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HARVARD    UNIVERSITY 

Library  of  the 

Museum  of 

Comparative  Zoology 


SuL Latin  OF  TH 

Museum   of 

Comparative 

Zoology 


Studies  in  Organismic  and  Evolutionary 

Biology 
in  honor  of  A.  W.  Crompton 


MCZ 

LIBRARY 

FEB  2  2  2002 

Parish  A.  Jenkins,  Jr., 

l\/lichael  D.  Shapiro, 

f-^ARVARD 

and 

UNIVERSITY 

Tomasz  Owerkowicz 

Editors 

HARVARD  UNIVERSITY 

CAMBRIDGE,  MASSACHUSETTS,  U.S.A. 


VOLUME  156,  NUMBER  1 
10  OCTOBER  2001 


PUBLICATIONS  ISSUED 

OR  DISTRIBUTED  BY  THE 

MUSEUM  OF  COMPARATIVE  ZOOLOGY 

HARVARD  UNIVERSITY 


Breviora  1952- 

bulletin  1863- 

Memoirs  1865-1938 

JOHNSONiA,  Department  of  Mollusks,  1941-1974 

Occasional  Papers  on  Mollusks,  1945- 

SPECIAL  PUBLICATIONS. 

1.  Whittington,  H.  B.,  and  W.  D.  I.  Rolfe  (eds.),  1963  Phylogeny  and 
Evolution  of  Crustacea.  192  pp. 

2.  Turner,  R.  D.,  1966.  A  Survey  and  illustrated  Catalogue  of  the  Tere- 
dinidea  (Mollusca:  Bivalvia).  265  pp. 

3.  Sprinkle,  J.,  1973.  Morphology  and  Evolution  of  Blastozoan  Echino- 
derms.  284  pp. 

4.  Eaton,  R.  J.,  1974.  A  Flora  of  Concord  from  Thoreaus  Time  to  the 
Present  Day.  236  pp. 

5.  Rhodin,  A.  G.  J.,  and  K.  Miyata  (eds.),  1983.  Advances  in  Herpetology 
and  Evolutionary  Biology:  Essays  in  Honor  of  Ernest  E.  Williams. 

725  pp. 

6.  Angelo,  R.,  1990.  Concord  Area  Trees  and  Shrubs.  118  pp. 

Other  Publications. 

Bigelow,  H.  B.,  and  W.  C.  Schroeder,  1953.  Fishes  of  the  Gulf  of  Maine. 
Reprinted  1964. 

Brues,  C.T.,  A.  L.  Melander,  and  F.  M.  Carpenter,  1954.  Classification  of 
Insects.  (Bulletin  of  the  M.  C.  Z,  Vol.  108.)  Reprinted  1971. 

Creighton,  W.  S.,  1950.  The  Ants  of  North  America.  Reprinted  1966. 

Lyman,  C.  P.,  and  A.  R.  Dawe  (eds.),  1960.  Proceedings  of  the  First  In- 
ternational Symposium  on  Natural  Mammalian  Hibernation.  {Bulletin 
of  the  M.  C.  Z,  VoL  124.) 

Ornithological  Gazetteers  of  the  Neotropics  (1975-). 

Peters  Check-hst  of  Birds  of  the  World,  vols.  1-16. 

Proceedings  of  the  New  England  Zoological  Club  1899-1947.  (Complete 
sets  only.) 

Proceedings  of  the  Boston  Society  of  Natural  History. 

Price  list  and  catalog  of  MCZ  publications  may  be  obtained  from  Publica- 
tions Office,  Museum  of  Comparative  Zoology,  Harvard  University,  Cambridge, 
Massachusetts  02138,  U.S.A. 

This  publication  has  been  printed  on  acid-free  permanent  paper  stock. 

©The  President  and  Fellows  of  Harvard  College  2001. 


STUDIES  IN  ORGANISMIC  AND  EVOLUTIONARY  BIOLOGY  IN 
HONOR  OF  A.  W.  CROMPTON 

PARISH  A.  JENKINS,  JR.,  MICHAEL  D.  SHAPIRO,  AND  TOMASZ  OWERKOWICZ,  EDITORS 
CONTENTS 


Introduction  1 

A  Probainognathian  Cynodont  from  South 
Africa  and  the  Phylogeny  of 
NonmammaUan  Cynodonts.  By  James  A. 
Hopson  and  James  W.  Kitching 5 

On  Microconodon,  a  Late  Triassic  Cynodont 
from  the  Newark  Supergroup  of  Eastern 
North  America.  By  Hans-Dieter  Sues 37 

A  Cynodont  from  the  Upper  Triassic  of  East 
Greenland:  Tooth  Replacement  and 
Double-Rootedness.  By  Michael  D. 
Shapiro  and  Parish  A.  Jenkins,  Jr.  49 

On  Two  Advanced  Carnivorous  Cynodonts 
from  the  Late  Triassic  of  Southern  Brazil. 
By  Jose  F.  Bonaparte  and  Mario  Costa 
Barberena  59 

The  Inner  Ear  and  Its  Bony  Housing  in 
Tritylodontids  and  Implications  for 
Evolution  of  the  Mammalian  Ear.  By 
Zhexi  Luo  81 

A  New  Specimen  and  a  Functional 

Reassociation  of  the  Molar  Dentition  of 

Batodon  tenuis  (Placentalia,  Incertae 

Sedis),  Latest  Cretaceous  (Lancian),  North 

America.  By  Craig  B.  Wood  and  William 

A.  Clemens 99 

The  Evolution  of  Mammalian  Development. 

By  Kathleen  K.  Smith  119 

Sldn  Impressions  of  Triassic  Theropods  as 
Records  of  Foot  Movement.  By  Stephen 
M.  Gatesy 137 

A  Diminutive  Pterosaur  (Pterosauria: 
Eudimorphodontidae)  from  the 
Greenlandic  Triassic.  By  Farish  A.  Jenkins, 
Jr.,  Neil  H.  Shubin,  Stephen  M.  Gatesy, 
and  Kevin  Padian 151 


Immature  Rhizondontids  from  the  Devonian  of 
Nortli  America.  By  Marcus  C.  Davis,  NeU 
H.  Shubin,  and  E.  B.  Daeschler  171 

How  Do  Mysticetes  Remove  Prey  Trapped  in 

Baleen?  By  Alexander  J.  Werth  189 

Tongue-Jaw  Linkages:  The  Mechanisms  of 

Feeding  Revisited.  By  Karen  M.  Hiiemae 

and  Jeffrey  B.  Palmer  205 

Extrinsic  Versus  Intrinsic  Lingual  Muscles:  A 

False  Dichotomy?  By  Kurt  Schwenk  219 

Electromyographic  Pattern  of  the  Gular  Pump 
in  Monitor  Lizards.  By  Tomasz 
Owerkowicz,  Elizabeth  L.  Brainerd,  and 
David  R.  Carrier  237 

Synchronization  of  Electromyographic  Activity 
in  Oral  Musculature  During  Suckling  and 
Drinking.  By  A.  J.  Thexton  and  Rebecca 
Z.  German  249 

Sonomicrometry  and  Kinematic  Estimates  of 
the  Mechanical  Power  of  Bird  Flight.  By 
Douglas  R.  Warrick,  Bret  W.  Tobalske, 
Andrew  A.  Biewener,  and  Kenneth  P. 
Dial 257 

Trade-off  Between  Modeling  and  Remodeling 
Responses  to  Loading  in  the  Mammalian 
Limb.  By  Daniel  E.  Lieberman  and 
Osbjorn  M.  Pearson  269 

Muscle  Force  and  Stress  During  Running  in 
Dogs  and  Wild  Turkeys.  By  Thomas  J. 
Roberts 283 

Regulation  of  Skeletal  Muscle  Regeneration 
and  Bone  Repair  in  Vertebrates.  By  Uri 
Oron .-'..- 297 


Bull.  Mus.  Comp.  ZooL,  156(1):  i,  October,  2001         i 


STUDIES  IN  ORGANISMIC  AND  EVOLUTIONARY  BIOLOGY 
IN  HONOR  OF  A.  W.  CROMPTON 


Fuzz  Crompton 

INTRODUCTION  ly  eclectic  array  of  papers  spans  a  range  of 
In  grateful  tribute  to  Fuzz  Crompton,  subjects  and  approaches  that  constitute  a 
this  volume  presents  papers  delivered  at  a  challenge  to  any  conventionally  inclusive 
symposium  held  in  Fuzz's  honor  on  15  title.  And  yet  the  diversity  herein  is  rep- 
May  1999  at  the  Museum  of  Comparative  resentative  of  the  breadth  of  Fuzz's  inter- 
Zoology,  Harvard  University.  The  seeming-  ests,  the  scope  of  his  inspiration,  and  the 

Bull.  Mus.  Comp.  ZooL,  156(1):  1-3,  October,  2001         1 


2         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


extent  of  his  influence  in  both  teaching  electromyographic    data   from    living   sys- 

and  research.  Among  this  volumes  authors  tems    provided    the    essential    tools    wdth 

are  present  and  former  students  (and  stu-  which  to  interpret  the  evolutionary  history 

dents  of  former  students),  postdoctoral  fel-  and  transformations  embedded  in  fossils, 

lows,  colleagues,  and  collaborators,  all  of  From  his  work  our  understanding  of  the 

whom  gladly  joined  to  celebrate  his  man-  tribosphenic  dentition — that  once  fear- 

ifold  contributions  to  organismic  and  evo-  some  array  of  cusps,  crests,  cristi,  and  val- 

lutionary  biology.  Perhaps  the  only  aspect  leys — was  forever  transformed.  Tribos- 

of  these  proceedings  not  fully  conveyed  in  phenic  teeth,  no  longer  the  statuary  mark- 

these  published  papers  was  a  collegiality  at  ing  therian  beginnings,  became  but  one 

the  syinposium  that  spilled  over  into  the  expression  of  the  functional  continuum  in 

open  joviality  of  a  reunion,  an  enthusiasm  synapsid    evolution.    Not    content   with 

for  science,  and  a  delight  in  professional  odontology  explained.  Fuzz's  studies  with 

friendships  that  all  derive  from  the  man  his  students  and  collaborators  became  ever 

we  honored.  more    complex    orchestrations    of  experi- 

Launching  a  career  remarkable  for  ac-  mental  apparatus  as  he  elucidated  the  in- 
complishment.  Fuzz's  publication  record  terrelationships  of  jaw  and  tongue  move- 
began  with  a  paper  that  appeared  in  Acta  ments,  the  patterns  of  chewing  and  the 
Zoologica  in  1953,  "The  development  of  mechanics  of  jaws,  the  millisecond  events 
the  chondrocranium  of  Spheniscus  demer-  of  swallov^ng,  and  the  neurobiology  of 
sus  with  special  reference  to  the  columella  that  most  primal  of  mammalian  feeding 
auris  of  birds,"  a  product  of  his  graduate  patterns,  suckling.  Marsupials,  primates, 
work  at  Stellenbosch  University.  But  it  was  insectivores,  pigs,  and  goats  were  among 
with  a  second  doctorate,  completed  in  a  his  subjects,  but  in  each  case  the  real  sub- 
stunningly  short  two  years  and  under  the  ject  was  integrative  biology,  with  results 
guidance  of  Francis  Rex  Parrington,  FRS,  that  were  invariably  exemplary.  This  inte- 
at  Cambridge  University,  that  he  redirect-  grative  approach  was  especially  empha- 
ed  his  investigations  into  vertebrate  pale-  sized  in  Biology  21,  Structure  and  Physi- 
ontology,  and  specifically  into  the  mor-  ology  of  the  Vertebrates,  a  course  offered 
phology  and  relationships  of  mammallike  by  Fuzz  and  the  late  Dick  Taylor  for  al- 
reptiles,  and  eventually  into  the  origins  of  most  three  decades.  At  the  top  of  the  scale 
mammals.  A  series  of  classic,  oft-cited  pa-  in  terms  of  the  required  workload,  the  ex- 
pers  over  the  next  two  decades  made  ma-  perience  was  consistently  and  enthusiasti- 
jor  advances  in  our  understanding  of  the  cally  rated  by  students  as  providing  the 
intricacies  of  dental  and  cranial  evolution  highest  of  intellectual  returns,  and  a 
among  synapsids  of  the  Mesozoic.  source  of  genuine  enjoyment. 

Fuzz's  early  interests  in  the  tangible  re-  Unless    we    aspire    to    monographic 

cord  of  vertebrate  evolution  soon  expand-  lengths,  we  cannot  adequately  recount  by 

ed  into  what  is  now  generally  known  as  way  of  gratitude  all  of  Fuzz  Crompton's 

functional  morphology — understanding  contributions    to    science,    teaching,    and 

the  mechanics  and  other  functional  inte-  promoting  the  careers  of  others.  And  yet 

grations  of  structural  features.   In  a  fun-  there  is  one  contribution,  distinctively  in- 

damental   sense,   as   he   himself  so   often  tegrative,  that  must  appear  in  this  perma- 

said,    he    wanted    to    know   how    animals  nent  record  of  die  Museum  of  Compara- 

worked.  Although  precedents  for  such  an  tive  Zoology  if  we  are  to  salute  him  at  all. 

approach  had  previously  been  established  During  his  career,  which  began  as  Curator 

in  vertebrate  paleontology,  it  was  Fuzz's  of  Palaeontology  Collections   in   the   Na- 

signal  contribution  that  he  placed  his  anal-  tional  Museum  in  Bloemfontein,  South  Af- 

yses  in  the  context  of  experimental  work  rica.  Fuzz  served  as  Director  of  three  ma- 

on  extant  animals.   Cineradiographic  and  jor  museums:  first  at  The  South  African 


Introduction  'Jenkins  et  al. 


Museum,  then  at  Yale's  Peabody  Museum 
of  Natural  History,  and  finally  at  the  Mu- 
seum of  Comparative  Zoology.  During  the 
course  of  this  extensive  experience  he  orig- 
inated the  concept  of  Professor/Curator  in 
face  of  the  long-standing  belief,  reinforced 
by  practice,  that  these  were  separate  spe- 
cies with  different  territories.  On  the  pre- 
mise that  natural  history  museums  ought 
not  to  be  simply  repositories,  but  are  jus- 
tifiable to  the  extent  that  they  promote  re- 
search and  knowledge  of  our  natural 
world,  the  conclusion  is  inescapable  that 
senior  museum  staff  must  be,  first  and 
foremost,  scientists  of  distinction.  In  a  uni- 
versity setting,  as  a  consequence,  positions 
supported  by  museum  resources  inust  be 
professorial,  with  standards  and  expecta- 
tions no  less  than  those  held  for  every  fac- 
ulty appointment.  No  longer  would  cura- 


tors exist  as  another  class  of  citizenry  apart 
from  academic  departments.  Rather,  pro- 
fessors with  adininistrative  appointments 
as  curators  would  continue  to  ensure  the 
museums  growth  and  participation  in  ac- 
ademic research  and  instruction.  The  con- 
cepts of  Professor  and  Curator,  once  a  du- 
ality, became  inseparably  integrated.  At 
Harvard,  this  legacy  froin  Fuzz  Cromp- 
ton's  visionary  directorship  persists  today, 
to  the  intellectual  enhancement  of  the 
MuseuiTj  of  Comparative  Zoology,  the  De- 
partment of  Organisinic  and  Evolutionary 
Biology,  and  the  University. 

Parish  A.  Jenkins,  Jr. 
Michael  D.  Shapiro 
Tomasz  Owerkowicz 

Cambridge,  Massachusetts 
10  April  2001 


Symposium  participants,  1 5  May  1 999.  From  left  to  right,  front  row:  Parish  Jenkins,  Jose  Bonaparte,  Neil  Shubin,  Kathleen  Smith, 
Fuzz  Crompton,  Ken  Dial,  Nick  Hotton.  Second  row:  Jim  Hopson,  Christine  Janis,  Craig  Wood,  Zhexi  Luo,  Rebecca  German, 
Allan  Thexton,  Tomasz  Owerkowicz.  Third  row:  Steve  Gatesy,  Dan  Lieberman,  Kurt  Schwenk,  Alex  Werth,  Beth  Brainerd.  Fourth 
row:  Uri  Oron,  Mike  Shapiro,  Tom  Roberts,  Andy  Biewener  (photograph  by  Leon  Claessens). 


A  PROBAINOGNATHIAN  CYNODONT  FROM  SOUTH  AFRICA  AND 
THE  PHYLOGENY  OF  NONMAMMALIAN  CYNODONTS 


JAMES  A.  HOPSON^  AND  JAMES  W.  KITCHING^ 

Abstract,  a  new  small  cynodont  from  subzone  B 
of  the  Cynognathus  Assemblage  Zone  (earliest  Mid- 
dle Triassic)  of  South  Africa  is  described  as  Lumkuia 
ftizzi.  It  is  represented  by  a  nearly  complete  skull  and 
lower  jaw,  a  shoulder  girdle  and  forelimb,  and  artic- 
ulated dorsal  and  caudal  vertebrae.  It  is  placed  in  the 
eucynodont  clade  Probainognathia  on  the  basis  of 
four  unequivocal  synapomorphies,  including  absence 
of  a  parietal  foramen  and  expanded  plates  on  the  ribs 
and  a  secondary  palate  extending  posteriorly  to  the 
level  of  the  orbit.  Lumkuia  is  the  oldest  and  most 
primitive  probainognathian  represented  by  adequate 
material.  A  cladistic  analysis  strongly  supports  the 
monophyly  of  Cynodontia,  Epicynodontia  (a  new  tax- 
on  including  Galesaurus,  Thrinaxodon,  and  eucyno- 
donts),  and  Eucvnodontia.  The  analysis  also  supports 
the  eucynodont  clades  Probainognathia  and  Cynog- 
nathia,  and  Gomphodontia  as  a  subgroup  of  the  latter. 
Within  Probainognathia,  a  chiniquodontid  clade  and 
a  tritheledontid  +  mammaliaform  clade  are  well  sup- 
ported. Probainognathus  is  sister  to  the  latter  clade, 
but  this  node  breaks  down  in  trees  two  steps  longer 
than  the  shortest  tree.  Tritylodontids  are  deeply  nest- 
ed within  the  traversodont  gomphodonts,  with  "Sca- 
lenodon"  hirschoni  weakly  supported  as  their  sister 
taxon. 

INTRODUCTION 

The  Eucynodontia  (Kemp,  1982,  1988), 
that  is,  those  cynodonts  more  derived  than 
the  basal  Triassic  Thrinaxodon,  have  tra- 
ditionally been  divided  into  a  carnivorous 
line  leading  to  maminals  and  a  herbivo- 
rous, or  gomphodont,  line  leading  to  the 
Jurassic  tritylodontids  (Crompton  and  El- 
lenberger,  1957;  Crompton,  1972b;  Hop- 
son  and  Kitching,  1972;  Sues,  1985;  Hop- 
son  and  Barghusen,  1986;  Hopson,  1991b, 
1994).  However,  Kemp  (1982,  1983,  1988) 


'  Department  of  Organismal  Biology  and  Anatomy, 
University  of  Chicago,  1027  East  57th  Street,  Chi- 
cago, Illinois  60637. 

'  Bernard  Price  Institute  for  Palaeontological  Re- 
search, University  of  the  Witwatersrand,  Johannes- 
burg, South  Africa. 


noted  that  tritylodontids  and  mammals 
share  many  derived  features  that  are  ab- 
sent in  Triassic  cynodonts,  which  led  him 
to  suggest  that  tritylodontids  should  be 
separated  from  the  herbivorous  cynodonts 
and  placed  in  the  carnivorous  line  close  to 
Mammalia;  the  herbivorous  specializations 
of  tritylodontids  thus  would  be  convergent 
on  those  of  gomphodonts.  Rowe  (1986, 
1988,  1993)  went  still  further  in  obliter- 
ating the  distinction  between  the  carnivo- 
rous and  herbivorous  lineages  by  inter- 
leaving Middle  Triassic  to  Early  Jurassic 
cynodonts  in  a  paraphyletic  series  of  car- 
nivorous and  gomphodont  taxa  that  lead  to 
a  terminal  clade  Mammaliamorpha,  con- 
taining tritylodontids  and  traditionally  de- 
fined mammals  (termed  Mammaliaformes 
by  Rowe).  The  sister-group  relationship  of 
Tritylodontidae  and  Mammaliaformes  has 
become  widely  accepted  (Wible,  1991;  Lu- 
cas and  Luo,  1993;  Martinez  et  al,  1996), 
although  Sues  (1985)  and  Hopson  (1991b, 
1994)  have  argued  against  it. 

The  senior  author  (Hopson,  1990, 
1991a,b,  1994)  has  summarized  the  results 
of  his  cladistic  analyses  of  cynodont  rela- 
tionships, although,  to  date,  has  not  pub- 
lished the  data  on  which  they  are  based. 
Hopson  recognizes  a  primarily  herbivo- 
rous clade  that  includes  tritylodontids,  the 
Cynognathia  of  Hopson  and  Barghusen 
(1986),  and  a  carnivorous  clade  that  in- 
cludes mammals,  which  has  been  desig- 
nated Probainognathia  (Hopson,  1990).  A 
data  matrix  of  synapsids  as  a  whole  was 
pubhshed  by  Sidor  and  Hopson  (1998), 
but  it  lacks  critical  taxa  and  characters  for 


Bull.  Mus.  Comp.  ZooL,  156(1):  5-35,  October,  2001         5 


6         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


resolving  lower-level  relationships  within 
nonmammalian  cynodonts. 

In  May,  1988,  while  studying  in  the  Ka- 
roo fossil  collection  of  the  Bernard  Price 
Institute  for  Palaeontological  Research 
(BPI)  at  the  University  of  the  Witwaters- 
rand,  Hopson  noted  a  small  skull  and  par- 
tial skeleton  (BP/1/2669)  from  the  Cynog- 
nathus  Assemblage  Zone.  The  specimen 
was  identified  in  the  catalog  as  a  juvenile 
Trirachodon,  but  its  skull  morphology 
more  closely  reseinbled  that  of  Prohain- 
ognathus  and  the  Chiniquodontidae,  car- 
nivorous eucynodonts  best  known  from 
the  Middle  and  Late  Triassic  of  South 
America.  A  notice  of  the  specimen,  with 
preliminary  conclusions  on  its  phylogenet- 
ic  significance,  was  presented  at  the  48th 
annual  meeting  of  the  Society  of  Verte- 
brate Paleontology  (Hopson  and  Kitching, 
1988). 

This  new  cynodont  is  named  and  briefly 
described  here.  It  is  compared  with  Thri- 
naxodon,  as  a  member  of  a  more  primitive 
cynodont  grade;  with  Prohainognathus  and 
chiniquodontids,  as  members  of  the  Pro- 
bainognathia;  and  with  Cijnognathus  and 
early  gomphodont  genera,  as  members  of 
the  Cynognathia.  One  purpose  of  this  pa- 
per is  to  justify  the  establishment  of  the 
eucynodont  clades  Cynognathia  (sensu 
Hopson  and  Barghusen,  1986)  and  Pro- 
bainognathia  {sensu  Hopson,  1990,  1991a, 
1994). 

MATERIALS  AND  METHODS 

Specimen  BP/1/2669  had  been  partially 
prepared  at  the  BPI  so  that  portions  of  the 
skeleton  were  exposed  on  both  sides  of  a 
small  sandstone  slab.  The  skull  and  lower 
jaws  were  subsequently  removed  from  the 
slab  and  more  fully  prepared  by  Ms.  Claire 
Vanderslice.  Although  portions  of  the  ex- 
ternal surface  of  the  skull  are  damaged, 
the  palate,  braincase,  and  medial  surface 
of  the  lower  jaw  are  beautifully  preserved. 
Because  the  postcranial  elements  are,  for 
the  most  part,  heavily  eroded,  they  have 
been  further  prepared  only  slightly. 

Comparisons  with  other  cynodonts  are 


based  on  specimens,  stereophotographs, 
notes  and  drawings,  and  published  ac- 
counts. The  data  matrix  of  cynodonts  in- 
cludes characters  published  by  Sidor  and 
Hopson  (1998),  with  many  new  characters 
added,  particularly  from  the  dentition.  The 
matrix  was  analyzed  using  the  3.1  version 
of  PAUP  (Swofford,  1993).  In  the  follow- 
ing section,  phylogenetic  definitions  of  a 
number  of  suprageneric  taxa  are  given, 
with  a  distinction  made  between  node- 
based  and  stem-based  definitions,  as  rec- 
ommended by  Sereno  (1999). 

SYSTEMATIC  PALEONTOLOGY 
Therapsida  Broom,  1905 

Cynodontia  Owen,  1861 

Definition.  The  most  inclusive  clade  in- 
cluding Mammalia  and  excluding  Bauria. 
This  clade  and  its  sister  group,  the  Ther- 
ocephalia  (defined  as  the  most  inclusive 
clade  including  Bauria  and  excluding 
Mammalia),  are  stem-based  members  of  a 
node-based  Eutheriodontia  (defined  as  the 
least  inclusive  clade  including  Mammalia 
and  Bauria).  (See  Sereno  [1999]  for  dis- 
cussion of  node-stem  triplets.) 

Epicynodontia  new  taxon 

Definition.  The  most  inclusive  clade  in- 
cluding Mammalia  and  excluding  Procy- 
nosuchus.  This  clade  includes,  among  oth- 
ers, Galesaurus,  Thrinaxodon,  and  eucy- 
nodonts. 

Eucynodontia  Kemp,  1982 

Definition.  The  least  inclusive  clade  in- 
cluding Mammalia  and  Exaeretodon.  This 
is  a  node-based  taxon,  with  two  stem- 
based  subgroups:  Cynognathia  (defined  as 
the  most  inclusive  clade  including  Exaer- 
etodon and  excluding  Prohainognathus) 
and  Probainognathia  (defined  below). 
Within  Cynognathia  is  a  major  stem-based 
subgroup,  the  Gomphodontia  (defined  as 
the  most  inclusive  clade  including  Exaer- 
etodon and  excluding  Cynognathus). 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching        7 


Probainognathia  Hopson,  1 990  orbital  wall  only  to  the  level  of  the  lacrimal 

Definition.  The  most  inclusive  clade  in-  ^ramina  and  an  orbital  process  of  the  pal- 

cluding    Probainognathus    and    excluding  ^^"^^  ^^  ^^^^^^g-  ^^  }^  "^°^^,  primitive  than 

Exaeretodon.  other  eucynodonts  m  that  the  dentaiy  does 

not  extend  as  tar  posteriorly,  resulting  in  a 

Family  LUMKUIIDAE  new  family  longer  dorsal  exposure  of  the  surangular 

between  the  rear  of  the  dentary  and  the 

Definition.  The  most  inclusive  clade  in-  articular.  At  the  rear  of  primary  palate  is 

eluding  Lumkuia   and   excluding  Ecteni-  ^n  autapomorphic  feature:  the  pterygoids 

^^^on.  form   a  deep   median  depression  with  a 

,        ,    .     ,       .                             .           .  nearly   vertical    posterior   wall,    behind 

Livm/cty/a  ftvzz/ new  genus  and  species  u-  u  4-u      r                          i.       j-     u 

^                      ^  wiiicfi  tJiey  lorm  a  prominent  median  boss 

Etymology.   The  generic  name  is  from  anterior  to  the  interpterygoidal  vacuities, 

the  Lumku  Mission,  near  which  the  spec-  The  presence  of  interpterygoidal  vacuities 

imen  was  found.  The  species  name  is  in  suggests  that  the  type  specimen  may  be  a 

honor  of  A.  W.  "Fuzz"  Crompton,  in  rec-  subadult  individual, 
ognition  of  his  distinguished  career  as  a 

student  of  cynodonts  and  early  mammals.  DESCRIPTION 

Holotype.    BP/1/2669,   partial   skeleton,  Qy,,A\ 
including  skull  with  lower  jaws;  left  sca- 

pulocoracoid  and  clavicle,  interclavicle,  In  dorsal  view  (Fig.  1),  the  general  ap- 

and  proximal  part  of  right  clavicle;  most  of  pearance  of  the  skull  o^  Lumkuia  is  similar 

left  forelimb;  and  two  articulated  segments  to  that  of  Thrinaxodon,  although  the  pre- 

of  the  axial  skeleton;  the  latter  consist  of  orbital  region  is  shorter  and  the  temporal 

10   dorsal  vertebrae  with   associated  ribs  fossa  longer.  Thus,  the  center  of  the  orbits 

and  eight  caudal  vertebrae.  lies   anterior  to  the   middle  of  the  skull. 

Horizon  and  Locality.  The  specimen  is  whereas    in    Thrinaxodon    the    orbits    are 

from  the  Burgersdorp  Formation,  in  sub-  centered  exactly  at  midlength.  The  ptery- 

zone  B  of  the  Cynognathus  Assemblage  goid  flanges,  which  in  Thrinaxodon  lie  be- 

Zone.    It   was    collected   by   Father   Paul  low  the  middle  of  the  orbits,  are  visible  in 

Reubsamen  in  the  vicinity  of  the  Lumku  Lumkuia   behind   the   postorbital  bar  (as 

Catholic  Mission,  near  the  town  of  Lady  they  commonly  are  in  eucynodonts).  As  in 

Frere,  Eastern  Cape  Province,  South  Af-  Thrinaxodon,  the  sagittal  crest  terminates 

rica.  above   the   occiput,    so   that  the   occipital 

Age.  The  Cynognathus  Assemblage  condyles  are  visible  from  above.  This  con- 
Zone  in  the  region  of  Lady  Frere  is  rep-  trasts  with  Ecteninion  and  Probainogna- 
resented  by  subzone  B  of  Hancox  et  al.  thus  (although  not  chiniquodontids),  in 
(1995;  B.  S.  Rubidge,  personal  communi-  which  the  sagittal  crest  overhangs  the  oc- 
cation),  which  is  considered  to  be  of  early  ciput  and  covers  the  condyles.  The  lamb- 
Middle  Triassic  (Anisian)  age  (Hancox  and  doidal  crests  in  Lumkuia,  as  in  Thrinaxo- 
Rubidge,  1997).  don,   diverge  at  greater  than  90  degrees 

Diagnosis.   Lumkuia  fiizzi  is  character-  and  extend  posteriorly  at  their  outer  ends 

ized  by  a  unique  combination  of  primitive  only  a  short  distance  beyond  the  occipital 

and  derived  features.  It  possesses  the  fol-  condyles.  In  Probelesodon  and  Chiniquo- 

lowing  probainognathian  features:  parietal  don,  and  in  gomphodonts,  the  sagittal  crest 

foramen  absent;  rear  of  secondary  palate  terminates  slightly  in  front  of  the  condyles 

lies   below   anterior   border   of  orbit;   ex-  but  the  lambdoidal  crests   diverge  at  an 

panded  plates  on  ribs  absent.  It  is  more  acute  angle  and  extend  back  well  beyond 

primitive  than  other  probainognathians  in  the  condyles.  The  zygomatic  arches  of  Lw- 

that  the  frontal  extends  down  the  medial  mkuia  are  more  flared  and  rounded  in  pro- 


8         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


^m> 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching        9 


Figure  1.  Skull  of  Lumkuia  fuzzi  (BP/1/2669)  in  dorsal  view  (on  left  enlarged  x3).  Scale  bar  =  10  mm.  Abbreviations;  e, 
epipterygoid;  eo,  exoccipital;  f,  frontal;  fic,  foramen  of  lacrimal  canal;  j,  jugal;  I,  lacrimal;  mx,  maxilla;  n,  nasal;  op,  opisthotic;  p, 
parietal;  pi,  palatine;  pm,  premaxilla;  po,  postorbital;  pp,  postparietal;  pr,  prootic;  prf,  prefrontal;  pt,  pterygoid;  ptpf,  pterygopar- 
occipital  foramen;  q,  quadrate;  qj,  quadratojugal;  sm,  septomaxilla;  sq,  squamosal;  V^j,  trigeminal  foramen. 


10         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching 


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12         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching        13 


Figure  3.  Skull  of  Lumkuia  fuzzi  (BP/1/2669)  in  ventral  view  (on  left  enlarged  x3).  Scale  bar  =  10  mm.  Abbreviations:  a, 
angular;  ar,  articular;  bo,  basioccipital;  d,  dentary;  e,  epipterygoid;  eo,  exoccipital;  hf,  hypoglossal  foramina;  ic,  internal  carotid 
foramina;  iptv,  interpterygoidal  vacuity;  j,  jugal;  jf,  jugular  foramen;  Ifpr,  lateral  flange  of  prootic;  mpf,  major  palatine  foramen;  mx, 
maxilla;  op,  opisthotic;  pa,  pila  antotica;  pi,  palatine;  pm,  premaxilla;  pr,  prootic;  pra,  prearticular;  ps,  parasphienoid;  pt,  pterygoid; 
ptb,  pterygoid  boss;  ptpf,  pterygoparoccipital  foramen;  q,  quadrate;  qj,  quadratojugal;  qre,  quadrate  ramus  of  epipterygoid;  ref 
lam,  reflected  lamina;  rps,  parasphenoid  rostrum;  s,  stapes;  sa,  surangular;  sp,  splenial;  sq,  squamosal;  t,  tabular;  v,  vomer. 


14         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


file  than  those  of  Thrinaxodon,  being  wid-  described  below,  with  only  salient  features 
est  anterior  to,  rather  than  at,  the  level  of  noted.  The  facial  portions  of  the  premax- 
the  jaw  joint;  in  this  Lumkuia  resembles  ilia  and  septomaxilla  are  missing.  On  the 
other  Triassic  probainognathians  and  dif-  palate,  backwardly  pointing  processes  of 
fers  from  cynognathians.  the  premaxillae  separate  the  elongate,  slit- 
In  lateral  view  (Fig.  2),  the  skull  and  like,  incisive  foramina.  The  premaxilla 
lower  jaw  of  Lumkuia  appear  to  be  more  forms  all  but  the  posteriormost  parts  of  the 
robust  than  in  Thrinaxodon  (Fig.  5A),  due  lateral  border  of  the  incisive  foramen  and 
to  the  shorter  snout,  longer  temporal  re-  the  fossa  for  the  lower  canine, 
gion,  and  deeper  dentary.  Also,  as  in  other  The  alveolar  border  of  the  maxilla  is 
eucynodonts  except  Ctjnognathus  (Fig.  straight,  turning  up  slightly  at  the  level  of 
6A),  the  jaw  joint  is  located  more  anteri-  the  last  tooth  and  passing  smoothly  into 
orly,  so  that  the  lambdoidal  crests  extend  the  suborbital  bar  where,  a  short  distance 
well  behind  the  articular  region.  The  ca-  behind  the  last  postcanine,  it  contacts  the 
nines  are  more  robust  and  the  posterior  jugal.  In  the  palate,  the  maxilla  contributes 
cheek  teeth  proportionately  larger  than  in  to  the  rear  margin  of  the  incisive  foramen 
Thrinaxodon  and  Probainognathus  (Fig.  and  the  posteriormost  part  of  the  lower  ca- 
5C),  although  not  in  Ecteninion  and  chi-  nine  fossa.  The  maxilla  forms  the  anterior 
niquodontids.  The  zygomatic  arch  appears  two  thirds  of  the  secondary  palate,  extend- 
to  be  no  more  robust  than  that  of  ThH-  ing  as  far  back  as  the  gap  between  the 
naxodon,  except  perhaps  posteriorly,  third  and  fourth  postcanines.  The  inajor 
whereas  that  of  Probainognathus,  and  es-  palatine  foramen  opens  anteroventrally  on 
pecially  of  chiniquodontids  and  cynogna-  the  maxillary— palatine  suture  well  lateral 
thians,  is  much  deeper.  to  the  midline. 

In  ventral  view  (Fig.  3),  the  symphyseal  The  nasals  have  largely  flaked  off,  leav- 

region  is  shorter  than  that  of  Thrinaxodon  ing   some   bone   only  posterolaterally   As 

and  the  shorter  jaws  diverge  at  a  greater  shown  by  impressions  on  the  surface  of 

angle.  The  secondary  palate  is  only  slightly  the  frontals,  the  nasals  overlap  the  frontals 

inore    developed,    with    a   nearly   straight  and  the  nasofrontal  suture  lies  a  short  dis- 

rather  than  concave  posterior  margin.  Be-  tance  behind  the  anterior  border  of  the  or- 

hind  the  pterygoid  flanges,  the  basicranial  bit. 

axis  is  more  transversely  compressed  than  The  eroded  dorsal  surface  of  the  fron- 
in  Thrinaxodon,  so  that  the  subtemporal  tals  preserves  a  slightly  undulating  midline 
fossa  is  proportionately  wider.  suture.  The  contact  with  the  parietals  on 
In  occipital  view  (Fig.  4),  the  most  dis-  the  skull  roof  is  not  preserved,  but  prob- 
tinctive  difference  from  Thrinaxodon  is  in  ably  lay  between  the  posteriormost  part  of 
the  constriction  of  the  base  of  the  zygo-  the  temporal  crests  of  the  postorbitals.  In 
matic  arch  and  the  separation  of  the  zy-  the  medial  wall  of  the  orbit,  a  thin  strip  of 
goma  from  the  more  flaring  lambdoidal  frontal  is  exposed  behind  the  large  de- 
crest  by  a  V-shaped  notch.  In  noneucyno-  scending  flange  of  prefrontal,  extending 
donts,  such  as  Procynosuchus,  Galesaurus,  ventrally  about  to  the  level  of  the  lacrimal 
and  Thrinaxodon,  the  lambdoidal  crest  is  foramina. 

continuous  with  the  dorsal  ridge  on  the  zy-  Within  the  orbit,  the  prefrontal  overlies 
gomatic  arch.  Only  in  eucynodonts,  with  the  frontal  and  is  itself  overlain  by  the  lac- 
the  exception  of  Cynognathus,  is  there  a  rimal;  it  extends  ventrally  nearly  to  the  lev- 
distinct  break  between  the  two  crests,  with  el  of  the  palatine  on  the  dorsal  surface  of 
the  lambdoidal  crest  passing  back  poste-  the  palate. 

rior  to  the  medial  end  of  the  dorsal  zygo-  The  lacrimal  has  a  short  exposure  on  the 

matic  ridge.  face  compared  with  that  o{  Thrinaxodon  or 

The  individual  skull  bones  are  briefly  Probainognathus.     Within     the     orbit,     it 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching        15 


Figure  4.  Skull  of  Lumkuia  fuzzi  (BP/1/2669)  in  occipital  view  (upper  drawing  enlarged  x3).  Scale  bar  =  10  mm.  Abbreviations: 
bo,  basioccipital;  earn,  external  auditory  meatus;  eo,  exoccipital;  f,  frontal;  j,  jugal;  I,  lacrimal;  If,  lacrimal  foramina;  op,  opisthotic; 
p,  parietal;  po,  postorbital;  pp,  postparietal;  prf,  prefrontal;  pt,  pterygoid;  ptf,  posttemporal  foramen;  q,  quadrate;  qj,  quadratojugal; 
s,  stapes;  so,  supraoccipital;  sq,  squamosal;  t,  tabular. 


forms  the  anterior  half  of  the  orbital  wall 
and  most  of  its  floor.  Paired  lacrimal  fo- 
ramina open  forward  inside  the  anterior 
rim  of  the  orbit;  a  small  forannen  opens 
anterolaterally  from  the  lower  lacrimal  ca- 
nal on  to  the  facial  portion  of  the  lacrimal. 
A  posterolaterally  directed  process  of 
the  postorbital  forms  the  dorsal  part  of  the 
postorbital  bar;  it  extends  down  internal  to 
the  postorbital  process  of  the  jugal  for  an 
indeterminate  distance.  The  upper,  more 


horizontal,  part  of  the  postorbital  bar  is 
roughly  triangular  in  cross  section;  its  pos- 
terior face  forms  a  flat  vertical  surface  that 
is  continuous  posteromedially  with  a  ver- 
tical lappet  of  postorbital  that  overlies  the 
lateral  surface  of  the  parietal.  The  poste- 
rior parts  of  the  paired  postorbitals  con- 
verge backwards  as  temporal  crests  and 
merge  into  the  median  sagittal  crest  on  the 
parietals.  These  vertical  surfaces  on  the 
postorbital  mark  the  area  of  attachment  of 


16         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  5.  Skulls  in  lateral  and  ventral  views  of  (A,  B)  Thrinaxodon  liorhinus,  and  (C,  D)  Probainognathus  jenseni.  Scale  bars 
=  20  mm.  Abbreviations:  a,  angular;  ar,  articular;  bo,  basioccipital;  d,  dentary;  e,  epipterygoid;  ec,  ectopterygoid;  eo,  exoccipital; 
f,  frontal;  ic,  internal  carotid  foramen;  j,  jugal;  1,  lacrimal;  mx,  maxilla;  n,  nasal;  op,  opisthotic;  p,  parietal;  pi,  palatine;  pm, 
premaxilla;  po,  postorbital;  pr,  prootic;  prf,  prefrontal;  ps,  parasphenoid;  pt,  pterygoid;  q,  quadrate;  qj,  quadratojugal;  ref  lam, 
reflected  lamina;  s,  stapes;  sa,  surangular;  sm,  septomaxilla;  sq,  squamosal;  t,  tabular;  v,  vomer. 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching        17 


B 


ref  lam 


op  qj 


Figure  6.  Skulls  in  lateral  and  ventral  views  of  (A,  B)  Cynognathus  crateronotus,  and  (C,  D)  Diademodon  mastacus.  Scale  bar 
in  A  =  100  mm,  in  B  =  90  mm.  Abbreviations:  a,  angular;  ar,  articular;  bo,  basioccipital;  d,  dentary;  e,  epipterygoid;  ec,  ectop- 
terygoid;  eo,  exoccipital;  f,  frontal;  j,  jugal;  I,  lacrimal;  mx,  maxilla;  n,  nasal;  op,  opisthotic;  p,  parietal;  pi,  palatine;  pm,  premaxilla; 
po,  postorbital;  pr,  prootic;  prf,  prefrontal;  ps,  parasphenoid;  pt,  pterygoid;  q,  quadrate;  qj,  quadratojugal;  ref  lam,  reflected  lamina; 
s,  stapes;  sm,  septomaxilla;  spj,  suborbital  process  of  jugal;  sq,  squamosal;  t,  tabular;  v,  vomer. 


18         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


the  anteriormost  portion  of  the  temporahs  zygomatic  processes,  separated  at  the  level 

muscle.   A  medially  extending  horizontal  of  the  V-shaped  notch.  The  cranial  process 

lappet  of  postorbital  contacts  the  sliver  of  is  a  relatively  flat,  triangular  plate  extend- 

frontal  exposed  in  the  orbital  wall.  ing  nearly  to  the  apex  of  the  posterior  end 

The  dorsal  parts  of  the  fused  parietals  of  the  sagittal  crest.  The  cranial  process 
are  damaged,  but  enough  is  preserved  to  overhangs  the  anterior  opening  of  the 
indicate  that  the  sagittal  crest  was  relative-  posttemporal  foramen  and  its  flaring  rear 
ly  low  anteriorly  and  increased  only  mod-  border  forms  the  lambdoidal  crest.  The  V- 
erately  in  height  posteriorly.  No  evidence  shaped  notch  has  an  anteroposteriorly 
of  a  parietal  foramen  is  preserved  and  it  rounded  dorsal  surface  that  separates  the 
was  almost  certainly  absent.  The  ventral  lambdoidal  ridge  from  the  dorsal  ridge  on 
margin  of  the  parietal  contacts  the  dorsal  the  zygomatic  process.  Directly  below  the 
edge  of  the  orbitosphenoid,  behind  which  notch  is  a  triangular  lappet  of  squamosal 
it  is  overlapped  by  the  dorsal  margin  of  the  that  on  its  medial  surface  bears  a  depres- 
epipterygoid  back  to  its  midlength.  Be-  sion  for  the  incompletely  ossified  distal 
tween  the  parietal  and  the  dorsal  margins  end  of  the  paroccipital  process.  Antero- 
of  the  epipterygoid  and  prootic  is  an  elon-  medially,  the  lappet  appears  to  contact  the 
gate  opening  into  the  cranial  cavity.  Lead-  lateral  flange  of  the  prootic.  Laterally,  it 
ing  to  this  opening  from  behind,  along  the  forms  the  medial  wall  of  the  recess  for  the 
prootic-parietal  suture,  is  a  deeply  incised  quadrate,  which  is  open  behind  as  an  in- 
groove  that  begins  at  the  anterior  opening  verted  V-shaped  emargination.  The  emar- 
of  the  posttemporal  foramen.  The  groove  gination  is  bounded  laterally  by  a  slender, 
presumably  contained  the  supraorbital  ra-  pointed  process  that  descends  between  the 
mus  of  the  ramus  superior  of  the  stapedial  upper  ends  of  the  quadrate  and  quadra- 
artery,  with  a  meningeal  branch  entering  tojugal.  Further  laterally,  the  zygomatic 
the  cranial  cavity  through  the  elongate  portion  of  the  squamosal  forms  a  descend- 
opening  (Rougier  et  al.,  1992;  Wible  and  ing  process  behind  the  jugal  that  in  life 
Hopson,  1995).  The  parietals  broaden  pos-  presumably  contacted  the  surangular  (al- 
teriorly,  where  they  are  overlain  by  the  though  here  a  contact  is  absent  because 
cranial  process  of  the  squamosal,  and  con-  the  lower  jaw  appears  to  have  shifted 
tribute  to  the  roof  of  the  posttemporal  fo-  slightly  forward).  The  zygomatic  process 
ramen.  curves  foiward  from  this  level  extending 

The  jugal  is  a  relatively  slender  bone,  over  the  jugal  nearly  to  the  level  of  the 

not  unlike  that  of  Thrinaxodon  and  Pro-  postorbital  bar.  A  shallow  sulcus,  the  ex- 

bainognathus.  In  the  zygomatic  arch,  the  ternal   auditory   meatus,   extends   up   and 

jugal  is  overlain  dorsally  by  the  zygomatic  foi-ward  from  the  distal  end  of  the  paroc- 

process  of  the  squamosal  and  bounded  be-  cipital  process  on  to  the  posterolateral  sur- 

hind  by  a  descending  lappet  of  squamosal,  face  of  the  zygoma. 

A  moderate-sized,  anterolaterally  directed  The  fused  vomers  form  the  center  of 

foramen  pierces  the  jugal  below  the  orbit,  the    arched    roof   of  the    primary   palate 

A  short  distance  behind  the  last  postca-  above  the  secondaiy  palate  and  roof  the 

nine,  the  jugal  passes  medial  to  the  rear  of  choanal  trough  to  a  point  just  behind  the 

the    maxilla   to   contact   the    anterolateral  level  of  the  last  postcanine. 

margin  of  the  pterygoid,  and  perhaps  the  The  palatal  plates  of  the  palatines  form 

palatine,  at  the  anterior  border  of  the  sub-  the  posterior  third  of  the  short  secondary 

temporal  fossa.  The  jugal  is  exposed  be-  palate,  underlying  the  posterior  margins  of 

hind  the  lacrimal  in  the  posterior  part  of  the  maxillae.  A  small  foramen  pierces  the 

the  orbital  floor.  palatine  a  short  distance  posterointernal  to 

The    squamosal    may   be    described   as  the  major  palatine  foramen.  The  rear  mar- 
consisting  of  two  portions,  the  cranial  and  gin  of  the  secondary  palate  is  thickened 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching        19 


and  slightly  rugose.  As  in  other  Triassic  tween  the  ridges  is  divided  by  the  long  ros- 
probainognathians,  the  lateral  margin  of  trum  of  the  parasphenoid  to  form  paired 
the  secondary  palate  curves  dorsally,  so  interpteiygoidal  vacuities.  Such  vacuities 
that  the  palatine  meets  the  maxilla  in  the  are  present  in  Dvinia  and  Procynosiichus 
floor  of  a  narrow  longitudinal  trough  in-  and  in  juveniles  of  Thrinaxodon  (Estes, 
temal  to  the  posterior  postcanines.  This  1961),  but  are  usually  absent  in  postpro- 
trough  continues  back  beyond  the  level  of  cynosuchid  cynodonts. 
the  secondary  palate,  where  it  is  bounded  The  orbitosphenoid  is  roughly  the  shape 
medially  by  slender  ridges  that  extend  of  an  elongate  half-cylinder,  with  a  U- 
back  nearly  to  die  lateral  margins  of  the  shaped  cross  section.  It  lies  on  the  midline 
pterygoid  flanges.  An  ectopterygoid  is  not  below  the  postorbitals  and  parietals  in  the 
present,  so  the  posterolateralmost  part  of  space  between  the  postorbital  bar  and  the 
the  palatine  contacts  the  pterygoid,  and  anterodorsal  end  of  the  epipteiygoid. 
perhaps  the  jugal,  internal  to  the  last  post-  The  ascending  lamina  of  the  epiptery- 
canine.  The  palatine  is  here  pierced  by  goid  is  extremely  long  fore  to  aft,  being 
several  small  foramina,  with  a  larger  open-  nearly  twice  the  length  of  the  prootic  por- 
ing between  its  posterior  margin  and  the  tion  of  the  braincase  sidewalk  This  con- 
overlying  pteiygoid.  The  palatines  form  trasts  sharply  with  the  condition  in  Pro- 
the  lateral  walls  of  the  choanal  trough,  bainognathus  and  Ecteninion,  in  which  the 
contacting  the  vomer  and  pterygoids  me-  ascending  lamina  tapers  anterodorsally  and 
dially  and  contributing  to  the  anterior  half  is  much  shorter  than  the  prootic.  The  as- 
of  the  more  medial  palatal  ridges  that  cending  lamina  is  suturally  joined  to  the 
bound  the  posterior  half  of  the  trough,  anterodorsal  margin  of  the  prootic  above 
The  palatine  is  exposed  on  the  upper  sur-  the  anterior  border  of  the  large  trigeminal 
face  of  the  primary  palate  as  a  broad  plate  foramen.  The  epipterygoid  contacts  the 
that  lacks  a  dorsal  orbital  process.  basicranial  wing  of  the  pterygoid  ventrally 

The  ectopterygoid  is  absent.  Although  and  appears  to  have  a  short  medial  contact 

described  in  other  Triassic  probainogna-  with  the  basipterygoid  process.  Its  quad- 

thians  (Romer,  1969,  1970;  Martinez  et  ak,  rate  ramus  is  a  shallow  vertical  lamina  that 

1996),   we    believe    its   presence   has    not  extends  back  below  the  trigeminal  fora- 

been  convincingly  demonstrated.  men  to  meet  the  lateral  flange  of  the  pro- 

The  pteiygoids  form  the  rear  of  the  cho-  otic.  The  epipterygoid  continues  back  for 

anal  trough,  which  is  uniquely  deep  and  is  a  short  distance  in  contact  with  the  lateral 

bordered  behind  by  a  near-vertical  wall.  At  flange,  terminating  at  the  level  of  the  an- 

the   posterior   end   of  the    medial  palatal  terior  border  of  the  pteiygoparoccipital  fo- 

ridges,  where  they  converge  at  the  rear  of  ramen.  That  portion  of  the  epipteiygoid 

the  choanal  trough,  is  a  prominent  median  behind  the  basipterygoid  joint  forms  the 

boss;   this   feature   appears   to  be   unique  lateral  wall  of  a  ventrally  open  space,  the 

among  cynodonts.  Lateral  to  the  anterior  cavum  epiptericum. 

end  of  the  medial  palatal  ridge,  adjacent  The  basisphenoid  consists  of  slightly  ex- 
to  the  suture  with  the  palatine,  are  one  or  panded  anterior  basipterygoid  processes 
more  slitlike  openings  that  pierce  the  pter-  that  contact  the  pterygoids  and  epipteiy- 
ygoid.  Laterally,  the  deep,  triangular  pter-  goids,  a  very  narrow  middle  portion  that 
ygoid  flanges  descend  well  down  the  inside  underlies  the  sella  turcica  and  is  pierced 
of  the  lower  jaws.  The  ridges  forming  their  by  paired  carotid  foramina,  and  an  ex- 
rear  margins  converge  posteriorly  and  ex-  panded  posterior  part  that  contacts  the 
tend  on  to  the  basipteiygoid  rami  of  the  prootic  dorsally  and  the  basioccipital  pos- 
pteiygoids,  nearly  meeting  where  the  lat-  teriorly.  The  dermal  parasphenoid  is  fused 
ter  contact  the  basipteiygoid  processes  of  to  its  ventral  surface,  forming  a  near-hor- 
the    basisphenoid.    An    elongate    gap    be-  izontal,    triangular   plate    posteriorly   that 


20         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


covers   the  basisphenoid-basiooccipital  opisthotic  with  the  space  occupied  by  the 

contact.  Further  forward,  the  parasphen-  inner  ear.   Deep  within  the  jugular  fora- 

oid  passes  between  the  carotid  foramina  men  is  a  low  ridge  that  extends  a  short 

and  forms  an  elongate  midline  process,  the  distance  into  the  opening  from  its  postero- 

rostrum,  that  extends  forward  between  the  lateral  wall.  This  ridge  in  more  derived  cy- 

pterygoids  to  separate  the  interpteiygoidal  nodonts,    such    as   Prohainognathus    (Fig. 

vacuities.  The  anterior  end  of  the  paras-  5D)  and  Massetognathus  (Rougier  et  al., 

phenoid  is  suturally  joined  to  the  ptery-  1992,  figs.  7B,  D),  is  a  long  fingerlike  pro- 

goids  immediately  behind  and  dorsal  to  jection  that  extends  toward  the  medial  wall 

the  median  pterygoid  boss.  of  the  foramen.  In  tritheledontids,  tritylo- 

The  prootic  portion  of  the  ossified  otic  dontids,  and  mammaliaforms,  the  foramen 

capsule  lacks  a  sutural  separation  from  the  is  fully  subdivided,  with  a  true  jugular  fo- 

opisthotic   portion,    although   the   prootic  ramen  posteriorly  (transmitting  nerves  and 

typically  contributes  to  the  anterior  part  of  vessels  from  the  cranial  cavity),  and  a  peri- 

the  paroccipital  process  and  rim  of  the  fe-  lymphatic  foramen  anteriorly  (transmitting 

nestra  ovalis.  The  lateral  flange  of  the  pro-  the  perilymphatic  duct  from  the  inner  ear 

otic  extends  posterolaterally  from  behind  cavity). 

the  trigeminal  foramen;  although  the  distal  The  basioccipital  is  exposed  midventral- 

end  of  the  lateral  flange  is  damaged,  it  un-  ly  behind  the  parasphenoid,  with  which  it 

doubtedly  contacted  the  squamosal  in  life,  has  an  interdigitating  transverse  suture.  It 

thus  enclosing  the  large,  oval,  pterygopar-  forms  the  midventral  part  of  the  foramen 

occipital  foramen.  The  lateral  surface  of  magnum,  bearing  a  narrow  transverse  ar- 

the  prootic  bears  a  slight  groove  that  ex-  ticular  facet  for  the  atlas  intercentiaim. 
tends  between  the  latter  opening  and  the  The  paired  exoccipitals  form  the  occip- 

trigeminal  foramen.  Such  a  groove  is  usual  ital  condyles,  damaged  here,  which  extend 

in  cynodonts,  although  here  it  is  unusually  about  one  third  of  the  distance  up  the  lat- 

faint.  The  system  of  grooves  and  foramina  eral  sides  of  the  foramen  magnum.  More 

in  the  lateral  surface  of  the  prootic  are  in-  dorsally,  they  meet  the  supraoccipital,  but 

terpreted  as  transmitting  arteries  and  veins  the    sutural    contact   cannot   be    distin- 

(see  Rougier  et  al.,  1992;  Wible  and  Hop-  guished.  The  exoccipital  contributes  to  the 

son,  1995).  Deep  to  the  outer  margin  of  posteromedial  wall  of  the  jugular  foramen, 

the  trigeminal  foramen,  the  ossified  pila  which  bears  a  shallow  depression  in  which 

antotica    extends    anterodorsally    approxi-  lie  two  hypoglossal  foramina,  a  smaller  an- 

mately  to  the  level  of  the  basipteiygoid  terior    one    and    a    larger   posterior   one, 

joint.  Just  in  front  of  the  fenestra  ovalis  is  which  open  into  the  cranial  cavity  shortly 

the   small,   posterolaterally  directed  fora-  in  front  of  the  occipital  condyle, 
men  for  the  facial  (Vllth)  nei-ve.  The  median  supraoccipital  forms  an  in- 

The  opisthotic  forms  the  posterior  half  determinate  part  of  the  dorsal  border  of 

of  the  rim  of  the  fenestra  ovalis;  most  of  the  foramen  magnum.  The  supraoccipital 

the  paroccipital  process;  and  the  anterior,  is  overlain  by  the  tabular  laterally  and  the 

anteromedial,  and  lateral  borders  of  the  postparietal  above.  The  postparietal  occu- 

jugular  foramen.  The  ventral  surface  of  the  pies    the    upper    surface    of   the    occiput 

paroccipital  process  slopes  up  and  foi-ward  above  the  supraoccipital  and  tabulars  and 

from  its  rounded  posteroventral  margin,  to  between  the  flaring  lambdoidal  crests, 

form  the  posterodorsal  wall  of  the  middle  Middorsally,  the  postparietal  has  a  short, 

ear  cavity  (Hopson,  1966).  The  opisthotic  pointed  process  that  extends  forward  be- 

contacts  the  basioccipital  medially  and  the  tween  the  fused  parietals.  The  tabulars  oc- 

exoccipital  posteromedially  and  posterolat-  cupy  the  entire  occiput  lateral  to  the  su- 

erally  on  the  margins  of  the  jugular  fora-  praoccipital,   completely  surrounding  the 

men.  This  foramen  is  confluent  within  the  small,  circular  posttemporal  foramina. 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching        21 


The  quadrate  is  exposed  on  the  right  dentary  is  a  slightly  projecting  pseudan- 
side,  where  it  has  shifted  slightly  forward  gular  process,  above  which  the  lower  mar- 
from  its  contact  with  the  squamosal.  The  gin  of  the  bone  curves  up  and  back  over 
transversely  oriented  articular  condyle  of  the  postdentary  elements.  A  low  out- 
the  quadrate  is  about  as  wide  as  the  total  turned  ridge  overlies  the  surangular  and 
bone  is  high.  The  flat  posterior  surface  of  angular  and  continues  forward  across  the 
its  ascending  process  is  oriented  obiquely  masseteric  fossa,  fading  into  its  surface  be- 
to  the  transverse  axis  and  fits  against  a  low  the  last  upper  postcanine.  The  mas- 
matching  surface  on  the  anterior  face  of  seteric  fossa  extends  forward  as  a  slight  de- 
the  squamosal.  The  posterolateral  third  or  pression  to  the  level  of  the  fifth  upper 
so  of  the  quadrate  is  exposed  from  behind  postcanine.  The  coronoid  process  rises 
in  the  inverted  V-shaped  emargination  of  slightly  above  the  dorsal  border  of  the  zy- 
the  squamosal.  The  lateral  end  of  the  gomatic  arch  just  behind  the  postorbital 
quadrate  condyle  extends  well  beyond  the  bar.  The  lateral  surface  of  the  coronoid 
outer  margin  of  the  ascending  process;  its  process  forms  a  broad,  slightly  concave 
dorsal  surface  is  clasped  by  the  transverse-  trough  between  out-turned  anterodorsal 
ly  expanded  lower  end  of  the  quadratoju-  and  posteroventral  borders.  The  slightly 
gal.  convex   posterior   margin    of  the   process 

The  quadratojugal  has  a  transversely  slopes  down  to  meet  the  surangular  about 

compressed  ascending  process  that  fits  into  5  mm  anterior  to  the  articular  glenoid, 

a  narrow  groove  in  the  squamosal  behind  As  is  usual  in  eucynodonts,  the  laterally 

the  lateral  part  of  the  ascending  process  of  exposed  postdentary  bones  are  much  shal- 

the  quadrate.  The  quadratojugal  is  separat-  lower  than  in  Thrinaxodon  (Fig.  5A),  with 

ed  from  the  quadrate  posteriorly  by  a  thin  their  lower  border  sloping  up  and  back, 

descending  prong  of  squamosal.  The  lower  The  surangular  has  less  exposure  behind 

end  of  the  bone  is  expanded  transversely,  the  dentary  than  in  Thrinaxodon,  but  more 

its  medial  portion  overlying  the  lateral  con-  than  in  other  eucynodonts,  where  the  den- 

dyle  of  the  quadrate  and  its  lateral  portion  tary  nearly  reaches  the  articular  (Figs.  5C, 

forming  a  free  rounded  process.  6A,  C).  On  the  medial  surface  of  the  jaw. 

An  incomplete  right  stapes  is  preserved  the  surangular  has  a  flat  dorsal  surface  that 

nearly  in  situ,  its  oval  footplate  separated  is  buttressed  by  an  overlying  ridge  on  the 

slightly  from  the  depression  that  houses  dentary.  The  exposed  part  of  the  suran- 

the  fenestra  ovalis.  The  preserved  poste-  gular  behind  the  dentary-  has  a  transversely 

rior  cms  of  the  stapes  extends  anterolat-  thickened  upper  margin.  Anterolateral  to 

erally  toward  the   medial   surface   of  the  the   articular  glenoid  is   a  slightly  raised 

quadrate  condyle.  area  that  in  life  may  have  contacted  the 

descending  flange  of  the  squamosal;  how- 
Lower  Jaw  ever,  it  lacks  the  prominent  articular  boss 

The  right  lower  jaw  is  essentially  com-  that  contacts  the  squamosal  in  Cynogna- 

plete  and  well  preserved.  The  large  den-  thus  and  Diademodon  (Crompton,  1972a). 

tary  consists  of  a  deep  tooth-bearing  hor-  The  angular  covers  most  of  the  suran- 

izontal  ramus  and  a  broad  ascending  pro-  gular  laterally  and  has  a  dorsal  ridge  that 

cess  (for  insertion  of  jaw-closing  muscles),  overhangs  its  concave  outer  surface.  The 

each  forming  about  one  half  of  its  length,  reflected  lamina  is  damaged,  but  it  appears 

The  short,  deep  symphysis  is  fused.  The  to  be  more  slender  than  that  of  Thrinax- 

anteroventral  surface  of  the  fused  dentar-  odon.  The  articular  is  transversely  narrow- 

ies   bears   numerous   tiny   foramina.   Two  er  than  in  Thrinaxodon,  more  closely  re- 

smafl  mental  foramina  fie  below  the  first  sembling  that  of  Probainognathus  and 

and  second  postcanines.  At  the  posterior  Probelesodon.  The  remaining  postdentary 

end  of  the  convex  lower  margin  of  the  elements  are  similar  to  those  of  Thrinax- 


22         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


odon,  except  that  the  splenials  are  fused  in      ence  of  an  anterior  accessory  cusp  cannot 

the  rear  of  the  symphysis.  be  determined.  Both  upper  and  lower  po- 

stcanines  appear  to  lack  lingual  cingula. 
Dentition 


The  dental  formula  is:  14/3,  Cl/1,  Pc7/ 


Postcranial  Skeleton 


5.  The  incisors  are  all  small  and  closely  The  poorly  preserved  shoulder  girdle, 

spaced.  The  canines  are  long  and  broad,  forelimb,   and  caudal  vertebrae  show  no 

with  extremely  robust  roots.  The  canines  unusual  features  and  will  not  be  described, 

have  a  rounded  anterior  surface  and,  in  The  dorsal  vertebral  series,  although  not 

the  uppers  at  least,  an  unserrated  ridge  well   preserved,    merits    description    inas- 

posteriorly.  much  as  it  possesses  features  that  distin- 

The  upper  postcanines  increase  in  size  guish  probainognathians  from  cynognathi- 
from  first  to  sixth,  with  the  seventh  being  ans.  The  articulated  section  of  the  dorsal 
slightly  smaller  than  the  fifth.  The  first  vertebral  column  contains  10  vertebrae  ex- 
three  have  a  slightly  recurved  main  cusp  posed  in  ventral  view.  On  the  partially  ex- 
and  a  small  posterior  accessory  cusp.  The  posed  left  side,  the  last  two  vertebrae  show 
fourth  is  well  preserved  on  the  left,  where  a  pair  of  articulating  zygapophyses,  thus 
it  possesses  a  large  recurved  main  cusp,  a  establishing  directionality  along  the  col- 
smaller  accessory  cusp  behind  it,  and  a  umn.  The  last  nine  vertebrae  preserve 
second,  much  smaller,  posterior  accessory  ribs.  Of  these,  the  last  two  possess  features 
cusp  near  the  base  of  the  crown.  Anterior,  that  together  characterize  cynodont  lum- 
and  slightly  internal,  to  the  main  cusp  is  a  bar  vertebrae  (Jenkins,  1971):  the  rib  at- 
very  small  accessory  cusp;  this  cusp  is  ab-  tachments  are  entirely  on  the  vertebral 
sent  on  the  right,  perhaps  obliterated  by  body,  and  these  ribs  are  synostosed  to  the 
wear.  Upper  postcanine  5  is  much  larger  vertebrae  with  a  serrate  suture.  In  the 
than  Pc^,  but  is  nearly  identical  in  mor-  more  anterior  ribs,  the  capitular  articula- 
phology.  Upper  postcanine  6  has  a  small  tion  spans  two  adjacent  centra;  whether 
anterointernal  cusp,  a  strongly  recurved  any  are  synostosed  is  uncertain,  although 
main  cusp,  and  a  smaller  recurved  poste-  the  first  rib,  at  least,  appears  to  be  free, 
rior  accessory  cusp.  The  rear  of  the  crown  The  anterior  four  pairs  of  ribs  are  dam- 
is  damaged,  so  the  presence  of  a  second  aged  distally,  but  they  appear  to  be  an- 
posterior  cusp  is  uncertain.  The  damaged  teroposteriorly  compressed,  thus  resem- 
seventh  postcanine  has  a  recurved  main  bling  typical  thoracic  ribs.  The  posterior 
cusp  followed  by  an  accessory  cusp,  but  five  sets  of  ribs  appear  to  be  short,  because 
the  presence  of  additional  cusps  is  uncer-  their  more  or  less  rounded  ends  retain 
tain.  The  teeth  are  set  at  a  slight  angle  to  some  matrix  distally.  These  ribs  are  per- 
the  line  of  the  tooth  row,  so  that,  where  haps  slightly  broader  than  those  preceding 
present,  the  posterior  accessory  cusp  con-  them,  but  they  do  not  expand  distally  to 
tacts  the  succeeding  crown  lingual  to  its  any  noticeable  degree.  The  last  rib  is 
anterior  accessory  cusp.  broader  than  the  preceding  ones,  as  is  the 

The  lower  postcanines  are  less  fully  ex-  last  (second)  lumbar  vertebra  of  Cijnog- 

posed.  The  first  tooth  is  damaged,  but  the  nathus   illustrated   by  Jenkins    (1971,    fig. 

well-preserved    second    closely    resembles  15A).    Also   as   in    Cijnogriathus,    the   last 

the  fourth  upper  postcanine;  both  resemble  three  sets  of  ribs  curve  slightly  forward, 

a  typical  lower  postcanine  of  Thrinaxodon.  However,  at  a  comparable  distance  from 

The  crowns  of  Vc^^,  are  exposed  lingually;  the  proximal  synostosis,  the  posterior  ribs 

the  third  and  fourth  have  an  anterior  ac-  of  Liinikuia  show  no  trace  of  the  distal  ex- 

cessory  cusp  and  at  least  one  posterior  ac-  pansions  seen  in  Galesaunis,  Thrinaxodon, 

cessoiy  cusp,  whereas  the  fifth  has  two  pos-  Cynognathus,   and  Diademodon  (Jenkins, 

terior  accessory  cusps,  although  tlie  pres-  1971).   Thus,   they  resemble   the   lumbar 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching        23 


ribs   of  the  probainognathians  Probeleso- 
don  and  Probainognathus  (Romer,  1973). 

PHYLOGENETIC  RELATIONSHIPS  OF 
LUMKUIA  FUZZI 

A  cladistic  analysis  of  cynodonts  was 
performed,  with  23  cynodont  taxa  and  the 
basal  therocephalian  Lycosuchus  and  a 
gorgonopsid  as  successive  outgroups  (see 
Appendix  2).  Of  101  characters,  43  are 
from  the  skull,  9  from  the  lower  jaw,  29 
from  the  dentition,  and  20  from  the  post- 
cranial  skeleton  (see  Appendix  1).  The 
aims  of  most  past  phylogenetic  analyses 
have  been  to  order  therapsid  taxa  with  re- 
spect to  mammals,  hence  only  taxa  and 
characters  that  served  to  do  this  were  in- 
cluded. We  have  made  a  special  effort  to 
include  a  large  sample  of  gomphodont  taxa 
and  to  include  characters,  particularly 
from  the  postcanine  dentition,  that  would 
specifically  aid  in  resolving  their  interre- 
lationships. The  data  were  analyzed  using 
a  random  addition  sequence  with  10  rep- 
licates and  the  tree  bisection— reconnection 
(TBR)  algorithm  of  PAUP  3.1  (Swofford, 
1993),  with  the  resulting  character  distri- 
bution optimized  under  delayed  transfor- 
mation (DELTRAN). 

Although  resolution  of  the  phylogenetic 
relationships  of  tritylodontids  with  respect 
to  tritheledontids  and  mammaliaforms  is 
not  the  principal  aim  of  this  study,  we  have 
attempted  to  deteriuine  where  these  three 
taxa  are  placed  under  different  treatments 
of  the  characters.  When  all  characters 
were  run  unordered,  the  tritheledontid 
Pachygenelus  and  the  mammaliaform 
Morganucodon  were  the  sister  group  of 
Tritylodontidae,  nested  deeply  within  the 
gomphodont  clade  (tree  length  =  233; 
Consistency  Index  (CI)  =  0.58;  Retention 
Index  (RI)  =  0.78;  Rescaled  CI  =  0.45). 
When  a  minimum  of  four  multistate  char- 
acters (18,  22,  63,  73)  were  ordered,  Pach- 
ygenelus and  Morganucodon  shifted  to  a 
probainognathian  clade,  where  they  re- 
mained under  tests  of  cladogram  robust- 
ness (see  below).  This  is  the  cladogram  il- 
lustrated here  (Fig.  7). 


The  analysis  (with  four  ordered  charac- 
ters) resulted  in  three  most  parsimonious 
trees  of  238  steps  (CI  =  0.57;  RI  =  0.77; 
RC  =  0.44).  The  trees  differ  only  in  the 
placement  of  the  basal  cynodonts  Ovinia 
and  Procynosuchus  with  respect  to  "high- 
er" cynodonts,  either  in  a  trichotomy  with 
the  latter,  as  their  sister  clade,  or  with  Pro- 
cynosuchus and  Ovinia  as  their  successive 
outgroups.  The  cladogram  (Fig.  7)  shows 
the  last  (our  preferred)  alternative. 

Three  near-basal  clades  are  supported  by 
large  numbers  of  unequivocal  synapomor- 
phies:  Cynodontia  by  26,  Epicynodontia  by 
14,  and  Eucynodontia  by  11.  A  dichotomy 
witliin  Eucynodontia  includes  a  well-char- 
acterized Cynognatliia,  witli  eight  unequiv- 
ocal synapomorphies,  and  a  less  well-char- 
acterized Probainognatliia,  witli  four  un- 
equivocal (and  two  equivocal)  synapomor- 
phies. Within  Cynognathia,  the 
Gomphodontia  are  characterized  by  five  un- 
equivocal (and  two  equivocal)  synapomor- 
phies. Witliin  tlie  latter  clade,  die  paraphy- 
letic  traversodonts  (including  Tritylodonti- 
dae as  a  derived  subgroup)  are  chai'acterized 
by  three  unequivocal  (and  one  equivocal) 
synapomorphies.  Characters  diagnosing 
each  clade  are  listed  in  Appendix  3. 

Lunikuia  is  the  basal  member  of  the  Pro- 
bainognatliia, although  Ecteninion  from  the 
early  Late  Triassic  is  more  derived  in  but  a 
single  feature:  a  frontal— palatine  contact  in 
the  orbital  wall.  Prohelesodon,  Chiniquo- 
don,  and  Aleodon  represent  a  nionophyletic 
Chiniquodontidae,  characterized  by  a  very 
long  secondary  palate  and  a  posterior  an- 
gulation of  the  maxilla.  Probainognathus  is 
allied  with  the  tritheledontid/mammali- 
aform  clade  by  two  synapomorphies:  the 
presence  of  postcanine  lingual  cingula  and 
a  medial  shift  of  die  maxillary  tooth  rows. 
Pachygenehis  and  Morganucodon  form  an 
extremely  robust  clade,  supported  by  18 
unequivocal  synapomorphies.  Although  this 
clade  shares  many  character  states  with  tri- 
tylodontids, the  latter  are  deeply  nested 
within  tlie  Gomphodontia  on  the  basis  of 
numerous  cynognathian  and  gomphodont 
synapomoipliies. 


24         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


#^ 


.r.v^    XO^ 


.^^/  ^A^y 


MM 


MM 


I 


PROBAINO- 
GNATHIA 


1 


1 


S 


Traversodonts' 


GOMPHODONTIA 
CYNOGNATHIA 


EUCYNODONTIA 


EPICYNODONTIA 


CYNODONTIA  Tree  Length:  238 

Consistency  Index  (CI):  0.57 
Retention  Index  (Rl):  0.77 
Rescaled  CI:  0.44 

Figure  7.  Cladogram  of  nonmammalian  cynodonts.  One  of  three  shortest  trees  (238  steps  in  length),  in  which  Ovinia  is  sister 
taxon  to  remaining  cynodonts.  "Traversodonts"  refers  to  Pascualgnathus  and  more  derived  gomphodonts,  usually  designated 
as  Traversodontidae.  However,  inclusion  of  Tritylodontidae  in  this  "family"  makes  it  paraphyletic,  hence  use  of  the  informal  term 
"traversodonts." 


The  robustness  of  this  cladogram  was 
tested  by  generating  trees  of  incrementally 
greater  length  (up  to  six  steps  longer)  to 
determine  where  specific  nodes  break 
down.  At  one  step  longer  (239  steps),  in 
the  strict  consensus  of  59  trees,  nearly  all 
resolution  within  Eucynodontia  breaks 
down,  leaving  only  the  grouping  of  the  chi- 
niquodontids  Aleodon  +  Chiniquodon  and 
of  Pachygenelus  +  Morganucodon.  How- 
ever, the  50%  majority-rule  consensus  tree 
has  the  same  topology  as  the  minimimi- 
length  tree.  At  two  steps  longer,  in  the 
50%  majority-rule  consensus  of  286  trees, 
the  node  between  Probainognathus  and 
Ecteninion   breaks    down,   yielding   a   tri- 


chotomy with  a  chiniquodontid  +  Pachtj- 
genelus/Morganucodon  clade.  At  three 
steps  longer,  in  the  50%  majority-rule  con- 
sensus of  1,024  trees,  the  node  between 
Tritylodontidae  and  "Scalenodon"  hir- 
schoni  breaks  down.  At  four  steps  longer 
(3,480  trees),  the  node  between  Probele- 
sodon  and  the  remaining  chiniquodontids 
breaks  down.  Only  in  the  50%  majority- 
rule  consensus  of  30,120  trees  that  are  six 
steps  longer  than  the  minimum-length 
tree  does  the  node  between  Lumkuia  and 
the  remaining  probainognathians  break 
down  (Fig.  8).  A  probainognathian  clade 
occurs  in  75%  of  these  trees  and  cynog- 
nathian  and  gomphodont  clades  both  oc- 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching        25 


Traversodonts'  (77) 

GOMPHODONTIA  (83) 
CYNOGNATHIA  (83) 


EUCYNODONTIA(IOO) 


EPICYNODONTIA  (100) 


CYNODONTIA(IOO) 


2-6: 
54-100: 


Shortest  Tree:  238  steps 

Number  of  steps  to  collapse  node 

Percent  of  trees  retaining  node  in 
Majority-Rule  consensus  of 
30,120  trees  of  <  or  =  244  steps 


Figure  8.  Cladogram  of  nonmammalian  cynodonts.  Shortest  tree  (238  steps)  is  shown,  with  numbers  In  bold  italics  (2-6) 
indicating  the  number  of  steps  required  to  collapse  that  node,  and  numbers  in  bold  (54-100)  indicating  the  percentage  of  trees 
retaining  that  node  in  a  50%  majority-rule  consensus  of  30,120  trees  of  less  than  or  equal  to  244  steps  (six  steps  longer  than 
minimum-length  tree). 


cur  in  83%  of  the  trees.  The  gomphodont 
genera  retain  the  ordering  seen  in  the 
minimum  length  tree  in  the  great  majority 
of  trees  that  are  six  steps  longer.  Tritylo- 
dontids  and  "S. "  hirschoni  form  a  trichot- 
omy with  the  Exaeretodon/Gomphodonto- 
suchiis  clade  in  54%  of  these  trees. 

In  order  to  determine  how  parsimoni- 
ous our  preferred  tree  is  to  that  of  Rowe 
(1993,  fig.  10.2),  we  used  MacClade  (Mad- 
dison  and  Maddison,  1992)  to  order  our 
19  eucynodont  taxa  in  the  most  parsimo- 
nious tree  in  which  the  cynognathian— pro- 
bainognathian dichotomy  is  not  recog- 
nized. This  turned  out  to  duplicate  the  or- 
der of  the  far  fewer  taxa  in  Rowe's  clado- 


gram except  that  tritheledontids,  not 
tritylodontids,  form  a  clade  with  mammal- 
iaforms  (Fig.  9A).  This  tree  is  267  steps 
long,  29  steps  longer  than  our  preferred 
tree.  In  the  comparison  of  this  tree  with 
our  preferred  tree  (Fig.  9B),  the  distribu- 
tion of  the  internal  carotid  foramina  is 
shown.  Absence  of  these  foramina  in  the 
basisphenoid  is  a  synapomorphy  of  Cynog- 
nathia  (Fig.  9B).  When  the  cynognathian- 
probainognathian  dichotomy  is  eliminated, 
the  distribution  of  this  character  becomes 
extremely  unparsimonious,  with  the  fo- 
ramina lost,  regained,  then  lost  and  sub- 
sequently regained  again. 


26         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


.^<^.o.-^5v^j.°^ 


B 


^o" 


.o<&^- 


□   □         nnnnnnn 


Figure  9.    Cladograms  constructed  using  MacClade  showing  distribution  of  internal  carotid  foramina  in  basispiienoid  (character 
26).  Absence  of  carotid  foramina  is  derived  (black).  (A)  Cladogram  in  which  19  eucynodont  taxa  are  ordered  in  the  most 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching        27 


CONCLUSIONS 

Lumkuia  fuzzi  is  a  basal  member  of  the 
eucynodont  clade  Probainognathia.  The  di- 
chotomy of  eucynodonts  into  Probainog- 
nathia and  Cynognathia  is  supported  by  this 
analysis,  as  is  the  placement  of  tlie  Trity- 
lodontidae  widiin  the  cynognathian  sub- 
group Gomphodontia.  The  sister  group  re- 
lationship of  Tridieledontidae  and  Mam- 
maliaformes  is  extremely  well  supported, 
aldiough  their  placement  in  Probainogna- 
thia, rather  than  as  sister  to  tritylodontids 
widiin  Cynognadiia,  is  less  firm,  requiring 
the  ordering  of  four  characters  to  achieve 
diis  placement.  This  uncertainty  results 
from  the  extraordinarily  large  number  of 
derived  (mammallike)  features  shared  by 
diese  three  groups,  features  treated  in  odi- 
er  recent  analyses  as  synapomorphies  but 
here  shown  more  likely  to  be  convergences. 
A  definitive  solution  to  this  phylogenetic 
problem  will  be  found  when  morphologic 
intermediates  between  typical  Triassic  cy- 
nodonts  and  these  primarily  Jurassic  (and, 
in  the  case  of  mammaliaforms,  later)  taxa 
are  incorporated  into  analyses.  Within  the 
gomphodonts,  Exaeretodon  has  a  very 
mammallike  postcranial  skeleton  and  helps 
bridge  the  morphologic  gap  between  Mid- 
dle Triassic  gomphodonts  and  tritylodon- 
tids. Bonaparte  and  Barberena  (2001)  de- 
scribe two  Late  Triassic  carnivorous  cyno- 
donts  that  are  also  very  mammallike  post- 
cranially,  and  that  appear  to  bridge  the  gap 
between  ProbainognatJms  and  tridieledon- 
tids/mammaliaforms  in  cranial  and  dental 
morphology.  We  believe  diese  newly  de- 
scribed Late  Triassic  cynodonts  will  provide 
critical  evidence  supporting  the  probain- 
ognathian—cynognathian  dichotomy  and  the 
occurrence  of  a  truly  extraordinary  amount 
of  homoplasy  in  eucynodont  evolution. 


ACKNOWLEDGMENTS 

We  thank  Drs.  M.  A.  Raath  and  B.  S. 
Rubidge  for  the  loan  of  material;  Ms.  Clai- 
re Vanderslice  for  preparation  and  illustra- 
tion of  specimens;  and  Mr.  C.  A.  Sidor  and 
Drs.  G.  W  Rougier,  J.  R.  Wible,  and  J.  A. 
Wilson  for  help  in  preparation  of  the  man- 
uscript. Hopson's  research  was  supported 
by  National  Science  Foundation  grants 
BSR  86-15016  and  89-06619.  We  are 
grateful  to  Dr.  F.  A.  Jenkins,  Jr.,  and  his 
co-organizers  of  the  symposium  for  pro- 
viding this  opportunity  to  honor  Fuzz 
Crompton.  Hopson  also  \\dshes  to  express 
his  pleasure  at  attending  the  symposium 
and  enjoying  the  fellowship  of  good 
friends  and  colleagues. 

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Paleobiology,  24:  254-273. 

Sues,  H.-D.  1985.  The  relationships  of  the  Tritylo- 
dontidae  (Synapsida).  Zoological  Journal  of  the 
Linnean  Society,  85:  205-217. 

Swofford,  D.  L.  1993.  PAUP:  Phylogenetic  Analysis 
Using  Parsimony,  Version  3.1.  Champaign,  Illi- 
nois: computer  software  and  documentation  dis- 
tributed by  Illinois  Natural  History  Survey. 

WlBLE,  J.  R.  1991.  Origin  of  Mammalia:  the  craniod- 
ental  evidence  reexamined.  Journal  of  Vertebrate 
Paleontology,  11:  1-28. 

WlBLE,  J.  R.,  AND  J.  A.  HOPSON.  1995.  Homologies 
of  the  prootic  canal  in  mammals  and  non-mam- 
malian cynodonts.  Journal  of  Vertebrate  Paleon- 
tology, 15:  331-356. 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching        29 


APPENDIX  1:  CHARACTER  LIST 

States  are  denoted  as   (0)    =   primitive 
state;  (1),  (2),  and  (3)  =  derived  states. 

Cranium 

1 .  Premaxilla  forms  posterior  border  in- 
cisive  foramen:    absent   (0),   present 

(1). 

2.  Nasal-lacrimal   contact:    absent    (0), 

present  (1). 

3.  Prefrontal:  present  (0),  absent  (1). 

4.  Postfrontal:  present  (0),  absent  (1). 

5.  Postorbital:  present  (0),  absent  (1). 

6.  Prefrontal-postorbital  contact:   ab- 
sent (0),  present  (1). 

7.  Parietal  foramen:  present  (0),  absent 

(1). 

8.  Vomer  intemarial  shape:  broad  plate 

(0),  parallel-sided  keel  (1). 

9.  Ectopterygoid:   contacts  maxilla  (0), 
does  not  contact  maxilla  (1),  absent 

(2). 

10.  Interpterygoid  vacuity  in  adult  be- 
tween pterygoid  flanges:  present  (0), 
absent  (1). 

11.  Palatal  exposure  of  maxifla  behind 
canine  greater  than  20%  distance 
from  canine  to  posterior  end  of  pal- 
atine: absent  (0),  present  (1). 

12.  Secondary  palatal  plate  on  maxilla: 
absent  (0),  present,  does  not  reach 
midline  (1),  present,  reaches  midline 

(2). 

13.  Secondary  palatal  plate  on  palatine: 
absent  or  low  ridge  (0),  present,  ex- 
tends nearly  to  midline  (1),  present, 
reaches  midline  (2). 

14.  Length  secondary  palate  relative  to 
toothrow:  shorter  (0),  about  equal 
(1),  longer  (2). 

15.  Length  secondary  palate  relative  to 
anterior  border  of  orbit:  shorter  (0), 
about  equal  (1),  longer  (2). 

16.  Teeth  on  pterygoid  flange:  present 
(0),  absent  (1). 

17.  Ventral  surface  of  basisphenoid  de- 
pressed below  occipital  condyles:  less 
than  Va  occipital  height  (0),  greater 
than  Va  occipital  height  (1). 


18.  Zygomatic  arch  dorsoventral  height: 
slender  (0),  moderately  deep  (1), 
very  deep  (2). 

19.  Zygomatic  arch  dorsal  extent:  below 
middle  of  orbit  (0),  above  middle  of 
orbit  (1). 

20.  Jugal  depth  in  zygomatic  arch  rela- 
tive to  exposed  squamosal  depth:  less 
than  twice  (0),  greater  than  twice  (1). 

21.  Jugal  suborbital  process:  absent  (0), 
present  (1). 

22.  Squamosal  groove  for  external  audi- 
tory meatus:  shallow  (0),  moderately 
deep  (1),  very  deep  (2). 

23.  Frontal-palatine  contact  in  orbit:  ab- 
sent (0),  present  (1). 

24.  Tabular  extends  around  posttemporal 
foramen:  absent  (0),  present  (1). 

25.  Descending  flange  of  squamosal  lat- 
eral to  quadratojugal:  absent  (0),  pre- 
sent not  contacting  surangular  (1), 
present  contacting  surangular  (2). 

26.  Internal  carotid  foramina  in  basi- 
sphenoid: present  (0),  absent  (1). 

27.  Groove  on  prootic  extending  from 
pterygoparoccipital  foramen  to  tri- 
geminal foramen:  absent  (0),  present 
and  open  (1),  present  and  enclosed 
as  a  canal  (2). 

28.  Trigeminal  nerve  exit:  between  pro- 
otic  incisure  and  epipterygoid  (0),  via 
foramen  between  prootic  and  epip- 
terygoid (1),  via  two  foramina  (2). 

29.  Quadrate  contact:  primarily  squa- 
mosal   (0),   primarily  crista  parotica 

(1). 

30.  Quadrate  ramus  of  pterygoid:  pre- 
sent (0),  absent  (1). 

31.  Quadrate  posteroventral  process  in 
squamosal  posterior  notch:  absent 
(0),  present  (1). 

32.  Epipteiygoid  ascending  process  at 
level  of  trigeminal  foramen:  rodlike 
(0),  moderately  expanded  (1),  greatly 
expanded  (2). 

33.  Epipterygoid-prootic  overlap:  absent 
(0),  present  (1). 

34.  Lateral  flange  of  prootic:  absent  (0), 
present  (1). 


30        Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


35.  Epipteiygoid— frontal  contact:  absent 
(0),  present  (1). 

36.  Separate  foramina  for  vestibular  and 
cochlear  nerves:  absent  (0),  present 

(1). 

37.  Double  occipital  condyles:  absent 
(0),  present  (1). 

38.  Stapedial  foramen  orientation:  an- 
teroposterior (0),  dorsoventral  (1). 

39.  Greatest  width  of  zygomatic  arches: 
near  middle  of  arch  (0),  at  posterior 
end  of  arch  (1). 

40.  Length  of  palatine  relative  to  maxilla 
in  secondary  palate:  shorter  (0), 
about  equal  (1),  longer  (2). 

41.  Posterolateral  end  of  maxilla:  passes 
obliquely  posterodorsally  into  subor- 
bital bar  (0),  forms  right  angle  ventral 
to  jugal  contact  (1). 

42.  Fenestra  rotunda  separation  from 
jugular  foramen:  confluent  (0),  par- 
tially separated  by  fingerlike  projec- 
tion from  posterolateral  wall  of  jug- 
ular foramen  (1),  completely  separat- 
ed (2). 

43.  V-shaped  notch  separating  lambdoi- 
dal  crest  from  zygomatic  arch:  absent 
(0),  present  (1). 

Lower  Jaw 

44.  Dentaiy  symphysis:  not  fused  (0), 
fused  (1). 

45.  Dentary  masseteric  fossa:  absent  (0), 
high  on  coronoid  region  (1),  extends 
to  lower  border  of  dentary  (2). 

46.  Dentary  overlap  of  dorsal  surface  of 
surangular:  short  (0).  long  (1). 

47.  Dentaiy  coronoid  process  height:  be- 
low middle  of  orbit  (0),  above  middle 
of  orbit  (1). 

48.  Position  of  dentary— surangular  dorsal 
contact  relative  to  postorbital  bar  and 
jaw  joint:  closer  to  postorbital  bar  (0), 
midway  between  (1),  closer  to  jaw 
joint  (2). 

49.  Postdentary  rod  height  relative  to  ex- 
posed length  (distance  between  base 
of  reflected  lamina  and  jaw  joint): 
greater  than  V2  length  (0),  about  Vi 
length  (1),  less  than  V2  length  (2). 


50.  Coronoid  mediolaterally  thickening: 
absent  (0),  present  (1). 

51.  Reflected  lamina  of  angular  posterior 
extent  relative  to  distance  from  angle 
of  dentary  to  jaw  joint:  greater  than 
V2  the  distance  (0),  less  than  V2  the 
distance  (1). 

52.  Reflected  lamina  of  angular  shape: 
deep  corrugated  plate  (0),  spoon- 
shaped  plate  (1),  hook  with  depth 
greater  than  V2  length  (2),  hook  with 
depth  less  than  V2  length  (3). 

Dentition 

53.  Upper  incisor  number:  five  or  more 
(0),  four  (1),  three  (2). 

54.  Lower  incisor  number:  four  or  more 
(0),  three  (1),  two  (2). 

55.  Incisor  cutting  margins:  serrated  (0), 
smoothly  ridged  (1),  denticulated  (2). 

56.  Incisor  size:  all  small  (0),  some  or  all 
enlarged  (1). 

57.  Upper  canine  size:  large  (0),  reduced 
in  size  (1),  absent  (2). 

58.  Lower  canine  size:  large  (0),  reduced 
in  size  (1),  absent  (2). 

59.  Canine  serrations:  present  (0),  absent 

(1). 

60.  Postcanine  shape:  single  point  (0), 
two  or  more  cusps  in  line  (1). 

61.  Upper  postcanine  buccal  cingulum: 
absent  (0),  present  (1). 

62.  Postcanine  lingual  cingulum:  absent 
(0),  narrow  (1),  lingually  expanded 
(2). 

63.  Number  of  upper  cusps  in  transverse 
row:  one  (0),  two  (1),  three  or  more 
(2). 

64.  Position  of  upper  transverse  cusp 
row  on  crown:  on  anterior  half  of 
crown  (0),  midcrown  almost  to  pos- 
terior margin  (1),  at  posterior  margin 
(no  posterior  cingulum)  (2). 

65.  Central  cusp  of  upper  transverse 
row:  absent  (0),  midway  between 
buccal  and  lingual  cusps  (1),  closer  to 
lingual  cusp  (2). 

66.  Longitudinal  shear  surface  of  main 
upper  cusp:    anterior  and  posterior 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching        31 


(to    transverse    ridge)    (0),    posterior 
only  (1),  anterior  only  (2). 

67.  Upper  anterobuccal  accessory  cusp: 
present  (0),  absent  (1). 

68.  Upper  posterobuccal  accessory  cusp: 
present  (0),  absent  (1). 

69.  Upper  anterolingual  accessory  cusp: 
absent  (0),  present  (1). 

70.  Upper  anterior  transverse  (cingulum) 
ridge:  low  (0),  high  (1). 

71.  Upper  lingual  ridge:  absent  (0),  pre- 
sent (1). 

72.  Transverse  axis  of  crown  strongly 
oblique  to  midline  axis:  absent  (0), 
present  (1). 

73.  Number  of  lower  cusps  in  transverse 
row:  one  (0),  two  (1),  three  or  more 
(2). 

74.  Lower  anterior  cingulum  or  cusp:  ab- 
sent (0),  present  (1). 

75.  Lower  posterior  basin:  absent  (0), 
present  (1). 

76.  Widest  lower  cusp  in  transverse  row: 
lingual  (0),  buccal  (1). 

77.  Posterior  portion  maxillary  tooth  row 
inset  from  lateral  margin  of  maxilla 
(cheek  developed):  absent  (0),  pre- 
sent (1). 

78.  Axis  of  posterior  part  of  maxillary 
tooth  row:  directed  lateral  to  subtem- 
poral fossa  (0),  directed  toward  cen- 
ter of  fossa  (1),  directed  toward  me- 
dial rim  of  fossa  (2). 

79.  Posterior  portion  of  maxillary  tooth 
row  extends  medial  to  temporal  fos- 
sa: absent  (0),  present  (1). 

80.  Posteriormost  postcanine(s)  gompho- 
dont:  absent  (0),  present  (1). 

81.  Postcanine  replacement  pattern  in 
adult:  "alternating"  (0),  widely 
spaced  waves  (three  or  more  teetlV 
wave)  (1),  single  wave  (2). 

Postcranium 

82.  Expanded  costal  plates  on  ribs:  ab- 
sent (0),  present  (1). 

83.  Lumbar  costal  plates  with  ridge  over- 
lapping preceding  rib:  absent  (0), 
present  (1). 

84.  Scapula  infraspinous  fossa  with  out- 


turned   anterior   and   posterior  bor- 
ders: absent  (0),  present  (1). 

85.  Acromion  process:  absent  (0),  pre- 
sent (1). 

86.  Scapular  constriction  below  acromi- 
on: absent  (0),  present  (1). 

87.  Scapular  elongation  between  acro- 
mion and  glenoid:  absent  (0),  present 

(1). 

88.  Procoracoid  in  glenoid:  present  (0), 
barely  present  or  absent  (1). 

89.  Procoracoid  contact  with  scapula: 
greater  than  coracoid  contact  (0), 
equal  to  or  less  than  coracoid  contact 

(1). 

90.  Humerus  ectepicondylar  foramen: 
present  (0),  absent  (1). 

91.  Ulna  olecranon  process:  absent  (un- 
ossified)  (0),  present  (1). 

92.  Manual  digit  III  phalanx  number: 
four  (0),  three  (1). 

93.  Manual  digit  IV  phalanx  number:  five 
(0),  four  (1),  three  (2). 

94.  Length  of  anterior  process  of  ilium 
anterior  to  acetabulum  (relative  to 
diameter  of  acetabulum):  less  than 
1.0  (0),  1.0-1.5  (1),  greater  than  1.5 
(2). 

95.  Length  of  posterior  process  of  ilium 
posterior  to  acetabulum:  (relative  to 
diameter  of  acetabulum):  between 
0.5  and  1.0  (0),  greater  than  1.0  (I), 
less  than  0.5  (2). 

96.  Dorsal  profile  of  ilium:  strongly  con- 
vex (0),  flat  to  concave  (1). 

97.  Total  length  of  pubis  relative  to  ace- 
tabulum diameter:  greater  than  1.5 
(0),  between  1.5  and  1.0  (1),  less  than 
1.0  (2). 

98.  Greater  trochanter  separated  from 
femoral  head  by  distinct  notch:  ab- 
sent (0),  present  (1). 

99.  Greater  trochanter  joined  to  femoral 
head   by  ridge:   present   (0),   absent 

(1). 

100.  Lesser  trochanter  position:  on  ven- 
tromedial surface  of  femoral  shaft 
(0),  on  medial  surface  of  femoral 
shaft  (1). 

101.  Vertebral  centra:  amphicoelous  (0), 
platycoelous  (1). 


32         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


APPENDIX  2:    CHARACTER  STATES 
States  are  denoted  as  0  (primitive);  and  1,  2,  or  3  (derived).  ?  =  state  unknown. 


1 

1111111112 

2222222223 

3333333334 

4444444445 

Taxon 

1234567890 

1234567890 

1234567890 

1234567890 

1234567890 

Gorgonopsid 

0000000000 

0007700100 

0000000000 

0000000007 

0000000020 

Lycosuchus 

0000000000 

0007700000 

0000000000 

010000000? 

0000000000 

Ovinia 

0101010010 

1110010000 

0001071100 

1211101100 

0000110000 

Procynosuchus 

0101010010 

1110010000 

0001001100 

1211101100 

0000110000 

Galesaurus 

0101010011 

1110010100 

0101101100 

1211101100 

0000211110 

Thrinaxodon 

0101010111 

1220010100 

0101101100 

1211101100 

0000211110 

Cynognathus 

0101010111 

1220010210 

1201211101 

1211101110 

0001211220 

Diademodon 

0101010171 

1220010211 

1201211201 

1211101110 

0011211220 

Trirachodon 

0101010121 

1220110211 

1201212201 

1211101110 

0011211220 

Pascualgnathus 

7101010121 

1220110211 

1201212201 

1211101110 

0711211220 

Scalenodon  angustifrons 

0101010121 

1220011211 

1201212201 

1211101110 

0111211220 

''Scalenodon"  hirschoni 

0101017121 

1220117711 

7271217701 

1711101170 

0771211220 

Luangwa 

7101010121 

1220717211 

1201212201 

1211101117 

0111211220 

Massetognathus 

1101010121 

1220211211 

0201212201 

1211101110 

0111211220 

Gomphodontosuchus 

7101017121 

122001771? 

7201217701 

1711171170 

0771211220 

Exaeretodon 

7101011121 

1220117210 

1271212201 

1211101110 

0711211220 

Tritylodontidae 

1111101121 

1220211211 

0211112211 

1211111110 

0210211221 

Lumkiiia 

0101011120 

1220110100 

0101201101 

1211101100 

0011211220 

Probainognathus 

1101011121 

1221110100 

0111201101 

1211101100 

0111211220 

Ecteninion 

7101011121 

1220110700 

0111201101 

1211101100 

0711211220 

Probelesodon 

1101011121 

1221210100 

0111201101 

1211101101 

1111211220 

Aleodon 

1101011121 

1222210700 

0111207701 

1711101102 

1771211220 

Chiniquodon 

7101011121 

1222210100 

0111201101 

1211101102 

1711211220 

Pachygenelus 

1111101120 

1222210000 

0011001101 

1211111102 

0210211221 

Mo  rga  n  ucodon 

0111101121 

1222210000 

0017002211 

7111111100 

0210211221 

APPENDIX  3:    SYNAPOMORPHIES  OF 
PRINCIPAL  TAXA  OF  CYNODONTIA 

Numbers  refer  to  characters  in  Appendix 
1.  Numbers  in  parentheses  refer  to  equiv- 
ocal synapomorphies  under  the  Delayed 
Transformation  (DELTRAN)  option  of 
PAUR 

Cynodontia 


2. 
4. 
6. 
9. 

11. 


12. 
13. 


Nasal— lacrimal  contact. 
Rostfrontal  absent. 
Rrefrontal-postorbital  contact. 
Ectopterygoid  does  not  contact  max- 
illa. 

Palatal  exposure  of  maxilla  behind 
canine  greater  than  20%  distance 
from  canine  to  posterior  end  of  pal- 
atine. 

Secondary  palatal  plate  on  maxilla. 
Secondary  palatal  plate  on  palatine. 


27. 


28. 


16.  Teeth  on  pterygoid  flange  absent. 
24.  Tabular    extends    around   posttem- 

poral  foramen. 

Groove  on  prootic  extending  from 

pterygoparoccipital  foramen  to  tri- 
geminal forainen. 

Trigeminal  nerve  exit  via  foramen 

between  prootic  and  epipterygoid. 
31.   Posteroventral  process  on  quadrate 

in  posterior  notch  of  squamosal. 
(32).  Ascending  process  of  epipterygoid 

greatly  expanded. 

Epipterygoid— prootic  overlap. 

Lateral  flange  of  prootic. 

Epipterygoid— frontal  contact. 

Double  occipital  condyles. 

Stapedial   foramen  with   dorsoven- 

tral  orientation. 

Dentaiy    masseteric    fossa    present 

high  on  coronoid  region. 


33. 
34. 
35. 
37. 
38. 

45. 


Probainognathian  Cynodont  From  South  Africa  •  Hop.son  and  Kitching        33 


APPENDIX  2:     EXTENDED 


5555555556 
1234567890 


6666666667 
1234567890 


lllllllllQ 
1234567890 


8888888889 
1234567890 


00000 
00000 
01001 
01001 
02111 
02111 
13110 
1311? 
13111 
1311? 
13110 
13221 
13110 
13112 
13111 
13211 
13221 
13111 
13111 
13111 
13111 
13111 
13111 
13221 
13101 


00000 
00000 
00011 
00011 
00011 
00011 
00001 
000?1 
00001 
000?1 
00001 

11?11 

000?1 
01111 
01111 
10111 
122?1 
00011 
00011 
00001 
000?1 
000?1 
000?1 

mil 

00111 


000?0????? 
000?0????? 
122110???? 
010?00???? 
000?00???? 
010?00???? 
000?00???? 
0221100100 
0221100??0 
0210010100 
1221220000 
0221221010 
1221221010 
1222221000 
0212021011 
0212021111 
0222121?10 
000?00???? 
010?00???? 
0?0?00???? 
000?00???? 
021?00???? 
021?00???? 
110?00???? 
110?00???? 


??000 
??000 
??210 
??010 
??0?0 
??010 
??010 
00110 
00210 
001?1 
00111 
10111 
10111 
10101 
11101 
11101 
1011? 
??010 
??010 
??0?0 
??010 
??110 
??110 
??010 
??010 


?000? 
?000? 
?000? 
?000? 
?0000 
?0000 
?0000 
?0000 
?1100 
01200 
01200 
01201 
01201 
01201 
11201 
11211 
?1211 
?0000 
?0100 
?0000 
?0000 
?0000 
?0000 
?0210 
?0100 


0000000000 
0000000000 
000?0??0?? 
0001000000 
0101000000 
0101000000 
?111100000 
1111107000 
1111100000 
2111110?00 
21???????? 
2????????? 
2101110000 
2101110100 
2????????? 
2001110100 
2001110111 
100117010? 
1001110??? 
970??????? 
7001110100 
1707777  70? 
7701110100 
0001111110 
1001111111 


1 
9999999990 
1234567890 

0000000000 
0120000000 
7771001000 
0011001700 
0011102700 
0011102000 
0121102700 
0121112000 
012  77777?? 
0771112000 
7771772  777 
7777777770 
0772112000 
012211200? 
7777777770 
1122012000 
1122212111 
?????777?? 
0772117000 
????7????? 
0122117000 
77???7777? 
7772117000 
1772212101 
1122212111 


1 
0 
1 


0 
0 
7 

0 
0 
0 
0 
0 
0 
0 
7 
7 
0 
0 
7 

0 
1 
0 
0 
7 

0 
7 

0 

1 
1 


46. 

52. 

55. 

59. 
60. 

74. 

94. 


97. 


Dentary  overlap  of  surangular  long. 
Reflected  lamina  of  angular  spoon- 
shaped  plate. 

Incisor  cutting  margins  smoothly 
ridged. 

Canine  serrations  absent. 
Postcanines  with  two  or  inore  cusps 
in  line. 

Lower  anterior  cingulum  or  cusp 
present. 

Length  anterior  process  of  ilium 
1.0-1.5  times  diameter  of  acetabu- 
lum. 

Length  of  pubis  between  1.5  and 
1.0  times  acetabular  diameter. 


Epicynodontia 

10.    Interpterygoidal  vacuity  between 

pterygoid  flanges  absent  in  adult. 
18.  Zygomatic  arch  moderately  deep. 


22.  Groove  for  external  auditory  meatus 
moderately  deep. 

25.  Descending  flange  of  squamosal  lat- 
eral to  quadratojugal  present. 

45.  Masseteric  fossa  extends  to  lower 
border  of  dentary. 

47.  Coronoid  process  of  dentaiy  ex- 
tends above  middle  of  orbit. 

48.  Dentary-surangular  dorsal  contact 
midway  between  postorbital  bar 
and  jaw  joint. 

49.  Height  of  postdentary  rod  about 
one  half  the  length  of  the  laterally 
exposed  portion  of  the  rod  (distance 
between  base  of  reflected  lamina 
and  jaw  joint). 

52.  Reflected  lamina  of  angular  hook- 
shaped,  with  depth  greater  than  one 
half  its  length. 

53.  Four  upper  incisors. 


34         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


54.  Three  lower  incisors. 

82.   Expanded  plates  on  ribs. 

95.  Lengdi  of  posterior  process  of  ilium 
greater  than  diameter  of  acetabu- 
lum. 

97.  Length  of  pubis  less  than  diameter 
of  acetabulum. 

Eucynodontia 

25.  Descending  flange  of  squamosal  lat- 
eral to  quadratojugal  contacts  sur- 
angular. 

30.  Quadrate  ramus  of  pterygoid  ab- 
sent. 

44.   Dentary  symphysis  fused. 

48.  Dentary-surangular  dorsal  contact 
closer  to  jaw  joint  that  to  postorbital 
bar. 

49.  Height  of  postdentaiy  rod  less  than 
one  half  the  length  of  the  laterally 
exposed  portion  of  the  rod. 

51.  Reflected  lamina  of  angular  less 
than  one  half  the  distance  from  an- 
gle of  the  dentary  to  jaw  joint. 

52.  Reflected  lamina  of  angular  hook- 
shaped,  with  depth  less  than  one 
half  its  length. 

81.  Postcanine  replacement  pattern  of 
widely  spaced  waves  (three  or  more 
teeth  per  wave). 

85.  Acromion  process  on  scapula. 

92.  Manual  digit  III  with  three  phalan- 
ges. 

93.  Manual  digit  IV  with  three  phalan- 
ges. 

Probainognathia 

7.   Parietal  foramen  absent. 
(9).   Ectopterygoid  absent. 
15.   Rear  of  secondary  palate  lies  below 
anterior  border  of  orbit. 
(43).  V-shaped  notch  separates  lambdoi- 
dal  crest  from  zygoma. 

82.  Expanded  plates  on  ribs  absent. 
88.   Procoracoid   barely   present   in    or 

absent  from  glenoid. 

Probainognathia  Minus  Lumkuia 

23.  Frontal  contacts  palatine  in  orbital 
wall. 


Probainognathia  Minus  Lumkuia,  Ectini- 
nion 

(1).   Premaxillae  form  posterior  border 

of  incisive  foramina. 
14.   Secondary   palate    about    equal    in 
length  to  tooth  row. 

(42).  Fenestra  rotunda  partially  separat- 
ed from  jugular  foramen  by  finger 
like  projection. 

(86).  Scapula  constricted  below  acromi- 
on process. 

(94).  Anterior  process  of  ilium  anterior 
to  acetabulum  greater  than  1.5 
times  acetabular  diameter. 

(96).  Dorsal  profile  of  ifium  flat  to  con- 
cave. 

Probainognathus,  Pachygenelus,  and  Mor- 
ganucodon 

62.   Narrow   postcanine   lingual   cingu- 

lum. 
78.  Axis  of  posterior  part  of  maxillary 

tooth  row  directed  toward  center  of 

temporal  fossa. 

Pachygenelus  and  Morganucodon. 

3.   Prefrontal  absent. 

5.  Postorbital  absent. 

6.  Prefrontal-postorbital    contact    ab- 
sent. 

(14).   Secondary  palate  longer  than  tooth- 
row. 
(15).   Secondary  palate  extends  posterior 
to  anterior  border  of  orbit. 

18.  Zygomatic  arch  slender. 

22.   Squamosal  groove  for  external  au- 
ditoiy  meatus  shallow. 

25.    Descending  flange  of  squamosal 
lateral  to  quadratojugal  absent. 

36.   Separate   foramina  in  petrosal  for 
vestibular  and  cochlear  nerves. 

42.   Fenestra  rotunda  completely  sepa- 
rated from  jugular  foramen. 

44.    Dentary  symphysis  not  fused. 

50.   Coronoid  mediolaterally  thickened. 

58.   Lower  canine  reduced  in  size. 

61.   Upper  postcanines  with  buccal  cin- 
gulum. 


Probainognathian  Cynodont  From  South  Africa  •  Hopson  and  Kitching        35 


87.  Scapula   elongated   between   acro- 
mion and  glenoid. 
(89).   Procoracoid    contact   with    scapula 
equal  to  or  less  than  coracoid  con- 
tact. 

91.  Ulnar  olecranon  process  present. 

95.  Posterior  process  on  ilium  less  than 
one  half  diameter  of  acetabulum. 

98.  Greater  trochanter  separated  from 
femoral  head  by  deep  notch. 

100.  Lesser  trochanter   on   medial   sur- 
face of  femoral  shaft. 

101.  Vertebral  centra  platycoelous. 

Chiniquodontidae 

(15).   Secondary  palate  extends  posterior 
to  anterior  border  of  orbit. 
41.   Posterolateral  end  of  maxilla  forms 
right  angle  ventral  to  jugal  contact. 

Cynognathia 

18.  Zygomatic  arch  very  deep. 

19.  Zygomatic  arch  extends  above  mid- 
dle of  orbit. 

21.  Suborbital  process  on  jugal. 

22.  Groove  for  external  auditoiy  mea- 
tus very  deep. 

26.  Basisphenoid  internal  carotid  fo- 
ramina absent. 

39.  Greatest  width  of  zygomatic  arches 
at  posterior  end  of  arch. 

59.  Canine  serrations  present. 

83.  Lumbar  costal  plates  with  ridge 
overlapping  preceding  rib. 

Gomphodontia 

20.  Depth  of  jugal  in  zygomatic  arch 
greater  than  twice  that  of  exposed 
part  of  squamosal. 

28.  Trigeminal  nerve  exit  via  two  fo- 
ramina. 


(43).  V-shaped  notch  separates  lambdoi- 
dal  crest  from  zygoma. 

62.  Upper  postcanine  internal  cingu- 
luin  lingually  expanded. 

63.  Upper  postcanines  with  three  cusps 
in  transverse  row. 

73.   Lower  postcanines  with  two  cusps 
in  transverse  row. 
(96).   Dorsal  profile  of  ilium  flat  to  con- 
cave. 

Traversodonts  (Incl.  Tritylodontidae) 

75.  Posterior  basin  on  lower  postcani- 
nes. 

(78).  Axis  of  posterior  part  of  maxillary 
tooth  row  directed  toward  medial 
rim  of  subtemporal  fossa. 

81.  Adult  postcanine  replacement  pat- 
tern consists  of  single  wave. 

86.  Scapula  constricted  below  acromi- 
on process. 

''Scalenodon"  hirschoni  +  Tritylodontidae. 

(53).  Three  upper  incisors. 

54.  Two  lower  incisors. 
(56).   Some  or  all  incisors  enlarged. 

Gomphodontosuchus  +  Exaeretodon 

63.  Two  cusps  in  transverse  row  on  up- 
per postcanines. 

65.  Central  cusp  of  upper  transverse 
row  absent. 

70.  High  anterior  transverse  ridge  on 
upper  postcanines. 

72.    Transverse     axis     of    postcanine 
crowns  strongly  oblique  to  midline 
axis. 
(74).   Lower  anterior  cingulum  or  cusp 
absent. 

76.  Widest  lower  cusp  in  transverse 
row  buccal. 


ON  MICROCONODON,  A  LATE  TRIASSIC  CYNODONT  FROM  THE 
NEWARK  SUPERGROUP  OF  EASTERN  NORTH  AMERICA 


HANS-DIETER  SUES^ 

Abstract.  Three  incomplete  dentaries  with  teeth 
and  several  isolated  postcanine  teeth  of  a  small  cy- 
nodont  synapsid  from  tlie  Upper  Triassic  (Camian) 
Tomahawk  Member  of  the  Vinita  Fonnation  of  the 
Richmond  basin  (Newark  Supergroup)  in  Virginia  are 
referable  to  Microconodon  tenuirostris  Osbom,  1886. 
This  taxon  was  previously  known  only  from  a  single 
specimen,  an  incomplete  right  dentary  with  four  post- 
canine  teeth  from  the  Upper  Triassic  (Camian)  Cum- 
nock Formation  of  North  Carolina.  Once  considered 
one  of  the  earliest  and  most  primitive  mammals,  Mi- 
crocoiiodon  is  a  derived  eucynodont  of  uncertain  af- 
finities. Its  more  posterior  postcanine  teeth  have 
three  or  four  anteroposteriorly  aligned  cusps,  lack 
cingula,  and  the  roots  of  some  postcanines  are  incip- 
iendy  divided. 

INTRODUCTION 

Emmons  (1857)  named  Dromatherium 
sylvestre  on  the  basis  of  three  small  tooth- 
bearing  jaws  from  Late  Triassic  coals  (ini- 
tially thought  to  be  Permian  in  age)  in  the 
Chatham  coal  field  of  central  North  Car- 
olina. He  interpreted  these  fossils  as  the 
oldest  known  mammalian  remains.  Dro- 
rtiatheriuni  quickly  became  widely  estab- 
lished as  the  first  reputed  American  Me- 
sozoic  mammal  and  as  the  oldest  mammal 
known  at  that  time  (e.g.,  Owen,  1871).  Os- 
bom (1886a)  restudied  two  of  the  jaws;  he 
could  not  trace  the  repository  for  the  third 
specimen  mentioned  by  Emmons,  which 
was  presumed  lost.  Osbom  recognized  the 
distinctive  nature  of  one  of  the  dentaries, 
housed  in  the  collections  of  the  Academy 
of  Natural  Sciences  of  Philadelphia  (ANSP 
10248),  and  made  it  the  holotype  of  a  new 
genus   and   species,   Microconodon  teniii- 


'-  Department  of  Palaeobiology,  Royal  Ontario  Mu- 
seum, 100  Queens  Park,  Toronto,  Ontario  M5S  2C6, 
Canada. 


rostris  (see  also  Osbom,  1886b,  1887).  Un- 
aware of  Osbom  s  work,  Gillette  (1978) 
still  listed  the  holotype  of  M.  tenuirostris 
as  a  "syntype"  of  D.  sylvestre. 

During  his  survey  of  all  Mesozoic  mam- 
mals then  known,  Simpson  (1926a,b)  re- 
examined the  holotypes  of  D.  sylvestre  and 
M.  tenuirostris.  He  removed  both  taxa 
from  the  Mammalia  and  referred  them  to 
the  Cynodontia,  as  had  first  been  suggest- 
ed by  Seeley  (1895).  In  support  of  his  re- 
assessinent,  Simpson  cited  evidence  for 
the  presence  of  more  than  one  bone  in  the 
lower  jaw,  the  undivided  roots  of  the  lower 
postcanine  teeth,  and  the  resemblance  of 
the  crowns  of  these  teeth  to  those  of  cer- 
tain nonmammalian  cynodonts.  The  first 
and  third  features  are  phylogenetically  un- 
informative  because  they  are  plesiomorph- 
ic  features.  The  second  character  is  of 
questionable  significance  because,  as 
Simpson  (1926b)  himself  observed,  the 
roots  of  the  more  posterior  postcanines  in 
the  holotype  of  M.  tenuirostris  are  incipi- 
ently  divided.  Since  Simpson's  redescrip- 
tion,  little  attention  has  been  paid  to  these 
fossils,  although  doubts  concerning  their 
phylogenetic  position  have  persisted  to  the 
present  day.  Hopson  and  Kitching  (1972) 
classified  Dromatherium  and  Microcono- 
don as  Cynodontia  incertae  sedis,  but  ex- 
plicitly noted  possible  mainmalian  affini- 
ties for  both  taxa.  Most  recently,  Hahn  et 
al.  (1994)  placed  both  forms,  together  with 
several  other  problematic  taxa  of  Late  Tri- 
assic nonmammalian  cynodonts  in  a  family 
Dromatheriidae,  which  they  considered 
the  sister-taxon  of  Mainmalia. 

The  holotypes  of  D.  sylvestre  and  M. 


Bull.  Mus.  Comp.  ZooL,  156(1):  37-48,  October,  2001         37 


38         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


tenuirostris  were  collected  from  coal 
seams  near  the  base  of  the  Cumnock  For- 
mation, of  late  Carnian  age  (Litwin  and 
Ash,  1993),  in  a  now  abandoned  mine  near 
Egypt,  Chatham  County,  North  Carolina. 
The  strata  belong  to  the  Sanford  subbasin 
of  the  Deep  River  basin  of  the  Newark 
Supergroup.  Simpson  (1926b)  provided  a 
meticulous  description  of  these  specimens, 
and  little  can  be  added  to  his  account. 
Both  fossils  have  been  adversely  affected 
by  early  attempts  at  preparation  and  con- 
servation. The  holotype  of  D.  sylvestre  was 
originally  housed  in  the  Museum  of  Wil- 
liams College  but  has  recently  been  per- 
manently transferred  to  the  collections  of 
the  National  Museum  of  Natural  History. 
The  postcanine  teeth  of  this  specimen 
have  been  badly  damaged  since  the  time 
of  Simpson  s  study,  and  most  details  of  his 
account  can  no  longer  be  verified.  Dro- 
matheriinn  sylvestre  is  quite  different  from 
M.  tenuirostris  in  most  comparable  fea- 
tures (Simpson,  1926a).  The  holotype  of 
M.  tenuirostris  (ANSP  10248)  holds  fewer 
teeth  than  the  holotype  of  D.  sylvestre,  but 
the  postcanines  of  M.  tenuirostris  are  bet- 
ter presei'ved. 

Three  partial  dentaries  with  teeth  and 
several  isolated  postcanine  teeth  of  a  small 
cynodont  from  the  Tomahawk  Member  of 
the  Vinita  Formation  (Turkey  Branch  For- 
mation sensu  Cornet  and  Olsen  [1990])  in 
the  Richmond  basin  (Newark  Supergroup) 
of  Virginia  (Sues  and  Olsen,  1990;  Sues  et 
al.,  1994)  closely  resemble  the  holotype  of 
M.  tenuirostris  in  all  comparable  charac- 
ters. They  appear  to  be  referable  to  the 
same  taxon  and  exliibit  significant  addi- 
tional anatomical  detail.  The  new  dentaries 
also  represent  different  ontogenetic  stages. 
The  purpose  of  this  paper  is  to  describe 
and  illustrate  this  material  and  to  assess 
the  affinities  of  M.  tenuirostris  within  the 
phylogenetic  framework  provided  by  re- 
cent hypotheses  of  cynodont  interrelation- 
ships (Rowe,  1988;  Battail,  1991;  Hopson, 
1991).  I  will  also  briefly  review  the  status 
of  several  possibly  related  but  poorly 
known  cynodont  taxa  from  the  Upper  Tri- 


Table  1.  Measurements  (in  mm)  for  the  an- 
teroposterior LENGTH  (L)  AND  BUCCOLINGUAL 
WIDTH  (W)  OF  POSTCANINE  (Pc)  TEETH  IN  THE  NEW 
SPECIMENS  REFERRED  TO  MiCROCONODON  TENUIROS- 
TRIS. 


Specimen 

Tooth 

L 

w 

USNM  437637 

PC3 

1.4 

ROM  44300 

PC4 

1.2 

0.65 

PCs 

1.6 

0.65 

Pc, 

1.9 

0.7 

ROM  44301 

PC4 

0.8 

0.3 

PC5 

0.9 

0.4 

Pc, 

1.3 

0.5 

assic  of  central  and  western  Europe  (Hu- 
ene,  1933;  Peyer,  1956;  Clemens,  1980; 
Hahn  et  al.,  1984,  1987,  1994;  Godefroit 
and  Battail,  1997),  New  Mexico  (Lucas 
and  Oakes,  1988),  and  Brazil  (Bonaparte 
and  Barberena,  1975,  2001). 

The  following  abbreviations  for  institu- 
tional names  preceding  catalogue  numbers 
are  used  in  this  paper:  ANSP,  Academy  of 
Natural  Sciences  of  Philadelphia;  ROM, 
Royal  Ontario  Museuin,  Toronto;  USNM, 
National  Museum  of  Natural  History  (for- 
merly United  States  National  Museum), 
Washington,  D.C. 

All  dental  measurements  (Table  1)  were 
made  with  a  graded  ocular  scale  on  a  Ni- 
kon SMZU  stereoscopic  microscope;  each 
measurement  was  repeated  three  times. 

SYSTEMATIC  PALEONTOLOGY 

Monophtjletic  Hierarchy.  Amniota:  Syn- 
apsida:  Therapsida:  Cynodontia: 
Eucynodontia  incertae  sedis. 

Genus  M icroconodon  Osborn,  1886 

Dromatherium  Emmons,  1857:  93  (in  part) 
Microconodon  Osbom,  1886a:  540 
Ttjtthoconiis  Palmer,  1903:  873  (objective  junior  syn- 
onyin) 

Type  Species.  Microconodon  tenuirostris 
Osborn,  1886  (by  monotypy). 

Diagnosis.  Dentary  with  very  slender 
horizontal  ramus.  Angular  region  of  den- 
tary without  distinct  process.  Posterior 
postcanine  teeth  with  three  or  four  an- 
teroposteriorly  aligned  cusps.  Postcanines 


MiCROCONODON  •  Sues  39 


Figure  1.  Microconodon  tenuirostris,  USNM  437637,  left  dentary  (with  splenial  and  attached  symphyseal  fragment  of  right 
dentary)  in  lingual  view.  Scale  bar  =  2  mm.  Abbreviations:  an,  angle  of  dentary;  ar.p,  articular  process  of  dentary;  c,  canine 
alveolus;  co.p,  coronoid  process;  co.r,  coronoid  ridge;  f.sp.,  articular  facet  for  splenial;  g.l,  groove  for  dental  lamina;  i1-3,  alveoli 
for  incisors  1-3;  i1r,  alveolus  for  right  first  incisor;  i.g,  internal  mandibular  groove;  m,  mental  foramen;  p1-8,  postcanine  1-8 
(tooth  or  alveolus);  r,  pit  for  replacement  tooth;  sp,  splenial;  t?,  tooth  fragment. 


without  cingula.  Root  of  some  postcanine 
teeth  constricted,  with  figure-eight  shape 
in  transverse  section. 

Comment.  Pahner  (1903)  regarded  Mi- 
croconodon Osbom,  1886  as  preoccupied 
by  Microconodiis  Traquair,  1877  and  pro- 
posed Tytthoconus  as  a  replacement  name. 
Pahner's  action  is  invalid  under  the  rules 
of  the  International  Code  of  Zoological 
Nomenclature,  and  Tytthoconus  Palmer, 
1903  is  an  objective  junior  synonym  of  Mi- 
croconodon Osbom,  1886. 

Microconodon  tenuirostris  Osbom,  1886 

Dromatherium  sijlvestre  Emmons,  1857:  93  (in  part) 
Microconodon  tenuirostris  Osbom,  1886a:  540 

Holotype.  ANSP  10248,  right  dentary 
with  four  preserved  postcanine  teeth,  lack- 
ing the  articular  process  and  part  of  the 
coronoid  process  (Simpson,  1926b).  The 
specimen  is  preserved  on  a  slab  of  coal, 
and  preservation  of  most  structural  details 
is  indistinct. 

Type  Horizon  and  Locality.  Basal  coals 
of  the  Cumnock  Formation,  Sanford  sub- 
basin  of  the  Deep  River  basin,  Newark  Su- 
pergroup; coal  mine  (now  abandoned)  at 
Egypt,  Chatham  County,  North  Carolina. 
Age:  Late  Triassic  (late  Camian;  Litwin 
and  Ash,  1993). 

Newly      Referred      Material.       USNM 


437637,  incomplete  left  dentary  lacking 
much  of  the  articular  and  coronoid  pro- 
cesses, with  alveoli  for  three  incisors  and 
the  canine,  seven  mostly  broken  postca- 
nine teeth,  and  attached  left  splenial  as 
well  as  fragment  of  the  symphyseal  end  of 
the  right  dentary  (Fig.  1).  ROM  44300,  in- 
complete left  dentary  with  alveoli  for  one 
incisor  and  the  canine,  three  postcanine 
teeth,  and  basal  portions  of  four  postcan- 
ines;  mandibular  symphysis  for  the  most 
part  preserved  only  as  an  impression  (filled 
in  with  epoxy  resin  during  preparation) 
and  posterior  portion  of  dentary  broken 
and  displaced  anterolaterally  (Fig.  2). 
ROM  44301,  anterior  portion  of  right  den- 
tary with  alveolus  for  canine,  five  pre- 
serN^ed  postcanine  teeth,  and  alveoli  for 
three  postcanines  (Fig.  3).  USNM  448579, 
isolated  complete  postcanine  tooth. 
USNM  448600  (Sues  et  al.,  1994,  fig.  8.4) 
and  ROM  44302,  isolated  postcanine  teeth 
with  most  of  the  root  broken  off. 

Horizon  and  Locality  of  Newly  Referred 
Material.  Tomahawk  Member  of  Vinita 
Formation  (Turkey  Branch  Formation  sen- 
sii  Comet  and  Olsen  [1990]),  Richmond 
basin,  Newark  Supergroup;  USNM  locality 
39981,  0.16  km  (0.1  miles)  east  of  the  east- 
em  branch  of  Little  Tomaliawk  Creek 
along  the  former  course  of  VA  652  (Old 


40         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


9  _J3 


Figure  2.  Microconodon  tenuirostris,  ROM  44300,  left  dentary  in  lingual  (top)  and  buccal  (bottom)  views.  Unshaded  areas 
represent  impressions  in  the  matrix  that  were  filled  in  with  colored  epoxy  resin  during  preparation.  Abbreviations  as  in  Figure  1. 
Scale  bar  =  2  mm. 


Hundred  Road),  near  Midlothian,  Ches- 
terfield County,  Virginia.  Latitude 
77°40'17"N,  longitude  37°27'50"W,  Halls- 
boro  7.5  Minute  Quadrangle.  Age:  Late 
Triassic  (late  Carnian  according  to  Lucas 
[1998]). 

Diagnosis.  Type  and  only  known  species 
of  genus,  as  diagnosed  above. 

Discussion.  The  new  material  from  the 


Richmond  basin  closely  resembles  ANSP 
10248,  the  holotype  of  Microconodon  ten- 
uirostris Osbom,  1886,  in  most  compara- 
ble features,  particularly  in  the  structure 
of  the  postcanine  teeth.  The  only  feature 
showing  variation  is  the  course  of  the  in- 
ternal mandibular  groove,  which  ap- 
proaches the  ventral  margin  of  the  dentary 
in  ROM  44301  but  extends  parallel  to  it  in 


Figure  3.  Microconodon  tenuirostris,  ROM  44301,  anterior  portion  of  right  dentary  in  lingual  view.  Unshaded  areas  represent 
impressions  in  the  mathx  that  were  filled  in  with  colored  epoxy  resin  during  preparation.  Abbreviations  as  in  Figure  1.  Scale  bar 
=  2  mm. 


MiCROCONODON  •  Sues        41 


ROM  44300  and  USNM  437637.  This  dif-  teeth.  A  narrow  groove,  which  presumably 

ference  may  be  ontogenetic  in  nature,  and,  housed  the  dental  lamina  in  life  (Cromp- 

in  the  absence  of  other  differences,  I  refer  ton,    1963),   extends   lingually  just   below 

all  specimens  to  the  same  taxon.  and  parallel  to  the  alveolar  margin  and  an- 
teriorly up  to  the  canine  alveolus.  The  in- 

DESCRIPTION  temal  mandibular  groove  (sulcus  primor- 

Dpntarv  dialis)  is  developed  on  the  lingual  surface 

close  to  the  ventral  margin  of  the  horizon- 

The  long  horizontal  ramus  of  the  den-  tal  ramus  of  the  dentary.  This  groove  ex- 

tary  is  slender  throughout  its  entire  length  tends  just  above,  and  anteriorly  approach- 

(Figs.   1-3).  Behind  the  mandibular  sym-  es,  the  ventral  margin  on  the  small  dentary 

physis,   the   alveolar   (dorsal)   and  ventral  ROM   44301    (Fig.   3),   but  its   course  is 

margins  of  the  ramus  are  rather  straight  more  or  less  parallel  to  and  well  above  the 

and  extend  more  or  less  parallel  to  each  margin   in   USNM   437637   (Fig.    1)   and 

other.  The  alveolar  margin  abruptly  rises  ROM  44300  (Fig.  2)  where  it  reaches  the 

toward    the    canine    alveolus    in    USNM  posterior  end  of  the  symphysis.  The  inter- 

437637;  this  rise  is  accompanied  by  a  lat-  nal  groove  forms  the  anterior  continuation 

eral  bulging  of  the  dentary.  Part  of  a  men-  of  the  well-developed  posterior  trough  for 

tal  foramen  is  visible  on  the  lateral  surface  the   reception   of  the  postdentary  bones, 

behind  the  canine  alveolus  in  ROM  44300.  The  angular  region  of  the  dentaiy  does  not 

Anteriorly,  the  ventral  margin  of  the  den-  form   a  distinct  process,   unlike  in   many 

tary  forms  a  slight  projection  below  the  ca-  other  cynodonts;  the  ventral  margin  of  the 

nine  in  ROM  44300  and  USNM  437637  dentary  curves  gently  upward  and  back- 

and  then  curves  forward  and  upward  in  all  ward  toward  the  articular  process.  Lateral 

specimens.  The  dentary  is  gently  convex  to  the  last  postcanine  tooth,  the  low  but 

beneath  the  incisors.  The  ventral  edge  is  anteroposteriorly  broad  coronoid  process 

rounded  and  thickened  back  to  the  region  smoothly  rises  posterodorsally  at  an  angle 

of  the   angle  where   it  becomes   sharper,  of  about  45°  relative  to  the  long  axis  of  the 

The  robust  symphyseal  portion  of  the  den-  dentary.  The  anterior  margin  of  the  pro- 

tary  holds  alveoli  for  a  large  canine  and  cess  forms  a  coronoid  ridge,  which  is  most 

three  apparently  slightly  procumbent  in-  pronounced   anteriorly,   before   it   merges 

cisors.  The  dentaries  are  fused  along  their  into  the  horizontal  ramus.  The  masseteric 

long,     sloping     symphysis.     In     USNM  fossa  is  weakly  defined.  No  distinct  facet 

437637,  a  fragment  of  the  symphyseal  por-  for  the  coronoid  bone  is  apparent  on  the 

tion  of  the  right  dentary,  containing  the  al-  medial  aspect  of  the  coronoid  process  of 

veolus  for  the  first  lower  incisor,  still  ad-  the  dentary.  The  lateral  ridge  on  the  artic- 

heres  to  the   left  element   (Fig.    1).   The  ular  process  of  the  dentaiy  is  expanded, 

mandibular  symphysis  extends  back  to  the  especially  more  posteriorly,  but  there  is  no 

level  of  the  posterior  margin  of  the  alve-  indication  that  it  contributed  to  a  mam- 

olus  for  the  canine.  The  buccal  surface  of  mallike  condyle  posteriorly, 
the  horizontal  ramus  of  the  dentary  is  con- 

vex  dorsoventrally.  A  faint  buccal  groove  i^pieniai 

on  the   horizontal   ramus   of  the   dentary  A  featureless,  elongate-triangular  bone 

ANSP    10248    noted   by   Osbom    (1886b,  in   the   posterior  portion   of  the   internal 

1887)  appears  to  be  the  result  of  postmor-  groove  of  the  dentary  in  USNM  437637 

tern  crushing  and  is  not  present  on  any  of  (Fig.   1)  represents  a  partial  left  splenial. 

the  specimens  from  the  Richmond  basin.  Articular  facets  for  the  splenial  on  the  den- 

The  lingual  surface  of  the  horizontal  ra-  tary  ROM  44300  (Fig.  2)  indicate  that  this 

mus  is  flat  near  its  symphyseal  end  but  be-  bone  may  have  entered  into  the  mandib- 

comes  gently  convex  below  the  postcanine  ular  symphysis  anteriorly. 


42         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Dentition 

The  incisors  and  canine  are  document- 
ed only  by  their  alveoli.  Three  alveoli  for 
incisors  are  present  in  USNM  437637. 
They  indicate  that  the  incisors  were  similar 
in  size  to  each  other  and  that  they  were 
slightly  procumbent.  The  large  alveolus  for 
the  canine  forms  an  elongate  oval  in  out- 
line. The  count  of  three  incisors  and  one 
canine  is  in  agreement  with  Simpson's 
(1926b)  estimate  based  on  a  series  of  de- 
pressions on  the  lateral  aspect  of  the  man- 
dibular symphysis  of  ANSP  10248,  which 
he  correctly  interpreted  as  crushed  alveoli. 

In  occlusal  view^,  the  crowns  of  the  post- 
canine  teeth  are  elliptical  in  outline  and 
buccolingually  narrow  (Sues  et  al.,  1994, 
fig.  8.4).  Those  of  the  tricuspid  and  tetra- 
cuspid  postcanines  are  more  than  twice  as 
long  anteroposteriorly  as  wide  buccolin- 
gually. No  wear  facets  indicative  of  cusp 
contact  resulting  from  tooth-to-tooth  oc- 
clusion are  present.  The  apex  of  the  prin- 
cipal cusp  is  slightly  blunted  by  abrasion 
on  most  teeth.  The  postcanine  teeth  pre- 
served in  situ  confirm  the  anatomical  ori- 
entations for  isolated  tooth  crowns  of  pos- 
sibly related  cynodont  taxa  proposed  by 
Peyer  (1956)  and  Hahn  et  al.  (1984).  In 
buccal  or  lingual  view,  the  slightly  more 
convex  cutting  edge  of  the  principal  cusp 
faces  anteriorly  (mesially);  in  anterior  or 
posterior  view,  the  vertical  curvature  of  the 
buccal  surface  is  slightly  more  convex  than 
that  of  the  lingual  surface. 

The  specimen  USNM  437637  has  seven 
postcanine  tooth  positions  and  ROM 
44300  has  eight  (the  last  alveolus  being  in- 
complete). The  specimen  ROM  44301 
preserves  eight  postcanine  teeth  or  alveoli, 
but  the  posterior  end  of  the  tooth-bearing 
ramus  of  the  dentary  is  not  preserved. 

The  crowns  of  the  anterior  two  postcan- 
ines of  ANSP  10248  and  of  the  anterior 
two  preserved  postcanines  (positions  2  and 
3)  in  ROM  44301  are  simple  cones.  In 
ANSP  10248  they  show  a  slight  posterior 
swelling.  This  single-cusped  type  of  post- 


canine is  absent  in  the  largest  known  spec- 
imen (USNM  437637). 

The  crowns  of  most  of  the  other  post-  n 
canine  teeth  are  tricuspid.  The  only  excep-  II 
tions  in  the  sample  described  here  are  the 
more  posterior  of  the  two  multicuspid  po- 
stcanines preserved  in  ANSP  10248  and 
the  seventh  postcanine  in  ROM  44300, 
both  of  which  have  one  anterior  and  two 
posterior  accessory  cusps.  The  specimen 
ROM  44300  shows  some  differentiation 
among  its  multicuspid  postcanine  teeth: 
compared  to  the  crowns  of  the  sixth  and 
seventh  postcanines,  that  of  the  fourth  is 
shorter  anteroposteriorly  and  taller.  The 
fourth  postcanine  also  has  relatively  small- 
er anterior  and  posterior  accessory  cusps 
that  are  placed  closer  to  the  base  of  the 
crown.  The  crowns  of  the  multicuspid 
postcanines  progressively  increase  in 
length  toward  the  posterior  end  of  the 
tooth  row.  The  buccolingually  narrow 
cusps  are  aligned  behind  one  another  in  a 
straight  line  and  are  clearly  separated  from 
each  other.  The  median  or  principal  cusp 
is  much  larger  than  the  anterior  (mesial)  || 
and  posterior  (distal)  accessory  cusps  and 
dominates  the  tooth  crown.  This  cusp  is 
broad  anteroposteriorly  and  somewhat 
compressed  buccolingually.  The  subequal 
accessory  cusps  are  symmetrically  posi- 
tioned in  front  and  behind  the  principal 
cusp  and  are  separated  from  the  latter  by  I 
distinct  V-shaped  notches.  A  distinct  cut- 
ting edge  extends  down  from  the  apex  of 
the  principal  cusp  along  both  the  anterior 
and  posterior  faces;  the  anterior  cutting 
edge  is  slightly  more  convex  than  the  pos- 
terior one.  Each  accessory  cusp  bears  a 
shaip  cutting  edge  only  on  the  side  facing 
the  central  cusp.  The  accessory  cusps  pro- 
ject slightly  away  from  the  principal  cusp. 
Neither  the  principal  nor  the  accessory 
cusps  are  recurved.  Cingula  are  absent. 
The  enamel  is  completely  smooth  on  most 
teeth.  Fine,  stained  lines  on  the  enamel  of 
the  isolated  postcanine  tooth  USNM 
448579  presumably  represent  postmortem 
fracturing  (see  Hahn  et  al.,  1984).  The  an- 
teroposteriorly broad   and   buccolingually 


MiCROCONODON  •  Sues 


43 


flattened  root  is  not  set  off  from  the  crown 
by  an  annular  constriction.  The  specimen 
USNM  448579  shows  a  pronounced  me- 
dian longitudinal  constriction  of  its  root, 
the  apical  portion  of  which  is  broken.  This 
incipient  division  of  the  root  is  not  evident 
on  any  of  the  teeth  preserved  in  situ  in  the 
referred  dentaries.  However,  this  division 
is  visible  on  the  two  multicuspid  postca- 
nine  teeth  preserved  in  ANSP  10248.  In 
ROM  44300  and  ROM  44301,  a  ring  of 
bone  connects  the  roots  of  at  least  soine 
functional  teeth  to  the  alveolar  margin;  de- 
tails are  not  clearly  visible  for  all  tooth  po- 
sitions. This  ankylosis  is  also  present  in 
basal  eucynodonts  such  as  Thrinaxodon 
(Crompton,  1963). 

In  ROM  44301,  small  pits  for  develop- 
ing replacement  teeth  are  present  in  the 
groove  for  the  dental  lamina  anterolingual 
to  postcanine  positions  4  and  6  and  lingual 
to  tooth  7  (Fig.  3).  Comparison  of  the  four 
known  dentaries  indicates  that  the  simple 
anterior  postcanines  were  lost  without  re- 
placement during  growth,  resulting  in  a 
progressively  longer  diastema  in  larger 
specimens,  as  in  many  nonmammalian  cy- 
nodonts  (Crompton,  1963)  and  in  the 
mammaliamorph  Sinoconodon  (Crompton 
and  Luo,  1993).  However,  in  the  latter, 
new  teeth  are  added  only  at  the  posterior 
end  of  the  postcanine  series.  The  small 
dentaries  ANSP  10248  (length:  16.5  mm) 
and  ROM  44301  (length  of  preserved  por- 
tion: 10.3  mm)  both  lack  a  diastema  be- 
tween the  canine  and  postcanine  teeth, 
and  the  postcanine  tooth  row  begins  im- 
mediately behind  the  canine  position.  On 
the  large  dentary  USNM  437637,  an  ex- 
tensive diastema  separates  the  alveolus  for 
the  canine  from  the  postcanine  teeth  (Fig. 
1);  a  tooth  fragment  attached  to  the  bone 
about  midway  probably  represents  a  dis- 
placed fraginent.  The  configuration  of  the 
tooth  row  is  consistent  with  evidence  from 
the  pattern  of  bone  grain  for  the  imma- 
turity of  ROM  44300  and  ROM  44301 
(Figs.  2,  3);  the  grain  on  the  latter  two 
dentaries  coinprises  fine  longitudinal 
grooves    and   pores    typical    of  immature 


bone  (Enlow,  1969).  The  specimen  USNM 
437637  does  not  show  this  type  of  bone 
grain  although  it  was  almost  identical  in 
length  to  ROM  44300  (estimated  lengths 
of  33  mm  and  34  mm,  respectively).  The 
surface  of  ANSP  10248  is  too  poorly  pre- 
served to  show  details  of  texture. 

DISCUSSION 

Taxa  Possibly  Related  to  Microconodon 

Lees  and  Mills  (1983:  179)  observed 
that  "[m]any  of  the  later  small  carnivorous 
cynodonts  and  early  mammals  had  molars 
consisting,  more  or  less,  of  a  single  main 
cusp,  flattened  bucco-lingually,  with  mesial 
and  distal  cuspules"  [accessoiy  cusps  in 
the  present  paper].  This  statement  aptly 
characterizes  the  postcanine  teeth  of  Mi- 
croconodon. 

Many  isolated  teeth  resembling  those  of 
Microconodon  as  well  as  jaw  fragments 
containing  such  teeth  have  been  reported 
from  the  Upper  Triassic  of  central  and 
western  Europe  (Peyer,  1956;  Clemens, 
1980;  Hahn  et  al,  1984,  1987,  1994;  Sig- 
ogneau-Russell  and  Hahn,  1994;  Godefroit 
and  Battail,  1997)  and  New  Mexico  (Lucas 
and  Oakes,  1988).  These  fossils  have  been 
variously  referred  to  nonmammalian  cy- 
nodonts or  mammals,  but,  in  some  cases, 
even  their  synapsid  affinities  remain  yet  to 
be  established  (see  below).  The  situation 
was  complicated  by  the  discovery  of  tri- 
cuspid teeth  in  the  Late  Triassic  "rham- 
phorhynchoid"  pterosaur  Eiidimorphodon 
(Wfld,  1978),  although  Halm  et  al.  (1984) 
have  provided  structural  criteria  for  distin- 
guishing between  teeth  of  Eiidimorphodon 
and  those  of  nonmammalian  cynodonts. 

Tricuspes  tuebingensis  Huene,  1933 
from  the  Rhaeto— Liassic  bonebed  at  Gais- 
brunnen  (Baden-Wiirttemberg,  Germany) 
as  well  as  Tricuspes  sigogneauae  Hahn  et 
al.,  1994  and  Tricuspes  tapeinodon  Gode- 
froit et  Battail,  1997  from  the  Upper  Tri- 
assic (Norian)  of  Saint-Nicolas-de-Port 
(France)  and  Hallau  (Switzerland)  are 
known  only  from  isolated  postcanine  teeth 
(Clemens,  1980;  Hahn  et  al.,  1994;  God- 


44         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


efroit  and  Battail,  1997).  Clemens  (1980)  cynodont  taxa  based  on  isolated  postcanine 

tentatively  placed  Tricuspes  in  the  Mam-  teeth  recovered  from  a  Rhaetian  bonebed 

malia  whereas  Hahn  et  al.  (1994)  referred  (Sables  de  Mortinsart)  at  Gaume,  southern 

it  to  the  nonmammalian  cynodont  taxon  Belgium:  Lepagia  gauniensis,  Gaumia  lon- 

Dromatheriidae.  The  tricuspid  and  tetra-  giradicata,  and  ?Gaumia  incisa.  They  also 

cuspid  postcanines  of  Tricuspes  closely  re-  referred  some  postcanines  from  the  Hallau 

semble   those   of  Microconodon   in   most  bonebed  to  L.  gaumensis  and  ?G.  incisa. 

features,  including  the  incipient  division  of  Hahn  et  al.  (1987)  assigned  Lepagia  to  the 

the  root.   However,  in  occlusal  view,  the  Chiniquodontidae,  and  Sigogneau-Russell 

apex  of  the  principal  cusp  in  Tricuspes  is  and  Hahn  (1994)  referred  it  to  the  Chi- 

slightly  displaced  so  that  the  cusps  are  ar-  niquodontidae    or    Probainognathidae    on 

ranged  in  a  broadly  V-shaped  pattern.  Fur-  the  basis  of  similarities  in  the  position  and 

thermore,  the  holotype  of  T  tuebingensis,  shape  of  the  splenial  between  Lepagia  and 

which  was  identified  as  a  right  lower  post-  Probainognathus.    However,  the  phyloge- 

canine  by  Clemens  (1980)  and  Godefroit  netic  significance  of  those  features  is  un- 

and  Battail  (1997)  but  as  a  left  lower  post-  certain  (see  Battail,  1991).  Tooth  crowns 

canine  by  Hahn  et  al.  (1994),  bears  an  ac-  of  Lepagia  are  asymmetrical  in  side  view 

cessory  cuspule  (Hahn  et  al.,  1994,  fig.  3,  and  have  a  principal  cusp  and  one  or  two 

m)  in  a  posterobuccal  (according  to  Clem-  anterior    and    posterior    accessory    cusps, 

ens)  or  posterolingual  (according  to  Hahn  Cingula  are  absent.  The  undivided  root  is 

et  al.)  position.  This  cuspule  is  absent  on  separated  from  the  crown  by  a  distinct  an- 

the  teeth  of  T  sigogneauae  and  T  tapei-  nular  constriction.  Hahn  et  al.  (1987)  left 

nodon  from  Saint-Nicolas-de-Port  (Hahn  the  systematic  position  of  Gaumia  unre- 

et  al.,  1994;  Godefroit  and  Battail,  1997).  solved,  and  Sigogneau-Russell  and  Hahn 

Hahn  et  al.  (1984)  named  Pseudotricon-  (1994)  considered  it  a  chiniquodontoid  of 
odon  wildi  on  the  basis  of  isolated  post-  uncertain  affinities.  Teeth  referable  to 
canine  teeth  from  a  mid-Norian  bonebed  Gaumia  are  distinguished  mainly  by  the 
in  Luxembourg.  Some  teeth  referred  to  P.  great  length  of  the  undivided,  distally  ta- 
wildi  have  three  cusps  whereas  others  pering  root,  which  is  set  off  from  the 
have  four  or  five.  The  tooth  crowns  are  crown  by  a  slight  constriction, 
devoid  of  cingula  and  closely  resemble  Lucas  and  Oakes  (1988)  described 
those  of  Microconodon  in  their  overall  ap-  "P.seudotriconodon"  chatterjeei  on  the  ba- 
pearance.  As  in  Microconodon,  the  cusps  sis  of  a  tiny  tooth-bearing  jaw  fragment 
are  aligned  directly  behind  one  another,  and  two  isolated  teeth  from  the  Bull  Can- 
Both  the  principal  and  accessory  cusps  yon  Formation  (Upper  Triassic:  lower  No- 
form  distinct  cutting  edges  anteriorly  and  rian)  of  New  Mexico.  "Pseudotriconodon" 
posteriorly,  unlike  the  condition  in  Micro-  chatterjeei  differs  from  P.  wildi  in  the 
conodon.  Incipient  root  division  appears  to  structure  of  its  teeth,  and  indeed  reference 
be  restricted  to  the  apical  portion  of  the  of  this  material  to  the  Cynodontia  remains 
root  on  some  postcanines  (Hahn  et  al.,  to  be  confirmed  by  additional  specimens. 
1984,  pi.  2,  fig.  6).  As  in  Microconodon,  The  cusps  of  "P."  chatterjeei  bear  numer- 
the  root  is  not  set  off  from  the  crown  by  ous  prominent  vertical  ridges  buccally  and 
an  annular  constriction  (Hahn  et  al.,  1984,  lingually;  similar  striations  are  present  on 
pi.  3,  figs,  la,  2a,  6d).  Pseudotriconodon  the  teeth  of  the  Late  Triassic  pterosaur 
possibly  differs  from  Microconodon  in  that  Eudimorphodon  (Wild,  1978;  Hahn  et  al., 
tetracuspid   and   pentacuspid  postcanines  1984). 

are  as  common  as  or  more  common  than  Therioherpeton  cargnini  from  the  Up- 

tricuspid  teeth  in  the  currently  available  per   Triassic    Santa    Maria    Formation    of 

samples  (Hahn  et  al.,  1984).  southern  Brazil  is  based  on  an  incomplete 

Hahn  et  al.  (1987)  described  three  new  skull    and    a   partial    postcranial    skeleton 


MiCROCONODON  •  Sues        45 


(Bonaparte  and  Barberena,  1975).  Cranial  odon  is  referable  to  the  Eucynodontia  as 

features  shared  with  both  Tritheledontidae  diagnosed  by  Hopson  (1991;  see  also  Mar- 

and  Mammaliaformes  include  the  absence  tinez  et  al.  [1996])  based  on  the  possession 

of  the  prefrontal  and  postorbital  (and  post-  of  the  following  apomorphies:  dentary 

orbital  bar).   The  2ygomatic  arch  is  very  considerably  enlarged  and  fused  mandib- 

slender  along  its  entire  length.  The  post-  ular  symphysis.  Microconodon  also  shares 

canine  teeth  lack  cingula  and  have  four  with  other  eucynodonts  a  splenial  reduced 

cusps  that  are  aligned  directly  behind  one  to  a  slender,  thin  bone  covering  the  inter- 

another  The  root  of  at  least  one  postca-  nal  groove  of  the  dentary  and  postdentary 

nine  shows  a  median  longitudinal  constric-  bones   (articular,   prearticular,   and  suran- 

tion  of  the  anteroposteriorly  broad  root,  gular)  forming  a  rodlike  complex  that  is 

Kemp  (1982)  referred  Therioherpeton  to  lodged  in  a  posterior  trough  on  the  lingual 

the  Tritheledontidae,  but  it  lacks  the  den-  surface  of  the  dentary  (inferred  from  the 

tal  features  diagnostic  for  the  latter  taxon  shape  of  the  trough).   The  material  cur- 

(Gow,  1980;  Shubin  et  al.,  1991).  rently  referable  to  Microconodon  is  insuf- 

Lucas  and  Luo   (1993)   suggested  that  ficient  to  permit  more  precise  determina- 

the  possible  basal  mammaliaform  Adelo-  tion  of  the  phylogenetic  relationships  of 

hasileus  cromptoni,  known  only  from  an  this  taxon. 

isolated  braincase  from  the  Tecovas  Mem-  Hahn  et  al.  (1984)  redefined  Dromath- 
berof  the  Dockum  Formation  (Upper  Tri-  eriidae  Gill,  1872,  to  include  Dromather- 
assic:  upper  Gamian)  of  Texas,  might  iurn,  Microconodon,  Pseudotriconodon, 
prove  referable  to  Microconodon.  How-  and  Therioherpeton.  Battail  (1991)  exclud- 
ever,  in  the  absence  of  associated  jaws  and  ed  Therioherpeton  from  the  Dromatheri- 
(or)  postcanine  teeth,  this  association  re-  idae,  but  hypothesized  a  sister-group  re- 
mains untestable.  lationship  between  the  two  taxa  based  on 

With  the  exception  of  Therioherpeton,  the  shared  absence  of  cingula  on  the  post- 
the  aforementioned  taxa,  including  Micro-  canine  teeth.  However,  Hopson  (1991) 
conodon,  are  poorly  represented  by  skel-  noted  that  cingula  are  also  absent  on  the 
etal  remains.  Although  the  similarity  in  the  postcanines  of  Prohelesodon  from  the 
structure  of  the  postcanine  teeth  in  all  Middle  Triassic  Ghaiiares  Formation  of 
these  forms  may  prove  to  be  phylogeneti-  Argentina,  and  this  character-state  may  ei- 
cally  significant,  it  is  more  prudent  to  con-  ther  diagnose  a  more  inclusive  grouping  or 
sider  them  incertae  sedis  among  the  Eu-  may  have  developed  more  than  once.  In- 
cynodontia  until  more  complete  speci-  deed,  the  distribution  of  cingula  is  appar- 
mens  become  available  for  study.  Therio-  ently  variable  among  derived  cynodont 
herpeton  shares  some  apomorphic  cranial  synapsids:  the  lower  postcanine  teeth  of 
features  with  both  Tritheledontidae  and  the  mammaliamorph  Sinoconodon  have 
Mammaliaformes,  but  the  distribution  of  weakly  developed  posterolingual  cingula 
those  characters  in  other  derived  cyno-  (Grompton  and  Luo,  1993),  whereas  those 
donts  has  yet  to  be  fully  documented.  I  of  the  tritheledontid  Pachygenelus  (Gow, 
believe  that  it  is  premature  to  use  these  1980;  Shubin  et  al.,  1991)  and  the  mam- 
features  to  diagnose  a  family-level  taxon  maliaform  Morganucodon  (Mills,  1971; 
Dromatheriidae,  as  has  been  proposed  by  Grompton  and  Luo,  1993)  have  well-de- 
Hahn  et  al.  (1994).  veloped  fingual  cingula.  Battail  (1991)  pro- 
posed a  clade  incTuding  Dromatheriidae 
Phylogenetic  position  of  Microconodon  ^^d  Therioherpeton,  which  he  placed  as 

Assessing  the  phylogenetic  position  of  the   sister-taxon  of  Tritheledontidae   (and 

Microconodon  is  difficult  because  of  the  possibly  Mammaliaformes)  on  the  basis  of 

very  limited  set  of  character-states  observ-  several  cranial  and  dental  characters.  The 

able  in  the  available  specimens.  Microcon-  former    cannot    be    determined    in    the 


46 


Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


known  material  referable  to  Microcono- 
don.  One  of  the  dental  characters  cited  by 
Battail,  the  more  or  less  oblique  implan- 
tation of  the  postcanine  teeth  relative  to 
the  long  axis  of  the  tooth  row,  is  absent  in 
Microconodon.  Most  recently,  Hahn  et  al. 
(1994)  have  redefined  the  Dromatheriidae 
to  include  Tricuspes  and  Meurthodon  Sig- 
ogneau-Russell  et  Hahn,  1994,  from  the 
Upper  Triassic  of  Saint-Nicolas-de-Port 
(France).  They  also  explicitly  considered 
Dromatheriidae  the  sister-taxon  of  "Mam- 
malia" (Mammaliaformes  sensu  Rowe 
[1988]).  The  currently  available  material  is 
insufficient  for  a  rigorous  test  of  this  in- 
triguing hypothesis. 

The  postcanine  teeth  of  Microconodon, 
Pseudotriconodon,  and  Therioherpeton 
differ  from  those  of  other  nonmammalian 
cynodonts  (Cynognathus,  Frobainogna- 
thus,  Probelesodon,  and  Pachygenelus  as 
well  as  the  sectorial  teeth  of  Diademodon 
and  other  basal  gomphodont  cynodonts)  in 
the  absence  of  the  backward  curvature  of 
the  principal  cusp  and  (with  the  exception 
of  Probelesodon)  in  the  lack  of  cingula. 
They  also  differ  from  the  postcanines  of 
Cynognathus  and  Probelesodon  in  the  ab- 
sence of  serrations  on  the  cutting  edges  of 
individual  cusps.  Furthermore,  the  post- 
canine teeth  of  Microconodon  and  Ther- 
ioheiyeton  share  incipient  division  of  the 
roots,  resulting  in  a  figure-eight  shape  in 
transverse  section.  Although  this  feature  is 
also  present  in  the  tritheledontid  Pachy- 
genelus (Shubin  et  al,  1991),  it  may  well 
prove  diagnostic  for  those  probainognathi- 
an  eucynodonts  closest  to  Tritheledontidae 
+  Mammaliaformes  (Hopson,  personal 
communication ) . 

Microconodon  tenuirostris  is  a  derived 
eucynodont,  but  the  currently  available 
material  does  not  permit  a  more  precise 
placement.  This  uncertainty  also  reflects 
the  still  inadequate  fossil  record  of  small 
cynodonts  from  Mid-  to  Late  Triassic  con- 
tinental strata. 

ACKNOWLEDGMENTS 

I  am  indebted  to  R  A.  Kroehler  (Na- 
tional Museum  of  Natural  History),  P.  E. 


Olsen    (Lamont-Doherty   Earth   Observa- 
tory, Columbia  University),  and  especially 
E.   B.  Sues  for  their  enthusiastic  help  in 
the  field.  W.  W.  Amaral  (Harvard  Univer- 
sity) assisted  in  the  preparation  of  the  new 
specimens  reported  in  this  paper.   E.   R. 
Daeschler  (Academy  of  Natural  Sciences 
of  Philadelphia)  arranged  for  the  extended 
loan  of  the  holotype  of  Microconodon  ten- 
uirostris.  S.  G.  Lucas  (New  Mexico  Mu- 
seum of  Natural  History)  kindly  provided 
a  cast  of  the  holotype  of  '^ Pseudotricono- 
don" chatterjeei  for  comparisons.   D.   M. 
Scott  prepared  the  illustrations  with  her 
customary  skill.  J.  A.  Hopson  (University 
of  Chicago)  and  Z.  Luo  (Carnegie  Muse- 
um of  Natural  History)  offered  construc- 
tive comments  on  a  draft  of  the  manu- 
script.  I  gratefully  acknowledge  financial 
support  from  the  National  Geographic  So- 
ciety (grants  3592-88  and  4232-89),  Na- 
tional   Science    Foundation    (NSF    EAR- 
9016677   to   H.-D.    S.    and   R    E.   Olsen), 
Smithsonian  Institution,  and  the  Natural 
Sciences  and  Engineering  Research  Coun- 
cil  of  Canada.    I   dedicate   this   paper  to 
Fuzz   Crompton   who   introduced   me   to 
nonmammalian   cynodonts    and   who   has 
made  so  many  important  contributions  to 
our  knowledge  of  these  animals  during  his 
long  and  distinguished  career. 

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A  CYNODONT  FROM  THE  UPPER  TRIASSIC  OF  EAST  GREENLAND: 
TOOTH  REPLACEMENT  AND  DOUBLE-ROOTEDNESS 


MICHAEL  D.  SHAPIRO^  AND  PARISH  A.  JENKINS,  JR. 

Abstract.  A  new  genus  and  species  of  cynodont 
from  the  Upper  Triassic  Fleming  Fjord  Formation  of 
East  Greenland  possesses  double-rooted  postcanine 
teeth  and  a  nonaltemate  pattern  of  tooth  replace- 
ment. The  specimen  represents  an  addition  to  the 
known  diversity  of  Early  Mesozoic  taxa  with  multi- 
rooted dentitions  (tritylodontids,  Sinoconodon  sp., 
haramiyids,  morganucodontids,  Meurthodon  galli- 
cus),  and  casts  doubt  on  traditional  interpretations  of 
the  interdependency  of  reduced  tooth  replacement 
patterns  and  teeth  with  multiple  roots. 

INTRODUCTION 

The  Upper  Triassic  Fleming  Fjord  For- 
mation of  Jameson  Land,  East  Greenland, 
preserves  a  diverse  fossil  vertebrate  fauna 
that  includes  mammals,  theropod  and  pro- 
sauropod  dinosaurs,  plagiosaurid  and  cy- 
clotosaurid  amphibians,  turtles,  aetosaurs, 
phytosaurs,  and  pterosaurs  (Jenkins  et  al., 
1994,  2001).  Mainmals  are  represented 
primarily  from  the  upper  Tait  Bjerg  Beds 
and  include  Kuehneotlieriuin,  cf  Brachij- 
zostrodon,  and  the  haramiyid  Haramijavia 
clemmenseni  (Jenkins  et  al.,  1994,  1997). 
We  describe  here  an  additional  compo- 
nent of  the  fauna,  a  cynodont  that  bears 
double-rooted  teeth,  the  only  known  spec- 
imen of  this  taxon.  A  comparable  form  of 
Late  Triassic  age  is  Meurthodon  gallicus 
(Russell  et  al.,  1976;  Sigogneau-Russell 
and  Hahn,  1994;  Godefroit  and  Battail, 
1997),  represented  by  isolated  teeth  from 
Rhaetic  deposits  in  France,  but  this  taxon 
differs  in  significant  details. 

The  following  abbreviations  of  institu- 
tional  names   are   used:    IRSNB,    Institut 


royal  des  Sciences  naturelles  de  Belgique, 
Brussels;  MCZ,  Museum  of  Comparative 
Zoology,  HaiA/ard  University,  Cambridge, 
Massachusetts;  MGUH,  Geological  Mu- 
seum, University  of  Copenhagen;  and 
MNHP,  Institut  de  Paleontologie,  Muse- 
um National  d'Histoire  Naturelle,  Paris. 

SYSTEMATIC  PALEONTOLOGY 
Order  Therapsida  Broom,  1905 
Infraorder  Cynodontia  Owen,  1861 


'  Department  of  Organismic  and  Evolutionary  Bi- 
ology, and  Museum  of  Comparative  Zoology,  Harvard 
University,  Cambridge,  Massachusetts  02138. 


Family  incertae  sedis 

Mitredon  cromptoni  new  genus  and 
species 

Etymology.  The  generic  term  refers  to 
the  highly  peaked  primaiy  cusps,  a  com- 
bination of  English  mitre,  the  high-peaked 
ecclesiastical  headdress,  from  Greek  mitra, 
turban,  and  Greek  odous  {odon),  tooth. 
The  specific  name  honors  A.  W.  Crompton 
for  his  important  contributions  to  our  un- 
derstanding of  the  paleobiology  and  evo- 
lution of  c)Tiodonts. 

Holotijpe.  MGUH  VP  3392,  MCZ  field 
number  11/G95  (Figs.  lA,  B),  a  partial  left 
dentary  bearing  an  incomplete  alveolus 
mesially,  three  unerupted  postcanine 
teeth,  roots  of  four  other  (erupted)  po- 
stcanines,  and  an  empty  tooth  ciypt  dis- 
tally 

Horizon.  Uppermost  dolostone  of  Tait 
Bjerg  Beds,  0rsted  Dal  Member  of  the 
Fleming  Fjord  Formation. 

Locality.  71°32.929'N,  22°55.450'W, 
north  of  y^renprisdal  at  its  confluence 
with  Pingel  Dal,  Jameson  Land,  East 
Greenland. 


Bull.  Mus.  Comp.  Zool.,  156(1):  49-58,  October,  2001         49 


50         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


A 


2  mm 


Figure  1.  Left  dentary  of  Mitredon  cromptoni,  MGUH  VP  3392,  in  (A)  lingual  view  and  (B)  occlusolabial  view.  In  occlusolabial 
view,  tfie  mandibular  canal  is  visible  distally  as  a  filled  cast  through  a  window  cut  in  the  labial  aspect  of  the  jaw;  the  canal 
obscures  the  basal  crown  of  Pc„. 


Age.  Late  Triassic  (PNorian— Rhaetic; 
Jenkins  et  al.,  1994). 

Diagnosis.  Cingular  cusps  on  postcanine 
teeth  absent  or  lost,  a  derived  character 
shared  with  galesaurid  cynodonts,  Ci/nog- 
nathiis,  and  Frobelesodon  (Hopson  and 
Kitching,  1972;  Hopson  and  Barghusen, 
1986).  Differs  from  Therioherpetidae 
(Bonaparte  and  Barberena,  1975)  and  oth- 
er nonmanimalian  cynodonts  in  possessing 
bifurcate  postcanine  tooth  roots  (hkely 
convergent  with  multirooted  tritylodon- 
tids)  and  lacking  alternate  tooth  replace- 
ment. Characters  shared  with  "chiniquo- 
donts"   are   crowns   of  lower  postcanines 


with  laterally  compressed  cusps  arranged 
in  a  longitudinal  row  and  clearly  separated 
from  each  other  (Bonaparte  and  Barber- 
ena, 1975;  Sigogneau-Russell  and  Hahn, 
1994).  A  feature  shared  with  Meui-thodon 
gallicus  (Russell  et  al.,  1976;  Sigogneau- 
Russell  and  Hahn,  1994)  and  some  "chi- 
niquodonts"  (Kemp,  1982)  is  a  recuived 
cusp  a  (following  the  nomenclature  of 
Crompton  and  Jenkins,  1968);  that  is,  the 
mesial  crest  is  longer  and  more  horizontal 
than  the  distal  crest,  which  is  shorter  and 
more  vertically  oriented.  A  derived  feature 
shared  with  Meurthodon,  Sinoconodon, 
and  Mammaliaformes  (sensu  Wible,  1991) 


Tooth  Replacement  and  Double-Rootedness  •  Shapiro  and  Jenkins        51 


B 


MGUH  VP  3392 


MNHPSNP1W 


MNHPSNP210W 


D 


IRSNBR163 


aligned  at  "gumline" 


aligned  at  cusps 


Figure  2.  Comparison  between  (A)  PCs  of  Mitredon  cromptoni,  MGUH  VP  3392,  (B)  tlie  type  specimen  of  Meurthodon  gallicus, 
and  (C,  D)  two  isolated  teeth  referred  to  Meurthodon  gallicus.  Specimens  MNHP  SNP210W  and  IRSNB  R163  were  selected  for 
comparison  in  addition  to  ihe  type  specimen  for  their  gross  similarity  to  MGUH  VP  3392.  In  each  column  (B,  0,  and  D),  a 
Meurthodon  tooth  (shaded)  is  compared  to  PCs  of  Mitredon  (outline)  in  two  ways  to  minimize  the  effects  of  size  and  completeness 
on  morphologic  comparison  between  specimens.  First,  the  middle  row  depicts  comparisons  based  on  alignment  of  two  teeth  at 
the  inferred  gumline.  Second,  in  the  bottom  row,  cusps  are  aligned  as  closely  as  possible.  Although  the  alignment  of  MGUH  VP 
3392  at  the  "gumline"  with  IRSNP  R163  and  with  the  cusps  of  MNHP  SNP1W  reveal  overall  similarities  in  shape,  all  specimens 
referred  to  Meurthodon  lack  a  cusp  e.  Cusp  b  of  PCj  in  Mitredon  is  also  substantially  smaller  than  the  corresponding  structure 
in  Meurthodon.  Cusp  designations  in  (A)  after  Crompton  and  Jenkins  (1968).  MNHP  SNP1W  redrawn  from  Sigogneau-Russell 
and  Hahn  (1994);  MNHP  SNP210W  and  IRSNB  R163  redrawn  from  Godefroit  and  Battail  (1997).  For  top  row,  scale  bar  = 
1  mm. 


is  roots  of  lower  postcanine  teeth  bifur- 
cate, a  character  once  considered  diagnos- 
tic of  Mammalia  (e.g.,  Crompton  and  Jen- 
kins, 1979).  Distinguished  from  M.  gallicus 
by  the  presence  of  a  cuspule  mesial  to 
cusp  b  (on  Pcj);  a  mesiodistally  longer  cusp 
a  (if  the  type  specimen  of  M.  gallicus  and 
Pcg  o£  Mitredon  cromptoni,  new  genus  and 
species,  are  scaled  to  the  same  mesiodistal 
length  at  the  crown— cervical  junction,  the 
mesiodistal  length  of  cusp  a  is  approxi- 
mately 60%  total  mesiodistal  crown  length 


in  the  latter,  and  only  40%  in  the  former; 
Fig.  2);  and  the  absolute  mesiodistal 
length  of  Pc,  is  20%  smaller  than  that  of 
the  type  specimen  of  M.  gallicus  (3.5  mm 
versus  4.2  mm).  None  of  the  three  lower 
teeth  of  MGUH  VP  3392  closely  resem- 
bles the  single  isolated  tooth  of  the  type 
specimen  of  M.  gallicus  (Russell  et  al., 
1976;  Signoneau-Russell  and  Hahn,  1994) 
nor  other  isolated  teeth  that  Godefroit  and 
Battail  (1997)  subsequently  referred  to 
that  taxon  (Fig.  2). 


52         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


A 


_,(PC,)     PC,      PC,      PC,      PC3       PC,       PC, 


m.ca 


B 


1  cm 


Figure  3.  Mitredon  cromptoni  and  contemporaneous  Greenlandic  mammals.  (A)  Schematic  reconstruction  of  the  left  lower  jaw 
of  Mitredon  cromptoni,  MGUH  VP  3392.  Lower  jaws  of  the  Late  Triassic  mammals  (B)  Haramiyavia  (redrawn  from  Jenkins  et 
al.  [1997])  and  (C)  Morganucodon  (redrawn  from  Hopson  [1994],  in  Bonaparte  and  Crompton  [1994]).  Abbreviations:  Pc,  post- 
canine  tooth;  i.gr,  internal  dentary  groove;  f.me,  mental  foramen;  m.ca,  mandibular  canal. 


DESCRIPTION 

Lower  Jaw 

The  specimen  is  a  partial  left  dentary, 
slightly  convex  along  its  ventral  margin, 
and  missing  the  anterior  and  posterior 
ends  of  the  ramus;  erupted  teeth  had  bro- 
ken off  postinortem,  but  several  unerupt- 
ed  teeth  are  preserved  within  the  ramus. 
Although  the  total  number  of  postcanine 
teeth  is  uncertain,  the  seven  tooth  posi- 
tions are  here  referred  to  as  Pcj  (most  me- 
sial) through  Pcy  (most  distal)  (Fig.  3).  The 
mental  foramen  is  situated  ventral  and  la- 


bial to  Pc2.  An  internal  groove  extends  lon- 
gitudinally along  the  inferior,  lingual  as- 
pect of  the  dentaiy,  indicating  the  pres- 
ence of  postdentary  bones.  The  mandibu- 
lar canal  is  exposed  through  breakage  on 
the  lingual  aspect  of  the  jaw  between  Pc, 
and  PC4  (Fig.  lA).  The  canal  passes  to  the 
labial  side  of  Pcg  and  is  preserved  in  cross 
section  at  the  break  across  the  posterior 
end  of  the  specimen  (Fig.  IB). 

Teeth 

Lower  postcanine   1   is  indicated  by  a 
partially  preserved  alveolus.   In   the  next 


Tooth  Replacement  and  Double-Rootedness  •  Shapiro  and  Jenkins        53 


tooth  position,  Pcj,  is  an  unerupted  tooth  bears  an  elongate,  tapered  cusp  a,  the  apex 
of  which  the  apex  of  cusp  a  and  most  of  of  which  is  directed  between  the  roots  of 
the  hngual  half  of  the  crown  are  preserved;  the  predecessor  tooth  (Fig.  3).  Cusp  c  is 
the  apex  of  cusp  a  abuts  a  root  fragment  rounded  and  without  a  pointed  apex,  un- 
of  the  eiaipted  tooth  that  was  in  the  pro-  like  the  other  c  cusps  preserved  in  this 
cess  of  being  replaced.  Cusp  a  is  laterally  specimen.  Much  of  this  cusp  lies  on  the 
compressed  and,  unlike  the  recurved,  lingual  side  of  the  mandibular  canal  and  is 
asymmetrical  cusp  a  of  the  unerupted  best  observed  occlusolabially.  Lower  post- 
tooth  at  PC5,  appears  to  be  nearly  sym-  canine  6  is  smaller  than  Pcj  (Fig.  3),  sug- 
metrical.  Two  successively  smaller  cusps  gesting  that  Pcr  inay  be  the  ultimate  tooth 
lie  distal  to  cusp  a;  their  apices  are  direct-  in  die  lower  dentition;  however,  a  cryptlike 
ed  slightly  distally,  comparable  to  the  distal  depression  distal  to  Pc^,  as  well  as  an  anal- 
cusps  of  Pc,  but  unlike  the  strictly  dorsally  ysis  of  tooth  replacement,  appears  to  in- 
directed  orientation  of  cusp  a.  The  mesial  dicate  that  a  more  distal  tooth  position 
end  of  the  tooth  is  not  presei^ved  and  (Pcj)  may  have  been  present, 
therefore  the  presence  or  absence  of  me- 
sial cusps  is  not  possible  to  determine.  The  DISCUSSION 

remains  of  the  crown  of  Pc,  are  sufficient  phy|ogenetic  Affinities 

to  determme  tliat  tlie  tooth  is  moi"pliolog- 

ically  distinct  from  those  at  Pc,  and  Pcg,  Based  on  dental  morphology,  Mitredon 


the  only  other  intact  teeth  in  the  jaw.  croniptoni  is  likely  to  be  closely  related  to 
Lower  postcanine  3  and  PC4  are  fully  Meiirthodon  gallicus.  Although  Sigogneau- 
erupted  teeth,  but  the  crowns  are  lost  and  Russell  and  Hahn  (1994)  interpreted  M. 
only  the  roots  remain.  gallicus  is  most  closely  related  to  Therioh- 
Lower  postcanine  5,  in  the  process  of  erpeton  cargnini,  we  believe  that  M. 
erupting  from  its  crypt,  was  exposed  by  crotnptoni  should  be  excluded  from  the 
preparation  (Figs.  lA,  B).  The  tooth  con-  Therioherpetidae  (as  originally  diagnosed 
sists  of  a  nearly  complete  crown  bearing  by  Bonaparte  and  Barberena,  1975)  on  the 
five  cusps,  and  the  upper  parts  of  two  basis  of  the  bifurcate  postcanine  tooth 
roots.  Mesial  cusps  b  and  e  are  the  smallest  roots  and  the  nonalternate  pattern  of  tooth 
and  cusp  a  is  the  largest,  the  latter  rising  replacement  (but  see  below  discussion  of 
2.55  mm  from  the  base  of  the  crown  to  root  variability  in  early  Mesozoic  cyno- 
the  point  at  which  the  apex  is  broken,  donts).  Inasmuch  as  M.  gallicus  also  has 
Cusps  c  and  d  are  successively  smaller  and  fully  bifurcate  postcanine  tooth  roots  (un- 
more  distally  directed  than  a.  Cusp  d  sup-  like  the  incipiently  double-rooted  condi- 
ports  a  distinct  cuspule  on  its  lingual  sur-  tion  of  T!  cargnini,  in  which  the  cross  sec- 
face;  in  an  examination  of  a  cast  of  Meur-  tion  of  the  single  root  is  in  the  shape  of  a 
thodon  gallicus,  J.  A.  Hopson  (personal  figure  8;  Bonaparte  and  Barberena,  1975), 
communication)  observed  a  "very  faint  the  inclusion  of  this  taxon  in  the  Therioh- 
swelling"  in  a  similar  position.  erpetidae  is  questionable  as  well. 

Both   a   functional   and   a   replacement  Mitredon   cromptoni   might  be  consid- 

tooth  are  present  at  the  Pc^  position.  The  ered  a  chiniquodontid  cynodont,  but  un- 

functional  tooth  is  preserved  only  by  a  pair  resolved  taxonomic  issues  at  the  familial 

of  roots  that  straddle  cusp  a  of  a  replac-  and  suprafamilial  levels,  as  well  as  the  in- 

ment    tooth    beneath.    The    fully   divided  completeness    of  the    present    specimen, 

roots  are  visible  as  ovoid  cross  sections  at  make    such    an    assignment    problematic, 

their  broken  surfaces  in  occlusal  view.  The  Most  taxa  referred  to  "chiniquodonts" 

replacement  tooth,  ex-posed  by  preparation  (Chiniquodontidae  or  Chiniquodontoidea) 

but  partially  obscured  in  labial  view  by  a  exhibit   alternate   tooth    replacement   and 

cast   of  the   mandibular  canal   (Fig.    IB),  postcanines  with  three  to  four  cusps  that 


54         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


--.  (PC,) 


1  cm 


Figure  4.  Schematic  reconstruction  of  the  left  lower  jaw  of  Mitredon  cromptoni,  MGUH  VP  3392.  Most  reptiles  and  many 
cynodonts  exhibit  a  tooth  replacement  pattern  characterized  by  tooth  eruption  in  every  second  tooth  position.  This  alternate 
replacement  pattern  results  from  narrow  spacing  between  Zahnreihen  (teeth  in  a  developmental  replacement  series;  Hopson, 
1980).  As  spacing  between  Zahnreihen  increases,  two  or  more  teeth  in  a  single  Zahnreihe  may  be  fully  erupted  and  functional 
in  the  tooth  row.  Each  tooth  in  a  single  Zahnreihe  potentially  may  have  a  different  crown  morphology,  and  thus  increased  spacing 
between  Zahnreihen  may  yield  a  heterogeneous  tooth  row.  The  dentition  of  M.  cromptoni  is  represented  by  three  Zahnreihen 
(heavy,  shaded  lines).  The  first  Zahnreihe  is  comprised  of  erupting  PCa  and  probably  Pc,  (represented  by  an  empty  alveolus). 
The  second  is  comprised  of  the  erupted  PC2  (root  fragment),  functional  PCj  and  PC4  (pairs  of  roots),  and  erupting  PCj  and  PCe. 
The  roots  of  PCg  are  part  of  the  most  distal  Zahnreihe. 


are  labiolingually  coinpressed  and  inesio- 
distally  aligned,  features  that  are  either 
primitive  for  cynodonts  or  widely  distrib- 
uted (e.g.,  in  galesaurids  and  cynognathids; 
Bonaparte  and  Barberena,  1975).  Al- 
though Sigogneau-Russell  and  Hahn 
(1994:  204)  assert  that  the  teeth  of  "chi- 
niquodonts"  are  easily  distinguished  from 
those  of  mainmals  and  other  therapsids, 
they  also  note  that  "chiniquodont"  denti- 
tions have  yet  to  be  studied  in  depth  and 
therefore  the  "problem  of  subdivision  of 
the  Chiniquodontoidea  into  families  has 
yet  to  be  resolved." 

Mitredon  cromptoni  also  shares  some 
similarities  with  the  Early  Jurassic  Sino- 
conodon,  which  also  has  double-rooted 
teeth  and  likely  replaced  the  molariform 
teeth  (Crompton  and  Sun,  1985;  Cromp- 
ton  and  Luo,  1993).  The  postcanine  teeth 
of  Sinoconodon,  which  have  four  mesio- 
distally  aligned  cusps,  resemble  the  teeth 
of  M.  cromptoni  in  lateral  profile.  In  Sin- 
oconodon postcanine  teeth  do  not  occlude, 
nor  do  upper  and  lower  postcanines  have 
a  consistent  relationship  to  one  another; 
the    single    jaw    of   M.    cromptoni,    from 


which  the  erupted,  functional  teeth  have 
been  lost  postmortem,  does  not  permit  an 
assessment  of  these  features.  In  view  of 
these  uncertainties,  we  are  reluctant  to  at- 
tempt a  more  precise  taxonomic  place- 
ment of  M.  cromptoni. 

Tooth  Replacement 

Mitredon  cromptoni  possesses  a  lower 
postcanine  dentition  with  at  least  three 
variants  of  crowii  stioicture.  Differences  in 
the  teeth  of  M.  cromptoni  appear  to  rep- 
resent different  tooth  replacement  fami- 
lies, or  Zahnreihen,  comparable  to  those 
described  for  the  cynodont  Thrinaxodon 
liorhinus  (Parrington,  1936;  Crompton, 
1963c;  Osborn  and  Crompton,  1973;  Fig. 
4).  However,  tooth  replacement  in  M. 
cromptoni  is  not  comparable  to  the  alter- 
nate pattern  seen  in  T.  liorhinus  and  allied 
forms.  Furthermore,  new  generations  of 
teeth  erupt  in  the  same  sagittal  plane  as 
do  previous  ones  (Pc^  and  Pcv-  eiiipt  di- 
rectly below  the  intact  roots  of  preceding 
teeth;  Figs.  1,  4),  not  in  a  more  lingual 
plane  as  in  T.  liorhinus. 

Although  the  number  of  crown  variants 


Tooth  Replacement  and  Double-Rootedness  •  Shapiro  and  Jenkins       55 


in  each  replacement  series  cannot  be  de- 
tennined,  we  would  interpret  tooth  re- 
placement and  variation  in  Mitredon 
cromptoni  as  representing  three  ZaJinreihe 
(Fig.  4).  The  most  mesial  Zahnreihe  con- 
sists of  Pci  and  the  erupting  Pc^.  The  next 
Zahnreihe  begins  mesially  with  the  root 
remnant  of  the  functional  tooth  at  the  Pco 
position.  The  functional  teeth  at  positions 
Pcr^  (represented  only  by  roots)  are  part 
of  this  second  Zahnreihe,  as  probably  also 
are  tlie  replacement  teetli  at  positions  Pc5_6. 
The  last  tooth  in  the  most  distal  Zahnreihe 
(and  thus  the  most  distal  tooth  in  the  den- 
tition) always  eiiapts  de  novo,  in  a  position 
not  previously  occupied  by  another  tooth. 
Lower  postcanine  6,  which  is  undergoing 
replacement,  therefore  cannot  be  the  ul- 
timate tooth  in  the  lower  dentition  of  M. 
cromptoni  and  we  would  expect  to  see  an- 
other erupting  distal  tooth  in  a  more  com- 
plete (and  perhaps  ontogenetically  older) 
speciinen.  Indeed,  a  shallow  ciypt  occurs 
distal  to  the  roots  of  the  functional  tooth 
at  PCfj,  evidence  of  yet  another  tooth  po- 
sition. The  erupted  Pcg  and  the  potential 
tooth  distal  to  it  represent  the  most  distal 
Zahnreihe. 

Functional  Stability  of  the  Tooth  Row  and 
Multirooted  Teeth 

Before  the  discovery  of  Mitredon 
cromptoni,  the  fossil  record  appeared  to 
provide  evidence  for  the  coevolution  of 
stable  patterns  of  occlusion  and  multiroot- 
ed teeth,  with  the  possible  implication  of 
a  functional  relationship.  In  the  primitive 
condition,  exemplified  by  Thrinaxodon 
and  many  other  cynodonts,  alternate  re- 
placement of  single-rooted  teeth  resulted 
in  continual  disruption  of  the  tooth  row, 
and  in  any  case  there  was  little,  if  any,  oc- 
clusion in  the  strict  sense  (tooth-to-tooth 
contact).  More  derived  lineages  (e.g.,  tri- 
tylodontids,  Sinoconodon,  morganucodon- 
tids,  and  haramiyids)  developed  replace- 
ment strategies  to  promote  stability  of  the 
tooth  row  and,  in  most  cases,  possessed 
double-  or  multirooted  postcanine  teeth. 
An  exception  is  the  gomphodont  cynodont 


Diademodon,  which  maintained  single- 
rooted  teeth  but  promoted  stabilit)'  within 
the  tooth  row  by  losing  teeth  mesially  and 
adding  teeth  distally  (Crompton,  1963a; 
Hopson,  1971).  Tritylodontids  (with  up  to 
six  roots  on  postcanine  teeth  in  Oligoky- 
phiis)  and  Sinoconodon  (in  which  postcan- 
ines  may  be  single-  or  double-rooted)  pos- 
sessed tooth  replacement  patterns  com- 
parable to  that  of  Diademodon,  but  with  a 
reduced  number  of  teeth  in  each  Zahn- 
reihe. Tritylodontids  did  not  replace  mesial 
teeth  but  instead  added  nonreplacing, 
"gomphodont"  teeth  de  novo  at  the  distal 
end  of  the  row  (Hopson,  1971).  Similarly, 
Sinoconodon  lost  anterior  postcanines  and 
added  sinall  distal  teeth,  which  were  sub- 
sequently replaced  by  a  second  generation 
of  larger  ones  as  jaw  size  increased 
(Crompton  and  Luo,  1993).  Thus,  Sino- 
conodon neither  followed  the  typical 
"mammalian"  diphyodont  tooth  replace- 
ment pattern  nor  possessed  true  molars 
(that  is,  Sinoconodon  did  not  bear  teeth 
that  erupted  de  novo  distally  in  the  tooth 
row  and  were  not  replaced  by  subsequent 
generations  of  teeth). 

Morganucodon  was  among  the  first 
inammals  to  possess  a  dentition  that  in- 
cluded true  molars.  Available  fossils  do  not 
reveal  how  many  times  (or  in  what  order) 
Morganucodon  replaced  generations  of 
deciduous  teeth,  but  dental  wear  patterns 
suggest  that  the  positional  relationships 
between  upper  and  lower  postcanine  teeth 
were  relatively  consistent  (Crompton  and 
Jenkins,  1968).  Fixed  dental  relationships 
were  also  promoted  by  interlocking  ante- 
rior and  posterior  accessory  cusps,  main- 
taining alignment  of  the  molars.  Similarly, 
the  occlusal  interlocking  of  cusps  and  ba- 
sins on  upper  and  lower  molariforms  of 
the  haramiyid  Haramiyavia  clemmenseni 
(Jenkins  et  al.,  1997)  would  have  required 
ontogenetic  stasis  of  the  tooth  row.  Al- 
though the  exact  sequence  of  tooth  re- 
placement cannot  be  ascertained  for  either 
of  these  mammalian  taxa,  their  occlusal 
configurations  are  evidence  that  relatively 
precise  relations  were  maintained  between 


56         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


upper  and  lower  dentitions  throughout  on-  dence  that  this  character  evolved  indepen- 
togeny.  dently  more  times  than  previously  recog- 
However,  Mitredon  cromptoni  has  a  nized.  In  Morganiicodon  and  Ktiehneoth- 
double-rooted  postcanine  dentition  but  erium,  premolar  and  molar  roots  range 
lacks  ontogenetic  stasis  in  the  lower  tooth  from  incompletely  divided  to  widely  diver- 
row.  The  tooth  replacement  pattern  of  M.  gent;  root  shape  also  varies,  froni  straight 
cromptoni  clearly  does  not  retain  the  al-  with  a  blunt  or  bulbous  terminus,  to  those 
temate  pattern  of  Thrinaxodon,  nor  are  that  are  curved  and  tapered  (Parrington, 
teeth  exclusively  lost  mesially  and  added  1971,  1978).  Root  morphology  in  Sinocon- 
distally,  as  in  gomphodonts,  tritylodontids,  odo7i  also  varies:  some  premolars  (Zhang 
and  Sinoconodon.  Instead,  M.  cromptoni  et  al.,  1998)  and  molars  of  Sinoconodon 
replaces  mesial  and  distal  postcanines  si-  are  fully  divided,  but  at  least  one  example 
multaneously  and  thus  compromises  the  is  known  w^here  the  two  roots  are  conflu- 
stability  of  the  tooth  row.  Of  the  teeth  rep-  ent  beneath  the  crown,  and  are  only  nar- 
resented  in  MGUH  VP  3392,  the  second  rowly  separated  distally  (Luo,  1994,  fig. 
and  fifth  were  being  replaced  and  likely  6.6).  Cui  and  Sun  (1987)  document  exten- 
lacked  functional  predecessors  at  the  time  sive  variability  among  tritylodontids,  which 
of  death.  Thus,  of  the  five  tooth  positions  until  recently  were  the  only  known  Early 
represented  by  replacement  teeth  or  func-  Mesozoic  cynodont  clade  (other  than 
tional  roots,  only  the  third,  fourth,  and  mammals)  with  multirooted  teeth.  In  some 
sixth  postcanines  were  occupied  by  func-  taxa  (e.g.,  Yiinnanodon)  the  roots  are  com- 
tional  teeth.  The  low  number  of  functional  pletely  separated,  whereas  in  others  {Oli- 
postcanines  in  MGUH  VP  3392  contrasts  gokijphiis  and  Lufengia)  transverse  sheets 
sharply  with  the  "uninterrupted  molari-  of  dentine  connect  root  pairs.  Bienother- 
form  series"  of  mammals  and  gomphodont  iinn  exliibits  differences  in  the  degree  of 
cynodonts  (Hopson,  1971:  17).  root  separation  along  the  upper  postcanine 
^,  ^  .  .  ,  . .  ,  .  .  -,-  row,  with  unseparated  roots  mesially  and 
The  Origins  of  Multirooted  Teeth  f^jl^  separated  roots  distally   In  general. 

Teeth  with   multiple   roots   have   tradi-  the  number  of  roots  in  tritylodont  teeth 

tionally  been  regarded  as  part  of  the  func-  varies  with  the  number  of  cusps  (Cui  and 

tionally   interdependent,    coevolved   com-  Sun,    1987).   Finally,   to  this   spectrum  of 

plex  of  the  mammalian  masticatoiy  system,  variation  may  be  added  Mitredon  cromp- 

which  includes  such  diagnostic  features  as  toni.  With  a  sectorial  crown  inoi"phology 

a  dentary— squamosal  jaw  joint  and  unilat-  and  a  tooth  replacement  pattern  that  is 

eral  mastication  (e.g.,  Crompton,  1963a, b;  comparable    to    no    known    mammal,    M. 

Barghusen    and    Hopson,    1970;    Kiihne,  cromptoni  is  best  inteipreted  as  a  cyno- 

1973;     Crompton     and     Parker,     1978;  dont  with  double-rooted  teeth. 
Crompton,  1989).  However,  several  fossil 

taxa  challenge  the  notion  that  "mammaU-  CONCLUSIONS 

an"  characters  are  limited  to  the  Mam-  Advanced  cynodonts  may  potentially  ex- 
malia.  For  example,  Shubin  et  al.  (1991)  hibit  a  mosaic  of  "mammalian"  and  "non- 
noted  that  unilateral  occlusion  may  have  mammalian"  characteristics.  Mitredon 
originated  not  with  the  Mammaliaformes  cromptoni,  Meurthodon  gallicus,  tritylo- 
but  with  the  common  ancestor  of  trithel-  dontids,  and  mammals  all  possess  postca- 
odontids  and  mammaliamoiphs,  or  may  nine  teeth  with  multiple  roots.  Previous 
have  evolved  independently  in  the  Mam-  analyses  (e.g..  Sues,  1985;  supported  by 
maliaformes.  Likewise,  the  presently  Wible,  1991)  point  to  an  independent  evo- 
known  structural  diversity  of  roots  within  lution  of  this  character  in  tritylodontids. 
taxa,  as  well  as  the  phylogenetic  distribu-  Hence,  if  M.  cromptoni  and  Meurthodon 
tion    of   multirooted    teeth,    provide    evi-  gallicus   are   indeed   "chiniquodonts"   (no 


Tooth  Replacement  and  Double-Rootedness  •  Shapiro  and  Jenkins        57 


recent  analyses  place  chiniquodonts  as  the 
sister  taxon  of  mammals),  then  multiple- 
rooted  postcanines  may  have  evolved  up  to 
three  separate  times  in  cynodonts  (follow- 
ing the  phylogenetic  hypotheses  of  Hop- 
son,  1994;  Hopson  and  Kitching,  2001). 
This  character  would  no  longer  be  useful 
in  the  diagnosis  of  Mammaliamorpha 
(Rowe,  1988)  or  Mammaliaformes  (Wible, 
1991).  Alternately,  double-rootedness  may 
have  evolved  only  once,  in  the  Mammali- 
aformes (Wible,  1991;  Hopson  and  Kitch- 
ing, 2001).  In  this  scenario,  Mitredon  and 
Meurthodon  would  fall  within  the  Trithel- 
odontidae  +  Mammaliaformes  clade,  clos- 
er to  mammaliaforms  than  to  trithelodon- 
tids. 

Double-rootedness  did  not  necessarily 
evolve  in  concert  with  tooth  row  stasis  dur- 
ing synapsid  evolution.  Mitredon  cromp- 
toni  has  double-rooted  teeth  but  retains  a 
tooth  replacement  pattern  uncharacteristic 
of  taxa  with  precise  occlusion  and  a  func- 
tionally uninterrupted  postcanine  tooth  se- 


ries. 


ACKNOWLEDGMENTS 

We  thank  W  W.  Amaral,  L.  B.  Clem- 
mensen,  W.  R.  Downs,  S.  M.  Gatesy,  H. 
E.  Jenkins  II,  D.  V.  Kent,  D.  C.  Roberts, 
and  N.  H.  Shubin  for  their  spirited  collab- 
oration in  fieldwork;  W  W  Amaral  for  his 
detailed  preparation  of  the  specimen;  K. 
Brown-Wing  for  the  precision  of  her  ren- 
derings in  Figure  1;  and  S.  M.  Gatesy  and 
J.  A.  Hopson  for  helpful  discussions.  J.  A. 
Hopson  generously  shared  his  unpub- 
lished drawings  and  observations  oi  Meur- 
thodon gallicus  and  provided  useful  in- 
sights in  his  review  of  the  manuscript.  We 
also  thank  Zhexi  Luo  for  his  thoughtful  re- 
view. This  work  was  supported  by  grants 
from  the  National  Science  Foundation,  the 
Carlsberg  Foundation,  and  the  Putnam 
Expeditionary  Fund  of  the  MCZ. 

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ON  TWO  ADVANCED  CARNIVOROUS  CYNODONTS  FROM  THE 
LATE  TRIASSIC  OF  SOUTHERN  BRAZIL 


JOSE  F.  BONAPARTE^  AND  MARIO  COSTA  BARBERENA^ 


Abstract.  Cranial  and  postcranial  remains  of  the 
cynodonts  Therioherpeton  cargnini  (Therioherpeti- 
dae)  and  a  taxon  originally  referred  to  as  Thrinaxodon 
brasiliensis  (of  indeterminate  familial  status)  are  de- 
scribed and  compared  wdth  other  advanced  cyno- 
donts and  morganucodontids.  Our  study  provides  ev- 
idence that  these  earlv  Late  Triassic  cvnodonts,  which 
possessed  primitive  carnivorous  dentitions  of  tlie 
Thrinaxodon  liorhiniis  type,  evolved  derived  charac- 
ters of  the  skull  and  postcranium  that  approximated 
the  mammtilian  level  of  organization  as  represented 
in  morganucodontids. 

INTRODUCTION 

Therioherpeton  cargnini  (Therioher- 
petidae)  is  represented  by  an  incoinplete 
skull  and  lower  jaw,  and  most  of  the  post- 
cranial  skeleton,  but  only  the  skull  and  a 
fragment  of  the  lower  jaw  have  been  de- 
scribed (Bonaparte  and  Barberena, 
1975).  The  genus  Therioherpeton  was  re- 
ferred to  the  fainily  "Therioherpetonti- 
dae"  by  Bonaparte  and  Barberena 
(1975),  but  Battail  (1991)  corrected  the 
familial  name  to  Therioherpetidae.  Like- 
wise, Thrinaxodon  brasiliensis  (Barber- 
ena et  al.,  1987),  of  indeterminate  famil- 
ial status,  is  also  represented  by  an  in- 
complete skull,  lower  jaws,  and  some 
postcranial  bones,  but  only  the  skull  and 
jaws  were  described.  In  this  paper  the 
complete  material  known  from  both  spe- 
cies is  analyzed  and  compared  with  other 
advanced   Triassic   cynodonts    and    mor- 


'  Museo  Argentino  de  Ciencias  Naturales,  Avenida 
Angel  Gallardo  470,  1405  Buenos  Aires,  Argentina. 

-  Institute  de  Geociencias,  Universidade  Federal 
de  Rio  Grande  do  Sul,  Avenida  Bento  Gon^alves 
9500,  91509-900  Porto  Alegre,  Rio  Grande  do  Sul, 
Brazil. 


ganucodontids,  and  T.  brasiliensis  is  as- 
signed to  a  new  genus.  The  advanced  an- 
atomical features  of  both  taxa  suggest  a 
close  proximity  to  the  mammalian  con- 
dition, not  very  different  from  that 
evolved  by  tritylodontids  and  tritheledon- 
tids. 

Anatomical  and  phylogenetic  issues 
concerning  advanced  cynodonts  and 
primitive  mammals  have  been  widely  an- 
alyzed (Kermack  et  al.,  1981;  Kemp, 
1982;  Jenkins,  1984;  Crompton  and  Sun, 
1985;  Sues,  1985;  Hopson  and  Barghu- 
sen,  1986;  Battail,  1991;  Hopson,  1991; 
Shubin  et  al.,  1991;  Crompton  and  Luo, 
1993;  Luo,  1994),  but  the  subject  is  far 
from  well  understood  because,  as  Cromp- 
ton and  Luo  (1993:  30)  remarked:  "A  lack 
of  moi-phological  information  makes  it 
difficult  to  intei-pret  the  relationships  of 
advanced  cynodonts  and  early  mammals." 
As  yet  undescribed  carnivorous  cynodonts 
(recently  discovered  in  southern  Brazil  in 
beds  of  early  Late  Triassic  age),  and  a  re- 
study  of  the  advanced  cynodonts  Therio- 
herpeton cargnini  (Bonaparte  and  Barber- 
ena, 1975)  and  Thrinaxodon  brasiliensis 
(Barberena  et  al.,  1987),  may  advance  our 
understanding  of  the  complex  sequence  of 
anatomical  changes  that  occurred  in  cy- 
nodonts and  that  foreshadow  the  level  of 
inammalian  organization  represented  by 
morganucodontids  (Kermack  et  al.,  1973, 
1981;  Crompton,  1974;  Jenkins  and  Par- 
rington,  1976;  Cow,  1986).  Unfortunately, 
available  cranial  material  of  neither  Thri- 
naxodon brasiliensis  nor  Therioherpeton 
cargnini  includes  critical  anatomical  data 
from  the  basicranial  region. 


Bull.  Mus.  Comp.  ZooL,  156(1):  59-80,  October,  2001         59 


60 


Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


SYSTEMATIC  PALEONTOLOGY 

Therapsida  Broom,  1905 

Cynodontia  Owen,  1861 

Family  Therioherpetidae  Bonaparte  and 
Barberena,  1975 

Diagnosis.  Differs  from  the  Thrinaxo- 
dontidae  by  a  more  extensive  secondary 
palate.  Differs  from  Thrinaxodontidae,  Cy- 
nognathidae,  Chiniquodontidae,  and  Pro- 
bainognathidae  in  the  following  featui-es: 
triangular  cross  section  of  the  2ygoinatic 
arch;  absence  of  a  postorbital  bar;  frontal 
borders  the  orbit  and  bears  an  anterolat- 
eral projection  that  contacts  a  lateral  por- 
tion of  the  nasal;  interorbital  wall  more 
highly  ossified;  larger  size  of  the  neural  ca- 
nal in  the  cervical  and  dorsal  vertebrae; 
parallel  dorsal  and  ventral  borders  of  the 
ilium;  convex  lateral  surface  of  ilium;  a 
narrow,  elongate  neck  of  the  ischium;  ob- 
turator foramen  relatively  large;  greater 
trochanter  of  the  femur  extends  to  the 
same  proximal  level  as  the  femoral  head. 
Therioherpetidae  differs  from  Trithele- 
dontidae  in  the  transverse  narrowness  of 
the  upper  postcanines.  Therioherpetidae 
differs  from  gomphodont  cynodonts,  in- 
cluding Tritylodontidae,  in  possessing  tri- 
conodont  upper  and  lower  postcanines, 
and  in  the  triangular  cross  section  of  the 
zygomatic  arch.  Therioherpetids  differ 
from  basal  mammals  in  lacking  an  articular 
condyle  of  the  dentary  and  fully  bifurcated 
roots  on  postcanine  teeth  (but  see  Shapiro 
and  Jenkins,  2001). 

Genus  Therioherpeton  Bonaparte  and 
Barberena,  1975 

Type  Species  Therioherpeton  cargnini 
Bonaparte  and  Barberena,  1975 

Holotype.  An  unnumbered  specimen  in 
the  private  collection  of  the  Patronato  Al- 
ves  Ramos,  Santa  Maria  City,  State  of  Rio 
Grande  do  Sul,  Brazil.  An  incomplete  skull 
lacking  the  basicranium,  and  preserving 
only  the  right  upper  fifth  postcanine;  a 
fragment  of  the  right  dentary;  an  isolated 


lower  postcanine  (the  fifth  or  sixth,  at- 
tached to  lingual  surface  of  Pc^);  29  artic- 
ulated, incomplete  vertebrae  including  4 
cervicals,  15  dorsals  and  (separated  by  a 
gap)  4  sacral  and  6  caudal  vertebrae;  as- 
sociated, incomplete  ribs;  left  scapular 
blade;  distal  half  of  the  right  humerus;  in- 
complete right  radius  and  ulna;  incom- 
plete ilia;  complete  pubis;  right  ischium; 
complete  left  and  incomplete  right  femur; 
fragments  of  tibiae  and  fibulae;  and  in- 
complete feet. 

Revised  Generic  and  Specific  Diagnosis. 
The  triconodont  upper  and  lower  postca- 
nines are  without  cingula.  The  secondary 
bony  palate  extends  nearly  to  the  level  of 
the  last  postcanine,  as  in  chiniquodontids 
and  Probainognathus.  As  in  Morganuco- 
don,  the  frontals  have  an  extensive  poste- 
rior projection,  anteriorly  contact  the  lat- 
eral aspect  of  the  nasals,  and  anterolater- 
ally  project  to  the  lacrimals.  Prefrontals 
and  postorbitals  are  absent.  The  cervical 
vertebrae  are  craniocaudally  short,  trans- 
versely wide,  dorsoventrally  low,  and  ex- 
hibit a  very  large  neural  canal.  The  iliac 
blade  lacks  a  posterior  projection,  the  lat- 
eral surface  is  convex,  and  the  dorsal  and 
ventral  borders  are  subparallel.  The  obtu- 
rator fenestra  is  large.  The  greater  tro- 
chanter extends  proximally  to  the  level  of 
the  femoral  head,  with  which  it  is  con- 
nected by  a  sheet  of  bone. 

Horizon  and  Locality.  Upper  Santa  Ma- 
ria Formation.  A  road  cut  on  the  BR-216 
highway  (outcrop  BR- 14  in  Bortoluzzi  and 
Barberena,  1967),  200  m  northwest  of 
Cerriquito,  Township  of  Santa  Maria,  Rio 
Grande  do  Sul,  Brazil. 

Age.  Probably  early  Late  Triassic. 

DESCRIPTION 

Skull  (Figs.  1—4).  Only  the  salient  char- 
acters of  the  type  and  only  known  skull  of 
this  species,  originally  described  by  Bon- 
aparte and  Barberena  (1975),  may  be  not- 
ed here.  The  more  significant  characters 
are  the  absence  of  the  prefrontal  and  post- 
orbital,  the  large  lacrimal,  the  frontal  bor- 
dering the  orbit  with  a  long  posterior  pro- 


Advanced  Triassic  Cynodonts  from  Brazil  •  Bonaparte  and  Barberena        61 


PCS 


8  mm 


B 


8  mm 


^^ 


Figure  1 .  Therioherpeton  cargnini.  Skull  and  dentary  fragment  in  (A)  right  lateral  and  (B)  dorsal  views.  (C)  Incomplete  interorbital 
wall  viewed  from  the  left  side.  (D)  Upper  postcanine  5  in  occlusal,  lingual,  and  buccal  views,  and  Pc5o,6  in  buccal  and  occlusal 
views.  Abbreviations:  AL,  alisphenoid;  D,  dentary;  FM,  maxillary  foramina;  FR,  frontal;  J,  jugal;  L,  lacrimal;  MX,  maxilla;  N,  nasal; 
PAL,  palatine;  P,  parietal;  PP,  prearticular  process;  PR,  prootic;  SQ,  squamosal. 


cess,  and  an  anterolateral  projection  of  the 
frontal  in  dorsal  view.  The  parietal  crest  is 
low  (Fig.  lA)  and  the  dorsal  area  of  the 
braincase  is  large  (Fig.  3);  the  z)'gomatic 
arch  is  slender  with  a  triangular  cross  sec- 
tion (Figs.  lA,  4).  The  lateral  surface  of 
the  maxilla  bears  three  large  foramina 
(Fig.  lA).  The  upper  and  lower  postcani- 
nes  (Fig.  ID)  are  of  the  triconodont  type 
and  lack  cingula,  and  the  upper  teeth  show 
clear  indications  of  an  incipient  bifurcation 
of  the  roots. 

The  secondary  bony  palate  of  Therio- 


herpeton was  misinterpreted  by  Bonaparte 
and  Barberena  (1975)  because  an  unossi- 
fied,  or  damaged,  area  of  the  right  palatine 
was  considered  as  part  of  the  internal  na- 
res.  Restudy  of  the  palatine  revealed  that 
its  posterior  margin  is  in  fact  complete, 
and  thus  represents  the  posterior  border 
of  the  secondaiy  bony  palate,  which  is  in 
line  with  the  penultimate  postcanine  (Fig. 
2). 

Postcranial  Skeleton  (Figs.  5-8).  The  as- 
sociated postcranium  was  found  in  nearly 
articulated  condition  lying  on  the  external 


62         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  2.  Therioherpeton  cargnini.  Ventral  view  of  the  incomplete  skull  of  the  holotype.  The  secondary  osseous  palate  shows 
an  unossified  area  of  the  palatine.  However,  the  posterior  border  of  the  right  palatine  is  well  preserved.  Most  of  the  ventral  side 
of  the  skull  roof  from  nasals  to  parietals  is  shown. 


side  of  the  rib  cage  of  a  rhynchosaur,  prob- 
ably Scaphonijx  sp.  (Schultz,  1986).  All  but 
six  vertebrae  are  incomplete.  Three  cei"vi- 
cals  are  articulated  in  a  small,  isolated 
block,  associated  with  the  blade  of  the 
right  scapula.  The  centra  of  these  verte- 
brae are  anteroposteriorly  short,  trans- 
versely wide,  and  dorsoventrally  low,  and 
have  a  wide  neural  canal.  The  inferred  last 
cervical,  articulated  with  a  series  of  15  dor- 
sals (Fig.  5A),  also  has  a  short,  wide,  and 
dorsoventrally  low  centrum;  the  neural  ca- 


nal is  wider  than  the  centrum  because  the 
pedicles  of  the  neural  arch  project  dorso- 
late  rally. 

The  anteroposterior  lengths  of  the  seven 
anterior  dorsals  gradually  increase;  neural 
canals  remain  very  large  (Fig.  5A).  The  8th 
through  10th  dorsals  preserve  the  neural 
spines,  which  are  posterodorsally  inclined. 
The  centra  of  the  11th  through  14th  dor- 
sals are  longer  than  those  of  preceding 
vertebrae;  in  these  vertebrae,  the  large 
neural  canal  is  formed  in  part  by  the  ven- 


Figure  3.     Therioherpeton  cargnini.  Dorsal  view  of  the  incomplete  skull  of  the  holotype,  showing  the  anterolateral  projection  of 
the  frontals  as  well  as  their  extensive,  wedge-shaped  posterior  projection. 


Advanced  Triassic  Cynodonts  from  Brazil  •  Bonaparte  and  Barberena        63 


Figure  4.     Therioherpeton  cargnini.  Right  lateral  view  of  the  incomplete  skull  and  jaw  of  the  holotype.  Note  the  slender  zygomatic 
section  of  the  jugal,  and  the  incipiently  bifurcated  root  of  Pc^ 


tromedial  surfaces  of  the  neural  pedicles 
that  contribute  to  the  floor  of  the  neural 
canal.  The  number  of  dorsal  vertebrae  is 
uncertain  because  of  a  gap  between  the 
fifteenth  dorsal  and  the  next  group  of  ver- 
tebrae. The  zygapophyses  of  the  last  dorsal 
vertebrae  are  anteroposteriorly  robust  and 
oriented  almost  horizontally,  with  little  in- 
clination toward  the  median  plane.  The 
vertebrae  forming  the  sacrum  are  difficult 
to  discern  individually,  although  one  bears 
fragments  of  sacral  ribs.  We  infer  that 
there  might  be  three  or  possibly  four  sa- 
cral vertebrae.  All  are  rather  robust,  and 
the  neural  canals  are  as  wide  as  the  centra. 

Subcylindrical  fragments  (and  many 
molds)  preserve  15  incomplete  ribs  on  the 
right  side  and  17  on  the  left  side  (Figs.  5A, 
6).  There  is  no  evidence  of  overlapping 
uncinate  processes  as  are  known  in  many 
cynodonts.  Cervical  ribs,  which  are  short, 
thick,  and  posteriorly  deflected,  articulate 
behind  the  anterior  margins  of  the  centra, 
not  between  adjacent  centra  as  in  Thri- 
naxodon  liorhinus  (Jenkins,  1971).  The 
dorsal  ribs,  which  in  cross  section  are  fig- 
ure 8-shaped,  exliibit  no  clear  indication 
of  a  lumbar  region,  except  that  the  poste- 
rior dorsal  ribs  gradually  decrease  in 
length. 

The  pectoral  girdle  is  represented  only 


by  the  blade  of  the  right  scapula  (not  fully 
prepared  at  present).  The  anterior  and 
posterior  borders  of  the  blade  project  lat- 
erally, forming  a  deep  sulcus  for  musculus 
supracoracoideus,  similar  to  the  condition 
in  Thrinaxodon  liorhinus  (Jenkins,  1971). 
The  distal  half  of  the  right  humerus  is  pre- 
served, and  appears  to  be  relatively  prim- 
itive by  virtue  of  its  great  distal  width  and 
the  presence  of  an  ectepicondylar  fora- 
men. The  Pright  radius  and  ulna  are  in- 
completely preserved  and  reveal  no  diag- 
nostic characters. 

Of  the  two  incomplete  ilia,  the  left  ilium 
(Fig.  5B)  preserves  part  of  the  blade, 
which  has  almost  parallel  dorsal  and  ven- 
tral borders  and  lacks  a  posterior  process. 
The  lateral  aspect  of  the  blade  is  dorso- 
ventrally  convex.  The  pubic  pedicle  is 
more  developed  and  stronger  than  the 
area  of  ischial  contact.  The  ischium  (Fig. 
5D)  has  an  elongate,  narrow  neck,  and 
forms  wdth  the  pubis  a  large  obturator  fe- 
nestra. The  pubis  (Fig.  5C)  exliibits  a  wefl- 
defined,  "twisted"  neck  below  the  acetab- 
ulum. A  thickening  of  the  anterior  margin 
of  the  pubis  ventral  to  the  neck  represents 
a  pubic  process.  The  inferior  border  of  the 
pubic  ramus  is  rather  straight,  whereas  the 
superior  border  is  concave  and  forms  part 


64         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


5  mm 


Figure  5.  Therioherpeton  cargnini.  (A)  Sequence  of  articulated  incomplete  vertebrae  and  ribs  from  the  putative  last  cervical  (at 
the  bottom)  to  the  10th  dorsal.  (B)  Incomplete  left  ilium  in  lateral  (left)  and  ventral  (right)  views.  (C)  Both  pubes  in  dorsal  view 
as  preserved,  and  the  left  pubis  in  lateral  view.  (D)  Right  ischium  in  lateral  (left)  and  medial  (right)  views.  (E)  Reconstruction  of 
the  right  half  of  the  pelvis  in  lateral  view.  Abbreviations:  AA,  acetabular  area;  ANP,  area  for  neural  pedicles;  CC,  cervical  centrum; 
CSA,  crista  supracetabularis;  IP,  ischial  plate;  IT,  ischial  tuberosity;  NC,  neural  canal;  NF,  neural  fossa;  Nl,  neck  of  the  ischium; 
NSP,  neural  spine;  OBT,  obturator  foramen;  PP,  pubic  pedicle;  PPR,  pubic  process;  R,  rib;  SA,  symphysial  area. 


of  the  margin  of  the  large  obturator  fe- 
nestra. 

The  left  femur  is  nearly  complete  (Figs. 
7A,  8).  The  proximal  end  gradually  ex- 
pands mediolaterally,  and  the  trochanters 
are  less  defined  than  in  Oligokijphus  (Kiih- 
ne,  1956)  and  Morganiicodon  (Jenkins  and 
Parrington,  1976).  The  femoral  head  is  an- 
teromedially   and    somewhat   dorsally   di- 


rected, although  the  precise  orientation  is 
obscured  by  slight  deformation.  The  prox- 
imally  positioned  lesser  trochanter  is  sim- 
ilar to  that  of  Oligokijphus  and  Morganii- 
codon, and  different  from  the  more  ven- 
trally  placed  trochanters  of  Probelesodon 
(Romer  and  Lewis,  1973),  Massetognatlins 
(Jenkins,  1970),  and  Exaeretodon  (Bona- 
parte,   1963).    The    greater   trochanter   is 


Advanced  Triassic  Cynodonts  from  Brazil  •  Bonaparte  and  Barberena        65 


Figure  6.     Therioherpeton  cargnini.  Part  of  the  presacral  vertebral  column  showing  broad  neural  arches,  posterodorsally  directed 
neural  spines,  and  ribs  without  overlapping  processes. 


B 


5  mm 


Figure  7.  Therioherpeton  cargnini.  (A)  Left  femur  in  anterior  and  lateral  views.  (B)  Distal  portions  of  right  tibia  and  fibula 
articulated  with  the  incomplete  foot  in  plantar  view.  Abbreviations:  AST,  astragalus;  CAL,  calcaneum;  ENC,  entocuneiform;  F, 
fibula;  FH,  femoral  head;  GT,  greater  trochanter;  LC,  lateral  condyle;  LT,  lesser  trochanter;  NAV,  navicular;  SCG,  supracondylar 
groove;  T,  tibia;  ll-V,  metatarsals  II  through  V. 


66 


Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  8.     Therioherpeton  cargnini.  On  the  left  is  a  series  of  incomplete  sacrocaudal  vertebrae  in  dorsal  view.  Also  present  are 
the  left  femur,  left  pubis,  incomplete  left  ilium,  and  incomplete  left  foot.  The  ilium  rests  on  a  rhynchosaur  {Scaphonyx  sp.)  rib. 


proximally  positioned  and  is  united  with 
the  femoral  head  by  a  thin  lamina  of  bone. 
Morphologically,  the  greater  trochanteric 
structure  is  similar  to  that  of  Oligokijphus 
and  Morganiicodon,  and  very  different 
from  the  condition  in  Cijnognathus  (Jen- 
kins, 1971),  Prohelesodon  (Romer  and 
Lewis,  1973),  Massetognathiis  (Jenkins, 
1970),  and  Exaeretodon  (Bonaparte, 
1963).  The  lateral  femoral  condyle  has  a 
larger  radius  of  curvature  than  the  medial; 
a  shallow  supracondylar  groove  is  present 
on  dorsal  surface  of  the  distal  end. 

The  astragalus,  which  is  larger  than  the 
calcaneum,  is  only  partially  superimposed 
on  the  latter  (Fig.  7B).  Inasmuch  as  the 
calcaneum  is  damaged  along  its  proximal 
margin,  the  presence  or  absence  of  a  cal- 
caneal tuber  cannot  be  determined.  The 
relatively  elongate,  slender  proportions  of 
the  metatarsals  resemble  those  of  Oligo- 
kijphus (Kiihne,  1956),  rather  than  those 
of  Exaeretodon  (Bonaparte,  1963)  or 
"PAleodon/?Scalenodon"  (Jenkins,  1971). 

A  Stimmanj  of  the  Distinctive  Features 
of  Therioheipeton.  Although  Therioher- 
peton possesses  many  features  that  are 
found  in  other  Triassic  cynodont  families, 
the  following  assemblage  is  characteristic 
only  of  Therioherpeton  and  represents  the 


degree  to  which  this  taxon  approaches  the 
morganucodontid  level  of  organization. 

1)  Absence  of  prefrontal  and  postorbital 
bones  as  well  as  a  postorbital  bar  (also 
in  tritheledontids  and  tritylodontids). 

2)  Frontal  bordering  the  orbit  (also  in 
tritheledontids  and  tritylodontids). 

3)  Frontal  with  anterolateral  projection 
in  dorsal  view,  and  an  elongate  pos- 
terior projection. 

4)  Large  lacrimal  (also  in  tritheledontids 
and  tritylodontids). 

Comment.  The  first  three  characters 
listed  above  differentiate  Therioherpeton 
from  the  Thrinaxodontidae,  Cynognathi- 
dae,  Chiniquodontidae,  and  Probaino- 
gnathidae.  Some  of  the  characters  are 
shared  with  the  Tritylodontidae  (Kiihne, 
1956;  Sun,  1984;  Sues,  1985)  and  Trithe- 
ledontidae  (Crompton,  1958;  Bonaparte, 
1980),  but  in  tritylodontids  the  zygomatic 
arch  is  deep  and  the  dentition  very  de- 
rived, whereas  in  tritheledontids  the  spe- 
cialized incisors,  reduced  canines,  and  bul- 
bous upper  postcanines  differ  from  the 
corresponding  features  in  Therioherpeton. 
The  upper  postcanines  of  the  tritheledon- 
tids are  transversely  expanded,  whereas  in 
Therioherpeton  they  are  narrow,  with  the 


Advanced  Triassic  Cynodonts  from  Brazil  •  Bonaparte  and  Barherena        6' 


cusps  in  line.  The  structure  of  the  frontal 
resembles  that  of  Morganucodon  (Ker- 
mack  et  al.,  1981)  in  the  type  of  contact 
^^dth  the  nasal,  a  possible  result  of  the  ab- 
!  sence  of  the  prefrontal,  as  well  as  in  the 
j  long,  tapering  contact  with  the  parietals. 

i  5)  Contact  between  the  ventral  process 
of  frontal  and  dorsal  process  of  pala- 
tine (also  in  tritheledontids  and  trity- 
lodontids;  and  in  Probainognathus 
and  chiniquodontids;  J.  A.  Hopson, 
personal  communication). 

6)  Large  infraorbital  foramen  and  two 
well-defined  foramina  for  the  trigem- 
inal nei^ve  in  the  maxilla  (also  in  tri- 
theledontids and  tritylodontids). 

7)  Carnivorous— insectivorous  dentition, 
similar  to  that  of  Thrinaxodon  and 
Morganucodon,  but  with  upper  post- 
canines  without  cingula  and  possess- 
ing incipiently  bifurcated  roots. 

8)  Articular  process  of  the  dentary  pos- 
teriorly and  transversely  expanded, 
without  indication  of  a  condyle,  and 
set  at  a  higher  level  than  the  alveoli  (a 
common  feature  in  derived  cyno- 
donts; J.  A.  Hopson,  personal  com- 
munication). 

9)  Cervical  centra  anteroposteriorly 
short,  transversely  wide  and  dorsoven- 
trally  low  (also  in  Oligokijphus,  other 
tritylodontids,  and  Morganucodon) . 

10)  Neural   canal   of  presacral   vertebrae 
wider  than  the  centi-um. 

Comment.  The  neural  canal  in  Therio- 
herpeton  is  proportionally  larger  than  that 
in  most  cynodonts  wdth  which  we  were 
able  to  make  a  comparison.  Neural  canal 
size  in  the  cervical,  thoracic,  sacral,  and 
proximal  caudal  vertebrae  of  Oligokijphus 
(Kiihne,  1956)  approaches  that  of  Therio- 
het-peton,  but  is  nonetheless  proportionally 
smaller.  The  neural  canal  of  Therioherpe- 
ton  is  in  fact  almost  identical  in  propor- 
tions to  that  in  Morganucodon  (Jenkins 
and  Parrington,  1976). 

11)  Absence  of  anapophyses. 

12)  Ribs  without  expanded  processes  (also 


in  Exaeretodon,  chiniquodontids,  Pro- 
bainognathus, and  tritylodontids;  and 
in  tritheledontids  as  well;  J.  A.  Hop- 
son,  personal  communication). 

13)  Neural  spines  of  presacral  vertebrae 
posterodorsally  directed  (also  in  trity- 
lodontids). 

Comment.  Short,  posterodorsally  direct- 
ed neural  spines  in  the  posterior  dorsals 
are  known  only  in  Oligokijphus  and  Ther- 
ioherpeton.  In  Morganucodon,  the  poste- 
rior dorsals  bear  vertical  neural  spines, 
with  fully  differentiated  lumbar  vertebrae. 
The  similarities  between  some  derived  ax- 
ial characters  in  Oligokijphus  and  Therio- 
herpeton  suggest  the  probability  of  parallel 
evolution. 

14)  Iliac  blade  with  dorsal  and  ventral 
borders  subparallel,  without  posterior 
process  (also  in  some  tritylodontids; 
and  tritheledontids;  J.  A.  Hopson,  per- 
sonal communication). 

15)  Lateral  side  of  the  iliac  blade  dorso- 
ventrally  convex  (also  in  tritylodontids 
and  tritheledontids;  J.  A.  Hopson,  per- 
sonal communication). 

16)  Ischium  with  narrow  neck  posterior  to 
the  acetabulum,  and  a  concave  dorsal 
border  (also  in  Oligokijphus  and  tri- 
theledontids; J.  A.  Hopson,  personal 
communication ) . 

17)  Large  obturator  fenestra  (also  in  tri- 
tylodontids and  tritheledontids;  J.  A. 
Hopson,  personal  communication). 

18)  Pubis  narrow  with  reduced  distal  con- 
tact with  the  ischium  (also  in  trithe- 
ledontids; J.  A.  Hopson,  personal 
communication). 

Comment.  The  available  parts  of  the 
ilia,  the  complete  pubes,  and  the  ischium 
show  that  the  pelvis  of  Theriohetyeton  is 
more  derived  than  that  in  any  known  cy- 
nodont  family  except  the  Tritylodontidae 
(Kuhne,  1956)  and  Trithelodontidae  (J.  A. 
Hopson,  personal  communication). 

19)  Greater  trochanter  at  the  same  level 
as  the  femoral  head  (also  in  Oligoky- 


68 


Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


phiis  and  tritheledontids;  J.  A.  Hop- 
son,  personal  communication). 
20)   Elongate,  slender  metatarsals  (also  in 
Oligokyplms) . 

SYSTEMATIC  PALEONTOLOGY 
Therapsida  Broom,  1905 
Cynodontia  Owen,  1861 
Family  Incertae  Sedis 
Genus  Prozostrodon  New  Genus 

Type  species,  Prozostrodon  brasiliensls  (Barberena, 
Bonaparte,  and  Sa  Teixeira,  1987). 

Synonymy  Thrinaxodon  brasiliensis  Barberena,  Bon- 
aparte, and  Sa  Teixeira,  1987. 

Holotype.  PV  0248T,  Department  of  Pa- 
leontology and  Stratigraphy,  Universidade 
Federal  de  Rio  Grande  do  Sul,  Brazil. 

Etymology.  The  generic  designation  al- 
ludes to  the  cingula  of  lower  postcanine 
teeth  (Greek,  zoster,  a  girdle  or  band),  in 
combination  with  Latin,  pro-,  before,  in 
reference  to  the  hypothesized  antecedant 
phylogenetic  position  of  the  taxon. 

Revised  Generic  and  Specific  Diagnosis. 
Reduced  prefrontal  and  postorbital;  lacri- 
mal with  large  dorsal  exposure;  pro- 
nounced posterodorsal  process  of  the  pre- 
maxilla  between  septomaxilla  and  maxilla. 
Posterior  projection  of  the  frontal  shorter 
than  in  Therioherpeton;  anterolateral  pro- 
cess of  the  frontal  shorter  than  in  Therioh- 
erpeton, and  contacts  the  posterolateral 
border  of  the  nasal,  as  in  Therioherpeton 
and  Morganiicodon.  Frontal,  palatine,  and 
orbitosphenoid  extensively  contact  one  an- 
other in  the  orbital  wall.  Five  conical  up- 
per incisors;  four  lower  incisors  slightly 
spatulate  and  procumbent  (as  in  Morgan- 
iicodon). Triconodontlike  postcanines 
without  well-defined  cingula  on  the  uppers 
(except  for  an  incipient  buccal  cingulum 
on  the  distal  upper  postcanine,  as  in  Thri- 
naxodon liorhinus  and  chiniquodontids); 
lingual  cingula  on  lower  postcanines  bear 
up  to  nine  small  cusps  (as  in  Thrinaxodon 
liorhinus).  Length  of  lower  tooth  row 
more  than  half  the  length  of  the  dentary 
(as    in    Morganiicodon).    Secondary   bony 


palate  extends  posteriorly  beyond  the  last 
upper  postcanine,  as  in  chiniquodontids 
and  tritheledontids.  Neural  canal  of  the 
presacral  vertebrae  large  (as  in  Oligopky- 
phiis),  but  smaller  than  in  Therioherpeton. 
Neural  spines  posterodorsally  inclined  (as 
in  tritylodontids).  Zygapophyses  of  poste- 
rior dorsal  vertebrae  anteroposteriorh 
elongated,  with  anterior  and  posterior  fac- 
ets that  are  transversely  concave  and  con- 
vex, respectively.  Ribs  without  expanded 
processes.  Iliac  blade  with  a  vestigial  pos- 
terior process  and  a  convex  lateral  surface 
(as  in  Therioherpeton  and  tritylodontids; 
also  in  tritheledontids;  J.  A.  Hopson,  per- 
sonal communication). 

Horizon  and  Locality.  Facies  Alemoa  of 
the  Santa  Maria  Formation,  200  m  north- 
west of  the  hill  Cerriquito,  in  a  road  cut 
of  route  BR-216,  Municipio  of  Santa  Ma- 
ria, State  of  Rio  Grande  do  Sul,  southern 
Brazil. 

Age.  Early  Late  Triassic. 

Material.  An  incomplete  skull  lacking 
most  of  the  parietal  crest,  the  braincase, 
and  zygomatic  arch.  The  orbital,  preorbit- 
al,  and  infraorbital  regions,  secondary 
bony  palate,  and  upper  dentition  are  near- 
ly complete.  The  right  dentary  and  denti- 
tion are  complete;  the  left  dentary  also  has 
a  complete  dentition  but  lacks  the  ascend- 
ing ramus  and  articular  process.  The  post- 
cranium  is  represented  by  three  incom- 
plete presacral  vertebrae,  14  dorsal  centra, 
seven  dorsal  neural  arches,  several  frag- 
mentary ribs,  interclavicle,  incomplete 
right  humerus,  proximal  half  of  the  left  hu- 
merus, incomplete  right  ilium,  distal 
halves  of  both  femora,  and  a  disarticulated 
right  foot. 

Comments.  Significant  features  of  the 
skull  have  been  more  clearly  exposed 
through  recent  preparation.  The  skull 
shows  some  postmortem  cracking  and  dis- 
tortion. 

DESCRIPTION 

Skull  {Figs.  9-11).  The  prefrontal  and 
postorbital  are  reduced,  and  there  is  no 
indication  of  a  postorbital  bar  (Fig.  9).  The 


Advanced  Triassic  Cynodonts  from  Brazil  •  Bonaparte  and  Barberena        69 


PRF 


PAP 


Figure  9.  Prozostrodon  braslliensis,  new  genus.  Incomplete  skull  in  (A)  dorsal,  (B)  ventral,  and  (C)  left  lateral  views.  (D) 
Incomplete  right  lower  jaw  in  medial  view.  Abbreviations:  Al,  alveolus  for  incisor;  ALS,  alisphenoid;  CO,  coronoid;  D,  dentary; 
FE,  ethmoidal  foramen;  FM,  maxillary  foramina;  FPB,  fossa  for  postdentary  bones;  FR,  frontal;  GDL,  groove  of  dental  lamina; 
L,  lacrimal;  MX,  maxilla;  N,  nasal;  OBS,  orbitosphenoid;  P,  parietal;  PA,  prearticular;  PAL,  palatine;  PAP,  prearticular  process; 
PRF,  prefrontal;  PMX,  premaxilla;  PO,  postorbital;  PT,  pterygoid;  RPC,  replacing  postcanine;  SF,  symphysial  foramen;  SGR, 
symphysial  groove;  SMX,  septomaxilla;  SPL,  splenial;  SPT  F,  sphenopalatine  foramen. 


70         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  10. 
is  sliown. 


Prozostrodon  brasillensis,  new  genus.  Dorsal  view  of  the  holotype  sl<ull.  The  anterolateral  projection  of  the  frontal  I 


frontal  borders  the  orbit  and  extends  an- 
terolaterally  to  contact  the  lateral,  poste- 
rior portion  of  the  nasal,  as  in  Therioher- 
peton.  The  orbital  process  of  the  frontal 
contacts  the  dorsal  process  of  the  palatine 
and  the  orbitosphenoid,  similar  to  that  of 
Morganucodon  (Kermack  et  al.,  1981,  fig. 
96).  The  sphenopalatine  foramen  in  Mor- 
ganucodon is  bordered  by  the  palatine  and 
orbitosphenoid  (Kermack  et  al.,  1981), 
whereas  in  Prozostrodon  it  is  entirely  en- 
closed by  the  palatine,  possibly  the  prim- 
itive condition,  with  the  orbitosphenoid  in 


a  more  posterior  position.  Despite  this  dif- 
ference, it  is  interesting  to  note  the  struc- 
tural similarities  of  the  interorbital  regions 
of  Morganucodon  and  Prozostrodon,  with 
the  exception  that  the  distance  between 
the  ethmoidal  foramen  (Fig.  9C)  and  the 
anterior  border  of  the  orbit  is  proportion- 
ally shorter  in  Morganucodon,  possibly 
representing  a  derived  condition. 

A  small  prefrontal  is  present  (Fig.  9A), 
anteriorly  reduced  by  the  posterior  expan- 
sion of  the  lacrimal.  A  small  orbital  process 
of  the  prefrontal  is  possibly  present,  con- 


Figure  1 1 .     Prozostrodon  brasiliensis,  new  genus.  Ventral  view  of  the  holotype  skull. 


Advanced  Triassic  Cynodonts  from  Brazil  •  Bonaparte  and  Barberena        71 


tacting  a  similar  process  of  the  frontal,  but  comprises   five  incisors,   one  canine,   and 

it  cannot  be  positively  identified  because  seven  postcanines  (Fig.  9C).  The  incisors 

the  sutures  are  not  clear.  are  slender  and  posteriorly  recurved.  All 

The  postorbital  is  represented  only  on  five  incisors,  which  are  slender  and  slightly 
the  left  side  (Fig.  9C)  as  a  small  plate  over-  recurved,  are  present  on  the  right;  four  in- 
lapping  the  frontal  and  parietal  on  their  cisors  and  an  alveolus  for  the  fifth  incisor 
dorsolateral  surfaces.  The  bone  has  some  are  present  on  the  left, 
external  sculpturing,  but  there  is  no  indi-  In  right  upper  postcanine  row,  the  third 
cation  of  the  postorbital  bar.  and  seventh  (last)  teeth  were  in  the  pro- 

The  premaxilla  has  a  narial  process  con-  cess  of  erupting.  Postcanine  crowns  are  of 
tacting  the  nasal  (Fig.  9C).  The  lateral  pos-  the  "triconodont"  type,  with  cusps  aligned 
terodorsal  process  contacting  the  maxilla  is  mesiodistally.  In  the  three  posterior  post- 
slender  and  is  partially  covered  by  the  canines,  four  cusps  (A,  B,  C,  and  D)  are 
maxilla.  The  premaxilla  has  a  long  contact  present.  The  labial  side  is  mesiodistally 
with  the  septomaxilla  and  does  not  reach  convex,  whereas  the  lingual  face  is  rather 
the  nasal.  concave  or  flat,  with  some  ill-defined  wear; 

The  slender  septomaxilla  of  Prozostro-  the   lack   of  well-defined   facets   suggests 

don   (Fig.  9C)  appears  similar  to  that  of  that  no  precise  occlusion  was  present.  The 

Sinoconodon  (Crompton  and  Luo,  1993),  mesiolingual  corner  of  the  last  left  post- 

although  it  is  uncertain  whether  a  septo-  canine  bears  a  poorly  defined,  low  cusp  in 

maxillary  foramen  is  present  or  not.  a  position  that  might  be  expected  of  an 

The  rather  large  maxilla  projects  later-  incipient  lingual  cingulum.  Conversely,  the 
ally  over  the  premaxilla  up  to  the  level  of  last  right  postcanine  (in  the  process  of 
the  third  incisor  (Fig.  9C).  A  posterior  pro-  erupting)  bears  a  small  buccal  cusp  distal- 
cess  of  the  maxilla  forms  the  anterior  por-  ly;  there  is  no  indication  of  buccal  cingular 
tion  of  the  zygomatic  arch.  A  large  infra-  development  in  the  functional  postca- 
orbital  foramen  lies  below  the  anterior  nines.  The  occurrence  of  cingular  cuspules 
margin  of  the  lacrimal,  and  two  well-de-  only  on  the  last  upper  postcanine  in  Fro- 
fined  maxillary  foramina  are  present  above  zostrodon  is  perhaps  comparable  to  the 
the  anterior  border  of  the  first  postcanine.  condition   in   Thrinaxodon   liorhimis   (Os- 

The  anteroposteriorly  elongate  palatines  bom  and  Crompton,  1973;  also  suggested 
of  Frosos^roffon  (Fig.  9B)  resemble  a  sim-  for  Pachygenelus;  Cow,  1980)  in  which 
ilar  configuration  in  the  bony  palate  of  chi-  morphological  complexity  increases  to- 
niquodontids  and  morganucodontids.  Al-  wards  the  distal  end  of  the  tooth  row.  The 
though  the  posterior  border  of  the  right  roots  of  the  upper  postcanines  show  evi- 
palatine  is  broken,  the  left  side  is  com-  dence  of  incipient  bifurcation,  as  originally 
pletely  preserved  and  extends  posterior  to  indicated  by  Barberena  et  al.  (1987). 
the  last  postcanine;  this  condition  is  similar  Lower  Jaw  and  Dentition  (Figs.  9D,  12). 
to  that  in  Probelesodon  kitchingi  (Sa  Teix-  The  dorsal  and  ventral  margins  of  the 
eira,  1979)  and  trithelodontids,  and  is  a  lit-  elongate  body  of  the  mandible  (Fig.  9D) 
tie  more  extensive  than  in  Therioher})efon.  are  subparallel  as  far  forward  as  the  pos- 
The  posterior  half  of  the  secondary  bony  terior  border  of  the  symphysis.  Anterior  to 
palate  is  widest  posteriorly  where  the  tooth  this  point,  the  dentary  extends  anterodor- 
row  diverges  posterolaterally.  There  is  a  sally,  elevating  the  alveolar  plane  of  the  in- 
deep  sulcus  along  the  palatine-maxilla  su-  cisors  and  canine  above  that  of  the  postca- 
ture  to  accommodate  the  crowns  of  the  nines. 

lower  postcanines  when  the  jaw  is  closed.  The  articular  process  is  transversely  ex- 
Greater  and  lesser  palatine  foramina  are  panded,  mostly  medially,  without  evidence 
present.  of  an  articular  condyle.  The  postero ventral 
Upper  Dentition.   The  upper  dentition  angle   of  the   dentary  is   broadly  convex. 


72         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  12.     Prozostrodon  brasiliensis,  new  genus.  Right  lower  jaw  of  the  holotype  in  nnedial  view.  Note  the  incipiently  bifurcatec 
postcanine  roots. 


lacking  a  posteriorly  projecting  angular 
process.  A  coronoid  is  probably  present, 
largely  fused  to  the  medial  side  of  the  as- 
cending ramus.  The  unfused  symphysis  ex- 
hibits rugosity  indicative  of  ligamentous 
insertion,  and  a  symphysial  fossa  and  fo- 
ramen as  in  Cynognathus  (Kermack  et  al., 
1973). 

The  lower  dentition  consists  of  four  in- 
cisors, one  canine,  and  10  postcanines 
(Barberena  et  al.,  1987).  The  incisors  are 
slightly  procumbent  and  recurved,  with 
some  mesiodistal  expansion  of  the  crown 
in  the  first  three.  The  fourth  incisor  is 
shorter,  mesiodistally  narrow,  and  separat- 
ed from  the  canine  by  a  short  diastema. 

The  well-preserved  postcanines  become 
more  complex  toward  the  back  (as  is  com- 
mon in  carnivorous— insectivorous  cyno- 
donts;  Osborn  and  Crompton,  1973)  as 
well  as  increase  in  size.  The  following  ac- 
count is  based  on  the  right  postcanines. 
Lower  postcanine  1  is  small,  conical,  and 
without  accessory  cusps.  Lower  postcanine 
2  bears  a  large  main  cusp  a  with  smaller 
cusps  b  (mesially)  and  c  (distally).  A  slight 
lingual  cingulum  is  present.  On  Pcg,  cusp 
a  has  a  sharp  distal  edge,  and  cusps  b  and 
c  are  positioned  on  the  buccal  half  of  the 
tooth.  Incipient  division  of  the  root  is  ap- 
parent in  buccal  aspect.  Lower  postcanine 


4,  substantially  larger  than  preceding  post- 
canines and  also  exhibiting  incipient  root 
division,  possesses  a  (broken)  lingual  cin- 
gulum and  a  mesial  and  distal  lingual  cus- 
pule.  Lower  postcanine  5  is  mesiodistally 
longer  than  Pc^  and  has  larger  accessory 
cusps  b  and  c.  The  lingual  cingulum  is  not 
continuous  mesiodistally,  but  has  anterior 
and  posterior  sections,  each  bearing  a  cus- 
pule.  The  base  of  the  crown  is  larger  than 
the  root,  which  is  well  differentiated  from 
the  crown  and  exliibits  a  vertical  groove. 
Lower  postcanine  6,  which  is  almost  fully 
erupted,  bears  a  conical,  recurved  cusp  a, 
and  a  cusp  d  on  the  distal  margin.  Cusp  c 
is  larger  than  cusp  b.  The  cingulum,  which 
is  more  developed  than  in  the  preceding 
postcanines,  extends  along  most  of  the  lin- 
gual side  and  bears  six  cuspules.  Cusp  a  is 
broken  on  Pc-,  but  cusps  b,  c,  and  d  are 
present  and  aligned  with  the  base  of  cusp 
a.  The  lingual  cingulum  is  continuous.  The 
occlusal  surface  of  the  cingulum  and  the 
surface  above  it  suggest  abrasion  by  food 
while  chewing.  The  root  is  deeply  grooved. 
Lower  postcanine  8  is  complete,  with  ba- 
sically the  same  features  as  in  Pc-^.  Lower 
postcanine  9,  mesiodistally  the  longest 
postcanine,  has  a  proportionally  lower 
crown  as  well  as  the  lowest  cusp  a  (on  the 
left  side,   Pcg  appears  to  be  in  the  final 


Advanced  Triassic  Cynodonts  from  Brazil  •  Bonapane  and  Barberena        73 


5  mm 


10  mm 


Figure  13.  Prozostrodon  brasiliensis,  new  genus.  (A)  Cervical  centrum  in  dorsal  view.  (B)  Anterior  dorsal  vertebra  in  lateral 
view.  (C,  D,  E)  Lateral  views  of  three  neural  arcties  from  the  dorsal  series.  (F)  Incomplete  ribs.  Abbreviations:  DP,  diapophysis; 
?DP,  ?diapophysis;  NP,  contact  for  neural  pedicle;  NSP,  neural  spine;  PP,  parapophysis;  PRZ,  prezygapophysis;  PZ,  postzy- 
gapophysis;  PRZP,  prezygapophysial  process. 


Stage  of  eruption).  Seven  small  cusps  form     jected  dorsolaterally,  the  neural  canal 


the  lingual  cingulum.  The  degree  of  incip- 
ient root  bifurcation  is  greater  than  in  pre- 
ceding postcanines,  representing  a  mor- 
phological gradient  that  is  also  expressed 
in  the  increasing  complexity  of  the  cingula. 
The  right  Pc^o  is  unei"upted;  cusp  a  and 


would  have  been  relatively  wide.  The  par- 
apophyseal  facets  are  located  entirely  on 
the  anteroventral  margin  of  the  centnjm; 
there  is  no  indication  that  rib  heads 
spanned  adjacent  vertebrae. 

A  nearly  complete  anterior  dorsal  ver- 


part  of  c  are  exposed  just  below  the  groove  tebra  (Fig.  13B)  exliibits  a  parapophysis  on 

for  the  dental  lamina.  The  left  Pci,,  is  just  the  dorsolateral  region  of  the  centrum,  a 

beginning  to   eiaipt;   the   position   of  this  large    diapophysis    that    projects    laterally 

tooth  distal  to  the  end  of  the  alveolar  row  from  the  middle  of  the  pedicle,  and  a  neu- 

is   evidence   that   the   individual  was   still  ral  spine  that  is  directed  posterodorsally 

growing.  The  centrrmi  is  moderately  amphicoelous. 

Postcraniiim.  One  centrum  (Fig.  13 A)  is  The   neural   canal   is   large   but   narrower 

tentatively  considered  to  be  cervical  be-  than  the  centnnn,  differing  in  this  respect 

cause  it  is  transversely  wide  and  antero-  from  Therioherpeton  (and  possibly  reflec- 


posteriorly  short,  as  are  the  cervicals  of 
Therioherpeton.  The  facets  for  the  pedi- 
cles of  the  neural  arch  are  in  a  dorsolateral 
position;  if  the  pedicles  were  to  have  pro- 


tive  of  the  more  adult  stage  of  Prozostro- 
don; J.  A.  Hopson,  personal  communica- 
tion). 

The  dorsolumbar  region  is  further  rep- 


74         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


CAP 


B 


'I 


10  mm 


Figure  14.  Prozostrodon  brasiliensis,  new  genus.  (A)  ?Right  clavicle  in  ?posterior  view.  (B)  Interclavicle  in  dorsal  view.  (C) 
Right  humerus  in  ventral  view.  Abbreviations:  AAC,  attachment  area  for  right  clavicle;  CAP,  contact  with  acromial  process;  CI, 
contact  with  interclavicle;  DC,  deltopectoral  crest;  ECT,  ectepicondyle;  ECR,  ectepicondylar  ridge;  ENF,  entepicondylar  foramen; 
ENR,  entepicondylar  ridge;  ENT,  entepicondyle;  GT,  greater  trochanter;  HC,  humeral  capitulum;  PP,  posterior  projection. 


resented  by  an  incomplete  vertebra  and 
four  incomplete  neural  arches.  The  former 
has  a  massive  centrum  with  marked  am- 
phicoely.  The  transverse  processes  are  di- 
rected laterally  and  the  broken  base  of  the 
neural  spine  indicates  that  the  spine  was 
directed  posterodorsally.  The  neural  canal 
is  large  but  narrower  than  the  centrum. 
StiTictural  variations  in  the  spinous  pro- 
cesses and  zygapophyses  are  evidence  of 
regional  variation  along  the  dorsolumbar 
column. 

In  one  neural  arch  (Fig.  13C),  the  ro- 
bust prezygapophyses  are  positioned  more 
ventrally  than  the  postzygapophyses; 
postzygapophyseal  facets  are  anteroposte- 
riorly  elongate  and  transversely  convex, 
possibly  representing  a  specialization  for 
dorsoventral  flexure  of  the  vertebral  col- 
umn (J.  A.  Hopson,  personal  communica- 
tion). The  neural  spine,  with  almost  par- 
allel anterior  and  posterior  borders,  is  pos- 
terodorsally directed,  and  more  steeply  in- 
clined than  in  Exaeretodon  (Bonaparte, 
1963).  Another  neural  arch  (Fig.  13E)  has 


a  similarly  elongate  set  of  postzygapophys- 
es with  convex  facets,  and  prezygapophys- 
es with  transversely  concave  facets.  Jenkins 
and  Parrington  (1976,  figs.  2A-D)  illus- 
trated a  neural  arch  in  Morganucodon  with 
zygapophyses  and  a  neural  spine  of  com- 
parable structure. 

A  different  type  of  dorsal  vertebra  (Fig. 
13D),  represented  by  two  neural  arches, 
possibly  derives  from  a  position  posterior 
to  those  described  above.  The  zygapophy- 
seal  facets  have  less  curvature  and  the 
damaged  neural  spine  appears  to  be  short- 
er than  in  the  previously  described  neural 
arches. 

Ribs  (Fig.  13F).  Eight  to  10  ribs  are  rep- 
resented by  20  fraginents,  and  none  show 
any  indication  of  processes  or  expansions. 
Most  are  figure  8— shaped  in  cross  section. 

Clavicle  (Fig.  14 A).  Most  of  the  Pright 
clavicle  is  present.  On  the  proximal  end 
are  furrowlike  rugosities  representing  the 
area  of  attachment  with  the  interclavicle. 
The  wide  distal  end  is  complexly  config- 
ured with  surfaces  representing  the  aero- 


Advanced  Triassic  Cynodonts  from  Brazil  •  Bonaparte  and  Barberena        75 


mial  attachment.  The  greatest  curvature  of 
the  shaft  is  closer  to  the  distal  end. 

Interclavicle  {Fig.  14B).  This  Y-shaped 
eleinent,  with  broad  anterolateral  exten- 
sions for  reception  of  the  clavicles,  is  an- 
teroposteriorly  shorter  (19  mm)  than  wide 
(23  mm).  The  ventral  surface  is  not  ex- 
posed. 

Scapulocoracoid.  These  bones  are  rep- 
resented only  by  small  fragments  that  are 
too  fragmentary  to  provide  useful  infor- 
mation on  the  glenoid  and  other  features 
of  interest. 

Huiiienis  (Fig.  14C).  The  left  humerus  is 
represented  by  the  proximal  half,  including 
the  deltopectoral  crest  and  the  humeral 
head.  The  right  humenis  is  almost  com- 
plete, lacking  only  tlie  humeral  head  and 
part  of  the  proximal  end,  and  a  small  por- 
tion of  the  distal  end  including  the  articular 
surface  for  the  ulna.  The  humerus  is  struc- 
turally no  more  derived  than  that  of  Exaer- 
etodon,  and  is  similar  to  that  of  Probeleso- 
don  lewisi  (Romer  and  Lewis,  1973).  The 
entepicondylar  foramen  is  very  large,  and 
opens  distally  into  a  deep  sulcus  that  con- 
tinues to  the  entepicondylar  terminus.  The 
entepicondyle,  which  is  larger  than  the  ec- 
tepicondyle,  terminates  in  a  distinct  projec- 
tion. Near  the  anterior  margin  that  extends 
proximally  from  the  ectepicondyle  is  a  small 
ectepicondylar  foramen;  this  margin  ex- 
tends farther  proximally  onto  the  diaphysis 
than  does  the  comparable  margin  from  the 
entepicondyle. 

Ilium  (Fig.  15A).  The  right  ilium  is  al- 
most complete  except  for  the  most  anterior 
end  of  the  iliac  blade.  The  neck  above  the 
acetabulum  is  well  defined,  and  the  poste- 
rior end  of  the  iliac  blade  bears  a  veiy  short 
process.  Both  of  these  features  are  derived 
compared  with  the  structure  seen  in  TJiri- 
naxodon  and  CynognatJms  (Jenkins,  1971) 
and  in  Exaeretodon  (Bonaparte,  1963).  The 
outer  surface  of  the  iHac  blade  is  largely 
convex  dorsoventrally,  not  concave  as  in  the 
above  cited  cynodonts,  and  its  dorsal  and 
ventral  borders  are  nearly  parallel  to  one 
anotlier 

Foot  (Figs:  15B,  C).  The  right  hind  foot 


is  complete,  except  for  the  lateral  part  of 
the  calcaneum.  The  superposition  of  as- 
tragalus and  calcaneum  appears  to  be  of 
the  type  present  in  Exaeretodon  (Bona- 
parte, 1963),  defined  by  Jenkins  (1971)  as 
the  "therapsid  type  of  plantigrady"  How- 
ever, the  metatarsals  and  phalanges  are 
proportionally  longer  than  in  Exaeretodon. 
The  phalangeal  formula  is  2-3-3-3-3. 

Comparison  of  Prozostrodon  with  other 
Cynodonts.  The  referral  of  PV  0248T  to 
the  genus  Thrinaxodon  by  Barberena  et  al. 
(1987)  is  untenable,  as  pointed  out  by  Bat- 
tail  (1991),  who  interpreted  the  specimen 
as  a  chiniquodontid.  The  following  derived 
characters  present  in  the  holotype  of  Pro- 
zostrodon brasiliensis  are  not  found  in 
specimens  of  Thrinaxodon  from  the  Early 
Triassic  of  South  Africa  (Parrington,  1946; 
Estes,  1961)  and  Antarctica  (Colbert  and 
Kitching,  1977). 

1)  Frontal  bordering  the  orbit  (also  in 
Therioherpeton,  tritheledontids,  and 
tritylodontids). 

2)  Contact  between  the  ventral  process  of 
frontal  and  dorsal  process  of  palatine 
(also  in  tritheledontids  and  tritylodon- 
tids; additionally  present  in  Probainog- 
nathtts,  Ecteninion,  and  chiniquodon- 
tids;  J.  A.  Hopson,  personal  communi- 
cation). 

3)  Presence  of  an  orbitosphenoid  contact- 
ing frontal  and  palatine,  and  medially 
placed  relative  to  the  dorsal  process  of 
the  palatine  (also  in  Morganucodon; 
Kermack  et  al,  1981). 

4)  Secondary  bony  palate  with  large  pal- 
atines that  extend  to  the  level  of  the  last 
postcanine. 

5)  Incipient  bifurcation  of  the  roots  in  the 
upper  and  lower  postcanines. 

6)  Small  postorbital  and  prefrontal. 

7)  Absence  of  postorbital  bar  (also  in 
Therioherpeton,  tritheledontids,  and 
tritylodontids). 

8)  Large  infraorbital  and  two  well-defined 
foramina  for  the  trigeminal  nerve  in  the 
maxilla  (also  in  tritheledontids  and  tri- 
tylodontids). 


76         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  15.  Prozostrodon  brasiliensis,  new  genus.  (A)  Incomplete  right  ilium  in  lateral  view.  (B)  Right  foot  as  preserved.  (C) 
Reconstruction  of  right  foot  in  dorsal  view.  Abbreviations:  A,  acetabular  area;  AST,  astragalus;  CAL,  calcaneum;  C,  cuneiform; 
EC,  ectocuneiform;  ENC,  entocuneiform;  IC,  ischial  contact;  IB,  iliac  blade;  MC,  mesocuneiform;  NAV,  navicular;  PC,  pubis 
contact;  PP,  posterior  process  of  the  ilium;  l-V,  metatarsals  I  through  V. 


This  combination  of  derived  characters  dontidae,  and  Probainognathidae.  The  lack 

precludes  referral  of  Prozostrodon  brasi-  of  gliriform  specialization  in  the  incisors 

liensis  not  only  to  the  Thrinaxodontidae,  and   the   transversely  narrow  postcanines 

but  also  to  the  Cynognathidae,  Chiniquo-  preclude  referral  of  the  specimen  to  the 


Advanced  Triassic  Cynodonts  from  Brazil  •  Bonaparte  and  Barberena 


1 1 


Tritheledontidae   or   to   any   gomphodont 
family,  including  the  Tritylodontidae. 

A  Summary  of  the  Distinctive  Features 
of  Prozostrodon.  In  addition  to  the  char- 
acters listed  above  as  well  as  in  the  diag- 
nosis, Prozostrodon  possesses  other  dis- 
tinctive features.  Although  many  of  these 
features  may  be  found  among  various  oth- 
er taxa,  only  in  Prozostrodon,  as  far  as  we 
are  aware,  do  they  occur  together.  The 
suite  is  as  follows. 

1)  Reduced  unossified  area  between 
frontal,  orbitosphenoid,  and  alisphe- 
noid  (also  in  tritylodontids  and  Ecten- 
inion;  Martinez  et  al.,  1996). 

2)  Sphenopalatine  foramen  within  the 
posterior  portion  of  the  dorsal  process 
of  palatine. 

3)  Anteroposteriorly  long  palatines  in  the 
secondary  bony  palate  (also  in  chini- 
quodontids,  tritheledontids,  and  some 
tritylodontids). 

4)  Root  of  the  zygomatic  arch  distinctly 
offset  from  the  posterior  margin  of 
the  maxilla  (also  in  Probainognathus, 
chiniquodontids,  tritylodontids,  trav- 
ersodontids,  and  diademodontids). 

5)  Carnivorous— insectivorous  dentition 
comparable  in  general  moi-phology  to 
that  of  Thrinaxodon  and  Morganuco- 
don,  but  with  cingula  on  the  upper 
postcanines  that  are  either  poorly  de- 
veloped or  absent  altogether 

6)  Posterior  portion  of  the  upper  tooth 
row  inset  from  the  lateral  border  of 
the  maxilla  (also  in  traversodontids, 
tritylodontids,  tritheledontids,  and 
Probainognathus ) . 

7)  Incipient  bifurcation  of  the  upper 
postcanine  roots. 

8)  Incipient  bifurcation  of  the  lower 
postcanine  roots  (also  in  Pachygenehis 
and  Microconodon;  H.-D.  Sues,  per- 
sonal communication;  and  in  Therio- 
herpeton) . 

9)  Mandibular  symphysis  unfused,  an- 
teroposteriorly elongated,  dorsoven- 
trally  narrow  (as  in  Thrinaxodon 
[primitive],  tritheledontids,  and  trity- 


lodontids [derived];  J.  A.  Hopson,  per- 
sonal communication). 

10)  Presence  of  symphysial  fossa  and  fo- 
ramen in  the  lower  jaw  (also  in  Cy- 
nognathus;  Kermack  et  al.,  1973). 

11)  Articular  process  of  the  dentary  ex- 
tended posteriorly  and  expanded 
transversely,  without  indication  of  a 
condyle,  and  set  above  the  level  of  the 
postcanine  teeth  (a  feature  of  derived 
cynodonts;  J.  A.  Hopson  personal 
communication). 

12)  Cervical  centra  anteroposteriorly 
short,  transversely  wide,  and  dorso- 
ventrally  low  (also  in  tritylodontids 
and  Morganucodon) . 

DISCUSSION 

The  specimens  of  Therioherpeton  (skull 
length,  38  mm)  and  Prozostrodon  (skull 
length  estimated  to  be  67  mm)  are  rela- 
tively small,  and  consideration  should  be 
given  to  whether  the  smaller  of  the  two 
represents  a  juvenile  individual.  Four  fea- 
tures of  Therioherpeton,  in  comparison  to 
those  in  Prozostrodon,  might  be  interpret- 
ed as  evidence  of  immaturity:  the  frontals 
extend  further  posteriorly;  the  anterior 
portion  of  the  braincase  is  proportionally 
wider;  the  postcanines  lack  cingula;  the 
neural  canals  of  presacral  vertebrae  are 
proportionally  larger.  However,  the  possi- 
bility that  these  are  juvenile  characters  is 
contradicted  by  the  state  of  ossification  in 
the  postcranium  of  Therioherpeton.  With 
the  exception  of  the  pelvis,  in  which  the 
three  elements  are  not  synostosed,  we  find 
no  evidence  of  a  subadult  condition.  Fur- 
thermore, Therioherpeton  does  not  exliibit 
the  proportionately  large  orbital  size  that 
is  characteristic  of  juvenile  individuals.  A 
juvenile  skull  of  cf.  Probainognathus  (Bon- 
aparte and  Crompton,  1994,  figs.  1,  2)  of 
comparable  length  (39  mm)  to  that  of 
Therioherpeton  exliibits  a  skull  to  orbit  ra- 
tio of  3.5,  versus  an  estimated  5.0  for  Ther- 
ioherpeton. In  a  putatively  inature  skull  of 
Probainognathus  (Romer,  1970,  fig.  2)  the 
ratio  of  skull  to  orbital  length  is  6,  only 
slightly  greater  than  in  Therioherpeton.  Al- 


78        Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


c 


HZ 


Thrinaxodon 

Lumkuia 

Probainognathus 

Ecteninion 

Probelesodon 

Aleodon 

Chiniquodon 

Prozostrodon 

Therioherpeton 

Pachygenelus 

Morganucodon 

Cynognathus 

Gomphodontia 


Figure  16.  The  hypothesized  phylogenetic  positions  of  Ther- 
ioherpeton and  Prozostrodon.  The  cladogram  was  generated 
by  Dr.  J.  A.  Hopson,  who  incorporated  information  from  the 
Brazilian  genera  described  in  this  paper  into  his  data  set  of 
cynodont  characters. 


though  we  do  not  beheve  that  the  type  of 
Therioheiyeton  represents  a  juvenile,  we 
remain  open  to  the  possibiUt^'  that  the  four 
characters  cited  above  eventually  might  be 
shown  to  be  juvenile  characters  retained 
in  adulthood. 

The  hypothesized  relationships  of  Ther- 
ioJierpeton  and  Prozostrodon  are  depicted 
in  Figure  16.  The  relative  positions  in  the 
cladogram  of  the  two  genera  seem  due  to 
the  persistence  of  a  prefrontal  and  post- 
orbital  and  the  shorter  posterior  projection 
of  the  frontal  in  Prozostrodon,  and  to  the 
more  derived  characters  present  in  the 
pelvis  and  proxiinal  feinur  of  Therioher- 
peton. 

The  materials  of  Therioheiyeton  and 
Prozostrodon,  although  incomplete,  pro- 
vide new  anatomical  information  to  fur- 
ther elucidate  the  complex  transition  be- 
tween cynodonts  and  primitive  mammals. 
The  taxa  described  here  support  the  hy- 
pothesis that  the  ancestry  of  mammals  lay 
among  the  clade  of  carnivorous— insectiv- 
orous cynodonts  (Hopson,  1991,  1994; 
Hopson  and  Kitching,  2001),  rather  than 
among    goinphodont    cynodonts,    and    in 


particular  the  Tritylodontidae  (Kemp, 
1982,  1983).  Sues  (1985)  reviewed  in  de- 
tail most  of  the  synapomorphies  that 
Kemp  (1982,  1983)  proposed  in  support  of 
his  interpretation  that  tritylodontids  and 
primitive  mammals  were  closely  related, 
and  concluded  that  many  of  these  pur- 
portedly shared  derived  features  are  either 
superficial  similarities,  are  symplesio- 
morphic,  or  are  the  result  of  parallel  de- 
velopment but  which,  nonetheless,  evi- 
dence structural  differences. 

We  regard  the  dentition  o{  Prozostrodon 
as  iTioi"phologically  intermediate  between 
that  of  Thrinaxodon  liorhinus  from  the 
Early  Triassic  and  those  evolved  among 
Late  Triassic  and  Early  Jurassic  morganu- 
codontids.  Although  tritheledontids  such 
as  Pachygenelus  have  been  considered  as 
closely  related  to  mammals  (Hopson  and 
Barghusen,  1986),  and  are  represented 
cladistically  as  the  sister  taxon  to  mainmals 
(Fig.  16;  see  also  Shubin  et  al.,  1991),  we 
interpret  the  tritheledontid  dentition  as 
derived,  particularly  with  respect  to  the 
buccolingual  expansion  of  the  upper  post- 
canines.  In  contrast,  the  entire  dentition  of 
Prozostrodon  (and  what  is  known  of  that 
of  Therioherpeton)  is  substantially  similar 
to  that  in  morganucodontids,  with  only 
slight  differences  in  the  development  of 
upper  postcanine  cingula.  During  a  span 
of  time  that  witnessed  major  modifications 
in  cranial  and  postcranial  morphology, 
dental  patterns  were  fundamentally  con- 
served. 

ACKNOWLEDGMENTS 

Drafts  of  this  paper  were  critically  re- 
viewed by  Drs.  Z.  Kielan-Jaworowska,  G. 
W.  Rougier,  H.-D.  Sues,  and  J.  A.  Hopson. 
Very  special  thanks  are  accorded  Dr.  J.  A. 
Hopson  for  his  generous  help  and  advice 
on  improvements,  and  for  the  use  of  his 
database  in  the  cladogram  presented  here. 
We  also  thank  Drs.  F.  A.  Jenkins,  Jr.,  and 
M.  D.  Shapiro  for  editorial  assistance.  The 
senior  author  expresses  gratitude  to  two 
colleagues  at  the  Fundacao  Zoobotanica 
de  Porto  Alegre,  Brazil:  Dr.  ].  Ferigolo  for 


Advanced  Triassic  Cynodonts  from  Brazil  •  Bonaparte  and  Barberena        79 


interesting  discussions  on  the  subject;  and 
Ana  M.  Riveiro  for  field  and  laboratory  as- 
sistance. The  senior  author  is  also  grateful 
to  the  CNPq.  of  Brazil,  and  to  the  Museo 
Argentino  de  Ciencias  Naturales,  Buenos 
Aires,  for  support  in  developing  most  of 
this  research  in  the  Museu  de  Ciencias 
Naturais  de  Porto  Alegre,  Brazil. 

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Shapiro,  M.  D.,  and  F.  A.  Jenkins,  Jr.  2001.  A  cy- 
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Shubin,  N.  H.,  a.  W.  Crompton,  H.-D.  Sues,  and 
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dontidae  (Synapsida).  Zoological  Journal  of  the 
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ca,  B  27:  270-284. 


THE  INNER  EAR  AND  ITS  BONY  HOUSING  IN  TRITYLODONTIDS 
AND  IMPLICATIONS  FOR  EVOLUTION  OF  THE  MAMMALIAN  EAR 


ZHEXI  LUO^ 

Abstract.  The  inner  ear  structures  underwent  fun- 
damental changes  during  the  evolution  from  non- 
mammalian  cynodonts  ("mammallike  reptiles")  to 
earlv  mammals.  The  petrosal  bone  in  mammals  has 
an  enlarged  pars  cochlearis  containing  an  elongate 
cochlea.  The  elongation  of  the  bony  cochlear  canal  is 
usually  correlated  with  the  development  of  a  ventral 
eminence  of  the  pars  cochlearis,  known  as  the  pro- 
montorium.  Both  cochlear  canal  and  promontorium 
are  regarded  as  apomorphies  of  mammals.  In  con- 
trast, nonmammalian  cynodonts  lack  the  promonto- 
rium. If  present  at  all,  the  bony  cochlear  recess  is 
small,  globular,  and  poorly  differentiated  from  the 
vestibule  in  most  cynodonts.  The  trit)'lodontid  Yun- 
nanodon  has  an  intermediate  condition.  Unlike  most 
nonmammalian  cynodonts,  Yiinnanodon  has  a  dis- 
tinctive cochlear  canal  in  an  enlarged  pars  cochlearis, 
but  it  lacks  the  promontorium  and  retains  the  basi- 
sphenoid  wing,  a  primitive  feature  of  many  cyno- 
donts. These  characters  in  tritylodontids  suggest  that 
a  distinctive  cochlear  canal  in  an  enlarged  pars  coch- 
learis probably  evolved  in  the  common  ancestor  to 
trit^'lodontids,  tritheledontids,  and  mammahaforms, 
and  before  the  emergence  of  the  petrosal  promon- 
torium in  mammaliaforms.  The  promontorium  sub- 
sequently formed  by  the  displacement  of  the  neigh- 
boring parasphenoid-basisphenoid  complex  and  ba- 
sioccipital  bone  by  the  pars  cochlearis  in  the  early 
evolution  of  mammaliaforms. 

INTRODUCTION 

The  bony  structure  surrounding  the  in- 
ner ear  differs  between  mammals  and 
nonmammahan  cynodonts.  The  inner  ear 
of  cynodonts  is  enclosed  by  the  prootic 
and  the  opisthotic,  known  collectively  as 
the  periotic  bones,  as  well  as  by  the  ex- 
occipital  and  the  basioccipital.  The  basi- 
sphenoid  wing  (or  parasphenoid  ala), 
which  is  a  large  coinponent  of  the  paras- 


'  Section  of  \'ertebrate  Paleontology,  Carnegie  Mu- 
seum of  Natural  History,  Pittsburgh,  Pennsylvania 
1521.3. 


penoid-basisphenoid  complex,  overlaps 
the  prootic  and  indirectly  contributes  to 
the  cochlear  housing.  The  bony  housing 
for  the  inner  ear  in  cynodonts  is  formed 
by  multiple  bones,  as  documented  in  great 
detail  for  Thrinaxodon  (Olson,  1944;  Es- 
tes,  1961;  Fourie,  1974;  Rowe  et  al,  1993), 
Probelesodon,  Massetognathus  (Quiroga, 
1979),  and  Probainognathiis  (Allin,  1986). 
This  mosaic  pattern  is  primitive  for  cyno- 
donts because  it  is  also  present,  albeit  in  a 
slightly  different  condition,  in  noncyno- 
dont  therapsids  (Olson,  1944;  Cox,  1962; 
Sigogneau,  1974). 

In  contrast,  the  bony  housing  of  the  in- 
ner ear  in  early  mammaliaforms  (inodified 
from  Rowe  [1988]  to  include  Adelobasi- 
leus  and  Sinoconodon)  is  formed  exclusive- 
ly by  the  petrosal,  which  is  the  single  bone 
composed  of  the  fused  prootic  and  opis- 
thotic elements  of  nonmammalian  cyno- 
donts (Kermack  et  al.,  1981;  Rowe,  1988; 
Luo  et  al.,  1995).  The  parasphenoid-basi- 
sphenoid coinplex,  the  basioccipital,  and 
the  exoccipital  are  excluded  by  an  enlarged 
petrosal  from  the  bony  housing  for  the  in- 
ner ear,  as  has  been  docuinented  in  a  wide 
range  of  mammaliaforms  and  early  main- 
mals,  such  as  Sinoconodon  (Luo  et  al., 
1995),  morganucodontids  (Kermack  et  al., 
1981;  Gow,  1985;  Graybeal  et  al,  1989; 
Luo  and  Ketten,  1991;  Crompton  and 
Luo,  1993),  triconodontids  (Kermack, 
1963;  Crompton  and  Luo,  1993;  Rougier 
et  al.,  1996),  docodonts  (Lillegraven  and 
Krusat,  1991),  monotremes  (Kuhn,  1971; 
Zeller,  1989;  Luo  and  Ketten,  1991;  Fox 
and  Meng,  1997),  multituberculates 
(Miao,  1988;  Luo  and  Ketten,  1991;  Lil- 


Bull.  Mus.  Comp.  ZooL,  156(1):  81-97,  October,  2001         81 


82 


Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No. 


legraven  and  Hahn,  1993;  Meng  and  Wyss, 
1995;  Fox  and  Meng,  1997;  Hurum,  1998), 
and  archaic  therians  (Wible  et  al.,  1995; 
Hu  et  al.,  1997).  In  mammals,  the  pars 
cochlearis  that  contains  the  cochlear  canal 
is  much  larger  than  in  cynodonts,  forming 
a  ventrolateral  eminence  known  as  the 
promontorium,  which  is  a  very  conspicu- 
ous external  feature  in  the  mammalian 
basicranium  (Gow,  1985;  Hopson  and  Bar- 
ghusen,  1986;  Rowe,  1988;  Luo  et  al., 
1995). 

Mammals  and  nonmammalian  cyno- 
donts differ  also  in  features  of  the  inner 
ear.  In  the  noncynodont  therapsids,  such 
as  dicynodonts  (Cox,  1962)  and  gorgon- 
opsids  (Sigogneau,  1974),  the  sacculococh- 
lear  cavity  (or  recess)  is  not  differentiated 
from  the  vestibular  cavity  (Olson,  1944; 
Cox,  1962;  Sigogneau,  1974).  At  the  an- 
terior end  of  this  sacculocochlear  cavity  is 
the  fenestra  vestibuli  or  oval  window, 
which  accommodates  the  stapes  that  trans- 
mitted sound  vibrations  from  the  middle 
to  the  inner  ear.  The  cochlear  part  of  the 
osseous  inner  ear  is  more  distinctive  from 
the  vestibule  in  primitive  cynodonts  such 
as  Thrinaxodon  (Estes,  1961;  Fourie, 
1974).  In  advanced  cynodonts  (Quiroga, 
1979;  Allin  and  Hopson,  1992),  the  bony 
cochlear  structure  is  more  developed  than 
in  Thrinaxodon  and  noncynodont  therap- 
sids. The  bony  cochlea  is  represented  by  a 
small  and  globular  cavity  but  is  too  short 
to  be  termed  the  cochlear  canal  (except  for 
tritylodontids,  and  perhaps  tritheledontids; 
see  below). 

In  contrast,  in  Early  Jurassic  mammalia- 
forms,  the  cochlear  canal  is  elongate  and 
differentiated  from  the  saccular  cavity 
(Graybeal  et  al.,  1989;  Luo  and  Ketten, 
1991;  Luo  et  al,  1995).  The  elongate  co- 
chlear canal  is  a  shared  derived  feature  of 
diverse  mammalian  groups  during  the  Me- 
sozoic,  as  documented  in  multitubercula- 
tes  (Miao,  1988;  Luo  and  Ketten,  1991; 
Lillegraven  and  Hahn,  1993;  Meng  and 
Wyss,  1995;  Fox  and  Meng,  1997;  Hurum, 
1998),  docodonts  (Lillegraven  and  Krusat, 
1991),  and  possibly  in  symmetrodont  ther- 


ians (Wible  et  al,  1995;  Hu  et  al.,  1997). 
The  elongate  bony  cochlear  canal  suggests 
a  better-developed  cochlear  duct,  which 
may  indicate  a  better  sensitivity  to  high- 
frequency  sound  that  is  very  important  in 
the  hearing  function  of  all  extant  mam- 
mals, and  probably  important  for  at  least 
some  of  the  earliest  mammals  (Rosowski 
and  Graybeal,  1991;  Rosowski,  1992;  Hu- 
rum, 1998). 

Given  these  differences  in  the  structure 
of  the  inner  ear  and  its  bony  housing  be- 
tween mamiuals  on  the  one  hand  and  non- 
mammalian  cynodonts  on  the  other,  the 
ear  structures  must  have  undergone  exten- 
sive transformation  during  the  early  evo- 
lution of  mammals  after  their  divergence 
from  nonmammalian  cynodonts.  To  eluci- 
date the  pattern  of  this  phylogenetic  trans- 
formation, it  is  essential  to  obtain  some  de- 
tailed anatomical  information  on  the  inner 
ear  and  the  surrounding  bones  in  such  de- 
rived cynodonts  as  tritylodontids  and  tri- 
theledontids. Some  earlier  studies  of  the 
ear  region  of  tritylodontids  reported  the 
presence  of  a  cochlear  canal  (Kiihne,  1956; 
Hopson,  1965).  Two  additional  studies 
(Gow,  1986;  Sun  and  Cui,  1987)  offered 
observations  on  the  basicranial  structures 
surrounding  the  inner  ear.  This  paper  de- 
scribes the  inner  ear  and  its  bony  housing 
in  the  tritylodontid  Yunnanodon,  and  their 
anatomical  relationships  as  revealed  by  se- 
rial sections.  The  new  information  has  im- 
plications for  the  evolution  of  the  ear  re- 
gion through  the  transition  from  nonmam- 
malian cynodonts  to  mammals,  given  the 
fact  that  tritylodontids  are  considered  by 
some  to  be  closely  related  to  mammals 
(Kemp,  1983;  Rowe,  1988;  Wible,  1991; 
Wible  and  Hopson,  1993;  Luo,  1994;  Luo 
and  Crompton,  1994;  but  see  the  alterna- 
tive phylogeny  by  Crompton  [1972],  Sues 
[1985a],  and  Hopson  and  Barghusen 
[1986]). 

MATERIALS  AND  METHODS 

Fossil  remains  of  Yunnanodon  (Cyno- 
dontia,  Tritylodontidae)  are  from  the  Up- 
per Red  Beds  of  the  Lower  Lufeng  For- 


mation    of   Yunnan,    China    (Sun    et    al., 
1985),  which  is  considered  to  be  Early  Ju- 

Irassic  (Sinemurian  to  Phensbachian)  by  re- 
cent studies  (Luo  and  Sun,  1993;  Luo  and 
Wu,  1995).  Yunnanodon  is  the  smallest  tri- 
tylodontid  known  from  the  Lower  Lufeng 
Formation  (Cui,  1976,  1986;  Luo  and  Wu, 
J  1994),  with  a  skull  length  ranging  from  36 
'  to  47  mm.  Yunnanodon  has  only  two  cusps 
in  the  lingual  row  of  the  upper  postcani- 
nes,  the  main  diagnostic  character  distin- 
guishing this  taxon  from  other  tritylodon- 
tids  in  the  Lower  Lufeng,  all  of  which  have 
three  lingual  cusps  on  the  upper  teeth 
(Cui,  1976;  Luo  and  Wu,  1994).  Yunnan- 
odon is  comparable  to  Dinnebitodon  from 
ll  the  Kayenta  Formation  of  Arizona  (Sues, 
1985b)  in  some  derived  dental  characters 
(Luo  and  Wu,  1995). 

Several  skull  specimens  of  Yunnanodon 
(Cui,  1976;  Sun  and  Cui,  1987)  were  re- 
examined in  tliis  study  (Institute  of  Verte- 
ij  brate  Paleontology  and  Paleoanthropology, 
'I  Beijing:  IVPP  5071  [holotype];  7204;  7205; 
7219).  A  duplicate  skull  (courtesy  of  A.-L. 
Sun)  was  sectioned  by  using  a  Croft  Grind- 
er to  expose  its  internal  structures  (Croft, 
1950;  Crompton,  1955).  Camera  lucida 
drawings  and  photographs  were  taken  of 
each  serial  (transverse)  section  exposed  by 
grinding,  in  the  place  of  the  original  spec- 
imen. The  reconstruction  of  the  basicranial 
bones  and  the  inner  ear  was  made  from  the 
serial  sections  by  using  the  Slicer  Dicer® 
program  by  Visualogic,  Inc.,  Bellevue, 
Washington.  Measurement  of  the  length 
and  internal  diameters  of  the  cochlear  canal 
was  based  on  the  original  sections  (camera 
lucida  drawing  and  photos,  both  with 
scales).  The  measurement  of  the  internal 
diameter  of  the  semicircular  canal  was 
made  from  the  original  sections.  The  di- 
ameter of  the  arc  of  the  semicircular  canal 
{sensu  Hurum,  1998)  was  taken  from  the 
graphic  models  of  inner  ear  endocasts  as 
rendered  by  the  Slicer  Dicer  program. 

DESCRIPTION  AND  COMPARISON 

Petrosal 

The  petrosal  forms  the  bony  housing  for 
the  entire  inner  ear  in  Yunnanodon.  The 


Tritylodontid  Inner  Ear  •  Luo        83 


petrosal  excludes  all  other  bones  from  the 
immediate  bony  housing  of  the  inner  ear. 
No  suture  marks  the  separation  of  the  two 
periotic  bones  (prootic  and  opisthotic)  in 
Yunnanodon  (Figs.  1,  2).  This  has  been 
documented  in  other  tritylodontids  (Kii- 
hne,  1956;  Hopson,  1964,  1965;  Sun, 
1984;  Cow,  1986;  Sues,  1986).  The  ossifi- 
cation of  the  cartilaginous  otic  capsule  of 
the  chondrocranium  begins  in  several  os- 
sification centers  in  amniotes  (de  Beer, 
1937).  The  absence  of  the  prootic-opis- 
thotic  suture  implies  that  the  separate  em- 
bryonic ossification  centers  coalesced  into 
a  single  bone  in  adult  tritylodontids,  in- 
stead of  two  separate  prootic  and  opis- 
thotic bones  of  other  therapsids  (Olson, 
1944)  and  extant  diapsid  reptiles  (de  Beer, 
1937).  The  absence  of  the  prootic— opis- 
thotic suture  in  tritylodontids  is  a  derived 
condition  in  comparison  to  many  other 
nonmammalian  cynodonts,  as  pointed  out 
by  many  authors  (Kemp,  1983;  Sun,  1984; 
Hopson  and  Barghusen,  1986;  Sues,  1986; 
Rowe,  1988;  Wible,  1991;  Luo,  1994). 

The  pars  cochlearis  that  encloses  the 
bony  cochlear  canal  is  large  relative  to  the 
rest  of  the  petrosal,  as  shown  in  the  serial 
sections  and  in  the  broken  basicranial 
specimens  (e.g.,  IVPP  5071  as  described 
by  Sun  and  Cui  [1987]).  The  promonto- 
rium,  defined  as  the  ventral  eminence  of 
the  pars  cochlearis  in  extant  mammals 
{sensu  Williams  et  al.  [1989]  and  Luo  et 
al.  [1995]),  is  represented  by  a  bulging 
area  posterior  to  the  basisphenoid  wing 
and  anterior  to  the  crista  interfenestralis  in 
the  skull  with  an  incomplete  basisphenoid 
wing  (Fig.  2).  In  a  more  or  less  intact  bas- 
icranium  (IVPP  7219),  the  medial  part  of 
the  pars  cochlearis  is  covered  medially  by 
the  basioccipital,  and  anteriorly  by  the  ba- 
sisphenoid wing  (more  details  below).  The 
ventral  (and  external)  exposure  of  the  pars 
cochlearis  in  the  intact  skulls  appears  to  be 
much  smaller  than  its  entire  size  (Fig.  1) 
because  much  of  the  pars  cochlearis  is  su- 
perficially covered  by  the  sphenoid  com- 
plex and  the  basioccipital  bone. 

In  some  possibly  juvenile  skulls  in  which 


84         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  1.  Basicranium  and  inner  ear  of  Yunnanodon  (Tritylodontidae,  Cynodontia)  in  ventral  views.  (A)  Basicranium  and  its 
position  in  sl<ull  (ventral  view  of  basicranium;  the  squamosal  is  not  illustrated  in  the  stipple  drawing;  modified  from  Luo  [1994]; 
skull  outline  modified  from  Cui  [1976]  and  Luo  and  Wu  [1994]).  (B)  Approximate  position  of  the  inner  ear  (purple)  to  the  sur- 


Tritylodontid  Inner  Ear  •  Luo 


85 


the  petrosal,  the  basisphenoid,  and  the  ba- 
sioccipital  are  separated  from  one  another, 
the  pars  cochlearis  can  be  broadly  ex- 
posed. This  led  Sun  and  Cui  (1987)  to  sug- 
gest that  Yunnanodon  developed  a  pro- 
montoriumlike  structure  (  =  the  pars  coch- 
learis), an  observation  that  is  confirmed 
here.  The  medial  aspect  of  the  pars  coch- 
learis has  a  flat  facet  that  may  be  exposed 
in  some  specimens  in  which  the  basioccip- 
ital  has  become  detached  from  the  basi- 
cranium.  This  facet  appears  to  be  identical 
to  the  medial  facet  of  the  promontorium 
in  Sinoconodon  (Crompton  and  Luo,  1993; 
Luo  et  al.,  1995).  The  overlap  of  this  flat 
facet  by  the  lateral  lappet  of  the  basioccip- 
ital  in  the  intact  skulls  is  very  similar  to  the 
condition  in  subadult  specimens  of  Sino- 
conodon. 

The  fenestra  vestibuli  (oval  window)  is 
oval  in  outline,  with  a  long  diameter  of 
—  1.8  mm  and  a  short  diameter  of  —1.5 
mm  (based  on  IVPP  7219).  The  fenestra 
vestibuli  is  separated  by  a  thin  crista  in- 
terfenestralis  from  the  perilymphatic  fo- 
ramen (round  window  or  foramen  cochle- 
ae). The  latter  is  located  in  the  same  de- 
pression as  (but  separated  from)  the  jug- 
ular foramen.  The  lateral  trough  of  the 
petrosal  is  bound  medially  by  the  pars 
cochlearis  and  laterally  by  the  lateral 
flange.  The  large  ventral  opening  of  the 
cavum  epiptericum  is  anterior  to  the  lat- 
eral trough.  The  facial  foramen  is  located 
anterior  to  the  fenestra  vestibuli.  The  lat- 
eral flange  is  perforated  by  two  vascular 
foramina.  The  pterygoparoccipital  fora- 
men, which  probably  carried  the  superior 
ramus  of  the  stapedial  artery  (Wible  and 
Hopson,  1995),  is  posterior  to  the  lateral 
flange.  The  anterior  paroccipital  process  of 


the  petrosal  is  bulbous.  It  supports  the 
quadrate  in  the  intact  skull.  The  posterior 
paroccipital  process  is  represented  by  a 
horizontal  ridge  with  a  free-standing  lat- 
eral (distal)  end.  The  anterior  and  poste- 
rior paroccipital  processes  are  separated 
by  the  stapedial  muscle  fossa  and  its  as- 
sociated groove.  The  dorsal  aspects  of  the 
anterior  and  posterior  paroccipital  pro- 
cesses are  in  contact  with  the  squamosal 
(Figs.  1,  2).  These  petrosal  features  are 
characteristic  of  all  tritylodontids.  The  tab- 
ular bone  is  present  on  the  occiput,  cov- 
ering much  of  the  mastoid  part  of  the  pe- 
trosal posteriorly.  This  primitive  feature  is 
shared  by  many  cynodonts  but  is  absent  in 
Morganucodon  and  more  derived  inam- 
mals. 

Sphenoid  Complex 

The  basisphenoid  is  an  endochondral 
ossification  whereas  the  parasphenoid  is  an 
intramembranous  ossification  that  under- 
lies the  former  (Goodrich,  1930;  de  Beer, 
1937);  the  two  elements  are  fused  early  in 
development  to  form  the  basisphenoid— 
parasphenoid  complex  in  extant  diapsids 
(Goodrich,  1930;  de  Beer,  1937;  Bellairs 
and  Kamal,  1981;  Rieppel,  1993),  and  this 
complex  reaches  posteriorly  to  border  on 
the  basioccipital.  In  one  cranial  study  of 
living  diapsids  (Oelrich,  1956),  the  un- 
paired anterior  median  element  of  this 
complex  is  considered  to  be  the  paras- 
phenoid in  adult  diapsids,  whereas  the 
paired  posterolateral  parts  of  this  complex 
are  identified  as  the  basisphenoid.  In  living 
mammals,  the  intramembranous  paras- 
phenoid ossification  forms  an  unpaired 
median  structure  in  the  rostrum  of  the  ba- 
sisphenoid-parasphenoid  complex  (Jollie, 


rounding  basicranial  bones  (note  that  the  basisphenoid  [green]  is  superficially  overlapping  the  petrosal  [gray]  but  does  not  directly 
envelope  the  cochlea  [purple]).  (C)  Basicranial  structure.  (D)  Inner  ear  endocast  (ventral  view).  Abbreviations  (color  code  for 
bones):  app,  anterior  paroccipital  process;  asc,  anterior  semicircular  canal;  bo,  basioccipital  (yellow);  bs,  basisphenoid  (green); 
bsw,  basisphenoid  wing  (=parasphenoid  ala  [green]);  ce,  cavum  epiptericum;  cif,  crista  interfenestralis;  co,  bony  cochlear  canal; 
80,  exoccipital  (blue);  fc,  foramen  cochleae;  fc-jf,  the  confluent  foramen  cochleae  and  jugular  foramen;  ff,  facial  foramen  (VII); 
fst,  fossa  for  stapedial  muscle;  fv,  fenestra  vestibuli;  jf,  jugular  foramen;  If,  lateral  flange  of  the  petrosal;  Isc,  lateral  semicircular 
canal;  It,  lateral  trough;  oc,  occipital  condyle;  od,  odontoid  notch  of  basioccipital;  pe,  petrosal  (gray);  ppp,  posterior  paroccipital 
process  of  the  petrosal;  psc,  posterior  semicircular  canal;  sq,  squamosal  (pink). 


86         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


bsw 


cochlear 
housing 


Figure  2.  Basicranium  and  inner  ear  of  Yunnanodon  (Tritylodontidae,  Cynodontia).  (A)  Basicranium  (detailed  features  in  the 
ventrolateral  view,  with  skull  tilted,  based  on  IVPP  7219)  and  its  position  In  skull  (skull  outline  In  lateral  view,  with  zygoma 
removed).  The  dashed  line  in  the  stipple  drawing  represents  the  posterior  limit  of  the  preserved  part  of  the  baslsphenoid  wing, 
which  is  most  probably  incomplete  In  the  illustrated  skull.  As  a  result,  the  pars  cochlearis  (cochlear  housing)  Is  more  exposed 
than  in  the  intact  skull.  (B)  Approximate  anatomical  relationships  of  Inner  ear  (purple)  to  the  surrounding  baslcranlal  structures 
(basicranium  Is  tilted  ventrolaterally,  more  so  than  In  Fig.  2A).  (C)  Baslcranlal  structure.  (D)  Inner  ear  endocast  (lateral  view). 
Abbreviations  (color  code  for  bones):  ar,  articular  bone;  app,  anterior  parocclpltal  process;  asc,  anterior  semicircular  canal;  bo, 
basiocclpltal  (yellow);  bs,  baslsphenoid  (green);  bsw,  baslsphenoid  wing  (  =  parasphenoid  ala  [green]);  ce,  cavum  epiptericum; 
CO,  bony  cochlear  canal;  dfx,  dorsal  flex  of  the  baslsphenoid;  eo,  exoccipital  (blue);  fc-jf,  the  confluent  foramen  cochleae  and 
jugular  foramen;  ff,  facial  foramen;  fst,  fossa  for  stapedial  muscle;  fv,  fenestra  vestibuli;  If,  lateral  flange  of  the  petrosal;  Isc, 
lateral  semicircular  canal;  It,  lateral  trough;  oc,  occipital  condyle;  od,  odontoid  notch;  pc,  pars  cochlearis  (cochlear  housing);  pe, 
petrosal  (gray);  ppp,  posterior  parocclpltal  process  of  the  petrosal;  psc,  posterior  semicircular  canal;  q,  quadrate;  sq,  squamosal 
(pink). 


Tritylodontid  Inner  Ear  •  Luo        87 


1962),  whereas  the  posterolateral  parts  of 
this  complex  are  formed  of  endochondral 
ossification  (J.  R.  Wible,  personal  com- 
munication). The  anatomical  term  "basi- 
sphenoid  wing"  (Kiihne,  1956;  Crompton, 
1964;  Luo  et  al.,  1995)  is  synonymous  with 
the  "parasphenoid  ala"  in  other  studies  of 
tritylodontids  (Hopson,  1964;  Gow,  1986; 
Sues,  1986).  Both  terms  have  been  applied 
to  the  paired  posterior  extensions  from  the 
main  body  of  the  sphenoid  complex.  The 
basisphenoid  wing  is  used  here  for  cyno- 
donts  and  mammaliaforms. 

The  basisphenoid  has  a  strong  dorsal 
flexion  posteriorly  in  Yiinnanodon,  as  is 
typical  of  other  tritylodontids.  The  basi- 
sphenoid has  a  ventral  tuberosity.  Bifur- 
cating from  the  ventral  tuberosity  are  the 
crests  of  the  basisphenoid  wings  (Fig.  1). 
The  basisphenoid  wing  covers  the  anterior 
and  ventral  aspects  of  the  pars  cochlearis, 
and  conceals  the  anterior  part  of  the  pars 
cochlearis  from  ventral  view  (Figs.  IC, 
3B).  The  basisphenoid  wing  does  not 
reach  the  rim  of  the  fenestra  vestibuli  in 
Yunnanodon  (Figs.  IB,  C). 

The  development  of  the  basisphenoid 
dorsal  flexion  and  the  basisphenoid  wing 
may  vary  considerably  in  relation  to  overall 
skull  size  among  tritylodontids.  In  the  larg- 
er skulls  o{  Bienotheriiun  (Hopson,  1964), 
Bienotheroides  (Sun,  1984),  and  Kaijen- 
tatherium  (Sues,  1986),  the  crest  on  the 
basisphenoid  wing  is  hypertrophied  and 
accentuates  the  dorsal  flexion  of  the  basi- 
cranium.  The  hypertrophied  basisphenoid 
crest  reaches  posterolaterally  near  the  fe- 
nestra vestibuli.  In  Tritylodon,  the  basi- 
sphenoid wing  borders  on  the  fenestra  ves- 
tibuli and  reaches  the  facial  foramen 
(Gow,  1986).  The  basisphenoid  wing  is 
much  larger  and  more  pronounced  in 
these  larger  tritylodontids  than  in  smaller 
tritylodontids,  such  as  Yunnanodon  (Fig. 
1)  and  Bocatherium  (Clark  and  Hopson, 
1985).  The  pars  cochlearis  is  always  pre- 
sent in  tritylodontids.  However,  its  external 
exposure  as  the  promontorium  is  a  variable 
feature  in  the  basicranium,  partly  because 
of  the    allometric   effect   from    the   wide 


range  of  skull  sizes  in  this  diverse  group. 
The  pars  cochlearis  tends  to  be  better  ex- 
posed in  small  tritylodontids  with  a  weaker 
basisphenoid  wing,  but  the  pars  cochlearis 
may  not  have  any  external  exposure  at  all 
if  covered  by  a  hypertrophied  basisphe- 
noid wing  in  large  tritylodontids,  such  as 
Bienotherium  and  Tritylodon. 

Basioccipital 

The  basioccipital  is  elongate  and  plate- 
like. Its  anterior  part  intrudes  between  the 
two  basisphenoid  wings  (Fig.  IB).  The  lat- 
eral part  of  the  basioccipital  forms  a  lappet 
and  overlaps  the  ventral  surface  of  the  pars 
cochlearis  extensively  (Fig.  3B),  as  evi- 
denced by  a  specimen  in  which  the  suture 
of  two  bones  is  visible.  Therefore,  in  the 
intact  specimens  of  Yunnanodon,  the  me- 
dial part  of  the  pars  cochlearis  is  concealed 
from  ventral  view  by  the  basioccipital.  The 
overlap  of  the  basioccipital  lateral  lappet 
on  the  pars  cochlearis  may  be  more  exten- 
sive in  large  tritylodontids  than  in  such 
small  taxa  as  Yunnanodon.  The  posterior 
part  of  the  basioccipital  does  not  seem  to 
border  on  the  jugular  foramen,  which  is 
encircled  by  the  petrosal  and  the  exoccip- 
ital  (Fig.  1).  An  odontoid  notch  is  present 
on  the  posterior  border  of  the  basioccipi- 
tal. 

Cochlear  Housing 

The  serial  sections  of  Yiinnanodon  show 
that  the  cochlear  canal  is  entirely  envel- 
oped by  the  pars  cochlearis,  which  is  ex- 
ternally covered  by  the  basisphenoid  wing 
and  by  the  lateral  lappet  of  the  basioccip- 
ital (Fig.  3B).  This  is  consistent  with  an 
earlier  observation  on  Tritylodon  by  Gow 
(1986)  that  the  basisphenoid  wing  (paras- 
phenoid ala)  is  a  superficial  part  of  the 
compound  bony  structure  around  the  co- 
chlea. However,  the  serial  sections  indicate 
that  the  basisphenoid  wing  and  the  pars 
cochlearis  are  distinctive  structures  in 
Yunnanodon,  but  not  homologous  to  each 
other  as  suggested  by  Gow  (1986);  the  ba- 
sisphenoid wing  does  not  directly  envelop 
the  cochlear  canal.  It  should  be  pointed 


88 


Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Larger  tritylodonts  Pa 


E.  Multituberculates 


bs-bo 


bsw 
A.  Probelesodon 

Figure  3.  Comparison  of  tine  basicranial  structures  in  cynodonts  and  mammals  (schematic  transverse  section  at  the  level  of 
the  posterior  part  of  the  cavum  epiptericum  and/or  the  anterior  part  of  the  cochlea).  (A)  Probelesodon  lewisi  (Romer,  1970; 
based  on  MCZ  3774,  serial  section  212;  Museum  of  Comparative  Zoology,  Harvard  University;  courtesy  of  A.  W.  Crompton;  the 
basisphenoid  and  basioccipital  are  indistinguishable  in  the  section).  (B)  Yunnanodon  brevirostre  (composite  sl<etches  based  on 
several  sections  of  a  specimen  provided  by  A.-L.  Sun)  and  a  generalized  large  tritylodont  (showing  the  proportional  difference 
of  the  basisphenoid  wing  and  the  basioccipital  lappet).  (C)  Sinoconodon  rigneyi  (based  on  sections  of  IVPP  8689;  Institute  of 
Vertebrate  Paleontology  and  Paleoanthropology,  Beijing).  (D)  Morganucodon  watsoni  (based  on  sections  of  MCZ  20998,  Gray- 
beal  et  al.  [1989]).  (E)  Nemegtbaatar  gobiensis  (modified  from  Hurum,  1998,  fig.  5).  Abbreviations:  al,  anterior  lamina  of  the 
petrosal;  bo,  basioccipital;  bs,  basisphenoid;  bsw,  basisphenoid  wing  (parasphenoid  ala);  ce,  cavum  epiptericum  (for  the  trigem- 
inal ganglion);  co,  cochlear  canal;  ep,  epipterygoid  (alisphenoid);  If,  lateral  flange  of  the  petrosal;  pa,  pila  antotica;  pc,  pars 
cochlearis;  pr,  promontorium  (ventral  or  external  eminence  formed  by  the  pars  cochlearis). 


out  that  the  presence  of  the  promontorium 
in  Yunnanodon,  as  first  noted  by  Sun  and 
Cui  (1987),  is  reconfirmed  here.  However, 
the  promontorium  on  their  specimen 
(IVPP  5071)  is  exposed  because  of  the 
postmortem  detachment  of  the  basisphe- 


noid and  the  basioccipital  (see  Fig.  2).  In 
the  intact  specimens  of  Yunnanodon,  the 
pars  cochlearis  is  mostly  concealed  in  ven- 
tral view.  In  one  specimen  (IVPP  7219), 
the  basisphenoid  wing  seems  to  cover  at 
least  one  half  of  the  pars  cochlearis  on  one 


Tritylodontid  Inner  Ear  •  Luo        89 


side,   but   its   absence   on   the   other  side  The  saccular  and  utricular  recesses  are 

leaves    much    of  the   pars    cochlearis   ex-  divided  in  Yiinnanodon,  similar  to  those  of 

posed.  Bienotheriutn    as    illustrated    by    Hopson 

(1965,  fig.   12).  The  junction  of  the  bony 

Inner  Ear  utricular  recess  and  the  ampullae  of  the 

The  cochlear  canal  is  a  tubular  structure  anterior  and  lateral  semicircular  canals  is 

with  a  bulge  in  the  middle  part  (best  seen  slightly  more  inflated  than  the  rest  of  the 

in  lateral  view;  Fig.  2).  The  canal  is  ap-  vestibule.  All  three  bony  semicircular  ca- 

proximately  1.9  mm  in  length  as  measured  nals  have  somewhat  irregular  shapes.  The 

from  the  anterior  border  of  the  fenestra  bony    tubes    of    the    semicircular    canals 

vestibuli  to  the  apex  of  the  cochlear  canal  range  from  0.4  to  0.5  mm  in  diameter.  The 

{sensu  Luo  et  al.  [1995]),  or  about  3.7  mm  anterior  semicircular  canal  has  the  largest 

if  measured  from  the  posterior  border  of  arc  with  a  maximum  radius  of  —1.7  mm. 

the  fenestra  to  the  apex  (sensu  Rosowski  The    posterior    semicircular    canal    has    a 

and  Graybeal  [1991]).  The  inner  surface  of  maximum  radius  of  1.1  mm.  The  posterior 

the  bony  cochlear  canal  is  simple  and  de-  part  of  this  canal  is  bent  to  form  an  angle, 

void  of  internal  structures.  The  lateral  semicircular  canal  is  the  small- 

The  canal  is  slightly  constricted  anterior  est,  with  a  radius  to  its  arc  of  0.8  mm.  The 
to  the  fenestra  vestibufi  (Fig.  2A).  From  lateral  and  posterior  semicircular  canals 
serial  sections  it  appears  that  the  cochlear  are  located  within  the  petrosal  deep  to  the 
canal  is  connected  to  the  bony  saccular  fossa  for  the  stapedial  muscle  (Fig.  2).  The 
cavity  by  a  relatively  narrow  and  short  anterior  semicircular  canal  is  located  with- 
channel.  This  channel  probably  housed  in  the  petrosal  portion  of  the  side  wall  for 
the  ductus  reuniens,  the  membranous  the  braincase  and  dorsal  to  the  bulbous 
structure  that  connects  the  saccule  to  the  anterior  paroccipital  process.  On  the  en- 
basal  (proximal)  part  of  the  cochlear  duct,  docranial  surface  of  the  braincase,  the  an- 
On  the  basis  of  these  bony  features,  it  may  terior  semicircular  canal  forms  the  rim  of 
be  inferred  that  the  cochlear  part  was  bet-  the  subarcuate  fossa  and  almost  encircles 
ter  differentiated  from  the  saccular  part  of  the  fossa, 
the  membranous  labyrinth  than  in  the  p-.o-^.  looinM 
primitive    condition    of  other    cynodonts.  LJIoUUbolUN 

The  middle  portion  of  the  cochlear  canal  In  the  primitive  condition  of  noncyno- 

is  bulging  with  a  maximum  diameter  about  dont  therapsids  such  as  dicynodonts  (Fig. 

1.7  mm  but  its  anterior  portion  tapers  to-  4A;  Olson,  1944;  Cox,  1962)  and  gorgon- 

wards  the  apex  that  is  slightly  turned  in  opsids  (Olson,  1944;  Sigogneau,  1974),  the 

dorsolateral  direction.  The  bulging  middle  sacculocochlear  cavity  (  =  "lagenar  recess" 

portion  of  the  cochlea  is  reminiscent  of  the  of  Sigogneau  [1974])  is  not  differentiated 

globular  outline  of  the  cochleas  in  other  from  the  rest  of  the  bony  vestibular  cavity 

advanced  nonmammalian  cynodonts  (Qui-  in  the  inner  ear  (Fig.  4A).  The  fenestra 

roga,   1979).  The  bone  near  the  anterior  vestibuli  may  be  either  on  the  lateral  as- 

apex  is  fractured  in  serial  sections  (repre-  pect,  or  on  the  ventrolateral  aspect  in  the 

sented  by  dashed  line  on  the  endocasts  in  sacculocochlear  cavity. 

Figs.  1  and  2).  The  floor  (fundus)  of  the  A  smaH  and  globular  cochlear  cavity  is 

internal  acoustic  meatus  is  fully  ossified,  as  differentiated  from  the  main  part  of  the 

already  described  in  Oligokijphus  (Kuhne,  saccular  recess  in  the  cynodont  Thrinaxo- 

1956),  Bienothehum  (Hopson,  1964),  and  don.  The  cochlear  cavity  is  distinctive  from 

Tritylodon  (Gow,  1986).  The  cochlear  and  the  fenestra  vestibuli  in  the  lateral  view 

vestibular  branches  of  the  vestibulococh-  (Fig.   4B)   and  from  the  vestibule  in  the 

lear  cranial  nerve  (VIII)  had  separate  fo-  medial  view  (not  illustrated;  Fourie,  1974; 

ramina  to  the  inner  ear.  Rowe  et  al,    1993;   E.   F.   Allin,  personal 


90 


Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  4.  Comparison  of  inner  ear  endocasts  of  cynodonts  and  primlfive  mammals.  (A)  A  generalized  inner  ear  endocast  of  a 
dicynodont  (modified  from  Olson  [1944]  and  Cox  [1962]).  (B)  A  generalized  inner  ear  endocast  of  Thhnaxodon  (a  composite 
figure  based  on  descriptions  and  figures  of  Olson  [1944],  Fourie  [1974],  and  illustrations  by  courtesy  of  Dr.  Allin).  (C)  Probele- 
sodon  (modified  and  reversed  from  Quiroga  [1979]).  (D)  Probainognathus  (modified  from  Allin  [1986]).  (E)  Yunnanodon  (baaed 


Tritylodontid  Inner  Ear  •Luo        91 


communication).  However,  the  cochlear 
cavity  does  not  extend  anteriorly  beyond 
the  fenestra  vestibuli.  The  bony  housing  of 
the  inner  ear  has  contributions  from  sev- 
eral bones:  the  prootic,  the  opisthotic,  the 
exoccipital,  and  the  supraoccipital,  none  of 
which  are  fused  with  one  another.  The  co- 
chlear component  of  the  prootic  bone  is 
very  small  (Fourie,  1974).  The  basisphe- 
noid  wing  contributes  to  the  cochlear 
housing  extensively.  On  the  external  sur- 
face of  the  basicranium,  the  basisphenoid 
wing  reaches  and  participates  in  the  rim  of 
the  fenestra  vestibuli,  concealing  the  pro- 
otic froin  the  ventral  view. 

The  more  advanced  Probelesodon  and 
Probainognathus  have  a  globular  cochlear 
cavity  that  is  larger  in  proportion  to  the 
whole  inner  ear  (Figs.  4C,  D;  Quiroga, 
1979;  Allin,  1986).  The  cochlear  structure 
also  extends  anterior  to  the  fenestra  ves- 
tibuli (Figs.  4C,  D).  A  larger  size  and  a 
more  anterior  orientation  of  the  cochlear 
structure  are  both  derived  characteristics, 
compared  to  that  o{  Thrinaxodon,  and  very 
different  from  the  poorly  differentiated 
sacculocochlear  recess  in  dicynodonts  and 
gorgonopsians. 

Probelesodon  and  Probainognathus  are 
more  primitive  than  Yiinnanodon  in  that 
their  cochlear  cavity  is  iTiuch  smaller  (Fig. 
4),  as  is  the  pars  cochlearis  of  the  prootic. 
The  pars  cochlearis  does  not  form  an  ex- 
ternal promontorium.  The  cochlear  cavity 
does  not  extend  anteromedially,  dorsal  to 
the  basisphenoid  wing.  The  basisphenoid 
wing  bears  a  prominent  crest  and  reaches 
near  the  fenestra  vestibuli.  The  rim  of  the 
fenestra  vestibuli  is  formed  by  an  elevated 
and  thickened  ring  (Lucas  and  Luo,  1993; 
Luo,  1994).  The  prootic  and  the  opisthotic 
are  separate  bones.   All  these  characters 


are   unlike   those   of  tritylodontids   and 
mainmaliaforms. 

The  tritylodontid  Yunnanodon  (Fig.  4E) 
is  more  derived  than  other  nonmammalian 
cynodonts  including  Probelesodon,  Pro- 
bainognathus, and  Massetognathus  (Qui- 
roga, 1979;  Allin,  1986)  in  possessing  a 
longer  and  larger  cochlear  canal.  The  co- 
chlear canal  extends  far  beyond  the  ante- 
rior rim  of  the  fenestra  vestibuli.  The  prox- 
imal part  of  the  canal  is  distinctive  from 
the  saccular  region.  The  cast  of  the  co- 
chlear canal  of  Yunnanodon  is  similar  to 
those  of  Sinoconodon  (Luo  et  al.,  1995) 
and  Morganucodon  (Graybeal  et  al.,  1989; 
Luo  and  Ketten,  1991).  The  cochlear  canal 
is  even  longer  in  Yunnanodon  than  in  Sin- 
oconodon in  absolute  size.  Its  proportion 
to  the  overall  length  of  the  skull  is  about 
the  same  as  in  the  latter.  The  only  feature 
of  the  cochlea  that  may  be  interpreted  as 
a  primitive  character  is  the  bulging  middle 
part  that  somewhat  resembles  the  more 
globular  cochleas  in  Probainognathus  (Al- 
lin, 1986)  and  Massetognathus  (Quiroga, 
1979). 

The  cochlear  canal  does  not  extend  the 
entire  length  of  the  pars  cochlearis  in  Yun- 
nanodon, thus  resembling  those  of  Sino- 
conodon and  Haldanodon,  in  the  propor- 
tion of  the  cochlear  canal  to  the  pars  coch- 
learis. Although  the  cochlea  is  housed  in  a 
pars  cochlearis  with  an  externally  exposed 
promontorium  in  all  known  mammali- 
aforms  and  mammals,  the  presence  of  the 
petrosal  promontorium  is  not  necessarily 
correlated  to  a  fully  elongated  cochlea,  as 
evidenced  by  Sinoconodon  (Luo  et  al., 
1995)  and  the  late  Jurassic  docodont  Hal- 
danodon (Lillegraven  and  Krusat,  1991). 
In  both  mammals  the  cochlea  is  short  rel- 
ative  to  the   size   of  the  pars   cochlearis. 


on  reconstruction  from  serial  sections  from  a  specimen  courtesy  of  A.-L.  Sun).  (F)  Sinoconodon  (based  on  sections  of  IVPP 
8689).  (G)  Morganucodon  (modified  from  Graybeal  et  al.  [1989]  and  Luo  and  Ketten  [1991]).  Figures  not  to  the  same  scale. 
Abbreviations;  asc,  anterior  semicircular  canal;  co,  cochlear  canal;  cr,  globular  cochlear  recess  (undifferentiated  from  the  vesti- 
bule); fc-jf,  confluent  foramen  cochleae  and  jugular  foramen;  fv,  fenestra  vestibuli  (oval  window);  Isc,  lateral  semicircular  canal; 
psc,  posterior  semicircular  canal;  sc,  undifferentiated  osseous  sacculocochlear  structure  (essentially  a  part  of  the  vestibule). 


92         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Yunnanodon,  Sinoconodon,  and  Haldano- 
don  share  this  primitive  condition,  in  con- 
trast to  the  more  derived  Morganiicodon, 
triconodontids,  and  multituberculates,  in 
which  the  cochlear  canal  extends  the  full 
length  of  the  pars  cochlearis  (and  the  pro- 
montorium). 

The  overlap  of  the  basioccipital  on  the 
flat  medial  facet  of  the  pars  cochlearis  is 
present  in  both  Yunnanodon  and  Sinocon- 
odon (Figs.  3B,  C).  However,  unlike  the 
condition  in  Sinoconodon  and  other  early 
mammaliaforms  in  which  the  basisphenoid 
wing  is  lost  and  the  pars  cochlearis  is  ven- 
trally  exposed  (Fig.  3C),  the  pars  coch- 
learis of  Yunnanodon  is  not  well  exposed, 
because  of  coverage  by  the  well-developed 
basisphenoid  wing  (Fig.  3B).  It  should  be 
noted  that  the  presence  of  a  pars  coch- 
learis may  be  a  shared  derived  condition 
of  mammals,  tritylodontids,  tritheledon- 
tids,  and  possibly  probainognathids.  As  re- 
ported by  Crompton  (1994),  the  trithele- 
dontid  Pachygenelus,  a  taxon  closely  relat- 
ed to  mammals,  has  a  small  cochlea  con- 
tained within  the  pars  cochlearis  that  is 
also  concealed  by  the  basisphenoid  and 
the  basioccipital — very  similar  to  the  con- 
figuration in  Yunnanodon  as  described  in 
this  paper.  A  juvenile  skull  of  a  probain- 
ognathid  cynodont  (Bonaparte  and 
Crompton,  1994)  also  has  a  proinonto- 
riumlike  structure  in  the  ear  region.  Al- 
though this  structure  is  not  known  in  the 
adult  specimens  of  Probainognathus,  Pro- 
bainognathus  possibly  has  a  small  pars 
cochlearis  that  is  covered  by  the  basisphe- 
noid and  basioccipital  and  not  exposed  as 
the  promontorium  in  the  fully  grown 
skulls. 

Tritylodontids  and  tritheledontids  are 
both  considered  to  belong  to  the  mam- 
maliamorphs  (modified  from  Rowe  [1988] 
to  include  tritheledontids;  see  also  Wible 
[1991],  Wible  and  Hopson  [1993],  Luo 
[1994],  and  Luo  and  Crompton  [1994]). 
The  characteristics  of  the  inner  ear  and  its 
bony  housing  in  these  two  groups,  as  de- 
scribed by  Crompton  (1994)  and  here,  of- 
fer fresh  insight  into  the  pattern  of  early 


evolution  of  the  anatomical  structures  of 
the  basicranium  and  the  inner  ear  (Fig.  5). 

The  development  of  an  elongate  cochle- 
ar canal  and  change  in  the  pattern  of  os- 
sification of  the  basicranial  bones  are  cor- 
related (Fig.  5).  It  is  hypothesized  that  in 
advanced  cynodonts,  such  as  Probainog- 
nathus (Allin,  1986),  Probelesodon,  and 
Massetognathus  (Quiroga,  1979),  an  ex- 
pansion of  the  cochlear  recess  occurs  with- 
in the  prootic.  This  development  is  related 
to  a  greater  reduction  of  the  basisphenoid 
wing  in  these  derived  cynodonts  (Fig.  5: 
node  B)  than  in  Thrinaxodon  and  other 
basal  cynodonts. 

In  mammaliamorphs  (Fig.  5,  node  C, 
including  tritheledontids),  embryonic  os- 
sifications of  the  otic  capsule  must  have 
fused  into  a  single  petrosal  bone  in  the  ful- 
ly grown  adults,  instead  of  two  separate  os- 
sifications (prootic  and  opisthotic).  This 
change  may  have  made  the  bony  housing 
for  the  entire  inner  ear  more  rigid;  as  a 
result  the  inner  ear  may  be  better  insulat- 
ed and  less  susceptible  to  interference. 
Related  to  the  change  in  ossification,  a 
short  but  distinctive  cochlear  canal  is  de- 
veloped within  a  neomorphic  pars  coch- 
learis, as  described  for  Yunnanodon  here, 
and  for  Pachygenelus  by  Crompton  (1994). 
In  Sinoconodon  and  more  derived  mam- 
mals (Fig.  5,  node  D),  the  basisphenoid 
wing  is  lost  so  that  the  pars  cochlearis  is 
exposed  on  the  ventral  surface  of  the  bas- 
icranium. However,  the  ventral  coverage 
of  the  pars  cochlearis  by  the  basioccipital, 
a  primitive  condition,  is  retained  at  least  in 
part  in  Sinoconodon. 

In  Morganiicodon  and  more  derived 
mammals  except  docodonts  (Fig.  5,  node 
D),  the  cochlear  canal  is  more  elongate 
than  those  of  Sinoconodon  and  Yunnano- 
don, and  extends  the  full  length  of  the  pars 
cochlearis.  Related  to  the  elongation  of  the 
cochlear  canal,  the  external  surface  of  the 
promontorium  is  also  more  inflated.  The 
basioccipital  is  shifted  medially  (Fig.  3). 
Correspondingly,  the  flat  medial  facet  on 
the  promontorium  as  seen  in  Sinoconodon 
and  Yunnanodon  is  lost. 


/ 

/ 

/ 

^      Placentals 

/ 

/ 

m 

Marsupials 

C/5 
Q. 

E 

o 

E 
E 

03 

Zhangheotherium 
VMultituberculates 

c 
o 

"O 

o 

c 

O 

E 

.eg 

£ 
E 

03 

E 
E 

03 

I 

^  Monotremes 

Morganucodon 

—     Sinoconodon 

Pachygenelus 

1 

Probainognathus 

\ 

Probelesodon 

v_ 

ThrinaYnrinn 

"Therapsids" 


Tritylodontid  Inner  Ear  •  Luo 


Transformations 


93 


Inner  Ear 

cochlear 
canal  coil 


cochlear 
duct  coil 

cochlear 
elongation 


cochlear 
canal 


.cochlear 
cavity 


Bony  Housing 


inflated  promontorium 
&  bo  reduction 

-  promontorium 
&  loss  of  bsw 

periotic  fusion 


bsw  reduction 


prootic  housing 


Figure  5.  Stepwise  transformation  of  the  bony  housing  of  inner  ear  and  the  cochlear  structures  from  nonmammalian  cynodonts 
to  mammals.  Phylogeny  is  based  on  Kemp  (1983),  Rowe  (1988),  Wible  (1991),  Wible  and  Hopson  (1993),  Luo  (1994),  Luo  and 
Crompton  (1994),  and  Hu  et  al.  (1997).  Definitions  of  mammaliamorphs  and  mammaliaforms  are  modified  from  Rowe  (1988). 
Character  evolution  from  nodes  A  through  E  is  explained  in  text.  The  membranous  labyrinth  of  the  cochlea  (cochlear  duct)  is 
coiled  (node  F)  in  all  living  mammals  (Zeller,  1989;  Luo  and  Ketten,  1991;  Fox  and  Meng,  1997),  although  in  monotremes  the 
bony  labyrinth  of  the  cochlea  (cochlear  canal)  lacks  the  corresponding  coil.  Multituberculates  (node  G)  have  a  straight  or  slightly 
curved  cochlear  canal  without  coil  (Luo  and  Ketten,  1991;  Meng  and  Wyss,  1995;  Hurum,  1998),  as  in  the  symmetrodont 
Zhangheotherium  (node  H;  see  Hu  et  al.  [1997]).  Only  the  living  marsupials  and  placentals  (node  I)  have  a  fully  coiled  bony 
labyrinth  (cochlear  canal)  in  correlation  with  the  coiled  membranous  labyrinth  (cochlear  duct;  Zeller,  1 989;  Luo  and  Ketten,  1 991 ; 
Fox  and  Meng,  1997).  Either  the  coiled  membranous  cochlear  duct  in  living  monotremes  must  be  considered  as  convergent  to 
those  of  living  therians,  or  the  uncoiled  cochleas  of  multituberculates  and  Zhangheotherium  (Hu  et  al.,  1997)  must  be  regarded 
as  an  atavistic  reversal  to  those  of  mammaliaforms.  The  coiled  cochlear  structures  within  the  pars  cochlearis  are  homoplasic 
among  main  lineages  of  the  mammalian  crown  group.  Abbreviations:  bo,  basioccipital;  bsw,  basisphenoid  wing. 


Mammals  are  most  specialized  among 
living  vertebrates  in  their  hearing  adapta- 
tion, much  of  which  is  attributable  to  their 
derived  inner  and  middle  ear  structures. 
The  pars  cochlearis  containing  a  cochlea  is 
one  of  the  most  complex  character  systems 
of  the  mammalian  skull,  and  is  crucial  for 
more  sensitive  hearing,  especially  for  high 
frequency  sound.  The  assembly  of  such  a 
complex  character  system  udth  significant 
functional  adaptation  occurred  in  several 
incremental  steps  during  the  morphologic 


evolution  of  nonmammalian  cynodonts 
and  early  mammals  (Fig.  5). 

The  development  and  the  emergence  of 
the  pars  cochlearis  in  the  basicranium  are 
correlated  with  the  transformation  of  the 
cochlear  canal.  It  is  hypothesized  that, 
through  the  transition  from  nonmammali- 
an cynodonts  to  early  mammaliaforms,  the 
enlarged  pars  cochlearis  with  a  cochlear 
canal  had  preceded  the  development  of 
the  petrosal  promontorium.  The  promon- 
torium is  developed  by  the  emergence  of 


94         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


the  pars  cochlearis  on  the  basicranium  to 
displace  the  neighboring  sphenoid  com- 
plex and  basioccipital  bone.  Inflation  of 
the  external  promontorium  of  the  pars 
cochlearis  is  associated  with  the  elongation 
of  the  cochlear  canal.  The  seemingly  dras- 
tic transformation  of  the  ear  region  in  the 
basicranium  is  achieved  in  a  stepwise 
transformation  though  the  phylogenetic 
transition  from  nonmammalian  cynodonts 
to  mammals. 

After  an  elongate  cochlea  developed 
within  the  enlarged  pars  cochlearis  of  the 
petrosal  in  mammaliaforms,  further  evo- 
lution of  the  cochlear  coiling  in  the  crown 
group  of  mammals  shows  a  considerable 
degree  of  homoplasy  (Fig.  5).  The  living 
monotremes  have  a  coiled  cochlear  duct 
(membranous  labyrinth)  but  without  the 
corresponding  coil  of  the  bony  cochlear 
canal  (bony  labyrinth).  Multituberculates 
have  a  straight  or  slightly  curved  bony  co- 
chlear canal  without  coil  (Luo  and  Ketten, 
1991;  Meng  and  Wyss,  1995;  Hurum, 
1998),  as  in  the  symmetrodont  Zhangh- 
eotherium  (Hu  et  al.,  1997).  Only  the  liv- 
ing marsupials  and  placentals  have  a  fully 
coiled  membranous  labyrinth  (cochlear 
duct)  that  is  intricately  associated  with  the 
coiled  bony  labyrinth  (cochlear  canal;  Zell- 
er,  1989;  Luo  and  Ketten,  1991;  Fox  and 
Meng,  1997).  Either  the  coiling  of  the 
membranous  cochlear  duct  in  living  mono- 
tremes must  be  considered  as  convergent 
to  those  of  li\dng  therians,  or  the  uncoiled 
cochleas  of  multituberculates  and  Zhangh- 
eotherium  (Hu  et  al.,  1997)  must  be  re- 
garded as  an  atavistic  reversal  to  those  of 
mammaliaforms  (Fig.  5). 

ACKNOWLEDGMENTS 

Professor  A.  W.  Crompton  has  been  an 
inspiration  for  this  work.  I  thank  Profes- 
sors A.-L.  Sun  and  Z.-M.  Dong,  X.-C.  Wu, 
and  Mr.  G.  Cui  for  generously  providing 
the  tritylodontid  specimens  and  their  casts. 
For  access  to  comparative  materials,  I 
thank  Professors  A.  W.  Crompton  and  F. 
A.  Jenkins,  Jr.,  and  Mr.  C.  R.  Schaff  (Har- 
vard University);  Professor  J.  A.   Hopson 


(University  of  Chicago);  and  Professor  A.- 
L.  Sun  (Institute  of  Vertebrate  Paleontol- 
ogy and  Paleoanthropology).  Professor 
Crompton  provided  the  Croft  grinder. 
Professor  Sun  helped  with  the  serial  sec- 
tions. Mr.  J.  A.  Georgi  assisted  in  comput- 
erized reconstruction  and  Mr.  M.  A.  Klin- 
gler  assisted  in  illustrations.  During  this 
study,  I  benefited  from  discussion  with 
Drs.  E.  F.  Allin,  A.  W.  Crompton,  J.  A. 
Hopson,  T  Rowe,  and  J.  R.  Wible.  Dr.  Al- 
lin graciously  provided  his  unpublished 
drawings  of  Thrinaxodon  for  this  study. 
The  manuscript  benefited  from  the  critical 
and  editorial  reviews  by  Drs.  Allin,  Hop- 
son,  Jenkins,  Shapiro  and  Wible,  and  an 
anonymous  reviewer.  This  research  was 
supported  by  a  National  Science  Founda- 
tion CAREER  Award  (DEB  9527892),  the 
National  Geographic  Society,  and  the  Net- 
ting and  O'Neil  Funds  of  Carnegie  Mu- 
seum of  Natural  History. 

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A  NEW  SPECIMEN  AND  A  FUNCTIONAL  REASSOCIATION  OF  THE 
MOLAR  DENTITION  OF  BATODON  TENUIS 
(PLACENTALIA,  INCERTAE  SEDIS),  LATEST  CRETACEOUS 
(LANCIAN),  NORTH  AMERICA 


CRAIG  B.  WOOD!  AND  WILLIAM  A.  CLEMENS^ 

Abstract.  Batodon  tenuis  Marsh,  1892,  a  rare,  mi- 
nute, eutherian  mammal,  is  a  member  of  several  Late 
Cretaceous  (Lancian  North  American  Land  Mammal 
Age),  North  American  local  faunas.  A  hitherto  un- 
described  fragment  of  maxilla  from  the  Hell  Creek 
Formation,  Garfield  Count>',  Montana,  documents 
tlie  association  of  M-  and  M^  Analysis  of  the  small 
available  sample  of  upper  and  lower  molars  in  func- 
tional orientation  strengthens  the  basis  for  their  as- 
sociation, provides  a  functional  explanation  for  the 
enlargement  of  the  talonid  of  Mj,  and  suggests  only 
one  species  is  represented.  Currently,  B.  tenuis,  with 
an  estimated  body  mass  of  approximately  5  g,  is  the 
smallest  known  eutherian  mammal  from  the  Creta- 
ceous. The  phylogenetic  position  of  B.  tenuis  in  the 
poorlv  documented.  Cretaceous  radiation  of  euthe- 
rians  is  still  unclear. 

INTRODUCTION 

In  a  search  of  University  of  California 
Museum  of  Paleontology  (UCMP)  collec- 
tions to  find  uncataloged  and  fragmentary 
teeth  of  Late  Cretaceous  marsupials  for 
enamel  microstructure  research  (Wood  et 
al.,  1999),  an  important  new  specimen  re- 
ferable to  Batodon  tenuis  came  to  light 
(Wood  and  Clemens,  1990).  Batodon  ten- 
uis Marsh  1892  is  a  tiny,  very  rare.  Late 
Cretaceous  eutherian  mammal  previously 
known  from  isolated  teeth  and  only  three 
jaw  fragments  containing  more  than  one 
tooth  (see  Lillegraven  [1969],  Clemens 
[1973],  Archibald  [1982],  Storer  [1991], 
and  Lofgren  [1995]).  The  type  specimen, 
USNM  2139,  is  a  dentary  fragment  with 


'  Department  of  Biology,  Providence  College, 
Providence,  Rhode  Island  02918. 

-  Museum  of  Paleontology,  University  of  Cahfomia, 
Berkeley,  California  94720. 


Pi^i  in  place.  The  new  specimen,  UCMP 
136091,  is  a  fragment  of  a  right  maxillaiy 
with  almost  undainaged  M-^^  in  place  (Fig. 
1).  This  specimen  is  only  the  second  max- 
illary fragment  of  B.  tenuis  containing 
more  than  one  tooth  to  be  discovered  and 
contains  the  first  record  of  M^  for  the  spe- 
cies and  genus.  The  systematic  affinities  of 
Batodon  are  unclear,  and,  as  discussed  be- 
low, we  choose  to  regard  this  rare  genus 
as  incertae  sedis  within  the  Placentalia. 

Butler  (1961,  1972a),  Fox  (1975),  and 
Crompton  and  Kielan-Jaworowska  (1978), 
among  others,  have  advocated  a  functional 
approach  to  description  and  phylogenetic 
analysis  of  tribosphenic  mammals.  A  great 
deal  of  this  and  later  work  (including  this 
paper)  are  due  to  the  influence  of  Profes- 
sor A.  W  Cromptons  foundational  work 
on  the  origin  and  function  of  tribosphenic 
molar  teeth  (see  Crompton  [1971]  as  a 
landmark  example;  also  Crompton  and 
Hiiemae  [1969]  and  Crompton  and  Sita- 
Lumsden  [1970]). 

Our  first  goal  in  this  study  was  to  deter- 
mine whether  functional  correspondence 
of  the  new  specimen  (UCMP  136091) 
with  the  M2_3  present  in  UA  3721  (the  only 
known,  associated  last  two  lower  molars 
referred  to  B.  tennis  [Lillegraven,  1969]) 
reasonably  substantiates  allocation  of  both 
upper  and  lower  molars  to  the  same  spe- 
cies. Furthermore,  we  wished  to  deter- 
inine  if  the  molars  preserved  in  the  new 
specimen  show  close  size  and  morphologic 
similarity  to  all  other  previously  referred 


Bull.  Mus.  Comp.  Zool.,  156(1):  99-118,  October,  2001 


99 


100         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


1MM 

Figure  1.     Stereophotograph  of  UCMP  136091,  Batodon  tenuis,  maxillary  fragment  with  M^ 


specimens,  so  that  greater  confidence 
could  be  expressed  in  their  allocation  to  a 
single  species.  This  paper  perhaps  may 
serve  as  a  case  study  in  the  utility  of  func- 
tional association  of  isolated  Mesozoic 
postcanine  elements,  an  easy  and  yet  of- 
ten-neglected method.  Finally,  we  com- 
pare the  estimated  body  mass  of  B.  tenuis 
to  those  of  other  small  eutherians  and  an- 
alyze hypotheses  of  its  phylogenetic  rela- 
tionships. 

MATERIALS  AND  METHODS 

Nomenclature 

Here  we  follow  McKenna  and  Bell 
(1997)  in  formally  recognizing  Placentalia 
as  the  appropriate  name  for  the  clade  that 
frequently  is  dubbed  Eutheria.  Informally, 
reflecting  vernacular  use,  the  terms  euthe- 
rian  and  placentalian  are  recognized  as 
synonyms. 

Provenance  and  History 

The  new  maxillaiy  fragment,  UCMP 
136091,  described  here  comes  from  con- 
centrates obtained  in  1974  by  screen  wash- 
ing sedimentary  rocks  of  the  Hell  Creek 
Formation  at  the  Flat  Creek  Locality  5  (V- 
73087)  in  Garfield  County,  Montana.  Ar- 


chibald (1982:  166)  described  four  isolated 
teeth  of  B.  tenuis  from  this  locality.  The 
new  specimen  was  discovered  after  he 
coinpleted  his  monographic  study. 

Marsh  (1892)  established  B.  tenuis  on  a 
fragment  of  a  dentary  (USNM  2139)  con- 
taining Po^  from  the  Lance  Formation,  Ni- 
obrara County,  Wyoming.  The  type  locality 
is  UCMP  locality  no.  V-5003  (Clemens, 
1973),  also  referred  to  as  Mammal  locality 
no.  1  (Lull,  1915).  Additional  specimens  of 
B.  tenuis  have  been  reported  from  Lancian 
North  American  Land  Mammal  Age 
(NALMA)  local  faunas  of  the  Lance  For- 
mation, Wyoming  (Clemens,  1973);  the 
Scollard  Formation,  Alberta  (Lillegraven, 
1969);  the  Hell  Creek  Formation,  Mon- 
tana (Archibald,  1982);  and  the  French- 
man Formation,  Saskatchewan  (Storer, 
1991). 

A  boundary  between  the  Lancian  NAL- 
MA and  the  older,  still  poorly  character- 
ized "Edmontonian"  NALMA,  has  not 
been  defined.  In  part  this  reflects  the  pres- 
ence of  marine  units  (e.g.,  the  Beaipaw 
Shale)  separating  the  terrestrial  deposits 
producing  Lancian  and  "Edmontonian"  lo- 
cal faunas  (see  Lillegraven  and  McKenna, 
1986).   Recently  Hicks  et  al.   (1999)  esti- 


Functional  Molar  Association  in  Batodon  •  Wood  and  Clemens        101 


mated  the  duration  of  deposition  of  the 
Hell  Creek  Formation  in  North  Dakota, 
which  has  yielded  Lancian  local  faunas,  as 
encompassing  approximately  the  last  1.7 
million  years  (ca.  65.5-67.2  million  years 
before  the  present)  of  the  Cretaceous. 
This  can  be  taken  as  a  minimum  duration 
of  the  Lancian  NALMA  and  probably  in- 
cludes the  ages  of  all  known  occurrences 
of  B.  tenuis. 

Until  recently,  the  genus  Batodon  had 
not  been  reported  in  older,  Judithian 
NALMA  local  faunas  of  the  North  Amer- 
ican Western  Interior.  Some  of  these  are 
known  from  large  samples  obtained  by 
screen  washing  (e.g.,  Montellano,  1992). 
In  an  abstract,  Carrano  et  al.  (1997)  re- 
cently noted  the  discovery  of  Batodon  sp. 
at  an  unspecified  locality  in  the  type  area 
of  the  Judith  River  Formation.  When  fully 
documented,  this  record  would  greatly  ex- 
tend the  range  of  the  genus  over  approx- 
imately the  last  13  milHon  years  of  the 
Cretaceous. 

Batodon  tenuis  was  not  represented  in 
the  large  sample  of  the  early  Paleocene 
(Puercan  NALMA)  Hells  Hollow  local 
fauna  (Archibald,  1982).  Lofgren  (1995) 
recovered  four  isolated  teeth  referable  to 
B.  tenuis  from  channel  fillings  in  the  Hell 
Creek  Formation,  McCone  County,  Mon- 
tana, which  he  interpreted  to  have  been 
deposited  during  the  Puercan.  Because  of 
reworking,  these  channel  fillings  contain  a 
mixture  of  fossils  of  Puercan  and  Lancian 
vertebrates.  Sloan  and  Van  Valen  (1965) 
did  not  report  the  occurrence  of  B.  tenuis 
in  their  collections  from  the  Bug  Creek 
Anthills  locality  in  McCone  County.  The 
UCMP  collections  made  at  this  locality 
(Bug  Creek  Anthills,  V-87038,  87074, 
87151)  include  four  isolated  molars  refer- 
able to  this  species.  The  time  of  deposition 
of  the  channel  filling  at  Bug  Creek  Anthills 
and  the  composition  of  its  vertebrate  fauna 
have  been  disputed.  The  strongly  support- 
ed hypothesis  that  the  Bug  Creek  Anthills 
channel  filling  was  deposited  in  the  Puer- 
can and  contains  a  mixture  of  latest  Cre- 
taceous   and    early    Paleocene   vertebrate 


fossils  has  not  been  falsified  (for  discussion 
of  this  problem  see  Lofgren  et  al.  [1990] 
and  Lofgren  [1995]).  In  the  following  anal- 
ysis we  include  data  on  the  molars  from 
Bug  Creek  Anthills  locality  and  the  chan- 
nel fillings  investigated  by  Lofgren  (1995) 
but  do  not  interpret  them  as  documenting 
an  extension  of  the  range  of  Batodon  into 
the  Puercan.  At  least  in  the  North  Amer- 
ican Western  Interior,  the  genus  Batodon 
appears  to  have  become  extinct  at  the  end 
of  the  Cretaceous. 

Functional  Orientation 

To  obsei-ve  their  functional  orientation 
teeth  are  rotated  around  their  anterior- 
posterior  axes  until  the  line  of  sight  is  par- 
allel with  the  direction  of  movement  of  the 
lower  teeth  as  they  were  drawn  into  cen- 
tric occlusion  with  the  upper  teeth.  In  this 
orientation  the  paracone  and  metacone 
just  mask  views  of  their  respective  conules. 
All  polished  wear  facets  on  upper  and  low- 
er teeth  are  produced  by  simultaneous, 
parallel  shear  in  this  direction  ("phase 
one,"  see  Kay  and  Hiiemae  [1974]).  When 
the  proper  degree  of  rotation  has  been  at- 
tained, the  shear  facets  disappear  from 
view  because  they  are  aligned  parallel  with 
the  line  of  sight.  This  orientation  best  il- 
lustrates the  relative  lengths  of  shearing 
blades  and  other  functional  elements  of 
the  crown.  In  this  orientation,  upper  and 
lower  teeth  can  be  drawn  separately  on 
tracing  paper,  or  as  computer-based  im- 
ages, and  then  superimposed  to  show  pre- 
cise occlusal  relationships  of  all  their  cor- 
responding parts.  Wood  et  al.  (1979)  used 
this  technique  to  support  association  of 
rare,  isolated  upper  and  lower  teeth  of  the 
Paleocene  "primate,"  Torrejonia.  Howev- 
er, in  general,  this  technique  has  not  en- 
joyed wide  application  in  the  study  of  tri- 
bosphenic  dentitions. 

In  this  paper  our  figures  are  labeled  as 
"functional"  when  specimens  are  illustrat- 
ed in  the  functionally  rotated  view,  and 
"crown"  in  the  orientation  that  has  tradi- 
tionally been   labeled   as   "occlusal  view" 


102         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


(but  see  Crompton  and  Kielan-Jaworows- 
ka  [1978]  for  additional  terms). 


Abbreviations 
AMNH 

NALMA 

P  2004.565 

UA 
UCMP 

USNM 

V-5711 

RESULTS 


American  Museum  of  Nat- 
ural History 

North      American      Land 
Mammal  Age 

Specimen    numbers    given 
in  this  format  are  from  the 
Saskatchewan    Museum   of 
Natural  Histoiy 
University  of  Alberta 
University    of    California 
Museum  of  Paleontology 
Natural    History   Museum, 
Smithsonian  Institution 
Locality  designations  given 
in  this  format  are  from  the 
UCMP  locality  catalog 


Description  of  New  Specimen 

When  discovered  much  of  the  new  max- 
illary fragment  (UCMP  136091)  was  ob- 
scured by  loosely  adhering  sand  grains. 
The  parastylar  region  of  M-  was  missing. 
During  cleaning  the  M-  separated  from 
the  M^  allowing  the  adjacent  sides  of  the 
molars  to  be  illustrated  fully.  Subsequent- 
ly, the  maxillary  fragments  were  rejoined 
and  the  molars  exactly  restored  to  their 
original  positions.  Figure  1  is  a  stereopho- 
tograph  of  the  cleaned  and  restored  spec- 
imen in  crown  view.  Figure  2  is  made  up 
of  line  drawings  of  the  two  molars  in  tra- 
ditional crown,  lingual  oblique,  labial,  an- 
terior, functional,  and  posterior  views. 

The  crown  view  of  M^  of  UCMP  136091 
(Fig.  2 A)  does  not  clearly  illustrate  some 
postmortem  damage  to  the  tooth.  At  high- 
er magnifications  of  the  anterior  view  (Fig. 
2E)  the  enamel  is  obviously  broken  and 
lacking  from  the  extremely  narrow  area  of 
attachment  of  a  parastylar  lobe.  The  an- 
terior root  beneath  the  paracone  is  also 
freshly  broken.  The  parastylar  lobe  is  bro- 


ken away  from  all  other  known  upper  mo- 
lars except  UA  4081,  P  2004.565,  and  the 
M^  of  UCMP  136091.  On  M^  of  UA  4081 
(Fig.  3),  the  parastylar  lobe  is  a  prominent 
but  very  thin  and  delicate  structure;  one 
may  surmise  that  it  survived  only  because 
it  was  protected  by  the  stout  metastylar 
blade  of  M^. 

Superimposed  crown  views  (not  illus- 
trated) of  the  M2  of  UCMP  136091  and  of 
UA  4081  are  remarkably  coincident,  es- 
pecially in  the  areas  of  the  protocones, 
paracones,  metacones,  and  conules.  Dif- 
ferences are  in  a  slightly  inore  robust  labial 
edge  of  the  metastylar  area  of  UCMP 
136091  and  its  more  robust  precingulum. 
The  postcingulum  of  UA  4081  is  slightly 
more  robust  than  that  of  UCMP  136091 
and  is  absolutely  larger  in  its  labial  exten- 
sion beneath  the  metaconule.  Although 
not  the  case  on  the  molars  of  UCMP 
136091,  on  some  molars  of  B.  tennis  the 
pre-  and  postcingula  meet  on  the  lingual 
slope  of  the  protocone  (Lillegraven,  1969). 
Some  apical  wear  is  apparent  on  the  rims 
of  the  pre-  and  postcingula  of  M-s  of  B. 
tenuis.  Evidently  they  did  not  produce  a 
shear.  The  cingula  appear  to  have  served 
as  stops  for  the  lower  teeth  as  they  came 
to  their  limits  in  centric  occlusion.  Perhaps 
selective  pressures  would  be  less  for  pre- 
cision in  shape  of  these  structures  than 
would  have  been  the  case  for  the  func- 
tional shearing  blades  higher  on  the  crown 
(but  see  Polly,  1998a). 

The  specimen  UCMP  102909  lacks 
clearly  developed  internal  wings  of  the 
conules.  On  UCMP  117649,  one  of  the 
specimens  described  by  Archibald  (1982), 
the  metaconule  has  a  distinct  internal 
wing;  a  weaker  but  still  distinct  internal 
wing  is  present  on  the  paraconule.  The 
stages  of  wear  of  UCMP  136091  and  UA 
4081  are  approximately  equivalent.  The 
conules  of  both  have  distinct  internal 
wings  that  are  emphasized  by  wear,  which 
produced  chevrons  of  dentine  within  the 
enamel  lining  of  the  trigon  basin. 

In  labial  and  lingual  oblique  views  of 
Batodon  molars,  the  paracones  and  meta- 


II 


Functional  Molar  Association  in  Batodon  •  Wood  and  Clemens        103 


B 


CROWN 


LINGUAL  OBLIQUE 


LABIAL 


ANTERIOR 


F 


MM 


FUNCTIONAL 


POSTERIOR 


Figure  2.  Line  drawings  of  M^  ^  UCMP  136091,  Batodon  tenuis.  (A)  Crown  views;  arrows  to  M='  indicate  projecting  metacone 
and  metaconule;  arrowhead  to  M^  indicates  damaged  part  of  parastylar  area.  Posterior  is  to  left  and  anterior  is  to  right.  (B) 
Ungual  oblique  views;  additional  large  arrow  on  M^  indicates  heavily  worn  groove  between  nnetacone  and  paracone.  (C)  Labial 
views;  arrowhead  indicates  damaged  parastylar  area  of  M=^.  (D)  Functionally  rotated  views.  (E)  Anterior  views;  arrowhead  indi- 
cates damaged  parastylar  region  of  M=.  (F)  Posterior  views.  Abbreviations:  me,  metacone;  pa,  paracone;  pr,  protocone;  ac, 
anterior  protocone  cingulum  (precingulum);  pc,  posterior  protocone  cingulum. 


cones  are  closely  conjoined  from  their  ba- 
ses to  perhaps  one  half  or  two  thirds  of 
the  distance  to  their  apices.  Such  mor- 
phology might  suggest  that  little  or  no 
shear  occurred  directly  between  the  para- 
cone and  inetacone.  However,  in  worn 
specimens,  it  is  evident  that  the  hypoconid 


of  the  lower  molar  scraped  a  strong  groove 
on  the  lingual  surfaces  of  those  cusps  be- 
fore passing  between  the  internal  conule 
wings  and  into  the  deeply  excavated  trigon 
basin.  A  comparably  large  hypoconid  is  not 
evident  in  Cenozoic  genera  such  as  Pa- 
laeoryctes  or  Didelphodus,  but  is  approxi- 


104         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


CROWN 


LINGUAL  OBLIQUE 


LABIAL 


POSTERIOR 


I  MM 


FUNCTIONAL 


Figure  3.  Line  drawings  of  M'-^,  from  cast  of  UA  4081,  Batodon  tenuis,  from  the  Scollard  Formation,  Alberta,  Canada  (see 
Lillegraven  [1969]).  (A)  Crown  view.  (B)  Lingual  oblique  view  of  M^  only.  (C)  Labial  view.  (D)  Functional  view,  orientation  as  in 
Figure  2D.  (E)  Posterior  view  of  M==  only. 


mated  in  some  Lancian  species  of  Cimo- 
lestes.  Lipotyphlans,  many  condylarths, 
and  their  descendants  often  emphasize 
shearing  between  the  hypoconid  and  the 
blades  of  the  centrocrista  that  Hnk  the 
metacone  and  paracone,  which  usually  are 
well  separated  to  their  bases. 

Superimposed  labial  and  lingual  oblique 


views  of  M2  of  UCMP  136091  and  M^  of 
UA  4081  demonstrate  that  the  former  has 
a  slightly  less  bowed  ectoflexus  and  a  more 
robust  and  absolutely  larger  metacone  and 
metastylar  blade.  Slightly  greater  wear  on 
the  metastylar  blade  of  UA  4081  might 
overemphasize  the  difference,  but  we  sus- 
pect that  the  difference  is  real,  yet  within 


Functional  Molar  Association  in  Batodon  •  Wood  and  Clemens        105 


the  limits  of  individual  variation.  A  small  cone.  The  pre-  and  postcingula  are  prom- 
cuspule  or  expansion  of  the  external  edge  inent,  but  the  postcingulum  is  relatively 
of  the  central  stvlar  shelf  is  present  on  small  in  comparison  to  those  of  other  mo- 
both  specimens.  On  M-s  of  B.  tenuis  the  lars.  The  cingula  are  more  widely  separat- 
paracone  is  taller  than  the  metacone.  ed  by  the  strong  lingual  slope  of  the  pro- 
Using  the  cervical  limit  of  enamel  as  a  tocone  than  on  M-. 
base  line,  in  anterior  and  posterior  views  The  metacone  is  reduced  in  size,  but 
of  M-  the  protocones  of  all  specimens  are  still  quite  prominent;  it  forms  a  distinct 
almost  as  high  as  the  paracones,  and  about  projection  in  the  lingual  oblique  view  (Fig. 
the  same  height  or  higher  than  the  meta-  2B).  Metacone  and  paracone  are  closely 
cones.  The  profile  of  the  protocone  is  es-  conjoined  at  their  bases,  as  on  M-,  and 
pecially  pointed  and  triangular.  As  Lille-  wear  emphasizes  the  greater  angle  at 
graven  (1969:  82)  noted,  because  of  the  which  they  diverge.  A  wear  facet  extends 
exaggerated  protocone,  the  stylar  shelf  of  down  the  conjoined  lingual  slopes  of  the 
Batodon  appears  relatively  narrow,  but  in  metacone  and  paracone  showing  that  the 
absolute  width  its  proportions  are  compa-  hypoconid  of  Mj  sheared  down  into  the 
rable  to  the  stylar  shelf  of  Ciniolestes  cer-  trigon  basin  past  the  distinct  internal  wings 
beroides,  for  exainple.  of  the  conules.  The  internal  surface  on  the 
In  anterior  view  (Fig.  2E),  the  paracone  paraconule  wall  is  worn  flat.  Resembling 
is  quite  steep-sided  and  apically  almost  the  metacone,  the  metaconule  projects 
rectangular  in  outline.  In  contrast,  the  pos-  posteriorly.  The  posterior  inclination  of  the 
terior  profile  of  the  metacone  sweeps  la-  metacone  and  metaconule  accoinmodated 
bially  into  the  large  metastylar  blade.  The  strong  hypoconid  shear  within  the  trigon. 
posterior  metaconule  wing  is  clearly  a 
strong  enechelon  shearing  blade  contact- 
ing the  preprotocristid  of  the  lower  molar  Storer  (1991)  described  the  mammals  of 
after  it  passed  the  metastylar  blade.  The  the  Lancian  Gryde  local  fauna,  Saskatch- 
anterior  wing  of  the  paraconule  also  forms  e\van.  The  sample  included  an  upper  right 
a  strong  shearing  blade  for  the  postproto-  molar,  P  2004.565  (Fig.  4),  that  has  been 
cristid,  but  the  primary  blade  on  the  an-  identified  tentatively  as  an  M^  of  B.  tenuis. 
terior  slope  of  the  paracone,  the  prepara-  Storer  (1991)  noted  that  the  specimen  has 
crista,  is  less  distinct,  as  often  is  the  case  a  more  anteriorally  directed  preparacrista 
in  "proteutherians"  (see  Crompton  and  than  the  M-  of  UA  4081  (Fig.  3).  Also,  P 
Kielan-Jaworowska  [1978]).  2004.565  has  a  relatively  smaller  parastylar 

lobe.  These  moi^phologic  differences  sup- 
port  Storer  s  tentative  identification,  which 

The  specimen  UCMP  136091  is  the  first  is  accepted  here, 
speciinen  of  B.  tenuis  to  preserve  M^  in 

association  with  other  identifiable  molars.  Lower  Dentition 

The  M^  of  the  new  specimen  has  a  robust  The  type  specimen  of  B.  tenuis,  USNM 
parastylar  lobe  with  a  deep  groove  to  re-  2139,  is  an  anterior  dentaiy  fragment  con- 
ceive the  protoconid  of  M3.  In  anterior  taining  P2_4.  The  specimen  AMNH  58777 
view,  the  paracone-parastylar  shearing  preserves  P^,  a  major  part  of  P3,  and  P4  and 
blade  is  more  distinct  than  on  M^,  and  the  Mj.^  (illustrated  in  Clemens,  1973).  Com- 
shearing  blade  of  the  anterior  paraconule  parable  small  size  and  morphologic  simi- 
wing  is  also  strong.  The  protocone  is  con-  larity  of  P4  to  that  of  USNM  2139  are  the 
siderably  less  triangular  in  anterior  view,  basis  for  reference  of  AMNH  58777  to  B. 
but  is  as  triangular  as  that  of  M-  in  pos-  tenuis.  Likewise  small  size  and  close  mor- 
terior  view.  The  protocone  is  taller  than  phologic  similarity  of  the  molars  of  AMNH 
the  metacone  but  not  as  tall  as  the  para-  58777  and  UA  3721  (Fig.  5)  are  the  bases 


106         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


B 


CROWN 


LINGUAL  OBLIQUE 


LABIAL 


ANTERIOR 


MM 


D 


FUNCTIONAL 


POSTERIOR 


Figure  4.  Line  drawings  of  ?M\  P  2004.565,  Batodon  tenuis,  from  the  Gryde  local  fauna,  Frenchman  Formation,  Saskatchewan, 
Canada  (see  Storer  [1991]).  Note  that  in  all  views  the  parastylar  area  is  intact.  (A)  Crown  view.  (B)  Lingual  oblique  view.  (C) 
Labial  view.  (D)  Functional  view.  (E)  Anterior  view.  (F)  Posterior  view. 


Functional  Molar  Association  in  Batodon  •  Wood  and  Clemens        107 


h^cld 


Mp  pad      med  M-a 

CROWN 


ANTERIOR         POSTERIOR 


LINGUAL 


FUNCTIONAL 


IMM 


LABIAL 


Figure  5.  Line  drawings  of  M2_3,  from  cast  of  UA  3721,  Batodon  tenuis,  from  the  Scollard  Formation,  Alberta,  Canada  (see 
Lillegraven  [1969]).  (A)  Crown  view.  (B)  Lingual  view.  (C)  Labial  view.  (D)  Anterior  view  of  M^  and  posterior  view  of  M3.  (E) 
Functionally  rotated  orientation.  Abbreviations:  pad,  paraconid;  med,  metaconid;  prd,  protoconid;  hyd,  hypoconid;  hycid,  hypo- 
conulid;  entd,  entoconid. 


for  reference  of  the  latter  to  this  species. 
Detailed  descriptions  of  the  morphology 
of  these  specimens  can  be  found  in  Lille- 
graven (1969)  and  Clemens  (1973). 

Functional  Relationships  of  Upper  and 
Lower  Molars 

Figure  6  illustrates  correspondingly 
numbered  functional  shear  blades  on  up- 
per and  lower  molars  (after  Crompton  and 
Hiiemae  [1969]).  Figures  7  and  S  are  com- 
posite (same-scale)  drawings  of  the  M-^^  of 
UCMP  136091  and  the  M^  and  fragment 


of  M^  of  UA  4081,  each  shown  in  occlusion 
with  M,^3  of  UA  3721  (Fig.  5).  All  the 
teeth  are  illustrated  in  functional  orienta- 
tion. The  occlusal  fit  of  UCMP  136091 
with  UA  3721  (Fig.  7)  is,  overall,  some- 
what better  than  for  UA  3721  and  the  up- 
per molars  of  UA  4081  (Fig.  8).  The  M^-^ 
of  UCMP  136091  occlude  very  well  with 
M2_3  of  UA  3721  (Fig.  7),  especially  in  the 
areas  between  the  hypoconid  and  para- 
cone— metacone  embrasure.  With  these 
functional  units  of  opposing  second  and 
third  molars  in  place,  some  other  function- 


lOS         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


4a      3o 


2a -^ 


Figure  6.  Line  drawings  of  M=  ^  UCMP  136091,  and  UA  3721,  Batodon  tenuis,  to  indicate  corresponding  functional  shear 
blades  (see  Crompton  and  Hiiemae  [1969]  and  Crompton  and  Kielan-Jaworowsl<a  [1978]).  (A)  M^^^,  UCMP  136091  in  crown 
view.  Abbreviations:  la,  preparacrista;  lb,  preparaconule  crista  (anterior  wing);  2a,  postmetacrista;  2b,  postmetaconule  crista 
(posterior  wing);  3a,  postparacrista;  3b,  postmetaconule  crista  (posterior  wing);  4a,  premetacrista;  4b,  premetaconule  crista 
(anterior  wing);  5,  preprotocrista;  6,  postprotocrista.  (B)  UA  3721  in  functional  view.  Abbreviations:  siiear  blades:  1,  postproto- 
cristid;  2,  preprotocristid;  3,  cristid  obliqua;  4,  posthypocristid;  5,  postmetacristid  and  posterior  wall  of  metaconid;  6,  pre-entoconid 
cristid. 


al  units  are  not  quite  in  perfect  occlusion. 
The  slight  gap  between  metacone  and  hy- 
poconulid  of  the  second  molar  could  be 
due  to  slightly  greater  wear  on  the  upper 
tooth  or  simply  to  intraspecific  variation  in 
size.  However,  the  protocones  of  M-"^^^  are 
slightly  too  extended  lingually  to  fit  com- 
fortably into  the  talonid  basins  of  Mo_3. 
This  most  probably  indicates  individual 
variability  in  size.  The  function  of  the  po- 
stcingulum  of  M^  as  an  embrasure  stop  is 


clearly  reflected  in  the  narrowed  and  dor- 
soventrally  lowered  configuration  of  the 
paraconid  of  M3. 

Lillegraven  (1969:  84)  and  subsequent 
students  of  B.  tenuis  have  commented  on 
the  posterior  projection  of  the  hypoconu- 
lid  and,  therefoi^e,  the  "extended  talonid" 
of  M3.  The  large,  posteriorly  projecting 
metacone  and  metaconule  of  M^  are  func- 
tionally related  to  the  extended  talonid  of 
M3.  Shearing  facets  on  the  anterior  face  of 


Functional  Molar  Association  in  Batodon  •  Wood  and  Clemens        109 


UCMP  136091 


UA  3721 


B 


Figure  7.  Functional  views  of  IVl^-^  (UCMP  136091)  and  M2_3  (UA  3721,  reversed),  Batodon  tenuis.  (A)  Separated  views  of 
molars.  (B)  Upper  and  lower  molars  shown  in  centric  occlusion.  Corresponding  strong  shear  blades  3  and  4  on  the  third  molar, 
as  well  as  a  functional  postcingulum  and  extended  hypoconulid,  indicate  that  the  upper  and  lower  dentitions  represent  the  same 
species. 


the  metacone  (facet  4a,  Fig.  6)  and  inter- 
nal metaconule  wing  (facet  4b,  Fig.  6)  oc- 
cluded against  the  posterior  side  of  the  hy- 
poconid  and  labial  side  of  the  enlarged  hy- 


poconulid. The  remainder  of  the  hypocon- 
ulid is  covered  by  the  postcingulum  of  the 
upper  molar,  but  it  is  not  clear  whether 
crushing  occurred  between  thein  at  full 


110         Bulletin  Museum  of  Comparative  Zoologtj,  Vol.  156,  No.  1 


UA408I 


UA372I 


B 


Figure  8.     Functional  views  of  fragmentary  M'  and  M^  (UA  4081,  reversed)  and  Mj 
of  molars.  (B)  Upper  and  lower  molars  shiown  in  centric  occlusion. 


(UA  3721 ,  reversed).  (A)  Separated  views 


occlusion.  Although  not  unique  among  eu- 
therians,  enlargement  of  the  hypoconulid 
and  posterior  projection  of  metacone  and 
metaconule  are  not  seen  in  many  palaeo- 
ryctids  (Cimolestes  and  Procerbenis  ex- 
cepted) or  in  undoubted  lipotyphlans  in 
which  there  is  a  trend  to  reduce  the  entire 
size  of  the  last  molar.  This  morphology 
could  be  either  a  plesiomorphic  or  an  au- 
tapomorphic  condition  of  B.  tenuis.  In  Ba- 
todontoides  (see  Bloch  et  al.  [1998]),  M,  is 


smaller  than  Mo,  as  is  the  case  in  the  larger 
geolabidids  (Lillegraven  et  al.,  1981).  Par- 
antjctoides  (Fox,  1979,  1984)  has  an  ex- 
tended Mj  talonid,  and  Fox  (1984:  15) 
considered  an  M3  hypoconulid  "strongly 
developed,  projecting  upward  in  finger- 
like fashion"  to  be  a  primitive  character 
state  for  eutherian  mammals. 

Although  the  overall  fit  is  not  as  good  as 
for  UCMP  136091,  M^  of  UA  4081  oc- 
cludes reasonably  well  with  M^  of  UA  3721 


Functional  Molar  Association  in  Batodon  •  Wood  and  Clemens        111 


Table  1.    Measurements  (mm)  of  molars  referred  to  Batodon  tenuis* 


Locality' 

State 

Specimen 

Tooth 

Length 

Width 

Comments 

Upper  molars 

W3087 

MT 

UCMP  136091 

M^ 

0.97 

1.64 

Lacks  parastyle 

V730S7 

MT 

UCMP  136091 

M^ 

0.99 

1.45 

Parastyle  present 

UA  4081 

M^ 

1.09 

1.69 

Parastyle  present 

UA  4081 

M2 

0.82 

Excluding  parastyle 

V73087 

MT 

UCMP  117649 

M2? 

0.92 

1.55 

Lacks  parastyle 

V70201 

MT 

UCMP  102909 

M2? 

0.82 

1.76 

Lacks  parastyle 

V87308 

MT 

UCMP  133080 

M^? 

1.00  (b) 

1.62 

Width 
frigonid 

Width 
talonid 

Lacks  parastyle 

Lower  molars 

V73087 

MT 

UCMP  117651 

M3? 

1.28 

0.82 

0.65 

UA  3721 

M3 

1.11 

0.75 

0.60 

UA  3721 

M2 

1.04 

0.82 

0.60 

V73087 

MT 

UCMP  117652 

M,? 

0.63 

V70201 

MT 

UCMP  92590 

M.,? 

1.33 

0.77 

0.70 

V70201 

MT 

UCMP  100638 

Mo? 

1.16 

0.80 

0.70 

V70201 

MT 

UCMP  98188 

M„? 

1.21 

0.77 

0.60 

V87074 

MT 

UCMP  133764 

M,? 

1.21 

0.77 

0.68 

V87151 

MT 

UCMP  132174 

M2? 

1.26 

1.09 

V5711 

WY 

AM  58777 

M2 

1.25  (a) 

0.80  (a) 

0.65  (a) 

V5711 

WY 

AM  58777 

Ml 

1.30  (a) 

0.75  (a) 

0.70  (a) 

V73087 

MT 

UCMP  117650 

P4 

1.21 

0.60 

V87038 

MT 

UCMP  133081 

P. 

1.21 

0.60 

V5711 

WY 

AM  58777 

P4 

1.25  (a) 

0.50  (a) 

V5003 

WY 

USNM  2139 

P4 

1.20  (a) 

*  All  measurements  taken  by  C.B.W.  w^th  the  exception  of  those  taken  by  W.A.C.  (a)  and  Donald  Lofgren 


(b). 


(Fig.  8).  In  fact,  for  occlusion  of  the  pro- 
tocone  into  the  talonid  basin,  UA  4081  has 
a  better  size  and  fit.  The  iTiain  discrepancy 
is  in  the  area  of  the  paracone-cristid  obli- 
qua,  or  (if  adjusted  there)  between  pro- 
toconid  and  parastylar  area.  The  differenc- 
es are  not  great  and  may  be  as  expected 
with  an  attempt  to  occlude  the  upper  and 
lower  dentitions  of  different  individuals 
from  the  saine  species. 

Reference  of  Specimens  to  One  Species, 
Batodon  tenuis 

One  of  the  purported  diagnostic  char- 
acters of  B.  tenuis  is  its  diminutive  size. 
The  fossils  referred  to  this  species  are  the 
smallest  eutherian  teeth  found  in  Lancian 
local  faunas  of  the  North  American  West- 
em  Interior.  Geographically  these  sites  ex- 
tend froin  central  Alberta  in  the  north  to 
central    eastern    Wyoming    in    the    south. 


Making  allowances  for  individual  and  pos- 
sible latitudinal  variation,  are  the  patterns 
and  ranges  of  variation  in  dimensions  what 
might  be  expected  for  a  primitive  euthe- 
rian species? 

Measurements  and  locality  data  for  the 
available  sample  of  B.  tenuis  are  given  in 
Table  1.  In  order  to  avoid  introduction  of 
variation  through  use  of  different  instru- 
ments, coefficients  of  variation  (CVs)  were 
calculated  only  for  specimens  iTieasured  by 
C.B.W.  In  general  CV  values  are  within 
the  ranges  found  in  other  early  tribos- 
phenic  eutherian  species  known  from 
much  larger  sainples  (see  Polly  [1998b]  for 
a  recent  discussion  of  CVs  in  smaller 
mammals).  Of  course,  the  range  of  coef- 
ficients for  B.  tennis  might  be  the  product 
of  small  sample  size  and  uncertainty  in  dis- 
tinguishing between  isolated  specimens 
such  as  those  representing  M^  and  M^.  Co- 


112         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Table  2.    Statistical  summary  for  dimensions  (mm)  of  teeth  referred  to  Batodon  tenuis.* 


Tooth 


Dimension 


Number 


OR 


Mean 


SD 


c;\' 


M,,  all  specimens 

M2,  excluding  UCMP  132174 


Length 

4 

0.8-1.0 

0.88 

0.08 

8.50 

Width 

5 

1.5-1.8 

1.65 

0.08 

4.75 

Length 

2 

1.2-1.2 

1.21 

0.00 

0.00 

Width,  trigonid 

2 

0.6-0.6 

0.60 

0.00 

0.00 

Length 

6 

1.0-1.3 

1.20 

1.00 

8.14 

Width,  trigonid 

6 

0.8-1.1 

0.84 

0.13 

15.04 

Width,  talonid 

6 

0.6-0.7 

0.65 

0.05 

7.29 

Length 

5 

1.0-1.3 

1.19 

0.10 

8.79 

Width,  trigonid 

5 

0.8-0.8 

0.79 

0.02 

2.93 

Width,  talonid 

5 

0.6-0.7 

0.65 

0.05 

7.29 

*  OR,  Observed  range;  SD,  Standard  deviation;  CV,  coefficient  of  variation. 


efficients  for  widths  are  generally  lower, 
and  it  is  this  dimension  that  usually  is  least 
affected  by  position  in  the  tooth  row.  One 
glaring  exception  is  in  width  of  trigonid  of 
M,.  However,  when  measurements  of 
UCMP  132174  are  removed  from  the  cal- 
culation, the  discrepancy  is  much  less  ev- 
ident (see  Table  2).  Some  reassessment  of 
the  identity  of  UCMP  132174,  an  isolated 
molar,  may  be  indicated.  It  is  evident  by 
inspection  that  some  of  the  dimensions  on 
specimens  from  the  Scollard  Formation, 
Alberta,  are  on  the  small  end  of  the  size 
range.  However,  this  is  not  consistently 
true  for  all  dimensions.  With  these  excep- 
tions, at  present,  variation  in  dental  di- 
inensions  does  not  deinand  recognition  of 


Table  3.    Measurements  (mm)  of  anterior  and 
posterior  margins  of  M^  of  Batodon  tenuis  ex- 
cluding THE  STi'LAR  AREA. 

Lengths 


Locality 

Specimen 

.interior 

Posterior 

V73087 

UCMP  136091 

4.1 

4.0 

UA  4081 

4.1 

4.0 

V73087 

UCMP  117649 

3.7 

4.5 

V70201 

UCMP  102909 

3.9 

4.1 

V87308 

UCMP  133080 

3.6 

4.0 

Statistical  summary  of  dimensions  of  margins  for  M-'* 


Dimension 

Num- 
ber 

OR 

Mean 

SD 

CV 

Anterior  margin 
Posterior  margin 

5 
5 

3.6-4.1 
4.0-4.5 

3.88 
4.12 

0.23 
0.22 

5.88 
5.26 

*  OR,  Observed  range;  SD,  standard  deviation;  CV, 
coefficient  of  variation. 


more  than  one  species  of  Batodon  in  the 
Lancian  local  faunas  sainpled  to  date. 

Interestingly,  ineasurements  of  the  an- 
terior and  posterior  margins  (protocone  to 
paracone,  protocone  to  inetacone  in  crown 
view,  excluding  the  stylar  areas)  of  M-  of 
B.  tenuis  (Table  3)  are  much  more  uniform 
than  standard  measurements  for  length  on 
the  tribosphenic  crown.  Measureinents  of 
these  nonstandard  dimensions  for  the  new 
specimen  (UCMP  136091)  and  for  UA 
4081  are,  in  fact,  identical.  Mention  was 
made  above  of  the  coincidence  of  proto- 
cone and  conule  outline  in  superimposed 
drawings,  and  of  the  possibility  that  this 
area  could  be  under  greater  selective  pres- 
sure for  uniformity  than  would  other  parts 
of  the  teeth.  Such  a  possibility  would  be 
purely  hypothetical  at  present,  of  course, 
and  is  based  on  an  inadequate  sample,  but 
extended  comparative  studies  of  better- 
known  genera  would  be  a  worthwhile  test 
of  this  idea.  Although  Polly  (1998a)  has  re- 
ported that  developmental  factors  may 
correlate  better  than  functional  factors  in 
tooth  crown  measurements  of  viverravid 
carnivores,  new  data  from  extant  Sorex 
may  demonstrate  different  patterns  of  var- 
iability (D.  Polly,  personal  communica- 
tion). 

In  smnmary,  reference  of  the  smallest 
tribosphenic  eutherian  teeth  from  Lancian 
localities  in  the  North  American  Western 
Interior  to  a  single  species,  B.  tenuis,  is 
supported   by   several   lines   of  evidence. 


Functional  Molar  Association  in  Batodon  •  Wood  and  Clemens        113 


\Mien  merged  into  a  single,  albeit  small 
sample,  observed  ranges  and  coefficients 
of  variation  of  taxonomically  significant 
tooth  dimensions  are  what  would  be  ex- 
pected to  characterize  a  single  species 
(Polly,  1998b).  Sizes  and  configurations  of 
cusps,  basins,  and  shearing  crests  of  upper 
and  lower  teeth  document  a  common  oc- 
clusal pattern.  Possibly  diagnostic  special- 
ization of  occluding  elements  of  the  pos- 
terior parts  of  M^  and  M.,  add  support  to 
the  proposed  association  of  upper  and  low- 
er molars. 

DISCUSSION 

Dentition 

Analyses  of  patterns  of  occlusion  using 
the  functional  orientation  have  strength- 
ened the  basis  for  association  of  the  upper 
and  lower  dentitions  of  B.  tenuis.  Its  upper 
dentition  is  now  known  from  P^  through 
M3  (P^  illustrated  by  Lillegraven  [1969] 
but  lost  before  publication;  Storer  [1991] 
offers  a  possible  P\  P  2004.30);  the  lower 
is  knowTi  from  P^  through  M3.  Although 
more  anterior  teeth  are  unknown  or  rep- 
resented only  by  fragments,  it  is  clear  that 
the  canine  was  large  (USNM  2139)  and 
that  the  dental  formula  was  I?,  CI,  P4, 
M3. 

Body  Mass 

By  Cenozoic  standards.  Cretaceous 
marsupials,  eutherians,  and  their  closely 
related  sister  groups  were  animals  of  small 
to  very  small  body  mass.  Lillegraven  et  al. 
(1987)  argued  that  small  body  masses,  in 
the  context  of  metabolic  and  reproductive 
constraints,  played  a  significant  role  in  the 
origin  and  diversification  of  tlie  earliest 
marsupials  and  eutherians.  Because  most 
Cretaceous  and  early  Cenozoic  mammals 
were  known  from  only  isolated  teeth, 
many  early  estiinates  of  body  mass  were, 
at  best,  educated  guesses.  Then,  based  on 
data  from  living  species,  Gingerich  and 
Smith  (1984)  pioneered  the  development 
of  a  method  to  use  the  area  of  the  crown 
of  M,  to  estimate  the  body  mass  of  extinct 


eutherians.  Recently,  Bloch  et  al.  (1998) 
presented  a  version  of  this  technique  mod- 
ified specifically  to  estimate  the  body  mas- 
ses of  lipotyphlans  and  proteutherians.  In 
their  sui-vey  of  the  modem  lipotyphlans, 
Bloch  et  al.  (1998)  divided  the  group  into 
seven  classes  of  body  mass.  The  three 
smallest  classes  and  the  percentage  of 
modem  species  included  in  each  were  1— 
3  g  (3%),  3-7  g  (26%),  and  7-20  g  (35%). 
Bloch  et  al.  (1998)  demonstrated  that,  in 
comparison  to  the  range  of  variation  of 
body  masses  of  extant  lipotyphlans,  late 
Paleocene  (Clarkforkian)  and  early  Eocene 
(Wasatchian)  purported  lipotvphlans  oc- 
cupied the  lower  end  of  the  range  of  var- 
iation. The  body  mass  of  the  extinct  spe- 
cies, Batodontoides  vanhouteni,  from  the 
Wasatchian  of  Wyoining,  was  estiinated  to 
have  been  approximately  1.3  g,  and,  thus, 
was  the  smallest,  nonvolant,  Cenozoic  eu- 
therian  yet  knov\ai. 

Bloch  et  al.  (1998)  did  not  extend  their 
study  to  include  Cretaceous  eutherians.  In 
Table  4  we  present  measureinents  of  lower 
first  molars  and  estimates  of  body  mass  of 
the  smallest  eutherians  or  probable  euthe- 
rians in  several  local  faunas  ranging  from 
the  Aptian-Albian  (ca.  110  million  years 
before  the  present)  through  the  Lancian. 
The  estimated  body  mass  (8.05-8.53  g)  of 
Montanalestes  keebleri  of  Early  Creta- 
ceous  (Aptian-Albian)  age,  die  most  prim- 
itive pui-ported  eutherian  (Cifelli,  1999) 
from  North  America,  falls  sfightly  above 
the  arbitrary  boundary  between  the  sec- 
ond and  third  modern  lipotyphlan  body 
mass  classes.  Similarly,  Prokennalestes  mi- 
nor, the  smallest  known  Asian  eutherian, 
also  of  Early  Cretaceous  age,  has  an  esti- 
mated body  mass  of  6.76  g,  falling  slightly 
below  this  boundary.  The  oldest  (Aquilan— 
Judithian)  and  most  primitive  North 
American  genus  of  unquestioned  eutheri- 
an affinity  is  Faranijctoides,  which  is 
knov\Ti  from  two  species,  P.  nialeficus  (Fox, 
1984)  and  P.  sternbergi  (Fox,  1979).  Esti- 
mates of  body  mass  of  these  species  range 
between  9  and   16  g,  that  is,  within  the 


114         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Table  4.    Estimates  of  body  mass  of  species  of  Batodon,  Paranyctoides,  Prokennalestes,  and  Mon- 

tanalkstes. 


Me 

usurements  nf  M 

- 

Widtli 

Width 

Taxon 

Length 

trigonid 

taloiiid 

Estimated  mass 

Notes,  references 

Batodon  tenuis 

1.30 

0.75 

0.70 

5.39 

AMNH  58777,  Clemens,  1973 

Paranyctoides  stembergi 

1.50 

0.90 

1.25 

15.63 

UA  14822,  C.B.W.  measurements 

Paranyctoides  nialeficus 

1.6 

1.0 

1.1 

14.10 

UA  16168,  Fo.x,  1984 

1.5 

0.8 

0.9 

9.16 

UA  17170,  Fox,  1984 

1.5 

0.7 

0.9 

9.16 

UA  16171,  Fox,  1984 

1.5 

0.9 

1.0 

10.87 

UA  16175,  Fox,  1984 

1.6 

0.9 

1.0 

12.08 
11.07 

UA  16181,  Fox,  1984 
Average 

Prokennalestes  minor 

1.4 

0.8 

0.6 

6.76 

Kielan-Jaworowska  and  Dashzeveg, 
1989 

Montanalestes  keebleri 

1.42 

0.91 

0.65 

8.53 

Left  Mj,  R.  Cifelli,  personal  com- 
munication 

1.45 

0.86 

0.64 

8.05 
8.29 

Right  Ml,  R.  Cifelli,  personal 

communication 
Average 

third   class   of  body   mass   recognized  by 
Bloch  et  al.  (1998). 

Isolated  lower  first  and  second  molars  of 
B.  tenuis  cannot  be  distinguished  with  cer- 
tainty, and  we  have  not  used  them  for  es- 
timates of  body  mass.  Only  one  Mj  of  B. 
tenuis  has  been  found  in  place  in  a  dentary 
(AMNH  58777).  The  body  mass  of  this  in- 
dividual is  estimated  as  having  been  5.39 
g.  On  the  basis  of  the  estimates  derived 
from  the  formula  provided  by  Bloch  et  al. 
(1998),  B.  tenuis  is  the  smallest  known 
Cretaceous  eutherian,  but  it  still  falls  with- 
in the  second  class  of  body  masses  of  mod- 
ern lipotyphlans.  Batodon  tenuis  was  not 
as  minute  as  the  Eocene  Batodontoides 
vanhouteni  or  the  modern  Suncus  etrus- 


cus. 


A  variety  of  taphonomic  and  collecting 
biases  limit  the  chances  of  recovery  of  the 
remains  of  very  small  maiumals,  and  the 
available  sample  of  Cretaceous  eutherians 
is  small  in  absolute  number  of  specimens 
and  biogeographically  patchy.  The  possi- 
bility that  even  smaller  Cretaceous  euthe- 
rians will  be  discovered  cannot  be  exclud- 
ed. However,  it  is  of  interest  that  the 
smallest  currently  known  Cretaceous  eu- 
therians have  estimated  body  inasses  in 
the  range  of  3-20  g.  This  is  the  range  of 


body  masses  that  includes  61%  of  modem 
lipotyphlans  (Bloch  et  al.,  1998)  and  small 
luembers  of  other,  more  distantly  related 
eutherian  orders. 

Systematic  Affinities 

Currently,  a  lively  debate  is  swirling 
around  the  questions  of  the  time  of  origin 
of  crown-group  Mammalia  in  general  and 
eutherian  orders  in  particular  (see  Gib- 
bons [1998]).  Several  molecular  phyloge- 
neticists  (for  example  see  Springer  [1997] 
and  Kumar  and  Hedges  [1998])  have  re- 
ported data  from  molecular  clock  esti- 
mates, suggesting  that  modern  eutherian 
clades  may  have  begun  to  diverge  as  long 
ago  as  the  Early  Cretaceous,  despite  the 
lengthy  gap  in  the  fossil  record  that  such 
dates  would  imply  (but  see  Nessov  et  al., 
1998).  Studies  by  Foote  et  al.  (1999)  and 
Alroy  (1999)  are  examples  of  quantitative 
arguments  from  the  fossil  record  that  cast 
doubt  on  the  molecular  data.  Novacek 
(1999)  has  addressed  this  question  from  a 
phylogenetic  slant.  These  authors  argue 
that  the  major  ordinal  level  clades  of  the 
crown-group  Placentalia  did  not  differen- 
tiate until  after  the  extinction  of  the  non- 
avian  dinosaurs  inarking  the  end  of  the 
Cretaceous. 


Functional  Molar  Association  in  Batodon  •  Wood  and  Clemens        115 


Debate  over  the  times  of  origin  of  the  spheres  demonstrate  that  the  tribosphenic 
major  clades  of  eutherians  is  part  of  an  ex-  dentition  was  but  one  outcome  in  early  ex- 
tensive revision  of  our  understanding  of  periments  in  the  evolution  of  more  com- 
the  pattern  of  the  early  evolution  of  the  plex  triangularly  symmetrical  teeth  (see 
Mammalia.  For  example,  eutherians  and  Kielan-Jaworowska  et  al.  [1998]  and  Bon- 
marsupials  were  long  thought  to  be  char-  aparte  [1996]). 

acterized  by  the  synapomorphy  of  a  tri-  Against  this  background  of  rapidly  ex- 

bosphenic  dentition.  Discoveries  of  many  panding  knowledge  of  the  complexities  of 

mammals  with  tribosphenic  dentitions,  early  mammalian  evolution,  interpreta- 

which  cannot  be  confidently  referred  to  tions  of  the  phylogenetic  affinities  of  B. 

the  crown-groups  Placentalia  and  Marsu-  tenuis  play  a  role  in  discussions  of  the  be- 

pialia,    such    as   Montanalestes    (Cifelli,  ginning  of  the  radiation  of  the  eutherian 

1999),  show  that  this  type  of  dentition  is  a  crown  group.  Is  Batodon  a  member  of  a 

sviiapomoiphy  of  a  more  inclusive  group,  lineage  within  the  crown-group  Placenta- 

A  recently  discovered  Middle  Jurassic  lia,  thus  favoring  the  hypothesis  that  the 

mammal   from    Madagascar,  Ambondro  radiation  of  modern  eutherian  orders  be- 

(Flynn  et  al.,  1999),  suggests  a  more  an-  gan  in  the  Late  Cretaceous,  or  is  it  a  mem- 

cient  origin  of  the  tribosphenic  dentition  ber  of  a  lineage  not  involved  in  their  an- 

than  previously  expected.  cestry?  Lillegraven  (1969)  and  several  later 

Other  recent  discoveries  reveal  greater  workers  referred  Batodon  to  the  Palaeo- 

complexity  in  the  evolutionary  radiation  of  ryctidae,  which  was  classified  in  the  order 

mammals  with  a  reversed  triangular  sym-  Proteutheria,    an   admittedly  paraphyletic 

metry  of  their  cheek  teeth,  the  holotheri-  taxon  with  unclear  phylogenetic  affinities 

ans,  during  the  Jurassic  and  Cretaceous.  A  (see  Butler,   1972b).  Others  opted  for  an 

newly  discovered  Early  Cretaceous  Austra-  even  less  specific  reference  of  the  Palaeo- 

lian  mammal,  Ausktribosphenos,  exliibits  a  ryctidae  placing  it  in  the  order  Insectivora, 

surprising  combination  of  dental  and  man-  incertae  sedis  (Clemens,  1973)  or  the  in- 

dibular  characteristics.  Rich  et  al.   (1997,  fraclass    Eutheria,    incertae    sedis    (Archi- 

1999)  maintain  that  the  dentition  of  Aws/c-  bald,    1982;   Lofgren,    1995).    In  contrast, 

tribosphenos  is  not  only  fully  tribosphenic  Novacek    (1976)    and    Lillegraven    et    al. 

but  also  exhibits  eutherian  characteristics  (1981)  suggested  that  Batodon  is  an  early 

closer   to    those    of  the    Erinaceomorpha  lipotyphlan,  probably  allied  to  or  even  an- 

than   any  other  group.   This  dental   mor-  cestral  to  the  Geolabididae.  Fox  (1984:  19) 

phology  is  combined  with  very  plesiom-  doubted  these  suggestions  of  lipotyphlan 

Orphic   mandibular   structures    such   as    a  affinity.   McKenna  and  Bell  (1997)  classi- 

Meckelian   groove   and  postdentaiy  bone  fied  Batodon  and  Batodontoides  as  mem- 

sulci  or  facets  (Rich  et  al.,   1999).  Alter-  bers  of  Geolabididae,  within  Lipotyphla. 
native  interpretations  suggest  that  Ausktri-  Bloch  et  al.  (1998)  reviewed  the  system- 

bosphenos  is  a  representative  of  an  endem-  atic  assignments  of  Batodon  and  Batodon- 

ic  Australian  radiation  of  holotherians  toides.  They  reported  a  necessarily  limited, 

(Kielan-Jaworowska  et  al.,   1998;   Rich  et  computer-assisted  cladistic  analysis  of  den- 

al,  1998).  An  even  older,  isolated  tribos-  tal  characters  that  indicated  that  Batodon 

pheniclike  upper  molar  has  been  reported  is  a  basal  member  of  a  monophyletic  Geo- 

from    Late   Jurassic   deposits    in    China  labididae,   with    Ciniolestes,    Palaeoryctes, 

(Wang  et  al.,  1998).  The  authors  maintain  and  Asioryctes  as  successive  outgroups.  Al- 

that  it  is  probably  the  missing  upper  molar  though  a  helpful  beginning,  this  outcome 

of  the  pseudotribosphenic  genus  Shuoth-  may  be  variable  depending  on  which  and 

erium  (Chow  and  Rich,  1982).  These  and  how  many  characters  are  selected,  and  by 

other  holotherians  recently  discovered  in  inclusion  of  other  taxa  such  as  other  mem- 

both    the    northern    and    southern    hemi-  bers  of  Palaeoryctidae  and/or  perhaps  a  se- 


116        Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


ries  of  additional  taxa  between  Palaeoryc- 
tes  and  Asioryctes.  Differences  between 
Botodon  and  Batodontoides  tliat  would 
bear  reexamination  in  the  more  extended 
study  would  be  M3  morphology,  M3  size 
relative  to  Mj  ,,  talonid  cusps  in  all  three 
lower  molars,  and  presence  or  absence  of 
upper  molar  conules. 

MacPhee  and  Novacek  (1993)  summa- 
rized the  issues  concerning  relationships 
between  proteutherians,  palaeoryctids, 
and  lipotyphlans.  An  important  part  of  the 
problem,  perhaps  presently  insurmount- 
able, is  the  lack  of  comparative  cranial  ma- 
terial for  most  of  the  earlier  taxa.  Known 
material,  such  as  that  for  Asioryctes  (Kie- 
lan-Jaworowska,  1981),  is  mostly  devoid  of 
apomorphic  characters  needed  for  such  an 
analysis.  Palaeoryctids  (see  Thewissen  and 
Gingerich  [1989])  and  leptictids  (see  No- 
vacek [1986]),  skulls  of  which  are  known, 
have  a  few  characters  that  can  be  parsi- 
moniously inteipreted  as  synapomoiphies 
of  the  Lipotyphla.  Given  the  limited 
amount  of  information  on  its  dentition  and 
the  lack  of  cranial  data,  we  conclude  that 
currently  B.  tenuis  is  best  classified  as 
Placentalia,  incertae  sedis. 

ACKNOWLEDGMENTS 

This  work  would  not  have  occurred 
without  the  encouragement  and  support  of 
Professor  A.  W.  Crompton.  We  sincerely 
thank  Mr.  Al  Coleman,  who  took  the  ster- 
eophotograph  reproduced  in  Figure  1,  and 
L.  Laszlo  Meszoly  for  the  drawings  (Fig- 
ures 2-8,  based  on  sketches  made  by 
C.B.W.  through  a  camera  lucida  attached 
to  a  Wild-Heerbrug  M3  stereo  micro- 
scope) that  also  illustrate  this  paper. 
Thanks  are  also  due  to  Dr.  John  Storer  for 
facilitating  reillustration  of  P  2004.565.  Fi- 
nancial support  for  this  study  came,  in 
part,  from  the  University  of  Galifornia  Mu- 
seum of  Paleontology  and  a  series  of  grants 
(most  recently  EAR  9505841)  from  the 
National  Science  Foundation.  Providence 
College  provided  additional  support  by 
means  of  sabbatical  leave  and  grants  from 
its  Committee  to  Aid  Faculty  Research. 


Finally,  thanks  go  to  P.  David  Polly,  Ri- 
chard Cifelli,  an  anonymous  reviewer,  and 
several  other  colleagues  who  provided 
data,  helpful  discussions  of  aspects  of  the 
study,  or  reviews  of  drafts  of  the  manu- 
script. 

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THE  EVOLUTION  OF  MAMMALIAN  DEVELOPMENT 


KATHLEEN  K.  SMITH^ 


Abstract.  The  developmental  and  reproductive 
strategies  of  marsupial  mammals  differ  from  those  of 
placental  mammals.  In  marsupials,  most  maternal  nu- 
tritional support  of  the  developing  young  is  through 
lactation.  The  young  are  bom  at  an  extremely  altricial 
state  and  undergo  luost  development  while  attached 
to  the  teat.  In  order  to  achieve  functional  indepen- 
dence at  an  altricial  state,  the  marsupial  embryo 
accelerates  the  development  of  certain  bones  of  the 
facial  region,  most  cranial  musculature,  and  a  few  ad- 
ditional stmctures.  At  the  same  time,  relative  to  pla- 
centals,  marsupials  delay  significantly  the  develop- 
ment of  central  nervous  system  structures,  in  partic- 
'ilar  the  forebrain.  In  this  paper  I  present  preliminary 
results  concerning  the  origins  of  these  heterochronies 
in  ontogeny  and  phylogeny.  In  ontogeny,  heteroch- 
ronies are  initiated  in  marsupials  by  shifting  the  tim- 
ing of  neural  crest  differentiation  and  migration  rel- 
ative to  eutherians  and  other  amuiotes.  Further,  early 
fore-  and  midbrain  differentiation  is  delayed  relative 
:o  the  hindbrain.  Preliminary  data  from  nonmam- 
nalian  amniotes  and  monotremes  is  discussed  to  as- 
sess phylogenetic  origins.  Comparisons  with  non- 
iiammalian  amniotes  suggest  that  the  pattern  ob- 
iei"ved  in  marsupials  is  derived,  and  that  observed  in 
olacentals  is  primitive.  Preliminary  data  on  mono- 
remes  suggest  that  the  monotreme  condition  is 
iomewhat  intermediate  beKveen  the  two  therian  taxa. 
Finally,  the  implications  of  these  results  for  contro- 
.  ersies  regarding  the  evolution  of  mammalian  repro- 
luction  are  discussed. 

NTRODUCTION 

Mammalian  reproduction  is  character- 
zed  by  distinctive  adaptations  for  maternal 
lutrient  provision  to  the  young.  In  therian 
mammals  this  provisioning  occurs  via  two 
routes.  First,  during  a  period  of  intrauter- 
ne  embryonic  development  exchange  of 
lutrient  material  between  the  mother  and 
s  oung  occurs  through  a  placenta.  Although 
:his    adaptation    is    most   often    identified 


'  Department  of  Biology,   Duke   University,   Dur- 
ham, North  Carolina  27710. 


with  mainmals,  intrauterine  development 
and  the  existence  of  a  placenta  is  not  un- 
common among  vertebrates  (e.g.,  squa- 
mate  reptiles;  Shine,  1985).  Second,  and 
virtually  unique  to  mammals,  nutrition  is 
provided  postnatally  to  the  young  through 
specialized  mammary  glands.  The  origin 
and  evolution  of  these  distinctive  traits  has 
been  a  topic  of  much  discussion.  This  dis- 
cussion has  been  enriched  in  part  because 
the  two  clades  of  living  therian  inam- 
mals — inarsupials  and  placentals — possess 
quite  different  strategies  of  reproduction, 
with  differential  emphasis  on  these  two 
processes  of  maternal  investment.  (The 
terms  marsupial-placental  and  metatheri- 
an— eutherian  are  each  to  some  degree  un- 
satisfactory to  distinguish  the  two  clades; 
however,  they  are  used  informally  and  in- 
terchangeably throughout  the  text.  In  par- 
ticular, the  characters  discussed  in  this  pa- 
per are  only  accessible  in  extant  taxa,  and 
inferences  cannot  be  extended  to  mein- 
bers  of  any  clade  known  only  in  the  fossil 
record.) 

Marsupials  are  considered  lactational 
specialists,  where  a  relatively  short  intra- 
uterine period  of  maternal— fetal  inter- 
change is  followed  by  an  extended  period 
of  lactation  (e.g.,  Renfree,  1983,  1993, 
1995).  In  contrast,  eutherians  are  charac- 
terized by  relatively  longer  periods  of  in- 
trauterine development,  with  extensive  fe- 
tal—inaternal  interchange,  and  variable  re- 
liance on  lactation.  Because  the  period  of 
organogenesis  is  so  short  in  marsupials,  the 
neonates  show  minimal  development  of 
most  systems  and  are  always  highly  altri- 
cial. Eutherian  neonates  exliibit  a  range  of 
developiTient  from  altricial  to  highly  pre- 


Bull.  Mus.  Comp.  ZooL,  156(1):  119-135,  October,  2001         119 


120        Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


cocial;  however,  even  the  most  altricial  eu- 
therian  is  far  more  developed  than  the 
most  precocial  marsupial. 

Because  the  reproductive  mode  and  rel- 
ative state  of  the  neonate  in  marsupials 
and  placentals  is  so  different,  a  rich  liter- 
ature exists  that  contrasts  these  strategies 
and  speculates  on  the  evolutionary  signif- 
icance of  the  observed  patterns.  Three  ba- 
sic inteipretations  have  been  made.  In  the 
first  intei-pretation  the  marsupial  condition 
is  seen  as  a  primitive  condition,  in  which 
significant  constraints  prevent  long  periods 
of  intrauterine  development  (e.g.,  Lille- 
graven,  1975;  Lillegraven  et  al.,  1987).  Hy- 
pothesized constraints  have  included  an 
inability  to  develop  an  efficient  maternal- 
fetal  exchange  system,  physical  constraints 
on  embryo  size  due  to  the  configuration  of 
the  reproductive  tract,  or  an  inability  to 
develop  immunologic  protection  of  the  fe- 
tus. At  times  explicitly,  but  always  implic- 
itly, the  marsupial  condition  is  seen  as  a 
primitive  and  less  efficient  mode  of  repro- 
duction, as  evidenced  by  the  competitive 
difficulties  marsupials  face  in  the  presence 
of  eutherians. 

A  second  view  is  that  the  marsupial 
mode  has  evolved  in  response  to  a  number 
of  specific  selective  pressures,  with  partic- 
ular adaptive  advantages  (e.g.,  Hayssen  et 
al.,  1985;  Kirsch,  1977a,b;  Parker,  1977).  It 
is  argued  that  because  little  initial  mater- 
nal investinent  occurs  during  intrauterine 
development,  the  female  can  reduce  or 
abandon  her  litter  in  response  to  harsh  or 
uncertain  conditions  with  ininimal  loss  of 
lifetime  reproductive  effort.  This  view 
clearly  assumes  that  the  marsupial  condi- 
tion is  derived,  and  that  if  a  competitive 
inferiority  exists,  it  is  due  to  other  factors, 
such  as  the  consequences  of  marsupials 
having  evolved  in  greater  isolation  than 
have  eutherians. 

A  third  view  is  that  marsupial  and  eu- 
therian  modes  of  reproduction  are  simply 
part  of  a  single  continuum  (Tyndale-Biscoe 
and  Renfree,  1987).  Marsupials  and  pla- 
centals each  provide  nutrition  to  the  de- 
veloping young  through  both  placental  and 


lactational  exchange.  The  hypothesis  has 
been  made  that  the  primitive  therian  con- 
dition was  characterized  by  an  altricial  ne- 
onate as  a  consequence  of  small  body  size 
in  the  earliest  therian.  During  evolution, 
marsupials  and  placentals  simply  empha- 
sized different  ends  of  the  maternal  in- 
vestment continuum.  Eutherians  took  the 
strategy  of  greater  and  greater  maternal  in- 
vestment through  placentation,  and  be- 
cause of  longer  periods  of  intrauterine  de- 
velopment, neonates  are  less  altricial. 
Highly  precocial  young  are  thought  to  be 
correlated  with  the  evolution  of  large  body 
size.  In  contrast,  marsupials  have  relied  on 
the  strategy  of  more  investment  via  lacta- 
tion and  have  reduced  the  period  of  intra- 
uterine development,  resulting  in  a  more 
altricial  neonate.  The  differences  between 
the  two  are  simply  the  results  of  two  dif- 
ferent, but  not  necessarily  inferior  or  su- 
perior, strategies  of  provisioning  the 
young.  Both  marsupials  and  placentals  are 
assumed  to  have  diverged  from  a  primitive 
condition  that  was  somewhat  intermediate. 
This  debate  has  proved  difficult  to  re- 
solve, in  part  because  mammalian  repro- 
duction is  so  distinctive,  and  in  part  be- 
cause reproductive  modes  are  difficult  to 
reconstruct  in  the  fossil  organisms.  In  this 
paper  I  will  focus  on  the  evolution  of 
mammalian  development.  I  argue  that  eu- 
therian  and  marsupial  reproductive  strat- 
egies are  reflected  in  distinct  developmen- 
tal patterns;  therefore,  information  on  the 
evolution  of  development  can  provide  new 
data  for  phylogenetic  analysis  of  the  evo- 
lution of  reproduction.  I  first  review  pre- 
viously published  work  on  organogenesis 
in  marsupials  and  placental  mammals.  I 
then  introduce  new  comparative  work  that 
extends  this  previously  published  work,  to 
address  questions  about  the  origins  of 
these  differences  in  development  and  in 
evolution. 

CRANIOFACIAL  DIFFERENTIATION  IN 
MARSUPIAL  AND  PLACENTAL 
MAMMALS 

It  has  long  been  recognized  that,  rela- 
tive  to   eutherians,   marsupials   accelerate 


Evolution  of  Mammalian  Development  •  Smith 


121 


the  development  of  certain  structures  such 
as  the  tongue,  the  bones  around  the  oral 
apparatus  and  the  bones  and  muscles  of 
the  forehmb  (e.g.,  Hill  and  Hill,  1955;  Lee 
and  Cockburn,  1985;  Khma,  1987;  Maier, 
1987,  1993;  Tyndale-Biscoe  and  Renfree, 
1987,  and  references  therein;  Hughes  and 
Hall,  1988;  Nelson,  1988;  Filan,  1991; 
Clark  and  Smith,  1993;  Gemmell  and  Sel- 
wood,  1994).  This  advancement  is  inter- 
preted as  an  adaptive  response  to  the  func- 
tional requirements  placed  on  the  neonate 
by  the  marsupial  life  histoiy  The  extreme- 
ly altricial  neonate  must  independently 
travel  to,  identify,  and  enter  the  pouch  or 
teat  region,  and  recognize  and  attach  to 
the  teat.  The  neonate  must  have  sufficient 
functional  maturity  to  suckle  and  process 
food  while  it  completes  its  development. 
However,  by  and  large,  no  broad-based, 
detailed  comparisons  of  development  have 
been  made  to  identify  the  specific  heter- 
ochronies that  characterize  marsupials.  In 
a  series  of  studies  I  presented  such  an 
analysis  for  major  craniofacial  stmctures 
(Smith,  1996,  1997;  Nunn  and  Smith, 
1998). 

In  these  studies,  relatively  complete  de- 
velopmental series  of  six  placental  and  four 
inarsupial  mammals  were  examined.  The 
placentals  include  the  laboratoiy  mouse, 
Mus  musculus  (Rodentia);  the  doinestic 
cat,  Felis  domestica  (Camivora);  the  do- 
mestic pig,  Siis  scrofa  (Artiodactyla);  the 
pangolin,  Manis  javanica  (Pholidota);  the 
tarsier,  Tarshis  spectrum  (Primates);  and 
the  tree  shrew,  Tupaia  javanica  (Scanden- 
tia).  The  four  marsupials  are  the  gray 
short-tailed  opossum,  Monodelphis  domes- 
tica (Didelphidae);  the  tammar  wallaby, 
Macropiis  eiigenii  (Macropodidae);  the 
eastern  quoll,  a  species  of  marsupial  "cat," 
Dasyunis  viverrinus  (Dasyuridae);  and  a 
bandicoot,  Perameles  nasuta  (Perameli- 
dae).  Care  was  taken  to  chose  taxa  that 
represent  the  phylogenetic  breadth  of 
their  clades.  Figure  1  illustrates  the  phy- 
logenetic relations  ainong  these  taxa.  Most 
specimens  were  part  of  the  Hubrecht 
Comparative     Embryology    collection    in 


2  12  0 


2  12  2 


2022 


2  12  0 


2  2  11 


2  2  11 


2  2  11 


2  2  20 


2  2  12 


2  2  12 


Monodelphis 

Perameles 

Dasyurus 

Macropus 

Manis 

Sus 

Felis 

Mus 

Tupaia 

Tarsius 


Figure  1.  Phylogeny  of  the  taxa  used  in  the  comparative 
studies.  Phylogeny  for  marsupials  taken  from  Sanchez-Villagra 
(1 999)  and  Springer  et  al.  (1 998);  that  for  placentals  taken  from 
Novacek  (1990).  The  numbers  on  each  line  illustrate  results 
from  the  event-pair  analysis  (Smith,  1997)  and  represent  the 
character  states  for  the  following  pairs  of  events  (in  order): 
parietal-telencephalon,  dentary-telencephalon,  alisphenoid- 
exoccipital,  jugal-craniofacial  muscles.  Character  state  0 
means  the  first  element  in  the  pair  occurs  before  the  second; 
character  state  1  means  the  first  and  second  elements  appear 
at  same  time  (in  the  sample  available);  character  state  2 
means  the  first  element  in  the  pair  occurs  after  the  second. 
These  event  pairs  represent  a  variety  of  phylogenetic  patterns. 
The  pair  parietal-telencephalon  has  a  uniform  pattern  in  ther- 
ians — the  parietal  always  ossifies  after  the  telencephalon 
evaginates.  The  pair  dentary-telencephalon  separates  mar- 
supials and  placentals.  In  marsupials  the  dentary  ossifies  at 
the  same  time  or  before  the  telencephalon  appears;  in  euthe- 
rians  the  dentary  always  ossifies  after  appearance  of  the  tel- 
encephalon. The  alisphenoid  also  separates  the  two  clades 
with  the  exoccipital  preceding  the  alisphenoid  in  all  marsupials, 
and  the  alisphenoid  and  exoccipital  ossifying  at  the  same  time 
in  all  eutherians  (with  the  exception  of  Mus).  Finally,  the  pair 
jugal-craniofacial  muscles  represents  a  case  in  which  no  phy- 
logenetic pattern  of  the  developmental  relation  of  these  two 
elements  is  apparent.  See  Smith  (1997)  for  further  discussion 
of  these  events. 


The  Netherlands,  although  others  were 
obtained  from  a  number  of  sources.  For 
each  taxon  at  least  10  stages  were  available 
for  the  period  between  the  first  and  last 
developmental  events  examined.  All  spec- 
imens examined  were  serially  sectioned 
embiyos,  originally  embedded  in  paraffin 
and  stained  with  common  histologic  stains. 
Details  on  the  taxa,  sources,  and  stages  ex- 
amined can  be  found  in  Smith  (1997). 
Each  specimen  was  exainined  to  deter- 


122         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


mine  the  state  of  28  elements  of  the  cra- 
nial skeletal,  muscular,  and  central  nervous 
systems  (CNSs),  which  serve  as  landmarks 
for  the  most  critical  stages  in  the  differ- 
entiation of  craniofacial  structures.  The 
kinds  of  events  examined  are  briefly  sum- 
marized here;  further  details  are  provided 
in  Smith  (1997).  The  initial  ossification 
center  of  12  bones  of  the  dermal  and  en- 
dochondral skeletons  was  documented. 
Other  conditions  of  the  cranial  skeleton  in- 
cluded, for  example,  the  first  contact  be- 
tween the  membrane  bones  over  the  cra- 
nial roof,  the  differentiation  of  cartilage  in 
the  cranial  base,  closure  of  the  secondaiy 
palate,  and  the  development  of  a  joint  cap- 
sule at  the  dentary-squamosal  joint  (see 
Clark  and  Smith  [1993,  and  references 
therein]  for  more  detail  on  development 
of  the  cranial  skeleton). 

Three  stages,  ranging  from  the  first  fu- 
sion in  myoblasts  to  the  age  at  which  all 
craniofacial  muscles  were  distinguishable, 
were  used  as  measures  of  muscle  devel- 
opment (for  more  detail  on  the  assessment 
of  muscle  development  see  Smith  [1994]). 
Finally,  six  events  were  examined  that  in- 
dicate maturation  of  the  CNS  and  cranial 
sense  organs.  These  included,  for  example, 
the  evagination  of  the  telencephalic  vesi- 
cles, the  filling  of  the  lens  vesicle  by  pri- 
mary lens  cells,  and  the  appearance  of  at 
least  four  distinct  layers  in  the  cortex. 

Two  different  approaches  were  taken  to 
analyze  the  comparative  data  (see  Smith 
[1997]  and  Nunn  and  Smith  [1998]  for  de- 
tails on  methods).  The  first  method  con- 
structs a  matrix  for  each  taxon  in  which  the 
timing  of  each  event  is  compared  to  the 
timing  of  every  other  event.  This  creates  a 
series  of  pair- wise  comparisons,  where  the 
timing  of  event  A  is  compared  to  event  B, 
C,  D,  and  so  on  (forming  pairs  A-B,  A-C, 
A-D,  as  well  as  B-C,  B-D,  and  so  on).  The 
data  set  studied  here  included  28  events, 
which  produced  378  event  pairs.  Each  pair 
was  assigned  one  of  three  character  states, 
reflecting  the  relative  timing  of  the  two 
events.  The  three  states  were  character 
state  0,  when  event  A  (the  first  event  in 


the  pair)  occurred  before  event  B  (the  sec- 
ond event  in  the  pair);  character  state  1, 
when  A  occurred  in  the  same  stage  as  B; 
and  character  state  2,  when  A  occurred  af- 
ter B.  The  character  state  for  each  pair  of 
events  was  then  mapped  on  a  phylogeny, 
to  determine  whether  any  group  of  taxa 
(e.g.,  marsupials  or  placentals,  or  subsets 
within  a  major  clade)  had  a  unique  char- 
acter state  distribution  (Fig.  1;  see  Smith 
[1997]). 

The  second  approach  is  quantitative. 
Each  event  in  the  sequence  was  given  a 
rank  order  number  between  1  and  28  (be- 
cause there  were  28  events),  with  events 
occurring  at  the  same  time  ranked  as  a  tie. 
An  analysis  of  variance  ( ANOVA)  was  then 
performed  to  determine  which  events  had 
a  significantly  different  rank  between  mar- 
supials and  placentals.  In  addition,  meth- 
ods were  also  developed  to  correct  for 
phylogenetic  nonindependence  in  the  as- 
sessment of  significance  (see  Nunn  and 
Smith  [1998]). 

Although  the  two  analytical  methods  are 
quite  different,  they  provide  congruent  re- 
sults and  allow  a  determination  of  which 
shifts  in  relative  timing — heterochrony — 
characterize  craniofacial  organogenesis  in 
marsupial  and  placental  mammals.  In  the 
ANOVA  the  following  11  events  had  sig- 
nificantly different  ranks  in  the  two  clades: 
the  evagination  of  the  telencephalon;  con- 
tact between  the  olfactory  bulb  and  the  ol- 
factory epithelium;  layering  in  the  cortex; 
the  differentiation  of  the  thalamus  and  hy- 
pothalamus; filling  of  the  lens  vesicle  by 
primary  lens  cells;  the  initial  ossification  of 
the  dentary,  maxillary,  premaxillaiy,  and 
exoccipital  bones;  the  closure  of  the  sec- 
ondary palate;  and  the  meeting  of  the  der- 
mal bones  over  the  cranial  roof.  The  initial 
ossification  of  the  dentary,  maxillary,  pre- 
maxillary,  and  exoccipital  bones  and  the 
closure  of  the  secondary  palate  occurred 
early  in  marsupials  relative  to  placentals 
(i.e.,  they  had  a  significantly  lower  rank); 
the  other  events  were  late  in  marsupials 
when  compared  to  placentals.  This  same 
set   of  characters   exliibited  shifts   in   the 


Evolution  of  Mammalian  Development  •  Stnith 


123 


Eutherian  cranial  development 


m.  Mi 


HB 


B 


Metathehan  cranial  development 


0 


I&, 

5 

6 

B 


TIME 

Figure  2.  A  summary  of  the  relative  timing  of  development  of  craniofacial  features  in  metattierians  and  eutherians.  The  upper 
set  of  boxes  (light  stippling)  for  each  clade  represents  events  in  central  nervous  system  (CNS)  development;  the  lower  set  of 
boxes  (dark  stippling)  represents  events  in  the  development  of  skeletal-muscular  systems.  The  arrow  at  the  bottom  represents 
time.  The  letter  B  represents  the  approximate  time  of  birth  in  each  group.  For  comparison,  the  two  taxa  were  scaled  and  aligned 
relative  to  the  timing  of  the  events  of  the  skeletal-muscular  system;  the  CNS  in  each  clade  was  plotted  relative  to  the  scaled 
skeletal-muscular  system  events.  Key  to  numbers:  1,  evagination  of  telencephalon;  2,  pigment  in  retina;  3,  connection  between 
the  olfactory  epithelium  and  olfactory  bulb,  layering  present  in  the  cortex,  thalamus  and  hypothalamus  present,  primary  lens  cells 
fill  lens  vesicle;  4,  tongue  muscle  cells  begin  fusion  and  cartilage  present  in  basicranium;  5,  ossification  of  premaxillary,  maxillary, 
and  dentary  bones;  6,  closure  of  secondary  palate,  all  major  components  of  craniofacial  muscle  present,  muscle  maturation, 
differentiation  of  tooth  buds,  appearance  of  ear  ossicles,  first  ossification  in  most  membrane  bones;  7,  ossification  of  most 
endochondral  bones,  meeting  of  membrane  bones  over  cranial  roof,  and  differentiation  of  mandibular  joint  cartilage  and  capsule. 


event-pair  character  analysis.  In  the  event- 
pair  analysis,  58  of  the  378  event-pairs  had 
character  states  that  distinguished  marsu- 
pial and  placental  mammals.  Fifty-seven  of 
these  58  event-pairs  contained  either  one 
or  two  events  that  were  found  to  differ  in 
the  ANOVA. 

These  specific  results  reveal  that  cranio- 
facial development  in  marsupials  and  pla- 
cental is  distinguished  by  major  shifts  in 
the  relative  timing  of  the  differentiation  of 
the  somatic  structures  of  the  head  relative 
to  the  differentiation  of  the  CNS  (Fig.  2). 
These  heterochronies  have  two  major 
components.  First,  in  eutherians  the  onset 
of  morphogenesis  of  the  CNS  begins  long 
before  the  appearance  of  any  cranial  skel- 
etal or  inuscular  tissues.  In  inarsupials  cra- 
nial  skeletal   and   muscular  tissues   begin 


develop inent  early  relative  to  CNS  differ- 
entiation. Second,  in  eutherians  the  events 
of  CNS  development  examined  are  com- 
pleted before  most  somatic  stiiictures  be- 
gin differentiation,  whereas  in  marsupials 
morphogenesis  of  these  same  elements  ex- 
tends long  into  the  period  of  cranial  skel- 
etal development.  More  broadly,  relative 
to  eutherians,  marsupial  development  can 
be  characterized  by  two  steep  heteroch- 
ronies, or  shifts  in  developmental  timing: 
cranial  musculoskeletal  tissues  are  highly 
advanced  in  onset  and  rate  of  develop inent 
relative  to  the  tissues  of  the  CNS,  and  in 
the  body  as  a  whole,  the  rostral  portion  is 
highly  advanced  relative  to  the  caudal  por- 
tion (Smith,  1996,  1997;  Nunn  and  Smith, 
1998). 

The  early  development  of  musculoskel- 


124         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


etal  tissues  is  almost  certainly  a  result  of 
the  necessity  for  the  marsupial  neonate  to 
possess  certain  functional  abilities  relative- 
ly early  in  its  normal  developmental  peri- 
od. The  fact  of  this  early  adaptation  has 
long  been  recognized.  However,  the  ad- 
aptations of  the  marsupial  neonate  do  not 
simply  involve  the  advancement  of  the 
forelimbs  and  a  few  structures  around  the 
oral  apparatus  and  birth  at  an  altricial 
state.  Instead,  the  developmental  trajec- 
tory of  all  cranial  tissues  seems  to  be  shift- 
ed. This  whole-scale  shift  is  best  inter- 
preted as  the  interaction  of  the  adaptive 
innovations  with  constraints  imposed  by 
two  developmental  processes  (Smith, 
1997). 

The  first  process  involves  CNS  devel- 
opment and  the  constraints  arising  from 
the  sensitivity  of  nervous  tissue  to  ener- 
getic fluctuations  during  differentiation. 
The  absence  of  nutrients  during  organo- 
genesis of  the  brain  can  lead  to  long-last- 
ing neural  deficiencies  (e.g.,  Dobbing, 
1972;  Winick  et  al,  1972;  Cheek,  1975; 
Dodge  et  al,  1975;  Winick,  1976,  1979; 
Shoemaker  and  Bloom,  1977;  Hetzel  and 
Smitli,  1981;  Dhopeshwarkar,  1983;  Hersch- 
kowitz,  1989).  Because  of  these  critical  re- 
quirements, Sacher  and  Staffeldt  (1974) 
proposed  that  neurogenesis  is  the  rate-lim- 
iting step  in  mammalian  development. 
The  second  set  of  processes  involves  the 
development  of  mesenchymal-derived  tis- 
sues and  the  importance  of  initial  cell  con- 
densation size  during  skeletogenesis  (Grii- 
neberg,  1963;  Atchley  and  Hall,  1991; 
Hall,  1991;  Hall  and  Miyake,  1992,  1995; 
Dunlop  and  Hall,  1995;  Miyake  et  al, 
1996,  1997).  This  work  shows  that  in  gen- 
eral, condensation  must  be  adequate  be- 
fore cartilage  will  differentiate  and  bone 
formation  will  begin.  Therefore,  it  is  likely 
that  the  processes  of  skeletogenesis  re- 
quire the  developing  embryo  to  allocate  a 
sufficient  number  of  cells,  and  presumably 
energy,  to  the  skeletal  system  at  the  veiy 
earliest  stage  of  differentiation. 

In  eutherian  mammals  the  onset  of  neu- 
rogenesis and  the  initial  period  of  growth 


of  the  CNS  begin  early,  when  little  com- 
petition exists  from  other  tissues,  and 
growth  and  differentiation  continue 
throughout  the  extended  embryonic  and 
fetal  periods  when  nutrition  is  relatively 
constant.  However,  metatherians  face  the 
competing  demands  of  the  adaptations 
that  allow  function  of  the  systems  most 
critical  to  independent  suivival  of  the  al- 
tricial neonate,  the  extremely  short  period 
from  primitive  streak  to  birth  (which  av- 
erages 6  days  for  marsupials  as  a  group  and 
is  less  than  3  days  in  dasyurids;  Tyndale- 
Biscoe  and  Renfree,  1987),  the  necessity 
for  sufficient  allocation  to  these  systems 
for  moiphogenesis,  and  the  rate-limiting 
nature  of  neurogenesis.  Marsupials  appar- 
ently avoid  the  constraints  arising  from 
these  competing  demands  by  shifting  the 
bulk  of  neural  differentiation  to  the  ex- 
tended postnatal  period  and  devoting  em- 
bryonic resources  to  tissues  that  must  be 
functional  at  birth  (see  Smith  [1997]  for 
more  discussion  of  this  hypothesis). 

THE  DEVELOPMENTAL  ORIGINS  OF 
HETEROCHRONY 

The  discussion  above  focused  on  events 
that  occur  during  organogenesis,  after  the 
basic  systems  have  appeared.  These  data 
do  not  address  when  these  heterochronies 
originate  in  development.  At  least  two 
competing  hypotheses  have  been  devel- 
oped. First,  these  shifts  possibly  represent 
patterns  of  acceleration  and  deceleration 
of  moi"phogenesis  of  cranial  structures 
once  the  major  elements  of  the  embiyo 
have  differentiated.  Therefore,  these 
changes  would  represent  relatively  minor 
terminal  shifts  in  development,  and  sug- 
gest that  there  is  significant  conservation 
of  the  basic  body  plan.  Alternatively,  it  may 
be  that  these  shifts  occur  early  in  devel- 
opment and  represent  major  changes  in 
patterning  of  the  tissues  of  the  head,  and 
indeed  the  embryo  as  a  whole.  Of  partic- 
ular interest  is  the  fact  that  the  bones  and 
connective  tissues  of  the  facial  region, 
which  are  greatly  accelerated  relative  to 
the  CNS  in  marsupials,  are  in  fact  derived 


Evolution  of  Mammalian  Development  •  Smith 


125 


Figure  3.  Photographs  of  a  10.5-day-gestation  embryo  Monodelphis  domestica  (approximately  six  somites);  (A)  is  a  dorsal  view 
and  (B)  is  an  anterior-dorsal  view  of  same  specimen.  Neural  crest  migration  occurs  early  relative  to  neural  tube  differentiation 
in  marsupials.  Although  no  closure  of  the  neural  tube  has  occurred,  streams  of  neural  crest  have  migrated  into  the  first  arch 
region,  are  migrating  into  the  second  arch  region,  and  appear  to  be  about  to  migrate  into  posterior  regions.  Further,  at  this  time 
the  hindbrain  is  fairly  well  differentiated,  with  recognizable  rhombomeres,  yet  little  or  no  development  of  midbrain  or  forebrain 
regions  has  occurred.  This  is  quite  different  from  the  pattern  seen  in  eutherians.  Key:  C,  cervical  region;  O,  otic  sulcus  (region 
of  rhombomeres  5  and  6);  PC,  preotic  sulcus  (between  rhombomeres  2  and  3);  FB,  forebrain  region;  1 ,  the  first  stream  of  neural 
crest,  which  appears  to  populate  the  first  arch  and  frontonasal  region;  2,  the  second  stream  of  neural  crest,  which  appears  to 
provide  cells  to  the  second  arch;  3,  the  third  stream,  which  appears  to  go  to  the  third  through  sixth  branchial  arches. 


from  a  neural  tissue — the  neural  crest  (re- 
viewed in  Le  Douarin  [1982],  Noden 
[1983,  1987,  1991],  Hall  [1987],  and  Hall 
and  Horstadius  [1988]).  The  relative  tim- 
ing of  neural  crest  differentiation  serves  as 
the  earliest  "decision  point"  in  embryonic 
allocation  to  neural  or  to  mesenchymal  tis- 
sues. Do  these  differences  originate  with 
shifts  in  the  relative  timing  or  pattern  of 
neural  crest  migration?  A  positive  answer 
would  support  the  hypothesis  that  this  is  a 
fundamental  change  in  development  and 
tliat  early  development  is  potentially  plas- 
tic. 

Neural  crest  migration  has  been  studied 
extensively  in  a  number  of  nonmammalian 
vertebrates,  particularly  in  the  quail-chick 
system  (e.g.,  Le  Douarin,  1982;  Noden, 
1983,  1987,  1991;  Hall  and  Horstadius, 
1988).  The  studies  of  mammals  thus  far 
have  indicated  essential  similarity  \\dth 
other  vertebrates  although  a  few  important 
differences  exist  (see,  for  example,  Nichols 
[1981,  1986,  1987],  Serbedzija  et  al. 
[1992],  Morriss-Kay  et  al.  [1993],  Tan  and 
Morriss-Kay  [1985,  1986],  Trainor  and 
Tam  [1995],  and  Peterson  et  al.  [1996]). 
One   difference   is   that   in   the   mammals 


studied  neural  crest  migration  begins  rel- 
atively early  when  the  anterior  part  of  the 
neural  tube  is  still  open,  whereas  in  other 
vertebrates  migration  is  typically  after  neu- 
ral tube  closure  (e.g.,  Le  Douarin,  1982; 
Hall  and  Horstadius,  1988;  Hanken  et  al., 
1997).  In  both  mice  and  rats  neural  crest 
appears  to  begin  migration  at  the  five-  to 
six-somite  stage  (8  or  9  days;  Nichols, 
1981;  Morriss-Kay  et  al,  1993).  Other 
than  the  unpublished  studies  of  Hill  and 
Watson  (1958),  no  studies  of  neural  crest 
migration  have  been  conducted  in  any 
marsupial. 

Preliminary  results  from  a  study  of  neu- 
ral crest  inigration  in  inarsupials  suggest 
that  the  shift  in  the  differentiation  of  the 
CNS  and  somatic  tissues  is  initiated  by  a 
shift  in  the  relative  timing  of  neural  crest 
differentiation  relative  to  neural  tube  dif- 
ferentiation. In  a  five-  to  six-somite  em- 
bryo (approximately  10  days  gestation)  of 
M.  domestica  (Fig.  3),  significant  neural 
crest  migration  has  already  occurred;  how- 
ever, no  folding  has  taken  place  in  the  neu- 
ral plate.  In  marsupials  substantial  migra- 
tion of  neural  crest  into  the  first  arch  and 
future    frontonasal    regions   has    occurred 


126         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  4.  Whole-mount  staining  of  embryos  with  antibody  to  Distal-less  protein.  Methods  follow  Hanken  et  al.  (1992).  (A) 
Monodelphis  after  10.5  days  of  gestation  (10-12  somites);  (B)  Mus  at  10-  to  12-somite  stage;  (C)  Monodelphis  after  10  days, 
20  hours  of  gestation  (16  somites);  (D)  Mus  at  14-  to  16-somite  stage.  (A)  and  (B)  represent  early  stages  in  neural  crest 
accumulation  in  branchial  arches.  Note  that  although  the  anterior  neural  tube  is  open  in  tjoth  embryos,  the  fore-  and  midbrain 
are  much  more  robust  (both  in  thickness  of  neuroepithelium  and  length  of  region)  in  the  mouse,  but  that  much  less  accumulation 
of  neural  crest  has  occurred  in  the  frontonasal  and  first  arch  regions  in  this  animal.  In  (C)  and  (D)  the  same  pattern  continues — 
in  Monodelphis  the  neural  tube  is  still  open  anteriorly,  whereas  in  the  mouse  the  neural  tube  is  complete  and  regional  differ- 
entiation is  beginning.  However,  massive  accumulations  of  neural  crest  occur  in  the  facial  region,  particularly  in  the  maxillary 
process,  in  Monodelphis  relative  to  the  mouse.  Key:  arrows  represent  approximate  forebrain-midbrain  and  midbrain-hindbrain 
junctions;  o,  otic  vesicle;  mx,  maxillary  process;  md,  mandibular  process. 


before  any  closure  of  the  tube  occurs  at 
any  point  along  its  length.  Further,  al- 
though the  hindbrain  is  well  differentiated 
at  this  stage,  with  evidence  of  all  rhom- 
bomeres,  little  proliferation  or  differenti- 
ation occurs  in  either  the  fore-  or  midbrain 
regions.  In  eutherians  significant  prolifer- 
ation of  tissues  in  the  fore-  and  midbrain 
regions  occurs  before  neural  crest  migra- 
tion begins,  and  rhombomere  subdivision 
occurs  after  this  period.  These  preliminaiy 
studies  do  indicate  that  the  neural  crest 
arises  from  the  same  rhombomeric  seg- 
ments that  have  been  reported  in  other 
vertebrates  (e.g.,  Noden,  1991).  However, 
because  little  differentiation  of  fore-  and 
midbrain  regions  occurs  at  this  stage,  it  is 


difficult  to  assess  the  contribution  of  these 
regions  to  the  neural  crest  in  marsupials. 
Migration  of  the  neural  crest  was  fur- 
ther examined  using  an  antibody  to  Distal- 
less  proteins.  These  proteins,  produced  by 
genes  of  the  mammalian  Dlx  family,  bind 
to  a  number  of  cell  types,  including  mi- 
grating neural  crest  (Robinson  and  Ma- 
hon,  1994;  Panganiban  et  al.,  1995;  Han- 
ken et  al.,  1997).  This  antibody  is  not  an 
exclusive  marker  of  neural  crest,  but  it 
does  stain  migrating  neural  crest  and  al- 
lows comparison  of  neural  crest  migration 
in  marsupials  and  eutherians  relative  to 
other  tissues  (Fig.  4).  Apparently,  relative 
to  neural  tube  development,  significantly 
more  neural  crest  occurs  in  the  branchial 


Evolution  of  Mammalian  Development  •  Smith        127 


arch  region  in  Monodelphis  than  in  Mus. 
For  example,  in  both  the  10-  to  12-somite 
and  16-somite  stages  in  Mus  (Figs.  4B,  D) 
the  neural  tube  is  considerably  advanced 
relative  to  Monodelphis  (Figs.  4A,  C)  yet 
the  relative  size  of  the  first  and  second 
arches  is  much  smaller  in  Mus.  In  partic- 
ular, little  or  no  accumulation  of  neural 
crest  is  apparent  in  the  maxillary  region  in 
Mus.  Analysis  of  the  preliminary  data  sug- 
gests a  number  of  features  of  the  pattern 
of  neural  crest  migration  in  marsupials.  In 
marsupials  neural  crest  seems  to  migrate 
at  a  tiine  that  is  earlier,  relative  to  neural 
tube  closure,  than  in  eutherians,  or  other 
amniotes  (and  indeed,  apparently  other 
vertebrates).  In  addition,  the  neural  tube 
seems  to  differentiate  neural  crest  cells  in 
larger  populations  relative  to  allocation  to 
neural  structures  in  inarsupials.  Finally, 
differentiation  of  the  hindbrain,  the  region 
that  supplies  much  of  the  neural  crest  to 
the  branchial  arches,  seems  to  be  ad- 
vanced relative  to  the  forebrain  in  marsu- 
pials, so  that  the  major  delay  in  CNS  de- 
velopment is  concentrated  primarily  in 
forebrain  structures. 

Analysis  of  these  data  on  early  devel- 
opment suggests  that  the  differences  be- 
tween marsupials  and  placentals  in  the  rel- 
ative maturation  of  neural  and  somatic  tis- 
sues occur  during  the  early  events  in  tissue 
differentiation.  Therefore,  the  heteroch- 
ronies are  not  shifts  in  the  relative  rates  of 
growth  or  differentiation  of  terminal  struc- 
tures. These  results  are  consistent  with  the 
hypothesis  that  early  development  is  fairly 
plastic  and  may  be  modified  to  meet  spe- 
cific demands  at  a  distinctive  stage  in  de- 
velopment (see  Raff  [1996]). 

THE  PHYLOGENETIC  ORIGINS  OF 
HETEROCHRONY 

Thus  far  I  have  considered  two  clades — 
eutherians  and  metatherians.  Although  I 
have  implied  that  the  marsupial  condition 
is  derived,  I  have  not  yet  provided  the  ev- 
idence. Below,  the  patterns  observed  in 
marsupials  and  placentals  first  will  be  com- 
pared with  those  of  nonmammalian  am- 


niotes. I  will  then  discuss  preliminary  data 
on  early  development  in  monotremes. 

Early  Development  of  Amniotes 

Marsupial  development,  relative  to  that 
of  eutherians,  was  shown  above  to  be  char- 
acterized by  at  least  three  major  sets  of 
heterochronies.  First,  a  relative  delay  oc- 
curs in  differentiation  of  the  CNS  and  in 
particular  in  the  forebrain  region.  Second, 
the  differentiations  of  the  branchial  arch 
and  facial  regions  are  advanced.  These 
shifts  seem  to  be  effected  in  part  by  shift- 
ing forward  the  relative  timing  of  neural 
crest  differentiation  and  migration.  Third, 
not  discussed  in  detail  above,  is  the  exis- 
tence in  marsupials  of  an  extreme  rostral- 
caudal  gradient  of  development.  Although 
to  some  degree  a  rostral-caudal  gradient 
exists  in  eutherians,  so  that  at  a  given  stage 
the  forelimb  is  advanced  relative  to  the 
hind  limb,  this  gradient  is  extreme  in  mar- 
supials (Fig.  5).  For  example,  this  gradient 
is  reflected  by  the  relative  differentiation 
of  the  somites,  where  in  marsupials  pos- 
terior seginents  develop  relatively  late. 
However,  the  most  striking  expression  of 
this  gradient  is  the  relative  development  of 
the  fore-  and  hind  limb  buds.  In  inarsu- 
pials  the  foreliinb  bud  is  massive  at  a  time 
when  the  hind  limb  bud  is  not  yet  present. 

These  three  features  may  be  defined  as 
three  character  complexes  (each  of  which 
contains  a  multitude  of  individual  charac- 
ters) that  inay  be  examined  in  a  broader 
phylogenetic  context.  In  Figure  6  early 
embryos  of  a  chicken  (Gallus)  and  snap- 
ping turtle  {Chelijdra),  are  compared  with 
those  o{ Monodelphis  and  Mus.  Eutherians 
share  with  the  nonmammalian  amniotes 
the  advancement  of  the  neural  tube,  the 
relatively  small  branchial  arches,  and  the 
relative  similarity  of  the  rate  of  fore-  and 
hind  limb  development.  In  each,  the  mar- 
supial condition  is  quite  distinct,  and  inust 
be  intei-preted  as  derived.  Therefore,  in 
this  context,  placentals  possess  what  must 
be  taken  as  the  priinitive  amniote  condi- 
tion. 


128         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  5.  Three  stages  of  development  in  Monodelphis  do- 
mestica:  (A)  approximately  11  days  of  gestation;  (B)  approxi- 
mately 12  days  of  gestation;  (C)  approximately  13  days  of  ges- 
tation. Note  that  in  each  specimen  the  anterior  part  of  the  body 
is  greatly  advanced  relative  to  the  posterior  in  size  and  relative 
degree  of  differentiation.  In  particular,  the  forelimb  is  highly 
advanced  relative  to  the  hind  limb  at  all  stages. 


Comparisons  Across  Mammalia 

To  assess  the  condition  at  the  node 
Mammaha,  information  on  monotremes, 
the  third  major  clade  of  extant  mammals, 
is  needed.  Clear  possession  by  mono- 
tremes of  the  derived  elements  of  marsu- 


pial development  would  be  parsimoniously 
interpreted  as  a  shared  derived  resem- 
blance. On  the  other  hand,  resemblance  of 
monotremes  to  the  eutherian  condition 
(which  is  shared  with  nonmammalian  am- 
niotes)  would  further  highlight  the  derived 
and  specialized  nature  of  marsupial  devel- 
opment and  reproduction. 

Few  monotreme  embryos  are  available 
for  study.  Most  are  in  the  Hill  Collection, 
part  of  the  Hubrecht  Comparative  Embry- 
ology Laboratoiy.  Preliminary  evaluation 
of  some  of  this  material  indicates  that 
inonotremes  exliibit  a  mosaic  of  marsupi- 
allike and  placentallike  developmental 
characters.  First,  monotreines  share  with 
marsupials  and  nonmammalian  amniotes 
many  primitive  characteristics  of  the  ear- 
liest embiyo.  For  example,  all  develop  as 
a  flat  blastodisc  on  a  large  yolk,  in  a  man- 
ner that  is  quite  distinct  froin  that  of  eu- 
therians  (Hughes,  1993).  In  addition  to 
these  shared  primitive  characters  of  early 
development  in  marsupials  and  mono- 
tremes, monotremes  and  marsupials  share 
some  derived  characters.  For  example, 
early  in  development  in  monotremes  the 
branchial  arches  apparently  are  accelerat- 
ed relative  to  the  neural  tube. 

Somewhat  later  in  development,  mono- 
tremes seeiu  to  resemble  eutherians  more 
closely.  Figure  7  shows  sections  of  embry- 
onic Monodelphis  and  Mtis,  and  a  pre- 
hatching  Ornithorhynchus  (platypus)  em- 
bryo. In  order  to  define  an  equivalent 
landmark,  they  are  matched  for  the  same 
relative  stage  of  development  of  the  eye. 
In  Miis,  the  telencephalon  is  differentiated 
as  distinct  hemispheres  and  cell  prolifera- 
tion is  well  underway  in  both  the  telen- 
cephalon and  diencephalon.  However,  the 
cells  that  will  form  the  cartilages,  bones, 
and  muscles  of  the  face  show  little  or  no 
evidence  of  condensation  or  differentia- 
tion. In  contrast,  in  Monodelphis  the  tel- 
encephalon has  just  begun  evagination 
(not  shown  in  this  section)  but  little  or  no 
proliferation  of  cells  has  occurred  in  either 
the  telencephalon  or  diencephalon.  Yet,  at 
this  stage  cartilage  is  fully  differentiated 


Evolution  of  Mammalian  Development  •  Smith 


129 


Figure  6.  Embryos  of  (A)  Monodelphis;  (B)  Mus;  (C)  Gallus;  and  (D)  Chelydra.  Note  that  in  (B)  through  (D)  the  forelimb  bud 
(FL)  and  hind  limb  bud  (HL)  are  approximately  the  same  size;  in  (A)  the  forelimb  bud  is  massive,  whereas  the  hind  limb  is  not 
yet  at  the  bud  stage.  Further  note  that  in  (B)  through  (D)  the  telencephalon  (T),  as  well  as  the  other  regions  of  the  brain  are 
recognizable  as  distinct  swellings;  no  such  divisions  yet  exist  in  (A).  Finally  note  that  the  branchial  arches  and  frontonasal  region 
(N)  are  massive  in  (A),  and  relatively  small  in  the  other  taxa. 


and  present  in  the  nasal  and  basicranial  re- 
gions; bone  is  present  in  the  dentary,  pre- 
maxilla,  and  maxilla;  and  the  tongue  mus- 
culature has  differentiated  (see  Smith 
[1994,  1997]).  The  Omithorhynchus  em- 
bryo is  intermediate  between  these  con- 
ditions, although  it  is  more  similar  to  the 
eutherian  than  inetatherian  condition.  The 
major  subdivisions  are  present  in  the  neu- 
ral tube  and  proliferation  of  the  neuroep- 
ithelium  is  well  underway  in  both  the  tel- 
encephalon and  diencephalon,  yet  like  eu- 
therians  no  cartilage,  bone,  or  muscle  is 
present.  Therefore,  monotremes  do  not 
exhibit  the  same  degree  of  advancement 


of  cranial  musculoskeletal  tissues  as  mar- 
supials. 

Until  more  monotreme  material  is  ob- 
tained and  analyzed,  the  issue  of  the  con- 
dition at  the  node  Mammalia  is  obscure. 
Monotremes  apparently  share  many  prim- 
itive characters  with  marsupials,  as  well  as 
some  derived  features  of  early  develop- 
ment. However,  indication  also  exists  that 
aspects  of  the  developmental  trajectory  of 
monotremes  resemble  that  of  eutherians 
(and  nonmammalian  amniotes).  Under- 
standing the  mosaic  of  patterns  is  essential 
to  our  efforts  to  reconstruct  the  phyloge- 
netic  relations  of  mainmals  and  model  the 


130         BtiUetin  Museum  of  Comparative  Zoologij,  Vol.  156,  No.  1 


^^99  ( Ji^^^JftlA 

■'  ■  '9 

Kb^P 

t ':    1'°    "^'^SH 

^     VK,OtiMnBQ||HW 

\>j^^^^^^Ba 

iV 

origins  of  mammalian  developmental  ad- 
aptations. 

DISCUSSION 

Developmental  Plasticity  and  Conservation 

The  processes  that  distinguish  marsupial 
and  placental  maminals  begin  at  the  ear- 
liest point  in  the  differentiation  of  tissues 
of  the  craniofacial  region.  They  involve 
fundamental  shifts  in  early  patterning 
events,  and  comprise  changes  in  a  complex 
series  of  events.  These  changes  may  be 
traced  back  to  the  appearance  of  the  neu- 
ral plate,  where  at  this  stage  large  numbers 
of  cells  differentiate  into  migratory  neural 
crest  cells,  rather  than  neural  tissues. 
Within  the  neural  tube  the  hindbrain  dif- 
ferentiates early  and  the  midbrain  and 
forebrain  are  delayed.  In  addition,  a  local- 
ized acceleration  of  somitic  differentiation 
occurs  in  the  cervical  and  upper  thoracic 
regions  and  a  marked  delay  occurs  in  cau- 
dal somites.  The  distinction  is  not  a  simple 
shifting  foi"ward  in  time,  or  speeding  up 
the  rate  of  development  of  a  few  features, 
nor  is  it  due  to  the  establishment  of  a  sim- 
ple anterior— posterior  gradient  of  acceler- 
ation along  the  body  axis.  The  changes  in- 
volve multiple  advancements  and  delays  of 
sets  of  cells,  tissues,  and  organs,  within  and 
between  regions. 

Developmental  differences  between  mar- 


Figure  7.  Sections  through  the  head  of  (A)  Monodelphis;  (B) 
Ornithorhynchus;  (C)  Mus.  Specimens  were  chosen  for  ap- 
proximate match  in  the  relative  development  of  the  eye.  In 
Monodelphis  the  neural  tube  is  at  an  early  stage  with  no  sig- 
nificant proliferation  of  the  neural  epithelium  (although  the  tel- 
encephalon has  evaginated — not  visible  in  this  section).  How- 
ever, at  this  time  the  maxillary,  dentary,  and  premaxillary 
bones  have  begun  ossification;  cartilage  is  present  in  the  ba- 
sisphenoid  and  basiocclpital  regions;  and  muscle  has  differ- 
entiated in  the  tongue.  In  Mus  the  telencephalon  is  evaginated, 
and  significant  proliferation  of  neural  epithelium  has  occurred 
in  all  regions  of  the  brain,  but  no  cartilage,  bone,  or  muscle 
have  begun  differentiation.  Ornithorhynchus  resembles  Mus: 
no  bone,  muscle,  or  cartilage  are  present,  yet  the  neural  epi- 
thelium has  started  proliferation.  However,  unlike  Mus,  con- 
densations for  bones,  muscles,  and  cartilages  apparently  have 
been  initiated.  Key:  C,  connective  tissue  in  basicranium;  TEL, 
telencephalon;  arrow,  ossification  in  the  maxillary  bone;  T, 
tongue. 


Evolution  of  Mammalian  Development*  Smidi 


131 


supials  and  placentals  thus  are  not  late 
changes  or  terminal  additions  to  a  conser- 
vative mammalian  developmental  pro- 
gram. Little  evidence  exists  that  develop- 
ment in  the  two  groups  of  therians  can  be 
characterized  simply  as  two  ends  of  a  con- 
tinuuin.  The  developmental  trajectory  in 
marsupials  is  highly  modified  from  very 
early  stages  in  order  to  produce  a  specific 
adaptive  configuration  of  the  neonate.  This 
suggests  that  development,  even  at  its  ear- 
hest  stages,  is  highly  plastic. 

The  observation  of  significant  early  plas- 
ticity, even  in  animals  in  which  the  adults 
are  quite  siinilar,  is  important  for  under- 
standing the  ways  in  which  development 
and  evolution  interact.  If  it  is  common  for 
early  development  to  be  shifted  in  funda- 
mental ways,  with  little  change  in  adult 
structure,  then  the  degree  to  which  devel- 
opmental processes  impose  constraints  on 
the  generation  of  form  may  have  been 
overestimated.  These  issues,  on  relative 
consen'ation  or  plasticity  of  development, 
and  therefore  the  possible  severity  of  de- 
velopmental constraints,  can  only  be  re- 
solved by  studies  that  are  both  broad  phy- 
logenetically  and  detailed  developmentally 
(e.g.,  Richardson  et  al.,  1977;  Hall,  1984; 
Wray  and  Raff,  1991;  Hanken  et  al.,  1992, 
1997;  Swalla  et  al.,  1993;  Richardson, 
1995;  Olsson  and  Hanken,  1996;  Raff, 
1996;  Lowe  and  Wray,  1997;  Smith,  1997). 

Evolution  of  Mammalian  Development 

Comparative  patterns  of  development  in 
marsupials  and  placentals  can  be  mapped 
in  relation  to  two  outgroups.  When  mono- 
tremes  are  added  to  the  comparison,  veiy 
preliminary  observations  suggest  that  the 
primitive  condition  for  mammals  is  some- 
what intermediate,  but  probably  is  char- 
acterized by  an  altricial  neonate  and  an 
early  shift  in  the  relative  development  of 
branchial  arches  relative  to  neural  tissue. 
However,  when  mammals  are  compared 
with  nonmaminalian  amniotes,  the  inar- 
supial  condition  appears  highly  derived, 
and  the  pattern  seen  in  eutherians  closely 


resembles  the  outgroup,  or  primitive  con- 
dition. 

This  set  of  observations  implies  one  of 
three  scenarios.  First,  it  is  possible  that  the 
primitive  mammalian  developmental  con- 
dition was  monotreine-  or  marsupiallike, 
and  the  resemblance  of  placentals  to  other 
amniotes  is  an  evolutionary  reversion. 
However,  it  must  be  emphasized  that 
these  are  not  simple  shifts  in  growth  rates 
of  terminal  structures,  but  instead  changes 
in  the  early  patterning  of  multiple  systems. 
Because  of  the  complexity  of  the  charac- 
ters, this  is  not  a  parsimonious  hypothesis. 
Further,  if  this  scenario  is  true,  then  sev- 
eral vital  questions  remain  unanswered. 
Are  the  shared  characters  of  marsupials 
and  monotremes  reflective  of  the  initial 
adaptations  of  mammalian  reproduction? 
If  so,  why  did  development  change  so  rad- 
ically in  response  to  the  initial  mammalian 
reproductive  pattern?  Did  this  primitive 
reproductive  pattern  place  the  constraints 
on  embryo  resource  allocation  hypothe- 
sized above  or  are  other  factors  in  opera- 
tion? Finally,  why  did  eutherian  develop- 
ment revert  to  what  appears  to  be  a  prim- 
itive amniote  pattern? 

Second,  it  is  possible  that  marsupials 
and  monotremes  share  derived  characters 
relative  to  eutherians  +  nonmammalian 
amniotes.  This  pattern  would  provide  sup- 
port for  the  recently  revived  Marsupionta, 
a  hypothesized  monophyletic  group  con- 
sisting of  marsupial  and  monotreme  mam- 
mals (e.g.,  Gregoiy,  1947).  The  existence 
of  the  Marsupionta  has  been  supported  re- 
cently by  molecular  data  (i.e.,  Janke  et  al., 
1996,  1997;  Penny  and  Hasegawa,  1997; 
Kirsch  and  Mayer,  1998);  however,  virtu- 
ally all  morphologic  and  paleontological 
evidence  firmly  supports  the  Theria  (e.g., 
Crompton,  1980;  Rowe,  1988;  Jenkins, 
1990;  Hopson  and  Rougier,  1993;  Wible 
and  Hopson,  1993;  Zeller,  1993;  Kirsch 
and  Mayer,  1998).  Finally,  it  is  possible 
that  the  derived  conditions  that  marsupials 
and  monotremes  share  are  independently 
derived.  As  I  have  argued  above,  this  is  a 
complex    series    of  characters,    and    thus 


132        Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


such  convergence  would  involve  complex 
series  of  convergent  changes. 

The  resolution  of  the  relative  merit  of 
these  scenarios  requires  more  research  on 
development  in  a  variety  of  animals,  in 
particular  monotremes.  Focus  on  two  is- 
sues— the  degree  to  which  marsupials  and 
monotremes  share  derived  characters,  and 
the  complexity  of  the  developmental  pro- 
cesses involved — ^will  help  to  assess  the 
likelihood  of  reversion  or  convergence  in 
the  lands  of  characters  and  processes  dis- 
cussed here. 

To  conclude,  the  patterns  of  develop- 
ment described  here  allow  a  number  of 
generalizations  about  the  evolution  of 
mammalian  reproductive  strategies.  First, 
marsupials  are  not  simply  primitive  with 
regard  to  eutherians,  at  least  in  the  context 
of  amniotes  as  a  whole.  Early  develop inent 
in  marsupials  is  derived  when  compared 
with  other  amniotes.  Second,  early  devel- 
opment is  quite  distinct  in  marsupials,  so 
that  the  entire  developmental  trajectory  in 
marsupial  and  placental  mammals  differs. 
These  two  sets  of  observations  seem  to  re- 
fute the  hypothesis  that  marsupials  and 
placentals  are  merely  two  ends  of  a  con- 
tinuum. The  developmental  data  support 
the  hypotheses  that  marsupials  and  pla- 
centals have  followed  two  distinct  paths, 
each  derived  in  its  own  right.  I  hope  that 
further  detailed  information  will  provide 
infonnation  on  the  most  likely  state  at  the 
node  Mammalia  and  may  allow  the  specif- 
ic functional  correlates  of  monotreme, 
marsupial,  and  placental  developmental 
patterns  to  be  assessed.  Analysis  of  these 
data  may  help  resolve  phylogenetic  issues 
as  well  as  further  efforts  to  reconstruct  the 
evolution  of  mammalian  reproduction. 

ACKNOWLEDGMENTS 

I  thank  Drs.  J.  Hanken,  W.  M.  Kier,  and 
J.  A.  W.  Kirsch  for  comments;  G.  Pangan- 
iban  for  the  antibody  to  dll;  Alex  van  Niev- 
elt  for  comments  and  technical  support; 
the  curators  at  the  Hubrecht  Comparative 
Embryology  Collection  at  the  National 
Laboratory    of    Developmental     Biology, 


Utrecht,  the  Netherlands,  and  the  Cornell 
University  Comparative  Embryology  Col- 
lection, Ithaca,  New  York,  for  allowing  me 
access  to  specimens  in  their  care;  and  Na- 
tional Science  Foundations  grants  IBN 
9407616  and  9816985  for  support.  Finally, 
I  wish  to  express  particular  gratitude  to  Dr. 
A.  W.  Crompton  for  his  influence  on  me 
during  my  career,  and  his  numerous  con- 
tributions to  our  understanding  of  verte- 
brate, and  particularly  mammalian,  evolu- 
tion, function,  and  morphology. 

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WiNICK,  M.  1976.  Malnutrition  and  Brain  Develop- 
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.  1979.  Nutrition,  Pre-  and  Postnatal  Devel- 
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W^INICK,  M.,  P.  Rosso,  and  J.  A.  Brasel.  1972.  Mal- 
nutrition and  cellular  growth  in  the  brain:  exis- 
tence of  critical  periods,  pp.  200-206.  7;!  K.  El- 
liot and  J.  Knight  (eds.).  Lipids,  Malnutrition  and 
the  Developing  Brain:  Ciba  Foundation  Sympo- 
sium. Amsterdam:  Elsevier,  viii  +  326  pp. 

Wray,  G.  a.,  and  R.  a.  Raff.  1991.  The  evolution 
of  developmental  strategy  in  marine  inverte- 
brates. Trends  in  Ecology  and  Evolution,  6:  45- 
50. 

ZelleR,  U.  1993.  Ontogenetic  evidence  for  cranial 
homologies  in  monotremes  and  therians,  with 
special  reference  to  OrnithoHujnchns,  pp.  95- 
107.  In  F.  S.  Szalay,  M.  J.  Novacek,  and  M.  C. 
McKenna  (eds.).  Mammal  Phylogeny — Mesozoic 
Differentiation,  Multituberculates,  Monotremes, 
Early  Therians  and  Marsupials.  New  York: 
Springer,  x  +  249  pp. 


SKIN  IMPRESSIONS  OF  TRIASSIC  THEROPODS  AS  RECORDS  OF 
FOOT  MOVEMENT 


STEPHEN  M.  GATESY^ 

Abstract.  A  sample  of  20  Late  Triassic  theropod 
footprints  from  Greenland  preserves  evidence  of  ped- 
al integument.  Skin  impressions  range  from  dimples, 
valleys,  peaks,  and  ridges,  to  parallel  striations.  These 
features  were  created  by  tlie  scale-covered  digital 
pads  as  the  skin— sediment  interface  was  broken. 
Therefore,  sldn  impressions  document  aspects  of 
both  the  direction  and  timing  of  sldn  motion,  allowing 
foot  movements  during  the  stance  phase  of  locomo- 
tion to  be  inferred.  Sldn  impressions  represent  a  pre- 
viously unrecognized  source  of  functional  data  for  re- 
constructing theropod  locomotion. 

INTRODUCTION 

Dinosaur  footprints  vary  widely  in  the 
amount  of  detail  they  preserve.  The  ma- 
jority of  tracks  show  diffusely  contoured 
iinprints  of  each  digit,  although  some  are 
more  clearly  defined  by  digital  pad  and 
claw  impressions.  Very  few  preserve  the 
finest  level  of  detail — evidence  of  integu- 
mentary structures  (Lockley,  1989).  Many 
factors  are  responsible  for  the  relative  rar- 
ity of  tracks  bearing  traces  of  minute  fea- 
tures. Almost  all  of  these  factors  relate  to 
scale,  which  can  range  over  two  orders  of 
magnitude  from  the  entire  foot  to  an  in- 
dividual epidermal  tubercle.  For  example, 
larger  features  permanently  deform  sub- 
strates of  widely  differing  properties, 
whereas  smaller  features  require  much 
more  stringent  conditions  to  leave  their 
mark  (Allen,  1997;  Currie  et  al,  1991). 
Imprints  of  gross  structures  are  also  more 
likely  to  be  preserved  and  discovered  as 
undeqDrints  or  overprints  (Langston,  1986; 
Lockley,  1989).  In  contrast,  fine  details  are 


'  Department  of  Ecology  and  Evolutionary  Biology, 
Box  G,  Brown  University,  Providence,  Rhode  Island 
02912. 


only  visible  if  the  "true"  track  survives  and 
is  directly  exposed.  Finally,  large  imprints 
are  more  resistant  to  erosion  than  are 
small  ones,  both  before  burial  and  after 
exposure. 

Reports  of  skin  impressions  in  fossil  di- 
nosaur tracks  are  uncommon  in  the  ich- 
nological  literature.  Classic  works  include 
only  brief  references  to  "papillae",  "tuber- 
cles", and  "pits"  (Hitchcock,  1858;  Lull, 
1953),  and  one  illustration  (Hitchcock, 
1858,  plate  X).  "Striations",  "striae",  and 
"furrows"  are  also  described  in  passing 
(Baird,  1957;  Hitchcock,  1858;  Woodhams 
and  Hines,  1989).  The  most  thoroughly 
documented  pedal  skin  imprints  have 
been  attributed  to  ornithischians  (Currie 
et  al.,  1991).  In  this  study  I  report  on  Late 
Triassic  theropod  tracks  from  Greenland 
that  preserve  evidence  of  integumentary 
detail.  I  analyze  sldn  impressions  as  re- 
cords of  foot  movement  and  discuss  their 
contribution  to  reconstructing  theropod 
locomotion. 

MATERIALS  AND  METHODS 

In  1989,  extensive  horizons  containing 
dinosaur  tracks  were  discovered  in  the 
0rsted  Dal  Member  of  the  uppermost 
Fleming  Fjord  Fonnation  of  Jameson 
Land,  East  Greenland  (Gatesy  et  al.,  1999; 
Jenkins  et  al.,  1994).  These  cyclically  bed- 
ded siliciclastic  and  carbonate-bearing 
strata  were  deposited  in  an  extensive  rift 
lake  system  of  Norian— Rhaetic  age  (Clein- 
mensen  et  al.,  1998).  Herein,  I  report  on 
20  tracks  with  skin  impressions  that  were 
collected  froin  four  localities  (see  map  in 
Jenkins  et  al.,   1994):  eight  prints  at  Tait 


Bull.  Mus.  Comp.  Zool.,  156(1):  137-149,  October,  2001         137 


138         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Bjerg  (L  layer),  two  at  Macknight  Bjerg  (S 
layer),  one  at  Sydkronen  (SS  layer),  and 
nine  at  Wood  Bjerg  (C  layer).  These  spec- 
imens are,  with  one  exception,  isolated 
prints.  Individual  trackways  were  either 
too  poorly  exposed  or  impossible  to  iden- 
tify because  of  a  high  density  of  similarly 
sized  tracks.  Specimens  will  be  housed  at 
the  Geological  Museum  at  the  University 
of  Copenhagen;  herein,  temporary  identi- 
fication numbers  are  used. 

All  tracks  were  exposed  by  natural 
weathering;  excavation  and  mechanical 
preparation  have  proven  largely  unsuc- 
cessful. Original  material  was  collected 
and  analyzed  for  this  study,  but  silicone 
(Silastic)  or  alginate  molds  were  made  of 
one  half  of  the  tracks  and  some  were  cast 
in  plaster.  Impressions  on  tracks,  molds, 
and  casts  were  studied  using  a  Wild  M7-S 
binocular  dissecting  microscope  and  fiber- 
optic illuminators.  An  axis  drav^i  along  the 
length  of  the  iinprint  of  digit  III  was  used 
as  a  reference  to  measure  the  relative  me- 
diolateral  orientation  of  features  within  a 
track.  The  distribution  of  skin  imprints 
within  and  among  specimens  was  tabulat- 
ed by  dividing  each  track  into  22  subre- 
gions  (see  below.  Fig.  3,  and  Table  1).  Un- 
fortunately, it  is  typically  extremely  diffi- 
cult to  discern  whether  a  region  lacks  skin 
impressions  because  of  a  true  absence 
rather  than  incomplete  exposure  or  local- 
ized damage.  Therefore,  distribution  fre- 
quencies represent  raw  percentages  that 
were  not  adjusted  to  coinpensate  for  dif- 
ferential preseivation. 

All  figures  show  impressions  as  if  they 
were  made  by  right  feet;  left  footprints 
were  reversed  to  ease  coinparison  among 


tracks.  Illustrations  of  skin  impressions 
(Fig.  1)  were  made  from  camera  lucida 
drawings.  Stipple  density  was  varied  to 
represent  depth,  rather  than  shadow. 
Track  outlines  and  regions  of  skin  impres- 
sion were  traced  over  digitized  video  im- 
ages. Stereo  images  of  skin  iinpressions 
(Fig.  2)  were  created  by  image  processing 
digitized  video  images  in  Adobe  Photo- 
shop 2.5.  Three-dimensional  vectors  were 
modelled  and  rendered  in  Studio  8.5  soft- 
ware froin  Alias|Wavefront  using  data  inea- 
sured  from  striations  with  a  protractor  and 
ruler. 

RESULTS  AND  DISCUSSION 

Ichnology 

Skin  impressions  are  only  found  in  rel- 
atively shallow  tracks  (maximum  depth  4— 
21  miTi).  All  preserve  imprints  of  digital 
pads  and  claws,  but  lack  evidence  of  the 
manus  or  hallux  (Gatesy  et  al.,  1999;  Jen- 
kins et  al.,  1994).  Tracks  in  the  sample 
range  from  15  to  23  cin  in  length  (Table 
1;  estimated  in  nearly  complete  speci- 
mens), with  a  mean  of  18.8  ±  2.7  cm  (N 
=  19).  Such  prints  are  referable  to  the 
ichnogenus  Grallator  {Anchisaiiripii.s; 
Hitchcock,  1858;  Lull,  1904;  Olsen  and 
Galton,  1984),  which  has  been  attributed 
to  small  to  medium-sized  theropod  dino- 
saurs (e.g.,  Farlow  and  Lockley,  1993;  Ol- 
sen et  al,  1998). 

Identification  of  Skin  Impressions 

Tracks  with  skin  impressions  were  rec- 
ognized in  the  field  by  their  distinctive  re- 
ticulate texture  (Figs.  1,  2).  The  floor,  and 
less  frequently  the  walls,  of  digital  pad  im- 


Figure  1.  Examples  of  skin  impressions  in  Late  Triassic  theropod  prints  from  Greenland.  Reticulate  patterns  are  found  on  ttie 
floor  and  walls  of  digital  pad  impressions;  micromorphology  varies  from  hexagonally  arranged  dimples  (a,  L.04)  to  bumps,  ridges, 
and  valleys  (b,  L.OO).  Striations  are  found  on  the  borders  of  depressions.  Entry  striations  (c,  L.01)  were  formed  by  scales  plowing 
down  and  forward  in  early  stance,  whereas  exit  striations  (d,  L.OO)  were  created  as  digital  pads  were  withdrawn  in  late  stance. 
All  tracks  are  drawn  as  those  made  by  right  feet.  Shaded  areas  designate  preservation  of  skin  impressions.  Illustrations  of  skin 
impressions  show  depth,  not  shadow;  deeper  areas  are  darkly  stippled  relative  to  lighter,  elevated  areas.  Textures  in  a-d  are 
drawn  from  a  perspective  perpendicular  to  the  impressed  sediment,  rather  than  the  horizontal  bedding  plane. 


Scale  bar:  5  cm  for  track  outlines  and  2  mm  for  skin  impression  details. 


Theropod  Skin  Impressions  •  Gatesy        139 


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140         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


pressions  bear  structures  forming  densely 
packed,  loosely  hexagonal  arrays.  The  spe- 
cific microtopography  of  these  arrays  is 
variable  within  and  among  tracks.  In  some, 
concave  dimples  are  separated  by  raised 
laminae  (Figs,  la,  2a).  This  morphology 
may  represent  a  relatively  accurate  mold 
of  convex  reticulate  scales  (Lucas  and  Stet- 
tenheim,  1972)  covering  the  digital  pads. 
In  others,  arrays  are  formed  from  convex 
peaks  of  sediment.  Between  these  two  ex- 
tremes are  less  regular  patterns  of  peaks, 
ridges,  dimples,  and  troughs  (Figs,  lb,  2b). 
The  size  of  components  making  up  all  ar- 
rays is  relatively  consistent,  both  within 
and  among  tracks.  Dimples  are  approxi- 
mately 1  mm  in  diameter  and  peaks  are 
spaced  approximately  1  mm  apart.  These 
characteristic  reticulate  patterns  are  not 
found  on  sediment  outside  of  dinosaur 
tracks. 

Along  the  borders  of  digital  pad  depres- 
sions, and  more  rarely  within  them,  are  re- 
gions bearing  parallel  grooves.  Grooves  are 
spaced  0.5—1.5  mm  apart.  In  some  cases 
these  furrowed  areas  abut  reticulate  ar- 
rays, but  many  are  isolated  patches. 
Grooved  sediment  is  found  within  para- 
bolic tracts  (Figs.  Ic,  2c,  3)  posterior  to 
pad  imprints  of  digits  II  and  IV.  These  are 
likely  entry  striations  that  formed  as  the 
scale-covered  digital  pads  plowed  through 
the  sediment  before  settling  into  their 
deepest  position.  Similar  grooves  are  lo- 
cated along  the  medial  and  lateral  walls  of 
the  impression  of  digit  III  (Figs.  Id,  2d, 
3).  Such  grooves  are  interpreted  as  exit 
striations,  which  were  created  by  scales 
scraping  the  sediment  as  the  digital  pads 
of  digit  III  were  lifted  from  the  substrate. 
In  two  specimens,  claw  scrapes  and  stria- 
tions sweep  posteriorly;  these  were  formed 
when   the   foot   slipped  backward  before 


breaking  ground   contact   (Thulborn   and 
Wade,  1984,  1989). 

Distribution  of  Skin  Impressions 

Reticulate  arrays  are  found  within  all 
nine  digital  pad  depressions  (two  for  II, 
three  for  III,  and  four  for  IV),  as  well  as 
in  the  area  around  the  base  of  the  toes. 
However,  skin  impressions  are  unequally 
distributed  within  and  among  prints;  some 
regions  preserve  skin  imprints  much  more 
frequently  than  others  (Fig.  3;  Table  1). 
Arrays  produced  by  the  proximal  pad  of 
digit  II,  proximal  pad  of  digit  III,  and 
proximal-middle  pad  of  digit  IV  are  pres- 
ent in  60%,  65%,  and  70%  of  the  tracks 
sampled,  respectively.  Impressions  tend  to 
decrease  in  frequency  distally,  with  the  ex- 
ception of  the  proximal  pad  of  digit  IV. 
Overall,  reticulate  imprints  of  skin  are  rel- 
atively common  for  each  digit  (II,  50%; 
III,  38%;  IV,  51%)  as  well  as  for  the  toe 
base  area  (50%). 

Striations  are  much  less  widespread 
(Fig.  3).  Entry  striations  are  lacking  from 
digit  III,  but  present  at  low  frequencies 
(5-25%)  posterior  to  pad  imprints  of  digits 
II  and  IV.  The  impression  of  digit  III  can 
bear  exit  striations  medially,  laterally,  or 
both;  medial  grooves  produced  by  the 
withdrawal  of  the  distal  pad  are  most  com- 
mon (20%).  Evidence  of  backward  slip- 
ping is  relatively  rare. 

The  uneven  distribution  of  skin  impres- 
sions within  tracks  likely  stems  from  an  in- 
teraction among  several  influences.  Each 
portion  of  every  pad  depression  exliibits 
sldn  texture  in  at  least  one  of  the  20  tracks, 
showing  that  the  entire  plantar  surface  was 
capable  of  leaving  reticulate  arrays.  How- 
ever, the  timing  or  magnitude  of  pressure 
could  have  differentially  altered  the  sedi- 
ment's cohesiveness  and  adhesion,  affect- 


Figure  2.     Stereophotographs  of  skin  impressions  showing  variety  of  reticulate  (a,  L.04  and  b,  L.OO)  and  striated  (c,  L.01  and 
d,  L.OO)  textures.  In  all  cases  thie  lighting  is  from  the  upper  left. 

Scale  bars:  5  mm. 


Theropod  Skin  Impressions  •  Gatesy       141 


a 


I 


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'-'*"''-  •" 


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142         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Table  1.     Distribution  of  skin  impressions  in  20  theropod  footprints.  Presence  of  reticulate 

texture  (r)  and  entry  or  exit  striations  (s)  is  indicated  for  the  nine  toe  pads  and  the  toe  base. 

Entry  and  exit  tracts  not  bearing  striations  are  designated  by  t. 


Track 

l.i'ii'j;tli 
Side         (em) 

Proximal 

Di0t  II 
Distal 

Digit  III 
Proximal 

Digit  III 
Middle 

Digit  III 
Distal 

Digit  IV 
Proximal 

Digit  IV 
Proximal- 
Middle 

Digit  IV 
Distal- 
Middle 

Digit  IV 
Distal 

Toe 
Base 

L.OO 

L         21 

R 

R 

R 

S 

S 

R   t 

S 

t 

t 

R 

L.Ol 

R         23 

R 

S 

R 

t 

S 

S 

R 

t 

R 

S 

R 

R 

L.02 

R         21 

R 

R 

R 

R 

R 

R 

R 

R 

S 

R 

L.03 

R         16 

R 

R 

R 

R 

R 

R 

R 

L.04 

R        inc. 

R 

R 

R 

R 

L.05 

R         20 

R 

R 

R 

R 

R 

L.06 

L?        17 

R 

R 

R 

R 

L.07 

L         22 

R 

R 

S 

R 

R 

R 

R 

R 

S.Ol 

L         21 

R 

S 

R 

s 

R 

S 

R 

s 

R 

s 

R 

R 

S 

s 

R 

S.02 

L         18 

R 

R 

R 

R 

R 

R 

R 

SS.OO 

R         19 

R 

R 

C.I 

R         19 

S 

t 

R 

t 

R 

t 

R 

t 

t 

cm 

R         21 

S 

t 

R   t 

R 

R 

C.A 

L         18 

R 

t 

R 

t 

R 

s 

R 

s 

R 

C.B 

R         17 

t 

t 

R 

R 

t 

R 

t 

s 

t 

R 

C.Ol 

R         16 

R 

t 

t 

R 

t 

C.02 

R         16 

t 

R 

R 

C.03 

L         23 

R 

t 

R 

R 

R 

t 

t 

R 

C.04 

R         15 

R 

s 

t 

s 

t 

C.05 

R         15 

R 

t 

t 

R 

R 

R 

R 

Percent  of  sample 

60 

20 

40 

10 

65 

5 

30 

10 

20 

20 

40     5 

70 

10 

50 

25 

45 

10 

50 

m 


Figure  3.  Relative  frequency  of  sl<in  impressions  within 
prints.  Numbers  show  the  percentages  of  the  track  sample  (N 
=  20)  having  reticulate  arrays  or  striations  in  each  of  22  sub- 
regions.  Shaded  areas  posterior  to  the  impressions  of  digits  II 
and  IV  represent  entry  tracts,  many  of  which  bear  striations 
(see  Table  1).  Shaded  areas  medial  and  lateral  to  the  impres- 
sion of  digit  III  are  exit  tracts. 


ing  the  likelihood  of  skin  leaving  a  mark 
(Currie  et  al.,  1991).  Intraprint  depth  var- 
iation may  also  play  a  role.  The  distal  por- 
tions of  each  toe  often  left  the  deepest, 
narrowest  depressions.  Such  contour 
might  make  skin  imprints  from  distal  pads 
less  likely  to  be  freed  froin  overlying  ma- 
trix by  natural  erosion.  Field  identification 
and  collection  could  impose  an  additional 
bias,  because  a  reticulate  texture  was  more 
easily  recognized  than  entry  or  exit  stria- 
tions. An  analysis  of  variation  within  a  sin- 
gle trackway  could  elucidate  the  relative 
contribution  of  these  factors,  but  such  data 
are  as  yet  unavailable  from  Greenland. 

Formation  Dynamics 

With  every  step,  walking  theropods  ap- 
plied forces  against  the  ground.  On  a  re- 
ceptive substrate,  sediment  conformed  to 
the  plantar  surface  of  the  penetrating  foot. 
However,  skin  impressions  were  only  cre- 
ated as  the  integuinent  moved  off  the  sub- 
strate.  If  the  skin— sediment  interface  di- 


Theropod  Skin  Impressions  •  Gatesy        143 


Figure  4.  Simplified  depiction  of  skin  impression  formation. 
As  a  section  of  a  digital  pad  is  driven  vertically  into  thie  ground 
(a  to  b),  thie  receptive  substrate  molds  itself  to  the  reticulate 
scales,  creating  a  skin-sediment  interface  (b).  If  the  pad  is 
withdrawn  at  a  steep  angle,  a  relatively  accurate  representa- 
tion of  the  integument  is  exposed  (c).  In  contrast,  if  the  pad 
plows  through  the  sediment,  scales  on  the  skin  tangential  to 
the  direction  of  motion  will  create  striations  (d).  Therefore,  skin 
impressions  can  act  as  three-dimensional  records  of  skin 
movement. 


vided  cleanly,  each  subregion  of  the  track 
would  reflect  the  integumentary  stinicture 
it  last  apposed.  This  perspective,  empha- 
sizing the  dynamic  nature  of  skin  impres- 


sion formation,  has  both  spatial  and  tem- 
poral connotations. 

Motion  of  the  skin  relative  to  the  sedi- 
ment during  separation  strongly  influences 
sldn  impression  morphology  (Fig.  4).  This 
relationship  is  easily  visualized  by  two  ex- 
amples, both  starting  with  a  patch  of  skin 
in  contact  with  a  receptive  substrate  (Fig. 
4b).  If  the  patch  is  lifted  normal  to  the 
skin-sediment  interface,  it  will  have  a 
good  chance  of  leaving  behind  a  relatively 
accurate  mold  of  its  integumentary  surface 
(Fig.  4c).  Clear  impressions  of  a  reticulate 
scale  pattern  are  indicative  of  sldn  with- 
drawn relatively  steeply  up  and  away  from 
the  sediment.  In  contrast,  if  the  patch  is 
dragged  through  the  sediment,  its  scales 
will  leave  behind  a  series  of  parallel  stria- 
tions (Fig.  4d).  The  last  scales  to  contact 
the  substrate  will  plow  furrows  along  the 
path  of  skin  movement.  Thus,  the  dynam- 
ics of  separation  allow  skin  impressions  to 
act  as  three-dimensional  records  of  integ- 
umentary motion. 

Time  is  also  represented,  because  all 
skin  imprints  in  a  track  are  not  formed  si- 
multaneously. The  moving  toes  generate 
skin  impressions  sequentially  as  localized 
subregions  of  the  pedal  integument  vacate 
their  underlying  area  of  substrate.  For  the 
remainder  of  the  discussion,  I  focus  on  the 
breaking  of  the  sldn-sediment  interface 
and  the  formation  of  skin  impressions  in 
specific  portions  of  the  track.  Based  on 
such  evidence,  I  analyze  aspects  of  thero- 
pod foot  movement  in  three  periods  with- 
in the  stance  phase. 

Early  Stance:  Entry  Tracts  and  Entry 
Striations 

The  stance  phase  of  the  stride  cycle  be- 
gins with  ground  contact.  In  early  stance 
("touch-down"  of  Thulbom  and  Wade, 
1989),  the  area  of  skin-sediment  contact 
increased  as  the  digital  pads  penetrated 
the  substrate.  However,  Triassic  theropod 
feet  did  not  follow  a  simple  vertical  path. 
The  convex  plantar  surface  of  most  digital 
pads  entered  the  substrate  obliquely, 
forming    a    teardrop-shaped    impression. 


144         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Such  parabolic  entry  tracts,  primarily  pro-  one  pad.  Spreading  (abduction)  of  digits  II      | 

duced  by  digits  II  and  IV,  are  preserved  in  and  IV  can  be   inferred  from   one  print 

70%  of  the  prints.  In  50%  of  the  sample,  (S.Ol),  but  is  not  clearly  supported  by  an- 

entry   tracts    bear   striations    that   were  other    (L.Ol).    Again,    trackways    bearing 

formed  as  scales  plowed  through  the  sed-  multiple  prints  with  skin  impressions  could 

iment.   Specifically,  striations  are  furrows  test  these  hypotheses,  but  await  discovery 

made  by  the  last  scales  to  vacate  the  sub-  in  the  0rsted  Dal. 

strate.  Such  scales  are  located  on  those  Digit  III  must  have  followed  a  down 
portions  of  a  pad's  surface  tangential  to  the  and  foi"ward  trajectoiy  similar  to  digits  II 
direction  of  penetration  (Figs.  4d,  5b).  and  IV,  but  clear  entry  tracts  are  only  pre- 
Thus,  entry  striations  are  three-dimension-  served  in  a  single  specimen  (C.A).  One 
al  motion  vectors,  which  verify  that  the  possible  explanation  is  overprinting, 
digital  pads  moved  down  and  forward  im-  caused  by  motion  nearly  parallel  to  the 
mediately  after  ground  contact.  lo'^g  ^^s  of  digit  III  in  early  stance.  The 
An  oblique  penetration  is  expected  if  distal  pad  of  digit  III  may  have  produced 
theropods  walked  using  the  same  general  an  entry  tract  that  was  quickly  obliterated 
mechanism  employed  by  living  tetrapods  by  the  advancing  middle  pad,  which  in 
(e.g.,  Alexander  1977).  A  stance  limb  ini-  turn  had  its  entry  tract  erased  by  the  prox- 
tially  pushes  both  down  and  forward  imal  pad.  A  similar  mechanism  could  ex- 
against  the  substrate,  causing  the  animal  to  plain  the  variation  in  entry  tracts  and  stri- 
decelerate.  Under  such  a  loading  regime,  ations  made  by  digits  II  and  IV.  Motion  of 
the  direction  and  distance  a  theropods  the  foot  parallel  to  the  long  axis  of  digit  III 
digital  pads  move  after  contact  depend  on  would  minimize  overprinting  in  the  diver- 
substrate  consistency.  Entry  striations  re-  gent  side  digits.  For  example,  two  speci- 
veal  that  feet  penetrated  at  relatively  shal-  mens  with  entry  striation  angles  of  —  1° 
low  slopes  (Fig.  6).  Of  the  12  specimens  (C.B)  and  —2°  (C.I)  preserve  entry  tracts 
measured,  the  average  slope  was  only  16°.  from  all  six  pads  of  digit  II  and  IV.  In  con- 
Digital  pad  movements  also  vary  in  their  trast,  a  more  oblique  trajectory  would  tend 
mediolateral  direction  with  respect  to  the  to  obliterate  all  but  the  most  proximal  en- 
long  axis  of  the  footprint.  Striation  orien-  try  tract  of  a  digit  oriented  parallel  to  foot 
tations  vary  from  —39°  (intorted)  to  +15°  movement.  A  specimen  (C.A)  showing  en- 
(extorted)  with  respect  to  the  long  axis  of  try  striations  made  by  distal  pads  of  digit 
digit  III.  Entry  striations  produced  by  the  IV  angled  medially  shows  entry  tracts  from 
proximal  pad  of  digit  II  are  intorted  (mean  the  middle  and  distal  pads  of  digit  III,  but 
—  19°)  in  all  four  specimens  showing  this  very  little  signs  of  entry  from  digit  II.  In 
detail  (Fig.  6).  If  the  impression  of  digit  this  case,  the  foot  was  likely  laterally  ro- 
III  lies  parallel  to  the  theropods  direction  tated  (toed-out)  at  impact,  possibly  during 
of  travel,  digit  lis  proximal  pad  would  a  sharp  turn, 
have  moved  forward  and  laterally  in  early 

stance.  Alternatively,  if  the  entire  foot  was  ^id  Stance:  Pad  Deformation 
medially  rotated  (toed-in)  at  the  time  of         As  the  limb  force  increased  and  became 

contact    (e.g.,    Padian    and    Olsen,    1989;  more  vertically  oriented,  each  digital  pad 

Thulborn  and  Wade,  1989),  the  proximal  ceased   moving   foiAvard.    Loading  would 

pad  of  digit  II  may  have  slid  primarily  for-  have  caused  a  theropods  pads  to  deform 

wards.  The  sequence  of  pad  touchdown  and  settle  into  their  mid  stance  ("weight- 

and  relative  movement  among  pads  could  bearing"  of  Thulborn  and  Wade,  1989)  po- 

potentially  be  recorded  in  prints  with  a  sitions  (Figs.  5a— c).  Although  the  amount 

complete  complement  of  entiy  striations.  of  deformation  that  took  place  is  difficult 

Unfortunately,  only  tliree  prints  have  striae  to  quantify,  the  presence  of  at  least  some 

documenting  the  entry  path  of  more  than  vertical  compression  and  horizontal  expan- 


Theropod  Skin  Impressions  •  Gatesy        145 


a 


Figure  5.  Effects  of  pad  deformation  and  recoil  on  sl<in  im- 
pressions. A  digital  pad  entering  the  substrate  obliquely  in  ear- 
ly stance  (a  to  b)  creates  an  entry  tract  witfi  entry  striations  (*). 
In  mid  stance  the  limb  drives  the  pad  down  vertically  (b  to  c), 
flattening  the  pad  and  obliterating  the  entry  tract  as  new  skin 
is  forced  against  the  substrate  (small  arrows).  In  late  stance 
the  load  is  reduced,  allowing  the  viscoelastic  pad  to  return  to 
its  unflattened  shape  before  liftoff  (d).  Peripheral  skin  is  peeled 
off  at  a  relatively  steep  angle  (small  arrows),  leaving  reticulate 
arrays.  In  most  cases  the  pad  can  exit  its  depression  without 
contacting  the  walls.  Pad  deformation  has  been  exaggerated 
for  clarity. 


sion  can  be  inferred.  The  viscoelastic  paw 
pads  of  living  mammals  have  been  found 
to  reduce  impact  forces  (Alexander  et  al., 
1986);  avian  digital  pads  also  deform  in 
early  stance  (Gatesy,  personal  observa- 
tion). 

In  Triassic  theropods,  the  profile  of  dig- 
ital pad  depressions  in  Greenlandic  tracks 
is  direct  evidence  of  pad  flattening.  Some 
prints  have  almost  horizontal  floors,  de- 
spite having  entry  tracts  with  a  fluted,  U- 
shaped  profile.  Such  impressions  are  best 


explained  by  pad  deformation,  rather  than 
toes  with  a  flat  plantar  surface  (Lockley 
and  Hunt,  1994:  38).  As  a  pad  compressed, 
new  skin  around  the  periphery  would  con- 
tact the  substrate.  This  increase  in  depres- 
sion diameter  could  partially  or  even  com- 
pletely obliterate  entry  tracts  and  striations 
made  earlier  in  stance  (Figs.  5b,  c).  In 
tracks  retaining  such  traces  of  entry,  the 
pads  must  have  plowed  forward  far 
enough  to  escape  mid-stance  overprinting. 
Thus,  pad  deformation  may  explain  the 
relative  size  of  entry  tracts  from  digits  II 
and  IV  and  their  absence  in  some  prints. 
Movements  of  the  proximal  pad  of  digit 
III,  for  which  an  entry  tract  has  never 
been  found,  are  difficult  to  infer.  One  pos- 
sibility is  that  this  pad  made  an  entry  tract 
that  it  subsequently  oveiprinted  during 
mid-stance  deformation.  Alternatively,  the 
proximal  pad  of  digit  III  may  not  have 
contacted  the  substrate  in  early  stance. 
The  pad  could  have  descended  and  de- 
formed only  after  forward  motion  of  the 
foot  was  complete.  The  toe  base  region, 
which  also  never  shows  signs  of  oblique 
entry,  likely  delayed  contact  as  well.  Thus, 
mid  stance  was  a  period  during  which  skin 
contact  was  maximized,  leading  to  the  de- 
stioiction  of  earlier  sldn  impressions  rather 
than  the  creation  of  new  ones. 

Late  Stance:  Reticulate  Arrays,  Exit 
Striations,  and  Backward  Scrapes 

During  the  second  half  of  stance,  the 
limb's  force  against  the  ground  decreased 
and  was  directed  down  and  backwards.  In 
late  stance  ("Idck-off  of  Thulbom  and 
Wade,  1989),  the  foot  was  withdrawn, 
thereby  breaking  sldn— sediment  interfaces 
and  creating  all  skin  impressions  other 
than  entry  striations.  Three  main  types  of 
imprints  were  left  behind:  reticulate  ar- 
rays, exit  striations,  and  backward  slips. 

Reticulate  arrays  were  exposed  on  the 
walls  and  floors  of  the  digital  pad  depres- 
sions. In  the  formation  of  most  tracks  in 
the  sample,  regions  of  skin  moved  up  and 
away  from  the  indented  sediment  at  an  an- 
gle   steep    enough    to    prevent    striations. 


146         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


' 


Figure  6.  Summary  stereo  renderings  of  the  tliree-dimensional  orientation  of  entry  and  exit  striations  for  17  pads  from  nine 
different  specimens.  Vectors  represent  the  direction  of  the  striations  only,  not  their  length,  and  have  been  placed  around  a 
diagrammatic  track  outline  adjacent  to  their  appropriate  pads.  Entry  striations  are  roughly  parallel  with  the  long  axis  of  the  track 
and  slope  downwards  at  a  low  angle,  indicating  that  the  pads  of  digits  II  and  IV  mostly  slid  forward  after  contact.  In  contrast, 
exit  striations  created  by  the  middle  and  distal  pads  of  digit  III  have  a  very  small  forward  component;  most  motion  was  upward 
upon  toe  withdrawal. 


This  scenario  is  reasonable  for  the  central 
regions  of  the  floor  of  each  pad  impres- 
sion, but  what  about  the  peripheral  areas 
and  walls?  Could  skin  have  moved  normal 
to  all  surfaces  simultaneously?  One  possi- 
ble explanation  is  pad  recoil.  If  a  pad  was 
deformed  in  mid  stance,  a  decreased  load 


would  allow  pad  soft  tissues  to  rebound, 
thereby  vacating  the  walls  and  outer  por- 
tions of  its  depressions  floor  first  (Fig.  5d). 
Skin  abutting  the  center  of  the  floor  of  the 
pad  depression  would  rise  slightly  later. 
Such  a  mechanism  could  explain  the  ab- 
sence of  exit  striations  for  most  pads.  Re- 


Theropod  Skin  Impressions  •  Gatesy        147 


coil  would  reduce  a  pad's  transverse  di-  bom,   1982),  or  interpreted  trackways  as 

ameter  enough  to  allow  a  clean  withdrawal  evidence   of  limb   posture    (e.g.,    Lockley 

\\dthout  wall  contact.  and  Hunt,  1995;  Padian  and  Olsen,  1989). 

Not  all  pads  avoided  scraping  the  walls  A   wealth    of  locomotor   information   has 

of  their  depression  upon  withdrawal.   In  been   gleaned   from   the  two-dimensional 

some  relatively  deep  tracks,  pads  of  digit  position  of  prints  with  respect  to  one  an- 

III    intersected    with    sediment,    creating  other  (stride  length,  step  angle,  trackway 

striation-bearing  exit  tracts.  The  three-di-  width,  and  toed-in  versus  toed-out),  but 

mensional  orientation  of  exit  striations  is  little  emphasis  has  been  given  to  the  mor- 

based  on  a  small  sample  (Fig.  6),  but  some  phology  of  single  prints.  One  exception  is 

patterns  can  be  discerned.  The  distal  and  Thulbom   and   Wade    (1984,    1989),   who 

middle  pads  of  digit  III  left  relatively  ver-  were  able  to  explain  much  of  the  variation 

tical  striations  upon  withdrawal  at  the  very  in  their  large  sample  by  relating  specific 

end  of  stance  (Figs.  Id,  2d,  6).  When  mea-  features  of  a  track  to  events  during  the 

sured  in  the  horizontal  plane,  skin  move-  stance  phase.  Walking  dynamics  have  also 

ment  was  primarily  transverse  with  respect  been  inferred  from  subsurface  sediment 

to  the  long  axis  of  the  print.  These  trajec-  deformation    (Avanzini,    1998).    Most    re- 

tories  are  consistent  with  digit  III  being  cently,   deep  tracks  have  been   shown  to 

lifted  up  and  out  of  its  depression  rather  preserve  the  three-dimensional  foot  move- 

than  being  dragged  forward  (Fig.  6).  How-  ments    of   Late    Triassic    theropods    from 

ever,  neither  medial  nor  lateral  exit  stria-  Greenland  (Gatesy  et  al.,  1999).  One  con- 

tions  predominate;  both  are  present  in  two  cern  with  these  data  is  the  possible  effects 

specimens.    In   most   cases   the   third   toe  of  sinking  on  locomotion.  Did  theropods 

seems  to  have  been  removed  without  sig-  walk    differently    on    soft    and    firm    sub- 

nificant  transverse  deviation.  strates? 

At   least  two   prints   show  evidence   of  Data  from   skin  impressions  may  help 

backward  movement  of  toes  before  liftoff,  answer   this    question,    because    they   are 

Such   slippage   occurred  when  the  down  found    in    relatively    shallow   tracks.    Evi- 

and  backward  limb  force  overcame  friction  dence  of  pad  movement  during  locomo- 

between  sldn  and  sediment.  In  one  case  tion  on  a  firm  substrate  can  be  compared 

(L.06)  slipping  produced  an  elongate  claw  to   foot  trajectories  preserved  in  deep 

scrape  ("retro-scratches"  of  Thulborn  and  prints.   The   effects   of  sinking  on   stance 

Wade,  1989)  as  well  as  scale-induced  stri-  phase  movements,  if  any,  can  then  be  as- 

ations.  These  marks  converge  posteriorly,  sessed  in  order  to  discern  locomotor  func- 

indicating  adduction  of  digits  II-IV  upon  tion   under  a  variety  of  substrate  condi- 

flexion  of  the  metatarsophalangeal  joints  tions.  Results  from  this  analysis  of  sldn  im- 

(Baird,  1957;  Gatesy  et  al.,  1999).      "  pressions  of  20  Greenlandic  tracks  must  be 

considered  preliminaiy,  but  they  contrib- 

Previous  Work  and  Future  Directions  ^^^  to  ^  more  detailed  documentation  of 

Study  of  vertebrate  tracks  has  increased  foot  movements  in  basal  theropods.  Pedal 

dramatically  in  the  past  two  decades  (e.g.,  function   may  have  been  very  similar  to 

Farlow  and  Chapman,  1997;  Gillette  and  that  seen  in  living  ground-dwelling  birds, 

Lockley  1989;  Lockley  1991,  1997,  1998;  but   this   hypothesis   requires  testing  and 

Thulborn,   1990).  Along  with  this  revival  verification. 

has  been  a  heightened  awareness  of  the  Clearly,    much    more   work   is    needed, 

contribution  footprints  can   make  to  un-  Trackways  with  skin  impressions  would  be 

derstanding    dinosaur    locomotion.    Many  particularly  informative  about  the  effects 

workers  have   applied  Alexanders   (1976)  of  speed,  turning,  and  preservational  vari- 

method  to  calculate  speed  (e.g.,  Farlow,  ation.  A  broader  suivey  of  theropod  tracks 

1981;    Russell   and   Belland,    1976;   Thul-  with  skin  impressions  from  other  locafities 


148         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


and  ages  is  sorely  needed.  Analyses  of  fos- 
sils will  also  benefit  from  a  better  under- 
standing of  track  formation  in  living  ani- 
mals, particularly  birds.  Surprisingly,  a 
complete  description  of  avian  foot  motion 
during  terrestrial  locomotion  is  unavailable 
(for  preliminary  accounts  see  Cracraft, 
1971;  Gatesy,  1999;  Gatesy  et  al.,  1999). 
Techniques  such  as  high-speed  film  or  vid- 
eo should  allow  features  such  as  tracts  and 
striations  to  be  related  directly  to  skin  mo- 
tion. Simple  manipulations  may  elucidate 
variation  in  reticulate  patterns  and  permit 
a  more  precise  interpretation  of  reticulate 
arrays  in  fossil  tracks.  Extant  forms  also  al- 
low the  magnitude,  direction,  and  position 
of  the  limb's  force  against  the  substrate  to 
be  measured  (e.g.,  Roberts,  2001)  and  re- 
lated to  foot  movement.  Finally,  a  more 
sophisticated  analysis  of  substrate  proper- 
ties and  their  effects  on  track  formation 
dynamics  (e.g.,  Allen,  1997)  is  needed  for 
dinosaurs.  In  time,  a  combination  of  such 
approaches  may  delineate  both  general 
features  of  theropod  locomotion  as  well  as 
more  specific  details  of  its  evolutionary 
history. 

ACKNOWLEDGMENTS 

Footprints  were  collected  as  part  of  a 
joint  Harvard  University  and  University  of 
Copenhagen  expedition,  with  support 
from  the  National  Science  Foundation,  the 
Carlsberg  Foundation,  and  the  Putnam 
Expeditionary  Fund  of  Harvard  University. 
I  particularly  thank  F.  A.  Jenkins,  Jr.,  N. 
H.  Shubin,  W.  W.  Amaral,  K.  M.  Middle- 
ton,  and  other  members  of  the  field  crew 
for  their  help,  and  J.  O.  Farlow  for  com- 
ments and  advice.  Sldn  impressions  in  Fig- 
ure 1  were  drawn  by  Peggy  Price.  This  pa- 
per is  dedicated  to  my  advisor.  Fuzz 
Crompton,  who  taught  me  that  variation  is 
often  information,  not  just  noise  to  be  av- 
eraged out. 

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A  DIMINUTIVE  PTEROSAUR 
(PTEROSAURIA:  EUDIMORPHODONTIDAE) 
FROM  THE  GREENLANDIC  TRIASSIC 


PARISH  A.  JENKINS,  JR.,^  NEIL  H.  SHUBIN,^  STEPHEN  M.  GATESY,^  AND  KEVIN  PADIAN^ 


Abstract.  A  diminutive  eudimorphodontid  ptero- 
saur, from  the  Late  Triassic  Fleming  Fjord  Formation 
of  East  Greenland,  possesses  relatively  short  wings, 
short  ulnae  and  tibiae,  and  long  metatarsals.  The  new 
species,  smaller  than  any  known  individual  of  Eudi- 
morphodon,  is  unique  among  known  pterosaurs  in 
having  pro.ximal  limb  segments  (humerus,  ulna,  fe- 
mur, tilaia)  of  nearly  equal  length.  Although  the 
Greenlandic  pterosaur  is  probably  a  juvenile,  as  in- 
dicated primarily  by  the  lack  of  synostosis  of  axial  and 
limb  girdle  components,  the  appendicular  propor- 
tions of  the  specimen  are  too  different  from  those  in 
other  knowai  pterosaurian  taxa  to  be  accounted  for 
solely  by  immaturit)'.  The  bicondylar  fourth  metacar- 
pophalangeal joint,  in  which  the  dorsal  condyle  has  a 
larger  radius  of  curvature  and  a  more  extensive  artic- 
ular surface  than  the  ventral  condyle,  appears  to  be 
intermediate  between  a  primitive  unicondylar  joint 
and  the  asymmetric  trochlea  common  among  ptero- 
saurs. This  spectrum  of  joint  configurations  repre- 
sents increasing  mechanical  stability,  consonant  with 
the  interpretation  that  the  mechanism  evolved  among 
basal  pterosaurs  to  accommodate  wing  folding  during 
the  upstroke  in  flapping  flight. 

INTRODUCTION 

The  earliest  well-documented  records 
of  pterosaurs  are  from  Late  Triassic  (No- 
rian)  deposits  in  Italy.  Eiidimorphodon 
ranzii,  first  described  from  a  single,  nearly 
coinplete  skeleton  froin  the  Zorzino  lime- 
stones   (Middle    to    Upper    Norian)    near 


'  Department  of  Organismic  and  Evolutionary  Bi- 
ologv,  and  Museum  of  Comparative  Zoology,  Harvard 
Universit)',  Cambridge,  Massachusetts  02138. 

-  Department  of  Organismal  Biology  and  Anatomy, 
University  of  Chicago,  Chicago,  Illinois  60637. 

^  Department  of  Ecolog)-  and  Exolutionar)'  Biology, 
Brown  University,  Providence,  Rhode  Island  02912. 

^  Department  of  Integrative  Biology,  and  Museum 
of  Paleontology,  University  of  California,  Berkeley, 
Cahfomia  94720. 


Bergamo  (Zambelli,  1973),  is  now  known 
from  four  additional  specimens,  including 
juveniles  (Wild,  1978,  1994).  Another 
specimen,  designated  as  a  different  species 
(E.  rosenfeldi),  derives  from  the  lower  part 
of  the  Dolomia  di  Fomi  (Middle  Norian) 
in  Udine  Province  (Dalla  Vecchia,  1995). 
Other  contemporaneous  taxa  from  Berga- 
mo Province  include  Peteinosaunis  zam- 
bellii  (represented  by  two  specimens; 
Wild,  1978),  also  from  the  Zorzino  lime- 
stones, and  Preondactijlus  huffarinii 
(known  from  a  single  specimen;  Wild, 
1984;  Dalla  Vecchia,  1998)  from  the  Do- 
lomia di  Fomi.  A  compacted  assemblage 
of  pterosaur  bones,  interpreted  as  a  gastric 
pellet,  was  referred  to  P.  hujfarinii  by  Dal- 
la Vecchia  et  al.  (1989)  principally  on  the 
basis  of  estimated  limb  length  ratios.  The 
specimen  derives  from  a  fossiliferous, 
Middle  Norian  zone  in  the  Dolomia  di 
Fomi  (Roghi  et  al.,  1995),  150-200  m  low- 
er in  the  section  that  yielded  tlie  type  of 
P.  bujfarinii  (Dalla  Vecchia  et  al,  1989). 

Some  pterosaurs  of  the  Late  Triassic  al- 
ready had  attained  moderate  size.  Padian 
(1980)  described  a  partial  wing  skeleton 
from  a  pterosaur  with  a  wingspan  of  1.5  m 
that  he  recognized  was  neither  Eiidimor- 
phodon nor  Peteinosaunis.  Wild  (1984),  in 
his  description  of  the  type  of  Preondactij- 
lus bujfarinii,  referred  the  wing  skeleton 
to  this  taxon  on  the  basis  of  phalangeal 
proportions,  although  the  type  of  P.  biif- 
farinii  is  smaller,  with  a  wingspan  estimat- 
ed at  45  cm  (Wellnhofer,  1991)  or  "a  little 
less   than   50   cm"    (Dalla  Vecchia,    1998: 


Bull.  Mus.  Comp.  Zool.,  156(1):  151-170,  October,  2001         151 


152         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


358).  Adult  Eiidimorphoclon  ranzii  had  a 
wingspan  of  1  m  (Wild,  1978). 

Here  we  describe  a  tiny  pterosaur, 
which  we  interpret  as  a  young  individual 
of  a  new  species  of  Eiidirnorphodon,  with 
an  estimated  24-cm  wingspan,  from  the 
Late  Triassic  Fleming  Fjord  Formation, 
Jameson  Land,  East  Greenland  (Jenkins  et 
al,  1994). 

The  following  abbreviations  of  institu- 
tional names  are  used:  MCSNB,  Museo 
Civico  di  Scienze  Naturali,  Bergamo; 
MCZ,  Museum  of  Comparative  Zoology, 
Harvard  University,  Cambridge,  Massa- 
chusetts; MFSN,  Museo  Friulano  di  Storia 
Naturale,  Udine;  and  MGUH,  Geological 
Museum,  University  of  Copenhagen. 

SYSTEMATIC  PALEONTOLOGY 

Class  Reptilia  Laurent!,  1768 

Subclass  Archosauria  Cope,  1869 

Order  Pterosauria  Kaup,  1834 

Family  Eudimorphodontidae  Wellnhofer, 
1978 

Genus  Eudimorphodon  ZambeWi,  1973 

Eudimorphodon  cromptonellus  new 
species 

Holotype.  MGUH  VP  3393  (MCZ  field 
no.  13/91G;  Fig.  1). 

Etymology.  The  specific  epithet  coin- 
bines  a  patronym  honoring  A.  W.  Cromp- 
ton  for  his  contributions  to  our  under- 
standing of  the  evolution  of  vertebrate 
structure  and  function,  with  Latin  -elliis, 
diminutive  in  reference  to  the  small  size 
of  the  type. 

Diagnosis.  A  very  small  pterosaur  that 
shares  with  Eudimorphodon  ranzii  (as  di- 
agnosed by  Wild,  1978:  179,  and  later 
emended  by  Wild,  1994:  97-102)  a  het- 
erodont  dentition  composed  of  uni-,  tri-, 
and  quinticuspid  teeth  (vinknown  in  any 
other  pterosaurian  taxon);  additionally, 
some  teeth  are  quadricuspid.  Eudimor- 
phodon rosenfeldi  (Dalla  Vecchia,  1995) 
also  has  quinticuspid  teeth  but  the  denti- 
tion   is    incompletely   known.    The    tooth 


count  is  estimated  at  11  or  12  postpre- 
maxillary  teeth,  which  is  14  or  15  fewer 
than  the  type  of  E.  ranzii  and  three  or  four 
fewer  than  the  number  reconstructed  for 
the  Milano  juvenile  specimen  of  E.  ranzii 
(Wild,  1978,  figs.  25,  27).  The  tibia  is  rel- 
atively shorter  than  in  any  known  ptero- 
saur (104%  of  the  femur);  the  ulna  is  rel- 
atively shorter  than  in  most  other  ptero- 
saurs (111%  of  the  humerus;  some  speci- 
mens of  Canipylognathoides  zitteli  have 
coinparable  humero-ulnar  proportions,  see 
Table  2).  As  in  the  Milano  juvenile,  no  ev- 
idence is  found  of  the  two  enlarged,  fang- 
like maxillary  teeth  situated  beneath  the 
ascending  process  that  are  characteristic  of 
adult  E.  ranzii.  Differs  from  the  juvenile 
specimen  (MCSNB  8950)  referred  to  E. 
ranzii  by  Wild  (1994)  in  that  the  metatar- 
sals are  approximately  25%  longer,  where- 
as all  other  limb  bone  lengths  are  substan- 
tially shorter.  The  new  taxon  differs  from 
E.  rosenfeldi  (Dalla  Vecchia,  1995)  in  hav- 
ing a  huinerus  that  is  shorter  than  the  fe- 


mur. 


Horizon  and  Locality.  Lower  part  of  the 
Carlsberg  Fjord  beds  in  the  0rsted  Dal 
Member  of  the  Fleming  Fjord  Formation, 
Scoresby  Land  Group,  Jameson  Land,  East 
Greenland.  On  the  southern  flank  of  Mack- 
night  Bjerg  (Geodsetisk  Instituut,  Gr0nland 
series  1:250,000,  Carlsberg  Fjord  Quadran- 
gle), a  localized  bone  assemblage  was  dis- 
covered in  1989  by  William  W.  Amaral  at 
71°22.277'N,  22°33.341'W  (the  Macknight 
Bjerg  quarry;  the  latitude  and  longitude  co- 
ordinates given  here,  taken  in  1995  by  av- 
eraging multiple  global  positioning  system 
readings  to  reduce  anomalies  due  to  drift, 
differ  slightly  from  those  reported  by  Jen- 
kins et  al.  (1994)  based  on  a  single  reading 
from  a  hovering  helicopter).  Excavated  in 
1991  and  1992,  this  locality  presented  a 
rich  taphocoenosis  of  vertebrate  remains, 
predominantly  the  plagiosaurine  Gerro- 
thorax  cf.  pulcherrimus  but  also  the  capi- 
tosaur  Cyclotosaurus  cf  posthumus  (Jen- 
kins et  al.,  1994).  In  addition  to  the  ptero- 
saur, the  only  otlier  associated  skeletal  ma- 
terial of  a  terrestrial  tetrapod  found  at  this 


Triassic  Pterosaur  From  Greenland  •  Jenkins  et  al.         153 


Figure  1 .     Stereophotographs  of  Eudimorphodon  cromptonellus  (MGUH  VP  3393),  new  species,  preserved  in  two  matrix  blocks 
(A,  see  Fig.  3  for  details;  B,  see  Fig.  2). 


154         Bulletin  Museuin  of  Comparative  Zoology,  Vol.  156,  No.  1 


site  was  that  of  a  Plepidosauromoiph  rep- 
resented by  a  partial  postcranial  skeleton 
and  lower  jaws. 

Age.  Late  Triassic  (PNorian-Rhaetian) 
(Jenkins  et  al.,  1994;  Clemmensen  et  al., 
1998). 

Material.  A  fairly  complete  but  largely 
disarticulated  and  partly  crushed  skeleton. 
Identifiable  cranial  bones  include  both 
mandibles  and  maxillae,  as  well  as  a  nasal, 
lacrimal,  jugal,  quadrate,  and  squamosal. 
Other  cranial  elements  are  too  damaged  to 
offer  a  basis  for  useful  description.  Post- 
cranial  remains  include  numerous  ceivical 
and  dorsal  vertebrae  (most  neural  arches 
are  disassociated  from  centra),  several  cau- 
dal vertebrae,  and  rib  fragments.  Appen- 
dicular elements  include  the  right  scapula; 
a  partial  coracoid;  the  right  humerus,  ra- 
dius, ulna,  fourth  metacarpal,  and  wing 
phalanges;  both  femora,  a  tibia,  and  a  fib- 
ula; metatarsals;  and  numerous  pedal  pha- 
langes. 

Comments.  The  specimen  was  discov- 
ered in  the  process  of  splitting  coarsely 
bedded  matrix  in  the  Macknight  Bjerg 
quarry;  parts  of  the  skeleton  are  thus  pre- 
served on  part  and  counterpart  blocks 
(Figs.  1—3).  Postmortem  tissue  maceration 
resulted  in  disarticulation  of  most  of  the 
bones,  but  transport  was  minimal  and 
some  natural  associations  are  preserved 
(skull,  cervical  vertebrae,  right  manus, 
right  hind  limb). 

DESCRIPTION 

Skull 

Maxilla.  The  right  maxilla  (Figs.  2,  4), 
largely  complete  except  for  some  damage 
to  its  rostral  and  caudal  ends,  is  13.5  mm 
in  length.  A  posteriorly  recurved  ascending 
process  is  preseived,  which  in  Eudimor- 
phodon  ranzii  separates  the  antorbital  fe- 
nestra from  the  external  naris  (Wild,  1978, 
fig.  1).  The  maxilla  bears  11  teeth  with  an 
apparent  diastema  between  the  third  and 
fourth.  The  diastema,  which  is  situated  an- 
teroventral  to  the  ascending  process  of  the 
maxilla  approximately  in  the  locus  of  the 


enlarged  fanglike  teeth  of  adult  E.  ranzii 
(Wild,  1978,  fig.  25b),  shows  no  evidence 
of  alveoli.  The  last  seven  teeth  are  poste- 
rior to  the  ascending  process  of  the  max- 
illa. The  left  maxilla  (in  medial  aspect,  Fig. 
2),  partly  overlain  and  obscured  by  the 
right  maxilla,  is  fractured  and  deformed 
but  is  complete  posteriorly  where  it  lies  in 
contact  with  the  jugal.  Nine  teeth  are  pre- 
sent, but  most  are  incompletely  preserved; 
a  gap  (Pdiastema)  between  the  fourth  (in 
the  process  of  eruption)  and  fifth  is  suffi- 
cient to  have  accommodated  three  tooth 
positions. 

Other  Cranial  Bones.  Most  cranial 
bones  are  obscured  by  postmortem  col- 
lapse, crushing,  and  disarticulation  of  the 
skull.  However,  a  few  can  be  identified, 
but  offer  little  detail  that  warrants  further 
description  beyond  that  illustrated  (Figs. 
2,  3).  Crushed  bone  superorostral  to  the 
anterior  ends  of  the  maxillae  represents 
part  of  the  right  nasal,  and  possibly  the 
posterior  part  of  the  premaxilla.  No  evi- 
dence is  found  of  premaxillaiy  teeth.  The 
slender  right  lacrimal  lies  behind  the  as- 
cending process  of  the  maxilla.  The  jugal 
is  represented  by  a  postorbital  process. 
Both  the  right  squamosal  and  quadrate  lie 
separate  from  the  skull.  The  squamosal  has 
a  deep  notch  that  represents  the  superior 
border  of  the  inferior  temporal  fenestra. 
The  quadrate  bears  a  large,  bulbous  artic- 
ular condyle. 

Dentition.  The  teeth  are  buccolingually 
narrow  and  vary  in  mesiodistal  length  from 
0.42  to  1  mm.  The  relatively  simple,  uni- 
cuspid  mesial  teeth,  exemplified  by  the 
most  mesial  tooth  presei'ved  in  the  right 
maxilla  (Fig.  4)  and  left  mandible  (Fig.  2), 
are  the  smallest  (0.42,  0.48  mm  in  length, 
respectively);  the  mesial  crest  that  de- 
scends from  the  apical  cusp  is  slightly 
more  convex  than  the  distal  crest.  The  re- 
mainder of  the  dentition  comprises  mul- 
ticusped  teeth  sti*ucturally  similar  to  those 
oi  EtidimorpJiodon  ranzii  (Wild,  1978)  but 
unlike  that  in  any  other  known  pterosaur. 
The  enamel  is  smooth  and  without  surfi- 
cial  grooves;  Wild  (1978,  fig.  28)  regarded 


Triassic  Pterosaur  From  Greenland  'Jenkins  et  al.         155 


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Triassic  Pterosaur  From  Greenland  'Jenkins  et  al.         157 


the  textural  difference  in  enamel  among  possibly  conceals  a  second  distal  accessory 
specimens  of  E.  ranzii  as  ontogenetic  cuspule  at  the  base  of  the  crown.  The 
(adults  possess  grooves  that  run  apicobas-  fourth  tooth,  in  the  process  of  eruption, 
ally;  juveniles  lack  them).  Accessory  cus-  displays  three  cusps,  but  the  basal  mesial 
pules  are  developed  along  the  mesial  and  and  distal  cuspules,  if  present,  would  be 
distal  crests  descending  from  the  primary,  obscured.  The  fifth  tooth  has  two  acces- 
or  apical,  cusp;  comparable  to  the  vari-  sory  cuspules  mesially,  but  only  one  dis- 
ability illustrated  by  Wild  (1978,  fig.  7)  for  tally.  Of  the  six  most  distal  teeth,  all  appear 
the  Milano  juvenile  specimen  of  E.  ranzii,  to  be  quinticuspid,  except  for  the  relatively 
teeth  may  bear  a  single  accessory  cuspule  small  eighth  tooth  (mesiodistal  length, 
(along  the  distal  crest),  or  two,  three,  or  0.45  mm),  which  appears  to  be  tricuspid, 
four  cuspules.  Mesial  teeth  (ranging  in  The  11  teeth  of  the  right  maxilla  (Fig. 
mesiodistal  length  from  0.54  to  0.78  mm)  4)  are  the  best  preserved  of  the  entire  den- 
tend  to  be  tricuspid,  with  the  accessory  tition.  A  diastema  between  the  third  and 
cuspules  situated  at  the  mesial  and  distal  fourth  teeth  is  evidence  that  the  maxillary 
base  of  the  crown.  Teeth  in  the  distal  part  tooth  count  could  have  been  12  or  more, 
of  the  row  (ranging  in  mesiodistal  length  The  most  mesial  tooth  is  unicuspid  and 
from  0.83  to  1.08  mm)  tend  to  be  quinti-  relatively  small  (mesiodistal  length,  0.42 
cuspid.  Accessory  cuspules,  particularly  mm);  the  second  also  appears  to  be  uni- 
the  basal  ones,  tend  to  be  oriented  in  pal-  cuspid,  but  the  third  is  clearly  tricuspid 
mate  fashion,  splaying  from  the  central  (respective  lengths,  0.54,  0.72  mm).  The 
(apical)  axis;  in  adult  E.  ranzii,  cuspules  remaining  eight  teeth  (4th-llth)  vary  in 
either  parallel  the  central  axis  or  converge  mesiodistal  lengths  from  0.8  to  1  mm,  with 
slightly  (Wild,  1978,  fig.  8).  One  tricuspid  the  exception  of  the  most  distal  tooth  (0.6 
tooth  illustrated  by  Wild  (1978,  fig.  7)  of  a  mm).  The  fourth  and  very  probably  the 
juvenile  E.  ranzii  (the  Milano  specimen)  fifth  are  quinticuspid.  However,  the  sixth 
exliibits  a  similar  splaying  of  accessory  cus-  and  seventh  are  quadricuspid,  with  a  sin- 
pules,  gle  accessory  cuspule  on  the  distal  crest  of 

Eleven    teeth    are   present   in    the    left  the  sixth  and  mesial  crest  of  the  seventh, 

mandible  (nine  shown  in  Fig.  3;  the  two  The  9th  is  tricvispid,  the  10th  quinticuspid, 

most  distal  in  Fig.  2).  The  most  mesial,  and  the  most  distal  a  small  tricuspid.  As  in 

unicuspid  tooth  is  followed  by  a  bicuspid  the  smaller,  Milano  juvenile  specimen  of 

(with  a  minute  accessory  cuspule  on  the  Eudimorphodon   ranzii   (Wild,   1978,   figs, 

distal  crest).    Most  of  the  remaining  left  25,  27),  no  evidence  is  found  of  the  two 

mandibular  teeth,  insofar  as  preserved,  ap-  enlarged,  fanglike  maxillary  teeth  situated 

pear  to  be  tricuspid,  with  the  exception  of  beneath   the   ascending   process   that   are 

the  penultimate,  which  is  quinticuspid.  characteristic  of  adult  £.  ranzii.  Few  of  the 

The  11  teeth  of  the  right  mandible,  bet-  10  left  maxillary  teeth  preserve  any  details 
ter  preserved  than  those  of  the  left,  all  ex-  of  the  crowns;  the  fifth,  sixth,  and  seventh 
hibit  three  or  more  accessory  cuspules;  the  are  certainly  quinticuspid. 
mesial  dentition  appears  to  be  unrepre-  A  definitive  tooth  count  cannot  be  as- 
sented because  there  are  no  uni-  or  bicus-  certained  because  of  postmortem  damage; 
pid  teeth.  The  most  mesial  tooth  bears  two  neither  the  premaxillary  teeth,  nor  the 
accessory  cuspules  mesially,  and  at  least  fanglike,  mesialmost  teeth  of  the  lower  jaw 
one  distally  (the  basal  part  of  the  crown,  known  in  presumably  ontogenetically  old- 
where  a  second  distal  cuspule  would  be  ex  s^eciVLxens  o{  Eudimorphodon  ranzii  dLve 
positioned,  is  obscured  by  the  next  over-  preserved.  Nonetheless,  the  tooth  counts 
lying  tooth).  The  second  tooth  is  tricuspid,  in  both  maxillae  and  both  mandibles  are 
The  third  tooth  is  at  least  quadricuspid;  sufficiently  comparable  to  estimate  11  or 
the  obliquity  of  its  position  in  the  alveolus  12   postpremaxillary   teeth,   two   to   three 


158         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


1  mm 


Figure  4.     Lateral  view  of  the  right  maxilla  of  Eudimorphodon  cromptonellus  (MGUH  VP  3393),  new  species. 


fewer  than  the  number  reconstructed  for 
the  Milano  juvenile  (Wild,  1978,  figs.  25, 

27). 

Postcranial  Skeleton 

Vertebrae.  Approximately  six  cervical, 
eight  dorsal,  one  Psacral,  and  one  (possibly 
two)  caudal  vertebrae  are  represented. 
However,  postmortem  disturbance  consid- 
erably obscures  vertebral  details.  Although 
some  vertebrae  are  more  or  less  associated 
in  a  series,  inost  are  disarticulated  from 
one  another.  Furthermore,  in  most  cases 
the  neural  arches  and  centra  themselves 
are  disarticulated;  the  only  complete  ver- 
tebra is  an  elongate  midcaudal  (Fig.  3; 
centrum  length  5.7  min;  overall  length,  7.6 
mm).  Reconstruction  is  further  hampered 
by  the  overlap  of  bones  that  have  collapsed 
one  on  the  other.  Of  the  eight  isolated  cen- 
tra that  appear  undistorted  and  are  suffi- 
ciently exposed  for  measurement,  all  are 
of  uniform  length  (1.7—1.75  mm).  The 
most  complete  neural  arch  (Fig.  3),  which 
is  isolated,  is  1.6  mm  in  length  (including 


the  small  pre-  and  postzygapophyses), 
lacks  transverse  processes,  has  a  neural  ca- 
nal width  of  1.25  inin,  and  has  a  spinous 
process  height  of  0.8  inm.  The  arch's  lack 
of  transverse  processes  and  relatively  re- 
stricted neural  canal,  considered  with  its 
proximity  to  the  hind  foot  and  a  midcaudal 
vertebra,  are  evidence  that  the  element  is 
derived  from  the  proximal  caudal  series. 
Two  neural  arches  (also  separated  from 
their  respective  centra;  Fig.  2)  are  inter- 
preted as  representing  dorsal  vertebrae  by 
virtue  of  their  association  with  elements  of 
the  shoulder  girdle  and  the  presence  of 
transverse  processes  (approximately  1  mm 
in  length)  that  project  horizontally  from 
the  jvmction  of  the  laminae  and  pedicles. 
The  breadth  of  the  neural  canal  is  1.5  mm 
in  the  smaller,  and  2.25  mm  in  the  larger 
specimen;  likewise,  the  respective  distanc- 
es between  the  distal  ends  of  the  trans- 
verse processes  are  4.1  and  4.75  mm. 
However,  these  ineasurements  are  only 
approxiinate  because  of  slight  postmortem 


Triassic  Pterosaur  From  Greenland  'Jenkins  et  al.        159 


displacement  between  the  left  and  right 
halves  of  the  arches. 

Shoulder  Girdle.  A  dissociated  scapula 
and  partial  coracoid  are  the  only  shoulder 
elements  preserved.  The  evidence  of  a 
sternum  is  equivocal.  A  comminuted, 
sheetlike  expanse  of  bone  associated  with 
the  humeral  head  (?st.  Fig.  3)  may  be  ster- 
nal, and  at  one  end  is  a  process  that  re- 
sembles a  cristospine.  The  coracoid  (pre- 
sented in  medial  aspect.  Fig.  2)  is  6.5  mm 
long  as  preserved,  but  the  sternal  end  has 
disintegrated  beneath  vertebral  remains. 
The  acrocoracoid  process  is  partly  \asible. 
The  scapula  (in  dorsomedial  aspect.  Fig. 
2)  is  12.6  mm  in  length  as  presei-ved;  deg- 
radation of  the  caudal  end  of  the  blade 
raises  the  likelihood  of  somewhat  greater 
length  (at  least  13  mm). 

Forelimb.  The  right  humerus,  18.2  mm 
long,  has  a  slightly  sigmoidal,  dorsoventral 
curvature;  the  proximal  end  as  a  whole  is 
reflected  dorsally,  and  the  distal  end  is  re- 
flected ventrally.  The  deltopectoral  crest  is 
subtriangular,  comparable  to  that  in  juve- 
nfle  Eudimorphodon  ranzii  but  unlike  the 
shape  in  adults,  which  is  quadrangular 
(Wfld,  1978,  fig.  29).  The  humeral  head  is 
oriented  dorsally,  and  possesses  the  typi- 
cally pterosaurian  sellar  shape  (Padian, 
1983).  The  diaphysis  at  midshaft,  which  is 
slightly  flattened,  is  1.4  mm  in  width.  The 
distal  end,  3.3  mm  in  width,  lacks  cortical 
bone;  radial  and  ulnar  condyles  are  not 
distinct. 

The  right  radius  and  ulna  (Fig.  3;  esti- 
mated lengths,  19.5  and  20.1  mm,  respec- 
tively) lie  approximately  parallel  to  each 
other.  The  proximal  shaft  of  the  ulna  is 
crushed;  the  proximal  shaft  of  the  radius 
is  broken,  with  the  fragmented  ends  over- 
lapping. Much  of  the  distal  ulnar  and  ra- 
dial shafts  lie  beneath  the  humerus,  pos- 
terior skull,  and  other  bones.  The  proximal 
end  of  the  ulna  overlaps  that  of  the  radius; 
neither  is  well  presei-ved  in  this  region. 
The  distal  ulna,  preserved  in  lateral  view, 
exliibits  a  bicondylar,  topically  pterosaurian 
shape,  and  the  distal  radius  has  the  char- 


acteristic ventral  process  that  broadens  the 
articulation  with  the  proximal  cai-pals. 

Metacarpals  and  manual  phalanges  lie 
beneath  the  distal  ends  of  the  radius  and 
ulna  and  the  adjacent  jaw.  The  right  fourth 
or  wing  metacarpal  (8.4  mm  length)  is  pre- 
sented in  medial  view  (R.mc  4,  Fig.  3). 
The  well-ossified  distal  articular  surface  is 
bicondylar  (Fig.  5A),  unlike  the  trochlear 
form  that  is  conventional  among  ptero- 
saurs (Fig.  5B).  However,  as  in  other 
pterosaurs,  the  dorsal  (=extensor  side) 
condyle  has  a  radius  of  curvature  greater 
than  that  of  the  ventral  (=flexor  side)  con- 
dyle. Metacaqjal  I  (5.6  mm  length)  lies 
parallel  to  IV  (Fig.  3).  In  most  pterosaurs 
these  tv\^o  bones  are  nearly  equal  in  length 
(I  is  slightly  shorter  than  IV),  whereas  in 
this  specimen  metacai'pal  I  is  only  67%  of 
IV,  comparable  to  the  ratio  that  can  be  es- 
timated for  the  adult  holotype  of  Eudi- 
morphodon ranzii  (MCSNB  2888;  Wild, 
1978,  fig.  17).  Metacaipals  I  and  IV  are 
separated  by  a  phalanx  (2.7  mm)  and  two 
incomplete  elements  (3.8  and  3.9  mm) 
that  are  probably  also  phalanges  (Fig.  3). 
The  third  metacarpal  (8.3  mm),  which  lies 
beneath  the  adjacent  jaw,  overlies  another 
metacarpal  (here  interpreted  as  a  right 
metacarpal  II;  7.4  mm  length;  R.mc  2,  Fig. 
3)  that  became  fully  exposed  when  meta- 
carpal IV  was  removed.  Associated  with 
these  bones  is  a  small,  rounded,  flat  bone 
that  may  be  a  distal  carpal.  No  manual 
claws  are  evident. 

Parts  of  a  proximal  (first)  wing  phalanx 
are  associated  with  the  distal  end  of  a  wing 
metacarpal  on  one  block  (Fig.  3)  and  the 
posterior  end  of  the  skull  on  the  counter- 
part block  (Fig.  2).  The  bone  was  broken 
when  the  matrix  containing  the  entire 
specimen  was  first  cleaved  during  quarry- 
ing. Mid-diaphyseal  diameter  is  1.1  mm, 
but  the  shaft  broadens  at  both  ends;  the 
shaft  closest  to  the  occiput  (presumably 
the  distal  end)  has  a  diameter  of  about  2 
mm.  As  preserved,  the  restored  length  of 
the  bone  is  12.2  mm.  However,  cross-sec- 
tional diameters  of  the  two  broken  ends 
differ  (1.56,  1.05  mm  versus  1.1,  0.9  mm). 


160         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


B 


Figure  5.    The  distal  end  of  riglit  metacarpal  IV  of  (A)  Eudimorphodon  cromptonellus,  new  species,  and  (B)  Rhamphorhynchus 
sp.  (after  Wellnfiofer,  1975a,  fig.  13c)  in  distal  (above)  and  medial,  or  ulnar,  views.  Not  to  scale. 


and  thus  a  diaphyseal  section  appears  to 
be  missing.  The  other  proximal  wing  pha- 
lanx overlies  the  humeral  head  and  is  com- 
plete (18  mm  length)  although  broken  at 
midshaft  and  crushed  distally  (Fig.  3). 

Other  wing  phalanges  are  identified  on 
the  basis  of  the  dimensions  of  their  artic- 
ular ends.  A  second  wing  phalanx  (20.5 
mm  length)  lies  behind  the  skull  (Fig.  2); 
the  breadth  of  the  proximal  and  distal  ends 
are  respectively  1.5  and  1.2  mm.  The  prox- 
imal half  of  the  other  second  wing  phalanx 
protrudes  from  beneath  the  metatarsals 
(Fig.  3);  its  proximal  end  (1.35  mm 
breadth)  contacts  the  distal  end  of  a  prox- 


imal wing  phalanx.  The  proximal  two 
thirds  of  a  third  wing  phalanx  (Fig.  2)  is 
tentatively  identified  on  the  basis  of  the 
breadth  of  its  proximal  end  (1.15  mm). 
Several  fragmentary  bones  may  represent 
fourth  wing  phalanges,  but  are  too  incom- 
plete to  assess. 

Hind  Limb.  Both  femora  are  preserved 
in  close  association  (Fig.  3).  The  complete 
right  femur  (19.7  mm  length)  is  presented 
in  dorsolateral  view,  with  only  the  distal 
end  partially  obstructed  by  overlying  bone. 
The  left  femur,  represented  by  the  diaph- 
ysis  and  distal  end  (fragment  length,  15.75 
mm),  was  removed  for  histologic  exami- 


Triassic  Pterosaur  From  Greenland  •Jenkins  et  al.         161 


nation  (see  below),  as  was  another  frag- 
ment (length,  4.5  mm),  possibly  repre- 
senting the  proximal  end.  Some  distortion 
of  the  femora  is  apparent,  but  nonetheless 
botli  preserve  indications  of  the  cuivature 
(i.e.,  dorsal  deflection  of  the  proximal  end, 
and  lateral  deflection  of  the  distal  end) 
that  is  characteristic  of  pterosaurs  and  di- 
nosaurs (Padian,  1986).  The  proximal  end 
expands  into  a  distinct  head  that  is  slightly 
upturned  and  inflected  medially;  a  plane 
normal  to  the  broadly  convex  articular  sur- 
face would  intersect  the  longitudinal  axis 
of  the  shaft  at  about  45°.  The  distal  end  of 
the  femur  bears  two  contiguous  condyles 
separated  only  by  a  slight  sulcus;  the  larger 
medial  condyle  is  more  hemispheroidal  in 
comparison  to  the  ovoid,  less  convex  lat- 
eral condyle. 

A  tibia  is  preserved,  and  a  fibula  is  ten- 
tatively identified  (Fig.  3).  Unlike  the  con- 
dition in  adult  Eudirnorphodon  ranzii 
(Wild,  1978:  214)  and  most  pterosaurs,  no 
tibiofibular  synostosis  is  apparent;  the 
bones  have  been  completely  separated 
postmortem.  The  right  tibia,  contiguous 
with  the  distal  end  of  the  right  femur,  is 
complete,  although  its  proximal  end  lies 
beneath  vertebrae.  The  length  of  the  ex- 
posed bone  is  19  mm;  inasmuch  as  a  prox- 
imal expansion  is  evident,  the  extent  of  the 
obscured  part  is  probably  no  more  than  1- 
2  mm,  giving  an  estimated  length  of  20.5 
mm.  The  narrowest  diameter  of  the  cylin- 
drical shaft  is  1.1  mm.  Distally  the  tibia  is 
expanded  (2.3  mm  width)  to  support  an 
astragalar  facet  that  is  set  transversely  to 
the  shaft.  Identification  of  the  fibula,  usu- 
ally established  on  the  basis  of  tibial  asso- 
ciation, cannot  be  made  unambiguously  in 
the  present  specimen.  The  presumed  fib- 
ula (fi.  Fig.  3)  is  incomplete;  as  preserved, 
the  bone  is  13.8  mm  in  length  (and  thus 
longer  than  the  closely  associated  metatar- 
sals). The  Pproximal  end  diameter  is  1.3 
mm.  A  displaced  fragment  near  its  Pdistal 
end,  if  fibular,  would  indicate  an  overall 
fibular  length  of  about  15  mm. 

No  tarsal  bones  can  be  identified,  with 
the  possible  exception  of  a  medial  distal 


tarsal  associated  with  the  phalanges  of 
Pdigit  V  (Fig.  3).  However,  four  complete 
but  disarticulated  metatarsals  are  pre- 
served among  the  hind  limb  bones  (Fig. 
3).  Midshaft  diameters  vary  from  0.4  to  0.5 
mm.  The  distal  ends,  adjacent  to  pedal 
phalanges,  bear  articular  surfaces  that  are 
relatively  flat,  as  in  Dimorphodon  wein- 
trauhi  (Clark  et  al,  1998).  The  lengths  of 
the  metatarsals  (12,  11.35,  11.25,  and  10.5 
mm)  would  correspond  to  the  relative  pro- 
portions of  the  second,  third,  first,  and 
fourth  metatarsals  in  the  juvenile  speci- 
men of  Eudirnorphodon  ranzii  (MCSNB 
8950  B)  described  by  Wild  (1994)  in  which 
II  >  III  >  I  >  IV.  In  pterosaurs  generally, 
either  metatarsal  II  or  III  is  the  longest 
(Wellnhofer,  1978).  The  series  of  four 
metatarsals  in  the  Greenlandic  specimen 
may  represent  bones  from  different  feet, 
and  the  identifications  here  are  suggested 
on  the  basis  of  relative  lengths.  Specimen 
MCSNB  8950  B  is  in  every  comparable 
feature  a  larger  individual  than  the  Green- 
landic form  except  in  metatarsal  lengths, 
which  are  (I)  8.1  mm,  (II)  8.85  mm,  (III) 
8.6  mm,  and  (IV)  7.4  mm  (Wild,  1994,  fig. 
4). 

At  least  15  disarticulated  pedal  phalan- 
ges, including  a  claw,  are  preserved  in  the 
region  of  the  metatarsals.  Inasmuch  as 
there  are  primitively  only  12  nonungual 
phalanges  in  a  pterosaur  foot  (excepting 
pterodactyloids,  which  have  only  10),  the 
probability  that  elements  of  both  feet  are 
comingled  is  increased  still  further. 

DISCUSSION 

The  Greenlandic  pterosaur  is  smaller 
than  any  known  individual  of  Eiidimor- 
phodon  or  any  other  Triassic  pterosaur 
(Table  1);  only  some  smafl  (ostensibly  ju- 
venile) specimens  of  Pterodactijlus  spp. 
are  of  comparable  size  (Wellnhofer,  1970). 
However,  a  precise,  quantitative  compari- 
son of  size  is  limited  by  disarticulation,  and 
especially  the  lack  of  any  reliable  indica- 
tion of  axial  length.  Although  the  speci- 
mens of  Eudimorphodon  with  which  the 
Greenlandic  form  may  be  compared  are 


162         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


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Triassic  Pterosaur  From  Greenland  'Jenkins  et  al.         163 


articulated,  none  is  complete  and  the 
lengths  of  some  limb  elements  can  only  be 
estimated.  Nonetheless,  the  size  range 
represented  by  the  available  sample  of  Eu- 
dimorphodon  may  be  approximated  by 
summing  the  lengths  of  the  humerus,  ulna, 
metacarpal  IV,  wing  phalanx  1,  femur  and 
tibia  (S  h  +  .  .  .  t,  Table  1).  By  this  index, 
MGUH  VP  3393  is  one-third  the  size  of 
the  type  and  largest  specimen  of  E.  ranzii, 
and  two-thirds  the  size  of  two  juvenile 
specimens  (Fig.  6). 

Taxonomic  Assignment 

The  distinctive  dentition  in  MGUH  VP 
3393  offers  secure  evidence  on  which  to 
assign  the  specimen  to  the  genus  Eiidi- 
moiyhodon,  but  allocation  to  a  known  spe- 
cies is  problematic.  Conspecificity  with  E. 
ranzii  appears  improbable  on  the  basis  of 
two  proportional  disparities.  First,  the 
lengths  of  the  metatarsals  in  the  juvenile 
E.  ranzii  (MCSNB  8950  B)  described  by 
Wild  (1994)  from  Ponte  Giurino  are  on 
the  order  of  25%  shorter  than  those  in 
MGUH  VP  3393  (Table  1),  although  al- 
most all  other  long  bone  lengths  indicate 
that  MCSNB  8950  is  larger  (Fig.  6).  Al- 
though the  Ponte  Giurino  Eiidimoij)hodon 
lacks  a  skull.  Wild  (1994:  112-115)  ex- 
pressed confidence  in  referring  the  speci- 
men to  E.  ranzii  based  primarily  on  the 
close  correspondence  of  limb  bone  lengths 
and  proportions  to  those  of  the  Milano  ju- 
venile. Second,  femoral  lengths  in  the 
Greenlandic  specimen  and  the  two  juve- 
nile but  larger  E.  ranzii  are  essentially  the 
same  (Table  1),  with  the  improbable  im- 
plication for  conspecificity  that  all  long 
bones,  except  the  femur,  increased  in 
length  during  early  development. 

Differences  in  limb  proportions  obviate 
the  possibility  that  the  Greenlandic  ptero- 
saur might  be  an  immature  conspecific  of 
Eudimorphodon  rosenfeldi.  Eudimorpho- 
don  rosenfeldi,  decribed  by  Dalla  Vecchia 
(1995)  on  the  basis  of  a  single,  smaller 
specimen  than  the  type  of  E.  ranzii,  was 
differentiated  in  part  from  E.  ranzii  by  the 
comparable  lengths  of  the  tibia  and  ulna. 


and  the  greater  length  of  the  tibia  relative 
to  the  humerus;  these  proportions  are 
more  or  less  shared  by  the  Greenlandic 
specimen  (Table  1).  However,  unlike  the 
condition  in  E.  rosenfeldi,  the  humerus  is 
shorter  than  the  femur  in  the  Greenlandic 
specimen,  a  primitive  condition  known 
among  pterosaurs  only  in  Preondactijlus 
buffarinii  (Dalla  Vecchia,  1998,  table  5). 
Furthermore,  the  hypothesis  that  the 
Greenlandic  specimen  is  an  immature  E. 
rosenfeldi  entails  seemingly  improbable  al- 
lometric  reversals  in  comparison  to  those 
known  in  congeners.  In  E.  ranzii,  the  hu- 
meral/femoral index  decreases  from  juve- 
nile to  adult  stages  (from  about  135%  to 
115%;  Table  2),  but  the  same  index  in- 
creases when  the  Greenlandic  specimen 
(92%)  and  E.  rosenfeldi  (109%)  are  com- 
pared. A  comparable  reversal  is  seen  in  the 
ulnar/femoral  index  (Table  2).  Finally,  the 
femoral/tibial  index  in  E.  ranzii  increases 
slightly  from  juvenile  to  adult  stages, 
whereas  an  approximately  30%  decrease 
occurs  in  the  same  index  between  MGUH 
VP  3393  and  E.  rosenfeldi  (Table  2). 

Assessment  of  Ontogenetic  Stage 

Various  criteria  have  been  employed  to 
differentiate  immature  from  adult  ptero- 
saurs: relative  body  size,  degree  of  ossifi- 
cation, and  osteometric  ratios  (Wellnhofer, 
1970,  1975a-c);  synostosis,  epiphyseal  os- 
sification, and  bone  histology  (Bennett, 
1993);  and  a  combination  of  morphomet- 
ric  and  histologic  features  (Padian  et  al., 
1995). 

Insofar  as  these  criteria  may  be  applied, 
the  Greenlandic  pterosaur  would  appear 
to  be  neither  a  hatchling  nor  an  adult,  and 
is  most  probably  a  juvenile.  The  lack  of 
intracranial  fusion,  as  well  as  the  lack  of 
synostosis  between  vertebral  arches  and 
centra,  and  between  scapula  and  coracoid, 
are  indicative  of  a  preadult  stage.  The  di- 
minutive size  of  the  individual  is  sugges- 
tive of  immaturity,  but  not  conclusive.  The 
limb  proportions  may  be  interpreted  as 
ontogenetically  immature,  or  phylogeneti- 
cally  primitive,  or  both.   In  the  series  of 


164         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


5  cm 


Triassic  Pterosaur  From  Greenland  'Jenkins  et  al.        165 


Pterodactylus  spp.  studied  by  Wellnhofer  images;  evidence  of  calcified  cartilage  is 
(1970),  juveniles  generally  possess  niore  preserved  in  a  few  areas.  Although  no 
comparable  humeral/radial  and  femoral/  trace  is  found  of  a  subchondral  bone  plate 
tibial  lengths  than  do  adults.  Although  the  or  transphyseal  canals,  a  delineation  is  vis- 
limb  proportions  of  the  Greenlandic  ible  between  the  diaphyseal  and  epiphy- 
pterosaur  represent  the  juvenile  end  of  seal— inetaphyseal  regions.  Histology  thus 
this  allometric  spectrum,  these  propor-  provides  primarily  negative  evidence  with 
tions  are  also  intermediate  between  vari-  which  to  assess  the  ontogenetic  stage  of 
ous  basal  pterosaurs  and  nonpterosaurians  the  Greenlandic  pterosaur. 
(Table  2). 

Histologic  sections  of  the  the  left  femur  Appendicular  Proportions 

yielded  less  than  definitive  results  because  Certain  appendicular  proportions  of  the 

of  extensive  diagenetic  alteration  and  re-  tiny  Greenlandic  form  lie  within  the  range 

sultant   artifacts.   As   in  pterosaurs   and  known  among  other  pterosaurs  (Table  2). 

birds,  the  diaphyseal  cortex  is  thin  (about  The  humerus  is  slightly  shorter  (92%)  than 

15— 20%  of  shaft  diameter).  The  wide  med-  the    femur,    a    condition    unusual    among 

ullary  cavity,  infilled  with  calcite,  shows  no  pterosaurs;    comparable    proportions    are 

trace  of  trabecular  projections  that  have  known    only    in    Preondactijlus    biijfarinii 

been  identified  in  chelonian,  crocodilian,  (Dalla  Vecchia,  1998,  table  5)  and  in  Pter- 

and  dinosaurian  embiyos  (Homer  et  al.,  odactylus  antiqiius,  P.  suevicus,  and  P.  mi- 

2001).  The  bone  cortex  is  mostly  parallel  cronijx    (Wellnhofer,    1970;    see    Bennett, 

fibered,  with  only  indistinct  indications  of  1996,   for  a  taxonomic  reallocation  of  P. 

localized  lamellar  deposition;  the  osteocy-  suevicus  to  the  genus  Cycnorhamphus).  In 

tic  spaces  are  variably  distributed.  No  fea-  both  juvenile   and  adult  Eiidimorphodon 

tures  are  present  that  might  be  expected  ranzii  as  well  as  in  other  pterosaurs,  these 

in  an  embryo  or  rapidly  growing  neonate,  proportions  are  reversed.  In  other  appen- 

nor  are  indicators  present  of  growth  stasis  dicular  proportions  the  Greenlandic  ptero- 

and  maturity.  The  parallel-fibered  matrix  saur  is  distinctive  (Table  2).  Relative  to  the 

differs  from  the  fibrolamellar  architecture  humerus  or  femur,  the  ulna  is  shorter  than 

knowii  in  later  pterosaurs,  which  has  been  in  any  known  pterosaur.  Similarly,  relative 

interpreted  as  indicative  of  rapid  growth  to  the  femur,  the  tibia  is  shorter  than  in 

(Bennett,  1993).  Vascular  canals  are  nearly  any  known  pterosaur.  Among  pterosaurs, 

all  longitudinally  oriented;  the  canals  ap-  the  Greenlandic  pterosaur  is  distinctive  in 

pear  to  be  primary,  but  no  evidence  is  pre-  having  the  relative  lengths  of  brachium  to 

sent  of  primary  osteonal  development.  The  antebrachium,    and   femur   to   cms,   both 

bone  is  less  vascularized  than  that  of  ein-  nearly  equal. 

bryonic   and   hatchling   dinosaurs,    and   is  The  length  of  the  metatarsus  also  ap- 

more  comparable  to  that  in  hatchling  alii-  pears   to  be   unusual.    Metatarsals  in  the 

gators  (see  Homer  et  al.,  2001).  Longitu-  Greenlandic  pterosaur  vary  from   132  to 

dinal  sections  through  the  epiphysis  reveal  156%  of  the  lengths  represented  in  a  ju- 

endosteo-endochondral    trabeculae,    most  venile  eudimoiphodontid  (MCSNB  8950 

of  which  are  diagenetically  altered  to  ghost  B),  which  is  particularly  notable  because 


<— 

Figure  6.  Limb  proportions  of  the  adult,  type  specimen  of  Eudimorphodon  ranzii  (MCSNB  2888),  top,  compared  with  a  juvenile 
E.  ranzii  (MCSNB  8950),  middle,  and  E.  cromptonellus,  new  species  (MGUH  VP  3393),  bottom.  The  limbs  are  positioned  in  the 
same  transverse  plane  to  permit  graphic  illustration  of  the  relative  lengths  of  the  long  bones;  no  postural  or  kinematic  represen- 
tation is  intended.  Data  on  E.  ranzii  are  from  Wild  (1978,  1994).  Appendicular  bone  lengths  are  estimated  for  the  metatarsus  of 
MCSNB  2888;  the  wing  phalanges  distal  to  the  break  in  the  proximal  wing  phalanx  of  MCSNB  2888;  and  the  first  and  fourth 
wing  phalanges  of  MGUH  VP  3393. 


166         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Table  2.    Limb  segment  proportions.  Data  from  (a)  Ewer,  1965;  (b)  Sereno  and  Arcucci,  1994;  (c) 

PADIAN,  personal  OBSERVATION;  (d)   DALLA  VECCHIA,   1998;  (e)  WILD,   1978;  (f)  WILD,   1994;  (g)   DALLA 
VECCHIA,   1995;   (h)  UNWIN,   1988,  and  PADIAN,  personal  OBSERVATION  (l)  WELLNHOFER,   1978,  AND  Pa- 

DIAN,  personal  OBSERVATION.  •' 


Humerus/ 

Humerus/ 

Femur/ 

Ulna/ 

Humerus/ 

femur 

ulna 

tibia 

femur 

tibia 

N 

(%) 

(%) 

(%) 

(%) 

(%) 

Euparkeria  capensis 

1 
(a) 

68 

112 

117 

60 

79 

Marasuch us  lilloensis 

1 

(b) 

69 

107 

80 

64 

55 

Scleromoclihis  taijlori 

7 
(c) 

62 

91 

93 

69 

57 

Eudiinorphodon  cromptonelhis. 

1 

92 

90 

96 

102 

89 

new  species,  MGUH  VP  3393 

Preondactijhis  biiffariuii. 

1 

98 

76 

74 

129 

73 

MFSN  1770 

(d) 

Peteinosaunis  zambeUU, 

1 

104 

80 

76 

130 

79 

MCSNB  3359 

(e) 

Eudimorplwdon  ranzii. 

1 

137 

74 

76 

184 

104 

juvenile,  Milano  specimen 

(e) 

Eiidimoiyhodon  ranzii. 

1 

133 

78 

77 

171 

102 

juvenile,  MCSNB  8950 

(f) 

Eudimorplwdon  ranzii, 

1 

115 

72 

82 

159 

94 

adult,  tyi^e,  MCSNB  2888 

(e) 

Eudi moi~phodon  rosenfcldi 

1 

109 

74 

68 

149 

75 

MFSN  1797 

(g) 

Dinior})hodon  macroni/x 

1^ 

(h) 

104-109 

77 

64-72 

130-134 

67-75 

Donjgnathus  banthensis 

15 

120-138 

59-71 

65-81 

191-210 

82-105 

Campylognathoides  liasicus 

W 
6 

123-141 

78-86 

75-94 

153-169 

100-132 

Campijlognathoides  zitteli 

1-2 

(i) 

108 

85-94 

74 

126 

80-100 

every  other  limb  dimension  (wdth  the  ex- 
ception of  femoral  length)  indicates  that 
MCSNB  8950  is  a  larger  animal  (Table  1; 
Fig.  6).  Similarly,  even  the  shortest  meta- 
tarsal of  the  Greenlandic  pterosaur  (ca.  11 
mm)  is  longer  than  the  longest  metatarsals 
of  Pterodactijlus  specimens  that,  in  other 
limb  dimensions,  appear  to  be  otherwise 
comparably  sized  or  even  larger  (P.  ele- 
gans,  no.  49,  7.8  mm;  P.  elegans,  no.  12, 
9.5  iTim;  P.  inicronyx;  no.  42,  8.8  mm; 
Wellnhofer,  1970,  fig.  19).  In  most  ptero- 
saurs, the  average  length  of  metatarsals  I— 
IV  is  less  than  that  of  metacarpal  IV.  Ex- 
ceptions are  Peteinosaunis  zamheUii 
(Wild,  1978,  pi.  14)  and  Campijlognathoi- 
des zitteli  (Pheninger,  1895:  216-217; 
Wellnhofer,   1978:   38),   in  which  average 


metatarsal  lengths  are  greater  (105%, 
129%,  respectively).  The  Greenlandic 
form  is  even  inore  exceptional,  having 
metatarsals  that  average  141%  of  metacar- 
pal IV  length. 

Wild  (1978)  interpreted  Peteinosaunis 
zamhellii  as  the  most  primitive  pterosaur 
then  known  on  the  basis  of  the  relative 
shortness  of  the  wing  compared  to  the 
length  of  the  hind  limb.  Wild  (1984:  54) 
later  cited  various  limb  segment  ratios  in 
support  of  his  obseiA/ation  that  Preondac- 
tijhis hiiffarinii  is  unique  among  ptero- 
saurs for  "...  an  unproportionally  long 
hind-limb,"  and  a  wing  that  is  "extraordi- 
narily short."  More  recently,  a  reanalysis  of 
Pr.  hujfarinii  led  Dalla  Vecchia  (1998:  365) 
to  conclude  that  Pe.  zanibellii,  Pr  hiijfar- 


Triassic  Pterosaur  From  Greenland  'Jenkins  et  ol.        167 


inii,  and  Dimorphodon  macronyx  are  extended  to  promote  maximum  thrust,  and 
"probably  the  most  primitive  of  all  known  during  upstroke  the  effective  wingspan  is 
pterosaurs."  Direct  comparison  of  these  shortened.  Nonetheless,  the  analogy  is 
taxa  with  the  Greenlandic  pterosaur  is  lim-  limited  by  anatomical  differences.  Birds 
ited  because  the  fourth  wing  phalanx  in  possess  a  multiaxial  carpometacaipal  joint 
MGUH  VP  3393  is  unknown,  and  the  complex  with  numerous  degrees  of  free- 
lengths  of  various  phalanges  can  only  be  dom  and  movement  possibilities  (Vazquez, 
estimated.  Nonetheless,  a  restricted  com-  1992).  Reduction  of  aerofoil  drag  of  the 
parison  may  be  made  on  the  basis  of  distal  wing  during  upstroke  in  birds  may 
summed  lengths  of  the  propodial,  meso-  be  further  promoted  by  a  rotation  of  the 
podial,  and  metapodial  elements  (S  hu-  feathers  that  opens  slots  between  them 
merus  +  ulna  +  metacarpal  IV/X  femur  +  (the  valve  function  of  Norberg,  1985),  or 
tibia  +  average  metatarsal  length).  The  by  a  closure  of  the  imbricating  fan  of 
proportionate  lengths  of  the  proximal  fore-  feathers.  The  fiber-stiffened  distal  patagi- 
limb  to  proximal  hind  limb,  thus  defined,  um  of  pterosaurs  (i.e.,  distal  to  the  meta- 
are  90%  in  the  Greenlandic  pterosaur,  carpophalangeal  joint;  Padian  and  Rayner, 
95%  in  Pr.  hiijfarinii,  and  100%  in  Pe.  1993;  see  also  Unwin  et  al.,  1993)  has  no 
zauibellii.  In  D.  macronyx  the  proportion  comparable  intrinsic  mechanisms  for 
is  104%,  in  Campylognathoides  liasicus  changes  in  shape,  and  thus  shortening  ef- 
124%,  in  juvenile  Eudiinoiyhodon  ranzii  fective  wingspan  would  appear  to  be  the 
and  Dorygnathus  banthensis  130%,  but  in  only  alternative  mechanism  for  reducing 
Campylognathoides  zitteli,  with  its  unusu-  aerofoil  drag  during  upstroke.  The  joint 
ally  short  hind  limb,  94%.  that  permits  the  largest  range  of  excursion 

is  the  metacarpophalangeal  joint.  Howev- 

The  Pterosaurian  Wingbeat  Cycle  ^^   th^  pterosaurian  metacaipophalangeal 

Most   reconstructions   of  pterosaurs   in  joint  is  a  uniaxial  joint,  with  one  degree  of 

flight  depict  the  wings  fully  extended  in  a  freedom;   the   asymmetrical   form   of  this 

position  that  is  suggestive  of  soaring,  al-  joint,    which    entails    a    screwlike    motion 

though  general  agreement  exists  that  all  (Wellnhofer,  1978),  provides  for  radial  de- 

except  the  largest  pterosaurs  were  capable  viation  of  the  wing  finger  upon  wing  ex- 

of  sustained,  flapping  flight.  The  only  at-  tension,   and  ulnar  deviation   and  flexion 

tempt  to  illustrate  the  excursion  of  an  en-  upon  wing  folding. 

tire  wing  is  by  Wellnhofer  (1991:  153),  but  The  bicondylar  form  of  the  metacai-po- 

his  diagram  of  a  pterodactyloid  only  de-  phalangeal     joint     in     Eudimorphodon 

picts   the   downstroke,    and   shows    major  cromptoneUiis  appears  to  be  intermediate 

flexion  at  the  wrist  and  little  at  the  meta-  between  a  primitive,  unicondylar  joint  and 

carpophalangeal  joint.    Subsequently,   Pa-  the  trochlear  form  of  later  pterosaurs.  This 

dian  and  Rayner  (1993:  143,  fig.  13C)  sug-  spectrum  of  joint  configurations  represents 

gested  that  the  pterosaurian  "...  metacar-  increasing  mechanical  stability,  consonant 

pophalangeal  joint  is  ideally  adapted  for  with  the  interpretation  that  the  joint  was 

sweeping  the  wingtip  during  the  upstroke  actively  employed  in  flapping  flight.  As  in 

in  a  movement  analogous  to  that  in  birds,  other  pterosaurs,  the  joint  in  Eudimoiyho- 

With  their  long,  thin  wings  the  pterosaur  don    cromptoneUiis    is    stiiicturally   asym- 

wingbeat  would  have  appeared  very  simi-  metric:  the  dorsal  condyle  has  a  larger  ra- 

lar  to  that  of  long-winged  birds  such  as  dius  of  curvature,  and  a  more  extensive  ar- 

gulls  or  albatrosses."  ticular  surface,  than  the  ventral  condyle 

As  a  first-order  approximation,  an  avian  (Fig.   5).    However,   the  joint   surfaces   at 

model   of  a  pterosaurian   wingbeat  cycle  their    extensor    end    are    evenly    aligned, 

fulfills  fundamental  aerodynamic  require-  Thus,  during  the  downstroke,  the  extend- 

ments:  upon  downstroke  the  wing  is  fully  ed  distal  wing  (supported  by  the  four  pha- 


168         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  7.  Reconstruction  of  metacarpophalangeal  (mp)  joint  function  in  Eudimorphodon  cromptonellus,  new  species,  during 
flapping  flight.  The  wing,  in  dorsolateral  view,  is  shown  in  an  extended  position  during  early  downstroke  and  in  a  flexed  position 
in  early  upstroke.  The  inset  above  depicts  mp  joint  relations,  disarticulated  for  illustrative  purposes,  in  the  extended  (E)  and 
flexed  (F)  positions.  The  axis  of  the  mp  joint  in  an  extended  position  (e)  is  normal  to  the  metacarpal  shaft  because  of  the 
symmetry  of  the  condyles  in  this  region;  the  proximal  phalanx  is  thus  aligned  with  metacarpal  IV.  The  mp  joint  axis  in  a  flexed 
position  (f)  is  oblique  to  the  metacarpal  shaft  because  of  condylar  asymmetry,  resulting  in  a  slight  rotation  and  flexion  of  the 
distal  wing  as  the  mp  joint  undergoes  ulnar  deviation.  The  excursion  of  the  mp  joint  during  the  upstroke  of  flapping  flight  is 
consonant  with  the  distribution  of  fibers  as  interpreted  by  Wild  (1994:  109)  for  the  congener  E.  ranz//  (MCSNB  8950).  Elongate, 
membrane  stiffening  fibers  occur  in  the  distal  wing,  whereas  short  fibers  in  the  proximal  wing  allow  flexibility. 


Triassic  Pterosaur  From  Greenland  'Jenkins  et  al.        169 


langes)  is  aligned  with  the  proximal  wing 
(Fig.  7)  because  the  joint's  axis  at  the  ex- 
tensor end  of  the  metacarpophalangeal 
joint  is  perpendicular  to  the  plane  of  the 
entire  wing  (Fig.  7,  top  inset).  Were  the 
metacai-pophalangeal  joint  to  be  flexed 
during  upstroke,  the  shift  in  the  joint  s  axis 
(Fig.  7,  top  inset),  which  results  from  con- 
dylar asymmetry,  engenders  a  rotation  and 
flexion  of  the  distal  wing  out  of  the  plane 
of  the  proximal  wing.  Thus,  during  up- 
stroke, the  distal  wing  would  be  directed 
ventrally  and  somewhat  everted  (i.e.,  the 
ventral  surface  turned  to  face  slightly  lat- 
erally). On  this  interpretation,  the  trafling 
position  of  the  distal  wing  relative  to  the 
proximal  wing  during  the  upstroke  would 
be  comparable  to  that  seen  in  birds,  but 
the  rotation  and  flexion  would  seem 
uniquely  pterosaurian. 

ACKNOWLEDGMENTS 

Field  work,  supported  by  grants  from 
the  National  Science  Foundation,  the 
Carlsberg  Foundation,  and  the  Putnam 
Expeditionary  Fund  of  the  Museum  of 
Comparative  Zoology,  was  initiated  on  the 
basis  of  geological  studies  by  L.  B.  Clem- 
mensen  (University  of  Copenhagen).  We 
thank  W.  W  Amaral  for  preparation  of  the 
specimen;  A.  H.  Coleman  and  P.  Chan- 
doha  for  photography;  L.  L.  Meszoly  for 
drawing  Figures  2  and  3;  and  K.  Brown- 
Wing  for  rendering  Figures  5,  6,  and  7. 
For  histologic  examination  of  the  femur, 
we  are  grateful  to  M.  Goodwin  (University 
of  California  Museum  of  Paleontology) 
and  E.  Lamm  (Museum  of  the  Rockies) 
for  technical  assistance,  A.  Paulsen  for 
photography,  and  J.  R.  Horner  and  A.  de 
Ricqles  for  consultation.  Finally,  we  thank 
S.  C.  Bennett,  F.  M.  Dalla  Vecchia,  K.  M. 
Middleton,  P.  Wellnhofer,  and  R.  Wild  for 
authoritative,  helpful  reviews. 

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IMMATURE  RHIZODONTIDS  FROM  THE  DEVONIAN  OF 
NORTH  AMERICA 


MARCUS  C.  DAVIS/  NEIL  H.  SHUBIN,^^*  AND  E.  B. 

Abstract.  New  fossils  from  the  Duncannon  Mem- 
ber of  the  Catsldll  Formation  provide  material  for 
hypotheses  about  the  evolution  of  fin  development 
and  function  in  extinct  sarcopterygians.  The  rhizo- 
dontid  affinity  of  these  specimens  is  supported  by  the 
pattern  of  overlap  between  the  clavicle  and  cleith- 
rum,  the  robustness  of  the  pectoral  girdle,  the  pres- 
ence of  unjointed  and  elongate  lepidotrichia  in  the 
pectoral  appendage,  and  the  presence  of  multiple  lat- 
eral line  canals.  The  small  bodv  size  and  weakly  os- 
sified endochondral  skeletons  indicate  that  these  in- 
dividuals are  immature.  The  pectoral  fin  includes 
both  dermal  and  endochondral  elements;  massive, 
unjointed  dermal  rays  that  compose  the  bulk  of  the 
appendage  envelop  the  endochondral  bones.  The  em- 
phasis on  both  dermal  and  endochondral  elements  in 
rhizodontids  is  an  unexpected  intermediate  condition 
between  ray-finned  and  lobe-finned  designs  that 
could  not  be  predicted  from  current  models  of  der- 
mal fin  development.  The  large  size  of  rhizodontids 
and,  perhaps,  aspects  of  their  locomotor  and  feeding 
strategies,  may  have  necessitated  fins  with  large  sur- 
face areas.  Expansion  of  the  surface  area  of  the  fins 
was  accomplished  by  elaboration  of  the  dermal  ra- 
dials.  The  evolution  of  an  extensive  endochondral 
skeleton  in  rhizodontids  may  relate  to  the  role  of  the 
endochondral  skeleton  in  the  control  of  movements 
and  shape  of  this  expanded  fin. 

INTRODUCTION 

Rhizodontid  sarcopterygians  are  large, 
predatory  fish  that  have  a  variety  of  unique 
features  of  the  skull,  pectoral  girdle,  fins, 
and  lateral  line  systems  (Andrews,  1985). 
Many  of  these  features,  such  as  the  un- 
jointed and  elongate  lepidotrichia  in  the 
pectoral    fins,    suggest    that    rhizodontids 


*  Corresponding  Author 

'  Department  of  Organismal  Biolog)'  and  Anatomy, 
University  of  Chicago,  1027  East  57th  Street,  Chi- 
cago, Illinois  60637. 

-  Department  of  Vertebrate  Biolog>',  Academy  of 
Natural  Sciences  of  Philadelphia,  1900  Benjamin 
Franklin  Parkway,  Philadelphia,  Pennsylvania  19103. 


DAESCHLER2 
may  have  been  specialized  for  modes  of 
locomotion  and  predation  unseen  in  other 
sarcopterygian  taxa.  Represented  by  eight 
or  nine  genera  froin  the  Devonian  and 
Carboniferous,  these  fish  typically  attain 
lengths  greater  than  3  m.  Because  of  the 
many  similarities  between  the  endochon- 
dral skeletons  of  rhizodontid  fins  and  tet- 
rapod  limbs,  these  taxa  have  figured  prom- 
inently in  studies  of  the  origin  of  tetrapod 
limbs  (e.g.,  Gregory  and  Raven,  1941). 

Remains  of  rhizodontid  sarcopterygians 
are  major  components  of  Late  Devonian 
and  Early  Carboniferous  nonmarine  fossil 
assemblages  (Andrews,  1985;  Young  et  al., 
1992).  Scales,  isolated  vertebrae,  and  teeth 
are  the  most  common  rhizodontid  ele- 
ments encountered;  these  are  usually  as- 
signed to  the  genera  Rhizodus  and  Strep- 
sodus.  However,  more  complete  material 
is  rare.  The  most  complete  specimens  are 
known  from  the  Dinantian  of  Foulden, 
United  Kingdom  {Strepsodiis,  several  par- 
tially articulated  specimens  [Andrews, 
1985]),  the  Lower  Carboniferous  of  Aus- 
tralia (Barameda,  an  articulated  partial 
skeleton  preserved  as  a  natural  mold 
[Long,  1989]),  the  Frasnian  of  Antarctica 
(Notorhizodon,  isolated  cranial  and  girdle 
elements  [Young  et  al,  1992]),  and  the  Fa- 
mennian  of  New  South  Wales,  Australia 
(Gooloogongia,  articulated  individuals  pre- 
served as  natural  molds  [Johanson  and 
Alilberg,  1998])  and  of  North  America 
(Saiiriptenis,  isolated  pectoral  fins  and 
scales  [Hall,  1843;  Daeschler  and  Shubin, 
1998]). 

A  number  of  features,  particularly  in  the 
paired  fins  and  associated  girdles,  distin- 


Bull.  Mus.  Comp.  ZooL,  156(1):  171-187,  October, 


2001 


171 


172         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


guish  rhizodontids  as  a  clade.  Rhizodontid 
pectoral  girdles  are  unique  in  both  their 
massive  relative  size  as  well  as  the  nature 
of  the  internal  articulations  between  con- 
stituent bones.  The  ventral  laminae  of  the 
clavicles  and  cleithra  are  broad,  orna- 
mented plates  that  extend  cranially,  en- 
closing the  caudal  portion  of  the  gular  re- 
gion (Andrews,  1985,  fig.  10b).  In  porole- 
piforiTis  and  osteolepids  (for  example  see 
Eusthenopteron  [Andrews  and  Westoll, 
1970,  fig.  1]),  the  dorsal  lamina  of  the 
cleithrum  is  overlapped  medially  by  the 
clavicle,  whereas  the  ventral  lamina  of  the 
clavicle  is  overlapped  medially  by  the 
cleithrum.  In  rhizodontids  the  pattern  of 
overlap  is  reversed:  the  dorsal  lamina  of 
the  cleithrum  is  overlapped  laterally  by  the 
clavicle,  and  the  ventral  lamina  of  the  clav- 
icle is  overlapped  laterally  by  the  cleith- 
rum. The  function  of  this  massive  shoulder 
girdle,  with  its  unusual  pattern  of  overlap 
between  constituent  elements,  is  un- 
kno"wn. 

Although  rhizodontid  pectoral  girdles 
are  readily  distinguished  from  those  of 
other  sarcopteiygians,  the  pectoral  fins  of 
rhizodontids  share  a  number  of  similarities 
with  the  limbs  of  tetrapods.  The  best- 
known  rhizodontid  fins  are  isolated  ap- 
pendages that  have  been  assigned  to  the 
genus  Sauriptenis.  Sauriptents  possesses  a 
limblike  arrangement  of  endochondral 
bones,  including  distal  radials  that  have 
been  compared  to  tetrapod  digits  (Gregoiy 
and  Raven,  1941;  Daeschler  and  Shubin, 
1998).  Despite  differences  in  the  size  and 
shape  of  corresponding  elements  in  Sau- 
riptenis and  tetrapods,  the  pattern  of  en- 
dochondral bones  is  extremely  similar.  The 
phylogenetic  significance  of  these  similar- 
ities is  muddled  by  the  fact  that  recent  cla- 
distic  studies  do  not  support  a  sister-group 
relationship  between  tetrapods  and  rhizo- 
dontids. Missing  data  are  probleinatic  in 
the  cladistic  analysis  of  the  higher  level  re- 
lationships of  rhizodontids  because  few 
overlapping  characters  occur  between  taxa 
such  as  Sauriptenis  (consisting  of  isolated 
fins  and  scales)   and  Gooloogongia  (con- 


sisting of  a  relatively  complete  skull  and 
body,  but  with  poorly  preserved  fins). 

Here  we  describe  immature  rhizodontid 
specimens,  which  we  refer  to  the  genus 
Sauriptenis,  from  the  Famennian  Catsldll 
Formation  of  North  Ainerica.  The  relative 
completeness  of  the  skeletons  provides  an 
opportunity  to  examine  the  morphology  of 
rhizodontids  in  greater  detail  and  to  assess 
hypotheses  on  the  ontogeny  of  the  paired 
fin  skeleton  in  nontetrapod  sarcopterygi- 
ans. 

GEOLOGICAL  SETTING 

The  new  rhizodontid  material  was  re- 
covered from  the  Late  Devonian  Red  Hill 
locality  in  Clinton  County,  Pennsylvania 
(Fig.  1).  Red  Hill  is  a  road-cut  exposure  of 
the  Duncannon  Member  of  the  Catsldll 
Formation.  During  the  Late  Devonian, 
the  Catskill  Delta  extended  from  the  foot- 
hills of  the  Acadian  highlands  within  the 
Old  Red  Continent  (Euramerica)  to  the 
epicontinental  Catskill  Sea  that  lay  to  the 
west  (Woodrow,  1985).  The  fossiliferous 
horizons  at  Red  Hill  have  been  interpreted 
to  represent  channel  margin  and  overbank 
deposits  of  a  wide  river  flowing  across  a 
low-gradient  floodplain  under  a  subtropi- 
cal climate  (Woodrow  et  al.,  1995).  The  2- 
m-thick  fossiliferous  zone  at  Red  Hill  has 
produced  the  most  abundant  and  well-pre- 
served vertebrate  fossils  discovered  to  date 
from  the  Catskill  Formation. 

The  rhizodontids  were  recovered  from 
a  grayish-red,  poorly  bedded  sandy  silt- 
stone  unit  within  the  fossiliferous  zone. 
Their  degree  of  articulation  is  exceptional, 
even  for  Red  Hill,  and  suggests  that  the 
specimens  were  quickly  buried,  did  not 
undergo  significant  postmortem  transport, 
and  were  not  subsequently  reworked.  The 
two  specimens  on  which  this  study  is 
based  are  preserved  on  opposite  sides  of 
the  same  block  of  matrix.  Remarkably, 
these  specimens  are  the  only  rhizodontids 
known  from  Red  Hill. 

Red  Hill  has  yielded  a  diverse  assem- 
blage of  freshwater  vertebrates,  terrestrial 
plants,  and  invertebrates.  Among  the  ver- 


Immature  Rhizodontids  from  North  America  •  Davis  et  al. 


173 


Figure  1 .     Location  of  Red  Hill  site,  Clinton  County,  Pennsylvania,  USA.  Shaded  areas  represent  Devonian  age  sediments. 
Abbreviations;  80,  Interstate  80;  120,  Pennsylvania  State  Route  120. 


tebrates  from  the  fossiliferous  zone  are 
two  early  tetrapod  taxa,  at  least  three  taxa 
of  osteolepiform  sarcopteiygians,  an  early 
actinopterygian,  groenlandaspidid  and 
phyllolepid  placoderms,  gyracanthid  acan- 
thodians,  and  chondrichthyans.  This  ver- 
tebrate fauna  is  associated  with  progyni- 
nosperm  and  lycopsid  plants  as  well  as  pa- 
lynomorphs.  In  addition,  trigonotarbid  ar- 
thropods are  preserved  both  as  body  fossils 
and  traces. 


SYSTEMATIC  PALEONTOLOGY 

Sarcopterygii  Romer,  1955 

Rhizodontida  Andrews  and  Westoll,  1970 

cf.  Sauripterus  Hall,  1843 

Diagnosis.  Rhizodontid  affinities  are 
supported  by  the  following  features: 
cleithruin  overlaps  dorsal  lamina  of  clavi- 
cle medially  and  ventral  lamina  of  clavicle 
laterally  (reversed  from  the  condition  seen 


174         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


in  osteolepiforms);  laterally  expanded  ven- 
tral lamina  of  clavicle  and  cleithrum;  ros- 
trally  expanded  ventral  lamina  of  cleith- 
rum relative  to  the  condition  seen  in  os- 
teolepiforms; scapulocoracoid  sits  dorsal  to 
the  junction  of  dorsal  and  ventral  laminae 
of  cleithrum;  dermal  skeleton  of  the  paired 
fins  coinposed  of  elongate,  unjointed  lep- 
idotrichia;  no  postaxial  process  on  the  ul- 
nare;  accessoiy  lateral  lines.  Assigned  to 
the  genus  Sauriptenis  based  on  the  follow- 
ing: radius  anteroposteriorly  broader  than 
ulna  relative  to  the  condition  seen  in  Bar- 
ameda  (Long,  1989)  and  Strepsodus  (An- 
drews, 1985);  ventral  laminae  of  cleithra 
meet  at  midline. 

These  specimens  also  have  unique  char- 
acters seen  in  no  other  known  rhizodontid: 
no  entepicondyle  on  the  humerus;  no  dis- 
tal radials  in  the  pectoral  fin;  no  articula- 
tions between  fin  endochondral  elements; 
disproportionally  large  pectoral  fins  rela- 
tive to  body  size  (when  compared  to  all 
rhizodontids  and  osteolepids  for  which  this 
can  be  measured);  elongate  interclavicle 
(craniocaudal  length  greater  than  that  of 
ventral  laminae  of  clavicle).  Many  of  these 
characters  can  be  interpreted  as  being  re- 
lated to  the  ontogenetic  stage  of  ossifica- 
tion in  the  fin  endoskeleton.  Therefore, 
these  specimens  are  referred  to  the  genus 
Saiiriptenis  as  immature  individuals. 

Horizon  and  Locality.  The  Duncannon 
Member  of  the  Catskill  Formation.  USA, 
Pennsylvania,  Clinton  County,  Red  Hill 
(coordinates  41°20.645'N,  77°40.800'W). 

Age.  Late  Devonian;  late  Famennian 
stage  (Fa2c  substage);  Riigospora  flexu- 
osa-Grandispora  cornuta  palynomorph 
zone  (Traverse,  in  press). 

Material. '  All  specimens  are  housed  in 
the  Academy  of  Natural  Sciences  of  Phil- 
adelphia (ANSP):  ANSP  20980,  a  well- 
preserved  skeleton  lacking  most  cranial  el- 
ements and  median  fins,  preserved  as  part 
and  counterpart  (Figs.  2,  3);  ANSP  20981, 
a  smaller  individual  consisting  of  a  left 
dentary,  paired  gulars,  pectoral  girdle  and 
fins,  preserved  on  the  reverse  side  of  the 
ANSP  20980  counterpart  block  (Fig.  4). 


DESCRIPTION 

Operculogular  Series.  Lateral  gulars,  a 
left  operculum,  and  portions  of  the  sub- 
mandibular series  are  preserved  on  ANSP 
20981.  The  lateral  gulars  are  preserved  in 
internal  view,  with  the  left  gular,  which  is 
relatively  more  complete,  overlapping  the 
right.  Both  sides  lack  the  rostral  margin.  It 
is  difficult  to  determine  whether  a  median 
gular  was  present.  The  ornamentation  on 
the  internal  surface  consists  of  shallow 
grooves  that  radiate  caudally  from  the  ros- 
trolateral  margin.  Medial  to  this  margin, 
two  small  teeth  are  presei"ved  in  cross  sec- 
tion (Fig.  4,  f.  vom).  These  teeth  may  have 
been  derived  from  the  left  derinopalatine 
or  vomer,  both  of  which  are  not  preserved. 
A  recessed  edge  along  the  lateral  margin 
of  the  left  gular  marks  the  contact  for  the 
submandibulars.  The  submandibular  se- 
ries lies  medial  to  the  labial  margin  of  the 
dentary  and  lateral  to  the  left  gular.  The 
bone  in  this  area  appears  very  thin  and 
broken,  making  it  impossible  to  identify 
sutures. 

A  left  opercular  is  preseived  in  ANSP 
20981  (Fig.  4).  The  external  surface  is 
sparsely  ornamented  with  a  series  of  shal- 
low, parallel  grooves  that  extend  dorsoven- 
trally  across  the  bone.  The  margins  of  the 
opercular  lack  this  ornamentation  and  ap- 
pear relatively  smooth.  The  opercular  is 
narrow  rostrocaudally  and  deep  dorsoven- 
trally  This  shape  is  similar  to  that  of  Goo- 
loogongia  (Johanson  and  Ahlberg,  1998, 
fig.  2g),  but  unlike  the  rounded  operculars 
of  Barameda  (Long,  1989,  fig.  5b)  and 
Strepsodus  (Andrews,  1985,  fig.  lb).  In  po- 
rolepiforms  and  osteolepids  the  opercular 
extends  caudally  to  contact  the  cranial 
margin  of  the  dorsal  lamina  of  the  cleith- 
rum. The  proportions  of  the  opercular  in 
ANSP  20981  make  it  unlikely  that  it  abut- 
ted against  the  dorsal  lamina  of  the  cleith- 
rum. The  resulting  gap  was  likely  filled  by 
soft  tissue,  as  in  Latinieria  (Jarvik,  1980). 
A  preopercular  lies  rostral  to  the  opercu- 
lar. The  poor  preservation  of  the  sutures 


Immature  Rhizodontids  from  North  America  •  Davis  et  al.        175 


10  mm 


Figure  2.  ANSP  20980  in  part.  (A)  Photograph  of  specimen.  (B)  Labeled  drawing:  light  shading  represents  fossil  or  fossil 
impression,  dark  shading  represents  matrix.  Boxed  area  refers  to  Figure  5. 

Abbreviations  for  Figs.  2-7:  ano,  anocleithrum;  bo,  internal  boss  of  scale;  cen,  centra;  dm,  cleithrum;  dm.  dl,  dorsal  lamina  of 
cleithrum;  dm.  vl,  ventral  lamina  of  cleithrum;  civ.  dl,  dorsal  lamina  of  clavicle;  civ.  vl,  ventral  lamina  of  clavicle;  d1,  d8,  digits  1, 
8;  de,  dentary;  epi,  epicaudal  lobe;  f.  par,  parasymphysial  fang;  f.  vom,  vomerine  fang;  gul,  gular;  H,  humerus;  hyp,  hypocaudal 
lobe;  iciv,  interdavide;  i,  intermedium;  j.  lep,  jointed  lepidotrichia;  Ibw,  lateral  body  wall;  m.  ex,  median  extrascapular;  mil,  main 
lateral  line;  op,  opercular;  pcf,  pectoral  fin;  pif,  pelvic  fin;  pop,  preopercular;  pot,  posttemporal;  R,  radius;  subm,  submandibular 
series;  sll,  secondary  lateral  line;  su,  supradeithrum;  U,  ulna;  u,  ulnare;  unj.  lep,  unjointed  lepidotrichia. 


176         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  3.    ANSP  20980  in  part.  (A)  Photograph  of  specimen.  (B)  Labeled  drawing.  Boxed  area  refers  to  Figure  6. 


Immature  Rhizodontids  from  North  America  •  Davis  et  al.        177 


5  mm 


Figure  4.    ANSP  20981  in  visceral  view.  (A)  Photograph  of  specimen.  (B)  Labeled  drawing. 


178         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


makes  it  impossible  to  identify  the  rostral 
and  dorsal  margins  of  this  bone. 

Dentanj.  On  ANSP  20981,  a  left  den- 
tary  is  preserved  lateral  to  the  left  gular 
and  submandibulars  (Fig.  4).  The  distal 
portion  of  the  dentary  is  obscured.  A  series 
of  mesiodistally  oriented  striations  orna- 
ment the  labial  surface  of  the  dentary.  No 
sutures  are  \dsible  that  would  indicate  the 
presence  of  infradentary  bones,  nor  is  it 
possible  to  identify  coronoids  or  coronoid 
teeth.  Total  dentary  length  is  estimated  to 
be  approximately  20  mm. 

Four  incomplete  teeth  are  preserved  on 
the  dentary.  These  teeth  are  oval  in  cross 
section  and  are  buccolingually  com- 
pressed. The  largest  and  most  mesial  of 
the  four  is  a  parasymphysial  fang  (Fig.  4, 
f.  par).  Rhizodontid  teeth  are  generally  sig- 
moid in  shape  and  possess  lingual  stria- 
tions (see  Andrews,  1985;  Long,  1989). 
The  extreme  small  size  of  the  teeth  and 
state  of  preservation  make  it  difficult  to 
determine  whether  ANSP  20981  possesses 
these  tooth  characters.  The  dentaiy  of 
ANSP  20981  is  similar  to  that  ascribed  to 
PStrepsodus  anculonaniensis  (RSMGY 
1980.40.36  [Andrews  1985,  figs.  9b,  c])  in 
the  overall  proportion  of  the  dentary  and 
the  position  of  the  parasymphysial  fang. 

Extrascapular  Series.  An  incomplete 
median  extrascapular  is  the  only  cranial  el- 
ement that  can  be  identified  with  confi- 
dence on  ANSP  20980.  The  bone  is  rough- 
ly trapezoidal  in  shape,  narrowing  crani- 
omedially.  A  craniolaterally  directed  occip- 
ital commissural  canal  crosses  the  center 
of  the  median  extrascapular  (Fig.  5).  In 
Gooloogpngia  and  Bararneda,  only  a  small 
area  of  contact  is  present  between  the  me- 
dian extrascapular  and  the  postparietals 
(Johanson  and  Ahlberg,  1998,  figs.  2d,  f). 
It  is  not  possible  to  determine  the  nature 
of  this  contact  on  ANSP  20980  because 
the  rostral  margin  of  the  median  extra- 
scapular is  incomplete  and  postparietals 
are  not  preserved. 

Pectoral  Girdle.  The  articulation  be- 
tween the  dorsal  laminae  of  the  clavicle 
and  cleithrum  is  preserved  on  both  left 


and  right  sides  of  ANSP  20980  and  on  the 
right  side  of  ANSP  20981.  The  rostral  and 
caudal  margins  of  the  dorsal  lamina  of  the 
cleithrum  are  subparallel  to  each  other 
(Fig.  5).  This  condition  is  also  seen  in  the 
specimen  of  Sauripterus  described  by 
Daeschler  and  Shubin  (1998)  and  in  Goo- 
loogongia  (Z.  Johanson,  personal  commu- 
nication). In  other  rhizodontids  the  dorsal 
lamina  tends  to  narrow  at  midlength  be- 
fore expanding  to  meet  the  ventral  lamina. 

Rhizodontid  cleithra  possess  a  de- 
pressed flange  that  extends  along  the  cau- 
dal margin  of  the  dorsal  lamina;  this  flange 
is  absent  on  ANSP  20980  and  ANSP 
20981.  The  right  cleithrrun  associated  with 
the  fin  of  Sauriptenis  described  by  Daes- 
chler and  Shubin  (1998)  also  lacks  this 
flange,  as  does  that  of  Gooloogongia  (Z. 
Johanson,  personal  communication). 

The  cleithra  are  split  internally  between 
part  and  counterpart,  leaving  cancellous 
bone  exposed  in  many  places.  However, 
the  dorsal  lamina  of  the  right  cleithrum  is 
completely  preserved  in  internal  view.  The 
external  surface  is  exposed  at  the  intersec- 
tion of  the  dorsal  and  ventral  laminae. 
Both  the  internal  and  external  surfaces  are 
ornamented  with  subparallel  ridges  that 
extend  dorsoventrally  (Fig.  5). 

On  ANSP  20980  the  ventral  laminae  of 
the  right  clavicle  and  cleithrum  overlap 
those  of  the  left  as  a  result  of  postmortem 
inturning  and  compression  of  the  entire 
girdle  (Fig.  5).  In  ANSP  20981,  the  re- 
verse is  true  with  the  left  ventral  laminae 
of  both  the  cleithrum  and  clavicle  overlap- 
ping the  right.  The  lateromedially  directed 
ventral  contact  between  clavicle  and 
cleithnuTi  is  preserved  in  ANSP  20981 
(Fig.  4). 

An  interclavicle  lies  in  association  with 
the  ventral  laminae  of  the  clavicles  and 
cleithra  in  both  ANSP  20980  and  ANSP 
20981.  The  interclavicles  have  been  dis- 
placed dorsocaudally  from  the  position 
they  were  likely  to  have  occupied  in  life 
(Figs.  4,  5).  In  both  specimens  the  rostro- 
caudal  length  of  the  interclavicle  appears 
to  be  greater  than  that  of  the  ventral  cla- 


Immature  Rhizodontids  from  North  America  •  Davis  et  al.        179 


B 


5  mm 


Figure  5.     Shoulder  girdle  of  ANSP  20980  in  ventral  view.  (A)  Photograph  of  specimen.  (B)  Labeled  drawing. 


180         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


vicular  lamina.  This  condition  suggests  that  cleithrum  is  a  rectangular  bone  that  con- 
the  interclavicle  may  have  been  incorpo-  tacts  the  posttemporal  rostrally  and  the 
rated  into  part  of  the  contact  between  ven-  rostrodorsal  margin  of  the  cleithrum  cau- 
tral  cleithral  laminae.  The  elongation  of  dally.  The  posttemporal  is  somewhat 
the  interclavicle  caudally  is  a  unique  con-  smaller  and  more  triangular  in  shape  than 
dition  that  is  not  seen  in  other  rhizodon-  the  supracleithrum.  The  posttemporal 
tids  or  sarcopterygians.  An  interclavicle  is  contacts  the  median  extrascapular  rostro- 
not  preserved  with  either  known  specimen  laterally  and  the  supracleithrum  caudally. 
of  San riptenis  (Hall,  1843;  Daeschler  and  The  anocleithrum  is  subdermal,  a  condi- 
Shubin,  1998),  making  it  impossible  to  de-  tion  shared  with  porolepiformes,  actinistia, 
termine  whether  the  elongation  of  the  in-  and  dipnoi  (Alilberg,  1989).  In  osteolepi- 
terclavicle  is  a  characteristic  of  ANSP  formes  (e.g.,  Eusthenopteron  [Jarvik, 
20980  and  ANSP  20981  only  or  o£  Saurip-  1980])  the  anocleithrum  contacts  the  su- 
teni.s  in  general.  ANSP  20981  is  also  un-  pracleithrum  rostrally  and  the  cleithmm 
usual  in  possessing  cleithra  that  meet  at  caudally,  preventing  contact  between  the 
the  ventral  midline,  lending  further  sup-  supracleithrum  and  cleithrum. 
port  to  the  possibility  that  the  interclavicle  Paired  Fins.  In  ANSP  20980,  the  lead- 
was  fused  to  the  symphysis  of  the  cleithra.  ing  edge  of  the  pectoral  fin  forms  a  gentle 
Contact  between  the  ventral  cleithra  lam-  arc,  with  the  greatest  degree  of  curvature 
inae  is  also  preserved  in  the  adult  Saiirip-  at  midlength  (Fig.  6).  The  trailing  edge  of 
terus  specimen.  the  fin  is  composed  of  poorly  presei"ved 

On   ANSP   20980,    a  poorly  preserved  lepidotrichia  that  appear  jointed.  The  bulk 

right  scapulocoracoid  is  present  medial  to  of  the  fin  is  supported  by  lepidotrichia  that 

the  caudal  margin  of  the  broken  cleith-  are  unjointed  for  most  of  their  length.  The 

rum.  The  scapulocoracoid  is  preserved  as  lepidotrichia  are  arranged  in  two  layers, 

a  small  section  of  diaphanous  bone,  similar  one  forming  the  dorsal  surface  of  the  fin 

in  texture  to  the  endochondral  elements  of  and  one  forming  the  ventral  surface.  All 

the  pectoral  fin.  The  lack  of  any  diagnostic  endochondral  elements,  except  for  the  hu- 

morphology  on   the  scapulocoracoid  is  merus,   thus   are   enveloped   dorsally  and 

most  likely  due  to  the  ontogenetic  stage  of  ventrally  by  unjointed  lepidotrichia.  These 

the   specimen,   as   the   endochondral  ele-  layers  span  all  but  the  most  proximal  re- 

ments  of  the  pectoral  fin  are  also  weakly  gion  of  the  fin,  with  preaxial  lepidotrichia 

ossified  (see  below).  The  scapulocoracoid  extending  more  proximally  than  do  those 

appears    to    lie    dorsal    to    the    curvature  on  the  postaxial  edge. 

formed  by  the  intersection  of  the  dorsal  The  endochondral  elements  of  the  fin 

and  ventral  cleithral  laminae.  This  relative-  are  weakly  ossified;  the  central  region  of 

ly  dorsal  position  of  the  scapulocoracoid  is  each  element  consists  of  relatively  dense 

seen  in  other  rhizodontids  such  as  Strep-  bone  matrix,  whereas  the  cortical  regions 

sochis    (Andrews,    1985)    and    Sauriptems  are  thin  and  translucent.  The  five  elements 

(personal  observations).  In  osteolepids,  the  that  are  present  correspond  to  the  humer- 

scapulocoracoid   assumes   a   more  ventral  us,  radius,  ulna,  intermedium,  and  ulnare 

position  than  in  rhizodontids  and  rests  in  of  derived  sarcopterygians.  The  humerus 

the  curvature  formed  by  the  intersection  of  ANSP  20980  lacks  postaxial  processes, 

of  the  cleithral  laminae.  and  thus  differs  from  those  of  all  other  rhi- 

All  bones  of  the  supercleithral  series  are  zodontids.  The  radius  is  anteroposteriorly 

preserved  in  articulation  on  the  left  side  of  broader  than  the  ulna.  The  overall  pro- 

ANSP  20980.  Corresponding  elements  are  portions  of  the  radius  of  ANSP  20980,  rel- 

present  on  the  right  side,  but  are  disartic-  ative  to  the  ulna  and  humerus,  are  very 

ulated  and  partially  obscured  by  the  dorsal  similar  to  those  of  Sauripterus  (Daeschler 

lamina  of  the  right  cleithrum.  The  supra-  and    Shubin,    1998).    Other   rhizodontids. 


Immature  Rhizodontids  from  North  America  •  Dovis  et  al.        181 


5  mm 


Figure  6.     Left  pectoral  fin  of  ANSP  20980  showing  endoskeletal  and  dermal  elements.  (A)  Photograph  of  specimen.  (B)  Labeled 
drawing. 


182         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


5  mm 


Figure  7.    Comparison  of  the  pectoral  fins  of  (A)  ANSP  20980,  (B)  Sauripterus,  and  (C)  Barameda.  Barameda  modified  from 
Long  (1989). 


such  as  Barameda,  possess  a  radius  that  is 
narrower  than  the  ulna  (Fig.  7).  Further- 
more, a  relatively  narrow  radius  is  also 
seen  in  osteolepids,  including  derived  taxa 
such  as  Panderichthijs  (Vorobyeva  and 
Schultze,  1991).  Like  Barameda  and  Sau- 
riptenis,  the  ulnare  also  lacks  postaxial 
processes.  In  addition,  the  ulnare  and  in- 
termedium terminate  at  the  same  distal 
level,  a  feature  shared  with  Saiiriptenis, 
Barameda,  and  basal  tetrapods. 

The  richly  branched  series  of  preaxial 


radials  that  distinguish  the  fins  of  Bara- 
meda and  Sauripterus  are  not  obseived  in 
the  pectoral  fins  of  ANSP  20980.  Further- 
more, there  are  no  articulations  between 
any  of  the  endochondral  elements,  despite 
the  fact  that  all  bones  appear  to  be  pre- 
served in  situ.  The  distinct  separations  be- 
tween adjacent  endochondral  bones  may 
reflect  the  immaturity  of  the  specimens,  as 
all  bones  are  also  weakly  ossified.  The  lack 
of  distal  radials  may  also  be  attributed  to 
ontogeny  given  that  they  are  the  most  dis- 


Immature  Rhizodontids  from  North  America  •  Davis  et  al.        183 


tal  elements  of  the  fin.  If  ossification  of  the  the  preservation  or  ontogenetic  stage  of 

endoskeleton  proceeded  proximally  to  dis-  the  specimen  cannot  be  determined.  Rhi- 

tally,  then  distal  radials  may  not  have  os-  zodontids  may  have  exliibited  a  high  de- 

sified  by  this  stage.  ANSP  20981   repre-  gree  of  variation  in  the  timing  and  degree 

sents    a    smaller    individual    and,    indeed,  of  endochondral  ossification.  For  example, 

there  is  no  evidence  of  endochondral  os-  Foulden  rhizodontids  Strepsodus  and  Rln- 

sification  in  either  pectoral  fin.  The  entire  zodus  show  variation  in  the  degree  of  os- 

fin  is  composed  of  long,   unjointed  lepi-  sification  of  the  axial  skeleton  that  is  in- 

dotrichia.  The  absence  of  endochondral  el-  dependent  of  body  size, 
ements  may  be  due  to  lack  of  preservation.  Unpaired  Fins.  Vertebrae  and  the  pelvic 

but  it  suggests  that  ANSP  20981  may  be  girdle  are  not  preserved  and  presumably 

ontogenetically    younger     than     ANSP  were  unossified.  The  central  lobe  of  the 

20980.  Both  specimens  indicate  that  ossi-  caudal  fin  contains  a  linear  series  of  in- 

fication  of  the  fin  dermal  skeleton  preced-  completely    developed    centra    (Fig.    3B). 

ed  that  of  the  fin  endoskeleton.  These   ossifications  cover  the  dorsal  and 

The  pectoral  fins  of  ANSP  20980  are  ventral  surfaces  of  small  impressions  in  the 

disproportionally  large  for  a  sarcopterygi-  central  axis  of  the  fin.  Although  lepidotri- 

an.  Ratios  of  fin  length  to  body  length  for  chia  are  present  for  both  the  epaxial  and 

ANSP  20980  can  be  compared  to  the  type  hypaxial  lobes  of  the  caudal  fin,  they  are 

of  PStrepsodus  anculonamensis  (RSMGY  incomplete  distally   Dorsal  and  anal  fins 

1980.40.36  [Andrews,  1985])  and  other  os-  are  not  preserved. 

teolepids.  The  proximodistal  length  of  the  Body  Scales.   Body  scales  are  split  be- 

pectoral  fin  of  Strepsodus  is  approximately  tween  part  and  countei-part  leaving  most 

15%  of  the  total  body  length  (50  mm  fin/  scales  exposed  in  internal  view.  Like  other 

345  mm  estimated  total  length).  This  ratio  rhizodontids,  cosmine  is  absent.  Scales  are 

is  not  unusual  for  a  sarcopterygian:  Eusth-  thin,  roughly  circular  in  shape,  and  have  a 

enopteron  (14.9%,  based  on  Jarviks  1980  series  of  bony  ridges  that  radiate  from  an 

reconstruction),  Osteolepis  (15.3%  [Jarvik,  unornamented    central    plateau    (Fig.    6). 

1980]),  and  Panderichthys  (16.5%,  based  Concentric   rings   of  bone   connect  these 

on  Vorobyeva  and  Schultzes  1991  recon-  ridges,  giving  the  surface  a  woven  appear- 

struction)    all    share    similar    proportions,  ance.  There  are  none  of  the  breaks  or  gaps 

ANSP  20980  has  a  pectoral  fin  that  is  near-  in  these  ridges  that  have  been  hypothe- 

ly  one  fourth  of  the  animal's  body  length  sized  to  be  the  growth  lines  described  for 

(62  mm  fin/254  mm  estimated  total  length,  other    species    such    as    Strepsodus    (An- 

or   24.4%).    When    corrected   for   body  drews,   1985).   Internally,  scales  possess  a 

length,  the  fin  surface  area  of  the  new  rhi-  fusiform  boss  with  the  rounded  caudal  end 

zodontid  is  2.4  times  that  of  Strepsodus.  underlying  the  growth  center.  The  sugges- 

The  type  of  PStrepsodus  anculonamensis  is  tion  has  been  made  that  these  bosses  are 

also  considered  to  be  an  immature  speci-  either  points  of  scale  attachment  to  un- 

men,  yet  its  fin  proportions  are  similar  to  derlying  tissues  or  structural  supports  for 

those  of  adult  rhizodontids,  as  well  as  oth-  the  nonoverlapping  part  of  the  scale  (An- 

er  sarcopteiygians.  The  proportionally  en-  drews,  1985). 

larged  fin  of  ANSP  20980  may,  in  part.  The  thin  scales  that  cover  the  ventral 
correlate  to  its  ontogenetic  stage,  but  may  and  dorsal  surfaces  of  the  pectoral  fin  con- 
also  be  a  unique  characteristic  of  either  form  to  the  shape  of  the  underlying  lepi- 
the  genus  Sauriptenis,  or  of  this  specimen,  dotrichia  without  any  sign  of  fracture.  The 

A  series  of  small,  unjointed  lepidotrichia  most  distal  fin  scales  extend  approximately 
are  the  only  pelvic  fin  elements  that  are  15  mm  beyond  the  distal  edge  of  the  in- 
preserved  (Fig.  3).  Whether  the  lack  of  en-  termedium  (approximately  three  fifths  of 
dochondral  elements  in  this  area  is  due  to  total  fin  length  from  base  to  tip).  This  pat- 


184         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


tern  of  overlap  contrasts  with  the  speci- 
men of  PStrepsodus  anculonamensis  de- 
scribed by  Andrews  (1985:  73)  where 
scales  extend  "almost"  to  the  fin  margin. 

Lateral  Lines.  Rhizodontids  are  highly 
derived  in  that  they  have  multiple  lateral 
line  canals.  On  ANSP  20980,  sensory 
pores  of  the  main  lateral  line  canal  extend 
along  the  dorsal  body  wall  from  the  cleith- 
rum  to  the  caudal  fin  (Figs.  2,  3).  These 
oval-shaped  pores  possess  no  discernible 
internal  morphology,  and  are  flanked  dor- 
sally  and  ventrally  by  elongate  ridges  of  el- 
evated bone.  Faint  traces  of  accessory  lat- 
eral line  canals  can  be  seen  along  the  scale 
rows  that  lie  dorsal  and  ventral  to  the  main 
lateral  line.  Although  no  sensory  pores  can 
be  identified,  accessory  lines  can  be  in- 
ferred from  the  presence  of  a  furrow  that 
runs  craniocaudally  along  the  center  of  the 
scale  rows  adjacent  to  the  main  line.  In- 
deed, this  furrow  corresponds  in  appear- 
ance to  the  accessory  lines  described  for 
Strepsodus  (Andrews,  1985,  fig.  5c).  The 
presence  of  multiple  lateral  lines  may  be  a 
synapomorphy  of  Rhizodontida,  as  all  rhi- 
zodontids for  which  articulated  scale  rows 
can  be  identified  (Sauriptenis,  Gooloogon- 
gia,  and  Strepsodus)  possess  accessory  lat- 
eral lines.  The  only  other  evidence  of  sen- 
soiy  structures  on  ANSP  20980  is  the  oc- 
cipital commissural  canal  on  the  median 
extrascapular. 

ONTOGENETIC  STATUS 

The  small  size  and  incomplete  ossifica- 
tion of  the  skeletons  suggest  that  ANSP 
20980  and  ANSP  20981  are  immature  in- 
dividuals. Indeed  these  features  account 
for  most  of  the  differences  between  the 
fins  of  ANSP  20980  and  ANSP  20981  and 
those  of  other  specimens  of  Sauripterus. 
These  differences  are  most  profound  in 
the  endochondral  portion  of  the  fin  skel- 
eton, where  these  elements  are  poorly  os- 
sified, lack  articulations  between  corre- 
sponding bones,  and  lack  any  processes.  In 
ANSP  20980  the  cortex  of  each  endochon- 
dral element  is  less  ossified  than  the  med- 
ullary regions.  Furthermore,  the  lack  of  ar- 


ticulations between  endochondral  ele- 
ments differs  greatly  from  other  rhizodon- 
tids; larger  specimens  of  Sauripterus  and 
Barameda  possess  well-defined  articula- 
tions between  all  endochondral  bones. 
Likewise,  the  absence  of  both  distal  radials 
and  a  postaxial  process  on  the  humerus 
may  be  ontogenetic  features  that  relate  to 
the  degree  of  ossification  of  the  specimen. 
All  rhizodontids,  and  virtually  all  sarcop- 
terygians,  have  postaxial  processes  on  the 
humerus.  In  addition,  all  rhizodontids  pos- 
sess numerous  preaxial  radials,  many  of 
which  are  richly  branched  (Fig.  7). 

The  degree  of  ossification  of  the  axial 
skeleton  could  also  be  used  to  assess  the 
ontogenetic  stage  of  the  new  specimens. 
In  ANSP  20980,  no  hemal  or  neural  arch- 
es are  observed  in  any  portion  of  the  axial 
skeleton.  Although  trunk  centra  are  absent 
in  the  caudal  fin,  there  are  the  impressions 
of  three  segmented  units,  whose  dorsal 
and  ventral  surfaces  are  ossified.  We  inter- 
pret these  ossifications  to  represent  par- 
tially ossified  ring  centra.  Ring  centra  are 
known  from  the  Foulden  material,  from 
Baranneda,  and  are  associated  with  the 
type  of  Sauripterus.  However,  axial  ossifi- 
cation does  not  always  correlate  to  body 
size.  Small,  presumed  immature,  individ- 
uals of  Rhizodus  and  Strepsodus  possess 
partially  ossified  neural  and  hemal  arches 
caudal  to  the  first  dorsal  fin.  Similarly,  the 
large  rhizodontids  described  from  Foulden 
do  not  possess  ossified  ring  centra  (An- 
drews, 1985).  The  complete  lack  of  neural 
arches,  hemal  arches,  and  caudal  fin  sup- 
ports, and  the  partially  ossified  caudal  ring 
centra  are  suggestive,  although  not  defin- 
itive, evidence  of  an  immature  condition. 

DISCUSSION 

The  discovery  of  immature  Sauripterus 
provides  new  material  for  hypotheses 
about  the  evolution  of  fin  development 
and  function  in  extinct  sarcopterygians. 
Three  stages  of  growth  are  currently 
known  for  fin  development  in  Sauriptenis. 
In  the  earliest  stage,  represented  by  ANSP 
20981,  unjointed  lepidotrichia  are  promi- 


Immature  Rhizodontids  from  North  America  •  Davis  et  al.        185 


iient  and  no  endochondral  ossifications  are  velopment  of  the  dermal  skeleton  seems  to 
present  in  the  fin.  In  a  later  stage,  such  as  occur  in  rhizodontids,  even  in  immature 
that  seen  in  ANSP  20980,  the  endochon-  forms.  The  dermal  skeleton,  both  within 
dral  skeleton  is  weakly  ossified  and  lacks  the  fin  and  across  the  entire  pectoral  girdle, 
the  distal  preaxial  radials  seen  in  adults,  is  well  ossified,  whereas  endochondral  ele- 
Adults,  such  as  those  of  Sauriptenis,  con-  ments  are  weakly  developed, 
tain  fins  with  pronounced  lepidotrichia  It  would  seem  paradoxical  that  the  ex- 
and  endochondral  radials.  The  endochon-  pansion  of  the  endochondral  radials  in  rhi- 
dral  skeleton  does  not  play  a  role  in  sup-  zodontids  is  correlated  with  the  origin  of 
port  and  locomotion  until  later  stages  of  large  and  unjointed  dermal  rays.  After  all, 
growth,  after  the  animal  reaches  a  body  the  endochondral  elements  would  not  in- 
size  of  at  least  25  cm.  By  the  time  the  an-  teract  with  the  substrate:  the  main  surfaces 
imal  is  an  adult,  dermal  and  endochondral  of  the  fin  would  be  entirely  defined  by  the 
fin  supports  are  both  greatly  expanded  and  lepidotrichia.  Why  expand  endochondral 
ossified.  Therefore,  the  ossification  and  skeletal  elements  that  do  not  seem  to  play 
elaboration  of  endochondral  fin  supports  a  direct  role  in  support  and  locomotion? 
may  correlate  with  the  functional  demands  The  answer  to  this  question  may  lie  in  the 
placed  on  these  large  predatory  fish.  fact  that  in  adult  Sauripterus  the  endo- 
This  emphasis  on  both  dermal  and  en-  chondral  bones  provide  surfaces  for  the  at- 
dochondral  elements  in  rliizodontids  is  an  tachment  of  muscles.  The  humerus  and  ra- 
unexpected  intermediate  condition  be-  dius,  in  particular,  contain  crests  and  pro- 
tween  ray-finned  and  lobe-finned  designs  cesses  for  muscles  that  presumably  would 
and  would  not  be  predicted  from  current  have  played  a  role  in  motions  at  the  shoul- 
models  of  dermal  fin  development.  Thor-  der  and  elbow.  The  enhancement  of  the 
ogood  (1991)  proposed  tliat  the  differences  endochondral  skeleton  in  rhizodontids 
between  ray-finned  and  lobe-finned  de-  niay  be  correlated  to  their  increased  role 
signs  are  due  to  a  heterochronic  shift  dur-  ^s  control  elements  for  the  dermal  fin  skel- 
ing  development.  The  relative  amounts  of  eton.  The  large  size  of  rhizodonts  and,  per- 
dermal  skeleton  and  endoskeleton  in  the  fin  ^^pg  aspects  of  their  locomotor  and  feed- 
are  hypothesized  to  relate  to  the  timing  of  j^g  strategies,  may  have  called  for  fins  with 
the  shift  between  an  apical  ectodermal  j^rge  surface  areas.  The  enlarged  surface 
ridge  and  apical  ectodermal  fold  during  ^rea  was  established  by  die  expansion  of 
early  fin  bud  development  (Fig.  8).  The  hy-  ^^g  dermal  fin  supports,  whereas  the  con- 
pothesis  suggests  that  ray-finned  fishes,  ^j-qJ  of  movements  was  provided  by  elab- 
such  as  teleosts,  have  an  early  shift  from  oration  of  the  endochondral  radials. 
ridge  to  fold,  leading  to  a  greater  propor- 
tion of  the  skeleton  being  of  dermal  origin.  ACKNOWLEDGMENTS 
A  developmentally  later  shift  from  ridge  to 

fold,  or  the  extreme  case  of  no  shift  what-  This  paper  is  dedicated  to  Fuzz  Cromp- 
soever,  would  result  in  an  appendage  that  ton  in  recognition  of  his  patlibreaking  syn- 
is  primarily  or  exclusively  endochondral  in  tliesis  of  experimental  morphology  and  ex- 
design.  The  new  specimens,  and  the  pre-  peditionary  paleontology.  We  would  fike  to 
viously  described  Sauripterus  fins,  repre-  thank  Doug  Rowe  for  many  years  of  dili- 
sent  a  mosaic  between  these  morphological  gent  excavation  at  Red  Hill,  C.  Frederick 
and  developmental  extremes.  Witli  an  ex-  Mullison  for  his  skillful  preparation  of  the 
tensively  developed  dermal  skeleton,  and  specimens,  and  Robert  Carroll  and  FUchard 
interleaved  endochondral  elements,  San-  Cloutier  for  their  generous  access  to  Eiisth- 
nptenis  does  not  fit  in  a  model  based  solely  enopteron  specimens  for  comparative  pur- 
on  comparisons  between  teleosts  and  de-  poses.  We  also  wdsh  to  thank  Zerina  Johan- 
rived  sarcopterygians.  Indeed,  a  great  de-  son  and  Farish  A.  Jenkins,  Jr.,  for  helpful 


186        Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


B 


-Time 


I 


Figure  8.  (A)  Transition  from  apical  ectodermal  ridge  (AER,  left)  to  apical  ectodermal  fold  (AEF,  right)  during  early  fin  devel- 
opment. Cross  section  along  proximodistal  axis.  (B)  "Clock  model"  of  heterochrony  and  phenotype.  A  developmentally  early 
transition  from  AER  to  AEF  would  result  in  an  "actinopterygian"  phenotype  (here  represented  by  the  pectoral  fin  of  Amia).  A 
developmentally  later  transition  from  AER  to  AEF  would  result  in  a  "sarcopterygian"  phenotype  (here  represented  by  Eusthen- 
opteron).  A  and  B  modified  from  Thorogood  (1991).  Fins  modified  from  Jarvik  (1980;  Early)  and  Andrews  and  Westell  (1970;  Late). 


discussions.  Kalliopi  Monoyios  provided 
editorial  assistance.  This  research  was  sup- 
ported by  the  Academy  of  Natural  Sciences 
of  Philadelphia  and  the  National  Science 
Foundation  (EAR  9628163  to  N.  H.  S.). 


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HOW  DO  MYSTICETES  REMOVE  PREY  TRAPPED  IN  BALEEN? 


ALEXANDER  J.  WERTH^ 

Abstract.  Mysticete  whales  trap  prey  in  a  sieve  of 
baleen,  the  structure  of  which  varies  in  such  param- 
eters as  the  number  of  plates,  their  overall  dimen- 
sions, and  the  number  and  density  of  hairlike  fringes 
that  form  on  the  medial  surface,  creating  filters  of 
different  mesh  size.  Many  prey  items  presumably  en- 
tangle in  the  mat  of  interwoven  fringes,  necessitating 
that  they  be  freed  for  oral  transport  and  swallowing. 
Although  the  tongue  is  commonly  implicated  in  such 
removal,  this  has  never  been  studied.  Three  hypoth- 
eses for  prey  release  are  presented:  mechanical  scrap- 
ing or  shaking  of  baleen  by  the  tongue,  shaking  of 
the  head  or  lips  to  dislodge  prey  with  the  aid  of  grav- 
ity, and  use  of  a  rapid  flushing  "backwash"  current  to 
draw  water  into  the  mouth  through  baleen.  Pre\d- 
ously  unpublished  data  on  mysticete  tongue  structure 
and  function  support  all  hvpotheses;  behavioral  ob- 
servations of  foraging  whales  and  morphologic  find- 
ings such  as  baleen  growth  and  wearing  also  aid  in 
their  evaluation.  All  three  mechanisms  are  likely  to 
be  used  depending  on  the  type  of  baleen  and  size, 
type,  and  density  of  prey. 

INTRODUCTION 

For  as  long  as  whales  have  been  distin- 
guished from  fishes,  the  role  of  baleen  or 
"whalebone"  in  trapping  prey  has  been 
recognized.  Indeed,  given  this  singular, 
highly  derived  tissue  s  unique  consti-uction 
and  arrangement  in  rows  of  serial  plates, 
baleen's  sievelike  function — filtering  large 
quantities  of  small  prey  from  high  volumes 
of  seawater — seems  obvious,  all  the  more 
so  with  cursory  examination  of  mysticete 
diet  and  foraging  behavior. 

Yet  for  all  that  has  long  been  known 
about  prey  capture  in  the  mammalian  sub- 
order Mysticeti  ("mustached"  whales),  one 
aspect  is  only  dimly  understood:  how  are 
entangled  prey  removed  from  the  filter  be- 
fore transport  and  deglutition?  The  tongue 


'  Department  of  Biology,  Hampden-Sydney  Col- 
lege, Hampden-Sydney,  Virginia  23943. 


is  commonly  implicated  in  this  function, 
but  this  is  a  grossly  inadequate  and  vague 
answer.  Because  of  manifest  logistical  lim- 
itations a  clear,  Jonahs-eye  view  inside  a 
live  whales  closed  mouth  is  unattainable. 
The  experimental  techniques  of  cineradi- 
ography and  electromyography  that  have 
greatly  elucidated  precise  mechanisms  of 
lingual  function  in  other  inammals  are,  re- 
grettably, inapplicable.  Hence  the  best 
(and  indeed  perhaps  only)  way  to  address 
this  question  is  to  rely  on  speculative  in- 
ference based  on  the  functional  anatomy 
of  the  tongue  and  associated  oral  struc- 
tures. This  paper  introduces  and  com- 
pares, on  the  basis  of  moiphological  and 
ecological  evidence,  three  hypotheses  con- 
cerning removal  of  trapped  prey  from 
mysticete  baleen. 

PREY  CAPTURE 

Before  proceeding  to  a  discussion  of 
plausible  prey  removal  mechanisins  it  is 
necessary  to  consider  briefly  the  mecha- 
nisms by  which  prey  are  captured.  Mysti- 
cetes  vary  dramatically  in  foraging  meth- 
ods. Variation  occurs  mainly  along  family 
lines,  and  is  reflected  in  the  baleen  itself 
as  well  as  in  other  oral  stiiictures  and  (con- 
comitantly) in  diet  and  foraging  ecology,  all 
of  which  have  consequences  for  prey  re- 
moval. 

Foraging  and  Diet 

Right  whales  (Balaenidae)  utilize  a  type 
of  suspension  feeding  similar  to  that  of 
more  primitive  vertebrates,  which  pump 
or  push  water  constantly  and  unidirection- 
ally  through  the  mouth  (Sanderson  and 
Wassersug,   1993).   Balaenid  skim  feeders 


Bull.  Mus.  Comp.  ZooL,  156(1):  189-203,  October,  2001 


189 


190         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


cruise  slowly  through  swarms  of  minute  ring  the  bottom  and  sucking  in  muddy  wa- 
zooplankton,  primarily  copepods,  amphi-  ter  from  which  prey  are  winnowed  (Klaus 
pods,  and  euphausiids  (Lowry  and  Frost,  et  al.,  1990;  Weitkamp  et  al.,  1992).  Ram 
1984;  Carroll  et  al.,  1987).  Skim  feeding  is  gulping  necessitates  forward  lunges  paral- 
inost  commonly  observed  at  the  oceans  lei  to  or  through  the  surface;  the  gray 
surface  (Watldns  and  Schevill,  1979;  Mayo  whale  can  feed  while  stationaiy.  In  both 
and  Mai-x,  1990),  yet  stomach  content  data  cases  prey  are  filtered  as  the  mouth  closes 
and  scratched,  muddy  rostra  indicate  that  to  expel  engulfed  water  (and,  in  the  gray 
skim  feeding  occurs  at  all  levels  of  the  wa-  whale,  sediment).  As  Pivorunas  noted 
ter  column,  including  the  bottom.  The  (1979),  baleen  does  not  actually  catch 
enormous  head,  constituting  one  third  of  prey;  it  merely  retains  prey  as  water  is  ex- 
an  adult  balaenid's  15-  to  20-in  length,  pelled  from  the  oral  cavity, 
functions  as  an  immense  plankton  tow  net  As  expected,  the  type,  size,  and  abun- 
(as  in  other  continuous  filter  feeders  such  dance  of  preferred  prey  correlate  with  for- 
as  manta  rays  and  whale  and  basking  aging  ecology.  For  example,  the  sei  whale 
sharks),  although  the  "seine"  is  not  pulled  (Balaenoptera  horealis)  occasionally  eats 
along  but  rather  propelled  by  the  whale's  schooling  fish  as  do  other  rorquals,  yet 
foiAvard  locomotion  at  leisurely  speeds  of  more  commonly  feeds  on  copepods  or  oth- 
approximately  4  km  per  hour  during  for-  er  zooplankton  and  hence  engages  in  skim 
aging  (Reeves  and  Leatherwood,  1985;  feeding  much  like  that  employed  by  ba- 
Carroll  et  al.,  1987;  Lowry,  1993).  A  con-  laenids  (Kawamura,  1974).  The  gray  whale 
stant  current  of  prey-laden  water  enters  primarily  uses  suction  to  ingest  benthic 
anteriorly,  passes  through  baleen  "racks"  macroinvertebrates  (e.g.,  gammarid  ani- 
on either  side  of  the  mouth,  and  exits  lat-  phipods,  inysids,  and  molluscs;  Murison  et 
eral  to  the  phaiyngeal  orifice  at  the  trailing  al.,  1984;  Nerini,  1984)  yet  has  been  ob- 
edge  of  the  lips.  Tiny  zooplankton  in  the  served  feeding  on  shoals  of  fish  in  luid- 
steady  stream  of  incurrent  water  are  water  (Sund,  1975).  Although  well-docu- 
caught  in  the  finely  fringed  baleen,  and  mented  ecological  partitioning  exists  with- 
field  obseiA/ations  suggest  that  right  whales  in  mysticetes,  opportunism  is  the  rule.  Var- 
{Euhalaena  glacialis)  graze  for  hours  with  iation  in  type,  size,  and  abundance  of  prey 
few  interruptions  for  breathing  or  closing  might  alter  the  behavior  of  prey  capture  as 
the  mouth  (Watkins  and  Schevill,  1979;  well  as  removal  of  trapped  prey  in  any 
Mayo  and  Mai'x,  1990),  leading  to  anec-  mysticete  species, 
dotal  speculation  that  they  may  spend  long 
periods     skimming     before     gathering  ^"^^   MOrpnoiogy 

enough  prey  to  swallow.  The  differences  between  continuous 
In  contrast,  other  mysticetes  are  not  and  intermittent  (ram  and  suction)  filter- 
continuous  filter  feeders  but  are  intermit-  feeding  inysticetes  are  manifested  not  only 
tent  filter  feeders  that  ingest  discrete  in  diet  but  more  aptly  in  key  features  of 
mouthfuls  of  water  and  separate  food  from  oral  anatomy.  Unlike  other  mysticetes,  ba- 
this  water  before  expelling  it.  A  single  laenids  possess  no  throat  grooves  yet  have 
mouthful  is  engulfed  either  by  ram  feed-  a  large  anterior  cleft  (the  subrostral  gap) 
ing  in  rorquals  (Balaenopteridae)  such  as  between  baleen  racks.  The  high,  arched 
fin  and  humpback  whales  (Jurasz  and  Jur-  skull  accommodates  extremely  long,  nar- 
asz,  1979;  Watkins  and  Schevill,  1979;  row  baleen  plates  (Fig.  1),  and  the  huge 
Hain  et  al.,  1982)  or  by  intraoral  suction  semicircular  lower  lips,  which  extend  far 
in  the  gray  whale  (E.schrichtiiis  rohustus,  above  the  mandible  (like  the  arched,  deep- 
Eschrichtiidae),  whose  tongue  is  rapidly  sided  lower  jaw  of  flamingos;  Milner, 
depressed  and  retracted  to  expand  the  oral  1981),  cover  the  baleen  laterally  and  en- 
cavity  and  create  negative  pressure,  stir-  fold  the  narrow  rostrum  when  the  mouth 


Mysticete  Prey  Removal  •  Werth 


191 


Figure  1.  Baleen  size,  shape,  and  fraying  correlate  with  prey  type  and  size.  Right  whales  (top)  skim  microplankton  with  narrow, 
finely  fringed  baleen  >4  m  in  length.  Rorquals  (center)  gulp  schooling  shrimp  and  fish  with  shorter  (<  1  m),  wider,  coarser  baleen. 
The  gray  whale  (bottom)  sucks  in  benthic  invertebrates  and  filters  them  with  short  (<40  cm),  coarsely  fringed  baleen. 


is  closed.  Like  the  subrostral  gap,  the  or- 
olabial  sulcus — a  gutterlike  groove  medial 
to  the  lip — promotes  continuous,  unidirec- 
tional flow  as  filtered  water  passes  to  an 
"exliaust  port"  at  each  lip's  trailing  edge, 
lateral  to  the  phaiyngeal  opening.  The 
tongue  is  firm,  muscular,  and  extraordi- 
narily large;  it  is  estimated  to  average  4- 
6%  of  total  body  mass  (Omura,  1958),  so 
that  in  a  standard  50-ton  or  50,000-kg 
whale,  the  tongue  weighs  2,000-3,000  kg 
and   measures   several   meters   in   length. 


Ceivical  vertebrae  are  fused,  yet  the  man- 
dibular symphysis  is  loose  and  the  lips 
highly  mobile,  controlled  by  labial  mus- 
culature (Lambertsen  et  al.,  1989).  The 
gray  whales  tongue  is  also  firm  and  mus- 
cular and  this  whale  has  a  small  subrostral 
gap,  although  this  is  far  less  pronounced 
than  the  gap  found  in  balaenids  (Wolman, 
1985).  The  scarred,  abraded  jaws  of  Es- 
chrichtiiis  disclose  its  benthic  suction 
feeding,  as  do  mud  plumes  trailing  behind 
feeding  whales  and  suction-generated  pits 


192         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


that  scar  the  ocean  floor  (Oliver  and  Slat-  filter  itself  varies  substantially  in  numerous 

tery,  1985;  Nelson  and  Johnson,  1987).  ways    (Fig.    1),   including  the   number  of 

Likewise,  rorquals  possess  singular  mor-  flexible  triangular  laminae  or  plates  in  each 
phologic  features  for  lunge  feeding.  Posi-  rack,  which  ranges  from  100  in  Eschri- 
tive  inertial  pressure  opens  the  mouth  just  chtius  to  480  in  the  fin  whale  (Balaenop- 
as  a  bag  is  opened  by  pulling  it  through  tera  physalus),  although  the  bowhead  (Ba- 
air;  water  and  prey  are  passively  enveloped  laena  niysticetus)  and  most  large  rorquals 
rather  than  displaced  forward  or  sucked  generally  have  about  300—350  plates  per 
internally  (Orton  and  Brodie,  1987).  Key  rack  (Leatherwood  et  al.,  1983).  Plates  are 
innovations  include  the  flaccid  and  de-  arranged  transversely  like  teeth  of  a  comb 
formable  tongue  and  oral  floor  with  inter-  and  suspended  from  the  maxillae  at  inter- 
muscular fascial  cleft;  the  cavum  ventrale,  vals  of  roughly  1  cm.  Plates  are  generally 
which  receives  engulfed  water  and  the  dis-  only  a  few  millimeters  thick  (anteroposte- 
placed  baglike  tongue  (von  Schulte,  1916;  riorly)  yet  vary  greatly  between  species  in 
Pivorunas,  1979);  accordionlike  longitudi-  other  dimensions,  notably  length,  measur- 
nal  throat  pleats  and  elastic  throat  wall  ing  just  5—25  cm  in  Eschrichtius  yet  often 
(Orton  and  Brodie,  1987);  wide-opening  exceeding  4  m  in  Balaena  (requiring  that 
jaws  with  locking  temporomandibular  joint  they  fold  posteriorly  as  the  mouth  closes), 
to  prevent  opening  during  rapid  locomo-  However,  baleen  seldom  grows  wider  than 
tion  and  frontomandibular  stay  to  store  Id-  35  cm  in  any  species,  so  that  the  shape  of 
netic  energy  for  jaw  closure  (Lambertsen,  the  triangle  varies  markedly.  Baleen  also 
1983;  Lambertsen  et  al.,  1995);  unfused  differs  in  such  characteristics  as  latero- 
mandibular  symphysis  with  fibrocartilage  medial  curvature  (Lambertsen  et  al., 
arms  extending  to  mandibular  raiui  (Pivo-  1989),  flexibility  (very  stiff  in  Eschrichtius; 
nanas,  1977);  and  flat,  streamlined  rostrum  said  to  be  most  pliable  in  the  pygmy  right 
(Gaskin,  1976).  Storro-Patterson  (1981)  whale,  Caperea  niarginata;  Leatherwood 
speculated  that  a  blue  whale  (Balaenop-  et  al.,  1983),  and  less  consequential  factors 
tera  musculus)  might  engulf  1,000  tons  of  such  as  color,  although  the  latter  may  re- 
water  in  a  single  gulp.  Pivorunas  (1979)  late  to  prey  capture,  as  has  been  supposed 
gave  a  more  conservative  estimate  of  at  for  jaw  and  flipper  color  (Mitchell,  1970; 
least  60  m^  (approximately  70  tons)  of  wa-  Brodie,  1977). 

ter,  still  a  huge  amount  of  water  equal  to  Certainly   most   significant   from   the 

roughly  50%  of  a  blue  whale  s  total  body  standpoint  of  prey  retention  is  the  varia- 

volume.   Lambertsen  s  recent  calculations  tion  in  type  and  density  of  baleen  fringes, 

from    computer    modeling    (Zackowitz,  Although  the  plates  themselves  form  a  sort 

2000)  suggest  an  almost  identical  engulf-  of  rudimentary  sieve,  the  true  task  of  fil- 

ment  voluine  of  15,000  gallons  (56.85  m^)  tration  is  accomplished  by  the  many  thin, 

in    humpbacks.    Specialized   behaviors   of  hairlike  projections  that  develop  on  each 

rorqual  lunge  feeding,  including  ingenious  plate's  medial  side,  forming  a  network  of 

bubble  entrapment  devices  einitted  by  the  meshed  fibers  (Tomilin,  1957;  Williamson, 

blowholes  (Gormley,  1983;  Wiirsig,  1988)  1973).  All  baleen  develops  as  a  dermal— 

or   lobtailing,    flipper   slapping,    and   flick  epidermal    interaction    in    which    conical 

feeding  to  concentrate  prey  (Evans,  1987;  dermal  papillae  extend  ventrally  from  an 

Clapham  et  al.,  1995),  are  as  remarkable  underlying  basal  plate  of  connective  tissue 

and  resourceful  as  the  mechanics  of  en-  through  an  epidermal  layer,  at  which  time 

gulfment.  the  papillae  are  enveloped  in  a  homy  layer 

of  keratin  to  form  long  bristles  called  horn 

°^'®®"  tubes  (Slijper,  1962).  These  tough,  fibrous 

More  important  than  these  divergences  strands  are  likewise  surrounded  and  ce- 

in  oral  morphology  and  ecology,  the  baleen  mented  together  by  a  layer  of  compacting 


Mysticete  Prey  Removal  •  Werth        193 


horn,  while  a  soft  cushioning  layer  of  in- 
termediate horn  provides  a  dense  cortex 
covering  the  anterior  and  posterior  faces 
of  the  plate.  Friction  abrades  the  matrix 
medially,  wearing  away  compacting  horn 
to  reveal  the  hollow  horn  tubes  that  re- 
main as  the  frayed  fibers  comprising  the 
sieving  apparatus,  whereas  the  long  side  of 
the  scalene  triangle  facing  the  lip  remains 
smooth.  Cells  in  the  rubbery,  pliant  epi- 
thelium of  the  guins  anchor  baleen  to  the 
palate  and  proliferate  to  replenish  abraded 
gingival  tissue,  just  as  all  papillae  grow  at 
a  uniform  rate  to  replace  worn  horn  tubes. 
The  visible  portions  of  baleen  consist  ex- 
clusively of  dead  comified  cells,  but  the 
dermal  process  remains  a  living  tissue,  so 
that  baleen  is  analogous  to  the  part-living 
tissue  in  an  ungulate  hoof  (Slijper,  1962). 
Baleen's  anisotropic  nature,  with  a  homo- 
geneous cortical  layer  surrounding  free, 
hollow,  cylindrical  tubes,  affords  maximal 
strength  with  minimal  mass  (Slijper,  1962). 
Baleen  is  tough  yet  elastic,  a  suitable  ma- 
terial to  meet  the  demands  of  constant 
friction.  Sadly,  the  exceptional  physical 
characteristics  of  this  material  also  ren- 
dered it  an  extremely  valuable  commodity 
that  fueled  the  whaling  industry. 

The  hairlike  bristles  that  fray  on  the  me- 
dial side  intertwine  to  form  a  fibrous  mat. 
The  slender,  springy  plates  of  the  sldm- 
feeding  balaenids  and  sei  whale  possess 
35—70  fine  filainentous  fringes  per  square 
centimeter  (Leathei-wood  et  al.,  1983).  Mi- 
croscopic examination  of  bowhead  baleen 
reveals  several  distinct  histologic  units,  in- 
cluding simple  (bristle)  and  compound 
(hair)  filaments,  according  to  their  gingival 
origin  (Haldiman  et  al.,  1981;  Haldiman 
and  Tarpley,  1993).  In  contrast,  fibers  of 
rorqual  and  gray  whale  baleen  are  luuch 
shorter,  coarser  (thicker  in  diameter),  and 
fewer  in  overall  number  and  density 
(about  30  fringes  per  plate;  Watson,  1981); 
they  are  inore  like  rough  scrub-bioish  bris- 
tles than  fine  hairs,  and  are  typically  more 
wavy  than  the  fine  strands  of  skim  feeders. 
However,  these  rough  bristles  are  suffi- 
ciently long  that  they  may  link  with  other 


fibers  from  the  same  and  adjacent  plates 
to  form  an  interwoven,  loosely  braided 
mesh.  In  a  mathematical  model  correlating 
plate  and  fringe  features,  Pivorunas  (1976) 
suggested  that  the  angle  at  which  fringes 
develop  from  the  medial  surface  seems 
more  critical  for  prey  retention  than  fringe 
density,  and  that  shorter  fringes  alleviate 
drawbacks  of  having  fewer  fringes.  Where 
plates  angle  laterally,  as  in  rorquals  (Fig. 
2),  many  fringes  are  exposed  on  the  medial 
surface  by  friction,  so  that  the  coarse  fibers 
in  this  tangled,  brushlike  mat  need  not 
have  such  siuall  diameter,  whereas  in  ba- 
laenids fewer  fringes  can  be  exposed  on 
the  relatively  straighter  medial  side.  In  any 
event  the  most  fundamental  distinction 
between  baleen  of  different  species  is  the 
spacing  between  fringes,  and  thus  the  po- 
rosity of  the  filter. 

Because  baleen  is  not  a  rigid  material, 
its  filter  porosity  varies  according  to  hy- 
drodynamic  factors  such  as  the  swimming 
velocity  of  ram  feeders;  size  and  density  of 
retained  prey;  and  direction,  rate,  and 
pressure  of  water  flow  (Sanderson  and 
Wassersug,  1990).  The  mysticete  filter- 
feeding  apparatus  acts  simply  as  a  sieve — 
no  active  adjustment  of  filter  porosity  ac- 
cording to  prey  size  or  density  is  made  be- 
fore engulfment — ^with  filter  elements  (ba- 
leen fringes)  spaced  inore  closely  than  the 
sizes  of  items  to  be  captured.  However,  al- 
though no  particles  are  directly  intercept- 
ed by  adhering  to  a  stick)'  surface,  it  is  pos- 
sible although  unlikely  that  tiny  prey 
(smaller  than  the  filter  spacing)  may  be 
trapped  by  other  methods  of  aerosol  filtra- 
tion, such  as  inertial  impaction  or  gravita- 
tional deposition  (Rubenstein  and  Koehl, 
1977).  Although  small  suspension  feeders 
must  contend  with  the  constraints  inher- 
ent in  moving  in  a  dense,  viscous  fluid, 
mysticete  filtration  may  depend  more  on 
inertial  forces  that  prevail  at  high  Reynolds 
numbers  (Vogel,  1994). 

Baleen  whales  consume  whole  organ- 
isms, whereas  small  filtering  organisms  of- 
ten feed  on  detritus  (fragiuented  organic 
debris;  Sanderson  and  Wassersug,   1993). 


194         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


rostrum 


baleen 


gular  groove 


Figure  2.  Diagrammatic  cross  sections  through  the  closed 
mouth  of  a  right  whale  (top),  rorqual  (middle),  and  gray  whale 
(bottom),  showing  the  different  dimensions  and  relations  of  oral 
features  (baleen,  lips,  tongue,  and  mouth  floor)  that  affect  prey 
prehension  and  extrication  in  these  families. 


Yet  as  with  other  suspension  feeders,  mys- 
ticetes  feed  in  abbreviated  trophic  chains 
and  thus  reap  great  energy  input,  a  critical 
factor  in  their  attainment  of  huge  body 
size  and  (before  their  decimation  by  hunt- 
ing) wide  distribution.  Each  whale  con- 
sumes gigantic  quantities  of  prey,  with  es- 
timates  ranging   from   200-1,000   kg  per 


meal  and  200,000-600,000  kg  annually 
(Gaskin,  1982).  Like  other  strainers  mys- 
ticetes  are  not  selective;  they  locate  patchy 
food  sources  and  trap  whatever  is  there. 
Although  the  filter  porosity  determines  the 
smallest  prey  retained,  fine  filters  catch 
large  prey  as  well  as  small  and  hence  may 
be  more  versatile  (Gaskin,  1982).  Howev- 
er, dietary  studies  indicate  that  coarse- 
fringed  mysticetes  are  less  selective  (Nem- 
oto,  1959,  1970),  ingesting  items  ranging 
from  plankton  and  fish  to  hapless  seabirds, 
whereas  balaenids  are  specialized  feeders 
with  more  restrictive  diets.  In  fact,  it  may 
be  unnecessarily  costly  to  use  a  finer  filter 
than  is  needed  to  trap  preferred  prey,  par- 
ticularly during  continuous  filtration,  be- 
cause this  increases  pressure  drag,  slowing 
an  animal  and  preventing  capture  of  large 
or  evasive  prey.  Watkins  and  Schevill 
(1976)  noted  that  the  water  level  inside 
the  mouth  of  a  right  whale  during  surface 
skim  feeding  is  higher  than  that  of  the  sur- 
rounding sea  (although  gravity  would  then 
force  water  out  through  baleen).  A  pho- 
togrammetric  study  of  bowhead  baleen 
curvature  by  Lambertsen  et  al.  (1989)  sug- 
gested that  hydrodynamic  rather  than  pas- 
sive hydraulic  forces  may  develop,  creating 
Bernoulli  and  Venturi  effects  within  the 
mouth  to  improve  filtering  efficiency. 
Werth  (1995)  devised  mathematical  and 
physical  models  of  the  bowhead  mouth  to 
test  these  predictions  and  confirmed  that 
both  hydrodynamic  effects  might  reduce 
turbulent  flow  and  avoid  creation  of  an  an- 
terior pressure  wave  so  that  balaenids 
could  capture  elusive  prey  even  at  slow 
swimming  speeds.  Foraging  in  tight  for- 
mation may  achieve  the  same  effect  (Wiir- 
sig,  1988,  1989). 

PREY  REMOVAL 

The  process  of  prey  removal  from  the 
mysticete  filter  is  an  intriguing  question 
that  has  not  yet  been  satisfactorily  ad- 
dressed, much  less  resolved.  Given  the 
fine  porosity  of  the  filter  (because  it  in- 
volves baleen  strands  rather  than  simple 
laminae)  in  all  species  and  the  small  prey 


Mysticete  Prey  Removal  •  Werth        195 


size  of  many  species,  prey  may  become 
trapped  not  only  on  but  actually  in  this  fil- 
ter, necessitating  that  they  be  freed  before 
they  can  be  swallowed. 

Consider  an  analogy  with  a  dip  net  used 
to  clean  a  swimming  pool.  One  way  to  re- 
move debris  that  accumulates  on  the  net 
would  be  to  scrape  the  mesh  or  einploy 
some  other  direct  mechanical  means  to 
brush  off  collected  material.  Alternatively, 
the  net  might  be  shaken  vigorously  so  that 
debris  falls  off  with  the  aid  of  gravity.  A 
third  method  relies  on  hydrodynamic  rath- 
er than  mechanical  forces:  by  rapidly  jerk- 
ing the  net  backwards,  a  backwash  flow 
would  filter  through  the  net  and  free 
trapped  items.  Undoubtedly  additional 
ways  exist  to  clean  the  net,  yet  these  are 
the  simplest  and  most  obvious  methods. 

Just  as  a  clogged  dip  net  must  be 
cleaned  periodically  for  effective  filtration, 
so  too  the  baleen  sieve  must  be  cleared  for 
it  to  continue  removing  planktonic  or  nek- 
tonic  prey  from  ingested  water.  Clearly  the 
mysticete  filter  is  more  complex  than  a  dip 
net  screen,  for  its  pore  size  is  not  fixed  and 
is  likely  pressure  dependent.  Although 
only  continuous  skimmers  appear  routine- 
ly to  ingest  items  small  enough  to  be  deep- 
ly ensnared  in  fringes  (i.e.,  copepods  1—5 
mm  in  length),  the  rapid,  explosive  expul- 
sion of  water  in  intermittent  filter  feeders 
might  serve  to  drive  prey  further  into  the 
meshwork  of  fringes,  as  a  huge  volume  of 
water  exits  the  mouth  at  high  velocity  and 
pressure.  Still,  the  relationship  between 
filter  element  spacing  and  prey  size  in 
most  intermittent  filter  feeders — namely 
their  coarser  fringes  and  attendant  trend 
toward  larger  prey  ( 10-  to  50-cm  schooling 
fish  and  squid) — means  that  much  of  their 
food  accumulates  on  rather  than  within 
the  sieve  during  collection  (and  is  unlikely 
to  penetrate  it  during  water  expulsion).  Yet 
euphausiids  (10  cm)  are  a  favored  prey  of 
most  rorquals  and  the  gray  whale  eats 
many  small  invertebrates  (1-15  cm),  all  of 
which  could  easily  become  enmeshed  in 
fringes.  Clearly,  ingestion  of  any  prey 
(large  or  small)  in  large  quantities  would 


mean  that  many  items  (not  all,  yet  enough 
to  be  swallowed)  simply  fall  onto  the 
tongue  upon  water  expulsion.  Also,  most 
macroscopic  prey  are  negatively  rheotropic 
(i.e.,  preferring  to  swim  against  a  current); 
if  still  alive  they  will  attempt  to  swim  away 
from  the  expulsive  flow,  out  of  the  ensnar- 
ing mesh  and  into  the  center  of  the  mouth. 

Baleen,  unlike  some  dip  nets,  is  not 
meant  to  gather  debris,  although  Eschri- 
cJitius  might  be  expected  occasionally  to 
collect  sediment  along  with  intended  prey 
from  the  benthic  substrate.  Inorganic  ma- 
terial must  be  removed  from  the  filter  so 
as  to  prevent  clogging  of  the  baleen,  as 
well  as  separated  froin  food  so  as  to  pre- 
vent its  ingestion,  although  sand  and  peb- 
bles have  been  found  in  gray  whale  stom- 
achs (Tomflin,  1954;  Pike,  1962).  Unfor- 
tunately, although  baleen  could  easily  be- 
come fouled  with  spilled  oil  (Geraci  and 
St.  Aubin,  1990;  Loughlin,  1994),  this  ma- 
terial is  unlikely  to  be  removed  effectively 
by  any  means,  such  that  not  only  the  toxic 
effects  of  its  ingestion  but  also  the  obvia- 
tion  of  filtration  would  pose  dire  conse- 
quences for  all  mysticetes. 

The  combination  of  coarse  brushlike  ba- 
leen and  large  prey  commonly  ingested  by 
rorquals  means  that  their  food  is  far  less 
likely  to  become  entangled  than  in  species 
with  fine  fringes  and  correspondingly 
smaller  prey,  particularly  sei  and  right 
whales.  The  large  prey  of  intermittent  fil- 
ter feeders  might  simply  fall  onto  the 
tongue  or  swim  out  of  baleen  without  need 
of  any  removal  mechanisms.  Accumula- 
tions of  minute  prey  might  also  drop  in 
this  manner,  leaving  some  organisms  re- 
maining in  the  baleen  yet  creating  a  suf- 
ficiently large  bolus  to  be  swallowed.  Re- 
current dislodging  of  enmeshed  items,  es- 
pecially tiny  prey,  may  be  metabolically 
costly.  However,  such  costs  must  be  bal- 
anced with  the  need  for  periodic  baleen 
cleaning  to  present  the  freest,  least 
clogged  filter  for  optimal  prey  capture  and/ 
or  to  preclude  swallowing  of  too  large  a 
bolus  or  too  thick  a  slurry  of  prey.  Do  mi- 
croplankton  that  gather  on  gill  rakers  of 


196         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


filter-feeding  sharks  eventually  migrate  to  lateral — that  could  abrade,  shake,  or  oth- 
the  pharynx  in  similarly  large  masses?  As  erwise  disturb  or  wear  the  mat  of  inter- 
with  mysticetes,  the  act  of  filtration  has  re-  woven  fringes  and  thereby  release  entan- 
ceived  inuch  more  attention  than  the  topic  gled  prey.  According  to  this  idea,  prey  ei- 
of  how  collected  prey  are  processed  in-  ther  fall  onto  the  tongues  central  furrow 
traorally.  However,  even  if  large  prey  and  and  are  subsequently  transported  to  the 
accumulated  small  prey  drop  off  baleen  rear  of  the  oral  cavity  for  swallowing  via 
spontaneously,  small  prey  clearly  become  lingual  elevation  and  retraction  and  de- 
enmeshed  in  the  filter,  necessitating  that  pression,  or  else  prey  removal  and  trans- 
they  be  removed  for  transport  and  swal-  port  steps  occur  concurrently  with  such 
lowing  (as  well  as  to  restore  the  filters  po-  lingual  movements,  perhaps  in  a  cyclic  se- 
rosity  and  efficiency).  ries  controlled  by  a  central  pattern  gen- 

By  extension  from  the  dip-net  analogy,  erator. 
I  propose  three  hypotheses  to  explain  the  A  major  drawback  of  this  mechanism  is 
most  likely  mechanisms  for  removal  of  that  the  tongue  might  push  prey  more 
prey  trapped  in  baleen  fringes.  Two  are  deeply  into  fringes,  furthering  entangle- 
mechanical — direct  dislodging  of  items  via  ment.  Other  potential  disadvantages  in- 
lingual  scraping  and  indirect  release  by  elude  inefficient  clearing  of  prey  from 
vigorous  head  shaking,  whereas  one  is  hy-  fringes  that  do  not  directly  contact  the 
drodynamic,  relying  on  a  powerful,  rapid  tongue  as  well  as  rapid  abrasion  and,  ulti- 
reversed-flow  backwash  to  flush  items,  mately,  removal  of  baleen.  Baleens  occa- 
These  options  need  not  be  mutually  exclu-  sional  presence  in  whale  feces  is  offered  as 
sive:  a  species  might  use  all  three  process-  evidence  that  it  regularly  wears  away,  pro- 
es  to  "cleanse  the  palate"  depending  on  viding  compelling  circumstantial  support 
prey  type  and  density  or  other  circum-  for  this  hypothesis.  Isotopic  studies  of 
stances.  Additionally,  the  extent  to  which  bowhead  baleen  confirm  that  its  growth 
individuals  might  devise  unique  methods  varies  with  age  (Schell  and  Saupe,  1993), 
of  prey  removal  ought  not  to  be  discount-  exceeding  50  cm  of  growth  in  the  first  year, 
ed.  then  decreasing  by  about  10  cm  per  year 

Although  no  discussion  of  baleen  clean-  until  stabilizing  at  about  20  cm  or  less  in 

ing  has  been  published  previously,  super-  older  animals.  Whether  the  bowhead s  an- 

ficial  references  implicate  the  tongue  in  nual  addition  of  this  much  baleen  is  suf- 

passing.  Indeed  the  tongue  plays  a  central  ficient  to  offset  potential  loss  from  abrasive 

role  in  two  of  the  baleen  cleaning  strate-  prey  removal  can  only  be  addressed  in  the- 

gies  presented  and  analyzed  here  on  the  ory.  Yet,  although  abrasion  might  be  hy- 

basis  of  anatomical  and  observational  evi-  pothesized  to  be  reduced  in  nonsldmming 

dence.  Specifically,  those  mechanisms  in-  mysticetes  that  need  not  release  tiny  prey 

volving  the  tongue  depend  predominantly  from    fine    fringes,    Ruud's    (1940,    1945) 

on    changes    in    its    position    rather   than  studies  of  fin  whale  baleen  growth  provide 

shape,  which  is  supported  by  preliminary  data  comparable  to  those  from  bowheads, 

study  of  lingual  myology.  suggesting  a  constant  level  of  abrasion  not 

correlated  with  diet  and  foraging  method. 

Prey  Removal  Via  Direct  Lingual  Scraping  ^  more  serious  fault  of  this  fine  of  rea- 

or  bnaKing  soning   is    that   lingual    scraping   would 

The  most  common  supposition  is  that  abrade  baleen's  medial  surface  far  more 

the  tongue  is  applied  directly  to  scrape  ba-  than  its  lateral  surface,  resulting  in  differ- 

leen  and  free  trapped  items.  Although  this  ential  wear  and  continually  narrowing 

is  mainly  presumed  to  involve  lingual  ele-  plates.  However,  not  only  does  plate  shape 

vation  and  retraction,  it  might  entail  any  not  change  with  age,  but  growth  is  uni- 

motion- — anteroposterior,  dorsoventral,  or  form  along  the  entire  base  of  the  plate 


Mysticete  Prey  Removal  •  Werth        197 


(Ruud,  1940,  1945),  so  that  such  differ- 
ential wear  could  not  be  countered  by  dif- 
ferential growth.  Nor  could  baleen  be 
scraped  solely  from  below  to  wear  evenly, 
because  baleen  angles  laterally  in  all  mys- 
ticetes  and  the  tongue  contacts  only  its 
medial  surface  (Fig.  2).  Still,  support  for 
the  lingual  scraping  hypothesis  might 
come  from  anotlier  type  of  differential  ba- 
leen wear  seen  in  gray  whales:  they  seem 
predominantly  right  handed,  with  signifi- 
cantly shorter  baleen  on  this  side  (Kasuya 
and  Rice,  1970).  This  asymmetry  has  been 
ascribed  to  friction  from  benthic  suction 
ingestion  on  the  right  side  (head  scarring 
and  barnacle  placement  are  likewise  asym- 
metrical), yet  the  wear  might  be  incurred 
not  during  prey  capture  but  during  sub- 
sequent scraping  removal  of  prey  and  sed- 
iment that  is  trapped  chiefly  in  the  right 
rack. 

The  effect  of  such  scraping  on  the 
tongue  must  also  be  considered,  and  at 
least  in  the  case  of  Balaena  the  dorsum  is 
covered  by  a  thick,  keratinized  stratified 
squamous  epithelium  with  a  well-devel- 
oped stratum  comeum  (Tarpley  1985; 
Haldiman  and  Tarpley,  1993).  A  homy, 
cornified  corium  is  similarly  present  on  the 
tongue  of  Euhalaena  (Werth,  1990,  1993), 
yet  no  data  are  available  for  other  mysti- 
cetes.  Unfortunately,  although  compara- 
tive mysticete  lingual  myology  would  shed 
light  on  the  ability  of  the  tongue  to  per- 
form the  movements  necessaiy  for  the 
scraping  motions  outlined  above,  few  pub- 
lished data  exist. 

The  lingual  inovements  necessary  for 
this  manner  of  prey  removal  involve 
changes  in  the  tongue's  position  rather 
than  its  shape.  Use  of  the  human  tongue 
to  remove  food  particles  trapped  between 
teeth  or  on  the  palate  is  familiar.  Yet,  al- 
though the  mysticete  tongue  might  deform 
to  shorten  or  curl  and  thereby  contact  lo- 
calized regions  of  baleen,  it  is  likely  that 
prey  become  uniformly  distributed 
throughout  the  filter,  so  that  displacement 
of  the  entire  tongue  organ  via  protraction 
and  retraction,  elevation  and  depression. 


and  lateral  shifting  would  probably  be 
more  effective  in  prey  removal  than  lin- 
gual shape  deformation.  This  view  accords 
with  myologic  findings  of  balaenid  tongues 
(Werth,  1990,  1993),  which  have  extrinsic 
muscles  (originating  outside  the  tongue) 
that  appear  to  be  greater  contributors  to 
its  body  (by  mass  and  cross-sectional  area) 
than  are  intrinsic  muscles,  which  exist 
solely  within  the  tongue.  Analysis  of  un- 
published data  (Werth,  in  preparation) 
froin  fresh,  frozen,  and  preserved  fetal,  ne- 
onate, and  adult  right  and  bowhead  whales 
suggests  that  although  scattered  fibers  of 
the  inusculus  (m.)  lingualis  proprius,  es- 
pecially verticalis  (perpendiculares)  and 
transversus  fibers,  are  found  on  the  dor- 
sum of  the  tongue  root  and  tip  as  they  in- 
tergrade  with  plentiful  adipose  tissue  (pre- 
sumably for  nutritional  storage  or  ther- 
moregulation), the  m.  genioglossus  is  a 
much  larger  contributor  to  the  tongue 
body,  based  on  gross  examination  and  cal- 
culation of  relative  cross-sectional  area. 
The  m.  hyoglossus  and  m.  styloglossus,  al- 
though significantly  smaller  than  the  m. 
genioglossus,  nonetheless  are  well  devel- 
oped in  all  age  classes  (see  also  Lambert- 
sen  et  al.,  1989).  Taken  together,  analysis 
of  these  data  on  component  muscles  (sim- 
ilar to  data  from  an  odontocete  "great 
whale,"  the  sperm  whale;  Werth,  1998) 
suggests  that  although  the  balaenid  tongue 
possesses  a  limited  ability  for  shape 
change,  it  is  well  suited  to  the  elevation, 
retraction,  and  depression  that  underlie 
the  lingual  scraping  hyjDothesis. 

Although  gray  whales  also  possess  a 
large,  firm,  elevated,  muscular  tongue,  the 
conspicuous  flaccidity  of  the  adult  rorqual 
tongue  would  seem  to  preclude  much  of 
the  activity  described  here.  Pivorunas 
(1979)  noted  major  changes  in  the  balaen- 
opterid  tongue  as  it  transformed  from  a 
solid,  muscular  structure  used  in  suckling 
to  the  deformable,  flaccid  sheet  seen  in 
adults.  From  birth  until  around  weaning 
muscle  fiber  is  replaced  with  adipose  and 
elastic  connective  tissues  as  the  increasing- 
ly saccular  organ  flattens  and  spreads  lat- 


198         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


erally.  Intrinsic  muscle  fibers  are  scattered  sibly,  plates  rapping  together,  although  the 

and  poorly  developed;  as  in  balaenids,  the  rattle  is  presumably  associated  with  skim 

tongue  may  sei-ve  as  a  seasonal  store  of  foraging,  not  prey  release.  Although  ob- 

adipose  tissue   (Howell,   1930;  Tarpley,  servation   of  lateral  head   movement  has 

1985).  The  tongue  is  thought  to  play  a  role  been  limited,  any  degree  and  direction  of 

in  expelling  water  from  the  oral  cavity  in  motion    (including    dorsoventral    shaking, 

all  mysticetes,  yet  the  elastic  recoil  of  gular  which  has  not  been  documented)  might 

closure  may  accomplish  much  of  this  func-  dislodge  prey.   Unfortunately,  fine  baleen 

tion  in  rorquals  and  obviate  the  need  for  fringes  might  adhere  together  closely  (the 

a  muscular  tongue  in  this  family.  way  gill  lamellae  clump)  in  air,  impeding 

A  related  yet  alternative  notion  is  that  proper  prey  removal.  Head  shaking  un- 
the  tongue  could  simply  slap  or  shake  prey  derwater  might  resolve  this  problem,  yet 
free,  perhaps  by  vibrating  plates  or  waving  because  many  prey  are  neutrally  buoyant 
them  anteroposteriorly.  This  could  allevi-  in  seawater  gravitational  forces  would  not 
ate  baleen  abrasion  (and  to  a  lesser  extent  prove  effective;  prey  would  more  likely 
lingual  abrasion,  although  it  would  involve  float  or  even  swim  off  fringes  in  water  cur- 
similar  muscle  actions),  as  well  as  the  in-  rents  inside  the  oral  cavity  generated  by 
ability  of  the  tongue  to  free  prey  from  head  shaking. 

fringes  not  directly  contacting  the  tongue.  As  with  the  lingual  scraping  hypothesis. 

Any   motion   that   might    jostle   plates   or  a  serious  shortcoming  of  this  plan  is  that 

knock  them  together  could  release  prey,  it  might  not  release  prey  adequately,  yet 

although  this  would  likely  be  less  efficient  because  balaenids  skim  for  hours  with  lit- 

with  minute  prey  trapped  in  fine,  filamen-  tie   apparent   swallowing   (at  least  with 

tons  fringes.  However,  the  fact  that  skim-  sparsely   distributed   prey),    a   good   head 

mers    continuously    filter    might    obligate  shake  would  likely  dislodge  sufficient  food 

them  to  purge  their  filter  continuously,  in-  to  swallow.  A  major  disadvantage  of  head 

stead  of  at  long  intervals  as  was  suggested  shaking  would  seem  to  be  the  metabolic 

earlier.  This  is  especially  crucial  in  light  of  cost  of  moving  the  entire  head,  which,  al- 

the  fact  that  the  filter  is  at  best  inefficient  though  it  need  not  be  particularly  rapid 

and  at  worse  useless  when  clogged  with  nor  vigorous,  would  certainly  require  more 

prey  or  other  items.  Balaenids'  long  plates  energy  than  simply  moving  the  tongue.  Yet 

might  also  clean  themselves  to  some  extent  simpler  ways  may  exist  to  move  the  head, 

by  rubbing  or  squeezing  together  when  In  one  of  the  few  published  mentions  of 

they  fold  posteriorly  as  the  mouth  closes;  prey  release,  Gaskin  (1982)  postulated  that 

however,  this  is  not  feasible  for  the  much  the  short,  lunging  inishes  of  right  whales 

shorter    plates    of   the    skim    feeding    sei  during  bouts  of  skim  feeding  could  agitate 

whale.  and  reinove  clinging  food  particles. 

Another  solution,  at  least  in  balaenids 

Prey  Removal  Via  Head  or  Lip  Shaking  ^i^^^e  large  lower  lips  abut  the  baleens 

A  second  hypothesis,  also  mechanical  in  lateral  edge  (Fig.  2),  would  be  to  flap  the 
nature,  stems  from  obsei-vations  of  occa-  lips  or  shake  only  the  lower  jaw  rather  than 
sional  head-shaking  behavior  in  southern  the  entire  head.  Lambertsen  et  al.  (1989) 
right  whales  (Payne,  in  press).  Whales  described  the  bowhead's  strong  labial  mus- 
have  been  seen  shaking  their  heads  rapidly  culature,  particularly  the  temporalis  and 
from  side  to  side  above  the  surface  with  a  deep  masseter,  which  have  extensive  in- 
sound  audible  from  a  great  distance.  This  sertions  on  the  coronoid  process.  Although 
sound  is  not  unlike  the  "baleen  rattle"  of  these  muscles,  like  the  specialized  mysti- 
right  whale  skim  feeding  (Watkins  and  cete  temporomandibular  articulations  and 
Schevill,  1976),  produced  by  water  lapping  mandibular  symphysis,  have  been  impli- 
over  partially  submerged  plates,  and,  pos-  cated  in  mandibular  adduction  for  balaen- 


Mysticete  Prey  Removal  •  Werth 


199 


id  feeding  (especially  to  establish  the  or- 
olabial  sulcus  and  support  baleen;  Es- 
chricht  and  Reinhardt,  1866),  they  could 
play  a  further  role  in  prey  removal.  Prelim- 
inary study  also  discloses  the  presence  of 
small  slips  of  labial  musculature  arising 
solely  from  the  lower  jaw  of  Balaena 
(Lambertsen  et  al,  1989;  Werth,  1993); 
the  extent  to  which  these  control  the  lips 
is  unknown.  A  combination  of  surface  and 
submerged  head  shaking,  forward  lunging, 
mandibular  rotation,  and  cheek  flapping  in 
right  whales  might  allow  for  mechanical 
removal  of  trapped  prey  without  direct 
contact  between  tongue  and  baleen  and 
substantial  wear  on  either.  The  study  of 
Ray  and  Schevill  (1974)  of  benthic  suction 
feeding  in  a  young  captive  gray  whale  con- 
firmed that  each  lip  could  be  moved  in- 
dependently and  curled  away  from  the  ba- 
leen. Mandibular  rotation  has  also  been  as- 
sociated with  enhanced  gape  and  enlarge- 
ment of  the  oral  cavity  for  improved  water 
engulfment  in  balaenopterids  (Lillie,  1915; 
Howell,  1930),  yet  the  ability  of  rorqual 
lips  to  knock  baleen  is  doubtful,  for  al- 
though the  lips  contact  the  short  baleen, 
they  protrude  little  above  the  mandible 
and  are  likely  far  less  mobile  than  those  of 
gray  and  right  whales. 

Prey  Removal  Via  Hydrodynamic  Flushing 

A  third  cleaning  strategy  entails  back- 
washing  a  small  amount  of  water  into  the 
mouth  to  remove  items  from  baleen  and 
deposit  them  on  the  tongue  for  transport 
and  swallowing.  As  in  the  first  hypothesis, 
the  tongue  is  directly  involved,  although  it 
would  not  contact  baleen.  By  rapidly  de- 
pressing and/or  retracting  the  tongue,  the 
oral  space  would  enlarge,  briefly  generat- 
ing a  suction  pressure  to  draw  water 
through  baleen  into  the  mouth.  Just  as  a 
dip  net  can  be  rinsed  by  rapidly  jerking  it 
back  to  reverse  the  flow  through  it,  so  wa- 
ter might  momentarily  enter  a  whale's 
mouth  from  the  sides  and  thereby  release 
captured  items,  so  long  as  gape  was  suffi- 
ciently closed  to  prevent  water  from  en- 
tering ventral  to  the  baleen  racks.  Rapid 


abduction  of  the  jaws  might  be  coupled 
with  lingual  depression  to  create  sufficient 
negative  pressure  to  pull  water  in.  The  en- 
suing current  need  not  be  strong,  merely 
sufficient  to  reverse  the  water  flow  and  de- 
liver prey  into  the  center  of  the  oral  cavity. 
Note  that  this  idea  differs  from  the  pre- 
ceding two  in  that  it  depends  on  hydro- 
dynainic  rather  than  mechanical  forces, 
with  water  (rather  than  a  solid  object)  sup- 
plying the  cleaning  mechanism. 

Not  only  would  this  flushing  method  re- 
quire substantial  lingual  (and  likely  labial) 
mobility,  but  its  efficacy  would  vary  de- 
pending on  such  mobility  as  well  as  other 
factors — namely  prey  size  and  type  and 
coarseness  of  baleen  strands — that  deter- 
mine how  likely  items  are  to  lodge  in  fring- 
es. Although  rorquals  might  not  possess  a 
sufficiently  firm  and  muscular  tongue  to 
achieve  even  weak  intraoral  suction  pres- 
sures, their  coarser  fringes  and  typically 
larger  prey  (with  the  exception  of  the  sei 
whale)  ought  to  ensure  that  even  euphau- 
siids  would  not  become  entangled,  but 
would  simply  drop  onto  the  tongue  once 
the  mouthful  of  engulfed  water  was  ex- 
pelled. Certainly  the  suction-feeding  gray 
whale  could  generate  sufficient  negative 
pressure  to  flush  baleen  effectively.  In  es- 
sence the  sole  difference  between  suction- 
generated  prey  capture  and  release  would 
be  gape  and,  to  a  minor  extent,  lip  posi- 
tion: although  a  wide  gape  would  allow  for 
prey  ingestion,  a  narrow  gape  would  sim- 
ply result  in  a  stream  of  cleansing  water 
through  baleen  plates.  A  foraging  gray 
whale  could  right  its  body  or  remain  in  a 
side-swimming  position  (although  not  con- 
tacting the  substrate)  for  this  backflushing. 
Just  as  the  mouthful  of  engulfed  water  is 
expelled  from  the  mouth  through  baleen, 
the  mouthful  of  water  for  prey  flushing 
could  likewise  be  expelled  by  intermit- 
tently filter- feeding  mysticetes,  either  be- 
fore or  after  deglutition  of  accumulated 
prey.  However,  note  that  although  whales 
can  handle  the  osmotic  load  of  swallowed 
seawater,  they  do  not  drink  seawater  (Sli- 
jper,    1962).   The   potential   for  increased 


200         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


V 


seawater  ingestion  from  this  rinsing  flow 
might  pose  a  serious  problem  for  baleen 
cleaning  via  backwash. 

Although  balaenid  tongues  should  also 
prove  adequate  to  generate  backwash  flow, 
their  delicate  hairlike  baleen  fringes  might 
preclude  prey  release.  Indeed,  any  extra 
water  flow  (in  any  direction)  might  only 
serve  to  ensnare  items  further.  Such  hy- 
drodynamic  considerations  are  crucial,  for 
recall  that  this  is  a  nonstatic  three-dimen- 
sional filter  with  porosity  dependent  on 
flow  (Sanderson  and  Wassersug,  1990). 
The  higher  the  water  pressure,  the  denser 
the  filter  becomes  (i.e.,  the  smaller  the 
pores),  promoting  prey  capture  and  allow- 
ing ever  smaller  prey  to  be  captured.  As 
flow  through  the  filter  slows,  the  compact- 
ed mesh  expands,  so  that  it  can  be  rinsed 
much  more  easily.  Hence,  a  backwash  flow 
should  not  be  notably  rapid  or  powerful. 
However,  the  fact  that  most  swimming 
prey  are  negatively  rheotropic  further 
complicates  matters;  live  prey  would  tend 
to  swim  upstream  and  burrow  deeper  into 
baleen  during  backwashing. 

Although  comparative  mysticete  tongue 
muscle  studies  are  sorely  lacking,  myologic 
studies  of  right  whales  suggest  that  die 
tongue  is  capable  of  undergoing  the  move- 
ments needed  to  generate  backwash  flow. 
The  rapid  mouth  closure  and  water  expul- 
sion observed  in  right  whales  by  Mayo  and 
Marx  (1990)  may  relate  to  such  prey  re- 
moval. Although  this  behavior  (which  was 
observed  to  occur  roughly  once  an  hour) 
is  described  as  flushing,  no  direct  evidence 
exists  to  confirm  that  it  indeed  frees 
trapped  prey.  Limited  observation  of  "nod- 
ding behavior,"  in  which  a  right  whale 
quickly  dips  its  head  and  jerks  it  back 
(Gaskin,  1982;  Mayo  and  Marx,  1990), 
might  likewise  be  construed  as  supporting 
the  backwash  hypothesis,  although  this  be- 
havior might  also  support  the  claim  of  prey 
removal  via  head  shaking  or  brief  forward 
lunging  described  previously. 

CONCLUSIONS 

Baleen    cleaning    is    not    so    simple    as 
might  initially  be  assumed,  with  many  fac- 


tors to  be  taken  into  consideration,  chief 
among  these  the  relation  between  the  fil- 
tration apparatus  and  filtered  items.  Given 
the  respective  strengths  and  weaknesses  of 
the  three  prey  removal  hypotheses,  all 
seem  equally  likely  to  occur,  especially  in 
skim  feeders.  Confirmation  of  baleen 
wearing  and  replenishment,  along  with  the 
purported  actions  of  tongue  musculature, 
support  the  claim  of  baleen  cleaning  by 
tongue  scraping — although  the  lack  of  dif- 
ferential wear  calls  this  into  serious  ques- 
tion— or  by  gentler  rubbing,  which  would 
minimize  abrasive  loss  of  baleen.  Limited 
observations  of  lateral  head  shaking  and 
nodding  in  Eubalaena  provide  indirect 
support  for  the  other  hypotheses.  Moipho- 
logic  evidence  seems  to  sustain  rather  than 
preclude  each  conjectural  means  of  prey 
removal.  It  may  well  be  that  different  spe- 
cies and  individuals  in  different  situations 
use  all  three  mechanisms. 

ACKNOWLEDGMENTS 

I  am  greatly  indebted  to  Laurie  Sander- 
son, whose  critical  comments  greatly  im- 
proved the  content  and  clear  expression  of 
the  ideas  presented  here.  Richard  Wasser- 
sug and  Jim  Mead  also  provided  many  use- 
ful insights  in  their  careful  reviews  of  this 
paper.  Discussions  with  Scott  Kraus,  Tom 
Albert,  Larry  Barnes,  Roger  Payne,  Tom 
Ford,  Butch  Rommel,  Dan  Hillmann, 
Stormy  Mayo,  and  Craig  George  helped 
me  to  formulate  and  develop  the  hypoth- 
eses of  prey  removal  and  their  respective 
strengths  and  weaknesses.  The  ongoing 
anatomical  study  of  bowhead  tongues  de- 
scribed in  this  paper  was  supported  finan- 
cially and  logistically  by  the  North  Slope 
Borough,  Department  of  Wildlife  Man- 
agement, Barrow,  Alaska  (contract  C2189) 
and  Alaska  Eskimo  Whaling  Commission, 
which  generously  permitted  me  to  use 
data  from  haivested  whales  and  examine 
specimens  housed  at  the  Lousiana  State 
University  School  of  Veterinary  Medicine. 

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TONGUE-JAW  LINKAGES:  THE  MECHANISMS  OF  FEEDING 
REVISITED 


KAREN  M.  HIIEMAE'  AND  JEFFREY  B.  PALMERS 

Abstract.  Since  the  first  description  of  cyclical 
tongue  movements  in  feeding  (opossum  and  cat), 
studies  on  a  range  of  mammals  (fruit  bat,  tenrec,  rab- 
bit, hyrax,  macaque,  and  man)  have  been  completed. 
This  review  examines  those  data  to  determine  wheth- 
er a  pattern  of  tongue-jaw  linkage  in  feeding  is  com- 
mon to  all  mammals.  Major  directional  changes  in 
hyoid  and  tongue  surface  movement  occur  at  com- 
parable points  in  tlie  jaw  movement  cycle  regardless 
of  craniofacial  anatomy  and  dietetic  specialization.  In 
all  cases,  the  hyoid  and  tongue  surface  move  forward 
during  the  early  part  of  jaw  opening,  with  a  return 
movement  during  later  jaw  opening  and  closing.  The 
role  of  this  cychcal  tongue  movement  in  the  transport 
and  manipulation  of  food  is  common  to  all  mammals 
studied,  save  that  triturated  food  is  moved  through 
the  palatoglossal-palatopharyngeal  arches  for  bolus 
formation  earlier  in  the  tongue  cycle  in  macaque  and 
man.  New  data  on  swallowing  in  man  suggest  that 
Homo  has  a  specialized  pattern  for  liquid  bolus  for- 
mation but  otherwise  retains  the  basic  mammalian 
pattern. 

INTRODUCTION 

In  a  letter  to  Nature,  Crompton  et  al. 
(1975)  reported  that  the  hyoid  bone  moves 
continuously  in  feeding  in  the  American 
opossum  {Didelphis  virginiana).  This  sim- 
ple observation  refuted  the  then  conven- 
tional wisdom,  based  on  limited  human 
studies,  that  the  hyoid  only  moves  in  swal- 
lowing. Attention  has  since  focused  on  the 
interrelationships  between  jaw  and  hyoid 
movement,  jaw  movement,  and  hyoid  and 
tongue  surface  movement,  and  the  role  of 
these  movements  in  the  acquisition,  pro- 


'  Institute  for  Sensory  Research,  and  Department 
of  Bioengineering  and  Neuroscience,  Syracuse  Uni- 
versity, Syracuse,  New  York  13244-5290. 

-  Department  of  Physical  Medicine  and  Rehabih- 
tation.  The  Johns  Hopkins  University  School  of  Med- 
icine, Good  Samaritaji  Hospital,  Baltimore,  Maryland 
21239. 


cessing,  and  transport  of  food  in  mammals. 
In  1978,  Hiiemae,  Thexton,  and  Crompton 
posited  that  cyclical  movements  of  the 
tongue,  by  facilitating  the  intraoral  man- 
agement of  food,  including  its  transport  to 
the  pharynx  for  bolus  accumulation  and 
swallowing,  were  integral  to  the  feeding 
process.  A  sufficient  body  of  evidence  has 
now  accumulated  from  experimental  stud- 
ies (listed  in  the  Appendix)  examining 
feeding  behavior  in  representative  terres- 
trial maiTunals  with  very  different  dietetic 
adaptations  to  make  a  synthesis  possible. 
This  review  examines  the  proposition  that 
a  pattern  of  linked  jaw  and  hyoid-tongue 
movement  is  common  to  all  terrestrial 
mammals  witli  type  I  tongues  (Doran, 
1975). 

Although  the  craniofacial  anatomy  of 
terrestrial  mammals  has  a  common  Bau- 
plan,  anatomical  details  vary  widely  both 
among  and  within  orders  (Hiiemae,  2000; 
Turnbull,  1970).  However,  the  basic  phys- 
iological functions  performed  by  the  teeth, 
jaws,  tongue  and  associated  soft  tissues  do 
not  vaiy  (Hiiemae,  2000).  These  functions 
are  associated  with  the  acquisition,  reduc- 
tion (if  needed),  transport,  and  swallowing 
of  food  for  chemical  digestion.  It  follows 
that  because  all  mammals  have  the  same 
Bauplan,  subserving  the  same  biological 
functions,  it  is  reasonable  to  postulate  that 
the  mechanisms  used  to  fulfill  these  phys- 
iological functions  will  be  essentially  the 
same.  If  a  patterned  linkage  exists  between 
the  cyclical  moveinents  of  the  jaws  and  the 
cyclical  movements  of  both  the  tongue 
surface  and  the  hyoid,  that  linkage  should 
be  expressed  by  a  consistent  relationship 


Bull.  Mus.  Comp.  Zool.,  156(1):  205-217,  October,  2001 


205 


206         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


betAveen  jaw  and  tongue— hyoid  movement  is  a  basic  mammalian  pattern;  and  to  brief- 
events  in  all  feeding  cycles  in  all  species  ly  revisit  the  issue  of  whether  the  inam- 
examined.  malian  pattern  could  have  its  antecedents 
Bramble  and  Wake  (1985)  developed  a  in  the  mechanisms  for  food  transport  de- 
theoretical  model  for  a  generalized  feeding  veloped  in  phylogenetically  earlier  terres- 
cycle  in  nonmammalian  terrestrial  tetra-  trial  tetrapods. 

pods,  largely  based  on  a  synthesis  of  ki-  cydcdimcmtai    cti  mice 

nesiological      and      electromyographic  EXPERIMENTAL  STUDIES 

(EMG)  data  from  terrestrial  salamanders.  Intraoral  behavior  is  particularly  difficult 
turtles,  and  lizards.  This  model  had  fea-  to  study.  The  only  techniques  that  allow 
tures,  such  as  rate  change  and  direction  of  the  concurrent  recording  of  jaw  move- 
jaw  and  hyolingual  motion,  similar  to  those  ment,  hyoid  movement,  tongue  surface 
reported  in  mammals  (Bramble  and  Wake  movement  (provided  radiopaque  markers 
1985,  fig.  13.3).  They  suggested  that  there  are  used),  and  food  position  (if  treated 
might  be  homologies  between  mammalian  with  barium  sulfate)  are  cinefluorography 
feeding  mechanisms,  especially  intraoral  (CFG)  or  videofluorography  (VFG).  It 
transport,  and  those  obsei'ved  in  nonmam-  must  be  emphasized  that  any  CFG  or 
malian  vertebrates,  such  that  the  patterns  VFG  record  is  a  2D  projection  or  image 
seen  in  mammals  might  have  evolved  in  of  3D  events.  If  a  structure,  such  as  the 
earlier  terrestrial  tetrapods.  While  ac-  hyoid,  has  little  mediolateral  movement, 
knowledging  the  absence  of  experimental  then  the  2D  image  seen  in  lateral  projec- 
data,  they  extended  their  analysis  to  sug-  tion  probably  accurately  represents  its 
gest  that  the  central  pattern  generator  movement  pattern.  Data  for  macaque  and 
(CPG)  maintaining  the  rhythmic  jaw  man  confirm  that  no  such  confidence  can 
movements  of  feeding  identified  in  mam-  be  attached  to  tongue  surface  movement 
mals  (Bremer,  1923;  Dellow  and  Lund,  data.  Although  CFG  and  VFG  have  been 
1971),  might  be  present  in  antecedent  used  in  many  studies  of  feeding  in  mam- 
forins,  and  that  the  output  of  such  a  CPG  mals  representative  of  omnivores  (includ- 
was  regulated  by  sensoiy  modulation  from  ing  the  Pecora),  carnivores,  herbivores,  ro- 
oral  receptors.  Smith  (1994:  294)  argued,  dents,  and  primates,  relatively  few  (see 
for  that  to  be  true,  neuromotor  patterns  Hiiemae,  2000;  and  the  Appendix)  have 
had  to  be  homologous,  that  is,  despite  examined  the  temporal  relationships  be- 
changes  in  peripheral  anatomy,  the  neu-  tween  jaw  and  tongue— hyoid  movements 
romotor  output  from  the  central  nervous  during  feeding  sequences.  Comparison 
system  (CNS)  had  to  be  conserved.  She  and  synthesis  of  those  reports  to  address 
observed  that  similarities  in  movement  the  question  of  whether  a  common  pattern 
patterns  (or,  functional  behaviors,  our  exists  is  complicated  by  the  rate  of  exper- 
term)  had  been  extended  "to  hypotheses  imental  data  acquisition,  the  methods  used 
of  neuromotor  conservatism,  to  assertions  for  analysis,  the  form  in  which  data  were 
of  evolutionary  constraints."  Taking  a  presented,  and  the  need  to  reconcile  the 
broad-brush  approach  using  examples  underlying  behavioral  patterns  regardless 
from  a  broad  range  of  vertebrate  taxa  to  of  the  terminology  used, 
test  the  hypothesis  that  terrestrial  verte- 

brates   have   a  conservative   feeding  pro-  "'"'^!,'^'^^' ^'vX.?.^,^^^^ 

gram,  she  found  fittle  evidence  for  its  sup-  HYOID-JAW  COMPLEX 
port.  Although  the  proportions  of  the   skull 

The  purpose  of  this  review  is  to  examine  and  lower  jaw,  as  well  as  the  general  po- 

what    is    now    known    about    tongue— jaw  sition  of  the  hyoid  and  the  shape  of  the 

movements   in   feeding  in   mammals,   in-  tongue,  differ  markedly  between  mammals 

eluding  man;  to  determine  whether  there  (Hiiemae,   2000),   the   muscles  producing 


Tongue-Jaw  Linkages  •  Hiiemoe  and  Palmer        207 


jaw,  hyoid,  or  tongue  movement  are  gen-  ented  pharyngeal  surface  (Hiiemae,  2000; 
erally  homologous.  Hyoid  position  is  Hiiemae  and  Palmer,  1999).  If  a  basic- 
known  to  be  controlled  by  the  interplay  of  mammalian  pattern  exists,  it  follows  that 
activity  in  three  groups  of  muscles.  The  these  morphological  changes  should  not 
anterior  suprahyoids  (anterior  belly  of  di-  affect  its  expression,  although  the  mechan- 
gastric  and  geniohyoid)  pull  the  hyoid  for-  ical  outcomes  may  be  different, 
ward  and  can  depress  the  lower  jaw.  The  Doran  (1975)  identified  two  types  of 
mylohyoid  can  also  elevate  the  hyoid,  syn-  mammalian  tongues,  both  with  oral  and 
chronously  raising  the  floor  of  the  mouth  pharyngeal  parts.  Type  I,  found  in  most 
and  so  the  tongue  body.  The  hyoid  is  con-  mammals  (and  all  those  mammals  in  which 
nected  to  tlie  skull  base  by  the  posterior  its  movement  has  been  studied),  can  be 
belly  of  digastric  and  the  stylohyoid  (pos-  protruded  to  a  maximum  of  50%  of  its 
tenor  supraliyoids),  which  can  pull  the  hy-  resting  length.  Type  II  tongues  are  found 
oid  backward  and  upward.  The  infrahyoids  in  a  few  mammals,  such  as  the  anteaters, 
connect  the  hyoid  to  the  sternum  (ster-  and  can  be  extensively  protruded  outside 
nohyoid),  the  scapula  (omohyoid),  and  the  the  mouth  for  food  gathering.  Livingstone 
thyi-oid  cartilage  (thyrohyoid).  The  major  (1956)  argued,  first,  that  the  movement  of 
infrahyoids  (sternohyoid  and  omohyoid)  the  tongue  depends  largely  on  the  move- 
act  to  pull  the  hyoid  back,  down,  or  both,  ment  of  the  hyoid;  second,  that  change  of 

The  biomechanics  of  the  hyoid  complex  position,  coupled  with  a  change  of  form 
are  poorly  understood.  Using  EMG  and  results  from  extrinsic  muscle  action,  and, 
movement  data,  Crompton  et  al.  (1977)  last,  that  the  intrinsic  muscles  provide  for 
demonstrated  the  mechanism  by  which  a  great  deal  of  mobility.  It  follows  that  if 
jaw  and  hyoid  movements  were  produced  the  tongue  base  shortens  (geniohyoid,  my- 
in  Didelphis,  whether  divergent  (i.e.,  the  lohyoid),  canying  the  hyoid  and  the  body 
hyoid  traveling  backward,  away  from  the  of  the  tongue  foiAvard,  then  the  effect  of 
symphysis,  in  jaw  closing,  lengthening  the  contraction  of  the  genioglossus,  which  pro- 
tongue  base)  or  convergent  (the  hyoid  tnjdes  the  tongue,  will  be  augmented, 
traveling  forward,  toward  the  symphysis,  in  Similarly,  the  action  of  hyoglossus  or  sty- 
jaw  opening,  shortening  the  tongue  base),  loglossus,  either  of  which  can  pull  the 
No  comparable  study  has  been  conducted  tongue  backward,  will  be  augmented  by 
for  any  other  mammal.  However,  the  retraction  of  the  hyoid.  However,  given  the 
changing  pattern  of  shortening  and  length-  pattern  of  insertion  of  both  genioglossus 
ening  in  these  muscles  regulates  hyoid  po-  (medially)  and  hyoglossus  (laterally),  con- 
sition  and  so  the  length  of  the  tongue  base,  traction   of  either  will   affect  the   overall 

Nonanthropoid  mammals  have  antero-  shape  of  the  tongue  body.  Nevertheless,  as 

posteriorly    (AP)    elongate    and    vertically  Kier  and  Smith  (1985)  and  Smith  and  Kier 

shallow  tongues.   However,  the  evolution  (1989)  have  emphasized,  the  tongue  has 

of  the  anthropoid  primates  resulted  in  pro-  constant  volume,  such  that  a  change  in  any 

gressive  change  in  tongue  shape,  with  con-  dimension    must    be    accompanied    by 

comitant  changes  in  the  anatomy  of  the  changes  in  the  other  two.  This  makes  the 

orophaiynx.  As  described  by  Thexton  and  distinction  between  extrinsic  and  intrinsic 

Crompton  (1998),  the  shape  of  the  tongue  muscles,    while    anatomically   convenient, 

in  macaque  has  changed  from  that  seen  in  somewhat  arbitrary  with  respect  to  func- 

Didelphis  and  most  other  mammals:  it  is  tion.  Schwenk  (2001)  further  advances  this 

shorter  anteroposteriorly  but  has  greater  argument. 

vertical  height.  In  man,  the  tongue  is  still  To  summarize,  it  follows  that  move- 
shorter  with  much  greater  height,  such  ments  of  the  lower  jaw  are  linked  to  hyoid 
that  the  hyoid  is  widely  separated  from  its  position;  movements  of  the  body  of  the 
oral  surface,  creating  a  long,  vertically  ori-  tongue  are  linked  to  the  length  of  its  base, 


208        Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


itself  affected  by  hyoid  position  and  lower  terns  of  activity  within  cycles  and  within 

jaw  movements;  and  the  working  surfaces  sequences  for  those  mammals  studied 

of  the  tongue  (oral  and  pharyngeal)  have  show  any  commonality  across  species  and 

their  shape  affected  by  both  of  the  above,  orders. 

but  augmented  by  the  activity  of  the  in- 

trinsic  Lscles.     ^                   ^  PATTERNS  OF  TONGUE  AND  HYOID 

MOVEMENT 

ISSUES  IN  SYNTHESIS  ^jj  j^^  movement  cycles  have  closing 

The  rhythmic  movements  of  the  jaw  in  and  opening  strokes  separated  by  an  IP 
feeding,  especially  chewing,  are  well  de-  phase  of  variable  duration  (very  short  in 
scribed.  Those  movements  are  now  known  some  carnivores  and  insectivores,  longer  in 
to  be  associated  with  rhythmic  hyoid  most  omnivores  and  herbivores  with  a  sub- 
movements.  At  the  same  time,  the  tongue  stantial  lateromedial  or  posteroanterior 
not  only  changes  its  gross  position  but  also  lower  molar  traverse  in  occlusion  on  the 
changes  shape  depending  on  the  condition  working  side).  For  all  mammals  studied, 
of  the  food  in  the  mouth  and  stage  in  se-  the  hyoid  moves  from  its  most  backward 
quence:  ingestion  with  stage  I  transport;  and  downward  position,  at  about  mini- 
processing;  bolus  formation  with  stage  II  mum  gape,  to  its  most  forward  and  up- 
transport;  and  deglutition  (see  Hiiemae,  ward  position  during  opening,  reversing 
2000;  Hiiemae  and  Palmer,  1999).  We  also  direction  before  maximum  gape  (Fig.  1). 
now  know  that  the  overall  jaw  cycle  time  Tongue  marker  orbits  also  demonstrate 
varies  between  species  studied,  and  also  this  reversal  (Fig.  2). 

within  each  sequence  in  a  given  species.  To  test  the  hypothesis  that  all  mammals 

such  that  the  time  spent  in  closing  (Fast  show  the  same  jaw  and  tongue  movement 

Close  [FC],  Slow  Close  [SC]/Power  Stroke  patterns,  regardless  of  cycle  duration,  or 

[PS]),  Intercuspal  Phase  (IP),  and  opening  phase  duration  within  cycles,  and  tongue 

(Slow  Open  [SO]  or  Ol,  02,  Fast  Open  shape,  the  available  data  were  analyzed  us- 

[FO])  also  varies,  based  on  the  changing  ing  distinct  movement  turnpoints  as  event 

rate  of  jaw  movement.   It  follows  that  if  markers    (Palmer  et   al.,    1997).   The  jaw 

jaw,    hyoid,    and   tongue    movements    are  movement  event  markers  were  maximum 

linked,  that  is,  their  movements  are  inter-  and  minimum  gape.   For  the  tongue— hy- 

dependent,    then   there   should   be   some  oid,  they  were  maximum  forward  (MF  for 

consistent  relationship,  regardless  of  sep-  hyoid  or  TF  for  tongue);  maximum  down 

aration  in  time,  between  specific  events  in  (MD  or  TD),  maximum  back  (MB  or  TB), 

jaw,  hyoid,  and  tongue  movement  cycles,  and  maximum  up  (MU  or  TU),  relative  to 

For  such  linkage  to  exist,  synchrony  is  not  the   upper  occlusal   plane.   The   available 

essential,  rather  events  should  occur  in  a  data  were   brought  to   a  consistent  time 

consistent  sequence.  scale    (normalized)    and   these   turnpoints 

If  the  hypothesis  that  there  is  such  link-  (hyoid— tongue  marker),  as  reported,  were 

age  and  that  same  linkage  will  be  found  in  established  relative  to  maximum  and  min- 

all  mammals  is  to  be  exliaustively  tested,  imum  gape  and  entered  into  a  bar  chart  as 

then  a  rigorous  comparative  analysis  using  accurately    as    possible.    The    results    are 

a  set  of  uniform  event  criteria  and  tech-  shown  in  Figure  3. 

niques  such  as  interval  analysis  is  required.  In  every  species,  TF  occurs  before  max- 

Clearly  this  is  infeasible  for  the  full  range  imum  gape  in  opening.  In  all  these  mam- 

of  mammals  so  far  studied  given  the  issues  mals,  including  tenrec  and  opossum  (data 

in  data  collection  and  reduction  alluded  to  limited  to  text  descriptions),  the  tongue 

above.  Instead,  we  are  forced  to  examine  marker  (anterior  tongue  marker,  ATM,  or 

the  available  qualitative  (behavioral)  data  middle  tongue  marker,  MTM)  reaches  its 

and  attempt  to  determine  whether  the  pat-  most  backward  position  concurrent  with  or 


Tongue-Jaw  Linkages  •  Hiiemae  and  Palmer        209 


HYRAX  (derived  from  German  and  Franks,  1991) 

100      150       200       250 
^ 


MACAQUE    (derived  from  Hiiemae  et  al.,  1995) 
msec  0 


100       200       300      400      500       600 
h \ r+ 


JAW 


\ 


RABBIT  (derived  from  Cortopassi  and  f^uhl,  1990) 

50       100      150      200 
H ^ h-i — h 


Open 

ATM 
For 

\ 

Up 

MTM 
For 

A 


Up 

PTM 
For 


t 


Up 


HYOID 
For 


t 


Up 


Figure  1 .  Gape-time  (GT)  plots  for  a  single  cycle  of  jaw,  tongue,  and  hyoid  movement  in  hyrax,  rabbit,  and  macaque  redrawn 
from  data  in  the  papers  cited  (no  attempt  has  been  made  to  represent  actual  distances  traveled  in  any  direction).  The  pattern 
of  upward  and  fonward  movement  of  the  tongue  surface  in  the  first  part  of  opening  is  shown  by  the  extra  thicl<  lines,  the 
synchronous  downward  movement  by  thicl<  lines.  The  hyrax  and  rabbit  records  (published  figures,  or  text)  provide  no  basis  for 
dividing  the  opening  jaw  movement  into  01 ,  02,  or  FO/03  phases;  however,  the  macaque  cycle  (a  composite)  shows  the  pattern 
of  jaw  movement  when  the  SO  phase  has  two  components.  The  reversal  of  ATM  and  MTM  movement  at  the  S02-FO  transition 
is  clearly  shown  (see  text). 

Abbreviations:  ANT.  T,  anterior  tongue;  ATM,  anterior  tongue  marker;  MID.  T,  middle  tongue;  MTM,  middle  tongue  marker; 
POST.  T,  posterior  tongue;  PTM,  posterior  tongue  marker. 


210         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


(a)  LAPPING 
ATM 


MTM 


PTM 


Hyoid 


>^ 


(b)  STAGE  I  TRANSPORT 


\^>-^  J> 


(C)  INTRA-ORAL  MANIPULATION 


(d)  STAGE  II  TRANSPORT 


Palatal 


Anterior 

^ I         Movemen 


Movement  in  SO  (01 ,  01 +02) 

Figure  2.  The  trajectory,  shown  as  loops,  of  anterior  (ATIVI), 
middle  (MTM),  and  posterior  (PTM)  tongue  markers,  and  the 
hyoid,  in  opossum,  (a)  Lapping  (a  low-amplitude  jaw  move- 
ment without  FO  or  FC):  (b)  stage  I  transport  (movement  of 
food  from  an  extraoral  position  or  from  the  front  of  the  oral 
cavity  to  the  molar  region);  (c)  chewing  (processing)  cycles 
where  food  has  to  be  repositioned  on  the  occlusal  surfaces  of 
the  postcanines  (manipulation);  and  (d)  stage  II  transport,  in 
which  triturated  food  is  moved  through  the  palatoglossal  arch- 
es for  bolus  formation  and  deglutition.  Although  the  tongue  and 
hyoid  movements  in  lapping  show  long  elliptical  loops,  the  in- 
troduction of  the  FO  and  FC  phases  when  feeding  on  solid 
food  increases  their  vertical  dimension.  (FO  dashed  line,  FC 
thin  solid  line,  SC  longer  dotted  line).  Regardless  of  stage  in 
sequence,  the  tongue  surface  (ATM,  MTM)  is  moving  from  a 
maximum  tongue  back  (TB)  to  a  maximum  tongue  fonward 
(TF)  position  during  early  opening,  reaching  its  most  forward 
position  in  opening,  but  before  maximum  gape.  Redrawn  from 
Hiiemae  and  Crompton  (1985,  fig.  14-12). 


Pteropus  giganteus    [frultbat,  Mid.  Tongue] 
Max.  Gape  MIn.  Gape        Max.  Gape 


TD      TB  TU  TF 

Oryctolagus  cuniculus    [rabbit,  Mid.  Tongue] 


'J^v'^r^v^vr 


r^jT^^^j^J. 


TD  TB     TU  TF 

Procavia  syriacus  [hyrax,  Mid.  Tongue] 


TB  TF 

Felis  domesticus  [cat,  Ant.  Tongue,  Lapping] 


TB  TF 

Macaca  fascicularis    [macaque.  Ant.  Tongue] 


TD      TB 


Homo  sapiens   [man.  Ant.  Tongue] 


Figure  3.  Tongue  turnpoints  (TB  and  TF,  with  TD  and  TU 
where  available,  see  text)  for  chewing  cycles  in  mammals 
where  time  data  is  available  (no  data  for  opossum  are  included 
because  the  gape-time  plot  data  from  which  Fig.  2  was  pre- 
pared were  not  published).  Cycle  times  have  been  normalized 
to  express  the  time  of  events  within  cycles  expressed  as  the 
percentage  of  time  after  initial  maximum  and  before  terminal 
maximum  gape.  The  common  rhythmic  pattern  of  AP  tongue 
movement  is  shown. 

Vertical  bars  mark  start  maximum  gape,  minimum  gape,  and 
terminal  maximum  gape.  Forward  tongue  movement  in  open- 
ing is  shown  by  the  wavy  stippling;  backward  movement  is 
shown  by  the  dots.  The  blank  periods  (fruit  bat,  rabbit,  ma- 
caque, and  man)  indicate  the  time  in  which  the  tongue  surface 
is  rising. 


Tongue-Jaw  Linkages  •  HUemae  and  Palmer        211 


before  minimum  gape.  The  exceptions  ap- 
pear to  be  h>Tax  and  opossum,  where  a 
\ery  short  IP  often  occurs.  However,  the 
time  compressed  data  in  German  and 
Franks  (1991,  fig.  2)  show  a  short  foi-ward- 
backward  oscillation  before  the  computed 
minimum  gape  in  stereotypical  chewing 
cycles.  If  TB  is  taken  as  the  first  of  these 
backward  positions,  then  the  pattern  for 
hyrax  is  consistent  with  that  for  the  other 
species  (as  shown  in  Fig.  3).  In  some  re- 
cords for  the  opossum  (Hiiemae  and 
Crompton,  1985),  TB  occurs  before  min- 
imum gape.  Unfortunately,  because  the  or- 
bits shown  in  the  published  figures  are  ex- 
amples of  actual  cycles,  rather  than  a  sta- 
tistically derived  norm  based  on  analysis  of 
large  numbers  of  cycles,  this  result  has  to 
be  taken  as  strongly  supportive,  rather 
than  confirmatoiy,  of  a  generalized  pat- 
tern. 

It  should  also  be  noted  that  there  is  lit- 
tle likelihood  that  the  tongue  markers 
were  in  comparable  positions  in  these  sep- 
arate experiments,  because  the  published 
data  used  for  each  analysis  referred  to 
mid-tongue  or  anterior  tongue.  Further, 
strong  evidence  exists  that  although  mark- 
ers in  the  anterior  and  middle  parts  of  the 
tongue  tend  to  move  in  synchrony,  forward 
movement  of  the  posterior  tongue  and  hy- 
oid  may  be  slightly  delayed  (Hiiemae  et 
al,  1995).  This  suggests  that  were  the  orig- 
inal data  to  be  revisited,  a  much  clearer 
demonstration  of  a  common  pattern  might 
be  obtained.  However,  we  consider  it  sig- 
nificant that  an  analytical  approach  devel- 
oped to  describe  tongue— hyoid— jaw  move- 
ments in  macaque  and  man  shows  the 
same  pattern  when  applied  to  other  mam- 
mals. 

The  jaw  movement  cycle  is  designed  to 
assure  food  reduction  in  a  chewing  stroke 
(SC/PS).  The  remainder  of  the  jaw  move- 
ment cycle  serves  to  reposition  the  lower 
jaw  for  the  next  such  stroke.  Concurrently, 
there  is  a  tongue  movement  cycle  with  its 
major  activity  occurring  during  opening 
and  the  FC  phase  of  closing.  German  and 
Franks  (1991)  analyzed  the  temporal  re- 


lationships between  minimum  gape  and 
the  start  of  tongue  and  hyoid  protrusion  in 
hyrax.  They  found  that  the  tongue  and  hy- 
oid tumpoints  for  the  onset  of  forward 
movement  were  synchronized  to  within 
one  frame  of  the  computed  minimum 
gape,  but  that  no  predictable  linkage  oc- 
curred between  tongue-hyoid  movement 
events  and  maximum  gape.  This  study  pro- 
vides a  convincing  demonstration  of  the 
existence  of  a  possible  switch  from  the  jaw 
movement  cycle  required  for  food  reduc- 
tion to  a  tongue  movement  cycle  function- 
ing to  control  intraoral  food  position  and 
food  transport  in  hyrax  at  minimum  gape. 
However,  this  study  cannot  be  readily  ex- 
trapolated to  other  mammals,  especially 
anthropoids,  where  no  minimum  gape  is 
clearly  visually  identifiable  given  a  long  IP 
phase. 

Although  there  is  no  stereotypical  jaw 
movement  cycle  in  macaque  (Thexton  and 
Hiiemae,  1997),  Hiiemae  et  al.  (1995) 
were  able  to  show  that  TF  (ATM  and 
MTM),  always  occurred  within  30  milli- 
seconds (usually  less)  of  the  last  rate 
change  in  opening,  that  is,  with  the  initi- 
ation of  FO.  Furthermore,  when  02  was 
present,  the  amplitude  of  forward  tongue 
movement  was  greatest.  However,  gape  at 
the  02-F0  transition  was  always  small.  If, 
as  Thexton  and  Crompton  (1989)  argue, 
the  Ol  and  02  phases  of  lapping  (cat, 
opossum)  correspond  to  SO  (Ol  ±  02)  in 
chewing,  then  the  extensive  tongue  pro- 
trusion involved  in  lapping  exemplifies  the 
anatomical  relationship  between  tongue- 
hyoid  movement  and  gape  amplitude, 
leading  to  the  hypothesis  that  extensive 
tongue  protrusion  can  only  occur  within  a 
relatively  narrow  range  of  gape,  because 
additional  jaw  opening  (FO)  requires  hy- 
oid retraction.  It  also  explains  the  EMG 
data,  which  show  low-level  activity  in  the 
adductors  (masseter  or  medial  pterygoid) 
during  02,  suggesting  an  antagonist  func- 
tion that  resists  jaw  opening  and  promotes 
protraction  of  the  hyoid  bone  and  the 
tongue  body. 

It  must  be  emphasized  that  these  results 


212         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


must  not  be  construed  as  implying  that  and  hyoid  movement,  to  functional  (food 

tongue  and  jaw  movements  are  invariably  processing)  needs  cycle  to  cycle  within  se- 

time  and  movement  linked.  Quite  the  re-  quence. 

verse   is   true.    The   interdependence  be-  To  summarize,  as  the  jaw  movement  cy- 

tween  jaw— hyoid— tongue  movement  dein-  cle  (close,  IP,  open)  proceeds,  there  are 

onstrated  here   applies   only  to  chewing,  concomitant  inovements  of  both  the  hyoid 

lapping,  and  food  transport.  Even  in  chew-  and  the   tongue   surface.   The  hyoid  and 

ing  sequences,  albeit  in  man,  the  rhythm  tongue  move  forward  and  variably  upward, 

may  be   disrupted   during   the   collection  starting  at  minimum  gape  or  within  IP,  and 

and  aggregation  of  food  particles   (clear-  reverse  direction  during  opening,  before 

ance)  for  bolus  formation  (Hiiemae  et  al,  maximum  gape,  or  at  the  small  maximum 

1996;  Hiiemae  and  Palmer,  1999;  Palmer  gape  used  in  lapping  (end  02). 
et  al.,  1997). 

Intrinsic  Tongue  Movement.  Cortopassi  MECHANISMS  IN  FEEDING 
and  Muhl  (1990)  described  AP  move-  Vertical  and  AP  tongue  movements  dur- 
ments  of  the  rabbit  tongue  surface  as  un-  ing  feeding  cycles  have  a  common  pattern 
dulating.  This  could  be  explained  as  a  across  all  the  adult  mammals  studied  re- 
function  of  the  time  delay  between  the  ini-  gardless  of  dietary  specialization,  stage  in 
tiation  of  an  anteriorly  or  posteriorly  di-  sequence,  and  type  of  food.  The  question 
rected  moveinent  between  the  various  arises:  how  does  tliis  apparent  common 
parts  of  the  tongue.  Where  comparative  pattern  subserve  the  physiological  process- 
data  are  available,  such  a  sequential  pat-  es  required  for  transmission  of  swallow- 
tern  with  the  anterior  tongue  leading  able  food  to  the  gastrointestinal  tract  for 
seems  to  be  present.  However,  there  is  no  chemical  digestion?  The  corollary  has  to 
doubt  that  in  the  fruit  bat  (de  Gueldre  and  be  addressed:  how  is  the  linkage  between 
de  Vree,  1984),  cat  (Thexton  and  Mc-  forward  tongue  movement  in  early  jaw 
Garrick,  1988,  1989),  and  macaque  (Hiie-  opening  correlated  with  the  backward 
mae  et  al.,  1995),  there  is  differential  ex-  movement  of  food  within  and  through  the 
pansion  and  contraction  of  the  tongue  sur-  oral  cavity?  How  does  the  tongue,  acting 
face,  as  measured  by  lengthening  or  short-  against  the  hard  palate,  and  with  the 
ening  of  the  Euclidean  distance  between  cheeks  (variably  developed  in  inammals), 
tongue  inarkers.  produce  the  documented  aggregation  and 

These  studies  show  that  the  tongue  can  distal  movement  of  swallowable  food? 
be    considered    as    ha\dng    three    distinct  Feeding  sequences  are  now  considered 

components:   the  anterior  tongue   (tip  to  to    have    four    stages:    stage    I    transport 

anterior  postcanines),  the  mid-tongue  (re-  (movement  of  food  from  the  anterior  oral 

lated  to  the  cheek  teeth),  and  the  posterior  cavity  to  the  postcanines);  processing  (food 

tongue  (the  postfaucial,  or  pharyngeal,  sur-  reduction  in  chewing  or  by  tongue— hard 

face).  As  might  be  expected,  the  amplitude  palate    compression,    or    both);    stage    II 

of  possible  expansion  and  contraction  is  transport  (movement  of  swallowable  food 

greatest  in  the  anterior  tongue  and  least  in  through  the  palatoglossal— palatopharyn- 

the  posterior.  However,  in  chewing  cycles  geal   arches   with   bolus   formation),   and, 

(macaque)  when  little  or  no  anteroposte-  last,    deglutition.    Tongue    movements    in 

rior   food   transport   is   occurring,   expan-  processing  are  poorly  understood,  but 

sion— contraction  (measured  in  lateral  pro-  clearly    involve    rotation    of  the    working 

jection)   is   restricted  to  the   middle   seg-  (gustatory)  surface  of  the  tongue  about  its 

ment.  This  may  be  illustrative  not  only  of  long  (AP)  axis  to  position  food,  or  maintain 

the  2D  representation  of  3D  events  men-  food  position,   in   readiness   for  the   next 

tioned  above,  but  also  of  the  tongues  ca-  chewing  cycle   (Hiiemae,   2000;    Hiiemae 

pacity  to  respond,  independently  of  jaw  and  Crompton,  1985). 


Tongue-Jaw  Linkages  •  Hiiemae  and  Palmer        213 


Tongue  and  hyoid  movement  patterns  to  avoid  the  risk  of  aspiration  into  a  respi- 
for  stage  I  and  II  transport  have  been  de-  ratory  tract  whose  aditus  (true  vocal  folds) 
scribed  for  most  of  the  mammals  studied  lies  well  below  the  oral  cavity.  We  find 
(see  the  Appendix;  Hiiemae  and  Cromp-  (Hiiemae  and  Palmer,  1999)  that  in  H.  sa- 
ton,  1985).  In  all  cases,  food,  whether  liq-  piens,  boli  formed  from  natural  bites  (e.g., 
aid  or  solid,  is  carried  backward  through  6-8  g  of  normal  foods)  normatively  form 
the  mouth  to  the  postcanines,  or  from  the  in  the  oropharynx.  In  short,  man  is  a  mam- 
oral  cavity  to  the  pharynx,  on  a  backwardly  mal.  Equally,  we  argue  that  for  ingested 
traveling  tongue  surface  or  by  virtue  of  a  liquids,  the  bolus  is  formed,  contained, 
backwardly  traveling  tongue-palate  con-  and  organized  within  the  oral  cavity,  and 
tact.  For  stage  I  transport,  the  only  differ-  swallowed  therefrom.  We  argue  that  the 
ences  in  the  mechanism,  between  mam-  pivotal  evolutionary  change  in  hominid  de- 
nials studied,  can  be  directly  correlated  velopment  has  been  the  development  of  a 
with  the  length  of  the  tooth  row.  The  pro-  behavioral  mechanism  for  process  man- 
cess  may  take  several  cycles  in  macaque  agement  of  liquids,  which  can  flow,  in  con- 
( German  et  al.,  1989)  but  can  be  accom-  trast  to  solids,  which,  even  when  triturat- 
plished  in  a  single  cycle  in  man  (Hiiemae  ed,  probably  cannot, 
and  Palmer,  in  preparation).  Superficially,  ^(^^(^,  IJSIONq 
the  mechanisms  of  stage  II  transport  show  ^UiNULUoiUiMo 

the  greatest  differences.  In  the  mammals  Jaw,  hyoid,  and  tongue  movements,  dur- 
studied,  except  macaque  and  man,  aliquots  ing  the  rhythmic  cycles  of  normal  feeding 
of  swallowable  food  are  moved  through  in  mammals  including  man,  are  interde- 
the  palatoglossal  arches  (fauces)  during  the  pendent,  that  is,  there  is  a  consistent  event 
upward  and  backward  movement  of  the  order  relationship  between  movements  of 
tongue  in  late  FO  (03)  and  FC  (Hiiemae  the  jaw  and  the  hyoid,  and  the  grosser 
and  Crompton,  1985).  This  is  described  as  movements  of  the  tongue.  This  should  oc- 
the  squeeze-wedge  mechanism.  In  ma-  casion  no  surprise  given  the  physiological 
caque  (Franks  et  al.,  1984,  see  also  Thex-  and  gross  anatomical  homologies  among 
ton  and  Crompton,  1998)  and  man  (Hiie-  the  structural  elements  involved.  That 
mae  and  Palmer,  1999)  the  upward  and  said,  the  available  data  cannot  support  any 
forward  movement  of  the  tongue  in  IP  detailed  conclusions  about  the  actual  be- 
brings  the  anterior  surface  of  the  tongue  havior  of  the  tongue  surface  during  feed- 
into  contact  with  the  anterior  palate,  and  ing  sequences  for  mammals  in  general, 
that  contact  rapidly  spreads  backward  However,  if  food  is  to  be  of  metabolic  util- 
( middle  and  posterior  tongue)  forcing  the  ity,  it  has  to  reach  the  gastrointestinal  tract 
food  mass  through  the  fauces.  This  mech-  for  chemical  digestion.  A  primary  role  of 
anism,  squeeze-back,  depends  on  forward  the  tongue— hyoid  complex  is  the  move- 
movement  of  the  tongue  coupled  with  a  ment  of  swallowable  food  into  the  pharynx 
posteriorly  traveling  tongue-palate  con-  for  bolus  formation  and  then  deglutition, 
tact.  Although  the  mechanisms  of  stage  I  and 

All  nonanthropoid  mammals  form  the  stage  II  transport  are  now  well  document- 
bolus  in  the  oropharynx  (piriform  fossae-  ed  (at  least  for  representative  species,  see 
valleculae).  Without  prejudice  to  the  air-  Hiiemae,  2000;  Hiiemae  and  Crompton, 
way,  given  an  intranarial  larynx,  the  bolus  1985;  Hiiemae  and  Palmer,  1999),  the  pre- 
is  moved  into  the  esophagus  from  the  oro-  cise  role  of  the  pattern  of  complex  and 
pharynx  (see  Thexton  and  Crompton,  poorly  understood  changes  in  tongue  sur- 
1998).  It  has  long  been  axiomatic  that  man  face  position  and  shape  during  intraoral 
is  different  because  in  Homo  sapiens,  the  food  management  are  not. 
bolus  is  formed  in  the  oral  cavity  and  pro-  The  available  data  do  support  a  generic 
pulsively  expelled  across  the  oropharynx,  mammalian  model  that  posits  that  two  cy- 


214         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


clical,  linked  but  not  interlocked  mecha- 
nisms are  operative  during  feeding  se- 
quences in  mammals.  Cyclical  jaw  move- 
ments position  the  teeth  for  food  reduc- 
tion in  SC,  and  then  complete  a  cycle  to 
reposition  the  teeth  for  the  next  chewing 
stroke.  Concomitantly,  the  hyolingual  sys- 
tem is  also  cycling.  Tongue  movements,  fa- 
cilitated by  changes  in  gross  tongue  posi- 
tion as  a  function  of  hyoid  moveinent,  and 
implemented  by  changes  in  tongue  sur- 
face—palate contacts,  manipulate  and 
transport  food  within  and  through  the  oral 
cavity  during  the  SO-FO  and  FC  phases 
of  the  jaw  inovement  cycle.  Although  the 
order  of  events  is  the  same  for  all  the 
mammals  studied,  the  temporal  linkages 
between  them  seem  tighter  in  opossum 
and  hyrax,  where  the  start  of  tongue  and 
hyoid  protrusion  is  closely  associated  with 
minimum  gape.  In  macaque  and  man, 
both  of  which  have  more  vertically  orient- 
ed tongues,  the  definitive  (functional)  for- 
ward movement  begins  during  IP  and,  at 
least  in  macaque,  ends  with  the  last  rate 
change  in  opening.  Rate  changes  do  occur 
in  opening  in  man,  but  are  only  clearly  as- 
sociated with  cycles  in  which  stage  II 
transport  is  occurring  (work  in  progress). 

These  conclusions  are,  of  necessity, 
based  largely  on  qualitative  data.  What  in- 
ferences can  be  drawn  as  to  why  this  pat- 
tern is  present  and  whether  it  evolved 
from  an  antecedent  premammalian  pat- 
tern? For  most  mammals,  solid  food  has 
to  be  processed  before  it  can  be  swal- 
lowed, requiring  powered  tooth— food- 
tooth  contact,  that  is,  the  jaws  have  to  sep- 
arate and  then  close  with  the  food  posi- 
tioned between  the  teeth.  The  tongue,  giv- 
en the  variable  development  of  highly 
mobile  cheeks  in  nonanthropoid  mam- 
mals, is  the  primary  agent  for  food  manip- 
ulation and  positioning.  Clearly,  food  po- 
sitioning must  occur  in  advance  of  a  power 
stroke  if  such  is  to  be  effective  and  the 
tongue  not  be  traumatized.  The  amplitude 
of  jaw  movement  must  be  such  as  to  allow 
large  bites  of  material  to  be  properly  po- 
sitioned. It  is  possible  that  the  rotational 


movements  of  the  tongue  surface  associ- 
ated with  food  positioning  are  a  mamma- 
lian adaptation. 

Equally,  we  argue  that,  both  ontogenet- 
ically  and  phylogenetically,  the  fundamen- 
tal functional  mammalian  behavior  is  food 
transport.  Liquids,  requiring  no  process- 
ing, are  simply  moved  through  the  mouth, 
into  the  oropharynx,  and  swallowed.  The 
rhythmic  cycle  of  hyolingual  movement  is 
the  conveyor  belt  moving  material  back- 
ward. Tongue  contacts  with  the  hard  pal- 
ate act  as  the  stop  to  ensure  the  unidirec- 
tional (posterior)  movement  of  food.  In 
mammalian  lapping,  the  amplitude  of  jaw 
movement  is  miniinal,  sufficient  to  pro- 
trude the  tongue,  allow  it  to  collect  an  al- 
iquot, and  then  retract.  This  low-ampli- 
tude gape  (02)  is  maintained  as  the 
tongue  completes  its  aliquot  collection. 
The  jaw  cycle  is  modified  when  solid  food 
requiring  processing  is  introduced.  The 
FO  phase,  with  a  longer  close  (FC  and 
SC)  appears.  The  underlying  hyolingual 
cycle  remains  the  same,  its  reversal  from 
foiAvard  to  backward  movement  occurring 
at  a  gape  in  the  range  associated  with  lap- 
ping. 

What  is  significant  is  that  every  mammal 
studied  adopts,  within  and  between  se- 
quences, a  cyclical  behavior  that  can,  post 
hoc,  be  correlated  with  the  initial  consis- 
tency of  the  food,  and  by  inference,  with 
the  effect  of  its  processing.  This,  given  that 
functional  behavior  can  change  from  cycle 
to  cycle,  implies  continuous  sensory  feed- 
back to  the  CNS,  which  regulates  the  out- 
put from  the  CPG(s)  producing  rhythmic 
jaw  and  hyolingual  movement. 

As  Bramble  and  Wake  (1985)  observed, 
mammals  are  by  no  means  unique  in  hav- 
ing jaws  and  a  hyolingual  complex.  Their 
model  for  solid  food  transport  in  general- 
ized terrestrial  tetrapods  looks,  as  they 
stated,  functionally  very  similar  to  that 
documented  for  solid  food  transport  in 
mammals:  the  hyolingual  complex  is  pro- 
truded as  the  jaws  open  and  retracted  dur- 
ing jaw  closure.  Does  a  commonality  of 
outcome  (food  delivered  to  the  digestive 


Tongue-Jaw  Linkages  •  Hiiemae  and  Palmer        215 


tract)  require  a  commonality  of  mecha- 
nism? This  is  the  issue  at  the  core  of  the 
question  posed  by  Smith  (1994)  when  she 
addressed  the  question:  is  this  consistent 
pattern  reflective  of  a  'conserved  neuro- 
motor system'?  Two  issues  must  be  ad- 
dressed. The  first,  given  phylogenetically 
old  osseocartilaginous  and  soft  tissue  ele- 
ments, connected  by  muscle  blocks  ar- 
ranged to  generate  movement  in  specific 
directions,  is  biomechanical.  What  muscle 
blocks  contract  in  what  way  to  produce 
what  result  temporally  and  spatially?  Do 
they  do  so  in  a  predictable  and  patterned 
order?  If  viewed  simply  as  jaw  elevators 
and  depressors,  and  hyolingual  protractors 
and  retractors,  then  the  activity  of  those 
muscle  blocks,  as  modeled  by  Bramble 
and  Wake  (1985),  could  represent  the  sub- 
strate on  which  the  more  complex  mam- 
malian pattern  evolved. 

We  argue  that,  given  our  current  knowl- 
edge of  the  CNS  control  of  rhythmic  jaw- 
hyolingual  behaviors  in  mammals  and  in 
nonmammalian  tetrapods,  it  is  premature 
to  focus  on  neuromotor  systems  per  se. 
(Given  the  foregoing,  one  might  ask  "what 
is  a  neuromotor  system":  anatomically  or 
Rmctionally  homologous  structures?)  It  is 
now  clear  that  complex  CNS  linkages  form 
the  CPGs  for  rhythmic  jaw  movement  and 
swallowing  in  mammals  (Dellow  and 
Lund,  1971;  Jean,  1990),  although  how 
linked  tongue  rhythmic  behavior  fits  into 
those  identified  CPGs  is  not  yet  known. 
However,  we  do  know  that  there  is  a  com- 
plex, and  probably  itself  experientially 
modulated,  web  of  interconnectivity  be- 
tween the  sensory  and  motor  nuclei  in  the 
pons  and  medulla  for  all  the  cranial  nerves 
(CN  V,  VII,  IX,  X,  XI,  XII)  involved.  The 
importance  of  smell  and  taste  in  the  selec- 
tion of  foods  for  transport  and  processing 
(Gilbertson,  1998)  cannot  be  ignored:  in- 
put from  those  sensors  clearly  affects  feed- 
ing behavior.  At  a  time  when  the  sources 
of  sensory  input  from  the  mammalian  oro- 
facial complex  modulating  rhythmic  motor 
output  are  a  matter  of  dispute,  broader- 
brush  inferences  for  the  evolution  of  these 


functional  behaviors  and  their  control  in 
terrestrial  tetrapods  are  intriguing.  Nev- 
ertheless, as  such,  they  hopefully  can  serve 
as  a  stimulus  to  further,  and  difficult,  re- 
search focused  on  the  CNS  rather  than  on 
the  qualitative  analysis  of  functional  be- 
haviors as  the  basis  for  modeling  CNS  con- 
trol mechanisms. 

ACKNOWLEDGMENTS 

This  review  is  dedicated  to  A.  W. 
Crompton  (A.  W.  C),  without  whose  sup- 
port and  encouragement  (especially  for  K. 
M.  H.  in  the  late  1960s  through  early 
1970s)  much  of  this  body  of  research  could 
never  have  been  accomplished.  Almost  all 
of  the  authors  cited  in  the  Appendix  were 
participants  or  beneficiaries  of  the  Yale 
and  then  the  Museum  of  Comparative  Zo- 
ology research  effort  that  A.  W  C.  over- 
saw. Since  1991,  Syracuse  University  Bio- 
engineering  undergraduates  electing  Se- 
nior Thesis  Research  in  K.  M.  H.'s  labo- 
ratory at  the  Institute  for  Sensory 
Research  have  made  much  of  the  analysis 
reported  here  possible  (1992-1999).  We 
also  acknowledge  the  superb  technical 
support  afforded  by  Xuezhen  Wu  and 
Chune  Yang  in  Jeffrey  Palmer's  laboratory 
at  Johns  Hopkins  University.  U.S.  Public 
Health  Ser\dce  Awards,  first  NIH  DE 
05738,  and  later  NIH  DC  02123,  aug- 
mented by  institutional  resources  (Syra- 
cuse University  and  Johns  Hopkins  Uni- 
versity), supported  this  research. 

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APPENDIX 

The  following  lists  those  mammals  for 
which  data  on  tongue  and  hyoid  move- 
ment in  feeding  are  available,  with  the 
sources  used  in  preparing  this  review.  The 
order  represents  the  approximate  chronol- 
ogy of  these  studies. 

Opossum  {Didelphis  virginiana) 

CFG  (lateral  projection),  EMG,  tongue 
and  hyoid  luarkers. 

Sources.  Crompton,  1989;  Crompton  et 
al.,  1977;  Hiiemae  and  Crompton,  1985; 
Thexton  and  Crompton,  1989,  1998. 

Cat  (Felis  domesticus) 

CFG  (lateral  projection),  tongue  and 
hvoid  markers. 

J 

Sources.  Hiiemae  et  al.,  1978;  Thexton 


and  McGarrick,  1988,  1989;  Thexton  et  al., 
1980,  1982. 

Fruit  bat  {Pteropus  giganteus) 

CFG   (lateral  and  dorsoventral  projec- 
tion), tongue  (10)  and  hyoid  markers. 
Source,  de  Gueldre  and  De  Vree,  1984. 

Macaque  {Macaca  fascicularis) 

CFG  (lateral  projection),  EMG,  tongue 
and  hyoid  ixiarkers. 

Sources.  Franks  et  al.,  1984;  German  et 
al.,  1989;  Hiiemae  and  Crompton,  1985; 
Hiiemae  et  al.,  1995. 

Tenrec  {Tenrec  ecaudatus) 

CFG   (lateral  and  dorsoventral  projec- 
tions), EMG,  tongue  and  hyoid  markers. 
Source.  Oron  and  Crompton,  1985. 

Hyrax  {Procavia  syriacus) 

CFG  (lateral  projection),  tongue  and 
hyoid  markers. 

Sources.  Franks  et  al.,  1985;  German 
and  Franks,  1991. 

Rabbit  {Oryctolagus  cuniculus) 

VFG  (lateral  and  dorsoventral  projec- 
tion), hyoid  marker,  tongue  and  hyoid 
markers. 

Sources.  Anapol,  1988;  Cortopassi  and 
Muhl,  1990. 

IVIan  {Homo  sapiens  sapiens) 

VFG  (lateral  and  posteroanterior  pro- 
jection), EMG,  tongue  and  hyoid  markers. 

Sources.  Hiiemae  and  Palmer,  1999; 
Palmer  et  al.,  1992,  1997. 


EXTRINSIC  VERSUS  INTRINSIC  LINGUAL  MUSCLES: 
A  FALSE  DICHOTOMY? 


KURT  SCHWENK^ 

Abstract.  The  muscular  tongue  of  amniote  verte- 
brates is  traditionally  described  as  a  composite  of  two 
muscle  types:  extrinsic  muscles  originate  outside  the 
tongue  and  insert  within  it;  intrinsic  muscles  arise  and 
insert  completely  within  the  tongue.  Whole-tongue 
movements  are  attributed  to  the  former,  lingual 
shape  change  to  the  latter.  This  dichotomous  view  of 
tongue  structure  and  function  has  endured  since  the 
mid-19th  century,  despite  persistent  indications  of  its 
inadequacy.  A  histologic  analysis  of  the  musculi  ge- 
nioglossus  and  verticalis  in  mammals  and  the  mus- 
culus  (m.)  hyoglossus  in  lepidosaurian  reptiles  finds 
that  the  "extrinsic"  m.  genioglossus  contributes  exten- 
sively to  the  "intrinsic"  m.  verticalis;  the  verticalis 
"muscle"  is  composed  of  fibers  from  at  least  three 
nominally  separate  muscles,  both  extrinsic  and  intrin- 
sic (genioglossus,  longitudinahs  inferior,  intrinsic  ver- 
ticalis fibers);  and  the  "extrinsic"  m.  hyoglossus  in  lep- 
idosaurs  comprises  both  extrinsic  and  intrinsic  parts, 
which  may  be  histochemically  differentiated.  Current 
models  of  the  tongue  as  a  muscular  hydrostat  suggest 
tliat  it  functions  as  an  integrated  functional  unit  and 
that  the  traditional  atomistic,  dichotomous  view  is  in- 
accurate and  misleading.  The  notion  of  individuated 
"muscles"  is  inapplicable  within  the  tongue  and 
should  be  replaced  by  reference  to  "fiber  systems." 

Apart  from  simplifying  matters  to  the  student  of 
anatomy,  the  division  of  the  lingual  muscles  into 
extrinsic  and  intrinsic  groups  is  of  no  proper  sci- 
entific significance  (Abd-El-Malek,  1938:  26) 

INTRODUCTION 

The  evolution  of  tetrapod  vertebrates 
from  piscine  ancestors  was  attended  by  the 
appearance  of  a  mobile,  muscular  tongue. 
The  tongue,  in  effect,  assumed  the  ances- 
tral role  of  water  in  the  dynamics  of  feed- 
ing and  is  used  by  tetrapods  today  to  cap- 
ture, support,  manipulate,  transport,  and 


'  Department  of  Ecology  and  Evolutionary  Biology, 
University  of  Connecticut,  Storrs,  Connecticut 
06269-3043. 


swallow  prey  in  the  terrestrial  environ- 
ment. These  functions  depend  on  the  ca- 
pacity of  the  tongue,  and  the  associated 
hyobranchial  apparatus,  to  generate  com- 
plex movements  in  three  dimensions, 
within  the  mouth  and  without.  The  fonn 
and  internal  anatoiny  of  the  tongue  vary 
widely  among  tetrapods,  as  does  the  na- 
ture and  extent  of  its  movements  (e.g., 
Livingston,  1956;  Schwenk,  2000a).  Mam- 
mals, lepidosaurian  reptiles  and  terrestrial 
turtles  possess  the  most  inuscular  and  ar- 
chitecturally intricate  tongues  among  tet- 
rapods, and  these  evince  the  greatest  com- 
plexity of  motion.  Contradictions  about  the 
muscular  constituents  of  these  amniote 
tongues  and  their  role  in  generating 
tongue  movement  is  the  subject  of  this  pa- 
per. 

The  tongue  of  inost  nonarchosaurian 
amniotes  is  a  large,  inuscular  mass,  often 
with  little  or  no  internal  skeletal  support. 
The  corpus  of  the  tongue  comprises  or- 
thogonal arrays  of  interweaving  muscle  fi- 
bers, the  pattern  of  which  is  taxonomically 
variable.  Despite  extensive  comingling  of 
muscle  fibers  within  the  tongue,  early 
anatomists  treated  the  tongue  like  any  oth- 
er part  of  the  musculoskeletal  system  and 
partitioned  it  into  nominally  discrete  mus- 
cles. Initially,  virtually  all  tongue  muscles 
were  thought  to  arise  from  elements  of  the 
skeleton  outside  the  tongue  (e.g.,  the  man- 
dible, hyobranchium,  and  styloid  process 
of  the  skull  in  mammals)  and  the  muscles 
were  divided  on  the  basis  of  their  separate 
origins  (Barnwell,  1976).  However,  by  the 
early  19th  century  it  was  recognized  that 
some  inuscle  fibers  arise  and  insert  entire- 


Bull.  Mus.  Comp.  Zool.,  156(1):  219-235,  October,  2001         219 


220         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


ly  within  the  tongue  and  several  "intrinsic 
muscles"  were  thus  recognized  in  addition 
to  the  better  known  "extrinsic  muscles" 
(Barnwell,  1976).  Intrinsic  muscles  were 
identified  on  the  basis  of  their  direction 
(transverse,  longitudinal,  or  circular)  and 
position  (superior/dorsal  or  inferior/ven- 
tral) within  the  tongue. 

The  distinction  between  extrinsic  and 
intrinsic  muscles  was  formalized  by  Salter 
(1852;  in  Barnwell,  1976)  who,  in  addition, 
attributed  different  kinds  of  tongue  move- 
ment to  the  two  muscle  types:  extrinsic 
muscles  were  said  to  move  the  whole 
tongue  by  virtue  of  dieir  external  skeletal 
attachments,  whereas  intrinsic  muscles 
were  thought  to  "move  the  tongue  on  it- 
self." Thus,  by  the  mid-19th  century,  two 
parallel  dichotomies  were  established  in 
the  literature:  an  anatomical  division  of  the 
tongue  into  extrinsic  and  intrinsic  muscles, 
and  a  functional  division  relating  the  for- 
mer to  w^hole  tongue  movements  and  the 
latter  to  changes  in  tongue  shape. 

Remarkably,  this  dichotomous  view  of 
tongue  form  and  function  has  endured  in 
the  literature  to  the  present  time  (e.g., 
Sonntag,  1925;  McGregor,  1938;  Bennett 
and  Hutchinson,  1946;  Cooper,  1953;  Liv- 
ingston, 1956;  Oelrich,  1956;  Sondhi, 
1958;  Bowman,  1968;  Perkell,  1969;  War- 
wick and  Williams,  1973;  Miyawaki,  1974; 
Barnwell  et  al.,  1978b;  Langdon  et  al., 
1978;  Hellstrand,  1980,  1981;  Tanner  and 
Aveiy,  1982;  Schwenk,  1986;  Smith,  1988; 
Delheusy  et  al,  1994;  Herrel  et  al.,  1995). 
For  example,  in  describing  a  lizard  tongue, 
Oelrich  (1956:  54)  stated:  "The  extrinsic 
muscles,  genioglossus  and  hyoglossus,  con- 
trol the  motions  of  the  tongue;  the  intrin- 
sic muscles  control  its  shape."  Hellstrand 
(1980:  187)  began  his  paper  on  the  cat 
tongue  by  pointing  out  that  it  "is  provided 
with  muscles  termed  extrinsic  or  intrinsic 
according  to  whether  they  run  partly  or 
totally  within  the  tongue.  Functionally,  the 
extrinsic  muscles  are  usually  classified  as 
protruders  or  retractors  and  the  intrinsic 
as  shaping  or  modeling  agents."  In  Gray's 
Anatomy    (Warwick   and  Williams,    1973: 


1239,  1240)  it  is  noted  that  within  the  hu- 
man tongue,  "there  are  two  sets  of  mus- 
cles, extrinsic  and  intrinsic;  the  former 
have  attachments  outside  the  tongue,  the 
latter  are  contained  within  it."  Each  ex- 
trinsic muscle  is  said  to  move  the  tongue 
in  some  way,  that  is,  retract,  depress,  or 
elevate  it.  In  contrast,  it  is  held  that  the 
intrinsic  muscles,  in  toto,  are  "mainly  con- 
cerned in  altering  the  shape  of  the 
tongue." 

Despite  the  persistence  of  the  dichoto- 
mous descriptive  convention,  those  who 
have  investigated  tongue  anatomy  in  some 
detail  have  often  questioned  the  accuracy 
or  appropriateness  of  the  dichotomy — an- 
atomically, functionally,  or  in  both  ways 
(e.g.,  Bennett,  1935;  Abd-El-Malek,  1938; 
Bennett  and  Hutchinson,  1946;  Sondhi, 
1958;  Barnwell  et  al.,  1978a;  Langdon  et 
al.,  1978;  Cave,  1980;  Lowe,  1980;  Kier 
and  Smith,  1985;  Schwenk,  1986;  Smith, 
1986,  1992;  Smith  and  Kier,  1989;  Sokoloff 
and  Deacon,  1992;  Napadow  et  al,  1999). 
Some  authors  have  expressed  doubt,  even 
while  beginning  with  the  conventional 
view.  Oelrich  (1956:  55),  for  example,  not- 
ed that  extrinsic  and  intrinsic  fibers  inter- 
lace within  the  tongue  and  admitted  that 
the  intrinsic  muscles  "do  not  maintain 
their  integrity  throughout,  but  at  some  lev- 
els are  intermingled  to  such  an  extent  that 
their  identity  is  obscured."  Schwenk 
(1986:  137)  pointed  out  that  in  tuatara 
(Sphenodon),  the  "distinction  is  not  always 
demonstrable  in  eveiy  part  of  the  tongue 
because  both  intrinsic  and  extrinsic  fibers 
interlace  complexly."  Barnwell  et  al. 
(1978a:  8)  concluded  that  the  nominally 
intrinsic  musculus  (m.)  longitudinalis  su- 
perior of  the  huinan  tongue  "is  comprised 
of  both  intrinsic  and  extrinsic  fiber 
groups."  It  is  telling  that  many  writers 
seem  compelled  to  state  the  conventional 
view,  despite  their  evident  dissatisfaction. 
This  ambivalence  is  clear,  for  example,  in 
a  textbook  account  that  virtually  contra- 
dicts itself  within  the  space  of  two  sen- 
tences: "Generally,  'movements'  other 
than  those  that  basically  alter  the  shape  of 


Tongue  Muscles  •  Schwenk       221 


the  tongue  are  the  result  of  contractions  of 
the  extrinsic  muscles,  though  one  group 
seldom  functions  alone.  The  overlapping, 
intermingling,  and  decussating  nature  of 
the  intrinsic  and  extrinsic  inuscle  groups 
permit  the  fine  coordinated  effort  so  nec- 
essary in  speech"  (Hiatt  and  Gartner, 
1982:  239-240). 

Others  have  rejected  the  traditional  di- 
chotomy altogether.  For  example,  in  his 
study  of  cat  tongue  anatomy  and  function, 
Abd-El-Malek  (1938)  concluded  with  the 
remark  quoted  at  the  outset  of  this  paper, 
suggesting  that  the  dichotomy  is  no  more 
than  a  convenience,  without  scientific 
merit.  He  particularly  rejected  the  func- 
tional dichotomy,  suggesting  that  "most,  if 
not  all,  of  the  intrinsic  muscles  are  in- 
volved in  every  movement  of  the  tongue. 
Indeed,  in  many  movements  both  intrinsic 
and  extrinsic  muscles  so  called,  are  work- 
ing together."  Other  authors  take  the  rad- 
ical view  that  all  putative  intrinsic  muscle 
fibers  are  nothing  more  than  extensions  of 
extrinsic  muscles  (Lesbre  [1922]  in  Cave 
[1980]  for  the  horse,  Eqiiiis;  Cave  [1980] 
for  the  rhinoceroses.  Rhinoceros,  Cera- 
totheriiini,  and  Diceros;  and  Sondhi  [1958] 
for  the  monitor  lizard,  Varanus).  Accord- 
ing to  Cave  (1980:  128):  "The  so-called  in- 
trinsic tongue  muscles  are  not  therefore, 
morphological  entities  but  merely  contin- 
uations of  the  extrinsic  muscles."  Sondhi 
(1958:  175)  concluded:  "While  there  can 
be  no  doubt  that  the  'intrinsic  muscles'  can 
be  distinguished  from  each  other  in  cer- 
tain regions  of  the  tongue,  the  fact  that 
they  arise  directly  as  a  result  of  the  change 
in  course  of  certain  bundles  of  the  [extrin- 
sic] hyoglossus  fibres  indicates  that  they  do 
not  deserve  the  status  of  independent 
muscles."  It  is  worth  noting  that  the  stud- 
ies of  Lesbre  and  Cave  were  based  on 
gross  dissection  without  the  benefit  of  his- 
tologic sections,  and  Sondhi's  sections 
were  of  poor  quality. 

The  purpose  of  this  paper  is  to  explore 
the  anatomical  relationship  between  "ex- 
trinsic" and  "intrinsic"  lingual  muscles  in 
representative  mammals  and  lepidosaurian 


reptiles.  The  mammalian  genioglossus  and 
verticalis  muscles,  and  lepidosaurian  hyo- 
glossus muscle  are  investigated  in  detail 
and  used  as  exemplars.  Results  of  the  mor- 
phologic investigation  are  considered  in 
light  of  current  models  of  tongue  function 
in  order  to  assess  the  structural  and  func- 
tional validity  of  the  dichotomous  view. 
Based  on  this  analysis,  a  synthetic  view  of 
tongue  form  and  function  is  proposed. 

MATERIALS  AND  METHODS 

Reference  material  included  complete, 
serial  paraffin  sections  of  tongues  from  two 
mammalian  species  (domestic  cat.  Fells  ca- 
tus,  three  specimens;  crab-eating  ma- 
caque, Macaca  fascicularis,  three  speci- 
mens) and  more  than  100  lepidosaurian 
reptile  species  (one  to  three  specimens 
each),  including  tuatara  (Sphenodon  piinc- 
tatus;  Schwenk,  1986)  and  representatives 
of  every  major  squamate  clade  (Schwenk, 
1988,  2000b,  unpubfished  data).  The  em- 
phasis here  is  on  the  cat  (Camivora,  Feli- 
dae)  and  generalized  lizards  (Squamata, 
Iguanidae)  that  putatively  retain  the  ple- 
siomorphic  condition  (Schwenk,  1986, 
1988,  2000b).  Histologic  results  were  com- 
pared to  literature  accounts  of  tongue 
anatomy. 

Sections  were  prepared  using  standard 
paraffin  techniques  (Presnell  and  Schreib- 
man,  1997).  Whole-tongue  specimens 
were  sectioned  whenever  possible  to  facil- 
itate fiber  tracing.  Some  previous  studies 
have  suffered  from  the  myopic  view  of- 
fered by  partial  or  fragmented  specimens. 

Both  transverse  and  sagittal  sections  (6— 
10  |jLm)  were  prepared  for  most  species, 
but  only  transverse  sections  were  available 
for  Sphenodon  and  some  squaiuates  (note 
that  transverse  tongue  sections  correspond 
to  'coronal'  sections  in  the  parlance  of  hu- 
man anatomy).  Sections  were  stained  with 
heiTiatoxylin  and  picro-ponceau  or  hema- 
toxylin and  eosin  (Presnell  and  Schreib- 
man,  1997). 

In  addition  to  paraffin  sections,  frozen 
tissue  sections  were  available  for  several 
squamate  species.  These  were  stained  for 


222         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


myosin  adenosine  triphosphatase  and  sue-  rupted  across  its  width  by  invading  bands 

cinic  dehydrogenase  using  standard  tech-  of  transversus.  However,  interpreting  sec- 

niques,  as  part  of  an  ongoing  histochemical  tions  here  is  difficult  because  the  sheets 

study    of    tongue    muscle    fiber    types  apparently  do  not  run  in  a  plane,  becom- 

(Schwenk    and    Anapol,    in    preparation),  ing  curved  or  cup-shaped,  instead.  Finally 

These  data  are  preliminary  and  referred  to  some  vertical  fibers  cross  anteroposteriorly 

here  only  in  passing.  between  adjacent  sheets  to  form  anasto- 
moses (especially  evident  in  the  free,  an- 

RESULTS  tenor  part  of  the  tongue;  e.g..  Fig.  3).  De- 

Genioglossus  and  Verticalis  Muscles  in  ^P^*^  these  complications,  throughout 

thp  Pflt  most  or  the  tongue  tlie  extreme  regularity 

of  the  alternating  vertical  and  transverse 

Preliminary  observations  indicate  that  sheets  is  its  most  striking  feature.  The 
the  findings  reported  here  for  the  cat  are  sheets  of  vertical  and  transverse  fibers  con- 
equally  valid  for  the  macaque.  Based  on  stitute  the  nominal  intrinsic  muscles,  m. 
consideration  of  the  literature,  the  findings  verticalis  and  m.  transversus,  respectively, 
are  likely  to  apply  as  well  to  many  mam-  In  the  cat  they  are  separated  into  left  and 
mals  with  generalized  tongues,  including  right  moieties  by  a  complete  median  sep- 
other  carnivorans,  opossums,  and  humans,  tum. 

However,  with  the  exception  of  humans.  The  m.  transversus  fibers  originate  from 

detailed  information  is  lacking  for  these  the  median  septum  and  run  radially  across 

and   other   species,   including   many  with  the  width  of  the  tongue  to  insert  into  the 

highly  divergent  tongue  forms  (e.g.,  mono-  lamina  propria  of  the  lingual  tunic  dorsally 

tremes:  Doran  and  Baggett,  1970;  Doran,  laterally,  and  ventrolaterally.  Some  m.  ver- 

1973;  and  nectar-feeding  bats:  Greenbaum  ticalis  fibers  originate  from  the  lamina  pro- 

and    Phillips,    1974;    T    Griffiths,    1978).  pria  of  the  tongue's  ventral  surface  and  nan 

Therefore,  the  results  of  this  study  cannot  dorsomedially  to  the  lamina  propria  of  the 

necessarily  be  extrapolated  to  mammals  as  dorsal  surface  (but  see  below).  In  the  lat- 

a  whole.  eral  part  of  the  tongue,  dorsolaterally  nm- 

When  viewed  in  transverse  section,  ning  transversus  fibers  cross  dorsomedially 
most  mammalian  tongues  are  divisible  into  running  verticalis  fibers  in  an  X-like  pat- 
cortical  and  medullary  regions.  The  cortex  tern  (i.e.,  peipendicular,  but  approximately 
is  distinguished  by  the  presence  of  longi-  45°  to  the  vertical).  Toward  the  midline 
tudinal  fibers,  whereas  the  core  of  the  verticalis  fibers  become  more  nearly  ver- 
tongue  is  filled  with  transverse  and  vertical  tical  (see  below). 

fibers.  "Transverse"  and  "vertical"  are  con-  The  m.  genioglossus  is  one  of  the  major 
venient  descriptors  for  these  more-or-less  extrinsic  muscles  of  the  tongue  and  is  as- 
perpendicular  sets  of  fibers,  but  fibers  of  sumed  to  be  its  principal  protractor  and 
both  groups  are  often  quite  oblique,  protruder.  In  the  cat,  the  m.  genioglossus 
Throughout  most  of  the  medullary  zone,  originates  medially  from  two  heads  on  the 
vertical  and  transverse  fibers  are  organized  mandible  near  the  symphysis.  A  ventral 
into  thin  sheets  of  muscle  that  nm  across  head  gives  rise  to  fibers  that  run  posteri- 
the  width  of  the  tongue,  alternating  one  orly,  inserting  onto  the  anteroventral  sur- 
after  the  other  along  the  tongue's  length  face  of  the  basihval.  Fibers  from  a  larger 
(Fig.  1).  Tracing  individual  verticalis  sheets  dorsal  head  run  posterodorsally  in  a  fanlike 
through  serial  sections  confirmed  that  in  array,  penetrating  the  tongue  midventrally 
most  of  the  tongue  each  sheet  runs  across  along  the  posterior  two  thirds  of  its  length, 
the  full  width  of  the  medullary  core.  How-  The  most  anterior  of  these  fibers  curve 
ever,  in  the  anteriormost  part  of  the  shaiply  dorsad  as  they  enter  the  tongue's 
tongue,   a  verticalis   sheet   may  be   inter-  medullaiy  core  and  nm  vertically  to  the 


Tongue  Muscles  •  Schwenk       223 


Figure  1 .  Alternating  sheets  of  vertical  (musculus  [m.]  verticalis)  and  transverse  (m.  transversus)  muscle  fibers  in  the  medullary 
core  of  the  cat  midtongue.  Note  extreme  regularity  of  alternating  sheets.  (A)  Parasagittal  section;  verticalis  sheets  are  thicker 
than  transversus  sheets  in  this  region.  Anterior  is  to  the  left.  Scale  bar  =  0.2  mm.  (B)  Transverse  section  near  the  midline,  in 
the  ventromedial  portion  of  the  tongue's  right  half;  medial  septum  to  the  right.  Section  is  slightly  oblique  relative  to  plane  of 
transversus  and  verticalis  sheets  so  that  it  passes  through  several  adjacent  layers.  As  for  (A),  note  extreme  regularity  of  alter- 
nating pattern.  Darker-staining  tissue  at  the  margins  of  each  sheet  is  collagenous  connective  tissue  of  the  thin  fascial  plane 
separating  each  sheet.  Note  that  the  ventralmost  transverse  fibers  run  ventrolaterally  and  the  dorsalmost  fibers  run  laterally. 
Dorsal  to  these,  out  of  the  photographic  frame,  the  transverse  fibers  run  dorsolaterally,  that  is,  the  transverse  fibers  radiate 
laterally  from  their  midline  origin  on  the  median  septum.  Scale  bar  =  0.2  mm. 


lamina  propria  of  the  dorsal  surface,  but 
posteriorly  the  fibers  become  progressively 
more  longitudinal,  cuiAdng  gently  dorsad  at 
their  distal  ends  to  meet  the  posterior  sur- 
face of  the  tongue  as  it  slopes  downward 
to  the  root  of  the  tongue.  In  (fetal)  hu- 
mans, the  anteriormost  fibers  form  a  third 
bundle  that  turns  sharply  anterior  as  it  en- 
ters the  tongue,  running  to  the  tip  (Lang- 


don  et  al.,  1978),  but  in  the  cat  (Abd-El- 
Malek,  1938;  this  study)  and  several  other 
mammals  (Doran  and  Baggett,  1972),  no 
comparable  bundle  is  found  and  the  most 
anterior  genioglossus  fibers  run  more  or 
less  vertically.  The  unattached,  anterior 
part  of  the  tongue  is  therefore  devoid  of 
genioglossus  fibers. 

In  reconstructions  of  the  genioglossus. 


224         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


its  fibers  are  often  shown  in  sagittal  view 
to  end  at  the  base  of  the  tongue  before 
penetrating  the  medullary  core,  or  to  run 
obliquely  across  the  alternating  sheets  of 
vertical  and  transverse  fibers  toward  the 
dorsal  and  posterior  surfaces  of  the  tongue 
(e.g.,  Kallius,  1910;  Abd-El-Malek,  1938; 
Warwick  and  Williams,  1973;  Crouch, 
1978;  Walker  and  Homberger,  1992).  In- 
dependence of  the  genioglossus  from  the 
medullary,  intrinsic  fiber  system  is  implied 
in  these  and  other  descriptions.  In  actu- 
ality, as  genioglossus  fibers  turn  dorsally 
into  the  tongue,  they  become  confluent 
with  the  serially  arranged  sheets  of  verti- 
calis  fibers  (Fig.  2A).  As  such,  for  most  of 
the  tongue's  length,  the  medial  portion  of 
the  verticalis  inuscle  comprises  genioglos- 
sus fibers.  In  other  words,  a  large  portion 
of  the  "intrinsic"  verticalis  muscle  is  com- 
posed of  "extrinsic"  fibers. 

Although  the  previous  observations 
seem  to  support  the  radical  position  of 
Cave  (1980)  and  others  suggesting  that  in- 
trinsic fibers  are  merely  extensions  of  ex- 
trinsic muscles,  this  view  is  vitiated  by  a 
full  consideration  of  m.  verticalis  anatomy. 
Although  the  medial  portion  of  each  ver- 
ticalis sheet  comprises  extrinsic  genioglos- 
sus fibers,  its  lateral  portion  derives  from 
purely  intrinsic  fibers  that  originate  on  the 
lamina  propria  of  the  ventral  surface  (Fig. 
2B).  Although  medial  genioglossus  fibers 
are  relatively  vertical  and  lateral  intrinsic 
fibers  are  oblique  (running  dorsomedially; 
see  above),  fibers  of  both  sorts  blend  in- 
sensibly across  the  breadth  of  a  single  ver- 
ticalis sheet  to  form  a  continuous  structur- 
al unit.  These  units  are  repeated  serially 
along  the  length  of  the  tongue,  alternating 
with  sheets  of  m.  transversus.  Extrinsic 
and  intrinsic  components  of  the  verticalis 
are  also  clearly  evident  in  the  opossum, 
Monodelphis  (Smith,  1994,  fig  2a). 

Given  the  absence  of  genioglossus  fibers 
in  the  anterior,  free  part  of  the  tongue,  one 
might  expect  the  sheets  of  verticalis  in  this 
region  to  be  uniformly  intrinsic.  Indeed, 
this  is  true  laterally,  as  elsewhere  in  the 
tongue  (Fig.  3A).  However,  in  place  of  ge- 


I 


Figure  2.  The  relationship  between  musculus  (m.)  verticalis 
and  m.  genioglossus  fibers  in  the  cat  tongue.  (A)  Parasagittal 
section  near  the  midline,  anterior  to  the  left.  Ventrally,  the  ge- 
nioglossus muscle  (g)  penetrates  the  tongue's  medullary  core 
where  it  curves  dorsad  and  is  separated  into  separate  layers 
by  intervening  sheets  of  transversus  fibers  (t).  Thus,  in  this 
medial  portion  of  the  tongue  the  vertical  fibers  of  the  medulla, 
nominally  m.  verticalis  (v),  are  actually  contributed  by  the  ex- 
trinsic genioglossus.  However,  note  that  some  verticalis  fibers 
continue  a  more  vertical  descent  through  the  genioglossus  to 
an  intrinsic  point  of  origin  (curved  arrow).  Scale  bar  =  0.2  mm. 
(B)  Transverse  section  through  the  ventrolateral  part  of  the 
tongue's  right  side  showing  longitudinal  fibers  of  lingual  cortex 
and  the  origin  of  intrinsic  verticalis  fibers  from  the  ventrolateral 
lamina  propria  (arrows).  These  lateral,  purely  intrinsic  fibers, 
form  an  uninterrupted  continuum  within  a  single  verticalis 
sheet  with  the  medial  genioglossus  fibers.  Scale  bar  =  0.2 
mm. 


Tongue  Muscles  •  Schwenk       225 


Figure  3.  The  free,  anterior  portion  of  the  cat  tongue  in  sag- 
ittal section.  The  tongue  tip  is  toward  the  left.  Note  that  longi- 
tudinal fibers  run  beneath  the  tongue's  dorsal  and  ventral  sur- 
faces forming  the  cortex,  whereas  the  medulla  is  filled  by  the 
alternating  sheets  of  vertical  and  transverse  fibers.  These 
sheets  are  not  so  regularly  disposed  as  they  are  posteriorly 
(Fig.  1)  and  anastomoses  between  verticalis  sheets  are  fre- 
quent. (A)  Section  through  lateral  part  of  the  tongue.  Note  that 
vertical  fibers  penetrate  the  cortex  to  arise  and  insert  from  dor- 
sal and  ventral  laminae  propria,  that  is,  they  are  intrinsic  fibers. 
The  dark-staining  structure  just  above  the  ventral  longitudinal 
fibers  is  a  nerve,  kinked  to  permit  extension  during  hydrostatic 
tongue  elongation.  The  white  areas  are  vascular  spaces  slight- 
ly distended  by  perfusion  of  the  tongue.  Scale  bar  =  0.2  mm. 
(B)  Section  more  medial  to  (A),  near  to  midline.  In  contrast  to 


nioglossus  fibers,  the  medial  portion  of 
each  verticalis  sheet  is  here  occupied  by 
ventral  longitudinal  fibers  that  turn  dorsad 
into  the  verticalis  (Fig.  3B).  The  ultimate 
origin  of  all  ventral  longitudinal  fibers  has 
not  been  traced  with  certainty,  but  most 
clearly  belong  to  the  intrinsic  m.  longitu- 
dinalis  inferior.  Among  the  ventral  longi- 
tudinal fibers  of  the  lingual  cortex,  longi- 
tudinalis  inferior  fibers  are  generally  the 
most  median  (e.g.,  Barnwell  et  al.,  1978b). 
Nonetheless,  longitudinal  fibers  of  the  cor- 
tex are  notoriously  difficult  to  segregate 
according  to  source  and  it  remains  possi- 
ble that  some  of  the  fibers  contributing  to 
the  verticalis  in  the  anterior  part  of  the 
tongue  derive  from  the  extrinsic  styloglos- 
sus muscle.  Sections  show  that  styloglossus 
fibers  course  anteroventrally  along  the 
sides  of  the  tongue,  joining  the  ventral  lon- 
gitudinal system  anteriorly,  but  it  is  not 
certain  that  these  fibers  extend  far  enough 
anteriorly  and  medially  to  contribute  to 
the  verticalis  in  the  free  part  of  the  tongue. 
Although  (extrinsic)  m.  hyoglossus  fibers 
are  said  to  nan  \\dthin  the  ventral  longitu- 
dinal system  of  some  inammals  (e.g.,  hu- 
mans, Barnwell  et  al.,  1978b),  my  sections 
(and  those  of  Abd-El-Malek,  1938)  indi- 
cate that  in  the  cat,  all  hyoglossus  fibers 
run  anterodorsally  into  the  dorsal  longitu- 
dinal system. 

In  conclusion,  the  extrinsic  genioglossus 
muscle  makes  a  substantial  contribution  to 
the  putatively  intrinsic  verticalis  muscle. 
Anteriorly,  the  verticalis  also  includes  fi- 
bers of  a  second  intrinsic  muscle,  the  lon- 
gitudinalis  inferior,  and  possibly  extrinsic 
fibers  of  the  st\'loglossus.  The  verticalis 
"muscle"  thus  includes  fibers  from  three, 
or  possibly,  four  different  sources:  intrinsic 
vertical  fibers;  intrinsic  longitudinal  fibers; 
extrinsic  genioglossus  fibers;  and  possibly. 


(A),  vertical  fibers  are  here  contributed  by  the  extensively  de- 
veloped ventral  longitudinal  system.  These  fibers  represent 
musculus  longitudinalis  inferior,  although  it  is  possible  that  ex- 
trinsic styloglossus  fibers  also  contribute.  Compare  to  Figure 
2A.  Scale  bar  =  0.2  mm. 


226         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  4.  Transverse  section  througli  the  midtongue  of  a  lizard  (Holbrookia  texana,  Iguanidae).  The  circular  structure  in  the 
center  is  the  lingual  (entoglossal)  process  of  the  hyobranchium,  which  is  surrounded  by  fibers  of  the  midline  intrinsic  muscle, 
musculus  (m.)  verticalis  (V).  Dorsal  to  the  verticalis  is  the  m.  transversalis  (T)  and  on  either  side  are  the  paired  hyoglossus 
bundles  (H);  the  lateral  part  of  each  bundle  is  cut  off  in  the  figure.  Note  that  within  each  hyoglossus  bundle  the  fibers  are 
separated  into  two  parts:  a  dense,  more  vertically  oriented  dorsolateral  portion  (1)  and  a  more  loosely  organized,  more  longi- 
tudinally oriented  ventromedial  portion  (2).  Scale  bar  =  0.2  mm. 


extrinsic  styloglossus  fibers.  An  individual 
sheet  of  verticalis  occupies  a  transverse 
plane  across  the  width  of  the  tongue  com- 
prising a  continuum  of  vertically  oriented 
muscle  fibers,  yet  within  a  given  sheet,  a 
large  proportion  of  the  fibers  are  contrib- 
uted by  a  nominally  separate  muscle,  usu- 
ally from  outside  the  tongue.  Further- 
more, the  muscles  making  this  contribu- 
tion vary  along  the  length  of  the  tongue. 
Thus,  the  nominal  m.  verticalis  satisfies 
neither  the  definition  of  "intrinsic,"  nor 
even  the  usual  notion  of  a  "muscle."  None- 
theless, the  serial  coherence  of  the  verti- 
calis is  maintained  throughout  the  med- 
ullaiy  core,  despite  the  disparate  sources 
of  its  constituent  fibers. 

The  Hyoglossus  Muscle  in  Lepidosaurlan 
Reptiles 

Lepidosaurs  include  the  tuatara  of  New 
Zealand  (Sphenoclon)  and  the  squamates, 
comprising  lizards,  snakes,  and  amphisba- 
enians.  The  lepidosaurian  tongue,  with  few 
exceptions,  is  a  highly  mobile  organ  that 
rivals  that  of  mammals  in  its  internal  com- 
plexity.   However,    unlike    mammals,    the 


principal  longitudinal  muscles  of  the 
tongue  lie  within  its  core  and  not  its  pe- 
riphery. These  are  the  hyoglossus  muscles, 
evident  in  transverse  section  as  two  large, 
cylindrical  or  subcylindrical  bundles  (Fig. 
4).  In  a  few  taxa  (notably  gekkotans)  they 
subdivide  anteriorly  into  multiple  bundles, 
but  in  the  vast  majority  of  species  they  re- 
main paired  for  the  length  of  the  tongue 
(Schwenk,  1988,  2000b). 

As  in  maminals,  the  hyoglossus  is  one  of 
the  major  extrinsic  muscles  of  the  lepido- 
saurian tongue.  It  is  traditionally  described 
as  originating  on  the  first  ceratobranchial 
of  the  hyobranchial  apparatus  and  insert- 
ing within  the  tongue  near  its  tip  (e.g., 
Gnanamuthu,  1937^  Oelrich,  1956;  Del- 
heusy  et  al.,  1994;  Herrel  et  al,  1997, 
1999)  and  is  regarded  as  the  principal  re- 
tractor of  the  tongue. 

Some  studies  have  indicated  that  hyo- 
glossus anatomy  is  more  complex  than  sug- 
gested by  conventional  descriptions.  In  his 
figures  of  transversely  sectioned  Sphen- 
oclon embryos,  Edgeworth  (1935)  identi- 
fied a  separate  ventromedial  bundle  within 
the  hyoglossal  mass,  which  he  called  the 


Tongue  Muscles  •  Schwenk       227 


isr 

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m  .       *'-v      .t-^ — z* 

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Figure  5.  Transverse  section  through  the  midtongue  of  two 
iguanid  lizards.  (A)  Opiums  sebae.  showing  the  lingual  pro- 
cess and  musculus  (m.)  verticalis  medially,  as  in  Figure  4.  On 
either  side  of  the  verticalis  are  the  hyoglossus  bundles  (trun- 
cated laterally  by  the  photograph)  showing  subdivision  of  the 
muscle  into  three  portions  (1,  2,  3)  indicated  by  differences  in 
fiber  density  and  orientation.  Dorsally,  parts  1  and  2  appear  to 
be  separated  by  a  thin  fascial  plane,  but  ventrally  the  three 
zones  blend  insensibly.  Scale  bar  =  0.4  mm.  (B)  Stenocercus 


longitudinalis  linguae.  Schwenk  (1986)  did 
not  report  such  a  di\dsion  in  his  study  of 
an  adult  specimen,  but  the  sections  reveal 
different  fiber  orientations  in  the  ventro- 
medial and  dorsolateral  portions  of  the 
hyoglossus  bundle,  supporting  the  notion 
of  a  subdivided  hyoglossus  in  Sphenodon. 
Smiths  (1988)  transverse  sections  of  agam- 
id  lizard  tongues  show  distinct  partitioning 
of  the  hyoglossus  into  two  or  three  divi- 
sions. Smith  (1986)  suggested  that  each 
hyoglossus  bundle  within  the  highly  mod- 
ified tongues  of  inonitor  lizards  (Varatms) 
comprises  a  series  of  shorter  fibers  lam- 
ning  obliquely  within  the  longitudinal  bun- 
dle, possibly  spiraling,  and  inserting  into 
the  surrounding  epimysium  along  the 
length  of  the  bundle.  She  disagreed  with 
Sondlii's  (1958)  suggestion  that  hyoglossus 
fibers  in  this  genus  turn  within  the  tongue 
to  form  the  circular  fibers  surrounding  the 
hyoglossus  bundles.  Indeed,  she  showed 
that  the  circular  muscles  were,  themselves, 
composed  of  shorter,  oblique  fibers  ar- 
rayed helically  around  each  hyoglossus 
bundle. 

A  cursory  survey  of  tongue  sections 
from  a  variety  of  species  indicates  that  in- 
ternal hyoglossus  partitioning  is  common- 
place among  lepidosaurs.  Transverse  sec- 
tions of  iguanian  lizards,  in  particular,  of- 
ten reveal  two  (Fig.  4)  or  even  three  (Figs. 
5A,  B)  different  moieties,  as  indicated  by 
fiber  orientation  and,  sometimes,  fascial 
planes.  The  number  and  distinctness  of 
the  hyoglossus  divisions  vary  among  spe- 
cies and,  notably,  along  the  length  of  the 
tongue.  In  some  sections  it  is  evident  that 
one  division  contains  vertically  oriented  fi- 


sp.,  showing  three-part  subdivision  of  the  hyoglossus,  as  in 
(A).  The  dark-staining  band  separating  transverse  fibers  from 
the  verticalis  (v)  and  hyoglossus  (1,  2,  3)  is  the  collagenous 
connective  tissue  of  the  dorsal  transverse  septum.  The  division 
between  verticalis  and  hyoglossus  fibers  is  indicated  on  one 
side  by  three  small  arrows.  Fibers  of  the  middle  hyoglossus 
subdivision  (2)  in  this  part  of  the  tongue  are  vertically  oriented 
and  originate  on  the  dorsal  transverse  septum  (large  arrows). 
These  fibers  represent  an  intrinsic  component  of  the  putatively 
extrinsic  m.  hyoglossus  in  lepidosaurs.  Scale  bar  =  0.1  mm. 


228         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


I  mi] 


Figure  6.  Parasagittal  sections  of  the  tongues  in  two  lizards.  (A)  Sceloporus  sp.  (Iguanidae).  Anterior  to  the  left.  The  dorsal 
surface  of  the  tongue  is  covered  by  long,  filamentous  papillae.  Beneath  the  papillary  surface  is  a  layer  of  intrinsic  longitudinal 
and  transverse  fibers.  Directly  beneath  the  latter  is  the  dark-staining  connective  tissue  band  of  the  dorsal  transverse  septum 
(arrows).  The  plane  of  section  passes  through  the  verticalis  (v)  posteriorly  and  the  hyoglossus  (i  and  e)  anteriorly.  Note  that  the 
longitudinal  hyoglossus  bundle  occupies  the  depth  of  the  tongue  from  the  transverse  septum  dorsally  to  the  base  of  the  tongue 
ventrally  (compare  Figs.  4  and  5).  The  extrinsic  hyoglossus  is  shown  here  to  consist  of  an  intrinsic  component  (i),  originating  on 
the  dorsal  transverse  septum  and  running  anteroventrally  toward  the  tongue  tip,  and  an  extrinsic  component  (e),  running  anter- 
odorsally  from  the  hyobranchium  (the  posterior  extent  of  this  muscle  is  not  evident  in  this  section).  Scale  bar  =  0.2  mm.  (B) 
Gonatodes  antillensis  (Gekkonidae).  Anterior  to  the  right.  In  gekkotans  and  other  scleroglossan  squamates,  the  dorsal  transverse 
septum  is  weakly  developed  or  absent.  Nonetheless,  the  hyoglossus  bundle  comprises  fibers  with  an  intrinsic  origin  (i)  and  an 
extrinsic  origin  (e),  as  in  (A).  Scale  bar  =  0.2  mm. 


bers  taking  origin  from  the  connective  tis- 
sue plane  of  the  dorsal  transverse  septum 
(Fig.  5B).  Sagittal  sections  reveal  that 
these  fibers  form  a  substantial  bundle  run- 
ning anteroventrally  froin  the  dorsal  trans- 
verse septum  to  the  tongue  tip,  joining  an- 
terodorsally  directed  fibers  arriving  from 


the  hyobranchium  (Fig.  6).  In  transverse 
section  these  separate  groups  of  fibers  are 
evident  as  the  aforementioned  subdivi- 
sions within  the  hyoglossus  bundle.  In  oth- 
er words,  the  hyoglossus  inuscle  in  most 
lepidosaurs  minimally  includes  two  dis- 
tinct components:  an  intrinsic  part,  origi- 


Tongue  Muscles  •  Schwenk       229 


nating  within  tlie  tongue  from  the  dorsal 
transverse  septum,  and  an  extrinsic  com- 
ponent, originating  from  the  hyobran- 
chium. 

This  brief  characterization  does  not  cap- 
ture the  full  complexity  of  the  hyoglossus 
muscle.  Changes  in  cross-sectional  shape 
of  individual  fibers  along  the  length  of  the 
tongue  suggest  some  degree  of  spiraling 
within  the  bundle  so  that  extrinsic  and  in- 
trinsic fibers  are  interwoven.  As  such,  the 
number,  form,  and  distinctness  of  the  hyo- 
glossus divisions  vary  anteroposteriorly. 
However,  no  matter  how  great  its  internal 
complexity,  conser\'atively  two  different 
sources  of  fibers  contribute  to  the  hyo- 
glossus muscle,  including  one  that  is  fully 
intrinsic. 

Analysis  of  preliminary  data  indicates 
that  the  intrinsic  component  of  the  hyo- 
glossus is  histochemically  distinct  in  iguan- 
ids  (Sceloporus  graciosus  and  Phnjtiosorna 
platijrhinos)  and  a  gecko  (unidentified 
species),  but  not  in  a  teiid  {Ameiva  un- 
dulatus).  In  Varanus  niloticus,  the  hyo- 
glossus is  neither  subdivided  nor  does  it 
show  histochemically  distinct  compart- 
ments (Schwenk  and  Anapol,  in  prepara- 
tion). This  is  consistent  with  Smiths  (1986) 
interpretation  of  hyoglossus  anatoiny  in 
Varanus.  The  tongues  of  Ameiva  and  Var- 
anus are  both  specialized  for  rapid  length- 
ening of  the  tongue  for  chemosensory 
tongue-flicking  (Smith,  1984,  1986; 
Schwenk,  2000b),  whereas  iguanids  and 
gekkotans  exhibit  more  variable  and  com- 
plex lingual  shape  changes  associated  with 
feeding  and  other  behaviors.  It  is  tempting 
to  relate  the  different  histochemical  pro- 
files to  these  functional  differences,  but 
this  is  highly  speculative  at  this  point. 

In  summary,  the  putatively  extrinsic 
hyoglossus  muscle  includes  both  an  extrin- 
sic and  an  intrinsic  component  in  many,  if 
not  most,  lepidosaurian  reptiles.  The  in- 
trinsic component  originates  from  the  dor- 
sal, transverse  septum  in  the  posterior  and 
midtongue  and  runs  anteroventrally  to  the 
tongue  tip.  The  extrinsic  component  arises 
from  the  first  ceratobranchial  of  the  hyob- 


ranchiuin  and  runs  anterodorsally  to  the 
tongue  tip.  It  is  likely  that  these  fiber 
groups  spiral  and  are  complexly  interwo- 
ven, changing  orientation  along  the  length 
of  the  tongue.  The  intrinsic  fiber  compo- 
nent is  histochemically  distinct  in  basal  liz- 
ards with  functionally  generalized  tongues. 

DISCUSSION 

The  Anatomical  Dichotomy 

The  results  of  this  study  clearly  indicate 
the  inadequacy  of  segregating  tongue  mus- 
cles into  "extrinsic"  and  "intrinsic"  types. 
Indeed,  the  traditional  notion  of  what  con- 
stitutes a  "muscle,"  based  as  it  is  on  more 
typical  components  of  the  musculoskeletal 
system,  inay  be  inapplicable  within  the 
tongue.  Only  three  muscles  were  consid- 
ered here  in  any  detail,  but  comparable 
issues  arise  for  nearly  every  noininal  inus- 
cle  in  the  amniote  tongue.  The  genioglos- 
sus  is  putatively  an  extrinsic  muscle,  but  it 
contributes  substantially  to  the  vertical  fi- 
ber  system  of  the  tongue's  medullary  core, 
presumed  to  consist  of  intrinsic  fibers. 
Conversely,  the  putatively  intrinsic  verti- 
calis  muscle  is  largely  composed  of  extrin- 
sic (genioglossus)  fibers,  as  well  as  fibers 
from  one  to  two  other  nominally  separate 
muscles  (longitudinalis  inferior  and  stylo- 
glossus). The  lepidosaurian  hyoglossus  is 
putatively  an  extrinsic  muscle,  but  a  large 
portion  of  its  fibers  arises  intrinsically. 
Thus,  the  dichotomous  view  of  tongue 
musculature  is  falsified. 

The  Functional  Dichotomy 

Tongue  movement  derives  from  one  or 
a  combination  of  three  different  mecha- 
nisms evident  among  tetrapods:  (1)  whole- 
tongue  movement  coupled  to  hyobranchial 
movement;  (2)  whole-tongue  movement 
independent  of  hyobranchial  movement; 
or  (3)  length  or  shape  changes  intrinsic  to 
the  tongue  and  independent  of  hyobran- 
chial movement  (e.g.,  Livingston,  1956; 
Schwenk,  2000a,b).  In  the  traditional  \dew, 
mechanism  two  is  attributed  to  the  action 
of  the  extrinsic  inuscles  and  inechanism 


230         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


three  to  the  intrinsic  muscles.  To  exempli- 
fy the  differences  among  mechanisms, 
consider  tongue  protrusion.  The  tongue 
can  be  protruded  if  it  is  "pushed"  beyond 
the  ]aw  margins  by  protraction  of  the 
hyobranchial  apparatus.  Alternatively,  the 
tongue  can  be  "pulled"  out  of  the  mouth 
by  muscles  linking  it  to  the  mandible.  In 
this  case,  movement  of  the  tongue  relative 
to  a  fixed  hyobranchium  must  be  possible, 
as  occurs,  for  example,  in  many  lizards 
when  the  tongue  slides  along  the  lingual 
process  of  the  basihyal  (Schwenk,  2000b). 
Finally,  the  tongue  can  protrude  beyond 
the  jaw  margins  if  it  elongates  anteriorly 
by  changing  its  shape,  despite  being  fixed 
to  a  stationary  hyobranchium  posteriorly. 
Obviously,  these  mechanisms  might  be 
combined  to  effect  tongue  protrusion. 

The  first  two  types  of  tongue  movement 
conform  to  traditional  models  of  muscu- 
loskeletal movement,  but  the  third  implies 
a  far  more  complex  mechanism.  The  na- 
ture of  this  mechanism  and  its  relationship 
to  the  tongues  internal  architecture  were 
appreciated  by  Owen  (1868:  394),  who  de- 
scribed it  in  reference  to  the  giraffe  and 
its  ability  to  strip  an  acacia  tree  of  leaves 
with  its  highly  protiTisible  tongue: 

The  muscular  fibres  in  the  free  and  flexible  part  of 
the  tongue  present  an  arrangement  adequate  to  all 
its  movements.  The  stylo-glossi  and  inferior  lingua- 
les  expand  into  a  layer  of  longitudinal  fibres  .  .  . 
these  longitudinal  muscles  inclose  a  mass  of  fibres, 
which  run  in  die  transverse  direction.  The  action 
of  the  transverse,  combined  with  that  of  several 
short  vertical,  fibres  near  the  margins,  and  of  those 
forming  the  thin  circular  stratum  smrounding  the 
stylo-glossi  at  the  middle  part  of  the  tongue,  serves 
to  attenuate  or  diminish  the  transverse  diameter  of 
the  tongue  and  increase  its  length;  while  thus  rig- 
idly extended  the  apex  of  the  tongue  can  be  cui-ved 
upward  or  downward  by  tlie  superficial  longitudinal 
fibres  .... 

The  intrinsic  mechanism  of  tongue 
elongation  outlined  by  Owen  (1868)  and 
others  (e.g.,  M.  Griffiths,  1968,  1978;  Win- 
kelmann,  1971,  in  T  Griffiths,  1978)  was 
formalized  by  Kier  and  Smith  (1985)  in 
their  "muscular  hydrostat"  model  of 
tongue  movement  (also  Smith  and  Kier, 


1989).  They  modeled  the  tongue  (and  sim- 
ilar organs)  as  a  constant-volume  cylinder 
filled  with  incompressible  fluid  (intracel- 
lular water).  They  recognized  that  a  re- 
duction in  one  dimension  must  cause  a 
compensatory  increase  in  another  and 
showed  that  muscular  hydrostats  are  char- 
acterized by  orthogonal  arrays  of  muscle 
fibers  arranged  to  modulate  the  tongues 
diameter  and  length.  In  addition,  superfi- 
cial longitudinal  fibers  cause  bending  and 
helical  or  oblique  fibers  cause  torsion.  Dif- 
ferential, localized  activity  of  these  fiber 
systems  can  potentially  create  a  vast  range 
of  complex  shape  changes  in  tongue  form. 

In  light  of  the  muscular  hydrostat  model 
of  tongue  function,  it  is  clear  that  the  se- 
rial, orthogonal  arrangement  of  muscle  fi- 
bers in  the  medullary  region  of  the  mam- 
malian tongue  serves  to  lengthen  the 
tongue  by  decreasing  its  diameter,  regard- 
less of  whether  individual  fibers  originate 
intrinsically  or  extrinsically  Likewise,  lon- 
gitudinal fibers  of  the  cortex  participate  in 
tongue  shortening,  retraction,  bending, 
and  torsion,  regardless  of  nominal  origin. 
In  other  words,  within  the  tongue,  muscle 
fibers  behave  as  organized  systems  that  do 
not  correspond  to  the  extrinsic— intrinsic 
dichotomy:  within  the  vertical  fiber  sys- 
tem, both  intrinsic  and  extrinsic  fibers 
function  together  to  reduce  the  vertical  di- 
mension of  the  tongue.  Furthermore,  the 
serial  vertical  system  must  often  act  in 
concert  with  the  serial  transverse  system 
to  reduce  tongue  diameter  uniformly 
along  its  length.  By  implication,  a  relatively 
"simple"  action,  such  as  tongue  elongation, 
involves  minimally  four  nominal  "mus- 
cles," including  both  "extrinsic"  and  "in- 
trinsic" types. 

Similarly,  the  lepidosaurian  tongue  is  ca- 
pable of  hydrostatic  shape  change.  Al- 
though the  m.  hyoglossus  is  assumed  to  be 
a  tongue  retractor,  its  internal  complexity, 
as  described  here,  suggests  that  it  may  be 
active  during  "intrinsic"  shape  changes  as 
well.  Schwenk  (2000b)  suggested  that  the 
foretongue  in  lizards  is  somewhat  inde- 
pendent of  the  hind  tongue,  with  the  for- 


Tongue  Muscles  •  Schwenk        231 


mer  more  specialized  for  hydrostatic  elon- 
gation independent  of  the  hyobranchium 
and  the  latter  more  tightly  coupled  to  the 
hyobranchium.  If  so,  it  is  possible  (but 
speculative)  that  the  traditional  notion  of 
whole-tongue  retraction  attributed  to  the 
hyoglossus  resides  in  its  extrinsic  compo- 
nent and  the  anterior,  intrinsic  component 
functions  predominantly  to  retract  the 
foretongue  after  it  is  hydrostatically  elon- 
gated (as  during  tongue-flicking  behavior 
or  lapping).  This  interpretation  implies  a 
functional  heterogeneity  within  the  hyo- 
glossus muscle,  which  is  consistent  with  its 
histochemical  partitioning  in  some  spe- 
cies— a  hypothesis  that  could  be  tested 
electromyographically. 

The  Tongue  as  a  Functional  Unit 

Based  on  the  traditions  of  musculoskel- 
etal anatomy,  our  expectation  for  muscles 
is  that  they  are  discrete  entities  with  an 
origin,  an  insertion,  and  an  action.  Al- 
though we  accept  that  individual  fibers 
might  not  run  the  full  course  of  a  muscle 
(e.g.,  Loeb  et  al.,  1987),  the  muscle,  as  a 
whole,  is  clearly  delimited  by  its  origin  and 
insertion,  coherence,  and  separation  from 
adjacent  muscles.  Furthermore,  the  clear 
relationship  between  these  anatomical  at- 
tributes and  a  muscle's  action(s)  reinforces 
our  sense  that  muscles  are  discrete  inor- 
phologic  units  whose  homologous  counter- 
parts can  be  identified  in  other  species.  As 
such,  muscles  satisfy  the  requirements  of 
a  "character"  in  the  traditional  neo- 
Darwinian  sense:  they  are  "quasi-indepen- 
dent" (Lewontin,  1984)  and  "quasi-auton- 
omous" (Wagner,  1999)  parts  of  the  phe- 
notype.  In  other  words,  they  are  capable 
of  evolutionary  change  somewhat  indepen- 
dent of  change  in  other  characters  and  are 
developmentally  autonomous  units  indi- 
viduated from  other  such  units. 

There  is  no  denying  that  several  lingual 
"muscles"  have  "typical"  origins  outside 
the  tongue,  but  once  within  the  tongue 
they  deviate  from  the  traditional  concep- 
tion of  a  muscle  and  seem  to  be  subject  to 
a  different  set  of  rules.  These  rules  are  dic- 


tated by  the  muscular  hydrostat  model  of 
tongue  movement.  Fibers  are  arrayed 
within  the  tongue  to  generate  global  or  lo- 
cal reductions  in  diameter,  reductions  in 
length,  lateral  bending,  dorsoventral  bend- 
ing, torsion,  and  a  nearly  infinite  variety  of 
shape  changes — all  by  virtue  of  the  incom- 
pressibility  of  intracellular  fluid  and  the 
principle  of  compensatoiy  deformation  in 
a  constant  volume  stmcture — regardless  of 
the  extrinsic  or  intrinsic  origin  of  the  fi- 
bers. 

In  light  of  muscular  hydrostatic  func- 
tion, the  atomization  of  the  tongue  into  in- 
dividuated muscles  is  insupportable.  In- 
stead, the  tongue  is  better  viewed  holisti- 
cally  as  a  single  functional  unit  (Schwenk, 
2001).  This  does  not  imply  that  the  tongue 
is  a  single  evolutionary  character,  but  rath- 
er emphasizes  that  the  components  of  the 
tongue  are  more  tightly  integrated  func- 
tionally with  each  other  than  they  are  with 
other  parts  of  the  oral  apparatus.  As  such, 
proper  tongue  function  depends  on  the 
closely  coordinated  action  of  its  many  parts 
acting  in  concert  to  achieve  a  given  func- 
tional output.  An  action  such  as  tongue 
elongation  emerges  as  the  instantaneous 
manifestation  of  countless  vertical  and 
transverse  muscle  fiber  contractions,  re- 
gardless of  their  point  of  origin  or  nominal 
affiliation.  Indeed,  the  highly  organized  in- 
ternal architecture  of  the  tongue  is  literally 
the  incarnation  of  this  extreme  functional 
coherence,  a  coherence  that  belies  its  dis- 
parate anatomical  components.  In  a  mam- 
mal, for  example,  it  is  important  that 
sheets  of  vertical  fibers  are  arranged  along 
the  length  of  the  tongue;  it  is  not  impor- 
tant whether  the  fibers  within  each  sheet 
derive  extrinsically  from  the  genioglossus, 
or  intrinsically  from  the  lamina  propria  or 
the  longitudinalis  inferior.  Similarly,  Bam- 
well  et  al.  (1978a)  noted  that,  despite  ex- 
trinsic and  intrinsic  contributions,  the  dor- 
sal longitudinal  muscle  layer  functions  as 
"a  whole."  Thus,  rather  than  "muscles," 
within  the  tongue  it  is  more  accurate  (and 
I  believe  preferable)  to  refer  to  fiber  sys- 
tems. Vertical  and  transverse  fiber  systems 


232         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


contribute  to  reduction  in  tongue  diame- 
ter, regardless  of  which  "muscles"  provide 
them  with  fibers. 

A  holistic  view  of  tongue  form  and  func- 
tion is  furtlier  supported  by  tongue  devel- 
opment in  mammals.  From  the  earliest 
stages,  orientations  of  all  muscle  fibers 
within  the  tongue  are  evident  (Smith, 
1994).  In  Monodelphis,  Smith  (1994:  158) 
observed,  "adjacent  cells  simultaneously 
orient  into  one  of  the  three  mutually  per- 
pendicular planes,  so  that  the  three-di- 
mensional arrangement  of  muscle  fibers  in 
the  tongue  is  present  at  the  earliest  stages 
observed."  As  such,  sheets  of  vertical  and 
transverse  fibers  begin  to  organize  within 
the  tongue  in  situ  without  regard  to  the 
subsequent  connection  or  insertion  points 
of  their  constituent  fibers.  For  example,  a 
given  vertical  fiber,  ultimately  connects  to 
the  lamina  propria  within  the  tongue, 
whereas  an  adjacent  cell  connects  extrin- 
sically  within  the  genioglossus.  Another 
nearby  cell  orients  transversely  and  con- 
tributes to  the  adjacent  sheet  of  transverse 
fibers  (K.  K.  Smith,  personal  communica- 
tion). 

I  have  here  focused  on  the  anatomy  of 
the  tongue  and  completely  neglected  the 
issue  of  motor  control.  Such  a  discussion 
is  beyond  the  scope  of  this  paper.  How- 
ever, it  is  worth  noting  that,  although  a 
muscle  such  as  the  genioglossus  is  mor- 
phologically continuous  from  its  origin  on 
the  mandible  to  its  insertion  into  the  lam- 
ina propria  of  the  tongues  dorsal  surface, 
individual  fibers  may  not  run  its  full 
length.  As  such,  some  fibers  might  have  an 
intrafascicular  origin  within  the  muscle 
mass  (Loeb  et  al.,  1987).  Thus,  the  fiber 
population  actually  penetrating  the  tongue 
possibly  has  an  intrafascicular  origin  within 
the  genioglossus.  Such  an  arrangement 
would  allow  segregation  of  the  muscle  into 
extrinsic  and  intrinsic  motor  units,  thereby 
simplifying  control.  Strain  mapping  data 
from  the  human  tongue  in  vivo  are  consis- 
tent with  this  hypothesis  (Napadow  et  al., 
1999),  although  simplifying  assumptions  of 
the  analysis  somewhat  weaken  its  support. 


The  ability  of  the  tongue  to  form  localized 
deformations  and  to  protnide,  for  exam- 
ple, in  cylindrical,  spatulate  and  cupped 
conformations  (personal  observation) 
strongly  implies  separate  motor  control  of 
both  vertical  and  transverse  fiber  systems, 
as  well  as  regional  control  of  these  systems 
along  the  length  of  the  tongue.  As  such, 
functional  integrity  of  lingual  fiber  systems 
need  not  imply  coarseness  of  control.  Fi- 
nally, finite  element  analyses  that  model 
the  tongue  as  a  series  of  regional  elements 
with  certain  contractile  and  viscoelastic 
properties,  regardless  of  fiber  source,  are 
effective  in  predicting  patterns  of  tongue 
shape  change  (Wilhelms-Tricarico,  1995; 
Sanguineti  et  al.,  1997),  further  supporting 
a  holistic  conception  of  tongue  function- 
ality. 

CONCLUSIONS 

The  results  of  this  study  refute  the  di- 
chotomous  view  of  the  lingual  muscula- 
ture, both  anatomically  and  functionally. 
The  distinction  of  "intrinsic"  from  "extrin- 
sic" muscles  may  serve  as  a  convenience 
for  description  or  instruction,  as  suggested 
by  Abd-El-Malek  (1938),  but  our  current 
understanding  of  tongue  function  suggests 
that  the  convention  is  no  longer  tenable. 
It  acts  only  to  reinforce  an  outmoded,  at- 
omistic view  of  the  tongue  that  deflects  us 
from  a  more  complete  conception  of  this 
remarkable  organ.  The  muscular  hydrostat 
model  dictates  that  the  tongue  acts  as  a 
functional  unit  and  as  such,  internal 
tongue  form  manifests  functional  unity 
rather  than  the  separate  contributions  of 
individuated  muscles.  Thus,  within  the 
tongue  there  is  a  blurring  of  distinctions 
among  muscles,  even  those  arising  from 
outside  the  tongue,  so  that  muscle  individ- 
uality is  lost.  In  this  context,  the  notion  of 
a  lingual  "muscle"  is  not  meaningful  and 
reference  to  "fiber  systems"  more  accu- 
rately, if  still  inadequately,  represents  the 
tongue's  inner  workings.  Therefore,  a  ho- 
listic view  of  tongue  form  and  function 
highlights  coherence  over  separability  and 


Tongue  Muscles  •  Schwenk       233 


the  precedence  of  functional  integrity  over 
anatomical  atomization. 

ACKNOWLEDGMENTS 

I  am  deeply  indebted  to  Fuzz  Cromp- 
ton,  to  whom  this  contribution  is  dedicat- 
ed, for  his  friendship,  mentorship,  and 
support.  My  two  years  as  a  postdoctoral 
fellow  in  his  lab  were  among  the  most  en- 
joyable and  instructive  of  my  career.  I 
thank  Parish  A.  Jenkins,  Jr.,  for  organizing 
the  symposium  in  honor  of  Fuzz  and  for 
inviting  me  to  participate.  I  am  grateful  for 
the  support  and  guidance  of  Karen  Hiie- 
mae,  who  first  introduced  me  to  mammal 
tongues.  Kathleen  Smith  shared  her  exten- 
sive knowledge  of  tongue  stioicture,  func- 
tion, and  development.  Elizabeth  Jock- 
usch,  Kathleen  Smith,  and  an  anonymous 
reviewer  critically  read  the  manuscript. 
Various  phases  of  this  work  were  support- 
ed by  Marvalee  Wake,  University  of  Cali- 
fornia, Berkeley;  the  Graduate  College 
and  Department  of  Oral  Anatomy,  Uni- 
versity of  Illinois  at  Chicago;  A.  W.  Cromp- 
ton,  the  Department  of  Organismic  and 
Evolutionary  Biology,  and  the  Milton 
Fund,  Harvard  University;  the  University 
of  Connecticut  Research  Foundation;  and 
grants  NIH  F32  DE05467  and  NSF  IBN- 
9601173  to  the  author. 

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ELECTROMYOGRAPHIC  PATTERN  OF  THE  GULAR  PUMP  IN 
MONITOR  LIZARDS 

TOMASZ  OWERKOWICZ/  ELIZABETH  L.  BRAINERD,^  AND  DAVID  R.  CARRIERS 

ABSTRACT.    Gular  pumping  in  monitor  lizards  is  wicz,  1996).  In  a  gular  pump  cycle,  a  mon- 

knovvn  to  play  an  important  role  in  lung  ventilation,  ^^^^  i-^^j.^  flj-st  draws  fresh  air  into  its  large 

but  its  evolutionary  origin  has  not  yet  been  addressed.  ,  i     /       i      \  m,  j    4-1  ^ 

To  determine  whether  Ae  g^ilar  pump  derives  from  phaiyngea     (gukr)    cavity    and    then    COn- 

die  buccal  pump  of  basal  tetrapods  or  is  a  novel  in-  tracts  its  throat  muscles  to  create  positive 

vention,  we  investigated  the  electromyographic  activ-  pressure,    thus   forcing   air  into   the   lungS. 

it\-  associated  with  gular  pumping  in  savannah  mon-  Multiple   gular  pumps   may  OCCUr  ill   SUC- 

itor    lizards    (Varanus    exanthenmticus).    Electrodes  ^^^^;^^^    between    COStal    breaths.    Gular 

were  implanted  in  hyobranchial  muscles,  and  their  .11                1               ^        ■        n         l.^ 

activity'  patterns  were  recorded  synchronously  with  pumping  has   been    shown   to   Slgmhcantly 

hyoid  kinematics,  respiratory  airflow,  and  gular  pres-  increase  both   minute  ventilation  and  aei- 

sure.  Movement  of  the  highly  mobile  hyoid  apparatus  obic  capacity  of  savannah   monitor  lizards 

effects  large-volume  airflows  in  and  out  of  the  gular  (Varauiis  exanthematicus)  during  exercise 

cavity.  The  stemohyoideus  and  branchiohyoideus  de-  ,„          1         .                 ,      IQQQ') 

press,  retract,  and  abduct  die  hyoid,  thus  expanding  ('^werKOWlCZ  et  ai.     i^yy; 

the  gular  cavit>'.  The  omohyoideus,  constrictor  colli.  Little  IS  known  about  the  actual  mecli- 

intermandibularis,    and   mandibulohyoideus   elevate,  anism  of  gular  pumping  and  its  evolution. 

protract,  and  adduct  the  hyoid,  thus  compressing  the  \    highly    expandable    pharynx,    supported 

gular  cavity.  Closure  of  the  choanae  by  the  sublingual  ,        ^^   elaborate   hyobranchial  basket,   is   a 

plicae  precedes  gular  compression,  allowang  positive  /                  .     .       r                     r              •.         1-         j 

pressure  to  be  generated  in  the  gular  cavity  to  force  characteristic    feature    of   monitor    lizards. 

air  into  the  lungs.  The  large  size  and  compressibility  of  the 

The  gular  pump  of  monitor  lizards  is  found  to  ex-  pharynx  make  it  ideally  suited  for  puinping 

hibit   a   neuromotor   pattern    similar   to   the   buccal  j^          volumes  of  air.  Smith  (1986)  studied 

pump  of  extant  amphibians,  and  both  mechanisms  m        r         .  ■             r  .  1          .                   1    4-    ^^    ;  ^    17 

f     ,^    ,        1          ^        1      Ti  ■       „„    f   fi.  .f  ^u^  the  function  oi  throat  musculature  in  V. 

involve  homologous  muscles.  This  suggests  that  the  j                 r      j                   j 

gular  pump  may  have  been  retained  from  the  ances-  exanthenuiticilS    during    feeding,    and    re- 

tral  buccal  pump.  This  hypothesis  remains  to  be  test-  corded  hyobranchial   muscle  activity  and 

ed  by  a  broad  comparative  analysis  of  gular  pumping  hyoid    movements.    Bels    et   al.    (1995:    99) 

among  the  amniotes.  provided  a  kinematic  analysis  of  the  throat 

threat  display  in  Varanus  griseus,  "a  ven- 

INTRODUCTION  tilatory  bucco-pharyngeal  breathing  pump 

Monitor  Hzards   (genus   Varanus)   have  (VBPBP),"  consisting  of  alternating  expan- 

recently  been  found  to  supplement  their  sions  and  compressions  of  the  gular  cavity, 

lung  ventilation  with  gular  pumping  dur-  These   studies   have  documented  the  ex- 

ing    locomotion    (Brainerd    and    Owerko-  treme  excursions  of  the  hyoid  apparatus 

during  a  wide  repertoire  of  monitor  be- 

,.  „            .■      ^    1        u         1  IT  haviors.   However,  the  electromyographic 

'Museum  ot  Comparative  Zoology,  Harvard  Uni-  ,-^^  ,^s     ■                        r    ^             1           y    o     r 

versity,  26  Oxford  Street,  Cambridge,  Massachusetts  (EMG)   Signature  of  the  gular  pump,  as  a 

02138.  ventilatory  mechanism,  has  not  been  re- 

'  Department  of  Biology  and  Organismic  and  Evo-  ported, 

lutionaiy  Biology  Program,  University  of  Massachu-  ^j^.^"  ^^^  1     ^-^^  ^^  determine  how  throat 

setts,  Amherst,  Massachusetts  01003.  ,           ,.-^...                i-       .      i    1      •              1 

^  Department  of  Biology,  University  of  Utali,  Salt  muscle  activity  IS  coordinated  during  gular 

Lake  City,  Utali  84112.  pumping    ill    V.    exantheniaticus.    Which 

Bull.  Mus.  Comp.  Zool.,  156(1):  237-248,  October,  2001         237 


238         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


muscles  are  responsible  for  gular  expan- 
sion, and  which  ones  are  responsible  for 
compression?  How  is  pressure  generated 
in  the  gular  cavity?  What  controls  the  air- 
flow pattern? 

The  evolutionary  origin  of  the  gular 
pump  also  presents  an  interesting  dilem- 
ma. Squamates  have  been  presumed  to 
ventilate  their  lungs  solely  by  means  of 
costal  aspiration  (Gans,  1970;  Carrier, 
1987;  but  see  Deban  et  al.,  1994);  they  rely 
on  contraction  of  intercostal  muscles  to 
create  negative  pressure  in  the  pleural  cav- 
ity to  suck  air  into  the  lungs.  The  use  of  a 
pressure  pump  was  thought  to  be  reserved 
for  air-breathing  fish  and  amphibians 
(Liem,  1985;  Brainerd  et  al,  1993).  In  this 
mechanism,  air  is  gulped  into  the  buccal 
(mouth)  cavity,  and  subsequently  the  hyoid 
apparatus  generates  positive  pressure, 
forcing  air  into  the  lungs.  The  gular  pump 
of  inonitor  lizards  clearly  qualifies  as  a 
pressure  pump  and  therefore  breaks  with 
this  traditional  phylogenetic  separation  of 
breathing  mechanisms.  However,  the  gular 
pump  differs  from  the  buccal  pump  be- 
cause the  hyoid  apparatus  of  monitor  liz- 
ards is  positioned  posteriorly  in  the  throat, 
whereas  the  hyoid  apparatus  of  amphibi- 
ans resides  in  the  mouth  cavity  between 
mandibular  rami.  The  presence  of  gular 
pumping  behavior  has  not  been  rigorously 
investigated  in  other  lizard  genera,  and  it 
is  unclear  whether  gular  pumping  is  a 
uniquely  derived  trait  of  monitor  lizards  or 
whether  its  ancestry  can  be  traced  back  to 
buccal  pumping  of  basal  tetrapods. 

Therefore,  this  study  attempts  to  ad- 
dress the  origin  of  gular  pumping  from  a 
functional  perspective.  How  similar  is  the 
EMG  pattern  of  the  gular  pump  to  that  of 
the  amphibian  buccal  pump?  Is  the  gular 
pump  a  case  of  neuromotor  conservatism 
in  evolution,  or  has  it  evolved  de  novo  in 
monitor  lizards? 

MATERIALS  AND  METHODS 

Animals 

Experiments  were  performed  on  four 
savannah    monitor   lizards    (230-2,400    g) 


during  and  immediately  after  locomotion 
on  a  motorized  treadmill  at  speeds  of  1—5 
km/h.  The  animals  were  maintained  at  25— 
40°C  on  a  14:10  hour  light: dark  photo- 
period  and  were  fed  a  diet  of  mice. 

Terminology 

This  study  follows  the  terminology  of 
Smith  (1986)  in  her  description  of  the  os- 
teology and  myology  of  the  varanid  gular 
region. 

Videoradiography 

Videos  of  the  lizards  were  taken  with  a 
Sony  DCR  VXIOOO  digital  camcorder  (60 
fields/s  at  1/250  s  shutter  speed)  and  the 
Siemens  X-ray  fluoroscope  at  the  Museum 
of  Comparative  Zoology  Laboratories  at 
Harvard  University.  Video  recordings  were 
made  separately  in  lateral  and  dorsoventral 
projections.  Select  video  fields  were  im- 
ported into  Adobe  Photoshop  on  a  Power 
Macintosh  computer. 

To  better  visualize  inovements  of  the 
floor  of  the  mouth  relative  to  the  skull  and 
hyoid,  lead  markers  (1.6  X  0.5  mm)  were 
placed  unilaterally  in  the  left  sublingual 
plica  and  in  the  anterior  epithelial  border 
of  the  left  choana.  Marker  implantation 
was  performed  percutaneously  with  a  20- 
gauge  needle  and  plunger  while  the  ani- 
mals were  under  1—2%  halothane  anesthe- 
sia. 

Pneumotachography 

Two  animals  were  used  to  measure  air- 
flow during  gular  pumping.  A  lightweight 
mask,  fashioned  from  clear  acetate  and  ep- 
oxy,  was  custom-fitted  and  taped  over  the 
lizard's  snout  to  enclose  the  mouth  and 
nostrils.  A  bias  flow  of  humidified  air 
(1,200  ml/min)  was  drawn  through  the 
mask.  A  pneumotachograph  (8421  series 
0-5  LPM,  H.  Rudolph,  Kansas  City,  Mis- 
souri), connected  to  a  differential  pressure 
transducer  (MP  45-1-871,  Validyne,  Noitli- 
ridge,  California)  downstreain  from  the 
animal,  measured  airflow  through  the 
mask.  The  system  was  calibrated  against 


EMG  Pattern  of  Gular  Pump  •  Owerkowicz  et  al.        239 


repeated  injections  of  measured  aliquots  Pennsylvania).  The  signals  were  amplified 

of  air  into  the  mask.  5,000-20,000    times    (as    appropriate    for 

each  channel)  with  Grass  P511J  amplifiers 

Pressure  Recordings  (Quincy,  Massachusetts),  with  a  bandpass 

Two  animals   (not  used  for  airflow  re-  of  100-1,000  Hz  (with  the  60-Hz  notch 
cordings)  were  instrumented  to  measure  filter   in).    The   signals   were   acquired   at 
gular  pressure  during  gular  pumping.  With  5,000  Hz  and  analyzed  on  a  Power  Mac- 
the  animal  under  1-2%  halothane  gas  an-  intosh   computer  using  AcqKnowledge 
esthesia,  a  skin  incision  was  made  between  (BioPac  Systems,  Santa  Barbara,  Califor- 
the   ceratohyal   and   ceratobranchial.   The  nia)    and    Igor    Pro    (WaveMetrics,    Inc., 
underlying  muscles  were  carefully  blunt-  Lake  Oswego,  Oregon)  software.  Electro- 
dissected  and  a  13-gauge  needle  was  in-  myographic  and  pressure  signals  were 
serted  through  the  pharyngeal  epithelium  temporally    synchronized   with   video    re- 
into  the  gular  cavity.  A  20-  to  30-cm-long  cordings  by  means  of  a  light-emitting  di- 
polyethylene  cannula  (1.14-mm  inner  di-  ode  trigger  (Thexton  Unlimited,  London, 
ameter,   1.57-mm  outer  diameter),  previ-  United  Kingdom), 
ously  sterilized  and  heat-flared  at  the  distal 
end,  was  threaded  through  the  hole  and  RESULTS 
securely  sutured  to  the  lateral  wall  of  the  Kinematics 
gular  cavity.  Before  each  recording  session, 

the  cannula  was  cleared  of  mucus  to  pre-  Four  stages  of  hyobranchial  movement 

vent  capillarity  artefacts  and  connected  to  characterize    each    gular    pumping    cycle 

a  differential  pressure  transducer  (PX138-  (Fig.    1):    resting,    active   expansion,   early 

0.3D5V,  Omega  Engineering,  Inc.,  Stam-  closure,  and  compression.  The  cycle  usu- 

ford,  Connecticut).  The  pressure  transduc-  ally  begins  with  the  expansion  of  the  hyob- 

er  was  calibrated  against  10  cm  H2O  after  ranchial  basket.  From  its  resting  position 

each  recording  session.  (Fig.    lA),  the  basihyoid  and  the  lingual 

process    are    drawn    slightly   ventrad   and 

Electromyography  caudad.   The   anterior  processes   are   ab- 

Electromyographic  activity  was  record-  ducted    and,    pivoting   on    the    basihyoid, 

ed   in   the   following   muscles:   constrictor  swung  laterad.  The  ceratohyals  and  cera- 

colli,   intermandibularis,   mandibulohyoid-  tobranchials  rotate  to  assume  a  more  ver- 

eus,  omohyoideus,  sternohyoideus,  and  tical  orientation  (Fig.  IB), 

branchiohyoideus.  Patch  and  sew-through  The  compressive  phase  of  the  pump  cy- 

bipolar  electrodes,  as  detailed  by  Loeb  and  cle  begins  with  the  elevation  of  the  buccal 

Cans  (1986)  and  Carrier  (1996),  respec-  floor  to  abut  the  palate,  thereby  closing  off 

tively,    were    constructed   of  0.28-mm-di-  the  mouth  and  nostrils.  As  highlighted  by 

ameter  Teflon-coated  stainless  steel  wire  radiopaque   markers,   each   choana  is   oc- 

(Cooner  Wire  Co.,  Chatsworth,  California)  eluded  by  its  ipsflateral  sublingual  pfica. 

and  silastic-reinforced  sheeting  (Specialty  The  glottis  is  located  in  the  gular  cavity. 

Manufacturing,  Inc.,  Saginaw,  Michigan),  while  the  hyoid  remains  in  a  retracted  and 

In  each  electrode,  the  exposed  portions  of  expanded  configuration  (Fig.  IC).  Finally, 

wires  were  2  mm  long  and  1  mm  apart,  the  basihyoid  is  protracted  and  elevated. 

With  the  animal  anesthetized,  electrodes  while  the  trachea  slides  rostrad  in  the  gu- 

were  surgically  implanted  and  firmly  an-  lar  cavity.  The  anterior  processes  are  ad- 

chored  in  the  desired  muscles.  The  elec-  ducted,   and  the  ceratohyals   and  cerato- 

trode  wires  were  then  passed  subcutane-  branchials  fold  horizontally  (Fig.  ID).  The 

ously  under  the  pectoral  girdle  to  a  single  hyobranchium  then  relaxes  and  passively 

exit  on  the  tiTink's  dorsum  and  soldered  to  returns  to  its  resting  state  (Fig.   lA);  an- 

connectors    (Microtech,    Inc.,    Boothwyn,  other  pumping  cycle  may  follow. 


240         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  1.  Still  frames  from  an  X-ray  positive  video  (shutter  speed  1/250  s)  showing  one  gular  pump  cycle  in  Varanus  exanthe- 
maticus  (body  mass  =  600  g).  The  left  column  shows  the  animal  in  lateral  projection,  the  right  column  in  dorsoventral  projection. 
Although  not  recorded  simultaneously,  frames  in  each  row  portray  corresponding  stages  of  a  pump  cycle.  (A)  Gular  cavity  relaxed. 
(B)  Gular  cavity  expanded.  (C)  Buccal  floor  elevated.  (D)  Gular  cavity  compressed.  Radiopaque  markers  (arrows)  are  placed  at 
the  choana  (Ch),  the  sublingual  plica  (SP),  and  the  glottis  (G).  Note  the  closure  of  the  mouth  and  nares,  which  seals  the  gular 
cavity,  as  demonstrated  by  proximity  of  markers  Ch  and  SP  in  (C). 


EMG  Pattern  of  Gular  Pump  •  Owerkowicz  et  al.        241 


IM  post 


CCpost 


BHap 


Time  (s) 


IMpost 


Time  (s) 


Figure  2.  Raw  electromyograms  of  hyobranchial  muscles  during  gular  pumping  in  Varanus  exanthematicus.  (A)  Three  gular  pump 
cycles  recorded  simultaneously  with  airflow  at  the  snout.  Gular  expansion  (negative  airflow)  is  initially  passive  because  of  the  gravitational 
drop  of  the  hyoid,  and  then  active  as  the  branchiohyoideus  and  stemohyoideus  begin  to  contract.  Gular  compression  occurs  during  the 
zero-flow  plateau,  as  air  is  pressed  into  the  lungs.  Minimal  air  leakage  occurs — note  the  spikes  showing  early  closure  of  the  nares  (N) 
and  the  late  closure  of  the  glottis  (G).  The  asterisk  indicates  unanticipated  activity  of  the  omohyoideus  due  to  neck  bending.  (B)  A  costal 
breath  followed  by  four  successive  gular  pump  cycles,  recorded  simultaneously  with  gular  pressure.  Gular  expansion  generates  little 
negative  pressure,  but  peak  compressive  pressures  up  to  15  cm  HJD  have  been  recorded.  Abbreviations:  CC,  m.  constrictor  colli;  IM, 
m.  intermandibularis;  MH,  m.  mandibulohyoideus;  BH,  m.  branchiohyoideus  (ceratohyoid  head);  BH  ap,  m.  branchiohyoideus  (comuhyoid 
head);  SH,  m.  stemohyoideus;  OH,  m.  omohyoideus;  ant,  anterior;  post,  posterior. 


Active  expansion  was  not  observed  in 
every  pump  cycle.  The  aniinals  often 
chose  to  proceed  to  closure  and  compres- 
sion directly  from  the  resting  stage,  in 
which  case  the  volume  of  air  pumped  was 
not  as  great  as  when  preceded  by  active 
expansion.  Furthermore,  resting  gular  vol- 
ume was  dependent  on  the  positioning  of 
the  hyobranchial  apparatus  in  the  neck  of 
the  animal,  which  varied  with  the  animal's 
posture  and  muscle  tone  of  associated  pec- 
toral musculature  (stemohyoideus  and 
oinohyoideus — see  below). 

Airflow 

The  airflow  pattern  at  the  aniinal's 
mouth  and  nostrils  (Fig.  2A)  is  consistent 
with  a  biphasic  nature  of  each  gular  pump, 
whereby  a  filling  (expansive)  phase  is  im- 


mediately followed  by  an  emptying  (com- 
pressive) phase.  Average  filling  volumes 
ranged  froin  6  to  15  inl,  but  individual  gu- 
lar inspirations  up  to  33  ml  were  also  re- 
corded. Early  in  the  pump  cycle,  animals 
were  observed  to  rely  on  passive  filling  of 
the  gular  cavity  by  gravitational  drop  of  the 
hyoid  (correspondent  to  the  return  of  the 
hyoid  from  compressed  to  resting  stage). 
Passive  filling  was  followed  by  active  ex- 
pansion, as  indicated  by  concomitant  activ- 
ity in  the  branchiohyoideus  and  stemohy- 
oideus, which  resulted  in  faster  (more  neg- 
ative) airflow  and  greater  filling  volumes. 

Early  in  the  filling  phase,  airflow  into 
the  gular  cavity  was  rapid,  as  shown  by  the 
steep  descent  of  the  airflow  trace  to  its 
minimum  value.  Late  in  the  filling  phase, 
inspiratory  airflow  gradually  diininished  to 


242         Bulletin  Museum  of  Comparative  Zoologij,  Vol.  156,  No.  1 


nil.  A  slight  overshoot  of  the  zero-flow  line  milliseconds  by  almost  simultaneous  acti- 
(N  in  Fig.  2A)  marked  early  closure  of  the  vation  of  the  stemohyoideus  and  mandi- 
mouth  and  nostrils,  and  the  beginning  of  bulohyoideus  III.  The  intensity  of  their  fir- 
the  emptying  phase.  A  zero-flow  plateau  ing  remained  roughly  constant  while  these 
was  recorded  for  the  duration  of  the  einp-  muscles  were  active.  All  three  muscles  were 
tying  phase,  as  air  was  forced  from  the  gu-  turned  off  before  the  end  of  the  filling 
lar  cavity  into  the  lungs.  The  emptying  phase,  with  activity  in  die  branchiohyoideus 
phase  terminated  in  a  small  expiratory  persisting  for  up  to  150  milliseconds  after 
spike  (0.5—1.0  ml),  after  the  inferred  clo-  the  offset  of  the  stemohyoideus  and  man- 
sure  of  the  glottis  (G  in  Fig.  2A)  and  open-  dibulohyoideus  III. 

ing  of  the  mouth  and  nares.  Unless  anoth-  Gular  compression  began  with  a  burst 

er  pumping  cycle   occurred  immediately  of  activity  in  the  intermandibularis  anteri- 

afterwards,  passive  filling  followed  and  a  or,  which  was  followed  within   100  milli- 

longer  apnoeic  period  ensued.  seconds  by  contraction  of  the  constrictor 

colli,  intermandibularis  posterior,  and  all 

rressure  three   heads   of  mandibulohyoideus.   The 

Each  costal  breath  was  followed  by  as  intensity  of  their  firing  generally  increased 

many  as  five  gular  pumps,  with  successive  from  onset  to  offset.  Activity  ceased  in  all 

pump  cycles  generating  increasingly  posi-  muscles  together,  once  gular  pressure  had 

tive  gular  pressures  (Fig.  2B).  Peak  pres-  peaked. 

sures  up  to  15  cm  H2O  were  recorded.  The  activity  of  the  mandibulohyoideus 
With  the  onset  of  each  compressive  phase.  III  was  biphasic;  it  contracted  during  gular 
gular  pressure  cliiTibed  steeply  and  expansion  and  compression,  but  not  con- 
reached  peak  pressure  within  200  millisec-  tinuously  (Fig.  2B).  It  was  briefly  (50—100 
onds.  For  most  pumping  cycles,  gular  milliseconds)  silent  between  the  two  phas- 
pressure  hovered  within  5%  of  peak  value  es  of  the  pumping  cycle, 
for  less  than  100  milliseconds,  although  The  omohyoideus  was  usually  quiescent 
gular  pressure  would  soinetimes  remain  during  gular  pumping.  When  participating 
elevated  at  peak  for  up  to  400  millisec-  in  gular  pumping,  the  omohyoideus  was 
onds.  Thereafter,  gular  pressure  dropped  predominantly  active  during  gular  com- 
rapidly  (within  100  milliseconds),  often  pression.  However,  it  might  occasionally 
dipping  to  subatmospheric  levels,  and  then  fire  during  gular  expansion  (*  in  Fig.  2A), 
equilibrated  with  the  atmospheric  pres-  which  tended  to  decrease  the  gular  filling 
sure.  volume.  In  such  instances,  activity  of  the 

Gular  pressure  varied  little  from  atmo-  omohyoideus  was  correlated  with  changes 

spheric  pressure  during  the  filling  phase  of  in  posture  and/or  neck  bending  by  the  an- 

a  pump  cycle.  Active  gular  expansion  gen-  imal. 

erated  only  slightly  subatmospheric  pres-  During  locomotion,  regular  phasic  activ- 

sures  (—0.2  to  —0.4  cm  H^O).  ity   was    observed    in    most    hyobranchial 

muscles,  but  was  especially  prominent  in 

Electromyographic  Activity  the  stemohyoideus  and  omohyoideus.  The 

Recordings   from   hyobranchial   muscles  rate  of  discharge  was  the  same  as  the  foot- 
produced  a  consistent  activity  pattern  dur-  fall  frequency,  and  in  the  latter  two  mus- 
ing gular  pumping  (Fig.  2A,  B).  Although  cles  the  signal  amplitude  was  greater  than 
they  remained  quiescent  during  passive  fill-  in  stationary  animals, 
ing,    branchiohyoideus    (both    cerato-    and  niQn  iQQinM 
cornuhyoid  heads),  stemohyoideus,  and 

mandibulohyoideus    III   were   tumed   on  Hyobranchial  Muscle  Function 

during  active  gular  expansion.  Onset  of  the  The  role  of  individual  muscles  involved 

branchiohyoideus  was  followed  in  50—200  in  the  gular  pump  can  be  inferred  by  con- 


EMG  Pattern  of  Gular  Pump  •  Owerkowicz  et  al.        243 


A 


B 


MH  III  -♦ 


MHII   -♦ 


MH  I   ^ 


OH  scap 


OH  scap 


■►  OH  clav 


Figure  3.  The  hyobranchial  apparatus  of  Varanus  exanthematicus,  in  ventral  (top  row)  and  lateral  (bottom  row)  views.  Force 
vectors  (gray  arrows)  show  the  sites  of  insertion  and  lines  of  action  of  the  hyobranchial  muscles,  as  measured  in  dissected 
specimens.  (A)  The  hyoid  in  its  expanded  configuration;  contraction  of  musculi  (mm.)  mandibulohyoideus  and  omohyoideuswill 
result  in  hyoid  compression.  Constrictor  colli  and  intermandibularis  are  not  shown,  because  they  do  not  insert  directly  on  the 
hyoid.  (B)  The  hyoid  in  its  compressed  configuration;  contraction  of  the  branchiohyoideus,  sternohyoideus,  and  mandibulohyoi- 
deus III  will  result  in  hyoid  expansion.  Abbreviations:  ap,  anterior  process;  bh,  basihyoid;  cb,  ceratobranchial;  ch,  ceratohyal; 
clav,  clavicular;  Ip,  lingual  process;  scap,  scapular;  others  as  in  Figure  2. 


sidering  their  insertion  sites  on  the  hyoid 
apparatus  (Fig.  3),  the  patterns  of  their 
EMG  activity,  and  the  kinematics  of  the 
hyoid  elements  during  each  gular  pump 
cycle. 

Gular  expansion  results  from  the  coor- 
dinated activity  of  the  sternohyoideus, 
branchiohyoideus,  and  mandibulohyoideus 
III.  The  sternohyoideus  pulls  the  cerato- 
branchial in  a  caudoventrad  direction,  giv- 
ing it  a  more  vertical  orientation.  This  ac- 
tion tends  to  retract  and  depress  the  ba- 
sihyoid, while  pointing  the  lingual  process 
ventrad.  With  the  ceratobranchial  stabi- 
lized by  the  sternohyoideus,  the  bran- 
chiohyoideus tends  to  abduct  the  anterior 
process  and  retract  the  ceratohyal.  How- 
ever, the  proximal  end  of  the  anterior  pro- 


cess pivots  about  the  basihyoid,  and  the 
ceratohyal  has  its  distal  end  anchored  to 
the  lower  jaw  by  the  mandibulohyoideus 
in.  The  broad,  loose  nature  of  articulation 
between  the  ceratohyal  and  the  anterior 
process  allows  sliding  to  occur  between 
these  two  elements.  Thus,  as  the  anterior 
process  swings  laterad,  it  pushes  against 
the  ceratohyal,  the  angle  between  these 
two  elements  increases,  and  the  ceratohyal 
assumes  a  more  vertical  orientation.  Alto- 
gether, these  muscles  tend  to  expand  the 
gular  cavity  in  the  lateral  and  dorsoventral 
dimensions. 

Gular  compression  begins  with  the  early 
closure  of  mouth  and  nostrils.  The  inter- 
mandibularis anterior,  positioned  under 
the  sublingual  plicae,  contracts  to  elevate 


244         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  4.  Cross  section  of  the  snout  of  Varanus  exanthe- 
maticus  at  tlie  anterior  border  of  the  choanae.  Each  nasal  pas- 
sage connects  to  its  ipsilateral  choana  just  posterior  to  this 
plane.  Elevation  of  the  mouth  floor  allows  the  sublingual  plica 
to  plug  the  choana  above.  The  congruent  outlines  of  the  lower 
and  upper  jaws  allow  an  airtight  closure  of  the  mouth,  sealed 
with  saliva  from  labial  and  sublingual  glands.  Abbreviations: 
Ch,  choana;  LG,  labial  gland;  LJ,  lower  jaw;  N,  nasal  passage; 
SG,  sublingual  gland;  SP,  sublingual  plica;  UJ,  upper  jaw. 


the  buccal  floor  and  push  the  pHcae 
against  the  choanae  (SP  -^  Ch  in  Fig.  4), 
thus  blocking  airflow  through  the  nasal 
passages.  Although  no  recordings  were 
taken  from  the  adductor  mandibulae,  this 
muscle  is  most  likely  to  be  responsible  for 
keeping  the  mouth  closed,  while  the  thick, 
fleshy  gums  (Auffenberg,  1981)  seal  the 
oral  margins  with  secretion  of  salivary 
glands  lining  both  lingual  and  labial  as- 
pects of  the  lower  jaw.  The  gular  cavity  is 
effectively  made  airtight  for  the  duration 
of  gular  compression. 

Muscles  responsible  for  gular  compres- 
sion include  the  omohyoideus,  constrictor 
colli,  intermandibularis  posterior,  and 
mandibulohyoideus.  The  clavicular  and 
scapular  heads  of  the  omohyoideus  attach 
the  ceratobranchials  to  the  respective  parts 
of  the  pectoral  girdle,  and  their  contrac- 
tion retracts  and  elevates  the  basihyoid. 
The  constrictor  colli  encircles  the  floor  and 
sides  of  the  gular  cavity,  forming  a  sleeve 
in  which  the  hyobranchial  basket  is  sus- 
pended. Together  with  its  anterior  exten- 
sion, the  intermandibularis  posterior,  this 
superficial  transverse  muscle  elevates  the 


hyoid  apparatus.  On  the  other  hand,  the 
mandibulohyoideus  connects  the  hyoid  to 
the  lower  jaw  and,  along  with  the  sterno- 
hyoideus  and  omohyoideus,  controls  its 
anteroposterior  position  in  the  neck.  As 
the  basihyoid  is  protracted,  the  ceratohyals 
and  ceratobranchials  assume  a  more  hori- 
zontal orientation,  in  effect  folding  the 
hyobranchial  basket.  The  orthogonal  ori- 
entation of  muscle  fibres  in  the  constrictor 
colli  and  intermandibularis  to  the  mandi- 
bulohyoideus means  that  their  synchro- 
nous activity  will  squeeze  the  air  out  of  the 
gular  cavity. 

With  the  onset  of  locomotion,  most 
hyobranchial  muscles  show  bursts  of  activ- 
ity in  phase  with  the  footfall  pattern.  This 
is  particularly  pronounced  in  the  sterno- 
hyoideus  and  omohyoideus;  their  firing  in- 
tensity during  locomotion  is  several  times 
greater  than  at  rest.  Yet  it  is  hard  to  imag- 
ine their  acting  as  locomotor  muscles.  It  is 
more  likely  that  with  every  retraction  of 
the  forelimb  these  muscles  are  stretched 
and  fire  reflexively  to  stabilize  the  hyoid, 
keeping  it  in  position  for  pumping.  Low- 
intensity  phasic  activity  detected  in  other 
hyobranchial  muscles  is  probably  an  arte- 
fact of  cross-talk  from  the  underlying  axial 
muscles  of  the  neck,  participating  in  the 
lateral  bending  of  the  neck  during  loco- 
motion. 

Airflow  and  Pressure  Changes 

The  pneumotachograph  and  the  pres- 
sure transducer  provide  complementary 
information  about  the  patterns  of  airflow 
and  pressure  generation  outside  and  inside 
the  gular  cavity.  During  gular  expansion, 
pressure  drops  only  slightly  below  the  at- 
mospheric level.  The  lizard's  mouth  and 
nares  are  wide  open  (Fig.  IB)  and  provide 
little  resistance  to  airflow  into  the  gular 
cavity.  Gular  expansion,  whether  passive  or 
active,  is  too  slow  for  gular  pressure  to 
turn  more  negative;  instead,  it  quickly 
equilibrates  with  atmospheric  pressure. 

Inspiratory  airflow  ceases  when  the 
mouth  and  nares  are  shut  (see  above).  The 
"corking"  of  the  choanae  by  the  sublingual 


EMG  Pattern  of  Gular  Pump  •  Owerkowicz  et  al.        245 


plicae  expels  an  aliquot  of  air  from  the  nar-  rived  varanids,  do  not  necessarily  possess 
ial  passages  (N  in  Fig.  2A).  The  gular  pres-  the  same  ensemble  of  hyobranchial  mus- 
sure  increases  from  this  point  on  and  air  cles  found  in  Lissamphibia,  and  even 
is  pressed  through  the  open  glottis  into  the  among  the  latter,  the  muscular  organiza- 
trachea  and  lungs.  The  plateau  at  zero-  tion  of  the  throat  is  highly  variable.  How- 
flow  indicates  the  efficacy  of  the  oral  seal,  ever,  muscle  homologies  can  be  estab- 
Only  at  the  very  end  of  compression  lished  with  a  fair  degree  of  certainty  by 
does  a  puff  of  air  leak  out  of  the  mouth  determining  their  anatomical  relations  and 
and  nares  at  a  high  flow  rate  (G  in  Fig.  motor  nerve  supply  (Fiirb ringer,  1888,  in 
2A).  The  hyobranchial  muscles  have  al-  Cunningham,  1890).  The  constrictor  colli 
ready  turned  off  by  this  time,  yet  their  of  lizards  and  the  interhyoideus  of  am- 
contraction  clearly  persists  for  approxi-  phibians  seem  to  be  homologous,  by  virtue 
mately  120  milliseconds  (a  reasonable  time  of  having  a  common  precursor  in  the  con- 
period  for  slow-twitch  fibers  in  isometric  strictor  hyoideus,  as  found  among  the  Dip- 
contraction)  and  gular  pressure  remains  noi  (Edgeworth,  1935).  Except  for  its  la- 
elevated.  This  expiratory  "gular  leakage"  teralmost  third  head  with  a  disparate  mo- 
possibly  represents  excess  air,  which  was  tor  innervation  and  therefore  origin  (Riep- 
not  pressed  into  the  lungs.  The  fact  that  pel,  1978),  the  mandibulohyoideus  is 
this  occurs  at  the  end  of  every  pumping  clearly  a  highly  differentiated  version  of 
cycle  indicates  that  the  glottis  always  closes  the  geniohyoideus,  ubiquitous  among  the 
before  the  nares  open.  Such  carefully  co-  vertebrates.  The  rectus  cervicis  of  caeci- 
ordinated  timing  suggests  that  this  may  be  lians  is  homologous  with  the  stemohyoid- 
a  hard-wired  mechanism  designed  to  pre-  eus  in  both  frogs  and  monitor  fizards. 
vent  air  escaping  from  the  lungs,  which  Lacking  a  pectoral  girdle,  caecilians  lack 
have  been  pressurized  by  gular  pumping.  an  omohyoideus. 

The  branchiohyoideus  is  found  in  nei- 

Origin  of  Gular  Pumping  j-j-^^^j.  anurans  nor  caecilians.   Its  putative 

The  gular  pump  of  monitor  lizards  bears  homologue,  subarcualis  rectus  I  (not  the 

striking  resemblance  to  the  buccal  pump  larval   branchiohyoideus    extemus;    Edge- 

of  extant  amphibians,  in  function  and  in  worth,  1935,  contra  Smith,  1920),  is  pre- 

mechanism.  Both  pumps  generate  positive  sent  in  urodeles,  but  the  EMG  activity  of 

pressure  to  force  air  from  the  phaiyngeal  this  muscle  during  buccal  pumping  is  yet 

cavity   into   the   lungs.    Both   employ  the  to  be  investigated.  Nevertheless,  EMG  ev- 

hyobranchial  apparatus  to  produce  volu-  idence  from  feeding  studies  in  Ambystonia 

metric  changes   of  the  buccal   and  gular  (Lauder  and  Shaffer,  1985;  Reilly  and  Lau- 

cavdties.  This  similarity  suggests  that  buc-  der,  1991)  shows  that  the  subarcualis  rec- 

cal  pumping  and  gular  pumping  may  be  tus  I  is  active  during  buccal  expansion  in 

homologous  behaviors.  However,  the  de-  aquatic  and  terrestrial  prey  capture,  and  its 

rived  moq^hologv'  of  the  monitor  lizards  role  in  generating  buccal  expansion  during 

and   their  deeply  nested  position   in   the  suction  feeding  has  been  deduced  from  its 

squamate  phylogeny  (Estes  et  al.,   1988)  anatomical  position  and  fiber  orientation 

suggest  the  possibility  that  gular  pumping,  in  various  salamanders  (Erdman  and  Cun- 

as  ventilatory  behavior,  may  have  evolved  dall,  1984;  Lauder  and  Shaffer,  1988;  Lo- 

independently  in  monitor  lizards.  This  al-  renz-Elwood    and    Cundall,    1994).    This 

temative  hypothesis  would  be  supported  suggests  that  the  subarcuaHs  rectus  I  func- 

by  finding  that  the  gular  and  buccal  pumps  tions  in  much  the  same  way  in  the  buccal 

are  powered  by  nonhomologous  muscles,  pump  of  salamanders  as  does  the  bran- 

or  that  the  patterns  of  their  activation  are  chiohyoideus  in  the  gular  pump  of  lizards, 

markedly  different.  Having    established    the    homology    of 

Lepldosaurs,   especially  the  highly  de-  hyobranchial  muscles  of  amphibians  and 


246         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


IM 
IH 

GH 
OH 
RC 
BH 


E        C 

I 

I 

(not  measured) 


CD 


absent 


E        C 


(A) 

Dermophis 


(B) 

Rana 


(C) 

Varanus 


Figure  5.  Comparison  of  hyobranchial  muscle  activity  patterns  during  a  single  pressure  pump  cycle  in  (A)  a  caecilian  {Der- 
mophis), (B)  a  frog  (Rana),  and  (C)  a  monitor  lizard  (Varanus).  Homologous  muscles  are  shown  in  the  same  row.  Each  pumping 
cycle  (E  +  C)  has  been  scaled  to  the  same  duration  time  (the  scale  bars  are  0.2  seconds).  Pressures  (bottom  trace)  have  been 
scaled  to  the  same  peak  value;  maximum  peak  pressures  range  from  4  cm  HjO  (frog)  to  15  cm  Hfi  (caecilian  and  monitor 
lizard).  Abbreviations:  E,  active  expansion;  C,  compression;  GH,  m.  geniohyoideus;  IH,  m.  interhyoideus;  RC,  m.  rectus  cervicis; 
others  as  in  Figure  2.  (A)  is  modified  from  Carrier  and  Wake  (1995);  (B)  is  a  composite  of  de  Jongh  and  Gans  (1969)  and  West 
and  Jones  (1974);  and  (C)  is  from  this  study. 


lizards,  it  is  possible  to  directly  compare 
their  activity  patterns  in  the  gular  pump  of 
V.  exanthematicus  and  in  the  buccal  pump 
of  a  caecilian  (Carrier  and  Wake,  1995) 
and  an  anuran  (de  Jongh  and  Gans,  1969; 
West  and  Jones,  1974).  Differences  in 
pressure  profiles  aside,  all  three  neuro- 
motor patterns  clearly  are  similar  (Fig.  5). 
This  suggests  that  homologous  hyobran- 
chial muscles  function  in  much  the  same 


way  in  these  distantly  related  clades. 
Therefore,  the  homology  of  the  gular  and 
buccal  pumping  behaviors  cannot  be  re- 
jected. 

Nevertheless,  analysis  of  the  present 
data  does  not  allow  us  to  conclude  with 
confidence  that  the  gular  and  buccal 
pumps  are  homologous  behaviors.  Neuro- 
motor similarity  is  not  sufficient  to  claim 
that    a    behavioral    mechanism    has    been 


EMG  Pattern  of  Gular  Pump  •  Otverkowicz  et  al.        247 


conserved  in  evolution  (Smith,  1994).  Un- 
like other  situations  in  which  the  neuro- 
motor pattern  is  conser\'ed  despite  func- 
tional divergence  (e.g.,  in  the  evolution  of 
terrestrial  and  aerial  locomotion;  Goslow 
et  al.,  1989),  the  gular  pump  may  repre- 
sent functional  convergence  with  the  buc- 
cal pump  by  using  homologous  structures. 
The  question  of  homology  in  the  case  of 
the  gular  pump  is  made  even  more  com- 
plex by  the  fact  that  cycles  of  gular  expan- 
sion and  compression  are  also  used  in 
feeding  (Smith,  1986),  gular  flutter  (Heat- 
wole  et  al.,  1973),  and  throat  displays  (Bels 
et  al.,  1995).  One  or  more  of  these  behav- 
iors could  have  retained  the  ancestral  mo- 
tor pattern  for  hyobranchial  movement 
and  this  pattern  could  have  been  co-opted 
for  lung  ventilation  (with  appropriate 
modification  of  narial  and  glottal  vaKdng). 
The  next  study  undertaken  to  explore  the 
homology  of  buccal  and  gular  pumping 
should  be  a  broad  comparative  analysis  to 
map  the  character  of  gular  pumping  (its 
presence  or  absence)  on  the  phylogeny  of 
Amniota.  Preliminaiy  investigations  within 
Squamata  indicate  that  gular  pumping  is 
widespread  among  nonserpentine  squa- 
mates  (Deban  et  al.,  1994;  Al-Ghamdi  et 
al.,  2001;  Brainerd  and  Owerkowicz,  per- 
sonal obsei-vation).  This  result,  combined 
wdth  our  finding  of  neuromotor  similarity 
in  the  pumping  mechanisms  of  monitor 
lizards  and  amphibians,  suggests  that  the 
gular  pump  of  lizards  may  have  been  re- 
tained continuously  from  a  buccal  pump- 
ing ancestor. 

ACKNOWLEDGMENTS 

Fuzz  Crompton  provided  the  original 
inspiration  for  this  study  by  explaining  the 
nuance  between  "gular"  and  "buccal."  Un- 
der Fuzz's  guidance,  T.  O.  honed  his  ex- 
perimental skills  in  radiographic,  electro- 
myographic, and  histologic  techniques 
used  in  this  study.  T.  O.  wishes  to  express 
his  gratitude  to  Fuzz  for  his  mentorship 
and  support  over  the  last  decade.  We 
thank  C.  Farmer  and  L.  Claessens  for 
lending    a    hand    wdth    the    surgeries,    K. 


Schwenk  for  his  invaluable  critique  of  the 
early  version  of  the  manuscript,  and  the 
Festschrift  editors  F.  A.  Jenkins,  Jr.,  and 
M.  D.  Shapiro  for  their  infinite  patience. 
We  appreciate  L.  Meszoly  for  his  render- 
ing of  the  hyoid  apparatus,  and  C.  Musin- 
sky  for  applying  finishing  touches  to  the 
figures.  This  work  was  supported  by  the 
Chapman  Fellowship  (Harvard  University) 
to  T.  O.,  and  by  National  Science  Foun- 
dation grants  IBN-9875245  to  E.  L.  B.  and 
IBN-9807534  to  D.  R.  C. 

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332-344. 


SYNCHRONIZATION  OF  ELECTROMYOGRAPHIC  ACTIVITY  IN  ORAL 
MUSCULATURE  DURING  SUCKLING  AND  DRINKING 


A.  J.  THEXTON'  AND  REBECCA  Z.  GERMAN^^ 

Abstract.  Suckling  and  drinking  are  rh>thmic  ac- 
tivities, widi  an  electromyographic  pattern  that  is 
characterized  by  a  significant  coactivation  of  muldple 
muscles  that  are  not  obvious  svoiergists.  If  die  rh\i;hm 
and  coactivation  were  due  to  conventional  excitation 
of  motor  neurons  by  a  single,  central  source  of 
rhvthm  generation  then,  within  the  periods  of  coac- 
tiv  ation,  there  should  also  be  a  degree  of  sy:ichroni- 
zation  of  muscle  action  potentials,  similar  to  that  es- 
tablished for  respiration.  Both  respiration  and  suck- 
ling are  activities  that  can  persist  in  die  absence  of 
the  cerebral  hemispheres.  However,  in  a  preliminary 
study  of  suckling,  evidence  for  synchronization  was 
not  characteristic  of  most  of  the  coactive  muscles. 
Marked  rhythmic  coactivation  of  muscles  is  also  char- 
acteristic of  the  cerebrally  directed,  more  mature  ac- 
tivit)'  of  drinking.  Synchronization  of  action  potentials 
in  other  conscious  movements  suggests  that  cere- 
brally directed  drinking  might  differ  from  suckling 
with  respect  to  the  level  of  synchronization.  We  test- 
ed this  hvpothesis  in  miniature  pigs  by  cross-corre- 
lation analysis  of  the  electromyographic  activitv'  re- 
corded in  multiple  oral  and  submandibular  muscles 
during  suckling  and  drinking  in  the  same  animals. 
Evidence  of  intraburst  synchronization  was  found  in 
only  a  few  muscles  (sternohyoid,  omohyoid,  and  ge- 
niohyoid) during  suckling,  but  that  evidence  was  ab- 
sent in  drinking  in  exactly  the  same  muscles  in  the 
same  animals.  A  tentative  ex-planation  for  the  paucit\' 
of  evidence  for  sjiichronization  in  suckling,  despite 
the  coactivation  of  muscles,  is  that  the  rhythmic  mus- 
cle activitv  is  generated  by  plateau  potentials  in  in- 
dividual motor  neurons;  this  is  a  phylogenetically 
primitive  mechanism  with  respect  to  mammals.  The 
absence  of  evidence  for  svnchronization  in  drinking 
may  reflect  the  fact  that  the  neural  mechanisms  for 
drinking  precede  those  for  suckling  phylogenetically, 
although  not  ontogenetically. 

INTRODUCTION 

Rhythmic  oral  movements  can  be  gen- 
erated  by   brainstem    mechanisms   alone. 


'  Physiology  Department,   Kings  College  London 
(School  of  Biomedical  Sciences  of  Guy's,  King's  and 


Suckling  occurs  in  the  anencephalic  hu- 
man infant  (Hall,  1833;  Gamper,  1926; 
Monnier  and  Willi,  1953)  and  rhythmic 
chewing  or  lapping  movements  can  be 
elicited  in  decerebrate  animals  (Bremer, 
1923).  These  reports  are  consistent  with 
the  subsequent  localization  of  a  central 
pattern  generator  (CPG)  for  rhythmic  oral 
movements  within  the  brainstem  (Dellow 
and  Lund,  1971).  Nevertheless,  cerebro- 
cortical  centers  have  been  described  for 
both  mastication  and  for  suckling  (Iriki  et 
al.,  1988).  When  these  higher  centers  are 
functional,  they  may  simply  supply  drive  to 
the  CPG  (Bremer,'  1923;  Lund  and  Del- 
low,  1971)  but  their  activity  may  also  in- 
teract with  the  brainstem  mechanisms  in 
other  ways,  including  direct  monosynaptic 
connections  to  trigeminal  motor  neurons 
(Mishima  et  al,  1982;  Moriyama,  1987; 
Ohta  et  al,  1989;  Ohta  and  Saeki,  1989). 
The  pattern  of  activity  of  cortical  motor 
neurons  can,  in  the  case  of  the  limbs,  be 
directly  related  to  the  amplitude  and  to 
the  direction  of  a  resultant  limb  movement 
(Georgopoulos,  1995)  so  that  a  similar  ac- 
tion in  directing  oral  activity  towards  ex- 
traorally  located  food  is  to  be  expected  in, 
for  example,  drinking. 

When  the  infant  pig  locates  on  an  arti- 
ficial teat,  rhythmic  suckling  is  only  trig- 
gered when  milk  is  present  (German  et  al., 
1997)  and  suckling  then  continues  as  a  re- 


st. Thomas's  Hospitals),  St.  Thomas's  Campus,  Lam- 
beth Palace  Road,  London  SEl  9RT. 

-  Department  of  Biological  Sciences,  Universitv'  of 
Cincinnati,  Cincinnati,  Ohio  45221-0006. 

^  To  whom  correspondence  should  be  addressed. 


Bull.  Mus.  Comp.  ZooL,  156(1):  249-256,  October,  2001         249 


250         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


sponse  to  the  intraoral  delivery  of  the  liq-  the   drive   to   the   inotor   neurons   during 

uid.  Conversely,  drinking  is  directed  to  the  suckling  does   not  produce   simultaneous 

acquisition  of  an  extraorally  located  liquid  intraburst  spikes  during  EMG  activity  in 

and  the  maintained  direction  of  this  activ-  most  of  the  coactive  muscles  (but  does  in 

ity  is  likely  to  involve  cortical  activity.  The  just  a  few  hyoid  muscles).  This  contrasts 

postnatal  maturation  of  cerebral  functions  with  studies  of  rhythmic  somatic  activity 

might  then  relate  to  the  ability  to  change  (Sears  and  Stagg,  1976)  in  adult  animals 

from  suckling  to  drinking.  and  with  studies  of  cortically  directed  ac- 

Consequently,  the  aim  of  this  study  was  tivity  (Datta  and  Stephens,  1990)  where 
to  test  the  proposition  that  some  aspect  of  synchronization  can  be  regularly  demon- 
the  generation  or  control  of  the  pattern  of  strated.  Consequently,  the  initial  hypoth- 
electromyographic  (EMG)  activity  in  esis  was  that,  in  drinking,  action  potentials 
drinking  differed  from  that  in  suckling.  As  within  bursts  of  EMG  activity  of  some 
a  first  stage  in  this  investigation,  a  form  of  pairs  of  muscles  might  show  greater  de- 
analysis  was  adopted  that  had  originally  grees  of  synchronization,  compared  to  the 
been  developed  in  relation  to  the  rhythmic  more  immature  acti\dty  of  suckling, 
activity  of  respiration  (Sears  and  Stagg,  /^  o 
1976).  Respiration  is  a  similar  activity  to  MATERIALS  AND  METHODS 
suckling  and  drinking  in  the  sense  that  res-  Three  miniature  pigs  (Sii.s  scrofa),  each 
piration  is  generated  by  a  CPG  and  as  such  3  weeks  old,  were  trained  to  feed  in  a  box 
involves  a  number  of  different  muscles  from  an  artificial  teat.  At  this  age  pigs  are 
that  exliibit  simultaneous  bursts  of  EMG  at  the  start  of  weaning;  some  individuals 
activity.  Each  of  these  bursts  of  EMG  ac-  will  repeatedly  change  their  mode  of  in- 
tivity  consists  of  a  number  of  individual  gestion  from  suckling  to  drinking  and  back 
spikes  or  muscle  action  potentials,  hence-  again  within  a  few  minutes  (depending 
forth  referred  to  as  intraburst  spikes.  Some  upon  how  the  food  is  made  available). 
of  these  intraburst  spikes  occur  at  the  Consequently,  data  comparisons  can  be 
same  time  in  the  muscles  of  different  in-  made  in  which  there  is  no  significant  time 
tercostal  spaces,  that  is,  the  different  mus-  delay  during  which  electrodes  can  move  or 
cles  are  not  only  coactivated  but  show  syn-  deteriorate  or  during  which  other  longer- 
chronous  firing  within  the  periodic  bursts,  term  maturational  changes  can  confuse  the 
indicating  that  some   of  the   motor  neu-  picture. 

rones  receive  identical  synchronous  acti-  The  methods  used  in  these  experiments 

vation.  have  been  described  in  detail  elsewhere 

The  demonstration  of  synchronization  (Thexton  et  al.,  1998)  so  that  only  a  brief 
of  spikes  within  bursts  of  EMG  activity  oc-  description  is  given  here.  Under  general 
curring  at  the  same  time  (in  two  different  anesthesia  (halothane/oxygen),  the  sub- 
but  coactive  or  synergistic  muscles)  only  mandibular  musculature  was  exposed  and 
indicates  that  a  proportion  of  the  action  individual  muscles  identified.  Bipolar  fine 
potentials  arriving  presynaptically  at  the  wire  electrodes  were  then  inserted  into  the 
motor  neurons  are  also  synchronous.  Cor-  muscles  and  the  leads  passed  via  a  sub- 
tically  originating  activity  acting  on  two  cutaneous  tunnel  to  a  multipole  connector 
synergistic  muscles  is  often  associated  with  on  the  back.  After  recovery,  the  animals 
a  degree  of  such  synchronization  in  the  were  again  fed  in  the  box,  allowing  the 
EMGs.  Similarly,  a  CPG  supplying  two  multipole  connector  to  be  connected  to 
synergistic  muscles  will  also  produce  syn-  amplifiers.  The  amplified  signals  were  then 
chronization  of  a  proportion  of  the  spikes  recorded  on  tape  for  off-line  digitization, 
in  the  two  EMGs.  All  analysis  was  carried  out  on  the  digi- 

In  contrast,  pilot  studies  on  infant  pigs  tized  data. 
(Banks  and  Thexton,  1999)  indicated  that  The  EMG  activity  in  the  relevant  mus- 


Synchronization  in  Muscles  During  Suckling  •  Thexton  and  German       251 


cles  was  first  half-wave  rectified  and  the 
spike  peaks  identified.  The  spike  peaks 
were  then  converted  to  point  events  and 
all  events,  wdth  an  amplitude  less  than  10% 
of  the  maximum,  were  eliminated  as  being 
due  largely  to  noise,  that  is,  they  were  set 
to  zero;  all  the  other  events  were  given  a 
\alue  of  one.  A  pairwise  correlation  be- 
tween the  two  series  of  point  events  was 
then  calculated.  This  was  then  repeated 
for  different  time  shifts  of  one  data  set  rel- 
ative to  the  other,  for  example,  from  f,,  — 
40  milliseconds  to  ^o  +  40  milliseconds, 
where  t^  is  zero  time  shift  between  the  two 
data  sets  (Fig.  1).  If  any  tendency  exists 
for  intraburst  spikes  to  occur  either  syn- 
chronously in  the  two  data  streams  or  with 
a  regular  time  lag  in  one  data  stream  with 
respect  to  the  other,  they  come  to  corre- 
spond with  each  other  at  one  of  the  time 
shifts  and  so  produce  a  larger  correlation 
at  that  time  shift. 

The  EMG  activities  were  analyzed  to 
determine  if  any  difference  existed  in  the 
level  of  synchronization  occurring  in  suck- 
ling and  drinking.  The  hypothesis  was  that 
if  the  two  activities  arose  or  were  centrally 
influenced  in  different  ways,  as  indicated 
in  the  Introduction,  there  might  be  differ- 
ent levels  of  synchronization. 

RESULTS 

The  data  analyzed  in  this  study  were  the 
multichannel  EMG  activities  recorded  in 
a  variety  of  muscles  during  suckling  and 
during  drinking.  The  EMG  activity  record- 
ed during  a  short  period  of  drinking  is 
shown  in  Figure  2.  The  period  contained 
just  over  six  cycles  of  movement  including 
three  cycles  in  which  swallowing  was  pre- 
sent; the  three  swallowing  cycles  were  as- 
sociated with  the  three  higher-amplitude 
bursts  of  activity  in  the  hyoglossus.  Simul- 
taneous bursts  of  EMG  activity  occurred 
in  a  number  of  muscles  that  are  innervated 
by  different  motor  nuclei,  for  example,  di- 
gastric (V),  stylohyoid  (VII),  and  hyoglos- 
sus (XII).  This  coactivation  of  sets  of  mus- 
cles is  characteristic  of  the  activity  in  feed- 


ing in  the  weaning  pig,  whether  suckling 
or  drinking  (Thexton  et  al.,  1998). 

When  the  EMG  signals  obtained  from 
the  submandibular  muscles  during  suck- 
ling were  processed,  they  produced  a  se- 
ries of  correlograms  that,  for  the  most 
part,  were  flat  (Figs.  3A-C).  Across  all 
three  animals  the  expected  central  peaks, 
indicative  of  short-  or  medium-term  syn- 
chronization, were  generally  absent,  as 
previously  reported  (Banks  and  Thexton, 
1999).  The  only  cross-correlograms  with 
visible  central  peaks,  which  were  consis- 
tent with  synchronization,  were  those  that 
were  obtained  by  the  crosscorrelation  of 
geniohyoid,  sternohyoid,  and  omohyoid 
activity  (Figs.  3D,  E);  of  these,  the  cross- 
correlation  between  sternohyoid  and  omo- 
hyoid activity  provided  the  clearest  evi- 
dence (in  two  out  of  three  animals). 

When  the  same  analyses  were  applied 
to  drinking  data,  the  results  were  similar 
in  so  far  as  the  cross-correlograms  were 
generally  flat.  However,  the  results  dif- 
fered in  that  no  obvious  central  peaks  oc- 
curred in  the  cross-correlations  derived 
from  the  geniohyoid,  sternohyoid,  or  omo- 
hyoid signals.  Direct  intra- animal  compar- 
isons were  also  made  between  the  cross- 
correlations  of  omohyoid,  sternohyoid,  and 
geniohyoid  activity  in  suckling  and  the 
same  cross-correlations  in  drinking.  In  two 
animals  (that  within  minutes  would  change 
from  suckling  to  drinking  and  back  again) 
the  evidence  for  intraburst  synchroniza- 
tion, which  was  clearly  evident  in  muscles 
such  as  sternohyoid  and  omohyoid  during 
suckling  (Fig.  3E),  was  always  absent  in 
drinking  (Fig.  3F). 

DISCUSSION 

One  of  the  earliest  studies  that  provided 
evidence  of  intraburst  synchrony  among 
the  motor  units  of  cocontracting  muscles 
(Sears  and  Stagg,  1976)  was  carried  out  on 
the  respiratory  system,  that  is,  on  a  rhyth- 
mic activity  produced  by  a  brainstem  pat- 
tern generator.  Suckling  and  drinking  sim- 
ilarly involve  cocontracting  muscles  and, 
on  current  evidence,  are  also  generated  by 


252         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


A     Data  2  shifted  0  time  units  with  respect  to  Data  1 


1  T 


1  -^ 


01001010101000 

LUil 


00101001010100 


Cross 

Products:       00001    000000000 

Sum=1 


E     Data  2  shifted  +2  time  units  with  respect  to  Data  1 


I  Mill 


1  -L 


Cross 

Products:      OOOOIOIOOOOOOO 

Sum=2 


B     Data  2  shifted  -1  time  units  with  respect  to  Data  1 


1  T 


1    -L 


MM 


Cross 

Products:      01000010101000 

Sum=4 


C     Data  2  shifted  -2  time  units  with  respect  to  Data  1 

1  - 

lllll 

0  ■ 

1  - 

Cross 
Produc 

ts: 

D    0 

D    0    0 

0    0 

0    0 

0    0    0    0    0 

Sum=0 

D     Data  2  shifted  +1  time  units  with  respect  to  Data  1 


I  Mill 


1  -L 


Cross 

Products:       000000001    01    000 

Sum=2 


Figure  1.  Cross-correlation  using  two  ultrashort  sections  of  synthetic  data  in  binary  form.  Such  data  sets  are  produced  If  the 
peaks  of  half-wave  rectified  electromyographic  (EMG)  activity  are  reduced  to  point  processes  indicating  the  presence  or  the 
absence  of  a  spike  peak;  the  example  shown  could  represent  the  spikes  in  a  single  burst  of  EMG  activity.  In  (A),  the  two  data 
series  (shown  both  as  binary  and  as  graphical  data)  are  initially  correctly  aligned  in  time  (zero  time  shift  or  Q.  At  each  point  in 
time,  the  product  of  the  values  in  the  two  series  is  obtained  and  this  is  then  summed.  In  (B),  data  set  2  is  moved  one  unit  back 


Synchronization  in  Muscles  During  Suckling  •  Thexton  and  German        253 


Swallow 


Swallow 


Swallow 


GH, 

GG 

OMO 

STH 

HYOG 

HYOG 

DIG 


1 


Time  -  sec 

Figure  2.  Raw  electromyogram  (EMG)  signals  recorded  from  representative  muscles  during  drinking.  In  several  muscles  two 
sets  of  electrodes  were  inserted  to  establish  that  the  signals  recorded  were  not  obviously  site  dependent  within  the  muscle. 
Abbreviations  used:  GH,  geniohyoid;  GG,  genioglossus;  OMO,  omohyoid;  STH,  sternohyoid;  HYOG,  hyoglossus;  DIG,  digastric; 
subscript  numbers  identify  two  electrodes  in  the  same  muscle.  All  muscles  are  unilateral. 


a  brainstein  pattern  generator.  Conse- 
quently, the  assumption  was  that  synchro- 
ny would  also  be  present  between  coacti- 
vated  muscles  during  suckling  and  drink- 
ing. However,  most  cross-correlograms  be- 
tween inuscle  activities  showed  no 
evidence    for    intraburst    synchronization 


during  either  suckling  or  drinking  (Fig.  3; 
Banks  and  Thexton,  1999).  Nevertheless, 
peaks  that  were  consistent  with  synchro- 
nization were  evident  in  the  cross-corre- 
lograins  of  sternohyoid,  geniohyoid,  and 
omohyoid  activities,  with  the  cross-corre- 
lation between  stemohvoid  and  omohyoid 


in  time  (t  ,)  relative  to  data  set  1;  again  the  products  of  the  values  in  the  two  series  are  obtained  and  summed.  In  (C),  the 
process  is  repeated  with  data  set  2  moved  back  two  units  back  in  time  (f^s)  relative  to  data  set  1 .  In  (D),  the  process  is  repeated 
with  a  time  shift  of  +1  time  units  (f,)  and  in  (E)  with  a  time  shift  of  +2  time  units  (y.  In  (F),  the  sum  of  cross  products  (a  count 
of  those  spikes  that  coincided  at  a  particular  time  shift)  is  plotted  against  the  time  shift.  In  these  synthetic  data,  the  maximum 
correspondence  between  spikes  in  the  two  data  sets  occurred  with  a  shift  of  f  ,.  In  practice  two  data  sets  each  at  least  15,000 
time  units  long,  containing  many  hundreds  of  spike  locations,  are  cross-correlated. 


254         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


DIG-GH  (suck) 


GH-OMO  (suck) 


A. 


200  T 


:ll4lH«av^l|/ll^^ 


0  I   I   I    I   I    I   I   I    I   I   I 
-40  0 

ms 


+40 


I   I    I   I    I   I   I    I   I   I   I    I   I   I   I    I 

-40  0  +40 

ms 


HYOG-STYLO  (suck) 


STH-OMO  (suck) 


B. 


E. 


80  T 


c. 


GG-GH  (suck) 


300  T 


■MH^^fif^^ 


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

40  0  +40 

ms 


STH-OMO  (drink) 


'^°i4Ww»w^^ 


1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 

40  0  +40 

ms 


I 


Figure  3.  Cross-correlations  between  signals  detected  by  different  pairs  of  electrodes  in  one  animal.  Abbreviations  used:  DIG, 
digastric;  GH,  geniohyoid;  HYOG,  hyoglossus;  STYLO,  styloglossus;  GG,  genioglossus;  OMO,  omohyoid;  STH,  sternohyoid. 
The  horizontal  axis  indicates  time  shift  relative  to  zero  time  shift  (fg).  Examples  of  cross-correlations  that  were  commonly  found 
in  suckling  are  shown  in  (A),  (B),  and  (C).  Some  evidence  of  short-term  synchronization  (elevation  of  central  region  ±  2  milli- 
seconds) in  suckling  is  present  in  (D)  and  stronger  evidence  is  present  in  (E).  In  (F),  the  activities  in  the  same  muscles  as  in 
(E)  were  recorded  during  drinking  and  were  cross-correlated  but  with  no  sign  of  a  central  peak. 


providing    the    clearest    evidence    of   the 
presence  of  synchronization. 

Before  deahng  with  the  significance  of 
this  finding,  it  is  necessary  to  comment 
briefly  on  its  vahdity.  First,  the  results 
shown  in  Figure  3E  indicate  that  the 
cross-correlation  method  used  in  this  pa- 
per was  intrinsically  capable  of  detecting 
synchronization  within  the  recorded  EMG 


signals.  However,  motor  neurons  are  acti- 
vated froin  multiple  sources  within  the 
central  and  peripheral  nei'vous  systems 
and  not  all  the  motor  neurons  supplying 
units  in  a  given  muscle  are  subject  to  the 
same  neural  influences.  Consistent  with 
this,  some  motor  units  have  different  tasks 
from  others  within  the  same  muscle.  If 
EMG  activity  is  recorded  with  an  intra- 


Synchronization  in  Muscles  During  Suckling  •  T/j^xfon  and  German        255 


muscular  wire  electrode  (which  only  re- 
cords from  a  limited  number  of  motor 
units)  the  record  will  represent  a  restricted 
sample  of  the  different  motor  units  within 
that  muscle.  If,  by  chance,  the  sample 
from  one  of  the  two  muscles  being  cross- 
correlated  does  not  include  motor  units 
that  receive  drive  synchronous  with  the 
sample  in  the  other  muscle,  then  the 
cross-correlograms  will  be  flat.  This  sug- 
gests that  those  motor  units,  the  activity  of 
which  generated  flat  correlograms,  were 
essentially  firing  randomly  in  time.  How- 
ever, such  correlograms  do  not  prove  that 
other  motor  units  within  the  muscles 
would  not  exliibit  synchrony.  Therefore, 
the  general  failure  to  detect  signs  of  syn- 
chrony in  this  study  is  best  interpreted  as 
indicating  a  scarcity  of  synchronized  units 
in  most  coactive  muscles,  with  synchro- 
nized units  simply  being  more  frequently 
found  in  the  coactive  geniohyoid,  sterno- 
hyoid, and  omohyoid  muscles  during  suck- 
ling. 

One  possible  scenario  is  that  a  large 
number  of  neurons  and  synapses  intervene 
between  the  CPG  neurons  generating  the 
rhythmic  activity  and  most  of  the  motor 
neurons  receiving  that  rhythinic  drive.  Be- 
cause of  the  nonlinear  input-output  rela- 
tions at  each  synapse,  considerable  tem- 
poral dispersion  of  the  signals  would  then 
occur  and  the  original  synchronous  drive 
would  become  diluted  by  other  influences 
also  acting  at  those  synaptic  relays.  Thus, 
although  the  rhythmic  drives  to  the  motor 
neurons  of  the  different  coactive  muscles 
would  still  be  expected  to  wax  and  wane 
together,  little  of  the  intraburst  spike  gen- 
eration would  still  be  synchronous  in  the 
coactive  muscles.  However,  this  mecha- 
nism would  not  be  consistent  with  the 
abrupt  "on"  and  "off"  of  the  bursts  seen 
in  the  recorded  EMG  activity  (Fig.  2). 

Thus,  a  problem  may  exist  with  the  con- 
cept of  a  CPG  producing  the  activities  of 
suckling  or  drinking  purely  by  supplying  a 
rhythmically  fluctuating  drive  to  the  dif- 
ferent motor  neuron  groups  producing  the 
EMG  pattern  seen  in  Figure  2.  In  fact,  the 


absence  of  consistent  evidence  for  syn- 
chrony (Fig.  3)  suggests  that  the  drive 
from  the  CPG  may  not  directly  supply  se- 
ries of  action  potentials  that  produce  a  cu- 
mulative depolarization  of  most  of  the  mo- 
tor neurons  and,  therefore,  most  of  the 
spike  production  in  the  coactive  muscles. 
However,  if  the  central  pattern  generator 
functioned  as  an  on-off  switch,  simply 
triggering  the  motor  neurons  into  becom- 
ing their  own  independent  burst  genera- 
tors, no  synchronization  would  occur  be- 
tween intraburst  spikes  in  coactive  mus- 
cles. That  situation  can  arise  when  motor 
neurons  are  simply  triggered  to  produce 
long-lasting  depolarizations  known  as  pla- 
teau potentials.  Although  such  potentials 
are  well  known  in  invertebrates  (Croll  et 
al.,  1985),  they  have  only  relatively  recent- 
ly been  described  as  occurring  in  mam- 
mals. It  is  of  particular  interest  that  these 
potentials  have  been  found  in  mammalian 
motor  nuclei  involved  in  generating  the 
movements  of  feeding  (Mosfeldt  Laursen 
and  Rekling,  1989;  Rekling  and  Feldman, 
1997). 

Whatever  the  mechanisms  involved  in 
generating  the  rhythmic  movements,  the 
results  clearly  do  not  support  the  initial 
ontogenetic  hypothesis,  that  the  EMG  sig- 
nals in  the  more  mature  and  probably  cor- 
tically  directed  activity  of  drinking  would 
show  more  synchronization  than  in  suck- 
ling. However,  suckling  is  an  evolutionary 
novelty  (Clark  and  Smith,  1993;  German 
and  Crompton,  2000),  whereas  mammali- 
an drinking  is  probably  a  substantially  old- 
er evolutionary  trait,  functionally  resem- 
bling drinking  in  other  nonmammalian  tet- 
rapods.  Consequently,  the  neural  basis  of 
drinking  could  reflect  the  evolutionary 
heritage  of  mammals  and,  in  that  sense,  be 
less  derived  than  suckling.  The  limited  ev- 
idence for  synchrony  during  suckling, 
which  is  absent  in  drinking,  might  reflect 
the  contemporaneous  evolution  of  suck- 
ling and  the  more  developed  central  ner- 
vous system  that  characterizes  maminals. 


256         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


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SONOMICROMETRY  AND  KINEMATIC  ESTIMATES  OF  THE 
MECHANICAL  POWER  OF  BIRD  FLIGHT 


DOUGLAS  R.  WARRICK,^  BRET  W.  TOBALSKE,^  ANDREW  A.  BIEWENER,^  AND  KENNETH  P.  DIAU' 


Abstract.  To  improve  our  measurements  of  me- 
chanical power  output  of  fl>'ing  birds,  we  examined 
the  congruency  between  two  recording  techniques  of 
pectoralis  muscle-length  change  (sonomicrometric 
and  kinematic)  used  in  empirical  measures  of  the  me- 
chanical power  output  of  black-billed  magpies  flying 
over  their  fufl  range  of  flight  speeds  (0-14  m/s)  in  a 
variable-speed  wdnd  tunnel.  Simultaneous  recordings 
of  pectoralis  muscle  force  (obtained  from  strain  gaug- 
es attached  to  the  muscle's  humeral  insertion)  were 
integrated  with  the  bA'O  recording  technicjues  to  gen- 
erate a  work-loop  for  each  wingbeat.  Although  the 
overall  shapes  of  the  power  curves  obtained  by  the 
h\'o  techniques  were  similar,  estimates  of  muscle 
lengtli  change  using  sonomicrometric  data  were,  on 
average,  very  similar  to  those  obtained  by  one-axis 
kinematics  and  slightly  lower  than  those  obtained  by 
two-axis  kinematics.  Given  these  small  differences, 
our  sonomicrometry  measurements  indicate  that  ki- 
nematic estimates  of  muscle  length  change,  when 
combined  with  humeral  strain  measurements,  can 
provide  an  accurate  estimate  of  pectoralis  work  and 
power  output  during  bird  flight.  However,  a  key  ad- 
vantage of  sonomicrometry  is  that  it  provides  a  direct 
measure  of  the  lengthening  and  shortening  of  the 
muscle's  fascicles  relative  to  their  rest  length,  which 
is  not  possible  to  derive  from  wing  motion  alone. 

INTRODUCTION 

The  cost  of  flight  is  central  to  under- 
standing the  biology  of  any  fl>Tng  animal. 
In  particular,  without  knowing  the  meta- 
bolic costs  of  flight,  conclusions  obtained 
from  time  and  energy  budget  studies  of 
birds  regai-ding  selection  for  migration 
habits,  optimal  foraging  behaviors,  and  re- 
productive strategies  will  remain  unclear 


'  Division  of  Biological  Sciences,  University  of 
Montana,  Missoula,  Montana  59812. 

-  Concord  Field  Station,  Harvard  University,  Bed- 
ford, Massachusetts  01730. 

^  To  whom  reprint  requests  should  be  addressed. 


(Welham    and   Ydenberg,    1993;    Heden- 
strom  and  Alerstam,  1995). 

Various  approaches  have  been  taken  to 
address  the  metabolic  power  requirements 
of  flight.  The  mechanical  cost  of  flight  may 
be  modeled  using  aerodynamic  theory 
(Pennycuick,  1975;  Rayner,  1979),  and  the 
metabolic  cost  of  flight  can  then  be  in- 
ferred using  estimates  of  the  muscular  ef- 
ficiency of  converting  metabolic  energy  to 
mechanical  work  (Pennycuick,  1989; 
Thomas  and  Hedenstrom,  1998).  Meta- 
bolic power  has  been  measured  directly 
over  a  limited  midrange  of  flight  speeds  by 
means  of  oxygen  consumption  studies  of 
birds  flying  in  a  wind  tunnel  (Tucker,  1968, 
1972;  Berger  et  al,  1970;  Torre-Bueno 
and  LaRochelle,  1978;  Rothe  et  al,  1987). 
Other  methods  have  included  measure- 
ments of  doubly-labeled  water  (Hails, 
1979;  Flint  and  Nagy,  1984)  and  heart  rate 
(Berger  et  al,  1970;  Butler  et  al,  1977)  of 
birds  in  flight.  More  recently,  infrared  im- 
aging has  also  been  used  to  assess  meta- 
bolic power  (Speakman  et  al.,  1997;  Ward 
et  al.,  1997).  However,  many  of  these  stud- 
ies have  been  restricted  to  a  narrow  range 
of  flight  speeds  and  flight  behavior,  pre- 
venting a  complete  picture  of  metabolic 
cost  versus  flight  speed.  Thus,  models  of 
mechanical  power  are  the  most  useful 
means  currently  available  for  predicting 
flight  costs  over  a  wide  range  of  speeds. 
The  wide  acceptance  and  use  of  such  me- 
chanical power  models  (Welham  and 
Ydenberg,  1993;  Pennycuick,  1997)  sug- 
gests that  it  may  prudent  to  provide  an  in- 
dependent test  of  their  accuracy. 

In  a  previous  study  (Dial  et  al.,  1997), 


Bull.  Mus.  Comp.  ZooL,  156(1):  257-268,  October,  2001         257 


258         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


the  mechanical  power  output  of  black- 
billed  magpies  (Pica  pica)  was  measured 
using  force-calibrated  strain  gauges  at- 
tached to  the  deltopectoral  crest  (DPC), 
which  serves  as  the  insertion  site  of  the 
primary  downstroke  flight  muscle  (mus- 
culus  pectoralis)  on  the  humerus.  These 
force  measurements  were  integrated  with 
kinematics  of  the  wing  to  estimate  the  me- 
chanical power  output  of  the  pectoralis 
and,  hence,  the  whole  bird.  When  appro- 
priate kinematic  parameters  (Tobalske  and 
Dial,  1996;  Tobalske  et  al,  1997)  are  in- 
corporated in  models  based  on  aerody- 
namic theory,  predicted  power  output 
agrees  reasonably  well  with  our  earlier 
measureinents  of  mechanical  power  out- 
put of  magpies  (Rayner,  1999).  Our  pre- 
vious measurements  used  kinematic  esti- 
mates of  pectoralis  length  change.  How- 
ever, some  questions  remain  regarding  es- 
timates of  the  magnitude  and  timing  of 
pectoralis  length  change  inferred  from  dis- 
tal wing  movement  in  the  work  of  Dial  et 
al.  (1997).  In  the  present  study,  we  reas- 
sess the  mechanical  power  output  of  mag- 
pies based  on  direct  sonomicrometric 
measurements  of  pectoralis  fascicle  length 
changes  and  compare  these  data  directly 
with  corresponding  kinematic  estimates 
based  on  wing  excursion. 

MATERIALS  AND  METHODS 

Bird  Training  and  Wind  Tunnel  Trials 

Three  black-billed  magpies  were  trained 
to  fly  in  a  wind  tunnel  (Tobalske  and  Dial, 
1996)  over  a  range  of  flight  speeds  (0—14 
m/s)  that  represented  the  full  extent  that 
the  animals  were  willing  to  fly.  Birds  were 
housed  in  the  University  of  Montana's  an- 
imal facility  and  given  food  and  water  ad 
libitum.  The  protocol  for  all  facilities,  care, 
and  surgical  procedures  was  approved  by 
the  Institutional  Animal  Care  and  Use 
Committee  established  at  the  University  of 
Montana. 

Force-Strain  Measurements 

Birds  were  anesthetized  (25  mg/kg  ke- 
tamine  and  2  mg/kg  xylazine,  supplement- 


ed as  needed)  and  the  feathers  removed 
over  the  left  shoulder  and  the  middle  of 
the  back  between  the  scapulae.  A  15-mm 
incision  was  made  in  the  skin  overlying  the 
DPC,  which  was  then  exposed  by  gently 
parting  the  fascicles  of  the  deltoid  muscle. 
The  dorsal  surface  of  the  DPC  was  pre- 
pared by  lightly  scraping  away  the  perios- 
teum and  then  swabbing  the  underlying 
bone  surface  with  methyl-ethyl  ketone  to 
remove  any  residual  tissue  and  to  dry  the 
site.  A  strain  gauge  (single-element  metal 
foil  type  FLE-05-11,  Tokyo  Sokki  Kenk- 
yujo,  Ltd.,  Tokyo,  Japan)  was  then  at- 
tached to  the  dorsal  surface  of  the  DPC 
using  self-catalyzing  cyanoaciylate  adlie- 
sive,  with  its  principal  axis  aligned  approx- 
imately 15°  proximal  to  the  perpendicular 
axis  of  the  humeral  shaft  (Dial  and  Biew- 
ener,  1993).  Strain  gauge  lead  wires  (36 
gauge.  Teflon  insulated;  Micromeasure- 
ments  Inc.)  ran  beneath  the  deltoid  and 
subcutaneously  to  a  miniature  connector 
plug  (Microtech  FG-6  [X2])  that  was 
mounted  on  the  back  of  the  bird  by  su- 
turing the  plug's  epoxy  base  securely  to  the 
intervertebral  ligaments  using  0  silk.  The 
sldn  was  drawn  snugly  around  the  protrud- 
ing connector  plug,  and  the  surrounding 
skin  was  covered  with  elastic  surgical  tape. 

The  DPC  strain  signals  were  transmit- 
ted to  bridge  amplifiers  (Vishay  model 
2120A,  Micromeasurements  Inc.)  via  two 
light-weight  shielded  cables  running 
through  a  small  hole  in  the  top  of  the  wind 
tunnel  test  section.  Raw  in  vivo  DPC 
strains,  sonomicrometry  signals,  and  elec- 
tromyograms  (see  below)  were  sampled  at 
5,000  Hz  by  a  Keithley  Instruments  A/D 
converter  and  stored  in  a  computer.  To 
monitor  the  quality  of  the  recordings  dur- 
ing the  experiment,  live  data  from  each  tri- 
al were  printed  on  a  Gould  2400  chart  re- 
corder. 

In  past  studies,  the  tensile  strains  ex- 
perienced by  the  DPC  during  flight  were 
calibrated  to  pectoralis  force  in  situ  after 
flight  trials.  However,  in  all  three  birds,  af- 
ter flights  at  all  eight  speeds  had  been  re- 
corded, either  the  bonding  of  the  strain 


Mechanical  Power  Output  of  Magpie  Flight  •  Warrick  et  al.        259 


gauge  to  die  bone  or  the  strain  gauge  itself  0.74-mm   offset  was   added  to  all  length 

failed.  Rather  than  attempting  to  reattach  measurements.     Total     fascicle     length 

the  strain  gauge  to  the  DPC  in  the  same  change  (L)  for  the  pectoralis  was  calculat- 

position  or  use  another  strain  gauge  for  ed  as: 

calibration,  we  chose  to  leave  the  DPC  j    _  j  tr     j                          /i\ 

strain   data  uncalibrated  as  raw  voltages.  i     ir     r. 

Although  this  precluded  a  quantification  of  where  L,  is  the  change  in  distance  between 

pectoralis  force  and  calculation  of  muscle  the  sonomicrometry  crystals,  L\^  is  the  local 

work,    relative    work-loops    derived    from  resting  length  between  the  crystals,  and  L^ 

raw  DPC  strain  voltages  coupled  with  fas-  is  the  total  (average)  resting  length  of  the 

cicle  length  changes  (from  sonomicrome-  pectoralis    muscle    fascicles    measured   to 

try,   next  section)  provide  valuable  infor-  with  0.5  mm  using  digital  calipers, 
mation  concerning  the  relative  change  in 

mechanical  power  as  a  function  of  flight  vVOrK-lOOps 

speed  (henceforth  "uncalibrated  power").  The  work  done  throughout  one  wing- 
To  average  the  data  for  all  three  birds,  the  beat  cycle  (W^^.^)  'was  calculated  by  inte- 
uncalibrated  power  required  for  flight  at  grating  the  change  in  DPC  strain  with  the 
all  speeds  was  normalized  relative  to  the  change  in  fascicle  length: 
maximum  ("relative")  power  recorded  for  ^^^  _  v-p  /j  _  j  \i  (n\ 
each  individual,  which  for  all  three  birds  "^^  ~  ^  "^  "  "^''^  ^  ' 
was  observed  during  hovering  flight.  where  F  is  the  DPC  strain  voltage  and  L 

is  the  pectoralis  fascicle  length  at  the  same 

Sonomicrometry  point  in  the  time  series  n.  Only  that  part 

Sonomicrometiy  crystals    (2-mm   SL-2,  of  the  wingbeat  cycle  during  which  posi- 

Triton  Inc.)  were  implanted  in  the  anterior  tive    strain   voltages   were    recorded   (i.e., 

region  of  the  left  pectoralis  muscle  of  each  when  the  gauge  measured  tensile  strain, 

bird  in  a  position  thought  to  represent  best  rather  than  the  compressive  strain  experi- 

the  contraction  of  the  entire  muscle  (as  enced  by  the  DPC  during  upstroke)  was 

suggested  in  Shigeoka  [1999]).  Each  ciys-  used  to  calculate  relative  pectoralis  work, 

tal  was  mounted  on  a  stainless  steel  wire  Relative  work  (volt  X  mm)  was  then  divid- 

featuring  two  anchoring  points  ("loops"),  ed  by  the  cycle  time  {t)  for  each  individual 

After  a  skin  incision  was  made  to  expose  work-loop  to  obtain  an  estimate  of  relative 

the  pectoralis  muscle,  the  muscles  fasci-  muscle  power  (Fig.   1).  Measurements  of 

cles  were  parted  using  surgical  scissors,  relative  power  were  obtained  over  a  range 

creating  two  openings  into  which  the  crys-  of  speeds,  based  on  averages  at  each  speed 

tals  were  inserted.  Once  aligned,  the  ciys-  obtained  from  a  minimum  of  two  wing- 

tals  were  held  in  place  by  suturing  the  two  beats  (for  magpie  3  during  hovering  flight) 

anchoring  loops  to  the  surrounding  muscle  and  a  maximum  of  23  wingbeats  (magpie 

tissue  and  fascia.  The  wires  for  the  crystals  3  at  8  m/s). 
were  passed  subcutaneously  to  the  dorsal 

side  of  the  bird  and  connected  to  the  back  Kinematics 

plug.  After  closing  the  incision,  the  birds  Each  trial  was  videotaped  from  lateral 

were  allowed  to  recover  from  the  anesthe-  (Panasonic  S-VHS)  and  caudal  (Sony  Hi-8 

sia  for  approximately  24  hours.  The  resting  Handicam)  views.  Video  from  each  trial 

length  between  the  crystals  (resting  fasci-  was  captured  on  computer  (Iomega  Buz 

cle  length,  LJ  was  taken  while  the  bird  Video  Capture),   and  bitmap  still  images 

was  standing  at  rest,  with  its  wings  held  (60  fields  per  second  [fps])  were  digitized 

against  its  body.   To  compensate  for  the  using  NIH  Image.  The  x  and  ?/ coordinates 

faster  transmission  of  the  ultrasound  pulse  of  the  bird's  eye,  tail  base,  and  wing  tip 

through  the  epoxy  lens  of  each  ciystal,  a  were  scaled  using  a  2-cm  grid  background 


260         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Magpie  3 


14  ms" 


10 


12 


14 


Flight  speed  (m  s'  ) 


Figure  1 .  Work-loops  (insets)  created  by  plotting  the  change  in  tensile  strain  (y  axis,  in  volts  not  calibrated  to  force)  of  the 
deltopectoral  crest  by  the  fiber  length  (x  axis,  mm).  The  area  of  the  work-loop  above  zero  volts  was  integrated  to  calculate  work 
done  by  the  pectoralis.  Dividing  this  area  by  the  wingbeat  cycle  time  yields  a  measure  of  relative  power.  The  mean  relative 
power  output  (±  SDs)  of  magpie  3  is  shown  over  the  range  of  flight  speeds. 


located  behind  the  bird,  adjusted  for  cam- 
era parallax,  and  imported  into  Microsoft 
Excel.  The  eye  and  base  of  the  tail  were 
used  to  establish  the  orientation  of  the 
body  from  which  the  excursion  of  the  wing 
tip  was  measured  (Fig.  2).  From  lateral 
views,  the  excursion  of  the  wing  tip  was 
calculated  both  one  dimensionally  (in  the 
dorsoventral  plane,  following  Dial  et  al. 
[1997];  Fig.  2A)  and  two  dimensionally 
(dorsoventral  and  anteroposterior  planes; 
Fig.  2B).  Wing-tip  excursion  was  used  to 
estimate  DPC  excursion  and,  hence, 
change  in  pectoralis  fiber  length  by  the 
formula  L  =  sin~^{h/b)r,  where  h  is  die 
wing-tip  excursion  (either  one  or  two  di- 
mensionally), b  is  wing  length  ineasured 
from  the  wing  tip  to  the  glenoid,  and  r  is 


the  distance  from  the  glenoid  to  the  DPC. 
For  those  wingbeats  in  which  simulta- 
neous sonomicrometric  and  kinematic  data 
were  available  (n  =  20;  magpie  1,  n  =  9; 
magpie  2,  n  =  7;  magpie  3,  n  =  5),  fascicle 
length  changes  obtained  using  the  two 
methods  were  compared  using  reduced 
major  axis  regression. 

RESULTS 

Sonomicrometry  and  strain-gauge  data 
were  obtained  from  magpies  2  and  3  over 
the  entire  speed  range,  whereas,  because 
of  equipment  failure,  ineasurements  of 
magpie  1  were  only  obtained  over  speeds 
from  0  to  8  m/s. 

As  was  the  case  in  our  earlier  study 
(Dial  et  al,  1997),  all  three  birds  exiiibited 


Mechanical  Power  Output  of  Magpie  Flight  •  Warrick  et  al. 


261 


10  12 

Sonomicrometry  (mm) 


14 


16 


B 


16  T 


10  12 

Sonomicrometry     (mm) 


14 


16 


Figure  2.  Wing  kinematics  (insets)  as  measured  from  lateral  video  images  (60  fields  per  second).  The  one-axis  (dorsoventral 
excursion  only)  wingbeat  amplitude  (2A  inset)  was  measured  as  in  Dial  et  al.  (1997),  whiereas  thie  two-axis  excursion  (2B  inset) 
also  incorporated  thie  anteroposterior  movement  of  the  wing.  (A)  Correlation  of  one-axis  kinematic  estimate  of  fiber  length  change 
(i.e.,  deltopectoral  crest  excursion)  with  fiber  length  change  as  measured  by  sonomicrometry.  (B)  Correlation  of  two-axis  kine- 
matic estimate  of  fiber  length  change  with  fiber  length  change  as  measured  by  sonomicrometry. 


the  greatest  muscle  power  output  during 
hovering  flight  (Fig.  1).  Minimum  power 
speeds  differed  between  the  three  birds, 
being  6  m/s,  4  in/s,  and  10  m/s,  respec- 
tively, for  magpies  1,  2,  and  3.  However, 
the  low  power  output  of  magpie  3  at  10 
m/s  was  probably  due  to  a  ceiling  effect, 
because  this  bird  insisted  on  flying  close 
(<30  cm)  to  the  ceiling  of  the  test  cham- 
ber. This  likely  resulted  in  the  disruption 
of  tip  vortices  and  consequent  reduction 


in  drag,  causing  the  low  observed  power 
output. 

Strain  estimated  from  single-axis  kine- 
inatics  was  positively  correlated  with  strain 
ineasured  for  the  same  muscle  contraction 
using  sonomicrometry.  Although  signifi- 
cant, the  correlation  was  not  strong  (r-  = 
0.36;  ij  =  0.98x-  +  0.78;  F  =  0.003,  df  = 
18;  Fig.  2A).  Fiber  length  changes  esti- 
inated  from  two-axis  kinematics  and  son- 
omicrometry exliibited  a  stronger  correla- 


262         Btilletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


tion  (r2  =  0.52,  ij  =  1.02.T  +  2.4;  P  < 
0.0001,  df  =  18;  Fig.  2B). 

Our  sonomicrometric  measurements  of 
fascicle  strain  reported  here  were  10% 
greater  than  those  estimated  in  our  pre- 
vious study  of  magpie  flight  based  on 
wingbeat  kinematics  (Dial  et  al.,  1997). 
Across  all  speeds,  mean  fascicle  strain  (L/ 
L/lOO)  obtained  from  sonomicrometry  av- 
eraged 27.6%  for  magpie  1,  36.2%  for 
magpie  2,  and  35.0%  for  magpie  3.  The 
greatest  fascicle  strain  was  recorded  dur- 
ing hovering  flight  for  magpies  1  and  3 
(32.2  ±  1.1%  and  46.0  ±  0.9%,  respec- 
tively), whereas  magpie  2  exliibited  the 
greatest  strain  at  14  m/s  (43.5  ±  0.3% 
[SE]). 

Averaging  the  relative  muscle  power 
among  birds  (by  first  normalizing  each  in- 
dividual's uncalibrated  relative  power  out- 
put at  each  speed  to  the  maximum  for  that 
individual)  yielded  relative  power  curves 
similar  to  those  that  we  previously  report- 
ed (Figs.  4A,  B).  When  the  maximum  rel- 
ative power  obtained  for  magpies  in  this 
study  is  set  to  the  maximum  power  (W) 
reported  in  Dial  et  al.  (1997),  Figure  4B 
reveals  a  similar  shape  for  the  power 
curves  derived  from  the  two  approaches 
(sonometric  versus  kinematic).  This  is  par- 
ticularly the  case  over  the  intermediate 
speed  range  (8-12  m/s),  where  a  marked 
increase  in  mean  power  output  at  8  m/s  is 
observed  in  both  sets  of  data.  In  the  pre- 
sent study  two  of  the  three  birds  exliibited 
this  increase,  whereas  power  increased  at 
8  m/s  for  all  three  individuals  in  the  pre- 
vious study. 

DISCUSSION 

Our  new  results  for  magpies,  obtained 
from  direct  measurements  of  muscle 
length  change  using  sonomicrometry,  but 
relying  on  a  relative  estimate  of  pectoralis 
force  and,  thus,  power  output,  generally 
agree  well  with  the  measurements  of  me- 
chanical power  output  that  we  obtained  in 
our  previous  study  using  kinematic  esti- 
mates of  muscle  length  change  (Dial  et  al., 
1997).  For  both  data  sets,  power  output 


was  highest  during  hovering,  dropped  rap- 
idly (—40%)  at  2  m/s,  reached  minimum 
values  at  intermediate  speeds,  and  then  in- 
creased again  modestly  (—20%)  at  the  fast- 
est speeds  (12  and  14  m/s).  As  was  the  case 
in  our  earlier  study  (Dial  et  al.,  1997),  min- 
imum power  speed  varied  among  birds  (6, 
4,  and  10  m/s  for  magpies  1,  2,  and  3,  re- 
spectively), and  no  bird  exliibited  mini- 
mum power  at  8  m/s  (Fig.  3A).  Conse- 
quently, our  sonomicrometry  measure- 
ments provide  support  for  the  use  of  ki- 
nematic data  (accounting  for  both  humeral 
elevation— depression  and  protraction— re- 
traction) to  estimate  muscle  length  change 
and,  when  combined  with  DPC  strain 
measurements,  to  calculate  muscle  work 
and  power  output. 

Given  that  all  three  birds  possessed  fair- 
ly uniform  wing  and  tail  dimensions,  the 
variance  in  power  curves  among  birds  was 
most  likely  due  to  differences  in  flight  be- 
havior. As  noted  above,  differences  in  the 
birds'  flight  positions  in  the  test  section  of 
the  wind  tunnel  also  likely  affected  our  es- 
timated power  output.  For  example,  the 
low  power  obtained  at  10  m/s  for  magpie 
1  may  well  have  resulted  from  its  flying  in 
close  proximity  to  the  ceiling  of  the  tunnel. 
Individual  differences  may  also  reflect  dif- 
fering behavioral  reactions  that  the  birds 
exliibited  having  to  fly  at  a  fairly  uniform 
speed  because  of  the  space  restrictions  of 
the  wind  tunnel.  Magpies  (or  any  bird,  for 
that  matter)  rarely  fly  at  steady  speeds  in 
the  wild,  instead  exliibiting  gait  modula- 
tion and  intermittent  flight;  when  flying  in 
a  wind  tunnel,  magpies  adopt  a  more  reg- 
ular pattern  of  gait  modulation  than  they 
exliibit  outdoors  (Tobalske  et  al.,  1997).  It 
is  likely  that  some  birds  are  more  adept 
(i.e.,  capable  of  assuming  body  postures 
and  wing  presentations  that  reduce  their 
flight  power  requirement)  than  others  at 
flying  with  greater  modulation  of  their 
normal  flight  pattern.  Nevertheless,  our 
findings  of  a  fairly  flat  power  curve  over 
much  of  this  species'  speed  range  are  gen- 
erally consistent  with  aerodynamic  theoiy 
(Rayner,  1999;  Fig.  4B;  Appendix),  existing 


Mechanical  Power  Output  of  Magpie  Flight  •  Warrick  et  al. 


263 


B 


0 


8 


10  12 


14 


Flight  speed  (m  s' ) 
I  Sonomicrometry  D  Kinematic  (Dial  et  al.  '97) 


Magpie  3  sonomicrometry  vs 
Dial  et  al.  '97  Kinematic 


8  10  12 


14 


Flight  speed  (m  s' ) 


■  Sonomicrometry  D  Kinematic  (Dial  et  al '97) 

Figure  3.  (A)  Mean  percent  (standard  deviations)  pectoralis  muscle  strain  (change  in  fiber  length/resting  fiber  length  x  100)  of 
the  three  magpies  over  the  range  of  flight  speeds.  (B)  Mean  pectoralis  muscle  strain  for  magpie  3  compared  with  pectoralis 
muscle  strain  estimated  from  distal  wing  kinematics  from  our  previous  study. 


metabolic  data  (Ellington,  1991),  and  our 
earlier  findings  based  on  force  measure- 
ments and  wing  kinematics. 

Despite  the  general  consistency  of  our 
measurements  of  pectoralis  length  change 
with  those  based  previously  on  wing  ki- 
nematics, sonomicrometry  has  a  clear  ad- 


vantage by  providing  a  direct  measure  of 
the  lengthening  and  shortening  of  the 
muscle's  fascicles  relative  to  their  resting 
length.  This  enables  an  assessment  of  the 
fractional  length  change  of  the  muscle  as- 
sociated with  active  lengthening  versus  ac- 
tive shortening.  Consistent  with  earlier  ki- 


264         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Relative  "Power" 


0.5   - 


10 


12 


14 


16 


Flight  speed  (m  s' ) 


Magpie  1 
"Magpie  3 


-  Magpie  2 
•mean% 


^^^>>>v>>.X> 


I 


10        12        14        16        18        20       22        24       26       28 

Flight  speed  (m  s"  ) 
•Sonomicrometry  "=-^"Dial  et  al. '97 

Theoretical,  C=  0.05  ""  ~  Theoretical,  C=  0.4 


Figure  4.  (A)  Mean  relative  power  (mean  uncalibrated  power  for  a  bird  at  a  flight  speed  normalized  to  the  bird's  maximum 
power  output  speed,  which  was  0  m/s  In  all  cases)  of  all  three  magpies  over  the  range  of  flight  speeds.  (B)  Mean  power  output 
of  magpies  flying  over  the  same  range  of  speeds  from  Dial  et  al.  (1997)  and  the  present  study.  For  purposes  of  comparing  the 
shapes  of  the  power  curves,  the  uncalibrated  relative  power  at  hovering  was  set  to  equal  the  mean  power  at  hovering  from  Dial 
et  al.  (1997).  The  theoretical  power  curve  was  derived  from  modified  momentum  jet  theory,  using  a  Q  coefficient  of  either  0.4 
(dashed  line  upper;  Pennycuick,  1989)  or  0.05  (dashed  line  lower;  Pennycuick  et  al.,  1996)  and  an  Induced  power  factor  of  1.2 
(see  Appendix).  Note  that  although  magpies  seem  to  possess  sufficient  power  to  fly  at  speeds  well  above  20  m/s,  their  top 
sustainable  speed  In  the  wind  tunnel  was  14  m/s. 


nematic  estimates  (Dial  and  Biewener, 
1993)  and  recent  sonomicrometiy  mea- 
surements of  length  changes  in  pigeons 
(Biewener  et  al.,  1998),  we  find  that  pec- 
toralis  force  development  during  the 
downstroke  of  magpies  is  achieved  over  a 


surprisingly  large  range  of  muscle  length 
change  (35—50%  of  resting  length,  over  the 
range  of  recorded  speeds).  Moreover,  this 
is  achieved  primarily  by  the  muscle  being 
lengthened  (mean:  28%)  versus  being 
shortened  (inean:  10%)  relative  to  its  rest- 


Mechanical  Power  Output  of  Magpie  Flight  •  Warrick  et  al.        265 


ing   length.    This   large   length   change   is  component).   For  lift  to  be  produced,   a 

clearly  linked  to  the  pectoralis's  function  in  portion  of  the  wing  inust  have  a  positive 

generating  considerable  mechanical  power  angle  of  attack  relative  to  incident  air.  If, 

by  moving  the  wing  through  a  broad  range  at  faster  speeds,  the  angular  velocity  of  the 

(approximately  80—110°)  during  the  down-  wing  during  downstroke  is  not  sufficient  to 

stroke.  maintain  a  positive  angle  of  attack  while 

Classical  aerodynamic  theory  predicts  a  directing  the  net  aerodynamic  force  for- 
U-shaped  power  curve  for  any  flying  ob-  ward  (i.e.,  providing  thrust),  the  animal 
ject.  Under  steady-state  conditions,  the  will  be  unable  to  sustain  flight, 
underlying  physics  of  this  relationship  is  It  is  noteworthy  that  the  empirical  curve 
inevitable.  However,  one  conclusion  sug-  of  inechanical  power  was  generally  similar 
gested  by  analysis  of  our  empirical  data  to  predicted  curves  at  slow  and  interme- 
relative  to  theoretical  power  curves  (Fig.  diate  speeds  (Fig.  3B),  particularly  given 
4B)  is  that  magpies  may  not  be  able  to  fly  that  we  used  published  values  for  induced 
fast  enough  to  achieve  the  speeds  neces-  power  factor  and  drag  coefficients  in  pre- 
sary  to  incur  a  significant  rise  in  power  re-  dieting  the  mechanical  power  required  for 
quirement,  such  as  a  U-shaped  curve  flight  in  die  magpie  (Appendix).  We  as- 
would  predict.  Our  ineasurements  of  me-  sumed  an  induced  power  factor  of  1.2, 
chanical  power  output  at  0  and  2  m/s  which  gives  an  estimate  of  induced  power 
might  seem  to  suggest  that  magpies  should  during  hovering  that  is  approximately  30% 
be  able  to  attain  speeds  of  up  to  18-28  m/  lower  than  that  that  would  result  from  vor- 
s  (Fig.  3B).  However,  the  greater  power  tex  theory  (Rayner,  1979;  Ellington,  1984). 
output  achieved  at  these  very  low  speeds  However,  a  magpie  flying  in  the  closed- 
likely  reflects  nonsustainable  flight  perfor-  section  flight  chamber  could  have  enjoyed 
mance  and  a  significant  anaerobic  energy  a  27—31%  reduction  in  power  costs  be- 
supply.  Consistent  with  this  interpretation,  cause  of  lift  recirculation  (Rayner,  1994; 
we  found  that  well-trained  birds  (before  Tobalske  and  Dial,  1996).  Thus,  it  would 
surgery)  rarely  achieved,  and  could  never  be  unwise  to  use  our  data  to  address  the 
sustain,  16  m/s  in  the  tunnel.  This  is  also  validity  of  inomentum  jet  theory  versus 
consistent  with  observations  of  the  maxi-  vortex  theory  as  applied  to  slow  flight  in 
mum  flight  speeds  recorded  for  magpies  birds.  Further  research  into  inechanical 
in  the  field  being  only  11  m/s  (Tobalske  et  power  output  during  free  flight,  in  the  ab- 
al.,  1997),  as  well  as  our  observation  of  a  sence  of  ground  effects,  therefore,  would 
low  variance   in  power  output  at  higher  be  worthwhile. 

speeds  (Dial  et  al.,  1997).  We  have  argued  At  fast  speeds,  our  empirical  data  are 

tliat  decreased  variation  in  wingbeat  kine-  less  than  predicted  values  obtained  from  a 

matics  and  power  output  suggests  a  more  model  using  a  coefficient  of  body  drag  = 

constrained  flight  style  as  an  animal  ap-  0.4  (Pennycuick,   1989)  and  greater  than 

proaches   its   limit   of  sustainable   perfor-  those  from  a  more  recent  model  using  a 

mance.  Consequently,  we  interpret  14  m/  coefficient  of  body  drag  =   0.05  (Penny- 

s  as  this  species'  maximum  sustained  flight  cuick  et  al.,  1996).  Assuming  our  estimates 

speed.  of  induced  and  profile  power  are  correct. 

An  alternative  explanation  for  the  ob-  this  comparison  suggests  that  the  coeffi- 

served  maximum  flight  speed  may  be  that  cient  of  body  drag  for  the  magpie  should 

the  inagpies  were  unable  to  generate  suf-  be  somewhere  between  0.4  and  0.05,  and 

ficient  thrust  at  speeds  greater  than  14  m/  that  the  magpie  has  a  relatively  "dirty"  or 

s.  A  bird  engaged  in  flapping  flight  gen-  nonstreamlined  shape  compared  to  soine 

crates  lift  with  its  wings  that  provides  both  bird    species    (Pennycuick    et    al.,    1996). 

weight    support    (vertical    component    of  With   regard  to  predictions  of  minimum 

aerodynamic  force)  and  thrust  (horizontal  cost  of  transport  (work  per  unit  distance. 


266         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


or  power  divided  by  flight  speed),  which  is 
generally  expected  by  ecologists  and  oth- 
ers to  define  maximum  range  speed,  or  i;,,,^, 
it  can  be  inferred  from  Figure  4B  that  pre- 
dicted u,„r  would  differ  greatly  depending 
upon  parasite  drag.  Using  our  empirical 
data,  we  calculate  u^ir  to  be  12  m/s.  In  con- 
trast, v„^^  was  10  m/s  using  a  coefficient  of 
body  drag  of  0.4  and  18  m/s  using  a  co- 
efficient of  body  drag  of  0.05.  This  brief 
analysis  shows  that  a  specific  prediction  of 
t;,^r  for  a  given  bird  species  should  be  re- 
garded with  caution,  if  not  distrust,  unless 
direct  measures  of  mechanical  or  meta- 
bolic power  are  used  to  support  the  pre- 
diction. 

ACKNOWLEDGMENTS 

K.  P.  D.  and  A.  A.  B.  would  like  to  thank 
A.  W.  "Fuzz"  Crompton  for  his  input  and 
extraordinarily  positive  attitude  toward  our 
research  efforts  and  life  in  general.  We 
thank  F.  A.  Jenkins,  Jr.,  for  the  invitation 
to  the  Crompton  Symposium  and  for  the 
review  by  his  editorial  staff  of  this  manu- 
script for  publication.  This  project  was 
funded  by  NSF-IBN-9507503  to  K.  P.  D. 

LITERATURE  CITED 

Berger,  a.  J.,  J.  S.  Hart,  and  O.  Z.  Roy.  1970. 
Respiration,  oxygen  consumption  and  heart  rate 
in  some  birds  during  rest  and  flight.  Zeitschrift 
fiir  Vergleichende  Physiologie,  66:  201-214. 

BiEWENER,  A.  A.,  W.  R.  Corning,  and  B.  W.  To- 
BALSKE.  1998.  In  vivo  pectoraHs  muscle  force — 
length  behavior  during  level  flight  in  pigeons 
(Colli inba  livia).  Journal  of  Experimental  Biolo- 
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APPENDIX  1 


■v 


Numerous  assumptions  are  intrinsic  to 
mathematical  models  of  mechanical  power 
in  animal  flight,  and  it  is  beyond  the  scope 
of  this  paper  to  compare  the  family  of 
curves  that  could  be  generated  using  dif- 
ferent aerodynamic  theories  (Pennycuick, 
1975;  Rayner,  1979;  Ellington,  1984)  and 
their  associated  estiinates  of  lift  and  drag 
on  a  body  and  flapping  wings.  As  an  alter- 
native, we  modeled  aerodynamic  power 
using  equations  and  simplifying  assump- 
tions in  Norberg  (1990),  which  were  mod- 
ified froin  the  work  of  Pennycuick  (1975) 
and  Rayner  (1979).  Total  power  was  cal- 
culated as  the  sum  of  induced,  parasite, 
and  profile  power;  thus,  we  neglected  in- 
ertial power  (Van  den  Berg  and  Rayner, 
1995)  and  ventilation  and  circulation  fac- 
tors (Pennycuick,  1975).  We  selected  an 
induced  power  factor  of  1.2  (Pennycuick, 
1975,  1989)  even  though  induced  power 
factors  of  1.5  or  1.7  are  predicted  from 
vortex  theory  (Rayner,  1979;  Ellington, 
1984).  For  drag  coefficients  on  the  body 
and  wings,  we  employed  values  from  pub- 
lished  sources    (Pennycuick,    1975,    1989; 


Pennycuick  et  al,  1996;  Rayner,  1979), 
and  we  treated  the  body  as  a  flat  plate 
(Pennycuick,  1975)  rather  than  a  tilted-cyl- 
inder  (Rayner,  1979).  Our  predicted  me- 
chanical power  curves  should  not  be  in- 
terpreted to  represent  the  only,  or  best, 
curves  that  can  be  synthesized  from  exist- 
ing theory. 

Symbols  and  assumed  values: 

b      =  wing  span  =  0.573  m 

Cb  =  drag  coefficient  for  body,  0.4  (Pen- 
nycuick, 1989)  or  0.05  (Pennycuick 
et  al,  1996) 

C,^  =  drag  coefficent  for  wdngs,  0.02  (Ray- 
ner, 1979) 

g  =  gravitational  acceleration,  9.805  m 
s-2 

k  =  induced  power  factor,  1.2  (Penny- 
cuick, 1975,  1989) 

m    =   body  inass  =  0.174  kg 

Pi  =  induced  power  during  forward 
flight 

Fji,    =   induced  power  during  hovering 

Fp^  =   parasite  power 

^pro  ~  profile  power,  assuming  constant 
wing  area  and  mean  resultant  veloc- 
ity (Norberg,  1990). 

P{  =  total  mechanical  power  during  for- 
ward flight 

Fi,  =  total  mechanical  power  during  hov- 
ering 

S  =  coinbined  surface  area  of  both 
wings  =  0.064  m"- 

Sb  =  frontal  area  of  body  0.00238  m'^ 
(Pennycuick,  1989) 

Sj    =   disk  area,  0.2578  m^ 

S,  =  strip  area  at  distance  r  from  wing 
root 

T  =  wingbeat  duration,  s,  assumed 
wingbeat  frequency  of  7.5  Hz 

t  =  proportion  of  wingbeat  in  down- 
stroke  (assuined  0.55) 

V     =   flight  velocity 

V,    =   induced  velocity 

V^  =  resultant  velocity  on  wing  at  strip 
distance  r  from  wing  root 

W   =  body  weight,  1.706  N 

(f)  =  wing  amplitude  in  radians,  assumed 
to  be  1.57  (  =  90°) 


268         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


p      =   air  density,  1.115  kg  m  ^.  To  calculate  induced,  parasite,  and  profile 

powers: 

To  calculate  total  mechanical  power  dur-  p   _  uti/2/o    .c  /cr\ 

ing  hovering  flight:  ' 

PiH  =  \^wy{2pv,s,r'         (6) 

Fk  =  P.H  +  Pp.  +  Pp.  (3)  ^^^  ^  0.5pt;3S,C,  (7) 

And  during  forward  flight:  ^J^ 

P,ro  =    2    [(1-77  -  10-3)  pb'^sp.yr'T^] 

r   =    0.01 

P,=  P,  +  F,,„  +  P,„  (4)  (8) 


TRADE-OFF  BETWEEN  MODELING  AND  REMODELING 
RESPONSES  TO  LOADING  IN  THE  MAMMALIAN  LIMB 


DANIEL  E.  LIEBERMAN^  AND  OSBJORN  M.  PEARSON^ 


Abstract.  This  paper  tests  the  hypothesis  that  cor- 
tical bone  growth  (modeUng)  and  repair  (Haversian 
remodeling)  responses  to  exercise-induced  mechani- 
cal loading  vary  according  to  loading  and  position 
within  the  skeleton.  Higher  rates  of  modeling  and 
Haversian  remodeling  are  predicted  to  occur  in  re- 
sponse to  loading,  but  a  trade-off  is  predicted  be- 
tween modeling  and  Haversian  remodeling,  with  pro- 
portionately higher  Haversian  remodeling  rates  at 
distal  than  proximal  midshafts,  and  proportionately 
higher  modeling  rates  at  proximal  than  distal  mid- 
shafts. The  hypothesis  is  tested  with  cross-sectional 
and  histologic  data  from  juvenile  sheep  (Ovis  aries) 
who  trotted  at  low  speed  (4  km/h)  for  60  min/d  on  a 
treadmill  for  90  days,  compared  with  sedentary  con- 
trols. Exercised  sheep  had  higher  periosteal  modeling 
and  Haversian  remodeling  rates  than  controls.  In 
both  groups,  midshaft  periosteal  growth  rates  were 
higher  in  proximal  than  distal  elements  in  inverse 
proportion  to  the  area-normalized  inertial  cost  of  ac- 
celerating mass;  midshaft  Haversian  remodeling  rates 
were  higher  in  distal  than  proximal  elements  in  pro- 
portion to  the  same  energetic  cost.  The  results  sug- 
gest that  growing  animals  modulate  modeling  versus 
remodeling  responses  to  loading  at  different  skeletal 
locations  in  order  to  optimize  cross-sectional  strength 
relative  to  the  kinetic  energy  cost  of  accelerating  add- 
ed mass. 

INTRODUCTION 

This  paper  tests  a  hypothesis  initially 
proposed  by  Lieberman  and  Crompton 
(1998)  about  the  processes  by  which  bones 
optimize  in  vivo  responses  to  mechanical 
loading.  The  observation  that  bones  adjust 
dynamically  to  their  functional  environ- 
ment (Wolffs  law)  has  been  well  substan- 
tiated over  the  last  100  years  despite  a 
poor  understanding  of  the  high  degree  of 


'  Department  of  Anthropology,  Harvard  University, 
Cambridge,  Massachusetts  02138. 

-  Department  of  Anthropology,  University  of  New 
Mexico,  Albuquerque,  New  Mexico  87131. 


variability  that  characterizes  osteogenic  re- 
sponses to  mechanical  loading  (see  Lanyon 
and  Rubin,  1985;  Bertram  and  Swartz, 
1991).  Such  variations  are  of  special  inter- 
est for  understanding  the  general  trend 
among  most  cursorially  adapted  mammals 
for  distal  limb  elements  to  have  smaller  di- 
ameters than  proximal  elements,  which 
gives  the  limb  a  tapered  shape  (Smith  and 
Savage,  1956;  Alexander,  1980,  1996;  Cur- 
rey,  1984).  Limb  tapering  is  almost  cer- 
tainly an  adaptation  to  minimize  the  ki- 
netic energetic  cost  of  limb  acceleration. 
At  a  given  angular  velocity,  this  cost  for  a 
limb  segment  is  proportional  to  the  prod- 
uct of  its  mass  and  the  square  of  its  mo- 
ment arm  (Hildebrand,  1985).  However, 
limb  tapering  has  a  structural  cost.  By  re- 
ducing bone  mass,  limb  tapering  decreases 
the  second  moment  area  (/)  available  to 
counteract  bending  forces  that  may  ac- 
count for  approximately  75-95%  of  mid- 
shaft strains  (Bertram  and  Biewener, 
1988).  If  applied  forces  are  similar  in  prox- 
imal and  distal  elements,  then  tapered  dis- 
tal elements  will  experience  higher  strains 
than  proximal  elements,  potentially  lead- 
ing to  the  generation  and  propagation  of 
microcracks  and  other  structural  damage 
that  ultimately  contribute  to  mechanical 
failure  (Currey,  1970,  1984;  Carter  et  al., 
1981a,b;  Martin  and  Burr,  1982,  1989; 
Burr  et  al,  1985;  Burr,  1993;  Mori  and 
Burr,  1993).  As  a  result,  distal  elements 
may  have  lower  safety  factors  than  proxi- 
mal elements  (Currey,  1984;  Alexander, 
1998). 

Some   mammals,   most  notably  equids, 
have    evolved    structural    adaptations    to 


Bull.  Mus.  Comp.  Zool.,  156(1):  269-282,  October,  2001         269 


270         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


avoid  the  potentially  higher  stresses  that 
may  result  from  limb  tapering,  including 
orientating  distal  elements  in  line  with 
ground  reaction  forces  to  decrease  bend- 
ing (Gambaiyan,  1974;  McMahon,  1975; 
Biewener,  1983a,  1989,  1990;  Biewener  et 
al.,  1988),  shortening  of  distal  elements  to 
reduce  their  bending  moments  (Gambar- 
yan,  1974;  Alexander,  1977),  and  de- 
creased curvature  of  distal  elements  to 
minimize  compressive  bending  and  buck- 
ling (Biewener,  1983a,b;  Pauwels,  1980; 
Bertram  and  Biewener,  1992).  However, 
many  cursorially  adapted  mammals,  in- 
cluding most  ungulates,  are  characterized 
by  tapered  limbs  with  long  distal  elements 
that  have  high  excursion  angles  (Gambar- 
yan,  1974).  These  species  are  predicted  to 
experience  high  functional  strains  in  their 
distal  elements  and  must  compensate 
through  other  means. 

The  two  most  important  in  vivo  pro- 
cesses by  which  distal  and  proximal  ele- 
ments can  adapt  differentially  to  functional 
loading  are  growth  (referred  to  as  model- 
ing) and  repair  (Haversian  remodeling). 
Modeling  responses  are  the  best  studied. 
Modeling  increases  resistance  to  bending 
stresses  by  augmenting  I  so  that  a  given 
force  generates  less  strain  (Wainwright  et 
al.,  1976).  Bones  model  in  response  to  me- 
chanical loads  through  increases  in  peri- 
osteal apposition  (Chamay  and  Tchantz, 
1972;  Goodship  et  al.,  1979;  Lanyon  et  al., 
1982;  Lanyon  and  Rubin,  1984;  Rubin  and 
Lanyon,  1984a,b,  1985;  Biewener  et  al., 
1986;  Raab  et  al,  1991),  and  through  in- 
hibition of  endosteal  resorption  (Woo  et 
al.,  1981;  Ruff  et  al,  1994).  The  optimal 
way  for  bones  to  minimize  mass  and  max- 
imize /  (which  is  a  fourth-power  function 
of  bone  radius),  is  to  add  mass  periosteally 
and  remove  mass  endosteally.  Because 
marrow  is  50%  as  dense  as  bone,  the  op- 
timum diameter  to  thickness  (D/t)  ratio  in 
mammals  is  predicted  to  be  4.6  (Alexan- 
der, 1981;  Currey,  1984).  One  study  of  ter- 
restrial mammals  (Currey,  1984:  109-111) 
found  the  median  D/t  ratio  to  be  approx- 
imately 4.4  (albeit  with  considerable  vari- 


ation), with  a  higher  median  value  for  the 
femur  (5.6)  and  correspondingly  lower  val- 
ues for  the  humerus  and  other  more  distal 
limb  elements. 

The  other  mechanism  by  which  bones 
adapt  to  high  functional  loads  is  to  in- 
crease the  frequency  of  bone  repair  re- 
sponses through  Haversian  remodeling. 
Haversian  remodeling  is  a  sequential  ac- 
tivation of  vascularborne  osteoclasts  on  a 
resorption  surface  that  cuts  a  channel 
through  old  bone,  followed  by  circumla- 
mellar  deposition  of  new  bone  by  osteo- 
blasts around  a  central  neurovascular 
channel  (Frost,  1963;  Martin  and  Burr, 
1989).  Haversian  remodeling  was  once 
thought  to  be  a  mechanism  for  maintain- 
ing calcium  homeostasis  (de  Ricqles  et  al., 
1991),  but  most  calcium  exchange  occurs 
in  osteocyte  canaliculi  and  through  remod- 
eling of  trabecular  bone  (Parfitt,  1988b). 
Instead,  Haversian  remodeling  in  cortical 
bone  is  probably  an  adaptation  to  strength- 
en bone  by  removing  weakened  tissue  or 
reorienting  its  structure  (Currey,  1970, 
1984;  Carter  and  Hayes  1976a,b,  1977a,b; 
Carter  et  al.,  1981a,b;  Martin  and  Burr, 
1982;  Schaffler  et  al,  1989,  1990).  Al- 
though secondary  osteonal  (Haversian) 
bone  is  weaker  in  vitro  than  young  primary 
osteonal  bone  (Currey,  1959;  Carter  et  al., 
1976;  Carter  and  Hayes  1977a,b;  Vincen- 
telli  and  Grigorov,  1985;  Schaffler  and 
Burr,  1988),  secondary  osteonal  bone  is 
stronger  than  microcrack-damaged  prima- 
ry bone  (Schaffler  et  al,  1989,  1990).  Hav- 
ersian remodeling  may  also  increase  elas- 
ticity and  halt  microfracture  propagation 
(Currey,  1984).  Several  studies  demon- 
strated that  remodeling  preferentially  oc- 
curs in  older  regions  of  bones  that  have 
presumably  accumulated  more  damage 
than  younger  bone  (Frost,  1973;  Bouvier 
and  Hylander,  1981;  Currey,  1984),  and 
that  loading  significantly  increases  remod- 
eling rates  (Hert  et  al.,  1972;  Bouvier  and 
Hylander,  1981,  1996;  Burr  et  al,  1985; 
Schaffler  and  Burr,  1988;  Mori  and  Burr, 
1993;  Lieberman  and  Crompton,  1998). 
However,   the  effectiveness  of  Haversian 


Trade-Off  Responses  to  Loading  in  the  Mammalian  Limb  •  Lieberman  and  Pearson        271 


Kinetic  energy 


Metabolic  energy 


Radius  of  Gyration 
Proximal  ►  Distal 

Figure  1 .  Predicted  variation  in  kinetic  versus  metabolic  en- 
ergy costs  of  adding  mass  as  a  function  of  moment  arm  length 
(radius  of  gyration).  Kinetic  energy  costs  increase  exponen- 
tially as  a  function  of  moment  arm,  but  ttie  metabolic  energy 
cost  of  growing  or  repairing  bone  is  predicted  to  be  constant. 


remodeling  for  counteracting  functional 
strains  has  three  major  constraints.  The 
basic  multicellular  unit  through  which 
Haversian  remodeling  occurs  requires 
blood  supply  and  cannot  take  place  in 
avascular  bone  (de  Ricqles  et  al,  1991). 
Haversian  remodeling  also  weakens  bone 
by  increasing  porosity,  although  presum- 
ably less  so  than  the  effects  of  microfrac- 
ture accumulation  (Parfitt,  1988a;  Schaf- 
fler  and  Burr,  1988;  Martin,  1995).  Finally, 
Haversian  remodeling  is  an  ineffective 
short-term  solution  to  high  in  vivo  strains 
because  the  remodeling  sequence  time  of 
a  basic  multicellular  unit  is  approximately 
30-40  days  from  activation  to  termination 
(Martin  and  Burr,  1989). 

Trade-Off  Model 

Modeling  and  remodeling  are  the  most 
labile  osteogenic  responses  to  mechanical 
loading  that  generate  phenotypically  plas- 
tic variations  in  bone  shape  and  strength. 
However,  the  effects  of  modeling  and  re- 
modeling on  limb  bones  are  predicted  to 
vary  because  of  different  costs  and  bene- 
fits, the  most  important  of  which  are  the 
energetic  costs  of  moving  bone  tissue  and 
the  metabolic  costs  of  growing  new  bone 
tissue  (illustrated  in  Fig.  1).  The  dominant 
long-term  cost  of  adding  bone  mass 
through  modeling  is  most  likely  the  kinetic 


energy  E^,)  of  accelerating  and  decelerating 
the  added  mass.  During  the  swing  phase, 
limbs  function  like  pendulums  in  which  E^^ 
increases  exponentially  in  more  distal 
bones  as  a  function  of  m^Rf,  where  m^  is 
the  mass  of  a  given  bone,  i,  and  R^  is  its 
radius  of  gyration  (Hildebrand,  1985).  In 
particular,  limb  acceleration  becomes  in- 
creasingly costly  as  the  frequency  of  loco- 
motion diverges  inore  from  the  natural 
frequency  of  oscillation  of  the  limb  in 
which  gravitational  potential  energy  at  the 
beginning  of  swing  phase  is  converted  to 
kinetic  energy  at  midswing  and  then  back 
to  gravitational  potential  energy  at  the  end 
of  the  swing  phase.  Therefore,  the  ener- 
getic costs  of  weight  increments  are  influ- 
enced both  by  the  location  of  added  mass 
and  by  the  divergence  of  stride  frequency 
from  the  natural  oscillation  frequency  of 
the  limb.  Thus,  at  a  given  speed,  modeling 
responses  to  strain  are  more  expensive  (to 
the  second  power)  in  terms  of  kinetic  en- 
ergy in  distal  than  in  proximal  elements 
(Myers  and  Steudel,  1985;  see  also  Taylor 
et  al,  1974).  Such  costs  may  be  consider- 
able in  some  species.  Taylor  and  col- 
leagues estimate  that  approximately  66% 
of  E^.  required  for  a  horse  to  nm  at  15  m/ 
s  is  spent  to  accelerate  and  decelerate  the 
three  distal  limb  segments,  whose  mass  is 
approximately  80%  bone  tissue  (Fedak  et 
al.,  1982,  Heglund  et  al,  1982a,b). 

An  additional  cost  of  modeling  and  re- 
modeling is  the  metabolic  energy  cost  (£,„) 
of  growing  and  repairing  bone  tissue.  Al- 
though cortical  bone  is  probably  expensive 
to  synthesize,  £,„  for  both  primary  and 
Haversian  bone  is  likely  to  be  constant  re- 
gardless of  skeletal  location  (see  Fig.  1). 
However,  Haversian  remodeling  is  pre- 
dicted to  incur  long-term  higher  metabolic 
costs  than  modeling  because  it  leaves  a 
bone  insufficiently  strong  to  resist  further 
strain  damage;  in  such  cases.  Haversian  re- 
modeling must  reoccur  regularly.  There- 
fore, where  mass  and  size  do  not  impose 
high  kinetic  energetic  costs,  changes  in 
cross-sectional  geometry  generated  by 
modeling  are  probably  more  effective  re- 


272         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


sponses  to  loading  than  Haversian  remod- 
eling because  they  leave  the  bone  perma- 
nently stronger  and  avoid  any  potential  in- 
creases in  porosity  that  Haversian  remod- 
eling causes.  Further  research  is  necessary 
to  establish  the  inetabolic  costs  of  cortical 
bone  growth  and  turnover. 

On  the  basis  of  the  above-defined  costs 
and  benefits,  Lieberman  and  Crompton 
(1998)  proposed  a  trade-off  model  to  pre- 
dict variations  in  modeling  and  Haversian 
remodeling  rates  in  response  to  mechani- 
cal loading  with  respect  to  the  nature  of 
the  applied  forces  (exercise)  and  skeletal 
location.  In  order  to  compare  functionally 
comparable  (hoinotypic)  sites,  the  model 
focuses  solely  on  bone  midshafts,  which 
are  usually  the  location  of  highest  bending 
forces  (Biewener  et  al.,  1986;  Biewener 
and  Taylor,  1986).  Although  both  modeling 
and  Haversian  remodeling  rates  at  bone 
midshafts  are  predicted  to  be  higher  in  an- 
imals whose  limbs  experience  more  load- 
ing, the  relative  frequency  of  modeling 
and  Haversian  remodeling  rates  are  ex- 
pected to  vary  as  a  function  of  their  radius 
of  gyration  (R;  see  Fig.  2).  Because  the 
energetic  cost  of  modeling  increases  ex- 
ponentially with  increasing  R,  but  the  en- 
ergetic cost  of  remodeling  is  hypothesized 
to  remain  constant,  midshafts  of  more 
proximal  elements  are  predicted  to  re- 
spond to  applied  forces  with  proportion- 
ately higher  modeling  rates  than  midshafts 
of  more  distal  elements.  In  contrast,  mid- 
shafts of  more  distal  elements  are  predict- 
ed to  respond  to  applied  forces  with  pro- 
portionately higher  Haversian  remodeling 
rates  than  midshafts  of  more  proximal  el- 
ements. 

Although  Lieberman  and  Croinpton 
(1998)  provided  preliminary  data  in  sup- 
port of  the  trade-off  model,  their  sample 
size  was  small  and  their  analysis  did  not 
include  kinematic  or  kinetic  data.  This 
study  tests  the  model  more  completely  by 
comparing  the  cross-sectional  geometry 
and  histology  of  the  midshaft  femur,  tibia, 
and  metatarsal  in  a  larger  sample  of  exer- 
cised and  sedentary  control  subjects.  Two 


specific  hypotheses  are  tested  with  kine- 
matic, kinetic,  and  morphometric  data. 
First,  osteogenic  responses  to  strains  are 
predicted  to  vary  according  to  loading  and 
to  position  within  the  skeleton.  In  partic- 
ular, higher  rates  of  both  modeling  and 
Haversian  remodeling  are  predicted  to  oc- 
cur at  homotypic  sites  in  exercised  animals 
than  in  matched  controls.  Second,  a  trade- 
off is  predicted  between  modeling  and 
Haversian  remodeling  responses,  with  pro- 
portionately higher  Haversian  remodeling 
rates  at  distal  than  at  proximal  midshafts, 
and  proportionately  higher  modeling  rates 
at  proximal  than  at  distal  midshafts  (stan- 
dardized by  body  mass  and  element 
length).  Forthcoming  publications  will 
present  data  on  variations  in  peak  strains 
at  distal  and  proximal  midshafts,  and  dif- 
ferences in  trade-off  responses  between 
juvenile,  subadult,  and  adult  subjects. 

MATERIALS  AND  METHODS 

Subjects  and  Exercise  Training 

Eleven  juvenile  rams  (Ovis  aries;  Dor- 
set) were  divided  into  control  (n  =  5)  and 
exercise  (n  =  6)  groups.  One  animal  in  the 
exercise  group  (lamb  10)  had  a  respiratory 
infection  for  4  weeks  and  was  excluded 
froin  all  calculations  because  it  gained  al- 
most no  weight  during  that  period.  Sub- 
jects were  40  days  old  at  the  start  of  the 
experiment,  which  lasted  89  days.  For  1 
week  before  the  start  of  the  experiment, 
the  exercise  group  animals  were  habituat- 
ed to  run  in  an  enclosed  box  on  a  Mar- 
quette 1800  treadmill  (GE  Medical  Sys- 
tems, Milwaukee,  WI).  Exercise  group  an- 
imals ran  every  day  at  a  horizontal  incli- 
nation for  60  minutes  at  a  Froude  speed 
of  0.5  (approximately  4  km/h),  generating 
approximately  6,000  loading  cycles  per  da) 
per  limb.  At  this  speed,  which  is  well  be- 
low maximum  running  speed,  the  sheep's 
gait  is  a  slow  trot.  Subjects  were  housed  in 
raised  1.0-m-  cages,  limiting  additional 
loading  to  minor  locoinotor  activity  and 
sedentary  weight  support.  All  subjects 
were  fed  the  saine  quantity  of  hay  per  day 


Trade-Off  Responses  to  Loading  in  the  Mammalian  Limb  •  Liebennan  and  Pearson        273 


•a 
o 

2 


Radius  of  Gyration 

Proximal  '        Distal 


Radius  of  Gyration 

Proximal  '         Distal 


Figure  2.  Predicted  trade-off  between  periosteal  growth 
(modeling)  and  Haversian  remodeling  (repair)  rates  in  cortical 
bone  as  a  function  of  the  radius  of  gyration. 


and  water  ad  libitum.  Fluorescent  dyes 
that  incorporate  into  bone  mineral  were 
administered  by  intraperitoneal  injection 
at  the  start  of  the  experiment  (calcein,  20 
mg/kg),  on  day  30  (oxytetracyline,  50  mg/ 
kg),  and  on  day  63  (xylenol  orange,  25  mg/ 
kg).  Body  mass  was  measured  weekly.  At 
the  end  of  the  experiment,  total  limb 
length  from  the  greater  trochanter  of  the 
femur  to  the  ground  was  measured  for 
each  subject.  The  subjects  were  then  eu- 
thanized, and  their  limbs  bones  were  re- 
moved and  defleshed.  The  radii  of  gyration 
from  the  femoro-acetabular  joint  to  the 
midshaft  of  the  femur,  tibia,  and  metatar- 
sal were  measured  at  simulated  midstance 
using  a  plastic  tape  measure  (accurate  to  1 
mm)  on  each  animal  after  death.  Articular 
lengths  of  the  femur,  tibia,  and  metatarsal 
were  measured  using  digital  calipers  (ac- 
curate to  0.01  mm).  Femoral  length  was 
measured  from  the  most  proximal  point  on 
the  femoral  head  to  the  line  connecting 
the  two  distal  condyles.  Tibial  length  was 
measured  from  the  center  of  the  lateral 
condylar  surface  to  the  center  of  the  distal 
articular  surface.  Metatarsal  length  was 
measured  from  the  center  of  the  proximal 
articular  surface  to  the  most  distal  point  of 
the  distal  articular  surface. 

Cross-Sectional  Geometry  and  Histologic 
Analysis 

A  2-cm  section  was  cut  from  the  limb 
midshaft  of  each  left  femur,  tibia,  and 
metatarsal,  and  the  inarrow  was  removed. 


After  measuring  their  densities,  sections 
were  fixed  in  100%  ethanol,  and  then  si- 
multaneously stained  and  dehydrated  in  a 
solution  of  1%  basic  fuchsin  in  denatured 
ethanol  under  20  mm  Hg  vacuum.  Sample 
solution  was  changed  every  24  hours  for  1 
week.  Samples  were  then  embedded  in 
poly-methyl  methacrylate  polymer  (Osteo- 
bed®,  Polysciences  Inc,  Warrington, 
Pennsylvania).  Two  sections  were  cut  from 
each  embedded  midshaft  using  an  Iso- 
met®  1000  low-speed  saw  (Buehler  Ltd., 
Lake  Bluff,  Illinois),  affixed  to  glass  shdes 
with  Epotek®  301  epoxy  (Epoxy  Technol- 
ogy Inc.,  Billerica,  Massachusetts),  ground 
to  approximately  100  ixm  thick  using  a 
Hillquist®  1005  thin-section  machine 
(Hillquist  Inc,  Fall  City,  Washington),  pol- 
ished using  a  Hillquist®  900  grinder,  and 
cover-slipped. 

Cross-sections  were  analyzed  using  an 
Olympus®  SZH  10  stereozoom  micro- 
scope with  cross-polarized  light  and  a 
Highlight®  3000  Fluorescence  (Olympus 
America,  Mellville,  New  York).  Digitized 
images  were  captured  using  a  Pro- Series® 
CCD  technical  video  camera  (Media  Cy- 
bernetics, Silver  Spring,  Maryland)  con- 
nected to  a  Macintosh®  4440  computer 
wdth  a  Scion®  LG-3  capture  board  (Scion 
Corp.,  Frederick,  Maryland).  A  version  of 
NIH  Image,  v  1.61  (W.  Rasband,  National 
Institutes  of  Health)  with  a  macro  written 
by  M.  Warfel  (Cornell  University),  was 
used  to  calculate  cortical  area,  medullary 
area,  the  maximum  and  minimum  second 
moment  areas  (Z^^„  I„,J,  and  the  polar  mo- 
ment of  inertia  (/).  These  measurements 
were  averaged  for  the  two  sections  from 
each  inidshaft. 

Haversian  systems  were  counted  and 
measured  using  NIH  Image.  Only  com- 
plete secondary  osteons  with  reversal  lines 
were  counted.  Haversian  density  was  com- 
puted as  the  total  number  of  complete  sec- 
ondary osteons  divided  by  cortical  bone 
area.  Linear  periosteal  growth  was  mea- 
sured along  the  anterior,  posterior,  medial, 
and  lateral  axes  of  each  section  as  the  dis- 
tance from  the  line  of  the  calcein  dye  (ad- 


I 


274         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


ministered  on  day  1  of  the  experiment,  see 
above)  to  the  periosteal  surface.  Periosteal 
modeling  rate  (PMR)  was  calculated  as  the 
average  of  periosteal  growth  from  the  four 
axes  divided  by  the  number  of  days  in  the 
experiment.  Haversian  density  and  PMR 
were  averaged  for  the  two  sections  from 
each  midshaft. 

Kinematic  Analysis 

To  acquire  data  on  limb  element  ori- 
entation and  angular  velocity,  three  sub- 
jects were  recorded  at  the  end  of  the  ex- 
periment (after  surgery  in  which  strain 
gauges  were  attached  to  the  limbs;  strain 
data  are  reported  in  a  forthcoming  paper). 
The  subjects  were  videotaped  in  lateral 
view  using  a  SONY®  DCR  VX-1000  Han- 
dycam  (Sony  Corp.,  Tokyo,  Japan)  at  60 
fields/s.  Subjects  were  recorded  approxi- 
mately 4  and  24  hours  after  surgery,  and 
ran  with  a  normal  gait  (e.g.,  with  full 
weight-bearing  on  all  limbs  and  no  signs 
of  favoring  one  limb  over  another,  showing 
no  signs  of  lameness,  distress,  or  discom- 
fort). At  least  five  complete  gait  cycles 
were  digitized  for  each  animal  at  4.0  km/ 
h.  NIH  Image  was  used  to  measure  the 
orientation  of  the  longitudinal  axes  of  the 
femur,  tibia,  and  metatarsal  relative  to  the 
horizontal  plane  of  the  treadmill  in  each 
frame.  These  data  were  used  to  calculate 
angular  velocity  (w)  following  the  method 
of  Winter  (1990). 

Analysis 

All  cross-sectional  dimensions  were 
standardized  by  body  mass  (calculated  as 
mean  mass  during  the  final  3  weeks),  and 
second  moment  areas  were  standardized 
by  both  body  mass  and  element  length.  In 
order  to  evaluate  osteogenic  responses  to 
mechanical  loading  in  terms  of  kinetic  en- 
ergy costs,  the  area-normalized  inertial 
cost  (ANIC)  of  each  midshaft  cross-section 
(0  was  estimated  (following  Winter,  1990) 
in  joules  as 


ANIC  =  0.57,0)2 


where 


7,  =  7?,2.CAD 

in  which  co  is  the  angular  velocity  in  radi- 
ans, K,  is  the  radius  of  gyration  in  meters, 
CA  is  cortical  area  expressed  in  m-,  and  D 
is  bone  density  in  kg/m^.  Note  that  ANIC 
is  not  an  estimate  of  the  kinetic  energy 
cost  of  accelerating  the  limb  segment  as  a 
whole,  but  instead  estimates  the  kinetic 
energy  cost  of  accelerating  the  midshaft  of 
each  limb  segment. 

Because  of  the  small  sample  sizes,  and 
to  avoid  assuming  normal  distribution  of 
the  data,  all  tests  of  significance  between 
elements  and  between  groups  were  cal- 
culated using  nonparametric  methods  (in 
most  cases,  Wilcoxon  two-sample  test). 

RESULTS 

Cross-Sectional  Geometry 

Cross-sectional  properties  of  the  femur, 
tibia,  and  metatarsal  in  the  exercised  and 
control  sheep  are  summarized  in  Table  1, 
along  with  data  on  body  mass  and  element 
length  at  the  end  of  the  experiment  used 
to  standardize  comparisons.  Little  differ- 
ence in  element  length  and  body  mass 
(less  than  1%  in  all  cases)  was  found  be- 
tween exercise  and  control  groups.  No  sig- 
nificant effects  were  found  of  exercise  on 
overall  cross-sectional  area  and  shape: 
mass-adjusted  medullary  area  (MA),  CA, 
and  midshaft  shape  as  measured  by  7^^ 
7„,in  did  not  differ  significantly  between 
groups;  CA/kg  in  the  tibia  was  nearly  sig- 
nificant at  the  a  =  0.05  level  (F  =  0.08). 
The  value  of  7  differed  significantly  be- 
tween exercise  and  control  groups  in  cer- 
tain elements:  distal  elements  had  abso- 
lutely smaller  and  weaker  midshafts  than 
the  femur,  and  the  difference  in  7  between 
exercise  and  control  groups  was  more  pro- 
nounced in  the  tibia  and  metatarsal  than 
it  was  in  the  femur.  When  standardized  for 
element  length  and  body  mass,  7,,,.^^,  7„,i,„ 
and/  were  25—29%  higher  in  the  exercised 
than  in  control  groups  in  the  tibia  (P  < 
0.05);  20%  higher  in  the  metatarsal  (P  = 
0.05-0.08);  and  13-16%  higher  in  the  fe- 
mur (P  =  0.17-0.25). 


I! 


Trade-Off  Responses  to  Loading  in  the  Mammalian  Limb  •  Lieberman  and  Pearson        275 


Table  1.     Standardized  cross-sectional  properties. 


\'ar 

able" 

Controls 

Exercised 

%  Difference  t 

n 

Mean 

-t- 

1  SD 

n 

Mean  ± 

1  so 

P  (Wilcoxon) 

Body  mass 

(kg)l 

5 

38.56 

-1- 

3.50 

5 

38.82  ± 

2.20 

0.7 

0.60 

Femur 

Articular 

length  (mm) 

5 

174.3 

+ 

6.8 

5 

174.8  ± 

3.0 

0.3 

0.60 

MA/kg 

5 

2.77 

+ 

0.79 

5 

2.73  ± 

0.79 

-1.3 

0.92 

CA/kg 

5 

3.45 

-H 

0.42 

5 

3.57  ± 

0.21 

3.5 

0.75 

^„,.ykg-L 

5 

0.57 

-H 

0.09 

5 

0.66  ± 

0.08 

16.2 

0.25 

/..ykg.L 

5 

0.43 

+ 

0.07 

5 

0.49  ± 

0.05 

12.5 

0.25 

*-  max  *  min 

5 

1.31 

+ 

0.09 

5 

1.35  ± 

0.06 

3.1 

0.35 

;/kg-L 

5 

0.99 

+ 

0.16 

5 

1.15  ± 

0.12 

14.6 

0.17 

nbia 

Articular  length  (mm) 

5 

194.3 

-+- 

7.6 

5 

193.7  ± 

3.9 

-0.3 

0.92 

MA/kg 

5 

0.94 

-+- 

0.3215 

5 

1.05  ± 

0.1224 

11.8 

0.60 

CA/kg 

5 

3.17 

■+■ 

0.2474 

5 

3.55  ± 

0.3204 

11.9 

0.08 

/...Ag-L 

5 

0.29 

■+■ 

0.0376 

5 

0.38  ± 

0.0529 

29.3 

0.03 

/,„.„/kg-L 

5 

0.22 

-\- 

0.0258 

5 

0.27  ± 

0.0387 

24.9 

0.03 

■*  ina.v  ■*  min 

5 

1.36 

■+■ 

0.0575 

5 

1.41  ± 

0.1029 

3.7 

0.60 

;/kg.L 

5 

0.51 

■+■ 

0.0625 

5 

0.65  ± 

0.0889 

27.4 

0.03 

Metatarsal 

Articular 

length  (mm) 

5 

135.1 

■+■ 

4.5 

5 

135.8  ± 

3.0 

0.5 

0.75 

MA/kg 

5 

0.87 

-+- 

0.3030 

5 

1.01  ± 

0.18 

15.4 

0.46 

CA/kg 

5 

2.50 

-+- 

0.2597 

5 

2.66  ± 

0.26 

6.0 

0.17 

/.a/kg-L 

5 

0.25 

-H 

0.0313 

5 

0.30  ± 

0.05 

20.7 

0.08 

/.iAg.L 

5 

0.22 

-H 

0.0287 

5 

0.27  ± 

0.04 

20.5 

0.05 

■*  ma.v  ■*  min 

5 

1.14 

+ 

0.0453 

5 

1.14  ± 

0.07 

0.2 

0.92 

//kg.L 

5 

0.47 

+ 

0.0593 

5 

0.57  ± 

0.09 

20.6 

0.08 

°  MA,  mass-adjusted  medullary  area;  CA,  cortical  area;  /,„„,  maximum  second  moment  area; 
ength;  7^,„„  minimum  second  moment  area;  J,  polar  moment  of  inertia. 
t  Calculated  as  [(exercised  group  mean  —  control  mean)/control  mean]  X  100. 
\  Average  of  the  last  3  weeks  of  body  mass. 


L,  articular 


[nergetic  Costs 

The  ANIC  of  each  inidshaft  cross-sec- 
don  is  useful  for  evaluating  osteogenic  re- 
sponses to  mechanical  loading  in  teriTis  of 

nergetic  costs  (see  above).  This  estiinate 
requires  data  on  cortical  area  (see  Table  1) 
as  well  as  D,  R,,  and  co  for  each  eleinent 
^suminarized  in  Table  2).  As  Table  2  in- 
dicates, no  significant  differences  existed 
in  D  between  runners  and  controls  for  any 
slements.  Peak  co  in  the  femur  was  consid- 

rably  lower  than  that  of  the  tibia  and 
metatarsal,  which  were  roughly  siinilar. 
Maxiinum  angular  excursion  was  approxi- 
mately 47°  for  the  femur,  68°  for  the  tibia, 
and  62°  for  the  metatarsal;  these  ranges 
are  similar  to  those  of  other  midsized  un- 
gulates (e.g.,  cervids)  but  are  considerably 


greater  than  those  reported  for  larger  cur- 
sorially  specialized  mammals  such  as  hors- 
es (Gambaryan,  1974;  Biewener  et  al., 
1988).  The  above-described  differences  in 
CO,  combined  with  the  substantial  differ- 
ences in  CA  (see  Table  1)  and  R,  (Table  2) 
resulted  in  estimates  of  area  normalized 
inertial  cost  that  were  roughly  10  times 
higher  for  the  tibia  than  for  the  femur,  and 
roughly  twice  as  high  in  the  metatarsal  as 
in  the  tibia.  No  statistically  significant  dif- 
ferences in  ANIC  were  detected  between 
the  exercise  and  control  groups. 

Modeling  and  Haversian  Remodeling 

Table  3  summarizes  histologic  data  on 
average  periosteal  growth  rates  (PGR)  in 
|xm/d  for  the  femur,  tibia,  and  inetatarsal. 


276         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Table  2.     Kinematic  and  density  data  used  to  calculate  inertial  cost  of  midshaft  cross  sections 


Density  {kg/m') 

Angular  \'elocity  (w,  radiaus/s) 

Group 

Femur 

Tibia 

Metatarsal 

Femur 

Tibia                    Metatarsal 

Controls  (n  =  5) 
Exercised  (n  =  5) 

1,976  ±  66 
1,974  ±  104 

1,995  ±  83 
1,902  ±  119 

1,897  ±  152 
1,846  ±  186 

NAf 
6.89  ±  1.3 

NA                   NA 
12.6  ±  1.8      11.2  ±  0.7 

"  ANIC,  area-normalized  inertial  cost,  calculated  as  0.05CAdensity-R,^-a)^  using  average  value  of  w  for  the 
three  exercised  animals.  CA,  cortical  area;  K,,  radius  of  gyration  of  a  given  bone,  i. 
t  NA,  not  available. 


Analysis  of  these  data  indicated  that  PGR  trols  at  the  midshaft  of  the  femur,  tibia, 
is  significantly  higher  in  the  exercised  than  and  inetatarsal;  these  animals  also  had  sig- 
the  in  control  group  for  all  three  elements,  nificantly  higher  secondaiy  osteonal  den- 
In  addition,  although  PGR  for  the  femur  sities  than  controls  at  the  midshaft  of  the 
is  significantly  higher  (F  <  0.05)  than  for  tibia  and  metatarsal,  but  not  the  femur, 
the  tibia  in  both  groups,  PGR  is  signifi-  Therefore,  this  study  supports  the  findings  ■ 
cantly  higher  in  the  tibia  than  in  the  meta-  of  previous  studies  that  indicated  that 
tarsal  in  the  exercised  (P  =  0.02)  but  not  growth  (periosteal  modeling)  and  repair 
in  the  controls  {P  =  0.31),  largely  because  (Haversian  remodeling)  in  cortical  bone 
of  the  markedly  higher  tibial  PGR  in  the  occur  in  response  to  the  functional  strains 
exercised  versus  control  groups.  There-  generated  by  luechanical  loading  (e.g., 
fore,  modeling  in  response  to  exercise  oc-  Lanyon  et  al.,  1982;  Lanyon  and  Rubin, 
curs  more  rapidly  at  the  midshaft  in  prox-  1984;  Rubin  and  Lanyon,  1984a,b,  1985; 
imal  versus  distal  elements  of  the  limb  in  Burr  et  al.,  1985;  Biewener  et  al,  1986; 
proportion  to  the  kinetic  energy  cost  of  ac-  Raab  et  al,  1991;  Bouvier  and  Hylander, 
celerating  added  mass,  with  an  especially  1996).  However,  further  research  is  nec- 
pronounced  effect  on  the  tibial  midshaft,  essary  to  establish  the  nature  of  the  strain 
This  relationship  is  illustrated  in  Figure  signal  that  induces  these  responses  (e.g., 
3 A,  which  shows  that  midshaft  modeling  magnitude,  frequency),  and  the  extent  to 
rates  in  the  hind  limb  are  inversely  pro-  which  osteogenic  responses  to  mechanical 
portional  to  estimates  of  midshaft  ANIC.  loading  change  with  age.  These  results  ad- 
Analysis  of  data  on  Haversian  remodeling  ditionally  support  the  trade-off  model  for 
rates  in  Table  3  also  indicated  that  second-  growing  animals  of  Lieberman  and 
ary  osteon  density  is  higher  in  distal  than  Crompton  (1998).  Cortical  bone  growth 
in  proximal  midshafts,  with  more  pro-  and  repair  mechanisms  in  juvenile  sheep 
nounced  differences  between  exercised  vary  inversely  at  homotypic  sites  as  a  func- 
and  control  groups  in  distal  than  in  prox-  tion  of  the  kinetic  energy  cost  of  acceler- 
imal  midshafts.  Analysis  of  these  results  in-  ating  additional  mass.  In  particular,  mid- 
dicated  that  Haversian  remodeling  in  re-  shaft  periosteal  growth  rates  are  signifi- 
sponse  to  exercise  occurs  at  higher  levels  cantly  higher  in  proximal  than  in  distal  el- 
at  the  midshaft  in  distal  versus  proximal  ements  in  inverse  proportion  to  the 
elements  of  the  limb  in  proportion  to  es-  estimated  ANIC  of  accelerating  mass,  and 
timates  of  midshaft  ANIC,  as  shown  in  midshaft  Haversian  remodefing  rates  are 
l^igure  3B.  significantly  higher  in  distal  than  in  proxi- 
nicjpi  iQQinM  '^^^  elements  in  proportion  to  the  same 

energetic  cost. 
Growing  sheep  that  exercised  at  mod-  Optimization  of  modeling  and  remod- 
erate  levels  for  90  days  had  significantly  eling  responses  in  distal  and  proximal  el- 
higher  periosteal  modeling  rates  than  con-  ements  in  growing  animals  is  a  probable 


Trade-Off  Responses  to  Loading  in  the  Mammalian  Limb  •  Lieberman  and  Pearson        277 


Table  2.     Extended. 


Radius  of  g)'ration  (m) 

ANIC  (joules)" 

Femur 

Tibia 

Metatarsal 

F'emur 

Tibia 

Metatarsal 

0.09  ±  0.01 
0.09  ±  0.00 

0.20  ±  0.01 
0.20  ±  0.01 

0.33  ±  0.03 
0.33  ±  0.02 

0.05  ±  0.01 
0.05  ±  0.01 

0.20  ±  0.01 
0.19  ±  0.01 

0.33  ±  0.03 
0.32  ±  0.02 

adaptation  for  limb-bone  tapering  to  en- 
able distal  elements  to  remain  lighter  than 
proximal  elements,  thereby  reducing  the 
kinetic  energy  costs  of  locomotion  (Hil- 
debrand,  1985).  By  modulating  growth 
and  repair  responses  to  loading  between 
proximal  and  distal  elements,  aniixials  save 
kinetic  energy,  albeit  at  the  expense  of 
higher  metabolic  energy  costs  over  the 
long  term.  Currently,  no  data  exist  on  the 
metabolic  cost  of  Haversian  remodeling, 
but  this  cost  is  predicted  to  be  less  in  the 
long  term  than  the  kinetic  energy  cost  of 
accelerating  additional  distally  located 
mass  that  might  otherwise  be  necessary. 
One  important  limitation  of  the  trade-off 
model  tested  here  is  that  differential  mod- 
eling versus  Haversian  reinodeling  re- 
sponses to  inechanical  loading  may  not  oc- 
cur in  all  regions  of  the  skeleton  or  in  tra- 
becular bone,  and  are  likely  to  change  with 
age.  As  aniinals  inature,  periosteal  growth 
rates  in  response  to  a  given  strain  stiinulus 
decline,  although  endosteal  gro\vth  inay 
increase,  leading  to  stenosis  (Woo  et  al., 
1981;  Ruff  et  al,  1994),  and  Haversian  re- 


modeling rates  probably  increase  regard- 
less of  skeletal  location.  These  hypothe- 
sized effects  can  be  tested  by  comparing 
the  above  results  with  modeling  and  re- 
modeling responses  in  adult  sheep  sub- 
jected to  the  same  mechanical  loads. 

The  variable  responses  to  mechanical 
loading  documented  here  suggest  that  any 
relationships  between  loading  and  bone 
cross-sectional  dimensions  are  more  com- 
plex than  is  sometimes  assumed.  In  partic- 
ular, the  higher  periosteal  growth  rates  of 
the  exercised  juvenile  sheep  influenced 
overall  midshaft  I  more  than  cortical  or 
medullary  areas  (see  Table  1),  providing 
experimental  support  for  coinparative 
studies  that  indicate  tliat  /  and  not  cortical 
areas  should  be  used  to  estimate  biome- 
chanical  adaptations  from  bone  cross  sec- 
tions (Jungers  and  Minns,  1979;  Ruff  and 
Hayes,  1983;  Ruff,  1989;  Ruff  and  Runes- 
tad,  1992;  Lieberman,  1997).  In  addition, 
proximodistal  differences  in  modeling  ver- 
sus Haversian  remodeling  rates  suggest 
tliat  inferences  about  biomechanical  ad- 
aptations to  loading  from  cross-sectional 


Table  3.     Histologic  data. 


Element  or  variable 


Controls 

Exercised 

7c 
Difference" 

p 

11 

Mean  ±  1  SD 

n 

Mean  ±   1  SD 

(W'ilcoxon 

3 

11.03  ±  0.71 

5 

13.92  ±  1.59 

26.1 

<0.05 

4 

6.99  ±  0.72 

5 

11.04  ±  1.07 

58.0 

<0.05 

4 

6.43  ±  0.96 

5 

8.28  ±  1.14 

28.8 

<0.05 

5 

0.42  ±  0.45 

5 

0.51  ±  0.51 

21.4 

NS 

5 

2.34  ±  1.13 

5 

4.67  ±  2.79 

99.6 

<0.05 

5 

7.89  ±  2.26 

5 

16.31  ±  4.71 

206.7 

<0.05 

Femur:  average  growth  ratet  (jjuin/d) 
Tibia:  average  growth  ratet  (|xm/d) 
Metatarsal:  average  growth  ratef  (jjuni/d) 
Femur  osteon  densityl 
Tibia  osteon  density* 
Metatarsal  osteon  density! 


"  Calculated  as  [(exercised  group  mean  —  control  mean)/control  mean]  X  100. 

t  Average  growtli  rate  (periosteal  modeling  rate)  calculated  as  mean  growth  rate  (|jLm/d)  of  anterior,  pos- 
terior, medial,  and  lateral  cortices. 

I  Osteon  density  was  calculated  as  the  total  number  of  secondary  osteons  in  the  entire  section  divided  by 
the  cortical  area  (mm^). 


278         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


geometry  of  the  midshaft  may  be  less  re- 
hable  in  distal  elements,  especially  the 
metatarsal,  than  in  more  proximal  ele- 
ments. One  unexpected  result  from  this 
study  is  that  /  discriminates  better  be- 
tween exercise  and  control  groups  at  the 
tibial  midshaft  than  in  the  femur  or  meta- 
tarsal. The  greater  percent  difference  be- 
tween treatment  groups  in  the  tibia  than 
in  the  femur  or  metatarsal  may  be  a  func- 
tion of  different  local  muscle  forces,  dif- 
ferences in  element  orientation,  or  be- 
cause the  femur  has  a  higher  safety  factor 
than  more  distal  elements.  Bertram  and 
Biewener  (1992)  also  found  more  variation 
in  limb  bone  curvature  relative  to  body 
mass  in  the  femur  than  in  more  distal  el- 
ements among  a  wide  range  of  mammals, 
possibly  suggesting  that  the  femur  may  be 
relatively  stronger  and  therefore  experi- 
ences lower  strains  than  more  distal  ele- 
ments. This  hypothesis  needs  to  be  tested 
with  in  vivo  strain  data. 

Perhaps  the  most  important  problem 
raised  by  the  trade-off  between  modeling 
and  Haversian  remodeling  documented 
here  is  the  mechanism  by  which  bones 
modulate  proximodistal  differences  in  os- 
teogenic responses  to  mechanical  loading. 
Several  hypotheses  merit  further  study. 
First,  different  modeling  and  Haversian 
remodeling  responses  to  mechanical  load- 
ing may  be  a  function  of  differences  in 
strain  magnitude,  strain  polarity,  or  other 
aspects  of  strain  energy  histoiy.  Frost 
(1990)  and  Martin  and  Burr  (1989)  pro- 
posed that  remodeling  and  modeling  are 
mutually  exclusive  responses  below  or 
above  specific  strain  thresholds  (mininnum 
effective  strains).  However,  preliminary 
data  (to  be  presented  in  a  subsequent  pa- 
per) on  cross-sectional  strains  normal  to 
the  tibia  and  metatarsal  midshaft  in  the 
sheep  indicate  that  the  tibia  and  luetatarsal 
experience  either  similar  bending  strains, 
or  that  the  metatarsal  experiences  slightly 
more  bending  in  the  sagittal  plane  than 
the  tibia.  Another  hypothesis  is  that  Hav- 
ersian remodeling  rates  may  be  positively 
correlated  with  strain  magnitudes  or  strain 


energy  history.  Secondary  osteonal  bone  is 
not  as  strong  as  primary  osteonal  and  cir- 
cumlamellar  bone  (Currey,  1959;  Carter 
and  Hayes,  1977a;  Vincentelli  and  Grigo- 
rov,  1985),  so  any  differential  response  to 
elevated  strain  levels  might  actually  exag- 
gerate the  apparent  trade-off  between 
modeling  and  remodeling  in  proximal  ver- 
sus distal  bones.  However,  these  and  other 
hypotheses  can  only  be  evaluated  with  in 
vivo  strain  data  from  the  midshaft  of  the 
femur,  tibia,  and  metatarsal  in  conjunction 
with  histologic  data  on  growth  and  remod- 
eling rates. 

Another  possibility  is  that  variations  in 
vascular  or  cellular  density  may  modulate 
growth  versus  repair  responses  to  loading 
in  different  limb  elements.  Bone  vascular 
density  must  constrain  remodeling  re- 
sponses to  some  extent  because  bone  mor- 
phogenetic  units  require  arteries  to  supply 
nutrients  and  cells  (Winet  et  al.,  1990; 
Singh  et  al.,  1991).  Avascular  cortical  bone 
tissue  is  rarely  if  ever  reconstructed  by  os- 
teoclasts (de  Ricqles  et  al.,  1991),  and  thus 
has  little  potential  to  respond  to  loading 
through  Haversian  remodeling.  Moreover, 
the  vascular  density  of  bone  may  be  partly 
rate-dependent  (de  Ricqles,  1975),  possi- 
bly explaining  the  correlation  between  re- 
modeling rates  and  vascular  density 
(Green  et  al.,  1987).  Further  research  is 
needed  to  test  if  a  correlation  exists  be- 
tween the  density  of  vascular  channels  in 
the  primary  cortex  of  the  femur,  tibia,  and 
metatarsal  and  Haversian  remodeling 
rates.  An  additional  possibility  is  that  os- 
teocytes  act  as  strain  transducers  (Lanyon, 
1993;  Turner  et  al.,  1994,  1995),  poten- 
tially limiting  Haversian  remodeling  re- 
sponses in  primary  compact  bone  in  pro- 
portion to  their  density.  Osteocytes  possi- 
bly play  a  role  in  sensing  and  transducing 
information  on  strains  and/or  microcracks 
to  precursor  stem  and  mesenchymal  cells 
(Lanyon,  1993),  which  may  limit  the  ability 
of  acellular  cortical  bone  to  undergo  Hav- 
ersian remodeling.  Differences  in  osteo- 
cyte  density  have  been  implicated  as  a  pos- 
sible  contributing   factor  to   osteoporosis 


Trade-Off  Responses  to  Loading  in  the  Mammalian  I^imb  *  Liebemmn  and  Pearson        279 


A 


18 


FEMUR 


TIBIA 


METATARSAL 


Midshaft  Area  Normalized  Inertial  Cost  (joules  *10    ) 


B 


20- 


t;5    15- 


CN 


i   10 

Q 

B 

>^ 

t/5 

C 
at 


(L) 

X 


5- 


0- 


'■               I 

/m) 

;                  ( 

y ^FTATARSAT 

TIBIA      // 

>^ 

FEMUR 

'                1                ' 

'                   1 

.0 


.5 


1.0 


1.5 


Midshaft  Area  Normalized  Inertial  Cost  (joules  *10    ) 


Figure  3.  Observed  trade-off  between  modeling  (A)  and  Haversian  remodeling  (B)  in  the  hindlimb  as  a  function  of  area-nor- 
malized inertial  cost  of  accelerating  mass  at  the  midshaft  of  the  femur,  tibia,  and  metatarsal.  Density  ellipses  are  plotted  for  10% 
(shaded)  and  65%  (unshaded)  within-group  variation  for  exercised  (solid  line)  and  control  (dashed  line)  groups. 


(Mullender  et  al.,  1996),  but  these  remain 
to  be  tested  in  the  sample  here. 

The  observed  trade-off  between  mod- 
ehng  and  remodehng  in  cortical  bone  sug- 
gests that  a  more  complete  understanding 
of  WolfPs  law  will  require  integration  of 
both  intraindividual  as  well  as  interindivid- 


ual  variations  in  the  mechanisins  by  which 
bones  respond  dvnamically  to  their  func- 
tional environment.  In  particular,  further 
research  needs  to  address  the  effects  of 
age,  variations  in  strain  levels,  and  the  in- 
terinediary  factors  that  modulate  the  ap- 
parent trade-off  between  growth  and  re- 


280         Bulletin  Museum  of  Comparative  Zoologij,  Vol.  156,  No.  1 


pair  processes  that  occurs  between  proxi- 
mal and  distal  elements  in  the  limb  and 
presumably  elsewhere  in  the  skeleton. 

ACKNOWLEDGMENTS 

Thank  you.  Fuzz,  for  inspiring  the  se- 
nior author's  interest  in  experimental  skel- 
etal biology  and  functional  morphology, 
and  for  many  years  of  training,  support, 
and  humorous  encouragement.  We  also 
thank  Andy  Biewener,  Brigitte  Demes, 
Brian  Richmond,  and  Bernard  Wood  for 
comments  on  the  manuscript;  Robin  Bern- 
stein for  helping  to  make  the  thin  sections; 
and  Mike  Toscano  for  running  the  sheep. 
This  research  was  supported  by  National 
Science  Foundation  IBN  96-03833  and  by 
funding  from  the  American  Federation  for 
Aging  Research. 

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MUSCLE  FORCE  AND  STRESS  DURING  RUNNING  IN  DOGS  AND 
WILD  TURKEYS 


THOMAS  J.  ROBERTS^ 

Abstract.  The  function  of  the  avian  hind  limb  dur- 
ing running  has  received  considerable  attention,  par- 
ticularly as  a  potential  analog  for  locomotor  function 
in  extinct  bipeds.  Comparisons  of  limb  kinematics  in 
avian  rrmners  and  mammalian  quadrupeds  have  re- 
vealed consistent  differences  in  the  pattern  of  joint 
excursions,  presumably  related  to  the  constraints  of 
bipedal  support  in  birds.  The  present  study  asks 
whether  these  kinematic  differences  are  paralleled  by 
differences  in  muscle  forces  and  stresses  developed 
in  hind  limb  locomotor  muscles  in  birds  and  quadru- 
pedal mammals.  High-speed  video  and  force-plate 
analyses  along  with  anatomical  measurements  were 
used  to  estimate  muscle  forces  and  stresses  in  the 
locomotor  muscles  of  small  dogs  and  wild  turkeys 
during  running.  Turkeys  and  dogs  developed  remark- 
ably similar  patterns  of  force  in  hind  limb  muscles, 
despite  large  differences  in  the  magnitude  of  ground 
reaction  force  moments.  It  was  expected  that  differ- 
ences in  absolute  muscle  force  in  hind  limb  muscles 
would  be  matched  by  differences  in  cross-sectional 
area  of  muscle  available  to  produce  force,  to  maintain 
similar  muscle  stress.  Instead,  muscle  stresses  varied 
widely  between  homologous  joints  in  dogs  and  tur- 
keys, and  between  joints  within  species.  The  distri- 
bution of  muscle  stress  between  joints  may  reflect 
differences  in  the  design  of  the  avian  and  mammalian 
limb  for  high -power  locomotor  activities. 

INTRODUCTION 

Avian  and  inainmalian  runners  move 
their  limbs  in  very  different  ways.  Mam- 
malian runners  and  most  quadrLipeds  re- 
tract their  hind  limbs  during  stance  phase 
primarily  by  a  large  extension  of  the  femur 
at  the  hip;  the  knee  flexes  and  extends  over 
only  a  small  angle  (Goslow  et  al.,  1981). 
Hip  extension  in  birds  is  negligible  at  low 
speeds  and  increases  with  running  speed 
(Gatesy,  1999a).  At  all  speeds,  the  knee 
undergoes  substantial  flexion  in  birds  and 


^  Oregon  State  University,  Department  of  Zoology, 
3029  Cordley  Hall,  Corvallis,  Oregon  97331-2914. 


accounts  for  a  greater  angle  change  than 
the  hip,  providing  inost  of  the  inovement 
for  retraction  of  the  limb  (Storer,  1971;  Ja- 
cobson  and  Hollyday,  1982;  Gatesy, 
1999a).  The  suggestion  has  been  inade 
that  these  differences  in  limb  moveiTient 
patterns  are  necessitated  by  the  constraints 
of  balance  in  bipedal  birds  (Storer,  1971; 
Gatesy,  1990).  The  horizontally  oriented 
femur  of  birds  positions  the  foot  beneath 
the  center  of  mass  for  standing  and  slow 
movement.  The  result  is  that  the  restricted 
inovement  of  the  avian  femur  leaves  the 
knee  to  act,  at  least  kineinatically,  as  the 
functional  equivalent  of  the  mammalian 
hip  (Gatesy  and  Biewener,  1991). 

It  is  unclear  how  these  kinematic  differ- 
ences, or  the  requirements  of  balance  in  a 
biped,  are  reflected  in  the  pattern  of  force 
development  in  locomotor  inuscles.  Be- 
cause muscle  forces  are  critical  to  the  en- 
ergetics of  running  and  the  mechanical 
stresses  on  muscles,  tendons,  and  bones, 
the  most  important  consequence  of  varia- 
tion in  limb  morphology  may  be  variation 
in  timing  and  magnitude  of  muscle  forces 
(Biewener,  1989;  Kram  and  Taylor,  1990; 
Roberts  et  al.,  1998).  It  has  recently  been 
shown  that  dogs  and  wild  turkeys  produce 
similar  total  muscle  forces  per  unit  ground 
reaction  force  (GRF)  during  running 
(Roberts  et  al.,  1998).  The  present  study 
addresses  two  questions  about  the  design 
of  the  avian  and  mainmalian  hind  limb  for 
locomotor  force  production:  is  the  timing 
of  flexor  and  extensor  forces  the  same  at 
homologous  joints  in  dogs  and  turkeys, 
and  are  the  stresses  developed  in  the  lo- 


Bull.  Mus.  Comp.  Zool.,  156(1):  283-295,  October,  2001         283 


284         Btilletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


comotor  muscles  equivalent  at  equivalent  tional  area  of  muscle  to  maintain  similar 

speeds?  stress.  The  similar  stress  hypothesis  is  sup- 

The  muscle  forces  required  to  balance  ported  by  the  observation  that  kangaroo 
gravitational  and  inertial  forces  during  rats  and  white  rats  maintain  the  same  level 
running  are  determined  primarily  by  the  of  peak  stress  in  their  ankle  extensors,  de- 
mechanical  advantage  for  force  production  spite  a  fourfold  difference  in  peak  GRF 
against  the  ground.  The  mechanical  advan-  per  limb  (Perry  et  al.,  1988). 
tage  at  any  given  joint  can  change  signifi-  In  the  present  study,  GRF-based  joint 
cantly  during  the  stance  phase,  as  the  po-  moments  are  measured  in  dogs  and  tur- 
sition  of  the  GRF,  and  its  leverage,  chang-  keys  running  over  a  force  plate.  These  data 
es  with  respect  to  the  joint  (Biewener,  are  combined  with  anatomical  data  to  cal- 
1989;  Carrier  et  al.,  1998).  These  changes  culate  the  required  muscle  forces  and  the 
in  muscle  mechanical  advantage  mean  that  total  stress  in  major  locomotor  muscles  at 
the  timing  of  the  maximum  muscle  force  homologous  joints  in  dogs  and  turkeys, 
may  be  independent  of  the  timing  of  the  Higher  hind  limb  muscle  forces  are  to  be 
GRF.  Forces  at  all  joints  must  be  carefully  expected  in  turkeys  compared  with  dogs 
coordinated  during  running  to  maintain  because  they  support  their  weight  on  two 
balance.  Presumably,  the  significant  differ-  limbs  rather  than  four.  To  maintain  similar 
ences  in  limb  posture  and  running  kine-  stress,  turkeys  should  have  a  greater  cross- 
matics  in  bipedal  birds  and  quadrupeds  sectional  area  of  hind  limb  muscle  in  pro- 
might  be  associated  with  distinct  differ-  portion  to  higher  absolute  muscle  forces, 
ences  in  the  timing  and  coordination  of 
joint  moments  and  muscle  forces.  MATERIALS  AND  METHODS 

One  possible  morphologic  indicator  of  Animals 
the  forces  that  are  developed  during  lo- 
comotion is  the  cross-sectional  area  of  ex-  Three  small  terriers  (Canis  famiUaris) 
tensor  muscles  at  a  joint.  The  range  of  pos-  and  three  wild  turkeys  (Meleagris  gallo- 
sible  joint  forces  is  limited  by  the  total  V^^o)  were  used  in  these  studies.  These 
cross-sectional  area  of  muscle  available  species  were  chosen  because  they  were 
and  the  maximum  stress  that  can  be  de-  approximately  the  same  body  mass,  4.5  ± 
veloped  by  verirebrate  skeletal  muscle.  It  l^  kg  and  5.3  ±  2.3  kg  for  the  dogs  and 
has  been  hypothesized  that  locomotor  turkeys,  respectively.  The  methods  for  an- 
muscles  should  undergo  the  same  peak  mial  training  and  the  data  collection  meth- 
stresses  during  equivalent  movements  in  ods  for  dogs  and  turkeys  have  been  de- 
terrestrial  runners  (Peny  et  al.,  1988).  This  scribed  in  detail  previously  (Roberts  et  al., 
hypothesis  is  based  upon  the  idea  that  the  1998),  and  will  be  presented  only  briefly 
muscular  system,  like  the  skeletal  system,  here. 

should  be   neither  over-   nor  underbuilt,  ,,       ,     r-          >< 
u  ^.     4.U     4_u  4-  j-u             ■4_  r     r        „  Muscle  ForcG  Measurements 
but  rattier  tliat  the  capacity  tor  torce  gen- 
eration should  be  matched  to  the  demand  High-speed  video  and  force-plate  mea 


(Biewener,  1990).  Because  the  maximum  surements  were  made  as  animals  ran  freely 
stress  that  can  be  developed  is  a  nearly  in-  over  a  15-m  track.  Measurements  were 
variant  property  of  skeletal  muscle,  the  made  at  the  speeds  that  were  initially  free- 
equivalent  stress  hypothesis  states  that  a  ly  chosen  by  the  animals,  approximately 
similar  fraction  of  the  capacity  for  force  3.5  m/s  for  the  turkeys  and  2.0  m/s  for  the 
production  in  the  extensors  of  a  joint  dogs.  Joint  moments  of  force  were  calcu- 
should  be  used  at  equivalent  speeds.  Thus,  lated  from  the  magnitude  and  position  of 
any  differences  in  force  requirements  at  a  the  GRF  vector  relative  to  the  joint  cen- 
joint  in  different  species  will  be  matched  ters  of  rotation  as  determined  by  force- 
by  a  proportional  difference  in  cross-sec-  plate  and  high-speed  video  analysis  (Rob- 


Muscle  Stress  During  Running  *  Roberts        285 


erts  et  al.,  1998).  Moments  were  deter- 
mined for  the  hip,  knee,  and  ankle  (dog 
and  turkey),  as  well  as  the  shoulder,  elbow, 
and  wrist  (dogs  only).  Measurements  in- 
cluded only  the  GRF-based  moments. 
Moments  due  to  accelerations  of  limb  seg- 
ments relative  to  the  center  of  mass  also 
contribute  to  the  required  muscle  force. 
Limb  inertia— based  moments  are  usually 
small  in  birds  and  quadrupedal  mammals 
(Clark  and  Alexander,  1975;  Pandy  et  al., 
1988),  but  may  be  significant  at  more  prox- 
imal joints.  Muscle  forces  (F,„)  were  cal- 
culated from  the  measured  joint  moments 
and  the  average  muscle  moment  arm  mea- 
sured at  each  joint: 


R 


(1) 


where  the  joint  moment  is  the  product  of 
GRF  magnitude  F,  (N)  and  moment  arm 
R  (m),  and  f  (m)  is  the  average  muscle 
moment  arm  at  that  joint. 

Calculation  of  muscle  force  and  stress 
requires  anatomical  measurements  of 
muscle  moment  arms  and  cross-sectional 
areas  for  muscles  active  during  support. 
The  average  moment  arm  (f)  was  calcu- 
lated for  the  extensor  muscles  at  a  joint 
from  an  average  weighted  by  the  cross- 
sectional  area  of  each  individual  muscle 
(Roberts  et  al.,  1998).  This  measure  as- 
sumed that  the  relative  contribution  of  a 
given  muscle  to  the  total  force  produced 
at  a  joint  was  proportional  to  the  muscle  s 
force-generating  capacity.  Muscle  physio- 
logic cross-sectional  area  (A„)  was  calcu- 
lated as: 


A„  — 


m-cos  6 


(2) 


where  m  is  the  mass  of  the  muscle  (g),  6 
is  the  fiber  pinnation  angle,  p  is  the  density 
of  muscle  (g/cm^)  ,  and  €  is  muscle  fascicle 
length  (cm). 

Measurements  were  included  for  mus- 
cles that  are  primarily  extensors  of  the 
joint  (or  flexors  in  the  case  of  the  wrist), 
and  are  active  during  stance  phase  based 


on  electromyographic  activity  (Tokurild, 
1973;  Goslow  et  al.,  1981;  Gatesy,  1999b). 
Muscles  included  for  turkeys  were  ilioti- 
bialis  lateralis  pars  postacetabularis,  iliofi- 
bularis,  flexor  cruris  lateralis,  flexor  cruris 
medialis,  puboischiofemoralis,  and  ischio- 
femoralis  (hip  extensors);  femorotibiales 
(knee  extensors);  and  gastrocnemius,  fi- 
bularis  longus,  flexor  hallucis  longus,  flexor 
digitorum  longus,  flexor  perforatus  digiti  II 
and  III,  and  flexor  perforans  et  perforatus 
digiti  II,  III,  and  IV  (ankle  extensors). 
Muscles  included  for  dogs  were  gluteus 
medius,  gluteus  superficialis,  biceps  fe- 
moris,  and  semimembranosus  (hip  exten- 
sors); vastus  lateralis,  medialis,  and  inter- 
medins (knee  extensors);  gastrocnemius, 
plantaris,  and  deep  digital  flexors  (ankle 
extensors);  supraspinatus  (shoulder  exten- 
sor); triceps  brachii  (elbow  extensor);  and 
flexor  digitorum  profundus,  flexor  digito- 
rum superficialis,  flexor  carpi  ulnaris,  and 
flexor  carpi  radialis  (wrist  flexors).  Some  of 
the  anatomical  measurements  were  taken 
from  specimens  available  from  unrelated 
experiments.  These  animals  were  of  simi- 
lar weight  and  condition.  Small  corrections 
to  the  muscle  dimension  measurements 
were  made  for  differences  in  the  body 
mass  of  the  experimental  subjects  by  as- 
suming geometric  scaling  (Roberts  et  al., 
1998). 

Contribution  of  Biarticular  Muscles  to 
Extensor  Muscle  Forces 

In  addition  to  the  muscle  forces  re- 
quired to  overcome  GRF  based  moments, 
extensor  muscles  must  produce  force  to 
balance  antagonist  flexor  muscle  forces. 
Cocontraction  of  muscles  that  are  primar- 
ily joint  flexors  was  assumed  to  be  negli- 
gible during  stance.  However,  many  biar- 
ticular (or  multiarticular)  extensor  muscles 
also  act  as  flexors.  The  flexor  forces  pro- 
duced by  biarticular  extensor  muscles  ac- 
tive during  stance  were  included  as  part  of 
the  calculation  of  total  muscle  force  re- 
quired at  a  joint.  Thus,  part  of  the  calcu- 
lated extensor  moment  at  several  joints  in- 
cludes a  component  of  force  necessary  to 


286         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


counteract  cocontraction  of  multiarticular 
muscles.  The  contribution  of  a  biarticular 
muscle  to  a  joint  flexor  moment  was  cal- 
culated from  the  extensor  force  it  devel- 
oped at  its  extensor  articulation,  assuming 
that  force  was  distributed  among  extensor 
muscles  in  proportion  to  their  cross-sec- 
tional area.  The  flexor  moment  was  then 
calculated  from  the  force  produced  in  the 
biarticular  muscle  and  its  flexor  moment 
arm. 

Flexor  forces  in  dogs  included  gastroc- 
nemius flexion  of  the  knee  and  flexion  of 
the  shoulder  by  the  long  head  of  triceps 
brachii.  In  turkeys,  extensor  muscle  forces 
were  required  to  balance  flexor  moments 
produced  at  the  knee  by  the  hip  extensors 
flexor  cruris  lateralis  and  medialis,  and  il- 
iofibularis.  The  following  ankle  extensors 
also  produced  a  flexor  moment  at  the  knee 
in  turkeys:  gastrocnemius  lateralis  and  me- 
dialis, and  the  digital  flexors  flexor  hallucis 
longus,  flexor  perforatus  digiti  II,  III,  and 
IV,  and  flexor  perforans  et  perforatus  digiti 
II  and  III.  Mulitiarticular  muscles  also  act- 
ed to  reduce  extensor  forces  in  two  cases. 
Some  of  the  digital  flexors  that  contribute 
to  flexion  of  the  wrist  also  act  to  extend 
the  elbow  in  dogs  (flexor  digitorum  pro- 
fundus, flexor  digitorum  superficialis,  flex- 
or carpi  radialis,  and  flexor  carpi  ulnaris). 
In  turkeys,  iliotibialis  lateralis  pars  posta- 
cetabularis  was  included  primarily  as  a  hip 
extensor  but  it  also  contributes  an  extensor 
moment  at  the  knee. 

The  presence  of  inultiple  biarticular 
muscles  that  both  flex  and  extend  the  knee 
and  the  hip  makes  calculation  of  muscle 
forces  an  indeterminate  problem,  because 
it  is  impossible  to  know  the  degree  of  co- 
contraction  of  antagonist  muscle  groups 
(Winter,  1990).  This  problem  was  avoided 
in  the  present  study  by  omitting  the  con- 
tribution of  the  rectus  feinoris  to  knee  ex- 
tension and  hip  flexion  in  dogs.  Electro- 
myographic studies  suggest  that  this  mus- 
cle is  active  during  the  second  two  thirds 
of  stance  phase  in  trotting  dogs  (Tokuriki, 
1973).  Rectus  femoris  is  approximately 
35%  of  the  total  cross-sectional  area  of  the 


extensor  muscles  at  the  knee;  omission  of 
this  muscle  may  lead  to  an  underestimate 
of  hip  extensor  forces  late  in  stance  and  a 
small  overestimate  of  knee  inuscle  stress 
in  dogs. 

Muscle  Stress  Measurements 

Muscle  stress  was  determined  by  divid- 
ing the  peak  measured  muscle  force  by  the 
total  physiologic  cross-sectional  area  of  ex- 
tensor muscles  at  a  joint.  This  measure  is 
equivalent  to  the  muscle  stress  in  each  in- 
dividual muscle  at  a  joint  only  if  the  force 
is  evenly  distributed  among  muscles  in 
proportion  to  each  muscle  s  cross-sectional 
area.  Although  this  assumption  has  proven 
accurate  for  hopping  kangaroo  rats  (Biew- 
ener  et  al.,  1988),  force  buckle  measure- 
ments in  cats  suggest  that  the  relative  con- 
tribution of  individual  ankle  extensors  to 
total  extensor  force  can  change  with  speed 
of  movement  and  locomotor  activity 
(Walmsley  et  al.,  1978).  Although  variation 
in  distribution  of  muscle  force  between 
muscles  may  make  it  difficult  to  calculate 
stresses  in  individual  muscles,  the  measure 
of  muscle  stress  of  a  whole  muscle  group 
will  still  reflect  the  fi'action  of  the  capacity 
for  force  production  that  is  being  used  in 
the  muscle  group. 

Statistical  Analyses 

To  calculate  an  average  force  versus 
time  plot  for  all  of  the  trials  it  was  neces- 
sary to  normalize  for  variation  in  both 
stride  time  and  total  force  between  indi- 
vidual trials.  Moment  and  force  measure- 
ments in  an  individual  trial  were  divided 
by  the  peak  GRF  for  that  trial.  To  control 
for  variation  in  ground  contact  time,  each 
original  stance  period  was  intei"polated  to 
a  wave  of  30  points  using  the  cubic  spline 
inteipolation  function  in  the  coinputer 
software  application  Igor  (Wavemetrics, 
Lake  Oswego,  OR).  The  interpolation  also 
applied  a  smoothing  function  to  the  data. 
Average  muscle  moment  and  force  curves 
are  represented  as  the  means  and  standard 
deviations  for  all  of  the  running  trials. 

Analysis  of  variance  was  used  to  test  for 


Muscle  Stress  During  Running  •  Roberts        287 


significant  differences  at  P  <  0.05.  Values 
presented  are  means  ±  one  standard  de- 
viation unless  indicated  othei-wise.  All  in- 
dicated differences  are  significant  at  F  < 
0.05. 

RESULTS 
Muscle  Forces 

Dogs  and  turkeys  produce  remarkably 
similar  patterns  of  force  at  homologous 
joints  in  the  hind  limb.  Figure  1  presents 
joint  moments  (FyR)  during  stance  phase 
normalized  to  the  peak  GRF  produced 
during  the  step.  Hip  moments  were  great- 
est early  in  stance  and  relatively  small  dur- 
ing the  second  half  of  stance  in  both  dogs 
and  turkeys.  Ankle  moments  were  also  at 
their  maximum  early  in  the  stance  phase. 
In  both  the  dog  and  the  turkey,  the  knee 
musculature  produced  a  net  flexor  mo- 
ment early  in  stance,  followed  by  an  ex- 
tensor moment.  This  cyclic  flexor— extensor 
moment  pattern  also  occurred  at  the 
shoulder  of  the  dog.  The  highest  knee  mo- 
ments occurred  during  the  second  half  of 
stance  phase  in  both  dogs  and  turkeys.  The 
peak  GRF,  indicated  by  an  arrow,  occurs 
earlier  in  stance  in  the  turkey  hind  limb 
than  in  the  dog  hind  limb  or  forelimb. 

The  hind  limb  muscles  of  turkeys  pro- 
duce greater  joint  moments  per  unit  GRF 
compared  with  dogs  (Fig.  1).  Hip  mo- 
ments per  unit  GRF  were  3.1-fold  greater 
in  the  turkey  (turkey,  0.085  ±  0.013;  dog, 
0.027  ±  0.013),  knee  moments  were  great- 
er by  a  factor  of  2.4  (turkey,  0.034  ±  0.012; 
dog,  0.014  ±  0.004),  and  ankle  moments 
were  1.8-fold  greater  in  the  turkey  (turkey, 
0.082  ±  0.012;  dog,  0.046  ±  0.006).  These 
differences  suggest  that  the  turkey's  rela- 
tively horizontally  oriented  femur  and  long 
tibiotarsus  and  tarsometatarsus  result  in 
greater  GRF  moment  arms  (R)  at  the  hip, 
knee,  and  ankle. 

Despite  the  large  differences  observed 
in  muscle  moments  (Fig.  1),  muscle  forces 
produced  per  unit  GRF  were  similar  in 
the  knee  and  the  hip  in  dogs  and  turkeys 
(Fig.  2).  Muscle  forces  presented  in  Fig- 


ure 2  were  calculated  from  joint  moments 
by  dividing  by  the  average  muscle  moment 
arm  (P;  Equation  1),  and  including  mo- 
ments produced  by  biarticular  agonists  or 
antagonists.  This  similarity  in  muscle  forc- 
es at  the  knee  and  hip  indicates  that  mus- 
cle moment  arms  (r)  at  these  joints  are 
proportionately  larger  in  the  turkeys  to 
compensate  for  the  higher  moments  re- 
sulting from  differences  in  limb  posture. 
The  average  muscle  moment  arm  at  the 
ankle  was  similar  in  dogs  and  turkeys; 
muscle  forces  were  larger  in  turkeys,  as 
were  the  muscle  moments. 

The  contribution  of  biarticular  muscle 
agonists  and  antagonists  to  the  extensor 
muscle  forces  calculated  at  the  knee,  el- 
bow, and  shoulder  is  represented  in  Figure 
2  by  the  difference  between  the  total  cal- 
culated extensor  force  (bold  line)  and  the 
extensor  muscle  force  calculated  neglect- 
ing the  contribution  of  biarticular  muscles 
(dotted  line).  Interestingly,  flexor  forces 
produced  by  biarticular  muscles  seem  to 
provide  the  flexor  moment  necessary  to 
balance  the  GRF  early  in  stance  at  the 
knee  and  shoulder.  Later  in  stance  the  ex- 
tensor force  necessary  is  increased  by  the 
action  of  two-joint  muscles,  assuming  that 
these  muscles  are  fully  active  throughout 
stance. 

Muscle  Stresses 

Muscle  stresses  were  quite  variable  be- 
tween joints  in  dogs  and  turkeys  (Fig.  3) 
rrmning  at  the  speeds  measured  in  this 
study.  The  values  presented  in  Figure  3 
were  obtained  by  dividing  the  peak  force 
produced  by  the  total  physiologic  cross- 
sectional  area  of  the  extensor  muscles  at  a 
joint.  Stress  varied  by  more  than  fivefold 
between  joints  in  dogs,  from  59  ±  28  kN/ 
m-  in  the  hip  extensors  to  309  ±  59  kN/ 
m-  in  the  shoulder  extensors.  Generally, 
hind  limb  stresses  were  lower  than  fore- 
limb  stresses,  and  stresses  were  higher 
moving  distally  in  the  dog  hind  limb.  Tur- 
keys showed  less  variation  in  muscle  stress 
between    joints    and    generally    operated 


288         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


B 

Z 


c 

g 
O 


0.10 


Turkey 


Dog 

hind  limb 

4 

m 

1        •        •        •        - 

Hip 

1, 

Dog  forelimb 


100  0 


100  0 


Stance  time  (%) 


Figure  1.  Muscle  moments  during  the  stance  phase  normalized  to  the  peak  ground  reaction  force  (GRF).  Mean  values  and 
standard  deviations  are  presented  for  12  strides  of  three  animals.  Positive  moments  represent  extensor  muscle  moments,  with 
the  exception  of  the  wrist;  wrist  flexor  muscle  moments  are  represented  as  positive.  Arrows  indicate  the  time  of  the  peak  GRF. 


with  higher  hind  limb  muscle  stresses  than 
did  dogs. 

Higher  muscle  stresses  at  a  joint  can  be 
due  to  either  higher  muscle  forces  or  a 
smaller  cross-sectional  area  of  muscle 
available.  Table  1  allows  a  comparison  of 
the  contribution  to  differences  in  muscle 
stress  of  muscle  mechanical  advantage,  the 
total  GRF  produced,  and  muscle  cross- 
sectional  area.  The  muscle  force  produced 
per  peak  GRF  is  determined  by  the  mus- 


cle mechanical  advantage,  and  is  signifi- 
cantly different  in  the  dog  and  turkey  only 
at  the  ankle.  The  peak  GRF  on  a  single 
hind  limb  in  turkeys  was  equal  to  2.4  X 
body  weight.  Dogs  developed  a  total  peak 
GRF  of  2  X  body  weight,  but  only  41%  of 
this  was  developed  by  the  hind  limbs; 
therefore,  the  dog  hind  limb  GRF  was  0.8 
X  body  weight.  When  this  difference  in 
hind  limb  GRF  is  included,  it  is  apparent 
that,  at  equivalent  speeds,  turkeys  produce 


Pi 

o 

(U 
Oh 


CO 


Turkey 


Muscle  Stress  During  Running  •  Roberts        289 


Dog  forelimb 


Dog  hind  limb 

Hip 

1. 

0 


Knee 


Knee 

^+^H+t±tm*H.,^ 

•  ■i'i..i..l..'rn 

1. 

100  0 


100  0 


Stance  time  (%) 


Figure  2.  Muscle  forces  during  tine  stance  phase  in  dogs  and  turkeys.  Muscle  force  values  are  normalized  to  the  peak  ground 
reaction  force  (GRF)  developed  during  the  stance  phase  to  give  a  dimensionless  ratio.  Solid  lines  represent  the  muscle  forces 
necessary  to  balance  the  GRF  moment  and  to  balance  flexor  moments  produced  by  two-joint  muscles.  Dotted  lines  indicate  the 
muscle  forces  required  to  balance  GRF  moments  only.  Arrows  indicate  the  time  of  peak  GRF.  Means  and  standard  deviations 
are  presented  for  12  runs  of  three  animals. 


much  higher  absolute  muscle  forces  at  all 
joints  than  do  dogs  (Table  1).  At  the  ankle, 
for  example,  turkeys  produced  muscle 
forces  equivalent  to  16.9  X  body  weight, 
whereas  dogs  produce  only  3  X  body 
weight  with  ankle  extensor  muscles.  At  the 
knee  and  the  hip,  the  differences  in  mus- 
cle cross-sectional  area  are  too  small  to 
compensate  for  the  large  differences  in 
force,    and    therefore    stresses    in    turkey 


muscles  are  much  higher.  However,  at  the 
ankle,  the  large  difference  in  muscle  cross- 
sectional  area  compensates  for  both  the 
turkeys  higher  hind  limb  GRFs  and  its 
poorer  mechanical  advantage;  despite  a 
5.6-fold  difference  in  muscle  force,  stress- 
es are  not  significantly  different  at  the  an- 
kle in  dogs  and  turkeys. 

The  speeds  measured  in  this  study  were 
approximately  2.0  m/s  in  the  dogs  and  3.5 


290         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


400 


S   200 


Hind  limb 


Fore  limb 


Ankle 


Shoulder     Elbow        Wrist 


Figure  3.  Stress  (force/cross-sectional  area  [/4J)  developed  in  limb  muscles  of  dogs  and  turkeys.  Stresses  are  presented  for 
the  extensors  at  the  joint  indicated,  with  the  exception  of  the  wrist  values,  which  represent  flexor  stresses.  Values  are  means 
and  standard  deviations. 


m/s  in  the  turkeys.  Despite  the  large  dif- 
ference in  absolute  speed,  the  average 
GRF  developed  during  stance  was  similar 
in  the  two  species,  1.3  ±  0.1  X  body 
weight  in  the  bird  and  1.1  ±  0.1  X  body 
weight  in  the  dog.  This  suggests  that  the 
animals  were  operating  at  similar  duty  fac- 
tors, one  of  the  criteria  that  has  been  used 
to  determine  equivalent  speeds  in  running 
mammals  (Biewener,  1983).  The  turkeys 
were  able  to  run  at  faster  speeds  with  duty 
factors  similar  to  those  of  dogs  because 


they  have  longer  legs.  The  small  difference 
in  average  GRF  at  the  speeds  used  in  this 
study  indicates  that  some  of  the  difference 
in  estimated  muscle  stress  may  be  due  to 
a  15—20%  difference  in  the  magnitude  of 
GRF  between  the  dogs  and  turkeys. 

DISCUSSION 

Patterns  of  Force  Development  and  Limb 
Design 

The  results  of  the  present  study  dein- 
onstrate  that  the  timing  of  muscle  force 


Table  1.     Muscle  force  per  unit  peak  ground  reaction  force  (GRF),  total  GRF  and  muscle 

FORCE  IN   MULTIPLES  OF  BODY  WEIGHT  (BW),   MUSCLE  CROSS-SECTIONAL  AREA  (Acs),  AND  MUSCLE  STRESS 

FOR  DOG  AND  TURKEY  HIND  LIMBS. 


Muscle  force  per  GRF 

Peak  GRF  per  BW 

Muscle  force  per  BW 

A,.,  (CU1-) 

Muscle  stress  (kN/m-) 

Hip 

Turkey 

2.3  ±  0.3 

2.4   ±   0.2 

5.8  ±  0.8 

15.9  ±  1.0 

180  ±  28 

Dog 

1.8  ±  1.0 

0.8   ±   0.1 

1.6  ±  0.8 

12.8  ±  2.0 

59  ±  28 

Ratio 

1.3 

3.1* 

3.6* 

1.2 

3.1* 

Knee 

Turkey 

2.3  ±  0.8 

2.4  ±  0.2 

5.7  ±  2.0 

11.0  ±  0.6 

248  ±  65 

Dog 

1.4  ±  0.4 

0.8  ±  0.1 

1.2  ±  0.3 

7.8  ±  0.7 

71  ±  20 

Ratio 

1.6 

3.1* 

4.8* 

1.4* 

3.5* 

Ankle 

Turkey 

6.9  ±  0.7 

2.4  ±  0.2 

16.9  ±  2.3 

50.6  ±  8.4 

163  ±  21 

Dog 

3.6  ±  0.5 

0.8  ±  0.1 

3.0  ±  0.5 

11.4  +  1.5 

125  ±  26 

Ratio 

1.9* 

3.1* 

5.6* 

4.4* 

1.3 

*  Denotes  significant  difference  between  dogs  and  turkeys,  p  <  0.05. 


Muscle  Stress  During  Running  •  Roberts       291 


development  is  remarkably  similar  at  ho-  produced  per  unit  GRF  were  similar  at  the 
mologous  joints  in  the  hind  limbs  of  dogs  knee  and  the  hip  in  dogs  and  turkeys.  Tur- 
and  turkeys.  This  siinilarity  exists  despite  keys  produced  higher  joint  moments  at  the 
differences  in  the  timing  and  magnitude  of  knee  and  hip  because  they  have  larger 
joint  angular  excursions  in  bipedal  birds  muscle  moment  arms,  rather  than  higher 
and  quadrupedal  mammals  (Gatesy  and  muscle  forces.  Thus,  differences  in  mus- 
Biewener,  1991),  as  well  as  differences  in  culoskeletal  anatomy  can  compensate  for 
limb  posture.  Both  dogs  and  turkeys  pro-  differences  in  limb  posture  to  achieve  sim- 
duce  peak  net  extensor  muscle  moments  ilar  mechanical  advantage  for  force  pro- 
early  in  the  stance  phase  at  the  ankle  and  duction.  It  has  recently  been  demonstrat- 
the  hip,  and  late  in  the  stance  phase  at  the  ed  that  the  pattern  of  joint  excursions 
knee.  In  both  species,  the  knee  muscula-  changes  markedly  with  increases  in  walk- 
ture  produces  a  net  flexor  moment  early  ing  or  running  speed  in  guinea  fowl  (Ga- 
in stance,  followed  by  a  net  extensor  mo-  tesy,  1999a).  There  appears  to  be  little 
ment  for  approximately  the  last  two  thirds  change  with  speed  in  the  average  inechan- 
of  stance  phase.  The  similarity  in  joint  mo-  ical  advantage  with  which  muscles  gener- 
ment  timing  between  animals  that  have  ate  force  in  running  quadrupedal  mam- 
significantly  different  limb  morphology  mals  (Biewener,  1989),  but  it  remains  to 
and  have  independently  evolved  cursori-  be  seen  whether  significant  changes  in  the 
ality  tempts  the  speculation  that  this  pat-  pattern  of  force  development  occur  across 
tern  of  joint  moments  is  a  common  feature  speed  in  running  bipeds, 
of  hind  limb  dynamics  in  runners.  How- 
ever, human  runners  exliibit  patterns  of  Biarticular  Muscles  and  Joint  Moment 
joint   moments   different  from   those   ob-  rattems 

served  in  the  present  study.  In  particular.  Several  functional  advantages  have  been 

the  knee  musculature  produces  an  exten-  proposed  for  muscles  that  articulate  across 

sor  moment  diroughout  stance  and  a  net  two  or  more  joints.  Two- joint  muscles  can 

flexor  muscle  moment  is  produced  at  the  operate  to  maintain  a  uniform  length  due 

hip  during  the  second  half  of  stance  phase  to  compensating  displacements  at  two 

(Winter,  1983).  Also,  studies  of  larger  dogs  joints    (Goslow    et    al.,    1973;    McCleam, 

have  found  that,  at  the  hip,  the  net  muscle  1985),  and  can  function  to  transfer  power 

extensor   moment  during  early  stance  is  from    distal    to    proximal    limb    segments 

followed  by  a  significant  net  muscle  flexor  (Gregoire  et  al.,   1984).   It  has  also  been 

moment  during  the  second  half  of  stance  shown  that  two-joint  muscles  play  an  im- 

(Carrier  et  al.,  1998).  portant  role  in  controlling  the  orientation 

The  suggestion  has  been  made  that  the  of  the  GRF  during  various  movements  in 

differences  in  limb  posture  and  joint  ex-  humans  (Jacobs  and  van  Ingen  Schenau, 

cursion    patterns    during    locomotion    be-  1992;  van  Ingen  Schenau  et  al.,  1992).  At 

tween   bipedal   birds   and   quadrupedal  the  same  time,  it  can  be  argued  that  most 

mammals  are  associated  with  the  problem  biarticular  muscles  are  energetically  dis- 

of  bipedal  support  in  birds  ( Store r,  1971;  advantageous  because  they  produce  flexor 

Gatesy,    1990).   The  horizontally  oriented  forces  that  must  be  balanced  by  cocon- 

femur  in  birds  allows  them  to  position  the  traction    of  antagonist    extensor   muscles, 

point  of  support  under  the  center  of  mass  The  present  results  suggest  that  two-joint 

during  standing  or  slow  movement  (Storer,  muscles,  in  both  birds  and  dogs,  provide 

1971).    The    present    study    demonstrates  an  important  mechanism  for  balancing  al- 

that  in  turkeys,  this  difference  in  limb  ori-  temating  flexion  and  extension  moments  at 

entation    results    in    greater    muscle    mo-  a  joint.  The  flexor  moments  produced  at 

ments  per  unit  GRF  compared  with  qua-  the  knee  in  dogs  and  turkeys  appear  to  be 

drupedal  dogs.    However,   muscles  forces  quantitatively  matched  to  the  knee  flexion 


292         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


forces  contributed  by  biarticular  hip  and 
ankle  extensors  (Fig.  2).  Thus,  early  in 
stance  biarticular  muscles  at  the  knee  pro- 
duce force  that  supports  body  weight  at 
both  the  joint  they  act  to  extend  (hip  or 
ankle)  and  the  joint  they  act  to  flex.  The 
long  head  of  triceps  brachii  also  appears  to 
function  early  in  stance  to  provide  support 
through  both  its  flexor  function  at  the 
shoulder  and  its  extensor  function  at  the 
elbow.  Later  in  the  stride  biarticular  mus- 
cles tend  to  increase  the  extensor  force  re- 
quired at  the  knee  and  shoulder.  However, 
electromyographic  studies  indicate  that 
most  of  the  biarticular  inuscles  considered 
in  the  present  study  are  most  active  early 
in  stance  in  dogs  (Tokuriki,  1973;  Goslow 
et  al.,  1981),  allowing  for  the  possibility 
that  energetically  disadvantageous  cocon- 
traction  may  be  reduced  during  the  sec- 
ond half  of  the  stance  phase.  It  may  be 
that  the  important  role  that  biarticular 
muscles  appear  to  play  in  maintaining  the 
proper  orientation  of  the  GRF  (Jacobs  and 
van  Ingen  Schenau,  1992;  van  Ingen 
Schenau  et  al.,  1992)  explains  in  part  the 
similarity  in  joint  moment  patterns  at  the 
knee  in  dogs  and  turkeys. 

Muscle  Stress  and  Strategies  for  Force 
and  Power  Development 

Many  of  the  muscle  stresses  estimated 
in  the  present  study  are  near  the  upper 
end  of  the  range  of  muscle  stresses  typi- 
cally measured  in  vitro  for  vertebrate  skel- 
etal muscle.  Peak  isometric  stress  mea- 
surements typically  range  from  100  to  300 
kN/m^  (Josephson,  1993).  Muscles  can  de- 
velop stresses  above  peak  isometric  when 
actively  lengthening  (Katz,  1939),  and 
stress  is  reduced  as  relative  shortening  ve- 
locity increases  (Hill,  1938).  Thus,  differ- 
ences in  muscle  stress  between  joints  are 
proportional  to  differences  in  fraction  of 
recruited  cross-sectional  area  only  if  the 
muscles  are  operating  at  similar  relative 
shortening  velocities.  The  high  stresses  es- 
timated in  the  present  study  at  the  knee 
of  the  turkey  and  the  wrist  and  shoulder 
of  the  dog  suggest  that  these  muscles  may 


be  operating  near  their  limit  of  force  pro- 
duction, or  undergoing  sufficient  length- 
ening to  operate  at  high  active  muscle 
stresses.  Stresses  measured  at  the  wrist 
likely  overestimate  actual  muscle  stresses, 
because  some  of  the  wrist  moment  is  bal- 
anced by  force  produced  in  stretched  lig- 
aments (Alexander,  1974).  Shoulder  stress 
measurements  may  also  overestimate  ac- 
tual muscle  stress  if  moments  due  to  limb 
inertia  are  significant.  Previous  measure- 
ments of  stresses  in  running  quail  reported 
lower  values  than  those  reported  here  for 
turkeys  (80-100  kN/m^;  Clark  and  Alex- 
ander, 1975).  However,  the  low  speed  and 
GRF  (approximately  1.3  X  body  weight 
peak  GRF)  measured  in  quail  make  direct 
comparison  of  stress  values  with  the  pre- 
sent study  difficult.  It  is  important  to  note 
that  the  present  measurements  of  muscle 
cross-sectional  areas  do  not  account  for 
the  volume  of  noncontractile  elements 
within  inuscle  (mitochondria,  capillaries, 
and  so  on),  which  can  be  as  much  as  40% 
of  the  inuscle  volume  in  bird  pectoralis 
muscle  (James  and  Meek,  1979;  Conley  et 
al.,  1987).  Differences  in  noncontractile 
element  components  between  muscles  or 
between  species  represent  a  potential 
source  of  error  in  comparisons  of  muscle 
stress.  However,  the  variation  in  voluine  of 
nonmyofibrillar  components  between 
these  largely  oxidative  muscles  is  unlikely 
to  be  very  large,  and  could  not  account  for 
the  several-fold  differences  in  muscle 
stress  found  between  inuscle  groups  with- 
in dogs  and  between  dogs  and  turkeys. 

The  similar  stress  hypothesis  for  inuscle 
was  originally  formulated  upon  the  idea 
that  animals  should  operate  their  limb 
muscles  with  the  same  reserve  capacity  for 
force  development  at  equivalent  speeds 
(Perry  et  al.,  1988).  The  hypothesis  was 
supported  by  observations  of  similar  stress 
in  the  ankle  extensors  in  a  bipedal  hopper, 
the  kangaroo  rat,  and  a  quadrupedal  run- 
ner, the  white  rat  (Perry  et  al.,  1988).  The 
similar  scaling  of  locomotor  forces  and 
muscle  cross-sectional  area  across  body 
size   also   supports   the   similar  stress   hy- 


Muscle  Stress  During  Running  *  Roberts        293 


pothesis  (Biewener,  1990).  The  results  versus  force  development.  The  large  mass 
from  the  present  study  for  the  ankle  joint  of  largely  parallel-fibered  muscles  located 
provide  another  example  of  how  large  dif-  proximally  in  the  limb  is  well  suited  to  pro- 
ferences  in  muscle  morphology  can  com-  viding  high  power  outputs,  whereas  the 
pensate  for  differences  in  muscle  forces  to  short  pinnate  fibers  of  the  ankle  in  con- 
produce  similar  stress  in  different  animals,  junction  with  their  long  tendons  function 
However,  a  comparison  of  stresses  be-  well  as  springs  (Alexander,  1974). 
tween  joints  in  the  dog  reveals  that  the  If  differences  in  muscle  stress  between 
similar  stress  hypothesis  is  not  supported  joints  reflect  specializations  of  different 
for  comparisons  between  different  muscle  muscle  groups  for  power  versus  force  de- 
groups  operating  at  different  joints.  velopment,  then  a  Comparison  of  muscle 
Why  do  some  muscle  groups  operate  stresses  in  dogs  and  turkeys  may  provide 
with  a  greater  reserve  capacity  for  force  insight  into  how  avian  and  luammalian 
development  (i.e.,  low  stress)  during  run-  limbs  are  designed  to  provide  work  for 
ning?  This  variation  in  reserve  capacity  high-power  activities.  Turkeys  operate 
may  reveal  a  specialization  of  some  mus-  with  the  same  reserve  capacity  for  force  at 
cles  for  locomotor  activities  that  involve  the  hip  and  the  ankle.  Furthennore,  the 
high  mechanical  power  outputs.  The  cross-  muscle  mass  distribution  is  strikingly  dif- 
sectional  area  of  active  muscle  required  to  ferent  in  birds  compared  with  mammals, 
produce  force  during  high-power— output  The  muscle  mass  available  to  extend  the 
activities  such  as  acceleration,  jumping,  or  ankle  in  birds  is  greater  than  that  available 
incline  running  can  be  greater  than  that  to  extend  the  hip  (compared  with  a  hip 
required  during  level  running  because  of  muscle  mass  greater  than  three  times  the 
an  increase  in  GRF  or  a  change  in  muscle  ankle  muscle  mass  in  dogs;  Roberts  et  al., 
mechanical  advantage.  Perhaps  more  im-  1998).  The  mechanical  power  that  can  be 
portantly,  the  cross-sectional  area  of  active  developed  at  a  joint  is  proportional  to  the 
muscle  must  also  increase  if  the  relative  muscle  mass  (assuming  equivalent  muscle 
shortening  velocity  of  the  muscle  increas-  properties);  thus  the  large  muscle  mass  at 
es,  as  has  been  demonstrated  for  the  lat-  the  ankle  in  birds  represents  a  significant 
eral  gastrocnemius  muscle  in  turkeys  run-  potential  source  of  power  for  movement, 
ning  on  an  incline  (Roberts  et  al.,  1997).  The  present  ineasureinents  of  muscle 
It  might  be  expected  that  muscle  groups  stress  suggest  that  turkeys  may  power  ac- 
that  operate  with  a  high  reserve  capacity  celerations  and  jumps  as  inuch  with  the 
during  level  running  are  the  most  impor-  ankle  musculature  as  with  the  hip.  In  fact, 
tant  power  producers  during  acceleration  measurements  of  turkeys  running  uphill 
or  jumping.  It  has  been  generally  assumed  suggest  that  the  gastrocnemius  increases 
that  it  is  the  muscles  that  articulate  be-  muscle  shortening,  recruitinent,  and  pow- 
tween  the  limb  and  the  body  (extrinsic  er  output  to  provide  the  power  to  run  up- 
muscles),  and  particularly  those  in  the  hill  (Roberts  et  al.,  1997).  Thus,  differenc- 
hind  limb,  that  are  the  primary  sources  of  es  in  muscle  mass  distribution  and  limb 
power  for  acceleration  (Gray,  1968).  Like-  design  between  running  birds  and  mam- 
wise,  it  has  been  shown  that  jumping  dogs  mals  may  reflect  differences  in  strategies 
produce  the  greatest  muscle  work  and  for  powering  accelerations,  rather  than  dif- 
power  at  the  hip  with  a  smaller  contribu-  ferences  in  muscle  function  during  steady- 
tion  at  the  knee  and  almost  no  change  in  speed  running, 
ankle  muscle  function  froin  running  to  ^....^..,.  ^^^.  .^».-^^ 
jumping  (Alexander,  1974).  Alexander  ACKNOWLEDGMENTS 
(1974)  suggested  that  differences  in  mus-  I  thank  M.  S.  Chen  for  help  with  ex- 
cle  architecture  in  proximal  versus  distal  periments  and  data  analysis,  and  the  late 
muscles  reflects  a  specialization  for  power  C.  R.  Taylor  for  his  help  and  support  with 


294         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


the  project.  The  project  was  supported  in 
part  by  National  Institutes  of  Health  grant 
ROl  AR18140. 

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REGULATION  OF  SKELETAL  MUSCLE  REGENERATION  AND  BONE 
REPAIR  IN  VERTEBRATES 

URI  ORON^ 

Abstract.    The  aim  of  the  present  study  was  to  in-  long  bones  in  rats  (Markel  et  al.,  1991).  In 

vestigate  the   effect  of  low-energy  laser  irradiation  ^^.j^g^.  models,  bone  repair  was  investigated 

(LELI)  on  the  process  of  skeletal  muscle  regenera-  .       .1               j    11                  -1,        r  4-1  ^   4--U- .    ,fi-^^ 

L          J  u               ■        ,-    A       A     ^    T->^ft„^^  ;..  in  the  medullary  cavity  ot  the  tibia  atter 

tion  and  bone  repair  m  toads  and  rats.  Denned  m-  J              J                     r            1 

juries  (partial  excision  or  cold  injury)  to  the  gastroc-  ablation  or  removal  ot  marrow  trom  long 

nemius  muscle  and  hole  injury  to  the  tibia  in  rats  bones.     Ill    this    model,    regeneration    was 

were  performed.  The  rate  of  regeneration  in  skeletal  found  tO  be  preceded  by  a  local  phase  of 

muscles  was  analyzed  by  quantitative^  histomoipho-  ^^^05^^^!    bo^e    formation    (Liang    et    al., 

metric  methods,  and  bone  repair  was  determmed  us-  ,„„^.     „               .             p  ,1                              c^ 

inghistomorphometric  methods.  Low-energy  laser  ir-  1992).    Promotion   of  the  procesS   of   boiie 

radiation  (He-Ne  laser)  was  applied  directly  to  the  repair  has  been  achieved  in  the  past  by 

injured  sites  for  2  minutes  at  different  time  intervals  autOgeilOUS    bone    grafting,    application    of 

postinjuiy.  The  rate  of  skeletal  muscle  regeneration  ^^rious  growth  factors   (mainly  bone  mor- 

was  enhanced  Uvo- and  eightfold  in  the  rat  and  toad,  ,               ^                        .           re                         4-     „1 

respectively,  whereas  bone^epair  was  enhanced  two-  phogenetlC     proteins     [Spencer     et     al., 

fold  by  the  LELI.  Although  mechanism  of  the  laser  1991  J),    USe   ot    low-mtensity  pulsed  ultra- 

irradiation  is  not  yet  clearly  understood,  it  is  associ-  souild  and  electromagnetic  fields  (Cane  et 

ated  with  gene  activation  in  the  ceU  and  the  trigger-  .^\      1993)^  and  by  low-energy  laser  irradi- 

ing   of  a   cascade    of  intracellular   events   initiating  ^^.^^^     (LELI)     in     vivo     (Kusakari     et     al., 

changes  in  physiologic  processes  in  tlie  celi.  OQO^ 

,- ,T._,_r->i  1,^-ri^M  Low-energy  laser  irradiation  has  recent- 

INTRODUCTION  ,1          r        1  .          j  1  .                 lv.i^^ 

ly  been  lound  to  modulate  various  biolog- 

The  process  of  skeletal  muscle  regen-  ical  processes  in  tissue  cultures  and  animal 

eration  after  injuiy  has  been  well  docu-  models  (Belkin  et  al.,   1988;  Karu,   1989, 

mented  and  reviewed  in   mammals   (All-  1998;  Galletti  et  al.,  1992;  Conlan  et  al., 

brook,  1981;  Carlson  and  Faulkner,  1983),  1996).  For  example,  laser  irradiation  was 

and  to  a  much  lesser  extent  in  amphibians  found  to  increase   mitochondrial  respira- 

(Carlson,    1970).   The  possible   regulatory  tion    and    adenosine    triphosphate    (ATP) 

mechanisms  associated  with  the  process  of  synthesis  (Morimoto  et  al.,   1994;  Zhu  et 

muscle  regeneration,  and  the  stimulation  al.,  1997)  and  to  modulate  oxidative  me- 

of  the  dormant  satellite  cells  after  injury  tabolism  in  the  mitochondria  (Yu  et  al., 

are  not  yet  fully  understood.  1997).    Low-energy  laser   irradiation   also 

Osteogenesis  and  bone  repair  after  trau-  was  demonstrated  to  elevate  activity  of  an- 

ma  are  regulated  by  such  mechanisms  as  tioxidant  enzymes  such  as  superoxide  dis- 

growth  factors  and  hormones,  among  oth-  mutase  and  catalase  (Zhu  et  al.,  1997)  and 

ers  (Marks  and  Popoff,  1988).  Several  ex-  to  enhance  nitric  oxide  (NO)  production 

perimental  models  have  followed  the  heal-  in  rat  lymphocytes  (Chi  et  al.,  1995).  The 

ing  of  osseous  defects  (usually  fractures)  in  biostimulatoiy  effect  of  LELI  was  also  in- 
vestigated in  several  experimental  animal 

r^    ,        ^           o  A, 7-     T-      1^  models  after  injury.  Helium-neon  laser  ir- 

'  Department  of  Zoologv,  George  S.  Wise  Faculty  -,.      .                    -^i                  ..1l         i 

of  Life  Sciences,  Tel  A^v  University,  Ramat  Aviv  radiation  was  demonstrated  to  elevate 

69978,  Israel.  coinpouiid  action  potential  after  crush  in- 
Bull.  Mus.  Comp.  Zool.,  156(1):  297-303,  October,  2001         297 


298         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


jury  to  the  ischiadic  nerve  (Rochkind  et  al.,  ture    (3-4   months   old,   300-350   g   body 

1987),  as  well  as  slow  Wallerian  degener-  weight)   Sprague-Dawley  male  rats  (Lev- 

ation  in  the  injured  optic  nerve  (Schwartz  instein  Inc.,  Yoknean,   Israel).   Rats  were 

et  al.,  1987;  Assia  et  al.,  1989).  The  inflam-  anesthetized  with  Avertin  (1  ml/100  g  body 

matory  response  after  cold  injury  to  toad  weight    intraperitoneally).    A    longitudinal 

muscle  also  was  demonstrated  to  be  mark-  incision  was  made  through  the  skin  and 

edly  decreased  by  laser  irradiation  (Bibi-  muscles  to  expose  the  tibia  on  its  proximal 

kova  and  Oron,  1993),  and  neoformation  and  medial  surfaces  about  10—15  mm  dis- 

of  blood  vessels  in  the  injured  zone  was  tal  to  the  knee  joint.  A  hole  was  drilled  in 

demonstrated  to  be  elevated  by  laser  ir-  the  cortical  bone  of  the  tibia  in  the  center 

radiation  (Bibikova  et  al.,  1994).  Recently,  gf  its  medial  aspect  about  9  inm  distal  to 

we  have  shown  that  LELI  causes  indue-  the  knee  joint   (diaphyseal  region)   using 

tion  of  cell  cycle  regulatory  proteins  in  sat-  hand-driven  dental  drills  of  increasing  di- 

ellite  cells  from  skeletal  muscles  due  to  ac-  ameter  in  order  to  obtain  a  final  hole  di- 

tivation  of  early  cell  cycle  regulatory  genes  ameter  of  1.6  mm.  The  hole  was  created 

(Ben-Dov  et  al.,  1999).  in  such  a  manner  as  to  penetrate  the  cor- 

The  aim  of  the  present  study  was  to  in-  tical  bone  and  damage  the  trabeculae  in 

vestigate  the  effect  of  LELI  on  skeletal  the  medullary  canal,  but  not  to  damage  the 

muscle  regeneration  in  rats  and  toads  and  contralateral  cortical  bone.  Care  was  taken 

bone  repair  in  rats.  not  to  injure  the  periosteum  in  the  vicinity 

of  the  hole.   After  the  inuscles  and  sldn 

MATERIALS  AND  METHODS  were  sutured,  the  rats  were  injected  intra- 

Surgical  Procedures  muscularly   with    Penicillin    G    Sodium 

(leva,  retach- 1  ikva,   Israel)  at  a  dose  ot 

Foity-nine  male  toads  {Bufo  viridis)  and  100  U/g  body  weight,  followed  by  3  days 

30  mature  male  laboratory  rats  (Charles  of  bioxin  (Solmycin  500,  Teva,  Petach-Tik- 

River)  were  used  for  the  experiments.  Par-  va,  Israel)  in  the  drinking  water  (1  g/L).  In 

tial  excision  to  the  gastrocneinius  inuscle  the    above    model    a   spontaneous   partial 

of  the  rats  was  performed  as  previously  de-  healing  of  the  gap  injury  (probably  due  to 

scribed  (Roth  and  Oron,  1985).  Cold  in-  its  low  diameter  relative  to  the  tibia  width) 

jury  to  the  toads'  muscles  was  performed  occurs  at  about  3  weeks  after  injury,  and  a 

by  placing  the  end  of  a  copper  rod  (1.8-  complete  healing  occurs  at  longer  time  in- 

mm  diameter),  prechilled  in  liquid  nitro-  teivals. 
gen,   against  the  muscle  for   10  seconds. 

This  created  an  injured  zone  of  about  4  Laser  Irradiation 

mm  in  diameter.  Four  to  six  injured  ex-  An  He-Ne  laser  (Ealing,  Electro-Optics, 

perimental    (laser-irradiated)    and   control  Holliston,   Massachusetts,   USA)  was  em- 

(injured  and  irradiated  by  red  light)  toads  ployed  at  632  nm,  5.3-mW  power  output, 

or  rats  were  used  for  each  time  interval  (9,  and  1.9-miTi  beam  diameter.  Laser  irradi- 

14,  and  30  days  for  toads;  3,  8,  and  11  days  ation  was  always  applied  directly  on  the 

for  rats)  postinjury.  In  brief,  after  removal  injured  zones  of  the  skeletal  muscles  of  the 

of  the  skin  and  biceps  femoris  muscle  the  toads  and  rats  after  removal  of  the  skin 

gastrocnemius  was  exposed.  A  special  de-  and  muscle.   In  order  to  cover  the  total 

vice  with  two  fixed  scalpel  blades  was  ap-  area  of  the  injured  zone  (which  was  larger 

plied  to  create  a  fixed  excision  (5X2  mm)  than  the  laser  beam  diameter)  in  the  mus- 

in  the  middle  part  of  the  lateral  belly  of  cles,  the  laser  was  applied  several  times  to 

the  gastrocnemius  muscle.  The  biceps  fe-  each  of  the  visibly  injured  zones.  Laser  ir- 

inoris  and  the  skin  were  then  closed.  radiation  to  toad  injured  zones  in  the  mus- 

Surgery  to  create  a  fixed  injuiy  to  the  cles  was  applied  every  alternate  day,  from 

tibia  was  performed  on  a  total  of  52  ma-  4  days  until  14  days  post— cold  injury,  for 


Regeneration  of  Bone  and  Skeletal  Muscle  •  Oron        299 


2.3  minutes  each  time  (31  J/cm^).  Laser  ume  fraction  of  typical  stnictures  such  as 
irradiation  to  the  rats' skeletal  muscles  was  inononucleated  cells,  inyotubes,  and 
applied  as  for  the  toad,  but  only  on  the  young  myofibers  in  the  injured  area.  The 
second  and  third  day  postinjury.  In  the  laser  irradiation  during  the  process  of 
case  of  the  hole  injury  in  the  tibia,  laser  inuscle  regeneration  caused  a  significant 
irradiation  was  applied  on  days  5  and  6  change  in  the  voluine  fraction  of  these 
postinjury  once  a  day  for  2.3  minutes  (31  structures  in  the  trauinatized  area  at  all 
J/cm-)  directly  on  the  hole  injury  after  time  intervals  after  injury.  Young  myofi- 
careful  removal  of  the  sutures  in  the  skin  bers  populated  15.5  ±  7.9%  and  65.0  ± 
and  muscles  above  it.  In  all  control  (sham-  9.5%  of  the  muscle  regenerates  in  the  in- 
operated)  experimental  animals,  the  laser  jured  zone  in  the  laser-irradiated  toad 
was  applied  but  was  not  connected  to  a  muscles  at  9  and  14  days,  respectively; 
power  source.  whereas  in  control  nonirradiated  inuscle 

regenerates  young  myofibers  were  not  ev- 

Histology  and  HiStomorphometry  i^ent  at  9  days  postinjury,  and  comprised 

At  various  time  intervals  postinjury  the  only  5.3  ±  2.9%  of  the  area  at  14  days 
rats  were  anesthetized  with  chloroform,  (Figs.  1,  2a).  The  process  of  muscle  regen- 
and  the  gastrocnemius  muscle  exposed,  re-  eration  in  toads  was  almost  completed  af- 
moved,  fixed  in  Bouin's  fixative,  and  em-  ter  30  days  (90%  of  the  regenerated  area 
bedded  in  paraffin.  Serial  sections  were  was  occupied  by  mature  muscle  fibers)  in 
prepared  from  each  muscle  and  stained  the  laser-treated  muscles,  whereas  in  con- 
with  hematoxylin  and  eosin  and  Masson's  trol  muscles  only  young  myofibers  still 
trichrome  stain.  Morphometric  measure-  populated  a  large  part  (75.7  ±  13.2%)  of 
ments  were  per^formed  on  the  entire  in-  the  injured  zone  (Fig.  2b).  In  the  case  of 
jured  zones  of  four  to  six  randomly  chosen  the  rat  gastrocnemius  muscle,  young  myo- 
sections  per  each  muscle,  using  the  point  fibers  were  not  evident  in  the  injured  zone 
mounting  method.  The  volume  fraction  of  either  experimental  or  control  muscles 
(%  of  the  total  volume  of  injured  zone)  at  3  days  postinjury.  Their  volume  fraction 
was  calculated  for  each  of  the  structures  was  twofold  significantly  higher  in  LELI- 
analyzed.  The  results  were  finally  statisti-  treated  rat  muscles  as  compared  to  control 
cally  analyzed  using  the  three-level  nested  muscles  at  8  and  11  days  postsurgeiy,  re- 
analysis  of  variance.  spectively  (data  not  shown). 

Injured  tibial  bone  from  six  rats  was  tak-  The  morphometric  analysis  of  the  tissue 

en  at  each  time  interval  (10,  13,  and  15  components  of  the  hole  in  the  rat  tibia  in- 

days)  postinjury.  This  bone  was  fixed,  de-  dicated  that  at  all  time  intenals  (10,  13, 

calcified,   and  processed  for  histology  as  and  15  days)  the  relative  areas  occupied 

described  above.   Histomorphometry  was  by  compact  bone  in  the  hole  injury  were 

performed  to  determine  the  area  fraction  higher  in  the  LELI-treated  rats  than  in  the 

of  various  structures  (woven  bone,  com-  control  (Figs.  3,  4).  At  15  days  postinjury 

pact  bone,  and  so  on)  in  the  gap  created  to  the  tibia,  this  value  comprised  92  ±  9% 

in  the  tibia  out  of  the  total  area  of  the  gap  in  the  LELI-treated  rats,  which  was  sig- 

(injured)   zone.   This   process   was   per-  nificantly  (P  <  0.01)  higher  than  the  area 

formed  with  a  microscope  and  the  aid  of  that  the   compact  bone   occupied   (58    ± 

a  video  camera  and  screen  using  Sigma  8%)  in  the  control  nonirradiated  rats. 

Scan  software.  __    ^ 

DISCUSSION 

ntbULIb  'pj^g  results  of  the  present  study  clearly 

The  process  of  muscle  regeneration  in  indicate  that  the  process  of  muscle  regen- 

control  muscles  after  cold  injury  was  char-  eration  after  partial  excision  injury  or  cold 

acterized  by  sequential  changes  in  the  vol-  injury  is  markedly  promoted  by  direct  ex- 


300         Bulletin  Museum  of  Comparative  Zoology,  Vol.  156,  No.  1 


Figure  1 .  Light  micrographs  of  regenerated  area  in  control  nonirradiated  (a)  and  laser-irradiated  (b)  toad  gastrocnemius  muscle 
14  days  postinjury.  Note  mainly  myotubes  (MT)  and  mononucleated  (MN)  cells  in  (a)  as  compared  to  mainly  young  myofibers 
(YU)  with  large  diameter  in  (b).  x40. 


30    DAYS    AFTER    INJURY 


YOUNG    MYOFIBERS 


# 


c 
o 


u 

eg 


4) 

E 
_2 

o 

> 


MN  YM  MF 

Histological    structures 


^ 


14 
Days    after    injury 


30 


Figure  2.  Volume  fraction  of  young  myofibers  at  various  time  intervals  post-cold  injury  to  the  toad  gastrocnemius  muscle  injury 
(a)  and  of  mononucleated  cells  (MN),  young  myofibers  (YM),  and  mature  myofibers  (MP)  at  30  days  postinjury  (b).  Values  are 
mean  ±  SEM  of  control  nonirradiated  (dashed  columns)  and  laser-irradiated  (solid  columns)  muscles. 


Regeneration  of  Bone  and  Skeletal  Muscle  •  Oron 


301 


COMPACT    BONE 


«• 


^ 


E 

O 
> 


10  13  15 

Days    After    Injury 

Figure  3.  Volume  fraction  of  compact  bone  at  the  site  of  in- 
jury to  the  rat  tibia  at  different  time  intervals  postinjury.  Note 
less  compact  bone  in  the  control  nonirradiated  rats  (dashed 
columns)  as  compared  to  low-energy  laser-irradiated  rats  (sol- 
id columns).  *P  <  0.05;  **P  <  0.01. 


posure  to  He-Ne  laser  irradiation  (during 
the  regeneration  process)  in  both  toads 
and  rats,  although  in  the  toads  the  pro- 
motion effect  was  higher.  We  have  recent- 
ly shown  that  LELI  promotes  proliferation 
of  satellite  cells  from  skeletal  muscle  origin 
grown  in  culture  (Ben-Dov  et  al.,  1999). 
These  cells  are  considered  to  be  the  stem 
cells  for  muscle  regeneration  and,  there- 


fore, their  enhanced  proliferation  by  LELI 
in  vitro  may  explain  the  enhanced  kinetics 
of  regeneration  in  vivo,  as  demonstrated  in 
the  present  study.  Because  we  have  pre- 
viously found  that  LELI  also  proinotes 
new  blood  vessel  formation  (angiogenesis) 
at  the  site  of  skeletal  inuscle  regeneration 
(Bibikova  et  al.,  1994),  it  might  be  postu- 
lated that  a  better  oxygen  and  nutrient 
supply  will  also  contribute  to  enhancement 
of  the  regeneration.  Assia  et  al.  (1989)  sug- 
gested that  in  the  case  of  optic  nerve  re- 
generation after  crush  injury,  LELI  acts  to 
slow  degenerative  processes  rather  than 
promoting  regeneration,  and  that  the  ef- 
fect of  laser  irradiation  is  transient  and 
subsides  markedly  when  irradiation  ceases. 
In  the  present  work,  the  effect  of  laser  ir- 
radiation was  not  transient  because  the 
ainount  of  newly  formed  young  myofibers 
was  twofold  higher  in  the  injured  zone  of 
experimental  rats  after  two  subsequent  la- 
ser irradiations.  Tissue  reaction  to  injury  in 
cranial  nerves  and  skeletal  muscles  is  most 
probably  entirely  different  and  they  may 
react  differently  to  laser  irradiation.  The 
results  of  the  present  study  also  indicate 


Figure  4.  Light  micrographs  of  longitudinal  section  of  the  injured  zone  in  the  tibia  of  control  (a)  and  laser-irradiated  (b)  rat  at 
13  days  postinjury.  Note  the  gap  in  the  tibia  (marked  by  arrows)  that  is  filled  only  with  woven  bone  (WB)  in  the  control  nonir- 
radiated rat  and  partially  filled  with  compact  bone  (CB)  that  bridges  the  gap  in  the  laser-irradiated  rat.  x120. 


302         Bulletin  Museum  of  Comparative  Zoologtj,  Vol.  156,  No.  1 


that  LELI  may  promote,  to  a  much  higher  hances  synthesis  of  ATP.  Changes  in  plas- 

extent,  biological  processes  in  cells  with  ma  membrane   conduction  and  transient 

lower  metabolic  rates  such  as  in  the  toads  increase  of  calcium  flux  into  the  cells  have 

(as  compared  to  the  rats).  These  results  also  been  observed  in  cells  irradiated  in 

corroborate  the  notion  that  during  a  high  vitro  by  low  energy  lasers  (Lubart  et  al., 

state  of  metabolism  and  proliferation,  cells  1997).  These  changes  are  photochemical 

are  affected  to  a  lesser  extent  by  laser  ir-  in  nature;  the  energy  is  probably  absorbed 

radiation  (Karu,  1989,  1998).  in    intracellular   chromophores    and    con- 

This   communication   also   indicates  by  verted  into  metabolic  energy  involving  the 

direct  measurements  that  the  rate  of  bone  respiratory   (cytochrome)   chain   (Karu, 

repair  in  the  cortical  part  of  the  tibia  in  an  1989,  1998;  Galletti  et  al,  1992). 

experimental  model  in  the  rat  is  enhanced  We  have  recently  shown   (Ben-Dov  et 

by  LELI.  Kusakari  et  al.  (1992)  previously  al.,   1999)  that  LELI  causes  induction  of 

reported  stimulation  of  DNA  and  protein  cell  cycle  regulatory  proteins  in  satellite 

synthesis,  and  alkaline  phosphatase  activity  cells  from  skeletal  muscles,  due  to  activa- 

in  osteoblastlike  tissue  culture  by  LELI.  tion  of  early  cell  cycle  regulatory  proteins. 

These  results  corroborate  the  results  of  the  Furthermore,  it  was  recently  found  (un- 

present  study  indicating  that  the  enhance-  published    data,    this    laboratoiy)    in    the 

ment  of  bone  repair  may  be  caused  by  en-  same  system  that  LELI  induces  activation 

hanced  proliferation  of  osteoblasts  at  the  of  receptors  on  the  cell  plasma  membrane 

injured  site.  and  other  components  associated  with  cell 

The  present  study  demonstrates  that  proliferation  (kinase  enzymatic  activity)  in 
LELI  can  promote  skeletal  muscle  regen-  a  certain  signal  transduction  pathway  in 
oration  as  well  as  bone  repair,  indicating  the  cell.  Thus,  it  may  be  postulated  that 
that  the  biostimulation  may  have  a  com-  the  LELI  biostimulates  the  cell  via  certain 
mon  mechanism  that  triggers  certain  cell  mechanisms  at  the  molecular  level.  How- 
processes  that,  in  turn,  will  enhance  cell  ever,  the  precise  interaction  of  the  laser 
proliferation  and  differentiation  in  the  irradiation  with  cellular  components  or 
skeletal  tissues.  Thus,  it  may  be  hypothe-  molecules  that  trigger  a  cascade  of  intra- 
sized  that  the  mechanism  of  biostimulation  cellular  processes  that  eventually  lead  to 
by  LELI  may  be  general  for  various  tissues  changes  in  physiologic  processes  in  the 
and  in  different  groups  of  vertebrates,  cells  will  have  to  be  elucidated  by  further 
However,  parameters  such  as  energy,  studies, 
wavelength,  and  timing  of  laser  may  differ 

for  different  tissues  and  according  to  the  LITERATURE  CITED 

physiologic  state  of  the  cells  to  be  biosti-  Allbrook,  D.    1981.   Skeletal  muscle  regeneration, 

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