Mitt. Mus. Nat.kd. Berl.. Geowiss. Reihe 4 (2001) 139-165 05. I I. 2001

Feeding mechanisms and ecology of pycnodont fishes (Neopterygii, tPycnodontiformes)

Jiirgen Kriwet’

With 16 figures and 1 tablc

Abstract

The functional morphology of the jaw apparatus and the skull and the feeding habits of the extinct pycnodont fishes arc reconstructed in comparison with some extant halecostomes. For this, a short review of the functional units of the pycnodont head is given. The feeding mechanisms of pycnodonts exhibit a transition from simple stcrcotypic feeding kinematics. which are characteristic for primitive actinopterygians, to the modulating feeding kinematics of advanced teleosts and is called lim- ited modulating fccding kinematics herein. Two structural specialisations which are found in halecostomes (operculum with distinct ni. levator operculare and the interopercular bone with the interopercular ligament) are supposed to be absent iii pycnodonts, whereas they maintain the two primitive couplings for direct mandibular depression (epaxial muscles - neurocra- niunr. hypaxial muscles - cleithrum-ni. sternohyoideus - hyoid apparatus). Advanced pycnodonts developed a new structure (upper jaw protrusion resulting in an enlargment of the buccopharyngeal cavity), that is absent in halecomorphs (e.g., hiiirr cnlvn) and basal pycnodonts (e.g.. tArdunfrons, tMesturzis). The premaxillae and maxillae are firmly fixed in basal pycno- donts, whereas the premaxillac and maxillae are free and movable in advanced pycnodonts. Pycnodonts were benthic foragers with a combination of biting or nipping and suction feeding based on the “truncated cone morphology” of the buccopharyti- gcai cavity. 11 is concluded. that pycnodonts certainly were omnivorous leeders with a general broad range of prey. But they wcrc also a highly specialised group on generic level in respect to their prey. This is indicated by gut contents, as far as thcy are known. which comprise only monospecific remains of shelled invertebrates (e.g., spines of echinoderms. shells of bivalves). The ecological dcmands of pycnodonts are discussed.

Keg words: Neopterygii, Pycnodontiformes, fccding, gut contents, ecology.

Zusammenfassung

Die funktionelle Anatoinie des Nahrungsaufnahmeapparates sowie das Fressverhalten der seit dem Eozan ausgestorbenen Neopterygier-Gruppe der Pycnodontier wird im Vcrgleich zu einigen rezenten Halecostomen (Amin cnlvn. verschiedene Te- leosker) untersucht und diskutiert. Dazu wird cine kurze Ubersicht iiber die funktioncllen Einheiten des Pycnodonticrschii- dels gegeben. Die Kirrcmatik des Nahrungsaufnahmeappat-ates der Pycnodontier stellt einen Ubcrgang von der einl~iclren. stereotypischcn Kinematik primitiver Actinopterygier zu der modulierenden Kinematik fortschrittlicher Teleosteer dar tind wird hier als limitierte, modulierende Kinematik bezeichnet. Zwei structurellc Spezialisationen, die bei Halecostonii cntw- ckelt sind (Operculum mit distinkten m. levator operculare und das Interoperculare mit dem interuperculare Ligament) fclr- len bci Pycnodontiern, wogegcn sie die zwei primitiven Verbindungen zwischen den epaxialen Muskeln und dein Neurocrani- um und zwischen den hypaxialen Muskeln, dem Cleithrum und dcm Sternohyoidmuskel fur die direkte Unterkieferabscnkuti~ bcibehalten. Fortschrittliche Pycnodontier entwickeln aber eine neue Struktur (bewegliches Maxillare und Preniaxil1;ii-e 7111- Erweiterung des buccopharyngealen Raumes), die bei Halecomorphen als auch ursprunglichen Pycnodontiern (z. B. TArdirtr- rrcins. tMesturus) fehlt: Maxillare und Pramaxillare werden aus dem Schadelverband gelost und beide werden gegeneinnnder beweglich. Wahrend der Mandibulardepression schwingt das nun freie Maxillare um einen vorderen Artikulationszapfen antc- ro-ventrad und druckt das Pramaxillare nach vorne in Richtung Bcute. Die Okomorphologische Untersuchung zeigt, dass der Rachcnraum als ..truncated-cone”, wie er fur Teleosteer mit ausgepragtem Schnappsaugmechanismus typisch ist. rekonstruiert werdcn kann. Die Kinematik dcs Kieferapparates der Pycnodontier reprasentiert somit eine Kombination aus reincm Beilkn und Schnappsaugen. Pycnodontier ernahrten sich vermutlich omnivor sowohl von schalentragenden als auch schalcnloscn Invertebraten ernahrten. Vermutlich waren die cinzehien Gattungen aber hochspezialisierte Beutegreifer. Dies Iiisst sich niit- hilfe der uberliefertcn Mageninhalte zeigen, die monospezifisch fur jede Gattung sind.

Schliisselworter: Neopterygii, Pycnodontiformes. Fressverhalten, Mageninhalte. Okologie.

’ Institut fur Palaontologie, Museum fur Naturkunde, Zentralinstitut der Humboldt-Univcrsitat zu Berlin. lnvalidenstralk 43. D-1011.5 Berlin, Germany. Received February 2001. acceptcd J~ly2001

WILEY-VCH Verlag Berlin GmbH. 13086 Berlin. 2001 1l.3S-l943/01/041l-I~139$ 17.50-.50~0 140 Kriwet. J.. Feeding mechanisms and ecology of pycnodonts

Introduction functional units), ligaments and arthrology, and motion analysis based on electromyography and The jaws and heir associated elements of fishes high 5peed motion pictures of prey capture and are used in many ways to capture. process. trans- respiratory. This enumeration of approaches, port, and swallow food (eg. Gillis & Lauder which are all commonly used in living forms, elu- 1995). The stricture of the dentition and compo- cidates the problems one deals with in palaeon- sition of the diet of modern actinopterygians tology. The inability to study soft tissues and re- have been wicely used to infer the nutrition of lated kinematics in fossils is the reason, why the fossil actinoptc rygians and to make assuinptions inference of function from structure alone is on ecological demands. It is accepted. that the widely used in palaeontology, although the extra- study of funci ional morphology enables us to polation of function from form may only give better understiind selective forces in the evolu- limited knowledge of the real functions. The tion of organisms (Osse 1969. Lauder 1990. head of actinopterygians is generally divided into 1995). The funstional morphology of the feeding several functional units (“intimately associated apparatus and its kinematics must be carefully aggregations of bony elements, ligaments, and examined to understand the processes of food muscles performing in a close union”) of one or capture and ils processing correctly. Neverthe- more functions for studying its functional anato- less. only obse .vations which are not possible in my (e.g.. Liem 1967. Osse 1969). This definition fossils. could give reliable results. Stomach con- confirms the problems in palaeontology again, tents could prove or disprove the deduced func- because the reconstruction of soft tissues is tional and eco ogical demands. This is a difficult rather speculative in most cases. task in fossils. because the preservation of sto- Generally. five methods for studying the func- mach contents is not the rule. The literature on tional morphology in modern fishes are used. feeding habits including the functional morphol- Some of these methods have been applied to ogy of the sku 1 and feeding apparatus in combi- functional morphology in fossils. (1) The phylo- nation with a study of stomach contents in ex- genetic method relies on the phylogenetic rela- tant and fossil actinopterygians is extremely tionships of organisms; relationships between sparse. Nevertheless. the biomechanical fragmen- structure and function found in Recent taxa are tation of shells by certain extant actinopterygians applied to extinct relatives (e.g., Stanley 1970, and its importteleost! (Laudcr 1983). Most authors im- der 1995 discussed the phylogenetic (1) and ply, that functim and structure of skeletal com- paradigm (2) methods and their difficulties to plexes are closAy related as no part works alone some extent.). (3) ‘he ecomorphological para- but interacts with other components (e.g.. Dulle- digm (e.g.. Clements & Bellwood 1988, Liem meijer 1974, 7homas 1978). Hence. the under- 1993). This paradigm accepts, that the morphol- standing of the relationships between function ogy of the skull relates to how the animal feeds. and structure would explain complex and dy- Variations observed in the skull anatomy are namic processes like feeding and respiratory me- thus correlated with inter- or intraspecific differ- chanisms. The 8,tudy of functional anatomy of the ences in diet. (4) High-speed cinematography in head of extant actinopterygians involves several combination with recording of the electrical ac- closely relateti topics: the cranial osteology. tivity pattern of muscles (e.g., Liem 1970, Lauder myology (the description of muscles between 1995). This combined methods is only possible in Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 4 (2001) 141 extant forms. Lauder (1995) presented a case framework for interpreting the functional mor- study concerning the feeding habits of extant os- phology of pycnodont feeding. In addition, pre- teoglossomorphs based on the electrical activity served gut contents are considered to reconstruct pattern of muscles. The results show, that there their feeding ecology. exists considerable discordance between struc- ture and function in the musculo-skeletal system. The key reason for this is the nervous system. Material and Methods Minor changes of the central nervous structure and function have the capability of extremely Pycnodont material: Remains of pycnodont fishes are abundant in Mesozoic and Palaeogene deposits world-wide. changing the accuracy of predictions based on Therefore. most museums have a lot of pycnodont material. musculo-skeletal morphology alone (Lauder In the last few years, more than 1000 specimens belonging to 1990, 1991, 1995). The results are in fact very about 145 species of pycnodonts have been studied (Kriwet 2001). This material is housed in 32 institutional collections pessimistic for palaeontologists, because they im- all over Europe and thc U.S.A. Most material, which forms ply, that it is impossible to reconstruct the func- the basis of this study, consists of more or less articulated tional morphology alone from the bony parts of specimens from the Late Triassic, Early to Late Jurassic. Late Cretaceous, and Eocene. In addition, isolated dentitions and an organism. (5) The importance of soft tissues disarticulated skulls were used to study the joints of the jaw in the study of the functional morphology of fos- elements and the abrasion patterns on teeth. Some isolated sil taxa was also discussed by Witmer (1995). elements (e.g., vomers, prearticulars, teeth) and an isolated skull were studied in transversal ground section. Several spe- Generally, the reconstruction of soft tissues in cimens were prepared using acetic acid, but most material fossils is based on comparison with extant rela- was alrcady mechanically prepared. Drawings were prepared tives. Consequently, Witmer (1995) introduced under Wild M5 and M8 microscopes. Photographs were pre- pared by the author and W. Harre (Berlin). A complete list the extant phylogenetic bracket approach (EPB). of the investigated material is presented in Kriwet (2001). This method resembles the phylogenetic method and it is not useful to repeat it herein. described above. Myology, ligaments, and arthrology: The knowl- Recently, Westneat (1999) reinforced the value edge of the myology, the arrangement of ligaments. and the of biomechanical principles and mechanical mod- joints or couplings betwcen bony structures are important to els of the musculo-skeletal system derived from understand the kinematics during feeding. Unfortunately. the reconstruction of soft tissues in exclusively fossil known taxa living taxa for the study of the functional mor- is speculative. Nevertheless, there are many osteological re- phology of fossils. The models used by him are lated features like tuberosities, crests. grooves. fenestrae. fos- based on sets of morphometric variables, that sae, foramina, and septa and the absence of certain bones (e.g., interoperculum, urohyal), that allow some assertions have direct functional relevance to force and ve- about soft tissue anatomy. In addition. the soft tissues and locity characteristics of actinopterygian jaws. the arrangement of muscles and ligaments in the skull of ex- Pycnodonts are generally regarded as shell- tant sparids, acanthurids, nandids, and Anurrhichns hps. which are assumed to be similar to pycnodonts in their denti- crushers. Their ecology and feeding habits were tion and to some extent also in their skull-shapc and the ex- described in general terms by Nursall (1996a). tant Anziu have been studied for comparison based on litera- He proposed, that pycnodonts inhabited shallow ture data (e.g., Lubosch 1929, Dobben 1937. Willem 1942. 1944, 1945. 1947, Osse 1969, Liem 1970, Winterbottom 1974. marginal, often reefal seas and were restricted to Bellwood 1994) and by personal observations. The study of durophagous habit. In contrats to this, Poyato- ligaments is extremely important in functional analysis of the Ariza et al. (1998) suggested, that pycnodonts feeding apparatus, because ligaments determine the direc- tion, degree, and speed of motions between the bony elc- were also adapted to fresh-waters. I will present ments (Liem 1970). Mobile joints between the functional new results and discuss herein the feeding habits units and within the units are important in understanding of the extinct pycnodont fishes, which are inter- functional anatomy and analysing the motion of these units. The articulations between functional units found in Recent preted as a monophyletic group and as sister to teleosts and Amia were described by Alexander (1967a. b. all other neopterygians (Kriwet 2001). Thus, the 1970), Liem (1970), Lauder (1979, 1982), and Jollie (1984). kinematics of the feeding apparatus are studied The data are summarised in Kriwet (2001). by briefly analysing the morphology of the skull Feeding in halecomorphs and teleosts: The evolu- including the bony structures as well as pre- tion of different feeding strategies and kinematics of actinop- terygians is related to changes in the structural and func- sumed soft tissues in comparison with extant ha- tional network of the skull. Most functional studies of the lecomorphs (e.g., Amia) and teleosts (e.g., Anar- feeding habits of actinopterygians are focused on extant tele- rhichas, Lamprolagus, Scarus). Linkage models osts so far. Data of the head morphology and the feedins kinematics of the extant halecomorph Anzia and fossil and are developed in comparison to those estab- extant teleosts are takcn from Arratia (1997, 1999). Alexan- lished by Lauder (1982) to show the interactions der (1967a, b), Gosline (1965), Lauder (197Y, 1980a. 1982). of the skeletal and proposed soft tissues during Liem (1970), Patterson (1973, 1977). Patterson & Rosen (1977), and others. Additionally, the head morphology of ex- feeding. The development of mechanical models tant sparids, roaches, and Anarrhichas were investigated. The provides for the first time a broad conceptual structural network in the head of pycnodonts related to 112 Krin ct. J.. Feeding mechanisms and ecology of pycnodonts mouth opening ai d suction leeding is reconstructed as net- dont skull are the dermatocranium, the endocra- work following La idcr ( IYS0:i). nium including the parasphenoid and vomer, the 1 n s t i t u t i ona 1 i, b b r e 1.i ii t i on \: Certain specimens cited suspensorium apparatus including hyomandibula, in the test arc ho'.ised in ttie follo\iinp institutions: AMNH. Department 01 Vt rtchrate Paleontolopy. American bluscum prcoperculum. ectopterygoid, entopterygoid, and ol Natural Histor!. Ne\v Yor-k: BGMM. Biiryernieisrer MUI- metapterygoid. symplectic, and quadrate, the op- ler Museum. Soln hofen: BMNH. The Natural History Mu- ercular apparatus, the jaw apparatus, the hyoid seum. London: B!,P. Ra! el-ische Staatswiiimlung fur Paliion- tologie und histori ,che Geologic. Miinchen: 4lB. kfuseunl fiir apparatus, and the branchial apparatus. The pec- Naturkunde. Bcdi I: MGSR. Musro Gcol6gico del Seminario. toral girdle is also functionally important in de- Barcelona: MNH:% Museum national d'Histoire naturclle. prcsting the mandible, because it is pulled ante- Paris: and VFKC Verein der Freunde und Fbrderer dcs Naturkundemuseu ns Ostba\ern e.\'. riorly when the mandible is adducted. For interprctation of the pectoral girdle see Nursall (1996b. 1999a. b) and Kriwet (2001).

Cranial skeleton C I- a n i u in : The dermato- and endocranium of pycnodonts have been described by several The cranial sk1:leton of pycnodonts is only sum- authors (e.g.. Dunkle 81 Hibbard 1946, Gayet marised hereir . Functional units of the pycno- 1984. Bell 1986, Lambers 1991, Nursall 1996b,

io

PasP of vo Pm m

ang s art sym cha chp br den pra ang art sym chaw br A B

Fig. 1. Restoration of p!ciiodont heads in lateral \.ien. A. iG~,rot/ic.,/rcv(/cgo/!iis. B. -i-Proscir7ere.sdegrrrzs. Not to scale. ang. angular bone [- articular of Allis I S97 and dermarticular of Cioodrich 10301: art. articular bone; br. branchiostcgal rays: cha. anterior ceratt,hyal [= ccratoh!al of Bridge 1877. Allis 1897 and others: distal ceratohyal of Patterson 1973.1; chp. postey- pihyal 01' Bridge 1877. Allis 1887a and others: prosimal ceratohyal of Patterson 1973.1; cl, cleithrum [= '71: den. dentalosplenial [= dentar! of Grantle 19 Brmis 1998 and others. The dentary of actinopterygiaiis might not bc homc.logous iyith the dentary of sxcopterygians (Jarvik IOSO. Jollic 1 Y86) and the term dentalosplenial proposed by Jollie 1981. l0Fh is I-etaincd]:dps. dcrlnopterosplicll~~tic.follo\\ing Kriwet et nl. 1099 [= dermopterotic of Wenz 198Ya, b, Nursall 1 Y96b. 1W)a. Compound bone con\istinp of portions of the dermopterotic and dermosphenotic]; dso, dermosupraocci- pital. folloiving N~rsall1996b. 199Ya: dt. dermal tesscrae: enp. endopterygoid [= entopterygoid of Allis 1897, Nursall 199hb. and others: pter\y lid of Jvllie 10S4: mesopteryyoid of Bridge 18771: ect. ectopterygoid: hyo. hyomandibula; io. infraorbital, tubular ossification5 surrounding ttie infraorbital canal: m. maxilla: ma. marginal skull bones [= dermal elements at the poster- ior. margin of the skull. The homolog! of these bones is uncle;ir]: met. nicsethmoid [= cttimoid]; mpt. metaptcrygoid: nu, ntichal scutc [= m:dian cstiascapulai- of hursall lYY9al: of. olfactory fossa: or. orbit: op. operculum; pa. parietal bone (The dermal skull bone called frontal in actinopter!gians b! many authors. e.g.. Jollie 1984a. Nursall 190hb. 1009a. and Grande & Bemi< 1 99s is not iomologous to the frontal of sarcopterygians. e.5.. Schultre & Arsenauld 1985, Arratia & Cloutier 1996, hut corrc5ponds to the parietal of tctrapods.]: pasp. parasphenoid: pif. posterior infraorbital [dermosphenotic]: pm. prcrnaxilla [= rhiiiopremasill;ii-y I ~f Jar\ ik 1980]: pop. preoperculuni: pp. postparietal hone [The term postparietal is used here for actinopter- >piaiis t'ollov iny Sc hultre 1003 instead of the term parietal: see also pa.]: ppe. postparietal pi-oce~s[= postparietal peniculus of Nurwll lL196h. I99 ?a]: pra. preitrticular honc: q. quadrate: s. scale. sc. sclerotic ring elements: scl. supracleithrum: sym. sym- plectic: vo. imm. Mitt. Mu. Nat.kd. Berl., Geowiss. Reihe 4 (2001) 113

1999a, b, Kriwet 1999a, 2001, Kriwet et al. 1999). (Fig. 1B) of pycnodonts is almost vertical, as it is The cranium of pycnodonts is considerably re- in teleosts. It consists of ectopterygoid, entopter- duced in comparison to that of Ginglymodi, Ha- ygoid, metapterygoid, hyomandibula, quadrate. lecomorphi, and teleosts. The standard pattern of preoperculum, and symplectic. the dermal skull of adults includes an unpaired The pterygoid bones are placed above each dermosupraoccipital, paired postparietals, parie- other, and this condition has been proposed as a tals, dermopterosphenotics (compound bones), synapomorphy for pycnodonts (Lambers 1991, and posterior infraorbitals (Fig. lA, B). In con- Nursall 1996b, 1999b). trast to other neopterygians, pycnodonts lack na- The quadrate is massive, situated ventrally to sal, rostral, supra- and suborbital, supramaxilla, the entopterygoid, and abuts the symplectic posttemporal, suboperculum, interoperculum, (Fig. 2). In contrast to teleosts, the quadrate and gular bones. The endocranium of pycno- lacks the postero-ventral process. A quadratoju- donts displays fewer ossified elements than that gal is not present contrary to the assumptions of other neopterygians (Kriwet 2001). The endo- made by Nursall & Maisey (1991). cranium is badly preserved in most specimens, The form of the preoperculum differs among and only few elements seem to be consistent pycnodonts. It is rather triangular in some forms. throughout the Pycnodontiformes. The general- where the upper part is only partly reduced (e.g., ised pattern includes a large median meseth- tGibbodon) to roughly rectangular in more ad- moid, unpaired supraotic and orbitopterosphe- vanced ones with largely reduced preoperculum noid, and paired hyomandibulae, symplectics, (e.g., tPycnodus, tProscinetes: Fig. 1B). This re- quadrates, metapterygoids, exoccipitals, prootics, duction of the upper dermal part of the preoper- pterotics, sphenotics, and epioccipitals. Dermal culum is striking. The degree of reduction is not elements of the endocranium are the paired consistent within pycnodonts but varies from ento- and ectopterygoids, and the unpaired para- genus to genus. The preoperculum is strongly re- sphenoid and vomer. The braincase is covered duced in size in advanced pycnodonts (e.g., t&c- dorsally by a median chondral bone, which is lo- nodus). cated within the otico-occipital region. This bone The hyomandibula is tightly fixed to the med- is rather large and consists of a slightly ex- ial surface of the preoperculum supporting it panded base and a large ascending plate, which (Nursall 1999b). The hyomandibula is more or ends just beneath the dermal skull covering. Nur- less exposed above the preoperculum depending sall (1 996b) identified this bone as supraoccipital on the reduction of the upper part of the preo- and interpreted it as a synapomorphy for pycno- perculum. The exposed part of the hyomandibu- donts. However, he assumed this bone also being la is almost as large or even larger than the re- a synapomorphy of pycnodonts and teleosts in maining preoperculum in advanced pycnodonts the same paper. Maisey (1999) studied this bone such as t Coeiodus, ~Stemmatodus,t Tepexichthys, in acid-prepared specimens of Neoproscinetes pe- and tPycnodus. The upper part of the hyomandi- nalvni and concludes, that the supraoccipital bula of primitive pycnodonts such as tMesturzis bone of Nursall (1996b, 1999b) is actually the and tBrembodus is broad and flattened in lateral supraotic sensu Patterson (1979, because of its view. It articulated with an elongated and nar- supposed position in front of the occipital fissure, row facet on the neurocranium. This morphology its position above the anterior semicircular ca- limited rotation of the hyomandibula in more nals, and its fusion with the pterosphenoid. This primitive pycnodonts. An articulation process assumption corresponds well to the phylogenetic was developed at the antero-dorsal edge of the hypotheses proposed by Arratia (1999) and Kri- hyomandibular head in t Gyrodus, tlenienjn. and wet (200l), which show, that the supposed su- INeoproscinetes mediating rotation mainly praoccipital bone of pycnodonts is not homolo- around it. Thus, rotation of the suspensorium gous with that of Leptolepis coryphaenoides and was more efficient in more advanced pycno- more advanced teleosts. donts. The opercular process of the hyomandibu- la was reduced in almost if not all pycnodonts. Suspensorium apparatus: The preopercu- Lambers (1991, 1992) indicated a vestigial oper- lum is included in the opercular series by most cular process in tGyrodus spp., which has not authors. But functionally, the preoperculum of been observed herein. actinopterygians belongs to the suspensorium ap- The exposed upper part of the hyomandibula paratus, since it serves as the origin of the adduc- exhibits irregularly arranged tubercles or ridges tor mandibulae muscles. The suspensorium in most pycnodonts similar to the sculpture of I44 Krinet. J . Feedin2 mechanisms and ecology ot pycnodonts

A 5 mm vo POP

< cha -p ante -ior B

Fig. 2. Mandibular articulation ol pycnodonts (A) itnd its di-a\ving (B) exemplified by Pycrioilus p[oressus (BMNM P. 1634) displaying the two articulation pair\. Acid prepared specimen from the Eocene of Montc Bolca. Northern Italy. The symplec- tic abuts the qmdr ttc and there is an additional articulation surface hetwccn both (ariow). ang. angular bone: art. articular- hone: h. reniains of hranchial ra! s: cha. anterior cerntohyal: chp. posterior ceratohyal: den, dentalosplenial: dent. tccth of dentosplenial: m. maxilla: met. mesethinoid bone: pc. processus coronoideus; pm. premaxilla; pmt. preniaxillnr! I-eth: pop. prcoperculum: pra. prearticular bone: q. quadrate: sgm. symplectic: vo. voiner. Mitt. Mus. Nat.kd. Berl.. Geowiss. Reihe 4 (2001) 14.5

the dermal bones. This dermal-like pattern of the The elongation of the suspensorium of pycno- hyomandibula was suggested to present some donts is related to the shortening of the lower kind of dermalisation by Nursall (1996b, 1999a, jaw and the placement of the quadrate-mandibu- b), and he consequently called this part of the lar articulation below the orbit and not posterior hyomandibula dermohyomandibula. However, to it as in primitive actinopterygians. this sculpture is only superficial, and the hyo- mandibula is an endochondral bone. Subse- Opercular apparatus: The opercular appa- quently, the dermal-like pattern rather corre- ratus of pycnodonts is reduced compared to that sponds to membranous outgrowth than to a true of other neopterygians (Fig. lA, B). The series is dermalisation, and the term dermohyomandibula composed of a large and more or less triangular implies wrong homologies. Membranous out- preoperculum (above described), an operculum growth on the anterior or posterior region of the fixed to the postero-dorsal border of the preo- hyomandibula is found in many advanced acti- perculum, and two short acinaciform (slender) nopterygians (G. Arratia, pers. comm.). Thus, the branchiostegal rays, which articulate with the term proposed by Nursall (1996b) is not retained ceratohyal elements. The operculum is small, herein. The development of the membranous narrow, and dagger-shaped in almost all pycno- outgrowth of the upper part of the hyomandibu- donts. tPycn0du.s is the only pycnodont, that la in pycnodonts is related to the reduction of lacks an operculum. The functional significance the preoperculum, since only the exposed hyo- of the reduction of the operculum is unclear (see mandibular parts show the dermal-like structure. below). The development of membranous outgrowth re- There is no subopercular bone in pycnodonts. flects a change in an existing structure rather The interoperculum developed in association than the development of a new bone with any with a mobile maxilla and a forwardly directed implied homology. The sculptured part of the jaw articulation in the evolution of actinoptery- hyomandibula was mostly misinterpreted as op- gians towards the characteristic halecostome suc- erculum (e.g., Blot 1987) or dorsal preoperculum tion feeding (Schaeffer & Rosen 1961, Lauder (Wenz 1989a). 1980b, 1982). Thus, the interopercular bone is a The symplectic articulates with the antero-ven- key element in the chain of elements transmit- tral edge of the medial surface of the preopercu- ting contraction of the levator operculi muscle to lum (Figs lB, 2A, B). The symplectic was prob- the mandible (Lauder 1983). Subsequently, the ably fixed to the preoperculum by connective absence of the interoperculum and the asso- tissue. This condition is different to that found in ciated interoperculo-mandibular ligament in pyc- many other neopterygians, in which the symplec- nodonts indicates that there must have been an- tic is not in contact with the preoperculum. The other way to transmit the forces from the symplectic and quadrate are slightly inclined ante- opercular apparatus to the mandible. ro-ventrally to the hyomandibula in pycnodonts.

- A B 2 mm

Fig. 3. Jaw elements of iProscinete.\ elegnns (Agassiz 1833) from the Kimmeridgian (Upper Jurassic) of southern Germany showing foramen of mandibular sensory canal. A. Premaxillae (BSP-1885 IX 61). B. Right dentalosplenial (BSP-1885 IX 60). 140 Krhet. J.. Fccdine mechanisms and ecoloev of nvcnodonts

The reduced number of branchiostegal rays in elements in pycnodonts indicates a small bran- pycnodonts is t.triking. A reduced number is also chiostegal membranc and suggests relative small found in some primitive actinopterygians such as potential for opercular chamber expansion. haplolepids. redfieldiifornis. saurichthyids. and le- The branchial opening of pycnodonts was high pisosteiforms (Lambers 1991) and some teleosts but rathcr narrow, probably because of the fore- (McAllister 1 9 58). However. the lonxst number shortened skull and the reduced operculum. found in othx actinopterygians is generally three. Acinacjform rays are also present in Jaw apparatus: The jaw apparatus of pycno- tMiicroseiniris and f Pmpteurs (Bartram 1977) donts is unique. The upper jaw consists of paired and advanced eleosts (McAllister 1968). The re- premaxillac and maxillae as in other actinoptery- duction of the branchiostegal rays to two short gians (Fig. IA. B). But the premaxillae bear a

PasP met vo \ I I

/ b<

B

FIQ.4. \icrtical 5cc1ion (A) and its dra\tins (R)through ;in isol;itecI and Eraginentap skiill 01 tG,vi.odrt.s sp. froin the Oxforciian (L:ppcr Juraa\ic) o Chile displayin? internal characters niid ;irticulntion hr~\\ecmvonier and premaxilla. For further explana- tions sec text. ang. anplar hone b. reinailis of hi-anchial arches: met. mcscthmoid: pasp. p;irasphenoid: pc. processus coronoicleus; pm, prcinasilla: pmt. pi tiiimillai-y tooth: pra. prearticulai- hone: q. quadrate: vo. voiiiei-. Mitt. Mus. Nat.kd. Bcrl., Geowiss. Reihc 4 (2001) 1-17

single row of styliform or chisel-shaped grasping lateral surface of the skull. In some pycnodonts, teeth, whereas the maxillae are edentulous, as in the ventral margin of the maxillae is concave or most durophagous fishes. The lower jaw is com- deeply notched. Generally, the maxillae were an- posed of dentalosplenials, prearticulars, angulars, chored anteriorly by an articular peg. The articu- and articulars (Figs 1A, B, 2). lar peg fits into a shallow indent posteriorly to The premaxilla is composed of a tooth-bearing the premaxilla in most pycnodonts, with the ex- portion and the ascending premaxillary process ception of ~Mestuvu.~spp. and probably iAdim- (Fig. 3A). The ascending premaxillary process fvons sp., where the maxilla is rather narrow and roofs the snout anteriorly and covers one third long without any anterior articulatory peg. Com- of the length of the anterior mesethmoid edge in parison with Recent teleosts with similar denti- advanced pycnodonts. In some primitive pycno- tions (e.g., sparids, acanthurids) indicates the donts it is rather short and covered by the der- possibility, that the maxilla was fixed posteriorly methmoid bone or dermal tesserae (e.g., tGyro- to the mandibular arch by a ligamentum maxillo- dus, tAvduu,frons, and tMesturus; Fig. 1A). There mandibulare. is some confusion about the homology of the na- The lower jaw is suspended from the suspen- sal process of the premaxilla within neoptery- sory apparatus by the quadrato-symplectic-man- gians, e.g., in Amia (Grande & Bemis 1998). The dibular joint (Figs lB, 2). The mandible is short nasal process of Amia forms the most profound compared to that of primitive actinopterygians. part of the nasal cavity. But in pycnodonts, the and the prearticular makes up most of the man- process is completely superficial and is actually dibular arch. It was called “splenial” in the past like the superficial position of the ascending pro- (e.g., Lambers 1991) but may be the result of the cess of teleosts. There is no articular process of fusion of the splenial, a prearticular portion, and the premaxilla in pycnodonts. In advanced tele- probably coronoids. The paired prearticular osts, the articular process of the premaxilla is bones form a more or less pronounced basin, in well-developed and articulates with the prcmaxil- which the flat or convex oral surface of the vo- lary process of the maxilla forming the protrusi- merine dentition accurately fits during mandibu- ble upper jaw. Nursall (199913) reported, that the lar abduction. Both prearticulars meet medially connection between premaxilla and mesethmoid along a long and vertically oriented symphysis, was not tight in tMacromesodon rnacropterus which is either rather short (e.g., tHuclrocii/.s) or (BMNH 37109). This assessment was based on very long (e.g., tAnomoeodus and tlenzanja). X-ray photographs. In addition to this, a vertical Thurmond (1974) assumed, that both prearticu- section through an isolated skull of tGyrodus sp. lars were not tightly fixed and proposed a lateral from the Oxfordian of Chile was prepared to adductivehbductive mandibular action. How- elucidate the topology of cranial elements ever, Nursall (1999b) suggested that the prearti- (Fig. 4). It shows, that the ascending process of culars were tightly fixed and rejected the inter- the premaxillary bone is loosely attached to the pretation of Thurmond (1974). But the surfaces anterior surface of the mesethmoid bone with of the symphysis shows a rugose pattern indicat- some kind of articulation or attachment between ing the presence of some kind of connective tis- the premaxilla and the anterior edge of the vo- sue allowing some lateral movements during mer. No nasal depression is found on the snout mouth closure. to fix the premaxillary process as it is found in The dentalosplenials are rather slender and several advanced teleosts (e.g., Nanididae). The are firmly sutured antero-ventrally to the prearti- morphology of the premaxilla of primitive tele- culars in pycnodonts during life but got easily osts differs from that of pycnodonts. The pre- disarticulated and lost after death (Fig. 3B). The maxilla of ‘pholidophorids’ and ILeptolepis is angulars cover the postero-lateral portion of the small, and the ascending process is rather short, mandible (Figs lA, B, 2). The articulars lie medi- similar to the condition found in tMesturus. ally to the angulars. There is no independent ret- Nevertheless, it is assumed, that the premaxilla roarticular ossification. of these teleosts was already mobile (e.g., Patter- Distinct coronoid ossifications are not present son 1977, Lauder 1982). The premaxilla has be- in pycnodonts. A distinct and stout process is come secondarily firmly fixed to the neurocra- tightly fused postero-lateral to the prearticular nium in several predaceous teleosts as Hoplias bone (Figs 1, 5). This process is usually called and Salmo (Lauder 1982). coronoid process, although the bones included in The maxillae of pycnodonts are easily lost the coronoid process are different in actinoptery- after death due to their loose attachment on the gians. Consequently, the coronoid process of pyc- 13s Kriwet. J.. Feedine mechanisms and ecology of uvcnodonts

pra ang ait q hh syrn cha POP art < - __ A B

Fig. 5, Mandibular articulation in some p!,cnodonts. A. t.\.itrc.,.o/iiesotlo/i sp. (BMNH P.11774), left side. B. tMacromcwdon sp. (BMNH 37109). rirht side. Scale bars = 5 mm. Arrows point to anterior. ang. angular bone art. articulai- bone: cha. anterior ceratohyal: chp. posterior ceratohyal: den, dentalosplenial; enp, endopter- ygoid: hh. hypohy. il: io. infraorhital: mpt. metapterygoid: ni. maxilla: pc. processus coronoideus; pop. preoperculum: pra. pre- articular bone: q. c,uadrntc: sym. aymplectic. nodonts is not homologous to that of 'palaeonis- restricted to the unpaired vomer in the roof of coids' or teleosts. The presence of a coronoid the mouth and the paired prearticulars, premaxil- process was c(msidered a neopterygian synapo- lae. and dentalosplenials (Figs lA, B, 3, 6). The morphy by Gardiner (1984). However. a well-de- teeth are rigidly fixed to these bons. Sometimes, veloped 'coronoid process' was demonstrated for the teeth are embedded in shallow depressions primitive 'palxoniscoids' by Gardiner (1967) or sit on small bony elevations. There is only a and Gottfried (1992). This contradicts the as- single generation of teeth; the teeth are not re- sumption of direct correlation between presence placed (Kriwet 2001). of a 'coronoid process' and a free maxilla in Each premaxilla and dentalosplenial bars a 'subholosteans' as proposed by Schaeffer (1956). single series of few styliform or incisiform teeth The mandibular articulation in pycnodonts is (Fig. 3). The vomcrine and prearticular teeth are special, with sii nilarities to the mandibular articu- molariform and generally arranged in longitudi- lation of halec imorphs (Nursall 1996b. 1999a. b. nal rows forming a more or less dense pavement Kriwet 1999a. 2001). For descriptions of the (Fig. 6). Usually, there is a distinct main tooth mandibular articulation of haleconiorphs com- row. which is characterised by the largest teeth pare Patterson (1973, Olsen (1984). and Grande and a varying number of medial and lateral 8r Bemis (1958). In contrast to halecomorphs. tooth rows. both quadrate and symplectic take part in the mandibular ar iculation in pycnodonts with the Hyoid apparatus: The morphology of the quadrate lying vertical to the symplectic and hyoid arch of pycnodonts corresponds to the both are geneially closely arranged in the same general pattern found in non-teleostean actinop- plane (Figs 2 4. 5). The similarity between terygians. It consists of a single hypohyal, an amiids and pjcnodonts in mandibular articula- anterior and a posterior ceratohyal, and an inter- tion is, that bo:h quadrate and symplectic arc in- hyal (Fig. 1A. B). The anterior ceratohyal sup- volved. But ir amiids, the quadrate articulates ports the two branchiostegal rays on each side of with the anteri ir articular element (Bridge's ossi- the head. It is generally short with a notched cle 'c') and thc symplectic with the posterior one ventral margin and a plate-like posterior portion (Bridge's ossicie *d*).the whole complex being in lateral aspect. The anterior ceratohyal of pyc- invested with :i well-developed articular capsule. nodonts is very similar to that found in several This articular :apsule may have been also pre- teleosts and macrosemiids (Bartram 1977, Lam- sent in pycnodlmts. hers 1991). but the pycnodont one is smaller in Pycnodonts have been defined by their unique respect to the skull and more irregular. The hy- tooth morphology and arrangement. Teeth are pohyal and the rod-like interhyal are also small Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 4 (2001) 119

Fig. 6. Isolated dentitions of tcyrou’us planidens Woodward 1895 (MB. f.7173) from the Upper Jurassic (Tithonian) of We!- mouth, England. A. Vomerine dentition. B. Right prearticular dentition. Scale bar = 10 mm.

but generally well-ossified. The attachment of deglutition. Unfortunately, their branchial skele- these bones to each other or to any part of the ton is badly preserved due to disarticulation and suspensorium and/or opercular apparatus is un- other taphonomic processes. Therefore, informa- clear but may have been articulated via broad tion is very limited, and it is impossible to recon- cartilaginous surfaces with each other as it is struct the branchial skeleton of pycnodonts. found in inany extant actinopterygians. There Traces of gill filaments and branchial arches are may have been ligamentous connections between found in many specimens, both mechanically and the hyoid arch and the mandible, the suspensor- acid prepared (Fig. 4A, B). The ceratobranchials ium, and/or pectoral girdle. are easily discernible. They are U-shaped in There is no epihyal, basihyal, and urohyal in cross section, the U opening posteriorly. Gill fila- pycnodonts. ments arise from the hollow of the U. There are five ceratobranchials present. Other Structures Branchial apparatus and branchial and elements may correspond to the pharyngo-. teeth: The branchial skeleton and its asso- epi-, and hypobranchials. But they are too scat- ciated elements vary among fossil and extant ac- tered for accurate identification. The best pre- tinopterygians. The branchial chamber is closely served structures found in the branchial chamber associated with respiration and feeding and the of pycnodonts are branchial teeth (Kriwet 1999b, associated muscles play important roles during 2001). 150 Kiiuet. J . Feeding mechanisms and ecology of pycnodonts

Myology, ligaments, and arthrology pothesised to be the sister group to halecostomes + the fossil aspidorhynchiforms within neoptery- The knowledge. of the myology. the arrangement gians (Kriwet 2001). In addition, the soft tissues of ligaments, a id the joints or couplings between and the arrangement of muscles and ligaments in bony structure are also important to understand the skull of extant sparids, acanthurids, nandids, the kinematics during feeding. Unfortunately. the and Anarrliichas liips, which are assumed to be reconstruction of soft tissues in exclusively fossil similar to pycnodonts in their dentition and to known taxa is speculative as mentioned above. some extent also in their skull-shape, and some Nevertheless. t aere are many osteological related extant rani-feeding teleosts (e.g., Amia, Lampro- features like tclberosities. crests, grooves. fenes- logus) have been studied for comparison (Fig. 7). trae, fossae. fo .amina. and septa and the absence A tentative reconstruction of the superficial head of bones (e.g.. interoperculum. urohyal) that al- musculaturc participating in feeding of pycno- low some assel tions about soft tissue anatom!. donts is presented in Figure 8 based on these comparisons. It is assumed, that pycnodonts pos- My o 1 (I g y : The interpretation and reconstruc- sessed at least a tripartite adductor maiidibulae tion of soft tissues and joints related to feeding with the superficial part of the m. adductor man- in pycnodonts are based on the situation in dibulae (Fig. 8: A,) originating from the straight Amia and tek osts. because pycnodonts are hy- anterior margin of the preoperculum and the

LAP EP AOP Da LAP AOP EP LOP

IML AAP AM2 AM1 iop pop sop mx Ak lML AM2 A B pa

AM2 AM3 iop pop C rig. 7. Lateral htx d musculature of different teleosls. A. Lroiipdogrrc rrrr~1~rrr.x.a ram feeder. Modified aftcr Liem (19%). B. A/iurr/iicfio\ Irr, I//.\. 3 shell crusher. Modificd after Dohhen ( 19.37). C. Scrrrrrr ,.irhro~,ioltrcc.irs.a herbivore actinoptcrygian. hlodilierl altcr C'lcment\ cEr Bell\\ood ( 1WS). AAI? adductor arc us palatini niuscle5: AMl. AM2. AM3. di\ isioiis of the adductor niandibulac muscles; AOP, adductor oper- culi niuwlt.: den. ~~iitalosplenial:EP. epaxial muscles: IML. interoperculo-mandibular ligamcnt: iop, interoperculum: LAP, le\ ator arcus pala ini niuxlr: LOP. Ic\ ator operculi muscle: nix. maxilla: n. nasal hone: op. operculum: p. palatine arch: pa, parietal hone: pasla. pirasplienoid: pin. premasilla: pop. preoprrculum: sop. suhoperculum: vo, vomer. Mitt. Mus. Nat.kd. Bcrl.. Geowiss. Reihe 4 (2001) 151 head of the hyomandibula, whereas the other lar process (pers. obser. in lemanjn). This may parts of the adductor mandibulae muscles must indicate, that those pyciiodonts had a less devel- have been inserted on the angular bone and oped palatine muscle complex. The palatine mus- probably along the postero-lateral surface of the cle complex is important for feeding and respira- prearticular bone. An indication for this is found tory in actinopterygians (e.g., Winterbottom in tAnornoeodcts spp., where the lateral (oral) 1974, Lauder 1980b) and assisted ingestion and border of the long prearticulars is rather broad swallowing of prey. However, the size of the pa- and exhibits a rugose surface. There is no reason latine muscle complex is an adaptation to the to believe, that the adductor muscles were not available space (Osse 1969). expanded above the suspensory apparatus onto There are two muscles (adductor and levator the side of the cranium as in extant shell-feeders muscles) between the neurocranium and the op- with deep skulls (e.g., Anarrhichas). ercular apparatus, that mediate the motion and Nursall (1999a) reconstructed a very large pa- rotation of the opercular apparatus in Recent latine arch muscle group consisting of levator actinopterygians. The condition of muscle inser- and adductor palatini, protractor and adductor tion, which are responsible for motion of the hyomandibulae, and levator and dilatator oper- suspensorium and related bones is different in culi muscles in pycnodonts without distinctive teleosts, where they inserted on the medial sur- hyomandibular head (e.g., Mesturus, Ardua- face of the large and free operculum. and in from). This muscle complex originated from the pycnodonts, where the operculum is sinall and massive prootic and sphenotic and inserted on sutured to the postero-dorsal margin of the operculum, pterygoquadrate arcade, and hyo- large preoperculum. In addition. the preopercu- mandibula. There are only minor traces of mus- lum is tightly fixed to the underlying hyomandi- cle attachment on the sphenotic and prootic bula. Therefore, I hypothesise, that the inser- bones in pycnodonts with hyomandibular condy- tions of most of the adductor and probably the

EP

PPe

LAP AOP LOP

Fig. 8. Tentative restoration of lateral head musculature of a generalised ad- OP vanced pycnodont. Thc adductor iiiaii- dibulae muscles of pyciiodoiits such as tMestunrs and t Gyrotlus are covered by skull elements and not exposed. POP AAP. adductor arcus palatini muscles: AMl, AM2, divisions of the adductor mandibulae muscles: ang. ongular bone: AOP. adductor operculi muscle: cha. anterior ceratohyal: clip. postcrior cl ccratohyal: cl, clcithrum: den. denta- losplenial: dso. dermosupraoccipital: EP. epaxial muscles: hyo. hpomandihu- la: LAP, levator arcus palatini muscle: LOP, levator operculi musclc; met. mesetlimoid bone: mx. maxilla: or. or- bit; op. operculum; pa. parietal hone: pasp, parasphenoid: pm. preniaxilla: pop. preoperculum; pp. postparietal bone: ppe. postparietal process: pra. prearticular bone: vo. vomer. 152 Ki-iblet. J.. Feeding mrchariisms and ccology of pycnodonts complete levator muscles have been shifted toral girdle was mainly fixed by ligaments to the from the dorszl margin of the operculum to the neurocranium: only minor indication of muscles head of the hyomandibula and the upper edge have been found so far in Gyrodrts, lemanjtr, and of the preopt rculum (Fig. 8). Consequently. a Coelotlzrs (e.g.. typical rugosities). distinct levato - muscle. which originated from The epaxial musculature plays an iniportant the operculum was not developed. This is espe- role in cranial elevation during mouth opening. cially evident n tq\~c/iotlzrs.which lacks the op- It generally extents anteriorly on the dorsal sur- erculum comrletely and is supported by the face of the neurocranium in living neopterygians, presence of riigosities and sniall crests on the e.g.. Scrrriis spp.. Antrrrhichas. In pycnodonts, medial surfact of the hyomandibular head in epaxial niu\cles wcrc attached to the medial sur- pycnodonts. faces of the large post-temporal fossae and the Thc operculir process also plays an important lateral sides of the supraotic crest, at least in role in expanc ing the buccopharyngeal cavity in pycnodonts without caudally directed postparie- teleosts. becatise it assists in abduction. adduc- tal brush-like processes such as tArdunfrons, tion. and rotalion of tlic operculum. But pycno- iG YI'O di I P, t Mesti 1 ri is, and f Micropycn o don. donts lack an Iipercular process for muscle inser- Nevertheless, the lateral surfaces of the supraotic tion. crest exhibit almost no traces of muscle attach- Consequently, the hyomandibula must be re- ment. Many pycnodonts have postparietal pro- garded as a m-Ijor key element in expanding the cesses (postparietal peniculus of Nursall 1996b), buccopharyngt al cavity in pycnodonts. because that are brush-like and fixed to the medial sur- most of the inuscle masses (c.g.. m. adductor face of the postparietal bones. They represent hyomandibulac:). that mediate the rotation and osseou\ extensions of occipital tendons and have motion of the opercular apparatus and suspen- formed an attachment for the upper, anteriorly sorium originate and insert from the well-devel- directed extension of an anterior myoseptum oped hyomanc ibula. (Nursall 199%). Thus, the postparietal processes The ventral head muscles of pycnodonts ~vere would have increased and concentrated the con- possibly different in arrangement and develop- tractile forces of the anterior epaxial rnyomeres, ment from th sse of other neopterygians. since resulting in cranial elevation. the prearticu1.m are large and fused along a long s)imphys:al line. For instance. it is sug- L i g a m e n t s : The reconstruction of ligaments is gested. that th.: 111. hypohyoideus has nevcr been extremely difficult, because the osteologically re- developed or was secondarily reduced. because lated features such as tuberosities, crests, grooves pycnodonts 1al:k a suboperculum (Kriwet 2001 ). etc. are almost always obscured by fractures or But pycnodonts certainly had a muscle mass si- sediment. However, the anatomy of the skull milar to the s,.ernnhyoideus. The m. sternohyoi- provides some information on the ligamentous deus is generaily a large muscle. that lies deep to network (e.g.. niaxillo-mandibular). the superficial layer of the ventro-lateral muscles The maxilla of most pycnodonts was not in extant teleosts. It originates from the clei- firmly fixed to the cheek, but was mobile in thrum and inxrts on the urohyal. It is rather many pycnodonts. The mobility and movement speculative to assume a sternohyoid muscle fcor of the maxilla during mouth opening and mouth pycnodonts. b(:cause they lack an urohyal. How- closure is supported and augmented by the liga- ever. a similar muscle mass must have been pre- ment niaxillo-mandibular (= ligamentum primor- sent. that un ted the pectoral girdle and the diale) in teleosts. There is no reason to believe hyoid apparat ils to mediate the posterior-direc- the condition in pycnodonts to be different from ted translatioil of the hyoid apparatus during that of teleosts. I suppose, that the maxillo-man- mandibular dt pression. I hypothesise. that there dibular ligament originated at the posterior mar- was a small ar d short muscle. that connected the gin of the maxilla and inserted on the mandible both dentalosrdenials at the anterior part. bvhich in the region of the coronoid process. The liga- was similar tc the 111. intermandihularis portion ment follows the abduction of the mandible and of the geniot yoid muscles of extant halecos- becomes taut, pulling the posterior part of the tomes. maxilla ventrally. It augments the action of the The reconstruction of muscles. that originate ni. adductor mandibulae during the initial phase from or inser on the pectoral girdle is rarely of mandibular adduction and conducts the maxil- possible due t) the preservation of most pycno- la back to its original position during mouth clos- dont specimens. It is assumed here. that the pec- ing where it is held by the ligament. Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 4 (2001) I53

There were certainly also ligaments between pensorium joints. The palato-quadrate-parasphe- the other functional units elements (e.g., hyoid noid consists of the metapterygoid, which articu- and branchial apparatus). However, a recon- lates anteriorly with the parasphenoid below the struction of those ligaments is impossible. orbit in the snout in pycnodonts. This joint is in- Pycnodonts lack an interopercular bone and terpreted as synapomorphy of pycnodonts by consequently the interoperculo-mandibular liga- Nursall (1999b). ment, which connects the mandible to the oper- The joints of the upper jaw of pycnodonts are cular apparatus. Thus, there is no connection be- different from that of teleosts. The premaxillo- tween the jaw and the opercular apparatus as in neurocranial, the maxillo-prevomerine, and the halecostomes and teleosts. This interpretation is maxillo-premaxillary joints are not present. The also supported by the reduced size of the preo- rather short ascending arm of the premaxilla perclc (J.R. Nursall, pers. comm. 2001). A similar found in some pycnodonts. e.g., tGyrodzis and condition is also found in primitive actinoptery- tMesturus, indicates, that the premaxilla was not gians like ‘palaeoniscoids’. mobile but more or less fixed to the cranium. This arrangement probably supports stronger A r t h r o 1 o g y : The suspensorium apparatus of bite. But in most pycnodonts the dorsal ascend- pycnodonts forms a narrow, functional triangle. ing arm of the premaxilla is rather long and The three angles are represented by the cranio- superficial, not fitting into a rostra1 fossa on the hyomandibular, the palato-cranial, and the dorsal aspect of the neurocranium (premaxillo- mandible-suspensorium joint (Nursall 1996b, Kri- neurocranial joint of teleosts). It is not firmly wet 2001). fixed but free and moves with the maxilla. The The cranio-hyomandibular joint is similar to joint between premaxilla and maxilla usually that found in Recent teleosts but it is not uni- consists of an articular process on the antero- form in pycnodonts, depending on the morphol- medial aspect of the maxilla. A distinct articular ogy of the head of the hyomandibula and the process of the premaxilla is lacking. associated fossa on the endocranium, e.g., oval in The branchial apparatus is suspended from the iGyrodzu, circular in th’eoproscinetes. It is usual- endocranium by the first pharyngobranchial. The ly synovial with an articulation head on the hyo- junction between the pharyngobranchial and the mandibula (e.g., tfemanja palma, Kriwet 2001). endocranium was ligamentous or there was con- tMestitriis is lacking such an articulation head nective tissue. (Nursall 1999a). The groove for the hyomandibu- In addition, the junctions between the bran- lar articulation is formed by the sphenotic and chial elements was certainly cartilaginous. The pterotic bones. In contracts, the hyomandibula cartilaginous epiphyses are useful to mininiise articulates dorsally into a cartilaginous groove in any shock to the branchial system during biting Amin. that is mostly located under the dermop- and allows simultaneous movements by the terotic (Grande & Bemis 1998). transmission of muscular forces. The palato-cranial joint of pycnodonts differs The hyoid apparatus of pycnodonts consists of from that of Amia and teleosts. It is formed by anterior and posterior ceratohyals, a hypohyal, the palatine process of the entopterygoid. The and an interhyal. Each anterior ceratohyal sup- palatinal process of each entopterygoid articu- ports two branchiostegal rays. The junctions be- lates with the posterior end of the vomer. Usual- tween these bones to each other or to any part ly, the palatine complex articulates with the eth- of the suspensorium andlor opercular apparatus moid complex and the maxilla and forms a were probably ligamentous and/or cartilaginous. palato-maxillary joint in teleosts, which is absent But no indications to support such a connection in pycnodonts. have been found so far. The mandible-suspensorium joint consists of There is no distinct operculo-hyomandibular two articular surfaces of the quadrate and the joint as in teleosts and in Amia. Nevertheless. symplectic bones. This kind of articulation is Lambers (1991, 1992) reported a vestigial oper- rather peculiar in pycnodonts and similar to that cular process in t Gyrodus, which would mean. found in Amid. Both quadrate and symplectic that the operculum is free. However, no vestigial take part in the mandibular articulation (see opercular process was found during this study. above). The operculum articulates tightly with the preo- Other joints arc the palato-quadrate-parasphe- perculum. The hyomandibula is fixed to the noid, premaxillo-maxillary, branchial apparatus- medial surface of the preoperculum. neurocranium, hyoid-opercular, and hyoid-sus- 154 Kriwet. J.. Feeding mechanisms and ccology of pycnodonts

The ecomorphology of the pycnodont skull design. But it is not possible to reconstruct the behaviroal parameters of fossil organisms. There- The mode of leeding is especially obvious in the fore. I suggest, that the best way to reconstruct dentition of vertebrates. Usually, the feeding pre- the ccomorphology of a fossil organism is to use ferences are deduced from the morphology and the information obtained from the skeletal anat- number of tee h. It is generally accepted. that the omy of the head and anterior body in combina- morphology o an organism is controlled by the tion with the data from soft tissue reconstruc- environment and that the optimal connection be- tions. from the joints betwccn functional units, tween form acd function of an organism and the and from the general shape. environment ij the result of natural selection. The buccopharyngeal cavity of extant actinop- This discovery resulted in the drafting of the eco- terygians was described as changeable pipe or morphological paradigm (e.g., Davis & Birdsong cone. that can be expanded and compressed in 1973. Bare1 1083). The ecomorphological para- various ways by the action of the muscles, based digm. as curre itly accepted. means. that the mor- on functional morphological analyses of the feed- phology of the skull relates to how the organism ing apparatus of teleosts (truncated cone model, feeds. and accepts a close fit between feeding e.g.. Ossc & Muller 1980) (Fig. 9). The bucco- morphology and prey capture and processing. pharyngeal cavity of deep bodied teleosts (e.g., Thus. interspec ific and even intraspecific variation Calariiiis sp.) can be described as cone-shaped in morphology is correlated to differences in diet. pipe (Fig. 9A). The co-ordinated activity of the However. tl-e application of the ecomorpholo- epaxial muscles, sternohyoideus, levator arcus gical paradign? without a broad conceptual fra- palatini. and dilatator operculi muscles in con- mework may lead to misinterpretations. because nection with spreading of the branchiostegal many ecomor~~hologicalstudie5 either treat the membrane results in the explosive expansion of ecological sigr ificance of morphological appear- the cone-shaped buccopharyngeal cavity. This ances without knowledge of their function or produces a steep negative pressure in the buccal endless data : ets of various measurements are cavity. In contrast to that, the buccopharyngeal collected in tke hope of finding any significant cavity of ram feeders (most primitive actinopter- patterns. Lieni (1993) stated. that behavioral ygians including the ‘palaeoniscoids’ and preda- parameters of en play a greater role than skull cerous teleosts) is represented by a cylindrically

SOC

soc hvo

mx den pop iop sop

den art q pop iop sop A B

Fig. 9. The niorph ,logy of the buccopharyngeal cavity of telemts presented as conc. A. Ctrltinz//ssp.. a shell crusher. B. Scrlrno sp.. a rain-feeder. art. articular bone. den. dentalosplenial: hyo. hyomandibula: iop. interoperculum: la. lacrimal: mx, maxilla; n. nasal bonc; op, operculuni: p. pal: tiiic arch: pa. parietal bone: pasp. parasphenoid: pm. premaxilla: pop, preoperculum; pp, postparietal bone; pt. posttemporal bane: q. quadrate: scl. supracl~itlirum:SOC. supraoccipihl hone: sop. suboperculum. Mitt. Mus. Nat.kd. Berl.. Geowiss. Reihe 4 (2001) i 5.5

shaped buccopharyngeal cavity producing very The skull of pycnodonts displays most charac- small negative pressures (e.g., Lauder 1980c; ters typical for suction feeding such as a deep Fig. 9B). Compression of the buccopharyngeal skull with well-developed supraotical crest, a cavity is effected by actions of the adductor man- deep and vertical suspensorium, an elongated dibulae, adductor arcus palatini, and geniohyoi- and highly differentiated levator arcus palatini deus muscles in extant actinopterygians. muscle, a protrusible upper jaw, short mandibles Thus, the basic feeding patterns of actinoptery- and maxillae, and a small mouth gape. However. gians are ram feeding, biting, and suction. Many pycnodonts lack the urohyal and consequently generalised teleosts combine elements of all associated musles (e.g., m. geniohyoideus) and three patterns in response to the functional de- ligaments as they are found in extant actinopter- mands presented by particular prey, e.g., fixed to ygians. The buccopharyngeal cavity represents a the substrate or free-swimming in mid- or sur- truncated cone when the diameter of the rather face waters. Liem (1993) proposed suction feed- small mouth opening is connected with the dia- ing based on the findings in Hemitilapia oxy- meter of the esophagus at the level of the bran- vhynchtrs as generalised morphological pattern. chial teeth (Fig. 10). The morphology of the trun- Suction feeding is related to a deep skull, well- cated cone is very similar to that found in developed supraoccipital crest for insertion of teleosts with strong suction kinematics (e.g., par- well-developed epaxial muscles, deep suspensor- rot fishes). This would indicate, that pycnodonts ium to accommodate an elongate and highly dif- may have created steep negative pressures in the ferentiated levator arcus palatini muscle, a pro- orobranchial chamber when the mouth was trusible upper jaw, rather short mandibles and opened to overtake prey. However, the rather maxillae, small gape, cone-shaped design of the small branchiostegal membrane may have lim- buccopharyngeal cavity, and a well-developed ited the creation of a steep negative pressure urohyal in extant teleosts. Teleosts without jaw during mouth opening. Consequently, suction teeth but with well-developed pharyngeal denti- feeding was not as effective as in comparable cx- tions show the largest cone-shape (e.g., cichlids). tant teleosts. The biting pattern is lost in these teleosts.

Fig. 10. A. Truncated cone model of a generalised pycnodont while mouth is closed. The small end of the cone terminates at the mouth and the large end deep within the buccopharyngeal cavity. B. Truncated cone model of a generalised pycnodont while mouth opening. Expansion of the buccopharyngeal cavity by rotation of the opcrcular apparatus and suspensoriuni creates a negative pressure, drawing water into the mouth. Arrows indicate the dircctions of muscle contraction and move- ment of associated skeletal elements. AAP. adductor arcus palatini muscles: EP, epaxial muscles: LAP, levator arcus palatini musclc: LOP. levator operculi muscle. 156 Krinct. J.. Feeding mechanisms and ecology of uvcnodonts

Feeding kinematics Pycnodonts are hypothesised to have devel- oped structural innovations compared to prinii- As halecostolr es, pycnodonts retained the cou- tive actinopterygians, but which are also found in pling of primil ive actinopterygians (Fig. 1 1 ): the halecomorphs and teleosts, e.g., palatine arch epaxial-neuroc -anium coupling. that elevates the muscle group consisting of levator and adductor skull and a ventral coupling involving the hypax- palatini. protractor and adductor hyomandibulae, ial muscles. clc ithrum. and sternohyoideus appa- and levator-dilator operculi muscle group. The ratus. The gel-iohyoideus was probably absent. arcus palatini muscle, which is absent in primi- because of the lacking urohyal (see above). Cra- tive actinopterygians (Fig. 11) connects the neu- nial kinesis is I ather common in actinopterygians (e.g., Schaeffer & Rosen 1961. Liem 1979) and is related to the actions of mouth opening and clos- ing, especially to the movement of the upper jaw. The postzro-dorsally directed rise of the skull is supported by the epaxial musculature of the body. nu,, there are rather large insertion areas for epaiial musculature on the posterior neurocranium in extant teleosts, when cranial . [PFCTORALl kinesis is we1 1-developed. Large posttemporal fossae separatt d by a median supraotic crest oc- cur in pycnodonts (Nursall 1996b. 1999b. pers. observ.). The i ntero-dorsal portions of the epax- t ial myomeric nuscles were fixed to the medial anterior surfaces of tht. fossae and the median crest of Fig. 12. Structural network in the head of halecomorphs re- the supraotic 1- one probably by occipital tendons lated to mouth opcning and suction feeding. Solid rectangles: bony elements: parallelograms: muscles: interrupted rectan- similar to the condition found in many extant gles: ligaments. Modified from Lauder (1 982). actinopterygialks (e.g.. Gemballa 1995). There- AOP. adductor operculi muscle: EP, cpaxial muscles; GH. fore, it is suggested. that cranial kinesis was also genio-hyoideus muscle: HY. hypaxial (obliquus inferioris) musculature: IML. interoperculo-mandibular ligament; LOP, efficient in py xodonts. The brush-like. internal levator operculi muscle: MHL, mandibulo-hyoid ligament: extensions of he postparietals (parietal penicu- MML. mnxillo-mandibular ligament; SH, sterno-hyoideus lus of Nursall 1996b. 1999b). that is present in musk advanced pycr odonts. formed an additional at- tachment for :ollagen fibres from the anterior myosepta and iugments the action of the epaxial muscles (Fig. 8 I.

@ "EUR0CRAN'UMJ4 / / jxEq & PROTRUSION OPENING

~PERCULUM~

anterior

Fig. I.?. Complex structural nctwork in the head of teleosts - related to mouth opening. upper jaw protrusion, and feeding. anterior Solid rectangles: bony elements: parallelograms: muscles; in- tcrrupted rectangles: ligaments. Modificd from Lauder Fig. 1 I. Structural network in the head o! 'palaeoniscoids' re- ( 1982). lated to mouth or ening and feeding. Solid rectangles: bony AMl. first division of the adductor mandibulae muscles: elements: parallel(~gi-ams:muscles: interrupted rectangles: li- AOP. adductor operculi muscle; EP, epaxial muscles; GH. eaments. Modified from Lauder (1982). 9enio-hyoideus muscle: HI: hypaxial (obliquus inferioris) AOP. adductor oljei-culi muscle: EP. epaxial muscles: GH. musculature: IHL, interoperculo-mandibular ligament; IML, cenio-hyoideus m .iscle: HY. hppaxial (obliquus interioris) interopcrculo-mandibular ligament; LAP, levator arcus palati- musculature: MHI ,. mandihulo-hyoid ligament: SH. sterno- iii muscle: LOP. levator operculi muscle: MML, maxillo-man- hvoideus muscle. dibular ligament: SH. stcrno-hyoideus muscle. Mitt. Mus. Nat.kd. Berl., Geowiss. Rcihe 4 (2001) 157

A -anterior B -anterior Fig. 14. Structural network in the head of pycnodonts. A. During mouth opening. B. During bottom and suction feeding. Solid rectangles: bony elements; parallelograms: muscles; interrupted rectangles: ligaments. AOP, adductor operculi muscle; EP, epaxial muscles; GH, equivalent to genio-hyoideus muscle of teleosts: HY. hypaxial (obliquus inferioris) musculature; LAP, levator arcus palatini muscle; LOP, levator operculi muscle: MHL, niandibulo-hyoid ligament; MML, maxillo-mandibular ligament; SH, equivalent to sterno-hyoideus muscle of teleosts.

rocranium with the suspensory apparatus and maxilla is moved anteriorly. Angular-maxillary supports the mandibular depression by levation swing is initiated by neurocranial elevation of the suspensorium (Figs 12, 13, 14: LAP). The (epaxial neurocranial coupling). In pycnodonts, m. adductor arcus palatini lies medial to the m. the maxilla is free and movable in more ad- levator arcus palatini. The action of the adductor vanced pycnodonts with the exception of tArtiun- arcus palatini muscles was probably that to draw frons and tMesturus and probably also of the hyomandibula and the pterygoid arch inward +Hadrodus and tMicropycnodon. The maxilla is and forward. It is hypothesised herein, that the generally large and wide, always edentulous and suspensorial abduction is caused mainly by the forms the postero-lateral margin of the mouth m. levator arcus palatini and probably the the cleft. It was anchored anteriorly by ligaments levator portion of the operculum muscles, and an articular peg, that was situated in a whereas the hyoid apparatus apparently did not groove posterior to the premaxillary process in take part in the abduction of the suspensory ap- most pycnodonts (except in Mesturus and closely para tus. allied genera as tArduafrons). It is hypothesised, It is also proposed herein, that the levator and that during mandibular abduction the maxilla dilatator operculi muscles, two structural speciali- would swing antero-ventrally caused by the 1. sations, which are found in halecostomes, have maxillo-mandibularis on its neurocranial pivot. been shifted mostly from the opercular appara- forming a sidewall to the buccal opening pre- tus to the suspensorium, because of reduction of venting water flow into the oral cavity from the the operculum (Fig. 14, LOP, AOP). The levator corners of the mouth. Two forces are generally is thus not a distinct muscle. In addition, the in- important in maxillary swing. The force resulting teropercular bone with the interopercular liga- from the mandibular depression is transferred to ment, which are important structures in teleosts the maxilla via the maxillo-mandibular ligament, for mouth opening, are absent in pycnodonts. so that the distal portion of the maxilla is moved There are other possible structural innova- anteriorly. Progressive increase of the 'coronoid' tions, which arc related to control of water flow process height reduces the slack in the maxillo- and suction feeding in teleosts (Fig. 13). In con- mandibular ligaments, which are inserted near to trast to primitive actinopterygians, where the or even on it, increasing the efficiency and speed maxilla forms the lateral wall of the adductor of the jaw movements. In addition, a torquing chamber, the maxilla becomes free from the force is brought to the antero-medial process on cheeks and pivots on a medially directed process the maxilla, when the neurocranium is elevated posterior to the vomer. The maxilla swings extre- by the epaxial muscle initiating the forward mely forward during mouth opening. The force, swing of the maxilla. The maxillary swing results that results from the mandibular depression is in antero-posteriorly oriented streamlines, which transferred to the maxilla via the maxillo-man- increase the velocity of water flow into the oral dibular ligament, and the distal portion of the cavity. But it also would play against the premax- 158 Krinet. J.. Feeding mechanisms and ecology of pycnodonts illary process Nith its antero-medial articulation ((;oslitie 1965). The orientation of the m. adduc- peg. so that tlie premaxilla consequently moves tor mandibulae also plays an important role in slightly forward enlarging the buccopharyngeal increasing the biting force. The more vertical the cavity. In addilion. the medial and anterior por- orientation of the m. adductor mandibulae, the tions of the niaxillo-niandibular ligament insert greater is the resulting biting force. The effec- on the ventral surface of the premaxilla in many tiveness of short jaws and vertical orientation of extant actinor terygians. This arrangement was adductor muscles was demonstrated for extant probably also present in pycnodonts. Thus. low- teleosts such as Avzrirrhichns and Esox by Dob- ering of the lower jaw results in pulling the max- hen (1937: Fig. IS). The relationships between illa antero-ven rally. which causes upper .jaw pro- econiorphologically relevant elements such as trusion. It can be assumed. that the protrusion of jaw length. orientation of adductor muscles, and the premaxilla is also supported by the lips in its biting force found in Annrr.hzchas can be trans- final stage. eiihancing grasping or nipping at ferred to pycnodonts. The mandible of pycno- prey more efft ctively. Upper jaw protrusion was donts is rather short with well-developed 'coro- a structural n ivelty in pycnodonts, which was noid' process. This, the almost vertical not achieved 1)y halecomorphs. Forward protru- suspensorium, and the deep and foreshortened sion of the inandible happens simultaneously skull indicate, that the adductor muscles have with protrusioii of the premaxilla. The protrusion been large. and more or less vertically oriented of the upper j; ws is well marked in extant deep- reaching far up the lateral side of the neurocra- bodied actinopterygians (Alexander 1970). nium. The development of a temporal opening The vomer fits more or less accurately into the in the side-wall of the dermocranium in some U- or V-shapcd basin. which is formed by the higher pycnodonts is related to an increase of paired prearticulars acting thus as a mortar for adductor muscle mass and improvement of its the pestle (the wirier). when the mouth closes. action by providing extra space during muscle The long and vertically oriented symphysis of contraction. the prearticulars exhibits tuberosities and The morphology of the mandible and the dor- grooves sugge. ting connective tissue between the so-ventrally arranged quadrate-symplectic-man- two halves of the lower jaw. There is no reason dibular joint with supposed extensive cartilage to believe. tha there was not at least minor lat- and connective tissue filling of the articular sur- eral adductive and abductive mandibular action faces and capsules suggest, that mandibular as postulated by Thurmond (1971. 1974). Lateral movement had its fulcrum on the symplectic-ar- movements of the mandibles may have been ticular connection (Nursall 1999b). There was very limited but would increase the volume of the orobranchial chamber during mouth opening when the susFensorium and the mandibular ar- ticulation are I otated outwards. The inflection of the parasphenoid is also related to jaw function in pycnodonts. It deepens the foundations of the vomer. the relatively fixed element of the A "grinding mill". and strengthcncd the base of the vomer. serving to disperse the forces applied to it during biting. But it also foreshortens the skull including the :nandible. since the suspensorium maintains a slight forwardly directed projection. LT...... Lz' ...... ;..' This also decrc ases the potential mouth opening. f ..' f ,,,..-" ,.I. The preopercidum of pycnodonts is large and - ._. B C lateral. but its anterior margin provides a firm line of attachrr ent for mandibular adductor mus- Fie. 15. Schematic models showing the relationships bctwccn cles. It is hypc ithcsised. that musculi adductores length of mandihle. orientation of adductor muscles mandibulae wxe attached to the strong coro- (strippled line). angle between maiidible and suspcnsorium. and the resulting biting force (f) as function of thcsc para- noid process. increasing the strength during meters. A. E5o.i hrc?r/.s. a ram feeder. B. Annrrhichns h/pii.s. a mouth closing. The biting force resulting by the shell crushei-. C. Geiicralised pycnodont. No1 to scale. It is action of the adductor mandibulae muscles is evidcnt. that the resulting biting force (f) is greater in acti- nopteryTians with short mandibles, more vertical suspensor- considerably ir creased by short jaws and vertical iuni. and deep skull (B and C) than in predacerous teleosts orientation 01 adductor niandibulae muscles with long .jau elements (A). Mitt. Mus. Nat.kd. Berl., Gcowiss. Reihe 4 (2001) I s9

probably an antero-posterior component of man- Schaeffer & Rosen (1961) summarised the dibular movement in addition to the simple bit- evolution of feeding mechanisms in actinoptery- ing action. Thus, the mandible could slip to and gians in a widely accepted paper. They recog- fro enhancing the action of nipping but also nised at least three major adaptive levels of acti- gives a shearing moment to chewing during man- nopterygian feeding mechanisms. The pure biting dibular abduction. However, wear facets found mechanism is interpreted as the most basal form on many prearticular teeth indicate an additional of food acquiring by them, whereas suction feed- lateral directed shear moment of the jaws during ing is the most advanced one. Contrary, Mallat mouth closure. (1981) stated, that suspension feeding was prob- Spreading of the branchiostegal membrane is ably the most primitive method of prey capture caused by the paired branchiostegal rays. The re- in vertebrates, whereas Lauder (1985) and Lau- duction of the plate-like branchiostegal rays to der & Shaffer 1993 hypothesise, that suction two short ones in pycnodonts may be related to feeding represents primarily the conservative increased mobility of the hyoid arch in the dor- biomechanical pattern found in gnathostomes. so-ventral plane. On the other hand, the reduc- Suction feeding is the process of aquatic prey tion indicates a small branchiostegal membrane capture, in which the mouth cavity is rapidly ex- (see above). This in turn suggests relative small panded to produce a negative pressure inside the potential for opercular chamber expansion, buccopharyngeal cavity relative to the surround- which would affect the feeding habits. Spreading ing water. This creates an unidirected flow of of the branchiostegal membrane and thus of the water into the mouth, when the mouth is orobranchial chamber seems to be less effective opened. Suction feeding of pycnodonts may not than in teleosts. The dorsal branchiostegal ele- have been as efficient as in higher teleosts, since ments, from which the interoperculum is sup- the morphology of the opercular apparatus and posed to be derived, form a functional linkage the correlated muscles resulting in opercular le- between the hyoid arch, operculum, and mand- vation and the transfer of the resulting torque to ible in halecostomes and played an important the mandible via the interoperculum were not role in the early evolution of the levator operculi developed. Nevertheless, it can also be proposed. coupling. 1 assume, that the linkage was present that pycnodonts transmitted the forces operating directly between the branchiostegals and the the mandible via the mandibular articulation, opercular apparatus without the transmitting in- since the symplectic bone is tightly sutured to teroperculum, because the interoperculum is the medial surface of the preoperculum. But suc- lacking in pycnodonts. tion feeding was probably not the same in pyc- Expansion of the orobranchial chamber is nodonts. tMesturus, jHadrodus, and tArCIm- caused by the depression of the hyoid apparatus, from, which are interpreted as basal forms by spreading of the branchiostegal membrane, (Nursall 1996b, Kriwet 2001) are characterised and upper jaw protrusion. A muscle mass, which by comparably large mouth gapes and long max- extended from the ventral aspect of the paired illa, which were probably more fixed than in ad- prearticulars to the ceratohyal and epihyal, was vanced forms. It can be assumed, that suction certainly present. The action of the ventral mus- feeding was less effective amongst these pycno- cles was augmented by drawing the hyoid appa- donts. ratus ventro-caudally by the sternohyoid muscles. In summary, pycnodonts were able to enlarge their buccopharyngeal cavity to produce negative Digestive system and gut contents pressures during mouth opening. This is caused by the slightly oblique orientation of the suspen- The digestive system of actinopterygians is divided sorium in pycnodonts, which results in an in- into pharynx, esophagus, stomach (ventriculus). crease of the volume of the orobranchial cavity, and intestine. The study of stomach contents is im- when the hyomandibula is rotated, by upper and portant in order to understand the feeding habits lower jaw protrusion, which would also increase of actinopterygians. Unfortunately, stomach or the velocity of the water flow directly in front of gastrointestinal contents are rarely preserved in the mouth, and enlarging of the branchial cham- fossil vertebrates. The conservation of fossil diges- ber. Thus, pycnodonts evolved a suction feeding tive remains is correlated to particular taphonomic mechanism, which is similar to that of teleosts. processes, which are found, e.g., in the sedimen- This is also supported by the ecomorphology of tary processes of lithographic limestone deposi- the skull. tion in southern Germany and France. 160 Krkvet. J.. Feeding mechanisms and ecology of pycnodonts

I hypothesis?, that the pharynx of pycnodonts Traces of the digestive system have been re- was rather short, because of the foreshortening cognised in some specimens of tPycnodus plates- of thc head. Jbe branchial chamber. which was siis (MNHN Bol 126. MNHN Bol 127, MNHN high but also short. is characterised by the pre- Bol 134. MNHN Bol 135) and in tGyrodus hem- sence of branchial teeth in some species (Kriwet go~ti.s(VFKO-X 11). The passage of the esopha- 1009b). The uniserial arrangement of branchial gus into the gut is located rather high in the teeth in pycncdonts corresponds to the type of skull just below the posteriorly extending para- Recent oninivl ire actinopterygians: but they are sphenoid and notochord. The branchial teeth, not homologox to the pharyngeal teeth of ci- when prescnt. are also found in this position. chlids or cyprinids (Kriwet 2001). It is assumed. The intestine bends down in a vertical plane and that there is 110 specialised mastication process is U- to V-shaped, making a turning just poster- nor a horny Flate below the occipital region of ior to the pectoral girdle and running more or the head in thi. dorsal wall of the esophagus sup- less horizontal to the anus in ~Pycnodus.Con- porting the br mchial teeth in pycnodonts based trary. the intestine of tCyrocliis seems to be on the niorphl )logy of their basioccipital. It can longer and more coiled (Fig. 16). I postulate, that be supposed. that the main role of branchial the digestive system consisted of a long, rather teeth of pynodonts was to remove food parti- slender and coiled tube-like structure without cles suspended in the water ingested during feed- an!’ expansion. which may indicate, that pycno- ing. In the sant way. indigestible shell fragments donts did not have any stomach but only an in- were sieved odt and probably regurgitated like testine. This observation agrees well with the re- in many recent durophagous actinopterygians. sults found in Recent bottom-feeding teleosts This also ma;’ lead to the consequence. that without stomach but well-developed jaw denti- there are almxt no gut contents preserved in tions and/or pharyngeal teeth and feeding specia- pycnodonts. Mastication was mainly effected by lisations on a single but abundant species. Acid the molariforr dentition. digestion is not present in those fishes and indi-

Fi9. 16. Remains of tlic intestine ol fC;\~ro~/ir.\hc,.\-rrgornrt (VFKO-X 1 1 ) from tlic upper Kimmeridgian (Upper Jurassic) of Brunn (southern (erniany) ;I$ susgestcd by the presence of monospecific spines of ecliinoids (arrows). Mitt. Mus. Nat.kd. Berl.. Geowiss. Reihe 4 (2001) 161

Table 1 muscles). Therefore, it is necessary to simplify Gut contents of certain pycnodonts biological problems into manageable dimensions Genus Gut contents for practical reasons, especially when fossils are considered. Consequently, the functional mor- tArdiirzfions spines of monospecific phology of the pycnodont feeding apparatus was (a singlc specimen) echinoderms tC;?rorlrrs (two specimens) spines of monospecific deduced from form and structure (anatomy as echinoderms well as ecomorphology) and in comparison with tlenznrzjrr (a singlc specimen) ? small actinopterygian several extant actinopterygians. It is possible. vertebrae -i-Nirrsa/lirr(two specimens) spines of monospecific that the assumptions may not be correct in every echinoderms detail. since pycnodonts have no extant close re- fProscir1etes shells of monospecific latives to compare with (Kriwet 2001). But in (a single specimen) bivalves -1. Tepnichthvs shells of monospecific addition to the general assumptions on the mode (several specimens) bivalves of living of pycnodonts proposed so far (e.g.. -/Pycnodir.s(two specimens) shclls of monospecific bivalves Nursall 1996a) the perceptions, especially those f Nrop roscin etes monospecific snails (a single specimen) (coral fragments?) of the feeding kinematics, the ecomorphological patterns, and the gut contents made in this study are of special interest for the reconstruction of gestible food remains such as shell fragments are the ecology of pycnodonts. rejected. It is shown, that the feeding kinematics of pyc- So far, gut contents of pycnodonts have only nodonts are more complex than in halecomorphs be found with certainty in eight genera (Tab. 1). and exhibit a transition from the simple stereoty- Remarkably, the gut contents are extremely pic feeding kinematics that is characteristic for stereotypic. They always consist of monospecific primitive actinopterygians without upper jaw invertebrate remains (Fig. 16). The only excep- protrusion and less effective enlarging mechan- tion may be tlernanjn. Some very small actinop- isms of the buccopharyngeal cavity to the modu- terygian vertebrae are preserved in the coelomic lating feeding kinematics of advanced teleosts in- cavity of an acid prepared specimen (AMNH cluding upper jaw protrusion and effective 13963) indicating small actinopterygians as prey. enlargement of the buccopharyngeal cavity. Actually, it is not clear whether the vertebrae Thus, the pycnodon feeding mechanism may be are true gut contents or were scattered in the best addressed as limited modulating feeding ki- limestone matrix and have been accumulated in nematics involving both basal (bottom feeding) the cavity during acid preparation. Monotypy of and advanced patterns (suction feeding). Starting prey is very characteristic for Recent bottom- of mouth opening is caused by elevation of skull, feeding actinopterygians, which prefer to feed abduction of suspensorium, and by depression of mainly on a single and locally abundant species. the hyoid apparatus. Slight expansion of the They only change to other prey under unfavour- branchiostegal rays and rotation of the suspen- able conditions (e.g., Dugas 1986). A summary sorium increases the orobranchial cavity during of pycnodont gut contents is listed in Table 1 continuous suspensorial abduction and hyoid de- based on personal observations, literature data pression. The angular-maxillary swing, protrusion (Lehman 1966, Blot 1987, Nursall 1999a), and of mandible, and continuous hyoid depression personal communications, e.g., for jNeoprosci- during mouth opening result in an anteriad di- netes by I. Rutzky (AMNH, New York). Maisey rected protrusion of the premaxilla. Prey is in- (1996) indicated small pieces of corals in the ab- gested by nipping and suction (combination of dominal cavity of pycnodonts but without any biting and suction feeding). Mouth closing is specific reference (tNeoproscinetes?). mainly caused by adduction of mandibular mus- cles and is supported by hyoid retraction, lower- ing of neurocranium, suspensorial adduction, and Conclusions relaxing of involved ligaments. But feeding kinematics were not completely This study deals with the feeding mechanisms the same in pycnodonts (Kriwet 1999a). One and the involved elements of the head of fossil group, which is mainly composed of tMe~tum.~, pycnodont fishes. Unfortunately, it is not possi- tArdunfrons, and perhaps tMicropycnodorz and ble, to make direct observations in exclussively tHadrodus, is characterised by long maxilla and fossil forms (e.g., high-speed cinematography and premaxilla, which were fixed to the skull without examination of the electrical activity pattern of articulations and rather deep mouth clefts. Suc- I62 Krinet. J.. Feeding mechanisms and ecology of pycnodonts

tion feeding wzs obviously less effective. and nip- pathway of jaw protrusion in gcneralised per- ping at benthic prey was not supported by pro- coids to the highly modulated pathways in ci- trusion of uppcr jaws. I assume. that the adduc- chlids). Evolutionary patterns may be correlated tor muscles wxe less well-developed in basal with differences in the structural network of cou- pycnodonts with coniplete dermal covering of plings. Adaptation is not a response of a charac- the cheeks. anc which lack a temporal opening. ter to external conditions but it is the response Thus, biting ')r nipping as well as suction feed- to the totality of the external environment and ing was the m,de of food capture in more ad- the evolutionary inventory of an organism, which vanced pycnodmts although it is not possible to form together the matrix for evolutionary trans- reconstruct the total range in respect to the dif- formations. The prey specification may have ferent phases (nipping. biting. inertial suction made pycnodonts extremely vulnerable to feeding). The 1 entrally directed mouth cleft and changes in the environment and to competition the horizontal to obliquely arranecd ectoptcry- by teleosts. It seems, that their evolutionary in- goid are clear indications. that pJrnodonts were ventory was depleted and optimising of adapta- benthic forage 's with mixed feeding strate9ies tions in a functional and constructional sense when conipareii to the condition found in extant bvas not possible any more. coral fishes (e.;!..Davis & Birdsong 1973. Kotrs- chal & Thomson 1989) and cichlids (e.g.. Liem 1979). Pycnodljnts as ecomorph may be best Acknowledgements grouped within the omnivorous group in contrast

to the assumpt ons proposed by Nursall (1996a). This stud! was part of a project under the supervisorship of It is also hypathesised. that pycnodonts were H.-I? Schultre and Ci. Arratia (Berlin). I gratefully acknowl- highly specialised predators on generic or e\'en edge hoth for all their help. suggestions. and encouragement. The!, also pro\ ided inany valuable comments on diI'l'ercnt specific level l-ased on the few specimens with drafts of the manuscript. Partial financial support was pro- preserved inte: tine contents. Specialisation on a \ ided by the German Scientific Foundation (DFG, Schu 212/ single but abuidant prey is a common feature 13-1). I \vould like to thank the following persons and iiistitu- tion\ for permisson to study material under their care: G. among extant coral fishes. Nevertheless. many of Ai i-atia (MLI~~LII~Ifur Naturkunde, Berlin), A. Aspes (Museo those specialist :s have the potential to switch on Ci\ icc cli Storia Naturale. Verona. Italy). R. B(ittcher (Staat- other prey if they are forced to (e.g.. in capture). 1ichc.s Museuni fur Naturkunde. Stuttgart), A. Broschinski (fiiedersiichsisches Landesniuseuni Hannover), S. Calzada After ingestior. shelled prey was crushed with (4lusco Geoldgico Del Seminario. Barcelona. Spain), J. A. the help of the molariform teeth and well-dcvel- ('oopcr (Booth Museum. Brighton, U.K.), P. Forey and A. oped adductor muscles. Abrasion of the occlusal Lon&ttoiii (The Natural History Museum, London, U.K.), surfaces found in many specimens indicates. that C. Heunisch (Bundesanstalt fur Geowissenschaften und Roh- stotic'. Hanno\rr). M.Gayet (UMR 5565 CNRS - IJFR des the prey was lot only crushed. but that there Sciences dc la Terre. [JniversitC Claude Bernard Lyon 1. was probably .ilso a milling component. There Lyon. France). J. GOmez-Alba Ruiz (Museo de Geolcigia, Barcelona. Spain). L. Grande (Department of Geology, Field are two possib lities for the absence of intestine Museum of Natural History. Chicago. U.S.A.), H. Jahnke contents. (1) It may be related to prey without ( Inytitut und Museum fiir Geologie und Palaontologie, Get- rigid exoskeletl in and which have consequently tinern). B. Ki-rhs (Pali~ontologischesInstitut der Freien Uni- \eI-sitiit. Berlin). A. Licbau (Institut und Museum fur Geolo- no fossiliferou: potential. (2) The rareness of Fie und Paliiontologie. Tubingen). J. G. Maisey and 1. Rutzky shell and other prey fragments in the visceral (American hluseuni of Natural History. New York, U.S.A.), area may be cue to the fact. that most of the A. hliiller (Institut fur Paliiontologie. IJniversitat Leipzig), G. >lu\cio (Museo Friulaiio di Storia Naturalc, Udine, Italy). A. hard material 'vas rejected after being crushed. Paganoni (Museo Civic0 di Scienze Naturali "E. Caffi", Ber- similar to the 2ondition found in many Recent ganio. Italy). R. Purdy (Division of Paleontology. United durophagous ac tinopterygians (pers. obser.). St ii tc's National Museu in. Snii thsonian Tnsti t u tion, Washing- ton D.C.. U.S.A.). s. Rodriguez and F. Vigouroux (Museum The last pyciiodonts lived right alongside with d'Histoire naturelle. I.yon. France), M. Rnpcr (Biirgermeister the first re e f-d\gel 1 i ng t c Ic 0st s with si m i 1a r c col o - Miiller Museum. Solnhofcn. Germany), 0. Schultz (Natur- gical demands. which appeared in the Eocene historisches hluseuni Wien. Austria). M. Tentor and F. Dalla Ilia (Museo Palcontologico Cittadino-Gruppo Spcleolo- (e.g.. Kriwct 2001). It seems, that these teleosts gico Monfalconense. A.D.F.. Monfalcone. Italy), A. Tintori were more successful than pycnodonts. Liem ( Istituto di Paleontologia dell'Universit8 degli Studi di Mila- (1 980) showed that the adaptive sensitivity to ni. Mailand and Museo della Vicaria S. Lorenzo, Zogno, changes in the :xternal environment depends on Italy). G. Viohl (Jura Museum. Naturwissenscliaftliche Sainmlungcn Eichstiitt). I? Wellnhofer (Bayerischc Staats- the structure 0. the network of interacting con- saninilung fur Paliiontologie und historische Geologie, straints in tht feeding kinematics. A minor hlunchen). S. WcnL (Museum national d'Histoire naturelle, r Paris. France). K. A. Frickhinger (Plancgg) is thanked for change in the etwork may transfer a static fea- information on material housed in private collections. I am ture into a dy ianiic character (e.g.. the simple also grateful to the following persons Lor information and Mitt. Mus. Nat.kd. Berl., Geowiss. Reihe 4 (2001) I63 discussions: A. Averianov (St. Petersburg, Russia), P. Brito 487-492. Dowden. Hutchinson & Ross. Stroushurg. (Rio de Janeiro, Brazil). G. R. Case (New Jersey, U.S.A.), A. Pennsylvania. de la Pcfia (Madrid. Spain). B. G. Gardiner (London, U.K.), Davis, W. P. & Birdsong, R. S. 1973. Coral reef fishes which M. Gayet (Lyon, France), J. G. Maisey (New York, U.S.A.), forage in the water column: A review of their morphol- A. Mudroch (Hannover), J. R. Nursall (Whaletown, Cana- ogy, behavior, ecology, and evolutionary implications. - da). G. V. R. Prasad (Jammu Tawi, India), F. Pfeil (Munich), Helgolander Wissenschaftliche Meeresuntcrsucliun#en 24: the late C. Patterson (London. [J.K.), F. J. Poyato-Ariza 292-306. (Madrid. Spain), D. R. Schwimmer (Columbus, U.S.A.), J. D. Dobben, W. H. van 1937. iiber den Kiefermechanismus tler Stewart (Los Angeles, U.S.A.), D. Thies (Hannover), and S. Knochenfische. - Archivcs Nederlandaises de Zoologit' Wenz (Paris, France). M. Roper provided the specimen for 2: 1-72. Figure 16. I am dccply indebted to J. R. Nursall and A. Tin- Dugas. C. N. 1986. Food habits of black drum. Pogonirr.~cro- tori for many valuable comments on an earlier draft of the ntis, in southeast Louisiana with emphasis on their pred;t- mansucript. 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