  and  with  some 

illustrated  here  are  only  chosen  points  along  temporal  variation  involved.    The  second 

a  continuum.  sample,  of  M.  pennsylvanicus,  was  taken 

The  42  different  measurements  are  repre-  over  a  wider  territory  than  samples  three 

sented  by  histograms  in  Figs.  3  and  4.  The  and  four,  which  were  collected  near  a  small 

most  striking  pattern  is  the  high  variation  city.  Since  there  is  a  high  interpopulational 

in  the  width  measurements  in  the  anterior  variation  in  M.  pennsylvanicus,  even  within 

part  of  Ml  and  the  posterior  part  of  M'^.  the  same  subspecies   (Snyder,   1954),  the 

Although  this  varies  slightly  in  magnitude  difference  in  uniformity  of  the  collecting 

between   samples,   the   general   pattern   is  restrictions  might  be  thought  to  affect  the 

much  the  same.    The  width  measurements  relative  amount  of  within-sample  variation, 

of  M^  have  relatively  low  coefficients  of  With  but  one  or  two  exceptions,  the  mea- 

variation,   all   under   six.    The   M^   width  surements  did  not  show  this  expected  vari- 

measurements  also  have  relatively  low  co-  ational  gradient  between  samples.    There 

efficients  of  variation.  The  width  measure-  also  proved  to  be  no  pattern  differences 

ment  number  three  of  M^,  which  includes  of  appreciable  magnitude  between  the  two 

the  incipient  angle,  has  a  larger  coefficient  sexes  of  M.  pennsylvanicus. 


477 


VARIABILITY  IN  MICROTUS  MOLARS 


223 


In  the  uppers  the  measurements  of  M. 
paropcrarhis  tend  to  be  more  variable  than 
the  samples  of  M.  pcnnsylvaniciis,  especially 
the  posterior  part  of  M^  where  the  co- 
efficient of  variation  is  about  double,  at 
least  in  the  width  measurements.  In  the 
width  measurements  of  the  phylogenetically 
more  stable  teeth  IVP  and  M-  there  is  no 
notable  difference  in  magnitude  between 
M.  paroperarius  and  M.  pennsylvanicus. 

The  M-  widths  have  a  relatively  low  to 
moderate  variation,  with  a  coefficient  of 
variation  of  about  six  or  less,  and  no  out- 
standing pattern  within  the  tooth.  M3 
width  measurements  tend  to  be  more  vari- 
able than  those  of  the  M2  with  the  anterior 
width  measurements  having  the  greater 
variation.  The  coefficients  of  variation  are 
very  large  in  the  anterior  part  of  Mi  (note 
width  measurements  five,  six,  and  seven). 
Another  peculiarity  of  Mi  in  M.  pennsyl- 
vanicus is  that  the  width  measurements  in 
the  midsection  of  this  tooth  are  less  vari- 
able than  either  the  anterior  or  posterior 
ones.  Some  of  the  other  teeth  show  this  to 
a  minor  degree  (note  M^  and  M-).  In  the 
lowers  the  anterior  length  measurements 
(a)  are  more  variable  than  the  posterior 
length  (p)  in  every  case  except  the  Mo  of 
sample  four.  Unlike  the  uppers,  the  lowers 
add  on  to  the  anterior  margins  of  the  teeth, 
and  we  may  conclude  from  the  coefficients 
of  variation  in  Fig.  4  that  these  anterior 
areas  of  the  lower  molars  also  have  the 
greatest  variation. 

In  both  the  posterior  lengths  (p)  and  the 
whole  lengths  (L)  there  is  a  trend  toward 
greater  variation  in  an  anterior  to  posterior 
direction  in  both  the  uppers  and  lowers. 
This  is  not  so  well  marked  in  the  anterior 
length  (a)  measurements. 

Of  the  measurements  of  the  entire  tooth 
length,  the  length  (L)  of  M3  is  the  most 
variable  in  M.  pennsylvanicus  while  the 
length  (L)  of  M^  is  the  most  variable  in 
M.  paroperarius.  This  is  a  case  where  the 
patterns  produced  by  the  length  variations 
(L)  are  somewhat  misleading.  In  M.  penn- 
sylvanicus M^  is  the  upper  tooth  with  the 
most  variation,  which  both  the  width  and 


the  length  measurements  suggest.  Mi,  on 
the  other  hand,  is  the  most  variable  tooth 
in  form  among  the  lowers.  This  is  evident 
in  the  width  measurements  but  does  not 
show  up  in  the  length  (L)  measurements  of 
M.  pennsylvanicus.  Although  Mi  is  the 
most  variable  lower  tooth  it  has  developed 
a  long  stable  posterior  area  which  dampens 
the  variations  occurring  at  the  anterior  part 
of  the  tooth,  thereby  producing  a  decep- 
tively low  coefficient  of  variation  for  the 
entire  tooth  length.  This  effect  is  not 
present  to  the  same  degree  in  the  Mi  of 
M.  paroperarius  (see  Fig.  2).  At  this  early 
phylogenetic  stage  the  tooth  has  a  rela- 
tively smaller  stable  posterior  section. 

M3  has  a  relatively  higher  variability 
than  the  other  phylogenetically  more  stable 
teeth  M^  M-,  and  M2.  It  is  the  one  tooth 
that  crosses  over  the  incisor  root  and  has  a 
limited  role  in  adding  to  the  crown  com- 
plexity of  the  tooth-row,  and  may  even 
be  in  a  state  of  reduction  in  this  particular 
genus.  In  some  other  genera  of  microtines, 
Dicrostonyx  for  example,  the  incisor  root 
does  not  cross  over  in  this  fashion  and  the 
M3  has  developed  a  more  complex  crown 
pattern.  Also,  it  is  not  reduced  in  size 
laterally  as  it  is  in  Microtus.  These  facts 
suggest  that  the  peculiar  relationship  of  M3 
to  the  incisor  places  some  limitations  on  its 
potential  for  increased  complexity. 

In  many  of  the  cricetines  both  the  upper 
and  lower  third  molars  have  undergone 
considerable  reduction;  this  is  not  the  case 
in  Microtus.  Some  individuals  of  M.  penn- 
sylvanicus have  a  longer  M^  than  M^. 

In  summary  then,  a  quantification  in 
these  two  species  of  the  molar  variability 
reveals  an  overall  pattern  of  higher  vari- 
ation in  the  posterior  parts  of  the  upper 
molars  and  the  anterior  parts  of  the  lowers. 
The  greatest  amount  of  variation  is  present 
in  the  anterior  end  of  Mi  and  the  posterior 
end  of  M^.  A  direct  positive  correspon- 
dence exists  between  those  areas  of  the 
teeth  which  are  changing  phylogenetically 
and  those  which  exhibit  a  greater  magni- 
tude of  variation. 


478 


224 


R.  D.  GUTHRIE 


Supporting  Evidence 

The  significance  of  a  positive  association 
between  the  rapidly  evolving  tooth  charac- 
ters and  a  relatively  high  variability  in 
Microtus  is  dependent  upon  its  general  ap- 
plicability. This  may  be  either  a  special 
case  or  an  expression  of  a  more  general 
phenomenon.  The  following  is  a  presenta- 
tion of  evidence  supporting  its  more  general 
nature. 

In  the  microtines  this  association  is  not 
limited    to    the   M.   paroperarius-pennsyl- 
vaniciis  line,   but   rather  it  is   a  common 
feature  of  the  whole  group.  Dicrostonyx  has 
the  most  complex  crown  pattern  of  the  sub- 
family.   D.  torqiiatus,    the   species    repre- 
sented in  the  second  phase  of  the  last  glaci- 
ation   (Zeuner,   1958),  has  a  variable  ex- 
pression of  new  salient  angles  on  the  pos- 
terior margin  of  M^  and  M-  and  the  an- 
terior margin  of  Mo  and  M3.  These  salient 
angles  are  highly  variable  in  their  occur- 
rence, grading  to  complete  absence  in  some 
individuals.    The  characteristic  species  of 
the  last  glaciation,  phase  one  (early  Wis- 
consin),  was   D.    henseli,   which   did    not 
possess  the  salient  angle  or  bud  as  did  D. 
totquatus.  This  bud  seems  to  be  a  nascent 
character  developing  through  the  last  glacial 
age.  D.  groenlandicus,  a  recent  species,  has 
this   character  present   in   all   individuals. 
D.  hudsonius,  a  species  with  a  distribution 
presently  limited  to  the  Hudson  Peninsula, 
is  a  living  relict  representative  of  the  D. 
henseli  tooth  pattern  of  the  early  part  of 
the  last  glaciation.   D.  torquatus  exists  as 
the  modern  Old  World  collared  lemming. 
Thus  there  is  a  chronological  and  geographi- 
cal representation  of  the  stages  of  develop- 
ment of  this  salient  angle.    The  fossil  D. 
henseli  and  the  recent  D.  hudsonius  do  not 
have  the  salient  angle.   D.  torquatus,  both 
modern  and  fossil,  has  a  varied  expression 
of  the  salient  angle  from  absent  to  fully 
present  (Hinton,  1926).   In  populations  of 
D.  groenlandicus  all   individuals   have   it. 
Some   taxonomists   give   these   forms   only 
subspecific  status;   however,  the  principle 
dealt  with  here  remains  valid. 

Kurten  (1959)  suggested  that  the  aver- 


age rate  of  mammalian  evolution  during 
the  Pleistocene  was  relatively  higher  than 
during  the  Tertiary.  His  analysis  of  the 
variability  in  several  rapidly  evolving 
groups,  widely  separated  taxonomically,  re- 
vealed an  increase  in  the  coefficient  of 
variation  in  more  lines  than  a  decrease. 
Although  his  study  did  not  deal  in  detail 
with  the  specific  characters  which  are 
changing  (he  used  an  average  of  several 
measurements),  it  did  serve  to  illustrate 
that  rapidly  evolving  populations  do  not 
all  tend  toward  morphological  uniformity. 
On  the  contrary,  it  suggested  the  opposite. 
Wright,  in  the  discussion  at  the  end  of 
Kurten's  paper,  proposed  that  recombina- 
tion is  responsible  for  this  ampHfication  of 
potential  variability. 

Skinner  and  Kaisen  (1947)  noted  that 
while  there  are  few  diagnostic  patterns  in 
the  evolution  of  Bison  cheek  teeth,  there  is 
a  general  trend  toward  the  molarization  of 
P4.  The  metastylid  and  median  labial  root 
of  the  P4  increase  in  frequency  through 
time.  In  early  fossil  Bison  these  characters 
are  virtually  absent  and  in  modern  ones 
almost  universally  present.  The  increases 
in  the  complexity  of  P4  seem  to  have  oc- 
curred over  a  relatively  short  period  of  time 
during  the  late  Pleistocene.  Since  these 
evolving  areas  range  from  absent  to  fully 
developed  in  some  populations  during  this 
period  of  incipiency,  the  variability  is 
greater  than  that  of  the  analogous  areas  of 
neighboring  teeth. 

Simpson  (1937)  discussed  a  sample  of 
?)2>  Eocene  notoungulates,  Henricosbornia 
lophodonta,  which  he  considered  to  be  from 
one  population,  since  their  variation  is 
normally  distributed  and  they  are  from  the 
same  horizon  and  locality.  These  were 
originally  described  by  Ameghino  as  be- 
longing to  17  species,  seven  genera,  and 
three  families,  principally  on  the  basis  of 
the  variation  present  in  the  upper  third 
molar.  The  variations  present  within  this 
primitive  form  are  characteristic  of  later 
species,  genera,  and  families  with  which 
Ameghino  was  familiar.  Here  is  an  exam- 
ple of  a  considerable  amount  of  variation 


479 


VARIABILITY  IN  MICROTUS  MOLARS 


225 


in  one  population,  the  elements  of  which 
are  later  characteristic  of  higher  taxa.  It 
would  be  consistent  with  the  evidence  to 
assume  that  the  tooth  is  undergoing  evolu- 
tionary change  in  a  manner  which  contrib- 
utes to  the  types  characteristic  of  later 
higher  taxa. 

Hooper's  (1957)  study  of  the  dentition 
of  Peromyscus  gives  supporting  evidence  to 
the  main  thesis  proposed  here  of  rapid  evo- 
lution being  accompanied  by  high  pheno- 
typic  variation.  A  series  of  P.  mankulatus 
from  Distrito  Federal,  Mexico,  for  example, 
has  highly  variable  molars.  The  mesoloph 
and  mesostyle  patterns  found  in  this  one 
series  resemble  the  common  patterns  of  the 
other  17  species  of  Peromyscus  studied.  In 
other  words,  the  mesostyle  and  mesoloph 
patterns  observed  in  1 7  species  of  Peromys- 
cus are  also  seen  in  this  single  series. 
P.  mankulatus  is  first  known  from  the  Wis- 
consin age  and  has  expanded  its  distribu- 
tion over  a  considerable  part  of  North 
America.  It  is  considered  to  be  one  of  the 
"younger"  species  of  Peromyscus  (King, 
1961),  and  therefore  has  recently  under- 
gone evolutionary  change  at  the  species 
level. 

The  occurrence  of  the  crochet  in  horse 
teeth  is  another  example  of  an  incipient 
character  that  is  highly  variable  in  the 
same  population  (Simpson,  1953;  Stirton, 
1940).  The  acquisition  of  this  plication  is 
one  of  the  first  features  in  a  general  trend 
toward  increased  tooth  complexity.  The 
crochet,  an  anastomosing  ridge  between 
metaloph  and  protoloph,  shows  up  in  the 
Miohippus-Parahippus  line.  It  is  also  pres- 
ent in  some  species  of  Archeohippus  and 
sometimes  in  the  milk  teeth  of  Hypohippus 
(Stirton,  1940).  The  incipient  crochet  juts 
out  as  a  peninsula  or  pier  from  the  meta- 
conular  part  of  the  metaloph  toward  the 
protoloph.  The  degree  of  its  development 
is  extremely  variable,  from  absence  to  a 
small  spur  extending  halfway  across,  to  a 
complete  connection  between  the  two  lophs. 
The  crochet  varies  both  in  frequency  and 
extent  between  populations  and  within 
them,   occurring  in   its   various   stages   of 


representation  in  individuals  of  the  same 
species  at  one  locality. 

Butler  (1952),  speaking  of  the  molariza- 
tion  of  premolars  in  Eocene  horses,  stated 
that  the  metaconule  evolving  in  the  pre- 
molars is  most  variable  at  the  intermedi- 
ate stages  of  molarization. 

Wood's  (1962)  discussion  of  the  tooth 
cusp  variations  in  the  early  paramyid  ro- 
dents showed  that  the  hypocone  is  added 
to  the  tooth  by  two  basically  different 
means.  In  some  forms  it  is  derived  from 
an  enlargement  of  the  posterointernal  cin- 
gulum;  in  others  it  originates  as  a  division 
of  the  protocone.  Wood  attributed  these 
two  distinctly  different  means  of  achieving 
fundamentally  the  same  end  product  to  a 
general  selection  toward  the  development 
of  a  posterointernal  cusp  irrespective  of  the 
nature  of  its  origin.  The  addition  of  the 
fourth  cusp,  hypocone,  is  a  common  phe- 
nomenon in  many  lines  during  this  part  of 
the  Tertiary,  and  seems  to  be  correlated 
with  the  exploitation  of  more  demanding 
food  substances.  Wood  stated,  "There  is 
no  question  but  that  all  of  these  variants 
may  occur  within  a  single  genus  and  some- 
times within  a  single  species."  Here  again, 
when  a  directional  selection  pressure  is 
being  applied,  more  phenotypic  variation  is 
exhibited  in  the  incipient  than  in  the  non- 
incipient  cusps. 

The  lower  third  premolar  is  used  to  char- 
acterize various  genera  of  fossil  rabbits. 
Hibbard  (1963)  observed  much  variation 
within  a  primitive  rabbit  genus,  Nekrolagus, 
and  found  at  a  low  frequency  a  pattern  of 
the  P3  that  is  characteristic  of  modern 
genera.  The  common  tooth  pattern  of 
Nekrolagus  is  also  found  at  a  very  low  fre- 
quency in  some  modern  genera.  This  com- 
parative study  documents  a  chronological 
frequency  change  in  which  the  early  fossil 
populations  have  the  incipient  characters 
represented  at  a  low  frequency  and  the 
modern  populations  at  a  high  frequency. 
Here  is  another  case  in  which  there  is  a 
high  variation  associated  with  incipient 
characters,  and  the  axis  of  this  variation  is 
parallel  to  phylogenetic  change. 


480 


226 


R.  D.  GUTHRIE 


Another  opportunity  to  try  the  hypothe- 
sis is  on  the  results  of  artificial  selection 
experiments.  If  the  hypothesis  does  ap- 
proximate the  real  condition,  the  character 
that  is  artificially  selected  for  or  against 
should  behave  in  a  manner  similar  to  the 
evolving  characters  that  have  just  been  dis- 
cussed. That  is,  characters  undergoing  arti- 
ficial selection  could  be  expected  not  to  ex- 
perience a  decrease  in  their  phenotypic 
variation,  but  to  maintain  or  even  increase 
the  variation. 

MacArthur  (1949)  selected  for  large 
and  small  size  in  mice  using  the  weight  at 
60  days  as  a  measure  of  size.  In  the  un- 
selected  control  the  coefficient  of  variation 
was  11.1.  However,  in  the  strain  selected 
for  large  size  it  was  12.8,  and  in  the  small 
line  14.3. 

Falconer  (1955)  also  selected  for  large 
and  small  size  in  mice  using  the  sixth  week 
weight  as  a  measure  of  size.  He  stated, 
''The  phenotypic  variability,  also,  does  not 
reflect  the  expected  decline  of  genetic  vari- 
ance, and  in  addition  reveals  a  striking  and 
unexpected  change  in  the  small  line."  He 
further  reported  that  the  large  line  showed 
a  slight  increase  in  variation  over  the  whole 
course  of  the  experiment,  although  it  re- 
mained relatively  low  compared  to  the  vari- 
ation of  the  small  line.  The  coefficient  of 
variation  in  the  small  line  increased  to 
about  double  the  original  value  between 
the  seventh  and  ninth  generations  and  re- 
mained at  this  high  level.  The  realized 
heritability  remained  substantially  constant 
up  to  the  point  at  which  response  ceased. 
This  phenomenon,  he  suggested,  was  due 
to  the  release  of  genetic  variation  through 
recombination. 

In  their  selection  experiments  for  wing 
length  in  Drosophila,  Reeve  and  Robertson 
(1953)  found  that  the  coefficients  of  vari- 
ation at  the  twentieth  to  seventy-ninth  gen- 
erations were  all  below  two  in  the  unselected 
strain  and  all  two  or  above  in  the  selected 
strain.  The  strain  selected  for  long  wings 
showed  an  increase  of  about  50  per  cent  in 
total  variance.  They  attributed  this  en- 
tirely to  an  increase  in  additive  genetic 


variance,  which  rose  about  two  and  one- 
half  times,  while  the  absolute  amount  of 
other  genetic  variance  remained  about  the 
same.  This  led  them  to  suppose  that  selec- 
tion for  long  wing  length  would  be  far  more 
effective  in  the  selected  than  in  the  un- 
selected stock. 

Clayton  and  Robertson  (1957),  selecting 
for  low  and  high  bristle  number  in  Drosoph- 
ila, concluded  that  "Selection  had  by  no 
means  led  to  uniformity,  but  in  some  cases 
even  magnified  the  total  variation." 

Robertson  (1955)  selected  for  thorax 
length  in  three  stocks  of  Drosophila  with 
about  the  same  initial  amount  of  variation. 
The  coefficient  of  variation  in  the  small 
lines  increased  immediately  in  the  first  gen- 
erations and  was  higher  than  the  control 
in  all  three  lines,  although  there  were  be- 
tween-strain  differences  in  the  pattern  of 
increase  in  variation.  In  the  large  lines  the 
variation  fluctuated  around  that  of  the  con- 
trol stock.  Thus,  in  the  large  strains  the 
changes  in  response  to  selection  occurred 
without  appreciable  change  in  the  coeffi- 
cient of  variation,  while  the  variation  of 
the  small  line  increased. 

Although  the  changes  in  variation  ac- 
companying selection  response  in  these  ex- 
periments do  not  behave  in  a  completely 
uniform  manner,  they  do  maintain  and 
usually  increase  the  initial  magnitude  of 
variation.  Thus,  evidence  supporting  the 
association  between  directional  selection 
and  a  constant  or  increased  variation  is 
found  both  in  rapidly  evolving  groups  and 
in  artificial  selection  experiments  in  which 
the  degree  of  variational  change  has  been 
recorded. 

The  Theory  and  Model 

The  most  frequently  employed  explana- 
tion for  an  inordinate  amount  of  variation 
is  vestigiality.  In  such  a  case  the  charac- 
ters under  consideration  are  not  becoming 
more  complex  phylogenetically  but  are  de- 
creasing in  pattern  complexity.  Morpho- 
logical characters  which  are  in  the  process 
of  reduction  or  elimination  exhibit  more 
variation    than   do    their   more    functional 


481 


VARIABILITY  IN  MICROTUS  MOLARS 


227 


homologues.  This  high  correlation  between 
vestigial  and  highly  variable  characters  no 
doubt  influenced  Hinton  (1926)  to  believe 
the  microtines  to  be,  in  tooth  form,  degen- 
erate descendants  of  the  multituberculates 
and  consequently  undergoing  reduction  in 
tooth  complexity.  However,  there  is  a  time 
gap  in  the  fossil  record  of  some  35  million 
years  between  the  multituberculates  and 
microtines.  The  concept  of  the  vestigial 
nature  of  microtine  teeth  has  been  perpetu- 
ated by  some  mammalogists  (Goin,  1943; 
Hall  and  Kelson,  1959).  But  the  position 
that  microtines  did  not  arise  from  a  crice- 
tine  stock  and  have  not  undergone  a  gen- 
eral increase  in  tooth  complexity  is  untena- 
ble. Not  only  does  the  fossil  record  support 
an  increase  in  microtine  tooth  complexity, 
but  there  is  an  almost  complete  continuum 
of  recent  intermediate  forms  between  the 
Microtinae  and  Cricetinae.  Vestigiality  can 
be  discounted  as  an  explanation  of  the 
variation  differential  in  the  other  examples 
as  well,  as  these  characters  are  also  in- 
creasing in  complexity. 

Lately,  much  attention  has  been  given  to 
the  loss  of  buffering  capacity  against  en- 
vironmental stress  as  the  genome  tends 
toward  homozygosity  (Lerner,  1954).  Since 
directional  selection  reduces  the  amount  of 
individual  heterozygosity,  the  loss  of  buf- 
fering would  result  in  a  greater  magnitude 
of  individual  deviation  from  the  mean,  in- 
creasing the  phenotypic  variation  of  that 
population.  This  process  may  be  the  cardi- 
nal factor  involved  in  an  explanation  of  the 
phenomenon  of  an  increase  in  variation  ac- 
companying directional  selection.  However, 
there  is  some  discouraging  evidence  against 
an  explanation  of  this  nature.  (1)  The  in- 
crease of  phenotypic  variation  becomes  evi- 
dent early  in  artificial  selection  (Robertson, 
1955)  before  an  appreciable  amount  of 
genetic  variance  could  have  been  lost  by 
selection.  (2)  A  character  in  which  selec- 
tion has  considerably  altered  the  mean  can 
often  be  returned  with  little  difficulty  to 
the  original  mean  by  reversed  selection. 
This  reversal  could  not  take  place  if  the 
population  had  reached  a  relatively  homozy- 


gous  level    for    that   particular   character. 

(3)  A  correlate  of  the  latter  is  that  often  a 
substantial  heritable  component  is  still 
present  after  the  mean  has  been  considera- 
bly altered   by  selection    (Lerner,    1958). 

(4)  Bader  (1962)  showed  that,  in  tooth 
form,  inbred  mice  exhibit  slightly  less 
phenotypic  variation  than  wild  popula- 
tions; and  the  outcrossed  heterozygote  is 
less  variable  than  either.  (5)  If  the  tooth 
variation  discussed  here  in  Microtus  is  non- 
genetic,  it  is  difficult  to  explain  the  phylo- 
genetic  increase  in  tooth  complexity,  since 
the  most  important  cause  of  evolutionary 
change  is  selection  acting  upon  heritable 
variation.  From  some  preliminary  crosses 
of  microtines  (Steven,  1953;  Zimmermann, 
1952),  it  does  seem  that  these  variations 
are  heritable.  In  at  least  one  species  of 
Microtus  [M.  arvalis)  there  is  also  a  geo- 
graphic cline  in  the  frequency  of  tooth 
complexity.  The  variations  were  classed 
into  two  discrete  types  (simple  or  com- 
plex) ;  the  frequency  of  ''complex"  ranges 
from  five  per  cent  to  95  per  cent  in  the 
cline  from  northern  to  southern  Europe 
(Zimmermann,  1935). 

The  accumulated  evidence  from  breeding 
experiments  suggests,  contrary  to  the  "wild 
type"  or  normality  concept,  that  there  is 
considerable  heterozygosity  underlying  the 
relatively  coherent  facade  of  the  phenotype. 
The  variation  expressed  in  the  phenotype  is 
only  a  fraction  of  the  total  possible  varia- 
tion present  (Mather,  1956).  There  is  a 
diversity  of  opinion  as  to  the  mechanisms 
involved  in  the  maintenance  of  this  large 
amount  of  potential  variability.  The  posi- 
tion that  the  balanced  additive  factors 
maintain  the  stored  variabihty  has  much 
evidence  in  its  favor  in  terms  of  its  general 
applicabiUty  to  evolution  at  the  intrapopu- 
lational  level.  Stated  in  more  detail,  this 
position  asserts  that  there  exist  balanced 
systems  of  linked  heterozygous  polygenes 
structurally  associated  and  maintained  by 
selection  and  perhaps  also  by  decreased 
recombination. 

Delayed  responses  to  selection  are  best 
accounted  for  on  the  basis  of  genetic  link- 


482 


228 


R.  D.  GUTHRIE 


age.  A  rather  common  phenomenon  in  ex- 
perimental breeding  is  for  a  selected  strain 
to  reach  a  plateau  of  response  only  to  have 
it  resume  progress  after  a  period  of  relaxa- 
tion of  the  selection  pressures.  The  most 
plausible  explanation  of  this  phenomenon 
is  linkage  disassociation;  the  various  ele- 
ments are  unable  to  segregate  out  im- 
mediately because  of  linkage  restrictions 
(Mather,  1949).  The  ineffectiveness  of  ex- 
periments to  reduce  the  variation  by  selec- 
tion for  intermediates  (Lerner's  type  II  se- 
lection, Lerner,  1958;  Falconer,  1957),  and 
the  ineffectiveness  of  selection  for  the  ex- 
tremes to  alter  the  variation  (type  III  se- 
lection. Falconer  and  Robertson,  1956) 
both  suggest  that  the  additive  genetic  ma- 
terial resides  in  balanced  linkage  groups. 

Structural  change,  which  often  inhibits 
crossing  over,  may  establish  an  isolation  of 
segments  of  the  chromosome  where  crossing 
over  is  likely  to  occur  only  with  configura- 
tions of  that  same  type;  however,  the  gen- 
eral importance  of  this  mechanism  is  still 
not  clear.  As  well  as  promoting  these  de- 
vices that  inhibit  recombination,  selection 
can  operate  directly  to  maintain  these 
blocks  intact  (Lerner,  1958)  and  this  is 
probably  the  most  important  mechanism. 
Carson  (1959)  reports  that  most  natural 
inversions  are  heterotic  when  removed  from 
nature  to  the  laboratory  culture,  and  that 
strains  derived  from  a  single  pair  of  wild 
flies  retain  with  extreme  tenacity  most  of 
their  initial  inversion  variability. 

The  advantages  of  a  system  of  balanced 
linkage  groups  are  multiple.  The  popula- 
tion can  maintain  a  high  degree  of  hetero- 
zygosity in  many  individuals  without  the 
rigorous  selection  required  if  these  elements 
were  segregating  at  random.  The  close 
linkage  association  also  serves  as  a  buffer 
against  random  fluctuations  away  from  the 
optimum.  And  perhaps  most  important,  it 
holds  genetic  material  in  reserve,  thereby 
maintaining  an  evolutionary  plasticity. 

There  is  evidence  that  integrated  chro- 
mosome segments  are  important  in  the  as- 
sociation or  correlation  of  continuously  dis- 
tributed characters,  and  that  they  behave 


in  a  manner  similar  to  single  independent 
genes  acting  pleiotropically.  To  resolve  or 
disassociate  the  correlation  of  two  charac- 
ters by  selection  would  produce  strong  evi- 
dence for  linkage.  Such  disassociation  has 
been  accomplished  (Mather  and  Harrison, 
1949;  Mather,  1956).  Correlation  due  to 
pleiotropy  is,  of  course,  more  resistent  to 
evolutionary  change  than  the  more  labile 
system  of  linkage  groups.  Linkage  groups 
can  originate  or  be  disposed  of  by  the  selec- 
tion for  various  recombination  and  struc- 
tural patterns.  It  would  be  a  slow  process 
for  the  population  to  await  a  new  mutation 
at  one  locus  which  acted  upon  the  desired 
characters  in  exactly  the  right  magnitude. 

Selection  can  maintain  a  frequency  of  bal- 
anced genetic  material  within  each  chromo- 
somal block  or  "internally"  at  levels  that 
insure  a  considerable  proportion  of  "rela- 
tionally"  balanced,  or  heterozygous,  indi- 
viduals in  the  population.  As  long  as  this 
block  remains  intact  it  will  carry  reserves 
of  variability  which  may  be  released  and 
made  available  for  segregation  by  crossing 
over.  With  selection  against  the  cross- 
overs, this  residual  genetic  variability  can 
be  maintained  (Lerner,  1958).  In  order  to 
maintain  the  internally  balanced  linked 
groups  a  selection  intensity  would  be  re- 
quired equivalent  to  the  frequency  of  cross- 
overs which  deviate  from  the  balanced  con- 
figuration (Falconer,  1960). 

The  increase  in  variation  of  evolving 
characters  may  be  further  enhanced  when 
an  interbreeding  population  experiences  the 
stress  of  two  selective  optima.  This  condi- 
tion would  occur  in  most  evolutionary 
changes  when  the  group  is  partially  exploit- 
ing two  adaptive  zones.  Thus,  a  character 
in  transition  may  be  expected  to  experience 
some  reduction  in  stabilizing  selection  along 
its  axis  of  change. 

The  high  variation  usually  associated 
with  vestigiality  can  also  be  accounted  for 
in  the  context  of  this  theory.  A  vestigial 
character  is  in  essence  an  evolving  charac- 
ter, as  reduction  plays  a  great  part  in  evo- 
lutionary change.  According  to  the  ex- 
planation given  for  the  greater  amount  of 


483 


VARIABILITY  L\  MICROTUS  MOLARS 


229 


variation  in  evolving  characters,  the  stored 
variability  is  maintained  in  a  linked  system 
by  stabilizing  selection.  When  this  balance 
is  altered  by  directional  selection,  the  vari- 
ability is  released.  Due  to  its  decreasing 
functional  role,  the  variation  of  a  vestigial 
character  would  also  be  compounded  by  a 
decrease  in  stabilizing  selection. 

Carson  (1955),  in  his  discussion  of  the 
genetic  composition  of  marginal  popula- 
tions, surmised  that,  since  the  marginal 
populations  contain  fewer  inversions  than 
central  populations,  the  more  stringent 
selection  on  the  periphery  is  against  the 
heterotic  groups  which  predominate  in  the 
central  population.  These  findings  are  in 
agreement  with  the  idea  expounded  here, 
that  directional  selection  away  from  the 
mean  is  selection  for  the  breakdown  of 
present  linkage  configurations.  Carson  fur- 
ther reported  that  when  strong  artificial 
selection  was  applied  to  both  marginal  and 
central  population  lines,  the  marginal  lines 
showed  the  greater  initial  response.  This 
difference  would  exist  if  the  genetic  ma- 
terial has  been  made  available  for  segrega- 
tion in  the  marginal  populations  by  the 
breakdown  of  the  linkage  groups. 

Reeve  and  Robertson  (1953),  selecting 
for  wing  length  in  Drosophila,  found  that 
the  selected  strain  showed  an  increase  in 
additive  genetic  variance  of  250  per  cent, 
all  other  genetic  variance  remaining  about 
the  same.  They  further  suggest  that  selec- 
tion for  long  wing  length  would  be  more 
effective  in  the  selected  than  in  the  un- 
selected  stock.  Robertson  (1955)  states: 
"Selection  generally  leads  to  an  increase  in 
variance  which  appears  to  be  largely  due  to 
the  increased  effects  of  genetic  segregation 
and  this  constitutes  an  aid  to  selection 
progress." 

This  release  of  additive  genetic  variation 
provides  a  mechanism  whereby  directional 
selection,  in  continuously  distributed  poly- 
genic systems,  increases  its  own  resolving 
power.  Selection  against  the  mean  and  its 
present  balance  situation  is  selecting  against 
the  present  linkage  configurations,  which 
results  in  a  breakdown  of  these  integrated 


units.  The  genetic  components  are  then  re- 
leased and  made  available  for  novel  segre- 
gants  hitherto  unavailable.  The  conse- 
quence of  this  is  an  increase  in  phenotypic 
variation,  which  is  heritable  in  an  additive 
fashion.  As  the  amount  of  variation  is  a 
determining  factor  of  the  effectiveness  of 
selection,  in  conjunction  with  selection  in- 
tensity and  heritability,  further  selection 
gains  are  facilitated. 

To  set  up  a  simple  visual  model  of  this 
theory  let  us  suppose,  as  is  expressed  in 
Fig.  5,  that  there  is  a  series  of  loci  with 
alleles  acting  in  an  additive  fashion  either 
to  the  left  or  right  of  the  mean.  Loci  a,  b, 
c,  and  d  control  the  size  of  character  X  and 
e,  f,  g,  and  h  control  Y.  The  contribution 
of  each  allele  is  specified.  Further,  suppose 
these  are  balanced  "internally"  and  "rela- 
tionally,"  with  an  equal  frequency  of  each 
linkage  group.  The  mean  will  be  consid- 
ered as  zero  with  the  deviations  from  it  in 
both  positive  and  negative  directions.  A 
stabilizing  selection  for  the  mean  would 
cull  out  deviants,  the  crossovers,  from  this 
configuration.  The  genetic  material  present 
is  potentially  able  to  produce  an  individual 
representative  of  any  point  in  the  figure, 
but  this  particular  linkage  configuration 
limits  the  phenotypes  to  a  coherent  cluster 
around  the  mean.  The  broken  circle  repre- 
sents a  variation  of  two  standard  deviations 
from  the  mean,  if  each  locus  were  acting 
individually  with  an  equal  frequency  of 
each  allele.  The  linked  configuration,  how- 
ever, would  produce  a  population  with  a 
lower  variation,  expressed  here  at  two  stan- 
dard deviations  by  the  solid  inner  circle. 

If  a  new  adaptive  optimum  (A'-)  were 
created  with  a  consequent  directional  selec- 
tion of  moderate  magnitude  exerted  on  the 
distribution,  the  linkage  groups  would  be 
selected  against  by  a  selection  for  the  cross- 
overs in  the  direction  of  the  new  adaptive 
optimum,  resulting  in  a  partial  breakdown 
of  the  coherent  phenotype. 

A  structural  association  of  the  loci  con- 
trolling the  two  characters  (Fig.  6)  would 
result  in  their  correlation.  The  points  all 
fall  along  the  diagonal  axis  between   +2 


484 


230 


R.  D.  GUTHRIE 


6 
5 
4 

C+)  3 
2 

1 

Y       0 

1 

2 

(-)  3 
4 


• 

y                                                                                        N 

y 
/ 

a,   b2 
32   b, 

\ 
\ 
\ 
\ 
\ 

c,    d2        e 

C2    d,        e 

a=0.5 
b  =  1.0 

e 

f 

■     g 

h 

'  o 

\ 

c  =  0.5 
d=  1.0 
e  =  0.5 
f  =1.0 
g  =  0.5 
h  =  1.0 

' 

\ 

"^                                                                                     y 

1 

1 
/ 

y  • 

sub1=(— ) 
sub2=(+) 

a  ,  b,  c,  d 

2     '1 


3 
(-) 


0 
X 


3 
(+) 


gl     ^2 
%2    hi 


Fig.  S.  An  elementary  model  of  the  non-correlated  case  of  two  characters  X  and  Y,  where  low 
phenotypic  variation  is  maintained  by  selection  for  the  linkage  configuration  represented  in  the  upper 
right.  With  equal  frequencies  of  each  linkage  group  the  variation  of  the  population,  at  two  standard 
deviations,  would  be  circumscribed  by  the  solid  circle.  The  dashed  Hne  represents  the  same  loci  with 
no  linkage.  Selection  for  A'o  would  increase  the  variation  as  the  linkage  configuration  would  be 
selected  against. 


and  -2  units,  as  shown  by  the  ellipse.  If 
one  were  to  think  in  terms  of  the  major 
axis  of  variation  as  size,  this  provides  a  rela- 
tively constant  individual  shape  throughout 
a  population  in  which  the  individuals  are 
varying  in  size.  As  in  Fig.  5  it  will  be  noted 
that  an  imposed  directional  selection  will 
produce  an  increase  in  variation.  Even 
directional  selection  parallel  with  the  main 
axis  of  size  will  increase  the  variation.  The 
greatest  increase  in  variation,  however, 
would  be  produced  by  a  selection  pressure 
at  right  angles  to  the  principal  axis  of  vari- 
ation, toward  X2,  which  would  be  selection 
for  shape  changes.  The  long-term  effect  of 


this  type  of  selection  would  be  twofold:  ( 1 ) 
an  increase  in  phenotypic  variation,  and 
(2)  a  decrease  in  the  correlation  of  char- 
acters X  and  F.  Unlike  the  situation  in 
Fig.  5,  if  a  selection  pressure  is  exerted  on 
only  one  character  (perpendicular  to  the 
scale  of  the  other),  the  second  character  is 
also  initially  affected.  However,  it  is  an 
inherent  mechanism  of  the  model  that  the 
linkage  which  provides  the  correlation  of 
the  characters  will  be  selected  against  when 
only  one  character  is  subjected  to  direc- 
tional selection.  This  system  then  would 
further  contribute  to  evolutionary  plas- 
ticity. 


485 


VARIABILITY  IN  MICROTUS  MOLARS 


231 


6 
5 

4 

(+)3 
2 

1 
Y  0 
1 
2 
(— )  3 
4 


a^   ^2  ej  f2        c^  dj  g^  hj 
32  b,  ejf^        C2  d^  g2h^ 


e 
f 
g 
h 


b.  c  .d 


■bi 


3 
C— ) 


0 
X 


3 


a  =  0 

b=  1 


c  =  0.5 


d=l 
e  =  0 
f  =  1 
g=0.5 

h=1.0 


sub  1  =  (— ) 
sub  2  =  (-I-) 


Fig.  6.  Same  as  Fig.  S  except  that  characters  A'  and  Y  are  now  correlated  due  to  the  linkage  asso- 
ciation. This  new  linkage  configuration  maintains  a  coherence  differentially  on  the  size  and  shape  axes. 
Selection  toward  A^o  would  considerably  increase  the  variation  along  the  shape  axis. 


I  do  not  wish  to  imply  that  the  theory 
expressed  here  accounts  for  all  the  various 
behavior  exhibited  by  residual  genetic  varia- 
tion. Rather,  I  have  investigated  one  aspect, 
the  association  of  directional  selection  and 
the  maintenance  or  increase  of  the  initial 
phenotypic  variation,  and  have  hopefully 
offered  a  plausible  explanation,  which  will 
be  further  explored  soon  by  breeding  experi- 
ments with  Microtus. 

Summary 

This  is  a  study  of  the  intrapopulational 
variability  present  in  the  dentition  of  two 
species  of  Microtus,  and  the  more  general 
questions  arising  from  it.  The  central  thesis 


is  that  quantitative  characters  undergoing 
rapid  evolution  do  not  show  the  decline  in 
phenotypic  variation  predicted  by  our  pres- 
ent evolutionary  concepts.  On  the  contrary, 
the  variation  is  maintained  and  usually  in- 
creased. 

Of  the  two  species  used,  the  fossil  species 
is  thought  to  be  ancestral  to  the  modern 
meadow  vole ;  thus  the  study  materials  com- 
prise an  evolutionary  line  with  two  grades 
of  tooth  complexity  represented.  In  the 
molar  crowns  of  both  species,  the  areas 
which  are  changing  phylogenetically  are 
those  which  vary  most  within  the  popula- 
tion. Evidence  from  other  sources  in  which 
characters  are  undergoing  directional  selec- 


486 


in 


R.  D.  GUTHRIE 


tion,  both  evolutionary  and  artificial,  sug- 
gests that  a  greater  variation  in  characters 
undergoing  directional  selection  is  a  general 
condition. 

A  theory  to  account  for  association  be- 
tween rapidly  evolving  characters  and  a 
relatively  higher  amount  of  phenotypic 
variation  is  that  the  coherence  of  the  popu- 
lation around  the  mean  is  due  to  balanced 
heterozygous  linkage  groups  and  that  with 
the  application  of  directional  selection  this 
organization  is  partially  broken  down.  The 
genetic  variation  is  then  released  and  made 
available  for  recombination.  The  relatively 
high  variability  associated  with  vestigial 
characters  is  also  fitted  into  the  context  of 
the  theory.  The  theory  suggests  that  direc- 
tional selection  on  continuously  distributed 
characters  increases  its  own  effectiveness. 

Acknowledgments 

I  wish  to  express  my  appreciation  to  Dr. 
E.  C.  Olson,  University  of  Chicago,  the 
chairman  of  my  graduate  committee,  for 
his  encouragement  and  assistance  with  the 
presentation.  Thanks  are  also  due  to  Dr. 
Vernon  Harms  and  Dr.  Brina  Kessel,  Uni- 
versity of  Alaska,  for  their  helpful  criti- 
cisms of  the  manuscript.  My  deepest  grati- 
tude goes  to  Dr.  R.  S.  Bader,  University  of 
Illinois,  for  the  many  stimulating  discus- 
sions which  were  to  form  the  nucleus  of  my 
interests  in  evolutionary  mechanisms.  I 
wish  to  thank  also  those  in  charge  of  collec- 
tions at  the  University  of  Kansas  Museum 
of  Natural  History,  University  of  Michigan 
Museum  of  Zoology,  Carnegie  Museum,  and 
Chicago  Museum  of  Natural  History  for 
the  use  of  the  specimens. 

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Snyder,    D.    P.      1954.      Skull    variation    in    the 

meadow    vole    (Microtus    pennsylvanicus)    in 

Pennsylvania.    Ann.  Carnegie  Mus.,  33:   201- 

234. 
Steven,  D.  M.     1953.     Recent  evolution  in   the 

genus  Cleithrionomys.    Symp.  Soc.  Exp.  Biol., 

7:  310-319. 
Stirton,  R.  a.     1940.     Phylogeny  of  the  North 

American    Equidae.     Univ.    CaUfornia    Publ., 

Bull.  Dept.  Geol.  Sci.,  25:   165-198. 
Zeuner,  F.  E.     1958.    Dating  the  past.   Methuen, 

London. 
Zimmermann,  K.     1935.     Zur  Rassenanalyse  der 

mitteleuropaischen    Feldmause.     Arch.    Natur- 

gesch.,  N.  F.  5. 
.      1952.      Die    simplex-Zahnform    der    Feld- 

maus,   Microtus  arvalis.    Pallas.    Verb.   Deut. 

Zool.  Ges.,  Freiburg. 


488 


Sonderdruck  aus  Z.  f.  Saugetierkunde  Bd.  32  (1967)  H.  3,  S.  167—172 

Alle   Rcdite,    audi    die   der  Obersetzung,    des    Nachdrucks    und    dcr    photomechanischcn    Wiedergabe,    vorbehalten. 

VERLAG    PAUL    PAREY    ■    HAMBURG  1    •    SPITALERSTRASSE  12 

©    1967   Verlag   Paul   Parey,   Hamburg   und   Berlin 

Evolutionary  adaptations  of  temperature  regulation  in  mammals^ 


By  L.  Jansky 


Eingang  des  Ms.  25.  10.  1966 


Generally  speaking,  adaptations  may  take  place  either  during  individual  life  of  animals 
(acclimations  and  acclimatizations),  or  they  may  be  specific  to  certain  species  (evolu- 
tionary adaptations)  (Hart  1963b).  They  may  be  realized  by  different  mechanisms  with 
different  degree  of  efficiency,  however  the  aim  of  all  adaptations  is  essentially  the 
same  —  to  reduce  the  dependence  of  animals  on  environmental  conditions  and  thus  to 
increase  their  ecological  emancipation.  The  study  of  physiological  mechanisms  of 
adaptations  is  therefore  of  great  ecological  importance  since  it  helps  us  to  elucidate 
physiological  processes  influencing  limits  of  distribution  of  different  species  and  having 
a  profound  effect  on  the  quality  or  density  of  animal  populations.  The  comparison  of 
individual  and  evolutionary  adaptations  permits  us  to  trace  the  evolutionary  progres- 
sive physiological  processes  and  to  contribute  to  the  problems  of  phylogeny. 

In  lowered  temperatures  mammels  tend  to  lose  heat.  Theoretically,  they  can  prevent 
hypothermia  either  by  increasing  heat  production  in  the  body  or  by  reducing  heat  loss 
from  the  body  to  the  environment.  Heat  production  is  realized  by  shivering;  heat 
conservation  may  be  manifested  by  reducing  the  body  surface,  by  improving  its  insu- 
lation qualities  and  by  decreasing  the  body— air  temperature  gradient  according  to 
formula:  „        „ 

•y     np 

H  =  K  ~ (1)       (Hart,  1963b) 


I 


:2 

O 

o 

Q 

o 

t— 

Lu 

3: 


Uj 
CK 

>- 

Q 
O 
QQ 


^OLD    ADAPTED 

WARM    ADAPTED 


nonshivering 
thermogenesis 


lower  critical    temperature 


Fig.  1.  Scheme  of  heat  production  of  rats  adapted  to  warm  (30°  C)  and  cold 
(5°  C)  environments.  According  to  Hart  &  Jansky,  1963 

^  Presented  at  the  40th  meeting  of  the  German  Mammalogical  Society  in  Amsterdam. 


489 


168 


L.  Jansky 


INSULATION   °C/CAL/mVhR 


CD 

o 

D 


o                          -^ 

— ^ 

o 

iC^ 

en                        o 

en 

r®-r— 

,      1      1      ,      ,      ,      .      1      ,      . 

1 

CD 

r- 

!>•     1— -o 

DEER    MOUSE 

>C 

•           0 

Co 
X3 

1  i 

•    ^^o       LEMMING 

o 

2 

-  o 

ft^tSe^         RED  SQUIRREL 

rn      rn 

- 

m^ooS)               MUSKRAT 

HARE 

•     «Oti^qd    fssss^'ss^'sssa 

RED  FOX 

-^ 

o 

•«•    ••               o    %o    oo 

WOLVERINE 

•     •        ••    aoo  #0 (K^ss^ir^K^^               u/r;/ /- 

o 

•     ••              •        •                                           00 

BLACK    BEAR 

••••        o^^^lt^^ 

POLAR    BEAR 

o 
o 
o 

- 

Fig.  2.  Seasonal  changes  in  fur  insulation  in  various  mammals  (Hart,  1956) 

(H  =  heat  production,  K  =  a  constant  representing  the  body  surface  area,  Tr  =  body 
temperature,  Ta  =  air  temperature,  I  =  insulation  qualities  of  the  body  surface.) 

Similary,  the  adaptations  of  temperature  regulation  to  cold  can  be  realized  either 
by  increasing  the  capacity  of  heat  production  or  by  mechanisms  leading  to  reduction 
of  heat  loss  from  the  body.  The  adaptation  to  cold  appears  as  a  shift  of  the  lowest 
temperature  limit  animals  can  survive  (lower  critical  temperature). 

In  our  earlier  work  we  have  shown  that  the  individual  adaptations  are  manifested 
predominantly  by  an  increased  capacity  of  heat  production  owing  to  the  development 
of  a  new  thermogenetic  mechanism  —  called  nonshiveringthermogenesis  (Hart,  Jansky 
1963).  Physiological  background  of  this  phenomenon  consists  in  an  acquired  sensitivity 
of  muscular  tissue  to  thermogenetic  action  of  noradrenaline  liberated  from  sympathetic 
nervous  endings  (Hsieh,  Carlson  1957).  Nonshivering  thermogenesis  potentiates  heat 
production  from  shivering  and  in  rats  shifts  the  lower  critical  temperature  for  about 
20°  C  (from  -18°  C  down  to  -  37°  C;  Fig.  1). 

Mechanisms  controlling  heat  loss  by  changes  in  body  surface  area  or  by  changes  in 
body-air  temperature  gradient  are  not  common  in  individual  adaptations.  On  the  other 
hand  it  is  well  known,  that  certain  species  can  improve  body  insulation  in  winter 


490 


Evolutionary  adaptations  of  temperature  regulation  in  mammals 


169 


season.  However,  this  phenomenon  becomes  functionally  justified  only  in  animals  of 
greater  size  (size  of  fox  and  larger;  Fig.  2.  Hart  1956). 

The  individual  adjustments  with  the  aid  of  nonshivering  thermogenesis  are  encoun- 
tered both  in  acclimations  under  laboratory  conditions  and  in  seasonal  acclimati- 
zations induced  in  the  same  species  under  natural  conditions.  They  are  undoubtelly 
very  efficient  and  biologically  important.  On  the  other  hand,  from  the  ecological  point 
of  view,  they  have  also  their  negative  side.  The  increased  heat  production  results  in 
higher  demands  for  energy  restitution  in  the  body,  which  is  attained  in  cold  adapted 
animals  by  an  increased  food  consumption.  As  a  result,  individuals  adjusted  this  way 
become  more  dependent  on  the  quantity  and  availability  of  food  and  they  are  forced 
to  use  more  effort  to  provide  it.  The  reduced  dependence  of  animals  on  temperature 
factors  is  thus  substituted  by  increased  dependence  on  food  factors. 

Contrary  to  individual  adaptations,  in  evolutionary  adaptations  mechanisms  lea- 
ding to  the  reduction  of  the  heat  loss  are  greatly  emphasized.  Their  importance  consists 
in  the  fact  that  they  save  energy  for  the  organism  and  have  lower  demands  to  its 
restitution  in  the  body.  This  fact  is  obviously  evolutionary  very  important  —  in  the 
processes  of  phylogeny  there  occurs  natural  selection  of  those  individuals  that  are  less 
impeded  by  the  lack  of  food,  often  occuring  in  nature. 

Evolutionary  adaptations  are  realized  in  the  first  place  by  an  increased  insulation 
of  the  body  cover  (fur.  Fig.  3).  This  adjustment,  typical  for  arctic  animals,  can  reduce 
the  heat  loss  so  efficiently,  that  even  considerably  reduced  ambient  temperatures  (down 
to  —  50^  C)  do  not  result  in  an  increased  heat  production  in  larger  animals.  (Fig.  4; 
ScHOLANDER  et  al.  1950a,  b).  The  same  role  plays  a  thick  layer  of  subcutaneous  fat 
which  appears  in  some  mammals,  such  as  seal  and  swine.  The  insulation  qualities  of  this 
fat  layer  can  be  increased  by  an  active  restriction  of  the  blood  flow  to  this  area.  This 
results  in  superficial  hypothermia,  which  also  efficiently  prevents  the  heat  loss  (Irving 
1956).  Animals  endowed  with  superficial  hypothermia  have  normal  thermogenetic 
abilities.  However,  compared  to  the  species  from  tropical  regions  with  little  insulation 
and  to  arctic  species  with  great  surface  insulation  they  show  a  reduced  sensitivity 
of  afferent  sensory  input  INSULATION 
to  temperature  stimuli 
(Fig.  5). 

A  tendency  to  reduce 
heat  loss  by  reduction  of 
the  body  surface  area 
may  be  considered  as 
another  type  of  evolutio- 
nary adaptations.  This 
phenomenon  occurs  in 
animals  living  perma- 
nently in  cold  climate, 
which  are  generally  lar- 
ger and  have  shorter  body 
appendages  than  animals 
from  tropical  zone(BERG- 
mann's  and  Allen's  ru- 
les). Both  the  validity  and 
the  physiological  signifi- 
cance of  these  rules  have  0  10  20  30  40  50  60  70 
been  recently  questionend  THICKNESS  IN  MM 
by  several  workers,  how-  pj^  j  Insulation  in  relation  to  winter  fur  thidtness  in  arctic 
ever.                                                          and  tropical  mammals  (Scholander  et  all.,  1950  b) 


P  COTTON 


40  r 


30  - 


491 


170 


L.  Jansky 


400 


300 
Co 
d  200 

S 

^  100 


MAMMALS 


ARCTIC 


TROPICAL 


BASAL    METABOLIC   RAIE  =   100 


■  OBSERVED 
EXTRAPOLATED 


-70  ^LOWEST     -50 
TEMP  ON  EARTH 


-30  -10  10 

AIR   TEMPERATURE  IN    "C 


^ 


30  / 

BODY    TEMP 


Fig.  4.  The  effect  of  environmental  temperature  on  metabolism  of  arctic  and  tropical  mammals 

(ScHOLANDER  et  all.,  1950  a) 


300 


-J 

5 

o  200 


5: 

O 

Uj 


SWINE 


INFANT 
CARIBOUo\° 

THICK-  FURRED   o' 
ANIMALS,    MAN 

WHITE  RAT 
MUSKRAT 


The  reduction  of  heat  loss  by  changing  the  body-air  temperature  gradient  can  be 
realized  either  by  active  choice  of  higher  environmental  temperature  or  by  consi- 
derable lowering  of  body  temperature. 

It  is  generally  recognized  that  the  active  choice  of  the  environmental  temperature 
occurs  by  seasonal  migrations  and  by  changes  in  patterns  of  daily  activity.  It  was 

found  that  different  species  of 
voles  and  shrews  transfer  the 
peak  of  daily  activity  to  war- 
mer part  of  the  day  in  a  cold 
weather  (Jansky  &  Hanak 
1959). 

The  mechanisms  leading  to 
reduction  of  body-air  tempera- 
ture gradient  by  lowering  of 
body  temperature  are  especially 
developed  in  hibernators.  Ac- 
cording to  the  latest  view  hiber- 
nation is  not  considered  as  a 
lack  of  temperature  regulation 
rather  as  a  special  adaptation  of 
thermogenetic  processes.  There 
are  two  reasons  for  that:  first, 
hibernators  have  the  same  capa- 
city of  heat  production  as  other 
hemeotherms  of  similar  size 
(see  Jansky,  1965)  and  second, 
the  entering,  the  arousal  and 
the  deep  hibernation  are  under 
remarkably  precise  physiological 
control  (see  Lyman,  1963). 

This  indicates  a  leading  role 
of  central  nervous  system  in 
controlling  hibernation,  which 
is  adapted  to  hypothermal  con- 


100 


0 


HARBOR  ( 
SEAL  ^•. 


HARPO 
SEAL  " 


GO 


0 


10 
SKIN 


20 
TEMP 


30 


Fig.  3.  Heat  production  as  a  function  of  skin  tempera- 
ture under  fur  of  the  back   for  a  series  of  mammals 
(Hart,  1963  a) 


492 


nfter  hexameihonium 


2/.0  nun. 


Evolutionary  adaptations  of  temperature  regulation  in  mammals  171 

ditions  and  it  is  functional  at  all  levels  of  body  temperature.  This  adaption  has  certainly 
its  metabolic  background,  however  only  little  is  known  about  this  phenomenon  so  far. 
The  control  of  entering  into  hibernation  is  realized  by  the  active  inhibition  of 
shivering  heat  production  by  signals  from  subcortical  centres  of  the  brain.  Simultane- 
ously with  the  decrease  in  shivering  an  active  inhibition  of  the  activity  of  the  sym- 
pathetic nervous  system  also  takes  place,  which  is  manifested  by  the  reduction  of  heart 
rate  and  by  vasodilatation.  These  changes  facilitate  the  lowering  of  body  temperature 
of  animals  which  is  realized  successively  in  the  form  of  "undulating"  cooling  so  the 
organism  can  slowly  prepare  to  hypothermia  (Fig.  6).  Nervous  control  of  hibernation 
persists  in  deep  hypo- 
thermia as  evident  from  ''c 
the  sensitivity  to  thermal 
and  other  stimuli.  The 
arousal  from  hibernation 
is  equally  an  active  pro- 
cess, very  efficiently  con- 
trolled, so  that  organism 
can     produce     a     great 

amount  of  heat  in  mini-  "^i^-i  ^  1  *  '"''"^' 

mum  of  time.  The  coordi- 
nation of  thermogenetic 
processes  depends  also  on 
the  activity  of  nervous 
centres.  Characteristic  or  fig,  (,_  Changes  in  body  temperature  of  the  bat  Myotis  myotis 
awakening  is  the  prepon-  during  entering  hibernation  (Jansky,  Hajek,  1961) 

derence    of    sympathetic 

nervous  system,  leading  to  vasoconstriction  and  to  an  increase  in  heart  rate.  The  main 
source  of  heat  in  awakening  is  again  constituted  by  shivering.  However,  nonshivering 
heat  production  was  also  found  during  arousal  and  also  the  rapidly  beating  heart, 
working  against  a  high  pressure,  may  contribute  a  certain  amount  of  heat. 


Summary 

On  the  basis  of  all  mentioned  data  we  conclude  that  the  adaptations  of  temperature  regula- 
tion to  cold  may  be  realized  either  by  an  increased  ability  to  produce  heat  or  by  reducing 
the  heat  loss.  While  the  individual  adaptations  are  manifested  chiefly  metabolically  as  evident 
from  an  Increased  capacity  of  heat  production,  the  Inherited  adaptations  are  realized  mainly 
by  mechanisms  leading  to  the  heat  loss  reduction  (e.  g.  Increased  Insulation  by  fur  or  by 
superficial  hypothermia,  reduction  of  body  surface  area,  active  choice  of  environmental  tem- 
perature and  lowering  the  body  temperature).  The  control  of  the  mentioned  adjustments  con- 
sists In  the  changes  In  function  of  the  central  and  sympathetic  nervous  systems  Inducing 
changes  In  intensity  of  the  energy  metabolism  (individual  adaptations),  changes  in  the  plasti- 
city of  vasomotor  medianlsms  and  In  heat  production  of  hibernators  during  entering  into 
and  awakening  from  hibernation  (evolutionary  adaptations).  Morphologically  based  adjust- 
ments (Improvement  of  insulation  by  fur)  appearing  in  both  evolutionary  and  individual 
adaptations  forms  the  connecting  link  between  both  types  of  adaptations. 


Zusammenfassung 

Aus  alien  erwahnten  Daten  folgern  wir,  dafi  die  Adaptatlonen  der  Temperaturregullerung 
bel  Kalte  entweder  durch  die  erhohte  Warmeproduktion  oder  durch  die  Verringerung  des 
Warmeverlustes  errelcht  werden.  Wiihrend  die  Indlviduellen  Adaptatlonen  hauptsachlich  meta- 
bollscher  Art  sind,  was  durch  die  erhohte  Kapazltat  der  Warmeproduktion  In  Erschelnung  tritt, 
findet  man  erbllche  Adaptatlonen  zumelst  in  Form  von  Mechanlsmen,  die  eine  Verringerung 
des  Warmeverlustes  bewlrken  (z.  B.  erhohte  Isollerung  durch  das  Fell  oder  durch  oberflachllche 


493 


172  L.  Jansky 

Hypothermic,  Verringerung  der  Korperoberflache,  aktive  Wahl  der  Umgebungstemperatur 
und  Abslnken  der  Korpertemperatur).  Die  Steuerung  der  erwahnten  Anpassungen  beruht  auf 
Veranderungen  in  der  Funktion  des  zentralen  und  des  sympathischen  Nervensystems,  welche 
Veriinderungen  in  der  Intensitat  des  Energiestoffwechsels  (individuelle  Adaptationen)  hervor- 
rufen,  weiterhin  Veranderungen  in  der  Plastizitat  der  vasomotorischen  Mechanismen  und  in  der 
Warmeproduktion  von  Winterschlafern  beim  Einritt  in  den  Winterschlaf  und  beim  Erwachen 
(evolutive  Adaptationen).  Morphologische  Adaptationen  (Verbesserung  der  Isolierung  durch 
das  Fell),  die  sowohl  als  evolutive  und  auch  als  individuelle  Adaptationen  vorkommen,  stellen 
die  Verbindung  zwischen  beiden  Typen  der  Adaptation  her. 

Literature 

Hart,  J.  R.  (1956):  Seasonal  changes  in  insulation  of  the  fur.  Can.  J.  Zool.  34:  53 — 57. 

—  (1963a):  Surface  cooling  versus  metabolic  response  to  cold.  Fed.  Proc.  22:  940 — 943. 

—  (1963b):  Physiological  responses  to  cold  in  nonhibernating  homeotherms.  Temperature  — 
Its  Measurements  and  Control  in  Science  and  Industry  3:  373 — 406. 

Hart,  J.  S.,  and  Jansky,  L.  (1963):  Thermogenesis  due  to  exercise  and  cold  in  warm  and  cold 
acclimated  rats.  Can.  J.  Biochem.  Physiol.  41:  629 — 634. 

HsiEH,  A.  C.  L.,  and  Carlson,  L.  D.  (1957):  Role  of  adrenaline  and  noradrenaline  in  chemical 
regulation  of  heat  production.  Amer.  J.  Physiol.  190:  243 — 246. 

Irving,  L.  (1956):  Physiological  insulation  of  swine  as  bare-skinned  mammals.  J.  Appl.  Phy- 
siol. 9:  414— 420. 

Jansky,  L.  (1965):  Adaptability  of  heat  production  mechanisms  in  homeotherms.  Acta  Univ. 
Carol.-Biol.  1—91. 

Jansky,  L.,  and  Hajek,  I.  (1961):  Thermogenesis  of  the  bat  Myotis  myotis  Borkh.  Physiol. 
Bohemoslov.  10:  283—289. 

Jansky,  L.,  and  Hanak,  V.  (1959):  Studien  iiber  Kleinsaugerpopulationen  in  Siidbohmen.  II. 
Aktivitat  der  Spitzmause  unter  natUrlichen  Bedingungen.  Saugetierkundliche  MItteilungen 
8:  55—63. 

Lyman,  C.  P.  (1963):  Homeostasis  in  Hibernation.  Temperature  —  Its  Measurement  and 
Control  in  Science  and  Industry  3:  453 — 457. 

Scholander,  p.  F.,  Hock,  R.,  Walters,  V.,  Johnson,  P.,  and  Ikving,  L.  (1950a):  Heat  regu- 
lation in  some  arctic  and  tropical  mammals  and  birds.  Biol.  Bull.  99:  237 — 271. 

Scholander,  P.  P.,  Walters,  V.,  Hock,  R.,  and  Irving,  L.  (1950b):  Body  insulation  of  some 
arctic  and  tropical  mammals  and  birds.  Biol.  Bull.  99:  225 — 236. 

Author's  address:  L.  Jansky,  Ph.  D.,  Department  of  Comparative  Physiology,  Charles  Uni- 
versity, Prague  2,  VInicna  7,  CSSR 


494 


SECTION  6— ZOOGEOGRAPHY  AND  FAUNAE  STUDIES 

Studies  of  faunas,  both  of  local  areas  and  of  broad  regions,  have  contributed 
substantially  to  the  literature  in  mammalogy.  From  the  earliest  contributions 
to  the  present,  papers  and  books  dealing  with  faunistics  have  included  much 
information  on  systematics,  ecology,  distribution,  ethology,  and  reproduction, 
among  other  topics.  The  sobriquet  "natural  historian"  implied  an  interest  in 
all  these  fields  and  more. 

Darlington's  (1957)  book  Zoogeography  and  Udvardy's  (1969)  Dynamic 
Zoogeography  are  the  best  single  sources  of  general  information  on  the  sub- 
ject; Hesse  et  al.  ( 1937 )  is  a  substantial  and  still  useful  earlier  reference. 
Insular  biogeography  was  aptly  dealt  with  by  Carlquist  ( 1965 )  and  in  a  more 
mathematically-oriented  way  by  MacArthur  and  Wilson  (1967).  Matthew's 
(1939)  Climate  and  Evolution  and  Dice's  (1952)  Natural  Communities  are 
but  two  of  the  other  general  treatises  that  should  be  called  to  the  attention  of 
the  beginning  student. 

Among  the  major  f aunal  catalogues  are  Allen  ( 1939 )  for  Africa,  Ellerman 
and  Morrison-Scott  (1951)  for  the  Palearctic  Region,  Miller  and  Kellogg 
(1955)  and  Hall  and  Kelson  (1959)  for  North  America,  Cabrera  (1958,  1961) 
for  South  America,  and  Troughton  (1965)  for  Australia.  At  the  regional  or 
provincial  level,  Kuroda's  (1940)  treatment  of  Japanese  mammals,  Laurie  and 
Hill  (1954)  on  New  Guinea  and  the  Celebes,  and  Peterson's  (1966)  The  Mam- 
mals of  Eastern  Canada  are  good  examples  as  are  many  of  the  state  lists  pub- 
lished for  North  America  (e.g.,  DeKay,  1842;  Miller,  1899;  Hall,  1946;  Jackson, 
1961;  Baker  and  Greer,  1962;  Jones,  1964),  of  which  Hall's  Mammals  of  Nevada 
stands  out  in  completeness  of  coverage  from  most  points  of  view.  In  terms  of 
smaller  geographic  areas,  Harper  ( 1927 )  on  the  Okefinokee  Swamp,  Johnson 
et  al.  (1948)  on  the  Providence  Mountains  of  California,  Anderson  (1961)  on 
the  Mesa  Verde  of  Colorado,  and  Foster's  ( 1965)  study  of  the  Queen  Charlotte 
Islands  illustrate  that  substantial  information  can  be  gleaned  from  the  study  of 
a  geographically  restricted  fauna.  These  papers  as  well  as  several  reproduced 
here  certainly  indicate  that  the  serious  student  of  faunistics  must  be  as  broadly 
trained  as  any  student  in  the  discipline  of  mammalogy. 

Because  of  the  sustained  interest  in  faunal  studies  over  the  years,  it  was 
inevitable  that  certain  "rules,"  "laws,"  and  "systems" — directed  at  overall 
explanations  for  natural  phenomena  associated  with  distribution  and  variation 
— would  emerge.  These  have  been  of  two  basic  sorts,  various  "ecological  rules" 
such  as  those  proposed  by  Allen,  Bergmann,  and  Gloger,  and  the  biogeographic 
systems  proposed  on  a  world-wide  scale  by  Wallace  and  others  and  ap- 
plied more  specifically  to  North  America  by  Merriam  (Life-zones),  Shelford 
( Biomes ) ,  and  Dice  ( Biotic  Provinces ) .  Space  does  not  permit  the  reproduc- 
tion of  the  lengthy  papers  dealing  with  these  subjects,  but  a  short  contribution 
by  Dice,  which  is  included,  serves  to  introduce  the  reader  to  this  aspect  of 
mammalian  zoogeography. 

Other  selections  for  this  section  deal  with  zoogeographic  problems  related 
to  Pleistocene,  sub-fossil,  and  Recent  faunas  (Guilday,  Koopman  and  Martin, 
and  Findley  and  Anderson).    One  paper  concerns  a  local  fauna  (Jones  and 


495 


Lawlor )  but  also  includes  information  relevant  to  other  sections  of  this  anthol- 
ogy. The  essay  by  Davies  covers  an  entire  order  (or  suborder  according  to 
many  other  authors )  of  mammals,  whereas  the  short  paper  by  Davis  deals  with 
the  relationship  of  soil  types  and  altitude  to  the  distribution  of  a  single  species 
in  a  restricted  area.  The  final  paper  is  a  statistical  treatment  by  Hagmeier  of 
distributional  patterns  on  a  continental  basis.  This  analysis  is  based  on  data 
compiled  in  one  of  the  faunal  catalogues  (Hall  and  Kelson)  cited  above. 


496 


THE  CANADIAN  BIOTIC  PROVINCE  WITH  SPECIAL 
REFERENCE  TO  THE  MAMMALS 

Lee  R.  Dice 
University  of  Michigan 

In  eastern  North  America  many  zoogeographers  recognize  six  life  zones, 
all  assumed  to  be  transcontinental  in  extent  and  named,  respectively,  Arctic 
(or  Arctic-alpine).  Hudsonian,  Canadian,  Transition,  Upper  Austral,  and 
Lower  Austral  (Merriam,  '98:  18-53).  The  AUeghanian,  Carolinian,  and 
Austroriparian  faunas  are  the  eastern  portions,  respectively,  of  the  Transi- 
tion, Upper  Austral,  and  Lower  Austral  life  zones.  In  addition,  some 
zoogeographers  recognize  a  Tropical  region  which  covers  the  southern  part 
of  Florida. 

Ecologists,  on  the  contrary,  divide  eastern  North  America  somewhat 
differently.  Shelford,  Jones,  and  Dice  ('26:  60-73)  recognized  here  the 
Arctic  Tundra,  Northern  Coniferous  Forest,  Mixed  Coniferous  and  De- 
ciduous Forest,  Deciduous  Forest,  and  Southeastern  Coniferous  Forest  biotic 
areas.  Weaver  and  Clements  ('29,  frontis)  divide  the  eastern  part  of  the 
continent  among  the  Tundra,  Boreal  Forest,  Lake  Forest,  Deciduous  Forest, 
and  Tropical  climaxes. 

There  is  rather  general  agreement  among  biogeographers  on  the  im- 
portance of  the  Tundra  (Arctic)  and  Boreal  Forest  (Hudsonian)  divisions. 
Also  most  students  of  distribution  would  accept  the  Southeastern  Coniferous 
Forest  (Austroriparian)  as  at  least  a  minor  unit.  On  the  other  hand,  there 
is  little  agreement  on  the  biogeographical  division  of  the  remaining  middle 
portion  of  eastern  North  America. 

In  order  to  examine  the  several  biotic  provinces  of  northeastern  North 
America  I  drove  by  automobile  in  the  summer  of  1936  through  considerable 
parts  of  eastern  Canada  and  of  the  northeastern  United  States.  The  observa- 
tions made  on  this  trip  and  a  subsequent  study  of  the  available  descriptions  of 
the  vegetation  and  faunas  of  the  area  have  convinced  me  that  the  so-called 
Canadian  and  AUeghanian  faunas  are  only  different  aspects  of  the  same  eco- 
logical complex.  The  name  Canadian  is  more  descriptive  of  this  complex 
than  is  the  name  AUeghanian,  and,  therefore,  the  term  Canadian  biotic  prov- 
ince is  here  adopted  for  that  part  of  northeastern  North  America  in  which 

503 


497 


LEE   R.    DICE 


Ecology,  Vol.  19,  No.  4 


Fig.  1.     Map  of  eastern  North  America  showing  the  distribution  of  the  several  biotic 

provinces. 


498 


October,  1938  CANADIAN   BIOTIC   PROVINCE  505 

hardwoods  form  the  climax  and  conifers  of  several  kinds  form  several  types 
of  subclimaxes.  A  biotic  province  is,  according  to  my  definition,  a  major 
biogeographic  division  of  a  continent,  characterized  by  the  biotic  communi- 
ties which  compose  it. 

The  Canadian  biotic  province  as  here  recognized  (fig.  1)  covers  much 
of  southern  Quebec,  including  the  Gaspe  Peninsula,  and  all  of  New  Bruns- 
wick, Nova  Scotia,  and  the  adjacent  islands.  It  extends  southward  to  include 
much  of  New  England,  most  of  New  York  state,  and  the  mountainous  parts 
of  Pennsylvania.  It  covers  Michigan  and  Wisconsin,  except  their  southern 
parts;  the  northeastern  half  of  Minnesota;  and  all  of  southern  Ontario, 
except  along  Lake  Erie.  The  province  is  in  my  interpretation  not  trans- 
continental, although  there  are  some  similarities  between  its  biota  and  that 
of  the  western  mountains. 

An  excellent  description  of  the  vegetation  of  the  Canadian  biotic  province 
has  been  given  by  Nichols  ('35:  403-422)  under  the  designation  Hemlock — 
white  pine — northern  hardwood  region.  Nichols,  however,  includes  the 
southern  Appalachian  Mountains  in  his  region,  while  I  consider  it  better  to 
include  these  mountains  in  the  Carolinian  biotic  province,  by  which  they  are 
surrounded. 

The  western  end  of  the  northern  boundary  of  the  Canadian  province 
should  in  my  opinion  be  placed  a  little  north  of  the  position  given  by  Nichols 
('35,  fig.  4),  so  as  to  include  all  the  important  stands  of  sugar  maple,  white 
pine,  and  Norway  (red)  pine  (see  Howe  and  Dymond,  '26:  288-291).  An 
unpublished  study  of  the  plant  ecology  of  Isle  Royale  by  Clair  A.  Brown 
shows  that  there  are  considerable  stands  of  sugar  maple  forest  on  this  island, 
which  lies  in  the  northern  part  of  Lake  Superior.  The  northernmost  im- 
portant stands  of  sugar  maple  and  white  pine  observed  by  me  along  the  road 
between  North  Bay  and  Cobalt,  Ontario,  were  about  50  miles  north  of  North 
Bay,  on  the  rocky  ridges  of  the  Timagami  Provincial  Forest. 

A  second-growth  forest  of  white  spruce  and  pine  was  studied  at  James 
Lake,  11  miles  south  of  Latchford,  or  about  66  miles  by  road  north  of  North 
Bay.  This  forest  was  growing  on  moderately  high  rolling  rocky  hills,  and 
the  soil,  while  often  thin,  contained  much  humus.  White  birch  was  the  most 
common  tree,  and  balsam  fir,  black  ash,  and  aspen  were  numerous.  There 
were  a  few  small  white  and  Norway  pines,  and  a  few  of  a  species  of  poplar 
with  long  leaves.  A  maple  (Acer  spicatum)  was  the  most  common  shrub. 
Signs  of  snowshoe  hare  were  numerous,  and  red  squirrels  and  chipmunks 
(Taniias)  were  seen.  Ten  red-backed  voles  {Clethrionomys  gafferi  gafferi 
and  1  deer-mouse  {Peromyscus  maniculatus  gracilis)  were  trapped  on  a 
short  trap-line.  This  situation  obviously  is  transitional  between  the  Hud- 
sonian  and  Canadian  provinces. 

The  transition  between  the  Canadian  and  Hudsonian  provinces  is  in  some 
places  rather  abrupt.  On  the  northern  margins  of  their  ranges  the  sugar 
maple,  yellow  birch,  and  white  pine  occur  only  in  the  most  favorable  habitats 


499 


506  LEE    R.    DICE  Ecology,  Vol.  19,  No.  4 

and  a  slight  change  in  topography  or  soil  may  make  it  impossible  for  these 
Canadian  province  species  to  exist. 

As  an  example  of  a  fairly  abrupt  transition  I  submit  herewith  two  logs 
of  the  vegetation  observed  in  the  summer  of  1936  along  the  highway  in  two 
parts  of  northern  Ontario.  The  distance  each  type  of  forest  was  traversed 
by  the  highway  was  determined  by  readings  of  the  automobile  mileage  meter 
at  each  change  in  vegetation.  The  figures  given  cannot  be  assumed  to  be  a 
dependable  measure  of  the  proportionate  occurrence  of  the  several  vegetation 
types  in  the  two  regions,  because  the  highway  undoubtedly  avoids  the  steeper 
rocky  slopes  and  at  least  the  more  widespread  of  the  bogs.  Nevertheless,  the 
figures  do  give  a  general  indication  of  the  relative  abundance  of  the  several 
ecologic  types  in  the  two  situations. 

The  stretch  of  highway  logged  in  the  Canadian  province  extends  from 
10  miles  north  of  North  Bay,  Ontario,  to  a  point  10  miles  further  north. 
The  road  here  crosses  a  number  of  rocky  ridges,  and  the  general  exposure  is 
to  the  south.  In  the  10  miles  of  the  log  72  per  cent  is  dominated  by  forests 
of  sugar  maple,  yellow  birch,  and  white  pine.  Bogs,  in  which  black  spruce 
was  most  conspicuous,  cover  22  per  cent  of  the  distance.  In  these  bogs  there 
occur  also  some  balsam  fir  and  some  tamarack.  Burns  and  badly  mixed 
vegetation  cov^  6  per  cent  of  the  recorded  distance.  Much  of  the  maple 
forest  along  t1ie  highway  has  been  logged,  and  part  of  both  the  upland  forest 
and  of  the  bogs  has  been  burned. 

For  contrast,  there  is  available  the  log  of  the  dominant  vegetation  along 
the  highway  from  Cochrane  south  nearly  to  Swastika,  a  distance  of  94.7 
miles,  all  in  the  Hudsonian  province.  The  black  spruce  type  of  vegetation 
formed  the  original  cover  for  49  per  cent  of  this  distance.  Much  of  this 
black  spruce  occurs  in  lowland  bogs  called  muskegs,  and  these  muskegs  are 
especially  extensive  on  the  nearly  flat  plain  near  Cochrane.  A  few  balsam 
firs  occur  with  the  black  spruce  at  least  as  far  north  as  Cochrane,  and  in  the 
better  drained  situations  the  white  spruce  also  occurs.  Sphagnum  forms  a 
heavy  mat  under  the  spruces  and  Labrador  tea  is  a  characteristic  low  shrub. 
Near  Cochrane  the  black  spruce  type  of  bog  vegetation  is  not  restricted 
to  low  and  undrained  situations,  but  extends  also  over  the  lower  hills. 
Another  important  type  of  vegetation  between  Cochrane  and  Swastika  is 
the  jack  pine  forest,  which  covers  11  per  cent  of  the  log.  This  forest 
type  is  restricted  to  sandy  areas.  Associated  with  the  jack  pine  are  fre- 
quently the  aspen,  the  black  and  the  white  spruces,  and  less  commonly 
the  white  birch.  Blueberries  are  a  characteristic  low  shrub.  Fires  have  been 
frequent  in  this  region  and  26  per  cent  of  the  distance  between  the  two  cities 
is  dominated  by  aspen.  Mixed  types  of  vegetation  of  various  sorts,  includ- 
ing arbor  vitae,  black  spruce,  alder,  willow,  aspen,  balsam  fir,  white  spruce, 
jack  pine,  and  white  birch  made  up  11  per  cent  of  the  vegetation.  Clearings 
in  which  the  original  type  of  vegetation  could  not  be  determined  from  the 
road  cover  3  per  cent  of  the  distance. 


500 


October,  1938  CANADIAN   BIOTIC   PROVINCE  507 

Although  the  sections  of  highway  described  above  in  the  Canadian  and 
Hudsonian  provinces,  respectively,  are  only  about  150  miles  apart  at  their 
nearest  approach,  there  are  very  obvious  differences  in  their  vegetation.  In 
the  Hudsonian  province  near  Cochrane  the  sugar  maple,  yellow  birch,  and 
white  pine  type  of  forest  characteristic  of  the  Canadian  province  is  absent, 
while  the  spruce  bog  is  the  most  extensive  community.  Climatic  differences 
related  to  latitude  are  probably  in  large  part  responsible  for  these  dissimi- 
larities in  vegetation.  However,  the  soil  characters  of  the  two  regions  are 
very  different  and  these  variations  in  soil  greatly  affect  the  vegetation. 

The  rocky  ridges  10  to  20  miles  north  of  North  Bay  are  probably  at 
nearly  the  northern  limit  of  the  forest  of  sugar  maple,  yellow  birch,  and 
white  pine,  and  it  is  doubtful  if  this  type  of  forest  could  exist  at  Cochrane 
even  on  rocky  slopes.  On  the  other  hand,  the  general  lack  of  jack  pine 
along  the  highway  near  North  Bay  is  obviously  due  to  the  absence  of  sandy 
soil  in  this  area,  for  jack  pine  forest  is  an  important  vegetation  type  on  sandy 
soils  much  further  south. 

North  of  Quebec  sugar  maples  occur  on  the  southern  slopes  of  the 
mountains  of  the  Laurentides  National  Park,  but,  so  far  as  could  be  seen 
on  a  hasty  drive  through  this  park,  all  the  higher  parts  of  the  mountains  are 
dominated  by  spruce  forest  (see  also  Fuller  and  Marie- Victorin,  '26:  295- 
296).  On  the  northern  slopes  of  these  mountains,  toward  Lake  St.  John, 
sugar  maples  reappear,  and  numbers  of  these  trees  were  noted  near  Abbey- 
ville.  The  position  of  the  boundary  between  the  Hudsonian  and  Canadian 
in  this  region  must  therefore  be  drawn  somewhat  arbitrarily. 

The  tip  of  the  Gaspe  Peninsula  has  been  excluded  by  Nichols  from  the 
Hemlock  region  (Canadian  province).  It  is  true  that  the  high  interior  parts 
of  the  peninsula  would  be  expected  to  be  dominated  by  spruce  forests.  How- 
ever, along  the  northeastern  Gaspe  coast,  on  crossing  a  ridge  several  hundred 
feet  high  between  the  villages  of  Chloridorme  and  Gaspe,  I  noted  the  occur- 
rence of  a  few  white  pines  and  sugar  maples,  along  with  fir.  spruce,  arbor- 
vitae.  aspen,  white  birch,  and  mountain  ash.  Several  kinds  of  mammals 
reach  their  northern  limits  in  the  Gaspe  peninsula,  and  probably  occur  over 
most  of  the  peninsula.  It  therefore  is  much  simpler  for  the  mammalogist 
if  all  the  peninsula  is  included  in  the  same  province.  I  have  for  this  reason 
drawn  the  northern  boundary  of  the  Canadian  province  down  the  middle  of 
the  Bay  of  St.  Lawrence. 

The  southern  boundary  of  the  Canadian  province  in  the  Appalachian 
Mountains  is  difficult  to  place,  because  isolated  areas  of  northern  type  forests 
and  fauna  recur  on  the  Appalachian  Mountains  south  as  far  as  North  Caro- 
lina and  Tennessee.  I  have  here  arbitrarily  drawn  the  southern  boundary 
of  the  Canadian  province  at  the  southern  border  of  the  state  of  Pennsylvania. 
It  is,  however,  quite  possible  that  a  more  natural  division  between  the  north- 
ern and  southern  Appalachian  Mountains  may  occur  somewhere  in  West 
Virginia. 


501 


508  LEE  R.  DICE  Ecology,  Vol.  19,  No.  4 

The  climax  vegetation  of  the  Canadian  province  is  a  hardwood  forest,  in 
which  the  sugar  maple  (Acer  sacchanim)  and  yellow  birch  (Betula  lutea) 
are  the  most  characteristic  trees.  The  eastern  white  pine  (Pinus  strobus)  and 
the  eastern  hemlock  (Tsuga  canadensis)  occur  frequently.  The  beech  {Fagus 
grandifolia)  is  also  characteristic,  except  that  it  does  not  occur  in  the  extreme 
western  part  of  the  province.  Numerous  other  trees  and  many  shrubs  are 
characteristic.  The  Canadian  province  therefore  corresponds  closely  to  the 
"northern  hardwood  forest"  of  some  foresters  (Frothingham,  '15:  1-7). 

The  pines  {Pinus  strobus,  P.  resinosa,  and  P.  divaricata) ,  often  growing 
in  a  pure  stand  of  one  species,  are  in  many  places  an  important  subclimax  stage 
in  the  Canadian  province.  The  pine  forests  nearly  always  occupy  sandy  or 
gravelly  soil.  On  some  very  poor  sandy  soils  the  pine  forest  may  persist 
indefinitely  as  an  edaphic  climax,  for  in  such  situations  insufficient  humus 
may  accumulate  ever  to  make  the  site  suitable  for  a  hardwood  forest.  On 
good  soil  the  pines  are  usually  quickly  succeeded  and  shaded  out  by  hard- 
woods, although  the  white  pine  often  persists  in  the  climax  forest.  Some 
of  the  white  pine  trees  in  the  climax  forest  may  be  relicts  of  an  earlier  pine 
stage,  persisting  by  reason  of  their  height,  but  some  probably  spring  up  from 
time  to  time  in  openings  in  the  forest  produced  by  the  fall  of  large  trees. 

In  poorly  drained  situations  in  the  Canadian  province,  many  areas  are 
covered  by  bogs  and  swamps  in  which  there  occur  varying  mixtures  of 
balsam  fir  {Abies  balsamea),  black  spruce  {Picea  mariana),  white  spruce 
{Picea  canadensis) ,  northern  white  cedar  {Thuja  occidentalis) ,  and  tamarack 
{Larix  laricina),  with  occasional  hardwoods  such  as  black  ash  and  red  maple. 
As  pointed  out  by  Nichols  ('35:  411-412)  these  bogs  and  swamps  "closely 
resemble  the  climatic  climax  of  the  northern  conifer  forest  region,"  which 
here  is  called  the  Hudsonian  province. 

Following  fires  in  the  forest  of  the  Canadian  province  there  often  springs 
up  a  first  forest  of  aspen  {Populus  tremuloides  and  P.  grandidentata)  or  of 
white  birch  {Be tula  papyrifera).  The  aspens  and  birches  are  usually  fol- 
lowed by  pines. 

In  northern  Michigan,  if  hardwood  forest  on  clay  soil  is  destroyed  by 
fire,  there  may  be  no  complete  succession  through  aspens  and  pines,  but  at 
least  in  some  situations  the  hardwood  forest  regenerates  directly  after  a 
brushy  stage,  and  the  aspen  and  pines  stages  are  omitted. 

Sandy  soils  and  also  poorly  drained  situations  occur  over  nearly  the  whole 
area  of  the  Canadian  province,  alternating  irregularly  with  good  soils  and 
with  well  drained  situations.  In  some  districts  hundreds  or  thousands  of 
square  miles  may  be  covered  mostly  with  sandy  soil,  with  accompanying  pine 
forests.  In  other  places  equal  areas  of  poorly  drained  soil  may  support 
forests  of  spruces  and  firs.  Nevertheless,  on  the  better  soils  throughout 
this  whole  area  the  northern  hardwood  type  of  forest  natively  formed  the 
characteristic  vegetation,  and  it  certainly  is  the  ultimate  climax  for  the 
climate.     The  firs  and  pines  which  have  been  assumed   to  distinguish  the 


502 


October,  1938  CANADIAN    BIOTIC    PROVINCE  509 

Alleghanian  biota  from  the  Canadian  biota  are  actually  successional  stages 
which  mostly  are  characteristic  only  of  certain  soil  types.  These  soil  types 
and  their  accompanying  coniferous  vegetation  recur  throughout  most  of  the 
area  which  has  been  called  Alleghanian  as  well  as  over  the  area  previously 
assigned  to  the  Canadian. 

Spruce  forests  occur  on  the  upper  parts  of  mountains  and  in  lowland 
bogs  over  most  of  the  Canadian  province  and  also  even  in  parts  of  the 
Carolinian  province.  The  fauna  and  flora  of  these  isolated  spruce  habitats 
resemble  in  part  the  fauna  and  flora  of  the  Hudsonian  province.  Neverthe- 
less, it  is  futile  to  attempt  to  mark  on  the  map  every  local  spruce  habitat. 
In  my  opinion  it  is  better  to  treat  these  isolated  habitats  as  minor  communi- 
ties of  the  province  in  which  they  occur.  Actually  these  isolated  spruce 
communities  are  never  exactly  like  the  major  communities  of  the  Hudsonian 
province,  which  they  resemble  superficially,  for  most  or  all  of  the  larger 
Hudsonian  mammals  are  missing. 

No  attempt  will  here  be  made  to  consider  all  of  the  kinds  of  animals 
which  are  characteristic  of  the  Canadian  biotic  province.  In  this  report  I 
shall  confine  my  attention  entirely  to  the  mammals,  the  group  of  animals 
with  which  I  am  most  familiar.  However,  it  is  known  that  some  other 
classes  of  land  vertebrates  and  some  kinds  of  invertebrates  also  are  restricted 
in  distribution  by  some  of  the  same  ecological  barriers  as  are  the  mammals. 

In  making  up  the  lists  of  mammals  I  have  followed  in  general  the  nomen- 
clature of  Miller  ('24).  For  data  on  the  distribution  of  the  several  species 
I  have  used  such  revisions  as  are  available,  chiefly  in  the  valuable  North 
American  Fauna  series  prepared  by  the  United  States  Biological  Survey. 
Unfortunately,  many  species  and  genera  have  not  been  recently  revised  and 
the  distribution  of  some  species  has  never  been  adequately  mapped.  For 
records  of  the  distribution  of  many  of  the  ungulates  and  larger  carnivores 
I  have  depended  chiefly  upon  the  maps  presented  by  Seton  ('29). 

The  following  species  of  mammals  range  over  most  or  all  of  the  Canadian 
province  as  I  have  defined  it:  Condylura  cristata  (Star-nosed  mole),  Sorex 
cinereiis  (Masked  shrew),  Sorcx  palustris  (Water  shrew),  Microsorex  Jioyi 
(Pigmy  shrew),  Blarina  hrevicauda  (Short-tailed  shrew),  Myotis  lucifngus 
(Little  brown  bat),  Myotis  kecnii  (Little  brown  bat),  Lasionycteris  nncti- 
vagans  (Silver-haired  bat),  Eptesicus  fuscus  (Large  brown  bat),  Lasiurus 
borealis  (Red  bat),  Ursiis  americanus  (Black  bear),  Procyon  lotor  (Rac- 
coon), Maries  americana  (Marten),  Maries  pennanii  (Fisher),  Musiela  vison 
(Mink),  Musiela  cicognanii  (Short-tailed  weasel),  Musiela  frenata  (Long- 
tailed  weasel),  Gulo  luscus  (Wolverine),  Luira  canadensis  (Otter),  Mephiiis 
mephitis  (Striped  skunk),  Vulpes  fulva  (Red  fox),  Canis  lycaon  (Timber 
wolf),  Lynx  canadensis  (Canada  lynx),  Marniota  monax  (Woodchuck), 
Taniias  striaius  (Chipmunk),  Sciurus  hudsonicus  (Chickaree),  Glaucomys 
sabrinus  (Flying-squirrel),  Castor  canadensis  (Beaver),  Peromyscus  nianicu- 
laius    (Deer-mouse),    Synaptomys   cooperi    (Bog-lemming),    Clethrionomys 


503 


510  LEE  R.  DICE  Ecology,  Vol.  19,  No.  4 

gapperi  (Red-backed  vole),  Microtus  pennsylvanicus  (Meadow-vole),  On- 
datra sibctJiica  (Muskrat),  Zapus  Jindsonius  (Meadow  jumping-mouse), 
Napaeozapus  insignis  (Woodland  jumping-mouse),  Ercthizon  dorsatum 
(Porcupine),  Lcpus  americanus  (Snowshoe  hare),  OdocoUcus  virginianus 
(White-tailed  deer),  Alces  amcricana  (Moose). 

Of  these  species  the  masked-shrew,  silver-haired  bat,  black-bear,  fisher, 
mink,  otter,  red-fox.  wolf,  chickaree,  beaver,  deer-mouse,  meadow-vole, 
muskrat,  and  meadow  jumping-mouse  (Zapus)  ranged  natively  over  most 
or  all  of  the  Hudsonian  of  eastern  Canada  as  well  as  over  the  Canadian,  and 
all  of  them  also  extended  into  biotic  provinces  south  of  the  Canadian.  These 
then  are  wide-ranging  forms  which  extend  beyond  the  Canadian  province 
on  both  sides. 

A  few  species  which  are  mainly  of  more  northern  distribution  ranged 
south  natively  into  the  northern  part  of  the  Canadian.  These  are  the  Arctic 
shrew  {Sorcx  arcticus),  wolverine,  northern  lemming-vole  (Syuaptomys 
horcalis),  heather-vole  (Pliciiacoinys  uiigava),  and  caribou  (Rangifer  cari- 
bou). Most  of  these  forms  are  rare  in  the  Canadian  and  for  the  larger 
forms  the  original  southward  distribution  in  eastern  North  America  is  not 
well  known.  However,  probably  none  of  them  originally  extended  as  far 
south  as  the  southern  boundary  of  the  Canadian  province. 

Species  which  ranged  natively  over  most  of  the  Hudsonian  of  eastern 
Canada  and  which  in  eastern  North  America  reached  their  southern  limits 
near  the  southern  border  of  the  Canadian  as  here  mapped  are  the  marten, 
short-tailed  weasel,  Canada  lynx,  northern  flying-squirrel  (Glaucomys  sa- 
brinus),  red-backed  vole,  porcupine,  and  snowshoe  hare. 

The  moose  seems  to  have  been  the  only  form  which  was  limited  in  its 
southward  distribution  in  eastern  North  America  by  the  southern  border  of 
the  Canadian  province  as  here  mapped,  and  which  also  ranged  into  the 
southern  part  only  of  the  Hudsonian  province. 

The  pigmy-shrew  (Microsorex)  is  rare  and  its  distribution  not  well 
known.  Although  it  seems  to  occur  mostly  in  the  Hudsonian  and  Canadian 
provinces  it  also  occurs  in  other  areas  to  the  southward  and  westward. 

The  hoary  bat  (Lasiunis  ciucrca)  occurs  in  the  Canadian  province,  and 
is  at  least  in  part  a  migrant,  breeding  farther  north  as  well  as  farther  south. 

Species  which  range  from  districts  south  of  the  Canadian  province  north 
across  the  whole  Canadian  and  into  the  southern  part  of  the  Hudsonian 
province  are  the  little  brown  bat  (Myotis  lucifugus),  striped  skunk,  and 
woodchuck. 

Species  of  more  southern  distribution  which  reach  their  northern  limits 
at  or  close  to  the  northern  boundary  of  the  Canadian  province  are  the  short- 
tailed  shrew,  little  brown  bat  (Myotis  keenii),  large  brown  bat,  red-bat, 
raccoon,  long-tailed  weasel,  chipmunk  (Tatnias),  Lemming-vole  (Synaptomys 
cooperi),  and  white-tailed  deer.  The  deer  is  now  extending  its  range  further 
northward. 


504 


October,  1938  CANADIAN    BIOTIC    PROVINCE  511 

Species  wliich  mainly  arc  of  more  southern  distribution  but  which  natively 
ranged  into  some  of  the  southern  parts  of  the  Canadian  province  are  the  mole 
(Scalopus  aquaticiis),  pipistrelle  {Pipistrellus  suhflavus),  gray-fox  (Urocyon 
cinercoargoitcus),  cougar  (Fclis  couguar),  bob-cat  (Lynx  rufus),  gray- 
squirrel  (Sciurus  caroli)ieusis),  fox-squirrel  (Sciitrus  nigcr),  flying-squirrel 
(Glaucomys  volans),  wood-mouse  (Peromyscus  Icucopus),  American  elk 
{Cervus  canadensis),  and  bison  (Bison  bison).  In  southern  Michigan  the 
mole,  fox-squirrel,  and  wood-mouse  were  probably  originally  mostly  absent 
from  the  Canadian  province,  but  with  the  clearing  of  the  forests  they  have 
extended  their  ranges  some  distance  into  the  province.  The  bob-cat  has  in 
Michigan  in  historic  time  greatly  extended  its  range  northward. 

The  star-nosed  mole  and  woodland  jumping-mouse  (Napaeosapus)  cover 
most  of  the  area  of  the  Canadian  province  and  both  extend  south  in  suitable 
habitats  along  the  Appalachian  Mountains.  In  addition  both  also  extend 
slightly  beyond  the  limits  of  the  province  in  other  directions. 

Several  species  of  mammals  occupy  part  only  of  the  Canadian  province 
and  also  range  south  into  the  Carolinian  province  along  the  Appalachian 
Mountains.  These  are  the  hairy-tailed  mole  (Parascaiops  breweri),  smoky- 
shrew  (Sorcx  fuiiieus),  another  shrew  (Sorcx  dispar),  woodrat  (Neotoma 
pennsylvanica) ,  rock-vole  (Microtus  chrotorrhinus) ,  and  New  England  cot- 
tontail (Sylvilagus  transitionalis) . 

Several  species  which  are  mostly  more  western  in  distribution  range 
into  the  western  parts  of  the  Canadian  province.  These  are  the  least-weasel 
(Mustcla  rixosa),  badger  (Taxidea  taxus),  coyote  (Canis  lafrans),  western 
chipmunk  (Eutamias  minimus),  and  cottontail  (Sylvilagus  floridanus) .  Of 
these  the  coyote  has  within  recent  time  considerably  extended  its  range  east- 
ward. The  cottontail  seems  not  to  have  originally  occurred  in  the  Canadian 
province,  but  in  recent  years  it  has  spread  northward  in  Michigan  and  east- 
ward in  Wisconsin  well  into  the  province. 

The  Gaspe  shrew  (Sorex  gaspensis)  seems  to  be  the  only  species  of 
mammal  restricted  to  the  Canadian  province,  but  this  species  occurs  only  in 
the  Gaspe  region,  so  that  it  is  not  characteristic  of  all  the  province. 

Certain  subspecies  of  mammals  are  largely  limited  to  the  Canadian  prov- 
ince, but  no  one  subspecies  which  is  restricted  to  the  Canadian  completely 
covers  the  whole  province.  In  Sorcx  palustris  the  two  subspecies  albibarbis 
and  gloveralleni  are  largely  confined  to  the  northeastern  part  of  the  Canadian 
province  and  the  subspecies  hydrobadistes  largely  to  the  western  part  of  the 
province.  In  Peromyscus  maniculatus  the  subspecies  abietorum  covers  largely 
the  eastern  part  of  the  province,  gracilis  the  western  part,  while  the  subspecies 
nubiterrae  extends  from  the  south  somewhat  into  the  province  in  Pennsyl- 
vania and  possibly  in  southern  New  York.  In  Synaptomys  cooperi  the  sub- 
species cooperi  covers  practically  the  Canadian  area,  but  it  extends  in  places 
slightly  south  of  the  boundaries  of  the  province. 

It  is  shown  by  the  above  discussion  that  several  of  the  mammals  which 


505 


512  LEE  R.  DICE  Ecology,  Vol.  19,  No.  4 

occur  in  the  Canadian  province  are  wide-ranging  species  which  occupy  biotic 
provinces  both  to  the  north  and  to  the  south  of  the  Canadian.  A  number  of 
the  mammals  of  the  Canadian  biotic  province  are  species  which  are  char- 
acteristic of  the  eastern  deciduous  forests,  and  some  of  these  species  reach 
their  northern  Hmits  at  the  northern  edge  of  the  province  where  the  deciduous 
forests  terminate.  A  few  others  extend  still  further  north  into  the  Hud- 
sonian  province  or  completely  across  it.  Several  species  of  mammals  found 
in  the  Canadian  province  are  characteristic  of  the  northern  spruce  forests 
(Hudsonian  province)  and  a  few  of  these  species  reach  their  southern  limits 
at  or  near  the  southern  border  of  the  Canadian  province.  No  species  of 
mammal  which  ranges  over  all  or  over  most  of  the  Canadian  province  seems 
to  be  restricted  to  that  province.  However,  a  few  subspecies  or  groups  of 
related  subspecies  are  restricted  fairly  closely  to  the  limits  of  the  province. 

In  its  mammalian  fauna  the  Canadian  biotic  province  is  characterized  by 
the  intermingling  of  species  which  are  abundant  in  the  eastern  deciduous 
forest  with  those  which  are  abundant  in  the  northern  spruce  forests.  This 
is  what  would  be  expected  from  the  fact  that  the  important  mammalian 
habitats  of  the  Canadian  province  are  predominantly  of  two  types,  hardwood 
forest  and  conifer  swamp  and  bog.  It  is  true  that  in  the  Canadian  province 
there  is  a  considerable  occurrence  of  pine  forest,  which  is  largely  absent  from 
the  Hudsonian  province,  and  which,  at  least  in  the  interior,  is  mostly  absent 
from  the  Carolinian  province.  However,  the  pine  forests  have  a  very  sparse 
population  of  mammals,  and  no  form  of  mammal  seems  to  be  restricted  to 
the  northern  pine  forest  habitat. 

The  assemblage  of  mammalian  species  ranging  over  most  of  the  Canadian 
province  is  different  from  the  assemblages  of  species  living  in  either  of  the 
adjacent  provinces.  This  is  true  in  spite  of  the  fact  that  no  species  or  sub- 
species of  mammal  which  ranges  over  all  the  province  is  restricted  to  it.  It 
is  believed,  therefore,  that  the  Canadian  biotic  province  as  described  above 
forms  a  natural  biogeographical  unit  for  the  mammals  as  well  as  for  the 
vegetation. 

If  a  faunal  area  is  to  be  recognized  between  the  Hudsonian  and  the  Can- 
adian provinces  as  here  described  it  will  have  to  be  cut  off  from  the  southern 
part  of  the  Hudsonian,  from  the  northern  part  of  the  Canadian,  or  made 
up  of  parts  of  both  provinces. 

All  of  the  mammals  listed  above  as  occupying  only  the  southern  part  of 
the  Hudsonian  of  eastern  Canada  range  far  to  the  southward  and  all  of  them 
extend  into  the  Carolinian  province,  except  the  fisher,  flying-squirrel  (Glau- 
comys  subrinus),  and  moose,  which  stop  at  the  northern  boundary  of  the 
Carolinian.  None  of  these  forms,  therefore,  could  be  made  the  basis  for  a 
subdivision  of  the  Hudsonian  of  eastern  Canada  into  two  longitudinal  belts, 
the  southern  of  which  might  be  called  the  Canadian. 

Of  the  forms  of  more  northern  distribution  which  range  south  into  the 
northern  part  of  the  Canadian  as  here  delimited,  the  Arctic-shrew  is  rare  and 


506 


October,  1938  CANADIAN    BIOTIC   PROVINCE  513 

has  a  discontinuous  distribution  in  this  area;  the  original  range  of  the  wol- 
verine in  this  area  is  questionable  and  the  species  is  now  extirpated ;  the 
northern  lemming-vole  occurs  only  in  the  most  eastern  part  of  the  area;  the 
heather-vole  extends  into  only  the  extreme  northern  edge  of  the  Canadian; 
and  the  caribou  was  probably  nomadic  and  erratic  in  occurrence  as  it  is  now 
in  other  parts  of  its  range.  It  is  evident  that  no  division  of  the  Canadian  to 
form  also  an  Alleghanian  fauna  can  be  made  on  the  basis  of  the  distribution 
of  these  forms. 

A  small  number  of  forms  of  southern  distribution  extend  their  range  into 
the  southern  part  of  the  Canadian  as  I  have  mapped  it.  Of  these  it  is  ques- 
tionable if  the  eastern  mole  {Scalopus  aquaticus),  pipistrelle,  southern  flying- 
squirrel  (Glaucomys  volans),  mole-mouse,  or  bison  ever  natively  extended 
far  into  the  province.  The  fox-squirrel  is  absent  from  the  eastern  part  of 
the  province.  The  cougar,  elk,  and  bison  are  now  absent  from  the  region, 
and  the  gray-fox  has  been  nearly  or  completely  extirpated  in  Michigan.  On 
the  other  hand  the  eastern-mole,  bob-cat,  fox-squirrel,  wood-mouse,  prairie 
deer-mouse  and  Mearns  cottontail  are  extending  their  ranges  northward  in 
Michigan  until  they  now  occupy  a  considerably  larger  part  of  the  Canadian 
than  they  did  at  the  time  the  region  was  first  settled.  It  would  therefore 
seem  inadvisable  to  base  any  major  faunal  area  on  the  distribution  of  these 
species. 

The  Canadian  province,  as  I  have  described  it,  is  not  especially  well  marked 
by  its  mammalian  species,  and  to  establish  two  faunal  divisions  in  this  area 
instead  of  one,  would  mean  that  each  of  the  two  would  not  only  have  no 
characteristic  species  of  mammals,  but  that  only  a  few  forms  would  reach 
their  limits  at  or  near  the  presumed  faunal  boundaries. 

Two  biotic  districts,  an  eastern  and  a  western,  can  be  recognized  as  sub- 
divisions of  the  Canadian  biotic  province.  The  red  spruce  (Picea  rubra) 
which  occurs  over  the  eastern  part  of  the  Canadian  and  which  also  extends 
southward  along  the  Appalachian  Mountains,  is  absent  from  the  western  part 
of  the  province  (Nichols,  '35,  fig.  5F).  The  beech  is  more  widespread  in 
the  province  than  the  red  spruce,  but  it  is  absent  from  western  Michigan, 
western  Wisconsin,  and  Minnesota  (Transeau,  '35,  fig.  12).  The  Gaspe 
shrew  which  occurs  locally  in  the  eastern  part  of  the  Canadian  province,  is 
absent  from  the  western  part.  Several  species  of  prairie  mammals,  as  al- 
ready mentioned,  invade  the  western  part  of  the  Canadian,  but  do  not  occur 
in  the  eastern  part.  Further,  the  water-shrew,  woodchuck,  chipmunk,  deer- 
mouse,  snowshoe  hare,  and  perhaps  other  species  of  mammals  are  repre- 
sented by  different  subspecies  in  the  eastern  and  western  parts,  respectively, 
of  the  province. 

New  Brunswick  does  not  greatly  differ,  however,  from  northern  Michigan, 
either  in  its  vegetation  or  in  its  mammalian  fauna.  There  is  no  sharp  transi- 
tion at  any  place  between  an  eastern  and  western  district  of  the  Canadian 


507 


514  LEE  R.  DICE  Ecology,  Vol.  19,  No.  4 

province,  and  it  is  impossible  to  suggest,  with  the  present  lack  of  detailed  in- 
formation, where  the  boundary  between  the  two  districts  should  be  placed. 

Summary 

A  detailed  consideration  of  the  vegetation  and  of  mammalian  distribution 
in  eastern  North  America  shows  that  the  so-called  Canadian  and  Alleghanian 
faunas  are  only  different  aspects  of  the  same  major  ecologic  complex.  They 
are  therefore  here  combined  under  the  name  Canadian  biotic  province. 

The  Canadian  biotic  province  is  characterized  by  a  hardwood  climatic 
climax  in  which  the  hemlock  and  white  pine  frequently  occur.  Pines  of 
several  species  constitute  an  important  subclimax,  or  edaphic  climax,  on  sandy 
and  gravelly  soils.  In  poorly  drained  situations  spruces  of  several  species, 
balsam  fir,  arbor  vitae,  and  tamarack  form  another  subclimax  or  group  of 
subclimaxes. 

No  species  or  subspecies  of  mammal  which  occurs  all  over  the  Canadian 
province  is  limited  to  the  province.  Nevertheless,  the  assemblage  of  species 
living  in  the  province  is  different  from  the  assemblages  living  in  the  adjacent 
provinces.  Furthermore,  a  number  of  species  of  mammals  reach  their  dis- 
tributional limits  at  or  near  the  northern  or  southern  boundaries  of  the 
province. 

Literature  Cited 

Frothingham,  E.  H.     1915.     The  northern  hardwood  forest:  its  composition,  growth, 

and  management.     U.  S.  Dcpt.  Agric,  Bull.  285,  79  pp. 
Fuller,  Geo.  D.,  and  Brother  Marie- Victorin.     1926.     The  Province  of  Quebec.     In 

Naturalist's    Guide   to   the   Americas,    pp.   293-299.     Baltimore:    Williams   and 

IVilkins  Co. 
Howe,   C.   D.,  and  J.   R.   Dymond.     1926.     Ontario.     In  Naturalist's    Guide   to   the 

Americas,  pp.  288-293.     Baltimore:   Williams  and  Wilkins  Co. 
Merriam,  C.  Hart.     1898.     Life  zones  and  crop  zones  of  the  United  States.     U.  S. 

Dept.  Agric.,  Div.  Biol.  Surv.,  Bull.  10,  79  pp. 
Miller,  Gerrit  S.,  Jr.     1924.     List  of  North  American  Recent  mammals,  1923.     U.  S. 

Nat.  Mus.,  Bidl.  US.     16  +  673  pp. 
Nichols,    G.    E.     1935.     The    hemlock — white    pine — northern    hardwood    region    of 

eastern  North  America.     Ecology  16:  403-422. 
Seton,  Ernest  T.     1929.     Lives  of  game  animals.     Garden  City,  N.   Y.:  Doubleday, 

Doran,  and  Co. 
Shelford,  V.  E.,  L.  Jones,  and  L.  R.  Dice.     1926.     Descriptive  list  of  North  Ameri- 
can biota  (south  to  central  Mexico).     In  Naturalist's  Guide  to  the  Americas, 

pp.  60-74.     Balti)nore:   Williams  and  Wilkins  Co. 
Transeau,  Edgar  N.     1935.     The  prairie  peninsula.     Ecology  16:  423-437. 
Weaver,  John  E.   and  Frederic   E.   Clements.     1929.     Plant    Ecology.     Nczv   York: 

McGraii'-Hill  Book  Co.     xx  -f  520  pp. 


508 


PLEISTOCENE  ZOOGEOGRAPHY  OF  THE  LEMMING,  DICROSTONYX^ 

John  E.  Guilday 
Carnegie  Museum,  Pittsburgh,   Pa. 

Received  August   30,   1962 


The  collared  lemmings,  genus  Dicros- 
tonyx  Gloger,  are  currently  divided  into 
two  subgenera.  Misothermus  Hensel  con- 
tains a  single  species,  D.  hudsonius  Pallas, 
isolated  on  the  tundra  of  northern  and 
coastal  L^ngava  from  all  other  Dicrostonyx 
(see  fig.  1).  The  subgenus  Dicrostonyx 
Gloger  contains  the  remaining  species  of 
the  genus,  D.  torquatus  Pallas  of  the  palae- 
arctic,  D.  groenlandicus  (Traill)  of  the 
nearctic,  and  D.  exsul  G.  M.  Allen  confined 
to  St.  Lawrence  Island  in  the  Bering 
Straits.  The  torquatus-groenlandicus-exsid 
species  group  may  be  conspecific  as  inti- 
mated by  Ellerman  and  Morrison-Scott 
(1951,  p.  653).  It  is  clear  that  they  are 
more  closely  related  to  one  another  than  to 
the  isolated  D.  hudsonius. 

In  the  absence  of  any  fossil  record  and 
interpreting  on  the  basis  of  modern  geo- 
graphical distribution  alone,  one  might 
argue  that  the  differentiation  of  D.  hudson- 
ius dated  from  the  Wisconsin  glaciation; 
that  as  the  ice  front  and  its  presumed 
periglacial  tundra  belt  shrank  to  the  north, 
the  eastern  segment  of  the  retreating  lem- 
ming population  was  cut  off  by  Hudson 
Bay.  The  bay  eventually  cut  the  Canadian 
tundra  into  an  eastern  and  a  western  com- 
ponent, each  with  its  distinctive  form  of 
collared  lemming.  This  does  not  appear  to 
be  the  case,  however. 

The  inaccuracy  of  this  interpretation  is 
shown  by  the  fossil  record.  The  one  record 
from  the  North  American  Pleistocene,  frag- 
mentary skulls  and  mandibles  of  at  least 
four  individuals  from  Sinkhole  no.  4,  New 
Paris,  Pennsylvania  (Guilday  and  Doutt, 
1961),  is  that  of  typical  Misothermus  (for 
characters,  see  Miller,  1898;  Hinton,  1926; 


^  Research    conducted    under    National    Science 
Foundation   Grant   no.   G-20868. 

Evolution  17:   194-197.     June,  1963  194 


Hall  and  Kelson,  1959),  indistinguishable 
from  the  modern  D.  hudsonius.  Carbon 
particles  taken  from  a  position  five  feet 
higher  in  the  sinkhole  matrix  were  dated  at 
11,300  ±  1,000  years  (Yale  Univ.  lab.  no. 
727).  The  age  of  the  lemming  remains  is 
somewhat  in  excess  of  this.  The  Miso- 
thermus dental  pattern  was  fixed  prior  to 
the  Wisconsin  recession  and  the  formation 
of  present  Hudson  Bay. 

There  have  been  two  species  of  collared 
lemmings  described  from  the  palaearctic 
Pleistocene.  Dicrostonyx  guliclmi  Sandford 
based  upon  cranial  material  from  Hutton 
Cave,  Somersetshire,  England,  is  a  late 
Pleistocene  form  of  the  living  D.  torquatus, 
and  may  be  conspecific  with  it  (see  Kowal- 
ski,  1959,  p.  229).  It  is  a  common  Eur- 
asian Pleistocene  fossil. 

The  second  Old  World  fossil  form,  D. 
henseli  Hinton,  described  from  cranial 
material  from  a  fissure  deposit  at  Ightham, 
Kent,  England,  appears  to  be  a  typical 
Misothermus  (see  the  description  by  Hin- 
ton, 1926,  p.  163).  D.  {Misothermus) 
henseli  has  been  recorded  from  the  Pleis- 
tocene of  England,  Ireland,  Jersey,  France, 
and  Germany  (Hinton,  1926;  Brunner, 
various  papers) ;  D.  {Dicrostonyx)  tor- 
quatus (or  gulielmi),  from  the  Pleistocene 
of  England,  Ireland,  France,  Poland,  Czech- 
oslovakia (Hinton,  1926;  Kowalski,  1959; 
Fejfar,  1961).  This  by  no  means  exhausts 
the  list  of  Old  World  Pleistocene  Dicro- 
stonyx localities.  But  enough  has  been 
cited  to  indicate  a  geographical  and  pos- 
sibly a  chronological  overlap  between  the 
two  species.  Both  forms  were  recovered 
by  Hinton  from  Merlin's  Cave,  Wye  Valley, 
Herefordshire,  England  (22  D.  gulielmi 
skulls,  4  D.  henseli)  and  at  Langwith  Cave, 
Derbeyshire  (1  D.  gulielmi,  2  or  3  D.  hen- 
seli).   Brunner  recorded  D.  henseli  from 


509 


ZOOGEOGRAPHY  OF  DICROSTONYX 


195 


Fig.  1.  Outline  map  of  North  America,  showing  approximate  limit  of  continental  glaciation. 
A.  Mainland  modern  distribution  of  the  subgenus  Dicrostonyx  in  America.  B.  Modern  distribution  of 
the  subgenus  Misothermus. 


thirteen  Bavarian  cave  deposits.  In  one, 
the  Markgrabenhohle,  Brunner  (1952c,  p. 
465)  reported  that  25%  of  the  mandibles 
resembled  D.  gulielmi  in  possessing  a  small 
anteroexternal  vestigial  angle  on  M3,  "eine 
deutliche  aiissere  Schmeltzfalte."  Many 
uncorrelated  fissure,  cave,  and  terrace  de- 
posits are  involved,  however.  And  while 
they  are  all  middle  to  late  Pleistocene  in 
age,  their  sequential  position  within  that 
time  span  has  not  been  established  with 
any  degree  of  confidence. 


The  facts  at  hand  seem  to  indicate  that 
two  forms  of  the  genus  Dicrostonyx  inhab- 
ited Eurasia  and  perhaps  North  America 
during  the  Pleistocene,  and  that  one  of  them 
survives  as  a  postglacial  relict,  isolated  in 
the  tundra  of  Ungava  (fig.  2).  The  pre- 
Wisconsin  origin  of  the  Misothermus  dental 
pattern  is  demonstrated  by  fossil  forms  in 
both  continents. 

If  we  assume,  as  does  Hinton  (1926), 
that  Misothermus  is  not  a  true  phylogenetic 
category  but  that  D.  henseli  and  D.  hud- 


510 


196 


JOHN  E.  GUILDAY 


Fig.  2.  Postulated  distribution  of  Dicrostonyx  (A)  and  Misotherntus  (B)  in  North  America  at 
Wisconsin  glacial  maximum.  Note  site  of  Sinkhole  no.  4,  New  Paris,  Bedford  County,  Pennsylvania. 
Hachures  indicate  approximate  limit  of  continental  glaciation. 


sonius  are  of  independent  origin  from 
Dicrostonyx  proper,  we  are  faced  with  the 
apparent  coincidence  that  a  form  (henseli) 
was  replaced  by  modern  Dicrostonyx  in  the 
Old  World  while  its  morphological  equiva- 
lent, D.  hudsonius,  which  ranged  as  far 
south  as  central  Pennsylvania  during  late 
Wisconsin  times,  survives  today  only  where 
it  is  completely  isolated  from  all  contact 
with  the  Eurasian-Western  Nearctic  Dicro- 
stonyx. 

Both  D.  henseli  and  D.  hudsonius  appear 


to  have  been  completely  or  partially  re- 
placed by  true  Dicrostonyx.  Is  it  possible 
that  modern  D.  hudsonius  (or  some  form  of 
Misothermus)  at  one  time  ranged  through- 
out the  holarctic,  and  that  it  was  replaced 
during  late  Pleistocene  times  by  lemmings 
of  the  subgenus  Dicrostonyx,  first  in  the 
Old  World,  later  in  the  New;  this  latter 
replacement  occurring  sometime  after  the 
post-Wisconsin  formation  of  Hudson  Bay 
and  the  division  of  the  mainland  North 


511 


ZOOGEOGRAPHY  OF  DICROSTONYX 


197 


American   tundra   into   an   eastern   and   a 
western  component? 

I  wish  to  thank  Dr.  J.  Kenneth  Doutt, 
Curator  of  Mammals,  Miss  Caroline  A. 
Heppenstall,  Assistant  Curator  of  Mam- 
mals, and  Dr.  Craig  C.  Black,  Gulf  Associ- 
ate Curator  of  Vertebrate  Fossils,  Carnegie 
Museum,  for  their  helpful  criticism. 

Summary 
The  modern  distribution  of  Dicrostonyx 
hudsonius  Pallas  (confined  to  the  tundra  of 
Ungava)  is  believed,  on  the  basis  of  the 
fossil  record,  to  be  a  relict  of  a  former 
holarctic  pre-Wisconsin  distribution. 

References  Cited 

Brunner,  Georg.  1949.  Das  Gaisloch  bei  Miiri- 
zinghof  (Mfr.)  mit  Faunen  aus  dem  Altdiluvium 
und  aus  jiingeren  Epochen.  Neuen  Jahrbuch 
Mineral.,  etc.     Abhandlungen,  91(B):   1-34. 

.      1951.     Eine   Faunenfolge   von   Wiirm   III 

Glazial  bis  in  das  Spat-Postglazial  aus  der 
"Quellkammer"  bei  Pottenstein  (Ofr.).  Geol. 
Bl.    NO-Bayern,  1:   14-28. 

.     19S2a.     Das    Dohlenloch    bei    Pottenstein 

(Obfr.).  Eine  Fundstelle  aus  dem  Wiirm  II 
Glazial.  Abhandlungen  Naturhist.  Ges.  Niirn- 
berg,  27(3):  49-60. 

.     19S2b.     Der  "Distlerkeller"  in  Pottenstein 

Ofr.  Eine  Faunenfolge  des  Wiirm  I-III  inter- 
stadial.    Geol.  Bl.  NO-Bayern,  2:  95-105. 

.  1952c.  Die  Markgrabenhohle  bei  Potten- 
stein (Oberfranken).  Eine  Fauna  des  Altdi- 
luviums  mit  Talpa  episcopalis  Kormos  u.  a. 
Neues  Jahrbuch  Geol.  Palaontol.  Mh.,  10: 
457-471. 

.     1953a.     Die  Heinrichgrotte  bei  Burggaillen- 

reuth  (Oberfranken).  Eine  Faunenfolge  von 
Wiirm  I-Glazial  bis  Interstadial.  Neues  Jahr- 
buch Geol.  Palaontol.  Mh.,  6:   251-275. 

.     19S3b.     Die  Abri  "Wasserstein"  bei  Betzen- 

stein  (Ofr.).     Eine  subfossile  Fauna  mit  Sorex 


tniniitissimus   H.   de    Balsac.      Geol.    Bl.   NO- 
Bayern,  3:  94-105. 

— .  1955.  Die  Hohle  am  Butzmannsacker  bei 
Auerbach  (Opf.).  Geol.  Bl.  NO-Bayern,  5: 
109-120. 

— .  1956.  Nachtrag  zur  Kleinen  Teufelshohle 
bei  Pottenstein  (Oberfranken).  Eine  Ubergang 
von  der  letzten  Riss-Wiirm-Warm-fauna  zur 
Wiirm  I-Kaltfauna.  Neues  Jb.  Geol.  Palaontol. 
Mh.,  2:  75-100. 

— .  1957a.  Die  Breitenberghohle  bei  Gosswein- 
stein/Ofr.  Eine  Mindel-Riss-und  eine  post- 
glaziale  Mediterran-Fauna.  Neues  Jb.  Geol. 
Palaontol.  Mb.,  7-9:  352-378,  385-403. 

— .  1957b.  Die  Caciliengrotte  bei  Hirschbach 
(Opf.)  und  ihre  fossile  Fauna.  Geol.  Bl.  NO- 
Bayern,  7:  155-166. 

— .       1958.      Das    Guckerloch    bei    Michelfeld 
(Opf.).     Geol.  Bl.  NO-Bayern,  8:    158-172. 
1959.     Das  Schmeidberg-Abri  bei  Hirsch- 


bach (Oberpfalz).    Palaont.  Z.,  33:   152-165. 

Ellerman,  J.  R.,  AND  T.  C.  S.  Morrison-Scott. 
1951.  Checklist  of  Palaeoarctic  and  Indian 
mammals.  British  Museum  (Natural  History) . 
London.     810  p. 

Fejfar,  Oldrich.  1961.  Review  of  Quaternary 
Vertebrata  in  Czechoslovakia.  Instytut  Geo- 
logiczny.  Odbitka  z  Tomu  34  Prac.  Czwar- 
torzed  Europy  Srodkowej  I  Wschodniej,  p. 
109-118. 

Guilday,  J.  E.,  and  J.  K.  Doutt.  1961.  The  Col- 
lared Lemming  (Dicrostonyx)  from  the  Penn- 
sylvania Pleistocene.  Proc.  Biol.  Soc.  Wash- 
ington, 74:   249-250. 

Hall,  E.  R.,  and  R.  K.  Kelson.  1959.  The  mam- 
mals of  North  America.    Vol.  II,  p.  547-1083. 

Hinton,  M.  a.  C.  1926.  Monograph  of  the  voles 
and  lemmings  (Microtinae)  living  and  ex- 
tinct. Vol.  I.  Richard  Clay  and  Sons,  Suffolk. 
488  p. 

KowALSKi,  K.  1959.  Katalog  Ssakow  Plejstocenu 
Polski.  Polska  Akademia  Nauk.  Inst.  Zool. 
Oddzial  W  Krakowie.     267  p. 

Miller,  G.  S.,  Jr.  1896.  Genera  and  subgenera 
of  voles  and  lemmings.  North  American 
Fauna  no.  12,  80  p.,  U.  S.  Dept.  Agriculture. 


512 


SUBFOSSIL  MAMMALS  FROM  THE  GOMEZ  FARIAS  REGION  AND 
THE  TROPIGAL  GRADIENT  OF  EASTERN  MEXICO 

By  Karl  F.  Koopman  and  Paul  S.  Martin 

In  the  spring  of  1953  Byron  E.  Harrell  and  P.  S.  Martin  collected  superficial 
animal  remains  at  three  cave  localities  in  the  Sierra  Madre  Oriental  of  south- 
western Tamaulipas.  Locally,  the  mountains  are  sufficiently  humid  to  support 
small,  isolated  patches  of  Cloud  Forest  and  Tropical  Evergreen  Forest  ( Martin, 
1958).  At  this  latitude,  23°  north,  these  two  tropical  plant  foraiations  appear 
to  reach  their  limit.  In  recent  years  four  faunal  papers  on  mammals  of  southern 
Tamaulipas  have  appeared,  each  reporting  certain  tropical  species  unknown 
at  higher  latitudes  (Baker,  1951;  Goodwin,  1954;  Hooper,  1953;  de  la  Torre, 
1954).  Southern  Tamaulipas  appears  to  be  of  primary  significance  in  the 
Gulf  lowlands  faimal  gradient,  a  system  extending  from  southern  Veracruz 
to  southern  Texas.  In  the  lowlands  of  eastern  Mexico  many  of  the  dominant 
tropical  American  taxa  reach  their  range  limits.  We  seek  to  define  the  north- 
eastern section  of  this  gradient  with  regard  to  tropical  mammal  faunas,  to  relate 
it  to  shifts  in  vegetation  and  to  indicate  the  relative  importance  of  the  Gomez 
Farias  region  as  a  faunal  terminus.  The  Gomez  Farias  region  is  defined  as 
the  area  from  22°48'  to  23°30'  north  latitude  and  99°  to  99°30'  west  longitude, 
or  approximately  the  rectangle  enclosed  by  the  towns  of  Llera,  Jaumave, 
Ocampo  and  Limon. 

In  establishing  the  presence  of  eight  species  known  in  the  Gomez  Farias 
region  only  from  the  skeletal  remains,  and  in  extending  the  altitudinal  or 
ecological  ranges  of  others,  the  present  collection  supplements  previous  reports. 
It  indicates  the  value  of  using  owl  peUet  deposits  as  a  cross  check  on  standard 
trapping  technique. 

DESCRIPTION  OF  DEPOSITS 

Cretaceous  limestones  comprising  the  precipitous  east  slope  of  the  Sierra 
Madre  Oriental  near  the  village  of  Gomez  Farias  are  severely  folded.  Under 
torrential  summer  rains  they  have  eroded  into  very  rough  karst  terrain  with 
virtually  no  surface  drainage.  Caves  and  sink  holes,  a  characteristic  of  karst, 
are  a  common  feature.  Most  do  not  appear  to  be  inhabited  by  bats  or  owls. 
Of  those  that  are,  the  constant  high  humidity  and  frequent  flushing  from 


513 


JOURNAL  OF  MAMMALOGY 


Vol  40,  No.  1 


percolating  rainwater  apparently  prevent  accumulation  of  deep  bone  or  guano 
deposits.  Large  bat  colonies  numbering  thousands  of  individuals  occur  in 
Tropical  Deciduous  Forest  in  the  Canyon  of  the  Rio  Boquilla,  8  km.  southwest 
of  Chamal,  and  in  a  guano  cavern  at  El  Abra,  8  km.  northeast  of  Antiguo 
Morelos.  However,  no  colonies  of  similar  size  have  been  found  in  the  more 
himiid  portions  of  the  G6mez  Farias  region. 

Of  approximately  thirty  caves  and  sink  holes  explored  near  Gomez  Farias, 
material  from  three  is  represented  in  our  collection.  All  occur  in  the  mountains 
west  of  the  village  of  G6mez  Farias,  latitude  29°03'  north,  longitude  99°09' 
west,  and  within  16  km.  of  each  other  ( see  Table  1 ) .  The  following  information 
will  serve  to  characterize  them: 

1.  Paraiso.  Aserradero  del  Paraiso  is  the  name  of  a  small  sawmill  located 
in  Tropical  Evergreen  Forest  13  km.  north-northwest  of  Chamal.  A  narrow 
ravine  about  1  km.  south  of  the  sawmill  harbors  several  caves,  including  a 
deep,  wet  grotto  with  permanent  water.    On  the  sloping  floor  of  a  small 


Table  1. — Mammals  from  cave  deposits  in  the  Gdmez  Farias  region  (numbers  refer  to 

anterior  skull  parts  identified) 


Distance  from  G6mez  Farias: 

Elevation  in  meters: 

Vegetation  type: 


PABAISO 


SW 


13  km. 
420 

Tropical  Ever- 
green Forest 


RAJ^CHO  DEL  CIELO 

6  km.  NW 

1050 

Cloud  Forest 


INFERNO 

7  km.  W 

1320 

Cloud  Forest 


Didelphis  marsupudis  — 
Marmosa  mexicana 


Cryptotis  pergracilis 

Cryptotis  mexicana 

Chilonycteris  parnellii 

Enchisthenes  harti  

Artibeus  cinereus 

Centurio  senex 

Eptesicus  fuscus 

Lasiurus  cinereus 

Antrozous  paUldus 

Sylvilagus  floridanus 

Glaucomys  volans 

Liomys  irroratus 


Reithrodontomys  mexicanus 
Reithrodontomys  megalotis  . 

Baiomys  taylori 

Peromyscus  boylei 

Peromyscus  pectorclis  

Peromyscus  ochraventer 

Oryzomys  alfaroi 

Sigmodon  hispidus 

Neotoma  angustapalata 

Total  identifications 


3 
1 


1 
1 
1 
1 


3 
29 

9 
51 


1 
3 


1 
2 


1 
9 


1 
18 

10 

1 

1 

1 

12 

5 
1 

17 
2 
7 
5 

17 
98 


514 


Feb.,  1959  KOOPMAN  AND  MARTIN— MAMMALS  OF  EASTERN  MEXICO  3 

dry  cave  on  the  west  wall  of  this  ravine  many  scattered  (apparently  water- 
transported)   small  bones  were  found. 

2.  Rancho  del  Cielo.  A  small  sink  and  cave  several  hundred  meters  east 
of  this  important  Cloud  Forest  collecting  locality  contained  a  few  bat  remains 
and  fresh  owl  pellets. 

3.  Inferno  (also  designated  Infemillo).  A  rather  large  cave  adjacent  to  an 
abandoned  sawmill  of  this  name  is  located  in  upper  Cloud  Forest  roughly 
2  km.  south  of  tlie  mill  settlement  called  La  Gloria.  Abundant  pellet  remains 
were  found  on  a  dislodged  boulder  just  inside  the  cave  mouth. 

All  the  caves  are  surrounded  by  heavy  forest,  much  of  it  recently  lumbered. 
Jagged,  shrub-covered  or  almost  bare  karst  ridges  and  pinnacles  confine  the 
areas  of  tall  forest  to  valleys,  pockets  and  gentle  slopes.  A  more  complete 
description  of  the  Gomez  Farias  region  is  in  preparation  (Martin,  1958). 

Although  the  bam  owl,  Tyto  alba,  occurs  in  a  very  large  cavern  at  El  Abra 
north  of  Antiguo  Morelos,  the  only  raptor  definitely  known  to  roost  in  caves 
in  the  Gomez  Farias  region  is  the  wood  owl,  Ciccaba  virgata.  While  it  is 
possible  that  certain  non-volant  mammals  died  from  other  causes,  all  skeletal 
remains  of  these,  and  perhaps  even  some  of  the  bats,  can  be  ascribed  to  Ciccaba. 

Cave  records  do  not  make  ideal  locality  data,  especially  when  information 
on  ecological  or  altitudinal  distribution  is  sought.  We  assume  that  the  forest 
types  and  the  elevation  in  the  immediate  vicinity  of  each  cave  represent  the 
habitat  in  which  the  owls  fed,  but  this  is  by  no  means  certain.  The  hunting 
range  and  nocturnal  movements  of  Ciccaba  are  unknown. 

There  is  no  stratigraphic  evidence  for  assuming  that  any  material  is  older  than 
very  recent.  Limestone  deposit  on  certain  bones  may  represent  the  concretion 
of  a  single  rainy  season. 

SYSTEMATIC  TREATMENT  OF  THE  MAMMALS 

We  emphasize  first  that  only  a  fraction  of  the  mammalian  and  none  of  the 
bird  bones  have  been  identified.  Very  little  attempt  has  been  made  to  identify 
any  of  the  post-cranial  elements,  and  in  the  case  of  the  cricetine  rodents  only 
the  best  of  cranial  material  could  be  identified  witli  any  confidence.  Particular 
difficulty  was  encountered  with  lower  jaws  of  cricetines,  even  when  teeth 
were  present.  As  a  result,  determinations  in  this  group  are  considered  less 
reliable  than  in  the  others.  In  particular  this  applies  to  the  Feromyscus- 
Baiomys-Reithrodontomys  group  of  genera,  in  which  not  only  specific  but  also 
good  generic  characteristics  were  hard  to  find  in  most  of  the  material.  Size, 
molar  form,  palatal  morphology  and  shape  of  the  zygomatic  plate  were  found 
to  provide  the  most  useful  taxonomic  characters  in  this  subfamily. 

In  many  cases  a  closely  adhering  limestone  drip  deposit  was  present  and 
was  sometimes  difficult  to  remove  without  damaging  tlie  underlying  bone. 
No  attempt  has  been  made  to  identify  subspecies.  In  our  opinion  the  theoretical 
requirements  of  population  sampling  and  measurement,  as  employed  in  sub- 


515 


4  JOURNAL  OF  MAMMALOGY  Vol.  40,  No.  1 

specific  identification,  are  not  met  in  any  but  perhaps  the  best  fossil  material. 
For  the  following  species  determinations  Koopman  alone  is  responsible. 

Didelphis  marsupialis. — Inferno:  one  rostral  fragment  of  a  young  individual. 
Previously  recorded  from  Gomez  Farias  (Hooper,  1953). 

Marniosa  mexicana. — Inferno:  three  rostral  fragments  and  15  mandibles. 
On  the  basis  of  dentition,  these  are  clearly  opossums,  but  of  the  Middle  Amer- 
ican genera  of  Didelphidae,  all  but  Marmosa  are  much  too  large.  Of  the  four 
species  of  this  genus  occurring  north  of  Panama,  all  but  M.  mexicana  differ 
from  the  subfossil  material  either  in  larger  size  or  greater  development  of  a 
precondylar  crest  on  the  outer  side  of  the  mandible.  The  species  has  not 
previously  been  recorded  north  of  Jalapa,  Veracruz. 

Cryptotis  per  gracilis. — Paraiso:  one  rostnmi  and  two  mandibles.  Restriction 
to  the  family  Soricidae  and  the  genus  Cryptotis  may  be  made  on  the  basis  of 
dentition.  In  eastern  Mexico  north  of  the  Isthmus  of  Tehuantepec  (states  of 
Tamaulipas,  San  Luis  Potosi,  Hidalgo,  Puebla  and  Veracruz)  the  following 
six  species  of  Cryptotis  are  known:  C.  parva,  C.  pergracilis,  C.  obscura,  C. 
micrura,  C.  mexicana  and  C.  nelsoni.  All  except  C.  parva  and  C.  pergracilis 
may  be  ruled  out  on  the  basis  of  larger  size.  While  clear-cut  cranial  differences 
between  the  latter  two  species  appear  to  be  absent,  the  eastern  race  of  per- 
gracilis, C.  p.  pueblensis,  has  a  somewhat  deeper  nasal  emargination  of  the 
rostrum  than  the  southwestern  race  of  parva,  C.  p.  berlandieri.  Though  slightly 
broken  anteriorly,  the  subfossil  rostrum  appears  to  have  a  nasal  emargination 
somewhat  closer  to  that  of  C.  pergracilis  pueblensis  than  to  that  of  the  two 
Tamaulipan  specimens  of  C.  parva  berlandieri  recorded  by  Goodwin  (1954). 
However,  no  direct  comparison  of  the  Paraiso  specimens  with  C.  pergracilis 
pueblensis  was  made,  but  only  with  a  sketch.  Unfortunately  our  material  seems 
inadequate  to  solve  the  problem  of  specific  status,  i.e.,  are  C.  parva  and 
C.  pergracilis  sympatric  in  southern  Tamaulipas,  do  they  integrade  through  a 
narrow  hybrid  zone,  or  is  there  a  more  complex  arrangement? 

The  northernmost  previous  record  of  C.  pergracilis  is  Platanito  in  San  Luis 
Potosi. 

Cryptotis  mexicana. — Inferno:  six  rostra,  four  mandibles,  and  three  humeri; 
Rancho  del  Cielo:  one  rostrum.  Specimens  were  trapped  at  the  latter  locality 
(Goodwin,  1954). 

Chilonycteris  parnellii. — Paraiso:  one  mandible.  Goodwin  (1954)  records 
a  series  from  El  Pachon.  As  Koopman  (1955)  has  pointed  out,  the  mainland 
C.  rubiginosa  and  the  West  Indian  C.  parnellii  are  almost  certainly  conspecific. 
Since  Koopman  believed  that  C.  parnellii  Gray  had  several  months  priority  over 
C.  rubiginosa  Wagner,  the  combined  species  was  called  C.  parnellii.  De  la  Torre 
(1955)  has  shown  that  this  is  not  the  case  and,  finding  no  way  of  determining 
which  name  was  published  first,  recommended:  "In  the  absence  of  conclusive 
evidence,  the  better  known  and  more  widely  used  name  rubiginosa  should  be 
retained." 

Unfortunately,  if  there  is  no  clear  priority,  the  law  of  the  first  reviser  would 


516 


Feb.,  1959         KOOPMAN  AND  MARTIN— MAMMALS  OF  EASTERN  MEXICO  5 

seem  to  hold,  in  this  case  tlie  first  to  use  one  of  the  two  names  to  include  both 
forms,  i.e.,  Koopman  (1955).  It  is  not  legally  possible  to  withdraw  from  this 
position.  Therefore  it  appears  that  C.  parnellii  must  stand  as  the  name  assigned 
to  both  mainland  and  West  Indian  large  Chilonycteris. 

The  question  of  nomenclature  should  not  obscure  the  more  significant  taxo- 
nomic  conclusion  that  a  single  species  is  involved. 

Artibeus  cinereus. — Rancho  del  Cielo:  two  partial  skulls,  one  lower  jaw. 
De  la  Torre  has  also  recorded  this  species  from  Rancho  del  Cielo. 

Enchisthenes  harti. — Inferno:  one  partial  skull.  The  short  broad  rostrum 
and  characteristic  molar  pattern  rule  out  all  American  bats  outside  the  Steno- 
derminae.  Of  the  Middle  American  stenodermines,  only  Uroderma  bilobatum, 
Vampyrops  helleri  and  Enchisthenes  harti  agree  with  the  Inferno  skull  in  size 
and  dental  formula  (i-  o^  p-  m^).  Both  Uroderma  and  Vampyrops,  however, 
have  rostra  considerably  longer  than  that  of  the  subfossil  skull.  On  the  other 
hand,  there  is  close  resemblance  to  skulls  of  Enchisthenes  from  Honduras  and 
Ecuador.  De  la  Torre  (1955)  has  recently  summarized  the  knovsoi  records, 
specimens  from  Ciudad  Guzman  in  Jalisco  being  the  closest  to  Tamaulipas 
geographically.  Four  other  localities  extend  the  distribution  south  to  Trinidad 
and  Ecuador. 

Centurio  senex. — Inferno:  one  rostrum.  Of  all  the  North  and  Middle  Amer- 
ican bats,  only  Centurio  senex  agrees  with  the  subfossil  skull  in  dental  formula 
(i^  c^  p^  m^)  and  in  the  palate  being  more  than  twice  as  wide  as  it  is  long. 
The  Inferno  rostnim  resembles  a  skull  of  Centurio  senex  in  all  important 
respects.   De  la  Torre  (1954)  recorded  a  single  specimen  from  Pano  Ayuctle. 

Eptesicus  fuscus. — Paraiso:  one  mandible.  Several  characters  of  this  bone 
inmiediately  narrow  the  field  considerably.  These  are  mandibular  length,  tooth 
size,  dental  formula  (is  Ci  p2  ma),  molar  pattern  and  height  of  the  coronoid 
process.  This  leaves  us  with  only  two  North  and  Middle  American  species, 
Eptesicus  fuscus  and  Dasypterus  intermedius.  Of  these,  Dasypterus  may  be 
ruled  out  on  the  basis  of  its  more  robust  mandibular  ramus.  Comparison  of 
the  Paraiso  mandible  with  Eptesicus  fuscus  reveals  no  important  differences. 
I  have  been  able  to  find  no  other  records  of  this  bat  in  Tamaulipas,  the  nearest 
localities  being  Rio  Ramos  in  Nuevo  Leon  to  the  west  (Davis,  1944)  and 
Caiiada  Grande  in  San  Luis  Potosi  to  the  southwest  (Dalquest,  1953).  Good 
series  from  Tamaulipas,  if  they  could  be  obtained,  should  show  integradation 
between  E.  f.  fuscus  and  £.  /.  miradorensis. 

Lasiurus  cinereus. — Inferno:  one  nearly  complete  skull.  All  other  species  of 
North  and  Middle  American  bats  may  easily  be  excluded  from  consideration 
on  the  basis  of  size,  rostral  shape  and  dental  formula  ( i^  c^  p^  m^ ) .  It  matches 
L.  cinereus  closely.  Since  this  bat  is  migratory,  it  is  impossible  to  say  whether 
this  individual  belonged  to  a  resident  population  or  was  merely  a  winter  visitor. 
The  nearest  previous  records  are  Matamoros  in  northern  Tamaulipas  (Miller, 
1897)  and  EI  Salto  in  eastern  San  Luis  Potosi  (Dalquest,  1953). 

Antrozous  pallidus. — Paraiso:    one  partial  lower  jaw.    Mandible  and  tooth 


517 


6  JOURNAL  OF  MAMMALOGY  Vol.  40,  No.  1 

size,  molar  pattern  and  dental  formula  (12  Ci  p2  ma)  rule  out  all  North  and 
Middle  American  bats  except  Promops  centralis  and  Antrozous.  Promops  may 
be  excluded  by  the  quite  different  appearance  of  the  labial  surface  of  the 
coronoid  region.  Of  the  two  species  of  Antrozous  recognized  by  Orr  ( 1954 ) , 
A.  bunkeri  is  distinctly  larger  than  the  Paraiso  mandible.  A.  pallidus  resembles 
it  in  all  respects.  The  University  of  Michigan  Museum  of  Zoology  has  six 
specimens  from  Tula,  which  were  mentioned  by  Orr  (1954). 

Sylvilagus  floridanus. — Paraiso:  one  maxillary  fragment  of  a  young  indi- 
vidual. Goodwin  (1954)  records  the  species  from  Gomez  Farias,  Pano  Ayuctle 
and  Chamal. 

Glaucomys  volans. — Inferno:  two  palatal  fragments,  ten  mandibles;  Rancho 
del  Cielo:    one  mandible;  Paraiso:    one  mandible.    From  the  dental  formula 

0        2  ^ 

(ii  Co  Pi  ms)  these  specimens  are  clearly  referable  to  the  Sciuridae,  of  which 
all  northeastern  Mexican  species  except  Eutamms  hulleri,  E.  dorsalis  and  Glau- 
comys volans  are  clearly  too  large.  In  Eutamias,  however,  the  mandible  is 
much  less  deep  than  in  the  Tamauhpas  material.  The  latter  bears  a  convincing 
resemblance  to  G.  volans.  The  nearest  locahty  from  which  the  species  had 
previously  been  obtained  is  Santa  Barbarita  in  San  Luis  Potosi  ( Dalquest,  1953 ) . 

Liomys  irroratus. — Paraiso:  one  maxillary  fragment.  Goodwin  (1954)  re- 
cords a  series  from  Pano  Ayuctle. 

Oryzomys  alfaroi. — Inferno:  four  maxillary  fragments,  one  partial  skull; 
Paraiso:  three  mandibles.  Goodwin  (1954)  and  Hooper  (1953)  have  each 
recorded  the  species  from  Rancho  del  Cielo. 

R.  (Reithrodontomys)  megalotis. — Inferno:  one  partial  skull.  Identification 
of  this  fragment  is  tentative.  The  species  has  already  been  recorded  from 
Rancho  del  Cielo  by  both  Goodwin  (1954)  and  Hooper  (1953). 

R.  (Aporodon)  mexicanus. — Inferno:  five  partial  skulls;  Rancho  del  Cielo: 
two  partial  skulls.  The  species  has  been  recorded  previously  from  Rancho 
del  Cielo  by  Goodwin  (1954)  and  Hooper  (1953). 

Peromyscus  boylei. — Inferno:  two  partial  skulls,  15  maxillaries;  Rancho  del 
Cielo:  one  mandible.  The  species  is  recorded  by  Goodwin  (1954)  from  both 
Rancho  del  Cielo  and  Rancho  Viejo. 

Peromyscus  pectoralis. — Inferno:  one  partial  skull,  one  maxillary.  It  has 
been  recorded  by  Goodwin  (1954)  from  both  La  Joya  de  Salas  and  2  km.  west 
of  El  Carrizo. 

Peromyscus  ochraventer. — Inferno:  one  partial  skull,  six  maxillaries.  The 
species  has  been  recorded  from  Rancho  del  Cielo  by  both  Goodwin  (1954) 
and  Hooper  (1953). 

Baiomys  taylori. — Paraiso:  one  mandible.  Goodwin  (1954)  and  Hooper 
(1953)  have  recorded  it  from  Pano  Ayuctle. 

Sigmodon  hispidus. — Paraiso:  one  rostral  half,  ten  maxillaries,  two  pre- 
maxillaries,  three  braincase  elements,  16  mandibles.  The  species  has  been 
recorded  from  Pano  Ayuctle  by  Goodwin  (1954)  and  Hooper  (1953). 

Neotoma  angustapalata. — Inferno:   four  partial  rostra,  five  maxillaries,  eight 


518 


Feb.,  1959         KOOPMAN  AND  MARTIN— MAMMALS  OF  EASTERN  MEXICO  7 

mandibles;  Rancho  del  Cielo:  one  maxillary;  Paraiso:  one  maxillary  fragment, 
two  premaxillaries,  six  mandibles.  There  is  also  a  great  deal  of  additional 
Neotoma  material  from  Inferno  that  probably  belongs  here,  but  which  has 
not  been  specifically  identified.  Both  Goodwin  (1954)  and  Hooper  (1953) 
list  specimens  from  Rancho  del  Cielo  and  El  Pachon  although,  as  Hooper 
points  out,  the  precise  status  of  N.  angnstapalata  and  its  various  southern 
Tamaulipas  populations  is  far  from  clear.  At  the  present  time  this  name  appears 
to  be  something  of  a  "catch-aU."  It  is  felt,  however,  that  a  revision  should  be 
based  on  entire  specimens  rather  than  on  skeletal  fragments. 

FAUNAL  COMPARISONS  AND  THE  STATUS  OF  GLAUCOMYS 

The  identifications  summarized  in  Table  1  represent  total  number  of  an- 
terior skull  elements  and  not  total  number  of  individuals,  which  may  be  some- 
what less.  Although  such  data  do  not  lend  themselves  to  close  quantitative 
inspection,  we  feel  that  the  faunas  sampled  near  Inferno  and  Paraiso  reveal 
important  differences.  Two  quite  different  habitats.  Cloud  Forest  and  Tropical 
Evergreen  Forest,  are  represented.  It  would  be  surprising  if  the  faunas  were 
qualitatively  similar.  Peromyscus,  the  dominant  genus  comprising  27  per  cent 
of  the  Inferno  deposits,  is  unrepresented  at  Paraiso.  In  turn,  Sigmodon,  which 
comprises  57  per  cent  of  the  material  obtained  at  Paraiso,  is  absent  from  Inferno. 
Such  a  discrepancy  may  reflect  an  ecological  shift  in  the  dominant  cricetine 
form.  Other  rather  common  species  which  appeared  only  in  the  Cloud  Forest 
caves  include:  Marmosa  mexicana  (18%),  Cryptotis  mexicana  (10%)  and 
Reithrodontomys  mexicanus  (5%).  One  genus,  Neotoma,  occurs  at  both 
localities  with  a  relatively  constant  frequency,  17-18  per  cent. 

Within  the  G6mez  Farias  region  the  following  are  known  only  from  their 
skeletal  remains:  Marmosa  mexicana,  Cryptotis  per  gracilis,  Chilonycteris 
parnellii,  Enchisthenes  harti,  Eptesicus  fuscus,  Lasiurus  cinereus,  Antrozous 
pallidus  and  Glaucomys  volans.  Presence  of  the  latter  is  perhaps  of  greatest 
interest.  In  Middle  America  flying  squirrels  are  very  poorly  known,  presumably 
the  result  of  their  nocturnal  and  arboreal  habits  rather  than  an  inherent  scarcity. 
We  are  aware  of  ten  other  locaHty  records  between  Chihuahua  and  Honduras, 
each  represented  by  one  or  two  specimens.  In  the  Gomez  Farias  region  remains 
of  Glaucomys  appeared  at  each  cave  locality,  suggesting  a  general  range 
through  humid  forest,  both  Cloud  Forest  and  Tropical  Evergreen  Forest, 
between  420  and  1,320  meters.  To  our  knowledge  Glaucomys  has  not  previously 
been  collected  in  lowland  tropical  forests  (below  1,000  meters). 

THE  LOWLAND  TROPICAL  GRADIENT  IN  EASTERN  MEXICO 

We  might  imagine  a  lowland  tropical  fauna  to  decline  with  increasing  lati- 
tude at  a  rather  regular  rate.  However,  in  reality  the  environment  and  fauna 
undergo  a  series  of  discrete  changes,  stepwise  ( see  Fig.  1 ) .  In  eastern  Mexico 
four  major  tropical  lowland  vegetation  types  are  represented.  From  south  to 
north  they  terminate  in  the  following  sequence:    Rainforest,  Tropical  Ever- 


519 


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JOURNAL  OF  MAMMALOGY 


Vol  40.  No.  1 


green  Forest,  Tropical  Deciduous  Forest  and  Thorn  Forest  (Leopold,  1950). 
Each  terminus  is  marked  by  a  steepening  of  the  faunal  gradient. 

In  defining  the  lowland  tropical  fauna  we  have  excluded  those  genera  with 
distributional  centers  in  temperate  montane  habitats  or  of  limited  lowland  tropi- 
cal ranges,  e.g.,  Idionycteris,  Neotoma,  Sciurus,  Sigmodon  and  Baiomys.  On  the 
other  hand,  some  of  the  species  selected  may  range  into  montane  habitats  or 
reach  temperate  latitudes,  such  as  Marmosa  mexicana  and  Didelphis  mar- 
supialis.  In  general  the  species  hsted  in  Table  2  are  of  wide  distribution  in 
lowland  tropical  America.  Although  they  occupy  tropical  environments  of 
the  Mexican  escarpment  and  coastal  plain,  we  exclude  Baiomys  and  Sigmodon 
because  their  phylogeny  indicates  a  north  temperate  origin  and  in  the  case  of 
Baiomys  because  it  does  not  range  extensively  into  Central  America.  Clearly 
the  question  of  "tropicality"  can  be  vexing.  As  one  might  expect  the  bats  have 
much  more  extensive  ranges  than  the  small  terrestrial  mammals.  The  faunas 
of  Trinidad  and  southern  Tamaulipas  share  18  species  of  bats,  but  none  of 
rodents. 


NORTHERN      LIMIT    OF    TROPICAL     MAMMALS 


10  20  30  40    VEGETATION 

NUMBER    OF    TROPICAL    SPECIES  TYPE 


Fig.  1. — Relationship  between  lowland  tropical  mammals  and  latitude  in  northeastern 
Mexico.  Known  range  limits  for  43  species  listed  in  Table  2  are  shown  on  the  map.  Major 
vegetation  types  are  indicated  at  the  right.  Tropical  Evergreen  Forest  is  abbreviated  to  TEF. 


520 


Feb.,  1959  KOOPMAN  AND  MARTIN— MAMMALS  OF  EASTERN  MEXICO  9 

The  general  relationship  between  vegetation,  latitude  and  tropical  fauna  is 
shown  on  Fig.  1.  In  southern  Tamaulipas  a  rapid  "tliinning"  of  tropical  forms 
is  evident.  Between  23°  and  24°  north  latitude  the  following  17  genera  find 
their  range  limits:  Philander,  Marmosa,  Chilonycteris,  Pteronotus,  Micro- 
nycteris,  Macrotus,  Glossophaga,  Sturnira,  Artibeus,  Enchisthenes,  Centurio, 
Natalus,  Wwgeesa,  Molossus,  Heterogeomys,  Eira  and  Mazama.  At  this  latitude 
(24°  north)  the  Tropical  Deciduous  Forest,  well  developed  and  widespread 
east  of  the  Sierra  de  Tamaulipas  and  the  Sierra  Madre  Oriental,  disappears. 
Small,  perhaps  relict,  stands  of  Cloud  Forest  and  Tropical  Evergreen  Forest  in 
the  Gomez  Farias  region  also  enrich  the  environmental  opportunity  for  tropical 
mammals.  However,  these  habitats,  especially  the  Tropical  Evergreen  Forest, 
are  more  extensive  in  southeastern  San  Luis  Potosi  and  northern  Veracruz. 

In  this  region  seven  genera  terminate:  Carollia,  Tamandua,  Coendou,  Cuni- 
culus,  Potos,  Galictis  and  Ateles.  Although  the  vegetation  near  Xilitla,  San  Luis 
Potosi,  has  been  designated  as  Rainforest,  it  seems  preferable  to  reserve  that 
term  for  the  more  luxuriant  forests  of  southern  Veracruz  with  their  short  dry 
season.  Lowland  tropical  forests  near  Xilitla  appear  taller  and  richer  than 
those  of  southern  Tamaulipas;  however,  the  area  has  suffered  a  long  history 
of  intensive  Huastecan  agriculture.  Almost  certainly  the  primeval  fauna  of 
southeastern  San  Luis  Potosi  included  a  larger  number  of  tropical  genera  at 
their  northern  limit. 

While  we  have  not  attempted  to  represent  tropical  distributions  and  plant 
formations  south  of  San  Luis  Potosi,  the  following  genera  or  subgenera  approach 
their  northern  limit  in  southern  Veracruz:  Caluromys,  Vampyrum,  Rhynchiscus, 
Centronycteris,  Mimon,  Chrotopterus,  Hylonycteris,  Chiroderma,  Alouatta, 
Tylomys,  Dasyprocta,  Tayassu,  Tapirella  and  Jentinkia.  Is  there  a  relationship 
between  these  and  the  northern  limit  of  Rainforest  (see  Leopold,  1950)? 

Extending  from  central  Tamaulipas  northward  to  Nuevo  Leon  and  southern 
Texas  is  a  rather  barren  Thorn  Forest  and  Thorn  Scrub.  Gradually  these  arid 
habitats  lose  their  tropical  character  as  the  Rio  Grande  Valley  is  approached. 
By  comparison  with  plant  formations  to  the  south,  this  environment  is  poor 
in  tropical  fauna.  The  shift  from  tropical  to  temperate  thorn  scrub  involves 
no  sharp  faunal  boundary  among  the  mammals.  Oryzomys  couesi  and  Liomys 
irroTOtus  are  among  the  forms  reaching  southern  Texas.  At  this  latitude  the 
herpetological  fauna  includes  such  tropical  genera  as  Coniophanes,  Drymobius, 
Leptodeira,  Smilisca  and  Hypopacus.  However,  among  the  reptiles  and  am- 
phibians, as  well  as  the  mammals,  the  greatest  reduction  in  tropical  fauna  is 
found  in  southern  Tamaulipas  (Martin,  1958). 

DISCUSSION 

Although  our  analysis  in  confined  to  eastern  Mexico,  some  interesting  com- 
parisons can  be  made  with  the  tropical  biota  of  the  Pacific  Coast.  Arid  tropical 
vegetation  and  the  genera  Macrotus,  Balantiopteryx,  Chilonycteris,  Pteronotus, 
Mormoops,  Glossophaga,  Desmodus,  Natalus,  Rhogeesa  and  Nasua  extend  far- 


521 


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JOURNAL  OF  MAMMALOGY 


Vol.  40,  No.  1 


Table  2. — Northern  limits  of  neotropical  mammals 


LOCALITY  AND  APPROX.  ELEV. 


REFERENCE 


SPECIES    PRESENT 


San  Luis  Potosi: 

A.  Tamazunchale,  120  m. 

B.  Xilitla  and  vicinity 
630-1350  m. 


Dalquest,  1953 
Dalquest,  1953 


1.  Tamandua  tetradactyla 

2.  Sturnira  ludovici 

3.  Coendou  mexicanum 

4.  Cuniculus  paca 

5.  Potos  flavus 

6.  Galictis  canaster 


C.  Rio  Verde,  990  m. 

Dalquest,  1953 

7. 

Molosstis  major 

D.  VaUes,  75  m. 

Koopman,  1956 

8. 

Balantiopteryx  plicata 

E.  EI  Salto,  660  m. 

Dalquest,  1953 

9. 

Carollia  perspicillata 

Tamaulipas: 

F,  Rancho  del  Cielo 

Goodwin,  1954 

10. 

Marmosa  mexicana 

and  vicinity, 

Hooper,  1953 

11. 

Enchisthenes  harti 

1000-1320  m. 

present  report 

12. 

Oryzomys  alfaroi 

13. 

Reithrodontomys 
(Aporodon)  mexicanus 

14. 

Mazama  americana 

Pano  Ayuctle,  100  m. 

Goodwin,  1954 

15. 

Micronycteris  megalotis 

Hooper,  1953 

16. 

Sturnira  lilium 

de  la  Torre,  1954 

17. 

Artibeus  jamaicensis 

18. 

A.  lituratus 

19. 

A.  cinereus 

20. 

Eira  barbara 

G.  2  km.  W  of  El  Carrizo, 

Baker,  1951 

21. 

Philander  opossum 

800  m. 

22. 

Heterogeomys  hispidus 

H.  Jaumave,  730  m. 

UMMZ  specimens 

23. 

Macrotus  mexicanus 

I.  10-16  mi.  WSW 

Anderson,  1956 

24. 

Chilonycteris  parnellii 

Piedra,  400  m. 

25. 

Glossophaga  soricina 

26. 

Centurio  senex 

27. 

Natalus  mexicanus 

J.  2  mi.  S  Victoria, 

Davis,  1951 

28. 

Molossus  rufus 

400  m. 

K.  30  km.  NW  Victoria, 

Malaga-Alba,  1954 

29. 

Diphylla  ecaudata 

1000  m. 

L.  La  Pesca,  10  m. 

Anderson,  1956 

30. 

Rhogeesa  tumida 

M.  Rancho  Santa  Rosa, 

Anderson,  1956 

31. 

Pteronotus  davyi 

260  m. 

N.  8  mi.  SW  Padilla, 

Lawrence,  1947 

32. 

Oryzomys  melanotis 

100  m. 

Nuevo  Ledn: 

O.  25  km.  SW  Linares, 

Malaga-Alba,  1954 

32. 

Desmodus  rotundus 

700  m. 

P.  20  mi.  NW  General 

Hooper,  1947 

33. 

Oryzomys  fulvescens 

Teran,  300  m. 

Tera.^: 

Q.  Hidalgo  Co.,  60  m. 

Blair,  1952b 

34. 

Oryzomys  couesi 

R.  Raymondville,  30  m. 

Blair,  19526 

35. 

Liomys  irroratus 

522 


Feb.,  1959         KOOPMAN  AND  MARTIN— MAMMALS  OF  EASTERN  MEXICO  H 

Table  2. — Continued 


LOCALITY  AND  APPROX.  ELEV. 


REFERENCE 


SPECIES    PRESENT 


Coahuila  and  West  Texas: 

Edwards  Plateau,  Texas: 
Eastern  United  States: 


Baker,  1956 
Miller  and 
KeUogg,  1955 
Blair,  1952a 
Blair,  1952& 
Miller  and 
KeUogg,  1955 


36.  Choeronycteris  mexicana 

37.  Leptonycteris  nivalis 

38.  Mormoops  megalophylla 

39.  Nasua  narica 

40.  Dasypus  novemcinctus 

41.  Didelphis  marsupialis 


ther  north  on  the  western  side.  On  the  other  hand  the  humid  tropical  fauna  and 
plant  formations,  e.g.,  Cloud  Forest,  Tropical  Evergreen  Forest  and  Rainforest, 
are  absent  or  poorly  represented  on  the  Pacific  slope  north  of  Chiapas.  As  a 
general  rule  for  those  species  or  vicariant  species  occurring  on  both  sides  of 
Mexico,  the  arid  tropical  forms  range  farther  north  on  the  west,  and  the  humid 
tropical  forms  farther  north  on  the  eastern  side.  This  pattern  is  evident  also  in 
the  distribution  of  lowland  tropical  birds,  reptiles,  insects,  etc. 

Other  than  noting  a  rather  close  "fit,"  it  is  beyond  our  purpose  to  explore  the 
causal  relationship  between  formation  and  fauna.  In  brief  our  conclusions 
may  be  summarized  as  follows: 

1.  The  decline  of  the  tropical  fauna  in  eastern  Mexico  corresponds  with  the 
vegetation  gradient. 

2.  Where  the  vegetation  gradient  steepens  and  a  plant  formation  is  lost, 
one  finds  a  variety  of  tropical  animals  at  their  range  limits. 

3.  In  southern  Tamauhpas  the  northern  limit  of  many  tropical  mammals 
corresponds  roughly  to  the  boundary  of  Tropical  Deciduous  Forest.  Contribu- 
ting to  the  rich  tropical  fauna  of  the  Gomez  Farias  region  are  relict  outposts 
of  Tropical  Evergreen  Forest  and  Cloud  Forest. 

4.  The  problem  of  establishing  a  Nearctic-Neotropical  faunal  boundary  in 
eastern  Mexico  can  be  approached  reaUstically  in  terms  of  steps  in  an  environ- 
mental gradient. 

ACKNOWLEDGMENTS 

First  we  wish  to  thank  Dr.  Byron  E.  Harrell  for  assistance  in  the  field  work.  We  are 
indebted  to  the  Mammal  Department  of  the  American  Museum  of  Natirral  History  for 
use  of  their  facilities  including  collections  of  comparative  material.  Mr.  Sydney  Anderson 
of  the  Museum  of  Natural  History,  University  of  Kansas,  and  Dr.  William  H.  Burt,  Museirai 
of  Zoology,  University  of  Michigan,  kindly  advised  us  concerning  specimens  in  their  care. 

LITERATURE  CITED 

Anderson,  Sydney.     1956.     Extensions  of  known  ranges  of  Mexican  bats.    Univ.  Kans. 

Publ.  Mus.  Nat.  Hist.,  9:  349-351. 
Baker,  Rollin  H.     1951.     Mammals  from  Tamauhpas,  Mexico.    Univ.  Kans.  Publ.  Mus. 

Nat  Hist.,  5:  207-218. 


523 


12  JOURNAL  OF  MAMMALOGY  Vol.  40,  No.  1 

.     1956.     Mammals  of  Coahuila,   Mexico.    Univ.   Kans.   Publ.   Mus.   Nat.   Hist., 

9:  125-335. 
Blair,  W.  Frank.     1952a.     Bats  of  the  Edwards  Plateau  in  Central  Texas.    Tex.  Jour. 

Sci.,  4:  95-98. 
.     19526.     Mammals  of  the  Tamaulipan  Biotic  Province  in  Texas.  Tex.  Jour.  Sci., 

4:  230-250. 
Dalquest,  Walter  W.     1953.     Mammals  of  the  Mexican  State  of  San  Luis  Potosi.    La. 

State  Univ.  Studies,  No.  1:  1-112. 
Davis,  William  B.     1944.     Notes  on  Mexican  mammals.    Jour.  Mamm.,  25:   370—403. 
.     1951.     Bat,  Molossus  nigricans,  eaten  by  the  rat  snake,  Elaphe  laeta.    Jour. 

Mamm.,  32:  219. 
GooDWTN,  George  G.     1954.     Mammals   from   Mexico   collected  by   Marian   Martin  for 

the  American  Museum  of  Natural  History.   Amer.  Mus.  Novit.,  No.  1689:  1-16. 
Hooper,  Emmet  T.     1947.     Notes  on  Mexican  mammals.   Jour.  Mamm.,  28:  40-57. 
.     1953.     Notes  on  mammals  of  Tamauhpas,  Mexico.   Occ.  Pap.  Mus.  Zool.,  Univ. 

Mich.,  No.  544:  1-12. 
Koopman,  Karl  F.     1955.     A  new  subspecies  of  Chilonycteris  from  the  West  Indies  and 

a  discussion  of  the  mammals  of  La  Gonave.   Jour.  Mamm.,  36:  109-113. 
.     1956.     Bats  from  San  Luis  Potosi  with  a  new  record  for  Balantiopteryx  plicata. 

Jour.  Mamm.,  37:  547-548. 
Lawrence,   Barbara.     1947.     A  new  race  of  Oryzomys  from  Tamauhpas.    Proc.   New 

England  Zool.  Club,  24:  101-103. 
Leopold,  A.  Starker.     1950.     Vegetation  zones  of  Mexico.    Ecology,  31:  507-518. 
Malaga-Alba,  Aurelio.     1954.     Vampire  bat  as  carrier  of  rabies.    Amer.  Jour.   Pubhc 

Health,  44:  909-918. 
Martin,  Paul  S.     1958.     Herpetology  and  biogeography  of  the   G6mez   Farias   region, 

Mexico.    Misc.  Publ.  Mus.  Zool.,  Univ.  Mich.  In  press. 
Miller,    Gerrit    S.,    Jr.     1897.     Revision    of    the    North    American    bats    of   the    family 

Vespertilionidae.    N.  Amer.  Fauna  13:   1-155. 
and  Remustgton  Kellogg.     1955.     List  of  North  American  Recent  mammals. 

Bull.  U.S.  Nat.  Mus.,  205:   1-954. 
Orr,  Robert  T.     1954.     Natural  history  of  the  paUid  bat,  Antrozom  pallidus  (Le  Conte). 

Proc.  Calif.  Acad.  Sci.,  28:  165-246. 
Torre,  Lins  de  la.     1954.     Bats  from  southern  Tamaulipas,  Mexico.    Jotu.  Mamm.,  35: 

113-116. 
.     1955.     Bats  from  Guerrero,  Jalisco,  and  Oaxaca,   Mexico.    Fieldiana:     Zool., 

37:  695-703. 

Dept.  of  Biology,  Queens  College,  Flushing,  New  York  and  Ijistitut  de  Biologie,  Universite 
de  Montreal,  Montreal,  Canada.   Received  August  6,  1957. 


524 


ZOOGEOGRAPHY  OF  THE  MONTANE  MAMMALS  OF  COLORADO 

By  James  S.  Findley  and  Sydney  Anderson 

In  Colorado  the  distribution  of  montane  or  boreal  habitats  is  at  present  closely- 
associated  with  the  local  chmate  produced  by  the  mountains.  Peculiarities  of  this 
habitat  are  high  precipitation,  both  in  winter  and  summer,  cool  temperatures,  a 
continuous  water  supply  and  a  coniferous  forest.  Certain  mammals  are  more  or 
less  restricted  in  geographic  range,  in  this  part  of  the  continent,  to  the  mountains. 

In  Pleistocene  time  the  distribution  of  boreal  habitat  and  hence  of  boreal 
mammals  has  undoubtedly  fluctuated  widely  with  the  advances  and  retreats 
of  continental  and  alpine  glaciers.  The  contemporary  pattern  of  distribution  is, 
at  least  in  part,  a  result  of  the  most  recent  major  glacial  advance  and  retreat 
which  took  place  in  the  Wisconsinan  Age.  It  seems  probable  to  us  that  most 
contemporary  subspecies  have  differentiated  in  late  Pleistocene  time;  otherwise 
the  frequent  correspondence  of  their  ranges  with  current  topographical  and 
ecological  features,  which  stem  from  late  Pleistocene  events  in  many  cases,  seems 
inexplicable.  In  the  western  United  States  the  Boreal  Zone  is  found  at  higher 
and  higher  elevations  as  one  proceeds  southward  until  it  is  scattered  on  isolated 
mountain  peaks.  The  presence  of  isolated  populations  of  boreal  mammals  on 
some  of  these  mountains  is  evidence  of  a  former  displacement  southward  and 
downward  in  altitude  of  the  Boreal  Zone  in  a  glacial  age,  presumably  the  Wis- 
consin, and  subsequent  elevation  of  the  Boreal  Zone  in  altitude  and  latitude  in  an 
ensuing  interglacial  interval,  presumably  the  Recent.  These  southern,  marginal 
populations  would  have  been  the  first  to  become  isolated  with  the  retreat  of 
the  ice. 

The  separation  of  boreal  habitat  in  the  mountains  of  Colorado  from  boreal 
habitat  in  the  Uinta  and  Wasatch  Mountains  of  Utah  and  the  mountains  of 
northwestern  Wyoming  is  probably  of  later  origin  than  is  the  isolation  of  the 
southern  boreal  "islands."  We  have  studied  the  boreal  mammals  of  Colorado  in 
their  relation  to  those  of  Utah  and  northwestern  Wyoming.  These  mammals  may 
be  grouped  according  to  the  pattern  of  their  variation  and  distribution  as  follows: 

Group  I. — Rare,  extinct,  or  insufficiently  known  to  use  in  this  study:  Alces 
americana,  Ovis  canadensis,  Lepus  americanus,  Sylvilagus  nuttallii,  Phenacomys 
intermedius,  Mustela  erminea,  and  Gulo  luscus. 

Group  II. — Occurring  only  north  and  west  of  the  barrier  formed  by  the  Wyo- 
ming Basin  and  the  Green  River  (Fig.  1) :  Eutamias  amoenus,  Glaucomys  sahrinus, 
Microtus  richardsoni,   and  Martes  pennanti. 

Group  III. — Occurring  only  southeast  of  the  above  mentioned  barrier:  Sciurus 
aberti. 

Group  IV.— Occurring  in  the  mountains  of  northwestern  Wyoming  and  the 
mountains  of  Colorado  as  a  single  subspecies;  this  group  includes  eight  of  fifteen 
species  that  occur  on  both  sides  of  the  barrier  shown  in  Figure  1 :  Sorex  cinereus, 
Sorex  vagrans,  Sorex  palustris,  Clethrionomys  gapperi,  Microtus  montanus,  Micro- 
tus longicaitdus,  Zapus  princeps,  and  Erethizon  dorsatum. 

Group  V. — Occurring  in  the  mountains  north  of  the  Wyoming  Basin  and  the 
mountains  southeast  of  the  basin,  but  as  different  subspecies:  Martes  americana, 


525 


Feb.,  1956 


FINDLEY  AND  ANDERSON— MONTANE  MAMMALS 


81 


105 


Fig.  1. — The  distribution  of  the  Boreal  Zone  (diagonally  lined)  in  Wyoming,  Colorado, 
and  Utah.  The  major  barrier  (consisting  of  the  Wyoming  Basin  and  the  Green  River)  sepa- 
rating the  boreal  habitat  in  Colorado  from  the  mountains  of  Utah  and  northwestern  Wyo- 
ming is  shown. 

Marmota  flaviventris,  Citellus  lateralis,  Eutamias  vmbrinus,  Tamiasciurus  hud- 
sonicus,  Microtus  pennsylvanicus,  and  Ochotona  princeps. 

In  Figure  1  we  have  mapped  the  distribution  of  boreal  habitat  and  the  barrier 
discussed.  We  note  that  the  arboreal  species,  namely,  the  two  tree  squirrels, 
the  flying  squirrel,  the  marten,  and  the  fisher,  occur  either  on  one  side  of  the 
barrier  only  or  else  have  distinct  northern  and  southeastern  subspecies.  The  other 
species  that  occur  only  on  one  side  of  the  barrier  or  that  have  separate  sub- 
species on  the  north  side  and  on  the  southeast  side  of  the  Wyoming  Basin  are: 
Marmota  flaviventris,  Ochotona  princeps,  Microtus  richardsoni,  Microtus  pennsyl- 
vanicus, Citellus  lateralis,  and  two  species  of  Eutamias.  The  species  named  im- 
mediately above  and  the  arboreal  species  (in  comparison  to  the  next  group  of 
species  to  be  discussed)  seem  to  be  relatively  restricted  in  the  range  of  habitats 
that  they  utilize.  The  pattern  in  the  chipmunks  is  complicated  by  other  species 
of  less  montane  chipmunks  whose  presence  may  act  as  a  biological  barrier.  The 


526 


82  JOURNAL  OF  MAMMALOGY  Vol.  S7,No.  1 

red  squirrel,  the  marten,  and  the  golden-mantled  ground  squirrel  have  popula- 
tions in  Colorado  and  northern  Utah  that  are  alike  and  differ  from  corresponding 
populations  on  the  northern  side  of  the  Wyoming  Basin. 

The  species  that  have  a  single  subspecies  occurring  on  both  the  north  side 
and  the  southeast  side  of  the  Wj^oming  Basin  are  as  follows:  three  species  of 
shrews,  three  microtines,  the  jumping  mouse,  and  the  porcupine.  The  porcupine 
is  a  ubiquitous  creature,  prone  to  wander.  The  other  seven  species  are  small 
mammals  which  may  migrate  by  way  of  narrow  avenues  found  along  stream- 
courses  where  the  water  draining  from  montane  areas  supports  growths  of  brush, 
scrub  willow,  and  grasses  and  sedges.  Furthermore,  these  species  do  not  seem  to 
be  dependent  upon  forests  or  forest-edge  communities.  If  the  montane  mammals 
here  dealt  with  are  arranged  in  order  of  their  decreasing  dependence  upon  mon- 
tane conditions  it  is  seen  that  those  kinds  appearing  early  in  the  list  are  those  that 
occur  only  on  one  side  of  the  barrier  shown  in  Figure  1  or  those  that  have  distinct 
northern  and  southeastern  subspecies  (that  is,  belong  in  Group  V).  Those  that 
appear  later  in  such  a  list  are  in  general  those  that  are  subspecifically  the  same 
north  and  southeast  of  the  Wyoming  Basin  (Group  IV).  It  might  be  concluded 
that  montane  meadow  and  streamside  habitats  connected  the  southern  and 
central  Rockies  across  the  Wyoming  Basin  long  after  they  ceased  to  be  con- 
nected by  continuous  forests.  The  red-backed  mouse,  Clethrionomys,  is  restricted 
to  the  forested  areas  of  the  mountains  more  than  the  other  species.  Investigation 
of  the  most  recent  work  on  Clethrionomys  (Cockrum  and  Fitch,  Univ.  Kansas 
Publ.,  ]\Ius.  Nat.  Hist.,  5:  283,  1952),  reveals  that  these  authors  regarded  north- 
western Wyoming  and  the  Bighorn  Mountains  as  centers  of  incipient  subspecies. 
Judging  by  their  comments  on  C.  gapperi  galei  and  on  C.  g.  uintaensis  in  Utah 
we  feel  that  the  four  populations,  (1)  in  the  Uinta  Mountains,  (2)  in  north- 
western Wyoming,  (3)  in  the  Bighorn  Mountains,  and  (4)  in  northern  Colorado, 
are  dilTerentiated  from  one  another  and  might  be  regarded  equally  well  as  one  or 
as  four  subspecies.  The  latter  supposition  would  place  them  in  Group  V  and  would 
obviate  the  seeming  inconsistency. 

On  the  basis  of  the  information  presented  above  it  seems  that:  (1)  The  ranges 
of  montane  species  are  correlated  with  their  dependence  upon  special  habitats; 
the  more  dependent  species  are  more  restricted  in  range,  both  locally 
and  regionally.  (2)  The  more  dependent,  and  therefore  relatively  restricted, 
species  show  more  differentiation  on  opposite  sides  of  the  Wyoming  Basin  than 
the  species  that  are  less  restricted.  (3)  The  closest  affinities  of  the  boreal  mammals 
in  the  Rocky  Mountains  of  Colorado  are  with  the  boreal  mammals  of  the  Uinta 
Mountains  across  the  Green  River  Canyon  rather  than  with  those  of  the  central 
Rocky  Mountains  to  the  north  of  the  Wyoming  Basin.  (4)  The  discontinuity  in 
the  boreal  forest  produced  by  the  erosion  of  the  Green  River  Canyon  has  become 
important  as  a  barrier  to  montane  mammals  later  than  the  discontinuity  caused 
by  the  desiccation  of  the  Wyoming  Basin. 

Department  of  Zoology,  University  of  New  Mexico,  Albuquerque,  and  Museum 
of  Natural  History,  University  of  Kansas,  Lawrence.  Received  February  6,  1955. 


527 


Mammals  from  Isla  Cozumel,  Mexico, 

With  Description  of  a  New  Species 

of  Harvest  Mouse 

BY 
J.  KNOX  JONES,  JE.,  AND  TIMOTHY  E.  LAWLOR 

Isla  Cozumel,  or  Cozumel  Island,  lies  in  the  Gulf  of  Mexico  ap- 
proximately 16  kilometers  ofiF  the  east  coast  of  the  Yucatan  Penin- 
sula. Administratively,  the  island  is  attached  to  the  Mexican  Ter- 
ritory of  Quintana  Roo.  The  strait  that  separates  Cozumel  from 
the  mainland  reaches  a  depth  of  more  than  300  meters,  and  the 
current  in  the  strait  is  swift.  The  island  itself  is  approximately  45 
kilometers  long  (northeast-southwest)  and  averages  about  14  kilo- 
meters wide.  "It  is  composed  of  limestone  and  its  greatest  eleva- 
tion is  about  10  meters  above  the  sea"  (Paynter,  1955:8).  Vegeta- 
tionally,  Cozumel  supports  mostly  scrubby  deciduous  forest  and 
mangrove  swamps. 

From  August  7  to  11,  1962,  a  field  party  from  the  Museum  of  Nat- 
ural History  of  The  University  of  Kansas  collected  vertebrate 
animals  in  the  vicinity  of  San  Miguel  on  die  west  coast  of  Cozumel. 
The  present  report  concerns  the  mammals  obtained  or  observed 
by  the  party,  among  which  are  several  species  previously  unreported 
from  the  island.  One  of  these  is  a  new  harvest  mouse  of  the  genus 
Reithrodontomijs  that  is  named  and  described  beyond.  Mention 
is  made  also  of  species  previously  reported  from  Cozumel,  especially 
by  Hall  and  Kelson  (1959),  Koopman  (1959),  Merriam  (1901),  and 
Thomas  (1888). 

Field  operations  on  Cozumel  were  supported  by  funds  made  available 
through  a  contract  ( DA-49-193-MD-2215)  between  the  U.  S.  Aniiy's  Medical 
Research  and  Development  Command  and  The  University  of  Kansas. 

Didelphis  tnarsupialis  cozumelae  Merriam,  1901. — Ten  specimens  (91428- 
37),  including  six  pouch  young,  were  taken  3/2  km.  N  San  Miguel,  where 
opossums  were  seen  nightly  at  a  garbage  dump.  The  female  that  carried  the 
si.\  young  was  obtained  on  August  8;  the  young  weighed  an  a\erage  of  18.4 
(17^6-19.5)  grams. 

We  tentatively  retain  the  subspecific  name  cozumelae  for  the  insular  opos- 
sums. Comparison  of  our  material  with  specimens  of  D.  in.  i/ticatancnsis  from 
the  adjacent  mainland  fails  to  support  Merriam's  (1901:102)  contention  that 
the  two  differ  in  certain  cranial  features  or  that  cozumelae  is  the  larger  in 
size  of  body.     The  tail  does,  however,  average  shorter  in  relation  to  length  of 

(411) 


528 


412  Unu'ersity  of  Kansas  Publs.,  Mus.  Nat.  Hist. 

body  than  in  specimens  from  the  mainland,  and  the  white  tip  on  the  tail  is 
noticeably  shorter  (one-half  to  two-thirds  as  long). 

Selected  measurements  of  an  adult  male  and  the  largest  axailable  female 
(the  one  with  young)  are,  respectively:  total  length,  770,  633;  length  of  tail, 
319,  300;  length  of  hind  foot,  60,  53;  length  of  ear,  54,  52;  greatest  length  of 
skull,  115.1,  90.7;  zygomatic  breadth,  63.5,  45.2;  palatal  length,  65.7,  54.8; 
length  of  M1-M4,  19.5,  17.9. 

Micronycteris  megalotin  mexicana  Miller,  1898. — Our  only  specimen 
(91539),  a  female  in  juvenal  pelage  and  with  unfused  phalangeal  epiphyses, 
was  taken  in  a  mist  net  stretched  between  two  palm  trees  adjacent  to  the 
cottage  in  which  we  stayed.  Goldman  (1951:443)  earlier  listed  this  species 
from  Cozumel  under  the  name  Macroius  pijgmaeus. 

Artibeus  jamaicensis  yucatanicus  J.  A.  Allen,  1904. — Judging  from  our 
experience,  this  species  is  the  commonest  of  the  bats  occurring  on  Cozumel. 
Eighteen  individuals  were  collected  as  follows:  4  km.  N  San  Miguel,  6 
(91724-29);  3)^  km.  N  San  Miguel,  12  (91730-40,  91781).  All  specimens 
taken  were  netted,  either  along  small  roads  through  the  scrubby  forest  or  among 
coconut  palms  adjacent  to  residences  near  the  beach.  Five  of  11  females  ob- 
tained were  lactating;  the  testes  of  one  male  measured  10  mm.  Several  authors 
previously  have  reported  this  bat  from  the  island. 

Artibeus  lituratus  palmarum  Allen  and  Chapman,  1897. — One  specimen 
(91780),  a  male  having  testes  measuring  6  mm.,  was  netted  along  with 
several  individuals  of  A.  jainaicensis  among  coconut  palms  SM  km.  N  San 
Miguel.     This  species  has  not  been  reported  previously  from  Cozumel. 

Artibeus  phaeotis  phaeotis  (Miller,  1902). — A  male  and  two  females  of 
this  small  fruit-eating  bat  were  trapped  in  mist  nets  stretched  across  a  narrow 
road  in  the  forest  4  km.  N  (91790)  and  3)i  km.  N  (91791-92)  San  Miguel. 
Each  of  the  females  carried  a  single  embryo  ( 23  and  25  mm.  crown-rump ) . 
Although  this  species  long  has  been  known  from  the  Yucatan  Peninsula,  it 
was  not  fomierly  known  from  Cozumel. 

Previous  authors  ( Hershkovitz,  1949:449,  Dalquest,  1953:64,  and  Davis, 
1958:164,  among  others)  have  regarded  A.  p.  phaeotis  (type  locality,  Chichen- 
Itza,  Yucatan)  as  a  subspecies  of  Artibeus  cinereus.  Apparently  none  of  the 
authors  who  thus  treated  plmeotis  examined  the  holotype,  which  actually  is 
identical  with  the  species  later  described  by  Andersen  (1906:422)  as  Artibeus 
turpis  (type  locality,  Teapa,  Tabasco).  Therefore,  A.  p.  phaeotis  replaces  A.  t. 
iurpis  as  the  correct  name  for  the  bat  of  the  Caribbean  lowlands  of  southern 
Mexico  and  adjacent  areas  that  is  characterized  by  its  small  size,  relatively 
broad  and  naked  uropatagium,  and  short,  up-turned  rostrum.  The  slightK' 
smaller  subspecies  of  Pacific  coastal  areas  (see  Davis,  1958:163)  henceforth 
should  bear  the  name  Artibeus  phaeotis  nanus. 

We  are  grateful  to  Dr.  C.  O.  Handley,  Jr.,  of  the  U.  S.  National  Museum, 
who  currently  is  revising  the  genus  Artibeus,  for  allowing  one  of  us  (Jones)  to 
examine  the  holotype  of  phaeotis.  Our  attention  first  was  drawn  to  this  mat- 
ter when  we  discovered  that  all  individuals  of  small  Artibeus  in  our  collection 
from  the  Yucatan  Peninsula  resembled  "turpis,"  which  was  not  reported  from 
there,  rather  than  "cinereus,"  which  was  said  to  occur  there. 

Measurements  of  the  male  and  two  females  are,  respectively:  total  length, 
57,  54,  58;  length  of  hind  foot,  12,  10,  11;  length  of  ear,  14,  16,  17;  length  of 


529 


Mammals  from  Isla  Cozumel,  Mexico  413 

forearm,  38.2,  38.3,  40.8;  greatest  length  of  skull,  19.6,  19.1,  19.3;  zygomatic 
breadth,  11.5,  11.7,  11.7;  length  of  maxillary  tooth-row,  6.0,  5.8,  5.9. 

Natalus  stramineus  saturatus  Dalquest  and  Hall,  1949. — This  species,  previ- 
ously unreported  from  the  island,  is  represented  in  the  U.  S.  National  Museum 
by  32  specimens  in  alcohol  from  San  Miguel. 

Oryzomys  palustris  cozumelae  Merriam,  1901. — Rice  rats  were  abundant 
in  tangled,  second-growth  brush  and  vines.  Thirty-six  specimens  were  col- 
lected from  3  km.  N  (92185-86)  and  3)i  km.  N  (92168-84,  92187-203)  San 
Miguel.  A  female  obtained  on  August  8  carried  three  embryos  that  measured 
15mm.  (crown-rump)  and  our  sample  contains  many  two-thirds  to  three- 
fourths  grown  young. 

Up  to  now,  O.  p.  cozumelae  has  been  regarded  as  a  distinct  species,  al- 
though its  close  relationship  with  O.  palustris  of  the  adjacent  mainland  has 
been  recognized  (see  Goldman,  1918:43).  None  of  the  specimens  among  our 
material  are  as  large  as  the  holotype  of  cozumelae,  but  a  number  fall  within 
the  range  of  variation  cited  for  adults  by  Goldman  ( loc.  cit. ) .  When  our 
specimens  were  compared  with  individuals  of  O.  p.  couesi  from  the  Yucatan 
Peninsula,  we  found  that  cozumelae  differed  noticeably  only  in  being  larger 
externally;  cranially,  couesi  and  cozumelae  differ  only  in  minor  details  (for 
example,  the  skull  of  cozumelae  averages  slightly  larger,  is  less  arched  over 
the  orbits,  and  has  heavier  teeth  and  larger  nasals),  and  the  latter  averages 
only  slightly  darker  than  mainland  specimens.  Furthermore,  adults  of  co- 
zumelae do  not  exceed  in  external  size  individuals  from  several  of  the  named 
populations  of  O.  palustris.  For  all  these  reasons,  and  because  cozumelae  long 
has  been  recognized  as  only  an  insular  relative  of  palustris,  we  employ  the 
name  Oryzomys  palustris  cozumelae  for  it.  We  feel  the  relationships  of  the 
insular  population  are  best  reflected  by  such  usage. 

Reithrodontomys  spectabilis  new  species 

Holotype. — Adult  male,  skin  and  skull,  no.  92294  Museum  of  Natural  His- 
tory, The  University  of  Kansas,  from  2/2  km.  N  San  Miguel,  Isla  Cozumel, 
Quintana  Roo;  obtained  by  Ticul  Alvarez  on  August  8,  1962  (original  no.  848). 

Distribution. — Known  only  from  Cozumel  Island. 

Diagnosis. — Size  large  both  externally  and  cranially  (see  measurements); 
tail  long  in  relation  to  head  and  body  (134-148  per  cent  in  adults),  scantily 
haired;  pelage  short  and  relatively  sparse;  upper  parts  brownish  ochraceous 
over-all,  brighter  ochraceous  on  sides;  underparts  grayish  white,  the  individual 
hairs  wlaite  terminally  and  plumbeous  basally;  pinkish  buff  pectoral  spot  some- 
times present;  tail  dark  brown  above,  only  slightly  paler  below;  braincase 
relatively  flattened  and  uninflated;  zygomatic  arches  broad  and  strong;  rostrum 
relatively  short  and  broad;  mesopterygoid  fossa  broad;  auditory  bullae  large 
but  only  moderately  inflated;  incisive  foramina  rarely  reaching  level  of  Ml; 
teeth  huge;  first  and  second  molars  typical  of  the  subgenus  Aporodon  in 
having  well  developed  mesolophs(ids)  and  mesostyles(ids);  third  lower  molar 
essentially  a  smaller  replica  of  first  two;  baculum  long  ( 9.5  and  10.9  mm.  in 
two  adult  males),  slender,  curved  dorsally  at  the  distal  end,  broadly  arrow- 
shaped  basally  (width  of  base  1.1  and  1.2  mm.  in  the  two  adult  bacula 
studied),  possibly  largest  among  members  of  genus.  The  skull  and  teeth  are 
illustrated  in  Figure  1. 


530 


414 


University  of  Kansas  Publs.,  Mus.  Nat.  Hist. 


Fig.   1.    Skull  and  teeth  of  Reithrodontomys  spectahilis.     Right  upper  (A)  and 

left  lower  (B)  molars  of  KU  92293  (x  15),  and  dorsal  (C)  and  ventral  (D) 

views  of  skull  of  holotype,  KU  92294    (x3).     T.  H.  Swearingen  made  the 

drawings  from  photographs  by  J.  F.  Downhower. 

Measurements. — E.\ternal  and  cranial  measurements  of  the  holotype  followed 
by  average  and  (in  parentheses)  extreme  measurements  of  eight  specimens 
(four  males  and  four  females,  including  the  tvpe)  are:  total  length,  216,  213.8 
(205-221);  length  of  tail,  124,  125.7  (121-132);  length  of  hind  foot,  22,  21.3 
(20-22);  weight  (in  grams),  20.6,  20.2  (18.1-21.4);  greatest  length  of  .skull, 
24.7,  25.2  (24.6-26.2);  zygomatic  breadth,  12.2,  12.3  (11.8-12.7);  interorbital 
breadth,  3.7,  3.7  (3.5-3.9);  breadth  of  braincase,  11.2,  11.2  (11.0-11.5);  depth 
of  skull,  8.5,  9.0  (8.5-9.4);  length  of  rostrum,  8.8,  9.0  (8.7-9.8);  breadth  of 
rostnnn,  4.1,  4.2  (3.9-4.5);  length  of  incisive  foramen,  4.4,  4.5  (4.4-4.8); 
breadth  of  mesoptervgoid  fossa,  1.7,  1.7  (1.5-1.8);  length  of  palatal  bridge,  3.9, 
4.0  (3.8-4.3);  alveolar  length  of  maxillary  tooth-row,  3.8,  3.8  (3.7-3.9); 
alveolar  length  of  mandibular  tooth-row,  3.4,  3.5  (3.4-3.7). 


531 


Mammals  from  Isla  Cozumel,  Mexico  415 

Ccmipamans. — The  new  species  is  a  member  of  the  subgenus  Aporodon 
and  is  allied  to  Reithrodontotnys  mexicarms  and  R.  gracilis  of  the  R.  mexicanus 
species  group.  It  is  the  largest  member  of  the  mexicanus  group  as  defined  by 
Hooper  ( 1952 )   and  among  the  largest  species  of  the  genus  Reithwdontomys. 

Of  the  two  kinds  to  which  it  appears  most  closely  related,  the  new  species 
resembles  R.  gracilis  of  the  adjacent  mainland  of  the  Yucatan  Peninsula  to 
a  somewhat  greater  degree  than  R.  mexicanus,  known  nearest  Cozumel  Island 
from  the  highlands  of  Guatemala  and  Honduras.  In  comparison  with  gracilis, 
R.  spectabilis  is  immediately  recognized  by  its  much  larger  size  (total  length 
averaging  213.8  in  adult  spectabilis  but  only  175.7  in  six  adult  R.  g.  gracilis 
from  the  Yucatan  Peninsula,  length  of  hind  foot  21.3  and  17.8,  greatest  length 
of  skull  24.7  and  21.9,  zygomatic  breadth  12.2  and  10.8),  generally  darker 
coloration,  and  in  having  a  massive  skull  with  broader,  heavier  zygomatic 
arches.  R.  spectabilis  resembles  R.  gracilis  (in  contrast  to  R.  mexicanus)  in 
that  the  dark  tarsal  stripe  does  not  extend  onto  the  hind  foot  and  in  having 
a  flattened  and  relatively  uninflated  braincase,  incisive  foramina  that  rarely 
reach  the  level  of  Ml,  and  in  other  general  features  of  the  cranium.  The 
breadth  and  depth  of  the  braincase  are  even  less,  relative  to  length  of  the  skull, 
than  in  gracilis — the  breadth  averages  44.6  per  cent  of  the  greatest  lengdi  of 
skull  (47.5  in  gracilis  studied),  and  the  depth  of  skull  averages  35.9  in  rela- 
tion to  length  (36.9  in  gracilis). 

R.  spectabilis  resembles  R.  mexicanus  more  than  R.  gracilis  in  size  (measure- 
ments of  mexicanus  studied — subspecies  hmcelU  and  orintis — are  intermediate 
between  those  of  spectabilis  and  gracilis)  and  to  some  extent  in  general  colora- 
tion. Cranially,  aside  from  averaging  smaller,  mexicanus  can  be  distinguished 
most  easily  from  spectabilis  by  its  proportionately  broader  and  deeper  braincase. 

Because  of  its  resemblance  in  many  features  to  the  smaller  R.  gracilis,  we 
assume  that  the  precursors  of  R.  spectabilis  reached  Cozumel  from  the  adjacent 
mainland  of  the  Yucatan  Peninsula.  The  magnitude  of  the  differences  be- 
tween the  two  species  suggests,  to  us  at  least,  that  they  have  been  separated 
for  a  relatively  long  time,  since  at  least  late  Pleistocene. 

Remarks. — Some  of  the  harvest  mice  from  Cozumel  Island  were 
trapped  in  tangled,  second-growth  vines  and  brush  adjacent  to 
(beachward  from)  scrub  forest;  Oryzomys  palti.^ris  coziimelae  was 
abundant  in  this  same  habitat.  Other  individuals  were  taken  in 
forest  in  traps  set  at  the  bases  of  trees  and  along  a  stone  wall.  One 
specimen  was  caught  by  hand  at  night  as  it  climbed  in  the  branches 
of  a  small  tree,  indicating  that  the  Cozumel  harvest  mouse  is  at 
least  partly  arboreal  in  habits. 

Our  sample  contains  several  juvenal  and  subadult  specimens. 
One  female,  trapped  on  August  9,  had  been  recently  lactating,  but 
no  other  females  evidenced  gross  reproductive  activity.  The  testes 
of  two  adult  males  measured  13  and  14  mm. 

Specimens  examined,  16,  as  follows:  2^2  km.  N  San  Miguel,  3  (92294-96): 
33^  km.  N  San  Miguel,  13  (92281-93). 

Peromyscus  Icucopus  cozumelae  Merriam,  1901. — Six  white-footed  mice 
were  trapped  along  trails  in  scrub  forest  or  in  places  marginal  between  forest 


532 


416  University  of  Kansas  Publs.,  Mus.  Nat.  Hist. 

and  second-growth  bnisli.  Our  specimens  are  from  3/2  km.  N  (92417-21)  and 
2)2  km.  N  (92422)  San  Miguel.     A  female  obtained  on  August  11  was  lactating. 

P.  I.  cozumehie  differs  from  the  subspecies  of  the  mainland  of  the  Yucatan 
Peninsula  (P.  /.  castcincus)  in  being  larger,  both  externally  and  cranially,  and 
in  having  heavier  teeth.     The  two  kinds  closely  resemble  each  other  in  color. 

Dasyprocta  punctata  yucatanica  Goldman,  1913. — According  to  Merriam 
(1901:100),  D.  punctata  was  introduced  on  Cozumel  "shortly  before"  the  visit 
of  Nelson  and  Goldman  to  the  island  in  1901.  Goldman  actually  observed  an 
individual  in  the  forest  near  San  Miguel.  Natives  reported  to  us  that  agoutis 
still  occur  on  the  island. 

Agouti  paca  subsp. — On  the  morning  of  August  11,  William  E.  Duellman 
observed  a  paca  along  a  trail  through  the  forest  appro.ximately  4  km.  N  San 
Miguel.  We  queried  local  residents  concerning  the  status  o*^  this  large  rodent 
on  the  island  and,  while  aware  of  its  presence,  they  had  no  knowledge  of 
whether  or  not  it  had  been  introduced. 

Urocynn  cinereoargenteus  subsp. — We  did  not  obtain  specimens  of  the 
gray  fox,  but  local  residents  reported  its  occurrence  to  us.  Earlier,  Merriam 
(1901:99)  wrote  of  this  species  on  Cozumel  as  follows:  "The  only  mammal 
heard  of  [by  Nelson  and  Goldman]  which  was  not  secured  is  a  small  Gray  Fox 
( Urocyon )  reported  by  natives  as  rather  rare,  but  more  common  on  the  eastern 
and  southern  parts  of  the  island.  From  the  accounts  it  agrees  with  the  Rac- 
coon, Nasua,  and  Peccary  in  being  much  smaller  than  the  mainland  species." 

Procyon  pygmaeus  Merriam,  1901. — A  subadult  male  raccoon  (92565)  was 
shot  on  August  8  from  a  coconut  palm  situated  along  the  beach  3/2  km.  N  San 
Miguel.  Two  other  individuals  were  seen  in  the  same  tree  and  the  three  may 
have  been  from  the  same  family  group.  Our  specimen  diflFers  in  cranial 
features  from  raccoons  of  the  Yucatan  Peninsula  ( P.  lotor  shufeldti )  in  ways 
described  by  Goldman  (1950:76-77),  and  we  follow  Goldman  in  preserving 
specific  recognition  for  pygmaeus.  It  is  perhaps  worthy  of  note  that  our  speci- 
men has  a  distinct  "interparietal"  bone  approximately  13  mm.  long  by  8  mm. 
wide,  at  the  juncture  of  the  parietal  and  frontal  bones. 

Nasua  nelsoni  Merriam,  1901. — According  to  local  residents,  coatis  are  com- 
mon in  the  vicinity  of  San  Miguel.  Several  were  seen  at  night  and  in  early 
morning  by  our  party.  One  (92570),  an  adult  female  with  well-developed 
teats  (probably  recently  lactating),  was  obtained  3/2  km.  N  San  Miguel. 

We  retain  N.  nelsoni  as  a  full  species  because  it  differs  so  strikingly  in  size 
from  the  coati  (Nasua  narica  yucatanica)  of  the  adjacent  mainland.  Measure- 
ments of  our  specimen,  followed  in  parentheses  by  measurements  of  an  adult 
female  of  yucatanica  from  7  km.  N  and  51  km.  E  Escarcega,  Campeche,  are 
as  follows:  total  length,  741  (990);  length  of  tail,  332  (485);  length  of  hind 
foot,  76  (99);  length  of  ear,  35  (40);  greatest  length  of  skull,  103.4  (118.6); 
zygomatic  breadth,  50.3  (58.3);  interorbital  constriction,  20.4  (24.5);  palatal 
length,  62.7  (72.9);  breadth  of  braincase,  38.3  (42.0);  alveolar  length  Ml- 
M3,  16.6  (19.9).  Aside  from  its  over-all  smaller  size,  the  skull  of  nehoni  is 
notable  for  its  more  delicate  construction  and  distinctly  smaller  bullae  when 
compared  with  N.  n.  yucatanica. 

Trichechus  manatus  manatus  Linnaeus,  1758. — Local  residents  reported  that 
manatees  were  observed  occasionally  along  the  west  coast  of  the  island  and 
that  they  were  common  in  the  bays  and  lagoons  on  the  adjacent  coast  of 
Quintana  Roo. 


533 


Mammals  from  Isla  Cozumel,  Mexico  417 

Tayassu  tajacu  nanus  Merriam,  1901. — The  collared  peccary  of  Cozumel 
was  described  as  a  subspecies  distinct  from  that  on  the  adjacent  mainland  of 
Yucatan  ( T.  t.  angulatus)  on  the  basis  of  smaller  size  and  blacker  nose  and 
chin.  Subsequenth-,  Hershkovitz  (1951:567)  noted  that  the  species  had  been 
introduced  on  the  island  from  the  adjacent  mainland  (see  also  de  Vos  et  al, 
1956:176)  and  suggested  that  the  small  size  claimed  for  nanus  resulted  from 
heavy  hunting  pressure,  which  did  not  allow  animals  to  attain  adult  size.  Ad- 
ditional specimens  are  needed  before  Hershkovitz's  interesting  hypothesis  can 
be  tested.  Natives  on  Cozumel  reported  the  collared  peccary  as  common  and 
intensively  hunted. 

Mammals  Reportedly  Collected  on  Cozumel  by  G.  F.  Gaumer 

George  F.  Gaumer,  well-known  naturalist  who  lived  for  many  years  on  the 
Yucatan  Peninsula,  reported  himself,  or  sent  to  others,  a  number  of  mammals 
alleged  to  have  come  from  the  island  of  Cozumel.  Some  of  these  probabK 
originated  from  the  island  but  others  seemingly  did  not,  as  discussed  below. 

Oldfield  Thomas  (1888),  in  the  first  technical  paper  dealing  with  mam- 
mals from  Cozumel,  reported  five  species  that  were  collected  by  Gaumer  and 
communicated  to  Thomas  by  Salvin  and  Godman.  These  five  were  Didelphis 
marsupialis,  Pteronotus  parnellii,  Artiheus  jamaicensis,  Tadarida  laticaudaia, 
and  "Nasua  nasica."  The  opossum,  Jamaican  fruit-eating  bat,  and  coati  (in 
the  fonn  of  the  small  Nasua  nelsoni)  subsequently  have  been  found  to  be 
common  on  the  island.  No  other  records  of  the  two  remaining  bats,  Pteronotus 
and  Tadarida,  have  been  forthcoming,  but  each  is  widespread  on  the  adjacent 
Yucatan  Peninsula  and  we  do  not  doubt  that  each  occurs  on  Cozumel. 

In  his  "Monografia  de  los  mamiferos  de  Yucatan,"  Gamner  (1917:117)  re- 
ported the  presence  of  the  Yucatan  deer  mouse,  Peromyscus  yucatanicus,  on 
the  island.  He  did  not,  however,  record  Peromyscus  leucopus  from  Cozumel 
and  Koopman  (1959:237)  concluded  that  Gaumer  confused  the  two  species. 
We  are  inclined  to  agree  with  Koopman,  because  insofar  as  we  know  P. 
yucatanicus  does  not  occur  on  the  island.  Gaumer  (op.  cit. :6S)  also  recorded 
the  white-lipped  peccary  (as  "Dicotyles  labiatus")  from  Cozumel  but  this, 
too,  seems  to  be  in  error. 

By  far  the  most  perplexing  collection  of  mammals  relating  to  Cozumel  is  a 
lot  of  specimens  acquired  from  Gaumer  by  the  Museum  of  Natural  History  in 
the  early  1900's.  Many  of  these  specimens  were  cited  by  Hall  and  Kelson 
(1959)  and  all  species  represented  were  listed  by  Koopman  (1959).  The 
holotype  and  paratypes  of  Mimon  cozumehe  Goldman  (1914)  were  among 
the  specimens  in  this  collection.  Aside  from  M.  cozumelae,  species  represented 
(and  their  catalogue  numbers)  are:  Micronycteris  megalotis  mexicana  (1659- 
60);  Glossophaga  soricina  leachii  (1655-58);  Artiheus  jamaicensis  yucatanicus 
(1641-42);  Centurio  senex  (1669-70);  Lasiurus  horealis  teliotis  (1655);  Pleco- 
tus  (possibly  mexicanus)  (1658);  Molossus  ater  nigricans  (1663-64);  Ateles 
geoffroyi  yucatai^ensis  ( 885 ) ;  Tamandua  tetradactyla  mexicana  ( 869-872,  880 ) ; 
Heterogeomys  hispidus  yucatanensis  (1370);  Nasua  narica  yucatanica  (876-77, 
1599-1600);  Galictis  allamandi  canaster  (873);  and  Tayassu  sp.  (875 — said 
to  be  T.  t.  nanus,  probably  solely  on  supposed  geographic  grounds,  but  speci- 
men not  now  to  be  found ) . 

Most  of  the  labels  that  now  accompany  the  above-listed  specimens  are  not 
the  original  labels  of  Gaumer,  and,  in  any  event,  bear  no  additional  informa- 
tion that  could  support  or  refute  the  contention  that  the  specimens  actualK 


534 


418  University  of  Kansas  Publs.,  Mus.  Nat.  Hist. 

came  from  Cozumcl.  Many  other  specimens  received  at  the  same  time  arc 
labeled  simply  as  from  "Yucatan."  Some  of  the  specimens  said  to  be  from 
Cozumel  obviously  did  not  come  from  there  as  shown  below  and  there  is  a 
strong  possibility  that  others  did  not.  Perhaps  few  or  none  of  the  specimens 
actually  originated  on  the  island. 

Of  the  eight  bats,  only  two  (A.  iamaicensis  and  M.  megalotis)  have  been 
obtained  on  Cozumel  by  other  collectors.  One,  Plecotus,  seems  likely  not  to 
occur  there  (see  also  Koopman,  1959:237).  The  remaining  five  (Mimon, 
Glossophaga,  Ccnturio,  Lasiurus,  and  Molossus)  are  widespread  in  Middle 
America  and  each  is  known  from  the  adjacent  mainland.  We  took  G.  soricinn 
on  the  much  smaller  Isla  Mujeres  that  lies  to  the  north  of  Cozumel.  There  is 
a  strong  possibility  that  all  five  species  actually  occur  on  Cozumel  and  that 
additional  collecting  will  establish  their  presence  on  the  island.  We  are 
especially  hopeful  of  this  development  with  reference  to  Mimon  cozumelae. 

With  reference  to  the  six  strictly  terrestrial  kinds,  we  doubt  that  any  save 
Tayassii  occurs  on  the  island.  The  major  habitat,  sciub  forest,  doubtfully  would 
support  tamanduas  or  monkeys  (although  the  latter  might  have  been  intro- 
duced) and  neither  was  reported  to  us  by  local  residents  (nor  was  the  grison 
mentioned).  We  especially  questioned  natives  about  the  occurrence  of  pocket 
gophers  but  they  assured  us  that  "tuzas"  were  not  present.  All  four  coatis, 
formerly  labeled  "Nasiia  r^elsoni"  are  unquestionably  the  much  larger  N.  narica 
yucatonica  that  occurs  only  on  the  adjacent  mainland. 

Zoogeog,raphy 

As  Koopman  (1959)  pointed  out,  the  zoogeographic  relationships 
of  Cozumel,  at  least  with  respect  to  mammals,  are  undoubtedly  with 
the  adjacent  mainland,  not  with  the  Antilles.  Even  though  the 
strait  that  separates  Cozumel  from  the  mainland  of  Quintana  Roo  is 
deep,  and  the  current  in  it  strong,  we  suppose  that  most  of  the 
mammals  that  occur  on  the  island  reached  it  by  "rafting"  across  the 
strait  or  possibly  from  the  mainland  to  the  south  of  Cozumel.  At 
a  time  of  ma.ximal  glaciation,  because  of  a  lowering  of  the  sea  level, 
the  strait  would  have  been  reduced  to  appro.ximately  half  its  present 
width,  theoretically  making  "rafting"  much  easier  than  now,  es- 
pecially if  favorable  winds  prevailed.  At  least  three  of  the  mammals 
that  currently  inhabit  the  island  are  known  or  suspected  to  have 
been  introduced  by  man. 


535 


Mammals  from  Isla  Cozumel,  Mexico  419 

LITERATURE  CITED 

Andersen,  K. 

1906.  Brief  diagnoses  of  a  new  genus  and  ten  new  forms  of  stenodermatous 
bats.    Ann.  Mag.  Nat.  Hist.,  18:419-423,  December. 

Dalquest,  W.  W. 

1953.  Mexican  bats  of  the  genus  Artibeus.  Proc.  Biol.  Soc.  Washington, 
66:61-66,  August  10. 

Davis,  W.  B. 

1958.  Review  of  Mexican  bats  of  the  Artibeus  "cinereus"  complex.  Proc. 
Biol.  Soc.  Washington,  71:163-166,  1  fig.,  December  31. 

de  Vos,  a.,  Manville,  R.  H.,  and  Van  Gelder,  R.  G. 

1956.  Introduced  mammals  and  their  influence  on  native  biota.  Zoologica, 
41:163-194,  1  fig.,  December  31. 

Gaumeb,  G.  F. 

1917.  Monografia  de  los  mamiferos  de  Yucatan.  Dept.  de  Talleres 
Graficos  de  la  Secretaria  de  Fomento,  Mexico,  xii  -f  331  pp.,  57 
pis.,  2  photographs,  1  map. 

Goldman,  E.  A. 

1914.  A  new  bat  of  the  genus  Mimon  from  Mexico.  Proc.  Biol.  Soc. 
Washington,  27:75-76,  May  11. 

1918.  The  rice  rats  of  North  America  (genus  Oryzomys).  N.  Amer. 
Fauna,  43:1-100,  6  pis.,  11  figs.,  September  23. 

1950.  Raccoons  of  North  and  Middle  America.  N.  Amer.  Fauna,  60: 
vi  -f-  1-153,  22  pis.,  2  figs.,  November  7. 

1951.  Biological  investigations  in  Mexico.  Smiths.  Misc.  Coll.,  115: 
xiii  +  1-476,  frontispiece,  71  pis.,  1  map,  July  31. 

Hall,  E.  R.,  and  Kelson,  K.  R. 

1959.  The  mammals  of  North  America.  2  vols,  (xxx-f  1-546 -j- 79  and 
viii  +  547-1083  -f  79),  illustrated,  March  31. 

Hershkovitz,  p. 

1949.  Mammals  of  northern  Columbia.  Preliminary  report  no.  5:  bats 
(Chiroptera).     Proc.  U.  S.  Nat.  Mus.,  99:429-454,  May  10. 

1951.  Mammals  from  British  Honduras,  Mexico,  Jamaica  and  Haiti. 
Fieldiana-Zool.,  Chicago  Mus.  Nat.  Hist.,  31:547-569,  July  10. 

Hooper,  E.  T. 

1952.  A  systematic  review  of  the  harvest  mice  (genus  Reithrodontomys) 
of  Latin  America.  Misc.  Publ.  Mus.  ZooL,  Univ.  Michigan,  77: 
1-255,  24  figs.,  12  maps,  January  16. 

Koopman,  K.  F. 

1959.  The  zoogeographical  hmits  of  the  West  Indies.  Jour.  Mamm.  40: 
236-240,  May  21. 

Merriam,  C.  H. 

1901.  Six  new  mammals  from  Cozumel  Island,  Yucatan.  Proc.  Biol.  Soc. 
Washington,  14:99-104,  July  19, 

Paynter,  R.  a.,  Jr. 

1955.  The  omithogeography  of  the  Yucatan  Peninsula.  Bull.  Peabody 
Mus.  Nat.  Hist.,  9:1-347,  4  pis.,  2  maps. 

Thomas,  O. 

1888.    List  of  mammals  obtained  by  Mr.  G.  F.  Gaumer  on  Cozimiel  and 
Ruatan  Islands,  Gulf  of  Honduras.     Proc.  Zool.  Soc.  London    d 
129,  June.  ^ 

Transmitted  July  7,  1964. 


536 


RELATION  OF  SIZE  OF  POCKET  GOPHERS  TO  SOIL 

AND  ALTITUDE 

By  William  B.  Davis 

While  working  out  the  distribution  and  taxonomy  of  pocket  gophers  in 
southern  Idaho,  I  became  interested  in  the  problem  of  correlation  of  size  with 
soil  conditions  and  altitude,  I  do  not  claim  to  have  settled  a  problem; 
in  fact,  I  intend  merely  to  point  out  one  that,  to  me,  warrants  further 
study. 

The  specimens  and  field  notes  on  which  this  discussion  is  based  are  con- 
tained in  the  Museum  of  Vertebrate  Zoology,  Berkeley,  California.  I  wish 
to  thank  the  officials  of  that  museum  for  the  many  privileges  extended  me; 
also,  to  acknowledge  the  generous  assistance  of  Messrs.  David  Johnson  and 
D.  Tillotson  in  supplying  additional  specimens  and  information. 

Pocket  gophers,  especially  the  males,  tend  to  increase  in  size  with  age. 
The  ultimate  size  attained  appears  to  be  correlated  directly  with  the  type 
of  soil  inhabited,  and  indirectly  with  altitude.  At  high  elevations  where 
the  soil  usually  is  shallow  and  rocky,  or  at  lower  elevations  where  the  same 
general  environmental  conditions  prevail,  races  and  individuals  of  the  same 
species  tend  to  be  small.  In  places  of  this  kind  the  skulls  of  males  and  fe- 
males often  are  indistinguishable;  they  are  smooth  and  lack  ridges.  They 
are  juvenile  in  character  and  in  many  respects  appear  not  to  have  developed 
beyond  the  subadult  state  of  forms  living  under  better  enviroimiental  con- 
ditions. If  one  compare  individuals  from  poorer  soils  (for  pocket  gophers) 
with  others  from  progressively  better  and  deeper  ones,  the  size  of  both  sexes 
is  found  generally  to  increase,  males  more  so  than  females.  Under  optimum 
conditions  the  actual  weight  of  the  skulls  may  average  two  or  even  three 
times  that  of  individuals  that  live  amid  adverse  conditions.  In  the  deeper 
soils  sexual  dimorphism  is  evident  and  the  skulls  of  both  sexes  are  angular 
in  outline  and  have  well  developed  sagittal,  lambdoidal,  and  temporal 
ridges. 

This  general  reduction  in  size  at  higher  altitude  is  illustrated  by  specimens 
from  near  Pocatello,  Idaho.  There  the  species  Thomomys  quadratus  occurs 
altitudinally  from  4400  feet  on  the  floor  of  Portneuf  Valley  to  over  7000 
feet  in  the  Bannock  Mountains.  Individuals  taken  from  the  valley  are 
considerably  larger  than  those  from  higher  altitudes.  The  skulls  are  massive, 
prognathous,  angular,  and  ridged,  the  males  much  larger  than  the  females. 
Individuals  taken  at  progressively  higher  altitudes  are  smaller,  the  skulls 
tend  to  be  less  angular  and  ridged,  as  well  as  less  prognathous,  and  the  degree 
of  sexual  dimorphism  is  reduced.  Taking  the  product  of  three  dimensions 
of  the  skull,  basilar  length,  zygomatic  breadth,  and  palatofrontal  depth,  as 
an  index  of  size,  the  following  results  were  obtained : 


537 


DAVIS — POCKET  GOPHERS  339 

Males  Females  Difference 

4500  feet 1295  (3)*  1035  (3)  260 

5000  feet 1360  (4)  930  (3)  430 

5800  feet 1060  (2)  880  (2)  180 

6300  feet 920  (6)  840  (6)  80 

7000  feet 920  (2)  850  (1)  70 


* 


Number  of  specimens  averaged. 


Certain  discrepancies  are  evident  in  the  comparisons.  Males  from  5000 
feet  are  larger  than  those  from  4500  feet;  the  female  from  7000  feet  is  larger 
than  those  from  6300  feet.  These  exceptions  do  not  invalidate  the  general 
principle  because  age  differences  in  the  males  and  too  few  specimens  in  the 
females  probably  account  for  the  deviations  from  the  expected  size.  A 
reduction  in  length  of  body,  length  of  hind  foot,  and  length  of  tail  accom- 
panies a  reduction  in  "volume"  of  the  skull. 

Similar  results  were  obtained  in  a  study  of  another  species  in  another 
locality.  Thomomys  bottae  occurs  on  the  floor  of  Monitor  Valley,  Nevada, 
at  an  altitude  of  6900  feet,  and  also  on  the  adjacent  Toquima  Mountains, 
which  rise  to  over  10,000  feet.  Individuals  taken  at  altitudes  ranging  from 
9000  to  10,000  feet  on  the  mountain  are  considerably  smaller  than  those 
from  the  valley;  specimens  from  Meadow  Creek  Canyon,  at  8000  feet  on 
the  east  side  of  the  mountain,  are  intermediate  in  size.  Sexual  dimorphism 
is  pronounced  in  specimens  from  the  valley;  it  is  slight  in  specimens  from 
above  9000  feet.     These  facts  are  evident  from  the  following  tabulation. 

Males  Females  Difference 

6900  feet 1775  (6)  1250  (6)  525 

8000  feet 1320  (2)  1060  (2)  260 

9000  to  10000  feet 1060  (5)  920  (2)  140 

Similarly,  specimens  of  Thomomys  bottae  taken  at  different  elevations 
on  Mt.  Moriah  in  eastern  Nevada  and  western  Utah  exhibit  the  same  trend. 
Skulls  of  specimens  from  5000  feet  elevation  are  much  larger  than  those  from 
high  on  the  mountain.  Between  the  two  extremes  the  skulls  are  intermedi- 
ate, grading,  as  evidenced  below,  from  large,  with  pronounced  sexual  di- 
morphism, at  the  bottom,  to  small  at  the  top,  with  little  difference  between 
males  and  females. 

Males 

5000  feet 1664  (3) 

5400  feet 1268  (2) 

6000  feet 1177  (2) 

6700  feet — 

9100  feet 1139  (3) 

9800  feet 1086  (1) 

11400  feet — 


Females 

Difference 

1221  (5) 

443 

1085  (3) 

183 

1001  (2) 

— 

994  (6) 

45 

1009  (1) 

77 

971  (2) 

— 

538 


340  JOURNAL   OF   MAMMALOGY 

Again,  certain  discrepancies  appear,  but  the  gradation  is  clearly  evident. 

Aside  from  consistently  smaller  size,  specimens  of  both  quadratus  and 
hoitae  from  the  higher  altitudes  are  but  little  different  from  those  at  low 
levels.  The  most  significant  difference  is  found  in  the  relatively  shorter 
rostrum  in  specimens  from  high  altitudes.  This  I  interpret  as  an  expression 
of  arrested  development.  Numerous  studies  have  shown  that  the  rostrum 
in  subadult  pocket  gophers  is  consistently  relatively,  as  well  as  actually, 
shorter  than  in  adults. 

Gradation  from  large  to  small  size  is  found  in  every  area  studied  in  the 
Great  Basin  where  one  species  occupies  both  the  valley  floor  and  the  adjacent 
mountain.  Because  of  this,  it  becomes  increasingly  difficult  to  reconcile 
present  practices  in  taxonomy  with  the  situation  as  it  actually  exists.  The 
tendency  of  certain  students  to  assign  all  the  populations  of  pocket  gophers 
occurring  on  different,  isolated  mountain  tops  to  one  subspecies  and  those 
occurring  in  the  lowlands  to  another  defeats  the  purpose  of  systematics. 
To  me,  it  is  illogical  to  assume  that  the  several  alpine  populations  are  closely 
related  inter  se  and  genetically  different,  as  a  unit,  from  the  populations  of 
the  same  species  occurring  in  the  valleys.  Nor  does  it  seem  logical  to  assume 
that  the  populations  of  a  species  in  two  valleys,  separated  by  a  high  mountain 
range  on  which  small  individuals  of  the  same  species  occur,  are  genetically 
related  inter  se  and  at  the  same  time  genetically  distinct  from  the  smaller 
alpine  individuals. 

Various  authors  have  referred  the  alpine  populations  of  pocket  gophers 
in  southern  Idaho  to  Thomomys  uinta  or  Thomomys  quadratus  uinta  and 
those  in  the  lowlands  to  Thomomys  bridgeri  or  Thomomys  quadratus  bridgeri. 
In  doing  this  the  topography  and  geologic  history  of  the  area  probably  were 
not  considered.  In  this  region  the  mountains  certainly  are  older  than  the 
genus  Thomomys  and  consequently  we  cannot  assume  that  populations  now 
restricted  to  alpine  areas  once  occupied  a  continuous  range  that  subsequently 
was  disrupted  by  geologic  changes.  Nor  can  we  assume  that  the  population 
of  large  pocket  gophers  moved  in  and  usurped  the  lowland  portions  of  a  range 
once  occupied  by  the  smaller  animals.  Such  an  assumption  would  neces- 
sitate a  divergence  of  the  two  at  a  time  earlier  than  that  suggested  by  cranial 
characters.  Furthermore,  it  would  necessitate  a  migration  of  the  large  in- 
dividuals over  high  passes  in  order  to  explain  their  present  distribution  in 
southern  Idaho. 

In  interpreting  the  past  history  of  Thomomys  quadratus  in  southeastern 
Idaho  I  have  assumed  that  during  the  Pleistocene  most  of  the  mountains 
were  glaciated  and  the  lower  valleys  under  water,  so  that  intermediate  alti- 
tudes alone  were  available  to  pocket  gophers.  It  is  well  known  that  the 
yearly  increase  of  a  successful  species  is  greater  than  the  carrying  capacity 
of  the  area  occupied,  and  that  as  a  result  of  population  pressure  every  avail- 
able niche  is  sought  out  and  occupied.  As  the  glaciers  receded  and  the  lakes 
decreased  in  extent,  additional  territory  became  available  both  above  and 


539 


DAVIS — POCKET  GOPHERS  341 

below  the  former  range.  This  new  territory  was  occupied  by  the  surplus 
of  the  yearly  increase.  Those  gophers  that  moved  down  hill  encountered 
deeper  and  richer  soils  and  consequently  could  grow  larger  without  handicap. 
Those  that  moved  uphill  found  conditions  progressively  more  adverse;  the 
soil  was  shallower  and  rockier  and  plant  food  less  abundant,  although  suffi- 
cient to  maintain  life.  Only  individuals  with  small  bodies  could  survive 
amid  such  conditions.  Whether  size  per  se  be  heritable  or  due  to  ontogenetic 
processes  is  not  of  prime  importance  to  the  question  at  issue  because  the  end 
result — size — in  either  instance  is  the  limiting  factor  in  shallow  soil.  Ul- 
timately, from  a  population  of  pocket  gophers  of  medium  size,  both  the 
mountains  and  the  lowlands  became  populated,  the  former  by  small  indi- 
viduals, the  latter  by  large  ones.  The  parent  stock  probably  remained  at 
intermediate  levels. 

Such  an  interpretation  explains  many  facts  of  distribution.  Each  high 
mountain  in  southern  Idaho  harbors  a  population  of  dwarfed  individuals, 
in  each  valley  the  gophers  are  large,  and  at  middle  altitudes,  of  intermediate 
size.  The  alpine  populations,  even  on  isolated  mountain  tops,  resemble  one 
another  more  than  they  do  those  in  the  valleys,  yet  it  is  difficult  to  conceive 
of  them  as  being  subspecifically  related  inter  se  and  at  the  same  time  sub- 
specifically  distinct  from  those  at  lower  elevations.  The  similar  cranial 
characters  of  the  two  extremes,  the  gradation  from  large  size  to  small,  and 
the  topography  and  geologic  history  of  the  region,  point  toward  the  conclu- 
sion that  the  alpine  and  lowland  forms  are  of  the  same  subspecies.  This 
applies  also  to  the  two  localities  in  Nevada  whence  specimens  were  examined. 

The  only  other  logical  method  I  see  of  treating  these  alpine  populations 
is  to  name  each  one  of  them,  a  practice  that  would  lead  to  confusion  and  ridi- 
cule, yet  one  that  is  followed  by  some  students. 

We  should  be  more  cautious  in  our  designation  of  new  races.  All  too 
little  attention  has  been  given  to  the  study  of  the  effect  of  environment  upon 
the  size  of  animals.  If  environmental  conditions  produce  a  condition  of 
arrested  development,  should  animals  exhibiting  this  condition  be  recognized 
by  name?  Whether  pocket  gophers  from  alpine  areas  would  increase  in 
size  if  transplanted  to  better  soil  at  lower  elevations,  or  whether  they  would 
retain  their  identity,  is  not  known.  An  experiment  designed  to  test  this 
point  would  be  well  worth  while. 

SUMMARY 

1.  In  each  of  three  localities  in  southern  Idaho  and  the  Great  Basin  where 
the  same  species  of  pocket  gopher  inhabits  both  the  lowlands  and  the  adjacent 
mountain,  a  gradation  from  large,  sexually  dimorphic  individuals,  at  lower 
elevations  where  the  soil  is  deeper,  to  small  individuals  with  little,  if  any, 
sexual  dimorphism,  at  higher  elevations  where  the  soil  is  shallower,  is 
exhibited. 

2.  Since  the  same  trend  occurs  at  each  of  three  widely  separated  locaUties, 


540 


342  JOURNAL   OF   MAMMALOGY 

it  seems  logical  to  conclude  that  the  gradient  is  a  true  one ;  also  that  the  popu- 
lations at  the  two  extremes  of  such  a  gradient  are  not  worthy  of  recognition 
by  separate  names. 

3.  The  possibiUty  of  this  gradient  occurring  in  other  locaUties  should  merit 
careful  consideration  in  systematic  work  with  Thomomys  so  that  the  formal 
naming  of  populations  not  worthy  of  recognition  by  name  will  be  avoided. 

Department  of  Wild  Game,  Agricultural  and  Mechanical  College  of  Texas, 
College  Station,  Texas. 


541 


THE  PINNIPEDIA:   AN  ESSAY  IN  ZOOGEOGRAPHY* 

J.  L.  DAVIES 

STUDIES  that  seek  to  explain  the  present  distribution  of  animal  forms 
must  draw  on  a  wide  and  varied  field  of  evidence.  Some  of  the  evidence, 
notably  that  provided  by  the  paleontologists,  is  direct  and  generally 
capable  of  reliable  interpretation;  but  rarely,  except  for  some  groups  of  land 
mammals,  is  the  fossil  evidence  sufficient.  More  commonly,  paleontology 
can  provide  only  the  framework,  perhaps  one  or  two  major  clues,  or  even 
just  a  tiny  piece  of  the  whole  picture.  The  most  successful  ventures  into  the 
field  of  historical  zoogeography  have  been  made  by  paleomammalogists  who 
have  studied  particularly  the  groups  living  in  relatively  large  numbers  in 
habitats  where  sedimentation  is  most  rapid.  Thus  the  historical  geography  of 
such  plains-dwelling  groups  as  the  horses  and  the  elephants  is  comparatively 
well  known,  but  forms  that  inhabit  mountains,  forests,  or  seas  are  represented 
only  fragmentarily  in  the  fossil  record.  For  these  latter  groups  other  evidence 
must  be  invoked,  and  it  is  provided  by  the  taxonomy,  physiology,  ecology, 
and  distribution  of  the  existing  forms.  This  evidence,  although  easier  to 
accumulate,  is  not  capable  of  such  reliable  interpretation  as  that  provided  by 
paleontology,  but  it  must  always  be  explained  and  often  provides  the  only 
clues  available. 

A  third,  more  nebulous,  category  of  evidence  derives  from  our  knowledge 
of  past  climates  and  past  distributions  of  land  and  sea.  At  present,  however, 
this  knowledge  is  so  uncertain  that  it  is  clearly  dangerous  to  place  too  much 
reliance  on  it;  at  the  same  time,  it  should  not  be  disregarded,  since  it  can  often 
indicate  possibilities  and  probabilities  and  provide  a  set  of  limits  within  which 
the  correct  solution  to  any  given  problem  may  be  found. 

Finally,  it  is  necessary  to  keep  in  mind  present  trends  of  thought  in  the 
fields  of  genetics  and  evolution,  because,  although  there  is  anything  but 
unanimity  of  opinion  within  these  fields,  the  most  generally  accepted  concepts 
will  have  an  important  bearing  on  possible  zoogeographical  conclusions. 

Individual  bits  of  evidence  culled  from  all  four  sources — paleontological, 
neozoological,    paleogeographical,    and    evolutionary — may    often    appear 

*The  writer  is  indebted  to  Professor  Peter  Scott,  head  of  the  Department  of  Geography  at  the  Uni- 
versity of  Tasmania,  for  reading  and  commenting  on  the  manuscript. 

>  Mr.  Davies  is  Senior  Lecturer  in  the  Department  of  Geography,  University  of 
Tasmania,  Hobart. 


542 


THE  PINNIPEDIA  475 

tenuous  and  circumstantial  by  themselves,  but  if  they  are  placed  together  to 
make  a  unified  picture,  each  one  supporting  others,  the  probability  of  their 
correctness,  and  the  correctness  of  the  whole  picture,  is  much  increased. 

The  present  essay  examines  an  order  of  marine  carnivorous  mammals,  the 
Pinnipedia,  which  is  divided  by  taxonomists  into  three  families:  the  seals 
(Phocidae),  the  sea  lions  (Otariidae),  and  the  walruses  (Odobenidac).'  The 
order  is  comparatively  poorly  represented  in  the  fossil  record,  and  paleon- 
tologists have  hesitated  to  discuss  its  distributional  history.  Published  dis- 
cussions of  pinniped  geography  have  been  by  neozoologists,  who  based  their 
findings  on  the  taxonomy  and  distribution  of  existing  forms,  and  such  a 
hmitation  of  the  field  of  evidence  has  led  to  some  conclusions  that  are  doubt- 
ful and  even  demonstrably  wrong.  For  instance.  Von  Boetticher"  followed 
Sclater^  in  postulating  a  southern  origin  for  the  sea  lions  and  a  spread  from 
south  to  north,  though  the  fossil  evidence  alone  makes  this  highly  unlikely. 

The  present  study  attempts  to  use  evidence  from  as  many  fields  as  possible, 
and,  although  it  lacks  the  firm  basis  of  paleontological  data  that  would  be 
desirable,  it  does  seem  to  provide  the  only  theory  of  pinniped  origin  and 
spread  that  is  fully  tenable  in  the  light  of  the  facts  as  they  are  known  at  present. 

The  evidence  of  existing  distribution  is  summarized  on  a  series  of  maps 
that,  together  with  a  series  published  previously,'^  represent  an  attempt  to  map 
the  distribution  o£  all  pinniped  forms. ^  The  fossil  evidence  was  gathered 
together  in  1 922  by  Kellogg,^  but  his  work  is  now  out  of  date  in  some  respects 
and  must  be  supplemented  from  a  rather  scattered  literature. 

'  The  fossil  Semantor  was  placed  in  a  fourth  family  by  G.  G.  Simpson:  The  Principles  of  Classification 
and  a  Classification  of  Mammals,  Bull.  Amer.  Museum  of  \at.  Hist.,  Vol.  85,  1945,  pp.  1-350,  but  this 
animal  was  almost  certainly  a  mustelid  (see  E.  Thenius:  Uber  die  systematische  und  phylogenetische 
Stellung  der  Genera  I'roineles  und  Semantor,  Sitziingsber.  Oster.  Akad.  der  IViss.  in  IVien,  Vol.  158,  1949, 
PP-  323-336). 

^  H.  von  Boetticher:  Die  geographische  Vcrbreitung  der  Robben,  Zeitschr.  fur  SHugetierkunde , 
Vol.  9.  1934.  pp.  359-368. 

■'P.  L.  Sclater:  On  the  Distribution  of  Marine  Mammals,  Proc.  Zool.  Soc.  of  London,  1897,  pp. 
349-359- 

•*J.  L.  Davies:  Pleistocene  Geography  and  the  Distribution  of  Northern  Pinnipeds,  Ecology,  Vol. 
39.  '•95«,  PP-  97-113- 

■'  The  scientific  nomenclature  used  here  corresponds  with  that  of  Simpson  {op.  cit.  [see  footnote  1 
above])  except  that  Sivertsen  (Erling  Sivertsen:  A  Survey  of  the  Eared  Seals  (Family  Otariidae)  with 
Remarks  on  the  Antarctic  Seals  CoUerted  by  M/K  "Norvegia"  in  1928-1929,  Scientific  Results  of  the 
S'orwegian  .Antarctic  Expeditions  \0.36,  Det  Norske  Videnskaps-Akademi  i  Oslo,  1954)  has  been  followed 
in  separating  the  Australian  sea  lion  as  Xeophoca  and  including  in  that  genus  Hooker's  sea  lion,  formerly 
known  as  Phocarctos,  which  Simpson  makes  a  synonym  o(  Otaria 

''  Remington  Kellogg:  Pinnipeds  from  Miocene  and  Pleistocene  Deposits  of  California,  Univ.  of 
California  Pubis.,  Bull.  Dept.  ofCeol.  Sciences,  Vol.  13.  No.  4,  1922. 


543 


476 


THE   GEOGRAPHICAL   REVIEW 

A  Working  Hypothesis 


The  general  argument  that  will  be  advanced  depends  largely  on  one  work- 
ing hypothesis:  The  pinnipeds  are,  and  always  have  been,  generally  tied  to  a 
cold-water  environment. 

There  can  be  little  disagreement  with  the  statement  that  present-day 
pinnipeds  are  cold-water  animals  and,  with  a  few  exceptions,  are  found  where 
sea  temperature  does  not  exceed  20°  C.  at  any  time  of  the  year  (Fig.  1).  The 


over  27.5°  C. 


Fig.  1 — Pinnipeds  and  sea  temperatures.  Distribution  of  pinnipeds  is  shown  in  black;  shaded  areas 
indicate  warm-month  mean  sea-surface  isotherms.  The  exceptional  genus  Moiiachiis  has  been  omitted 
from  this  map  for  the  salce  of  clarity,  but  see  Figure  8. 

greatest  concentrations  both  of  species  and  of  numbers  are  found  in  the  sub- 
arctic North  Atlantic  and  North  Pacific  and  around  the  fringe  of  Antarctica. 
The  one  major  oceanic  region  from  which  they  are  entirely  absent  is  the 
Indo-Malayan-West  Pacific,  which  is  also  the  only  warm-water  region  with 
a  continuous  history  as  such  since  the  beginning  of  the  Tertiary.  In  addition, 
all  fossil  forms  have  been  recovered  from  regions  where  sea  temperatures 
when  the  deposits  were  formed  lay  within  prevailing  existing  tolerances.  The 
distribution  of  pinnipeds  is,  and  possibly  always  has  been,  generally  com- 
plementary to  that  of  the  reef-forming  corals,  and  there  is  no  evidence  that 
they  have  ever  inhabited  tropical  waters. 

That  pinnipeds  are  physiologically  adapted  to  life  in  a  cold-water  environ- 
ment needs  little  elaboration.  In  particular,  they  have  progressed  far  in  the 
development  of  insulating  hair  and  blubber  and  of  highly  efficient  circulatory 
systems.  The  upper  limit  of  exterior  temperature  at  which  internal  tempera- 


544 


THE   PINNIPEDIA  477 

ture  regulation  becomes  difficult  is  presumably  not  high,  and  most,  if  not  all, 
species  experience  obvious  difficulty  in  regulating  body  temperatures  while 
on  land.^ 

Physiological  adaptation  provides  evidence  that  pinnipeds  have  long  fre- 
quented cold  waters,  but  it  does  not  provide  a  reason.  The  reasons  are  proba- 
bly many  and  include  the  abundance  of  available  food  in  the  colder  high- 
latitude  waters  and  the  virtual  absence  of  competitors.  The  large  carnivorous 
reptiles  and  fishes  have  been  and  are  warm- water  forms:  it  has  remained  for 
the  homoiothermal  seals  and  whales  to  exploit  the  cold-water  environment. 

Origin  of  the  Pinnipedia 

Pinniped  ancestry  has  long  been  debated.  Separate  creodont  origin,  as 
suggested  by  Wortman,^  now  seems  most  unlikely,  and  the  general  consensus 
would  probably  be  that  the  pinnipeds  are  derived  from  the  ancestral  dog-bear 
stock.^  Recent  serological  work^°  has  indicated  a  close  relationship  with  the 
bears,  a  relationship  forecast  on  morphological  grounds  by  Weber"  among 
others.  The  present  study  is  concerned  only  with  the  time  and  place  of 
pinniped  origin,  and  in  order  to  arrive  at  reasonable  estimates  it  is  not  neces- 
sary to  discuss  these  arguments  at  length. 

The  latest  possible  time  of  origin  is  determined  by  the  earliest  fossil 
pinnipeds,  which  are  sea  Hons  from  the  lower  Miocene  of  California,  and,  as 
these  are  fairly  advanced  and  diversified  forms,  the  latest  probable  date  must 
surely  be  sometime  about  the  middle  Oligocene.  The  earliest  possible  time 
of  origin  is  determined  by  the  earliest  occurrence  of  the  ancestral  group.  If 
the  early  dog-bear  stock  is  accepted  as  ancestral,  then  this  date  is  upper 
Eocene;  if  it  is  necessary  to  look  to  the  miacid  creodonts  as  ancestors,  the  date 
is  pushed  back  into  the  lower  Eocene,  and  even  possibly  into  the  upper 
Paleocene.  Derivation  from  the  "inadaptive"  creodonts  would  push  it  still 
farther  back  in  the  Paleocene,  but  this  likelihood  does  not  seem  to  be  en- 
visaged today  and  need  not  be  considered  here.  The  possible  extremes  are 
thus  upper  Paleocene  to  lower  Miocene,  and  the  probable  extremes  middle 

^  See,  for  instance,  G.  A.  Bartholomew  and  F.  Wilke:  Body  Temperature  in  the  Northern  Fur  Seal, 
Callorhitms  ursinus,  Journ.  of  Mammalogy ,  Vol.  37,  1956,  pp.  327-337. 

*J.  L.  Wortman:  Osteology  o(  Patriofelis ,  a  Middle  Eocene  Creodont,  Bull.  Amer.  Museum  of  Nat. 
Hist.,  Vol.  6,  1894,  pp.  129-164. 

9  See,  for  instance,  W.  D.  Matthew:  The  Carnivora  and  Insectivora  of  the  Bridger  Basin,  Middle 
Eocene,  Memoirs  Amer.  Museum  of  Nat.  Hist.,  Vol.  9,  1909,  pp.  289-567,  references  on  pp.  413-417;  A.  S. 
Romer:  Vertebrate  Paleontology  (Chicago,  1933);  and  Simpson,  op.  cit.  [see  footnote  1  above]. 

'°  C.  A.  Leone  and  A.  L.  Wiens:  Comparative  Serology  of  Carnivores,  JoMr«.  of  Mammalogy,  Vol. 
37,  1956,  pp.  11-23. 

"  M.  C.  W.  Weber:  Die  S^ugetiere  (Jena,  1909). 


545 


478  THE   GEOGRAPHICAL   REVIEW 

Eocene  to  middle  Oligocene.  A  late  Eocene  or  early  Oligocene  date  is  sug- 
gested by  Simpson/^  and  because  of  the  highly  specialized  nature  of  the 
lower  Miocene  pinnipeds,  Kellogg'-'  concluded  that  the  pinniped  stock 
originated  no  later  than  the  Eocene.  Most  considerations  point,  therefore, 
to  the  upper  Eocene  as  the  likely  time  of  origin. 

The  place  of  origin  is  limited  by  the  distribution  of  the  ancestral  group, 
and  whether  the  ancestral  group  is  canoid,  miacid,  or  creodont,  an  area  some- 
where in  the  Holarctic  is  inevitable.  The  Carnivora  did  not  reach  Africa  until 
the  Oligocene  and  South  America  until  the  Pliocene,  and  only  the  dingo  has 
arrived  in  Australia.  To  judge  by  this  evidence  and  by  the  success  of  the 
relatively  ancient  penguins,  the  Carnivora  have  never  reached  Antarctica. 
But,  although  an  origin  somewhere  within  the  Holarctic  seems  certain  on 
paleontological  grounds,  further  limitation  must  be  attempted  by  reference 
to  other  considerations.  Matthew'"^  suggested  the  Arctic  Basin  as  the  most 
likely  place,  and  the  arguments  in  its  favor  appear  overwhelming.  It  is 
centrally  placed  to  provide  the  fossil  and  living  sea  lions  of  the  North  Pacific 
and  the  fossil  and  living  seals  and  walruses  of  the  North  Atlantic.  Its  shores 
have  an  abundance  of  shallow  waters  and  wide,  long  estuaries  that  would 
provide  the  right  conditions  for  a  first  venture  into  the  marine  environment. 
The  Pacific  shores  are  steep  and  surf-battered,  with  mountain  folds  parallel  to 
the  coast.  This  difference  between  Arctic  and  Pacific  coasts  must  have  con- 
tinued throughout  Cenozoic  time  and  stems  from  fundamental  structural  and 
tectonic  differences. 

The  third  major  argument  in  favor  of  the  Arctic  Basin  as  the  birthplace  of 
the  Pinnipedia  hinges  on  the  postulate  that  they  have  always  been  cold- 
water  animals.  If  the  group  originated  as  a  cold-water  form,  it  can  have 
originated  only  in  the  Arctic,  which  was  the  only  northern  marine  region 
where  sea  temperatures  in  the  Eocene  were  comparable  with  temperatures 
tolerated  by  pinnipeds  today  and  by  those  fossil  forms  which  have  so  far 
been  discovered.  The  most  satisfactory  conclusion,  therefore,  is  that  the 
pinnipeds  originated  from  an  ancestral  dog-bear  stock  in  the  middle  or  late 
Eocene  Arctic  Basin.  From  the  Arctic  there  was  a  spread  southward  during 
succeeding  periods,  which  was  influenced  in  rate  and  extent  by  certain  geo- 
morphic  and  climatic  barriers  and  avenues. 

"  Op.  cit.  [see  footnote  i  above]. 
'■5  Op.  cit.  [see  footnote  6  above]. 

'^  W.  D.  Matthew:  Climate  and  Evolution  (2nd  edit.),  Special  Pubis.  New  York  Acad,  of  Set.,  Vol.  1, 
1939- 


546 


the  pinnipedia  479 

Geomorphic  Barriers  and  Avenues 

Much  has  been  written  on  problems  connected  with  land  mammals  and 
past  distributions  of  land  and  sea.  In  a  consideration  of  the  pinnipeds  the  same 
problems  must  be  faced,  but  from  the  opposite  direction.  Here  the  primary 
concern  is  with  the  existence  or  nonexistence  of  seaways  between  the  Arctic 
and  the  North  Pacific,  between  the  Arctic  and  the  North  Atlantic,  and  be- 
tween the  Caribbean  and  the  East  Pacific.  Studies  in  the  geography  of  land 
animals  have  been  concerned  with  the  existence  of  land  bridges  across  these 
seaways  and  obviously  have  an  important  bearing  on  the  question. 

There  is  general  agreement  that  the  two  Americas  were  separated  almost 
continuously  from  the  middle  Paleocene  to  the  late  Pliocene,  and  during  this 
time  there  must  have  been  virtually  no  obstacle  to  migration  between  the 
Caribbean  and  the  East  Pacific. 

Simpson'^  has  examined  in  detail  paleomammalogical  evidence  for  the 
existence  of  a  land  bridge  between  North  America  and  Asia  and  between 
North  America  and  Europe  during  the  Cenozoic.  A  transatlantic  land  bridge 
may  have  existed  in  the  Eocene,  and  possibly  even  in  the  Oligocene,  but 
Simpson  could  find  no  supporting  evidence.  The  problem  remains  open,  but 
it  seems  unlikely  that  there  was  any  continuous  barrier  between  the  Arctic 
Sea  and  the  North  Atlantic  at  these  times.  Considerable  marine  deposition 
took  place  throughout  Europe  during  the  early  Tertiary,  and  there  must  have 
been  seas  separating  Western  Europe  from  the  main  Eurasian  land  mass  and 
joining  the  northern  seas  with  the  Tethyan  Mediterranean.  Ekman^^  mentions 
a  probable  connection  (Obik)  betv^een  the  Tethys  Sea  and  the  Arctic  Sea 
in  the  Eocene. 

Regarding  the  North  American-Asian  bridge  across  present-day  Bering 
Strait,  Simpson  reaches  fairly  firm  conclusions  from  the  degree  of  interchange 
of  land-mammal  faunas  between  the  two  continents.  The  evidence  suggests 
that  there  was  a  land  bridge  continually,  if  not  continuously,  throughout  the 
Tertiary  except  about  the  middle  Eocene  and  the  middle  to  late  Oligocene. 
There  may  also  have  been  a  shorter  break  during  the  early  Pliocene.  From 
this  it  may  be  deduced  that  interchange  of  sea  faunas  would  have  been  pro- 
nounced at  these  three  times,  but  it  would  be  wrong  to  infer  that  it  did  not 
take  place  at  other  times.  It  seems  fairly  clear  that  in  the  million  years  or  so 

's  G.  G.  Simpson:  Holarctic  Mammalian  Faunas  and  Continental  Relationships  during  the  Cenozoic, 
Bull.  Geol.  Soc.  of  America,  Vol.  58,  1947,  pp.  613-687. 

'*  Sven  Ekman:  Zoogeography  of  the  Sea  (translated  from  the  Swedish  by  Elizabeth  Palmer; 
London,  1953),  p.  96. 


547 


480  THE   GEOGRAPHICAL   REVIEW 

of  the  Pleistocene  there  was  interchange  of  seal  populations  through  Bering 
Strait,  even  though  important  movements  of  land  mammals  took  place  across 
it.  It  is  reasonably  certain  that  there  v;^as  a  series  of  sea-level  fluctuations, 
though  Simpson  believes  the  land  connection  must  have  been  constant  in  the 
early  Pleistocene,  w^hen  most  of  the  land  movements  took  place.  To  a  great 
extent  the  Pleistocene  epoch  w^as  exceptional.  The  rapid  fluctuations  in  sea 
level  that  took  place  then  were  related  to  the  expansion  and  contraction  of 
glacier  ice,  and  no  reason  is  known  why  there  should  have  been  similar  rela- 
tively rapid  fluctuations  in  earlier  epochs.  The  most  that  can  be  assumed  is 
that  the  middle  Eocene,  the  middle  and  late  Oligocene,  and  perhaps  the 
early  Pliocene  were  times  of  exceptionally  easy  movement  between  the 
Arctic  and  the  North  Pacific.  Movements  at  other  times  would  not  have  been 
precluded,  but  there  would  have  been  much  less  time  for  them  to  occur,  and 
they  are  therefore  less  likely. 

Climatic  Barriers  and  Avenues 

Climatic  barriers,  though  less  tangible  and  potentially  less  difficult  to 
overcome,  are  none  the  less  real.  If  the  hypothesis  that  the  pinnipeds  have 
always  been  cold-water  forms  is  allowed,  it  follows  that  the  major  climatic 
barrier  to  their  spread  would  be  high  sea  temperatures.  Evidence  regarding 
Cenozoic  sea-surface  temperatures  in  the  North  Pacific  has  been  summarized 
by  Durham. ^^  There  seems  to  be  no  such  convenient  and  documented  sum- 
mary for  the  North  Atlantic,  but  the  general  history  of  its  marine  fauna 
during  the  Cenozoic  is  outlined  by  Ekman.'^  Durham's  summary  shows  that 
in  the  Eocene  the  cold-water  environment  in  the  North  Pacific  was  of  small 
extent  and  the  February  surface  isotherm  of  20°  C.  lay  somewhere  between 
50°  and  60°  N.  The  August  20°  C.  isotherm  would  have  been  even  farther 
north.  During  succeeding  epochs  there  was  a  gradual  southward  movement 
of  isotherms,  so  that  the  cold-water  environment  expanded  progressively 
until  the  early  Pliocene.  There  was  then  a  small  northward  movement, 
followed  by  increasing  cooling  in  the  Pleistocene. 

A  similar  progressive  cooling  of  the  seas  took  place  in  the  North  Atlantic. 
The  tropical  faunas  of  the  Eocene  gave  way  to  subtropical  faunas  in  the 
Oligocene,  and  these  in  turn  were  replaced  in  a  mass  invasion  of  northern 
forms  at  the  beginning  of  the  Miocene.  The  climatic  deterioration  extended 

''J.  W.  Durham:  Cenozoic  Marine  Climates  of  the  Pacific  Coast,  Bull.  Geol.  Soc.  of  America,  Vol. 
61,  1950,  pp.  1243-1263. 

'*  Op.  cit.  [see  footnote  16  above]. 


548 


THE  PINNIPEDIA  48 1 

to  the  West  Indian  region,  where,  according  to  Ekman,'^  Caribbean  tempera- 
ture "seems  to  have  sunk  from  26-27°  C.  to  19-20°."  During  the  Phocene, 
temperatures  recovered  and  tropical  faunas  reappeared  in  the  West  Indies.  A 
similar  deterioration  and  recovery  occurred  in  the  Mediterranean  region  but 
not  to  so  marked  a  degree. 

Much  less  is  known  about  fluctuations  in  sea  temperatures  in  the  Southern 
Hemisphere.  The  most  significant  feature  here  is  the  corridor  formed  by  the 
Peru  Current,  which  brings  cold  water  almost  to  the  equator.  There  is  no 
reason  for  believing  that  it  was  much  less  effective  through  the  latter  half  of 
the  Cenozoic  at  least,  and  there  is  clear  evidence  in  the  distribution  of  existing 
genera  and  species  that  the  current  has  served  as  a  route  for  pinniped  migra- 
tion on  at  least  two  occasions. 

The  conclusions  to  be  drawn  from  this  summary  of  climatic  barriers  and 
avenues  are  as  follows.  The  cold-water  environment,  defined  for  present 
purposes  as  that  where  surface  temperature  does  not  exceed  20°  C,  was  of 
small  extent  in  the  Eocene  and  was  virtually  limited  in  the  north  to  the  Arctic 
Basin.  In  the  Oligocene  and  Miocene  it  spread  considerably,  so  that  by  the 
end  of  the  Miocene  it  extended  south  to  California  and  to  the  Caribbean. 
Since  the  Central  American  isthmus  did  not  exist  at  this  time,  there  was  no 
land  barrier  between  the  cold  Caribbean  and  the  cold  west-coast  waters  of 
South  America.  There  were  thus  two  cold-water  routes  available,  one  from 
the  North  Atlantic  via  the  Caribbean  to  Peruvian  waters,  the  other  from  the 
North  Pacific  along  the  west  coasts  of  the  two  Americas.  Toward  the  end  of 
the  Pliocene,  the  route  from  the  Atlantic  disappeared  because  of  the  rein- 
vasion  of  the  Caribbean  by  tropical  waters  and  the  closing  of  the  isthmus. 
However,  the  availability  of  the  Pacific  route  depended  only  on  sea  tempera- 
tures, and  it  became  usable  again  on  several  occasions  during  the  Pleistocene. 

Family  Beginnings 

Despite  suggestions  to  the  contrary,  it  seems  unlikely  that  the  pinniped 
families  are  of  separate  origin.  There  is  general  agreement  that  seals  diverged 
from  sea  lions  and  walruses  at  a  very  early  stage  and  that  the  split  into  the 
latter  two  families  occurred  later.  The  walruses  are,  in  fact,  little  more  than 
highly  specialized  sea  lions.  In  all  three  families  the  limbs  are  used  for  swim- 
ming and  the  tail  is  vestigial.  This  suggests  that  they  are  descended  from  an 
ancestral  form  in  which  the  tail  was  too  short  to  develop  into  an  organ  of 

'^  Ibid.,  p.  71. 


549 


482  THE   GEOGRAPHICAL   REVIEW 

propulsion,  whereas  in  all  other  aquatic  mammals  it  is  used,  m  a  varyhig 
degree,  as  propeller  or  rudder  or  both.  The  physiological  researches  of 
HowelP°  strongly  suggest  that,  doghke,  the  original  pinnipeds  used  both  fore 
and  hind  hmbs  in  swimming  but  that  subsequently  they  split  into  two  groups, 
one  ancestral  to  the  seals,  in  which  use  of  the  hind  limbs  came  to  predominate, 
the  other  ancestral  to  the  sea  lions  and  walruses,  in  which  the  fore  limbs  were 
used  more  and  more.  All  the  evidence  of  present  and  past  distributions  points 
to  the  Bering  land  barrier  as  the  place  where  this  split  occurred;  for  no  sea 
lions,  either  fossil  or  existing,  are  knowm  from  the  Arctic  and  the  North 
Atlantic,  and  the  only  seals  reliably  recorded  from  the  North  Pacific  are  living 
forms  derived  during  the  Pleistocene  from  the  Arctic  and  the  North  Atlantic. 
If  the  original  split  did  take  place  at  the  Bering  barrier,  it  would  have  been 
necessary  for  the  ancestral  population  to  spread  from  the  Arctic  to  the  North 
Pacific  at  a  time  when  the  barrier  was  nonexistent,  for  the  barrier  to  reappear, 
splitting  the  population  into  two,  and  for  it  to  remain  in  existence  long 
enough  to  prevent  further  contact  and  interbreeding  between  the  two 
groups. 

The  split  between  sea-lion  and  walrus  ancestors  followed  after  an  interval 
long  enough  for  the  Pacific  group  to  acquire  the  considerable  number  of 
characters  common  to  both  families.  This  time,  population  movement  was 
reversed,  and  a  more  northern,  bottom-feeding  group  took  advantage  of 
another  sinking  of  the  Bering  bridge  to  spread  back  into  the  Arctic.  A  subse- 
quent re-emergence  of  the  land  or  increasing  ecological  specialization  then 
cut  this  group  off  for  an  indefinite  period,  so  that  it  evolved  independently 
into  the  later  walruses,  which  before  the  Pleistocene  are  known  only  from 
the  Arctic  and  the  North  Atlantic. 

It  IS  immediately  evident  that  this  picture  of  family  origins  fits  readily  into 
the  history  of  the  Bering  bridge  as  deduced  by  Simpson.  The  break  in  the 
middle  Eocene  could  have  been  that  required  for  the  spread  of  the  original 
population  between  Arctic  and  Pacific.  It  was  followed,  according  to  Simp- 
son, by  a  strong  land  connection  in  the  late  Eocene  and  the  early  Oligocene, 
which  would  have  allowed  time  for  characters  common  to  sea  lions  and 
walruses  to  develop  in  the  Pacific  group,  and  then  by  a  break  in  the  middle 
Oligocene,  which  would  have  permitted  walrus  ancestors  to  move  back  into 
the  Arctic.  However,  the  bridge  did  not  close  strongly  again  until  the  early, 
or  perhaps  even  the  middle,  Miocene,  so  that  continued  separation  of  ancestral 

"  A.  B.  Howell:  Contribution  to  the  Comparative  Anatomy  of  the  Eared  and  Earless  Seals  (Genera 
Zaloplnis  and  Phoca),  Proc.  U.  S.  Natl.  Museum,  Vol.  73,  1928,  pp.  1-142. 


550 


THE   PINNIPEDIA  483 

walruses  would  be  attributable  to  their  increasing  adaptation  to  life  in  shallow, 
northern  waters.  Prorosmarus ,  the  earliest  known  walrus,  appears  in  the  upper 
Miocene  of  Atlantic  North  America. 

Such  a  timetable  would  necessitate  a  slightly  earlier  origin  for  the  pinni- 
peds than  might  be  favored  by  most,  but  this  seems  no  insuperable  obstacle. 
A  long  interval  need  not  have  occurred  between  the  first  entry  into  the  marine 
environment  and  the  spread  from  Arctic  to  Pacific;  an  early  canoid  fissipcd 
ancestry  is  not  incompatible  with  the  sequence  of  events  postulated  above. 

The  Sea  Lions  (Otariidae) 

The  earliest  sea  lions  were  found  in  the  lower  Miocene  of  Oregon  and 
California.  According  to  the  hypothesis  of  generally  continuous  association 
between  pinnipeds  and  cold  water,  this  would  be  expected,  since  it  was  in 
the  Miocene  that  the  requisite  low  sea  temperatures  reached  California.  That 
pinnipeds  are  absent  from  Paleogene  formations  in  California,  Oregon,  and 
Washington  is  not  surprising;  for  if  the  hypothesis  is  correct,  we  can  expect  to 
find  sea-lion  forms  older  than  the  extinct  Allodesmus  and  Desinatophoca,  not 
in  the  United  States,  but  in  Eocene  and  Oligocene  marine  deposits  of  Canada 
and  Alaska.  Unfortunately,  such  deposits  are  rare  and  have  been  little  worked. 

The  cold-water  environment  spread  southward  until  by  the  end  of  the 
Miocene  or  the  early  Pliocene  it  had  reached  its  greatest  extent.  By  this  time  a 
large  number  of  sea-lion  types  had  arisen  in  the  North  Pacific;  in  addition  to 
Allodesmus  and  Desmatophoca,  the  genera  Neotherium ,  Pithaiwtaria,  Diisigna- 
thus,  PontoUs,  Atopotarus,  and  Pliopedia  have  been  named.  All  are  now  extinct. 
By  this  time  too  the  East  Pacific  cold-water  route  to  the  Southern  Hemisphere 
was  available.  The  population  groups  that  spread  along  this  avenue  were 
ancestral  to  the  present-day  southern  sea  lion,  Otaria,  the  Australian  sea  lion, 
Neophoca,  and  the  southern  fur  seal,  Arctocephalus;  and  the  earliest  known 
southern  member  of  the  family  comes  from  the  Pliocene  beds  of  the  Parana 
in  Argentina.^'  It  is  possible  that  Otaria  is  derived  from  the  same  stock  as  the 
northern  sea  lion,  Eumetopias ,  and  that  Neophoca  is  related  to  the  California 
sea  lion,  Zalophus;  Arctocephalus  is  usually  linked  with  the  northern  fur  seal, 
Callorhinus.  The  probable  lines  of  spread  of  the  ancestral  forms  are  well  shown 
by  the  distribution  of  the  present-day  sea  lions  illustrated  in  Figure  2.  All 
fossil  sea  lions  have  been  found  within  the  regions  inhabited  by  existing  forms. 

"  These  deposits  are  listed  as  Miocene  in  Kellogg,  op.  cit.  [see  footnote  6  above],  but  are  now  believed 
to  be  of  Pliocene  age  and  are  listed  as  such  in  Simpson,  The  Principles  of  Classification  .  .  .  of  Mammals 
[see  footnote  1  above]. 


551 


484 


THE   GEOGRAPHICAL   REVIEW 


Fig.  2 — Distribution  of  the  sea  lions  (family  Otariidae). 

Fig.  3 — Distribution  of  the  sea-lion  genera  Zalophus  and  Neophoca. 

When  distributions  are  examined  at  the  generic  instead  of  the  family  level, 
it  becomes  clear  that  the  East  Pacific  cold-water  route  has  been  used  on  several 
occasions;  for  the  species  that  today  occupy  sections  of  this  route  are  not 
derived  from  the  original  populations  that  spread  southw^ard  but  from  newer 
groups  that  spread  both  southward  and  northward  along  the  route  on  later 
occasions.  These  later  occasions  can  almost  certainly  be  equated  with  the 
glacial  ages  of  the  Pleistocene.  Renewed  spread  from  the  north  is  suggested 
by  the  genus  Zalophus,  represented  by  the  California  sea  lion,  which  is  found 
as  far  south  as  the  Tres  Marias  Islands  off  the  Mexican  coast,  and  by  its  close 
relative  Zalophus  woUehaeki  of  the  Galapagos  (Fig.  3).  Renewed  spread  from 
the  south  is  suggested  by  the  distribution  of  the  southern  sea  lion,  Otaria, 
which  has  spread  northward  as  far  as  northern  Peru  (Fig.  4). 

The  distribution  of  the  southern  fur  seal,  Arctocephalus ,  is  particularly 


552 


THE    PINNIPEDIA 


485 


Fig.  4 — Distribution  of  the  sea-lion  genera  Eumctopias  and  Otaria. 
Fig.  5 — Distribution  of  the  southern  fur  seals,  Arctocephaltis. 

interesting,  since  it  indicates  at  least  three  transequatorial  population  move- 
ments (Fig.  5).  The  genus  itself  is  derived  by  evolution  in  the  Southern 
Hemisphere  from  an  ancestral  stock  that  spread  southward  at  the  time  of 
general  movement  of  the  sea-lion  family,  which  is  here  assigned  to  the  late 
Miocene  or  the  early  Pliocene.  It  has  spread  successfully  throughout  the 
temperate  Southern  Hemisphere  and  has  given  rise  to  a  series  of  allopatric 
species  that  are  a  bone  of  contention  among  taxonomists.  But  according  to  a 
recent  study  by  King"  the  East  Pacific  cold-water  corridor  is  inhabited  by 
two  species,  the  ranges  of  which  overlap  considerably.  They  are  both  re- 
corded from  Juan  Fernandez,  off  Chile.  There  seems  little  doubt  that  these 
two  sympatric  species,  A.  phiUppi  and  A.  attstralis,  are  the  result  of  two 

"J.  E.  King:  The  Otariid  Seals  of  the  Pacific  Coast  of  America,  Bull.  Brit.  Museum  (.V.if.  Hist.): 
Zoology,  Vol.  2,  1954,  pp.  311-337- 


553 


486  THE   GEOGRAPHICAL   REVIEW 

separate  movements  along  the  cold-water  route.  During  a  glacial  age  of  the 
Pleistocene  an  Arctocephalus  population  spread  northward  to  California; 
during  the  subsequent  interglacial  it  became  cut  off  and  had  an  opportunity 
to  evolve  independently  into  the  A.  philippi  group.  In  a  subsequent  glacial 
it  spread  south  again,  while  at  the  same  time  the  main  A.  australis  population 
of  South  America  once  more  moved  north.  The  two  now  overlap  and  pre- 
sumably have  diverged  sufficiently  to  enable  them  to  remain  distinct  species. 

The  Walruses  (Odobenidae) 

Early  walruses,  Prorosmarus,  Alachtherium ,  and  Trichecodon,  were  ap- 
parently restricted  to  the  North  Atlantic,  but  the  fact  that  they  came  of  an 
ancestry  shared  by  the  sea  lions  implies  that  the  walruses  as  a  whole  originated 
in  the  North  Pacific  or  at  least  in  the  vicinity  of  Bering  Strait.  They  first 
appear  in  upper  Miocene  beds  of  eastern  North  America,  and  their  gravita- 
tion across  the  Arctic  and  into  the  North  Atlantic  was  part  of  a  general  move- 
ment of  marine  animals  in  this  direction  in  mid-Tertiary  time  that  is  cor- 
related with  a  southward  expansion  of  the  cold-water  habitat.  According  to 
Ekman,^^  a  considerable  part  of  the  North  Atlantic  Boreal  fauna  was  derived 
from  the  North  Pacific  about  this  time.  The  present  walrus,  Odohenus,  is  also 
essentially  Arctic-North  Atlantic  in  distribution,  and  its  entry  into  the  Bering 
Sea  is  almost  certainly  of  Pleistocene  date.  The  distribution  of  Odohenus  has 
been  discussed  and  mapped  in  an  earlier  paper. ^"^ 

The  Seals  (Phocidae) 

The  Phocidae  are  the  most  diverse  and  well  distributed  of  the  pinniped 
famihes  (Fig.  6),  and  the  members  are  best  adapted  to  marine  hfe.  Ancestral 
seals  were  separated  from  the  sea  lion-walrus  stock  at  a  very  early  stage, 
and  the  initial  development  of  the  family  undoubtedly  took  place  in  the 
Arctic-North  Atlantic  region.  By  the  middle  Miocene,  when  the  fossil 
record  begins,  at  least  five  genera  had  made  their  appearance,  and  two  of  the 
present  subfamilies,  the  Phocinae  and  the  Monachinae,  were  distinguishable. 
The  existing  genus  Phoca  was  also  recognizable.  Here,  as  in  the  North  Pacific, 
the  coincidence  is  found  between  the  southward  extension  of  the  cold-water 
environment  and  the  sudden  appearance  of  pinnipeds  in  fossil  beds,  and  here 
the  negative  fossil  record  can  be  quoted  with  greater  confidence;  for  the 
marine  Paleogene  beds  of  Europe  are  much  more  extensive  and  better  worked 

^■5  Op.  cit.  [see  footnote  16  above],  p.  159. 
"•  Da  vies,  op.  cit.  [see  footnote  4  above]. 


554 


THE   PINNIPEDIA 


487 


^ 

Vh 

/   fM 

^^^C\ 

'          1 

\  ^ 

Distribution  of 

Phocidae 

J                \           \_- 

1 

L^i 

Fig.  6 — Distribution  of  the  seals  (family  Phocidae). 

Fig.  7 — Distribution  of  the  northern  seals  (subfamily  Phocinae). 


than  those  of  North  America.  There  is  even  more  reason,  then,  for  the  con- 
clusion that  both  seals  and  walruses  were  confined  to  the  Arctic  until  the 
Miocene,  when  they  moved  south  into  the  North  Atlantic.  This  southward 
movement  to  occupy  an  expanding  environment  would  have  been  accom- 
panied by  a  marked  multiplication  of  forms  and  of  numbers,  which  would 
explain  the  comparative  variety  of  genera  and  species  named  from  the 
Miocene  and  Pliocene  of  Europe.  By  the  end  of  the  Miocene,  three  major 
groups,  which  today  are  named  as  subfamilies,  had  formed;  a  fourth  sub- 
family is  named  from  the  Pliocene. 

THE   NORTHERN    SEALS    (pHOCINAe) 

The  subfamily  Phocinae  must  always  have  been  the  northernmost  seal 


555 


488  THE   GEOGRAPHICAL   REVIEW 

group,  Since  it  alone  has  succeeded  in  invading  the  North  Pacific  across  the 
Arctic  and,  unhke  the  other  groups,  it  has  no  Southern  Hemisphere  repre- 
sentative. The  fossil  genera,  Aliophoca,  Leptophoca,  PropJwca,  Callopfwca, 
Gryphoca,  Platyphoca,  and  Phocanclla,  have  been  described  from  North 
Atlantic  shores,  and  the  existing  genera,  Phoca,  Erignathus,  and  Halichocrus, 
are  North  Atlantic  and  Arctic  in  distribution,  though  the  first  tw^o  have 
recently  separated  representatives  in  the  North  Pacific  (Fig.  7). 

THE   MONK   SEALS    (mONACHINAe) 

The  monk  seals  v^ere  v^ell  represented  in  Miocene  and  Pliocene  European 
waters  by  species  of  such  now  extinct  genera  as  Monothcriwii ,  Paleophoca ,  and 
Pristiplwca.  The  group  seems  to  have  been  in  the  van  of  phocid  expansion 
southward  and  later  in  its  history  to  have  been  particularly  characteristic  of 
the  Tethyan  Mediterranean.  Only  the  ancestors  of  the  present-day  Monachus 
survived  the  constriction  and  rewarming  of  the  Mediterranean  toward  the 
end  of  the  Pliocene,  a  feat  they  doubtless  accomplished  by  adapting  them- 
selves to  the  warmer  environment.  Thus  arose  the  one  major  exception  to  the 
rule  of  association  between  pinnipeds  and  cold  water.  Indeed,  Monachus  was 
so  successful  that,  at  a  time  when  the  Mediterranean  was  open  to  the  west,  it 
was  able  to  spread  across  the  Atlantic  to  the  Caribbean  and  enter  the  Pacific 
shortly  before  the  Central  American  isthmus  closed  toward  the  end  of  the 
Pliocene.  Subsequently,  the  Pacific  population  was  able  to  spread  to  the 
Hawaiian  Islands  (Fig.  8).  There  is  some  possibihty  that  the  spread  from 
Caribbean  to  Pacific  took  place  in  the  Pleistocene  rather  than  the  Pliocene. 
King,^^  in  a  recent  discussion  of  the  monk  seals,  points  to  many  characters  in 
which  the  Caribbean  tropicalis  population  is  much  closer  to  the  Hawaiian 
schaninslandi  population  than  to  the  Mediterranean  monachus  population.  In 
fact,  schaninslandi  and  tropicalis  appear  to  be  so  close  anatomically  that  by 
analogy  with  other  species  it  seems  doubtful  whether  they  could  have  been 
separated  since  the  Pliocene.  To  meet  this  objection,  King  suggests  an  over- 
land migration  across  Panama  in  the  Pleistocene,  but  this  seems  even  more 
doubtful,  and  if  the  transisthmian  spread  did  take  place  at  that  time,  it  is 
more  probably  related  to  a  high  sea-level  stage  during  an  interglacial.  How- 
ever, there  seems  to  be  no  other  evidence  to  substantiate  such  a  possibility. 
The  Monachus  westward  spread  seems  to  have  been  an  isothermal  one,  taking 
place  along  the  northern  fringe  of  tropical  waters. 

^5 J.  E.  King:  The  Monk  Seals  (Genus  Monachus),  Dull.  Brit.  Museum  (iVar.  Hist.):  Zoohj^y,  Vol.  3, 
19>6,  pp.  203-256. 


556 


THE   PINNIPEDIA 


489 


Fig.  8 — Distribution  of  the  monk  seals  and  Antarctic  seals  (subfamilies  Monachinae  and  Lobo- 
dontinae). 

Fig.  9 — Distribution  of  the  bladdemosed  seals  (subfamily  Cystophorinae). 

THE   ANTARCTIC    SEALS    (lOBODONTINAe) 

The  Antarctic  seals  (Fig.  8)  comprise  four  species,  each  of  which  has  been 
placed  in  a  separate  genus,  though  they  are  probably  derived  by  adaptive 
radiation  from  one  group.  The  Weddell  seal,  Leptoiiychotcs  weddelli,  lives 
farther  south  than  any  other  mammal;  it  keeps  breathing  holes  in  the  ice  and 
feeds  principally  on  fish  and  squid.  The  crabeater  seal,  Lohodon  carcinophaga , 
lives  along  the  edge  of  the  pack  ice  and  feeds  on  pelagic  crustaceans.  The 
leopard  seal,  Hydrurga  leptonyx,  ranges  from  the  ice  edge  northward  to  the 
subantarctic  islands  and  feeds  on  fish,  penguins,  and  young  seals.  The  Ross 
seal,  Ommatophoca  rossi,  is  little  known  but  seems  to  be  a  deep  diver,  feeding 
mainly  on  squid.  The  four  species  are  thus  to  some  extent  separated  geo- 
graphically, and  they  occupy  distinct  ecological  niches.  Their  evolutionary 


557 


490  THE   GEOGRAPHICAL   REVIEW 

divergence  has  an  analogy  in  the  rapid  development  o£  the  many  forms  of 
Australian  marsupials  from  a  possible  common  ancestor  that  found  itself  in  a 
continent  unpopulated  by  other  mammals.  In  the  case  of  the  Antarctic  seals, 
the  nature  of  this  common  ancestor  can  only  be  inferred  from  a  consideration 
of  anatomical  relationships. 

In  her  study  of  the  monk  seals,  King  points  to  many  relationships 
between  the  Antarctic  seals  and  the  monk  seals.  There  is  little  doubt  that  the 
two  groups  are  much  more  closely  related  than  either  is  to  any  other  group. 
In  fact,  a  few  taxonomists  include  them  both  in  the  subfamily  Monachinae. 
The  inference  to  be  drawn  from  this  is  that  the  Antarctic  seals  were  derived 
from  a  group  of  ancestral  monk  seals  that  spread  southward  to  the  Caribbean 
at  the  time  of  sea-water  cooling  in  the  Miocene  and  took  advantage  of  the 
absence  of  the  isthmian  barrier  to  enter  the  East  Pacific  cold-water  route  to 
the  south.  Unfortunately,  only  one  fossil  find  can  be  called  in  evidence  on 
this  question  of  Lobodontinae  antecedents.  A  mandible  and  some  teeth  found 
in  late  Miocene  or  early  Pliocene  beds  in  Argentina  were  given  the  name  of 
Prionodt'lphis  rovereti  and  were  later  found  to  belong  to  a  seal.  Of  these, 
Kellogg^^  says:  "The  ornamentation  and  general  configuration  of  the  crowns 
of  these  teeth  are  not  unlike  those  of  corresponding  teeth  of  the  Recent  West 
Indian  Seal,  Monachus  tropicalis.  Teeth  of  this  type  conceivably  might  also 
represent  a  stage  ancestral  to  that  of  the  Recent  Antarctic  Weddell  seal, 
Leptonychotes  weddelli.'' 

THE  BLADDERNOSED    SEALS    (cYSTOPHORINAe) 

The  bladdernosed  seals  form  much  the  smallest  seal  subfamily,  being 
represented  only  by  Mesotaria  from  the  Pliocene  of  Europe  and  by  the  living 
hooded  seal,  Cystophora,  of  the  North  Atlantic  and  the  elephant  seal,  Mi- 
rounga,o£  the  East  Pacific  and  Subantarctic  (Fig.  9).  Their  derivation  from 
the  main  seal  stock  implies  origin  in  the  North  Atlantic,  a  conclusion  sup- 
ported by  the  presence  o£  Cystophora  and  Mesotaria  in  this  region.  Invasion  of 
the  Southern  Hemisphere  would  then  have  been  roughly  contemporary  with 
that  by  the  ancestors  of  the  Antarctic  seals  and  would  have  followed  the  same 
Caribbean-East  Pacific  route.  The  elephant  seals  arose  subsequently  in  the 
Southern  Hemisphere,  where  the  existing  species,  leonina,  has  succeeded  in 
colonizing  most  of  the  anti-Boreal  zone.  It  has  also  reinvaded  the  Northern 

^*  Remington  Kellogg:  Tertiary,  Quaternary,  and  Recent  Marine  Mammals  of  South  America  and 
the  West  Indies,  Proc.  Eighth  Amer.  Sci.  Congr.,  Washington,  1940,  Vol.  3,  Washington,  1942,  pp.  445- 
473;  reference  on  p.  453. 


558 


THE  PINNIPED  I A  491 

Hemisphere  by  retracing  the  ancestral  route  of  dispersal  along  the  west  coast 
of  South  America.  But  this  later  spread  must  have  taken  place  in  a  Pleistocene 
glacial  age,  and  by  this  time  the  door  into  the  Caribbean  was  closed,  with 
the  result  that  the  product  of  the  expansion,  the  group  known  as  Miroiinga 
angnstirostris ,  is  found  in  the  Lower  California  region,  having  been  cut  off 
from  the  main  elephant-seal  population  by  the  rewarming  of  the  seas. 

Rates  of  Evolution 

The  postulation  that  pinnipeds  did  not  enter  the  Southern  Hemisphere 
until  the  late  Miocene  or  the  early  Pliocene  will  probably  meet  with  the 
objection  that  this  provides  too  little  time  for  southern  forms  to  have  de- 
veloped to  the  extent  that  they  have.  But  uneven  rates  of  evolution  are  as 
marked  in  the  pinnipeds  as  in  other  groups  of  mammals.  The  existence  of 
clearly  defmed  seals,  sea  lions,  and  walruses  by  the  Miocene  has  long  inhibited 
zoologists  from  placing  the  date  of  pinniped  origin  as  late  as  might  seem 
desirable  on  other  grounds.  It  is  even  more  notable  that  seals  of  the  modern 
genus  Phoca,  and  only  slightly  distinguishable  from  the  modern  species  Phoca 
vititliua,  are  recorded  from  the  Miocene.  The  evidence,  although  small  in 
bulk,  clearly  shows  that  there  was  comparatively  rapid  evolution  up  to  the 
Miocene  but  that  since  then  rates  have  been  extremely  slow,  at  least  in  the 
Northern  Hemisphere. 

The  general  hypothesis  of  pinniped  origin  and  dispersal  advanced  here 
seems  to  provide  a  satisfactory  explanation  for  this  change  in  the  evolutionary 
tempo.  From  what  is  known  or  inferred  about  the  evolutionary  processes, 
rates  would  have  been  rapid  in  the  early  stages  when  the  ancestral  pinnipeds 
were  first  entering  the  new  marine  environment.  Equally,  the  expansion  of 
the  cold-water  environment  from  the  late  Eocene  through  the  Oligocene  and 
Miocene  would  also  have  provided  conditions  for  rapid  evolution,  bringing, 
as  it  must  have  done,  great  increases  in  population  numbers  and  in  varieties  of 
habitats.  But  by  the  end  of  the  Miocene  the  expansion  had  come  to  a  halt:  all 
available  regions  had  presumably  been  occupied  and  most  readily  utilized 
habitats  exploited.  The  one  major  exception  was  the  Southern  Hemisphere. 
The  seal  and  sea-lion  groups  that  entered  southern  waters  discovered  a  whole 
new  cold-water  environment  in  which  they  were  able  to  multiply  enor- 
mously and  to  occupy  a  variety  of  habitats.  A  second  golden  age  of  pinniped 
evolution  dawned,  but  one  that  has  lasted  a  much  shorter  time  than  that  of 
the  Paleogene  in  the  Northern  Hemisphere.  As  a  result,  differentiation  in  the 
south  has  reached  the  generic  stage  only. 


559 


492 


THE   GEOGRAPHICAL   REVIEW 


Regional  Geography  of  the  Pinnipeds 

Sclater^'  proposed  marine  zoogeographical  regions  based  on  the  distribu- 
tion of  marine  mammals,  and  Von  Boetticher^^  re-examined  them  with 
reference  to  the  distribution  of  the  pinnipeds.  The  usefulness  of  these  regional 
defmitions  may  be  doubted,  but  it  is  worth  while  to  review  them  here  in 
order  to  summarize  some  of  the  conclusions  reached  in  the  present  study. 
Figure  lO  shows  Sclater's  regions  somewhat  modified. 


Notopelagia 


Fig.  10 — Pinniped  regions:  I,  Arctatlantis;  II,  Arctirenia;  III,  Mesatlantis;  IV,  Mesirenia;  V,  Noto- 
pelagia. The  arrows  indicate  the  two  major  dispersal  routes  between  the  Northern  and  Southern  Hemi- 
spheres. 

I.  Arctatlantis  extends  from  Bering  Strait  across  the  Arctic  to  about  the 
August  sea-surface  isotherm  of  20°  C.  It  is  the  region  of  development  of  the 
seals  and  walruses,  and  there  is  no  evidence  that  the  sea  lions  have  ever 
penetrated  it.  It  is  characterized  today  by  the  presence  of  Halichoerm  and 
Cystophora,  which  are  endemic,  and  by  Phoca,  Erignathus,  and  Odohcnus, 
which  were  probably  endemic  until  the  Pleistocene. 

II.  Arctirenia  extends  from  Bering  Strait  south  to  about  the  August  sea- 
surface  isotherm  of  20°  C.  Here  the  sea  lions  developed  and  still  have  their 
headquarters.  The  walruses  must  have  originated  in  the  extreme  north  of 
Arctirenia  but  early  moved  into  Arctatlantis.  Both  seals  and  walruses  spread 
into  the  northern  section  of  Arctirenia  during  the  Pleistocene;  earlier  in- 

^^  Op.  cit.  [see  footnote  3  above]. 
^'  Op.  cit.  [see  footnote  2  above]. 


560 


THE    PINNIPEDIA  493 

cursions  may  have  occurred  but  left  no  trace.  The  region  is  characterized 
by  the  presence  of  Callorhinus  and  Ewnetopias,  which  are  endemic,  and  by 
Zalophus,  which  would  be  endemic  if  it  had  not  spread  to  the  Galapagos. 
Comparatively  recently,  Phoca,  Eri^nathus,  and  Odohemis  entered  from  the 
Arctic  and  Arctocephalus  and  Aliroim^a  spread  into  the  extreme  southeast  off 
Lower  California. 

III.  Mcsatlantis  comprises  the  Mediterranean  and  Caribbean  Seas. 

IV.  Mesirenia  consists  of  the  seas  around  the  Hawaiian  Islands.  Regions 
III  and  IV  are  the  home  of  the  relic  genus  Monachus,  the  only  surviving  monk 
seal,  which  is  endemic  and  the  only  form  that  occurs  here. 

V.  Notopelagia  extends  from  Antarctica  northward  to  about  the  February 
sea-surface  isotherm  of  20°  C.  and  thus  includes  the  Southern  Ocean  and  the 
coastal  waters  of  Chile  and  Peru.  All  forms — Lohodon,  Omniatophoca, 
Leptoriycfwtes ,  Hydrur<^a,  Mirounga,  Otaria,  Neophoca,  and  Arctocephalus — are 
endemic  except  that  Mirounga  and  Arctocephalus  have  partly  invaded  Arcti- 
renia.  All  have  evolved  in  the  Southern  Hemisphere  from  ancestral  groups 
derived  from  the  north. 


561 


A  Numerical  Analysis  or  tne 
Distributional  Patterns  or  Nortn 
American  Mammals.  11.  Re -evaluation 
or  tne  Provinces 


EDWIN  M.  HAGMEIER 


Abstract 


In  an  earlier  paper,  numerical  techniques  were  developed  and  used  to  analyze  distribu- 
tion patterns  of  the  native  terrestrial  mammals  of  North  America.  An  error  in  method  is 
here  corrected,  indicating  that  35  provinces,  13  superprovinces,  four  subregions,  and  one 
region  may  be  recognized.  The  methods  used  are  relatively  objective,  quantitative,  and 
suited  to  computerization. 


Introduction 

In  an  earlier  paper  ( Hagmeier  and  Stults, 
1964,  hereafter  referred  to  as  H  &  S ) ,  quan- 
titative and  relatively  objective  methods 
were  used  to  demonstrate  that  ( 1 )  the 
range  limits  of  North  American  terrestrial 
mammals  are  grouped,  (2)  that  as  a  result 
it  was  possible  to  delimit  geographic  re- 
gions of  faunistic  homogeneity  which  were 
termed  mammal  provinces,  and  (3)  that 
such  provinces  could  be  useful  in  the  analy- 
sis of  other  zoogeographic  phenomena. 

This  paper  is  concerned  with  the  recal- 
culation of  some  of  the  data  of  the  second 
item  above.  It  was  assumed  in  our  earher 
paper  (H  &  S)  that  several  of  the  large 
provinces  of  the  northern  half  of  the  con- 
tinent required  further  analysis.  On  initia- 
tion of  this  analysis,  it  became  apparent  that 
an  error  in  method  had  been  made  which 
required  correction.  As  a  consequence  of 
the  correction,  the  number  of  North  Ameri- 
can mammal  provinces  is  here  increased 
from  22  to  35,  two  of  which  are  of  uncertain 
status. 

The  general  philosophy,  methodology, 
and  conclusions  reached  in  our  earlier  paper 
( H  &  S )  do  not  differ  from  those  arrived 
at  here,  and  the  earlier  paper  should  be 
referred  to  for  accounts  of  these.   The  ma- 


terial given  here,  since  it  is  essentially  re- 
visionary,  is  presented  in  as  brief  a  form  as 
possible.  Because  of  the  changes  reported 
here,  the  analysis  of  mammal  areas  given  in 
H  &  S  (p.  141-146  and  Figs.  6c-8d)  needs 
revision,  and  this  revision  will  form  the  sub- 
ject of  a  future  paper.  Since  submission 
of  our  earlier  paper  (H  &  S),  Simpson 
( 1964 )  has  considered  variation  in  abun- 
dance of  species  of  North  American  mam- 
mals in  a  superior  manner,  and  his  work 
should  be  referred  to  for  a  treatment  of  the 
subject. 

Derivation  of  Provinces 

In  our  earlier  paper  ( H  &  S ) ,  the  ranges 
of  all  242  species  of  native  terrestrial  North 
American  mammals  were  converted  into  a 
model,  first  by  separately  computing  the 
percentage  of  species  and  genera  whose 
ranges  ended  within  blocks  50  miles  by  50 
miles  throughout  the  continent  (each  such 
value  was  called  Index  of  Faunistic  Change, 
or  IFC),  second  by  plotting  species  and 
genus  IFCs  on  maps  of  North  America,  and 
third  by  fitting  isarithms.  The  species  IFC 
map  resulting  was  given  as  H  &  S,  Figure 
1.  Low  IFC  values  indicated  faunistic 
homogeneity,  and  regions  characterized  by 
such   values   were  termed  primary   areas. 


279 


562 


280 


SYSTEMATIC  ZOOLOGY 


Fig.  1.     Eighty-six  primary  areas  derived  through  examination  of  IFC  Map  ( H  &  S,  Fig.  1 ). 


Twenty-four  of  these  were  identified  through 
examination  of  IFC  maps  of  both  species 
and  genus  and  species  checklists  of  each 
were  prepared  (H  &  S,  Table  2).  The  per- 
centage of  species  common  to  all  combina- 
tions of  pairs  of  provinces  (Coefficients  of 
Community,  or  CCs,  Jaccard,  1902)  were 
then  computed.  CCs  were  then  subjected 
to  cluster  anah  sis  using  the  weighted  pair- 
group  method,  and  simple  averages  (Sokal 
and  Sneath,  1963:180-184,  304-312;  H  &  S: 
132,  137),  and  drawn  up  in  the  form  of  a 
dendrogram  (H  &  S,  Fig.  5).  Primary  areas 
pooled  at  a  mean  CC  level  lower  than  62.5% 
were  termed  mammal  provinces,  those  pool- 


ing at  below  39%  were  teraied  mammal 
superprovinces,  those  below  22.5%,  mam- 
mal subregions,  those  below  8%  as  mammal 
regions. 

The  basis  of  our  error  lay  in  the  fact  that 
we  attempted  to  identify  only  the  24  North 
American  mammal  areas  corresponding  to 
those  described  by  Kendeigh  ( 1961 )  in  his 
modification  of  Dice's  (1943)  scheme  of 
biotic  provinces.  This  error  became  appar- 
ent only  when  subsequent  analysis  of  parts 
of  certain  of  these  provinces  showed  that 
the  parts  in  some  cases  merited  full  prov- 
ince status. 

The  correction  made  and  reported  here 


565 


DISTRIBUTION  OF  NORTH  AMERICAN  MAMMALS 


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Fig.  2.  Final  trellis  or  matrix  giving  Coefficients  of  Community  ( percentage  of  species  common  to 
pairs  of  provinces).  Ordering  of  provinces  is  that  resulting  from  cluster  analysis.  Heavy  lines  outline 
superprovinces  and  subregions.  The  classes  of  shading  shown  in  the  mirror  image  are  determined  by 
the  critical  mean  CC  values  used  to  obtain  higher  categories  of  areas. 


571 


DISTRIBUTION  OF  NORTH  AMERICAN  MAMMALS  289 

consisted  of  laying  a  transparent  overlay  of  primary  areas  with  CCs  higher  than  65% 

over  the  species  IFC  map  ( H  &  S,  Fig.  1 )  (as  determined  by  actual  calculation  or  by 

and  drawing  hues  through  all  regions   of  averaging    during    cluster    analysis)    were 

high  IFC  value,  dehmiting  ultimately  a  total  pooled    to    create    secondary    areas.     The 

of  86  (rather  than  the  original  24)  primary  whole  process  was  then  repeated.    A  new 

areas.   The  distribution  of  these  is  given  as  species  checklist  was  prepared  for  each  area, 

Figure  1.  The  genus  IFC  map  was  not  used  CCs    were    computed    and    subjected    to 

in  the  corrected  analysis.  cluster   analysis,    and   a   new   dendrogram 

Subsequent  procedure  was  that  of  our  prepared.  Pooling  of  areas  was  again  done 
earlier  paper.  Species  checkHsts  of  each  of  where  CC  values  were  higher  than  65%. 
the  primary  areas  were  prepared,  and  CCs  In  all,  four  such  sets  of  sequential  opera- 
were  computed  and  subjected  to  cluster  tions  were  carried  out.  In  the  final  opera- 
analysis.  Because  of  the  large  number  of  tion,  the  total  number  of  primary  areas  had 
CCs  involved  (86!  =3,741),  calculation  of  been  reduced  from  86  to  38  secondary  areas, 
CCs  in  this  and  subsequent  operations  was  all  but  three  of  which  had  CCs  lower  than 
done  by  computer.  65%  (2E  and  2W,  6E  and  6W,  and  7E  and 

In  our  earlier  paper  (H  &  S:  137-138),  7W;  see  Figs.  2  and  3).  These  three  sets 
a  mammal  province  was  defined  as  an  area  of  secondary  areas  were  not  pooled  because 
with  a  mean  CC  of  62.4%)  or  less,  when  com-  they  occur  over  large  geographic  areas  and 
pared  to  other  areas  by  cluster  analysis,  because  I  was  concerned  with  their  detailed 
This  decision  was  based  on  the  work  of  analysis.  The  35  secondary  areas  with  CCs 
Preston  (1962),  who  found  that  analysis  of  less  than  65%  constitute  mammal  provinces 
faunas  by  means  of  a  "Resemblance  Equa-  by  the  standards  used  here  and  are  so 
tion"  (RE)  indicated  that  values  oi  z  (as  treated,  although  two  pairs  of  these  fall 
derived  from  the  RE )  of  about  0.27  repre-  within  the  questionable  range  60-65%  ( 15 
sented  the  break  between  faunistic  homo-  and  16,  34  and  35,  see  Fig.  4 ) .  Figure  2  is 
geneity  and  heterogeneity.  In  our  earher  the  matrix  resulting  from  cluster  analysis, 
paper  we  converted  z  to  S  (Similarity),  showing  ordering  of  provinces  and  Coeffici- 
where  S  =  100  (l-z),  and  calculated  both  ents  of  Community  between  pairs.  Figure 
S  and  CC  for  all  items  in  the  matrix.  These  3  is  a  map  showing  geographic  distribution 
were  compared  by  regression,  giving  a  slope  of  the  provinces,  and  Figure  4  is  a  dendro- 
b  =  1.17  ±  0.02.  Conversion  of  Preston's  gram  delineating  the  faunistic  relationships 
critical  z  value  to  S  gave  an  S  of  73%,  and  existing  between  provinces,  as  determined 
conversion  of  the  critical  value  of  S  to  CC  by  cluster  analysis.  A  species  checklist  for 
equaled  73/1.17  =  62.4%,  and  hence  our  use  each  of  the  provinces,  as  it  was  used  in  the 
of  this  value.  We  did  not,  however,  allow  final  operation,  is  given  as  Table  1. 
for  the  effects  of  statistical  error.  If  this  is  In  our  earher  paper  (H  &  S),  mammal 
incorporated,  in  the  form  of  plus  and  minus  provinces  were  grouped  into  the  higher  cat- 
two  standard  errors  ( providing  limits  at  the  egories  of  superprovinces,  subregions,  and 
95%  level  of  probabihty),  the  critical  CC  regions.  The  method  used  in  deriving  these 
value  falls  within  the  range  60.30-64.60%.  was  to  draw  lines  across  the  dendrograms  at 
As  a  result,  in  this  and  subsequent  papers  I  suitable  CC  levels,  the  choice  of  CC  level 
propose  the  use  of  a  CC  value  of  65%  as  being  arbitrary  but  providing  what  ap- 
critical  for  the  determination  of  mammal  peared  to  be  a  useful  classification  (H  &  S: 
provinces.  This  is  a  conservative  standard,  139-140,  149).  I  have  tried  here  to  make 
and  all  values  lying  between  60  and  65%  as  little  change  from  the  original  scheme  as 
should  be  considered  suspect,  and  are  re-  possible;  however,  a  small  number  of  minor 
ported.  adjustments  have  been  necessary. 

The  results  of  cluster  analysis  were  evalu-  The  0-8%  CC  range  of  the  dendrogram 

ated  according  to  this  new  standard.   Pairs  still  stands  as  a  level  useful  for  the  category 


572 


290 


SYSTEMATIC  ZOOLOGY 


ALASKAN 


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Fig.  3.     Final  grouping  of  primary  areas  into  mammal  provinces.    Broken  lines  indicate  subdivisions 
of  provinces.    The  approximate  relationships  of  island  faunas  are  also  shown. 


of  region.  At  this  level,  one  region,  the 
Nearctic  is  isolated.  Subregions  in  our  ear- 
lier paper  stood  between  the  20-25%  CC 
range;  this  is  changed  here  to  the  22-27%  CC 
range,  and  still  encompasses  four  subre- 
gions, following  Wallace  ( 1876 ) .  The  cate- 
gory of  superprovince  was,  in  the  earlier 
paper,  set  at  a  mean  CC  level  of  about  39%. 
The  selection  of  this  value  was  based  on 


conclusions  reached  by  Savage  (1960),  de- 
tails of  which  may  be  obtained  from  H  &  S, 
p.  139-140.  The  39%  level  would,  in  the 
case  of  the  dendrogram  used  here  ( Fig.  4 ) 
give  11  superprovinces.  Several  cluster  at  a 
level  very  httle  higher  than  this,  and  I  have 
arbitrarily  moved  the  limit  up  to  about 
42.5%,  so  as  to  encompass  these,  giving  a 
total  of  13  superprovinces.   These  decisions 


Fig.  4.  Final  dendrogram  showing  relationship  between  provinces.  Ordering  of  provinces  and  mean 
Coefficients  of  Community  ( CC )  are  the  results  of  cluster  analysis.  Solid  vertical  lines  show  mean  CC 
levels  at  which  regions,  subregions,  superprovinces,  and  provinces  segregate.  The  three  vertical  lines 
for  provinces  represent  the  mean  critical  value  plus  and  minus  two  standard  errors.  Per  cent  similarity 
is  mean  Coefficient  of  Community  ( CC ) .  The  "diamonds"  of  provinces  2,  6,  and  7  represent  the  mean 
CCs  at  which  the  subdivisions  of  these  provinces  pool  on  cluster  analysis. 


573 


DISTRIBUTION  OF  NORTH  AMERICAN  MAMMALS 


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292 


SYSTEMATIC  ZOOLOGY 


continue  to  fill  the  desirable  requirements 
outlined  in  our  earlier  paper. 

Good  single  values  for  each  of  these  hier- 
archic levels  would  be:  provinces  62.5%, 
superprovinces  42.5%,  subregions  25%,  and 
regions  5%.  By  this  scheme  the  35  mammal 
provinces  of  North  America  are  grouped 
into  13  superprovinces,  four  subregions,  and 
one  region.  These  are  named  and  their  dis- 
tributions mapped  on  Figures  5a  and  5b. 
They  are  also  blocked  out  in  the  matrix 
(Fig.  2)  and  marked  by  lines  drawn  at  ap- 
propriate CC  levels  on  the  dendrogram 
(Fig.  4).  The  problem  of  nomenclature  of 
mammal  areas  is  discussed  subsequently. 

The  nearest  approach  to  the  biotic  prov- 
inces of  Dice  ( 1943),  and  Kendeigh  ( 1961 ) 
through  the  analysis  carried  out  here,  is  ob- 
tained by  fitting  a  line  at  about  the  54% 
CC  level  of  the  dendrogram.  The  more  in- 
tuitive decisions  of  these  workers  implies  a 
degree  of  segregation  about  10%  lower  than 
the  one  used  here. 

Nomenclature  and  Status  of  Areas 

No  changes  in  the  names  or  status  of 
regions  or  subregions  over  those  of  our 
earlier  paper  have  resulted  from  the  reanal- 
ysis.  Because  of  the  increase  in  numbers  of 
provinces  however,  minor  adjustments  in 
these  and  in  other  categories  have  been 
obligatory. 

As  few  name  changes  as  possible  have 
been  made.  Where  new  names  have  been 
appHed,  an  attempt  has  been  made  to  take 
them  from  the  literature  and  to  apply  them 
on  the  basis  of  priority.  Where  there  has 
been  need  to  coin  names,  I  have  tried  to 
follow  the  spirit  of  earher  workers.  As  an 
aid  to  recognition,  names  of  provinces  are 
in  the  form  of  adjectives,  names  of  super- 
provinces  in  the  form  of  nouns. 

Those  cases  in  which  provinces  segregate 
within  the  doubtful  60-65%  CC  range,  or  in 
which  segregation  occurs  at  a  level  only 
slightly  higher  than  657©,  are  here  de- 
scribed. More  detailed  analyses  will  doubt- 
less result  in  some  changes  in  status  within 
these  groups. 


The  following  provinces  are  new  and 
have  been  named  by  me:  no.  1,  Ungavan; 
no.  12,  Humboldtian;  no.  25,  Kaibabian;  no. 
30,  Uintian;  no.  31,  San  Matean;  no.  34, 
DiabHan  and  no.  35,  San  Bernardinian. 
Those  provinces  that  are  new  but  that  have 
been  given  an  older  name  are,  together  with 
the  source  of  the  name:  no.  3,  Alaskan 
(Allen,  1892);  no.  5,  Yukonian  (Cooper, 
1859);  no.  10,  Vancouverian  (Van  Dyke, 
1939);  no.  13,  Sierran  and  no.  23,  Colum- 
bian (Miller,  1951).  The  names  Saskatche- 
wan and  Mapimi  are  here  converted  to  the 
adjectival  forms,  Saskatchewanian,  ai?d 
Mapimian. 

The  Hudsonian  (no.  6)  is  a  new  province. 
The  name  was  formerly  applied  to  the  prov- 
ince here  termed  Canadian  (no.  7),  and 
the  Canadian  of  earlier  workers  is  here 
termed  Alleghenian  (no.  14),  following  the 
precedence  set  by  Cooper  (1859),  and 
Allen  (1892),  after  Kendeigh  (1954).  The 
Carolinian  ( 16 )  is  a  new  province.  The 
name  was  applied  to  what  is  here  largely 
represented  by  the  Louisianian  province 
(22),  in  our  earlier  paper.  Its  present  ap- 
plication is  the  correct  one,  however,  by  the 
standards  of  older  workers.  The  Louisian- 
ian should  properly  be  called  the  Austrori- 
parian,  following  Dice  (1943),  Kendeigh 
(1961),  and  H  &  S.  Because  it  has  super- 
province  as  well  as  province  status,  and  re- 
quires the  nounal  form  of  the  same  as  well 
as  an  adjectival  one,  I  have  applied  Allen's 
(1892)  terminology  to  it. 

Not  all  provinces  segregate  clearly.  The 
northern  limit  of  no.  3,  the  Alaskan,  was  dif- 
ficult to  locate,  it  being  a  region  of  broad 
transition.  Its  mapped  limit  is  relatively 
arbitrary.  The  Sitkan  province  of  H  &  S  is 
here  included  in  the  Yukonian  (no.  5),  and 
the  Vancouverian  (no.  10),  clustering  with 
the  former  with  a  CC  of  76%.  That  part  of 
the  Yukonian  province  made  up  of  the 
Brooks  Range  very  nearly  segregates  with  a 
CC  of  66%. 

The  Eskimoan,  Hudsonian,  and  Canadian 
provinces  (nos.  2,  6,  and  7)  have,  for  rea- 
sons given  elsewhere,  each  been  split  into 
eastern  and  western  components.  Of  these, 


575 


DISTRIBUTION  OF  NORTH  AMERICAN  MAMMALS 


293 


OREGON 
COLUMBIA 

CALIFORNIA 
MOHAVE 

MAPIMI 

NAVAHO 


a.  SUBREGIONS 


b.  SUPERPROVINCES 


Fig.  5,  a  and  b.     The  distribution  of  mammal  subregions  and  mammal  superpiovinces,  as  determined 
from  the  dendrogram. 


the  Eskimoan  components  cluster  with  a 
CC  of  67%,  and  the  Canadian  with  a  CC  of 
66%.  These  are  nearly  critical  values,  indi- 
cating that  the  components  ahnost  merit 
province  status. 

The  Oregonian  (no.  11)  almost  segre- 
gates into  western  coastal  and  eastern  Cas- 
cadian  provinces,  pooHng  with  a  CC  of  66%. 
The  Alleghenian  (no.  14)  segregates  from 
the  eastern  component  of  the  Canadian  (no. 
7)  with  a  CC  of  only  64%,  a  critical  value. 
It  clusters  with  the  CaroHna  superprovince 
on  analysis,  however,  and  does  so  with  prov- 
ince rating. 

The  Carolinian  (no.  16)  is  not  a  clearly 
defined  province  and  probably  should  have 
been  pooled  with  the  Illinoian  (no.  15),  the 
two  clustering  with  a  CC  of  64%.  The  Car- 
olinian is  made  up  of  three  distinctive  geo- 
graphic components;  that  east  of  the  Appa- 
lachian Mountains  clusters  with  the  rest  of 
the  province  with  a  CC  of  67%,  and  that  of 
the  Ozark  Mountains  clusters  at  66%.  Two 
of  these  components  are  distinct  enough 
from  the  Illinoian  that  I  have  provisionally 
kept  the  Carolinian  as  a  full  province. 


The  Balconian  (no.  19)  was  incorrectly 
identified  by  H  &  S  as  part  of  what  is  here 
called  the  Tamaulipan  (no.  20).  The  Bal- 
conian in  its  present  sense  stands  as  a  full 
province. 

The  Louisianian  (no.  22),  under  the 
name  Austroriparian,  was  in  part  identified 
as  the  Carolinian  by  H  &  S.  Its  distribution 
as  determined  by  reanalysis  is  the  more 
realistic  one. 

The  larger  part  of  the  Columbian  prov- 
ince (no.  23)  was  named  Artemesian  by 
H  &  S.  The  latter  tenn  is  here  applied  to  a 
restricted  portion  of  the  Columbian  as  prov- 
ince no.  24.  The  Palusian  of  H  &  S  is 
here  pooled  with  the  Columbian,  with  a 
CC  of  70%. 

The  Mohavian  province  (no,  32)  presents 
something  of  a  puzzle.  It  was  not  recog- 
nized through  examination  of  the  IFC  map 
but  appeared  through  scrutiny  of  individ- 
ual species  maps.  Once  recognized,  how- 
ever, cluster  analysis  caused  it  to  segregate 
out  to  the  extent  of  meriting  superprovince 
status,  and  I  have  accepted  it  as  this.  Its 
geographic  limits,  however,  have  been  de- 


576 


294 


SYSTEMATIC  ZOOLOGY 


termined  subjectively,  and  they  should  be 
considered  as  suspect. 

The  Diablian  (no.  34)  is  also  of  uncer- 
tain status,  as  it  clusters  with  the  San  Ber- 
nardinian  (no.  35)  with  a  CC  of  617o,  a 
critical  value.  Because  not  all  of  the  latter 
occurs  in  the  area  studied,  its  analysis  is 
incomplete,  and  for  this  reason  the  distinc- 
tion is  provisionally  accepted  here. 

Of  superprovinces,  the  Texas,  Columbia, 
Mapimi,  and  Mohave  are  new,  and  the 
names  Hudson  and  Austroriparian  of  H  & 
S  are  replaced  by  the  names  Canada  and 
Louisiana,  for  reasons  given  elsewhere. 

Insular  Faunas 

Sixt\'-four  species  (27%)  of  the  total 
mammal  fauna  occur  on  the  larger  islands 
adjacent  to  the  continent  and  on  the  islands 
of  the  Great  Lakes.  Insular  faunas  were  in 
each  case  compared  with  the  faunas  of 
several  of  the  nearest  mainland  provinces 
by  means  of  the  Coefficient  of  Community 
and  Simpson's  Coefficient  ( SC ) .  The  latter 
is  a  measure  of  the  percentage  of  species 
occurring  on  an  island  that  also  occur  in 
in  the  mainland  province  (Simpson,  1943; 
H  &  S:    131).  Results  are  given  in  Table  2. 

Most  island  faunas  give  a  CC  much  lower 
than  Preston's  critical  65%  value  when  com- 
pared with  the  faunas  of  adjacent  mainland 
provinces  (Table  2).  Most  islands  would 
therefore  merit  full  province  status,  if  this 
standard  were  to  be  applied.  The  generally 
low  CC  obtained,  however,  is  the  result  of 
the  small  size  of  insular  faunas,  a  bias  being 
introduced  as  a  consequence  of  it.  Simp- 
son's Coefficient  is,  in  these  circumstances, 
a  more  reliable  measure,  and  I  attribute 
greater  significance  to  it.  No  critical  value 
of  SC  is  available,  however.  Because  of 
this,  and  because  there  is  more  interest 
in  similarities  than  dissimilarities,  island 
faunas  have  in  all  cases  been  named  as  part 
of  the  fauna  of  the  adjacent  province  to 
which  they  show  nearest  relationship  as 
determined  primarily  by  Simpson's  Coef- 
ficient. 


Table  2. 


Island 

No.  of 
species 

Adjacent 
provinces 

CC 

SC 

Long  Island 

29 

14  Alleghanian 
16  Carolinian 

51 
52 

93 
61 

Cape  Breton 

31 

14  Alleghanian 
7E  E.  Canadian 

55 
64 

94 

87 

Prince  Edward 
Island 

29 

7E  E.  Canadian 
14  Alleghanian 

68 
48 

93 
90 

Anticosti 

5 

6E  E.  Hudsonian 
7E  E.  Canadian 
14  Alleghanian 

17 
13 
10 

100 
100 
100 

Newfoundland 

12 

6E  E.  Hudsonian 
7E  E.  Canadian 
14  Alleghanian 

40 
28 
19 

100 
92 
83 

Belcher 

3 

1  Ungavan 
6E  E.  Hudsonian 
7E  E.  Canadian 

25 
10 

3 

100 
100 

33 

Manitoulin 

25 

14  Alleghanian 
7E  E.  Canadian 

49 
62 

100 
96 

Isle  Royale 

9 

7E  E.  Canadian 
14  Alleghanian 

24 
18 

100 
100 

Arctic  Archi- 
pelago 
Kodiak 

10 
12 

2E  E.  Eskinioan 
1   Ungavan 
5  Yukonian 
4  Aleutian 
3  Alaskan 

67 
57 
33 
57 
39 

100 
80 

100 
92 
85 

Alexander  Archi 
pelago 

-  21 

10  Vancouverian 
5  Yukonian 

61 
44 

95 
90 

Queen  Charlottes  12 

10  Vancouverian 
5  Yukonian 

36 
24 

92 
83 

Vancouver 

22 

11  Oregonian 
10  Vancouverian 

33 
54 

83 
79 

Long  Island  shows  closest  relationship  to 
the  Alleghenian  province  (no.  14),  not  the 
Carolinian  (no.  16),  as  might  have  been 
expected.  Cape  Breton  is  nearest  to  the 
Alleghenian  by  Simpson's  Coefficient;  I 
have  placed  it  there  though  it  shows  a  very 
high  CC  with  the  eastern  Canadian  (64%)r 
Prince  Edward  Island  lies  nearest  to  the 
eastern  Canadian  province  (no.  7E),  which 
is  surprising  in  the  light  of  its  geographic 
proximity  to  the  Alleghenian.  Anticosti  is 
grouped  with  the  eastern  Hudsonian  (no. 
6E ),  on  the  basis  of  its  high  CC,  as  is  New- 
foundland, the  latter  on  the  basis  of  both 
coefficients.  Belcher  Island  is,  because  of 
its  CC  only,  treated  as  being  most  closely 
related  to  the  Ungavan  (no.  1).  Manitoulin 
has  highest  SC  with  the  Alleghenian,  high- 


577 


DISTRIBUTION  OF  NORTH  AMERICAN  MAMMALS 


295 


est  CC  with  the  eastern  Canadian,  but  be- 
cause greater  weight  is  given  to  Simpson's 
Coefficient,  I  have  grouped  it  with  the 
Alleghenian.  Isle  Royale  shows  closest  af- 
finity with  the  eastern  Canadian  province. 

Of  the  islands  of  the  west  coast,  the  Alex- 
ander Archipelago  and  the  Queen  Charlotte 
Islands  show  closest  relationship  to  the 
Vancouvarian  (no.  10).  Vancouver  Island, 
on  the  basis  of  its  SC  only,  is  closest  to  the 
Oregonian  (no.  11). 

Kodiak  Island  has  highest  CC  with  the 
Aleutian  (no.  4),  but  highest  SC  with  the 
Yukonian  (no.  5),  and  following  the  policy 
set  previously  is  considered  most  closely  re- 
lated to  the  latter. 

Of  the  Arctic  archipelago  and  Greenland, 
the  following  groups  of  islands  have  identi- 
cal faunas:  group  1,  Baffin,  Southampton, 
and  Coats  islands;  group  2,  Somerset  Island; 
group  3,  Banks  Island;  group  4,  Greenland, 
Sverdrup  Islands,  Borden  and  Prince  Pat- 
rick islands;  group  5,  Victoria,  Prince  of 
Wales,  Melville,  Bathurst,  Comwalhs, 
Devon,  and  Ellesmere  islands.  The  faunas 
of  these  groups  of  islands,  together  with 
those  of  the  Ungavan  and  eastern  Eskimoan 
provinces  (nos.  1  and  2E)  were  analyzed 
by  first  computing  Coefficients  of  Com- 
munity between  them,  then  subjecting 
these  to  cluster  analysis,  using  the  methods 
outlined  previously.  All  of  the  island  groups 
cluster  at  a  mean  level  of  61%  or  higher, 
falling  within  the  critical  range  or  better. 
The  groups  taken  together  segregate  from 
the  eastern  Eskimoan  with  a  mean  CC  of 
54%  and  from  the  Ungavan  with  a  mean 
CC  of  44%.  The  equivalent  mean  SCs  are 
1007o  and  85%  respectively.  As  a  result  I 
have  treated  all  of  the  Arctic  archipelago 
and  Greenland  as  part  of  the  eastern  com- 
ponent of  the  Eskimoan  province. 

A  generalized  mapping  of  these  relation- 
ships is  given  in  Figure  3.  It  should  be 
noted  that  the  affinities  of  Cape  Breton, 
Prince  Edward  and  Long  islands  are  indi- 
cated incorrectly  here. 

Discussion 
The    general    conclusions    reached    as    a 


result  of  this  re-evaluation  differ  in  no  way 
from  those  obtained  through  our  earlier 
analysis  (H  &  S;  147-151),  and  they  are 
not  treated  further.  It  is  important  that  the 
subjectivity  of  the  methods  used  here  be 
kept  in  mind  however.  The  sources  and 
attempted  controls  of  these  have  been  dis- 
cussed in  our  earlier  paper  (H  &  S:  148- 
149,  151 )  and  include  taxonomic  errors,  dis- 
tributional errors,  choice  of  point  or  block 
for  sample;  size  of  sample  block,  fitting  of 
isarithms,  selection  of  primary  areas,  choice 
of  coefficient  of  association,  choice  of  clus- 
tering method,  and  others. 

The  methods  used  here  are  ideally  suited 
to  computer  techniques.  This  reanalysis 
could  not  in  fact  have  been  completed 
within  reasonable  time  had  such  techniques 
not  been  available.  Miller,  Parsons,  and 
Kof sky  ( 1960 )  have  described  the  use  of 
so-called  successive  scanning  mode  micro- 
densitometers,  which  automatically  map  the 
densities  of  films  and  other  kinds  of  trans- 
parencies. Such  devices  are  sold  by  Beck- 
man  and  Whitley  of  San  Carlos,  California, 
under  the  registered  trade  name  of  Iso- 
densitracer.  The  use  of  such  a  device  on  a 
transparent  map  showing  the  distribution  of 
all  North  American  mammals  drawn  in  inks 
or  paints  which  gave  progressively  less 
translucency  as  additional  layers  were 
added,  would  be  ideal  in  the  development 
of  more  refined  IFC  maps. 

The  IFC  map  used  in  this  work  ( H  &  S, 
Fig.  1)  was  based  on  the  computation  of  the 
percentage  of  species  whose  ranges  ended 
within  blocks  50  miles  to  a  side.  The  abso- 
lute value  of  an  IFC  is  a  function  of  size  of 
block  (H  &  S:  148).  I  suggest  that  any 
future  use  of  IFCs  incorporate  as  subscript 
to  values  given,  a  statement  of  the  area  of 
the  block  in  kilometers.  Converting  size  of 
block  used  here  to  square  kilometers  gives 
an  area  per  block  of  approximately  6,500 
square  kilometers,  and  the  IFCs  used  here 
are  symbolized  as  IFCe.Goo-  Subscripts  made 
up  of  a  statement  of  length  of  side  of  a 
block  rather  than  area  would  be  less  cum- 
bersome.    I    suspect   however   that   circles 


578 


296 


SYSTEMATIC  ZOOLOGY 


may  prove  more  useful  than  blocks  as  sam- 
pling units,  especially  if  microdensitometers 
are  used,  which  make  the  use  of  area 
necessary. 

Since  preparation  of  our  earlier  study,  a 
number  of  similar  papers  have  been  drawn 
to  my  attention  or  have  been  published. 
Munroe  ( 1956 )  gave  a  fine  account  of  the 
ecologic  and  zoogeographic  features  of  Can- 
ada and  an  analysis  of  the  insect  faunas  of 
the  continent.  Udvardy  ( 1963 )  provided  an 
excellent  analysis  of  the  bird  faunas  of 
North  America.  His  methods  differed  from 
ours  in  that,  rather  than  treating  all  species 
simultaneously,  he  grouped  them  by  type  of 
distribution  pattern,  and  then  prepared 
maps  showing  numbers  of  species  geo- 
graphically, by  type  of  pattern.  By  this 
method  he  was  able  to  recognize  the  pres- 
ence of  17  primary  faunas  and  25  secondary 
ones.  The  methods  used,  while  different  in 
basic  respects  from  those  used  here,  could 
easily  prove  to  be  more  useful. 

The  following  should  be  added  to  our 
earlier  summary  of  coefficients  of  associa- 
tion (H  &  S:  131-132).  Smith  (1960)  used 
the  term  "Faunistic  Relation  Factor"  ( FRF ) 
for  the  Coefficient  of  Community,  and 
Huheey  ( 1965)  called  it  a  "Divergence  Fac- 
tor" ( D ) ,  when  subtracted  from  100.  Fager 
(1965)  has  devised  a  new  coefficient  in  the 
form  of  100  C/yJniUo  -  V2\/n2,  where  rii  is 
less  than  rin.  Long  ( 1963 )  gives  a  review  of 
coefficients  and  suggests  use  of  an  "average 
resemblance  formula"  first  used  by  Kulczn- 
ski  in  1927,  and  hsted  in  H  &  S,  p.  132. 

In  our  earlier  study  (H  &  S:  128-129,  148) 
we  pointed  out  that  our  work  has  been 
based  on  Webb's  ( 1950 )  analysis  of  the 
mammals  and  herpetofauna  of  Texas  and 
Oklahoma.  The  work  of  Ryan  ( 1963 )  who 
improved  on  Webb's  technique  in  analyz- 
ing the  mammal  faunas  of  Central  America 
was  not  known  to  us  at  the  time.  Subse- 
quently, Huheey  ( 1965 )  published  an  ac- 
count of  further  modifications  of  the  tech- 
nique in  the  study  of  the  herpetofauna  of 
Illinois.  Since  the  methods  used  in  all  of 
these  are  related,  and  because  they  are  sim- 
ilar in  principle,  their  comparison  may  be  of 


interest,  and  I  have  attempted  to  do  this 
briefly  in  the  account  following.  Webb's 
(1950)  method  was  to  lay  a  grid  of  sample 
points  at  100-mile  intervals  on  a  map  of  the 
area  to  be  studied,  to  prepare  a  species 
checklist  for  each  sample  point,  to  compute 
Coefficients  of  Community  between  sample 
points  and  then  plot  these,  to  draw  lines 
connecting  CCs  of  equal  value,  providing 
a  form  of  "contour  map,"  and  to  consider 
"valleys"  with  CCs  of  75%  or  more  as  "bio- 
geographic  regions."  A  key  point  underly- 
ing Webb's  analysis  lies  in  the  fact  that  he 
found  CCs  computed  in  a  north-south 
plane  to  differ  statistically  from  those  com- 
puted in  an  east-west  plane.  Since  he 
found  that  the  east-west  data  gave  most 
significant  results,  he  accepted  these  in  the 
preparation  of  his  final  map  and  rejected 
the  north-south  data.  Webb  deserves  com- 
mendation for  being  first,  to  my  knowledge, 
to  devise  a  numerical  technique  for  biogeo- 
graphic  analyses  in  two  dimensions. 

Ryan's  ( 1963 )  analysis  used  a  methodol- 
ogy only  slightly  different  from  that  of 
Webb.  Because  of  the  unusual  shape  of 
the  area  studied,  the  grid  of  one  portion  of 
it  was  made  up  of  points  100  kilometers 
( about  62  miles )  to  a  side,  of  a  second  por- 
tion of  it,  50  kilometers  ( about  31  miles )  to 
a  side.  CCs,  called  "Similarity  Values"  by 
both  Webb  and  Ryan,  were  calculated  for 
both  the  north-south  and  east-west  planes, 
and  both  sets  of  data  were  used  in  prepara- 
tion of  the  final  contour  maps,  so  far  as  I 
can  determine.  Ryan  called  the  contour 
lines  "isobiots."  It  is  not  clear  whether 
Webb's  75%  rule  for  biogeographic  regions 
was  used. 

Huheey's  ( 1965 )  method  differed  to  some 
degree  from  the  preceding.  It  was  to  lay  a 
grid  of  20  miles  to  a  side  onto  the  area  to 
be  studied.  Within  each  block  of  the  grid  a 
species  checklist  was  prepared.  For  each  of 
the  four  sides  of  all  blocks,  a  Divergence 
Factor  ( D )  was  computed,  where  D  = 
100-CC;  thus  D  is  the  complement  of  the 
Coefficient  of  Community.  Huheey  refers 
to  the  CC  by  Smith's  ( 1960)  term,  "Faunis- 
tic Relation  Factor,"  or  FRF.   The  average 


579 


DISTRIBUTION  OF  NORTH  AMERICAN  MAMMALS 


297 


of  the  four  Ds  for  each  block  was  computed, 
this  being  the  mean  D  for  that  block.  Fin- 
ally, contour  lines  called  "isometabases" 
were  drawn  around  mean  Ds  of  equal  value. 
From  the  contour  map  herpetofaunal  re- 
gions were  described. 

Webb's  and  Ryan's  methods,  it  will  be 
observed,  are  essentially  the  same,  differing 
only  in  distance  between  sample  points  and 
planes  in  which  CCs  are  computed.  Hu- 
heey's  method,  and  the  method  used  in  this 
and  in  our  earlier  study  differ  considerably, 
though  they  seek  identical  ends  through 
development  of  contour  maps  depicting 
faunistic  change.  I  have  been  led  to  under- 
stand that  still  other  techniques  and  refine- 
ments of  those  discussed  here  are  in  prepa- 
ration. For  example,  Valentine  (1965)  re- 
ported a  study  of  the  distribution  of  north- 
eastern Pacific  molluscan  distributions  us- 
ing methods  similar  to  those  employed  in 
this  and  in  our  earlier  paper.  It  is  apparent 
that  there  is  need  for  a  comparative  testing 
of  the  several  methods  of  analysis  presently 
at  hand,  using  the  same  basic  materials  in 
each.  I  plan  to  attempt  such  a  study. 

Earlier  (H  &  S:  129),  we  mentioned  a 
partial  testing  of  Webb's  original  method 
on  the  mammal  fauna  of  North  America. 
In  view  of  the  preceding,  a  brief  account  of 
the  testing  follows:  Webb's  method  was 
followed  exactly,  except  that  the  grid  of 
sample  points  was  placed  on  a  northeast- 
southwest  plane,  giving  better  coverage  of 
certain  coastal  areas.  A  number  of  varia- 
tions in  the  planes  in  which  CCs  were  com- 
puted were  attempted.  These  variations 
included:  (1)  computing  and  plotting  CCs 
in  the  northeast-southwest  plane  only;  (2) 
doing  the  same  in  the  northwest-southeast 
plane  only;  (3)  averaging  adjacent  CCs 
taken  in  both  planes  and  plotting  these;  (4) 
plotting  highest  CCs  only  of  pairs  computed 
in  both  planes.  We  did  not  try  Ryan's 
device  of  plotting  all  CCs  taken  in  both 
planes.  However,  of  the  variants  tested, 
none  gave  results  that  appeared  anywhere 
near  reasonable  in  terms  of  what  we  knew 
generally  of  the  distribution  of  biogeo- 
graphic  and  ecologic  zones.    The  variants 


used  by  Ryan  and  Huheey,  however,  ap- 
pear to  work  well  on  the  basis  of  their 
evidence,  and  my  conclusions  apply  in  no 
way  to  their  results. 

No  attempt  has  been  made  to  take  into 
account  the  effects  of  altitude  on  mammal 
distributions.  Dice,  in  his  original  study  of 
biotic  provinces  (1943)  described  such  ef- 
fects in  terms  of  "life  belts"  and  named  a 
number  of  these.  Kendeigh  ( 1954 )  on  the 
other  hand  did  not  see  altitude  as  a  con- 
founding factor  in  delimitation  of  biotic 
provinces.  He  wrote:  "A  mountain  range 
may  have  several  life  zones  represented  on 
it,  but  only  a  single  biotic  province,  pro- 
vided there  is  a  similar  tendency  for  specific 
or  subspecific  distinctiveness  of  the  fauna 
in  all  the  zones.  The  two  concepts  there- 
fore have  quite  different  objectives." 

I  have  not  been  able  to  decide  which  of 
the  two  views  applies  in  studies  of  the  sort 
carried  out  here.  It  should  be  realized,  how- 
ever, that  the  methods  employed  here  are 
capable  of  analyzing  the  effects  of  altitude 
on  distribution,  and  segregating  altitudinal 
provinces,  if  they  exist,  given  distribution 
maps  of  sufficient  accuracy  in  the  first 
place.  The  maps  used  here  failed  to  show 
details  of  vertical  distribution,  and  as  a 
consequence  this  aspect  of  the  problem  has 
not  proven  solvable. 

An  attempt  was  made  to  analyze  altitud- 
inal distribution  in  a  different  way.  Each 
species  of  mammal  was  given  its  life  zone 
distribution,  this  infonnation  being  collated 
from  a  large  number  of  sources,  chiefly 
certain  of  the  North  American  Fauna  Series. 
The  faunas  of  each  of  the  life  zones  within 
provinces  occurring  in  generally  mountain- 
ous parts  of  the  continent  were  treated  as 
primary  areas.  Coefficients  of  Community 
were  computed,  and  the  results  subjected  to 
cluster  analysis.  The  initial  results  were  un- 
satisfactory, however,  and  because  of  this 
and  because  of  the  circularity  of  reasoning 
involved,  the  method  was  abandoned. 

No  attempt  has  been  made  to  relate  the 
distribution  of  mammal  areas  to  the  distri- 
bution of  other  natural  units,  either  physio- 
graphic, climatic,  or  vegetational,  although 


580 


298 


SYSTEMATIC  ZOOLOGY 


a  comparison  of  Figure  3  to  maps  showing 
the  distribution  of  such  features  (e.g., 
Lobeck,  1948;  Thomethwaite,  1948;  Rowe, 
1959;  Shantz  and  Zon,  1923),  shows  that  the 
relationship  is  very  close. 

Summary 

1.  An  earlier  study  demonstrated  that 
range  limits  of  North  American  terrestrial 
mammals  were  grouped,  and  that  regions  of 
faunistic  homogeneity  could  as  a  conse- 
quence be  identified. 

2.  The  method  used  to  identify  such 
regions  was  to  compute  percentage  of  spe- 
cies whose  ranges  ended  in  blocks  fifty 
miles  on  a  side  (IFCs),  and  to  then  fit 
isarithms.  Topographic  "valleys"  in  the  map 
represented  regions  of  faunistic  homoge- 
neity, or  "primary  areas,"  and  for  24  of 
these,  species  checklists  were  prepared.  Tlie 
percentage  of  species  common  to  pairs  of 
primary  areas  (CCs)  were  computed,  and 
the  results  subjected  to  cluster  analysis,  us- 
ing the  method  of  weighted  pair-groups 
with  simple  averages.  This  resulted  in  a 
matrix  and  dendrogram  showing  relation- 
ships and  ordering  of  primary  areas.  Using 
a  conversion  of  Preston's  Resemblance 
Equation,  a  CC  of  62.5%  was  considered 
critical.  Primary  areas  with  a  CC  lower  than 
this  were  considered  "mammal  provinces." 
By  this  criterion,  22  mammal  provinces 
grouped  into  nine  superprovinces,  four  sub- 
regions,  and  one  region  were  recognized. 

3.  Many  more  primary  areas  should  have 
been  derived  from  the  IFC  map.  Starting 
with  86  primary  areas  and  carrying  out  four 
sequential  sets  of  cluster  analyses  leads  to 
the  conclusion  that  a  minimum  of  from  33 
to  35  mammal  provinces  occur  in  the  con- 
tinent. These  are  mapped,  named,  and 
briefly  described.  For  statistical  reasons, 
the  upper  limit  of  Preston's  critical  value  is 
raised  to  a  CC  of  65 7o. 

4.  Higher  categories  of  mammal  areas 
are  derived  by  grouping  the  provinces  on 
the  matrix  and  dendrogram  at  appropriate 
mean  CC  levels.  A  mean  CC  of  42.5%  gives 
13  superprovinces;  a  mean  CC  of  25%,  four 


subregions;  a  mean  CC  of  5%,  one  region 
(the  Nearctic).  These  are  mapped,  named, 
and  briefly  described.  In  general,  provinces 
are  named  as  adjectives  derived  from  geo- 
graphic place-names,  superprovinces  as 
nouns.  Where  possible  the  names  of  these 
and  of  regions  and  subregions  are  taken 
from  the  literature  on  a  priority  basis. 

5.  Approximately  one-quarter  of  the 
mammal  species  of  the  continent  also  occur 
on  nearby  continental  islands.  Island  faunas 
are  always  smaller  than  those  of  the  adja- 
cent mainland  and  always  show  closest 
faunistic  similarity  to  nearby  provinces. 

6.  The  methods  used  have  the  advantage 
of  being  relatively  objective,  repeatable, 
and  well-suited  to  computer  operations.  The 
use  of  a  successive  scanning  mode  micro- 
densitometer  may  prove  useful  in  the  prepa- 
ration of  accurate  IFC  maps. 

7.  Accounts  of  several  techniques  in  bio- 
geographic  analysis  similar  in  aim  and 
method  to  those  used  here  have  recently 
appeared.  These  are  briefly  compared. 
There  is  need  for  a  critical  testing  and 
evaluation  of  these  to  determine  which 
provides  the  best  basis  for  further  refine- 
ment. 

8.  While  the  methods  used  here  are  suit- 
able for  analyzing  the  effects  of  altitudinal 
zonation  on  distribution,  lack  of  requisite 
detail  in  the  distribution  maps  now  avail- 
able makes  such  analyses  impractical. 

9.  There  appears  to  be  a  high  degree  of 
correlation  between  the  distribution  of 
mammal  areas  and  other  kinds  of  natural 


areas. 


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