Journal of Paleontology, 87(5), 2013, p. 755–774 Copyright Ó 2013, The Paleontological Society 0022-3360/13/0087-755$03.00 DOI: 10.1666/12-117

SHARKS AND RAYS (CHONDRICHTHYES, ELASMOBRANCHII) FROM THE LATE MIOCENE GATUN FORMATION OF PANAMA CATALINA PIMIENTO,1,2,3 GERARDO GONZA´ LEZ-BARBA,4 DANA J. EHRET,5 AUSTIN J. W. HENDY,1,2 1 2 BRUCE J. MACFADDEN, AND CARLOS JARAMILLO 1Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA, ,[email protected].; ,[email protected].; ,[email protected].; 2Smithsonian Tropical Research Institute, Center for Tropical Paleoecology and Archaeology, Box 2072, Panama, Republic of Panama, ,[email protected].; 3Department of Biology, University of Florida, Gainesville, FL 32611, USA; 4Museo de Historia Natural, Area de Ciencias del Mar, La Paz, Universidad Autonoma de Baja California Sur, AP 23080, Mexico, ,[email protected].; and 5Alabama Museum of Natural History, University of Alabama, Tuscaloosa, Alabama, 35487, USA, ,[email protected].

ABSTRACT—The late Miocene Gatun Formation of northern Panama contains a highly diverse and well sampled fossil marine assemblage that occupied a shallow-water embayment close to a purported connection between the Pacific and Atlantic (Caribbean) oceans. However, the diverse chondrichthyan fauna has been poorly documented. Based on recent field discoveries and further analysis of existing collections, the chondrichthyan fauna from this unit comprises at least 26 taxa, of which four species are extinct today. The remaining portion of the total chondrichthyan biodiversity has affinities with modern taxa and is therefore comprised of long-lived species. Based on known records of the modern geographic distribution range of the Gatun chondrichthyans, the fauna has mixed biogeographic affinities suggesting that around 10 million yr ago, a connection likely occurred between the Pacific Ocean and the Caribbean Sea. Given the known habitat preferences for modern chondrichthyans, the Gatun fauna was primarily adapted to shallow waters within the neritic zone. Finally, comparisons of Gatun dental measurements with other faunas suggest that many of the taxa have an abundance of small individuals, in agreement with previous studies that proposed this area as a paleonursery habitat for the species Carcharocles megalodon.

INTRODUCTION noted three species from the Miocene deposits of Monkey Hill HE LATE Miocene Gatun Formation comprises fossiliferous (present-day Colon). Of most significance to the current study, T sediments that crop out on the Caribbean coast of the Gillette (1984) described the fossil chondrichthyans from the Isthmus of Panama, and contains a highly diverse macro- and Gatun Formation. Based on screenwashing of sediments at a microfossil fauna (e.g., Woodring, 1957–1982; Collins et al., now inaccessible (i.e., covered by urban development) locality, 1996, 1999; Jackson and Budd, 1996; Jackson et al., 1999; Uhen he described the diversity, ecology, and biogeography of 14 et al., 2010; Hendy, 2013). Previous studies of the invertebrate chondrichthyan taxa. Most recently, Pimiento et al. (2010) fauna from the Gatun Formation indicate this area was a studied the natural history of the species Carcharocles shallow-water embayment that supported a neritic environment megalodon fromtheGatunFormationandproposedthatthey (Teranes et al., 1996). It has been postulated that this area was a used this area as a nursery habitat. Lastly, Pimiento et al. (2013) strait connecting the Pacific Ocean and the Caribbean Sea described the chondrichthyan fauna from the early Miocene (Coates and Obando, 1996), although subsequent workers have Culebra Formation and studied their paleoenvironmental setting suggested that any connection likely existed in a more distal and paleobiogeography. location (Collins et al., 1996, 1999; Teranes et al., 1996; Kirby Over the past 20 yr, the Gatun Formation localities have been et al., 2008). Regardless, all these studies show that the Gatun extensively quarried to extract sediment for construction marine faunas existed during a time of active transoceanic projects in the Colon region and contour surfaces for residential interchange and dispersal before the time of the final closure of developments. These quarries have both uncovered fresh the Central American Seaway (CAS). outcrops, but these are typically ephemeral (e.g., Gillette’s It is generally accepted that the final closure of the CAS took locality). Extraction activities have increased substantially in place about 3 million yr ago (Duque-Caro, 1990; Coates et al., recent years and numerous well-established outcrops are being 1992, 2003, 2004; Coates and Obando, 1996; Bartoli et al., completely removed or covered by urban development. We 2005). However, a number of recent studies suggest that the predict that many of the critical outcrops of the Gatun Formation shoaling of the Isthmus began during the middle–late Eocene will soon disappear. Given that the only systematic paleontology and likely resulted in the final closure during the middle paper on the chondrichthyans of the Gatun Formation was Miocene (Farris et al., 2011; Montes et al., 2012a, 2012b). In published 28 yr ago based on a single locality and collection any case, this closure was a key vicariant event for tropical method, we consider it important to recover and document new biotic evolution (Cronin and Dowsett, 1996) that resulted in the specimens from different sections before they are no longer separation of the once continuous marine distribution, and an available. Accordingly, we have collected and/or studied a total increase of habitat and biogeographic complexity (e.g., Wood- of 800 specimens from 15 localities from the Gatun Formation. ring, 1974; Rosen, 1975; Jackson and Budd, 1996; Aguilera et This material includes the original specimens described in al., 2011). Gillette (1984), new specimens collected by our team, and Fossil chondrichthyans from Panama are poorly known in the additional specimens in the Smithsonian National Museum of literature. The earliest record was reported by Blake (1862) who Natural History, Washington, D.C. 755 756 JOURNAL OF PALEONTOLOGY, V. 87, NO. 5, 2013

The purpose of this report is to revise and update the fossil Formation, Maryland (Tedford et al., 2004); Can´ımar Forma- record of the chondrichthyan fauna from the Gatun Formation. tion, Cuba (Iturralde-Vinent, 1969); Grand Bay Formation of Here, we review and describe all relevant known material. Carriacou; Grenadines, Lesser Antilles (Donovan and Gunter, Furthermore, based on our study of the fossil specimens and the 2001); and Rio Banano Formation, Costa Rica (Taylor, 1975; information available on extant related species, we evaluate the Laurito, 1999); 3) younger, early Pliocene assemblages include: diversity, taxonomic composition, paleobiogeography, paleo- Yorktown Formation, North Carolina (Ward and Bohaska, environment, and paleoecology of the chondrichthyan fauna of 2008); Bone Valley, Florida (Morgan, 1994; Tedford et al., the Gatun Formation. Results of this study enhance our 2004); Pisco Formation (upper part), Peru (De Muizon and understanding of the chondrichthyans of the ancient Neotropics DeVries, 1985); and Cubagua Formation, Venezuela (Aguilera, at a time when the Pacific Ocean and the Caribbean Sea were 2010). connected through Central America. With respect to the paleogeography, it has been postulated that the Gatun Formation was deposited within an archipelagic GEOLOGICAL SETTING strait connecting the Pacific Ocean and the Caribbean Sea The fossil chondrichthyan teeth described in this paper were (Coates and Obando, 1996). Subsequent workers indicated that collected from late Miocene marine sediments of the Gatun waters had shoaled to the point the strait was restricted (Collins Formation. This formation crops out in a broad area of northern et al., 1996, 1999). Most recently, it has been suggested that Panama (Fig. 1) extending along the northern shore of Lake contrary to an archipelago, a subaerial peninsula connected to Gatun, approximately 15 km northward to the Caribbean Sea, North America existed during this time (Kirby and MacFadden, and approximately 50 km east and west of Colon City, within 2005; Kirby et al., 2008). Regardless, all these studies show that the Panama Canal structural basin. In the study area, the gently a passageway existed between Central and South America, and dipping (58) Gatun Formation is thought to overlie unnamed it was located near to the deposition of sediments of the Gatun Cretaceous–Paleogene volcanic and volcaniclastic sediments or Formation. Therefore, the Gatun faunas existed during a time of the upper Oligocene sediments of the Caimito Formation active transoceanic interchange and dispersal (Collins et al., (Woodring, 1957–1982; Coates et al., 1992; Coates, 1999) 1996, 1999; Newkirk and Martin, 2009). (Fig. 2). With regard to the paleoecology of the Gatun Formation, The Gatun Formation, with a stratigraphic thickness of 500 m, foraminifera (Collins, 1996), invertebrates (e.g., Coates and consists of three informal members (Fig. 2) referred to as the lower, middle, and upper Gatun in most publications (e.g., Obando, 1996; Collins et al., 1996; Jackson et al., 1999; Hendy, Woodring, 1957–1982; Coates, 1999). Of relevance to this 2013) and fish otoliths (Aguilera and Rodrigues de Aguilera, report, most of the fossils collected during our study, and likely 1999) indicate a shallow-water marine shelf neritic environ- those of Gillette (1984), occur within the lower member. The ment. A recent review of the paleoenvironments of the Gatun lithology of these sediments consists of massive, gray-green Formation suggests that most of the formation accumulated in clayey siltstone and interbedded concretions. This member of depths ranging from shallow subtidal to 50 m, although the the Gatun Formation is highly fossiliferous, with diverse sediments of the upper member accumulated in as much as 100 molluscan assemblages (up to 259 genera and 359 species: m of water (Hendy, 2013). Studies of oxygen isotope ratios Woodring, 1957–1982; Jackson et al., 1999). At some localities preserved in mollusk shells from the Gatun Formation indicate within the Gatun Formation (e.g., Las Lomas, located ~12 km that it was deposited in a productive shallow-water embayment, southeast of Colon, locality 1 in Fig. 1.2) the highly fossiliferous and that salinity, annual temperature variations, relative nature of the sediments and weathering processes result in seasonality and productivity were different during the late pavements of macrofossils (primarily bivalves and gastropods). Miocene relative to those of today (Teranes et al., 1996). Within this taphonomic context, marine vertebrate macrofossils REPOSITORIES, COLLECTING TECHNIQUES AND STATISTICAL ANALYSES recovered by surface prospecting consist mostly of chon- drichthyan teeth and ray tooth plates, as well as osteichthyan Specimens from the following vertebrate paleontology teeth (e.g., barracuda), turtle shell fragments, and rare collections were examined during this study and are abbreviated mammalian bones (Uhen et al., 2010). In addition, screen- in the text as follows: UF, Vertebrate Paleontology Collection, washing of the siliciclastic matrix yielded rich microfossil Florida Museum of Natural History, University of Florida, assemblages, including benthic foraminifera (Collins, 1996), Gainesville, Florida; SMU, Shuler Museum of Paleontology, osteichthyan otoliths (Aguilera and Rodrigues de Aguilera, Southern Methodist University, Dallas, Texas; and USNM, 1999), and many small chondrichthyan taxa (Gillette, 1984). Smithsonian Institution, National Museum of Natural History, Multiple lines of biostratigraphic evidence from the rich Washington, D.C. marine invertebrate fauna indicate that the Gatun Formation is The UF material was collected by surface prospecting and late Miocene in age, spanning from about 11.8 to 8.4 million yr screenwashing between August 2007 and September 2011 from ago (Coates, 1999; Jackson et al., 1999; Hendy, 2013; Fig. 2). 12 localities (Figs. 1, 2) by the Panama Canal Project (PCP) Among other similarly diverse and relatively well-sampled field team at the Center for Tropical Paleoecology and marine faunas in coastal regions of the western hemisphere, Archaeology of the Smithsonian Tropical Research Institute several faunas containing chondrichthyans bracket those of the (STRI). This material is housed at UF and relevant data are Gatun Formation: 1) older, early–middle Miocene assemblages available on the UF online database (http://www.flmnh.ufl.edu/ include: Shark tooth Hill, California (Pyenson et al., 2009); databases/VP/intro.htm), where every fossil locality is coded Pungo River, North Carolina (Ward and Bohaska, 2008); (YPA, see caption Fig. 1.2). The screenwashing methodology Agricola fauna, Florida (Morgan, 1994); Calvert fauna, consisted of washing approximately 500 kg of sediment from Maryland (Tedford et al., 2004); Domo de Zaza, Cuba the three most fossiliferous localities (Las Lomas, Isla Payardi (MacPhee et al., 2003; Iturralde-Vinent et al., 1969); Cantaure and San Judas; localities 1, 2, and 5 respectively in Figs. 1, 2). Formation, Venezuela (Aguilera, 2010); and Uscari Formation, Samples were processed using standard screenwashing methods. Costa Rica (Pizarro, 1975; Laurito, 1999); 2) roughly contem- We used sets of screens of 6, 1.5, 1, and 0.5 mm open mesh. poraneous late Miocene assemblages include: St. Marys Screenwashed matrix was picked for chondrichthyan teeth using PIMIENTO ET AL.—LATE MIOCENE SHARKS AND RAYS FROM PANAMA 757

FIGURE 1—Area of study. 1, location of Gatun Formation (shaded box) in northern Panama; 2, expanded geological map showing exposures of the Gatun Formation and surrounding rock units (modified from Coates et al., 1992) including the 15 fossil localities collected during this study: 1, YPA017 Las Lomas: 98210 15.6600 N, 79850011.3400 W; 2, YPA021 Isla Payardi: 9822057.1800 N, 79849016.5000 W; 3, YPA022 Cuatro Altos: 982007.0800 N, 79852058.8000 W; 4, YPA020 Banco EE: 9817059.1100 N, 7985505.3600 W; 5, YPA032 San Judas: 982115.6600 N, 7985011.327400 W; 6, YPA044 Sand Dollar Hill: 982102.62800 N, 79848035.53200 W; 7, YPA030 Alborada: 9820027.02400 N, 7984900.80400 W; 8, YPA033 Texaco: 9820058.847400 N, 79848047.30400 W; 9, YPA045 I.D.A.A.N.: 9820035.519400 N, 7984804500 W; 10, YPA 046 Third Set of Locks: 9816046.9200 N, 79854048.2400 W; 11, YPA043 Highway Extension 9820037.500 N, 7984900.9900 W; 12, USNM: USGS 58461, Gatun Dam: 9815046.0800 N, 79856026.1600 W; 13, USNM:USGS 8375, Gatun Dam: 9815053.279400 N, 798550’54.479400 W; 14, USNM: TU960, Refiner´ıa Panama: 9822056.6400 N, 79849016.3200 W; 15 Sabanitas (Gillette, 1984) 9820059.9900 N, 79847059.999400 W. Lower Gatun localities include 1, 2, 5–9, 11, 14, 15; middle Gatun localities include 3, 10, 12, 13; and the upper Gatun locality is 4. YPA¼fossil locality code in the FLMNH database (http://www.flmnh.ufl.edu/ databases/VP/intro.htm). a magnifying glass for the coarser matrix, and a stereomicro- housed in the SMU Vertebrate Paleontology collection. This scope for the finest matrix. material was collected in 1978 and 1979 from an exposure at a In addition to the material collected in the field, we also single locality called ‘‘Sabanitas’’, now inaccessible (locality 15 borrowed specimens described by Gillette (1984), which are in Figs. 1, 2). His collection method consisted of screenwashing 758 JOURNAL OF PALEONTOLOGY, V. 87, NO. 5, 2013

sum, we identified a total of 26 taxa for the Gatun chondrichthyan fauna. Most of the material comes from a relatively limited thickness of stratigraphy in the lower Gatun Formation, specifically Las Lomas and San Judas (localities 1 and 2, respectively, in Fig. 2). These localities were among the most fossiliferous and accessible of exposures in the formation, and have been exposed for a significant period of time, resulting in considerable weathering of stratigraphic surfaces and concentration of macrofossils. Furthermore, a majority of specimens from this study were collected by surface prospecting. However, some small-toothed taxa such as Ginglymostoma delfortriei, Rhizo- prionodon sp., Sphyrna lewini, Taeniura aff. grabata, Mobula munkiana, Mobula thurstoni and Mobula hypostoma were only found using screenwashing. Taxa with a broad range of tooth size such as Sphyrna sp., Carcharhinus sp., Negaprion brevirostris, Aetobatus narinari,andRhinoptera cf. steindach- neri were found with both screenwashing and surface prospect- ing techniques (Fig. 3). A randomized species accumulation curve (Fig. 4) was produced to analyze the sampling effort (field days) in relation with the species richness. This curve was created using the vegan package (Oksanen et al., 2010) of the R program (R- Development-Core-Team, 2012). The accumulation curve indicates that increased effort will unlikely result in finding a significant number of additional taxa, and we therefore have confidently sampled most of the biodiversity of the Gatun chondrichthyan community.

SYSTEMATIC PALEONTOLOGY The specimens were described following the terminology of Cappetta (1987, 2012), Herman et al. (1997, 1998, 1999, 2000), and Shimada (2002). The material was first identified by the authors using comparative collections available at UF. Identi- fications were then verified by Dr. G. Hubbell using his private collection in Gainesville, FL. The geographic distribution of each taxon was retrieved from the literature and aided by using the Paleobiology Database (www.paleodb.org). All original sources of data are cited herein. Macro-teeth were measured with calipers, whereas the micro-teeth were measured using the FIGURE 2—Stratigraphy and sampling of the Gatun Formation. Fossil images produced by the SEM (scanning electron microscope). localities are indicated by the numbers defined in Figure 1.2. The number of Toothmeasurementswerecomparedwhenpossiblewitha sampling days (white) and elements recovered (black) from fossil localities are pooled for 50 m intervals of the composite stratigraphy of Hendy (2013). previous work on the Neogene chondrichthyans of the Pungo River Formation (middle Miocene) and the Yorktown Formation (early Pliocene) at Lee Creek Mine, North Carolina (Purdy et ~900 kg of sediment using traditional wet-sieving methods (for al., 2001), which are older and younger, respectively, than the more detailed information see Gillette, 1984). Furthermore, we Gatun Formation. Shark teeth measurements are abbreviated as borrowed specimens deposited at the USMN collected by R. follows: CH, tooth crown height; CW, tooth crown width; TL, Stewart and W. P. Woodring (former USGS collections), and by total body length. E. and H. Vokes (former Tulane University collections), both between the 1950s and 1970s. Class CHONDRICHTHYES Huxley, 1880 In total, 800 specimens were studied from 15 different Subclass ELASMOBRANCHII Bonaparte, 1838 Order ORECTOLOBIFORMES Applegate, 1974 localities. Of the 634 specimens collected by our team (UF Family GINGLYMOSTOMATIDAE Gill, 1872 material, screenwashing and surface prospecting, 12 localities) Genus GINGLYMOSTOMA Mu¨ller and Henle, 1838 we identified 24 taxa. Of the 161 specimens borrowed from the GINGLYMOSTOMA DELFORTRIEI (Daimeries, 1889) Gillette’s (1984) work (SMU material, screenwashing, one Figure 5.1 locality), we identified eight taxa, of which two were distinct from our collecting efforts (Ginglymostoma delfortriei and Description.—Ginglymostoma delfortriei tooth from the Gatun Sphyrna lewini). It is noteworthy that in contrast to our Formation measures CH¼5.0 mm and W¼8.4 mm (Fig. 5.1). For a detailed description see Gillette (1984). identifications, Gillette (1984) reported 14 taxa. The difference Material.—Two isolated teeth; indeterminate position (SMU in number of taxa is due to the fact that some specimens were 76460 and SMU 76470). missing from the SMU and in part reflects the redescription of Occurrence.—Lower Gatun locality 15 (Figs. 1, 2). the originally collected material. Lastly, specimens borrowed Remarks.—In the Pungo River Formation, Purdy et al. (2001) from USNM (three localities) contributed only three taxa. In described one nurse shark tooth (Ginglymostoma sp.). This PIMIENTO ET AL.—LATE MIOCENE SHARKS AND RAYS FROM PANAMA 759

FIGURE 3—Late Miocene chondrichthyans from the Gatun Formation of Panama and proportional abundances (100%¼800 teeth) of each taxa using two different collection techniques. Key: gray¼missing specimens from the SMU collection and therefore not available for comparison; *¼in agreement with our identification, but the taxonomy has been updated; **¼assigned to a different species; þ¼new records; †¼extinct taxa. specimen is very different from the G. delfortriei teeth studied and USNM 960; lower anteriors: UF 237950, UF 237959, UF here, with fewer cusps and a transverse groove. Ginglymostoma 245995; upper laterals: UF 237914, UF 237951–237952, UF delfortriei is also reported in Venezuela and Costa Rica (Aguilera 242802–242803, UF 245852, UF 245885–245886, UF 246033; and Rodrigues de Aguilera, 2001; Laurito, 1999). Regarding the lower lateral: UF 237953; upper posterior: UF 237957, UF ecology, extant species of the family Ginglymostomatidae (nurse 245925, UF 246002; lower posterior: UF 237956, UF 245844, UF sharks) are subtropical and tropical, associated with corals, rocky 245996; indeterminate position: UF 237913, UF 237958, UF reefs, sandy areas and mangroves; with a depth range of intertidal 237960, UF 242801, UF 246001, UF 247250–247254, UF to 70 m (Compagno et al., 2005). 247256, UF 257576–257579, UF 266846, UF 266853–266858. Order LAMNIFORMES Berg, 1958 Occurrence.—Lower Gatun localities 1, 2, 7, 8, 14; middle Family OTODONTIDAE Glikman, 1964 Gatun locality 10; upper Gatun locality 4 (Figs. 1, 2). Genus CARCHAROCLES Jordan and Hannibal, 1923 Remarks.—Teeth of C. megalodon (referred in Gillette, 1984 as CARCHAROCLES MEGALODON (Agassiz, 1843) Figure 5.2–5.4

1835 Carcharodon megalodon AGASSIZ, pl. 29, figs. 1–6. Description.—Large size, triangular shape. Broad serrated crown, lingual face convex, labial face flat, large neck; robust, thick, angled or U-shaped root with dispersed foramina (Fig. 5.2– 5.4). Juvenile teeth of C. megalodon can have lateral cusplets (Fig. 5.4; Ward and Bonavia, 2001; Pimiento et al., 2010). Carcharocles megalodon differs from Carcharodon carcharias by having larger teeth with larger roots and finer, more regular and lobed serrations (Nyberg et al., 2006); lacking a labiolin- gually flattened crown (Purdy et al., 2001); and the presence of a neck. Carcharocles megalodon teeth from the Gatun Formation ranges in size from CH¼11.2 to 72.3 mm and CW¼16.1 to 63.2 mm. Material.—Forty-nine (49) isolated teeth; upper anteriors: UF FIGURE 4—Species accumulation curve for the chondrichthyans of the 237898, UF 237949, UF 237954–237955, UF 242804, UF 247248 Gatun Formation. Shaded polygon represents confidence intervals. 760 JOURNAL OF PALEONTOLOGY, V. 87, NO. 5, 2013

FIGURE 5—Shark teeth from the late Miocene Gatun Formation, Panama. 1, †Ginglymostoma delfortriei (Daimeries, 1889), SMU 76470, indeterminate position; 2–4, †Carcharocles megalodon (Agassiz, 1843): 2, UF 237950, largest anterior tooth; 3, UF 237959, smallest anterior tooth; 4, UF 237914, lateral tooth; 5–8, †Hemipristis serra (Agassiz, 1843): 5, UF 237941, largest upper tooth; 6, UF 237924, smallest upper tooth; 7, SMU 76467, smallest lower tooth; 8, UF 242806, largest complete lower tooth; 9, Galeocerdo cuvier (Peron and Lesueur, 1822), UF 237902, indeterminate position; 10, †Physogaleus contortus (Gibbes, 1849), UF 237908, indeterminate position; 11, Carcharhinus falciformis (Bibron, 1841 in Muller and Henle 1839–1841), UF 241817, upper tooth, square showing location of gap lacking of serrations; 12, Carcharhinus leucas (Valenciennes, 1839 in Muller and Henle 1839–1841), UF 241829, upper tooth; 13, Carcharhinus obscurus (Lesueur, 1818), UF 242839, upper tooth; 14, Carcharhinus perezi (Poey, 1876), UF 242851, upper tooth; 15, Carcharhinus plumbeus (Nardo, 1827), UF 242860, upper tooth; 16, 17, Carcharhinus sp.: 16, UF 238004, upper tooth; 17, UF 241828, lower tooth; 18, Negaprion brevirostris (Poey, 1868), UF 241814, indeterminate position; 19, Rhizoprionodon sp. (Griffith and Smith, 1834), SMU 76475, indeterminate position; 20, Sphyrna lewini (Griffith and Smith, 1834), SMU 76458, upper tooth; 21, Sphyrna mokarran (Ru¨ppell, 1837), UF 237912, upper tooth; 22, Sphyrna sp., UF 242868, upper tooth. Scale bar¼5 mm.

Procarcharodon megalodon and in Purdy et al., 2001 as a juvenile stage (Fig. 5.4). The taxonomic assignment of this Carcharodon megalodon) can reach CH¼168 mm and TL is species has been debated for nearly a century with numerous estimated to have been over 15 m (Gottfried et al., 1996). Teeth possible interpretations. For discussion on our assignment here to from the Yorktown Formation are larger than teeth from the Carcharocles, and not Carcharodon, Procarcharodon or Mega- Gatun Formation, ranging in size from CH¼60.0 to 150.0 mm selachus, see Pimiento et al. (2010) and Ehret et al. (2012). (Purdy et al., 2001). Tooth morphology of C. megalodon changes Megatoothed sharks of the genus Carcharocles were common and with the age. During the juvenile stage, teeth may or may not widely distributed in tropical to warm-temperate coastal habitats present lateral cusplets (for discussion see Applegate and (Gottfried el al., 1996; Purdy, 1996). Carcharocles megalodon Espinosa-Arrubarrena, 1996; Ward and Bonavia, 2001; Pimiento was a cosmopolitan species (Cappetta, 1987; Purdy, 1996; Purdy et al., 2010, 2013). UF 237914 presents lateral cusplets indicating et al., 2001). In the Neotropics, it has been reported both in the PIMIENTO ET AL.—LATE MIOCENE SHARKS AND RAYS FROM PANAMA 761

Caribbean and the Pacific (Iturralde-Vinent et al., 1996; Long- shore and off-shore waters from 1 to 30 m depth (Compagno, bottom, 1979; De Muizon and DeVries, 1985; Long, 1993; 1984). Laurito, 1999; Donovan and Gunter, 2001; Nieves-Rivera et al., 2003; Aguilera and Rodrigues de Aguilera, 2001; Portell et al., Family CARCHARHINIDAE Jordan and Evermann, 1896 2008). The species may have occurred in waters as deep as 300 m, Genus GALEOCERDO Mu¨ller and Henle, 1837 although it is more frequently collected from sediments GALEOCERDO CUVIER (Peron and Lesueur, 1822) representing neritic environments (e.g., Aguilera and Rodrigues Figure 5.9 de Aguilera, 2001). The relatively small size of many of the C. megalodon teeth from the Gatun Formation indicates a prepon- Description.—Large and robust teeth with slanted crowns; derance of juveniles, and suggests that this species used the mesial edge rounded, with fine serrations at the base of crown, shallow waters of northern Panama as a nursery area during the which is basally and apically straight, forming an obtuse angle; late Miocene (Pimiento et al., 2010). distal edge has a pronounced notch and have coarser serrations on the heel and base; U-shaped root with no central foramen (Fig. Order CARCHARHINIFORMES Compagno, 1977 5.9). Galeocerdo cuvier teeth are similar to those from Family HEMIGALEIDAE Compagno, 1984 Physogaleus aduncus, but have a broader and larger crown, and Genus HEMIPRISTIS Agassiz, 1843 a more strongly convex mesial cutting edge. Galeocerdo cuvier HEMIPRISTIS SERRA (Agassiz, 1843) teeth from the Gatun Formation range in size from CH¼7.4 to Figure 5.5–5.8 17.8 mm and CW¼14.4 to 24.5 mm. A transverse groove is present in the root of some, but not all teeth. Description.—Upper teeth have distally curved crowns, Material.—Twenty five (25) isolated teeth; indeterminate oblique coarse serrations not continued to the apex, rectilinear position: UF 237901–237907, UF 241809–241812, UF 242819– mesial cutting edge, concave distal cutting edge with fewer 242822, UF 245908, UF 245943–245944, UF 245982, UF serrations; root high and compressed with a lingual protuberance 247315, UF 266859, SMU 76456, SMU 76465, SMU 76466, forming a Z-shape. Upper teeth are generally broader than the and SMU 76475. corresponding lowers (Fig. 5.5, 5.6). Lower teeth have unserrated, Occurrence.—Lower Gatun localities 1, 2, 8, 15 (Figs. 1, 2). long, pointing and lingually inclined crowns; convex labial faces, Remarks.—Extant G. cuvier can reach up to TL¼7.5 m small cusplets near the base, and bilobated roots with a lingual (Compagno, 1984). Based on fossil teeth, it probably grew to protuberance (Fig. 5.7, 5.8). Upper teeth of H. serra differ from less than half this length in the past (Kent, 1994). The teeth the genus Carcharhinus by having a distinctively smooth apex collected in the Yorktown Formation range from CH¼13.5 to 29.1 and oblique serrations; lower teeth differ from the genus mm and CW¼24.4 to 33.0 mm (Purdy et al., 2001), which are Carcharias by having incomplete cutting edges on both mesial larger than those found in the Gatun Formation. In the Neotropics, and distal side margins that are limited to approximately the G. cuvier is reported in the Miocene of Venezuela and Brazil apical third of the crown (Kent, 1994). In the Gatun Formation (Aguilera and Rodrigues de Aguilera, 2001; Reis, 2005). Extant this species varies greatly in size, from CH¼ 5.4 to 21.6 mm and G. cuvier have a cosmopolitan distribution in coastal-pelagic, CW¼ 5.2 to 29.0 mm. tropical and warm-temperature waters, with tolerance for a wide Material.—One hundred twenty two (122) isolated teeth; range of habitats at depths from intertidal waters to 140 m uppers: UF 237919–237948, UF 241803–241808, UF 241835, (Compagno, 1984, 1988). UF 242810–242817, UF 245891–245892, UF 255909, UF 255915–255916, UF 245926–245927, UF 245935–245942, UF Genus PHYSOGALEUS Cappetta, 1980 245985, UF 245993, UF 245997–245998, UF 247260–247262, PHYSOGALEUS CONTORTUS (Gibbes, 1849) UF 247278–247281, UF 247286–247290, UF 247308–247309, Figure 5.10 UF 266771–266784, UF 266825, UF 266831, UF 266833, UF 266837, USMN 22018 and USMN 8375; lowers: UF 241801– 1848–1849 Galeocerdo contortus GIBBES, p. 193, pl. XXV, 241802, UF 242805–242809, UF 242818, UF 245845–245846, figs. 71–74. UF 245854, UF 245856, UF 245861, UF 245863, UF 245874, UF Description.—Teeth are very similar to the genus Galeocerdo 245879, UF 245883–245884, UF 245889–245890, and SMU with finely serrated, long, thick and warped crowns; pronounced 76467; indeterminate position: UF 266844, UF 266849–266850, notch, small serrations on heel of distal side; undulating margin and UF 267984. and fine serrations on mesial edge; U-shaped root with prominent Occurrence.—Lower Gatun localities 1, 2, 6, 8, 9, 15; middle protuberance on lingual face and transverse groove (Fig. 5.10). Gatun: localities 3, 10, 12; upper Gatun locality 4 (Figs. 1, 2). Physogaleus contortus differs from the genus Galeocerdo in Remarks.—Purdy et al. (2001) suggested that H. serra seems to having very prominent and bulging root with the deep notch, and increase in size through its evolutionary history. The large size of a much more erect crown in lateral view (Leder, 2005). H. serra teeth suggests that this species reached total lengths Physogaleus contortus teeth from the Gatun Formation range much greater than the living Hemipristis elongatus, perhaps up to from CH¼10.0 to 11.1 mm and CW¼12 to 15.5 mm. TL¼6 m (Kent, 1994). Adult teeth of H. serra teeth from Pungo Material.—Two teeth; indeterminate position: UF 237908 and River Formation range from CH¼14.1 to 29.1 mm and CW¼12.3 UF 245984. to 35.5 mm (Purdy et al., 2001). In contrast, teeth from the Gatun Occurrence.—Lower Gatun locality 1 (Figs. 1, 2). Formation are smaller than from the older Pungo River Remarks.—Teeth of P. contortus (referred in Gillette, 1984 and Formation, suggesting that the interpretation of increasing body Purdy et al., 2001 as Galeocerdo contortus) from the Pungo River size through time is not generally applicable for this species. Formation range from CH¼12.0 to 19.0 mm. Physogaleus Hemipristis serra is particularly abundant in neritic deposits contortus typically occurs with Galeocerdo cuvier in Neogene containing warm-water faunas and scarce in deposits with cold- localities along the east coast of the United States. Counts of adapted species (Cappetta, 1987). It is common in other Miocene specimens collected in Lee Creek Mine indicate that it is twice as and Pliocene strata in Atlantic and Pacific basins of the common as Galeocerdo (Purdy et al., 2001). In contrast, only two Neotropics (Cappetta, 1987; Iturralde-Vinent et al., 1996; Laurito, specimens have been identified relative to the more common G. 1999; Purdy et al., 2001; MacPhee et al., 2003; Aguilera and cuvier in the Gatun Formation. Although uncommon in the Rodrigues de Aguilera, 2001, 2004; Portell et al., 2008). The Neotropics, it has been reported in Cuba (Iturralde-Vinent et al., extant H. elongatus is a tropical coastal shark that inhabits in- 1996) and the genus Physogaleus is noted from Costa Rica 762 JOURNAL OF PALEONTOLOGY, V. 87, NO. 5, 2013

(Laurito, 1999). This species exhibits a cosmopolitan distribution concave, with convex apex (Fig. 5.13). Lower teeth have erect during the Miocene (Cappetta, 1987). crowns slightly broader in the apex in lingual view, and straight or moderately arched root lobes. Carcharhinus obscurus differs Genus CARCHARHINUS Blainville, 1816 from other species of Carcharhinus by having coarser serrations CARCHARHINUS FALCIFORMIS (Bibron, 1841 at the base of the crown. Carcharhinus obscurus from the Gatun in Muller and Henle 1839–1841) Formation measure from CH¼7.7 to 10.1 mm and CW¼11.2 to Figure 5.11 16.28 mm. Description.—Teeth triangular with narrow cusps; mesial edge Material.—Six isolated teeth; uppers: UF 237915, UF 237917– straight with a gap lacking of serrations at mid point (square in 237918, and UF 241818; lowers: UF 237916 and UF 242839. Fig. 5.11), coarser serrations at the base, finer serrations at the Occurrence.—Lower Gatun locality 1 (Figs. 1, 2). apex; root with a transverse groove. They can have distal edges Remarks.—Teeth of C. obscurus from Yorktown Formation with angular notch perpendicular to the base. Carcharhinus measure from CH¼17.0 to 22.0 mm and CW¼18.0 to 25.0 mm. In falciformis differs from other species of Carcharhinus by having extant individuals, sharks with corresponding tooth sizes have an a gap lacking of serrations at the midpoint of the mesial cutting estimated TL¼~3 m (Purdy et al., 2001), suggesting that C. edge. In the Gatun Formation, teeth range in size from CH¼5.1 to obscurus from the Gatun Formation was smaller. In the 7.2 mm and CW¼4.9 to 6.4 mm. Neotropics, C. obscurus has been reported in Cuba and the Material.—Three isolated upper teeth: UF 241817, UF 270844, Grenadines (Iturralde-Vinent et al., 1996; MacPhee et al., 2003; and UF 271113. Portell et al., 2008). Recent C. obscurus have a cosmopolitan Occurrence.—Lower Gatun localities 1, 7 (Figs. 1, 2). distribution. They are common in coastal and pelagic, inshore and Remarks.—Purdy et al. (2001) reported this species from the offshore, warm-temperate and tropical, and continental and middle Miocene Pungo River Formation. Their single tooth oceanic waters from intertidal to 400 m depth (Compagno, 1984). measured CH¼14.2 mm and CW¼15.0 mm, which is twice as CARCHARHINUS PEREZI (Poey, 1876) large as the largest Gatun specimen. Teeth in extant individuals Figure 5.14 vary in morphology, with some individuals not exhibiting the mid point gap discussed above (Fig. 5.11) (Purdy et al., 2001). In the Description.—High teeth with narrow crown; distal edge Neotropics, C. falciformis has been reported in the Miocene of inclined, well-developed or rounded distal angular notch; mesial Costa Rica (Laurito, 1999). The extant C. falciformis is a large edge straight or slightly convex, medium to coarse serrations (Fig. epipelagic shark with a circumtropical distribution. It inhabits 5.14). Lower teeth with straight crowns, finely serrated cutting near shore, warm-shallow waters, from 18 to 500 m depth edges and nearly straight root edges; however, in some cases, (Compagno, 1984; Purdy et al., 2001). roots can vary mesially and distally to some extent. Some lateral teeth are slightly straight, making them difficult to differentiate CARCHARHINUS LEUCAS (Valenciennes, 1839 from lower teeth. Carcharhinus perezi differs from other in Muller and Henle 1839–1841) Carcharhinus species by having a coarsely serrated crown, an Figure 5.12 inclined distal edge, and a straight mesial edge. Carcharhinus Description.—Teeth triangular; crowns finely serrated, serra- perezi from the Gatun Formation range from CH¼5.8 to 10.8 mm tions become progressively coarser near the base of crown, mesial and CW¼10.6 to 16.9 mm. edge straight or slightly convex with a shallow or absent notch, Material.—Twenty four (24) isolated teeth; uppers: UF distal edge more concave with a shallow notch; U-shaped root. 241819–241820, UF 241822, UF 242840–242842, UF 242844– Some teeth have a well-developed transverse groove (Fig. 5.12). 242846, UF 242848–242853, UF 242855–242857; lowers: UF Lower teeth have thick crowns and cutting edges are finely 242845–242846; indeterminate position: UF 241821, UF 241843, serrated (Purdy et al., 2001). Carcharhinus leucas differs from UF 241847, and UF 241854. other Carcharhinus species in having a more equilateral crown Occurrence.—Lower Gatun locality 1; middle Gatun locality 3 shape. Carcharhinus leucas from the Gatun Formation measure (Figs. 1, 2). from CH¼7.5 to 10.7 mm and CW¼13.6 to 14.2 mm. Remarks.—Teeth of C. perezi from Pungo River Formation Material.—Fifteen (15) isolated teeth; uppers: UF 237979, UF measure from CH¼13.0 to 18.0 mm and CW¼13.0 to 22.0 mm, 237981, UF 237983, UF 237985,–237989, UF 241829–241830, which corresponds to sharks of TL¼2 m (Purdy et al., 2001). This and UF 242838; lowers: UF 237980, UF 237982, and UF 237984; suggests that C. perezi from the Gatun Formation was represented indeterminate position: UF 247296. by smaller individuals. In the Neotropics, C. perezi has been Occurrence.—Lower Gatun locality 1; middle Gatun locality 3 reported in the Grenadines and Brazil (Reis, 2005; Portell et al., (Figs. 1, 2). 2008). Extant sharks of this species inhabit tropical waters of the Remarks.—Teeth of C. leucas from Pungo River Formation Caribbean Sea, and inshore of continental and insular shelves range from CH¼17.0 to 20.0 mm and CW¼16.0 to 22.0 mm. down to at least 30 m depth (Compagno, 1984). These probably belong to individuals that had a TL¼2to3m (Purdy et al., 2001), and are larger than individuals from the CARCHARHINUS PLUMBEUS (Nardo, 1827) Gatun Formation. In the Neotropics, C. leucas has been reported Figure 5.15 in Cuba and the Grenadines (Iturralde-Vinent et al., 1996; Description.—Narrow crown; moderate serrations on edges, MacPhee et al., 2003; Portell et al., 2008). Extant individuals are distal edge inclined, mesial edge straight or slightly convex; thick large circumtropical epipelagic sharks, and are widespread in root (Fig. 5.15). Carcharhinus plumbeus may present a well- warm oceans, rivers, and coastal lakes, in shallow (,30 m) depths developed transverse groove or a central foramen and a U- or V- (Compagno, 1984, 1988). shaped root. Carcharhinus plumbeus teeth are very similar to those from Carcharhinus obscurus, but C. plumbeus have CARCHARHINUS OBSCURUS (Lesueur, 1818) Figure 5.13 narrower and more elongated crowns with an apical convexity in cutting edges (Purdy et al., 2001). Carcharhinus plumbeus Description.—Teeth have a broad crown; lingual surface flat, differs from Carcharhinus perezi in having finer serrations and labial surface convex; thick root with a transverse groove. Upper apical convexity. Specimens from the Gatun Formation measure teeth have basal crown serrations coarser than the apex, nearly from CH¼6.8 to 10.6 mm and CW¼10.3 to 6.1 mm. vertical distal cutting edge, mesial edge inclined distally, Material.—Five isolated teeth; uppers: UF 242858–242862. PIMIENTO ET AL.—LATE MIOCENE SHARKS AND RAYS FROM PANAMA 763

Occurrence.—Lower Gatun locality 1 (Figs 1, 2). Genus NEGAPRION Whitley, 1940 Remarks.—Teeth of C. plumbeus teeth from Pungo River NEGAPRION BREVIROSTRIS (Poey, 1868) Formation measure from CH¼14.0 to 19.0 mm. Teeth of this size Figure 5.18 correspond to sharks of TL¼2 m (Purdy et al., 2001), indicating Description.—Teeth of N. brevirostris have a T-shape; narrow that C. plumbeus from the Gatun Formation was represented by unserrated crown perpendicular to the root; and flat roots with smaller individuals. In the Neotropics, they have been reported transverse groove. They can also have a slightly curved, inclined in the Miocene of Venezuela and Cuba (Iturralde-Vinent et al., crown; lingual face flat and labial face slightly convex; elongated 1996; Aguilera and Rodrigues de Aguilera, 2001; MacPhee et root lobes, and strongly obtuse basal root angle. Moderate al., 2003). Extant C. plumbeus are cosmopolitan, coastal-pelagic ontogenetic heterodonty is observed in this species with smaller sharks of warm temperate and tropical waters, found in insular specimens lacking serrations on heels (Fig. 5.18) while larger and continental shelves and deep waters adjacent to them. They individuals exhibit them (Compagno, 1984; Purdy et al., 2001). range from intertidal waters to 280 m in depth (Compagno, Lower teeth of N. brevirostris differ from the genus Carcharhinus 1984). by not having serrations on the crown. Negaprion brevirostris CARCHARHINUS sp. from the Gatun Formation measurements range from CH¼3.7 to Figure 5.16, 5.17 13.7 mm and CW¼4.3 to 16.3 mm. Material.—Ninety four (94) isolated teeth; indeterminate Description.—Upper teeth of the Carcharhinus sp. from the position: UF 237961–237978, UF 241813–241816, UF 241833– Gatun Formation have triangular shape; straight crown in anterior 241834, UF 242863–242867, UF 245847, UF 245864, UF teeth and curved in laterals, flat labial face, slightly convex 245875, UF 245881–245882, UF 245893, UF 245913–245914, lingual face, serrated cutting edges, and cusps separated or not UF 245945–245951, UF 245983, UF 245986, UF 245999, UF from heels. Roots can present a clear transverse groove in small 247263–247264, UF 247267, UF 247288, UF 266785–266787, forms (Fig. 5.16). Lower teeth have narrower cusps, crown well UF 266824, UF 266828, UF 266836, UF 266839, UF 266845, UF separated from heel, cutting edges serrated, with a transverse 266847, SMU 76455, SMU 76458–76459, SMU 76465, SMU groove (Fig. 5.17). Lower teeth of Carcharhinus sp. differ from 76469, and SMU 76474–76475. Negaprion brevirostris by having serrated cutting edges and from Occurrence—Lower Gatun localities 1, 2, 5, 6, 8, 9, 15; middle the genus Sphyrna by having a thinner root and the lack of an Gatun locality 10; upper Gatun locality 4 (Figs. 1, 2). expanded lingual heel. This genus is abundant in the Gatun Remarks.—In the Miocene, this species is referred to as Formation with teeth ranging greatly in size, from CH¼1.9 to 12.9 Negaprion eurybathrodon (e.g., Cappetta, 1987; Purdy et al., mm and CW¼4.1 to 17.6 mm. 2001). However, since the tooth morphology of the Gatun Material.—Three hundred seventeen (317) isolated teeth; specimens is not different from the modern lemon shark, we uppers: UF 237990–237999, UF 238001–238018, UF 238021– assign them to N. brevirostris. Cappetta (1987) established the 238025, UF 238032, UF 241823–241825, UF 241827, UF maximum CH of for Negaprion to be 20 mm. Purdy et al. (2001) 242825–242826, UF 242829, UF 242832, UF 242871; lowers: reported teeth in the Pungo River Formation, measuring from UF 237992, UF 237995, UF 237998–UF 237999, UF 241828, UF CH¼14 to 21 mm and stated that in extant N. brevirostris teeth of 241831–241832, UF 242823–242824, UF 242827–242828, UF this size are found in sharks of TL¼2.1 to 3 m, which is the size 242830–242831, UF 242833, UF 242836, UF 242871; lateral: range for mature adults according to Compagno (1984). This SMU 76475; indeterminate position: UF 238019, UF 241826, UF suggests that most of the specimens assigned to N. brevirostris in 242834–242835, UF 242837, UF 245848–245851, UF 245853, the Gatun Formation are juveniles. The lack of serrations on the UF 245855, UF 245857–245860, UF 245866–245873, UF heels of most of the specimens corroborates this hypothesis. In the 245876–245878, UF 245880, UF 245887–245888, UF 245894– Neotropics, N. brevirostris (¼N. eurybathrodon)hasbeen 245907, UF 245910–245912, UF 245917–245921, UF 245928– reported in the Miocene of Venezuela, Cuba and Ecuador 245934, UF 245959–245981, UF 245987–245992, UF 245994, (Iturralde-Vinent et al., 1996; (Aguilera and Rodrigues de UF 246000, UF 247258, UF 247268–247277, UF 247282– Aguilera, 2001; MacPhee et al., 2003; Longbottom, 1979). Extant 247285, UF 247291, UF 247298–247299, UF 247307, UF N. brevirostris inhabits tropical and temperate estuarine and 247310–247314, UF 266791–266823, UF 266826–266827, UF intertidal through offshore (0–92 m) waters of the Atlantic and the 266829–266830, UF 266832, UF 266834, UF 266835, UF Pacific Ocean (Compagno, 1984; Kent, 1994). 266838, UF 266840–266843, UF 266848, UF 266851–266852, Genus RHIZOPRIONODON Whitley, 1929 UF 267979, UF 267982–267983, SMU 76457–76459, SMU RHIZOPRIONODON sp. 76463, SMU 76465, SMU 76469, SMU 76472–76475, and Figure 5.19 USMN 58461. Occurrence.—Lower Gatun localities 1, 2, 5–9, 11, 14, 15; Description.—Rhizoprionodon sp. teeth have a slightly re- middle Gatun localities 10, 12; upper Gatun locality 4 (Figs. 1, 2). curved crown; cutting edges finely serrated or smooth, mesial Remarks.—Much taxonomic confusion exists within this edge curved, distal heel with a notable notch; roots straight, low, genus (Purdy et al., 2001). The identification of individual with a deep and transverse groove (Fig. 5.19). Rhizoprionodon Carcharhinus species based solely on isolated teeth is extremely differs from Sphyrna by having a notch in distal heel and shorter difficult given the degree of similarity in tooth morphology. crown. Rhizoprionodon sp. from the Gatun Formation measures This problem is particularly acute in lower teeth, which are very from CH¼2.5 and 3.3 mm and CW¼3.9 and 5.6 mm. similar among most species (Kent, 1994). Factors influencing Material.—Six isolated teeth; indeterminate position: UF variation in tooth shape within the genus Carcharhinus include: 267978, UF 267980–267981, SMU 76461, SMU 76464 and variation among species, variation within a species, differences SMU 76475. within individuals of a species (Naylor and Marcus, 1994) and Occurrence.—Lower Gatun localities 1, 15 (Figs. 1, 2). within a tooth row. Upper teeth of the genus Carcharhinus have Remarks.—Cappetta (1987) stated that teeth from Rhizoprio- been documented up to CH¼20 mm (Cappetta, 1987). Sharks of nodon are less than CH¼4 mm. However, teeth from Pungo River this genus are wide-ranging in tropical waters, with some Formation measured from CH¼3.2 to 5.2 mm and CW¼4.3 to 5.7 ranging in warm temperate waters. Most species are coastal and mm (Purdy et al., 2001). Total length in extant adult individuals a few are oceanic. Some species are very common in coral reefs averages in about TL¼1 m (Compagno, 1984). Extant specimens (Compagno, 1988). of this genus are mainly distributed in the Atlantic Ocean, 764 JOURNAL OF PALEONTOLOGY, V. 87, NO. 5, 2013 including Rhizoprionodon lalandii, Rhizoprionodon porosus, and studied here. This suggests that individuals from the Gatun Rhizoprionodon terraenovae (Compagno, 1984). Extant R. Formation were small. Extant species inhabit all temperate and lalandii occurs normally in lagoons and estuaries. R. porosus is tropical seas, and are found mostly in coastal waters (Compagno, found usually close inshore. Rhizoprionodon terraenovae inhabits 1988). coastal warm, temperate, and tropical waters, usually less than 10 m in depth (Compagno, 1984; Compagno et al. 2005). Subdivision BATOIDEA Compagno, 1973 Order RAJIFORMES Berg, 1940 Family SPHYRNIDAE Gill, 1872 Family RHYNCHOBATIDAE Garman, 1913 Genus SPHYRNA Rafinesque, 1810 Genus RHYNCHOBATUS Mu¨ller and Henle, 1837 SPHYRNA LEWINI (Griffith and Smith, 1834) RHYNCHOBATUS LUEBBERTI (Ehrenbaum, 1914) Figure 5.20 Figure 6.1, 6.2 Description.—Shyrna lewini have a stout to slender crown, Description.—In apical view, convex-shaped crown; angular cutting edges either smooth or weakly serrated, thick and bulky mesial and distal sides; occlusal surface with fine granular root and a deep transverse groove. The S. lewini specimens from ornamentation above the smooth labial side; lingual edge smooth; the Gatun Formation have a well-developed notch on the distal shallow mesial and distal depressions with an irregularly-shaped edges and the crowns are inclined (Fig. 5.20). Shyrna lewini is and well-developed uvula (Fig. 6.1). In basal view, root relatively differentiated from other Sphyrna species by having smooth to high and situated on the lingual half of the base of the crown; weakly serrated cutting edges. The teeth measurements range labial part angled; lingual part with a well-developed trilobation. from CH¼2.7 and 5.4 mm and CW¼5.2 and 11.0 mm. A large foramen is present in the median groove, as well as a Material.—Four isolated teeth; uppers: SMU 76454, SMU smaller mesial and distal foramen (Fig. 6.2). This specimen 76458 and SMU 76462; lower: SMU 76449. measures 2.6 mm long and 3.2 mm wide. Occurrence.—Lower Gatun locality 15 (Figs. 1, 2). Material.—One isolated male tooth; lower lateral: UF 247214. Remarks.—This species is among the most abundant of the Occurrence.—Lower Gatun locality 1 (Figs. 1, 2). hammerhead sharks. In the Neotropics, it has been reported from Remarks.—Rhynchobatus luebberti is a large batoid from the the Miocene of Cuba (Iturralde-Vinent et al., 1996; MacPhee et eastern Atlantic, reaching up to TL¼3 m. It is a benthic species al., 2003). Extant individuals have a cosmopolitan distribution living on soft mud or sand in the intertidal zone, up to 70 m depth; and occur in coastal warm-temperate and tropical seas, ranging however, it is not generally found in waters deeper than 35 m from the surface to at least 275 m in depth (Compagno, 1984). (Compagno and Marshall, 2006). The dentition of R. luebberti has SPHYRNA MOKARRAN (Ru¨ppell, 1837) been described and illustrated by Herman et al. (1997), where it is Figure 5.21 possible to appreciate the variable ornamentation. Description.—Shyrna mokarran teeth exhibit triangular shape, RHYNCHOBATUS sp. increasingly oblique crown, serrated cutting edges, thick and Figure 6.3, 6.4 bulky root, and deep transverse groove (Fig. 5.21). Shyrna Description.—In apical view, crown with arched transverse mokarran differs from other species of Sphyrna by having one keel from mesial to distal sides dividing the labial and lingual heel more pronounced than the other. Teeth from the Gatun parts. Labial part with a depression followed by second shorter Formation measure from CH¼7.6 to 9.4 mm and CW¼9.6 to 16.4 mm. keel, a parallel irregular folding, and a convex smooth surface Material.—Four isolated teeth; uppers: UF 237909–UF completing the labial edge of the crown. Lingual part with smooth 237912. surface, shallow mesial and distal depressions, and well- Occurrence.—Lower Gatun locality 1 (Figs. 1, 2). developed uvula (Fig. 6.3). In basal view, root relatively high, Remarks.—This species is not well documented in the fossil situated on the lingual half of the base of the crown; labial part record. In the circum-Caribbean region, it has only previously angled; the lingual part with well-developed trilobation. Foramen been reported from the Miocene of Cuba, although there is no present in medial groove (Fig. 6.4). This specimen measures 0.9 description of the specimens (MacPhee et al., 2003). Modern S. mm long and 0.9 mm wide. mokarran has a circumtropical distribution and inhabits coastal- Material.—One isolated tooth; lateral: UF 271961. pelagic and semi-oceanic, tropical habitats, from 1–80 m Occurrence.—Lower Gatun locality 1 (Fig. 1, 2). (Compagno et al., 2005). Remarks.—Symphysial teeth have been reported as quite wide, up to about CW¼5 mm (Cappetta, 1987), in contrast to the SPHYRNA sp. specimen collected from the Gatun Formation. In the Neotropics, Figure 5.22 it otherwise has been reported in the Miocene of Venezuela (Aguilera and Rodrigues de Aguilera, 2001). This genus consists Description.—Serrated and labio-lingually flattened crown; of six extant species found in the tropical and subtropical Indo- apex inclined or slanted distally; acute notch; thick, bulky root; Pacific, with a single species in the eastern Atlantic: R. luebberti transverse groove present (Fig. 5.22). The mesial cutting edge of (Compagno and Marshall, 2006). Sphyrna sp. is generally convex and slightly sigmoid; cusps are slender. Sphyrna sp. teeth from the Gatun Formation have thicker Order MYLIOBATIFORMES Compagno, 1973 crowns and weaker serrations than Sphyrna lewini.The Family UROTRYGONIDAE McEachran et al., 1996 measurements for this taxa range from CH¼3.1 to 8.9 mm and Genus UROBATIS Garman, 1913 CW¼7.4 to 10.6 mm. UROBATIS sp. Material.—Thirty four (34) isolated teeth; upper: UF 242868; Figures 6.5, 6.6, 7.1, 7.2 lower: UF 238020; indeterminate position: UF 242869–242870, UF 245862, UF 245865, UF 245922–245924, UF 245952– Description.—In apical view, crown with a trapezoid contour; 245958, UF 247265–247266, UF 247293, UF 266788–266790, lingual half of the occlusal area with a transverse depression SMU 76459, SMU 76463, SMU 76465, and SMU 76475. edged by an irregular transverse crest, labial part slightly convex Occurrence.—Lower Gatun localities 1, 15 (Figs. 1, 2). with a coarse reticulated ornamentation with deep depressions Remarks.—Cappetta (1987) established the maximum tooth (Fig. 6.5). Lingual side smooth, V-shaped, and with transverse size for this genus to be CH¼20 mm, much larger than the teeth keel with irregular ornamentation that runs from the mesial to the PIMIENTO ET AL.—LATE MIOCENE SHARKS AND RAYS FROM PANAMA 765

FIGURE 6—Batoid micro-teeth from the late Miocene Gatun Formation, Panama. 1, 2, Rhynchobatus luebberti (Ehrenbaum, 1914), UF 247214, male tooth, lower lateral in apical and basal view, respectively; 3, 4 Rhynchobatus sp., UF 271961, lateral tooth in apical and basal view, respectively; 5, 6, Urobatis sp. UF 267987, female tooth, lateral in apical and basal view, respectively; 7–10 Taeniura aff. grabata (Geoffroy Saint-Hilaire, 1817): 7, 8, UF 267992, female tooth, lateral in apical and basal view, respectively; 9, 10, UF 267994, male tooth, anterior in apical-labial and basal view, respectively; 11–14 Mobula munkiana (Notarbartolo Di Sciara, 1987): 11, 12, UF 267993, female tooth in apical and basal view, respectively; 13, 14, UF 267989, male tooth in apical and basal view, respectively; 15, 16, Mobula thurstoni (Lloyd, 1908), UF 267995, female tooth, indeterminate position in apical and basal view, respectively; 17–20, Mobula hypostoma (Bancroft, 1831): 17, 18, UF 267985, female tooth in labial-apical and basal view, respectively; 19, 20, UF 267988, male tooth in apical and basal view, respectively. distal sides of the crown; labial side with a decreasing contour Occurrence.—Lower Gatun localities 1, 5 (Figs. 1, 2). that fits on the next tooth. The crown-root junction lies in a Remarks.—Urotrygonidae (American round rays) were for- shallow depression. In basal view, root asymmetric with two well merly included in the Urolophidae (Indo-Pacific round rays; see differentiated lobes, the right lobe is much more slender than the McEachran et al., 1996). This family of round rays inhabits left lobe, indicating a lateral position; it is oblique toward the rear estuaries, lagoons, and neritic waters (usually in less than 15 m) of the tooth, and slightly diverges at the root base; root base with of tropical and warm temperate seas (Allen and Robertson, 1994; a well-developed deep median groove that encloses a central Ebert, 2003). The tooth morphology of the Gatun specimen is foramen (Fig. 6.6). Lingual and labial foramina and root coating very similar to the extant ray Urobatis halleri. Fossil specimens are absent. The flat crown is a diagnostic feature of a female. This are described in Cappetta (1987), with a maximum width of 2 specimen is 0.5 mm long and 0.9 mm wide. mm. Today, U. halleri is restricted to the eastern Pacific, from A partial caudal spine was also recovered. The enameloid of California to Colombia, and is the most common species of the the dorsal section has serrations (Fig. 7.1) whereas the ventral family (McEachran et al., 1996). Urobati halleri is commonly side does not (Fig. 7.2). Dorsal spine groove present, ventral part found in sand rubble or rock bottoms close to reefs, and is a convex. This specimen is 21.0 mm long. demersal species occurring in depths of no more than 91 m Material.—One isolated tooth, female, lateral: UF 267987. One (Michael, 1993; Allen and Robertson, 1994). With regards to the caudal spine: UF 247226. spine, Schwartz (2007) described the caudal spines of stingrays 766 JOURNAL OF PALEONTOLOGY, V. 87, NO. 5, 2013

Occurrence.—Lower Gatun localities 1, 5; middle Gatun locality 3 (Figs. 1, 2). Remarks.—Dental description and images have been published (Herman et al., 1998; p. 158, pls. 18, 19), but only represent female dentition. Taeniura grabata is recorded in the eastern central, the southeast Atlantic Ocean and in the western Indian Ocean. It is a demersal species occurring in marine neritic tropical or warm temperate waters from 10 to 300 m depth, on sand and rock-sand bottoms (Serena et al., 2009).

Family MYLIOBATIDAE Bonaparte, 1838 Genus AETOBATUS Blainville, 1816 AETOBATUS cf. NARINARI (Euphrasen, 1790) Figure 7.3, 7.4 Description.—Crown mesio-distally flatted, almost straight and arched outward; interlocking ornamentation almost absent, but exhibit relatively fine vertical costules on the lingual and labial surfaces; a narrow lingual ledge is present. Root shifted inwards from the crown, so that the labial side overhangs the labial root edge interlocking the teeth. Root polyaulacorhizid (i.e., vascu- larized through many small foramina concentrated in several grooves running parallel from the labial to the lingual face) with numerous evenly shaped basal grooves, each with scattered FIGURE 7—Batoid macro-teeth from the late Miocene Gatun Formation, foramina along the center of the groove (Fig. 7.3, 7.4). Lower Panama. 1, 2, Urobatis sp.: 1, UF 247226, dorsal side, 2, UF 247226, ventral teeth mesio-distally V-shaped. Upper teeth almost straight. UF side; 3, 4, Aetobatus cf. narinari (Euphrasen, 1790), UF 247202–UF 247205, upper teeth in labial and lingual view, respectively; 5, 6 Myliobatis cf. 247202–UF 247205 specimens represent a single tooth measuring californica (Gill, 1865), UF 247209–UF 247210, symphysial teeth in labial 66.0 mm long, 8.0 mm wide and 4.5 mm high. and lingual view, respectively; 7, 8 Rhinoptera cf. steindachneri (Evermann Material.—One complete tooth: UF 247202–247205; 21 and Jenkins, 1892), UF 247240, upper symphysial tooth in labial and lingual fragments of isolated teeth, uppers: UF 247201, UF 247228– view, respectively. 247229, UF 247230–247232, UF 247236, UF 247241–247246; lowers: UF 247215 and UF 247229; indeterminate position: UF 266761–266763, UF 266765, UF 266767, UF 266769, 271103– from the northwest Pacific Ocean, indicating that spine 271104, and UF 271104. morphology can be good indicators of their habitat. The Occurrence.—Lower Gatun localities 1, 5, 6, 7, 11 (Figs. 1, 2). morphology of the Gatun specimen described here corresponds Remarks.—This is a cosmopolitan species occurring in tropical to a benthic environment. continental or insular platforms within the neritic zone. They are abundant in warm to temperate-warm shallow water deposits Family DASYATIDAE Jordan, 1888 (Compagno and Last, 1999). Genus TAENIURA Mu¨ller and Henle, 1837 TAENIURA aff. GRABATA (Geoffroy Saint-Hilaire, 1817) Genus MYLIOBATIS Cuvier, 1816 Figure 6.7–6.10 MYLIOBATIS cf. CALIFORNICA (Gill, 1865) Figure 7.5, 7.6 1817 Taeniurops grabata GEOFFROY SAINT-HILAIRE, p. 218, pl. XXV, figs. 1, 2. Description.—Low crown with smooth surface. Abrasion Description.—In apical view, female teeth with a broad crown, marks on lateral side preserved; triangular contour. Interlocking granular ornamentation on lingual and labial faces; narrow lingual rounded transverse keel dividing the crown into lingual and labial ledge present. Root shifted inward from the crown, so that the part; labial margin of the crown less arched than the lingual labial crown edge overhangs the labial root edge interlocking the margin; both margins join in the mesial and distal marginal teeth. Teeth of M. californica differ from the genus Rhinoptera in angles; lingual central ridge absent; lingual surface slightly having a much smaller ledge between the crown and the root. UF convex with ornamentation consisting on coarse irregular costules 247209–UF 247210 are a pair of articulated incomplete along the transverse keel. Labial surface with a deep depression symphysial teeth measuring 33.0 mm long, 13.0 mm wide and along the transverse keel, and well-developed reticulated 8.0 mm high. The occlusal face is eroded, evidencing these are ornamentation in the labial margin (Fig. 6.7). In basal view, functional teeth (Fig. 7.5, 7.6). labial part of the crown with a broad and relatively flat rim that Material.—One articulated pair of incomplete teeth; upper: UF gradually narrows to half its width. Crown-root junction situated 247209–UF 247210 and six fragments of isolated teeth; on a deep depression in the center of the basal surface of the indeterminate position: UF 247211, UF 266760, UF 266764, crown. Root narrow, moderately high, with a slightly oval to UF 266766, UF 266768, and UF 271105. circular shape; root base with a well-developed deep median Occurrence.—Lower Gatun localities 1, 5, 6 (Figs. 1, 2). grove that encloses two or three central foramina. Lingual and Remarks.—Myliobatis californica occurs in the eastern Pacific, labial foramina, and root coating are absent (Fig. 6.8). UF 267994 from tropical to subtropical waters in the inner continental or shows male diagnostic character consisting of a pointed crown insular platform of the neritic zone. They are frequently found in with irregular reticulated ornamentation (Fig. 6.9, 6.10). Mea- benthopelagic and demersal environments, and in both saltwater surements of specimens range from 1.5 to 3.1 mm long and 1.9 to and euryhaline habitats from Oregon to the Pacific coast of 3.0 mm wide. Mexico. In the Pacific, M. californica and Myliobatis peruvianus Material.—Five isolated teeth; female, anteriors: UF 267991 are very similar in morphology, but the latter is smaller, and and UF 267998; female laterals: UF 267992 and UF 267997; restricted to Ecuador, Peru and Chile. The geographic ranges of male, anterior: UF 267994. both species overlap in the Galapagos Islands (Michael, 1993). PIMIENTO ET AL.—LATE MIOCENE SHARKS AND RAYS FROM PANAMA 767

Genus RHINOPTERA Kuhl in Cuvier, 1829 MOBULA THURSTONI (Lloyd, 1908) RHINOPTERA cf. STEINDACHNERI (Evermann and Jenkins, 1891) Figure 6.15, 6.16 Figure 7.7, 7.8 Description.—Specimens from the Gatun have a female tooth Description.—Upper teeth straight; crown enlarged and flat morphology. UF 267995 has an almost oval shape at the base of with a hexagonal contour in the occlusal face. Lingual face with a the crown (Fig. 6.15). In basal view, apical edge of the crown central depression between the crown and the root; labial face with four triangular cusps; the enameloid on the labial face shows with a transverse ledge, which interlocks with the next tooth in irregular folding. Root oriented mesio–distally, much smaller the dental plate. Root shifted inwards from the crown on the than the crown, and with two wide lobes (Fig. 6.16). This tooth is lingual and the labial faces; crown overhangs the root edge 0.6 mm long and 1.1 mm wide. UF 267996 displays a crown interlocking the teeth. Root polyaulacorhizid with numerous lobes mesio-distally elongated with five irregular points and enameloid and grooves, not extending beyond margin of crown. Upper on the labial crown with irregular folding. This tooth measures symphysial teeth larger than laterals (Fig. 7.7, 7.8). In lower teeth, 0.6 mm long and 2.0 mm wide. the lateral longitude is short, and the lingual and labial faces Material.—Two isolated teeth, female, lowers: UF 267995– distance is wider than in upper teeth. Teeth of Rhinoptera cf. 267996. steindachneri from the Gatun Formation are elongated and more Occurrence.—Lower Gatun locality 1 (Figs. 1, 2). symmetrical and slender than Myliobatis. Complete specimens Remarks.—This species has a circumtropical distribution. It measure from 4.0 to 5.0 mm long, 3.0 to 26.0 mm wide, and 3.0 to occurs in the open ocean, neritic waters, sub-tidal aquatic beds, 5.0 mm high. and coral reefs; in depths of between intertidal waters and 100 m Material.—Thirty three (33) teeth; 10 complete and 23 (Clark et al., 2006). incomplete isolated teeth; uppers: UF 247216, UF 247219– 247220, UF 247222, UF 247224–247225, UF 247235, UF MOBULA HYPOSTOMA (Bancroft, 1831) 247237–247238, UF 247240, UF 247244–247245, and UF Figure 6.17–6.20 247247; lowers: UF 247206–UF 247208, UF 247212–UF 247213, UF 247217–247218, UF 247221, UF 247223, UF Description.—Teeth of M. hypostoma from the Gatun Forma- 247227, UF 247233–247234, and UF 247239; indeterminate tion present both female and male morphology. Female position 266758–UF 266759, UF 266770, UF 271106–271107, morphology consists on an elongated crown with a 458 inclination UF 271110, and UF 271112. in direction to the lingual side, three isolated cusps, two laterals, Occurrence—Lower Gatun localities 1, 2, 5, 7 (Figs. 1, 2). one on each side (mesial and distal); smooth enameloid (Fig. Remarks.—Rhinoptera steindachneri is restricted to the eastern 6.17); and root much smaller than the crown with two lobes (Fig. Pacific where it is a benthopelagic species occurring exclusively 6.18). Male morphology consists on a tripod crown; one wide in the neritic zone of the inner part of continental and insular central main cusp, slender lateral cusps (Fig. 6.19); and root with platforms (Smith and Bizzarro, 2006). two lobes separated by a nutritive groove (Fig. 6.20). UF 267986 is an incomplete tooth consisting on a main wide cusp, and two Genus MOBULA Rafinesque, 1810 other cusps; root with two wide lobes separated by a wide MOBULA MUNKIANA (Notarbartolo Di Sciara, 1987) nutritive groove. Specimens from the Gatun Formation range in Figure 6.11–6.14 size from 0.5 to 0.6 mm long and 0.9 to 1.1 mm wide. Description.—Teeth of M. munkiana from the Gatun Forma- Material.—Three isolated teeth, female, lowers: UF 267985– tion presents both female and male morphology. Female teeth 267986; male, lower: UF 267988. display an almost hexagonal crown and smooth enameloid; Occurrence.—Lower Gatun locality 5 (Figs. 1, 2). mesial edge with a wide triangular cusp followed by a smaller Remarks.—The extant M. hypostoma is a pelagic-neritic one and then a transversal edge crown; root short with respect to species occurring in coastal tropical and subtropical waters of the crown (Fig. 6.11–6.12). Male teeth have a wide triangular the western Atlantic (Bizzarro et al., 2009). crown and smooth enameloid with two wide triangular points, DIVERSITY AND TAXONOMIC COMPOSITION and two smaller lateral denticles, one on each side (mesial and distal). Root slender, positioned at the very basal lingual edge of Taking advantage of the ongoing excavations of different the crown, with two wide lobes elongated mesio-distally, and outcrops from the late Miocene Gatun Formation of Panama, separated by a wide groove with large foramina (Fig. 6.13, here we review and describe all known material. Accordingly, 6.14). The labial basal edge overhangs the empty space of the we identified a total of 26 taxa belonging to five orders, nine absence of the root for the interlocking system between the families, and 16 genera (Fig. 3) in 15 different localities (Figs. teeth. UF 267990 shows a wide and triangular main central cusp 1, 2). Of this assemblage, only four species are now extinct (see with two wide triangles directed to the lingual side, and two low † in Fig. 3); the remaining are extant and hence represent long- lateral cusps; the mesial cusp is wider, whereas the distal cusp is lived taxa. Most of the chondrichthyan species represented in slender. In the labial side, the basal edge of the crown shows the Gatun Formation possess a fossil record at least from the wide irregular folding and a root elongated mesial-distally. The Miocene, though some also occur in the Eocene and Oligocene. root is positioned at the very lingual edge. UF 267999 displays a It has been proposed that the rate of evolutionary change in male tooth morphology, smooth enameloid; pointed crown with sharks is much slower compared with other organisms (Martin lateral prolongation directed to the lingual side of the mouth; et al., 1992). Based on tooth morphology of fossil and Recent basal crown almost oval in basal view. The specimens of the specimens, we can assert that the chondrichthyan fauna of the Gatun Formation measure from 0.5–1.2 mm long and 0.9–2.3 mm wide. late Miocene Gatun Formation has not changed significantly for Material.—Four isolated teeth; female lowers: UF 267989– several million years, and has been remarkably resilient to 267990, female upper: UF 267993 male lower: UF 267999. numerous environmental changes, for example, and relevant to Occurrence.—Lower Gatun localities 1, 2, 5 (Figs. 1, 2). this study, to the major geographic and oceanographic changes Remarks.—Teeth of the genus Mobula are generally small. associated with the closure of the CAS. Mobula munkiana occurs in the eastern tropical Pacific. It is a Gillette (1984) described 14 chondrichthyans from one single pelagic and demersal species, usually found in coastal shallow locality in the Gatun Formation. As stated earlier, we were water habitats of around 15 m depth (Bizzarro et al., 2006). unable to resample that site due to loss of the relevant outcrops. 768 JOURNAL OF PALEONTOLOGY, V. 87, NO. 5, 2013

However, the material borrowed from SMU allowed us to make on its morphology, we interpret that the specimens Gillette some comparisons. While our identifications are fairly consis- (1984) referred to Isistius sp. belong to the sharpnose shark, tent with those of Gillette (1984), there are a number of key Rhizoprionodon. In addition, five new specimens of Rhizoprio- differences and additions that expand our knowledge of nodon were collected in this study. While lower Isistius teeth are chondrichthyan fauna of the Gatun Formation (Fig. 3). present in the Miocene of Venezuela (Aguilera and Rodrigues The following species reported by Gillette (1984) are in de Aguilera, 2001) and in the Pliocene of North Carolina (Purdy agreement with our identifications: Ginglymostoma delfortriei, et al., 2001), no upper teeth have been described from the fossil Carcharocles megalodon, Hemipristis serra, Carcharhinus sp., record, which may be related to their weaker mineralization and Physogaleus contortus. While no other teeth of G. (Cappetta, 1987). The reidentification of these teeth to delfortriei were collected during the present study, the SMU Rhizoprionodon is also more consistent with the habitat specimens confirm the presence of this species in the Gatun reconstruction of the Gatun Formation. This species inhabits Formation. The fact that no further material was recovered warm coastal waters, whereas Isistius tends to be an oceanic, during this study is not surprising given that these teeth are epipelagic to bathypelagic shark (Compagno, 1984; Purdy et al., small and not typically found during typical surface collecting. 2001). Therefore, on the basis of paleoecological evidence of However, we did not find this species during our screenwashing other sharks and associated invertebrate taxa, its presence in the efforts either. Additional C. megalodon specimens were GatunFormationwouldbehighlyirregular.Anadditional21 collected during this study. The cosmopolitan nature of the taxa have been identified from the Gatun Formation of Panama species is documented by the presence of C. megalodon teeth (see þ in Fig. 3). Gillette (1984) reported the presence of worldwide (Cappetta, 1987; Purdy, 1996; Purdy et al., 2001). Aetobatus sp. and Myliobatis sp.; however these specimens were The most common teeth found in the Gatun Formation are missing from the SMU collection, and we were therefore unable undifferentiated Carcharhinus, representing about 40% of the to confirm the identification. Nevertheless, it is possible that our total sampled fauna (Fig. 3). This genus varies greatly in size records of Aetobatus aff. narinari and Myliobatis cf. californica and morphology (Naylor and Marcus, 1994), making it difficult are the same species that Gillette had reported. to identify to the species level. The second most common taxon is H. serra,representing15% of the total sampled fauna (Fig. 3). PALEOBIOGEOGRAPHY The presence of Physogaleus (Galeocerdo) contortus reported The modern-day pattern of separate Pacific and Atlantic by Gillette (1984) was confirmed by the collection of two faunas was derived from a large, once contiguous Eocene– specimens in this study. It should be noted however, that the Miocene province (Woodring, 1966, 1974) that encompassed specimens described in Gillette’s work were not present in the the tropical Eastern Pacific and the Caribbean. Gillette (1984), SMU collection for comparison. in comparing the fauna of the Gatun Formation to that of There are a number of key differences and additions to the Ecuador, Florida, and North Carolina, recognized many of the chondrichthyan fauna of the Gatun Formation resulting from features of Woodring’s (1966, 1974) proposed Tertiary Carib- this study. Gillette (1984) identified one white shark tooth bean faunal province and extended it further to the north, to (Carcharodon carcharias), describing it as being highly worn, include the southeast Atlantic coast of North America. Studies missing its edges and serrations. However, this specimen was of benthic foraminifera (Collins et al., 1996) from the Gatun also missing from the SMU collection and we were therefore Formation show a strong Caribbean affinity. This is explained unable to confirm the identification. Regardless, the presence of by an effective biogeographic restriction between Pacific and a white shark tooth in the late Miocene is unlikely because Caribbean surface waters (Collins et al., 1996; Kirby et al., modern C. carcharias does not become common in the fossil 2008) by the time the Gatun sediments deposited. Concurrently, record until the Pliocene (Ehret et al., 2009, 2012). Without being able to study the specimen, it is difficult to speculate most of the chondrichthyan taxa from the Gatun Formation have which species was represented by this fragmentary tooth. The also been reported in other Miocene Caribbean marine original description lacks enough detail to be definitive, and assemblages of the Neotropics (see Systematic Paleontology therefore the specimen could also be attributed to a small C. section and Fig. 8). megalodon or perhaps the extinct mako shark Carcharodon On the other hand, most of the taxa described here have hastalis (see Ehret et al., 2012 for discussion on the systematic related modern species that have a cosmopolitan distribution in of this species). However, no mako sharks have been recovered today’s oceans, except for Carcharhinus perezi,whichis from the Gatun Formation of Panama. The absence of this taxon restricted to the Caribbean Sea (Fig. 8). The genus Rhizoprio- may be due to the typically bathyal or mesopelagic depth range nodon has extant representatives mainly distributed in the of this species (Aguilera and Rodrigues de Aguilera, 2001). Atlantic Ocean (Rhizoprionodon terranovae, Rhizoprionodon Additional omissions in our study relative to Gillette’s (1984) lalandii, and Rhizoprionodon porosus, Compagno, 1984). Of the original descriptions include Physogaleus (Galeocerdo) adun- batoids, Rhynchobatus luebberti and Mobula hypostoma are cus, Sphyrna arambourgi, Sphyrna zygaena,andIsistius sp. currently restricted to the Atlantic Ocean; Taeniura aff grabata These differences reflect the reanalysis and redescription of the is distributed in both the eastern Atlantic and the Indian Oceans; original material. The teeth from the SMU collection were not and Myliobatis cf. californica, Rhinoptera cf. steindachneri and catalogued until this study, making the identification of the Mobula munkiana are currently restricted to the eastern Pacific individual specimens described by Gillette (1984) somewhat (Fig. 8). problematic. The teeth that Gillette (1984) referred as Phys- Regardless of the strong Caribbean affinity of the fossils from ogaleus (Galeocerdo) aduncus were missing from the SMU the Gatun Formation, the chondrichthyan fauna has modern collection and not available for comparison. Sphyrna arambour- mixed biogeographic affinities, including cosmopolitan and gi and S. zygeana have been reidentified as the scalloped Pacific distributions. This suggests that around 10 million yr hammerhead shark (Sphyrna lewini) in this study. The ago, a connection between the two oceans was likely maintained morphology of these fossil teeth is more consistent with S. and that despite the ongoing shoaling of isthmus region (Montes lewini than either S. arambourgi or S. zygaena.Furthermore,the et al., 2012b), the chondrichthyan fauna was not isolated in presence of Isistius sp. in the Gatun Formation is refuted. Based Central America. PIMIENTO ET AL.—LATE MIOCENE SHARKS AND RAYS FROM PANAMA 769

FIGURE 8—Biogeography and depth preferences of the chondrichthyans from the Gatun Formation. Key: e¼extant distribution; x¼fossil occurrences in the Neotropics; dashed line separates the neritic zone (below the 200 m); gray box indicates total depth range observed by Hendy (2013) from the Gatun Formation. References for the bathymetry of each taxa are presented in the Systematic Paleontology section.

PALEOENVIRONMENT AND PALEOECOLOGY While Hendy (2013; Fig. 8) indicated considerable fine-scale Previous studies of the Gatun Formation indicate that this area fluctuations in paleobathymetry through the stratigraphy of the was a shallow-water embayment with depths between 20 and 40 Gatun Formation, those variations are beyond the resolution of m and salinity conditions similar to those found in large bays the depth preference analysis carried out here. Nevertheless, (Coates and Obando, 1996; Teranes et al., 1996, 1999; Hendy, they might be used as a framework for interpreting changes in chondrichthyan taxonomic composition (Fig. 9). For the most 2013). Based on depth preferences of extant chondrichthyans part, taxonomic composition changes little throughout the related to the fossil taxa occurring in the Gatun Formation, we stratigraphy, but it is noteworthy that no batoids have been assert that this area was a shallow paleoenvironment. Many of recorded from the deepest water section (upper member) of the the chondrichthyans that inhabited this environment occurred in Gatun Formation. The absence of batoids in this section is not the neritic zone, above 200 m depth (Fig. 8, dashed line). Taxa surprising, given their preferences for shallow continental with larger depth ranges (greater than 200 m) represent a small waters (Carpenter and Niem, 1999). proportion of the total assemblage (3.14% of total of specimens) Tooth-size comparisons of specimens from the Gatun and include Carcharhinus falciformis (three specimens, 0.38%), Formation were made when possible with measurements of Carcharhinus obscurus (six specimens, 0.75%), Carcharhinus chondrichthyan specimens from two formations exposed at the plumbeus (five specimens, 0.63%), Sphyrna lewini (six speci- Lee Creek Mine, Aurora, North Carolina (Purdy et al., 2001): mens, 0.75%)andTaeniura aff. grabata (five specimens, the Pungo River Formation (middle Miocene) and the Yorktown 0.63%; Fig. 2). In addition, the absence of other pelagic fauna Formation (early Pliocene). These formations are older and commonly found in Miocene assemblages of the region such as younger, respectively, than the late Miocene Gatun Formation Alopias, Carcharodon, Isurus and Odontaspis (Portell et al., (11.8 to 8.4 million yr ago; Coates, 1999). Based on the size of 2008; Aguilera and Rodrigues de Aguilera, 2001; Ward and the isolated teeth found within the Gatun Formation, we assert Bonavia, 2001; Iturralde-Vinent et al., 1996; Laurito, 1999), that chondrichthyans inhabiting Panama during the late Miocene supports the hypothesis that the Gatun Formation represents a were generally smaller than those at the comparable sites. shallow-water environment. Nevertheless, we cannot conclude that the small size observed in 770 JOURNAL OF PALEONTOLOGY, V. 87, NO. 5, 2013

FIGURE 9—Stratigraphy, chondrichthyan taxonomic composition, and paleobathymetry of the Gatun Formation. The abundance of the eight most abundant taxa (.20 elements) is pooled for each 50 m intervals of the composite stratigraphy in Figure 2. Each gray box representing estimated paleobathymetry indicates the shallowest and deepest estimated paleodepth for each 50 m interval (adapted from Hendy, 2013). the Gatun Formation is related to juvenile stages of the different (TL) of the individuals following the methods described in taxa without a careful study of the ontogenetic changes that Pimiento et al. (2010). Our estimates show that most of the new occur in each species, nor without estimates of their total length. individuals were also juveniles, including one neonate present in On the other hand, rigorous analyses have been made for the our new subsample (Table 1). These results are in agreement species Carcharocles megalodon in Pimiento et al. (2010). with the nursery area hypothesis proposed for C. megalodon. Based on different size comparisons and estimates of their total Additionally, our observation of a generally small tooth-size in length, the relatively small size of C. megalodon teeth from the the chondrichthyan fauna, suggests that other species may have Gatun Formation indicates a preponderance of juveniles, and had high proportions of juveniles, and that different shark suggests that this species used northern Panama as a paleo- species could have shared this nursery. More analyses on the nursery area. Nursery areas are geographically discrete zones other chondrichthyan taxa from the Gatun Formation are needed that can be shared by multiple species, and where neonates are in order to test this hypothesis. present and juveniles are found in high proportions (Castro, 1993; Heupel et al., 2007; Pimiento et al., 2010). CONCLUSIONS In this study, we were able to collect further 22 C. megalodon We have analyzed the diversity, taxonomic composition, specimens beyond those that were included in the 2010 work. biogeography, paleoenvironments and paleoecology of the Twelve teeth were complete enough to estimate the total length chondrichthyans from the late Miocene of Panama based on PIMIENTO ET AL.—LATE MIOCENE SHARKS AND RAYS FROM PANAMA 771

TABLE 1—Carcharocles megalodon teeth measurements from the Gatun support. Lastly, we thank J. Ceballos for editing an earlier version Formation, Panama (modified from Pimiento et al., 2010). Neonates: T¼up of this manuscript, and O. Aguilera and an anonymous reviewer to 4 m; juveniles: T¼4–10 m; adults: TL¼from 10 m (Gottfried et al., 1996). who helped improving it. C. Jaramillo thanks the University of Specimen CW (mm) CH (mm) Position TL (m) Yale Edward P. Bass Distinguished Visiting Environmental UF 237898 53.0 50.0 upper anterior 5.9 Scholarship and A. Hendy acknowledges support from the Jon UF 237914 31.4 46.4 upper lateral 8.0 A. and Beverly L. Thompson Endowment. C. Pimiento thanks J. UF 237949 35.7 32.9 upper anterior 3.9 McLaughlin for support. This is University of Florida Contribu- UF 237950 47.7 54.2 lower anterior 7.3 UF 237951 26.8 17.6 upper lateral 3.1 tion to Paleontology number 628. 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