Evolution of Prey Capture Strategies and Diet in Tiie Pinnipedimorpha

Home , Caribbean monk seal, Enaliarctos, Imagotaria, Monachinae, Phocinae

ORYCTOS,Vol.4 : 83- 107,Décembre2002

EVOLUTIONOF PREY CAPTURE STRATEGIES AND DIET IN TIIE PINNIPEDIMORPHA (MAMMALIA,CARNIVORA)

Peter J. ADAM" and Annalisa BERTA'?

rPresentaddress (for correspondence):Department of OrganismalBiology, Ecology,and Evolution, University of California, Los Angeles,621 CharlesE. Young Dr., South,Los Angeles,California, U.S.A. 90095-1606,E-mail: [email protected] 'Departmentof Biology, SanDiego StateUniversity, 5500 CampanileDr., SanDiego, California, U.S.A. 92182-4614,E-mail: (AB) [email protected]

ABSTRACT : Pinnipedsrepresent a lineage of terrestrial carnivoresthat have secondarilyadapted to a marine existence and must capture and processprey under water. We examined known diets and skull morphologies associated with different prey capture strategiesin extant and fossil pinnipedimorphs using a phylogenetic context to reveal their evolutionary feeding history and diversity. Unlike their arctoid ancestors,no extant pinnipedimorph masticates food. Prey capture is accomplished by four methods, characterizedby numerous craniodental features (in parentheses): 1) pierce feeding (homodonty; M1 anterior to dentary midlength; enlargedorbit); 2) suction feeding (elon- gate and vaulted palate; robust pterygoid hamuli; mandibular fusion); 3) filter feeding (high-crowned, intricately cusped postcanine teeth; upper and lower teeth interdigitating; post-dental ridges); and 4) grip and tear feeding (straight, sharply pointed postcaninecusps; enlarged incisors). Pierce feeding is typical of most pinnipedimorphs, while filter feeding is limited to extant crabeaterseals and grip and tear feeding to living leopard seals.A tendency toward suction feeding occurs in at least four independentlineages (otariine sea lions, bearded seal, and dusignathine and odobeninewalruses), although it is best developedin odobenines.Only a weak correlation between functional anatomy and diet was observedfor extant taxa. For example, suction feeding is utilized by walruses to capture and consumebenthic mollusks, but skulls with convergent evolution of suction associatedcharacters are also well designedfor capturing larger fish and squid (e.g. Otaria byronia).

Keywords: Pinnipedia, Phocidae, Otariidae, Odobenidae,Evolution, Adaptation, Feeding, Diet, Morphology, SkUII

Evolution des Strategies de Capture de la Proie et Regirne alimentaire chez les Pinnipedimorpha (Mammalia, Carnivora)

Résumé : Les Pinnipèdesconstituent une lignée de Carnivores terrestresadaptés secondairement à une existence marine ; ils doivent capturer et manipuler leurs proies sous I'eau. Nous avons étudié les régimes alimentaireset les morphologiescrâniennes associés aux différentesstratégies de capture de la proie chez les pinnipédimorphesactuels et fossiles.Les résultatssont intégrésdans un cadrephylogénétique afin de retracerl'histoire et la diversité évolutive des modes d'alimentation. A la différence de leurs ancêtresarctoides, aucun pinnipédimorphe connu ne mastique sa nourriture. La capturede la proie est effectuéeselon quatremodes caractérisés par de nombreux traits du crâneet des dents (caractèresentre parenthèses): 1) I'alimentation par percement (homodontie; M1 est situé à I'avant de la mi- longueur de la denture;orbite agrandie);2) I'alimentation par succion (palais allongé et voûté; hamuli du ptérygoide robuste; fusion mandibulaire); 3) l'alimentation filtrante (dents postérieuresaux caninesavec une couronnehaute et des cuspidescomplexes; dents supérieureset inférieures inter digitées; crêtes situéesà l'arrière des sériesdentaires 83 ORYCTOS,YoL.4,2002

de la mandibule et des maxillaires); et 4) l'alimentation par <(cuspides des post-canines droites et très pointues; incisives agrandies).L alimentation par percement caractérisela plupart des pinnipédi- morphes, alors que l'alimentation filtrante paraît être limitée aux phoques actuels se nourrissant de crabeset I'alimentation par paraît être limitée aux phoques léopards. Une tendancevers l'alimentation par succion s'observe dans quatre lignées indépendantesau moins (les lions de mer, le phoque barbu ainsi que les morsesdusignathines et odobénines),mais elle est la plus développéechez les morsesodobénines. La relationentre l'anatomie fonctionnelle et le régime alimentaire observé sur les taxons actuels présenteune faible corrélation. Par exemple,l'alimentation par succion est utilisée par les morsespour captureret consommerdes mollusquesben- thiques et d'autres invertébrés,mais des crânesprésentant une évolution convergentedes caractèresliés à l'alimentation pas succion sont également bien adaptésà la capture de poissons et de calmars de plus grande taille (par exempleI'otarie du sud, Otaria byronia).

Mots clés : Pinnipedia, Phocidae, Otariidae, Odobenidae,Evolution, Adaptation, Régime alimentaire, Morpholo- gie, Crâne

mammals,the wholly aquatic cetaceans(whales), INTRODUCTION sirenians(manatees and dugongs),sea otter and the amphibiouspinnipeds (seals, sea lions, andwalruses) There have been many hypothesesdeveloped to representfour lineagesthat have readaptedto life in explain causalfactors leading to the invasion of land the water.Fossil evidencealso suggeststhat at least by primitive tetrapodsduring the Late Devonian.The one edentate(a marine sloth; de Muizon & McDo- most popularof thesetheories include reduced pre- nald, 1995)and ursid (bear;Tedford et aI., 1994),and dation and competitive pressureson land and an the desmostylians(Inuzuka et al.,1994) were secon- increased availability of food and other resources darily aquatic. Similar to the invasion of land from relative to the marine environment (Holman, 1970; the water, moving from a terrestrial to an aquatic Vermeij& Dudley,2000). Regardless of the cause(s), environment requires the evolution of methods for the shift from an aquaticenvironment to a terrestrial copingwith increasedheat loss, salinity, gas exchan- one hasled to a greatdiversification of terrestrialver- ge, locomotion, and feeding,among others. Attempts tebrates, as well as to the development of many to determinethe causalmechanisms behind seconda- remarkablemethods for coping with suchchallenges ry re-invasionsof the water are typically speculative, as gasexchange, water loss, locomotion, and feeding but utilization of nearshoremarine food resources in a non-fluid environment.Despite these evolutiona- with subsequentaquatic adaptationand diversifica- ry <>however, secondary re-adap- tion appears to be a common postulate (see for tation to a wholly aquatic lifestyle has occurred in exampleDomning's (1978) study of sireniansand many independentlineages of amniote vertebrates O'Leary & Uhen's(1999) examination of cetaceans). and has resultedin remodeling of terrestrially adap- Vermeij & Dudley (2000) further note that for such ted morphologiesand physiologiesto cope with an an invasion to take place,the invading taxon must be aquatic environment (Vermeij & Dudley, 2000). able to effectively competefor resourcesin the new Among living reptiles, chelonians (turtles and tor- environment. Thus, knowledge of the feeding toises),hydrophiids (sea snakes),crocodilians, and methodsand capabilitiesof fossil marine teffapodsis the marine iguana have secondarily- and indepen- requisite to understandingpossible factors that may dently - returned to a marine existence.The extinct haveallowed them to secondarilyinvade marine habi- plesiosaurs,ichthyosaurs, placodonts, and mosasaurs tats. Here, we examinethe functional morphology of are well-known secondarilymarine reptiles from the feedingin living and extinct pinnipedsand attemptto Mesozoic.The birds also have numeroussecondarily document evolutionary transitions and diversity in aquaticmembers, including southernsphenisciforms feeding behavioursand diet within the group. Our (penguins),several northern alcids (auks),and fossil analysis is conductedwithin a phylogeneticframe- taxa such as the CretaceousHesperornis. Among work, thus allowing us to elucidate the probable 84 ADAM & BERTA- EVOLUTIONOF PREYCAPTURE STRATEGIES AND DIET IN THE PINNIPEDIMORPHA timing of changes in feeding strategies between evidenced by both morphological (e.g. Berta and lineages. Wyss, 1994) and (in part) molecular (Vrana et al., Extant pinnipeds are carnivoran mammals that 1994) data. include three major lineages,the Phocidae (<> Two major extinct cladesare known in addition seals), Odobenidae (walruses), and Otariidae (fur to extant lineages. Enaliarctos is the most basal sealsand sea lions). It hasbeen argued that pinnipeds known taxon, and has been recoveredfrom deposits areparaphyletic, with phocidshaving close ties with of late Oligocene to Miocene age in western North the Mustelidae(otters and kin) and otariids plus odo- America and Japan(Berta, l99la; Kohno, 1992).A benidshaving a common ancestrywith ursids (e.g. secondbasal taxon, Pteronarcfos,is known from Wozencraft,1989). However, overwhelming eviden- western North American Miocene deposits (Berta, ce from both morphological(e.g. Berta & Wyss, l99lb). Enaliarctos and Pteronarctos,together with 1994;Bininda-Emonds & Russell,I996;Yruna et al., the Pinnipediaconstitute the Pinnipedimorpha(sensu 1994) and molecular(e.9. Flynn & Nedbal, 1998; Berta & Wyss, 1994).The extinct group formed by Ledje & Ârnason,l996a,b) sourcesclearly indicates Allodesmus,Desmatophoca, and Pinnarctidion is the that the group is monophyletic,although their precise sister group to the Phocidae,and with the phocids origin within arctoid carnivores remains contro- comprisethe Phocoidea.Table 1 summarizeschrono- versial.A second,more recentdebate over pinniped logical and locality data for these and other fossil relationshipsconcerns the position of the Odobeni- taxaincluded in this analysis. dae to the other two extant lineages.Odobenids have That modern pinnipeds are well adaptedfor an been traditionally groupedwith the Otariidae as the aquatic life is clearly evidencedby their possession Otarioidea, a hypothesis that has received support of limbs specializedfor swimming, developmentof from both morphological(e.g. Bininda-Emonds& thick blubber or fur for thermoregulation,ability to Russell,1996;Wozencraft, 1989) and molecular (e.g. withstand prolonged apnea while diving through Ledje & Ârnason, I996a, b) evidence.Others have behavioural modifications (e.g. bradycardia), and foundodobenids and phocids to be moreclosely rela- dependenceon the ocean for most of their needs. ted (togetherconstituting the Phocomorpha),a result However, they lead an amphibious lifestyle in that

Taxon Age and Locality Basal Pinnipedimorphs Enalinrctos Late Oligocene - Early Miocene; easternand westem north Pacific Pteronacrtos Early Miocene; easternnorth Pacific

Otariidae Thalassoleon Late Miocene - Early Pliocene; eastem and western north Pacific

Phocoidea Acrophoca Late Miocene - Early Pliocene; easternsouth Pacific Allodesmus Middle Miocene - Late Miocene: easternand westem north Pacific Desmatophoca Early Miocene - Middle Miocene; eastem north Pacific Homiphoca Early Pliocene; easternand westem south Atlantic Pinnarctidion Early Miocene; easternnorth Pacific Piscophoca Early Pliocene; easternnorth Pacific Odobenidae Aivukus Late Miocene; easternnorth Pacific Alachtherium Early Pliocene - Early Pleistocene;eastem north Atlantic Dusignathus Late Miocene - Late Pliocene: easternnorth Pacific Gomphotaria Late Miocene; eastem north Pacific Imagotaria Late Miocene; eastem north Pacific Table 1. Summary Neotherium Middle Miocene; easternnorth Pacific ofknown ranges and ages Pontolis Late Miocene: easternnorth Pacific of fossil taxa included Protodobenus Early Pliocene; eastem north Pacific in this study. Valenictus Late Miocene - Late Pliocene; eastern north Pacific

85 ORYCTOS,YoL4,2002

they are still strongly tied to land (or ice), where bir- on benthicbivalves. Although many otariids,elephant thing, nursing, and moulting occur. The earliest seals,and the walrus will occasionallykill and eat known pinnipedimorphswere likewise well-adapted (often conspecific)pinnipeds or penguins(e.g. Brad- to life in the water,as Enaliarcloshas a skeletalmor- shawet al.,1998; Gentry& Johnson,1981; Harcourt, phology that is well suited for swimming (Berta & 1993;Hofmeyr& Bester,1993;Lowry & Fay, 1984), Ray, 1990).This, and the discoveryof distinctly pho- only the leopard seal is known to dependon warm- cid femorafrom older Late Oligocenedeposits of the bloodedprey as a regular food source(Hiruki et aL, easternUnited States(Koretsky & Sanders,in press) 1999; Sinitr & Stone, 1983).The willingnesswith stronglysuggest that pinnipedimorphsoriginated well which leopard seals approach and confront large before 29 Mya (million years ago). Regardless,a warm-bloodedprey is clearly illustrated in accounts marine-baseddiet has been hypothesized for all of close encountersof this species with humans known taxa including Enaliarctos (Berta & Ray, (Delacaet al.,1975). 1990),and therehas beenno suggestionthat any pin- Determining the diet of fossil vertebratesis far nipedimorphregularly fed or feedson terrestrialfood more problematicthan it is for extant taxa. However, resources.Prey capture, handling, and swallowing a numberof methodsallow for suchpredictions. First- occursin the water for all modernspecies. ly, observationon in situ fossilizedstomach contents The diet of living speciesis readily determined of a complete or nearly complete skeletonprovides throughdirect observation,stomach content analysis, the most direct and accuratemethod for predicting scat analysis, and a variety of other methods (see diet. Although this method has been used in some Bowen & Sinitr, 1999).Extant pinnipeds utilize many cases(e.9. see Currie et a1.,1995for hadrosaurs),the marinefood resources,which can be groupedinto the conditionsneeded to preservegut contentsin associa- five broad categoriesof: 1) fish, 2) cephalopodmo- tion with a skeletonare rarely met. A secondmethod llusks (squid and octopi), 3) bivalve mollusks (clams commonlyused to assessdiet is to cataloguepotential and kin), 4) small decapodcrustaceans (planktonic prey that occurin the samegeologic horizon and local- euphausidkrill and benthic shrimp), and 5) large ity as the predator.This method is undesirable,how- warm-blooded prey (including penguins and other ever,as carcasses of predatoror prey may be transport- seals).Pinnipeds show considerableoverlap in their ed prior to fossilizationand no direct correspondence utilization of these resources,and for some species betweenthe two can be assumed.Isotope analysis is a seasonal,sexual, ontogenetic, and geographicvaria- third methodfor diet assessment,and hasproven very tions in diet have been recorded (e.g. Dellinger & useful in determining whether basal whales fed in Trillmich, 1999;Fay,1982;Tollit et aI.,1998).How- freshwateror marinehabitats (e.g. Roe et a1.,1998). ever, somegeneral trends in diet can be identified, as However,the isotopemethod fails to indicatespecific revealedin fig. 1 (basedprimarily on King, 1983and prey taken by a predator and is thereforeof limited Riedman, 1990 and supplementedby: Daneri, 1996; utility in assessingthe precisediet of fossil taxa. A Fay, 1982; Fisher & Stewart, 1997; George-Nasci- founh method involves the analysesof microwear mentoet a1.,1985;Koen Alonso et a1.,1999;Lowry patternson teeth,and has proven useful in determining et al.,1980, 1988;Oritsland; 1977;Pinedo & Barros, the diets of other fossil carnivores(e.9. Van Valken- 1983;Rice, 1973; and Siniff & Stone,1983). Most burgh et al., 1990).Application of this techniqueto pinnipeds are piscivorous or teuthophagous(squid pinnipeds,however, fails to reveal probable diet as eating).Notable exceptionsinclude the Antarctic fur pinnipedsdo not masticatetheir food, and no correl- seal(Arctocephalus gazella), leopard seal(Hydrurga ation exists between striation morphology and leptonyx), and crabeaterseal (Inbodon carcinopha- (known) diet in modern taxa (Berta & Adam, unpu- gus), which feed extensively (or exclusively,in the blisheddata;but see Gordon (1984), who was ableto caseof Z. carcinophagzs)onAntarctic krrll(Euphau- predict tongue movementsin the walrus from tooth sia superba)and the beardedseal(Erignathus barba- striations). rzs) which feeds on small benthic crustaceansand The final and most commonly used method for bivalve mollusksin theArctic. The walrus (Odobenus inferring the diet of fossil taxa uses techniquesof rosmarus)is a specialistthat feedsalmost exclusively functionalmorphology and analogywith living forms. 86 ADAM & BERIA - EVOLUTIONOF PREYCAPTURE STRATEGIES AND DIET IN THE PINNIPEDIMORPHA

By examiningthe morphologyassociated with a par- tabl. 2. For brevity, descriptions of the feeding ticular method of capturing and handling prey in methodsand their associatedcharacters are presented living species,inferences of feeding behaviour and in the resultssection below, along with characterdis- diet can often be drawn for fossil taxa with similar tributions amongtaxa examined.In additionto pinni- morphologies(e.9. Van Valkenburgh 1989). Appli- peds,representative examples of the terrestrialcanoid cation of comparativemethods within a phylogenetic carnivore groups Canidae,Procyonidae, Mustelidae, framework also allows for more rigorous evaluation and Ursidaewere also includedfor comparison.Inso- of specific hypothesesof unpreservedtraits (e.g. be- far as was possible,we sampledtwo specimenseach haviour) derivedfrom preservedmorphology (Lauder of malesand females,and usedonly adult specimens 1995;Witmer 1995). [as judged from suture closure and developmentof Aquatic tetrapods,including pinnipeds,are large- secondary sexual characteristics(e.g. pronounced ly limited to using the headfor both prey captureand sagittalcrests)l as listed in tabl. 3. Although most cha- handling, as the forelimbs are typically modified for racters consisted of simple binary codings, others swimming (Tayloa 1987).Thus, the skull, teeth,and werederived from standardmeasurements of the skull mandiblesprovide the mostreliable indicators of feed- and dentaryas detailedin f,rg.2. In caseswhere origi- ing and diet in aquaticforms, and are the regions of nal fossilsor castscould not be observed,we relied on the body on which we have concentratedour efforts. published descriptionsand photographs(Barnes & We identified the major feeding behavioursof living Raschke,1991; Deméré,1994a, D; de Muizon,1981; pinnipedsand craniodentalfeatures and diets associa- de Muizon & Hendey,1980; Horikawa,1994; Kohno ted with these bahaviours.We then scored better et al., 1994;Repenning & Tedford, 1977). known fossil taxa for functional charactersin an In order to infer evolutionarypatterns and diver- attempt to deducethe feeding behaviourand diet of sity of feeding strategies,we employed a phylogen- extinct forms. However,as revealed below, there does etic framework. Unfortunately,no phylogeny produ- not appearto be a strong correlation betweenmor- ced to date includes complete samplesof fossil and phologiesconsistent with differentfeeding behaviours extant pinnipedimorphspecies (although we are pre- and diet in pinnipeds,as different methodsof capture sentlydeveloping such an analysis).ln lieu of this, we may be employedto obtainmany prey types. constructeda compositephylogeny of the pinnipedimorphs (fig. 1) basedon the framework of Berta & Wyss' (1994) morphologicalanalysis, which includes METHODS AND MATERHLS better known fossil taxa. Onto this framework we grafted more completeconsensus phylogenies of the We surveyed the literature to identify prey cap- extant Otariidaeand phocid subfamiliesMonachinae ture methodsemployed by modernpinnipeds, and esta- and Phocinae,as presentedby Bininda-Emondset al. blished functional charactersof the skull, mandibles, (1999). For the Odobenidae,we used Deméré's and teeth associatedwith each feeding type. The (1994a)phylogenetic analysis, but included one add- conditionof thesecharacters was then assessedfor all itional taxon, Protodobenzs,which we place incertae modernpinnipeds in addition to numerousfossil taxa sedisas the sistertaxon to Odobenusplus Valenicrus. for which adequatematerial was available.Museums This result is consistentwith preliminary analysesof from which specimenswere examinedare listed in our own data set (Adam & Berta,in preparation).

Abbreviation Museum Name Table2.Summary AMNH AmericanMuseum of Natural History (New York, New York) of museumnames LACM Los AngelesCounty Museumof Natural History (Los Angeles,California) and abbreviations. NMI\{H National Museumof Natural History (Washington,D.C.) NSMT National ScienceMuseum (Tokyo, Japan) SDI\IHM SanDiego Natural History Museum(San Diego, California) SDSU SanDiego StateUniversity Museumof Toology (SanDiego, California) UC}MZ University of CalgaryMuseum of Tnology (Calgary,Canada)

87 ORYCTOS,YoL.4.2002

Canivon Enalidntos I nercno?clos t Thalzssolan I Callorhinus ursinus Ttlophus cdifornianus Eumctopiæ iubotus Auiabyonia Phoardos hookqi Ncophou cincru -1jI Arctoæphalus pusillus A. tropbalis A. gazella G,,I A. townscndi A. philippii A. gabpagocnsis _4i A. lonlcri oustrulis Allodamus f Pinnarctidlon î Pinnipedid

Plscophou f trt Hydrurgo lqtonyx I Labodon stdnophdgus Izptonyholcs wcddclli OmmalophoÛ rosrl Mi rou nga angus rlrost rls M. Iconina Monachinae Monachus se;hauin slandl -\j tropialis M. monrchùs Erignalhus barbotus Cislophora cilstata Phou grochlandiu P, kscitrtl Halichoæus grypus Phou Ëtullns P. brgha P. slblriæ -1jI P. hispUa P. uspitz N@lhcrtum t Irrugotatla I KEYTOSYMBOLS I ?, caPS"lono.t = lish -l= Prototlobenus I =o-rurrroseats =crustaoerns Valenlclus t { ô = bivalvemollusks = unknown I | -

Figure 1. Composite phylogeny derived from Berta & Wyss (1994),Bininda-Emonds et aI. (lggg),and Deméré (199a@. Primary diets of extant taxa are indicated to the right by symbols representingfrsh, cephalopods,bivalve mollusks, crustaceans, and penguins/seals(see key). f denotesfossil taxa.

Due to the hybrid natureof our phylogeny,branch observedmorphological changes associated with dif- and tree strength indices (e.g. bootstrap and jack- ferent feedingbehaviours occur at either more or less knife values and tree consistencyindices) could not inclusivelevels of the phylogenetichypothesis used be calculated.With respectto the two major contro- here.As a result, our observationsare not affectedby versiesover pinnipedinternal relationships(i.e. point the contrastingopinions held for either basal pinni- of origin within arctoid carnivoresand relationships ped affinities or odobenid-phocid-otariidrelation- of walrusesto phocidsor otariids),however, all of the ships.

88 ADAM & BERIA - EVOLUTION OF PREY CAPTURE STRATEGIES AND DIET IN THE PINNIPEDIMORPHA

Group Species Specimensexamined

Terrestrial Canislatrans NMNH 250483,250484.551009.551042 carnivores Procyonlotor NMNH 360771,360782,360783,507418 Lutracanadensis NMNH 127606,131449,136746,136747 Ursusmaritimus NMNH 512105,512108,5l2lll,5l2tt2 Basal Enaliarctosemlongi T NMNH 250345,314290,314540 pinnipedimorphs Pteronarctosgoedertae I LACM 5058/123083*;NMNH 167648,2062i4,250282,250320,335432 Otariidae Arctocephalusaustralis NMNH 484934,484936,484937,50lll9,504900 A.forsteri NMNH 396062,396921,504891,550479,550480 A. galapagoensis NMNH 259790,259832 A. gazella NMNH 392266a,392266b A. philippi SDMNH21550 A. pusillus LACM 52231;NMNH 34902,484928 A. townsendi NMNH 83618,395886 A. tropicalis NMNH 550090,550091 Callorhinusursinus NMNH 286145,286149,286152,286269,286270 Eumetopiasjubatus NMNH 13217,14507,21073,21302,21309,2'709'70,276031,276040; SDNHM23174 Neophocacinerea NMNH 484832,504729,571463;UCMZ1994.001 Otaria byronia NMNH 23240,484912,50lll4, 55022j: SDNHM 233,14 Phocarctoshookeri NMNH 3M983,344985,395143,484526,848531 hlophus califurnianus NMNH 16296;SDSU 1010, 5-597, uncatalogued Thalassoleonmexicanus f NMNH 215020* Phocoidea Cystophoracristata NMNH 188909,188911, 188914, 188915, 188927, 188931 Erignathusbarbatus NMNH 230954,290657 , 500249,500250, 50025 I , 5504I I Halichoerusgrypus NMNH 19837,35291,504211,50429'l Hydrurga leptonyx NMNH 270326 , 275208 , 275245 , 396931, 57 1676 lzptonychotesweddelli NMNH269528,269529,269530,395810,504875,550074 Lobodoncarcinophagus NMNH269531,296532,275204,550080,550083 Miroungaangustirostris NMNH38234,20927,21895,260867 M.leonina NMNH 15336.20927.241199.484893 Monachusmonachus AMNH 73607,73608;NMNH 23250,219059 M. schauinslandi NMNH 243839,243840,243849,334574,334577,395999 M. tropicalis NMNH 100361,102523,102533,102534 Ommatophocarossi NMNH 270321,275206,302975,339989 Phocacaspica NMNH 341615,341616,341617 P.fasciata NMNH 22915,311'77t,399449,504959, 571867 P.groenlandica NMNH 99436,188766, 188769, 188766, 188773,188775 P.hispida NMNH 16136,225766,225767,225'781,225794,305090 P.largha NSMT29056,29066,29067,29069 P sibirica NMNH 175689,175690,550028,550030, 550034 P vitulina NMNH 504085,504110, 504298,550044,55004'l Acrophocalongirostris T NMNH 360407*,421632 Allodesmuskernensis T I-ACiNl127939* Desmatophocabrachycephala T MUNH 120199* Pinnarctidion rayi t NMNH 250321 Piscophocapacifica I NMNH 360406* Odobenidae Odobenusrosmarus NMNH 21331,22014.22104 Aivukuscedroensis I NMNH 215019* Dusignathusseftoni J SDNHM 38342 Imagotariadownsit tttvtNH 13487,175349* Pontolismagnus T NMNH 3792 Protodobenusjaponicus I NMNH 140726* ValenictuschulavistensisT SDNHM36786,38228,63026,63237

Table3. List of specimensexamined in this study.Museum abbreviations are defined in Table2. T denotesfossil taxa, * indicatescast specimens. 89 ORYCTOS.YoI.4.2002

Taxon Pierce Feeding Suction Feeding Filter Feeding Grip & Tear Feeding

Pl P2 P3 P4 P5 51 52 53 54 55 56 Fl F2 F3 F4 Gl G2 Canidae 00000 0000000000 00 Mustelidae 00001 0000000000 00 Procyonidae 00000 0100000000 00 Ursidae 00000 0000000000 00 Basal Pinnipedimorphs Enaliarctos t tl0ll 0000000000 00 Pteronarclos I tl01l 0000?00000 00 Otariidae Arctocephalusaustralis I I I I I 0000 00000 00 A. forsteri lllll 0000 00000 00 A.galapagoensis I I I I I 0000 00000 00 A. gazella rllll 0000 00000 00 A. towndsendi lllll 0000 00000 00 A. tropicalis lllll 0000 00000 00 A. philippii lll1l 0000 00000 00 A. pusillus llllt 0000 00000 00 Callorhinusursinus I I 1 I I 0000 00000 00 Eumetopiasjubatus I 1 I I I 1000 00000 00 Neophocacinerea I I I I I 1000 00000 00 Otaria byronia lllll 2tl0 00000 00 Phocarctoshookeri I I I I I 1000 00000 00 Zalophuscalifurnianus I I I 1 1 0000 00000 00 Thalassoleon I lllll 0000 00000 00 Phocoidea Cystophoracristata 1 I I I I 000 I 2 00000 00 Erignathusbarbatus I I I I I 301 0 I 00000 00 Halichoerusgrypus I I I I I 000 0 I 00000 00 Hydrurgaleptonyx I I I I I 000 I 00110 ll lnbodoncarcinophagus I I I I 1 000 I 0llll 00 Miroungaangustirostris I I 1 I I 000 2 00000 00 M. leonina ll1lr 000 2 00000 00 Monachusmonachus I I I I 1 000 00000 00 M.schauinslandi I I I I I 000 00000 00 M. tropicalis lllll 000 00000 00 Omrnatophocarossii I I I I I 000 00000 00 Phoca caspica lll1l 000 0 00000 00 P. fasciata llllt 000 0 00000 00 P. groenlandica ltlll 000 0 00000 00 P hispida lltll 000 0 00000 00 P. largha lltll 000 0 00000 00 P. sibirica ltlll 000 0 00000 00 P. vitulina 11111 000 0 00000 00 Acrophoca J 11111 000 I 00100 00 Allodesmus I lrllt 012 0 00000 00 DesmatophocaT I I I I I 000 0 00000 00 Homiphoca f ltllt 000 I 00000 00 Pinnarctidion I l?ll1 000 0 ?0000 00 Piscophoca t tlllt 0?? I i 00000 00 Odobenidae Odobenus rosmarus l0 tor2lt23l 0000 00 Aivukus J 1? tlt10?1?00000 00 Alachtherium I 101 2111100000 00 Dusignathus I 111 10?121 0000 00 Gomphotaria I lll 1102300000 00 Imagotaria I l 1 r I 0 0 oltt 0 0 0 0 0 00 Neotherium t r?l 0000?00000 00 Pontolis f 1?1 1000200000 00 Prolodobenus I 10tll?0100000 00 ValenictusI ?2 ?0r2ll33l 0000 00

Table 4. Summary matrix of codings for characters associatedwith different pinnipedimolph feeding strategies.Numerical codings (0-3) representcharacter statesdescribed in the text. Unknown character statesare indicated by a question mark (?). t denotesfossil taxa. ADAM & BERTA - EVOLUTIONOF PREYCAPTTJRE STRATEGIES AND DIET IN TTIEPINNIPEDMORPHA

RESULTS facets.(0=yes,1=no) Within the Carnivora, the carnassialdentition Feeding Strategies (fourth upperpremolar, FB, and lower first molar,M1) is typically modified to form a cutting (e.g. most Methods by which aquatic vertebratescapture felids and mustelids)or crushing(e.g. ursids) surface, and handle prey have been reviewed in Taylor or a combination of these (e.9. canids). When in (1987),and most recentlyby Werth (2000a)for mari- occlusion, opposingteeth meet each other and form ne mammals. From these works and our literature distinct shearingor grinding surfaces.In a non-mas- survey,we identified four generalfeeding behaviours ticatory, pierce feeding strategy,opposing teeth do usedby pinnipedimorphsto secureand processprey. not meet at occlusion and no distinct occlusal wear These are: I) pierce, II) suction, III) filter, and IV) facetsare present. We scoredthe presence(state 0) or grip and tear feeding.Descriptions of thesestrategies absence(state 1) of occlusalwear facetson postcan- and the morphologiesassociated with eachare given ine teeth for this character.Precise occlusion of the below. We assignedan alpha-numericcode to each postcanineteeth occurs only in terrestrial carnivo- functional characterassociated with a particularfeeding rans. As noted by Berta (l98la, b), however, both type, with P, S, F, and G representingeach of the four Enaliarctos andPteronarctos have a well developed feeding strategiesdescribed above, respectively. paraconeand metaconeon P, in addition to distinct Table4 summarizesour observationsand codingsfor wear facetson the carnassialset. The remainingpost- thesecharacters. canine teeth, however, do not bear distinct occlusal wear facets. We thus scored these basal pinnipedi- I. Pierce Feeding. Masticationinvolves the mechan- morphs with derived state 1, but recognizethat they ical breakdownof bite-size items of food into smal- more likely representan intermediatestage in the loss ler piecesthat canbe more readily swallowedcoupled of precisepostcanine masticatory efficiency. Of addi- with the beginning of chemicaldigestion by salivary tional note is that in extant otariid taxa, occlusionof juices. Modern pinnipedsdo not orally processtheir the posteriorteeth is so imprecisethat posteriorlower prey, but insteadtypically (as with most other marine postcanineslie labial to the upperswhen the jaws are tetrapods)hunt prey that they can swallow whole in occlusion. To the best of our knowledge, this (Taylor,1987; Werth,2000a). The ability to mastic- condition has not been noted before for otariids and ate is therefore primitive for arctoid carnivores,as is not found in any other mammaliangroup. The odo- exemplified by the Canidae,Mustelidae, Procyoni- benine Valenictuswas scored as unknown for this dae, and Ursidae.In contrast,most aquatictetrapods characteras it lacks postcanineteeth. utilize a piercing bite, where prey are capturedin the mouth and held in place by (usually) small, sharp P2. Location of M1 on dentary. (0 = at approxi- teeth.Below we identify threecharacters (P1-P3) that mate midpoint of dentary length, l. = anterior to are typically found within the Carnivora and which midpoint of dentary length) can be used to differentiate between the primitive Greaves(1983, 2000) proposed a modelwherein masticatory feeding strategy (state 0 for characters he predictedthat in carnivorans,the most beneficial P1-P3) and the derived piercing strategy(state I for trade-off betweenmaximum gape and maximal bite charactersPl-P3). Furthermore,the pursuit of prey force at the carnassialset will occur when the lower under water requiresadaptation of the specialsenses carnassial(M1) is locatedat a position that is less to allow for prey detection. Charactersassociated than 60Voof the distancefrom the mandibular con- with thesechanges are also presentedbelow (P4-P5) dyle to the anteriortip of the dentary.According to his as indicative of the terrestrial-aquatictransition. We model, to increasebite force the carnassialsshould be assumethat the derived condition of theselatter cha- positionedcloser (i.e. <6OVo)to the jaw joint. To ractersis indicatiVeof under water hunting and swa- increasegape while still maintaining maximal bite llowing of whole prey, and by corollary non-mastic- force, Greaves (2000) predicted that a carnivore atory pierce feeding.These characters,are : shouldbecome larger. Although not addressedby his Pl. Postcanine teeth with distinct occlusal wear model, it can be assumedthat if freed from bite force 9l ORYCTOS.Yol.4.2002 constraints,a carnivorancould also increaseeffective carnassial gape by positioning these teeth farther anterior along the dentary length without a need to increaseoverall size.A loss of masticatoryability at the carnassialdentition, therefore, would be indicated by an anteriormigration of M1. Our observedratio of MMIL/DL (flig. 2) revealed that among examined terrestrial carnivores,all specieshad M1 positioned approximatelyat or posterior to the midpoint of the greatestlength of the dentary(state 0). In contrast,all pinnipedimorphs with the exception of the walrus had the M1 positioned well anterior to the midpoint Mr Pr Ps PzPr of the dentarylength (statel; fig.3). Pinnarctidion, Aivukus,andValenictus wete coded as unknowndue to the absenceof M1 or absenceof well preserved mandibles.

Figure 3. Lateral view of right dentaries of (A) a coyote (Canis latrans), (B) Enaliarctos mealsi, (C) Pteronarctos goedertae, (D) California sea lion (hlophus califurnianus), and (E) harbour seal (Phoca vitulina\, scaled to the same size. The dark vertical line represents the midpoint of the dentary length (DL), and premolars (P1-f and molars (M1-3) are labeled (P1 and P3 not preserved in (B)). Note that M1 (darkened)is positioned anterior to the midpoint in all pinnipedimorphs (B-E) (characterP2).

<_ Figure 2. Pictorial summary of standard measurements taken from skulls and mandibles. Pictured is the skull and lower jaw of a bearded seal, Erignathus barbatus. From top to bottom: skull, left lateral view; left dentary, lateral view; skull, venhal view. CBl;condy- lobasal length; Dl=dentary length; MMll=distance of M1 from mandibular condyle; Ol=orbit length (measured as the greatest distance between the tip of the postorbital process and the anterodorsal rim of the orbit); Pl=palate length. 92 ADAM & BERIA - EVOLUTIONOF PREYCAPTURE STRATEGIES AND DIET IN THE PINNIPEDIMORPHA

P3. Condition of postcanine teeth. clade examinedhere. Insufficient material precluded (0 = premolars and molars differentiated, assessmentof orbit size in Neotheriumand Pontolis. I = postcanine teeth homodont) The correspondencebetween homodonty and P5. Infraorbital foramen. pierce feedinghas beenwell established,with homo- (0 = unenlarged, I = enlarged) donty characterizingmost secondarilymarine verte- Berta & Wyss (1994) found that an enlarged brates(Taylor, 1987; Werth,2000a).In the primitive infraorbital canal is synapomorphicfor the Pinnipe- condition (state0), molarsand premolarsare well dif- dimorpha. However, the trend towards a large ferentiated and each tooth contributes differently to infraorbital canalis widespreadamong aquatic mam- the masticatorybreakdown of a bolus. Among taxa mals (Dehnhardt et al., 1999). Although not well exhibiting homodonty,the premolarsand molars are understood,it is believedthat the mystacialvibrissae, similarly shapedand simply usedto seizeand cripple which are innervatedby the maxillary branch of the prey prior to being swallowedwhole (state1). The ter- trigeminal nerve passing through the infraorbtal restrial carnivores examined here, plus Enaliarctos canal, act in monitoring the fluid environment of andPteronarctos, ate characteized by state0, where- aquatic mammals (Ashton & Oxnard 1958; Dehn- as all later pinnipedshave homodont dentition (un- hardt et al., 1999). Tactile sensitivity studiesof the known inValenictus). vibrissaeof captive pinnipedsindicate that they are exceptionallysensitive (e.9. Kastelein& van Gaalen, P4. Orbit size. (0 = unenlarg€d, 1 = enlarged) 1988;Kastelein et al.,1990), andit hasbeen sugges- Under water, the amount of light availablefor a ted that pinniped vibrissaeplay an important role in predatorto visually detectevasive prey drops drama- detectingprey movementsimmediately prior to cap- tically. In responseto low light levels, a number of ture (Renouf, 1980). The ability of harbour seals marinepredators (e.9. ichthyosaurs) have enlarged the (Phoca vitulina) to detect water eddies left by eyes relative to their terrestrialcounterparts (Motani moving objectswith their vibrissaehas only recently et al.,1999). Largereyes enable these predators to col- beendemonstrated (Dehnhardt et a1.,2001).Pending lect more of the availablelight by photoreceptivecells a more thoroughunderstanding of vibrissaeand how of the retina.Motani et al. (1999) note, however,that they are used during prey capture in an aquatic eye sizealso increases with greaterdependence of the medium, we here interpret a large infraorbital canal visual systemin detectingprey. Terrestrial camivorans to reflect an enlargedmaxillary branch of the trige- dependlargely on vision in detectingtheir prey and minal nerve innervatingthe vibrissal pads.Increased typically have binocular vision with overlappingleft vibrissal innervationis, in turn, indicativeof taxa that and right fields of view. Pinnipedsalso detect prey have completedthe transition from land to water and using visual cues,although overlapping fields of view which likely pursuedevasive prey underwater. Enlar- tend to be situatedmore dorsally than in terrestrial ged canalsare indicatedby both an increasein size carnivorans(Hobson, 1966). Given that both terres- and by the anterioropening of the canal on the zygo- trial carnivores and pinnipeds use visual cues and matic arch (state 1). Unenlargedinfraorbital forami- binocularity to detect prey, any difference in eye size na are smaller,with their anterioropening located on is likely to reflect an adaptationto lower light levels the rostrum, and are indicative of prey pursuit and under water.Among our sample,terrestrial carnivores captureon land (state0). Among our sampletaxa, all havemaximum orbit sizes(OL, frg.2) thatrangefrom pinnipedimorphsplus the mustelidLuta are charac- l3-I8Voof condylobasallength (CBL, fie.2) (state0) teized, by enlargedinfraorbital foramina. whereasin pinnipedimorphsthis ratio rangesfrom 21- 33Vo(state 1), with exceptionof the group of odobe- II. Suction feeding. In a fluid environment, the nine walrusesAlachtherium, Valenictus,Protodobe- simple act of openingof the jaws createslow press- nus, and Odobenus(fig. 4). Similar differenceswere ure inside of the oral cavity relative to the environ- observedfor absolute orbit size, and we believe that ment, and water moves into the mouth due to the potential effects of eye size scaling negatively with pressure differential. The ability to generate suction body size (Motani et al., 1999) are negligible for the has been observedfor severalpinnipeds, such as the 93 ORYCTOS,Yot.4.2002 crabeater seal (Lobodon carcinophagus;Klages & Cockcroft, 1990). Suction forces generatedby most taxa appearto be rather small and functional only at Orblt Length Palate Lengûh short distances,however, and it is questionablewhe- oL/cBL (%) PL/CBL (o/") ther or not they are sufficient to capturelarge mobile prey such as fish and squid. Crabeaterseals may be Canidac a Must.lldac t able to use their limited suction to capturemultiple Procyonldac small planktonickrill on which they feed, althoughin Ureldac I Enallarctos the wild they appearto take single prey with simple I ! Ptcronerctost. ! biting motions(Kooyman, 1981). Although long sus- Thalecsolænt ! pected (Fay, 1982; Gordon, 1984), the direct use of Cellorhlnus urslnug I iZaloph ua êet llonl enu I I suction to capture and consumeprey by a pinniped Eumatople' lubatug I Ohrla byronla has only been recently demonstratedfor the walrus Phocarctoo hookcri a by Kastelein and colleagues(Kastelein & Mosterd Ncophæa clncrca I Arctoccphcl us pu cl II uc I 1989;Kastelein et aL, 1994).The walrus is able to A. troplcallc I A. gazclla producean impressive-118.8 kPa of oral pressure I A. townccndl I under water and -87.9 kPa in air (Kasteleinet aL, A. phlttpplt a A. galapagocnalc I I 1994).Suction feeding has alsobeen demonstrated in A.lorstad I I ziphiid (Heyning & Mead, 1996) and globicephalid A. tustr'/tlt I I Allodccmucl I (Werth, 2000a,b) odontocetecetaceans and the mys- Plnnarcfldlon I ! I Dcematophocal I ticete gray whale (Eschrichtius (Werth, I robustus) Acrophoca t I I 2O0Oa).There are numerousskeletal characters asso- Homlphocal I a Placophocat ? ciated with producing large suction forces with the HNruryâ loptonyx a mouth (below), and analogousmodifications of the Lobodon carclnophcgue t Laptonychotc. waddcill T I skull are seen in many suction feeding taxa. For Ommalophoca rossl I Mhoung â angu ctlroctrl e I ! example,suction feeding has been predictedfor the ll. lconlna I I Mon ac hua cc haul nslandI I I Pliocene cetacean Odobenocetops,which displays N. troplcalla I I remarkable convergencein skull morphology with n. montchus I I Erlgnathus barbatus I the modernwalrus (de Muizon,I993a, b; de Muizon Cyctophora cdsttt a a Phoca grocnlandlca et al.,1999). I I P, leeclata I Descriptions of the mechanics and functional H.llchocrus grypuE I I Phoca vltullna I I morphology of suction feeding in the walrus are P.,',rght I I P. slblrlca I I given in Gordon (1984) and Kasteleinet aI. (1991, P. hlcplda I ! 1994, 1997), and are summarizedas follows: once a P. cacplca T I Ncoth.rlumt I walrus has exhumed its bivalve prey using a jet of lmagotarlat I water followed by vibrissal inspection(Kastelein & Dutlgnathus t Pon|,otlst Mosterd, 1989), the whole bivalve is positionedbe- Gomp,holerlal tween the gum and upper lip. The tongue is pressed Alvukucl Alachthcrlumt against the hard palate and the lips pressedtightly Protodoænust Valcnlctus t against each other. The walrus then retracts its Odobcnus roamerua tongue, generatingnegative inffaoral pressure.The foot, body, and siphon are torn from the shells and swallowed.The shell, plus any soft remains,are not ingestedand simply dropped.These observations are consistentwith the general absenceof shells in the Figure 4. Chart showing the range of values obtained for orbit size (OL/CBL; character P4) and palate length (PLICBL; character S2). stomachsof wild walrus (Fay, 1982). Unknown values are indicated by question marks (?). Vertical solid lines depict threshold values used to define character states (see text).

94 ADAM & BERTA - EVOLUTON OF PREYCAPTURE STRATEGIES AND DIET IN TTIEPINNIPEDIMORPHA

Although early authorsassumed that the tusks of 52. Lengthening of hard palate. walrusesplayed a role in the excavationof benthic (0=absentrl=present) mollusks (seereferences in Fay,1982), observations As noted above,large intraoral pressurechanges on live animalsindicate that the tusks are not usedin are generatedin suctionfeeders. Kastelein & Gerrits prey capture(Fay,1982; Kastelein & Mosterd,1989; (1990) postulated that in order to cope with these Kastelein & Gerrits, 1990). Rather,the enlargedca- pressures,the hard palate of the walrus is extended nine tusksof Odobenusand (presumably)other fossil posteriorly. Posterior expansion of the hard palate walrusesare usedduring intraspecificbattles to esta- necessarilyreplaces part of the soft palate, a struct- blish dominancehierarchies (Miller, 1975) and on ure that is likely insufficiently constructedfor coping occasionto gain purchaseon slipperyice (Fay, 1982). with large intraoral pressurechanges. In most taxa We thereforeexclude any characterspertaining to the examinedhere, palatal length (PL, fig. 2) is lessthan use of tusks in feeding. Characters(51-56) funct- 65Voof CBL. Numeroustaxa, however,stand out in ionally associatedwith suctionfeeding are : having a palatal length greaterthan 65VoCBL (state 1) (fig. 4) : l) Alachtherium,Odobenus rosmerus, S1. Vaulting of hard palate. (0 = palate relatively Protodobenus, and Valenictus among odobenines, flat, 1 = palate transversely arched, 2 - palate 2) the dusignathine Gomphotaria, 3) Allodesmus transversely and longitudinally archedr 3 - palate amongphocoids, and 4) Otaria amongotariids. State flat but with raised maxillary alveolar processes) 1 also characteizesProcyon lotor.This omnivorous In most terrestrial carnivores and pinnipedi- species,however, is not predictedto havesuction fed, morphs,the hardpalate is flat (state0). The walrus,in as it does not capture food underwater with the contrast,has a palatethat is concavedorsally in both mouth. The posterior palatal extension seen in its transverseand longitudinal planes(state 2). Presum- skull may indicatepalatal strengthening to accommo- ably, this >provides greaterintraoral space date torsional forces acting on the rostrum resulting and presentsthe tongue with an extendedspace in from masticationof hard food items. which it can be protractedprior to being retractedto produce suction (Kastelein and Gerrits, 1990). This 53. Condition of pterygoid hamuli. additionalspace would allow for greatersuction force (0 = weakly developed, 1 = robust and knob-like) to be generatedrelative to a flat palate.A similar vaul- In associationwith the large intraoral pressure ting in both transverseand longitudinal planes is changes generated during suction, the pterygoid observedin the odobeninesAlachtherium and VaIe- hamuli of the walrus skull havealso become enlarged nictus, as well as the southernsea lion, Otaria. As (Deméré, 1994a; Kastelein & Gerrits, 1990; fig. 5). recognizedby Deméré (I994a), in someodobenines Normally, these structures are thin and blade-like (Aivukus, Dusignathus, Gomphotaria, Imagotaria, (state0), but in the odobenidsAlachtherium, Odobe- Pontolis, and Protodobenus)and otariids (Eumeto- nus,andValenictus plus the southernsea lion (Otaria pias, Neophoca,and Phocarctos)the palate is trans- byronia) and beardedseal, the hamuli are enlarged versely,but not longitudinally,concave (state 1). We and knob-like. Kastelein et al. (1991) consider this proposethat this representsan intermediatecondition enlargementto be correlated with strong develop- in the evolution of suctionfeeding, although a lack of ment of the m. velumpalatini in the walrus, which is information on the suctionabilities of thesetaxa pre- the primary supportingmuscle of the (reduced)soft cludesconfirmation of this. We alsorecognize a third palate.Enlargement of this muscle (and the hamuli) condition as representedin the beardedseal (Erigna- is assumedto be relatedto reinforcing the soft palate thus barbatus),in which althoughthe palateis relat- for large intraoral pressurechanges during suction ively flat, the maxillary alveolarprocessesare enlarged feeding. The shapeof the hamuli is unknown in the and give the ventralrosffal surfacea concaveappear- odobenidsProtodobenus (contra Horikawa, 1994), ancein transversesection (state 3). The ridge formed Aivukus, and Dusignathus,as well as the phocoids by these alveolar processesmay act in a similar Allodesmus andP isc opho c a. fashionto the concavemoulding of the palatein taxa characterizedby state1.

95 ORYCTOS.YoI.4.2002

characteristicsif it is to be interpretedas being indicative of suction feeding.Although the retention of an ancestralnumber of incisors(state 0) is charac- teristic of terrestrial carnivores, basal pinnipedimorphs,and otariids,incisor loss is a commonfea- ture amongphocomorphs. The lossof a singleupper incisor (state1) is found in monachinephocids and the phocine Cystophora cristata (hooded seal), as well asin the fossilphocids Acrophoca, Homiphoca, and Piscophoca.State 1 also characteizesthe odobenid generaAivukus, Alachtherium, Dusignathus, andImagotarla [multistatewith state0, after Demé- ré (1994a)1.The loss of two upperincisors (state 2) is found only in the dusignathinewalrus Gomphota- ria andthe modernwalrus. A completeloss of upper incisors(state 3) is found in the odobenineValenic- tus.

55. Number of lower incisors (per quadrant). (0 = three, 1 = twor 2 = orru.-3= none) As with the precedingcharacter, a loss of inci- sorsin the lower jaw is associatedwith the free passageof food from the areaof the gum and lip to the mouth during suction,and not with the generationof suction.Retention of all three incisors (state0) is found in terrestrial carnivoransand the basal pinni- pedimorphEnaliarctos. The loss of a singleincisor (state 1) characteizesliving and extinct otariids and phocoids, with the exception of the elephant Figure 5. Ventral view of the skull of a modern suction-feeding wal- (Mirounga) and hooded (Cystophoracristata) seals rus (Odobenus rosmarus) showing robust pterygoid hamuli (arrows; which havelost two lower incisors(state 2). Among character S3). the odobenidsexamined here, Alachtherium, Imago- taria, and Protodobenzshave lost a single lower incisor,Dusignathus and Pontolis have lost two, and 54. Number of upper incisors (per quadrant). Gomphotaria, Odobenus, and Valenictushave lost (0 = three, 1 = twor 2 = orrï3 = none) all lower incisors(state 3). The numberof lower inci- Kastelein& Mosterd(1989) report that walruses sorsis unknown fot Enaliarctos andPteronarctos, as extract their bivalve prey from the shellsby placing well as for Pinnarctidion and the fossil odobenids it between the upper lip and gum prior to lingual Aivukus andNeotherium (Deméré. 1994a). retraction.As the tongueis retracted,the soft partsof the mollusk are drawn into the mouth (which is typi- 56. Condition of mandibular symphysis. cally in occlusionduring suction).A loss of incisor (0 = dentaries not ankylosed, teethin thejaws is likely an adaptivefeature to allow 1 = dentaries ankylosed) the free passageof these soft items into the mouth Scapino(1981) developeda methodfor classi- from the area of the upper gum and labium, where fying the rigidity of the mandibular symphysesin the shellis secured.As discussedbelow. incisor loss carnivores, and attempted to correlate symphyseal does not contribute to the generationof suctionper structurewith torsional forces acting upon the lower se, and this charactermust be associatedwith other jaw during feeding.Although not addressedin his 96 ADAM & BERTA - EVOLUTIONOF PREYCAPTURE STRATEGIES AND DIET IN TI{E PINMPEDIMORPHA paper,the enlargedlingual musclesoriginating from predictedthat crabeaterseals were able to filter feed lowerjaws of the walrus(Gordon, 1984;Kasteleinet basedon numerousaspects of their jaws and skull, as al., 1997) would likely causeconsiderable torsional describedbelow. Mitchell (1989) noted similar mor- forces to be experiencedby the mandibles during phological featuresin the toothedmysticete Llanoce- suction feeding.Assuming a similar responseto tor- tus denticrenatus,and predicted that it may havebeen sion in terrestrialcarnivores and pinnipeds,we coded an efficient filter feeder. two statesaccording to whetherthe mandibularsym- physis was completely ankylosed (state 1) or not Fl. Postcanine tooth cuspation. (0 = cusps absent (state 0). In the unfused state,the mandibular sym- or not latticeJike, I = cusps lattice-like) physes are relatively flexible and, in our opinion, Among mammals,the postcaninedentition of the might becomedeformed by forces generatedby the crabeaterseal is unique in that each tooth bears 3-5 lingual musculatureduring tongue retraction. With long, distinct and posteriorly bent cusps (fig. 6A). time, such deformationwould likely result in consi- The teeth appearto be quite delicate, and in lateral derable wear on occluding teeth and render them view each tooth is lattice-like, the form of which inefficient at food capture and perhapsmake them would effectively allow the passageof water but not prone to developingpathologies. A more solid foun- of prey any larger than a couple of millimeters in dation would be provided if lingual musculatureatta- length (King, 1961; state 1). In other pinnipeds, ched to fused dentaries,a condition that would allow althoughdistinct cuspsare often present(e.g. among little or no mandibular deformation accompanying phocines),none bears the long sieve-likeprocesses of tongue retraction during suction feeding. A fused Lobodon. mandibular symphysis is therefore associatedwith suction feeding, as is an overall increase in the robustnessof the mandibles (Kastelein & Gerrits, 1990).Among our sampledpinnipedimorphs, only the odobenines Odobenus and Valenictus and the dusignathineDusignathzs have a fused mandibular symphysis.Among outgrouptaxa, only the polar bear (Ursus maritimus) has fused mandibles.This latter taxon feedson seals,and may require additionalrein- forcement of the lower jaw to cope with potentially large, strugglingprey.

III. Filter feeding. The ability to filter feed by any marine mammal is remarkable,as the flow of water through the mouth is bidirectional, meaning that -\-*'._._-_, _ water enteringthe oral cavity throughthe mouth must alsobe expelledout throughthe mouth.Filter feeding is bestknown in baleenwhales, which usually take in large mouthfuls of water and prey, and expel water Figure 6. Left lateral view of the dentary of (A) a crabeater seal via protraction of the tongue as prey items are trap- (htbodon carcinophagus) showing the unique cusp pattern (charac- ped on the inner surfaceof the baleen.In the balae- ter F3) and post-dental ridge (arrow; character F4) associatedwith nids (right (Eubalaenasp.) and bowhead(Balaena filter feeding, and (B) a leopard seal (Hydrurga leptonyx) showing mysticetus)whales), a unidirectionalflow of water is the enlarged incisors (compare with A; character Gl) and sharply accomplished by maintaining an open gape and pointed cusps of the postcanine dentition (character G2) associated swimming slowly through the water (Werth, 2000a). with grip and tear feeding. Among pinnipeds,the ability to filter feed has only beendemonstrated in captivecrabeater seals (Klages & Cockcroft, 1990). Previously,King (1961) had

97 ORYCTOS,Yot.4,2002

F2. Postcanine tooth interdigitation. only the killer whale (Orcinus orca) andleopardseal = (0 not or only slightly interdigitating, (Hydrurga leptonyx) regularly feed on, and are I = strongly interdigitating) capableof dismembering,large prey (Werth, 2000a). In addition to the lattice-like appearanceof indi- In the killer whale, the carcassof a large prey item vidual teeth in crabeaterseals (characterF1), King may be torn apart with coordinatedefforts of two or (1961) also notes that when the mouth is closed, more individuals, pressed against the substrateto upper and lower teeth interdigitatein sucha way that hold the carcasswhile swallowablechunks are torn only very small gaps penetratebetween the cheek off, or similarly sized pieces may be removed by teeth (state 1). Thus, both individual teeth (character biting and shakingmovements of the head(Guinet e/ Fl) and their occlusalinteraction preclude the escape a1.,2000;Werth, 2000a).Leopard seals appear to uti- of small prey from within the oral cavity while water lize only the last of thesetechniques. When feeding is being expelled.Precise interdigitation of upper and on another seal or penguin, the leopard seal grasps lower postcanineteeth is alsoobserved in the leopard onto the prey item at the water surfaceof and, sha- seal(Hydrurga leptonyx)as well as the fossil phocid king its head from side to side, tears off bite size Acrophoca. In contrast, among other pinnipedi- piecesof fat and skin (Hiruki et al., 1999:Werth. morphs the teeth either occludeor, if they interdigit- 2000a). ate,large gapsexist betweenthe teeth through which small prey would likely escape(state 0). Gl. Enlarged incisors. 0 = absent, I = present and not procumbent. F3. Height of postcanine teeth. As might be expectedof an animal that dismem- (0 = low crowned, I = high crowned) bers prey by gripping the skin and blubber with the In order to prevent prey escape,the postcanine anteriordentition and shakingits head,the incisorsof teethof a filter feedingpinniped (e.g.Lobodon) must the leopard seal are unusuallyrobust and caniniform be high crownedsuch that the apexof the tooth close- (fig. 6B; state1). In mostother pinnipedimorphs, the ly approachesthe gingivum of the opposingjaw in incisors are small and of a size comparableto terres- occlusion.The postcaninesof the crabeaterand leo- trial carnivorans(state 0). One exceptionis the Wed- pard sealsare markedly high crowned (state l) relat- dell seal (Leptonychotesweddel/i), which has enlar- ive to the low crowned teeth of other pinnipedi- ged, procumbent, and caniniform incisors that are morphs and terrestrialcarnivores (state 0). used to crack ice that forms over breathing holes (Stirling, 1969). We consider the procumbency of F4. Post-toothrow processes. these teeth to render them inefficient as gripping (0=absentrl=present) teeth,and thereforegroup enlarged,but procumbent, An additional feature of the crabeaterseal fee- incisors with unenlargedincisors (this categorization ding apparatusis the presenceof conspicuouspost- is made with respectto feeding behaviouronly - we dentalridges on the maxillaand dentary (King, 1961; recognizethat large, procumbentincisors are clearly fig. 6A; state1). In occlusion,these ridges interdigi- autapomorphicin L. weddelli with respectto phylo- tate in a manner similar to that describedabove for geneticcharacter transformation). the teeth (characterF3), and likely act in preventing prey escape through the edentulous angle of the G2. Shape of postcanine tooth cusps. 0 = not long mouth.Although King (1961)reports that similar,but and sharp, 1 = long and sharp. smaller,ridges develop in otherlobodontine seals, we Although the postcaninedentition of the leopard were unable to confirm this from our sampledspeci- seal is homodont, it is unique among pinnipeds in mens. The absenceof postdentalridges (state 0) is that eachtooth has threedistinct and sharpcusps that plesiomorphic,and indicatesnon-filter feeding. bear witness to their habit of catching large strug- gling prey (fie. 6B; state 1). Other pinnipedimorphs IV. Grip and tear feeding. With few exceptions, (with the exceptionof the crabeaterseal, seecharac- marine predatorsfeed on prey that they are able to ter Fl), have relatively simple homodontpostcanine consume whole. Among modern marine mammals, dentition with no sharpand elongatecusps (state 0). 98 ADAM & BERTA - EVOLUTIONOF PREYCAPTTJRE STRATEGIES AND DIET IN THE PINNIPEDIMORPHA

DISCUSSION forces to captureand dismemberprey is characteris- tic of suctionfeeding. Filter feeding is accomplished Evolution of feeding strategies by taking a mouthful of prey-ladenwater, and subse- quently straining the water and swallowing the prey. Pinnipeds arose from terrestrial arctoid carni- Grip andtear feedinginvolves graspinga largewarm- voresprevious to the Late Oligocene,and have evol- bloodedprey item with the anteriordentition and rip- ved four methods for capturing their prey under ping swallowablepieces from it with shakesof the water. Pierce feeding involves grabbing prey and head. swallowing it whole. The use of strong suctional

(Infercrca) Cernlvoro f Plæ (II) P5 t Plæ(II) P4 Thalassolæn I Plæ (II) P2 t? aÂlnus (Plcrce) Zalop h u s callfo ra h n u s (Pl æ) Eumdopl$Jubatus (PlscCsuctlon?) s3 s2 jI Olarla byontd (Src,t|on?) --r Phourdoshookerl (PlercdSucalon?) Figure 7. Naophoctclnaæ (Ptcrcdsucalon?) pzsillzs (Pleru) Condensed phylogenetic tree of troptcdlls (Plcm) the Pinnipedimorpha showing gazdla (Plæ) character transformations asso- A. lovnscndl (Plerce) Itq t philtppll ciated with feeding strategies. (Plcru) --i complcx t Each thick vertical bar crossing Allodamus t Plcrcc (II) an internode indicates one or Plæ01) more transfonnations, with the I Pl.rc€ (U) .? specific character indicated I Pleu (t) above each bar. In the case of PlercÊ (D Plere (I) reversals, specific characters are indicated below thickened lines. Hydruryd lqtonlx (GdP s4-1 & lÈrdr'rre",Fnl For multistatecharacters (S1, 54, {

and S5), the specific state for Lobodon ancinophagur @lten) each transformation is indicated Lqtonldror$ vdddlt (Plae\ following the character code. Ommatophoûrossl (Pl€rce) Mlrounga epp. (Plæ) Transformation positions are spp. (Plæ) based on the delayed transfor- s3 mation (DELTRAN) criterion. -E?igrrolhus barbatus (Suc'don?) rl-l Predicted and known feeding (Plcroe) behaviours are indicated for all Phoa,lHallùoqus (næ'-. taxa, in addition to level of infe- æmPlæ l-l rence (in parentheses) for fossil Neothslu^ I Plcrce (IV) Imagotada (IV) taxa. Principle prey types are I Plcrc€ s6 also indicated to the right (sym- i+1 Sucdon (II) bols as in fig. 1). For clarity, we f s$3 have collapsed larger monophy- s+2 Plæ(rv) letic groups that do not have any s2 .,, Sucdon (II) internal character transforma- P|ere (IV) tions associated with feeding s3 s2 and which do not differ marked- f Sudlon (II) st-1 ly in diet. A complete (uncollap- Sudlon (U) s6 sed) phylogeny is depicted in Valenlaus I Sucdon (II) fie. l. fosmûfus Sucdon (II)

99 ORYCTOS.YoL.4.2002

rilhen charactersassociated with thesedifferent morphic bracketingtaxon. We considerlevel II and feeding strategiesare consideredin a phylogenetic IV inferencesto be similar in their level of support. framework(fig.1; de Luis & Adam, 1998),a number of trendsbecome evident. However, the interpretation of behaviourand other unpreservedrai$ from functional osteologicalcharacters warrants considerable caution, as has been admonishedby numerous authors (e.9. Lauder, 1995; Witmer, 1995). Witmer (1995) providesa methodfor Extlnl trron A Fotrll irron Exhnt taron I evaluatinginferences (pl.rlomoDhlc) (rld.r trron lo to.rll) on the condition of unpreservedtraits (e.g.behaviour) llo:phologlc Inlù y.r tlo?phologlctmhr y.r ilo.phologlc ùrlt yr Bchrvloural yx in fossil taxa from preserved(e.g. osteodental)traits tnlt; YES Blhrvlourd tnll: within an explicit phylogenetic framework. He definesthree levels of inference.as follows. A level I inference (fig. 8A) requires that two extant taxa, which havea similar behaviouraltrait that is function- Ertrnt hxon A Entnl tlron B (pl.3lono.phlc) ally related to a common morphologic trait, bracket (.lrL. t|ron to tortll) Morphologlct|rlt: no llorphologlc lrrlt y[ a fossil taxon of interest. If the fossil taxon also Bahavlounl tnlt: no shares the morphologic trait, it can be decisively assumedthat it too possessedthe (unpreserved)behaviouraltrait. Level II inferences(fig. 88) occurwhen the two bracketing extant taxa have dissimilar mor- Erùnl tuon A Fortll trxon Ertlnl Lron B phologic and behaviouraltraits. If it can be estab- (plrdomorphlc) (rl.lor t|ron to to.rll) ilorphologlc l?altrno llorphologlc lrlhr ycr ilorphologlc tnlt: no lished that the extant sister taxon to the fossil taxon Bahlvlourd lrdt no E.hrvlounl lralt: no EahrYlouaaltrrh: no and the fossil taxon itself shareda certain preserved feature that is functionally related to a behavioural trait in the extant taxon (but not possessedby the more basallypositioned extant taxon), then it is equi- Ertrnl lrron B vocal as to whetheror not the fossil taxonpossessed (.ldcr trron to to.dl) that behaviour.In level III inferences(fig. 8C), brac- llorphologlc tnlt no Bahavlourd tralt no keting extant taxa have dissimilar morphologicaland behaviouraltraits, and the morphological feature of interestin the fossil taxon is not sharedby either of D Level lV inference the bracketingtaxa. Inference on the behaviourof the - fossil taxon in this caseis purely speculative. To Witmer's (1995)three levels of inference,we heredefine a fourth basedon Lauder's(1995) observation that changesin behaviouraltraits may precede correspondingmorphological changes along a phylo- genetictrajectory. In this situation,the fossil taxon of interest would sharea similar (plesiomorphic)mor- Figure 8. Schematic representationof different levels of inference phological featurewith the basally positionedextant that can made using the extant phylogenetic bracket method within bracket for which a known, functionally related, a phylogenetic framework. See text for further details (A-C adapted behaviourexists. The other extantbracket, conver- from Witmer, 1995; D new inference). sely, would possessa different morphology and behaviour.Although the fossil taxon possessesthe plesiomorphicmorphology, any inferenceabout its behaviouris equivocal(fig. 8D) - it may or may not be similar to the behaviourpossessed by the plesio-

100 ADAM & BERTA- EVOLUTIONOF PREY CAPTURE STRATEGIES AND DIET IN THE PINNIPEDIMORPHA

Bearingthese cautions in mind, it is possibleto is the modernwalrus, which doesnot possesssimilar evaluatethe probablefeeding strategiesutilized by piercefeeding habits or morphology. fossil taxa. Relative to terrestrialcarnivorans, pierce Morphologiesconsistent with filter and grip and feedingin pinnipedimorphsis evidencedby their lack tear feeding are found only within the Phocidae. of preciseocclusion (character Pl), anteriormigra- Lobodon is unique in having all four filter feeding tion of the postcaninedentition (character P2), and characters(lattice-like postcanine dental cusps, pre- tendency towards homodonty (character P3). The ciseinterdigitation of postcanines,high crownedteeth, stem pinnipedimorphsEnaliarctos and Pteronarctos and postcanineridges). Lobodon's sister species, still possesseda distinctly carnassialdentition, Hydrurga,is similarin havinghigh crowned,interdi- althoughother postcanine teeth in thesetaxa show a gitating teeth in addition to uniquely possessing trendtoward homodonty (fig. 7). This is likely repre- enlargedincisors and sharp postcanine cusps associa- sentativeof an intermediatecondition in the evolu- ted with grip and tear feeding.This suggeststhat tion of piercefeeding of later pinnipeds.That extant Hydrurga also has a limited capacity to filter feed, and fossil pinnipedimorphspursue(d) prey underwa- and that grip and tear feeding evolved from a filter ter is furtherevidenced by their enlargedorbits (cha- feeding ancestor.The possessionof interdigitating racter P4) and maxillary branch innervating the teeth in the fossil taxon Acrophoca, whTlesuperfi- vibrissalpad (indicatedby enlargedinfraorbital fora- cially indicativeof potentialfilter feeding,must be mina; characterP5). treatedas a level III inferencewhen placedin a phy- Pierce feeding appearsto be plesiomorphic for logeneticframework as it is not immediatelybracke- the Pinnipedimorpha,and is the first evolving prey ted by any extant filter feeding ancestors. capturing strategy of pinnipedimorphs when they Although not includedin this phylogeneticana- evolvedfrom arctoidcarnivores during the Late Oli- lysis, the westemAtlantic fossil sealLobodon vetus goceneor earlier.It is also the strategythat characte- (known only from a single tooth) appearsto have rizes most fossil and living pinnipedimorphs,inclu- postcaninedentition that bears striking similarity to ding the basal taxa Enaliarctos and Pteronarctosin L. carcinophagusand may place the origin of filter additionto all otariids(with the exceptionof Otaria), feeding as early as the Miocene. Unfortunately,the the fossil phocoidsAllodesmus, Desmatophoca, Pin- dating and taxonomic affinities of this specimenare narct i di on, Acropho c a, H omiphoc a, andP i s c o pho c a, questionableas the geologicage of depositson New plus all extant phocids except the monachines Jersey'scoastal plain are problematicand the holo- Hydrurga andLobodon and the phocineErignathus, type specimenhas been lost (Ray, 1976).No fossil as well as the odobenidsNeotherium, Imagotaria, record exists for L. carcinophagusor Hydrurga. lf Pontolis, andAivukus. Some of thesetaxa are,how- the fossil record of L. vetus is inaccurate(which is ever,also charactenzedby traits associatedwith suc- probable),then filter and grip and tear feedingappear tion feeding,a problem that is discussedlater. For to be recentfeeding behavioursfound only in extant Enaliarctos,Pteronarctos, Thalassoleon, and the fos- taxa. sil phocoidsAllodesmus, Pinnarctidion, and Desma- Suction feeding is characterizedby elongation tophoca,the assignmentof piercefeeding is a level II and vaulting of the hard palate, enlargementof the inferencein that there is no basal extant bracketing pterygoid hamuli, and fusion of the mandibularsym- taxon relative to thesegroups that displayspierce fee- physis. Although included above with other charac- ding. For the threetaxon group including Acrophoca, ters indicating suction feeding, the loss of incisors assignmentof piercefeeding represents a level I infe- doesnot by itself indicatethis type of feeding,as inci- rence in that extant pierce feeding relatives occur sors (or lack thereof)do not contributeto the genera- both as sistertaxa and immediatelybasal to thesefos- tion of suction forces.Rather, incisor loss in the pre- sil forms (1.e.among monachineand phocine pho- sence of other suction feeding characteristicsindi- cids, respectively).A level IV inferenceis evokedin catesthat the entranceinto the oral cavity is relative- assigning Neotherium, Imagotaria, Pontolis, and ly free of obstruction- a featurethat would enhance Aivukus to the pierce feedingclass, as the only extant the efficiency ôf suctionfeeding. For this reason,the bracketingtaxon abovethe node uniting thesegenera loss of either upper or lower incisors (characters54 101 ORYCTOS,YoL.4.2002

and 55, respectively)were ignored in lineagesthat to behavioural studies, examination of recently did not exhibit other adaptationsfor feeding by suc- ingestedprey recoveredfrom the stomachsof these tion (e.9. in lineagespredicted to feed by piercing speciesmay shed some light on how the prey were prey, mentionedabove). captured. A trend towardssuction feeding is observedin a numberof independentpinniped lineages. Among the odobenids,fossil membersof both the dusignathine DIET OF FOSSIL PINNIPEDIMORPHS and odobeninelineages appear to have independent- ly adaptedto suctionfeeding (a level II inference).As As noted above, the diet of extant speciesis previously noted by Barnes and Raschke(1991), generally well known. Given that we know the diets Gomphotaria shows several adaptationsconsistent of living pinnipeds and have generatedhypotheses with suctionfeeding, including an elongateand transfor the different feeding strategiesused to capture versely archedpalate and the loss of two upper and their prey, what can we predict about the diet of fos- all three lower incisors.Dusignathus has a similarly sil taxa? In lieu of alternativemethods for determi- transverselyarched palate, has lost one upper incisor, ning the diet of fossil taxa (e.g. preservedstomach and in addition has a fully ankylosed mandibular contents),we must rely on analogieswith the func- \À/ith symphysis. the exceptionof Aivukus,all odobe- tional morphology associatedwith different feeding nine walrusesshare enlarged pterygoid hamuli (un- strategiesand diet in living taxa. This method known in Protodobenus),elongated hard palatesand, requires secondaryspeculations (i.e. diet) to be with the exception of Protodobenus,have deeply drawn from primary speculation(i.e. feeding beha- vaulted palates.Valenictus and Odobenzsalso have viours), and the compoundedsources of error require fully ankylosedmandibles. All odobenineshave lost that predictionsof diet in fossil forms be treatedwith some or all (Valenictus) of the incisors, with the considerablecaution. Indeed, the unfortunateanswer exceptionof Protodobenus. to the questionposed above is that evenamong extant In addition to the odobenids,adaptations for suc- speciesthere appearsto be only loose correlationbe- tion feeding (not considering incisor loss) are also tween specific diets and different feeding strategies. seenin the extant southernsea lion (Otaria) and the For example,suction feeding has been demons- bearded seal (Erignathus). Unfortunately, neither trated for the walrus and is predicted here for both basicdescriptions nor behaviouralstudies offeeding Otaria and Erignathus basedon similarities in cra- in Otaria have been published, and it cannot be niodental functional morphology. These taxa, how- confirmed whetheror not this sealion is able to feed ever,feed on very different food items.Both the wal- by suction.Deméré (1994a) and Burns (1981) both rus and Erignathus feed on the soft portions of ben- indicate thatErignathus is an efficient suctionfeeder, thic bivalve mollusks, while the latter also feeds on although behavioural studiesconfîrming this have not epibenthic crustaceans(Lowry et al., 1980). In beenconducted. As such,designating either species contrast,Otaria eats comparativelylarger and more as a suction feeder requires a level III inference,as mobile fish and squid (George-Nascimentoet al., neitheris immediatelybracketed by a known suction 1985;Koen Alonso et al., 1999).Thus, suctionfee- feeding taxon. However, severalcharacters associa- ding appearsto be an efficient method for capturing ted with suction feeding in pinnipedsare also found and consuminga wide variety of food items, andpre- in suction feeding ziphiid whales (Heyning and dictions of diet in fossil taxa using functional mor- Mead, 1996).Given the taxonomicallybroad-ranging phology must take this into consideration. commonality of these characters,we postulate that The diet of Protodobenusjaponicus has pre- both Otaria andErignathus do indeedhave a limited viously beenpredicted to be primarily fish and squid, capacity to suction feed, although their abilities are based on the observationthat this specieshas well unlikely to be as strong as has already been obser- developedupper incisors that would have precluded ved in the walrus. This hypothesisis readily tes- bivalve dismembermentas seenin the modernwalrus table, as both speciesare extant (although such a (Horikawa, 1994: p. 325). This prediction parallels studyis beyondthe scopeof this paper).In addition the observedmorphology and known diet of Otaria. r02 ADAM & BERTA- EVOLUTIONOF PREYCAPTURE STRATEGIES AND DIET IN THE PINNIPEDIMORPHA

However,Erignathus also possesses upper inci- squid-eatingOtaria. Previouspredictions of diet for sors and is efficient at removing the foot of clams fossil taxabased on morphologymay or may not be (Serripessp.), presumablybecause the foot is ex- correctin light of this broadertaxonomic survey and posedwhen the clam is excavated.In light of a broader phylogeneticframework. taxonomic survey, the diet of Protodobenuscannot Given theseproblems, how can we progressto accurately be predicted. Similar argumentscan be betterresolve the diet of fossil pinnipeds?Certainly madefor Deméré's(I994b: p.97) postulationthat the the strongestarguments will be thosethat utilize all sympatric odobenidsValenictus chulavistensls and availablesources of evidence.We recommendthat an Dusignathusseftoni fed on benthic invertebratesand important first step is the assessmentof the above fish or squid(respectively) and Barnes and Raschke's charactersin the fossil speciesto assesspotential fee- (1991:p. l0) predictionof molluskivoryfor Gom- ding behaviour.It is also possiblethat other,as yet photaria pugnax. undescribed,craniodental features might revealclues In a similarfashion, filter feedingis a specializa- to the diet of extinctpinnipeds. For example,a com- tion of the crabeaterseal (Lobodon) and, to a lesser parativebiomechanical analysis of lever arms of the extent,the leopardseal (Hydrurga).I(rill constitutes masseterand temporalismuscles acting on the lower a large proportionof the known diet in theseseals, jaw in relationto feedingbehaviour or diet has not and it might be surmisedthat fossil taxa exhibiting yet beenconducted for thepinnipedimorphs. Similar- charactersconsistent with a filter feedingstrategy fed ly, we observedreduced (relative to other pinnipeds) on krill. However, krill also constitutesa large por- orbital size in all odobenineswith the exception of tion of the diet of the Antarctic fur seal(Arctocepha- Aivukus- this might be expectedof speciesthat do lus gazella), a speciesthat shows no characters not rely solely on visual cues for detectingsessile consistentwith filter feeding.Furthermore, A. galel- prey(i.e. benthic invertebrates). However, too little is Ia and other piscivorous/teuthophagousmembers of known about the visual systemsin pinnipedsat pre- the Arctocephalusclade are so similar in cranioden- sent to infer how the structureand orientationof the tal featuresthat distinguishingskulls from individual eyesmight contributeto the captureof different types speciesof the genusis problematic(Repenning et al., ofprey. In looking for new charactersto predict diet, I97I). Given this similarity, it is improbablethat rhe however,we stressthat any study should be compa- distinctdiet of A. gazellacould havebeen accurately rative and should sample broadly those taxa des- predictedfrom craniodentalfeatures alone. cribed above as having different feeding behaviours and/or diets. The use of a phylogenetic framework will also benefit such a study to assesswhether the SUMMARY AND FUTURE DIRECTIVES morphology in question (and perhaps diet) is the result of homology or homoplasy. We have shown that although commonly Clues from the environmentat the time of depo- employedmorphologic features of the skull and teeth sition should also be taken into consideration.For may be usedto predict the feedingbehaviour of pin- example, sedimentsassociated with a given fossil nipeds, extending these observationsto predict the pinnipedimorph, and the potential prey that they diets of fossil or unknown taxa warrantsconsiderable contain, should be examined.As noted earlier,how- caution.Among living species,pierce feeding is most ever, pre-depositionaltransport of carcassespresents commonly associatedwith piscivorousor teuthopha- problemsin that predator-preyinteractions cannot be gous diet. However, a pierce feeding morphology is assumed.Examination of multiple, independentspe- also sufficient for capturingzooplankton, as observed cimensof the fossil taxon would help to reduceambi- in A. gazella. Similarly, the apparentspecializations guity. of the stenophagousLobodon for filter feedingdo not Barnesand Raschke (1991) additionally used preclude other speciesfrom a zooplanktonicdiet. A featuresof swimming behaviourto infer the probable suction feeding morphology, although commonly diet of Gomphotariapugnax. The specimenof Gom- associatedwith a benthic invertebratediet (e.g. Odo- photaria that they described(LACM 121508) is benus andErignathus), is also found in the fish- and pathologicalin that the right elbow is ankyloseddue 103 ORYCTOS.YoL.4.2002

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