Late Miocene chondrichthyans from Lago Bayano, Panama: Functional diversity, environment and biogeography

Victor J. Perez; Catalina Pimiento; Austin Hendy; Gerardo González-Barba; Gordon Hubbell; Bruce J. MacFadden

doi:10.1017/jpa.2017.5

Late Miocene chondrichthyans from Lago Bayano, Panama: Functional diversity, environment and biogeography

Published online by Cambridge University Press: 11 April 2017

Victor J. Perez ,

Catalina Pimiento ,

Austin Hendy ,

Gerardo González-Barba ,

Gordon Hubbell and

Bruce J. MacFadden

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Victor J. Perez: Affiliation:
Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA, 〈[email protected]〉; 〈[email protected]〉 Department of Geological Sciences, University of Florida, Gainesville, FL 32611, USA
Catalina Pimiento: Affiliation:
Paleontological Institute and Museum, University of Zürich, Ch-8006 Zürich, Switzerland, 〈[email protected]〉 Smithsonian Tropical Research Institute, Center for Tropical Paleoecology and Archaeology, Box 2072, Panama, Republic of Panama
Austin Hendy: Affiliation:
Smithsonian Tropical Research Institute, Center for Tropical Paleoecology and Archaeology, Box 2072, Panama, Republic of Panama Natural History Museum of Los Angeles, Los Angeles, CA 90007, USA, 〈[email protected]〉
Gerardo González-Barba: Affiliation:
Museo de Historia Natural, Area de Ciencias del Mar, La Paz, Universidad Autonoma de Baja California Sur, AP 23080, Mexico, 〈[email protected]〉
Gordon Hubbell: Affiliation:
Jaws International, Gainesville, FL, USA, 〈[email protected]〉
Bruce J. MacFadden: Affiliation:
Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA, 〈[email protected]〉; 〈[email protected]〉 Department of Geological Sciences, University of Florida, Gainesville, FL 32611, USA

Article contents

Abstract
Introduction
Geologic setting
Materials and methods
Systematic paleontology
Discussion
Conclusion
References

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Abstract

This newly described chondrichthyan fauna from the late Miocene Chucunaque Formation of Lago Bayano reveals a prolific and highly diverse assemblage from Panama, and one of the richest shark faunas from the Neotropics. Strontium geochronology indicates an age of 10–9.5 Ma for the chonrichthyan-bearing strata. Field efforts resulted in 1429 identifiable specimens comprising at least 31 taxa, of which at least eight are new to the documented fossil record of Panama. With this information an analysis of functional diversity was conducted, indicating ecosystems dominated by generalist species feeding upon a wide range of organisms, from plankton to marine mammals. A probabilistic approach of paleobathymetric estimation suggests a neritic environment. Previous studies based on foraminifera have suggested that the Chucunaque Formation had a greater Pacific Ocean affinity, making this the first Miocene chondrichthyan fauna described from the Pacific shelf of Panama. However, our geographic comparisons show that this fauna has mixed Caribbean and Pacific biogeographic affinities, which likely supports the previously purported connection between chondrichthyan faunas during the late Miocene.

Type: Articles
Information: Journal of Paleontology , Volume 91 , Issue 3 , May 2017 , pp. 512 - 547

DOI: https://doi.org/10.1017/jpa.2017.5 [Opens in a new window]
Copyright: Copyright © 2017, The Paleontological Society

Introduction

Lago Bayano in Panama Province, Panama is an artificial lake that contains an extraordinarily rich assemblage of chondrichthyans. Hundreds of shark and ray teeth erode from host sediments and concentrate on the shorelines of emerged lake islands as a result of annual water-level fluctuations. Prior to the damming of the Rio Bayano drainage that created Lago Bayano, Stewart (Reference Stewart1966) made a geological reconnaissance of this region and mapped what is now Lago Bayano as the Chucunaque Formation (Shelton, Reference Shelton1952). Chondrichthyan remains were noted to be common in the marine mudstones and sandstones of the deeply incised river valleys, although no collections were retained. More recently, Coates et al. (Reference Coates, Collins, Aubry and Berggren2004) mapped the Chucunaque Formation throughout the Darien Province of Panama. Even though marine vertebrates were not reported, this study confirmed a late Miocene age for the unit, and noted a foraminiferal assemblage indicating a Pacific Ocean affinity. In the present study, new biostratigraphic and Sr-isotope analyses derived from marine invertebrate fauna yield ages of 10–9.5 Ma for chondrichthyan-bearing strata in Lago Bayano.

The closure of a Central American Seaway (CAS) and consequent formation of the Isthmus of Panama during the Neogene extremely affected tropical American (=Neotropical) marine communities and increased the biogeographic complexity of the region (e.g., Coates and Obando, Reference Coates and Obando1996). Miocene chondrichthyan faunas are fundamental to understand these processes because they were: (1) abundant and widely distributed during this time, and (2) have been proven to be good paleobathymetry indicators of the deposits adjacent to the CAS (e.g., Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a; Carillo-Briceño et al., 2015a). However, previous studies on Miocene chondrichthyans of Panama have been limited to Caribbean faunas (e.g., the Gatun Formation, Gillette, Reference Gillette1984; Pimiento et al., Reference Pimiento, Ehret, MacFadden and Hubbell2010; Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a; the Culebra Formation, Pimiento et al., Reference Pimiento, Gonzalez-Barba, Hendy, Jaramillo, MacFadden, Montes, Suarez and Shippritt2013b; and the Chagres Fromation, Carrillo-Briceño et al., Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a). Hence, the chondrichthyan fauna of Lago Bayano is the first Miocene fauna from the Pacific shelf of Panama to be described. The only other chondrichthyan fauna described from the Pacific of Panama was the Eocene Tonosi Formation from the Azuero Peninsula (Vasquez and Pimiento, Reference Vasquez and Pimiento2014). Other late Miocene shark assemblages from the region include Ecuador (Longbottom, Reference Longbottom1979; Carrillo-Briceño et al., Reference Carrillo-Briceño, Aguilera and Rodriguez2014), Venezuela (Sánchez-Villagra et al., Reference Sanchez-Villagra, Burnham, Campbell, Feldmann, Gaffney, Kay, Lozsan, Purdy and Thewissen2000; Aguilera and Rodrigues de Aguilera, Reference Aguilera and Rodrigues De Aguilera2001; Carrillo-Briceño et al., Reference Carrillo-Briceño, Maxwell, Aguilera, Sánchez and Sánchez-Villagra2015b), Jamaica (Donovan and Gunter, Reference Donovan and Gunter2001), Costa Rica (Laurito and Valerio, Reference Laurito and Valerio2008), and Grenada (Portell et al., Reference Portell, Hubbell, Donovan, Green, Harper and Pickerill2008). All of these studies have provided a better understanding on the composition of marine communities during a time of rapid change.

It has been argued that while most works on ancient chondrichthyan faunas provide valuable information about taxonomic diversity, they are somehow limited in their ecological interpretations because they ignore species functions in ecosystems (Moore, Reference Moore2001; Hooper et al., Reference Hooper, Solan, Symstad, Diaz, Gessner, Buchmann, Degrange, Grime, Hulot, Mermillod-Blondin, Roy, Spehn and Van Peer2002). To address this issue, functional diversity is often measured as a means to quantify the impact of species on ecosystems (Petchey and Gaston, Reference Petchey and Gaston2006). The correlation that exists between tooth morphology and diet can be used to apply a functional diviersity approach to the study fossil chondrichthyan faunas (e.g., Bertolini, Reference Bertolini1933; Moss, Reference Moss1977; Cappetta, Reference Cappetta1986, Reference Cappetta1987, Reference Cappetta2012; Frazzetta, Reference Frazzetta1988; Kent, Reference Kent1994). Specifically, a classification scheme has been outlined by Kent (Reference Kent1994) in which chondrichthyan dentitions are subdivided into nine types: five homodont forms (cutting, grasping, clutching, crushing, and vestigial) and four heterodont forms (cutting-grasping, grasping-cutting, grasping-crushing, and clutching-crushing). A more complex scheme was developed by Compagno (Reference Compagno1990) that grouped sharks, rays, and chimaeroids into ecomorphotypes based on varying life histories, which incorporates the morphology, habitat, and behavior of each taxon. These ecomorphotypes have been utilized in numerous studies of extant sharks, especially those pertaining to conservation (Martin, Reference Martin2005; Zhou and Griffiths, Reference Zhou and Griffiths2008; Lucifora et al., Reference Lucifora, García and Worm2011; Grogan et al., Reference Grogan, Lund and Greenfest-Allen2012; Ritter, Reference Ritter2014), but have not been employed in many paleontological studies. Here, we integrate dentition types and ecomorphotypes as a measure of functional diversity. This approach provides novel information regarding the function of chondrichthyan species in the ecosystems adjacent to the CAS during the late Miocene.

This paper describes the taxonomy and systematics of the chondrichthyan fauna from Lago Bayano and interprets the diversity, paleoenvironment, and paleobiogeographic significance of this new and prolific marine vertebrate fauna. These interpretations will be based in functional diversity analyses and a unique approach toward analyzing paleobathymetry. We will show that this new discovery sheds a light on the dynamics of ancient marine faunas in the New World tropics during the late Miocene.

Geologic setting

The thick sequence of Cretaceous through Neogene sediments that occupy the central lowlands paralleling the San Blas and Darien highlands of Darien Province in eastern Panama forms the Bayano, Chucunaque-Tuira, and Atrato basins (Stewart, Reference Stewart1966; Duque-Caro, Reference Duque-Caro1990; Coates et al., Reference Coates, Collins, Aubry and Berggren2004). The Chucunaque-Tuira and Atrato basins were subject to a detailed review by Coates et al. (Reference Coates, Collins, Aubry and Berggren2004) who established the lithostratigraphy used herein, provided biostratigraphic and paleobathymetric context, and interpreted their geological history. The Bayano Basin was not investigated, however, and our present understanding of the geology is built around the geological reconnaissance of Stewart (Reference Stewart1966), extrapolation of Coates et al. (Reference Coates, Collins, Aubry and Berggren2004), and more recent mapping as a part of a broader study into the tectonic history of the Panama Isthmus (Montes et al., Reference Montes, Bayona, Cardona, Bush, Silva, Moron, Hoyos, Ramirez, Jaramillo and Valencia2012a, Reference Montes, Cardona, Bayona, McFadden, Buchs, Morón, Silva, Hoyos, Restrepo-Moreno, Ramírez, Wilson, Ortiz, Farris, Jaramillo, Valencia, Bryan and Flores2012b). Attempts to map this region, locate contacts, and measure stratal thickness have been challenged by lack of exposure, discontinuous outcrops (often submerged or forested), and obscure folding and faults. In a general sense, the succession in the Lago Bayano area consists of Cretaceous volcanic intrusives (Darien Formation), Oligocene–early Miocene agglomerates (Porcona Formation), early–middle Miocene limestone (Clarita Formation), turbiditic sandstone and claystone (Membrillo Formation), overlain by late Miocene fossiliferous and conglomeratic sandstone and siltstone (Chucunaque Formation) (Terry, Reference Terry1956; Stewart, Reference Stewart1966; Coates et al., Reference Coates, Collins, Aubry and Berggren2004). These units can be observed along the shoreline of southern Lago Bayano, Rio Maje, Rio Tigre, Carratera Panamericana, and minor roads (Fig. 1; Table 1).

Figure 1 Map of Lago Bayano, Panama with collecting sites denoted by black circles. Numbers labelling each collecting site refer to the last three digits of the Smithsonian Tropical Research Institute (STRI) field number (Table 1).

Table 1 List of localities bearing chondrichthyan remains within Lago Bayano. GPS coordinates of STRI 300029 (Bayano 8) were improperly recorded and are not reported here; most likely this locality is within the cluster of islands that did bear chondrichthyan remains in southeastern Lago Bayano (Fig. 1). Specimens from Bayano 12 are all from a single locality, however sample labels and GPS coordinates were lost during transport and reported by FLMNH Site Key in the text. All GPS coordinates were taken using WGS84 datum. STRI locality (STRI Loc.) numbers can be searched in the STRI Geological Sample Database (http://biogeodb.stri.si.edu/jaramillo/fossildb). FLMNH=Florida Museum of Natural History and STRI=Smithsonian Tropical Research Institute.

Stewart’s (Reference Stewart1966) original description of the geology in this region was done prior to the damming of the Rio Bayano and the formation of the artificial lake that is now Lago Bayano. In this initial description he noted the presence of chondrichthyan remains in Miocene-aged sandstones of the Chucunaque Formation in the deeply incised Rio Bayano and its tributaries. Other marine fossils (e.g., molluscs and foraminifera) were recognized in other Miocene-aged units, but chondrichthyan remains were restricted to the sandstone facies of the Chucunaque Formation. The construction of the Bayano Dam in 1976 flooded 350 km² of rainforest to form Lago Bayano, making it difficult to reconstruct original sediment composition and sedimentary structures of the Chucunaque Formation at many of the chondrichthyan-bearing localities. The chondrichthyan remains utilized in this study are left as a residue among reworked gravel, sand, and mud grains along island shorelines. In the southeastern-most portion of the lake, exposed uneroded blocks comprise strongly weathered and sparsely fossiliferous orange mudstone. The islands in the northern portion of southern Lago Bayano contain a more varied range of facies, including fossiliferous, gritty orange sandstone and a fine-grained tuffaceous white sandstone.

In much of the Darien Province, the Chucunaque Formation of Shelton (Reference Shelton1952) is Messinian in age (7.1–5.6 Ma), although Coates et al. (Reference Coates, Collins, Aubry and Berggren2004) suggested that it could be older than 9.4 Ma in the western part of their study area on the basis of calcareous nannofossil biostratigraphy. This age is consistent with ⁸⁷Sr/⁸⁶Sr dates of 10–9.5 Ma derived from calcerous Lindapectin shells that were deposited in association with the chondrichthyan remains on the shoreline of STRI 290138 (N 9.1552, W 78.7824) and STRI 300032 (N 9.1411, W 78.7545; Tables 1, 2). In July 2015, a research group returned to Lago Bayano and observed unusually low lake levels, which resulted in some minor exposures of the in situ fossiliferous layer along STRI 290116 and STRI 300032. Calcareous microfossils picked from this in situ layer were dated using ⁸⁷Sr/⁸⁶Sr isotopic ratios from STRI 300032, and found to be consistent with the ages of the Lindapectin (personal communication, A. Waite, 2016). This fauna is therefore Tortonian in age and correlative with the other important chondrichthyan-bearing units in Central and South America, including the Gatun Formation and Alajuela Formation of central Panama (Gillette, Reference Gillette1984; Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a; MacFadden et al., Reference MacFadden, Jones, Jud, Moreno, Morgan, Portell, Perez, Moran and Wood2017), Angostura Formation of Ecuador (Carrillo-Briceño et al., Reference Carrillo-Briceño, Aguilera and Rodriguez2014), and upper Urumacro Formation of Venezuela (Carrillo-Briceño et al., Reference Carrillo-Briceño, Maxwell, Aguilera, Sánchez and Sánchez-Villagra2015b).

Table 2 Strontium isotope data and age estimates from the Chucunaque Formation of Lago Bayano.

Materials and methods

In 2010 we began to collect fossils from Miocene sediments exposed along the islands of Lago Bayano (Fig. 1). The sharks and ray teeth are most easily collected when lake levels are low and fossiliferous sedimentary zones are exposed. Chondrichthyan remains were collected from 12 localities within Lago Bayano, resulting in 1422 teeth and seven non-dental elements. Surface collecting was done at all 12 localities and produced 768 chondrichthyan teeth and two vertebral centra. Matrix was collected from five of the 12 localities and washed through a set of screens with 6, 1.5, 1.0, and 0.5 mm mesh, which produced 654 chondrichthyan teeth, two vertebral centra, two stingray caudal spines, and one stingray dermal denticle. To illustrate that we have accurately sampled both surface and screenwashed material, randomized species accumulation curves were created (Fig. 2) using the vegan package (Oksanen et al., Reference Oksanen, Blanchet, Kindt, Legendre, O’Hara, Simpson, Solymos, Stevens and Wagner2010) in the program R (R Development Core Team, 2012).

Figure 2 Sampling effort for surface-collected and screenwashed material via two randomized species accumulation curves. (1) Accumulation curves reported as number of specimens versus number of species (i.e., richness) for surface-collected (light gray) and screenwashed material (dark gray), respectively; shaded polygons represent confidence intervals. (2) Accumulation curve reported as number of localities (i.e., collecting sites versus richness) for surface-collected (light gray) and screenwashed material (dark gray), respectively; shaded polygons indicates the confidence interval.

Age estimates derived from ⁸⁷Sr/⁸⁶Sr isotopic ratios of marine calcareous shells and marine calcareous sediment may be compared to global ratios of ⁸⁷Sr/⁸⁶Sr through geologic time to estimate a geological age (Burke et al., Reference Burke, Denison, Hetherington, Koepnick, Nelson and Otto1982; Koepnik et al., Reference Koepnick, Burke, Denison, Heatherington, Nelson, Otto and Waite1985; Hodell and Woodruff, Reference Hodell and Woodruff1994; McArthur, Reference McArthur1994). Samples were obtained from the Lago Bayano assemblage itself, and from presumably coeval strata outcropping nearby (Table 2). Age estimates were determined using the Miocene and Pliocene portions of Look-Up Table Version 4:08/03 (Howarth and McArthur, Reference Howarth and McArthur1997; McArthur et al., Reference McArthur, Howarth and Bailey2001) associated with the strontium isotopic age. Strontium isotope analyses of Lago Bayano samples used well-preserved calcitic shells and followed the sampling and analytical protocols of Kirby et al. (Reference Kirby, Jones and Ávila2007, Reference Kirby, Jones and MacFadden2008). These were performed on a Micromass Sector 54 Thermal Ionization Mass Spectrometer (TIMS) in the Department of Geological Sciences at UF. Strontium was loaded onto oxidized tungsten single filaments and run in triple collector dynamic mode. Data were acquired at a beam intensity of ~1.5 V for ⁸⁸Sr, with corrections for instrumental discrimination made assuming ⁸⁶Sr/⁸⁸Sr ratio of 0.1194. Errors in measured ⁸⁷Sr/⁸⁶Sr are better than ±0.00002 (2 σ), based on long-term reproducibility of NBS 987 (⁸⁷Sr/⁸⁶Sr=0.71024). Due to the poor preservation of shell material in the Lago Bayano succession, ⁸⁷Sr/⁸⁶Sr isotope analyses were only conducted on samples from two localities (STRI 290138 and 300032) where calcitic shells of Lindapecten were present; at many localities even calcitic taxa are represented as external molds.

Information regarding biology, anatomy, distribution, habitat preferences, and feeding mechanisms were gathered from the literature cited below. Much of this information can be found in a coherent format in The IUCN Red list of Threatened Species (www.iucnredlist.org) or Fishbase (www.fishbase.org). Measurements of macro teeth were taken using calipers, whereas measurements of micro teeth were taken directly from SEM images. Crown height (CH=the distance between the crown tip and crown-root margin) and crown width (CW=maximum distance between the mesial and distal edge at the crown-root margin) were measured for labio-lingually flatten teeth (i.e., most taxa belonging to the subdivision Selachii). Crown length (CL=tooth thickness, defined herein as the maximum distance between the labial and lingual edge in occlusal view) was additionally measured in teeth with a broad occlusal surface (i.e., those belonging to the superorder Batomorphii and the genus Mustelus). In order to measure CH, a line was drawn from the crown apex perpendicular to the crown-root contact (e.g., Pimiento et al., Reference Pimiento, Ehret, MacFadden and Hubbell2010, fig. S2). It is important to note that many other authors will report the tooth height, which is generally a measurement of the entire tooth (crown and root) and is not directly comparable to the CH measurements reported herein.

Taxonomic composition is reported as a histogram depicting the relative abundance of chondrichthyan genera. Functional diversity is interpreted via two proxies (dentition types and ecomorphotypes). Dentition types, as defined by Kent (Reference Kent1994), were assigned to each taxon based on tooth morphology of fossil and modern representatives. For example, in the case of Carcharhinus plumbeus, fossil occurrences were limited to upper teeth that have a cutting-type morphology; however, based on the dentition of the living representatives, we can infer a cutting-grasping type dentition. Ecomorphotypes, as defined by Compagno (Reference Compagno1990), were assigned to each taxon based on morphology, habitat, and behavior of modern analogs. Both proxies were then plotted as pie charts that illustrate the relative abundance of dentition types and ecomorphotypes, respectively. A weighted analysis of paleodepth frequency was performed using R. This analysis incorporated the abundance (in the fossil assemblage) and depth preference (as reported in the literature) from taxa with modern analogs. Taxa that were unable to be assigned to the species level and those that are extinct were not included in this analysis in order to reduce potential bias. The data were then resampled 10,000 times and plotted as a histogram that provides a 95% confidence interval and a mean depth. This method was applied to the chondrichthyan fauna from the Chucunaque Formation, the Gatun Formation, and the Piña Sandstone facies of the Chagres Formation. The average and maximum depth estimates are reported in Figure 14 and Table 4. The average depth is the average of the usual depth range and the maximum depth is the upper limit of the usual depth range of each taxon. All data utilized for these analyses are available in Table 3.

Table 3 Complete taxonomic list of the chondrichthyes of Lago Bayano, including a summary of all relevant data for the subsequent analyses. References for common depth ranges and biogeographic affinity (i.e., Atlantic vs. Pacific) can be found in the Systematic Paleontology section, ecomorphotypes are based on Compagno (Reference Compagno1990), and descriptions of dentition types can be found in Kent (Reference Kent1994). * indicates a new taxon for the fossil record of Panama. † indicates an extinct species.

Institutional abbreviations and repositories

The specimens described here are conserved in the Vertebrate Paleontology Collection of the Florida Museum of Natural History (FLMNH), University of Florida (UF). Specimen information can be found in the FLMNH Vertebrate Paleontology Database (http://www.flmnh.ufl.edu/vertpaleo-search/) or in the Smithsonian Tropical Research Institute (STRI) Geological Sample Database (http://biogeodb.stri.si.edu/jaramillo/fossildb).

Systematic paleontology

Class Chondrichthyes Huxley, Reference Huxley1880

Subclass Elasmobranchii Bonaparte, Reference Bonaparte1838

Order Squaliformes Goodrich, Reference Goodrich1909

Family Centrophoridae Bleeker, Reference Bleeker1859

Genus Centrophorus Müller and Henle, Reference Müller and Henle1837

Type

Centrophorus granulosus Müller and Henle, Reference Müller and Henle1837 (Cappetta, Reference Cappetta2012).

Centrophorus sp.

Figure 3.1, 3.2

Figure 3 SEM images of specimens belonging to the subdivision Selachii. (1, 2) Centrophorus sp., UF 281349, lower anterolateral tooth in lingual and labial view, respectively; (3–6) cf. Iago sp.: (3, 4) UF 281382, lateral tooth in lingual and labial view, respectively; (5, 6) UF 281383, anterolateral tooth in lingual and labial view, respectively; (7–9) Mustelus sp., UF 281384, indeterminate position in occlusal, lingual, and baso-labial view, respectively; (10–13) Mustelus sp., UF 281386, indeterminate position in occlusal, basal, lingual, and labial view, respectively; (14–19) Physogaleus sp.: (14, 15) UF 281354, upper lateral tooth in lingual and labial view, respectively; (16, 17) UF 281353, anterior tooth in lingual and labial view, respectively; (18, 19) UF 281351, indeterminate position in lingual and labial view, respectively; (20, 21) Carcharhinus sp., UF 281338, pathologic upper tooth in lingual and labial view, respectively.

Occurrence

STRI 290109.

Description

Small, asymmetric tooth with a broad crown and an apron indicative of the order Squaliformes. However, it is worth noting that the apron is not characteristic of all families within the order Squaliformes, as it is absent in the upper teeth of Dalatiidae, Oxynotidae, and Etmopteridae. The mesial edge is convex basally and straight apically, has coarse serrations near the base that become smaller apically and disappear prior to the apex; the distal edge is slightly convex with a complete cutting edge. There is a prominent notch on the distal edge; however, the distal heel is not entirely preserved. The labial face is flat with an elongate apron that extends well onto the root. The lingual face is convex with a short uvula that comes to a point. In labial view on the mesial side, the root is narrow, has a slightly concave basal margin, and a large foramen adjacent to the apron. On the distal side, the root is mostly broken off, but appears to have been larger than the mesial side. On the lingual face, there is a slight lingual bulge at the extremity of the uvula, a large infundibulum beneath the uvula, and a depression on the mesial side of the root. Centrophorus sp. from the Chucunaque Formation has a CH=2.06 mm and CW=2.28 mm.

Material

One isolated tooth; anterolateral: UF 281349.

Remarks

No teeth from the order Squaliformes were identified from the Gatun Formation (Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a); however, they dominate the Piña Sandstone facies of the Chagres Formation (Carrillo-Briceño et al., Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a). In contrast, only a single tooth from the Chucunaque Formation was identified as belonging to this order. Cappetta (Reference Cappetta1987, Reference Cappetta2012) mentioned that the apron does not extend past the root in Centrophorus; however, that character cannot be addressed with this specimen (Fig. 3.2). Cappetta (Reference Cappetta1987, p. 53) described Centrophorus as being “not rare in bathyal deposits” in the Miocene of France. Carrillo-Briceño et al. (Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a) identified 11 teeth as Centrophorus aff. C. granulosus. Extant Centrophorus granulosus are widespread with occurrences in the Eastern Atlantic, Western Central Atlantic, the Indian Ocean, and the Western Pacific (Compagno, Reference Compagno1984; Last and Stevens, Reference Last and Stevens1994; and Compagno and Niem, Reference Compagno and Niem1998); however, it is not known from the Eastern Pacific (White et al., Reference White, Ebert, Naylor, Ho, Clerkin, Veríssimo and Cotton2013). Extant representatives of the family Centrophoridae most commonly occur at depths of 1000–1500 m, however they have been reported at depths as shallow as 50 m (Compagno et al., Reference Compagno, Dando and Fowler2005).

Order Lamniformes Berg, Reference Berg1958

Family Otodontidae Glikman, Reference Glikman1964

Genus Carcharocles Jordan and Hannibal, Reference Jordan and Hannibal1923

Type

Carcharodon auriculates Blainville, Reference Blainville1818 (Cappetta, Reference Cappetta2012).

Carcharocles megalodon (Agassiz, Reference Agassiz1835)

Figure 4.1–4.5

Figure 4 Lamniformes: Carcharocles, Isurus, and Alopias from the Chucunaque Formation. (1–5) Carcharocles megalodon (Agassiz, Reference Agassiz1843): (1, 2) UF 275110, upper right anterior (most complete tooth) in lingual and labial view, respectively (scale bar=5 cm); (3–5) UF 275108, upper tooth bearing a vestigial lateral cusplet in lingual, labial, and lateral view, respectively (scale bar=5 cm); (6–16) Isurus oxyrinchus (Rafinesque, Reference Rafinesque1810): (6–8) UF 275124, lower right lateral in lingual, labial, and distal lateral view, respectively (scale bar=1 cm); (9–12) UF 281169, upper left lateral in lingual, labial, mesial lateral, and distal lateral view, respectively (scale bar=1 cm); (13–16) UF 281181, upper lateral tooth in lingual, labial, distal lateral, and mesial lateral view, respectively (scale bar=1 cm); (17–20) Alopias superciliosus (Lowe, 1840), UF 275057, lower position in lingual, labial, distal lateral view, and mesial lateral, respectively (scale bar=1 cm); (21–24) Alopias cf. A. vulpinus (Bonnaterre, Reference Bonnaterre1788), UF 281321, upper position in lingual, labial, mesial lateral, and distal lateral view, respectively (scale bar=1 cm). Photo credit: S. Moran and R. Leder.

Holotype

An upper anterior tooth attributed to Carcharodon megalodon (TE-PLI 18) preserved in the Staatliches Museum für Naturkunde in Karlsruhe, Germany (Purdy et al., Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001). Originally described in Agassiz (Reference Agassiz1835, pl. 29, figs. 2, 3).

Occurrence

STRI 290116, STRI 290125, STRI 290139, STRI 290144, STRI 290145, STRI 300029, STRI 300032, STRI 430011, and STRI 430012.

Description

Large, triangular teeth; broad crown, uniform (or nearly uniform) serrations, convex lingual face with a distinct neck (i.e., bourlette), flat or convex labial face. Robust, thick, and U-shaped root with dispersed foramina; foramina tend to be concentrated at the crown-root contact on the labial face (Fig. 4.1, 4.2). Carcharocles megalodon exhibits monognathic and dignathic heterodonty. Upper teeth are broader, especially at the crown apex, with more convex cutting edges. Lower teeth are narrower with sigmoidal, straight, or concave cutting edges. There is an increasing asymmetry antero-laterally throughout the jaw. Posterior teeth are much smaller than anterior teeth with a more obtuse to nearly straight basal root margin. One specimen, UF 275108, has a reduced lateral cusplet (i.e., a vestigial cusplet; Fig. 4.3–4.5). Carcharocles megalodon from the Chucunaque Formation range from CH=24.6–88.2 mm and CW=28.6–88.0 mm.

Materials

Sixty isolated teeth; upper anterior: UF 275085, UF 275097, UF 275110, UF 275111, UF 275118, and UF 275132; lower anterior: UF 275129 and UF 275136; upper lateral: UF 275084, UF 275092, UF 275109, UF 275114, UF 275128, and UF 275139; lower lateral: UF 275086, UF 275131, and UF 275134; posterior: UF 275053; indeterminate position: UF 275051–52, UF 275096, UF 275098–99, UF 275107–08, UF 275112–13, UF 275117, UF 275126–27, UF 275130, UF 275133, UF 275135, UF 275137, UF 275138, UF 275148, UF 275151, and UF 275156.

Remarks

The generic assignment of this species has been highly contested over the last century, with Carcharocles, Megaselachus, Carcharodon, Procarcharodon, and Otodus all being suggested as the most appropriate. A morphometrics study by Nyberg et al. (Reference Nyberg, Ciampaglio and Wray2006) determined that C. megalodon is not ancestral to Carcharodon carcharias, suggesting it belongs in a separate lineage with Otodus obliquus as the ancestor. Consequently, the oldest alternative generic assignment takes precedence, which is Carcharocles (Jordan and Hannibal, Reference Jordan and Hannibal1923). For a more detailed discussion on this topic see Pimiento et al. (Reference Pimiento, Ehret, MacFadden and Hubbell2010). In the Chucunaque Formation, C. megalodon is intermediate in size between that of the Gatun Formation and the Yorktown Formation (Purdy et al., Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001; Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a; Pimiento and Balk, Reference Pimiento and Balk2015), but more closely aligns with the size range observed in the Gatun Formation, which has been proposed to be a paleonursery for C. megalodon (Pimiento et al., Reference Pimiento, Ehret, MacFadden and Hubbell2010). The lack of lateral cusplets and a broader crown are said to delineate C. megalodon from Carcharocles chubutensis, although neither of those characteristics is absolutely definitive (Kent, Reference Kent1994). Lateral cusplets may still occur in juvenile individuals of C. megalodon (Pimiento et al., Reference Pimiento, Ehret, MacFadden and Hubbell2010), or as vestigial characters in adults (Fig. 4.3–4.5). Carcharocles megalodon had a cosmopolitan distribution, occurring in tropical to temperate coastal habitats (Gottfried et al., Reference Gottfried, Compagno and Bowman1996; Purdy, Reference Purdy1996; Pimiento et al., Reference Pimiento, MacFadden, Clements, Varela, Jaramillo, Velez‐Juarbe and Silliman2016). Recent studies have calculated the most likely time of extinction of this species to be 2.6 Ma (Pimiento and Clements, Reference Pimiento and Clements2015). In the region, C. megalodon occurs in both the Caribbean and the Pacific (Longbottom, Reference Longbottom1979; De Muizon and DeVries, Reference De Muizon and De Vries1985; Long, Reference Long1993; Iturralde-Vinent et al., Reference Iturralde-Vinent, Hubbell and Rojas1996; Laurito, Reference Laurito1999; Aguilera and Rodrigues de Aguilera, Reference Aguilera and Rodrigues De Aguilera2001; Donovan and Gunter, Reference Donovan and Gunter2001; Nieves-Rivera et al., Reference Nieves-Rivera, Ruiz-Yantin and Gottfried2003; Portell et al., Reference Portell, Hubbell, Donovan, Green, Harper and Pickerill2008; Carrillo-Briceño et al., Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a).

Family Lamnidae Müller and Henle, Reference Müller and Henle1838

Genus Isurus Agassiz, Reference Agassiz1843

Type

Isurus oxyrinchus (Rafinesque, Reference Rafinesque1810) (Cappetta, Reference Cappetta2012).

Isurus oxyrinchus (Rafinesque, Reference Rafinesque1810)

Figure 4.6–4.16

Holotype

Originally described as Oxyrhina desori by Agassiz (Reference Agassiz1843, pl. 37, figs. 8–10) from the Miocene of Switzerland. Purdy et al. (Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001) recognized one tooth among the syntypes (ETHGI P145) described by Agassiz (Reference Agassiz1843) as the second upper anterior of Isurus, and named it the lectotype of Isurus oxyrinchus.

Occurrence

Family Triakidae Gray, Reference Gray1851

Genus Iago Compagno and Springer, Reference Compagno and Springer1971

Type

Eugaleus omanensis Norman, Reference Norman1939 (Cappetta, Reference Cappetta2012).

cf. Iago sp.

Figure 3.3–3.6

Occurrence

STRI 290109 and YPA105.

Description

Extremely small teeth with a short crown and root. The crown is distally arched with complete cutting edges. The mesial edge is slightly sigmoid, with a concave base and straight or concave apex; while the distal edge is convex or straight. There is a prominent rounded distal heel that forms a distinct notch. Lingual face is convex and the labial face is flat with weak folds at the crown base. The crown-root contact on the lingual face shows two distinct depressions on the mesial and distal edges where the crown thins out. On the labial face this contact is sharp, forming a distinct ridge. The root is high up on the lingual face with an observable lingual protuberance and distinct transverse furrow that penetrates the labial face. From the Chucunaque Formation cf. Iago sp. range from CH=0.61–0.86 mm and CW=1.01–1.67 mm.

Materials

Thirty-six isolated teeth; lateroposterior: UF 281374, UF 281376, UF 281379; indeterminate position: UF 281373; UF 281375, UF 281377, UF 281378, and UF 281380–83.

Remarks

These are among the smallest shark teeth found in Lago Bayano and are only found through screenwashing efforts. Teeth of cf. Iago sp. are about half the size of those attributed to Physogaleus sp. There are distinct similarities to Iago oamanensis imaged in Herman et al. (Reference Herman, Hovestadt-Euler and Hovestadt1988), particularly the complete cutting edges with a rounded distal heel that forms an acute notch with the principle cusp. Lateral teeth of some species of Triakis, such as T. semifasciata and T. acutipinna, have a similar morphology (Herman et al., Reference Herman, Hovestadt-Euler and Hovestadt1988); however, anterior teeth bear lateral cusplets that were not observed in any of the recovered specimens. Neither Iago nor Triakis have previously been reported from the fossil record of Panama. There are two extant species of Iago, I. garricki and I. omanensis, both of which have a bathydemersal habit. Iago garricki is a tropical species occurring in the Pacific Ocean on upper continental and insular slopes between 250 and 475 m. Iago omanensis occurs in the Indian Ocean and prefers warm, poorly oxygenated water at depths of less than 110 to over 1000 m (Compagno et al., Reference Compagno, Dando and Fowler2005).

Genus Mustelus Linck, Reference Linck1790

Type

Squalus mustelus Linnaeus, Reference Linnaeus1758 (Cappetta, Reference Cappetta2012).

Mustelus sp.

Figure 3.7–3.13

Occurrence

STRI 290109, STRI 290113, and YPA105.

Description

The occlusal surface is smooth and has an elongate, roughly elliptical outline in apical view. The labial edge forms a prominent ridge at the crown-root margin and has a convex edge with folds that may be weak or strongly pronounced. The lingual face has a large central uvula with vertical, flexuous enameloid ripples and a somewhat sinuous outline. Root is thick with a medial groove that forms two short, asymmetric root lobes; there is a foramen nested within the medial groove that is oriented toward the labial side; the basal margin is flat, but slopes toward the labial face. The folds on the labial edge and the enameloid ripples on the lingual uvula are a diagnostic feature for the genus Mustelus (Herman, Reference Herman1982; Cappetta, Reference Cappetta1987; Leder, Reference Leder2013). Two specimens of Mustelus sp. were imaged: UF 281384 in Figure 3.7–3.9 has a CH=0.23 mm, CW=1.17 mm, and CL=0.64 mm; and UF 281386 in Figure 3.10–3.13 has a CH=0.27 mm, CW=1.37 mm, and a CL=0.64 mm.

Materials

Sixteen isolated teeth; indeterminate position: UF 281384–88.

Remarks

Mustelus sp. from the Chucunaque Formation bears similarities to those described by Carrillo-Briceño et al. (Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a), with weak folding on the lingual uvula; however the images provided by Carrillo-Briceño et al. (Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a) do not show the labial face or the root. Mustelus sp. from the Pungo River Formation of the Lee Creek Mine have a CW=1–1.3 mm and a CL roughly half the length of the CW (Purdy et al., Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001). Among the 28 extant species of Mustelus, all have a demersal habit, with most preferring subtropical to tropical conditions; however, Mustelus antarcticus, M. asterias, and M. mustelus prefer temperate waters (Compagno et al., Reference Compagno, Dando and Fowler2005). Some species occur in up to 800 m depth (Kiraly et al., Reference Kiraly, Moore and Jasinski2003), but most species generally occur at depths <200 m (Compagno, Reference Compagno1984).

Family Hemigaleidae Campagno, 1984

Genus Hemipristis Agassiz, Reference Agassiz1843

Type

Hemipristis serra Agassiz, Reference Agassiz1843 (Cappetta, Reference Cappetta2012).

Hemipristis serra Agassiz, Reference Agassiz1843

Figure 5.1–5.16

Figure 5 Carcharhiniformes I: Hemipristis, Galeocerdo, and Physogaleus from the Chucunaque Formation. (1–16) Hemipristis serra Agassiz, Reference Agassiz1843: (1–4) UF 281404, upper anterior tooth in lingual, labial, distal lateral, and mesial lateral view, respectively; (5–8) UF 281174, upper lateral tooth in lingual, labial, distal lateral, and mesial lateral view, respectively; (9–12) UF 281396, upper symphyseal tooth in lingual, labial, distal lateral, and mesial lateral view, respectively; (13–16) UF 281405, lower lateral tooth in lingual, labial, mesial lateral, and distal lateral view, respectively; (17–20) Galeocerdo aduncus (Agassiz, Reference Agassiz1835), UF 275083, indeterminate position in lingual, labial, mesial lateral, and distal lateral view, respectively; (21–28) Galeocerdo cuvier (Peron and Lesueur, Reference Peron and Lesueur1822): (21–24) UF 281397, indeterminate position in lingual, labial, distal lateral, and mesial lateral view, respectively; (25–28) UF 275145, indeterminate position in lingual, labial, distal lateral, and mesial lateral view, respectively; (29–32) Physogaleus contortus (Gibbes, Reference Gibbes1849), UF 281170, indeterminate position in lingual, labial, mesial lateral, and distal lateral view, respectively. Photo credit: R. Leder.

Holotype

Originally described by Agassiz (Reference Agassiz1843, pl. 27, figs. 18–30) from the Miocene of southern Germany. Cappetta (Reference Cappetta2012, fig. 279G–I) illustrated two syntypes: an upper lateral, UM LEE 4, and a lower anterior, UM LEE 5.

Occurrence

Type

Trigonodus secundus Winkler, Reference Winkler1876 (Cappetta, Reference Cappetta2012).

Physogaleus contortus (Gibbes, Reference Gibbes1849)

Figure 5.29–5.32

Holotype

Originally described as Galeocerdo contortus from the Eocene of South Carolina and the Miocene of Virginia by Gibbes (Reference Gibbes1849, pl. 25, figs. 71–74).

Occurrence

STRI 290109, STRI 290116, STRI 290145, STRI 300029, STRI 300032, and STRI 430011.

Description

Moderately large teeth with a slender, distally angled crown. The mesial edge is finely serrated with a warped profile, while the distal edge is notched with fine serrations on the heel and even finer serrations apical of the notch. The root is robust with a U-shaped basal margin and a large lingual protuberance bearing a nutrient groove. Physogaleus contortus from the Chucunaque Formation range from CH=6.1–14.9 mm and CW=9.2–17.1 mm.

Materials

Eighteen isolated teeth; indeterminate position: UF 275037, UF 275059, UF 275064, UF 275069, UF 275125, UF 275146, UF 281170, and UF 281171.

Remarks

Distinguishing features between Physogaleus and Galeocerdo are mentioned above, however it is worthwhile to also mention that Physogaleus has finer serrations on the distal heel with a less drastic distal notch and a more pronounced lingual protuberance on the root. The distribution of Physogaleus contortus is difficult to surmise given the confusion that exists regarding its distinction from the genus Galeocerdo (Cappetta, Reference Cappetta1980, Reference Cappetta1987, Reference Cappetta2012; Gillette, Reference Gillette1984; Kent, Reference Kent1994; Purdy et al., Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001; Ward and Bonavia, Reference Ward and Bonavia2001) and recent re-assignment to the genus Physodon (Leder, Reference Leder2013). Springer (Reference Springer1964) stated that the type specimen of Physodon muelleri described by Müller and Henle (1841) actually belonged to a male Scoliodon laticaudus, and chose to synonymize the two genera (Cappetta, Reference Cappetta1987, Reference Cappetta2012). Leder (Reference Leder2013) described Physodon (=Physogaleus) contortus from the Eocene of Crimea; in which he noted similarities with both Galeocerdo and Physogaleus, but overall determined it was unique and, consequently, chose to resurrect the genus Physodon described by Müller and Henle (1841). Cappetta (Reference Cappetta1980, Reference Cappetta1987, Reference Cappetta2012) described P. contortus as being a characteristic component of the Miocene deposits of the Gulf Atlantic Coastal Plain that does not occur in Europe; however, Purdy et al. (Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001) recognized misidentifications by Storm (Reference Storm1894), Leriche (Reference Leriche1927), and Caretto (Reference Caretto1972) that actually represent P. contortus from Europe. Physogaleus contortus from the Gatun Formation range from CH=10.0–11.1 and CW=12–15.5 mm (Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a) and from the Pungo River Formation range from CH=12.0–19.4 mm and CW=12.0–19.5 mm (Purdy et al., Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001). Purdy et al. (Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001) noted that P. contortus is twice as common as Galeocerdo in the Lee Creek Mine, whereas only two specimens of P. contortus were identified from the Gatun Formation (Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a). In the Chucunaque Formation, P. contortus (N=19) and Galeocerdo (N=17) have nearly the same abundance. The slender, more delicate crown of P. contortus indicates a greater reliance on grasping than cutting during feeding, suggesting a different ecological niche than that of Galeocerdo.

Physogaleus sp.

Figure 3.14–3.19

Occurrence

STRI 290109 and YPA105.

Description

Small teeth, with a triangular shape and a distally arched, labio-lingually compressed crown. The mesial edge is convex or straight; the distal edge is slightly concave to nearly straight. There is a strong distal notch with well-defined lateral cusplets on the distal heel; the mesial heel may or may not bear lateral cusplets. Anterior teeth are more erect and symmetrical than lateral teeth; anterior teeth have a CH:CW ratio close to 1:1, whereas lateral teeth have a CH:CW ratio closer to 1:2. Leder (Reference Leder2013) reported similar height:width ratios for Physogaleus tertius teeth of 1:1 to 5:6 for anteriors and 1:2 for the posterolateral positions. The root has a lingual bulge with nutrient pores at the crown-root margin and a prominent axial nutrient groove that penetrates the labial face; the labial face is narrow with a smooth, nearly horizontal crown-root margin. Physogaleus sp. from the Chucunaque Formation has a range of CH=1.61–3.21 mm and CW=1.81–3.83 mm.

Materials

Fifteen isolated teeth; anterior: UF 281353; upper: UF 281354, UF 281357; lower anterior: UF 281351, UF 281359; indeterminate position: UF 281352, UF 281356, UF 281358, and UF 281360.

Remarks

Interpretation of Physogaleus and related genera, such as Galeorhinus and Physodon, among others, is highly debated. Cappetta (Reference Cappetta1987, Reference Cappetta2012) suggested that fossils identified as Galeorhinus and Physodon may be male and female teeth belonging to the extinct genus Physogaleus. The genus Physogaleus has not yet been reported from Panama, with the exception of Physogaleus contortus, which has since been reassigned to the genus Physodon based on the work of Leder (Reference Leder2013). Galeorhinus cf. G. galeus identified from the Chagres Formation (Carrillo-Briceño et al., Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a) shares many similarities with Physogaleus sp. reported herein; however, they are distinct. Galeorhinus often has a concave mesial apex and convex distal edge, lacks lateral cusplets on the mesial edge, and has robust serrations on the distal heel that rise high up the crown. These teeth are also similar to cf. Iago sp., but differ, especially, in terms of size and the presence of lateral cusplets. Physogaleus sp. is about twice the size of cf. Iago sp. and has well-defined lateral cusplets, although the presence of cusplets may vary depending on the position within the jaw. Physogaleus has been reported from the Eocene of Morocco, West Africa, Egypt, Belgium, Crimea, and Georgia, United States; the Oligocene of Belgium, France, and Hungary; and the Miocene of France (Cappetta, Reference Cappetta1987; Leder, Reference Leder2013).

Genus Carcharhinus Blainville, Reference Blainville1816

Type

Carcharias melanopterus Quoy and Gaimard, Reference Quoy and Gaimard1824 (Cappetta, Reference Cappetta2012)

Carcharhinus falciformis (Bibron, 1841 in Müller and Henle, 1839–Reference Müller and Henle1841)

Type

Aprionodon acutidens subsp. queenslandicus Whitley, Reference Whitley1939 (Cappetta, Reference Cappetta2012).

Negaprion brevirostris (Poey, Reference Poey1868)

Figure 7.1–7.4

Figure 7 Carcharhiniformes III: Negaprion, Rhizoprionodon, and Sphyrna from the Chucunaque Formation. (1–4) Negaprion brevirostris (Poey, Reference Poey1868), scale bar=1 cm: (1, 2) UF 275080, upper left lateral tooth in lingual and labial view, respectively; (3, 4) UF 275080, lower tooth in lingual and labial view, respectively; (5–8) Rhizoprionodon sp., scale bar=0.5 cm: (5, 6) UF 322848, indeterminate position in lingual and labial view, respectively; (7, 8) UF 322849, indeterminate position in lingual and labial view, respectively; (9–12) Sphyrna lewini (Griffith and Smith, Reference Griffith and Smith1834), UF 281176, upper position in lingual, labial, mesial lateral, and distal lateral view, respectively (scale bar=1 cm); (13–18) Sphyrna mokarran (Ruppell, 1837): (13–16) UF 275043, upper position in lingual, labial, mesial lateral, and distal lateral view, respectively, (scale bar=1 cm); (17, 18) UF 275066, upper lateral tooth in lingual and labial view, respectively (scale Bar=0.5 cm); (19–26) Sphyrna zygaena, scale bar=1 cm: (19–22) UF 275073, upper lateral tooth in lingual, labial, mesial lateral, and distal lateral view, respectively; (23–26) UF 275073, lower anterior tooth in lingual, labial, distal lateral, and mesial lateral view, respectively. Photo credit: R. Leder.

Holotype

Originally described as Hypoprion brevirostris by Poey (Reference Poey1868, p. 451, pl. 4, figs. 5, 6, 20). The holotype is unknown; however, the type locality is Cuba (Compagno, Reference Compagno1984).

Occurrence

STRI 290116 and STRI 430012.

Description

Tall, narrow crown, with a convex lingual face and flat labial face that extends onto the root. The cutting edges are complete and extend onto the heels, and may or may not bear serrations. Root is moderately thick with a weak transverse groove. Lateral teeth tend to bear a distal inclination and subsequently exhibit increasing asymmetry. A distinct dignathic heterodonty exists, with upper teeth having a broader crown than lower teeth. Negaprion brevirostris from Lago Bayano range from CH=7.7–11.6 mm and CW=4.8–16.1 mm.

Materials

Three isolated teeth; upper: UF 275080; lower: UF 275150.

Remarks

In the Miocene, this species has been identified as an extinct species, Negaprion eurybathrodon (Cappetta, Reference Cappetta1987; Kent, Reference Kent1994; Purdy et al., Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001); however Pimiento et al. (Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a) recognized that the Miocene morphotype is analogous to the extant species, Negaprion brevirostris, and aptly reassigned it to N. brevirostris. Purdy et al. (Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001) reported anterolateral teeth of N. eurybathrodon (= N. brevirostris) from Lee Creek ranging from CH=14.0–21.0 mm, corresponding to a mature adult body size range of TL=2.1–3 m (Compagno, Reference Compagno1984). Teeth from the Chucunaque Formation and the Gatun Formation (CH=3.7–13.7 mm; Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a) are smaller than those of Lee Creek. Negaprion brevirostris has been identified in the Miocene of Venezuela, Cuba, and Ecuador (Longbottom, Reference Longbottom1979; Iturralde-Vinent et al., Reference Iturralde-Vinent, Hubbell and Rojas1996; Aguilera and Rodrigues de Aguilera, Reference Aguilera and Rodrigues De Aguilera2001; MacPhee et al., Reference MacPhee, Iturralde-Vinent and Gaffney2003). Carrillo-Briceño et al. (Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a) reported two teeth attributed to N. brevirostris from the neritic Rio Indio facies, but no occurrences in the bathyal Piña Sandstone facies of the Chagres Formation. Extant individuals occur in tropical and temperate, estuarine and marine waters generally at depths of 0–92 m (Compagno, Reference Compagno1984; Kent, Reference Kent1994). Negaprion brevirostris frequents mangrove fringes and coral reefs, but occasionally can be found in open ocean near surface waters for migration purposes (Compagno, Reference Compagno1984; Compagno et al., Reference Compagno, Dando and Fowler2005).

Genus Rhizoprionodon Whitley, Reference Whitley1929

Type

Carcharias (Scoliodon) crenidens Klunzinger, Reference Klunzinger1880 (Cappetta, Reference Cappetta2012).

Rhizoprionodon sp.

Figure 7.5–7.8

Occurrence

STRI 290109, STRI 290116, and YPA105.

Description

Small teeth with a short, slender crown; complete cutting edges; and a recurved mesial edge and straight to convex distal edge forming a distinct notch with a rounded distal heel. The root is thin with a deep transverse groove that penetrates a horizontal basal margin. Rhizoprionodon sp. from the Chucunaque Formation range from CH=1.9–2.4 mm and CW=4.1–5.1 mm.

Materials

Fifty-five isolated teeth; indeterminate position: UF 275091, UF 281364–281268, and UF 281370.

Remarks

Much confusion remains regarding the identification of Rhizoprionodon teeth, due to the closely aligned teeth of Sphyrna and, possibly synonymous, teeth of Scoliodon and Loxodon that were established by Springer (Reference Springer1964). Rhizoprionodon sp. differs from Sphyrna lewini in having a shorter crown, recurved mesial edge, and less pronounced root. Rhizoprionodon sp. differs in proportional size relative to Sphyrna, with Sphyrna having a greater crown height to width ratio (Purdy et al., Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001). Cappetta (Reference Cappetta1987) mentioned a marked sexual dimorphism in Rhizoprionodon, but it is possible that fossil specimens described may actually represent the morphologically similar Scoliodon and/or Loxodon. Consequently, identification of teeth from this genus should be treated with some degree of skepticism. Cappetta (Reference Cappetta1987) states that Rhizoprionodon teeth do not exceed CH=4 mm; however, Purdy et al. (Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001) reported a range from CH=3.2–5.2 mm and CW=4.3–5.7 mm. Teeth of the Gatun Formation (CH=2.5–3.3 mm and CW=3.9–5.6 mm; Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a) are more closely aligned with those of the Chucunaque Formation. Rhizoprionodon previously has been reported from the middle and late Miocene of France, Belgium, and Portugal (Cappetta, Reference Cappetta1987). Carrillo-Briceño et al. (Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a) noted Rhizoprionodon as a small component (~4%; N=20) of the bathyal Piña Sandstone facies, but no occurrences in the neritic Rio Indio facies of the Chagres Formation. Extant individuals can be found worldwide in shallow, nearshore tropical and temperate waters (Compagno, Reference Compagno1984; Kent, Reference Kent1994). Rhizoprionodon terraenovae occurs at depths ranging from the intertidal zone to 280 m, but usually occur at depths less than 10 m (Compagno, Reference Compagno1984; Compagno et al., Reference Compagno, Dando and Fowler2005).

Family Sphyrnidae Gill, Reference Gill1872

Genus Sphyrna Rafinesque, Reference Rafinesque1810

Type

Squalus zygaena Linnaeus, Reference Linnaeus1758 (Cappetta, Reference Cappetta2012).

Sphyrna lewini (Griffith and Smith, Reference Griffith and Smith1834)

STRI 290109, STRI 300032, STRI 430011, STRI 430012, and YPA105.

Description

Moderately broad, labio-lingually flattened crown; convex to sigmoidal mesial edge and straight to concave distal edge. There is a distal inclination forming an acute notch with a rounded distal heel. The cutting edges and heel may or may not bear weak serrations. The root is thick with a transverse groove that penetrates a horizontal basal margin. Anterior teeth are more erect and lack the acute distal notch. Sphyrna zygaena from the Chucunaque Formation range from CH=2.6–8.1 mm and CW=4.8–9.6 mm.

Materials

Ninety-six isolated teeth; indeterminate position: UF 275044, UF 275058, UF 275073, UF 275142, UF 281175, and UF 281371–73.

Remarks

Sphyrna zygaena tend to have thicker, broader crowns and a more sigmoid mesial edge than Sphyrna lewini; however, the differences between the two species are sparse, especially in smaller individuals of S. zygaena. Compagno (Reference Compagno1988) noted that there is weak ontogenetic heterodonty in the genus Sphyrna. In juveniles and young adults of the extant S. zygaena, teeth have smooth cutting edges, but larger individuals become weakly serrate (Gilbert, Reference Gilbert1967). Gillette (Reference Gillette1984) originally identified S. zygaena from the Gatun Formation, however Pimiento et al. (Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a) reassigned these teeth to S. lewini (CH=2.7–5.4 mm and CW=5.2–11.0 mm) and Sphyrna sp. (CH=3.1–8.9 mm and CW=7.4–10.6 mm). Purdy et al. (Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001) reported teeth from the Pungo River Formation occurring in a size range of CH=8.0–11.0 mm, which corresponds with the larger teeth identified as S. zygaena from the Chucunaque Formation. Teeth from all three formations are much smaller than the upper limit of 20 mm reported by Cappetta (Reference Cappetta1987). Extant Sphyrna zygaena inhabit all temperate and tropical seas, and most commonly occur in coastal waters over continental shelves from depths of 0–200 m (Compagno et al., Reference Compagno, Ebert and Smale1989); however, it has been proposed that the distribution of S. zygaena in tropical environments is incompletely known due to probable confusion with S. lewini (Casper et al., Reference Casper, Domingo, Gaibor, Heupel, Kotas, Lamónaca, Pérez Jimenez, Simpfendorfer, Smith, Stevens, Soldo and Vooren2005).

Order Carcharhiniformes incertae sedis

Figure 8.1–8.11

Figure 8 Non-dental elements from the Chucunaque Formation. (1–11) Carcharhiniform centra: (1–4) UF 281195, posterior, anterior, ventral, and dorsal view, respectively (scale bar=1 cm); (5–7) UF 281196, anterior, posterior, and dorsal view, respectively (scale bar=1 cm); (8, 9) UF 281400: (8) indeterminate anterior-posterior face (scale bar=200 μm); (9) indeterminate dorsal-ventral face (scale bar=100 μm); (10, 11) UF 281399, indeterminate anterior-posterior face and indeterminate dorsal-ventral face, respectively (scale bar=100 μm). (12–14) Myliobatiformes incertae sedis: (12, 13) UF 281317, caudal spine in lateral and dorsal view, respectively (scale bar=1 mm); (14) UF 281499, caudal spine in dorsal view (scale bar=1 mm); (15, 16) Batomorphii incertae sedis, UF 281401, dermal denticle in apical and lateral view, respectively (scale bar=1 mm). Photo credit: S. Moran.

Occurrence

STRI 290139, STRI 290145, and YPA105.

Description

Scyliorhiniod-type (Tessman, Reference Tessman1966) vertebral centra with smooth dorsoventral edges and two sets of paired foramina; the caudal and cranial faces are concave with a circular to oval-shaped outline and distinct annuli, except in the smallest specimen (UF 281399). In lateral view, the centra have a cylindrical, disk-like to hourglass shape. Posterior vertebrae are more compressed than anterior positions (Kent, Reference Kent1994). The shape of the dorsal and ventral foramina, the presence or absence of septa, and the distribution of vertebral pores are diagnostic characteristics for identifying different genera (Kent, Reference Kent1994; Purdy et al., Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001). These centra can confidently be assigned to the order Carcharhiniformes because they lack the septate dorsoventral walls diagnostic for Lamniformes; however, they lack features that would allot for more specific identification. These centra range from a dorsoventral diameter of 1.27–33.56 mm and a wall length of 0.87–14.38 mm.

Materials

Four isolated vertebrae; indeterminate position: UF 281195–96 and UF 281399–400.

Remarks

Post-cranial elements are rare for chondrichthyan taxa. Typically the only non-dental remains recovered are vertebral centra because they are more densely calcified than the rest of the cartilaginous skeleton (Kent, Reference Kent1994). However, the morphologic variability in vertebral centra is more conservative than that of teeth, making it difficult to identify isolated specimens to genus or species. Purdy et al. (Reference Purdy, Schneider, Applegate, McLellan, Meyer and Slaughter2001) identified vertebrae of Hemipristis serra, Galeocerdo cf. G. cuvier, and Carcharhinus spp. based on dispersal of nutrient pores and the shape of dorsal and ventral foramen. Vertebrae from the Chucunaque Formation lack characteristics to warrant identification beyond Carcharhiniformes, in part because of their preservation, but mostly due to their inherent non-descript nature. Chondrichthyan vertebral centra have been recovered from the Eocene Tonosi Formation (Vasquez and Pimiento, Reference Vasquez and Pimiento2014) and the early Miocene Culebra Formation (Pimiento et al., Reference Pimiento, Gonzalez-Barba, Hendy, Jaramillo, MacFadden, Montes, Suarez and Shippritt2013b) of Panama. The four centra described here are the first chondrichthyan vertebral elements described from the late Miocene of Panama. Despite their lack of taxonomic information, vertebral centra can provide a lot of information about the individual from which they originated and the environment in which they resided. Vertebral centra have coupled growth bands, in which light bands represent growth during cold seasons and dark bands represent growth during warm seasons (Calliet et al., Reference Cailliet, Natanson, Welden and Ebert1985, Reference Cailliet, Radke and Welden1986, Reference Cailliet, Smith, Mollet and Goldman2006; Calliet and Goldman, Reference Cailliet and Goldman2004).

Subdivision Batoidea Compagno, Reference Compagno1973

Order Rajiformes Berg, Reference Berg1940

Family Rhynchobatidae Garman, Reference Garman1913

Genus Rhynchobatus Müller and Henle, Reference Müller and Henle1837

Type

Rhinobatus laevis Bloch and Schneider, Reference Bloch and Schneider1801 (Cappetta, Reference Cappetta2012).

Rhynchobatus sp.

Figure 9.1–9.3

Figure 9 Batoid I: Rhynchobatus, Urobatis, and Dasyatis SEM images from the Chucunaque Formation. (1–3) Rhynchobatus sp., UF 281314, indeterminate position in apico-lingual, baso-labial, and occlusal view, respectively; (4–6) Urobatis sp., UF 281316, indeterminate female tooth in lingual, baso-labial, and occlusal view, respectively; (7–11) Dasyatis sp.: (7–9) UF 281233, indeterminate female tooth in apico-lingual, baso-labial, and occlusal view, respectively; (10, 11) UF 281237, indeterminate male tooth in apico-lingual and labial view, respectively.

Occurrence

STRI 290116.

Description

In apical view, the crown is convex with a transverse crest dividing the lingual and labial faces. On the labial face, the crown is downward sloping with a well-defined uvula and secondary keel; there are foramina on the mesial and distal edges of the root. The lingual face is smooth with a high root that forms a distinct ridge at the crown-root contact; there is a prominent medial groove, with a foramen, that divides the root and lateral lobes on both the mesial and distal edges, giving the root a trilobate form (Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a). The dimensions of this specimen are a CW=4.17 mm, a CL=2.48 mm, and a CH=3.64 mm.

Materials

One isolated tooth; indeterminate position: UF 281314.

Remarks

The dimensions of this tooth are much larger than those reported from the Gatun Formation (length=0.9 mm, width=0.9 mm; Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a); however Compagno (1987) reported a CW of up to 5 mm for Rhynchobatus. Aguilera and Rodrigues de Aguilera (Reference Aguilera and Rodrigues De Aguilera2001) documented this genus from the Miocene of Venezuela. There are six extant species of Rhynchobatus that occur in the tropical and subtropical Indo-Pacific and a single species in the eastern Atlantic, R. luebberti (Compagno and Marshall, Reference Compagno and Marshall2006). Rhynchobatus luebberti is a benthic species often occurring in the intertidal zone, from 0–70 m depth, but most commonly found in less than 35 m depth (Compagno and Marshall, Reference Compagno and Marshall2006). Rhynchobatus djiddensis is a reef-associated species that occurs inshore and in shallow estuaries, generally between 2 and 50 m depth (Sommer et al., Reference Sommer, Schneider and Poutiers1996).

Six isolated tooth fragments; indeterminate position: UF 281225–26.

Remarks

Teeth of Aetobatus sp. can be distinguished from Rhinoptera by their lower crown, rounded and distally oriented extremities, and oblique root lobes that extend beyond the crown (Laurito and Valerio, Reference Laurito and Valerio2008). Aetobatus cf. A. narinari was reported from the Gatun Formation and was fairly common (N=22); however, only one specimen was a complete tooth with the following dimensions: CW=66.0 mm, CL=8.0 mm, and CH=4.5mm (Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a). In contrast, Aetobatus sp. from the Chucunaque Formation is fairly uncommon (N=6) and no complete specimens were recovered for an accurate size comparison. Aetobatus and Rhinoptera, as well as Myliobatis and Aetomylaeus, have dental plates that are formed by numerous interlocking teeth that comprise a large crushing surface primarily used to feed on mollusks and decapods (Compagno, Reference Compagno1997). Extant Aetobatus narinari has a cosmopolitan distribution in subtropical and tropical seas, commonly occurring in shallow waters between 1 and 60 m depth (Mundy, Reference Mundy2005).

Family Rhinopteridae Jordan and Evermann, Reference Jordan and Evermann1896

Genus Rhinoptera Kuhl in Cuvier, Reference Cuvier1829

Type

Myliobatis marginata Geoffroy Saint-Hilaire, 1809 (Cappetta, Reference Cappetta2012).

Rhinoptera sp.

Figure 10.4–10.15

Occurrence

STRI 290109, STRI 290116, STRI 300029, STRI 300032, and STRI 430011.

Description

Thick, elongate teeth with a smooth occlusal surface and hexagonal outline; fragmented tooth plates often have a rectangular outline. In cross-section, the enamel is comprised of vertical prisms that radiate outward from the pulp cavity, indicating extensional growth. Labial face bears a transverse platform, which interlocks with the lingual visor of the proceeding tooth (Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a). Symphyseal teeth interlock with smaller lateral teeth via their angular extremities (Cappetta, Reference Cappetta1987). In lateral teeth, the crown is thicker towards the mesial edge than the distal edge. Root is polyaulacorhizid with numerous lobes, fewer lobes in the smaller lateral teeth; the root is short relative to the crown. Rhinoptera sp. from the Chucunaque Formation has a CH=1.9–4.3 mm, CW=3.1–5.7 mm, and CL=6.4–16.4 mm.

Materials

Thirty-eight isolated teeth; 10 complete and 18 fragments; symphyseal: 281307; lateral: UF 281227, UF 281304, UF 281308, UF 281311, UF 281313; indeterminate position: UF 281302-281303, UF 281305–06, and UF 281309-281311.

Remarks

Rhinoptera can be distinguished from Aetobatus by its high crown and hexagonal outline with angular extremities. Rhinoptera is also often confused with Myliobatis; however, Rhinoptera differs in having a higher crown, a more angular occlusal surface, and a thicker lingual cingulum (Laurito and Valerio, Reference Laurito and Valerio2008). Myliobatis was not observed in the Chucunaque Formation, but has been reported from the Gatun Formation, along with Rhinoptera cf. R. steindachneri (Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a). The small, yet significant, relative abundance of Rhinoptera in the Gatun Formation (~4%) is comparable to that seen in the Chucunaque Formation (2.7%; Fig. 12). The size range of Rhinoptera teeth from the Gatun Formation (CH=3.0–5.0 mm, CW=3.0–26.0 mm, and CL=4.0–5.0 mm) is fairly close to that observed in Bayano. The significantly larger range in CW can likely be explained by the occurrence of a large symphyseal tooth in the Gatun Formation. Rhinoptera steindachneri occurs in tropical waters in the eastern Pacific, usually between 0 and 30 m depth (Humann and Deloach, Reference Humann and Deloach1993).

Family Mobulidae Gill, Reference Gill1893

Genus Mobula Rafinesque, Reference Rafinesque1810

Type

Mobula auriculata Rafinesque, Reference Rafinesque1810 (Cappetta, Reference Cappetta2012).

Mobula thurstoni (Lloyd, Reference Lloyd1908)

Figure 11.1–11.15

Order Myliobatiformes incertae sedis

Figure 8.12–8.14

Occurrence

YPA105.

Description

Fragmentary dorsoventrally compressed caudal spines. UF 281317 has four barbs that are directed toward the base of the spine. The barbs and dorsal surface are covered in an enameloid sheath. There is a nutrient pore beneath each of the barbs. The caudal spine fragment has a length of 4.50 mm and a width of 2.09 mm (Fig. 8.12, 8.13).

Materials

Two isolated caudal spine fragments: UF 281317 and UF 281499.

Remarks

It is difficult to identify complete caudal spines to the genus or species level, let alone a fragment of one. Pimiento et al. (Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a) described a single caudal spine from the Gatun Formation and attributed it to the genus Urobatis. Carrillo-Briceño et al. (Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a) reported a single caudal spine in both the neritic Rio Indio facies and the bathyal Piña Sandstone facies of the Chagres Formation, but was unable to identify either beyond Batomorphii. Schwartz (Reference Schwartz2007) analyzed 34 extant species of rays in search of diagnostic characters for stingray caudal spines. Characteristics taken into account were total spine length, pre-base length, number of serrations, presence of serrations on the spine base, and presence and size of a dorsal groove. Schwartz (Reference Schwartz2007) found that no single character was sufficient for identifying a spine, however an aggregate of all of these characters could elucidate the identity. The fragment described herein lacks sufficient characters to identify it beyond the order Myliobatiformes.

Superorder Batomorphii incertae sedis

Figure 8.15, 8.16

Occurrence

YPA105.

Description

A simple, slender dermal denticle with a reticulate dentine interior coated by an enameloid sheath. The basal plate is elongate and oval-shaped, forming a platform for a conical, posteriorly oriented apex. The dermal denticle has a basal length of 1.40 mm, basal width of 0.47 mm, and a height of 1.51 mm.

Materials

One isolated dermal denticle: UF 281401.

Remarks

Dermal denticles, or placoid scales, have a composition analogous to teeth with a pulp cavity, dentine interior, and enameloid exterior (Kent, Reference Kent1994); and it has been stated that teeth were evolutionarily derived from dermal denticles (Peyer, Reference Peyer1968). In sharks, dermal denticles tend to cover the entire body—aiding in hydrodynamics, acting as a predation deterrent, and reducing skin abrasion (Applegate, Reference Applegate1967; Reif, Reference Reif1988; Kent, Reference Kent1994). In stingrays, and some sharks, dermal denticles are often modified as a defensive measure (Kent, Reference Kent1994). The dermal denticle described herein is likely of this sort; in which it has been modified as a defensive thorn, lacking the flattened, fluted morphology typical of dermal denticles that primarily function for enhanced hydrodynamics. A number of batoids possess caudal thorns that are specialized for a defensive purpose, including Dasyatis. Typically, caudal thorns of Dasyatis have a stellate basal plate (Nair and Soundararajan, Reference Nair and Soundararajan1976; Silas and Selvaraj, Reference Silas and Selvaraj1985); however the morphology of dermal denticles can vary based on position in the body, throughout ontogeny, between sexes, between individuals, and between different species (Roberts and Karnasuta, Reference Roberts and Karnasuta1987). No other dermal denticles have been described from the fossil record of Panama, however this is likely due to a collection bias given their extremely small size and relatively delicate form.

Discussion

Taxonomic composition

In total, 1422 dental remains revealed at least 31 different chondrichthyan taxa (Table 3), 23 of which belong to the subdivision Selachii (modern sharks) and 8 of which belong to the subdivision Batomorphii (skates, rays, and sawfish). There are five orders consisting of 12 families and 19 genera (Fig. 12). Seven non-dental remains were also described, including four vertebral centra, one dermal denticle, and two fragmentary caudal spines. At least 15 of the 31 taxa identified represent extant species (Table 3), confirming that the late Miocene chondrichthyans are long-lived species. Also, among the 31 taxa recognized, at least eight are new records for the fossil record of Panama (Table 3).

Figure 12 Relative abundance of chondrichthyan genera from the Chucunaque Formation.

There is undoubtedly some degree of bias in the sample, whether it is due to collection, preservation, or identification. The best way to reduce the potential bias is with a large sample size, and the sample described herein (N=1422) is the largest reported from Panama to date. Furthermore, our sampling efforts, as exhibited in randomized species accumulation curves (Fig. 2) indicate that it is unlikely that more collecting (either surface prospecting or screewhasing) will result in many additional taxa. Hence, the sample utilized in this study comprises an accurate representation of the chondrichthyan biodiversity present in the Chucunaque Formation. There are three additional marine Miocene formations from Panama that have documented chondrichthyan remains: the early Miocene Culebra Formation with 12 taxa represented by 45 dental remains and 10 vertebral centra (Pimiento et al., Reference Pimiento, Gonzalez-Barba, Hendy, Jaramillo, MacFadden, Montes, Suarez and Shippritt2013b); the middle–late Miocene Gatun Formation with 26 taxa represented by 800 dental remains (Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a); and the late Miocene Chagres Formation with 30 taxa represented by 513 dental remains (Carrillo-Briceño et al., Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a). The 1422 teeth collected and 31 taxa described herein from Lago Bayano comprise the most prolific and diverse chondrichthyan fauna known from Panama. Despite significant collection effort, all of these samples are subject to some degree of collection bias, and likely taphonomic bias. As such, proportions are reported to aid in the juxtaposition of these faunas, but should still be interpreted with caution.

Carcharhinus is by far the most abundant genus present in the Chucunaque Formation, representing over 50% of specimens identified (Fig. 12). Species of the genus Carcharhinus are the most abundant and diverse sharks in modern nearshore environments, with over 30 different species attributed to this genus (Compagno, Reference Compagno1984; Kent, Reference Kent1994; Naylor and Marcus, Reference Naylor and Marcus1994). Carcharhinus is also the most abundant genus represented in the Gatun Formation (~40%; Pimiento et al., 2013) and tied with Hemipristis as the most abundant genus in the Rio Indio Member of the Chagres Formation (~32%; Carrillo-Briceño et al., Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a). In contrast, the deeper water Piña Sandstone facies of the Chagres Formation is dominated by species within the order Squaliformes, with only ~11% of the chondrichthyan fauna being represented by the genus Carcharhinus (Carrillo-Briceño et al., Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a).

The second most abundant genus in the Chucunaque Formation is Mobula (~12%; Fig. 12). Mobulids (Mobula and Manta rays) are the largest stingrays alive today, and typically have a pelagic, coastal habit in tropical and sub-tropical waters (Notarbartolo Di Sciara, Reference Notarbartolo Di Sciara1987; Adnet et al., Reference Adnet, Cappetta, Guinot and Notarbartolo Di Sciara2012). Mobula has been recognized from the Gatun Formation of Panama, but is much less abundant (~1%; Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a). The paucity of Mobula in the paleontology literature can likely be attributed to preservation and collection bias. Mobula teeth are extremely small and have a very thin enameloid, and yet they are very common in the Chucunaque Formation. Increased screenwashing efforts in other tropical and sub-tropical Neogene localities may reveal more Mobula occurrences.

Functional diversity

Six of the nine dentition types described by Kent (Reference Kent1994) were observed: cutting, crushing, clutching, vestigial, cutting-grasping, and grasping-cutting (Table 3; Fig. 13.1). The generalist, cutting-grasping type dentition was the most prevalent, being represented by ~69% of the total sample. This dentition type is the most common today, and it allows for a wide variety of prey options, but it is most commonly found among sarcophagous (i.e., those eating fleshy prey such as bony fishes and marine mammals) and ichthyophagous (those eating fish) sharks (Kent, Reference Kent1994). The second most common dentition type is the vestigial form (~12%), which is essentially a specialized tooth form for filter feeding, reflecting a planktivorous diet (Kent, Reference Kent1994). This dentition type is represented by species within the genus Mobula. However, teeth of Mobula are not solely for filter feeding, but also possess some characteristics indicative of clutching and/or grinding. It has even been suggested that Mobula teeth may play a role during reproduction (Michael, 1993). Third is the clutching type (~7%), which is more typical of small to moderately sized sharks that primarily feed on small fishes and hard-bodied, benthic taxa (i.e., crustaceans, molluscs, and echinoids) by grabbing and gripping their prey with powerful shortened jaws (Kent, Reference Kent1994). The fourth and fifth most common dentition types are the cutting type and the crushing type, both comprising 5.75% of the specimens identified. The cutting type is adapted for sarcophagous taxa (Kent, Reference Kent1994). The crushing type is a specialized form for feeding on armored benthic invertebrates (i.e., durophagous), such as molluscs and crustaceans, and is most typically found in bottom-dwelling taxa (Kent, Reference Kent1994). Lastly, a very small portion, 0.5%, had a grasping-cutting type dentition, which is represented by taxa in the genus Isurus. This dentition type relies more on capturing rather than dismembering the prey, which may be a more effective feeding strategy when operating in open water and feeding on more active prey items. Kent (Reference Kent1994) attributed this dentition type to ichthyophagous and teuthyophagous (i.e., those feeding on squid) sharks. It is also worth noting the absence of any taxa that have solely a grasping type dentition, such as Carcharias, which is a relatively common genus in Miocene deposits and in modern nearshore environments. In fact, among the four chondrichthyan-bearing Miocene deposits in Panama, only one tooth identified as Carcharias has been reported from the Chagres Formation (Carillo-Briceño et al., 2015a).

Figure 13 Two proxies for functional diversity. (1) Relative abundance of different dentition types as described by Kent (Reference Kent1994); (2) Relative abundance of different ecomorphotypes as described by Compagno (Reference Compagno1990).

Furthermore, there were 12 ecomorphotypes represented by the chondricthyan fauna of Lago Bayano, most of which represent littoral taxa (Table 3; Fig. 13.2). The littoral ecomorphotype refers to relatively non-specialized taxa that inhabit continental shelves and feed on moderately sized prey comprised of bony fishes, crustaceans, and cephalopods, among other organisms (Compagno, Reference Compagno1990). Within the littoral habitus there are more specialized ecomorphotypes, including the cancritrophic (demersal sharks primarily feeding on bottom dwelling crustaceans), teuthitrophic (diet primarily consisting of cephalopods), sphyrnid (littoral to semilittoral with a specialized cephalofoil bowplane), eurytrophic (omnivores trending toward apex predator), and archipelagic (apex predators), that were also observed (Table 3; Fig. 13.2). Compagno (Reference Compagno1990) grouped the eagle rays and cownose rays (Myliobatidae) with the devilrays (Mobulidae) into the aquilopelagic habitus because of their pectoral-driven locomotion, despite their very different feeding adaptations (Adnet et al., Reference Adnet, Cappetta, Guinot and Notarbartolo Di Sciara2012). The aquilopelagic habitus represents ~15% of the chondrichthyan fauna from the Chucunaque Formation. The oceanic habitus (~1.5%) is represented by three ecomorphotypes: macroceanic, tachypelagic, and microceanic. The remaining taxa are batoids placed in the rajobenthic (~1.5%) and rhynchobathic (<0.1%) ecomorphotypes. Based on our functional diversity analyses, the ecosystems of Lago Bayano were dominated by generalist taxa that lived in nutrient-rich waters with abundant zooplankton.

Paleobathymetry

The weighted paleobathymetry method was applied to the chondrichthyan fauna of the Chucunaque Formation, as well as the Gatun Formation and the Piña Sandstone facies of the Chagres Formation. For the Chucunaque Formation, 15 species of the 31 total taxa were included, which were represented by 525 specimens (37% of the total number of material collected). For the Gatun Formation, 17 of the 26 taxa identified by Pimiento et al. (Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a) were included, which represented ~32% (N=257) of the specimens identified. For the Piña Sandstone facies of the Chagres Formation, 12 of the 28 taxa identified by Carrillo-Briceño et al. (Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a) were included, which represented ~14% (N=70) of the specimens identified. This paleobathymetry method was not tested on the Rio Indio facies of the Chagres Formation because the chondrichthyan fauna therein is comprised of only four taxa identified to the species level that have modern analogs (Carrillo-Briceño et al., Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a).

Our results (Table 4; Fig. 14) show that the Chucunaque Formation was most likely deposited in a neritic environment (mean depth of 110 m). Previous studies (see Coates et al., Reference Coates, Collins, Aubry and Berggren2004) proposed that this formation was deposited in the inner-neritic to upper-bathyal zone at different localities, based on benthic foraminiferal asssemblages. Variability in paleobathymetry throughout the Neogene succession and within individual sections was thought to correspond to spatial and temporal differences in sediment deposition and basin tectonics. Nevertheless, the river outcrops surveyed by Coates et al. (Reference Coates, Collins, Aubry and Berggren2004) were deposited in adjacent sedimentary basins (Chucunaque-Tuira and Sambu), whereas Lago Bayano resides on the western margin of the Bayano Basin, which likely experienced reduced subsidence and less accommodation space. Therefore there is little issue with the chondrichthyan fauna indicating a neritic environment for the Chucunaque Formation of Lago Bayano.

Figure 14 Paleobathymetric estimates for the Chucunaque Formation, Gatun Formation, and the Piña Sandstone facies of the Chagres Formation, showing the mean average depth. Depth ranges used in this analysis can be found in the Systematic Paleontology section as well as in Table 3.

Table 4 Results of the weighted paleobathymetric analysis. Min and max values represent 95% confidence intervals. Previous estimates are based on Pimiento et al. (Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a) for the Gatun and Carrillo-Briceño et al. (Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a) for the Piña Sandstone facies of the Chagres Formation.

Similar to the Chucunaque Formation, the Gatun was deposited in a neritic environment (mean depth of 55 m), whereas the Piña Sandstone facies was deposited within the upper bathyal zone (mean depth of 370 m). The Chucunaque Formation and the Gatun Formation are both dominated by the order Carcharhiniformes (~78% and ~83%, respectively), which is the most diverse and abundant group alive today in nearshore environments (Compagno, Reference Compagno1990; Kent, Reference Kent1994). In contrast, the deeper water Piña Sandstone facies of the Chagres Formation is dominated by the order Squaliformes (~70%). The most abundant taxon identified from the Chagres Formation, Isistius sp. (N=272), was not included in the paleobathymetric analysis because it was only identified to the generic level, and hence the depth range can only be inferred from the different living species within this genus or via other fossil occurrences. Carrillo-Briceño et al. (Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a) reported that Isistius (~70% of the Piña Sandstone facies) occurs at depths of 0–3700 m, usually between 0 and 1000 m, based on the extant species Isistius brasiliensis; however, they also noted that other living species of Isistius prefer shallow water and even make daily vertical migrations through the water column. If the preferred depth of I. brasiliensis were used as a proxy, its inclusion would have increased the mean average to ~470 m, but the estimate would still remain in the bathyal zone. The estimate for the Piña Sandstone facies is deeper than what was determined by Carrillo-Briceño et al. (Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a) based on chondrichthyan evidence alone. However, Collins et al. (Reference Collins, Coates, Berggren, Aubry and Zhang1996) reported that the Chagres Formation was deposited in 200–500 m depth based on foraminiferal assemblages. Therefore, the depth inferred herein for the Piña Sandstone facies of the Chagres Formation would still fall within the range predicted by Collins et al. (Reference Collins, Coates, Berggren, Aubry and Zhang1996) and is permissible given the presence of other deep-water taxa such as whales and billfishes (Uhen et al., Reference Uhen, Coates, Jaramillo, Montes, Pimiento, Rincon, Strong and Velez-Juarbe2010; Carrillo-Briceño et al., Reference Carrillo-Briceño, De Gracia, Pimiento, Aguilera, Kindlimann, Santamarina and Jaramillo2015a; Velez-Juarbe et al., Reference Velez-Juarbe, Wood, De Gracia and Hendy2015).

Despite the fact that both the Chucunaque Formation and the Gatun Formation are interpreted as having been deposited in the neritic zone, the paleobathymetric prediction for the Chuncunaque Formation is nearly twice as deep as the Gatun Formation. This can be explained by the presence of pelagic taxa such as Isurus and Alopias in the Chucunaque Formation, which are absent in the Gatun Formation (Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a). Furthermore, there are at least six taxa from the Chucunaque Formation (Isurus oxyrinchus, Alopias superciliosus, Alopias cf. A. vulpinus, Carcharhinus falciformis, Carcharhinus obscurus, and Sphyrna lewini), comprising 15% of the chondrichthyan fauna, that have depth ranges beyond the neritic zone (Table 3). The presence of these taxa may indicate the influence of deeper oceanic waters in the Bayano Basin (e.g., via upwelling systems) or may be explained by the migratory habits of these sharks. Many oceanic species migrate to shallow, coastal waters to give birth (Compagno, Reference Compagno1984, Reference Compagno1998; Bass et al., Reference Bass, Heemstra and Compagno1986; Mundy, Reference Mundy2005), which aids in reducing competition between juveniles and adults, and may help to prevent cannibalism (Compagno, Reference Compagno1990). Likewise, Carrillo-Briceño et al. (Reference Carrillo-Briceño, Aguilera and Rodriguez2014) recognized a chondrichthyan fauna, from the middle Miocene to early Pliocene of Ecuador, indicating a shallow- to deep-water assemblage and suggested that it may reflect a short platform environment bordered by deep water. The late Miocene Curré Formation (Laurito and Valerio, Reference Laurito and Valerio2008) from Costa Rica bears a sparse chondrichthyan assemblage (N=89), relative to the Chucunaque Formation; however the two faunas are similar given that both are dominated by the order Carcharhiniformes, but also contain the genus Isurus. Laurito and Valerio (Reference Laurito and Valerio2008) inferred a neritic depth based on the chondrichthyan fauna and suggested that the depth is likely less than 35 m based on the occurrence of Pholididae traces. The presence of deep-water taxa along the Pacific Shelf of Costa Rica, Panama, and Ecuador during the late Miocene supports the idea of a proximal open ocean environment influencing the neritic Chucunaque Formation.

Our estimates presented here are a reflection of the taxonomic composition of the three localities studied and are in agreement with previous studies. However, there are obvious limitations to this method; namely, ignoring a large number of specimens either due to an inability to identify to the species level or because the species is extinct and lacks a modern analog to constrain its depth prefence. Further, there is undoubtedly some degree of preservational and/or collection bias, either due to uneven sampling efforts between screenwashed and surface collected material, or as an unavoidable result of thanatocoenosis (i.e., accumulation and deposition after death), as was suggested by Cappetta and Nolf (Reference Cappetta and Nolf1991) in their paleobathymetric analysis. Even so, using the subsample of taxa that do have modern analogs and taking into account their relative abundance offers a quantitative, probabilistic approach that in theory will provide a more accurate paleodepth estimate. Likewise, Carrillo-Briceño et al. (Reference Carrillo-Briceño, Argyriou, Zapata, Kindlimann and Jaramillo2015c) employed a similar probabilistic approach using maximum likelihood estimation to predict the paleobathymetry of the Miocene Uitpa Formation in Colombia based on chondrichthyan occurrences.

Paleobiogeography

The chondrichthyan fauna from the Gatun Formation has mixed biogeographic affinities, with evidence of taxa currently restricted to the Atlantic including Carcharhinus perezi, Rhynchobatus luebberti, Mobula hypostoma, and Taeniurops aff. T. grabata and Pacific-restricted taxa including Myliobatis cf. M. californica, Rhinoptera cf. R. steindachneri, and Mobula munkiana (Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a). Of the 15 extant taxa observed from the Chucunaque Formation, all occur in both the Atlantic and the Pacific oceans today, with the possible exception of C. aff. macloti, given that extant C. macloti is restricted to the Pacific. Also, it is possible that the Type II Mobula teeth observed in the Chucunaque Formation actually belong to Mobula hypostoma, which would mean that there is an Atlantic-restricted species on the Pacific side of the evolving Panamanian isthmus. If even one of these species were accurately identified as representing a species that is currently restricted to the opposing side of the isthmus, it would support the hypothesis that there was a continued marine connection between 9 Mya and 10 Mya.

The Chucunaque Formation of Lago Bayano is roughly contemporaneous with the upper part of the Gatun Formation (Hendy, Reference Hendy2013; Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a). The Gatun Formation of the Panama Canal Basin is considered to have had a Caribbean affinity based on benthic foraminiferal assemblages (Collins et al., Reference Collins, Coates, Berggren, Aubry and Zhang1996), whereas the Chucunaque Formation of the Bayano Basin has been interpreted as having a Pacific affinity (Coates et al., Reference Coates, Collins, Aubry and Berggren2004). The two distinct foram assemblages have been utilized to interpret restriction of deep-water circulation by ~8 million years ago; however, this deep-water connection is thought to have returned ~6 million years ago based on Pacific foraminifera in the bathyal Chagres Formation (Collins et al., Reference Collins, Coates, Berggren, Aubry and Zhang1996). Despite the fact that there was, likely, ongoing shoaling of the Isthmus of Panama and restriction of deep-water circulation (Montes et al., Reference Montes, Bayona, Cardona, Bush, Silva, Moron, Hoyos, Ramirez, Jaramillo and Valencia2012a, Reference Montes, Cardona, Bayona, McFadden, Buchs, Morón, Silva, Hoyos, Restrepo-Moreno, Ramírez, Wilson, Ortiz, Farris, Jaramillo, Valencia, Bryan and Flores2012b; Sepulchre et al., Reference Sepulchre, Arsouze, Donnadieu, Dutay, Jaramillo, Le Bras, Martin, Montes and Waite2014), there must have still remained a marine connection between the Caribbean Sea and Pacific Ocean ~10 million years ago to allow for exchange of marine vertebrates (Pimiento et al., Reference Pimiento, González-Barba, Ehret, Hendy, MacFadden and Jaramillo2013a). Sepulchre et al. (Reference Sepulchre, Arsouze, Donnadieu, Dutay, Jaramillo, Le Bras, Martin, Montes and Waite2014) incorporated neodymium isotopic data into a model in order to resolve the history of water masses connecting the Pacific to the Caribbean, and found that a seaway 50–200 m deep would likely have been present ~10 million years ago, which is consistent with the depth estimates for the Gatun and Chucunaque Formations, derived from the weighted paleobathymetric analysis (Table 4; Fig. 14).

The Lago Bayano fauna is therefore highly significant because it represents the first described Miocene chondrichthyan fauna from the Pacific shelf of Panama. The only other Miocene chondrichthyan faunas that have been described from the Pacific shelf of the evolving Central American isthmus are from the middle Miocene Punta Judas Formation (Laurito, Reference Laurito2004) and the late Miocene Curré Formation (Laurito and Valerio, Reference Laurito and Valerio2008) from Costa Rica. The Curré Formation was tentatively assigned as being late Miocene because of the occurrence of chondrichthyan taxa typical of the Miocene and terrestrial mammal remains (Laurito and Valerio, Reference Laurito and Valerio2005, Reference Laurito and Valerio2008; Valerio and Laurito, Reference Valerio and Laurito2008). The co-occurrence of terrestrial taxa as well as marine fauna in the Curré Formation is very similar to that of the late Miocene Alajuela Formation (MacFadden et al., Reference MacFadden, Morgan, Jones and Rincon2015, Reference MacFadden, Jones, Jud, Moreno, Morgan, Portell, Perez, Moran and Wood2017), providing evidence that at least some emergent land was present within the Central American isthmus. Coates and Obando (Reference Coates and Obando1996) reconstructed the CAS during the late Miocene as an archipelagic strait on the basis of tectonic evidence and nannofossil assemblages. Alternatively, it has been proposed that a continuous peninsula connected Panama to North America as early as 19 million years ago, based on comparable body sizes between contemporaneous land mammals found in North America and Panama (Kirby and MacFadden, Reference Kirby and MacFadden2005; Kirby et al., Reference Kirby, Jones and MacFadden2008). However, neither reconstruction excludes the notion of a marine connection between the Pacific Ocean to the Caribbean Sea throughout the Miocene.

After uplift of the Isthmus of Panama and complete closure of the CAS many taxa had populations in both the Pacific and Atlantic, with a few species becoming restricted to either side. With the information available we cannot yet ascertain if the reason these taxa became restricted is due to the closure of the CAS, but it is highly probable that the uplift of the Isthmus of Panama was a contributing factor. Given that chondrichthyan taxa are highly mobile, and that many are capable of trans-oceanic migrations, it is possible that they could continue to exchange between the Pacific and Atlantic via a meridional route after complete closure of the CAS. However, temperature restrictions would make this unlikely. A more reasonable explanation for the co-occurrence of Atlantic-restricted and Pacific-restricted taxa between 9 and 10 million years ago is that there was in fact a marine connection between the Caribbean Sea and the Pacific Ocean.

Conclusion

This overview of the chondrichthyan fauna from the late Miocene Chucunaque Formation reveals the most prolific and diverse assemblage from Panama, with at least 31 taxa, eight of which are new to the fossil record of Panama. Furthermore, the Lago Bayano fauna is the first described Miocene chondrichthyan assemblage from the Pacific shelf of the Panamanian isthmus, and ⁸⁷Sr/⁸⁶Sr isotopic ratios reported provide the first geochronology for the region. At least 15 of the taxa identified have affinities with extant species, which offers the opportunity to utilize the habitat preferences of the corresponding living species to make inferences regarding functional diversity, paleoenvironment, and paleobiogeography. The Bayano ecosystems are dominated by generalist sharks (with cutting-grasping type dentitions) and filter-feeding rays. A weighted paleobathymetric analysis provides evidence for a paleoenvironment in the neritic zone, with a mean average estimate of 110 m. Finally, the geographic ranges of the fauna indicate mixed geographic affinity, which offers insight into a marine connection between the Caribbean Sea and the Pacific Ocean during a time of active shoaling in Central America.

Acknowledgments

This work was funded by U.S. National Science Foundation (NSF) grant 0966884 (OISE, EAR, DRL), 1358919 (EAR, OISE), and the Smithsonian Tropical Research Institution (STRI). We appreciate additional funding, in-kind support, and field assistance by C. Jaramillo, C. Montes, D. Ramirez, C. Suarez, L. Londoño, and V. Zapata (STRI), and R. Portell (FLMNH). We also acknowledge the generosity and guidance of the local Embrerá at Puente Bayano, in particular N. Ortega and S. Quiroz. In addition, R. Perez is acknowledged for donating the Toyota vehicles used for fieldwork, and the Dirección de Recursos Minerales are thanked for providing collecting permits. We thank R. Leder and S. Moran for help with macro photographs. We also appreciate the assistance from A. Heatherington with SEM images, D. Jones, G. Kamenov, and A. Waite for their help with the Sr-isotope analyses, the insightful comments of J. Carrillo-Briceño, as well as guidance on statistical methods (especially developing the R code for the bathymetric analyses) provided by M. Kowaleski. A Forschungskredit postdoctoral fellowship from the University of Zürich (FK-15-105) supported C.P. This is a contribution of the NSF Partnerships for International Research and Education Panama Canal Project and the University of Florida Contribution to Paleobiology number 762.

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Table 2 Strontium isotope data and age estimates from the Chucunaque Formation of Lago Bayano.

Table 3 Complete taxonomic list of the chondrichthyes of Lago Bayano, including a summary of all relevant data for the subsequent analyses. References for common depth ranges and biogeographic affinity (i.e., Atlantic vs. Pacific) can be found in the Systematic Paleontology section, ecomorphotypes are based on Compagno (1990), and descriptions of dentition types can be found in Kent (1994). * indicates a new taxon for the fossil record of Panama. † indicates an extinct species.

Figure 3 SEM images of specimens belonging to the subdivision Selachii. (1, 2) Centrophorus sp., UF 281349, lower anterolateral tooth in lingual and labial view, respectively; (3–6) cf. Iago sp.: (3, 4) UF 281382, lateral tooth in lingual and labial view, respectively; (5, 6) UF 281383, anterolateral tooth in lingual and labial view, respectively; (7–9) Mustelus sp., UF 281384, indeterminate position in occlusal, lingual, and baso-labial view, respectively; (10–13) Mustelus sp., UF 281386, indeterminate position in occlusal, basal, lingual, and labial view, respectively; (14–19) Physogaleus sp.: (14, 15) UF 281354, upper lateral tooth in lingual and labial view, respectively; (16, 17) UF 281353, anterior tooth in lingual and labial view, respectively; (18, 19) UF 281351, indeterminate position in lingual and labial view, respectively; (20, 21) Carcharhinus sp., UF 281338, pathologic upper tooth in lingual and labial view, respectively.

Figure 4 Lamniformes: Carcharocles, Isurus, and Alopias from the Chucunaque Formation. (1–5) Carcharocles megalodon (Agassiz, 1843): (1, 2) UF 275110, upper right anterior (most complete tooth) in lingual and labial view, respectively (scale bar=5 cm); (3–5) UF 275108, upper tooth bearing a vestigial lateral cusplet in lingual, labial, and lateral view, respectively (scale bar=5 cm); (6–16) Isurus oxyrinchus (Rafinesque, 1810): (6–8) UF 275124, lower right lateral in lingual, labial, and distal lateral view, respectively (scale bar=1 cm); (9–12) UF 281169, upper left lateral in lingual, labial, mesial lateral, and distal lateral view, respectively (scale bar=1 cm); (13–16) UF 281181, upper lateral tooth in lingual, labial, distal lateral, and mesial lateral view, respectively (scale bar=1 cm); (17–20) Alopias superciliosus (Lowe, 1840), UF 275057, lower position in lingual, labial, distal lateral view, and mesial lateral, respectively (scale bar=1 cm); (21–24) Alopias cf. A. vulpinus (Bonnaterre, 1788), UF 281321, upper position in lingual, labial, mesial lateral, and distal lateral view, respectively (scale bar=1 cm). Photo credit: S. Moran and R. Leder.

Figure 5 Carcharhiniformes I: Hemipristis, Galeocerdo, and Physogaleus from the Chucunaque Formation. (1–16) Hemipristis serra Agassiz, 1843: (1–4) UF 281404, upper anterior tooth in lingual, labial, distal lateral, and mesial lateral view, respectively; (5–8) UF 281174, upper lateral tooth in lingual, labial, distal lateral, and mesial lateral view, respectively; (9–12) UF 281396, upper symphyseal tooth in lingual, labial, distal lateral, and mesial lateral view, respectively; (13–16) UF 281405, lower lateral tooth in lingual, labial, mesial lateral, and distal lateral view, respectively; (17–20) Galeocerdo aduncus (Agassiz, 1835), UF 275083, indeterminate position in lingual, labial, mesial lateral, and distal lateral view, respectively; (21–28) Galeocerdo cuvier (Peron and Lesueur, 1822): (21–24) UF 281397, indeterminate position in lingual, labial, distal lateral, and mesial lateral view, respectively; (25–28) UF 275145, indeterminate position in lingual, labial, distal lateral, and mesial lateral view, respectively; (29–32) Physogaleus contortus (Gibbes, 1849), UF 281170, indeterminate position in lingual, labial, mesial lateral, and distal lateral view, respectively. Photo credit: R. Leder.

Figure 6 Carcharhiniformes II: Carcharhinus from the Chucunaque Formation. (1–4) Carcharhinus falciformis (Bibron, 1841 in Muller and Henle, 1839–1841), UF 281162, upper tooth in lingual, labial, distal lateral, and mesial lateral view, respectively (scale bar=1 cm); (5–7) Carcharhinus brevipinna (Blainville, 1816), UF 281159, upper tooth in lingual, labial, and distal lateral view, respectively (scale bar=1 cm); (8–13) Carcharinus aff. C. macloti (Müller and Henle, 1839): (8, 9) UF 281323, upper anterior tooth in lingual and labial view, respectively (scale bar=0.5 cm); (10) UF 281325, upper lateral in lingual view (scale bar=0.5 cm); (11–13) UF 275061, upper lateral tooth in lingual, labial, and mesial lateral view, respectively (scale bar=1 cm); (14–20) Carcharhinus obscurus (Lesueur, 1818): (14–16) UF 281147, upper tooth in lingual, labial, and distal lateral view, respectively (scale bar=1 cm); (17–20) UF 281152, lower tooth in lingual, labial, mesial lateral, and distal lateral view, respectively (scale bar=1 cm); (21–24) Carcharhinus plumbeus (Nardo, 1827), UF 281143, upper tooth in lingual, labial, mesial lateral, and distal lateral view, respectively (scale bar=1 cm); (25–49) Carcharhinus sp.: (25–28) UF 281165, upper anterior tooth in lingual, labial, distal lateral, and mesial lateral view, respectively (scale bar=1 cm); (29–32) UF 281348, upper anterior tooth in lingual, labial, distal lateral, and mesial lateral view, respectively (scale bar=1 cm); (33–36) UF 275141, lower anterior tooth in lingual, labial, distal lateral, and mesial lateral view, respectively (scale bar=1 cm); (37–39) UF 275141, lower lateral tooth in lingual, labial, distal lateral, and mesial lateral view, respectively (scale bar=1 cm); (40–42) UF 281164, lower posterior tooth in lingual, labial, distal lateral view, respectively (scale bar=1 cm); (43–46) UF 281182, lower posterior tooth in lingual, labial, mesial lateral, and distal lateral view, respectively (scale bar=1 cm); (47) UF 281402, upper pathologic tooth in lingual view; (48) UF 281167, upper pathologic tooth in lingual view (scale bar=1 cm); (49) UF 281168, upper pathologic tooth in apical view (scale bar=1 cm). Photo credit: R. Leder.

Figure 7 Carcharhiniformes III: Negaprion, Rhizoprionodon, and Sphyrna from the Chucunaque Formation. (1–4) Negaprion brevirostris (Poey, 1868), scale bar=1 cm: (1, 2) UF 275080, upper left lateral tooth in lingual and labial view, respectively; (3, 4) UF 275080, lower tooth in lingual and labial view, respectively; (5–8) Rhizoprionodon sp., scale bar=0.5 cm: (5, 6) UF 322848, indeterminate position in lingual and labial view, respectively; (7, 8) UF 322849, indeterminate position in lingual and labial view, respectively; (9–12) Sphyrna lewini (Griffith and Smith, 1834), UF 281176, upper position in lingual, labial, mesial lateral, and distal lateral view, respectively (scale bar=1 cm); (13–18) Sphyrna mokarran (Ruppell, 1837): (13–16) UF 275043, upper position in lingual, labial, mesial lateral, and distal lateral view, respectively, (scale bar=1 cm); (17, 18) UF 275066, upper lateral tooth in lingual and labial view, respectively (scale Bar=0.5 cm); (19–26) Sphyrna zygaena, scale bar=1 cm: (19–22) UF 275073, upper lateral tooth in lingual, labial, mesial lateral, and distal lateral view, respectively; (23–26) UF 275073, lower anterior tooth in lingual, labial, distal lateral, and mesial lateral view, respectively. Photo credit: R. Leder.

Figure 8 Non-dental elements from the Chucunaque Formation. (1–11) Carcharhiniform centra: (1–4) UF 281195, posterior, anterior, ventral, and dorsal view, respectively (scale bar=1 cm); (5–7) UF 281196, anterior, posterior, and dorsal view, respectively (scale bar=1 cm); (8, 9) UF 281400: (8) indeterminate anterior-posterior face (scale bar=200 μm); (9) indeterminate dorsal-ventral face (scale bar=100 μm); (10, 11) UF 281399, indeterminate anterior-posterior face and indeterminate dorsal-ventral face, respectively (scale bar=100 μm). (12–14) Myliobatiformes incertae sedis: (12, 13) UF 281317, caudal spine in lateral and dorsal view, respectively (scale bar=1 mm); (14) UF 281499, caudal spine in dorsal view (scale bar=1 mm); (15, 16) Batomorphii incertae sedis, UF 281401, dermal denticle in apical and lateral view, respectively (scale bar=1 mm). Photo credit: S. Moran.

Figure 9 Batoid I: Rhynchobatus, Urobatis, and Dasyatis SEM images from the Chucunaque Formation. (1–3) Rhynchobatus sp., UF 281314, indeterminate position in apico-lingual, baso-labial, and occlusal view, respectively; (4–6) Urobatis sp., UF 281316, indeterminate female tooth in lingual, baso-labial, and occlusal view, respectively; (7–11) Dasyatis sp.: (7–9) UF 281233, indeterminate female tooth in apico-lingual, baso-labial, and occlusal view, respectively; (10, 11) UF 281237, indeterminate male tooth in apico-lingual and labial view, respectively.

Figure 10 Batoid II: Aetobatus and Rhinoptera images from the Chucunaque Formation. (1–3) Aetobatus sp., UF 281226, distal tooth fragment in occlusal, basal, and lateral view, respectively; (4–15) Rhinoptera sp.: (4–7) UF 281307, symphyseal (i.e., medial) tooth in occlusal, basal, lingual, and lateral view, respectively; (8) UF 281309, cross-section in lateral view; (9–11) UF 281308, lateral (i.e., intermediate) tooth in occlusal, basal, and lingual view, respectively; (12–15) UF 281304, lateral (i.e., distal) tooth in occlusal, basal, lingual, and labial view, respectively (scale bars=5 mm). Photo credit: S. Moran.

Figure 11 Batoid III: Images of Mobula teeth from the Chucunaque Formation. (1–15) Mobula thurstoni (Lloyd, 1908): (1–5) UF 281291, lateral tooth in occlusal, lingual, labial, basal, and profile view, respectively; (6–10) UF 281292, anterolateral tooth in occlusal, lingual, labial, basal, and lateral view, respectively; (11–13) UF 281256, SEM image of a left lateral tooth in occlusal, lingual, and labial view, respectively; (14, 15) UF 281283, SEM image of a lateral tooth in occlusal and lateral view, respectively; (16–25) Mobula cf. M. tarapacana (Phillippi, 1893): (16–20) UF 281270, lateral male tooth in occlusal, lingual, labial, basal, and lateral view, respectively; (21–25) UF 281289, lateral female tooth in occlusal, lingual, labial, basal, and lateral view, respectively; (26–50) Mobula sp.: (26–31) Type I: (26, 27) UF 281279, SEM image of a lateral tooth in occlusal and lateral view, respectively; (28–30) UF 281280, SEM image of an anterior tooth in occlusal, lingual, and labial view, respectively; (31) UF 281287, SEM image of a indeterminate tooth position in occlusal view; (32–45) Type II: (32, 33) UF 281243, SEM image of an anterior tooth in occlusal and lateral view, respectively; (34, 35) UF 281241, SEM image of an anterior tooth in occlusal and lateral view, respectively; (36–38) UF 281251, SEM image of an aneterior male tooth in occlusal, lingual, and lateral view, respectively; (39, 40) UF 281253, SEM image of a lateral male tooth in occlusal and lateral view, respectively; (41–45) UF 281490, lateral tooth in occlusal, lingual, labial, basal, and lateral view, respectively; (46–50) Type III: (46–48) UF 281255, SEM image of a female? lateral tooth in occlusal, lingual, and apico-labial view, respectively (49, 50) UF 281299, SEM image of a female? tooth in occlusal and lingual view, respectively (scale bars=1 mm).

Figure 12 Relative abundance of chondrichthyan genera from the Chucunaque Formation.

Figure 13 Two proxies for functional diversity. (1) Relative abundance of different dentition types as described by Kent (1994); (2) Relative abundance of different ecomorphotypes as described by Compagno (1990).

Table 4 Results of the weighted paleobathymetric analysis. Min and max values represent 95% confidence intervals. Previous estimates are based on Pimiento et al. (2013a) for the Gatun and Carrillo-Briceño et al. (2015a) for the Piña Sandstone facies of the Chagres Formation.