Journal of Vertebrate Paleontology 29(2):0–0, June 2009 # 2009 by the Society ofProof Vertebrate Paleontology Only

ARTICLE

MEGAPIRANHA PARANENSIS, A NEW GENUS AND SPECIES OF (, TELEOSTEI) FROM THE UPPER OF ARGENTINA

ALBERTO LUIS CIONE,1 WASILA M. DAHDUL,*,2 JOHN G. LUNDBERG,2 and ANTONIO MACHADO-ALLISON3 1Divisio´ n Paleontologı´a de Vertebrados, Museo de La Plata, 1900 La Plata, Argentina, [email protected]; 2The Academy of Natural Sciences, Department of Ichthyology, 1900 Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103, U.S.A., [email protected], [email protected]; 3Instituto de Zoologia Tropical, Universidad Central de Venezuela, Apartado de Correos 47058, Caracas, 1041-A, Venezuela, [email protected]

ABSTRACT—Megapiranha paranensis from the Upper Miocene of Argentina is described based on a large, partially toothed premaxilla as a new genus and species of serrasalmid fish ( and ) and is diagnosed and distinguished from other serrasalmids based on the following unique combination of characters: seven premaxillary teeth with the first four arranged in a shallow, zig-zag row, and third tooth shaped similarly to the fourth and fifth teeth; large, triangular, unicuspid crowns with finely serrated cutting edges. The phylogenetic position of Megapiranha was determined by parsimony analysis of morphological characters. The resulting analysis recovered Megapiranha as sister to the clade (Pygopristis, Pygocentrus, Pristobrycon, Serrasalmus) and is supported by two synapomorphies: (1) teeth triangular in labial view with well-developed cutting edges, and (2) serrations along both sides of tooth cutting edges. The pattern of tooth placement exhibited by the fossil Megapiranha is intermediate between the double-row condition of pacus and the single-row condition of piranhas, and suggests how the double row of teeth may have been rearranged into a single row in the evolution of piranhas.

INTRODUCTION late Miocene fossil vertebrate locality along the Rı´o Parana´ near the city of Parana´, Entre Rı´os, Argentina. Whereas the fossil The Serrasalmidae are a family of South American fresh- premaxilla and teeth are obviously distinct from modern serra- water characiform fishes including the well known flesh-eating salmids, its sharp, blade-like and somewhat compressed teeth piranhas and herbivorous and pacus (Ringuelet et al., bear some similarity to piranhas. Further, the arrangement of 1967; Machado-Allison, 1983a, b; Je´gu, 2003). Correlated with teeth on the fossil is intermediate between the distinct double- their dietary diversity, serrasalmids exhibit a remarkable array and single-row patterns of modern serrasalmids, suggesting as of specialized dentitions and jaws. The herbivorous and omniv- did William Gosline how the teeth may have been rearranged orous species have broad, heavy jaw bones each with a double in the origin of piranhas. This fossil is described here as a new row of seven roughly circular teeth bearing one or two low genus and species of Serrasalmidae; its relationships and evolu- cutting edges. The slender jaw bones of piranhas each bear a tionary significance are discussed. single, narrowly compressed row of six interlocking, blade-like Institutional Abbreviations—MLP, Museo de La Plata, La jaw teeth. In 1951, Gosline suggested that the characteristic Plata, Argentina; CICYTTP, Centro de Investigaciones Cientı´- single row arrangement of teeth of piranhas was derived from ficas y Transferencia Tecnologı´a a la Produccio´ n, Diamante, the primitive double row condition of herbivorous serrasalmids. Argentina. Gosline hypothesized that the primitive double row of teeth were “pressed into a single row,” with one tooth dropping out. Gosline knew of no examples of an intermediate pattern. GEOGRAPHIC AND STRATIGRAPHIC PROVENANCE Both piranhas and pacus are widespread today in the tropical lowlands of eastern South America. The oldest known fossil The Neogene fossiliferous beds in the Parana´ riverside cliffs serrasalmids are isolated teeth from the Upper of near the city of Parana´, Entre Rı´os, Argentina have been scien- Bolivia (Gayet and Meunier, 1998; Dahdul, 2007). These and tifically known since 1827 when Alcide D’Orbigny visited the several other fossil teeth and jaw elements from Cenozoic rocks area (D’Orbigny, 1842; Fig. 1). The complex relationships be- F1 pertain to the herbivorous pacus (Lundberg, 1998; Cione et al., tween the marine and continental units cropping out of the 2000; Dahdul, 2004, 2007). The fossil record of piranhas on the cliffs provoked different interpretations. Most authors identi- other hand is presently limited to a few isolated teeth of Neo- fied only one marine unit recognizable at the base of the cliffs gene age (Lundberg, 1998). (e.g. Ameghino, 1906; Scartascini, 1954; Acen˜ olaza, 1976). This One of us (AC) found a very large and partially toothed marine unit is overlain by a thick fluvial and a terrestrial se- serrasalmid premaxilla in the Roth Collection of the Museo de quence. However, other authors proposed two or three marine La Plata (Argentina). The specimen comes from the well known transgressions (Frenguelli, 1920; Cordini, 1949). The current stratigraphic scheme was proposed by Acen˜olaza (1976; 2000; see also Acen˜ olaza and Acen˜ olaza, 1999; Fig. 2) who interpreted F2 the marine rocks as having originated during a single ingression *Corresponding author. Current address: Department of Biology, Uni- represented by the Parana´ Formation. Acen˜ olaza (1976, 2000) versity of South Dakota, Vermillion, SD 57069, [email protected] suggested that the marine beds located at higher levels in the Proof1 Only 2Proof JOURNAL OF VERTEBRATE PALEONTOLOGY, Only VOL. 29, NO. 2, 2009

FIGURE 1. Map of the Entre Rı´os province in Argentina showing the approximate location of the holotype of Megapiranha paranensis between the cities of Parana´ (ca. 3143’S 6031’W) and Villa Urquiza (ca. 3138’S 6022’W). City limits indicated by hatchmarks and coordinates estimated from center of cities as indicated by black dot (modified from Cione et al. 2000).

riverside cliffs are relicts of an ancient topography that was The term “Piso Mesopotamiense” or “Mesopotamiense” was wrongly interpreted as different marine ingressions, especially widely in use in the Argentinian vertebrate paleontology litera- by Frenguelli (1920). The Parana´ Formation is mainly composed ture. This term was introduced for the first time by Doering of green mudstones and sandstones with oyster banks (Acen˜ o- (1882; see also Ameghino, 1883). Frenguelli (1920) restricted the laza, 1976, 2000; Chebli et al., 1989) and was apparently depos- “Mesopotamiense” to the “Conglomerado osı´fero.” One of us ited during the large marine encroachment that covered the discussed extensively the use of state/age concept in South Amer- Chacopampean region during the middle Miocene (“Mid Trans- ica (Cione and Tonni, 1995, 1996) although we did not addressed gressive Onlap Sequence;” see Uliana and Biddle, 1988; del Rı´o, the “Mesopotamiense” problem. Cozzuol (1993) proposed to 1991). This trangression probably persisted in the East of Argen- define the “Mesopotamiense” as a formal stage/age unit. tina until the Tortonian (see below). The fluvial Ituzaingo´ For- Unfortunately, most of the fossils in collections from the Parana´ mation overlies the marine unit. This formation is composed of a area do not include adequate provenance. Labels in collections basal conglomerate (“Conglomerado osı´fero”) with abundant usually only state that the material comes from the base of the vertebrate remains which is overlain by almost unfossiliferous cliffs near Parana´. However, recent field work has confirmed that whitish to yellow brown sandstones and green mudstones. Ter- almost all of the Miocene terrestrial and freshwater aquatic verte- rigenous Pleistocene (Ensenadan to Lujanian in the southern brates come from the “Conglomerado Osı´fero” at the base of the South American continental scale; see Cione and Tonni, 1995, Ituzaingo´ Formation. Field work is presently in progress and more 1996, 2001; Fig. 2), poorly fossiliferous beds assigned to different precise information will be obtained. The “Conglomerado osı´fero” units overlay the Ituzaingo´ Formation (Acen˜ olaza, 1976; occurs in paleochannels, is laterally interrupted and rarely crops Iriondo, 1980; Chebli et al., 1989). The Ituzaingo´ Formation (as out because of landslides. There is no basis for recognizing chron- Entre Rı´os Formation) was correlated with the “Formacio´ n ostratigraphic, biostratigraphic, geochronologic or even biochro- Puelche” of the Buenos Aires province subsoil (Reig, 1957; see nologic units based on the fossil and stratigraphic representation below). According to the mammals occurring in the “Conglom- of the “Conglomerado osı´fero.” Consequently, we consider here erado osı´fero” and the stratigraphic relationships, the age of the the “Piso Mesopotamiense” sensu Frenguelli (1920) or “Mesopo- base of Ituzaingo´ Formation is almost exclusively Tortonian tamiense” as invalid. In this paper, we will refer to the fossil con- (late Miocene) or Huayquerian in the local chronology (Pascual tent of the base (“Conglomerado osı´fero”) of a lithostratigraphic and Odreman Rivas, 1971; Cione and Tonni, 1995; Fig.2). The unit (Ituzaingo´ Formation) as present in several localities near Huayquerian ranges from about 9 Ma to about 6 Ma (Marshall Parana´ without recognizing a local chronostratigraphic or bio- et al., 1983). Proofstratigraphic Only unit (Cione et al., 2000). CIONE ET AL.—NEW FOSSIL SERRASAMINE FROM ARGENTINA 3

ProofFormation Only (elasmobranchs, teleosteans, cetaceans, sirenians and pinnipeds) and the “Conglomerado Osı´fero” at the base of the continental Ituzaingo´ Formation (elasmobranchs, teleosteans, crocodilians, chelonians, birds, and different groups of terrestrial and aquatic mammals). The material here described comes from the “Conglomerado osı´fero” of the Ituzaingo´ Formation. The holotype (MLP 96-XI- 5-1) was collected by Santiago Roth at the beginning of the 20th century in an indeterminate locality between the cities of Parana´ and Villa Urquiza, Entre Rı´os (Fig. 1). Additional material includes an isolated tooth (CICYTTP-PV-P-1-125) from the Conglomerado osı´fero cropping out in the base of the Parana´ riverside eastern cliffs in the SLC1 (Colonia La Celina, Entre Rı´os, 31370S60200W) by Jorge Casciotta, Alberto Cione, Jorge Noriega and Leopoldo Soibelzon in June, 1999.

MATERIAL AND METHODS Comparative material included alcohol preserved, dried skele- tal and cleared, alizarin-stained specimens (Appendix 1). Tooth and surface attachment measurements ( 0.1 mm) are listed in the Table. The reconstructed standard length of Megapiranha T was estimated by eye from digital image scaling of the propor- tional difference in size between the fossil premaxilla and those of modern Colossoma macropomum and Serrasalmus rhombeus of known standard length. We assessed the phylogenetic position of Megapiranha by in- cluding the species in the morphological character matrix of Dahdul (submitted, Proc. Acad. Nat. Sci.). Megapiranha was coded for 8 characters related to the premaxilla and premaxil- lary teeth (Appendix 2), and all other characters were coded as missing. Parsimony analysis of 102 characters coded for 33 terminal taxa (29 serrasalmids, 4 outgroup taxa) was conducted using PAUP*4.0b10 (Swofford, 1998). All characters were un- FIGURE 2. Generalized stratigraphic section of the late Cenozoic ordered and weighted equally. Heuristic searches were con- strata at the left side cliffs along the Rı´o Parana´ near the city of Parana´, ducted with 1000 random sequence additions used to obtain Entre Rı´os, Argentina (modified from Acen˜ olaza, 1976). starting trees via stepwise addition and the tree bisection recon- nection (TBR) branch swapping method. The strict consensus tree (Supplementary Figure 1, www.vertpaleo.org/publications/ JVPContent.cfml) was generated from the resulting equally par- simonious trees. Branch support was estimated from bootstrap Some marine vertebrates (mainly sharks and rays) occur in the proportions (1000 pseudoreplicates) (Felsenstein, 1985). “Conglomerado osı´fero.” It has to be determined if the marine Character state optimization on the strict consensus tree was vertebrate remains were reworked from the Parana´ Formation performed using the trace option in MacClade 4.08. Character or they actually inhabited the channels where the “Conglomer- optimization based on accelerated transformation (ACCTRAN) ado osı´fero” was deposited. Until now, we have corroborated is presented because it favors reversals over parallel gains, un- that the Parana´ Formation includes mainly marine and some like delayed transformation (DELTRAN), although we also freshwater and terrestrial vertebrates (Cione et al., 2002, 2005). indicate optimizations that are supported unambiguously (i.e., In sum, present evidence indicates that most of the Miocene by both ACCTRAN and DELTRAN). Characters that chan- material from the Parana´ area come from the marine Parana´ ged along branches participating in polytomies were not recon-

TABLE. Tooth measurements (mm) of the fossil Megapiranha paranensis premaxilla.

Tooth Position

Measurement 1 234567Isolated tooth Labial basoapical height — — 14.1 11.2 11.6 — — — Lingual basoapical height — — 12.1 5.8 9.3 — — — Labial basoapical height (direct) — — 14.4 11.2 12.8 — — — Lingual basoapical height (direct) — — 13.8 8.8 11.8 — — — Base labiolingual distance — 12.2 12.4 8.3 11.0 12.6 9.9 9.5 Base mesiodistal distance 9.7 9.3 10.4 6.6 8.4 9.0 7.6 8.7 Crown mesiodistal distance — — 12.0 7.8 10.2 — — — Base mesiodistal apex distance — — 5.2 3.8 4.6 — — — Labial basoapical height/ Lingual basoapical height — — 1.16 1.93 1.25 — — — Labiolingual base distance/ Mesiodistal base distance — 1.31 1.19 1.26 1.31 1.43 1.30 10.9 Crown area (mm2)Proof — — 166.6 Only 69.2 129.9 — — — 4 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 29, NO. 2, 2009

structed because ACCTRANProof and DELTRAN could not be per- OnlyMEGAPIRANHA PARANENSIS, sp. nov. formed along these branches. Material—Holotype: MLP 96-XI-5-1, fragmentary right pre- SYSTEMATIC PALEONTOLOGY maxilla with three complete teeth and one fragmentary tooth. Additional material: CICYTTP-PV-P-1-125, isolated tooth crown. Order CHARACIFORMES sensu Fink and Fink, 1981 Type Locality—Cliffs in the Parana´ eastern riverside near the Family CHARACIDAE Agassiz, 1844 city of Parana´, Provincia de Entre Rı´os, Argentina. Subfamily SERRASALMIDAE Gu¨ nther, 1864 Stratigraphic Unit and Age—Ituzaingo´ Formation, Huayquer- MEGAPIRANHA, gen. nov. ian Age, Late Miocene (see above). F3 (Fig. 3) Etymology—The generic name Megapiranha refers to the Type Species—Megapiranha paranensis, sp. nov. large size of the species as inferred from the size of the fossil Diagnosis—As for type and only species. premaxilla and its relationship to modern piranhas. The specific

FIGURE 3. Megapiranha paranensis, MLP 96-XI-5-1, holotype (left) and illustration (right). A, D, labial view, with numbers indicating tooth and tooth scar positions; B, E, lingualProof view; C, F,occlusalview.Abbreviations: ap, ascending process; Onlyda, dentigerous arm; s, symphysis. Scale bar equals 1 cm. CIONE ET AL.—NEW FOSSIL SERRASAMINE FROM ARGENTINA 5 name, paranensis, refersProof to its locality of origin along the Rı´o Tooth Only replacement trench on labial face of premaxilla above Parana´ near the city of Parana´, Argentina. 1st to 6th teeth, missing parts of its bony cover, no replacement Diagnosis—Megapiranha paranensis is a genus of serrasalmid teeth preserved. Foramina on bony cover of replacement trench characiform fish distinguished by a distinctive and phylogeneti- present above the 5th and 6th teeth. Outer surface of premaxilla cally derived premaxillary dentition, shape and unusually large rugose with a row of 12 foramina dorsal to tooth bases, probably size. 1) Seven premaxillary teeth; mesial four teeth arranged in a for blood vessels or nerves. Basal width of ascending process shallow zig-zag, partly overlapping row; third tooth shaped simi- spans mesialmost four teeth. larly to fourth and fifth teeth (in mesiodistal sequence positional Symphyseal surface immediately medial to innermost tooth homologies of these seven teeth in relation to those of serrasal- with a stout “peg” dorsal to a broadly U-shaped flat surface, mids bearing two rows of teeth: 1st = inner row tooth (IRT) 1, together forming at least part of interdigitating premaxillary sym- 2nd = outer row tooth (ORT) 1, 3rd = IRT 2, 4th = ORT 2, 5th = physeal joint (bone margin broken more dorsally). ORT 3, 6th = ORT 4, 7th = ORT 5). Other serrasalmids have two rows of seven teeth with IRT2 (=3rd tooth) shaped differently Comparative Description, Relationships and Discussion from outer row teeth (Colossoma, Piaractus, Mylossoma, Acno- don,“Myleus” clade, Metynnis), a zig-zag row of five teeth (Cato- In addition to its autapomorphic features Megapiranha exhi- prion), or a single row of six teeth (piranhas). 2) Large unicuspid bits a combination of plesiomorphic and derived characteristics crowns of all known teeth (3rd, 4th, 5th) similarly shaped in labial of the premaxilla and premaxillary teeth shared with one or view as nearly equal-sided triangles above constricted bases; each more genera of serrasalmids (see Appendix 2 for list of charac- cusp at midpoint above increasingly sloped and finely-serrate ters coded for Megapiranha in the phylogenetic analysis). In the sides that together form a labio-lingually compressed, mesiodis- phylogenetic analysis of serrasalmid relationships, Megapiranha tally straight, blade-like crest close to labial edge. Other serrasal- was recovered as sister to the piranha clade (Pygopristis, Pygo- mids have either complexly shaped, broad teeth (Colossoma, centrus, Pristobrycon, Serrasalmus)(Fig. 4). Because we were F4 Piaractus, Mylossoma, Acnodon,“Myleus” clade, Metynnis), tu- only able to code Megapiranha for a small portion of morphol- berculate teeth (Catoprion), or triangular and compressed but ogical characters, we discuss only the characters coded for the multicuspidate teeth with serrated cutting edges (piranhas). fossil in the following comparative description. Several plesio- Additional features found in unique combination in Megapir- morphic characters are present in Megapiranha. anha are: premaxillary mesiodistal axis nearly straight; its dorsal (1) The fossil bears seven premaxillary teeth, a characteristic of margin smoothly concave lateral to a broad-based, scarcely ta- all serrasalmid genera except the derived condition of five pering ascending process; tooth bases in same horizontal plane; teeth in Catoprion mento and six teeth in piranhas (of which symphyseal joint partly interdigitating. Other serrasalmids with a the last is apparently a compound tooth, Fig. 5; Machado- F5 straight mesiodistal axis of the premaxilla have a straight dorsal Allison, 1982). margin, tooth bases of inner and outer row teeth lying in different (2) Attachment scars of the distal most teeth are subcircular planes (Colossoma, Mylossoma, Piaractus, Acnodon, Metynnis, similar to most serrasalmids and not labiolingually com- “Myleus” clade), and additionally some lack the premaxillary pressed as in the derived condition seen in piranhas. joint (Acnodon, Metynnis,“Myleus” clade). Serrasalmids that have the premaxillary dorsal margin curved and tooth bases in In Megapiranha, the distal end of the premaxillary dentigerous the same horizontal plane have a curved mesiodistal axis of the arm does not extend significantly beyond the distalmost tooth to premaxilla and lack the interdigitating joint (Catoprion and pir- form a pedicle-like process as it does in the basal clade anhas). (Colossoma, Piaractus, Mylossoma) and some outgroups (Zanata Description—Labial, lingual, and occlusal views in Figure 3 and Vari, 2005, character 52). The lack of a premaxillary pedicle illustrate premaxillary and tooth shape and dentition pattern; is a derived condition shared with Acnodon,“Myleus” clade, measurements given in the Table. Metynnis, Catoprion, and piranhas. Megapiranha is known from a partial right premaxilla with The following derived premaxillary characters support the well preserved labial and lingual surfaces, ventral and medial placement of Megapiranha as sister to the piranha clade (Pygo- part of interdigitating symphysis, base of ascending process, pristis, Serrasalmus, Pristobrycon, and Pygocentrus). dorsal and ventral margins of dentigerous arm; but missing distal ends of ascending process, dentigerous arm, dorsal part of sym- physis and thin bone over replacement tooth trench. Large size, total premaxilla length >6.9 cm. Evidence of seven teeth, considered the complete premaxil- lary dentition; 3rd, 4th and 5th teeth from symphysis complete and unworn; 7th tooth fragmentary, crown broken; 1st, 2nd and 6th from symphysis missing but positions determined by attach- ment scars. Crowns of 3rd, 4th and 5th teeth differing in size: 3rd largest, about 2.4 X > 4th, and 1.3 X > 5th but similar in shape as per Diagnosis and Figure 3, plus each crown roughly pentagonal in occlusal view; labial face baso-apically convex; lingual face baso- apically concave, labial and lingual faces each with a low, round- ed rise vertically subtending median cusp, and thin horizontal ridge appearing as a line encircling middle of crown, possibly expressing junction between enamel and dentine on tooth sur- face (Shellis and Berkovitz, 1976). FIGURE 4. Summary tree of serrasalmid relationships based on strict consensus tree (Supplementary Figure 1S) resulting from maximum parsi- Crenulated tooth bases and tooth attachment scars differing in mony analysis of 102 morphological characters. Species are collapsed into size over a range of 1.6 times as measured by mesiodistal diame- monophyletic genera where possible; paraphyletic assemblages of multiple ter (Table); size rank of teeth from largest to smallest: 3rd, 1st, genera are represented by triangles. Character number is given above and 2nd, 6th, 5th, 7th, 4th. Attachment scars crater-shaped with labio- character state below the square symbol for character state change based lingually convex floorsProof and elevated rims. on ACCTRANOnly optimization. Characters are listed in Appendix 2. 6 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 29, NO. 2, 2009

(1) All teeth triangularProof and bladelike, labio-lingually compressed, (Machado-Allison, Only 1982, character 27), and Catoprion has tu- with well developed cutting edges (Machado-Allison, 1982, berculate teeth (Machado-Allison, 1982, character 187). Mod- character 215). All other serrasalmids have complexly shaped, ern piranhas differ from Megapiranha in having a large central circular or polygonal-shaped teeth with shorter cutting edges cusp flanked by at least one smaller cusp (with the exception

FIGURE 5. Right premaxillae of serrasalmids in labial and occlusal views. A, B, Megapiranha paranensis; C, D, Colossoma macropomum; E, F, Serrasalmus rhombeus. Numbers indicate tooth and tooth scar positions and arrows on Megapiranha fossil indicate direction of tooth movement in evolution. Teeth 1 and 3 are the plesiomorphically inner row teeth. Abbreviations: ap, ascending process; da, dentigerous arm; s, symphysis. Scale bars equal 1 cm. Proof Only CIONE ET AL.—NEW FOSSIL SERRASAMINE FROM ARGENTINA 7

of pentacuspid dentitionProof in Pygopristis denticulatus,Machado- to ACCTRANOnly optimization, this character arose independently Allison, 1982, character 201) whereas the preserved teeth on in the two lineages. Differences in the structure of these joints the Megapiranha fossil are unicuspid. Similarity in tooth mor- also suggest that they were independently evolved. In the pacus phology also exists between Megapiranha and some species in the joint is formed of two thin, obliquely oriented ridges, in the genera Myleus, Tometes, Mylesinus,andOssubtus.Like contrast to the thicker, more horizontally oriented possibly sin- Megapiranha, the outer row teeth in these species are arrow- gle joint of Megapiranha. The reconstructed size of Megapiranha head shaped in labial profile but also tend to be tall and blunt, was estimated between 95 cm and 128 cm, much larger than that with lateral lobes in some species; none are as distinctly trian- seen in modern piranhas but comparable to Colossoma macro- gular and pointed with increasingly sloped edges as those of pomum, Piaractus brachypomus, and P. mesopotamicus. Megapiranha. In addition, the preserved crowns of Megapir- Several characters are suggestive of relationships between anha in positions 3-5 are concave lingually and have the trans- Megapiranha and other serrasalmid subgroups but could not be verse crest on the labial side (Fig. 3), characteristics shared optimized on the consensus tree because they involved branches with modern piranhas. This differs from the condition seen in participating in a polytomy. all other serrasalmids in which IRT 2 (homologue of tooth 3) (1) The dorsal margin of the premaxillary dentigerous arm is has the cutting edge on the lingual side and is concave labially concave in Megapiranha, Catoprion, and piranhas (Fig. 5), or centrally (Fig. 5). whereas it is straight or moderately convex in all other ser- (2) Cutting edges of premaxillary teeth are finely serrate in rasalmids and outgroups. In addition, the upper distal mar- F6 Megapiranha (Fig. 6) and piranhas, unlike the plesiomorphic gin does not taper in Megapiranha but remains high, a condition of having smooth cutting edges of the premaxillary character shared only with Pygopristis denticulatus, the basal teeth. species in the piranha clade. Megapiranha bears an interdigitating symphyseal joint of the (2) Premaxillary teeth are roughly arranged in a double row premaxilla, a character shared only with the basal pacu clade with the mesial four teeth displaced in a shallow zig-zag consisting of Colossoma, Piaractus, and Mylossoma. According pattern, a condition shared with Catoprion mento and Myle-

FIGUREProof 6. Detail of cutting edge serrations (arrow) on 3rd tooth Only of Megapiranha paranensis. Scale bar equals 1 cm. 8 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 29, NO. 2, 2009

sinus paraschomburgkiiProof(Jegu´ , 1989). However, as noted OnlyLITERATURE CITED above, tooth morphology and number differ among Mega- Acen˜ olaza, F. G. 1976. Consideraciones bioestratigra´ficas sobre el Ter- piranha, Catoprion, and Mylesinus, and the phylogenetic ciario marino de Parana´ y alrededores. Acta Geolo´ gica Lilloana position of Mylesinus within the “Myleus” clade suggests 13:91–107. that the similarity in tooth position arose independently in Acen˜ olaza, F. G. 2000. La Formacio´ n Parana´ (Mioceno medio): est- that lineage. ratigrafı´a, distribucio´ n regional y unidades equivalentes. Serie de Correlacio´ n Geolo´ gica 14:9–28. The zig-zag arrangement of teeth on the fossil premaxilla is Acen˜ olaza, F. G., and G. Acen˜ olaza. 1999. Trazas fo´ siles del Terciario seemingly intermediate between the single tooth row of piranhas marino de Entre Rı´os (Formacio´ n Parana´, Mioceno medio), Repu´ b- and the double tooth row of all other serrasalmids (Fig. 5). Gos- lica Argentina. Boletı´n de la Academia Nacional de Ciencias, line (1951) envisioned an evolutionary shift of tooth position Co´ rdoba 64:209–233. leading from 2-rowed to single rowed dentition that implies a Agassiz, L. 1844. Report on the fossil fishes of the London clay. Report morphologically intermediate condition such as that preserved of the British Association for the Advancement of Science 13: in Megapiranha and modern Catoprion and M. paraschomburg- 279–310. Ameghino, F. 1906. Les Formations Sedimentaires du Cre´tace´ Supe´rieur kii. Like Megapiranha, Catoprion and M. paraschomburgkii et du Tertiaire de Patagonie avec un paralle´le entre leurs faunes have IRT 1, IRT 2, and ORT 3 widely spaced; these teeth are in mammalogiques et celles de l’ancien continent. Anales del Museo contact in all other serrasalmids that possess a double tooth row Nacional de Buenos Aires 15 (ser. 3a, 8):1–568. (Fig. 5). This arrangement suggests that the primitive IRT 1 Chebli, G. A., O. Tofalo, and G. Turzzini. 1989. Mesopotamia; pp. shifted forward to become the first, mesial most tooth and the 79–100 in G.A. Chebli and L. Spalletti (eds.), Cuencas Sedimentar- IRT 2 shifted forward between ORT 1 and ORT 2 to become ias Argentinas. San Miguel de Tucuma´n, Universidad Nacional de the 3rd tooth of the derived single series. ORT 4 and ORT 5 Tucuma´n, Instituto de Correlacio´ n Geolo´ gica, Serie Correlacio´ n supposedly fuse during development resulting in the six tooth Geolo´ gica, 6:Tucuma´n. condition seen in modern piranhas (Machado-Allison, 1982). Cione, A. L., and E. P. Tonni. 1995. Chronostratigraphy and “Land- mammal ages” in the Cenozoic of southern South America: princi- The placement of the Megapiranha fossil as sister to the pira- ples, practices, and the “Uquian” problem. Journal of Paleontology nha clade provides support for Gosline’s (1951) hypothesis on 69:135–159. the evolution of the single-row from the double-rowed state. Cione, A. L., and E. P. Tonni. 1996. Reassesment of the Pliocene- Whereas Gosline hypothesized the loss of one tooth in the evo- Pleistocene continental time scale of southern South America. Cor- lution of the six toothed piranha condition, developmental evi- relation of the Chapadmalalan with Bolivian sections. Journal of dence suggests that the sixth tooth in modern piranhas results South American Earth Sciences 9:221–236. from the fusion of the two distal-most teeth (Machado-Allison, Cione, A. L., and E. P. Tonni. 2001. Correlation of Pliocene to Holocene 1982). Alternatively, the size and relative overlap of teeth southern South American and European mammal-bearing units. in modern piranhas might suggest that the first IRT was lost Bolettino della Societa´ Paleontologica Italiana 40:167–174. Cione, A. L., M. M. Azpelicueta, M. Bond, A. A. Carlini, J. R. Casciotta, (P. Buckup, pers. comm.). Under this scenario, the 3rd tooth of M. A. Cozzuol, M. de la Fuente, Z. Gasparini, F. J. Goin, J. Noriega, modern piranhas is homologous to tooth 4 of Megapiranha. Both G. J. Scillato-Yane´, L. Soibelzon, E. P. Tonni, D. Verzi, and of these teeth are the smallest in their respective tooth series, M. G. Vucetich. 2000. Miocene vertebrates from Entre Rı´os prov- and the third tooth in modern piranhas sits in an offset position ince, eastern Argentina; pp. 191–237 in F. G. Acen˜ olaza and relative to the second and fourth tooth, appearing as though it R. Herbst (eds.), El Neo´ geno de Argentina. INSUGEO Serie Corre- moved from a labial to lingual position in evolution. lacio´ n Geolo´ gica, 14:Tucuma´n. Serrasalmid fossils are reported from the Late Cretaceous and Cione, A. L., E. P. Tonni, and J. San Cristo´ bal. 2002. A Middle-Pleisto- span much of the Cenozoic (Roberts, 1975; Gayet and Meunier, cene marine transgression in central-eastern Argentina. Current 1998; Rubilar, 1994; Lundberg, 1998). These fossils consist of Research in the Pleistocene 19:16–18. Cione, A. L., J. R. Casciotta, M. M. Azpelicueta, M. J. Barla, and isolated teeth and fragmentary jaws nearly indistinguishable M. A. Cozzuol. 2005. Peces marinos y continentales del Mioceno from modern serrasalmids and include subgroup (true piranha del a´rea mesopota´mica argentina, procedencia estratigra´fica y rela- clade and Mylossoma sp.) and species level (Colossoma macro- ciones biogeogra´ficas. Miscela´nea INSUGEO 12:49–64. pomum) identifications (Lundberg et al., 1986; Lundberg, 1997; Cordini, R. 1949. Contribucio´ n al conocimiento de la geologı´a econo´ m- Dahdul, 2004; Dahdul, 2007). The fossil Megapiranha is the first ica de Entre Rı´os. Anales de la Direccio´ n General de Industrias record of an extinct serrasalmid. Piranha fossils from the 13.5 my y Minerı´a 2:1–45. La Venta, Colombia locality provide an older age estimate for Cozzuol, M. A. 1993. Mamı´feros acua´ticos del Mioceno medio y tardı´o lineages basal to the true piranha clade, including Megapiranha de Argentina. Sistema´tica, evolucio´ n y biogeografı´a. Unpublished as it is phylogenetically placed here. Ph.D. dissertation Universidad Nacional de La Plata, Facultad de Ciencias Naturales y Museo de La Plata, Argentina. The ecology of Megapiranha is difficult to reconstruct. De- Dahdul, W. M. 2004. Fossil serrasalmid fishes (Teleostei: Characiformes) spite their reputation as carnivores, some piranha species are from the Upper Miocene of north-western Venezuela; pp. 23–28 in primarily herbivorous, and several species include plant material M. Sa´nchez-Villagra and J. Clack (eds.), Palaeontology of the and scales in their diet (Nico, 1991). This suggests that the ex- Castillo Formation in North-western Venezuela. Special Papers in tremely compressed tooth morphology seen in piranhas did not Palaeontology 71. evolve in correlation with carnivory. In light of this plasticity, the Dahdul, W. M. 2007. Phylogenetics and diversification of the Neotro- compressed crowns and round tooth bases of the Megapiranha pical Serrasalminae (Ostariophysi: Characiformes). Unpublished specimen may have been suited to a range of feeding behaviors. Ph.D. dissertation University of Pennsylvania, Philadelphia, Penn- sylvania, 107 pp. del Rı´o, C. J. 1991. Revisio´ n Sistema´tica de los Bivalvos de Ia Formacio´ n ACKNOWLEDGMENTS Parana´ (Mioceno medio). Provincia de Entre Rı´os-Argentina. Aca- We thank M. Sabaj for photographs of the fossil, K. Luckenbill demia Nacional de Ciencias Exactas, Fisicas y Naturales, Mono- for assistance in figure preparations, and anonymous reviewers grafı´a, 7, 93 pp. for their helpful comments on the manuscript. This project was Doering, A. 1882. Informe oficial de la Comisio´ n cientı´fica agregada al ´ ´ ´ ´ Estado Mayor General de la expedicionalRıo Negro. Geologıa. supported by grants from the Agencia Nacional de Promocion Buenos Aires 299-530. Cientı´fica y Tecnolo´ gica, Consejo Nacional de Investigaciones D’Orbigny, A. 1842. Voyage dans l’Amerique me´ridionale. P. Bertrand, Cientı´ficas y Te´cnicas, and Universidad Nacional de La Plata. Paris, 188 pp. WD also received support from a University of Pennsylvania Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using Paleontology SummerProof Stipend. bootstrap. Only Evolution 39:783–791. CIONE ET AL.—NEW FOSSIL SERRASAMINE FROM ARGENTINA 9

Fink, S. V., and W. L.Proof Fink. 1981. Interrelationships of the ostariophy- Roberts, Only T. R. 1975. Characoid fish teeth from Miocene deposits in the san fishes (Teleostei). Zoological Journal of the Linnean Society 72: Cuenca Basin, Ecuador. Journal of Zoology 175:259–271. 297–353. Rubilar, A. 1994. Diversidad ictiolo´ gica en depositos continentales mio- Frenguelli, J. 1920. Contribucio´ n al conocimiento de la geologı´a de Entre cenos de la Formacio´ n Cura-Mallin, Chile (37–39 S): implicancias Rı´os. Boletı´n de la Academia Nacional de Ciencias de Co´ rdoba paleogeogra´ficas. Revista Geolo´ gica de Chile 21:3–29. (Repu´ blica Argentina) 24:55–256. Scartascini, G. 1954. El lı´mite Plio-Pleistoceno de la Provincia de Entre Gayet, M., and F. Meunier. 1998. Maastrichtian to early late Paleocene Rı´os. Revista del Museo Municipal de Ciencias Naturales de Mar freshwater Osteichthyes of Bolivia: additions and comments; pp. del Plata 1:55–77. 85–11 in Z. M. Lucena, R. E. Reis, R. P. Vari, and C. A. Lucena Shellis, R. P., and B. K. Berkovitz. 1976. Observations on dental anato- (eds.), Phylogeny and Classification of Neotropical Fishes. EDI- my of piranhas (Characidae) with special reference to tooth struc- PUCRS, Porto Alegre. ture. Journal of Zoology 180:69–84. Gosline, W. 1951. Notes on the Characid fishes of the subfamily Serra- Swofford, D. L. 1998. PAUP* 4.0b10. Phylogenetic analysis using parsi- salminae. Proceedings of the California Academy of Sciences 27: mony. Sinauer Associates, Inc., Sunderland, MA. 17–64. Uliana, M. A., and K. T. Biddle. 1988. Mesozoic-Cenozoic paleogeo- Gu¨ nther, A. 1864. Catalogue of Fishes in the British Museum. London, 5: graphic and geodynamic evolution of southern South America. i–xii+ 1–455. Revista Brasileira de Geocieˆncias 18:172–190. Iriondo, M. H. 1980. El Cuaternario de Entre Rı´os. Revista de la Asocia- Zanata, A. M., and R. P. Vari. 2005. The family Alestidae (Ostariophysi, cio´ n de Ciencias Naturales del Litoral 11:125–141. Characiformes): a phylogenetic analysis of a trans-Atlantic clade. Je´gu, M. 1989. Une nouvelle espe`ce du genre Mylesinus (Pisces, Serra- Zoological Journal of the Linnean Society 145:1–144. salmidae), M. paraschomburgkii,de´crite des bassins du Trombetas et du Uatuma˜ (Bre´sil, Amazonie). Revue d’Hydrobiologie Tropi- Submitted July 30, 2007; accepted October 4, 2008 cale 22:49–62. Je´gu, M. 2003. Subfamily Serrasalminae (pacus and piranhas); pp. APPENDIX 1. Comparative material examined, listed as species, num- 182–196 in R. E. Reis, C. J. J. Ferraris, and S. O. Kullander (eds.), ber of specimens, specimen preparation, and catalog number. Abbrevia- CLOFFSCA, Check List of Freshwater Fishes from South and Cen- tions: CS, cleared and counterstained; sk, skeleton. Institutional tral America. EDIPUCRS, Porto Alegre. Abbreviations: ANSP, Academy of Natural Sciences, Philadelphia, Je´gu, M. 2004. Taxinomie des Serrasalminae phytophages et phylogenie Pennsylvania; DUF, Duke University, Durham, North Carolina; INPA, des Serrasalminae (Teleostei: Characiformes: Characidae). PhD Instituto Nacional de Pesquisas da Amazonia, Manaus, Brazil; MNHN, thesis Museum National d’Histoire Naturelle, 423 pp. Muse´um National d’Histoire Naturelle, Paris, France; MBUCV, Univer- Lundberg, J. G. 1997. Fishes of the Miocene La Venta Fauna: additional sidad Central de Venezuela, Museo de Biologia, Caracas, Venezuela; taxa and their paleobiotic implications; pp. 67–91 in R. F. Kay, MZUSP, Universidade de Sa˜o Paulo, Museu de Zoologia, Sa˜o Paulo, R. H. Madden, R. L. Cifelli, and J. J. Flynn (eds.), Vertebrate Brazil; UNT, Universidade Federal do Tocantins, Porto Nacional, Brazil. Paleontology in the Neotropics: The Miocene Fauna of La Venta, Acnodon normani, 1, sk, UNT 1989; Catoprion mento, 1, sk, MBUCV Colombia. Smithsonian Institution Press, Washington, D.C. uncat.; Colossoma macropomum, 8, sk, INPA 20906; Colossoma macro- Lundberg, J. G. 1998. The temporal context for the diversification of pomum, 1, sk, DUF 1072; Metynnis sp., 1, sk, DUF 1178; Metynnis neotropical fishes, pp. 49–68 in Z. Lucena, R. Reis, R. Vari, and argenteus, 1, sk, MBUCV uncat. C. Lucena (eds.), Phylogeny and Classification of Neotropical Fish- Mylesinus paucisquamatus, 1, sk, UNT 1988; Myleus setiger, 1, sk, UNT es. EDIPUCRS, Porto Alegre. 1984; Myleus schomburgkii, 1, sk, ANSP 180812; Mylossoma acanthoga- Lundberg, J. G., A. Machado-Allison, and R. F. Kay. 1986. Miocene ster, 1, sk, MBUCV uncat.; Mylossoma aureum, 3, sk, MBUCV uncat.; characid fishes from Colombia: evolutionary stasis and extirpation. Mylossoma duriventre, 1, sk, ANSP 178553; Mylossoma duriventre, 1, sk, Science 234:208–209. DUF 1059; Mylossoma duriventre, 1, sk, DUF 1063; Ossubtus xinguense, Machado-Allison, A. 1982. Studies on the systematics of the subfamily 1, CS, MNHN 1998-1168; Piaractus brachypomus, 1, sk, ANSP 178554; Serrasalminae (Pisces-Characidae). PhD thesis The George Piaractus brachypomus, 1, sk, DUF 1050; Piaractus mesopotamicus, 1, sk, Washington University, Washington, D.C., 267 pp. ANSP 182451; Pristobrycon cf. calmoni, 1, sk, DUF 160; Pygocentrus Machado-Allison, A. 1983a. Estudios sobre la subfamilia Serrasalminae cariba, 1, sk, DUF 1173; Pygocentrus cariba, 1, sk, DUF 1174; Pygocen- (Teleostei, Characidae). Parte I. Estudio comparado de los juveniles trus nattereri, 1, sk, ANSP 178555; Pygopristis denticulatus, 1, sk, ANSP de las “Cachamas” de Venezuela (Ge´neros Colossoma y Piaractus). uncat.; Serrasalmus brandtii, 1, sk, MZUSP 04-54; Serrasalmus rhombeus, Acta Biolo´ gica Venezuelica 11:1–101. 1, sk, ANSP 178558. Machado-Allison, A. 1983b. Estudios sobre la sistema´tica de la subfami- lia Serrasalminae (Teleostei, Characidae). Parte II. Discusio´ n sobre APPENDIX 2. Subset of the morphological characters and character la condicio´ n monofile´tica de la subfamilia. Acta Biolo´ gica Venezue- states reported in Dahdul (submitted, Proc. Acad. Nat. Sci.) and coded lica 11:145–195. for Megapiranha paranensis. These characters were optimized on the Marshall, L., R. Hoffstetter, and R. Pascual. 1983. Mammals and stratig- strict consensus tree (Fig. 6). raphy: geochronology of the continental mammal-bearing Tertiary 1. Premaxillae interdigitated at symphysis: 0, absent; 1, present. of South America. Palaeovertebrata Me´moire Extraordinaire 1–93. 2. Distal end of premaxillary dentigerous arm: 0, extended to form Nico, L. G. 1991. Trophic ecology of piranhas (Characidae: Serrasal- elongate, pedicle-like process; 1, truncated, not extending significantly minae) from savanna and forest regions in the Orinoco river beyond posteriormost tooth. basin of Venezuela. Ph.D. dissertation, University of Florida, Flor- 3. Dorsal margin of premaxillary dentigerous arm: 0, straight or mod- ida, 210 pp. erately convex dorsal margin; 1, concave dorsal margin lateral to ascend- Ortı´, G., P. Petry, J. I. R. Porto, M. Je´gu, and A. Meyer. 1996. Patterns ing process of premaxilla. of nucleotide change in mitochondrial ribosomal RNA genes 4. Tooth arrangement on premaxilla: 0, single row of teeth; 1, two rows and the phylogeny of piranhas. Journal of Molecular Evolution 42: of teeth; 2, three rows of teeth; 3, teeth roughly arranged in double-row 169–182. with mesial four teeth displaced in shallow zig-zag pattern. Pascual, R., and O. Odreman Rivas. 1971. Evolucio´ n de las comunidades 5. Shape of jaw teeth: 0, crown with peaked transverse cutting edge, de los vertebrados del Terciario argentino. Los aspectos paleozoo- crown usually expanded in axis perpendicular to cutting edge, inner row geogra´ficos y paleoclima´ticos relacionados. Ameghiniana 8:372–412. teeth with central valley bordered anteriorly by ridge and posteriorly by Reig, O. A. 1957. Sobre la posicio´ n sistema´tica de Zygolestes paranensis cutting edge; 1, all teeth tuberculate; 2, all teeth pentacuspidate; 3, all Amegh. y de Zygolestes entrerrianus Amegh. con una reconsidera- teeth triangular, bladelike. cio´ n de la edad y correlacio´ n del “Mesopotamiense.” Holmbergia 6. Cutting edge of jaw teeth: 0, smooth, without serrations; 1, finely 5:209–226. serrated. Ringuelet, R. A., R. H. Ara´mburu, and A.A.d. Ara´mburu. 1967. Los 7. Number of premaxillary teeth: (0) 7; (1) 6; (2) 5; (3) greater than 7. peces argentinos de agua dulce. Comisio´ n de Investigaciones Cientı´- 8. Attachment base of the distal most teeth: 0, circular to subcircular; ficas, La Plata, 602Proof pp. 1, labiolingually Only compressed.